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Gut Pathogens
Published in: Gut Pathogens 1/2017

Open Access 01-12-2017 | Research

Helicobacter pylori virulence genes of minor ethnic groups in North Thailand

Authors: Phawinee Subsomwong, Muhammad Miftahussurur, Ratha-korn Vilaichone, Thawee Ratanachu-ek, Rumiko Suzuki, Junko Akada, Tomohisa Uchida, Varocha Mahachai, Yoshio Yamaoka

Published in: Gut Pathogens | Issue 1/2017

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Abstract

Background

There are few studies analyzed concurrently the prevalence and genotypes of Helicobacter pylori infection with the ancestor origins from different ethnics, especially with including minority groups. We recruited a total of 289 patients in MaeSot, Thailand (154 Thai, 14 Thai-Chinese, 29 Karen and 92 Hmong ethnics). The virulence genes and genealogy of the strains were determined by PCR-based sequencing.

Results

Based on culture and histology/immunohistochemistry, the prevalence of H. pylori infection was 54.5% (158/289). Among 152 isolates cultured, the East-Asian-type cagA was predominant genotype among strains from Hmong, Thai-Chinese and Thai (96.0% [48/50], 85.7% [6/7] and 62.7% [47/75], respectively), whilst majority of strains from Karen had Western-type cagA (73.3% [11/15]). Patients infected with the East-Asian-type cagA strains had significantly higher activity and intestinal metaplasia in the antrum and activity in the corpus than those with Western-type cagA (P = 0.024, 0.006 and 0.005, respectively). The multilocus sequencing typing analysis discriminated that most strains from Hmong and Thai-Chinese belonged to hspEAsia (92.0 and 85.7%, respectively), whereas strains from Karen predominantly possessed hpAsia2 (86.7%) and strains from Thai were classified into hspEAsia (45.2%) and hpAsia2 (31.1%).

