Effect of carbon dioxide pneumoperitoneum and wound closure technique on port site tumor implantation in a rat model

  • J. M. Burns
  • B. D. Matthews
  • H. S. Pollinger
  • G. Mostafa
  • C. S. Joels
  • C. E. Austin
  • K. W. Kercher
  • H. J. Norton
  • B. T. Heniford
Original article



The purpose of this study was to evaluate the effects of carbon dioxide (CO2) pneumoperitoneum and wound closure technique on port site tumor implantation.


A standard quantity of rat mammary adenocarcinoma (SMT2A)was allowed to grow in a flank incision in Wistar-Furth rats (n = 90) for 14 days. Thereafter, 1-cm incisions were made in each animal in three quadrants. There were six control animals. The experimental animals were divided into a 60-min CO2 pneumoperitoneum group (n = 42) and a no pneumoperitoneum (n = 42) group. The flank tumor was lacerated transabdominally in the experimental groups. The three wound sites were randomized to closure of (a) skin; (b) skin and fascia; and (c) skin, fascia, and peritoneum. The abdominal wounds were harvested en bloc on postoperative day 7.


Histologic comparison of the port sites in the pneumoperitoneum and no-pneumoperitoneum groups did not demonstrate a statistically significant difference in tumor implantation for any of the closure methods. Evaluation of the closure techniques showed no statistical difference between the pneumoperitoneum group and the no-pneumoperitoneum group in the incidence of port site tumor implantation. Within the no-pneumoperitoneum group, there was a significant increase (p = 0.03) in tumor implantation with skin closure alone vs all three layers. Additionally, when we compared all groups by closure technique, the rate of tumor implantation was found to be significantly higher (p = 0.01) for skin closure alone vs closure of all three layers.


This study suggests that closure technique may influence the rate of port site tumor implantation. The use of a CO2 pneumoperitoneum did not alter the incidence of port site tumor implantation at 7 days postoperatively.


Port site metastasis Laparoscopy Tumor biology Pneumoperitoneum Carbon dioxide insufflation Cancer 


