case study of echinococcosis

• Case report
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• Published: 08 June 2020

A young woman from an Echinococcus -endemic area with progressive abdominal distension: a case report

• Albrecht Boehlig 1 ,
• Valentin Blank 2 , 3 ,
• Thomas Karlas 2 ,
• Henning Trawinski 4 ,
• Hans-Michael Hau 5 ,
• Andri Arnosson Lederer 5 &
• Thomas Berg 1  

Journal of Medical Case Reports volume  14 , Article number:  65 ( 2020 ) Cite this article

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Cystic echinococcosis is a zoonotic infection caused by Echinococcus granulosus . This case report shows the difficulty in differential diagnosis in a patient with highly suspected hydatid disease.

Case presentation

A 29-year-old Chinese woman presented with progressive abdominal distension. Imaging results revealed a large multicystic tumor with typical features of hydatid disease. There was no clear relationship between the cystic tumor and the liver, which led to the assumption of primary extrahepatic cystic echinococcosis. After albendazole therapy was initiated, a laparotomy was performed and a huge ovarian cystadenoma was diagnosed.

Conclusions

This case highlights the possible challenges of differential diagnosis in patients with suspicion of hydatid cysts.

Peer Review reports

Hydatid disease is a zoonotic infection caused by cestode species from the genus Echinococcus . The cystic form of echinococcosis is caused by Echinococcus granulosus [ 1 ]. Both the cystic and the alveolar forms of echinococcosis are endemic in Western China, which has one of the highest prevalence rates of up to 6.8% [ 2 , 3 ]. The diagnosis relies mainly on imaging results. Therapeutic options range from percutaneous interventions, surgery, and antihelminthic therapy to “watch and wait” strategies. Although echinococcosis is a preventable and treatable disease, echinococcosis continues to be a major public health problem in many countries [ 4 ]. This case report aims to demonstrate the case of a patient from an Echinococcus -endemic area with highly suspected hydatid disease and an unexpected outcome with a challenging differential diagnosis.

In May 2019, a 29-year-old Chinese woman presented to her physician because of progressive abdominal pressure and loss of appetite over the last 3 months. She complained of lack of strength and could only eat a small portion of meals because her abdomen felt increasingly distended. No fever or enlarged lymph nodes were reported. In addition, her weight increased by 3 kg in the last 9 months despite reduced food intake. Her past medical history was unremarkable. Her heritage is the western part of China. At presentation, she had been living in Germany for 5 years and reported no trips abroad within the last 6 months. Her last visit to China was in 2016. She is currently a student at university.

A physical examination showed a slightly distended abdomen with pressure pain in the right upper quadrant and very scarce bowel sounds. Laboratory results revealed only slight elevation of aspartate aminotransferase (0.72 μkat/l; reference range 0.17–0.6); all other liver enzymes were within normal range. There were no pathologic levels of white blood cells (5.0 × 10 9 /l; reference range 3.5–9.8), lymphocytes (1.61 × 10 9 /l; reference range 1–2.9), eosinophils (0.09 × 10 9 /l; reference range 0–0.5), and neutrophils (2.92 × 10 9 /l; reference range 1.6–7.1) and liver function tests, such as bilirubin (10.5 μmol/l; reference range < 17.1), albumin (50.6 g/l; reference range 35–52) and international normalized ratio (1.0). Furthermore, there were no elevated inflammatory parameters (C-reactive protein 2.32 mg/l; reference range < 5) and normal values for tumor markers such as alpha-fetoprotein, carbohydrate antigen 19-9, and carcinoembryonic antigen.

An abdominal ultrasound revealed a huge polycystic formation with cyst-in-cyst configuration filling nearly her whole abdomen. The whole tumor-like mass was approximately 27 × 14 × 23 cm (see Fig.  1 a, b). Due to the abdominal mass, the liver parenchyma was displaced cranially to diaphragm and could only be investigated by a transcostal view. Therefore, the incomplete liver examination could neither prove nor exclude further liver cysts. There was no sharp delineation between the abdominal cystic formation and the liver parenchyma. Furthermore, there was no evidence of another originating organ association of the huge cystic mass. Relying on clinical and imaging results, the diagnosis of hydatid disease (infection by E. granulosus ) was suspected and staged as CE2, which refers to an active infection with many cyst-in-cyst lesions according to the World Health Organization (WHO) classification [ 4 ]. Consequently, we performed an Enzyme-linked Immunosorbent Assay (ELISA) test for Echinococcus species, which turned out to be negative. Due to the capsule isolation of the parasite from the host’s immune system, serology tests, such as indirect hemagglutination and ELISA, may be negative in approximately 20% of cases [ 5 ], especially in extrahepatic manifestations. In addition, false negative serology test results have been reported in our center in cases with immunosuppression [ 6 ].

a Abdominal ultrasound (panorama mode in sagittal plane) revealing the large cystic mass filling nearly the whole abdomen with a cranio-caudal diameter of approximately 27 cm. The main cystic tumor consists of many smaller cyst-in-cyst structures. b Ultrasound image with the typical cyst-in-cyst sign suspicious for diagnosis of hydatid disease in stage CE2. c, d Magnetic resonance imaging scan of the abdomen ( b , T1 sequence axial; c , T2 sequence coronal) showing the marked-off large cystic mass filling nearly the whole abdomen and displacing parenchymal organs and intestinal structures

Due to the highly suspected diagnosis of hydatid disease, we initiated an antihelminthic therapy with albendazole 2 × 400 mg per day prior to planned intervention to prevent spread of hydatid cysts in other organs. In particular, under consideration of the risk of cyst rupture and the increasing symptoms of our patient due to progressive compression, a further diagnostic workup was performed in June 2019 prior to the scheduled surgery. We refrained from doing a biopsy of the cysts in advance to confirm the diagnosis. Transvaginal and transabdominal gynecologic sonography revealed normal-sized ovaries, but the right ovarium was of limited visibility. A magnetic resonance imaging (MRI) scan which was performed to rule out cysto-biliary fistulas did not show a distinct relationship between the cystic tumor and the liver, which confirmed the ultrasound findings and led to the assumption of primary extrahepatic cystic echinococcosis (see Fig.  1 c, d). A preoperative chest X-ray showed no signs of pulmonary cysts.

In July 2019, a median laparotomy was performed and intraoperatively the cystic tumor appeared to derive from the right ovary. In consequence, a right adnexectomy was performed and multiple biopsies and cytological examinations from the peritoneum were done. The explanted cystic tumor turned out to be a multilocular mucinous cystadenoma weighing 6135 g originating from the right ovary. Histology revealed an intestinal subtype and the remaining ovarian tissue showed only slight fibrotic changes. The remaining left ovary showed no abnormalities and was kept in situ because of the childbearing age of our patient. As a consequence of the histologic result, we stopped albendazole therapy. A follow-up gynecological examination in the postoperative period showed no significant pathological findings. Eventually, she recovered well from surgery and was discharged on the seventh postoperative day. She was referred to her local gynecologist for regular follow-up visits. Retrospectively, this ovarian tumor was not suspected in the preoperative gynecological workup.

Discussion and conclusions

This case report highlighted an unexpected outcome of an ovarian cystadenoma in a patient with highly suspected hydatid disease.

Ovarian mucinous cystadenoma is the most common ovarian neoplasm responsible for 20% of all ovarian tumors. They are mostly benign in 80% of cases and are commonly asymptomatic at early stages. They origin from mucin-producing epithelial cells and their average diameter ranges from 15 to 30 cm [ 7 ]. Such ovarian tumors can grow to a very large size with heavy weight, which has been demonstrated in a case report from the early twentieth century showing a multicystic ovarian tumor with a weight of nearly 149 kg [ 8 ].

Typical organ manifestations of hydatid disease involve the liver (75%) and the lungs (15%). Less frequently, cysts can be situated in other abdominal organs and the abdominal cavity [ 9 , 10 , 11 ]. Primary peritoneal hydatidosis accounts for just 2% of all intra-abdominal hydatid diseases [ 12 ]. In such cases, the diagnostic workup can be challenging and may cause diagnostic delay. Involvement of the ovary is seen very rarely and can be secondary due to peritoneal spread of daughter cysts after rupture of a liver hydatid cyst [ 13 ]. In particular, in cases with a history of Echinococcus exposure in endemic areas, imaging findings may be misleading. Our case clearly illustrates that even a cyst-in-cyst configuration, which is a very typical sign of active Echinococcus infection [ 4 ], may also derive from ovarian lesions, especially from cystadenoma or cystadenocarcinoma. In particular, in women of reproductive age, hydatid cysts may be unilocular and can mimic ovarian cystadenoma [ 13 ]. Therefore, a careful consideration of imaging findings is required and a biopsy should be considered in unclear cases.

In conclusion, imaging features have a low specificity in the diagnosis of hydatid disease and cystic ovarian cystadenoma may represent one of the less well-described potential differential diagnoses, especially in cases with exclusive extrahepatic manifestations.

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Acknowledgements

The authors acknowledge support from the German Research Foundation (DFG) and Universitaet Leipzig within the program of Open Access Publishing.

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Albrecht Boehlig & Thomas Berg

Clinic of Gastroenterology, Hepatology, Infectious Diseases and Pneumology, University Hospital Leipzig, Leipzig, Germany

Valentin Blank & Thomas Karlas

Integrated Research and Treatment Center AdiposityDiseases Leipzig, Faculty of Medicine, University of Leipzig, Leipzig, Germany

Valentin Blank

Division of Infectiology and Tropical Medicine, Clinic of Gastroenterology, Hepatology, Infectious Diseases and Pneumology, University Hospital Leipzig, Leipzig, Germany

Henning Trawinski

Divison of Hepatobiliary and Transplant Surgery, Department of Visceral, Transplant, Thorax and Vascular Surgery, University Hospital Leipzig, Leipzig, Germany

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AB wrote the manuscript. VB created the final Fig. 1. All authors read and approved the final manuscript.

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Correspondence to Albrecht Boehlig or Thomas Berg .

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Boehlig, A., Blank, V., Karlas, T. et al. A young woman from an Echinococcus -endemic area with progressive abdominal distension: a case report. J Med Case Reports 14 , 65 (2020). https://doi.org/10.1186/s13256-020-02388-8

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DOI : https://doi.org/10.1186/s13256-020-02388-8

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• Cystic tumor
• Echinococcus granulosus
• Hydatid disease
• Ovarian cystadenoma

Journal of Medical Case Reports

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CASE REPORT article

Case report: diagnosis of human alveolar echinococcosis via next-generation sequencing analysis.

• 1 Department of Neurology, The Second Medical Center, Chinese PLA General Hospital, Beijing, China
• 2 Department of Neurology, The First Medical Center, Chinese PLA General Hospital, Beijing, China
• 3 Department of Neurology, Beijing Children's Hospital, Capital Medical University, National Center for Children's Health, Beijing, China

Introduction: Alveolar echinococcosis (AE) is a rare parasitic disease caused by the infection of Echinococcus multilocularis . AE may mimic malignancy both in clinical presentation and radiological imaging, which is often misdiagnosed as metastatic tumor. Recently, next-generation sequencing (NGS) technologies are increasingly being used to address a diverse range of biological questions. Here, we describe a rare case of alveolar echinococcosis diagnosed by pan-pathogen screening, using next-generation sequencing. To the best of our knowledge, this is the first reported case of AE which was definitely diagnosed relying NGS of cerebrospinal fluid (CSF).

Case Presentation: A 33-year-old man presented with repeat seizure and progressive headache for six months. Head magnetic resonance imaging (MRI) showed multiple masses with edema. Lung and abdominal computer tomography (CT) revealed multiple masses in bilateral lung, liver and the right adrenal gland. Bacterial, tuberculosis and fungal infection were excluded by CSF examination. Repeated target biopsy on the masses in the lung and liver showed as fibrous connective tissue without positive findings. NGS of CSF was performed and detected nucleic acid sequences of E. multilocularis . Consequently, the patient has accepted 1-year albendazole therapy. His case was followed up through imaging procedures.

Conclusion: The next-generation sequencing of CSF is a reliable and sensitive diagnostic method for the detection of pathogenic microorganisms, and may allow the accurate diagnosis of alveolar echinococcosis. In view of this case, we recommend NGS as a potential tool for diagnosis of cerebral AE, especially if repeated biopsies are negative.

Introduction

Brain alveolar echinococcosis is a fatal parasitic disease caused by Echinococcus multilocularis ( Deplazes et al., 2017 ), which is often misdiagnosed as metastatic tumor or intracranial tuberculosis. Diagnosis of AE relies on clinical presentation, imaging examinations, serological test and biopsy if available. However, metastatic tumors and AE are difficult to differentiate through imaging examinations. In addition, serological test sometimes results in biologically false-positive results. Herein, we present a rare case of cerebral AE which was finally confirmed by NGS. This is the first reported case which is conclusively diagnosed as cerebral AE by NGS of CSF.

Case Presentation

A 33-year-old man presented repeat seizures and progressive headache for six months. A complete blood count (CBC) showed: hemoglobin 123g/L, white blood cell count 7.73 × 10 9 /L, and percentage of eosinophil 0.009. Liver function showed: alanine transaminase (ALT) 92.8 U/L, aspartate aminotransferase (AST) 44.9U/L, alkaline phosphatase (ALP) 135.1U/L, γ-glutamyl transferase (γ-GT) 313.4 U/L, total bilirubin (TBil) 22.7 mmol/L, direct bilirubin (DBil) 19.4 mmol/L. Head MRI ( Figure 1 ) showed multiple masses with edema. Lung and abdominal CT ( Figure 2 ) presented with several lesions in bilateral lungs, liver and right adrenal gland. Bacterial, tuberculosis and fungal infection were excluded by CSF examination. Serological evaluation of multiple parasite antigen by ELISA were applied. Cysticercosis Immunoglobulin G (IgG) and liver hydatid IgG antibody were both positive. Repeated target biopsy on the masses in the lung and liver showed fibrous connective tissue without positive findings. In addition, we performed positron emission tomography with fluorodeoxyglucose integrated with CT ( 18 F-FDG PET/CT) that showed uptake in all masses with a maximum standardized uptake value of 7.2. Accordingly, it was still hard to draw a definitive pathogenic diagnosis. Therefore, the next-generation sequencing of CSF was performed. The CSF was collected according to standard procedures, and DNA was extracted directly from the sample with TIANamp Micro DNA Kit. The extracted DNA was sonicated to a size of 200–300 bp (Bioruptor Pico protocols). The DNA libraries were constructed and sequencing using the BGISEQ-100 platform. After removing human sequences, the remaining sequencing data were aligned to the microbial databases and detected 161 nucleic acid sequences of E. multilocularis ( Table 1 , E. multilocularis sequences which detected were provided as Supplementary Material ). On this basis, the patient was diagnosed as having AE. Consequently, the patient was recommended a 1-year albendazole therapy. During 1 year of follow-up, symptoms and neurological signs were not aggravated, with decreased seizure frequency. Follow-up CT after 1 year of albendazole treatment revealed slightly decreased multiple lesions and partly relieved surrounding edema in brain. The lesion in the liver (red arrow) was evidently diminished and calcification was slightly increased. The thickened right adrenal gland (yellow arrow) has obviously decreased in size ( Figure 3 ).

Figure 1 . Brain MRI images of the patient. Multiple lesions revealed with isointensity on T1WI (A,B) , hypointensity on T2WI (C,D) surrounded by edema, hypointensity on DWI (E,F) and irregular ring enhancement after injection of Gd-DTPA (G,H) .

Figure 2 . Lung and abdominal CT images of the patient. Multiple Lesions were found in bilateral lung (A,B) and the liver (C) . The right adrenal gland (yellow arrow) was obviously thickened (D) .

Table 1 . List of parasites detected.

Figure 3 . Follow-up CT images of the patient after 1-year albendazole therapy. Brain CT images revealed multiple lesions has slightly shrink and surrounding edema was slightly relieved (A–C) . Abdominal CT images showed that the lesion in liver was obviously diminished accompanied with calcification (D,E) .

Discussion and Conclusions

We reported a special human alveolar echinococcosis case involving the brain, lung, liver, adrenal gland, which was confirmed by NGS. AE is endemic in certain parts of the world, especially in Europe, Northern America, and Central Asia ( Deplazes et al., 2017 ). A recent meta-analysis indicated that the pooled prevalence of AE in China was 0.96% ( Wang et al., 2020 ). In China, the AE endemic area is restricted to the northwest region ( Qian et al., 2017 ), for example, Qinghai province and Gansu province. In most cases, AE is initially located in the liver and spreads into other organs by infiltration or metastasis formation. Extrahepatic lesions are usually located in the lung and brain ( Tappe et al., 2008 ). Adrenal AE, however, is rare, with only 9 cases reported in the literature so far ( Huang and Zheng, 2013 ; Spahn et al., 2016 ; Seidel et al., 2017 ). Our case suggests that AE may involve all parts of the body. We should suspect the diagnosis of AE in a patient with exposure history of parasite and a mass in the adrenal gland.

The diagnosis of AE is complicated by diverse clinical features and mimicking of differential diagnoses. For this case, the patient's biopsy results were negative. Therefore, a biopsy is likely to have lower sensitivity for the diagnosis of AE due to limited tissue specimens. Imaging findings of multiple lesions are helpful in differential diagnosis; however, it can be misinterpreted as other metastatic tumors even by experienced radiologists due to their limited awareness of this condition. Another difficulty in the differential diagnosis of AE and cysticercosis is that serologic test revealed that both of cysticercosis IgG and liver hydatid IgG were all positive. Is it a co-infection or immunological cross-reaction? We prefer immunological cross-reaction since there are common antigens between Cysticercus cellulosae and E. multilocularis . While mixed infection of 2 pathogens is extremely rare. Furthermore, NGS detected nucleic acid sequences of E. multilocularis without sequences of C. cellulose , which conclusively exclude cysticercosis.

Finally, AE diagnosis has been confirmed by NGS for this patient. NGS technologies are increasingly being used to address a diverse range of biological and epidemiological questions since NGS provides pathogen identification without prior target knowledge. In addition, other genetic diagnostic methods, such as PCR, is not applicable for screening of rare and unknown pathogens. We believe that this is the first reported case of AE which was definitely diagnosed relying next-generation sequencing of CSF. Clinicians should promptly recognize that NGS of CSF might be provided as a potential test for detecting cerebral AE.

The limitation of this study includes small sample size. Therefore, if there are similar cases in the future, we should expand the sample size and validate the accuracy of NGS method. In conclusion, the NGS of CSF is a reliable and sensitive diagnostic method to detect pathogenic microorganisms, which may allow accurate diagnoses of cerebral AE.

Data Availability Statement

The original contributions presented in the study are included in the article/ Supplementary Material , further inquiries can be directed to the corresponding author/s.

Ethics Statement

The studies involving human participants were reviewed and approved by This work was supported by National Natural Science Foundation of China (No. 81601086, 81771358). The patients/participants provided their written informed consent to participate in this study. Written informed consent was obtained from the individual(s) for the publication of any potentially identifiable images or data included in this article.

Author Contributions

All co-authors have seen and agree with the contents of the manuscript, that the ICMJE requirements for authorship have been met, and that each author believes that the manuscript represents honest work. All authors contributed to the article and approved the submitted version.

This work was supported by National Natural Science Foundation of China (Grant No.81601086, 81771358).

Conflict of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Acknowledgments

We would like to thank the patient and his family who are the focus of this report.

Supplementary Material

The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fgene.2021.666225/full#supplementary-material

Deplazes, P., Rinaldi, L., Rojas, C., Torgerson, P. R., and Jenkins, E. J. (2017). Global distribution of alveolar and cystic echinococcosis. Adv. Parasitol . 95, 315–493. doi: 10.1016/bs.apar.2016.11.001

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Seidel, A. K., Pless, M., Michel, C., Soll, C., Hochuli, C., and Gubler, J. (2017). A rare differential diagnosis of an adrenal mass: a case report. Case Rep. Oncol. 10, 981–986. doi: 10.1159/000481501

Spahn, S., Helmchen, B., and Zingg, U. (2016). Alveolar echinococcosis of the right adrenal gland: a case report and review of the literature. J. Med. Case Rep. 10:325. doi: 10.1186/s13256-016-1115-0

Tappe, D., Weise, D., Ziegler, U., Müller, A., Müllges, W., and Stich, A. (2008). Brain and lung metastasis of alveolar echinococcosis in a refugee from a hyperendemic area. J. Med. Microbiol. 57(Pt 11), 1420–1423. doi: 10.1099/jmm.0.2008/002816-0

Wang, X., Dai, G., Li, M., Jia, W., Guo, Z., and Lu, J. (2020). Prevalence of human alveolar echinococcosis in China: a systematic review and meta-analysis. BMC Public Health 20:1105. doi: 10.1186/s12889-020-08989-8

Keywords: alveolar echinococcosis, next-generation sequencing, adrenal gland, Echinococcus multilocularis , diagnose

Citation: Li K, Ma Y, Ban R and Shi Q (2021) Case Report: Diagnosis of Human Alveolar Echinococcosis via Next-Generation Sequencing Analysis. Front. Genet. 12:666225. doi: 10.3389/fgene.2021.666225

Received: 09 February 2021; Accepted: 16 June 2021; Published: 09 July 2021.

