Determinants of Schistosoma mansoni transmission in hotspots at the late stage of elimination in Egypt | Infectious Diseases of Poverty

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The current strategy for schistosomiasis elimination is primarily based on preventive chemotherapy with periodic administration of the anti-schistosomal drug (PZQ) to school-aged children and other high-risk groups [30]. PZQ reduces morbidity and might have an impact on transmission, but rarely eliminates infection [31, 32].

This study aims to identify the different ecological factors responsible for the sustained transmission of diseases in three hotspot areas of the Governorate of Kafr El-Sheikh. Seasonal variation and its influence on environmental factors affecting the prevalence of human and snail infection were the primary variables examined. In addition, sociodemographic and behavioral risk factors may play a significant role in maintaining the infection cycle.

Seasonal variation and schistosomiasis prevalence in snails and humans

In this study, the overall prevalence of S. mansoni infection was (13.1%); 7.2% (31/432) in the summer and 19.2% (82/429) in the fall. The studied villages were considered to have low and moderate endemicity during summer and fall, respectively [24]. The current prevalence of schistosomiasis is relatively lower than that which was previously reported two years earlier in Arab El-Mahder village (30%), Kafr El-Sheikh. In Village II, the prevalence of infection was nearly identical during the summer and fall (26.3% and 27.1%, respectively), whereas it increased from 0.7% in the summer to 18.2% in the fall in Village I. This low prevalence during the summer can be attributed to chemotherapy campaigns conducted four months prior to the survey or to the difference in sampling technique between the two seasons. It is important to note that the number of B. alexandrina snails collected per location in the summer was greater than in the fall with an equal proportion of infected watercourses in each season. However, the prevalence of human infection was greater in the fall. This disparity between human and snail infection can be attributed to human activity; residents of Village I preferred to swim in the waterways of other villages where their farms were located. In addition, Village II’s watercourses were severely polluted and had a high water level, resulting in a low snail population despite the high prevalence of human infection. In addition to the fact that snail prevalence is not the only predictor of human infection, the point prevalence of S. mansoni infection should not be used to estimate the annual prevalence of infection.

Intensity of infection

Indeed, the effectiveness of MDA programs for S. mansoni is mainly monitored by measuring changes in infection prevalence, drug treatment coverage, and the prevalence of heavy infection (≥ 400 epg) [1]. Regarding infection intensity, the majority of children in this study was 98.2% (111/113) had either light or moderate infection, and the prevalence of infection was either between 10%–50%. This finding could be due to the intensive MDA campaign implemented by the Egyptian MOHP.

Sociodemographic factors

Age

In endemic areas, the infection is usually acquired during childhood [33]. The prevalence and intensity of rise infection with age and peaks at approximately 15 to 20 years. In older adults, the prevalence of infection does not change significantly, but intensity (parasite burden) decreases [34]. In this study, the mean age of infected children was significantly older than the uninfected children. Additionally, the age group of 11–15 years was more susceptible to infection than the age group of 6–10 years. Indeed, children aged 11–15 years can become more vulnerable for schistosomiasis when engaging in recreational activities such as swimming and playing in the water, when fetching water for household or agriculture activities. In the same line, many studies highlighted that different age groups had different susceptibility to infection. [35, 36]. On the other hand, a study conducted in Côte d’Ivoire found no difference in the prevalence of S. mansoni infection among the three investigated age groups [37].

Sex

The global distribution of schistosomiasis among both sexes is not fully addressed. However, most published surveys have found an equal prevalence of infection among men and women. However, the intensity of infection is more severe in females [38]. Nonetheless, in the current study, the prevalence of infection among girls was lower than that of boys, with no difference in intensity. We speculate that boys are more frequently exposed to water canals than girls. Moreover, the total surface area exposed to water varies due to a variety of water-related activities. Due to religious issues, customs, and traditions of the Egyptians, girls are prohibited from swimming in water canals while boys are permitted to do. Girls’ primary water activities include fetching water and washing clothes and dishes with their hands and legs only exposed. In line with this finding, another study conducted in Senegal found that males had higher infection rates [39]. Interestingly, the Côte d’Ivoire study found a similar prevalence among boys and girls; However, this may be due to the fact that significantly more boys (727 vs. 460) participated in the survey [37].

Education

In this study, maternal illiteracy was associated with a higher prevalence of severe infection. In particular, our findings revealed that 74.7% of infected children had illiterate mothers. A study conducted in Santo Antonio de Jesus, Bahia State, Brazil, found that an increase in the education level of the household’s head was strongly associated with a reduction in the prevalence and intensity of infection in the household [40]. Nonetheless, the paternal education level had no significant effect on the prevalence of infection. Angora et al., [37] reached a similar conclusion; The parental level of education was significantly associated with infection, but the maternal odds ratio was greater than three times the odds of paternal education. The higher risk associated with maternal illiteracy may be explained by the longer time mothers spend with their children and the profound influence they have on them.

