ABSTRACT
In this review, I describe the progress in a study that focused on the risk factors for schistosomiasis around the globe for the purposes of the review. Human schistosomiasis affects 229 million people; at least 90% are in sub-Saharan Africa, and 54% are school-aged children. Schistosoma haematobium infects 112 million people, Schistosoma japonicum infects 3.1 million people, and Schistosoma mansoni infects 54 million people. Schistosomiasis can occur in endemic and non-endemic areas. A high risk of schistosomiasis can occur in, for example, preschool-aged children, school-aged children, and workers in endemic schistosomiasis areas. These people make contact with infested freshwater day by day. In addition, environmental factors and socioeconomic factors can affect the transmission of schistosomiasis. Various factors can cause the transmission of schistosomiasis, for example, climate changes and proximity to infested freshwater bodies. People with high risks for schistosomiasis need great attention for treatment and/or prevention programs. Risk factors for schistosomiasis, for example, human behavior and socioeconomic status, can affect the transmission of schistosomiasis. Many developing countries in Africa, Asia, and South America are at risk of this disease. High-risk people need special attention in programs for schistosomiasis elimination.
HIGHLIGHTS
Dynamic transmission of schistosomiasis occurs in Africa, Asia, Europe, and Latin America.
Risk factors for schistosomiasis can include human behavior, women and preschool-aged children, school-aged children, and environmental factors.
(Ar)praziquantel is for preschool-aged children and praziquantel is for school-aged children, adolescents, and adults.
INTRODUCTION
Species . | Regions . | References . |
---|---|---|
Schistosoma haematobium | Africa, the Middle East, Francea, India | WHO (2023) |
Elbaz & Esmat (2013) | ||
Schistosoma guineensis | Central Africa | WHO (2023) |
West Africa | Mone et al. (2012) | |
Schistosoma intercalatum | Central Africa | WHO (2023) |
Schistosoma japonicum | The Far East (China, Indonesia, Philippines) | Nelwan (2019, 2024) |
Schistosoma malayensis | Southeast Asia (Malaysia) | Gordon et al. (2019) |
Schistosoma mansoni | Africa, the Americas, the Caribbean, the Middle East | WHO (2023) |
Nelwan (2019, 2024) | ||
Schistosoma mekongi | Southeast Asia (Cambodia and Laos) | WHO (2023) |
Gordon et al. (2019) |
Species . | Regions . | References . |
---|---|---|
Schistosoma haematobium | Africa, the Middle East, Francea, India | WHO (2023) |
Elbaz & Esmat (2013) | ||
Schistosoma guineensis | Central Africa | WHO (2023) |
West Africa | Mone et al. (2012) | |
Schistosoma intercalatum | Central Africa | WHO (2023) |
Schistosoma japonicum | The Far East (China, Indonesia, Philippines) | Nelwan (2019, 2024) |
Schistosoma malayensis | Southeast Asia (Malaysia) | Gordon et al. (2019) |
Schistosoma mansoni | Africa, the Americas, the Caribbean, the Middle East | WHO (2023) |
Nelwan (2019, 2024) | ||
Schistosoma mekongi | Southeast Asia (Cambodia and Laos) | WHO (2023) |
Gordon et al. (2019) |
Note: WHO: World Health Organization.
aCorsica.
Schistosomiasis is still a public health problem in tropical and subtropical regions; approximately 90% of cases occur in sub-Saharan Africa. Various factors can facilitate the transmission of schistosomiasis. This can comprise living near freshwater bodies, socioeconomic factors affecting work activities, and climate change (Angora et al. 2019). The transmission of schistosomiasis may have a relationship with the human immunodeficiency virus (HIV). However, the relationship between HIV and the transmission of the disease still needs more studies for confirmation. Some studies suggest that it does not have an association with HIV risk (Bochner et al. 2020). Other studies have shown that schistosomiasis increases infection with HIV (Manz et al. 2020).
Schistosoma can infect preschool-aged children (1–4 years old) (N'Goran et al. 2023), school-aged children (6–15 years old) (Yang & Zhou 2023), adolescents, and adults. (Ar)praziquantel is used to treat schistosomiasis. Praziquantel is a drug for treating all Schistosoma infections in preschool-aged children, school-aged children, adolescents, and adults (Olliaro et al. 2020).
As one of the objectives of this review, a study of risk factors for schistosomiasis focused on some important issues comprising climate and environment, human behavior, women and preschool-aged children, school-aged children, and socioeconomics.
