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Global Prevalence of Helicobacter pylori Infection: Systematic Review and Meta-Analysis

  • Author Footnotes
    ∗ Authors share co-first authorship.
    James K.Y. Hooi
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    Department of Medicine and Therapeutics, Institute of Digestive Disease, State Key Laboratory of Digestive Diseases, LKS Institute of Health Science, Chinese University of Hong Kong, Hong Kong, China
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    Wan Ying Lai
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    Department of Medicine and Therapeutics, Institute of Digestive Disease, State Key Laboratory of Digestive Diseases, LKS Institute of Health Science, Chinese University of Hong Kong, Hong Kong, China
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    Wee Khoon Ng
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    ∗ Authors share co-first authorship.
    Affiliations
    Department of Medicine and Therapeutics, Institute of Digestive Disease, State Key Laboratory of Digestive Diseases, LKS Institute of Health Science, Chinese University of Hong Kong, Hong Kong, China

    Department of Gastroenterology and Hepatology, Tan Tock Seng Hospital, Singapore
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    Michael M.Y. Suen
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    Department of Medicine and Therapeutics, Institute of Digestive Disease, State Key Laboratory of Digestive Diseases, LKS Institute of Health Science, Chinese University of Hong Kong, Hong Kong, China
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  • Fox E. Underwood
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    Departments of Medicine and Community Health Sciences, University of Calgary, Calgary, Alberta, Canada
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  • Divine Tanyingoh
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    Departments of Medicine and Community Health Sciences, University of Calgary, Calgary, Alberta, Canada
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  • Peter Malfertheiner
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    Department of Gastroenterology, Hepatology and Infectious Diseases, Otto-von-Guericke University of Magdeburg, Magdeburg, Germany
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  • David Y. Graham
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    Gastroenterology, Baylor College of Medicine, Houston, Texas
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  • Vincent W.S. Wong
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    Department of Medicine and Therapeutics, Institute of Digestive Disease, State Key Laboratory of Digestive Diseases, LKS Institute of Health Science, Chinese University of Hong Kong, Hong Kong, China
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  • Justin C.Y. Wu
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    Department of Medicine and Therapeutics, Institute of Digestive Disease, State Key Laboratory of Digestive Diseases, LKS Institute of Health Science, Chinese University of Hong Kong, Hong Kong, China
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  • Francis K.L. Chan
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    Department of Medicine and Therapeutics, Institute of Digestive Disease, State Key Laboratory of Digestive Diseases, LKS Institute of Health Science, Chinese University of Hong Kong, Hong Kong, China
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  • Joseph J.Y. Sung
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    Department of Medicine and Therapeutics, Institute of Digestive Disease, State Key Laboratory of Digestive Diseases, LKS Institute of Health Science, Chinese University of Hong Kong, Hong Kong, China
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    § Authors share co-senior authorship.
    Gilaad G. Kaplan
    Correspondence
    Gilaad G. Kaplan, MD, MPH, FRCPC, Teaching Research and Wellness Center, 3280 Hospital Drive NW, 6D17 Calgary, Alberta, T2N 4N1, Canada. fax: 1 403 592 5050.
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    Departments of Medicine and Community Health Sciences, University of Calgary, Calgary, Alberta, Canada
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    Siew C. Ng
    Correspondence
    Reprint requests Address requests for reprints to: Siew C. Ng, MBBS, MRCP, PhD, Department of Medicine and Therapeutics, Chinese University of Hong Kong, Hong Kong. fax: (852) 2637 3852.
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    Department of Medicine and Therapeutics, Institute of Digestive Disease, State Key Laboratory of Digestive Diseases, LKS Institute of Health Science, Chinese University of Hong Kong, Hong Kong, China
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Open AccessPublished:April 26, 2017DOI:https://doi.org/10.1053/j.gastro.2017.04.022

      Background & Aims

      The epidemiology of Helicobacter pylori infection has changed with improvements in sanitation and methods of eradication. We performed a systematic review and meta-analysis to evaluate changes in the global prevalence of H pylori infection.

      Methods

      We performed a systematic search of the MEDLINE and EMBASE databases for studies of the prevalence of H pylori infection published from January 1, 1970 through January 1, 2016. We analyzed data based on United Nations geoscheme regions and individual countries. We used a random effects model to calculate pooled prevalence estimates with 95% confidence intervals (CIs), weighted by study size. We extrapolated 2015 prevalence estimates to obtain the estimated number of individuals with H pylori infection.

      Results

      Among 14,006 reports screened, we identified 263 full-text articles on the prevalence of H pylori infection; 184 were included in the final analysis, comprising data from 62 countries. Africa had the highest pooled prevalence of H pylori infection (70.1%; 95% CI, 62.6−77.7), whereas Oceania had the lowest prevalence (24.4%; 95% CI, 18.5−30.4). Among individual countries, the prevalence of H pylori infection varied from as low as 18.9% in Switzerland (95% CI, 13.1−24.7) to 87.7% in Nigeria (95% CI, 83.1−92.2). Based on regional prevalence estimates, there were approximately 4.4 billion individuals with H pylori infection worldwide in 2015.

      Conclusions

      In a systematic review and meta-analysis to assess the prevalence of H pylori infection worldwide, we observed large amounts of variation among regions—more than half the world’s population is infected. These data can be used in development of customized strategies for the global eradication.

      Keywords

      Abbreviations used in this paper:

      CI (confidence interval), HP (Helicobacter pylori), UN (United Nations)

       Background and Context

      There are multiple reports on individual countries’ Helicobacter pylori (HP) prevalence over the past few decades. However, global and regional HP prevalence and their trend with time is not well reported.

