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Malaria: The Past and the Present

Jasminka talapko.

1 Faculty of Dental Medicine and Health, Josip Juraj Strossmayer University of Osijek, Crkvena 21, HR-31000 Osijek, Croatia; rh.zmdf@okpalatj (J.T.); rh.zmdf@vecva (A.V.)

Ivana Škrlec

Tamara alebić.

2 Faculty of Medicine, Josip Juraj Strossmayer University of Osijek, Josipa Huttlera 4, HR-31000 Osijek, Croatia; [email protected] (T.A.); moc.liamg@71ikujm (M.J.)

Melita Jukić

3 General Hospital Vukovar, Županijska 35, HR-32000 Vukovar, Croatia

Aleksandar Včev

Malaria is a severe disease caused by parasites of the genus Plasmodium , which is transmitted to humans by a bite of an infected female mosquito of the species Anopheles . Malaria remains the leading cause of mortality around the world, and early diagnosis and fast-acting treatment prevent unwanted outcomes. It is the most common disease in Africa and some countries of Asia, while in the developed world malaria occurs as imported from endemic areas. The sweet sagewort plant was used as early as the second century BC to treat malaria fever in China. Much later, quinine started being used as an antimalaria drug. A global battle against malaria started in 1955, and Croatia declared 1964 to be the year of eradication of malaria. The World Health Organization carries out a malaria control program on a global scale, focusing on local strengthening of primary health care, early diagnosis of the disease, timely treatment, and disease prevention. Globally, the burden of malaria is lower than ten years ago. However, in the last few years, there has been an increase in the number of malaria cases around the world. It is moving towards targets established by the WHO, but that progress has slowed down.

1. Introduction

Malaria affected an estimated 219 million people causing 435,000 deaths in 2017 globally. This burden of morbidity and mortality is a result of more than a century of global effort and research aimed at improving the prevention, diagnosis, and treatment of malaria [ 1 ]. Malaria is the most common disease in Africa and some countries in Asia with the highest number of indigenous cases. The malaria mortality rate globally ranges from 0.3–2.2%, and in cases of severe forms of malaria in regions with tropical climate from 11–30% [ 2 ]. Different studies showed that the prevalence of malaria parasite infection has increased since 2015 [ 3 , 4 ].

The causative agent of malaria is a small protozoon belonging to the group of Plasmodium species, and it consists of several subspecies. Some of the Plasmodium species cause disease in human [ 2 , 5 ]. The genus Plasmodium is an amoeboid intracellular parasite which accumulates malaria pigment (an insoluble metabolite of hemoglobin). Parasites on different vertebrates; some in red blood cells, and some in tissue. Of the 172 of Plasmodium species, five species can infect humans. These are P. malariae , P.falciparum , P.vivax , P.ovale , and P.knowlesi . In South-East Asia, the zoonotic malaria P.knowlesi is recorded. Other species rarely infect humans [ 5 , 6 , 7 , 8 ]. All the mentioned Plasmodium species cause the disease commonly known as malaria (Latin for Malus aer —bad air). Likewise, all species have similar morphology and biology [ 9 ].

The Plasmodium life cycle is very complex and takes place in two phases; sexual and asexual, the vector mosquitoes and the vertebrate hosts. In the vectors, mosquitoes, the sexual phase of the parasite’s life cycle occurs. The asexual phase of the life cycle occurs in humans, the intermediate host for malaria [ 9 , 10 ]. Human malaria is transmitted only by female mosquitoes of the genus Anopheles . The parasite, in the form of sporozoite, after a bite by an infected female mosquito, enters the human blood and after half an hour of blood circulation, enters the hepatocytes [ 11 ]. The first phase of Plasmodium asexual development occurs in the hepatocytes, and then in the erythrocytes. All Plasmodium species lead to the rupture of erythrocytes [ 7 , 9 , 12 , 13 ].

The most common species in the Americas and Europe are P.vivax and P.malariae , while in Africa it is P.falciparum [ 14 ].

2. Discovery of Malaria

It is believed that the history of malaria outbreaks goes back to the beginnings of civilization. It is the most widespread disease due to which many people have lost lives and is even thought to have been the cause of major military defeats, as well as the disappearance of some nations [ 15 ]. The first descriptions of malaria are found in ancient Chinese medical records of 2700 BC, and 1200 years later in the Ebers Papyrus [ 2 ]. The military leader Alexander the Great died from malaria [ 15 ]. The evidence that this disease was present within all layers of society is in the fact that Christopher Columbus, Albrecht Dürer, Cesare Borgia, and George Washington all suffered from it [ 16 , 17 ].

Although the ancient people frequently faced malaria and its symptoms, the fever that would occur in patients was attributed to various supernatural forces and angry divinities. It is, thus, stated that the Assyrian-Babylonian deity Nergal was portrayed as a stylized two-winged insect, as was the Canaan Zebub (‘Beelzebub, in translation: the master of the fly’) [ 17 ]. In the 4th century BC, Hippocrates described this disease in a way that completely rejected its demonic origins and linked it with evaporation from swamps which, when inhaled, caused the disease. That interpretation was maintained until 1880 and Laveran’s discovery of the cause of the disease [ 18 ]. Laveran, a French military surgeon, first observed parasites in the blood of malaria patients, and for that discovery he received the Nobel Prize in 1907 [ 19 ].

Cartwright and Biddis state that malaria is considered to be the most widespread African disease [ 14 ]. The causative agent of malaria is a small protozoon belonging to the group of Plasmodium species, and it consists of several subspecies [ 14 ].

3. The Development of Diagnostic Tests for Proving Malaria through History

Malaria can last for three and up to five years, if left untreated, and depending on the cause, may recrudesce. In P. vivax and ovale infections, the persistence of the merozoites in the blood or hypnozoites in hepatocytes can cause relapse months or years after the initial infection. Additionally, relapse of vivax malaria is common after P. falciparum infection in Southeast Asia. Relapse cases were observed in P. falciparum infections, which can lead to a rapid high parasitemia with subsequent destruction of erythrocytes [ 20 , 21 ]. Children, pregnant women, immunocompromised and splenectomized patients are especially vulnerable to malaria infection, as well as healthy people without prior contact with Plasmodium . A laboratory test for malaria should always confirm clinical findings. The proving of malaria is carried out by direct methods such as evidence of parasites or parts of parasites, and indirect methods that prove the antibodies to the causative agents ( Table 1 ) [ 2 , 5 , 22 ].

Diagnostic tests for proving malaria.

The gold standard method for malaria diagnosis is light microscopy of stained blood films by Giemsa. Due to a lack of proper staining material and trained technicians, this method is not available in many parts of sub-Saharan Africa. The sensitivity of the method depends on the professional expertise, and it is possible to detect an infection with 10–100 parasites/μL of blood. A negative finding in patients with symptoms does not exclude malaria, but smears should be repeated three times in intervals of 12–24 h if the disease is still suspected [ 23 , 24 ]. Diagnosis of malaria using serologic testing has traditionally been done by immunofluorescence antibody testing (IFA). IFA is time-consuming and subjective. It is valuable in epidemiological studies, for screening possible blood donors. It also demands fluorescence microscopy and qualified technicians [ 23 , 25 , 26 ].

Rapid Diagnostic Tests (RDT) for the detection of antigens in the blood are immunochromatographic tests to prove the presence of parasite antigens. No electrical equipment, and no special experience or skills are required to perform these tests. The RDTs are now recommended by WHO as the first choice of test all across the world in all malaria-endemic areas. The sensitivity of the antigen test varies depending on the selected antigens represented in the test. For some RDTs is 50–100 parasites/μL (PfHRP2) to <100 parasites/μL [ 27 , 28 ]. The FDA approved the first RDT test in 2007. It is recommended that the results of all RDT tests should be confirmed by microscopic blood analysis [ 29 ]. It is known that antigens detected with RDT test remain in the blood after antimalarial treatment, but the existence of these antigens varies after treatment. The false-positive rates should be less than 10% [ 30 ]. Several RDT tests in the eight rounds of testing revealed malaria at a low-density parasite (200 parasites/μL), had low false-positive rates and could detect P. falciparum or P. vivax infections or both [ 30 ]. False-positive rates of P. vivax were typically small, between 5% and 15%. On the other hand, the false-positive rates of P. falciparum range from 3–32% [ 30 , 31 ]. Good RDTs might occasionally give false-negative results if the parasite density is low, or if variations in the production of parasite antigen reduce the ability of the RDT to detect the parasite. False negative results of the RDT test for P. falciparum ranged between 1% and 11% [ 31 , 32 , 33 , 34 ]. The overall sensitivity of RDTs is 82% (range 81–99%), and specificity is 89% (range 88–99%) [ 35 ].

Polymerase chain reaction (PCR) is another method in the detection of malaria. This method is more sensitive and more specific than all conventional methods in the detection of malaria. It can detect below one parasite/μL. PCR test confirms the presence of parasitic nucleic acid [ 23 , 36 ]. PCR results are often not available fast enough to be useful in malaria diagnosis in endemic areas. However, this method is most helpful in identifying Plasmodium species after diagnosis by microscopy or RDT test in laboratories that might not have microscopic experts. Additionally, PCR is useful for the monitoring of patients receiving antimalaria treatment [ 36 , 37 ].

Indirect methods are used to demonstrate antibodies to malaria-causing agents. Such methods are used in testing people who have been or might be at risk of malaria, such as blood donors and pregnant women. The method is based on an indirect immunofluorescence assay (IFA) or an ELISA test. The IFA is specific and sensitive but not suitable for a large number of samples, and the results are subjective evaluations. For serological testing, ELISA tests are more commonly used [ 26 ].

Rapid and accurate diagnosis of malaria is an integral part of appropriate treatment for affected person and the prevention of the further spread of the infection in the community.

4. Malaria Treatment through History

Already in the 2nd century BC, a sweet sagewort plant named Qinghai (Latin Artemisia annua ) was used for the treatment of malaria in China [ 38 ]. Much later, in the 16th century, the Spanish invaders in Peru took over the cinchona medication against malaria obtained from the bark of the Cinchona tree (Latin Cinchona succirubra ). From this plant in 1820 the French chemists, Pierre Joseph Pelletie, and Joseph Bienaimé Caventou isolated the active ingredient quinine, which had been used for many years in the chemoprophylaxis and treatment of malaria. In 1970, a group of Chinese scientists led by Dr. Youyou Tu isolated the active substance artemisinin from the plant Artemisia annua , an antimalarial that has proved to be very useful in treating malaria. For that discovery, Youyou Tu received the Nobel Prize for Physiology and Medicine in 2015 [ 39 , 40 , 41 ]. Most of the artemisinin-related drugs used today are prodrugs, which are activated by hydrolysis to the metabolite dihydroartemisinin. Artemisinin drugs exhibit its antimalarial activity by forming the radical via a peroxide linkage [ 42 ]. WHO recommends the use of artemisinin-based combination therapies (ACT) to ensure a high cure rate of P. falciparum malaria and reduce the spread of drug resistance. ACT therapies are used due to high resistance to chloroquine, sulfadoxine-pyrimethamine, and amodiaquine [ 1 ]. Due to the unique structure of artemisinins, there is much space for further research. Extensive efforts are devoted to clarification of drug targets and mechanisms of action, the improvement of pharmacokinetic properties, and identifying a new generation of artemisinins against resistant Plasmodium strains [ 42 ].

