JOURNAL OF LAPAROENDOSCOPIC & ADVANCED SURGICAL TECHNIQUES Volume 24, Number 5, 2014 ª Mary Ann Liebert, Inc. DOI: 10.1089/lap.2013.0416
Delayed Gastric Emptying After Esophagectomy for Malignancy Bin Li, MD, Jian-Hua Zhang, MD, Cheng Wang, MD, Tie-Niu Song, MM, Zhi-Qiang Wang, MM, Yun-Jiu Gou, PhD, Jian-Bao Yang, MM, and Xiao-Ping Wei, MM
Abstract
Background: Controversy still exists about the need for pyloric drainage procedures after esophagectomy with gastric conduit reconstruction. Although pyloric drainage may prevent postoperative delayed gastric emptying (DGE), it may also promote dumping syndrome and bile reflux. The aims of this study were to audit the incidence and management of DGE in patients without routine pyloric drainage after esophagectomy in a university medical center. Patients and Methods: From July 2006 to June 2012, data from 356 consecutive patients who underwent esophagectomy with a gastric conduit without pyloric drainage for esophageal or gastric cardia carcinoma were reviewed. Major observation parameters were the incidence, management, and outcomes of DGE. Results: Overall incidence of DGE was 15.7% (56 of 356). Early DGE developed in 26 patients, and late DGE developed in 30 patients. There were no differences in demographic and intraoperative data between the two groups with or without DGE. More DGE was documented in patients with an intra-right thoracic gastric conduit (P = .031). A higher incidence of postoperative pneumonia was observed in patients exhibiting early DGE, but without significance (P = .254). There were also no significant impacts on respiratory failure (P = .848) and anastomotic leakage (P = .257). There was an increased postoperative hospital stay with DGE, but without significance (P = .089). Endoscopic balloon dilatation of the pylorus was used to manage 33.9% of patients with DGE, yielding a 78.9% (15 of 19) success rate without complications. In 3 patients endoscopy showed the pylorus was open, and their symptoms improved over time. One patient with tumor-related DGE was treated by pyloric stent. The remaining patients were adequately treated with conservative management. Conclusions: Omitting the operative drainage procedure does not lead to an increased frequency of DGE after esophagectomy with a gastric conduit. Many patients responded to conservative management, and endoscopic balloon pyloric dilatation can be effective in managing the DGE postoperatively.
Introduction
E
sophageal carcinoma is the eighth most common cancer in the world, with an estimated 482,300 new diagnosis and 406,800 cancer deaths annually.1 Surgical resection remains the mainstay of treatment, whether performed for curative intent or for palliation of dysphagia.2 After esophagectomy, the stomach is predominantly used to restore continuity of the upper gastrointestinal (UGI) tract. However, complications related to the gastric conduit, such as delayed gastric emptying (DGE), are not uncommon, which may cause debilitating symptoms, delayed recovery, and poor quality of life.3,4
In an effort to promote gastric emptying, many surgeons perform pyloric drainage procedures, such as pyloroplasty or pyloromyotomy. But, no consensus has yet been reached on the need for pyloric drainage procedures after esophagectomy with gastric conduit reconstruction. Arguments for routine pyloric drainage include prevention of postoperative DGE to reduce the incidence of aspiration pneumonia and to improve early postoperative outcomes.5,6 Opponents argue that pyloric drainage may predispose to dumping syndrome and duodenal bile reflux esophagitis, impairing late postoperative functional outcomes without consistent benefits.7–9 In addition, several studies have documented an improvement in gastric emptying over time.10–12 Consequently, the benefits
Department of Thoracic Surgery, Lanzhou University Second Hospital, Lanzhou University Second Clinical Medical College, Lanzhou, People’s Republic of China.
306
DGE AFTER ESOPHAGECTOMY FOR MALIGNANCY
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of routine pyloric drainage procedures are most likely to be realized in the immediate postoperative period by preventing aspiration pneumonia and gastric stasis.13 Indeed, DGE can be successfully managed postoperatively, and most patients respond adequately to medical therapy and endoscopic balloon pyloric dilatation.14–18 For these reasons, no pyloric drainage procedure was performed routinely after esophagectomy with gastric conduit reconstruction at our hospital. The aims of the current study were to audit the incidence and management of postoperative DGE in patients who underwent esophagectomy without pyloric drainage procedure in a single university medical center.
Furthermore, a nasogastric tube was placed in the intrathoracic stomach for gastrointestinal decompression, and a feeding tube was placed in the duodenum for postoperative nutritional support routinely. No pyloric drainage procedure was undertaken in this study. Nasogastric drainage was maintained on average 5–7 days or until barium swallow examination was performed on postoperative day (POD) 5–7 to confirm the absence of anastomotic leakage or DGE. The enteral feeding usually began on POD 2. Liquid oral diet was usually begun on POD 6–8, in the absence of signs of leakage. If a leakage was present, nutrition was maintained by a combined parenteral and feeding tube, and oral diet was resumed following closure of the leakage.
Patients and Methods
Assessments and management of postoperative DGE
Patients
Routine barium swallow examination was performed on POD 5–7 to assess for evidence of the leakage and DGE. Anastomotic leakage was defined as the extravasation of water-soluble contrast medium or the visualization of oral ingested methylene blue in the cervical or thoracic drainage. Clinical symptoms (e.g., nausea, emesis, bloating, regurgitation, chest pressure, and early satiety), barium swallow examination, gastric conduit dilatation or persistent air fluid level on radiography, and retention of food on UGI endoscopy supported the diagnosis of DGE. Operative mortality was defined as any death during the first 30 days after operation or during the same hospitalization as the operation. After discharge, patients were routinely examined every 3 months during the first year, every 6 months during the following 2 years, and annually thereafter at our hospital. In the case of DGE, barium swallow examination was conducted immediately. UGI endoscopy was immediately recommended in patients with symptoms of DGE and routinely recommended to be performed annually at follow-up with or without symptoms. DGE was managed with conservative management, including continuous gastrointestinal decompression by a nasogastric tube, traditional Chinese medicine–based therapies (acupuncture and physiotherapy), use of prokinetic medications (domperidone or cisapride), and observation, or by definitive management (endoscopic balloon pyloric dilatation). Pyloric dilatations were performed with controlled radial expansion balloon dilators over a guidewire visualized under fluoroscopic guidance to a maximal diameter of 20 mm. Endoscopic dilatation was performed using a 10-mm flexible UGI endoscope (Olympus, Tokyo, Japan), where the balloon dilator was inflated for at least 2 minutes, achieving a predetermined diameter at each session. Pyloric dilatation was performed until pyloric patency was achieved when the 10-mm endoscope could easily traverse the pyloric channel without resistance. Patients who required balloon pyloric dilatation were followed up, and dilatation sessions were applied if necessary until resolution of DGE symptoms.