       New Findings

      This is the first study to summarize comprehensive global HP prevalence. HP prevalence in different regions of the world is stable or decreasing.

       Limitations

      This study contains reports from 62 out of 196 countries, with data lacking in several developing countries. Reports were also conducted at different time periods, with several countries lacking recent data, limiting accuracy for inter-region comparison.

       Impact

      This review estimates that more than half the world’s population is infected with HP. Our data can be used to prioritize public health efforts in countries with the highest HP prevalence.
      Helicobacter pylori (HP) is a gram-negative microaerophilic bacterium that infects the epithelial lining of the stomach. The discovery of HP as a cause of peptic ulcer disease in 1983 resulted in a change of what was once a difficult and debilitating disease into one that could be reliably cured with a course of antibiotics, albeit with escalating concerns due to mounting antibiotic resistance.
      • Marshall B.J.
      • Warren J.R.
      Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration.
      • Malfertheiner P.
      • Megraud F.
      • O'Morain C.
      • et al.
      Current concepts in the management of Helicobacter pylori infection: the Maastricht III Consensus Report.
      • Liou J.M.
      • Fang Y.J.
      • Chen C.C.
      • et al.
      Concomitant, bismuth quadruple, and 14-day triple therapy in the first-line treatment of Helicobacter pylori: a multicentre, open-label, randomised trial.
      In many countries, the incidence of HP infection has been decreasing in association with improved standards of living.
      • Graham D.Y.
      History of Helicobacter pylori, duodenal ulcer, gastric ulcer and gastric cancer.
      • Nagy P.
      • Johansson S.
      • Molloy-Bland M.
      Systematic review of time trends in the prevalence of Helicobacter pylori infection in China and the USA.
      Yet the prevalence of this bacterium is still ubiquitous, especially in the Far East.
      • Graham D.Y.
      History of Helicobacter pylori, duodenal ulcer, gastric ulcer and gastric cancer.
      It is the main cause of chronic gastritis and the principal etiological agent for gastric cancer and peptic ulcer disease.
      • Malfertheiner P.
      • Megraud F.
      • O'Morain C.
      • et al.
      Current concepts in the management of Helicobacter pylori infection: the Maastricht III Consensus Report.
      • Wang C.
      • Yuan Y.
      • Hunt R.H.
      The association between Helicobacter pylori infection and early gastric cancer: a meta-analysis.
      In most regions, the main mechanism of spread is intrafamilial transmission.
      • Yokota S.
      • Konno M.
      • Fujiwara S.
      • et al.
      Intrafamilial, preferentially mother-to-child and intraspousal, Helicobacter pylori infection in japan determined by mutilocus sequence typing and random amplified polymorphic DNA fingerprinting.
      The prevalence remains high in most developing countries and is generally related to socioeconomic status and levels of hygiene. Global and regional HP prevalence has not been systematically reported until now.
      Recent interest has focused on HP eradication as a strategy of eliminating gastric cancer. However, the epidemiology and clinical manifestations of the infection has been changing, especially in developed countries. For example, gastric cancer and peptic ulcer incidence has continued to fall in Western Europe, the United States, and Japan. Global eradication strategies require up-to-date information regarding HP prevalence and disease burden.
      We performed a systematic review of population-based studies reporting HP prevalence of different countries over different time periods, with the premise that these data would provide crucial updates about HP global disease burden and the information to plan appropriate strategies for allocating health care resources. We pooled HP prevalence estimates in different regions and countries, examined the trend in HP prevalence over the past 4 decades, and estimated the number of people infected with HP globally. Understanding the global epidemiologic patterns of HP will aid us in prioritizing and customizing public health efforts to better manage the burden of this disease.

      Materials and Methods

       Literature Search and Study Selection

      This systematic review was performed in accordance to the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) 2009 guidelines.
      • Moher D.
      • Liberati A.
      • Tetzlaff J.
      • et al.
      PRISMA Group
      Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement.
      A search using keywords from a combination of Medical Subject Headings and free text including terms related to HP and prevalence was performed in MEDLINE and EMBASE via OvidSP. All suitable published papers from January 1, 1970 to January 1, 2016 were identified and subsequently catalogued using EndNote X7. The search strategy is described in the Supplementary Table 1.
      Comprehensive inclusion and exclusion criteria were predefined (Table 1) to facilitate objective screening of papers. Only published original observational reports on the prevalence of HP in study populations that were reflective of the general population at national or sub-national levels were included. Systematic reviews, meta-analyses, conference presentations, and letters or correspondences were excluded. Suitable reports identified in hand searches were also included for review. Reports that focused only on specific sub-groups that were not reflective of the general population were excluded (eg, migrants and prisoners). The first phase involved a group of 3 reviewers (J.H., W.Y.L., and M.S.) who independently catalogued all reports using the set criteria. Outcome of this initial categorization was then cross-checked by a different reviewer within this group to ensure its accuracy with a 90% level of agreement. In the second phase, full-text papers were obtained for all identified potential reports for detailed analysis of inclusion suitability. All conflicts of opinion and uncertainties were discussed and resolved by consensus with third-party reviewers (W.K.N., W.T., and S.C.N.). The search was not limited by language. Reports written in neither English nor Chinese had been translated by Google Translate or by colleagues proficient in that language for evaluation of their suitability. Attempts were also made to clarify with the corresponding authors regarding any uncertainties or missing data (eg, study periods not explicitly stated) in selected reports. The reports were then grouped by countries and subsequently into regions based on the United Nations (UN) geoscheme devised by the UN Statistics Division.

