Advertisement
Original Communications| Volume 128, ISSUE 5, P799-805, November 2000

Download started.

Ok

Effect of laparotomy and laparoscopy on the establishment of lung metastasis in a murine model

      Abstract

      Background. Laparoscopic surgery is now applied to patients with gastrointestinal cancer. In animal studies, extraperitoneal tumor growth has been significantly less after laparoscopy than after laparotomy, but whether hematogenous metastasis occurs less frequently after laparoscopy is unknown. The aim of this study was to compare the frequency and growth of lung metastasis and serum levels of IL-6 and tumor necrosis factor-α (TNF-α) in mice treated by laparotomy and in mice treated by laparoscopy. Methods. We used 182 male BALB/c mice. Colon 26 cancer cells (5 × 104) were injected into the tail vein, and the mice were assigned to a laparotomy group (3-cm laparotomy), a laparoscopy group (carbon dioxide pneumoperitoneum at 6 to 8 mm Hg for 30 minutes), or a control group. Lung weight, number of lung metastases, and serum levels of IL-6 and TNF-α were measured and compared among the 3 groups. Results. The lung weight and number of metastases on the lung surface and cut section in the laparotomy group (0.44 ± 0.21 g, 55.7 ± 46.7, 23.0 ± 19.0) were significantly larger than those in the laparoscopy group (0.32 ± 0.15 g, 29.9 ± 25.5, 13.1 ± 9.9) or the control group (0.28 ± 0.13, 29.3 ± 26.2, 11.1 ± 11.1). Three hours after the procedures, the serum level of IL-6 was significantly higher in the laparotomy group (1353 ± 790 pg/mL) than in the laparoscopy group (671 ± 353 pg/mL) or the control group (333 ± 341 pg/mL). The lung weight, number of lung metastases, and levels of IL-6 and TNF-α were not different between the laparoscopy and control groups. Conclusions. Our results indicate that, although laparotomy accelerates tumor metastasis to the lung in this murine model, laparoscopy does not increase the frequency and growth of lung metastasis. The laparoscopic approach may suppress hematogenous metastasis to the lung because of decreased surgical stress and reduced cytokine response. (Surgery 2000;128:799-805.)
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Surgery
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Kitano S
        • Shimoda K
        • Miyahara M
        • Shiraishi N
        • Bandoh T
        • Yoshida T
        • et al.
        Laparoscopic approaches in the management of patients with early gastric carcinomas.
        Surg Laparosc Endosc. 1995; 5: 359-362
        • Poulin EC
        • Mamazza J
        • Schlachta CM
        • Grégoire R
        • Roy N.
        Laparoscopic resection does not adversely affect early survival curves in patients undergoing surgery for colorectal adenocarcinoma.
        Ann Surg. 1999; 229: 487-492
        • Leung KL
        • Yiu RYC
        • Lai PBS
        • Lee JFY
        • Thung KH
        • Lau WY
        Laparoscopic-assisted resection of colorectal carcinoma: five-year audit.
        Dis Colon Rectum. 1999; 42: 327-333
        • Milsom JW
        • Böhm B
        • Hammerhofer KA
        • Fazio V
        • Steiger E
        • Elson P.
        A prospective, randomized trial comparing laparoscopic versus conventional techniques in colorectal cancer surgery: a preliminary report.
        J Am Coll Surg. 1998; 187: 46-57
        • Shiraishi N
        • Adachi Y
        • Kitano S
        • Bandoh T
        • Katsuta T
        • Morimoto A.
        Indication for and outcome of laparoscopy-assisted Billroth I gastrectomy.
        Br J Surg. 1999; 86: 541-544
        • Adachi Y
        • Suematsu T
        • Shiraishi N
        • Katsuta T
        • Morimoto A
        • Kitano S
        • et al.
        Quality of life after laparoscopy-assisted Billroth I gastrectomy.
        Ann Surg. 1999; 229: 49-54
        • Wexner SD
