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Open Access 01-12-2014 | Research

Evaluation of the effects of hyaluronic acid-carboxymethyl cellulose barrier on ovarian tumor progression

Authors: Laetitia Picaud, Benoît Thibault, Eliane Mery, Monia Ouali, Alejandra Martinez, Jean-Pierre Delord, Bettina Couderc, Gwenael Ferron

Published in: Journal of Ovarian Research | Issue 1/2014

Abstract

Background

Hyaluronic acid is a prognostic factor in ovarian cancers. It is also a component of Hyaluronic Acid-Carboxymethyl Cellulose (HA-CMC) barrier, an anti-adhesion membrane widely used during abdominal surgeries in particular for ovarian carcinosis. 70% of patients who undergo ovarian surgery will relapse due to the persistence of cancer cells. This study’s objective was to determine the oncological risk from use of this material, in the presence of residual disease, despite the benefit gained by it decreasing post-surgical adhesions in order to provide an unambiguous assessment of its appropriateness for use in ovarian surgical management.

Methods

We assessed the effects of HA-CMC barrier on the in vitro proliferation of human ovarian tumor cell lines (OVCAR-3, IGROV-1 and SKOV-3). We next evaluated, in vivo in nude mice, the capacity of this biomaterial to regulate the tumor progression of subcutaneous and intraperitoneal models of ovarian tumor xenografts.

Results

We showed that HA-CMC barrier does not increase in vitro proliferation of ovarian cancer cell lines compared to control. In vivo, HA-CMC barrier presence with subcutaneous xenografts induced neither an increase in tumor volume nor cell proliferation (Ki67 and mitotic index). With the exception of an increased murine carcinosis score in peritoneum, the presence of HA-CMC barrier with intraperitoneal xenografts modified neither macro nor microscopic tumor growth. Finally, protein analysis of survival (Akt), proliferation (ERK) and adhesion (FAK) pathways highlighted no activation on the xenografts imputable to HA-CMC barrier.

Conclusions

For the most part, our results support the lack of tumor progression activation due to HA-CMC barrier. We conclude that the benefits gained from using HA-CMC barrier membrane during ovarian cancer surgeries seem to outweigh the potential oncological risks.

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Baiocchi G, Cestari LA, Macedo MP, Oliveira RAR, Fukazawa EM, Faloppa CC, Kumagai LY, Badiglian-Filho L, Menezes ANO, Cunha IW, Soares FA: Surgical implications of mesenteric lymph node metastasis from advanced ovarian cancer after bowel Resection. J Surg Oncol 2011, 104: 250–254. 10.1002/jso.21940CrossRefPubMed

Chéreau E, Ballester M, Rouzier R, Coutant C, Daraï E: Advanced ovarian cancer: criteria of resectability. Bull Cancer 2009, 96: 1189–1197.PubMed

Gladieff L, Chatelut E, Dalenc F, Ferron G: Pharmacological bases of intraperitoneal chemotherapy. Bull Cancer 2009, 96: 1235–1242.PubMed

Ward BC, Panitch A: Abdominal adhesions: current and novel therapies. J Surg Res 2011, 165: 91–111. 10.1016/j.jss.2009.09.015CrossRefPubMed

Oikonomakis I, Wexner SD, Gervaz P, You S-Y, Secic M, Giamundo P: Seprafilm: a retrospective preliminary evaluation of the impact on short-term oncologic outcome in colorectal cancer. Dis Colon Rectum 2002, 45: 1376–1380. 10.1007/s10350-004-6428-1CrossRefPubMed

Kusunoki M, Ikeuchi H, Yanagi H, Noda M, Tonouchi H, Mohri Y, Uchida K, Inoue Y, Kobayashi M, Miki C, Yamamura T: Bioresorbable hyaluronate-carboxymethylcellulose membrane (Seprafilm) in surgery for rectal carcinoma: a prospective randomized clinical trial. Surg Today 2005, 35: 940–945. 10.1007/s00595-005-3061-0CrossRefPubMed

