|Year : 2018 | Volume
| Issue : 1 | Page : 23-27
Primary bile reflux gastritis versus Helicobacter pylori gastritis: a comparative study
Enaase A.M.E Barakat1, Neven F Abbas2, Nashwa Y El-Kholi3
1 Department of Internal Medicine, Taibah University, Medina, Kingdom of Saudi Arabia
2 Department of Internal Medicine, Faculty of Medicine, Mansoura University, Mansoura, Egypt
3 Department of Internal Medicine, Al-Azhar University, Cairo, Egypt
|Date of Submission||20-Jun-2017|
|Date of Acceptance||12-Jul-2017|
|Date of Web Publication||20-Mar-2018|
Enaase A.M.E Barakat
Department of Internal Medicine, Faculty of Medicine, University of Mansoura, Mansoura, 35516
Kingdom of Saudi Arabia
Source of Support: None, Conflict of Interest: None
Background Bile reflux gastritis (BRG) is a common disorder, with few data on its pathophysiology and clinical course, whereas Helicobacter pylori is the well-known, commonest cause of chronic gastritis.
Aim The aim of this study was to compare between BRG and H. pylori-related gastritis, as regards demographic data, comorbid conditions, and pattern of upper gastrointestinal involvement.
Patients and methods It included 130 patients with endoscopic features of gastritis, subdivided into three groups: group A with BRG (56 patients); group B with H. pylori gastritis (58 patients); group C with gastritis in the presence of both H. pylori and bile reflux (16 patients). Statistical analysis was made to compare between the three groups as regards demographic data, history, and examination findings including endoscopic findings.
Results BRG is more common among younger age (21–30 years) and elderly patients (71–80 years), whereas H. pylori gastritis is more common in patients in the middle age group (31–60 years), the female/male ratio was 1.5 : 1 in patients with BRG, 1 : 1 in H. pylori gastritis. Nausea was the commonest symptom in patients with BRG (69.6%), whereas epigastric pain/discomfort was the commonest symptom (77.6%) in H. pylori gastritis. Diabetes was found to be more common in patients with H. pylori gastritis (29.3%) followed by BRG (26.8%), whereas obesity was more common in patients with BRG (76.8%) followed by H. pylori gastritis (65.5%). Endoscopy showed antral gastritis in cases with BRG (57.1%), pangastritis in H. pylori and mixed etiology gastritis (60.3 and 68.8%, respectively), reflux esophagitis in both BRG and H. pylori gastritis (41.1 and 44.8%, respectively), higher than mixed etiology gastritis (25%). Endoscopic Barrett’s mucosa was diagnosed in 10.7% of cases with BRG and 12.1% of cases with H. pylori gastritis. Duodenitis, duodenal erosions, or ulcerations were more common in cases with mixed etiology gastritis (62.5%), than in H. pylori gastritis (24.1%), followed by BRG (14.3%).
Conclusion BRG is a common, underdiagnosed condition, with distinct clinical and endoscopic features from H. pylori gastritis.
Keywords: bile reflux, diabetes mellitus, gastritis, Helicobacter pylori, obesity
|How to cite this article:|
Barakat EA, Abbas NF, El-Kholi NY. Primary bile reflux gastritis versus Helicobacter pylori gastritis: a comparative study. Egypt J Intern Med 2018;30:23-7
|How to cite this URL:|
Barakat EA, Abbas NF, El-Kholi NY. Primary bile reflux gastritis versus Helicobacter pylori gastritis: a comparative study. Egypt J Intern Med [serial online] 2018 [cited 2020 Feb 26];30:23-7. Available from: http://www.esim.eg.net/text.asp?2018/30/1/23/227958
| Introduction|| |
Bile reflux gastritis (BRG) is caused by an excessive reflux of bile, pancreatic, and intestinal secretions into the stomach. It occurs in either: gastric resection and primary biliary reflux due to the failure of pylorus . This can cause many complications such as peptic ulcer and antral gastritis . The combination of bile reflux and Helicobacter pylori infection may cause progression to gastric cancer not by traditional stepwise: inflammation–atrophy–metaplasia .
The aim of this prospective study was to compare between BRG and H. pylori gastritis, as regards demographic data, comorbid conditions, and pattern of upper gastrointestinal involvement during endoscopic diagnosis.
| Patients and methods|| |
This was a prospective comparative study including 130 patients with endoscopically diagnosed gastritis, who were subdivided into three groups:
- Group A having biliary reflux gastritis (endoscopic evidence of gastritis in the presence of excess bile in the stomach and negative rapid urease test for H. pylori, using gastric biopsy) included 56 patients.
