Skip to main content
JGH Open: An Open Access Journal of Gastroenterology and Hepatology logoLink to JGH Open: An Open Access Journal of Gastroenterology and Hepatology
. 2019 Nov 6;4(3):417–421. doi: 10.1002/jgh3.12267

Is water‐soluble contrast enema examination for integrity of rectal anastomosis necessary prior to ileostomy reversal?

Hui Lu Goh 1, Lauren Hawkins 1, Sivesh K Kamarajah 2,3, Sharad Karandikar 1, Mark Goldstein 1,
PMCID: PMC7273697  PMID: 32514447

Abstract

Background and Aim

Routine use of water‐soluble contrast enema (WSCE) to assess anastomotic integrity is debated. This study aimed to evaluate the role of WSCE to assess anastomotic integrity following anterior resections (AR) with defunctioning stoma prior to reversal and identify factors to limit its selective use.

Methods

This retrospective study evaluated all WSCE performed over a 7‐year period at a high‐volume colorectal unit. Risk factors for radiological abnormality/leak, including malignancy, chemoradiotherapy, and immediate postoperative complications, were recorded. A gastrointestinal specialist radiologist and surgeon validated all WSCEs reported as abnormal.

Results

Of the 486 WSCE studies identified, 92 were excluded (repeat studies (n = 51), pediatric cases [n = 2], no AR [n = 39]). A total of 394 WSCE studies were evaluated (260 cancer; 134 noncancer patients); 14% (37/260) of cancer patients and 8% (10/134) of noncancer patients had abnormal studies (P = 0.072). Of the 37 abnormal studies in cancer patients, 73% (27/37) radiological leaks were found, and 41% (n = 11/27) of these patients had postoperative complications. Of the 10 abnormal studies in noncancer patients, 20% (2/10) radiological leaks were found, but none of these patients had postoperative complications. Overall leak rates were 7% (29/394), and rates were significantly higher in cancer patients than noncancer patients (10 vs 2%, P = 0.005).

Conclusion

Routine use of WSCE may not be necessary prior to reversal. WSCE should be selectively used in event of postoperative leak or complications. Noncancer resections are less likely demonstrate a leak.

Keywords: leaks, outcome, rectal cancer, water‐soluble contrast


Routine use of water‐soluble contrast enema (WSCE) may not be necessary prior to reversal. WSCEs should be selectively used in the event of a postoperative leak or complications. Noncancer resections are less likely to demonstrate a leak.

graphic file with name JGH3-4-417-g002.jpg

Introduction

Anastomotic leaks (AL) following colorectal resection pose demonstrate short‐ and long‐term sequelae and increased postoperative morbidity and mortality.1, 2 The risk factors for developing an anastomotic leak are multifactorial, and it is difficult to identify a single causative risk factor for anastomotic leaks.1 A proximal defunctioning stoma can reduce the risk of serious sequelae, such as pelvic sepsis and collections. Stoma formations do not reduce the rate of anastomosis dehiscence postresection but can reduce it to subclinical anastomotic leaks.3 Traditionally, anastomotic integrity has been assessed endoscopically or radiologically to prevent complications from the primary anastomosis prior to reversal.

Water‐soluble contrast enemas (WSCEs) are a frequently used investigation method to assess anastomotic integrity and have been shown to be superior to computed tomography imaging for distal anastomoses.4 In recent years, there has been much debate regarding the routine use of WSCEs to assess anastomotic integrity compared to a simple digital rectal examination.5, 6, 7 However, these studies have focused predominantly on cases following resection for colorectal cancer, with limited data in noncancer resections.

The primary aim of this study is to examine the role of WSCEs to assess integrity following colorectal anterior resection (AR) in both cancer and noncancer patients. The secondary aim was to identify patient groups to be able to use WSCEs selectively based on their demographic, pathology, and postoperative complications.

