Rapid Communication Open Access
Copyright ©2006 Baishideng Publishing Group Co., Limited. All rights reserved.
World J Gastroenterol. Mar 28, 2006; 12(12): 1957-1961
Published online Mar 28, 2006. doi: 10.3748/wjg.v12.i12.1957
Seroprevalence of Helicobacter pylori in dyspeptic patients and its relationship with HIV infection, ABO blood groups and life style in a university hospital, Northwest Ethiopia
Feleke Moges, Afework Kassu, Department of Microbiology and Parasitology, Gondar College of Medicine and Health Sciences, University of Gondar, Ethiopia
Getahun Mengistu, Department of Internal Medicine, Faculty of Medicine, Addis Ababa University, Ethiopia
Solomon Adugna, Department of Biochemistry, Gondar College of Medicine and Health Sciences, University of Gondar, Ethiopia
Berhanu Andualem, Department of Biology, Faculty of Applied Science, University of Gondar, Ethiopia
Takeshi Nishikawa, Hokkaido University of Education, Sapporo Campus, Division of Medicine and Nursing, Japan
Afework Kassu, Fusao Ota, Department of Preventive Environment and Nutrition, Institute of Health Biosciences, The University of Tokushima, Japan
Supported by University of Gondar
Correspondence to: Feleke Moges, Department of Microbiology and Parasitology, Gondar College of Medicine and Health Sciences, University of Gondar, PO Box 196, Gondar, Ethiopia. felekemogesy@yahoo.com
Telephone: +251-8-110174-250 Fax: +251-8-111479
Received: June 22, 2005
Revised: June 22, 2005
Accepted: June 22, 2005
Published online: March 28, 2006

Abstract

AIM: To determine the prevalence of Helicobacter pylori (H pylori) among dyspeptic patients and to assess the relationship between H pylori infection, blood group, HIV infection and life style of the patients.

METHODS: In a hospital-based cross-sectional study, patients attending Outpatient Department of University of Gondar Hospital were enrolled. Socio-demographic information was collected using questionnaires. Serum was analyzed for anti-H pylori IgG antibodies using a commercial kit. HIV serostatus was determined by enzyme-linked immunosorbent assay (ELISA). Blood grouping was performed by slide agglutination tests.

RESULTS: A total of 215 dyspeptic patients were included in the study. One hundred and sixteen patients (54%) were females and 99 (46%) were males. Anti-H pylori IgG antibodies were detected in sera of 184 (85.6%) patients. The prevalence was significantly higher in patients aged 50 years and above. Twenty point five percent of the patients were found to be seropositive for HIV. No significant association was found between sex, ABO blood groups, consumption of spicy diets, socio-economic status and seropositivity for H pylori. However, alcohol consumption was significantly associated with H pylori serology.

CONCLUSION: The prevalence of H pylori infection is associated with a history of alcohol intake and older age. The effect of different diet, alcohol and socioeconomic status as risk factors for H pylori infection needs further study.

Key Words: H pylori, Blood group, HIV, Life style



INTRODUCTION

Helicobacter pylori (H pylori), a flagellate Gram negative rod, infects over half of the world’s population[1] and plays a pivotal role in the etiology of a number of gastroduodenal diseases and development of gastric malignancy[2-4]. H pylori has been recognized as grade one carcinogen[5] and the National Institute of Health Consensus Development Conference Statement recommended that all patients who are found to have gastric or duodenal ulceration and concurrent H pylori infection should receive treatment aimed at eradicating the bacterium[6].

Low socio-economic status, low level of education, consumption of alcohol, gender and occupation are the risk factors for H pylori infection[7]. In addition, blood group antigens, which mediate attachment of H pylori to gastric mucosa, are associated with a risk of developing peptic ulcer and gastric cancer[1]. About 95% of patients with duodenal ulcers and perhaps 80% of patients with peptic ulcers are infected with this bacterium and its eradication greatly diminishes the recurrence of these ulcers[8]. However, there have been very few studies on the prevalence of H pylori in Ethiopian patients[9,10]. Therefore, the aim of this study was to determine the prevalence of H pylori among dyspeptic patients and to assess the relationship between H pylori infection, blood group, HIV infection and life style of patients attending Gondar University Hospital in Northwest Ethiopia.