The German chemist Othmer Zeidler synthesized dichlorodiphenyltrichloroethane (DDT) in 1874 during his Ph.D. At that time, no uses of DDT was found, and it just became a useless chemical [ 43 ]. The insecticide property of DDT was discovered in 1939 by Paul Müller in Switzerland. DDT began to be used to control malaria at the end of the Second World War [ 40 ]. During the Second World War, the success of DDT quickly led to the introduction of other chlorinated hydrocarbons which were used in large amounts for the control of diseases transmitted by mosquito [ 43 ]. From the late Middle Ages until 1940, when DDT began to be applied, two-thirds of the world’s population had been exposed to malaria, a fact that represented a severe health, demographic, and economic problem [ 29 , 40 , 41 , 44 , 45 ]. DDT is an organochlorine pesticide which was applied in liquid and powder form against the insects. During the Second World War people were sprayed with DDT. After the war, DDT became a powerful way of fighting malaria by attacking the vector [ 43 ].

Five Nobel Prizes associated with malaria were awarded: Youyou Tu in 2015. Ronald Ross received the Nobel Prize in 1902 for the discovery and significance of mosquitoes in the biology of the causative agents in malaria. In 1907, the Nobel was awarded to the already-mentioned Charles Louis Alphonse Laveran for the discovery of the causative agent. Julius Wagner-Jauregg received it in 1927 for the induction of malaria as a pyrotherapy procedure in the treatment of paralytic dementia. In 1947 Paul Müller received it for the synthetic pesticide formula dichlorodiphenyltrichloroethane.

Attempts to produce an effective antimalarial vaccine and its clinical trials are underway. Over the past several decades’ numerous efforts have been made to develop effective and affordable preventive antimalaria vaccines. Numerous clinical trials are completed in the past few years. Nowadays are ongoing clinical trials for the development of next-generation malaria vaccines. The main issue is P. vivax vaccine, whose research requires further investigations to identify novel vaccine candidates [ 46 , 47 , 48 ]. Despite decades of research in vaccine development, an effective antimalaria vaccine has not yet been developed (i.e., with efficacy higher than 50%) [ 49 , 50 , 51 ]. The European Union Clinical Trials Register currently displays 48 clinical trials with a EudraCT protocol for malaria, of which 13 are still ongoing clinical trials [ 52 ]. The malaria parasite is a complex organism with a complex life cycle which can avoid the immune system, making it very difficult to create a vaccine. During the different stages of the Plasmodium life cycle, it undergoes morphological changes and exhibits antigenic variations. Plasmodium proteins are highly polymorphic, and its functions are redundant. Also, the development of malaria disease depends on the Plasmodium species. That way, a combination of different adjuvants type into antigen-specific formulations would achieve a higher efficacy [ 53 , 54 ]. Drugs that underwent clinical trials proved to be mostly ineffective [ 5 , 7 , 55 ]. However, many scientists around the world are working on the development of an effective vaccine [ 56 , 57 , 58 ]. Since other methods of suppressing malaria, including medication, insecticides, and bed nets treated with pesticides, have failed to eradicate the disease, and the search for a vaccine is considered to be one of the most important research projects in public health by World Health Organization (WHO).

The best way to fight malaria is to prevent insect bites. Malaria therapy is administered using antimalarial drugs that have evolved from quinine. According to its primary effect, malarial vaccines are divided into pre-erythrocytic (sporozoite and liver-stage), blood-stage, and transmission-blocking vaccines [ 9 , 54 ]. Most medications used in the treatment are active against parasitic forms in the blood (the type that causes disease) ( Table 2 ) [ 59 ]. The two crucial antimalarial medications currently used are derived from plants whose medical importance has been known for centuries: artemisinin from the plant Qinghao ( Artemisia annua L, China, 4th century) and quinine from Cinchona (South America, 17th century). Side-by-side with artemisinin, quinine is one of the most effective antimalarial drugs available today [ 13 , 39 , 40 ]. Doxycycline is indicated for malaria chemoprophylaxis for travel in endemic areas. It is also used in combination with the quinine or artesunate for malaria treatment when ACT is unavailable or when the treatment of severe malaria with artesunate fails. The disadvantage of doxycycline is that children and pregnant women cannot use it [ 29 ]. Due to the global resistance of P. falciparum to chloroquine, ACTs are recommended for the treatment of malaria, except in the first trimester of pregnancy. ACTs consist of a combination of an artemisinin derivative that fast decreases parasitemia and a partner drug that eliminates remaining parasites over a more extended period. The most common ACTs in use are artemether-lumefantrine, artesunate-amodiaquine, dihydroartemisinin-piperaquine, artesunate-mefloquine, and artesunate with sulfadoxine-pyrimethamine. The ACTs were very efficient against all P. falciparum until recently when numbers of treatment failures raised in parts of Southeast Asia. Atovaquone-proguanil is an option non-artemisinin-based treatment that is helpful for individual cases which have failed therapy with usual ACTs. Although, it is not approved for comprehensive implementation in endemic countries because of the ability for the rapid development of atovaquone resistance. Quinine remains efficient, although it needs a long course of treatment, is poorly tolerated, especially by children, and must be combined with another drug, such as doxycycline or clindamycin. Uncomplicated vivax, malariae, and ovale malaria are handled with chloroquine except in case of chloroquine-resistant P. vivax when an ACT is used [ 7 , 29 , 60 , 61 , 62 ].

Overview of the most commonly used antimalarials.

CNS—central nervous system.

4.1. Malaria in Europe

In Europe, malaria outbreaks occurred in the Roman Empire [ 63 , 64 ] and the 17th century. Up until the 17th century it was treated as any fever that people of the time encountered. The methods applied were not sufficient and included the release of blood, starvation, and body cleansing. As the first effective antimalarial drug, the medicinal bark of the Cinchona tree containing quinine was mentioned and was initially used by the Peruvian population [ 14 ]. It is believed that in the fourth decade of the 17th century it was transferred to Europe through the Spanish Jesuit missionaries who spread the treatment to Europe [ 65 ].

Contemporary knowledge of malaria treatment is the result of the work of a few researchers. Some of researchers are Alphonse Laveran, Ronald Ross, and Giovanni Battista Grassi. In November 1880, Laveran, who worked as a military doctor in Algeria, discovered the causative agents of malaria in the blood of mosquitoes and found that it was a kind of protozoa [ 66 ]. Laveran noticed that protozoa could, just like bacteria, live a parasitic way of life within humans and thus cause disease [ 66 ]. Nearly two decades later, more precisely in 1898, Ronald Ross, a military doctor in India, discovered the transmission of bird malaria in the saliva of infected mosquitos, while the Italian physician Giovanni Battista Grassi proved that malaria was transmitted from mosquitoes to humans, in the same year. He also proved that not all mosquitoes transmit malaria, but only a specific species ( Anopheles ) [ 17 ]. This discovery paved the way for further research.

The global battle against malaria started in 1955, and the program was based on the elimination of mosquitoes using DDT and included malarial areas of the United States, Southern Europe, the Caribbean, South Asia, but only three African countries (South Africa, Zimbabwe, and Swaziland). In 1975, the WHO announced that malaria had been eradicated in Europe and all recorded cases were introduced through migration [ 67 , 68 ].

4.2. Malaria in Croatia

In Croatia, the first written document that testifies to the prevention of malaria is the Statute of the town of Korčula from 1265. In 1874, the Law on Health Care of Croatia and Slavonia established the public health service that was directed towards treating malaria. There was no awareness nor proper medical knowledge about malaria, but the drainage was carried out to bring the ‘healthy air’ in the cities [ 69 , 70 ]. In 1798 physician Giuseppe Arduino notified the Austrian government about malaria in Istria. A government representative Vincenzo Benini accepted a proposed sanitary measure of the drainage of wetlands [ 71 ]. In 1864, the drainage of wetlands around Pula and on the coastal islands began, and since 1902 a program for the suppression of malaria by treatment of patients using quinine has been applied [ 72 ]. In 1922, the Institute for Malaria was founded in Trogir. In 1923, on the island of Krk, a project was started to eradicate malaria by the sanitation of water surfaces and the treatment of the patients with quinine, led by Dr. Otmar Trausmiller [ 66 ]. Since 1924, besides chemical treatment, biological control of mosquitoes has been established by introducing the fish Gambusia holbrooki to Istria and the coast [ 73 ]. In 1930 legislation was passed to enforce village sanitation, which included the construction of water infrastructure and safe wells, contributing to the prevention of malaria. Regular mosquito fogging with arsenic green (copper acetoarsenite) was introduced, and larvicidal disinfection of stagnant water was carried out.

Since malaria occurs near swamps, streams, ravines, and places where mosquitoes live near water, this disease has been present throughout history in Croatia, and it has often become an epidemic [ 74 ]. It was widespread in the area of Dalmatia, the Croatian Littoral region, Istria, and river flows. In the area of the Croatian Littoral, it was widespread on some islands, such as Krk, Rab, and Pag, while the mainland was left mainly clear of it [ 75 ]. The ethnographer Alberto Fortis (1741–1803) who traveled to Dalmatia, noted impressions recording details of malaria that was a problem in the Neretva River valley. Fortis wanted to visit that area, but the sailors on ship were afraid, probably because the were afraid to go to a place where there had been a disease outbreak known as the Neretva plague [ 76 ]. This Neretva plague was, in fact, malaria, and it is believed that due to it, the Neretva was nicknamed “Neretva—damned by God” [ 77 , 78 ]. Speaking of the Neretva region, Fortis states that the number of mosquitoes in that wetland area was so high that people had to sleep in stuffy canopy tents to defend themselves. Fortis also states that there were so many mosquitoes that he was affected by it. During the stay, Fortis met a priest who had a bump on the head claiming it had occurred after a mosquito bite and believed that the fever that infected the people of the Neretva Valley was also a consequence of the insect bites there [ 76 ]. In a manuscript, Dugački described some of the epidemics in Croatia. Thus, noted the small population of Nin in 1348, which was the result of the unhealthy air and high mortality of the population. Three centuries later, in 1646, the fever was mentioned in Novigrad, while the year 1717 was crucial for to the Istrian town of Dvigrad, which was utterly deserted due to malaria. At the beginning of the 20th century, more precisely in 1902, the daily press reported that the Provincial Hospital in Zadar was full of people affected by malaria. The extent to which this illness was widespread is proved by the fact that at the beginning of the 20th century about 180,000 people suffered from it in Dalmatia [ 18 ]. The volume and frequency of epidemics in Dalmatia resulted in the arrival of the Italian malariologist Grassi and the German parasitologist Schaudin. The procedures of quininization began to be applied, and in 1908 25 physicians and 423 pill distributors were to visit the villages and divide pills that had to be taken regularly to the people to eradicate malaria [ 75 ].

Likewise, in Slavonia, malaria had also a noticeable effect, and it was widespread in the 18th century due to a large number of swamps that covered the region. Such areas were extremely devastating for settlers who were more vulnerable to the disease than its domestic population [ 79 ]. Friedrich Wilhelm von Taube (1728–1778) recorded the disease and stated that the immigrant Germans were primarily affected by malaria and that the cities of Osijek and Petrovaradin can be nicknamed "German Cemeteries" [ 80 ]. According to Skenderović, the high mortality of German settlers from malaria was not limited only to the Slavonia region but also to the Danubian regions in which the Germans had settled in the 18th century, with Banat and Bačka [ 79 ] having the most significant number of malaria cases. The perception of Slavonia in the 18th century was not a positive one. Even Taube stated that Slavonia was not in good standing in the Habsburg Monarchy and that the nobility avoided living there. As some of the reasons for this avoidance, Taube mentioned the unhealthy air and the many swamps in the area around in which there was a multitude of insects. Taube noted that mosquitoes appear to be larger than in Germany and that its bite was much more painful. A change in the situation could only be brought about by drying the swamp, in his opinion [ 80 ]. Since malaria had led to the death of a large number of people, the solution had to be found to stop its further spread. Swamp drying was finally accepted by the Habsburg Monarchy and some European countries as a practical solution and, thus, its drainage began during the 18th century, resulting in cultivated fields [ 79 ].