        • Cohen SM
        Port site metastases after laparoscopic colorectal surgery for cure of malignancy [review].
        Br J Surg. 1995; 82: 295-298
        • Neuhaus SJ
        • Texler M
        • Hewett PJ
        • Watson DI
        Port-site metastases following laparoscopic surgery [review].
        Br J Surg. 1998; 85: 735-741
        • Jones DB
        • Guo LW
        • Reinhard MK
        • Soper NJ
        • Philpott GW
        • Connett J
        • et al.
        Impact of pneumoperitoneum on trocar site implantation of colon cancer in hamster model.
        Dis Colon Rectum. 1995; 38: 1182-1188
        • Mathew G
        • Watson DI
        • Rofe AM
        • Baigrie CF
        • Ellis T
        • Jamieson GG
        Wound metastases following laparoscopic and open surgery for abdominal cancer in a rat model.
        Br J Surg. 1996; 83: 1087-1090
        • Allendorf JDF
        • Bessler M
        • Kayton ML
        • Oesterling SD
        • Treat MR
        • Nowygrod R
        • et al.
        Increased tumor establishment and growth after laparotomy vs laparoscopy in a murine model.
        Arch Surg. 1995; 130: 649-653
        • Bouvy ND
        • Marquet RL
        • Jeekel J
        • Bonjer HJ
        Laparoscopic surgery is associated with less tumour growth stimulation than conventional surgery: an experimental study.
        Br J Surg. 1997; 84: 358-361
        • Da Costa ML
        • Redmond HP
        • Finnegan N
        • Flynn M
        • Bouchier-Hayes D.
        Laparotomy and laparoscopy differentially accelerate experimental flank tumour growth.
        Br J Surg. 1998; 85: 1439-1442
        • Iwanaka T
        • Arkovitz MS
        • Arya G
        • Ziegler MM
        Evaluation of operative stress and peritoneal macrophage function in minimally invasive operations.
        J Am Coll Surg. 1997; 184: 357-363
        • Da Costa ML
        • Redmond HP
        • Bouchier-Hayes DJ
        The effect of laparotomy and laparoscopy on the establishment of spontaneous tumor metastases.
        Surgery. 1998; 124: 516-525
        • Edmiston KH
        • Gangopadhyay A
        • Shoji Y
        • Nachman AP
        • Thomas P
        • Jessup JM
        In vivo induction of murine cytokine production by carcinoembryonic antigen.
        Cancer Res. 1997; 57: 4432-4436
        • Baykal A
        • Kaynaroglu V
        • Hascelik G
        • Sayek I
        • Sanac Y.
        Epinephrine and endotoxin tolerance differentially modulate serum cytokine levels to high-dose lipopolysaccharide challenge in a murine model.
        Surgery. 1999; 125: 403-410
        • Suematsu T
        • Shiromizu A
        • Yamaguchi K
        • Shiraishi N
        • Adachi Y
        • Kitano S.
        Convenient murine pneumoperitoneal model for the study of laparoscopic cancer surgery.
        Surg Laparosc Endosc. 1999; 9: 279-281
        • Vittimberga Jr, FJ
        • Foley DP
        • Meyers WC
        • Callery MP
        Laparoscopic surgery and the systemic immune response [review].
        Ann Surg. 1998; 227: 326-334
        • Stage JG
        • Schulze S
        • Möler P
        • Overgaard H
        • Andersen M
        • Rebsdorf-Pedersen VB
        • et al.
        Prospective randomized study of laparoscopic versus open colonic resection for adenocarcinoma.
        Br J Surg. 1997; 84: 391-396
        • Bouvy ND
        • Giuffrida MC
        • Tseng LN
        • Steyerberg EW
        • Marquet RL
        • Jeekel H
        • et al.
        Effects of carbon dioxide pneumoperitoneum, air pneumoperitoneum, and gasless laparoscopy on body weight and tumor growth.
        Arch Surg. 1998; 133: 652-656
        • West MA
        • Hackam DJ
        • Baker J
        • Rodriguez JL
        • Bellingham J
        • Rotstein OD
