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Journal of Ovarian Research
Published in: Journal of Ovarian Research 1/2018

Open Access 01-12-2018 | Research

Wounding promotes ovarian cancer progression and decreases efficacy of cisplatin in a syngeneic mouse model

Authors: Yooyoung Lee, Alexandra Kollara, Taymaa May, Theodore J. Brown

Published in: Journal of Ovarian Research | Issue 1/2018

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Abstract

Background

Primary cytoreductive surgery followed by adjuvant chemotherapy is the standard treatment for advanced epithelial ovarian cancer. The average interval between surgery and chemotherapy initiation is approximately 4-weeks at most centers; however, since surgery may accelerate residual tumor growth, a shorter interval may be more beneficial.

Methods

The murine ID8 cell model of ovarian cancer was used to examine the efficacy of cisplatin treatment administered perioperatively or 7 days after surgical wounding. Luciferase-expressing cells ID8 cells were injected intraperitoneally (i.p.) into female C57/Bl6 mice. Fourteen days post-injection, animals received an abdominal incision or anesthesia alone and received i.p. cisplatin either on the surgical day or 7 days later, or received no chemotherapy. Additional animals received cisplatin 28 days after wounding for comparison.

Results

Abdominal tumor mass increased 2.5-fold in wounded vs. unwounded animals as determined by bioluminescent in vivo tumor imaging. Cisplatin administered on the day of wounding decreased tumor burden by 50%, as compared to 90% in unwounded animals. Cisplatin on day 7 or day 28 decreased tumor burden by 80 and 37% respectively.

Conclusions

Surgical wounding increases ovarian tumor mass and decreases perioperative cisplatin efficacy in this animal model. Administration of cisplatin 1 week after surgery was more effective than cisplatin administered perioperatively or 4 weeks after surgery.

