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Keywords:

  • epidemiology;
  • Nepal;
  • social composition;
  • Taenia asiatica;
  • Taenia solium
  • épidémiologie;
  • Népal;
  • composition sociale;
  • Taenia asiatica;
  • Taenia solium
  • epidemiología;
  • Nepal;
  • composición social;
  • Taenia asiatica;
  • Taenia solium

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Ethical aspects
  6. Results
  7. Discussion
  8. Acknowledgements
  9. References

The transmission of the zoonotic pork tapeworms Taenia solium and T. asiatica depends on a combination of specific risk factors, such as open defecation, backyard pig raising and the consumption of raw or undercooked pork and viscera. A community-based survey was conducted among 289 households in south–eastern Nepal to study the heterogeneity of these risk factor frequencies as a function of the social composition of the population. The frequency of open defecation, backyard pig raising and pork consumption differed significantly (P < 0.005) among the different coexisting caste and ethnic groups. In the same survey, the taeniosis prevalence was examined among the different groups. Tapeworm carriers were identified at a high prevalence among the Dum, one of the most disadvantaged communities of Nepal. A PCR-RFLP assay revealed that all collected tapeworm specimens were T. asiatica, a species thus far not known to occur in South Asia. These results can help to understand the epidemiology of T. solium in Nepal, which appears to be more complex than thought so far.

La transmission de la zoonose du porc Taenia solium et T. asiatica dépend d’une combinaison de facteurs de risque spécifiques, tels que la défécation en plein air, l’élevage de porcs dans l’arrière-cour et la consommation de viande de porc crue ou mal cuite et des viscères. Une enquête basée sur la communauté a été menée auprès de 289 ménages dans le sud-est du Népal afin d’étudier l’hétérogénéité des fréquences de ces facteurs de risque en fonction de la composition sociale de la population. La fréquence de la défécation en plein air, de l’élevage de porcs dans l’arrière cour et de la consommation de porc différait significativement (P < 0,001) entre les différentes castes et groupes ethniques coexistants. Dans la même enquête, la prévalence de téniase a été examinée entre les différents groupes. Les porteurs de ténia ont été identifiés avec une prévalence élevée chez les Dum, l’une des communautés les plus défavorisées du Népal. Un test PCR-RFLP a révélé que tous les échantillons prélevés contenaient T. asiatica, une espèce jusque-là non connue en Asie du Sud. Ces résultats peuvent aider à comprendre l’épidémiologie de T. solium au Népal, qui semble être plus complexe qu’on ne le pensait jusqu’ici.

La transmisión de las tenias del cerdo zoonóticas, Taenia solium y T. asiatica, depende de una combinación de factores de riesgo específicos, tales como la defecación a campo abierto, la cría de cerdos en patios traseros y el consumo de carne y vísceras de cerdo crudas o mal cocidas. Se llevó a cabo un estudio comunitario en 289 hogares del sudeste de Nepal, para averiguar la heterogeneidad en la frecuencia de estos factores de riesgo en función de la composición social de la población. La frecuencia de la defecación a campo abierto, de la cría de cerdos en el patio trasero y del consumo de cerdo diferían de forma significativa (P < 0.001) entre las diferentes castas y grupos étnicos. En el mismo estudio se examinó la prevalencia de teniasis entre los diferentes grupos. Se identificó una alta prevalencia de portadores de tenia entre los Dum, una de las comunidades más desaventajadas. Una prueba de PCR-RFLP reveló que los especímenes de tenia recolectados eran de T. asiatica, una especie que hasta ahora se desconocía que estuviese presente en el sudeste asiático. Estos resultados podrían ayudar a entender la epidemiología de T. solium en Nepal, la cual parece ser más compleja de lo que hasta ahora se pensaba.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Ethical aspects
  6. Results
  7. Discussion
  8. Acknowledgements
  9. References

Taenia solium is a neglected zoonotic parasite endemic to most underdeveloped countries and regions where pig raising and pork consumption are not restricted (Dorny et al. 2009). Its life cycle involves humans as definitive and pigs as intermediate hosts, but its clinical importance is mainly related to the accidental intake of tapeworm eggs by humans and their development into cysticerci in the host’s central nervous system – a condition called neurocysticercosis. The presence of this parasite in Nepal was first reported more than 30 years ago (cited by Joshi et al. 2004); yet further research has remained limited. As a result, very little is known about the local risk factors and the public health importance of this zoonosis.

The epidemiology of the T. solium is characterised by a focal distribution of human tapeworm carriers and porcine cysticercosis cases. Socio-economic, cultural and religious differences between communities have been claimed responsible for this phenomenon (Morales et al. 2006; Somers et al. 2006; Carabin et al. 2009). Indeed, the transmission of this pork tapeworm strongly depends on the presence of a combination of specific risk factors. Open defecation, pigs having free access to human faeces and uncontrolled slaughtering of infected pigs are major factors and are strongly linked to poverty and underdevelopment. To complete the parasite’s life cycle, humans must eat infected pork raw or undercooked, which is mainly influenced by cultural preferences.

