Introduction

Taeniosis and cysticercosis are different stages of Taenia solium infection involving swine as intermediate hosts and humans as definitive and/or intermediate hosts. Taeniosis is the intestinal infection with the adult cestode in humans and is caused by consumption of raw or undercooked pork containing viable cysticerci of T. solium. Ingestion of infective eggs passed by a person with taeniosis either by autoinfection, direct contact with another tapeworm carrier or indirectly via ingestion of contaminated food, water, or hands may also lead to cysticercosis in humans whereby larval tapeworm cysts develop in the muscles, eye and central nervous system. Pigs get cysticercosis by ingesting T. solium eggs primarily as a result of eating feces of a human tapeworm carrier. Human cysticercosis causes a variety of neurological symptoms, most commonly seizures due to cysts in the brain, a condition known as neurocysticercosis [1], [2].

Cysticercosis imposes substantial global burden on human beings related to epilepsy, ocular disorders, other neurological manifestations, and economic losses related to disability and lost productivity [3], [4]. A World Health Organization (WHO)-commissioned systematic review of studies reporting the frequency of neurocysticercosis (NCC) worldwide done by [5] estimated the proportion of NCC among people with epilepsy of all ages to be 29.0% (95% CI: 22.9%–35.5%), indicating epilepsy is consistently associated with NCC in over one quarter of patients residing in regions where T. solium infections are endemic. In sub-Saharan Africa, people with cysticercosis have been estimated to have a 3.4. to 3.8-fold increased risk for developing epilepsy [6]. These estimates confirm the importance of NCC infection in the etiology of epilepsy in developing countries and suggest that NCC may be associated with a very large burden in cysticercosis endemic areas where epilepsy is prevalent, that is, those countries where pork consumption occurs, pigs are managed under free-range conditions, and sanitation is poor or absent enabling pigs to have access to human feces [5]. Although the recognition of its status as a serious and emerging threat to public health in Africa is increasing [7] (WHO, 2010), the data on incidence in humans is very limited in most endemic areas due to a lack of adequate surveillance, monitoring and reporting systems [8].

In Tanzania T. solium is considered widespread in the northern, central, and southern regions based on porcine cysticercosis surveys [9], [10], [11], [12], [13]. These surveys provide initial evidence that T. solium infection is of national importance. Despite the high prevalences of porcine cysticercosis reported in different areas of the country, the presence of human T. solium infection has only been confirmed at one hospital in Mbulu district, Manyara region in the northern highlands where 13.7% of patients with epilepsy were detected to have probable/definitive NCC based on brain scans using computerised tomography and western blot to detect antibodies to larval T. solium [14]. However, there is still a lack of information on the T. solium situation (both taeniosis and cysticercosis) in the general human population [15], thus the basis for conducting the present cross-sectional survey with the aim of establishing the prevalence and identifying risk factors associated with the transmission of human T. solium infections in rural communities in the southern highlands of Tanzania which is the main pig raising area of the country [16].

Methods

Results

By the end of the study 70 households dropped out such that 830 in total completed the survey (92.2% compliance). Out of 830 enrolled participants, 476 (57.4%) were males and 354 (42.6%) were females. The age range of study participants was 15–60 years with mean age of 37.9±11.3 (SD) years. A large proportion of participants had finished primary education (77.1%) and the least had college or university education (0.5%). Regarding participants' religions, Christians were the majority (82.4%), followed by no religion/pagans (15.9%), and Muslims (1.7%). Furthermore, inhabitants enrolled in the study consisted mostly of farmers (85.4%).

Of the 830 human sera examined, Ag-ELISA found 16.7% with active cysticercosis while Ab-ELISA detected an overall seroprevalence of 45.3%. Furthermore, among the 427 participants in total who tested positive serologically, 20.6% tested positive with both tests, while 11.9% tested positive with Ag-ELISA only and 67.5% tested positive with Ab-ELISA only (see Table 1).

