- About this Journal ·
- Abstracting and Indexing ·
- Aims and Scope ·
- Article Processing Charges ·
- Articles in Press ·
- Author Guidelines ·
- Bibliographic Information ·
- Citations to this Journal ·
- Contact Information ·
- Editorial Board ·
- Editorial Workflow ·
- Free eTOC Alerts ·
- Publication Ethics ·
- Reviewers Acknowledgment ·
- Submit a Manuscript ·
- Subscription Information ·
- Table of Contents
Gastroenterology Research and Practice
Volume 2014 (2014), Article ID 481365, 10 pages
Risk Factors and Prevalence of Helicobacter pylori Infection in Persistent High Incidence Area of Gastric Carcinoma in Yangzhong City
1Department of Gastroenterology, People’s Hospital of Yangzhong County, Yangzhong 212200, China
2Department of Gastroenterology, The First Affiliated Hospital of Nanjing Medical University, Nanjing 210029, China
3Department of Gastroenterology, Shengze Hospital of Nanjing Medical University, Wujiang, Jiangsu, China
Received 20 September 2013; Accepted 5 December 2013; Published 14 January 2014
Academic Editor: D. Fan
Copyright © 2014 Yangchun Zhu et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Aim. The aim of this study was to investigate the prevalence and risk factors of H. pylori infection in areas with high prevalence of gastric cancer in Jiangsu Province, China. Methods. A prospective epidemiologic survey of H. pylori infection was accomplished in a natural population of 5417 individuals in Yangzhong city. Questionnaires and 13C-urea breath test for H. pylori infection were performed. Results. Among 5417 subjects who completed questionnaires and 13C-urea breath test, 3435 (63.41%) were H. pylori positive. The prevalence reached a peak at the age of 30–39 years (90.82%). There was significant difference between sexes and women had a higher infection rate than men. The prevalence of H. pylori infection was also associated with eating kipper food and fried food. No association between H. pylori prevalence and smoking or drinking was found. Compared to healthy individuals, people with dyspeptic diseases (peptic ulcer, gastroenteritis) presented a high prevalence of H. pylori infection. Using multivariate logistic regression analysis, age and history of peptic ulcer and gastroenteritis were the independent predictors for H. pylori infection. Conclusions. Yangzhong city had a high prevalence of H. pylori infection and was related to several risk factors. The underlying mechanisms are needed to be further investigated.
Helicobacter pylori is a microaerophilic Gram-negative spiral bacterium . Its helix shape is thought to have evolved to penetrate the mucoid lining of the stomach . It is linked to the development of chronic gastritis, gastric ulcers, duodenal ulcers, and stomach mucosal atrophy. Moreover, Helicobacter pylori is well recognized as a class I carcinogen because chronic inflammation and atrophy can further lead to malignant transformation [3, 4]. At least half the world’s population is infected by this bacterium, making it the most widespread infection in the world, especially in the developing world where rates are estimated to be around 80% .
H. pylori is contagious, although the exact route of transmission is not known [6, 7]. Person-to-person transmission by either the oral-oral or fecal-oral route is most likely. H. pylori may also be transmitted orally by means of fecal matter through the ingestion of waste-tainted water . Many of the reported factors for H. pylori infection included poor hygiene, deficient sanitation, and crowded living conditions . However, the roles of many other factors associated have not been elucidated.
The aim of the current study was to determine the prevalence of Helicobacter pylori in the census population in Yangzhong city of Jiangsu Province, where there is a high prevalence of gastric cancer, and to assess the risk factors for Helicobacter pylori by an extended anamnesis, involving data on sex, age, educational level, smoking, drinking, as well as dietary factors.
2.1. Study Population
A total of 5417 healthy individuals aged between 30 and 69 years old from six rural villages in Yangzhong counties, northern Jiangsu province, from August 2009 to October 2011 underwent a comprehensive medical survey at the Center for Preventive Medicine in Yangzhong hospital as part of a survey study. There are seven administrative sub-autonomous regions in Yangzhong city, 77 counties in total. We assigned a consecutive number from 1 to numbering counties of each region. Then we used a computer programme randomly chose one county from each region, except which population is significantly less than others.
