Hostname: page-component-8448b6f56d-m8qmq Total loading time: 0 Render date: 2024-04-16T22:11:00.224Z Has data issue: false hasContentIssue false
  • English
  • Français

Occurrence of Taenia species in pigs in slaughterhouses in Phu Tho province, northern Vietnam

Published online by Cambridge University Press:  14 October 2020

T.T.M. Nguyen ,
V. Dermauw ,
J. Noh ,
N.H. Chien ,
T.T.H. Dao ,
T.G.T. Nguyen ,
A. Van Hul  and
P. Dorny Open the ORCID record for P. Dorny [Opens in a new window]
T.T.M. Nguyen
Affiliation:
National Center for Veterinary Diagnosis, Tan Chung Chua, Hien Ninh, Soc Son, Hanoi, Vietnam Institute of Tropical Medicine, Department of Biomedical Sciences, Nationalestraat 155, 2000Antwerp, Belgium Ghent University, Faculty of Veterinary Medicine, Salisburylaan 133, 9820Merelbeke, Belgium
V. Dermauw
Affiliation:
Institute of Tropical Medicine, Department of Biomedical Sciences, Nationalestraat 155, 2000Antwerp, Belgium
J. Noh
Affiliation:
Centers for Disease Control and Prevention, Parasitic Diseases Branch, Atlanta, America
N.H. Chien
Affiliation:
Vietnam National University of Agriculture, Faculty of Veterinary Medicine, Trau Quy, Hanoi, Vietnam
T.T.H. Dao
Affiliation:
National Institute of Veterinary Research, 86 Truong Chinh Street, Phuong Mai, Dong Da, Hanoi, Vietnam
T.G.T. Nguyen
Affiliation:
National Institute of Veterinary Research, 86 Truong Chinh Street, Phuong Mai, Dong Da, Hanoi, Vietnam
A. Van Hul
Affiliation:
Institute of Tropical Medicine, Department of Biomedical Sciences, Nationalestraat 155, 2000Antwerp, Belgium
P. Dorny*
Affiliation:
Institute of Tropical Medicine, Department of Biomedical Sciences, Nationalestraat 155, 2000Antwerp, Belgium Ghent University, Faculty of Veterinary Medicine, Salisburylaan 133, 9820Merelbeke, Belgium
*
Author for correspondence: P. Dorny, E-mail: pdorny@itg.be
Get access Rights & Permissions [Opens in a new window]

Abstract

Pigs act as the intermediate hosts of the zoonotic tapeworms Taenia solium and Taenia asiatica, as well as of the non-zoonotic Taenia hydatigena. In Vietnam, human taeniasis and cysticercosis have been reported throughout the country; however, data on porcine cysticercosis are scarce. Our study aimed to estimate the prevalence of Taenia spp. in slaughtered pigs in two districts in Phu Tho, a mountainous province in northern Vietnam from where neurocysticercosis patients commonly originate. The carcasses of 399 pigs from 51 small-scale abattoirs were checked for cysticerci, while tongue, liver, masseter muscles, diaphragm and heart were sliced and examined. Retrieved cysticerci underwent polymerase chain reaction–restriction fragment length polymorphism and sequencing for species confirmation. Blood was also collected to detect antibodies by lentil lectin-purified glycoprotein enzyme-linked immunoelectrotransfer blot (LLGP-EITB) and recombinant T24H antigen (rT24H)-EITB and circulating antigens by B158/B60 Ag-ELISA. In two pigs, T. asiatica cysticerci were found, confirming the presence of the parasite in pigs in Vietnam at a low prevalence (0.5%; 95% exact confidence interval (CI): 0–1.19%). Cysticerci of T. solium were found in none of the pigs, although one serum sample was positive for antibodies in both LLGP-EITB and rT24H-EITB. Furthermore, a high prevalence of T. hydatigena cysticercosis was observed (18.0%; 95% Wilson score CI: 14.6–22.1%). In more than half of the T. hydatigena-positive pigs, circulating antigens were detected by Ag-ELISA, confirming that this test cannot be used to diagnose T. solium cysticercosis in this region. Finally, Spirometra erinaceieuropaei was found in one pig liver. It is the first record of this zoonotic cestode species in pigs in Vietnam. Overall, the findings confirmed the complex epidemiology of Taenia spp. in pigs in Vietnam.