- Group B having H. pylori gastritis (endoscopic evidence of gastritis and positive rapid urease test for H. pylori, using gastric biopsy) included 58 patients.
- Group C having gastritis, in the presence of both H. pylori and bile reflux, included 16 patients.
All patients included in the study were above 18 years old (adults), of both sexes and were selected by the gastroenterologist among patients with upper gastrointestinal dyspeptic symptoms (e.g. nausea, epigastric discomfort, or pain) attending the inpatient and outpatient clinics of the Gastroenterology and Hepatology Unit at the Internal Medicine Department, Riyadh National Hospital, between July 2010 and June 2014. All the patients provided written informed consent. The Institutional Review Board (IRB) of Riyadh National Hospital approved the study.
Patients were excluded from the study if they have hiatal hernia diagnosed by endoscopy (to exclude the contributing factor to reflux esophagitis). Patients with prior upper gastrointestinal surgery causing abnormal emptying mechanisms of the stomach (e.g. gastric bypass surgery) and patients unfit or are nonwilling to do gastrointestinal endoscopy were also excluded from this study.
The patients’ demographic data, history, and examination findings including endoscopic findings were recorded. In diagnostic upper gastrointestinal endoscopy, the presence of bile into the stomach, erythema of the gastric mucosa with or without erosions, mucosal ulcerations were recognized, and H. pylori test (rapid urease test) results were obtained.
SPSS, version 18 (SPSS Inc., Chicago, Illinois, USA) was used to conduct all the analysis. Independent t-test and one-way analysis of variance test were used to compare between different groups.
| Results|| |
Over a 4-year period we investigated the distinctive features of BRG from H. pylori gastritis, the mean age of patients with BRG was 45.03+14.4 years, patients with H. pylori gastritis was 43.62+13.1 years, whereas the mean age of patients with mixed etiology gastritis was 38.25+14.1 years. There was no significant difference on comparing different groups (P=0.22) ([Table 1]).
Age distribution of patients with BRG showed a bimodal pattern where it was more common among younger age groups (21–30 years) and elderly patients (71–80 years), whereas H. pylori gastritis was more common among patients in the middle age group (31–60 years) ([Figure 1]).
|Figure 1 Age distribution of patients in different gastritis groups. HP, Helicobacter pylori.|
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Female patients were more common in the BRG group, with a ratio of 1.5 : 1. In patients with mixed etiology gastritis men predominate (ratio of 2 : 1), whereas patients with H. pylori gastritis showed equal sex distribution (1 : 1) ([Table 1]).
Nausea was the most commonly reported symptom in patients with BRG followed by epigastric pain/discomfort (69.6 and 58.9%, respectively), whereas in patients with H. pylori gastritis, epigastric pain/discomfort was the most commonly reported symptom followed by heartburn (77.6 and 36.2%, respectively). Epigastric pain/discomfort was also the most commonly reported symptom in patients with mixed etiology gastritis, followed by nausea (81.2 and 56.3%, respectively). Heartburn was found to be present in patients with either BRG or H. pylori gastritis with comparable frequency (33.9% in BRG vs. 36.2% in H. pylori gastritis), whereas it was less common in patients with mixed etiology gastritis (18.8%).
Hematemesis was more common in patients with mixed etiology gastritis (12.5%) than H. pylori gastritis (8.6%), followed by BRG (3.6%) ([Table 2]).
The study investigated the association of gastritis with diabetes mellitus (DM) and obesity. Diabetes was found to be more common in patients with H. pylori gastritis (29.3%), followed by BRG (26.8%) and gastritis of mixed etiology (12.5%), whereas obesity was more frequent in patients with BRG (76.8%) followed by H. pylori gastritis (65.5%) and gastritis of mixed etiology (56.3%). The mean of BMI was compared in the three groups and there was no significant difference among them (P: 0.35) ([Table 3]).
|Table 3 Prevalence of diabetes mellitus and obesity in patients in different groups|
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Endoscopic findings were reported in the three groups; antral gastritis was the commonest endoscopic finding in cases with BRG (57.1%), whereas pangastritis was the commonest in H. pylori and mixed etiology gastritis (60.3 and 68.8%, respectively).