Methods

This retrospective study evaluated WSCEs over a 7‐year period (October 2009 to April 2016) performed in a multisite, high‐volume colorectal unit. Consecutive patients undergoing WSCE were identified from the radiology database. Clinical notes and electronic records were also used to collate the inpatient data. Demographic, clinical, operative, and postoperative data were recorded and evaluated to identify risk factors for a radiological abnormality and/or leak, including malignancy, chemoradiotherapy, and postoperative complications. Postoperative complications were defined as the presence of complications according to the Clavien‐Dindo Classification grade.8 A radiologist with gastrointestinal specialization and a colorectal surgeon with more than 15 years of experience reviewed and validated all WSCEs reported as abnormal. Pediatric patients, repeat studies on the same patient, and patients who did not have anastomosis following AR were excluded. All WSCEs were performed by one of four consultant gastrointestinal radiologists with rectal intubation using a Foley catheter of varying sizes, with dilute gastrografin passed rectally.

Statistical analysis

Continuous variables were expressed as mean ± SD or median (interquartile range) and analyzed using t‐test or Mann–Whitney test where appropriate. Categorical variables were expressed as percentages and analyzed using chi‐square test or Fisher's exact test where appropriate. For all analyses, a P‐value <0.05 was considered statistically significant. Data analysis was undertaken using R Foundation Statistical Software (R 3.2.1, R Foundation for Statistical Computing, Vienna, Austria) as previously described.9, 10, 11, 12, 13, 14, 15, 16, 17, 18, 19, 20

Results

Of the WSCE studies performed, 81% (394/486) of WSCEs were included in the study cohort. Excluded cases were 51 repeat studies, two pediatric cases, and 39 cases that did not have an AR. The median age of the entire cohort was 60 years (interquartile range: 50–70 years), and a majority of patients were male (61%, 241/394). This study broadly classifies patients into two main groups: cancer (n = 260) versus non‐cancer resections (n = 134) (Table 1). Cancer patients were significantly older than noncancer patients (66 vs 46 years old, P < 0.001).

Table 1.

Indications of water‐soluble contrast enema

Indications Cancer, n = 270 (%) Noncancer, n = 163 P‐value
Check anastomosis integrity 260 (96) 134 (82) <0.001
Others 10 (4) 29 (18)

Others include strictures, fistula, hernia, and inflammatory bowel disease.

Statistical test used was chi‐square test.

There was no significant difference in gender between both groups. As seen in Figure 1, patients in the noncancer category had bowel resections following diverticular disease (strictures), inflammatory bowel disease (ulcerative colitis and Crohn's disease), colonic perforation, adhesions, fistula, incarcerated hernia, gynecological complications (resection following endometriosis stricture), urological complications (colonic injury during bladder or prostate surgery), and miscellaneous indications.

Figure 1.

Figure 1

Results by disease. UC, ulcerative colitis; WSCE, water‐soluble contrast enema.

Of the WSCE studies performed, 12% (n = 47/394) were abnormal. There were no significant differences in rates of abnormal studies between cancer and noncancer patients (14 vs 8%, P = 0.072) (Table 2). Of the 37 abnormal studies on cancer patients, 73% (27/37) were radiological leaks compared to 10 abnormal studies in non‐cancer patients, of which 20% (2/10) were radiological leaks.

Table 2.

Abnormal studies in cancer and noncancer group stratified by indications

Cancer group
Radiological leak, n = 28 (%) Stricture, n = 9 (%) Fistula, n = 3 (%) Others n = 3 (%) P‐value
Check anastomosis integrity 27 (96) 7 (78) 2 (67) 1 (33) 0.012
Specific pathology 1 (4) 2 (12) 1 (33) 2 (67)
Noncancer group
Radiological leak, n = 2 (%) Stricture, n = 6 (%) Fistula, n = 5 (%) Others n = 6 (%) P‐value
Check anastomosis integrity 2 (100) 3 (50) 1 (20) 4 (67) 0.219
Specific pathology 0 (0) 3 (50) 4 (80) 2 (33)

Others include hernia and inflammatory bowel disease.

Statistical test used was chi‐square test.

Of the WSCE studies conducted, only 7% (n = 29/394) had a leak radiologically (Table 3). The rates of radiological leaks were significantly higher in cancer patients than noncancer patients (10 vs 2%, P = 0.005). In patients with a radiological leak, there were no significant differences in age between cancer and noncancer patients (median: 65 vs 56 years old, P = 0.2). In the cancer patients, 41% (n = 11/27) with abnormal studies had postoperative complications or an identified leak postsurgery. All noncancer patients with abnormal studies had no postoperative complications or an identified leak postsurgery. In noncancer patients, 7% (n = 8/124) with normal studies had postoperative complications. Similarly, 9% (n = 19/223) of cancer patients with normal studies had postoperative complications.