MATERIALS AND METHODS

The study was conducted at the Hospital of Gondar University, Northwest Ethiopia, from February 2003 to June 2003. Patients who presented with complaints of dyspepsia were included in the study. Institutional ethical clearance was obtained from the Research and Publication Committee of Gondar University.

Socio-demographic and relevant clinical information was collected by a questionnaire. A senior internist examined the patients and filled the questionnaires. The variables included sex, age, ethnicity, smoking, stress, nutrition, alcohol consumption, exercise and socio-economic factors. After informed consent was obtained from each patient and appropriate pre-test counseling was provided about 5mL of venous blood was collected in vacutainer tubes and sera were separated by centrifugation immediately after clotting. Serological status of H pylori infection was tested with commercial H pylori serology kits (HEXAGON H.PYLORI, Germany) following instructions of the manufacturer. The kit was used for the detection of H pylori IgG antibodies in serum. It could detect anti-H pylori antibodies with a highsensitivity (97%) and specificity (95%) when compared with ELISA (HEXAGON H.PYLORI, Germany). Blood grouping was performed by slide agglutination test using monoclonal anti-A, anti-B, anti-AB and anti-D (Rho) antibodies. Testing for the presence of HIV antibodies was determined by ELISA following the manufacturer’s instructions (Vironostica HIV Uni-Form II plus O, Organon Teknika, Boxtel, The Netherlands). HIV serology test was carried out anonymously with all clinical and laboratory data identified by a code number. Data entry and analysis were performed using SPSS version 10 statistical package. χ2 test was used to compare the categorical data and logistics regression was used to avoid the confounder effect and to calculate the risk ratio. Odds ratio (OR) and 95% confidence interval (CI) were used to measure the strength of association. P < 0.05 was considered statistically significant.

RESULTS

A total of 215 dyspeptic patients were included in the study. Table 1 shows the socio-demographic characteristics of the study population in relation with H pylori serostatus. The mean age of the subjects was 35 years (range 14-74 years). A substantial majority (55.8%) of the patients were young adults aged 20-40 years. Females constituted 54% of the patients. Fifty three percent of the patients were farmers followed by students (13.5%). Regarding the marital status, 62.8% were married, 18.1% were singles and 10.2% were divorced. Fifty nine point one percent of the patients came from Gondar town and the remaining 48.1% came from rural areas.

Table 1 Association between socio-demographic characteristics and seropositivity for antibodies against H. pylori infection in dyspeptic patients (Northwest Ethiopia, 2003).
CharacteristicsnSerum anti-HP+[ n (%)]Serum anti-HP- [n (%)]OR (95% CI)P value
Sex0.2
Male9988 (88.9)11 (11.1)1
Female11696 (82.8)20 (17.2)0.6 (0.272,1.32)
Age group (yr)0.2
<202218 (81.8)4 (18.2)1
20-296251 (82.3)11 (17.7)1.03 (0.29, 3.65)
30-395847 (81.0)11 (19.0)0.95 (0.27, 3.37)
40-493227 (84.4)5 (15.6)1.20 (0.28, 5.08)
50-592727 (100.0)0 (0.0)2205.4 (0.0, 4.7E+19)
60-691010 (100.0)0 (0.0)2205.4 (0.0, 1.5E+3)
70-7944 (100.0)0 (0.0)2205.4 (0.0, 5.6E+45)
Occupation0.69
Farmer11497 (85.1)17 (14.9)1
House wife1412 (85.7)2 (14.3)1.05 (0.22,5.12)
Govt employee2018 (90)2 (10.0)1.57 (0.34, 7.43)
Student2924 (82.8)5 (17.2)0.84 (0.28, 2.51)
Unemployed1414 (100.0)0 (0.0)639.67 (0.0, 3.6E+39)
Merchant65 (83.3)1 (16.7)0.87 (0.09, 7.97)
Soldier22 (100.0)0 (0.0)639.67 (0.0, 1.5E+39)
Others1612 (75.0)4 (25.0)0.52 (0.15, 1.82)
Address
Rural127109 (85.8)18 (14.2)1
Urban8875 (85.2)13 (14.8)0.95 (0.44, 2.06)
Marital status0.7
Married135117 (86.7)131
Widowed1311 (84.6)2 (15.4)0.85 (0.17, 4.13)
Divorced2218 (81.8)4 (18.2)0.69 (0.21, 2.28)
Single3932 (82.1)7 (17.9)0.70 (0.27, 1.83)
Underage66(100.0)0(0.0)206.42 (0.0, 1.1E+15)