Conclusions

Helicobacter pylori genotypes were relatively different among ethnic groups in Thailand and were associated with the source of ancestor even living in a small rural town. Caution and careful check-up are required especially on Hmong ethnic associated with high prevalence of virulence genotypes of H. pylori.
Appendix
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Literature
1.
2.
de Martel C, Forman D, Plummer M. Gastric cancer: epidemiology and risk factors. Gastroenterol Clin North Am. 2013;42:219–40.CrossRefPubMed
3.
Suzuki R, Shiota S, Yamaoka Y. Molecular epidemiology, population genetics, and pathogenic role of Helicobacter pylori. Infect Genet Evol. 2012;12:203–13.CrossRefPubMed
4.
Yamaoka Y. Mechanisms of disease: Helicobacter pylori virulence factors. Nat Rev Gastroenterol Hepatol. 2010;7:629–41.PubMedPubMedCentral
5.
Higashi H, Tsutsumi R, Fujita A, Yamazaki S, Asaka M, Azuma T, Hatakeyama M. Biological activity of the Helicobacter pylori virulence factor CagA is determined by variation in the tyrosine phosphorylation sites. Proc Natl Acad Sci USA. 2002;99:14428–33.CrossRefPubMedPubMedCentral
6.
Argent RH, Kidd M, Owen RJ, Thomas RJ, Limb MC, Atherton JC. Determinants and consequences of different levels of CagA phosphorylation for clinical isolates of Helicobacter pylori. Gastroenterology. 2004;127:514–23.CrossRefPubMed
7.
Miftahussurur M, Yamaoka Y, Graham DY. Helicobacter pylori as an oncogenic pathogen, revisited. Expert Rev Mol Med. 2017;19:e4.CrossRefPubMed
8.
Yamaoka Y, Orito E, Mizokami M, Gutierrez O, Saitou N, Kodama T, Osato MS, Kim JG, Ramirez FC, Mahachai V, Graham DY. Helicobacter pylori in North and South America before Columbus. FEBS Lett. 2002;517:180–4.CrossRefPubMed
9.
10.
Wirth T, Wang X, Linz B, Novick RP, Lum JK, Blaser M, Morelli G, Falush D, Achtman M. Distinguishing human ethnic groups by means of sequences from Helicobacter pylori: lessons from Ladakh. Proc Natl Acad Sci USA. 2004;101:4746–51.CrossRefPubMedPubMedCentral
11.
Linz B, Balloux F, Moodley Y, Manica A, Liu H, Roumagnac P, Falush D, Stamer C, Prugnolle F, van der Merwe SW, et al. An African origin for the intimate association between humans and Helicobacter pylori. Nature. 2007;445:915–8.CrossRefPubMedPubMedCentral
12.
Falush D, Wirth T, Linz B, Pritchard J, Stephens M, Kidd M, Blaser M, Graham D, Vacher S, Perez-Perez G, et al. Traces of human migrations in Helicobacter pylori populations. Science. 2003;299:1582–5.CrossRefPubMed
13.
Vilaichone RK, Mahachai V, Tumwasorn S, Wu JY, Graham DY, Yamaoka Y. Molecular epidemiology and outcome of Helicobacter pylori infection in Thailand: a cultural cross roads. Helicobacter. 2004;9:453–9.CrossRefPubMed
14.
Dixon M, Genta R, Yardley J, Correa P. Classification and grading of gastritis. The updated Sydney System. International Workshop on the Histopathology of Gastritis, Houston 1994. Am J Surg Pathol. 1996;20:1161–81.CrossRefPubMed
15.
Bornschein J, Selgrad M, Wex T, Kuester D, Malfertheiner P. Serological assessment of gastric mucosal atrophy in gastric cancer. BMC Gastroenterol. 2012;12:10.CrossRefPubMedPubMedCentral
16.
Rugge M, Meggio A, Pennelli G, Piscioli F, Giacomelli L, De Pretis G, Graham DY. Gastritis staging in clinical practice: the OLGA staging system. Gut. 2007;56:631–6.CrossRefPubMed
17.
