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Published in: Surgical Endoscopy 11/2018

01-11-2018

Minimally invasive esophagectomy attenuates the postoperative inflammatory response and improves survival compared with open esophagectomy in patients with esophageal cancer: a propensity score matched analysis

Authors: Kotaro Yamashita, Masayuki Watanabe, Shinji Mine, Tasuku Toihata, Ian Fukudome, Akihiko Okamura, Masami Yuda, Masaru Hayami, Naoki Ishizuka, Yu Imamura

Published in: Surgical Endoscopy | Issue 11/2018

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Abstract

Background

Minimally invasive esophagectomy (MIE) for patients with esophageal cancer has recently spread worldwide. However, whether MIE is less invasive has not yet been fully evaluated.

Methods

We retrospectively analyzed data from 551 patients who underwent curative esophagectomy for esophageal cancer from 2005 to 2014: 145 patients underwent minimally invasive esophagectomy (MIE) and 406 patients underwent open transthoracic esophagectomy (OE). We compared postoperative CRP levels with propensity score matching. In addition, long-term outcomes were also compared between the groups.

Results

Operative time was significantly longer, and intraoperative blood loss was significantly less in the MIE group compared with the OE group. Although the incidence of postoperative complications was similar between the 2 groups, postoperative serum CRP levels during the first 3 and 5 postoperative days and peak postoperative CRP levels were significantly lower after MIE versus OE (MIE vs. OE, median, 15.21 vs. 19.50 mg/dl; P < 0.001). The MIE group had significantly more favorable disease-free survival (DFS) and overall survival (OS) rates than the OE group (3-year DFS rate, 81.7 vs. 69.3%, log-rank P = 0.021; 3-year OS rate, 89.9 vs. 79.2%, log-rank P = 0.007). MIE was an independent prognostic factor for patients with esophageal cancer. The incidence of regional lymph node recurrence was lower in the MIE group.

