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

  • Shinsuke Kanekiyo
  • Shigeru Takeda
  • Masahito Tsutsui
  • Mitsuo Nishiyama
  • Masahiro Kitahara
  • Yoshitaro Shindo
  • Yukio Tokumitsu
  • Shinobu Tomochika
  • Yoshihiro Tokuhisa
  • Michihisa Iida
  • Kazuhiko Sakamoto
  • Nobuaki Suzuki
  • Shigeru Yamamoto
  • Shigefumi Yoshino
  • Shoichi Hazama
  • Tomio Ueno
  • Hiroaki Nagano
Article

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.

Keywords

Esophageal cancer Minimally invasive surgery Cytokines Surgical stress Prone position 

Notes

Acknowledgements

The study was supported by JSPS KAKENHI Grant Number 24791379.

Compliance with ethical standards

Disclosures

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.

References

  1. 1.
    Cancer Registry and Statistics. Cancer Information Service NCC, Japan. http://ganjoho.jp/public/index.html
  2. 2.
    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 100:95–104CrossRefPubMedGoogle Scholar
  3. 3.
    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 13:110–137CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Biere SS, Cuesta MA, van der Peet DL (2009) Minimally invasive versus open esophagectomy for cancer: a systematic review and meta-analysis. Minerva Chir 64:121–133PubMedGoogle Scholar
  5. 5.
    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 379:1887–1892CrossRefPubMedGoogle Scholar
  6. 6.
    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 4:462–464PubMedPubMedCentralGoogle Scholar
  7. 7.
    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 4:465–466PubMedPubMedCentralGoogle Scholar
  8. 8.
    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 11:310CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    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 13:230CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    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 2012:683213Google Scholar
  11. 11.
    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 255:197–203CrossRefPubMedGoogle Scholar
  12. 12.
    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 24:2965–2973CrossRefPubMedGoogle Scholar
  13. 13.
    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 196CrossRefPubMedGoogle Scholar
  14. 14.
    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 26:53–59CrossRefPubMedGoogle Scholar
  15. 15.
    Madbouly KM, Senagore AJ, Delaney CP (2010) Endogenous morphine levels after laparoscopic versus open colectomy. Br J Surg 97:759–764CrossRefPubMedGoogle Scholar
  16. 16.
    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 100:600–609CrossRefPubMedGoogle Scholar
  17. 17.
    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 99:1554–1561CrossRefPubMedGoogle Scholar
  18. 18.
    Fukunaga T, Kidokoro A, Fukunaga M, Nagakari K, Suda M, Yoshikawa S (2001) Kinetics of cytokines and PMN-E in thoracoscopic esophagectomy. Surg Endosc 15:1484–1487CrossRefPubMedGoogle Scholar
  19. 19.
    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 151:667–673CrossRefPubMedGoogle Scholar
  20. 20.
    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 46:1305–1310CrossRefPubMedGoogle Scholar
  21. 21.
    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 192:322–329CrossRefPubMedGoogle Scholar
  22. 22.
    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 22:783–790CrossRefPubMedGoogle Scholar
  23. 23.
    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 39:682–688CrossRefPubMedGoogle Scholar
  24. 24.
    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 34:2830–2836CrossRefPubMedGoogle Scholar
  25. 25.
    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 104:623–628CrossRefPubMedGoogle Scholar
  26. 26.
    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 85:137–142CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    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 11:4–6PubMedGoogle Scholar
  28. 28.
    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 38:131–137CrossRefPubMedGoogle Scholar
  29. 29.
    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 24:1621–1629CrossRefPubMedGoogle Scholar
  30. 30.
    Dantoc M, Cox MR, Eslick GD (2012) Evidence to support the use of minimally invasive esophagectomy for esophageal cancer: a meta-analysis. Arch Surg 147:768–776CrossRefPubMedGoogle Scholar
  31. 31.
    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 37:195–201PubMedGoogle Scholar
  32. 32.
    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 102:169–178CrossRefPubMedGoogle Scholar
  33. 33.
    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 94:767–773CrossRefPubMedGoogle Scholar
  34. 34.
    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 4:298–304CrossRefPubMedGoogle Scholar
  35. 35.
    Hirai T, Matsumoto H, Kubota H, Yamaguchi Y (2014) Regulating surgical oncotaxis to improve the outcomes in cancer patients. Surg Today 44:804–811CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  • Shinsuke Kanekiyo
    • 1
  • Shigeru Takeda
    • 1
  • Masahito Tsutsui
    • 1
  • Mitsuo Nishiyama
    • 1
  • Masahiro Kitahara
    • 1
  • Yoshitaro Shindo
    • 1
  • Yukio Tokumitsu
    • 1
  • Shinobu Tomochika
    • 1
  • Yoshihiro Tokuhisa
    • 1
  • Michihisa Iida
    • 1
  • Kazuhiko Sakamoto
    • 1
  • Nobuaki Suzuki
    • 1
  • Shigeru Yamamoto
    • 1
  • Shigefumi Yoshino
    • 2
  • Shoichi Hazama
    • 3
  • Tomio Ueno
    • 4
  • Hiroaki Nagano
    • 1
  1. 1.Department of Gastroenterological, Breast and Endocrine SurgeryYamaguchi University Graduate School of MedicineUbeJapan
  2. 2.Oncology CenterYamaguchi University HospitalUbeJapan
  3. 3.Department of Translational Research and Developmental Therapeutics against CancerYamaguchi University School of MedicineUbeJapan
  4. 4.Department of Digestive SurgeryKawasaki Medical SchoolKurashikiJapan

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