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Heart, Lung and Esophageal Surgery Institute, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania
Accepted for publication April 28, 2008.
* Address correspondence to Dr Luketich, Heart, Lung, and Esophageal Surgery Institute, University of Pittsburgh Medical Center, 200 Lothrop Street, Pittsburgh, PA 15232 (Email: luketichjd{at}upmc.edu).
Presented at the Forty-fourth Annual Meeting of The Society of Thoracic Surgeons, Fort Lauderdale, FL, Jan 28–30, 2008.
| Abstract |
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Methods: A retrospective review from 1995 to 2007 identified patients who developed either a diaphragmatic hernia or a redundant gastric conduit after esophagectomy. The presenting symptoms, operative approach, and outcomes after surgery were recorded.
Results: Forty-three patients (representing 4% of the esophagectomy volume in this time period) were identified with a diaphragmatic hernia (n = 21), redundant gastric conduit (n = 19), or both (n = 3). Mean time from esophagectomy to diagnosis was 32 months for diaphragmatic hernia and 18 months for redundant conduit. The majority of hernias occurred to the left of the gastric conduit. A mechanical obstruction to gastric emptying was noted in 54% of patients with a redundant conduit. Forty patients underwent revisional surgery (minimally invasive: 35; open: 5). The recurrence rate after repair of a diaphragmatic hernia was 29%. Symptoms improved in 85% of patients after revision of a redundant conduit.
Conclusions: A diaphragmatic hernia or redundant conduit may occur years after esophagectomy. Hernias almost always occur adjacent to the greater curve of the stomach. The development of a redundant conduit may be associated with a functional outflow obstruction. Surgical correction of these conditions can alleviate symptoms in the majority of patients.
| Introduction |
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However, a small number of patients may develop symptoms months or years after their esophagectomy, and the cause may be surgically correctable. Two such conditions are the following: (1) a diaphragmatic hernia in which bowel herniates into the chest (Fig 1); and (2) a redundant conduit that impairs gastric emptying (Fig 2). The development of these conditions may be insidious and symptoms ascribed to the normal constellation of complaints that occur after esophagectomy. In this report we review our experience with the management of these late postesophagectomy complications. The anatomic basis of these conditions, their clinical presentation, and the results of operative correction are discussed.
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| Patients and Methods |
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Esophagectomy Technique
This review encompassed the clinical activities of five thoracic surgeons at the University of Pittsburgh Medical Center. A minimally invasive esophagectomy (MIE) was preferred by four of these five surgeons. The MIE procedure has been well-described in previous publications [4, 5]. The operation involves thoracoscopic mobilization of the esophagus, laparoscopic pyloroplasty, creation of a 5- to 6-cm-wide gastric tube, and a cervical esophagogastric anastomosis. In general, division of the left crus was performed to enlarge the hiatus and accommodate the gastric conduit. However, the decision to enlarge the hiatus was individualized. For example, division of the crura was not performed in patients with a large, preexisting hiatal hernia. After creation of the anastomosis, traction was gently applied to the distal stomach to reduce excess conduit into the abdomen. Three stitches were then placed between the conduit and the diaphragm to prevent postoperative herniation. These stitches were placed at the 3 o'clock position (between the greater curve of the conduit and the left crus), at the 12 o'clock position, and at the 9 o'clock position (between the lesser curve of the conduit and the right crus). A subset of patients in this study underwent a minimally invasive Ivor Lewis esophagectomy, in which a high thoracic anastomosis is constructed [6]. Other than the location of the anastomosis, the conduct of the operation was similar to the standard MIE procedure.
An open transhiatal esophagectomy was preferred by one surgeon in this study (RL). In this procedure whole stomach was used as a conduit, and a pyloromyotomy was routinely constructed. Three stitches were placed between the conduit and diaphragm similar to a standard MIE procedure.
Evaluation of Patients With a Diaphragmatic Hernia
After esophagectomy patients undergo routine CT scans to detect disease recurrence. The presence of a diaphragmatic hernia on CT scan was sufficient to recommend operative repair, even if the patient was asymptomatic. Recurrence of esophageal cancer was carefully ruled out using CT and positron emission tomography scans as appropriate before revisional surgery was considered.
