Observational Study Open Access
Copyright ©The Author(s) 2019. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastroenterol. Nov 14, 2019; 25(42): 6365-6372
Published online Nov 14, 2019. doi: 10.3748/wjg.v25.i42.6365
Epidemiologic characteristics of Helicobacter pylori infection in southeast Hungary
Lenke Bálint, Andrea Tiszai, Gábor Kozák, Ilona Dóczi, Veronika Szekeres, Orsolya Inczefi, Georgina Ollé, Krisztina Helle, Richárd Róka, András Rosztóczy
Lenke Bálint, Andrea Tiszai, Orsolya Inczefi, Georgina Ollé, Krisztina Helle, Richárd Róka, András Rosztóczy, Division of Gastroenterology, First Department of Medicine, University of Szeged, Szeged 6720, Hungary
Gábor Kozák, Department of Physiology, University of Szeged, Szeged 6720, Hungary
Ilona Dóczi, Department of Clinical Microbiology, University of Szeged, Szeged 6725, Hungary
Veronika Szekeres, Hungarian National Blood Transfusion Service, Szeged 6722, Hungary
ORCID number: Lenke Bálint (0000-0002-5814-3114); Andrea Tiszai (0000-0001-5608-0730); Gábor Kozák (0000-0002-3473-9351); Ilona Dóczi (0000-0003-4512-6486); Veronika Szekeres (0000-0001-8455-6484); Orsolya Inczefi (0000-0001-7974-1263); Georgina Ollé (0000-0003-1726-8436); Krisztina Helle (0000-0002-5477-2618); Richárd Róka (0000-0003-2373-2194); András Rosztóczy (0000-0002-8597-8934).
Author contributions: Bálint L, Rosztóczy A designed research, performed research, and wrote the paper; Tiszai A performed research; Kozák G designed research and analyzed data; Dóczi I contributed analytic tools; Szekeres V performed research; Inczefi O performed research; Ollé G performed research; Helle K performed research; Róka R performed research.
Institutional review board statement: The study was approved by the institutional review board of University of Szeged.
Informed consent statement: The institutional review board of University of Szeged waived the requirement to obtain informed consents from patients.
Conflict-of-interest statement: The authors have no conflict of interest to disclose.
Data sharing statement: No additional data are available.
STROBE statement: This study adopted the guidelines of the STROBE Statement.
Open-Access: This is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Corresponding author: András Rosztóczy, MD, PhD, Associate Professor, Division of Gastroenterology, First Department of Medicine, University of Szeged, Korányi fasor 8-10, Szeged 6720, Hungary. rosztoczy.andras@med.u-szeged.hu
Telephone: +36-62-545186 Fax: +36-62-545185
Received: September 2, 2019
Peer-review started: September 2, 2019
First decision: September 19, 2019
Revised: October 10, 2019
Accepted: October 18, 2019
Article in press: October 18, 2019
Published online: November 14, 2019

Abstract
BACKGROUND

Epidemiologic studies have revealed a decrease in the prevalence of Helicobacter pylori (H. pylori) infection in Western Europe.

AIM

To obtain data regarding the prevalence of H. pylori in Csongrád and Békés Counties in Hungary, evaluate the differences in its prevalence between urban and rural areas, and establish factors associated with positive seroprevalence.

METHODS

One-thousand and one healthy blood donors [male/female: 501/500, mean age: 40 (19–65) years] were enrolled in this study. Subjects were tested for H. pylori IgG antibody positivity via enzyme-linked immunosorbent assay. Subgroup analysis by age, gender, smoking habits, alcohol consumption, and urban vs non-urban residence was also performed.

RESULTS

The overall seropositivity of H. pylori was 32%. It was higher in males (34.93% vs 29.2%, P = 0.0521) and in rural areas (36.2% vs 27.94%, P = 0.0051). Agricultural/industrial workers were more likely to be positive for infection than office workers (38.35% vs 30.11%, P = 0.0095) and rural subjects in Békés County than those in Csongrád County (43.36% vs 33.33%, P = 0.0015).

CONCLUSION

Although the prevalence of H. pylori infection decreased in recent decades in Southeast Hungary, it remains high in middle-aged rural populations. Generally accepted risk factors for H. pylori positivity appeared to be valid for the studied population.

