Cited by 7Intestinal and Peritoneal AdhesionsHernia repair and managementEnhanced Recovery After Surgery

Laparoscopic application of sodium hyaluronate–carboxymethylcellulose barrier in abdominopelvic surgery: A Preferred Reporting Items for Systematic Reviews and Meta-Analyses for Systematic Review Protocols–compliant systematic review and meta-analysis

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Siebert, Terri, Moersdorf, Gerhard, Colberg, Torben·2024·Surgery

Abstract

Background We aimed to evaluate the incidence of postoperative adhesion formation and adhesion-related consequences (eg, bowel obstruction) after placement of a sodium hyaluronate–carboxymethylcellulose adhesion barrier after laparoscopic abdominopelvic surgery. Methods In this systematic review and meta-analysis, we searched the Medical Literature Analysis and Retrieval System Online and Embase via Ovid, Cochrane Central Register of Controlled Trials, ScienceDirect, BIOSIS Previews, Cumulative Index to Nursing and Allied Health Literature, and Clinical Trial Registries. A manual search (eg, Google Scholar and professional association websites) was also conducted to supplement the electronic database results. Two reviewers independently identified relevant studies based on inclusion and exclusion criteria and extracted data. Results A total of 28 studies were included in the systematic qualitative review. Three of the 28 studies included had comparable outcome measures, interventions, and control groups, allowing the pooling of study data. A total of 938 patients (490 patients in the sodium hyaluronate–carboxymethylcellulose barrier group and 448 in the no adhesion barrier group) from these 3 studies were included in the meta-analyses, which found the incidence of bowel obstruction was significantly lower (65% risk reduction) in the sodium hyaluronate–carboxymethylcellulose barrier group compared with the control group (relative risk = 0.35; 95% confidence interval, 0.19–0.63; P = .005) with extremely low heterogeneity between studies ( I 2 = 0; P = .41). The placement of sodium hyaluronate–carboxymethylcellulose barrier laparoscopically did not create new safety signals nor did it increase the incidence of adverse events. Conclusion Our meta-analysis found that laparoscopic application of a sodium hyaluronate–carboxymethylcellulose barrier in abdominopelvic surgery reduces the risk of bowel obstruction where applied during the early postoperative phase.

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Crossref · 10.1016/j.surg.2024.01.014

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  • Established HA-based products Hyalobarrier (gel) and Seprafilm (sheet) have demonstrated clinical efficacy in reducing adhesion formation, particularly in gynecologic and colorectal surgeries, with acceptable safety profiles.

    “Established products like Hyalobarrier (gel) and Seprafilm (sheet) have demonstrated clinical efficacy in reducing adhesion formation—particularly in gynecologic and colorectal surgeries—with acceptable safety profiles [124].”

    From Biomaterials in Postoperative Adhesion Barriers and Uterine Tissue Engineering (2025) · cites this paper as [124]

    The Discussion (page not available in our copy) reports that laparoscopically placed Seprafilm reduced postoperative bowel obstruction in colorectal surgery, using obstruction as a surrogate for adhesion formation; the Study limitations section reports no new safety signals or increase in adverse events. The paper does not address Hyalobarrier gel, and its colorectal result does not establish reduced adhesion formation for both products across gynecologic and colorectal surgery. (LLM, conf=0.88)

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Research works printed but not linked: 67