Recent literature suggests that the transmission dynamics of T. solium can be affected by co-occurring Taenia species, most notably T. hydatigena, T. saginata and T. asiatica (Conlan et al. 2009). The latter is a parasite with an analogous life cycle to that of T. solium, but with different behaviour in its intermediate hosts. In pigs, T. asiatica cysticerci are most commonly found in the liver, whereas T. solium cysticerci mostly occur in the muscles. T. asiatica is not known to cause cysticercosis in humans and thus has much less clinical importance. This parasite’s geographical distribution is presumed to be restricted to South-East Asia, not affecting South Asian countries such as Nepal (Eom et al. 2009).

The majority of the Nepalese population belongs to two distinct groups the caste-origin Hindu and the Janjati or indigenous nationalities. The complex migratory history of these groups has given rise to a coexisting mix of ethnic and caste groups, each with their own socio-economic status and cultural and religious practices (Pandey 2005). The caste or ethnic group to which a person belongs also influences his attitude towards pigs and pork. In the Hindu caste system, pigs are considered untouchable and can only be touched, raised and eaten by the lowest Hindu castes, the Dalit. In this respect, the Dum, one of the most disadvantaged Dalit communities usually living in urban slums, are known as traditional herdsmen of the Hurra pig, a primitive breed indigenous to the southern Terai plains of Nepal. In contrast, most Janjati consider pigs as valuable and use them in certain religious ceremonies.

So far the possible impact of this heterogeneity in cultural practices on the transmission of pork tapeworms has not received due attention. Therefore, this study aimed to determine the intraregional differences in transmission risk factors and taeniosis prevalences.

Materials and methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Ethical aspects
  6. Results
  7. Discussion
  8. Acknowledgements
  9. References

Between 2009 and 2011, we conducted a community-based survey in the eastern Terai of Nepal, a region with a high density of pigs and pork consumers. The study was set in Mrigauliya (Morang district), a rural village inhabited by a heterogeneous population: upper and lower Hindu castes and hill- and Terai-originating Janjati. Four Dum communities in nearby cities were also included.

A one-stage cluster sampling design was used to select the study area. One ward was randomly selected in Mrigauliya, and all households in this ward were included in the survey. The four Dum communities were selected based on their proximity to this study area. In total, 289 households were included in the study, comprising hill Janjati (n = 24), Terai Janjati (n = 110), high-caste Hindus (n = 51), Dum (n = 78) and other Dalit groups (n = 26). The education level and average life span, taken as proxy for the socio-economic status, were highest among the high-caste Hindus, followed by the hill Janjati and the Terai Janjati (results not shown). Both parameters were lowest among Dalit, and among the Dum in particular.

Using a questionnaire, information was gathered regarding the main risk factors for T. solium and T. asiatica transmission, that is, open defecation, backyard pig raising and frequent (i.e. weekly) pork consumption. In addition, suspected tapeworm carriers were identified by self-detection – the declaration of passing tapeworm segments in the stool. These cases were subsequently asked to identify a tapeworm segment out of a series of photos of common human helminths to eliminate false-positive statements. Thus identified tapeworm carriers were given niclosamide (2 g) and a purgative (bisacodyl, 10 mg) to kill and expel the tapeworm. Finally, collected tapeworm specimens were analysed by a PCR-RFLP assay of the mitochondrial 12S rDNA gene (Somers et al. 2007). Based on two specific restriction enzymes, DdeI and HinfI, this molecular tool is able to differentiate the three human Taenia species: T. solium, T. asiatica and T. saginata.

Fisher’s exact test was used to test whether differences in risk factor frequencies existed between the different caste and ethnic groups, using a significance level of 5%. Next, all ten pairwise comparisons between the five included caste and ethnic groups were performed using Fisher’s exact test at the Bonferroni corrected significance level of 0.5% (0.05/10).

Ethical aspects

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Ethical aspects
  6. Results
  7. Discussion
  8. Acknowledgements
  9. References

All participants were asked for their informed consent prior to being enrolled in the study. At the end of the study period, the inhabitants of the selected areas were invited to undergo a free medical check-up during a locally organised public health camp. This study was approved by the Nepal Health Research Council and by the Ethical Review Board of Ghent University Hospital.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Ethical aspects
  6. Results
  7. Discussion
  8. Acknowledgements
  9. References

Results of open defecation was significantly more common (P < 0.005) among Dalits and Terai Janjati than among hill Janjati and high-caste Hindus, whereas the Dum took an intermediate position (Figure 1a).

image

Figure 1.  Frequency of Taenia solium and T. asiatica transmission risk factors (a–c) in south–eastern Nepal, among five caste and ethnic groups, ordered by decreasing socio-economic status. Groups denoted by a different letter differ significantly from each other (P < 0.005).

