Top

Published in:

01-06-2017 | ORIGINAL ARTICLE

Advantages of laparoscopic compared to conventional surgery are not related to an innate immune response of peritoneal immune activation: an animal study in rats

Authors: Philipp Lingohr, Jonas Dohmen, Hanno Matthaei, Timo Schwandt, Kathy Stein, Gun-Soo Hong, Julia Steitz, Thomas Longerich, Edwin Bölke, Sven Wehner, Jörg C. Kalff

Published in: Langenbeck's Archives of Surgery | Issue 4/2017

Abstract

Purpose

Laparoscopic surgery (LS) has proved superior compared to conventional surgery (CS) regarding morbidity, length of hospital stay, rate of wound infection and time until recovery. An improved preservation of the postoperative immune function is assumed to contribute to these benefits though the role of the local peritoneal immune response is still poorly understood. Our study investigates the peritoneal immune response subsequent to abdominal surgery and compares it between laparoscopic and conventional surgery to find an immunological explanation for the clinically proven benefits of LS.

Methods

Wistar rats (N = 140) underwent laparoscopic cecum resection (LCR; N = 28), conventional cecum resection (CCR; N = 28), laparoscopic sham operation (LSO; N = 28), conventional sham operation (CSO; N = 28), or no surgical treatment (CTRL; N = 28). Postoperatively, peritoneal lavages were performed, leukocytes isolated and analyzed regarding immune function and phagocytosis activity.

Results

Immune function was inhibited postoperatively in animals undergoing LCR or CCR compared to CTRL reflected by a lower TNF-α (CTRL 3956.65 pg/ml, LCR 2018.48 pg/ml (p = 0.023), CCR 2793.78 pg/ml (n.s.)) and IL-6 secretion (CTRL 625.84 pg/ml, LCR 142.84 pg/ml (p = 0.009), CCR 169.53 pg/ml (p = 0.01)). Phagocytosis was not affected in rats undergoing any kind of surgery compared to CTRL. Neither cytokine secretion nor phagocytosis activity differed significantly between laparoscopic and conventional surgery.

Conclusions

According to our findings the benefits associated with LS compared to CS cannot be explained by differences in the postoperative peritoneal innate immune response. Further studies are needed to elucidate the causes for a more favorable postoperative outcome in patients after LS compared to CS.

Available only for authorised users

Tiwari MM, Reynoso JF, Tsang AW, Oleynikov D (2011) Comparison of outcomes of laparoscopic and open appendectomy in management of uncomplicated and complicated appendicitis. Ann Surg 254(6):927–932. doi:10.1097/SLA.0b013e31822aa8ea CrossRefPubMed

Guller U, Hervey S, Purves H, Muhlbaier LH, Peterson ED, Eubanks S, Pietrobon R (2004) Laparoscopic versus open appendectomy: outcomes comparison based on a large administrative database. Ann Surg 239(1):43CrossRefPubMedPubMedCentral

Sauerland S, Jaschinski T, Neugebauer EA (2010) Laparoscopic versus open surgery for suspected appendicitis. Cochrane Database Syst Rev 10:CD001546. doi:10.1002/14651858.CD001546.pub3

Pedersen AG, Petersen OB, Wara P, Ronning H, Qvist N, Laurberg S (2001) Randomized clinical trial of laparoscopic versus open appendicectomy. Br J Surg 88(2):200–205. doi:10.1046/j.1365-2168.2001.01652.x CrossRefPubMed

Poon JT, Law W-L, Wong IW, Ching PT, Wong LM, Fan JK, Lo OS (2009) Impact of laparoscopic colorectal resection on surgical site infection. Ann Surg 249(1):77–81CrossRefPubMed

Gupta A, Watson DI (2001) Effect of laparoscopy on immune function. Br J Surg 88(10):1296–1306. doi:10.1046/j.0007-1323.2001.01860.x CrossRefPubMed

Huang SG, Li YP, Zhang Q, Redmond HP, Wang JH, Wang J (2013) Laparotomy and laparoscopy diversely affect macrophage-associated antimicrobial activity in a murine model. BMC Immunol 14:27. doi:10.1186/1471-2172-14-27 CrossRefPubMedPubMedCentral

Jesch NK, Kuebler JF, Nguyen H, Nave H, Bottlaender M, Teichmann B, Braun A, Vieten G, Ure BM (2006) Laparoscopy vs minilaparotomy and full laparotomy preserves circulatory but not peritoneal and pulmonary immune responses. J Pediatr Surg 41(6):1085–1092. doi:10.1016/j.jpedsurg.2006.02.002 CrossRefPubMed

Moehrlen U, Ziegler U, Boneberg E, Reichmann E, Gitzelmann CA, Meuli M, Hamacher J (2006) Impact of carbon dioxide versus air pneumoperitoneum on peritoneal cell migration and cell fate. Surg Endosc 20(10):1607–1613. doi:10.1007/s00464-005-0775-4 CrossRefPubMed

10.

