Research Progress of CO2 Pneumoperitoneum Impacts on Invasiveness of Cancer Cells_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

The First Department of General Surgery， Affiliated Hospital of North Sichuan Medical College， Nanchong 637000， Sichuan Province， China;

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Keywords：

Laparoscopy; CO2 pneumoperitoneum; Tumor; Invasiveness; Metastasis

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Objective 　To summarize the research progress of CO2 pneumoperitoneum impacts on invasiveness of cancer cells.
Methods 　Currently published experimental and clinical researches related to the effect of CO2 pneumoperitoneum on invasiveness of cancer cells were reviewed.
Results 　CO2 pneumoperitoneum may affect the invasiveness of cancer cell through several ways， such as changing the structure and function of mesothelial cell， changing microenvironment of peritoneum， influencing the expression of oncogen， affecting the secretion of cell factor， and changing the adhesion of cancer cell.
Conclusions 　The consequences of these alterations to cancer cell and the microenvironment are not well understood， but they may facilitate tumor invasion and implantation. Further investigations in this area are very urgent.

Citation： LU Qijun,WANG Chongshu,DU Jiang. Research Progress of CO2 Pneumoperitoneum Impacts on Invasiveness of Cancer Cells. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2012, 19(12): 1362-1367. doi: Copy

1.	Bracale U， Barone M， Pema F， et al. Laparascopic colon resection for cancer：evidence based results[J]. Acta Chir Iugosl， 2010， 57(3)：37-40.
2.	Mareel M， Leroy A. Clinical， cellular， and molecular aspects of cancer invasion[J]. Physiol Rev， 2003， 83(2)：337-376.
3.	Griffiths JR， McIntyre DJ， Howe FA，et al. Why are cancers acidic? A carrier-mediated diffusion model for H＋ transport in the interstitial ﬂuid[J]. Novartis Found Symp， 2001， 240：46-62.
4.	Paget S. The distribution of secondary growths in cancer of the breast. 1889[J]. Cancer Metastasis Rev， 1989， 8(2)：98-101.
5.	Lackey LW， Ott DE. Terminal gas velocity during laparoscopy[J]. J Am Assoc Gynecol Laparosc， 2002， 9(3)：297-305.
6.	Ott DE. Desertification of the peritoneum by thin-film evaporationduring laparoscopy[J]. JSLS， 2003， 7(3)：189-195.
7.	Verguts J， Vergote I， Amant F， et al. The addition of 4% oxygen to the CO2 pneumoperitoneum does not decrease dramatically port site metastases[J]. J Minim Invasive Gynecol， 2008， 15(6)：700-703.
8.	Reismann M， Wehrmann F， Schukfeh N， et al. Carbon dioxide，hypoxia and low pH lead to overexpression of c-myc and HMGB-1oncogenes in neuroblastoma cells[J]. Eur J Pediatr Surg， 2009， 19(4)：224-227.
9.	Krause P， Bobisch NS， Thelen P， et al. The plasminogen activatorinhibitor system in colon cancer cell lines is influenced by the CO2 pneumoperitoneum[J]. Int J Colorectal Dis， 2011， 26(1)：37-43.
10.	Zhou HM， Feng B， Zhao HC， et al. Antitumor effects ofhyperthermic CO2 pneumoperitoneum on human gastric cancer cells[J]. Asian Pac J Cancer Prev， 2012， 13(1)：117-122.
11.	Li J， Wang JW， Zheng S， et al. Influences of laparoscopicresection on expressions of metastasis genes in colorectal cancer：report of microarray analysis and literature review[J]. Hepatogastroenterology， 2011， 58(112)：1975-1982.