METHODS
Google, ScienceDirect, and the PubMed database at the NCBI were used to search for articles on risk factors for schistosomiasis published between 2009 and 2024. Other relevant publications published before 2009 were also included. Keywords used for searches for articles include the following:
Climate risk factors for schistosomiasis,
Environmental risk factors for schistosomiasis,
Infection risks of Schistosoma spp.,
Schistosomiasis among women and preschool-aged children,
Schistosomiasis among children, and
HIV risks of schistosomiasis.
Infection risks with Schistosoma spp.
In particular, three Schistosoma spp. can infect humans: Schistosoma haematobium, Schistosoma japonicum, and Schistosoma mansoni (Nelwan 2019, 2024). Schistosoma haematobium occurs in Africa and the Middle East (Elbaz & Esmat 2013). It infects between 112 and 436 million people (Table 2) who are at risk of infection (Manz et al. 2020). Schistosoma haematobium affects the genital tract and urinary tract in 75% of infected people. Surprisingly, S. haematobium causes nearly 50% of the morbidity and approximately 150,000 deaths each year in sub-Saharan Africa. On this continent, this disease is prevalent, causing significant morbidity and mortality even compared to S. mansoni (Chala & Torben 2018). Schistosoma haematobium causes two-thirds of schistosomiasis in sub-Saharan Africa (Joof et al. 2021). Moreover, S. haematobium–Schistosoma bovis hybrids occur in Corsica, France (Rothe et al. 2021).
Parasites . | Infection . | Risk of infection . | References . |
---|---|---|---|
Schistosoma haematobium | 112 million | 436 million | Manz et al. (2020) |
Mushi et al. (2022) | |||
Schistosoma japonicum | 3.1 million | 70 million | Hinz et al. (2017) |
Nurwidayati et al. (2019) | |||
Qiu et al. (2019) | |||
Tenorio et al. (2021) | |||
Schistosoma mansoni | 54 million | 393 million | Mushi et al. (2022) |
Parasites . | Infection . | Risk of infection . | References . |
---|---|---|---|
Schistosoma haematobium | 112 million | 436 million | Manz et al. (2020) |
Mushi et al. (2022) | |||
Schistosoma japonicum | 3.1 million | 70 million | Hinz et al. (2017) |
Nurwidayati et al. (2019) | |||
Qiu et al. (2019) | |||
Tenorio et al. (2021) | |||
Schistosoma mansoni | 54 million | 393 million | Mushi et al. (2022) |
Schistosoma japonicum occurs in China, Indonesia, and the Philippines. In China, it infected 37,600 people in 2017 (Qiu et al. 2019). In Indonesia (Sulawesi), S. japonicum infects 68 (less than 1%) people in 2018 (Nurwidayati et al. 2019), and 10,000–15,000 people were at risk of infection (Garjito et al. 2008; Rosmini & Sumarni 2010). In the Philippines, this parasite infects 2.7 million people (Tenorio et al. 2021). Approximately 70 million people (Table 2) are at risk of S. japonicum in Asia (Gordon et al. 2012; Hinz et al. 2017; Zhu et al. 2017). Schistosoma japonicum causes intestinal schistosomiasis (World Health Organization 2023).
Schistosoma mansoni occurs in Africa, Latin America, the Middle East, the Caribbean (Hinz et al. 2017; Chala & Torben 2018), and the West Indies (Hinz et al. 2017). It infects approximately 54 million people (Manz et al. 2020), and 393 million people are at risk of infection (Table 2) (Mushi et al. 2022). Approximately 200,000 people die from chronic S. mansoni per year (Gunda et al. 2020). Schistosoma mansoni can infect wild primates in endemic areas. It is primarily a human parasite and not a zoonosis (Centers for Disease Control & Prevention 2024). It causes intestinal schistosomiasis in humans (Nyangulu et al. 2022; World Health Organization 2023).
Interactions on risk factors for schistosomiasis
Schistosomiasis transmissions can spread through human behavior, socioeconomic factors, climate factors, environmental factors, and HIV. Schistosomiasis transmission can spread through dam and irrigation projects, movement of population with schistosomiasis, seasonal migration of employees, and refugees (Nelwan 2019, 2024). In addition, populations that are infected with HIV and schistosomiasis can spread these diseases to others.
Populations with schistosomiasis were from endemic areas, which have certain environmental factors, such as living close to water sources. These water sources may include ponds, rivers, and lakes. In addition, environmental factors can be altered by climate changes, such as rainfall and temperature changes, floods, and droughts (De Leo et al. 2020). Droughts can cause high temperature in endemic areas that can reduce schistosomiasis. Rainfall can cause floods that can spread transmission of schistosomiasis to other areas.
It is clear that risk factors for schistosomiasis include human behavior and climate changes. These factors are absolutely interrelated to each other in the spread of schistosomiasis.