All participants underwent a free screening program, including physical check-up, 13C breath test, upper gastrointestinal endoscopy, blood tests, and a doctor’s interview. The study protocol was approved by the Ethical Committee of the people’s Hospital of Yangzhong city. All participants received detailed written information about the study in advance and signed written informed consent before enrollment in the study.
2.2. Exclusion Criteria
The following individuals were excluded from our study: people taking medication for gastroesophageal reflux symptoms or malignant diseases; people with a history of Helicobacter pylori (H. pylori) eradication or upper gastrointestinal surgery. Individuals with gastric or esophageal cancer detected at the time of endoscopic screening were also excluded.
This was a population-based study. All participants had been trained before they fulfilled the questionnaires. Collected information included sex, age, height, weight, individual education level, size of family, annual family income, marital status, self-reported socioeconomic group, and smoking and drinking habits. Health status, medical history, and medications taken in the past 2 months (particularly the use of proton pump inhibitors and antibiotics) were also recorded. Each questionnaire contained a total of 57 questions possibly related to H. pylori infection and transmission.
2.4. Detection of H. pylori Infection
Subjects were diagnosed with H. pylori infection if 13C-urea breath test (13C-UBT) was positive. The 13C-UBT was performed in the morning after at least 6 hours of fasting. The system is comprised of the following components: (a) a kit containing 50 mg of 13C-urea (a 99% 13C-enriched urea tablet); (b) a packet of granulated Citrica (a 4.5 gram packet containing 4 g of citric acid, 0.149 mg of aspartame, orange aroma, FD&C yellow #6); (c) an IDcircuit-sampling device; and (d) a BreathID device. All patients received 50 mg of 13C-urea with a 4.5 gram citric acid based powder (Citrica). The IDcircuit, a continuous nasal breath sampling device, transported the breath sample from the patient to the BreathID and did not require active cooperation. All performances followed the instructions. Our cut-off value is 4%, and we considered the patients negative when the value was less than 4% and positive when the value was larger than 4%.
2.5. Statistical Analysis
The data were recorded and analyzed by using EPIDATA 3.1 by double-input. Stata 12.0 was used for all statistical analyses. Multivariate analyses were restricted to those subjects with all relevant data available. A test and Fisher’s exact test of independence were used to compare the following variables of interest: sex, age, educational level, height, weight, pulse, blood pressure, size of family, annual family income, smoking, drinking, and the history of gastroenterology diseases. All the reported values, are two-sided, and value < 0.05 was regarded as statistically significant for all included studies. Logistic regression was used to select significant predictor variables and to estimate odds ratios (ORs) of these variables and, if possible, to predict outcomes.
3.1. Prevalence of H. pylori Infection and Social Factors
Among 5500 subjects, 5417 completed both the questionnaire and the H. pylori detection test and were qualified for inclusion in data analysis. The mean age was 50.15 years old. There were 2342 men, whose average age was 50.27 years, and the rest were women, whose average age was 50.06 years. The overall prevalence of H. pylori was 63.41%. The prevalence of H. pylori among male and female was 61.74% and 64.47%, respectively, suggesting that there was a significant difference between sexes () and women had a higher infection rate than men. As shown in Table 1, 30–39 years had the highest rate of H. pylori infection than other age groups.
The prevalence of H. pylori in the group with one member only (69.23%) was higher than that in the group with other members, without statistical difference. As for the association of prevalence and annual family income, in the six groups (with an average level of RMB 35890.95, approximately $US 5000), we found that individuals with an annual family income of RMB >80000 had the lowest risk of H. pylori infection (58.79%), whereas those with annual family income of RMB5000 or less had the highest risk of H. pylori infection (71.72%), and there was a significant difference between the groups (). Moreover, our study showed that the higher annual family income was, the lower the prevalence of H. pylori, which is significant in test for trend (). As for the education level, H. pylori infection is higher in illiterate (70.08%) and those who received university education had the lowest H. pylori infection rate (62.58%). But there were no significant associations seen for the subjects’ level of education in general ().
Regarding the body mass index (BMI) value, healthy people (BMI = 18.5 to 24.9) had lowest H. pylori infection rate (62.28%) while those underweight (BMI < 18.5) people had highest infection rate (66.34%), but there was no significant difference between the groups.
There was no apparent association between the H. pylori infection and other social factors, such as marriage status ().
