Helicobacter pylori in the Indonesian Malay’s descendants might be imported from other ethnicities

Syam A.F., Waskito L.A., Rezkitha Y.A.A., Simamora R.M., Yusuf F., Danchi K.E., Bakry A.F., Arnelis, Mulya E., Siregar G.A., Sugihartono T., Maulahela H., Doohan D., Miftahussurur M., Yamaoka Y.

Division of Gastroenterology, Department of Internal Medicine, Faculty of Medicine-Cipto Mangunkusumo Teaching Hospital, University of Indonesia, Jakarta, Indonesia; Faculty of Medicine, Universitas Airlangga, Surabaya, Indonesia; Institute of Tropical Disease, Universitas Airlangga, Surabaya, Indonesia; Department of Internal Medicine, Faculty of Medicine, University of Muhammadiyah Surabaya, Surabaya, Indonesia; Department of Internal Medicine, Faculty of Medicine, Universitas Airlangga, Surabaya, Indonesia; Division of Gastroentero-Hepatology, Department of Internal Medicine, Faculty of Medicine, Dr. Zainoel Abidin General Hospital, Universitas Syiah Kuala, Banda Aceh, Indonesia; Department of Internal Medicine, Dr. M Thomsen Nias Gunungsitoli General Hospital, Nias, Indonesia; Division of Gastroentero-Hepatology, Department of Internal Medicine, Faculty of Medicine, Sriwijaya University, Palembang, Indonesia; Division of Gastroenterology, Department of Internal Medicine, Faculty of Medicine, Andalas University, Padang, Indonesia; Department of Internal Medicine, Cimacan General Hospital, Cianjur, Indonesia; Division of Gastroentero-Hepatology, Department of Internal Medicine, Faculty of Medicine, University of Sumatera Utara, Medan, Indonesia; Division of Gastroentero-Hepatology, Department of Internal Medicine, Faculty of Medicine-Dr Soetomo Teaching Hospital, Universitas Airlangga, Jalan Mayjend Prof. Dr. Moestopo No. 6-8, Surabaya, 60286, Indonesia; Department of Environmental and Preventive Medicine, Oita University Faculty of Medicine, 1-1 Idaigaoka, Hasama Machi, Yufu City, Oita, 879-5593, Japan; Department of Medicine, Gastroenterology and Hepatology Section, Baylor College of Medicine, Houston, TX, United States


Background: Even though the incidence of H. pylori infection among Malays in the Malay Peninsula is low, we observed a high H. pylori prevalence in Sumatra, which is the main residence of Indonesian Malays. H. pylori prevalence among Indonesian Malay descendants was investigated. Results: Using a combination of five tests, 232 recruited participants were tested for H- pylori and participants were considered positive if at least one test positive. The results showed that the overall H. pylori prevalence was 17.2%. Participants were then categorized into Malay (Aceh, Malay, and Minang), Java (Javanese and Sundanese), Nias, and Bataknese groups. The prevalence of H. pylori was very low among the Malay group (2.8%) and no H. pylori was observed among the Aceh. Similarly, no H. pylori was observed among the Java group. However, the prevalence of H. pylori was high among the Bataknese (52.2%) and moderate among the Nias (6.1%). Multilocus sequence typing showed that H. pylori in Indonesian Malays classified as hpEastAsia with a subpopulation of hspMaori, suggesting that the isolated H. pylori were not a specific Malays H. pylori. Conclusions: Even though the ethnic groups live together as a community, we observed an extremely low H. pylori infection rate among Indonesian Malay descendants with no specific Indonesian Malay H. pylori. The results suggest that H. pylori was not originally among these groups and H. pylori was imported from other ethnic groups. © 2021, The Author(s).

