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Published in: Surgical Endoscopy 10/2006

01-10-2006

Impact of carbon dioxide versus air pneumoperitoneum on peritoneal cell migration and cell fate

Authors: U. Moehrlen, U. Ziegler, E. Boneberg, E. Reichmann, C. A. Gitzelmann, M. Meuli, J. Hamacher

Published in: Surgical Endoscopy | Issue 10/2006

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Abstract

Background

Postoperative systemic immune function is suppressed after open abdominal surgery, as compared with that after minimally invasive abdominal surgery. As a first line of defense, peritoneal macrophages (PMo) and polymorphonuclear neutrophil granulocytes (PMNs) are of primary importance in protecting the body from microorganisms. Previous studies have shown changes in these cell populations over time after open versus laparoscopic surgery. This study aimed to investigate the dynamics of cell recruitment and clearance of peritoneal cells.

Methods

Female NMRI mice (33 ± 2 g) were randomly assigned to carbon dioxide (CO2) or air insufflation. Intravasal cells with phagocytic capabilities were selectively stained by intravenous injection of the fluorescent dye PKH26 24 h before surgery. Gas was insufflated into the peritoneal cavity through a catheter, and the pneumoperitoneum was maintained for 30 min. Peritoneal lavage was performed 1, 3, 8, or 24 h after surgery. Apoptotic cells were assessed by flow cytometry using a general caspase substrate.

Results

The total peritoneal cell count did not differ between groups. The PKH26-positive PMo level was significantly increased after CO2, as compared with air, at 1 h and 24 h. The ratio of apoptotic PMo did not differ between the groups. In the peritoneal lavage, polymorphonuclear leukocytes (PMNs) were tripled in the air group, as compared with the CO2 group, whereas the ratio of apoptotic PMNs was significantly decreased. There was a higher fraction of PKH26-positive PMNs after air exposure, as compared with that after CO2.