Since epidemics of malaria continued to occur, there is one more significant record of the disease in the Medical Journal of 1877. In it, the physician A. Holzer cites his experiences from Lipik and Daruvar where he had been a spa physician for a long time. Holzer warns of the painful illness noticed at spa visitors suffering from the most in July and August. As a physician, Holzer could not remain indifferent to the fact that he did not see anyone looking healthy. It also pointed out that other parts of Croatia were not an exception. As an example, Holzer noted Virovitica County, where malaria was also widespread. He wanted to prevent the development and spread of the illness. Believing that preventing the toxic substances from rising into the air would stop the disease, the solution was to use charcoal that has the properties of absorbing various gases and, thus, prevents vapor rising from the ground [ 81 ].

Dr. Andrija Štampar (1888–1958) holds a prominent place in preventing the spread of malaria. Štampar founded the Department of Malaria, and numerous antimalaria stations, hygiene institutes, and homes of national health. Dr. Štampar devoted his life to educating the broader population about healthy habits and, thus, prevents the spread of infectious diseases. Many films were shown, including a film entitled ‘Malaria of Trogir’ in Osijek in 1927, with numerous health lectures on malaria [ 82 ]. After the end of the Second World War, a proposal for malaria eradication measures was drafted by Dr. Branko Richter. These measures, thanks to Dr. Andrija Štampar, are being used in many malaria-burdened countries. For the eradication of malaria in Croatia and throughout Yugoslavia, DDT has been used since 1947 [ 83 ].

Malaria is still one of the most infectious diseases that cause far more deaths than all parasitic diseases together. Malaria was eradicated in Europe in 1975. After that year, malaria cases in Europe are linked to travel and immigrants coming from endemic areas. Although the potential for malaria spreading in Europe is very low, especially in its western and northern parts, it is still necessary to raise awareness of this disease and keep public health at a high level in order to prevent the possibility of transmitting the disease to the most vulnerable parts of Europe [ 84 ].

Unofficial data show that malaria disappeared from Croatia in 1958, while the World Health Organization cites 1964 as the year when malaria was officially eradicated in Croatia [ 45 , 75 ]. Nonetheless, some cases of imported malaria have been reported in Croatia since 1964. The imported malaria is evident concerning Croatia’s orientation to maritime affairs, tourism, and business trips. Namely, malaria is introduced to Croatia by foreign and domestic sailors, and in rare cases by tourists, mainly from the countries of Africa and Asia [ 75 , 85 ]. According to the reports of the Croatian Institute of Public Health, since the eradication of this disease 423 malaria cases have been reported, all imported [ 86 ]. Figure 1 shows the number of imported malaria cases in Croatia from 1987–2017, and Figure 2 the causative Plasmodium species of those cases ( Figure 1 and Figure 2 ) [ 86 , 87 ].

Imported malaria cases in Croatia from 1987–2017.

The causative agents of imported malaria in Croatia.

There is also massive and uncontrollable migration from Africa and Asia (mostly due to climate change) of both humans and birds, from countries with confirmed epidemics. This issue is an insurmountable problem if measured by the traditional approach. Insecticides (DDT, malathion, etc.) synthetic pyrethroids, in addition to inefficiency, impact the environment (harm bees, fruits, vines, etc.). Consequently, scientists have patiently established a mosquito control strategy (University of Grenoble, Montpellier) which includes a meticulous solution to the mosquito vector effect (malaria, arbovirus infection, West Nile virus) by changes in agriculture, urbanism, public services hygiene [ 88 ].

Northeastern Slavonia is committed to applying methods that are consistent with such achievements, with varying success, as certain limitations apply to protected natural habitats (Kopački rit) [ 89 ].

There is a historical link between population movement and global public health. Due to its unique geostrategic position, in the past, Croatia has been the first to experience epidemics that came to Europe through land and sea routes from the east. Adriatic ports and international airports are still a potential entry for the import of individual cases of communicable diseases. Over the past few years, sailors, as well as soldiers who worked in countries with endemic malaria, played a significant role in importing malaria into Croatia. Successful malaria eradication has been carried out in Croatia. Despite that in Croatia are still many types of Anopheles , which means that the conditions of transmission of the imported malaria from the endemic areas still exist. The risk of malaria recrudesce is determined by the presence of the vector, but also by the number of infected people in the area. Due to climate change, it is necessary to monitor the vectors and people at risk of malaria. Naturally- and artificially-created catastrophes, such as wars and mass people migration from endemic areas, could favor recrudescing of malaria. Once achieved, eradication would be maintained if the vector capacities are low and prevention measures are implemented. The increased number of malaria cases worldwide, the recrudesce of indigenous malaria cases in the countries where the disease has been eradicated, the existence of mosquitoes that transmit malaria and the number of imported malaria cases in Croatia are alarming facts. Health surveillance, including obligatory and appropriate prophylaxis for travelers to endemic areas, remains a necessary public health care measure pointed at managing malaria in Croatia.

5. Malaria Trends in the World

The WHO report on malaria in 2017 shows that it is difficult to achieve two crucial goals of a Global Technical Strategy for Malaria. These are a reduction in mortality and morbidity by at least 40% by 2020. Since 2010, there has been a significant reduction in the burden of malaria, but analysis suggests a slowdown, and even an increase in the number of cases between 2015 and 2017. Thus, the number of malaria cases in 2017 has risen to 219 million, compared to 214 million cases in 2015 and 239 million cases in 2010. Figure 3 presents the reported number of malaria cases per WHO region from 1990–2017 [ 1 , 90 ]. The most critical step in the global eradication of malaria is to reduce the number of cases in countries with the highest burden (many in Africa). The number of deaths from disease is declining, thus, in 2017 there were 435,000 deaths from malaria globally, compared with 451,000 in 2016, and 607,000 deaths in 2010. Figure 4 presents the number of malaria deaths from 1990-2017 [ 1 , 90 ]. Despite the delay in global progress, there are countries with decreasing malaria cases during 2017. Thus, India in 2017, compared with 2016, recorded a 24% decline of malaria cases. The number of countries reporting less than 10,000 malaria cases is growing, from 37 countries in 2010, to 44 in 2016, and to 46 in 2017. Furthermore, the number of countries with fewer than 100 indigenous malaria cases growing from 15 in 2010, to 26 countries in 2017 [ 1 ].

Reported malaria cases per WHO region from 1990–2017.

Reported malaria deaths per WHO region from 1990–2017.

Funding in malaria has not changed much. During 2017, US$3.1 billion was invested in malaria control and elimination globally. That was 47% of the expected amount by 2020. The USA was the largest single international donor for malaria in 2017 [ 1 , 91 ].

The most common global method of preventing malaria is insecticide-treated bed nets (ITNs). The WHO report on insecticide resistance showed that mosquitoes became resistant to the four most frequently used classes of insecticides (pyrethroids, organochlorines, carbamates, and organophosphates), which are widespread in all malaria-endemic countries [ 1 , 7 , 92 ].

Drug resistance is a severe global problem, but the immediate threat is low, and ACT remains an effective therapy in most malaria-endemic countries [ 1 , 93 ].

According to the WHO, Africa still has the highest burden of malaria cases, with 200 million cases (92%) in 2017, then Southeast Asia (5%), and the Eastern Mediterranean region (2%). The WHO Global Technical Strategy for Malaria by 2020 is the eradication of malaria from at least ten countries that were malaria-endemic in 2015 [ 1 ].

The march towards malaria eradication is uneven. Indigenous cases in Europe, Central Asia, and some countries in Latin America are now sporadic. However, in many sub-Saharan African countries, elimination of malaria is more complicated, and there are indications that progress in this direction has delayed. Elimination of vivax and human knowlesi malaria infections are another challenge [ 7 ].

6. Conclusions

The campaign to eradicate malaria began in the 1950s but failed globally due to problems involving the resistance of mosquitoes to the insecticides used, the resistance of malaria parasites to medication used in the treatment, and administrative issues. Additionally, the first eradication campaigns never included most of Africa, where malaria is the most common. Although the majority of forms of malaria are successfully treated with the existing antimalarials, morbidity and mortality caused by malaria are continually increasing. This issue is the consequence of the ever-increasing development of parasite resistance to drugs, but also the increased mosquito resistance to insecticides, and has become one of the most critical problems in controlling malaria over recent years. Resistance has been reported to all antimalarial drugs. Therefore, research into finding and testing new antimalarials, as well as a potential vaccine, is still ongoing, mainly due to the sudden mass migration of humans (birds, parasite disease vector insects) from areas with a large and diverse infestation.

The process towards eradication in some countries confirms that current tools could be sufficient to eradicate malaria. The spread of insecticide resistance among the vectors and the rising ACT failures indicate that eradication of malaria by existing means might not be enough.

Thus, given the already complicated problem of overseeing and preventing the spread of the disease, it will be necessary to supplement and change the principles, strategic control, and treatment of malaria.

Abbreviations

Author contributions.

Writing the manuscript: J.T., I.Š., and T.A.; updating the text: J.T., I.Š., T.A., and A.V.; literature searches: J.T., I.Š., T.A., and M.J.; tables and figures drawing: I.Š. and M.J.; critical reviewing of the manuscript: A.V.; organization and editing of the manuscript: I.Š. and A.V.

This research received no external funding. The article processing charges (APC) was funded by Faculty of Dental Medicine and Health, Osijek, Croatia.

Conflicts of Interest

The authors declare no conflict of interest.

Essay on Malaria Awareness

Introduction.

Malaria is a common disease in tropical countries where children and pregnant women are the main victims. It is a parasitic infection caused by plasmodium, which can be deadly to these vulnerable sections. As children are more prone to this disease, it is important to create awareness in them. So, this essay on malaria awareness will be beneficial for them to know more about it.

The main symptom of malaria is high fever with chills. So, it is possible that people confuse it with a viral fever, and malaria gets untreated, leading to other serious consequences. Since it is the life of our children that is at stake, we must take necessary measures to prevent and treat malaria. This short essay on malaria awareness will alert both children and elders on how to tackle this life-threatening disease.

Importance of Malaria Awareness

Malaria is spread from one individual to another by female Anopheles mosquitoes, and the symptoms in affected individuals resemble that of any viral fever. This is why knowledge about the disease is given due importance in this essay on malaria awareness. While high temperature and headache are the most common signs of malaria, nausea and drowsiness are also found in sick people. By detecting the disease early, we will be able to start the treatment soon, thus reducing the risk in children.

As we mentioned earlier in the short essay on malaria awareness that malaria is more prevalent in tropical countries, travelling to such places with little awareness about the disease could be dangerous. Children could fall ill at the end of the trip, which will ruin all the fun they had. So, this malaria awareness essay will be useful to know that it is risky to travel in the wet season to places that have humid climates.

All these points emphasise that it is important to have knowledge about malaria to prevent infections in children as well as make their journeys memorable. They will also be able to write about a memorable day of my life .

