Abstract
Background
In this study, cytokine levels, outcome, and survival rates after esophagectomy for esophageal cancer were retrospectively investigated in a propensity score-matched comparison of operative approaches between the thoracoscopic esophagectomy (TE) in the prone position and open esophagectomy (OE).
Patients and Methods
Between 2005 and 2014, TE was performed on a group of 85 patients, which was compared with a group of 104 OE cases. Eventually, 65 paired cases were matched using propensity score matching.
Results
Although the TE group underwent a significantly longer operation time than the OE group (P < 0.001), the TE group exhibited less blood loss (P < 0.001) and had a shorter postoperative hospital stay (P = 0.038) than the OE group. The serum interleukin-6 levels on ICU admission (P < 0.001) and on POD 1 (P < 0.001) were significantly lower in the TE group. The interleukin-10 levels on ICU admission (P < 0.001), POD 1 (P = 0.016), and POD 3 (P < 0.001) were also significantly lower in the TE group. Pulmonary complication was significantly lower in the TE group (P = 0.043). The 5-year PFS rates in the TE and OE groups were 70.6 and 58.7% (P = 0.328), respectively, and OS rates were 64.9 and 50.2% (P = 0.101), respectively.
Conclusion
TE compared to OE is a less invasive procedure with lower surgical stress and less pulmonary complication for the treatment of esophageal squamous cell carcinoma.
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References
Cancer Registry and Statistics. Cancer Information Service NCC, Japan. http://ganjoho.jp/public/index.html
Hii MW, Smithers BM, Gotley DC, Thomas JM, Thomson I, Martin I, Barbour AP (2013) Impact of postoperative morbidity on long-term survival after oesophagectomy. Br J Surg 100:95–104
Tachimori Y, Ozawa S, Numasaki H, Fujishiro M, Matsubara H, Oyama T, Shinoda M, Toh Y, Udagawa H, Uno T, Registration Committee for Esophageal Cancer of the Japan Esophageal S (2016) Comprehensive registry of esophageal cancer in Japan, 2009. Esophagus 13:110–137
Biere SS, Cuesta MA, van der Peet DL (2009) Minimally invasive versus open esophagectomy for cancer: a systematic review and meta-analysis. Minerva Chir 64:121–133
Biere SS, van Berge Henegouwen MI, Maas KW, Bonavina L, Rosman C, Garcia JR, Gisbertz SS, Klinkenbijl JH, Hollmann MW, de Lange ES, Bonjer HJ, van der Peet DL, Cuesta MA (2012) Minimally invasive versus open oesophagectomy for patients with oesophageal cancer: a multicentre, open-label, randomised controlled trial. Lancet 379:1887–1892
Cuesta MA, Biere SS, van Berge Henegouwen MI, van der Peet DL (2012) Randomised trial, Minimally Invasive Oesophagectomy versus open oesophagectomy for patients with resectable oesophageal cancer. J Thorac Dis 4:462–464
Khan O, Nizar S, Vasilikostas G, Wan A (2012) Minimally invasive versus open oesophagectomy for patients with oesophageal cancer: a multicentre, open-label, randomised controlled trial. J Thorac Dis 4:465–466
Briez N, Piessen G, Bonnetain F, Brigand C, Carrere N, Collet D, Doddoli C, Flamein R, Mabrut JY, Meunier B, Msika S, Perniceni T, Peschaud F, Prudhomme M, Triboulet JP, Mariette C (2011) Open versus laparoscopically-assisted oesophagectomy for cancer: a multicentre randomised controlled phase III trial—the MIRO trial. BMC Cancer 11:310
van der Sluis PC, Ruurda JP, van der Horst S, Verhage RJ, Besselink MG, Prins MJ, Haverkamp L, Schippers C, Rinkes IH, Joore HC, Ten Kate FJ, Koffijberg H, Kroese CC, van Leeuwen MS, Lolkema MP, Reerink O, Schipper ME, Steenhagen E, Vleggaar FP, Voest EE, Siersema PD, van Hillegersberg R (2012) Robot-assisted minimally invasive thoraco-laparoscopic esophagectomy versus open transthoracic esophagectomy for resectable esophageal cancer, a randomized controlled trial (ROBOT trial). Trials 13:230
