Does waterpipe smoking increase the risk of Helicobacter pylori infection?
Özgür Sirkeci1, Emel Erkus Sirkeci2, Turgay Ulas3
1 Department of Gastroenterology, Faculty of Medicine, Süleyman Demirel University, Isparta, Turkey
2 Department of Emergency, Faculty of Medicine, Near East University, Nicosia, Northern Cyprus
3 Department of Hematology, Faculty of Medicine, Near East University, Nicosia, Northern Cyprus
|Date of Submission||20-Jun-2019|
|Date of Decision||26-Nov-2019|
|Date of Acceptance||21-Mar-2021|
|Date of Web Publication||29-Jan-2022|
Dr. Özgür Sirkeci
Department of Internal Medicine, Faculty of Medicine, Near East University Hospital, Near East University, Nicosia
Source of Support: None, Conflict of Interest: None
Background: In this study, we aimed to evaluate whether waterpipe smoking can be associated with the transmission of Helicobacter pylori infection or not. Materials and Methods: Between March 2018 and April 2019, 445 patients aged over 18 years old who were admitted to outpatient clinics with dyspeptic complaints were recruited for the study. Patients are divided into two groups – Group 1 is H. pylori-positive patients and Group 2 is negative. Waterpipe smoking, smoking, age, gender, and educational status were compared among groups. Results: Two hundred and sixty-one women (58%) and 184 men (42%), totally 445 patients, tested for H. pylori infection. Seventy-nine of 261 (30%) women and 60 of 184 (32%) men had H. pylori positive. One hundred and sixty-two of 445 (36%) patients were smoking cigarette and 66 of 445 (14%) patients were using waterpipe tobacco. Waterpipe smoking individuals were found to be associated with the H. pylori positivity (P < 0.001); whereas, age, gender, educational level, and smoking were not found to be statistically significant (all P > 0.05). In binary logistic regression analysis, waterpipe tobacco smoking was found to be the only independent predictor of H. pylori infection (P < 0.001, odds ratio = 5.51, confidence interval: 3.158–9.617). Conclusion: Waterpipe smoking seems to be an important risk factor for H. pylori infection and may be one of the reasons of high prevalence of H. pylori infection.
Keywords: Helicobacter pylori, infection, waterpipe smoking
|How to cite this article:|
Sirkeci Ö, Sirkeci EE, Ulas T. Does waterpipe smoking increase the risk of Helicobacter pylori infection?. J Res Med Sci 2022;27:7
| Introduction|| |
Helicobacter pylori is the main cause of gastric ulcer, duodenal ulcer, and nonulcer dyspepsia and is an important risk factor for stomach cancer.,, Worldwide, more than 50% of the population is infected with H. pylori and more common in developing countries. Low socioeconomic level, poor hygiene conditions, and overcrowded are the risk factors. Although transmission route of the H. pylori is still not clear, interpersonal, especially in the family, seems to be the main route.,,
Smoking, and also waterpipe smoking, is a common method of tobacco use in southwest Asia and northern Africa. In recent years, its popularity has increased and usage has become widespread in Europe and America, carries the same risks as smoking.,, The prevalence of respiratory diseases, lung cancer, cardiovascular diseases, and metabolic syndrome is increased in waterpipe smoking. In addition, impairment in oral hygiene and high incidence of periodontal disease are common outcomes of water pipe smoking. Infectious disease such as hepatitis C virus infection has also increased.,, Although the relationship between H. pylori and smoking has been evaluated in many studies, no study has been conducted to evaluate the relationship between H. pylori and waterpipe smoking. Therefore, we have designed this study whether waterpipe smoking can be associated with the transmission of H. pylori or not.
| Methods|| |
This cross-sectional study was conducted at Internal Medicine Department of Near East University Hospital, Nicosia, Cyprus. Local ethics committee reviewed and approved the study protocol in accordance with the ethical principles for human investigations. Written informed consents were obtained from all the patients.
Between March 2018 and April 2019, 445 patients aged over 18 years old who were admitted to outpatient clinics with dyspeptic complaints and who had no exclusion criteria were recruited to the study. The exclusion criteria were as follows: no history of upper gastrointestinal disease, bleeding, and surgery; patients who had received antibiotics, proton pump inhibitors, or antacids in the previous 4 weeks; history of eradication therapy for H. pylori; patients requiring upper endoscopy as defined in the American College of Gastroenterology dyspepsia guideline; patients using nonsteroidal anti-inflammatory agents frequently; and history of any other concomitant diseases such as acute and chronic inflammatory conditions, rheumatic diseases, malignancies, diabetes mellitus, hypertension, kidney disease, and liver disease.
We excluded patients with alarm symptoms, and therefore, patients require upper endoscopy, even if they were also H. pylori positive. We also evaluated H. pylori-negative patients for other causes of dyspepsia step by step; we considered patients with functional dyspepsia for whom we could not find a meaningful cause.
