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Original article
Evaluation of gastroesophageal reflux before and after sleeve gastrectomy using symptom scoring, scintigraphy, and endoscopy Aditya Sharmaa, Sandeep Aggarwala,*, Vineet Ahujab, Chandrashekhar Balb,c a
Departments of Surgical Disciplines, All India, Institute of Medical Sciences (AIIMS), New Delhi 110029, India b Gastroenterology, All India, Institute of Medical Sciences (AIIMS), New Delhi 110029, India c Nuclear Medicine, All India, Institute of Medical Sciences (AIIMS), New Delhi 110029, India
Abstract
Background: The effect of laparoscopic sleeve gastrectomy (SG) on gastroesophageal reflux disease (GERD) has been a controversial issue. There have been limited studies on this aspect and most of the published studies are retrospective. Therefore, a prospective study was designed to objectively assess the problem. The objective of this study was to assess the impact of SG on symptoms of gastroesophageal reflux using questionnaire, endoscopy, and radionuclide scintigraphy. Methods: Thirty-two patients undergoing laparoscopic sleeve gastrectomy were assessed for gastroesophageal reflux using Carlsson Dent Questionnaire and GERD questionnaire before and after surgery at three monthly intervals. They were also subjected to upper GI endoscopy (UGIE) and radionuclide scintigraphy both pre- and postoperatively. Results: Mean preoperative weight and body mass index were 126.5 kg and 47.8 kg/m2, respectively. Mean percent excess weight loss at 12 months was 64.3 ⫾ 18.4. Both the Carlsson Dent Score (CDS) and Severity Score (SS) exhibited a decline from 2.88 to 1.63 (p o 0.05) and 2.28 to 1.06 (p o 0.05), respectively after 12 months. Radionuclide scintigraphy revealed a significant rise of GERD from 6.25% to 78.1% in the postoperative period (p o 0.001). UGIE showed a rise in incidence of esophagitis from 18.8% to 25%; however, there was improvement in all patients except one in terms of reduction of severity of esophagitis. Conclusion: Presence of GERD may not be considered as a contra-indication for sleeve gastrectomy. There is improvement of GERD as assessed by symptom questionnaires, as well as improvement in grade of esophagitis. The new onset GERD detected on scintigraphy may not be pathologic as there is a decrease in total acid production postsurgery; however, it still remains an important issue and needs long-term follow-up. (Surg Obes Relat Dis 2014;]:00–00.) r 2014 American Society for Metabolic and Bariatric Surgery. All rights reserved.
Keywords:
Sleeve gastrectomy; Gastroesophageal reflux; Endoscopy; Scintigraphy
Morbidly obese patients have an increased prevalence of reflux symptoms and esophagitis [1]. The presence of gastroesophageal reflux disease (GERD) in such patients may affect the choice of weight loss procedure. Roux-en-Y * Correspondence: Dr Sandeep Aggarwal, Professor, Department of Surgical Disciplines, All India Institute of Medical Sciences (AIIMS), New Delhi 110029, India. E-mail: [email protected]
gastric bypass has been favored by some over sleeve gastrectomy (SG) in morbidly obese patients with GERD [1]. The effect of SG on GERD has been one of the points for criticism of the procedure; however, there is a paucity of prospective studies which have analyzed the problem of GERD after SG as a primary endpoint [2–7]. SG has carved its own niche as a sole weight loss procedure and has been rapidly adopted by surgeons worldwide [8–11] . Besides excellent weight loss, SG results in remarkable resolution/
http://dx.doi.org/10.1016/j.soard.2014.01.017 1550-7289 r 2014 American Society for Metabolic and Bariatric Surgery. All rights reserved.
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Thirty-five patients undergoing laparoscopic sleeve gastrectomy for morbid obesity were enrolled for the study and followed up for one year. We followed the standard National Institutes of Health Guidelines, which included patients with morbid obesity, defined as Body Mass Index (BMI) 440 kg/m2, patients with BMI 435 kg/m2 with obesity related co-morbidities. Patients with symptomatic GERD and/or hiatus hernia were not excluded fig. 1. A detailed preoperative evaluation was done. The sleeve was created in the standard fashion over a 36-F bougie starting at 4–5 cm from pylorus. The staple line was not reinforced. Hiatal hernia, if present, was not repaired in any of the patients as it was deemed small in all patients.
of 4 seven was considered to have GERD. The copyrights registration for both the questionnaires were done and submitted to the ethics committee of the institute. The study was approved by the institutional ethics committee (Ref no.269/01.07.2011). Patients were followed up at three monthly intervals and at each visit symptom questionnaires were administered and scores were documented. Additionally, all patients underwent upper gastrointestinal endoscopic (UGIE) examination and scintigraphy in the preoperative period as well as at six months after SG. On UGIE, severity of esophagitis was graded according to the Los Angeles (LA) scoring system on a scale from A through D [19]. For scintigraphy, a validated method for the objective study of GERD [6,20], the patients were given a capsule containing the radioactivity at a dose of .5 mci in the form of Tc99-labeled sulfur colloid. It was followed by 400 milliliters (mL) of orange juice. Data acquisition was carried out with a frame rate of 10 s/frame for 15 min. The GERD index was be calculated as follows: Background corrected esophageal counts/Background corrected total gastric counts 100%. A GERD index of Z4 was used as the cutoff to determine positivity for GERD. The result was noted as presence or absence of reflux.
