Prevalence and risk factors of helicobacter pylori in Turkey: a nationally-representative, cross-sectional, screening with the 13C-Urea breath test
© Ozaydin et al.; licensee BioMed Central Ltd. 2013
Received: 31 July 2013
Accepted: 13 December 2013
Published: 21 December 2013
Helicobacter pylori is an important global pathogen infecting approximately 50% of the world’s population. This study was undertaken in order to estimate the prevalence rate of Helicobacter pylori infections among adults living in Turkey and to investigate the associated risk factors.
This study was a nationally representative cross sectional survey, using weighted multistage stratified cluster sampling. All individuals aged ≥18 years in the selected households were invited to participate in the survey. Ninety two percent (n = 2382) of the households in 55 cities participated; 4622 individuals from these households were tested with the 13C-Urea breath test. Helicobacter pylori prevalence and associated factors were analysed by the t test, chi square and multiple logistic regression with SPSS11.0.
The weighted overall prevalence was 82.5% (95% CI: 81.0-84.2) and was higher in men. It was lowest in the South which has the major fruit growing areas of the country. The factors included in the final model were sex, age, education, marital status, type of insurance (social security), residential region, alcohol use, smoking, drinking water source. While education was the only significant factor for women, residential region, housing tenure, smoking and alcohol use were significant for men in models by sex.
In Turkey, Helicobacter pylori prevalence was found to be very high. Individuals who were women, elderly adults, single, had a high educational level, were living in the fruit growing region, had social security from Emekli Sandigi, were drinking bottled water, non smokers and regular alcohol consumers, were under less risk of Helicobacter pylori infection than others.
KeywordsHelicobacter pylori prevalence Risk factors of helicobacter pylori infection Smoking Alcohol use
Helicobacter pylori was first discovered in 1983, and eleven years later in 1994 the International Agency for Research on Cancers (IARC) classified H.pylori as a definite class 1 carcinogen [1, 2]. It is a small, spiral, gram-negative bacillus which inhabits the mucus layer overlying the gastric epithelial cells in humans. It produces a potent urease. The isolation of H.pylori from the human gastric mucosa and the demonstration of its involvement in gastritis, peptic ulcer disease and gastric cancers have radically changed our perception of these diseases. Development of atrophy and metaplasia of the gastric mucosa are strongly associated with H.pylori infection [2–5].
The greatest risk for infection appears to be during childhood and early adult years . Although infected individuals often have histological evidence of gastritis, the vast majority of infections are asymptomatic . Current evidence indicates that disparate disease outcomes are not related solely to the genetic diversity of H.pylori, but also to host factors and environmental agents . Further delineation of the host response to infection, to specific environmental exposures or to bacterial virulence factors is required to identify which patients infected with H.pylori are at greatest risk of developing disease. Identifying and understanding such interactions should promote the development of optimal outcomes.
H.pylori is a public health problem in both developed and developing countries . The IARC has stressed that the need for effective, population based screening programs is essential for tackling cancer .
Most previous studies have been carried out in clinical settings on small samples. There is limited evidence concerning the prevalence, determinants and mode of infection in representative population samples. This is the first population based study of a country-wide representative sample with a high response rate using the most sensitive and specific test the 13Carbon Urea Breath Test (13C-UBT) to have been carried out in Turkey. The aim of this survey was to estimate the prevalence rate of H.pylori infection among adults aged ≥18 years and to investigate the factors associated with an H.pylori infection in Turkey.
A study of the prevalence and risk factors of H.pylori infection in Turkey (TURHEP) was a nationally representative, population based cross-sectional screening with the 13C-Urea Breath Test. A weighted, multistage, stratified cluster sampling approach was used in the selection of the sample. For this study, 100 different residential areas were selected as clusters for an optimal distribution with a target sample size of 2500 selected households based on the results of the General Population Count of Turkey held in 2000 (Additional file 1: Figure S1). Households which were to be visited in each cluster were selected randomly by the Turkish Statistical Institute.
Breath sample collection
At the first visit, eligible and willing people were informed about a required minimal six-hour period of fasting. At the second visit, after ensuring that they had fasted, two breath samples were collected as first samples. The test solution, 75 mg 13C-urea in 30 ml drinkable water (Helicobacter Test INFAI, Germany), was given after 200 ml of standard orange juice had been drunk. Thirty minutes later two breath samples were taken. Samples were measured by isotope ratio mass spectrometry (IRMS) in Istanbul between August 2003 and February 2004.
The test results were evaluated as H.pylori-negative when the 13C difference between 0th minute sample and 30th minute sample was lower than 4.00 and as H.pylori-positive when it was equal to or higher than 4.00.
The study protocol was reviewed and approved by the Research Ethics Committee of the School of Medicine of Marmara University. All participants signed a written informed consent.
IRMS measurements were performed in the University and a trained technician employed by Marmara Health Education and Research Foundation measured the samples during the period of the study.