Between July 2006 and June 2012, in total, 369 consecutive patients diagnosed with esophageal or gastric cardia carcinoma underwent procedures at our hospital. Patients who had undergone previous gastric surgery (n = 3) or esophagectomy with colonic transposition (n = 2) or were not treated because of metastatic disease (n = 8) were excluded. The remaining 356 patients formed the cohort for this study. They were operated on by surgical teams with similar experience in esophageal surgery. Preoperative diagnostic assessment, consisting of ultrasonography of the neck, abdominothoracic computed tomography scan, UGI endoscopy with biopsy, barium swallow examination, and Tc-99m whole-body bone scan, was performed for all patients. Electrocardiography, the pulmonary function test, and hematological and biochemistry tests were performed routinely. All recruited patients did not receive either neoadjuvant chemotherapy or radiotherapy. The study protocol was approved by the Ethics Committee of our hospital. Surgical approach
Patients who underwent esophagectomy during the study period were included regardless of surgical approach. The standardized surgical approaches19 included conventional open esophagectomy (i.e., left thoracotomy, Ivor Lewis, and McKeown approaches) and minimally invasive esophagectomy (i.e., thoracoscopic laparoscopic and thoracoscopic laparotomic approaches), with either cervical or intrathoracic anastomosis. In brief, general anesthesia was administered by a double-lumen tube. The intrathoracic esophagus was mobilized en bloc within an envelope of the adjoining tissues. The stomach was isolated, the left gastric vessels were transected at their base, and the right gastroepiploic vessels were preserved. The esophagus was transected at least 5 cm proximal to the upper edge of the tumor, and thoracoabdominal standard two-field lymph node dissection was performed. Reconstruction of the gastrointestinal tract with a whole stomach or gastric tube was adopted on the surgeon’s preference. In the latter, a 6-cm-wide gastric conduit was created with a linear cutter stapler ( Johnson & Johnson, New Brunswick, NJ) along the greater curvature, and the staple line was inverted with interrupted 3-0 silk sutures. Then, the gastric conduit was delivered through the posterior mediastinum, and esophagogastric anastomosis was performed with a hand-sewn or circular stapler.
Statistical analysis
Demographic and perioperative data were retrieved from the prospectively entered database. Follow-up outpatient evaluations were obtained by medical records, telephone interviews, or mail correspondence. Related data were analyzed with SPSS statistical package software (version 16.0; SPSS Inc., Chicago, IL). The chi-squared test or Fisher’s
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LI ET AL.
exact test was used for categorical data. Student’s t test or the Mann–Whitney U test was used for continuous data. Two-tailed P < .05 was considered to indicate statistical significance. Results Perioperative clinicopathologic characteristics
In total, 356 patients were included. The average follow-up duration was 32.3 – 17.8 (range, 3–66; median, 29) months. Patients were divided into two groups based on the absence or presence of DGE. The demographic and perioperative characteristics were compared and summarized in Table 1. Age, gender, comorbidity, tumor location, and histological type were not significantly different between the two groups. Esophagogastric anastomosis was fashioned at the cervical level in 55 patients (40 by McKeown approach, 15 by min-
Table 1. Demographic and Clinicopathologic Data for Patients With or Without Delayed Gastric Emptying
Age (mean – SD) (years) Gender Male Female Comorbidity Yes No Tumor location Upper thoracic Middle thoracic Lower thoracic Gastric cardia Histological type Squamous cell carcinoma Adenocarcinoma Surgical approach Left thoracotomy Ivor Lewis McKeown Minimally invasive Stomach transposition Whole stomach Gastric tube Gastric conduit location Intra-left thoracic Intra-right thoracic Anastomotic position Cervical level Above the aortic arch or azygos vein Under the aortic arch or azygos vein Anastomotic technique Hand-sewn Circular stapler
No DGE (n = 300)
DGE (n = 56)
56.3 – 9.6
58.6 – 8.7
245 55
46 10
113 187
23 33
30 163 71 36
7 35 9 5
262
50
38
6
165 92 31 12
22 22 9 3
205 95
39 17
165 135
22 34
43 191
12 34
66
10
123 177
25 31
P value .107 .933 .630 .485
.684
.179
.846
imally invasive approach) and intrathoracic in 301 patients (187 by left thoracotomy, 114 by Ivor Lewis approach). All cervical anastomoses were single layer hand-sewn. Intrathoracic anastomosis was by hand-sewn or circular stapler according to the surgeon’s preference. There were no significant differences in surgical approach (P = .179), stomach transposition (P = .846), anastomotic position (P = .371), and anastomotic technique (P = .612) between the two groups. In addition, more DGE was documented in patients with an intra-right thoracic gastric conduit (34 versus 22; P = .031). There was no significant difference in the frequency of the gastric tube location between the intra-left thoracic (51 of 187) and intra-right thoracic (61 of 169) (P = .073). Incidence, management, and outcomes of postoperative DGE
The overall incidence of DGE was 15.7% (56 of 356) in our series, including those patients with clinical symptoms, delayed emptying on barium swallow, dilated conduit with persistent air fluid level, or retained food on UGI endoscopy. The management of DGE varied with the severity of symptoms, degree of radiographic obstruction, and time of presentation and is detailed in Table 2. Early DGE (within 30 days from esophagectomy) developed in 26 of 56 patients (46.4%); 20 were managed conservatively as previously mentioned, resulting in control of their symptoms, and 6 were definitively managed with endoscopic balloon dilatation of the pylorus. Repeat dilatation was necessary in 1 patient for symptomatic relief, and 1 patient who exhibited acute intrathoracic stomach dilation in the early postoperative period (POD 9) required emergency endoscopic balloon pyloric dilatation. Five patients had immediate and complete resolution of their symptoms, but in 1 patient showing an open pylorus, his symptoms improved with time. As presented in Table 3, a trend of higher incidence of postoperative pneumonia was observed in patients exhibiting early DGE versus normal emptying, but without statistical significance (23.1% versus 14.7%; P = .254). There was also had no significant impact on incidences of anastomotic leakage (P = .257) and respiratory failure (P = .848). There was a tendency to increased length of postoperative hospital stay in patients with early DGE; this was due to an a stay of approximately 2 days longer compared with patients
Table 2. Management of 56 Patients with Delayed Gastric Emptying DGE (n = 56)
.031 Management .371
.612
DGE, delayed gastric emptying; SD, standard deviation.