Among the patients, 184 (85.6%) were found to be positive for anti-H pylori antibodies. The sex specific prevalence in males was 88.9% which was not significantly different from that of females (82.8%). The prevalence of H pylori was significantly higher in patients aged 50 years and above (100%) when compared to patients aged < 50 years (82.2%) (χ2 = 8.54, γ= 1, P < 0.05). H pylori seroprevalence was not associated with residence, marital status, occupation and ethnic group of the patients (P > 0.05) (Table 1).

The prevalence of HIV among the patients was about 20.5% (44/215). The HIV seropositivity was not associated with H pylori seropositivity as only 19.6% (36/184) of the patients who were positive for H pylori were also positive for HIV while 25.8% (8/31) patients who were negative for H pylori were positive for HIV (Table 2). Analysis of demographic factors for HIV infection showed a significant association by residence (χ2 = 5.78, P < 0.01) and occupation (χ2= 24.78, γ= 7, P < 0.001) of the dyspeptic patients (Table 3)

Table 2 H pylori and HIV co-infection in dyspeptic patients attending Gondar University Hospital (Northwest Ethiopia, 2003).
H pylori
Totaln (%)Statistics
Seropositiven (%)Seronegativen (%)
HIV seropositive36 (19.6)8 (25.8)44 (20.5)P = 0.4
HIV seronegative148 (80.4)23 (74.2)171 (79.5)χ2 = 0.63
Table 3 Demographic factors for HIV infection in dyspeptic patients attending Gondar University Hospital (Northwest Ethiopia, 2003).
CharacteristicsHIV serostatus
P
Seropositive n (%)Seronegative n (%)
Male19 (19.2)80 (80.8)P = 0.6
SexOR= 0.87 (95% CI 0.42-1.77)
Female25 (21.6)91 (78.4)χ2= 0.18
Age group (yr)
10-2921 (25.3)62 (74.7)P = 0.3
30-4917 (18.7)74 (81.3)χ2= 2.23
≥ 506 (14.6)35 (85.4)γ = 2
ResidenceP< 0.01
Rural19 (15.0)108 (85.0)OR= 0.45 (95% CI 0.21-0.92)
Urban25 (28.4)63 (71.6)χ2= 5.78
Occupation
Farmer18 ( 15.8)96 (84.2)P< 0.001
Housewife3 (21.4)11 (78.6)χ2= 24.78
Gov’t employee2 (10.0)18 (90.0)γ = 7
Students4 (13.8)25 (86.2)
Unemployed8 (57.1)6 (42.9)
Merchant4 (66.7)2 (33.3)
Soldier02 (100)
Others5 (31.3)11 (68.7)

Analysis of blood group showed that 201 (93.5%) of the total subjects were rhesus positive (Rh+) and 14 (6.5%) were rhesus negative (Rh-). Among the total subjects blood group O was the most common blood group (43.3%) in the patients followed by blood groups B (28.4%), A (22.3%) and AB (6.0%), respectively. However, no statistically significant association was seen between H pylori infection and blood group of the patients (Table 4).

Table 4 Relationship between ABO blood groups and seropositivity of antibodies against Helicobacter pylori infection.
Blood groupSerum anti HP+[n (%)]Serum anti HP- [n (%)]
O76 (84.4)14 (15.6)
B59 (88.1)8 (11.9)
A41 (85.4)7 (14.6)
AB8 (80)2 (20)
Total184 (85.6)31 (14.4)

History of diet, alcohol consumption and socio-economic status were obtained from the patients. It was observed that seropositivity for anti-H pylori antibodies was significantly associated with history of alcohol consumption (OR= 2.78, 95% CI: 1.19-6.5, P < 0.01) (Table 5). Although there was a higher prevalence of H pylori infection in those with low socioeconomic status than in those having average income, the association was not statistically significant. Likewise, no statistically significant interaction was observed in the prevalence of H pylori infection and consumption of coffee and spicy foods (Table 5).