Epidemiology; Helicobacter pylori; Malays; Population genetics; Prevalence; Sumatra


Gut Pathogens

Publisher: BioMed Central Ltd

Volume 13, Issue 1, Art No 36, Page – , Page Count

Journal Link: https://www.scopus.com/inward/record.uri?eid=2-s2.0-85107355307&doi=10.1186%2fs13099-021-00432-6&partnerID=40&md5=50dff7290d04b23d89863e54b90dceb8

doi: 10.1186/s13099-021-00432-6

Issn: 17574749

Type: All Open Access, Gold, Green


Amieva, M., Peek, R.M., Pathobiology of Helicobacter pylori-Induced Gastric Cancer (2016) Gastroenterology. W.B. Saunders, pp. 64-78. , https://doi.org/10.1053/j.gastro.2015.09.004; Hooi, J.K.Y., Lai, W.Y., Ng, W.K., Suen, M.M.Y., Underwood, F.E., Tanyingoh, D., Global prevalence of helicobacter pylori infection: systematic review and meta-analysis (2017) Gastroenterology, 153, pp. 420-429; Graham, D.Y., History of Helicobacter pylori, duodenal ulcer, gastric ulcer and gastric cancer (2014) World J Gastroenterol, 20, pp. 5191-5204; Hatin, W.I., Nur-Shafawati, A.R., Zahri, M.K., Xu, S., Jin, L., Tan, S.G., Population genetic structure of peninsular Malaysia Malay sub-ethnic groups (2011) PLoS ONE., 6; Languange and Literature (2004) Encycl Malaysia; Din, M.A.O., The Malay Origin: Rewrite Its History (2011) J Melayu, 7, pp. 1-81; Fix, A.G., Malayan paleosociology: implications for patterns of genetic variation amongst the Orang Asli (1995) Am Anthropol, 97, pp. 313-323; Sysling, F., (2016) Racial Science and Human Diversity in Colonial Indonesia, , NUS Press; Hatin, W.I., Nur-Shafawati, A.R., Etemad, A., Jin, W., Qin, P., Xu, S., A genome wide pattern of population structure and admixture in peninsular Malaysia Malays (2014) Hugo J., 8, p. 5; Pitoyo, A.J., Triwahyudi, H., Dinamika Perkembangan Etnis di Indonesia Dalam Konteks Persatuan Negara (2017) Populasi, 25, pp. 64-81; Goh, K.L., Parasakthi, N., The racial cohort phenomenon: seroepidemiology of Helicobacter pylori infection in a multiracial South-East Asian country (2001) Eur J Gastroenterol Hepatol., 13, pp. 177-183; Syam, A.F., Miftahussurur, M., Makmun, D., Nusi, I.A., Zain, L.H., Risk Factors and Prevalence of Helicobacter pylori in Five Largest Islands of Indonesia: A Preliminary Study (2015) PLoS ONE, 10; Miftahussurur, M., Tuda, J., Suzuki, R., Kido, Y., Kawamoto, F., Matsuda, M., Extremely low Helicobacter pylori prevalence in North Sulawesi, Indonesia and identification of a Maori-tribe type strain: a cross sectional study (2014) Gut Pathog, 6, p. 42; Moodley, Y., Linz, B., Yamaoka, Y., Windsor, H.M., Breurec, S., Wu, J.Y., The peopling of the Pacific from a bacterial perspective (2009) Science., 323, pp. 527-530; Sasidharan, S., Jo, S., Lachumy, T., Ravichandran, M., Latha, Y., Rao, S., Epidemiology of Helicobacter pylori among multiracial community in Northern Peninsular, Malaysia: effect of age across race and gender (2011) Asian Pac J Trop Med, 4, pp. 72-75; Thevakumar, K., Chandren, J.R., Perez-Perez, G.I., Chua, E.G., Teh, L.K., Salleh, M.Z., Assessment of Risk and Sero-Prevalence of Helicobacter pylori Colonization among Remote Orang Asli Tribes in Peninsula Malaysia (2016) PLoS ONE, 11; Rajendra, S., Ackroyd, R., Robertson, I.K., Ho, J.J., Karim, N., Kutty, K.M., Helicobacter pylori, ethnicity, and the gastroesophageal reflux disease spectrum: A study from the East (2007) Helicobacter, 12, pp. 177-183; Kang, J.Y., Yeoh, K.G., Ho, K.Y., Guan, R., Lim, T.P., Quak, S.H., Racial