      Composition of macro Geographical (Continental) Regions, Geographical Sub-Regions, and Selected Economic and Other Groupings. Available at: http://unstats.un.org/unsd/methods/m49/m49regin.htm. Published September 26, 2016. Accessed November 18, 2016.

      Figure 1 details the process of report selection.
      Table 1Study Selection Criteria
      Criteria
      Selection, grading, and clarification of studies

       HP diagnosis must be confirmed by one of the following tests: HP serology, HP stool antigen, urea breath test, biopsies for Campylobacter-like organism test, rapid urease test, histology, or culture

       The study participants must be reflective of the general population in the region

       Data from multicenter and multinational studies were extracted separately and sorted by countries and regions

       Studies were classified as national (if stated in the report or multicenter study involving multiple regions in the country), sub-national (if only a particular region was evaluated), and city level

       Clarifications with the corresponding authors of studies with missing data were made if possible (eg, without specified HP diagnostic method or study period)

       Attempts were made to rectify any data errors found in the studies, in consultation with the corresponding authors whenever possible

      Exclusion criteria

       Publication type

      Guidelines

      Perspectives, correspondence, letters

      Conference abstract or presentation without formal publication

      Systematic reviews or meta-analyses

      Surveillance registration or national notifiable disease reports of HP

      Studies without defined study periods

       Study type

      Economic analyses

      Modeling, time series, or transmission studies; mortality or survival analyses; diagnostic assay or test performance studies; animal studies

       Study Population

      Study populations that are typically associated with higher prevalence of HP (eg, patients with gastric cancer, peptic ulcers)

      High-risk population groups (migrants, refugees, prisoners, individuals [groups] classified as low socioeconomic status, homeless people, adoptees)

      Study participants that were restricted to selected age groups (eg, children, elderly)

       Testing

      HP diagnosis made from methods other than the 4 conventional tests stated above

      Studies not reporting the method of HP diagnosis

      Self-reported HP infection

      Studies not reporting the number of individuals on which the prevalence estimate was based
      Figure thumbnail gr2
      Figure 2Global prevalence of HP choropleth map. Certain regions are magnified to better display the smaller countries. The online interactive global map showing the HP prevalence can be found at the following URL: https://people.ucalgary.ca/∼ggkaplan/HP2016.html.

       Data Extraction and Quality Appraisal

      Full-text review was performed for all the selected papers and data extracted and sorted by the following variables: name of study, leading author, journal, publication year, study period, type of study, study location (country and sub-national region), HP diagnostic methods used, participant details (number, age, sex ratio), total number of participants, number of HP positive participants, and HP crude prevalence rate. Data on prevalence as a percent of the number of HP-positive participants relative to total number tested were recorded or calculated with 95% confidence intervals (CIs). Papers with missing data, despite attempts to contact the corresponding authors, were excluded. The quality of the remaining papers was rated with the Cochrane Collaboration−endorsed Newcastle-Ottawa Quality Assessment Scale,

      Wells GA, Shea B, O'Connell D, et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomized studies in meta-analyses. Available at: http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp. Published 2014. Accessed November 18, 2016.

      which was designed to assess aspects of population-based studies of prevalence. The quality assessment of each paper is shown in Supplementary Table 2.

       Summarization of Data

      HP prevalence for each country was estimated by pooling the data from eligible papers. We used a random effects model to calculate pooled prevalence estimates with 95% CIs. Heterogeneity was assessed using the I2 measure and the Cochran Q-statistic. The following stratified analyses were conducted to address sources of heterogeneity: (1) geographic region based on classification by UN; (2) time period of evaluating prevalence of HP split into 1970 to 1999 and 2000 to 2016; (3) restricting analysis to adult only (aged 18 years and older); and (4) primary modality of testing HP, including serology, urea breath test, stool antigen, Campylobacter-like organism or histopathology, and serology or urea breath test.
      The prevalence data were grouped by geographic region based on the UN geoscheme: Northern America, Latin America and the Caribbean, Europe (Northern, Southern, Western, Eastern), Africa, Asia (Central, Eastern, Southern, South-Eastern, Western), and Oceania. Reports that focused on the indigenous population in the United States and Australia were analyzed separately from the respective general population of the country. When prevalence was reported for a multi-year period that extended over more than one time period, the study was included in the time period that captured the most updated data. If multiple studies reported prevalence for the same country and time period, the pooled estimate was taken.
      • Molodecky N.A.
      • Soon I.S.
      • Rabi D.M.
      • et al.
      Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review.
      Quartiles of prevalence data were used to create choropleth map. Next, we created a web-based interactive map to display comments associated with the prevalence of HP for each country. The static and interactive maps were created using QGIS 2.16.3

      QGIS Development Team. QGIS Geographic Information System. Open Source Geospatial Foundation Project. Available at: http://www.qgis.org/. Published 2016. Accessed January 21, 2017.

      with the HTML Image Map Plugin

      Duivenvoorde R. HTML Image Map Plugin for QGIS. Open Source Geospatial Foundation Project. http://hub.qgis.org/projects/imagemapplugin. Published 2014. Accessed January 21, 2017.

      for the interactive map. The geographic data were created by the Natural Earth Community.

      Natural Earth Development Team. Cultural Vectors. North American Cartographic Information Society. http://www.naturalearthdata.com. Published 2016. Accessed January 21, 2017.

