Skip to main content
Top
Published in: Gut Pathogens 1/2014

Open Access 01-12-2014 | Research

Extremely low Helicobacter pylori prevalence in North Sulawesi, Indonesia and identification of a Maori-tribe type strain: a cross sectional study

Authors: Muhammad Miftahussurur, Josef Tuda, Rumiko Suzuki, Yasutoshi Kido, Fumihiko Kawamoto, Miyuki Matsuda, Indah S Tantular, Suhintam Pusarawati, Nasronudin, Paul N Harijanto, Yoshio Yamaoka

Published in: Gut Pathogens | Issue 1/2014

Login to get access

Abstract

Background

Sulawesi in Indonesia has a unique geographical profile with assumed separation from Sundaland. Studies of Helicobacter pylori in this region are rare due to the region’s rural location and lack of endoscopy equipment. Indirect methods are, therefore, the most appropriate for measuring H. pylori infection in these areas; with the disposable gastric brush test, we can obtain gastric juice as well as small gastric tissue samples for H. pylori culture. We investigated the prevalence of H. pylori infection and evaluated human migration patterns in the remote areas of North Sulawesi.

Methods

We recruited a total of 251 consecutive adult volunteers and 131 elementary school children. H. pylori infection was determined by urine antibody test. A gastric brush test was used to culture H. pylori. We used next-generation and polymerase chain reaction based sequencing to determine virulence factors and multi-locus sequence typing (MLST).

Results

The overall H. pylori prevalence was only 14.3% for adults and 3.8% for children, and 13.6% and 16.7% in Minahasanese and Mongondownese participants, respectively. We isolated a single H. pylori strain, termed -Manado-1. Manado-1 was East Asian type cagA (ABD type), vacA s1c-m1b, iceA1 positive/iceA2 negative, jhp0562-positive/-(1,3) galT-negative, oipA ‘on’, and dupA-negative. Phylogenetic analyses showed the strain to be hspMaori type, a major type observed in native Taiwanese and Maori tribes.