Patient's age, gender, education level, using water pipe or not, and smoking are questioned and are noted. Those who use water pipe smoking in the past 1 month, at least once a week, are considered to waterpipe smoker. Dyspepsia was defined as per Rome III diagnostic criteria, as the presence of one or more dyspepsia symptoms such as postprandial fullness, early satiation, epigastric pain, and epigastric burning that are considered to originate from the gastroduodenal region and in the absence of any organic, systemic, or metabolic disease that is likely to explain the symptoms. Stool antigen test or urea breath test was applied to patients with dyspeptic complaints.
Stool samples were collected from the patients, and quantitative ELISA for H. pylori antigen was performed on the stool samples as per the manufacturer's instructions. Samples showing a concentration of H. pylori antigen higher than 0.05 μg/ml were considered as positive. Carbon-14 urea breath test after an overnight fast, C-14 UBT (Heliprobe System, Kibion AB, Uppsala, Sweden), was performed for all enrolled patients. After ingestion of 37 kBq (1 lCi) C-14 urea capsule with 50 mL water, the breath samples were collected at 10th, 20th, and 30th min after ingestion. During this 30-min C-14 UBT urea reaction period, patients lay on the left side horizontally. The results were expressed as both counts per minute (CPM), and grading (0–1 [negative for H. pylori infection, CPM B (50)) and 2 [positive for H. pylori infection, CPM (50)]) as suggested by the manufacturer.
Education levels were divided into four groups: secondary school graduates, junior high school graduates, high school graduates, and university graduates.
All statistical analysis was performed using SPSS for Windows version 24 (SPSS, Inc., Chicago, IL, USA). Chi-square test was used to examine the association of H. pylori-infected patients with categorical variables including water pipe smoking, smoking, sex, and educational level. Statistical difference of the numerical variable, age was performed using independent sample t-test. Binary logistic regression analysis was performed to determine independent predictors of H. pylori infection. A two-sided P > 0.05 was considered statistically significant.
| Results|| |
The clinical and demographic characteristics groups are presented in [Table 1]. During the study, 261 women (58%) and 184 men (42%) totally 445 patients tested for H. pylori infection. Seventy-nine of 261 (30%) women and 60 of 184 (32%) men had H. pylori positive. One hundred and sixty-two of 445 (36%) patients were smoking cigarette and 66 of 445 (14%) patients were using water pipe tobacco. Group ages were found to be statistically similar (P > 0.05). In Chi-square test, water pipe smoking individuals were found to be associated with the H. pylori positivity (P < 0.001); whereas, gender, educational level, and smoking were not found to be statistically significant (all P > 0.05). In binary logistic regression analysis, age, education level, and cigarette smoking were not found to be the predictors for H. pylori infection (all P > 0.05); whereas, only waterpipe tobacco smoking was found to be the only independent predictor of H. pylori infection (P < 0.001, odds ratio = 5.51, confidence interval: 3.158–9.617).
| Discussion|| |
To the best of our knowledge, this is the first study evaluating the association between H. pylori infection and waterpipe tobacco smoking. The main findings of the study were that (i) waterpipe smoking is associated with the H. pylori positivity (ii) and were found to be the independent predictor of H. pylori infection.
Many studies have been conducted concerning the possible relation H. pylori and smoking. This previous study results were conflicting. In the majority of them, no relation of cigarette smoking with H. pylori was found.,,, However, in some studies, positively and negatively relation was found. In our study, we found no relation between smoking habit and H. pylori infection. However, we did not classify patients according to their smoking duration and number of cigarettes smoked per day. Duration and frequency of cigarette smoking may have effects on H. pylori infection development. This may have affected our findings between smoking and H. pylori infection.
Water pipe smoking has the same and also more risks with cigarette smoking. There are many different types of water pipes; the basic version most frequently used has four main parts: the bowl where the tobacco is heated; the base filled with water or other liquids; the pipe, which connects the bowl to the base; and the hose and mouthpiece through which smoke is drawn. The specialty tobacco is heated, usually with burning embers or charcoal. The smoke passes through the water and is then drawn through the hose to the mouthpiece. Mouthpiece changes at every use but the other parts not. Hence, this structure may be facilitating factor for infection transmission.
Arabic type water pipe is used in our region. However, there are many types of waterpipe tobacco smoking with different structures. Different types of water pipes will have different harmful effects on human health. Lai et al. in a study among Vietnamese men showed that smoking waterpipe tobacco increases the risk of gastric cancer. Vietnamese type waterpipe tobacco does not include charcoal but Arabic type needs charcoal. This means more toxic effects on human health. Not only H. pylori transmission but also additional toxic effects may cause more complications such as cancer and ulcer.
The way of H. pylori transmission is unclear. Interpersonal transmission seems to be the main route, but environmental and parental ways are the other main reasons. Transmission events between individuals living in the same house are more frequent. Urita et al. investigated intrafamilial transmission of H. pylori and reported the mother-to-child and also grandmother-to-child transmission. They stated that mothers could transmit the infection through mouth secretions, using common spoons or tasting the child's food. Water pipe smoking may be responsible for H. pylori transmission in a similar way. Infected smoker may spread the bacteria into water pipe, and changing the mouthpiece may not be enough. With this hypothesis, we evaluated the water pipe smoking and H. pylori infection and found a strong relationship between water pipe smoking and H. pylori infection.