  1. Ruiz-Esparza GU, Wang X, Zhang X, et al. Nanoengineered shear-thinning hydrogel barrier for preventing postoperative abdominal adhesions. Nanomicro Lett. 2021;13:212.
  2. ten Broek RPG, Stommel MWJ, Strik C, van Laarhoven CJHM, Keus F, van Goor H. Benefits and harms of adhesion barriers for abdominal surgery: a systematic review and meta-analysis. Lancet. 2014;383:48e59.
  3. Fatehi Hassanabad A, Zarzycki AN, Jeon K, Deniset JF, Fedak PWM. Post-oper- ative adhesions: a comprehensive review of mechanisms. Biomedicines. 2021;9:867.
  4. Menzies D, Ellis H. Intestinal obstruction from adhesions-how big is the problem? Ann R Soll Surg England. 1990;72:60e63.
  5. ten Broek RPG, Krielen P, Di Saverio S, et al. Bologna guidelines for diagnosis and management of adhesive small bowel obstruction (ASBO): 2017 update of the evidence-based guidelines from the world society of emergency surgery ASBO working group. World J Emerg Surg. 2018;13:24.
  6. Aka AA, Wright JP, DeBeche-Adams T. Small bowel obstruction. Clin Colon Rectal Surg. 2021;34:219e226.
  7. Angenete E, Jacobsson A, Gellerstedt M, Haglind E. Effect of laparoscopy on the risk of small-bowel obstruction: a population-based register study. Arch Surg. 2012;147:359e365.
  8. Barmparas G, Branco BC, Schnüriger B, Lam L, Inaba K, Demetriades D. The incidence and risk factors of post-laparotomy adhesive small bowel obstruc- tion. J Gastrointest Surg. 2010;14:1619e1628.
  9. Schnuriger B, Barmparas G, Branco BC, Lustenberger T, Inaba K, Demetriades D. Prevention of postoperative peritoneal adhesions: a review of the literature. Am J Surg. 2011;201:111e121.
  10. Krielen P, Di Saverio S, Ten Broek R, et al. Laparoscopic versus open approach for adhesive small bowel obstruction, a systematic review and meta-analysis of short-term outcomes. J Trauma Acute Care Surg. 2020;88:866e874.
  11. Sajid MS, Khawaja AH, Sains P, Singh KK, Baig MK. A systematic review comparing laparoscopic vs open adhesiolysis in patients with adhesional small bowel obstruction. Am J Surg. 2016;212:138e150.
  12. Quah GS, Eslick GD, Cox MR. Laparoscopic versus open surgery for adhesional small bowel obstruction: a systematic review and meta-analysis of case-con- trol studies. Surg Endosc. 2019;33:3209e3217.
  13. Miyake H, Seo S, Pierro A. Laparoscopy or laparotomy for adhesive bowel obstruction in children: a systematic review and meta-analysis. Pediatr Surg Int. 2018;34:177e182.
  14. Bolnick A, Bolnick J, Diamond MP. Postoperative adhesions as a consequence of pelvic surgery. J Minim Invasive Gynecol. 2015;22:549e563.
  15. Diamond MP, Wexner SD, diZerega GS, et al. Adhesion prevention and reduction: current status and future recommendations of a multinational interdisciplinary consensus conference. Surg Innov. 2010;17:183e188.
  16. Fazio VW, Cohen Z, Fleshman JW, et al. Reduction in adhesive small-bowel obstruction by Seprafilm adhesion barrier after intestinal resection. Dis Colon Rectum. 2006;49:1e11.
  17. Park CM, Lee WY, Cho YB, et al. Sodium hyaluronate-based bioresorbable membrane (Seprafilm) reduced early postoperative intestinal obstruction after lower abdominal surgery for colorectal cancer: the preliminary report. Int J Colorectal Dis. 2009;24:305e310.
  18. Hashimoto D, Hirota M, Yagi Y, Baba H. Hyaluronate carboxymethylcellulose- based bioresorbable membrane (Seprafilm) reduces adhesion under the inci- sion to make unplanned re-laparotomy safer. Surg Today. 2012;42:863e867.
  19. Robb WB, Mariette C. Strategies in the prevention of the formation of post- operative adhesions in digestive surgery: a systematic review of the literature. Dis Colon Rectum. 2014;57:1228e1240.