Key Words: Helicobacter pylori, Epidemiology, Prevalence, Central Europe, Healthy volunteers, Enzyme-linked immunosorbent assay, Differences in urban and rural population

Core tip: Whereas a decrease in the prevalence of Helicobacter pylori (H. pylori) has been confirmed in Western Europe, its prevalence in Central Europe, which has a substantial rural population, is unclear. Therefore, this study analyzed the prevalence of H. pylori among healthy volunteers in two Hungarian counties. The results of the study illustrated that the seropositivity of H. pylori in this area was 32%. The prevalence was higher in males, among people living in rural areas. Agricultural/industrial workers were more likely to be positive for infection than office workers. Meanwhile, rural subjects in Békés County had higher prevalence than those in Csongrád County.



INTRODUCTION

Helicobacter pylori (H. pylori) infection is one of the most common chronic human bacterial infections worldwide, affecting up to half of the world’s population. It is the main cause of gastritis, gastroduodenal ulcer, gastric adenocarcinoma, and mucosa-associated tissue lymphoma. Its prevalence is variable in relation to geography, ethnicity, age, and socioeconomic factors[1,2,3].

The prevalence of H. pylori has declined worldwide, although wide variation has been observed.

According to a 2017 and a 2018 meta-analysis, the countries with the lowest H. pylori prevalence were Switzerland (13.1%-24.7%), Denmark (17.8%-26.5%), New Zealand (21.4%-26.5%), Australia (17.2%-32.1%), and Sweden (18.3%-34.1%) in the former meta-analysis, Indonesia (10.0%), Belgium (11.0%), Ghana (14.2%), and Sweden (15.0) in the latter, whereas those with the highest prevalence were Nigeria (83.1%-92.2%), Portugal (84.9%-87.9%), Estonia (75.1%-90.0%), Kazakhstan (74.9%–84.2%), and Pakistan (75.6%-86.4%) in the former study, Serbia (88.3%), South Africa (86.8%), Nicaragua (83.3), and Colombia (83.1%) in the latter. The former study used two periods to analyze the prevalence trend over time. The H. pylori prevalence after 2000 was lower than that before 2000 in Europe (48.8 vs 39.8), North America (42.7% vs 26.6%), and Oceania (26.6% vs 18.7%)[4,5].

The major risk factors for H. pylori infection include socioeconomic status and the household hygiene of the patient and family during childhood. A previous Hungarian study revealed greater seropositivity among undereducated subjects, in persons living without sewers, those living in crowded homes or having three or more brothers and sisters, and those with high alcohol consumption, and they observed significant differences in prevalence between industrial and office workers. A Russian study reported that 88% of the Moscow working population is infected with H. pylori, 78% in people younger than 30 years, 97% in individuals older than 60 years. Recent epidemiologic studies revealed decreases in the prevalence of H. pylori in Western Europe and the United States. Conversely, little is known regarding the prevalence of H. pylori in Central Europe, in which a substantial population resides in rural areas[6,7,8,9,10].

The aims of this study were to obtain data regarding H. pylori prevalence in Csongrád and Békés Counties in Hungary, evaluate differences in prevalence between urban and rural areas, and establish factors associated with positive seroprevalence.

MATERIALS AND METHODS

One-thousand and one healthy blood donors [male/female: 501/500, mean age: 40 (18–65) years] were consecutively enrolled in Csongrád and Békés Counties. Detailed demographic data are shown in Figure 1[11,12,13].

Figure 1
Figure 1 Csongrád and Békés Counties and detailed demographic data regarding Csongrád and Békés Counties.

In Hungary, blood donation is allowed for individuals weighing more than 50 kg and aged 18–65 years. Data collection was performed using an anonymous questionnaire including 26 questions associated with demographic parameters (gender, age, place of birth, childhood residence, marital status, current residence, crowding in family, and educational status) and medical status (symptoms associated with H. pylori infection and gastroduodenal ulcer disease, smoking habits, alcohol consumption, and family history of H. pylori infection, gastroduodenal ulcer disease, and gastric malignancy).

