Helicobacter pylori infection is one of the most common chronic bacterial infections among humans worldwide 1. It plays a major etiological role in the pathogenesis of chronic gastritis, peptic ulcer disease, gastric adenocarcinoma, and mucosa-associated lymphoid tissue lymphoma. However, most of the infected individuals remain asymptomatic 2.
Great variation exists in the prevalence of H. pylori infection among different countries and age groups 3. The infection is rare in developed countries compared with developing countries 4. In the developed world, H. pylori infection rate in asymptomatic individuals ranges from 5 to 15%, whereas in developing countries it varies between 36 and 82%. Infection is either acquired during early childhood (30–50%) or during adulthood (90%) in developing countries 5.
H. pylori infection is well known to be the most common human infection worldwide on the basis of the fact that ∼50% of the world’s population is infected and that human beings are the main carriers 6. High rates of H. pylori infection are associated with low socioeconomic status and educational levels, poor housing and personal hygiene, overcrowding, and unhygienic sources of drinking water 7.
There have been a few reports from different parts of Saudi Arabia on H. pylori infection in patients with gastrointestinal diseases, indicating a prevalence rate of 60–88% 8,9, but little information is available on the seroprevalence of H. pylori in the healthy asymptomatic population 10. Therefore, the current study was designed to determine the seroprevalence of H. pylori in asymptomatic healthy individuals in Al Madinah, Saudi Arabia, and the possible relationships between H. pylori infection and sociodemographic, lifestyle, and environmental factors.
Subjects and methods
A hospital-based cross-sectional study was conducted in outpatient clinics and also among inpatients of King Fahd Hospital, Al Madinah, Saudi Arabia, from October 2011 through to March 2012 after approval from the Research and Ethics Committee at the hospital. Healthy individuals (family members and visitors of patients admitted for various illnesses) between the ages of 15 and 50 years were enrolled in the study. All individuals included were residents of Al Madinah city, in good health with no symptoms referable to the upper gastrointestinal tract.
Enrollees were asked questions on whether they had suffered from any serious illness or had undergone surgery in the past 2 months, whether they had undergone gastric surgery or were suffering from a peptic ulcer, or whether anyone in their immediate family had a peptic ulcer. In addition, each individual was questioned about the presence and frequency of upper gastrointestinal (GIT) symptoms, the use of any medication in the last 2 months, specifically antibiotics, bismuth-containing compounds, or NSAIDs, and use of tobacco or smoking. Individuals were excluded if they had a history of peptic ulcer and frequent symptoms of upper gastrointestinal tract infection. To reduce the false-negative results induced by acid-suppressive drugs or antibiotics, all individuals taking such medications during the 4 weeks before testing were excluded.
A pilot-tested interview format was used as the research tool. It was designed to obtain data related to sociodemographic characteristics such as age, gender, housing and living conditions (residence, number of rooms in the house, number of household members sharing a bedroom, the source of drinking water, and sewage disposal), lifestyle, and dietary habits. The presence or absence of a medical history of atopic symptoms and family history of upper GIT symptoms was also assessed.
Informed consent was obtained from each individual before inclusion in the study. Each individual was informed about the aim of this screening survey and the procedure, making absolutely certain that he/she was fully capable of understanding the procedure and evaluating the risk factors involved. The individuals were aware of the fact that they could withdraw from the study at any time, without any repercussions.
A consecutive sample (a strict version of convenience sampling in which every available individual is selected) of 456 healthy individuals who accepted to participate was included in the study. From each individual, about 5 ml of venous blood was taken. The sample was allowed to clot at room temperature for about an hour and then cooled in a refrigerator for 1–2 h before being centrifuged. Sera were stored at −70°C until analyzed. The H. pylori IgG antibodies were identified at the Laboratory of Microbiology, King Fahd Hospital, using the enzyme-linked immunosorbent assay. All serum samples were tested qualitatively for the presence of H. pylori IgG antibodies using a bioelisa Helicobacter IgG kit19 following the instructions given by the manufacturer (Biokit, S.A. Barcelona, Spain). All tests were performed and results were analyzed by the principal investigator and rechecked by a specialized laboratory technician.
A socioeconomic scale was used (modified from Aggarwal’s scale) 11 to assess the socioeconomic status of the studied individuals on the basis of the following parameters: monthly income, education of the head of the family, occupation, family possessions, type of house, number of earning members in the family, and family support. The maximum aggregate score was 100. On the basis of the final score, the socioeconomic status of the individual is divided into three categories: high (score>75), middle (score 50–75), and poor (combined score<50).
