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Surgical Endoscopy
Published in: Surgical Endoscopy 11/2015

01-11-2015

Laparoscopic surgery minimizes the release of circulating tumor cells compared to open surgery for hepatocellular carcinoma

Authors: Wenda Li, Xue Zhou, ZeJian Huang, Hongwei Zhang, Lei Zhang, Changzhen Shang, Yajin Chen

Published in: Surgical Endoscopy | Issue 11/2015

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Abstract

Background

The aim of this study was to determine whether tumor manipulation enhances cancer cell release from the primary tumor in HCC patients and which surgical approach, open surgery or laparoscopic resection, is superior with respect to preventing tumor cells from scattering in the blood.

Methods

A total of 26 HCC patients were prospectively randomized to receive either open surgery (n = 14) or laparoscopic surgery (n = 12). Blood samples were obtained at three time points: preoperative, postoperative, and 24 h after surgery. The CD45−/CD44+/CD90+ cells were obtained and counted using quantitative flow cytometry. The serum levels of interleukin-6 (IL-6), interleukin-8 (IL-8), and tumor necrosis factor (TNF-α) were also compared between the two groups.

Results

There was no significant difference between the laparoscopic and open groups in terms of patient characteristics. The levels of CCSCs increased immediately after surgical manipulation, and the laparoscopy group released fewer tumor cells into the blood stream. The amount of CCSCs in both groups decreased to reach a similar level 24 h after surgery. Both IL-6 and IL-8 increased after surgery, and the mean postoperative increases in IL-6 and IL-8 serum levels were significantly less in the laparoscopic group than in the open group. The TNF-α levels showed no differences at any time point.

