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01-09-2019 | Esophagus Resection | Original Article

Inflammatory response and recurrence after minimally invasive esophagectomy

Authors: Akihiko Okamura, Kotaro Yamashita, Ryotaro Kozuki, Keita Takahashi, Tasuku Toihata, Yu Imamura, Shinji Mine, Masayuki Watanabe

Published in: Langenbeck's Archives of Surgery | Issue 6/2019

Abstract

Purpose

Esophagectomy for esophageal cancer is a very invasive surgery that induces an intense systemic inflammatory response. Postoperative infectious complications worsen survival after esophagectomy through inflammatory responses, and this study aimed to investigate the impact of the response on disease recurrence.

Methods

We assessed 230 patients who underwent curative minimally invasive esophagectomy for esophageal squamous cell carcinoma. The area under the curve of serum C-reactive protein levels from preoperative day through postoperative day 7 was defined as the cumulative magnitude of postoperative inflammatory response.

Results

Relapse-free survival was compared among quartiles of the area, and fourth quartile showed the worst relapse-free survival. Patients in the fourth quartile were the high group, and others were low group. Compared with low group (n = 173), high group (n = 57) showed significantly worse relapse-free survival and overall survival (P = 0.014 and 0.028, respectively). Multivariate analyses found that high group (P = 0.048) was an independent risk factor for recurrence but not overall survival. Higher body mass index (P < 0.001) and postoperative infections (P < 0.001) were independent risk factors to become high group. However, the influence of high group on recurrence was not affected by postoperative infections in interaction analysis (P = 0.889).

Conclusions

Postoperative intense systemic inflammatory response independently increased the risk of recurrence after curative minimally invasive esophagectomy for esophageal squamous cell carcinoma. Factors associating with intensified inflammatory response are higher body mass index and postoperative infections. Therefore, surgeons should make every effort to prevent postoperative infections to improve the long-term outcomes of patients.

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Okamura A, Takeuchi H, Matsuda S, Ogura M, Miyasho T, Nakamura R, Takahashi T, Wada N, Kawakubo H, Saikawa Y, Kitagawa Y (2015) Factors affecting cytokine change after esophagectomy for esophageal cancer. Ann Surg Oncol 22:3130–3135CrossRef

Takeuchi H, Saikawa Y, Oyama T, Ozawa S, Suda K, Wada N, Takahashi T, Nakamura R, Shigematsu N, Ando N, Kitajima M, Kitagawa Y (2010) Factors influencing the long-term survival in patients with esophageal cancer who underwent esophagectomy after chemoradiotherapy. World J Surg 34:277–284CrossRef

Booka E, Takeuchi H, Nishi T, Matsuda S, Kaburagi T, Fukuda K, Nakamura R, Takahashi T, Wada N, Kawakubo H, Omori T, Kitagawa Y (2015) The impact of postoperative complications on survivals after esophagectomy for esophageal cancer. Medicine 94:e1369CrossRef

Markar S, Gronnier C, Duhamel A, Mabrut JY, Bail JP, Carrere N, Lefevre JH, Brigand C, Vaillant JC, Adham M, Msika S, Demartines N, Nakadi IE, Meunier B, Collet D, Mariette C (2015) The impact of severe anastomotic leak on long-term survival and cancer recurrence after surgical resection for esophageal malignancy. Ann Surg 262:972–980CrossRef

Baba Y, Yoshida N, Shigaki H, Iwatsuki M, Miyamoto Y, Sakamoto Y, Watanabe M, Baba H (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

Yamashita K, Makino T, Miyata H, Miyazaki Y, Takahashi T, Kurokawa Y, Yamasaki M, Nakajima K, Takiguchi S, Mori M, Doki Y (2016) Postoperative infectious complications are associated with adverse oncologic outcomes in esophageal cancer patients undergoing preoperative chemotherapy. Ann Surg Oncol 23:2106–2114CrossRef

Kataoka K, Takeuchi H, Mizusawa J, Igaki H, Ozawa S, Abe T, Nakamura K, Kato K, Ando N, Kitagawa Y (2017) Prognostic impact of postoperative morbidity after esophagectomy for esophageal cancer: exploratory analysis of JCOG9907. Ann Surg 265:1152–1157CrossRef

Saeki H, Tsutsumi S, Tajiri H, Yukaya T, Tsutsumi R, Nishimura S, Nakaji Y, Kudou K, Akiyama S, Kasagi Y, Nakanishi R, Nakashima Y, Sugiyama M, Ohgaki K, Sonoda H, Oki E, Maehara Y (2017) Prognostic significance of postoperative complications after curative resection for patients with esophageal squamous cell carcinoma. Ann Surg 265:527–533CrossRef

Hayami M, Watanabe M, Ishizuka N, Mine S, Imamura Y, Okamura A, Kurogochi T, Yamashita K (2018) Prognostic impact of postoperative pulmonary complications following salvage esophagectomy after definitive chemoradiotherapy. J Surg Oncol 117:1251–1259CrossRef

10.

