alexa Epidemiology of Helicobacter pylori Infection among Symptomatic Patients, Correlation with Endoscopic Findings and itand#8217;s Association with Type II Diabetes Mellitus
ISSN: 2161-069X
Journal of Gastrointestinal & Digestive System

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Epidemiology of Helicobacter pylori Infection among Symptomatic Patients, Correlation with Endoscopic Findings and it’s Association with Type II Diabetes Mellitus

Antoine Abi Abboud* and Walid Abdel Khalek

Medicine Division of Gastroenterology, Faculty of Medical Sciences, Lebanese University, Lebanon

*Corresponding Author:
Antoine Abi Abboud
Medicine Division of Gastroenterology, Faculty of Medical Sciences
Lebanese University, Lebanon
Tel: 9613220520
E-mail: [email protected]

Received date: May 08, 2017; Accepted date: May 29, 2017; Published date: June 05, 2017

Citation: Abboud AA, Khalek WA (2017) Epidemiology of Helicobacter pylori Infection among Symptomatic Patients, Correlation with Endoscopic Findings and it’s Association with Type II Diabetes Mellitus. J Gastroint Dig Syst 7:508. doi:10.4172/2161-069X.1000508

Copyright: © 2017 Abboud AA, et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

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Background: Helicobacter pylori (H. pylori) is an important global pathogen infecting approximately 50% of the world’s population. This study was undertaken in order to estimate the prevalence of Helicobacter pylori infections among symptomatic patients in Lebanese Hospital Geitaoui University Medical Center (HLG-CHU) and Middle East Institute of Health (MEIH), to investigate the associated risk factors, the endoscopic findings and its association with type 2 diabetes.

Method: This is an observational analytic case-control study, carried out over a period of 6 months, from January 2016 till June 2016, including all patients complaining of upper gastrointestinal (GI) symptoms. The patients (n=226) were enrolled following same protocol in both the hospitals. All subjects completed a validated questionnaire and underwent upper GI endoscopy. The histo-pathological diagnosis of H. pylori infection in biopsy specimen was done using the modified Giemsa stain. H. Pylori prevalence and associated factors were analysed by Students t-test, Chisquare test and Fisher exact test. Statistical analysis was performed using the statistical program SPSS version 22.

Results: The overall prevalence was 38.9% with no difference between sexes. There was no association with age, residential region, alcohol and caffeine use and smoking. Low level of education and non-steroidal anti-inflammatory (NSAIDs) use were the only significant factors. Bloating, nausea and early satiety were significant predictors of H. pylori infection. The most commonly identified endoscopic finding was gastritis (78.3%), only duodenitis and oesophagitis were significantly associated with H. pylori. Prevalence of H. pylori was 38.8% and 39%, respectively, in patients with diabetes and having no diabetes.

Conclusion: H. Pylori prevalence was found to be high. Individuals who had low educational level and NSAIDs consumers, were under higher risk of infection than others. H. pylori infection appears not to be associated with diabetes.


Helicobacter pylori infection; Endoscopic findings; Type 2 diabetes mellitus


Helicobacter pylori (H. pylori) is a gram negative, non-spore forming spiral bacterium which colonizes the human stomach and is prevalent worldwide. Since its discovery in the 1980s, much has been learned about this bacterium and its associated disease states. In 1994, the National Institute of Health Consensus Conference, recognized H. pylori as a cause of gastric and duodenal ulcers. Later that year, the International Agency for Research on Cancer declared H. pylori to be a group I human carcinogen for gastric adenocarcinoma. There is also evidence that H. pylori infection is a risk factor for gastric mucosa-associated lymphomas (MALT lymphomas). Furthermore, the organism is thought to be involved in other human illnesses such as hematologic, autoimmune disorders, insulin resistance and the metabolic syndrome [1,2]. High rates of H. pylori infection are associated with low socioeconomic status and educational levels.

Evidence has recently been published suggesting that the prevalence of H. pylori infection might be increased in diabetic patients and in obese patients with an impaired glucose tolerance as opposed to normal population. It was hypothesized that alterations in glucose metabolism may have a role in promoting H. pylori colonization due to chemical changes in the gastric mucosa. Another explanation may be that the immune status in diabetic patients, which is strongly compromised, may lead to an increased susceptibility to H. pylori infection [3]. However, the link between H. pylori infection and diabetes remains controversial, as some studies indicate a higher prevalence of infection in diabetic patients, [4-8], while others report no difference [9-12].