On the basis of the childhood residence of the subjects, the following four groups of 250 subjects were established: Urban males, urban females, rural males, and rural females. Groups were matched by age. Subgroup analysis was performed according to living circumstances, residence in Békés or Csongrád County, smoking habits, alcohol and coffee consumption, occupation, intermittent agricultural work, pet or domestic animal rearing, gastrointestinal complaints, and family history of H. pylori infection, gastric ulcer, and gastric cancer.

All subjects were tested for H. pylori IgG antibody positivity using a Platelia H. pylori IgG enzyme-linked immunosorbent assay, which reportedly has 100% sensitivity and 90% specificity according to the manufacturer. These values were 95.6% and 85.1% in the validation study of Burucoa et al[14] respectively (Bio-Rad).

For the statistical analysis of different variables related to H. pylori infection, the chi-squared test or two-sample t-test was applied. The association between H. pylori infection and potential risk factors was established via univariate analysis, and odds ratios and 95% confidence intervals were calculated. In addition, a stratified analysis according to age (18–35, 35–50, and 50–65 years) was performed. The final model was developed using a generalized linear regression model via stepwise regression, with inclusion and exclusion criteria set at significance levels of 0.05 and 0.10, respectively. A two-sided P value < 0.05 was considered statistically significant. All statistical analyses were performed using MATLAB (Mathworks, Natwick, MA, United States).

RESULTS

The overall seropositivity of H. pylori was 32% in the studied healthy subjects. There was no statistically significant difference in prevalence between males and females (P = 0.0521) in our study. According to residence, the prevalence of H. pylori was significantly higher in rural areas than in urban areas (P = 0.0051). Furthermore, residence in rural areas for at least one year was associated with a significantly higher H. pylori prevalence than continuous urban residency (P = 0.0003). Parameters related to occupation were also associated with H. pylori infection. A higher prevalence was established for industrial workers and agricultural workers than for office workers and non-agricultural workers, respectively. Coffee consumption and pet or domesticated animal rearing were associated with H. pylori infection, whereas the rate of H. pylori positivity was similar for the remaining parameters. Detailed data are shown in Table 1-3.

Table 1 Sociodemographic factors associated with Helicobacter pylori prevalence.
Socio-demographic factorsH. pylori positive
H. pylori negative
TotalP valueOdds ratio (univariate)95%CI
n%n%
Sex0.0521
Female14629.235470.85001.0
Male17534.932665.15011.3016[0.9973, 1.6987]
Age0.000
44.563810.769337.359911.94570.9484[0.9363, 0.9606]
18-252514.914385.1168
25-353216.915783.1189
35-459734.418565.6282
45-5510643.613756.4243
55 +6151.35848.7119
Residence0.0809
Urban18530.043170.06161.0
Rural13635.324964.73851.2725[0.9706, 1.6683]
Childhood0.0051
Urban14027.936172.15011.0
Rural18136.231963.85001.4631[1.1201, 1.9110]
Min. one year in rural enviroment0.0003
Negative10425.630374.44071.0
Positive21736.537763.55941.6770[1.2695, 2.2153]
Table 2 Socioeconomic and lifestyle factors associated with Helicobacter pylori prevalence.
Socio-economic + lifestyle factorsH. pylori positive
H. pylori negative
TotalP valueOdds ratio (univariate)95%CI
n%n%
Smoking0.1121
Non-smoker16929.540370.55721.0
Smoker9134.217565.82661.2400[0.9090, 1.6915]
Former smoker6137.410262.61631.4261[0.9904, 2.0534]
Alcohol consumption0.1420
Never9536.016964.02641.0
Occasional21630.349769.77130.7731[0.5740, 1.0413]
Regular1041.71458.3241.2707[0.5434, 2.9715]
Coffee0.0390
Never8226.722573.33071.0
19436.316563.72591.5632[1.0929, 2.2358]
More than 114533.329066.74351.3720[0.9943, 1.8931]
Household population0.1649
Alone5139.27960.81301.0
Adults only13531.529468.54290.7113[0.4736, 1.0683]
Adults and children13530.530769.54420.6812[0.4538, 1.0224]
Work0.0000
Industrial18638.429961.64851.0
Office13526.238173.85160.5696[0.4355, 0.7450]
Agricultural work0.0012
No14027.437172.65111.0
Yes18136.930963.14901.5523[1.1882, 2.0279]
Domestic animals0.0015
No5423.517676.52301.0
Yes26734.650465.47711.7266[1.2301, 2.4236]
Table 3 Factors in patient history associated with Helicobacter pylori prevalence.
Patient historyH. pylori positive
H. pylori negative
TotalP valueOdds ratio (univar-iate)95%CI
n%n%
Familiy history of H. pylori0.8829
Negative16132.533567.54961.0
Positive1831.04069.0580.9363[0.5205, 1.6844]
NA14231.830568.2447
Family history of GI ulcer0.3810
Negative21733.343566.76521.0
Positive5729.713570.31920.8464[0.5965, 1.2009]
NA4729.911070.1157
Family history of GI cancer0.0014
Negative27732.158767.98641.0
Positive1763.01037.0273.6025[1.6284, 7.9701]
NA2733.85366.380
Abdominal pain0.8108
Negative26432.255567.88191.0
Positive5731.312568.71820.9586[0.6784, 1.3547]
Epigastrial pain0.1105
Negative21430.548769.57011.0
Positive10735.719364.33001.2617[0.9481, 1.6789]

