Hostname: page-component-848d4c4894-wzw2p Total loading time: 0 Render date: 2024-06-08T06:16:51.943Z Has data issue: false hasContentIssue false

Co-occurrence of swine cysticercosis due to Taenia solium and Taenia hydatigena in ethnic minority villages at the Thai–Myanmar border

Published online by Cambridge University Press:  28 August 2018

K. Chaisiri*
Affiliation:
Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand
T. Kusolsuk
Affiliation:
Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand
N. Homsuwan
Affiliation:
Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand
S. Sanguankiat
Affiliation:
Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand
P. Dekumyoy
Affiliation:
Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand
G. Peunpipoom
Affiliation:
Tak Provincial Livestock Office, Tak Province, Thailand
S. Khiriphattharaphon
Affiliation:
Nong Bua Health Promoting Hospital, Tha Song Yang, Tak province, Thailand
Y. Sako
Affiliation:
Department of Parasitology, Asahikawa Medical University, Asahikawa, Hokkaido, Japan
T. Yanagida
Affiliation:
Laboratory of Parasitology, Joint Faculty of Veterinary Medicine, Yamaguchi University, Yamaguchi, Japan
M. Okamoto
Affiliation:
Section of Wildlife Diversity, Center for Human Evolution Modeling Research, Primate Research Institute, Kyoto University, Inuyama, Aichi, Japan
A. Ito*
Affiliation:
Department of Parasitology, Asahikawa Medical University, Asahikawa, Hokkaido, Japan
*
Author for correspondence: K. Chaisiri, E-mail: kittipong.cha@mahidol.ac.th A. Ito, E-mail: akiraito@asahikawa-med.ac.jp
Author for correspondence: K. Chaisiri, E-mail: kittipong.cha@mahidol.ac.th A. Ito, E-mail: akiraito@asahikawa-med.ac.jp

Abstract

As part of the international joint projects working towards the control of taeniosis/cysticercosis in Asia Pacific, epidemiological studies on Taenia solium cysticercosis have been carried out in high-incidence populations, such as minority groups in Thailand. To assess the epidemiology of cysticercotic infections in pigs in the hill-tribe minority villages (Karen) in Tak province, Thailand, we conducted serological screening and necropsies. The patterns of antibody response to T. solium antigens were then investigated using immunoblot assays. Of the 188 pig serum samples tested for antibody responses to partially purified low-molecular-weight antigens of T. solium cyst fluid, positive responses were detected in 37 samples (19.7%). Based on these results, 16 pigs (10 seropositive and 6 seronegative) were necropsied for investigation of cysticerci and intestinal parasites. All seropositive pigs were coinfected with both T. solium and Taenia hydatigena cysticerci, except one, which was infected with T. hydatigena alone. Three of the six seronegative pigs were confirmed to be infected with T. hydatigena. Pigs infected with T. solium showed much stronger antibody responses than those infected with T. hydatigena. Our results demonstrate the co-occurrence of two swine cysticercoses due to T. solium and T. hydatigena in the studied areas. This study also reveals the importance of direct confirmation of the presence of cysticerci by necropsy after serological screening. In addition to the prevalence of swine cysticercosis in these endemic areas, our findings also reveal potential implications for the development of serological diagnostic assays for swine cysticercosis.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

Contributed equally to preparation of the manuscript.