Evaluation of gastroesophageal reflux (GER) symptoms
Statistical analysis
For the purpose of the study, all patients underwent assessment of reflux symptoms using two different questionnaires; GERD questionnaire [16,17] to assess Symptom-Severity (SS) score and Carlson Dent selfadministered questionnaire [18]. The GERD questionnaire uses a grading of symptoms of heartburn and regurgitation (Table 1). A severity score Z4 is considered positive for GERD. The Carlsson Dent Questionnaire (Table 2) was given to the patient and the Carlsson Dent Score (CDS) was calculated from the responses given. A patient with a score
All data were prospectively collected and continually updated in a computer database using the Microsoft Office Excel program, and then analyzed using STATAv12 and IBM SPSS v20 (data analysis and statistical software). Data was analyzed first by using descriptive statistics. The pairwise comparison at 12 months was done for CDS and SS using related samples Wilcoxon signed rank test. McNemar test was applied to see the changes in qualitative data. Differences were considered statistically significant for p-values o .05.
improvement of co-morbidities among morbidly obese individuals [10–15]. Since the impact of SG on GERD remains an unresolved issue, this prospective study was undertaken to objectively determine the problem of reflux in patients undergoing SG using symptom questionnaires, radionuclide scintigraphy, and upper gastrointestinal endoscopy (UGIE). Methods
8.00 7.00 6.00 5.00 4.00 3.00
W 2.00
2.88 2.28
3.09 2.16
2.81 1.81
2.38 1.63
1.50 E 1.06 B 1.00 4 0.00 C Pre op 3m 6m 9m 12m / -1.00 F P -2.00 O Fig. 1. Trend of mean Carlsson Dent Score (CDS) and mean Severity Score (SS) of patients
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Table 1 Symptom score (SS) Severity of symptoms of heartburn and regurgitation Grade 0: No symptoms. Grade 1: Mild symptoms with spontaneous remission. No interference with normal activity and sleep. Grade 2: Moderate symptoms with spontaneous, but slow, remission. Mild interference with normal activity and sleep. Grade 3: Severe symptoms without spontaneous remission. Marked interference with normal activity and sleep. Frequency of symptoms of heartburn and regurgitation Grade 0: Absent. Grade 1: Occasional (o 2 days per week). Grade 2: Frequent (2 to 4 days per week). Grade 3: Very frequent ( 4 4 days per week). The final score for each symptom was obtained by multiplying the scores for severity and frequency. The total score was obtained by adding the final scores of individual symptoms and noted as Symptom Score (SS).
Results Out of 35 patients, two patients did not meet scheduled follow up appointments and one patient refused UGIE in follow up. These three patients were excluded from the analysis. Of the 32 patients, 22 (68.8%) were females. Mean age for the patient population was 35.8 years (range-19–60). Mean preoperative weight and BMI were 126.5 kg and 47.8 kg/m2, respectively. Mean percent excess weight loss at 3 months, 6 months, 9 months, and 12 months was 22.7 ⫾ 7.4, 38.8 ⫾ 11.1, 50.02 ⫾ 15.4, and 64.3 ⫾ 18.4, respectively. Carlsson Dent Score (CDS) varied from –2 to 13. GERD Symptom score (SS) varied from 0 to 12. There was a statistically significant decrease in mean values of both CDS from 2.88 to 1.63 (p o 0.05) and SS from 2.28 to 1.06 (p o 0.05), respectively, after a 12 month period. Moreover, out of five patients who had CDS 47 suggestive of reflux preoperatively, only three patients had a CDS 47 at 12 months after surgery suggesting improvement. Similarly, out of eight patients who had SSZ4 (positive for GERD) in the preoperative only three patients had a SS Z4 at 12 months after surgery (Table 3). Esophagogastroduodenoscopy was done preoperatively and postoperatively at six months. Preoperatively six (18.8%) patients had esophagitis with 50% being LA grade B. Postoperatively the incidence of esophagitis increased to 25% (8/32), but this rise was not statistically significant. Moreover, there was improvement in five patients in terms of reduction of LA grading including one patient with resolution of esophagitis (Table 4). The preoperative and postoperative symptom scores of these five patients are depicted in Table 5. Eight patients (25%) were identified as having an hiatal hernia, which were all small on preoperative endoscopy and 11 (34.4%) patients showing hiatal hernia, all small, in postoperative period. Thus, three patients developed new onset hiatal hernia in the postoperative period.
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Out of 32 patients, 30 patients had no reflux on scintigraphy preoperatively. Twenty- four (80%) of these 30 patients presented with new onset GERD on scintigraphy done at six months after surgery. Preoperatively scintigraphic reflux was documented in only two (6.25%) patients. One of these patients exhibited resolution. Postoperatively the incidence of reflux significantly increased to 78.1% (25/32) (p value o 0.001). Discussion The problem of reflux after SG is an unresolved issue. Various studies have displayed conflicting outcomes Table 2 Carlsson Dent Questionnaire It is a self-administered questionnaire, kindly tick the appropriate choice 1. Which one of these four statements BEST DESCRIBES the main discomfort you get in your stomach or chest? (5) A burning feeling rising from your stomach or lower chest up toward your neck. (0) Feelings of sickness or nausea. (2) Pain in the middle of your chest when you swallow. (0) None of the above, please describe below: 2. Having chosen one of the above, please now choose which one of the next three statements BEST DESCRIBES the timing of your main discomfort? (–2) Any time, not made better or worse by taking food. (3) Most often within 2 hours of taking food. (0) Always at a particular time of day or night without any relationship to food. 3. How do the following affect your main discomfort? Worsens Improves No effect/Unsure (a) Larger than usual meals (1) (1) (0) (b) Food rich in fat (1) (1) (0) (c) Strongly flavored or spicy food (1) (1) (0) 4. Which one of the following BEST DESCRIBES the effect of indigestion medicines on your main discomfort? (0) No benefit (3) Definite relief within 15 minutes (0) Definite relief after 15 minutes (0) Not applicable (I don’t take indigestion medicines) 5. Which of the following BEST DESCRIBES the effect of lying flat, stooping, or bending on your main discomfort? (0) No effect (1) Brings it on or makes it worse (–1) Gives relief (0) Don’t know 6. Which of the following BEST DESCRIBES the effect of lifting or straining (or any other activity that makes you breath heavily) on your main discomfort? (0) No effect (1) Brings it on or makes it worse (–1) Gives relief (0) Don’t know or this does not apply to me 7. If food or acid-tasting liquid returns to your throat or mouth what effect does it have on your main discomfort? (0) No effect (2) Brings it on or makes it worse (0) Gives relief (0) Don’t know or this does not apply to me The figures in parenthesis shows score for individual response. Total score is calculated by adding the individual score of each question.
