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Heart, Lung and Esophageal Surgery Institute, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania
Accepted for publication June 1, 2007.
* Address correspondence to Dr Luketich, Heart, Lung and Esophageal Surgery Institute, University of Pittsburgh Medical Center, 200 Lothrop St, Pittsburgh, PA 15232 (Email: luketichjd{at}upmc.edu).
Presented at the Forty-third Annual Meeting of The Society of Thoracic Surgeons, San Diego, CA, Jan 29–31, 2007.
| Abstract |
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Methods: A retrospective review identified scleroderma patients who underwent surgical management of GERD from 1995 to 2006. Complications and reinterventions were recorded. Symptom control was assessed by validated questionnaires that measured dysphagia (0 to 5; 0 = no dysphagia), GERD–heartburn-related quality of life index (0 to 45; 0 = best, 45 = worst), and overall quality of life with the Medical Outcomes Study 36-Item Short Form Health Survey.
Results: Twenty-three scleroderma patients underwent surgical treatment for GERD (fundoplication, n = 10; RYGBP, n = 8; esophagectomy, n = 5). One patient died after esophagectomy and major morbidity occurred in 3 of the remaining 4 patients. No major complications occurred in any patient undergoing either fundoplication or RYGBP. Eighteen patients underwent evaluation by questionnaire at a median of 21 months postoperatively. Decreased dysphagia (0.42 versus 1.86, p = 0.05) and improved control of reflux (GERD–heartburn-related quality of life index score 4 versus 15.6, p = 0.05) were observed in the RYGBP patients compared with those undergoing fundoplication.
Conclusions: A high complication rate was seen among patients undergoing esophagectomy. Both reflux control and dysphagia rates were improved in the RYGBP group compared with fundoplication. This finding suggests that RYGBP may be an option for the primary management of scleroderma-associated gastroesophageal reflux.
| Introduction |
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The mechanism of reflux in scleroderma patients is multifactorial (see Fig 1). The two primary causes are an aperistaltic esophagus that is unable to clear physiologic reflux and an incompetent lower esophageal sphincter (LES). In many patients, no LES can be identified on manometry, and the esophagus and stomach essentially form a common cavity. In these cases, any increase in abdominal pressure will lead to esophageal reflux. Gastric dysmotility is also frequent in this disease and contributes to both alkaline and acid reflux into the esophagus. Finally, scleroderma patients have impaired production of saliva that is necessary to neutralize acid reflux.
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| Patients and Methods |
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Surgical Management
All patients who underwent surgical management of esophageal scleroderma were included in this study. Patients underwent a variety of surgical procedures, including esophagectomy, laparoscopic fundoplication with and without gastroplasty, and laparoscopic RYGBP. This review encompassed the clinical activities of seven thoracic surgeons, and the choice of procedure was one of individual preference. However, we have preferentially offered RYGBP in the latter half of this study. This practice reflects our increasing experience with RYGBP in the setting of redo antireflux surgery [5], as well as our concern that fundoplication or esophagectomy provided suboptimal GERD control in scleroderma patients.
The selection of patients for antireflux surgery was based on either failure of antisecretory medications to control symptoms of gastroesophageal reflux or the presence of erosive esophagitis or stricture despite optimal medical therapy. Patients whose symptoms of reflux were adequately controlled with medication were not included in this report. Patients selected for surgery underwent endoscopy, manometry, and a barium esophagram. We did not routinely obtain 24-hour pH studies if patients had typical symptoms of gastroesophageal reflux and there was evidence of reflux either on the barium esophagram or mucosal injury seen on endoscopy.
Our surgical techniques for laparoscopic Nissen fundoplication [6], Collis gastroplasty [7], and minimally invasive esophagectomy [8], have been described previously. For scleroderma patients, a floppy fundoplication was performed over a large-size bougie (54F to 60F).
The technique for laparoscopic RYGBP in scleroderma patients has been modified from our standard procedure used in patients with morbid obesity (Fig 2) [9]. In brief, all procedures were performed laparoscopically, even for patients who required oxygen supplementation for pulmonary fibrosis. A retrocolic, retrogastric Roux-en-Y gastrojejunostomy was created. In contrast to patients with morbid obesity, a larger, less restrictive gastrojejunal anastomosis was created. This was performed in an end-to-side fashion using either a 28-mm circular stapler or a 45-mm linear stapler. Another modification was the routine placement of a gastrostomy tube in the gastric remnant. The gastrostomy tube was used for nutritional support after discharge and was removed after several weeks. Finally, to minimize the degree of malabsorption, the length of the Roux limb was limited to less than 100 cm. In contrast, the Roux limb in morbidly obese patients is typically 150 cm.