Shimada H, Fukagawa T, Haga Y, Oba K (2017) Does postoperative morbidity worsen the oncological outcome after radical surgery for gastrointestinal cancers? A systematic review of the literature. Ann Gastroenterol Surg 1:11–23CrossRef

11.

Haldar R, Ben-Eliyahu S (2018) Reducing the risk of post-surgical cancer recurrence: a perioperative anti-inflammatory anti-stress approach. Future Oncol 14:1017–1021CrossRef

12.

Matsuda S, Takeuchi H, Kawakubo H, Fukuda K, Nakamura R, Takahashi T, Wada N, Saikawa Y, Kitagawa Y (2015) Correlation between intense postoperative inflammatory response and survival of esophageal cancer patients who underwent transthoracic esophagectomy. Ann Surg Oncol 22:4453–4460CrossRef

13.

Brierley JD, Gospodarowicz MK, Wittekind C (eds) (2017) TNM classification of malignant tumors. International Union Against Cancer, 8th edn. Wiley, Oxford

14.

Kuwano H, Nishimura Y, Oyama T, Kato H, Kitagawa Y, Kusano M, Shimada H, Takiuchi H, Toh Y, Doki Y, Naomoto Y, Matsubara H, Miyazaki T, Muto M, Yanagisawa A (2015) Guidelines for diagnosis and treatment of carcinoma of the esophagus April 2012 edited by the Japan Esophageal Society. Esophagus 12:1–30CrossRef

15.

Ando N, Kato H, Igaki H, Shinoda M, Ozawa S, Shimizu H, Nakamura T, Yabusaki H, Aoyama N, Kurita A, Ikeda K, Kanda T, Tsujinaka T, Nakamura K, Fukuda H (2012) A randomized trial comparing postoperative adjuvant chemotherapy with cisplatin and 5-fluorouracil versus preoperative chemotherapy for localized advanced squamous cell carcinoma of the thoracic esophagus (JCOG9907). Ann Surg Oncol 19:68–74CrossRef

16.

Toh Y, Sakaguchi Y, Ikeda O, Adachi E, Ohgaki K, Yamashita Y, Oki E, Minami K, Okamura T (2009) The triangulating stapling technique for cervical esophagogastric anastomosis after esophagectomy. Surg Today 39:201–206CrossRef

17.

Yoshida N, Baba Y, Watanabe M, Hiyoshi Y, Ishimoto T, Iwagami S, Kurashige J, Sakamoto Y, Miyamoto Y, Baba H (2015) Triangulating stapling technique covered with the pedicled omental flap for esophagogastric anastomosis: a safe anastomosis with fewer complications. J Am Coll Surg 220:e13–e16CrossRef

18.

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

19.

Oka M, Yamamoto K, Takahashi M et al (1996) Relationship between serum levels of interleukin 6, various disease parameters and malnutrition in patients with esophageal squamous cell carcinoma. Cancer Res 56:2776–2780PubMed

20.

Wang LS, Chow KC, Wu CW (1999) Expression and up-regulation of interleukin-6 in esophageal carcinoma cells by n-sodium butyrate. Br J Cancer 80:1617–1622CrossRef

21.

Yoneda M, Fujiwara H, Furutani A et al (2013) Prognostic impact of tumor IL-6 expression after preoperative chemoradiotherapy in patients with advanced esophageal squamous cell carcinoma. Anticancer Res 33:2699–2705PubMed

22.

Ogura M, Takeuchi H, Kawakubo H, Nishi T, Fukuda K, Nakamura R, Takahashi T, Wada N, Saikawa Y, Omori T, Miyasho T, Yamada S, Kitagawa Y (2013) Clinical significance of CXCL-8/CXCR-2 network in esophageal squamous cell carcinoma. Surgery 154:512–520CrossRef

23.

Nishi T, Takeuchi H, Matsuda S, Ogura M, Kawakubo H, Fukuda K, Nakamura R, Takahashi T, Wada N, Saikawa Y, Omori T, Kitagawa Y (2015) CXCR2 expression and postoperative complications affect long-term survival in patients with esophageal cancer. World J Surg Oncol 13:232CrossRef

24.