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Table 1. Prevalence of Taenia solium and other helminth infections in Mbozi district, Mbeya Region, Tanzania.

https://doi.org/10.1371/journal.pntd.0002102.t001

Of the 820 study participants who returned stool samples, 5.2% tested positive for taeniosis by copro-Ag-ELISA, and 79.1% of copro-Ag-ELISA positive participants had T. solium adult worm specific antibodies (taeniosis) using EITB indicating 4.1% of total participants had T. solium specific taeniosis. In addition, Taenia spp. eggs were detected using formol-ether concentration technique (microscopic examination) in 1.1% stool samples. Other parasite eggs detected during coprological examination included those of hookworms (14.1%), Schistosoma mansoni (1.6%) and Ascaris lumbricoides (1.0%) (see Table 1).

Generally most households surveyed had pit latrines (98.4%), however, 66% of pit latrines in those households had partial walls making them easily accessible to free roaming pigs. In addition, 54% reported using unsafe sources of drinking water such as stagnant, surface water from streams, ponds, or uncovered shallow wells. Information on personal hygiene indicated that multiple people using the same water in which to wash their hands by dipping was the most common method (54.3%), while no one reported washing their hands with soap.

With regard to information on symptoms associated with human cysticercosis 14.8% acknowledged a history of epileptic seizures, 52.0% severe chronic headaches, 17.1% loss of consciousness, and 50.8% partial seizures. Only history of epileptic seizures and chronic severe headaches were determined to be statistically important symptoms associated with human cysticercosis (p≤0.05) (Table 2).

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Table 2. Associations between reported neurological symptoms and T. solium positivity (Ag- and Ab-ELISA), Mbozi district, Tanzania.

https://doi.org/10.1371/journal.pntd.0002102.t002

Neurocysticercosis was detected by cranial CT scan in 30 (54.6%) of the 55 Ag-ELISA seropositives who accepted to undergo examination. All of the 28 seropositive people with a history of epileptic seizures were CT-scan positive for NCC. Twenty-eight of the thirty NCC cases detected by CT scan (93.3%) had more than 5 cysts in the brain.

Multiple regression analysis

The risk factors that were significant in the analysis as risks associated with human cysticercosis are presented in Table 3. Being older age was found to be a risk for seropositivity with human cysticercosis in the regression model, as the Ag-ELISA was higher in the age groups 36–45 years (OR = 2.5) and 46–60 years (OR = 2.6) as compared to young people (<25 years). In addition, those who reported washing their hands by the dipping method using the same water as others were more likely to be seropositive by Ag-ELISA (OR = 3.8).

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Table 3. Multivariate analysis on risk factors for human cysticercosis considered in the logistic regression analysis.

https://doi.org/10.1371/journal.pntd.0002102.t003

On the other hand, when fitting the risk factors for seropositivity with human cysticercosis by Ab-ELISA in the regression model, results showed the risk for seropositivity to be significantly higher for males as compared to females (OR = 1.6), and for people using an unsafe source of water (OR = 1.9). Furthermore, being confirmed a T. solium tapeworm carrier by copro-Ag-ELISA substantially increased the risk for being seropositive for cysticercosis by both tests.

Discussion

This is the first community-based study in Tanzania to determine the magnitude of human T. solium infection in an area previously reported to have a high prevalence of porcine cysticercosis. Findings indicate detection of active cysticercosis in 16.7% of the human population while 45.3% tested positive for exposure to larval T. solium through detection of antibodies. These findings are higher in comparison to that reported elsewhere in the region such as 4.6% (Ag-ELISA), 6.9% (EITB) and 40.8% (Ab-ELISA) in Burundi [25], 12.1% (Ab-ELISA) in Mozambique [26], 0.4%–3% (Ag-ELISA) in Cameroon [27], [28], and 7.7% (Ag-ELISA and EITB) in Senegal [29], but lower than the 21.6% (Ag-ELISA) recently reported from the Democratic Republic of Congo [30].

