Hostname: page-component-8448b6f56d-jr42d Total loading time: 0 Render date: 2024-04-23T12:04:07.345Z Has data issue: false hasContentIssue false
  • English
  • Français

Presence of three distinct genotypes within the Paragonimus westermani complex in northeastern India

Published online by Cambridge University Press:  24 August 2012

K. REKHA DEVI ,
KANWAR NARAIN ,
JAGADISH MAHANTA ,
TULIKA NIRMOLIA ,
DAVID BLAIR ,
SIDHARTHA P. SAIKIA  and
TAKESHI AGATSUMA
K. REKHA DEVI
Affiliation:
Department of Environmental Health Sciences, Kochi Medical School, Oko, Nankoku City, Kochi 783-8505, Japan Regional Medical Research Centre, N.E. Region (Indian Council of Medical Research), Post Box #105, Dibrugarh 786 001, Assam, India
KANWAR NARAIN
Affiliation:
Regional Medical Research Centre, N.E. Region (Indian Council of Medical Research), Post Box #105, Dibrugarh 786 001, Assam, India
JAGADISH MAHANTA
Affiliation:
Regional Medical Research Centre, N.E. Region (Indian Council of Medical Research), Post Box #105, Dibrugarh 786 001, Assam, India
TULIKA NIRMOLIA
Affiliation:
Regional Medical Research Centre, N.E. Region (Indian Council of Medical Research), Post Box #105, Dibrugarh 786 001, Assam, India
DAVID BLAIR
Affiliation:
School of Marine and Tropical Biology, James Cook University, Townsville, Queensland 4811, Australia
SIDHARTHA P. SAIKIA
Affiliation:
Regional Medical Research Centre, N.E. Region (Indian Council of Medical Research), Post Box #105, Dibrugarh 786 001, Assam, India
TAKESHI AGATSUMA*
Affiliation:
Department of Environmental Health Sciences, Kochi Medical School, Oko, Nankoku City, Kochi 783-8505, Japan
*
*Corresponding author: Department of Environmental Health Sciences, Kochi Medical School, Oko, Nankoku City, Kochi 783-8505, Japan. Fax: +81 88 880 2535. E-mail: agatsuma@kochi-u.ac.jp
Get access Rights & Permissions [Opens in a new window]

Summary

The name Paragonimus westermani (Kerbert, 1878) is commonly applied to members of a species complex that includes the well-known Asian lung fluke of medical and veterinary importance. Unambiguous molecular and morphological evidence showing the presence of a member of the complex in India has recently been published. In the present study we report the occurrence of 2 more members of the P. westermani complex in northeastern (NE) India. Surveys of the freshwater crabs Maydelliatelphusa lugubris in NE India revealed 2 morphologically distinct types of lung fluke metacercariae. Phylogenetic analyses, using DNA sequences from ITS2, 28S and cox1 gene regions indicate that these lung metacercariae belong to P. westermani complex. Type 1 metacercariae have a more basal position within the complex whereas type 2 metacercariae are closely related to the relatively derived forms of P. westermani from NE Asia (Japan, Korea, China) and Vietnam. A third type of metacercaria (type 3), detected in another crab host, Sartoriana spinigera in Assam, was phylogenetically close to P. siamensis, also a member of the P. westermani group. Molecular evidence has demonstrated the existence of 3 genotypes of lung flukes within the Paragonimus westermani complex in NE India. Two of these were previously unknown.

Keywords

Paragonimus westermani complexlung flukesIndia
Type
Research Article
Information
Parasitology , Volume 140 , Issue 1 , January 2013 , pp. 76 - 86
Copyright
Copyright © Cambridge University Press 2012

