Study and Ranking of Determinants of Taenia solium Infections by Classification Tree Models

Kabemba E. Mwape Department of Clinical Studies, School of Veterinary Medicine, University of Zambia, Lusaka, Zambia; Department of Veterinary Tropical Diseases, Faculty of Veterinary Sciences, University of Pretoria, Pretoria, South Africa; Department of Biomedical Sciences, Institute of Tropical Medicine, Antwerp, Belgium; Laboratory of Veterinary Parasitology, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium; Department of Disease Control, School of Veterinary Medicine, University of Zambia, Zambia; Petauke District Hospital, Petauke, Zambia; Institute of Health and Society, Université Catholique de Louvain, Brussels, Belgium

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Isaac K. Phiri Department of Clinical Studies, School of Veterinary Medicine, University of Zambia, Lusaka, Zambia; Department of Veterinary Tropical Diseases, Faculty of Veterinary Sciences, University of Pretoria, Pretoria, South Africa; Department of Biomedical Sciences, Institute of Tropical Medicine, Antwerp, Belgium; Laboratory of Veterinary Parasitology, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium; Department of Disease Control, School of Veterinary Medicine, University of Zambia, Zambia; Petauke District Hospital, Petauke, Zambia; Institute of Health and Society, Université Catholique de Louvain, Brussels, Belgium

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Nicolas Praet Department of Clinical Studies, School of Veterinary Medicine, University of Zambia, Lusaka, Zambia; Department of Veterinary Tropical Diseases, Faculty of Veterinary Sciences, University of Pretoria, Pretoria, South Africa; Department of Biomedical Sciences, Institute of Tropical Medicine, Antwerp, Belgium; Laboratory of Veterinary Parasitology, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium; Department of Disease Control, School of Veterinary Medicine, University of Zambia, Zambia; Petauke District Hospital, Petauke, Zambia; Institute of Health and Society, Université Catholique de Louvain, Brussels, Belgium

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Pierre Dorny Department of Clinical Studies, School of Veterinary Medicine, University of Zambia, Lusaka, Zambia; Department of Veterinary Tropical Diseases, Faculty of Veterinary Sciences, University of Pretoria, Pretoria, South Africa; Department of Biomedical Sciences, Institute of Tropical Medicine, Antwerp, Belgium; Laboratory of Veterinary Parasitology, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium; Department of Disease Control, School of Veterinary Medicine, University of Zambia, Zambia; Petauke District Hospital, Petauke, Zambia; Institute of Health and Society, Université Catholique de Louvain, Brussels, Belgium

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John B. Muma Department of Clinical Studies, School of Veterinary Medicine, University of Zambia, Lusaka, Zambia; Department of Veterinary Tropical Diseases, Faculty of Veterinary Sciences, University of Pretoria, Pretoria, South Africa; Department of Biomedical Sciences, Institute of Tropical Medicine, Antwerp, Belgium; Laboratory of Veterinary Parasitology, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium; Department of Disease Control, School of Veterinary Medicine, University of Zambia, Zambia; Petauke District Hospital, Petauke, Zambia; Institute of Health and Society, Université Catholique de Louvain, Brussels, Belgium

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Gideon Zulu Department of Clinical Studies, School of Veterinary Medicine, University of Zambia, Lusaka, Zambia; Department of Veterinary Tropical Diseases, Faculty of Veterinary Sciences, University of Pretoria, Pretoria, South Africa; Department of Biomedical Sciences, Institute of Tropical Medicine, Antwerp, Belgium; Laboratory of Veterinary Parasitology, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium; Department of Disease Control, School of Veterinary Medicine, University of Zambia, Zambia; Petauke District Hospital, Petauke, Zambia; Institute of Health and Society, Université Catholique de Louvain, Brussels, Belgium

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Niko Speybroeck Department of Clinical Studies, School of Veterinary Medicine, University of Zambia, Lusaka, Zambia; Department of Veterinary Tropical Diseases, Faculty of Veterinary Sciences, University of Pretoria, Pretoria, South Africa; Department of Biomedical Sciences, Institute of Tropical Medicine, Antwerp, Belgium; Laboratory of Veterinary Parasitology, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium; Department of Disease Control, School of Veterinary Medicine, University of Zambia, Zambia; Petauke District Hospital, Petauke, Zambia; Institute of Health and Society, Université Catholique de Louvain, Brussels, Belgium

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Sarah Gabriël Department of Clinical Studies, School of Veterinary Medicine, University of Zambia, Lusaka, Zambia; Department of Veterinary Tropical Diseases, Faculty of Veterinary Sciences, University of Pretoria, Pretoria, South Africa; Department of Biomedical Sciences, Institute of Tropical Medicine, Antwerp, Belgium; Laboratory of Veterinary Parasitology, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium; Department of Disease Control, School of Veterinary Medicine, University of Zambia, Zambia; Petauke District Hospital, Petauke, Zambia; Institute of Health and Society, Université Catholique de Louvain, Brussels, Belgium