Lee SW, Whelan RL (2006) Immunologic and oncologic implications of laparoscopic surgery: what is the latest? Clin Colon Rectal Surg 19(1):5–12CrossRefPubMedPubMedCentral

11.

Grieco MJ, Whelan RL (2011) Laparoscopy and Immunology. In: Minimally Invasive Surgical Oncology. Springer, pp 69–82

12.

Luster AD, Alon R, von Andrian UH (2005) Immune cell migration in inflammation: present and future therapeutic targets. Nat Immunol 6(12):1182–1190 doi:http://www.nature.com/ni/journal/v6/n12/suppinfo/ni1275_S1.html CrossRefPubMed

13.

Kolaczkowska E, Kubes P (2013) Neutrophil recruitment and function in health and inflammation. Nat Rev Immunol 13(3):159–175. doi:10.1038/nri3399 CrossRefPubMed

14.

Rothenberg ME, Hogan SP (2006) The eosinophil. Annu Rev Immunol 24:147–174. doi:10.1146/annurev.immunol.24.021605.090720 CrossRefPubMed

15.

Yousefi S, Gold JA, Andina N, Lee JJ, Kelly AM, Kozlowski E, Schmid I, Straumann A, Reichenbach J, Gleich GJ, Simon HU (2008) Catapult-like release of mitochondrial DNA by eosinophils contributes to antibacterial defense. Nat Med 14(9):949–953. doi:10.1038/nm.1855 CrossRefPubMed

16.

Shi C, Pamer EG (2011) Monocyte recruitment during infection and inflammation. Nat Rev Immunol 11(11):762–774. doi:10.1038/nri3070 CrossRefPubMedPubMedCentral

17.

Murray PJ, Wynn TA (2011) Protective and pathogenic functions of macrophage subsets. Nat Rev Immunol 11(11):723–737. doi:10.1038/nri3073 CrossRefPubMedPubMedCentral

18.

Jackson PG, Evans SRT (2000) Intraperitoneal macrophages and tumor immunity: a review. J Surg Oncol 75(2):146–154. doi:10.1002/1096-9098(200010)75:2<146::aid-jso14>3.0.co;2-1 CrossRefPubMed

19.

Sido B, Teklote J-R, Hartel M, Friess H, Büchler MW (2004) Inflammatory response after abdominal surgery. Best Pract Res Clin Anaesthesiol 18(3):439–454. doi:10.1016/j.bpa.2003.12.006 CrossRefPubMed

20.

Redmond H, Hofmann K, Shou J, Leon P, Kelly C, Daly J (1992) Effects of laparotomy on systemic macrophage function. Surgery 111(6):647–655PubMed

21.

Badia J, Whawell S, Scott-Coombes D, Abel P, Williamson R, Thompson J (1996) Peritoneal and systemic cytokine response to laparotomy. Br J Surg 83(3):347–348CrossRefPubMed

22.

Lee SW, Feingold DL, Carter JJ, Zhai C, Stapleton G, Gleason N, Whelan RL (2003) Peritoneal macrophage and blood monocyte functions after open and laparoscopic-assisted cecectomy in rats. Surg Endosc 17(12):1996–2002. doi:10.1007/s00464-003-8154-5 CrossRefPubMed

23.

Lingohr P, Dohmen J, Matthaei H, Schwandt T, Hong GS, Konieczny N, Bolke E, Wehner S, Kalff JC (2014) Development of a standardized laparoscopic caecum resection model to simulate laparoscopic appendectomy in rats. Eur J Med Res 19:33CrossRefPubMedPubMedCentral

24.

Using Stata to deal with violations of the homogeneity of variance assumption in ANOVA UCLA: Statistical Consulting Group. http://www.ats.ucla.edu/stat/stata/library/homvar.htm. Accessed 03 December 2014

25.