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Statistical Methods
The hypothesis of this study was that RYGBP would lead to a lower incidence of dysphagia and equal control of reflux compared with fundoplication. Comparison between these two groups was performed using the
2 test for categorical variables (for example, the presence or absence of dysphagia or bloating). A two-tailed t test was used for comparison of continuous variables (GERD-HRQOL scale or the dysphagia severity scale).
| Results |
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Patient characteristics are presented in Table 1. Preoperative heartburn and dysphagia were present in 96% and 61% of patients, respectively. Preoperative endoscopy revealed erosive esophagitis in 57% of patients. Stricture and Barretts esophagus were each present in 13% of patients. Nineteen patients (83%) underwent preoperative manometry: a hypotensive LES was documented in 11 of these patients (58%), and aperistaltis of the esophageal body in 15 (79%). There was no statistical difference in the frequency of stricture or esophageal aperistalsis between surgical groups.
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Surgical Management and Complications
Esophagectomy was performed in a total of 5 patients (open transhiatal, 2; minimally invasive esophagectomy, 3). In 1 of these patients, the esophagus was considered unsalvageable owing to a fibrotic stricture that did not respond to repeated dilations. In the remainder, esophagectomy was recommended by the individual surgeon although a long-segment stricture was not present. One patient with significant pulmonary hypertension died of intractable right heart failure after esophagectomy. Among the remaining 4 patients, pneumonia developed in 3, anastomotic leak in 1, and chylothorax that required thoracotomy in 1. One patient required a tracheostomy for respiratory failure. Two patients required subsequent dilation for anastomotic stricture.
Fundoplication was performed in 10 patients, and a RYGBP in 8 patients (see Table 1). All procedures were performed laparoscopically with no conversions to an open procedure. There were no major complications after these procedures. After RYGBP, 1 patient required anticoagulation therapy for the treatment of atrial fibrillation, and another patient required dilation of an anastomotic stricture.
Weight Loss After Roux-en-Y
The mean body mass index (BMI) of patients undergoing RYGBP was 32.3. Three patients were considered morbidly obese with a BMI above 35. In these patients, a longer limb bypass (>100 cm) was created. At 6-month follow-up, the mean BMI was 27 (84% of the preoperative BMI). Weight loss was greater at 6 months among patients with a longer limb bypass (77% of preoperative BMI).
Long-Term Follow-Up and Quality of Life Outcomes
Long-term follow-up was available for 18 patients (esophagectomy, 4; RYGBP, 7; fundoplication, 7). Of the 5 patients without long-term follow-up, 3 had died and 2 could not be located. Median follow-up was 21 months for the entire cohort (range, 1 to 63). Median follow-up for the esophagectomy group was 14 months (range, 8–18), for the RYGBP group it was 13 months (range, 1 to 59), and for the fundoplication group it was 36 months (range, 1 to 64).
Within this period, 1 patient treated with fundoplication required conversion to RYGBP. This patient had undergone two prior fundoplications for the treatment of intractable reflux. Dysphagia developed after the second surgery and did not improve with dilation. The patient was subsequently converted to RYGBP with significant improvement in her dysphagia.
One patient had nausea, vomiting, and dysphagia after RYGBP. Dilation of a mild anastomotic stricture did not relieve these symptoms. A diagnostic laparoscopy was performed and showed no evidence of an internal hernia or other mechanical problem. Ultimately, it was thought that her symptoms were due to small bowel dysmotility from progressive scleroderma.
Functional outcome as measured by telephone questionnaire is outlined in Table 2. A lower incidence of diarrhea (p = 0.10) and bloating (p = 0.03) was noted in the RYGBP group compared to the fundoplication group. Importantly, both the presence (p = 0.01) and severity (p = 0.05) of dysphagia were significantly lower in the RYGBP group compared with the fundoplication group.
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| Comment |
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A significant obstacle to defining the optimal surgical therapy for scleroderma has been the rarity of the disease. Most surgical series are therefore small and report the outcomes of a single procedure. Another limitation in assessing outcome is the systemic nature of the disease. As a result patients may have a poor quality of life from progressive pulmonary disease or gastrointestinal dysmotility despite "successful" antireflux surgery.