Human behavior factors
Preschool-aged children had a higher prevalence of Schistosoma egg excretion (OR = 2.54) than older children. The prevalence in this group could be due to early exposure to water bodies with schistosomiasis. This can happen when a mother or caregiver takes them to a water source for household chores. Under such conditions, children often play and swim naked in the infested water (Ndassi et al. 2019). Similarly, bathing, swimming, and irrigated farming make people susceptible to schistosomiasis infection. Male children are at a higher risk of being infected than female children (Joof et al. 2021). Preschool-aged children are susceptible to infections due to a low immune system (Ndassi et al. 2019). Washing and using bodies of water for recreation can increase the risk of infection (Gordon et al. 2019).
Usually, the intensity and prevalence of the infection decline in adulthood. However, a high prevalence can occur in adults who often come into contact with water in their daily activities. These activities can include bathing, fishing, washing clothes, and washing cars. In endemic areas, nearly every person is infected with schistosomes in their life (Colley et al. 2014). In Africa, schistosomes infect approximately 100 million females, of whom 83% live in rural areas (McCreesh et al. 2015). In areas with typical transmission patterns, 60–80% of school-aged children and 20–40% of adults may remain actively infected (Colley et al. 2014; Shams et al. 2022).
Studies in Cameroon show that high rates of S. haematobium infection in school-aged children and pregnant women occur in the rainy season. It is low in the dry season. Climate, human behavior, and socioeconomic factors play a significant role in the transmission of schistosomiasis. Through various contacts with water, the parasite infects humans. The risk of infection in pregnant women in Munyenge is determined by the frequency and intensity of contact with infected water during bathing and household activities. In endemic areas, school-aged children are at high risk of infection due to contact with infested water (Ndassi et al. 2019).
Schistosome infections also occur among infants and young children. They occur, in part, because of the low usage of standard diagnostics. Early childhood infection has a substantial role in host immunomodulation and the establishment of chronic anti-schistosome egg inflammation that contributes to pathological effects in endemic pediatric populations (Colley et al. 2014).
Infection status is comparable between the sexes. Studies have reported a sex-dependent pattern of infection. The lack of association between infection and sex may be because both activities cause the most exposure to cercariae-infested water (Ndassi et al. 2019).
Women and preschool-aged children
Approximately 390 million females are at risk of developing schistosomiasis infection (Hegertun et al. 2013). Schistosoma haematobium causes urogenital schistosomiasis. It affects an estimated 112 million people in sub-Saharan Africa, of whom 70 million suffer from hematuria (Nazareth et al. 2022). Approximately 16–56 million females are living with urogenital schistosomiasis, and approximately 150 million adolescent girls and women are at risk of developing urogenital schistosomiasis (Mazigo et al. 2022). Urogenital schistosomiasis affects 40–45 million women in sub-Saharan Africa (Rite et al. 2020; Mazigo et al. 2022).
Studies have established the adverse consequences of schistosomiasis on pregnancy outcomes, both in animals and humans. Schistosoma haematobium infection is associated with placental inflammation. This can lead to poor birth outcomes due to placental incompetence. Severe S. mansoni infection is also associated with a higher risk of anemia, which in turn can lead to maternal mortality or low birth weight. Anemia may be due to the loss of iron in urine and fecal waste. Proinflammatory cytokines due to schistosomiasis infection cause anorexia or loss of appetite in pregnant women. This can ultimately result in a decrease in the maternal weight, causing the baby to be born with a low birthweight. In Tanzania, there is a high prevalence of S. mansoni infection in pregnant women. This high intensity of infection puts the mother at higher risk of experiencing anemia during pregnancy (Adenowo et al. 2015).
Mutsaka-Makuvasa et al. (2018) stated that preschool-aged children and women in endemic foci were all considered high-risk groups. However, until now, preventive chemotherapy has only been targeted at primary school-aged children. It excludes preschool-aged children and women who have severe morbidity associated with schistosomiasis. Although the authors demonstrated that preschool-aged children are also infected with schistosomes, there is a dearth of data showing the dynamics of reinfection to inform current and future control strategies. In addition, for the success of any health program, consistent participation (compliance) of the target population in the program's intervention is a prerequisite (Mutsaka-Makuvasa et al. 2018).