Ways to Raise Malaria Awareness

Just like how crucial it is to bring attention to the spread of malaria, it is equally important to understand that prevention is better than cure. Since we know that malaria is transmitted through mosquitoes, the first and foremost step in raising awareness of the disease is by spreading messages about mosquito breeding and destroying its breeding places. In this section of the essay on malaria awareness, we will see effective methods to create awareness among children.

While elders can understand the gravity of the disease, it is a struggle to teach our children about the same. Malaria is a disease that must be feared but let us not induce this threat in our kids. Instead, let us focus on imparting knowledge about malaria, its symptoms, and treatment to them in a fun way. By asking them to do simple tasks like cleaning their houses and surroundings and emptying the stagnant water from broken cups and bottles, we can build their awareness about the disease.

This short essay on malaria awareness concludes that however much of the threat is malaria, we can control it with proper awareness. So, let us nurture our children to grow in health and happiness with BYJU’S amazing essays on various topics.

Frequently Asked Questions on Essay on Malaria Awareness

Why should we raise awareness about malaria.

Malaria is a dangerous disease that has the potential to threaten one’s life. So, it is essential to create awareness about it to understand the symptoms and thereby treat it without any delay.

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The essay on malaria awareness can be useful for children to know more about the disease and the ways to prevent it.

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EDITORIAL article

Challenges for diagnosis, treatment and elimination of malaria.

• 1 Department of Clinical Analysis, São Paulo State University, Araraquara, São Paulo, Brazil
• 2 Molecular Biology and Malaria Immunology Research Group, Instituto René Rachou, Fundação Oswaldo Cruz (FIOCRUZ), Belo Horizonte, Minas Gerais, Brazil
• 3 Department of Microbiology, Tumor and Cell Biology, Karolinska Institutet, Solna, Sweden
• 4 Department of Research, Dr. Heitor Vieira Dourado Tropical Medicine Foundation, Manaus, Amazonas, Brazil
• 5 Malaria Laboratory, Parasitology Section, Instituto Evandro Chagas (IEC), Health and Environmental Surveillance Secretariat (SVSA), Brazilian Ministry of Health (MOH), Ananindeua, Brazil

Editorial on the Research Topic Challenges for the diagnosis, treatment, and elimination of malaria

Malaria is a major cause of death in many tropical and sub-tropical countries, presenting about 627,000 deaths and 241 million cases in the world. Malaria is still an important public health problem that needs to be more effectively controlled. Delays in diagnosis and treatment are responsible for most deaths in many countries. Moreover, in most malaria-endemic countries, the lack of resources is a huge barrier to reliable and timely diagnosis. It is a global priority to reduce the high malaria burden and to achieve long-term malaria eradication. In this Research Topic, constituted by 10 papers, we review and discuss the current challenges of malaria transmission, diagnosis, treatment, control, and future eradication.

Challenges for diagnosis, vaccines, and treatment

Vector-targeted interventions are highly effective in preventing malaria transmission and are an essential component of elimination strategies. The detection of Plasmodium infection in mosquitoes can be used to estimate exposure and transmission intensity and is a critical part of the management of malaria. Hugo et al. have successfully unveiled a groundbreaking diagnostic test designed for the rapid detection of Plasmodium falciparum in mosquitoes, which can achieve results in less than 30 min. This test is specifically tailored for low-resource settings, offering an invaluable solution to address the challenges posed by limited infrastructure. The methodology integrates a swift and uncomplicated sample preparation procedure with isothermal amplification by utilizing recombinase polymerase amplification (RPA). This is coupled with a subsequent lateral flow detection (LFD) step. The synergy of these elements enables the test to deliver efficient and timely outcomes. Remarkably, the developed RPA-LFD test exhibits analytical sensitivity which is at par with the gold standard, PCR. This signifies its efficacy as a reliable tool for the surveillance of mosquito populations carrying the P. falciparum parasite. The rapidity, simplicity, and accuracy of this diagnostic method make it a promising asset in the ongoing efforts to monitor and control malaria in resource-constrained environments.

On the other hand, the study developed by Costa et al. aimed to describe the development of seven specific qPCR assays for the diagnosis of Plasmodium vivax and P. falciparum , targeting coding and non-coding mitochondrial genomic regions as well as evaluating the possible pitfalls associated with the development of these assays. Although qPCR assays with the tested mitochondrial targets reduced the occurrence of non-specific amplifications, they were not able to eliminate them, in addition to hindering the efficiency of specific amplifications. A Cq (quantification cycle) cutoff value could not exclude false-positive findings for most assays, except for PV_CYTB and PF_CYTB, which presented a cutoff value with good specificity. As noted, although mitochondrial targets are considered the most sensitive, they often lose specificity due to their high sequence conservation ( P. vivax and P. falciparum have at least 90% of mtDNA conservation). Therefore, in the panorama of molecular assays with mitochondrial targets to identify Plasmodium sp., it is crucial to include a screening phase to evaluate the possibility of cross-reaction between species of the genus Plasmodium or even nonspecific amplification in a panel of samples free of human malaria.

In the realm of vaccination, the absence of an effective malaria vaccine stands out as a crucial gap in current strategies. This gap becomes even more pressing with the emergence of drug-resistant P. falciparum strains and the resistance of mosquitoes to insecticides, presenting formidable challenges to malaria treatment and elimination. The study of Waweru et al. aimed to bridge this gap by targeting the PfRh5 complex, a pivotal player in the erythrocyte invasion process. This complex comprises Pf-reticulocyte binding homolog 5 (PfRh5), Pf-interacting protein (PfRipr), Pf-cysteine-rich protective antigen (PfCyRPA), and Pf-P113 protein. Antibodies targeting these proteins have been proven effective in inhibiting parasite invasion, rendering them promising candidates for a blood-stage vaccine. However, the hurdle lies in the genetic polymorphisms within these genes, which pose potential obstacles to vaccine development. To unravel these complexities, the researchers conducted whole-genome sequencing of P. falciparum isolates from high-transmission regions in Kenya, with a specific focus on the PfRh5 complex. The study unveiled a total of 58 variants within the PfRh5 complex, with PfRh5 exhibiting the highest degree of polymorphism. Significantly, the Lake Victoria parasite population displayed low polymorphisms, suggesting the plausible candidacy of PfRh5 components for a malaria vaccine. These findings underscore the imperative for further exploration into the specific impacts of mutations on the parasite invasion process, offering valuable insights to propel the advancement of malaria vaccine development.

Malaria in pregnancy (MiP) presents a multitude of risks to the well-being of both mothers and their unborn infants. While the connection between severe pregnancy outcomes, including miscarriage and stillbirth, and MiP is firmly established, there is a pressing need for a more comprehensive understanding of adverse pregnancy outcomes and their prevalence in malaria-endemic regions. Acquiring such knowledge is crucial to evaluate the effectiveness of implemented strategies aimed at preventing MiP, notably the safety and efficacy of MiP vaccines. Berhe et al. reviewed the primary adverse effects associated with MiP and delineated the existing strategies to mitigate its impact. The authors underscore the significance of thoroughly assessing this information as a prerequisite to initiating clinical trials for MiP vaccines. This emphasis on pre-trial evaluation ensures a well-informed approach to vaccine development and implementation, thereby maximizing the potential for success in combatting the adverse effects of malaria during pregnancy.

Prevention and control

Malaria continues to be a major global health concern, particularly in resource-constrained settings, significantly impacting children under 5 years old. Long-lasting insecticide-treated nets (LLINs) are a key intervention endorsed by the World Health Organization (WHO) to combat malaria, which show a potential to reduce cases by 50%. In Ghana, where malaria is hyper-endemic, primarily caused by P. falciparum , the transmission is year-round, which peaks from June to October. Dako-Gyeke et al. lead efforts to combat malaria through mass LLIN distribution campaigns. Despite progress, challenges persist in achieving strategic plan targets, with identified barriers to LLIN use in various studies. In response, a community health advocacy team (CHAT) was collaboratively created in six Ghanaian communities, which aimed to promote LLIN use through a person-centered approach, thus leveraging the Community Health Planning and Services (CHPS) program. The qualitative study delves into the opportunities and barriers during the pilot implementation of CHATs, which involved 43 members across six communities in Ghana’s Eastern and Volta regions. While CHATs effectively sensitized communities and positively influenced behavior change, the challenges included a lack of financial support for transportation and outreach activities.

Despite global efforts, regions like Djibouti and Ethiopia continue to report substantial transmission rates of malaria, which were exacerbated by disruptions from the COVID-19 pandemic. Moreover, studies across sub-Saharan Africa reveal varied knowledge, attitudes, and practices regarding malaria prevention. Factors such as education, income, age, and cultural beliefs may also influence prevention measures. In this context, the study by Addis and Wondmeneh focused on Ada’ar woreda district, in the pastoral region of Afar, Ethiopia, where malaria data is lacking. The research involved 422 households, revealing diverse knowledge, attitudes, and practices. Individuals with poor knowledge tend to practice inadequate prevention methods, and young adults exhibit suboptimal healthcare-seeking behaviors. The study highlights ongoing challenges in awareness and adherence to malaria control measures in the Afar region. The findings offer valuable insights for public health strategies in the Afar region, emphasizing the need for community-specific approaches to combat malaria.

Following the same context, Nigeria, which is celebrating 62 years of independence in 2022, faces a severe malaria burden, contributing significantly to the global caseload and mortality. The perspective article of Oboh et al. underscores that, despite numerous control initiatives, Nigeria consistently leads in both malaria cases and deaths. The diverse malaria transmission patterns across the country emphasize the need for tailored intervention strategies. To address this challenge, the authors advocate for a focused and research-driven approach, exploring vectorial capacity, insecticide susceptibility, hotspot identification, and the genetic makeup of P. falciparum . This targeted research has the potential to reveal crucial insights, including the migration of parasite populations. Achieving pre-elimination status demands prioritized efforts to comprehend the circulating Plasmodium strains, which will enable informed policy implementation for malaria transmission control in Nigeria.

Mozambique’s National Malaria Strategic Plan targets 85% population protection through testing and treatment. However, the country faces challenges due to climatic vulnerability, frequent natural disasters, and susceptibility to climate change. The study of Armando et al. explores the spatial and temporal dynamics of malaria transmission, which integrate socioeconomic, climatic, and land use data. Analyzing data from 2016 to 2018 at the district level, the study employs a Bayesian framework to model malaria cases. The results reveal an increased malaria risk associated with higher temperatures and specific climatic conditions. Moreover, the study identifies lag patterns and establishes links between climate variables and malaria incidence. Notably, education level, access to electricity, and toilet facilities impact malaria risk. The findings provide valuable insights to design early warning systems and targeted prevention strategies to mitigate seasonal malaria surges in Mozambique, where the disease imposes a significant health burden.

In contrast, one focus of the study of Wang et al. was to present the epidemiological data of imported malaria cases in China from 2011 to 2019, i.e., before WHO has declared it to be malaria-free in 2021. This historical epidemiological pattern of imported malaria in China is of utmost importance to provide evidence-based data to prevent malaria re-establishment in this country. Prevention of re-establishment (POR) is understood as any strategy capable of preventing the emergence of malaria outbreaks/epidemics or avoiding the reestablishment of indigenous malaria in a malaria-free country. These findings revealed that the majority of malaria reported cases were from migratory volunteers, regardless of Plasmodium species, being imported cases mainly from West and/or Central Africa and Southeast Asia. Therefore, POR of malaria is a key strategy adopted by countries with malaria-free certification to successfully sustain the “malaria-free status.”