With these limitations in mind, the present study compares outcomes after laparoscopic fundoplication, Roux-en-Y gastric bypass, and esophagectomy in patients with scleroderma-associated GERD. A total of 23 patients were identified over a 10-year period. Although the number of patients within each group is relatively small, this review represents the largest surgical series of scleroderma since the report of Orringer and coworkers [3] in 1981, a study that predated proton pump inhibitors. We would also note that this series originates from a center with a dedicated interest in esophageal disease, the management of end-stage lung disease (common in scleroderma patients), and the medical management of patients with rheumatologic disorders.
In the current series, perioperative complications were relatively high among patients treated with esophagectomy. In contrast, both fundoplication and RYGBP were performed without significant morbidity. These operations were performed laparoscopically despite the concern that abdominal cavity insufflation with carbon dioxide would not be tolerated in patients with pulmonary fibrosis.
Patients who underwent RYGBP were observed to have a statistically significant reduction in dysphagia and improved control of GERD symptoms compared with those who underwent fundoplication. Interestingly, RYGBP was not associated with an increase in other gastrointestinal symptoms such as abdominal bloating and diarrhea. Although the number of patients in each group of this study is relatively small, we believe these results are noteworthy. Scleroderma is a rare disease, and in the era of routine proton pump inhibitor use, a large esophageal center may see only one or two patients a year referred for antireflux surgery. Hence, it is unlikely that a larger single-institution series will be performed that compares outcomes among groups. A randomized study comparing RYGBP with fundoplication would require a multi-institutional approach of several specialized centers to yield a statistically significant result. A registry study would perhaps be able to resolve this issue, although it is not clear whether other centers have performed RYGBP for scleroderma patients.
The published literature on scleroderma-associated reflux is limited to relatively small series that do not compare the outcomes of one procedure over another (Table 3). In the largest series, 37 patients with scleroderma were treated with fundoplication and Collis gastroplasty [3]. Only 32% of patients complained of reflux postoperatively. Dysphagia was present in 38% of patients after surgery compared with 81% preoperatively. In the second largest study from Montreal, 14 patients underwent a variety of antireflux procedures [4]. Patients were followed postoperatively by barium swallow, endoscopy, and 24-hour pH studies. Pathologic reflux persisted in all patients by pH testing, although reduced by 50% in comparison with preoperative values. However, 71% of patients complained of dysphagia after surgery. Although these series document that acceptable long-term results can be achieved with fundoplication, one report has suggested otherwise. In a series of 11 patients from the Emory Clinic treated with fundoplication, reflux esophagitis recurred in every patient at a mean of 4 years postoperatively [15]. Esophagectomy with colon interposition was required in 3 of these patients. The authors of this study concluded that fundoplication was ineffective in the long-term management of scleroderma, and recommended esophagectomy as an alternative.
Esophagectomy is associated with significant morbidity, however. Furthermore, reflux may not be well palliated after esophagectomy. As many as 80% of esophagectomy patients suffer from pathologic reflux on the basis of pH studies [16]. Another concern with esophagectomy is that the small-vessel disease seen in scleroderma patients may lead to increased ischemia of the conduit, predisposing them to a higher rate of anastomotic leak and stricture.
Given these concerns, we propose that RYGBP is a reasonable alternative to esophagectomy. In contrast to esophagectomy, the mortality associated wiht RYGBP in large series is less than 1% [17]. And as we have shown in this series, the procedure can be performed laparoscopically in scleroderma patients with minimal morbidity. In addition to safety, the operation provides effective control of reflux by diverting gastric and duodenal secretions. Dysphagia is uncommon, although this may occur in the setting of an anastomotic stricture.
Although no reports of RYGBP in the setting of scleroderma have been published in the English language, the reflux control that can be obtained with this operation has been well documented. For instance, our group reported a series of 57 patients with morbid obesity and recalcitrant gastroesophageal reflux [18] who underwent RYGBP. At a mean follow-up of 18 months, all patients reported an improvement in reflux symptoms, and the mean GERD-HRQOL score was less than 1 (range, 0 to 45; 45 = worse symptoms). In a similar prospective study of 239 patients, 94% of patients noted an improvement in reflux symptoms at 9 months, and only 5% of patients required antireflux medications [19].
Certainly, no definitive conclusions can be drawn from the present study. The number of patients in each group was small, and that reflects the rarity of the disease. In addition, we could not document any difference in the overall quality of life between groups. In large measure, we believe, that is due to the progressive, systemic nature of the disease. For instance, several patients in this series had either received or were awaiting lung transplantation. Such severe lung disease would have a significant impact on quality of life, regardless of the adequacy of an antireflux procedure.