  1. 1.
    Agostini, A, Robin, F, Jais, JP, Aggerbeck, F, Vild, B, Blanc, F, Curu, L 2002Peritoneal closure reduces port site metastasesSurg Endosc16289291CrossRefPubMedGoogle Scholar
  2. 2.
    Allendorf, JD, Bessler, M, Kayton, ML, Oesterling, SD, Treat, MR, Nowygrod, R, Whelan, RL 1995Increased rumor establishment and growth after laparotomy vs. laparoscopy in a murine modelArch Surg130649653PubMedGoogle Scholar
  3. 3.
    Allendorf, JD, Bessler, M, Whelan, RL, Trokel, M, Laird, DA, Terry, MB, Treat, MR 1996Better preservation of immune function after laparoscopic-assisted vs. open bowel resection in a murine modelDis Colon Rectum39S67S72PubMedGoogle Scholar
  4. 4.
    Aoki, Y, Shimura, H, Li, H, Mizumoto, K, Date, K, Tanaka, M 1999A model of port-site metastases of gall bladder cancer: the influence of peritoneal injury and its repair on abdominal wall metastasesSurgery125553559CrossRefPubMedGoogle Scholar
  5. 5.
    Baker, DG, Masterson, TM, Pace, R, Constable, WC, Wanebo, H 1989The influence of the surgical wound on local tumor recurrenceSurg106525532Google Scholar
  6. 6.
    Bali, JE, Franklin, JA, Almeida, JA, Glass, JL, Diaz, JA, Reymond, M 2000How to prevent port site metastases in laparoscopic colorectal surgerySurg Endosc1410341036CrossRefPubMedGoogle Scholar
  7. 7.
    Berends, FJ, Kazemier, G, Bonjer, HJ, Lange, JF 1994Subcutaneous metastases after laparoscopic colectomyLancet34458CrossRefGoogle Scholar
  8. 8.
    Bouvy, ND, Marquet, RL, Jeekel, H, Bonjer, HJ 1996Impact of gas(less) laparoscopy and laparotomy on peritoneal tumor growth and abdominal wall metastasesAnn Surg224694700CrossRefPubMedGoogle Scholar
  9. 9.
    Brundell, SM, Tucker, K, Texler, M, Brown, B, Chatterton, B, Hewett, PJ 2002Variables in the spread of tumor cells to trocars and port sites during operative laparoscopySurgEndosc1614131419Google Scholar
  10. 10.
    Cass, AW, Million, RR, Pfaff, WW 1976Patterns of recurrence following surgery alone for adenocarcinoma of the colon and rectumCancer3728612865PubMedGoogle Scholar
  11. 11.
    Cirocco, WC, Schwartzmann, A, Golub, RW 1994Abdominal recurrence after laparoscopic colectomy for colon cancerSurg116842846Google Scholar
  12. 12.
    Clinical Outcome of Surgical Therapy Study Group2004A comparison of laparoscopically assisted and open colectomy for colon cancerN Engl J Med35020502059Google Scholar
  13. 13.
    Collet, D, Vitale, GC, Reynolds, M, Klar, E, Cheadle, WG 1995Peritoneal host defenses are less impaired by laparoscopy than by open operationSurg Endosc910591064PubMedGoogle Scholar
  14. 14.
    Committee on Care and Use of Laboratory Animals19XXGuide for the care and use of laboratory animalsUS Department of Health and Human Services. Public Health Services. National Institutes of HealthBethesda (MD), 20892, August 7, 2002Google Scholar
  15. 15.
    Curet, MJ, Putrakul, K, Pitcher, DE, Josloff, RK, Zucker, KA 2000Laparoscopically assisted colon resection for colon carcinoma: perioperative results and long-term outcomeSurg Endosc1410621066CrossRefPubMedGoogle Scholar
  16. 16.
    Ghosh, SK, Grassberg, AL, Kim, U 1979A tumor associated organ specific antigen characteristic of spontaneously metastatic rat mammary carcinomasJ Natl Cancer Inst6212291233PubMedGoogle Scholar
  17. 17.
    Goldstein, DS, Lu, ML, Hattori, T, Ratliff, TL, Loughlin, KR, Kavoussi, LR 1993Inhibition of peritoneal tumor-cell implantation: model for laparoscopic cancer surgeryJ Endourol7237241PubMedGoogle Scholar
  18. 18.
    Greene, FL 1995Principles of cancer biology in relation to minimal access surgical techniquesSemin Laparosc Surg2155157PubMedGoogle Scholar
  19. 19.
    Haji, A, Mutter, D, Wack, S, Bastien, C, Gury, JF, Marescaux, J, Aprahamian, M 2000Dual effect of laparoscopy on cell-mediated immunityEur Surg Res32261266CrossRefPubMedGoogle Scholar
  20. 20.
    Hewett, PJ, Thomas, WM, King, G, Eaton, M 1996Intraperitoneal cell movement during abdominal carbon dioxide insufflation and laparoscopy: an in vivo modelDis Colon Rectum39S62S66PubMedGoogle Scholar
  21. 21.
