The net immunologic advantage of laparoscopic surgery

  • Y. W. Novitsky
  • D. E. M. Litwin
  • M. P. Callery


The trauma of surgery evokes a variety of physiologic and immunologic alterations that should contribute to host defense. However, an exaggerated response to injury may result in immunosuppression and lead to significant postoperative morbidity and mortality. Laparoscopic surgery may result in less induced surgical trauma than conventional open surgery. Decreased postoperative pain and speedy functional recovery of laparoscopic patients may be attributable to the reduced inflammatory response and minimal immunosuppression. Inflammation, an early protective homeostatic immune response to injury, is characterized by the production of proinflammatory cytokines and by activation of cellular and humoral immune mechanisms. Postoperative levels of the inflammatory cytokines have been consistently lower after laparoscopic procedures, indicating a smaller degree of surgical insult and acute inflammatory reaction. Surgical stress derails the functions of both polymorphonuclear and mononuclear cells, which may lead to an increased risk of postoperative infection. Comparative studies of cellular immunity after laparoscopic and conventional surgery demonstrate immunologic advantage conferred by laparoscopy. Exaggerated activation of peritoneal immunity may lead to a relative local immunosuppression, resulting in ineffective intraperitoneal bacterial clearance and serious postoperative infections. Functions of the peritoneal macrophages are better preserved when laparotomy is avoided. Decreased perioperative stress may be particularly important for oncologic patients. Laparoscopic approaches may result in diminished perioperative tumor dissemination and better cancer outcomes. Although laparoscopy is “minimally invasive,” systemic immune responses still are undeniably activated. However, laparoscopic surgery appears to induce a smaller injury, resulting in proportionally decreased immunologic changes. In addition to improved cosmesis and faster functional recovery, a patient undergoing laparoscopic surgery may benefit most from a net immunologic advantage.


Surgical stress Laparoscopy Immune system activation Acute inflammatory response Cell-mediated immunity Peritoneal host defense 


  1. 1.
    Allendorf, JDF, Bessler, M, Kayton, ML, Oesterling, SD, Treat, MR, Nowygrod, R, Whelan, RL 1995Increased tumor establishment and growth after laparotomy vs laparoscopy in a murine modelArch Surg130649653PubMedGoogle Scholar
  2. 2.
    Allendorf, JD, Bessler, M, Whelan, RL, Trokel, M, Laird, DA, Terry, MB, Treat, MR 1996Better preservation of immune function after laparoscopic-assisted versus open bowel resection in a murine modelDis Colon Rectum39S67S72PubMedGoogle Scholar
  3. 3.
    Arya, G, Garcia, VF 1995Hypoxia/reoxygenation affects endotoxin toleranceJ Surg Res591316CrossRefPubMedGoogle Scholar
  4. 4.
    Baigrie, RJ, Lamont, PM, Kwiatkowski, D, Dallman, MJ, Morris, PJ 1992Systemic cytokine response after major surgeryBr J Surg79757760PubMedGoogle Scholar
  5. 5.
    Balague, C, Targarona, EM, Pujol, M, Filella, X, Espert, JJ, Trias, M 1999Peritoneal response to a septic challenge: comparison between open laparotomy, pneumoperitoneum laparoscopy, and wall-lift laparoscopySurg Endosc13792796CrossRefPubMedGoogle Scholar
  6. 6.
    Baumann, H, Gauodie, J 1994The acute-phase responseImmunol Today157480CrossRefPubMedGoogle Scholar
  7. 7.
    Biffl, WL, Moore, EE, Moore, FA, Peterson, VM 1996Interleukin-6 in the injured patient: marker of injury or mediator of inflammation?Ann Surg224647664CrossRefPubMedGoogle Scholar
  8. 8.
    Bolufer, JM, Delgado, F, Blanes, F, Martinez-Abad, M, Canos, JI, Martin, J, Oliver, MJ 1995Injury in laparoscopic surgerySurg Laparosc Endosc5318323PubMedGoogle Scholar
  9. 9.
    Brune, IB, Wilke, W, Hensler, T, Holzmann, B, Siewert, JR 1999Downregulation of T-helper type 1 immune response and altered proinflammatory and antiinflammatory T-cell cytokine balance following conventional but not laparoscopic surgeryAm J Surg1775560CrossRefPubMedGoogle Scholar
  10. 10.