  20. Hajibandeh S, Hajibandeh S, Saeed S, Bird J, Kannappa L, Ratnayake I. Effect of hyaluronate-based bioresorbable membrane (Seprafilm) on outcomes of abdominal surgery: a meta-analysis and trial sequential analysis of randomised controlled trials. Updates Surg. 2022;74:865e881.
  21. Zeng Q, Yu Z, You J, Zhang Q. Efficacy and safety of Seprafilm for preventing postoperative abdominal adhesion: systematic review and meta-analysis. World J Surg. 2007;31:2125e2131:discussion 2132.
  22. Zhao J, Huang C, Zhu J, Zhu J, Yuan R, Zhu Z. Efficacy and safety of Seprafilm for preventing intestinal obstruction after gastrointestinal neoplasms surgery: a systematic review and meta-analysis. Acta Chir Belg. 2021;121:1e15.
  23. Becker JM, Dayton MT, Fazio VW, et al. Prevention of postoperative abdominal adhesions by a sodium hyaluronate-based bioresorbable membrane: a pro- spective, randomized, double-blind multicenter study. J Am Coll Surg. 1996;183:297e306.
  24. Salum MR, Lam DT, Wexner SD, et al. Does limited placement of bioresorbable membrane of modified sodium hyaluronate and carboxymethylcellulose (Seprafilm) have possible short-term beneficial impact? Dis Colon Rectum. 2001;44:706e712.
  25. Moreira Jr H, Wexner SD, Yamaguchi T, et al. Use of bioresorbable membrane (sodium hyaluronate þ carboxymethylcellulose) after controlled bowel in- juries in a rabbit model. Dis Colon Rectum. 2000;43:182e187.
  26. Vrijland WW, Tseng LN, Eijkman HJ, et al. Fewer intraperitoneal adhesions with use of hyaluronic acid-carboxymethylcellulose membrane: a randomized clinical trial. Ann Surg. 2002;235:193e199.
  27. Salum M, Wexner SD, Nogueras JJ, et al. Does sodium hyaluronate-and carboxymethylcellulose-based bioresorbable membrane (Seprafilm) decrease operative time for loop ileostomy closure? Tech Coloproctol. 2006;10:187e191.
  28. Ha US, Koh JS, Cho KJ, et al. Hyaluronic acid-carboxymethylcellulose reduced postoperative bowel adhesions following laparoscopic urologic pelvic surgery: a prospective, randomized, controlled, single-blind study. BMC Urol. 2016;16: 28.
  29. Beck DE. The role of Seprafilm bioresorbable membrane in adhesion preven- tion. Eur J Surg Suppl. 1997;577:49e55.
  30. Hong MK, Ding DC. Seprafilm application method in laparoscopic surgery. JSLS. 2017;21, e2016.00097.
  31. Al-Musawi D, Thompson JN. Adhesion prevention: state of the art. Gynaecol Endoscop. 2001;10:123e130.
  32. Koketsu S, Sameshima S, Okuyama T, et al. An effective new method for the placement of an anti-adhesion barrier film using an introducer in laparoscopic surgery. Tech Coloproctol. 2015;19:551e553.
  33. Takeuchi H, Kitade M, Kikuchi I, Shimanuki H, Kinoshita K. A novel instrument and technique for using Seprafilm hyaluronic acid/carboxymethylcellulose membrane during laparoscopic myomectomy. J Laparoendosc Adv Surg Tech A. 2006;16:497e502.
  34. Shamseer L, Moher D, Clarke M, et al. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015: elaboration and expla- nation. BMJ. 2015;350:g7647.
  35. OCEBM Levels of Evidence Working Group. The Oxford 2011 levels of evidence. Oxford Centre for Evidence-Based Medicine.
  36. Tsuruta A, Itoh T, Hirai T, Nakamura M. Multi-layered intra-abdominal adhe- sion prophylaxis following laparoscopic colorectal surgery. Surg Endosc. 2015;29:1400e1405.
  37. Lee WK, Park YH, Choi S, Lee WS. Is liquid-based hyaluronic acid equivalent to sodium hyaluronate-based bioresorbable membrane to reduce small bowel obstruction in patients undergoing colorectal surgery. Asian J Surg. 2019;42: 443e449.