Early (n = 26)
Late (n = 30)
Conservative 20 (76.9%) 17 (56.7%) Pyloric balloon dilatation 6 (23.1%) 13 (43.3%) Number of dilatations 1.3 – 0.5 (1–2) 1.6 – 1.1 (1–4) (range) Interval between surgery 16.5 – 2.9 days 11.3 – 6.7 months and dilatation Successful treatment 5 (83.3%) 10 (76.9%) Data are number (%) or mean – standard deviation values as indicated. DGE, delayed gastric emptying.
DGE AFTER ESOPHAGECTOMY FOR MALIGNANCY
Table 3. Postoperative Outcomes in Patients With or Without Early Delayed Gastric Emptying No DGE (n = 300) Pneumonia 44 Respiratory failure 14 Anastomotic leakage 10 Postoperative hospital 11.8 – 4.6 stay (days) Operative mortality 6
Early DGE (n = 26) P value 6 1 2 13.9 – 5.9
.254 .848 .257 .089
1
.533
Data are number of patients or mean – standard deviation values as indicated. DGE, delayed gastric emptying.
without DGE, but this was not statistically significant (P = .089). There was no intraoperative death in our series. The operative mortality was 2.0% in the entire cohort and 3.8% and 2.0% in the early DGE and no DGE groups, respectively, without significant difference (P = .533). Among these patients, 3 died of respiratory failure, 2 of anastomotic leakage, 1 of myocardial infarction, and 1 of pulmonary embolism. Late DGE (more than 30 days from esophagectomy) developed in 30 of 56 patients (53.6%), and the mean interval after original surgery was 11.3 – 6.7 (range, 2–23; median, 5) months. Seventeen patients were managed conservatively, and 13 were treated by endoscopic balloon pyloric dilatation. Pyloric dilatation was effective in 10 patients, but in 2 patients endoscopy showed the pylorus was open, and their symptoms improved over time; in another patient, locoregional recurrence tumor-related DGE was treated by a pyloric stent. Consequently, endoscopic balloon dilatation of the pylorus was used in 33.9% (19 of 56) of patients exhibiting DGE; 78.9% (15 of 19) were successfully managed without complications. The remaining 66.1% (37 of 56) of patients were adequately treated with conservative management. No patient needed reoperation to manage DGE. Discussion
The incidence of DGE after esophagectomy for esophageal malignancy with a gastric conduit has been reported to range from 15% to 50%.17,18,20,21 In our series, DGE occurred in 15.7% (56 of 356) of patients, which is comparable to these previous reports, suggesting that omitting the operative drainage procedure does not lead to an increased frequency of DGE after esophagectomy with a gastric conduit. For multifactorial reasons, the function of this gastric conduit is significantly altered compared with the native stomach.12,22–25 During esophagectomy, the bilateral disconnection of the vagus nerve was inevitable, which led to dysmotility of the gastric conduit and delayed emptying because of coordination of the pyloric opening. In dividing the left gastric artery at its base, collateral damage to celiac axis nerves caused the gastric sympathectomy that further influenced motor function. The natural antireflux mechanisms of the esophagus were inevitably damaged during surgery. The use of narcotic drugs may also have compromised the gastrointestinal function. After the operation, the stomach was moved into the thoracic cavity, its anatomical structure and physiological function were changed, and the negative pressure in the thoracic cavity and positive pressure inside the
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stomach formed differential pressure. In addition, changes in the gastrointestinal peptide hormones after the operation acted together to worsen the situation. The pyloric drainage procedures—pyloroplasty or pyloromyotomy—were used typically to prevent DGE after esophagectomy, but this remains an ongoing debate. Some investigators found drainage procedures improved gastric emptying and decreased the risk of postoperative aspiration pneumonia, and therefore morbidity and mortality.5,6 However, others have not consistently documented the benefits of these procedures.7,8 Urschel et al.13 reevaluated the need for pyloric drainage in an examination of nine randomized controlled trials. This meta-analysis, which included 553 patients, demonstrated short-term improvement in gastric emptying using the pyloric drainage procedure at the time of esophagectomy, but this had little effect on postoperative pulmonary morbidity, mortality, length of hospital stay, and long-term foregut function. Furthermore, these procedures may be technically challenging during minimally invasive esophagectomy, and they are associated with a small but definable morbidity, such as duodenal leak, pyloric stricture, bile reflux, dumping syndrome, and even death.8,9,26,27 The data from our study show that there were no significant differences in the incidence of postoperative pneumonia, respiratory failure, anastomotic leakage, and mortality between two groups with or without DGE. The postoperative hospital stay with DGE was approximately 2 days longer, but the difference was not significant. Therefore, it currently remains difficult to evaluate the efficacy of pyloric drainage procedures at the time of esophagectomy. These ongoing controversies should motivate new solutions for DGE due to esophagectomy. Endoscopic balloon pyloric dilatation has been historically as efficacious as drainage procedures to prevent DGE in patients who undergo vagotomy for refractory ulcer disease. Many surgeons utilized balloon dilatation of the pylorus for DGE after esophagectomy for carcinoma. Swanson et al.21 used endoscopic pyloric balloon dilatation preoperatively; they suggested that preoperative endoscopic balloon dilatation can prevent clinically significant DGE in patients who undergo esophagectomy and obviate the need for pyloroplasty at esophagectomy. Manjari et al.28 compared intraoperative mechanical dilatation of the pylorus with forceps with pyloromyotomy and pyloroplasty; they found no difference among the three groups in terms of gastric emptying for liquids or solids, mechanical dilatation seemed to provide similar outcomes, and it can be utilized prophylactically. Kim et al.17 routinely performed pyloric drainage during esophagectomy and used endoscopic balloon dilatation in patients with DGE who were unresponsive to medical therapy; they found that two-thirds of patients with DGE showed increased rates of gastric emptying as measured by radioisotope imaging after balloon dilatation of the pylorus. Lanuti et al.29 demonstrated that postoperative balloon dilatation was equally effective in patients with or without pyloromyotomy exhibiting postoperative DGE. At our hospital, we used endoscopic balloon pyloric dilatation postoperatively. The results from the current study suggest that DGE commonly responds to conservative management and could be managed by endoscopic dilatation of the pylorus if necessary. In our series, 66.1% (37 of 56) of patients were adequately treated with conservative