Of the study participants who reported a history of epileptic seizures 22.8% were seropositive by Ag-ELISA (all these were also CT-scan positive for NCC) while 53.7% were positive by Ab-ELISA. These findings are higher in contrast to another study in Africa which used both tests whereby 1.2% and 44.6% of people having epileptic seizures were found positive by Ag-ELISA and Ab-ELISA, respectively, in Cameroon [31]. The findings on antibody detection in people having epileptic seizures were higher in this study compared to other reports elsewhere: 14% (EITB) in northern Tanzania [14], 35.7% (Ab-ELISA) in western India [32], 22.5% (EITB) in Peru [33] and 31.3% (EITB) in Mexico [34]. These results are of course influenced by the method or definition applied for epileptic seizures. Furthermore, the results are in agreement with findings in other studies indicating a strong association between epileptic seizures and cysticercosis [5], [35], [36], [37]. Indeed a recent community-based survey of adult active epilepsy in northern Tanzania [38] identified a high rate of focal onset seizures suggesting that a high proportion of epilepsy in the studied population may be due to identifiable, and possibly preventable, causes specifically referring to NCC and recommended further investigation of risk factors.

Three tests were used to diagnose taeniosis due to T. solium for prevalence estimation: the formol-ether concentration technique for detecting Taenia spp. eggs, the copro-Ag-ELISA for detecting antigens of Taenia species tapeworms [39] and the EITB-(eRS38) for detecting antibodies to adult T. solium tapeworms. The overall prevalence of taeniosis of 1.1% by formol-ether concentration technique, and 5.2% by copro-Ag-ELISA, are within the previous reported range of 0.6%–1.9% (microscopy) and 2.8%–14% (copro-Ag-ELISA) from comparable studies in Mexico and Peru [33], [40], [34]. These results also support previous findings that the prevalence of intestinal taeniosis is low in most endemic communities and microscopy-based figures underestimate the true prevalence of T. solium and would be a poor monitoring tool for control purposes. The detection of 4.1% T. solium-specific taeniosis cases in this study using EITB (eRS38) is substantial though we are unable to compare these findings to other surveys in Africa since, to the authors' knowledge, no other studies reporting the use of EITB for detection of T. solium tapeworm antibodies have been reported from the continent. However, further development of a simple and highly specific test for detecting T. solium taeniosis is warranted as the sensitivity of the EITB for taeniosis is reported to be 94.5–97% and there are reports of cross reaction of eRS38 to T. saginata and Schistosoma species [24], [41].

Consumption of T. solium cysticerci in pork is crucial for transmission of human T. solium infections (taeniosis/cysticercosis). Pork consumption was the only significant risk factor associated with NCC found among epileptic patients studied in northern Tanzania [42]. Home slaughtering of pigs with only limited or no inspection of the carcass/meat as well as frequent consumption of undercooked pork at local brew bars have been noted to be common practices in the southern highlands [43]. Community-based studies on porcine cysticercosis conducted in Tanzania have reported high prevalences of porcine cysticercosis in different parts of the country where pig keeping is popular: 17.4% (lingual exam) in the northern highlands district of Mbulu [11], 5.1%–16.9% (lingual exam) and 30.4%–32.0% (Ag-ELISA) in districts of Iringa, Mbeya and Ruvuma regions in the southern highlands [12]. As shown in Mbozi district infected pigs can be a sentinel of human infections with T. solium thus these other areas are likely to be endemic for human cysticercosis and taeniosis as well.

From Tanzania [12] reported increasing production and transportation of pigs from endemic rural communities where cysticercosis control regimens are limited or non-existent to large urban areas where pork demand is high and growing. Transportation of pigs and pork from rural cysticercosis endemic areas increases the risk of transporting infected and diseased pigs/pork into non-endemic urban areas for slaughter/sell as evidenced by [13] who found 5.9% of pigs brought into Dar es Salaam for slaughter were infected with T. solium by routine meat inspection. This has important epidemiologic implications for the country regarding transmission of cysticercosis/taeniosis especially in urban areas where pig keeping is not practiced but pork consumed.

Porcine cysticercosis has also been reported in many of the countries bordering Tanzania including Kenya, Uganda, Zambia, Democratic Republic of Congo and Mozambique [44], [45], [46], [47], [48]. These results indicate widespread presence of T. solium infections in the region such that cysticercosis should be viewed as an eastern and southern Africa regional issue rather than as a Tanzania specific problem.

