Trends in the surgical management of diverticulitis
Nicole Wieghard, Cristina B. Geltzeiler, Vassiliki L. Tsikitis
Oregon Health and Science University, Portland, OR, USA
Department of Surgery, Oregon Health and Science University, Portland, OR, USA
Abstract
Sigmoid diverticulitis is an increasingly common Western disease associated with a high morbidity and cost of treatment. Improvement in the understanding of the disease process, along with advances in the diagnosis and medical management has led to recent changes in treatment recommendations. The natural history of diverticulitis is more benign than previously thought, and current trends favor more conservative, less invasive management. Despite current recommendations of more restrictive indications for surgery, practice trends indicate an increase in elective operations being performed for the treatment of diverticulitis. Due to diversity in disease presentation, in many cases, optimal surgical treatment of acute diverticulitis remains unclear with regard to patient selection, timing, and technical approach in both elective and urgent settings. As a result, data is limited to mostly retrospective and non-randomized studies. This review addresses the current treatment recommendations for surgical management of diverticulitis, highlighting technical aspects and patterns of care.
Keywords Elective surgery for uncomplicated diverticulitis, primary anastomosis versus Hartmann procedure, Hinchey I-II, Hinchey III-IV, laparoscopic versus open
Ann Gastroenterol 2015; 28 (1): 25-30
Introduction
Colonic diverticulosis is extremely common in Western countries. Prevalence increases with age, and is estimated to affect approximately 70% of individuals by age 80 [1]. Manifestations of diverticular disease, which include diverticulitis, bleeding, abscess, free perforation, fistula, and stricture formation account for significant disease burden and are frequently associated with poor outcomes, including mortality [2]. Furthermore, hospitalizations for acute diverticulitis are increasing, leading to escalating costs in the US, now estimated to exceed 2.4 billion dollars annually [3-5].
Our evolving understanding of the pathophysiology and natural history of the disease, as well as improvements in diagnostic imaging and nonsurgical management of the disease have led to significant changes in treatment recommendations [6,7]. Less aggressive medical and surgical treatments have been proposed. In cases of acute uncomplicated diverticulitis, outpatient management has been advocated for, and the use of antibiotics challenged [8-10]. Similarly, in cases of complicated diverticulitis, nonsurgical management is preferred initially, including percutaneous drainage of abscesses, given the high morbidity and mortality of urgent operations [11,12]. Maintenance of intestinal continuity via primary anastomosis and the use of minimally invasive approaches are advocated for in elective and urgent settings.
Current practice guidelines are tailored to the individual patient, taking into account risk factors, disease severity on initial presentation, persistent symptoms, and patient preferences [6,13]. Technical aspects of the various surgical treatments are left to the discretion of the individual surgeon. This review will highlight both current surgical recommendations and practice trends.
Uncomplicated diverticulitis
Patients with uncomplicated diverticulitis usually have an indolent course with a low incidence of subsequent complications [9,14,15]. The majority of patients successfully respond to outpatient management [8,16]. Inpatient treatment with bowel rest and IV antibiotics is recommended for those with persistent abdominal pain that does not improve with outpatient antibiotic therapy. Recently, the use of antibiotics in mild episodes of the disease has been questioned. A randomized controlled trial from Europe found no difference in recurrence or development of complications after one year in those treated with antibiotics, versus those who did not receive them [10]. Clinical judgment remains an important aspect of managing acute diverticulitis and determining resolution of acute inflammation.
Recurrence of acute diverticulitis is lower than previously thought. It is frequently reported that about one third of all patients with acute diverticulitis will have a recurrent attack, often within one year [6,17]. Recurrence after an uncomplicated episode of diverticulitis, however, has recently been shown to be much lower, with one prospective study reporting a recurrence of only 1.7% over five years of follow up [15]. Notably, a complicated recurrence after recovery from an uncomplicated episode is very rare, a finding demonstrated in multiple studies [2,7,17].