    Carey, PD, Wakefield, CH, Thayeb, A, Monson, JR, Darzi, A, Guillou, PJ 1994Effects of minimally invasive surgery on hypochlorous acid production by neutrophilsBr J Surg81557560PubMedGoogle Scholar
  11. 11.
    Carter, JJ, Whelan, RL 2001The immunologic consequences of laparoscopy in oncologySurg Oncol Clin North Am10655677Google Scholar
  12. 12.
    Cava, A, Roman, J, Gonzalez, QA, Martin, F, Aramburo, P 1990Subcutaneous metastasis following laparoscopy in gastric adenocarcinomaEur J Surg Oncol166376PubMedGoogle Scholar
  13. 13.
    Chapman, AE, Levitt, MD, Hewett, P, Woods, R, Sheiner, H, Madden, GJ 2001Laparoscopic-assisted resection of colorectal malignancies: a systematic reviewAnn Surg234590606CrossRefPubMedGoogle Scholar
  14. 14.
    Cheadle, WG, Hershman, MJ, Wellhausen, SR, Polk, HC,Jr 1991HLA-DR antigen expression on peripheral blood monocytes correlates with surgical infectionAm J Surg161639645CrossRefPubMedGoogle Scholar
  15. 15.
    Chekan, EG, Nataraj, C, Clary, EM, Hayward, TZ, Brody, FJ, Stamat, JC, Fina, MC, Eubanks, WS, Westcott, CJ 1999Intraperitoneal immunity and pneumoperitoneumSurg Endosc1311351138CrossRefPubMedGoogle Scholar
  16. 16.
    Cho, JM, LaPorta, AJ, Clark, JR, Schofield, MJ, Hammond, SL, Mallory, PL 1994Response of serum cytokines in patients undergoing laparoscopic cholecystectomySurg Endosc813801384CrossRefPubMedGoogle Scholar
  17. 17.
    Clair, DG, Lautz, DB, Brooks, DC 1993Rapid development of umbilical metastases after laparoscopic cholecystectomy for unsuspected gallbladder carcinomaSurgery113355358PubMedGoogle Scholar
  18. 18.
    Collet, D, Vitale, GC, Reynolds, M, Klar, E, Cheadle, WG 1995Peritoneal host defenses are less impaired by laparoscopy than by open operationSurg Endosc910591064PubMedGoogle Scholar
  19. 19.
    DaCosta, ML, Redmond, HP, Finnegan, N, Flynn, M, Bouchie-Hayes, D 1998Laparotomy and laparoscopy differentially accelerate experimental flank tumour growthBr J Surg8514391442CrossRefPubMedGoogle Scholar
  20. 20.
    Davies, MG, Hagen, PO 1997Systemic inflammatory response syndromeBr J Surg84920935CrossRefPubMedGoogle Scholar
  21. 21.
    Decker, D, Schondorf, M, Bidlingmaier, F, Hirner, A, Ruecker, AA 1996Surgical stress induces a shift in the type-1/type-2 T-helper cell balance, suggesting downregulation of cell-mediated and upregulation of antibody-mediated immunity commensurate to the traumaSurgery119316325PubMedGoogle Scholar
  22. 22.
    Delgado, S, Lacy, AM, Filella, X, Castells, A, Garcia-Valdecasas, JC, Pique, JM, Momblan, D, Visa, J 2001Acute-phase response in laparoscopic and conventional colectomy in colon cancer: a randomized studyDis Colon Rectum44638646PubMedGoogle Scholar
  23. 23.
    Drouard, F, Delamarre, J, Capron, J 1991Cutaneous seeding of gallbladder cancer after laparoscopic cholecystectomyN Engl J Med3251316Google Scholar
  24. 24.
    Eggermont, AM, Steller, EP, Marquet, RL, Jeekel, J, Sugarbaker, PH 1988Local regional promotion of tumor growth after abdominal surgery is dominant over immunotherapy with interleukin-2 and lymphokine activated killer cellsCancer Detect Prev12421429PubMedGoogle Scholar
  25. 25.
    Franklin, ME, Kazantsev, B, Abrego, D, Diaz, EJ, Balli, J, Glass, L 2000Laparoscopic surgery for stage III colon cancer: long-term follow upSurg Endosc14612616CrossRefPubMedGoogle Scholar
  26. 26.
    Fusco, MA, Paluzi, MW 1993Abdominal wall recurrence after laparoscopic-assisted colectomy for adenocarcinoma of the colon: report of a caseDis Colon Rectum356858861Google Scholar
  27. 27.
