Piloting the effectiveness of pig health education in combination with oxfendazole treatment on prevention and/or control of porcine cysticercosis, gastrointestinal parasites, African swine fever and ectoparasites in Angónia District, Mozambique

Tropical Animal Health and Production volume 50, pages589–601(2018)Cite this article

Abstract

A community-based intervention combining health education (HE) and treatment of pigs for control of porcine cysticercosis (PC), gastrointestinal (GI) helminths, African swine fever (ASF) and external parasites was tested involving six villages of resource-poor smallholder pig farmers. Farmers and pigs of six rural villages were randomly allocated into group 1 (HE), which served as controls, and group 2 (HE + OFZ) pigs received a single oral dose of 30 mg/kg OFZ. Farmers were trained in pig health, housing and feeding. The proportion of farmers with confined pigs, the adoption rate of the introduced pig pen, the sero-prevalence of PC and ASF, the prevalence and intensity of GI nematodes and the prevalence of ectoparasites were measured at 9, 15 and 24 months after initiation and compared to a baseline survey to seek the effectiveness of the interventions. There was no clear effect of the intervention on the sero-prevalence of PC, but analysis of the rate of change in prevalence between the two groups showed significant effect with the rate of change to lower prevalence in the HE + OFZ group compared to the HE group. Although HE managed to improve the farmer’s knowledge in the control and prevention of ASF and ectoparasites, there was no significant reduction in the sero-prevalence of ASF and the prevalence of ectoparasites throughout the two-year period. The reported ineffectiveness of the intervention in this study suggested that more research is needed to develop more effective methods for controlling PC, ASF and pig parasites.

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Fig. 1

Abbreviations

ASF:

African swine fever

Ag:

antigen

CI:

confidence interval

FECs:

fecal egg counts

g:

gram

GI:

gastrointestinal

HE:

health education

OFZ:

oxfendazole

PC:

porcine cysticercosis

PI:

principal investigator

References

  1. Afonso S. M. S., Neves L., Afonso C. M. C., Nota A., Vilhena M. & Ito A. 2001. Cysticercus cellulosa in Tete Province, Mozambique. Lusaka, Zambia, 32.

  2. Afonso S. M. S., Vaz Y., Neves L., Pondja A., Dias G., Willingham A. L., Vilhena M., Duarte P. C., Jost C. C. & Noormahomed E. V. 2011. Human and porcine Taenia solium infections in Mozambique: identifying research priorities. Anim Health Res Rev 12: 1, 123–129.

    CAS  Article  PubMed  Google Scholar 

  3. Alfredo, Z. L. The effect of education on smallholder pig farmers knowledge, practices, and pig productivity in the Angónia district. 2015. https://researchspace.ukzn.ac.za/xmlui/bitstream/handle/10413/13329/Alfredo_Zeiss_Lacerda_2015.pdf?sequence=1&isAllowed=y, University of KwaZulu-Natal, Pietermaritzburg.

  4. Alvarez L., Saumell C., Fuse L., Moreno L., Ceballos L., Domingue G., Donadeu M., Dungu B. & Lanusse C. 2013. Efficacy of a single high oxfendazole dose against gastrointestinal nematodes in naturally infected pigs. Vet Parasitol 194: 1, 70–74.

    CAS  Article  PubMed  Google Scholar 

  5. Atuhaire D. K., Ochwo S., Afayoa M., Mwiine F. N., Kokas I., Arinaitwe E., Ademun-Okurut R. A., Okuni J. B., Nanteza A., Ayebazibwe C., Okedi L., Olaho-Mukani W. & Ojok L. 2013. Epidemiological overview of African swine Fever in Uganda (2001–2012). Journal of Veterinary Medicine 2013: 949639, e-9.

    Google Scholar 

  6. Awosanya E. J., Olugasa B., Ogundipe G. & Grohn Y. T. 2015. Sero-prevalence and risk factors associated with African swine fever on pig farms in southwest Nigeria. BMC Veterinary Research 11: 1, 133.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Braae U. C., Ngowi H. A. & Johansen M. V. 2013. Smallholder pig production: prevalence and risk factors of ectoparasites. Vet Parasitol 196: 1–2, 241–244.