Keywords

CysticercosisTaeniaSpirometrapigslaughterhousesVietnam
Type
Research Paper
Information
Journal of Helminthology , Volume 94 , 2020 , e201
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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.)

References

Anantaphruti, MT, Nawa, Y and Vanvanitchai, Y (2011) Human sparganosis in Thailand: an overview. Acta Tropica 118(3), 171–176.CrossRefGoogle ScholarPubMed
Bengtson, SD and Rogers, F (2001) Prevalence of sparganosis by county of origin in Florida feral swine. Veterinary Parasitology 97(3), 241–244.CrossRefGoogle ScholarPubMed
Blazek, K, Schramlova, J and Hulinska, D (1985) Pathology of the migration phase of Taenia hydatigena (Pallas, 1766) larvae. Folia Parasitologica 33, 127–137.Google Scholar
Conlan, JV, Vongxay, K, Khamlome, B, Dorny, P, Sripa, B, Elliot, A, Blacksell, SD, Fenwick, S and Thompson, RCA (2012) A cross-sectional study of Taenia solium in a multiple taeniid-endemic region reveals competition may be protective. American Society of Tropical Medicine and Hygiene 87(2), 281–291.CrossRefGoogle Scholar
De, NV, Le, TH, Lien, PTH and Eom, KS (2014) Current Status of taeniasis and cysticercosis in Vietnam. The Korean Journal of Parasitology 52(2), 125–129.Google ScholarPubMed
Devleesschauwer, B, Aryal, A, Tharmalingam, J, Joshi, DD, Rijal, S, Speybroeck, N, Gabriël, S, Victor, B and Dorny, P (2013) Complexities in using sentinel pigs to study Taenia solium transmission dynamics under field conditions. Veterinary Parasitology 193(1–3), 172–178.CrossRefGoogle ScholarPubMed
Dorny, P, Phiri, IK, Vercruysse, J, Gabriel, S, Willingham, AL, Brandt, J, Victor, B, Speybroeck, N and Berkvens, D (2004) A Bayesian approach for estimating values for prevalence and diagnostic test characteristics of porcine cysticercosis. International Journal for Parasitology 34(5), 569–576.CrossRefGoogle ScholarPubMed
Eom, KS, Jeon, HK and Rim, HJ (2009) Geographical distribution of Taenia asiatica and related species. The Korean Journal of Parasitology 47, 115–124.CrossRefGoogle ScholarPubMed
Eom, KS, Rim, HJ and Jeon, HK (2020) Taenia asiatica: historical overview of taeniasis and cysticercosis with molecular characterization. Advances in Parasitology 108, 133–173.CrossRefGoogle Scholar
Eom, KS, Jeon, H-K, Kong, Y, et al. (2002) Identification of Taenia asiatica in China: molecular, morphological, and epidemiological analysis of a Luzhai isolate. The Journal of parasitology 88(4), 758–764.CrossRefGoogle ScholarPubMed
Fan, PC, Chung, WC, Lin, CY and Wu, CC (1990) The pig as an intermediate host for Taiwan Taenia infection. Journal of Helminthology 64(3), 223–231.CrossRefGoogle ScholarPubMed
Fan, PC, Chung, WC, Lin, CY and Pawlowski, ZS (1992) Experimental infection with Taenia saginata (Poland strain) in Taiwanese pigs. Journal of Helminthology 66(3), 198–204.CrossRefGoogle ScholarPubMed
Food and Agriculture Organization (FAO) and World Health Organization (WHO) (2012) Multicriteria-based ranking for risk management of foodborne parasites. Microbiological Risk Assessment Series 23., WHO Press, Available at http://www.fao.org/3/a-i3649e.pdf.Google Scholar
Gomez-Puerta, L, Vargas-Calla, A, Castillo, Y, Lopez-Urbina, MT, Dorny, P, Garcia, HH, Gonzalez, AE and O'Neal, SE (2019) Evaluation of cross-reactivity to Taenia hydatigena and Echinococcus granulosus in the enzyme-linked immunoelectrotransfer blot assay for the diagnosis of porcine cysticercosis. Parasites & Vectors 12(1), 1–7.CrossRefGoogle Scholar