It has been found that sero-prevalence of active human cysticercosis in the studied communities showed an increase with age and reached a maximum in participants aged 36–60 years. This supports the finding among epilepsy patients in northern Tanzania with NCC who tended to be older with a later onset of seizures compared to those without NCC [42]. Similar observations were reported by [32] in western India and [49] in Chaco region, Bolivia. However, the age dependency was not observed with regard to detection of antibodies against cysticerci which has been shown by others [50] indicating the need for further studies on T. solium transmission dynamics in the area.

The prevalence of antibodies to cysticercosis in females was significantly higher than in males in this study which agrees with the findings reported by [40] in Guatemala showing higher infection proportions in females but contrasts with the findings reported by [51] in Vietnam which reported higher prevalence in males as well as the findings reported by [49] in Chaco region, Bolivia, which showed no significant difference between genders.

Strong association between taeniosis and human cysticercosis (both active and antibodies) was found in the present study similar to other studies conducted in different areas of the world [32], [33]. The significant numbers (34) of sera of the subjects diagnosed with active taeniosis by copro-Ag-ELISA were positive with both Ag-ELISA and Ab-ELISA. Similarly [33], [34], [51] found similar results that many study subjects in Peru, Mexico and Vietnam, respectively, were infected with both taeniosis and cysticercosis.

In [52] it was reported that cysticercosis may also occur in humans if eggs are conveyed to the mouth by unclean fingers after defecation or eating without washing hands. This study found significant association between the type of hand washing and human cysticercosis prevalence in contrast to the study by [53]. Washing with running water in contrast to dipping, may be due to a bias in the sense that availability of running water in the household reflects a different sanitary level in general.

Although the symptoms and signs of NCC are highly protean, it is commonly associated with late onset of epileptic seizures, focal neurological signs (partial seizures), severe chronic headache, intra-cerebral hypertension, and cognitive behavioral dysfunctions [33], [54], [55]. The frequencies of different manifestations, complications and disabilities associated with NCC estimated through a WHO-commissioned review found that among patients seen in neurology clinics, epileptic seizures were the most common manifestation (78.8%) followed by headaches (37.9%), focal deficits (16.0%) and signs of increased intracranial pressure (11.7%) [56]. High correlation was found in this study between history of epileptic seizures and seropositivity with Ag-ELISA and Ab-ELISA as well as CT scan results. All 28 participants with a history of epileptic seizures and seropositive by Ag-ELISA (as inclusion criteria for CT scan in this study) had NCC features on CT scan, and consequently at least 22.8% of participants reporting history of seizures had NCC, as mentioned earlier. This indicates a significant contribution of NCC to active epilepsy cases diagnosed in the current study. Nevertheless, this figure is higher than expected for developing countries. Using a questionnaire approach we cannot rule out false-positive answers, however if epileptic seizures were over-reported the proportion with confirmed NCC would actually go down. Similarly, severe chronic headache was an important factor associated with Ag-ELISA seropositivity, indicating increased intracranial pressure. Similar findings have been reported by [27], [32], [34].

Despite the fact that T. solium infections have been suggested to be successfully controlled in an endemic country like Mexico [57], the lack of diagnostic tools for detection of human cysticercosis/neurocysticercosis (e.g. serological tests, neuroimaging) and taeniosis (e.g. copro-Ag-ELISA, EITB) in Tanzania is a constraining factor for effective management and control of the infections at the community level. Moreover, the cost for the neuroimaging tests (CT scan or MRI) is too expensive for ordinary people and their availability is very limited in resource poor endemic areas. Detection of circulating T. solium cysticercosis antigen using Ag-ELISA has been shown to improve the diagnostic potential for neurocysticercosis, especially in areas where neuroimaging techniques are not accessible [58]. The establishment of affordable, reliable diagnostic tools as well as sustainable and appropriate preventive and control measures is warranted as the reduction of neurocysticercosis would be expected to significantly reduce the burden of epilepsy [59].

Supporting Information

Acknowledgments

We thank the U.S. Centers for Disease Control and Prevention, Atlanta, Georgia, USA and the University of Zambia, Lusaka, Zambia for assisting us with testing of samples. Dr. Deogratius Mtasiwa (Chief Medical Officer, Ministry of Health and Social Welfare, Tanzania) and Prof. Karim Hirji (Biostastistician Muhimbili University of Health and Allied Sciences, Tanzania) provided helpful assistance in conducting the study.