Papke LE, Wooldridge JM (1996) Econometric methods for fractional response variables with an application to 401 (K) plan participation rates. J Appl Econ 11(6):619–632CrossRef

26.

Robinson AP, White TM, Mason DW (1986) Macrophage heterogeneity in the rat as delineated by two monoclonal antibodies MRC OX-41 and MRC OX-42, the latter recognizing complement receptor type 3. Immunology 57(2):239–247PubMedPubMedCentral

27.

Grau V, Scriba A, Stehling O, Steiniger B (2000) Monocytes in the rat. Immunobiology 202(1):94–103. doi:10.1016/S0171-2985(00)80056-X CrossRefPubMed

28.

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 (2003) Postoperative cell mediated immune response is better preserved after laparoscopic vs open colorectal resection in humans. Surg Endosc 17(6):972–978CrossRefPubMed

29.

Brokelman WJ, Lensvelt M, Borel Rinkes IH, Klinkenbijl JH, Reijnen MM (2011) Peritoneal changes due to laparoscopic surgery. Surg Endosc 25(1):1–9. doi:10.1007/s00464-010-1139-2 CrossRefPubMed

30.

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(3):233–235CrossRefPubMed

31.

Gitzelmann CA, Mendoza-Sagaon M, Talamini MA, Ahmad SA, Pegoli W Jr, Paidas CN (2000) Cell-mediated immune response is better preserved by laparoscopy than laparotomy. Surgery 127(1):65–71

32.

Redmond HP, Watson RW, Houghton T, Condron C, Watson RG, Bouchier-Hayes D (1994) Immune function in patients undergoing open vs laparoscopic cholecystectomy. Arch Surg 129(12):1240–1246CrossRefPubMed

33.

Sylla P, Kirman I, Whelan RL (2005) Immunological advantages of advanced laparoscopy. Surg Clin North Am 85(1):1–18 viiCrossRefPubMed

34.

Cassatella MA, Locati M, Mantovani A (2009) Never underestimate the power of a neutrophil. Immunity 31(5):698–700. doi:10.1016/j.immuni.2009.10.003 CrossRefPubMed

35.

Akuthota P, Wang HB, Spencer LA, Weller PF (2008) Immunoregulatory roles of eosinophils: a new look at a familiar cell. Clinical & Experimental Allergy 38(8):1254–1263. doi:10.1111/j.1365-2222.2008.03037.x CrossRef

36.

Kita H (2011) Eosinophils: multifaceted biological properties and roles in health and disease. Immunol Rev 242(1):161–177. doi:10.1111/j.1600-065X.2011.01026.x CrossRefPubMedPubMedCentral

37.

Nathan C (2006) Neutrophils and immunity: challenges and opportunities. Nat Rev Immunol 6(3):173–182 doi:http://www.nature.com/nri/journal/v6/n3/suppinfo/nri1785_S1.html CrossRefPubMed

38.

Ure BM, Niewold TA, Bax NM, Ham M, van der Zee DC, Essen GJ (2002) Peritoneal, systemic, and distant organ inflammatory responses are reduced by a laparoscopic approach and carbon dioxide versus air. Surg Endosc 16(5):836–842CrossRefPubMed

39.

Iwanaka T, Arkovitz MS, Arya G, Ziegler MM (1997) Evaluation of operative stress and peritoneal macrophage function in minimally invasive operations. J Am Coll Surg 184(4):357–363PubMed

40.

Moehrlen U, Schwoebel F, Reichmann E, Stauffer U, Gitzelmann CA, Hamacher J (2005) Early peritoneal macrophage function after laparoscopic surgery compared with laparotomy in a mouse mode. Surg Endosc 19(7):958–963. doi:10.1007/s00464-004-2118-2 CrossRefPubMed

41.

Collet D, Vitale GC, Reynolds M, Klar E, Cheadle WG (1995) Peritoneal host defenses are less impaired by laparoscopy than by open operation. Surg Endosc 9(10):1059–1064. doi:10.1007/bf00188987 CrossRefPubMed

42.

Watson RW, Redmond HP, McCarthy J, Burke PE, Bouchier-Hayes D (1995) Exposure of the peritoneal cavity to air regulates early inflammatory responses to surgery in a murine model. Br J Surg 82(8):1060–1065CrossRefPubMed

43.