Since, in the current literature, there is no comprehensive review representing an evidence-based knowledge on the prevalence of H. Pylori infection and its potential associations with dyspeptic symptoms in the Middle Eastern countries [12-16] and in Lebanon [17-19]; and on the association of H. pylori and diabetes mellitus [19] we conducted this study aiming to determine the prevalence of H. pylori infection by using gastric biopsy detection in symptomatic patients, to examine potential risk factors that may influence the acquisition of H. pylori infection, and its possible association with diabetes.

Methodological Approach


All patients during the study period complaining of upper gastrointestinal symptoms (dyspepsia, epigastric pain, heart burn, hematemesis dysphagia, nausea, vomiting, anorexia, early satiety, weight loss, melena, bloating) for more than one month presenting for upper GI endoscopy were recruited consecutively upon signing a written informed consent.

Exclusion criteria were:

a) Patients of type-1 diabetes

b) Non-cooperative patients who refuse to give consent or participate in the study

c) Patients on H. pylori eradication therapy.

d) Patients who had used antibiotics during the preceding 30 days.

e) Patients with a history of vagotomy or operations on the upper gastrointestinal tract.

f) Patients with endoscopic diagnosis of gastric cancer proven by histopathological examination.


Study design

This is a prospective observational analytic case-control study, including n=226 patients carried out in two hospitals; HLG-CHU & MEIH over a period of 6 months, from January 2016 till June 2016.

Data collection

The study protocol was reviewed and approved by the local ethics committee, and signed informed consents were obtained from each participant. All enrolled subjects were interviewed, by means of a structured questionnaire, to obtain general demographic details and to gather information regarding recent use of drugs and their medical history.

Data analysis

Data was collected retrospectively from 226 patients who underwent gastric biopsy. Data collection was conducted through paper CRFs that was provided to each investigational site for the collection of all study data for enrolled patients. Data validation was performed by the execution of programmed and manual edit checks in order to control any erroneous, ambiguous or incomplete data.

Statistical analysis was performed using the statistical program SPSS version 22. Descriptive analysis of qualitative variables comprised the sample size, the frequencies and the percentages. Descriptive analysis of quantitative variables included the number, the mean, and the standard deviation. A statistical significant relation exists if p-value is less than 5% using α error equal to 5%. Tests used for the analytical analysis were Chi-square test, Fisher exact test, and Students t-test.


Among the 226 enrolled patients, 88 (38.9%) were positive for H. pylori infection: 40 males (54.54%) and 48 females (45.45%). The remaining 138 patients that were found negative for H. pylori infection. There were 60 males (43.47%) and 78 females (56.53%) among them as shown in (Table 1).

 Parameters  Biopsy Result Chi-Square p-Value Test
Negative Positive
Sex Male 60 60.0% 40 40.0% 0.085 0.771 Chi-Square
Female 78 61.9% 48 38.1%
Place of residence Village 13 59.1% 9 40.9% 0.040 0.842 Chi-Square
Town 125 61.3% 79 38.7%

Table 1: Association between epidemiologic factors and H. pylori infection.

The infection occurred more frequently among male participants (40%) as compared to females (38.1%), however the difference was statistically not significant (p=0.771) as presented in (Table 1). The data shown in Table 2 predicted that exposure to H. pylori was higher among participants in the age group 28-39 years (57.58%), though age was not found to be associated with infection status.

Age Positive biopsy Chi-Square p-value Test
Age < 18 2 50.00% 0.21 0.644 Fisher’s Exact Test
Age 18 - 28 7 26.92% 1.784 0.206 Fisher’s Exact Test
Age 29 - 39 19 57.58% 0.017 5.646 Chi-Square test
Age 40 - 50 20 45.45% 0.976 0.323 Chi-Square test
Age 51 - 61 11 27.50% 0.267 0.102 Chi-Square test
Age 62 - 72 10 31.25% 0.927 0.336 Chi-Square test
Age ≥ 73 3 21.43% 1.924 0.258 Fisher’s Exact Test

Table 2: Positivity of infection among different age groups.

The overall H. pylori infection rates were 40.9% in patients from villages, and 38.7% from towns; nonetheless, the difference was not statistically significant (P>0.05) as depicted in (Table 1).