Although the World Health Organization (WHO) has promoted “test and treat” guidelines since 2010, recommending that all suspected malaria cases be confirmed with a parasitological test, usually a rapid diagnostic test (RDT), prior to treatment, the compliance of this recommendation is not a reality, especially in malaria-endemic areas in developing countries. In these scenarios, febrile patients are presumptively treated as malaria without diagnostic confirmation. The state of the art of an observational study on private sector antimalarial sales in Uganda has been enumerated by Shelus et al. The main goal of this study was to expand the understanding and knowledge about the private sector malaria case management in Bugoye, western Uganda approximately 10 years after the Uganda Ministry of Health launched their “test, treat, and track” policy. Among the study’s key findings, the authors noted that, of the 934 customers with suspected malaria who visited study drug stores during the data collection period, only 25% (233/934) purchased a RDT. Therefore, most cases used to be treated presumptively and possibly may not even have the malaria infection. This practice of irrational use of medicines can cause many organic disorders, in addition to contributing to the selection of resistant strains of Plasmodium sp. to antimalarials. In view of this, it is mandatory to adopt interventions in the field of pharmacovigilance, with the aim of ensuring rational use of medicines in the private sector of Bugoye, western Uganda.

Author contributions

MP: Writing – original draft, Writing – review & editing. TN: Writing – original draft, Writing – review & editing. Gd: Writing – original draft, Writing – review & editing. GV: Writing – original draft, Writing – review & editing.

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.

The author(s) declared that they were an editorial board member of Frontiers, at the time of submission. This had no impact on the peer review process and the final decision.

Publisher’s note

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.

Keywords: malaria, Plasmodium , eradication, malaria transmission, diagnosis, treatment

Citation: Pucca MB, de Sousa TN, Cardoso de Melo G and Viana GMR (2024) Editorial: Challenges for diagnosis, treatment, and elimination of malaria. Front. Trop. Dis 5:1394693. doi: 10.3389/fitd.2024.1394693

Received: 01 March 2024; Accepted: 05 April 2024; Published: 18 April 2024.

Edited and Reviewed by:

Copyright © 2024 Pucca, de Sousa, Cardoso de Melo and Viana. 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: Manuela Berto Pucca, [email protected]

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.

How Malaria Spreads

• Most people get malaria from the bite of an infective mosquito.
• Most cases of malaria in the U.S. are in people who have traveled to or from areas where malaria is widespread.
• Once infected with malaria, it can take several days or even months to feel sick.

Malaria is a disease caused by a parasite.

How it spreads

Most people get malaria when bitten by a mosquito infected with the malaria parasite. Only female Anopheles mosquitoes can spread malaria. For the Anopheles mosquito to become infected, they must bite, or take a blood meal, from a person with the malaria parasites. About one week later, the mosquito will inject the parasites via her saliva into the next person she bites. And the cycle of infection continues.

In rare occasions, malaria can spread through

• blood transfusions,
• organ transplant,
• sharing needles or syringes contaminated with malaria-infected blood, or
• congenitally, meaning from a mother to her unborn infant before or during delivery.

How it does not spread

Malaria is not contagious. People can’t spread malaria to other people like a cold or the flu. You can’t get malaria through casual contact (sitting next to a person with malaria), close physical contact, or sexual contact.

Factors that increase risk

Anyone can get malaria. Most cases occur in people who live in countries with widespread malaria. People from countries with no malaria can become infected when they travel to countries with malaria.

Plasmodium falciparum  is the type of malaria that most often causes severe and life-threatening malaria. It is very common in many countries in Africa south of the Sahara Desert.

Populations most at risk

Individuals with the most risk of getting very sick and dying from malaria include

• People who have little or no immunity to malaria. This can include young children and pregnant women or travelers coming from areas with no malaria.
• People heavily exposed to the bites of mosquitoes infected with P. falciparum .
• People living in rural areas who lack access to health care.

Due to these risk factors, an estimated 90% of deaths caused by malaria occur in Africa south of the Sahara Desert. And most of these deaths occur in children under 5 years of age.

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Open Access

Peer-reviewed

Research Article

Modeling the shared risks of malaria and anemia in Rwanda

Roles Conceptualization, Data curation, Formal analysis, Investigation, Validation, Visualization, Writing – review & editing

* E-mail: [email protected]

¶ ☯ All these authors are contributed equally to this work.

Affiliation African Institute for Mathematical Sciences (AIMS), Kigali, Rwanda

Roles Methodology

Affiliation African Centre of Excellence in Data Science, University of Rwanda, Kigali, Rwanda

Roles Supervision

Affiliations African Institute for Mathematical Sciences (AIMS), Kigali, Rwanda, Department of Statistics, Federal University of Technology, Akure, Nigeria

• Pacifique Karekezi, 
• Jean Damascene Nzabakiriraho, 
• Ezra Gayawan

• Published: April 22, 2024
• https://doi.org/10.1371/journal.pone.0298259
• Peer Review
• Reader Comments

In sub-Saharan Africa, malaria and anemia contribute substantially to the high burden of morbidity and mortality among under-five children. In Rwanda, both diseases have remained public health challenge over the years in spite of the numerous intervention programs and policies put in place. This study aimed at understanding the geographical variations between the joint and specific risks of both diseases in the country while quantifying the effects of some socio-demographic and climatic factors. Using data extracted from Rwanda Demographic and Health Survey, a shared component model was conceived and inference was based on integrated nested Laplace approximation. The study findings revealed similar spatial patterns for the risk of malaria and the shared risks of both diseases, thus confirming the strong link between malaria and anaemia. The spatial patterns revealed that the risks for contracting both diseases are higher among children living in the districts of Rutsiro, Nyabihu, Rusizi, Ruhango, and Gisagara. The risks for both diseases are significantly associated with type of place of residence, sex of household head, ownership of bed net, wealth index and mother’s educational attainment. Temperature and precipitation also have substantial association with both diseases. When developing malaria intervention programs and policies, it is important to take into account climatic and environmental variability in Rwanda. Also, potential intervention initiatives focusing on the lowest wealth index, children of uneducated mothers, and high risky regions need to be reinforced.

Citation: Karekezi P, Nzabakiriraho JD, Gayawan E (2024) Modeling the shared risks of malaria and anemia in Rwanda. PLoS ONE 19(4): e0298259. https://doi.org/10.1371/journal.pone.0298259

Editor: Clement Ameh Yaro, University of Uyo, NIGERIA

Received: February 28, 2023; Accepted: January 22, 2024; Published: April 22, 2024

Copyright: © 2024 Karekezi 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 paper and its Supporting information files.

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

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

Introduction

In sub-Saharan Africa, malaria and anemia contribute substantially to the high burden of morbidity and mortality among under-five children. In Rwanda, both diseases have remained as public health challenge over the years in spite of the numerous intervention programs and policies put in place. The well-being and survival chances of women and young children have continued to be endangered by the diseases [ 1 , 2 ]. The occurrence and magnitude of other diseases and malnutrition are exacerbated by malaria parasite leading to severe morbidity and mortality in some extreme cases. Malaria parasites can consume iron molecules in an individual’s red blood cell causing low functional hemoglobin concentration. In the case of young children, low hemoglobin concentration results in severe anemia and prevents quick recovery [ 3 ]. Anemia, commonly caused by iron deficiency and this occurs in situation where there is insufficient amount of iron in the red blood cells [ 4 ]. Malaria parasites feed on iron in the blood cell, leading to shortage of hemoglobin (Hb) concentration level. Thus, there are synergies between the causal relationship of malaria and anemia. Plasmodium falciparum can encroach into the red blood cell leading to acute hemolysis thereby hindering the proper development of the red cell, causing severe anemia [ 5 ]. On the other hand, severe anemia worsens morbidity from malaria particularly in children [ 6 ].

In both the tropics and subtropics, anemia is considered a health risk for under-five children particularly for those who simultaneously suffer from malaria [ 7 ].

It is a condition in which the blood is in short of healthy red blood cells, which could be due to malfunctioning of existing red blood cells that affects the flow of oxygen to the body tissue [ 8 ]. Under-five children and pregnant women are most affected by the global public health issue; with the World Health Organization estimating that 42% of children under this group and 40% of pregnant women are anemic worldwide [ 9 ]. Children who suffer from anemia experience increased heart rate, poor wound and tissue healing, poor cognitive development all of which compromise the child’s quality of life [ 10 ].

Malaria and anemia put direct pressure on the already fragile health care systems of developing countries, and also negatively affect individuals and households because of the loss of income and other economic consequences that arise due to loss of man-hour occasioned by the time spent during the recovery process or in taking care of the sick one [ 2 ]. Many developing countries are malaria endemic, where a huge proportion of the annual documented 300 million clinical cases and 2 million deaths take place. For instance, in 2019, 95% of the 229 million reported malaria cases came from 29 developing, while malaria deaths were put at 409, 000 and about 67% of this number occurred among under-five children [ 11 ].

Sub-Saharan African countries jointly account for about 93% of all malaria cases and 94% of malaria deaths that took place in 2018 with majority of the death reported among under-five children [ 9 ]. This is in spite of the multiple evolving government policies coupled with interventions from international development agencies. In Rwanda, malaria is the second leading cause of morbidity and is responsible for about 7.4% per cent of outpatient hospital visits and 4.3% of malaria proportional mortality [ 12 ]. Prior to year 2012, the country experienced a downward trend in malaria cases culminating to a record low of 48 per 1,000. However, between this period and 2016, there was a reversal in the gains that saw the number of reported cases rising to about 403 per 1,000 in 2016 [ 13 ].

Consequently, malaria gains in the country can be considered fragile and sustained policies that can push back new cases need to be scaled up. Human activities and behaviour, climatic change, environmental modification, and insecticide resistance play important roles in the sudden surge in cases [ 13 , 14 ]

The incidence of malaria has been linked to altitude, with a higher prevalence in lowlands than in highlands settings, and more cases occur around May-June and November-December. In addition to favorable climate, closeness to marshlands, irrigation schemes, and movement of people within and across geographical border influence the transmission, particularly in the Southern and Eastern fringes of the country [ 14 , 15 ]. As earlier argued, higher malaria risk in a given location would also imply higher risk of anemia particularly in children.

Several studies have been undertaken to evaluate the incidence and determinants of malaria and anaemia among under-five children in Rwanda including their geographical distributions [ 1 , 14 , 16 – 18 ]. However, limited efforts have gone into modeling the possible co-morbidity of the two disease, and there exists a persistent knowledge gap in their spatial overlap that specifically highlight districts with high and low risks of the combined diseases. Moreover, only few studies have mapped malaria and anaemia prevalence while controlling for climatic conditions particularly temperature and rainfall in the country. It is important to understand the patterns of the spatial overlap of both (shared) and specific risks from malaria and anaemia at small scale levels across the country, and to quantify the dynamics of climatic conditions for the two diseases as these could effectively aid intervention programs that are aimed at addressing their occurrence among young children. Consequently, this study was designed to estimate the shared and specific spatial patterns of malaria and anemia among children under five years of age in Rwanda using data extracted from the 2014–2015 Rwanda Demographic and Health Survey (RDHS). We use a shared-component modeling approach within a Bayesian framework allowing for simultaneous estimation of metrical variables as nonlinear effects, location-specific random effects that account for spatial heterogeneity, and the usual linear effects of categorical variables. The model enables the distinct estimation of the underlying risk surface for the diseases in the form of a component shared by both diseases (refered to as the shared-component) and others that are specific to each disease (disease-specific components). The shared spatial component can be viewed as a surrogate for unobserved covariates that influence the spatial structure of both diseases. We considered the effects of temperature and rainfall as climatic in addition to other demographic factors on the shared risks of the two diseases. To produce approximations to the posterior marginals of all parameters of interest, we adopt the integrated nested Laplace approximations (INLA) approach.