Table 3.

Associated postoperative complications in those with abnormal and normal water‐soluble contrast enema studies

Abnormal studies—radiological leak Cancer, n = 27 (%) Other patients, n = 2 (%) P‐value
Inpatient complication 12 (44) 0 (0) 0.654
No complication 15 (56) 2 (100)
Normal studies Cancer, n = 223 (%) Other patients, n = 124 (%) P‐value
Inpatient complication 23 (10) 8 (7) 0.072
No complication 200 (90) 116 (93)

Discussion

Reversal of a defunctioning loop ileostomy in the presence of a radiological leak is associated with poor surgical outcome, increased health care, and financial costs.21 In low AR for rectal cancer, a temporary defunctioning ileostomy is recommended.22 The septic consequences of anastomotic dehiscence can be reduced by performing a loop ileostomy to divert fecal stream.23 Despite an increasing trend of diverting stomas being fashioned, no clear guidance exists as to when and how to assess anastomotic integrity and patency and the best way to manage patient with an established leak.

A WSCE is commonly performed prior to the reversal of defunctioning stoma for assessment of anastomotic integrity and to rule out any leak, blockage, or fistula formation.23, 24 These examinations are sometimes difficult to interpret in the presence of a pouch or when there is a “dog ear” from a colorectal anastomosis using the double‐stapling technique. This is usually performed 6–8 weeks after the primary operation, prior to ileostomy closure.25 It has been demonstrated that the use of WSCE in the immediate postoperative period has a low predictive value in detecting subclinical leaks and might disrupt an intact anastomosis by the pressure produced when installing the contrast.26 Furthermore, having a WSCE performed in the early postoperative period with an underlying sepsis could potentially spread infection hematogenously from excessive air insufflation.27

Its routine use, however, is debated. Several studies have shown that WSCE does not add value or alter patient management when the results of endoscopic or digital rectal examination are normal.25, 27, 28 In other studies, however, a contrast enema was effective in excluding clinically significant anastomotic problems, especially after clinical anastomotic leaks.5

The overall radiological leak rate on WSCE in this study was 7% (29/394). All leaks were identified by clinical acumen and confirmed radiographically. If a leak is suspected, a pelvic computed tomography (CT) scan is often used initially. A CT scan can not only detect a leak but can also accurately outline the presence and extent of pelvic abscess.28 In this study, seven patients in the cancer group had a CT scan performed postoperatively, which confirmed anastomotic leak. In four of these patients, subsequent contrast enemas were abnormal—three showed an anastomotic leak and one a fistula.

The majority of patients with a proven radiological leak on WSCE performed prior to reversal of ileostomy were male (80%, 24/30), with only 20% (6/30) female. Our findings agree with a systematic review conducted by Pommergaard et al. that male gender is one of the preoperative risk factors for anastomotic leakage after resection for colorectal cancer.29 It has been inferred that male gender poses a higher risk to anastomotic leakage due to the deeper and narrow pelvic anatomy, contributing to technical difficulties.30, 31 This study also found that 93% (27/29) with a confirmed radiological leak on WSCE were cancer resections, whereas 7% (2/29) were noncancer resections.

Several studies have evaluated a variety of risk factors of anastomotic leaks (AL); however, there is no universal agreement regarding the associated risk factors. Although it is generally accepted that variables such as low anastomotic level, smoking status, and presence of comorbidities are associated with leakage,32, 33, 34 other risk factors, including male gender and neoadjuvant chemoradiotherapy (nCRT), are not widely recognized.35 Although many studies have investigated risk factors of AL, it remains a life‐threatening complication that can arise in patients with no known risk factors.

Anastomotic leakage following AR has been reported with increased rates after nCRT.36, 37 It has been explained that preoperative radiotherapy results in local inflammation and tissue fibrosis, and could reduce wound healing, thus increasing the risk of anastomotic leakage.37 We identified five patients in the cancer group who received preoperative chemoradiotherapy prior to primary resection. Three of these patients who had preoperative chemoradiotherapy had an uneventful postoperative course and a subsequent normal WSCE study. One patient who received radiotherapy developed a postoperative complication or clinical leak following primary surgery but had a subsequent normal WSCE study. The second patient, however, developed a postoperative complication, with a confirmed leak on subsequent WSCE. Our study suggests that no evaluation by WSCE may be needed in those receiving neoadjuvant chemotherapy if there was no postoperative complication; however, further evaluation of this is required given the limited number of cases.

