Religion and gender behavior: understanding the variations in risk to urinary schistosomiasis among farmers

Abstract

Urinary schistosomiasis is a chronic and acute disease that is widely spread among the poor. It is caused by blood fluke of the genus Schistosoma, and transmitted to humans through water related activities by way of skin penetration. While schistosomiasis is rarely fatal, it could impact negatively on the economy and health status of infected individual. We evaluated the prevalence and dissimilarity of schistosomiasis among farmers in a cross sectional study, while grouping the farmers into different categories. Prior to the initiation of the study, we sought permission from the community head (Emir) and properly enlightened the community about the study. Then, we collected and analyzed urine samples from the consenting farmers using sedimentation techniques. The infection rate among participants was 46.3% (56/121), although with varying prevalence across different farming categories. We found no statistical difference among Muslim and Christian farmers even though there was higher infection rate (50.7%) among the Muslim than Christian (40%). Conversely, when classifying farming type by gender, male farmers, especially the male vegetable farmers were significantly different from female farmers of other farming types, while there was no statistical difference in the classification of farming type by religion. Although we found no statistical difference in the primary demographic factors of the participants, however the significant difference recorded in some of the combination of the participants’ demographic factors shows that religion and gender might be an underlining factors that are responsible for the prevalence of the infection among the study participants. Therefore, this study will guide the decision makers in appropriately allocating future interventions among the endemic groups.

Supplementary Information

The online version contains supplementary material available at 10.1007/s12639-021-01448-0.

Introduction

Schistosomiasis (also known as Biharziasis) is a major waterborne trematode parasitic disease and Neglected Tropical Disease (NTD) that continues to cause morbidity and mortality among endemic population, especially among the disadvantaged Sub- Saharan population (Adenowo et al. 2015; WHO 2013; Hottez and Kamath 2009). Schistosomiasis is a chronic and acute disease that is caused by platyhelminthes parasites of the genus Schistosoma, with three main species affecting humans namely, S. haematobium which causes urinary schistosomiasis, and S. japonicum & S. mansoni that cause intestinal schistosomiasis respectively (Utzinger et al. 2009).

Urinary Schistosomiasis affects more than 779 million people in 79 tropical and subtropical countries, with 101.3 million cases from Nigeria thereby making the country the most endemic in Africa (Steinmann et al. 2006; Ofoezie 2002). In fact, the history of schistosomiasis in Africa dates back to the origin of recorded history, with Herodotus in his writing fondly labelling Egypt as the land where men menstruate, the condition (haematuria) that was later discovered as the hallmark of schistosomiasis (Mahmoud 2004). The misery of schistosomiasis is a continuous chronicle of frustration with more than 500 million population worldwide still at risk, especially those with poor socioeconomic status that reside in underprivileged rural communities with inadequate basic amenities (Zhang et al. 2010). These factors put together usually force inhabitants to rely on non-potable water for their agricultural and domestic needs since they lack the financial capability to install boreholes for their daily needs. In addition, schistosomiasis is one of the main occupational diseases that is acquired through activities associated with fresh water, such as domestic chores, fishing, ablution (religious right among the Muslims) in the case of contaminated water, recreation and farming-especially the type of farming that bring farmers into frequent contact with contaminated water (Ofoezie 2002).

Humans are generally infected through skin penetration of the infective stage of the parasite called cercaria when they come in contact with contaminated fresh water during daily activities (WHO 2015; Steinmann et al. 2006). Although, urinary schistosomiasis is rarely fatal with most people in endemic countries asymptomatic, however, it could impact on economic and the quality of health of infected individual with learning disabilities, school absenteeism, poor work productivity and severe pathological effect such as; calcification of the urinary bladder, enlargement of the liver, spleen and the lymph node(WHO Update 2004).