Data were entered and analyzed using SPSS version 19.0 (SPSS Inc., Chicago, Illinois, USA). Bivariate analysis was conducted to test significant differences between H. pylori-positive and H. pylori-negative individuals with regard to selected variables. The χ2-test was used for qualitative variables (such as gender, residence, and dietary habits) and the t-test was applied for quantitative variables such as age and residential crowding.
To control for potential confounding factors, multivariate analyses using the forward stepwise (Wald) method were carried out to determine the independent predictors of H. pylori-seropositive state among the healthy individuals. Variables included in the final model of the multivariate analysis were age plus selected sociodemographic, lifestyle, and environmental variables. For each variable, the age-adjusted prevalence odds ratio (OR) and 95% confidence interval (CI) were presented and computed directly from the logistic regression. P-values less than 0.05 were considered significant.
A total of 456 healthy asymptomatic individuals residing in Al Madinah, Saudi Arabia, were enrolled in the study. Of them, 221 (48.5%) were men and 235 (51.5%) were women whose ages ranged from 15 to 50 years. The mean age was 36.4 (SD=9.8) years. Overall, seroprevalence of H. pylori was 28.3% (95% CI=25.0–33.0%). Seropositive individuals had a mean age of 37.9 (SD=9.3) years.
Table 1 shows the age-specific prevalence of H. pylori (χ2 for trend=18.9, P=0.013). Individuals aged 15–50 years showed gradually increasing seroprevalence (between 16.9 and 36.8%) with increasing age. The highest seroprevalence (36.8%) was seen among those aged 41–50 years.
Among the 456 individuals, an increased prevalence of H. pylori was found in men (37.1%) compared with women (27.5%), but it did not reach statistical significance (P=0.053). However, when each age group was examined individually, higher positive percentages of H. pylori antibodies were seen in male individuals aged 20 years or below (21.9%), in those between 21 and 30 years (24.3%), and in those between 41 and 50 years (53.3%) compared with female individuals of the same age groups (12.8, 15.0, and 24.0%, respectively); these differences were statistically significant (P<0.05; Table 1).
The possible associations of selected sociodemographic, environmental, lifestyle, and clinical variables with the frequency of H. pylori infection are presented in Table 2.
There was no significant association between the presence of H. pylori antibodies and gender (P=0.053). However, H. pylori-positive individuals were significantly older (mean age 36.9±10.4 years) compared with H. pylori-negative individuals (mean age 33.7±9.3 years) (P=0.029). H. pylori seropositivity was significantly more frequently encountered among individuals from rural areas (55.4%) than among urban residents (44.6%; P=0.000). A significantly higher proportion of H. pylori-positive individuals was of low socioeconomic status (65.3%) compared with seronegative individuals (34.7%) (P=0.0001). The mean crowding index of infected individuals was 3.8 (SD=1.6). This was significantly higher than that of noninfected individuals [1.9 (SD 0.5); P=0.003].
Environmental factors were found to be linked to H. pylori infection. A higher percentage of the H. pylori-positive group used tanks as sources of drinking water (61.3%) and for sewage disposal (80.2%) as compared with 38.7 and 19.8%, respectively, of the H. pylori-negative group. The differences were statistically significant (P=0.000 in each). The H. pylori-positive group had a significantly higher percentage of active smokers (57.9%) compared with the H. pylori-negative group (42.1%; P=0.0001). Further, individuals in the H. pylori-positive group consumed alcohol more frequently than those in the seronegative group (74.3 versus 25.7%), and the difference was statistically significant (P=0.001).
With regard to dietary habits, H. pylori-seropositive individuals consumed larger quantities of raw vegetables (58.2%), fruits (55.7%), and spicy food (54.1%) compared with those in the negative group (41.8, 44.3, and 45.9%, respectively), and the differences were statistically significant (P<0.05).
A higher proportion of H. pylori-seropositive individuals reported a history of asthmatic/atopic symptoms (54.7%) as compared with 45.4% in the negative group, and this difference was statistically significant (P=0.024). However, family history of upper GIT symptoms had no effect on the seropositive status of the studied individuals (P=0.078).