Elective surgery for uncomplicated diverticulitis
The guidelines for elective sigmoid colectomy for uncomplicated diverticulitis have changed [6]. The decision to proceed with elective resection should no longer be based on the number of episodes or age at onset [7], and routine “prophylactic” elective colectomy is no longer recommended after an acute episode [13,18]. Studies have shown that an increasing number of episodes of acute uncomplicated diverticulitis do not increase the risk of recurrence, complications, or the need for urgent operative management [18,19]. Further, the greatest risk of free perforation is during the first episode of disease [19]. Younger patients (age of onset <50 years) do not have a more aggressive course, as previously thought [20-22]. On the contrary, a lower threshold for both elective and urgent resection has been recommended in immunocompromised patients, given the associated increased risk for failure of medical management and increased risk of recurrent disease with significant morbidity [6,23].
Despite the restricted indications for elective surgery for acute diverticulitis, multiple population-based studies have shown a large increase in the number of elective colectomies performed in the United States [3,24]. This increase is most dramatic in younger patients, aged 18-44 years [3]. This data may suggest a delay in adoption of the practice guidelines and/or may reflect the increasing incidence of acute diverticulitis.
Complicated diverticulitis
Complicated diverticulitis encompasses a broad spectrum of disease presentation, ranging from small pericolic abscesses to perforation with generalized peritonitis and sepsis, as well as late complications, including fistula and stricture formation. Treatment of complicated diverticulitis in the acute setting depends on the patient’s overall clinical condition and degree of peritoneal contamination and infection. The most commonly used grading system to describe the severity of complicated diverticulitis is the Hinchey classification (Table 1) [25].
Table 1
Hinchey classification [25]
It has been estimated that about 15-20% of all patients admitted with acute diverticulitis, both complicated and uncomplicated, will require surgical intervention during their initial admission [6,26,27]. Those with complicated diverticulitis are even more likely to require an operation during their initial hospitalization, upwards of 50% of the time [4]. Given the substantial morbidity associated with urgent colectomy for complicated diverticulitis, however, there is a trend to favor non-operative management initially. The proportion of patients undergoing urgent colectomies has decreased in recent years, from 71 to 55% [4].
Hinchey I-II
The most common presentation of complicated diverticulitis is an abscess, estimated to occur in approximately 15% of patients [6]. For small abscesses <2 cm, medical management (bowel rest and IV antibiotics) is often sufficient. For larger abscesses >5 cm, image-guided percutaneous drainage is the preferred initial treatment [6,28,29]. According to recent studies, there has been a consistent increase in patients admitted with diverticular abscesses, as well as an increase in those undergoing percutaneous drain placement [4,26].
Hinchey III-IV
The incidence of free perforation (purulent and feculent peritonitis) appears to have remained stable in recent years at around 1.5% [4]. Patients who present with sepsis and diffuse peritonitis require urgent operative intervention [6]. Two single institution studies, however, have recently suggested nonoperative management for select patients in the absence of severe sepsis [30,31].
When treated nonoperatively, complicated diverticulitis is associated with high recurrence rates, reported up to 50%. When compared to those with uncomplicated diverticulitis higher incidences of late complications including persistent symptoms, abscess, fistula and stricture have been reported [32,33]. In several studies, the severity of the initial disease presentation, based on CT findings, is directly correlated to an increased risk of recurrence and subsequent complications [28,29,32]. To further evaluate this relationship, Ambrosetti et al developed a CT-based severity grade and correlated this retrospectively with patient outcomes, elucidating the value of imaging as a prognostic indicator to guide management [29]. A ”severe grade” on CT, which included evidence of abscess, extraluminal air, or extraluminal contrast was statistically predictive of medical treatment failure in the acute phase, and for increased risk of recurrence or additional complications after successful nonoperative management [29].