In spite of the partnership of Schistosomiasis Control Initiative in Nigeria (SCI) and the activities of the Nigeria Federal Ministry of Health (MOH), States MOH, Non-Governmental Organizations (NGOs), World Health Organization (WHO) and the West African Centre for International Parasite Control (WACIPAC) in the ongoing efforts to map the distribution of the disease and associated vectors in Nigeria, there remains paucity of information about Schistosomiasis especially in some underprivileged communities (Ezeh et al. 2019). In addition, the low educational status, poverty, poor basic social amenities, insecurity and insurgencies of tribal and religion crisis, political hostility among others have also greatly hindered success of research efforts in containing schistosomiasis in the country.

Given the continuous challenges in our quest to manage the ravaging effects of schistosomiasis, its interconnectedness with poor socioeconomic status and frequent contact with fresh water, it has become more pressing now than ever to investigate the association between schistosomiasis and the aforementioned factors among the high risk groups. To our knowledge, studies characterizing the prevalence of the disease among one of the most vulnerable groups (farmers) and the subsequent relationship among farming type, gender and religion are nonexistent in the study area. Therefore, this study aims to examine the prevalence of urinary schistosomiasis among farmers while characterizing the associated risk factors among their farming and religion type in a research naïve community (Shonga) that is situated near River Niger and Kainji Basin, where over 95% of the population depend on farming (Amin 2018). Outcome from our study will provide epidemiological data that are useful in directing future interventions and control measures in the study area and other communities with similar socio-ecological status.

Materials and methods

Study area and population

This study was carried out in Shonga “9°1′0′ N, 5°9′0′ E”, a rural community located near River Niger and Kainji Basin in Edu LGA of Kwara State, Nigeria. The predominant soil type in Shonga is loamy, which favors agricultural activities. Majority of the households are farmers with low socioeconomic status and they often utilize the distributaries channels from the two main rivers to irrigate their farms. Islam and Christianity form the major religion in this community, and basic infrastructural amenities like pipe borne water supply, health care services, waste management, sewerage and electricity are overly poor in this community.

Questionnaire administration

We administered structured questionnaire to obtain basic demographic data like gender, farming type and the religion of the participating farmers. The questionnaire was interpreted to the farmers in their native Nupe language to facilitate easier understanding.

Sample collection

The Head of the Farmers Association identified one hundred and fifty eight (158) registered farmers in the community, out of which only one hundred and twenty one (121) consented to giving their urine samples during the cross-sectional study. Following the method previously described by Cheesbrough (1998), we explicitly explain the procedure for urine sample collection and gave out sterile specimen bottles to all consenting farmers. The specimen bottles containing freshly collected urine samples (20 ml) were collected within the hours of 10:00am to 2:00 pm, and coded with the names of farmers omitted. Specimens were stored in closed containers with icepacks and transported immediately to the Microbiology and Parasitology Laboratory, College of Health Sciences, University of Ilorin, Ilorin, Nigeria for parasitological examination.

Parasitological analysis of urine samples

Laboratory analysis of the specimens for the detection of S. haematobium eggs was performed using sedimentation technique method earlier validated by Cheesbrough (1998). Briefly, 10 ml of each urine sample was centrifuged at 5000 rpm for 5 min. The supernatant was discarded to leave the sediment, which was then placed on a clean glass slide and covered with a cover slip. The slides were then microscopically examined using × 40 objective lens for the presence of eggs (terminal-spined ova) of S. haematobium. The urine sample of participants that showed the presence of S. haematobium eggs were referred to the University of Ilorin Teaching Hospital for adequate treatment.

Statistical analysis

Data obtained from this study were analyzed in R 3.6.1 version (R Core Team 2019) using descriptive statistics in percentage to obtain the frequency of schistosomiasis infections among the farmers and Fisher test for small samples to examine the association between the demographic variables. We used sugar cane farming as a reference point since it has been shown to be strongly correlated with schistosomiasis (Amorim et al. 2014), to analyze the association between faming type & gender and faming type & religion. Infected individuals were aggregated to get the number of positive participants in each group which subsequently form our response variable that is, the number of infected individual (count), hence we used generalized linear model (Poisson regression), with significance testing. p values of < 0.05 considered statistically significant..