A significant positive association was observed between age and H. pylori positivity (Table 1). To rule out this strong effect of age, three age groups were formed for further analysis. In the youngest group, the presence of epigastric pain was an independent risk factor for H. pylori positivity. By contrast, animal rearing was a risk factor for the middle age group, and male sex and living in rural areas for at least one year were risk factors in the oldest age group (Table 4).

Table 4 Independent risk factors associated with Helicobacter pylori prevalence.
Age 18-35Age 35-50Age 50-65
Male sexNot significantNot significantP = 0.0389; OR = 0.5847; CI: [0.0753 1.0940]
Rural residence in childhoodNot significantNot significantP = 0.0246; OR = 1.8537; CI: [1.3154 2.3920]
Animal rearingNot significantP = 0.0036; OR = 2.0855; CI: [1.5897 2.5812]Not significant
Epigastrial pain complaintP = 0.0026; OR = 2.5514; CI: [1.9422 3.1606]Not significantNot significant
DISCUSSION

This prospective study proved that the Hungarian prevalence of H. pylori infection has followed international trends, falling to 32% over the last two decades. The prevalence between 1990 and 2000 was similar throughout the country (58.6%–63.3%) excluding the capital, in which the prevalence was only 47.3% (Table 5). Although the Southeastern region of the country was not studied prospectively before this study, the H. pylori Workgroup of our institute conducted a retrospective analysis in 2005 and 2010 among patients with dyspepsia and gastroduodenal ulcer disease. The rate of seropositivity decreased from 46% to 38%. The 2017 meta-analysis used two periods to analyze the changes of prevalence trend. The H. pylori prevalence after 2000 was lower than that before 2000 in Europe (48.8 vs 39.8), North America (42.7% vs 26.6%), and Oceania (26.6% vs 18.7%). In the surrounding Central European countries, such as the Czech Republic and Slovakia, the prevalence of H. pylori infection followed the trends of our region, decreasing from 42% to 23% after 10 years in the former from 62% to 35% after 15 years in the latter[4,6,15-21].

Table 5 The prevalence between 1990 and 2000 throughout the country.
Date1993199920001998-2000
RegionTolnaVasSzabolcs-Szatmár-BeregPest
AuthorsTamássy et al[15]Lakner et al[6]Iszlai et al[16]Prónai et al[19]
MethodSerologySerologySerology13C-UBT
PopulationBlood donorsBlood donorsHealthy volunteersSymptomatic patients
n =4005337561027
Prevalence of H. pylori (%)63.362.358.647.3

Having examined the potential factors associated with a higher H. pylori prevalence, our results were in concordance with previous observations revealing a positive linear association with age. Furthermore, our study supported findings that rural subjects are more likely to be H. pylori-positive than urban residents. Although we could not establish a significant effect of gender on the seroprevalence, it is impressive that older rural males have an approximately sixfold higher risk of H. pylori positivity than young urban females (61.29% vs 11.11% P < 0.0001). Such results are most commonly explained by differences in socioeconomic status and household hygiene of the family during childhood. Furthermore, a new original finding is that people who lived in rural conditions for at least one year also had an increased risk for H. pylori seropositivity. An evaluation of the occupations of the subjects provided further proof that socioeconomic factors can influence H. pylori infection risk. Meanwhile, the lack of difference in risk between urban and rural residence can be explained by the general improvement of living standards in our country over the last two decades, as most rural people currently have access to water supply and sanitation[6-8,16,20-23].