Conclusions

Our data support that very low H. pylori infection prevalence in Indonesia. Identification of hspMaori type H. pylori in North Sulawesi may support the hypothesis that North Sulawesi people migrated from north.
Appendix
Available only for authorised users
Literature
1.
go back to reference Lee YY, Mahendra Raj S, Graham DY:Helicobacter pylori infection - a boon or a bane: lessons from studies in a low-prevalence population. Helicobacter. 2013, 18: 338-346. 10.1111/hel.12058.PubMedCentralCrossRefPubMed Lee YY, Mahendra Raj S, Graham DY:Helicobacter pylori infection - a boon or a bane: lessons from studies in a low-prevalence population. Helicobacter. 2013, 18: 338-346. 10.1111/hel.12058.PubMedCentralCrossRefPubMed
2.
go back to reference Tumonggor MK, Karafet TM, Hallmark B, Lansing JS, Sudoyo H, Hammer MF, Cox MP: The Indonesian archipelago: an ancient genetic highway linking Asia and the Pacific. J Hum Genet. 2013, 58: 165-173. 10.1038/jhg.2012.154.CrossRefPubMed Tumonggor MK, Karafet TM, Hallmark B, Lansing JS, Sudoyo H, Hammer MF, Cox MP: The Indonesian archipelago: an ancient genetic highway linking Asia and the Pacific. J Hum Genet. 2013, 58: 165-173. 10.1038/jhg.2012.154.CrossRefPubMed
3.
go back to reference Suerbaum S, Michetti P:Helicobacter pylori infection. N Engl J Med. 2002, 347: 1175-1186. 10.1056/NEJMra020542.CrossRefPubMed Suerbaum S, Michetti P:Helicobacter pylori infection. N Engl J Med. 2002, 347: 1175-1186. 10.1056/NEJMra020542.CrossRefPubMed
4.
go back to reference Sahara S, Sugimoto M, Vilaichone RK, Mahachai V, Miyajima H, Furuta T, Yamaoka Y: Role of Helicobacter pylori cagA EPIYA motif and vacA genotypes for the development of gastrointestinal diseases in Southeast Asian countries: a meta-analysis. BMC Infect Dis. 2012, 12: 223-10.1186/1471-2334-12-223.PubMedCentralCrossRefPubMed Sahara S, Sugimoto M, Vilaichone RK, Mahachai V, Miyajima H, Furuta T, Yamaoka Y: Role of Helicobacter pylori cagA EPIYA motif and vacA genotypes for the development of gastrointestinal diseases in Southeast Asian countries: a meta-analysis. BMC Infect Dis. 2012, 12: 223-10.1186/1471-2334-12-223.PubMedCentralCrossRefPubMed
5.
go back to reference Destura RV, Labio ED, Barrett LJ, Alcantara CS, Gloria VI, Daez ML, Guerrant RL: Laboratory diagnosis and susceptibility profile of Helicobacter pylori infection in the Philippines. Ann Clin Microbiol Antimicrob. 2004, 3: 25-10.1186/1476-0711-3-25.PubMedCentralCrossRefPubMed Destura RV, Labio ED, Barrett LJ, Alcantara CS, Gloria VI, Daez ML, Guerrant RL: Laboratory diagnosis and susceptibility profile of Helicobacter pylori infection in the Philippines. Ann Clin Microbiol Antimicrob. 2004, 3: 25-10.1186/1476-0711-3-25.PubMedCentralCrossRefPubMed
6.
go back to reference Tokudome S, Samsuria Soeripto WD, Triningsih FX, Suzuki S, Hosono A, Triono T, Sarjadi IW, Miranti IP, Ghadimi R, Moore MA:Helicobacter pylori infection appears essential for stomach carcinogenesis: observations in Semarang, Indonesia. Cancer Sci. 2005, 96: 873-875. 10.1111/j.1349-7006.2005.00122.x.CrossRefPubMed Tokudome S, Samsuria Soeripto WD, Triningsih FX, Suzuki S, Hosono A, Triono T, Sarjadi IW, Miranti IP, Ghadimi R, Moore MA:Helicobacter pylori infection appears essential for stomach carcinogenesis: observations in Semarang, Indonesia. Cancer Sci. 2005, 96: 873-875. 10.1111/j.1349-7006.2005.00122.x.CrossRefPubMed
7.