        Mechanism of decreased in vitro murine macrophage cytokine release after exposure to carbon dioxide: relevance to laparoscopic surgery.
        Ann Surg. 1997; 226: 179-190
        • Walker CBJ
        • Bruce DM
        • Heys SD
        • Gough DB
        • Binnie NR
        • Eremin O.
        Minimal modulation of lymphocyte and natural killer cell subsets following minimal access surgery.
        Am J Surg. 1999; 177: 48-54
        • Collet D
        • Vitale GC
        • Reynolds M
        • Klar E
        • Cheadle WG
        Peritoneal host defenses are less impaired by laparoscopy than by open operation.
        Surg Laparosc. 1995; 9: 1059-1064
        • Hirano T
        • Yasukawa K
        • Harada H
        • Taga T
        • Watanabe Y
        • Matsuda T
        • et al.
        Complementary DNA for a novel human interleukin (BSF-2) that induces B cell lymphocytes to produce immunoglobulin.
        Nature. 1986; 324: 73-76
        • Ohzato H
        • Yoshizaki K
        • Nishimoto N
        • Ogata A
        • Tagoh H
        • Monden M
        • et al.
        Interleukin-6 as a new indicator of inflammatory status: detection of serum levels of interleukin-6 and c-reactive protein after surgery.
        Surgery. 1992; 111: 201-209
        • Baigrie RJ
        • Lamont PM
        • Kwiatkowski D
        • Dallman MJ
        • Morris PJ
        Systemic cytokine response after major surgery.
        Br J Surg. 1992; 79: 757-760
        • Michie HR
        • Manogue KR
        • Spriggs DR
        • Revhaug A
        • O'Dwyer S
        • Dinarello CA
        • et al.
        Detection of circulating tumor necrosis factor after endotoxin administration.
        N Engl J Med. 1988; 318: 1481-1486
        • Ueo H
        • Inoue H
        • Honda M
        • Uchida I
        • Nishimura M
        • Arinaga S
        • et al.
        Production of interleukin-6 at operative wound sites in surgical patients.
        J Am Coll Surg. 1994; 179: 326-332
        • Harmon GD
        • Senagore AJ
        • Kibride MJ
        • Warzynski MJ
        Interleukin-6 response to laparoscopic and open colectomy.
        Dis Colon Rectum. 1994; 37: 754-759
        • Yoshida T
        • Kobayashi E
        • Suminaga Y
        • Yamauchi H
        • Kai T
        • Toyama N
        • et al.
        Hormone-cytokine response: pneumoperitoneum vs abdominal wall-lifting in laparoscopic cholecystectomy.
        Surg Endosc. 1997; 11: 907-910
        • Mannel DN
        • Orosz P
        • Hafner M
        • Falk W.
        Mechanisms involved in metastasis enhanced by inflammatory mediators.
        Circ Shock. 1994; 44: 9-13
        • Reichner JS
        • Mulligann JA
        • Palla ME
        • Hixson DC
        • Albina JE
        • Bland KI
        Interleukin-6 production by rat hepatocellular carcinoma cells is associated with metastatic potential but not with tumorigenicity.
        Arch Surg. 1996; 131: 360-365
        • Kinoshita T
        • Ito H
        • Miki C.
        Serum interleukin-6 level reflects the tumor proliferative activity in patients with colorectal carcinoma.
        Cancer. 1999; 85: 2526-2531
        • Jacobi CA
        • Sabat R
        • Böhm B
        • Zieren HU
        • Volk HD
        • Müller JM
        Pneumoperitoneum with carbon dioxide stimulates growth of malignant colonic cells.
        Surgery. 1997; 121: 72-78
        • Neuhaus SJ
        • Ellis T
        • Rofe AM
        • Pike GK
        • Jamieson GG
        • Watson DI
        Tumor implantation following laparoscopy using different insufflation gases.
        Surg Endosc. 1998; 12: 1300-1302
        • Jacobi CA
        • Wenger FA
        • Ordemann J
        • Gutt C
        • Sabat R
        • Müller JM
        Experimental study of the effect of intra-abdominal pressure during laparoscopy on tumour growth and port site metastasis.
        Br J Surg. 1998; 85: 1419-1422