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Published in: Surgical Endoscopy 12/2008

01-12-2008

CO2 pneumoperitoneum increases systemic but not local tumor spread after intraperitoneal murine neuroblastoma spillage in mice

Authors: Martin Metzelder, Joachim Kuebler, Akihiro Shimotakahara, Gertrud Vieten, Reinhard von Wasielewski, Benno Manfred Ure

Published in: Surgical Endoscopy | Issue 12/2008

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Abstract

Background

Minimally invasive techniques are increasingly used for biopsy and resection of neuroblastoma, but the impact on the behavior of spilled tumor cells is unknown. We aimed to investigate whether CO2 pneumoperitoneum can affect local or systemic tumor manifestation after spillage of neuroblastoma cells into the peritoneal cavity.

Methods

Murine neuroblastoma cells (Neuro2a, 1x106) were inoculated into the peritoneal cavity of 25 male A/J mice, which subsequently underwent CO2 pneumoperitoneum (n = 12) or laparotomy (n = 13) for 1 h. At the 28th postoperative day, local (peritoneal and surface of the gut) and systemic (liver, lung, spine) tumor spread was graded in a blinded manner (1–4 point scale) and specimens were histologically examined for tumor manifestation (hematoxylin and eosin stain) and tumor cell proliferation rate (Ki-67-stain). In the case of no visible lesion, five random sections were histologically examined. Peritoneal carcinosis was graded macroscopically.

Results

Tumor manifestations were detected in 10 out of 12 (83%) animals after CO2 pneumoperitoneum, and in 9 out of 13 (69%) after laparotomy (n.s.). Incidence of liver metastasis was higher after CO2 pneumoperitoneum versus laparotomy (83% versus 31%; p < 0.05). Incidence and grading of peritoneal carcinosis was not significantly different between the groups (n.s.). Intrapulmonary metastasis was found in one mouse of each group, but no metastasis of the spine. However, the grading of liver metastasis was higher after CO2 pneumoperitoneum compared to laparotomy (p < 0.05). Tumor cell proliferation (Ki-67 stain) in the liver did not differ between both groups. Moreover, proliferation always exceeded 50% of tumor cells, irrespective local or systemic tumor manifestation.