Kanada R, Uchida T, Tsukamoto Y, Nguyen LT, Hijiya N, Matsuura K, Kodama M, Okimoto T, Murakami K, Fujioka T, et al. Genotyping of the cagA gene of Helicobacter pylori on immunohistochemistry with East Asian cagA-specific antibody. Pathol Int. 2008;58:218–25.CrossRefPubMed
18.
Vilaichone RK, Panarat W, Aekpongpaisit S, Mahachai V. Clinical Characteristics and Helicobacter pylori status of gastric cancer in Thailand. Asian Pac J Cancer Prev. 2014;15:9005–8.CrossRefPubMed
19.
Nguyen LT, Uchida T, Kuroda A, Tsukamoto Y, Trinh TD, Ta L, Mai HB, Ho DQ, Hoang HH, Vilaichone RK, et al. Evaluation of the anti-East Asian cagA-specific antibody for cagA phenotyping. Clin Vaccine Immunol. 2009;16:1687–92.CrossRefPubMedPubMedCentral
20.
Yamaoka Y, El-Zimaity H, Gutierrez O, Figura N, Kim J, Kodama T, Kashima K, Graham D, Kim J. Relationship between the cagA 3′ repeat region of Helicobacter pylori, gastric histology, and susceptibility to low pH. Gastroenterology. 1999;117:342–9.CrossRefPubMed
21.
Atherton J, Cao P, Peek RJ, Tummuru M, Blaser M, Cover T. Mosaicism in vacuolating cytotoxin alleles of Helicobacter pylori. Association of specific vacA types with cytotoxin production and peptic ulceration. J Biol Chem. 1995;270:17771–7.CrossRefPubMed
22.
Yamazaki S, Yamakawa A, Okuda T, Ohtani M, Suto H, Ito Y, Yamazaki Y, Keida Y, Higashi H, Hatakeyama M, Azuma T. Distinct diversity of vacA, cagA, and cagE genes of Helicobacter pylori associated with peptic ulcer in Japan. J Clin Microbiol. 2005;43:3906–16.CrossRefPubMedPubMedCentral
23.
Matsunari O, Shiota S, Suzuki R, Watada M, Kinjo N, Murakami K, Fujioka T, Kinjo F, Yamaoka Y. Association between Helicobacter pylori virulence factors and gastroduodenal diseases in Okinawa, Japan. J Clin Microbiol. 2012;50:876–83.CrossRefPubMedPubMedCentral
24.
Uchida T, Nguyen LT, Takayama A, Okimoto T, Kodama M, Murakami K, Matsuhisa T, Trinh TD, Ta L, Ho DQ, et al. Analysis of virulence factors of Helicobacter pylori isolated from a Vietnamese population. BMC Microbiol. 2009;9:175.CrossRefPubMedPubMedCentral
25.
Rhead JL, Letley DP, Mohammadi M, Hussein N, Mohagheghi MA, Eshagh Hosseini M, Atherton JC. A new Helicobacter pylori vacuolating cytotoxin determinant, the intermediate region, is associated with gastric cancer. Gastroenterology. 2007;133:926–36.CrossRefPubMed
26.
Basiri Z, Safaralizadeh R, Bonyadi MJ, Somi MH, Mahdavi M, Latifi-Navid S. Helicobacter pylori vacA d1 genotype predicts risk of gastric adenocarcinoma and peptic ulcers in northwestern Iran. Asian Pac J Cancer Prev. 2014;15:1575–9.CrossRefPubMed
27.
Bakhti SZ, Latifi-Navid S, Mohammadi S, Zahri S, Bakhti FS, Feizi F, Yazdanbod A, Siavoshi F. Relevance of Helicobacter pylori vacA 3′-end region polymorphism to gastric cancer. Helicobacter. 2015;21(4):305–16.
28.
Mukhopadhyay AK, Kersulyte D, Jeong JY, Datta S, Ito Y, Chowdhury A, Chowdhury S, Santra A, Bhattacharya SK, Azuma T, et al. Distinctiveness of genotypes of Helicobacter pylori in Calcutta, India. J Bacteriol. 2000;182:3219–27.CrossRefPubMedPubMedCentral
29.
Uchida T, Kanada R, Tsukamoto Y, Hijiya N, Matsuura K, Yano S, Yokoyama S, Kishida T, Kodama M, Murakami K, et al. Immunohistochemical diagnosis of the cagA-gene genotype of Helicobacter pylori with anti-East Asian CagA-specific antibody. Cancer Sci. 2007;98:521–8.CrossRefPubMed
30.
Perez-Perez GI, Taylor DN, Bodhidatta L, Wongsrichanalai J, Baze WB, Dunn BE, Echeverria PD, Blaser MJ. Seroprevalence of Helicobacter pylori infections in Thailand. J Infect Dis. 1990;161:1237–41.CrossRefPubMed
31.