Reviewed by:

Copyright © 2021 Li, Ma, Ban and Shi. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY) . The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Qiang Shi, shiq301@163.com

Disclaimer: All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.

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Twenty-six years of involvement with cystic echinococcosis: a case report

Hosein safari.

1 Department of Neurosurgery, Golestan Hospital–Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Khuzestan Iran

Somayeh Mirzavand

2 Department of Parasitology, School of Medicine, Ahvaz Jundishapur University of Medical Sciences, P.O. Box 61357–15794, Ahvaz, Khuzestan Iran

Abdollah Rafiei

3 Infectious and Tropical Diseases Research Center, Health Research Institute, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Khuzestan Iran

Molouk Beiromvand

Associated data.

All data generated or analyzed during this study are included in the article.

Introduction

Spinal hydatidosis, a zoonotic disease caused by infection with Echinococcus spp. larvae, is rare, but its treatment remains a significant medical challenge. Approximately 70% of patients with spinal hydatidosis have lesions in their liver, 0–15% have lung involvement, and only 0.5–2% have bone involvement.

Case presentation

Here we report a 38-year-old Iranian man with spinal hydatidosis, who had a history of eight times surgery in over of 26 years due to hydatid cyst in the liver, lungs, and chest wall. At the most recent admission to hospital he presented with chest pain, paraplegia, and urinary incontinence. Magnetic resonance imaging revealed thoracic spinal hydatid disease. He underwent surgery, and the hydatid cysts were completely removed. Lower extremity forces recovered dramatically and completely within 4 weeks.

Spinal hydatidosis is a rare disease, but it is associated with a high degree of morbidity, mortality, and poor prognosis. Because of the infiltrative nature of hydatid disease, surgery alone is rarely curative. The current case study demonstrates the importance of a suitable surgical approach, adequate intraoperative prophylaxis to prevent cyst rupture, and prolonged complete paraplegia.

Human cystic echinococcosis (CE), caused by the larval form of Echinococcus granulosus sensu stricto is a parasitic zoonotic disease which mainly occurs in pastoral areas worldwide [ 1 – 3 ]. Lesions are localized to the liver in approximately 70% of patients with CE and to the lungs in approximately 20%; other cases show the involvement of other organs [ 1 ]. Bone involvement is seen in 0.5−2% of hydatid cases, with most of these cases involving hydatid cysts in the spine.

A 38-year-old Iranian man, residing in a rural area, was admitted to our surgery unit with a history of back pain, chest pain, paraplegia and urinary incontinence within the last 45 days. The patient had a history of hydatid cyst(s) in the liver, lungs, and chest wall. The first surgery occurred 26 years previously when he was 12 years old and underwent thoracotomy for two hydatid cysts in the left lung. Subsequently, in April 1999, the patient was diagnosed with a hydatid cyst in his left lung and underwent surgery again. Nine years later, after confirmation of a hydatid cyst in his left lung, he underwent thoracotomy. In May 2011, computerized tomography (CT) revealed multiple cysts located behind the left lung and the fourth rib (R4), leading to the diagnosis of paraspinal hydatidosis and a second thoracotomy. In May 2014, his imaging results demonstrated the presence of four hydatid cysts in the left hemithorax. Total cystectomy was performed for one cyst under the latissimus dorsi, and two cysts behind the third rib (R3) and one cyst behind his left clavicle were drained. In the same year, one hydatid cyst was detected in his liver, and hepatic resection was performed. In March 2018, imaging results demonstrated the presence of multiple cystic lesions under R3, R3 and the fifth rib (R5). Thoracotomy was once again performed, and the cystic lesions and the necks of R3, R4, and R5 were removed. After surgery, albendazole therapy (400 mg/kg) was initiated and continued.

In December 2019 the patient was referred to our surgery unit with progressive weakness. Spinal magnetic resonance imaging (MRI) showed multiple spinal epidural cystic lesions at the level of the third to fourth thoracic vertebrae (T3–T4) (Figs. ​ (Figs.1, 1 , ​ ,2) 2 ) and that the pedicles on both sides of T4, some parts of the lamina, and the vertebral body were destroyed. The patient underwent surgical resection with the costotransverse approach, and multiple epidural cystic lesions at the T3–T4 level were completely removed. Multiple extradural cystic lesions were carefully excised to avoid intraoperative rupture of the cysts. Intraoperatively, irrigation with hypertonic saline (as scolicidal agents) and cotton pads soaked with hypertonic saline were used. Since the T3 and T4 pedicles had been destroyed, posterior fusion with pedicular screw was performed. The diagnosis of hydatid cyst was confirmed by pathological examination, following which treatment with 400 mg/kg albendazole was started, with the recommendation that the treatment continue for 6 months. Within 2 weeks after surgery, his lower extremity forces dramatically returned and he was full force after 4 weeks.

a Sagittal magnetic resonance imaging image at the level of the second thoracic vertebra of the patient, showing a lesion consisting of multiple cysts (white arrow) in the thoracic spinal cord. b Two-dimensional myelogram image showing a multiple cystic lesion (white arrow)

a Intraoperative photos of the patient. b Multiple grape-like daughter cysts, which were completely removed by surgical resection with the costotransverse approach

Discussion and conclusions

Spinal hydatidosis is a rare form of hydatidosis and affects fewer than 1% of all patients with hydatidosis. Approximately one half of all patients with hydatidosis of bone have spinal hydatidosis; the other 50% have hydatidosis in the thoracic region. Previous studies have demonstrated that approximately 85% and 25–77% of patients suffered from back pain and paraplegia, respectively [ 4 ]. In our case, the lesion was extradural and located in the thoracic region (T3–T4), with paraspinal extension, and the patient had a history of back pain, chest pain, urinary incontinence, and paraplegia.

Surgical treatment with removal of the whole cyst(s) is the gold standard treatment in spinal hydatidosis [ 5 ]. Several factors, such as location of the cyst, familiarity with the surgical approach, and surgeon preference, are involved in the choice of surgical procedures [ 6 ]. Moreover, choosing the suitable surgical technique depends on an accurate diagnosis of the hydatid cysts in order to prevent intraoperative cyst spillage. Surgery in thoracic cases is mainly posterior [ 4 ]. During the surgery, most surgeons use scolicidal agents, such as hypertonic saline, 0.5% silver nitrate, chlorhexidine, and/or 80% ethanol to prevent rupture of hydatid cysts. Among these, 3% hypertonic saline is the most frequently used scolicidal agent [ 4 ].

Primary hydatid cysts usually contain daughter cysts, and the rupture of these daughter cysts can lead to secondary cysts [ 7 ]. The risk of release of the daughter cysts increases with bone involvement. Although it was not easy to distinguish primary or secondary cysts in the present case, the patient’s history suggests the possibility of secondary cysts. Despite a history of 1-month complete paraplegia, a dramatic neurologic recovery was observed, and thepatient fully recovered within 4 weeks. This finding suggests the slow growth nature of the lesion.

Because of the invasive nature of hydatid disease, surgery alone is rarely curative. Therefore, a correct preoperative diagnosis, choosing the suitable surgical technique, considering the infiltrative nature of the cyst, intraoperative prophylaxis to reduce spillage, and posterior surgical approach for treatment are of crucial importance in preventing recurrence.

Acknowledgements

Abbreviations, authors' contributions.

HS is the patient’s chief surgeon and he operated on the patient. MB, HS, AR, and SM wrote the manuscript. All authors read and approved the final manuscript.

Not applicable.

Availability of data and materials

Ethics approval and consent to participate, consent for publication.

Written informed consent was obtained from the patient for publication of this case report and any accompanying images. A copy of the written consent is available for review by the Editor-in-Chief of this journal.

Competing interests

The authors declare that they have no conflict of interest.

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• Open access
• Published: 10 December 2022

How climate, landscape, and economic changes increase the exposure of Echinococcus Spp.

• Xiaoyu Di 1 , 2   na1 ,
• Shuo Li 1 , 2   na1 ,
• Bin Ma 1 , 2 ,
• Xiaofan Di 1 , 2 ,
• Yuhao Li 1 ,
• Bei An 1 &
• Wenwen Jiang 3  

BMC Public Health volume  22 , Article number:  2315 ( 2022 ) Cite this article

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Metrics details

Echinococcosis is a global enzootic disease influenced by different biological and environmental factors and causes a heavy financial burden on sick families and governments. Currently, government subsidies for the treatment of patients with echinococcosis are only a fixed number despite patients’ finical income or cost of treatment, and health authorities are demanded to supply an annual summary of only endemic data. The risk to people in urban areas or non-endemic is increasing with climate, landscape, and lifestyle changes.

We conducted retrospective descriptive research on inpatients with human echinococcosis (HE) in Lanzhou hospitals and analyzed the healthcare expenditure on inpatient treatment and examined the financial inequalities relating to different levels of gross domestic product. The livestock losses were also estimated by infection ratio. The occurrence records of Echinococcus spp. composed of hospitalized patients and dogs infected in the Gansu province were collected for Ecological niche modeling (ENM) to estimate the current suitable spatial distribution for the parasite in Gansu province. Then, we imported the resulting current niche model into future global Shared Socioeconomic Pathways scenarios for estimation of future suitable habitat areas.

Between 2000 to 2020, 625 hospitalized HE patients (51% men and 49% women) were identified, and 48.32 ± 15.62 years old. The average cost of hospitalization expenses per case of HE in Gansu Province was ￥24,370.2 with an increasing trend during the study period and was negative with different counties’ corresponding gross domestic product (GDP). The trend of livestock losses was similar to the average cost of hospitalization expenses from 2015 to 2017. The three factors with the strongest correlation to echinococcosis infection probability were (1) global land cover (GLC, 56.6%), (2) annual precipitation (Bio12, 21.2%), and (3) mean temperature of the Wettest Quarter (Bio12, 8.5% of variations). We obtained a robust model that provides detail on the distribution of suitable areas for Echinococcus spp. including areas that have not been reported for the parasite. An increasing tendency was observed in the highly suitable areas of Echinococcus spp. indicating that environmental changes would affect the distributions.

This study may help in the development of policies for at-risk populations in geographically defined areas and monitor improvements in HE control strategies by allowing targeted allocation of resources, including spatial analyses of expenditure and the identification of non-endemic areas or risk for these parasites, and a better comprehension of the role of the environment in clarifying the transmission dynamics of Echinococcus spp. Raising healthcare workers’ and travelers’ disease awareness and preventive health habits is an urgent agenda. Due to unpredictable future land cover types, prediction of the future with only climatic variables involved needs to be treated cautiously.

Peer Review reports

Echinococcosis is a chronic parasitic infection of humans, domestic animals, and wildlife as a neglected parasitic disease [ 1 ], which gives precedent support for its elimination and control [ 2 ]. Treatment of human echinococcosis requires significant expenditure for the families of patients and countries [ 3 ]. Echinococcosis is usually expensive and causes a heavy financial burden on sick families [ 4 ]. Above 90% of the global burden of alveolar echinococcosis (AE) [ 5 ] and 34% of cystic echinococcosis (CE) are in China [ 6 ]. Currently, treatments in public hospitals in China are financed through three sources: government subsidies, patient fees, and drug markups. As poverty and infectious diseases reinforce each other, the Chinese government has committed to fighting and eliminating poverty-impoverished areas and has promoted health literacy for echinococcosis according to Healthy China 2030 [ 7 ]. The prevalence of human echinococcosis (HE) was positively related to the ethic ratio but negatively related to the Gross Domestic Product (GDP) [ 8 ]. Due to the high disease burden still shown in spite of national programme, appropriate policies and actions are demanded [ 3 ]. Echinococcosis is mostly distributed in endemic pastoral and semi-pastoral and poverty-stricken counties but few in non-endemic areas [ 6 ]. Health authorities are demanded to supply only an annual summary of endemic data. However, the risk to people non-endemic is increasing with climate, landscape, and lifestyle changes [ 4 ]. In the meantime, most endemic counties of echinococcosis are well-known tourist areas that receive thousands of visitors (local and outside) involved in ecotourism [ 9 ]. With ecotourism blooming [ 9 ], travelers are increasingly exposed to CE and AE by accidentally ingesting Echinococcus eggs in contaminated food, water, or soil [ 10 ].

Echinococcosis occurrence is highly dependent climatic factors including temperature and humidity [ 11 , 12 , 13 ] due to their influences on the survival of eggs and environment factors such as landscape factors (land use, grassland area ratio, vegetation coverage, land cover changes) [ 8 ]. Domestic dogs are the most important definitive host of both E. granulosus and E. multilocularis with the highest risk of transmitting CE and AE to humans due to their ability to wander freely in pastoral areas and prey on slaughtered live-stock. Landscape of the world has been altered, and novel environments have infiltrated [ 7 , 10 ]. Due to anthropogenic land use, lifestyle changes, and even microclimate changes, afforestation [ 14 ], particularly farming and fencing practices are linked to the distribution and dynamics of Echinococcus spp. intermediate hosts [ 15 ]. Hence, study demands to be applied to better understand the ecological processes that may result in variations in the transmission patterns of Echinococcus spp. based on shifting environmental factors [ 16 ].

Environmental niche models (ENMs) are powerful tools that can enhance the insight of the potential and actual distribution of species in question, as well as the way in which environmental factors may influence a species [ 17 ]. Furthermore, these models can be applied to forecast the influences of motivations of global environmental change, such as climatic or landcover alterations on the distribution of parasites [ 16 , 18 ]. Hence, integrating information about pure and projected environmental variations might allow us to prioritize inspecting activities to exploit the possibility of expecting the advent of pathogens, specifical mediators of endemic, emergent, and re-emergent zoonotic diseases in novel areas [ 18 ] .

Gansu Province is a co-endemic AE and CE areas with various environmental conditions belonging to the most impoverished region in China [ 19 ]. The temperature and precipitation in Gansu Province decrease from southeast to northwest, and the Hexi areas show an upward trend in annual precipitation [ 20 ]. There were 56 out of 368 Chinese endemic echinococcosis counties but uneven distributed in 81 counties and districts in Gansu Province [ 21 ]. Consequently, most investigations currently focus on endemic echinococcosis counties [ 21 , 22 ]. However, some HE cases have been reported in Lanzhou City [ 23 , 24 ]. Hence, it is very key to increase urban citizens and tourists’ awareness of risky practices that transmit the disease [ 25 ]. To our knowledge, no scientific studies have been conducted to analyze the health care expenditure on inpatient treatment and examined the financial inequalities relating to different levels of gross domestic product, determine their impacts [ 26 ] of climate and environmental changes on the shift in the distributional range of Echinococcus spp. in Gansu Province.

Here, we modeled the spatiotemporal dynamic distribution of Echinococcus spp. in Gansu Province from 2000 to 2020 by collecting echinococcosis scientific literature and hospital records, specifically quantifying impatient case characteristics. We aimed to address the following research questions: (1) describe patients’ characteristics related to echinococcosis at a province level to get a better picture of the current epidemiological scenario after the implementation of regional control programs, (2) estimate dynamics of Echinococcus spp. impact in terms of monetary losses including animal production losses and hospitalization expenditure in Gansu Province, (3) estimate the current spatial distribution of suitable conditions for the Echinococcus spp. in Gansu Province, (4) evaluate the potential influence of climatic change on the distribution of suitable conditions Echinococcus spp in the future (2070).

Gansu Province (32°110′N-42°570′N, 92°130′E-108°460′E) is situated at the intersection of the monsoon region in eastern China and the semiarid region in northwestern China (Fig.  1 including 81 counties and districts), bordering six endemic echinococcosis provinces [ 21 ].

The geographical location of Gansu Province, China (Available online for the map layer of Altitude and Remote Sensing Image: www. Gscloud.cn/). numbers indicate different counties or districts (See Additional file  1 supple Excel A1). Note Map was created with ArcMap from ArcGIS 10.8 by our team

Collection of clinical information and livestock losses

We conducted a retrospective descriptive study of HE cases between 2000 to 2020 from three hospitals in Lanzhou. Sociodemographic (sex, age, and county of residency) and clinical characteristics (length of hospitalization, noninvasive procedures and history of surgical intervention during hospitalization, and hospitalization cost to the health care system, and financing regime) were collected. The length of hospitalization was calculated by applying the admission and discharge dates for each case. This research estimated the economic losses for 523 patients who underwent surgery or non-surgery and 103 patients were removed due to lack of hospital expenditure information. The cost involved hospitalization only covered medical fees (e.g., drugs, diagnosis-related exams, and surgery). We also conducted a retrospective descriptive study of livestock infected ratio to estimate animal productivity losses.

Sampling collections and other occurrence data from public databases

To collect a database on the Echinococcus spp. sampling and detection localities, we carried out a systematic search in the Web of Science and China National Knowledge Infrastructure (CNKI) using the search terms “ Echinococcus ” or “ echinococcosis ” and “Gansu”, Distributions of dog and HE were collected through a literature review and national reports. Hence, the occurrence records of Echinococcus spp. composed of hospitalized patients and dogs infected in the Gansu province were collected for Ecological niche modeling (ENM) to estimate the current suitable spatial distribution for the parasite in Gansu province. When the available data lacked geographic coordinates, Google Earth 7.3.3 ( https://about.google/ ) was applied to obtain the approximate longitude and latitude based on the depicted geographic sites. Species occurrence data were organized into “.csv” format files following workflow (Additional file  2 supple Excel A2). A 1:1 million scale vector map of China’s administrative divisions, provided by the national basic geographic information system ( http://bzdt.ch.mnr.gov.cn/index.jsp ), was applied as the base map for analysis, and a sighting point map was generated by ArcGIS version 10.8 ( http://www.esri.com/arcgis ) (Fig. 1 ).

Species distribution modeling

Environmental variables are crucial components influencing species distribution. Nineteen bioclimatic variables have been demonstrated to be the key variables for modeling potential species distributions [ 13 ]. Moreover, landscape features and socio-ecological changes such as forest protection and the reforestation of some areas are important environmental factors affecting human disease distribution [ 10 , 11 , 14 ]. Thus, four types of environmental variables that affect the distribution of Echinococcus spp. are recognized in this study: (1) climate variables, 19 bioclimatic factors from the WorldClim database [ 27 ], with a resolution of 30″, (2) topographic variables, including altitude, slope, and aspect, downloaded from the Geospatial Data Cloud Platform of the Computer Network Information Center of the Chinese Academy of Sciences ( http://www.gscloud.cn/ ), (3) Vegetation variables, including vegetation coverage, land use type, and normalized vegetation index are obtained based on remote sensing interpretation data. The normalized difference vegetation index (NDVI) comes from the Chinese Academy of Sciences Geographical Sciences and Resource and Environmental Data Cloud Platform of the Resource Research Institute ( http://www.resdc.cn/ ). (4) Water source variables, including the distance to the river and the distance to the lake, use the vector data of rivers and lakes in the ArcGIS software generated by the distance function. A pair of variables with Pearson’s correlation > |0.80| was removed and remained the most important factor for consideration in the final model according to permutation importance and ecological meaning. All remained variables were resampled in ArcGIS software, and the raster layer with a unified resolution of 1000 m is converted to ASCII format using the Asia North Albers Equal Area Conic projection coordinate system.

Future climate data (2070a) are downloaded ( http://worldclim.org/ ) based on the BCC-CSM2-MR climate system model developed by the National Climate Center [ 28 ]. The model includes four emission scenarios proposed by the sixth International Coupled Models Comparison Program (CMIP6). WorldClim provides four shared socio-economic pathways (SPPs) for each model, corresponding to four CO 2 emission scenarios. They are as follows: (1) SSP5–8.5: High obsessive-compulsive situation, Radial forcing stabilizes at 8.5 W.m 2 in 2100. (2) SSP3–7.0: Moderate to the high obsessive-compulsive situation. Radial forcing stabilizes at 7.0 W.m 2 in 2100. (3) SSP2–4.5 Moderate obsessive-compulsive situation: Radiative forcing stabilizes at 4.5 W.m 2 in 2100. (4) SSP1–2.6 In the low obsessive-compulsive situation, radiative forcing stabilizes at 2.6 W.m 2 in 2070 [ 29 ]. The Beijing Climate Center Climate System Model 2 Medium Resolution (BCC-CSM2-MR) of the National (Beijing) Climate Center Climate System Model and the Center National de Recherches Météorologiques (CNRM) and CNRM-CM6–1 jointly developed by the Center National de Recherches Météorologiques (CNRM) and the Cerfacs [ 30 ] were applied in this study.