12.	Amin MA， Haas CS， Zhu K， et al. Migration inhibitory factor up-regulates vascular cell adhesion molecule-1 and intercellular adhesion molecule-1 via Src， PI3 kinase， and NFkappaB[J]. Blood， 2006， 107(6)：2252-2261.
13.	Mohri Y. Prognostic significance of E-cadherin expression inhuman colorectal cancer tissue[J]. Surg Today， 1997， 27(7)：606-612.
14.	Ma JJ， Feng B， Zhang Y， et al. Higher CO2-insufflation pressure inhibits the expression of adhesion molecules and the invasion potential of colon cancer cells[J]. World J Gastroenterol， 2009， 15(22)：2714-2722.
15.	Ordemann J， Höflich C， Braumann C， et al. Impact of pneumoperitoneum on expression of E-cadherin， CD44v6 and CD54 (ICAM-1) on HT-29 colon-carcinoma cells[J]. Zentralbl Chir， 2005， 130(5)：405-409.
16.	Kim ZG， Mehl C， Lorenz M， et al. Impact of laparoscopic CO2-insufflation on tumor-associated molecules in cultured colorectal cancer cells[J]. Surg Endosc， 2002， 16(8)：1182-1186.
17.	Matsuzaki S， Jardon K， Maleysson E， et al. Impact of intraperitoneal pressure of a CO2 pneumoperitoneum on the surgical peritoneal environment[J]. Hum Reprod， 2012， 27(6)：1613-1623.
18.	Heel KA， Hall JC. Peritoneal defences and peritoneum-associatedlymphoid tissue[J]. Br J Surg， 1996， 83(8)：1031-1036.
19.	Schmidt AI， Reismann M， Kübler JF， et al. Exposure to carbon dioxide and helium reduces in vitro proliferation of pediatrictumor cells[J]. Pediatr Surg Int， 2006， 22(1)：72-77.
20.	Kuntz C， Wunsch A， Bödeker C， et al. Effect of pressure and gas type on intraabdominal， subcutaneous， and blood pH inlaparoscopy[J]. Surg Endosc， 2000， 14(4)：367-371.
21.	Yavuz Y， Rønning K， Lyng O， et al. Effect of carbon dioxide pneumoperitoneum on tissue blood flow in the peritoneum， rectus abdominis， and diaphragm muscles[J]. Surg Endosc， 2003， 17(10)：1632-1635.
22.	Wildbrett P， Oh A， Naundorf D， et al. Impact of laparoscopic gases on peritoneal microenvironment and essential parameters of cell function[J]. Surg Endosc， 2003， 17(1)：78-82.
23.	Schlotterbeck H， Greib N， Dow WA， et al. Changes in coretemperature during peritoneal insufflation：comparison of two CO2 humidification devices in pigs[J]. J Surg Res， 2011， 171(2)：427-432.
24.	Neuhaus SJ， Watson DI. Pneumoperitoneum and peritonealsurface changes：a review[J]. Surg Endosc， 2004， 18(9)：1316-1322.
25.	Whelan RL， Franklin M， Holubar SD， et al. Postoperative cell mediated immune response is better preserved after laparoscopic vs. open colorectal resection in humans[J]. Surg Endosc， 2003， 17(6)：972-978.
26.	Gitzelmann CA， Mendoza-Sagaon M， Talamini MA， et al.Cell-mediated immune response is better preserved by laparoscopy than laparotomy[J]. Surgery， 2000， 127(1)：65-71.
27.	Wichmann MW， Hüttl TP， Winter H， et al. Immunologicaleffects of laparoscopic vs. open colorectal surgery：a prospective clinical study[J]. Arch Surg， 2005， 140(7)：692-697.
28.	Brokelman WJ， Lensvelt M， Borel Rinkes IH， et al. Peritoneal changes due to laparoscopic surgery[J]. Surg Endosc， 2011， 25(1)：1-9.
29.	Waiwut P， Shin MS， Inujima A， et al. Gomisin N enhances TNF-α-induced apoptosis via inhibition of the NF-κB and EGFR survival pathways[J]. Mol Cell Biochem， 2011， 350(1-2)：169-175.
