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. 2022 Jan 5;2:126–129. doi: 10.1016/j.ijregi.2021.12.012

Seroepidemiological survey of the prevalence of Helicobacter pylori infection in Sabah, Malaysia

Daisuke Mori a,1, Jecelyn Leaslie John b,1, Shahnaz Irwani Binti Sabri c, Saliz Mazrina Binti Shaharom c, Hidekatsu Iha d, Yoshio Yamaoka e, Takashi Matsumoto e,⁎, Kamruddin Ahmed a,b,⁎
PMCID: PMC9216690  PMID: 35757073

Highlights

  • •

    The prevalence of Helicobacter pylori was 28.4%, and was highest in subjects aged 30–39 years.

  • •

    Men were more likely to be infected than women.

  • •

    The H. pylori infection rate was highest among those of Kadazan (19.1%) ethnicity.

  • •

    Chinese and Malay ethnicities were protective against H. pylori infection.

Keywords: Helicobacter pylori, Seroepidemiology, Humans, Sabah, Malaysia

Abstract

Objective

Gastric cancer is an important cause of mortality in Sabah, Malaysia, but the prevalence of Helicobacter pylori infection in this state is unknown. Serology is an important tool for the surveillance of H. pylori infection. The objective of this study was to determine the prevalence of H. pylori infection by serology, and to provide information for policy discussions on H. pylori control programmes in Sabah.

Methods

This cross-sectional study analysed serum samples collected from blood donors in a hospital in Kota Kinabalu, Sabah. H. pylori antibody concentration was measured using a commercially available kit.

Results

The prevalence of H. pylori was 28.4% (204/718), and the infection rate was highest in subjects aged 30–39 years. Men were more likely to be infected than women. The H. pylori infection rate was highest among those of Kadazan (19.1%) ethnicity, followed by Dusun (15.7%), Bajau (14.7%) and Rungus (10.8%). Binary logistic regression analysis indicated that Chinese (P=0.026) and Malay (P=0.035) ethnicities were protective against H. pylori infection compared with other ethnicities.

Conclusions

The seropositivity rate of H. pylori in this study was similar to the overall seropositivity rate in Malaysia; however, Chinese and Malay ethnicities were found to be protective against H. pylori infection.

Introduction

Helicobacter pylori is a helically shaped, motile, Gram-negative bacterium (Alzahrani et al., 2014) that was first identified in 1982 and named Campylobacter pylori but later classified in the genus Helicobacter (Robin Warren and Marshall, 1983; Goodwin et al., 1989). H. pylori infects the stomach and can cause ulcers, inflammation of the stomach lining, and cancer (Yamaoka, 2010). Gastric cancer is one of the main causes of cancer-related death worldwide, accounting for 769 million deaths each year (Bray et al., 2018; Rawla and Barsouk, 2019; Sung et al., 2021). People infected with H. pylori have a six-fold higher risk of developing gastric cancer (Vohlonen et al., 2016). This infection can be acquired during childhood, and the risk of infection is strongly related to lifestyle factors such as living in crowded conditions, living without good sanitation, and living with infected individuals (Kusters et al., 2006). Infection occurs by direct person-to-person transmission via either the oral–oral or faecal–oral route (Allaker et al., 2002). Although no vaccine against H. pylori is currently available, the development of a vaccine is considered to be a powerful tool for preventing gastric cancer (Sutton and Boag, 2019).

In Malaysia, studies have shown a seropositive rate for H. pylori of 14.1–55% among blood donors (Uyub et al., 1994; Goh and Parasakthi, 2001; Sasidharan and Uyub, 2009). In studies of ethnic groups within Malaysia, the infection rate was reported to be higher in people of Chinese and Indian ethnicities than in those of Malay ethnicity (Goh and Parasakthi, 2001; Kaur and Naing, 2003; Alfizah et al., 2010). Most of these studies were performed in west Malaysia, and few studies have been undertaken in Sabah, a state with various ethnic groups that showed a high seroprevalence rate of 55% in a study conducted 16 years ago (Goh and Parasakthi, 2001). Although the seroprevalence of H. pylori is closely related to the incidence of gastric cancer (Rahman et al., 2014), the incidence of gastric cancer is low (range 4.3–5.9%) (Kaur et al., 2016, Suleiman et al., 2015). This discrepancy suggests that further studies are needed to determine the prevalence of H. pylori among the people of Sabah. However, testing for H. pylori by tissue biopsy and culture is impractical for a large number of people, and analysis using serology may be a more practical method to determine the prevalence of H. pylori among the population. Therefore, this surveillance study was conducted to determine the prevalence of H. pylori and to provide data for policy discussions on H. pylori control programmes in Sabah.