MaxEnt software (Version 3.4.4, http://www.cs.princeton.edu/_schapire/maxent/ ) were applied to model the habitat suitability of Echinococcus spp. in Gansu Province (Additional file  3 supple Fig. A1). The algorithm does not require a comprehensive and systematic survey of the distribution of a certain species, but it can maximize the use of the limited biological survey data of certain species distribution in a certain area over the years [ 31 , 32 , 33 ]. For further analyses, the results of MaxEnt were imported into ArcGIS version 10.8, and five categories of potential future habitats were reclassified as follows: very high potential (> 0.8), high potential (0.6 ~ 0.8), good potential (0.4 ~ 0.6), moderate potential (0.2 ~ 0.4), and least potential (< 0.2) [ 34 ].

Model evaluation

The area under the curve (AUC) of receiver operating characteristics [ 35 ] was applied to weight model performance. An AUC value lower than 0.7 indicates poor prediction accuracy, 0.7 to 0.9 indicates medium prediction accuracy and higher than 0.9 indicates high prediction accuracy of the predicted output of the model. Using random seeds, we repeat 15 times to calculate the average result [ 36 ].

Data analysis

Microsoft Excel and SPSS 11.5 (version 19.0; SPSS Inc., Chicago, IL) were applied to compare the prevalence and analyzed the risk factors linked with the demographic information. P  < 0.05 was examined as statistically significant.

Clinical characteristics of echinococcosis in Gansu Province

A total of 626 hospitalized HE patients were identified between 2000 and 2020. Organ involvement in all hospitalizations was as follows: 89.14% (558 cases) in liver infection, 0.32% (2 cases) in lung infection, 8.14% (51 cases) in other organ infection, and 2% (12 cases) in multiple organ infection.

The mean age of the 626 HE patients (males: females = 1.04 (319 vs. 307)) was 48.32 ± 15.62 years (range 2–89), with the 40–60 age group being slightly more indicative (45.69%). Of the 626 hospitalizations, 430 (68.69%) registered a surgical intervention. The average hospitalization duration was 16.14 days. Among the surgical inpatients, 62% of HE cases remained in the hospital for 14 days, 23% of which were hospitalized for less than or equal to 10 days, with up to 4 months of hospital stay in complicated cases (ranging from 1 to 125 days).

In the statistics of ethnic distribution, Han nationality accounted for the largest proportion (80.19%), followed by Tibetan (9.58%) and Hui nationality (8.95%, Fig.  2 A). Among the 626 patients, 285 patients were employed as agriculture, forestry, animal husbandry, and fishery workers. Twenty-five of the patients were government officials and civil servants, including two centers for disease control and prevention (CDC) staff, and 27 patients were professional technicians including 4 leather factory workers. Seven patients were engaged in transportation (Fig. 2 B). Of 626 cases, 158 patients were from Lanzhou city (25.24%).

Ethnic ( A ) and occupational ( B ) distributions of 626 patients from 2000 to 2020 in Gansu Province, China

Spatial and temporal socio-economic cost and trends in Gansu Province

The hospitalization median cost was ￥24,370.20 (35.6–22,8622) (Table  1 ). Western medicine accounted for the largest proportion of the total expenses (33.91%), the cost of the surgery itself (18.66%), and other components of the total expenses (22.28%) (Table 1 ). The general hospitalization expenses of echinococcosis patients increased with an annual growth rate of 8.95% from 2000 to 2020 (Fig.  3 ). The trend of livestock losses was increased but the highest loss was in 2016 (Fig. 3 ), which is similar to average cost of HE hospital expenses (Fig. 3 ).

Annual average cost per hospitalization expenditure due to AE and CE from 2000 to 2020 and annual livestock losses due to CE from 2015 to 2017 in Gansu Province, China

The cost of treating a case of echinococcosis in different counties was significantly negative with their corresponding GDP (Fig.  4 A). Human cases are distributed in different poverty-stricken counties, and a higher hospitalization median cost occurs in the key poverty-stricken counties (Fig. 4 B) and 9 land types of Gansu province (Fig. 4 C).

Information of Gansu Province. A  Average expenditure per case in different Counties; B The occurrence records sites (see Additional file 1 supple Excel A1) in different poverty-stricken counties in Gansu Province (sizes of the red spots indicate the number of patients); C  case locations (red spots) in different land types in Gansu Province from 2000 to 2022. D  Results of the MaxEnt distribution model of Echinococcus spp. under different land types. Binary prediction of suitable environmental conditions using two different reclassification thresholds. The red distribution represents the suitable area using a threshold that equates of the threshold and original distributions. Numbers indicate different counties or districts (See Additional file  1 supple Excel A1). Note Map as created with ArcMap from ArcGIS 10.8. The land cover vector layers were acquired from the Department of Natural Resources in Gansu Province, China

Contributions of environmental variables

Variable response curves show how each environmental variable affected the MaxEnt prediction, indicating how the logistic prediction changes with the alteration of each environmental variable. Three types of lands, i.e., “cultivated lands” (code 80), “waterbodies” (code 60), and “artificial surfaces” (code 10), were highly associated with the presence of Echinococcus spp. (Additional file 5 supple Fig. A2a). To attempt to reduce the influence of correlated variables on the analysis, one variable from each pair with correlation coefficients above than 0.8 was deleted. Variables that have been presented to be more important or meaningful were remained in the analysis. Of the 9 variables (Table  2 ) applied for modeling, the significant factors influencing the spatial distribution of Echinococcus spp. were land cover types (56.6% of variations), annual precipitation (21.2% of variations), and mean temperature of the Wettest Quarter (8.5% of variations) of the total variation. The variables with high permutation importance were precipitation in the warmest quarter (22.7%) and land cover types (20.4%). The additional information shows in more detail the respective response curves of the variables utilized in the MaxEnt model (Additional file  5 supple Fig. A2).

Suitable distribution area under current conditions

By using the MaxEnt model, the model predicted the potential distribution of Echinococcus spp. in Gansu Province, with a training AUC value of 0.929 and a test AUC value of 0.888, which indicates its high level of predictive performance (Additional file 5 supple Fig. A2b).

Using the reclassification tool of ArcMap from ArcGIS 10.8, based on the maximum training sensitivity plus specificity logistic threshold in the MaxEnt result as the threshold, the logical output results generated using MaxEnt software are expressed in terms of probability and range between zero and one. Based on the presence data, the model gave the currently suitable habitats of Echinococcus spp. under current climate conditions and land cover types (Fig. 4 D). Linxia Hui Autonomous Prefecture (Code number 66–73 in Fig. 4 D), Gannan Tibetan Autonomous Prefecture (Code number 74–81 in Fig. 4 D), Dingxi City (Code number 50–56 in Fig. 4 D), Pingliang City (Code number 28–34 in Fig. 4 D), Qingyang City (Code number 42–49 in Fig. 4 D), Lanzhou City (Code number 1 in Code number Fig. 4 D), Baiyin City (Code number 8–11 in Fig. 4 D), Tianshui City (Code number 41–47 in Fig. 4 D) and Longnan City (Code number 32–40 in Fig. 4 D) were found to be suitable habitat areas for Echinococcus spp. in Gansu Province.

Future changes in potential species distribution

Under four emission scenarios, the MaxEnt model was applied to identify suitable habitat areas of Echinococcus spp. in Gansu Province. The relative changes in the future potential species distribution were estimated by the difference between current and future distribution maps, which revealed that the range expansion of Echinococcus spp. in Gansu Province was linked with the changing climate, socioeconomic and human behaviors (Fig.  5 ). Under the conditions of the four shared economic pathways (SSPs), the suitable distribution areas of Echinococcus spp. were expanded. The highly suitable area of Echinococcus spp. in Gansu Province changed to varying degrees, showing a significant increase in SSP5–8.5, while under the other three emission scenarios, the highly suitable area does not change significantly compared to that under current climate conditions. The highly suitable area of Echinococcus spp. increased significantly in the Linxia Hui Autonomous Prefecture (Code number 66–73 in Fig. 5 ) and Gannan Tibetan Autonomous Prefecture (Code number 74–81 in Fig. 5 ), with the most apparent increase under SSP5–8.5, and under the other three emission scenarios, the highly suitable area was not that significantly different. Among which has expanded the most obviously, Qingyang (Code number 42–49 in Fig. 5 ), Wuwei (Code number 18–21 in Fig. 5 ), and Jiuquan (Code number 35–41 in Fig. 5 ) have also expanded significantly. Zhangye (Code number 22–27 in Fig. 5 ), Jinchang (Code number 6–7 in Fig. 5 ), Lanzhou (Code number 1–4 in Fig. 5 ), Dingxi (Code number 50–56 in Fig. 5 ), Linxia (Code number 66–73 in Fig. 5 ), Tianshui (Code number 12–17 in Fig. 5 ), and Longnan (Code number 57–65 in Fig. 5 ) have not seen significant changes, but they are suitable habitats for Echinococcus spp. (Fig. 5 ).

Future predictions (the 2070s) of Echinococcus spp. based on RCP8.5 under the conditions of the four shared economic pathway A) BCC 1-2.6, B) BCC 2-4.5, C) BCC 3-7.0 and D) BCC 5-8.5. Numbers indicate different counties or districts (See Additional file 1 supple Excel A1)

To our knowledge, this is the first ecological niche model that has been fully developed and implemented for Echinococcus spp. in Gansu Province. The prevalence of Echinococcus spp. is not only a matter of ecological factors but also the result of the comprehensive effect of society, infrastructure, and human habitat changes in endemic or non-endemic areas [ 37 ]. Since 2005, the Chinese government has launched an echinococcosis control project for 217 counties in western China including Gansu Province [ 38 ]. Moreover, Gansu Province has become a new ecotourism hotspot, and tourists would expose to a high risk of endemic areas of Echinococcus spp. Raising travelers’ disease awareness and preventive health habits is an urgent agenda and is the most efficient-reaching action with a small investment.

Case characteristics among patients with hydatid

Among the 626 patients, 89.14% had liver infection alone, which is consistent with previous research [ 39 ]. The proportion of lung infection is lower than in Herrador’s research (3.3%) [ 37 ]. The ratio of males vs females was 1.04, which is line with previous human case research [ 23 , 26 ]. In this study, the prevalence of echinococcosis in the Han population was the highest (Fig. 2 B), which is line with human case research in Gansu Province [ 40 ] but inconsistent with the conclusion that the Tibetan population ratio was positively correlated with the prevalence of human CE [ 8 ]. This might be caused by different ethnic ratios in different research areas [ 40 ].

Most echinococcosis patients are engaged in agriculture and animal husbandry (46%, Fig. 2 A) in Gansu Province, which can be evidenced by previous research [ 25 ] but also health care workers involved. Hence, raising awareness of echinococcosis among health care workers [ 41 ] are urgent. Most cases are distributed in pastoral areas or mixed areas between pastoral areas and farms, but some research results show that the number of urban patients is increasing [ 2 , 13 ], which can support an increase in the urban infection ratio (158/626 in our case vs 10/211) from previous research [ 23 , 24 ]. The average length of hospital stay was 14 days, which is shorter than Chinese average hospital stays of 17.12 days in China [ 26 ].

The average cost of echinococcosis was ￥24,370.2, in Gansu Province, which is slightly higher than ￥ 21,201.85 [ 26 ]. The average cost of echinococcosis varied from year to year with an increasing trend (Fig. 3 ), which is consistent with the average hospitalization cost of Chinese patients with echinococcosis [ 26 ]. The rapid increasing of medical expenditures (Fig. 3 ), mostly caused by the frequent use of advanced medical technologies and over-prescription of drugs by health care providers [ 41 ]. We also found there were similar upward trend both livestock loss and average cost of HE hospital discharges (Fig. 3 ). It supports that Echinococcosis not only damages people’s health and life but also ruins the healthy growth of agriculture and animal husbandry economies [ 2 ]. They also shared the same highest cost and loss in 2016 (Fig. 3 ). They might be explained by their intermediate host of Echinococcus spp [ 2 ] . The average cost of echinococcosis differed significantly among regions (Fig. 4 A and B). The majority of echinococcosis patients live at a low-income level (< 4000￥/family/annum), and the number of patients is positively related to the level of poverty (Fig. 4 A and B), which indicates that a reduction in socio-economic disadvantage could contribute to risk of Echinococcosis [ 5 , 41 ], and causes a heavy financial burden on sick families [ 4 ]. Thus, the prerequisite for effective disease control measures and appropriate policies and actions are essential from an economic point of view [ 3 , 37 ]. It also could help to fulfill the Chinese government commission of eliminating poverty-impoverished areas [ 7 ].

Epidemic characteristics of Echinococcus spp. in Gansu Province

Based on the distribution of the infected dogs and patients collected, we found that cultivated lands, water bodies, and artificial surfaces were more suitable land types for Echinococcus spp. (Table 2 , Fig. 4 C), which supports that Echinococcus spp. distribution is related to land use and vegetation type [ 8 ]. Moreover, the Chinese government has restored the degraded ecological landscape to forestation [ 41 ]. Afforestation [ 15 ], and particular farming and fencing practices have been demonstrated to change the distribution of various species of Echinococcus spp. hosts. Landscape features and climate factors can predict human disease hotspots [ 11 , 13 ]. Areas of artificial surfaces in Gansu Province during the last 2 decades have increased rapidly due to socio-economic development [ 32 ] since Gansu Province has restored arable land to nature. Future suitable areas of Echinococcus spp. are expanding under four scenarios (Fig. 5 ), which can be explained by predicted land cover in 2030 under the ecological protection scenario being more favorable [ 32 ].

Gannan Tibetan Autonomous Prefecture in southeast has a humid climate, low winter temperatures, and widely distributed livestock areas in Gansu Province [ 21 ], which keep it the most suitable habitats for Echinococcus spp. Suitable habitats of Echinococcus spp. is prominent toward the northwest in the 2070s (Fig. 5 A-D). This might be caused by the Hexi areas showing an increasing annual rainy day and its potential epidemic risk [ 20 ]. Some areas possess a suitable environment for echinococcosis, but have been rarely reported, such as Longnan (Code number 57–65 in Fig. 4 D), Tianshui (Code number 12–17 in Fig. 4 D), Pingliang (Code number 28–34 in Fig. 4 D), and Zhangye (Code number 22–27 in Fig. 4 D). Identification of these areas may help in the development of policies for at-risk populations in geographically defined areas.

Limitations to this study

There are several limitations to our study including the lack of future land cover types involved, which is inherent limitations of MaxEnt predicts. One is the assumption that the parasite niche will not evolve, and the other is the lack of wildlife host distribution data, but the host distribution will inevitably redistribute with climate change [ 18 ]. Nevertheless, it still has positive predictive significance. If regional social economic and land cover type in the future can be integrated into model, the resulting model will be more accurate [ 34 ]. This study did not separately analyze CE and AE, owing to a lack of information on the hospitalization record of echinococcosis types.

Conclusions

This study provides the first attempt to determine the cost of hospitalization with their local GDP in Gansu Province. Spatial analyses of expenditure and the identification of non-endemic areas or risk for these parasites may help in the development of policies for at-risk populations in geographically defined areas. A better comprehension of the role of the environment in clarifying the transmission dynamics of Echinococcus spp. will help monitor improvements in human echinococcosis control strategies by allowing targeted allocation of resources. Raising health care workers and travelers’ disease awareness and preventive health habits is an urgent agenda.

Availability of data and materials

The Gansu Province geographic information data analyzed in the current study are available in the national basic geographic information system [ http://bzdt.ch.mnr.gov.cn/index.jsp ].

The climate variables analyzed in the current study are available in the WorldClim database, [ http://worldclim.org/ ]. The topographic variables analyzed in the current study are available in the Geospatial Data Cloud Platform of the Computer Network Information Center of the Chinese Academy of Sciences, [ http://www.gscloud.cn/ ]. The normalized difference vegetation index analyzed in the current study is available in the Chinese Academy of Sciences Geographical Sciences and Resource and Environmental Data Cloud Platform of the Resource Research Institute, [ http://www.resdc.cn/ ]. The other datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Abbreviations

Gross Domestic Product

alveolar echinococcosis

cystic echinococcosis

human echinococcosis

environmental niche models

global land cover

diagnosis-related groups

normalized difference vegetation index

coupled model intercomparison project phase 6

shared socio-economic pathways

Beijing climate center climate system model 2 medium resolution

the center national de recherches météor ologiques

area under the curve

receiver operating characteristic

centers for disease control and prevention.

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Acknowledgments

We highly thank anonymous reviewers for their thoughtful and insightful comments and suggestions. All authors greatly appreciate Liuyang Chen from Lanzhou University for help with data processing and figure designs.

Author details

1 Department of Pathogenic Biology, School of Basic Medical Sciences, Lanzhou University, Lanzhou, China.

2 The Second Hospital of Lanzhou University, Lanzhou, China.

3 Laboratory Medicine Center, The Second Hospital of Lanzhou University, Lanzhou, China.

This work was supported by the Second Hospital of Lanzhou University Grant No. (202010730222, 202110730208, and CYXZ2020–33, 2020B 045 and CY2019 QN20).

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Xiaoyu Di and Shuo Li contributed equally to this work.

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Department of Pathogenic Biology, School of Basic Medical Sciences, Lanzhou University, Lanzhou, China

Xiaoyu Di, Shuo Li, Bin Ma, Xiaofan Di, Yuhao Li & Bei An

The Second Hospital of Lanzhou University, Lanzhou, China

Xiaoyu Di, Shuo Li, Bin Ma & Xiaofan Di

Laboratory Medicine Center, The Second Hospital of Lanzhou University, Lanzhou, China

Wenwen Jiang

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Study conception and design: Bei An. Data collection and data analysis: Xiaoyu Di, Shuo Li (Funding acquisition), Bin Ma, Xiaofan Di (Funding acquisition), Yuhao Li, and Wenwen Jiang (Funding acquisition). Drafting of the article: Xiaoyu Di and Bei An, Critical revision of the article: Xiaoyu Di and Bei An take all responsibility for the work and/or the conduct of the study, have access to the data, and controlled the decision to publish. The author(s) read approved the final manuscript.

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Supplementary Information

Additional file 1..

Excel A 1. Geographical distribution of echococcosis

Additional file 2.

Excel A 2. Geographical distribution of dogs with echococcosis from literatures

Additional file 3.

Supple FigA1. Procedure of MaXent modeling

Additional file 4.

Supple Table A1. Land types codes

Additional file 5. 

Supple FigA2. Modelling accuracy for predicting suitable habitats and Response curve results of MaxENT modelling of the environmental variables for potentially suitable habitat for Echinococcus spp.

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Di, X., Li, S., Ma, B. et al. How climate, landscape, and economic changes increase the exposure of Echinococcus Spp.. BMC Public Health 22 , 2315 (2022). https://doi.org/10.1186/s12889-022-14803-4

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Volume 30, Number 2—February 2024

Confirmed Autochthonous Case of Human Alveolar Echinococcosis, Italy, 2023

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In September 2023, a patient in Italy who had never traveled abroad was referred for testing for suspected hepatic cystic echinococcosis. Lesions were incompatible with cystic echinococcosis; instead, autochthonous alveolar echinococcosis was confirmed. Alveolar echinococcosis can be fatal, and awareness must be raised of the infection’s expanding distribution.

The main human echinococcal infections are caused by Echinococcus granulosus sensu lato, which causes cystic echinococcosis (CE), and E. multilocularis , which causes alveolar echinococcosis (AE). The parasites have different life cycles and cause different diseases ( 1 ). E. granulosus s.l./CE is endemic worldwide in livestock-raising areas, including Italy, and accounts for most human echinococcal infections ( 2 ). The parasite is transmitted in a domestic cycle between dogs and livestock and causes generally benign disease in humans marked by the formation of well-defined fluid-filled cysts mostly in the liver ( 1 , 2 ). E. multilocularis /AE is endemic to the Northern Hemisphere and is transmitted in a sylvatic cycle between wild canids (e.g., foxes) and small rodents (e.g., voles) ( 2 ).

Humans become infected with the 2 pathogens by accidental ingestion of parasite eggs from material contaminated with infected definitive host feces. In Europe, North America, and Asia, expanding distribution has been observed in recent decades ( 2 ). In Europe, the historical endemic areas are Austria, France, Germany, and Switzerland, and that range has expanded to include Eastern and Northern Europe ( 3 ). In Italy, infected foxes have been reported over the past 20 years in the Trentino-Alto Adige region ( 4 – 7 ). Autochthonous animal transmission might occur in the area ( 8 ), and prevalence in foxes seems to be increasing ( 9 ). A 2017 survey conducted in the Liguria region first detected E . multilocularis in fecal samples of dogs and wolves, suggesting a southward expansion of the parasite ( 10 ) ( Appendix Figure), as predicted by modeling ( 3 ). Surveillance of E. multilocularis in Europe is usually conducted voluntarily ( 11 ), and no structured surveillance program for animal infection in Italy occurs beside targeted surveillance through research projects.

