Transthoracic esophagectomy as a two-cavity operation

Diaphragmatic Hernia After Conventional or Laparoscopic-Assisted Transthoracic Esophagectomy Daniel Vallböhmer, MD, Arnulf H. Hölscher, MD, PhD, Till Herbold, MD, Christian Gutschow, MD, and Wolfgang Schröder, MD Department of Visceral and Vascular Surgery, University of Cologne, Cologne, Germany GENERAL THORACIC Background. Diaphragmatic herniation is a rare but morbid complication after esophagectomy. This retrospective study estimates its incidence after transthoracic esophagectomy and describes the clinical spectrum of diaphragmatic herniation. Methods. Between February 1, 1997, and June 31, 2007, 355 consecutive patients with esophageal cancer underwent transthoracic esophagectomy. A diaphragmatic hernia was detected in 9 patients (2.5%) after transthoracic esophagectomy. All patients were men, with a median age of 50 years. A retrospective analysis of clinicopathologic characteristics of these patients was performed. Results. The median time between esophagectomy and diagnosis of herniation was 8 months. The 9 patients presented with different degrees of symptoms: 3 were asymptomatic, 2 had minor symptoms, and 4 had acute symptoms. All had a herniation of abdominal organs into the left hemi. One patient was asymptomatic, and no surgical repair was performed. Another patient refused the recommended reoperation. The other 7 patients underwent surgical repair of the diaphragmatic hernia by an abdominal approach. All had reduction of the herniated bowel into the abdominal cavity and closure of the hiatal defect. Resection of small bowel was performed in 1 patient for strangulation, and another patient underwent splenectomy for bleeding. Median hospital stay was 16 days. One patient died secondary to mediastinitis from an anastomotic leakage of the esophagogastrostomy. Conclusions. Diaphragmatic herniation after esophagectomy mostly occurs into the left chest. Surgeons should be aware of this rare complication in patients presenting with symptoms of intestinal obstruction or respiratory complaints after esophagectomy. (Ann Thorac Surg 2007;84:1847 53) 2007 by The Society of Thoracic Surgeons Transthoracic esophagectomy as a two-cavity operation with intrathoracic esophagogastrostomy is a standardized surgical approach for patients with esophageal cancer [1]. During the last decade, the incidence of perioperative and postoperative complications has decreased [2]. Herniation of intraabdominal organs into the chest is an uncommon but historically morbid postoperative complication after esophagectomy [3]. Diaphragmatic herniation is either an early postoperative event or it can occur after several months. When it is acute, emergency laparotomy is mandatory to prevent bowel obstruction or strangulation. In addition, the hiatus must be closed after reduction of the abdominal organs [4, 5]. The aim of this retrospective study was to estimate the incidence of diaphragmatic herniation after transthoracic esophagectomy and to analyze clinical symptoms and surgical results. Patients and Methods Accepted for publication July 5, 2007. Address correspondence to Dr Hölscher, Department of Visceral and Vascular Surgery, University of Cologne, Kerpenerstr. 62, Cologne, D-50937, Germany; e-mail: arnulf.hoelscher@uk-koeln.de. From February 1, 1997, to June 31, 2007, 355 consecutive patients (54 women, 301 men) with esophageal cancer underwent en bloc esophagectomy with two-field mediastinal and abdominal lymphadenectomy and intrathoracic esophagogastrostomy by members of the Department of Visceral and Vascular Surgery, University of Cologne. Until December 2003, 168 patients underwent conventional one-stage en bloc esophagectomy with an open mobilization of the stomach and intrathoracic anastomosis. Starting in December 2003, 187 patients underwent laparoscopic mobilization of the stomach, including the cardia and preparation of the gastric conduit. After a mean delay of 4 days (range, 3 to 7 days), a conventional right-sided transthoracic en bloc esophagectomy was performed under a second anesthesia. Reconstruction was done by gastric pull-up and high intrathoracic esophagogastrostomy. The hiatus was not routinely adjusted to the gastric conduit during the abdominal or thoracic parts of the operation. If the hiatus was merely too wide, sutures to narrow the diaphragmatic crura were placed. In the case of a narrow hiatus, we partially divided the right crura to allow an easy passage later on of the gastric tube through the hiatus and prevent gastric outlet obstruction. The median patient age was 62 years (range, 19 to 81 years). Patients with advanced esophageal cancer (ct3/4, Nx, M0) received neoadjuvant radiotherapy (36 Gy, cisplatin, 5-FU) [6]. After discharge, patients were followed up at regularly scheduled intervals and routinely had 2007 by The Society of Thoracic Surgeons 0003-4975/07/$32.00 Published by Elsevier Inc doi:10.1016/j.athoracsur.2007.07.009