The link between epigastric pain and H. pylori seropositivity among young subjects supports the currently accepted, Rome IV diagnostic protocol for functional dyspepsia, which states the excluding H. pylori infection (known as “H. pylori-associated dyspepsia”) should be the first step in the presence of such symptoms. Conversely, improved household hygiene in recent decades likely explains the lack of a relationship between socioeconomic status and H. pylori prevalence in this group. The findings further supported the hypothesis that hygiene differences between urban and rural areas were more significant at their childhood than nowadays. In addition, young males had poorer hygiene, than young females at that during childhood[24].

This study has a limitation. In Hungary, blood donors are unpaid, healthy, and conscious volunteers; therefore, they may not completely represent all segments of the population of Southeast Hungary.

In conclusion, we proved that in line with the worldwide trends, the prevalence of H. pylori infection has decreased in Southeast Hungary with changes of society, including improvements in socioeconomic status and living standards, during recent decades. Meanwhile, the prevalence remains high in the middle-aged and older rural populations. Generally accepted risk factors for H. pylori positivity appeared valid for the studied population, whereas the presence of dyspeptic symptoms was identified as an independent risk factor in the young population.

ARTICLE HIGHLIGHTS
Research background

Epidemiologic studies have revealed a decrease in the prevalence of Helicobacter pylori (H. pylori) infection in Western Europe. Conversely, little is known regarding its prevalence in Central Europe, in which a substantial population resides in rural areas.

Research motivation

The last Hungarian epidemiologic studies on H. pylori were carried out approximately two decades ago and showed high seroprevalence rates. Therfore we aimed to obtain new data and to test whether it decreases similarly to the Western European tendencies.

Research objectives

The aims of the present study were to obtain data regarding the prevalence of H. pylori in Csongrád and Békés Counties in Hungary, evaluate the differences in its prevalence between urban and rural areas, and establish factors associated with positive seroprevalence.

Research methods

One-thousand and one healthy blood donors were enrolled. Data collection was performed using an anonymous questionnaire including 26 questions associated with demographic parameters and medical status. All subjects were tested for H. pylori IgG antibody positivity using IgG enzyme-linked immunosorbent assay.

Research results

The overall seropositivity of H. pylori was 32%. The prevalence of H. pylori was significantly higher in rural areas than in urban areas. Residence in rural areas for at least one year was associated with a significantly higher H. pylori prevalence than continuous urban residency. A significant positive association was observed between age, occupation, coffee consumption, pet or domesticated animal rearing and H. pylori positivity. Three age groups were formed for further analysis, in the youngest group, the presence of epigastric pain was an independent risk factor for H. pylori positivity.

Research conclusions

The prevalence of H. pylori infection decreased in recent decades in Southeast Hungary, it remains high in middle-aged rural populations. Generally accepted risk factors for H. pylori positivity appeared to be valid for the studied population. Furthermore, a new original finding is that people who lived in rural conditions for at least one year also had an increased risk for H. pylori seropositivity.

Research perspectives

The results of this study seems to consider the subsequent changes in seropositivity of H. pylori in Hungary. It would be interesting to test whether the significant positive association between age and H. pylori positivity continuous observed after 10 or 15 years or rather not, “new” infected will appear, or in the older age will stay low seropositivity. The other experience of this study is the link between epigastric pain and H. pylori seropositivity among young subjects, which supports the recommendation in countries with high H. pylori seropositivity, that patients with dyspeptic symptoms should be examined for H. pylori infection (Rome IV diagnostic protocol).