The primary outcome variable, the results of the H.Pylori UBT were categorized as positive or negative. Demographic variables (age, sex, residential region, geographic region, marital status, education), economic status (occupation, social security status 1a(Emekli Sandigi, SSK, BAG-KUR, Green Card, private insurance, foreign insurance or none), housing tenure, environmental condition (number in household, bedrooms, source of drinking water, type of toilet system, source of heating) in or out of the home as well as cigarette and alcohol consumption were considered in the analysis.
The geographic regions defined five major regions of the country (West, South, Central, North and East) (Additional file 1: Figure S1).
All analyses incorporated sampling weights that were adjusted for the complex study design of TURHEP.
The characteristics of H.pylori-positive and H.pylori-negative participants were compared using the chi-square test for categorical variables and the two sample t-test for continuous variables.
Odds ratios (OR) and 95% confidence intervals (CI) for the association between H.Pylori infection and each potential risk factor were estimated using multivariable logistic regression models. The covariates included in the models were those significantly associated with H.Pylori in the univariate analyses (p < 0.05). The group presenting the lowest infection risk was chosen as the indicator. The final model was developed using a stepwise procedure with backward elimination, with inclusion and exclusion criteria set at the significance level of 0.05 and 0.10 respectively. The multiple logistic regression model fit was determined by the Hosmer-Lemeshow test statistic. A model fits the data if the Hosmer-Lemeshow statistic has a p > 0.05. Significant predictors were identified and ORs calculated with 95% CIs. The following variables were considered in the model: sex, age, region (West, South, Central, North, East), residence (urban, rural), marital status (never married, currently married, widowed/divorced), education level (no education, primary complete, secondary complete, high school +), type of insurance (Emekli Sandigi, private/foreign, BAG KUR, SSK, none, green-card), occupation (employed/unemployed) housing-tenure (owned by a household-member, lodging/no-rent paid), household population per bedroom, source of drinking-water (bottled-water, piped-water, public-fountain, others:‘river/rain-water/etc.’, smoking (never, current-nonsmoker, current-occasional-smoker, regular-smoker) and alcohol consumption (regular drinker, current occasional-drinker, current non-drinker, never).
Results of the household, individual interviews and breathe samples
Household Response Rate (%)
Eligible individual interviewed
Eligible Individual Response Rate (%)
Number of people who had gastrectomy
Number of the people who had antibiotic treatment during the last 30 days
Number of people who used PPI during the last 14 days
Eligible people for test
Eligible people tested
Eligible people tested rate (%)
Among 5555 eligible individuals in households, 5549 were successfully interviewed (99.9%). The total number of eligible people for breath test was 4973 and of these 4663 breath samples were collected (93.7%). Three hundred and seventy two individuals who had used antibiotic therapy for any reason during the last 30 days, 242 individuals who had used proton- pump inhibitors during the last 14 days and 1 person who had had a gastrectomy were excluded. The main reason for failure to collect breath samples from the eligible people was that they could not stand the 6-hour fast or were unwilling to undertake the 6-hour fast. Also, a number of eligible individuals were obliged to be outside or working after 6 hrs and a few people did not agree to give breath samples although they gave no reason.
Of the 4663 breath samples, 4622 were measured (99.1%). Forty one breath-samples could not be measured for technical reasons (Table 1).
The basic socio-demographic characteristics and H. pylori infection
Socio-demographic factors associated with Helicobacter pylori infection
Adjusted odds ratios for Helicobacter pylori positivity for various risk factors in final model
Variable and categories
High school +
Source of drinking water
Bottled water/demijohn/pet water
Piped water (in house/garden/outside)
Other (river. rain water etc.)
Tried at past. currently non-smoker
Tried at past. currently occasional smoker
Tried at past. currently drinking occasionally
Tried at past. currently non-drinker
Socio-economic status and H.pylori infection
Socio-economic factors associated with Helicobacter pylori infection
Education (n = 4577)
High school +
Social security** (n = 4573)
Housing tenure (n = 4597)
Owned by a household member
Lodging/no money paid
Occupation (n = 4503)
Agriculture & animal husbandry
6 + person/home
Rooms for sleeping (n = 4575)
Source of the drinking water (n = 4594)
Piped water (in house/garden/outside)
Bottled water/demijohn/pet water
Other ((river, rain water etc.))
Type of toilet system (n = 4598)
Connected to drainage system
Other (No facility)
Source of heating (n = 4553)
Radiator (Central heating)
Natural gas stove
Family income (USD/month)*** (n = 4194)
Adjusted odds ratios for Helicobacter pylori positivity for various risk factors by sex
High school +
Owned by household members
Lodging/no money paid
Source of Drinking Water
Other (river. rain water etc.)
Tried at past. currently non-smoker
Tried at past. currently occasional smoker
Tried at past. currently drinking occasionally
Tried at past. currently non-drinker
Social security status was the only socio-economic status indicator in the final models. Those who had SSK and no social security were at greater risk than those who had insurance of Emekli Sandigi (Table 3).
