Global Prevalence of Helicobacter Pylori Infection PDF

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

analysis
James K.Y. Hooi, Wan Ying Lai, Wee Khoon Ng, Michael M.Y. Suen, Fox E.
Underwood, Divine Tanyingoh, Peter Malfertheiner, David Y. Graham, Vincent W.S.
Wong, Justin C.Y. Wu, Francis K.L. Chan, Joseph J.Y. Sung, Gilaad G. Kaplan,
Siew C. Ng
PII: S0016-5085(17)35531-2
DOI: 10.1053/j.gastro.2017.04.022
Reference: YGAST 61141
To appear in: Gastroenterology

Accepted Date: 19 April 2017
Please cite this article as: Hooi JKY, Lai WY, Ng WK, Suen MMY, Underwood FE, Tanyingoh D,
Malfertheiner P, Graham DY, Wong VWS, Wu JCY, Chan FKL, Sung JJY, Kaplan GG, Ng SC, Global
Prevalence of Helicobacter pylori Infection: Systematic Review and Meta-analysis, Gastroenterology
(2017), doi: 10.1053/j.gastro.2017.04.022.
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Title: Global Prevalence of Helicobacter pylori Infection: Systematic Review and
Meta-analysis
Short title: Helicobacter pylori global prevalence
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Authors: James K.Y. Hooi1,# , Wan Ying Lai1,#, Wee Khoon Ng1,2,#, Michael M.Y. Suen1,#, Fox
E. Underwood3, Divine Tanyingoh3, Peter Malfertheiner4, David Y. Graham5, Vincent W.S.
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Wong1, Justin C.Y. Wu1, Francis K.L. Chan1, Joseph J.Y. Sung1, Gilaad G. Kaplan3,*,
Siew C. Ng1,*
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Co-First Authors – the authors contributed equally to this work
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*Co-Senior Authors – the authors contributed equally to this work
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1. Department of Medicine and Therapeutics, Institute of Digestive Disease, State Key
Laboratory of Digestive Diseases, LKS Institute of Health Science, Chinese University of

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Hong Kong, Hong Kong, China
2. Department of Gastroenterology and Hepatology, Tan Tock Seng Hospital, Singapore.

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3. Departments of Medicine and Community Health Sciences, University of Calgary, Calgary,

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Alberta, Canada
4. Department of Gastroenterology, Hepatology and Infectious Diseases, Otto-von-Guericke

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University of Magdeburg, Magdeburg, Germany

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5. Gastroenterology, Baylor College of Medicine, Houston, Texas, United States

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Grant Support: Nil
Abbreviations: HP (Helicobacter pylori)
Correspondence:
Siew C Ng, MBBS, MRCP, PhD
Department of Medicine and Therapeutics
Chinese University of Hong Kong, Hong Kong
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Tel: 852 2632 1420
Fax: 852 2637 3852
E-mail: siewchienng@cuhk.edu.hk
Gilaad G. Kaplan, MD, MPH, FRCPC
Teaching Research and Wellness Center
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3280 Hospital Drive NW, 6D17
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Calgary, AB, T2N 4N1
Tel: 1 403 592 5015
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Fax: 1 403 592 5050
Email: ggkaplan@ucalgary.ca
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Disclosures: None of the authors have relevant conflict of interests to declare.
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Transcript Profiling: Nil
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Writing Assistance: Nil
Authors' contribution: All authors have contributed to the study design, study identification,
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data collection, and manuscript revision. All authors have seen and approved the manuscript.
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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.

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Acknowledgement: We are grateful to Haiyun Shi and Whitney Tang for their assistance in
the initial systematic search.

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Conflict of Interest Statements

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We declare no competing interests.
Manuscript word count: 5798
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Abstract:
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
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studies of the prevalence of H pylori infection published from January 1, 1970 through
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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
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estimates with 95% CIs, weighted by study size. We extrapolated 2015 prevalence estimates
to obtain the estimated number of individuals with H pylori infection.
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Results: Among 14,006 reports screened, we identified 263 full-text articles on the
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prevalence of H pylori infection; 184 were included in the final analysis, comprising data from
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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
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individual countries, the prevalence of H pylori infection varied from as low as 18.9% in
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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
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worldwide in 2015.
Conclusions: In a systematic review and meta-analysis to assess the prevalence of H pylori

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infection worldwide, we observed large amounts of variation among regions—more than half
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the world’s population is infected. These data can be used in development of customized
strategies for the global eradication.
Keywords: bacteria, incidence, Europe, stomach
Word Count = 266
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Impact Summaries
Background and context:
A significant proportion of the world’s population is infected with Helicobacter pylori (HP), but
global and regional prevalence is not well known, though it varies from low levels in highly
industrialized countries of the West to high levels in developing countries in Africa. Despite
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the prevalence of HP infection decreasing globally, it remains high in many countries.
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Numerous population-based studies have reported the prevalence of HP. We conducted a
systematic review of MEDLINE and EMBASE from 1 Jan 1970 to 1 Jan 2016 to examine the
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global prevalence of HP in the 21st century.
New findings:
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To our knowledge, this is the first study to report the prevalence of HP worldwide. Our study
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provides a comprehensive systematic review of population-based prevalence studies of HP.
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This systematic review identified 184 population-based prevalence studies of HP since 1 Jan
1970. The prevalence of HP varies based on time periods and geography. Overall, HP
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prevalence is decreasing in developed countries and in some developing countries. We also

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highlighted the areas with the highest HP burden.
Limitations:
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Main limitation of this systematic review contains reports from only 62 out of 196 countries
globally, with data lacking in several developing countries. Reports were also conducted at
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different time periods, with several countries lacking recent data, limiting accuracy for
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inter-region comparison. For some reports, only selected areas of countries were sampled
instead of the entire country (i.e. sub-national level), limiting its accuracy to reflect the
country’s true prevalence.
Impact:
This review suggests that approximately 4.4 billion individuals are colonized with HP. These
individuals are at risk for peptic ulcer disease and gastric cancer. Despite reduction in HP
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prevalence in many developed countries, the trend appears to have plateaued. Our data can
be used to prioritize public health efforts in countries with the highest prevalence of HP to
reduce the sequalae associated with infection by HP.
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Introduction
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
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mounting antibiotic resistance.1-3 In many countries, the incidence of HP infection has been
decreasing in association with improved standards of living.4,5 Yet the prevalence of this
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bacterium is still ubiquitous, especially in the Far East.4 It is the main cause of chronic
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gastritis and the principal etiological agent for gastric cancer and peptic ulcer disease.2,6 In
most regions, the main mechanism of spread is intra-familial transmission.7 The prevalence
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remains high in most developing countries and is generally related to socioeconomic status
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and levels of hygiene. Global and regional HP prevalence has not been systematically
reported until now.

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Recent interest has focused on HP eradication as a strategy of eliminating gastric cancer.

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However, the epidemiology and clinical manifestations of the infection has been changing,
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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
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strategies require up-to-date information regarding HP prevalence and disease burden.

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We performed a systematic review of population-based studies reporting HP prevalence of

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different countries over different time periods, with the premise that these data would provide
crucial updates regarding HP global disease burden and the information to plan appropriate
strategies for allocating healthcare resources. We pooled HP prevalence estimates in
different regions and countries, examined the trend in HP prevalence over the past four
decades, and estimated the number of people infected with HP globally. Understanding the
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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
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This systematic review was performed in accordance to the PRISMA 2009 guidelines.8 A
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search using keywords from a combination of Medical Subject Headings (MeSH) and free
text including terms related to HP and prevalence was performed in MEDLINE (R) and
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EMBASE via OvidSP. All suitable published papers from 1 Jan 1970 to 1 Jan 2016 were
identified and subsequently catalogued using EndNote X7. The search strategy is described
in Appendix 1.
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Comprehensive inclusion and exclusion criteria were predefined (Table 1) to facilitate
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objective screening of papers. Only published original observational reports on the

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prevalence of HP in study populations that were reflective of the general population at

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national or sub-national levels were included. Systematic reviews, meta-analyses,
conference presentations, and letters or correspondences were excluded. Suitable reports

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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 (e.g.
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migrants and prisoners). The first phase involved a group of three reviewers (J.H., W.Y.L.,
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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
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written neither in 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 correspondence authors regarding any uncertainties or missing data
(e.g. study periods not explicitly stated) in selected reports. The reports were then grouped by
countries and subsequently into regions based on the United Nations geoscheme devised by
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the United Nations Statistics Division (UNSD).9 Figure 1 details the process of report
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selection.
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Data Extraction and Quality Appraisal
Full text review was performed for all the selected papers and data extracted and sorted into
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the following variables: name of study, leading author, journal, publication year, study period,
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type of study, study location (country and sub-national region), HP diagnostic methods used,
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participant details (number, age, gender ratio), total number of participants, number of HP
positive participants, and HP crude prevalence rate. Data on prevalence as a percent of the
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number of HP positive participants relative to total number tested were recorded or calculated
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with 95% confidence intervals. Papers with missing data, despite attempts to contact the
correspondence authors, were excluded. The quality of the remaining papers was rated with
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the Cochrane Collaboration-endorsed Newcastle-Ottawa Quality Assessment Scale (NOS),10
which was designed to assess aspects of population-based studies of prevalence. The

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quality assessment of each paper is shown in Appendix 2.

