Jpn. J. Infect. Dis., 61, 179-183, 2008

Original Article

The Prevalence of Helicobacter pylori and Related Factors among University Students in Turkey Tayfun Yücel*, Dilek Aygin1, Selen S¸en1 and Oya Yücel Medical Faculty and 1School of Health, Sakarya University, Sakarya, Turkey (Received December 17, 2007. Accepted February 21, 2008) SUMMARY: The frequency and risk factors for contamination of Helicobacter pylori infection was investigated among Sakarya University students. Two-hundred students randomly chosen from among those who volunteered for the study and met its criteria were included. Data were obtained by a questionnaire. H. pylori positivity was checked with the monoclonal H. pylori stool antigen test. Statistical analysis was done with chi-square test. The average age of the subjects was 21.14 ± 2.06, and 76% of them were female. Monthly family income was below 575 Euros in 69.5% of them, and 56% were living in state dormitories. H. pylori positivity was found to be as high as 63% in our group. According to the questionnaire (age, gender, blood groups, family income, crowded family living conditions, smoking, alcohol and caffeine consumption, the presence of gastric symptoms, family history, and hygienic behaviors), no statistical differences were found between the H. pylori positive and negative students. These data support the finding that personal and environmental conditions in adults did not affect H. pylori infectivity, and that H. pylori might be acquired in childhood. prevalence and the effecting factors among the students at our university. The relationship between H. pylori positivity and the current or long standing hygienic and nutritional habits of our students and their families was investigated. The secondary purpose was to provide knowledge for health personnel who are conducting similar studies.

INTRODUCTION Helicobacter pylori prevalence varies according to the population groups and countries studied. Seroepidemiologic studies indicate that approximately 50% of adults in developed countries and 90% of adults in developing countries are seropositive for H. pylori (1). Epidemiological studies carried out in Turkey indicate that the total infection rate varies between 70 and 80%, but has decreased steadily over the years (2,3). Though contagion type and way of H. pylori is still controversial, it is thought to be transmitted person to person by mouth or by a fecal to oral route (1). While this infection, which is typically acquired during infancy (4,5), does not lead to any symptoms in some people, it can cause significant symptoms in others. An etiologic relation has been found between H. pylori and many gastroduodenal inflammatory and neoplastic diseases (4). In addition, in recent years, a number of studies have revealed that H. pylori is related to diseases such as iron deficiency anemia, migraine, and coronary heart disease (6). In 1994, World Health Organization (WHO) declared H. pylori to be a “first-degree carcinogen” (1,6). Each year, approximately 1 million people lose their lives due to H. pylori-related diseases (2). The studies that have been carried out in recent years point out that H. pylori prevalence can be related to factors such as low socioeconomic status, living in crowded conditions, low hygiene level (4,7), social status, age (8), region, ethnic group (4,9), nutrition factors (10), blood groups (4,11), and cigarette and alcohol consumption (7,11). For this reason, it is important for every section of society to be aware of the frequency of the infection and to participate in eradication studies. The main purpose of this study was to determine the H. pylori

MATERIALS AND METHODS The study was carried out in a young population consisting of Sakarya University students by cross-sectional and seroepidemiologic methods. It was conducted between September 1, 2006 and May 30, 2007. Students who had received treatment for gastrointestinal problems and those who were known to be H. pylori (+) were excluded. Since the study subjects were volunteers, after the purpose and procedures of the study were explained and the participant approval form signed, 200 students among those who volunteered, and whom the statistician found eligible, were selected. Limitations: The fact that only a group of young people in a university were included in the study is a limitation. The majority of students participating were enrolled in the School of Health and were from a lower socioeconomic status. The fact that no statistically significant differences were found might have been because only a small population was studied. Questionnaires: The assessment of the participants’ health status and social and demographic characteristics were based on data from questionnaires. The questionnaires included questions on age, gender, blood groups, family income, crowded family living conditions, smoking, alcohol and caffeine consumption, the presence of gastric symptoms, family history, and hygienic behaviors. The written approvals were collected, and face-to-face interviews were conducted with the participating students, during which the questionnaire form was filled out. Tubes for collection of feces samples were then given. The data was obtained through the questionnaire. After receiving the necessary permission from the authorities of the institution, the data collection process began.