Conclusions

CO2 pneumoperitoneum increased intrahepatic metastasis, but not local peritoneal carcinosis in a murine neuroblastoma model. This suggests that laparoscopy could promote systemic dissemination of intraperitoneally spilled tumor cells when no chemotherapy is applied. It remains to be determined whether this is due to local immune suppression or direct modulation of tumor cell behavior.
Literature
1.
go back to reference Allendorf JD, Bessler M, Kayton ML, Oesterling SD, Treat MR, Nowygrod R, Whelan L (1995) Increased tumor establishment and growth after laparotomy vs laparoscopy in a murine model. Arch Surg 130:649–653PubMed Allendorf JD, Bessler M, Kayton ML, Oesterling SD, Treat MR, Nowygrod R, Whelan L (1995) Increased tumor establishment and growth after laparotomy vs laparoscopy in a murine model. Arch Surg 130:649–653PubMed
2.
go back to reference Allendorf JD, Bessler M, Kayton ML, Whelan RL, Treat MR, Nowygrod R (1995) Tumor growth after laparotomy or laparoscopy. A preliminary study. Surg Endosc 9:49–52 Allendorf JD, Bessler M, Kayton ML, Whelan RL, Treat MR, Nowygrod R (1995) Tumor growth after laparotomy or laparoscopy. A preliminary study. Surg Endosc 9:49–52
3.
go back to reference Are C, Talamini MA (2005) Laparoscopy and malignancy. J Laparoendosc Adv Surg Tech 15:38–47CrossRef Are C, Talamini MA (2005) Laparoscopy and malignancy. J Laparoendosc Adv Surg Tech 15:38–47CrossRef
4.
go back to reference Bouvy ND, Marquet RL, Jeekel H, Bonjer HJ (1997) Laparoscopic surgery is associated with less tumor growth stimulation than conventional surgery: an experimental study. Br J Surg 84:358–361PubMedCrossRef Bouvy ND, Marquet RL, Jeekel H, Bonjer HJ (1997) Laparoscopic surgery is associated with less tumor growth stimulation than conventional surgery: an experimental study. Br J Surg 84:358–361PubMedCrossRef
5.
go back to reference Clinical Outcomes of Surgical Therapy Study Group (2004) A comparison of laparoscopically assisted and open colectomy for colon cancer. N Engl J Med 350:2050–2059CrossRef Clinical Outcomes of Surgical Therapy Study Group (2004) A comparison of laparoscopically assisted and open colectomy for colon cancer. N Engl J Med 350:2050–2059CrossRef
6.
go back to reference Dahn S, Schwalbach P, Wohlecke F, Benner A, Kuntz C (2003) Influence of different gases used for laparoscopy (helium, carbon dioxide, room air, xenon) on tumor volume, proliferation and apoptosis. Surg Endosc 17:1653–1657 PubMedCrossRef Dahn S, Schwalbach P, Wohlecke F, Benner A, Kuntz C (2003) Influence of different gases used for laparoscopy (helium, carbon dioxide, room air, xenon) on tumor volume, proliferation and apoptosis. Surg Endosc 17:1653–1657 PubMedCrossRef
7.
go back to reference Da Costa ML, Redmond HP, Finnegan N, Flynn M, Bouchier-Hayes D (1998) Laparotomy and laparoscopy differentially accelerate experimental flank tumour growth. Br J Surg 85:1439–1442PubMedCrossRef Da Costa ML, Redmond HP, Finnegan N, Flynn M, Bouchier-Hayes D (1998) Laparotomy and laparoscopy differentially accelerate experimental flank tumour growth. Br J Surg 85:1439–1442PubMedCrossRef
8.
go back to reference De Lagausie P, Berrebi D, Michon J, Philippe-Chomette P, El Ghoneimi A, Garel C, Brisse H, Peuchmar M, Aigrin Y (2003) Laparoscopic adrenal surgery for neuroblastomas in children. J Urol 170:932–935PubMedCrossRef De Lagausie P, Berrebi D, Michon J, Philippe-Chomette P, El Ghoneimi A, Garel C, Brisse H, Peuchmar M, Aigrin Y (2003) Laparoscopic adrenal surgery for neuroblastomas in children. J Urol 170:932–935PubMedCrossRef
9.
go back to reference Gutt CN, Bruttel T, Brier C, Paolucci V, Encke A (1998) CO2 pneumoperitoneum inhibits in vitro proliferation of human carcinoma cell. Langenbecks Arch Chir Suppl Kongressbd 115:535–540PubMed Gutt CN, Bruttel T, Brier C, Paolucci V, Encke A (1998) CO2 pneumoperitoneum inhibits in vitro proliferation of human carcinoma cell. Langenbecks Arch Chir Suppl Kongressbd 115:535–540PubMed