Footnotes

Manuscript source: Unsolicited manuscript

Specialty type: Gastroenterology and hepatology

Country of origin: Hungary

Peer-review report classification

Grade A (Excellent): 0

Grade B (Very good): B

Grade C (Good): C, C, C

Grade D (Fair): 0

Grade E (Poor): 0

P-Reviewer: Boyanova L, Mihara H, Reshetnyak VI, Triantafillidis JK S-Editor: Tang JZ L-Editor: A E-Editor: Zhang YL

References
1.  Hunt RH, Xiao SD, Megraud F, Leon-Barua R, Bazzoli F, van der Merwe S, Vaz Coelho LG, Fock M, Fedail S, Cohen H, Malfertheiner P, Vakil N, Hamid S, Goh KL, Wong BC, Krabshuis J, Le Mair A; World Gastroenterology Organization. Helicobacter pylori in developing countries. World Gastroenterology Organisation Global Guideline. J Gastrointestin Liver Dis. 2011;20:299-304.  [PubMed]  [DOI]  [Cited in This Article: ]
2.  Selgrad M, Bornschein J, Malfertheiner P. Helicobacter pylori: Infektion mit lokalen Komplikationen und systemischen Auswirkungen. Dtsch med Wochenschr. 2011;136:1790-1795.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 1]  [Cited by in F6Publishing: 2]  [Article Influence: 0.1]  [Reference Citation Analysis (0)]
3.  Fischbach W, Malfertheiner P, Hoffmann JC, Bolten W, Kist M, Koletzko S; Association of Scientific Medical Societies. Helicobacter pylori and gastroduodenal ulcer disease. Dtsch Arztebl Int. 2009;106:801-808.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 3]  [Cited by in F6Publishing: 5]  [Article Influence: 0.3]  [Reference Citation Analysis (0)]
4.  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;153:420-429.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 776]  [Cited by in F6Publishing: 561]  [Article Influence: 194.0]  [Reference Citation Analysis (0)]
5.  Zamani M, Ebrahimtabar F, Zamani V, Miller WH, Alizadeh-Navaei R, Shokri-Shirvani J, Derakhshan MH. Systematic review with meta-analysis: the worldwide prevalence of Helicobacter pylori infection. Aliment Pharmacol Ther. 2018;47:868-876.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 195]  [Cited by in F6Publishing: 140]  [Article Influence: 65.0]  [Reference Citation Analysis (0)]
6.  Lakner L, Jáger R, Toldy E, Sarang K, Varga L, Kovács LG, Döbrönte Z. A Helicobacter pylori infekció szeroepidemiológiai vizsgálata Vas megyében. Magy Belorv Arch. 1999;52:451-457.  [PubMed]  [DOI]  [Cited in This Article: ]
7.  Ford AC, Axon AT. Epidemiology of Helicobacter pylori infection and public health implications. Helicobacter. 2010;15:1-6.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 82]  [Cited by in F6Publishing: 66]  [Article Influence: 8.2]  [Reference Citation Analysis (0)]
8.  Goh KL, Chan WK, Shiota S, Yamaoka Y. Epidemiology of Helicobacter pylori infection and public health implications. Helicobacter. 2011;16:1-9.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 172]  [Cited by in F6Publishing: 156]  [Article Influence: 17.2]  [Reference Citation Analysis (0)]
9.  Reshetnyak VI, Reshetnyak TM. Significance of dormant forms of Helicobacter pylori in ulcerogenesis. World J Gastroenterol. 2017;23:4867-4878.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in CrossRef: 25]  [Cited by in F6Publishing: 19]  [Article Influence: 8.3]  [Reference Citation Analysis (0)]
10.  German SV, Zykova IE, Modestova AV, Ermakov NV. Epidemiological characteristics of Helicobacter pylori infection in Moscow. Gig Sanit. 2011;1:44-48.  [PubMed]  [DOI]  [Cited in This Article: ]
11.  Központi Statisztikai Hivatal, Hungarian Central Statistical Office  Magyarország számokban, 2014. Available from: https://www.ksh.hu/docs/hun/xftp/idoszaki/mosz/mosz13.pdf.  [PubMed]  [DOI]  [Cited in This Article: ]