We report a confirmed autochthonous human AE case in Italy. Ethics approval was not necessary because data were derived from routine clinical practice. The patient consented to the publication of this report.

In September 2023, a 55-year-old man in Italy was referred from his local hospital in Bolzano province, Trentino-Alto Adige region, to IRCCS Sacro Cuore Don Calabria Hospital, upon suspicion of CE. The patient was born and lived in Trentino-Alto Adige and had never traveled abroad; he worked in the tertiary sector and did not report contact with wild carnivores. He also did not report risk factors for E. granulosus infection.

Figure . Diagnostic tests for patient in Italy with confirmed autochthonous case of human alveolar echinococcosis, 2023; white arrows indicate lesions. A–D) Contrast-enhanced computed tomography arterial phase. E–H) T2-weighted magnetic resonance imaging....

The suspicion of CE was posed in June 2023, when he underwent abdominal ultrasound for a mild thrombocytopenia, revealing 5 recently developed small hepatic lesions (ultrasound results in 2016 were unremarkable). The lesions were described as septated and hypodense with no contrast enhancement and no calcifications on computed tomography performed in June 2023 ( Figure , panels A–D), hypointense in T1-weighted magnetic resonance imaging (MRI), and hyperintense in T2-weighted MRI ( Figure , panels E–H), with no diffusion restriction. No other lesions were present on total body imaging. Results of Echinococcus serologic testing using Western blot method were positive, but banding pattern was not reported.

We excluded the diagnosis of CE on the basis of the lesions’ morphology on ultrasound, which did not show any CE pathognomonic or compatible features. We observed 5 lesions: 1 with 2.3 cm diameter in hepatic segment I, 1 of 0.9 cm in VI, 2 subcapsular of 2.7 cm and 0.5 cm in VII, and 1 of 1.6 cm in segment VIII (adjacent to the median hepatic vein). The lesions were hypoechoic with irregular margins, particularly the lesion in segment I, which had fine and tightly packed septations ( Figure , panels I–L). The lesions were not enhancing on contrast-enhanced ultrasound ( Figure , panels I–L). Serologic testing using the Echinococcus Western Blot IgG (LDBIO Diagnostics, https://ldbiodiagnostics.com ) was positive for Echinococcus spp., showing genus-specific 7 kDa and 26–28 kDa bands, not assignable specifically to a species. Results of an 18 F-FDG-PET scan showed light hypermetabolism in delayed (4-hour) acquisitions ( Figure , panels M–P). Taken together, those results made the lesions highly indicative of AE.

We performed a biopsy of the only accessible lesion, located in segment VI, and submitted the specimen to the German Reference Laboratory for Tropical Parasites at the Bernhard-Nocht Institute for Tropical Medicine (Hamburg, Germany). A serum sample also submitted for further serologic testing showed low antibody titers against crude antigen preparations of E. multilocularis and E. granulosus (1:40–1:80 in indirect hemagglutination [negative <1:20] and 30–40 arbitrary units in ELISA [negative <20]). Results of Em18-ELISA ( 12 ) were negative. Histology revealed necrotic granuloma and fibrosis without PAS-positive structures. Results of PCR testing targeting cestode cytochrome oxidase and Echinococcus -specific 12S rDNA ( 13 ) were negative. In contrast, immunohistochemistry with the monoclonal antibody Em2G11 ( 14 ) stained positive for small particles of E. multilocularis (spems) ( Figure , panels Q–R). Spems consist of outer laminated layer of Em2 antigen in close proximity to AE lesions and thus confirmed the diagnosis of AE, defined by the WHO Informal Working Group on Echinococcosis (WHO-IWGE) as the presence of clinical-epidemiologic factors plus compatible imaging findings plus seropositivity for echinococcosis plus compatible histopathology ( 15 ). The laboratory uses Em2G11-IHC regularly for suspected AE. The immunohistochemistry has been extensively validated and is also used by other laboratories; CE lesions and other cestode lesions stain negatively ( 14 ), whereas lesions by neotropical E. vogeli stain faintly ( Appendix reference 16 ).

Staging according to the WHO-IWGE ( 1 , 15 ) was P2N0M0 (i.e., central lesions with proximal vascular and/or biliary involvement of 1 lobe, no regional involvement, no metastasis). We adopted a conservative management approach because removing the lesions would require major surgery and because the results of Em18 serologic testing and 18 F-FDG-PET scan suggested low-viability parasites ( 1 , 13 ). At the time of publication, the patient was receiving albendazole (400 mg 2×/d) with fat-containing meals and tolerating the medication well. Follow-up with contrast-enhanced ultrasound and serologic testing was scheduled every 6 months, MRI in 1 year, and 18 F-FDG-PET scan in 2 years ( 1 ).

Conclusions

AE is a complex disease with a high fatality rate (0%–25% 10-year survival) if untreated ( 1 ). It primarily affects the liver and is characterized by infiltrating, metastatic, tumor-like behavior ( 1 ). Unlike CE, AE lesions have no pathognomonic signs on imaging, and the differential diagnosis is mainly tumors ( 1 ). Even in AE-endemic areas, misdiagnosis and consequent incorrect treatment occurs frequently ( 1 ; Appendix reference 17 ).

Curative treatment options include surgery and albendazole if radical resection is achievable, or albendazole alone indefinitely in other cases ( 1 ). Treatment interruption can be envisaged in selected cases when serologic testing and 18 F-FDG-PET scans become negative ( 1 ). In this case, the Western blot banding pattern, low antibody concentrations against crude parasite antigens, negativity of Em18 ELISA, and faint hypermetabolism on 18 F-FDG-PET scan indicate low parasite viability ( 1 , 13 ). PCR on bioptic material was negative, explained by the absence of cell-containing larval structures on histology; however, E. multilocularis –specific immunochemistry was positive, confirming the diagnosis ( 1 , 13 ).

A report from 1928 mentioned 2 human AE cases identified in South Tyrol in 1906 and 1922 ( 2 ), but reports of human confirmed AE in Italy are otherwise lacking; a 2019 research review identified no reports from this country ( 12 ). Italian Hospital Discharge Records reports cases labeled as AE according to International Classification of Diseases, 9th Edition ( Appendix reference 18 ). From the analysis of cases that we could examine ( Appendix reference 19 ), those cases seem to be CE with multiloculated cyst morphology (CE2 and CE3b stages according to WHO-IWGE), erroneously recorded as E. multilocularis ( 1 ).

An expanding area of endemicity of E . multilocularis in Europe has been observed and predicted by modeling ( 3 ). Because of the high lethality of this disease if misdiagnosed and mistreated, physicians, especially in Italy’s alpine regions, must be informed about this infection and its possibility even in patients who have never lived in or traveled to known endemic areas.

Dr. Tamarozzi is a senior research physician and cohead of the WHO Collaborating Centre on Strongyloidiasis and other NTDs at the Department of Infectious-Tropical Diseases and Microbiology, IRCCS Sacro Cuore Don Calabria Hospital, in Negrar di Valpolicella, Verona, Italy, as well as a member of the steering committee of the WHO Informal Working Group on Echinococcosis. Her main field of work is the laboratory- and imaging-based diagnosis of neglected helminthic infections, in particular echinococcal infections.

Acknowledgments

We thank Andrea Angheben, Paola Rodari, Maria Luca D’Errico, and the infectious-tropical diseases ward at IRCCS Sacro Cuore Don Calabria hospital in Negrar for clinical management during the patient’s hospitalization; Stefano Tais for support with sample management; Ansgar Deibel for the discussion on the case diagnosis and management; and Dora Buonfrate for critically reviewing the manuscript.

Funding was provided through Italian Ministry of Health “Fondi Ricerca Corrente –L2” to IRCCS Sacro Cuore Don Calabria hospital, Negrar di Valpolicella, Verona, Italy.

F.T., M.D., E.O., and T.D. performed and interpreted imaging and laboratory tests; F.T., N.R., B.G., and F.G. clinically managed the patient. F.T., D.T., and G.B. wrote the manuscript. All authors reviewed and approved the published version of the manuscript.

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DOI: 10.3201/eid3002.231527

Original Publication Date: January 18, 2024

Table of Contents – Volume 30, Number 2—February 2024

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• Published: 27 March 2024

The effect of cystic echinococcosis (hydatid disease) on carcase weight in cattle in eastern Australia

• Victoria J. Brookes 1 , 8 ,
• Tamsin S. Barnes 2 , 3 ,
• David J. Jenkins 4 ,
• Matthew R. Van der Saag 5 ,
• Robert Dempster 6 &
• Cara S. Wilson 4 , 7  

Scientific Reports volume  14 , Article number:  7297 ( 2024 ) Cite this article

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Cystic echinococcosis is caused by the zoonotic tapeworm Echinococcus granulosus. There has been ongoing controversy over whether it causes weight loss in cattle. Recently implemented recording of comorbidities at processors has provided opportunity to investigate this effect. Using prevalence-based observational data from 1,648,049 adult cattle processed in seven states and territories in Australia (2019–2022), we explored associations between carcase weight, hydatid cysts, comorbidities, sex, age, and region. Linear mixed-effect regression models estimated the effect of cystic echinococcosis on carcase weight, guided by directed acyclic graphs to reduce bias. The highest, previously unreported, prevalence was in the southeast Queensland region. The estimated effect of cystic echinococcosis cysts on carcase weight ranged from a gain of 0.32 kg/carcase (standard error [se] 0.58 kg; two-tooth 2022) to a loss of −5.45 kg/carcase (se 0.63 kg; six-tooth 2019) with most point estimates (11/16) between 0 and −2.5 kg across all cattle grouped by year and dentition. This effect size would be practically undetectable in live cattle which is an important finding; cattle producers are unlikely to observe increased productivity through weight gain from cystic echinococcosis prevention in cattle, and awareness to strengthen prevention in domestic dogs around cattle properties to reduce human risk remains a public health focus.

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Introduction

Echinococcus granulosus is a tapeworm that causes the parasitic zoonosis, cystic echinococcosis. There are several species of Echinococcus globally, but only Echinococcus granulosus sensu stricto has been reported in Australia. Canid species are definitive hosts, harbouring the adult tapeworm. In Australia, these are domestic dogs, dingoes, their hybrids, and foxes. Herbivorous or omnivorous species are intermediate hosts in which the larval stage of the parasite develop within fluid-filled (hydatid) cysts in the viscera (offal). In Australia these are predominantly macropods, sheep, and cattle 1 , 2 . Although cattle are considered accidental hosts and infection is generally subclinical, hydatid cysts are frequently found in the viscera at processing 1 , 3 , where they are primarily reported in the liver and lungs 3 , 4 . Cysts are less frequently reported in the heart, kidney, spleen 1 , 3 , 5 and occasionally the brain and skeletal muscle 1 , 6 .

Factors associated with cattle and their environment influence the probability of hydatid cysts at processing. For example, the prevalence of hydatid cysts at processing has been reported to be higher in older cattle and those that are grass-fed 3 , 4 , 7 , 8 . Reported prevalence in cattle < 1 year old is low (< 3%) 3 , 9 , but for those that are > 4 years, prevalence of up to 39.5% has been reported 4 , 8 , and a recent study reported that the true prevalence in eight-tooth animals (estimated > 3.5 years) could be as high as 85.6% (Wilson, et al. 3 ). The prevalence of hydatid cysts at processing also varies with geographic origin of the cattle, with higher prevalence regions including the Great Dividing Range and along the northern coast of New South Wales 1 , 3 , 4 , 9 . This has been attributed to the distribution of wild dogs, macropods (more abundant in regions encroaching on the hills of the Great Dividing Range), and more favourable climatic conditions for survival of the environmental stage of the parasite 4 , 9 . Overall, previous estimates of prevalence have generally been lower than more recent estimates which have accounted for the sensitivity and specificity of meat inspection 1 , 3 , 4 , 7 .

Understanding the impact that cystic echinococcosis has on the weight of cattle has been constrained by the use of observational data and study design, and often, evidence to support claims that cystic echinococcosis causes weight loss has been weak or non-existent. Although it was reported that cystic echinococcosis reduced productivity in cattle in a case-study in Cyprus, the source population from which this was inferred was not described 10 . Similarly, in a review of the economic impact of hydatid infection in production animals, a reduction in carcass weight was also reported (up to 20%); however, supporting studies were not available 11 . A study conducted in 2006 estimated that globally, annual economic losses from cystic echinococcosis in livestock could be greater than USD 2 million due to liver condemnation, decreased carcase weight, decreased fecundity, reduced milk production and decreased hide value 12 , although there was great uncertainty about the effect of cystic echinococcosis on some parameters, including carcase weight. Whilst the effects of productivity losses due to offal condemnation can be directly measured, an effect of cystic echinococcosis on carcase weight has been difficult to estimate because other causes of reduced carcase weight such as concurrent disease, sex, system (grass fed versus feedlot), and cattle origin have not been recorded 13 . For example, unadjusted estimates of up to 16.2 kg reduction in carcase weight in cattle with cystic echinococcosis have been reported in Australian studies 14 , 15 . Recently however, multi-condition reporting for carcase and offal defects has been instigated in some Australian processors, whereas previously, processors could only report the main reason for downgrading or condemnation of carcases and offal at processing and would most likely record the predominant lesion. With the inclusion of other key variables that affect cattle carcase weight (for example, sex, location and system, breed and age 16 ), this provides an opportunity to more accurately estimate the impact of cystic echinococcosis on weight using observational data. Understanding the impact that cystic echinococcosis has on the weight, and therefore, the productivity of cattle is important for prevention and control, because it influences adoption of control strategies, such as deworming of domestic dogs, on-farm wild dog control, and potentially, the vaccination of cattle against infection with Echinococcus 17 , 18 .

To determine the impact of cystic echinococcosis on the weight of cattle, it would be ideal to conduct a randomised controlled trial in which the weight of some cattle that were randomly infected with E. granulosus could be compared with others that were not, (such that the only difference between the groups was cystic echinococcosis). However, this has low feasibility due to the long duration of this disease. Therefore, observational data such as abattoir records provide the next best option for causal inference. However, it is well known that observational data are prone to bias—infection with E. granulosus is not random so confounding occurs due to other causes of weight loss that are also associated with cystic echinococcosis, the analysed cattle might not be a representative sample of the source population (selection bias), and parameters might be measured or classified incorrectly (information bias). Recently, the use of directed acyclic graphs (DAGs) has become more prominent to avoid, or at least inform, sources of bias in observational studies through directing correctly structured analyses 19 . A recent study highlighted the challenges of statistical analysis without causal thinking and demonstrated how the understanding underlying structure of data (for example, using DAGs) is critical for causal inference 20 .

The objective of this study was to estimate the effect of the presence of hydatid cysts on carcase weight of cattle processed at several processors in eastern Australia using observational data with analyses guided by a DAG. These processors were selected because they report multiple comorbidities in carcases and the viscera, not only the predominant cause of downgrading or condemnation. This study has implications for public health as well as cattle productivity; if cystic echinococcosis reduces the carcase weight of cattle, producers will have more incentive to prevent disease in their cattle by controlling Echinococcus in dogs, which also reduces the risk of infection of people.

We hypothesised that the presence of hydatid cysts (infection with Echinococcus granulosus sensu stricto) in beef cattle reduces carcase weight at processing. The exposure variable of interest was the presence of hydatid cysts (measured as hydatid cysts reported at processing), and the outcome of interest was hot standard carcase weight (HSCW: weight within two hours of slaughter following standard trim) at processing. The target population was beef cattle in Australia, and the source population was adult beef cattle processed between 2 January 2019 and 26 July 2022 at five abattoirs in eastern Australia that had remained in the same region for their lifetime.

Eligible cattle had the same property identification code (PIC) region recorded at birth and prior to processing; we made the assumption that these cattle were likely to have stayed in that PIC region for their lifetime. PIC codes are unique property identifiers for properties on which livestock are held, incorporating spatial identifiers representing regions in which the property is located (here, referred to as ‘PIC region’). As part of Australia’s National Livestock Identification System (NLIS), all cattle are individually identifiable by an electronic device (generally an ear tag), all physical locations on which livestock are held are identified by means of a PIC, and all livestock location data and movements are recorded in a central database 21 , 22 .

Ethical approval was not required for this study. Data were obtained for cattle that were processed in the beef supply chain for human consumption not for the purposes of this study, and no samples were collected from cattle.

Data collection and cleaning

Data were provided for 3,364,737 cattle processed between 2 January 2019 to 26 July 2022 at five processors (three sites in Queensland, one site in New South Wales, and one site in South Australia). Following data cleaning in Excel 23 including checking for data consistency and removal of duplicates, cattle that had the same PIC region recorded at birth and prior to processing were selected.

Cattle were removed from the dataset if they were likely to be vealers (not weaned for more than seven days and no evidence of eruption of permanent incisor teeth; https://www.mla.com.au/general/glossary/#glossarySection_V , accessed 1 June 2023) by removing cattle with zero-tooth and HSCW < 150 kg, or any cattle with HSCW < 50 kg (likely vealers but dentition misclassified). A subset of 1,648,049 cattle for analysis remained.

Variables recorded for each animal relevant to the study were PIC at birth and prior to processing, processor, type of animal (vealer or beef), sex, dentition (zero-, two-, four-, six-, and eight-tooth), whether the animal was grain or grass fed, the presence of cystic echinococcosis and organs infected, the presence of other pathological conditions and causes of downgrading and condemnation including liver fluke (comorbidities), and HSCW. The presence of hydatid cysts was categorised to a single binary variable according to whether hydatid cysts were detected in any organ, following assessment of the proportion of cattle with hydatid cysts in the liver relative to other organs. Conditions other than fluke that were identified at processing and could have influenced carcase weight (comorbidities) were categorised as a binary variable for individual cattle according to whether there was presence of at least one comorbidity. We made no assumption about the severity of comorbidities other than a reduced carcase weight would be expected either due to smaller size (reduced growth) or trimming. Comorbidities included arthritis, bruising, and other carcass defects such as cancer, anaemia, antibiotic treatment, fracture, and myositis (see Supplementary Material for the full list of comorbidities). Age was classified according to dentition with zero-, two-, four-, six-, and eight-tooth cattle of approximate ages < 18 months, 18–30 months, 24–36 months, 30–42 months, and ≥ 42 months, respectively 24 .

Descriptive analyses

Descriptive statistical analyses of cattle characteristics, disease, and HSCW (outcome variable of interest) were conducted. Choropleth maps of characteristics of the cattle at processing from each PIC region were produced (QGIS v 3.28.2, https://qgis.org/en/site/ ). These were: the number of cattle, proportion of cattle in which hydatid cysts were detected (exposure variable of interest), proportion of cattle detected with fluke, proportion of cattle detected with comorbidities, proportion of grain-fed cattle, distribution of sex, dentition, and HSCW. Choropleth maps were also used to display the mode frequency of processor for cattle from each PIC region, and the Euclidean distance from PIC region centroid to processing site of cattle was calculated. A Kruskal–Wallis test (P > 0.05) was used to determine if the distribution of the Euclidian distances travelled by cattle from PICs to processors travelled differed between sites; otherwise (and in accordance with statistical rationale 25 , 26 , 27 ), we avoid the use of statistical hypothesis testing in the descriptive analyses because the purpose of this section is to demonstrate patterns in covariates before adjustment for bias in the ‘statistical analyses’ section.

Statistical analyses

All statistical analyses were conducted in R 28 and packages tidyverse 29 , plyr 30 , ggplot 31 , lubridate 32 , epiR 33 , lme4 34 , Performance 35 , nlme 36 , and reshape2 37 . In this section, analyses were conducted with the aim of minimising bias to determine the causal effect of cystic echinococcosis on cattle carcase weight.

A directed acyclic graph (DAG; Figure S1 ) of variables that influence, or could be influenced by, both the identification of cystic echinococcosis at processing and HSCW was developed using previously published information about risk factors for cystic echinococcosis in cattle in Australia and consultation with cystic echinococcosis and beef cattle industry experts (DJ, MVdS, RD, JL, CW). The DAG was used to identify the minimal sufficient adjustment set of variables to estimate the total effect of the presence of hydatid cysts on HSCW using linear, mixed-effects regression models that accounted for potential sources of bias using the lmer function in the lme4 package in R 34 . Due to the way in which parameters are estimated (maximum likelihood) estimates and the unbalanced nature of the observational data in this study, P values were not calculated; standard errors of estimates and 95% confidence intervals are presented in tables and plots, respectively.