In addition to anastomotic defects, it is also essential to evaluate colorectal anastomosis for radiological stricture (not functional). WSCE detected seven strictures in the cancer group and three strictures in the noncancer group. This comprises of 3% (15/433) of all WSCE studies. This is comparable to a cross‐sectional review performed across 11 studies, in which the rate of detected strictures varied from 0 to 25%.5 Our WSCE studies also identified two fistulas: one with abnormal anatomy in the cancer group and one fistula and four other strictures (adhesions, abnormal anatomy and mass) in noncancer patients.

The limitation of the study is that, being retrospective, it is unable to evaluate variation in surgical technique and experience of the surgeon, chemoradiotherapy regimen, and radiological technique for performing the WSCEs. The extent and variability of the pelvic pathology and preoperative risk factors for anastomotic dehiscence smoking or BMI could not be studied. Finally, multivariable analysis was not possible due to an insufficient number of cases to adjust for other confounding factors. Hence it is not clear if cancer surgery is associated with a higher likelihood of requiring WSCE.

In conclusion, this study appears to demonstrate that WSCE prior to reversal to demonstrate an anastomotic leak in the absence of a clinical postoperative anastomotic leak may not necessary. Patients with postoperative complications or at a high risk of anastomotic dehiscence are best served by WSCEs prior to reversal. Selective use of WSCEs will reduce patient radiation exposure and the cost to the health‐care system. Future studies should aim to further validate our findings in larger cohorts.

Declaration of conflict of interest: None.

