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      Taenia solium Cysticercosis in the Democratic Republic of Congo: How Does Pork Trade Affect the Transmission of the Parasite?

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          Abstract

          Background

          Taenia solium, a zoonotic parasite that is endemic in most developing countries where pork is consumed, is recognised as the main cause of acquired epilepsy in these regions. T. solium has been reported in almost all of the neighboring countries of Democratic Republic of Congo (DRC) but data on the current prevalence of the disease in the country itself are lacking. This study, focusing on porcine cysticercosis (CC), makes part of a first initiative to assess whether cysticercosis is indeed actually present in DRC.

          Methods

          An epidemiological study on porcine CC was conducted (1) on urban markets of Kinshasa where pork is sold and (2) in villages in Bas-Congo province where pigs are traditionally reared. Tongue inspection and ELISA for the detection of circulating antigen of the larval stage of T. solium were used to assess the prevalence of active CC in both study sites.

          Findings

          The overall prevalence of pigs with active cysticercosis did not significantly differ between the market and the village study sites (38.8 [CI95%: 34–43] versus 41.2% [CI95%: 33–49], respectively). However, tongue cysticercosis was only found in the village study site together with a significantly higher intensity of infection (detected by ELISA).

          Interpretation

          Pigs reared at village level are sold for consumption on Kinshasa markets, but it seems that highly infected animals are excluded at a certain level in the pig trade chain. Indeed, preliminary informal surveys on common practices conducted in parallel revealed that pig farmers and/or buyers select the low infected animals and exclude those who are positive by tongue inspection at village level. This study provides the only recent evidence of CC presence in DRC and gives the first estimates to fill an important gap on the African taeniasis/cysticercosis distribution map.

          Author Summary

          Taenia solium is a parasite that can affect both humans and pigs, causing important economic losses in pig production and being the main cause of acquired epilepsy in endemic areas. However, the parasite has been neglected in many African countries and particularly in the Democratic Republic of Congo (DRC), where recent data are non-existent. The present study is part of a first initiative to assess whether cysticercosis is actually present in DRC and to estimate its potential economic and public health importance. Focusing our work on porcine cysticercosis, we demonstrated high prevalence figures of active infections in villages in a rural area of DRC and in markets in the city of Kinshasa. Moreover, the intensity of infection was higher in pigs sampled in villages as compared to pigs sampled on urban markets. Preliminary surveys conducted in parallel in both study sites suggest an effect of pork trade on the transmission of the parasite selecting highly infected pigs at village level.

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          Most cited references19

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          Incorporating a Rapid-Impact Package for Neglected Tropical Diseases with Programs for HIV/AIDS, Tuberculosis, and Malaria

          Hotez et al. argue that achieving success in the global fight against HIV/AIDS, tuberculosis, and malaria may well require a concurrent attack on the neglected tropical diseases.
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            A Bayesian approach for estimating values for prevalence and diagnostic test characteristics of porcine cysticercosis.

            Several diagnostic techniques are used to estimate the prevalence of the zoonotic tapeworm Taenia solium in pigs, but none of these tests are perfect, making interpretation of results difficult. A Bayesian approach was used to estimate values for the prevalence and diagnostic test characteristic of porcine cysticercosis by combining results of four imperfect tests. Village pigs (N = 868) slaughtered in Lusaka (Zambia), were bled, and tongue and routine meat inspected; and serum antibody and parasite antigen concentrations were determined by ELISA. A model, based on a multinomial distribution and including all possible interactions between the individual tests required 31 parameters to be estimated, but actually allowed only 15 parameters (i.e. had 15 degrees of freedom) to be estimated. Therefore, prior expert opinion on specificity and (in)-dependence of the tests was entered in the model, resulting in a reduction of the number of parameters to be estimated. The estimated prevalence of porcine cysticercosis was 0.642 (95% confidence interval 0.54-0.91). The performances of the tests were (sensitivity (se)-specificity (sp)): tongue inspection (se 0.210-sp 1.000), meat inspection (se 0.221-sp 1.000), Ab-ELISA (se 0.358-sp 0.917), Ag-ELISA (se 0.867-sp 0.947). To validate the estimates obtained from the model we performed a second study: 65 randomly purchased Zambian village pigs were bled for serum antibody and antigen determination, their tongue and meat inspected; and in addition, the carcasses were dissected for total cysticercus counts (gold standard). Cysticerci were found in 31 pigs (prevalence 0.477, 95% confidence interval 0.35-0.60), overlapping with the estimated prevalence in the first study. Sensitivity and specificity values obtained for the aforementioned tests in this study were in agreement with those estimated. A Bayesian analysis framework offers the possibility to combine prior opinion with experimental data to more accurately estimate the real prevalence of porcine cysticercosis in the absence of a gold standard.
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              The emergence of Taenia solium cysticercosis in Eastern and Southern Africa as a serious agricultural problem and public health risk.