Initially, models were constructed using the entire dataset to broadly investigate the total effect of cystic echinococcosis on carcase weight with and without adjustment for confounding pathways, and to investigate the effect of clustering by PIC region. Model fit was assessed on the full model (all covariates included) using the entire dataset to evaluate assumptions about normality of residuals, normality of random effects, linear relationships, homogeneity of variance, and multicollinearity. Following this preliminary investigation, models to investigate the total effect of cystic echinococcosis on carcase weight which accounted for confounding pathways and clustering (by including PIC Region as a random effect) were constructed for groups of cattle of the same age (dentition) and year of processing so that the population in each group could be considered stable regarding exposure experiences (including covariates) and subsequent cystic echinococcosis incidence and duration. Plots of point estimates with 95% confidence intervals of the total estimated effect of cystic echinococcosis (detected at processing) on hot standard carcass weight and model summaries were reported.

Of the 1,648,049 eligible cattle, most were processed at the three Queensland sites (Qld1, Qld2, Qld3; n = 1,195,472, 72.5%; Fig.  1 ), of which the Qld3 site processed most (n = 523,772). The South Australian site processed the fewest cattle (n = 160,661). Most cattle were sourced from eastern regional and mid to mid-north coast Queensland (Figure S2 ). The median number of individual PICs in each PIC region was 49 (range 1–861), and the median number of cattle processed from each individual PIC was 1268 (range 1–218,627). The annual number of cattle processed at all the sites in the study decreased from 607,939 in 2019 to 196,263 in 2022 (2022 only includes data to 26 June 2022; Figure S3 ). The geographic extent of the source distribution for cattle processed at each site varied (Figure S4 ), and the median Euclidean distance of PIC region centroids from the processing site varied significantly between sites (Kruskal Wallis rank sum test Χ 2 194,994, df 4, P < 0.01; Figure S5 ).

Number of adult cattle with the same property identification code (PIC) region recorded at birth and prior to processing, at each processor and stratified by sex, in a study of the effect of cystic echinococcosis on carcase weight at five processors in eastern Australia, 2019–2022.

Cattle characteristics

Figure  2 shows the proportion of cattle by sex from each PIC region. A greater proportion of cattle were female from PIC regions in Queensland and the Northern Territory than from southern states. This is reflected in the proportion of female cattle processed at each site; most cattle processed at Queensland sites were female (n = 726,215, 60.7%; Fig.  1 ), and most cattle processed at the New South Wales and South Australia sites were male (n = 332,675, 73.5%) (Fig.  1 ). By dentition and sex, the largest group of cattle were eight-tooth females (n = 479,011), and the smallest was eight-tooth males (n = 60,757; Figure S6 ). Figure  3 shows that older cattle were more likely to have been sourced from northern PICs. The proportion of cattle that had been grain-fed also varied by region, with grain-fed cattle commonly being from southern PIC regions (Fig.  4 ).

Proportion of female cattle with the same property identification code (PIC) region recorded at birth and prior to processing, by PIC region, in a study of the effect of cystic echinococcosis on carcase weight at five processors in eastern Australia, 2019–2022. Map made by authors using QGIS 50 .

Age of cattle by mean dentition (one–eight teeth) with the same property identification code (PIC) region recorded at birth and prior to processing, by PIC region, in a study of the effect of cystic echinococcosis on carcase weight at five processors in eastern Australia, 2019–2022. Map made by authors using QGIS 50 .

Proportion of grain-fed cattle with the same property identification code (PIC) region recorded at birth and prior to processing, by PIC region, in a study of the effect of cystic echinococcosis on carcase weight at five processors in eastern Australia, 2019–2022. Map made by authors using QGIS 50 .

Proportion of cattle with the same property identification code (PIC) region recorded at birth and prior to processing with comorbidities (disease conditions other than hydatid cysts or liver fluke) detected at processing from each PIC region, in a study of the effect of cystic echinococcosis on carcase weight at five processors in eastern Australia, 2019–2022. Map made by authors using QGIS 50 .

Disease detection

The proportion of cattle with comorbidities detected at processing varied by PIC region (Fig.  5 ). In contrast, the proportion of cattle detected with hydatid cysts and liver fluke demonstrated a strong spatial pattern (Figs.  6 and 7 ). Hydatid cysts were more commonly detected in cattle from northern NSW and southeast and coastal Queensland, and carcases with liver fluke were more commonly detected in New South Wales and Victoria, especially southwest coastal regions. Of particular interest was the high proportion of cattle with hydatid cysts detected in the Brisbane region (Figure S7 ). Although fewer cattle were processed from this region, the proportion of cattle in which hydatid cysts were detected was consistently high (33–70%). The proportion of all cattle with hydatid cysts detected in any organ was 17.2% (n = 283,073). Of these, 94% of cattle had cysts detected in the liver (44% in liver and lung), and 6% had cysts detected in the lung only (S8). A negligible number of cattle had cysts detected in the spleen (n = 44), or heart (n = 29), and of these, most also had hydatid detected in the liver (n = 67; 92%). The proportion of cattle detected with hydatid cysts increased with age (S9). Hydatid cysts were also more commonly detected in cattle that had not been grain-fed, and in female cattle (Figure S10 ). Female cattle were less commonly grain-fed (Figure S10 ) and a higher proportion of them were older (eight-tooth) cattle (Figure S6 ).

Proportion of cattle with the same property identification code (PIC) region recorded at birth and prior to processing with hydatid cysts detected at processing from each PIC region, in a study of the effect of cystic echinococcosis on carcase weight at five processors in eastern Australia, 2019–2022. Map made by authors using QGIS 50 .

Proportion of cattle with the same property identification code (PIC) region recorded at birth and prior to processing with liver fluke detected at slaughter from each PIC region, in a study of the effect of cystic echinococcosis on carcase weight at five processors in eastern Australia, 2019–2022. Map made by authors using QGIS 50 .

Carcase weight

Hot standard carcase weight (HSCW) was similar between all age groups (Fig.  8 ). Female cattle were generally lighter, with mean HSCW 261.29 kg (95% range 182.4–363.6 kg, n = 846,117 cattle) compared to male cattle with a mean HSCW of 330.19 kg (95% range 235.8–433.4 kg, n = 801,932 cattle). Carcases from cattle that were not grain-fed were also lighter than grain-fed cattle (Fig.  9 ). Mean HSCW in grain-fed cattle was 340.4 kg (95% range 245.8–439.4 kg; n = 353,211 cattle), and mean HSCW in non-grain-fed cattle was 282.4 kg (95% range 188–379.9 kg, n = 1,294,828). Carcase weight was generally lower in carcases in which hydatid cysts were detected by approximately 14 kg (Fig.  9 ). Mean HSCW in cattle in which hydatid cysts were detected was 283.0 kg (95% range 189.2–404 kg; n = 283,073 cattle), and mean HSCW in cattle in which hydatid cysts were not detected was 297.3 kg (95% range 192–417.5 kg, n = 1,364,976).

Carcase weight (HSCW = hot standard carcase weight) of cattle with the same property identification code (PIC) region recorded at birth and prior to processing, stratified by sex, in a study of the effect of cystic echinococcosis on carcase weight at five processors in eastern Australia, 2019–2022.

Carcase weight (HSCW = hot standard carcase weight) of cattle with the same property identification code (PIC) region recorded at birth and prior to processing, by the presence of hydatid cysts at processing (left) and whether they were grain-fed (right), in a study of the effect of cystic echinococcosis on carcase weight at five processors in eastern Australia, 2019–2022.

There was a visual association between the monthly proportion of female cattle, cattle that were not grain-fed, the mean age of cattle, the mean carcase weight of cattle and the proportion of cattle in which hydatid cysts were detected (Figure S11 ). These findings are consistent with the strong spatial pattern of the mean weight of cattle processed increasing from northern to southern PICs (Fig.  10 ), where cattle in the northern PICs were more likely to be female, older, and not grain-fed (Figs.  2 , 3 and 4 ). This is also the region in which hydatid cysts were more commonly detected in processed cattle (Fig.  6 ).

Mean hot standard carcase weight of cattle which had remained on the same property identification code (PIC) region for their lifetime, from each PIC region in a study of the effect of cystic echinococcosis on carcase weight at five processors in eastern Australia, 2019–2022. Map made by authors using QGIS 50 .

Preliminary statistical models

Models to explore clustering and the unadjusted (confounding not considered) association of cystic echinococcosis on HSCW were conducted on the entire dataset of 1,648,049 adult beef cattle that had the same PIC region recorded at birth and prior to processing (Table 1 ).

The univariable, fixed effect, linear regression model indicated that without adjustment for confounding pathways, the association of the identification of cystic echinococcosis on carcase weight appeared to be large (carcases in which hydatid cysts were detected were on average 14.25 kg [standard error, se 0.12 kg] lighter than carcases in which hydatid cysts were not detected; Table 1 , A), consistent with univariable descriptive analyses (Fig.  9 ). However, in the full model (Table 1 , B), which included year of processing and covariates to reduce confounding as fixed effects (identified in the DAG [Figure S1 ]: sex, presence of comorbidities, presence of fluke, abattoir, grain-fed or not, PIC region), the total effect estimate of cystic echinococcosis on carcase weight was − 4.46 kg (carcases in which hydatid cysts were detected were on average 4.46 kg [se 0.1 kg] lighter than carcases in which hydatid cysts were not detected).

Models in which PIC region was included as a random effect indicated that carcase weight was moderately clustered by PIC region: the intraclass correlation coefficient (ICC) was high in the null model (Table 1 ; C) relative to the full model (Table 1 ; D), at 0.31 and 0.18, respectively. This is also consistent with the descriptive analyses – carcase weight was strongly associated with PIC region (Fig.  10 ), as were covariates grain-fed, sex, hydatid, and fluke detection (Figs.  2 , 3 , 4 , 6 , 7 ). Model assumptions held for normality of residuals, normality of random effects, linear relationship, homogeneity of variance, and lack of multicollinearity (Figure S12 ).

Final statistical models

Due to the nature of the data (prevalence rather than incidence of hydatid cysts), models with subgroups of cattle by age (dentition) and year were constructed to estimate the total effect of hydatid cysts on hot standard carcase weight by age and annual cohort. All models included covariates (sex, presence of comorbidities, presence of fluke, abattoir, grain-fed or not) to adjust for confounding pathways, and a random effect of PIC region.

The point estimates of the total effect of the presence of hydatid cysts ranged from − 5.45 kg (se 0.63 kg) to 0.32 kg (se 0.58 kg), in six-tooth cattle in 2019 and two-tooth cattle in 2022, respectively. Most point estimates (11 of 16) were between − 2.5 and 0 kg (Fig.  11 ). Model summaries (Tables S1 – S4 ) indicate clustering by PIC region, with ICCs ranging from 0.24 – 0.38. Plots of fixed effect coefficients for all covariates in the models are included in Supplementary Material for complete information about each model but should not be interpreted as effect estimates for these covariates (Figures S13 – S16 ).

Point estimates and 95% confidence intervals of total effects of the presence of hydatid cysts (detected at processing) on hot standard carcase weight (HSCW; kg) in linear mixed-effects regression analyses of cattle stratified by age (dentition) and year, which had the same property identification code (PIC) region recoded at birth and prior to processing. Models are listed by year (2019–2022) and age (dentition; two-eight tooth). Models included fixed effects covariates: sex, presence of comorbidities, presence of fluke, abattoir, grain-fed (yes/no), and random effect PIC region.

The geographic extent of cattle sourced in this dataset and the recording of comorbidities including fluke as well as hydatid cysts during processing provided greater opportunity to investigate cystic echinococcosis than has previously been possible. We estimated that in each age group and year of processing, carcase weight was lighter by approximately 0 – 2.5 kg in cattle in which hydatid cysts were detected. It has been assumed that infections in which there are many and large cysts (which are more likely in older cattle due to the duration over which cysts have developed) will have a greater effect on weight, if there is any effect at all 38 . However, it is also possible that earlier, active infections in younger cattle stimulate an immune response to the disease process (and thus, cause reduced weight, as can be observed with other diseases in cattle 39 , 40 ) than chronic infections in older cattle in which cysts are already walled off. The level of infection was not differentiated in cattle in the current study although was explored in a previous study in cattle processed in Australia from a wide geographic catchment area 38 . It was reported that cattle typically have light infections (few and small cysts), but it is the heavier infections that are more likely to be reported by the meat inspector regardless of age group 38 , 41 . However, whilst the estimated effect was consistent across age groups throughout the study years and is biologically plausible, the finding is based on observational data in which prevalence of cystic echinococcosis, not incidence, was reported. Therefore, we discuss this limitation and potential sources of bias below.

Another new finding from this study was that the highest apparent prevalence of hydatid cysts at processing centered on cattle sourced from the Brisbane region. Whilst high prevalence has been demonstrated previously along the Great Dividing Range and coastal northern New South Wales and most of the Queensland coastline, as well as regional Queensland, previous studies have not focused or have had few cattle from the Brisbane region 3 , 4 . Our study provides more comprehensive evidence that the distribution of cystic echinococcosis in cattle is consistent with the distribution of wild dogs and dingoes along the Great Dividing Range and coast where the climate is conducive to survival of Echinococcus eggs on pasture.

Residual confounding of the estimated total effect of hydatid cysts on carcase weight in this study is possible despite accounting for major variables that influence both carcase weight and the probability of infection with hydatid cysts (sex, grass or grain-fed, and comorbidities including fluke) in the statistical models. For example, breed of cattle was unknown, and is associated with geographic locality 4 ; Bos indicus breeds of cattle are more often reared in northern Australia where cystic echinococcosis is more prevalent, and could be lighter by age than Bos taurus breeds in southern Australia. Factors such as breed can be considered as management decisions that are influenced by the farm location (producers rear breeds suited to the regional climate, topography, and vegetation) and therefore, were broadly accounted for by the inclusion of PIC region in the statistical model. However, variation within PIC regions will occur. For example, cattle that are less well grown for age could also be more likely to come from areas where they are more likely to become infected with hydatid cysts, such as marginal grazing areas where hosts such as wild dogs and macropods or sheep are present. Data about proximity to unimproved land on which wild dogs could roam, types of fencing that might allow dogs to access cattle properties, and the presence of domestic dogs on the property were not available. Therefore, whilst farms within PIC regions are broadly similar, heterogeneity within PIC regions could explain the apparent lower weight of carcases from cattle with cystic echinococcosis.

We also considered the possibility of selection bias of the estimated effect of cystic echinococcosis on carcase weight through a variety of mechanisms. If cattle die on farm, either due to disease or home slaughter, this could be considered as ‘loss to follow-up’ in the study population, and an additional association with the probability of this loss to follow-up with exposure to hydatid cysts would result in a biased estimate of the effect of cystic echinococcosis on carcase weight. However, given the insidious nature of cystic echinococcosis (inapparent clinical signs), the probability of cattle dying due to cystic echinococcosis is negligible. In contrast, home slaughter could have an association with cystic echinococcosis if it is more likely practiced by non-commercial producers in marginal cattle-rearing areas where cattle will also be lighter due to poorer grazing as well as also more likely to be infected with hydatid cysts. However, given the small population of home-slaughtered cattle relative to the number that are processed commercially in Australia, we believe that bias of the estimated effect of hydatid cysts on carcase weight due to this would be negligible.

The selection of processors in the study could induce selection bias via a ‘Berkson bias’ mechanism that is also worth considering. For example, if processors are more likely to have attracted producers from regions which are systematically more (or less) likely to have cattle with hydatid cysts (producers in northern PIC regions generally go to Queensland processors, and those in southern PIC regions where cystic echinococcosis is less prevalent generally go to processors in southern states), and these processors also target cattle of particular weights for specific markets, an apparent statistical association would be created between cystic echinococcosis and carcase weight (selection bias; Fig.  12 ). Overall, we believe selection bias via this mechanism is unlikely due to the diverse geographic range of the processors in this study and their large source regions. This pathway of selection bias (Fig.  12 ) was also partially blocked by variables associated with ‘management decision’ that were included to control confounding.

Directed acyclic graph of a mechanism for selection bias of the estimated effect of cystic echinococcosis on carcase weight, via processor. Management decisions influence cystic echinococcosis and a producer’s choice of processor, but live weight subsequently achieved on farm can also influence where an animal is eventually processed. The variable, ‘Processor’, is inherently controlled (red box), because the dataset is from selected processors, and is also controlled within the analysis. The variable ‘management decisions’ is only partially controlled by PIC region (an ancestor variable), and whether cattle are grainfed, and their sex and age (dentition).

Lastly, measurement error and misclassification of any variables included in the analyses could cause information bias of the effect of cystic echinococcosis on carcase weight. The sensitivity and specificity of hydatid cyst detection at processing can be low 41 (although in this study, is likely to be improved due to recording of comorbidities) and is likely to vary between meat inspectors and processors, and with numbers, sizes and locations of cysts in cattle. As mentioned above, it has been suggested that if cysts do affect weight, then many and large cysts could be more likely to have a greater effect on weight 13 , 38 . The number and size of cysts was not reported in the dataset used in the current study; however, in a previous study in Australia, we found that the probability of detection was higher in cattle with multiple cysts (data not available on detection probability according to size or location of cysts) 41 . Therefore, cattle with a greater number of cysts are more likely to be represented in this dataset; consequently, we can expect that a true effect would not be greater than our estimated effect. Regarding detection differences between sites, the liver and lungs are the main predilection sites for hydatid cysts in intermediate hosts 5 , 42 , 43 , and most studies of Australian cattle report cysts either solely in the liver or in both liver and lungs (less commonly lung only) 1 , 4 , 44 . This is consistent with findings in the current study. Unusually, one study of Australian cattle arriving in Japan found cysts predominantly in the lungs 45 . Another from Chile found that cysts were more likely to be solely in the lungs in young cattle or when cattle were co-infected with fluke 46 . Unlike the current study, findings in all these previous studies were not consistently stratified by major confounding factors such as age, comorbidities including fluke, and origin of cattle; therefore, differences in proportions of cysts in various locations are difficult to interpret and the findings in the current study should not be interpreted as misclassification. In addition, in the current study, the geographic distributions of cystic echinococcosis and fluke in Australia are consistent with known epidemiology (wild dogs in the Great Dividing Range are considered important hosts for Echinococcus granulosus , and coastal, warmer regions are areas in which water and the snail involved in the lifecycle of Fasciola hepatica [fluke] is found) and demonstrated relatively different geographic distributions 47 , 48 . Therefore, whilst some cattle with cystic echinococcosis in the lungs but not the liver (if fluke co-infection truly influenced cyst location) might have been misclassified as negative (if lung cysts are less likely to be detected), the proportion of cattle in which this would have occurred would have been small in this Australian context and we consider it would have little influence on the effect estimate in the current study. Regarding misclassification bias associated with processors, in the current study, this potential source of information bias was accounted for by including processors in the analyses; however, this will not account for differences within processors (variation between inspectors) or regional differences. Whilst the variation between inspectors within each processing site could be considered relatively low (they are all trained on the same pathways and learn from each other at the same site), regional differences could be marked due to the spatial variation in relative frequency of other diseases. For example, hydatid cysts might be more readily detected in cattle from northern PIC regions because fluke (another parasitic condition found in the liver) is less likely in this region and does not provide a competing diagnosis. If there is a higher probability of hydatid detection in northern PIC regions where cattle are inherently lighter, this effect could be incorrectly attributed to hydatid cysts rather than changes in detection probability, accounting for the effect estimated in this study. It is known that increasing time for meat inspection increases the sensitivity of disease detection 49 , and although processors in which multiple morbidities can be recorded were selected for this study, it is likely that recording is still influenced by processing line speed and that the most obvious or expected conditions would be recorded first, followed by other conditions as time allows. The influence of bias due to differing probability of hydatid detection in PIC regions in this study is minimised by the inclusion of PIC region as a covariate in the statistical analyses.

As well as the sources of bias discussed above, another limitation of the data used in this study is recording of prevalent, not incident, exposures and outcomes. Estimation of an unbiased effect measure using prevalence data depends on an underlying stable cohort so that exposure histories are comparable between groups, with known incidence and duration of cystic echinococcosis. Whilst the analysis was stratified by age and year of processing to increase stability within groups, dentition was used as a proxy for age in this study, which is a broad representation of actual age. To determine subtle effects (for example, a producer keeping cattle for a few extra weeks to reach a target weight because they were slower to gain weight due to cystic echinococcosis) would require knowledge of days since infection with hydatid to determine if weight gain is slowed by infection. Even with accurate age data, cattle will be exposed at different times depending on their herd circumstances (therefore, duration of time with hydatid will vary). The effect becomes more marked as cattle reach eight-teeth because they can be any age > 3.5 years. Cattle that are 3.5 years old are more likely to be in better body condition than those that are 10 years old. Older cattle are also more likely to have detectable hydatid cysts due to the longer exposure time to Echinococcus eggs in the environment and the longer time for cysts to develop in their viscera 38 .