Conclusions

Our results showed that patients with laparoscopic surgery have lower IL-6, IL-8 secretion and less CTCs, which may suggest an advantage by restricting CTCs release and a preserved immune response. Further studies are needed to investigate the relationship between the number of CCSCs after surgery and long-term survival rates.
Literature
1.
2.
Fan ST, Mau Lo C, Poon RT, Yeung C, Leung Liu C, Yuen WK, Ming Lam C, Ng KK, Ching Chan S (2011) Continuous improvement of survival outcomes of resection of hepatocellular carcinoma: a 20-year experience. Ann Surg 253:745–758CrossRefPubMed
3.
Fan ST, Yang ZF, Ho DW, Ng MN, Yu WC, Wong J (2011) Prediction of posthepatectomy recurrence of hepatocellular carcinoma by circulating cancer stem cells: a prospective study. Ann Surg 254:569–576CrossRefPubMed
4.
Allard WJ, Matera J, Miller MC, Repollet M, Connelly MC, Rao C, Tibbe AG, Uhr JW, Terstappen LW (2004) Tumor cells circulate in the peripheral blood of all major carcinomas but not in healthy subjects or patients with nonmalignant diseases. Clin Cancer Res 10:6897–6904CrossRefPubMed
5.
6.
Reya T, Morrison SJ, Clarke MF, Weissman IL (2001) Stem cells, cancer, and cancer stem cells. Nature 414:105–111CrossRefPubMed
7.
Yang ZF, Ho DW, Ng MN, Lau CK, Yu WC, Ngai P, Chu PW, Lam CT, Poon RT, Fan ST (2008) Significance of CD90+ cancer stem cells in human liver cancer. Cancer Cell 13:153–166CrossRefPubMed
8.
Yang ZF, Ngai P, Ho DW, Yu WC, Ng MN, Lau CK, Li ML, Tam KH, Lam CT, Poon RT, Fan ST (2008) Identification of local and circulating cancer stem cells in human liver cancer. Hepatology 47:919–928CrossRefPubMed
9.
Romsdahl MM, McGrath RG, Hoppe E, McGrew EA (1965) Experimental model for the study of tumor cells in the blood. Acta Cytol 9:141–145PubMed
10.
11.
Fan ZC, Yan J, Liu GD, Tan XY, Weng XF, Wu WZ, Zhou J, Wei XB (2012) Real-time monitoring of rare circulating hepatocellular carcinoma cells in an orthotopic model by in vivo flow cytometry assesses resection on metastasis. Cancer Res 72:2683–2691CrossRefPubMed
12.
Park SY, Choi GS, Park JS, Kim HJ, Ryuk JP, Choi WH (2012) Influence of surgical manipulation and surgical modality on the molecular detection of circulating tumor cells from colorectal cancer. J Korean Surg Soc 82:356–364PubMedCentralCrossRefPubMed
13.
Nguyen KT, Gamblin TC, Geller DA (2009) World review of laparoscopic liver resection-2,804 patients. Ann Surg 250:831–841CrossRefPubMed
14.
Rao A, Rao G, Ahmed I (2011) Laparoscopic left lateral liver resection should be a standard operation. Surg Endosc 25:1603–1610CrossRefPubMed
15.
Ahn KS, Han HS, Yoon YS, Cho JY (2011) Laparoscopic anatomic S4 segmentectomy for hepatocellular carcinoma. Surg Laparosc Endosc Percutan Tech 21:e183–e186CrossRefPubMed
16.
Abu Hilal M, Pearce NW (2008) Laparoscopic left lateral liver sectionectomy: a safe, efficient, reproducible technique. Dig Surg 25:305–308CrossRefPubMed
17.
Chan AC, Poon RT, Cheung TT, Chok KS, Chiu DW, Chan SC, Lo CM (2014) Laparoscopic versus open liver resection for elderly patients with malignant liver tumors: a single center experience. J Gastroenterol Hepatol 29:1279–1283CrossRefPubMed
18.
Fallahzadeh MK, Zibari GB, Hamidian Jahromi A, Chu Q, Shi R, Shokouh-Amiri H (2013) Laparoscopic versus open liver resection for benign and malignant solid liver tumors: a case-matched study. J Laparoendosc Adv Surg Tech A 23:908–911CrossRefPubMed
19.
Fancellu A, Rosman AS, Sanna V, Nigri GR, Zorcolo L, Pisano M, Melis M (2011) Meta-analysis of trials comparing minimally-invasive and open liver resections for hepatocellular carcinoma. J Surg Res 171:e33–e45CrossRefPubMed
20.
Kim H, Suh KS, Lee KW, Yi NJ, Hong G, Suh SW, Yoo T, Park MS, Choi Y, Lee HW (2013) Long-term outcome of laparoscopic versus open liver resection for hepatocellular carcinoma: a case-controlled study with propensity score matching. Surg Endosc 28:950–960CrossRefPubMed
21.
Li N, Wu YR, Wu B, Lu MQ (2012) Surgical and oncologic outcomes following laparoscopic versus open liver resection for hepatocellular carcinoma: a meta-analysis. Hepatol Res 42:51–59CrossRefPubMed
22.
Parks KR, Kuo YH, Davis JM, O’ Brien B, Hagopian EJ (2014) Laparoscopic versus open liver resection: a meta-analysis of long-term outcome. HPB (Oxford) 16:109–118CrossRef
23.
Rao AM, Ahmed I (2013) Laparoscopic versus open liver resection for benign and malignant hepatic lesions in adults. Cochrane Database Syst Rev 5:CD010162PubMed
24.
Simillis C, Constantinides VA, Tekkis PP, Darzi A, Lovegrove R, Jiao L, Antoniou A (2007) Laparoscopic versus open hepatic resections for benign and malignant neoplasms—a meta-analysis. Surgery 141:203–211CrossRefPubMed
25.
26.
Huang MT, Wei PL, Wang W, Li CJ, Lee YC, Wu CH (2009) A series of laparoscopic liver resections with or without HALS in patients with hepatic tumors. J Gastrointest Surg 13:896–906CrossRefPubMed
27.