go back to reference Tokudome S, Soeripto , Triningsih FX, Ananta I, Suzuki S, Kuriki K, Akasaka S, Kosaka H, Ishikawa H, Azuma T, Moore MA: Rare Helicobacter pylori infection as a factor for the very low stomach cancer incidence in Yogyakarta, Indonesia. Cancer Lett. 2005, 219: 57-61. 10.1016/j.canlet.2004.09.043.CrossRefPubMed Tokudome S, Soeripto , Triningsih FX, Ananta I, Suzuki S, Kuriki K, Akasaka S, Kosaka H, Ishikawa H, Azuma T, Moore MA: Rare Helicobacter pylori infection as a factor for the very low stomach cancer incidence in Yogyakarta, Indonesia. Cancer Lett. 2005, 219: 57-61. 10.1016/j.canlet.2004.09.043.CrossRefPubMed
8.
go back to reference Zhao Y, Wang J, Tanaka T, Hosono A, Ando R, Soeripto S, Ediati Triningsih FX, Triono T, Sumoharjo S, Astuti EY, Gunawan S, Tokudome S: Association between HLA-DQ genotypes and haplotypes vs Helicobacter pylori infection in an Indonesian population. Asian Pac J Cancer Prev. 2012, 13: 1247-1251. 10.7314/APJCP.2012.13.4.1247.CrossRefPubMed Zhao Y, Wang J, Tanaka T, Hosono A, Ando R, Soeripto S, Ediati Triningsih FX, Triono T, Sumoharjo S, Astuti EY, Gunawan S, Tokudome S: Association between HLA-DQ genotypes and haplotypes vs Helicobacter pylori infection in an Indonesian population. Asian Pac J Cancer Prev. 2012, 13: 1247-1251. 10.7314/APJCP.2012.13.4.1247.CrossRefPubMed
9.
go back to reference Syam AF, Rani AA, Abdullah M, Manan C, Makmun D, Simadibrata M, Djojoningrat D, Sato T: Accuracy of Helicobacter pylori stool antigen for the detection of Helicobacter pylori infection in dyspeptic patients. World J Gastroenterol. 2005, 11: 386-388.PubMedCentralCrossRefPubMed Syam AF, Rani AA, Abdullah M, Manan C, Makmun D, Simadibrata M, Djojoningrat D, Sato T: Accuracy of Helicobacter pylori stool antigen for the detection of Helicobacter pylori infection in dyspeptic patients. World J Gastroenterol. 2005, 11: 386-388.PubMedCentralCrossRefPubMed
10.
go back to reference Syam AF, Abdullah M, Rani AA, Nurdjanah S, Adi P, Djumhana A, Tarigan P, Wibawa ID: Evaluation of the use of rapid urease test: pronto dry to detect H pylori in patients with dyspepsia in several cities in Indonesia. World J Gastroenterol. 2006, 12: 6216-6218.PubMedCentralPubMed Syam AF, Abdullah M, Rani AA, Nurdjanah S, Adi P, Djumhana A, Tarigan P, Wibawa ID: Evaluation of the use of rapid urease test: pronto dry to detect H pylori in patients with dyspepsia in several cities in Indonesia. World J Gastroenterol. 2006, 12: 6216-6218.PubMedCentralPubMed
11.
go back to reference Saragih JB, Akbar N, Syam AF, Sirait S, Himawan S, Soetjahyo E: Incidence of helicobacter pylori infection and gastric cancer: an 8-year hospital based study. Acta Med Indones. 2007, 39: 79-81.PubMed Saragih JB, Akbar N, Syam AF, Sirait S, Himawan S, Soetjahyo E: Incidence of helicobacter pylori infection and gastric cancer: an 8-year hospital based study. Acta Med Indones. 2007, 39: 79-81.PubMed
12.
go back to reference Aulia D, Manz GO, Simadibrata M: Pepsinogen I concentration in organic dyspepsia patients at Gastroenterology Division, Department of Internal Medicine, Cipto Mangunkusumo Hospital. Acta Med Indones. 2009, 41: 107-114.PubMed Aulia D, Manz GO, Simadibrata M: Pepsinogen I concentration in organic dyspepsia patients at Gastroenterology Division, Department of Internal Medicine, Cipto Mangunkusumo Hospital. Acta Med Indones. 2009, 41: 107-114.PubMed
13.
go back to reference Miftahussurur M, Shiota S, Suzuki R, Matsuda M, Uchida T, Kido Y, Kawamoto F, Maimunah U, Adi P, Rezkitha Y, Nasronudin ?, Nusi I, Yamaoka Y: Identification of Helicobacter pylori infection in symptomatic patients in Surabaya, Indonesia, using five diagnostic tests. Epidemiol Infect. 2014, ?: 1-11. 10.1017/S095026881400154X. [Epub ahead of print] Miftahussurur M, Shiota S, Suzuki R, Matsuda M, Uchida T, Kido Y, Kawamoto F, Maimunah U, Adi P, Rezkitha Y, Nasronudin ?, Nusi I, Yamaoka Y: Identification of Helicobacter pylori infection in symptomatic patients in Surabaya, Indonesia, using five diagnostic tests. Epidemiol Infect. 2014, ?: 1-11. 10.1017/S095026881400154X. [Epub ahead of print]