Materials and methods

The study

From August 2016 to April 2019, blood samples were collected from blood donors who attended the Department of Blood Transfusion for blood donation at Hospital Queen Elizabeth II, Kota Kinabalu, Sabah, Malaysia. Physically and mentally healthy blood donors aged ≥18 years were enrolled in this study. Selection of participants was also based on the distribution of the major ethnic groups in Sabah. For each ethnic group, when ≥100 samples were collected, the first 100 samples were analysed, but when ≤100 samples were collected, all samples were analysed for antibodies against H. pylori.

Demographic data including gender, age and ethnicity were recorded as the possible independent predictors of, or protective factors against, infection. Three millilitres of blood were collected from each participant, left at room temperature for clot formation, and centrifuged at 3000 rpm for 15 min to separate the serum. The serum was transferred to a cryotube using sterile procedures, and serum samples were transported via cold chain to the laboratory of Borneo Medical and Health Research Centre, Universiti Malaysia Sabah. Samples were stored at –80°C until further analysis.

The concentration of serum antibodies against H. pylori was measured with a solid-phase two-step sandwich enzyme immunoassay using a commercial kit (E-Plate Eiken H. pylori antibody II, Eiken Chemical Co., Ltd., Tokyo, Japan) according to the manufacturer's instructions. The cut-off value of 10 U/mL was considered to be a positive indicator of antibodies against H. pylori. The sensitivity and specificity of this kit are 91.2% and 97.4%, respectively (Ueda et al., 2014).

Statistical analysis was performed using SPSS Version 27 (IBM Corp., Armonk, NY, USA). All categorical variables are described as frequency and percentage. Chi-squared test was used to investigate the associations of H. pylori infection with gender, age group and ethnicity. Variables with P<0.05 in the univariate analyses were selected for multi-variate analysis using binary logistic regression to examine their relationship with H. pylori infection. Odds ratios (ORs) and 95% confidence intervals (CIs) were calculated, and P-values <0.05 were considered to indicate significance.

Ethical approval

The authors assert that all procedures contributing to this work comply with the ethical standards of the relevant national and institutional committees on human experimentation and with the Helsinki Declaration of 1975, as revised in 2008 and approved by Medical Research and Ethics Committee, Ministry of Health Malaysia (NMRR-19-699-47195).

Results

Serum samples were collected from 718 blood donors. Their mean age was 34.8 years (range 18–66 years). The male-to-female ratio was 3.4:1, with 556 (77.4%) men and 162 (22.6%) women. Blood donors were from 14 ethnic groups; most were Kadazan, followed by Dusun, Bajau, Malay and Chinese.

The prevalence of serum antibodies against H. pylori was 28.4% (204/718). The male-to-female ratio of seropositive samples was 3.4:1, with 158 (77.5%) and 46 (22.5%) positive samples from men and women, respectively. The H. pylori infection rate was highest in people of Kadazan (19.1%, 39/204) ethnicity, followed by Dusun (15.7%, 32/204), Bajau (14.7%, 30/204) and Rungus (10.8%, 22/204). The sample was classified according to six age group categories: 18–19, 20–29, 30–39, 40–49, 50–59 and 60–69 years. The highest infection rate was in subjects aged 30–39 years. The prevalence of H. pylori seropositivity differed significantly between ethnic groups (P=0.000), but did not differ between men and women (P=0.825) or between age groups (P=0.936) (Table 1). The univariate analysis showed that people of Chinese (P=0.000), Kadazan (P=0.011), Malay (P=0.001) and Rungus (P=0.000) ethnicities had higher seroprevalence for H. pylori than other ethnic groups. Binary logistic regression analysis (Table 2) showed that being Chinese (P=0.026) and Malay (P=0.035) were significant protective factors against having H. pylori infection compared with other ethnic groups.

