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Genetic variation of Gongylonema pulchrum from wild animals and cattle in Japan based on ribosomal RNA and mitochondrial cytochrome c oxidase subunit I genes

Published online by Cambridge University Press:  12 September 2012

P. Makouloutou ,
A. Setsuda ,
M. Yokoyama ,
T. Tsuji ,
E. Saita ,
H. Torii ,
Y. Kaneshiro ,
M. Sasaki ,
K. Maeda  and
Y. Une
...Show all authors
P. Makouloutou
Affiliation:
Laboratory of Veterinary Parasitology, Faculty of Agriculture, Yamaguchi University, 1677-1 Yoshida, Yamaguchi753-8515, Japan
A. Setsuda
Affiliation:
Osaka City Government Meat Inspection Centre, 5-2-48 Nanko-minami, Osaka559-0032, Japan
M. Yokoyama
Affiliation:
Nature and Environment Division, Institute of Natural and Environmental Sciences, University of Hyogo, 940 Sawano, Aogaki-cho, Tanba, Hyogo669-3842, Japan Wildlife Management Research Centre, Hyogo Prefecture, 940 Sawano, Aogaki-cho, Tanba, Hyogo669-3842, Japan
T. Tsuji
Affiliation:
Wildlife Management Research Centre, Hyogo Prefecture, 940 Sawano, Aogaki-cho, Tanba, Hyogo669-3842, Japan
E. Saita
Affiliation:
Wildlife Management Research Centre, Hyogo Prefecture, 940 Sawano, Aogaki-cho, Tanba, Hyogo669-3842, Japan
H. Torii
Affiliation:
Nara University of Education, Takabatake-cho, Nara630-8528, Japan
Y. Kaneshiro
Affiliation:
NPO Shikoku Institute of Natural History, 470-1 Shimobu-otsu, Susaki, Kochi785-0023, Japan
M. Sasaki
Affiliation:
Division of Biomedical Science, Department of Basic Veterinary Medicine, Obihiro University of Agriculture and Veterinary Medicine, Inada-cho, Obihiro, Hokkaido080-8555, Japan
K. Maeda
Affiliation:
Laboratory of Microbiology, Faculty of Agriculture, Yamaguchi University1677-1 Yoshida, Yamaguchi753-8515, Japan
Y. Une
Affiliation:
Laboratory of Veterinary Pathology, School of Veterinary Medicine, Azabu University, 1-17-71 Fuchinobe, Sagamihara252-5201, Japan
H. Hasegawa
Affiliation:
Department of Biology, Faculty of Medicine, Oita University, Hasama, Yufu, Oita879-5593, Japan
H. Sato*
Affiliation:
Laboratory of Veterinary Parasitology, Faculty of Agriculture, Yamaguchi University, 1677-1 Yoshida, Yamaguchi753-8515, Japan
*
* E-mail: sato7dp4@yamaguchi-u.ac.jp
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Abstract

The gullet worm (Gongylonema pulchrum) has been recorded from a variety of mammals worldwide, including monkeys and humans. Due to its wide host range, it has been suggested that the worm may be transmitted locally to any mammalian host by chance. To investigate this notion, the ribosomal RNA gene (rDNA), mainly regions of the internal transcribed spacers (ITS) 1 and 2, and a cytochrome c oxidase subunit I (COI) region of mitochondrial DNA of G. pulchrum were characterized using parasites from the following hosts located in Japan: cattle, sika deer, wild boars, Japanese macaques, a feral Reeves's muntjac and captive squirrel monkeys. The rDNA nucleotide sequences of G. pulchrum were generally well conserved regardless of their host origin. However, a few insertions/deletions of nucleotides along with a few base substitutions in the ITS1 and ITS2 regions were observed in G. pulchrum from sika deer, wild boars and Japanese macaques, and those differed from G. pulchrum in cattle, the feral Reeves's muntjac and captive squirrel monkeys. The COI sequences of G. pulchrum were further divided into multiple haplotypes and two groups of haplotypes, i.e. those from a majority of sika deer, wild boars and Japanese macaques and those from cattle and zoo animals, were clearly differentiated. Our findings indicate that domestic and sylvatic transmission cycles of the gullet worm are currently present, at least in Japan.