14.
go back to reference Falush D, Wirth T, Linz B, Pritchard JK, Stephens M, Kidd M, Blaser MJ, Graham DY, Vacher S, Perez-Perez GI, Yamaoka Y, Mégraud F, Otto K, Reichard U, Katzowitsch E, Wang X, Achtman M, Suerbaum S: Traces of human migrations in Helicobacter pylori populations. Science. 2003, 299: 1582-1585. 10.1126/science.1080857.CrossRefPubMed Falush D, Wirth T, Linz B, Pritchard JK, Stephens M, Kidd M, Blaser MJ, Graham DY, Vacher S, Perez-Perez GI, Yamaoka Y, Mégraud F, Otto K, Reichard U, Katzowitsch E, Wang X, Achtman M, Suerbaum S: Traces of human migrations in Helicobacter pylori populations. Science. 2003, 299: 1582-1585. 10.1126/science.1080857.CrossRefPubMed
15.
go back to reference Linz B, Balloux F, Moodley Y, Manica A, Liu H, Roumagnac P, Falush D, Stamer C, Prugnolle F, van der Merwe SW, Yamaoka Y, Graham DY, Perez-Trallero E, Wadstrom T, Suerbaum S, Achtman M: An African origin for the intimate association between humans and Helicobacter pylori. Nature. 2007, 445: 915-918. 10.1038/nature05562.PubMedCentralCrossRefPubMed Linz B, Balloux F, Moodley Y, Manica A, Liu H, Roumagnac P, Falush D, Stamer C, Prugnolle F, van der Merwe SW, Yamaoka Y, Graham DY, Perez-Trallero E, Wadstrom T, Suerbaum S, Achtman M: An African origin for the intimate association between humans and Helicobacter pylori. Nature. 2007, 445: 915-918. 10.1038/nature05562.PubMedCentralCrossRefPubMed
16.
go back to reference Yamaoka Y:Helicobacter pylori typing as a tool for tracking human migration. Clin Microbiol Infect. 2009, 15: 829-834. 10.1111/j.1469-0691.2009.02967.x.PubMedCentralCrossRefPubMed Yamaoka Y:Helicobacter pylori typing as a tool for tracking human migration. Clin Microbiol Infect. 2009, 15: 829-834. 10.1111/j.1469-0691.2009.02967.x.PubMedCentralCrossRefPubMed
17.
go back to reference Yamaoka Y: Mechanisms of disease: Helicobacter pylori virulence factors. Nat Rev Gastroenterol Hepatol. 2010, 7: 629-641.PubMedCentralPubMed Yamaoka Y: Mechanisms of disease: Helicobacter pylori virulence factors. Nat Rev Gastroenterol Hepatol. 2010, 7: 629-641.PubMedCentralPubMed
18.
go back to reference Perger R: Did the genus Parandrocephalus Heller, 1916 (Coleoptera, Cerambycidae, Callichromatini) cross the Wallace line? The taxonomic status of Parandrocephalus blairi Bentanachs & Vives 2009 and a new subgenus of Hexamitodera Heller, 1896, with notes on convergent evolution and secondary sexual characters. Zookeys. 2013, 293: 77-89. 10.3897/zookeys.293.5133.CrossRefPubMed Perger R: Did the genus Parandrocephalus Heller, 1916 (Coleoptera, Cerambycidae, Callichromatini) cross the Wallace line? The taxonomic status of Parandrocephalus blairi Bentanachs & Vives 2009 and a new subgenus of Hexamitodera Heller, 1896, with notes on convergent evolution and secondary sexual characters. Zookeys. 2013, 293: 77-89. 10.3897/zookeys.293.5133.CrossRefPubMed
19.
go back to reference Wigboldus JS: A History of the Minahasa c. 1615-1680. Archipel. 1987, 34: 63-101. 10.3406/arch.1987.2374.CrossRef Wigboldus JS: A History of the Minahasa c. 1615-1680. Archipel. 1987, 34: 63-101. 10.3406/arch.1987.2374.CrossRef
20.
go back to reference Moodley Y, Linz B, Yamaoka Y, Windsor HM, Breurec S, Wu JY, Maady A, Bernhöft S, Thiberge JM, Phuanukoonnon S, Jobb G, Siba P, Graham DY, Marshall BJ, Achtman M: The peopling of the Pacific from a bacterial perspective. Science. 2009, 323: 527-530. 10.1126/science.1166083.PubMedCentralCrossRefPubMed Moodley Y, Linz B, Yamaoka Y, Windsor HM, Breurec S, Wu JY, Maady A, Bernhöft S, Thiberge JM, Phuanukoonnon S, Jobb G, Siba P, Graham DY, Marshall BJ, Achtman M: The peopling of the Pacific from a bacterial perspective. Science. 2009, 323: 527-530. 10.1126/science.1166083.PubMedCentralCrossRefPubMed