Location and size of the abscess on presentation also contributed to the risk of recurrence and failure of nonoperative treatment [17,28]. In a prospective study of 73 patients with diverticular abscesses, pelvic abscesses were associated with worse outcomes when compared to mesocolic abscesses [34]. In a retrospective study of 218 patients undergoing percutaneous drainage, a larger abscess, defined as size greater than 5 cm, was also significantly associated with higher recurrence rates [35].
Controversy exists as to whether or not elective colon resection after successful nonoperative management of complicated diverticulitis is necessary. This notion is supported by the fact that observation after percutaneous drainage appears to be safe in selected patients [35].
According to the American Society of Colon and Rectal Surgeons (ASCRS) practice parameters, elective colon resection should typically be advised after a complicated episode is initially treated nonoperatively, due to the high incidence of medical treatment failure, recurrence, and late complications [6]. In addition, patients with fistula formation or stricturing disease are recommended for resection. A summary of recommendations from the ASCRS Practice Parameters for Sigmoid Diverticulitis and the Association of Coloproctology of Great Britain and Ireland (ACPGBI) Position Statement on Elective Resection for Diverticulitis are presented in Table 2 [6,13].
Table 2
Comparison of published surgical treatment recommendations
Technical aspects of surgical management
Primary anastomosis versus Hartmann procedure (HP)
Options for definitive surgery involve resection of the affected colon with or without anastomosis. The two-stage approach, commonly called HP, refers to sigmoid colectomy with end colostomy and later colostomy reversal. HP became the standard procedure for perforated diverticulitis in the 1980s [36]. It is associated with a high morbidity and mortality, as well as a high rate of non-reversed colostomies, reported up to 55% [11,12]. Surgical management, therefore, has evolved away from HP to establishing intestinal continuity, via sigmoid colectomy and primary anastomosis (PA), with or without protective diverting loop ileostomy (DLI). This is often constructed in the presence of abscess or free perforation.
The surgical resection margin should extend proximally to compliant bowel (does not need to be free of diverticula) and distally to the upper rectum (where the taeniae coli coalesce). An adequate distal margin is the most important factor in determining recurrence after resection [6]. Recurrence risk with colocolonic anastomosis is up to four times higher than that of colorectal anastomosis [37]. Some have advocated for routine splenic flexure mobilization to facilitate tension-free anastomosis [13]. We believe, however, the need for this is determined intra-operatively, based on the patient body-habitus and length of colon resected.
The vast majority of elective resections, approximately 95%, are performed with PA [24]. Although historically, HP has been the procedure of choice in the urgent setting, retrospective studies comparing HP to PA with or without DLI have shown similar short-term outcomes (including mortality and postoperative infections) [38-42]. A systematic review concluded that the overall morbidity and mortality were higher for HP than for PA, suggesting that PA with or without proximal DLI is safe in patients with diverticular peritonitis [11]. Patient selection remains an important component. In most of these studies, the patients selected for PA were younger, with lower Hinchey scores [38]. In a trial by Oberkofler et al, which randomized 62 patients to PA with DLI versus HP found similar mortality and complication rates, only 58% of the patients who underwent HP, however, had future reversal of their stoma [43]. Furthermore, colostomy use has been associated with higher comorbidities [3]. Concordant with recommendations from the literature, recent data has shown that the use of primary anastomosis in the acute setting is increasing [24].
The current body of evidence suggests that primary anastomosis can and should be performed in patients with acute complicated diverticulitis, conditions permitting. Ultimately, this decision is left to the judgment of the surgeon, taking into account the clinical status of the patient including comorbidities, health of the remaining intestine, and extent of peritoneal contamination.
Approach to colon resection: laparoscopic versus open
Elective setting: The laparoscopic approach has been shown to have several advantages over open surgery, including lower mortality and postoperative complication rates, shorter hospital stays, and lower overall cost [44-48]. In the Sigma trial, which randomized 100 patients to laparoscopic vs open colectomy in the elective setting, the laparoscopic group had fewer major complications, though in long-term follow up, there were no differences between the two groups [49,50]. Two additional small-randomized trials failed to show a significant difference in outcomes, but these studies were underpowered and had difficulty with enrollment due to patients’ preference for laparoscopic surgery [51,52].