differences in Helicobacter pylori seroprevalence in Singapore: correlation with differences in peptic ulcer frequency (1997) J Gastroenterol Hepatol, 12, pp. 655-659; Maran, S., Lee, Y.Y., Xu, S.H., Raj, M.S., Abdul Majid, N., Choo, K.E., Towards understanding the low prevalence of Helicobacter pylori in Malays: Genetic variants among Helicobacter pylori -negative ethnic Malays in the north-eastern region of Peninsular Malaysia and Han Chinese and South Indians (2013) J Dig Dis, 14, pp. 196-202; Schmidt, H.M.A., Ha, D.M., Taylor, E.F., Kovach, Z., Goh, K.L., Fock, K.M., Variation in human genetic polymorphisms, their association with Helicobacter pylori acquisition and gastric cancer in a multi-ethnic country (2011) J Gastroenterol Hepatol, 26, pp. 1725-1732; Goh, K.L., Lessons learnt from the epidemiology of Helicobacter pylori infection in Malaysia: JGHF Marshall and Warren Lecture 2017 (2018) J Gastroenterol Hepatol (Australia).; Ansari, S., Yamaoka, Y., Helicobacter pylori virulence factors exploiting gastric colonization and its pathogenicity (2019) Toxins.; Lee, Y.Y., Ismail, A.W., Mustaffa, N., Musa, K.I., Majid, N.A., Choo, K.E., Sociocultural and dietary practices among malay subjects in the north-eastern region of peninsular Malaysia: a region of low prevalence of Helicobacter pylori Infection (2012) Helicobacter, 17, pp. 54-61; Sairam, K., Rao, C.V., Goel, R.K., Effect of Centella asiatica Linn on physical and chemical factors induced gastric ulceration and secretion in rats (2001) Indian J Exp Biol, 39, pp. 137-142. , COI: 1:CAS:528:DC%2BD3MXhvVartLo%3D, PID: 11480209; Pasaribu, K.M., Gea, S., Ilyas, S., Tamrin, T., Sarumaha, A.A., Sembiring, A., Fabrication and in-vivo study of micro-colloidal Zanthoxylum acanthopodium-loaded bacterial cellulose as a burn wound dressing (2020) Polymers (Basel).; Majumder, M., Sharma, H.K., Zaman, K., Lyngdoh, W., Evaluation of physico-chemical properties and antibacterial activity of the essential oil obtained from the fruits of Zanthoxyllum acanthopodium DC. Collected from Meghalaya (2014) India. TIC., 1, p. e10; Yurliasni, Y., Aktivitas Antimikroba Khamir Asal Dadih (susu kerbau fermentasi) Terhadap Beberapa Bakteri Patogen (2010) J Agripet, 10, pp. 19-24; Leng, J., Prehistory of the Indo-Malaysian Archipelago. Peter Bellwood. 1997. Revised edition. University of Hawai’i Press, Honolulu, x + 385 pp., 92 figures, 61 plates, 3 tables, notes, references, index. $58.00 (cloth), $32.95 (paper) (1998) Am Antiq, 63, pp. 518-519. , –,., https://doi.org/10.2307/2694651; Goto, Y., Syam, A.F., Darnindro, N., Hapsari, F.C.P., Risk factors for and prevalence of helicobacter pylori infection among healthy inhabitants in Northern Jakarta Indonesia (2016) Asian Pacific J Cancer Prev, 17, pp. 4469-4475; Yang, X., Nishibayashi, H., Takeshita, T., Morimoto, K., Prevalence of Helicobacter pylori infection in Japan: Relation to educational levels and hygienic conditions (1999) Environ Health Prev Med, 3, pp. 202-206; Karita, M., Teramukai, S., Matsumoto, S., Risk of Helicobacter pylori transmission from drinking well water is higher than that from infected intrafamilial members in Japan (2003) Dig Dis Sci, 48, pp. 1062-1067; Miftahussurur, M., Noninvasive Helicobacter pylori Diagnostic Methods in Indonesia Gut and Liver. Editorial Office of Gut and Liver, 2020, pp. 