Several factors influence the risk of schistosome infection in preschool-aged children, including those that have been identified in other age groups (Okakunor et al. 2018). The rate of schistosomiasis in preschool-aged children is 53.9%. A significant increase in age is associated with an increased prevalence and intensity of antibody responses and egg-patent infections, consistent with the results of studies elsewhere. This occurs because the cumulative rate and duration of daily exposure to environmental water bodies increase as children grow. It also occurs as the population of Schistosoma worms in infected children matures to full egg-laying stage, thereby increasing levels of soluble egg antigen (SEA). High cumulative water contact rates in habitats where suitable snails occur suggest a risk of transmission in this age group. The condition of the mothers is more concerning because 94.5% of the mothers have positive schistosomiasis. More than half of the women bathe or wash clothes in environmental water daily (Poole et al. 2014).
Although the prevalence of schistosomiasis is higher in children, preschool-aged children (less than 5 years) have long been considered to be at low risk of infection. However, prevalence data from a number of epidemiological studies have resulted in an estimate that at least 50 million preschool-aged children in Africa have schistosomiasis. Moreover, the true global infection and disease burden have not been quantified. This makes it difficult to develop operational and economic plans for controlling schistosomiasis in preschool-aged children. In addition, gaps relating to infection, disease dynamics, and treatment need to be addressed if we are to provide sustainable control of infection and schistosomal disease in preschool-aged children and strengthen schistosomiasis elimination programs (Osakunor et al. 2018).
A study on the shores of Lake Albert and Victoria showed that almost 50% of children aged 3 months and over had an active infection. What is even more surprising is that the rate of reinfection, especially on the Lake Albert shoreline, is very high. Even in a 6-month period, the follow-up of two praziquantel administrations only slightly reduced local prevalence. The situation at Lake Victoria is more favorable, probably due to the slower general transmission dynamics. Assessing the risk of infection and the rate of reinfection in young children is problematic because of the differences between active and passive water contact mechanisms. A pilot study in Lake Albert has attempted to reveal why transmission appears to be so high. This study uses a novel application of global positioning system (GPS) data loggers. In this study, young children were shown to typically have up to 30 min of active daily water contact in addition to a more equivocal level of passive water contact. However, taken together, this reveals an astounding amount of water contact risk and leads to clusters of stable but previously equivocal transmission within communities (Stothard et al. 2013).
School-aged children
The World Health Organization estimates that the number of countries considered endemic for schistosomiasis was 78 in 2011 (Ismail et al. 2014). Schistosomiasis affects 250 million people worldwide (Yang & Zhou 2023), with more than 90% living in sub-Saharan Africa and 54% of whom are school-aged children (Kokaliaris et al. 2021). Mutsaka-Makuvasa et al. (2018) stated that approximately 206.4 million people needed preventive chemotherapy, including 111.2 million school-aged children, and 95.2 million adults needed treatment.
In 2010, in the Eastern Cape Province of South Africa, there was an alarming prevalence of 73% in school-aged children with schistosomiasis infection. Mozambique revealed a prevalence of 47% of S. haematobium infection and 1% of S. mansoni infection. In Zarima town, northwest Ethiopia, the prevalence of S. mansoni infection was 37.9%. Southwestern Cameroon revealed a prevalence of S. haematobium of 69.17%, which confirms the high endemicity in the area. Most of the lakes in the area are the habitat of the intermediate host Bulinus globosus of S. haematobium. School-aged children in Agboville, Côte d'Ivoire, showed a prevalence of 85.3 and 53.8% for S. haematobium and S. mansoni, respectively (Adenowo et al. 2015). Schistosoma haematobium has a peak prevalence of urogenital schistosomiasis among school-aged children (Ndassi et al. 2019).
Chu et al. (2012) reported that Schistosoma intercalatum infects school-aged children in the Democratic Republic of São Tomé and Príncipe. However, the S. intercalatum infection rate in school-aged children is not high, reaching almost 2.4%. It is lower than 36.2% in a previous study in that country. Girls have a higher infection rate than boys. It seems that girls often accompany their mothers in water and related activities such as swimming and bathing. In addition, the country has conducted a school-aged child-based deworming program using a mebendazole-only regime annually since 2005. This drug is only useful for killing some soil-borne worms, namely Ascaris lumbricoides but not S. intercalatum (Chu et al. 2012).
In Kwazulu-Natal, South Africa, the prevalence of S. haematobium decreased from 37.5 to 5.78% between the baseline and follow-up surveys. The positive impact of praziquantel treatment on children, which were positive at baseline, can explain that reduction. The occurrence and persistence of droughts over the study period may also explain these findings. Reducing infection transmission after a chemotherapy control program shows a reduction in incidence, prevalence, and infection intensity. However, in the Ivory Coast, it was found that infection rates were increasing rapidly. The infection rates reached the baseline prevalence within a short time of 12 months after successful treatment. This can occur after participants return to their daily activities, which require contact with infected water and snails (Kabuyaya et al. 2018).