GSO (General Statistics Office of Vietnam. Statistical Data) (2019) Available at https://gso.gov.vn/default.aspx?tabid=714 (accessed 22 January 2019) (in Vietnamese).Google Scholar
Hall, T (1999) BioEdit: a user-friendly biological sequence alignment program for windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Huan, LV (1994) Parasitic helminths in pigs in several southern provinces and preventative measures. Hanoi, National Institution of Veterinary Research (in Vietnamese).Google Scholar
Kim, JG, Ahn, CS, Sohn, WM, Nawa, Y and Kong, Y (2018) Human sparganosis in Korea. Journal of Korean Medical Science 33(44), 1–15.CrossRefGoogle ScholarPubMed
Lan, NTK, Quyen, NT and Hoat, PC (2011) Xác định tương quan giữa tỷ lệ nhiễm sán dây Taenia hydatigena trưởng thành ở chó và tỷ lệ nhiễm ấu sán cysticercus tenuicollis ở trâu, bò, lợn - thử nghiệm thuốc tẩy sán dây cho chó. Veterinary Sciences and Techniques 18(6), 60–65 (in Vietnamese, with English abstract).Google Scholar
Lapar, MLA, Toan, NN, Staal, S, Minot, N, Tisdell, C, Que, NN and Tuan, NDA (2012) Smallholder competitiveness: insights from household pig production systems in Vietnam. International Association of Agricultural Economists (IAAE) Triennial Conference, Foz Do Iguaçu, Brazil, 1–27.Google Scholar
Le, TH, Nga, NB, van De, N, Cong, LD and Doanh, NQ (2002) Phát hiện loài sán dây Taenia asiatica ký sinh trên ngươi ở Việt Nam bằng phương pháp giám định sinh học phân tử. Academia Journal of Biology 24(1), 23–29 (in Vietnamese).Google Scholar
Le, AT, Do, LQT, Nguyen, HBT, Nguyen, HNT and Do, AN (2017) Case report: the first case of human infection by adult of Spirometra erinaceieuropaei in Vietnam. BMC Infectious Diseases 17(1), 1–4.CrossRefGoogle ScholarPubMed
Martin, SW, Meek, AH and Willeberg, P (1987) Veterinary epidemiology: principles and methods. Ames, USA, Iowa State University Press, pp. 343.Google Scholar
Michelet, L and Dauga, C (2012) Molecular evidence of host influences on the evolution and spread of human tapeworms. BRV Biological Reviews 87(3), 731–741.CrossRefGoogle ScholarPubMed
Muigg, V, Ruf, MT, Schwarzkopf, S, et al. (2019) Case report: human subcutaneous sparganosis in a Thai migrant. The American Journal of Tropical Medicine and Hygiene 101(5), 1170–1173.CrossRefGoogle Scholar
Ng-Nguyen, D, Stevenson, MA and Traub, RJ (2017) A systematic review of taeniasis, cysticercosis and trichinellosis in Vietnam. Parasites &Vectors 10(1), 1–15.Google ScholarPubMed
Ng-Nguyen, D, Noh, J, Breen, K, Stevenson, MA, Handali, S and Traub, RJ (2018) The epidemiology of porcine Taenia solium cysticercosis in communities of the central highlands in Vietnam. Parasites & Vectors 11(360), 1–8.CrossRefGoogle ScholarPubMed
Nga, NTD, Ninh, HN, Hung, PV and Lapar, ML (2014) Smallholder pig value chain development in Vietnam: situation analysis and trends. Available at https://cgspace.cgiar.org/bitstream/handle/10568/53935/pr_situation_analysis_vietnam_web.pdf?sequence=7. (accessed 2 October 2020).Google Scholar
Nguyen, MTT, Gabriël, S, Abatih, EN and Dorny, P (2016) A systematic review on the global occurrence of Taenia hydatigena in pigs and cattle. Veterinary Parasitology 226, 97–103.CrossRefGoogle ScholarPubMed
Noh, J, Rodriguez, S, Lee, YM, Handali, S, Gonzalez, AE, Gilman, RH, Tsang, VCW, Garcia, HH and Wilkins, PP (2014) Recombinant protein- and synthetic peptide-based immunoblot test for diagnosis of neurocysticercosis. Journal of Clinical Microbiology 52(5), 1429–1434.CrossRefGoogle ScholarPubMed