Download figure to PowerPoint

The hill Janjati raised pigs significantly more frequently (P < 0.005) than the other Dalit, whereas the Terai Janjati and the Dum took a middle position. High-caste Hindus did not raise pigs (Figure 1b).

Weekly pork consumption was significantly more frequent (P < 0.005) among the Dum than among any other caste or ethnic group. High-caste Hindus consumed no pork at all (Figure 1c).

Tapeworm carriers were only identified in the Dum community, at a remarkably high prevalence of 13.5% (71/524). All of these carriers were provided with niclosamide and bisacodyl. After three rounds of community visits, tapeworms could be collected from 16 (22.5%) suspected carriers. Unexpectedly, molecular diagnosis revealed that all collected specimens were T. asiatica, and not T. solium.

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Ethical aspects
  6. Results
  7. Discussion
  8. Acknowledgements
  9. References

In this study, we investigated the occurrence of risk factors for the transmission of the zoonotic pork tapeworms T. solium and T. asiatica in five caste and ethnic groups in south–eastern Nepal. Significant differences were found in the frequencies of open defecation, backyard pig raising and frequent pork consumption. Open defecation tended to be more common as the socio-economic status decreased. However, the Dum, assumed to be the poorest group in our study, did not have the highest open defecation frequency, perhaps because two of the four Dum communities had been the subject of toilet construction programmes. The hill Janjati more commonly raised pigs, but tended to keep their pigs in sheds, whereas the Terai Janjati and Dalit preferred tethering and free ranging systems. All Dum households reported to consume pork at least once a week, which was significantly more often than the other Dalit and the Janjati. Frying and boiling were the most common ways of preparing pork among all pork-consuming respondents, but some Dum claimed to eat undercooked meat and viscera of home-raised Hurra piglets during certain religious and social festivities. High-caste Hindus neither raised nor ate pigs.

Identification of tapeworm carriers and subsequent tapeworm isolation and species determination revealed that T. asiatica is endemic to the south–east of Nepal. This raises questions about the true geographical spread of this parasite, because it does not appear to be restricted to South–East Asia, as thought so far (Eom et al. 2009). On the other hand, no T. solium tapeworm carriers could be identified in our study, although this parasite is known to be endemic to Nepal, and the transmission risk factors were present in the studied populations. This might be due to the low tapeworm recovery rate in our study or to the low sensitivity of self-detection for T. solium proglottids, which are immobile and, consequently, less visible, unlike T. asiatica and T. saginata tapeworms (Somers et al. 2007). However, predominance of one tapeworm species in a certain area may also be caused by interspecific competition, as suggested by Conlan et al. (2009), and therefore does not necessarily exclude a high prevalence of other species in other areas.

Strong intraregional differences in transmission risk exist between caste and ethnic groups in Nepal, complicating the epidemiology of the pork tapeworms. In our study, we could not identify a clear link between the socio-economic status of a group and its overall frequency of transmission risk factors, reflecting the importance of cultural and social risk factors. The high taeniosis prevalence among the Dum suggests, however, that certain groups might be of particular importance for maintaining the life cycles of the zoonotic pork tapeworms. In our study, we could only identify T. asiatica, and not T. solium, which is the only pork tapeworm of clinical importance. However, given the fact that both tapeworms share the same risk factors, we hypothesise that such groups might also be at higher risk for T. solium transmission. Moreover, in other areas, T. solium might have a competitive advantage over T. asiatica, in line with the hypothesis of interspecific competition (Conlan et al. 2009). More research is therefore warranted to identify other such high-risk groups in Nepal, and to confirm our findings for T. solium. Such information could eventually lead to targeted control programmes, which would not only have an impact on the targeted groups, but also on the population as a whole.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Ethical aspects
  6. Results
  7. Discussion
  8. Acknowledgements
  9. References

We are very grateful to the people of Mrigauliya and adjacent areas for their willingness to participate in our study. We would like to thank Mr Tej Raj Karki, Mr Keshab Karki and Mrs Bimala Poudel for their technical assistance in the field, and Mr Bjorn Victor and Ms Inne Pauwels of the Institute of Tropical Medicine for performing the molecular analyses. This study was supported by the Flemish Interuniversity Council, Belgium.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Ethical aspects
  6. Results
  7. Discussion
  8. Acknowledgements
  9. References
  • Carabin H, Millogo A, Praet N et al. (2009) Seroprevalence to the antigens of Taenia solium cysticercosis among residents of three villages in Burkina Faso: a cross-sectional study. PLoS Neglected Tropical Diseases 3, e555.
  • Conlan JV, Vongxay K, Fenwick S, Blacksell SD & Thompson RC (2009) Does interspecific competition have a moderating effect on Taenia solium transmission dynamics in Southeast Asia? Trends in Parasitology 25, 398403.
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