    Hofer, SOP, Shrayer, D, Reichner, JS, Hoekstra, HJ, Wanebo, HJ 1998Wound-induced tumor progression: a probable role in recurrence after tumor resectionArch Surg133383389PubMedGoogle Scholar
  22. 22.
    Hughes, ES, McDermott, FT, Polglase, AL, Johnson, WR 1983Tumor recurrence in the abdominal wall scar tissue after large-bowel cancer surgeryDis Colon Rectum26571572PubMedGoogle Scholar
  23. 23.
    Ishida, H, Murata, N, Yamada, T, Shimomura, K 2000Influence of trocar placement and CO2 pneumoperitoneum on port site metastasis following laparoscopic tumor surgerySurg Endosc14193197CrossRefPubMedGoogle Scholar
  24. 24.
    Jacobi, CA, Ordemann, J, Bohm, B, Zieren, HU, Sabat, R, Muller, JM 1997Inhibition of peritoneal tumor cell growth and implantation in laparoscopic surgery in a rat modelAm J Surg174359363CrossRefPubMedGoogle Scholar
  25. 25.
    Joels, CS, Mostafa, G, Matthews, BD, Kercher, KW, Sing, RF, Norton, HJ, Heniford, BT 2003Factors affecting intravenous analgesic requirements after colectomyJ Am Coll Surg197780785CrossRefPubMedGoogle Scholar
  26. 26.
    Johnstone, P, Rohde, D, Swartz, S, Fetter, JE, Wexner, SD 1996Port site recurrences after laparoscopic and thoracoscopic procedures in malignancyJ Clin Oncol1419501956PubMedGoogle Scholar
  27. 27.
    Jones, DB, Quo, LW, Reinhard, MK, Soper, NJ, Philpott, GW, Connett, J, Fleshman, JW 1995Impact of pneumoperitoneum on trocar site implantation of colon cancer in hamster modelDis Colon Rectum3811821188PubMedGoogle Scholar
  28. 28.
    Kim, ZG, Mehl, C, Lorenz, M, Gutt, CN 2002Impact of laparoscopic CO2 insufflation on rumor-associated molecules in cultured colorectal cancer cellsSurg Endosc1611821186CrossRefPubMedGoogle Scholar
  29. 29.
    Lacy, AM, Garcia-Valdecasas, JC, Salvadora, D, Castells, A, Taura, P, Pique, JM, Visa, J 2002Laparoscopy-assisted colectomy versus open colectomy for treatment of non-metastatic colon cancer: a randomized trialLancet35922242229PubMedGoogle Scholar
  30. 30.
    Lecuru, F, Agostini, A, Camatte, S, Robin, F, Aggerbeck, M, Jais, JP, Vilde, F,  et al. 2002Impact of pnuemoperitoneum on tumor growthSurg Endosc1611701174CrossRefPubMedGoogle Scholar
  31. 31.
    Liu, C, McFadden, D 2000Laparoscopic port sites do not require fascial closure when non-bladed trocars are usedAm Surg66853854PubMedGoogle Scholar
  32. 32.
    Lujan, HJ, Gustavo, P, Jacobs, M, Viamonte, M, Hartmann, R 2002Long-term survival after laparoscopic colon resection for cancerDis Colon Rectum45491501CrossRefPubMedGoogle Scholar
  33. 33.
    Mathew, G, Watson, KI, Rofe, AM, Baigrie, CF, Ellis, T, Jamieson, GG 1997Adverse impact of pneumoperitoneum on intraperitoneal implantation and growth of tumour cell suspension in an experimental modelAust N Z J Surg61289292Google Scholar
  34. 34.
    Nduka, CC, Monson, JRT, Menzies-Gow, N, Darzi, A 1994Abdominal wall metastases following laparoscopyBr J Surg81648652PubMedGoogle Scholar
  35. 35.
    Nelson, H, Petrelli, N, Carlin, A, Couture, J, Fleshman, J, Guillem, J, Miedema, B,  et al. 2001Guidelines 2000 colon and rectal cancer surgeryJ Natl Cancer Inst93583596PubMedGoogle Scholar
  36. 36.
    Neuhaus, SJ, Ellis, T, Rofe, AM, Pike, GK, Jamieson, GG, Watson, DI 1998Tumor implantation following laparoscopy using different insufflation gasesSurg Endosc1213001302CrossRefPubMedGoogle Scholar
  37. 37.
    Neuhaus, SJ, Texler, M, Hewett, PJ, Watson, DI 1998Port-site metastases following laparoscopic surgeryBr J Surg85735741CrossRefPubMedGoogle Scholar
  38. 38.
    Neuhaus, SJ, Watson, DI, Ellis, T, Dodd, T, Rofe, AM, Jamieson, GG 1998Efficacy of cytotoxic agents for the prevention of port site metastasesArch Surg133762766CrossRefPubMedGoogle Scholar
  39. 39.
    Neuhaus, SJ, Ellis, T, Jamieson, GG, Watson, DI 1999Experimental study of the effect of intraperitoneal heparin on tumour implantation following laparoscopyBr J Surg86400404CrossRefPubMedGoogle Scholar
  40. 40.
    Neuhaus, SJ, Watson, DI, Ellis, T, Rofe, AM, Jamieson, GG 1999Influence of cytotoxic agents on intraperitoneal tumor implantation after laparoscopyDis Colon Rectum421015PubMedGoogle Scholar