The source of drinking water was a significant factor in the final models. The people who used piped water, spring/public fountain and other (river, rain water etc.) were at greater risk than those who used bottled water/demijohn/PET bottled water as drinking water (Table 3).
Housing was a significant factor only in the men’s model. Men lodging/or paying no money for their housing were at more risk than those who lived in a house owned by a household member (Table 5).
Lifestyle factors and prevalence of H.pylori infection
Lifestyle factors associated with Helicobacter pylori infection
Smoking cigarettes (n = 4605)
Tried at past, currently non-smoker
Tried at past, currently occasional smoker
Drinking alcohol (n = 4593)
Analysis of factors and H.pylori infection by sex
Since sex was a significant factor for H.pylori infection it was necessary to analyze factors separately for each sex. In men, age, marital status, social security status, housing tenure, type of drinking water, smoking, alcohol use and geographic region were factors. However, for women, age, marital status, social security status, type of drinking water and education were factors (Table 5).
So far as we know this study is the most representative one that is based on a sample derived from the population of one country, estimating the factors associated with the prevalence of Helicobacter pylori infection and using the 13C-UBT. Furthermore, the response rates were very high. In this study, it was produced highly significant estimates [Design effect (DEFT) = 2.01 and standard error = 0.008].
Awareness of Helicobacter pylori is little more than a decade old. Yet there have been many studies all over the world about its epidemiology. Most prevalence data have used random sampling of blood donors, clinic attendees or industrial employees; none of these groups provides a truly normal population as emphasised by Pounder .
Studies that have used labelled breath tests in a normal population to detect Helicobacter pylori infection are very rare. However, they are highly sensitive, specific and are also recommended by the Maastricht 2–2000 Consensus Report and by the Canadian Helicobacter Study Group Consensus conference, 2004 [7, 13, 14].
When comparing the rates from previous studies directly with our study, it should be kept in mind that other studies also differ from ours in terms of variation by age, type of population, type of diagnostic test and study time at which the study was done.
In TURHEP, the weighted overall prevalence of Helicobacter pylori infection was 82.5% (95% CI 81.0-84.2) with 13C-UBT. Helicobacter pylori prevalence has been reported to reach 70% or more in developing countries and to be less than 40% in developed countries [15–37].
There was an inverse association between age and infection in our study. Earlier studies have shown differing trends regarding age and Helicobacter pylori prevalence. Whereas Helicobacter pylori prevalence increased with age at earlier ages, there was a slight decrease in populations over 60 years of age in France and over 50 years in the other countries (Vietnam, Algeria and Ivory Coast) . Infection increased up to the 40–49 age group, then decreased in analyses for Southern Brazil and Northern India [17, 30]. Also, the prevalence peaked at ages 45 to 64 and dropped after the age 65 in Chile and the Czech Republic [31, 37]. In Ankara (Turkey), seroprevalence was 58.4% for ages 15–19, 62.6% for ages 20–29, 67.6% for ages 30–39, 81.3% for ages 40–49 and 66.3% for over 50 years . In India also the prevalence was increasing to 100% by 60 then decreasing to 80% by 70 years (n = 238, ages 3–70) and in Athens, whereas the seroprevalence was increasing from 14.2% for ages 15–24 to 67.4% for ages 55–64, it decreased to 57.9% for ages >65 [18, 32]. Only in Beninese populations, in 2005 (n = 446, over 2 years old) no association was found between seroprevalence and age . In contrast, some studies claimed that Helicobacter pylori prevalence increased with age [15, 16, 19, 21, 24–26, 29, 33–35, 39–43].
We found that men in Turkey were at greater risk than women for Helicobacter pylori infection. Likewise, in Northern California, men had a higher prevalence of antibodies across all strata of race/ethnicity, age, education and income (OR = 2.0, 95% CI 1.2-3.1) . Also, in Northern Ireland, infection was more common in males (60.9%) than females (55.2%, p < 0.01, Or for males versus females was 1.19 (95% CI 1.02-1.40) . In Leeds (UK), Spain and Chile, it was higher in men [31, 36, 44]. Conversely, in some studies, which mostly had small samples, there was no difference found in Helicobacter pylori prevalence between the sexes [15–18, 21, 22, 24–26, 28, 29, 34, 37–39],. To our knowledge, only one study from Israel found that the relative risk of Helicobacter pylori infection was increased in women smokers . We agree with Moayyedi-et-al. that the positive association of Helicobacter pylori with the male sex should probably not be interpreted as a direct causal relationship . The reason for the possible gender difference is unclear but may relate to young boys having poorer hygiene than young girls. Because of social gender roles in Turkey, men seek less healthy facilities for toilet needs than women, and men are outdoors more than women, which brings more risks of infection. Further, men tend to participate in more of the risky behaviours such as smoking, alcohol drinking than women.