GENERAL THORACIC 1848 VALLBÖHMER ET AL Ann Thorac Surg DIAPHRAGMATIC HERNIA AFTER ESOPHAGECTOMY 2007;84:1847 53 Fig 1. Chest roentgenogram of patient 4 shows bowel loops and airfluid levels in the lower half of the left hemi. The mediastinum is shifted to the right side. esophagogastroscopy, chest roentgenogram, ultrasound imaging of the liver, and computed tomography of the and abdomen. A diaphragmatic hernia was detected after transthoracic esophagectomy in 9 patients (2.5%): in 4 of the 168 patients (2.4%) undergoing the conventional one-stage en bloc esophagectomy and in 5 patients (2.7%) of the 187 who had undergone laparoscopic mobilization of the stomach conduit at a separate procedure from the intrathoracic operation (Figs 1 and 2). A retrospective analysis of these patients clinicopathologic characteristics forms the basis of this study. The local Institutional Review Board (IRB) approved this retrospective study and indicated that individual consent could be waived because individual patients were not identified. Surgical Repair Seven patients had a reoperation: five were emergencies and two were elective. The seven operative procedures were performed by a transabdominal approach, and in all 7 patients, a herniation of the small bowel and colon occurred into the left chest. In addition, the spleen had also herniated into the left chest in one patient. The operative procedures consisted of reduction of the herniated bowel into the abdominal cavity, followed by posterior repair of the hiatal defect with primary closure in 6 patients and with an absorbable mesh in 1 patient. Two patients required additional procedures at the time of the reoperation for the diaphragmatic hernia. Resection of an ischemic jejunal segment was performed in 1 patient for bowel strangulation. This patient also required a resection of the transverse colon with protective loop ileostomy because segmental ischemia of this area developed 2 days after repair of the diaphragmatic hernia. In another patient, a splenectomy was performed due to bleeding. Two patients did not have operative repair of the diaphragmatic hernia. One patient was observed because he was completely asymptomatic. Another patient declined elective repair because he felt his symptoms were not bothersome (mild chest pressure). Clinical Outcome The median hospital stay of the 5 patients who were discharged home was 16 days (range, 8 to 28 days). These patients had no postoperative complications. In another patient, postoperative upper endoscopy was complicated by an aspiration event that required mechanical ventilation. He recovered without incident, was extubated, and was transferred after 18 days to the Department of Radiation Therapy to initiate therapy to his lumbar metastases. The other patient died after a prolonged and complicated postoperative course. This patient actually under- Results Patient Characteristics All 9 patients with diaphragmatic hernia were men, and their median age of 50 years (range, 35 to 69 years). On final pathology, 8 patients had adenocarcinoma and 1 patient had squamous cell carcinoma. All tumors were located in the distal esophagus, and in 2 patients there was involvement of the cardia. Seven patients had undergone neoadjuvant radiochemotherapy (Table 1) [6]. Symptoms Three patients were asymptomatic, and 6 patients had clinical symptoms. Three patients complained about acute diffuse abdominal, and 3 patients had chest, of which 1 had acute onset chest, 1 had minor chest pressure, and another had intermittent episodes of chest. The median time between esophagectomy and the diagnosis of herniation was 8 months (range, 0.3 to 30 months). Fig 2. Thoracic computed tomography scan of patient 4 shows the gastric conduit is present behind the trachea. In the posterior lateral left hemi, multiple bowel loops are evident within the hiatal hernia. The left lung is compressed within the left anterior hemi.