    CAS  Article  PubMed  Google Scholar 

  8. Braae U. C., Magnussen P., Lekule F. P., Harrison W. & Johansen M. V. 2014. Temporal fluctuations in the sero-prevalence of Taenia solium cysticercosis in pigs in Mbeya Region, Tanzania. Parasit Vectors 7: 574.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Braae U. C., Kabululu M. L., Normark M. E., Nejsum P., Ngowi H. A. & Johansen M. V. 2015. Taenia hydatigena cysticercosis in slaughtered pigs, goats, and sheep in Tanzania. Trop Anim Health Prod 47: 8, 1523–1530.

    Article  PubMed  Google Scholar 

  10. Brandt J. R., Geerts S., De D. R., Kumar V., Ceulemans F., Brijs L. & Falla N. 1992. A monoclonal antibody-based ELISA for the detection of circulating excretory-secretory antigens in Taenia saginata cysticercosis. Int J Parasitol 22: 4, 471–477.

    CAS  Article  PubMed  Google Scholar 

  11. Carabin H. & Traore A. A. 2014. Taenia solium taeniasis and cysticercosis control and elimination through community-based interventions. Curr Trop Med Rep 1: 4, 181–193.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Chattopadhyay A. K. & Bandyopadhyay S. 2013. Seasonal variations of EPG levels in gastro-intestinal parasitic infection in a southeast asian controlled locale: a statistical analysis. Springerplus 2: 205.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Chenais E., Boqvist S., Sternberg-Lewerin S., Emanuelson U., Ouma E. A., Dione M. M., Aliro T., Crafoord F., Masembe C. & Stahl K. 2015. Knowledge, attitudes and practices related to African swine fever within smallholder pig production in Northern Uganda. Transbound Emerg Dis 1–15.

  14. Chilundo A. G., Mukaratirwa S., Pondja A., Afonso S., Miambo R. & Johansen M. V. 2017. Prevalence and risk factors of endo- and ectoparasitic infections in smallholder pigs in Angónia district, Mozambique. Veterinary Parasitology: Regional Studies and Reports 7: 1–8.

    Google Scholar 

  15. Cubillos C., Gomez-Sebastian S., Moreno N., Nunez M. C., Mulumba-Mfumu L. K., Quembo C. J., Heath L., Etter E. M., Jori F., Escribano J. M. & Blanco E. 2013. African swine fever virus serodiagnosis: a general review with a focus on the analyses of African serum samples. Virus Res 173: 1, 159–167.

    CAS  Article  PubMed  Google Scholar 

  16. Dohoo, I., Martin, W., & Stryhn, H. 2003. Veterinary epidemiology research. AVC Inc., Prince Edward Island.

    Google Scholar 

  17. Dorny P., Phiri I. K., Vercruysse J., Gabriël S., Willingham A. L., III, Brandt J., Victor B., Speybroeck N. & Berkvens D. 2004. A Bayesian approach for estimating values for prevalence and diagnostic test characteristics of porcine cysticercosis. Int J Parasitol 34: 5, 569–576.

    CAS  Article  PubMed  Google Scholar 

  18. FAO. Regional strategy for the control of African swine fever in Africa. Empres-animal health 360 44: 2. 2014. http://www.fao.org/3/a-i4257e/a-i4257e03.pdf.

  19. Gallardo, C., Vázquez, B., & Arias, M. Validation study of the INGENASA ASF serological Kit. Competition ELISA INGEZIM PPA Compac (11.PPA K3). 1–11. 2005. Madrid, Spain.

  20. Garcia H. H., Gonzalez A. E., Tsang V. C. W., O'Neal S. E., Llanos-Zavalaga F., Gonzalvez G., Romero J., Rodriguez S., Moyano L. M., Ayvar V., Diaz A., Hightower A., Craig P. S., Lightowlers M. W., Gauci C. G., Leontsini E. & Gilman R. H. 2016. Elimination of Taenia solium Transmission in Northern Peru. N Engl J Med 374: 24, 2335–2344.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Gonzalez A. E., Falcon N., Gavidia C., Garcia H. H., Tsang V. C. W., Bernal T., Romero M. & Gilman R. H. 1997. Treatment of porcine cysticercosis with oxfendazole: a dose-response trial. Vet Rec 141: 16, 420.

    CAS  Article  PubMed  Google Scholar 

  22. Gonzalez A. E., Gavidia C., Falcon N., Bernal T., Verastegui M., Garcia H. H., Gilman R. H. & Tsang V. C. 2001. Protection of pigs with cysticercosis from further infections after treatment with oxfendazole. Am J Trop Med Hyg 65: 1, 15–18.