30.	Amin AT， Shiraishi N， Ninomiya S， et al. Increased mRNA expression of epidermal growth factor receptor， human epidermal receptor， and survivin in human gastric cancer after the surgical stress of laparotomy versus carbon dioxide pneumoperitoneum in a murine model[J]. Surg Endosc， 2010， 24(6)：1427-1433.
31.	Tawfik Amin A， Shiraishi N， Ninomiya S， et al. Activation of nuclear factor kappa B and induction of migration inhibitory factor in tumors by surgical stress of laparotomy versus carbon dioxide pneumoperitoneum：an animal experiment[J]. Surg Endosc， 2010， 24(3)：578-583.
32.	Machado MC， Coelho AM， Martins JO， et al. CO2 abdominal insufflation decreases local and systemic inflammatory response in experimental acute pancreatitis[J]. Pancreas， 2010， 39(2)：175-181.
33.	Yu Y， Kuebler J， Groos S， et al. Carbon dioxide modifies the morphology and function of mesothelial cells and facilitates transepithelial neuroblastoma cell migration[J]. Pediatr Surg Int， 2010， 26(1)：29-36.
34.	Fuganti PE， Rodrigues Júnior AJ， Rodrigues CJ， et al. Acomparison of the effects of pneumoperitoneum and laparotomy on natural killer cell mediated cytotoxicity and Walker tumor growth in Wistar rats[J]. Surg Endosc， 2006， 20(12)：1858-1861.
35.	Mutsaers SE， Whitaker D， Papadimitriou JM. Changes in the concentration of microvilli on the free surface of healing mesothelium are associated with alterations in surface membrane charge[J]. J Pathol， 1996， 180(3)：333-339.
36.	Ryan GB， Grobéty J， Majno G. Mesothelial injury and recovery[J]. Am J Pathol， 1973， 71(1)：93-112.
37.	Rosário MT， Ribeiro U Jr， Corbett CE， et al. Does CO2 pneumoperitoneum alter the ultra-structuture of the mesothelium?[J]. J Surg Res， 2006， 133(2)：84-88.
38.	Du J， Yu PW， Tang B. Application of stereology to study the effects of pneumoperitoneum on peritoneum[J]. Surg Endosc， 2011， 25(2)：619-627.
39.	Yamaguchi K， Hirabayashi Y， Suematsu T， et al. Hyaluronic acid secretion during carbon dioxide pneumoperitoneum and its association with port-site metastasis in a murine model[J]. Surg Endosc， 2001， 15(1)：59-62.
40.	Volz J， Köster S， Schaeff B， et al. Laparoscopic surgery：the effects of insufflation gas on tumor-induced lethality in nude mice[J]. Am J Obstet Gynecol， 1998， 178(4)：793-795.
41.	Metzelder M， Kuebler J， Shimotakahara A， et al. CO2 pneumoperitoneum increases systemic but not local tumor spread after intraperitoneal murine neuroblastoma spillage in mice[J]. Surg Endosc， 2008， 22(12)：2648-2653.
42.	Nestler G， Schulz HU， Tautenhahn J， et al. Effects of theangiogenesis inhibitor angiostatin on the growth of CC531 colon carcinoma cells in vitro and in a laparoscopic animal model of peritoneal carcinomatosis[J]. Int J Colorectal Dis， 2006， 21(4)：314-320.
43.	孙铁为，李强，王锋. 一次性CO2气腹环境下氟尿嘧啶对大鼠肿瘤细胞生长及转移的影响[J]. 中国普外基础与临床杂志， 2009， 16(7)：545-549.
44.	Nakada H， Ishida H， Hashimoto D， et al. Influence of different pneumoperitoneal pressures on tumor cell distribution in rats[J]. Surg Endosc， 2005， 19(4)：563-568.
45.	Volz J， Volz-Köster S， Kanis S， et al. Modulation of tumor-induced lethality after pneumoperitoneum in a mouse model[J]. Cancer， 2000， 89(2)：262-266.
46.	Fondrinier E， Descamps P， Arnaud JP， et al. Carbon dioxidepneumoperitoneum and peritoneal carcinosis：review[J].J Gynecol Obstet Biol Reprod (Paris)， 2002， 31(1)：11-27.