Diamond MP, Burns EL, Accomando B, Mian S, Holmdahl L: Seprafilm® adhesion barrier: (1) a review of preclinical, animal, and human investigational studies. Gynecol Surg 2012, 9: 237–245. 10.1007/s10397-012-0741-9PubMedCentralCrossRefPubMed

Hubbard SC, Burns JW: Effects of a hyaluronan-based membrane (Seprafilm) on intraperitoneally disseminated human colon cancer cell growth in a nude mouse model. Dis Colon Rectum 2002, 45: 334–341. discussion 341–344 10.1007/s10350-004-6178-0CrossRefPubMed

Tan B, Wang JH, Wu QD, Kirwan WO, Redmond HP: Sodium hyaluronate enhances colorectal tumour cell metastatic potential in vitro and in vivo. Br J Surg 2001, 88: 246–250. 10.1046/j.1365-2168.2001.01664.xCrossRefPubMed

10.

Nedvetzki S, Gonen E, Assayag N, Reich R, Williams RO, Thurmond RL, Huang J-F, Neudecker BA, Wang F-S, Wang F-S, Turley EA, Naor D: RHAMM, a receptor for hyaluronan-mediated motility, compensates for CD44 in inflamed CD44-knockout mice: a different interpretation of redundancy. Proc Natl Acad Sci U S A 2004, 101: 18081–18086. 10.1073/pnas.0407378102PubMedCentralCrossRefPubMed

11.

Ricciardelli C, Rodgers RJ: Extracellular matrix of ovarian tumors. Semin Reprod Med 2006, 24: 270–282. 10.1055/s-2006-948556CrossRefPubMed

12.

Hiltunen EL, Anttila M, Kultti A, Ropponen K, Penttinen J, Yliskoski M, Kuronen AT, Juhola M, Tammi R, Tammi M, Kosma VM: Elevated hyaluronan concentration without hyaluronidase activation in malignant epithelial ovarian tumors. Cancer Res 2002, 62: 6410–6413.PubMed

13.

Anttila MA, Tammi RH, Tammi MI, Syrjänen KJ, Saarikoski SV, Kosma VM: High levels of stromal hyaluronan predict poor disease outcome in epithelial ovarian cancer. Cancer Res 2000, 60: 150–155.PubMed

14.

Yabushita H, Noguchi M, Kishida T, Fusano K, Noguchi Y, Itano N, Kimata K, Noguchi M: Hyaluronan synthase expression in ovarian cancer. Oncol Rep 2004, 12: 739–743.PubMed

15.

Kayastha S, Freedman AN, Piver MS, Mukkamalla J, Romero-Guittierez M, Werness BA: Expression of the hyaluronan receptor, CD44S, in epithelial ovarian cancer is an independent predictor of survival. Clin Cancer Res 1999, 5: 1073–1076.PubMed

16.

Cannistra SA, Kansas GS, Niloff J, DeFranzo B, Kim Y, Ottensmeier C: Binding of ovarian cancer cells to peritoneal mesothelium in vitro is partly mediated by CD44H. Cancer Res 1993, 53: 3830–3838.PubMed

17.

Jones LM, Gardner MJ, Catterall JB, Turner GA: Hyaluronic acid secreted by mesothelial cells: a natural barrier to ovarian cancer cell adhesion. Clin Exp Metastasis 1995, 13: 373–380.CrossRefPubMed

18.

Gardner MJ, Catterall JB, Jones LM, Turner GA: Human ovarian tumour cells can bind hyaluronic acid via membrane CD44: a possible step in peritoneal metastasis. Clin Exp Metastasis 1996, 14: 325–334. 10.1007/BF00123391CrossRefPubMed

19.

Li C-Z, Liu B, Wen Z-Q, Li H-Y: Inhibition of CD44 expression by small interfering RNA to suppress the growth and metastasis of ovarian cancer cells in vitro and in vivo. Folia Biol (Praha) 2008, 54: 180–186.

20.