Table 1. Patients With Diaphragmatic Herniation After Transthoracic Esophagectomy Patient Age (y) Histology (pt N M) Esophagectomy Symptoms 1 68 AC distal esophagus (pt1 N0 M0 R0) 2 64 SCC distal esophagus, (ypt3 N1 M0 R0) 3 49 ACC distal esophagus, (ypt2 N0 M0 R0) 4 59 AC distal esophagus and cardia, (ypt2 N1 M0 R0) 5 69 AC distal esophagus, (ypt0n0m0) 6 50 AC distal esophagus and cardia (ypt3n0m0r0) 7 45 AC distal esophagus (ypt3 N1 M0 GR0) 8 35 AC distal esophagus (ypt3 N1 M1(bone) R0) 9 50 AC distal esophagus (pt1n0 M0 R0) Interval Between TTE and Repair (m) Surgical Treatment Herniation Into the Left Thorax TTE None 0.3 Hiatoplasty Jejunum and transverse colon TTE atypic liver resection TTE TTE LG TTE LG TTE None 2 Splenectomy, hiatoplasty (previous resection of gastric conduit) Acute abdominal Acute abdominal Acute abdominal Minor thoracic pressure sensation Jejunum, left flexure of the colon and spleen 5 Hiatoplasty with net Jejunum and transverse colon 30 Partial jejunal resection and hiatoplasty; transverse colon resection and loop ileostomy during relaparotomy Jejunum and transverse colon 14 Hiatoplasty Jejunum and transverse colon 10 No operation Jejunum and colon LG TTE Thoracic 0.5 Hiatoplasty Jejunum and transverse colon LG TTE Acute thoracic 4 Hiatoplasty Jejunum and colon LG TTE None 8 No operation Jejunum and transverse colon AC adenocarcinoma; LG TTE laparoscopic gastrolysis and delayed transthoracic esophagectomy; SCC squamous cell cancer; TTE transthoracic esophagectomy. Ann Thorac Surg VALLBÖHMER ET AL 2007;84:1847 53 DIAPHRAGMATIC HERNIA AFTER ESOPHAGECTOMY 1849 GENERAL THORACIC

GENERAL THORACIC 1850 VALLBÖHMER ET AL Ann Thorac Surg DIAPHRAGMATIC HERNIA AFTER ESOPHAGECTOMY 2007;84:1847 53 Table 2. Publications About 44 Patients With Diaphragmatic Hernia After Esophagectomy Through 2006 First Author/Year No. of Patients Diagnosis Type of Operation Herniation of Interval Between Esophagectomy and Repair Surgical Procedure Terz, etc 1987 [7] 1 Cancer THE transverse colon, small 7 d Laparotomy bowel Barbier, etc 1988 [8] 3 Cancer THE?? No surgical repair Streitz, etc 1990 [9] 1? E? 3 m Thoracotomy Reich, etc 1996 [10] 1 Cancer THE omentum, colon, jejunum into the right Balasz, etc 1997 [11] 1 Cancer THE transverse colon into the left Heitmiller, etc 1997 [12] 2 Barrett dysplasia 1 THE, 1 TTE transverse colon, omentum into the left (n 1) and right (n 1) Van Sandick, etc 1999 [5] 9 Cancer 5 THE, 4 TTE transverse colon, small bowel, spleen Cordero, etc 2000 [13] 1 Cancer THE transverse colon into the left Delgado Tapia, etc 2000 [14] 1 Cancer THE transverse colon into the left 10 m Laparotomy and thoracotomy 6 d Laparotomy 6 and 3 d 1 laparotomy 2 d 44 m 5 laparotomy, 1 thoracotomy 3 no surgical repair 6 d laparotomy and thoracotomy?? Choi, etc 2001 [15] 1 Cancer THE colon into the left 6 m Laparotomy Franceschi, etc 2002 [16] 2 Cancer TTE colon, small bowel, 23 and 30 m Laparotomy mesocolon into the left Granke, etc 2002 [17] 1 Cancer THE omentum into the right 7 d Laparotomy Hamaloglu, etc 2002 [18] 1 Cancer THE colon, jejunum into the left 28 d Laparotomy Aly, etc 2004 [19] 1 Cancer E colon, small bowel, 26 m Laparotomy omentum into the left Audebert, etc 2005 [20] 7 Cancer 4 THE, 3 TTE colon, small bowel into the 2 7 y Laparotomy left Kaushik, etc 2005 [21] 1 Cancer THE colon into the left 28 d Laparotomy Fumagalli, etc 2006 [4] 2 Cancer TTE colon, small bowel, omentum into the left (n 1) and right (n 1) Current series 9 Cancer LG TTE small bowel, colon, spleen into the left 4 and 8 m Laparotomy and thoracotomy 0.3 30 m 7 laparotomy, 2 no surgical repair E esophagectomy; LG laparoscopic gastrolysis; THE transhiatal esophagectomy; TTE transthoracic esophagectomy. went two reoperations after esophagectomy (revision of the anastomosis for leak, then takedown of the gastric pull-up for necrosis) before the diaphragmatic hernia developed. Another reoperation was performed to place a jejunal feeding tube, at which time an incidental large diaphragmatic hernia was detected with