Evaluation of Patients With a Redundant Conduit
We hypothesized that a redundant conduit may develop from one of four possible causes. The first cause would be excess conduit that was left above the diaphragm during the initial esophagectomy (Fig 3). This redundancy should be demonstrated on the immediate postoperative barium swallow. The horizontal portion of the gastric conduit above the diaphragm would impair emptying, ultimately leading to symptoms of regurgitation and aspiration.
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| Results |
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In the time period of this study, 1,075 esophagectomies were performed at our institution (MIE: 581; open: 494). Therefore, the incidence of a diaphragmatic hernia at our institution was 2.8% (16 of 581) after MIE, compared with 0.8% (4 of 494) after open esophagectomy.
The indication for esophageal resection in these 24 patients were as follows: benign disease (n = 1); high-grade dysplasia (n = 6); and invasive esophageal cancer (stage I: 1; stage IIA:5; stage IIB:3; stage III: 8).
The diaphragmatic hernia was asymptomatic in four patients (17%). Abdominal pain was the most common presenting symptom (45%), followed by dyspnea and dysphagia (15% each) and constipation and nausea (10% each). Mean time to diagnosis was 32 months after esophagectomy (range, 46 days to 7 years).
In 21 (87%) of these patients, the hernia was located to the left of the gastric conduit and abdominal contents herniated into the left chest. The colon was the most commonly herniated organ (92%) followed by small bowel (21%). In 3 patients (13%) the hernia was posterior to the gastric conduit. Interestingly, in all of these patients abdominal contents herniated into the right chest.
Among these 24 patients, all except 2 underwent operative repair. One patient had known recurrence of his esophageal cancer and developed peritoneal carcinomatosis soon after the hernia was diagnosed. The other patient was asymptomatic and only pancreas and retroperitoneal fat had herniated across the hiatus.
The operation was performed electively in 18 patients (82%) and urgently for obstructive symptoms in 4 patients (18%). The surgical approach was through laparoscopy in 17 patients (77%) and a laparotomy in 5 (23%). Two of the laparoscopic cases (12%) were converted to an open procedure secondary to adhesions. In all of these cases the hernia was reduced into the abdomen and additional sutures were placed between the conduit and the diaphragm. In 9 patients (41%) this repair was reinforced by mesh (Surgisis Gold mesh [Cook Biotech Incorporated, West Lafayette, IN], n =5; Gore Tex [W.L. Gore Assoc, Flagstaff, AZ] buttress, n=1).
No perioperative complications occurred in 16 patients (73%). Minor complications included atrial fibrillation (9%), ileus (4.5%), pneumonia that resolved with antibiotics (4.5%), and pericardial effusion (4.5%). One death (4.5%) occurred in a patient who suffered a massive pulmonary embolism on postoperative day 3.
With a median radiographic follow-up of 13 months (range, 1 month to 9.8 years), 6 patients (29%) developed a recurrent hernia. The risk of recurrence was similar whether mesh was used or not (30% vs 27%). In every case, the recurrent hernia was located along the greater curve of the stomach. All of these patients underwent subsequent reoperation. The recurrence rate after the second operation was 33% (2 of 6).
Redundant Gastric Conduit
A total of 22 patients were identified with a redundant gastric conduit (including 3 patients also diagnosed with a diaphragmatic hernia). One patient had undergone an open transhiatal esophagectomy; the remainder had a minimally invasive esophagectomy (MIE with cervical anastomosis: 17, minimally invasive Ivor Lewis: 4). The overall incidence of this condition after MIE at our institution was 3.6%. Indications for esophagectomy were as follows: benign disease (n = 4), high-grade dysplasia (n = 8), and invasive esophageal cancer (stage 1: 2; stage 2A: 2; stage 2B: 1; stage 3: 5).
Symptoms were present in all of these patients. Dysphagia was the most common complaint (43%), followed by regurgitation (30%), reflux (26%) vomiting and aspiration pneumonia (22% each), and early satiety (9%). Mean time to diagnosis of a redundant conduit after esophagectomy was 18 months (range, 2 months to 2 years).