*Corresponding author: Mailing address: Kos¸uyolu, Veysi Pas¸a Sok. 100. Yıl Sitesi, H Blok, No:22, Üsküdar, ˙Istanbul, Turkey. Tel: +90-532-3138802, Fax: +90-264-2956602, E-mail: tayfuny @hotmail.com 179

were done with fresh stool samples. The results were evaluated within 10 min, and tests with any change of color of the test-line were interpreted as positive. Statistical analysis: Statistical analysis was performed using SPSS for Windows version 12.0 (SPSS Inc., Chicago, Ill., USA). Data was presented as mean ± SD. Chi-square analysis (χ2) was used in findings on comparison of Helicobacter positivity according to individual characteristics. Evaluations were carried out at the 99 - 95% confidence interval and P < 0.05 was considered statistically significant.

The questions on the questionnaire elicited the following information: 1. The individual characteristics of the students, including their background (age, place and region of birth, the longest lived place and region, place of accommodation, income level of parents, and number of family members), were recorded. 2. Whether the student had experienced any gastrointestinal problems for the last one month. 3. What the students’ habits were, including cigarette smoking, alcohol consumption, consumption of drinks such as coke, tea and coffee, and use of analgesic and anti-rheumatism drugs. The students were also questioned about the source of their drinking water. 4. The students were asked about whether they apply simple hygiene rules. 5. The students were asked whether they, or their family members, had any previous gastrointestinal diseases, symptoms and Helicobacter positivity. 6. The result of the Helicobacter test applied to the students was recorded. The students were asked whether they had experienced any gastrointestinal problems (number 2) to research the association between current gastrointestinal symptoms and H. pylori positivity. In addition, we questioned the students about their previous gastrointestinal symptoms (number 5). H. pylori analysis: The stool specimens collected were examined by a one step H. pylori antigen cassette test (Linear Chemicals, S.L, Barcelona, Spain) for the detection of H. pylori. It was a qualitative immunochromatographic assay using monoclonal antibodies. The test cassettes in the preapplication period were stored between 4 and 8°C during the study. An H. pylori stool antigen (HpSA) test was performed according to the manufacturer’s recommendation. The tests

RESULTS Among the students, the H. pylori positivity ratio was found to be 63% (126/200) in our study. It was found that the average age of the students was 21.14 ± 2.06; 76% of them were female and 24% male; the majority came from the Black Sea and Marmara regions; 56% of them were accommodated in state dormitories, and 69.5% of them had a monthly family income of 1,000 YTL (575 Euros) or lower. No statistically significant difference was found between these demographic characteristics and H. pylori positivity (Table 1). In Table 2, the “yes I comply with this hygiene rule” answers of the students to questions about simple hygiene rules were compared with H. pylori positivity. No statistically significant difference (P > 0.05) was detected between the students who follow hygiene rules and those who do not in terms of H. pylori positivity. It was found that the majority of H. pylori positive or H. pylori negative students followed hygiene rules such as washing their hands, using a fork and spoon, and washing foods. When gastrointestinal symptoms that had developed in the last one month were compared, it was found that the relation

Table 1. Comparison of demographic characteristics and Helicobacter positivity Demographic characteristic

Helicobacter (+) (n = 126) no. (%)1)

Helicobacter (–) (n = 74) no. (%)2)

χ2

P*

Age

20 and under 21 - 23 24 and over

55 (43.7) 59 (46.8) 12 (9.5)

28 (37.8) 40 (54.1) 6 (8.1)

0.976

0.614

Gender

Women Men

96 (76.2) 30 (23.8)

56 (75.7) 18 (24.3)

0.934

1.000

Educational status of mother

Not literate Primary school Secondary school High and university

14 (11.1) 82 (65.1) 11 (8.7) 19 (15.1)

9 (12.2) 41 (55.4) 12 (16.2) 12 (16.2)

3.065

0.382

Educational status of father

Not literate Primary school Secondary school High school University

9 (7.1) 44 (34.9) 24 (19) 36 (28.6) 13 (10.3)

2 (2.7) 30 (40.5) 16 (21.6) 18 (24.3) 8 (10.8)