The current residential region was found to be a risk factor for H.pylori infection. In Turkey, the western areas are more developed, more crowded, better educated, and have better housing conditions; families are smaller than in the East. The reason why H.pylori infections are lowest in individuals living in the South must be related to this being a major area for growing citrus fruits. These contain high levels of Vitamin C. People in the South can eat oranges, lemons, tangerines or bitter oranges frequently and continuously or drink the juices because citrus fruits are cheap and plentiful all the year round. It is known that Vitamin C is effective in the prevention of most infections. Also H.pylori can be expected not to survive in acidic gastric conditions produced by the acidic citrus fruits. Moreover, for regular smokers the highest H.pylori prevalence may result from an interaction between tobacco and Vitamin C. In contrast, the highest H.pylori infections were found in subjects living in eastern Turkey, which has the least available citrus fruits; they cannot be grown, and snow prevents their transport for several months each year; Besides, this region is the least developed. Although in TURHEP, dietary habits and daily consumptions were not included, supportive studies are available [45–48]. Additionally, garlic is frequently used in southern Turkey. One study presented garlic as a possible protective factor for gastric lesions with H.pylori infection .
Some studies with small sample sizes comparing the regions are available from Turkey. H.pylori infection was found to be 73.8% in the West, 48%-81% in the Central, 60%-85.4% in the Eastern parts of the country [38, 39, 49–51].
In most of studies it was found that H.pylori infections were inversely related to level of education [16, 22, 24, 34, 37, 42, 43]. Likewise in TURHEP, the lower the education of the subjects, especially for females, the higher the risk for H.pylori infection. However, two other studies found no association [19, 28].
The status of social security was a significant factor in the TURHEP study’s final model and in the models by sex. To our knowledge, this variable has not previously been used as a socio-economic status indicator in any study related with H.pylori infection. Some previous studies have presented an inverse association between H.pylori infection and family income as a socio-economic status indicator [29, 38, 42, 43, 52–54]. In TURHEP, the lower the income of the subjects, the higher the infection, but only in a univariate analysis. Some researchers have also studied the association between infection and social class/socio-economical class. In Korea in adults, the rate of infection was high and independent of socio-economic class. However, in children, it was inversely related to the socio-economic class of the child’s family . In Northern Ireland, the adjusted OR of infection in subjects from manual workers relative to those from non-manual occupations was 1.7 (95% CI: 1.47-1.98) . In Northern England, infection was more common in the lower social class groups . In Libya, 91% of a low socio-economic class was H.pylori-positive, while those of middle and high socio-economic classes showed 53% and 57% positivity respectively . In Northern India infection was not associated with socio-economic status .
Housing tenure, as another socio-economic indicator was found significant only in a model for males in TURHEP. In contrast, another study, showed no association between prevalence of H.pylori and type of housing (owned/rented).
In TURHEP, a water- H.pylori infection association was found in the final models. This association is a question about H.pylori infection being one of the water-borne contagious diseases. This association was mentioned in many studies from different parts of the world and it has been found that there is mostly a positive significant relation [1, 21, 25, 52]. On the other hand, no association was found in studies from Benin and Turkey [28, 39].
Smoking was a significant factor for H.pylori infection in TURHEP except for the female model. Similar results have been presented in some studies [19, 35–37]. However smoking was not associated with H.pylori infection in some other studies [15, 16, 21, 23, 30, 34, 43].
In TURHEP, regular alcohol consumption was found to be a protective factor except for the females model. Similar results have also been presented in some earlier studies [53–56]. In a EUROGAST Study, a univariate analysis showed that alcohol consumption was associated with a reduced prevalence of H.pylori, but this effect disappeared completely after adjustment in the multivariate analysis . No association was found between H.pylori and alcohol use in other studies [15, 21, 30, 35, 36].
In Turkey, H.pylori prevalence was found to be very high. Individuals, who were women, elderly adults, single, at high educational levels, living in southern Turkey, having social security of Emekli Sandigi, drinking bottled water, non-smokers and regular alcohol consumers, were under less risk of H.pylori infection than others.
In the TURHEP study, whereas prevalence was estimated as 82.5% (95%CI 81.0-84.2) in the adult population, age, sex, education and marital status were suggested as playing critical roles as co-factors for H.pylori infection. Social security, housing tenure and also water have dependant role. Whereas smoking, a common habit especially in men was positively associated, alcohol use, not as common as smoking, was a protective factor for H.pylori. Living in the southern region of Turkey, a citrus fruit growing area, is seen as a protective factor for H.pylori infection and was the most interesting result in TURHEP.
We have presented high quality data from normal, healthy individuals, representative of the whole country, from Turkey. The results of the TURHEP study, offer important public health implications for the prevention of H.pylori. In the future, cohort studies should be implemented to help define more significant risk factors.
aEmekli Sandigi: The pension fund for civil servants, SSK ‘Social Security Institution’ the insurance of employee, BAG-KUR: the insurance of tradesman, artists and other freelance workers, Green-Card: limited insurance of people do not have any other insurance.
