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. 1998 Mar;227(3):326–334. doi: 10.1097/00000658-199803000-00003

Laparoscopic surgery and the systemic immune response.

F J Vittimberga Jr 1, D P Foley 1, W C Meyers 1, M P Callery 1
PMCID: PMC1191269  PMID: 9527054

Abstract

OBJECTIVE: The authors review studies relating to the immune responses evoked by laparoscopic surgery. SUMMARY BACKGROUND DATA: Laparoscopic surgery has gained rapid acceptance based on clinical grounds. Patients benefit from faster recovery, decreased pain, and quicker return to normal activities. Only more recently have attempts been made to identify the metabolic and immune responses that may underlie this clinical success. The immune responses to laparoscopy are now being evaluated in relation to the present knowledge of immune responses to traditional laparotomy and surgery in general. METHODS: A review of the published literature of the immune and metabolic responses to laparoscopy was performed. Laparoscopic surgery is compared with the traditional laparotomy on the basis of local and systemic immune responses and patterns of tumor growth. The impact of pneumoperitoneum and insufflation gases on the immune response is also reviewed. CONCLUSIONS: The systemic immune responses for surgery in general may not apply to laparoscopic surgery. The body's response to laparoscopy is one of lesser immune activation as opposed to immunosuppression.

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Selected References

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  1. Alexander R. J., Jaques B. C., Mitchell K. G. Laparoscopically assisted colectomy and wound recurrence. Lancet. 1993 Jan 23;341(8839):249–250. doi: 10.1016/0140-6736(93)90121-v. [DOI] [PubMed] [Google Scholar]
  2. Allendorf J. D., Bessler M., Kayton M. L., Oesterling S. D., Treat M. R., Nowygrod R., Whelan R. L. Increased tumor establishment and growth after laparotomy vs laparoscopy in a murine model. Arch Surg. 1995 Jun;130(6):649–653. doi: 10.1001/archsurg.1995.01430060087016. [DOI] [PubMed] [Google Scholar]
  3. Aronsen K. F., Ekelund G., Kindmark C. O., Laurell C. B. Sequential changes of plasma proteins after surgical trauma. Scand J Clin Lab Invest Suppl. 1972;124:127–136. doi: 10.3109/00365517209102760. [DOI] [PubMed] [Google Scholar]
  4. Babineau T. J., Lewis W. D., Jenkins R. L., Bleday R., Steele G. D., Jr, Forse R. A. Role of staging laparoscopy in the treatment of hepatic malignancy. Am J Surg. 1994 Jan;167(1):151–155. doi: 10.1016/0002-9610(94)90066-3. [DOI] [PubMed] [Google Scholar]
  5. Baigrie R. J., Lamont P. M., Kwiatkowski D., Dallman M. J., Morris P. J. Systemic cytokine response after major surgery. Br J Surg. 1992 Aug;79(8):757–760. doi: 10.1002/bjs.1800790813. [DOI] [PubMed] [Google Scholar]
  6. Barkun J. S., Wexler M. J., Hinchey E. J., Thibeault D., Meakins J. L. Laparoscopic versus open inguinal herniorrhaphy: preliminary results of a randomized controlled trial. Surgery. 1995 Oct;118(4):703–710. doi: 10.1016/s0039-6060(05)80038-8. [DOI] [PubMed] [Google Scholar]
  7. Barsoum G. H., Windsor C. W. Parietal seeding of carcinoma of the gallbladder after laparoscopic cholecystectomy. Br J Surg. 1992 Aug;79(8):846–846. [PubMed] [Google Scholar]
  8. Baumann H., Gauldie J. Regulation of hepatic acute phase plasma protein genes by hepatocyte stimulating factors and other mediators of inflammation. Mol Biol Med. 1990 Apr;7(2):147–159. [PubMed] [Google Scholar]