    Gitzelmann, CA, Mendoza-Sagaon, M, Talamini, MA, Ahmal, SA, Pegoli, W, Paidas, CN 1999Cell-mediated immune response is better preserved by laparoscopy than laparotomySurgery1266571Google Scholar
  28. 28.
    Glaser, F, Sannwald, GA, Buhr, HJ, Kuntz, C, Mayer, H, Klee, F, Herfarth, C 1995General stress response to conventional and laparoscopic cholecystectomyAnn Surg221372380PubMedGoogle Scholar
  29. 29.
    Goshima, H, Saji, S, Furuta, T, Taneumura, H, Takao, H, Kida, H, Takahashi, H 1989Experimental study on preventive effects of lung metastases using LAK cells induced from various lymphocytes: special references to enhancement of lung metastasis after laparotomy stressJpn J Surg Soc9012451250Google Scholar
  30. 30.
    Hackam, DJ, Rotstein, OD 1998Host response to laparoscopic surgery: mechanisms and clinical correlatesCan J Surg41103110Google Scholar
  31. 31.
    Halevy, A, Lin, G, Gold-Deutsch, R, Lavi, R, Negri, M, Evans, S, Cotariu, D, Sackier, JM 1995Comparison of serum C-reactive protein concentration for laparoscopic versus open cholecystectomySurg Endosc9280282CrossRefPubMedGoogle Scholar
  32. 32.
    Harmon, GD, Senagore, AJ, Kilbride, MJ, Warzynski, MJ 1994Interleukin-6 response to laparoscopic and open colectomyDis Colon Rectum37754759PubMedGoogle Scholar
  33. 33.
    Hartley, JE, Mehigan, BJ, MacDonald, AW, Lee, PW, Monson, JR 2000Patterns of recurrence and survival after laparoscopic and conventional resections for colorectal carcinomaAnn Surg232181186CrossRefPubMedGoogle Scholar
  34. 34.
    Hewitt, PM, Ip, SM, Kwok, SP, Somers, SS, Li, K, Leung, KL, Lau, WY, Li, AK 1998Laparoscopic-assisted vs open surgery for colorectal cancers: comparative study of immune effectsDis Colon Rectum41901909PubMedGoogle Scholar
  35. 35.
    Hildebrandt, U, Kessler, K, Pistorius, G, Lindemann, W, Ecker, KW, Feifel, G, Menger, MD 1999Granulocyte elastase and systemic cytokine response after laparoscopic assisted and open resections in Crohn’s diseaseDis Colon Rectum4214801486PubMedGoogle Scholar
  36. 36.
    Hill, AD, Banwell, PE, Darzi, A, Menzies-Gow, N, Monson, JR, Guillou, PJ 1995Inflammatory markers following laparoscopic and open hernia repairSurg Endosc9695698CrossRefPubMedGoogle Scholar
  37. 37.
    Horgan, PG, Fitzpatrick, M, Couse, NF 1992Laparoscopy is less immunotraumatic than laparotomyMinim Invasive Ther1241244Google Scholar
  38. 38.
    Iwanaka, T, Arkovitz, MS, Arya, G, Ziegler, MM 1997Evaluation of operative stress and peritoneal macrophage function in minimally invasive operationsJ Am Coll Surg184357363PubMedGoogle Scholar
  39. 39.
    Jackson, PG, Evans, SR 2000Intraperitoneal macrophages and tumor immunity: previewJ Surg Oncol75146154CrossRefPubMedGoogle Scholar
  40. 40.
    Jacobi, CA, Ordemann, J, Zieren, HU, Volk, HD, Bauhofer, A, Halle, E, Muller, JM 1998Increased systemic inflammation after laparotomy vs laparoscopy in an animal model of peritonitisArch Surg133258262CrossRefPubMedGoogle Scholar
  41. 41.
    Jakeways, MS, Mitchell, V, Hashim, IA, Chadwick, SJ, Shenkin, A, Green, CJ, Carli, F 1994Metabolic and inflammatory responses after open or laparoscopic cholecystectomyBr J Surg81127131PubMedGoogle Scholar
  42. 42.
    Joris, J, Cigarini, I, Legrand, M, Jacquet, N, Groote, D, Franchimont, P, Lamy, M 1992Metabolic and respiratory changes after cholecystectomy performed via laparotomy or laparoscopyBr J Anaesth69341345PubMedGoogle Scholar
  43. 43.