Literature
  1. Baldwin LA, Huang B, Miller RW, Tucker T, Goodrich ST, Podzielinski I, DeSimone CP, Ueland FR, van Nagell JR, Seamon LG. Ten-year relative survival for epithelial ovarian cancer. Obstet Gynecol. 2012;120(3):612–8.View ArticlePubMed
  2. Coleman RL, Monk BJ, Sood AK, Herzog TJ. Latest research and treatment of advanced-stage epithelial ovarian cancer. Nat Rev Clin Oncol. 2013;10(4):211–24.View ArticlePubMedPubMed Central
  3. Chi DS, Eisenhauer EL, Lang J, Huh J, Haddad L, Abu-Rustum NR, Sonoda Y, Levine DA, Hensley M, Barakat RR. What is the optimal goal of primary cytoreductive surgery for bulky stage IIIC epithelial ovarian carcinoma (EOC)? Gynecol Oncol. 2006;103(2):559–64.View ArticlePubMed
  4. Al Rawahi T, Lopes AD, Bristow RE, Bryant A, Elattar A, Chattopadhyay S, Galaal K. Surgical cytoreduction for recurrent epithelial ovarian cancer. Cochrane Database Syst Rev. 2013;2:CD008765.
  5. Tewari KS, Java JJ, Eskander RN, Monk BJ, Burger RA. Early initiation of chemotherapy following complete resection of advanced ovarian cancer associated with improved survival: NRG oncology/gynecologic oncology group study. Ann Oncol. 2016;27(1):114–21.View ArticlePubMed
  6. Ceelen W, Pattyn P, Mareel M. Surgery, wound healing, and metastasis: recent insights and clinical implications. Crit Rev Oncol Hematol. 2014;89(1):16–26.View ArticlePubMed
  7. Demicheli R, Retsky MW, Hrushesky WJ, Baum M, Gukas ID. The effects of surgery on tumor growth: a century of investigations. Ann Oncol. 2008;19(11):1821–8.View ArticlePubMed
  8. Lange PH, Hekmat K, Bosl G, Kennedy BJ, Fraley EE. Acclerated growth of testicular cancer after cytoreductive surgery. Cancer. 1980;45(6):1498–506.View ArticlePubMed
  9. Retsky M, Demicheli R, Hrushesky W, Baum M, Gukas I. Surgery triggers outgrowth of latent distant disease in breast cancer: an inconvenient truth? Cancers (Basel). 2010;2(2):305–37.View Article
  10. Tyzzer EE. Factors in the production and growth of tumor metastases. J Med Res. 1913;28(2):309–32. 301PubMedPubMed Central
  11. Simpson-Herren L, Sanford AH, Holmquist JP. Effects of surgery on the cell kinetics of residual tumor. Cancer Treat Rep. 1976;60(12):1749–60.PubMed
  12. Gadducci A, Sartori E, Landoni F, Zola P, Maggino T, Maggioni A, Cosio S, Frassi E, LaPresa MT, Fuso L, et al. Relationship between time interval from primary surgery to the start of taxane- plus platinum-based chemotherapy and clinical outcome of patients with advanced epithelial ovarian cancer: results of a multicenter retrospective Italian study. J Clin Oncol. 2005;23(4):751–8.View ArticlePubMed
  13. Biagi JJ, Raphael MJ, Mackillop WJ, Kong W, King WD, Booth CM. Association between time to initiation of adjuvant chemotherapy and survival in colorectal cancer: a systematic review and meta-analysis. JAMA. 2011;305(22):2335–42.View ArticlePubMed
  14. Fisher B, Gunduz N, Saffer EA. Influence of the interval between primary tumor removal and chemotherapy on kinetics and growth of metastases. Cancer Res. 1983;43(4):1488–92.PubMed
  15. Roby KF, Taylor CC, Sweetwood JP, Cheng Y, Pace JL, Tawfik O, Persons DL, Smith PG, Terranova PF. Development of a syngeneic mouse model for events related to ovarian cancer. Carcinogenesis. 2000;21(4):585–91.View ArticlePubMed
  16. Greenaway J, Moorehead R, Shaw P, Petrik J. Epithelial-stromal interaction increases cell proliferation, survival and tumorigenicity in a mouse model of human epithelial ovarian cancer. Gynecol Oncol. 2008;108(2):385–94.View ArticlePubMed
  17. Yusa K, Zhou L, Li MA, Bradley A, Craig NL. A hyperactive piggyBac transposase for mammalian applications. Proc Natl Acad Sci U S A. 2011;108(4):1531–6.View ArticlePubMedPubMed Central
  18. Mathe A, Komka K, Forczig M, Szabo D, Anderlik P, Rozgonyi F. The effect of different doses of cisplatin on the pharmacokinetic parameters of cefepime in mice. Lab Anim. 2006;40(3):296–300.View ArticlePubMed
  19. Hofstetter G, Concin N, Braicu I, Chekerov R, Sehouli J, Cadron I, Van Gorp T, Trillsch F, Mahner S, Ulmer H, et al. The time interval from surgery to start of chemotherapy significantly impacts prognosis in patients with advanced serous ovarian carcinoma - analysis of patient data in the prospective OVCAD study. Gynecol Oncol. 2013;131(1):15–20.View ArticlePubMed
  20. Bogden AE, Moreau JP, Eden PA. Proliferative response of human and animal tumours to surgical wounding of normal tissues: onset, duration and inhibition. Br J Cancer. 1997;75(7):1021–7.View ArticlePubMedPubMed Central
  21. Abramovitch R, Marikovsky M, Meir G, Neeman M. Stimulation of tumour growth by wound-derived growth factors. Br J Cancer. 1999;79(9–10):1392–8.View ArticlePubMedPubMed Central
  22. Ramolu L, Christ D, Abecassis J, Rodier JF. Stimulation of breast cancer cell lines by post-surgical drainage fluids. Anticancer Res. 2014;34(7):3489–92.PubMed
  23. Hofer SO, Shrayer D, Reichner JS, Hoekstra HJ, Wanebo HJ. Wound-induced tumor progression: a probable role in recurrence after tumor resection. Arch Surg. 1998;133(4):383–9.View ArticlePubMed