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management; endoscopic balloon dilatation of the pylorus was used in 33.9% (19 of 56) of patients with DGE, yielding a 78.9% (15 of 19) success rate. Three patients did not improve as a result of the pyloric dilatation, with endoscopy showing each pylorus was open, suggesting that pyloric obstruction may not have been the source of their symptoms. These patients improved with time and were able to resume normal diet without significant symptoms. One patient with tumorrelated DGE was treated by a pyloric stent. No complications were identified in our study related to balloon pyloric dilation. No patient needed reoperation to manage DGE. Most episodes of DGE occurred within the first year of surgery, which confirms, despite vagotomy, the ability of the gastric conduit to recover motor function after esophagectomy over time.10–12 Although the effects of the balloon dilatation are temporary, gastric emptying may be sufficiently maintained to prevent the relapse of DGE. As gastric motor function improves with time after surgery, the effects of the dilatation may no longer be necessary and not be associated with the long-term sequelae of dumping and bile reflux. The data from our study showed a higher incidence of DGE in patients with intra-right thoracic gastric conduit, which was comparable to previous reports.29,30 Because we did not use a nuclear medicine gastric emptying scan to measure gastric emptying, the cause of differences in gastric emptying among the different surgical techniques cannot be determined. Conclusions
We understand the potential limitations in our study. First and foremost, retrospective data gathering introduces some selection biases into our results and analysis (e.g., there was inherent bias introduced by the surgeons as to whether they would make a gastric tube, and that clearly is a weakness of a retrospective study). Another weakness is the lack of a wellmatched control group. Moreover, there was no objective evaluation using radioisotope studies to confirm the lack of symptomatic DGE; this finding remains a component of reporting bias from the patients. Ideally, a prospective randomized controlled trial with preoperative or intraoperative versus selected postoperative endoscopic balloon pyloric dilatation might be useful to further evaluate the value and optimal perioperative timing (before, during, or after surgery) of endoscopic balloon pyloric dilatation in the management of DGE. In conclusion, omitting the pyloric drainage procedure does not lead to an increased incidence of DGE after esophagectomy with a gastric conduit for esophageal or gastric cardia carcinoma. Many patients responded to conservative management, and endoscopic balloon pyloric dilatation can be effective in managing the DGE postoperatively in most situations without complications. Disclosure Statement
No competing financial interests exist. References
1. Jemal A, Bray F, Center MM, et al. Global cancer statistics. CA Cancer J Clin 2011;61:69–90. 2. Boone J, Livestro DP, Elias SG, et al. International survey on esophageal cancer: Part I. Surgical techniques. Dis Esophagus 2009;22:195–202.
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3. Sutcliffe RP, Forshaw MJ, Tandon R, et al. Anastomotic strictures and delayed gastric emptying after esophagectomy: Incidence, risk factors and management. Dis Esophagus 2008;21:712–717. 4. Gockel I, Go¨nner U, Domeyer M, et al. Long-term survivors of esophageal cancer: Disease-specific quality of life, general health and complications. J Surg Oncol 2010;102: 516–522. 5. Mannell A, McKnight A, Esser JD. Role of pyloroplasty in the retrosternal stomach: Results of a prospective, randomized, controlled trial. Br J Surg 1990;77:57–59. 6. Fok M, Cheng SW, Wong J. Pyloroplasty versus no drainage in gastric replacement of the esophagus. Am J Surg 1991;162:447–452. 7. Law S, Cheung MC, Fok M, et al. Pyloroplasty and pyloromyotomy in gastric replacement of the esophagus after esophagectomy: A randomized controlled trial. J Am Coll Surg 1997;184:630–636. 8. Palmes D, Weilinghoff M, Colombo-Benkmann M, et al. Effect of pyloric drainage procedures on gastric passage and bile reflux after esophagectomy with gastric conduit reconstruction. Langenbecks Arch Surg 2007;392:135–141. 9. Velanovich V. Esophagogastrectomy without pyloroplasty. Dis Esophagus 2003;16:243–245. 10. Collard JM, Romagnoli R, Otte JB, Kestens PJ. The denervated stomach as an esophageal substitute is a contractile organ. Ann Surg 1998;227:33–39. 11. Izbe´ki F, Wittmann T, Odor S, et al. Synchronous electrogastrographic and manometric study of the stomach as an esophageal substitute. World J Gastroenterol 2005;11: 1172–1178. 12. Liu JF, Yu JH, Liu L, et al. The effects of blood motilin and gastrin on electrical activity and emptying of the intrathoracic stomach after esophagectomy for cancer [in Chinese]. Natl Med J China 2007;87:2346–2349. 13. Urschel JD, Blewett CJ, Young JE, et al. Pyloric drainage (pyloroplasty) or no drainage in gastric reconstruction after esophagectomy: A meta-analysis of randomized controlled trials. Dig Surg 2002;19:160–164. 14. Nakabayashi T, Mochiki E, Garcia M, et al. Gastropyloric motor activity and the effects of erythromycin given orally after esophagectomy. Am J Surg 2002;183:317–323. 15. Reddymasu SC, Singh S, Sankula R, et al. Endoscopic pyloric injection of botulinum toxin-A for the treatment of postvagotomy gastroparesis. Am J Med Sci 2009;337:161– 164. 16. Bemelman WA, Brummelkamp WH, Bartelsman JF. Endoscopic balloon dilation of the pylorus after esophagogastrostomy without a drainage procedure. Surg Gynecol Obstet 1990;170:424–426. 17. Kim JH, Lee HS, Kim MS, et al. Balloon dilatation of the pylorus for delayed gastric emptying after esophagectomy. Eur J Cardiothorac Surg 2008;33:1105–1111. 18. Lanuti M, DeDelva P, Morse CR, et al. Management of delayed gastric emptying after esophagectomy with endoscopic balloon dilatation of the pylorus. Ann Thorac Surg 2011;91:1019–1024. 19. Chinese Society of Esophageal Cancer, Chinese AntiCancer Association. Clinical practice guidelines for the diagnosis and treatment of esophageal cancer [in Chinese]. Beijing: Peking Union Medical College Press, 2011. 20. Lee HS, Kim MS, Lee JM, et al. Intrathoracic gastric emptying of solid food after esophagectomy for esophageal cancer. Ann Thorac Surg 2005;80:443–447.
