Abstract
Background:
Erosive esophagitis (EE) is frequently present in patients with gastroesophageal reflux disease (GERD), some of which may not have GERD symptoms. The prevalence of EE in the Saudi population is unknown. In this study, we aimed to determine the prevalence and risk factors of EE among patients undergoing esophagogastroduodenoscopy (EGD).
Methods:
We retrospectively reviewed consecutive adults who underwent EGD at an academic tertiary care center. Clinical and endoscopic data were collected. The prevalence and severity of EE were determined. Multivariate regression analysis was used to identify risk factors for EE.
Results:
Records for 3230 patients were reviewed, of which 2805 were included in this study. The mean age was 48.6 ±18.6 years, and 1088 (38.7%) were male. Two hundred and twenty six (8%) patients underwent EGD for GERD-related indications. EE was noted in 309 (11%) patients and 58 (25.6%) with GERD-related indications. For patients with EE, the mean age was 49.2 ± 18.7 years, and 132 (42.7%) were males. LA Grade A esophagitis was the most common (53.9%), followed by grade B (29.6%). Among all patients, only EGD for GERD-related indications and hiatal hernia were significantly associated with EE on multivariate analysis [(aOR = 3.1, 95% CI 2.2–4.4, P < 0.01) and (aOR = 1.4, 95% CI 1.1–1.9, P < 0.01), respectively]. Age, gender, and body mass index were not associated with EE.
Conclusion:
In this large cohort, EE was present in 11% of patients who underwent EGD and in 25% of patients with GERD. EGD for GERD-related indications and hiatal hernia are independent risk factors for the presence of EE.
Keywords: Epidemiology, erosive esophagitis, gastroesophageal reflux disease
INTRODUCTION
Gastroesophageal reflux disease (GERD) is one of the most common disorders encountered in clinical practice. Recent studies suggested a global increase in the prevalence and burden of GERD.[1,2] The prevalence of GERD in the Middle East is estimated to be between 8 and 33%.[1] In Saudi Arabia, GERD is highly prevalent. In three cross-sectional studies that used the GerdQ questionnaire with a cut off score of 8 for diagnosis, the prevalence of GERD is reported between 20% and 45%.[3,4,5] GERD is associated with several risk factors, including diet, lifestyle, and obesity. These risk factors have been associated with the increased GERD prevalence in the Saudi population.[6]
While most patients with GERD do not have a visible mucosal disease on esophagogastroduodenoscopy (EGD), a considerable proportion have erosive esophagitis (EE). EE is characterized by endoscopically visible breaks in the distal esophageal mucosa with or without GERD symptoms. Population-based studies of patients revealed that the prevalence of EE ranged from 6.4% to 15.5%, irrespective of the presence of GERD symptoms. Among individuals without symptoms of GERD, the prevalence of EE ranged from 6.1% to 9.5%.[7,8,9] In a large Japanese study, 47% of patients with EE were asymptomatic, while 37% were mildly symptomatic.[10] Parallel to the increase in GERD prevalence, EE prevalence appears to be increasing in Asian countries.[11] Several risk factors have been associated with EE, including symptomatic GERD, old age, male gender, obesity, smoking, and hiatal hernia.[8,12]
While symptomatic GERD and its risk factors are widely prevalent in the Saudi population, the prevalence of EE is unknown. Since a considerable proportion of patients with EE are asymptomatic, in this study, we aimed to determine the prevalence rate of EE among patients undergoing EGD. We also aimed to assess the severity of EE and evaluate the risk factors associated with the presence of EE.
PATIENTS AND METHODS
This study was a retrospective analysis of patients who underwent EGD at King Abdulaziz University Hospital, a tertiary academic center in Jeddah, Saudi Arabia. The Institution Review Board approved the study (Ref 508-21), dated Oct 21, 2021. We searched the hospital endoscopy database and identified all consecutive patients who underwent EGD between May 2014 and December 2018. The electronic records and the endoscopy reports were reviewed. Patients were included regardless of the indication for EGD if they were older than 18 years at the time of the procedure. For patients who had more than one EGD performed, they were included only once using the index procedure.