Table 1.

Demographic characteristics and univariate analysis of Helicobacter pylori infection among blood donors (n=718).

Total subjects n (%) Positive n (%) OR (95% CI) P-value
Gender
 Male 556 (77.4) 158 (77.5) 0.96 (0.65–1.41) 0.825
 Female 162 (22.6) 46 (22.5) Reference
Age group (years)
 18–19 10 (1.4) 2 (1.0) 0.63 (0.13–2.97) 0.553
 20–29 234 (32.6) 63 (30.9) 0.90 (0.63–1.27) 0.538
 30–39 243 (33.8) 68 (33.3) 0.97 (0.69–1.37) 0.855
 40–49 141 (19.6) 44 (21.6) 1.18 (0.79–1.76) 0.412
 50–59 83 (11.6) 25 (12.3) 1.10 (0.67–1.81) 0.714
 60–69 7 (1.0) 2 (1.0) Reference
Ethnicity
 Bajau 100 (13.9) 30 (14.7) 1.09 (0.69–1.74) 0.704
 Bisaya 13 (1.8) 2 (1.0) 0.45 (0.10–2.06) 0.293
 Brunei 71 (10) 25 (12.3) 1.42 (0.85–2.38) 0.181
 Bugis 15 (2.1) 4 (2.0) 0.91 (0.29–2.91) 0.880
 Chinese 100 (13.9) 13 (6.4) 0.33 (0.18–0.61) 0.000
 Dusun 100 (13.9) 32 (15.7) 1.22 (0.77–1.92) 0.391
 Iban 9 (1.3) 2 (1.0) 0.72 (0.15–3.48) 0.679
 Indian 10 (1.4) 2 (1.0) 0.63 (0.13–2.97) 0.553
 Kadazan 100 (13.9) 39 (19.1) 1.76 (1.13–2.72) 0.011
 Malay 100 (13.9) 14 (6.9) 0.37 (0.20–0.66) 0.001
 Murut 19 (2.6) 9 (4.4) 2.33 (0.93–5.81) 0.063
 Rungus 42 (5.8) 22 (10.8) 2.99 (1.59–5.60) 0.000
 Sino Dusun/Kadazan 26 (3.6) 5 (2.5) 0.59 (0.22–1.59) 0.290
 Sungai 13 (1.8) 5 (2.5) Reference
Open in a new tab

OR, odds ratio; CI, confidence interval.

Table 2.

Binary logistic regression of Helicobacter pylori seropositivity according to ethnicity (n=718).

Adjusted OR 95% CI P-value
Ethnicity
 Chinese 0.24 0.07–0.84 0.026
 Malay 0.26 0.07–0.91 0.035
Open in a new tab

OR, odds ratio; CI, confidence interval.

Discussion

Globally, there is a declining trend in the seroprevalence of H. pylori, and Malaysia is reflecting this trend (Hooi et al., 2017; Hee et al., 2018; Hanafiah et al., 2019). In agreement with this trend, the H. pylori seropositivity rate (28.4%) in the present study was considerably lower than the rate of 55.0% reported 16 years ago (Goh and Parasakthi, 2001). The rate in the current study is also similar to the rate of 28.6% for Malaysia as a whole (Hooi et al., 2017). However, the seroprevalence of H. pylori is lower in neighbouring Indonesia (14.3–22.1%) (Syam et al., 2015). In contrast, the seroprevalence of H. pylori is higher in neighbouring Thailand and the Philippines (54.1–76.1% and 60%, respectively) (Destura et al., 2004; Sahara et al., 2012). The reasons behind the declining seroprevalence rate in Sabah are unknown but may reflect improvements in the sanitation system (Tan and Goh, 2008; Watanabe et al., 2015). Differences between the test kits used in these studies may also affect the detection of seroprevalence (Vaira et al., 1994). However, the lower prevalence of H. pylori found in this study may explain the low prevalence of gastric cancer in Sabah (Kaur et al., 2016).