21.
go back to reference Dabiri H, Bolfion M, Mirsalehian A, Rezadehbashi M, Jafari F, Shokrzadeh L, Sahebekhtiari N, Zojaji H, Yamaoka Y, Mirsattari D, Zali MR: Analysis of Helicobacter pylori genotypes in Afghani and Iranian isolates. Pol J Microbiol. 2010, 59: 61-66.PubMed Dabiri H, Bolfion M, Mirsalehian A, Rezadehbashi M, Jafari F, Shokrzadeh L, Sahebekhtiari N, Zojaji H, Yamaoka Y, Mirsattari D, Zali MR: Analysis of Helicobacter pylori genotypes in Afghani and Iranian isolates. Pol J Microbiol. 2010, 59: 61-66.PubMed
22.
go back to reference Goh KL, Chan WK, Shiota S, Yamaoka Y: Epidemiology of Helicobacter pylori infection and public health implications. Helicobacter. 2011, 16 (Suppl 1): 1-9. 10.1111/j.1523-5378.2011.00874.x.PubMedCentralCrossRefPubMed Goh KL, Chan WK, Shiota S, Yamaoka Y: Epidemiology of Helicobacter pylori infection and public health implications. Helicobacter. 2011, 16 (Suppl 1): 1-9. 10.1111/j.1523-5378.2011.00874.x.PubMedCentralCrossRefPubMed
23.
go back to reference Okuda M, Kamiya S, Booka M, Kikuchi S, Osaki T, Hiwatani T, Maekawa K, Fukuda Y: Diagnostic accuracy of urine-based kits for detection of Helicobacter pylori antibody in children. Pediatr Int. 2013, 55: 337-341. 10.1111/ped.12057.CrossRefPubMed Okuda M, Kamiya S, Booka M, Kikuchi S, Osaki T, Hiwatani T, Maekawa K, Fukuda Y: Diagnostic accuracy of urine-based kits for detection of Helicobacter pylori antibody in children. Pediatr Int. 2013, 55: 337-341. 10.1111/ped.12057.CrossRefPubMed
25.
go back to reference Malaty HM, Kumagai T, Tanaka E, Ota H, Kiyosawa K, Graham DY, Katsuyama T: Evidence from a nine-year birth cohort study in Japan of transmission pathways of Helicobacter pylori infection. J Clin Microbiol. 2000, 38: 1971-1973.PubMedCentralPubMed Malaty HM, Kumagai T, Tanaka E, Ota H, Kiyosawa K, Graham DY, Katsuyama T: Evidence from a nine-year birth cohort study in Japan of transmission pathways of Helicobacter pylori infection. J Clin Microbiol. 2000, 38: 1971-1973.PubMedCentralPubMed
26.
go back to reference Hatin WI, Nur-Shafawati AR, Zahri MK, Xu S, Jin L, Tan SG, Rizman-Idid M, Zilfalil BA, Consortium HP-AS: Population genetic structure of peninsular Malaysia Malay sub-ethnic groups. PLoS One. 2011, 6: e18312-10.1371/journal.pone.0018312.PubMedCentralCrossRefPubMed Hatin WI, Nur-Shafawati AR, Zahri MK, Xu S, Jin L, Tan SG, Rizman-Idid M, Zilfalil BA, Consortium HP-AS: Population genetic structure of peninsular Malaysia Malay sub-ethnic groups. PLoS One. 2011, 6: e18312-10.1371/journal.pone.0018312.PubMedCentralCrossRefPubMed
27.
go back to reference Chen HL, Chen MJ, Shih SC, Wang HY, Lin IT, Bair MJ: Socioeconomic status, personal habits, and prevalence of Helicobacter pylori infection in the inhabitants of Lanyu. J Formos Med Assoc. 2014, 113: 278-283. 10.1016/j.jfma.2013.11.013.CrossRefPubMed Chen HL, Chen MJ, Shih SC, Wang HY, Lin IT, Bair MJ: Socioeconomic status, personal habits, and prevalence of Helicobacter pylori infection in the inhabitants of Lanyu. J Formos Med Assoc. 2014, 113: 278-283. 10.1016/j.jfma.2013.11.013.CrossRefPubMed
28.
go back to reference Cortes MC, Yamakawa A, Casingal CR, Fajardo LS, Juan ML, De Guzman BB, Bondoc EM, Mahachai V, Yamazaki Y, Yoshida M, Kutsumi H, Natividad FF, Azuma T: Diversity of the cagA gene of Helicobacter pylori strains from patients with gastroduodenal diseases in the Philippines. FEMS Immunol Med Microbiol. 2010, 60: 90-97. 10.1111/j.1574-695X.2010.00722.x.CrossRefPubMed Cortes MC, Yamakawa A, Casingal CR, Fajardo LS, Juan ML, De Guzman BB, Bondoc EM, Mahachai V, Yamazaki Y, Yoshida M, Kutsumi H, Natividad FF, Azuma T: Diversity of the cagA gene of Helicobacter pylori strains from patients with gastroduodenal diseases in the Philippines. FEMS Immunol Med Microbiol. 2010, 60: 90-97. 10.1111/j.1574-695X.2010.00722.x.CrossRefPubMed