One of eight gastroenterologists or a gastroenterology fellow under supervision performed the procedure. As per our routine practice, patients received conscious sedation using variable dosing of midazolam and fentanyl. Procedures were performed using an Olympus GIF-Q180 or GIF-HQ290 gastroscope. The following data were collected from the medical records: GERD diagnosis according to International Classification of Diseases coding preprocedure documentation, age, gender, height, weight, and the indication for EGD. Data were collected on the presence of EE and hiatal hernia. The severity of EE was graded based on endoscopic findings according to the LA classification: grade A (one or more mucosal break no longer than 5 mm that does not extend between the tops of two mucosal folds), grade B (one or more mucosal break more than 5 mm long that does not extend between the tops of two mucosal folds), grade C (one or more mucosal break that is continuous between the tops of two or more mucosal folds but which involve less than 75% of the circumference), and grade D (one or more mucosal break which involves at least 75% of the esophageal circumference). Hiatal hernia (HH) was defined as present when the distance from the proximal end of the gastric folds to the diaphragm was greater than 1 cm.
Statistical analysis
The mean, standard deviation, and median with range were used for continuous variables as appropriate. The percentage and count were used for categorical variables. Where applicable, statistical analysis for categorical variables was performed using the Chi-square or Fisher’s exact test. Where appropriate, statistical analysis for continuous variables was performed using the Student t-test or Mann–Whitney test. A multivariate regression model was used to evaluate risk factors for EE, including gender, age category (>40, 40–60, >60), obesity (BMI >30), HH, and EGD for GERD-related indication. The odds ratio (OR) and 95% confidence interval (95% CI) are given for each variable. A two-tailed P value <0.05 was considered statistically significant. Statistical analysis was performed using the R statistical software, version 1.2.5042 – © 2009-2020 RStudio, Inc.
RESULTS
Characteristics of study patients
Two thousand eight hundred and five patients underwent EGD and were included in the analysis after excluding 425 duplicate procedures. Of all included patients, 1088 (38.7%) were males, and the mean age was 48 years ± 18.6. The mean BMI was 29.7 ± 8.6. Indications for EGD are shown in Table 1. Epigastric pain/dyspepsia was the most common indication for EGD, in 971 (34.6) patients, followed by pre-bariatric surgery screening EGD in 561 (20%) and overt gastrointestinal bleeding in 272 (9.7%) patients. Two hundred and twenty six (8%) patients underwent EGD for GERD-related indications including screening for Barrett’s esophagus, assessment prior to surgical intervention, incomplete response to PPI, or the presence of associated alarming symptoms such as anemia, vomiting, dysphagia, bleeding, and weight loss.
Table 1.
Indications for EGD in the study cohort
| Indication | n | % |
|---|---|---|
| Epigastric pain/dyspepsia | 971 | 34.62% |
| Pre-bariatric surgery screening | 561 | 20% |
| Overt gastrointestinal bleeding | 272 | 9.7% |
| GERD | 226 | 8.06% |
| Iron deficiency anemia | 182 | 6.49% |
| Liver cirrhosis | 160 | 5.70% |
| Dysphagia/atypical chest pain | 186 | 6.63% |
| Weight loss/cancer | 129 | 4.60% |
| Nausea/vomiting | 44 | 1.57% |
| Diarrhea | 10 | 0.36% |
| Others or unspecified | 64 | 2.28% |
EGD, Esophagogastroduodenoscopy; GERD, gastroesophageal reflux
Characteristics of patients with and without erosive esophagitis
Tables 2 summarizes the characteristics of patients with and without EE. EE was diagnosed in this study in 309 (11%) of included patients. The mean age for patients with EE was 49.2 ± 18.7, and 132 (42.7%) were males. The mean BMI was 28.9 ± 8.1 years. 127 (41.1%) had HH. Fifty eight (18.7) patients had EGD for GERD-related indications. The prevalence of EE was 11.1%, 10.6%, and 12.7% in the age categories <40, 40–60, and >60 years, respectively. LA classification of EE was available for 293 patients. Grade A EE was the most common (53.9%), followed by grade B (29.6%). Figure 1 shows the distribution of LA classification among patients with EE. Of all patients included in this study, 2496 (88.9%) did not have EE. For those patients, the mean age was 48.7 ± 18.7 years, and 956 (38.3%) were males. The mean BMI was 29.8 ± 8.7 in 168 (6.7%) patients with EGD for GERD-related indications.
Table 2.