Overall, the number of laparoscopic colectomies performed for diverticular disease has been increasing, but remains lower than anticipated, with less than half of colectomies for diverticulitis being attempted laparoscopically [47,48].
Urgent setting: The role of laparoscopy in the urgent setting is incompletely evaluated [13]. In a small retrospective study, emergent laparoscopic surgery for patients with complicated diverticular disease was associated with decreased morbidity and a shorter length of stay, when compared to open procedures [53].
A laparoscopic HP has been proposed as a way to reduce the postoperative complications and expedite recovery. This has not been shown, however, to reduce postoperative morbidity and mortality after controlling for confounding variables and is therefore not currently recommended [54]. Overall, laparoscopic approach for one or two stage procedures is infrequently performed in the urgent setting and is reported in only 3.4-6% of all procedures [24,40].
Laparoscopic lavage
Current consensus holds that there is insufficient evidence to recommend laparoscopic lavage as an alternative to resection [6,7]. Laparoscopic lavage has been proposed as an alternative management strategy in patients with peritonitis in order to control contamination and bridge these patients to elective resection with primary anastomosis at a later date [55-58]. Small observational studies have shown fewer complications in patients with diverticulitis undergoing laparoscopic lavage versus primary resection. The patients selected for laparoscopic lavage were healthier with lower Hinchey grades. As a result, substantial selection bias confounds the generalizability of these results [55-58]. Anticipated future randomized trials may help clarify the role for laparoscopic lavage [59-62].
Concluding remarks
Overall, the surgical management of diverticular disease has evolved with current goals of maintaining intestinal continuity, using a laparoscopic approach, and controlling infection acutely to bridge patients to later one-stage procedures. Patient selection remains paramount to the surgical decision-making process and treatment plans should be individualized according to the needs of the patient.
Acknowledgment
The authors would like to thank Mary Kwatkosky-Lawlor for her assistance with the review process and the preparation of the bibliography.
References
1. Everhart JE, Ruhl CE. Burden of digestive disease in the United States Part II:Lower Gastrointestinal Diseases. Gastroenterology 2009;136: 741-754.
2. Humes DJ, West J. Role of acute diverticulitis in the development of complicated colonic diverticular disease and 1-year mortality after diagnosis in the UK:population-based cohort. Gut 2012;61: 95-100.
3. Etzioni DA, Mack TM, Beart RW Jr, Kaiser AM. Diverticulitis in the United States: 1998-2005. Changing patterns of disease and treatment. Ann Surg 2009;249: 210-217.
4. Ricciardi R, Baxter NN, Read TE, Marcello PW, Hall J, Roberts PL. Is the decline in surgical treatment for diverticulitis associated with an increase in complicated diverticulitis? Dis Colon Rectum 2009;52: 1558-1563.
5. Kozack LJ, DeFrances CJ, Hall MJ. National hospital discharge survey:2004 annual summary with detailed diagnosis and procedure data. Vital Health Stat 13 2006;162: 1-209.
6. Rafferty J, Shellito P, Hyman NH, Buie WD, Standards Committee of the American Society of Colon and Rectal Surgeons. Practice parameters for sigmoid diverticulitis. Dis Colon Rectum 2006;49: 939-944.
7. Regenbogen SE, Hardiman KM, Hendren S, Morris AM. Surgery for diverticulitis in the 21st Century:a systematic review. JAMA Surg 2014;149: 292-303.
8. Biondo S, Golda T, Kreisler R, et al. Outpatient versus hospital management for uncomplicated diverticulitis:a prospective, multicenter randomized clinical trial (DIVER Trial). Ann Surg 2014;259: 38-44.
9. Alonso S, Pera M, Pares S, et al. Outpatient treatment of patients with uncomplicated acute diverticulitis. Colorectal Dis 2010;12: 278-282.
