Identification and control of sources of Taenia solium infection – the attempts to eradicate the parasite

Open access

Abstract

Taenia solium is a parasite causing porcine cysticercosis and human taeniosis and cysticercosis, parasitic zoonoses with a serious public health and economic influence. It has been globally ranked as the top foodborne parasite by the Food and Agriculture Organisation of the United Nations (FAO) and the World Health Organisation (WHO). This parasite is transmitted mainly in countryside regions where animals are free roaming, having access to human faeces, and infected pork is widely available. More developed countries eliminated cysticercosis; nonetheless, there are insufficient data about the current endemicity status of T. solium, due to increased human migration from endemic areas. Formally submitted statistics on cysticercosis in pigs are extremely inadequate. This is the result of not reporting all cases of the disease by some countries and lack of molecular verification during identification of the parasite. There is a need to develop diagnostic tests with increased sensitivity and specificity. The purpose of the present review is to summarise current knowledge about diagnostic and control methods concerning T. solium infection. The article does not address the diagnostics of human cysticercosis, since there is a distinct medical field which should be discussed separately. The paper focuses mainly on identifying the sources of T. solium infection, presenting the methods to detect and control porcine cysticercosis and taeniosis in humans.

1. Allan J.C., Avila G., Garcia Noval J., Flisser A., Craig P.S.: Immunodiagnosis of taeniasis by coproantigen detection. Parasitology 1990, 101, 473–477.

2. Allan J.C., Wilkins P.P., Tsang V.C.W., Craig P.S.: Immunodiagnostic tools for taeniasis. Acta Trop 2003, 87, 87–93.

3. Assana E., Kanobana K., Tume C.B., Zoli P.A., Nguekam, Geerts S., Berkvens D., Dorny P.: Isolation of a 14 kDa antigen from Taenia solium cyst fluid by HPLC and its evaluation in enzyme linked immunosorbent assay for diagnosis of porcine cysticercosis. Res Vet Sci 2007, 82, 370–376.

4. Assana E., Kyngdon C.T., Gauci C.G., Geerts S., Dorny P., De Deken R., Anderson G.A., Zoli A.P., Lightowlers M.W.: Elimination of Taenia solium transmission to pigs in a field trial of the TSOL18 vaccine in Cameroon. Int J Parasitol 2010, 40, 515–519.

5. Bern C., Garcia H.H., Evans C., Gonzalez A.E., Verastegui M., Tsang V.C., Gilman R.H.: Magnitude of the disease burden from neurocysticercosis in a developing country. Clin Infect Dis 1999, 29, 1203–1209.

6. Braae U.C., Devleesschauwer B., Gabriel S., Dorny P., Speybroeck N., Magnussen P., Torgerson P., Johansen M.V.: CystiSim - An agent-based model for Taenia solium transmission and control. PLoS Negl Trop Dis 2016, 10, e0005184.

7. Chung J.Y., Kang S.Y., Bahk Y.Y., Kong Y., Huh S., Cho S.Y.: A Recombinant 10-kDa Protein of Taenia solium metacestodes specific to active neurocysticercosis. J Infect Dis 1999, 180, 1307–1315.

8. Deckers N., Dorny P.: Immunodiagnosis of Taenia solium taeniosis/cysticercosis. Trends Parasitol 2010, 26, 137–144.

9. Dorny P., Brandt J., Zoli A., Geerts S.: Immunodiagnostic tools for human and porcine cysticercosis. Acta Tropica 2003, 87, 79–86.

10. Dorny P., Phiri I.K., Vercruysse J., Gabriel S., Willingham A.L. 3rd, Brandt J., Victor B., Speybroeck N., Berkvens D.: A Bayesian approach for estimating values for prevalence and diagnostic test characteristics of porcine cysticercosis. Int J Parasitol 2004, 34, 569–576.

11. FAO/WHO: Multicriteria-based ranking for risk management of food-borne parasites. Report of a Joint FAO/WHO Expert Meeting 3–7 September 2012, FAO Headquarters, Rome, Italy. FAO/WHO, Geneva, 2014, p. 322.

12. Gabriël S., Dornya P., Mwape K.E., Trevisan C., Braae U.C., Magnussen P., Thys S., Bulaya C., Phiri I.K., Sikasunge C.S., Makungu C., Afonso S., Nicolau Q., Johansen M.V.: Control of Taenia solium taeniasis/cysticercosis: The best way forward for sub-Saharan Africa? Acta Trop 2017, 165, 252–260.

13. Gabriël S., Johansen M.V., Pozio E., Smit G.S., Devleesschauwer B., Allepuz A., Papadopoulos E., van der Giessen J., Dorny P.: Human migration and pig/pork import in the European Union: What are the implications for Taenia solium infections? Vet Parasitol 2015, 213, 38–45.