    CAS  Article  PubMed  Google Scholar 

  23. Goussanou J. S. E., Korsak K., Saegerman C., Youssao A. K. I., Azagoun E., Farougou S., Gabriël S., Dorny P. & Kpodekon M. T. 2014. Assessment of rotine inspection method for diagnostic of porcine cysticercosis in South East Benin by using inspection records and Ag-ELISA test. Int J Anim Veter Adv 6: 2, 80–86.

    Google Scholar 

  24. INE. III—Recenseamento geral da população e habitação: Indicadores socio-demográficos distritais—Província de Tete. 2010. http://www.tete.gov.mz/informacao/estatistica/resultados_censo_2007.pdf, Instituto Nacional de Estatística.

  25. Jufare A., Awol N., Tadesse F., Tsegaye Y. & Hadush B. 2015. Parasites of pigs in two farms with poor husbandry practices in Bishoftu, Ethiopia. Onderstepoort Journal of Veterinary Research 82: 1, 839.

    Article  PubMed  Google Scholar 

  26. Kabululu M. L., Ngowi H. A., Kimera S. I., Lekule F. P., Kimbi E. C. & Johansen M. V. 2015. Risk factors for prevalence of pig parasitoses in Mbeya Region, Tanzania. Vet Parasitol.

  27. Kagira J. M., Kanyari P. N., Maingi N., Githigia S. M., Ng'ang'a J. C. & Gachohi J. M. 2013. Relationship between the prevalence of ectoparasites and associated risk factors in free-range pigs in Kenya. ISRN Vet Sci 2013: 650890.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Kambarage, D. M., Karimuribo, E. D., Kusiluka, L. J. M., Mdegela, R. H., & Kazwala, R. R. Community health education in Tanzania: challenges, opportunities and the way forward in expert consultation on community based veterinary public health (VPH) systems. 2003. ftp://ftp.fao.org/docrep/fao/007/y5405e/y5405e04.pdf, FAO, Rome, Italy.

    Google Scholar 

  29. Kaufmann, J. 1996. Parasitic infections of domestic animals: A diagnostic manual. Birkhäuser, Basel, Boston, Berlin.

  30. Kumsa B. & Kifle E. 2014. Internal parasites and health management of pigs in Burayu District, Oromia Regional State, Ethiopia. J S Afr Vet Assoc 85: 1, 913.

    Article  PubMed  Google Scholar 

  31. Lekule F. P. & Kyvsgaard N. C. 2003. Improving pig husbandry in tropical resource-poor communities and its potential to reduce risk of porcine cysticercosis. Acta Trop 87: 1, 111–117.

    Article  PubMed  Google Scholar 

  32. Lightowlers M. W. 2013. Control of Taenia solium taeniasis/cysticercosis: past practices and new possibilities. Parasitology 140: 13, 1566–1577.

    CAS  Article  PubMed  Google Scholar 

  33. Lightowlers M. W. & Donadeu M. 2017. Designing a minimal intervention strategy to control Taenia solium. Trends in Parasitology.

  34. Lightowlers M. W., Assana E., Jayashi C. M., Gauci C. G. & Donadeu M. 2015. Sensitivity of partial carcass dissection for assessment of porcine cysticercosis at necropsy. Int J Parasitol 45: 13, 815–818.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  35. Marufu M. C., Chanayiwa P., Chimonyo M. & Bhebhe E. 2008. Prevalence of gastrointestinal nematodes in Mukota pigs in a communal area of Zimbabwe. Afr J Agric Res 3: 2, 91–95.

    Google Scholar 

  36. Matos C., Sitoe C., Afonso S. M. S., Banze J., Baptista J., Dias G., Rodrigues F., Atanasio A., Nhamusso A., Penrith M. L. & Willingham A. L., III. 2011. A pilot study of common health problems in smallholder pigs in Angónia and Boane districts, Mozambique. J S Afr Vet Assoc 82: 3, 166–169.

    CAS  Article  PubMed  Google Scholar 

  37. Ministério de Administração Estatal. Perfil do Distrito de Angónia. 2005, 1–63. 2005. www.portaldogoverno.gov.mz/por/content/.../1/.../Angonia.pdf.