Table 5 Relationship between Helicobacter pylori infection and life style in dyspeptic patients attending Gondar University Hospital (Northwest Ethiopia, 2003).
Serum anti-HP+n (%)Serum anti-HP-n (%)P value
Yes128 (90.1)14 (9.9)< 0.01
Alcohol intakeχ2 = 7.05
No56 (76.7)17 (23.3)γ = 1
Coffee24 (82.8)5 (17.2)= 0.2
Diets Spicy food108 (89.3)13 (10.7)χ2 = 3.15
Others52 (80)13 (20)γ = 2
DISCUSSION

The prevalence of H pylori IgG antibody among dyspeptic patients was 85.6%. This finding is higher than an earlier report from 136 patients with non ulcer dyspepsia from Addis Ababa, showing a prevalence of 65% for H pylori[9]. However it is comparable with a recent report from blood donors in Addis Ababa, where a seroprevalence of 89% has been observed[10]. When compared to studies from other countries like England, France, Scandinavia, Italy, Belgium and USA, the seroprevalence found in this study is much higher[11]. This may be explained by the association between H pylori and low socioeconomic status as evidenced by unsafe drinking water[12] and other factors like low educational level which would have an impact on personal hygiene and environmental sanitation[13].

Prevalence of H pylori increases with age. It is interesting to note that in patients aged 50 years and above its prevalence is 100%. Similar results have been reported in other studies indicating the high frequency of infection in the elderly[13]. This tendency is believed to be attributable to the environmental factors specific to these age group rather than aging[13]. The lack of significant association between sex, residence of patients and H pylori is in line with previous reports from elsewhere[14,15].

In the present study, more than one fifth of the patients (20.5%) were found to be seropositive for HIV and the seroprevalence of HIV in H pylori-infected patients was also very high (19.6%). This high prevalence of HIV in dyspeptic patients reflects the severe magnitude of HIV infection in the general population in Northwest Ethiopia. Recent studies showed that 51.4% tuberculosis patients[16] and 5% cataract patients[17] were seropositive for HIV in the region substantiating our present observation. Co-infection with HIV can debilitate the defense mechanism of patients and increase morbidity and mortality.

Blood group O is associated with duodenal ulcer disease, while gastric ulcer and gastric carcinoma are associated with blood group A[18]. Since the identification of H pylori, no pathogenic mechanism has been identified to support this earlier finding. Lewis B blood group antigen has recently been shown to function as a receptor for H pylori adhesins, mediating bacterial adherence to the gastric epithelial surface, which is essential for bacterial colonization[19]. Furthermore, substitution of the Lewis B antigen with blood group A and B determinants results in failure of H pylori binding[19]. Reduced exposure of the Lewis B epitope in persons of blood groups A and B could result in lower H pylori infection rates and a predominance of H pylori infection in persons of blood group O[20]. This is consistent with the reported association of blood group O with duodenal ulcer disease, but at variance with the association of blood group A with gastric ulcer and carcinoma, which is also related with H pylori infection. The present study did not demonstrate any significant difference in H pylori serological status of dyspeptic patients with varying blood groups, which is consistent with similar studies from other countries[18,20-22].

Histories of alcohol (local alcoholic drinks like “Tella”, “Teji”“Araki” and beer) consumption appears to be a risk factor for H pylori infection, which is in line with study from Finland[23]. However, different results have been reported in other countries[24]. The reason for this contradictory result might be due to the difference in the type of alcoholic beverages consumed and the life time history of alcohol consumption. Socioeconomic status does not appear to be a risk factor for H pylori infection, although a higher proportion of patients with low income are found to be positive for H pylori antibody. This result is in line with reports form Zambia and United Kingdom[25,26]. Spicy foods and coffee are considered to be risk factors for H pylori infection. However, no statistically significant interaction was observed in the present study, but it has been reported in Japan[27].

In conclusion, the prevalence of H pylori infection is very high and associated with history of alcohol intake and older age. Different diet, alcohol and socioeconomic status as risk factors for H pylori infection need further study.

ACKNOWLEDGMENTS

The authors acknowledge the Research and Publication Office of University of Gondar for financing and thank Drs. Moges Tiruneh, Yenew Kebede and Mr. Andargachew Mulu from Department of Medical Microbiology for their valuable comments and Mr. Getu Degu for statistical consultation. Our thanks also go to Mrs. Birhanemeskel Tegene, Abebaw Getahun and Tessema Zewudie for their technical assistance.