References

  • 1. Makela JT, Kiviniemi H, Laitinen S. Risk factors for anastomotic leakage after left‐sided colorectal resection with rectal anastomosis. Dis. Colon Rectum. 2003; 46: 653–60. [DOI] [PubMed] [Google Scholar]
  • 2. Petersen S, Freitag M, Hellmich G, Ludwig K. Anastomotic leakage: impact on local recurrence and survival in surgery of colorectal cancer. Int. J. Colorectal Dis. 1998; 13: 160–3. [DOI] [PubMed] [Google Scholar]
  • 3. den Dulk M, Marijnen CA, Collette L et al Multicentre analysis of oncological and survival outcomes following anastomotic leakage after rectal cancer surgery. Br. J. Surg. 2009; 96: 1066–75. [DOI] [PubMed] [Google Scholar]
  • 4. Nicksa GA, Dring RV, Johnson KH, Sardella WV, Vignati PV, Cohen JL. Anastomotic leaks: what is the best diagnostic imaging study? Dis. Colon Rectum. 2007; 50: 197–203. [DOI] [PubMed] [Google Scholar]
  • 5. Habib K, Gupta A, White D, Mazari FA, Wilson TR. Utility of contrast enema to assess anastomotic integrity and the natural history of radiological leaks after low rectal surgery: systematic review and meta‐analysis. Int. J. Colorectal Dis. 2015; 30: 1007–14. [DOI] [PubMed] [Google Scholar]
  • 6. Larsson A, Lindmark G, Syk I, Buchwald P. Water soluble contrast enema examination of the integrity of the rectal anastomosis prior to loop ileostomy reversal may be superfluous. Int. J. Colorectal Dis. 2015; 30: 381–4. [DOI] [PubMed] [Google Scholar]
  • 7. Shalabi A, Duek SD, Khoury W. Water‐soluble enema prior to ileostomy closure in patients undergoing low anterior resection: is it necessary? J. Gastrointest. Surg. 2016; 20: 1732–7. [DOI] [PubMed] [Google Scholar]
  • 8. Clavien PA, Barkun J, de Oliveira ML et al The Clavien‐Dindo classification of surgical complications: five‐year experience. Ann. Surg. 2009; 250: 187–96. [DOI] [PubMed] [Google Scholar]
  • 9. Kamarajah SK, Barmayehvar B, Sowida M, Adlan A, Reihill C, Ellahee P. Absence of association between preoperative estimated glomerular filtration rates and postoperative outcomes following elective gastrointestinal surgeries: a prospective cohort study. Anesthesiol. Res. Pract. 2018; 2018: 5710641. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10. Kamarajah SK. Adjuvant radiotherapy following pancreaticoduodenectomy for ampullary adenocarcinoma improves survival in node‐positive patients: a propensity score analysis. Clin. Transl. Oncol. 2018; 20: 1212–8. [DOI] [PubMed] [Google Scholar]
  • 11. Kamarajah SK, Sonnenday CJ, Cho CS et al Association of adjuvant radiotherapy with survival after margin‐negative resection of pancreatic ductal adenocarcinoma: a propensity‐matched National Cancer Database (NCDB) analysis. Ann. Surg. 2019. 10.1097/SLA.0000000000003242. [Epub ahead of print] [DOI] [PubMed] [Google Scholar]
  • 12. Bundred J, Kamarajah SK, Roberts KJ. Body composition assessment and sarcopenia in patients with pancreatic cancer: a systematic review and meta‐analysis. HPB (Oxford). 2019; 22: 10–22. [DOI] [PubMed] [Google Scholar]
  • 13. Kamarajah SK, Frankel TL, Sonnenday C, Cho CS, Nathan H. Critical evaluation of the American Joint Commission on Cancer (AJCC) 8th edition staging system for patients with Hepatocellular Carcinoma (HCC): a Surveillance, Epidemiology, End Results (SEER) analysis. J. Surg. Oncol. 2018; 117: 644–50. [DOI] [PubMed] [Google Scholar]
  • 14. Kamarajah SK. Fibrosis score impacts survival following resection for hepatocellular carcinoma (HCC): a Surveillance, End Results and Epidemiology (SEER) database analysis. Asian J. Surg. 2018; 41: 551–61. [DOI] [PubMed] [Google Scholar]
  • 15. Trivedi PJ, Reece J, Laing RW et al The impact of ileal pouch‐anal anastomosis on graft survival following liver transplantation for primary sclerosing cholangitis. Aliment. Pharmacol. Ther. 2018; 48: 322–32. [DOI] [PubMed] [Google Scholar]
  • 16. Kamarajah SK, Arntdz K, Bundred J, Gunson B, Haydon G, Thompson F. Outcomes of pregnancy in recipients of liver transplants. Clin. Gastroenterol. Hepatol. 2019; 17: 1398–404.e1. [DOI] [PubMed] [Google Scholar]
  • 17. Kamarajah SK. Pancreaticoduodenectomy for periampullary tumours: a review article based on Surveillance, End Results and Epidemiology (SEER) database. Clin. Transl. Oncol. 2018; 20: 1153–60. [DOI] [PubMed] [Google Scholar]
  • 18. Kamarajah SK, Sutandi N, Robinson SR, French JJ, White SA. Robotic versus conventional laparoscopic distal pancreatic resection: a systematic review and meta‐analysis. HPB (Oxford). 2019; 21: 1107–18. [DOI] [PubMed] [Google Scholar]