The length of follow-up is another potential limitation of this study. The median follow-up was longer in the fundoplication group than in the RYGBP group (36 months versus 13 months). It is possible that with longer follow-up the prevalence of dysphagia or recurrent reflux would increase among RYGBP patients. However, we believe that this is unlikely. Dysphagia after RYGBP is most often the result of an anastomotic stricture, which would be evident in the first few months after surgery. In regard to reflux, it would seem unlikely for symtoms to develop if they were well controlled in the first 2 years after RYGBP. In contrast, reflux can occur several years after fundoplication owing to anatomic disruption of the wrap.
Another issue not addressed in the present study is the success of medical management of scleroderma-associated reflux. Patients in this study were typically referred for antireflux surgery after they had either failed appropriate medical therapy or developed complications of reflux such as Barretts metaplasia or stricture. The number of patients with scleroderma whose symptoms of reflux were successfully treated by medication alone is not known. We would suspect that reflux symptoms are successfully managed in the majority of patients, given the small size of this surgical series.
In summary, we propose that RYGBP may be an acceptable alternative to fundoplication in patients with scleroderma-associated reflux. In this series, patients undergoing RYGBP were observed to have less dysphagia and improved control of reflux compared with the fundoplication group. Certainly, the small number of patients in this series does not allow any definitive treatment recommendations to be made. Ultimately, the choice of antireflux procedure will be based on individual surgeon and patient preference. In experienced centers, however, Roux-en-Y gastric bypass can be performed with very low morbidity and, we suggest, may lead to long-term palliation of reflux symptoms.
| Discussion |
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DR KENT: Yes.
DR WHYTE: Might that have been worse if you had not put a feeding tube in these people?
DR KENT: Thank you for your questions, Dr Whyte. I think that the major concern is palliation of symptoms, and of course scleroderma is an intractable and systemic disease. Dysphagia is a common symptom, and is often worse after fundoplication. So I think that dysphagia is relevant in assessing overall quality of life, but dysphagia is not the only issue. You also have to control heartburn, and we expected that we would show equal control of heartburn in the Roux-en-Y and fundoplication groups. In fact, it seemed that heartburn control was better after Roux-en-Y.
In terms of your second question, surprisingly, a significant number of patients in this study were obese. In fact, 3 of the 8 patients in the Roux-en-Y group were morbidly obese. In those patients, we constructed a longer limb bypass, with the expectation that they would lose some weight. So in the 5 patients who were not obese, the weight loss was far less.
DR WHYTE: Was early satiety a complaint that these people had after this, with such a small gastric remnant?
DR KENT: It was to a degree. One patient had a stricture after Roux-en-Y, and that did lead to some early satiety. An additional patient had significant nausea and vomiting after Roux-en-Y, and this was thought to be due to progressive bowel dysmotility. So scleroderma is a chronic, systemic disease, and very often symptoms progress despite an adequate operation.
DR MALCOLM M. DECAMP (Boston, MA): Excellent and elegantly-presented work. Sixty percent of your patients were lung transplant candidates. We know now over the last 5 years or so that there has been quite a large body of evidence favoring preemptive fundoplication before transplantation to improve posttransplant outcome and decrease the incidence of obliterative bronchiolitis. How many of these patients were able to go on to transplantation, and do you have any follow-up in terms of their transplant-related outcomes?
DR KENT: Thank you, Dr DeCamp. A total of 5 patients underwent pulmonary transplantation, 1 patient before antireflux surgery and 4 postoperatively. Among these 5 patients, 4 are doing well in terms of allograft function, and 1 died 2 years after transplant of bronchiolitis obliterans. I do agree with you that the data showing the importance of reflux control before transplantation are very strong, and we have been seeing more of these patients referred to us pretransplantation in order to address reflux.
DR DECAMP: As a follow-up to that, does your program consider an immotile esophagus a contraindication to transplantation?
DR KENT: No.
DR DECAMP: How do you document control of reflux after your operation before listing? I would suggest that the quality of life parameters probably arent stringent enough in that population.
DR KENT: I agree. I think that for most patients who are not undergoing transplantation, quality of life measures are sufficient. I think for patients who are anticipating transplantation, objective documentation of reflux control is important, such as with 24-hour pH studies.
| References |
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This article has been cited by other articles:
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N. J. Sheehan Dysphagia and other manifestations of oesophageal involvement in the musculoskeletal diseases Rheumatology, June 1, 2008; 47(6): 746 - 752. [Abstract] [Full Text] [PDF] |
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