Skip to main content

Advertisement

SpringerLink
Log in

Experimental assessment of tumor growth and dissemination of a microscopic peritoneal carcinomatosis after CO2 peritoneal insufflation or laparotomy

Clinical and biological results of a randomized animal study

  • Original Articles
  • Published:
Surgical Endoscopy Aims and scope Submit manuscript

Abstract

Background

Based on clinical observations and previous animal studies, laparoscopic surgery for malignant disease is regarded as controversial. We used a rat model to measure and compare the tumor growth, proliferation, and dissemination of a microscopic peritoneal carcinomatosis after CO2 intraperitoneal insufflation or laparotomy.

Methods

Peritoneal carcinomatosis was induced in three groups of 27 BD IX rats each with intraperitoneal injections of 106 DHD/K12 cells, an aneuploid tumor cell line. At 48 h after tumor cell injection, the animals were randomly divided into three groups to undergo different types of intervention. All animals were anesthetized for 20 min (Halothane). The control group had no surgical intervention (group C), group I had CO2 insufflation (7 mmHg), and group L had a midline laparotomy (5-cm). Neither bowel manipulation nor any other traumatic action was performed. Two weeks later, the rats were killed and the incidence, type, and dissemination of carcinomatosis were evaluated. We also measured the tumor’s weight. Malignant omentum was sampled for flow cytometry analysis (DNA ploidy, S-phase fraction).

Results

The incidence of carcinomatosis did not differ among the groups. The mean score of macroscopic characteristics of the carcinomatosis was 2.8±1.9 in group L, 2.9 ±1.9 in group I, and 3±1.9 in group C (NS). The location of the implants did not differ, except for parietal peritoneum location, which was more frequent in group L (p<0.01). The tumor weight was 4.96±3.2 in group L, 5.55g±3.2 in group C, and 5.75g±3.4 in group I (NS). The percentage of aneuploid cells and S-phase fraction did not differ statistically among the groups.

Conclusion

These results indicate that CO2 insufflation does not cause more effects than laparotomy when tumors cells are present before the beginning of the surgery. Further studies are needed to determine the influence of other steps in laparoscopic surgery on tumor growth and dissemination.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Allendorf JD, Bessler M, Horvath KD, Marvin MR, Laird DA, Whelan RL (1999) Increased tumor establishment and growth after open vs laparoscopic surgery in mice may be related to differences in postoperative T-cell function. Surg Endosc 13: 233–235 DOI: 10.1007/s004649900952

    Article  PubMed  CAS  Google Scholar 

  2. Allendorf JD, Bessler M, Whelan RL, Trokel M, Laird DA, Terry MB, Treat MR (1997) Postoperative immune function varies inversely with the degree of surgical trauma in a murine model. Surg Endosc 11: 427–430 DOI: 10.1007/s004649900383

    Article  PubMed  CAS  Google Scholar 

  3. Aoki Y, Shimura H, Li H, Mizumoto K, Date K, Tanaka M (1999) A model of port-site metastases of gallbladder cancer: the influence of peritoneal injury and its repair on abdominal wall metastases. Surgery 125: 553–559

    PubMed  CAS  Google Scholar 

  4. Bauer KD, Bagwell CB, Giaretti W, Melamed M (1993) Consensus review of the clinical utility of DNA flow cytometry in colorectal cancer. Cytometry 14: 486–491

    Article  PubMed  CAS  Google Scholar 

  5. Berguer R, Cornelius T, Dalton M (1997) The optimum pneumoperitoneum pressure for laparoscopic surgery in the rat model: a detailed cardiorespiratory study. Surg Endosc 11: 915–918

    Article  PubMed  CAS  Google Scholar 

  6. Bouvy ND, Marquet RL, Jeekel J, Bonjer HJ (1997) Laparoscopic surgery is associated with less tumour growth stimulation than conventional surgery: an experimental study [see Comments]. Br J Surg 84: 358–361

    Article  PubMed  CAS  Google Scholar 

  7. Canis M, Botchorishvili R, Wattiez A, Mage G, Pouly JL, Bruhat MA (1998) Tumor growth and dissemination after laparotomy and CO2 pneumoperitoneum: a rat ovarian cancer model. Obstet Gynecol 92: 104–108

    Article  PubMed  CAS  Google Scholar 

  8. Chekan EG, Nataraj C, Clary EM, Hayward TZ, Brody FJ, Stamat JC, Fina MC (1999) Intraperitoneal immunity and pneumoperitoneum. Surg Endosc 13: 1135–1138 DOI: 10.1007/s004649901189

    Article  PubMed  CAS  Google Scholar 

  9. Chew DK, Borromeo JR, Kimmelstiel FM (1999) Feritoneal mucinous carcinomatosis after laparoscopic-assisted anterior resection for early rectal cancer: report of a case. Dis Colon Rectum 42: 424–426