  9. Bessler M., Whelan R. L., Halverson A., Treat M. R., Nowygrod R. Is immune function better preserved after laparoscopic versus open colon resection? Surg Endosc. 1994 Aug;8(8):881–883. doi: 10.1007/BF00843460. [DOI] [PubMed] [Google Scholar]
  10. Bloechle C., Emmermann A., Treu H., Achilles E., Mack D., Zornig C., Broelsch C. E. Effect of a pneumoperitoneum on the extent and severity of peritonitis induced by gastric ulcer perforation in the rat. Surg Endosc. 1995 Aug;9(8):898–901. doi: 10.1007/BF00768887. [DOI] [PubMed] [Google Scholar]
  11. Bolufer J. M., Delgado F., Blanes F., Martínez-Abad M., Canos J. I., Martín J., Oliver M. J. Injury in laparoscopic surgery. Surg Laparosc Endosc. 1995 Aug;5(4):318–323. [PubMed] [Google Scholar]
  12. Bouvy N. D., Marquet R. L., Jeekel H., Bonjer H. J. Impact of gas(less) laparoscopy and laparotomy on peritoneal tumor growth and abdominal wall metastases. Ann Surg. 1996 Dec;224(6):694–701. doi: 10.1097/00000658-199612000-00005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Callery M. P., Strasberg S. M., Doherty G. M., Soper N. J., Norton J. A. Staging laparoscopy with laparoscopic ultrasonography: optimizing resectability in hepatobiliary and pancreatic malignancy. J Am Coll Surg. 1997 Jul;185(1):33–39. [PubMed] [Google Scholar]
  14. Callery M. P., Strasberg S. M., Soper N. J. Complications of laparoscopic general surgery. Gastrointest Endosc Clin N Am. 1996 Apr;6(2):423–444. [PubMed] [Google Scholar]
  15. Carey P. D., Wakefield C. H., Thayeb A., Monson J. R., Darzi A., Guillou P. J. Effects of minimally invasive surgery on hypochlorous acid production by neutrophils. Br J Surg. 1994 Apr;81(4):557–560. doi: 10.1002/bjs.1800810425. [DOI] [PubMed] [Google Scholar]
  16. Carozzi S., Caviglia P. M., Nasini M. G., Schelotto C., Santoni O., Pietrucci A. Peritoneal dialysis solution pH and Ca2+ concentration regulate peritoneal macrophage and mesothelial cell activation. ASAIO J. 1994 Jan-Mar;40(1):20–23. [PubMed] [Google Scholar]
  17. Cava A., Román J., González Quintela A., Martín F., Aramburo P. Subcutaneous metastasis following laparoscopy in gastric adenocarcinoma. Eur J Surg Oncol. 1990 Feb;16(1):63–67. [PubMed] [Google Scholar]
  18. Cho J. M., LaPorta A. J., Clark J. R., Schofield M. J., Hammond S. L., Mallory P. L., 2nd Response of serum cytokines in patients undergoing laparoscopic cholecystectomy. Surg Endosc. 1994 Dec;8(12):1380–1384. doi: 10.1007/BF00187340. [DOI] [PubMed] [Google Scholar]
  19. Collet D., Vitale G. C., Reynolds M., Klar E., Cheadle W. G. Peritoneal host defenses are less impaired by laparoscopy than by open operation. Surg Endosc. 1995 Oct;9(10):1059–1064. doi: 10.1007/BF00188987. [DOI] [PubMed] [Google Scholar]
  20. Cruickshank A. M., Fraser W. D., Burns H. J., Van Damme J., Shenkin A. Response of serum interleukin-6 in patients undergoing elective surgery of varying severity. Clin Sci (Lond) 1990 Aug;79(2):161–165. doi: 10.1042/cs0790161. [DOI] [PubMed] [Google Scholar]
  21. Drouard F., Delamarre J., Capron J. P. Cutaneous seeding of gallbladder cancer after laparoscopic cholecystectomy. N Engl J Med. 1991 Oct 31;325(18):1316–1316. doi: 10.1056/NEJM199110313251816. [DOI] [PubMed] [Google Scholar]
  22. Dugue L., Fritsch S., Felten A., Gossot D., Colomer S., Celerier M., Lagrange P., Revillon Y. Effets de l'insufflation intra-péritonéale sur la dissémination hématogène des infections abdominales. Résultats préliminaires d'une étude expérimentale chez le rat. Ann Chir. 1995;49(5):423–426. [PubMed] [Google Scholar]