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Taenia solium taeniasis/cysticercosis is an important public health problem occurring mainly in developing countries. This work aimed to study the determinants of human T. solium infections in the Eastern province of Zambia and rank them in order of importance. A household (HH)-level questionnaire was administered to 680 HHs from 53 villages in two rural districts and the taeniasis and cysticercosis status determined. A classification tree model (CART) was used to define the relative importance and interactions between different predictor variables in their effect on taeniasis and cysticercosis. The Katete study area had a significantly higher taeniasis and cysticercosis prevalence than the Petauke area. The CART analysis for Katete showed that the most important determinant for cysticercosis infections was the number of HH inhabitants (6 to 10) and for taeniasis was the number of HH inhabitants > 6. The most important determinant in Petauke for cysticercosis was the age of head of household > 32 years and for taeniasis it was age < 55 years. The CART analysis showed that the most important determinant for both taeniasis and cysticercosis infections was the number of HH inhabitants (6 to 10) in Katete district and age in Petauke. The results suggest that control measures should target HHs with a high number of inhabitants and older individuals.

Author Notes

* Address correspondence to Sarah Gabriël, Department of Biomedical Sciences, Institute of Tropical Medicine, Nationalestraat 155, B-2000 Antwerp, Belgium. E-mail: sgabriel@itg.be
† These authors contributed equally to the scientific and the conceptual work of the manuscript.

Financial support: This work was funded by the Flemish Inter University Council, Research Initiative Programme, Zambia (VLIR-UOS.ZIUS2008RIP-8961), with the Belgian Directorate for Development Co-operation through the 3rd framework agreement with ITM, and by the EU grant ADVANZ-Advocacy for the fight against Neglected Zoonotic Diseases (FP7 KBBE contract no: 0312030, http://www.advanz.org).

Authors' addresses: Kabemba E. Mwape and Isaac K. Phiri, Department of Clinical Studies, School of Veterinary Medicine, University of Zambia, E-mails: evans.mwape@unza.zm and igphiri@yahoo.co.uk. Nicolas Praet and Sarah Gabriël, Department of Biomedical Sciences, Institute of Tropical Medicine, Antwerp, Belgium, E-mails: npraet@itg.be and sgabriel@itg.be. Pierre Dorny, Department of Biomedical Sciences, Institute of Tropical Medicine Antwerp, Belgium; Laboratory of Veterinary Parasitology, Faculty of Veterinary Medicine, Ghent University, Belgium, E-mail: pdorny@itg.be. John B. Muma, Department of Disease Control, School of Veterinary Medicine, University of Zambia, E-mail: jmuma@unza.zm. Gideon Zulu, Petauke District Hospital, Petauke, Zambia, E-mail: gideonzulu@yahoo.com. Niko Speybroeck, Institute of Health and Society, Université Catholique de Louvain, Belgium, E-mail: Niko.Speybroeck@uclouvain.be.

  • 1.

    Garcia HH, Del Brutto OH, Nash TE, White AC Jr, Tsang VC, Gilman RH, 2005. New concepts in the diagnosis and management of neurocysticercosis (Taenia solium). Am J Trop Med Hyg 72: 39.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2.

    Roman G, Sotelo J, Del Brutto O, Flisser A, Dumas M, Wadia N, Botero D, Cruz M, Garcia H, de Bittencourt PR, Trelles L, Arriagada C, Lorenzana P, Nash TE, Spina-França A, 2000. A proposal to declare neurocysticercosis an international reportable disease. Bull World Health Organ 78: 399406.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3.

    Mayta H, Gilman RH, Prendergast E, Castillo JP, Tinoco YO, Garcia HH, Gonzalez AE, Sterling CR; Cysticercosis Working Group in Peru, 2008. Nested PCR for specific diagnosis of Taenia solium taeniasis. J Clin Microbiol 46: 286289.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    Ngowi HA, Kassuku AA, Carabin H, Mlangwa JE, Mlozi MR, Mbilinyi BP, Willingham AL 3rd, 2010. Spatial clustering of porcine cysticercosis in Mbulu district, northern Tanzania. PLoS Negl Trop Dis 4: e652.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    Phiri IK, Ngowi H, Afonso S, Matenga E, Boa M, Mukaratirwa S, Githigia S, Saimo M, Sikasunge C, Maingi N, Lubega GW, Kassuku A, Michael L, Siziya S, Krecek RC, Noormahomed E, Vilhena M, Dorny P, Willingham AL 3rd, 2003. The emergence of Taenia solium cysticercosis in eastern and southern Africa as a serious agricultural problem and public health risk. Acta Trop 87: 1323.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6.