Social class or status

Schistosomiasis is more prevalent in areas of poor socioeconomic conditions. Due to their low educational attainment, high unemployment rates, poor sanitary and housing conditions, and lack of access to health facilities, the inhabitants of these regions are at risk [12]. This study reported a higher prevalence in the low socioeconomic class (13.98%) than in the middle socioeconomic class (10%), but the difference was not statistically significant. The high social class effect could not be evaluated because most children were of low or intermediate social class. Extensive research has been conducted on the effects of poverty on the prevalence, incidence, and cost of schistosomiasis over time. Schistosomiasis is a clear example of a disease caused by poverty [41].

In this study, watercourse proximity was not significantly associated with S. mansoni infection. In contrast, a detailed epidemiological study conducted in São Lourenço da Mata, Brazil, revealed that leisure water contact, particularly swimming, was the only type of water contact that was significantly associated with schistosomiasis among people between the ages of 10 and 25 and that better socioeconomic conditions were associated with a decrease in the frequency of water contact [42].

Human water contact activities

Water contact is required in order to acquire schistosomiasis. However, 40.7% of infected children reported no contact with watercourses. This issue needs to be further discussed as if they did not encounter the water stream, what the supposed route of infection would be. Direct observations were made with an emphasis on the behavior of community members to understand how they might become infected. There are two possible explanations for this finding. First, these children may not recognize the danger of some adopted behaviors, such as dumping trash into watercourses. This may expose their legs or bodies to a stream of water. Secondly, the stigma associated with using watercourses or being infected with S. mansoni may have contributed to the children’s denial of contact with watercourses. The site of contact is supposed to be associated with acquiring infection, 23.6% of children who were contacting the center of the canal got schistosomiasis compared to 10.5% of those contacting the bank.

Health facilities within the villages

The limited accessibility to diagnostic, chemotherapeutic, and preventive services significantly constrains the health-seeking behavior of infected people with schistosomiasis and developing other infectious diseases, particularly in countries. In addition to health illiteracy, the costs of travel and health service fees, geographic distance, social factors, and the frequent unavailability of services are among the most significant obstacles that individuals face when attempting to access health services [43, 44].

In this study, a small proportion (12%) of the population reported visiting the local health care unit in the villages, although it was accessible to the population within its catchment area. This issue was investigated while providing health education sessions. Stakeholders and fathers of screened children reported that doctors are not always available and the unit is severely under-resourced. Others stated that drugs are dispensed to relatives and acquaintances.

Environmental factors

Our results shed light on the significant seasonal variation in the number of collected snails, including B. alexandrina, which is correlated with significant seasonal variations in temperature, salinity, turbidity, TC, and EC. Another important finding was that the type of vegetation had a significant effect on population density; duckweeds and grasses had a significant association with the presence of snails, which may be due to their importance as a food source, and snails may attach themselves to various plant parts to avoid the direct effect of sunlight, feed, or gain access to oxygen [45]. It is unknown to what extent snail population growth is attributable to these studied factors, as environmental changes measured across months were not always correlated with the total number of collected snails. However, this finding should shed light on other environmental factors implicated in snail survival. On equal terms, Monde et al., [46] reported that no single environmental parameter is a major determinant of host snail distribution, however, environmental parameters can account for 41 to 43% of the variation in snail density.

Due to the grant’s limited duration and budget, we were unable to cover all seasons and months. During the summer, schools were inaccessible due to summer vacation, and patients were recruited from mass gathering sites such as markets. Some children who were screened did not provide three consecutive daily stool samples; However, we collected three stool samples above the minimum required sample size to compensate for the dropouts. In addition, the shedding technique was adopted to diagnose snail infection, although this conventional method yields less diagnostic accuracy than other more advanced techniques, such as molecular techniques. Lastly, we were unable to provide PZQ to the infected children due to the MOHP’s treatment policy, which states that only the MOHP should administer treatment. As a result, we have provided the health authorities with a comprehensive report containing the names of infected children to treat them.

To the best of our knowledge, this is the first report to examine environmental factors implicated in the persistent transmission of schistosomiasis at the late stages of elimination in hotspots in Egypt. Additionally, the study validated the concept of community engagement, as community members were interviewed to address the alleged barriers to the elimination of schistosomiasis, and their perspectives on causes of persistent transmission were revealed. According to, these factors were taken into account when constructing the questionnaire. The fact that the research team consisted of five different specialties affiliated with four institutes and organizations was an additional strength. This factor facilitated effective collaboration in highlighting the interaction between epidemiological, malacological, environmental factors, and human infection. Lastly, the research team provided citizens with health education sessions on how to safely interact with watercourses, how to avoid infection, how to detect disease symptoms early, and where to seek medical care.

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