2.546

0.636

Occupation of mother

Working Not working

14 (11.1) 112 (88.9)

10 (13.5) 64 (86.5)

0.255

0.614

Occupation of father

Working Not working

93 (73.8) 33 (26.2)

14 (85.1) 60 (14.9)

3.485

0.062

Gastrointestinal disease

had did not have

22 (17.5) 104 (82.5)

14 (18.9) 60 (81.1)

0.067

0.795

1)

: Percentage in H. pylori (+) s. : Percentage in H. pylori (–) s. * No statistically significant difference (P > 0.05). 2)

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Table 2. Comparison of hygiene applications and Helicobacter positivity Some hygiene application1) I do not share materials such as fork, spoon and knife with someone else during the meal. I wash my hands before the meals. I wash my hands after toilet. I like eating meal with my hands without using fork and spoon. I do not eat vegetables and fruit without first washing them. I do not share my bed with someone else.

Helicobacter (+) (n = 126) no. (%)2)

Helicobacter (–) (n = 74) no. (%)3)

χ2

P*

99 (78.6)

60 (81.1)

0.180

0.671

109 (86.5) 122 (98.6)

57 (77) 73 (98.6)

2.970 0.636

0.085 0.525

12 (9.5)

3 (4.1)

2.011

0.156

111 (88.1)

64 (86.5)

0.110

0.740

62 (49.2)

29 (39.2)

1.886

0.170

1)

: Ones who answered yes in hygiene applications were considered. : Percentage in Helicobacter (+) s. 3) : Percentage in Helicobacter (–) s. * No statistically significant difference (P > 0.05). 2)

Table 3. Comparison of gastrointestinal symptoms developed in last 1 month and Helicobacter positivity Gastrointestinal disease1)

Helicobacter (+) (n = 126) no. (%)2)

Helicobacter (–) (n = 74)

15 (11.9) 6 (4.8)

5 (6.8) 7 (9.5)

11 (8.7)

13 (17.6)

3.448

0.063

10 (7.9) 19 (15.1) 12 (9.5) 20 (15.9) 40 (31.7) 19 (15.1) 1 (1.4) 18 (14.3) 40 (31.7)

4 (5.4) 13 (17.6) 3 (4.1) 12 (16.2) 26 (35.1) 13 (17.6) 1 (1.4) 9 (12.2) 29 (39.2)

0.459 0.215 2.011 0.004 0.242 0.215 0.146 0.180 1.143

0.498 0.643 0.156 0.949 0.623 0.643 0.702 0.671 0.285

Stomachache immediately after meals Stomachache 2 - 3 h after the meals Gnawing pain at midnight (when the stomach is empty) Loss of weight Lack of appetite Sudden intense, permanent stomachache Nausea Stomach bloating Anemia Bloody and black feces Eructation Sour stomach, burning

χ2

P*

1.373 1.693

0.241 0.193

no. (%)3)

1)

: Ones who answered yes in gastrointestinal symptoms were considered. : Percentage in Helicobacter (+) s. 3) : Percentage in Helicobacter (–) s. * No statistically significant difference (P > 0.05). 2)

between them was not statistically significant (P > 0.05) (Table 3). In Table 4, other questions in the questionnaire were compiled and a common chi-square table was prepared for the H. pylori positive cases. No statistically significant difference was found between H. pylori positivity and the student’s department, place of birth, accommodation place and number of people, and income level of the family. In addition, when Helicobacter positivity was compared with smoking, alcohol, coke, tea and coffee consumption and asetil salisilic acid and rheumatism drug use, no statistically significant difference was found. No statistical difference was found between the source of drinking water (network water, bottled water), the subjects who had digestive system disease in the family, or the conditions of H. pylori positivity. There were no correlations between blood groups and H. pylori positivity, either (Table 4).