Chen XP, Zhao H, Zhao XP (2002) Alternation of AFP-mRNA level detected in blood circulation during liver resection for HCC and its significance. World J Gastroenterol 8:818–821PubMed
28.
29.
Aselmann H, Wolfes H, Rohde F, Frerker M, Deiwick A, Jager MD, Klempnauer J, Schlitt HJ (2001) Quantification of alpha 1-fetoprotein mRNA in peripheral blood and bone marrow: a tool for perioperative evaluation of patients with hepatocellular carcinoma. Langenbecks Arch Surg 386:118–123CrossRefPubMed
30.
Xu W, Cao L, Chen L, Li J, Zhang XF, Qian HH, Kang XY, Zhang Y, Liao J, Shi LH, Yang YF, Wu MC, Yin ZF (2011) Isolation of circulating tumor cells in patients with hepatocellular carcinoma using a novel cell separation strategy. Clin Cancer Res 17:3783–3793CrossRefPubMed
31.
Wu LJ, Pan YD, Pei XY, Chen H, Nguyen S, Kashyap A, Liu J, Wu J (2012) Capturing circulating tumor cells of hepatocellular carcinoma. Cancer Lett 326:17–22CrossRefPubMed
32.
Yamashita T, Forgues M, Wang W, Kim JW, Ye Q, Jia H, Budhu A, Zanetti KA, Chen Y, Qin LX, Tang ZY, Wang XW (2008) EpCAM and alpha-fetoprotein expression defines novel prognostic subtypes of hepatocellular carcinoma. Cancer Res 68:1451–1461CrossRefPubMed
33.
de Boer CJ, van Krieken JH, Janssen-van Rhijn CM, Litvinov SV (1999) Expression of Ep-CAM in normal, regenerating, metaplastic, and neoplastic liver. J Pathol 188:201–206CrossRefPubMed
34.
Juratli MA, Sarimollaoglu M, Siegel ER, Nedosekin DA, Galanzha EI, Suen JY, Zharov VP (2013) Real-time monitoring of circulating tumor cell release during tumor manipulation using in vivo photoacoustic and fluorescent flow cytometry. Head Neck
35.
Wind J, Tuynman JB, Tibbe AG, Swennenhuis JF, Richel DJ, van Berge Henegouwen MI, Bemelman WA (2009) Circulating tumour cells during laparoscopic and open surgery for primary colonic cancer in portal and peripheral blood. Eur J Surg Oncol 35:942–950CrossRefPubMed
36.
Akiyoshi S, Mimori K, Sudo T, Tanaka F, Shibata K, Mori M (2013) Laparoscopic surgery minimizes the surgical manipulation of isolated tumor cells leading to decreased metastasis compared to open surgery for colorectal cancer. Surg Today 43:20–25CrossRefPubMed
37.
Wang SW, Sun YM (2014) The IL-6/JAK/STAT3 pathway: potential therapeutic strategies in treating colorectal cancer (review). Int J Oncol 44:1032–1040PubMed
38.
Taniguchi K, Karin M (2014) IL-6 and related cytokines as the critical lynchpins between inflammation and cancer. Semin Immunol 26:54–74CrossRefPubMed
39.
Benoy IH, Salgado R, Van Dam P, Geboers K, Van Marck E, Scharpe S, Vermeulen PB, Dirix LY (2004) Increased serum interleukin-8 in patients with early and metastatic breast cancer correlates with early dissemination and survival. Clin Cancer Res 10:7157–7162CrossRefPubMed
40.
Bachelot T, Ray-Coquard I, Menetrier-Caux C, Rastkha M, Duc A, Blay JY (2003) Prognostic value of serum levels of interleukin 6 and of serum and plasma levels of vascular endothelial growth factor in hormone-refractory metastatic breast cancer patients. Br J Cancer 88:1721–1726PubMedCentralCrossRefPubMed
41.
42.
Leibovich-Rivkin T, Liubomirski Y, Bernstein B, Meshel T, Ben-Baruch A (2013) Inflammatory factors of the tumor microenvironment induce plasticity in nontransformed breast epithelial cells: EMT, invasion, and collapse of normally organized breast textures. Neoplasia 15:1330–1346PubMedCentralCrossRefPubMed
43.
Lacy AM, Delgado S, Castells A, Prins HA, Arroyo V, Ibarzabal A, Pique JM (2008) The long-term results of a randomized clinical trial of laparoscopy-assisted versus open surgery for colon cancer. Ann Surg 248:1–7CrossRefPubMed
44.
Aminsharifi A, Salehipoor M, Arasteh H (2012) Systemic immunologic and inflammatory response after laparoscopic versus open nephrectomy: a prospective cohort trial. J Endourol 26:1231–1236CrossRefPubMed
45.
Tai LH, de Souza CT, Belanger S, Ly L, Alkayyal AA, Zhang J, Rintoul JL, Ananth AA, Lam T, Breitbach CJ, Falls TJ, Kirn DH, Bell JC, Makrigiannis AP, Auer RA (2013) Preventing postoperative metastatic disease by inhibiting surgery-induced dysfunction in natural killer cells. Cancer Res 73:97–107CrossRefPubMed
46.
Smerage JB, Budd GT, Doyle GV, Brown M, Paoletti C, Muniz M, Miller MC, Repollet MI, Chianese DA, Connelly MC, Terstappen LW, Hayes DF (2013) Monitoring apoptosis and Bcl-2 on circulating tumor cells in patients with metastatic breast cancer. Mol Oncol 7:680–692CrossRefPubMed
Metadata
Title
Laparoscopic surgery minimizes the release of circulating tumor cells compared to open surgery for hepatocellular carcinoma
Authors
Wenda Li
Xue Zhou
ZeJian Huang
Hongwei Zhang
Lei Zhang
Changzhen Shang
Yajin Chen
Publication date
01-11-2015
Publisher
Springer US
Published in
Surgical Endoscopy / Issue 11/2015
Print ISSN: 0930-2794
Electronic ISSN: 1432-2218
DOI
https://doi.org/10.1007/s00464-014-4041-5

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