Blaser MJ (2008) Understanding microbe-induced cancers. Cancer Prev Res (Phila) 1:15–20CrossRef

25.

Chochi K, Ichikura T, Kinoshita M, Majima T, Shinomiya N, Tsujimoto H, Kawabata T, Sugasawa H, Ono S, Seki S, Mochizuki H (2008) Helicobacter pylori augments growth of gastric cancers via the lipopolysaccharide-toll-like receptor 4 pathway whereas its lipopolysaccharide attenuates antitumor activities of human mononuclear cells. Clin Cancer Res 14:2909–2917CrossRef

26.

Bonnet M, Buc E, Sauvanet P, Darcha C, Dubois D, Pereira B, Dechelotte P, Bonnet R, Pezet D, Darfeuille-Michaud A (2014) Colonization of the human gut by E. coli and colorectal cancer risk. Clin Cancer Res 20:859–867CrossRef

27.

Watanabe M, Mine S, Nishida K, Yamada K, Shigaki H, Oya S, Matsumoto A, Kurogochi T, Okamura A, Imamura Y, Sano T (2016) Improvement in short-term outcomes after esophagectomy with a multidisciplinary perioperative care team. Esophagus 13:337–342CrossRef

28.

Miki Y, Toyokawa T, Kubo N, Tamura T, Sakurai K, Tanaka H, Muguruma K, Yashiro M, Hirakawa K, Ohira M (2017) C-reactive protein indicates early stage of postoperative infectious complications in patients following minimally invasive esophagectomy. World J Surg 41:796–803CrossRef

29.

Okamura A, Watanabe M, Fukudome I, Yamashita K, Yuda M, Hayami M, Imamura Y, Mine S (2018) Relationship between visceral obesity and postoperative inflammatory response following minimally invasive esophagectomy. World J Surg 42:3651–3657CrossRef

30.

Asti E, Bonitta G, Melloni M, Tornese S, Milito P, Sironi A, Costa E, Bonavina L (2018) Utility of C-reactive protein as predictive biomarker of anastomotic leak after minimally invasive esophagectomy. Langenbeck's Arch Surg 403:235–244CrossRef

31.

Park JK, Kim JJ, Moon SW (2017) C-reactive protein for the early prediction of anastomotic leak after esophagectomy in both neoadjuvant and non-neoadjuvant therapy case: a propensity score matching analysis. J Thorac Dis 9:3963–3702

32.

Yamashita K, Watanabe M, Mine S, Toihata T, Fukudome I, Okamura A, Yuda M, Hayami M, Ishizuka N, Imamura Y (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. Surg Endosc 32:4443–4450CrossRef

33.

Mariette C, Markar SR, Dabakuyo-Yonli TS et al (2019) Hybrid minimally invasive esophagectomy for esophageal cancer. N Engl J Med 380:152–162CrossRef

34.

Kataoka K, Takeuchi H, Mizusawa J, Ando M, Tsubosa Y, Koyanagi K, Daiko H, Matsuda S, Nakamura K, Kato K, Kitagawa Y (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

35.

Rahman SH, Evans J, Toogood GJ, Lodge PA, Prasad KR (2008) Prognostic utility of postoperative C-reactive protein for posthepatectomy liver failure. Arch Surg 143:247–253 discussion 53CrossRef

36.

Thompson D, Pepys MB, Wood SP (1999) The physiological structure of human C-reactive protein and its complex with phosphocholine. Structure 7:169–177CrossRef

37.

Watt DG, Horgan PG, McMillan DC (2015) Routine clinical markers of the magnitude of the systemic inflammatory response after elective operation: a systematic review. Surgery 157:362–380CrossRef

Title: Inflammatory response and recurrence after minimally invasive esophagectomy
Authors: Akihiko Okamura
Kotaro Yamashita
Ryotaro Kozuki
Keita Takahashi
Tasuku Toihata
Yu Imamura
Shinji Mine
Masayuki Watanabe
Publication date: 01-09-2019
Publisher: Springer Berlin Heidelberg
Keywords: Esophagus Resection
Esophagus Resection
Published in: Langenbeck's Archives of Surgery / Issue 6/2019
Print ISSN: 1435-2443
Electronic ISSN: 1435-2451
DOI: https://doi.org/10.1007/s00423-019-01818-6

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Inflammatory response and recurrence after minimally invasive esophagectomy

Abstract

Purpose

Methods

Results

Conclusions

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusions

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