Clustering of Necropsy-Confirmed Porcine Cysticercosis Surrounding Taenia solium Tapeworm Carriers in Peru

Andres G. Lescano Emerging Diseases and Climate Change Research Unit, School of Public Health and Administration, Universidad Peruana Cayetano Heredia, Lima, Peru;
Department of International Health, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland;

Search for other papers by Andres G. Lescano in
Current site
Google Scholar
PubMed
Close
,
Ian W. Pray School of Public Health, Oregon Health and Science University and Portland State University, Portland, Oregon;

Search for other papers by Ian W. Pray in
Current site
Google Scholar
PubMed
Close
,
Armando E. Gonzalez Department of International Health, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland;
School of Veterinary Medicine, Universidad Nacional Mayor de San Marcos, Lima, Peru;

Search for other papers by Armando E. Gonzalez in
Current site
Google Scholar
PubMed
Close
,
Robert H. Gilman Department of International Health, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland;
Department of Microbiology, School of Sciences, Universidad Peruana Cayetano Heredia, Lima, Peru;
Research Department, Asociación Benéfica PRISMA (Proyectos en Informatica, Salud, Medicina y Agricultura), Lima, Peru;

Search for other papers by Robert H. Gilman in
Current site
Google Scholar
PubMed
Close
,
Victor C. W. Tsang Division of Parasitic Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia;

Search for other papers by Victor C. W. Tsang in
Current site
Google Scholar
PubMed
Close
,
Ricardo Gamboa Center for Global Health Tumbes, Universidad Peruana Cayetano Heredia, Lima, Peru;

Search for other papers by Ricardo Gamboa in
Current site
Google Scholar
PubMed
Close
,
M. Claudia Guezala School of Veterinary Medicine, Universidad Nacional Mayor de San Marcos, Lima, Peru;

Search for other papers by M. Claudia Guezala in
Current site
Google Scholar
PubMed
Close
,
Viterbo Aybar School of Veterinary Medicine, Universidad Nacional Mayor de San Marcos, Lima, Peru;
Center for Global Health Tumbes, Universidad Peruana Cayetano Heredia, Lima, Peru;

Search for other papers by Viterbo Aybar in
Current site
Google Scholar
PubMed
Close
,
Silvia Rodriguez Instituto de Ciencias Neurológicas, Cysticercosis Unit, Lima, Peru

Search for other papers by Silvia Rodriguez in
Current site
Google Scholar
PubMed
Close
,
Lawrence H. Moulton Department of International Health, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland;

Search for other papers by Lawrence H. Moulton in
Current site
Google Scholar
PubMed
Close
,
Elli Leontsini Department of International Health, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland;

Search for other papers by Elli Leontsini in
Current site
Google Scholar
PubMed
Close
,
Guillermo Gonzalvez Department of Microbiology, School of Sciences, Universidad Peruana Cayetano Heredia, Lima, Peru;

Search for other papers by Guillermo Gonzalvez in
Current site
Google Scholar
PubMed
Close
,
Seth E. O’Neal School of Public Health, Oregon Health and Science University and Portland State University, Portland, Oregon;

Search for other papers by Seth E. O’Neal in
Current site
Google Scholar
PubMed
Close
,
Hector H. Garcia Department of International Health, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland;
Department of Microbiology, School of Sciences, Universidad Peruana Cayetano Heredia, Lima, Peru;
Center for Global Health Tumbes, Universidad Peruana Cayetano Heredia, Lima, Peru;
Instituto de Ciencias Neurológicas, Cysticercosis Unit, Lima, Peru

Search for other papers by Hector H. Garcia in
Current site
Google Scholar
PubMed
Close
, and
for the Cysticercosis Working Group in Peru Emerging Diseases and Climate Change Research Unit, School of Public Health and Administration, Universidad Peruana Cayetano Heredia, Lima, Peru;
Department of International Health, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland;
School of Public Health, Oregon Health and Science University and Portland State University, Portland, Oregon;
School of Veterinary Medicine, Universidad Nacional Mayor de San Marcos, Lima, Peru;
Department of Microbiology, School of Sciences, Universidad Peruana Cayetano Heredia, Lima, Peru;
Research Department, Asociación Benéfica PRISMA (Proyectos en Informatica, Salud, Medicina y Agricultura), Lima, Peru;
Division of Parasitic Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia;
Center for Global Health Tumbes, Universidad Peruana Cayetano Heredia, Lima, Peru;
Instituto de Ciencias Neurológicas, Cysticercosis Unit, Lima, Peru