Similar to a trend reported previously (Goh and Parasakthi, 2001), the present study also found that men were more likely to be seropositive for H. pylori than women. However, other studies have not found a gender difference in seroprevalence (De Martel and Parsonnet, 2006; Franck et al., 2017; Bálint et al., 2019), which may reflect genetic variations between people living in different geographic regions. Also in agreement with a previous study (Goh and Parasakthi, 2001), the present study found that people aged 20–39 years were at higher risk of testing positive for H. pylori compared with those aged ≥40 years. Another study reported that subjects aged 41–60 years had significantly lower prevalence because of declining H. pylori strains that carry the CagA virulence factor (Franck et al., 2017).

According to the racial cohort theory proposed in other studies, the rate of H. pylori infection is higher in people of Chinese and Indian ethnicities than in those of Malay ethnicity (Kang et al., 1990; Goh, 1997; Goh and Parasakthi, 2001). As in the present study, Goh and Parasakthi (2001) found that the rate of infection was highest in people of Kadazan ethnicity in Malaysia. However, the binary logistic multi-variate analysis in the present study showed that Chinese and Malay ethnicities were protective against H. pylori infection, and that seroprevalence was low and similar in both groups. Other studies have reported that ethnicity is a major significant risk factor for H. pylori infection in regions where the levels of H. pylori strains with different CagA virulence factors differ between ethnic groups ( Den Hollander et al., 2013, Goh, 1997). The presence of different virulence factors of H. pylori can also influence the outcome of infection in different ethnic groups (Hanafiah and Lopes, 2020). More studies are needed to identify the virulence factors carried by H. pylori colonizing people of Chinese and Malay ethnicities in Sabah. It is possible that the similarity in host genetic factors between people of Chinese and Malay ethnicities may be related to their similar susceptibility to H. pylori infection (Tan and Goh, 2008).

Although there is no universally accepted single test for the diagnosis of H. pylori infection, culture and histology results are considered as the gold standards (Rojas-Rengifo et al., 2019). Studies showed that when culture was taken as the gold standard, the sensitivity and specificity of serological tests were 80–95% and 80 – 95%, respectively (Logan and Delaney, 2001). When histology was considered as the gold standard, the sensitivity and specificity of serological tests were 76–84% and 79–90%, respectively (Chey and Wong, 2007). Furthermore, the sensitivity, specificity, and positive and negative predictive values of different commercially available serological tests vary considerably (Burucoa et al., 2013). Despite these limitations, serological testing is a convenient method for mass screening for H. pylori infection. In the present study, there was a possibility of misidentification of H. pylori infection due to the use of serological testing.

The major limitations of this study are that most of the blood donors were men and, because of limited resources, only three variables were included in this study. Other factors, such as diet, genetic predisposition, environmental and socio-economic conditions, and cultural background, are crucial factors that can affect susceptibility to H. pylori infection, and should be included in future studies. In addition, future studies could enrol family members to examine the role of intrafamily transmission, which has been reported to be important to the spread of H. pylori. Despite these limitations, this cross-sectional study provides updated data on the seroprevalence of H. pylori infection among the population of Sabah. These data can be used to support regional initiatives for H. pylori surveillance, prevention and eradication programmes.

In conclusion, this study found a relatively low seroprevalence rate for H. pylori among the population of Sabah, and that people aged <40 years were mainly affected. Chinese and Malay ethnicities seem to be protective against the development of H. pylori infection in this population.

Acknowledgments

Acknowledgements

The authors wish to thank the Director General of Health Malaysia for the permission to publish this article. The authors also wish to thank the staff of the Department of Blood Transfusion, Hospital Queen Elizabeth II, Kota Kinabalu, Sabah for full support and cooperation during sample collection.

Conflict of interest statement

None declared.

Funding

This study was supported by Launching Grant for Centre of Excellence from Universiti Malaysia Sabah (Grant No. AM18006). The funder had no role in the study design; collection, analysis and interpretation of data; writing of the manuscript; and the decision to submit the manuscript for publication.

