Skip to main content

Advertisement

Log in

Improved abdominal wall wound healing by helium pneumoperitoneum

  • Original Article
  • Published:
Surgical Endoscopy And Other Interventional Techniques Aims and scope Submit manuscript

Abstract

Background

Despite widespread use of the endoscopic technique in the treatment of inguinal and incisional hernias, knowledge about its impact on abdominal wall wound healing is rare. Questions remain regarding the risk of port-site hernias and hernia recurrence. The current study investigated the gas-dependent effects of pneumoperitoneum on laparotomy wound healing.

Methods

Laparotomy was performed in 54 male Sprague–Dawley rats. A carbon dioxide (n = 18) or helium (n = 18) pneumoperitoneum of 3 mmHg was maintained before and after laparotomy, with an overall duration of 30 min. The rats in the control group (n = 18) received no pneumoperitoneum. The animals were killed after 5 and 10 days, and the abdominal wall was explanted for subsequent histopathologic examinations of the laparotomy wound. The granuloma formation in hematoxylin and eosin–stained sections was analyzed. Infiltration of macrophages (CD68) and expression of matrix metalloproteinases (MMP-8 and MMP-13) were examined by immunohistochemistry. The collagen type 1 to type 3 ratio was investigated by cross-polarization microscopy after Sirius Red staining.

Results

After 5 and 10 days, the percentages of CD68-positive cells, granuloma formation, and expression of MMP-8 did not differ between the groups. In contrast, after both 5 and 10 days, the expression of MMP-13 and the collagen 1 to 3 ratio were significantly higher after helium pneumoperitoneum than in the control animals.

Conclusions

The results suggest that helium pneumoperitoneum may ameliorate wound healing within the abdominal wall and could therefore represent a beneficial gas for endoscopic hernia repair.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. LeBlanc KA (2005) Incisional hernia repair: laparoscopic techniques. World J Surg 29: 1073–1079

    Article  PubMed  Google Scholar 

  2. Bay-Nielsen M, Kehlet H, Strand L, Malmstrom J, Andersen FH, Wara P, Juul P, Callesen T (2001) Quality assessment of 26,304 herniorrhaphies in Denmark: a prospective nationwide study. Lancet 358: 1124–1128

    Article  PubMed  CAS  Google Scholar 

  3. Cohen RV, Alvarez G, Roll S, Garcia ME, Kawahara N, Schiavon CA, Schaffa TD, Pereira PR, Margarido NF, Rodrigues AJ (1998) Transabdominal or totally extraperitoneal laparoscopic hernia repair? Surg Laparosc Endosc 8: 264–268

    Article  PubMed  CAS  Google Scholar 

  4. Si Z, Rhanjit B, Rosch R, Rene PM, Klosterhalfen B, Klinge U (2002) Impaired balance of type I and type III procollagen mRNA in cultured fibroblasts of patients with incisional hernia. Surgery 131: 324–331

    Article  PubMed  Google Scholar 

  5. Zheng H, Si Z, Kasperk R, Bhardwaj RS, Schumpelick V, Klinge U, Klosterhalfen B (2002) Recurrent inguinal hernia: disease of the collagen matrix? World J Surg 26: 401–408

    Article  PubMed  Google Scholar 

  6. Junge K, Klinge U, Rosch R, Mertens PR, Kirch J, Klosterhalfen B, Lynen P, Schumpelick V (2004) Decreased collagen type I/III ratio in patients with recurring hernia after implantation of alloplastic prostheses. Langenbecks Arch Surg 389: 17–22

    Article  PubMed  Google Scholar 

  7. Klinge U, Si ZY, Zheng H, Schumpelick V, Bhardwaj RS, Klosterhalfen B (2001) Collagen I/III and matrix metalloproteinases (MMP) 1 and 13 in the fascia of patients with incisional hernias. J Invest Surg 14: 47–54

    Article  PubMed  CAS  Google Scholar 

  8. Klinge U, Si ZY, Zheng H, Schumpelick V, Bhardwaj RS, Klosterhalfen B (2000) Abnormal collagen I to III distribution in the skin of patients with incisional hernia. Eur Surg Res 32: 43–48