  38. Mkupasi E. M., Ngowi H. A., Sikasunge C. S., Leifsson P. S. & Johansen M. V. 2013a. Efficacy of ivermectin and oxfendazole against Taenia solium cysticercosis and other parasitoses in naturally infected pigs. Acta Trop 128: 1, 48–53.

    CAS  Article  PubMed  Google Scholar 

  39. Mkupasi E. M., Sikasunge C. S., Ngowi H. A. & Johansen M. V. 2013b. Efficacy and safety of anthelmintics tested against Taenia solium cysticercosis in pigs. PLoS Negl Trop Dis 7: 7, e2200.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  40. Mwangi, J. N., Abou-Sabaa, A., Balayah, M., Umar, L., Agboma, P., & Soliman, W. Mozambique family farming income enhancement project—appraisal report. 9–10. 2000. http://www.afdb.org, African Development Fund.

  41. Ngowi H. A., Kassuku A. A., Maeda G. E., Boa M. E., Carabin H. & Willingham A. L., III. 2004. Risk factors for the prevalence of porcine cysticercosis in Mbulu District, Tanzania. Vet Parasitol 120: 4, 275–283.

    CAS  Article  PubMed  Google Scholar 

  42. Ngowi H. A., Carabin H., Kassuku A. A., Mlozi M. R., Mlangwa J. E. & Willingham A. L., III. 2008. A health-education intervention trial to reduce porcine cysticercosis in Mbulu District, Tanzania. Prev Vet Med 85: 1–2, 52–67.

    CAS  Article  PubMed  Google Scholar 

  43. Ngowi H. A., Mkupasi E. M., Lekule F. P., Willingham III A. L. & Thamsborg S. M. 2011. Impact of farmer education on their knowledge, attitudes, and practices in Southern Tanzania: a case for Taenia solium control. Livestock Research for Rural Development 23: 1.

    Google Scholar 

  44. Nsoso S. J., Mosala K. P., Ndebele R. T. & Ramabu S. S. 2000. The prevalence of internal and external parasites in pigs of different ages and sexes in Southeast District, Botswana. Onderstepoort Journal of Veterinary Research 67: 3, 217–220.

    CAS  PubMed  Google Scholar 

  45. Odo, G. E., Agwu, E. J., Ossai, N. I. K., Ezea, C. O., Nwokolo, E. C., & Eneje, V. A survey of ectoparasites of local pigs, Sus scrofa domesticus at Emene Town area in Enugu State. Academia Journal of Biotechnology 4: 4, 126–137. 2016.

    Google Scholar 

  46. OIE. African swine fever. Manual of diagnostic tests and vaccines for terrestrial animals. 2012. http://www.oie.int/fileadmin/Home/eng/Health_standards/tahm/2.08.01_ASF.pdf , World organization for animal health.

  47. Ortiz P., Terrones S., Cabrera M., Hoban C., Ceballos L., Moreno L., Canton C., Donadeu M., Lanusse C. & Alvarez L. 2014. Oxfendazole flukicidal activity in pigs. Acta Tropica 136: 10–13.

    CAS  Article  PubMed  Google Scholar 

  48. Ouma E., Dione M. M., Lule P., Rosel K. & Pezo D. 2013. Characterization of smallholder pig production systems in Uganda: constraints and opportunities for engaging with market systems.http://ageconsearch.umn.edu/bitstream/160677/2/Emily%20Ouma%20,%20Michel%20Dione%20et%20al.pdf,

  49. Penrith M. L., Thomson G. R., Bastos A. D., Phiri O. C., Lubisi B. A., Du Plessis E. C., Macome F., Pinto F., Botha B. & Esterhuysen J. 2004. An investigation into natural resistance to African swine fever in domestic pigs from an endemic area in southern Africa. Rev Sci Tech 23: 3, 965–977.

    CAS  Article  PubMed  Google Scholar 

  50. Penrith M. L., Lopes P. C., Lopes da Silva M. M., Quembo C. J., Nhamusso A. & Banze J. 2007. African swine fever in Mozambique: review, risk factors and considerations for control. Onderstepoort Journal of Veterinary Research 74: 2, 149–160.