Carpenter PM, Dao AV: The role of hyaluronan in mesothelium-induced motility of ovarian carcinoma cells. Anticancer Res 2003, 23: 3985–3990.PubMed

21.

Bourguignon LY, Zhu H, Shao L, Chen YW: CD44 interaction with c-Src kinase promotes cortactin-mediated cytoskeleton function and hyaluronic acid-dependent ovarian tumor cell migration. J Biol Chem 2001, 276: 7327–7336. 10.1074/jbc.M006498200CrossRefPubMed

22.

Bourguignon LY, Peyrollier K, Gilad E, Brightman A: Hyaluronan-CD44 interaction with neural Wiskott-Aldrich syndrome protein (N-WASP) promotes actin polymerization and ErbB2 activation leading to beta-catenin nuclear translocation, transcriptional up-regulation, and cell migration in ovarian tumor cells. J Biol Chem 2007, 282: 1265–1280. 10.1074/jbc.M604672200CrossRefPubMed

23.

Bashir S, Ananth CV, Lewin SN, Burke WM, Lu Y-S, Neugut AI, Herzog TJ, Hershman DL, Wright JD: Utilization and safety of sodium hyaluronate-carboxymethylcellulose adhesion barrier. Dis Colon Rectum 2013, 56: 1174–1184. 10.1097/DCR.0b013e31829ec889CrossRefPubMed

24.

Bae DS, Woo J-W, Paek SH, Kwon H, Chai YJ, Kim S-J, Choi JY, Lee KE, Youn Y-K: Antiadhesive effect and safety of sodium hyaluronate-carboxymethyl cellulose membrane in thyroid surgery. J Korean Surg Soc 2013, 85: 199–204. 10.4174/jkss.2013.85.5.199PubMedCentralCrossRefPubMed

25.

Leitao MM Jr, Byrum GV 3rd, Abu-Rustum NR, Brown CL, Chi DS, Sonoda Y, Levine DA, Gardner GJ, Barakat RR: Postoperative intra-abdominal collections using a sodium hyaluronate-carboxymethylcellulose (HA-CMC) barrier at the time of laparotomy for uterine or cervical cancers. Gynecol Oncol 2010, 119: 208–211. 10.1016/j.ygyno.2010.07.027CrossRefPubMed

26.

Tabata T, Kihira T, Shiozaki T, Tanida K, Kondo E, Nagao K, Okugawa T, Sagawa N: Efficacy of a sodium hyaluronate-carboxycellulose membrane (seprafilm) for reducing the risk of early postoperative small bowel obstruction in patients with gynecologic malignancies. Int J Gynecol Cancer 2010, 20: 188–193. 10.1111/IGC.0b013e3181c7fe84CrossRefPubMed

27.

Tan A, Argenta P, Ramirez R, Bliss R, Geller M: The use of sodium hyaluronate-carboxymethylcellulose (HA-CMC) barrier in gynecologic malignancies: a retrospective review of outcomes. Ann Surg Oncol 2009, 16: 499–505. 10.1245/s10434-008-0235-1CrossRefPubMed

28.

Bristow RE, Montz FJ: Prevention of adhesion formation after radical oophorectomy using a sodium hyaluronate-carboxymethylcellulose (HA-CMC) barrier. Gynecol Oncol 2005, 99: 301–308. 10.1016/j.ygyno.2005.06.057CrossRefPubMed

29.

Bristow RE, Santillan A, Diaz-Montes TP, Gardner GJ, Giuntoli RL 2nd, Peeler ST: Prevention of adhesion formation after radical hysterectomy using a sodium hyaluronate-carboxymethylcellulose (HA-CMC) barrier: a cost-effectiveness analysis. Gynecol Oncol 2007, 104: 739–746. 10.1016/j.ygyno.2006.09.029CrossRefPubMed

30.