  23. Forse R. A., Babineau T., Bleday R., Steele G., Jr Laparoscopy/thoracoscopy for staging: I. Staging endoscopy in surgical oncology. Semin Surg Oncol. 1993 Jan-Feb;9(1):51–55. doi: 10.1002/ssu.2980090110. [DOI] [PubMed] [Google Scholar]
  24. Fusco M. A., Paluzzi M. W. Abdominal wall recurrence after laparoscopic-assisted colectomy for adenocarcinoma of the colon. Report of a case. Dis Colon Rectum. 1993 Sep;36(9):858–861. doi: 10.1007/BF02047384. [DOI] [PubMed] [Google Scholar]
  25. Gauldie J., Richards C., Harnish D., Lansdorp P., Baumann H. Interferon beta 2/B-cell stimulatory factor type 2 shares identity with monocyte-derived hepatocyte-stimulating factor and regulates the major acute phase protein response in liver cells. Proc Natl Acad Sci U S A. 1987 Oct;84(20):7251–7255. doi: 10.1073/pnas.84.20.7251. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Glaser F., Sannwald G. A., Buhr H. J., Kuntz C., Mayer H., Klee F., Herfarth C. General stress response to conventional and laparoscopic cholecystectomy. Ann Surg. 1995 Apr;221(4):372–380. doi: 10.1097/00000658-199504000-00007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Gurtner G. C., Robertson C. S., Chung S. C., Ling T. K., Ip S. M., Li A. K. Effect of carbon dioxide pneumoperitoneum on bacteraemia and endotoxaemia in an animal model of peritonitis. Br J Surg. 1995 Jun;82(6):844–848. doi: 10.1002/bjs.1800820639. [DOI] [PubMed] [Google Scholar]
  28. Halevy A., Lin G., Gold-Deutsch R., Lavi R., Negri M., Evans S., Cotariu D., Sackier J. M. Comparison of serum C-reactive protein concentrations for laparoscopic versus open cholecystectomy. Surg Endosc. 1995 Mar;9(3):280–282. doi: 10.1007/BF00187768. [DOI] [PubMed] [Google Scholar]
  29. Hall G. M., Desborough J. P. Interleukin-6 and the metabolic response to surgery. Br J Anaesth. 1992 Oct;69(4):337–338. doi: 10.1093/bja/69.4.337-a. [DOI] [PubMed] [Google Scholar]
  30. Hamid J., Bancewicz J., Brown R., Ward C., Irving M. H., Ford W. L. The significance of changes in blood lymphocyte populations following surgical operations. Clin Exp Immunol. 1984 Apr;56(1):49–57. [PMC free article] [PubMed] [Google Scholar]
  31. Hansbrough J. F., Bender E. M., Zapata-Sirvent R., Anderson J. Altered helper and suppressor lymphocyte populations in surgical patients. A measure of postoperative immunosuppression. Am J Surg. 1984 Sep;148(3):303–307. doi: 10.1016/0002-9610(84)90459-8. [DOI] [PubMed] [Google Scholar]
  32. Harmon G. D., Senagore A. J., Kilbride M. J., Warzynski M. J. Interleukin-6 response to laparoscopic and open colectomy. Dis Colon Rectum. 1994 Aug;37(8):754–759. doi: 10.1007/BF02050137. [DOI] [PubMed] [Google Scholar]
  33. Hill A. D., Banwell P. E., Darzi A., Menzies-Gow N., Monson J. R., Guillou P. J. Inflammatory markers following laparoscopic and open hernia repair. Surg Endosc. 1995 Jun;9(6):695–698. doi: 10.1007/BF00187942. [DOI] [PubMed] [Google Scholar]
  34. Jones D. B., Guo L. W., Reinhard M. K., Soper N. J., Philpott G. W., Connett J., Fleshman J. W. Impact of pneumoperitoneum on trocar site implantation of colon cancer in hamster model. Dis Colon Rectum. 1995 Nov;38(11):1182–1188. doi: 10.1007/BF02048334. [DOI] [PubMed] [Google Scholar]
  35. Joris J., Cigarini I., Legrand M., Jacquet N., De Groote D., Franchimont P., Lamy M. Metabolic and respiratory changes after cholecystectomy performed via laparotomy or laparoscopy. Br J Anaesth. 1992 Oct;69(4):341–345. doi: 10.1093/bja/69.4.341. [DOI] [PubMed] [Google Scholar]
  36. Kloosterman T., von Blomberg B. M., Borgstein P., Cuesta M. A., Scheper R. J., Meijer S. Unimpaired immune functions after laparoscopic cholecystectomy. Surgery. 1994 Apr;115(4):424–428. [PubMed] [Google Scholar]