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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: (a) geographic

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region based on classification by UN; (b) time period of evaluating prevalence of HP split into
1970 to 1999 and 2000 to 2016; (c) restricting analysis to adult only (age ≥ 18 years); and (d)
primary modality of testing HP including serology, urea breath test, stool antigen, CLO or
histopathology, and serology or urea breath test.
The prevalence data were grouped by geographic region based on the UN geoscheme:
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Northern America, Latin America and the Caribbean, Europe (Northern, Southern, Western,
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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
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separately analyzed 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
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was included in the time period that captured the most updated data. If multiple studies
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reported prevalence for the same country and time period, the pooled estimate was taken.11
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Quartiles of prevalence data were used to create choropleth maps. Next, we created a
web-based interactive map to display comments associated with the prevalence of HP for
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each country. The static and interactive maps were created using QGIS 2.16.312 with the
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HTML Image Map Plugin13 for the interactive map. The geographic data were created by the
Natural Earth Community.14

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Population-based studies that reported HP prevalence with two or more time points for the
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same country were included for temporal trend analyses. For the assessment of potential
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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 average prevalence.
R Studio Version 0.99.903 was used for statistical analysis. The R-metafor package was
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used to generate 95% confidence intervals 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
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There was no funding source for this study. The corresponding authors had full access to all
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data in the study and had final responsibility for the decision to submit for publication.
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Results
A total of 14,006 records were identified from both databases, of which 6,188 records were
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duplicates, 7,611 records were excluded based on selection criteria, 22 records were
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removed due to inaccessible full text, and 3 records could not be translated for review (Figure
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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
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Caribbean, 13 from Northern America, and 6 from Oceania), reporting HP prevalence in 62

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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
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(n=12), Japan (n=11), United States (US) (n=10), Germany (n=8) and Iran (n=8). A summary
of the distribution of papers by regions is shown in Appendix 3 and details of individual

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papers (including age range, gender, and methods to diagnose HP) in Appendix 4 and
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Appendix 5.
Prevalence of HP in the indigenous population of the US 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 US, the pooled HP prevalence
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estimate for the general population was 35.6% (95% CI 30.0–41.1), but it was 74.8%
(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%
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CI 13.1–24.7), Denmark (22.1%, 95% CI 17.8–26.5), New Zealand (24.0%, 95% CI
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21.4–26.5), Australia (24.6%, 95% CI 17.2–32.1), and Sweden (26.2%, 95% CI 18.3–34.1).
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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).
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Regions with the lowest reported HP prevalence were Oceania (24.4%, 95% CI 18.5–30.4),
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Western Europe (34.3%, 95% CI 31.3–37.2), and Northern America (37.1%, 95% CI
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32.3–41.9). HP prevalence and the number of people with HP living in the general population
in the six UN regions were reported in Tables 2 and 3. Forest plots of pooled HP prevalence
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stratified by country and UN region are shown in Appendix 6. Significant heterogeneity was
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observed for pooled analyses in each region (Appendix 6). In order to assess potential
sources of heterogeneity, pooled prevalence was stratified by modality of testing for HP

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(Appendix 7) and adult-only studies (Appendix 8).

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Two time periods (1970–1999 and 2000–2016) were used to analyze the HP prevalence
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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
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shown in Appendix 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
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review shows that approximately 4.4 billion individuals in 2015 worldwide were estimated to
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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
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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
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America (37.1%) and Oceania (24.4%). At the turn of the 21st century the prevalence of HP
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has been declining in highly industrialized countries of the Western world, whereas prevalence
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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
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sequalae associated with HP, including peptic ulcer disease and gastric cancer. These
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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
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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
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from 18.4% to 26.2% and that in non-whites ranges from 34.5% to 61.6%.15,16 Prevalence can
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be as high as 75.0% in the Alaskan Native population.17
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 thus require
further efforts and research focused on prevention of HP acquisition and HP eradication.

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Innovative strategies will likely be needed to reduce HP prevalence in areas such as Africa,
India, and South America, whereby access to healthcare and resources may be limited.
HP has been identified as a Group I carcinogen by the International Agency for Research on
Cancer (IARC) and currently is considered a necessary but insufficient cause of gastric
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adenocarcinoma.18-22 Approximately 89% of all gastric cancers can be attributable to HP
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infection.23 Gastric cancer remains the third most common cancer worldwide with more than
half coming from China, Japan, and Korea. Prognosis is poor with only one in five patients
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surviving longer than five years after diagnosis. HP eradication has been associated with a
reduction of gastric cancer incidence and this benefit is present irrespective of risk group.24-26
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There is also evidence that screening and eradication of HP in young adults in China would
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be cost-effective and could help in preventing one gastric cancer in every four to six cases.26
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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.

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Increasing prophylactic HP vaccination appears to be an option.27 The development of HP

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vaccine has been challenging, but there is yet to be an effective vaccine available in the
market. One promising phase III trial of an oral vaccine in China has demonstrated
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vaccine-mediated protection against HP, leading to a reduced risk of HP acquisition amongst
the younger population.28 The high global prevalence of HP in many parts of the world and
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the non-diminishing HP prevalence in developed countries should serve as the impetus for
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researchers to hasten the process to create an effective vaccine. Of interest, HP vaccination
has also been demonstrated to be cost effective in US, which has one of the lowest HP
prevalence globally.29
In Africa, despite the high HP prevalence, the reported incidence of gastric cancer was
considerably lower compared to China or Japan and was postulated to be related to the
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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 towards a Th2 type
(anti-inflammatory), which may reduce risk of gastric cancer.30,31 The now defunct
phenomenon known as ‘African Enigma’ was attributed to the inadequate sampling of the
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African population obtained through endoscopic data, limited access to health care, and a
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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 previously reported.32
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Ongoing efforts to monitor HP prevalence and its disease burden in a systematic manner is
crucial, as it will minimize any skewed data, which may adversely affect the allocation of
healthcare resources.
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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
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other ethnic groups.4 Malaysia’s population consisted of approximately 67.4% Malays33 and
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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%)
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and Indians (50.7%).34 Besides Malaysia, the Malays in Singapore also had a low HP
prevalence of 25.0%.35 Of interest, the age-standardized rate of gastric cancer is 1.7 per
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100,000 in Malay males, 1.1 per 100,000 in Malay females, compared to 5.6 per 100,000 in
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Chinese males and 4.1 per 100,000 in Chinese females.36 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%,17 while the Martu community in Western
Australia had a prevalence of 91.0%.37 These differences likely reflect the disparity in care,
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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
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population-based data, which limited selection bias. Secondly, we pooled data to highlight
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differences within and between different regions around the world. Recent declines in HP
prevalence – particularly in more industrialized nations such as the United States of America,
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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
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important for consequent stabilization of the prevalence. What remains unclear is whether the
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prevalence of HP will continue to drop or remain static. Regardless, surveillance cohorts that
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track disease burden and preventive strategies are paramount to discovering or confirming
suspected environmental factors.

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This paper has some limitations. This systematic review contains reports from only 62 out of
196 countries globally. Reports were also conducted at different time periods, with several
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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
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available. For some reports, only selected areas of countries were sampled instead of the
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entire country (i.e. 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 average 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

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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 healthcare
facilities. HP is also usually not routinely included in health screening, reducing the chance of
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identifying this disease in the general population. Furthermore, the reports used different
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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
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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
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titers. Despite these limitations, IgG serology was commonly used as it is a relatively simple,
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less invasive and convenient method to screen large populations. In the developing world,
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defining HP prevalence is considerably more challenging because many countries lack
healthcare systems that compile outcomes into population-based registries.

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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
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seemed to have remained stable in parts of Asia and Latin America, and the Caribbean when
compared to the developed areas in Europe, North America, and Oceania, due to better
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diagnostics but also a declining HP prevalence. HP prevalence is related to the acquisition

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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.
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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
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HP.
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Figures:
Figure 1: Flowchart of study selection

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Figure 2: Global prevalence of Helicobacter pylori choropleth map. The online interactive
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global map showing the HP prevalence can be found at the following URL:
https://people.ucalgary.ca/~ggkaplan/HP2016.html
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Tables:
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Table 1: Study selection criteria
Table 2: HP prevalence and number of people living with HP in the general population within
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each country grouped by UN regions

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Table 3: HP prevalence and number of people living with HP in general population in the UN
regions
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Figure 1: Flowchart of study selection
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Figure 2: Global prevalence of Helicobacter pylori (Interactive Map: https://people.ucalgary.ca/~ggkaplan/HP2016.html)
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Certain regions are magnified to display the smaller countries better.

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Tables:
Table 1: Study Selection Criteria

Selection, grading, and clarification of studies
● HP diagnosis must be confirmed by either one of the following tests: HP serology, HP stool
antigen, urea breath test, biopsies for Campylobacter-like organism (CLO) test, rapid urease
test, histology, or culture
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● The study participants must be reflective of the general population in the region
● Data from multicentre and multinational studies were extracted separately and sorted by
countries and regions
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● Studies were classified as national (if stated in the report or multicentre study involving multiple
regions in the country), sub-national (if only a particular region was evaluated), and city level
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● Clarifications with the corresponding authors of studies with missing data were made if possible
(e.g. without specified HP diagnostic method or study period)
● Attempts were made to rectify any data errors found in the studies, in consultation with the
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corresponding authors whenever possible
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Exclusion criteria
Publication Type
● Guidelines
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● Perspectives, correspondence, letters

● Conference abstract or presentation without formal publication
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● Systematic reviews or meta-analyses

● Surveillance registration or national notifiable disease reports of Helicobacter Pylori
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● Studies without defined study periods

Study Type
● Economic analyses
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● Modelling, time series, or transmission studies; mortality or survival analyses; diagnostic assay
or test performance studies; animal studies
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Study Population
● Study populations that are typically associated with higher prevalence of HP (e.g. patients with
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gastric cancer, peptic ulcers)

● High-risk population groups (migrants, refugees, prisoners, individuals [groups] classified as low
socio-economic status, homeless people, adoptees)
● Study participants that were restricted to selected age groups (e.g. children, elderly)
Testing
● HP diagnosis made from methods other than the four 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
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Table 2: HP prevalence and number of people living with HP in the general population within each country grouped by UN regions
Number of Number of Prevalence estimates Population size HP-positive
reporting studies participants (%, 95% CI) per country* population
UN African region
Benin 1 446 74.1 (70.0–78.1) 10 880 000 8 056 640
Burkina Faso 1 188 46.8 (39.7–53.9) 18 106 000 8 475 419
Democratic Republic of Congo 1 133 77.4 (70.3–84.6) 77 267 000 59 835 565
Egypt 1 200 40.9 (15.4–66.4) 91 508 000 37 435 923
Libya 1 360 76.4 (72.0–80.8) 6 278 000 4 795 764
Nigeria 2 648 87.7 (83.1–92.2) 182 202 000 159 700 053
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South Africa 2 1 539 77.6 (59.8–95.5) 54 490 000 42 306 036
Tunisia 2 348 72.8 (53.7–91.9) 11 254 000 8 191 787
UN Latin American and Caribbean region
Argentina 1 493 49.1 (44.7–53.5) 43 417 000 21 313 405
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Bahamas 1 204 57.8 (51.1–64.6) 388 000 224 419
Brazil 6 2 937 71.2 (66.0–76.4) 207 848 000 147 946 206
Chile 1 2 615 74.6 (72.9–76.2) 17 948 000 13 383 824
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Ecuador 1 90 72.2 (63.0–81.5) 16 144 000 11 659 197
Guadeloupe^ 1 854 49.0 (35.3–62.8) 468 000 229 367
Mexico 2 11 820 52.5 (24.7–80.3) 127 017 000 66 709 328
Panama 1 74 54.1 (42.7–65.4) 3 929 000 2 123 625
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UN Northern American region
Canada 1 316 38.0 (32.6–43.3) 35 940 000 13 646 418
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Greenland 2 756 41.4 (37.9– 44.9) 56 000 23 178
United States of America+ 8 16 235 35.6 (30.0–41.1) 321 774 000 114 455 012
UN Asian region
Central Asia (n=1)
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Kazakhstan 1 288 79.5 (74.9–84.2) 17 625 000 14 013 638

