Endoscopic Assessment Prior to Bariatric Surgery in Saudi Arabia

Background: There are marked local inconsistencies in the Arabian Peninsula about the role of preoperative esophagogastroduodenoscopy (EGD) in bariatric surgery. Thus, this study was conducted to determine the frequency of endoscopic and histological findings in the Saudi population presenting for pre-bariatric surgery evaluation. Material and Methods: This was a retrospective study that included all the patients who were evaluated by EGD at Dammam Medical Complex, Dammam, Saudi Arabia, between 2018 and 2021 as a part of their pre-bariatric-surgery evaluation. Results: A total of 684 patients were included. They consisted of 250 male and 434 female patients (36.5% and 63.5%, respectively). The mean ± standard deviation for the patients' age and body mass index (BMI) were 36.4±10.6 years and 44.6±5.1 kg/m2, respectively. Significant endoscopic or histopathological findings as defined by the presence of large (≥ 2 cm) hiatus hernia, esophagitis, gastroesophageal reflux disease (GERD), Barrett esophagus, gastric ulcer, duodenal ulcer, or intestinal metaplasia were found in 143 patients (20.9%); 364 patients (53.2%) were diagnosed to have Helicobacter pylori infection. Conclusion: The high number of significant endoscopic and histopathological findings in our study supports the routine use of preoperative EGD in all bariatric surgery patients. However, omitting EGD before Roux-en-Y gastric bypass (RYGB) in asymptomatic patients is still reasonable as the most frequently found significant findings, esophagitis, and hiatus hernia, are less likely to impact the operative plans in RYGB. Similarly, active surveillance and treatment of H. pylori infections in obese patients are important but it is not clear whether H. pylori eradication should be done before bariatric surgery.


Introduction
Obesity represents a major global problem and a leading cause of death in the world accounting for around 3.4 million deaths annually. It is estimated that 20% of the world's adult population will be obese by the year 2030 [1]. In Saudi Arabia, the weighted prevalence of obesity is estimated to be between 24.7% and 35.5%, which is higher than the global average [2][3][4]. The impact of overweight and obesity in Saudi Arabia is found to directly cost a total of $3.8 billion annually, which was equal to 4.3% of the total health expenditure in the country in 2019 [5].
With the knowledge of these effects, the rate of bariatric surgeries continued to increase over time with more than 500,000 operations performed annually in the world [22]. Bariatric surgeries are also becoming more popular in the Saudi community. Around 52% of the Saudi population think that surgery is the best intervention to cure obesity [23], and 53% of 1129 interviewed Saudi individuals stated that they would seek a bariatric surgeon's help if they were morbidly obese [24], and more than 25,000 procedures are performed every year by surgeons in Saudi Arabia [25]. Esophagogastroduodenoscopy (EGD) assessment before bariatric operations differs in its necessity. The European Association for Endoscopic Surgery provided a conditional recommendation for routine preoperative EGD [26]. Similarly, the Saudi Arabian Society for Metabolic and Bariatric Surgery advises EGD as a routine preoperative investigation for all bariatric surgeries in its 2020-2021 guidelines update [25]. Others, on the other hand, conclude that standard preoperative assessment by EGD is not indicated in patients who are planned for bariatric surgery as the number needed to screen to find clinically significant abnormalities is high and recommend EGD only in patients with upper gastrointestinal symptoms [27][28][29].
Owing to this non-consensus regarding the need for routine preoperative EGD in bariatric surgery patients, this study was conducted to determine the frequency of endoscopic and histopathologic findings in the Saudi population presenting for pre-bariatric surgery evaluation.

Materials And Methods
This was a retrospective study that included all the patients who were evaluated by EGD at Dammam Medical Complex, Dammam, Saudi Arabia, between 2018 and 2021 as a part of their pre-bariatric-surgery evaluation.
Patients who had a previous gastric surgery that might alter the normal anatomy and histology (e.g., previous bariatric surgery) were excluded.

Results
A total of 754 records for pre-bariatric surgery endoscopy were retrieved in the study period. Eleven records were found to be duplicates and 28 patients had a history of previous gastric surgery and were excluded. Thirty-one patients did not tolerate the endoscopic procedures and were also excluded. The remaining 684 patients were included in the analysis ( Figure 1).

FIGURE 1: Flowchart for the reviewed patients
The included patients consisted of 250 male and 434 female patients (36.5% and 63.5%, respectively) with a male-to-female ratio of 0.58 ( Figure 2).