In the logistic regression analysis (Table 3), after controlling for the confounding factors, significant independent predictors of the seropositive state among the healthy individuals in Al Madinah were: rural residence (adjusted OR=2.5, 95% CI=1.3, 4.7), crowded housing (adjusted OR=1.6, 95% CI=1.1, 2.6), low socioeconomic status (adjusted OR=3.3, 95% CI=1.6, 8.8), using tanks for drinking water supply (adjusted OR=2.2, 95% CI=1.2, 7.4), active smoking (adjusted OR=5.6, 95% CI=3.2, 9.8), alcohol drinking (adjusted OR=2.3, 95% CI=1.5, 6.2), eating raw vegetables (adjusted OR=3.2, 95% CI=1.4, 7.1), eating spicy food (adjusted OR=2.1, 95% CI=1.3, 3.5), and presence of atopic symptoms (adjusted OR=2.5, 95% CI=1.3, 5.9). No association was found between infection and age, gender, source of sewage disposal, eating fruits, and family history of upper GIT symptoms. These variables explain 79% of the variables predicting the seropositive state of H. pylori infection among the healthy individuals (R2=0.786) withoverall significance (P=0.001).
Infection with H. pylori occurs worldwide, but prevalence varies greatly between countries and between population groups within the same country. In this study, an overall prevalence of H. pylori infection was detected in 28.3% of asymptomatic individuals examined. A higher figure was shown in a study from Turkey 12, in which 53% of asymptomatic individuals were seropositive for anti-H. pylori antibodies. Compared with the present findings, higher seroprevalence rates of H. pylori were reported from Libya 13 (76%), Nigeria 14 (80%), Tunis 3 (83%), and Bangladesh 15 (92%). These differences reflect the socioeconomic factors in the previous studies including large families, crowded living conditions, and poor sanitation.
Earlier studies from Riyadh and Makkah, Saudi Arabia, showed an overall prevalence of 66 and 51%, respectively, for H. pylori infection in asymptomatic individuals 16,17. This clearly shows that the overall seroprevalence of H. pylori has decreased in this country. Improvements in the standard of living in Saudi Arabia have resulted in a marked reduction in H. pylori transmission.
An earlier study from Saudi Arabia 16 found an increase in H. pylori seroprevalence with advancing age, reaching 70% for those aged 20 years or more. In the present study, there was a gradual increase in prevalence rate with age from 16.9% among those aged 20 years or below to 36.8% for those between 41 and 50 years. A similar phenomenon was found in another study 18 in which asymptomatic individuals aged over 40 years showed 45–55% seropositivity for H. pylori. This finding further substantiates the age of acquisition of H. pylori as infection with H. pylori is a long-term chronic infection.
In accordance with many previous studies 19,20, gender appears to have no effect on the acquisition of H. pylori in our individuals. However, in the study by Broutet et al21., attention was given to gender differences, indicating that the prevalence of H. pylori infection was higher in men with upper digestive tract symptoms and nonupper digestive tract symptoms than in women. The reason for the possible gender difference in H. pylori prevalence is unclear but may be related to the frequency of eating in restaurants and smoking 22. Moreover, a meta-analysis indicated that male gender was a factor associated with the prevalence of H. pylori infection but the authors acknowledged that the study was limited by the unavailability of primary data from some studies, making it difficult to control for confounding variables 23.
The present study assessed the risk factors associated with the prevalence of H. pylori infection. The influence of socioeconomic factors on the prevalence of infection has been less well characterized 24. The present work indicated that low socioeconomic status is an independent factor associated with higher prevalence of infection.
The current results confirmed literature reviews suggesting that the transmission of H. pylori microorganisms may be facilitated by precarious hygiene conditions and crowded homes in low-income families 25. A cross-sectional survey in Lebanon showed that H. pylori infection is prevalent in asymptomatic healthy individuals. Low socioeconomic status, poor parental education, and tap water as the drinking water source were significant determinants of the prevalence of H. pylori infection. As this infection starts early in childhood and increases with age, prevention is achievable by improving the levels of education and the standards of hygiene among families of low socioeconomic standards 26.
The influence of lifestyle on the prevalence of H. pylori infection remains controversial. In the present study, active smokers were more likely to have H. pylori infection compared with nonsmokers or passive smokers, and this association remained significant when adjusted for confounding factors. El-Barrawy and colleagues demonstrated that infection prevailed mostly (70%) in smokers (113 of 161). According to the odds ratio, the risk of infection was 5.3 times higher for smokers than for nonsmokers, which was significant. They attributed their finding to the destructive effect of smoking on the immunity of the gastric mucosa and lining layers, hence increasing their susceptibility to infection by H. pylori. Communal Shisha smoking might carry the risk of passing the infection from a diseased person to an uninfected one, in the form of oral infection 27.