herniation of small bowel and left flexure of the colon and spleen into the left chest. This patient required splenectomy. The patient eventually died 8 weeks after the esophagectomy secondary to severe mediastinitis caused by the initial anastomotic leakage of the esophagogastrostomy. Comment Diaphragmatic herniation is an uncommon postoperative complication after esophagectomy, with a reported incidence of 0.4% to 6% [5]. To date, 36 cases with this complication after esophagectomy have been reported in the literature, mainly with herniation of intraabdominal organs into the left hemi, as shown in our series (Tables 1 and 2) [4, 5, 7 21]. Hiatal hernia can occur in the early postoperative period or as a late complication [8, 15]. When it occurs early, its cause can most likely be attributed to the lack of peritoneal adhesions. With longer follow-up, other mechanisms such as progressive hiatal dilatation, increased intraabdominal pressure, and the pull of negative intrathoracic pressure may contribute to its development. Another reason might be the more frequent use of minimally invasive procedures in esophageal surgery, leading to less peritoneal adhesions, especially in the hiatal region [22, 23]. In fact, 5 of our 9 patients with

Ann Thorac Surg VALLBÖHMER ET AL 2007;84:1847 53 DIAPHRAGMATIC HERNIA AFTER ESOPHAGECTOMY diaphragmatic herniation after esophagectomy underwent laparoscopic mobilization of the stomach (gastrolysis), a procedure that reduces the physiologic stress of the two-cavity operation for the patient while allowing the construction of a comparable gastric conduit as is done with open surgery [23]. An interesting finding was that in all of our study patients, diaphragmatic herniation occurred into the left chest, which is consistent with the cases described so far (Table 2). At this point, we can only speculate about the underlying mechanisms for why herniation into the left chest occurs more often. Possibly, as an open space occurs in the left upper abdomen after gastric pull-up, small or large bowel can fall into this space and herniate into the left chest. Another possible explanation for the more frequent herniation into the left chest is simply that in the left-sided hiatal region, the plain serosal surface is located at the greater curvature of the gastric conduit, leading to less peritoneal adhesions than at the lesser curvature. The lesser curvature with fewer serosal surfaces and the gastric dissection plane probably induces more peritoneal adhesions. In addition, the right-sided hiatal region is covered by the lateral segment of the left lobe of the liver, which possibly prevents a herniation into the right chest. The presence of symptoms in patients with herniation of intraabdominal organs into the chest is variable and to some extent depends on the specific organ that has herniated. Symptoms can therefore include respiratory distress, abdominal, intestinal obstruction, and gastrointestinal bleeding [8, 9, 15]. The main complaint in our patients was abdominal or thoracic. When diaphragmatic herniation persists or increases, reoperation is usually recommended to prevent potential complications such as strangulation or perforation [8, 13]. Most published reports indicate a transabdominal approach is preferred, as was our preference. Others have advocated thoracotomy in cases of extensive abdominal adhesions [8, 10, 13, 19]. Finally, some have managed patients with diaphragmatic hernias expectantly with a wait and see approach [8, 12]. We believe surgical repair should only be waived in cases of small or asymptomatic hernias or if the patient has a short life expectancy due to progressive cancer. Ideally, the best approach would be to prevent diaphragmatic herniation in the first place after esophagectomy [8, 13]. One of the critical steps in performing an esophagectomy is the enlargement of the hiatus to allow sufficient mobilization of the esophagus and to ease the transdiaphragmatic passage of the gastric conduit, which of course increases the risk of diaphragmatic