Type
Research Papers
Information
Journal of Helminthology , Volume 87 , Issue 3 , September 2013 , pp. 326 - 335
Copyright
Copyright © Cambridge University Press 2012 

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References

Alicata, J.E. (1935) Early developmental stages of nematodes occurring in swine. U.S. Department of Agriculture Technical Bulletin 489, 1–96.Google Scholar
Anderson, R.C. (1992) Nematode parasites of vertebrates. Their development and transmission. 578 pp. Oxfordshire, CAB International.Google Scholar
Coombs, D.W. & Springer, M.D. (1974) Parasites of feral pig X: European wild boar hybrids in southern Texas. Journal of Wildlife Diseases 10, 436–441.CrossRefGoogle ScholarPubMed
Crusz, H. & Sivalingam, V. (1950) A note on the occurrence of Gongylonema pulchrum Molin, 1857, in man in Ceylon. Journal of Parasitology 36, 25–26.CrossRefGoogle ScholarPubMed
Eberhard, M.L. & Busillo, C. (1999) Human Gongylonema infection in a resident of New York City. American Journal of Tropical Medicine and Hygiene 61, 51–52.CrossRefGoogle Scholar
Eslami, A. & Farsad-Hamdl, S. (1992) Helminth parasites of wild boar, Sus scrofa, in Iran. Journal of Wildlife Diseases 28, 316–318.CrossRefGoogle ScholarPubMed
Halajian, A., Eslami, A., Salehi, N., Ashraft-Helan, J. & Sato, H. (2010) Incidence and genetic characterization of Gongylonema pulchrum in cattle slaughtered in Mazandaran Province, northern Iran. Iranian Journal of Parasitology 5, 10–18.Google ScholarPubMed
Hara, T., Nozaki, R., Makata, S., Yamada, K., Yoneda, Y. & Takao, Y. (2010) [A human case of gongylonemosis detected by endoscopy]. Clinical Parasitology 20, 58–60(in Japanese).Google Scholar
Haruki, K., Furuya, H., Saito, S., Kamiya, S. & Kagei, N. (2005) Gongylonema infection in man: a first case of gongylonemosis in Japan. Helminthologia 42, 63–66.Google Scholar
Inukai, T. (1952) [The sika deer on Hokkaido and its prosperity and decline]. Hoppo Bunka Kenkyu Houkoku (The Report of Northern Cultural Research of Hokkaido University) 7, 1–45(in Japanese).Google Scholar
Kirkpatrick, C.E., Leiby, D.A., Abraham, D. & Duffy, C.H. III (1986) Gongylonema pulchurm Molin (Nematoda: Gongylonematidae) in black bears (Ursus americanus Pallas) from Pennsylvania. Journal of Wildlife Diseases 22, 119–121.CrossRefGoogle ScholarPubMed
Kitamura, E., Yokohata, Y., Suzuki, M. & Kamiya, M. (1997) Metazoan parasites of sika deer from east Hokkaido, Japan and ecological analyses of their abomasal nematodes. Journal of Wildlife Diseases 33, 278–284.CrossRefGoogle ScholarPubMed
Kudo, N., Oyamada, T. & Ito, K. (1992) Epizootiology of the gullet worm, Gongylonema pulchrum Molin, 1957, from cattle in Aomori Prefecture, Japan. Japanese Journal of Parasitology 41, 266–273(in Japanese with English summary).Google Scholar
Kudo, N., Oyamada, T., Okutsu, M. & Kinoshita, M. (1996) Intermediate hosts of Gongylonema pulchrum Molin, 1957, in Aomori Prefecture, Japan. Japanese Journal of Parasitology 45, 222–229(in Japanese with English summary).Google Scholar
Kudo, N., Koreguchi, T., Ikadai, H. & Oyamada, T. (2003) Experimental infection of laboratory animals and sheep with Gongylonema pulchrum in Japan. Journal of Veterinary Medical Science 65, 921–925.CrossRefGoogle ScholarPubMed
Kudo, N., Kuratomi, K., Hatada, N., Ikadai, H. & Oyamada, T. (2005) Further observations on the development of Gongylonema pulchrum in rabbits. Journal of Parasitology 91, 750–755.CrossRefGoogle ScholarPubMed
Lichtenfels, J.R. (1971) Morphological variation in the gullet nematode, Gongylonema pulchrum Molin, 1857, from eight species of definitive hosts with a consideration of Gongylonema from Macaca spp. Journal of Parasitology 57, 348–355.CrossRefGoogle ScholarPubMed
Lucker, J.T. (1932) Some cross transmission experiments with Gongylonema of ruminant origin. Journal of Parasitology 19, 134–141.CrossRefGoogle Scholar