      Population-based studies that reported HP prevalence with two or more time points for the same country were included for temporal trend analyses. For the assessment of potential changes of HP prevalence over time, we stratified prevalence estimates into two time periods, 1970−1999 and 2000−2016. To obtain the number of people affected with HP, we extrapolated our prevalence estimates to the total 2015 population living in countries and regions as per the UN Population Division. We assumed that countries with missing data in a region had comparable prevalence to our pooled mean prevalence.
      R Studio, version 0.99.903, was used for statistical analysis. The R-metafor package was used to generate 95% CIs from logistic regression models then converted to prevalence using the expit transformation. The results of the pooled prevalence estimates were then organized by geographical region.

       Role of Funding Source

      There was no funding source for this study. The corresponding authors had full access to all data in the study and had final responsibility for the decision to submit for publication.

      Results

      A total of 14,006 records were identified from both databases, of which 6188 records were duplicates, 7611 records were excluded based on selection criteria, 22 records were removed due to inaccessible full text, and 3 records could not be translated for review (Figure 1). Two records were found in hand searches, and a total of 184 papers were included after full-text review (11 from Africa, 75 from Asia, 66 from Europe, 13 from Latin America and Caribbean, 13 from Northern America, and 6 from Oceania), reporting HP prevalence in 62 countries with 257,768 (48.5%) participants tested HP-positive, out of a total of 531,880 participants. The countries with the highest number of reports were China (n = 21), Korea (n = 12), Japan (n = 11), United States (n = 10), Germany (n = 8), and Iran (n = 8). A summary of the distribution of papers by regions is shown in Supplementary Table 3 and details of individual papers (including age range, sex, and methods to diagnose HP) in Supplementary Tables 4 and 5.
      Prevalence of HP in the indigenous population of the United States and Australia was higher than the general population. In Australia, the pooled HP prevalence estimate for the general population was 24.6% (95% CI, 17.2%−32.1%), but was as high as 76.0% (95% CI, 72.3%−79.6%) in the rural Western Australian indigenous community. In the United States, the pooled HP prevalence estimate for the general population was 35.6% (95% CI, 30.0%−41.1%), but it was 74.8% (95% CI, 72.9%−76.7%) in the Alaskan indigenous population. The countries with the highest HP burden were Nigeria (87.7%; 95% CI, 83.1%−92.2%), Portugal (86.4%; 95% CI, 84.9%−87.9%), Estonia (82.5%; 95% CI, 75.1%−90.0)%, Kazakhstan (79.5%; 95% CI, 74.9%−84.2%), and Pakistan (81.0%; 95% CI, 75.6%−86.4%). Countries with the lowest HP prevalence were Switzerland (18.9%; 95% CI, 13.1%−24.7%), Denmark (22.1%; 95% CI, 17.8%−26.5%), New Zealand (24.0%; 95% CI, 21.4%−26.5%), Australia (24.6%; 95% CI, 17.2%−32.1%), and Sweden (26.2%; 95% CI, 18.3%−34.1%).
      Regions with the highest reported HP prevalence were Africa (70.1%; 95% CI, 62.6%−77.6%), South America (69.4%; 95% CI, 63.9%−74.9%), and Western Asia (66.6%; 95% CI, 56.1%−77.0%). Regions with the lowest reported HP prevalence were Oceania (24.4%; 95% CI, 18.5%−30.4%), Western Europe (34.3%; 95% CI, 31.3%−37.2%), and Northern America (37.1%; 95% CI, 32.3%−41.9%). HP prevalence and the number of people with HP living in the general population in the 6 UN regions were reported in Tables 2 and 3. Forest plots of pooled HP prevalence stratified by country and UN region are shown in Supplementary Table 6. Significant heterogeneity was observed for pooled analyses in each region (Supplementary Table 6). In order to assess potential sources of heterogeneity, pooled prevalence was stratified by modality of testing for HP (Supplementary Table 7) and adult-only studies (Supplementary Table 8).
      Table 2Helicobacter pylori Prevalence and Number of People Living With H pylori in the General Population Within Each Country Grouped by United Nations Regions
      VariableNo. of reporting studiesNo. of participantsPrevalence estimates,