Polley, LR and Mostert, PE (1980) Ascaris suum in Saskatchewan pigs: an abattoir survey of prevalence and intensity of infection. Canadian Veterinary Journal 21(11), 307–309.Google ScholarPubMed
R Core Team (2020) R: a language and environment for statistical computing. Vienna, Austria, R Foundation for Statistical Computing.Google Scholar
Rodriguez-Hidalgo, R, Geysen, D, Benítez-Ortiz, W, Geerts, S and Brandt, J (2002) Comparison of conventional techniques to differentiate between Taenia solium and Taenia saginata and an improved polymerase chain reaction restriction fragment length polymorphism assay using a mitochondrial 12 rDNA fragment. Journal of Parasitology 88(5), 1007–1011.CrossRefGoogle Scholar
Rodriguez-Hidalgo, R, Benitez-Ortiz, W, Praet, N, Saa, L, Vercruysse, J, Brandt, J and Dorny, P (2006) Taeniasis-cysticercosis in Southern Ecuador: assessment of infection status using multiple laboratory diagnostic tools. Mem Inst Oswaldo Cruz, Rio de Janeiro 101(7), 779–782.CrossRefGoogle ScholarPubMed
SDAH (Sub-department of Animal Health, Vietnam) (2018) Available at https://phutho.gov.vn/vi/tinh-hinh-kinh-te-xa-hoi-nam-2017-tren-dia-ban-tinh-phu-tho (accessed 22 March 2020 (in Vietnamese).Google Scholar
Somers, R, Dorny, P, Geysen, D, Nguyen, LA, Thach, DC, Vercruysse, J and Nguyen, VK (2007) Human tapeworms in north Vietnam. Transactions of the Royal Society of Tropical Medicine and Hygiene 101(3), 275–277.CrossRefGoogle ScholarPubMed
Tang, THC, Wong, SSY, Lai, CKC, et al. (2017) Molecular identification of Spirometra erinaceieuropaei tapeworm in cases of human sparganosis, Hong Kong. Emerging Infectious Diseases 23(4), 665–668.CrossRefGoogle ScholarPubMed
Trieu, HS (2012) Nghiên cứu kiểu gen mầm bệnh lâm sàng, cận lâm sàng, kết quả điều trị sán dây Taenia spp và ấu trùng sán dây lợn trên bệnh nhân tại Viện sốt rét-Ký sinh trùng - côn trùng trung uống 2007–2010. PhD thesis, Hanoi University of Medicine (in Vietnamese).Google Scholar
Trung, DD, Praet, N, Cam, TDT, Lam, BVT, Manh, HN, Gabriãl, S and Dorny, P (2013) Assessing the burden of human cysticercosis in Vietnam. Tropical Medicine & International Health 18(3), 352–356.Google ScholarPubMed
Tsang, VCW, Brand, JA and Boyer, AE (1989) An enzyme-linked immunoelectrotransfer blot assay and glycoprotein antigens for diagnosing human cysticercosis (Taenia solium). The Journal of Infectious Diseases 159, 50–59.CrossRefGoogle Scholar
Vien, HV, Thach, DTC, Thuan, LK, Dung, DT, Tan, HV, Duc, NT and Tuyet, TT (2013) Thực trạng một số yếu tố nguy cơ liên quan nhiễm sán dây và hiệu quả biện pháp phòng chống tại xã Long Cốc, huyện Tân Sơn, tỉnh Phú Thọ. Journal of Malaria and Parasite Diseases Control 6, 60–67 (in Vietnamese).Google Scholar
Vietnam Livestock Production (2018) Biểu đồ sản lượng thịt theo địa phương. Available at http://channuoivietnam.com/bieu-do-thong-ke-san-pham-chan-nuoi/bieu-phan-bo-san-luong-thit-heo-2013/ (accessed 22 March 2020) (in Vietnamese).Google Scholar
World Health Organization (WHO) (2015) Department of Control of Neglected Tropical Diseases: Assembling a framework for intensified control of taeniasis and neurocysticercosis caused by Taenia solium: report of an informal consultation. Geneva, WHO Headquarters, 17–18 July 2014. Ed. B. Abela Ridder. (Accessed 2 October 2020).Google Scholar
World Health Organization (WHO) ( (2015) WHO estimates of the global burden of foodborne diseases. Foodborne diseases burden epidemiology reference group 2007-2015. World Health Organization, pp. 255. www.who.int (accessed on 2 October, 2020).Google Scholar