              Pig production has increased significantly in the Eastern and Southern Africa (ESA) region during the past decade, especially in rural, resource-poor, smallholder communities. Concurrent with the increase in smallholder pig keeping and pork consumption, there have been increasing reports of porcine cysticercosis in the ESA region. This article reviews the findings concerning the presence and impact of porcine cysticercosis in seven of the ESA countries. Most of the reported findings are based on surveys utilising lingual palpation and post-mortem examination, however, some also used serological assays. In Tanzania, community-based studies on porcine cysticercosis indicate a prevalence of 17.4% in the northern highlands district of Mbulu and a prevalence range of 5.1-16.9% in the southern highlands. In Kenya recent surveys in the southwestern part of the country where smallholder pig keeping is popular indicate that 10-14% of pigs are positive for cysticercosis by lingual examination. Uganda has the most pigs in Eastern Africa, most of which are kept under smallholder conditions. Preliminary surveys in 1998 and 1999 at slaughterhouses in Kampala indicated a prevalence of porcine cysticercosis between 0.12 and 1.2%, however, a rural survey in northern Uganda in 1999 indicated 34-45% of pigs slaughtered in selected villages were infected. Additionally, a new survey of 297 pigs slaughtered in Kampala in 2002 indicated that pigs from the central region of the country were negative for cysticercosis while 33.7% of the pigs coming from the rural Lira district in the north were positive. Interestingly 8 piglet foetuses removed from an infected slaughtered sow coming from Lira district were all found to harbour cysts of T. solium providing evidence of congenital transmission of porcine cysticercosis. In Mozambique, abattoir records indicate that porcine cysticercosis is present in all provinces of the country. A serological survey on pigs in rural Tete Province found 15% of pigs positive. In Zimbabwe, a retrospective study in official abattoirs around the country from 1994 to 2001 reported a mean prevalence of 0.34% which is in contrast to a post-mortem survey in 1999, which showed that the prevalence of porcine cysticercosis in rural west Zimbabwe where smallholder pig keeping is popular was 28.6%. In Zambia, abattoir records reported porcine cysticercosis in six of the nine provinces. Routine meat inspection of 1316 pigs at a slaughter slab in Lusaka showed that 20.6% of the pigs had cysticercosis whereas serological testing of 874 pigs at the same abattoir indicated that 56.6% were found to have circulating antigens of Taenia solium. Field surveys based on lingual palpation in Southern and Eastern Provinces of Zambia revealed prevalences of 8.2-28.4 and 5.2%, respectively. South Africa has the largest number of pigs in Southern Africa and cysticercosis has been recognised as a problem in the country for many decades. There is strong evidence supporting the high prevalence of neurocysticercosis infecting humans from resource-poor areas of the country where pigs are being raised under smallholder conditions. In spite of this community-based surveys on porcine cysticercosis have never been conducted in South Africa and the last slaughterhouse survey was conducted nearly 40 years ago. The prevalences of porcine cysticercosis found in these ESA countries rank among the highest in the world and the disease is emerging as an important constraint for the nutritional and economic well being of resource-poor smallholder farming communities. The current findings suggest the widespread presence of human tapeworm carriers and thus a high risk of human cysticercosis in both rural areas and urban centres in the ESA region. More research is required in the region to assess the extent and public health and economic impact of T. solium infection in order to determine whether and what prevention and control efforts are needed.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, USA )
                1935-2727
                1935-2735
                September 2010
                7 September 2010
                : 4
                : 9
                : e817
                Affiliations
                [1 ]Institute of Tropical Medicine, Antwerp, Belgium
                [2 ]Department of Infectious and Parasitic Diseases, Research Unit of Epidemiology and Risk Analysis Applied to Veterinary Sciences, Faculty of Veterinary Medicine, University of Liege, Liege, Belgium
                [3 ]Institut National de Recherche Biomédicale, Kinshasa, Democratic Republic of Congo
                [4 ]Tropical Medicine Department, Kinshasa University, Kinshasa, Democratic Republic of Congo
                [5 ]Kimpese Health Zone, Kimpese, Democratic Republic of Congo
                [6 ]Laboratoire Vétérinaire de Kinshasa, Kinshasa, Democratic Republic of Congo
                [7 ]Institute of Health and Society, Université Catholique de Louvain, Brussels, Belgium
                Universidad Peruana Cayetano Heredia, Peru
                Author notes

                Conceived and designed the experiments: N. Praet, K. Kanobana, P. Lutumba, K. Polman, P. Dorny, J. Sumbu. Performed the experiments: N. Praet, K. Kanobana, C. Kabwe, V. Maketa, P. Lukanu, P. Lutumba, P. Matondo, J. Sumbu. Analyzed the data: N. Praet, K. Kanobana, N. Speybroeck. Wrote the paper: N. Praet, K. Kanobana.

                Article
                10-PNTD-RA-1034R3
                10.1371/journal.pntd.0000817
                2935392
                20838646
                ba1a0abf-15aa-40e3-a2d2-04987bdcfbfc
                Praet et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 2 April 2010
                : 11 August 2010
                Page count
                Pages: 6
                Categories
                Research Article
                Infectious Diseases/Neglected Tropical Diseases
                Public Health and Epidemiology

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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