10. Chabok A, Pahlman L, Hjern F, Haapaniemi S, Smedh K;AVOD Study Group. Randomized clinical trial of antibiotics in acute uncomplicated diverticulitis. Br J Surg 2012;99: 532-539.
11. Salem L, Flum DR. Primary anastomosis or Hartmann's for patients with diverticular peritonitis?A systematic review. Dis Colon Rectum 2004;47: 1953-1964.
12. Vermeulen J, Coene PP, Van Hout NM, et al. Restoration of bowel continuity after surgery for acute perforated diverticulitis:should Hartmann's procedure be considered a one-stage procedure? Colorectal Dis 2009;11: 619-624.
13. Fozard, JB, Armitage NC, Schofield JB, Jones, OM. ACPGBI position statement on elective resection for diverticulitis. Colorectal Dis 2011; 13(Suppl. 3):I-II.
14. Morris AM, Regenbogen SE, Hardiman KM, Hendren S. Sigmoid diverticulitis:a systematic review.JAMA Surg 2014;311: 287-297.
15. Salem TA, Molloy RG, O'Dwyer PJ. Prospective, five-year follow-up study of patients with symptomatic uncomplicated diverticular disease. Dis Colon Rectum 2007;50: 1-5.
16. Etzioni DA, Chiu VY, Cannom RR, Burchette RJ, Haigh PI, Abbas, MA. Outpatient treatment of acute diverticulitis:rates and predictors of failure. Dis Colon Rectum 2010;53: 861-865.
17. Hall JF, Roberts PL, Ricciardi et al. Long-term follow-up after an initial episode of diverticulitis:what are the predictors of recurrence? Dis Colon Rectum 2011;54: 283-288.
18. Broderick-Villa G, Burchette RJ, Collins JC, Abbas MA, Haigh PI. Hospitalization for acute diverticulitis does not mandate routine elective colectomy. Arch Surg 2005;140: 576-583.
19. Ritz JP, Lehmann KS, Frericks B, Stroux A, Buhr HJ, Holmer C. Outcome of patients with acute diverticulitis:Multivariate analysis of risk factors for free perforation. Surgery 2011;149: 606-613.
20. Hjern F, Josephson T, Altman D, Holmstrom, Johansson C. Outcome of younger patients with acute diverticulitis. Br J Surg 2008;95: 758-764.
21. Lopez-Borao J, Kreisler E, Millan M, et al. Impact of age on recurrence and severity of left colonic diverticulitis. Colorectal Dis 2012;14: 407-412.
22. Ritz JP, Lehmann KS, Stroux A, Buhr HJ, Holmer C. Sigmoid diverticulitis in young patients:a more aggressive disease than in older patients? J Gastrointest Surg 2011;15: 667-674.
23. Yoo PS, Garg R, Salamone LF, Floch MH, Rosenthal R, Longo WE. Medical comorbidities predict the need for colectomy for complicated and recurrent diverticulitis. Am J Surg 2008;196: 710-714.
24. Masoomi H, Buchberg BS, Magno C, Mills SD, Stamos MJ. Trends in diverticulitis management in the United States from 2002 2007. Arch Surg 2011;146: 400-406.
25. Hinchey EJ, Schaal PG, Richards PK. Treatment of perforated diverticular disease of the colon. Adv Surg 1978;12: 85-109.
26. Salem L, Anaya DA, Flum DR. Temporal changes in the management of diverticulitis. J Surg Res 2005;124: 318-323.
27. Morris AM, Regenbogen SE, Hardiman KM, Hendren S. Sigmoid diverticulitis:a systematic review.JAMA Surg 2014;311: 287-297.
28. Kaiser AM, Jiang J-K, Lake JP, et al. The management of complicated diverticulitis and the role of computed tomography. Am J Gastroenterol 2005;100: 910-917.