    Article  PubMed  CAS  Google Scholar 

  9. Agalar F, Hamaloglu E, Daphan C, Tarim A, Onur R, Renda N, Sayek I (2000) Effects of CO2 insufflation and laparotomy on wound healing in mice. Aust N Z J Surg 70: 739–742

    Article  PubMed  CAS  Google Scholar 

  10. Murray JA, Cornwell EE, III, Velmahos GC, Rivkind AI, Hedman T, Abrahams JH, Katkhouda N, Berne TV, Demetriades D (2001) Healing of traumatic diaphragm injuries: comparison of laparoscopic versus open techniques in an animal model. J Surg Res 100: 189–191

    Article  PubMed  CAS  Google Scholar 

  11. Wickens JC, Whelan RL, Allendorf JD, Donahue J, Buxton E, McKee A, Panageas K, Gleason N, Lee S, Bessler M (1998) Wound tensile strength and contraction rate are not affected by laparotomy or pneumoperitoneum. Surg Endosc 12: 1166–1170

    Article  PubMed  CAS  Google Scholar 

  12. Robbins SB, Pofahl WE, Gonzalez RP (2001) Laparoscopic ventral hernia repair reduces wound complications. Am Surg 67: 896–900

    PubMed  CAS  Google Scholar 

  13. Ikechebelu JI, Obi RA, Udigwe GO, Joe-Ikechebelu NN (2005) Comparison of carbon dioxide and room air pneumoperitoneum for day-case diagnostic laparoscopy. J Obstet Gynaecol 25: 172–173

    Article  PubMed  CAS  Google Scholar 

  14. Kollmorgen CF, Thompson GB, Grant CS, van Heerden JA, Byrne J, Davies ET, Donohue JH, Ilstrup DM, Young WF (1998) Laparoscopic versus open posterior adrenalectomy: comparison of acute-phase response and wound healing in the cushingoid porcine model. World J Surg 22: 613–619

    Article  PubMed  CAS  Google Scholar 

  15. Gutt CN, Kuntz C, Schmandra T, Wunsch A, Heinz P, Bouvy N, Bessler M, Sanger P, Bonjer J, Allendorf J, Jacobi CA, Whelan R (1998) Metabolism and immunology in laparoscopy: first workshop on experimental laparoscopic surgery, Frankfurt, 1997. Surg Endosc 12: 1096–1098

    Article  PubMed  CAS  Google Scholar 

  16. 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: 1059–1064

    Article  PubMed  CAS  Google Scholar 

  17. 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: 1135–1138

    Article  PubMed  CAS  Google Scholar 

  18. Jacobi CA, Ordemann J, Halle E, Volk HD, Muller JM (1999) Impact of laparoscopy with carbon dioxide versus helium on local and systemic inflammation in an animal model of peritonitis. J Laparoendosc Adv Surg Tech A 9: 305–312

    Article  PubMed  CAS  Google Scholar 

  19. Wildbrett P, Oh A, Naundorf D, Volk T, Jacobi CA (2003) Impact of laparoscopic gases on peritoneal microenvironment and essential parameters of cell function. Surg Endosc 17: 78–82

    Article  PubMed  CAS  Google Scholar 

  20. Rosch R, Stumpf M, Junge K, Ardic D, Ulmer F, Schumpelick V (2004) Impact of pressure and gas type on anastomotic wound healing in rats. Langenbecks Arch Surg 389: 261–266

    Article  PubMed  Google Scholar 

  21. Portera CA, Love EJ, Memore L, Zhang L, Muller A, Browder W, Williams DL (1997) Effect of macrophage stimulation on collagen biosynthesis in the healing wound. Am Surg 63: 125–131

    PubMed  CAS  Google Scholar 

  22. Browder W, Williams D, Lucore P, Pretus H, Jones E, McNamee R (1988) Effect of enhanced macrophage function on early wound healing. Surgery 104: 224–230

    PubMed  CAS  Google Scholar 

  23. Eljaafari A, Duperrier K, Mazet S, Bardin C, Bernaud J, Durand B, Gebuhrer L, Betuel H, Rigal D (1998) Generation of stable monocyte-derived dendritic cells in the presence of high concentrations of homologous or autologous serum: influence of extracellular pH. Hum Immunol 59: 625–634