Schistosomiasis is the main parasitic disease in Ethiopia. The prevalence ranges from 24 to 89.9% in various parts of the country and is high in school-aged children. In 1983, a very high prevalence of S. mansoni (89.9%) was reported among school-aged children in Sanja town. In 2019, the prevalence was 35%, a relatively moderate S. mansoni infection. This finding is consistent with research conducted in Timuga (34%) and Wondo Genet (37.2%). Conversely, this finding is lower than the 89.9% reported in the same region 5 years ago. The author's findings are lower than reports from the Zarima (89.5%) and Wolaita Zones (81.3%), but higher than reports from Uganda (7%) and Jima (24%). These prevalence variations could be due to the study periods, seasonal differences, or treatments targeting deworming programs. These programs include school-aged children, differences in the frequency of contact with infested water, the ecological distribution of snails, and climatic variability. In addition, differences in the methods used for stool examinations, sample sizes, and the variations in awareness regarding the transmission and prevention of S. mansoni infection may be the factors for the variations between findings. The extreme decrease in prevalence may be due to the adoption of targeted treatment programs. This includes school-aged children in primary schools, providing health education on how to prevent schistosomiasis, and community mobilization for the construction and use of latrines (Woldegerima et al. 2019).
M'Bra et al. (2018) found that the overall prevalence of schistosomiasis among school-aged children in Korbogo was 1.9%. It consists of 0.3% S. haematobium and 3.6% S. mansoni. Due to the low prevalence of S. haematobium, risk factor analysis was limited to S. mansoni. Boys are 7.8 times more likely to be infected with S. mansoni than girls. Children aged between 10 and 15 years old are 3.8 times more likely to have an infection than children aged 5–10 years old. In addition, living in homes far from water access points and not swimming in water bodies was significantly associated with decreased S. mansoni infection changes. Socioeconomic status does not affect the prevalence of S. mansoni (M'Bra et al. 2018).
Population studies of schistosomiasis-infected children reveal that schistosomiasis can cause health problems in infected children. These problems may include cognitive reasoning, fatigue, growth retardation, impairment of memory, weakness, impairment of memory, and an increased risk of anemia, which leads to poor academic performance. Thus, it limits the potential for children to be infected. Negative results in these children add to the socioeconomic burden on the society (Centers for Disease Control & Prevention 2024).
Socioeconomic factors
Kloos et al. (2008) suggested the need for more equitable schistosomiasis control interventions, which in turn may contribute to the alleviation of poverty. Socioeconomic factors influence the continuous transmission of the disease in sub-Saharan areas (Kloos et al. 2008). These factors include occupational activity, poor sanitation and hygiene, the unavailability of drinking water for household use, a lack of education about transmission and exposure reduction strategies, and limited access to effective treatment (Manz et al. 2020).
Socioeconomic conditions are associated with the incidence of schistosomiasis (Gazzinelli et al. 2006). Some studies have revealed that schistosomiasis is a social disease. Other studies have revealed no effect. For socioeconomic status, it is equivocal (Omondi et al. 2021). This relationship was first described in detail in Egypt and has since been researched in various endemic areas. In Brazil, the role of socioeconomic factors in S. mansoni has been investigated. In urban areas of Brazil, there is a strong relationship between socioeconomic variables and schistosomiasis. Better rural areas in a region with high schistosomiasis endemicity in Brazil show a weak to moderate association between most socioeconomic indicators and infection (Gazzinelli et al. 2006). This shows that socioeconomic conditions can affect the transmission of Schistosoma spp. infection in rural areas in particular.
Climate factors
Climate change also affects human host exposure patterns. Climate change can include hotter seasons, driving increased recreational use of infected water sources (Osakunor et al. 2018). There is an established link between climate change and the transmission of infectious diseases. Schistosomiasis is a unique example of a disease spread that is influenced by climate change and global warnings (Adenowo et al. 2015). A rise in ambient temperature from 20 to 30 °C will lead to an over 10-fold increase in the average burden of S. mansoni infection in endemic areas. The temperature optimum for schistosomiasis is 22–27 °C (Tabo et al. 2023). However, at temperatures above 30 °C, there is a decrease in the disease burden. This may be due to the higher mortality rate of the intermediate snail hosts. Although an increase in disease burden increases morbidity and mortality, there may be negligible increases in disease prevalence. Rainfall patterns also affect the transmission of the disease. In Senegal, Biomphalaria pfeifferi is responsible for S. mansoni transmission during the rainy season. Otherwise, in the dry season, S. haematobium infection is transmitted by B. globosus (Adenowo et al. 2015).