29. Ambrosetti P, Beeker C, Terrier F. Colonic diverticulitis:impact of imaging on surgical management - a prospective study of 542 patients. Eur Radiol 2002;12: 1145-1149.
30. Costi R, Cauchy F, LeBian A, Honart JF, Creuze N, Smadja C. Challenging a classic myth:pneumoperitoneum associated with acute diverticulitis is not an indication for open or laparoscopic emergency surgery in hemodynamically stable patients:A 10-year experience with nonoperative treatment. Surg Endosc 2012;26: 2061-2071.
31. Dharmarajan S, Hunt SR, Birnbaum EH, Fleshman JW, Mutch MG. The efficacy of nonoperative management of acute complicated diverticulitis. Dis Colon Rectum 2011;54: 663-671.
32. Nelson RS, Ewing BM, Wengert TJ, Thorson AG. Clinical outcomes of complicated diverticulitis managed nonoperatively. Am J Surg 2008;196: 969-974.
33. Ambrosetti, P. Value of CT for acute left-colonic diverticulitis:the surgeon's view. Dig Dis 2012;30: 51-55.
34. Ambrosetti P, Chauntems R, Soravia C, Peiris-Waser N, Terrier F. Long-term Outcome of mesocolic and pelvic diverticular abscesses of the left colon:a prospective study of 73 cases. Dis Colon Rectum 2005;48: 787-791.
35. Gaertner WB, Willis DJ, Madoff RD, et al. Percutaneous drainage of colonic diverticular abscess:is colon resection necessary? Dis Colon Rectum 2013;56: 622-626.
36. McDermott FD, Collins D, Heeney A, Winter DC. Minimally invasive and surgical management strategies tailored to the severity of acute diverticulitis. Br J Surg 2014;101: 90- 99.
37. Thaler K, Baig MK, Berho M, et al. Determinants of recurrence after sigmoid resection for uncomplicated diverticulitis. Dis Colon Rectum 2003;46:385-388.
38. Stumpf MJ, Vinces FY, Edwards J. Is primary anastomosis with proximal diversion safe in the surgical management of complications of acute diverticulitis? Am Surg 2007;73: 787-790.
39. Trenti L, Biondo S, Golda T et al. Generalized peritonitis due to perforated diverticulitis:Hartmann's procedure or primary anastomosis? Int J Colorectal Dis 2011;26: 377-384.
40. Tadlock MD, Karamanos E, Skiada D, et al. Emergency surgery for acute diverticulitis:which operation?A National Surgical Quality Improvement Program study. J Trauma Acute Care Surg 2013;74: 1385-1391.
41. Gawlick U, Nirula R. Resection and primary anastomosis with proximal diversion instead of Hartmann's:evolving the management of diverticulitis using NSQIP data. J Trauma Acute Care Surg 2012;72: 807-814.
42. Dreznik NI, Dueck DS, Arish A, et al. Emergency surgery for complicated acute diverticulitis. Colorectal Dis 2009;11: 198-202.
43. Oberkofler CE, Rickenbacher A, Raptis DA, et al. A multicenter randomized clinical trial of primary anastomosis or Hartmann's procedure for perforated left colonic diverticulitis with purulent or fecal peritonitis. Ann Surg 2012;256: 819-827.
44. Senagore AJ, Duepree HJ, Delaney CP, Dissanaike S, Brady KM, Fazio VW. Cost structure of laparoscopic and open sigmoid colectomy for diverticular disease:similarities and differences. Dis Colon Rectum 2002;45: 485-490.
45. Lawrence DM, Pasquale MD, Wasser TE. Laparoscopic versus open sigmoid colectomy for diverticulitis. Am Surg 2003;69: 499-503.
46. Levack M, Berger D, Sylla P, Rattner D, Bordeianou L. Laparoscopic decreases anastomotic leak rate in sigmoid colectomy for diverticulitis. Arch Surg 2011;146: 207-210.
