Sub-lineages of Taenia solium Asian Genotype Recorded in North India

Acta Parasitologica - Tập 67 - Trang 1237-1245 - 2022
Pallavi Moudgil1, Ramesh Kumar1, Naresh Jindal1, Aman D. Moudgil2
1Department of Veterinary Public Health and Epidemiology, College of Veterinary Sciences, Lala Lajpat Rai University of Veterinary and Animal Sciences, Hisar, India
2Department of Veterinary Parasitology, College of Veterinary Sciences, Lala Lajpat Rai University of Veterinary and Animal Sciences, Hisar, India

Tóm tắt

Porcine cysticercosis is a neglected zoonotic disease of significant veterinary and medical importance owing to its economic impact and public health significance. The present study aimed at genetic characterization of Taenia solium metacestodes in slaughtered pigs of Haryana (North India). A total of 213 (160 and 53 from Chandigarh and Hisar, respectively) slaughtered pigs intended for human consumption were screened for the presence of T. solium metacestodes. The retrieved metacestodes were confirmed molecularly based on the partial amplification of mitochondrial cytochrome c oxidase subunit 1 (CO1) gene. Evolutionary divergence, haplotype and nucleotide diversities and neutrality indices of the retrieved isolates were also assessed. Out of the 213 pigs, 2 (0.94%) revealed the presence of metacestodes involving 1 pig each from Chandigarh (0.62%) and Hisar (1.9%). The sequences obtained after custom sequencing were submitted to GenBank under the accession numbers LC661682-83. The present study haplotype clustered with haplotypes of Asian origin and showed variation from other haplotypes by 1–23 mutational steps. However, the present study isolates also showed nucleotide polymorphisms (A198T, A199G, A201T, G204A, T206A, C210T, T212G, T213A, T216G/A, T217C, T221C, C524T, G994A) at different positions, which indicated the presence of sub-lineages. Low nucleotide diversity (π = 0.020) and negative value of Tajima’s D (− 1.304) observed for the haplotypes under consideration was indicative of purifying selection and recent population expansion. Our study confirms the circulation of T. solium Asian genotype (with distinct sub-lineages) in study area and recommends strict control measures to contain the zoonotic disease.