Turkey, H. pylori infection occurs frequently. In a previous study, the distribution of H. pylori (+) frequency according to age groups was found to be: 96% in the 7 - 12 age group; 83% in the 13 - 18 age group; 75% in the 19 - 24 age group; 96% in the 25 - 29 age group; 91% in the 30 - 34 age group; 83% in the 35 - 39 age group; and 94% in the 40 - 65 age group (6). The average age of the students who took part in our study and the H. pylori (+) ratio is similar with the literature. Özden et al. noted that the rate of H. pylori (+) cases in their studies was 78.5%, and did not find a significant difference between age groups and gender distributions. However, it was emphasized that this ratio has been decreasing over the years (3). H. pylori positivity was detected at quite a high rate among our students (63%). The students who were known to be H. pylori (+) previously, and those with diagnosed and treated gastric disorders were excluded from the study because we were attempting to find out what the H. pylori positivity was in ordinary young people chosen at random, whether they had gastrointestinal symptoms or not. Young people were specifically chosen for the study because there are many papers in the literature about the H. pylori status of children or adults with gastrointestinal symptoms, but papers related

DISCUSSION Socioeconomic conditions (especially in infancy), genetic characteristics, hygiene levels, and family life habits influence the distribution of H. pylori in different populations. In 181

Table 4. Helicobacter positivity and chi-square comparison results Comparison of some questions with H. pylori positivity

χ2

P*

The faculty of the students Birth place Accommodation place Number of family members Income level Current cigarette smoking Current alcohol consumption Current coke consumption Current tea consumption Current coffee consumption Taking asetil salisilic acid Taking pain killer Taking rheumatism drugs Drinking water source Having digestive system diseases in the family Helicobacter (+) in the family Blood groups

7.262 1.821 0.341 0.782 9.089 3.401 0.235 1.653 1.446 1.928 0.063 0.002 0.252 2.209 0.057 0.469 3.844

0.297 0.873 0.843 0.941 0.106 0.065 0.628 0.199 0.229 0.165 0.802 0.965 0.616 0.137 0.811 0.791 0.427

infection risk. In many studies it was thought that the frequent consumption of vegetables, fruits, vitamin C, and probiotics were protective against H. pylori infection (7,10, 13). When Helicobacter positivity was compared between the people who had gastrointestinal problems in the last one month and those who did not, it was found that the difference was not significant in the literature. In a study which analyzed H. pylori frequency and its relation with dyspeptic complaints in hemodialysis patients, no significant difference in terms of H. pylori positivity distributions and dyspeptic complaints such as bloating, burning and a sour taste in the mouth were found (6,14,16). Our results were the same. Epidemiologic studies indicate inconsistent results about the relation between cigarette smoking, which is accepted as a risk factor for gastric cancer, and H. pylori infection. Recent studies which have analyzed the relation between cigarette smoking and H. pylori risk produced controversial results. While some studies suggested that H. pylori risk significantly rose with cigarette smoking, another study has suggested that it decreased the risk (2,11). However, like our study, many studies found no significant relation between cigarette smoking or alcohol consumption and H. pylori infection (17,18). Recent epidemiological studies which analyzed the relation between alcohol consumption and H. pylori infection, also did not find any relation (17), similar our results. Many studies have indicated that H. pylori can survive in water, and that there is a relation between drinking water source and H. pylori infection; the prevalence was more frequent, especially in places where untreated water was used (15,19,20). For example, it was noted that people who always drank boiled water had lower H. pylori prevalence (20). Malaty et al. did not find a relation between drinking water source and H. pylori positivity (13). In our study, it was found that the majority of the students drank network water and no one used boiled water, but there was no significant correlation between these students and the ones who drank bottled water in terms of H. pylori infection. Scientists have long observed, without investigating the scientific reasons for this that people with O blood groups were more susceptible to peptic ulcer. In 1993, Boren et al. reported that people with O blood groups had more H. pylori receptors, which had an affect in sticking Lewis b antigens to gastric mucosa (21). Some authors also reported that people with the O blood group were 3.74 times (2.99 - 5.75) more at risk for H. pylori positivity than other blood groups (1). On the other hand, some studies reported that there was no correlation between H. pylori infection and ABO blood groups (11). In our study, we did not find any correlations between H. pylori and blood groups. In recent studies, it has been suggested that H. pylori prevalence has been decreasing over the years. It was thought that better health, hygiene and socioeconomic conditions and the use of antibiotics could be the reasons for the decrease (3, 13,22). It has been noted that when the educational level of society increases, life style and sanitation conditions improve, and medical services and nutrition levels also improve; H. pylori prevalence then decrease (22-24). In conclusion, the high H. pylori positivity ratio (63%) that we obtained indicates that H. pylori infection is still a common problem among our young population. However, we did not find any strict relations between H. pylori positivity and risk factors in our study. These data support the finding that personal and environmental conditions do not affect H.