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21. Swanson EW, Swanson SJ, Swanson RS. Endoscopic pyloric balloon dilatation obviates the need for pyloroplasty at esophagectomy. Surg Endosc 2012;26:2023–2028. 22. Lerut T, Coosemans W, De Leyn P, Van Raemdonck D. Gastroplasty: Yes or no to gastric drainage procedure. Dis Esophagus 2001;14:173–177. 23. Aly A, Jamieson GG. Reflux after oesophagectomy. Br J Surg 2004;91:137–141. 24. Burrows WM. Gastrointestinal function and related problems following esophagectomy. Semin Thorac Cardiovasc Surg 2004;16:142–151. 25. Hirao M, Fujitani K, Tsujinaka T. Delayed gastric emptying after distal gastrectomy for gastric cancer. Hepatogastroenterology 2005;52:305–309. 26. Wang LS, Huang MH, Huang BS, Chien KY. Gastric substitution for resectable carcinoma of the esophagus: An analysis of 368 cases. Ann Thorac Surg 1992;53:289– 294. 27. Martin JT, Federico JA, McKelvey AA, et al. Prevention of delayed gastric emptying after esophagectomy: A single center’s experience with botulinum toxin. Ann Thorac Surg 2009;87:1708–1714.
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28. Manjari R, Padhy AK, Chattopadhyay TK. Emptying of the intrathoracic stomach using three different pylorus drainage procedures—Results of a comparative study. Surg Today 1996;26:581–585. 29. Lanuti M, de Delva PE, Wright CD, et al. Post-esophagectomy gastric outlet obstruction: Role of pyloromyotomy and management with endoscopic pyloric dilatation. Eur J Cardiothorac Surg 2007;31:149–153. 30. Finley FJ, Lamy A, Clifton J, et al. Gastrointestinal function following esophagectomy for malignancy. Am J Surg 1995;169:471–475.
Address correspondence to: Bin Li, MD Department of Thoracic Surgery Lanzhou University Second Hospital Lanzhou University Second Clinical Medical College 82 Cuiyingmen Chengguan District, Lanzhou 730030, Gansu Province People’s Republic of China E-mail: [email protected]
Delayed Gastric Emptying After Esophagectomy for Malignancy Bin Li, MD, Jian-Hua Zhang, MD, Cheng Wang, MD, Tie-Niu Song, MM, Zhi-Qiang Wang, MM, Yun-Jiu Gou, PhD, Jian-Bao Yang, MM, and Xiao-Ping Wei, MM
Abstract
Background: Controversy still exists about the need for pyloric drainage procedures after esophagectomy with gastric conduit reconstruction. Although pyloric drainage may prevent postoperative delayed gastric emptying (DGE), it may also promote dumping syndrome and bile reflux. The aims of this study were to audit the incidence and management of DGE in patients without routine pyloric drainage after esophagectomy in a university medical center. Patients and Methods: From July 2006 to June 2012, data from 356 consecutive patients who underwent esophagectomy with a gastric conduit without pyloric drainage for esophageal or gastric cardia carcinoma were reviewed. Major observation parameters were the incidence, management, and outcomes of DGE. Results: Overall incidence of DGE was 15.7% (56 of 356). Early DGE developed in 26 patients, and late DGE developed in 30 patients. There were no differences in demographic and intraoperative data between the two groups with or without DGE. More DGE was documented in patients with an intra-right thoracic gastric conduit (P = .031). A higher incidence of postoperative pneumonia was observed in patients exhibiting early DGE, but without significance (P = .254). There were also no significant impacts on respiratory failure (P = .848) and anastomotic leakage (P = .257). There was an increased postoperative hospital stay with DGE, but without significance (P = .089). Endoscopic balloon dilatation of the pylorus was used to manage 33.9% of patients with DGE, yielding a 78.9% (15 of 19) success rate without complications. In 3 patients endoscopy showed the pylorus was open, and their symptoms improved over time. One patient with tumor-related DGE was treated by pyloric stent. The remaining patients were adequately treated with conservative management. Conclusions: Omitting the operative drainage procedure does not lead to an increased frequency of DGE after esophagectomy with a gastric conduit. Many patients responded to conservative management, and endoscopic balloon pyloric dilatation can be effective in managing the DGE postoperatively.
Introduction
E
sophageal carcinoma is the eighth most common cancer in the world, with an estimated 482,300 new diagnosis and 406,800 cancer deaths annually.1 Surgical resection remains the mainstay of treatment, whether performed for curative intent or for palliation of dysphagia.2 After esophagectomy, the stomach is predominantly used to restore continuity of the upper gastrointestinal (UGI) tract. However, complications related to the gastric conduit, such as delayed gastric emptying (DGE), are not uncommon, which may cause debilitating symptoms, delayed recovery, and poor quality of life.3,4
In an effort to promote gastric emptying, many surgeons perform pyloric drainage procedures, such as pyloroplasty or pyloromyotomy. But, no consensus has yet been reached on the need for pyloric drainage procedures after esophagectomy with gastric conduit reconstruction. Arguments for routine pyloric drainage include prevention of postoperative DGE to reduce the incidence of aspiration pneumonia and to improve early postoperative outcomes.5,6 Opponents argue that pyloric drainage may predispose to dumping syndrome and duodenal bile reflux esophagitis, impairing late postoperative functional outcomes without consistent benefits.7–9 In addition, several studies have documented an improvement in gastric emptying over time.10–12 Consequently, the benefits
Department of Thoracic Surgery, Lanzhou University Second Hospital, Lanzhou University Second Clinical Medical College, Lanzhou, People’s Republic of China.