Search for other papers by for the Cysticercosis Working Group in Peru in
Current site
Google Scholar
PubMed
Close
Restricted access

The pork tapeworm, Taenia solium, is among the leading causes of preventable epilepsy in the world and is common in rural areas of developing countries where sanitation is limited and pigs have access to human feces. Prior studies in rural villages of Peru have observed clusters of T. solium cysticercosis among pigs that live near human tapeworm carriers. Such spatial analyses, however, have been limited by incomplete participation and substandard diagnostic tests. In this study, we evaluated the association between necropsy-confirmed cysticercosis in pigs and their distance to T. solium tapeworm carriers in six villages in northern Peru. A total of six (1.4%) tapeworm carriers were detected using copro-antigen enzyme-linked immunosorbent assay and seven of 10 (70%) pigs belonging to the tapeworm carriers were found with viable cyst infection on necropsy. This was significantly greater than the prevalence of viable cyst infection among pigs living < 500 m (11%) and > 500 m (0.5%) from a tapeworm carrier (P < 0.001 for distance trend). Similar statistically significant prevalence gradients were observed after adjustment for possible confounders and for other pig-level outcomes including infection with > 10 viable cysts, degenerated cyst infection, and serological outcomes. This investigation confirms that porcine cysticercosis clusters strongly around tapeworm carriers in endemic rural regions of northern Peru and supports interventions that target these hotspots.

Author Notes

Address correspondence to Ian W. Pray, School of Public Health, Oregon Health and Science University, 3181 SW Sam Jackson Park Rd., Portland, OR 97239, E-mail: pray@ohsu.edu or Andres G. Lescano, School of Public Health and Administration, Universidad Peruana Cayetano Heredia, Ave. Honorio Delgado 430, Urb. Ingenierıa, S.M.P., Lima, Peru, E-mail: willy.lescano@upch.pe.

Financial support: This study was partially funded by research grants numbers P01 AI51976 and U01 AI35894 from the National Institute of Allergy and Infectious Diseases, NIH, Bethesda, MD. Partial support was also received by R01NS080645 from the National Institute of Neurological Disorders and Stroke. Research grants from the Wellcome Trust (063109), the Food and Drug Administration (002309), and the Bill & Melinda Gates Foundation (23981) fund ongoing cysticercosis research by the authors. A. G. L. is sponsored by the training grant D43 TW007393 awarded by the Fogarty International Center of the U.S. National Institutes of Health.

Authors’ addresses: Andres G. Lescano, School of Public Health and Administration, Universidad Peruana Cayetano Heredia, Lima, Peru, E-mail: willy.lescano@upch.pe. Ian W. Pray and Seth E. O’Neal, School of Public Health, Oregon Health and Science University and Portland State University, Portland, OR, E-mails: pray@ohsu.edu and oneals@ohsu.edu. Armando E. Gonzalez and M. Claudia Guezala, School of Veterinary Medicine, Universidad Nacional Mayor de San Marcos, Lima, Peru, E-mails: agonza41@jhu.edu and cguezala@gmail.com. Robert H. Gilman, Department of International Health, Johns Hopkins University, Baltimore, MD, E-mail: gilmanbob@gmail.com. Victor C. W. Tsang, Georgia State University, Atlanta, GA, E-mail: vct123@gmail.com. Ricardo Gamboa and Viterbo Aybar, Centro de Salud Global Tumbes, Universidad Peruana Cayetano Heredia, Lima, Peru, E-mails: rgamboa@peruresearch.org and vayvar@peruresearch.org. Lawrence H. Moulton and Elli Leontsini, Department of International Health, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, E-mails: lmoulto1@jhu.edu and eleontsi@jhu.edu. Guillermo Gonzalvez and Hector H. Garcia, Department of Microbiology, School of Sciences, Universidad Peruana Cayetano Heredia, Lima, Peru, E-mails: gonzalvezg@paho.org and hgarcia1@jhu.edu.