Ethical approval

The study was approved by Medical Research and Ethics Committee, Ministry of Health Malaysia (NMRR-19-699-47195).

Author contributions

Conceived and designed the study: YY, TM and KA.

Collected samples and data: SIBS and SMBS.

Performed experiments: DM and JLJ

Analysed the data: DM, JLJ, SIBS, SMBS, YY, TM and KA.

Supervised the study: SIBS, TM and KA.

Initial manuscript drafting: JLJ and KA.

Final manuscript writing: DM, JLJ, SIBS, SMBS, YY, TM and KA.

All authors critically revised the manuscript for intellectual content and approved the final version submitted for publication.

Contributor Information

Takashi Matsumoto, Email: tmatsumoto9@oita-u.ac.jp.

Kamruddin Ahmed, Email: ahmed@ums.edu.my.

References

  1. Alfizah H, Am R, Mr I, Aminuddin A, Ay J. Four year analysis of Helicobacter pylori infection among patients with dyspepsia at Universiti Kebangsaan Malaysia Medical Centre. Med Heal. 2010;5:13–21. [Google Scholar]
  2. Allaker RP, Young KA, Hardie JM, Domizio P, Meadows NJ. Prevalence of Helicobacter pylori at oral and gastrointestinal sites in children: evidence for possible oral-to-oral transmission. J Med Microbiol. 2002;51:312–317. doi: 10.1099/0022-1317-51-4-312. [DOI] [PubMed] [Google Scholar]
  3. Alzahrani S, Lina TT, Gonzalez J, Pinchuk I.V., Beswick EJ, Reyes VE. Effect of Helicobacter pylori on gastric epithelial cells. World J Gastroenterol. 2014;20:12767–12780. doi: 10.3748/wjg.v20.i36.12767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bálint L, Tiszai A, Kozák G, Dóczi I, Szekeres V, Inczefi O, et al. Epidemiologic characteristics of Helicobacter pylori infection in southeast Hungary. World J Gastroenterol. 2019;25:6365–6372. doi: 10.3748/wjg.v25.i42.6365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68:394–424. doi: 10.3322/caac.21492. [DOI] [PubMed] [Google Scholar]
  6. Burucoa C, Delchier J-C, Courillon-Mallet A, de Korwin J-D, Mégraud F, Zerbib F, et al. Comparative evaluation of 29 commercial Helicobacter pylori serological kits. Helicobacter. 2013;18:169–179. doi: 10.1111/hel.12030. [DOI] [PubMed] [Google Scholar]
  7. Chey WD, Wong BCY. American College of Gastroenterology guideline on the management of Helicobacter pylori infection. Am J Gastroenterol. 2007;102:1808–1825. doi: 10.1111/j.1572-0241.2007.01393.x. [DOI] [PubMed] [Google Scholar]
  8. De Martel C, Parsonnet J. Helicobacter pylori infection and gender: a meta-analysis of population-based prevalence surveys. Dig Dis Sci. 2006;51:2292–2301. doi: 10.1007/s10620-006-9210-5. [DOI] [PubMed] [Google Scholar]
  9. Den Hollander WJ, Holster IL, den Hoed CM, van Deurzen F, van Vuuren AJ, Jaddoe VW, et al. Ethnicity is a strong predictor for Helicobacter pylori infection in young women in a multi-ethnic European city. J Gastroenterol Hepatol. 2013;28:1705–1711. doi: 10.1111/jgh.12315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Destura RV, Labio ED, Barrett LJ, Alcantara CS, Gloria VI, Daez MLO, et al. Laboratory diagnosis and susceptibility profile of Helicobacter pylori infection in the Philippines. Ann Clin Microbiol Antimicrob. 2004;3:2–7. doi: 10.1186/1476-0711-3-25. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Franck C, Hoffmann A, Link A, Schulz C, Wuttig K, Becker E, et al. Prevalence of Helicobacter pylori infection among blood donors in Saxony-Anhalt, Germany – a region at intermediate risk for gastric cancer. Z Gastroenterol. 2017;55:653–656. doi: 10.1055/s-0043-106311. [DOI] [PubMed] [Google Scholar]