3.2. Relationships between H. pylori Infection and Dietary Factors, Smoking, and Drinking
The results suggest that H. pylori infection increased for subjects who ate vegetable more than once a day (65.71%), compared to those who ate it less than every other day (64.71%, ) and every other day to once a day (63.19% ), and there was no difference in for trend (), as shown in Table 2.
In contrast, the prevalence of H. pylori was highest in subjects who never ate fruits (67.70%), compared to the lowest infection rate in those who ate fruits less than every other day (63.35%, ), and there was no significant difference in for trend ().
Our study also showed that those who never ate milk, egg, or meat had 100% infection of H. pylori and people who ate less than every other day had the lowest infection rate (63.28%, ). People who ate pickled food less than every other day had the highest infection (66.77%), while those who never ate pickled food had the lowest infection rate (62.39%, ).
However, there was no apparent association between H. pylori infection and other dietary-related factors, such as beans consumption (), onion and garlic use (), eating fried foods (), and hot food ().
Table 3 shows that there was no association between the prevalence of H. pylori infection and the use of tobacco or alcohol (Table 3). But there was significant relationship observed between H. pylori infection and the amount of cigarettes which a person had been smoking per day. Our data showed that people smoking 1 to 10 cigarettes per day had significantly higher rate of H. pylori infection than people smoking 11 to 20 cigarettes ().
3.3. Relationships between H. pylori Infection and Upper Gastroduodenal Diseases
The prevalence of H. pylori infection in individuals with history of gastroenteral diseases (64.60%) was higher than those without a history of this disease (57.26%, ) (Table 4).
3.4. Logistic Regression Model Analysis for H. pylori Infection
Thirty-six variables possibly related to H. pylori infection were assessed by using univariate logistic regression models analysis. The prevalence of H. pylori infection had a positive correlation with gender (), kipple food (), frequency of eating pickled food (), frequency of eating fried foods (), and digestive diseases (), and negative correlation with factors of age (), gastroenteral inflammation () and peptic ulcer () (Table 5(a)).
These eight factors then were introduced in the multivariate logistic regression analysis. Factors ultimately into the main effects model were independent factors for H. pylori infection. They were age (), history of gastroenteritis (), and history of peptic ulcer () (Table 5(b)).
To our knowledge, the present study was the first to demonstrate risk factors of H. pylori infection in Yangzhong country. However, five years ago, Shi et al.  also conducted a clinical trial investigating the prevalence of H. pylori infection in different areas, and compared to this previous study, our study found that the prevalence of H. pylori remained a continuously high rate in recent 5 years in Jiangsu province and that there were different risk factors related to H. pylori infection. The prevalence and onset of H. pylori in the general population are not clear since asymptomatic healthy individuals usually do not undergo endoscopic examination. Considering the large sample size and adjusting for various potential confounders, we believe that the results of this study accurately represent the risk factors of H. pylori infection in Yangzhong population.
In the present study, we determined an overall prevalence and investigated the risk factors of H. pylori in Yangzhong country. The prevalence of H. pylori infection varies all over the world, with less than 40% prevalence in developed countries and more than 80%–90% in developing countries . The overall prevalence of H. pylori was 63.41% in Yangzhong city, similar to another previous study in Jiangsu Province by Shi et al. (62.07%) . Since Yangzhong country is a high epidemic area of gastric cancer and lots of previous studies demonstrated that H. pylori infection can lead to gastric cancer [11, 12], our study was of great clinical importance. Recently, more attention has been given to the risk factors of H. pylori infection, such as gender, age, and socioeconomic status, but the result has still been controversial [13, 14].
Yangzhong is a relatively enclosed country with limited population shifts. So the prevalence of H. pylori infection is in its natural status. Thus, we randomly selected six regions in this country for the present study.
4.1. Prevalence of H. pylori Infection and Social Factors
Malcolm et al.  reported that the H. pylori infection was associated with age, sex, and socioeconomic conditions. In a previous study , there was no relationship between H. pylori and gender, age in adults, but annual family income was an important risk factor. Ariizumi et al.  found that the H. pylori infection rate was associated with age, but there was no statistical difference between H. pylori infection with gender and BMI. In Dore et al. study , no statistical difference was observed between different socioeconomic groups and age groups.