Reflux esophagitis was found in both BRG and H. pylori gastritis (41.1 and 44.8%, respectively) and in each was higher than mixed etiology gastritis (25%). Endoscopic Barrett’s mucosa was diagnosed in 10.7% of cases with BRG, 12.1% of cases with H. pylori gastritis, where none of the cases with mixed etiology gastritis showed Barrett’s mucosa ([Table 4]).
Duodenal involvement (as duodenitis, erosions, or ulcerations) was much more prominent in cases with mixed etiology gastritis (62.5%), than H. pylori gastritis (24.1%), followed finally by BRG where it was found in only 14.3% of patients ([Table 4]).
| Discussion|| |
BRG is a kind of gastritis which is caused by reflux of bile contents through the duodenum on the stomach . It is a common disorder which usually occurs after stomach surgeries in which the pyloric sphincter is damaged (secondary BRG) ,. Sometimes it can occur spontaneously without earlier surgeries (primary BRG) . Many studies described secondary BRG; however, primary BRG and its relation to H. pylori gastritis were not extensively studied previously. The aim of this study was to compare between primary BRG and H. pylori-related gastritis as regards demographic data, comorbid conditions, and pattern of upper gastrointestinal involvement during endoscopic diagnosis.
Age distribution of patients with BRG showed a bimodal pattern which was more common among younger age groups (21–30 years) and elderly patients (71–80 years), whereas H. pylori gastritis was more common among patients in the middle age group (31–60 years). This was agreed upon by Vere et al. , who found that the BRG was more frequent at older ages, with incidence being higher between 51 and 80 years. Another study on H. pylori has confirmed that H. pylori-associated nonatrophic gastritis and antral atrophic gastritis peak at the age of 41–50 years, with a decline thereafter . This can be explained by the need of shorter time to develop H. pylori-related gastritis than bile reflux − alkaline gastritis which has later presentation, whereas in the very young age group (21–30 years) of BRG, functional bowel disorders predominate and usually are more severe in this age group.
Female patients were more common in the BRG group, with a ratio of 1.5 : 1. In patients with mixed etiology gastritis men predominate (ratio of 2 : 1), whereas patients with H. pylori gastritis showed equal sex distribution (1 : 1); to our knowledge, no previous studies compared sex predominance in BRG compared with H. pylori gastritis, but individual studies on each showed similar results of female predominance in primary BRG ,,,,,, whereas men predominate in H. pylori infection ,. However, in another study, sex and age were not significantly different in H. pylori infection . This can be explained by the underlying functional pathophysiology of primary BRG which is frequent in female patients, contrary to the infection by H. pylori with similar exposure rates in either sex.
The study investigated the association of gastritis with DM and obesity as both may be considered as risk factors for primary BRG as it affects gastric motility and emptying. DM was found to be more common in patients with H. pylori gastritis (29.3%) followed by BRG (26.8%) and gastritis of mixed etiology (12.5%). The association between H. pylori and DM was first explored by Simon et al. , whereas the increased prevalence of reactive gastritis (which includes both BRG and NSAID-related gastritis) in diabetic patients was reported in another study . Immunosuppression in DM was hypothesized to be a predisposing factor for H. pylori infection ,, which can explain the increased prevalence of DM in patients with H. pylori gastritis in our study.
Obesity was more frequent in patients with BRG (76.8%) followed by H. pylori gastritis (65.5%) and gastritis of mixed etiology (56.3%). The mean of BMI was compared in the three groups and there was no significant difference among them (P=0.35). To our knowledge, none of the earlier studies investigated the role of obesity in BRG. Wolter et al.  have found that gastritis was the commonest endoscopic finding in obese patients during endoscopic evaluation before bariatric surgery, but they did not clarify the etiopathogenesis of gastritis. However, the association of obesity with other functional disorders like gastroesophageal reflux disease (GERD) was studied and confirmed ,,. The association of obesity with primary BRG in our study can be explained as obesity may affect the gastroduodenal reflux in a similar way as in gastroesophageal reflux.
Barrett’s esophagus (BE) is a premalignant condition which develops as a consequence of GERD ,,. In our study, reflux esophagitis was observed in both BRG and H. pylori gastritis (41.1 and 44.8%, respectively) and in each was higher than mixed etiology gastritis (25%). Endoscopic Barrett’s mucosa was diagnosed in 10.7% of cases with BRG, 12.1% of cases with H. pylori gastritis, where none of the cases with mixed etiology gastritis showed Barrett’s mucosa.