306
DGE AFTER ESOPHAGECTOMY FOR MALIGNANCY
307
of routine pyloric drainage procedures are most likely to be realized in the immediate postoperative period by preventing aspiration pneumonia and gastric stasis.13 Indeed, DGE can be successfully managed postoperatively, and most patients respond adequately to medical therapy and endoscopic balloon pyloric dilatation.14–18 For these reasons, no pyloric drainage procedure was performed routinely after esophagectomy with gastric conduit reconstruction at our hospital. The aims of the current study were to audit the incidence and management of postoperative DGE in patients who underwent esophagectomy without pyloric drainage procedure in a single university medical center.
Furthermore, a nasogastric tube was placed in the intrathoracic stomach for gastrointestinal decompression, and a feeding tube was placed in the duodenum for postoperative nutritional support routinely. No pyloric drainage procedure was undertaken in this study. Nasogastric drainage was maintained on average 5–7 days or until barium swallow examination was performed on postoperative day (POD) 5–7 to confirm the absence of anastomotic leakage or DGE. The enteral feeding usually began on POD 2. Liquid oral diet was usually begun on POD 6–8, in the absence of signs of leakage. If a leakage was present, nutrition was maintained by a combined parenteral and feeding tube, and oral diet was resumed following closure of the leakage.
Patients and Methods
Assessments and management of postoperative DGE
Patients
Routine barium swallow examination was performed on POD 5–7 to assess for evidence of the leakage and DGE. Anastomotic leakage was defined as the extravasation of water-soluble contrast medium or the visualization of oral ingested methylene blue in the cervical or thoracic drainage. Clinical symptoms (e.g., nausea, emesis, bloating, regurgitation, chest pressure, and early satiety), barium swallow examination, gastric conduit dilatation or persistent air fluid level on radiography, and retention of food on UGI endoscopy supported the diagnosis of DGE. Operative mortality was defined as any death during the first 30 days after operation or during the same hospitalization as the operation. After discharge, patients were routinely examined every 3 months during the first year, every 6 months during the following 2 years, and annually thereafter at our hospital. In the case of DGE, barium swallow examination was conducted immediately. UGI endoscopy was immediately recommended in patients with symptoms of DGE and routinely recommended to be performed annually at follow-up with or without symptoms. DGE was managed with conservative management, including continuous gastrointestinal decompression by a nasogastric tube, traditional Chinese medicine–based therapies (acupuncture and physiotherapy), use of prokinetic medications (domperidone or cisapride), and observation, or by definitive management (endoscopic balloon pyloric dilatation). Pyloric dilatations were performed with controlled radial expansion balloon dilators over a guidewire visualized under fluoroscopic guidance to a maximal diameter of 20 mm. Endoscopic dilatation was performed using a 10-mm flexible UGI endoscope (Olympus, Tokyo, Japan), where the balloon dilator was inflated for at least 2 minutes, achieving a predetermined diameter at each session. Pyloric dilatation was performed until pyloric patency was achieved when the 10-mm endoscope could easily traverse the pyloric channel without resistance. Patients who required balloon pyloric dilatation were followed up, and dilatation sessions were applied if necessary until resolution of DGE symptoms.
Between July 2006 and June 2012, in total, 369 consecutive patients diagnosed with esophageal or gastric cardia carcinoma underwent procedures at our hospital. Patients who had undergone previous gastric surgery (n = 3) or esophagectomy with colonic transposition (n = 2) or were not treated because of metastatic disease (n = 8) were excluded. The remaining 356 patients formed the cohort for this study. They were operated on by surgical teams with similar experience in esophageal surgery. Preoperative diagnostic assessment, consisting of ultrasonography of the neck, abdominothoracic computed tomography scan, UGI endoscopy with biopsy, barium swallow examination, and Tc-99m whole-body bone scan, was performed for all patients. Electrocardiography, the pulmonary function test, and hematological and biochemistry tests were performed routinely. All recruited patients did not receive either neoadjuvant chemotherapy or radiotherapy. The study protocol was approved by the Ethics Committee of our hospital. Surgical approach
Patients who underwent esophagectomy during the study period were included regardless of surgical approach. The standardized surgical approaches19 included conventional open esophagectomy (i.e., left thoracotomy, Ivor Lewis, and McKeown approaches) and minimally invasive esophagectomy (i.e., thoracoscopic laparoscopic and thoracoscopic laparotomic approaches), with either cervical or intrathoracic anastomosis. In brief, general anesthesia was administered by a double-lumen tube. The intrathoracic esophagus was mobilized en bloc within an envelope of the adjoining tissues. The stomach was isolated, the left gastric vessels were transected at their base, and the right gastroepiploic vessels were preserved. The esophagus was transected at least 5 cm proximal to the upper edge of the tumor, and thoracoabdominal standard two-field lymph node dissection was performed. Reconstruction of the gastrointestinal tract with a whole stomach or gastric tube was adopted on the surgeon’s preference. In the latter, a 6-cm-wide gastric conduit was created with a linear cutter stapler ( Johnson & Johnson, New Brunswick, NJ) along the greater curvature, and the staple line was inverted with interrupted 3-0 silk sutures. Then, the gastric conduit was delivered through the posterior mediastinum, and esophagogastric anastomosis was performed with a hand-sewn or circular stapler.