Materials and methods

The study used data obtained through the 2014–2015 Rwanda Demographic and Health Survey (RDHS). The survey, implemented by the National Institute of Statistics of Rwanda in partnership with the Rwanda Biomedical Center (RBC) and Rwanda Ministry of Health (MoH) between November 2014 and April 2015, provide essential data for quantifying and monitoring important demographic and health indicators at the national level, the five provinces, each of Rwanda’s 30 districts and for urban and rural areas. The survey was executed through a two-stage sampling design where enumeration areas (EAs), referred to as clusters, were selected at the first stage from the sampling frame used during the 2012 Rwanda Population and Housing Census (RPHC). A total of 492 clusters comprising 113 in urban and 379 in rural areas were selected. The second stage involves the selection of households from the listed EAs, which were picked at random. A total of 12,793 households were selected comprising of about twenty-six households from each EA.

Eligible women for interview were those aged 15 to 49 years who were the permanent residents of the selected households or those who slept in the households the night before the survey. There were 13,564 eligible women in the selected households and 13,497 were successfully interviewed, yielding a response rate of 99.5 percent. Information was also collected on children younger than five years of age from the caregivers in all the households. Anemia and malaria testing were executed in the sub-sample of households not selected for the male survey. After informed consent was obtained from the caregiver, children in these households were tested for malaria and anemia. The malaria test was executed through the rapid diagnostic test (RTD) and thick and thin blood smears. A drop of blood was taken by pricking the end of the finger in the case of RDTs and this was also used for anemia testing.

The response variables of interest were created from the malaria and anemia indicators with each variable taking the value of one if the child suffers from the ailment and zero if otherwise.

The independent variables considered include type of place of residence, sex of a household head, bed-net ownership, bed-nets usage, household wealth index, mother’s educational attainment, child’s sex, child’s age, and age of household head. The district of residence was geo-referenced. Furthermore, climate-related factors including temperature and rainfall were obtained from the GPS data set of the 2014–2015 RDHS to examine their effect on malaria and anemia co-morbidity. We extracted the shapefile of Rwanda from the Spatial Data Repository put together by The DHS Program [ 19 ]. This was used in constructing the adjacency matrix for the districts of Rwanda used in our Bayesian model and for plotting the estimates on maps.

Ethics statement

The study used a secondary data obtained from the Demographic and Health Survey after approval was secured. It should be noted that DHS adopts a coordinate displacement process to ensure the preservation of the identity of the respondents. Urban clusters are displaced on a distance of up to two kilometers and up to five kilometers for rural clusters. However, this would have minimal effect on our analysis since we used an area-level spatial approach that considers the districts of Rwanda hence every sampled individual would belong to a district notwithstanding the displacement of the coordinate.

Statistical analysis

Shared component model..

We implemented the model through a Bayesian inference that relies on the integrated nested Laplace approximation (INLA) as proposed by [ 21 ]. The prior distribution for σ d was log-normal with a mean of 0 and accuracy of 0.1. A weakly informative Gaussian prior with small precision τ β on the identity matrix was considered, and used for the fixed parameters and constant term, that is β ∼ N (0, τ β I ).

Data preparation and frequency tables were generated using Stata 14 while the Bayesian model was implemented using the R-INLA package.

Table 1 presents the descriptive analysis of the co-morbidity of malaria and anemia based on household characteristics of the under-five children. Overall, about 49% (1673/3446) of the children had malaria, anemia, or both. About 7.5% (259/3446) had malaria, 35.6% (1228/3446) had anemia, and another 5.4% (186/3446) suffered both malaria and anemia. Among the under-five children from rural areas, a greater proportion had malaria 8.7%, (239/2738), 36.9% (1009/2738) suffered anemia whereas 6.2% (169/2738) had both malaria and anemia. Among the children from female headed households, 10.4% (74/709) suffered malaria while 7.8% (55/709) had anemia and malaria. On other hand, slightly high proportion (35.7%, 976/2737) of children from male-headed households suffered anemia when compared with with female-headed households (35.5%, 252/709). Among children from households with no bed nets, 9.9% (53/538) suffered malaria, 37.7% (203/538) had anemia, and 8.6% (46/538) suffered both malaria and anemia. The proportion of the children who suffered malaria, anemia, or both illnesses varies with the use of bed nets such that 9.5% (27/284) of children from households in which some slept under bed nets suffered malaria, whereas 7.8% (75/967) of children who did not sleep under bed nets suffered both malaria and anemia. Children from the richest households were less likely to suffer the episodes of both malaria and anemia (0.5%, 3/627). Contrarily, among children from poorest households, about 10.1% (86/852) suffered both malaria and anemia. Children whose mothers attained at least primary education are less likely to suffer malaria, anemia, or both. The study findings also show that the proportion of children who had malaria, or both malaria and anemia did not vary with child’s sex. However, slightly high proportion of male children had anemia (36.7%, 645/1757).

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Table 2 presents results of the linear effects for malaria and anemia showing the posterior means, standard deviations, and 95% credible intervals. When compared with children from rural areas, those from urban settings are less likely to develop both diseases, though the estimate is not significant. Children from male-headed households are less likely to have both diseases compared with those from female-headed households. Whereas ownership of bed nets in households shows lower likelihood for contracting both diseases, the estimates for usage are not significant. The study findings revealed an association between wealth quintile and coexistence of the two diseases such that children from at least the poorer households are less likely to contract both diseases when compared with those from the poorest households. Children whose mothers attained primary level of education are less likely to suffer from both diseases when compared with those with no education but the result for secondary/higher education is not significant. The findings on the sex of the children show non-significant effects.

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The results for the spatial effects presented in Figs 1 to 12 , show the maps for the posterior means, standard deviations, and 95% credible intervals, respectively for the shared effects of malaria and anemia, specific-effects for malaria and for anemia, with the results displaying uneven distributions of the burden of the diseases across the districts of Rwanda. The findings from the shared random effects (Figs 1 to 4 ) reveal that the highest risks of contracting malaria and anemia can be found among children from Rutsiro, Nyabihu, Ruhango, Gisagara, and Rusizi districts, while those from Rubavu, Karongi, Ngororero, Kayonza, Gatsibo, Rwamagana, Gasabo and Rulindo have moderate risks. The joint effects of Malaria and anemia seem to be negligible across the other districts of the country. The standard deviation and credible intervals maps show that there is more uncertainty about the risk of malaria and anemia in various parts of the country, particularly in the districts of Nyagatare, Rubavu, Ruhango and Nyamasheke.

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In terms of the specific components, the spatial distributions for malaria (Figs 5 to 8 ) reveal a pattern that is somewhat similar to the shared spatial pattern obtained for the combined diseases. Specifically, the risks for malaria are highest among children living in Rutsiro, Nyabihu, Ruhango, Rusizi and Gisagara districts but moderate for those residing in Gatsibo, Kayonza, Rwamagana, Gasabo, Rulindo, Karongi, Ngororero, and Rubavu. However, the risks are lowest among those children living in Gakenke, Nyagatare, and Kirehe districts. The standard deviation and credible interval maps reflect high uncertainty in the districts of Rubavu, Kirehe, Nyagatare, Rusizi, Nyamasheke, Nyaruguru and Gisagara. In the case of anemia (Figs 9 to 12 ), the risks are higher among the children living in Rutsiro, Nyabihu, Rulindom, Ngoma, and Gisagara, followed by the districts of Rusizi, Huye, Nyanza, Ruhango, Ngororero, Gakenke, Gasabo, Nyarugenge, Kicukiro, and Kayonza. However, the risks for anemia are lower in the districts of Nyamasheke, Nyamagabe, Karongi, Muhanga, Kamonyi, Bugesera, Rwamagana, Gatsibo, Gicumbi, Nyagatare, Burera, Musanze and Rubavu. Nyaruguru and Kirehe.

The nonlinear effects of child’s age, age of household head, annual precipitation and mean temperature for the shared effects are presented in Figs 13 to 16 while those for the specific effects of malaria and anemia are presented in Figs 17 to 24 respectively. The Figures show the posterior means (middle lines) surrounded by the 95% credible intervals. The findings show a negative relationship between the likelihood of suffering from both diseases and the age of the child, indicating that as a child gets older, the likelihood of suffering from both diseases decreases. The estimates for household head show higher likelihood among children whose head of household is 75 years or older. For precipitation, the likelihood of shared risk increases with precipitation up to 120 mm/day, but starts decreasing when precipitation exceeds 120 mm/day though the credible intervals are generally wider. The findings revealed a positive association between temperature and risk of contracting both diseases, such that as temperature increases, the children become more prone to the two illnesses.

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The findings for malaria Figs 17 to 20 reveal a positive association between the likelihood of having malaria and child’s age up to around 30 months but beyond this age, the likelihood decreases. As for the shared pattern, the likelihood of suffering from malaria increases for children whose household heads are older than 75 years, but lower before this age. The chances of having malaria increases with precipitation below 135 mm/day, but beyond this point, the chances of having malaria decreases. As for temperature, the study findings reveal wider credible intervals reflecting higher uncertainty around the estimates thus, the estimates may need to be interpreted with caution. The non-linear effects of child’s age, age of household head, annual precipitation and mean temperature estimated for anemia are presented in Figs 21 to 24 . The findings show a negative association between the risk of having anemia and the child’s age similar to what was obtained for the shared component, while in the case of age of household head, the risks are similar throughout the ages. Moreover, the risk of having anemia rises with increase in precipitation while the estimates for temperature appears flat but with wider credible interval.

A shared component modeling approach was utilized to map co-morbidity of malaria and anaemia among under-five children in Rwanda. The Bayesian spatial model allows the mapping of spatial phenomena across small geographical units and to quantify the effects of both socio-demographic and climatic factors on co-morbidity of the diseases. The findings from the study have practical relevance in a country like Rwanda where children still suffer co-morbidity from several diseases. Moreover, they provide evidence for effective and efficient implementation of intervention programs and policies designed to eliminate malaria and anaemia in Rwanda. The linear effects have shown the significant association between socio-demographic characteristics of the children and co-morbidity from the two diseases. The findings show no significant difference in the likelihood of suffering from both disease among the under-five children residing in urban and rural areas. However, findings from some African countries have shown that under-five children from urban settings are less likely to suffer from both malaria and anaemia when compared with those from rural settings [ 23 , 24 ], while a Rwandan study has demonstrated lower likelihood for malaria among urban children [ 1 ]. In most rural settings in Rwanda, where more than two-thirds of the population reside, the majority of the caregivers are farmers and small scale traders who have limited access to information on disease control and prevention methods when viewed in respect to the urban dwellers. They equally suffer from acute presence of health professionals and healthcare facilities as is the case in many developing countries, and thus, overstretching the available few [ 1 ].

The findings of the study demonstrate inverse relationship between household wealth and the likelihood of co-morbidity from malaria and anaemia indicating that as wealth increases, the chances of co-morbidity reduces. These findings are consistent with those of [ 25 , 26 ], indicating that children from impoverished households have higher prevalence of malaria compared with those from wealthy families. This may be attributed to lack of ability to afford adequate and balanced diet for children from poor families. Moreover, wealthy households would have adequate resources to acquire preventive and curative measures that safe guide their children from diseases. The similar significant association between household wealth and likelihood of having malaria and anaemia among under-five children have been reported in several other places [ 2 , 24 ].