1. Bracale U， Barone M， Pema F， et al. Laparascopic colon resection for cancer：evidence based results[J]. Acta Chir Iugosl， 2010， 57(3)：37-40.
2. Mareel M， Leroy A. Clinical， cellular， and molecular aspects of cancer invasion[J]. Physiol Rev， 2003， 83(2)：337-376.
3. Griffiths JR， McIntyre DJ， Howe FA，et al. Why are cancers acidic? A carrier-mediated diffusion model for H＋ transport in the interstitial ﬂuid[J]. Novartis Found Symp， 2001， 240：46-62.
4. Paget S. The distribution of secondary growths in cancer of the breast. 1889[J]. Cancer Metastasis Rev， 1989， 8(2)：98-101.
5. Lackey LW， Ott DE. Terminal gas velocity during laparoscopy[J]. J Am Assoc Gynecol Laparosc， 2002， 9(3)：297-305.
6. Ott DE. Desertification of the peritoneum by thin-film evaporationduring laparoscopy[J]. JSLS， 2003， 7(3)：189-195.
7. Verguts J， Vergote I， Amant F， et al. The addition of 4% oxygen to the CO2 pneumoperitoneum does not decrease dramatically port site metastases[J]. J Minim Invasive Gynecol， 2008， 15(6)：700-703.
8. Reismann M， Wehrmann F， Schukfeh N， et al. Carbon dioxide，hypoxia and low pH lead to overexpression of c-myc and HMGB-1oncogenes in neuroblastoma cells[J]. Eur J Pediatr Surg， 2009， 19(4)：224-227.
9. Krause P， Bobisch NS， Thelen P， et al. The plasminogen activatorinhibitor system in colon cancer cell lines is influenced by the CO2 pneumoperitoneum[J]. Int J Colorectal Dis， 2011， 26(1)：37-43.
10. Zhou HM， Feng B， Zhao HC， et al. Antitumor effects ofhyperthermic CO2 pneumoperitoneum on human gastric cancer cells[J]. Asian Pac J Cancer Prev， 2012， 13(1)：117-122.
11. Li J， Wang JW， Zheng S， et al. Influences of laparoscopicresection on expressions of metastasis genes in colorectal cancer：report of microarray analysis and literature review[J]. Hepatogastroenterology， 2011， 58(112)：1975-1982.
12. Amin MA， Haas CS， Zhu K， et al. Migration inhibitory factor up-regulates vascular cell adhesion molecule-1 and intercellular adhesion molecule-1 via Src， PI3 kinase， and NFkappaB[J]. Blood， 2006， 107(6)：2252-2261.
13. Mohri Y. Prognostic significance of E-cadherin expression inhuman colorectal cancer tissue[J]. Surg Today， 1997， 27(7)：606-612.
14. Ma JJ， Feng B， Zhang Y， et al. Higher CO2-insufflation pressure inhibits the expression of adhesion molecules and the invasion potential of colon cancer cells[J]. World J Gastroenterol， 2009， 15(22)：2714-2722.
15. Ordemann J， Höflich C， Braumann C， et al. Impact of pneumoperitoneum on expression of E-cadherin， CD44v6 and CD54 (ICAM-1) on HT-29 colon-carcinoma cells[J]. Zentralbl Chir， 2005， 130(5)：405-409.
16. Kim ZG， Mehl C， Lorenz M， et al. Impact of laparoscopic CO2-insufflation on tumor-associated molecules in cultured colorectal cancer cells[J]. Surg Endosc， 2002， 16(8)：1182-1186.
17. Matsuzaki S， Jardon K， Maleysson E， et al. Impact of intraperitoneal pressure of a CO2 pneumoperitoneum on the surgical peritoneal environment[J]. Hum Reprod， 2012， 27(6)：1613-1623.
18. Heel KA， Hall JC. Peritoneal defences and peritoneum-associatedlymphoid tissue[J]. Br J Surg， 1996， 83(8)：1031-1036.
19. Schmidt AI， Reismann M， Kübler JF， et al. Exposure to carbon dioxide and helium reduces in vitro proliferation of pediatrictumor cells[J]. Pediatr Surg Int， 2006， 22(1)：72-77.
20. Kuntz C， Wunsch A， Bödeker C， et al. Effect of pressure and gas type on intraabdominal， subcutaneous， and blood pH inlaparoscopy[J]. Surg Endosc， 2000， 14(4)：367-371.
21. Yavuz Y， Rønning K， Lyng O， et al. Effect of carbon dioxide pneumoperitoneum on tissue blood flow in the peritoneum， rectus abdominis， and diaphragm muscles[J]. Surg Endosc， 2003， 17(10)：1632-1635.
22. Wildbrett P， Oh A， Naundorf D， et al. Impact of laparoscopic gases on peritoneal microenvironment and essential parameters of cell function[J]. Surg Endosc， 2003， 17(1)：78-82.
23. Schlotterbeck H， Greib N， Dow WA， et al. Changes in coretemperature during peritoneal insufflation：comparison of two CO2 humidification devices in pigs[J]. J Surg Res， 2011， 171(2)：427-432.
24. Neuhaus SJ， Watson DI. Pneumoperitoneum and peritonealsurface changes：a review[J]. Surg Endosc， 2004， 18(9)：1316-1322.
25. Whelan RL， Franklin M， Holubar SD， et al. Postoperative cell mediated immune response is better preserved after laparoscopic vs. open colorectal resection in humans[J]. Surg Endosc， 2003， 17(6)：972-978.