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Table 3 Number of patients positive and negative for GER based on two questionnaires
Table 5 Symptom scores of patients who showed improvement in endoscopic esophagitis grade
Questionnaire Score
Preoperative 3 months
6 months
9 months
12 months
Patient
E0
E6
SS0
SS6
CDS0
CDS6
CDS 4 7 CDS r 7 SS Z 4 SS o 4
5 27 8 24
4 28 4 28
5 27 3 29
3 29 3 29
1 2 3 4 5
B A D B C
A Absent A A A
6 2 8 8 2
2 2 2 2 2
11 3 5 4 5
0 4 3 7 2
4 28 7 25
CDS ¼ Carlsson Dent Score. SS ¼ Severity Score.
[2–7,18,19,21–26]. Braghetto et al. [6] analyzed data from 167 patients using a clinical questionnaire and found 27.5% patients (46/167) had reflux symptoms after SG. They have not documented the preoperative incidence of reflux. Three of their patients developed vomiting and were found to have stricture in the postoperative period. We had no incidence of stricture in our patient population. Tai et al. [2] used the Reflux Disease questionnaire in 66 patients with a median follow up of 12 months and found an increase in the prevalence of GERD after SG, from 12.1% to 47 %. In a similar study of 28 patients by Howard et al. [21] symptombased questionnaire was administered four weeks postoperatively to patients. New onset GERD symptoms were found in 22% of the patients. They concluded that SG might increase the prevalence of GERD symptoms. The primary aim of the study was to compare the symptoms of GERD using questionnaires before and after LSG. Our study reveals that there is a statistically significant decline in incidence of GERD symptoms as reflected by decrease in mean values of both CDS and SS from 2.88 to 1.63 (p o 0.05) and 2.28 to 1.06 (p o 0.05), respectively. This is in contrast to the above mentioned studies [2,6,21]. The maximum responses to the first question in the Carlsson Dent Questionnaire, which asks about the description of “main discomfort the patient feels in stomach or chest” in postoperative patients, was “none of the above.” Table 4 Table showing grade of endoscopic esophagitis before surgery and six months after surgery Postoperative grade (n) Pre operative grade (n)
None
LA-A
LA-B
Total
None LA-A LA-B LA-C LA-D Total
23 1 0 0 0 24
3 0 2 1 1 7
0 0 1 0 0 1
26 1 3 1 1 32
P value ¼ 0.2873. *Esophagitis grade using Los Angeles System. LA - A - Mucosal break o 5 mm in length. LA - B - Mucosal break 4 5 mm. LA - C - Mucosal break continuous between 4 2 mucosal folds. LA - D - Mucosal break 4 75% of esophageal circumference.
E0 ¼ Los Angeles esophagitis grade—Preoperative. E6 ¼ Los Angeles esophagitis grade—Postoperative at 6 months. SS0 ¼ Severity Score—Preoperative. SS6 ¼ Severity Score—Postoperative at 6 months. CDS0 ¼ Carlsson Dent Score—Preoperative. CDS6 ¼ Carlsson Dent Score—Postoperative at 6 months.
Upon asking further for a description of the discomfort it was either postprandial ”belching” or ”difficulty swallowing” rather than a ”burning feeling rising.” Similar to our study, Carabotti et al. [22] found that postprandial distress (PDS) rather than GERD is the main complaint post-SG. Using the Rome III criteria symptom questionnaire for upper GI symptoms in 97 patients who underwent SG, they found that before SG 52.7% patients were asymptomatic, 27% had GERD symptoms, 5.4% PDS, and 2.7% had epigastric pain symptoms. After median follow up of 13 months, 91.9 % patients complained of upper GI symptoms with prevalence of PDS being 59.4%. SG was associated with de novo dyspepsialike syndrome, with an OR of 7.00 (95 % CI 2.9 –18.3, p o .0001). On the other hand, the prevalence of GERD before and after surgery was not different (OR ¼ 1.083, 95 % CI .4652–2.530, p 4 .05). The symptom that was strongly related to SG was dysphagia (OR-4.7) (incidence-19.7%) similar to our response for the CD questionnaire. They further state that GI symptoms did not have a great impact on quality of life as also mentioned by Howard et al. [21] Regarding scintigraphic changes there is only single study by Braghetto et al. [6] after SG, which reported the incidence of GERD to be 70%; however, they have not documented the reflux preoperatively. In our study the preoperative incidence of reflux documented on scintigraphy was 6.25 %. Postoperatively the incidence significantly increased to 78.1 %. The possible reasons for the reflux include loss of angle of His, tubulization of stomach leading to high intragastric pressure, and dissection at phrenoesophageal junction with loss or damage to sling fibers [6]. Though we have not done any pressure studies, we strongly feel that increased intragastric pressure is mainly responsible for the increased reflux. There have been two schools of thought regarding the effect of SG on GERD and proponents of both have cited valid reasons for favoring each one of them. The mechanism for improvement post-SG cited are faster gastric emptying, reduction in gastric reservoir function, alteration of antrum–duodenal motor complex, gastrointestinal