Higher rates of H. pylori infection were found among smokers as compared to non-smokers (42.5% vs. 34.9%); however, the difference was found to be statistically non-significant (p=0.243).

All other variables; alcohol and caffeine consumption were not associated with H. pylori infection (p>0.05) (Table 3).

 Parameters  Biopsy Result Chi-Square p-Value Test
Negative Positive
Smoker No 69 65.1% 37 34.9% 1.365 0.243 Chi-Square
Yes 69 57.5% 51 42.5%
Alcohol No 89 57.8% 65 42.2% 2.174 0.140 Chi-Square
Yes 49 68.1% 23 31.9%
Caffeine No 81 57.4% 60 42.6% 2.061 0.151 Chi-Square
Yes 57 67.1% 28 32.9%

Table 3: Association between lifestyle factors and H. pylori infection.

A significant (p=0.024) association of H. pylori infection rate was found with a decreased level of education. Individuals with lower educational levels had a higher risk than high school graduates and those with a higher education (Table 4).

Level of  Education Biopsy Result Chi-Square p-Value Test
Negative Positive
Formal education primary 34 48.6% 36 51.4% 7.475 0.024 Chi-Square
secondary 36 62.1% 22 37.9%
tertiary 68 69.4% 30 30.6%

Table 4: Association between educational level and H. pylori infection.

No significant association (p>0.05) was found of H. pylori infection in patients with present medical history (Table 5). It is worth mentioning that in the diabetic group H. pylori was positive in 19/49 (38.8%) cases while in non-diabetics, H. pylori was positive in 69/177 (39%) cases (Table 5).

Parameters  Biopsy Result Chi-Square P-Value Test
Negative Positive
HTN No 96 61.1% 61 38.9% 0.002 0.969 Chi-Square
Yes 42 60.9% 27 39.1%
DM No 108 61.0% 69 39.0% 0.001 0.979 Chi-Square
Yes 30 61.2% 19 38.8%

No 106 62.0% 65 38.0% 0.362 0.548 Chi-Square
Yes 31 57.4% 23 42.6%
CKD No 134 60.4% 88 39.6% 2.597 0.159 Fisher Test
Yes 4 100.0% 0 0.0%

Table 5: Association between medical history and H. pylori infection.

The most common presenting symptoms were epigastric pain (70.4%), bloating (41.6%) and heart burn (41.2%). The most commonly identified endoscopic findings were gastritis (78.3%), duodenitis (30.1%), and esophagitis (22.6%). Only duodenitis and oesophagitis (Table 6) were significantly associated with H. pylori (p=0.025 and 0.000 respectively).

 Endoscopic Findings Biopsy Result Chi-Square P-Value
Negative Positive
Normal No 116 58.0% 84 42.0% 6.855 0.010
Yes 22 84.6% 4 15.4%
Gastric ulcer No 125 60.4% 82 39.6% 0.472 0.625
Yes 13 68.4% 6 31.6%
Duodenal ulcer No 135 61.9% 83 38.1% 1.937a 0.267
Yes 3 37.5% 5 62.5%
Gastritis No 33 67.3% 16 32.7% 1.039a 0.308
Yes 105 59.3% 72 40.7%
Duodenitis No 104 65.8% 54 34.2% 5.006a 0.025
Yes 34 50.0% 34 50.0%
Esophagitis No 124 67.4% 60 32.6% 16.682a 0.000
Yes 14 33.3% 28 66.7%

Table 6: Analysis of endoscopic lesions and correlation with H. pylori infection.


H. pylori is the most common chronic bacterial infection in humans [1,2]. Its prevalence varies greatly among countries and even among population groups within the same country. The prevalence of H. pylori colonization is about 30% in the United States and other developed countries as opposed to >80% in many developing countries [16]. In general, the overall prevalence of H. pylori infection in the Middle East, irrespective of time and age groups, ranged from 22% to 87.6% [16].

In this prospective survey, the histologic prevalence of H. pylori among 226 patients who underwent biopsies during upper GI endoscopy was 38.9%. This number is in line with the three previously conducted studies in Lebanon that estimated the prevalence between 21% and 52% [13-15]. In our study we found no difference in H. pylori prevalence between the sexes. Regarding the influence of the lifestyle on the prevalence of H. pylori infection our data supports the hypothesis that there is no significant association between H. pylori and alcohol use or smoking which was shown in multiple studies [20-23]. Markers of low socioeconomic status such as a low family income [24] and low educational level [25-28], had all a higher likelihood of carrying H. pylori infection. Likewise, our current results established that: lower the education of people the higher is the risk for H. pylori infection. In our studied population, the most common reason for referral was dyspepsia (87.2%).