553-559. , https://doi.org/10.5009/GNL19264; Makmun, D., Present status of endoscopy, therapeutic endoscopy and the endoscopy training system in Indonesia (2014) Dig Endosc, 26, pp. 2-9; Juniawan, R.F.D., Awalia, A., Henoch-Schönlein purpura: management and complication (2020) Biomol Heal Sci J, 3, pp. 113-1115; Miftahussurur, M., Waskito, L.A., Syam, A.F., Nusi, I.A., Wibawa, I., Rezkitha, Y.A.A., Analysis of risks of gastric cancer by gastric mucosa among Indonesian ethnic groups (2019) PLoS ONE., 14, pp. 1-19; Miftahussurur, M., Syam, A.F., Nusi, I.A., Makmun, D., Waskito, L.A., Zein, L.H., Surveillance of Helicobacter pylori antibiotic susceptibility in Indonesia: different resistance types among regions and with novel genetic mutations (2016) PLoS One.; Dixon, M.F., Genta, R.M., Yardley, J.H., Correa, P., Classification and grading of gastritis. The updated Sydney System. International Workshop on the Histopathology of Gastritis, Houston 1994 (1996) Am J Surg Pathol, 20, pp. 1161-1181; Uchida, T., Kanada, R., Tsukamoto, Y., Hijiya, N., Matsuura, K., Yano, S., Immunohistochemical diagnosis of the cagA-gene genotype of Helicobacter pylori with anti-East Asian CagA-specific antibody (2007) Cancer Sci, 98, pp. 521-528; Vilaichone, R.K., Mahachai, V., Shiota, S., Uchida, T., Ratanachu-ek, T., Tshering, L., Extremely high prevalence of Helicobacter pylori infection in Bhutan (2013) World J Gastroenterol., 19, pp. 2806-2810; Shiota, S., Matsunari, O., Watada, M., Yamaoka, Y., Serum Helicobacter pylori CagA antibody as a biomarker for gastric cancer in east-Asian countries (2010) Futur Microbiol, 5, pp. 1885-1893; Shiota, S., Cruz, M., Abreu, J.A., Mitsui, T., Terao, H., Disla, M., Virulence genes of Helicobacter pylori in the Dominican Republic (2014) J Med Microbiol, 63, pp. 1189-1196; Nguyen, T.L., Uchida, T., Tsukamoto, Y., Trinh, D.T., Ta, L., Mai, B.H., Helicobacter pylori infection and gastroduodenal diseases in Vietnam: a cross-sectional, hospital-based study (2010) BMC Gastroenterol, 10, p. 114; Miftahussurur, M., Syam, A.F., Makmun, D., Nusi, I.A., Zein, L.H., Helicobacter pylori virulence genes in the five largest islands of Indonesia (2015) Gut Pathog., 7, p. 26; Miftahussurur, M., Nusi, I.A., Akil, F., Syam, A.F.A.F., Wibawa, I.D., Rezkitha, Y.A., Gastric mucosal status in populations with a low prevalence of Helicobacter pylori in Indonesia (2017) PLoS One., 12, pp. 1-15; Pritchard, J.K., Stephens, M., Donnelly, P., Inference of population structure using multilocus genotype data (2000) Genetics, 155, pp. 945-959. , COI: 1:STN:280:DC%2BD3cvislKrtA%3D%3D; Linz, B., Balloux, F., Moodley, Y., Manica, A., Liu, H., Roumagnac, P., An African origin for the intimate association between humans and Helicobacter pylori (2007) Nature, 445, pp. 915-918; Falush, D., Wirth, T., Linz, B., Pritchard, J.K., Stephens, M., Kidd, M., Traces of human migrations in Helicobacter pylori populations (2003) Science., 299, pp. 1582-1585; Kumar, S., Stecher, G., Tamura, K., MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets (2016) Mol Biol Evol., 33, pp. 1870-1874; Saitou, N., Nei, M., The neighbor-joining method: a new method for reconstructing phylogenetic trees (1987) Mol Biol Evol, 4, pp. 406-425; Kimura, M., A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences (1980) J Mol Evol, 16, pp. 111-120

Indexed by Scopus

Leave a Comment