Rowland et al.20 have investigated the association between H. pylori and alcohol intake with conflicting results. The mechanisms that would promote an association with alcohol intake were unclear. However, this hypothesis is supported by our data. Alcohol consumption was a significant independent predictor for H. pylori infection.
Similar to the present study, a study from Kazakhstan was conducted among asymptomatic individuals between the ages of 10 and 60 years that examined various aspects of the local household environment and access to water. The study reported that transmission of H. pylori is largely opportunistic and can be water borne. If the rate of H. pylori transmission is to be reduced, an improvement in overall sanitation, including waste disposal and provision of clean water and safe food, as well as in household hygienic practices, is required 28.
It was reported that a pathogenetic link between H. pylori infection and diseases characterized by activation of inflammatory mediators and/or induction of autoimmunity might exist 29. In this regard, the present study indicated that asthmatic and/atopic symptoms among the studied group were significantly associated with H. pylori infection. A study conducted by Tsang et al.30 showed that patients with asthma had an H. pylori seropositivity of 47.3% compared with the 38.1% seen in controls. However, this difference was not statistically significant. Further studies should be undertaken to confirm the observed results.
The present study had some limitations. A consecutive sampling is the best choice among the nonprobability sampling techniques, as by studying all individuals available a good representation of the overall population is possible within a reasonable period of time. However, our results on the estimated levels of infection prevalence may not apply to the general population. Although the detection of H. pylori antigen in serum has a sensitivity and specificity of 85–90%, other tests (such as detection of H. pylori antigen in stool, the urease test, and culture of the organism from gastric biopsies) or test combinations may have improved our detection rate 31.
Conclusion and recommendations
This study revealed a declining seroprevalence of H. pylori in asymptomatic individuals of Al Madinah, Saudi Arabia. A population-based study would be needed to give a precise estimate of the burden of H. pylori infection and the relevant factors. This in turn will open avenues for more studies on the risk factors and mode of transmission of H. pylori.
The authors thank the staff of Microbiology Laboratory at King Fahd Hospital for technical assistance in this study. Thanks are also due to the participants involved in the study for their cooperation and help.
Conflicts of interest
There are no conflicts of interest.
1. Alborzi A, Soltani J, Pourabbas B, Oboodi B, Haghighat M, Hayati M, Rashidi M. Prevalence of Helicobacter pylori
infection in children (south of Iran). Diagn Microbiol Infect Dis. 2006;54:259–261
2. Uemura N, Okamoto S, Yamamoto S, Matsumura N, Yamaguchi S, Yamakido M, et al. Helicobacter pylori
infection and the development of gastric cancer. N Engl J Med. 2001;345:784–789
3. Ben Ammar A, Cheikh I, Kchaou M, Chouaib S, Ouerghi H, Chaâbouni H. Prevalence of Helicobacter pylori
infection in normal or asymptomatic patients. Tunis Med. 2003;81:200–204
4. Kim JH, Kim HY, Kim NY, Kim SW, Kim JG, Kim JJ, et al. Seroepidemiological study of Helicobacter pylori
infection in asymptomatic people in South Korea. J Gastroenterol Hepatol. 2001;16:969–975
5. Rothenbacher D, Brenner H. Burden of Helicobacter pylori
and H. pylori
-related diseases in developed countries: recent developments and future implications. Microb Infect. 2003;5:693–703
6. Go MF. Review article: natural history and epidemiology of Helicobacter pylori
infection. Aliment Pharmacol Ther. 2002;Suppl 16:3–15
7. Moraes MMC, Da Silva GAP. Risk factors for Helicobacter pylori
infection in children. J Pediatr (Rio J). 2003;79:21–28
8. Morad NA, Ahmed M-EBK, Al-Wabel A, Foli AK. Helicobacter pylori