In our study, significant difference was observed in gender, age, and annual family income. We suggested that female had a higher infection rate than male. The explanation for this difference can only be speculative at this moment, being most probably related to the hormonal differences between the two genders, as recent studies identified an important role of oxytocin in the gastric evacuation rate (GER) . Multivariate logistic regression model analysis also revealed that age was an important risk factor of H. pylori infection. The age group of 30–39 has shown a significant higher rate of H. pylori infection than other age groups. And the prevalence of H. pylori infection decreased with age. Previous studies showed that the infection rate was higher in childhood probably because people were usually infected with H. pylori when they were young . A lower prevalence rate of H. pylori infection in the elderly has also been reported by others and two hypotheses have been proposed to explain these findings: H. pylori could have been present in a small number or low activation which might not have been detected. And H. pylori could have been present in the past, but was eliminated on account of the development of an unfavorable gastric environment with age. At the mean time, there is a progressive gastric migration in a proximal direction. As for the annual household income, we found that the prevalence increased when it was less than RMB5000 and the higher it was, the lower the prevalence of H. pylori, which was consistent with other reports [20, 21]. This might be related to the better living and sanitary conditions, with separate bedrooms for children.
The risk factors for H. pylori infection also include more family members, lower education level, and abnormal BMI. We found that there was no statistical different between each group. Among these factors, higher educational level was slight but not significant decrease with the H. pylori infection, which may be explained by their difference kinds of occupation. We also found that normal body mass index had lowest infection rate and those underweight had the highest rate probably due to their decreased nutritional status and immunity.
4.2. Relationships between H. pylori Infection and Dietary Factors
H. pylori infection could also be related to food and eating habits . We investigated several dietary factors and found that eating kipper and fried food was positively associated with H. pylori infection. The consequence may be related to the way in which food is prepared, and dietary administration of salt may induce mucosal damage, such as diffuse erosion and degeneration, and destroy the mucosal barrier in the stomach. These changes in the gastric mucosa may be associated with an increased chance of persistent infection with H. pylori. Furthermore, salty food itself may be a source of H. pylori. The exact reason still needs to be further investigated.
4.3. Association between H. pylori and Drinking and Smoking
Two Japanese studies reported that smoking is negatively related to H. pylori infection [23, 24], but another study from Northern Ireland reported a positive relationship . Other studies [26–29] found no relationship between smoking and H. pylori infection.
In our study, there was no association between the prevalence of H. pylori infection and the use of tobacco. And no significant relationship was observed between H. pylori infection and the period of time over which a person had been smoking, consistent with our previous study . But in the present study, there was significant relationship observed between H. pylori infection and the amount of cigarettes smoked per day. Our data showed that people smoking 1 to 10 cigarettes per day had significantly higher rate of H. pylori infection than people smoking 11 to 20 cigarettes (), suggesting that the risk of H. pylori infection decreased with cigarette consumption per day.
The observed association of smoking with active H. pylori infection may result from various mechanisms with partly antagonistic effects on the risk of infection. Potentially relevant effects of smoking include an increase in acid and pepsin secretion and changes in gastric motility, prostaglandin synthesis, gastric mucosal blood flow, and mucus secretion .
As for drinking, our study showed that those who never drank beer had slightly higher rate of H. pylori infection than people who consumed mild and moderate beverage. Meanwhile, people never drinking wine had lower incidence of H. pylori infection. However, the difference has no significance.
Several previous studies have found the relation between Helicobacter pylori infection and alcohol consumption. Most of them did not find a significant association [31–35]. Interestingly, Brenner et al.  suggested a major protective effect of alcohol at moderate and high consumption but not at low consumption. Alcoholic beverages may directly and indirectly affect gastric mucosa, gastric acid secretion , and gastric emptying , leading to living condition changes of H. pylori in the stomach. In particular, moderate alcohol consumption might invigorate mucosal defense by its effects on prostaglandins . Last, alcoholic beverages are known to have strong direct antibacterial activity [40–42].
But our study showed that there was no association between the prevalence of H. pylori infection and the use of alcohol, due to small sample size and heterogeneity between different groups. Besides consumption beverage, we also addressed other more details such as the type of alcoholic consumed and history of alcohol consumption. However there was no significant founding. Further studies involving larger numbers of subjects and multicenters should address more detailed additional factors and potential interactions between alcohol consumption and other factors that might affect active H. pylori infection.