Footnotes

S- Editor Wang J L- Editor Wang XL E- Editor Bi L

References
1.  Montecucco C, Rappuoli R. Living dangerously: how Helicobacter pylori survives in the human stomach. Nat Rev Mol Cell Biol. 2001;2:457-466.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 366]  [Cited by in F6Publishing: 382]  [Article Influence: 16.6]  [Reference Citation Analysis (0)]
2.  Howden CW. Clinical expressions of Helicobacter pylori infection. Am J Med. 1996;100:27S-32S; discussion 32S-34S.  [PubMed]  [DOI]  [Cited in This Article: ]
3.  Marshall BJ. Helicobacter pylori. Am J Gastroenterol. 1994;89:S116-S128.  [PubMed]  [DOI]  [Cited in This Article: ]
4.  Mégraud F. Resistance of Helicobacter pylori to antibiotics. Aliment Pharmacol Ther. 1997;11 Suppl 1:43-53.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 154]  [Cited by in F6Publishing: 162]  [Article Influence: 6.0]  [Reference Citation Analysis (0)]
5.  International Agency for Research on Cancer Schistosomiasis, Liver flukes and Helicobacter pylori. IARC Monographs on the Evaluation of Carcinogenic Risk to Humans, Lyon: IARC 1994; 6.  [PubMed]  [DOI]  [Cited in This Article: ]
6.  NIH Consensus Conference. Helicobacter pylori in peptic ulcer disease. NIH Consensus Development Panel on Helicobacter pylori in Peptic Ulcer Disease. JAMA. 1994;272:65-69.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 524]  [Cited by in F6Publishing: 533]  [Article Influence: 17.8]  [Reference Citation Analysis (0)]
7.  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;143:257-262.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 117]  [Cited by in F6Publishing: 123]  [Article Influence: 4.4]  [Reference Citation Analysis (0)]
8.  Calam J Clinical Science of Helicobacter pylori infection: Ulcers and NSAIDS. Farthing M.JG and Patchett S.E.eds. In Helicobacter infection. India: Panther publishers 1998; 55-62.  [PubMed]  [DOI]  [Cited in This Article: ]
9.  Tsega E, Gebre W, Manley P, Asfaw T. Helicobacter pylori, gastritis and non-ulcer dyspepsia in Ethiopian patients. Ethiop Med J. 1996;34:65-71.  [PubMed]  [DOI]  [Cited in This Article: ]
10.  Desta K, Asrat D, Derbe F. Seroprevalence of H. pylori infection among health blood donors in Addis Ababa, Ethiopia. Ethiop J Health Sci. 2002;12:109-116.  [PubMed]  [DOI]  [Cited in This Article: ]
11.  Pounder RE, Ng D. The prevalence of Helicobacter pylori infection in different countries. Aliment Pharmacol Ther. 1995;9 Suppl 2:33-39.  [PubMed]  [DOI]  [Cited in This Article: ]
12.  Klein PD, Graham DY, Gaillour A, Opekun AR, Smith EO. Water source as risk factor for Helicobacter pylori infection in Peruvian children. Gastrointestinal Physiology Working Group. Lancet. 1991;337:1503-1506.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 335]  [Cited by in F6Publishing: 354]  [Article Influence: 10.7]  [Reference Citation Analysis (0)]
13.  Epidemiology of, and risk factors for, Helicobacter pylori infection among 3194 asymptomatic subjects in 17 populations. The EUROGAST Study Group. Gut. 1993;34:1672-1676.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 266]  [Cited by in F6Publishing: 300]  [Article Influence: 9.7]  [Reference Citation Analysis (0)]
14.  Yamashita Y, Fujisawa T, Kimura A, Kato H. Epidemiology of Helicobacter pylori infection in children: a serologic study of the Kyushu region in Japan. Pediatr Int. 2001;43:4-7.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 25]  [Cited by in F6Publishing: 26]  [Article Influence: 1.1]  [Reference Citation Analysis (0)]
15.  Karari EM, Lule GN, McLigeyo SO, Amayo EO. Endoscopic findings and the prevalence of Helicobacter pylori in chronic renal failure patients with dyspepsia. East Afr Med J. 2000;77:406-409.  [PubMed]  [DOI]  [Cited in This Article: ]