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hormonal modifications, decrease in intrabdominal pressure due to weight loss, decrease in total acid production, and an increase in lower esophageal sphincter pressure (LESP). The others claim modification of esophagogastric junction, converting it to a straight tubular segment, partial sectioning the sling fibers, increased intraluminal pressure, presence of hiatal hernia, and decreased LESP lead to worsening of GERD after SG. It is evident from above that issue of GERD after SG is a complex and unresolved problem. Braghetto et al. [6,23] also found a decrease in LESP: 14.2 ⫾ 5.8 mm of Hg to 11.2 ⫾ 5.7 mm of Hg at 26 months postoperatively, which might be responsible for this reflux; however, another study by Peterson et al. [24] on effect of SG on LESP and esophageal motility contradicts the above results. They found a significant increase in LESP from 8.4 mm of Hg to 21.2 mm of Hg in group of late postoperative patients ( 48 months post-SG) and 11 to 24 mm of Hg in other groups of early postoperative patients (six days). They further reviewed the video material of surgery and found the distance between the stapler line and the gastroesophageal junction affected the LESP. They concluded that SG significantly increases LES pressure and may be protective against GERD. In our study we have not done esophageal manometry and, thus, are unable to comment on the LESP; however, the reflux does increase significantly from 6.25% to 78.1% as evidenced by scintigraphy. Comparing the incidence of scintigraphic GERD and endoscopic esophagitis grade postoperatively it can be seen that the GERD is not translating to overt esophagitis in our study. The symptom scores also show significant reduction at 12 months. The plausible explanation could be the increase in pH potentially due to removal of two-thirds of the stomach and consequent reduction in parietal cell mass. Due to same reasons, the scintigraphic reflux is not leading to overt symptoms as assessed by the symptom scoring. A longer follow up period might be required to document esophageal changes and 24 hour pH studies and manometry will be required to resolve the issue of reflux content and pathogenicity. Del Genio et al. [25] performed 24-hour pH manometry and multichannel intraluminal impedance plus endoscopy before SG in 15 consecutive patients who had no preoperative symptoms of gastroesophageal reflux disease (GERD), hiatal hernia (HH), or Barrett's esophagus. One year after SG, LESP had not changed, but there were increased ineffective secondary waves with an increase in nonacid reflux during the day. They concluded that sleeve was an effective restrictive procedure that increased the postprandial reflux episodes but did not induce GERD. Moon et al. [26] have also attributed total acid reduction as a reason for a decrease in GERD after SG. Hiatus hernia is another important confounding factor. In our study, eight patients had a small hiatus hernia on preoperative endoscopy but only four of these had esophagitis. Two patients with LA-B and one with LA-A had improvement in the postoperative period with LA-B decreasing to LA-A and LA-A to no esophagitis. One
5
patient had persistent LA-B. Postoperatively three additional patients developed a small hiatus hernia. Tai et al. [2] compared hiatal hernia and esophagitis before and after sleeve gastrectomy in 66 patients. The incidence of esophagitis increased from 16.7% to 66.7% and that of hiatal hernia increased from 6.1% to 27.3%.They also found hiatal hernia occurred at a higher rate in patients with esophagitis than without esophagitis. Daes et al. [3] found HH in 34 patients (25%) in the study cohort of 66 patients, of which 29 (85.3 %) had preoperative symptoms of GERD. They treated hiatal hernia by various surgical methods. At six months to one year follow up, only two patients had GERD symptoms. Thus, they concluded that careful attention to surgical technique can result in reduction in occurrence of GERD symptoms. Similar guidelines were provided in the consensus statement compiled by Rosenthal [27], which states that aggressive identification of hiatal hernia should be done intraoperatively and posterior repair should be done after the creation of sleeve gastrectomy; however, in our study, improvement in the grade of esophagitis occurred despite the hiatus hernia not being repaired. Our study has certain limitations, which include the subjective nature of the symptom scores, lack of availability of 24 hour pH monitoring, and the fact that the comparison of esophagitis grade, scores and scintigraphy has been done at six months and not at one year. Conclusion The problem of GERD after SG seems to be a complex issue. The patients are more concerned with dyspepsia and postprandial discomfort (PDS) rather than GERD. There is a statistically significant decrease in mean values of both symptom scores viz. CDS and SS after a 12 month period. All the patients, except one, with preoperative esophagitis on endoscopy improved after SG. Though a number of patients in our study have a new onset GERD detected on scintigraphy, it may not be pathologic as there is reduction in subjective symptomatology and quantified esophagitis grade. So does SG constitute a contraindication for patients with GER? The answer based on the above facts seems to be no. Thus, the presence of esophagitis on endoscopy or symptoms attributed to GERD may not be considered as a contraindication for SG; however, the results of scintigraphy are a cause for concern and long term follow-up is required. References [1] Suter M, Dorta G, Giusti V, Calmes JM. Gastro-esophageal reflux and esophageal motility disorders in morbidly obese patients. Obes Surg 2004;14(7):959–66. [2] Tai CM, Huang CK, Lee CY, Chang CY, Lee CT, Lin JT. Increase in gastroesophageal reflux disease symptoms and erosive esophagitis 1 year after laparoscopic sleeve gastrectomy among obese adults. Surg Endosc 2013;27:1260–6.