Eastern Asia (n=47)
China 22 103 128 55.8 (51.8–59.9) 1 376 049 000 768 110 552
Japan 11 48 979 51.7 (44.7–58.7) 126 573 000 65 387 612
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Korea 11 121 493 54.0 (50.1–57.8) 25 155 000 13 571 123

Taiwan 3 10 616 53.9 (36.6–71.2) 23 381 000 12 600 021
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Southern Asia (n=13)

Iran 8 5 256 59.0 (51.5–66.5) 79 109 000 46 658 488
India 2 407 63.5 (53.4–73.5) 1 311 051 000 831 861 860
Lebanon 1 308 52.0 (46.4–47.5) 5 851 000 3 039 595
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Nepal 1 383 70.1 (65.9–75.1) 28514 000 19 974 057

Pakistan 1 205 81.0 (75.6–86.4) 1 88 925 000 152 991 465
South–Eastern Asia (n=8)
Malaysia 3 9 168 28.6 (19.0–38.2) 30 331 000 8 677 699
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Singapore 2 953 40.8 (37.7–43.9) 5 604 000 2 287 553

Thailand 1 179 43.6 (36.3–50.8) 67 959 000 29 616 532
Vietnam 2 1 241 70.3 (63.3–77.4) 93 448 000 65 712 634
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Western Asia (n=8)

Israel 2 688 68.9 (62.7–75.1) 8 064 000 5 555 290
Oman 2 499 49.1 (11.5–86.7) 4 491 000 2 205 081
Saudi Arabia 1 364 65.9 (61.1–70.8) 31 540 000 20 794 322
Turkey 3 6 036 77.2 (71.4–83.1) 78 666 000 60 761 618
UN European region
Eastern Europe (n= 10)
Czech Republic 3 4 644 41.2 (24.8–57.6) 10 543 000 4 342 662
Poland 3 7 806 66.6 (56.4–76.7) 38 612 000 25 707 870
Romania 1 960 68.5 (65.6–71.5) 19 511 000 13 372 839
Russian Federation 3 4 771 78.5 (67.1–89.9) 143 457 000 112 585 054
Northern Europe (n = 22)
Denmark 2 37 741 22.1 (17.8–26.5) 5 669 000 1 254 550
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Estonia 2 2 198 82.5 (75.1–90.0) 1 313 000 1 083 356
Finland 1 896 56.8 (46.5–67.0) 5 503 000 3 124 603
Iceland 2 834 36.0 (32.7–39.2) 329 000 118 341
Ireland 1 1 000 43.0 (39.9–46.1) 4 688 000 2 015 840
Latvia 1 3 564 79.2 (77.9–80.5) 1 971 000 1 561 229
Norway 3 4 068 30.7 (20.5–40.8) 5 211 000 1 597 172
Sweden 5 7 149 26.2 (18.3–34.1) 9 779 000 2 563 076
United Kingdom 5 15 098 35.5 (14.5–56.5) 64 716 000 22 974 180
Southern Europe (n= 22)
Albania 1 101 53.5 (43.7–63.2) 2 897 000 1 549 026
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Croatia 3 6 538 52.7 (42.5–62.8) 4 240 000 2 234 056
Greece 3 1 571 52.1 (40.2–64.0) 10 955 000 5 708 651
Italy 5 9 055 56.2 (46.9–65.4) 59 798 000 33 606 476
Portugal 1 2 067 86.4 (84.9–87.9) 10 350 000 8 942 400
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San Marino 2 3 765 47.5 (40.5–54.5) 32 000 15 200
Spain 7 2 721 54.9 (48.6–61.1) 46 122 000 25 307 141
Western Europe (n= 16)
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Belgium 3 27 845 32.7 (22.4–43.0) 11 299 000 3 694 773
France# 1 64 46.9 (34.7–59.1) 64 395 000 30 188 376
Germany 8 19 015 35.3 (31.2–39.4) 80 689 000 28 483 217
Netherlands 3 8 592 35.5 (30.1–41.0) 16 925 000 6 011 760
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Switzerland 1 175 18.9 (13.1–24.7) 8 299 000 1 565 191
UN Oceania region
Australia+ 4 4 485 24.6 (17.2–32.1) 23 969 000 5 905 962
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New Zealand 1 1 060 24.0 (21.4–26.5) 4 529 000 1 085 148
* Based on United Nations 2015 Revision of World Population Prospects total population estimates
^
Insular region of France located in the Caribbean
+
Data related to the indigenous population was excluded from this table
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Guadeloupe data not included in the pooled analysis for France due to different demographics
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Table 3: HP prevalence and number of people living with HP in the general population in the UN regions
Prevalence
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estimates Population size per
*
(%, 95% CI) region / country HP-positive population (range)
UN Africa region 79.1 (62.6–95.6) 1 186 178 282 938 267 021 (742 547 604 – 1 133 986 437)
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UN Latin American and Caribbean
63.4 (59.2–67.6) 634 386 567 402 201 083 (375 556 847 – 428 845 319)
region
Caribbean 52.6 (45.2–60.0) 43 199 297 22 731 470 (19 526 082 – 25 919 578)
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Central America 53.0 (32.6–73.5) 172 740 074 91 621 335 (56 313 264 – 126 963 954)
South America 69.4 (63.9–74.9) 418 447 196 290 318 665 (267 387 758 – 313 416 949)
UN Northern American region 37.1 (32.3–41.9) 357 838 036 132 614 776 (115 581 685 – 149 934 137)
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UN Asian region 54.7 (51.3–58.1) 4 393 296 014 2 403 132 920 (2 253 760 855 – 2 552 504 984)
Central Asia 79.5 (74.9–84.2) 67 314 033 53 521 388 (50 418 210 – 56 678 415)
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Eastern Asia 54.1 (50.8–57.5) 1 612 286 941 872 892 150 (819 041 766 – 92 706 4991)
Southern Asia 61.6 (55.9–67.4) 1 822 974 074 1 123 134 327 (1 019 042 507 – 1228 684 525)
South–Eastern Asia 43.1 (31.5–54.8) 633 489 946 273 287 563 (199 549 332 – 347 152 490)
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Western Asia 66.6 (56.1–77.0) 257 231 020 171 212 967 (144 306 602 – 198 067 885)
UN European region 47.0 (41.8–52.1) 738 442 070 347 067 773 (308 668 785 – 384 728 318)
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Eastern Europe 62.8 (48.3–77.2) 292 942 778 183 850 887 (141 491 361 – 226 151 824)
Northern Europe 41.6 (32.4–50.7) 102 357 768 42 550 124 (33 163 916 – 51 895 388)
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Southern Europe 55.0 (49.1–61.0) 152 347 892 83 852 280 (74 802 814 – 92 932 214)
Western Europe 34.3 (31.3–37.2) 190 793 632 66 396 184 (59 718 406 – 70 975 231)
UN Oceania region 24.4 (18.5–30.4) 39 331 130 9 608 595 (7 276 259 – 11 956 663)
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Global 4 356 096 968 (3 750 167 566 – 4 961 780 681)
* Based on United Nations 2015 Revision of World Population Prospects total population estimates
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Author names in bold designate shared co-first authorship
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Appendix
Appendix to ‘Global helicobacter pylori prevalence: A systematic review and meta–analysis of

population–based studies published between 1970 and 2016’.
This appendix provides supplemental information on this systematic review. It is divided into six
appendices (Appendix 1 – 6).
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Table of contents
Appendix 1: MEDLINE and EMBASE search strategy for article selection (from 1 Jan 1970
till 1 Jan 2016)
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Appendix 2: Quality assessment of selected papers
Appendix 3: Distribution of included papers by regions and countries
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Appendix 4: Country and region specific prevalence of HP since 1 Jan 1970 to 1 Jan 2016
in Northern America, Southern America, Oceania, Eastern Asia, Southern Asia,
Western Asia, Northern Europe, Southern Europe, Western Europe and
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Northern Africa
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Appendix 5: Studies included in this systematic review
Appendix 6: Pooled HP prevalence stratified by country and UN region

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Appendix 7: Pooled HP prevalence stratified by modality of testing
Appendix 8: Pooled HP prevalence stratified by adult-only studies

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Appendix 9: HP prevalence time trend in the six United Nations regions

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Appendix 1: MEDLINE and EMBASE search strategy for article selection (1 Jan 1970 to 1 Jan
2016)
Search Period
- EMBASE: 1 Jan 1970 to 1 Jan 2016