16.  Kassu A, Mohammad A, Fujimaki Y, Moges F, Elias D, Mekonnen F, Mengistu G, Yamato M, Wondmikun Y, Ota F. Serum IgE levels of tuberculosis patients in a tropical setup with high prevalence of HIV and intestinal parasitoses. Clin Exp Immunol. 2004;138:122-127.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 11]  [Cited by in F6Publishing: 11]  [Article Influence: 0.6]  [Reference Citation Analysis (0)]
17.  Kassu A, Mekonnen A, Bekele A, Abseno N, Melese E, Moges F, Wondmikun Y, Ota F. HIV and syphilis infection among elderly people in northwest Ethiopia. Jpn J Infect Dis. 2004;57:264-267.  [PubMed]  [DOI]  [Cited in This Article: ]
18.  Smith AW, Aathithan S, Power EG, Abdulla Y. Blood group antigens and Helicobacter pylori infections. Lancet. 1994;343:543.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 12]  [Cited by in F6Publishing: 12]  [Article Influence: 0.4]  [Reference Citation Analysis (0)]
19.  Borén T, Falk P, Roth KA, Larson G, Normark S. Attachment of Helicobacter pylori to human gastric epithelium mediated by blood group antigens. Science. 1993;262:1892-1895.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 840]  [Cited by in F6Publishing: 777]  [Article Influence: 25.1]  [Reference Citation Analysis (0)]
20.  Niv Y, Fraser G, Delpre G, Neeman A, Leiser A, Samra Z, Scapa E, Gilon E, Bar-Shany S. Helicobacter pylori infection and blood groups. Am J Gastroenterol. 1996;91:101-104.  [PubMed]  [DOI]  [Cited in This Article: ]
21.  Loffeld RJ, Stobberingh E. Helicobacter pylori and ABO blood groups. J Clin Pathol. 1991;44:516-517.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 27]  [Cited by in F6Publishing: 29]  [Article Influence: 0.9]  [Reference Citation Analysis (0)]
22.  Henriksson K, Uribe A, Sandstedt B, Nord CE. Helicobacter pylori infection, ABO blood group, and effect of misoprostol on gastroduodenal mucosa in NSAID-treated patients with rheumatoid arthritis. Dig Dis Sci. 1993;38:1688-1696.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 13]  [Cited by in F6Publishing: 15]  [Article Influence: 0.5]  [Reference Citation Analysis (0)]
23.  Paunio M, Höök-Nikanne J, Kosunen TU, Vainio U, Salaspuro M, Mäkinen J, Heinonen OP. Association of alcohol consumption and Helicobacter pylori infection in young adulthood and early middle age among patients with gastric complaints. A case-control study on Finnish conscripts, officers and other military personnel. Eur J Epidemiol. 1994;10:205-209.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 13]  [Cited by in F6Publishing: 13]  [Article Influence: 0.4]  [Reference Citation Analysis (0)]
24.  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;315:1489-1492.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 95]  [Cited by in F6Publishing: 108]  [Article Influence: 4.0]  [Reference Citation Analysis (0)]
25.  McLaughlin NJ, McLaughlin DI, Lefcort H. The influence of socio-economic factors on Helicobacter pylori infection rates of students in rural Zambia. Cent Afr J Med. 2003;49:38-41.  [PubMed]  [DOI]  [Cited in This Article: ]
26.  Parsons HK, Carter MJ, Sanders DS, Winstanley T, Lobo AJ. Helicobacter pylori antimicrobial resistance in the United Kingdom: the effect of age, sex and socio-economic status. Aliment Pharmacol Ther. 2001;15:1473-1478.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 2]  [Cited by in F6Publishing: 2]  [Article Influence: 0.1]  [Reference Citation Analysis (0)]
27.  Machida-Montani A, Sasazuki S, Inoue M, Natsukawa S, Shaura K, Koizumi Y, Kasuga Y, Hanaoka T, Tsugane S. Association of Helicobacter pylori infection and environmental factors in non-cardia gastric cancer in Japan. Gastric Cancer. 2004;7:46-53.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 103]  [Cited by in F6Publishing: 114]  [Article Influence: 5.7]  [Reference Citation Analysis (0)]