Acknowledgements and funding
The research leading to these results has received funding from SANDOZ Pharmaceutical Company and Marmara Health Education and Research Foundation.
The authors thank the members of Public Health Department of the School of Medicine of Marmara University, data collectors, all participants, Prof. Dr. Sibel Kalaca for her critical review of the analysis and Prof. Ray W. Guillery for his editing of the manuscript.
- Van Duynhoven YT, Jonge R: Transmission of Helicobacter pylori: a role for food?. Bull World Health Organ. 2001, 79 (5): 455-460. PMID 11417041PubMedPubMed CentralGoogle Scholar
- Helicobacter pylori: Disease Burden. [Online].[cited2007 Mar 19];[2.screen] Available from: URL:http://www.who.int/vaccine_research/disease/soa_bacterial/en/index1.html
- Suerbaum S, Michetti P: Helicobacter pylori infection. N Engl J Med. 2002, 347 (15): 1175-1186. 10.1056/NEJMra020542. PMID 12374879View ArticlePubMedGoogle Scholar
- Parsonnet J, Friedman GD, Vandersteen DP, Chang Y, Vogelman JH, Orentreich N, Sibley RK: Helicobacter pylori infection and the risk of gastric carsinoma. N Engl J Med. 1991, 325 (16): 1127-1131. 10.1056/NEJM199110173251603. PMID 1891020View ArticlePubMedGoogle Scholar
- Forman D, Newell DG, Fullerton F, Yarnell JW, Stacey AR, Wald N, Sitas F: Association between infection with Helicobacter pylori and risk of gastric cancer: evidence from prospective investigation. BMJ. 1991, 302 (6788): 1302-1305. 10.1136/bmj.302.6788.1302. PMID 2059685View ArticlePubMedPubMed CentralGoogle Scholar
- Gersten O, Wilmoth JR: The cancer transition in Japan since 1951. Demogr Res. 2002, 7 (5): 271-306. Available from URL:http://www.demographic-research.org/volumes/Vol7/5/ View ArticleGoogle Scholar
- Jones NL, Sherman P, Fallone CA, Flook N, Smaill F: Canadian Helicobacter Study Group Consensus Conference: update on the approach to Helicobacter pylori infection in children and adolescents—an evidence-based evaluation. Can J Gastroenterol. 2005, 19 (7): 399-408. PMID 16010300View ArticlePubMedGoogle Scholar
- Brown LM: Helicobacter pylori: epidemiology and routes of transmission. Epidemiol Rev. 2000, 22 (2): 283-297. 10.1093/oxfordjournals.epirev.a018040. PMID 11218379View ArticlePubMedGoogle Scholar
- IARC. Working Group: IARC Monographs on the Evaluation of Carcinogenic Risk to Humans. Schistosomes, liver flukes and Helicobacter Pylori, Vol. 61. 1994, Lyon, France: IARC, http://monographs.iarc.fr/ENG/Monographs/vol61/volume61.pdf,Google Scholar
- Leung WK, Hung LC, Kwok CK, Leong RW, Ng DK, Sung JJ: Follow up a serial urea breath test results in patients after consumption of antibiotics for non-gastric infections. World J Gastroenterol. 2002, 4: 703-706. PMID 12174382View ArticleGoogle Scholar
- Laine L, Estrada R, Trujillo M, Knigge K, Fennerty MB: Effect of proton pump inhibitor therapy on diagnostic testing for Helicobacter pylori. Ann Intern Med. 1998, 129 (7): 547-550. 10.7326/0003-4819-129-7-199810010-00007. PMID 9758575View ArticlePubMedGoogle Scholar
- Pounder RE, Nq D: The prevalence of Helicobacter pylori infection in different countries. Aliment Pharmacol Ther. 1995, 9 (Suppl.2): 33-39. PMID 8547526PubMedGoogle Scholar
- Malfertheiner P, Megraud F, O’Morain C, Hungin APS, Jones R, Axon A, Graham DY, Tytgat G: Current concepts in the management of Helicobacter pylori infection TheMaastricht 2–2000 Consensus Report. Aliment Pharmacol Ther. 2002, 16: 167-180.View ArticlePubMedGoogle Scholar
- Bourke B, Ceponis P, Chiba N, Czinn S, Ferraro R, Fishbach L, Gold B, Hyunh H, Jacobson K, Jones NL, Koletzko S, Lebel S, Moavyedi P, Ridell R, Sherman P, van Zanten S, Beck I, Best L, Boland M, Bursey F, Chaun H, Cooper G, Craig B, Creuzenet C, Critch J, Govender K, Hassall E, Kaplan A, Keelan M, Noad G, et al: Canadian Helicobacter Study Group Consensus Conference: update on the approach to Helicobacter pylori infection in children and adolescents – an evidence based evaluation. Can J Gastroenterol. 2005, 19 (7): 399-408. Review. Erratum in:Can J Gastroenterol. 2005 Aug;19(8):478. [PMID 16010300]View ArticlePubMedGoogle Scholar