A study has revealed that temperature higher than optimum temperature can reduce the transmission of S. mansoni in Africa. This causes the reduction of the main intermediate host, i.e., B. pfeifferi, in temperature more than optimum temperature. However, weather more warming in South America, especially Brazil, could expand habitat suitable for transmission of S. mansoni infection. In Africa, S. haematobium infection near the equator can also be reduced in high temperature. In Asia, average temperatures monthly under 0 °C prevents the northward spread of Oncomelania hupensis in China. Furthermore, climate change has already altered the distribution of schistosomiasis geographically. It moves from 33°15′ N to 33°41′ N. It is 48 km northward in 30 years (De Leo et al. 2020).
The epidemiology of schistosomiasis must be viewed in light of ongoing climate change. The last half century has shown signs of global warming. This is mainly due to the burning of coal and oil on an increasingly large scale. Since 1990, the Intergovernmental Panel on Climate Change (IPCC) for the United Nations Framework Convention on Climate Change (UNFCCC) has regularly produced reports on our understanding of climate change, including options for its mitigation. The IPCC bases its assessment on publications, scientific literature, and opinions from invited independent researchers. An important part of its work relates to global circulation models. These models are currently used to predict climate change for the next 80 years. Predictions are based on a complex mathematical representation of the Earth's energy balance between the atmosphere, total landmass, seas, and ice cover. These components interact as a combined system. The state arises from an equation based on the dynamic values of various climate variables, i.e., temperature, winds, etc., at any point in the world. Climate modeling uses current and historic data to try to predict future climate scenarios from now to the end of the 21st century (Yang et al. 2018).
McCreesh et al. (2015) concluded that climate change may have a major impact on the distribution and identity of S. mansoni infections over the coming decades. Temperatures are forecast to be suitable for increased transmission over much of eastern Africa over the next 15 years. This may lead to an increase in the prevalence and intensity of infection in some areas and possibly reduce the impact of control and elimination programs. In some areas, especially Rwanda, Burundi, southwest Kenya, and eastern Zambia, the increased risk of infection may be substantial. Schistosomiasis can spread to new areas beyond the reach of control programs. Better surveillance in these areas will allow education and control programs to be implemented promptly in new endemic areas, minimizing disease morbidity (McCreesh et al. 2015).
The progress or increase in the population dynamics of various health-related issues in sub-Saharan Africa can be linked to a number of climatic variations. Climate change in sub-Saharan Africa has health consequences and adversely affects the economic growth and development of certain sub-Saharan African countries. This can also have an additional impact on environmental issues. This is due to the vulnerability of sub-Saharan African countries to climate change compared to the rest of the world's continents. This vulnerability is due to high levels of poverty, armed conflict, and weak institutions in sub-Saharan Africa. This situation limits the ability of African countries to address the additional health challenges posed by climate change. The scope and categories of health-related issues caused by climate change in sub-Saharan Africa differ markedly from one community or region to another. This diversity is the result of differences in microclimates, geographical and socioeconomic factors, accessibility and availability of quality health infrastructure, and underlying epidemiology and communication capabilities. The influence of climate change on human health can be direct or indirect. These changes comprise increases in mortality and morbidity, patterns, and incidence of diseases such as allergic disorders, cancer of the skin, cardiorespiratory disease, eye diseases, and thermal stress. In addition, changes can also cause droughts, famine, forms of malnutrition, migratory infectious diseases, the unavailability of food and water, and increased population dynamics of vector and waterborne diseases. The most important impacts of climate change on human health comprise the increasing prevalence of neglected tropical diseases, malaria, malnutrition, diarrhea, and meningitis (Adekiya et al. 2020), especially schistosomiasis.
Environmental factors
Environmental factors that influence schistosomiasis transmission can include distance to snail habitats, building dams, land cover, especially elevation, rainfall, seasonal land surface temperature, and the presence of flooded agricultural land. The high prevalence of schistosomiasis in children is related to factors such as snail habitat, the building of dams (Gordon et al. 2019), and living close to pools or ponds, springs, and streams. Another study stated that it was not associated with S. haematobium infections. Water velocity is an important factor in the transmission of schistosomiasis since intermediate hosts can be imported into fast-flowing water. Bulinus spp. generally seem to prefer a low-flow environment. There is a negative association between slope and S. haematobium worms (Manz et al. 2020). In addition, lack of access to good sanitation contributes to open defecation, resulting in environmental pollution that increases the transmission of schistosomiasis (Angora et al. 2019).