12.  Központi Statisztikai Hivatal, Hungarian Central Statistical Office. Csongrád megye számokban, 2015.  Available from: http://www.ksh.hu/docs/hun/xftp/idoszaki/regiok/mesz/06_cs_14.pdf.  [PubMed]  [DOI]  [Cited in This Article: ]
13.  Központi Statisztikai Hivatal, Hungarian Central Statistical Office. Békés megye számokban, 2014.  Available from: http://www.ksh.hu/docs/hun/xftp/idoszaki/regiok/mesz/04_be.pdf.  [PubMed]  [DOI]  [Cited in This Article: ]
14.  Burucoa C, Delchier JC, Courillon-Mallet A, de Korwin JD, Mégraud F, Zerbib F, Raymond J, Fauchère JL. Comparative evaluation of 29 commercial Helicobacter pylori serological kits. Helicobacter. 2013;18:169-179.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 66]  [Cited by in F6Publishing: 57]  [Article Influence: 8.3]  [Reference Citation Analysis (0)]
15.  Tamássy K, Simon L, Mégraud F. Helicobacter pylori infekció magyarországi epidemiológiája (szeroepidemiológiai összehasonlító tanulmány). Orvosi Hetilap. 1995;136:1387-1391.  [PubMed]  [DOI]  [Cited in This Article: ]
16.  Iszlai É, Kiss E, Toldy E, Ágoston S, Sipos B, Vén L, Rácz F, Szerafin L. Helicobacter pylori szeroprevalencia és anti-CagA pozitivitás Szabolcs-Szatmár-Bereg megyében. Orvosi Hetilap. 2003;144:1713-1718.  [PubMed]  [DOI]  [Cited in This Article: ]
17.  Bálint L, Tiszai A, Lénárt Z, Makhajda E, Wittmann T. Helicobacter pylori Infection and eradication therapy of our out patients in 2005 and 2010 years. What has been changed with time? Z Gastroenterol. 2011;49:638.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 1]  [Article Influence: 0.1]  [Reference Citation Analysis (0)]
18.  Bálint L, Tiszai A, Dóczi I, Szekeres V, Makhajda E, Izbéki F, Róka R, Wittmann T, Rosztóczy A. Prevalence of Helicobacter pylori (HP) infection in south hungarian healthy subjects. Z Gastroenterol. 2012;50:476.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 1]  [Article Influence: 0.1]  [Reference Citation Analysis (0)]
19.  Prónai L, Tulassay Zs. A Helicobacter pylori eradikációjának sikertelensége: szempontok a további kezelés megítéléséhez. Orvosi Hetilap. 2003;144:1299-1302.  [PubMed]  [DOI]  [Cited in This Article: ]
20.  Kuzela L, Oltman M, Sutka J, Zacharova B, Nagy M. Epidemiology of Helicobacter pylori infection in the Slovak Republic. Hepatogastroenterology. 2012;59:754-756.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 2]  [Cited by in F6Publishing: 3]  [Article Influence: 0.2]  [Reference Citation Analysis (0)]
21.  Bureš J, Kopáčová M, Koupil I, Seifert B, Skodová Fendrichová M, Spirková J, Voříšek V, Rejchrt S, Douda T, Král N, Tachecí I. Significant decrease in prevalence of Helicobacter pylori in the Czech Republic. World J Gastroenterol. 2012;18:4412-4418.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in CrossRef: 28]  [Cited by in F6Publishing: 27]  [Article Influence: 3.5]  [Reference Citation Analysis (0)]
22.  de Martel C, Parsonnet J. Helicobacter pylori infection and gender: a meta-analysis of population-based prevalence surveys. Dig Dis Sci. 2006;51:2292-2301.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 86]  [Cited by in F6Publishing: 70]  [Article Influence: 5.7]  [Reference Citation Analysis (0)]
23.  Brown LMHelicobacter pylori: epidemiology and routes of transmission. Epidemiol Rev. 2000;22:283-297.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 547]  [Cited by in F6Publishing: 430]  [Article Influence: 27.4]  [Reference Citation Analysis (0)]
24.  Stanghellini V, Chan FK, Hasler WL, Malagelada JR, Suzuki H, Tack J, Talley NJ. Gastroduodenal Disorders. Gastroenterology. 2016;150:1380-1392.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 564]  [Cited by in F6Publishing: 336]  [Article Influence: 141.0]  [Reference Citation Analysis (0)]