We found that bed nets ownership reduce the risk of co-morbidity from malaria and anaemia but this was not the case for usage. Regular use of bed nets especially insecticide treated nets is a major vector control measure to prevent malaria and by extension, anemia [ 25 ]. A previous analysis of the data used in this study but where only malaria was consider revealed that both ownership and usage of bed nets reduce the risk of malaria [ 1 ]. The non-significant estimate obtained for usage in this case might have indicated that the usage of bed nets is not sufficient to cause a difference in co-morbidity from both diseases as it does for only malaria. Similar to some previous studies, we found children from male-headed household to be less prone to co-morbidity from the two diseases [ 26 , 27 ]. As with most sub-Saharan African countries the majority of Rwandan households are male-headed who often provide protective leads to members of the family than what can be obtained in households headed by female. We however found no substantial difference when the sex of the child was considered.

The findings show an association between mother’s educational attainment and likelihood of co-morbidity from the diseases. Children whose mothers completed at least primary education are less likely to suffer from both diseases. This association may be linked with the fact that higher educational attainment lead to improved knowledge, perception, and practice about strategies for preventing and treating diseases [ 28 , 29 ]. Educated mothers are at a vintage position to know where to find and how to expressed themselves to physicians such that their children get the best of treatments than the uneducated ones will do.

The study findings revealed spatial heterogeneity in the shared risks of malaria and anaemia, and also from the individual diseases among under-five children in Rwanda. It is interesting to note that the spatial pattern obtained for malaria is similar to that observed for the shared risks of the two diseases more than does the map obtained for anemia. This finding further reinforces the synergy between the epidemiology causal pathways of malaria and anemia, which ensures that anemia is often a complication that could arise from multiple episodes of malaria [ 2 ]. Districts with substantial high risks include Rutsiro, Nyabihu, Ruhango, Gisagara, and Rusizi, while moderate risks were estimated for Rubavu, Karongi, Ngororero, Kayonza, Gatsibo, Rwamagana, Gasabo and Rulindo. The majority of the districts with high risks are places with high rates of illiteracy and poverty which would limit caregivers ability of protect their children from infectious diseases [ 22 ]. The existence of Gishwati forest, in which many agricultural and farming activities take place, could aggravate the risks for both diseases in the districts of Rutsiro and Nyabihu [ 30 ]. Also, the higher risk of co-morbidity of these diseases in Rusizi district may be compounded by the abundance of breeding sites for anopheles mosquitoes in the Nyungwe forest and Bugarama plain as reported by [ 31 ]. The high temperature often experienced in the Bugarama plain, a rice farming environment, could also increase the risk of malaria transmission by mosquitoes [ 32 ]. The presence of several agricultural activities in Ruhango and Gisagara, coupled with cross border movement can define the increased likelihood of co-morbidity of malaria and anaemia. The irrigation-based agricultural practices mainly in the wetlands of the Eastern and Southern parts of the country has been reported to influence malaria through the creation of vector breeding sites [ 33 ]. The observed spatial variation could be also linked with numerous factors including spatial disparity in human behaviour, awareness, and media exposure to malaria, child feeding practices, and disease prevention strategies. The high prevalence of malaria across the western provinces can be further explained by the presence of Lake Kivu which has been reported to speed up malaria transmission [ 34 ].

The findings established nonlinear relationships between the shared risk of the two diseases and child’s age, age of household head, annual precipitation, and mean temperature, which were considered as metrical covariates. The findings show high likelihood for the shared risks of malaria and anemia among children below 24 months of age, and this is similar to what was obtained for the specific component of anemia. Findings from other African countries have similarly exhibited this pattern of relationship [ 4 ]. The first two years of life is a period of intense growth and development, making the children to have high demand for iron, but which may not be available in the required quantity particularly for children from low socio-economic settings. Weaning food may also be obtained from some unhygienic sources which could aggravate the risk of illness and subjecting the child to anemia. Moreover, due to the fragile nature of these children, they are highly susceptible to infections.

Temperature was revealed to be positively associated with the shared risks of malaria and anaemia. An increase in temperature could shorten the time period it takes for new generations of mosquitoes to emerge, as well as the parasite’s incubation period in mosquitoes [ 35 ]. Using an ecological model with malaria transmission data across African countries, [ 36 ] revealed that malaria transmission is at its optimal around temperature of 25° C , but this decreases substantially when temperature exceeds 28° C . The findings on annual precipitation reveals that when it is below 120 mm/day, the likelihood of co-morbidity of malaria and anemia increases with precipitation but when it is exceeds 120 mm/day, the risk decreases. Precipitation greater than 140mm destroys mosquitoes sites and leads to decrease in malaria transmission. The amount of precipitation determines the ample quantity and length of malaria transmission across different locations in a manner that in lower altitude regions, increase in precipitation might go with increase of available anopheles sites [ 37 , 38 ].

This study suffers from some limitations that need to be mentioned. The study was based on district level data but this could mask fine-scale variations because the districts are composed of several spatial units. A further analysis that creates maps at a continuous scale could provide more information on local variations than is obtainable here. As with similar studies that use data from cross-sectional survey, we were unable to make causal inference from our findings. An observational study in each of the districts could provide more information regarding the pattern of infection from malaria and anemia and why they vary from place to place. Furthermore, there are possibilities of bias responses to questions that seek to elicit information on ownership and use of bed nets as the accuracy depends solely on the willingness of the respondents to provide the right response. The wealth index variable that classified the children into different wealth strata, was also computed based on households assets commonly found in urban areas whereas, most rural dwellers who could posses other wealth indicators like livestock or other farm machinery would be classified in the lowest categories resulting in mis-classification. All these notwithstanding, the data source provide adequate information that allow for spatial analysis as done here and this provide information that can enhance intervention in the country.

This study aimed at understanding the shared spatial risks of malaria and anemia among under-five children in Rwanda using a shared component model while controlling for other important determinants. The study reveals that socio-demographic characteristics such as place of residence, mother’s educational level, wealth index, sex of household head, bed net ownership are among the major risk factors of the shared risk of the two diseases among Rwandan children. Rising precipitation particularly above 120 mm/day is associated with decreasing risk of co-morbidity of diseases. Furthermore, the risk of developing both diseases increases as the temperature rises. Findings from the study allow for the identification of the uneven spatial variations in joint and specific risks of suffering from malaria and anemia among young children in the country. Specifically, children from Rutsiro, Nyabihu, Ruhango, Rusizi, and Rusizi districts are particularly at higher risks. The regional variation of malaria is nearly identical to the spatial pattern of the shared risk of both diseases, indicating that malaria could the leading driver of anemia among children in the country. The study recommends considerable efforts to improve the existing intervention programs and control strategies that prioritize higher risk regions. Moreover, special attention needs to be accorded to individuals living in lowest wealth quintiles, female headed households, and children of uneducated mothers when developing malaria and anemia intervention programs and policies. Also, the study recommends that when formulating malaria and anemia intervention programs, climate and environmental factors particularly temperature and precipitation should be taken into account.

Supporting information

https://doi.org/10.1371/journal.pone.0298259.s001

Acknowledgments

PK is grateful to AIMS Rwanda for scholarship towards a master program during which the study was undertaken. The authors appreciate permission from The DHS Program to utilize the data set analysed in the study.

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The Bombastic 19th-Century Anti-Vaxxer Who Fueled Montreal's Smallpox Epidemic

“VACCINATE! VACCINATE!! VACCINATE!!! THERE’S MONEY IN IT!!! TWENTY THOUSAND VICTIMS!!! will be Vaccinated within the next ten days in this City under the present ALARM!!! That will put $10,000 into the pockets of the Medical Profession.” In case all the exclamation points and capitalized letters didn’t do the trick, Alexander Milton Ross embellished his poster with a large drawing of a police officer restraining a mother while Death vaccinated her child. It was terrifying, no doubt. For extra emphasis, the police officer held a piece of paper that read “Vaccination for the Jenner-ation of Disease,” a reference to the English physician Edward Jenner, who developed and promoted vaccination.

In 1885, Canada had no greater adversary of smallpox vaccination than Ross, an Anglo-Canadian physician and naturalist whose medical training was informed by the sanitary movement of the 19th century. Opposed to the germ theory emerging in Europe (that same year, Louis Pasteur’s rabies vaccine was announced to the world), Ross believed that smallpox was a filth disease and its only antidote was cleanliness. And though it’s true that smallpox could spread through soiled fabrics used by smallpox patients (such as bedding and clothing), its primary route of transmission was virus-laden respiratory droplets. The real danger thus lay in close and prolonged contact with smallpox patients, independent of how clean the setting was.

Vaccination, in Ross’s mind, was poisonous. He wanted everyone to know it too. Besides papering the city of Montreal with antivaccination posters and pamphlets, writing letters to newspapers and professional journals, and founding a magazine called the Anti-Vaccinator , he formed the Canadian Anti-Vaccination League as part of an international antivaccination crusade. “Though Police and the Profession cry Vaccinate! Vaccinate!! Vaccinate!!! and people in thousands follow their blind leaders, — I still say, DON’T,” Ross urged in a circular that he distributed throughout the city.

Ross believed that smallpox was a filth disease and its only antidote was cleanliness.

At the time, Montreal was struggling to fight off the largest epidemic of smallpox that it would ever face. For almost a century, smallpox vaccination had been widely used to prevent the disease, but many of the city’s inhabitants had refused the procedure.

Some of the holdouts were surely persuaded by Ross and his English-only propaganda. But most of the unvaccinated population and therefore the bulk of the cases consisted of French Canadians. To convince them of the evils of vaccination, French Canadian physician Joseph Emery Coderre formed the first Canadian antivaccination society in Montreal and published numerous antivaccination pamphlets in French in the 1870s. His ardent antivaccination views fed the fervor of protesters who attacked the city council in 1875, halting efforts to enact mandatory smallpox vaccination in Montreal and leaving the city vulnerable to devastating disease 10 years later. When compulsory vaccination was attempted again in 1885, the riot was even bigger. Shortly thereafter, Coderre and colleagues created an antivaccination journal , L’Antivaccinateur canadien-français , the Francophone counterpart to Ross’s magazine.

The misinformation promoted by Ross, Coderre, and their contemporaries should be familiar to anyone with a social media account in the 21st century. First off, they downplayed the threat of the epidemic in Montreal. Francophone newspapers wrote little about it, except to dismiss the panic, while Ross stressed in one of his pamphlets, “CAUTION. Do not be alarmed by the smallpox.” Simultaneously, they insisted that vaccination was the true danger. In the Anti-Vaccinator , Ross explained that vaccination didn’t prevent smallpox and actually infected people with the smallpox virus, along with other equally lethal pathogens. Coderre likewise insisted that victims of vaccination were everywhere. His writings included pages of individuals whom he believed were sickened or killed by the vaccine, either from contracting smallpox or some other malady such as gangrene and syphilis.

And then, of course, they spouted conspiracy theories. Provaccination doctors were accused of profiting from the practice, as Ross broadcast in his poster. One French Canadian doctor, in an open letter to Coderre published by the medical journal L’Union Médicale du Canada in 1875, laid out the same charge. He also perceived another conspiracy among English physicians in particular, attributing their advocacy of the smallpox vaccine to nationalistic conflicts of interest given that English physician Jenner was associated with it. Coderre replied in agreement, affirming that English doctors and public vaccinators practiced vaccination par intérêt — purely out of self-interest. These beliefs were consistent with a general distrust of the Anglophone elite, whose vaccines were seen as both poisoning and punishing the French Canadian community , which mostly lived in overcrowded tenements in the poorest quarters of the city.