  • 19. Kamarajah SK, Chapman SJ, Glasbey J et al Systematic review of the stage of innovation of biological mesh for complex or contaminated abdominal wall closure. BJS Open. 2018; 2: 371–80. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20. Kamarajah SK, Burns WR, Frankel TL, Cho CS, Nathan H. Validation of the American Joint Commission on Cancer (AJCC) 8th edition staging system for patients with pancreatic adenocarcinoma: a Surveillance, Epidemiology and End Results (SEER) analysis. Ann. Surg. Oncol. 2017; 24: 2023–30. [DOI] [PubMed] [Google Scholar]
  • 21. Asteria CR, Gagliardi G, Pucciarelli S et al Anastomotic leaks after anterior resection for mid and low rectal cancer: survey of the Italian Society of Colorectal Surgery. Tech. Coloproctol. 2008; 12: 103–10. [DOI] [PubMed] [Google Scholar]
  • 22. Moran B, Cunningham C, Singh T et al Association of Coloproctology of Great Britain & Ireland (ACPGBI): guidelines for the management of cancer of the colon, rectum and anus (2017) ‐ surgical management. Colorectal Dis. 2017; 19 (Suppl. 1): 18–36. [DOI] [PubMed] [Google Scholar]
  • 23. Shorthouse AJ, Bartram CI, Eyers AA, Thomson JP. The water soluble contrast enema after rectal anastomosis. Br. J. Surg. 1982; 69: 714–7. [DOI] [PubMed] [Google Scholar]
  • 24. Killeen S, Souroullas P, Ho Tin H et al Outcomes of asymptomatic anastomotic leaks found on routine postoperative water‐soluble enema following anterior resection for cancer. World J. Surg. 2013; 37: 2700–4. [DOI] [PubMed] [Google Scholar]
  • 25. Tang CL, Seow‐Choen F. Digital rectal examination compares favourably with conventional water‐soluble contrast enema in the assessment of anastomotic healing after low rectal excision: a cohort study. Int. J. Colorectal Dis. 2005; 20: 262–6. [DOI] [PubMed] [Google Scholar]
  • 26. Akyol AM, McGregor JR, Galloway DJ, George WD. Early postoperative contrast radiology in the assessment of colorectal anastomotic integrity. Int. J. Colorectal Dis. 1992; 7: 141–3. [DOI] [PubMed] [Google Scholar]
  • 27. Dimitriou N, Panteleimonitis S, Dhillon A et al Is the routine use of a water‐soluble contrast enema prior to closure of a loop ileostomy necessary? A review of a single institution experience. World J. Surg. Oncol. 2015; 13: 331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28. Kalady MF, Mantyh CR, Petrofski J, Ludwig KA. Routine contrast imaging of low pelvic anastomosis prior to closure of defunctioning ileostomy: is it necessary? J. Gastrointest. Surg. 2008; 12: 1227–31. [DOI] [PubMed] [Google Scholar]
  • 29. Pommergaard HC, Gessler B, Burcharth J, Angenete E, Haglind E, Rosenberg J. Preoperative risk factors for anastomotic leakage after resection for colorectal cancer: a systematic review and meta‐analysis. Colorectal Dis. 2014; 16: 662–71. [DOI] [PubMed] [Google Scholar]
  • 30. Hida J, Yasutomi M, Maruyama T et al Anterior resection following posterior transsacral stapling and transection of the anal canal for low‐lying rectal cancer in males. Surg. Today. 1998; 28: 768–9. [DOI] [PubMed] [Google Scholar]
  • 31. Targarona EM, Balague C, Pernas JC et al Can we predict immediate outcome after laparoscopic rectal surgery? Multivariate analysis of clinical, anatomic, and pathologic features after 3‐dimensional reconstruction of the pelvic anatomy. Ann. Surg. 2008; 247: 642–9. [DOI] [PubMed] [Google Scholar]
  • 32. Alves A, Panis Y, Trancart D, Regimbeau JM, Pocard M, Valleur P. Factors associated with clinically significant anastomotic leakage after large bowel resection: multivariate analysis of 707 patients. World J. Surg. 2002; 26: 499–502. [DOI] [PubMed] [Google Scholar]
  • 33. Buchs NC, Gervaz P, Secic M, Bucher P, Mugnier‐Konrad B, Morel P. Incidence, consequences, and risk factors for anastomotic dehiscence after colorectal surgery: a prospective monocentric study. Int. J. Colorectal Dis. 2008; 23: 265–70. [DOI] [PubMed] [Google Scholar]
  • 34. Kim JS, Cho SY, Min BS, Kim NK. Risk factors for anastomotic leakage after laparoscopic intracorporeal colorectal anastomosis with a double stapling technique. J. Am. Coll. Surg. 2009; 209: 694–701. [DOI] [PubMed] [Google Scholar]
  • 35. Wang L, Gu J. Risk factors for symptomatic anastomotic leakage after low anterior resection for rectal cancer with 30 Gy/10 f/2 w preoperative radiotherapy. World J. Surg. 2010; 34: 1080–5. [DOI] [PubMed] [Google Scholar]
  • 36. Law WI, Chu KW, Ho JW, Chan CW. Risk factors for anastomotic leakage after low anterior resection with total mesorectal excision. Am. J. Surg. 2000; 179: 92–6. [DOI] [PubMed] [Google Scholar]
  • 37. Vignali A, Fazio VW, Lavery IC et al Factors associated with the occurrence of leaks in stapled rectal anastomoses: a review of 1,014 patients. J. Am. Coll. Surg. 1997; 185: 105–13. [DOI] [PubMed] [Google Scholar]

Articles from JGH Open: An Open Access Journal of Gastroenterology and Hepatology are provided here courtesy of Wiley

RESOURCES