- MEDLINE(R): 1 Jan 1970 to 1 Jan 2016
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Keywords used
- HP or
- Helicobacter Pylori or
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- H$ Pylori or
- Campylobacter pylori &
- Prevalence
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* Representativeness
First Author (Publication Year) +
of the cases
Aguemon, B. D. (2005) B
Akin, L. (2004) A
Alavi, S. M. (2010) B
Al–Balushi, M. S. (2013) B
Al–Moagel, M. A. (1990) B
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Alwahaibi, N. (2013) B
Ang, T. L. (2005) A
Apostolopoulos, P. (2002) B
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Aro, P. (2004) A
Asfeldt, A. M. (2008) A
Awdalla, H. I. (2010) B
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Babus, V. (1997) A
Babus, V. (1998) B
Baena Diez, J. M. (2002) B
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Bakka, A. S. (2002) B
Bastos, J. (2013) A
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Bazzoli, F. (2001) A
Ben Ammar, A. (2003) B
Bergenzaun, P. (1996) B
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Blecker, U. (1995) A
Borch, K. (2000) B
Breckan, R. K. (2009) A
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Breckan, R. K. (2012) A
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Brenner, H. (1997) B
Brenner, H. (1999) A
Brown, L. M. (2002) B
Buckley, M. J. M. (1998) B
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Bures, J. (2006) A
Bures, J. (2012) A
Cardenas, V. M. (2006) A
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Cardenas, V. M. (2010) B
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Carter, F. P. (2011) B
Cataldo, F. (2004) B
Celinski, K. (2006) B
Chen, J. (2007) B
Chen, S. (2002) B
Chen, S. L. (2003) B
Chen, S. Y. (2005) B
Chen, T. S. (2007) B
Cheng, H. (2009) B
Collett, J. A. (1999) B
Correa, P. (1990) B
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Dahlerup, S. (2011) A
De Oliveira, A. M. R. (1999) B
Dite, P (1998) B
Do, M. Y. (2009) B
Dominici, P. (1999) A
Dooley, C. P. (1989) B
Dube, C. (2009) B
Everhart, J. E. (2000) B
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Fan, H. M. (2006) B
Farshad, S. (2010) B
Ferreccio, C. (2007) A
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Fich, A. (1993) B
Fitzgibbons, P. L. (1988) B
Forman, D. (1990) B
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Fujimoto, Y. (2007) B
Fujisawa, T. (1999) B
Fukao, A. (1993) B
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Gasbarrini, G. (1995) A
Gilboa, S. (1995) B
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Gill, H. H. (1994) B
Glupcyznski, Y. (1992) B
Goh, K. L. (2001) A
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Graham, D. Y. (1991) B
Guo, X. (2011) B
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Hirai, I. (2009) B
Hirai, I. (2010) B
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Hirayama, Y. (2014) B
Hoang, T. T. (2005) B
Holcombe, C. (1992) B
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Holtmann, G. (1994) B
Holtmann, G. (2001) B
Hong, S. N. (2012) B
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Jafarzadeh, A. (2006) B
Jafarzadeh, A. (2007) B
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Kang, J. Y. (1997) B
Katsanos, K. H. (2010) B
Kawamura, A. (2001) B
Kebria, F. G. (2011) B
Kikuchi, S. (2004) B
Kim, H. J. (2008) B
Kim, J. H. (2001) B
Kim, N. (2008) B
Koch, A. (2005) B
Kuepper–Nybelen, J. (2005) A
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Kumagai, T. (1998) B
Laszewicz, W. (2014) A
Le Bodic, M. F. (1987) B
Lee, S. P. (2015) B
Lehmann, F. S. (2000) B
Leja, M. (2012) A
Lim, S. H. (2013) B
Lin, J. T. (1993) B
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Lin, Y. L. (2010) B
Linneberg, A. (2003) A
Loffeld, R. J. (2003) B
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Loffeld, R. J. L. F. (2003) B
Luzza, F. (1997) B
Lyra, A. C. (2003) B
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Macenlle Garcia, R. (2006) B
Malaty, H. M. (1996) B
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Mansour, K. B. (2010) B
Martin–de–Argila, C. (1996) B
Marusic, M. (2013) A
Matysiak–Budnik, T. (1996) B
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McDonagh, T. A. (1997) A
Melius, E. J. (2013) B
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Mendall, M. A. (1992) B
Miendje Deyi, V. Y. (2011) A
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Milman, N. (2003) B
Moujaber, T. (2008) B
Murray, L. J. (1997) A
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Naja, F. (2012) A
Nam, J. H. (2014) B
Nascimento, R. S. (2002) B
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Nguyen, T. L. (2010) B
Nouraie, M. (2009) B
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Nurgalieva, Z. Z. (2002) B
Olmos, J. A. (2000) B
Ophori, E. A. (2011) B
Ozaydin, N. (2013) A
Palli, D. (1993) B
Pandeya, N. (2011) A
Parkinson, A. J. (2000) B
Pateraki, E. (1990) B
Patterson, T. (2012) B
Peach, H. G. (1997) B
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Pretolani, S. (1997) A
Ràfols Crestani, A. (2000) B
Rasheed, F. (2011) B
Replogle, M. L. (1996) B
Reshetnikov, O. V. (2001) B
Robertson, M. S. (2003) B
Rodrigo Sáez, L. (1997) A
Rothenbacher, D. (1997) B
PT
Russo, A. (1999) B
Salomaa–Rasenen, A. (2006) B
Sanchez Ceballos, F. (2007) B
RI
Santos, I. S. (2005) B
Santos, I. S. (2009) B
Sasaki, T. (2009) B
SC
Sasaki, T. (2009) B
Sasidharan, S. (2009) B
Sathar, M. A. (1994) B
U
Seher, C. (2000) A
Senra–Varela, A. (1998) B
AN
Sheikhian, A. (2011) B
Sherpa, T. W. (2012) B
Shi, R. (2008) B
M
Singh, V. (2002) B
So ̈rberg, M. (2003) B
Sporea, I. (2003) B
D
Stone, M. A. (1998) A
Sung, K. C. (2005) B
TE
Talaiezadeh, A. (2013) B
Tang, H. R. (2014) B
Thjodleifsson, B. (2007) B
EP
Tomasi, J. P. (1990) A
Torres, J. (1998) A
Tsukanov, V. V. (2007) B
C
Ueda, J. (2014) B
Us, D. (1998) B
AC
Uyub, A. M. (1994) B
van Blankenstein, M. (2013) B
Veldhuyzen Van Zanten, S. J. O. (1994) B
Vorobjova, T. (1994) A
Vyse, A. J. (2002) A
Wang, M. Y. (2011) B
Weill, F. X. (2002) B
Wex, T. (2011) B
Windsor, H. M. (2005) B
Wong, B. C. Y. (1999) B
ACCEPTED MANUSCRIPT
Wong, B. C. Y. (1999) B
Xu, C. (2014) B
Yim, J. Y. (2007) B
Zaterka, S. (2007) B
Zhang, D. H. (2009) B
Zhang, X. (1999) B
Zheng, Y. (2014) B
Zhou, X. (2013) B
PT
Zhou, Z. F. (1997) B
* All included papers were graded ‘A’ under the category of ‘Is the case definition adequate’
RI
+ Representativeness of the cases
A: Truly representative of the average prevalence of Helicobacter Pylori in the community
SC
B: Somewhat representative of the average prevalence of Helicobacter Pylori in the community
C: Selected group of users; e.g. nurses, volunteers
D: No description of the derivation of the cohort
U
A representative study population is a prerequisite for a study to be included in this systematic review.
Studies which included study populations that were not randomly sampled across the entire country
AN
or had a small population size were graded ‘B’.
M
D
TE
C EP
AC
ACCEPTED MANUSCRIPT
Appendix 3: Distribution of included reports by regions and countries
UN geoscheme Number of Number of Number of Total number

countries studies positive of
represented participants participants
detected
Africa 8 11 2 806 3 862
Asia 18 75 165 318 309 811
Europe 24 66 68 501 173 502
#
Latin America and Caribbean 8 13 12 696 19 087
Northern America 3 13 6 905 19 553
PT
Oceania 2 6 1 542 6 065
Total number of countries 62 184 257 768 531 880
#
Includes Guadeloupe which is an insular region of France located in the Caribbean
RI
U SC
AN
M
D
TE
C EP
AC
ACCEPTED MANUSCRIPT
Appendix 4: Country and region specific prevalence of HP since 1 Jan 1970 to 1 Jan 2016 in Northern America, Southern America, Oceania,
Eastern Asia, Southern Asia, Western Asia, Northern Europe, Southern Europe, Western Europe and Northern Africa
HP 95%
First Author At risk Sex
Country Region Study period prevalence Confidence Methods to diagnose HP Age Range
(Publication Year) population (Male%)
PT
(%) interval (%)
Africa (n=11)
Aguemon, B. D.
Benin Cotonou 2003–2004 240 75.4 70.0-80.9 Serology 2-73 48.3
RI
(2005)1
Aguemon, B. D.
Benin Pahou 2003–2005 206 72.3 66.2-78.4 Serology 2-73 44.2
(2005)1
Cataldo, F. (2004)2
SC
Burkina Faso ~ 188 46.8 39.7-53.9 Serology 16-65 53.7
Democratic
Glupcyznski, Y.
Republic of Katana ~ 133 77.4 70.3-84.6 UBT 5-67 ~
(1992)3
Congo
U
Awdalla, H. I. (2010)4 Egypt Nasr City ~ 100 28.0 19.2-36.8 Serology 16-60 57.0
Awdalla, H. I. (2010)4 Egypt Unshass ~ 100 54.0 44.2-63.8 Serology 16-60 63.0
AN
5
Bakka, A. S. (2002) Libya ~ 360 76.4 72.0-80.8 Serology 1-70 49.0
Holcombe, C. (1992)6 Nigeria Northern Nigeria 1989 268 85.1 80.8-89.3 Serology ≥5 ~
M
7
Ophori, E. A. (2011) Nigeria Agbor ~ 380 89.7 86.7-92.8 Serology ≥1 47.4
8
Sathar, M. A. (1994) South Africa ~ 1183 68.6 65.9-71.2 Serology 17-87 ~
D
Alice, Nkonkobe
Dube, C. (2009)9 South Africa 2008 356 86.8 83.3-90.3 Stool antigen 3m-60 yo 47.2
Municipality
TE
Ben Ammar, A.
Tunisia 2000 98 82.7 75.2-90.2 Histology, serology, RUT 18-80 50.0
(2003)10
Mansour, K. B.
Tunisia Tunis 2006–2007 250 63.2 57.2-69.2 Serology 25-55 84.8
(2010)11
EP
Central Asia (n=1)
Nurgalieva, Z. Z.
Kazakhstan 1999 288 79.5 74.9-84.2 Serology 10-69 ~
(2002)12
Eastern Asia (n=45)
C
13
Forman, D. (1990) China 1983 1882 60.4 58.2-62.6 Serology 35-64 50.0
AC
14
Zhou, Z. F. (1997) China Yunnan 1994 1084 51.1 48.1-54.1 Serology 5-80 85.1
Wong, B. C. Y.
China Changle (Fujian) 1994 755 81.7 79.0-84.5 Serology ~ ~
(1999a)15
Wong, B. C. Y.
China Changle (Fujian) 1994 1456 80.4 78.3-82.4 Serology 36-65 61.2
(1999b)16
Wong, B. C. Y.
China Hong Kong 1993–1994 397 58.4 53.6-63.3 Serology 36-65 57.4
(1999b)16
ACCEPTED MANUSCRIPT
Zanhuang County,
Zhang, X. (1999)17 China 1996–1997 1504 66.4 64.0-68.7 Serology ≥30 37.1
Hebei Province
Chen, S. (2002)18 China Shanghai urban 1990 896 42.8 39.5-46.0 Serology 7-85 61.2
18
Chen, S. (2002) China Shanghai rural 1990 1040 61.0 58.0-63.9 Serology 7-85 61.2
PT
Chen, S. (2002)18 China Shanghai urban 2001 1557 58.3 55.9-60.8 Serology 1-87 63.0
Linqu County,
Brown, L. M. (2002)19 China 1997–1998 3013 66.2 64.5-67.9 Serology and UBT 35-69 44.4
Shandong Province
RI
Chen, S. L. (2003)20 China Shanghai urban 1990 896 40.5 37.3-43.7 Serology 1-87 62.3
20
Chen, S. L. (2003) China Shanghai urban 2001 1557 58.3 55.9-60.8 Serology 1-87 63.1
SC
21 Serology, UBT, stool
Chen, S. Y. (2005) China Shanghai urban 2003–2004 1822 66.4 64.2-68.6 15-72 50.7
antigen
22
Fan, H. M. (2006) China Zunhua City, Hebei 2004 263 57.4 51.4-63.4 Serology 6-86 45.3
U
23
Chen, J. (2007) China Guangzhou 1993 830 56.0 52.7-59.4 Serology 3-92 51.1
Chen, J. (2007)23 China Guangzhou 2003 1471 47.0 44.5-49.6 Serology 3-92 51.7
AN
24
Shi, R. (2008) China Jiangsu 2004–2005 1371 62.1 59.5-64.6 Serology, UBT 5-100 42.7
Beijing: rural Pinggu
Cheng, H. (2009)25 China 2003 1232 46.8 44.0-49.5 UBT 2-79 53.1
and urban Haidian
M
Beijing: Yanqing
Zhang, D. H. (2009)26 China 2006 503 41.4 37.1-45.7 Stool antigen 40-79 47.4
County
D
Shandong: Muping
Zhang, D. H. (2009)26 China 2006 526 51.0 46.7-55.2 Histology 40-79 47.4
County
TE
Guo, X. (2011)27 China Northern China ~ 798 54.5 51.1-58.0 Serology > 17 55.3
28
Wang, M. Y. (2011) China ShanDong 2008–2010 1637 35.5 33.2-37.8 Serology, UBT ~ 60.8
EP
Zhou, X. (2013)29 China Jiangsu 2009–2011 5417 63.4 62.1-64.7 UBT 30-69 43.2
Tang, H. R. (2014)30 China Chengdu, Sichuan 2009–2012 8365 53.1 52.1-54.2 UBT 11-95 59.1
31
Zheng, Y. (2014) China Beijing 2005–2011 54036 47.0 46.6-47.4 UBT 15-81 68.0
C
32
Xu, C. (2014) China Zhejiang 2013 8820 43.8 42.7-44.8 UBT 39-53 59.7
AC
Chu–Tung, Po–Tzu,
Lin, J. T. (1993)33 Taiwan 1992 823 54.4 51.0-57.8 Serology <10->70 49.8
Pei–Nan, and Ta–An
Chen, T. S. (2007)34 Taiwan Taipei 1999–2000 482 68.3 64.1-72.4 Serology 56.9±14.0 58.1
Lin, Y. L. (2010)35 Taiwan Chiayi County 2004–2006 9311 39.2 38.3-40.2 CLO > 40 42.0
ACCEPTED MANUSCRIPT
Akita, Iwate, Miyagi,