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Original article
Evaluation of gastroesophageal reflux before and after sleeve gastrectomy using symptom scoring, scintigraphy, and endoscopy Aditya Sharmaa, Sandeep Aggarwala,*, Vineet Ahujab, Chandrashekhar Balb,c a
Departments of Surgical Disciplines, All India, Institute of Medical Sciences (AIIMS), New Delhi 110029, India b Gastroenterology, All India, Institute of Medical Sciences (AIIMS), New Delhi 110029, India c Nuclear Medicine, All India, Institute of Medical Sciences (AIIMS), New Delhi 110029, India
Abstract
Background: The effect of laparoscopic sleeve gastrectomy (SG) on gastroesophageal reflux disease (GERD) has been a controversial issue. There have been limited studies on this aspect and most of the published studies are retrospective. Therefore, a prospective study was designed to objectively assess the problem. The objective of this study was to assess the impact of SG on symptoms of gastroesophageal reflux using questionnaire, endoscopy, and radionuclide scintigraphy. Methods: Thirty-two patients undergoing laparoscopic sleeve gastrectomy were assessed for gastroesophageal reflux using Carlsson Dent Questionnaire and GERD questionnaire before and after surgery at three monthly intervals. They were also subjected to upper GI endoscopy (UGIE) and radionuclide scintigraphy both pre- and postoperatively. Results: Mean preoperative weight and body mass index were 126.5 kg and 47.8 kg/m2, respectively. Mean percent excess weight loss at 12 months was 64.3 ⫾ 18.4. Both the Carlsson Dent Score (CDS) and Severity Score (SS) exhibited a decline from 2.88 to 1.63 (p o 0.05) and 2.28 to 1.06 (p o 0.05), respectively after 12 months. Radionuclide scintigraphy revealed a significant rise of GERD from 6.25% to 78.1% in the postoperative period (p o 0.001). UGIE showed a rise in incidence of esophagitis from 18.8% to 25%; however, there was improvement in all patients except one in terms of reduction of severity of esophagitis. Conclusion: Presence of GERD may not be considered as a contra-indication for sleeve gastrectomy. There is improvement of GERD as assessed by symptom questionnaires, as well as improvement in grade of esophagitis. The new onset GERD detected on scintigraphy may not be pathologic as there is a decrease in total acid production postsurgery; however, it still remains an important issue and needs long-term follow-up. (Surg Obes Relat Dis 2014;]:00–00.) r 2014 American Society for Metabolic and Bariatric Surgery. All rights reserved.
Keywords:
Sleeve gastrectomy; Gastroesophageal reflux; Endoscopy; Scintigraphy
Morbidly obese patients have an increased prevalence of reflux symptoms and esophagitis [1]. The presence of gastroesophageal reflux disease (GERD) in such patients may affect the choice of weight loss procedure. Roux-en-Y * Correspondence: Dr Sandeep Aggarwal, Professor, Department of Surgical Disciplines, All India Institute of Medical Sciences (AIIMS), New Delhi 110029, India. E-mail: [email protected]
gastric bypass has been favored by some over sleeve gastrectomy (SG) in morbidly obese patients with GERD [1]. The effect of SG on GERD has been one of the points for criticism of the procedure; however, there is a paucity of prospective studies which have analyzed the problem of GERD after SG as a primary endpoint [2–7]. SG has carved its own niche as a sole weight loss procedure and has been rapidly adopted by surgeons worldwide [8–11] . Besides excellent weight loss, SG results in remarkable resolution/
http://dx.doi.org/10.1016/j.soard.2014.01.017 1550-7289 r 2014 American Society for Metabolic and Bariatric Surgery. All rights reserved.
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69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 QF1 86 Q6 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 T1 102 T2 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 122 123
Thirty-five patients undergoing laparoscopic sleeve gastrectomy for morbid obesity were enrolled for the study and followed up for one year. We followed the standard National Institutes of Health Guidelines, which included patients with morbid obesity, defined as Body Mass Index (BMI) 440 kg/m2, patients with BMI 435 kg/m2 with obesity related co-morbidities. Patients with symptomatic GERD and/or hiatus hernia were not excluded fig. 1. A detailed preoperative evaluation was done. The sleeve was created in the standard fashion over a 36-F bougie starting at 4–5 cm from pylorus. The staple line was not reinforced. Hiatal hernia, if present, was not repaired in any of the patients as it was deemed small in all patients.
of 4 seven was considered to have GERD. The copyrights registration for both the questionnaires were done and submitted to the ethics committee of the institute. The study was approved by the institutional ethics committee (Ref no.269/01.07.2011). Patients were followed up at three monthly intervals and at each visit symptom questionnaires were administered and scores were documented. Additionally, all patients underwent upper gastrointestinal endoscopic (UGIE) examination and scintigraphy in the preoperative period as well as at six months after SG. On UGIE, severity of esophagitis was graded according to the Los Angeles (LA) scoring system on a scale from A through D [19]. For scintigraphy, a validated method for the objective study of GERD [6,20], the patients were given a capsule containing the radioactivity at a dose of .5 mci in the form of Tc99-labeled sulfur colloid. It was followed by 400 milliliters (mL) of orange juice. Data acquisition was carried out with a frame rate of 10 s/frame for 15 min. The GERD index was be calculated as follows: Background corrected esophageal counts/Background corrected total gastric counts 100%. A GERD index of Z4 was used as the cutoff to determine positivity for GERD. The result was noted as presence or absence of reflux.