10.
go back to reference Gutt CN, Riemer V, Kim ZG, Jacobi CA, Paolucci V, Lorenz M (1999) Impact of laparoscopic colonic resection on tumor growth and spread in an experimental model. Br J Surg 86:1180–1184PubMedCrossRef Gutt CN, Riemer V, Kim ZG, Jacobi CA, Paolucci V, Lorenz M (1999) Impact of laparoscopic colonic resection on tumor growth and spread in an experimental model. Br J Surg 86:1180–1184PubMedCrossRef
11.
go back to reference Gutt CN, Gessmann T, Schemmer P, Mehrabi A, Schmandra T, Kim ZG (2003) The impact of carbon dioxide on experimental liver metastasis, macrophages, and cell adhesion molecules. Surg Endosc 17:1628–1631PubMedCrossRef Gutt CN, Gessmann T, Schemmer P, Mehrabi A, Schmandra T, Kim ZG (2003) The impact of carbon dioxide on experimental liver metastasis, macrophages, and cell adhesion molecules. Surg Endosc 17:1628–1631PubMedCrossRef
12.
go back to reference Holcomb GW, Tomita SS, Haase GM, Dillon PW, Newman KD, Applebaum H, Wiener ES (1995) Minimally invasive surgery in children with cancer. Cancer 76:121–128PubMedCrossRef Holcomb GW, Tomita SS, Haase GM, Dillon PW, Newman KD, Applebaum H, Wiener ES (1995) Minimally invasive surgery in children with cancer. Cancer 76:121–128PubMedCrossRef
13.
go back to reference Ishida H, Murata N, Yamada H, Nakada H, Takeuchi I, Shimomura K, Fujioka M, Idezuki Y (2000) Pneumoperitoneum with carbon dioxide enhances liver metastases of cancer cells implanted into the portal vein in rabbits. Surg Endosc 14:239–242PubMedCrossRef Ishida H, Murata N, Yamada H, Nakada H, Takeuchi I, Shimomura K, Fujioka M, Idezuki Y (2000) Pneumoperitoneum with carbon dioxide enhances liver metastases of cancer cells implanted into the portal vein in rabbits. Surg Endosc 14:239–242PubMedCrossRef
14.
go back to reference Iwanaka T, Arya G, Ziegler MM (1998) Minimally invasive surgery does not improve the outcome in a model of retroperitoneal murine neuroblastoma. Pediatr Surg Int 13:149–153PubMedCrossRef Iwanaka T, Arya G, Ziegler MM (1998) Minimally invasive surgery does not improve the outcome in a model of retroperitoneal murine neuroblastoma. Pediatr Surg Int 13:149–153PubMedCrossRef
15.
go back to reference Iwanaka T, Arya G, Ziegler MM (1998) Mechanism and prevention of port-site tumor recurrence after laparoscopy in a murine model. J Pediatr Surg 33:475–461CrossRef Iwanaka T, Arya G, Ziegler MM (1998) Mechanism and prevention of port-site tumor recurrence after laparoscopy in a murine model. J Pediatr Surg 33:475–461CrossRef
16.
go back to reference Iwanaka T, Arai M, Kawashima H, Kudou S, Fujishiro J, Imaizumi S, Yamamoto K, Hanada R, Kikuchi A, Aihara T, Kishimoto H (2004) Endosurgical procedures for pediatric solid tumors. Pediatr Surg Int 20:39–42PubMedCrossRef Iwanaka T, Arai M, Kawashima H, Kudou S, Fujishiro J, Imaizumi S, Yamamoto K, Hanada R, Kikuchi A, Aihara T, Kishimoto H (2004) Endosurgical procedures for pediatric solid tumors. Pediatr Surg Int 20:39–42PubMedCrossRef
17.
go back to reference Iwanaka T, Arai M, Yamamoto H, Fukuzawa M, Kubota A, Kouchi K, Nio M, Satomi A, Sasaki F, Yoneda A, Ohhama Y, Takahara H, Morikawa Y, Miyano T (2003) No incidence of port-site recurrence after endosurgical procedure for pediatric malignancies. Pediatr Surg Int 19:200–203PubMed Iwanaka T, Arai M, Yamamoto H, Fukuzawa M, Kubota A, Kouchi K, Nio M, Satomi A, Sasaki F, Yoneda A, Ohhama Y, Takahara H, Morikawa Y, Miyano T (2003) No incidence of port-site recurrence after endosurgical procedure for pediatric malignancies. Pediatr Surg Int 19:200–203PubMed
18.
go back to reference Izumi K, Ishikawa K, Tojigamori M, Matsui Y, Shiraishi N, Kitano S (2005) Liver metastasis and ICAM-1 mRNA expression in the liver after carbon dioxide pneumoperitoneum in a murine model. Surg Endosc 19:1049–1054PubMedCrossRef Izumi K, Ishikawa K, Tojigamori M, Matsui Y, Shiraishi N, Kitano S (2005) Liver metastasis and ICAM-1 mRNA expression in the liver after carbon dioxide pneumoperitoneum in a murine model. Surg Endosc 19:1049–1054PubMedCrossRef