      % (95% CI)
      Population size per country
      Based on UN 2015 Revision of World Population Prospects total population estimates.
      HP-positive population
      UN African region
       Benin144674.1 (70.0−78.1)10,880,0008,056,640
       Burkina Faso118846.8 (39.7−53.9)18,106,0008,475,419
       Democratic Republic of Congo113377.4 (70.3−84.6)77,267,00059,835,565
       Egypt120040.9 (15.4−66.4)91,508,00037,435,923
       Libya136076.4 (72.0−80.8)6,278,0004,795,764
       Nigeria264887.7 (83.1−92.2)182,202,000159,700,053
       South Africa2153977.6 (59.8−95.5)54,490,00042,306,036
       Tunisia234872.8 (53.7−91.9)11,254,0008,191,787
      UN Latin American and Caribbean region
       Argentina149349.1 (44.7−53.5)43,417,00021,313,405
       Bahamas120457.8 (51.1−64.6)388,000224,419
       Brazil6293771.2 (66.0−76.4)207,848,000147,946,206
       Chile1261574.6 (72.9−76.2)17,948,00013,383,824
       Ecuador19072.2 (63.0−81.5)16,144,00011,659,197
       Guadeloupe
      Insular region of France located in the Caribbean.
      185449.0 (35.3−62.8)468,000229,367
       Mexico211,82052.5 (24.7−80.3)127,017,00066,709,328
       Panama17454.1 (42.7−65.4)3,929,0002,123,625
      UN Northern American region
       Canada131638.0 (32.6−43.3)35,940,00013,646,418
       Greenland275641.4 (37.9−44.9)56,00023,178
       United States
      Data related to the indigenous population were excluded from this table.
      816,23535.6 (30.0−41.1)321,774,000114,455,012
      UN Asian region
       Central Asia (n = 1)
      Kazakhstan128879.5 (74.9−84.2)17,625,00014,013,638
       Eastern Asia (n = 47)
      China22103,12855.8 (51.8−59.9)1,376,049,000768,110,552
      Japan1148,97951.7 (44.7−58.7)126,573,00065,387,612
      Korea11121,49354.0 (50.1−57.8)25,155,00013,571,123
      Taiwan310,61653.9 (36.6−71.2)23,381,00012,600,021
       Southern Asia (n = 13)
      Iran8525659.0 (51.5−66.5)79,109,00046,658,488
      India240763.5 (53.4−73.5)1,311,051,000831,861,860
      Lebanon130852.0 (46.4−47.5)5,851,0003,039,595
      Nepal138370.1 (65.9−75.1)28,514,00019,974,057
      Pakistan120581.0 (75.6−86.4)188,925,000152,991,465
       South-Eastern Asia (n = 8)
      Malaysia3916828.6 (19.0−38.2)30,331,0008,677,699
      Singapore295340.8 (37.7−43.9)5,604,0002,287,553
      Thailand117943.6 (36.3−50.8)67,959,00029,616,532
      Vietnam2124170.3 (63.3−77.4)93,448,00065,712,634
       Western Asia (n = 8)
      Israel268868.9 (62.7−75.1)8,064,0005,555,290
      Oman249949.1 (11.5−86.7)4,491,0002,205,081
      Saudi Arabia136465.9 (61.1−70.8)31,540,00020,794,322
      Turkey3603677.2 (71.4−83.1)78,666,00060,761,618
      UN European region
       Eastern Europe (n = 10)
      Czech Republic3464441.2 (24.8−57.6)10,543,0004,342,662
      Poland3780666.6 (56.4−76.7)38,612,00025,707,870
      Romania196068.5 (65.6−71.5)19,511,00013,372,839
      Russian Federation3477178.5 (67.1−89.9)143,457,000112,585,054
       Northern Europe (n = 22)
      Denmark237,74122.1 (17.8−26.5)5,669,0001,254,550
      Estonia2219882.5 (75.1−90.0)1,313,0001,083,356
      Finland189656.8 (46.5−67.0)5,503,0003,124,603
      Iceland283436.0 (32.7−39.2)329,000118,341
      Ireland1100043.0 (39.9−46.1)4,688,0002,015,840
      Latvia1356479.2 (77.9−80.5)1,971,0001,561,229
      Norway3406830.7 (20.5−40.8)5,211,0001,597,172
      Sweden5714926.2 (18.3−34.1)9,779,0002,563,076
      United Kingdom515,09835.5 (14.5−56.5)64,716,00022,974,180
       Southern Europe (n = 22)
      Albania110153.5 (43.7−63.2)2,897,0001,549,026
      Croatia3653852.7 (42.5−62.8)4,240,0002,234,056
      Greece3157152.1 (40.2−64.0)10,955,0005,708,651
      Italy5905556.2 (46.9−65.4)59,798,00033,606,476
      Portugal1206786.4 (84.9−87.9)10,350,0008,942,400
      San Marino2376547.5 (40.5−54.5)32,00015,200
      Spain7272154.9 (48.6−61.1)46,122,00025,307,141