The small reduction in carcase weight due to the presence of hydatid cysts that was estimated in this study is a biologically plausible effect. Major sources of bias such as the influence of sex, age, comorbidities (including fluke) could be accounted for; therefore, this estimate is vastly reduced from previous crude estimates 10 , 11 , 14 , 15 . However, some sources of confounding, selection and information bias could not be ruled out and would most likely bias the estimate towards a negative effect on carcase weight as observed in our analyses; overall, it is likely that cystic echinococcosis has no appreciable effect on carcase weight in cattle.

Ultimately, if valid, such a small reduction in carcase weight would be a very small percentage of liveweight for most cattle and difficult to observe. Whilst this weight difference might be valuable at population level, it is debatable whether it would be sufficient for producers to be motivated to undertake greater control measures against hydatid infection in their cattle. A cost–benefit analysis (CBA) would need to be conducted to determine the value of development and implementation of control strategies (for example, vaccination) to producers and processors.

We believe that further collection of observational prevalence-based data is unlikely to further refine our estimate of the effect of cystic echinococcosis on carcase weight, given the difficulty of measuring age of cattle and time onset of disease, as well as potential common causes of cystic echinococcosis and carcase weight. Given the current findings, we suggest that if a CBA indicates an economically viable impact of control measures, a field-trial in which control strategies are randomised to cattle would need to be conducted. However, it should be noted that the study would be logistically difficult because a large number of cattle would be required to detect small differences in weight, and the cattle would need to be followed to processing with accurate records from birth.

A finding in the study that should not be overlooked is the high prevalence of cystic echinococcosis in cattle in the Brisbane region. This has not previously been highlighted. To reduce the risk of echinococcosis in people, cattle producers and domestic dog owners in this region should be targeted by public health interventions to ensure safe disposal of cattle and other intermediate hosts (macropods and sheep) that die on farm and the use of effective anthelmintics in dogs.

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Acknowledgements

We thank the processor who provided data for the study.

This study was supported by Virbac (Australia) Pty Ltd and Meat & Livestock Australia.

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Victoria J. Brookes

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Epivet Pty. Ltd., Withcott, QLD, 4352, Australia

School of Agricultural, Environmental and Veterinary Sciences, Faculty of Science and Health, Charles Sturt University, Wagga Wagga, NSW, 2678, Australia

David J. Jenkins & Cara S. Wilson

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All authors designed the study. C.W. and V.B. prepared and analysed the data and wrote the draft manuscript. All authors contributed to interpretation of findings, and reviewed the manuscript.

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Brookes, V.J., Barnes, T.S., Jenkins, D.J. et al. The effect of cystic echinococcosis (hydatid disease) on carcase weight in cattle in eastern Australia. Sci Rep 14 , 7297 (2024). https://doi.org/10.1038/s41598-024-57886-2

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Research Article

Osseous cystic echinococcosis: A case series study at a referral unit in Spain

Roles Formal analysis, Investigation, Methodology, Supervision, Writing – original draft, Writing – review & editing

* E-mail: [email protected] (BMM); [email protected] (RLV)

Affiliation National Referral Unit of Tropical Diseases, Infectious Diseases Department, Ramón y Cajal University Hospital, IRICYS, Madrid, Spain

Roles Formal analysis, Investigation

Roles Investigation, Visualization

Roles Formal analysis, Investigation, Methodology

Roles Formal analysis, Investigation, Visualization

Roles Conceptualization, Formal analysis, Investigation, Methodology, Writing – review & editing

• Begoña Monge-Maillo, 
• María Olmedo Samperio, 
• José Antonio Pérez-Molina, 
• Francesca Norman, 
• Carla Ruth Mejía, 
• Sandra Chamorro Tojeiro, 
• Rogelio López-Vélez

• Published: February 19, 2019
• https://doi.org/10.1371/journal.pntd.0007006
• Reader Comments

Cystic echinococcosis (CE) is present in all continents, except for the Antarctica. Characteristically, CE lesions are found in the liver and the lungs, but virtually any part of the body may be affected (the spleen, kidneys, heart, central nervous system, bones, among others). It is estimated that the incidence of bone involvement in CE is 0.5% to 4%.

Methodology

A retrospective study was performed of patients with osseous CE treated at the National Reference Unit of Tropical Diseases of the Ramon y Cajal Hospital, Madrid, Spain, between 1989 and December 2017. Epidemiological, clinical, diagnostic and therapeutic data of patients with long-term follow-up were collected.

Main findings

During the study period, of the 104 patients with CE, 27 exhibited bone involvement (26%). The bones most frequently affected were the spine, followed by the ribs, pelvis, femur, tibia and the scapula. The most common symptom was pain followed by medullar syndrome and pathologic fracture. In total, 81.5% of patients underwent surgery for osseous CE at least once. As many as 96% received albendazol either in (mostly long-term) monotherapy or in combination with praziquantel.

Conclusions

The diagnosis and management of osseous CE is challenging. In many cases osseous CE should be considered a chronic disease and should be managed on a case-by-case basis. Lifelong follow-up should be performed for potential recurrence and sequels.

Author summary

Echinococcosis occurs in humans as a result of infection by a cestodes of the genus Echinococcus . One of the species, E . granulosus , causes cystic echinococcosis (CE) in humans worldwide. In the lifecycle there is a definitive host (generally dogs) which host this parasites at the small bowel. From there, ground is shed with the eggs of the parasite through feces and the intermediate host (usually a sheep or other herbivores get infected). Humans act as an incidental intermediate host when they become infected through the consumption of water or food contaminated with Echinococcus eggs. Once the egg has been ingested, it penetrates the intestinal mucosa and through the circulatory system finds an anatomical site forming a cystic lesion (hydatid or hydatid cyst). Characteristically, CE are found in the liver and the lungs, but virtually any part of the body may be affected. Incidence of osseous CE is low, its diagnosis and management is challenging and there is little information published. In this study we report our experience at a referral unit during nearly 30 years in the management of a series of patients with osseous CE. Such information may be useful for other physicians when treating osseous CE.

Citation: Monge-Maillo B, Olmedo Samperio M, Pérez-Molina JA, Norman F, Mejía CR, Tojeiro SC, et al. (2019) Osseous cystic echinococcosis: A case series study at a referral unit in Spain. PLoS Negl Trop Dis 13(2): e0007006. https://doi.org/10.1371/journal.pntd.0007006

Editor: Francesca Tamarozzi, Istituto Superiore di Sanità, ITALY

Received: August 2, 2018; Accepted: November 19, 2018; Published: February 19, 2019

Copyright: © 2019 Monge-Maillo et al. This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All relevant data are within the manuscript and its Supporting Information files.

Funding: The authors received no specific funding for this work.

Competing interests: The authors have declared that no competing interest exist.

Introduction

Echinococcosis occurs in humans as a result of infection by the larval stages of cestodes of the genus Echinococcus [ 1 ]. Four species pose a risk to human health, namely: E . granulosus species complex, (which is subdivided into E . granulosus sensu stricto, Echinococcus felidis , Echinococcus equinus , Echinococcus ortleppi and Echinococcus canadensis ) which causes cystic echinococcosis (CE) and occurs worldwide including tropical and subtropical regions [ 2 ]; E . multilocularis , which causes alveolar echinococcosis and is confined to the northern hemisphere; and E . vogeli which cause neotropical polycystic echinococcosis and E . oligarthrus which cause neotropical unicystic echinococcosis that only occur in Latin America. Several studies have shown that Echinococcosis present an increasing risk to public health and can be regarded as an emerging or re-emerging disease [ 3 ].

In CE, the lifecycle of the parasite involves two hosts: a) the definitive host–generally dogs, although other carnivores such as wolves, dingoes, hyenas can also host this parasite. Adult parasites attach to the mucosa of the small bowel through hooklets and suckers and, from there, ground is shed with the eggs of the parasite through feces. b) The intermediate host–usually a sheep or other herbivores such as goats, horses, camels or pigs, among others–gets infected by the ingestion of ground contaminated with the eggs of the parasite. Once the egg has been ingested, the embryo hatches and penetrates the intestinal mucosa, enters host’s circulatory system and develops in the vesicular metacestode when it finds a suitable anatomical site. This stage of the parasite is a unilocular, fluid-filled cystic lesion (hydatid or hydatid cyst). When the definitive host eats the viscera with the hydatid cyst, the cycle is completed. Humans act as an incidental intermediate host when they become infected with oncospheres through the consumption of water or food contaminated with Echinococcus eggs [ 4 ].

Cystic echinococcosis is present in all continents except for the Antarctica. It primarily occurs in the Mediterranean basin, the Middle East, central Asia, western China, the Russian Federation, Latin America and north and east Africa. The prevalence of CE may exceed 5%, with incidence rates of 50/100 000 person-year in some areas such as South America (mainly Peru and Argentina), east Africa (mainly Kenya) and Asia (mainly China) [ 3 , 5 ].

In Spain, only infections with E . granulosus have been identified. Human CE was a mandatory notifiable disease from 1982 to 1996, being an important anthropo-zoonosis in terms of incidence and morbidity [ 6 ]. In 1985, epidemiological data showed an incidence of CE of 2.5/100,000 per year, with nearly 1000 new cases every year. The incidence of CE progressively decreased from 600–700 new cases per year in the 1980s to 300–500 new cases/year in the 1990s. In 1997, the incidence of CE was 0.78/100,000 per year. This decrease was probably the result of national control programs mainly based on slaughterhouse hygiene, public education and the regular administration of praziquantel to dogs [ 7 ]. However, incidence rates might be underestimated. The reason is that CE stopped being a mandatory notifiable disease in 1996 and, since then, surveillance has been primarily carried out in the autonomous communities where CE is endemic. Underestimation of incidence was shown in an epidemiological study of CE in Spain in the 1997–2012 period based on data from a Centralized Hospital Discharge Database. Incidence rates were found to be higher than the ones reported in previous studies [ 8 ].

Characteristically, CE lesions are found in the liver (70%) and the lungs (20%), but virtually any part of the body may be affected (the spleen, kidneys, heart, central nervous system, or bones). Based on published data, it is estimated that the incidence of bone involvement in CE is 0.5% to 4% of all cases of CE [ 5 ]. Sixty per cent of cases of osseous CE have been reported in Europe (especially in Turkey, Germany and Spain) and the former Soviet Union [ 6 ]. CE usually affects a single bone and the most frequent site of bone lesions is the vertebral column (40%-50%), followed by large bones (25%-30%), the pelvis (15%-20%) and–less frequently–the cranium, sternum, scapula and the phalanges [ 9 , 10 ].

Published literature on the management of osseous CE–a rare manifestation of a neglected disease–is scarce. This article describes the symptoms and management of patients with osseous CE treated in the National Referral Unit of Tropical Diseases in Madrid with long follow-up and compare the results obtained with the ones reported in the literature. The objective of this study is to increase the knowledge on the management and evolution of this neglected tropical disease and to be of use a reference for other physician who have to manage patients with osseous CE.

Ethics statement: As this is a retrospective analysis, data were analyzed anonymously, and written informed consent was not required from patients. The database from which patients’ information was obtained was approved by the Ramón y Cajal Hospital’s Ethics Committee (Comité Ético de Investigación Clínica, CEIC, Hospital Ramón y Cajal) and was used in accordance with current laws in Spain (Ley Orgánica de Protección de Datos de Carácter Personal 15/1999) that guarantee personal data protection.

A retrospective study was performed of patients with osseous CE treated in the National Referral Unit of Tropical Diseases of Ramon y Cajal Hospital of Madrid, Spain between 1989 and December 2017. The data collected included: a) Epidemiological data: age at diagnosis, gender and epidemiological risk factors for CE infection; b) Characteristics of osseous CE: location–categorized as axial skeleton (spinal, ribs and pelvis CE), appendicular skeleton (only limbs) and others–; number of sites involved, and evidence of concomitant CE in other visceral or soft tissues. The Dew/Braithwaite & Lees classification was not included to describe the spinal CE cases because it was not considerate necessary for the purpose of this study. c) Clinical presentation by bone location. d) Diagnostic variables: how the disease was first diagnosed, specific serological test, and the presence (or absence) of eosinophilia. e) Treatment: antiparasitic treatment (drugs administered, duration and toxicity of treatment), surgical treatment and percutaneous treatment. f) Follow-up: mean follow-up, complications after surgery, clinical outcome and sequela.

A total of 104 cases of CE were managed during the study period, of which 27 corresponded to osseous CE (26%).

Epidemiological data

-Sixteen patients were male (59.2%).

-The average age at diagnosis was 36 (IQR 24–62 years) being three patients under 20 years-old.

-All patients had lived in rural regions of Spain for a long time. Yet, exposure was limited to childhood in a case and to summer vacations in the second.

Characteristics of osseous CE

-In total, 44 bone sites were identified in the 27 patients with osseous CE.

-Twelve patients had only a bone involved; another 12 patients had two bones affected, and three patients had three or more bones involved. Therefore, more than half of patients had two or more bones affected by CE. The bones most frequently involved were the spine (17), followed by the ribs (11), pelvis (6), femur (5), tibia (2) and the scapula (1) ( Fig 1 ).

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https://doi.org/10.1371/journal.pntd.0007006.g001

- In the 17 patients with spinal osseous CE, lesions were located in the thoracic spine in eight patients (47%), the thoraco-lumbar spine in three (17.7%), the lumbo-sacrum spine in three (17.7%), the lumbar spine in one (5.8%), the sacrum in one (5.8%), and the thoraco-lumbo-sacral spine in a patient (5.8%).( Fig 2 ).

https://doi.org/10.1371/journal.pntd.0007006.g002

-Twelve of the patients had concomitant extraosseous CE: four in the lungs, two in the liver and six in both, the lung and the liver.

Clinical presentation by bone location

-The most frequent clinical presentation was pain, which was reported in 16 patients (59.2%): seven located in the spine, six in the pelvis, two in the ribs and one in the scapula, followed by medullar syndrome in 10 patients (37%) all located in the spine. A patient had a pathologic fracture (3.7%) in the femur.

Diagnostic variables

-The disease was first diagnosed by radiology (plain X-ray, computed tomography or magnetic resonance) in 18 patients (66.7%), surgery on suspicion of another illness in seven patients (26%), or by a biopsy of the lesion on suspicion of a bone tumor in two patients (7.4%).

-Serology (IHA followed by ELISA) was performed in 17 patients, with heterogeneity of the serology tests employed a long the study period, with 10 (59%) positive results.

-A hemogram was performed to all the patients. Six patients were positive for eosinophilia (22.2%).

Treatment characteristics

-Antiparasitic treatment: of the 27 patients included, 26 received antiparasitic therapy with albendazole 400mg/12 hours. A total of 18 received continuous long-term treatment with albendazole for an average of six years (IQR 0.25 to 16 years). Another seven patients received albendazole discontinuously for long periods. In a patient, treatment with albendazole was interrupted due to side effects. Sixteen (59.3%) patients were administered a combination therapy of albendazole plus praziquantel 600mg/8 hours for an average of five years (IQR 4 months to 15 years). Five patients with spinal involvement received a combination therapy with albendazole plus praziquantel plus nitazoxanide 500mg/12 hours. The duration of this combination therapy was four years in two patients and one year in a patient. Two patients were lost to follow-up and no data were available on the duration of treatment. Despite the long duration of antiparasitic therapy, tolerability was good. In fact, most patients had received antiparasitic drugs (Albendazole +/- Praziquantel) for more than 10 years on average with no side effects. A slight increase in transaminases was reported in seven patients, although treatment discontinuance was not required. Treatment had to be stopped due to side effects in only three patients: a patient developed alopecia and oral ulcers due to albendazole; another patient manifested angioedema under praziquantel treatment; and a patient developed exanthema during nitaxozanide treatment.

-Surgery: Twenty-two patients (81.5%) underwent at least a surgical intervention for osseous CE, none of which was curative. The average number of surgical interventions per patient for osseous CE by body site was: 10.2 (ranging from none to 32 interventions per patient) times for pelvic CE; 3.95 (ranging from 1 to 10 interventions per patient) times for spinal CE, 2.00 times for femur CE, and 1.00 time for rib CE ( Table 1 ). In patients with spinal CE, the most common intervention was laminectomy. Eight patients needed surgical fixation. Total limb amputation was performed in two of the six patients with pelvic CE, and another two needed iliac osteotomy. Patients with femur CE required bone resection and prosthesis.

https://doi.org/10.1371/journal.pntd.0007006.t001

-Percutaneous treatment: the PAIR technique (Puncture, Aspiration, Injection and Re-aspiration) was used in four patients. In three cases, puncture was in patients with CE in soft tissues next to osseous CE sites (two in the spine and one in the ribs). In the fourth patient, PAIR was performed for spinal decompression. Initially, neurological symptoms improved, but the patient ultimately relapsed.

-The average duration of follow-up was more than 20 years. Distribution of duration of follow up was: < 5 years follow up: 4 patients; 5–10 years follow up: 1 patient; 10–20 years follow up: 7 patients; >20 years follow up: 15 patients.

-Twenty-six episodes of complications associated with surgery were reported, being secondary bacterial infection the most frequent (16). A patient had the fixation material broken, another had iliac thrombosis and one died due to probable infectious abscess in the surgical area and respiratory infection three months after surgery ( Table 1 ).

-The most frequent sequels in spinal CE was medullary syndrome (13 patients) and severe pain (3 patients). Two patients with pelvic CE had a limb amputated and another patient developed severe functional disability. In patients with rib CE and femur CE, the most frequent sequel was severe residual pain.

-Despite surgery and long-term antiparasitic treatment, 25 of the 27 (92.6%) patients ultimately relapsed. Recurrence was not reported in two patients. Yet, these patients had been recently diagnosed patients and only had one-year follow-up.

Osseous CE is a rare location of hydatid diseases. In fact, 29 years of study were needed to get 27 cases. However, the prevalence of osseous CE among all cases of hydatid disease in this study was much higher than the one reported in the literature (26% vs 0.5%-4%) [ 11 ]. This may be due to the fact that our center is a referral unit of tropical and parasitological diseases, where less frequent o more complicated infectious diseases are managed.

The average age at diagnosis in our sample was 36 years mostly affecting men. This is consistent with the results of other series, where osseous CE was found to mostly occur in immunocompetent men with a median age of 37 years (peak age of disease is 21–40 years) [ 10 , 12 ].

According to the literature, osseous CE prevailingly invades the spine (45%), pelvis (14%), femur (10%), ribs (8%), humerus (2%), and less frequently other sites as the cranium, sternum, scapula and the phalanges [ 10 , 11 , 13 , 14 ]. This supports our results, except for the fact that, in our study, the ribs were more frequently affected than the pelvis or the femur, being rib involvement generally associated with spine involvement. As reported in the literature, in our series multifocal osseous involvement was prevailingly observed in patients with spinal echinococcosis, being the thoracic and lumbar spine the sites most frequently involved [ 1 ]. In fact, when several bones are affected, spread usually occurs by direct propagation, which would explain that most multifocal osseous sites were associated with spinal and rib involvement.

Osseous CE can remain asymptomatic for long due to its slow growth inside the bones. When symptoms appear, pain is the most frequent followed by pathological fracture, functional impairment or local swelling. Based on our data, nearly 60% of patients presented with pain. However, when the spine is involved, the most common symptoms are those associated with spinal cord compression or vertebral bone destruction [ 1 ] as it was observed in our series, where medullar syndrome was the second most frequent symptom. The symptom of spine CE may vary depending on the localization of the cystic which has been classified on five types (Dew/Braithwaite & Lees classification): type 1, medullar; type 2, intradural; type 3, extradural; type 4, vertebral; and type 5, paravertebral [ 15 , 16 ].

In most of our cases, diagnosis was performed by radiology with computed tomography or magnetic resonance. In patients with epidemiological risk factors, radiological findings are the most common initial signs suggestive of osseous CE. However, differential diagnosis with bone tumor, infection or inflammatory disease is required. Diagnosis based on radiological scanning is challenging, as there are no specific radiological findings for osseous CE. Generally, the most common findings are a single or multiple extensive osteolytic lesion containing trabeculae with cortical thinning. In other cases, pathological fractures with a periosteal reaction or lesions with calcification in neighboring soft tissues due to proximal spread can also be found [ 17 , 18 ]. In the spine, lesions can be described as a “bunch of grapes”. In this case, it is important to determine if there is neurological involvement or not. Initially, lesions are located at the vertebral body, but it can affect the canal, the perirachial space, the ribs or neighboring vertebrae [ 19 ].

Serology was performed in 63% of patients, although different testing techniques were used over the long period of study. This is important, because the sensitivity of serology can vary depending on the serological test employed [ 20 – 23 ]. Yet, the sensitivity of serology also depends on the integrity of CE and its location. In osseous CE, serology may be more sensitive due to the absence of a fibrous capsule and the contiguity of cyst CE to the tissues. Yet, the specific sensitivity of serology in these cases is unknown. In our series, we obtained a 60% sensitivity (taking into account the heterogeneity of the serology tests employed and the localization of osseous CE).