FIGURE 3: Patients' obesity class (n = 633)
Most of the studied patients were of the third World Health Organization (WHO) obesity class as defined by a body mass index (BMI) of ≥40 kg/m 2 (585 patients, 88.2%). Most of them also had at least one obesity-related comorbid condition (409 patients, 61.2%). Examples of these conditions include type 2 diabetes mellitus, hypertension, hyperlipidemia, nonalcoholic fatty liver disease, gastroesophageal reflux disease, debilitating osteoarthritis, and obstructive sleep apnea. The BMI was not recorded for 21 patients.
Forty-two patients (6.1%) were known to have a history of gastroesophageal reflux disease (GERD, 136 patients (19.9%) were using a proton pump inhibitor (PPI), 21 patients (3.1%) were on aspirin as a single antiplatelet therapy while three patients (0.4%) were on dual antiplatelets. Refer to Table 1 for the patients' demographics and medical backgrounds.

TABLE 1: Patients' demographics and medical backgrounds (n = 684)
One hundred and eighty-three patients (26.8%) had a hemoglobin of less than 12 g/dl. Among those anemic patients, the mean ± standard deviation for the patients' mean corpuscular volume (MCV) was 74.2 ± 10.2 fl. Thrombocytopenia and thrombocytosis were found in 10 (1.5%) and 31 (4.5%) patients, respectively.  Simple gastritis was the most common endoscopic finding appearing in 351 patients (51.3%) followed by hiatus hernia (206 patients, 30.1%), simple duodenitis (89 patients, 13.0%), and esophagitis (75 patients, 11.0%). Gastric and duodenal ulcers were found in 17 (2.5%) and 10 (1.5%) patients, respectively. No biopsy report was found in 39 patients. Three hundred and sixty-four patients (53.2%) were diagnosed to have H. pylori infections based on a histopathological assessment of their biopsies ( Figure 4). None of the study patients had malignant lesions. Refer to Table 3 for the patients' endoscopic and histopathological findings.

FIGURE 4: Helicobacter pylori infection (n = 684)
Three hundred and sixty-four patients (53%) were diagnosed to have H. pylori infections based on a histopathological assessment of their biopsies. No biopsy report was found in 39 patients (6%    There were no statistically significant differences between the patients with significant findings and the patients without them in age, BMI, diabetes mellitus, hypertension, and use of non-steroidal antiinflammatory drugs (NSAIDs) or antiplatelets but the patients with no significant findings had higher percentages of female patients (66.2% vs 53.2%) and of using PPIs (21.6% vs 13.3%) than the patients with significant findings (p-values = 0.005 and 0.035, respectively). Patients with significant findings had higher international normalized ratio (INR) values than the patients with no significant findings (1.3±3.3 vs 0.9±0.1, p-value = 0.038). Refer to Table 4 for the differences between patients with significant endoscopic and histopathological findings and patients without significant findings.

TABLE 4: Comparison between patients with significant endoscopic and histopathological findings^ and patients without significant findings (n = 684)
Significant findings were defined as having large (≥ 2 cm) hiatus hernia, esophagitis, GERD, Barrett esophagus, gastric ulcer, duodenal ulcer, or intestinal metaplasia. * Significant at p-value of less than 0.05 ALT: alanine aminotransferase; ALP: alkaline phosphatase, AST: aspartate aminotransferase, BMI: body mass index, GGT: gamma-glutamyl transferase, GERD: gastroesophageal reflux disease, INR: international normalized ratio, NAFLD: non-alcoholic fatty liver disease, NSAIDs: non-steroidal antiinflammatory drugs, PT: prothrombin time, PTT: partial thromboplastin time, PPI: proton pump inhibitor, WBC: white blood count There were no statistically significant differences between the patients with and without Helicobacter pylori infections in age, gender, BMI, diabetes mellitus, hypertension, and use of NSAIDs or antiplatelets. Refer to Table 5 for the differences between the patients with and without H. Pylori Infection.