The prevalence of dyspepsia ranges from about 20-30% worldwide [29]. Despite a high prevalence of H. pylori in dyspeptic patients (40.6%) no significant association was found. These findings are in agreement with the earlier investigations reporting no association between dyspepsia and H. pylori [30,31].

The endoscopy results during our present study well demonstrated normal appearance just in 11.5% of cases. Our findings are fully contradictory to the earlier reports where normal endoscopy demonstrated the highest prevalence among symptomatic patients [32-34]. According to the literature, in 50-60% of patients, no endoscopic cause was apparent and the dyspepsia was considered to be idiopathic [34]. It is worth noteworthy that 15.4% of endoscopically normal looking mucosa revealed positive H. pylori histologically. Our results add support to earlier studies which highlighted the problem of disparity between normal endoscopic gastric mucosal appearance and histology in dyspeptic patients undergoing endoscopy [33]. This observation emphasizes the need for routine gastric mucosal biopsy in all symptomatic patients undergoing endoscopy. Gastritis was the commonest endoscopic pathology in this study (78.3%). It is well established in the literature that the commonest cause of gastritis is H. pylori infection [35]. However, in this study the relationship between H. pylori and endoscopic gastritis was statistically not significant.

In our present study, duodenitis was found in 30.1% cases and oesophagitis in 18.6% cases, being the next most prevalent endoscopic findings after gastritis. In fact, significant relationships were found between duodenitis, oesophagitis and H. pylori with p-values of 0.025 and 0.000 respectively. Nevertheless, gastric ulcer (GU) (8.4%) and duodenal ulcer (DU) (3.5%) were the least prevalent findings. Although H. pylori infection was identified as the main cause of peptic ulcer disease (PUD) [36] no statistical significant correlation with H. pylori was found in our study.

The prevalence of H. pylori infection is estimated at over 90% for DU and 70% for GU [37,38]. However in our study, 31.6% of GU patients and 62.5% of DU patients were H. pylori positive. This decrease in the prevalence of PUD related to H. pylori was reported in several studies in Australia and the United States of America [20-37]. Several factors may have influenced the decreased rate of PUD associated with H. pylori such as the use NSAIDs. The association between H. pylori infection and use of NSAIDs in ulcer disease is controversial. H. pylori and NSAIDs are independent and synergistic risk factors for peptic ulcer disease and bleeding ulcer [36]. Our current results do not indicate any significant prevalence of PUD (12.5%) in patients positive for H. pylori and users of NSAIDs. The use of NSAIDs was not associated with H. pylori infection in patients with PUD. This result is also supported by a recent meta-analysis of Tang et al. [39].

Concerning diabetes, no association was found with H. pylori. In fact, the link between H. pylori infection and diabetes remained controversial, it was studied for the first time by Simon [26]. Simon reported a higher prevalence of H. pylori infection in diabetic patients compared with controls (62% vs. 21%) [26]. These data were further confirmed in 1996 by a case-control study that examined 143 diabetics [25]. Zelenkova had reported a prevalence of H. pylori to be lower in diabetics compared to non-diabetic controls (27% vs. 51%) [27,28]. In other studies, the prevalence of H. pylori infection was comparable between diabetic and control [10-17]. In our study we found no significant association between H. pylori and diabetes (p=0.979). This is in line with a study done by Naja et al. on the association of H. pylori infection with insulin resistance and metabolic syndrome (MetS) among Lebanese adults that found no association of H. pylori infection with IR or MetS, and concluded that the eradication of H. pylori infection to prevent IR or MetS is not warranted [15].


The analysis of the research results for H. pylori on 226 patients showed that our study led to data comparable to those reported in the literature, particularly to the overall prevalence which was 38.9%. This infection is associated with low level of education and does not depend on gender, age, and area of residence. Gastritis is the most common endoscopic finding. NSAID use was suggested as playing critical role as co-factor for H. pylori infection. Regarding the prevalence of H. pylori in ulcer disease, our results show a lower percentage compared with literature data. The present study suggests that H. pylori infection is not increased in diabetes mellitus.


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