Patients’ characteristics and univariate analysis of variables between patients with and without erosive esophagitis
| Characteristic | Total n=2805 | Patients with EE n=309 | Patients without EE n=2496 | P | OR (95% CI) |
|---|---|---|---|---|---|
| Age (mean, sd) | 48 ± 18.6 | 49.2 ± 18.7 | 48.6 ± 18.6 | 0.59 | - |
| Age category (n, %) | |||||
| <40 | 1082 (38.5) | 120 (38.8) | 962 (38.5) | reference | - |
| 40 – 60 | 911 (32.4) | 97 (31.3) | 814 (32.6) | 0.75 | 0.95 (0.71-1.26) |
| >60 | 812 (28.9) | 92 (29.7) | 720 (28.8) | 0.87 | 1.02 (0.76 – 1.36) |
| Gender, Male (n, %) | 1088 (38.7) | 132 (42.7) | 956 (38.3) | 0.14 | 1.2 (0.93 – 1.53) |
| *BMI (mean, sd) | 29.7 ± 8.6 | 28.8 ± 8.1 | 29.8 ± 8.7 | 0.07 | - |
| *BMI >30 (n, %) | 1668 (64.4) | 168 (60.8) | 1500 (60) | 0.2 | 0.84 (0.64 – 1.1) |
| Hiatal hernia (n, %) | 837 (29.8) | 127 (41.1) | 710 (28.4) | < 0.01 | 1.75 (1.36 – 2.25) |
| GERD diagnosis (n, %) | 226 (8) | 58 (18.7) | 168 (6.7) | < 0.01 | 3.19 (2.26 – 4.47) |
*BMI data were available for 2589 patients; BMI, Body mass index; GERD, gastroesophageal reflux disease
Figure 1.
Distribution of LA classification among patients with erosive esophagitis
Characteristics of patients with GERD
Two hundred twenty-six patients had EGD for GERD-related indications. The mean age was 46.5 ± 17.5% years, and 86 (38.1%) were males. The mean BMI was 29.5 ± 7.2. One hundred ten patients (48.7%) had HH. Of patients who had EGD for GERD-related indications, 58 patients had EE, resulting in a 25.7% prevalence of EE in these patients.
Risk factors for erosive esophagitis
On univariate analysis, only EGD performed for GERD-related indications and HH were significantly associated with EE, OR 3.2 (95% CI 2.26–4.47, P < 0.01), and OR 1.75 (95% CI 1.36–2.25, P < 0.01), respectively. Table 3 shows the results of the multivariate analysis. EGD for GERD-related indications and HH were the only two factors significantly associated with EE and adjusted ORs 3.1 (95% CI 2.2–4.4, P < 0.01) and 1.4 (95% CI 1.1–1.9, P < 0.01), respectively.
Table 3.
Multivariate analysis of risk factors for erosive esophagitis
| Risk factor | Odd ratio | 95% CI | P |
|---|---|---|---|
| Male gender | 1.17 | 0.9 – 1.52 | 0.22 |
| Age category | |||
| <40 | Reference | - | - |
| 40-60 | 0.96 | 0.71 – 1.31 | 0.83 |
| >60 | 1.1 | 0.8-1.5 | 0.54 |
| BMI >30 | 0.85 | 0.64 – 1.11 | 0.23 |
| Hiatal hernia | 1.47 | 1.13 – 1.91 | <0.01 |
| GERD indication | 3.14 | 2.2 – 4.42 | <0.01 |
BMI, Body mass index; GERD, gastroesophageal reflux disease
DISCUSSION
In this large cohort of patients who underwent EGD for any indication, we found the prevalence rate of EE to be 11%. The prevalence rate of EE varies among different geographic regions and populations. This regional variation can be attributed to differences in lifestyle, diet, genetics, and the presence of risk factors for GERD itself. The prevalence of EE in our study is within the range reported for population-based Western studies, 6.4%–15.5%.[7,8,9] In Asian countries which have a lower prevalence of GERD, a lower prevalence of EE has been identified.[10,11] However, a recent Taiwanese study found an increasing prevalence of EE comparable to the Western population.[13] Most cases of EE in our study were mild, LA grade A or B, which is consistent with other studies.[8,13]
In the present study, EGD for GERD-related indications and HH were independently associated with EE. While EE may occur in the absence of GERD symptoms, it is not surprising that those who have known GERD are more likely to have EE. The presence of an HH is a well-established risk factor for GERD and its complications, and the association between HH and EE has been consistent across multiple studies.[8,10,13,14] HH disrupts the normal anatomical barrier of the gastroesophageal junction. It could predispose to GERD by different mechanisms, including impaired lower esophageal sphincter pressure, transient lower esophageal sphincter relaxation, impaired esophageal acid clearance, and delayed gastric emptying.[15] The prevalence of HH in the Saudi population is 29% in an endoscopy-based study, and it is within the reported range worldwide.[16]