Evaluation of gastroesophageal reflux (GER) symptoms
Statistical analysis
For the purpose of the study, all patients underwent assessment of reflux symptoms using two different questionnaires; GERD questionnaire [16,17] to assess Symptom-Severity (SS) score and Carlson Dent selfadministered questionnaire [18]. The GERD questionnaire uses a grading of symptoms of heartburn and regurgitation (Table 1). A severity score Z4 is considered positive for GERD. The Carlsson Dent Questionnaire (Table 2) was given to the patient and the Carlsson Dent Score (CDS) was calculated from the responses given. A patient with a score
All data were prospectively collected and continually updated in a computer database using the Microsoft Office Excel program, and then analyzed using STATAv12 and IBM SPSS v20 (data analysis and statistical software). Data was analyzed first by using descriptive statistics. The pairwise comparison at 12 months was done for CDS and SS using related samples Wilcoxon signed rank test. McNemar test was applied to see the changes in qualitative data. Differences were considered statistically significant for p-values o .05.
improvement of co-morbidities among morbidly obese individuals [10–15]. Since the impact of SG on GERD remains an unresolved issue, this prospective study was undertaken to objectively determine the problem of reflux in patients undergoing SG using symptom questionnaires, radionuclide scintigraphy, and upper gastrointestinal endoscopy (UGIE). Methods
8.00 7.00 6.00 5.00 4.00 3.00
W 2.00
2.88 2.28
3.09 2.16
2.81 1.81
2.38 1.63
1.50 E 1.06 B 1.00 4 0.00 C Pre op 3m 6m 9m 12m / -1.00 F P -2.00 O Fig. 1. Trend of mean Carlsson Dent Score (CDS) and mean Severity Score (SS) of patients
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179 180 Q9 181 182 183 184 185 186 187 188 189 190 191 192 193 194 195 196 197 198 199 200 201 202 203 204 205 206 207 208 209 210 211 212 213 214 215 216 217 218 T3 219 220 221 222 223 224 225 226 T4 227 228 T5 229 230 231 232 233
Table 1 Symptom score (SS) Severity of symptoms of heartburn and regurgitation Grade 0: No symptoms. Grade 1: Mild symptoms with spontaneous remission. No interference with normal activity and sleep. Grade 2: Moderate symptoms with spontaneous, but slow, remission. Mild interference with normal activity and sleep. Grade 3: Severe symptoms without spontaneous remission. Marked interference with normal activity and sleep. Frequency of symptoms of heartburn and regurgitation Grade 0: Absent. Grade 1: Occasional (o 2 days per week). Grade 2: Frequent (2 to 4 days per week). Grade 3: Very frequent ( 4 4 days per week). The final score for each symptom was obtained by multiplying the scores for severity and frequency. The total score was obtained by adding the final scores of individual symptoms and noted as Symptom Score (SS).
Results Out of 35 patients, two patients did not meet scheduled follow up appointments and one patient refused UGIE in follow up. These three patients were excluded from the analysis. Of the 32 patients, 22 (68.8%) were females. Mean age for the patient population was 35.8 years (range-19–60). Mean preoperative weight and BMI were 126.5 kg and 47.8 kg/m2, respectively. Mean percent excess weight loss at 3 months, 6 months, 9 months, and 12 months was 22.7 ⫾ 7.4, 38.8 ⫾ 11.1, 50.02 ⫾ 15.4, and 64.3 ⫾ 18.4, respectively. Carlsson Dent Score (CDS) varied from –2 to 13. GERD Symptom score (SS) varied from 0 to 12. There was a statistically significant decrease in mean values of both CDS from 2.88 to 1.63 (p o 0.05) and SS from 2.28 to 1.06 (p o 0.05), respectively, after a 12 month period. Moreover, out of five patients who had CDS 47 suggestive of reflux preoperatively, only three patients had a CDS 47 at 12 months after surgery suggesting improvement. Similarly, out of eight patients who had SSZ4 (positive for GERD) in the preoperative only three patients had a SS Z4 at 12 months after surgery (Table 3). Esophagogastroduodenoscopy was done preoperatively and postoperatively at six months. Preoperatively six (18.8%) patients had esophagitis with 50% being LA grade B. Postoperatively the incidence of esophagitis increased to 25% (8/32), but this rise was not statistically significant. Moreover, there was improvement in five patients in terms of reduction of LA grading including one patient with resolution of esophagitis (Table 4). The preoperative and postoperative symptom scores of these five patients are depicted in Table 5. Eight patients (25%) were identified as having an hiatal hernia, which were all small on preoperative endoscopy and 11 (34.4%) patients showing hiatal hernia, all small, in postoperative period. Thus, three patients developed new onset hiatal hernia in the postoperative period.
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Out of 32 patients, 30 patients had no reflux on scintigraphy preoperatively. Twenty- four (80%) of these 30 patients presented with new onset GERD on scintigraphy done at six months after surgery. Preoperatively scintigraphic reflux was documented in only two (6.25%) patients. One of these patients exhibited resolution. Postoperatively the incidence of reflux significantly increased to 78.1% (25/32) (p value o 0.001). Discussion The problem of reflux after SG is an unresolved issue. Various studies have displayed conflicting outcomes Table 2 Carlsson Dent Questionnaire It is a self-administered questionnaire, kindly tick the appropriate choice 1. Which one of these four statements BEST DESCRIBES the main discomfort you get in your stomach or chest? (5) A burning feeling rising from your stomach or lower chest up toward your neck. (0) Feelings of sickness or nausea. (2) Pain in the middle of your chest when you swallow. (0) None of the above, please describe below: 2. Having chosen one of the above, please now choose which one of the next three statements BEST DESCRIBES the timing of your main discomfort? (–2) Any time, not made better or worse by taking food. (3) Most often within 2 hours of taking food. (0) Always at a particular time of day or night without any relationship to food. 3. How do the following affect your main discomfort? Worsens Improves No effect/Unsure (a) Larger than usual meals (1) (1) (0) (b) Food rich in fat (1) (1) (0) (c) Strongly flavored or spicy food (1) (1) (0) 4. Which one of the following BEST DESCRIBES the effect of indigestion medicines on your main discomfort? (0) No benefit (3) Definite relief within 15 minutes (0) Definite relief after 15 minutes (0) Not applicable (I don’t take indigestion medicines) 5. Which of the following BEST DESCRIBES the effect of lying flat, stooping, or bending on your main discomfort? (0) No effect (1) Brings it on or makes it worse (–1) Gives relief (0) Don’t know 6. Which of the following BEST DESCRIBES the effect of lifting or straining (or any other activity that makes you breath heavily) on your main discomfort? (0) No effect (1) Brings it on or makes it worse (–1) Gives relief (0) Don’t know or this does not apply to me 7. If food or acid-tasting liquid returns to your throat or mouth what effect does it have on your main discomfort? (0) No effect (2) Brings it on or makes it worse (0) Gives relief (0) Don’t know or this does not apply to me The figures in parenthesis shows score for individual response. Total score is calculated by adding the individual score of each question.