There is much recent evidence pointing to a role for duodenogastric bile reflux and bile acids in the pathogenesis of BE ,,,. Patients with BE have more evidence of BRG than subjects with uncomplicated GERD or nonulcer dyspepsia in the esophagus , as bile acids could be the source of carcinogens which act on the metaplastic mucosa to produce neoplasia . As regards H. pylori infection, it could pose a risk for the onset of GERD, which could in turn trigger BE . The combined effect of both BRG and H. pylori infection for the development of GERD and BE is an important area for further research.
| Conclusion|| |
BRG is a common problem with different presentation and risk factors, which may need specific management than H. pylori gastritis.
BRG is a new area of research, and more studies are needed on a larger scale to study its pathogenesis as a primary functional gastrointestinal disorder, its risk factors and complications.
The authors acknowledge the team at the Endoscopy Unit in Riyadh National Hospital for their effort in preparing the cases, assistance during the procedures, and continuous support which helped in the completion of the study.
Enaase A.M.E. Barakat is the guarantor of the article.
Enaase A.M.E. Barakat contributed to conception and design, performing endoscopic procedures, acquisition of data, and drafting of the manuscript; Neven F. Abass contributed to conception and design, interpretation of data, statistical support, and critical revision of the manuscript. Nashwa Y. El-Khouli carried out interpretation of data and critical revision of the manuscript.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Vere CC, Cazacu S, Comănescu V, Mogoantă L, Rogoveanu I, Ciurea T. Endoscopical and histological features in bile reflux gastritis. Rom J Morphol Emberyol 2005; 46:269–274.
Lee EL, Feldman M. Gastritis and gastropathies. In: Feldman M, Friedman L, Brandt LJ, editors. Sleisenger and Fordtran’s gastrointestinal and liver diseases. 8th ed. Philadelphia, PA: Saunders Elsevier; 2006. 1067–1083
Vdovychenko A. Is a bile reflux an additional cancerogenic factor in peptic ulcer, associated with Helicobacter pylori
infection? Rocz Akad Med Bialymst 2004; 49:72–74.
Saneimoghaddam A. Comparison of duodenogastric bile reflux in opium addicted and non-addicted patients with dyspepsia in Zahedan at 2009. [dissertation]. Zahedan, Iran: Zahedan University of Medical Sciences; 2008.
Benberin V, Bektayeva R, Karabayeva R, Lebedev A, Akemeyeva K, Paloheimo L et al.
Prevalence of H. pylori infection and atrophic gastritis among symptomatic and Dyspeptic adults in Kazakhstan. A hospital-based screening study using a panel of serum biomarkers. Anticancer Res 2013; 33:4595–4602.
Buxbaum KL. Bile gastritis occurring after cholecystectomy. Am J Gastroenterol 1982; 77:305–311.
Kellosalo J, Alavaikko M, Laitinen S. Effect of biliary tract procedures on duodenogastric reflux and the gastric mucosa, Scand J Gastroenterol 1991; 26:1272–1278.
Lorusso D, Pezzolla F, Cavallini A, Messa C, Giorgio P, Caruso ML et al.
A prospective study on duodenogastric reflux and on histological changes in gastric mucosa after cholecystectomy, Gastroenterol Clin Biol 1992; 16:328–333.
Nudo R, Pasta V, Monti M, Vergine M, Picardi N. Correlation between post-cholecystectomy syndrome and biliary reflux gastritis. Endoscopic study. Ann Ital Chir 1989; 60:291–300.
Scalon P, di Mario F, Del Favero G, Meggiato T, Rugge M, Baffa R et al.
Biochemical and histopathological aspects in duodenogastric reflux gastritis patients with or without prior cholecystectomy, Acta Gastroenterol Belg 1993; 56:215–218.
Scalon P, di Mario F, Rugge M, Meggiato T, Baffa R, Mantovani G et al.
Morpho-functional characteristics of reflux gastritis in patients after cholecystectomy and without cholecystectomy, Minerva Gastroenterol Dietol 1991; 37:113–116.
De Martel C, Parsonnet J. Helicobacter pylori
infection and gender: a meta-analysis of population-based prevalence surveys. Dig Dis Sci 2006; 51:2292–2301.