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

REFERENCES

Binchai, S., Rangsiruji, A., Ketudat, P., Morishima, Y. and Sugiyama, H. (2007). Molecular systematics of a new form of Paragonimus westermani discovered in Thailand. SE. Asian Journal of Tropical Medicine and Public Health 38 (Suppl. 1), 92–96.Google Scholar
Blair, D., Agatsuma, T. and Wang, W. (2007). Paragonimiasis. In World Class Parasites: Food-borne Parasitic Zoonoses: Fish and Plant-Borne Parasites, Vol. 11 (ed. Murrell, K. D. and Fried, B.), pp. 117–150. Springer Sciences + Business Media, LLG, New York, USA.CrossRefGoogle Scholar
Blair, D., Agatsuma, T., Watanobe, T., Okamoto, M. and Ito, A. (1997). Geographical genetic structure within the human lung fluke, Paragonimus westermani, detected from DNA sequences. Parasitology 115, 411–417.CrossRefGoogle ScholarPubMed
Blair, D., Davis, G. M. and Wu, B. (2001). Evolutionary relationships between trematodes and snails emphasizing schistosomes and paragonimids. Parasitology 123 (Suppl.), S229–S243.CrossRefGoogle ScholarPubMed
Blair, D., Xu, Z. B. and Agatsuma, T. (1999). Paragonimiasis and the genus Paragonimus. Advances in Parasitology 42, 113–222.CrossRefGoogle ScholarPubMed
Bowles, J., Blair, D. and McManus, D. P. (1995 a). A molecular phylogeny of the genus Echinococcus. Parasitology 110, 317–328.CrossRefGoogle ScholarPubMed
Bowles, J., Blair, D. and McManus, D. P. (1995 b). A molecular phylogeny of the human schistosomes. Molecular Phylogenetics and Evolution 4, 103–109. doi: 10.1006/mpev.1995.1011.CrossRefGoogle ScholarPubMed
Devi, K. R., Narain, K., Agatsuma, T., Blair, D., Nagataki, M., Wickramasinghe, S., Yatawara, L. and Mahanta, J. (2010). Morphological and molecular characterization of Paragonimus westermani in northeastern India. Acta Tropica 116, 31–38. doi: 10.1016/j.actatropica.2010.05.003.CrossRefGoogle ScholarPubMed
Devi, K. R., Narain, K., Bhattacharya, S., Negmu, K., Agatsuma, T., Blair, D., Wickramashinghe, S. and Mahanta, J. (2007). Pleuropulmonary paragonimiasis due to Paragonimus heterotremus: molecular diagnosis, prevalence of infection and clinicoradiological features in an endemic area of northeastern India. Transactions of the Royal Society of Tropical Medicine and Hygiene 101, 786–792. doi: 10.1016/j.trstmh.2007.02.028.CrossRefGoogle Scholar
Doanh, P. N., Dung do, T., Thach, D. T., Horii, Y., Shinohara, A. and Nawa, Y. (2011). Human paragonimiasis in Viet Nam: epidemiological survey and identification of the responsible species by DNA sequencing of eggs in patients’ sputum. Parasitology International 60, 534–537. doi: 10.1016/j.parint.2011.09.001.CrossRefGoogle ScholarPubMed
Doanh, P. N., Shinohara, A., Horii, Y., Habe, S. and Nawa, Y. (2009). Discovery of Paragonimus westermani in Vietnam and its molecular phylogenetic status in P. westermani complex. Parasitolology Research 104, 1149–1155. doi: 10.1007/s00436-008-1302-z.CrossRefGoogle ScholarPubMed
Doanh, P. N., Shinohara, A., Horii, Y., Habe, S., Nawa, Y. and Le, N. T. (2007 a). Description of a new lung fluke species, Paragonimus vietnamensis sp. nov. (Trematoda, Paragonimidae), found in northern Vietnam. Parasitology Research 101, 1495–1501. doi: 10.1007/s00436-007-0666-9.CrossRefGoogle ScholarPubMed
Doanh, P. N., Shinohara, A., Horii, Y., Habe, S., Nawa, Y. and Le, N. T. (2008). Discovery of Paragonimus proliferus in Northern Vietnam and their molecular phylogenetic status among genus Paragonimus. Parasitology Research 102, 677–683. doi: 10.1007/s00436-007-0811-5.CrossRefGoogle ScholarPubMed
Doanh, P. N., Shinohara, A., Horii, Y., Habe, S., Nawa, Y., The, D. T. and Le, N. T. (2007 b). Morphological and molecular identification of two Paragonimus spp., of which metacercariae concurrently found in a land crab, Potamiscus tannanti, collected in Yenbai Province, Vietnam. Parasitology Research 100, 1075–1082. doi: 10.1007/s00436-006-0411-9.CrossRefGoogle Scholar
Drummond, A. J., Ashton, B., Buxton, S., Cheung, M., Cooper, A., Duran, C., Field, M., Heled, J., Kearse, M., Markowitz, S., Moir, R., Stones-Havas, S., Sturrock, S., Thierer, T. and Wilson, A. (2011). Geneious Pro. v5.4.6, available from http://www.geneious.com/.Google Scholar