In the Far East, S. japonicum and the genus Oncomelania can be found in swamps and lakes, mountainous and hilly areas, and watersheds. The endemic S. japonicum areas are within 1 km of water bodies, such as lakes, rivers, and wetlands. Habitats of the genus Oncomelania, such as Oncomelania lorelindoensis and Oncomelania quadrasi, can be either natural habitats or disturbed habitats. Natural habitats can include floodplains, forests, and swamps. Disturbed habitats can be in the form of drainage canals, drainage canals of irrigation works, roadside ditches, small canals (Gordon et al. 2019), and former rice fields (Garjito et al. 2014) (Figure 1).
M'Bra et al. (2018) showed that the prevalence of S. mansoni infection can be affected by the presence of surface water points close to homes. In this case, people often have to cross open water to reach their destination. In addition, it is commonly observed that people defecate at or around these water points. Moreover, to make it easier to water plants, farmers often make wells around water points. Swimming also generally increases the risk of S. mansoni infection (M'bra et al. 2018).
Environmental factors that can also affect the presence of Schistosoma spp. and its intermediate hosts include humidity, pH, sunlight, and temperature (Samarang et al. 2018; Nelwan 2019, 2024). For example, pH and water temperature affect the existence on the infection of snails (Sokouri et al. 2024). In addition, environmental factors can also be in the form of rain, salinity, turbidity, vegetation, water current velocity, and desiccation fluctuations, which affect the persistence of schistosomiasis infection (Adekiya et al. 2020; Ghazy et al. 2022).
Human immunodeficiency virus
The interaction between HIV and schistosomiasis is contradictory. Some studies suggest that there is an increased risk of HIV transmission in schistosomiasis-infected individuals, which is especially severe in women with genital schistosomiasis. However, the microscopic schistosomiasis diagnosis in individuals with HIV seems to be less sensitive. Several articles describe a significant or nonsignificant reduction in S. haematobium and/or S. mansoni egg excretion in HIV coinfected individuals. Another study showed that there was no relationship between HIV status and schistosome egg excretion after adjusting for age (Manz et al. 2020).
Helminth infections and HIV are global health problems. Humans with schistosomiasis are at high risk of HIV infection. People infected with S. haematobium or S. mansoni are susceptible to HIV infection due to common high-risk behaviors, for example, multiple sexual partners and other exposures to sexually transmitted diseases. There is also overlap of some of the risk factors associated with HIV and S. mansoni infections in the same geographical setting or biological interaction between the two to increase the risk of individuals being coinfected with both. There is an association between HIV infection and schistosomiasis, according to epidemiological studies (Yang et al. 2018).
A study in Tanzania demonstrated that women who are infected with schistosomes have a threefold higher chance of acquiring HIV than women who are not infected. This chance remains the same for men with or without infection. In women, the risk of HIV is due to local physical changes, such as schistosome eggs in the woman's genitalia. The sequestration of eggs in the vaginal and cervical mucosal tissues leads to erosion, the formation of tiny cervical abnormalities, and ulceration. These abnormalities are in the form of yellow and/or grainy sandy patches surrounded by an irregular network of blood vessels. These blood vessels represent egg-induced angiogenesis and accelerate the transmission of HIV during sexual intercourse. In contrast, men who are infected with S. haematobium have a lower risk of acquiring HIV because eggs do not penetrate male genital organs that are exposed to the virus. However, other studies show a mild association between HIV acquisition and men's urogenital schistosomiasis. In addition, although S. mansoni eggs are not localized to the genitalia, infected individuals appear to be more susceptible to HIV. This association is a consequence of schistosome-associated immunomodulation, as opposed to egg-induced local tissue damage (Constain et al. 2018).
An HIV-infected woman with urogenital schistosomiasis increases transmission to male sexual partners, as well as transmission from an HIV-infected male to his sexual partners. It also accelerates the advancement of schistosomiasis in people already infected with HIV. Women with S. haematobium eggs in their Pap smear had a risk three times higher of having HIV (Adenowo et al. 2015).
Bochner et al. (2020) did not identify a statistically significant association between S. haematobium and the risk of HIV acquisition, either overall or in a sex-stratified analysis. One hypothesis in the field suggests that S. haematobium increases HIV acquisition risk, specifically in women. The estimated point of HIV acquisition among female sex workers with S. haematobium was 1.64. It was not statistically significant. Statistical power was limited with only 70 S. haematobium-infected individuals in the cohort. The results across all subgroups suggest that schistosomiasis is not associated with a large, increased risk of HIV acquisition. This finding is consistent with another study, which found a moderately positive association between S. haematobium and HIV. Very large studies will be needed to have sufficient statistical power to rule out whether S. haematobium is associated with a more moderate increase in HIV acquisition risk among women (Bochner et al. 2020).