    Sikasunge CS, Phiri IK, Phiri AM, Dorny P, Siziya S, Willingham AL 3rd, 2007. Risk factors associated with porcine cysticercosis in selected districts of eastern and southern provinces of Zambia. Vet Parasitol 143: 5966.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7.

    Mwanjali G, Kihamia C, Kakoko DV, Lekule F, Ngowi H, Johansen AV, Thamsborg SM, Willingham AL 3rd, 2013. Prevalence and risk factors associated with human Taenia solium infections in Mbozi District, Mbeya Region, Tanzania. PLoS Negl Trop Dis 7: e2102.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8.

    Murrell KD, 2005. WHO/OIE/FAO Guidelines for the Surveillance, Prevention and Control of Taeniasis/Cysticercosis. Murrell KD, ed. Paris, France: World Health Organization for Animal Health (OIE), 5771.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    Praet N, Verweij JJ, Mwape KE, Phiri IK, Muma JB, Zulu G, van Lieshout L, Rodriguez-Hidalgo R, Benitez-Ortiz W, Dorny P, Gabriel S, 2013. Bayesian modeling to estimate the test characteristics of coprology, coproantigen ELISA and a novel real-time PCR for the diagnosis of taeniasis. Trop Med Int Health 18: 608614.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Thang ND, Erhart A, Speybroeck N, Hung le X, Thuan le K, Hung CT, Ky PV, Coosemans M, D'Alessandro U, 2008. Malaria in central Vietnam: analysis of risk factors by multivariate analysis and classification tree models. Malar J 7: 28.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Bhattarai NR, Van Der Auwera G, Rijal S, Picado A, Speybroeck N, Khanal B, De Doncker S, Das ML, Ostyn B, Davies C, Coosemans M, Berkvens D, Boelaert M, Dujardin JC, 2010. Domestic animals and epidemiology of visceral leishmaniasis, Nepal. Emerg Infect Dis 16: 231237.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Protopopoff N, Van Bortel W, Speybroeck N, Van Geertruyden JP, Baza D, D'Alessandro U, Coosemans M, 2009. Ranking malaria risk factors to guide malaria control efforts in African highlands. PLoS ONE 4: e8022.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Yewhalaw D, Legesse W, Van Bortel W, Gebre-Selassie S, Kloos H, Duchateau L, Speybroeck N, 2009. Malaria and water resource development: the case of Gilgel-Gibe hydroelectric dam in Ethiopia. Malar J 8: 21.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Sikasunge CS, Phiri IK, Phiri AM, Siziya S, Dorny P, Willingham AL 3rd, 2008. Prevalence of Taenia solium porcine cysticercosis in the eastern, southern and western provinces of Zambia. Vet J 176: 240244.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Mwape KE, Phiri IK, Praet N, Muma JB, Zulu G, Van den Bossche P, de Deken R, Speybroeck N, Dorny P, Gabriël S, 2012. Taenia solium infections in a rural area of eastern Zambia—a community based study. PLoS Negl Trop Dis 6: 1594.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16.

    Mwape KE, Phiri IK, Praet N, Speybroeck N, Muma JB, Dorny P, Gabriel S, 2013. The incidence of human cysticercosis in a rural community of eastern Zambia. PLoS Negl Trop Dis 7: 2142.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17.

    Dorny P, Brandt J, Geerts S, 2004. Immunodiagnostic approaches for detecting Taenia solium. Trends Parasitol 20: 259260; author reply 260–251.

  • 18.

    Ritchie LS, 1948. An ether sedimentation technique for routine stool examinations. Bull US Army Med Dep 8: 326.

  • 19.

    Allan JC, Avila G, Garcia Noval J, Flisser A, Craig PS, 1990. Immunodiagnosis of taeniasis by coproantigen detection. Parasitol 101: 473477.

  • 20.

    Speybroeck N, 2012. Classification and regression trees. Int J Public Health 57: 243246.

  • 21.

    Suman P, Thys E, Mfoukou-Ntsakala A, Ali L, Ouedraogo M, Van den Bossche P, Van Huylenbroeck G, Berkvens D, Speybroeck N, 2010. Methodology for assessing determinants of manure use in urban areas of Africa. Waste Manag Res 28: 10761086.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22.

    Praet N, Speybroeck N, Rodriguez-Hidalgo R, Benitez-Ortiz W, Berkvens D, Brandt J, Saegerman C, Dorny P, 2010. Age-related infection and transmission patterns of human cysticercosis. Int J Parasitol 40: 8590.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    Garcia HH, Del Brutto OH, 1999. Heavy nonencephalitic cerebral cysticercosis in tapeworm carriers. The Cysticercosis Working Group in Peru. Neurology 53: 15821584.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24.