Conclusions

Air exposure triggered a higher transmigration rate of PMNs from the blood compartment into the peritoneal cavity and decreased PMN apoptosis, as compared with CO2. The lower proportion of PKH26-positive peritoneal macrophages in the air group might have been attributable to a higher inflammatory stimulation than in the CO2 group, leading to increased emigration of PMo to draining lymph nodes. All the findings underscore a complex cell-specific regulation of cell recruitment and clearance in the peritoneal compartment.
Literature
1.
go back to reference Allendorf JD, Bessler M, Whelan RL, Trokel M, Laird DA, Terry MB, Treat MR (1996) Better preservation of immune function after laparoscopic-assisted vs open bowel resection in a murine model. Dis Colon Rectum 39: S67–S72PubMedCrossRef Allendorf JD, Bessler M, Whelan RL, Trokel M, Laird DA, Terry MB, Treat MR (1996) Better preservation of immune function after laparoscopic-assisted vs open bowel resection in a murine model. Dis Colon Rectum 39: S67–S72PubMedCrossRef
2.
go back to reference Bellingan GJ, Caldwell H, Howie SE, Dransfield I, Haslett C (1996) In vivo fate of the inflammatory macrophage during the resolution of inflammation: inflammatory macrophages do not die locally, but emigrate to the draining lymph nodes. J Immunol 157: 2577–2585PubMed Bellingan GJ, Caldwell H, Howie SE, Dransfield I, Haslett C (1996) In vivo fate of the inflammatory macrophage during the resolution of inflammation: inflammatory macrophages do not die locally, but emigrate to the draining lymph nodes. J Immunol 157: 2577–2585PubMed
3.
go back to reference 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: 1135–1138PubMedCrossRef 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: 1135–1138PubMedCrossRef
4.
go back to reference 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: 1059–1064PubMedCrossRef 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: 1059–1064PubMedCrossRef
5.
go back to reference Colotta F, Re F, Polentarutti N, Sozzani S, Mantovani A (1992) Modulation of granulocyte survival and programmed cell death by cytokines and bacterial products. Blood 80: 2012–2020PubMed Colotta F, Re F, Polentarutti N, Sozzani S, Mantovani A (1992) Modulation of granulocyte survival and programmed cell death by cytokines and bacterial products. Blood 80: 2012–2020PubMed
6.
go back to reference Dumrese C, Maurus CF, Gygi D, Schneider MK, Walch M, Groscurth P, Ziegler U (2005) Chlamydia pneumoniae induces aponecrosis in human aortic smooth muscle cells. BMC Microbiol 5: 2PubMedCrossRef Dumrese C, Maurus CF, Gygi D, Schneider MK, Walch M, Groscurth P, Ziegler U (2005) Chlamydia pneumoniae induces aponecrosis in human aortic smooth muscle cells. BMC Microbiol 5: 2PubMedCrossRef
7.
go back to reference Gavrieli Y, Sherman Y, Ben Sasson SA (1992) Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 119: 493–501PubMedCrossRef Gavrieli Y, Sherman Y, Ben Sasson SA (1992) Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 119: 493–501PubMedCrossRef
8.
go back to reference 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: 65–71PubMedCrossRef 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: 65–71PubMedCrossRef
9.
go back to reference Glasser L, Fiederlein RL, Huestis DW (1985) Liquid preservation of human neutrophils stored in synthetic media at 22 degrees C: controlled observations on storage variables. Blood 66: 267–272PubMed Glasser L, Fiederlein RL, Huestis DW (1985) Liquid preservation of human neutrophils stored in synthetic media at 22 degrees C: controlled observations on storage variables. Blood 66: 267–272PubMed
10.
go back to reference Gutt CN, Oniu T, Schemmer P, Mehrabi A, Buchler MW (2004) Fewer adhesions induced by laparoscopic surgery? Surg Endosc 18: 898–906PubMedCrossRef Gutt CN, Oniu T, Schemmer P, Mehrabi A, Buchler MW (2004) Fewer adhesions induced by laparoscopic surgery? Surg Endosc 18: 898–906PubMedCrossRef
11.
go back to reference Hug H, Los M, Hirt W, Debatin KM (1999) Rhodamine 110-linked amino acids and peptides as substrates to measure caspase activity upon apoptosis induction in intact cells. Biochemistry 38: 13906–13911PubMedCrossRef Hug H, Los M, Hirt W, Debatin KM (1999) Rhodamine 110-linked amino acids and peptides as substrates to measure caspase activity upon apoptosis induction in intact cells. Biochemistry 38: 13906–13911PubMedCrossRef
12.
go back to reference 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: 357–363PubMed 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: 357–363PubMed
13.
go back to reference Kressel M, Groscurth P (1994) Distinction of apoptotic and necrotic cell death by in situ labeling of fragmented DNA. Cell Tissue Res 278: 549–556PubMed Kressel M, Groscurth P (1994) Distinction of apoptotic and necrotic cell death by in situ labeling of fragmented DNA. Cell Tissue Res 278: 549–556PubMed
14.
go back to reference Kurosaka K, Takahashi M, Watanabe N, Kobayashi Y (2003) Silent cleanup of very early apoptotic cells by macrophages. J Immunol 171: 4672–4679PubMed Kurosaka K, Takahashi M, Watanabe N, Kobayashi Y (2003) Silent cleanup of very early apoptotic cells by macrophages. J Immunol 171: 4672–4679PubMed