*No statistically significant difference (P > 0.05).

to young adults are rare. We also focused on young adults because they constitute the future of our society. No difference was found between H. pylori positivity and gender in our study. However, some studies in the literature have indicated that males are at significant risk for the infection (12), while other studies indicate that the infection risk is the same for males and females (9). These latter views support the findings of our study. It should be noted that most of our students came from the Black Sea and Marmara regions, but we did not find any regional differences in terms of H. pylori (+) in this study. The fact that most of the students live in state dormitories is related to the income level of the family, and income level is related to the educational level of the students’ parents. High H. pylori positivity is a result of this situation. So, in our study, no significant difference was found between H. pylori positivity and this data. A study conducted in China which supports our findings indicates that there is no relation between educational level, income level and H. pylori (+) (6). Many studies conducted worldwide have shown that H. pylori infection and social class factors are interrelated. In a study conducted, no relation was found between educational level, social status and H. pylori positivity (13). No significant difference was detected in terms of H. pylori positivity between the students who followed hygiene rules and those who did not. However, some studies have mentioned the positive results of complying with hygiene rules (2,4). As H. pylori DNA was found in the nails of infected people, the hands were thought to play a major role in the spread of the disease. There have been studies reporting that infrequent hand washing is related with infection (2). It was also suggested that unfavorable living conditions increased H. pylori prevalence. Crowded living conditions, especially a high number of children at home and number of people who share the same bed, increased the risk (2,14,15). However, our results did not support these previous results. Nutrition factors are the most important determinant of gastric cancer risk. However, very few studies refer to the relation between H. pylori and nutrition factors. In a crosssectional study conducted in Japan, it was reported that consuming salty foods was absolutely related to H. pylori 182

Dig. Dis., 50, 1214-1217. 12. Ito, L.C., Oba-Shinjo, S.M., Marie, S.K.N., et al. (2003): Lifestyle factors associated with atrophic gastritis among Helicobacter pyloriseropositive Japanese-Brazilians in São Paulo. Int. J. Clin. Oncol., 8, 362-368. 13. Malaty, H.M., Paykov, V., Bykova, O., et al. (1996): Helicobacter pylori and socioeconomic factors in Russia. Helicobacter, 1, 82-87. 14. Brown, L.M. (2000): Helicobacter pylori: epidemiology and routes of transmission. Epidemiol. Rev., 22, 283-297. 15. Nugalieva, Z.Z., Malaty, H.M., Graham, D.Y., et al. (2002): Helicobacter pylori ınfections in Kazakhstan: effect of water source and household hygiene. Am. J. Trop. Med. Hyg., 67, 201-206. 16. Hoffmann, K.M., Eherer, A.J. and Kreis, G.J. (2003): Are dyspeptic symptoms linked to Helicobacter pylori? A prospective cohort study among medical students. Wien Klin. Wochenschr., 115, 175-178. 17. Reshetnikov, O.V., Denisova, D.V., Zavyalova, L.G., et al. (2003): Helicobacter pylori seropositivity among adolescents in Novosibirsk, Russia: prevelance and associated factors. J. Pediatr. Gastroenterol. Nutr., 36, 72-76. 18. Farag, T.H., Stoltzfus, R.J., Khalfan, S.S., et al. (2007): Unexpectedly low prevalance of Helicobacter pylori infection among pregnant women on Pemba ˙Island, Zanzibar. Trans. R. Soc. Trop. Med. Hyg., 101, 915922. 19. Malaty, H.M., Kim, J.G., Kim, S.D., et al. (1996): Prevalance of Helicobacter pylori infection in Korean children: inverse relation to socioeconomic status despite a uniformly high prevalance in adults. Am. J. Epidemiol., 143, 257-262. 20. Oderga, G. (1999): Transmission of Helicobacter pylori infection. Can. J. Gastroenterol., 13, 595-597. 21. Borén, T., Falk, P., Roth, K.A., et al. (1993): Attachment of Helicobacter pylori to human gastric epithelium mediated by blood group antigens. Science, 17, 1892-1895. 22. Almad, M.A., Aliebreen, A.M., Tounesi, F.A., et al. (2007): Helicobacter pylori prevalence among medical students in high endemic area. Saudi Med. J., 28, 896-898. 23. Cataldo, F., Simpore, J., Greco, P., et al. (2004): Helicobacter pylori infection in Burkina Faso: an enigma within an enigma. Dig. Liver Dis., 36, 589-593. 24. Triantafillidis, J.K., Gikas, A., Hyphantis, T., et al. (2002): Helicobacter pylori infection in hospital workers over a 5-year period: correlation with demographic and clinical parameters. J. Gastroenterol., 37, 10051013. 25. Rotherbacher, D., Bode, G., Berg, G., et al. (1999): Helicobacter pylori among preschool children and their parents: evidence of parent-child transmission. J. Infect. Dis., 179, 398-402. 26. Wizla-Derambure, N., Michaud, L., Ategbo, S., et al. (2001): Familial and community environmental risk factors for Helicobacter pylori infection in children and adolescents. J. Pediatr. Gastroenterol. Nutr., 33, 58-63.