19.
go back to reference Jackson PG, Evans SR (2000) Intraperitoneal macrophages and tumor immunity: A review. J Surg Oncol 75:146–154PubMedCrossRef Jackson PG, Evans SR (2000) Intraperitoneal macrophages and tumor immunity: A review. J Surg Oncol 75:146–154PubMedCrossRef
20.
go back to reference Jacobi CA, Ordemann J, Bohm B, Zieren HU, Liebenthal C, Volk HD, Muller JM (1997) The influence of laparotomy and laparoscopy on tumor growth in a rat model. Surg Endosc 11:618–621PubMedCrossRef Jacobi CA, Ordemann J, Bohm B, Zieren HU, Liebenthal C, Volk HD, Muller JM (1997) The influence of laparotomy and laparoscopy on tumor growth in a rat model. Surg Endosc 11:618–621PubMedCrossRef
21.
go back to reference Jacobi CA, Wenger F, Sabat R, Volk T, Ordemann J, Muller JM (1998) The impact of laparoscopy with carbon dioxide versus helium on immunologic function and tumor growth in a rat model. Dig Surg 15:110–116PubMedCrossRef Jacobi CA, Wenger F, Sabat R, Volk T, Ordemann J, Muller JM (1998) The impact of laparoscopy with carbon dioxide versus helium on immunologic function and tumor growth in a rat model. Dig Surg 15:110–116PubMedCrossRef
22.
go back to reference Jacobi CA, Wenger FA, Ordemann J, Gutt C, Sabat R, Muller JM (1998) Experimental study of the effect of intra-abdominal pressure during laparoscopy on tumour growth and port site metastasis. Br J Surg 85:1419–1422PubMedCrossRef Jacobi CA, Wenger FA, Ordemann J, Gutt C, Sabat R, Muller JM (1998) Experimental study of the effect of intra-abdominal pressure during laparoscopy on tumour growth and port site metastasis. Br J Surg 85:1419–1422PubMedCrossRef
23.
go back to reference Jesch NK, Vieten G, Tschernig T, Schroedel W, Ure BM (2005) Mini-laparotomy and full laparotomy, but not laparoscopy, alter hepatic macrophage populations in a rat model. Surg Endosc 19:804–810 PubMedCrossRef Jesch NK, Vieten G, Tschernig T, Schroedel W, Ure BM (2005) Mini-laparotomy and full laparotomy, but not laparoscopy, alter hepatic macrophage populations in a rat model. Surg Endosc 19:804–810 PubMedCrossRef
24.
go back to reference Krams M, Hero B, Berthold F, Parwaresch R, Harms D, Rudolph P (2002) Proliferation marker KI-S5 discriminates between favorable and adverse prognosis in advanced stages of neuroblastoma with and without MYCN amplification. Cancer 94:854–861PubMedCrossRef Krams M, Hero B, Berthold F, Parwaresch R, Harms D, Rudolph P (2002) Proliferation marker KI-S5 discriminates between favorable and adverse prognosis in advanced stages of neuroblastoma with and without MYCN amplification. Cancer 94:854–861PubMedCrossRef
25.
go back to reference Kuebler JF, Kos M, Jesch NK, Metzelder ML, van der Zee DC, Bax KM, Vieten G, Ure BM (2007) Carbon dioxide suppresses macrophage superoxide anion production independent of extracellular pH and mitochondrial activity. J Pediatr Surg 42:244–248PubMedCrossRef Kuebler JF, Kos M, Jesch NK, Metzelder ML, van der Zee DC, Bax KM, Vieten G, Ure BM (2007) Carbon dioxide suppresses macrophage superoxide anion production independent of extracellular pH and mitochondrial activity. J Pediatr Surg 42:244–248PubMedCrossRef
26.
go back to reference Lacy AM, Garcia-Valdecasas JC, Delgado S, Castells A, Taura P, Pique JM, Visa J (2002) Laparoscopic assisted colectomy versus open colectomy for treatment of non-metastatic colon cancer: a randomised trial. Lancet 359:2224–2229PubMedCrossRef Lacy AM, Garcia-Valdecasas JC, Delgado S, Castells A, Taura P, Pique JM, Visa J (2002) Laparoscopic assisted colectomy versus open colectomy for treatment of non-metastatic colon cancer: a randomised trial. Lancet 359:2224–2229PubMedCrossRef
27.