    CAS  PubMed  Google Scholar 

  51. Pondja A., Neves L., Mlangwa J. E., Afonso S. M. S., Fafetine J., Willingham A. L., III, Thamsborg S. M. & Johansen M. V. 2010. Prevalence and risk factors of porcine cysticercosis in Angónia District, Mozambique. PLoS Negl Trop Dis 4: 2, e594.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Pondja A., Neves L., Mlangwa J. E., Afonso S. M. S., Fafetine J., Willingham A. L., III, Thamsborg S. M. & Johansen M. V. 2012. Use of oxfendazole to control porcine cysticercosis in a high-endemic area of Mozambique. PLoS Negl Trop Dis 6: 5, e1651.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  53. Rodriguez-Canul R., Argaez-Rodriguez F., de, I, Villegas-Perez S., Fraser A., Craig P. S., Cob-Galera L. & Dominguez-Alpizar J. L. 2002. Taenia solium metacestode viability in infected pork after preparation with salt pickling or cooking methods common in Yucatan, Mexico. J Food Prot 65: 4, 666–669.

    CAS  Article  PubMed  Google Scholar 

  54. Roepstorff, A. & Nansen, P. Epidemiology, diagnosis and control of helminth parasites of swine. 3, 35–68. 1998. http://www.fao.org/3/a-x0520e.pdf, FAO, Food and Agriculture Organization of the United Nations.

  55. Sarti E., Flisser A., Schantz P. M., Gleizer M., Loya M., Plancarte A., Avila G., Allan J., Craig P. S., Bronfman M. & Wijeyaratne P. 1997. Development and evaluation of a health education intervention against Taenia solium in a rural community in Mexico. Am J Trop Med Hyg 56: 2, 127–132.

    CAS  Article  PubMed  Google Scholar 

  56. Tamboura H. H., Banga-Mboko H., Maes D., Youssao I., Traore A. A., Bayala B. & Dembele M. A. 2006. Prevalence of common gastrointestinal nematode parasites in scavenging pigs of different ages and sexes in eastern centre province, Burkina Faso. Onderstepoort Journal of Veterinary Research 73: 53–60.

    CAS  Article  PubMed  Google Scholar 

  57. Thomas L. F., Bishop R. P., Onzere C., Mcintosh M. T., Lemire K. A., de Glanville W. A., Cook E. A. & Fèvre E. M. 2016. Evidence for the presence of African swine fever virus in an endemic region of Western Kenya in the absence of any reported outbreak. BMC Veterinary Research 12: 1, 192.

    Article  PubMed  PubMed Central  Google Scholar 

  58. Thrusfield M. V. 2007. Survey. In: Veterinary Epidemiology. Blackwell,.228–246.

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Acknowledgements

Thanks are extended to the Serviços Provinciais de Pecuária de Tete, Serviços Distritais das Actividades Económicas de Angónia and Estação Zootécnica de Angónia. Special thanks are to the smallholder pig keepers and livestock extension agents in Angónia districts for their support and time allocated during the study period. We would also like to thank Dr. Regina Miambo, Dr. Cláudio Gule, Dr. Elísio Chato, Dr. Lourenço Mapaco and Mr. Elísio Inácio Bendito for their valuable assistance in the field work.

Funding

The authors are grateful for the financial support by the Danish International Development Agency (DANIDA) (file no. 09-007LIFE) through the project, Securing Rural Livelihood through Improved Pig Production in Mozambique and Tanzania (SLIPP).

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Affiliations

  1. Faculty of Veterinary, Eduardo Mondlane University, Maputo, Mozambique

    A. G. Chilundo, A. Pondja, R. Miambo & S. Afonso

  2. School of Life Science, University of KwaZulu-Natal, Westville Campus, Durban, South Africa

    A. G. Chilundo & S. Mukaratirwa

  3. Section for Parasitology and Aquatic Pathobiology, Department of Veterinary and Animal Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, Dyrlægevej 100, DK-1870, Frederiksberg C, Denmark

    M. V. Johansen

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  1. A. G. Chilundo
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  2. M. V. Johansen
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Correspondence to A. G. Chilundo.

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Chilundo, A.G., Johansen, M.V., Pondja, A. et al. Piloting the effectiveness of pig health education in combination with oxfendazole treatment on prevention and/or control of porcine cysticercosis, gastrointestinal parasites, African swine fever and ectoparasites in Angónia District, Mozambique. Trop Anim Health Prod 50, 589–601 (2018). https://doi.org/10.1007/s11250-017-1474-6

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Keywords

  • Health education
  • Oxfendazole
  • Smallholder farmers
  • Prevalence
  • Porcine cysticercosis
  • GI helminths
  • African swine fever
  • Ectoparasites