Chinprasatsak S, Wilairatana P, Visalwadi P, Sanguansri P, Batara L, Kityaporn D, Looareesuwan S, Kurathong S, Charoenlarp P. Helicobacter pylori prevalence in northeastern Thailand. Southeast Asian J Trop Med Public Health. 1993;24:734–41.PubMed
32.
Isenbarger DW, Bodhidatta L, Hoge CW, Nirdnoy W, Pitarangsi C, Umpawasiri U, Echeverria P. Prospective study of the incidence of diarrheal disease and Helicobacter pylori infection among children in an orphanage in Thailand. Am J Trop Med Hyg. 1998;59:796–800.CrossRefPubMed
33.
Sriamporn S, Setiawan V, Pisani P, Suwanrungruang K, Sirijaichingkul S, Mairiang P, Parkin DM. Gastric cancer: the roles of diet, alcohol drinking, smoking and Helicobacter pylori in northeastern Thailand. Asian Pac J Cancer Prev. 2002;3:345–52.PubMed
34.
Tangmankongworakoon N, Mahachai V, Thong-Ngam D, Vilaichone RK, Tumwasorn S, Kullavanijaya P. Pattern of drug resistant Helicobacter pylori in dyspeptic patients in Thailand. J Med Assoc Thai. 2003;86(Suppl 2):S439–44.PubMed
35.
Atisook K, Kachinthorn U, Luengrojanakul P, Tanwandee T, Pakdirat P, Puapairoj A. Histology of gastritis and Helicobacter pylori infection in Thailand: a nationwide study of 3776 cases. Helicobacter. 2003;8:132–41.CrossRefPubMed
36.
Mitipat N, Siripermpool P, Jadwattanakul T, Chaunthongkum S. The prevalence of Helicobacter pylori infection in patients with gastrointestinal symptoms in Chon Buri, Thailand. Southeast Asian J Trop Med Public Health. 2005;36:341–6.PubMed
37.
Linpisarn S, Suwan W, Lertprasertsuk N, Koosirirat C, Steger HF, Prommuangyong K, Phornphutkul K. Helicobacter pylori cagA, vacA and iceA genotypes in northern Thai patients with gastric disease. Southeast Asian J Trop Med Public Health. 2007;38:356–62.PubMed
38.
Chomvarin C, Namwat W, Chaicumpar K, Mairiang P, Sangchan A, Sripa B, Tor-Udom S, Vilaichone RK. Prevalence of Helicobacter pylori vacA, cagA, cagE, iceA and babA2 genotypes in Thai dyspeptic patients. Int J Infect Dis. 2008;12:30–6.CrossRefPubMed
39.
Tanuma M, Rimbara E, Noguchi N, Boonyaritichaikij S, Kuwabara K, Fukunaga Y, Sasatsu M. Analysis of clarithromycin resistance and cagA status in Helicobacter pylori by use of feces from children in Thailand. J Clin Microbiol. 2009;47:4144–5.CrossRefPubMedPubMedCentral
40.
Hirai I, Sasaki T, Kimoto A, Yamamoto Y, Azuma T, Mahachai V, Hansomburana P, Lertkupinit C, Luangjaru S, Noophan P, et al. Infection of less virulent Helicobacter pylori strains in asymptomatic healthy individuals in Thailand as a potential contributing factor to the Asian enigma. Microbes Infect. 2010;12:227–30.CrossRefPubMed
41.
Vilaichone RK, Mahacahai V, Tumwasorn S, Kachintorn U. CagA genotype and metronidazole resistant strain of Helicobacter pylori in functional dyspepsia in Thailand. J Gastroenterol Hepatol. 2011;26(Suppl 3):46–8.CrossRefPubMed
42.
Chomvarin C, Phusri K, Sawadpanich K, Mairiang P, Namwat W, Wongkham C, Hahnvajanawong C. Prevalence of cagA EPIYA motifs in Helicobacter pylori among dyspeptic patients in northeast Thailand. Southeast Asian J Trop Med Public Health. 2012;43:105–15.PubMed
43.
Sakonlaya D, Apisarnthanarak A, Yamada N, Tomtitchong P. Modified toluidine blue: an alternative stain for Helicobacter pylori detection in routine diagnostic use and post-eradication confirmation for gastric cancer prevention. Asian Pac J Cancer Prev. 2014;15:6983–7.CrossRefPubMed
44.
