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First molecular identification of Strongyloides fuelleborni in long-tailed macaques in Thailand and Lao People's Democratic Republic reveals considerable genetic diversity

Published online by Cambridge University Press:  20 July 2018

T. Thanchomnang
Affiliation:
Faculty of Medicine, Mahasarakham University, Maha Sarakham 44000, Thailand
P.M. Intapan
Affiliation:
Department of Parasitology, Faculty of Medicine, and Research and Diagnostic Center for Infectious Diseases, Khon Kaen University, 40002, Thailand
O. Sanpool
Affiliation:
Department of Parasitology, Faculty of Medicine, and Research and Diagnostic Center for Infectious Diseases, Khon Kaen University, 40002, Thailand
R. Rodpai
Affiliation:
Department of Parasitology, Faculty of Medicine, and Research and Diagnostic Center for Infectious Diseases, Khon Kaen University, 40002, Thailand
L. Sadaow
Affiliation:
Department of Parasitology, Faculty of Medicine, and Research and Diagnostic Center for Infectious Diseases, Khon Kaen University, 40002, Thailand
I. Phosuk
Affiliation:
Faculty of Public Health Program, Mahidol University, Amnajcharoen Campus, Amnajcharoen 37000, Thailand
C. Somboonpatarakun
Affiliation:
Department of Parasitology, Faculty of Medicine, and Research and Diagnostic Center for Infectious Diseases, Khon Kaen University, 40002, Thailand
S. Laymanivong
Affiliation:
Centre of Malariology, Parasitology and Entomology, Ministry of Health, Vientiane, Lao PDR
S. Tourtip
Affiliation:
Faculty of Medicine, Mahasarakham University, Maha Sarakham 44000, Thailand
W. Maleewong*
Affiliation:
Department of Parasitology, Faculty of Medicine, and Research and Diagnostic Center for Infectious Diseases, Khon Kaen University, 40002, Thailand
*
Author for correspondence: W. Maleewong, Fax.: +66-43-202475, E-mail: wanch_ma@kku.ac.th

Abstract

Strongyloides fuelleborni is a soil-transmitted nematode parasite of non-human primates. The worm is prevalent also in human populations in Africa and South-East Asia. In this study, we amplified and sequenced a portion of the 18S ribosomal RNA gene (rRNA) and of the mitochondrial cytochrome c oxidase subunit 1 (cox1) gene of Strongyloides adult males recovered from faecal samples from long-tailed macaques (Macaca fascicularis) in Thailand and Lao PDR. The prevalence in Thailand was 31.1% (55/177) and in Lao PDR it was 62.1% (41/66), with an overall prevalence of 39.5% (96/243). All 18S rRNA sequences that we obtained (n = 96) showed 100% identity with published S. fuelleborni sequences. The 96 cox1 sequences that we obtained represented 32 new haplotypes. When included with the 17 previously known haplotypes from S. fuelleborni, the cox1 sequences fell into four clusters, which had clear geographical structure. This is the first molecular confirmation of S. fuelleborni in long-tailed macaques in Thailand and Lao PDR. Clearly, awareness needs to be raised of the zoonotic potential of S. fuelleborni. A monitoring programme should be organized, taking into account the role of reservoir hosts (i.e. monkeys) in the natural background of human strongyloidiasis caused by S. fuelleborni.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2018 

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References

Ashford, RW, Barnish, G and Viney, ME (1992) Strongyloides fuelleborni kellyi: infection and disease in Papua New Guinea. Parasitology Today 8, 314318.Google Scholar
Eudey, AA (2008) The crab-eating macaque (Macaca fascicularis): widespread and rapidly declining. Primate Conservation 23, 129132.Google Scholar
Fooden, J (1995) Systematic review of Southeast Asia long tail macaques, Macaca fascicularis (Raffles, 1821). Fieldiana Zoology 81, 1206.Google Scholar
Grove, DI (1989) Clinical manifestations. In Grove, DI (ed.), Strongyloidiasis—A Major Roundworm Infection of Man. London: Taylor & Francis, pp. 155173.Google Scholar
Hall, TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 9598.Google Scholar
Hasegawa, H et al. (2010) Molecular identification of the causative agent of human strongyloidiasis acquired in Tanzania: dispersal and diversity of Strongyloides spp. and their hosts. Parasitology International 59, 407413.Google Scholar
Hasegawa, H et al. (2016) Strongyloides infections of humans and great apes in Dzanga-Sangha Protected Areas, Central African Republic and in degraded forest fragments in Bulindi, Uganda. Parasitology International 65, 367370.Google Scholar
Jaleta, TG et al. (2017) Different but overlapping populations of Strongyloides stercoralis in dogs and humans. Dogs as a possible source for zoonotic strongyloidiasis. PLOS Neglected Tropical Diseases 11, e0005752.Google Scholar
Kimura, M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111120.Google Scholar
Koga, K et al. (1991) A modified agar plate method for detection of Strongyloides stercoralis. American Journal of Tropical Medicine and Hygiene 45, 518521.Google Scholar
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 18701874.Google Scholar
Labes, EM et al. (2011) Genetic characterization of Strongyloides spp. from captive, semi-captive and wild Bornean orangutans (Pongo pygmaeus) in Central and East Kalimantan, Borneo, Indonesia. Parasitology 138, 14171422.Google Scholar
Laymanivong, S et al. (2016) First molecular identification and report of genetic diversity of Strongyloides stercoralis, a current major soil-transmitted helminth in humans from Lao People's Democratic Republic. Parasitology Research 115, 29732980.Google Scholar
Librado, P and Rozas, J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 14511452.Google Scholar
Malaivijitnond, S and Hamada, Y (2008) Current situation and status of long-tailed macaques (Macaca fascicularis) in Thailand. Natural History Journal of Chulalongkorn University 8, 185204.Google Scholar
Nagayasu, E et al. (2017) A possible origin population of pathogenic intestinal nematodes, Strongyloides stercoralis, unveiled by molecular phylogeny. Scientific Reports 7, 4844.Google Scholar
Pampiglione, S and Ricciardi, ML (1971) The presence of Strongyloides fülleborni von Linstow, 1905, in man in Central and East Africa. Parassitologia 13, 257269.Google Scholar
Prasongdee, TK et al. (2017) An eleven-year retrospective hospital-based study of epidemiological data regarding human strongyloidiasis in northeast Thailand. BioMed Central Infectious Diseases 17, 627.Google Scholar
Ronquist, F et al. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539542.Google Scholar
Sandground, JH (1925) Speciation and specificity in the nematode genus Strongyloides. The Journal of Parasitology 12, 5980.Google Scholar
Schad, GA (1989) Morphology and life history of Strongyloides stercoralis. In Grove, DI (ed.), Strongyloidiasis: A Major Roundworm Infection of Man. London: Taylor & Francis, pp. 85104.Google Scholar
Speare, R (1989) Identification of species of Strongyloides. In Grove, DI (ed.), Strongyloidiasis: A Major Roundworm Infection of Man. London: Taylor & Francis, pp. 1184.Google Scholar
Thanchomnang, T et al. (2017) First molecular identification and genetic diversity of Strongyloides stercoralis and Strongyloides fuelleborni in human communities having contact with long-tailed macaques in Thailand. Parasitology Research 6, 19171923.Google Scholar
Wenz-Mücke, A et al. (2013) Human contact influences the foraging behaviour and parasite community in long-tailed macaques. Parasitology 140, 709718.Google Scholar