       Western Europe (n = 16)
      Belgium327,84532.7 (22.4−43.0)11,299,0003,694,773
      France
      Guadeloupe data not included in the pooled analysis for France due to different demographics.
      16446.9 (34.7−59.1)64,395,00030,188,376
      Germany819,01535.3 (31.2−39.4)80,689,00028,483,217
      Netherlands3859235.5 (30.1−41.0)16,925,0006,011,760
      Switzerland117518.9 (13.1−24.7)8,299,0001,565,191
      UN Oceania region
       Australia
      Data related to the indigenous population were excluded from this table.
      4448524.6 (17.2−32.1)23,969,0005,905,962
       New Zealand1106024.0 (21.4−26.5)4,529,0001,085,148
      a Based on UN 2015 Revision of World Population Prospects total population estimates.
      b Insular region of France located in the Caribbean.
      c Data related to the indigenous population were excluded from this table.
      d Guadeloupe data not included in the pooled analysis for France due to different demographics.
      Table 3Helicobacter pylori Prevalence and Number of People Living With H pylori in the General Population in the United Nations Regions
      VariablePrevalence estimates, %, 95% CI)Population size per region/country
      Based on United Nations 2015 Revision of World Population Prospects total population estimates.
      HP-positive population (range)
      UN Africa region79.1 (62.6−95.6)1,186,178,282938,267,021 (742,547,604−1,133,986,437)
      UN Latin American and Caribbean region63.4 (59.2−67.6)634,386,567402,201,083 (375,556,847−428,845,319)
       Caribbean52.6 (45.2−60.0)43,199,29722,731,470 (19,526,082−25,919,578)
       Central America53.0 (32.6−73.5)172,740,07491,621,335 (56,313,264−126,963,954)
       South America69.4 (63.9−74.9)418,447,196290,318,665 (267,387,758−313,416,949)
      UN Northern American region37.1 (32.3−41.9)357,838,036132,614,776 (115,581,685−149,934,137)
      UN Asian region54.7 (51.3−58.1)4,393,296,0142,403,132,920 (2,253,760,855−2,552,504,984)
       Central Asia79.5 (74.9−84.2)67,314,03353,521,388 (50,418,210−56,678,415)
       Eastern Asia54.1 (50.8−57.5)1,612,286,941872,892,150 (819,041,766−927,064,991)
       Southern Asia61.6 (55.9−67.4)1,822,974,0741,123,134,327 (1,019,042,507−1,228,684,525)
       South–Eastern Asia43.1 (31.5−54.8)633,489,946273,287,563 (199,549,332−347,152,490)
       Western Asia66.6 (56.1−77.0)257,231,020171,212,967 (144,306,602−198,067,885)
      UN European region47.0 (41.8−52.1)738,442,070347,067,773 (308,668,785−384,728,318)
       Eastern Europe62.8 (48.3−77.2)292,942,778183,850,887 (141,491,361−226,151,824)
       Northern Europe41.6 (32.4−50.7)102,357,76842,550,124 (33,163,916−51,895,388)
       Southern Europe55.0 (49.1−61.0)152,347,89283,852,280 (74,802,814−92,932,214)
       Western Europe34.3 (31.3−37.2)190,793,63266,396,184 (59,718,406−70,975,231)
      UN Oceania region24.4 (18.5−30.4)39,331,1309,608,595 (7,276,259−11,956,663)
      Global4,356,096,968 (3,750,167,566−4,961,780,681)
      a Based on United Nations 2015 Revision of World Population Prospects total population estimates.
      Two time periods (1970−1999 and 2000−2016) were used to analyze the HP prevalence trend with time. HP prevalence after 2000 was lower than before in Europe from 48.8% (95% CI, 39.4%−58.2%) to 39.8% (95% CI, 34.2%−45.3%), Northern America 42.7% (95% CI, 32.7%−52.6%) to 26.6% (95% CI, 19.0%−34.1%), and Oceania 26.6% (95% CI, 20.4%−32.8%) to 18.7% (95% CI, 11.6%−25.7%). In contrast, the prevalence of HP positivity was similar in Asia (53.6% before 2000 vs 54.3% after 2000), and Latin America and the Caribbean (62.8% before 2000 vs 60.2% after 2000). Summary of the time trend prevalence for each country and region is shown in Supplementary Table 9. After extrapolation to the 2015 world population, 4.4 billion individuals were estimated to be HP-positive globally (Table 3).