References

Abuseir, S et al. (2013) An immunoblot for detection of Taenia saginata cysticercosis. Parasitology Research 112, 20692073.Google Scholar
Anantaphruti, MT et al. (2007) Sympatric occurrence of Taenia solium, T. saginata, and T. asiatica, Thailand. Emerging Infectious Diseases 13, 14131416.Google Scholar
Anantaphruti, MT et al. (2010) Molecular and serological survey on taeniasis and cysticercosis in Kanchanaburi Province, Thailand. Parasitology International 59, 326330.Google Scholar
Braae, UC et al. (2015) Taenia hydatigena cysticercosis in slaughtered pigs, goats, and sheep in Tanzania. Tropical Animal Health and Production 47, 15231530.Google Scholar
Chaisiri, K et al. (2017) Gastrointestinal helminths and Taenia spp. in parenteral tissues of free-roaming pigs (Sus scrofa indicus) from hill-tribe village at the western border of Thailand. Tropical Biomedicine 34, 464470.Google Scholar
Conlan, JV et al. (2012) A cross-sectional study of Taenia solium in a multiple taeniid-endemic region reveals competition may be protective. American Journal of Tropical Medicine and Hygiene 87, 281291.Google Scholar
Davaasuren, A et al. (2017) Neurocysticercosis: a case study of a Mongolian traveler who visited China and India with an updated review in Asia. Travel Medicine and Infectious Disease 20, 3136.Google Scholar
Deckers, N and Dorny, P (2010) Immunodiagnosis of Taenia solium taeniosis/cysticercosis. Trends in Parasitology 26, 137144.Google Scholar
Dermauw, V et al. (2016) Taenia hydatigena in pigs in Burkina Faso: a cross-sectional abattoir study. Veterinary Parasitology 230, 913.Google Scholar
Dorny, P et al. (2004) A Bayesian approach for estimating values for prevalence and diagnostic test characteristics of porcine cysticercosis. International Journal for Parasitology 34, 569576.Google Scholar
Garcia, HH et al. (2016) Elimination of Taenia solium transmission in northern Peru. New England Journal of Medicine 374, 23352344.Google Scholar
Ishida, MM et al. (2003) Helminth antigens (Taenia solium, Taenia crassiceps, Toxocara canis, Schistosoma mansoni and Echinococcus granulosus) and cross-reactivities in human infections and immunized animals. Acta Tropica 89, 7384.Google Scholar
Ito, A (2013) Nothing is perfect! Trouble-shooting in immunological and molecular studies of cestode infections. Parasitology 140, 15511565.Google Scholar
Ito, A and Budke, CM (2014) Culinary delights and travel? A review of zoonotic cestodiases and metacestodiases. Travel Medicine and Infectious Disease 12, 582591.Google Scholar
Ito, A and Craig, PS (2003) Immunodiagnostic and molecular approaches for the detection of taeniid cestode infections. Trends in Parasitology 19, 377381.Google Scholar
Ito, A, Takami, T and Itoh, M (1991) Vaccine effect of intact metacestodes of Taenia crassiceps against T. taeniaeformis infection in rats. American Journal of Tropical Medicine and Hygiene 44, 696701.Google Scholar
Ito, A et al. (1998) Novel antigens for neurocysticercosis: simple method for preparation and evaluation for serodiagnosis. American Journal of Tropical Medicine and Hygiene 59, 291294.Google Scholar
Ito, A et al. (1999) ELISA and immunoblot using purified glycoproteins for serodiagnosis of cysticercosis in pigs naturally infected with Taenia solium. Journal of Helminthology 73, 183186.Google Scholar
Ito, A et al. (2002) Dogs as alternative intermediate hosts of Taenia solium in Papua (Irian Jaya), Indonesia confirmed by highly specific ELISA and immunoblot using native and recombinant antigens and mitochondrial DNA analysis. Journal of Helminthology 76, 311314.Google Scholar
Ito, A, Nakao, M and Wandra, T (2003) Human taeniasis and cysticercosis in Asia. Lancet 362, 19181920.Google Scholar
Ito, A et al. (2014) The present situation of human taeniases and cysticercosis in Asia. Recent Patents on Anti-Infective Drug Discovery 9, 173185.Google Scholar
Ito, A, Yanagida, T and Nakao, M (2016) Recent advances and perspectives in molecular epidemiology of Taenia solium cysticercosis. Infection, Genetics and Evolution 40, 357367.Google Scholar
Kobayashi, K et al. (2013) Rare case of disseminated cysticercosis and taeniasis in a Japanese traveller after returning from India. American Journal of Tropical Medicine and Hygiene 89, 5862.Google Scholar
Krecek, RC et al. (2008) Prevalence of Taenia solium cysticercosis in swine from a community-based study in 21 villages of the Eastern Cape Province, South Africa. Veterinary Parasitology 154, 3847.Google Scholar