  12. Goh KL. Prevalence of and risk factors for Helicobacter pylori infection in a multi-racial dyspeptic Malaysian population undergoing endoscopy. J Gastroenterol Hepatol. 1997;12:S29–S35. doi: 10.1111/j.1440-1746.1997.tb00455.x. [DOI] [PubMed] [Google Scholar]
  13. Goh KL, Parasakthi N. The racial cohort phenomenon: Seroepidemiology of Helicobacter pylori infection in a multiracial South-east Asian country. Eur J Gastroenterol Hepatol. 2001;13:177–183. doi: 10.1097/00042737-200102000-00014. [DOI] [PubMed] [Google Scholar]
  14. Goodwin CS, Armstrong JA, Chilvers T, Peters M, Collins MD, Sly L, et al. Transfer of Campylobacter pylori and Campylobacter mustelae to Helicobacter gen. nov. as Helicobacter pylori comb. nov. and Helicobacter mustelae comb. nov., respectively. Int J Syst Bacteriol. 1989;39:397–405. [Google Scholar]
  15. Hanafiah A, Binmaeil H, Ali RAR, Rose IM, Lopes BS. Molecular characterization and prevalence of antibiotic resistance in Helicobacter pylori isolates in Kuala Lumpur. Malaysia. Infect Drug Resist. 2019;12:3051–3061. doi: 10.2147/IDR.S219069. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hanafiah A, Lopes BS. Genetic diversity and virulence characteristics of Helicobacter pylori isolates in different human ethnic groups. Infect Genet Evol. 2020;78 doi: 10.1016/j.meegid.2019.104135. [DOI] [PubMed] [Google Scholar]
  17. Hee S, Id L, Id NK, Kwon JW, Kim SE, Baik GH, et al. Trends in the seroprevalence of Helicobacter pylori infection and its putative eradication rate over 18 years in Korea: a cross-sectional nationwide multicenter study. PLoS One. 2018;13 doi: 10.1371/journal.pone.0204762. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hooi JKY, Lai WY, Ng WK, Suen MMY, Underwood FE, Tanyingoh D, et al. Global prevalence of Helicobacter pylori infection: systematic review and meta-analysis. Gastroenterology. 2017;153:420–429. doi: 10.1053/j.gastro.2017.04.022. [DOI] [PubMed] [Google Scholar]
  19. Kang JY, Wee A, Math MV, Guan R, Tay HH, Yap I, et al. Helicobacter pylori and gastritis in patients with peptic ulcer and non-ulcer dyspepsia: ethnic differences in Singapore. Gut. 1990;31:850–853. doi: 10.1136/gut.31.8.850. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kaur G, Naing NN. Prevalence and ethnic distribution of Helicobacter pylori infection among endoscoped patients in North Eastern Peninsular Malaysia. Malay J Med Sci. 2003;10:66–70. [PMC free article] [PubMed] [Google Scholar]
  21. Kaur N, Abu Bakar SN, Lim JH, Sanudin NH, Chiu AEL, Mat Said M, et al. Sabah Cancer Registry Report 2012–2016. State Health Department; Sabah, Malaysia: Sabah: 2016. [Google Scholar]
  22. Kusters JG, Van Vliet AHM, Kuipers EJ. Pathogenesis of Helicobacter pylori infection. Clin Microbiol Rev. 2006;19:449–490. doi: 10.1128/CMR.00054-05. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Logan R, Delaney B. ABC of the upper gastrointestinal tract: implications of dyspepsia for the NHS. BMJ. 2001;323:675–677. doi: 10.1136/bmj.323.7314.675. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Rahman R, Asombang AW, Ibdah JA. Characteristics of gastric cancer in Asia. World J Gastroenterol. 2014;20:4483–4490. doi: 10.3748/wjg.v20.i16.4483. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Rawla P, Barsouk A. Epidemiology of gastric cancer: global trends, risk factors and prevention. Prz Gastroenterol. 2019;14:26–38. doi: 10.5114/pg.2018.80001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Robin Warren J, Marshall B. Unidentified curved bacilli on gastric epithelium in active chronic gastritis. Lancet. 1983;321:1273–1275. [PubMed] [Google Scholar]