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289 290 291 292 293 294 295 296 297 298 299 300 301 302 303 304 305 306 307 308 309 310 311 312 313 314 315 316 317 318 319 320 321 322 323 324 325 326 327 328 329 330 331 332 333 334 335 336 337 338 339 340Q10 341 342 343
Table 3 Number of patients positive and negative for GER based on two questionnaires
Table 5 Symptom scores of patients who showed improvement in endoscopic esophagitis grade
Questionnaire Score
Preoperative 3 months
6 months
9 months
12 months
Patient
E0
E6
SS0
SS6
CDS0
CDS6
CDS 4 7 CDS r 7 SS Z 4 SS o 4
5 27 8 24
4 28 4 28
5 27 3 29
3 29 3 29
1 2 3 4 5
B A D B C
A Absent A A A
6 2 8 8 2
2 2 2 2 2
11 3 5 4 5
0 4 3 7 2
4 28 7 25
CDS ¼ Carlsson Dent Score. SS ¼ Severity Score.
[2–7,18,19,21–26]. Braghetto et al. [6] analyzed data from 167 patients using a clinical questionnaire and found 27.5% patients (46/167) had reflux symptoms after SG. They have not documented the preoperative incidence of reflux. Three of their patients developed vomiting and were found to have stricture in the postoperative period. We had no incidence of stricture in our patient population. Tai et al. [2] used the Reflux Disease questionnaire in 66 patients with a median follow up of 12 months and found an increase in the prevalence of GERD after SG, from 12.1% to 47 %. In a similar study of 28 patients by Howard et al. [21] symptombased questionnaire was administered four weeks postoperatively to patients. New onset GERD symptoms were found in 22% of the patients. They concluded that SG might increase the prevalence of GERD symptoms. The primary aim of the study was to compare the symptoms of GERD using questionnaires before and after LSG. Our study reveals that there is a statistically significant decline in incidence of GERD symptoms as reflected by decrease in mean values of both CDS and SS from 2.88 to 1.63 (p o 0.05) and 2.28 to 1.06 (p o 0.05), respectively. This is in contrast to the above mentioned studies [2,6,21]. The maximum responses to the first question in the Carlsson Dent Questionnaire, which asks about the description of “main discomfort the patient feels in stomach or chest” in postoperative patients, was “none of the above.” Table 4 Table showing grade of endoscopic esophagitis before surgery and six months after surgery Postoperative grade (n) Pre operative grade (n)
None
LA-A
LA-B
Total
None LA-A LA-B LA-C LA-D Total
23 1 0 0 0 24
3 0 2 1 1 7
0 0 1 0 0 1
26 1 3 1 1 32
P value ¼ 0.2873. *Esophagitis grade using Los Angeles System. LA - A - Mucosal break o 5 mm in length. LA - B - Mucosal break 4 5 mm. LA - C - Mucosal break continuous between 4 2 mucosal folds. LA - D - Mucosal break 4 75% of esophageal circumference.
E0 ¼ Los Angeles esophagitis grade—Preoperative. E6 ¼ Los Angeles esophagitis grade—Postoperative at 6 months. SS0 ¼ Severity Score—Preoperative. SS6 ¼ Severity Score—Postoperative at 6 months. CDS0 ¼ Carlsson Dent Score—Preoperative. CDS6 ¼ Carlsson Dent Score—Postoperative at 6 months.
Upon asking further for a description of the discomfort it was either postprandial ”belching” or ”difficulty swallowing” rather than a ”burning feeling rising.” Similar to our study, Carabotti et al. [22] found that postprandial distress (PDS) rather than GERD is the main complaint post-SG. Using the Rome III criteria symptom questionnaire for upper GI symptoms in 97 patients who underwent SG, they found that before SG 52.7% patients were asymptomatic, 27% had GERD symptoms, 5.4% PDS, and 2.7% had epigastric pain symptoms. After median follow up of 13 months, 91.9 % patients complained of upper GI symptoms with prevalence of PDS being 59.4%. SG was associated with de novo dyspepsialike syndrome, with an OR of 7.00 (95 % CI 2.9 –18.3, p o .0001). On the other hand, the prevalence of GERD before and after surgery was not different (OR ¼ 1.083, 95 % CI .4652–2.530, p 4 .05). The symptom that was strongly related to SG was dysphagia (OR-4.7) (incidence-19.7%) similar to our response for the CD questionnaire. They further state that GI symptoms did not have a great impact on quality of life as also mentioned by Howard et al. [21] Regarding scintigraphic changes there is only single study by Braghetto et al. [6] after SG, which reported the incidence of GERD to be 70%; however, they have not documented the reflux preoperatively. In our study the preoperative incidence of reflux documented on scintigraphy was 6.25 %. Postoperatively the incidence significantly increased to 78.1 %. The possible reasons for the reflux include loss of angle of His, tubulization of stomach leading to high intragastric pressure, and dissection at phrenoesophageal junction with loss or damage to sling fibers [6]. Though we have not done any pressure studies, we strongly feel that increased intragastric pressure is mainly responsible for the increased reflux. There have been two schools of thought regarding the effect of SG on GERD and proponents of both have cited valid reasons for favoring each one of them. The mechanism for improvement post-SG cited are faster gastric emptying, reduction in gastric reservoir function, alteration of antrum–duodenal motor complex, gastrointestinal
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399 400 401 402 Q8 403 404 405 406 407 408 409 410 411 412 413 414 415 416 417 418 419 420 421 422 423 424 425 426 427 428 429 430 431 432 433 434 435 436 437 438 439 440 441 442 443 444 445 446 447 448 449 450 451 452 453