14. Garcia-Noval J., Allan J.C., Fletes C., Moreno E., DeMata F., Torres-Alvarez R., Soto de Alfaro H., Yurrita P., Higueros-Morales H., Mencos F., Craig P.S.: Epidemiology of Taenia solium taeniasis and cysticercosis in two rural Guatemalan communities. Am J Trop Med Hyg 1996, 55, 282–289.

15. Garcia H.H., Gonzalez A.E., Evans C.A., Gilman R.H.: Cysticercosis Working Group in Peru.: Taenia solium cysticercosis. Lancet 2003, 362, 547–556.

16. Garcia H.H., Gonzalez A.E., Gilman R.H., Moulton L.H., Verastegui M., Rodriguez S., Gavidia C., Tsang V.C.: Combined human and porcine mass chemotherapy for the control of T. solium. Am J Trop Med Hyg 2006, 74, 850–855.

17. Gonzalez A.E., García H.H., Gilman R.H., Tsang V.C.: Control of Taenia solium. Acta Trop 2003, 87, 103–109.

18. Gonzalez A.E., Gauci C.G., Barber D., Gilman R.H., Tsang V.C., Garcia H.H., Verastegui M., Lightowlers M.W.: Vaccination of pigs to control human neurocysticercosis. Am J Trop Med Hyg 2005, 72, 837–839.

19. Gonzalez A.E., Gavidia C., Falcon N., Bernal T., Verastegui M., Garcia H.H., Gilman R.H., Tsang V.C.: Protection of pigs with cysticercosis from further infections after treatment with oxfendazole. Am J Trop Med Hyg 2001, 65, 15–28.

20. González L.M., Montero E., Puente S., López-Velez R., Hernández M., Sciutto E., Harrison L.J., Parkhouse R.M., Gárate T.: PCR tools for the differential diagnosis of Taenia saginata and Taenia solium taeniasis/cysticercosis from different geographical locations. Diagn Microbiol Infect Dis 2002 42, 243–249.

21. Gripper L.B., Welburn S.C.: Neurocysticercosis infection and disease – A review. Acta Trop 2017, 166, 218–224.

22. Guezala M.C., Rodriguez S., Zamora H., Garcia H.H., Gonzalez A.E., Tembo A., Allan J.C., Craig P.S.: Development of a species-specific coproantigen ELISA for human Taenia soliumtaeniasis. Am J Trop Med Hyg 2009, 81, 433–437.

23. Huerta M., de Aluja A.S., Fragoso G., Toledo A., Villalobos N., Hernández M., Gevorkian G., Acero G., Díaz A., Alvarez I., Avila R., Beltrán C., Garcia G., Martinez J.J., Larralde C., Sciutto E.: Synthetic peptide vaccine against Taenia solium pig cysticercosis: successful vaccination in a controlled field trial in rural Mexico. Vaccine 2001, 12, 262–266.

24. Ito A., Wandra T., Yamasaki H., Nakao M., Sako Y., Nakaya K., Margono S.S., Suroso T., Gauci C., Lightowlers M.W.: Cysticercosis/taeniasis in Asia and the Pacific. Vector Borne Zoonotic Dis 2004, 4, 95–107.

25. Jardim E.A.G.V., Linhares G.F.C., Torres F.A.G., Araujo J.L.B., Barbosa S.M.: Specific discrimination between Taenia saginata and Taenia solium by one step PCR assay and duplex-PCR. Ciencia Rural, Santa Maria 2006, 36, 166–172.

26. Jayashi C.M., Kyngdon C.T., Gauci C.G., Gonzalez A.E., Lightowlers M.W.: Successful immunization of naturally reared pigs against porcine cysticercosis with a recombinant oncosphere antigen vaccine. Vet Parasitol 2012, 188, 261–267.

27. Karamon J., Sroka J., Cencek T., Różycki M., Chmurzyńska E., Bilska-Zając E., Zdybel J., Nowak P., Kędzierska J., Dębiak P.: Optimisation and comparison of three PCR procedures for molecular identification of Taenia solium. Bull Vet Inst Pulawy 2013, 57, 507–512.

28. Kyvsgaard N.C., Johansen M.V., Carabin H.: Simulating transmission and control of Taenia solium infections using a Reed-Frost stochastic model. Int J Parasitol 2007, 37, 547–558.

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

30. Lightowlers M.W.: Eradication of Taenia solium cysticercosis: A role for vaccination of pigs. Int J Parasitol 2010, 15, 1183–1192.