Kim T, Hochwald SN, Sarosi GA, Caban AM, Rossidis G, Ben-David K (2012) Review of minimally invasive esophagectomy and current controversies. Gastroenterol Res Prac 2012:683213
Mamidanna R, Bottle A, Aylin P, Faiz O, Hanna GB (2012) Short-term outcomes following open versus minimally invasive esophagectomy for cancer in England: a population-based national study. Ann Surg 255:197–203
Noshiro H, Iwasaki H, Kobayashi K, Uchiyama A, Miyasaka Y, Masatsugu T, Koike K, Miyazaki K (2010) Lymphadenectomy along the left recurrent laryngeal nerve by a minimally invasive esophagectomy in the prone position for thoracic esophageal cancer. Surg Endosc 24:2965–2973
Mangram AJ, Horan TC, Pearson ML, Silver LC, Jarvis WR (1999) Guideline for prevention of surgical site infection, 1999. centers for disease control and prevention (CDC) Hospital Infection Control Practices Advisory Committee. Am J Infect Control 27:97–132 quiz 133–134; discussion 196
Veenhof AA, Sietses C, von Blomberg BM, van Hoogstraten IM, vd Pas MH, Meijerink WJ, vd Peet DL, vd Tol MP, Bonjer HJ, Cuesta MA (2011) The surgical stress response and postoperative immune function after laparoscopic or conventional total mesorectal excision in rectal cancer: a randomized trial. Int J Colorectal Dis 26:53–59
Madbouly KM, Senagore AJ, Delaney CP (2010) Endogenous morphine levels after laparoscopic versus open colectomy. Br J Surg 97:759–764
Orci LA, Toso C, Mentha G, Morel P, Majno PE (2013) Systematic review and meta-analysis of the effect of perioperative steroids on ischaemia-reperfusion injury and surgical stress response in patients undergoing liver resection. Br J Surg 100:600–609
Park JY, Jo MJ, Nam BH, Kim Y, Eom BW, Yoon HM, Ryu KW, Kim YW, Lee JH (2012) Surgical stress after robot-assisted distal gastrectomy and its economic implications. Br J Surg 99:1554–1561
Fukunaga T, Kidokoro A, Fukunaga M, Nagakari K, Suda M, Yoshikawa S (2001) Kinetics of cytokines and PMN-E in thoracoscopic esophagectomy. Surg Endosc 15:1484–1487
Tsujimoto H, Takahata R, Nomura S, Yaguchi Y, Kumano I, Matsumoto Y, Yoshida K, Horiguchi H, Hiraki S, Ono S, Yamamoto J, Hase K (2012) Video-assisted thoracoscopic surgery for esophageal cancer attenuates postoperative systemic responses and pulmonary complications. Surgery 151:667–673
Takemura M, Higashino M, Osugi H, Tokuhara T, Fujiwara K, Fukuda Y, Kato H, Kinoshita H (1998) Changes of serum cytokine levels after thoracoscopic esophagectomy. Jpn J Thorac Cardiovasc Surg 46:1305–1310
Abe T, Oka M, Tangoku A, Hayashi H, Yamamoto K, Yahara N, Morita K, Tabata T, Ohmoto Y (2001) Interleukin-6 production in lung tissue after transthoracic esophagectomy. J Am Coll Surg 192:322–329
Yamada T, Hisanaga M, Nakajima Y, Kanehiro H, Watanabe A, Ohyama T, Nishio K, Sho M, Nagao M, Harada A, Matsushima K, Nakano H (1998) Serum interleukin-6, interleukin-8, hepatocyte growth factor, and nitric oxide changes during thoracic surgery. World J Surg 22:783–790
Ito Y, Oda M, Tsunezuka Y, Matsumoto I, Ishikawa N, Kawakami K, Ota Y, Watanabe G (2009) Reduced perioperative immune response in video-assisted versus open surgery in a rat model. Surg Today 39:682–688
Tsujimoto H, Ono S, Sugasawa H, Ichikura T, Yamamoto J, Hase K (2010) Gastric tube reconstruction by laparoscopy-assisted surgery attenuates postoperative systemic inflammatory response after esophagectomy for esophageal cancer. World J Surg 34:2830–2836