These authors contributed equally to this work.

Deceased.

  • 1.

    Commission on Tropical Diseases of the International League Against Epilepsy, 1994. Relationship between epilepsy and tropical diseases. Epilepsia 35: 8993.

  • 2.

    Lescano AG, García HH, Gilman RH, Guezala MC, Tsang VCW, Gavidia CM, Rodriguez S, Moulton LH, Green JA, Gonzalez AE; Cysticercosis Working Group in Peru, 2007. Swine cysticercosis hotspots surrounding Taenia solium tapeworm carriers. Am J Trop Med Hyg 76: 376383.

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

    O’Neal SE et al. 2012. Geographic correlation between tapeworm carriers and heavily infected cysticercotic pigs. PLoS Negl Trop Dis 6: e1953.

  • 4.

    Pray IW, Ayvar V, Gamboa R, Muro C, Moyano LM, Benavides V, Flecker RH, Garcia HH, O’Neal SE, 2017. Spatial relationship between Taenia solium tapeworm carriers and necropsy cyst burden in pigs. PLoS Negl Trop Dis 11: e0005536.

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

    O’Neal SE, Moyano LM, Ayvar V, Rodriguez S, Gavidia C, Wilkins PP, Gilman RH, Garcia HH, Gonzalez AE; Cysticercosis Working Group in Peru, 2014. Ring-screening to control endemic transmission of Taenia solium. PLoS Negl Trop Dis 8: e3125.

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

    Garcia HH et al. 2016. Elimination of Taenia solium transmission in northern Peru. N Engl J Med 374: 23352344.

  • 7.

    Tsang VC, Brand JA, Boyer AE, 1989. An enzyme-linked immunoelectrotransfer blot assay and glycoprotein antigens for diagnosing human cysticercosis (Taenia solium). J Infect Dis 159: 5059.

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

    Tsang VCW, Pilcher JA, Zhou W, Boyer AE, Kamango-Sollo EIP, Rhoads ML, Murrell KD, Schantz PM, Gilman RH, 1991. Efficacy of the immunoblot assay for cysticercosis in pigs and modulated expression of distinct IgM/ IgG activities to Taenia solium antigens in experimental infections. Vet Immunol Immunopathol 29: 6978.

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

    Jayashi CM, Gonzalez AE, Castillo Neyra R, Rodríguez S, García HH, Lightowlers MW, 2014. Validity of the enzyme-linked immunoelectrotransfer blot (EITB) for naturally acquired porcine cysticercosis. Vet Parasitol 199: 4249.

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

    Muro C et al. 2017. Porcine cysticercosis: possible cross-reactivity of taenia hydatigena to GP50 antigen in the enzyme-linked immunoelectrotransfer blot assay. Am J Trop Med Hyg 97: 18301832.

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

    Engel HN, Claire LE, 1986. Anatomy. Leman AD, Straw BE, Mengelin WL, eds. Diseases of Swine. Ames, IA: Iowa State University Press, 325.

  • 12.

    Bustos JA et al. 2012. Detection of Taenia solium taeniasis coproantigen is an early indicator of treatment failure for taeniasis. Clin Vaccine Immunol 19: 570573.

  • 13.

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

  • 14.

    Pearson RD, Hewlett EL, 1985. Niclosamide therapy for tapeworm infections. Ann Intern Med 102: 550551.

  • 15.

    Flisser A, Madrazo I, Plancarte A, Schantz P, Allan J, Craig P, Sarti E, 1993. Neurological symptoms in occult neurocysticercosis after single taeniacidal dose of praziquantel. Lancet 342: 748.

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

    Allan JC, Velasquez-Tohom M, Torres-Alvarez R, Yurrita P, Garcia-Noval J, 1996. Field trial of the coproantigen-based diagnosis of Taenia solium taeniasis by enzyme-linked immunosorbent assay. Am J Trop Med Hyg 54: 352356.