47. Masoomi H, Buchberg B, Nguyen B, Tung V, Stamos MJ, Mills S. Outcomes of laparoscopic versus open colectomy in elective surgery for diverticulitis. World J Surg 2011;35: 2143-2148.
48. Yang CY, Chaudhry OO, Halabi WJ, et al. Outcomes of laparoscopic colorectal surgery:data from the Nationwide Inpatient Sample 2009. Am J Surg 2012;204: 952-957.
49. Klarenbeek BR, Veenhof AA, Bergamaschi R, et al. Laparoscopic sigmoid resection for diverticulitis decreases major morbidity rates:a randomized control trial:short-term results of the Sigma trial. Ann Surg 2009;249: 39-44.
50. Klarenbeek BR, Bergamaschi R, Veenhof AA, et al. Laparoscopic versus open sigmoid resection for diverticular disease:follow-up assessment of the randomized control Sigma trial. Surg Endosc 2001;25: 1121-1126.
51. Gervaz P, Inan I, Perneger T, Schiffer E, Morel P. A prospective randomized single-blind comparison of laparoscopic versus open sigmoid colectomy for diverticulitis. Ann Surg 2010;252: 3-8.
52. Raue W, Paolucci V, Asperger W et al. LAPDIV-CAMIC Trial Group. Laparoscopic sigmoid resection for diverticular disease has no advantages over open approach:midterm results of a randomized controlled trial. Langenbecks Arch Surg 2011;396: 973-980.
53. Letarte F, Hallet J, Drolet S, et al. Laparoscopic emergency surgery for diverticular disease that failed medical treatment:a valuable option?Results of a retrospective comparative cohort study. Dis Colon Rectum 2013;56: 1395-1402.
54. Turley RS, Barbas AS, Lidsky ME, Mantyh CR, Migaly J, Scarborough JE. Laparoscopic Versus open Hartmann procedure for the emergency treatment of diverticulitis:a propensity-matched analysis. Dis Colon Rectum 2013;56: 72-82.
55. Afshar S, Kurer MA. Laparoscopic peritoneal lavage for perforated sigmoid diverticulitis. Colorectal Dis 2011;14: 135-142.
56. Myers E, Hurley M, O'Sullivan GC, Kavanagh D, Wilson I, Winter DC. Laparoscopic peritoneal lavage for generalized peritonitis due to perforated diverticulitis. Br J Surg 2008;95: 97-101.
57. Karoui M, Champault A, Pautrat K, Valleur P, Cherqui D, Champault G. Laparoscopic peritoneal lavage or primary anastomosis with defunctioning stoma for Hinchey 3 complicated diverticulitis:results of a comparative study. Dis Colon Rectum 2009;52: 609-615.
58. Rogers AC, Collins D, O'Sullivan GC, Winter DC. Laparoscopic lavage for perforated diverticulitis:a population analysis. Dis Colon Rectum 2012;55: 932-938.
59. Oresland T, Schultz JK, Yaqub S, Rashidi M, Nilsen FR. Scandinavian diverticulitis trial –SCANDIV. A randomized prospective multicenter trial. http://www.scandiv.com/Scandiv/SCANDIV.html [accessed 3/1/2014].
60. Swank HA, Vermeulen J, Lange JF, et al. The ladies trial:laparoscopic peritoneal lavage or resection for purulent peritonitis and Hartmann's procedure or resection with primary anastomosis for purulent or faecal peritonitis in perforated diverticulitis (NTR2037). Study protocol. BMC Surg 2010;10: 1471-2482.
61. Thornell A, Angenete E, Gonzalez E, et al. Scandinavian Surgical Outcomes Research Group, SSORG. Treatment of acute diverticulitis laparoscopic lavage vs resection (DILALA):study protocol or a randomized controlled trial. Trials 2011;12:186.
62. ClinicalTrials.gov. LapLAND laparoscopic lavage for acute non-feculent diverticulitis. ://clinicaltrials.gov/show/NCT0101 9239 [accessed 3/1/2014].