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; 49:742–749.
Kaur G, Naing NN. Prevalence and ethnic distribution of Helicobacter pylori
infection among endoscoped patients in north eastern Peninsular Malaysia. Malays J Med Sci 2003; 10:66–70.
Simon L, Toronoczky J, Toth M, Jámbor M, Sudár Z. The significance of Campylobacter pylori
infection in gastroenterologic and diabetic practice. Orv Hetil 1989; 130:1325–1329.
Małecki M, Bień AI, Galicka-Latała D, Klupa T, Stachura J, Sieradzki J. Reactive gastritis in patients with diabetics with dyspeptic symptoms. Przegl Lek 1996; 53:540–543.
Ojetti V, Pitocco D, Bartolozzi F, Danese S, Migneco A, Lupascu A et al.
High rate of Helicobacter pylori
re-infection in patients affected by type 1 diabetes. Diabetes Care 2002; 25:1485.
Oldenburg B, Diepersloot RJ, Hoekstra JB. High seroprevalence of Helicobacter pylori
in diabetes mellitus patients. Dig Dis Sci 1996; 41:458–461.
Wolter S, Duprée A, Miro J, Schroeder C, Jansen MI, Schulze-Zur-Wiesch C et al.
Upper gastrointestinal endoscopy prior to bariatric surgery-mandatory or expendable? An analysis of 801 cases. Obes Surg 2017; 27:1938–1943.
Van Oijen MG, Josemanders DF, Laheij RJ, van Rossum LG, Tan AC, Jansen JB. Gastrointestinal disorders and symptoms: does body mass index matter? Neth J Med 2006; 64:45–49.
Aro P, Ronkainen J, Talley NJ, Storskrubb T, Bolling-Sternevald E, Agréus L. Body mass index and chronic unexplained gastrointestinal symptoms: an adult endoscopic population based study. Gut 2005; 54:1377–1383.
Nocon M, Labenz J, Jaspersen D, Meyer-Sabellek W, Stolte M, Lind T et al.
Association of body mass index with heartburn, regurgitation and esophagitis: results of the Progression of Gastroesophageal Reflux Disease study. J Gastroenterol Hepatol 2007; 11:1728–1731.
Spechler SJ, Fitzgerald RC, Prasad GA, Wang KK. History, molecular mechanisms, and endoscopic treatment of Barrett’s esophagus. Gastroenterology 2010; 198:854–869.
Shaheen NJ, Richter JE. Barrett’s oesophagus. Lancet 2009; 373:850–861.
Marshall EEK, Anggiansah A, Owen WJ. Bile in the oesophagus: clinical relevance and ambulatory detection. Br J Surg 1997; 84:21–28.
Vaezi MF, Richter JL. Role of acid and duodenogastroesophageal reflux in gastroesophageal reflux disease. Gastroenterology 1996; 111:1192–1199.
Marshall RE, Anggiansah A, Owen WA, Owen WJ. The temporal relationship between oesophageal bile reflux and pH in gastro-oesophageal reflux disease. Eur J Gastroenterol Hepatol 1998; 10:385–392.
Stein HJ, Kauer WK, Feussner H, Siewert JR. Bile reflux in benign and malignant Barrett’s esophagus: effect of medical acid suppression and Nissen fundoplication. J Gastrointest Surg 1998; 2:333–341.
Nehra D, Howell P, Williams CP, Pye JK, Beynon J. Toxic bile acids in gastro-oesophageal reflux disease: influence of gastric acidity. Gut 1999; 44:598–602.
Dixon MF, Neville PM, Mapstone NP, Moayyedi P, Axon ATR. Bile reflux gastritis and Barrett’s oesophagus: further evidence of a role for duodenogastro-oesophageal reflux? Gut 2001; 49:359–363.
Busby WF Jr, Shuker DE, Charnley G, Newberne PM, Tannenbaum SR, Wogan GN. Carcinogenicity in rats of the nitrosated bile acid conjugates N
-nitrosoglycocholic acid and N
-nitrosotaurocholic acid. Cancer Res 1985; 45:1367–1371.
Tomasello G, Giordano F, Mazzola M, Jurjus R, Jurjus A, Damiani P et al.
Helicobacter pylori and Barrett’s esophagus: a protective factor or a real cause? J Biol Regul Homeost Agents 2017; 31:9–15.
[Table 1], [Table 2], [Table 3], [Table 4]