Conclusions

MIE significantly attenuated postoperative serum CRP levels compared with OE. MIE could contribute to improved survival.
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Literature
1.
go back to reference Herskovic A, Martz K, al-Sarraf M, Leichman L, Brindle J, Vaitkevicius V et al (1992) Combined chemotherapy and radiotherapy compared with radiotherapy alone in patients with cancer of the esophagus. N Engl J Med 326:1593–1598CrossRef Herskovic A, Martz K, al-Sarraf M, Leichman L, Brindle J, Vaitkevicius V et al (1992) Combined chemotherapy and radiotherapy compared with radiotherapy alone in patients with cancer of the esophagus. N Engl J Med 326:1593–1598CrossRef
2.
go back to reference Cooper JS, Guo MD, Herskovic A, Macdonald JS, Martenson JA Jr, Al-Sarraf M et al (1999) Chemoradiotherapy of locally advanced esophageal cancer: long-term follow-up of a prospective randomized trial (RTOG 85-01). Radiation Therapy Oncology Group. JAMA 281:1623–1627CrossRef Cooper JS, Guo MD, Herskovic A, Macdonald JS, Martenson JA Jr, Al-Sarraf M et al (1999) Chemoradiotherapy of locally advanced esophageal cancer: long-term follow-up of a prospective randomized trial (RTOG 85-01). Radiation Therapy Oncology Group. JAMA 281:1623–1627CrossRef
3.
go back to reference Ando N, Ozawa S, Kitagawa Y, Shinozawa Y, Kitajima M (2000) Improvement in the results of surgical treatment of advanced squamous esophageal carcinoma during 15 consecutive years. Ann Surg 232:225–232CrossRef Ando N, Ozawa S, Kitagawa Y, Shinozawa Y, Kitajima M (2000) Improvement in the results of surgical treatment of advanced squamous esophageal carcinoma during 15 consecutive years. Ann Surg 232:225–232CrossRef
4.
go back to reference Akiyama H, Tsurumaru M, Udagawa H, Kajiyama Y (1994) Radical lymph node dissection for cancer of the thoracic esophagus. Ann Surg 220:364–372 (discussion 72–3)CrossRef Akiyama H, Tsurumaru M, Udagawa H, Kajiyama Y (1994) Radical lymph node dissection for cancer of the thoracic esophagus. Ann Surg 220:364–372 (discussion 72–3)CrossRef
5.
go back to reference Tachimori Y, Ozawa S, Numasaki H, Fujishiro M, Matsubara H, Oyama T et al (2016) Comprehensive registry of esophageal cancer in Japan, 2009. Esophagus 13:110–137CrossRef Tachimori Y, Ozawa S, Numasaki H, Fujishiro M, Matsubara H, Oyama T et al (2016) Comprehensive registry of esophageal cancer in Japan, 2009. Esophagus 13:110–137CrossRef
6.
go back to reference Tachimori Y, Ozawa S, Numasaki H, Matsubara H, Shinoda M, Toh Y et al (2016) Efficacy of lymph node dissection for each station based on esophageal tumor location. Esophagus 13:138–145CrossRef Tachimori Y, Ozawa S, Numasaki H, Matsubara H, Shinoda M, Toh Y et al (2016) Efficacy of lymph node dissection for each station based on esophageal tumor location. Esophagus 13:138–145CrossRef
7.
go back to reference Mariette C, Dahan L, Mornex F, Maillard E, Thomas PA, Meunier B et al (2014) Surgery alone versus chemoradiotherapy followed by surgery for stage I and II esophageal cancer: final analysis of randomized controlled phase III trial FFCD 9901. J Clin Oncol 32:2416–2422CrossRef Mariette C, Dahan L, Mornex F, Maillard E, Thomas PA, Meunier B et al (2014) Surgery alone versus chemoradiotherapy followed by surgery for stage I and II esophageal cancer: final analysis of randomized controlled phase III trial FFCD 9901. J Clin Oncol 32:2416–2422CrossRef
8.
go back to reference Takeuchi H, Miyata H, Gotoh M, Kitagawa Y, Baba H, Kimura W et al (2014) A risk model for esophagectomy using data of 5354 patients included in a Japanese nationwide web-based database. Ann Surg 260:259–266CrossRef Takeuchi H, Miyata H, Gotoh M, Kitagawa Y, Baba H, Kimura W et al (2014) A risk model for esophagectomy using data of 5354 patients included in a Japanese nationwide web-based database. Ann Surg 260:259–266CrossRef
9.
go back to reference Matsuda S, Takeuchi H, Kawakubo H, Fukuda K, Nakamura R, Takahashi T et al (2015) Correlation between intense postoperative inflammatory response and survival of esophageal cancer patients who underwent transthoracic esophagectomy. Ann Surg Oncol 22:4453–4460CrossRef Matsuda S, Takeuchi H, Kawakubo H, Fukuda K, Nakamura R, Takahashi T et al (2015) Correlation between intense postoperative inflammatory response and survival of esophageal cancer patients who underwent transthoracic esophagectomy. Ann Surg Oncol 22:4453–4460CrossRef