      Discussion

      HP infection continues to be a major public health issue worldwide. This global systematic review shows that in 2015, approximately 4.4 billion individuals worldwide were estimated to be positive for HP. This is the most comprehensive and up-to-date systematic review of the worldwide prevalence of HP. We confirmed a wide variation in the prevalence of HP between regions and countries. Prevalence is highest in Africa (79.1%), Latin America and the Caribbean (63.4%), and Asia (54.7%). In contrast, HP prevalence is lowest in Northern America (37.1%) and Oceania (24.4%). At the turn of the 21st century, the prevalence of HP has been declining in highly industrialized countries of the Western world, whereas prevalence has plateaued at a high level in developing and newly industrialized countries. The widening differential gap in prevalence has important implications on the future worldwide prevalence of sequelae associated with HP, including peptic ulcer disease and gastric cancer. These differences in HP prevalence likely reflect the level of urbanization, sanitation, access to clean water, and varied socioeconomic status. There are significant differences in the HP prevalence even within the same country. Different racial groups in the United States have different HP prevalence. It was reported that the prevalence in non-Hispanic whites ranges from 18.4% to 26.2% and that in non-whites ranges from 34.5% to 61.6%.
      • Everhart J.E.
      • Kruszon-Moran D.
      • Perez-Perez G.I.
      • et al.
      Seroprevalence and ethnic differences in Helicobacter pylori infection among adults in the United States.
      • Cardenas V.M.
      • Mulla Z.D.
      • Ortiz M.
      • et al.
      Iron deficiency and Helicobacter pylori infection in the United States.
      Prevalence can be as high as 75.0% in the Alaskan Native population.
      • Parkinson A.J.
      • Gold B.D.
      • Bulkow L.
      • et al.
      High prevalence of Helicobacter pylori in the Alaska Native population and association with low serum ferritin levels in young adults.
      Our review demonstrated that there is still a significant burden of HP in most of the world. Even in Switzerland, which had the lowest reported HP prevalence (18.9%), there were still approximately 1.6 million infected individuals. Eradication of gastric cancer will require additional efforts and research focused on prevention of HP acquisition and HP eradication. Innovative strategies will likely be needed to reduce HP prevalence in areas such as Africa, India, and South America, where access to health care and resources may be limited.
      HP has been identified as a Group I carcinogen by the International Agency for Research on Cancer and currently is considered a necessary but insufficient cause of gastric adenocarcinoma.
      • Eslick G.D.
      • Lim L.L.
      • Byles J.E.
      • et al.
      Association of Helicobacter pylori infection with gastric carcinoma: a meta-analysis.
      Helicobacter and Cancer Collaborative Group
      Gastric cancer and Helicobacter pylori: a combined analysis of 12 case control studies nested within prospective cohorts.
      • Huang J.Q.
      • Sridhar S.
      • Chen Y.
      • et al.
      Meta-analysis of the relationship between Helicobacter pylori seropositivity and gastric cancer.
      • Parsonnet J.
      • Friedman G.D.
      • Vandersteen D.P.
      • et al.
      Helicobacter pylori infection and the risk of gastric carcinoma.
      • Uemura N.
      • Okamoto S.
      • Yamamoto S.
      • et al.
      Helicobacter pylori infection and the development of gastric cancer.
      Approximately 89% of all gastric cancers can be attributable to HP infection.
      International Agency for Research on Cancer Helicobacter pylori Working Group
      Helicobacter pylori Eradication as a Strategy for Preventing Gastric Cancer. (IARC Working Group Reports, No. 8).
      Gastric cancer remains the third most common cancer worldwide, with more than half coming from China, Japan, and Korea. Prognosis is poor, with only 1 in 5 patients surviving longer than 5 years after diagnosis. HP eradication has been associated with a reduction of gastric cancer incidence and this benefit is present irrespective of risk group.
      • Kosunen T.U.
      • Pukkala E.
      • Sarna S.
      • et al.
      Gastric cancers in Finnish patients after cure of Helicobacter pylori infection: a cohort study.
      • Takenaka R.
      • Okada H.
      • Kato J.
      • et al.
      Helicobacter pylori eradication reduced the incidence of gastric cancer, especially of the intestinal type.
      • Yeh J.M.
      • Kuntz K.M.
      • Ezzati M.
      • et al.
      Exploring the cost-effectiveness of Helicobacter pylori screening to prevent gastric cancer in China in anticipation of clinical trial results.
      There is also evidence that screening and eradication of HP in young adults in China would be cost-effective and could help in preventing 1 gastric cancer in every 4 to 6 cases.
      • Yeh J.M.
      • Kuntz K.M.
      • Ezzati M.
      • et al.
      Exploring the cost-effectiveness of Helicobacter pylori screening to prevent gastric cancer in China in anticipation of clinical trial results.
      The appropriate strategy may differ between countries and is further complicated by increasing antibiotic resistance, which could prove to be a major hindrance to eradication. Increasing prophylactic HP vaccination appears to be an option.
      • Lu B.
      • Li M.
      Helicobacter pylori eradication for preventing gastric cancer.
      The development of HP vaccine has been challenging, but there is yet to be an effective vaccine available in the market. One promising phase 3 trial of an oral vaccine in China has demonstrated vaccine-mediated protection against HP, leading to a reduced risk of HP acquisition among the younger population.
      • Zeng M.
      • Mao X.H.
      • Li J.X.
      • et al.
      Efficacy, safety, and immunogenicity of an oral recombinant Helicobacter pylori vaccine in children in China: a randomised, double-blind, placebo-controlled, phase 3 trial.
      The high global prevalence of HP in many parts of the world and the non-diminishing HP prevalence in developed countries should serve as the impetus for researchers to hasten the process to create an effective vaccine. Of interest, HP vaccination has also been demonstrated to be cost-effective in the United States, which has one of the lowest HP prevalences globally.
      • Rupnow M.F.
      • Chang A.H.
      • Shachter R.D.
      • et al.
      Cost-effectiveness of a potential prophylactic Helicobacter pylori vaccine in the United States.
      In Africa, despite the high HP prevalence, the reported incidence of gastric cancer was considerably lower compared with China or Japan and was postulated to be related to the predominant non-atrophic gastritis pattern in Africa; the archetypal hpAfrica2 type strain largely restricted in South Africa, which lacks cag A pathogenicity island; and lastly intestinal parasitic infestation modulating the immune response against HP toward a Th2 type (anti-inflammatory), which may reduce risk of gastric cancer.
      • Correa P.
      • Piazuelo M.B.
      Helicobacter pylori infection and gastric adenocarcinoma.
      • Kodaman N.
      • Pazos A.
      • Schneider B.G.
      • et al.
      Human and Helicobacter pylori coevolution shapes the risk of gastric disease.
      The now defunct phenomenon known as “African enigma” was attributed to the inadequate sampling of the African population obtained through endoscopic data, limited access to health care, and a relatively short life expectancy in the population. More recent and robust data on the African gastric ulcer and cancer prevalence confirmed that it is not as low as reported previously.
      • Graham D.Y.
      • Lu H.
      • Yamaoka Y.
      African, Asian or Indian enigma, the East Asian Helicobacter pylori: facts or medical myths.
      Ongoing efforts to monitor HP prevalence and its disease burden in a systematic manner is crucial, as it will minimize any skewed data, which can adversely affect the allocation of health care resources.
      As has been reported in the literature, our review observed that HP prevalence is lower in certain ethnic groups, like Malay, despite having the similar environmental exposures as other ethnic groups.
      • Graham D.Y.
      History of Helicobacter pylori, duodenal ulcer, gastric ulcer and gastric cancer.
      Malaysia’s population consisted of approximately 67.4% Malays

      Population Distribution and Basic Demographic Characteristic Report 2010. https://www.dosm.gov.my/v1/index.php?r=column/ctheme&menu_id=L0pheU43NWJwRWVSZklWdzQ4TlhUUT09&bul_id=MDMxdHZjWTk1SjFzTzNkRXYzcVZjdz09. Accessed November 18, 2016.