hormonal modifications, decrease in intrabdominal pressure due to weight loss, decrease in total acid production, and an increase in lower esophageal sphincter pressure (LESP). The others claim modification of esophagogastric junction, converting it to a straight tubular segment, partial sectioning the sling fibers, increased intraluminal pressure, presence of hiatal hernia, and decreased LESP lead to worsening of GERD after SG. It is evident from above that issue of GERD after SG is a complex and unresolved problem. Braghetto et al. [6,23] also found a decrease in LESP: 14.2 ⫾ 5.8 mm of Hg to 11.2 ⫾ 5.7 mm of Hg at 26 months postoperatively, which might be responsible for this reflux; however, another study by Peterson et al. [24] on effect of SG on LESP and esophageal motility contradicts the above results. They found a significant increase in LESP from 8.4 mm of Hg to 21.2 mm of Hg in group of late postoperative patients ( 48 months post-SG) and 11 to 24 mm of Hg in other groups of early postoperative patients (six days). They further reviewed the video material of surgery and found the distance between the stapler line and the gastroesophageal junction affected the LESP. They concluded that SG significantly increases LES pressure and may be protective against GERD. In our study we have not done esophageal manometry and, thus, are unable to comment on the LESP; however, the reflux does increase significantly from 6.25% to 78.1% as evidenced by scintigraphy. Comparing the incidence of scintigraphic GERD and endoscopic esophagitis grade postoperatively it can be seen that the GERD is not translating to overt esophagitis in our study. The symptom scores also show significant reduction at 12 months. The plausible explanation could be the increase in pH potentially due to removal of two-thirds of the stomach and consequent reduction in parietal cell mass. Due to same reasons, the scintigraphic reflux is not leading to overt symptoms as assessed by the symptom scoring. A longer follow up period might be required to document esophageal changes and 24 hour pH studies and manometry will be required to resolve the issue of reflux content and pathogenicity. Del Genio et al. [25] performed 24-hour pH manometry and multichannel intraluminal impedance plus endoscopy before SG in 15 consecutive patients who had no preoperative symptoms of gastroesophageal reflux disease (GERD), hiatal hernia (HH), or Barrett's esophagus. One year after SG, LESP had not changed, but there were increased ineffective secondary waves with an increase in nonacid reflux during the day. They concluded that sleeve was an effective restrictive procedure that increased the postprandial reflux episodes but did not induce GERD. Moon et al. [26] have also attributed total acid reduction as a reason for a decrease in GERD after SG. Hiatus hernia is another important confounding factor. In our study, eight patients had a small hiatus hernia on preoperative endoscopy but only four of these had esophagitis. Two patients with LA-B and one with LA-A had improvement in the postoperative period with LA-B decreasing to LA-A and LA-A to no esophagitis. One
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patient had persistent LA-B. Postoperatively three additional patients developed a small hiatus hernia. Tai et al. [2] compared hiatal hernia and esophagitis before and after sleeve gastrectomy in 66 patients. The incidence of esophagitis increased from 16.7% to 66.7% and that of hiatal hernia increased from 6.1% to 27.3%.They also found hiatal hernia occurred at a higher rate in patients with esophagitis than without esophagitis. Daes et al. [3] found HH in 34 patients (25%) in the study cohort of 66 patients, of which 29 (85.3 %) had preoperative symptoms of GERD. They treated hiatal hernia by various surgical methods. At six months to one year follow up, only two patients had GERD symptoms. Thus, they concluded that careful attention to surgical technique can result in reduction in occurrence of GERD symptoms. Similar guidelines were provided in the consensus statement compiled by Rosenthal [27], which states that aggressive identification of hiatal hernia should be done intraoperatively and posterior repair should be done after the creation of sleeve gastrectomy; however, in our study, improvement in the grade of esophagitis occurred despite the hiatus hernia not being repaired. Our study has certain limitations, which include the subjective nature of the symptom scores, lack of availability of 24 hour pH monitoring, and the fact that the comparison of esophagitis grade, scores and scintigraphy has been done at six months and not at one year. Conclusion The problem of GERD after SG seems to be a complex issue. The patients are more concerned with dyspepsia and postprandial discomfort (PDS) rather than GERD. There is a statistically significant decrease in mean values of both symptom scores viz. CDS and SS after a 12 month period. All the patients, except one, with preoperative esophagitis on endoscopy improved after SG. Though a number of patients in our study have a new onset GERD detected on scintigraphy, it may not be pathologic as there is reduction in subjective symptomatology and quantified esophagitis grade. So does SG constitute a contraindication for patients with GER? The answer based on the above facts seems to be no. Thus, the presence of esophagitis on endoscopy or symptoms attributed to GERD may not be considered as a contraindication for SG; however, the results of scintigraphy are a cause for concern and long term follow-up is required. References [1] Suter M, Dorta G, Giusti V, Calmes JM. Gastro-esophageal reflux and esophageal motility disorders in morbidly obese patients. Obes Surg 2004;14(7):959–66. [2] Tai CM, Huang CK, Lee CY, Chang CY, Lee CT, Lin JT. Increase in gastroesophageal reflux disease symptoms and erosive esophagitis 1 year after laparoscopic sleeve gastrectomy among obese adults. Surg Endosc 2013;27:1260–6.
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