associated dyspepsia in 208 patients from Southern Saudi Arabia. Ann Saudi Med. 1993;13:340–343
9. Zaman R. Diagnosis of Helicobacter pylori
infection. A study in the western province of Saudi Arabia. Saudi Med J. 1995;16:552–555
10. Koestermann FF, Arsene D, Dalloul A. Helicobacter pylori
antibodies in a Saudi population. Ann Saudi Med. 1996;16:60–63
11. Aggarwal OP, Bhasin SK, Sharma AK, Chhabra P, Aggarwal K. A new instrument (scale) for measuring the socioeconomic
status of a family: preliminary study. Indian J Comm Med. 2005;30:111–114
12. Us D, Hasçelik G. Seroprevalence
of Helicobacter pylori
infection in an asymptomatic Turkish population. J Infect. 1998;37:148–150
13. Bakka AS, Salih BA. Prevalence of Helicobacter pylori
infection in asymptomatic subjects in Libya. Diagn Microbiol Infect Dis. 2002;43:265–268
14. Oluwasola AO, Ola SO, Saliu L, Solanke TF. Helicobacter pylori
infection in South Nigerians: a serological study of dyspeptic patients and healthy individuals. West Afr J Med. 2002;21:138–141
15. Ahmad MM, Rahman M, Rumi AK, Islam S, Huq F, Chowdhury MF, et al. Prevalence of Helicobacter pylori
in asymptomatic population – a pilot serological study in Bangladesh. J Epidemiol. 1997;7:251–254
16. Al-Moagel MA, Evans DG, Abdulghani ME, Adam E, Evans DJ Jr., Malaty HM, Graham DY. Prevalence of Helicobacter
(formerly Campylobacter) pylori
infection in Saudi Arabia, and comparison of those with and without upper gastrointestinal symptoms. Am J Gastroenterol. 1990;85:944–948
17. Khan MA, Ghazi HO. Helicobacter pylori
infection in asymptomatic subjects in Makkah, Saudi Arabia. J Pak Med Assoc. 2007;57:114–117
18. Malaty HM, El-Kasabany A, Graham DY, Miller CC, Reddy SG, Srinivasan SR, et al. Age at acquisition of Helicobacter pylori
infection: a follow-up study from infancy to adulthood. Lancet. 2002;359:931–935
19. Kim JJ, Kim N, Park HK, Jo HJ, Shin CM, Lee SH, et al. Clinical characteristics of patients diagnosed as peptic ulcer disease in the third referral center in 2007. Korean J Gastroenterol. 2012;59:338–346
20. Rowland M, Daly L, Vaughan M, Higgins A, Bourke B, Drumm B. Age-specific incidence of Helicobacter pylori.
21. Broutet N, Sarasqueta A-M, Sakarovitch C, Cantet F, Lethuaire D, Mégraud F. Helicobacter pylori
infection in patients consulting gastroenterologists in France: Prevalence is linked to gender and region of residence. Eur J Gastroenterol Hepatol. 2001;13:677–684
22. Kaltenthaler EC, Elsworth AM, Schweiger MS, Mara DD, Braunholtz DA. Faecal contamination on children’s hands and environmental surfaces in primary schools in Leeds. Epidemiol Infect. 1995;115:527–534
23. 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;142:856–863
24. Malaty HM, Graham DY. Importance of childhood socioeconomic
status on the current prevalence of Helicobacter pylori
infection. Gut. 1994;35:742–745
25. Huang SSS, Hassan AKR, Keng EC, Ibrahim MI, Davis TME. Prevalence and predictors of Helicobacter pylori
infection in children and adults from the Penan ethnic minority of Malaysian Borneo. Am J Trop Med Hyg. 2004;71:444–450
26. Naous A, Al-Tannir M, Naja Z, Ziade F, El-Rajab M. Fecoprevalence and determinants of Helicobacter pylori
infection among asymptomatic children in Lebanon. J Med Liban. 2007;55:138–144
27. El-Barrawy MA, Morad MI, Gaber M. Role of Helicobacter pylori
in the genesis of gastric ulcerations among smokers and nonsmokers. East Mediterr Health J. 1997;3:316–321
28. Nurgalieva ZZ, Malaty HM, Graham DY, Almuchambetova R, Machmudova A, Kapsultanova D, et al. Helicobacter pylori
infection in Kazakhstan: effect of water source and household hygiene. Am J Trop Med Hyg. 2002;67(2 Suppl):201–206
29. Ichinose M. Inflammatory mechanisms in bronchial asthma and COPD. Tohoku J Exp Med. 2003;200:1–6
30. Tsang KW, Lam WK, Chan KN, Hu W, Wu A, Kwok E, et al. Helicobacter pylori seroprevalence
in asthma. Respir Med. 2000;94:756–759
31. Logan RPH, Walker MM. ABC of the upper gastrointestinal tract: epidemiology and diagnosis of Helicobacter pylori
infection. Br Med J. 2001;323:920–922