29.
go back to reference Graham DY, Kudo M, Reddy R, Opekun AR: Practical rapid, minimally invasive, reliable nonendoscopic method to obtain Helicobacter pylori for culture. Helicobacter. 2005, 10: 1-3. 10.1111/j.1523-5378.2005.00285.x.CrossRefPubMed Graham DY, Kudo M, Reddy R, Opekun AR: Practical rapid, minimally invasive, reliable nonendoscopic method to obtain Helicobacter pylori for culture. Helicobacter. 2005, 10: 1-3. 10.1111/j.1523-5378.2005.00285.x.CrossRefPubMed
30.
go back to reference Graham DY, Reddy S: Rapid detection of anti-Helicobacter pylori IgG in urine using immunochromatography. Aliment Pharmacol Ther. 2001, 15: 699-702. 10.1046/j.1365-2036.2001.00968.x.CrossRefPubMed Graham DY, Reddy S: Rapid detection of anti-Helicobacter pylori IgG in urine using immunochromatography. Aliment Pharmacol Ther. 2001, 15: 699-702. 10.1046/j.1365-2036.2001.00968.x.CrossRefPubMed
31.
go back to reference Nguyen LT, Uchida T, Tsukamoto Y, Trinh TD, Ta L, Ho DQ, Matsuhisa T, Uchida M, Takayama A, Hijiya N, Okimoto T, Kodama M, Murakami K, Fujioka T, Moriyama M: Evaluation of rapid urine test for the detection of Helicobacter pylori infection in the Vietnamese population. Dig Dis Sci. 2010, 55: 89-93. 10.1007/s10620-009-0720-9.CrossRefPubMed Nguyen LT, Uchida T, Tsukamoto Y, Trinh TD, Ta L, Ho DQ, Matsuhisa T, Uchida M, Takayama A, Hijiya N, Okimoto T, Kodama M, Murakami K, Fujioka T, Moriyama M: Evaluation of rapid urine test for the detection of Helicobacter pylori infection in the Vietnamese population. Dig Dis Sci. 2010, 55: 89-93. 10.1007/s10620-009-0720-9.CrossRefPubMed
32.
go back to reference Han SW, Flamm R, Hachem CY, Kim HY, Clarridge JE, Evans DG, Beyer J, Drnec J, Graham DY: Transport and storage of Helicobacter pylori from gastric mucosal biopsies and clinical isolates. Eur J Clin Microbiol Infect Dis. 1995, 14: 349-352. 10.1007/BF02116531.CrossRefPubMed Han SW, Flamm R, Hachem CY, Kim HY, Clarridge JE, Evans DG, Beyer J, Drnec J, Graham DY: Transport and storage of Helicobacter pylori from gastric mucosal biopsies and clinical isolates. Eur J Clin Microbiol Infect Dis. 1995, 14: 349-352. 10.1007/BF02116531.CrossRefPubMed
33.
go back to reference Yamaoka Y, Kodama T, Kita M, Imanishi J, Kashima K, Graham DY: Relationship of vacA genotypes of Helicobacter pylori to cagA status, cytotoxin production, and clinical outcome. Helicobacter. 1998, 3: 241-253. 10.1046/j.1523-5378.1998.08056.x.CrossRefPubMed Yamaoka Y, Kodama T, Kita M, Imanishi J, Kashima K, Graham DY: Relationship of vacA genotypes of Helicobacter pylori to cagA status, cytotoxin production, and clinical outcome. Helicobacter. 1998, 3: 241-253. 10.1046/j.1523-5378.1998.08056.x.CrossRefPubMed
34.
go back to reference 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: 876-883. 10.1128/JCM.05562-11.PubMedCentralCrossRefPubMed 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: 876-883. 10.1128/JCM.05562-11.PubMedCentralCrossRefPubMed
35.
go back to reference Takahashi A, Shiota S, Matsunari O, Watada M, Suzuki R, Nakachi S, Kinjo N, Kinjo F, Yamaoka Y: Intact long-type dupA as a marker for gastroduodenal diseases in Okinawan subpopulation, Japan. Helicobacter. 2013, 18: 66-72. 10.1111/j.1523-5378.2012.00994.x.PubMedCentralCrossRefPubMed Takahashi A, Shiota S, Matsunari O, Watada M, Suzuki R, Nakachi S, Kinjo N, Kinjo F, Yamaoka Y: Intact long-type dupA as a marker for gastroduodenal diseases in Okinawan subpopulation, Japan. Helicobacter. 2013, 18: 66-72. 10.1111/j.1523-5378.2012.00994.x.PubMedCentralCrossRefPubMed