After review of CT scans and barium swallows, the cause of the redundant conduit was identified to be the following: excess conduit left above the diaphragm at the time of esophagectomy in 5 patients (23%), mechanical obstruction to emptying in 12 patients (54%), and a twisted conduit in 3 patients (14%). In 2 patients (9%) no anatomic basis could be identified. Among those with a mechanical obstruction, a narrow hiatus was the cause in 8 patients (36%) and pyloric obstruction in 4 (18%). Of the 4 patients with pyloric obstruction, 2 did not have a pyloroplasty and 2 developed a stricture after pyloroplasty.
Revisional surgery was performed in 21 of 22 patients. The other patient was offered surgery and refused. All of the operations were performed electively. Among these 21 patients, 1 underwent a planned laparotomy and the remaining 20 had a minimally invasive approach (laparoscopy: 15; laparoscopy and thoracoscopy: 5). Two patients (9%) required conversion to an open procedure due to adhesions. During surgery, attachments of the conduit to the mediastinum were divided and excess conduit was reduced into the abdomen. In our early experience this was done entirely through the abdomen. More recently, we have combined laparoscopy with thoracoscopy. In this way the conduit could be mobilized off the mediastinum under direct vision. During laparoscopy the excess conduit was reduced into the abdomen and sutured to the diaphragm.
No complications occurred in 17 patients (81%). Among the remaining four patients, three required early reoperation (bleeding: 1; chylothorax: 1; placement of endoscopic stent for persistent obstruction: 1). The fourth patient had both a diaphragmatic hernia and redundant conduit (previously discussed) and died from a pulmonary embolism on postoperative day 3.
With a median follow-up of 12 months (range, 1 to 64 months), no patient has undergone subsequent surgery to revise the conduit. Sixty-five percent of patients (13 of 20) experienced either complete resolution or minimal symptoms after revision. Twenty percent (4 of 20) of patients had improved but persistent symptoms. The remaining 3 patients (15%) had severe symptoms despite surgery. Reoperation was recommended, but refused by two of these patients. The final patient underwent repair of a twisted conduit. His symptoms did not improve and a stent was placed one month later. He was lost to follow-up and presented 18 months later with profound malnutrition, regurgitation, and pneumonia. Despite gastric decompression and antibiotics the patient died from aspiration pneumonia.
| Comment |
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Diaphragmatic hernia has been described as a rare complication after both open and minimally invasive esophagectomy. Including this series, a total of 58 patients have been reported in the literature. Previous publications consist of either case reports [8–18] or small series of between 2 to 9 patients [19–25]. In these reports the incidence of this complication ranges from 0.4% to 6% after open esophagectomy and 4% after minimally invasive esophagectomy.
In this series a diaphragmatic hernia was more common after minimally invasive compared with an open esophagectomy (2.8% vs 0.8%). It is likely that the greater degree of adhesions that form after laparotomy contribute to this difference. Consequently we feel it is critical to suture the conduit to the diaphragm with nonabsorbable stitches during minimally invasive esophagectomy. When these sutures are placed, the incidence of this complication after MIE (2.8%) would appear comparable with open esophagectomy series (0.4% to 6%).
The majority of hernias occurred to the left of the conduit, consistent with previous reports. One possible reason is that fewer adhesions form along the left crus, as this is in contact with the smooth, serosal surface of the stomach. In contrast, the right crus is adjacent to the lesser curve of the stomach, which has been stapled to fashion the gastric conduit [25]. The adhesions that form adjacent to this staple line may prevent a hernia in this location. Also, it should be noted that diaphragmatic hernias occur adjacent to the right gastroepiploic artery. We purposefully do not place tacking stitches in this area to avoid injury to this artery.
The principles of repairing a diaphragmatic hernia are similar to surgical management of a giant paraesophageal hernia. We believe it is important to completely mobilize the crura posterior to the conduit, so the hiatus can be closed without tension. A relaxing incision in the left hemidiaphragm may also be considered. The peritoneal lining of the crura should be preserved as this adds integrity to the repair.