4.4. Relationships between H. pylori Infection and Digestive Diseases
Shi et al.  found that there was no association between H. pylori infection and histories of upper gastrointestinal diseases. However, our present study showed that there was no association between H. pylori infection and hepatitis and esophagitis, but a positive correlation was found between peptic ulcer and gastroenteritis. The data were confirmed by multivariate logistic regression analysis.
H. pylori is motile, even in the highly viscous mucus layer. This may allow the organisms to evade both gastric motility and peristalsis, and also to some extent gastric acidity. Although it is motile, it also may adhere to the gastric mucosa through specific adhesion mechanisms. The secretion of large amounts of urease results in any urea in the environment being converted into ammonia-with the result that the intense acidity of the stomach may be ameliorated in the microenvironment surrounding the bacterium.
About 50% of H. pylori strains produce cytotoxins, of which some have been specifically linked to active gastritis and peptic ulceration. These cytotoxins can cause local inflammation, though other secretions by the organism, such as proteases and phospholipases, can attack and damage mucosal cell membranes. Weakening the gastric-mucosal barrier permits back-diffusion of hydrogen ions resulting in further tissue injury, as well as causing local immune responses to the organism.
In conclusion, the prevalence of H. pylori infection was 63.41% in the populations of Yangzhong country, Jiangsu province, which is also a region of high-risk gastric cancer in China. The prevalence of H. pylori infection was linked to sex, age, kipper food, frequency of eating kipper foods and fried food, peptic ulcer, and gastroenteritis. The relationship between H. pylori infection and other risk factors, such as upper gastrointestinal symptoms and some health habits, is still to be investigated.
Yangchun Zhu, Xiaoying Zhou, and Junbei Wu contributed equally to this paper.
Conflict of Interests
The authors declare that there is no conflict of interests regarding the publication of this paper.
The authors would like to thank the National Natural Science Funds of China and Key Projects in the National Science & Technology Pillar Program during the Eleventh Five-year Plan Period for providing funds for our study. This work was supported by the National Natural Science Funds of China (nos. 81072032 and 81270476) and Key Projects in the National Science & Technology Pillar Program during the Eleventh Five-year Plan Period (2006BAI02A05).
- K. W. Tsang, W. K. Lam, K. N. Chan et al., “Helicobacter pylori sero-prevalence in asthma,” Respiratory Medicine, vol. 94, no. 8, pp. 756–759, 2000.
- L. M. Brown, “Helicobacter pylori: epidemiology and routes of transmission,” Epidemiologic Reviews, vol. 22, no. 2, pp. 283–297, 2000.
- P. Correa, “Human gastric carcinogenesis: a multistep and multifactorial process—first American Cancer Society Award lecture on cancer epidemiology and prevention,” Cancer Research, vol. 52, no. 24, pp. 6735–6740, 1992.
- J. G. Fox and T. C. Wang, “Inflammation, atrophy, and gastric cancer,” Journal of Clinical Investigation, vol. 117, no. 1, pp. 60–69, 2007.
- J. Torres, Y. Leal-Herrera, G. Perez-Perez et al., “A community-based seroepidemiologic study of Helicobacter pylori infection in Mexico,” Journal of Infectious Diseases, vol. 178, no. 4, pp. 1089–1094, 1998.
- F. Megraud, “Transmission of Helicobacter pylori: faecal-oral versus oral-oral route,” Alimentary Pharmacology and Therapeutics, vol. 9, supplement 2, pp. 85–91, 1995.
- D. R. Cave, “Transmission and epidemiology of Helicobacter pylori,” American Journal of Medicine, vol. 100, pp. 12S–17S, 1996.
- V. C. C. Dattoli, R. V. Veiga, S. S. Da Cunha, L. C. Pontes-De-Carvalho, M. L. Barreto, and N. M. Alcântara-Neves, “Seroprevalence and potential risk factors for Helicobacter pylori infection in Brazilian children,” Helicobacter, vol. 15, no. 4, pp. 273–278, 2010.
- R. Shi, S. Xu, H. Zhang et al., “Prevalence and risk factors for Helicobacter pylori infection in chinese populations,” Helicobacter, vol. 13, no. 2, pp. 157–165, 2008.
- L. Zhang, W. J. Blot, W.-C. You et al., “Helicobacter pylori antibodies in relation to precancerous gastric lesions in a high-risk Chinese population,” Cancer Epidemiology Biomarkers and Prevention, vol. 5, no. 8, pp. 627–630, 1996.