Nabata, D., Masuda, R. & Takahashi, O. (2004) Bottleneck effects on the sika deer Cervus nippon population in Hokkaido, revealed by ancient DNA analysis. Zoological Science 21, 473–481.CrossRefGoogle ScholarPubMed
Nagata, J., Masuda, R., Tamate, H.B., Hamasaki, S., Ochiai, K., Asada, M., Tatsuzawa, S., Suda, K., Tado, H. & Yoshida, M.C. (1999) Two genetically distinct lineages of the sika deer, Cervus nippon, in Japanese Islands: comparison of mitochondrial D-loop region sequences. Molecular Phylogenetics and Evolution 13, 511–519.CrossRefGoogle ScholarPubMed
Sato, H. (2009) Biology and transmission of the gullet worm (Gongylonema pulchrum Molin, 1857). Yamaguchi Journal of Veterinary Medicine 36, 31–54(in Japanese with English summary).Google Scholar
Sato, H., Une, Y. & Takada, M. (2005) High incidence of the gullet worm, Gongylonema pulchrum, in a squirrel monkey colony in a zoological garden in Japan. Veterinary Parasitology 127, 131–137.CrossRefGoogle Scholar
Sato, H., Suzuki, K., Osanai, A., Kamiya, H. & Furuoka, H. (2006) Identification and characterization of the threadworm, Strongyloides procyonis, from feral raccoons (Procyon lotor) in Japan. Journal of Parasitology 92, 63–68.CrossRefGoogle ScholarPubMed
Schwartz, B. & Lucker, J.T. (1931) Experimental transmission of Gongylonema scutatum to pigs. Journal of Parasitology 18, 46.Google Scholar
Smith, H.M., Davidson, W.R., Nettles, V.F. & Gerrish, R.R. (1982) Parasitisms among wild swine in the south-eastern United States. Journal of American Veterinary Medical Association 181, 1281–1284.Google Scholar
Suzuki, K., Nakamura, K., Takahashi, K. & Seki, N. (1992) Gongylonema pulchrum Molin, 1857 from cattle in Hokkaido. Journal of Japan Veterinary Medical Association 45, 120–124(in Japanese, with English summary).Google Scholar
Tamate, H.B., Tatsuzawa, S., Suda, K., Izawa, M., Doi, T., Sunagawa, K., Miyahira, F. & Tado, H. (1998) Mitochondrial DNA variations in local populations of the Japanese sika deer, Cervus nippon. Journal of Mammalogy 79, 1396–1403.CrossRefGoogle Scholar
Teacher, A.G.F. & Griffiths, D.J. (2011) HapStar: automated haplotype network layout and visualization. Molecular Ecology Resources 11, 151–153.CrossRefGoogle ScholarPubMed
Thompson, J.D., Higgins, D.G. & Gibson, T.J. (1994) CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.CrossRefGoogle ScholarPubMed
Uni, S., Abe, M., Harada, K., Kaneda, K., Kimata, I., Abdelmaksoud, N.M., Takahashi, K., Miyashita, M. & Iseki, M. (1992) New record of Gongylonema pulchrum Molin, 1857 from a new host, Macaca fuscata, in Japan. Annales de Parasitologie Humaine et Comparée (Paris) 67, 221–223.CrossRefGoogle Scholar
Uni, S., Kobayashi, S., Miyashita, M., Kimura, N., Kato, A., Aimi, M., Kimata, I., Iseki, M. & Shoho, C. (1994) Geographic distribution of Gongylonema pulchrum and Gongylonema macrogubernaculum from Macaca fuscata in Japan. Parasite 1, 127–130.CrossRefGoogle ScholarPubMed
Wilson, M.E., Lorente, C.A., Allen, J.E. & Eberhard, M.L. (2001) Gongylonema infection of the mouth in a resident of Cambridge, Massachusetts. Clinical Infectious Diseases 32, 1378–1380.CrossRefGoogle Scholar
Yamada, M., Hosoi, E., Tamate, H.B., Nagata, J., Tatsuzawa, S., Tado, H. & Ozawa, S. (2006) Distribution of two distinct lineages of sika deer (Cervus nippon) on Shikoku Island revealed by mitochondrial DNA analysis. Mammal Study 31, 23–28.CrossRefGoogle Scholar
Yokohata, Y. & Suzuki, S. (1993) The gullet nematode, Gongylonema pulchrum from sika deer, Cervus nippon in Hyogo Prefecture, Japan. Japanese Journal of Parasitiology 42, 440–444.Google Scholar
Zinter, D.E. & Migaki, G. (1970) Gongylonema pulchrum in tongues of slaughtered pigs. Journal of American Veterinary Medical Association 157, 301–303.Google ScholarPubMed