    Schantz PM, Moore AC, Munoz JL, Hartman BJ, Schaefer JA, Aron AM, Persaud D, Sarti E, Wilson M, Flisser A, 1992. Neurocysticercosis in an Orthodox Jewish community in New York City. N Engl J Med 327: 692695.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25.

    Garcia HH, Gilman RH, Gonzalez AE, Verastegui M, Rodriguez S, Gavidia C, Tsang VC, Falcon N, Lescano AG, Moulton LH, Bernal T, Tovar M; Cysticercosis Working Group in Perú, 2003. Hyperendemic human and porcine Taenia solium infection in Peru. Am J Trop Med Hyg 68: 268275.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    Sanchez AL, Gomez O, Allebeck P, Cosenza H, Ljungstrom L, 1997. Epidemiological study of Taenia solium infections in a rural village in Honduras. Ann Trop Med Parasitol 91: 163171.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27.

    Sarti E, 1997. Taeniasis and cysticercosis due to Taenia solium. Salud Publica Mex 39: 225231.

  • 28.

    Allan JC, Velasquez-Tohom M, Fletes C, Torres-Alvarez R, Lopez-Virula G, Yurrita P, Soto de Alfaro H, Rivera A, Garcia-Noval J, 1997. Mass chemotherapy for intestinal Taenia solium infection: effect on prevalence in humans and pigs. Trans R Soc Trop Med Hyg 91: 595598.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29.

    Diaz Camacho SP, Candil Ruiz A, Suate Peraza V, Zazueta Ramos ML, Felix Medina M, Lozano R, Willms K, 1991. Epidemiologic study and control of Taenia solium infections with praziquantel in a rural village of Mexico. Am J Trop Med Hyg 45: 522531.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    Sarti E, Schantz PM, Avila G, Ambriosio J, Medina-Santillan R, Flisser A, 2000. Mass treatment against human taeniasis for the control of cysticercosis: a population-based intervention study. Trans R Soc Trop Med Hyg 94: 8589.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31.

    Chung WC, Fan PC, Lin CY, Wu CC, 1991. Poor efficacy of albendazole for the treatment of human taeniasis. Int J Parasitol 21: 269270.

  • 32.

    Steinmann P, Zhou XN, Du ZW, Jiang JY, Xiao SH, Wu ZX, Zhou H, Utzinger J, 2008. Tribendimidine and albendazole for treating soil-transmitted helminths, Strongyloides stercoralis and Taenia spp.: open-label randomized trial. PLoS Negl Trop Dis 2: e322.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33.

    Kagira JM, Maingi N, Kanyari PW, Githigia SM, Ng'ang'a JC, Gachohi JM, 2010. Seroprevalence of Cysticercus cellulosae and associated risk factors in free-range pigs in Kenya. J Helminthol 84: 398403.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34.

    Ngowi HA, Kassuku AA, Maeda GE, Boa ME, Carabin H, Willingham AL 3rd, 2004. Risk factors for the prevalence of porcine cysticercosis in Mbulu District, Tanzania. Vet Parasitol 120: 275283.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35.

    Rodriguez-Canul R, Fraser A, Allan JC, Dominguez-Alpizar JL, Argaez-Rodriquez F, Craig PS, 1999. Epidemiological study of Taenia solium taeniasis/cysticercosis in a rural Village in Yucatan State, Mexico. Ann Trop Med Parasitol 93: 5767.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36.

    Diaz Camacho S, Candil Ruiz A, Uribe Beltran M, Willms K, 1990. Serology as an indicator of Taenia solium tapeworm infections in a rural community in Mexico. Trans R Soc Trop Med Hyg 84: 563566.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37.

    Lescano AG, Garcia HH, Gilman RH, Gavidia CM, Tsang VC, Rodriguez S, Moulton LH, Villaran MV, Montano SM, Gonzalez AE; Cysticercosis Working Group in Peru, 2009. Taenia solium cysticercosis hotspots surrounding tapeworm carriers: clustering on human seroprevalence but not on seizures. PLoS Negl Trop Dis 3: e371.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38.

    Ndimubanzi PC, Carabin H, Budke CM, Nguyen H, Qian YJ, Rainwater E, Dickey M, Reynolds S, Stoner JA, 2010. A systematic review of the frequency of neurocysticercosis with a focus on people with epilepsy. PLoS Negl Trop Dis 4: e870.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39.

    Mwape KE, Praet N, Benitez-Ortiz W, Muma JB, Zulu G, Celi-Erazoc M, Phiri IK, Rodriguez-Hidalgo R, Dorny P, Gabriël S, 2011. Field evaluation of urine antigen detection for diagnosis of Taenia solium cysticercosis. Trans R Soc Trop Med Hyg 105: 574578.

    • PubMed
    • Search Google Scholar
    • Export Citation
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