- T. De Sablet, M. B. Piazuelo, C. L. Shaffer et al., “Phylogeographic origin of Helicobacter pylori is a determinant of gastric cancer risk,” Gut, vol. 60, no. 9, pp. 1189–1195, 2011.
- N. Kim, R. Y. Park, S.-I. Cho et al., “Helicobacter pylori infection and development of gastric cancer in Korea: long-term follow-up,” Journal of Clinical Gastroenterology, vol. 42, no. 5, pp. 448–454, 2008.
- A. Kurzeja-Mirosław, K. Celiński, M. Słomka, A. Madro, and H. Cichoz-Lach, “The effects of environmental factors on the incidence of Helicobacter pylori infection in the adult population of the Lublin region,” Annales Universitatis Mariae Curie-Sklodowska. Sectio D, vol. 59, no. 2, pp. 247–253, 2004.
- G. I. Perez-Perez, D. Rothenbacher, and H. Brenner, “Epidemiology of Helicobacter pylori infection,” Helicobacter, vol. 9, supplement 1, pp. 1–6, 2004.
- C. A. Malcolm, W. G. MacKay, A. Shepherd, and L. T. Weaver, “Helicobacter pylori in children is strongly associated with poverty,” Scottish Medical Journal, vol. 49, no. 4, pp. 136–138, 2004.
- K. Ariizumi, T. Koike, S. Ohara et al., “Incidence of reflux esophagitis and Helicobacter pylori infection in diabetic patients,” World Journal of Gastroenterology, vol. 14, no. 20, pp. 3212–3217, 2008.
- M. P. Dore, M. Bilotta, H. M. Malaty et al., “Diabetes mellitus and Helicobacter pylori infection,” Nutrition, vol. 16, no. 6, pp. 407–410, 2000.
- J. Borg, O. Melander, L. Johansson, K. Uvnäs-Moberg, J. F. Rehfeld, and B. Ohlsson, “Gastroparesis is associated with oxytocin deficiency, oesophageal dysmotility with hyperCCKemia, and autonomic neuropathy with hypergastrinemia,” BMC Gastroenterology, vol. 9, article 17, 2009.
- R. E. Pounder and D. Ng, “The prevalence of Helicobacter pylori infection in different countries,” Alimentary Pharmacology and Therapeutics, vol. 9, supplement 2, pp. 33–39, 1995.
- C. Bodner, W. J. Andersen, T. S. Reid, and D. J. Godden, “Childhood exposure to infection and risk of adult onset wheeze and atopy,” Thorax, vol. 55, no. 5, pp. 383–387, 2000.
- B. D. Aguemon, M. J. Struelens, A. Massougbodji, and E. M. Ouendo, “Prevalence and risk-factors for Helicobacter pylori infection in urban and rural Beninese populations,” Clinical Microbiology and Infection, vol. 11, no. 8, pp. 611–617, 2005.
- S. Tsugane, “Salt, salted food intake, and risk of gastric cancer: epidemiologic evidence,” Cancer Science, vol. 96, no. 1, pp. 1–6, 2005.
- S. Kikuchi, M. Kurosawa, and T. Sakiyama, “Helicobacter pylori risk associated with sibship size and family history of gastric diseases in Japanese adults,” Japanese Journal of Cancer Research, vol. 89, no. 11, pp. 1109–1112, 1998.
- A. Ogihara, S. Kikuchi, A. Hasegawa et al., “Relationship between Helicobacter pylori infection and smoking and drinking habits,” Journal of Gastroenterology and Hepatology, vol. 15, no. 3, pp. 271–276, 2000.
- L. J. Murray, E. E. McCrum, A. E. Evans, and K. B. Bamford, “Epidemiology of Helicobacter pylori infection among 4742 randomly selected subjects from Northern Ireland,” International Journal of Epidemiology, vol. 26, no. 4, pp. 880–887, 1997.
- S. Tsugane, Y. Tei, T. Takahashi, S. Watanabe, and K. Sugano, “Salty food intake and risk of Helicobacter pylori infection,” Japanese Journal of Cancer Research, vol. 85, no. 5, pp. 474–478, 1994.