The interplay between human behavior, socioeconomic, and environmental changes
Human cultural habits, absent or poor sanitations, and the presence of intermediate hosts can cause schistosomiasis and can spread it to other areas (Calasans et al. 2018). Any water contact increases up to 3.14 times higher than people with no water contact (Reitzug et al. 2023). Schistosomiasis is associated with poor environmental and sanitation. It highly infects people in diverse water contact inhabiting areas where snail hosts occur (Angelo et al. 2018). In addition, this disease can affect people with low socioeconomic level (Klohe et al. 2021). Human habits, which use river or ditch water, result in a 2.31 higher risk for S. japonicum infection compared to the behavior that does not use it (Hariyanto 2007).
The weather condition variations have an impact on the fecundity and mortality of both intermediate hosts and schistosomiasis transmission during the life cycle of schistosomiasis (Adekiya et al. 2020). A favorable environment for intermediate hosts can be created by climate changes (Tabo et al. 2023). Intermediate hosts of human schistosomiasis include the genera Biomphalaria, Bulinus, Neotricula, Oncomelania, and Robertsiella. Intermediate hosts play an important role to maintain schistosomiasis. This means that in the favorable environment, such as optimum temperature, intermediate hosts can release the most cercariae into freshwater. Thus, more definite hosts can be reached by cercariae. For example, the genus Oncomelania can shed up to 160 cercariae daily (Nelwan 2019, 2024). This increases the risk of schistosomiasis in favorable environment.
Conditions in rainfall and without rainfall can cause floods and droughts, respectively. Floods in endemic schistosomiasis areas can spread the disease to new areas, result in snails in these areas, and can built new endemic areas of schistosomiasis. It can infect people with poor habits and poor sanitations in these new areas. Without rainfall, it increases temperature and causes droughts. High temperature above optimum temperature, i.e., 27 °C, results in reduced schistosomiasis, while low temperature under optimum temperature, i.e., 22 °C, causes schistosomiasis cases also to be reduced.
It seems that human behavior, socioeconomic conditions, and environmental changes compound each other in the transmission of schistosomiasis.
(Ar)praziquantel for preventive chemotherapy for schistosomiasis
(Ar)praziquantel is a drug for the treatment of Schistosoma infections. Arpraziquantel is a drug that can help treat schistosomiasis in preschool-aged children. It is safe at a single dose of 50 mg/kg for S. mansoni and 60 mg/kg for S. haematobium infection in preschool-aged children with schistosomiasis (Yang & Zhou 2023). Arpraziquantel is safe for children aged 3 months–6 years (N'Goran et al. 2023). Praziquantel is used to treat preschool-aged children, school-aged children, adolescents, and adults. Praziquantel dose is 40 mg/kg for all ages (Olliaro et al. 2020), especially for S. haematobium, S. japonicum, and S. mansoni. The dosage regime for treatment of S. japonicum and Schistosoma mekongi is 60 mg/kg orally in divided doses over 1 day (3 × 20 mg/kg doses 4-hourly, or 2 × 30 mg/kg either 4- or 6-hourly). For chemotherapy prevention in S. japonicum, it can be used at a dosage of 40 mg/kg (Gordon et al. 2019). However, the use of arpraziquantel still needs more study for treating S. japonica in preschool-aged children. However, the use of (ar)praziquantel with mass drug administration (MDA) will not eliminate schistosomiasis (Li et al. 2024). This means that treatment (MDA) for elimination, in future, should be used along with other techniques, such as vaccination and genetic manipulations. These techniques are under investigation.
CONCLUSIONS
Schistosomiasis occurs in Africa, Asia, Europe, and Latin America. Risk factors for schistosomiasis can comprise human behavior, preschool-aged children, school-aged children, climate change, environmental factors, and socioeconomic factors. For example, proximity to water bodies can increase the risk of schistosomiasis infection. Arpraziquantel is used for treating children aged 3 months–6 years. Praziquantel can be useful for treating schistosomiasis in preschool-aged children, school-aged children, adolescents, and adults. Recommendation includes the following: the use of protection tools against schistosomiasis for people doing activities in high-risk areas for schistosomiasis, provision of schistosomiasis-free water sources, and ongoing disease treatment. For future work, it can include vaccine development, drug developments, and phylogenetic relationships for treatment needs.
AUTHOR CONTRIBUTIONS
Exclusively, MN performed research and manuscript development.
DATA AVAILABILITY STATEMENT
All relevant data are included in the paper or its Supplementary Information.
CONFLICT OF INTEREST
The author declares there is no conflict.