31. Martinez-Ocaña J., Romero-Valdovinos M., de Kaminsky R.G., Maravilla P., Flisser A.: Immunolocalization of TSOL18 and TSOL45-1A, the successful protective peptides against porcine cysticercosis, in Taenia solium oncospheres. Parasit Vectors 2011, 4:3.

32. Mayta H., Gilman R.H., Prendergast E., Castillo J.P., Tinoco Y.O., Garcia H.H., Gonzalez A.E., Sterling C.R., Cysticercosis Working Group in Peru.: Nested PCR for specific diagnosis of Taenia solium taeniasis. J Clin Microbiol 2008, 46, 286–289.

33. Murrel K.D., Dorny P., Flisser A., Geerts S., Kyvsgaard N.C., McManus D., Nash T., Pawlowski Z.:WHO/FAO/OIE Guidelines for the surveillance, prevention and control of taeniosis/cysticercosis. OIE, WHO, FAO, Geneva, 2005.

34. OIE: Manual of Diagnostic Tests and Vaccines for Terrestrial Animals. Paris 2008, chapter 2.9.5.

35. Pawlowski Z., Allan J., Sarti E.: Control of Taenia solium taeniasis/cysticercosis: From research towards implementation. Int J Parasitol 2005, 35 1221–1232.

36. Praet N., Verweij J.J., Mwape K.E., Phiri I.K., Muma J.B., Zulu G., van Lieshout L., Rodriguez-Hidalgo R., Benitez-Ortiz W., Dorny P., Gabriel S.: Bayesian modelling to estimate the test characteristics of coprology, coproantigen ELISA and a novel real-time PCR for the diagnosis of taeniasis. Trop Med Int Health 2013, 18, 608–614.

37. Rodriguez S., Wilkins P., Dorny P.: Immunological and molecular diagnosis of cysticercosis. Pathog Glob Health 2012, 106, 286–298.

38. Sako Y., Nakao M., Ikejima T., Piao X.Z., Nakaya K., Ito A.: Molecular characterization and diagnostic value of Taenia solium low-molecular-weight antigen genes. J Clin Microbiol 2000, 38, 4439–4444.

39. Sarti E., Rajshekhar V.: Measures for the prevention and control of Taenia solium taeniosis and cysticercosis. Acta Trop 2003, 87, 137–143.

40. Sciutto E., Morales J., Martinez J.J., Toledo A., Villalobos M.N., Cruz-Revilla C., Meneses G., Hernandez M., Diaz A., Rodarte L.F., Acero G., Gevorkian G., Manoutcharian K., Paniagua J., Fragoso G., Fleury A., Larralde R., De Aluja A.S., Larralde C.: Further evaluation of the synthetic peptide vaccine S3Pvac against Taenia solium cysticercosis in pigs in an endemic town of Mexico. Parasitology 2007, 134, 129–133.

41. Sreedevi C., Hafeez M., Kumar P.A., Rayulu V.C., Subramanyam K.V., Sudhakar K.: PCR test for detecting Taenia solium cysticercosis in pig carcasses. Trop Anim Health Prod 2012, 44, 95–99.

42. Tsang V.C., Brand J.A., Boyer A.E.: An enzyme-linked immunoelectrotransfer blot assay and glycoprotein antigens for diagnosing human cysticercosis (Taenia solium). J Infect Dis 1989, 159, 50–59.

43. WHO: Accelerating work to overcome the global impact of neglected tropical diseases – A roadmap for implementation. WHO, Geneva, 2012, p. 42.

44. WHO: Taenia solium Taeniasis/Cysticercosis Diagnostic Tools. Report of a Stakeholder Meeting, 17–18 December 2015. WHO, Geneva, 2015, p. 26.

45. WHO:Taeniasis/cysticercosis (Updated March 2017) URL: http://www.who.int/mediacentre/factsheets/fs376/en/WHO, 2017.

46. WHO: Working to overcome the global impact of neglected tropical diseases. First WHO report on neglected tropical diseases. WHO, Geneva, 2010, p. 184.

47. Yamasaki H., Allan J.C., Sato M.O., Nakao M., Sako Y., Nakaya K., Qiu D., Mamuti W., Craig P.S., Ito A.: DNA Differential diagnosis of taeniasis and cysticercosis by multiplex PCR. J Clin Microbiol 2004, 42, 548–553.

Journal of Veterinary Research

formerly Bulletin of the Veterinary Institute in Pulawy

Journal Information


IMPACT FACTOR Bull Vet Inst Pulawy 2016: 0.462

CiteScore 2016: 0.46

SCImago Journal Rank (SJR) 2015: 0.230
Source Normalized Impact per Paper (SNIP) 2015: 0.383

Metrics

All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 118 118 21
PDF Downloads 48 48 10