Prevalence and Risk Factors of Human Taenia solium Cysticercosis in Mbulu District, Northern Tanzania

1. Introduction

Taeniasis and cysticercosis are human diseases caused by the pork tapeworm, Taenia solium. Cysticercosis in humans is the infection of the larval stage following the ingestion of pork tapeworm eggs (Galán-Puchades, 2016; Ito et al., 2015; Mata et al., 1996). Taeniasis is asymptomatic although carriers may suffer abdominal discomfort and weight loss(Okello & Thomas, 2017). The pork tapeworm larva in the human central nervous system causes neurocysticercosis(NCC), a serious medical condition in humans (Mahanty & Garcia, 2010). It is a brain disease that presents as epilepsy, chronic headache, visual disorders, dizziness, or nausea; the clinical manifestation depends on the immune response of the individual; the location of cysts, and their size and number (Del Brutto, 2014; Montano et al., 2005; Yancey et al., 2005).

Worldwide pork tapeworm infections prevail in poor subsistence farming communities in low and middle-income countries (Mwape et al., 2013; Rojas et al., 2019; Shukla et al., 2010). Taeniasis has been reported in Europe to range from 0.05-0.27% and ranges from 0-17.25% in Africa, Asia, and Latin America (Okello & Thomas, 2017). Neurocysticercosis causes up to 30 percent of all cases of acquired epilepsy in endemic localities (Mahanty & Garcia, 2010; Torgerson et al., 2015; Torgerson & Macpherson, 2011) which causes about 61 to 212 deaths annually in East African countries (Minani et al., 2022; Trevisan et al., 2017; Lozano et al., 2012).

Generally, pork tapeworm diseases in Africa have been estimated to be 0-13.9 % for taeniasis and 0.68-34.5% for cysticercosis and reported in 29 countries(Braae et al., 2015; Gulelat et al., 2022; Okello & Thomas, 2017). About 0.95-3.08 million people are estimated to suffer from symptomatic NCC in sub-Saharan Africa (Winkler, 2012). In Eastern Africa, human T. solium cysticercosis is endemic with pooled prevalence ranging from 14-20 % (Gulelat et al., 2022). The disease is endemic in Tanzania, with an average seroprevalence of about 17% and the disease accounted for 212 deaths and 17,853 NCC incident cases for the year 2012 (Mwang’onde et al., 2012; Mwanjali et al., 2013; Mwita et al., 2013; Trevisan et al., 2017).

Human T. solium cysticercosis is associated with community practices and poor sanitation. Open defecation, unsafe water sourcing, and consumption of uninspected and undercooked infected pork increase the risk of human infections. (Mwang’onde et al., 2012; Kabululu et al., 2020; Mwape et al., 2013; Ngowi et al., 2004,; Pondja et al., 2010). Studies have shown clean and safe water reduce infection in both human and pig, furthermore the clean practices of feeding pigs reduce the risks of infecting pigs (Kabululu et al., 2023). The underuse of pit latrines and improperly constructed toilets give access of pigs to toilets thus easily accessing faces (Kabululu et al., 2020). The pig-free-ranging practices is another risk factor for pork tapeworm transmission in the endemic communities (Mwanjali et al., 2013; Ngowi et al., 2004).

The prophylaxis treatment is among the means of reducing the transmission of intestinal and tissue worms. The current treatment guideline for pork tapeworm diseases gives directives for treatment in humans (Chemotherapy, 2021). The prophylaxis and vaccine in pigs is currently in research work not practiced in communities but the result showed the high efficacy of combined TSOL18 and oxfendazole (Kabululu et al., 2020). The current prophylactic treatment using praziquantel and albendazole for schistosomiasis and soil-transmitted helminths is targeting school children only (World Bank, 2018a).

Although pork tapeworm is listed by the World Health Organization (WHO) as the number one cause of food-borne diseases (Torgerson et al., 2015), it is not considered a priority disease in Tanzania, thus receiving less attention in terms of surveillance and interventions (CDC, 2017). The current nationwide intervention among school children using praziquantel and albendazole targets schistosomiasis and soil-transmitted helminths but not pork tapeworm (Resources, 2003; World Bank, 2018a). We conducted this study to determine the effect of anthelminthic treatment among school children on the transmission of pork tapeworm in communities of Mbulu district in Tanzania.