  24. Tagliabue E, Agresti R, Carcangiu ML, Ghirelli C, Morelli D, Campiglio M, Martel M, Giovanazzi R, Greco M, Balsari A, et al. Role of HER2 in wound-induced breast carcinoma proliferation. Lancet. 2003;362(9383):527–33.View ArticlePubMed
  25. Diegelmann RF, Evans MC. Wound healing: an overview of acute, fibrotic and delayed healing. Front Biosci. 2004;9:283–9.View ArticlePubMed
  26. Gunduz N, Fisher B, Saffer EA. Effect of surgical removal on the growth and kinetics of residual tumor. Cancer Res. 1979;39(10):3861–5.PubMed
  27. Fisher B, Gunduz N, Coyle J, Rudock C, Saffer E. Presence of a growth-stimulating factor in serum following primary tumor removal in mice. Cancer Res. 1989;49(8):1996–2001.PubMed
  28. Donaldson KL, Goolsby GL, Wahl AF. Cytotoxicity of the anticancer agents cisplatin and taxol during cell proliferation and the cell cycle. Int J Cancer. 1994;57(6):847–55.View ArticlePubMed
  29. Amin AT, Shiraishi N, Ninomiya S, Tajima M, Inomata M, Kitano S. Increased mRNA expression of epidermal growth factor receptor, human epidermal receptor, and survivin in human gastric cancer after the surgical stress of laparotomy versus carbon dioxide pneumoperitoneum in a murine model. Surg Endosc. 2010;24(6):1427–33.View ArticlePubMed
  30. Yan TD, Black D, Savady R, Sugarbaker PH. Systematic review on the efficacy of cytoreductive surgery combined with perioperative intraperitoneal chemotherapy for peritoneal carcinomatosis from colorectal carcinoma. J Clin Oncol. 2006;24(24):4011–9.View ArticlePubMed
  31. Lim MC, Chang S-J, Yoo HJ, Nam B-H, Bristow R, Park S-Y. Randomized trial of hyperthermic intraperitoneal chemotherapy (HIPEC) in women with primary advanced peritoneal, ovarian, and tubal cancer. J Clin Oncol. 2017;35(15 suppl) Abstr 5520
  32. van Driel WJ, Koole SN, Sikorska K, Schagen van Leeuwen JH, Schreuder HWR, Hermans RHM, de Hingh I, van der Velden J, Arts HJ, Massuger L et al. Hyperthermic intraperitoneal chemotherapy in ovarian Cancer. N Engl J Med 2018; 378(3):230–240.
  33. Curigliano G, Petit JY, Bertolini F, Colleoni M, Peruzzotti G, de Braud F, Gandini S, Giraldo A, Martella S, Orlando L, et al. Systemic effects of surgery: quantitative analysis of circulating basic fibroblast growth factor (bFGF), vascular endothelial growth factor (VEGF) and transforming growth factor beta (TGF-beta) in patients with breast cancer who underwent limited or extended surgery. Breast Cancer Res Treat. 2005;93(1):35–40.View ArticlePubMed
  34. Ikeda M, Furukawa H, Imamura H, Shimizu J, Ishida H, Masutani S, Tatsuta M, Kawasaki T, Satomi T. Surgery for gastric cancer increases plasma levels of vascular endothelial growth factor and von Willebrand factor. Gastric Cancer. 2002;5(3):137–41.View ArticlePubMed
  35. Maniwa Y, Okada M, Ishii N, Kiyooka K. Vascular endothelial growth factor increased by pulmonary surgery accelerates the growth of micrometastases in metastatic lung cancer. Chest. 1998;114(6):1668–75.View ArticlePubMed
  36. Baert T, Verschuere T, Van Hoylandt A, Gijsbers R, Vergote I, Coosemans A. The dark side of ID8-Luc2: pitfalls for luciferase tagged murine models for ovarian cancer. J Immunother Cancer. 2015;3:57.View ArticlePubMedPubMed Central
  37. Walton J, Blagih J, Ennis D, Leung E, Dowson S, Farquharson M, Tookman LA, Orange C, Athineos D, Mason S, et al. CRISPR/Cas9-mediated Trp53 and Brca2 knockout to generate improved murine models of ovarian high-grade serous carcinoma. Cancer Res. 2016;76(20):6118–29.View ArticlePubMedPubMed Central
  38. Tagliaferri P, Ventura M, Baudi F, Cucinotto I, Arbitrio M, Di Martino MT, Tassone P. BRCA1/2 genetic background-based therapeutic tailoring of human ovarian cancer: hope or reality? J Ovarian Res. 2009;2:14.View ArticlePubMedPubMed Central
  39. Tassone P, Di Martino MT, Ventura M, Pietragalla A, Cucinotto I, Calimeri T, Bulotta A, Neri P, Caraglia M, Tagliaferri P. Loss of BRCA1 function increases the antitumor activity of cisplatin against human breast cancer xenografts in vivo. Cancer Biol Ther. 2009;8(7):648–53.View ArticlePubMed
  40. Ansell DM, Campbell L, Thomason HA, Brass A, Hardman MJ. A statistical analysis of murine incisional and excisional acute wound models. Wound Repair Regen. 2014;22(2):281–7.View ArticlePubMedPubMed Central
  41. Perez R, Davis SC. Relevance of animal models for wound healing. Wounds. 2008;20(1):3–8.PubMed
  42. Kolb BA, Buller RE, Connor JP, DiSaia PJ, Berman ML. Effects of early postoperative chemotherapy on wound healing. Obstet Gynecol. 1992;79(6):988–92.PubMed
  43. Goodman MD, McPartland S, Detelich D, Saif MW. Chemotherapy for intraperitoneal use: a review of hyperthermic intraperitoneal chemotherapy and early post-operative intraperitoneal chemotherapy. J Gastrointest Oncol. 2016;7(1):45–57.PubMedPubMed Central
Metadata
Title
Wounding promotes ovarian cancer progression and decreases efficacy of cisplatin in a syngeneic mouse model
Authors
Yooyoung Lee
Alexandra Kollara
Taymaa May
Theodore J. Brown
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Journal of Ovarian Research / Issue 1/2018
Electronic ISSN: 1757-2215
DOI
https://doi.org/10.1186/s13048-018-0428-6

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