Fukao, A. (1993)36 Japan 1815 51.7 49.4-54.0 Serology 16-64 50.0
Okinawa
Replogle, M. L.
Japan Tokyo 1979–1993 1207 38.9 36.2-41.7 Serology 0-94 ~
(1996)37
Kumagai, T. (1998)38 Japan South Kiso town 1986–1994 664 73.2 69.8-76.6 Serology 6-80 ~
PT
Seven prefectures
(Nagano, Niigata,
Fujisawa, T. (1999)39 Japan Gunma, Toyama, 1974 264 72.7 67.4-78.1 Serology 0-89 43.6
RI
Shizuoka, Mie, and
Miyagi)
SC
Seven prefectures
(Nagano, Niigata,
Fujisawa, T. (1999)39 Japan Gunma, Toyama, 1984 238 54.6 48.3-61.0 Serology 0-89 43.6
Shizuoka, Mie, and
U
Miyagi)
Seven prefectures
AN
(Nagano, Niigata,
39
Fujisawa, T. (1999) Japan Gunma, Toyama, 1994 264 39.4 33.5-45.3 Serology 0-89 43.6
Shizuoka, Mie, and
Miyagi)
M
Malaty, H. M. (2003)40 Japan South Kiso town 1986 394 80.0 76.0-83.9 Serology 0-80 ~
Kikuchi, S. (2004)41 Japan 1989 3014 42.7 40.9-44.4 Serology 39->65 81.1
D
<=17 and
Fujimoto, Y. (2007)42 Japan Ishigaki City 2002 238 52.5 46.2-58.9 Serology 46.5
22-79
TE
Fujimoto, Y. (2007)42 Japan Kasuya Town 2002 3310 55.0 53.3-56.7 Serology 20-89 30.4
Fujimoto, Y. (2007)42 Japan Hoshino Village 2002 271 63.1 57.4-68.8 Serology 21-84 48.0
43
Hirai, I. (2009) Japan Osaka 2007 186 40.3 33.3-47.4 Stool antigen 40-63 35.0
EP
Kawamura, A. (2001)44 Japan Shimane 1998–1999 2263 43.0 41.0-45.1 Serology 16-80 70.6
45
Hirayama, Y. (2014) Japan Tokyo 2008 21144 27.5 26.9-28.1 Serology > 35 87.0
C
Seven areas in
Ueda, J. (2014)46 Japan 1997–2013 13707 41.2 40.4-42.0 Serology, stool antigen ≥ 20 42.4
Japan
AC
Malaty, H. M. (1996)47 Korea Seoul 1992–1993 413 42.6 37.9-47.4 Serology 1-75 ~
Kim, J. H. (2001)48 Korea Seoul 1998 1155 41.9 39.1-44.8 Serology 0-79 50.0
Sung.K.C (2005)49 Korea Seoul and Kyunggi 2001–2002 58981 70.9 70.5-71.3 Serology <30->60 62.7
Seoul, Jeju,
Yim, J. Y. (2007)50 Korea 2005 8020 59.6 58.5-60.7 Serology ≥ 20 54.1
Kangwon
Kim, H. J. (2008)51 Korea 2003–2007 713 57.6 54.0-61.3 CLO, histology 23-85 41.8
ACCEPTED MANUSCRIPT
Kim, N. (2008)52 Korea 2006 20154 60.4 59.7-61.1 Serology, CLO, histology 16->70 59.0
The Health
Promotion Centers
of Severance
Do, M. Y. (2009)53 Korea 1998 696 64.7 61.1-68.2 CLO, histology 17-92 69.1
hospital or Chung–
PT
Ang University
hospital
The Health
Promotion Centers
RI
of Severance
Ang University
SC
hospital
The Health
Promotion Centers
of Severance
U
Ang University
hospital
AN
The Health
Promotion Centers
of Severance
M
Ang University
hospital
The Health
D
Promotion Centers
of Severance
TE
Ang University
hospital
The Health
Promotion Centers
EP
of Severance
Ang University
hospital
C
The Health
Promotion Centers
AC
of Severance
Ang University
hospital
The Health
Promotion Centers
Do, M. Y. (2009)53 Korea of Severance 2005 1662 40.0 37.7-42.4 CLO, histology 17-92 71.1
Ang University
ACCEPTED MANUSCRIPT
hospital
Kim, J. H. (2001)48 Korea Kyonggi 1998 1308 47.3 44.6-50.0 Serology 0-79 50.0
48
Kim, J. H. (2001) Korea Kangwon 1998 251 53.4 47.2-59.6 Serology 0-79 50.0
48
PT
Kim, J. H. (2001) Korea Chungcheong 1998 799 43.7 40.2-47.1 Serology 0-79 50.0
Kim, J. H. (2001)48 Korea Kyungsang 1998 1266 47.1 44.3-49.8 Serology 0-79 50.0
48
Kim, J. H. (2001) Korea Cholla 1998 728 50.6 46.9-54.2 Serology 0-79 50.0
RI
Kim, J. H. (2001)48 Korea Cheju 1998 225 52.9 46.4-59.4 Serology 0-79 50.0
54
Hong, S. N. (2012) Korea Seoul 2010 2195 57.1 55.0-59.2 Serology ~ 62.0
SC
Lim, S. H. (2013)55 Korea Seoul 2011 5829 50.0 48.8-51.3 Serology Above 16 54.8
55
Lim, S. H. (2013) Korea Gyeonggi 2011 1683 53.4 51.0-55.7 Serology Above 16 54.8
Lim, S. H. (2013)55 Korea Chungcheong 2011 536 55.4 51.2-59.6 Serology Above 16 54.8
U
55
Lim, S. H. (2013) Korea Kyungsang 2011 914 65.1 62.0-68.2 Serology Above 16 54.8
AN
55
Lim, S. H. (2013) Korea Cholla 2011 1194 66.2 63.5-68.9 Serology Above 16 54.8
Lim, S. H. (2013)55 Korea Kangwon 2011 331 60.4 55.2-65.7 Serology Above 16 54.8
Lim, S. H. (2013)55 Korea Jeju 2011 299 58.9 53.3-64.4 Serology Above 16 54.8
M
Nam, J. H. (2014)56 Korea 2006–2007 632 59.0 55.2-62.9 Serology 21-68 49.2
Lee, S. P. (2015)57 Korea Seoul 2010–2013 3314 59.5 57.8-61.2 Serology <39->70 60.8
D
Southern Asia (n=13)
Jafarzadeh, A. (2006)58 Iran Rafsanjan 2004 138 73.2 65.8-80.6 Serology 17-60 47.1
TE
59
Jafarzadeh, A. (2007) Iran Rafsanjan 2005 200 67.5 61.0-74.0 Serology 20-60 51.4
Nouraie, M. (2009)60 Iran Tehran province 2005 2326 69.0 67.1-70.9 Serology 18-65 58.4
EP
Razi hospital in
Alavi, S. M. (2010)61 Iran 2004–2005 96 57.3 47.4-67.2 Serology <30->60 48.0
Ahvaz
Farshad, S. (2010)62 Iran 2005–2007 226 41.6 35.2-48.0 CLO 18-83 49.0
C
63
Kebria, F. G. (2011) Iran Golestan province 2008–2009 1028 66.4 63.6-69.3 Serology 1-83 47.6
Sheikhian, A. (2011)64 Iran Khorramabad 2008 381 43.0 38.1-48.0 Serology 15-88 40.5
AC
Talaiezadeh, A.
Iran Khuzestan Province 2009 861 53.5 50.2-56.9 Stool antigen 0-80 ~
(2013)65
Singh, V. (2002)66 India Chandigarh ~ 67 56.7 44.9-68.6 Serology, RUT, histology > 15 48.0
Gill, H. H. (1994)67 India Hospital ~ 340 67.4 62.4-72.3 Serology 0-68 66.8
Upper Khumbu
Sherpa, T. W. (2012)68 Nepal ~ 383 70.5 65.9-75.1 Stool antigen >=0 45.4
Region
ACCEPTED MANUSCRIPT
Rasheed, F. (2011)69 Pakistan Barakho, Islamabad 2009–2010 205 81.0 75.6-86.4 UBT > 19 49.0
mean
Naja, F. (2012)70 Lebanon 2009–2010 308 52.0 46.4-57.5 Serology age:40.97 ± 46.8
15.5
South-Eastern Asia (n=8)
PT
Uyub, A. M. (1994)71 Malaysia 1991–1992 1417 4.7 3.6-5.8 Serology 11-91 ~
Kuala Pilah, West
Goh, K. L. (2001)72 Malaysia ~ 626 31.8 28.1-35.4 Serology 12-92 43.3
RI
Malaysia
Kuala Lumpur, West