Similar to paraesophageal hernias, the recurrence rate after repair of a diaphragmatic hernia is relatively high (30%). No previous series has provided data on the recurrence rate after repair. This high recurrence rate was present whether mesh was used or not. In cases where mesh is necessary we have preferred to use a biodegradable mesh (Surgisis Gold; Cook Medical). In the three patients who required reoperation after mesh repair, the mesh had completely reabsorbed and the hernia recurred along the greater curve of the stomach. It is possible that using a permanent mesh would lower the recurrence rate after repair. We have been reluctant to use permanent mesh, however, as we have seen this material erode into the esophagus after repair of paraesophageal hernias. One clear conclusion from the present series is that the physiologic force that drives hernia development (the pressure gradient from the abdomen to the chest) is difficult to abolish despite careful surgical technique.
A redundant conduit is another diagnosis that may lead to significant symptoms after esophagectomy. This condition is physiologically equivalent to end-stage achalasia. The horizontal portion of the conduit that lies above the diaphragm prevents emptying by gravity. Severe reflux and dysphagia may develop and are difficult to palliate with medical therapy. Recurrent aspiration may lead to profound morbidity, and even death. We have found that placement of endoluminal stents [26] and pharyngostomy tubes [27] are useful to temporize severe symptoms, but they rarely lead to durable relief.
Few reports in the literature discuss the development of a redundant conduit. A recent case report described two patients who underwent surgical revision of a redundant conduit after open Ivor Lewis esophagectomy [28]. In one patient the cause was an anastomosis that was performed to the midportion, rather than the proximal stomach. In the second patient a horizontal portion of the stomach above the diaphragm was identified and resected. Volvulus of the gastric conduit has also been separately described in case reports [26, 29].
In our analysis the cause of a redundant gastric conduit was mechanical in 54% of patients. For some patients mechanical obstruction occurred at the level of the pylorus, but for several patients the obstruction was external to the conduit, at the level of the hiatus. One explanation is that the relatively thin gastric conduit may dilate over time with the resumption of oral intake. Thus, a hiatus that appears to be of adequate size during esophagectomy may in fact be too small. We would note that this observation is far easier to make retrospectively than intraoperatively. Of the 1,075 esophagectomies performed at our institution during this study period, only 9 patients developed a redundant conduit from hiatal obstruction.
Volvulus of the gastric conduit is another extremely rare cause of outlet obstruction [30, 31]. In our experience this has been documented in only three patients. It is interesting to note that in each of these patients the degree of twist on CT scan was no more than 120 degrees. Yet these patients were profoundly symptomatic, with one death from aspiration pneumonia. It is possible that other factors related to vagotomy and subsequent gastric dysmotility may be relevant in these patients.
Revisional surgery to correct a redundant conduit is a challenging undertaking. These operations may be performed with minimally invasive techniques but the threshold to convert to an open procedure should be very low. Our initial approach to this condition was through the abdomen. Adhesions between the conduit and the mediastinum were divided through the hiatus, the redundant conduit was reduced into the abdomen, and the size of the hiatus was calibrated as necessary. With more experience we have found that a combined thoracic and abdominal approach is far safer. The conduit can be completely mobilized from the mediastinum through the chest, taking care to preserve the gastroepiploic artery. If the conduit is excessively dilated it can be restapled into a 5-cm gastric tube. The conduit is then brought down into the abdomen and tacked to the diaphragm either laparoscopically or with an upper midline incision.
Although diaphragmatic hernia and redundant conduit may seem unrelated, mismatch of the conduit to the hiatus may be the precursor for both conditions. The division of the phrenoesophageal membrane and creation of an iatrogenic hernia involving the gastric conduit places patients at risk for herniation of bowel across the hiatus. Enlargement of the hiatus substantially increases this risk [24]. On the other hand, a hiatus that is of insufficient size may lead to a progressive obstruction of the conduit with severe symptoms. The challenge is to calibrate the size of the hiatus to the individual patient to minimize the development of both of these complications.
It should be emphasized that these conditions are rare after esophagectomy. To a degree the incidence of these complications will reflect the population of patients who undergo esophageal resection. In our experience the diagnosis of a diaphragmatic hernia or redundant conduit was made 18 to 32 months after surgery. Only a minority of patients with locally advanced esophageal cancer will be expected to survive to this time point. Thus, these late complications will be more frequent in surgical series where a majority of patients have either benign disease or early stage esophageal cancer. In the present series 63% of patients were in this category.