Statistical analysis
Demographic and perioperative data were retrieved from the prospectively entered database. Follow-up outpatient evaluations were obtained by medical records, telephone interviews, or mail correspondence. Related data were analyzed with SPSS statistical package software (version 16.0; SPSS Inc., Chicago, IL). The chi-squared test or Fisher’s
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exact test was used for categorical data. Student’s t test or the Mann–Whitney U test was used for continuous data. Two-tailed P < .05 was considered to indicate statistical significance. Results Perioperative clinicopathologic characteristics
In total, 356 patients were included. The average follow-up duration was 32.3 – 17.8 (range, 3–66; median, 29) months. Patients were divided into two groups based on the absence or presence of DGE. The demographic and perioperative characteristics were compared and summarized in Table 1. Age, gender, comorbidity, tumor location, and histological type were not significantly different between the two groups. Esophagogastric anastomosis was fashioned at the cervical level in 55 patients (40 by McKeown approach, 15 by min-
Table 1. Demographic and Clinicopathologic Data for Patients With or Without Delayed Gastric Emptying
Age (mean – SD) (years) Gender Male Female Comorbidity Yes No Tumor location Upper thoracic Middle thoracic Lower thoracic Gastric cardia Histological type Squamous cell carcinoma Adenocarcinoma Surgical approach Left thoracotomy Ivor Lewis McKeown Minimally invasive Stomach transposition Whole stomach Gastric tube Gastric conduit location Intra-left thoracic Intra-right thoracic Anastomotic position Cervical level Above the aortic arch or azygos vein Under the aortic arch or azygos vein Anastomotic technique Hand-sewn Circular stapler
No DGE (n = 300)
DGE (n = 56)
56.3 – 9.6
58.6 – 8.7
245 55
46 10
113 187
23 33
30 163 71 36
7 35 9 5
262
50
38
6
165 92 31 12
22 22 9 3
205 95
39 17
165 135
22 34
43 191
12 34
66
10
123 177
25 31
P value .107 .933 .630 .485
.684
.179
.846
imally invasive approach) and intrathoracic in 301 patients (187 by left thoracotomy, 114 by Ivor Lewis approach). All cervical anastomoses were single layer hand-sewn. Intrathoracic anastomosis was by hand-sewn or circular stapler according to the surgeon’s preference. There were no significant differences in surgical approach (P = .179), stomach transposition (P = .846), anastomotic position (P = .371), and anastomotic technique (P = .612) between the two groups. In addition, more DGE was documented in patients with an intra-right thoracic gastric conduit (34 versus 22; P = .031). There was no significant difference in the frequency of the gastric tube location between the intra-left thoracic (51 of 187) and intra-right thoracic (61 of 169) (P = .073). Incidence, management, and outcomes of postoperative DGE
The overall incidence of DGE was 15.7% (56 of 356) in our series, including those patients with clinical symptoms, delayed emptying on barium swallow, dilated conduit with persistent air fluid level, or retained food on UGI endoscopy. The management of DGE varied with the severity of symptoms, degree of radiographic obstruction, and time of presentation and is detailed in Table 2. Early DGE (within 30 days from esophagectomy) developed in 26 of 56 patients (46.4%); 20 were managed conservatively as previously mentioned, resulting in control of their symptoms, and 6 were definitively managed with endoscopic balloon dilatation of the pylorus. Repeat dilatation was necessary in 1 patient for symptomatic relief, and 1 patient who exhibited acute intrathoracic stomach dilation in the early postoperative period (POD 9) required emergency endoscopic balloon pyloric dilatation. Five patients had immediate and complete resolution of their symptoms, but in 1 patient showing an open pylorus, his symptoms improved with time. As presented in Table 3, a trend of higher incidence of postoperative pneumonia was observed in patients exhibiting early DGE versus normal emptying, but without statistical significance (23.1% versus 14.7%; P = .254). There was also had no significant impact on incidences of anastomotic leakage (P = .257) and respiratory failure (P = .848). There was a tendency to increased length of postoperative hospital stay in patients with early DGE; this was due to an a stay of approximately 2 days longer compared with patients
Table 2. Management of 56 Patients with Delayed Gastric Emptying DGE (n = 56)
.031 Management .371
.612
DGE, delayed gastric emptying; SD, standard deviation.
Early (n = 26)
Late (n = 30)
Conservative 20 (76.9%) 17 (56.7%) Pyloric balloon dilatation 6 (23.1%) 13 (43.3%) Number of dilatations 1.3 – 0.5 (1–2) 1.6 – 1.1 (1–4) (range) Interval between surgery 16.5 – 2.9 days 11.3 – 6.7 months and dilatation Successful treatment 5 (83.3%) 10 (76.9%) Data are number (%) or mean – standard deviation values as indicated. DGE, delayed gastric emptying.
DGE AFTER ESOPHAGECTOMY FOR MALIGNANCY
Table 3. Postoperative Outcomes in Patients With or Without Early Delayed Gastric Emptying No DGE (n = 300) Pneumonia 44 Respiratory failure 14 Anastomotic leakage 10 Postoperative hospital 11.8 – 4.6 stay (days) Operative mortality 6
Early DGE (n = 26) P value 6 1 2 13.9 – 5.9
.254 .848 .257 .089
1
.533
Data are number of patients or mean – standard deviation values as indicated. DGE, delayed gastric emptying.