Malaysia
SC
Kota Baru, West
Goh, K. L. (2001)72 Malaysia ~ 322 26.4 21.6-31.2 Serology 12-92 ~
Malaysia
Kota Kinabalu, East
U
Malaysia
AN
Sibu, East, East
Malaysia
Sasidharan, S.
Malaysia Penang 2000–2002 5370 14.2 13.2-15.1 Serology 10-70 68.5
(2009)73
M
Kang, J. Y. (1997)74 Singapore 1992–1993 358 40.2 35.1-45.3 Serology 20-60 ~
75
Ang, T. L. (2005) Singapore 1998 595 41.2 37.2-45.1 Serology 25-39,55-69 ~
D
Hirai, I. (2010)76 Thailand 2007–2008 179 43.6 36.3-50.8 Stool antigen 40-80 28.5
Hoang, T. T. (2005)77 Vietnam Urban Hanoi ~ 546 78.8 75.3-82.2 Serology 1-88 42.3
TE
77
Hoang, T. T. (2005) Vietnam Rural Hatay ~ 425 69.2 64.8-73.6 Serology 1-88 46.4
Nguyen, T. L. (2010)78 Vietnam Ho Chi Minh ~ 136 64.7 56.7-72.7 Serology, culture, histology 14-86 43.3
Nguyen, T. L. (2010)78
EP
Vietnam Urban Hanoi ~ 134 66.4 58.4-74.4 Serology, culture, histology 14-86 43.3
Western Asia (n=8)
Fich, A. (1993)79 Israel ~ 311 65.6 60.3-70.9 Serology 20-70 54.7
C
80
Gilboa, S. (1995) Israel Kibbutzim ~ 377 71.9 67.4-76.4 Serology 30-90 ~
AC
Us, D. (1998)81 Turkey Ankara 1996–1997 284 70.1 64.7-75.4 Serology 20-59 50.0
Gulveren Health
Akin, L. (2004)82 Turkey 2004 1089 77.4 74.9-79.9 Serology 25-64 54.3
District, Ankara
Ozaydin, N. (2013)83 Turkey 2000 1089 82.6 81.5-83.7 UBT Above 18 45.2
males with
Alwahaibi, N. (2013)84 Oman 2007–2010 366 30.1 25.4-34.8 CLO mean age 46.7
of 47.87±19
ACCEPTED MANUSCRIPT
years
females
with mean
age of
45.21±17.56
years
PT
Al–Balushi, M. S. SQU Hospital’s
Oman 2011–2012 133 68.4 60.5-76.3 Serology 15-50 73.7
(2013)85 Blood Bank
RI
Al–Moagel, M. A.
Saudi Arabia Riyadh City ~ 364 65.9 61.1-70.8 Serology 5-91 47.9
(1990)86
Eastern Europe (n=10)
SC
Czech The South Moravia
Dite, P. (1998)87 1998 309 58.9 53.4-64.4 Serology 20-59 ~
Republic Region
Czech
Bures, J. (2006)88 Across the country 2001 2509 41.7 39.8-43.6 UBT 5-100 47.4
U
Republic
Czech
Bures, J. (2012)89 2010 1826 23.6 21.6-25.5 UBT 5-98 46.9
AN
Republic
Matysiak–Budnik, T.
Poland Wroclaw 1992 656 73.0 69.6-76.4 Serology 0-86 ~
(1996)90
91
Celinski, K. (2006) Poland Lublin ~ 585 68.7 65.0-72.5 Serology 19-89 ~
M
92
Laszewicz, W. (2014) Poland 10 regions 2002–2003 6565 58.3 57.1-59.5 Serology 2-89 ~
93
Sporea, I. (2003) Romania Timis County ~ 960 68.5 65.6-71.5 Serology 18-60 78.5
D
94 Russian
Malaty, H. M. (1996) St. Petersburg ~ 520 61.9 57.8-66.1 Serology 1-75 ~
Federation
TE
Reshetnikov, O. Russian
Novosibirsk, Siberia 1994–1995 649 86.0 83.3-88.7 Serology 18-64 48.8
(2001)95 Federation
Eastern Siberia:
Tsukanov, V. V. Russian
Evenkia, Khakassia, ~ 3602 87.0 85.9-88.1 Serology 47.3
(2007)96
EP
Federation
Tuva
Northern Europe (n=19)

97
C
Linneberg, A. (2003) Denmark Copenhagen 1990–1991 1112 24.6 22.0-27.1 Serology 15-69 ~
East coast of the

AC
Dahlerup, S. (2011)98 Denmark Danish peninsula of ~ 36629 20.1 19.7-20.5 UBT 2-95 40.3
Jutland
Vorobjova, T., (1994)99 Estonia Karksi–Nuia 1990 1461 87.0 85.3-88.7 Serology 15-95 43.6
Vorobjova, T., (1994)99 Estonia Abja–Paluoja 1990 497 89.3 86.6-92.1 Serology 50-91 38.0
Thjodleifsson, B.
Estonia Tartu 1991–2001 240 69.2 63.3-75.0 Serology 25-50 40.0
(2007)100
ACCEPTED MANUSCRIPT
Finland population
Salomaa–Rasenen, A.
Finland based study; 1977–1980 336 64.9 59.8-70.0 Serology over 30 38.4
(2006)101Ω
Vammala
Finland population
PT
Finland based study; 1997–1998 336 58.9 53.7-64.2 Serology over 30 38.4
(2006)101Ω
Vammala
Finland population
RI
Finland based study; 1994 224 46.0 39.5-52.5 Serology 15-59 41.5
(2006)101Ω
Vammala
SC
Three primary care
Bergenzaun, P.
Iceland centres in Sweden, 1991–1992 387 35.7 30.9-40.4 Serology 0-over 80 ~
(1996)102
Iceland
U
Thjodleifsson, B.
Iceland Reykjavik 1991–2001 447 36.2 31.8-40.7 Serology 25 -50 48.3
(2007)100
AN
Buckley, M. J. M.
Ireland Dublin 1000 43.0 39.9-46.1 Serology 18-60 60.8
(1998)103
Riga, Kurzema,
M
Leja, M. (2012)104 Latvia Zemgale, Vidzeme, 2008–2009 3564 79.2 77.9-80.5 Serology 17-99 34.0
Latgale
Municipality of
D
Asfeldt, A. M. (2008)105 Norway 2004 916 38.0 34.9-41.1 Histology 18-85 44.8
Sørreisa
The city of Bodø (the
TE
Bodø Helicobacter
Study) and the
Breckan, R. K. municipality of
Norway 2004–2005 1736 21.2 19.3-23.1 Stool antigen "Adults" 44.7
(2009)106 Sørreisa (the
EP
Sørreisa Gastro–
intestinal Disorder
Study).
Breckan, R. K.
C
Norway Bodo and Sorreisa ~ 1416 32.9 30.5-35.4 Stool antigen "Adults" 54.6
(2012)107
AC
Three primary care

Bergenzaun, P.
Sweden centres in Sweden, 1991–1992 443 35.7 21.9-30.0 Serology 10-over 69 35.2
(1996)102
Iceland
Municipality of
Borch, K. (2000)108 Sweden ~ 482 44.8 40.4-49.3 Histology 35-85 54.4
Linköping
Sorberg, M. (2003)109 Sweden 25 Cities in Sweden 1995 3502 17.7 16.4-19.0 Serology 17-over 80 62.6
109
Sorberg, M. (2003) Sweden Stockholm 1995 1087 24.0 21.5-26.6 Serology 17-over 80 38.5
ACCEPTED MANUSCRIPT
Aro, P. (2004)110 Sweden Kalix and Haparanda 1998 989 34.3 31.3-37.2 Histology 18-80 ~
Thjodleifsson, B.
Sweden Uppsala 1991–2001 359 11.1 7.9-14.4 Serology 25-50 52.1
(2007)100
PT
Mendall, M. A.
UK London ~ 215 32.6 26.3-38.8 Serology, histology 18-82 ~
(1992)111
Murray, L. J. (1997)112 UK Northern Ireland 1986–1987 4742 50.5 49.1-51.9 Serology 12-64 ~
RI
McDonagh, T. A.
UK North Glasgow 1992 1428 65.9 63.4-68.4 Serology 25-74 49.2
(1997)113
Stone, M. A. (1998)114 UK Leicestershire ~ 1566 15.0 13.2-16.8 Serology 21-55 44.7
SC
Public Health
1986 and
Vyse, A. J. (2002)115 UK Laboratories in 7147 13.4 12.6-14.2 Serology 1-84 69.2
1996
England and Wales
U
Southern Europe (=21)
Katsanos, K. H.
AN
Albania 2005–2008 101 53.5 43.7-63.2 Histology <20 >50 59.4
(2010)116Ω∞
117
Babus, V. (1997) Croatia ~ 3082 60.4 58.7-62.1 Serology 20-70 ~
The communities of
M
Marija Bistrica, Zlatar
Bistrica, Valpovo and 25-34, 55-
Babus, V. (1998)118 Croatia ~ 456 50.9 46.3-55.5 Serology 22.4
Donji Miholjac, The 64
D
Zadar and Sibenik
communities
Marusic, M. (2013)119 Croatia Zagreb 2008–2011 3000 46.7 44.9-48.5 UBT 14-93 ~
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120 All over Greece,
Pateraki, E. (1990) Greece ~ 1069 64.0 61.1-66.9 Serology 1-50 ~
Athens
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Apostolopoulos, P.
Greece Athens 1997 201 49.3 42.3-56.2 Serology 16-85 ~
(2002)121
Apostolopoulos, P.
Greece Athens 1987 200 59.5 52.7-66.3 Serology 15-82 ~
(2002)121
C
Katsanos, K. H.
Greece 2005–2008 101 33.7 24.5-42.9 Histology <20 >50 59.4
(2010)116Ω∞
AC
Central and Northern