Tài liệu tham khảo

Singh SP, Singh BB, Kalambhe DG, Pathak D, Aulakh RS, Dhand NK (2018) Prevalence and distribution of Taenia solium cysticercosis in naturally infected pigs in Punjab, India. PLoS Negl Trop Dis 12(11):e0006960. https://doi.org/10.1371/journal.pntd.0006960 Meester M, Swart A, Deng H, van Roon A, Trevisan C, Dorny P, Gabriel S, Vieria-Pinto M, Johansen MV, van der Geissen J (2019) A quantitative risk assessment for human Taenia solium exposure from home slaughtered pigs in European countries. Parasite Vectors 12:82. https://doi.org/10.1186/s13071-019-3320-3 Satyaprakash K, Khan WA, Chaudhari SP, Shinde SV, Kurkure NV, Kolte SW (2018) Pathological and molecular identification of porcine cysticercosis in Maharashtra, India. Acta Parasitol 63(4):784–790. https://doi.org/10.1515/ap-2018-0094 Braae UC, Saarnak CF, Mukaratirwa S, Devleesschauwer B, Magnussen P, Johansen MV (2015) Taenia solium taeniosis/cysticercosis and the co-distribution with schistosomiasis in Africa. Parasite Vectors 8:323. https://doi.org/10.1186/s13071-015-0938-7 Braae UC, Devleesschauwer B, Sithole F, Wang Z, Willingham AL (2017) Mapping occurrence of Taenia soliumtaeniosis/cysticercosis and areas at risk of porcine cysticercosis in Central America and the Caribbean basin. Parasite Vectors 10:424. https://doi.org/10.1186/s13071-017-2362-7 Singh BB, Sharma R, Sharma JK, Juyal PD (2010) Parasitic zoonoses in India: an overview. Rev Sci Tech 29:629–637. https://doi.org/10.20506/rst.29.3.2007 Trevisan C, Devleesschauwer B, Schmidt V, Winkler AS, Harrison W, Johansen MV (2017) The societal cost of Taenia solium cysticercosis in Tanzania. Acta Trop 65:141–154. https://doi.org/10.1016/j.actatropica.2015.12.021 Zoli A, Shey-Njila O, Assana E, Nguekam J, Dorny P, Brandt J, Geerts S (2003) Regional status, epidemiology and impact of Taenia solium cysticercosis in western and central Africa. Acta Trop 87:35–42. https://doi.org/10.1016/s0001-706x(03)00053-6 Gweba M, Faleke O, Junaidu A (2010) Some risk factors for Taenia solium cysticercosis in semi intensively raised pigs in Zuru, Nigeria. Vet Ital 46(1):57–67 Sikasunge CS, Phiri IK, Phiri AM, Dorny P, Siziya S, Willingham AL 3rd (2007) Risk factors associated with porcine cysticercosis in selected districts of Eastern and Southern provinces of Zambia. Vet Parasitol 143(1):59–66. https://doi.org/10.1016/j.vetpar.2006.07.023 Chembensofu M, Mwape KE, Van Damme I, Hobbs E, Phiri IK, Masuku M, Zulu G, Colston A, Willingham AL, Devleesschauwer B, Van Hul A, Chota A, Speybroeck N, Berkvens D, Dorny P, Gabriël S (2017) Re-visiting the detection of porcine cysticercosis based on full carcass dissections of naturally Taenia solium infected pigs. Parasite Vectors 10:572. https://doi.org/10.1186/s13071-017-2520-y Mital AK, Choudhary P, Jain RB (2020) Prevalence and risk factors for neurocysticercosis in children with a first-onset seizure in rural North India. Paediatr Int Child Health 40(3):158–165. https://doi.org/10.1080/20469047.2020.1739381 Devi KR, Borbora D, Upadhyay N, Goswami D, Rajguru SK, Narain K (2021) Neurocysticercosis in patients with active epilepsy in the tea garden community of Assam, Northeast India. Sci Rep 11:7433. https://doi.org/10.1038/s41598-021-86823-w Goel D, Dhanai JS, Agarwal A, Mehlotra V, Saxena V (2011) Neurocysticercosis and its impact on crude prevalence rate of epilepsy in an Indian community. Neurol India 59:37–40. https://doi.org/10.4103/0028-3886.76855 Sahu PS, Patro S, Jena PK, Swain SK, Das BK (2015) Imaging and serological-evidence of neurocysticercosis among patients with seizures in Odisha, an unexplored eastern coastal province in India. J Clin Diagn Res 9(5):DC06-DC10. https://doi.org/10.7860/JCDR/2015/12609.5967 Pradhan S, Kumar R, Gupta RK (2003) Intermittent symptoms in neurocysticercosis: could they be epileptic? Acta Neurol Scand 107(4):260–266. https://doi.org/10.1034/j.1600-0404.2003.01380.x Singh G, Bawa J, Chinna D, Chaudhary A, Saggar K, Modi M, Sander JW (2012) Association between epilepsy and cysticercosis and toxocariasis: a population-based case–control study in a slum in India. Epilepsia 53:2203–2208. https://doi.org/10.1111/epi.12005 Raina SK, Razdan S, Pandita KK, Sharma R, Gupta VP, Razdan S (2012) Active epilepsy as indicator of neurocysticercosis in rural northwest India. Epilepsy Res Tret. https://doi.org/10.1155/2012/802747 Kumari A, Kumar R (2019) Neurocysticercosis-clinical and radiological appraisal from a tertiary centre of Bihar, India. J Med Sci Clin Res 7(1):961–964. https://doi.org/10.18535/jmscr/v7i1.169 Singh BB, Khatkar MS, Gill JP, Dhand NK (2017) Estimation of the health and economic burden of