- K. Shinchi, H. Ishii, K. Imanishi, and S. Kono, “Relationship of cigarette smoking, alcohol use, and dietary habits with Helicobacter priori infection in japanese men,” Scandinavian Journal of Gastroenterology, vol. 32, no. 7, pp. 651–655, 1997.
- G. Battaglia, F. Di Mario, M. Pasini et al., “Helicobacter pylori infection, cigarette smoking and alcohol consumption. a histological and clinical study on 286 subjects,” Italian Journal of Gastroenterology, vol. 25, no. 8, pp. 419–424, 1993.
- C. Zhong, K.-N. Li, J.-W. Bi, and B.-C. Wang, “Sodium intake, salt taste and gastric cancer risk according to Helicobacter pylori infection, smoking, histological type and tumor site in China,” Asian Pacific Journal of Cancer Prevention, vol. 13, no. 6, pp. 2481–2484, 2012.
- K. Endoh and F. W. Leung, “Effects of smoking and nicotine on the gastric mucosa: a review of clinical and experimental evidence,” Gastroenterology, vol. 107, no. 3, pp. 864–878, 1994.
- D. Forman, M. Coleman, G. De Backer et al., “Epidemiology of, and risk factors for, Helicobacter pylori infection among 3194 asymptomatic subjects in 17 populations,” Gut, vol. 34, no. 12, pp. 1672–1676, 1993.
- D. Y. Graham, H. M. Malaty, D. G. Evans, D. J. Evans Jr., P. D. Klein, and E. Adam, “Epidemiology of Helicobacter pylori in an asymptomatic population in the United States: effect of age, race, and socioeconomic status,” Gastroenterology, vol. 100, no. 6, pp. 1495–1501, 1991.
- M. Paunio, J. Hook-Nikanne, T. U. Kosunen et al., “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,” European Journal of Epidemiology, vol. 10, no. 2, pp. 205–209, 1994.
- E. T. H. Fontham, B. Ruiz, A. Perez, F. Hunter, and P. Correa, “Determinants of Helicobacter pylori infection and chronic gastritis,” American Journal of Gastroenterology, vol. 90, no. 7, pp. 1094–1101, 1995.
- T. Rokkas, C. Pursey, E. Uzoechina et al., “Campylobacter pylori and non-ulcer dyspepsia,” American Journal of Gastroenterology, vol. 82, no. 11, pp. 1149–1152, 1987.
- H. Brenner, D. Rothenbacher, G. Bode, and G. Adler, “Relation of smoking and alcohol and coffee consumption to active Helicobacter pyloli infection: cross sectional study,” British Medical Journal, vol. 315, no. 7121, pp. 1489–1492, 1997.
- A. Franke, H. Harder, A. K. Orth, S. Zitzmann, and M. V. Singer, “Postprandial walking but not consumption of alcoholic digestifs or espresso accelerates gastric emptying in healthy volunteers,” Journal of Gastrointestinal and Liver Diseases, vol. 17, no. 1, pp. 27–31, 2008.
- M. V. Singer, C. Leffmann, V. E. Eysselein, H. Calden, and H. Goebell, “Action of ethanol and some alcoholic beverages on gastric acid secretion and release of gastrin in humans,” Gastroenterology, vol. 93, no. 6, pp. 1247–1254, 1987.
- A. Robert, J. E. Nezamis, C. Lancaster, J. P. Davis, S. O. Field, and A. J. Hanchar, “Mild irritants prevent gastric necrosis through “adaptive cytoprotection” mediated by prostaglandins,” The American Journal of Physiology, vol. 245, no. 1, pp. G113–G121, 1983.
- L. O. Ingram and T. M. Buttke, “Effects of alcohols on micro-organisms,” Advances in Microbial Physiology, vol. 25, pp. 253–300, 1985.
- W. L. Peterson, P. A. Mackowiak, C. C. Barnett, M. Marling-Cason, and M. L. Haley, “The human gastric bactericidal barrier: mechanisms of action, relative antibacterial activity, and dietary influences,” Journal of Infectious Diseases, vol. 159, no. 5, pp. 979–983, 1989.
- M. E. Weisse, B. Eberly, and D. A. Person, “Wine as a digestive aid: comparative antimicrobial effects of bismuth salicylate and red and white wine,” British Medical Journal, vol. 311, no. 7021, pp. 1657–1660, 1995.