In summary, both diaphragmatic hernia and a redundant gastric conduit may develop years after esophagectomy. The onset of new gastrointestinal complaints should prompt an evaluation for one of these diagnoses. Consideration should be given to repair of diaphragmatic hernias even if asymptomatic, as patients may present with acute symptoms of bowel obstruction. However, the recurrence rate after repair of these hernias is high. Patients with symptoms from a redundant gastric surgery may also require revisional surgery, as medical and endoscopic therapies rarely offer durable relief. Revisional surgery for both of these conditions is technically demanding and on occasion more than one reoperation may be required. Thus, every attempt should be made during esophagectomy to minimize the risk of developing one of these challenging, late complications.
| Discussion |
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With regards to your patients with diaphragmatic hernia, you had 22 patients who underwent revision surgery and there was a 30% recurrence rate. This is clearly a very difficult group of patients to deal with. What's your advice and tips for the audience who has to tackle such patients?
DR KENT: Thank you for your comments. As you noted this is a difficult operation. No prior series of diaphragmatic hernia has documented the recurrence rate after repair but certainly recurrences can develop.
We have tried to use mesh with the hope that mesh would prevent recurrences, and unfortunately they do not. This may reflect, in part, our preference to use absorbable mesh, given the concern that nonabsorbable mesh could lead to other complications, such as erosion into the gastric conduit.
A crucial point is that you have to completely reduce the hernia and close the crura without tension. So we do a lot of work posteriorly to get the crura to close without tension, if at all possible. One could consider a relaxing incision in the diaphragm if the crura are still under tension at the end of the operation. And finally you want to tack the conduit to the diaphragm as completely as possible.
I think one problem is that these hernias tend to recur where it is difficult to place tacking sutures. The recurrences develop along the greater curve of the stomach, precisely where the gastroepiploic artery is located, and damaging that would be catastrophic.
DR DANIEL L. MILLER (Atlanta, GA): The big thing that I read from this, and I think this is a good point, is whether you divide the left crura?
DR KENT: Typically we do.
DR MILLER: Yes, and I learned 12 years ago not to do that. And so we divide the right crura. And when you divide the right, it takes away that hinge point. It's more of a straight shot, and you don't leave all of that open to the left side. Because when you're going back to repair that, that's very difficult because you've taken down so much of that left crura. I don't care how much you close posteriorly, you're not going to narrow it down any.
I think that's one thing that I realized in your paper because Vic Trastek used to do both when we trained at Mayo, and then he got away from the left. Because we did, we had some hernias to go up, and that seemed to take care of it because it scarred down over time, and that also helped the redundant portion a lot.
DR KENT: Yes, I think that is a good point.
DR THOMAS J. WATSON (Rochester, NY): I want to congratulate you on a very nice presentation regarding a difficult subject, one that has not been very extensively discussed in the literature. There are a lot of pearls, I am sure, in your manuscript.
I have three brief questions for you. Like so many problems in surgery, the best way to deal with these complications is to prevent them. Have you made changes to your esophagectomy technique in Pittsburgh in an effort to prevent these recurrences, particularly the hiatal hernias?
Secondly, what do you do with the asymptomatic patient, someone on whom you get a CT (computed tomographic) scan or other radiologic study for whatever reason, and you find a small knuckle of bowel up through the hiatus? Do you feel that these herniations should all be fixed, especially in light of the significant recurrence rate after repair, or can you safely observe these people?
Third question: You have encountered several of these redo, redo procedures where the hernias keep coming back. Have you ever been in the situation where you have to take the posterior mediastinal stomach out, close the hiatus, and then bring up a substernal conduit? Thanks a lot.
DR KENT: Thank you very much, Dr. Watson. I think prevention is the critical issue because these redo operations are very challenging, and the morbidity of these complications can be very high. So the key issue is whether these can be prevented.
And I think that the answer is to a degree no; that these complications will be encountered in a busy esophageal practice. But reviewing our data has led to a lot of thought and discussion about how these complications can be minimized.
I think one issue in regards to the diaphragm is that you cannot omit the step of placing those tacking sutures. Without question, the incidence of diaphragmatic hernia will be higher if those sutures are not placed.