  37. Lennard T. W., Shenton B. K., Borzotta A., Donnelly P. K., White M., Gerrie L. M., Proud G., Taylor R. M. The influence of surgical operations on components of the human immune system. Br J Surg. 1985 Oct;72(10):771–776. doi: 10.1002/bjs.1800721002. [DOI] [PubMed] [Google Scholar]
  38. Little D., Regan M., Keane R. M., Bouchier-Hayes D. Perioperative immune modulation. Surgery. 1993 Jul;114(1):87–91. [PubMed] [Google Scholar]
  39. Mahiout A., Brunkhorst R. Pyruvate anions neutralize peritoneal dialysate cytotoxicity. Nephrol Dial Transplant. 1995;10(3):391–394. [PubMed] [Google Scholar]
  40. Maruszynski M., Pojda Z. Interleukin 6 (IL-6) levels in the monitoring of surgical trauma. A comparison of serum IL-6 concentrations in patients treated by cholecystectomy via laparotomy or laparoscopy. Surg Endosc. 1995 Aug;9(8):882–885. doi: 10.1007/BF00768883. [DOI] [PubMed] [Google Scholar]
  41. McMahon A. J., O'Dwyer P. J., Cruikshank A. M., McMillan D. C., O'Reilly D. S., Lowe G. D., Rumley A., Logan R. W., Baxter J. N. Comparison of metabolic responses to laparoscopic and minilaparotomy cholecystectomy. Br J Surg. 1993 Oct;80(10):1255–1258. doi: 10.1002/bjs.1800801011. [DOI] [PubMed] [Google Scholar]
  42. Mealy K., Gallagher H., Barry M., Lennon F., Traynor O., Hyland J. Physiological and metabolic responses to open and laparoscopic cholecystectomy. Br J Surg. 1992 Oct;79(10):1061–1064. doi: 10.1002/bjs.1800791024. [DOI] [PubMed] [Google Scholar]
  43. O'Rourke N., Price P. M., Kelly S., Sikora K. Tumour inoculation during laparoscopy. Lancet. 1993 Aug 7;342(8867):368–368. [PubMed] [Google Scholar]
  44. O'Sullivan G. C., Murphy D., O'Brien M. G., Ireland A. Laparoscopic management of generalized peritonitis due to perforated colonic diverticula. Am J Surg. 1996 Apr;171(4):432–434. doi: 10.1016/S0002-9610(97)89625-0. [DOI] [PubMed] [Google Scholar]
  45. Ohzato H., Yoshizaki K., Nishimoto N., Ogata A., Tagoh H., Monden M., Gotoh M., Kishimoto T., Mori T. Interleukin-6 as a new indicator of inflammatory status: detection of serum levels of interleukin-6 and C-reactive protein after surgery. Surgery. 1992 Feb;111(2):201–209. [PubMed] [Google Scholar]
  46. Ortega A. E., Tang E., Froes E. T., Asensio J. A., Katkhouda N., Demetriades D. Laparoscopic evaluation of penetrating thoracoabdominal traumatic injuries. Surg Endosc. 1996 Jan;10(1):19–22. doi: 10.1007/s004649910003. [DOI] [PubMed] [Google Scholar]
  47. Paraskevopoulos J. A., Pechlivanides G. Parietal seeding of carcinoma of the gallbladder after laparoscopic cholecystectomy. Br J Surg. 1992 Aug;79(8):845–845. doi: 10.1002/bjs.1800790854. [DOI] [PubMed] [Google Scholar]
  48. Parry-Billings M., Baigrie R. J., Lamont P. M., Morris P. J., Newsholme E. A. Effects of major and minor surgery on plasma glutamine and cytokine levels. Arch Surg. 1992 Oct;127(10):1237–1240. doi: 10.1001/archsurg.1992.01420100099017. [DOI] [PubMed] [Google Scholar]
  49. Perlmutter D. H., Dinarello C. A., Punsal P. I., Colten H. R. Cachectin/tumor necrosis factor regulates hepatic acute-phase gene expression. J Clin Invest. 1986 Nov;78(5):1349–1354. doi: 10.1172/JCI112721. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Pezet D., Fondrinier E., Rotman N., Guy L., Lemesle P., Lointier P., Chipponi J. Parietal seeding of carcinoma of the gallbladder after laparoscopic cholecystectomy. Br J Surg. 1992 Mar;79(3):230–230. doi: 10.1002/bjs.1800790313. [DOI] [PubMed] [Google Scholar]