- Megraund F, Brassens-Rabbe MP, Denis F, Belbouri A, Hoa DQ: Seroepidemiology of campylobacter pylori infection in various populations. J Clin Microbiol. 1989, 27 (8): 1870-1873. PMID 2549098Google Scholar
- Al-Moagel MA, Evans DG, Abdulghani ME, Adam E, Evans E, Evans DJ, Malaty HM, Graham DY: Prevalence of Helicobacter (formerly Campylobacter) pylori infection in Saudia Arabia, and comparison of those with and without upper gastrointestinal symptoms. Am J Gastroenterol. 1990, 85: 944-8.PubMedGoogle Scholar
- Singh V, Trikha B, Nain CK, Singh K, Vaiphei K: Epidemiology of Helicobacter pylori and peptic ulcer in India. J Gastroenterol Hepatol. 2002, 17 (6): 659-665. 10.1046/j.1440-1746.2002.02746.x. PMID 12100610View ArticlePubMedGoogle Scholar
- Graham DY, Adam E, Reddy GT, Agarwal JP, Agarwal R, Evans DJ, Malaty HM, Evans DG: Seroepidemiology of H.pylori-infection in India. Dig Dis Sci. 1991, 36 (8): 1084-1088. 10.1007/BF01297451. 1864201View ArticlePubMedGoogle Scholar
- Fich A, Carel RS, Keret D, Goldin E: Sero prevalence of Helicobacter pylori in the Israeli population. Eur J Gastroenterol Hepatol. 1993, 5: 339-341. 10.1097/00042737-199305000-00007.View ArticleGoogle Scholar
- Zhou D, Yang H: Epidemiology of Helicobacter pylori infection in the People’s Republic of China. Chin Med J. 1995, 108 (4): 304-313. 7789221PubMedGoogle Scholar
- Malaty HM, Kim JG, Kim SD, Graham DY: Prevalence of helicobacter pylori infection in Korean children: inverse relation to socioeconomic status despite a uniformly high prevalence in adults. Am J Epidemiol. 1996, 143 (3): 257-262. 10.1093/oxfordjournals.aje.a008736. 8561159View ArticlePubMedGoogle Scholar
- Peach HG, Pearce DC, Farish SJ: Helicobacter pylori infection in an Australian regional city: prevalence and risk factors. Med J Aust. 1997, 167 (6): 310-313. PMID 9322776PubMedGoogle Scholar
- Gold BD, Khanna B, Huang LM, Lee CY, Banatvala N: Helicobacter pylori acquisition in infancy after decline of maternal passive immunity. Pediatr Res. 1997, 41 (5): 641-666. 10.1203/00006450-199705000-00007. PMID 9128285View ArticlePubMedGoogle Scholar
- Bakka AS, Salih BA: Prevalence of Helicobacter pylori infection in asymptomatic subjects in Libya. Diagn Microbiol Infect Dis. 2002, 43 (4): 265-268. 10.1016/S0732-8893(02)00411-X. PMID 12151185View ArticlePubMedGoogle Scholar
- Nurgalieva ZZ, Malaty HM, Graham DY, Almuchabetova R, Mahmudova A, Kapsultanova D, Osato MS, Hollinger FB, Zhangabylov A: Helicobacter pylori infection in Kazakhstan: effect of water source and household hygiene. Am J Trop Med Hyg. 2002, 67 (2): 201-206. PMID 12389948PubMedGoogle Scholar
- Sporea I, Popescu A, van Blankenstein M, Sirli R, Focşea M, Dănilă M: The prevalence of Helicobacter pylori infection in western Romania. Rom J Gastroenterol. 2003, 12 (1): 15-18. PMID 12673374PubMedGoogle Scholar
- Malekzadeh R, Merat S, Derakhshan MH, Siavoshi F, Yazdanbod A, Mikaeli J, Sotoudemanesh R, Sotoudeh M, Farashvash MJ, Nasseri-Moghaddam S, Pourshams A, Dolatshahi S, Abedi B, Babaei M, Arshi S, Majidpour A: Low Helicobacter pylori eradication rates with 4 and 7 day regimens in an Iranian population. J of Gastroenterol and Hepatol. 2003, 18: 13-17. 10.1046/j.1440-1746.2003.02897.x. PMID 12519218View ArticleGoogle Scholar
- Aguemon BD, Struelens MJ, Massougbodji A, Ouendo EM: Prevalence and risk- factors for Helicobacter pylori infection in urban and rural Beninese populations. Clin Microbiol Infect. 2005, 11 (8): 611-617. 10.1111/j.1469-0691.2005.01189.x. 16008612View ArticlePubMedGoogle Scholar
- Parente JML, Silva BB, Palha-Dias MP, Zaterka S, Nishimura NF, Zeitune JM: Helicobacter pylori infection in children of low and high socioeconomic status in northeastern Brazil. Am J Trop Med Hyg. 2006, 75 (3): 509-512. PMID 16968931PubMedGoogle Scholar