We found no association between gender and EE. This contrasts with the consistent association between male gender and EE found in many studies. In a large multicenter Western study, which recruited patients with troublesome heartburn, male gender was significantly associated with EE.[12] A similar higher prevalence of EE among males was reported in a Taiwanese study.[13] We have no clear explanation for the lack of association between EE and male gender in our study. We speculate that a higher proportion of male patients could have been receiving anti-acid therapy, lowering their prevalence of EE. Although we found no association between EE and male gender in the present study, male gender is an independent risk factor for Barrett’s esophagus in the Saudi population.[17]
In the present study, EE was not associated with obesity, defined as BMI > 30. Previous studies reported conflicting findings on the relationship between obesity and EE.[13,18] There are several suggested mechanisms through which obesity could contribute to GERD, including increased abdominal pressure, transient lower esophageal sphincter relaxation, and predisposition to HH. However, abdominal obesity, as measured by waist circumference, could be more important than BMI itself in the prevalence of GERD and its complications.[19] Future studies that include data on abdominal obesity could provide more insight into the relationship between EE and obesity.
There are several limitations to our study. We included patients who presented for endoscopy assessment, so the results may not be generalizable to the general population. However, it is unlikely that individuals without endoscopy indications will be subjected to endoscopy for research purposes. We were unable to collect data on other potential risk factors for EE, such as dietary habits, smoking, and alcohol. Due to a lack of sufficient recording, we could not collect data on GERD therapy, which could have influenced the presence of EE. Similarly, due to lack of standardized reporting, we could not provide data about the grade of HH. Nevertheless, our study is the largest study to evaluate the prevalence and risk factors for EE in a Saudi population.
In conclusion, the prevalence of EE in this large cohort of patients undergoing endoscopy is 11%, and most cases are mild. EGD for GERD-related indications and HH are independently associated with EE. Patients with GERD and HH should have their management optimized to prevent GERD complications.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
REFERENCES
- 1.Alzahrani MA, Alqaraawi AM, Alzubide SR, Abufarhaneh E, Alkhowaiter SS, Alsulaimi M, et al. The Saudi Gastroenterology Association consensus on the clinical care pathway for the diagnosis and treatment of GERD. Saudi J Gastroenterol. 2024 doi: 10.4103/sjg.sjg_82_24. doi: 10.4103/sjg.sjg_82_24. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.GBD 2017 Gastro-oesophageal Reflux Disease Collaborators. The global, regional, and national burden of gastro-oesophageal reflux disease in 195 countries and territories, 1990-2017: A systematic analysis for the Global Burden of Disease Study 2017. Lancet Gastroenterol Hepatol. 2020;5:561–81. doi: 10.1016/S2468-1253(19)30408-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Al Ghadeer HA, Alabbad ZE, AlShaikh SB, Ahmed SU, Bu-Khamseen AA, Alhashem AT, et al. Prevalence of gastroesophageal reflux disease and associated risk factors in the Eastern Region, Saudi Arabia. Cureus. 2021;13:e19599. doi: 10.7759/cureus.19599. doi: 10.7759/cureus.19599. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Alsuwat OB, Alzahrani AA, Alzhrani MA, Alkhathami AM, Mahfouz MEM. Prevalence of gastroesophageal reflux disease in Saudi Arabia. J Clin Med Res. 2018;10:221–5. doi: 10.14740/jocmr3292w. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Almadi MA, Almousa MA, Althwainy AF, Altamimi AM, Alamoudi HO, Alshamrani HS, et al. Prevalence of symptoms of gastroesophageal reflux in a cohort of Saudi Arabians: A study of 1265 subjects. Saudi J Gastroenterol. 2014;20:248–54. doi: 10.4103/1319-3767.136982. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Alkhathami AM, Alzahrani AA, Alzhrani MA, Alsuwat OB, Mahfouz MEM. Risk factors for gastroesophageal reflux disease in Saudi Arabia. Gastroenterol Res. 2017;10:294–300. doi: 10.14740/gr906w. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Dent J, Becher A, Sung J, Zou D, Agréus L, Bazzoli F. Systematic review: Patterns of reflux-induced symptoms and esophageal endoscopic findings in large-scale surveys. Clin Gastroenterol Hepatol. 2012;10:863–73.e3. doi: 10.1016/j.cgh.2012.02.028. doi: 10.1016/j.cgh.2012.02.028. [DOI] [PubMed] [Google Scholar]
- 8.Ronkainen J, Aro P, Storskrubb T, Johansson SE, Lind T, Bolling-Sternevald E, et al. High prevalence of gastroesophageal reflux symptoms and esophagitis with or without symptoms in the general adult Swedish population: A Kalixanda study report. Scand J Gastroenterol. 2005;40:275–85. doi: 10.1080/00365520510011579. [DOI] [PubMed] [Google Scholar]
- 9.Zou D, He J, Ma X, Chen J, Gong Y, Man X, et al. Epidemiology of symptom-defined gastroesophageal reflux disease and reflux esophagitis: The systematic investigation of gastrointestinal diseases in China (SILC) Scand J Gastroenterol. 2011;46:133–41. doi: 10.3109/00365521.2010.521888. [DOI] [PubMed] [Google Scholar]
- 10.Mochizuki N, Fujita T, Kobayashi M, Yamazaki Y, Terao S, Sanuki T, et al. Factors associated with the presentation of erosive esophagitis symptoms in health checkup subjects: A prospective, multicenter cohort study. PLoS One. 2018;13:e0196848. doi: 10.1371/journal.pone.0196848. doi: 10.1371/journal.pone. 0196848. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Jung HK. Epidemiology of gastroesophageal reflux disease in Asia: A systematic review. J Neurogastroenterol Motil. 2011;17:14–27. doi: 10.5056/jnm.2011.17.1.14. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Labenz J, Jaspersen D, Kulig M, Leodolter A, Lind T, Meyer-Sabellek W, et al. Risk factors for erosive esophagitis: A multivariate analysis based on the ProGERD study initiative. Am J Gastroenterol. 2004;99:1652–6. doi: 10.1111/j.1572-0241.2004.30390.x. [DOI] [PubMed] [Google Scholar]
- 13.Ou JL, Tu CC, Hsu PI, Pan MH, Lee CC, Tsay FW, et al. Prevalence and risk factors of erosive esophagitis in Taiwan. J Chin Med Assoc. 2012;75:60–4. doi: 10.1016/j.jcma.2011.12.008. [DOI] [PubMed] [Google Scholar]
- 14.Avidan B, Sonnenberg A, Schnell TG, Sontag SJ. Risk factors for erosive reflux esophagitis: A case-control study. Am J Gastroenterol. 2001;96:41–6. doi: 10.1111/j.1572-0241.2001.03449.x. [DOI] [PubMed] [Google Scholar]
- 15.Hyun JJ, Bak YT. Clinical significance of hiatal hernia. Gut Liver. 2011;5:267–77. doi: 10.5009/gnl.2011.5.3.267. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Alsahafi MA, Alajhar NA, Almahyawi AO, Alsulami HH, Alghamdi WA, Alharbi LA, et al. The prevalence and risk factors for hiatal hernia among patients undergoing endoscopy: A retrospective analysis. Saudi Med J. 2023;44:509–12. doi: 10.15537/smj.2023.44.5.20220903. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Alsahafi M, Mimish H, Salem F, Hijazi M, Aljahdli E, Jawa H, et al. The prevalence of Barrett's esophagus among a Saudi Arabian population. Dig Dis Sci. 2021;66:2311–6. doi: 10.1007/s10620-020-06503-z. [DOI] [PubMed] [Google Scholar]
- 18.Chen TS, Chang FY. The prevalence and risk factors of reflux esophagitis among adult Chinese population in Taiwan. J Clin Gastroenterol. 2007;41:819–22. doi: 10.1097/01.mcg.0000225658.30803.79. [DOI] [PubMed] [Google Scholar]
- 19.El-Serag H. The association between obesity and GERD: A review of the epidemiological evidence. Dig Dis Sci. 2008;53:2307–12. doi: 10.1007/s10620-008-0413-9. [doi: 10.1007/s10620-008-0413-9] [DOI] [PMC free article] [PubMed] [Google Scholar]