In some cases, uncertainty about diagnosis and the urgent need for differential diagnosis with bone tumors led to a surgical procedure for confirmation of diagnosis. However, except for cases where surgery is a therapeutic option, surgery and also the aspiration of the cyst must be avoided due to the risk for potential local dissemination, sensitization or even anaphylaxis [ 24 ]. Unfortunately, in many cases this cannot be avoided. In our series, 26% of patients underwent surgery on suspicion of another illness, and aspiration for anatomopathological diagnosis was performed in 7.4%.

Regarding therapeutic options, we found that more than 80% of patients underwent surgery, although complete curative results were not achieved. It is known that the only real curative approach for osseous CE is radical resection surgery. Yet, this is rarely possible, especially when the axial bone-spine, the pelvic bone or the femur are affected [ 14 ]. Several interventions are generally required, as observed in our series and in other series previously published [ 10 ]. In long bones, osseous CE can occasionally be completely resected with severe sequels from the potential amputation of the limb [ 25 ]. When osseous CE affects the pelvis, prognosis may depend on whether the coxo-femoral or the sacroiliac joints are affected or not [ 26 ]. When these joints are affected, complete resection may not be possible or cause severe functional disability. In our series, two of the six patients with pelvic CE needed total limb amputation and two required an iliac osteotomy.

In spinal CE, the type of surgery will depend on the location and extent of the disease. The primary purpose of surgery is decompression and stabilization of the spinal cord. Decompression is generally performed by laminectomy [ 27 , 28 ]. In our series, the most common interventions for spinal osseous CE were laminectomy and surgical fixation.

As surgical treatment is challenging, in most cases a combined treatment based on surgery and long-term antiparasitic therapy is the therapy of choice. In our series, apart from surgery, 96% of patients received albendazole. Adjuvant medical therapy can be given preoperatively and/or postoperatively to control the disease locally and prevent systemic spread and recurrence. In other cases, antiparasitic drugs are the only therapeutic option when surgery is not possible or involves severe risk or sequels [ 29 ]. However, there is no consensus on how antiparasitic drugs must be administered, whether therapy must be administered in combination or not, or the duration of treatment. Most authors suggest that when surgery is not curative or osseous CE is inoperable, medical treatment must be lifelong to control cyst growth [ 19 ]. In our series, the duration of therapy in patients who received albendazole was long, with an average of six years, reaching in some cases 16 years of medical treatment.

Albendazole was the first therapeutic option, as recommended in the literature [ 30 ]. The role of praziquantel in CE has not been well defined and there is insufficient data to support a clear recommendation for the use of praziquantel in prolonged chemotherapy [ 31 ]. Praziquantel seems to have a synergistic effect by increasing albendazole plasma levels and there is some evidence to support a role for the use of praziquantel in combination with albendazole during surgery or percutaneous procedures [ 31 – 33 ]. Although there is no consensus on when combination therapy must be administered, it has been given when the patient does not respond to albendazole alone [ 27 ]. In our series, due to the severity of some cases, mainly those suffering from spinal CE, or those with inoperable or non-responding lesions, nearly 60% of our patients received combination therapy of albendazole plus praziquantel.

Five patients with spinal osseous CE were treated with albendazole plus praziquantel plus nitazoxanide. Nitazoxanide has shown to be active in vitro and in vivo against E . multilocularis and E . granulosus . Yet, its possible effectiveness seems to be better when it is given in combination with other antiparasitic drugs reporting best results for nitazoxanide in combination with albendazole [ 34 – 36 ]. Our data on osseous CE and disseminated CE have been published elsewhere. We found that the combination of nitazoxanide with albendazole +/- praziquantel is effective for disseminated CE involving soft tissue, muscle or viscera. However, this combination therapy was not effective for chronic and extensive osseous lesions [ 37 ].

Patients with osseous CE require long-term follow-up for potential recurrence and possible complications or sequels associated with surgery or antiparasitic therapy [ 10 ]. Because a curative therapy is rarely feasible, follow-up is lifelong. In our series, the average duration of follow-up exceeded 20 years, and during that time nearly 93% of patients relapsed. Surveillance must be based on clinical data and radiology. As recurrence cannot be confirmed by serology, it is not used for follow-up [ 4 ]. The most common sequels reported in our series were medullary syndrome and severe pain in spinal CE. In pelvic CE, limb amputations and other severe functional disabilities were described. In patients with rib CE and femur CE, the most frequent sequel was severe pain. This is consistent with the literature, where persistent pain, fractures, paraplegia in spine CE or even death due to progression of the disease have been reported as frequent sequels and complications of osseous CE [ 10 ].

A strength of this study is that it includes patients with long-term follow-up. This offers a global vision of the evolution of osseous CE over time. However, the low incidence of osseous CE and the heterogeneity of cyst sites make it difficult to establish a diagnostic or therapeutic protocol based on our results. One possible limitation of this series is that it may provide information only about those most complicated cases of osseous CE, which are more frequently refereed to reference units.

This article reports experience with the management of osseous CE in a referral unit of tropical and parasitic diseases in Spain. Fortunately, the incidence of osseous CE is low, but its diagnosis and management is highly challenging. Diagnosis must be based on a combination of indicators based on clinical symptoms, radiological findings and serological results. In most cases, osseous CE must be considered a chronic disease, since complete surgical resection is unlikely and antiparasitic drugs are rarely curative. The absence of protocols for the management of this disease and its low prevalence force physicians to approach the disease on a case-by-case basis. Additionally, osseous CE requires long-term follow-up for recurrence and possible sequels.

Supporting information

S1 table. locations of osseous cystic echinococcosis based on a single or multiple bones affected..

https://doi.org/10.1371/journal.pntd.0007006.s001

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• Published: 19 June 2020

Human cystic echinococcosis in southwest Iran: a 15-year retrospective epidemiological study of hospitalized cases

• Reza Shahriarirad 1 , 2 ,
• Amirhossein Erfani 1 , 2 ,
• Mehrdad Eskandarisani 1 ,
• Mohammad Rastegarian 1 ,
• Hajar Taghizadeh 1 &
• Bahador Sarkari   ORCID: orcid.org/0000-0003-2045-9057 3 , 4  

Tropical Medicine and Health volume  48 , Article number:  49 ( 2020 ) Cite this article

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Cystic echinococcosis (CE) is considered as a neglected disease with significant mortality and morbidity in most of the developing countries. The current study aimed to retrospectively assess the demographic and epidemiologic features of human CE surgical cases in a 15-year period in Fars province, southwestern Iran.

A 15-year (2004–2018) retrospective study was conducted to find out the epidemiological and clinical picture of CE in patients who undergone surgeries for CE in two main hospitals in Fars Province, southwestern Iran. Hospital records were reviewed, and data were retrieved from each CE patient’s record.

A total of 501 CE surgical cases were recorded during a 15-year period, corresponding to an average annual incidence of 33.4 and a surgical incidence rate of 0.74/100,000 population. Of these, 242 (48.6%) were male, and 256 (52.4%) were female. Patients’ age ranged from 2 to 96 years, with a mean age of 34.92 (± 19.87) years. A significantly higher rate of CE cases was noted in subject’s ≥ 50 years of age. The highest frequency of cases (62:12.5%) was recorded in the year 2017. The most commonly involved organs were liver (339 cases; 57.8%) and lung (279 cases; 47.6%). Concurrent involvement of two organs was seen in 58 (9.9%) cases of both lung and liver, 10 (1.6%) cases of lung and other locations (but not liver), and 23 (3.9%) cases of liver and other locations (but not lung). Reoperation was noted in 67 (13.4%) of the cases. The size of the lung hydatid cyst varied, ranging between 2 and 24 cm (mean = 7.33, SD = 3.737). The size of liver hydatid cysts ranged from 1 to 26 cm (mean 9.04, SD = 4.275).

The findings of the current study demonstrated a nearly constant prevalence of CE during the last 15 years in southern Iran. Further studies are needed to find out the reasons behind the recurrence of the disease, which is substantial, in surgically-treated patients.

Cystic echinococcosis (CE), due to Echinococcus granulosus , is one of the most significant zoonotic diseases, throughout most parts of the world [ 1 ]. Herbivores such as sheep, goats, and swine are intermediate hosts of E. granulosus , which become infected by eating the worm eggs passed in the carnivores’ feces. Carnivores, as definitive hosts, ingest the cyst-containing organs of herbivores and harbor worms in their digestive system [ 2 ]. Humans become infected via ingesting embryonated eggs through hands, water, or food contaminated with parasite eggs that passed through the feces of definitive hosts. The oncospheres spread through blood and lymphatic circulation to the liver, the lungs, and other organs, where the development of the Echinococcus cysts occurs.

Cystic echinococcosis is asymptomatic at the early phases of the infection; however, it becomes symptomatic when the cysts become larger or complicated. Clinical manifestations of CE vary based on the size, location, and condition of the cystic structure [ 3 ].

CE is considered a neglected disease with significant mortality and morbidity in most of the developing countries [1, 4, 5 ]. The disease is a major health and economic challenges in the Middle East countries, including Iran where about 1% of all hospital surgeries are accounted for this disease [ 1 , 4 , 5 ]. A recent systematic review and meta-analysis reported the overall seroprevalence of CE in Iran to be 4.2% in human hosts, with the highest seroprevalence (5.8%) in the South and the least (2.2%) in the central areas of the country [ 6 ].

CE is more frequently occurring in rural and nomadic communities where people have continuous contact with dogs, the definitive host of E. granulosus . Studies in both West and East Azerbaijan and Hamedan provinces in Iran demonstrated that rural residents constitute the most common referral cases of CE [ 7 , 8 , 9 ].

CE is one of the most important parasitic diseases in Fars province in the southwest of Iran [ 5 , 10 ]. Fars province is the center of agriculture and animal husbandry in Iran and one of the most important and populated tribal nomads (Qashqai) resides in this area. The burden and incidence of CE which are the basis for the development of appropriate control programs are poorly known in Fars province, in southwestern Iran. Hence, the current study was designed and conducted to assess the demographic and epidemiological features of CE during a 15-year period in the south of Iran, based on the hospital records.

This study was conducted in Fars Province in southwestern Iran. The district is located at an altitude of 1545 m above the sea level at geographical coordinates of 29° 36′ 37″ N latitude and 52° 31′ 52″ E longitudes. The area has a hot summer and moderate winter. Agriculture has always been a major part of the economy in Fars province. The province has a population of 4.6 million.

Data collection

In this retrospective study, hospital records of CE patients were reviewed, and data were retrieved for a 15-year period, from 2004 to 2018 at the main university–affiliated and referral hospitals (Nemazi and Shahid Faghihi) in Shiraz, capital of Fars Province.

Hydatid cyst diagnosis was based on histopathological confirmation after the surgery. Moreover, those patients in which the CE was initially diagnosed by imaging findings and confirmed at surgery, and those with negative histopathological findings (although rare), but characteristic imaging findings and with a positive serology test (mainly CCIEP: Counter Current Immunoelectrophoresis) were considered and recorded as CE cases.

Only cases with a final diagnosis of any type of CE at hospital discharge which were recorded with a unique disease code (based on the ICD-9 and ICD-10: International Classification of Diseases; 122.9, and 122.8 for ICD9; B67.8, K77.0, B67.9, and J99.8 for ICD10) were included in the data analysis. Suspected cases were not included in the study.

From each patients’ hospital record, demographical data (age, sex, place of residence, etc.), history of the previous CE, hydatid cyst features (size, location, multiple organ involvement), treatment measurement (the type of surgery, drug therapy, recurrence), and duration of hospital stay were collected in a data sheet.

The hospital records for a few years of the study were not available in the hospital database. Therefore, the medical records were searched manually by members of the research team which consisted of physicians as well as medical students.

Statistical analysis

All the statistical analyses were performed by using statistical package for social sciences (SPSS Inc., Chicago, Illinois, USA) version 22.0. A descriptive analysis was performed on the demographics characteristics. Categorical and continuous data were reported as proportions and means ± SDs. Chi-square or Fisher’s exact test was used to test the differences between the categorical variables.

A total of 501 CE surgical cases were diagnosed and underwent surgery in two main hospitals in the 15-year period from 2004 to 2018, giving an average annual incidence of 33.4 cases and an annual incidence rate of 0.74 per 100,000 population. The mean age of the patients was 34.92 (± 19.87) years. The youngest patient was a 2-year-old girl, and the oldest one was a 96-year-old man. Of the total number of patients, 26% were ≥ 50 years old. Out of 501 CE cases, 242 (48.6%) were male while 256 (51.4%) were female. Furthermore, based on the gender of the patients, the median age of male cases was 30 years [IQR 14–48], (mean = 32.79, SD = 20.37), while for female, the median was 35 years [IQR 22–53] (mean = 36.77, SD = 19.31). The highest frequency of cases (62, 12.5%) was recorded in the year 2017. Figure 1 shows the frequency of CE cases, per year in the current study.

Frequency of CE cases per year, during 2004–2018 in Fars province, southwest Iran

Considering the residential areas of the patients, the majority of cases (76%) originating from Fars Province, whereas cases from neighboring Provinces mainly Kohgiluyeh and Boyer-Ahmad (7%) and Bushehr (4.4%), were also among the patients.

The median duration of hospital stay for patients was 7.5 days [IQR 5–13]. The most commonly involved organs were liver (339 cases; 57.8%), and lung (279 cases; 47.6%). Also, 46 (7.8%) cases had hydatid cyst in other locations including spleen, heart, and diaphragm. Among the lung hydatid cyst cases, 126 (64.9%) were located in the right lung while 103 (59.5%) were located in the left lung. Also, regarding the liver hydatid cysts, 193 (47.1%) of cases had cyst in the right lobe while 76 (18.9%) had cyst in the left lobe. Concurrent involvement of two organs was seen in 58 (9.9%) cases of both lung and liver, 10 (1.7%) cases of lung and other locations (excluding liver), and 22 (3.8%) cases of liver and other locations (excluding lung). Table 1 shows the location of hydatid cyst in CE cases in southwest Iran.

Multiple organ involvements of lung, liver, and spleen were seen in 2 (0.3%) cases, lung, liver and pelvic cavity in 1 (0.2%) case, lung liver, and sub-diaphragm in 1 (0.2%) case, and lung, liver, and pancreas in 1 (0.2%) case.

Secondary hydatid cyst or relapse was seen in 67 (13.37%) of the patients, in which the secondary cysts in 28 (41.8%) were lung cysts, 42 (62.7%) were liver cyst, 1 (1.5%) was pelvic cyst, 1 (1.5%) was spleen cyst, 1 (1.5%) was abdominal and peritoneal cavity, and 1 (1.5%) was in the mesothelium of the terminal ileum. It is worth mentioning that 11 of the cases underwent surgery due to tertiary hydatid cyst or relapse for the third time and also 3 of the cases underwent a fourth surgery due to hydatid cyst. Table 2 shows the demographic features of the CE patients along with the cyst features.

From the 279 cases of lung hydatid cyst, the majority (174: 74%) had a single cyst while 46 (19.6%) cases had two, and 15 (6.4%) cases had three or more cysts. It is worth knowing that from the 279 cases of lung hydatid cyst, 157 (56.3%) cases were male while 120 (43.3%) were female. There was a significant correlation between lung hydatid cysts and the patients’ gender ( P < 0.001). The size of the lung hydatid cyst varied, ranging between 2 and 24 cm (mean = 7.33, SD = 3.737) with the highest frequency (175, 96.2%) of the largest diameter of the cyst being in group 11 to 15 cm. The lung cyst area ranging from 2 to 490 cm 2 (mean 42.27, SD = 50.061) with the majority in under 26 cm 2 group (83:48.3%).

In our study, among the 339 cases of liver hydatid cyst, 194 (68.1%) had single cysts, 56 (19.6%) had two cysts, and 35 (12.3%) had three or more cysts. The size of liver hydatid cysts ranged from 1 to 26 cm (mean 9.04, SD = 4.275) with the highest frequency of the largest diameter of the cyst being in group 6 to 10 cm. The area square centimeters of the liver cyst ranged from 1 to 392 cm 2 (mean = 58.43, SD = 52.556) with the majority (82: 31.9%) in under 26 cm 2 group.

In other locations, apart from the lung and liver, the numbers of cysts varied were 21 (3.6%) cases had only a single cyst, 7 (1.2%) cases had two cysts, and 8 (1.4%) cases had three or more. The size of the cysts varied, ranging between 2 and 18 cm (mean = 8.73, SD = 4.527) with the highest frequency (19: 55.9%) being in the 6 to 10 cm group. The area square centimeters of the cysts in other locations ranged between 3 and 314cm 2 (mean = 59.14, SD = 64.287). Based on the surgical intervention for the patients, 142 (28.3%) underwent radical surgery while 360 (71.9%) underwent conservative surgery. Regarding the medications administered for the patients, 284 (56.6%) patients received anti-helminthic drugs, including albendazole in 282 (56.2%) and mebendazole in 5 (1%) cases.

CE is a zoonotic parasitic infection that occurs all over the world and causes substantial public health problems and economic losses. The Middle East is considered as the hot spot of CE in the world [ 1 , 10 ]. CE is endemic and highly prevalent in Iran where human cases have been reported from nearly every province in the country [ 5 , 10 , 11 , 12 ]. The incidence rate of CE in Iran has been reported to be 1.3–3/100,000 population. Our study demonstrated a surgical incidence of 0.74/100,000 inhabitants for CE in southern Iran. It should be noted that the 1.3–3/100,000 incidence of CE has been considered for all CE cases in Iran while our study only included cases that underwent surgery. This means that the total numbers of admitted cases (both surgical and non-surgical cases) in our center could be higher.

A higher rate of CE incidence (4.5 cases/100,000/year) has been reported in neighboring Iraq [ 13 ]. An incidence of 0.87 to 6.6 per 100,000 inhabitants has been reported for CE in Turkey [ 14 ]. A retrospective analysis of CE in Aydın Adnan Menderes University training and research hospital in Turkey, from 2005 to 2017, reported 247 pathologically confirmed cases [ 15 ]. In Pakistan, data regarding human CE is limited [ 16 ]. A retrospective study of hospital records from five major metropolitan cities of Pakistan reported 188 surgically confirmed cases of CE corresponding to an annual frequency of 18.8 cases/year [ 17 ]. Another retrospective study in Northeastern Punjab Province reported a total of 198 cases of CE during a 6-year period (2012–2017) [ 18 ].

Although cases of CE are being reported from all the 31 provinces of Iran, the disease is more prevalent in sheep-breeding areas, including Fars province in the south of the country. The present study describes a detailed status of the geographical distribution as well as the epidemiological features of CE in southern Iran through retrospective reviewing of the patients’ hospital records during a 15-year period. The annual surgical cases of CE were found to be 33.5 cases. It should be noted that some of the CE patients may seek treatment in local hospitals, where sufficient equipment are available for CE operation. It is also worth mentioning that there is a tendency by most surgeons to manage the CE by using a kind of “watch and wait” policy or chemotherapy instead of surgery and only the complicated cases undergoing operations. This again results in a decreased number of patients who undergo surgeries and decrease the number of CE hospital records. With these in mind, the actual annual prevalence rate of CE would be higher in the study area.

CE is reported to have a higher prevalence rate in women than in men in Iran which can be due to the household activities of women that are traditionally a part of their daily routine life [ 7 , 19 ]. This finding is in line with our previous study and also a retrospective hospital-based study by Abdulhameed in Basrah, Iraq, a neighboring country to Iran, where females were reported to be the main victims of CE [ 13 , 20 ]. Previous studies suggested that women have the highest chance of contact with sources of infection such as dogs, soil, and vegetable [ 5 , 21 , 22 ]. Housewives, particularly in rural areas, where the disease is more prevalent, have the highest chance of contact with the sources of infection. However, in studies of Cohen et al. [ 23 ] and Qaqish et al. [ 24 ], such associations were not observed.

In this regard, a meta-analysis by Khalkhali et al. on the prevalence of hydatid cysts in Iran found that although the rate of infection with hydatid cysts was higher in females than males, the difference was not statistically significant [ 6 ]. Thus, in some areas, a greater frequency of CE in males may be seen [ 25 , 26 , 27 ].

In our study, the majority of CE cases were ≥ 50 years old. This is mainly because CE is a slow-growing cyst in humans and usually presents the signs and symptoms at a higher age of life, whereas the infection may occur in younger people or even teenagers. The fact that all age groups, including children and young adults, were well represented in the confirmed CE cases and suggest that both adults and children are susceptible to infection, as previously documented [ 5 , 28 ]. In accordance with the available evidence, CE in Iran has no privilege for age. In a study by Moldovan et al., a total of 190 CE cases in two counties of Romania were reviewed and revealed the highest rate of infection in 60–69 years old patients [ 29 ].

CE is not uncommon in young children as 51 (10.16%) of cases in our study were children under 10 years old. In line with our findings, a retrospective study regarding CE cases in children in one of the hospitals in the south of Iran reported 57 children with CE during a 12-year period, 2003–2014 [ 28 ].