Results

A total of 121 urine samples were collected and examined for urinary schistosomiasis. The overall prevalence of the infection was 46.3% (56/121), out of which female and Muslim farmers were the most infected (Table 1). The characteristics of the study participants are as shown in Table 1, with sugar cane the most practiced farming type in the community followed by vegetable and rice farming while yam farming was the least practiced. Schistosomiasis infection was also non-statistically prevalent among the sugar cane farmers, while it was least prevalent among the yam farmers. Grouping farming by religion, muslims had the highest number of farmers with 58.7% (71/121) as oppose christains 41.3% (50/121). Muslim rice farmers were the most infected with urinary schistosomiasis, although without any significant difference. Considering schistosomiasis infection rate among participants by the farming type and gender, male vegetable farmers and female sugar cane farmers had the highest infection rate of 66.7% while male sugar cane farmer recorded the least infection rate 36.8% with infection prevalence variying between 16 and 56% (Supplementary material 1).

Table 1.

Prevalence of urinary schistosomiasis among the farmers of Shonga Community

	Number examined	Number infected (%)	p value
Sex
Female	43	22.0 (51.2%)
Male	78	34.0 (43.6%)	0.276
Total	121	56.0 (46.3%)
Religion
Christianity	50	20.0 (40.0%)
Islam	71	36.0 (50.7%)	0.534
Total	121	56.0 (46.3%)
Farming type
Sugar-cane	44	18.0 (40.9%)
Yam	17	7.0 (41.2%)
Rice	28	15.0 (53.6%)
Vegetable	32	16.0 (50.0%)	0.166
Total	121	56.0 (46.3%)

In addition, there was no statistical signifant difference in the primary demograhic factors of the particiants, however some of the combination of two or more of these factors were significantly different (Tables 1 and 2). The interaction of farming type and gender shows that male vegetable farmers were significantly different from the female vegetable farmers (OR 4.08, p = 0.001), while there were no significant difference among male and female of the other farming types when compared with sugar cane farming that served as the reference farming type (Table 2). Likewise, interaction between farming type and religion showed that there was no significant difference among Muslim/Christian farmers (Table 2). However, without the interaction effect, the model showed that vegetable farming was significantly different (OR 3.5, p = 0.027) by gender likewise yam farming (OR 0.13, p = 0.049) by religion from the other farming types, while the male farmers were in addition significantly different from their female counterpart (OR 3.5, p = 0.027).

Table 2.

Interaction effect of urinary schistosomiasis among farmers by gender and religion

Predictors	Infected farmers (gender)		Infected farmers (religion)
	OR (95% CI)	p value	OR (95% CI)	p value
Intercept	2.00 (0.75–5.33)	0.166	4.00 (2.00–8.00)	0.000
Farming type-Sugar-cane (Ref)	–	–	–	–
Farming type-Yam	5.63 (0.00–0.00)	0.996	0.13 (0.02–1.00)	0.049
Farming type-Rice	1.00 (0.25–3.99)	1.000	0.75 (0.26–2.16)	0.594
Farming type-Vegetable	3.50 (1.15–10.63)	0.027	0.62 (0.20–1.91)	0.409
Sex-Male	3.50 (1.15–10.63)	0.027
Farming type-Yam * Sex-Male	8.89 (0.00–0.00)	0.996
Farming type-Rice * Sex-Male	7.86 (0.16–3.87)	0.767
Farming type-Vegetable * Sex-Male	4.08 (0.01–0.26)	0.001
Religion-Islam			1.25 (0.49–3.17)	0.638
Farming type-Yam * Religion-Islam			4.80 (0.48–48.46)	0.184
Farming type-Rice * Religion-Islam			1.20 (0.30–4.82)	0.797
Farming type-Vegetable * Religion-Islam			1.76 (0.43–7.19)	0.431

OR odds ratio, CI confidence interval

Discussion and conclusions

The transmission and epidemiology of urinary schistosomiasis is associated with low socioeconomic status such as poverty, overcrowding and poor sanitation (Zhang et al. 2010), and other religious/occupational related activities like ablution, fishing and farming-irrigation activities. These factors that characterized Shonga and other similar communities usually encourage frequent human contact with probable contaminated water, and may account for the long standing history of schistosomiasis in the country (Amin 2018; Ofoezie 2002).