Krill LS, Ueda SM, Gerardi M, Bristow RE: Analysis of postoperative complications associated with the use of anti-adhesion sodium hyaluronate-carboxymethylcellulose (HA-CMC) barrier after cytoreductive surgery for ovarian, fallopian tube and peritoneal cancers. Gynecol Oncol 2011, 120: 220–223. 10.1016/j.ygyno.2010.10.037CrossRefPubMed

31.

Bourdel N, Matsuzaki S, Bazin J-E, Darcha C, Pouly J-L, Mage G, Canis M: Postoperative peritoneal dissemination of ovarian cancer cells is not promoted by carbon-dioxide pneumoperitoneum at low intraperitoneal pressure in a syngenic mouse laparoscopic model with controlled respiratory support: a pilot study. J Minim Invasive Gynecol 2008, 15: 321–326. 10.1016/j.jmig.2008.02.004CrossRefPubMed

32.

Sasaki T, Shimura H, Tanaka T, Nakashima K, Matsuo K, Ikeda S: Protection of trocar sites from gallbladder cancer implantation by sodium hyaluronate carboxymethylcellulose-based bioresorbable membrane (Seprafilm) in a murine model [corrected]. Surg Endosc 2004, 18: 246–251. 10.1007/s00464-003-8128-7CrossRefPubMed

33.

Pucciarelli S, Codello L, Rosato A, Del Bianco P, Vecchiato G, Lise M: Effect of antiadhesive agents on peritoneal carcinomatosis in an experimental model. Br J Surg 2003, 90: 66–71. 10.1002/bjs.4006CrossRefPubMed

34.

Misra S, Heldin P, Hascall VC, Karamanos NK, Skandalis SS, Markwald RR, Ghatak S: Hyaluronan-CD44 interactions as potential targets for cancer therapy. FEBS J 2011, 278: 1429–1443. 10.1111/j.1742-4658.2011.08071.xPubMedCentralCrossRefPubMed

35.

Ween MP, Hummitzsch K, Rodgers RJ, Oehler MK, Ricciardelli C: Versican induces a pro-metastatic ovarian cancer cell behavior which can be inhibited by small hyaluronan oligosaccharides. Clin Exp Metastasis 2011, 28: 113–125. 10.1007/s10585-010-9363-7CrossRefPubMed

36.

Kouvidi K, Berdiaki A, Nikitovic D, Katonis P, Afratis N, Hascall VC, Karamanos NK, Tzanakakis GN: Role of receptor for hyaluronic acid-mediated motility (RHAMM) in low molecular weight hyaluronan (LMWHA)-mediated fibrosarcoma cell adhesion. J Biol Chem 2011, 286: 38509–38520. 10.1074/jbc.M111.275875PubMedCentralCrossRefPubMed

37.

Mizrahy S, Raz SR, Hasgaard M, Liu H, Soffer-Tsur N, Cohen K, Dvash R, Landsman-Milo D, Bremer MGEG, Moghimi SM, Peer D: Hyaluronan-coated nanoparticles: the influence of the molecular weight on CD44-hyaluronan interactions and on the immune response. J Control Release 2011, 156: 231–238. 10.1016/j.jconrel.2011.06.031CrossRefPubMed

38.

Thibault B, Castells M, Delord J-P, Couderc B: Ovarian cancer microenvironment: implications for cancer dissemination and chemoresistance acquisition. Cancer Metastasis Rev 2013. doi:10.1007/s10555–013–9456–2.

Title: Evaluation of the effects of hyaluronic acid-carboxymethyl cellulose barrier on ovarian tumor progression
Authors: Laetitia Picaud
Benoît Thibault
Eliane Mery
Monia Ouali
Alejandra Martinez
Jean-Pierre Delord
Bettina Couderc
Gwenael Ferron
Publication date: 01-12-2014
Publisher: BioMed Central
Published in: Journal of Ovarian Research / Issue 1/2014
Electronic ISSN: 1757-2215
DOI: https://doi.org/10.1186/1757-2215-7-40

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Evaluation of the effects of hyaluronic acid-carboxymethyl cellulose barrier on ovarian tumor progression

Abstract

Background

Methods

Results

Conclusions

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

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