36.
go back to reference Atherton JC, Cao P, Peek RM, Tummuru MK, Blaser MJ, Cover TL: Mosaicism in vacuolating cytotoxin alleles of Helicobacter pylori. Association of specific vacA types with cytotoxin production and peptic ulceration. J Biol Chem. 1995, 270: 17771-17777. 10.1074/jbc.270.30.17771.CrossRefPubMed Atherton JC, Cao P, Peek RM, Tummuru MK, Blaser MJ, Cover TL: Mosaicism in vacuolating cytotoxin alleles of Helicobacter pylori. Association of specific vacA types with cytotoxin production and peptic ulceration. J Biol Chem. 1995, 270: 17771-17777. 10.1074/jbc.270.30.17771.CrossRefPubMed
37.
go back to reference Yamaoka Y, Kodama T, Gutierrez O, Kim JG, Kashima K, Graham DY: Relationship between Helicobacter pylori iceA, cagA, and vacA status and clinical outcome: studies in four different countries. J Clin Microbiol. 1999, 37: 2274-2279.PubMedCentralPubMed Yamaoka Y, Kodama T, Gutierrez O, Kim JG, Kashima K, Graham DY: Relationship between Helicobacter pylori iceA, cagA, and vacA status and clinical outcome: studies in four different countries. J Clin Microbiol. 1999, 37: 2274-2279.PubMedCentralPubMed
38.
go back to reference Yamaoka Y, El-Zimaity HM, Gutierrez O, Figura N, Kim JG, Kodama T, Kashima K, Graham DY, Kim JK: Relationship between the cagA 3? repeat region of Helicobacter pylori, gastric histology, and susceptibility to low pH. Gastroenterology. 1999, 117: 342-349. 10.1053/gast.1999.0029900342.CrossRefPubMed Yamaoka Y, El-Zimaity HM, Gutierrez O, Figura N, Kim JG, Kodama T, Kashima K, Graham DY, Kim JK: Relationship between the cagA 3? repeat region of Helicobacter pylori, gastric histology, and susceptibility to low pH. Gastroenterology. 1999, 117: 342-349. 10.1053/gast.1999.0029900342.CrossRefPubMed
39.
go back to reference Yamaoka Y, Kikuchi S, el-Zimaity HM, Gutierrez O, Osato MS, Graham DY: Importance of Helicobacter pylori oipA in clinical presentation, gastric inflammation, and mucosal interleukin 8 production. Gastroenterology. 2002, 123: 414-424. 10.1053/gast.2002.34781.CrossRefPubMed Yamaoka Y, Kikuchi S, el-Zimaity HM, Gutierrez O, Osato MS, Graham DY: Importance of Helicobacter pylori oipA in clinical presentation, gastric inflammation, and mucosal interleukin 8 production. Gastroenterology. 2002, 123: 414-424. 10.1053/gast.2002.34781.CrossRefPubMed
40.
go back to reference Kumar S, Nei M, Dudley J, Tamura K: MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform. 2008, 9: 299-306. 10.1093/bib/bbn017.PubMedCentralCrossRefPubMed Kumar S, Nei M, Dudley J, Tamura K: MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform. 2008, 9: 299-306. 10.1093/bib/bbn017.PubMedCentralCrossRefPubMed
41.
go back to reference Tamura K, Dudley J, Nei M, Kumar S: MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol. 2007, 24: 1596-1599. 10.1093/molbev/msm092.CrossRefPubMed Tamura K, Dudley J, Nei M, Kumar S: MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol. 2007, 24: 1596-1599. 10.1093/molbev/msm092.CrossRefPubMed
Metadata
Title
Extremely low Helicobacter pylori prevalence in North Sulawesi, Indonesia and identification of a Maori-tribe type strain: a cross sectional study
Authors
Muhammad Miftahussurur
Josef Tuda
Rumiko Suzuki
Yasutoshi Kido
Fumihiko Kawamoto
Miyuki Matsuda
Indah S Tantular
Suhintam Pusarawati
Nasronudin
Paul N Harijanto
Yoshio Yamaoka
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Gut Pathogens / Issue 1/2014
Electronic ISSN: 1757-4749
DOI
https://doi.org/10.1186/s13099-014-0042-0

Other articles of this Issue 1/2014

Gut Pathogens 1/2014 Go to the issue