neurocysticercosis in India. Acta Trop 165:161–169. https://doi.org/10.1016/j.actatropica.2016.01.017 Braae UC, Hung NM, Satrija F, Khieu V, Zhou XN, Willingham AL (2018) Porcine cysticercosis (Taenia solium and Taenia asiatica): mapping occurrence and areas potentially at risk in East and Southeast Asia. Parasit Vectors 11:613. https://doi.org/10.1186/s13071-018-3203-z Thakur R, Singh BB, Jindal P, Aulakh RS, Gill JPS (2018) The Clean India Mission: public and animal health benefits. Acta Trop 186:5–15. https://doi.org/10.1016/j.actatropica.2018.06.024 Yamasaki H, Allan JC, Sato MO, Nakao M, Sako Y, Nakaya K, Qiu D, Marnuti W, Craig PS, Ito A (2004) A differential diagnosis of taeniasis and cysticercosis by multiplex PCR. J Clin Microbiol 42(2):548–553. https://doi.org/10.1128/JCM.42.2.548-553.2004 Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98 Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096 Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbour-joining method. Proc Natl Acad Sci USA 101:11030–11035. https://doi.org/10.1073/pnas.0404206101 Bandelt H, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48. https://doi.org/10.1093/oxfordjournals.molbev.a026036 Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595. https://doi.org/10.1093/genetics/123.3.585 Sharma M, Devi KR, Sehgal R, Narain K, Mahanta J, Malla N (2014) Genetic similarity between Taenia solium cysticerci collected from the two distant endemic areas in North and North East India. Infect Genet Evol 21:436–439. https://doi.org/10.1016/j.meegid.2013.12.010 Mohan VR, Tharmalingam J, Muliyil J, Oommen A, Dorny P, Vercruysse J, Vedantam R (2013) Prevalence of porcine cysticercosis in Vellore, South India. Trans R Soc Trop Med Hyg 107:62–64. https://doi.org/10.1093/trstmh/trs003 Chawhan P, Singh B, Sharma R, Gill PS (2015) Prevalence and molecular epidemiology of porcine cysticercosis in naturally infected pigs (Sus scrofa) in Punjab. India Rev Sci Tech 34(3):953–960. https://doi.org/10.20506/rst.34.3.2408 Vaıdya V, Paturkar A, Zende R, Gatne M, Dıghe D, Waghmare R, Moon S, Bhave S, Jadhav P, Wavhal N (2018) Scenario of porcine cysticercosis and human taeniasis in Maharashtra State. India Turk J Vet Anim Sci 42(4):353–358 Sreedevi C, Hafeez M, Putcha AK, Vukka RC, Kothapalli SV, Krovvidi S (2012) PCR test for detecting Taenia solium cysticercosis in pig carcasses. Trop Anim Health Prod 44:95–99. https://doi.org/10.1007/s11250-011-9893-2 Campbell G, Garcia H, Nakao M, Ito A (2006) Genetic variation in Taenia solium. Parasitol Int 55:S121–S126. https://doi.org/10.1016/j.parint.2005.11.019 Jacob SS, Sengupta PP, Chandu AGS, Shamshad S, Yogisharadhya R, Sudhagar S, Ramesh P (2021) Existence of genetic lineages within Asian genotype of Taenia solium—genetic characterization based on mitochondrial and ribosomal DNA markers. Transbound Emerg Dis. https://doi.org/10.1111/tbed.14227 Nakao M, Okamoto M, Sako Y, Yamasaki H, Nakaya K, Ito A (2002) A phylogenetic hypothesis for the distribution of two genotypes of the pig tapeworm Taenia solium worldwide. Parasitology 124(6):657–662. https://doi.org/10.1017/s0031182002001725 Michelet L, Carod JF, Rakontondrazaka M, Ma L, Gay F, Dauga C (2010) The pig tapeworm Taenia solium, the cause of cysticercosis: biogeographic (temporal and spacial) origins in Madagascar. Mol Phylogenet Evol 55(2):744–750. https://doi.org/10.1016/j.ympev.2010.01.008 Yanagida T, Carod JF, Sako Y, Nakao M, Hoberg EP, Ito A (2014) Genetics of the pig tapeworm in Madagascar reveal a history of human dispersal and colonization. PLoS ONE 9(10):e109002. https://doi.org/10.1371/journal.pone.0109002 Solano D, Navarro JC, León-Reyes A, Benítez-Ortiz W, Rodríguez-Hidalgo R (2016) Molecular analyses reveal two geographic and genetic lineages for tapeworms, Taenia solium and Taenia saginata, from Ecuador using mitochondrial DNA. Exp Parasitol 171:49–56. https://doi.org/10.1016/j.exppara.2016.10.015 Hancock K, Broughel DE, Moura INS, Khan A, Pieniazek NJ, Gonzalez AE, Garcia HH, Gilman RH, Tsang VCW (2001) Sequence variation in the cytochrome oxidase I, internal transcribed spacer 1, and Ts14 diagnostic antigen sequences of Taenia solium isolates from South and Central America, India, and Asia. Int J Parasitol 31(14):1601–1607 Moudgil AD, Nehra AK, Nehra V, Sharma R, Vohra S, Moudgil P (2021) Phylogenetics and pathology of hydatid disease in slaughtered buffaloes of north India. Acta Parasitol 66(3):899–906. https://doi.org/10.1007/s11686-021-00348-w Michelet L, Dauga C (2012) Molecular evidence of host influences on the evolution and spread of human tapeworms. Biol Rev 87:731–741. https://doi.org/10.1111/j.1469-185X.2012.00217.x