Hajri A, Mutter D, Wack S, Bastien C, Gury JF, Marescaux J, Aprahamian M (2000) Dual effect of laparoscopy on cell-mediated immunity. Eur Surg Res 32(5):261–266CrossRefPubMed

44.

Novitsky YW, Czerniach DR, Kaban GK, Bergner A, Gallagher KA, Perugini RA, Litwin DE (2006) Immunologic effects of hand-assisted surgery on peritoneal macrophages: comparison to open and standard laparoscopic approaches. Surgery 139(1):39–45CrossRefPubMed

45.

Balague C, Targarona EM, Pujol M, Filella X, Espert JJ, Trias M (1999) Peritoneal response to a septic challenge. Comparison between open laparotomy, pneumoperitoneum laparoscopy, and wall lift laparoscopy. Surg Endosc 13(8):792–796CrossRefPubMed

46.

Sare M, Yesilada O, Gurel M, Balkaya M, Yologlu S, Fiskin K (1997) Effects of CO2 insufflation on bacterial growth in rats with Escherichia Coli-induced experimental peritonitis. Surg Laparosc Endosc 7(1):38–41CrossRefPubMed

47.

Chekan EG, Nataraj C, Clary EM, Hayward TZ, Brody FJ, Stamat JC, Fina MC, Eubanks WS, Westcott CJ (1999) Intraperitoneal immunity and pneumoperitoneum. Surg Endosc 13(11):1135–1138CrossRefPubMed

48.

Novitsky YW, Litwin DE, Callery MP (2004) The net immunologic advantage of laparoscopic surgery. Surg Endosc 18(10):1411–1419. doi:10.1007/s00464-003-8275-x CrossRefPubMed

49.

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. Aust N Z J Surg 69(1):14–18CrossRefPubMed

50.

Neuhaus SJ, Watson DI, Ellis T, Rofe AM, Mathew G, Jamieson GG (2000) Influence of gases on intraperitoneal immunity during laparoscopy in tumor-bearing rats. World J Surg 24(10):1227–1231CrossRefPubMed

51.

Neuhaus SJ, Watson DI (2004) Pneumoperitoneum and peritoneal surface changes: a review. Surg Endosc 18(9):1316–1322. doi:10.1007/s00464-003-8238-2 CrossRefPubMed

52.

Kuntz C, Wunsch A, Bay F, Windeler J, Glaser F, Herfarth C (1998) Prospective randomized study of stress and immune response after laparoscopic vs conventional colonic resection. Surg Endosc 12(7):963–967CrossRefPubMed

53.

Trokel M, Bessler M, Treat M, Whelan R, Nowygrod R (1994) Preservation of immune response after laparoscopy. Surg Endosc 8(12):1385–1388CrossRefPubMed

54.

Wehner S, Vilz TO, Stoffels B, Kalff JC (2012) Immune mediators of postoperative ileus. Langenbeck’s Arch Surg 397(4):591–601. doi:10.1007/s00423-012-0915-y CrossRef

Title: Advantages of laparoscopic compared to conventional surgery are not related to an innate immune response of peritoneal immune activation: an animal study in rats
Authors: Philipp Lingohr
Jonas Dohmen
Hanno Matthaei
Timo Schwandt
Kathy Stein
Gun-Soo Hong
Julia Steitz
Thomas Longerich
Edwin Bölke
Sven Wehner
Jörg C. Kalff
Publication date: 01-06-2017
Publisher: Springer Berlin Heidelberg
Published in: Langenbeck's Archives of Surgery / Issue 4/2017
Print ISSN: 1435-2443
Electronic ISSN: 1435-2451
DOI: https://doi.org/10.1007/s00423-016-1521-1

At a glance: The STEP trials

Springer Medicine

Advantages of laparoscopic compared to conventional surgery are not related to an innate immune response of peritoneal immune activation: an animal study in rats

Abstract

Purpose

Methods

Results

Conclusions

At a glance: The STEP trials

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 4/2017

EMG changes during continuous intraoperative neuromonitoring with sustained recurrent laryngeal nerve traction in a porcine model

Experiences with surgically treated primary or secondary hepatic sarcoma

Risk-adjusted treatment selection and outcome of patients with acute cholecystitis

Quantification of fluorescence angiography in a porcine model

Effective downsizing but enhanced intratumoral heterogeneity following neoadjuvant sorafenib in patients with non-metastatic renal cell carcinoma

Training or non-surgical factors—what determines a good surgical performance? A randomised controlled trial