pylori infectivity in adults. Some findings in the literature report that H. pylori may be acquired in childhood (25,26). As H. pylori positivity can lead to serious gastrointestinal problems throughout an individual’s life, we would like to emphasize how important it is for H. pylori screening to be conducted in our country and throughout the world. ACKNOWLEDGMENTS Our research was supported by Sakarya University Research Fund financially. Thanks to Remzi Altunıs¸ık for statistical analysis. Also thanks to two students of Sakarya University, School of Health, Aysun Kaya and Gülgün Temiz, for supporting sample collecting. Manuscript was translated into English by professional bureau of Aslıhan Eyübo˘glu. REFERENCES 1. Sgouros, S.N. and Bergele, C. (2006): Clinical outcome of patients with Helicobacter pylori infection: the bug, the host, or the environment. Postgrad. Med. J., 82, 338-342. 2. Özden, A. (2006): Helicobacter pylori 2006. Güncel Gastroenterol., 10, 287-291 (in Turkish). 3. Özden, A., Bozdayı, G., Özkan, M., et al. (2004): Changes in the seroepidemiological pattern of Helicobacter pylori infection over the last 10 years in Turkey. Turk. J. Gastroenterol., 15, 156-158. 4. Tadege, T., Mengistu, Y., Desta, K., et al. (2005): Seroprevalence of Helicobacter pylori infection in and its relationship with ABO blood groups. Ethiop. J. Health Dev., 19, 55-59. 5. Tsai, C,J., Perry, S., Sanchez, L., et al. (2005): Helicobacter pylori infection in different generations of Hispanics in the San Francisco Bay area. Am. J. Epidemiol., 162, 351-357. 6. Brown, L.M., Thomas, T.L., Ma, J.L., et al. (2002): Helicobacter pylori infection in rural China: demographic, lifestyle and environmental factors. Int. J. Epidemiol., 31, 638-645. 7. Sninchi, K., Ishii, H., Imanishi, K., et al. (1997): Relationship of cigarette smoking, alcohol use and dietary habi Helicobacter pylori infection in Japanese men. Scand. J. Gastroenterol., 32, 651-655. 8. Nugalieva, Z.Z., Opekun, A.R. and Graham, D.Y. (2006): Problem of distinguishing false-positive tests from acute or transient Helicobacter pylori infections. Helicobacter, 11, 69-74. 9. Replogle, M.L., Glaser, S.L., Hiatt, R.A., et al. (1995): Biologic sex as a risk factor for Helicobacter pylori infection in healthy young adults. Am. J. Epidemiol.,142, 856-863. 10. Triantafyllopoulou, M., Carroll, M. and Li, B. (2006): Helicobacter pylori ınfections. Online at < http://www.emedicine.com/ped/topic938. htm>. Accessed 18 July 2007. 11. Kanbay, M., Gür, G., Arslan, H., et al. (2005): The relationship of ABO blood group, age, gender, smoking, and Helicobacter pylori infection.

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