  38. Fujii S, Tsukamoto M, Shimada R, et al. Absorptive anti-adhesion barrier for the prevention of bowel obstruction after laparoscopic colorectal cancer surgery. J Anus Rectum Colon. 2018;2:1e8.
  39. Shimizu H, Kuriu Y, Arita T, et al. Simple and reliable method for the appli- cation of Seprafilm during laparoscopic surgery. Asian J Endosc Surg. 2022;15: 449e452.
  40. Nakashima M, Takeuchi M, Kawakami K. Effectiveness of barrier agents for preventing postoperative bowel obstruction after laparoscopic surgery: a retrospective cohort study. Surg Today. 2021;51:1335e1342.
  41. Reshef A, Hull TL, Kiran RP. Risk of adhesive obstruction after colorectal sur- gery: the benefits of the minimally invasive approach may extend well beyond the perioperative period. Surg Endosc. 2013;27:1717e1720.
  42. Hiranyakas A, Rather A, da Silva G, Weiss EG, Wexner SD. Loop ileostomy closure after laparoscopic versus open surgery: is there a difference? Surg Endosc. 2013;27:90e94.
  43. Nakase Y, Nakamura K, Sougawa A, et al. A novel procedure for introducing large sheet-type surgical material with a self-expanding origami structure using a slim trocar (chevron pleats procedure). Surg Endosc. 2017;31: 3749e3754.
  44. Chuang YC, Fan CN, Cho FN, Kan YY, Chang YH, Kang HY. A novel technique to apply a Seprafilm (hyaluronate-carboxymethylcellulose) barrier following laparoscopic surgeries. Fertil Steril. 2008;90:1959e1963.
  45. Ota K, Sato K, Ogasawara J, Takahashi T, Mizunuma H, Tanaka M. Safe and easy technique for the laparoscopic application of Seprafilm®in gynecologic sur- gery. Asian J Endosc Surg. 2019;12:242e245.
  46. Chuang YC, Lu HF, Peng FS, et al. Modified novel technique for improving the success rate of applying Seprafilm by using laparoscopy. J Minim Invasive Gynecol. 2014;21:787e790.
  47. Tsuzuki Y, Hirata T, Tsuzuki S, Wada S, Tamakoshi A. Risk factors of vaginal cuff infection in women undergoing laparoscopic hysterectomy for benign gyne- cological diseases. J Obstet Gynaecol Res. 2021;47:1502e1509.
  48. Weng CH, Chao AS, Huang HY, et al. A simple technique for the placement of seprafilm, a sodium hyaluronate or carboxymethylcellulose absorbable barrier, during laparoscopic myomectomy. J Minim Invasive Gynecol. 2019;27: 1203e1208.
  49. Huang PS, Sheu BC, Huang SC, Chang WC. Intraligamental myomectomy strategy using laparoscopy. J Minim Invasive Gynecol. 2016;23:954e961.
  50. Kusuki I, Suganuma I, Ito F, et al. Usefulness of moistening Seprafilm before use in laparoscopic surgery. Surg Laparosc Endosc Percutan Tech. 2014;24:e13. ee15.
  51. Takeuchi H, Kitade M, Kikuchi I, Shimanuki H, Kumakiri J, Takeda S. Influencing factors of adhesion development and the efficacy of adhesion-preventing agents in patients undergoing laparoscopic myomectomy as evaluated by a second-look laparoscopy. Fertil Steril. 2008;89:1247e1253.
  52. Chang WC, Chu LH, Huang PS, Huang SC, Sheu BC. Comparison of laparoscopic myomectomy in large myomas with and without leuprolide acetate. J Minim Invasive Gynecol. 2015;22:992e996.
  53. Huang C, Ding DC. Outcomes of adhesion barriers in gynecologic surgeries: a retrospective study at a medical center. Medicine (Baltimore). 2019;98, e18391.
  54. Hsu CS, Ding DC. Feasibility of wet and non-wet placement of Seprafilm in laparoscopic surgeries: a randomized controlled trial. J Clin Med. 2021;10:3526.
  55. Sano R, Ota Y, Tanaka T, Suzuki S, Shimoya K, Shiota M. A new technique for Seprafilm that can be practiced with a 5-mm trocar. Gynecol Minim Invasive Ther. 2021;10:168e170.