- Santos IS, Boccio J, Santos AS, Valle NCJ, Halal CS, Bachilli MC, Lopes RD: Prevalence of Helicobacter pylori infection and associated factors among adults in Southern Brazil: a population-based cross-sectional study. BMC Public Health. 2005, 5: 118-10.1186/1471-2458-5-118. PMID 16283940View ArticlePubMedPubMed CentralGoogle Scholar
- Ferreccio C, Rollan A, Harris PR, Serrano C, Gederlini A, Margozzini P, Gonzalez C, Aquilera X, Venegas A, Jara A: Gastric cancer is related to early Helicobacter pylori infection in a high-prevalence country. Cancer Epidemiol Biomarkers Prev. 2007, 16 (4): 662-667. 10.1158/1055-9965.EPI-06-0514. PMID 17416755View ArticlePubMedGoogle Scholar
- Apostolopoulos P, Vafiadis-Zouboulis I, Tzivras M, Kourtessas D, Katsilambros N, Archimandritis A: Helicobacter pylori (Hpylori) infection in Greece: the changing prevalence during a ten-year period and its antigenic profile. BMC Gastroenterol. 2002, 2: 11-10.1186/1471-230X-2-11. PMID 12014991View ArticlePubMedPubMed CentralGoogle Scholar
- Sitas F, Forman D, Yarnell WG, Burr ML, Elwood PC, Pedley S, Marks KJ: Helicobacter pylori infection rates in relation to age and social class in a population of Welsh men. Gut. 1991, 32 (1): 25-28. 10.1136/gut.32.1.25. PMID 1991634View ArticlePubMedPubMed CentralGoogle Scholar
- The EUROGAST Study Group: Epidemiology of, and risk factors for, Helicobacter pylori infection among 3194 asymptomatic subjects in 17 populations. Gut. 1993, 34 (12): 1672-1676. PMID 8282253View ArticleGoogle Scholar
- Murray LJ, McCrum EE, Evans AE, Bamford KB: Epidemiology of Helicobacter pylori infection among 4742 randomly selected subjects from Northern Ireland. Int J Epidemiol. 1997, 26 (4): 880-887. 10.1093/ije/26.4.880. PMID 9279623View ArticlePubMedGoogle Scholar
- Moayyedi P, Axon AT, Feltbower R, Duffett S, Crocombe W, Braunholtz D, Richards ID, Dowel AC, Forman D: Leeds HELP Study Group. Relation of adult lifestyle and socioeconomic factors to the prevalence of Helicobacter pylori infection. Int J Epidemiol. 2002, 31 (3): 624-631. 10.1093/ije/31.3.624. PMID 12055165View ArticlePubMedGoogle Scholar
- Bures J, Kopacova M, Koupil I, Vorisek V, Rejchrt S, Beranek M, Seifert B, Pozler O, Zivny P, Douda T, Kolesarova M, Pinter M, Palicka V, Holcik J: European Society for Primary Care Gastroenterology. Epidemiology of Helicobacter pylori infection in the Czech Republic. Helicobacter. 2006, 11 (1): 56-65. 10.1111/j.0083-8703.2006.00369.x. PMID 16423091View ArticlePubMedGoogle Scholar
- Us D, Hasçelik G: Seroprevalence of Helicobacter pylori infection in an Asymptomatic Turkish population. J of Infect. 1998, 37 (2): 148-150. 10.1016/S0163-4453(98)80169-2. PMID 9821089View ArticleGoogle Scholar
- Yilmaz E, Doğan Y, Gürgöze MK, Unal S: Seroprevalence of Helicobacte pylori infection among children and their parents in eastern Turkey. J Paediatr Child Health. 2002, 38 (2): 183-186. 12031003PubMedGoogle Scholar
- Kosunen TU, Höök J, Rautelin HI, Myllyla G: Age dependant increase of Camplylobacter pylori antibodies in blood donors. Scand J Gastroenterol. 1989, 24 (1): 110-114. 10.3109/00365528909092247. PMID 2648556View ArticlePubMedGoogle Scholar
- Perez-Perez GI, Taylor DN, Bodhidatta L, Wongsrichanalai J, Baze WB, Dunn BE, Echeverria PD, Blaser MJ: Seroprevalence of Helicobacter pylori infections in Thailand. J of Infect Dis. 1990, 161: 1237-1241. 10.1093/infdis/161.6.1237. PMID 2345304View ArticleGoogle Scholar
- Replogle ML, Glaser SL, Hiatt RA, Parsonnet J: Biologic sex as a risk factor for Helicobacter pylori infection in healthy young adults. Am J Epidemiol. 1995, 142 (8): 856-863. PMID 7572962PubMedGoogle Scholar
- Graham DY, Malaty HM, Evans DG, Evans DJ, Klein PD, Adam E: Epidemiology of Helicobacter pylori in an asymptomatic population in the United States: Effect of age, race and socipeconomic status. Gastroenterology. 1991, 100 (6): 1495-1501. PMID 2019355PubMedGoogle Scholar