    Article  PubMed  CAS  Google Scholar 

  10. Cohn DE, Tamimi HK, Goff BA (1997) Intraperitoneal spread of cervical carcinoma after laparoscopic lymphadenectomy. Obstet Gynecol 89: 864

    Article  PubMed  CAS  Google Scholar 

  11. Dorrance HR, Oien K, O’Dwyer PJ (1999) Effects of laparoscopy on intraperitoneal tumor growth and distant metastases in an animal model. Surgery 126: 35–40

    Article  PubMed  CAS  Google Scholar 

  12. Gutt CN, Schmandra TC (1999) Portal venous flow during CO2 pneumoperitoneum in the rat. Surg Endosc 13: 902–905 DOI: 10.1007/s004649901130

    Article  PubMed  CAS  Google Scholar 

  13. Hubens G, Pauwels M, Hubens A, Vermeulen P, Van Marck E, Eyskens E (1996) The influence of a penumoperitoneum on the peritoneal implantation of free intraperitoneal colon cancer cells. Surg Endosc 10: 809–812 DOI: 10.1007/s004649900166

    Article  PubMed  CAS  Google Scholar 

  14. Jacobi CA, Wenger FA, Ordemann J, Gutt C, Sabat R, Muller JM (1998) Experimental study of the effect of intra-abdominal pressure during laparoscopy on tumour growth and port site metastasis. Br J Surg 85: 1419–1422

    Article  PubMed  CAS  Google Scholar 

  15. Jacquet P, Sugarbaker PH (1995) Influence of wound healing on gastroinstestinal recurrence. Wounds 7: 40–47

    Google Scholar 

  16. Kruitwagen RF, Swinkels BM, Keyser KG, Doesburg WH, Schijf CP (1996) Incidence and effect on survival of abdominal wall metastases at trocar or puncture sites following laparoscopy or paracentesis in women with ovarian cancer [see Comments]. Gynecol Oncol 60: 233–237

    Article  PubMed  CAS  Google Scholar 

  17. Le Moine MC, Navarro F, Burgel JS, Pellegrin A, Khiari AR, Pourquier D, Fabre JM, Domergue J (1998) Experimental assessment of the risk of tumor recurrence after laparoscopic surgery. Surgery 123: 427–431

    Article  PubMed  Google Scholar 

  18. Lee SW, Southall JC, Allendorf JD, Bessler M, Whelan RL (1999) Tumor proliferative index is higher in mice undergoing laparotomy vs. CO2 pneumoperitoneum. Dis Colon Rectum 42: 477–481

    Article  PubMed  CAS  Google Scholar 

  19. Lee SW, Whelan RL, Southall JC, Bessler M (1999) Abdominal wound tumor recurrence after open and laparoscopic-assisted splenectomy in a murine model. Dis Colon Rectum 41: 824–831

    Article  Google Scholar 

  20. Little D, Regan M, Keane RM, Bouchier-Hayes D (1993) Perioperative immune modulation [see Comments]. Surgery 114: 87–91

    PubMed  CAS  Google Scholar 

  21. Mathew G, Watson DI, Ellis TS, Jamieson GG, Rofe AM (1999) The role of peritoneal immunity and the tumour-bearing state on the development of wound and peritoneal metastases after laparoscopy [see Comments]. Aust N Z J Surg 69: 14–18

    Article  PubMed  CAS  Google Scholar 

  22. Mathew G, Watson DI, Rofe AM, Ellis T, Jamieson GG (1997) Adverse impact of pneumoperitoneum on intraperitoneal implantation and growth of tumour cell suspension in an experimental model. Aust N Z J Surg 67: 289–292

    Article  PubMed  CAS  Google Scholar 

  23. Murata N, Ishida H, Nomura T, Yamada H, Idezuki Y (2000) The facilitation of peritoneal dissemination of a tumor by laparotomy in a rabbit model. Surg Today 30: 54–58

    Article  PubMed  CAS  Google Scholar 

  24. Mutter D, Hajri A, Tassetti V, Solis-Caxaj C, Aprahamian M, Marescaux J (1999) Increased tumor growth and spread after laparoscopy vs laparotomy: influence of tumor manipulation in a rat model. Surg Endosc 13: 365–370 DOI: 10.1007/s004649900991

    Article  PubMed  CAS  Google Scholar 

  25. Pauwels M, Lauwers P, Hendriks J, Hubens A, Eyskens E, Hubens G (1999) The effect of CO2 pneumoperitoneum on the growth of a solid colon carcinoma in rats. Surg Endosc 13: 998–1000 DOI: 10.1007/s004649901155

    Article  PubMed  CAS  Google Scholar 

  26. Pearlstone DB, Feig BW, Mansfield PF (1999) Port site recurrences after laparoscopy for malignant disease. Semin Surg Oncol 16: 307–312