10.
go back to reference Yamashita K, Makino T, Miyata H, Miyazaki Y, Takahashi T, Kurokawa Y et al (2016) Postoperative infectious complications are associated with adverse oncologic outcomes in esophageal cancer patients undergoing preoperative chemotherapy. Ann Surg Oncol 23:2106–2114CrossRef Yamashita K, Makino T, Miyata H, Miyazaki Y, Takahashi T, Kurokawa Y et al (2016) Postoperative infectious complications are associated with adverse oncologic outcomes in esophageal cancer patients undergoing preoperative chemotherapy. Ann Surg Oncol 23:2106–2114CrossRef
11.
go back to reference Baba Y, Yoshida N, Shigaki H, Iwatsuki M, Miyamoto Y, Sakamoto Y et al (2016) Prognostic impact of postoperative complications in 502 patients with surgically resected esophageal squamous cell carcinoma: a retrospective single-institution study. Ann Surg 264:305–311CrossRef Baba Y, Yoshida N, Shigaki H, Iwatsuki M, Miyamoto Y, Sakamoto Y et al (2016) Prognostic impact of postoperative complications in 502 patients with surgically resected esophageal squamous cell carcinoma: a retrospective single-institution study. Ann Surg 264:305–311CrossRef
12.
go back to reference Biere SS, van Berge Henegouwen MI, Maas KW, Bonavina L, Rosman C, Garcia JR et al (2012) Minimally invasive versus open oesophagectomy for patients with oesophageal cancer: a multicentre, open-label, randomised controlled trial. Lancet 379:1887–1892CrossRef Biere SS, van Berge Henegouwen MI, Maas KW, Bonavina L, Rosman C, Garcia JR et al (2012) Minimally invasive versus open oesophagectomy for patients with oesophageal cancer: a multicentre, open-label, randomised controlled trial. Lancet 379:1887–1892CrossRef
13.
go back to reference Takeuchi H, Miyata H, Ozawa S, Udagawa H, Osugi H, Matsubara H et al (2017) Comparison of short-term outcomes between open and minimally invasive esophagectomy for esophageal cancer using a nationwide database in Japan. Ann Surg Oncol 24:1821–1827CrossRef Takeuchi H, Miyata H, Ozawa S, Udagawa H, Osugi H, Matsubara H et al (2017) Comparison of short-term outcomes between open and minimally invasive esophagectomy for esophageal cancer using a nationwide database in Japan. Ann Surg Oncol 24:1821–1827CrossRef
14.
go back to reference Seesing MFJ, Gisbertz SS, Goense L, van Hillegersberg R, Kroon HM, Lagarde SM et al (2017) A propensity score matched analysis of open versus minimally invasive transthoracic esophagectomy in the Netherlands. Ann Surg 266:839–846CrossRef Seesing MFJ, Gisbertz SS, Goense L, van Hillegersberg R, Kroon HM, Lagarde SM et al (2017) A propensity score matched analysis of open versus minimally invasive transthoracic esophagectomy in the Netherlands. Ann Surg 266:839–846CrossRef
15.
go back to reference Weksler B, Sullivan JL (2017) Survival after esophagectomy: a propensity-matched study of different surgical approaches. Ann Thorac Surg 104:1138–1146CrossRef Weksler B, Sullivan JL (2017) Survival after esophagectomy: a propensity-matched study of different surgical approaches. Ann Thorac Surg 104:1138–1146CrossRef
16.
go back to reference Dindo D, Demartines N, Clavien PA (2004) Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 240:205–213CrossRef Dindo D, Demartines N, Clavien PA (2004) Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 240:205–213CrossRef
17.
go back to reference Katayama H, Kurokawa Y, Nakamura K, Ito H, Kanemitsu Y, Masuda N et al (2016) Extended Clavien-Dindo classification of surgical complications: Japan Clinical Oncology Group postoperative complications criteria. Surg Today 46:668–685CrossRef Katayama H, Kurokawa Y, Nakamura K, Ito H, Kanemitsu Y, Masuda N et al (2016) Extended Clavien-Dindo classification of surgical complications: Japan Clinical Oncology Group postoperative complications criteria. Surg Today 46:668–685CrossRef
18.
go back to reference Smithers BM, Gotley DC, Martin I, Thomas JM (2007) Comparison of the outcomes between open and minimally invasive esophagectomy. Ann Surg 245:232–240CrossRef Smithers BM, Gotley DC, Martin I, Thomas JM (2007) Comparison of the outcomes between open and minimally invasive esophagectomy. Ann Surg 245:232–240CrossRef