Iwagami, M., Ho, L. Y., Su, K., Lai, P. F., Fukushima, M., Nakano, M., Blair, D., Kawashima, K. and Agatsuma, T. (2000). Molecular phylogeographic studies on Paragonimus westermani in Asia. Journal of Helminthology 74, 315–322.CrossRefGoogle ScholarPubMed
Iwagami, M., Rajapakse, R. P., Paranagama, W., Okada, T., Kano, S. and Agatsuma, T. (2008). Ancient divergence of Paragonimus westermani in Sri Lanka. Parasitology Research 102, 845–852. doi: 10.1007/s00436-007-0820-4.CrossRefGoogle ScholarPubMed
Kannangara, D. W. D. and Karunaratne, G. M. S. (1969). Paragonimus siamensis – the fourth lung fluke reported from Ceylon. Ceylon Journal of Medical Science 18, 61–65.Google Scholar
Keiser, J. and Utzinger, J. (2009). Food-borne trematodiases. Clinical Microbiology Reviews 22, 466–483. doi: 10.1128/CMR.00012-09.CrossRefGoogle ScholarPubMed
Littlewood, D. T. and Johnston, D. A. (1995). Molecular phylogenetics of the four Schistosoma species groups determined with partial 28S ribosomal RNA gene sequences. Parasitology, 111, 167–175.CrossRefGoogle ScholarPubMed
Minin, V., Abdo, Z., Joyce, P. and Sullivan, J. (2003). Performance-based selection of likelihood models for phylogeny estimation. Systematic Biology 52, 674–683.CrossRefGoogle ScholarPubMed
Miyazaki, I. (1974). Lung flukes in the world – morphology and life history. In A Symposium on Epidemiology of Parasitic Diseases (ed. Sasa, M., Tanaka, H. and Kurihara, T.), pp. 101–135. International Medical Foundation of Japan, Tokyo, Japan.Google Scholar
Miyazaki, I. (1981). Taxonomical studies of the lung fluke occurring in the Philippines. Medical Bulletin of the Fukuoka University 8, 153–158.Google Scholar
Miyazaki, I. and Wykoff, D. E. (1965). On a new lung fluke, Paragonimus siamensis n.sp. found in Thailand (Trematoda: Troglotrematidae). Japanese Journal of Parasitology 14, 251–257.Google Scholar
Posada, D. and Crandall, K. A. (2001). Selecting the best-fit model of nucleotide substitution. Systematic Biology 50, 580–601.CrossRefGoogle ScholarPubMed
Singh, T. S., Sugiyama, H., Umehara, A., Hiese, S. and Khalo, K. (2009). Paragonimus heterotremus infection in Nagaland: A new focus of Paragonimiasis in India. Indian Journal of Medical Microbiology 27, 123–127. doi: 10.4103/0255-0857.49424.CrossRefGoogle ScholarPubMed
Sripa, B., Kaewkes, S., Intapan, P. M., Maleewong, W. and Brindley, P. J. (2010). Food-borne trematodiases in Southeast Asia epidemiology, pathology, clinical manifestation and control. Advances in Parasitology 72, 305–350. doi: 10.1016/S0065-308X(10)72011-X.CrossRefGoogle ScholarPubMed
Sugiyama, H., Morishima, Y., Binchai, S., Rangsiruji, A. and Ketudat, P. (2007). New form of Paragonimus westermani discovered in Thailand: morphological characteristics and host susceptibility. The Southeast Asian Journal of Tropical Medicine and Public Health 38 (Suppl. 1), 87–91.Google Scholar
Sugiyama, H., Sonoda, J., Tomimura, T. and Nishida, H. (1983). Studies on the geographical distribution of the lung fluke, Paragonimus westermani (Kerbert, 1878) in the southern Prefectures of the Kinki District, Japan: observations on the incidence of encysted larvae of P. westermani in Geothelphusa dehaani in Higashi-Yoshino area, Nara Prefecture. Nippon juigaku zasshi. The Japanese Journal of Veterinary Science 45, 227–236.CrossRefGoogle Scholar
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739. doi: 10.1093/molbev/msr121.CrossRefGoogle ScholarPubMed
Tandon, V., Prasad, P. K., Chatterjee, A. and Bhutia, P. T. (2007). Surface fine topography and PCR-based determination of metacercaria of Paragonimus sp. from edible crabs in Arunachal Pradesh, Northeast India. Parasitology Research 102, 21–28. doi: 10.1007/s00436-007-0715-4.CrossRefGoogle ScholarPubMed
Toscano, C., Yu, S. H., Nunn, P. and Mott, K. E. (1995). Paragonimiasis and tuberculosis, diagnostic confusion: a review of the literature. Tropical Diseases Bulletin 92, R1–R26.Google Scholar
Xia, X. and Xie, Z. (2001). DAMBE: software package for data analysis in molecular biology and evolution. The Journal of Heredity 92, 371–373.CrossRefGoogle ScholarPubMed
Yaemput, S., Dekumyoy, P. and Visiassuk, K. (1994). The natural first intermediate host of Paragonimus siamensis (Miyazaki and Wykoff, 1965) in Thailand. The Southeast Asian Journal of Tropical Medicine and Public Health 25, 284–290.Google ScholarPubMed