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

    Tello R, Terashima A, Marcos LA, Machicado J, Canales M, Gotuzzo E, 2012. Highly effective and inexpensive parasitological technique for diagnosis of intestinal parasites in developing countries: spontaneous sedimentation technique in tube. Int J Infect Dis 16: 20112013.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    Mayta H, Talley A, Gilman RH, Jimenez J, Verastegui M, Ruiz M, Garcia HH, Gonzalez AE, 2000. Differentiating Taenia solium and Taenia saginata infections by simple hematoxylin-eosin staining and PCR-restriction enzyme analysis. J Clin Microbiol 38: 133137.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Yolken RH, Stopa PJ, 1979. Analysis of nonspecific reactions in enzyme-linked immunosorbent assay testing for human rotavirus. J Clin Microbiol 10: 703707.

  • 20.

    Allan JC, Wilkins PP, Tsang VCW, Craig PS, 2003. Immunodiagnostic tools for taeniasis. Acta Trop 87: 8793.

  • 21.

    Sikasunge CS, Johansen MV, Willingham AL, Leifsson PS, Phiri IK, 2008. Taenia solium porcine cysticercosis: viability of cysticerci and persistency of antibodies and cysticercal antigens after treatment with oxfendazole. Vet Parasitol 158: 5766.

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

    Nelder JA, Wedderburn RWM, 1972. Generalized lineal models. J R Stat Soc Ser A 135: 370384.

  • 23.

    Pray IW, Swanson DJ, Ayvar V, Muro C, Moyano LM, Gonzalez AE, Garcia HH, O’Neal SE; Cysticercosis Working Group in Peru, 2016. GPS tracking of free-ranging pigs to evaluate ring strategies for the control of cysticercosis/taeniasis in Peru. PLoS Negl Trop Dis 10: e0004591.

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

    Pawlowsky Z, 2002. Taenia solium: basic biology and transmission. Singh G, Prabhakar S, eds. Taenia solium Cysticercosis: From Basic to Clinical Science. New York, NY: CABI Publishing, 114.

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

    Braae UC, Harrison W, Lekule F, Magnussen P, Johansen MV, 2015. Feedstuff and poor latrines may put pigs at risk of cysticercosis—a case-control study. Vet Parasitol 214: 187191.

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

    Huerta M et al. 2008. Parasite contamination of soil in households of a Mexican rural community endemic for neurocysticercosis. Trans R Soc Trop Med Hyg 102: 374379.

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

    Thevenet PS, Jensen O, Drut R, Cerrone GE, Grenóvero MS, Alvarez HM, Targovnik HM, Basualdo JA, 2005. Viability and infectiousness of eggs of Echinococcus granulosus aged under natural conditions of inferior arid climate. Vet Parasitol 133: 7177.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    Wachira TM, Macpherson CN, Gathuma JM, 1991. Release and survival of Echinococcus eggs in different environments in Turkana, and their possible impact on the incidence of hydatidosis in man and livestock. J Helminthol 65: 5561.

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

    Ilsøe B, Kyvsgaard NC, Nansen P, Henriksen SA, 1990. A study on the survival of Taenia saginata eggs on soil in Denmark. Acta Vet Scand 31: 153158.

  • 30.

    Coman BJ, Rickard MD, 1977. A comparison of in vitro and in vivo estimates of the viability of Taenia pisiformis eggs aged under controlled conditions, and their ability to immunise against a challenge infection. Int J Parasitol 7: 1520.

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

    Lawson JR, Gemmell MA, 1990. Transmission of taeniid tapeworm eggs via blowflies to intermediate hosts. Parasitology 100: 143146.

  • 32.

    Gomez-Puerta LA, Lopez-Urbina MT, Garcia HH, Gonzalez AE, 2014. Longevity and viability of Taenia solium eggs in the digestive system of the beetle Ammophorus rubripes. Rev Bras Parasitol Veterinária 23: 9497.

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

    Pajuelo MJ et al. 2015 Identification and characterization of microsatellite markers derived from the whole genome analysis of Taenia solium. PLoS Negl Trop Dis 9: 115.

    • PubMed
    • Search Google Scholar
    • Export Citation
Past two years Past Year Past 30 Days
Abstract Views 968 768 50
Full Text Views 1455 7 0
PDF Downloads 267 7 0
 

 

 

 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save