19.
go back to reference Kanekiyo S, Takeda S, Tsutsui M, Nishiyama M, Kitahara M, Shindo Y et al (2017) 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 32:1945–1953CrossRef Kanekiyo S, Takeda S, Tsutsui M, Nishiyama M, Kitahara M, Shindo Y et al (2017) 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 32:1945–1953CrossRef
20.
go back to reference 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 38:131–137CrossRef 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 38:131–137CrossRef
21.
go back to reference Scarpa M, Cavallin F, Saadeh LM, Pinto E, Alfieri R, Cagol M et al (2016) Hybrid minimally invasive esophagectomy for cancer: impact on postoperative inflammatory and nutritional status. Dis Esophagus 29:1064–1070CrossRef Scarpa M, Cavallin F, Saadeh LM, Pinto E, Alfieri R, Cagol M et al (2016) Hybrid minimally invasive esophagectomy for cancer: impact on postoperative inflammatory and nutritional status. Dis Esophagus 29:1064–1070CrossRef
22.
go back to reference Shiba H, Furukawa K, Fujiwara Y, Futagawa Y, Haruki K, Wakiyama S et al (2013) Postoperative peak serum C-reactive protein predicts outcome of hepatic resection for hepatocellular carcinoma. Anticancer Res 33:705–709PubMed Shiba H, Furukawa K, Fujiwara Y, Futagawa Y, Haruki K, Wakiyama S et al (2013) Postoperative peak serum C-reactive protein predicts outcome of hepatic resection for hepatocellular carcinoma. Anticancer Res 33:705–709PubMed
23.
go back to reference Mantovani A, Allavena P, Sica A, Balkwill F (2008) Cancer-related inflammation. Nature 454:436–444CrossRef Mantovani A, Allavena P, Sica A, Balkwill F (2008) Cancer-related inflammation. Nature 454:436–444CrossRef
24.
go back to reference McMillan DC (2009) Systemic inflammation, nutritional status and survival in patients with cancer. Curr Opin Clin Nutr Metab Care 12:223–226CrossRef McMillan DC (2009) Systemic inflammation, nutritional status and survival in patients with cancer. Curr Opin Clin Nutr Metab Care 12:223–226CrossRef
25.
go back to reference Bohle B, Pera M, Pascual M, Alonso S, Mayol X, Salvado M et al (2010) Postoperative intra-abdominal infection increases angiogenesis and tumor recurrence after surgical excision of colon cancer in mice. Surgery 147:120–126CrossRef Bohle B, Pera M, Pascual M, Alonso S, Mayol X, Salvado M et al (2010) Postoperative intra-abdominal infection increases angiogenesis and tumor recurrence after surgical excision of colon cancer in mice. Surgery 147:120–126CrossRef
26.
go back to reference Kataoka K, Takeuchi H, Mizusawa J, Ando M, Tsubosa Y, Koyanagi K et al (2016) A randomized Phase III trial of thoracoscopic versus open esophagectomy for thoracic esophageal cancer: Japan Clinical Oncology Group Study JCOG1409. Jpn J Clin Oncol 46:174–177CrossRef Kataoka K, Takeuchi H, Mizusawa J, Ando M, Tsubosa Y, Koyanagi K et al (2016) A randomized Phase III trial of thoracoscopic versus open esophagectomy for thoracic esophageal cancer: Japan Clinical Oncology Group Study JCOG1409. Jpn J Clin Oncol 46:174–177CrossRef
27.
go back to reference Watanabe M, Mine S, Nishida K, Yamada K, Shigaki H, Oya S et al (2016) Improvement in short-term outcomes after esophagectomy with a multidisciplinary perioperative care team. Esophagus 13:337–142CrossRef Watanabe M, Mine S, Nishida K, Yamada K, Shigaki H, Oya S et al (2016) Improvement in short-term outcomes after esophagectomy with a multidisciplinary perioperative care team. Esophagus 13:337–142CrossRef
Metadata
Title
Minimally invasive esophagectomy attenuates the postoperative inflammatory response and improves survival compared with open esophagectomy in patients with esophageal cancer: a propensity score matched analysis
Authors
Kotaro Yamashita
Masayuki Watanabe
Shinji Mine
Tasuku Toihata
Ian Fukudome
Akihiko Okamura
Masami Yuda
Masaru Hayami
Naoki Ishizuka
Yu Imamura
Publication date
01-11-2018
Publisher
Springer US
Published in
Surgical Endoscopy / Issue 11/2018
Print ISSN: 0930-2794
Electronic ISSN: 1432-2218
DOI
https://doi.org/10.1007/s00464-018-6187-z

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