Kungu, JM et al. (2017) Sero-prevalence of Taenia spp. cysticercosis in rural and urban smallholder pig production settings in Uganda. Acta Tropica 165, 110115.Google Scholar
Li, T et al. (2006) Taeniasis/cysticercosis in a Tibetan population in Sichuan Province, China. Acta Tropica 100, 223231.Google Scholar
Li, T et al. (2007) Taeniasis/cysticercosis in China. Southeast Asian Journal of Tropical Medicine and Public Health 38 (Suppl 1), 131139.Google Scholar
Lightowlers, MW (2010) Fact or hypothesis: concomitant immunity in taeniid cestode infections. Parasite Immunology 32, 582589.Google Scholar
Lightowlers, MW (2013) Control of Taenia solium taeniasis/cysticercosis: past practices and new possibilities. Parasitology 140, 15661577.Google Scholar
Lightowlers, MW et al. (2015) Sensitivity of partial carcass dissection for assessment of porcine cysticercosis at necropsy. International Journal for Parasitology 45, 815818.Google Scholar
Lightowlers, MW et al. (2016) Monitoring the outcomes of interventions against Taenia solium: options and suggestions. Parasite Immunology 38, 158169.Google Scholar
McCleery, EJ et al. (2015) Taeniasis among refugees living on Thailand–Myanmar border. Emerging Infectious Diseases 21, 18241826.Google Scholar
Muro, C et al. (2017) Porcine cysticercosis: possible cross-reactivity of Taenia hydatigena to GP50 antigen in the enzyme-linked immunoelectrotransfer blot assay. American Journal of Tropical Medicine and Hygiene 97, 18301832.Google Scholar
Nguyen, MT et al. (2016) A systematic review on the global occurrence of Taenia hydatigena in pigs and cattle. Veterinary Parasitology 226, 97103.Google Scholar
Pawlowski, Z (2016) Taeniosis/neurocysticercosis control as a medical problem—a discussion paper. World Journal of Neuroscience 6, 165170.Google Scholar
Phiri, IK et al. (2002) The prevalence of porcine cysticercosis in eastern and southern provinces of Zambia. Veterinary Parasitology 108, 3139.Google Scholar
R Core Team (2015) R: A Language and Environment for Statistical Computing. Available from: https://www.r-project.org/ [accessed 19 November 2017].Google Scholar
Rózsa, L, Reiczigel, J and Majoros, G (2000) Quantifying parasites in samples of hosts. Journal of Parasitology 86, 228232.Google Scholar
Sako, Y et al. (2013) Simple and reliable preparation of immunodiagnostic antigens for Taenia solium cysticercosis. Parasitology 140, 15891594.Google Scholar
Sato, MO et al. (2003) Evaluation of tongue inspection and serology for diagnosis of Taenia solium cysticercosis in swine: usefulness of ELISA using purified glycoproteins and recombinant antigen. Veterinary Parasitology 111, 309322.Google Scholar
Sato, MO et al. (2018) Taenia solium, Taenia saginata, Taenia asiatica its hybrids and other helminthic infections occurring in a Neglected Tropical Diseases’ highly endemic area in Lao PDR. PLoS Neglected Tropical Diseases 12, e0006260.Google Scholar
Schantz, PM, Wilkins, PP and Tsang, VCW (1998) Immigrants, imaging, and immunoblots: the emergence of neurocysticercosis as a significant public health problem. Emerging Infections 2, 213242.Google Scholar
Sciutto, E et al. (1998) Limitation of current diagnostic procedures for the diagnosis of Taenia solium cysticercosis in rural pigs. Veterinary Parasitology 79, 299313.Google Scholar
Sikasunge, CS et al. (2008) Prevalence of Taenia solium porcine cysticercosis in the eastern, southern and western provinces of Zambia. Veterinary Journal 176, 240244.Google Scholar
Subahar, R et al. (2001) Taenia solium infection in Irian Jaya (West Papua), Indonesia: a pilot serological survey of human and porcine cysticercosis in Jayawijaya District. Transactions of the Royal Society of Tropical Medicine and Hygiene 95, 388390.Google Scholar
Swastika, K et al. (2016) Swine cysticercosis in the Karangasem district of Bali, Indonesia: an evaluation of serological screening methods. Acta Tropica 163, 4653.Google Scholar
Wandra, T et al. (2016) Neurocysticercosis diagnosed in a patient with Taenia saginata taeniasis after administration of praziquantel: a case study and review of the literature. Primary Healthcare: Open Access 6, 14.Google Scholar
WHO (World Health Organization) (2016) Landscape Analysis: Management of Neurocysticercosis with an Emphasis on Low- and Middle-income Countries. Geneva: World Health Organization.Google Scholar
Wu, HW et al. (2017) Cysticercosis/taeniasis endemicity in Southeast Asia: current status and control measures. Acta Tropica 165, 121132.Google Scholar
Yang, HJ et al. (1998) Immunoblot analysis of a 10 kDa antigen in cyst fluid of Taenia solium metacestodes. Parasite Immunology 20, 483488.Google Scholar