Findings of the present study further documented that hydatid cyst occurs predominantly in the liver and lung and occasionally in the heart, spleen, abdomen, and pelvis. Moreover, the lungs are predominantly infected with hydatid cyst other than any organ possibly due to the presence of greater capillary beds in the lungs in comparison with other organs [ 30 , 31 , 32 ].

In the present study, data about the WHO ultrasound classification of the hydatid cysts were not available in the patients’ hospital records. Such data are very important for management as well as follow-up of patients. With the establishment of a regular registration system, such information would be included by radiologists to the patients’ hospital records.

The retrospective hospital surveys have been generally criticized for not providing precise estimates of the disease incidence as not all hospitals in a particular region or district are included in the study. Besides, retrospective hospital survey data on human CE cannot give an accurate picture of the prevalence of the infection. A certain number of cases are not observed in hospital records since the infection is asymptomatic or does not need surgical intervention. Besides, some data are not available in the hospital records. Yet, the hospital records can indicate the public health importance of the disease and, when done constantly over many years, can detect regional variations in the incidence of the infection [ 33 ]. More importantly, establishing a registered database for documenting cases of CE in endemic areas such as Iran is essential to reach a better understanding of the prevalence and extent of the disease. Such a system has recently been launched in a few provinces in Iran. Moreover, Iran and Turkey have recently joined the European Register of CE.

Taken together, findings of the current study revealed that human CE is a common infectious disease in the southwest of Iran with a relatively constant rate during the last 15-year period of evaluation. A health education program to increase awareness of how CE is transmitted, along with regular surveillance of the disease, would help to reduce the infection rate in this area of Iran. Moreover, the burden of disease in the investigated area would justify starting a well-organized control program as CE is a preventable disease.

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Acknowledgements

The technical assistant of staff in Nemazi and Faghihi hospitals is acknowledged.

The study was financially supported by the office of vice-chancellor for research of Shiraz University of Medical Sciences (Grant No. 94-01-01-9212).

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Reza Shahriarirad, Amirhossein Erfani, Mehrdad Eskandarisani, Mohammad Rastegarian & Hajar Taghizadeh

Thoracic and Vascular Surgery Research Center, Shiraz University of Medical Sciences, Shiraz, Iran

Reza Shahriarirad & Amirhossein Erfani

Department of Parasitology and Mycology, School of Medicine, Shiraz University of Medical Sciences, Shiraz, Iran

Bahador Sarkari

Basic Sciences in Infectious Diseases Research Center, Shiraz University of Medical Sciences, Shiraz, Iran

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BS and RS designed the study. RS, AE, ME, MR, and HT collected the data. BS, RS, MR, and AE carried out the statistical analysis and helped with manuscript writing. RS and AE drafted the manuscript. BS revised and proofread the manuscript. All authors read and approved the final version of the manuscript.

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Shahriarirad, R., Erfani, A., Eskandarisani, M. et al. Human cystic echinococcosis in southwest Iran: a 15-year retrospective epidemiological study of hospitalized cases. Trop Med Health 48 , 49 (2020). https://doi.org/10.1186/s41182-020-00238-3

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6 in 10 U.S. Catholics are in favor of abortion rights, Pew Research report finds

Jason DeRose

Pope Francis remains popular among U.S. Catholics, with 75% having favorable views of him, according to a Pew Research report. But many self-identified Catholics disagree with various teachings of their church. Andrew Medichini/AP hide caption

Pope Francis remains popular among U.S. Catholics, with 75% having favorable views of him, according to a Pew Research report. But many self-identified Catholics disagree with various teachings of their church.

Catholics in the U.S., one of the country's largest single Christian groups, hold far more diverse views on abortion rights than the official teaching of their church.

While the Catholic Church itself holds that abortion is wrong and should not be legal, 6 in 10 U.S. adult Catholics say abortion should be legal in all or most cases, according to a newly released profile of Catholicism by Pew Research .

Catholic opinion about abortion rights, according to the report, tends to align with political leanings: Fewer Catholic Republicans favor legal abortion than Catholic Democrats. And Pew says Hispanic Catholics, who make up one-third of the U.S. church, are slightly more in favor of legal abortion than white Catholics.

Despite church prohibitions, Catholics still choose IVF to have children

Pew found that 20% of the U.S. population identifies as Catholic, but only about 3 in 10 say they attend mass regularly. Opinions about abortion rights appear to be related to how often someone worships — just 34% of Catholics who attend mass weekly say abortion should be legal in all or most cases, whereas that number jumps to 68% among those who attend mass monthly or less.

Most U.S. Catholics are white (57%), but that number has dropped by 8 percentage points since 2007, according the new report. About 33% identify as Hispanic, 4% Asian, 2% Black, and 3% describe themselves as another race.

Pew Research also found that as of February, Pope Francis remains highly popular, with 75% of U.S. Catholics rating him favorably. However, there is a partisan divide, with Catholic Democrats more strongly supporting him.

About 4 in 10 U.S. Catholics view Francis as a major agent of change, with 3 in 10 saying he is a minor agent of change.

Catholic Church works to explain what same-sex blessings are and are not

Pew reports that many U.S. Catholics would welcome more change. Some 83% say they want the church to allow the use of contraception, 69% say priests should be allowed to get married, 64% say women should be allowed to become priests, and 54% say the Catholic Church should recognize same-sex marriage.

In December 2023, the Vatican issued guidance to priests that they may bless people in same-sex relationships. But the church insists those blessings not be construed in any way to be a form of marriage or even take place as part of a worship service.

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On this page, cystic echinococcosis, alveolar echinococcosis.

The diagnosis of E. granulosus infection (cystic hydatid disease) is suggested by identification of a cyst-like mass in a person with a history of exposure to sheepdogs in areas where the parasite is endemic. Cystic echinococcosis must be differentiated from benign cysts, cavitary tuberculosis, mycoses, abscesses, and benign or malignant neoplasms. Noninvasive imaging techniques such as CT scans, MRI, and ultrasound imaging are all used for detecting and defining the extent and condition of avascular fluid-filled cysts in most organs. These techniques have proved valuable for diagnosis and preoperative evaluation by staging the condition of the lesion, the extent of the lesion in reference to other organs and vital structures, and identifying the presence of additional occult lesions. Radiography permits the detection of hydatid cysts in the lungs; however, in other organ sites, calcification is necessary for visualization. Ultrasonography has been widely used for screening, clinical diagnosis, and monitoring of treatment of liver and intra-abdominal cysts. Cyst viability cannot be reliably determined with radiography or parasite antigen detection; calcification can be present in all stages of cysts.

Serologic tests, such as enzyme-linked immunosorbent assay (ELISA) and indirect hemagglutination test, are highly sensitive methods for detecting infection. Specific confirmation can be obtained by demonstrating echinococcal antigens by immunodiffusion (arc 5) procedures or immunoblot assays (8-, 21 –kD bands).

Alveolar echinococcosis closely mimics hepatic carcinoma or cirrhosis and is more commonly diagnosed in people of an advanced age. Plain radiographs show hepatomegaly and characteristic scattered areas of radiolucency outlined by calcific rings 2 to 4 mm in diameter. The usual CT image of E. multilocularis infection is that of indistinct solid tumors with central necrotic areas and perinecrotic plaque-like calcifications. Serologic test results are usually positive at high titers. Comparing a patient’s titers with both purified-specific and shared antigens permits the serologic discrimination between patients infected with E. multilocularis and those infected with E. granulosus .

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The incubation period of cystic echinococcosis is often prolonged for several years and most cases of cystic echinococcosis remain asymptomatic until the cysts reach a large enough size to cause dysfunction. Most primary infections in humans consist of a single cyst. The liver is the most common site of the hydatid cysts, followed by the lungs. Cysts in the spleen, kidneys, heart, bone and central nervous system are less common. In secondary echinococcosis, larval tissue spreads from the primary site and new cysts develop after spontaneous or trauma-induced cyst rupture or after release of viable parasite material during invasive treatment procedures.

Signs and symptoms may include hepatic enlargement with or without a palpable mass in the right upper quadrant, right epigastric pain, nausea, and vomiting. Rupture or leakage usually results in acute or intermittent allergic manifestations.

The primary infection of alveolar echinococcosis is in the liver, usually the right lobe, but direct extension to contiguous organs, as well as hematogenous metastases to the lungs and brain is not uncommon. Alveolar echinococcosis is inhibited by the host from completing its development and remains in the proliferative stage indefinitely. The larval mass resembles a malignancy in appearance and behavior. In chronic alveolar hydatid infections, the lesion consists of a central necrotic cavity filled with a white amorphous material that is covered with a thin peripheral layer of dense fibrous tissue. Host tissue is directly invaded by extension of the budding and proliferating cyst wall, causing a pressure necrosis of surrounding host tissue. A vigorous inflammatory and fibrous tissue reaction usually surrounds the larval mass. Diagnosis is often delayed until an advanced and inoperable stage; mortality rates have traditionally been high, ranging between 50% and 75%.

In the past, surgery was the only treatment for cystic echinococcal cysts. Chemotherapy, cyst puncture, and PAIR (percutaneous aspiration, injection of chemicals and reaspiration) have been used to replace surgery as effective treatments for cystic echinococcosis and, for some cases, no treatment but a conservative “watch and wait” approach is best. Treatment indications vary with cyst characteristics, including cyst type, location, size, and complications. Surgery may be the best treatment for liver cysts that are secondarily infected or cysts located in the brain, lungs, or kidney. Liver cysts larger than 7.5 cm are likely to have biliary communication; surgery may be the best option for these cysts. Many abdominal cysts can be treated by injection of protoscolicidal chemical solutions into the cyst, followed by evacuation, prior to further manipulations and extirpation of cysts.

For some patients, chemotherapy with benzimidazoles is the preferred treatment. Patients with small cysts or multiple cysts in several organs can be treated successfully with albendazole. Approximately one third of patients treated with chemotherapy with benzimidazole drugs have been cured of the disease and even higher proportions, between 30-50%, have responded with significant regression of the cyst size and alleviation of symptoms. Both albendazole 10 to 15 mg/kg body weight per day (max 800 mg orally in two doses) and, as a second choice for treatment, mebendazole 40-50 mg/kg body weight per day continuously for several months have been highly effective. Additionally, chemotherapy can be very effective when used in conjunction with surgery. Albendazole has been administered to patients prior to surgery for the intended purpose of facilitating the safe surgical manipulation of the cysts by inactivating protoscolices, altering the integrity of the cysts membranes, and reducing the turgidity of the cysts. A third treatment option, PAIR (percutaneous aspiration, injection of chemicals and reaspiration), has been shown to be effective. This option is indicated for patients with relapse after surgery, failure of chemotherapy alone, or who refuse surgery.

*Praziquantel may be useful preoperatively or in case of spillage of cyst contents during surgery (Bygott JM, Chiodini PL. Acta Tropica 2009; 111: 95-101).

* Oral albendazole is available for human use in the United States.

* Oral mebendazole is available for human use in the United States.

Alveolar echinococcosis requires chemotherapy with or without surgery; radical surgery is the preferred approach in suitable cases. Effective treatment involves benzimidazoles administered continuously for at least 2 years and patient monitoring for 10 years or more since recurrence is possible. This has inhibited progression of alveolar echinococcosis and reduced lesion size in approximately half of treated cases. Intermittent treatment with albendazole is not recommended.

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This information is provided as an informational resource for licensed health care providers as guidance only. It is not intended as a substitute for professional judgment.

Albendazole

Albendazole is pregnancy category C. Data on the use of albendazole in pregnant women are limited, though the available evidence suggests no difference in congenital abnormalities in the children of women who were accidentally treated with albendazole during mass prevention campaigns compared with those who were not. In mass prevention campaigns for which the World Health Organization (WHO) has determined that the benefit of treatment outweighs the risk, WHO allows use of albendazole in the 2nd and 3rd trimesters of pregnancy. However, the risk of treatment in pregnant women who are known to have an infection needs to be balanced with the risk of disease progression in the absence of treatment.

Pregnancy Category C: Either studies in animals have revealed adverse effects on the fetus (teratogenic or embryocidal, or other) and there are no controlled studies in women or studies in women and animals are not available. Drugs should be given only if the potential benefit justifies the potential risk to the fetus.

It is not known whether albendazole is excreted in human milk. Albendazole should be used with caution in breastfeeding women.

The safety of albendazole in children less than 6 years old is not certain. Studies of the use of albendazole in children as young as one year old suggest that its use is safe. According to WHO guidelines for mass prevention campaigns, albendazole can be used in children as young as 1 year old. Many children less than 6 years old have been treated in these campaigns with albendazole, albeit at a reduced dose.

Mebendazole

Mebendazole is in pregnancy category C. Data on the use of mebendazole in pregnant women are limited. The available evidence suggests no difference in congenital anomalies in the children of women who were treated with mebendazole during mass treatment programs compared with those who were not. In mass treatment programs for which the World Health Organization (WHO) has determined that the benefit of treatment outweighs the risk, WHO allows use of mebendazole in the 2nd and 3rd trimesters of pregnancy. The risk of treatment in pregnant women who are known to have an infection needs to be balanced with the risk of disease progression in the absence of treatment.

It is not known whether mebendazole is excreted in breast milk. The WHO classifies mebendazole as compatible with breastfeeding and allows the use of mebendazole in lactating women.

The safety of mebendazole in children has not been established. There is limited data in children age 2 years and younger. Mebendazole is listed as an intestinal antihelminthic medicine on the WHO Model List of Essential Medicines for Children, intended for the use of children up to 12 years of age.

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For Filmmakers, O.J. Simpson’s Trial Was a Powerful Case Study

In 2016, both an FX mini-series and an ESPN documentary re-examined the polarizing criminal accusations against Simpson and the nation’s divided conversation about race.

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By Emmanuel Morgan

More than 20 years after the O.J. Simpson trial, long after the headlines had faded and the news cycle had moved on to other scandals, the polarizing saga was thrust back into the national conversation thanks to two very different projects.

“ The People v. O.J. Simpson: American Crime Story ,” an FX mini-series directed by Ryan Murphy, won nine Emmys in 2016. That year’s “ O.J.: Made in America, ” a nearly eight-hour film for ESPN, won the Academy Award for best documentary feature.

“It was a story that combined everything that obsesses the American people,” the legal analyst Jeffrey Toobin said the day after Simpson died at 76 . Toobin’s 1996 book, “The Run of His Life: The People v. O.J. Simpson,” inspired the FX series.

Toobin said the Simpson odyssey captivated the country’s psyche. There was love, violence, sports and Hollywood. Even a fugitive on the run.

Simpson had been a star football player , winning the Heisman Trophy in college and the Most Valuable Player Award in the N.F.L. But for many people, his athletic highlights are overshadowed by a highway chase involving a white Ford Bronco and murder charges in the 1994 deaths of his ex-wife Nicole Brown Simpson and her friend Ronald L. Goldman.

As Americans followed the nine-month trial, their perception of the criminal case against Simpson, a prominent Black athlete who became an actor and a pitchman , was often split along racial lines. Simpson was acquitted in the criminal case and was later found liable for the deaths in a civil trial .

“I think the reason it still feels so raw is that it still feels like it’s today,” said Larry Karaszewski, a screenwriter for the FX mini-series. “A lot of times people think we’re at this post-racial moment, but it keeps coming back.”

Karaszewski said that like during Simpson’s trial, race was at the forefront of the national conversation when “The People v. O.J. Simpson” was being produced, during the rise of the Black Lives Matter movement after the fatal shooting of Trayvon Martin by a neighborhood watchman in 2012.

The mini-series focused on the Simpson trial, treating him as a secondary character while highlighting other key players in the courtroom , like Marcia Clark, the lead prosecutor, and Johnnie Cochran, one of Simpson’s prominent defense lawyers.

In contrast, ESPN’s documentary, an installment of the sports network’s “30 for 30” series, traced Simpson’s biography and contextualized it through the sports and socioeconomic history of the Los Angeles region. Its director, Ezra Edelman, has said he thought it was important to take that wider view.

“I was interested in the 30 years before the murders, the city, race and identity, and the juxtaposition with O.J.’s story,” he told The New York Times in 2016 . “This is a big American studies paper. This touches on everything in our culture.”

Through an ESPN spokeswoman, Edelman declined to comment after Simpson’s death. Several of the documentary’s producers did not respond to requests for comment.

Karaszewski said the distance from the trial allowed viewers of the FX series to watch the case with fresh eyes, without the emotional response to the verdict. And he and Toobin agreed that it also presented the saga and its characters — including Robert Kardashian, a defense lawyer whose family’s fame grew after the case — to new audiences.

“For those of us who lived through it, it brought it back up,” Toobin said, “but it introduced a whole generation of people who had no firsthand experience with the story.”

Emmanuel Morgan reports on sports, pop culture and entertainment. More about Emmanuel Morgan

Study: COVID-19 Vaccine Not Linked to Sudden Cardiac Death Among Young People

Cases of myocarditis and pericarditis have rarely been observed after COVID-19 vaccination. The CDC says the benefits of the COVID-19 vaccine outweigh any known risks.

No Link: COVID Vax, Sudden Cardiac Death

Lynne Sladky | AP-File

A healthcare worker fills a syringe with the Pfizer COVID-19 vaccine at Jackson Memorial Hospital, Oct. 5, 2021, in Miami.

The COVID-19 vaccine is not linked to sudden cardiac death among previously healthy young people, according to a new study published by the Centers for Disease Control and Prevention.

Investigators at the Oregon Health Authority looked at death certificate data for people ages 16-30 from June 2021 to December 2022 with cardiac or undetermined causes of death listed. They identified 40 deaths among people who received either the Pfizer or Moderna COVID-19 vaccine.

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Of those 40, three deaths occurred within 100 days of vaccination, with two in people who had underlying illness and one whose cause of death was undetermined. No death certificate attributed death to vaccination, according to the study .

“The data do not support an association of COVID-19 vaccination with sudden cardiac death among previously healthy young persons,” the researchers wrote.

The CDC has stated that cases of myocarditis and pericarditis – inflammation of the heart muscle and the lining outside the heart, respectively – have rarely been observed after COVID-19 vaccination. It’s more common among young males within a week of receiving the second shot. Most patients respond well to medicine and recover quickly.

The CDC maintains that the benefits of the COVID-19 vaccine outweigh any known risks.

The incorrect idea that COVID-19 vaccines are linked to death in young people gained immense attention on social media from conspiracy theorists with the hashtag #diedsuddenly. Certain events in real life, including Buffalo Bills player Damar Hamlin's cardiac arrest, offered fuel for speculation without evidence.

The CDC and other public health officials faced an uphill battle during the pandemic to convince people the COVID-19 vaccine was safe as public figures like Elon Musk, Joe Rogan and Robert F. Kennedy Jr. spread skepticism .

Still, more than 81% of all adults got at least one COVID-19 vaccine, according to CDC data .

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Tags: Coronavirus , CDC , vaccines , pandemic , public health , death

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Case Study: How Aggressively Should a Bank Pursue AI?

• Thomas H. Davenport
• George Westerman

A Malaysia-based CEO weighs the risks and potential benefits of turning a traditional bank into an AI-first institution.

Siti Rahman, the CEO of Malaysia-based NVF Bank, faces a pivotal decision. Her head of AI innovation, a recent recruit from Google, has a bold plan. It requires a substantial investment but aims to transform the traditional bank into an AI-first institution, substantially reducing head count and the number of branches. The bank’s CFO worries they are chasing the next hype cycle and cautions against valuing efficiency above all else. Siti must weigh the bank’s mixed history with AI, the resistance to losing the human touch in banking services, and the risks of falling behind in technology against the need for a prudent, incremental approach to innovation.

Two experts offer advice: Noemie Ellezam-Danielo, the chief digital and AI strategy at Société Générale, and Sastry Durvasula, the chief information and client services officer at TIAA.

Siti Rahman, the CEO of Malaysia-headquartered NVF Bank, hurried through the corridors of the university’s computer engineering department. She had directed her driver to the wrong building—thinking of her usual talent-recruitment appearances in the finance department—and now she was running late. As she approached the room, she could hear her head of AI innovation, Michael Lim, who had joined NVF from Google 18 months earlier, breaking the ice with the students. “You know, NVF used to stand for Never Very Fast,” he said to a few giggles. “But the bank is crawling into the 21st century.”

• Thomas H. Davenport is the President’s Distinguished Professor of Information Technology and Management at Babson College, a visiting scholar at the MIT Initiative on the Digital Economy, and a senior adviser to Deloitte’s AI practice. He is a coauthor of All-in on AI: How Smart Companies Win Big with Artificial Intelligence (Harvard Business Review Press, 2023).
• George Westerman is a senior lecturer at MIT Sloan School of Management and a coauthor of Leading Digital (HBR Press, 2014).

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