  41. 41.
    Neuhaus, SJ, Watson, KI, Ellis, T, Rofe, AM, Jamieson, GG 2000The effect of immune enhancement and suppression on the development of laparoscopic port site metastasesSurg Endosc14439443CrossRefPubMedGoogle Scholar
  42. 42.
    Niedbala, MJ, Crickard, K, Bernacki, RJ 1985Interactions of human ovarian tumor cells with human mesothelial cells grown on extracellular matrix: an in vivo model system for studying tumor cell adhesion and invasionExp Cell Res160449513CrossRefPubMedGoogle Scholar
  43. 43.
    Ordemann, J, Jacobi, CA, Schwenk, W, Stosslein, R, Muller, JM 2001Cellular and humoral inflammatory response after laparoscopic and conventional colorectal resectionsSurg Endosc15600608CrossRefPubMedGoogle Scholar
  44. 44.
    Reilly, WT, Nelson, H, Schroeder, G, Wieand, HS, Bolton, J, O’Connell, MJ 1996Wound recurrence following conventional treatment of colorectal cancerDis Colon Rectum39200207PubMedGoogle Scholar
  45. 45.
    Reymond, MA, Schneider, C, Kastl, S, Hohenberger, W, Kockerling, FJ 1998The pathogenesis of port-site recurrencesGastrointest Surg5406414CrossRefGoogle Scholar
  46. 46.
    Rudland, PS, Dunnington, DJ, Kim, U 1989Isolation and properties of cell lines from metastatic rat mammary carcinoma SMT2ABr J Cancer59854864PubMedGoogle Scholar
  47. 47.
    Schiavon, CA, Pollara, WM, Bevilacqua, RG, Younes, RN, Vieira da Motta, TB, Cohen, RV, Itinoshe, M,  et al. 1999Prevention of neoplastic port site implants in laparoscopy: an experimental studySurg Laparosc Endosc Percutan Tech9274278CrossRefPubMedGoogle Scholar
  48. 48.
    Siestses, C, Wiezer, MJ, Eijsbouts, QAJ, Leeuwen, PAM, Beelen, RHJ, Meijer, S, Cuesta, MA 2000The influence of laparoscopic surgery on postoperative polymorphonuclear leukocyte functionSurg Endosc14812816CrossRefPubMedGoogle Scholar
  49. 49.
    Volz, J, Koster, S, Weiss, M, Schmidt, R, Urbaschek, R, Melchert, F, Albrecht, M 1996Pathophysiologic features of a pneumoperitoneum at laparoscopy: a swine modelAm J Obstet Gynecol174132140PubMedGoogle Scholar
  50. 50.
    Vukasin, P, Ortega, AE, Greene, FL, Steele, GD, Simons, AJ, Anthoné, GJ, Weston, LA,  et al. 1996Wound recurrence following laparoscopic colon cancer resection: results of the American Society of Colon and Rectal Surgeons Laparoscopic RegistryDis Colon Rectum39S20S23PubMedGoogle Scholar
  51. 51.
    Watson, DI, Mathew, G, Ellis, T, Baigrie, CF, Rofe, AM, Jamieson, GG 1997Gasless laparoscopy may reduce the risk of port-site metastases following laparoscopic tumor surgeryArch Surg132166168PubMedGoogle Scholar
  52. 52.
    Watson, RW, Redomond, HP, McCarthy, J, Burke, PE, Bouchier-Hayes, D 1995Exposure of the peritoneal cavity to air regulates early inflammatory responses to surgery in a murine modelBr J Surg8210601065PubMedGoogle Scholar
  53. 53.
    West, MA, Hackam, DJ, Baker, J, Rodriguez, JL, Bellingham, J, Rotstein, OD 1997Mechanism of decreased in vitro murine macrophage cytokine release after exposure to carbon dioxide: relevance to laparoscopic surgeryAnn Surg226179190CrossRefPubMedGoogle Scholar
  54. 54.
    Wilkinson, NW, Shapiro, AJ, Harvey, SB, Stack, RS, Cornum, RL 2001Port-site recurrence reproduced in the VX-2 rabbit carcinoma model: an in vivo model comparing laparoscopic port sites and open incisionsJSLS5221226PubMedGoogle Scholar
  55. 55.
    Wu, J, Guo, LW, Ruiz, M, Pfister, SM, Connett, JM, Ficshman, JW 1998Excision of trocar sites reduces tumor implantation in an animal modelDis Colon Rectum4111071111PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2005

Authors and Affiliations

  • J. M. Burns
    • 1
  • B. D. Matthews
    • 2
  • H. S. Pollinger
    • 1
  • G. Mostafa
    • 1
  • C. S. Joels
    • 1
  • C. E. Austin
    • 1
  • K. W. Kercher
    • 1
  • H. J. Norton
    • 1
  • B. T. Heniford
    • 1
  1. 1.Department of General SurgeryJames G. Cannon Research Center, Carolinas Medical CenterCharlotteUSA
  2. 2.Department of Surgery, Washington UniversitySt. Louis

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