Their arguments are reminiscent of misinformation during subsequent epidemics and pandemics, all the way up to the present. It’s also noteworthy that while Ross thought sanitation was the answer to smallpox, Francophone newspapers printed recipes for at-home remedies , such as buckwheat root or mixtures of zinc sulfate, digitalis, and sugar. (A cure was never found for smallpox before its eradication, and treatments generally consisted of cleaning the wounds and easing the pain of the ill.) These ideas are akin to the popularization in the United States of non-FDA-approved treatments for COVID-19, such as ivermectin (an antiparasitic agent used to treat patients with certain worm infections and head lice) and hydroxychloroquine (a medication used for malaria and autoimmune conditions such as lupus and rheumatoid arthritis), which many people learned about through the internet, social media, and celebrity testimonials. Despite early hopes, neither of them turned out to be effective for preventing or treating COVID-19. But without any specific treatments for COVID-19 until long into the pandemic, it’s not surprising that some patients opted to take risks with these unproven remedies rather than heed public health warnings against them. Some physicians even participated in misinformation about the efficacy of these drugs and continued to prescribe them for COVID-19. And although many studies haven’t observed that ivermectin and hydroxychloroquine cause serious adverse effects in COVID-19 patients, they can still be dangerous if the patients forgo evidence-based COVID-19 treatments or vaccination against SARS-CoV-2 as a result of using them, as editors at the Journal of the American Medical Association pointed out last year .

To be fair, smallpox vaccination was far from perfectly safe in the late 19th century. Even Jenner himself couldn’t explain how his vaccine worked, and some methods (such as passing infectious material directly from the arm of a vaccinated person to an unvaccinated one) undoubtedly had the potential to introduce other infections. There were also some cases where children may have died as a result of faulty vaccine preparations. Furthermore, even if the vaccination was successful, it didn’t guarantee complete or lifelong immunity. Antivaccinationists, though, were incorrect about the risks and effects of the vaccine. And their dishonesty, at least in the case of Ross, raised questions about their own motives.

One State Board of Health report called him “a monster in human form who desired that a most terrible disease should decimate his patrons, that he might grow fat on their putrid bodies.”

Ross, the bombastic pamphleteer, was apparently a hypocrite at heart. In October 1885, while the smallpox epidemic was still raging in Montreal, he boarded a train to Toronto. As reported afterward by the Gazette , a medical inspector at the Ontario border asked Ross to show proof of recent smallpox vaccination, either in the form of a certificate or scar. It was a standard policy for travelers, but Ross tried his best to get out of it. Then when he couldn’t produce a certificate, he reluctantly took off his coat, rolled off his sleeve, and revealed “three perfect vaccination marks” on his arm. One of them was relatively fresh, and the others were from infancy and childhood, according to Ross. The article about the incident offered little by way of commentary, except to note the long history of doctors who believed in the efficacy of vaccination but opposed the practice since they would lose a source of revenue if smallpox declined. (Similarly, during the COVID-19 pandemic, the Fox News channel was a top broadcaster of vaccine skepticism in the United States, even though nearly all of the corporation’s employees were vaccinated .)

The news about Ross reached the United States, where it was met with outrage among the public health community. One State Board of Health report called him “a monster in human form who desired that a most terrible disease should decimate his patrons, that he might grow fat on their putrid bodies.”

By the end of the smallpox epidemic in Montreal in 1886, more than 3,200 people had died from the disease. The city lost almost 2 percent of its total population in 1885 alone, and more than 3 percent of its French Canadian community. Most of them were children. There were numerous blunders that helped the disease spread, as historian Michael Bliss recounts in his book “Plague: How Smallpox Devastated Montreal,” and the large population of unvaccinated children created by fear and ignorance was a major factor. Every one of the deaths could have been prevented, Bliss emphasizes. Unfortunately, it wasn’t until the disease ran out of unvaccinated or otherwise vulnerable hosts that the epidemic finally waned.

Misinformation about diseases is a timeless human challenge. Some opinions offered about the antivaccination riot in Montreal, such as in a New York Times editorial in 1875, ring a bell 150 years later. With shock that anyone would harbor such an absurd preconception against vaccination, a triumph of modern medicine, the editorial lamented that “in spite of all our boasted progress, curious revelations of popular ignorance and superstition are constantly showing us how little progress has been made.” But after laying blame on the fortune tellers in large cities, the quacks in medicine that flourished everywhere, and even the scientific research and scholarly writings that went above the heads of the public, there was still optimism: “When knowledge is more evenly distributed, there will be less of this fantastic and ignorant prejudice.”

Evenly distributed knowledge? That sounds a lot like the internet to me.

Sabrina Sholts is the curator of biological anthropology at the Smithsonian’s National Museum of Natural History, where she developed the major exhibit “Outbreak: Epidemics in a Connected World.” She is the author of “ The Human Disease ,” from which this article is excerpted.

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Melania Trump Avoids the Courtroom, but Is Said to Share Her Husband’s Anger

Melania Trump has long referred to the hush-money case involving Stormy Daniels as her husband’s problem, not hers. But she has privately called the trial a “disgrace” that could threaten his campaign.

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By Katie Rogers

Katie Rogers is the author of a book on first ladies and covered the Trump White House, including Melania Trump’s East Wing.

In January 2018, when she first saw reports that her husband had paid off a porn star, Melania Trump was furious. She jetted off to Palm Beach, leaving the president to languish in Washington. She eventually returned, only to take a separate car to Donald J. Trump’s first State of the Union address.

As a criminal trial against Mr. Trump opened on Monday , on charges that he had falsified records to cover up that sex scandal involving Stormy Daniels, Mrs. Trump did not appear. She has long privately referred to the case involving Ms. Daniels as “his problem” and not hers.

But Mrs. Trump, the former first lady, shares his view that the trial itself is unfair, according to several people familiar with her thinking.

In private, she has called the proceedings “a disgrace” tantamount to election interference, according to a person with direct knowledge of her comments who could not speak publicly out of fear of jeopardizing a personal relationship with the Trumps.

She may support her husband, but Mrs. Trump is bound to see headlines involving Mr. Trump and Ms. Daniels that could reopen old wounds. On Monday, Justice Juan M. Merchan, the judge presiding over the case, also said that Mrs. Trump could be among the potential witnesses as the trial gets underway.

All of this could put Mr. Trump on shaky ground with his wife, who has defended him in some critical moments — including when he bragged on tape about grabbing women by their genitals — and withheld her public support in others, like when she did not appear alongside him as he locked up victories on Super Tuesday.

“At the end of the day, she can make or break his candidacy,” said Stephanie Grisham, Mrs. Trump’s former press secretary who resigned on Jan. 6, 2021, and went on to write a memoir. “And at the end of the day, she could probably make or break him.”

Some of the more personally damaging details of Mr. Trump’s behavior may not come up in court. On Monday, Justice Merchan barred some testimony related to the timing of a reported affair between Mr. Trump and a former Playboy model, Karen McDougal. The National Enquirer, which has longstanding ties to Mr. Trump, bought the rights to Ms. McDougal’s story for $150,000 and then never published it — a practice known as “catch and kill.”

Jurors may hear about the relationship between Mr. Trump and Ms. McDougal, Justice Merchan ruled — but not accounts that the affair continued while Mrs. Trump was pregnant with their son, Barron. (If the court proceedings bring up Barron, whose privacy his mother fiercely guards, Ms. Grisham said, Mrs. Trump is likely to be “not happy” with her husband “all over again.”)

The trial is nonetheless all but certain to examine a timeline that Mrs. Trump would prefer not to revisit. Mr. Trump and Ms. Daniels met at a 2006 celebrity golf tournament, at a time when the Trumps had been married for a year and Mrs. Trump had recently given birth to Barron.

Mr. Trump has denied having a sexual encounter with Ms. Daniels. But prosecutors say that when Ms. Daniels looked to sell her story a decade later, Mr. Trump directed Michael D. Cohen, then his lawyer and fixer, to pay Ms. Daniels $130,000 to keep quiet. The reports of a payoff blindsided Mrs. Trump, who responded to the initial reports by getting out of town.

She canceled a trip to Davos, Switzerland, with Mr. Trump, made an impromptu visit to the Holocaust Memorial Museum, and then she jetted off to Mar-a-Lago, the Trumps’ beachside fortress in Palm Beach, Fla., where she spent part of her trip relaxing at the spa. She eventually reappeared, only to take a separate car to Mr. Trump’s State of the Union address and appear on the arm of a male military aide.

By now, allies of the Trumps say, Mrs. Trump has lumped the trial into all of the other legal problems her husband faces, and she is steelier than she was before.

Last month, she appeared next to Mr. Trump to welcome Viktor Orban , the prime minister of Hungary, during a visit to Mar-a-Lago. Weeks later, she voted alongside Mr. Trump in Florida, where she responded to a question about whether she would be campaigning more often with a cryptic “stay tuned.”

Supporters have hailed her scheduled appearance at a fund-raising event for the Log Cabin Republicans, a group of L.G.B.T. conservatives, as proof that Mrs. Trump is prepared to be more engaged on the campaign trail.

The event, scheduled for Saturday, will draw attendees who have paid at least $10,000 for a chance to interact with Mrs. Trump, according to a person familiar with the planning who was not authorized to detail it.

The event will be set up like a cocktail reception, and Mrs. Trump is expected to deliver remarks about her time as first lady and reiterate her support for her husband.

But there is one catch: The event will not be held in a battleground state or at any location on a traditional campaign trail. It will be held in a reception room at Mar-a-Lago, steps from Mrs. Trump’s suite.

The Log Cabin Republicans have been a source of income for Mrs. Trump before. According to a financial disclosure last year, Mrs. Trump received a $250,000 payment from the group in December 2022. Charles Moran, a representative of the group, said in an email that Mrs. Trump was not taking a fee from the Log Cabin Republicans for her appearance.

A spokeswoman for Mrs. Trump did not respond to a request for comment for this article, and neither did a representative for the Trump campaign.

Mrs. Trump’s allies say that she will likely appear again as the campaign continues — a sign, they say, that she realizes there is a real chance she could become first lady again — but that she is likely to be selective with her time.

For now, she is focused on Barron’s graduation from high school later this spring and preparing him for college. Mr. Trump complained repeatedly on social media on Monday that he might miss his son’s graduation because of the trial. Barron attends a private school near Mar-a-Lago and is expected to graduate in May.

Mrs. Trump’s allies say other personal issues could keep her from the campaign trail. She is said to still be mourning the death of her mother, Amalija Knavs, who died in January and was one of a small number of people in Mrs. Trump’s world who had her absolute trust. Her sister, Ines Knauss, is another confidante, but Ms. Knauss lives in New York City.

Another person Mrs. Trump trusts is Kellyanne Conway, who served as counselor to Mr. Trump in the White House; Mrs. Trump is pushing for Ms. Conway to return to Mr. Trump’s orbit in a formal capacity, a development first reported by the news site Puck . Ms. Conway, who was a confidante for both Mr. and Mrs. Trump when they were in the White House, has said that Mr. Trump cares deeply about his wife’s opinion — and, in some cases, he might even fear it.

“He listens to many of us,” she told a congressional committee in 2022, “but he reserves fear for one person, Melania Trump.”

Katie Rogers is a White House correspondent. For much of the past decade, she has focused on features about the presidency, the first family, and life in Washington, in addition to covering a range of domestic and foreign policy issues. She is the author of a book on first ladies. More about Katie Rogers

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