      and has a low pooled HP prevalence of 28.6%. Among the varied ethnicities in Malaysia, the prevalence of HP in Malays is 19.6%, which is significantly lower than the Chinese (40.0%) and Indians (50.7%).
      • Goh K.L.
      • Parasakthi N.
      The racial cohort phenomenon: seroepidemiology of Helicobacter pylori infection in a multiracial South-East Asian country.
      Besides Malaysia, the Malays in Singapore also had a low HP prevalence of 25.0%.
      • Kang J.Y.
      • Yeoh K.G.
      • Ho K.Y.
      • et al.
      Racial differences in Helicobacter pylori seroprevalence in Singapore: correlation with differences in peptic ulcer frequency.
      Of interest, the age-standardized rate of gastric cancer is 1.7 per 100,000 in Malay males, 1.1 per 100,000 in Malay females, compared to 5.6 per 100,000 in Chinese males and 4.1 per 100,000 in Chinese females.
      • AbM Azizah
      • Nor Saleh I.T.
      • Noor Hashima A.
      • et al.
      Malaysian National Cancer Registry Report 2007−2011. Malaysia Cancer Statistics, Data and Figure.
      The reasons for a lower prevalence in Malays and some other ethnic groups need to be further investigated, while genetic factors and environmental factors also must be evaluated. Additionally, indigenous populations in developed countries have much higher HP prevalence. For example, Alaskan Natives in the US had a HP prevalence of 75.0%,
      • Parkinson A.J.
      • Gold B.D.
      • Bulkow L.
      • et al.
      High prevalence of Helicobacter pylori in the Alaska Native population and association with low serum ferritin levels in young adults.
      while the Martu community in Western Australia had a prevalence of 91.0%.
      • Windsor H.M.
      • Abioye-Kuteyi E.A.
      • Leber J.M.
      • et al.
      Prevalence of Helicobacter pylori in Indigenous Western Australians: comparison between urban and remote rural populations.
      These differences likely reflect the disparity in care, reduced sanitation, and lower socioeconomic status that is observed in indigenous populations.
      This study has several strengths. It is one of the most comprehensive and up-to-date reviews on the evolution of the global epidemiology of HP in the 21st century. We included only population-based data, which limited selection bias. Secondly, we pooled data to highlight differences within and between different regions around the world. Recent declines in HP prevalence—particularly in more industrialized nations, such as the United States, China, and Japan—are likely due to rising standards of living, and improved sanitation. However, the cohort effect associated with these changes has become gradually less important for consequent stabilization of the prevalence. What remains unclear is whether the prevalence of HP will continue to drop or remain static. Regardless, surveillance cohorts that track disease burden and preventive strategies are paramount to discovering or confirming suspected environmental factors.
      This review has some limitations. This systematic review contains reports from only 62 of 196 countries globally. Reports were also conducted at different time periods, with several countries lacking recent data, limiting accuracy for inter-region comparison. HP prevalence is generally higher in developing countries, yet reports for many developing countries are not available. For some reports, only selected areas of countries were sampled instead of the entire country (ie, sub-national level), limiting its accuracy to reflect the country’s true prevalence. We assumed that countries with missing data in a region have comparable prevalence to our pooled mean prevalence. Future studies are necessary in areas lacking prevalence to HP to confirm our estimates. Also, our pooled analyses demonstrated significant heterogeneity. We explored some sources of heterogeneity, including age, geographic region, time period, and modality of testing. However, a comprehensive evaluation of heterogeneity was limited by the information available in the primary studies. As well, HP is not a notifiable disease in many countries and its prevalence is mainly derived from willing participants of population-based studies. It is likely these reports may underestimate the true prevalence, especially in areas with poorer access to health care facilities. HP is also usually not routinely included in health screening, reducing the chance of identifying this disease in the general population. Furthermore, the reports used different methods and assays for the diagnosis of HP, with different sensitivities and specificities, which may limit the accuracy of inter-region comparison. Additionally, an underestimation of the lifetime prevalence may occur in older subjects, as infection tends to disappear with the progression of gastric lesions caused by the HP, resulting in a decline in the circulating IgG titers. Despite these limitations, IgG serology was commonly used, as it is a relatively simple, less invasive, and convenient method to screen large populations. In the developing world, defining HP prevalence is considerably more challenging because many countries lack health care systems that compile outcomes into population-based registries.
      Thus, prevalence rates reported are likely to be underestimated in studies published early in the observation period and in developing countries. This may explain why HP prevalence seemed to have remained stable in parts of Asia and Latin America, and the Caribbean when compared with the developed areas in Europe, North America, and Oceania, due to better diagnostics, but also a declining HP prevalence. HP prevalence is related to the acquisition rate in children, which is related to sanitation and clean water. Despite rapidly falling pediatric HP prevalence in China, Korea, and Japan, HP prevalence remained relatively stable artefactually due to the mixed populations, which will take decades to demonstrate a significant change in rate. Lastly, most primary studies lacked key covariates to conduct regression models to evaluate for any additional factors significantly associated with HP prevalence.
      Despite these limitations, this systematic review provides a comprehensive overview of the prevalence of HP. Variation in prevalence of HP observed in different geographic areas and across time suggests that prevalence is influenced by living conditions, such as hygiene status and industrialization of society. Consequently, these data can be used to support regional initiatives to prevent and eradicate HP, with the goal of reducing the complications of HP.

      Acknowledgments

      The authors are grateful to Haiyun Shi and Whitney Tang for their assistance in the initial systematic search.
      Authors' contribution: All authors have contributed to the study design, study identification, data collection, and manuscript revision. All authors have seen and approved the manuscript. SCN and GGK had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.

      Supplementary Material

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      Linked Article

      • Prevalence of Helicobacter pylori Infection in Asia: Remembrance of Things Past?
        GastroenterologyVol. 154Issue 1
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          We read the systematic review and meta-analysis by Hooi et al1 with great interest. Their efforts should be commended for updating and expanding on global prevalence data on Helicobacter pylori infection that were published a few years ago.2 However, the data presented in their article did not capture current epidemiologic changes and the status quo in Asian countries, particularly those in Japan. Our estimate3 finds the prevalence of H pylori in Japan is rapidly decreasing owing in part to the abrupt increase in the number of patients who have been cured of H pylori infection (around 1.4 million per year from around 0.6 million from previous years) since the 2013 change in the health insurance policy to cover H pylori gastritis.
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