15.
go back to reference Lennard TW, Shenton BK, Borzotta A, Donnelly PK, White M, Gerrie LM, Proud G, Taylor RM (1985) The influence of surgical operations on components of the human immune system. Br J Surg 72: 771–776PubMed Lennard TW, Shenton BK, Borzotta A, Donnelly PK, White M, Gerrie LM, Proud G, Taylor RM (1985) The influence of surgical operations on components of the human immune system. Br J Surg 72: 771–776PubMed
16.
go back to reference Maus U, Herold S, Muth H, Maus R, Ermert L, Ermert M, Weissmann N, Rosseau S, Seeger W, Grimminger F, Lohmeyer J (2001) Monocytes recruited into the alveolar air space of mice show a monocytic phenotype but upregulate CD14. Am J Physiol Lung Cell Mol Physiol 280: L58–L68PubMed Maus U, Herold S, Muth H, Maus R, Ermert L, Ermert M, Weissmann N, Rosseau S, Seeger W, Grimminger F, Lohmeyer J (2001) Monocytes recruited into the alveolar air space of mice show a monocytic phenotype but upregulate CD14. Am J Physiol Lung Cell Mol Physiol 280: L58–L68PubMed
17.
go back to reference Melnicoff MJ, Morahan PS, Jensen BD, Breslin EW, Horan PK (1988) In vivo labeling of resident peritoneal macrophages. J Leukoc Biol 43: 387–397PubMed Melnicoff MJ, Morahan PS, Jensen BD, Breslin EW, Horan PK (1988) In vivo labeling of resident peritoneal macrophages. J Leukoc Biol 43: 387–397PubMed
18.
go back to reference Meszaros AJ, Reichner JS, Albina JE (2000) Macrophage-induced neutrophil apoptosis. J Immunol 165: 435–441PubMed Meszaros AJ, Reichner JS, Albina JE (2000) Macrophage-induced neutrophil apoptosis. J Immunol 165: 435–441PubMed
19.
go back to reference Moehrlen U, Schwobel 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: 958–963PubMedCrossRef Moehrlen U, Schwobel 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: 958–963PubMedCrossRef
20.
go back to reference Salamone G, Trevani A, Martinez D, Vermeulen M, Gamberale R, Fernandez-Calotti P, Raiden S, Giordano M, Geffner J (2004) Analysis of the mechanisms involved in the stimulation of neutrophil apoptosis by tumour necrosis factor-alpha. Immunology 113: 355–362PubMedCrossRef Salamone G, Trevani A, Martinez D, Vermeulen M, Gamberale R, Fernandez-Calotti P, Raiden S, Giordano M, Geffner J (2004) Analysis of the mechanisms involved in the stimulation of neutrophil apoptosis by tumour necrosis factor-alpha. Immunology 113: 355–362PubMedCrossRef
21.
go back to reference Savill J, Dransfield I, Hogg N, Haslett C (1990) Vitronectin receptor-mediated phagocytosis of cells undergoing apoptosis. Nature 343: 170–173PubMedCrossRef Savill J, Dransfield I, Hogg N, Haslett C (1990) Vitronectin receptor-mediated phagocytosis of cells undergoing apoptosis. Nature 343: 170–173PubMedCrossRef
22.
go back to reference Savill J, Fadok V, Henson P, Haslett C (1993) Phagocyte recognition of cells undergoing apoptosis. Immunol Today 14: 131–136PubMedCrossRef Savill J, Fadok V, Henson P, Haslett C (1993) Phagocyte recognition of cells undergoing apoptosis. Immunol Today 14: 131–136PubMedCrossRef
23.
go back to reference Trokel MJ, Bessler M, Treat MR, Whelan RL, Nowygrod R (1994) Preservation of immune response after laparoscopy. Surg Endosc 8: 1385–1387PubMedCrossRef Trokel MJ, Bessler M, Treat MR, Whelan RL, Nowygrod R (1994) Preservation of immune response after laparoscopy. Surg Endosc 8: 1385–1387PubMedCrossRef
24.
go back to reference Ure BM, Niewold TA, Bax NM, Ham M, 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: 836–842PubMedCrossRef Ure BM, Niewold TA, Bax NM, Ham M, 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: 836–842PubMedCrossRef
25.
go back to reference Vittimberga FJ Jr, Foley DP, Meyers WC, Callery MP (1998) Laparoscopic surgery and the systemic immune response. Ann Surg 227: 326–334PubMedCrossRef Vittimberga FJ Jr, Foley DP, Meyers WC, Callery MP (1998) Laparoscopic surgery and the systemic immune response. Ann Surg 227: 326–334PubMedCrossRef
26.
go back to reference 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: 1060–1065PubMed 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: 1060–1065PubMed
27.
go back to reference Watson RW, Rotstein OD, Nathens AB, Parodo J, Marshall JC (1997) Neutrophil apoptosis is modulated by endothelial transmigration and adhesion molecule engagement. J Immunol 158: 945–953PubMed Watson RW, Rotstein OD, Nathens AB, Parodo J, Marshall JC (1997) Neutrophil apoptosis is modulated by endothelial transmigration and adhesion molecule engagement. J Immunol 158: 945–953PubMed
Metadata
Title
Impact of carbon dioxide versus air pneumoperitoneum on peritoneal cell migration and cell fate
Authors
U. Moehrlen
U. Ziegler
E. Boneberg
E. Reichmann
C. A. Gitzelmann
M. Meuli
J. Hamacher
Publication date
01-10-2006
Publisher
Springer-Verlag
Published in
Surgical Endoscopy / Issue 10/2006
Print ISSN: 0930-2794
Electronic ISSN: 1432-2218
DOI
https://doi.org/10.1007/s00464-005-0775-4

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