go back to reference Lee SW, Gleason N, Blanco I, Asi ZK, Whelan RL (2002) Higher colon cancer tumor proliferative index and lower tumor cell death rate in mice undergoing laparotomy versus insufflation. Surg Endosc 16:36–39PubMedCrossRef Lee SW, Gleason N, Blanco I, Asi ZK, Whelan RL (2002) Higher colon cancer tumor proliferative index and lower tumor cell death rate in mice undergoing laparotomy versus insufflation. Surg Endosc 16:36–39PubMedCrossRef
28.
go back to reference Maitra A, Yashima K, Rathi A, Timmons CF, Rogers BB, Shay JW, Gazdar AF (1999) The RNA component of telomerase as a marker of biologic potential and clinical outcome in childhood neuroblastic tumors. Cancer 85:741–749 PubMedCrossRef Maitra A, Yashima K, Rathi A, Timmons CF, Rogers BB, Shay JW, Gazdar AF (1999) The RNA component of telomerase as a marker of biologic potential and clinical outcome in childhood neuroblastic tumors. Cancer 85:741–749 PubMedCrossRef
30.
go back to reference Mathew G, Watson DI, Rofe AM, Ellis T, Jamieson GG (1997) Adverse impact of pneumoperitoneum on intraperitoneal implantation and growth of tumour cell suspension in an experimental model. Aust NZ J Surg 67:289–292CrossRef Mathew G, Watson DI, Rofe AM, Ellis T, Jamieson GG (1997) Adverse impact of pneumoperitoneum on intraperitoneal implantation and growth of tumour cell suspension in an experimental model. Aust NZ J Surg 67:289–292CrossRef
31.
go back to reference Metzelder ML, Kuebler JF, Shimotakahara A, Glueer S, Grigull L, Ure BM (2007) Role of diagnostic and ablative minimally invasive surgery for pediatric malignancies. Cancer 109:2341–2348CrossRef Metzelder ML, Kuebler JF, Shimotakahara A, Glueer S, Grigull L, Ure BM (2007) Role of diagnostic and ablative minimally invasive surgery for pediatric malignancies. Cancer 109:2341–2348CrossRef
32.
go back to reference Neuhaus SJ, Watson DI (2004) Pneumoperitoneum and peritoneal surface changes: a review. Surg Endosc 18:1316–1322PubMedCrossRef Neuhaus SJ, Watson DI (2004) Pneumoperitoneum and peritoneal surface changes: a review. Surg Endosc 18:1316–1322PubMedCrossRef
33.
go back to reference Petty JK, Bensard DD, Partrick DA, Hendrickson RJ, Albano EA, Karrer FM (2006) Resection of neurogenic tumors in children: is thoracoscopy superior to thoracotomy? J Am Coll Surg 203:699–703PubMedCrossRef Petty JK, Bensard DD, Partrick DA, Hendrickson RJ, Albano EA, Karrer FM (2006) Resection of neurogenic tumors in children: is thoracoscopy superior to thoracotomy? J Am Coll Surg 203:699–703PubMedCrossRef
34.
go back to reference Sartorelli KH, Partrick D, Meagher DP (1996) Port-site recurrence after thoracoscopic resection of pulmonary metastasis owing to osteogenic sarcoma. J Pediatr Surg 31:1443–1444PubMedCrossRef Sartorelli KH, Partrick D, Meagher DP (1996) Port-site recurrence after thoracoscopic resection of pulmonary metastasis owing to osteogenic sarcoma. J Pediatr Surg 31:1443–1444PubMedCrossRef
35.
go back to reference Schmidt AI, Reismann M, Kubler JF, Vieten G, Bangen C, Shimotakahara A, Gluer S, Nustede R, Ure BM (2006) Exposure to carbon dioxide and helium reduces in vitro proliferation of pediatric tumor cells. Pediatr Surg Int 22:72–77PubMedCrossRef Schmidt AI, Reismann M, Kubler JF, Vieten G, Bangen C, Shimotakahara A, Gluer S, Nustede R, Ure BM (2006) Exposure to carbon dioxide and helium reduces in  vitro proliferation of pediatric tumor cells. Pediatr Surg Int 22:72–77PubMedCrossRef
36.
go back to reference Shimotakahara A, Kuebler JF, Vieten G, Metzelder ML, Petersen C, Ure BM (2007) Pleural macrophages are the dominant cell population in the thoracic cavity with an inflammatory cytokine profile similar to peritoneal macrophages. Pediatr Surg Int 23:447–451PubMedCrossRef Shimotakahara A, Kuebler JF, Vieten G, Metzelder ML, Petersen C, Ure BM (2007) Pleural macrophages are the dominant cell population in the thoracic cavity with an inflammatory cytokine profile similar to peritoneal macrophages. Pediatr Surg Int 23:447–451PubMedCrossRef
37.