2. Material and Methods

2.1. Study Area

The study was conducted in Mbulu District of northern Tanzania in March-April 2021. The district is among six districts of Manyara region in Tanzania located at latitude 3˚45′ and 4˚ S and longitude 35˚20′ and 36˚E at an altitude ranging from 1,000–2,400 meters above mean sea level. The district has an area of 3,800 square kilometres and a population of 320,279; among these, 161,548 are males and 158,731 are females. About 48,976 are in urban and 271,303 are in rural areas (National Bureau of Statistics & Office of Chief Government Stastician, 2013). Crop farming and livestock keeping are the main economic activities for 96% of the population (DPLO, 2015). The district administers anthelmintic to pre and school children annually as part of the national deworming program using praziquantel and albendazole targeting schistosomiasis, and soil-transmitted helminths which started in 2002 in Tanzania (Resources, 2003; World Bank, 2018a). Primary school Children in all villages in the district including those selected for study received the intervention conducted by Neglected Tropical Diseases Control program Tanzania collaborating with local governments. The study area was selected as a result of the high prevalence and cysticercosis burden of pork tapeworm from previous studies of 16.3% prevalence (Mwang’onde et al., 2012, 2018)

2.2. Study Design

This was a community-based cross-sectional study conducted in Mbulu district Northern Tanzania from March to April 2020.

2.3. Sampling and Sample Size

Three wards namely Maghang, Dinamu and Bashay were randomly selected from 15 pig-keeping wards, the inclusion criteria were pig keeping communities; three wards were excluded out of 18 wards. From each of the three wards, one village was randomly selected and included in this study (Figure 1). The households were conveniently sampled based on the presence of pigs and history of keeping pigs and the consent of the household leader. The consented adult and assented minor participants from households aged five years and above were recruited for the study, the study included five years because they are enrolled in pre-and primary school and are targeted by the deworming program. The study villages selected were Maghang Juu, Diyomati and Harsha. The sample size was computed using Fisher’s formula (Rotondi & Donner, 2012) Z= 1.96, p= 16.3%, d= 0.0418 estimating a sample size of 300 participants (Mwang’onde et al., 2012).

2.4. Data Collection

2.4.1. Questionnaire Method

The household leaders were asked about risk factors related to cysticercosis on source of water and participation in previous deworming programs. Observations and responses on the availability of pit latrines, water sources, and pigs keeping were recorded. The data were collected electronically using tablets installed with koBocollect software. The information recorded among study participants was on education, occupation, and participation in deworming programs by swallowing anthelmintic in the last deworming program.

2.4.2. Sample Collection

Five millilitres of blood was drawn from each participant including the head of households who consented and assented children in the household and transferred into a plain vacutainer tube and stored in a cool box packed with ice cubes. The blood samples were centrifuged at 1500 rounds per 15 minutes and the supernatant was transferred into cryovials and stored in a -20⁰ freezer until laboratory tests were done.

2.4.3. ELISA Method

The detection of cysticercosis was done using ApDia Ag ELISA (Reference number 650505; apDia, Raadsherenstraat 3 2300 Turnhout, Belgium) for the determination of viable metacestode of Taenia species (ApDia, 2004). ELISA cut-off value for antigen was calculated, a cut-off value = mean Optical Density (OD) negative × 2). A positive reaction corresponded to the antigen index above or equal to 1.3 while the antigen index value below or equal to 0.8 was negative. A grey zone between 0.8 and 1.3 was considered doubtful and was retested.

2.5. Data Analysis

Data were analysed using SPSS software, version 20. Continuous variables are summarized by the measure of central tendency and their respective dispersion. Categorical variables were summarized by proportions and frequencies and compared by chi-square test. Odds ratio and 95% confidence interval were used and a p-value of less than 5% was considered significant.

2.6. Ethical Consideration

This study was approved by the Medical Research Coordinating Committee of the National Institute for Medical Research in Tanzania (Reference No. NIMR/HQ/R.8c/Vol.1/1612). Written informed consent was obtained from all subjects’ ≥18 years, and consent was obtained from parents or guardians of the respective individuals below 18 years old following the subject’s assent.

3. Results

3.1. Demographic Characteristics

A total of 300 individuals were involved in the study. The median age was 19 years and the mode was 7, with a maximum of 89 and a minimum of 5 years. Female and male participants were almost equally represented (Figure 2 and Table 1).

3.2. Prevalence of Cysticercosis

The overall prevalence of human T.solium cysticercosis was 23(7.67%), among these 12(8.27%) were males and 11(7.09%) were females. The prevalence was higher 6(11.76%) among those aged 26-35 years and ±45 years. There was no statistically significant difference in the prevalence by age group, sex, and occupation (Table 2). Among the 300, 82(27.3%) had received anthelminthic during the previous year. Among 23(7.67%) who tested positive by antigen test 5(21.7%) received anthelmintic. The likelihood of infection among anthelminthic users and non-users was low by 28% [0.72 (0.26-2.01)], but the protection was not statistically significant.