Discussion
There are many reasons behind doing preoperative EGD in bariatric surgery patients. First, the endoscopic findings might lead to choosing a particular type of bariatric surgery type. For example, the findings of complicated GERD, Barrett's esophagus, or severe dysplasia will favor Roux-en-Y gastric bypass (RYGB) over sleeve gastrectomy [30,31]. Secondly, the endoscopic findings might alter the surgical plan. Hiatus hernia, if found, can be repaired concurrently with gastric banding, an intervention that is known to reduce postoperative intractable reflux necessitating reoperation or band removal [32]. Lastly, proceeding with bariatric surgeries without preoperative EGD will risk the surgeons facing surprising incidentalomas that are considered contraindications for surgery. The diagnosis of malignancy in a suspicious endoscopic lesion or the presence of oesophageal varices, for instance, might lead to cancellation of an original bariatric surgery plan [33]. On the other hand, performing a routine preoperative EGD for all bariatric surgery patients is not without any drawbacks. EGDs will add to the medical costs of bariatric procedures. Moreover, bariatric surgeries might get delayed for the EGDs, and delaying such procedures, as done during the coronavirus disease 2019 (COVID-19) crisis, is now known to have medical and psychological impacts on the patients from the continuously increasing weight and the associated depression [34].
There are marked local inconsistencies in the Arabian Peninsula about the role of preoperative EGD in bariatric surgery [35]. A total of 65% of 148 International Federation for the Surgery of Obesity and Metabolic Disorders-Middle East and North Africa Chapter (IFSO-MENAC) surgeon members who responded to a survey in 2019 reported that they did not request routine preoperative endoscopy for patients undergoing bariatric surgeries [36]. A study of 1555 patients in Qatar questioned the justifiability of preoperative EGD in asymptomatic patients scheduled for bariatric surgeries in the settings of a low percentage of significant findings that might change the surgical plans (10.5%) and a low rate of upper gastrointestinal cancers in the region [37]. A similar study of 1278 patients in the United Arab Emirates found the opposite, with 63.6% of the patients categorized to have abnormalities that had a direct impact on the surgical procedure and concluded that routine EGD is important for patients planned for bariatric surgery [38]. In Saudi Arabia, multiple smaller studies gave conflicting recommendations with one study advocating for preoperative EGD to be performed only if clinically indicated [39], and the others defending its use as a mandatory investigation for all patients undergoing bariatric surgery [33,40,41]. However, the high number of significant endoscopic and histopathological findings in our relatively larger study also supports the routine use of EGD in all bariatric surgery patients. It is still questionable though whether EGD before RYGB is really needed as the identification of abnormalities such as esophagitis or hiatal hernia by EGD does not usually affect the RYGB plan.
The prevalence of H. pylori infections at 53% in our sample of patients with obesity is comparable to the published data of an H. pylori prevalence of around 66-73% in obese patients in Saudi Arabia and higher than the known prevalence in non-obese patients, which ranges between 26% and 50% [42,43]. This indicates a possible link between obesity and H. pylori infections and could explain at least in part the increased risk of gastric cancer in obese patients [44]. Active surveillance and treatment of H. pylori infections in obese patients are important. However, it is unclear whether H. pylori should be eradicated before bariatric surgery as the rates of bleeding, leakage, hospital length of stay, and weight loss were comparable between H. pylori-positive and H. pylori-negative bariatric surgery patients [45,46]. Nevertheless, H. pylori is associated with increased marginal ulceration rates in patients undergoing RYGB [45], and postoperative foregut symptoms are more common in H. pylori-infected patients [47,48]. Moreover, anti-H. pylori antibody seropositivity was found to be associated with de novo gallstone formation [49], a well-known complication of bariatric surgeries [50]. Regrettably, our study failed to find significant predictors of H. pylori infection.
Our study has several limitations that should be considered. The first is that the number of included patients would have been bigger if it were not for the COVID-19 crisis and its caused restrictions on elective surgeries. Secondly, the patients were not categorized based on the presence and absence of gastrointestinal symptoms. Therefore, a correlation between the patient's symptoms and the presence of endoscopic findings could not be examined. Similarly, esophagitis was not classified based on the Los Angeles classification grades. Thus, even minimal esophagitis was considered to be a significant endoscopic finding although it might not change the management. In addition, due to the retrospective nature of the research, it was not clear if and to what degree the EGD findings impacted the original surgical plans. Lastly, the longterm postoperative outcomes were not considered.

Conclusions
The high number of significant endoscopic and histopathological findings in our study supports the routine use of preoperative EGD in all bariatric surgery patients. However, omitting EGD before RYGB in asymptomatic patients is still reasonable as the most frequently found significant findings, esophagitis and hiatus hernia, are less likely to impact the operative plans in RYGB. Similarly, active surveillance and treatment of H. pylori infections in obese patients are important but it is not clear whether H. pylori eradication should be done before bariatric surgery.

Additional Information Disclosures
Human subjects: Consent was obtained or waived by all participants in this study. Dammam Medical Complex Institutional Review Board, Dammam, Saudi Arabia issued approval END-01. Animal subjects: All authors have confirmed that this study did not involve animal subjects or tissue. Conflicts of interest: In compliance with the ICMJE uniform disclosure form, all authors declare the following: Payment/services info: All authors have declared that no financial support was received from any organization for the submitted work. Financial relationships: All authors have declared that they have no financial relationships at present or within the previous three years with any organizations that might have an interest in the submitted work. Other relationships: All authors have declared that there are no other relationships or activities that could appear to have influenced the submitted work.