26. Gitzelmann CA， Mendoza-Sagaon M， Talamini MA， et al.Cell-mediated immune response is better preserved by laparoscopy than laparotomy[J]. Surgery， 2000， 127(1)：65-71.
27. Wichmann MW， Hüttl TP， Winter H， et al. Immunologicaleffects of laparoscopic vs. open colorectal surgery：a prospective clinical study[J]. Arch Surg， 2005， 140(7)：692-697.
28. Brokelman WJ， Lensvelt M， Borel Rinkes IH， et al. Peritoneal changes due to laparoscopic surgery[J]. Surg Endosc， 2011， 25(1)：1-9.
29. Waiwut P， Shin MS， Inujima A， et al. Gomisin N enhances TNF-α-induced apoptosis via inhibition of the NF-κB and EGFR survival pathways[J]. Mol Cell Biochem， 2011， 350(1-2)：169-175.
30. Amin AT， Shiraishi N， Ninomiya S， et al. Increased mRNA expression of epidermal growth factor receptor， human epidermal receptor， and survivin in human gastric cancer after the surgical stress of laparotomy versus carbon dioxide pneumoperitoneum in a murine model[J]. Surg Endosc， 2010， 24(6)：1427-1433.
31. Tawfik Amin A， Shiraishi N， Ninomiya S， et al. Activation of nuclear factor kappa B and induction of migration inhibitory factor in tumors by surgical stress of laparotomy versus carbon dioxide pneumoperitoneum：an animal experiment[J]. Surg Endosc， 2010， 24(3)：578-583.
32. Machado MC， Coelho AM， Martins JO， et al. CO2 abdominal insufflation decreases local and systemic inflammatory response in experimental acute pancreatitis[J]. Pancreas， 2010， 39(2)：175-181.
33. Yu Y， Kuebler J， Groos S， et al. Carbon dioxide modifies the morphology and function of mesothelial cells and facilitates transepithelial neuroblastoma cell migration[J]. Pediatr Surg Int， 2010， 26(1)：29-36.
34. Fuganti PE， Rodrigues Júnior AJ， Rodrigues CJ， et al. Acomparison of the effects of pneumoperitoneum and laparotomy on natural killer cell mediated cytotoxicity and Walker tumor growth in Wistar rats[J]. Surg Endosc， 2006， 20(12)：1858-1861.
35. Mutsaers SE， Whitaker D， Papadimitriou JM. Changes in the concentration of microvilli on the free surface of healing mesothelium are associated with alterations in surface membrane charge[J]. J Pathol， 1996， 180(3)：333-339.
36. Ryan GB， Grobéty J， Majno G. Mesothelial injury and recovery[J]. Am J Pathol， 1973， 71(1)：93-112.
37. Rosário MT， Ribeiro U Jr， Corbett CE， et al. Does CO2 pneumoperitoneum alter the ultra-structuture of the mesothelium?[J]. J Surg Res， 2006， 133(2)：84-88.
38. Du J， Yu PW， Tang B. Application of stereology to study the effects of pneumoperitoneum on peritoneum[J]. Surg Endosc， 2011， 25(2)：619-627.
39. Yamaguchi K， Hirabayashi Y， Suematsu T， et al. Hyaluronic acid secretion during carbon dioxide pneumoperitoneum and its association with port-site metastasis in a murine model[J]. Surg Endosc， 2001， 15(1)：59-62.
40. Volz J， Köster S， Schaeff B， et al. Laparoscopic surgery：the effects of insufflation gas on tumor-induced lethality in nude mice[J]. Am J Obstet Gynecol， 1998， 178(4)：793-795.
41. Metzelder M， Kuebler J， Shimotakahara A， et al. CO2 pneumoperitoneum increases systemic but not local tumor spread after intraperitoneal murine neuroblastoma spillage in mice[J]. Surg Endosc， 2008， 22(12)：2648-2653.
42. Nestler G， Schulz HU， Tautenhahn J， et al. Effects of theangiogenesis inhibitor angiostatin on the growth of CC531 colon carcinoma cells in vitro and in a laparoscopic animal model of peritoneal carcinomatosis[J]. Int J Colorectal Dis， 2006， 21(4)：314-320.
43. 孙铁为，李强，王锋. 一次性CO2气腹环境下氟尿嘧啶对大鼠肿瘤细胞生长及转移的影响[J]. 中国普外基础与临床杂志， 2009， 16(7)：545-549.
44. Nakada H， Ishida H， Hashimoto D， et al. Influence of different pneumoperitoneal pressures on tumor cell distribution in rats[J]. Surg Endosc， 2005， 19(4)：563-568.
45. Volz J， Volz-Köster S， Kanis S， et al. Modulation of tumor-induced lethality after pneumoperitoneum in a mouse model[J]. Cancer， 2000， 89(2)：262-266.
46. Fondrinier E， Descamps P， Arnaud JP， et al. Carbon dioxidepneumoperitoneum and peritoneal carcinosis：review[J].J Gynecol Obstet Biol Reprod (Paris)， 2002， 31(1)：11-27.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Research Progress of CO2 Pneumoperitoneum Impacts on Invasiveness of Cancer Cells

Abstract Full text Figures/Tables Video References Cited by

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