We have not found relationship between H. pylori and gender, but in a recent meta-analysis, male sex was associated with a greater prevalence of H. pylori infection both in children and adults. We also have not found a significant relationship between H. pylori and educational level although in previous studies low educational level has been found as a risk factor. The study was done in a university hospital, and the hospital is located in university campus so many of our patients were university students, we think that this was the reason why we did not found a relationship between educational level and H. pylori infection.
| Conclusion|| |
In conclusion, waterpipe smoking seems to be important risk factor for H. pylori infection and may be one of the reasons of high prevalence of H. pylori infection. The prevalence of H. pylori is so high in Southeast Mediterranean and Middle East countries where the waterpipe smoking commonly used.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Sachs G, Scott DR, Wen Y. Gastric infection by Helicobacter pylori
. Curr Gastroenterol Rep 2011;13:540-6.
Aydogan T, Ulas T, Selcoki Y, Alkan R, Yılmaz OC, Yalcın KS, et al
. Effects of Helicobacter pylori
eradication on proteinuria: A prospective study. Wien Klin Wochenschr 2012;124:241-4.
Hacibekiroglu T, Basturk A, Akinci S, Bakanay SM, Ulas T, Guney T, et al
. Evaluation of serum levels of zinc, copper, and Helicobacter pylori
IgG and IgA in iron deficiency anemia cases. Eur Rev Med Pharmacol Sci 2015;19:4835-40.
Mohammadi M, Ghaleiha A, Rahnama R. Effectiveness of a peer-led behavioral intervention program on tobacco use-related knowledge, attitude, normative beliefs, and intention to smoke among adolescents at Iranian public high schools. Int J Prev Med 2019;10:111.
Zhong C, Li KN, Bi JW, Wang BC. Sodium intake, salt taste and gastric cancer risk according to Helicobacter pylori
infection, smoking, histological type and tumor site in China. Asian Pac J Cancer Prev 2012;13:2481-4.
Urita Y, Watanabe T, Kawagoe N, Takemoto I, Tanaka H, Kijima S, et al
. Role of infected grandmothers in transmission of Helicobacter pylori
to children in a Japanese rural town. J Paediatr Child Health 2013;49:394-8.
Cobb C, Ward KD, Maziak W, Shihadeh AL, Eissenberg T. Waterpipe tobacco smoking: An emerging health crisis in the United States. Am J Health Behav 2010;34:275-85.
Akl EA, Gaddam S, Gunukula SK, Honeine R, Jaoude PA, Irani J. The effects of waterpipe tobacco smoking on health outcomes: A systematic review. Int J Epidemiol 2010;39:834-57.
Mohammadpoorasl A, Bahari A, Marin S, Hajizadeh M. Obscenity of cigarette and hookah smoking in Iranian adolescents: A longitudinal school-based study. Int J Prev Med 2019;10:47.
] [Full text]
Shafique K, Mirza SS, Mughal MK, Arain ZI, Khan NA, Tareen MF, et al
. Water-pipe smoking and metabolic syndrome: A population-based study. PLoS One 2012;7:e39734.
Tsugane S, Tei Y, Takahashi T, Watanabe S, Sugano K. Salty food intake and risk of Helicobacter pylori
infection. Jpn J Cancer Res 1994;85:474-8.
Shinchi K, Ishii H, Imanishi K, Kono S. Relationship of cigarette smoking, alcohol use, and dietary habits with Helicobacter pylori
infection in Japanese men. Scand J Gastroenterol 1997;32:651-5.
Triantafillidis JK, Papatheodorou K, Kogevinas M, Manoussakis K, Nicolakis D. Prognostic factors affecting the survival of operated patients with colorectal cancer: Significance of delayed hypersensitivity skin reactions and nutritional status. Ital J Gastroenterol 1995;27:419-24.
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;315:1489-92.
An international association between Helicobacter pylori
infection and gastric cancer. The EUROGAST Study Group. Lancet 1993;341:1359-62.
Rayens MK, Ickes MJ, Butler KM, Wiggins AT, Anderson DG, Hahn EJ. University students' perceived risk of and intention to use waterpipe tobacco. Health Educ Res 2017;32:306-17.
Lai HT, Koriyama C, Tokudome S, Tran HH, Tran LT, Nandakumar A, et al
. Waterpipe tobacco smoking and gastric cancer risk among Vietnamese men. PLoS One 2016;11:e0165587.
Ibrahim A, Morais S, Ferro A, Lunet N, Peleteiro B. Sex-differences in the prevalence of Helicobacter pylori
infection in pediatric and adult populations: Systematic review and meta-analysis of 244 studies. Dig Liver Dis 2017;49:742-9.
Graham DY, Malaty HM, Evans DG, Evans DJ Jr., Klein PD, Adam E. Epidemiology of Helicobacter pylori
in an asymptomatic population in the United States. Effect of age, race, and socioeconomic status. Gastroenterology 1991;100:1495-501.