  56. Huang YT, Su YY, Wu KY, et al. Learning curve analysis of applying Seprafilm hyaluronic acid/carboxymethylcellulose membrane during laparoscopic hys- terectomy. Sci Rep. 2020;10, 16592.
  57. Khaitan E, Scholz S, Richards WO. Laparoscopic adhesiolysis and placement of Seprafilm: a new technique and novel approach to patients with intractable abdominal pain. J Laparoendosc Adv Surg Tech A. 2002;12:241e247.
  58. Khaitan L, Scholz S, Houston HL, Richards WO. Results after laparoscopic lysis of adhesions and placement of Seprafilm for intractable abdominal pain. Surg Endosc. 2003;17:247e253.
  59. Shinohara T, Kashiwagi H, Yanagisawa S, Yanaga K. A simple and novel tech- nique for the placement of antiadhesive membrane in laparoscopic surgery. Surg Laparosc Endosc Percutan Tech. 2008;18:188e191.
  60. Ha GW, Lee MR, Kim JH. Adhesive small bowel obstruction after laparoscopic and open colorectal surgery: a systematic review and meta-analysis. Am J Surg. 2016;212:527e536.
  61. Pecorelli N, Greco M, Amodeo S, Braga M. Small bowel obstruction and inci- sional hernia after laparoscopic and open colorectal surgery: a meta-analysis of comparative trials. Surg Endosc. 2017;31:85e99.
  62. Yamada T, Okabayashi K, Hasegawa H, et al. Meta-analysis of the risk of small bowel obstruction following open or laparoscopic colorectal surgery. Br J Surg. 2016;103:493e503.
  63. Bartels SA, Vlug MS, Hollmann MW, et al. Small bowel obstruction, incisional hernia and survival after laparoscopic and open colonic resection (LAFA study). Br J Surg. 2014;101:1153e1159.
  64. Burns EM, Currie A, Bottle A, Aylin P, Darzi A, Faiz O. Minimal-access colorectal surgery is associated with fewer adhesion-related admissions than open sur- gery. Br J Surg. 2013;100:152e159.
  65. ten Broek RP, Issa Y, van Santbrink EJ, et al. Burden of adhesions in abdominal and pelvic surgery: systematic review and meta-analysis. BMJ. 2013;347: f5588.
  66. Petersson J, Koedam TW, Bonjer HJ, et al. Bowel Obstruction and Ventral Hernia After Laparoscopic Versus Open Surgery for Rectal Cancer in A Randomized Trial (COLOR II). Ann Surg. 2019;269:53e57.
  67. Taylor GW, Jayne DG, Brown SR, et al. Adhesions and incisional hernias following laparoscopic versus open surgery for colorectal cancer in the CLASICC trial. Br J Surg. 2010;97:70e78.

Cited by

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Authors
Siebert, T., Moersdorf, G., & Colberg, T.
Affiliations
Baxter (United States) (US)
Corresponding author
Siebert, Terri
Venue
Surgery
Publisher
Elsevier BV
Published
2024-05
Volume
175
Issue
5
Pages
1358-1367
ISSN
0039-6060 (ISSN-L)
OpenAlex
W4392356175
Cited by
7
References
3
Citations by year
2026: 4 · 2025: 3
FWCI
0.71
Type
journal article
Language
en
Open access
Locations
  • Surgery (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
Funders
  • Baxter Healthcare Corporation
  • Baxter International Inc
Topics
  • Health Sciences › Medicine › Surgery › Intestinal and Peritoneal Adhesions
  • Health Sciences › Medicine › Surgery › Hernia repair and management
  • Health Sciences › Medicine › Surgery › Enhanced Recovery After Surgery
Keywords
anti-adhesion barrier, postoperative adhesions, intestinal obstruction, adhesion prevention, postoperative complications
MeSH terms
Abdomen, Systematic Reviews as Topic, Tissue Adhesions, Carboxymethylcellulose Sodium, Humans, Hyaluronic Acid, Intestinal Obstruction, Pelvis, Laparoscopy, Postoperative Complications

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