    Kirman, I, Poltoratskaia, N, Herlyn, D, Whelan, RL 2003Addition of interleukin-12 to GA 733 tumor protein vaccine lead to development of tumor protective immunity despite surgical stressSurg Endosc1711351139CrossRefPubMedGoogle Scholar
  44. 44.
    Kloosterman, T, Blomberg, BM, Borgstein, P, Cuesta, MA, Scheper, RJ, Meijer, S 1994Unimpaired immune function after laparoscopic cholecystectomySurgery115424428PubMedGoogle Scholar
  45. 45.
    Kopernik, G, Avinoach, E, Grossman, Y, Levy, R, Yulzari, R, Rogachev, B, Douvdevani, A 1998The effect of a high partial pressure of carbon dioxide environment on metabolism and immune functions of human peritoneal cells-relevance to carbon dioxide pneumoperitoneumAm J Obstet Gynecol17915031510PubMedGoogle Scholar
  46. 46.
    Kuntz, C, Wunsch, A, Bay, F, Windeler, J, Glaser, F, Herfarth, C 1996Laparoscopic colon resection in the rat: less immune and stress reaction and improved postoperative recoverySurg Endosc10568Google Scholar
  47. 47.
    Lacy, AM, Garcia-Valdecasas, JC, Delgado, S, Castells, A, Taura, P, Pique, JM, Visa, J 2002Laparoscopy-assisted colectomy versus open colectomy for treatment of non-metastatic colon cancer: a randomized trialLancet35922242229CrossRefPubMedGoogle Scholar
  48. 48.
    Lee, SW, Feingold, DL, Carter, JJ, Zhai, C, Stapleton, G, Gleason, N, Whelan, RL 2003Peritoneal macrophage and blood monocyte functions after open and laparoscopic-assisted cecectomy in ratsSurg Endosc1719962002CrossRefPubMedGoogle Scholar
  49. 49.
    Leung, KL, Meng, WCS, Lee, JFY, Thung, KH, Lai, PBS, Lau, WY 1999Laparoscopic-assisted resection of colonic carcinoma: a case-control studyJ Surg Oncol7197100CrossRefPubMedGoogle Scholar
  50. 50.
    Little, D, Regan, M, Keane, RM, Bouchier-Hayes, D 1993Perioperative immune modulationSurgery1148791PubMedGoogle Scholar
  51. 51.
    Malik, E, Buchweitz, O, Muller-Steinhardt, M, Kressin, P, Meyhofer-Malik, A, Diedrich, K 2001Prospective evaluation of the systemic immune response following abdominal, vaginal, and laparoscopically assisted vaginal hysterectomySurg Endosc15463466CrossRefPubMedGoogle Scholar
  52. 52.
    Maruszynski, M, Pojda, Z 1995Interleukin-6 (IL-6) levels in the monitoring of surgical traumaSurg Endosc9882885PubMedGoogle Scholar
  53. 53.
    Mathew, G, Watson, DI, Ellis, TS, Jamieson, GG, Rofe, AM 1999The role of peritoneal immunity and the tumour-bearing state on the development of wound and peritoneal metastases after laparoscopyAust N Z J Surg691418CrossRefPubMedGoogle Scholar
  54. 54.
    McMahon, AJ, O’Dwyer, PJ, Cruikshank, AM, McMillan, DC, O’Reilly, DS, Lowe, GD, Rumley, A, Logan, RW, Baxter, JN 1993Comparison of metabolic responses to laparoscopic and minilaparotomy cholecystectomyBr J Surg8012551258PubMedGoogle Scholar
  55. 55.
    McMasters, KM, Cheadle, WG 1993Regulation of macrophage TNF alpha, IL-1 beta, and Ia (I-A alpha) mRNA expression during peritonitis is site dependentJ Surg Res54426430CrossRefPubMedGoogle Scholar
  56. 56.
    Mealy, K, Gallagher, H, Barry, M, Lennon, F, Traynor, O, Hyland, J 1992Physiological and metabolic responses to open and laparoscopic cholecystectomyBr J Surg7910611064PubMedGoogle Scholar
  57. 57.
    Milsom, JW, Bohm, B, Hammerhofer, KA, Fazio, V, Steiger, E, Elson, P 1998A prospective randomized trial comparing laparoscopic versus conventional techniques in colorectal cancer surgery: a preliminary reportJ Am Coll Surg1874654CrossRefPubMedGoogle Scholar
  58. 58.