  51. Pullicino E. A., Carli F., Poole S., Rafferty B., Malik S. T., Elia M. The relationship between the circulating concentrations of interleukin 6 (IL-6), tumor necrosis factor (TNF) and the acute phase response to elective surgery and accidental injury. Lymphokine Res. 1990 Summer;9(2):231–238. [PubMed] [Google Scholar]
  52. Redmond H. P., Watson R. W., Houghton T., Condron C., Watson R. G., Bouchier-Hayes D. Immune function in patients undergoing open vs laparoscopic cholecystectomy. Arch Surg. 1994 Dec;129(12):1240–1246. doi: 10.1001/archsurg.1994.01420360030003. [DOI] [PubMed] [Google Scholar]
  53. Roumen R. M., van Meurs P. A., Kuypers H. H., Kraak W. A., Sauerwein R. W. Serum interleukin-6 and C reactive protein responses in patients after laparoscopic or conventional cholecystectomy. Eur J Surg. 1992 Oct;158(10):541–544. [PubMed] [Google Scholar]
  54. Sandoval B. A., Robinson A. V., Sulaiman T. T., Shenk R. R., Stellato T. A. Open versus laparoscopic surgery: a comparison of natural antitumoral cellular immunity in a small animal model. Am Surg. 1996 Aug;62(8):625–631. [PubMed] [Google Scholar]
  55. Sawyers J. L. Current status of conventional (open) cholecystectomy versus laparoscopic cholecystectomy. Ann Surg. 1996 Jan;223(1):1–3. doi: 10.1097/00000658-199601000-00001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Slade M. S., Simmons R. L., Yunis E., Greenberg L. J. Immunodepression after major surgery in normal patients. Surgery. 1975 Sep;78(3):363–372. [PubMed] [Google Scholar]
  57. Sunderland G. T., Chisholm E. M., Lau W. Y., Chung S. C., Li A. K. Laparoscopic repair of perforated peptic ulcer. Br J Surg. 1992 Aug;79(8):785–785. doi: 10.1002/bjs.1800790825. [DOI] [PubMed] [Google Scholar]
  58. Tanaka J., Kato Y., Umezawa A., Koyama K. Laparoscopic management of percutaneous transhepatic biliary drainage catheter dislodgement accompanied by bile peritonitis. J Am Coll Surg. 1994 Oct;179(4):480–482. [PubMed] [Google Scholar]
  59. Travis J. Structure, function, and control of neutrophil proteinases. Am J Med. 1988 Jun 24;84(6A):37–42. doi: 10.1016/0002-9343(88)90156-8. [DOI] [PubMed] [Google Scholar]
  60. Trokel M. J., Bessler M., Treat M. R., Whelan R. L., Nowygrod R. Preservation of immune response after laparoscopy. Surg Endosc. 1994 Dec;8(12):1385–1388. doi: 10.1007/BF00187341. [DOI] [PubMed] [Google Scholar]
  61. Vallina V. L., Velasco J. M. The influence of laparoscopy on lymphocyte subpopulations in the surgical patient. Surg Endosc. 1996 May;10(5):481–484. doi: 10.1007/BF00188390. [DOI] [PubMed] [Google Scholar]
  62. Vander Velpen G., Penninckx F., Kerremans R., Van Damme J., Arnout J. Interleukin-6 and coagulation-fibrinolysis fluctuations after laparoscopic and conventional cholecystectomy. Surg Endosc. 1994 Oct;8(10):1216–1220. doi: 10.1007/BF00591054. [DOI] [PubMed] [Google Scholar]
  63. Watson R. W., Redmond H. P., McCarthy J., Burke P. E., Bouchier-Hayes D. Exposure of the peritoneal cavity to air regulates early inflammatory responses to surgery in a murine model. Br J Surg. 1995 Aug;82(8):1060–1065. doi: 10.1002/bjs.1800820820. [DOI] [PubMed] [Google Scholar]
  64. West M. A., Baker J., Bellingham J. Kinetics of decreased LPS-stimulated cytokine release by macrophages exposed to CO2. J Surg Res. 1996 Jun;63(1):269–274. doi: 10.1006/jsre.1996.0259. [DOI] [PubMed] [Google Scholar]
  65. Wexner S. D., Cohen S. M. Port site metastases after laparoscopic colorectal surgery for cure of malignancy. Br J Surg. 1995 Mar;82(3):295–298. doi: 10.1002/bjs.1800820305. [DOI] [PubMed] [Google Scholar]

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