without DGE, but this was not statistically significant (P = .089). There was no intraoperative death in our series. The operative mortality was 2.0% in the entire cohort and 3.8% and 2.0% in the early DGE and no DGE groups, respectively, without significant difference (P = .533). Among these patients, 3 died of respiratory failure, 2 of anastomotic leakage, 1 of myocardial infarction, and 1 of pulmonary embolism. Late DGE (more than 30 days from esophagectomy) developed in 30 of 56 patients (53.6%), and the mean interval after original surgery was 11.3 – 6.7 (range, 2–23; median, 5) months. Seventeen patients were managed conservatively, and 13 were treated by endoscopic balloon pyloric dilatation. Pyloric dilatation was effective in 10 patients, but in 2 patients endoscopy showed the pylorus was open, and their symptoms improved over time; in another patient, locoregional recurrence tumor-related DGE was treated by a pyloric stent. Consequently, endoscopic balloon dilatation of the pylorus was used in 33.9% (19 of 56) of patients exhibiting DGE; 78.9% (15 of 19) were successfully managed without complications. The remaining 66.1% (37 of 56) of patients were adequately treated with conservative management. No patient needed reoperation to manage DGE. Discussion
The incidence of DGE after esophagectomy for esophageal malignancy with a gastric conduit has been reported to range from 15% to 50%.17,18,20,21 In our series, DGE occurred in 15.7% (56 of 356) of patients, which is comparable to these previous reports, suggesting that omitting the operative drainage procedure does not lead to an increased frequency of DGE after esophagectomy with a gastric conduit. For multifactorial reasons, the function of this gastric conduit is significantly altered compared with the native stomach.12,22–25 During esophagectomy, the bilateral disconnection of the vagus nerve was inevitable, which led to dysmotility of the gastric conduit and delayed emptying because of coordination of the pyloric opening. In dividing the left gastric artery at its base, collateral damage to celiac axis nerves caused the gastric sympathectomy that further influenced motor function. The natural antireflux mechanisms of the esophagus were inevitably damaged during surgery. The use of narcotic drugs may also have compromised the gastrointestinal function. After the operation, the stomach was moved into the thoracic cavity, its anatomical structure and physiological function were changed, and the negative pressure in the thoracic cavity and positive pressure inside the
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stomach formed differential pressure. In addition, changes in the gastrointestinal peptide hormones after the operation acted together to worsen the situation. The pyloric drainage procedures—pyloroplasty or pyloromyotomy—were used typically to prevent DGE after esophagectomy, but this remains an ongoing debate. Some investigators found drainage procedures improved gastric emptying and decreased the risk of postoperative aspiration pneumonia, and therefore morbidity and mortality.5,6 However, others have not consistently documented the benefits of these procedures.7,8 Urschel et al.13 reevaluated the need for pyloric drainage in an examination of nine randomized controlled trials. This meta-analysis, which included 553 patients, demonstrated short-term improvement in gastric emptying using the pyloric drainage procedure at the time of esophagectomy, but this had little effect on postoperative pulmonary morbidity, mortality, length of hospital stay, and long-term foregut function. Furthermore, these procedures may be technically challenging during minimally invasive esophagectomy, and they are associated with a small but definable morbidity, such as duodenal leak, pyloric stricture, bile reflux, dumping syndrome, and even death.8,9,26,27 The data from our study show that there were no significant differences in the incidence of postoperative pneumonia, respiratory failure, anastomotic leakage, and mortality between two groups with or without DGE. The postoperative hospital stay with DGE was approximately 2 days longer, but the difference was not significant. Therefore, it currently remains difficult to evaluate the efficacy of pyloric drainage procedures at the time of esophagectomy. These ongoing controversies should motivate new solutions for DGE due to esophagectomy. Endoscopic balloon pyloric dilatation has been historically as efficacious as drainage procedures to prevent DGE in patients who undergo vagotomy for refractory ulcer disease. Many surgeons utilized balloon dilatation of the pylorus for DGE after esophagectomy for carcinoma. Swanson et al.21 used endoscopic pyloric balloon dilatation preoperatively; they suggested that preoperative endoscopic balloon dilatation can prevent clinically significant DGE in patients who undergo esophagectomy and obviate the need for pyloroplasty at esophagectomy. Manjari et al.28 compared intraoperative mechanical dilatation of the pylorus with forceps with pyloromyotomy and pyloroplasty; they found no difference among the three groups in terms of gastric emptying for liquids or solids, mechanical dilatation seemed to provide similar outcomes, and it can be utilized prophylactically. Kim et al.17 routinely performed pyloric drainage during esophagectomy and used endoscopic balloon dilatation in patients with DGE who were unresponsive to medical therapy; they found that two-thirds of patients with DGE showed increased rates of gastric emptying as measured by radioisotope imaging after balloon dilatation of the pylorus. Lanuti et al.29 demonstrated that postoperative balloon dilatation was equally effective in patients with or without pyloromyotomy exhibiting postoperative DGE. At our hospital, we used endoscopic balloon pyloric dilatation postoperatively. The results from the current study suggest that DGE commonly responds to conservative management and could be managed by endoscopic dilatation of the pylorus if necessary. In our series, 66.1% (37 of 56) of patients were adequately treated with conservative
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management; endoscopic balloon dilatation of the pylorus was used in 33.9% (19 of 56) of patients with DGE, yielding a 78.9% (15 of 19) success rate. Three patients did not improve as a result of the pyloric dilatation, with endoscopy showing each pylorus was open, suggesting that pyloric obstruction may not have been the source of their symptoms. These patients improved with time and were able to resume normal diet without significant symptoms. One patient with tumorrelated DGE was treated by a pyloric stent. No complications were identified in our study related to balloon pyloric dilation. No patient needed reoperation to manage DGE. Most episodes of DGE occurred within the first year of surgery, which confirms, despite vagotomy, the ability of the gastric conduit to recover motor function after esophagectomy over time.10–12 Although the effects of the balloon dilatation are temporary, gastric emptying may be sufficiently maintained to prevent the relapse of DGE. As gastric motor function improves with time after surgery, the effects of the dilatation may no longer be necessary and not be associated with the long-term sequelae of dumping and bile reflux. The data from our study showed a higher incidence of DGE in patients with intra-right thoracic gastric conduit, which was comparable to previous reports.29,30 Because we did not use a nuclear medicine gastric emptying scan to measure gastric emptying, the cause of differences in gastric emptying among the different surgical techniques cannot be determined. Conclusions
We understand the potential limitations in our study. First and foremost, retrospective data gathering introduces some selection biases into our results and analysis (e.g., there was inherent bias introduced by the surgeons as to whether they would make a gastric tube, and that clearly is a weakness of a retrospective study). Another weakness is the lack of a wellmatched control group. Moreover, there was no objective evaluation using radioisotope studies to confirm the lack of symptomatic DGE; this finding remains a component of reporting bias from the patients. Ideally, a prospective randomized controlled trial with preoperative or intraoperative versus selected postoperative endoscopic balloon pyloric dilatation might be useful to further evaluate the value and optimal perioperative timing (before, during, or after surgery) of endoscopic balloon pyloric dilatation in the management of DGE. In conclusion, omitting the pyloric drainage procedure does not lead to an increased incidence of DGE after esophagectomy with a gastric conduit for esophageal or gastric cardia carcinoma. Many patients responded to conservative management, and endoscopic balloon pyloric dilatation can be effective in managing the DGE postoperatively in most situations without complications. Disclosure Statement
No competing financial interests exist. References
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Address correspondence to: Bin Li, MD Department of Thoracic Surgery Lanzhou University Second Hospital Lanzhou University Second Clinical Medical College 82 Cuiyingmen Chengguan District, Lanzhou 730030, Gansu Province People’s Republic of China E-mail: [email protected]