Yamasaki M, Miyata H, Fujiwara Y, Takiguchi S, Nakajima K, Kurokawa Y, Mori M, Doki Y (2011) Minimally invasive esophagectomy for esophageal cancer: comparative analysis of open and hand-assisted laparoscopic abdominal lymphadenectomy with gastric conduit reconstruction. J Surg Oncol 104:623–628
Di Padova F, Pozzi C, Tondre MJ, Tritapepe R (1991) Selective and early increase of IL-1 inhibitors, IL-6 and cortisol after elective surgery. Clin Exp Immunol 85:137–142
Hirai T, Matsumoto H, Yamashita K, Urakami A, Iki K, Yamamura M, Tsunoda T (2005) Surgical oncotaxis–excessive surgical stress and postoperative complications contribute to enhancing tumor metastasis, resulting in a poor prognosis for cancer patients. Ann Thorac Cardiovasc Surg 11:4–6
Maas KW, Biere SS, van Hoogstraten IM, van der Peet DL, Cuesta MA (2014) Immunological changes after minimally invasive or conventional esophageal resection for cancer: a randomized trial. World J Surg 38:131–137
Nagpal K, Ahmed K, Vats A, Yakoub D, James D, Ashrafian H, Darzi A, Moorthy K, Athanasiou T (2010) Is minimally invasive surgery beneficial in the management of esophageal cancer? A meta-analysis. Surg Endosc 24:1621–1629
Dantoc M, Cox MR, Eslick GD (2012) Evidence to support the use of minimally invasive esophagectomy for esophageal cancer: a meta-analysis. Arch Surg 147:768–776
Barbic J, Ivic D, Alkhamis T, Drenjancevic D, Ivic J, Harsanji-Drenjancevic I, Turina I, Vcev A (2013) Kinetics of changes in serum concentrations of procalcitonin, interleukin-6, and C-reactive protein after elective abdominal surgery. Can it be used to detect postoperative complications? Coll Antropol 37:195–201
Galizia G, Orditura M, Romano C, Lieto E, Castellano P, Pelosio L, Imperatore V, Catalano G, Pignatelli C, De Vita F (2002) Prognostic significance of circulating IL-10 and IL-6 serum levels in colon cancer patients undergoing surgery. Clin Immunol 102:169–178
Mokart D, Merlin M, Sannini A, Brun JP, Delpero JR, Houvenaeghel G, Moutardier V, Blache JL (2005) Procalcitonin, interleukin 6 and systemic inflammatory response syndrome (SIRS): early markers of postoperative sepsis after major surgery. Br J Anaesth 94:767–773
Oka Y, Murata A, Nishijima J, Yasuda T, Hiraoka N, Ohmachi Y, Kitagawa K, Yasuda T, Toda H, Tanaka N et al (1992) Circulating interleukin 6 as a useful marker for predicting postoperative complications. Cytokine 4:298–304
Hirai T, Matsumoto H, Kubota H, Yamaguchi Y (2014) Regulating surgical oncotaxis to improve the outcomes in cancer patients. Surg Today 44:804–811
Acknowledgements
The study was supported by JSPS KAKENHI Grant Number 24791379.
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Shoichi Hazama received research funding from NEC Corporation and Toyo Kohan Corporation. All authors had full access to all of the data in the study and had final responsibility for the decision to submit for publication. Drs. Kanekiyo, Drs. Takeda, Drs. Tsutsui, Drs. Nishiyama, Drs. Kitahara, Drs. Shindo, Drs. Tokumitsu, Drs. Tomochika, Drs. Tokuhisa, Drs. Iida, Drs. Sakamoto, Drs. Suzuki, Drs. Yamamoto, Drs. Yoshino, Drs. Ueno, Drs. Nagano have no conflicts of interest or financial ties to disclose.
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Kanekiyo, S., Takeda, S., Tsutsui, M. et al. Low invasiveness of thoracoscopic esophagectomy in the prone position for esophageal cancer: a propensity score-matched comparison of operative approaches between thoracoscopic and open esophagectomy. Surg Endosc 32, 1945–1953 (2018). https://doi.org/10.1007/s00464-017-5888-z
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DOI: https://doi.org/10.1007/s00464-017-5888-z