  27. Rojas-Rengifo DF, Mendoza B, Jaramillo C, Rodríguez-Urrego PA, Vera-Chamorro JF, Alvarez J, et al. Helicobacter pylori culture as a key tool for diagnosis in Colombia. J Infect Develop Countr. 2019;13:720–726. doi: 10.3855/jidc.10720. [DOI] [PubMed] [Google Scholar]
  28. Sahara S, Sugimoto M, Vilaichone RK, Mahachai V, Miyajima H, Furuta T, et al. 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;12:1. doi: 10.1186/1471-2334-12-223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Sasidharan S, Uyub AM. Prevalence of Helicobacter pylori infection among asymptomatic healthy blood donors in Northern Peninsular Malaysia. Trans R Soc Trop Med Hyg. 2009;103:395–398. doi: 10.1016/j.trstmh.2008.11.021. [DOI] [PubMed] [Google Scholar]
  30. Suleiman M, Kaur N, Ahmad N, Mat Said M. Sabah Cancer Registry Report 2006-2010. Sabah State Health Department; Sabah, Malaysia: 2015. [Google Scholar]
  31. Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, et al. Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71:209–249. doi: 10.3322/caac.21660. [DOI] [PubMed] [Google Scholar]
  32. Sutton P, Boag JM. Status of vaccine research and development for Helicobacter pylori. Vaccine. 2019;37:7295–7299. doi: 10.1016/j.vaccine.2018.01.001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Syam AF, Miftahussurur M, Makmun D, Nusi IA, Zain LH, Zulkhairi, et al. Risk factors and prevalence of Helicobacter pylori in five largest islands of Indonesia: a preliminary study. PLoS One. 2015;10:1–14. doi: 10.1371/journal.pone.0140186. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Tan HJ, Goh KL. Changing epidemiology of Helicobacter pylori in Asia. J Dig Dis. 2008;9:186–189. doi: 10.1111/j.1751-2980.2008.00344.x. [DOI] [PubMed] [Google Scholar]
  35. Ueda J, Okuda M, Nishiyama T, Lin Y, Fukuda Y, Kikuchi S. Diagnostic accuracy of the E-Plate Serum Antibody Test Kit in detecting Helicobacter pylori infection among Japanese children. J Epidemiol. 2014;24:47–51. doi: 10.2188/jea.JE20130078. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Uyub AM, Raj SM, Visvanathan R, Nazim M, Aiyar S, Anuar AK, et al. Helicobacter pylori infection in North-Eastern Peninsular Malaysia evidence for an unusually low prevalence. Scand J Gastroenterol. 1994;29:209–213. doi: 10.3109/00365529409090465. [DOI] [PubMed] [Google Scholar]
  37. Vaira D, Miglioli M, Mulè P, Holton J, Menegatti M, Vergura M, et al. Prevalence of peptic ulcer in Helicobacter pylori positive blood donors. Gut. 1994;35:309–312. doi: 10.1136/gut.35.3.309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Vohlonen I, Pukkala E, Malila N, Härkönen M, Hakama M, Koistinen V, et al. Risk of gastric cancer in Helicobacter pylori infection in a 15-year follow-up. Scand J Gastroenterol. 2016;51:1159–1164. doi: 10.1080/00365521.2016.1183225. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Watanabe M, Ito H, Hosono S, Oze I, Ashida C, Tajima K, et al. Declining trends in prevalence of Helicobacter pylori infection by birth-year in a Japanese population. Cancer Sci. 2015;106:1738–1743. doi: 10.1111/cas.12821. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Yamaoka Y. Mechanisms of disease: Helicobacter pylori virulence factors. Nat Rev Gastroenterol Hepatol. 2010;7:629–641. doi: 10.1038/nrgastro.2010.154. [DOI] [PMC free article] [PubMed] [Google Scholar]

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