    Article  PubMed  CAS  Google Scholar 

  27. Pezet D, Fondrinier E, Rotman N, Guy L, Lemesle P, Lointier P, Chipponi J (1992) Parietal seeding of gallblader cancer after laparoscopic cholecystectomy. N Engl J Med 79: 230

    CAS  Google Scholar 

  28. Scanlon EF, Murthy S (1991) The process of metastasis. CA Cancer J Clin 41: 301–305

    Article  PubMed  CAS  Google Scholar 

  29. Simpson-Herren L, Sanford AH, Holmquist JP (1976) Effects of surgery on the cell kinetics of residual tumor. Cancer Treat Rep 60: 1749–1760

    PubMed  CAS  Google Scholar 

  30. Sugarbaker PH (1995) Patient selection and treatment of peritoneal carcinomatosis from colorectal and appendiceal cancer. World J Surg 19: 235–240

    Article  PubMed  CAS  Google Scholar 

  31. Targarona EM, Martinez J, Nadal A, Balague C, Cardessa A (1998) Cancer dissemination during laparoscopic surgery: tubes, gas, and cells. World J Surg 22: 55–60

    Article  PubMed  CAS  Google Scholar 

  32. Vallina VL, Velasco JM (1996) The influence of laparoscopy on lymphocyte subpopulations in the surgical patient. Surg Endosc 10: 481–484 DOI: 10.1007/s0046499110094

    Article  PubMed  CAS  Google Scholar 

  33. van den Tol PM, van Rossen EE, van Eijck CH, Bonthuis F, Marquet RL, Jeekel H (1998) Reduction of peritoneal trauma by using nonsurgical gauze leads to less implantation metastasis of spilled tumor cells. Ann Surg 227: 242–248

    Article  PubMed  Google Scholar 

  34. Volz J, Koster S, Spacek Z, Paweletz N (1999) Characteristic alterations of the peritoneum after carbon dioxide pneumoperitoneum. Surg Endosc 13: 611–614 DOI: 10.1007/s004649901052

    Article  PubMed  CAS  Google Scholar 

  35. Volz J, Koster S, Spacek Z, Paweletz N (1999) The influence of pneumoperitoneum used in laparoscopic surgery on an intrabdominal tumor growth [see Comments]. Cancer 86: 770–774

    Article  PubMed  CAS  Google Scholar 

  36. Wang PH, Yuan CC, Chao KC, Yen MS, Ng HT, Chao HT (1997) Squamous cell carcinoma of the cervix after laparoscopic surgery: a case report. J Reprod Med 42: 801–804

    PubMed  CAS  Google Scholar 

  37. Watson DI, Mathew G, Ellis T, Baigrie CF, Rofe AM, Jamieson GG (1997) Gasless laparoscopy may reduce the risk of port-site metastases following laparascopic tumor surgery. Arch Surg 132: 166–168

    PubMed  CAS  Google Scholar 

  38. Whelan RL, Sellers GJ, Allendorf JD (1996) Trocar site recurrence is unlikely to result from aerosolization of tumor cells. Dis Colon Rectum 39: S7-S13

    Article  PubMed  CAS  Google Scholar 

  39. Witzig TE, Loprinzi CL, Gonchoroff NJ, Reiman HM, Cha SS (1991) DNA ploidy and cell kinetic measurements as predictors of recurrence and survival in stages B2 and C colorectal adenocarcinoma. Cancer 68: 879–888

    Article  PubMed  CAS  Google Scholar 

  40. Wu JS, Jones DB, Guo LW, Brasfield EB, Ruiz MB, Connett JM, Fleshman JW (1998) Effects of pneumoperitoneum on tumor implantation with decreasing tumor inoculum. Dis Colon Rectum 41: 141–146

    Article  PubMed  CAS  Google Scholar 

  41. Zirngibl H, Husemann B, Hermanek P (1990) Intraoperative spillage of tumor cells in surgery for rectal cancer. Dis Colon Rectum 33: 610–614

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Surgery, Centre Régional de Lutte Contre le Cancer Paul Papin, 2, rue Moll, 49033, Angers, France

    E. Fondrinier, M. Boisdron-Celle, A. Chassevent, G. Lorimier & E. Gamelin

Authors
  1. E. Fondrinier
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. Boisdron-Celle
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. Chassevent
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. G. Lorimier
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. E. Gamelin
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Online publication: 7 May 2001

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fondrinier, E., Boisdron-Celle, M., Chassevent, A. et al. Experimental assessment of tumor growth and dissemination of a microscopic peritoneal carcinomatosis after CO2 peritoneal insufflation or laparotomy. Surg Endosc 15, 843–848 (2001). https://doi.org/10.1007/s004640000315

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s004640000315

Key words

Search

Navigation