herniation. If an intraoperative enlargement of the hiatus is necessary, Reich and colleagues [10] have suggested performing an anterior incision of the hiatus rather than a lateral incision of the diaphragma to lower risk of herniation. The size of the hiatus should also be adjusted to the gastric conduit or the colon interposition during both the abdominal as well as thoracic parts of the operation [22]. In particular, after gastric pull-up with intrathoracic anastomosis, the hiatus should be inspected, and if it is too wide, sutures to narrow the diaphragmatic crura should be placed [3]. Finally, others recommend placing sutures between the graft and the crura to prevent hiatal herniation [22]. We do not routinely suture the graft along the crura. In our opinion, this may indeed prevent herniation but it may disturb vascularization of the conduit. Thus, suturing the graft along the crura is much easier during the abdominal portion of the Ivor Lewis technique, which is not possible after abdominal closure. In contrast, tacking sutures between the graft and the crura during the thoracic approach is more difficult because one needs to avoid disturbing the vessels of the lesser and greater curvature of the conduit. In conclusion, diaphragmatic hernia after esophagectomy is a rare but sometimes a severe complication. The herniation mostly develops into the left chest and contains small and sometimes large bowel. Surgical repair is recommended to reduce the herniated organs into the abdominal cavity, followed by the closure of the hiatal defect. Surgeons should be aware of this possible complication in patients presenting with symptoms of intestinal obstruction or respiratory complaints after esophagectomy. References 1851 1. Hölscher AH, Schroder W, Bollschweiler E, Beckurts KT, Schneider PM. How safe is high intrathoracic esophagogastrostomy? Chirurg 2003;74:726 33. 2. Dimick JB, Wainess RM, Upchurch GR Jr, Iannettoni MD, Orringer MB. National trends in outcomes for esophageal resection. Ann Thorac Surg 2005;79:212 6. 3. Hölscher AH, Vallböhmer D, Brabender J. The prevention and management of perioperative complications. Best Pract Res Clin Gastroenterol 2006;20:907 23. 4. Fumagalli U, Rosati R, Caputo M, Bona S, Zago M, Lutmann F, Peracchia A. Diaphragmatic acute massive herniation after laparoscopic gastroplasty for esophagectomy. Dis Esophagus 2006;19:40 3. 5. Van Sandick JW, Knegjens JL, van Lanschot JJ, Obertop H. Diaphragmatic herniation following oesophagectomy. Br J Surg 1999;86:109 12. 6. Schneider PM, Baldus SE, Metzger R, et al. Histomorphologic tumor regression and lymph node metastases determine prognosis following neoadjuvant radiochemotherapy for esophageal cancer: implications for response classification. Ann Surg 2005;242:684 92. 7. Terz JJ, Beatty JD, Kokal WA, Wagman LD. Transhiatal esophagectomy. Am J Surg 1987;154:42 8. 8. Barbier PA, Luder PJ, Schupfer G, Becker CD, Wagner HE. Quality of life and patterns of recurrence following transhiatal esophagectomy for cancer: results of a prospective follow-up in 50 patients. World J Surg 1988;12:270 6. 9. Streitz JM Jr, Ellis FH Jr. Iatrogenic paraesophageal hiatus hernia. Ann Thorac Surg 1990;50:446 9. 10. Reich H, Lo AY, Harvey JC. Diaphragmatic hernia following transhiatal esophagectomy. Scand J Thorac Cardiovasc Surg 1996;30:101 3. 11. Balazs A, Forgacs A, Flautner L, Kupcsulik P. A case of unusual complication of diaphragmatic herniation transverse colon following transhiatal esophagectomy. Orv Hetil 1997;138:2535 8. 12. Heitmiller RF, Gillinov AM, Jones B. Transhiatal herniation of colon after esophagectomy and gastric pull-up. Ann Thorac Surg 1997;63:554 6. 13. Cordero JA Jr, Moores DW. Thoracic herniation of the transverse colon after transhiatal esophagectomy. J Thorac Cardiovasc Surg 2000;120:416. GENERAL THORACIC