Italy, Genoa in
Palli, D. (1993)122 Italy 1985–1988 930 45.1 41.9-48.3 Serology 35-74 58.1
Northern Italy,
Cagliaro in Sardinia
Luzza, F. (1997)123 Italy Cirò 1995 705 63.3 59.7-66.8 Serology 1-87 38.7
Campogalliano, a
Dominici, P. (1999)124 Italy ~ 3289 59.7 58.0-61.4 Serology 12-65 ~
town in northern Italy
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with about 5000

residents.
Russo, A. (1999)125 Italy 1995–1997 2598 44.7 42.8-46.6 Serology 25-60 ~

126 Loiano and Mong–
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Bazzoli, F. (2001) Italy 1996 1533 67.9 65.6-70.2 UBT 28-80 51.7
Hidoro
Bastos, J. (2013)127 Portugal Porto 1999–2003 2067 86.4 84.9-87.9 Serology 18-92 ~
Nine districts in the
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Gasbarrini, G.
San Marino Republic of San 1990–1991 2237 51.0 48.9-53.1 Serology 20->70 46.8
(1995)128
Marino
Pretolani, S. (1997)129 San Marino 1990 1528 43.9 41.4-46.3 Serology 20-85 ~
SC
Martin–de–Argila, C.
Spain ~ 381 53.0 48.0-58.0 Serology 5-77 36.2
(1996)130
U
Rodrigo Sáez, L.
Spain Asturias 1995–1996 480 49.2 44.7-53.6 Serology up to 80 ~
(1997)131
AN
Senra–Varela, A. Ubrique and
Spain 1997 332 43.4 38.0-48.7 Serology 18-over 60 49.1
(1998)132 Grazalema, Barbate
Ràfols Crestani, A.
Spain Girona ~ 397 56.2 51.3-61.1 UBT 14-80 43.6
(2000)133
M
Baena Diez, J. M.
Spain Barcelona 1999–2001 267 52.4 46.4-58.4 Serology 1-69 ~
(2002)134
D
Macenlle Garcia, R.
Spain Province of Ourense 1998 383 69.2 64.6-73.8 UBT 18-over 84 51.2
(2006)135
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Sanchez Ceballos, F.
Spain Madrid 2004–2006 481 60.3 55.9-64.7 UBT 4-82 36.4
(2007)136
Western Europe (n=16)

EP
137
Tomasi, J. P. (1990) Belgium All over Belgium ~ 4053 42.3 40.8-43.8 Serology <20 >80 45.7
138
Blecker, U. (1995) Belgium Brussels ~ 1180 18.0 15.8-20.2 Serology 1-40 ~
C
Miendje Deyi, V. Y.
Belgium Brussels 1988–2007 22612 37.7 37.1-38.3 Culture 0-100 ~
(2011)139
Le Bodic, M. F.
AC
France Nantes ~ 64 46.9 34.7-59.1 Histology, culture ~ ~

(1987)140
Holtmann, G. (1994)141 Germany Essen ~ 180 31.7 24.9-38.5 HP Serology, CLO 20-over 50 58.9
142
Brenner, H. (1997) Germany Blaustein 1996 447 21.0 17.3-24.8 UBT 15-79 33.3
Rothenbacher, D.
Germany Ulm 1996 501 23.4 19.7-27.1 UBT 15-79 37.5
(1997)143
144
Brenner, H. (1999) Germany West Germany 1987–1988 1785 39.2 37.0-41.5 Serology 18-88 44.1
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Seher, C. (2000)145 Germany 1997–1998 6748 40.0 38.8-41.2 Serology 18-79 39.4
146
Holtmann, G. (2001) Germany Essen ~ 491 39.5 35.2-43.8 Serology 18-65 59.1
Kuepper–Nybelen, J. East and West
Germany 1997–1999 6545 40.7 39.5-41.9 Serology 18-79 ~
(2005)147 Germany
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Wex, T. (2011)148 Germany Saxony–Anhalt 2009–2010 2318 44.4 42.4-46.4 Serology 0-90 50.9
Loffeld, R. J. L. F.
Netherlands Zaanstreek region 1993–2000 8190 39.1 38.0-40.1 Histology 4-99 48.5
(2003)149
RI
Loffeld, R. J. (2003)150 Netherlands 402 35.6 30.9-40.3 Serology 19-65 ~
Rotterdam,
SC
van Blankenstein, M. Nijmegen, West,
Netherlands 2005 1551 31.7 29.4-34.0 Serology 17-80 ~
(2013)151 South, Zeeland,
Limburg
Lehmann, F. S.
Switzerland Bern ~ 175 18.9 13.1-24.7 Histology, CLO, UBT 18-81 58.9
(2000)152
U
Caribbean (n=2)
AN
Carter, F. P. (2011)153 Bahamas 2009 204 57.8 51.1-64.6 Serology 16-61 57.4
154 France
Weill, F. X. (2002) Main Islands 2000 764 55.2 51.7-58.8 Serology 18-70 45.9
(Guadeloupe)
France
M
Weill, F. X. (2002)154 Dependencies 2000 90 41.1 31.0-51.3 Serology 18-70 66.7
(Guadeloupe)
Central America
(n=3)
D
Torres, J. (1998)155 Mexico All 32 states 1987–1988 11605 66.5 65.7-67.4 Serology 1- 90 ~
Cardenas, V. M.
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Mexico Ciudad Juarez 2004 215 38.1 31.7-44.6 Stool antigen ≥0 ~
(2010)156
157
Sasaki, T. (2009) Panama El Pantano 2007 74 54.1 42.7-65.4 Stool antigen 21-82 62.2
South America (n=9)
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Olmos, J. A. (2000)158 Argentina 1996 493 49.1 44.7-53.5 Serology 18-80 36.1
De Oliveira, A. M. R.
Brazil Minas Gerais ~ 131 87.0 81.3-92.8 Serology 20-78 12.2
C
(1999)159
Nascimento, R. S. Urban of Uberlândia,
AC
Brazil 1997–1999 100 68.0 58.9-77.1 Serology ≥ 21 ~

(2002)160 Minas Gerais
Nascimento, R. S. Rural of Uberlândia,
Brazil 1997–2000 79 76.0 66.5-85.4 Serology ≥ 21 ~
(2002)160 Minas Gerais
Lyra, A. C. (2003)161 Brazil Salvador 1997–1999 274 68.3 62.7-73.8 Serology ~ 80.3
162
Santos, I. S. (2005) Brazil Pelotas ~ 359 64.4 59.4-69.3 UBT ≥ 20 ~
Zaterka, S. (2007)163 Brazil Sao Paolo ~ 993 65.7 62.7-68.6 Serology ~ 75.1
Santos, I. S. (2009)164 Brazil Pelotas 2006–2007 1001 70.7 67.9-73.6 UBT 18-45 ~
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Ferreccio, C. (2007)165 Chile 2003 2615 74.6 72.9-76.2 Serology ≥ 17 47.9

166
Sasaki, T. (2009) Ecuador 2007 90 72.2 63.0-81.5 Stool antigen ~ ~
Northern America (n=13)
Veldhuyzen Van
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Zanten, S. J. O. Canada Nova Scotia ~ 316 38.0 32.6-43.3 Serology 18-72 40.8
(1994)167
Milman N. (2003)168 Greenland Nuuk, Ilulissat 1993–1994 71 46.5 34.9-58.1 Serology 22-76 40.8
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Sisimiut community,
Koch, A. (2005)169 Greenland 1996–1998 685 40.9 37.2-44.6 Serology 5-87 47.0
West Greenland
SC
Fitzgibbons, P. L. United States
Los Angeles ~ 116 31.0 22.6-39.5 Histology 19-91 50.0
(1988)170 of America
United States
Dooley, C. P. (1989)171 ~ 113 31.9 20.8-37.6 Histology, Serology 18-91 46.0
U
of America
United States
Correa, P. (1990)172 New Orleans ~ 275 56.4 50.5-62.2 Serology 18-84 ~
AN
of America
Graham, D. Y. United States
Houston 1988–1990 485 52.2 47.7-56.6 Serology, UBT 15-80 47.6
Everhart, J. E. United States
1988–1991 7465 32.5 31.4-33.6 Serology ≥ 20 50.2
(2000)174
M
of America
Cardenas, V. M. United States
1999–2000 7462 27.1 26.1-28.1 Serology 3-70 ~
(2006)175Ω∞ of America
D
Cardenas, V. M. United States
El Paso Texas 2004 73 38.4 27.2-49.5 Stool antigen ≥0 ~
TE
United States
Patterson, T. (2012)176 Texas 2011 246 18.7 13.8-23.6 Serology ≥ 21 ~
of America
Parkinson, A. J. United States
Alaska 1980–1986 2080 74.8 72.9-76.7 Serology ≥0 50.0
United States
EP
178
Melius, E. J. (2013) Northern Plains ~ 166 52.4 44.8-60.0 UBT 5-88 48.8
of America
Oceania (n=6)
179
Collett, J. A. (1999) New Zealand Christchurch 1996 1060 24.0 21.4-26.5 Serology > 18 41.9
C
180
Peach, H. G. (1997) Australia Ballarat 1994–1995 217 30.4 24.3-36.5 Serology Adults ~
AC
Robertson, M. S.
Australia Victoria ~ 500 32.0 27.9-36.1 Serology 16-71 55.0
(2003)181
Moujaber, T. (2008)182 Australia 2002 2413 15.1 13.7-16.6 Serology 1-59 49.9
Pandeya, N. (2011)183 Australia 2002–2005 1355 22.3 20.1-24.5 Serology 18-79 ~
Windsor, H. M. Jigalong, Parnngurr,
Australia 2003–2004 520 76.0 72.3-79.6 UBT 2-90 43.3
(2005)184 Perth, Punmu
~ Information not available in primary source article
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Ω Age adjusted prevalence