go back to reference Southall JC, Lee SW, Allendorf JD, Bessler M, Whelan RL (1998) Colon adenocarcinoma and B-16 melanoma grow larger following laparotomy versus pneumoperitoneum in a murine model. Dis Colon Rectum 41:564–569PubMedCrossRef Southall JC, Lee SW, Allendorf JD, Bessler M, Whelan RL (1998) Colon adenocarcinoma and B-16 melanoma grow larger following laparotomy versus pneumoperitoneum in a murine model. Dis Colon Rectum 41:564–569PubMedCrossRef
38.
go back to reference Spurbeck WW, Davidoff AM, Lobe TE, Rao BN, Schropp KP, Shochat SJ (2004) Minimally invasive surgery in pediatric cancer patients. Ann Surg Oncol 11:340–343PubMedCrossRef Spurbeck WW, Davidoff AM, Lobe TE, Rao BN, Schropp KP, Shochat SJ (2004) Minimally invasive surgery in pediatric cancer patients. Ann Surg Oncol 11:340–343PubMedCrossRef
39.
go back to reference Suita S, Tajiri T, Higashi M, Tanaka S, Kinoshita Y, Takahashi Y, Tatsuta K (2007) Insights into infant neuroblastomas based on an analysis of neuroblastoma detected by mass screening at 6 months of age in Japan. Eur J Pediatr Surg 17:23–28PubMedCrossRef Suita S, Tajiri T, Higashi M, Tanaka S, Kinoshita Y, Takahashi Y, Tatsuta K (2007) Insights into infant neuroblastomas based on an analysis of neuroblastoma detected by mass screening at 6 months of age in Japan. Eur J Pediatr Surg 17:23–28PubMedCrossRef
40.
go back to reference Till H, Metzger R, Bergmann F, Haeberle B, Schaeffer K, von Schweinitz D, Gahlen J, Prosst RL (2006) Tumor model for laparoscopy in pediatric oncology: subperitoneal inoculation of human hepatoblastoma cells in nude rats. Eur J Pediatr Surg 16:231–234PubMedCrossRef Till H, Metzger R, Bergmann F, Haeberle B, Schaeffer K, von Schweinitz D, Gahlen J, Prosst RL (2006) Tumor model for laparoscopy in pediatric oncology: subperitoneal inoculation of human hepatoblastoma cells in nude rats. Eur J Pediatr Surg 16:231–234PubMedCrossRef
41.
go back to reference 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 16:836–842PubMedCrossRef 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 16:836–842PubMedCrossRef
42.
go back to reference Warmann S, Fuchs J, Jesch NK, Schrappe M, Ure BM (2003) A prospective study of minimally invasive techniques in pediatric surgical oncology: preliminary report. Med Pediatr Oncol 40:155–157PubMedCrossRef Warmann S, Fuchs J, Jesch NK, Schrappe M, Ure BM (2003) A prospective study of minimally invasive techniques in pediatric surgical oncology: preliminary report. Med Pediatr Oncol 40:155–157PubMedCrossRef
43.
go back to reference Ziegler MM, Naito H, McCarrick JW III, Topalian SL, Ricci JL, Ruben GD, Cooper A, Krasna IH (1986) C-1300 murine neuroblastoma: a suitable animal model of human disease. In:Brooks EF (ed) Malignant tumors in childhood. University of Texas, Austin, pp 114–126 Ziegler MM, Naito H, McCarrick JW III, Topalian SL, Ricci JL, Ruben GD, Cooper A, Krasna IH (1986) C-1300 murine neuroblastoma: a suitable animal model of human disease. In:Brooks EF (ed) Malignant tumors in childhood. University of Texas, Austin, pp 114–126
44.
go back to reference Ziegler MM, Ishizu H, Nagabuchi E, Takada N, Arya G (1997) A comparative review of the immunology of murine neuroblastoma and human neuroblastoma. Cancer 79:1757–1766PubMedCrossRef Ziegler MM, Ishizu H, Nagabuchi E, Takada N, Arya G (1997) A comparative review of the immunology of murine neuroblastoma and human neuroblastoma. Cancer 79:1757–1766PubMedCrossRef
Metadata
Title
CO2 pneumoperitoneum increases systemic but not local tumor spread after intraperitoneal murine neuroblastoma spillage in mice
Authors
Martin Metzelder
Joachim Kuebler
Akihiro Shimotakahara
Gertrud Vieten
Reinhard von Wasielewski
Benno Manfred Ure
Publication date
01-12-2008
Publisher
Springer-Verlag
Published in
Surgical Endoscopy / Issue 12/2008
Print ISSN: 0930-2794
Electronic ISSN: 1432-2218
DOI
https://doi.org/10.1007/s00464-008-9778-2

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