I think the recommendation to avoid dividing the left crus is a good one. And we pay great attention to calibrate the size of the hiatus to the conduit. So we do not enlarge the hiatus, for example, in patients with a large hiatal hernia. We may even partially close the hiatus posteriorly in those cases.
As far as observing patients with diaphragmatic hernias who are asymptomatic, we have been reluctant to do that, given that these patients can present with acute symptoms. That being said, there are patients who have developed a small recurrence after multiple attempts at repair, and we have followed those patients with serial CT scans.
DR JESSICA S. DONINGTON (New York, NY): The majority of cases in this series were done laparoscopically. The group at Pittsburgh has tremendous experience with that procedure. In my small experience I find the sizing of the hiatus difficult in the minimally invasive procedure. Open I can put my fingers in and get a good feel for the size of the hiatus. Your paper has demonstrated that too big a hiatus is bad and too little is equally as bad. What are your recommendations for how to appropriately size the hiatus in the minimally invasive procedure?
DR KENT: As you mentioned you must rely on visual rather than tactile cues during a minimally invasive esophagectomy.
We prefer to construct a thin gastric tube, about 5 cm in width. We like to see that we can easily pass a laparoscopic instrument between the crus and the conduit without difficulty at the end of the operation. The maneuver is similar to what is done during a Nissen fundoplication, where we pass an instrument between the wrap and the stomach, to ensure that the wrap is not too tight.
I would like to emphasize that only 9 patients from over 1,000 esophagectomies developed an obstruction at the hiatus, so it is a very rare complication. I think the mechanism in these 9 patients was that the conduit dilated over time with oral intake. Perhaps the pneumoperitoneum may also make it harder to assess the true size of the hiatus. So, in these small number of patients, our ability to calibrate the size of the hiatus to the conduit may have been diminished.
DR HIRAN C. FERNANDO (Boston, MA): Being an alumnus from Pittsburgh, I'm a big fan of minimally invasive esophagectomy. However, I also think that this is an issue that may be slightly higher in minimally invasive esophagectomies. Once you've done your neck anastomosis you then have to straighten out the conduit by pulling on the stomach inferiorly. It's a little difficult to know exactly if you're pulling too hard and getting too much tension on the neck anastomosis. And often when you review the X-rays postoperatively, you sometimes see the stomach looping over to the right side of the chest.
I believe that this might be something that may be minimized with the minimally invasive Ivor-Lewis approach because you can actually see how the conduit lies in the right chest.
In this series, do you know how many esophagectomies were performed with a neck anastomosis or with an Ivor-Lewis approach using an intrathoracic anastomosis?
DR KENT: Yes, there were. At Pittsburgh we have moved away from the neck anastomosis to an Ivor Lewis esophagectomy, primarily to avoid the morbidity of recurrent nerve injury. But one added benefit is that you can see the conduit in nearly its entire length from anastomosis to diaphragm. So the incidence of a twist, which is very rare, or redundancy, which is a little bit more common, should be decreased with that operation.
I think the drawback of the Ivor Lewis approach is that it is harder to put three tacking sutures between conduit and diaphragm. It can be done, but it is more difficult than when you are in the abdomen.
DR FERNANDO: And then just two other quick comments. If you can talk further about the "twist" patients; are you implying there was a twist between the upper and the lower anastomosis, since it would be difficult to manage this without taking one of the anastomoses down.
DR KENT: Yes.
DR FERNANDO: You also mentioned that it's important to place a posterior stitch. However, at the end of your laparoscopic procedure when you've opened everything up and you've opened the neck, at that point you're starting to lose a lot of pneumoperitoneum into the chest. So technically it's very difficult with everything collapsing on you to place that posterior stitch. So are you now placing a posterior stitch?
DR KENT: No. We have moved to the Ivor Lewis esophagectomy, so it is uncommon that we conclude the operation in the abdomen.
In terms of the twist, I think those patients are very rare, in fact we have only had three of them. These patients can be very difficult to treat. The one late death in this series was a patient with a twist who developed recurrent aspiration symptoms despite revisional surgery.
I think if we were to see such a patient again, we have discussed taking down the anastomosis, mobilizing the entire conduit, and redoing the anastomosis. Clearly that is a very difficult undertaking, but these patients can be very symptomatic.
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