∞ Gender adjusted prevalence
UBT: Urea Breath Test
RUT: Rapid Urease Test
CLO: Campylobacter like organism test
PT
RI
U SC
AN
M
D
TE
EP
C
AC
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HP diagnostic HP Prevalence 95% Confidence I-squared (%) P value

methods used (%) Interval
Serology 54.4 50.3-58.5 99.8 0.00
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Urea Breath Test 62.9 55.5-70.3 99.7 0.00
Stool Antigen 49.4 35.7-63.1 99.2 0.00
CLO, histology 51.4 46.0-56.8 97.1 0.00
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Serology, UBT 54.6 35.6-73.6 99.6 0.00
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Time trends in HP prevalence in UN African region

Country Prevalence Estimates 95% CI # of reporting studies # of subjects*
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1970–1999 2000–2016 1970–1999 2000–2016 1970–1999 2000–2016 1970–1999 2000–2016
Benin – 74.1 – 70.0–78.1 – 2 – 446
Nigeria 85.1 – 80.8–89.3 – 1 – 268 –
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South Africa – 86.8 – 83.3–90.3 – 1 – 356
Tunisia – 72.8 – 53.7–91.9 – 2 – 348
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UN Africa – 76.2 – 67.3–85.0 – 5 – 1 150
* Number of individuals included in analysis
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Time trends in HP prevalence in UN Asian region
1970–1999 2000–2016 1970–1999 2000–2016 1970–1999 2000–2016 1970–1999 2000–2016
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Eastern Asia 55.6 53.2 50.6–60.5 48.7–57.7 30 42 30978 242 245
China 60.5 52.2 53.0–68.0 48.1–56.4 11 14 13 753 88 577
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Taiwan 54.4 53.7 51.0–57.8 25.3-82.1 1 2 823 1 413
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Japan 55.5 46.5 44.9–66.2 36.5–56.4 8 6 8 308 38 856
Korea 50.2 55.8 45.5–54.9 51.3–60.3 10 20 8 094 113 399
+
Southern Asia – – – – – – – –
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Iran – 59.0 – 51.5–66.5 – 8 – 5 256
+
South–Eastern Asia – – – – – – – –
Malaysia 4.7 14.2 3.6–5.8 13.2–15.1 1 1 1 417 5 370
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Singapore 40.8 – 37.7–43.9 – 2 – 953 –

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+
Western Asia – – – – – – – –
Turkey 70.1 80.1 64.7–75.4 75.0-85.2 1 2 284 5 752
UN Asia 53.6 54.3 45.5–61.7 49.7–59.0 34 53 33 632 156 563
+ Insufficient data for pooled analysis

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Time trends in HP prevalence in UN European region

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1970–1999 2000–2016 1970–1999 2000–2016 1970–1999 2000–2016 1970–1999 2000–2016
Eastern Europe 66.1 41.2 52.3–80.0 20.4–61.9 2 3 965 10 900
Czech Republic 58.9 36.6 53.4–64.4 14.8–50.4 1 2 309 4 335
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Poland 73.0 58.3 69.6–76.4 57.1–59.5 1 1 656 6 565
Northern Europe 47.2 35.0 31.0–63.3 20.5–49.5 13 5 22 579 3 698
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Estonia 87.9 69.2 85.7–90.2 75.1–90.0 2 1 1 958 240
Finland 56.8 – 46.5–67.0 – 3 – 896 –
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Iceland 35.7 36.2 30.9–40.4 31.8–40.7 1 1 387 447
Norway – 29.5 – 13.1–46.0 – 2 – 2 652
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Sweden 25.4 11.1 17.8-33.0 7.9–14.4 4 1 6 021 359
UK 43.3 – 11.1-75.4 – 2 – 4 293 –
Southern Europe 53.3 49.4 47.2–59.3 36.2–62.6 11 3 11 127 849
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Greece 54.4 33.7 44.4–64.4 24.5–42.9 2 1 401 101
Italy 55.2 – 42.5–68.0 – 4 – 3 067 –
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San Marino 47.5 – 40.5–54.5 – 2 – 3 765
Spain 53.9 56.6 38.7-69.2 49.0–64.3 3 2 1 195 748
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Western Europe 27.9 38.8 15.4–40.5 36.4–41.3 5 4 15 626 12 461
Germany 33.1 44.4 27.8–38.6 42.4–46.4 5 1 15 626 2 318
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Netherlands – 35.5 – 30.1–41.0 – 3 – 10 143
UN Europe 48.2 39.7 40.3–56.2 32.5–46.9 31 15 50 297 27 908
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Time trends in HP prevalence in UN Latin American and the Caribbean region

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1970–1999 2000–2016 1970–1999 2000–2016 1970–1999 2000–2016 1970–1999 2000–2016
Bahamas – 57.8 – 51.1–64.6 – 1 – 204
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Guadeloupe – 49.0 – 35.3–62.8 – 1 – 854
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Mexico 66.5 38.1 65.7–67.4 31.7–44.6 1 1 11 605 215
Panama – 54.1 – 59.2–67.6 – 1 – 74
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Argentina 49.1 – 44.7–53.5 – 1 – 493 –
Brazil 68.2 71.3 63.5–72.9 68.1-74.6 2 2 374 1 080
Chile – 74.6 – 72.9–76.2 – 1 – 2 615
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Ecuador – 72.2 – 63.0–81.5 – 1 – 90
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UN Latin America and
62.8 60.2 53.6–71.9 52.0–68.4 4 9 12 472 5 132
Caribbean
^
Insular region of France located in the Caribbean
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Time trends in HP prevalence in UN Northern America region
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Greenland 41.4 – 37.9–44.9 – 2 – 756 –
United States of America 42.2 26.6 22.9–61.5 19.0–34.1 2 3 7 950 7 781
UN Northern America 42.7 26.6 32.7–52.6 19.0–34.1 4 3 8 706 7 781
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Time trends in HP prevalence in UN Oceania region

1970–1999 2000–2016 1970–1999 2000–2016 1970–1999 2000–2016 1970–1999 2000–2016
New Zealand 24.0 – 18.5–30.4 – 1 – 1 060 –
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Australia 30.4 18.7 24.3–36.5 11.6–25.7 1 2 217 3 768
UN Oceania 26.6 18.7 20.4–32.8 11.6–25.7 2 2 1 277 3 768
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Supplementary Material: (see separate file)

Appendix 1: MEDLINE and EMBASE search strategy for article selection (from 1 Jan 1970 to 1
Jan 2016)
Appendix 3: Distribution of included papers by regions and countries
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Appendix 4: Country and region specific prevalence of HP since 1 Jan 1970 to 1 Jan 2016 in
Northern America, Southern America, Oceania, Eastern Asia, Southern Asia, Western Asia,
Northern Europe, Southern Europe, Western Europe and Northern Africa
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Global Prevalence of Helicobacter pylori Infection: Systematic Review and Meta-

To appear in: Gastroenterology

Title: Global Prevalence of Helicobacter pylori Infection: Systematic Review and

Short title: Helicobacter pylori global prevalence

E. Underwood3, Divine Tanyingoh3, Peter Malfertheiner4, David Y. Graham5, Vincent W.S.

Laboratory of Digestive Diseases, LKS Institute of Health Science, Chinese University of

Hong Kong, Hong Kong, China

2. Department of Gastroenterology and Hepatology, Tan Tock Seng Hospital, Singapore.

3. Departments of Medicine and Community Health Sciences, University of Calgary, Calgary,

4. Department of Gastroenterology, Hepatology and Infectious Diseases, Otto-von-Guericke

University of Magdeburg, Magdeburg, Germany

5. Gastroenterology, Baylor College of Medicine, Houston, Texas, United States

Grant Support: Nil

Abbreviations: HP (Helicobacter pylori)

Siew C Ng, MBBS, MRCP, PhD

Department of Medicine and Therapeutics

Chinese University of Hong Kong, Hong Kong

Tel: 852 2632 1420

Fax: 852 2637 3852

Gilaad G. Kaplan, MD, MPH, FRCPC

Teaching Research and Wellness Center

Tel: 1 403 592 5015

Writing Assistance: Nil

integrity of the data and the accuracy of the data analysis.

the initial systematic search.

Conflict of Interest Statements

We declare no competing interests.

Manuscript word count: 5798

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.

individual countries. We used a random effects model to calculate pooled prevalence

to obtain the estimated number of individuals with H pylori infection.

Switzerland (95% CI 13.1–24.7) to 87.7% in Nigeria (95% CI 83.1–92.2). Based on regional

Conclusions: In a systematic review and meta-analysis to assess the prevalence of H pylori

strategies for the global eradication.

Keywords: bacteria, incidence, Europe, stomach

Word Count = 266

Background and context:

prevalence is decreasing in developed countries and in some developing countries. We also

highlighted the areas with the highest HP burden.

country’s true prevalence.

reduce the sequalae associated with infection by HP.

Helicobacter pylori (HP) is a gram-negative microaerophilic bacterium that infects the

reported until now.

Recent interest has focused on HP eradication as a strategy of eliminating gastric cancer.

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

strategies for allocating healthcare resources. We pooled HP prevalence estimates in

efforts to better manage the burden of this disease.

MATERIALS AND METHODS

Literature Search and Study Selection

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

the Cochrane Collaboration-endorsed Newcastle-Ottawa Quality Assessment Scale (NOS),10

which was designed to assess aspects of population-based studies of prevalence. The

quality assessment of each paper is shown in Appendix 2.

stratified analyses were conducted to address sources of heterogeneity: (a) geographic

histopathology, and serology or urea breath test.

Natural Earth Community.14