Piriyapong K, Tangaroonsanti A, Mahachai V, Vilaichone RK. Helicobacter pylori infection impacts on functional dyspepsia in Thailand. Asian Pac J Cancer Prev. 2014;15:10887–91.CrossRefPubMed
45.
Uchida T, Miftahussurur M, Pittayanon R, Vilaichone RK, Wisedopas N, Ratanachu-Ek T, Kishida T, Moriyama M, Yamaoka Y, Mahachai V. Helicobacter pylori infection in Thailand: a nationwide study of the cagA phenotype. PLoS ONE. 2015;10:e0136775.CrossRefPubMedPubMedCentral
46.
Higashi H, Tsutsumi R, Muto S, Sugiyama T, Azuma T, Asaka M, Hatakeyama M. SHP-2 tyrosine phosphatase as an intracellular target of Helicobacter pylori CagA protein. Science. 2002;295:683–6.CrossRefPubMed
47.
Hatakeyama M, Higashi H. Helicobacter pylori CagA: a new paradigm for bacterial carcinogenesis. Cancer Sci. 2005;96:835–43.CrossRefPubMed
48.
Hatakeyama M. Oncogenic mechanisms of the Helicobacter pylori CagA protein. Nat Rev Cancer. 2004;4:688–94.CrossRefPubMed
49.
Miftahussurur M, Syam AF, Makmun D, Nusi IA, Zein LH, Zulkhairi Akil F, Uswan WB, Simanjuntak D, Uchida T, et al. Helicobacter pylori virulence genes in the five largest islands of Indonesia. Gut Pathog. 2015;7:26.CrossRefPubMedPubMedCentral
50.
Moonieinda V. The Karen people: culture, faith and history. The Karen Buddhist Dhamma Dhutta Foundation. 2011.
51.
Summerer M, Horst J, Erhart G, Weißensteiner H, Schönherr S, Pacher D, Forer L, Horst D, Manhart A, Horst B, et al. Large-scale mitochondrial DNA analysis in Southeast Asia reveals evolutionary effects of cultural isolation in the multi-ethnic population of Myanmar. BMC Evol Biol. 2014;14:17.CrossRefPubMedPubMedCentral
52.
Wen B, Xie X, Gao S, Li H, Shi H, Song X, Qian T, Xiao C, Jin J, Su B, et al. Analyses of genetic structure of Tibeto-Burman populations reveals sex-biased admixture in southern Tibeto-Burmans. Am J Hum Genet. 2004;74:856–65.CrossRefPubMedPubMedCentral
53.
Michaud J. From southwest China into upper Indochina: an overview of Hmong (Miao) migrations. Asia Pac Viewp. 1997;38:119–30.CrossRef
54.
Kutanan W, Srikummool M, Pittayaporn P, Seielstad M, Kangwanpong D, Kumar V, Prombanchachai T, Chantawannakul P. Admixed origin of the Kayah (Red Karen) in northern Thailand revealed by biparental and paternal markers. Ann Hum Genet. 2015;79:108–21.CrossRefPubMed
55.
Imsamran W, Chaiwerawattana A, Wiangnon S, Pongnikorn D, Suwanrungrung K, Sangrajrang S, Buasom R. Cancer in Thailand, vol. 8. Bangkok: Cancer Registry Unit, National Cancer Institute Thailand; 2015.
56.
Devi SM, Ahmed I, Francalacci P, Hussain MA, Akhter Y, Alvi A, Sechi LA, Megraud F, Ahmed N. Ancestral European roots of Helicobacter pylori in India. BMC Genomics. 2007;8:184.CrossRefPubMedPubMedCentral
57.
Rajanubhab D. The introduction of Western culture in Siam. 1952:89–100. (pp. 89–100).
58.
Matsunari O, Miftahussurur M, Shiota S, Suzuki R, Vilaichone RK, Uchida T, Ratanachu-ek T, Tshering L, Mahachai V, Yamaoka Y. Rare Helicobacter pylori virulence genotypes in Bhutan. Sci Rep. 2016;6:22584.CrossRefPubMedPubMedCentral
Metadata
Title
Helicobacter pylori virulence genes of minor ethnic groups in North Thailand
Authors
Phawinee Subsomwong
Muhammad Miftahussurur
Ratha-korn Vilaichone
Thawee Ratanachu-ek
Rumiko Suzuki
Junko Akada
Tomohisa Uchida
Varocha Mahachai
Yoshio Yamaoka
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Gut Pathogens / Issue 1/2017
Electronic ISSN: 1757-4749
DOI
https://doi.org/10.1186/s13099-017-0205-x

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