    Okamoto, T, Tsuburaya, A, Yanoma, S, Yoshikawa, T, Cho, H, Takanashi, Y, Noguchi, Y 2003Inhibition of peritoneal metastasis in an animal gastric cancer model by interferon-gamma and interleukin-2Anticancer Res23149153PubMedGoogle Scholar
  59. 59.
    Ordemann, J, Jacobi, CA, Schwenk, W, Stosslein, R, Muller, JM 2001Cellular and humoral inflammatory response after laparoscopic colorectal resectionsSurg Endosc15600608CrossRefPubMedGoogle Scholar
  60. 60.
    Pearlstone, DB, Mansfield, PF, Curley, SA, Kumparatana, M, Cook, P, Feig, BW 1999Laparoscopy in 533 patients with abdominal malignancySurgery1256772CrossRefPubMedGoogle Scholar
  61. 61.
    Perttila, J, Salo, M, Ovaska, J, Gronroos, J, Lavonius, M, Katila, A, Lahteenmaki, M, Pulkki, K 1999Immune response after laparoscopic and conventional Nissen fundoplicationEur J Surg1652128CrossRefPubMedGoogle Scholar
  62. 62.
    Polk, HC,Jr, George, CD, Hershman, MJ, Wellhausen, SR, Cheadle, WG 1988The capacity of serum to support neutrophil phagocytosis is a vital host defense mechanism in severely injured patientsAnn Surg207686692PubMedGoogle Scholar
  63. 63.
    Redmond, HP, Watson, RW, Houghton, T, Condron, C, Watson, RG, Bouchier-Hayes, D 1994Immune function in patients undergoing open vs laparoscopic cholecystectomyArch Surg12912401246PubMedGoogle Scholar
  64. 64.
    Reilly, WT, Nelson, H, Schroeder, G, Weiand, HS, Bolton, J, O’Connell, MJ 1996Wound recurrence following conventional treatment of colorectal cancerDis Colon Rectum39200207PubMedGoogle Scholar
  65. 65.
    Riboli, E, Terrizzi, A, Arnulfo, G, Bertoglio, S 1984Immunosuppressive effect of surgery evaluated by the multitest cell-mediated immunity systemCan J Surg276063Google Scholar
  66. 66.
    Rixen, D, Siegel, JH, Abu-Salih, A, Bertolini, M, Panagakos, F, Espina, N 1995Physiologic state severity classification as an indicator of posttrauma cytokine responseShock42738PubMedGoogle Scholar
  67. 67.
    Romeo, C, Impellizzeri, P, Antonuccio, P, Turiaco, N, Cifala, S, Gentile, C, Passaniti, M, Marini, H, Squadrito, F, Altavilla, D 2003Peritoneal macrophage activity after laparoscopy or laparotomyJ Pediatr Surg3897101CrossRefPubMedGoogle Scholar
  68. 68.
    Rotstein, OD 2001Peritoneal host defenses: modulation by carbon dioxide insufflationSurg Infect2163168CrossRefGoogle Scholar
  69. 69.
    Roumen, RM, Meurs, PA, Kuypers, HH, Kraak, WA, Sauerwein, RW 1992Serum interleukin-6 and C-reactive protein responses in patients after laparoscopic or conventional cholecystectomyEur J Surg158541544PubMedGoogle Scholar
  70. 70.
    Sampson, LE, Chaplin, DJ 1996The influence of oxygen and carbon dioxide tension on the production of TNF alpha by activated macrophagesBr J Cancer27S133S135Google Scholar
  71. 71.
    Scheidbach, H, Schneider, C, Hugel, O, Scheuerlein, H, Barlehner, E, Konradt, J, Wittekind, C, Kockerling, F 2003Oncological quality and preliminary long-term results in laparoscopic colorectal surgerySurg Endosc17903910CrossRefPubMedGoogle Scholar
  72. 72.
    Schwenk, W, Jacobi, C, Mansmann, U, Bohm, B, Muller, JM 2000Inflammatory response after laparoscopic and conventional colorectal resections: results of a prospective randomized trialLangenbeck’s Arch Surg38529CrossRefGoogle Scholar
  73. 73.
    Sietses, C, Beelen, RH, Meijer, S, Cuesta, MA 1999Immunologic consequences of laparoscopic surgery: speculation on the causes and clinical implicationsLangenbeck’s Arch Surg384250258CrossRefGoogle Scholar
  74. 74.
    Sietses, C, Havenith, CE, Eijsbouts, QA, Leeuwen, PA, Meijer, S, Beelen, RH, Cuesta, MA 2000Laparoscopic surgery preserves monocyte-mediated tumor cell killing in contrast to the conventional approachSurg Endosc14456460Google Scholar
  75. 75.