GENERAL THORACIC 1852 VALLBÖHMER ET AL Ann Thorac Surg DIAPHRAGMATIC HERNIA AFTER ESOPHAGECTOMY 2007;84:1847 53 14. Delgado Tapia J, Ramirez Sanchez A, Molina Moreno M, Palop Manjon-Cabeza E, Ferron Orihuela JA. Diaphragmatic hernia after transhiatal esophagectomy. Rev Esp Anestesiol Reanim 2000;47:317 9. 15. Choi YU, North JH Jr. Diaphragmatic hernia after Ivor-Lewis esophagectomy manifested as lower gastrointestinal bleeding. Am Surg 2001;67:30 2. 16. Franceschi A, Mariette C, Balon JM, Fabre S, Triboulet JP. Diaphragmatic hernia after esophagectomy: 2 case reports and review of the literature. Ann Chir 2002;127:62 4. 17. Granke K, Hoshal VL Jr, Vanden Belt RJ. Extrapericardial tamponade with herniated omentum after transhiatal esophagectomy. J Surg Oncol 1990;44:273 5. 18. Hamaloglu E, Topaloglu S, Torer N. Diaphragmatic herniation after transhiatal esophagectomy. Dis Esophagus 2002;15:186 8. 19. Aly A, Watson DI. Diaphragmatic hernia after minimally invasive esophagectomy. Dis Esophagus 2004;17:183 6. 20. Audebert A, Wind P, Sauvanet A, Douard R, Benichou J, Cugnenc PH, Belghiti J. Diaphragmatic hernia is a rare complication of oesophagectomy for cancer. Ann Chir 2005; 130:21 25. 21. Kaushik R, Sharma R, Attri AK. Herniation of colon following transhiatal esophagectomy. Indian J Gastroenterol 2005; 24:122 3. 22. Luketich JD, Alvelo-Rivera M, Buenaventura PO, et al. Minimally invasive esophagectomy: outcomes in 222 patients. Ann Surg 2003;238:486 94. 23. Hölscher AH, Schneider PM, Gutschow C, Schröder W. Laparoscopic ischemic conditioning of the stomach for esophageal replacement. Ann Surg 2007;245:241 6. INVITED COMMENTARY Vallböhmer and colleagues [1] report 9 patients in whom intraabdominal organs herniated into the mediastinum or thoracic cavity after esophagectomy with gastric pullup. No fixation of the stomach to the crura was performed, and in selected patients, the hiatus was narrowed with sutures when it was thought to be too wide. Symptoms were present in 6 of the 9 patients, and the hernia was found at a median time of 8 months after esophagectomy. Reoperation was performed in 7 patients (5 emergency and 2 elective) and consisted of reduction of the herniated bowel/organ into the abdomen and posterior repair of the hiatal defect (6 primary repairs and 1 with absorbable mesh). A concomitant bowel resection was necessary in 1 patient, and another required splenectomy. The authors recommend operative repair in all but the smallest asymptomatic hernias or if the patient has a short life expectancy. They also advise adjusting the size of the hiatus to approximate the graft to reduce the potential for this complication to occur. Migration of abdominal organs through the enlarged hiatus after esophagectomy is a real entity, as pointed out in this article by Vallböhmer and colleagues. At our center, we routinely suture the graft, whether colon or stomach, to the left crus of the diaphragm to prevent herniation and redundancy of the graft (for colon grafts, primarily) or twisting of the graft in the mediastinum (for gastric pull-ups, primarily). It is also important to suture an enlarged hiatus closed to the point that it approximates the graft but not to the point that it compromises graft emptying. Graft herniation can occur early in the postoperative period but is not always appreciated immediately. I have seen it more commonly after a colon interposition and now close the crura posterior to the graft with several Fig 1. (A) Postoperative day 1 chest roentgenogram after esophagectomy with left colon interposition (mostly transverse colon based on left colic blood supply). (B) Postoperative day 2 chest roentgenogram in the same patient. Note the new air collection to the left of the hiatus representing herniated cecum and splenic flexure of the colon including the fresh colon-to-colon anastomosis. The colon herniated behind the colon graft, which was anastomosed to the antrum and had been sutured along the lateral edge of the left crus. The posterior crura had not been closed or sutured to the colon interposition, leaving the space through which the hernia occurred. 2007 by The Society of Thoracic Surgeons 0003-4975/07/$32.00 Published by Elsevier Inc doi:10.1016/j.athoracsur.2007.08.006