This study shows that the overall prevalence of urinary schistosomiasis is high (46.3%) among the farmers of Shonga, which is similar to the findings of Robert et al. (2008) that recorded 41.5% prevalence rate among farmers in Benue state, Nigeria. However, our result is lower than the 60% prevalence rate recorded by Farida and Hassan (2012) among rice growers in Morogoro, Tanzania, while it is higher than that of Damen et al. (2018), who recorded 18.7% among irrigation farmers in North-central of Nigeria. These variations may be related to several factors such as differences in socio-economic status, socio-cultural, public health provision, gender, personal hygiene, occupation and religion, as all these could influence regular human contact with contaminated water (Huang and Manderson 1992).

The significant difference noticed in some of the combination of the demographic factors as opposed to the non statistical significant difference in the primary demographic factors of the participants shows that religion and gender might be an underlining factors that are responsible for the prevalence of the infection among the study participants (Otuneme et al. 2019). These observed significant differences might be due to the varying usage of water among the participants. For example, females are more involved with water related activities (domestic chores) in the study area, while Muslims engage more with water related activities, i.e. “ablution rituals” which they do five times daily in addition to their regular anal or urethral orifice washing after urination or defecation. These practices might consequently predispose these groups to urinary schistosomiasis.

The result of the interactions between farming type and gender using sugar cane farming type as a reference point (given that this type of farming has been reported to be strongly correlated with schistosomiasis (Amorim et al. 2014)), shows that the male vegetable farmers were significantly different from their female counterparts, while there was no statistical difference in the classification of farming type by religion. In general, the observed differences in this study could be attributed to the varying level of engagement with water-related activities between the gender likewise confounding factors like religion/gender practices that influence regular human-water (probable contaminated) contact.

Although the generalization of our result is limited in statistical power due to our sample size and our seasonal sampling style, however the study shows that different factors could influence infection among the study participants. For example, the crop producers are statistically not uniformly exposed to the disease, especially when grouping the farmers by their gender and religion. While the authors agreed that it would be nice to conduct a similar investigation (longitudinal) with a larger population size for a more evidence-based inference, we however believe that our findings will be useful in guiding the policymakers in the appropriate channeling of future public health interventions in the study location as well as other communities with similar socio-environmental status during schistosomiasis control effort, especially among farmers who strive through the huddles to put food on our tables.

Supplementary Information

Below is the link to the electronic supplementary material.

Abbreviations

NTDs

Neglected tropical diseases

LGA

Local Government Area

WHO

World Health Organization

SCI

Schistosomiasis Control Initiative in Nigeria

WACIPAC

West African Centre for International Parasite Control

GLM

Generalized linear model

NGOs

Non-governmental organizations

TWAS

The World Academy of Sciences

CNPq

Conselho Nacional de Desenvolvimento Cientifico e Tecnologico

Author contributions

KAY, OAD and ABM collected the data. KAY wrote the first draft of the manuscript. AMA analyzed the data and critically revised the manuscript for important intellectual content. All authors read and approved the final version of the manuscript.

Funding

Adedayo Michael Awoniyi was a TWAS-CNPq PhD Fellow during this study.

Data availability

The datasets used and/or analyzed during the current study are available from the corresponding authors on reasonable request.

Declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval and consent to participate

Prior to the commencement of the study, we visited the community head (Emir) and explained the purpose of the research to him, after which we sought his approval for the study. Following this, we sensitized the community leaders (Chiefs), head of farmers association, women leaders and religion leaders about the purpose, importance and procedures of the study. Also, informed consent was verbally obtained from all participants included in the study. Participants were not forced to participate and were free to drop at any stage of the study.

Consent for publication

Not applicable.