    Article  PubMed  CAS  Google Scholar 

  24. Kuntz C, Wunsch A, Bodeker C, Bay F, Rosch R, Windeler J, Herfarth C (2000) Effect of pressure and gas type on intraabdominal, subcutaneous, and blood pH in laparoscopy. Surg Endosc 14: 367–371

    Article  PubMed  CAS  Google Scholar 

  25. Jackson PG Evans SR (2000) Intraperitoneal macrophages and tumor immunity: a review. J Surg Oncol 75: 146–154

    Article  Google Scholar 

  26. Gutt CN, Heinz P, Kaps W, Paolucci V (1997) The phagocytosis activity during conventional and laparoscopic operations in the rat: a preliminary study. Surg Endosc 11: 899–901

    Article  PubMed  CAS  Google Scholar 

  27. Neuhaus SJ, Watson DI, Ellis T, Lafullarde T, Jamieson GG, Russell WJ (2001) Metabolic and immunologic consequences of laparoscopy with helium or carbon dioxide insufflation: a randomized clinical study. ANZ J Surg 71: 447–452

    Article  PubMed  CAS  Google Scholar 

  28. Wood GC, Keech MK (1960) The formation of fibrils from collagen solutions. 1. The effect of experimental conditions: kinetic and electron-microscope studies. Biochem J 75: 588–598

    PubMed  CAS  Google Scholar 

  29. Vanamee P, Porter KR (1951) Observations with the electron microscope on the solvation and reconstitution of collagen. J Exp Med 94: 255–266

    Article  PubMed  CAS  Google Scholar 

  30. Nigra TP, Martin GR, Eagle H (1973) The effect of environmental pH on collagen synthesis by cultured cells. Biochem Biophys Res Commun 53: 272–281

    Article  PubMed  CAS  Google Scholar 

  31. Bard JB, Hulmes DJ, Purdom IF, Ross AS (1993) Chick corneal development in vitro: diverse effects of pH on collagen assembly. J Cell Sci 105: 1045–1055

    PubMed  CAS  Google Scholar 

  32. Lopez-Rivera E, Lizarbe TR, Martinez-Moreno M, Lopez-Novoa JM, Rodriguez-Barbero A, Rodrigo J, Fernandez AP, Alvarez-Barrientos A, Lamas S, Zaragoza C (2005) Matrix metalloproteinase 13 mediates nitric oxide activation of endothelial cell migration. Proc Natl Acad Sci U S A 102: 3685–3690

    Article  PubMed  CAS  Google Scholar 

  33. Armstrong DG Jude EB (2002) The role of matrix metalloproteinases in wound healing. J Am Podiatr Med Assoc 92: 12–18

    Google Scholar 

  34. Nwomeh BC, Liang HX, Diegelmann RF, Cohen IK, Yager DR (1998) Dynamics of the matrix metalloproteinases MMP-1 and MMP-8 in acute open human dermal wounds. Wound Repair Regen 6: 127–134

    Article  PubMed  CAS  Google Scholar 

  35. Wu N, Jansen ED, Davidson JM (2003) Comparison of mouse matrix metalloproteinase 13 expression in free-electron laser and scalpel incisions during wound healing. J Invest Dermatol 121: 926–932

    Article  PubMed  CAS  Google Scholar 

  36. Paraskeva PA, Ridgway PF, Jones T, Smith A, Peck DH, Darzi AW (2005) Laparoscopic environmental changes during surgery enhance the invasive potential of tumours. Tumour Biol 26: 94–102

    Article  PubMed  CAS  Google Scholar 

  37. Vaalamo M, Mattila L, Johansson N, Kariniemi AL, Karjalainen-Lindsberg ML, Kahari VM, Saarialho-Kere U (1997) Distinct populations of stromal cells express collagenase-3 (MMP-13) and collagenase-1 (MMP-1) in chronic ulcers but not in normally healing wounds. J Invest Dermatol 109: 96–101

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank the Karl Storz GmbH, Germany for the kind disposal of an insufflator modified for helium gas, and Mrs. Ellen Krott for careful assistance during this investigation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to R. Rosch.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rosch, R., Junge, K., Binnebösel, M. et al. Improved abdominal wall wound healing by helium pneumoperitoneum. Surg Endosc 20, 1892–1896 (2006). https://doi.org/10.1007/s00464-005-0816-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00464-005-0816-z

Keywords

Navigation