    Sietses, C, Wiezer, MJ, Eijsbouts, QA, Beelen, RH, Leeuwen, PA, Blomberg, BM, Meijer, S, Cuesta, MA 1999A prospective randomized study of the systemic immune response after laparoscopic and conventional Nissen fundoplicationSurgery12659CrossRefPubMedGoogle Scholar
  76. 76.
    Smit, MJ, Beelen, RH, Eijsbouts, QA, Meijer, S, Cuesta, MA 1996Immunological response in laparoscopic surgeryActa Gastroenterol Belg59245247PubMedGoogle Scholar
  77. 77.
    Stage, JG, Schulze, S, Moller, P, Overgaard, H, Andersen, M, Rebsdorf-Pedersen, VB, Nielsen, HJ 1997Prospective randomized study of laparoscopic versus open colonic resection for adenocarcinomaBr J Surg83391396CrossRefGoogle Scholar
  78. 78.
    Tang, CL, Eu, KW, Tai, BC, Soh, JGS, Machin, D, Seow-Choen, F 2001Randomized clinical trial of the effect of open versus laparoscopically assisted colectomy on systemic immunity in patients with colorectal cancerBr J Surg88801807CrossRefPubMedGoogle Scholar
  79. 79.
    Travis, J 1988Structure, function, and control of neutrophil proteinasesAm J Med843742CrossRefGoogle Scholar
  80. 80.
    Tung, PHM, Smith, CD 1999Laparoscopic insufflation with room air exaggerated interleukin-6 responseSurg Endosc13473475CrossRefPubMedGoogle Scholar
  81. 81.
    Ure, BM, Niewold, TA, Bax, NM, Ham, M, Zee, DC, Essen, GJ 2002Peritoneal, systemic, and distant organ inflammatory responses are reduced by a laparoscopic approach and carbon dioxide versus airSurg Endosc16836842CrossRefPubMedGoogle Scholar
  82. 82.
    Valina, VL, Velasco, JM 1996The influence of laparoscopy on lymphocyte subpopulations in the surgical patientSurg Endosc10481484CrossRefPubMedGoogle Scholar
  83. 83.
    Varga, G, Gal, I, Roth, E, Lantos, J, Jaberansari, MT 1997Inflammatory mediators and surgical trauma regarding laparoscopic access: neutrophil functionActa Chir Hung36368369PubMedGoogle Scholar
  84. 84.
    Vittimberga, FJ,Jr, Foley, DP, Meyers, WC, Callery, MP 1998Laparoscopic surgery and the systemic immune responseAnn Surg227326334CrossRefPubMedGoogle Scholar
  85. 85.
    Wakefield, CH, Carey, PD, Foulds, S, Monson, JRT, Guillou, PJ 1993Polymorphonuclear leukocyte activation; an early marker of the postsurgical sepsis responseArch Surg128390395PubMedGoogle Scholar
  86. 86.
    Watson, RW, Redmond, 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
  87. 87.
    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
  88. 88.
    Wexner, SD, Cohen, SM 1995Portesite metastasis after laparoscopic colorectal surgery for cure of malignancyBr J Surg82295298PubMedGoogle Scholar
  89. 89.
    Whelan, RL 2003Open versus laparoscopy-assisted colectomyLancet36175CrossRefPubMedGoogle Scholar
  90. 90.
    Whelan, RL, Franklin, M, Holubar, SD, Donahue, J, Fowler, R, Munger, C, Doorman, J, Balli, JE, Glass, J, Gonzalez, JJ, Bessler, M, Xie, H, Treat, M 2003Postoperative cell-mediated immune response is better preserved after laparoscopic vs open colorectal resection in humansSurg Endosc17972978CrossRefPubMedGoogle Scholar
  91. 91.
    Wollenberg, GK, DeForge, LE, Bolgos, G, Remick, DG 1993Differential expression of tumor necrosis factor and interleukin-6 by peritoneal macrophages in vivo and in cultureAm J Pathol14311211130PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Y. W. Novitsky
    • 1
  • D. E. M. Litwin
    • 1
  • M. P. Callery
    • 2
  1. 1.Department of SurgeryUniversity of Massachusetts Medical SchoolWorcesterUSA
  2. 2.Department of SurgeryBeth Israel Deaconess Medical Center, Harvard Medical SchoolBostonUSA

Personalised recommendations