- Leandro Liberato SV, Hernández Galindo M, Torroba Alvarez L, Sánchez Miramón F, Leandro Ciriza SE, Gómez Abadía A, Chueca Rodriquez P: Helicobacter pylori infection in the child population in Spain: prevalence, related factors and influence on growth. An Pediatr (Barc). 2005, 63 (6): 489–-494. PMID 16324613View ArticleGoogle Scholar
- Rokkas T, Liatsos C, Petridou E, Papatheodorou G, Karameris A, Ladas SD, Raptis SA: Relationship of Helicobacter pylori CagA(+) status to gastric juice vitamin C levels. Eur J of Clin İnvest. 1999, 29 (1): 56-62. 10.1046/j.1365-2362.1999.00432.x. PMID 10092990View ArticleGoogle Scholar
- You WC, Li JY, Zhang L, Jin ML, Chang YS, Ma JL, Pan KF: Etiology and prevention of gastric cancer: a population study in a high risk area of China. Chin J Dig Dis. 2005, 6 (4): 149-154. 10.1111/j.1443-9573.2005.00222.x. PMID 16246221View ArticlePubMedGoogle Scholar
- Kato I, Vivas J, Plummer M, Lopez G, Peraza S, Castro D, Sanchez V, Cano E, Andrade O, Garcia R, Franceschi S, Oliver W, Munoz N: Environmental factors in Helicobacter pylori related gastric precancerous lesions in Venezuela. Cancer Epidemiol Biomarkers Prev. 2004, 13 (3): 468-76.PubMedGoogle Scholar
- Simon JA, Hudes ES, Perez-Perez GI: Relation of serum ascorbic acid to Helicobacter pylori serology in US adults: the Third National Health and Nutrition Examination Survey. J Am Coll Nutr. 2003, 22 (4): 283-289. 10.1080/07315724.2003.10719305. PMID 12897042View ArticlePubMedGoogle Scholar
- Akarca US, Aydın A, Ozutemiz O, Musoglu A, Uslu Z: Ege yoresinde Helikobakter pylori infeksiyonunun seroprevalensi. Ege Tıp Derg. 1993, 32 (1–2): 31-35. [In Turkish]Google Scholar
- Ozden A, Dumlu S, Soylu K, Samur M, Uzunalimoglu O: The prevalence of Helicobacter pylori infection in a defined healthy population in Turkey [Abstract]. Hellenic J Gastroenterol. 1992, 5 (Suppl): 267-Google Scholar
- Turkdogan MK, Kaba I, Dulger C, Mete R, Akman N: abstract book of the forth East and Souteast Anatolia Hepato-Gastroenterology symposium. Epidemiological aspects of Helicobacter pylori infection in Van region of Eastern Turkey. 2004, 29-34.Google Scholar
- Klein PD, Graham DY, Gaillour A, Opekun AR, Smith EO: Water source as risk factor for Helicobacter pylori infection in Peruvian children. Lancet. 1991, 337 (8756): 1503-1506. 10.1016/0140-6736(91)93196-G. PMID 1675369View ArticlePubMedGoogle Scholar
- Murray LJ, Lane AJ, Harvey IM, Donovan JL, Nair P, Harvey RF: Inverse relationship between alcohol consumption and active Helicobacter pylori infection: the Bristol Helicobacter project. Am J Gastroenterol. 2002, 97 (11): 2750-2755. 10.1111/j.1572-0241.2002.07064.x. PMID 12425543View ArticlePubMedGoogle Scholar
- Brenner H, Rothenbacher D, Bode G, Adler G: Relation of smoking and alcohol and coffee consumption to active Helicobacter pylori infection: cross sectional study. BMJ. 1997, 315 (7121): 1489-1492. 10.1136/bmj.315.7121.1489. PMID 9420488View ArticlePubMedPubMed CentralGoogle Scholar
- Kuepper-Nybelen J, Rothenbacher D, Brenner H: Relationship between lifetime alcohol consumption and Helicobacter pylori infection. Ann Epidemiol. 2005, 15 (8): 607-613. 10.1016/j.annepidem.2004.11.001. PMID 16118005View ArticlePubMedGoogle Scholar
- Kuepper-Nybelen J, Thefeld W, Rothenbacher D, Brenner H: Patterns of alcohol consumption and Helicobacter pylori infection: results of a population-based study from Germany among 6545 adults. Aliment Pharmacol Ther. 2005, 21 (1): 57-64. 10.1111/j.1365-2036.2004.02276.x. PMID 15644046View ArticlePubMedGoogle Scholar
- The pre-publication history for this paper can be accessed here:http://www.biomedcentral.com/1471-2458/13/1215/prepub
This article is published under license to BioMed Central Ltd. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.