Skip to main content
Top
Published in: World Journal of Surgery 7/2018

01-07-2018 | Original Scientific Report

Locoregional Tumor Extension and Preoperative Smoking are Significant Risk Factors for Early Recurrence After Esophagectomy for Cancer

Authors: Styliani Mantziari, Pierre Allemann, Michael Winiker, Nicolas Demartines, Markus Schäfer

Published in: World Journal of Surgery | Issue 7/2018

Login to get access

Abstract

Background

Tumor recurrence during the first year after oncological esophagectomy has been reported in up to 17–66% of patients. However, little is known as to the risk factors potentially associated with this adverse outcome. The aim of this retrospective observational study was to identify clinically relevant parameters associated with early recurrence.

Methods

All patients with squamous cell cancer or adenocarcinoma of the esophagus or gastroesophageal junction, operated with curative intent in our center from 2000 to 2014, were screened for this study. Univariate analysis was conducted to identify variables potentially associated with early recurrence, and clinically relevant parameters with P < 0.1 were included in multiple logistic regression. Survival analyses were conducted with the Kaplan–Meier method. Significance threshold was set at P < 0.05.

Results

Among the 164 included patients, 46 (28%) presented early recurrence. Eight patients (17.4%) had locoregional and 38 patients (82.6%) metastatic recurrence. Advanced T and N stages, lymph node capsular effraction, a high positive-to-resected lymph node ratio, positive resection margins, poor response to neoadjuvant treatment, preoperative active smoking, malnutrition and dysphagia were associated with early recurrence on a univariate level. In multivariable analysis, preoperative smoking (OR 2.76, 95% CI 1.28–6.17), pT stage (OR 1.72, 95% CI 1.18–2.58) and an increased positive-to-resected lymph node ratio (OR 6.72, 95% CI 1.08–48.51) remained independently associated with ER.

Conclusion

Our study identified both patient- and tumor-related parameters as risk factors for early recurrence after oncological esophagectomy. Of particular interest, active smoking was significantly associated with this adverse outcome, highlighting the importance of preoperative smoking cessation.
Appendix
Available only for authorised users
Literature
1.
go back to reference Mariette C, Piessen G, Triboulet J (2007) Therapeutic strategies in oesophageal carcinoma: role of surgery and other modalities. Lancet Oncol 8(6):545–553CrossRefPubMed Mariette C, Piessen G, Triboulet J (2007) Therapeutic strategies in oesophageal carcinoma: role of surgery and other modalities. Lancet Oncol 8(6):545–553CrossRefPubMed
2.
go back to reference van Hagen P, Hulshof MC, van Lanschot JJ et al (2012) Preoperative chemoradiotherapy for esophageal or junctional cancer. N Engl J Med 366(22):2074–2084CrossRefPubMed van Hagen P, Hulshof MC, van Lanschot JJ et al (2012) Preoperative chemoradiotherapy for esophageal or junctional cancer. N Engl J Med 366(22):2074–2084CrossRefPubMed
3.
go back to reference Shapiro J, van Lanschot JJB, Hulshof MCCM et al (2015) Neoadjuvant chemoradiotherapy plus surgery versus surgery alone for oesophageal or junctional cancer (CROSS): Long-term results of a randomised controlled trial. Lancet Oncol 16(9):1090–1098CrossRefPubMed Shapiro J, van Lanschot JJB, Hulshof MCCM et al (2015) Neoadjuvant chemoradiotherapy plus surgery versus surgery alone for oesophageal or junctional cancer (CROSS): Long-term results of a randomised controlled trial. Lancet Oncol 16(9):1090–1098CrossRefPubMed
4.
go back to reference Allum WH, Stenning SP, Bancewicz J, Clark PI, Langley RE (2009) Long-term results of a randomized trial of surgery with or without preoperative chemotherapy in esophageal cancer. J Clin Oncol 27(30):5062–5067CrossRefPubMed Allum WH, Stenning SP, Bancewicz J, Clark PI, Langley RE (2009) Long-term results of a randomized trial of surgery with or without preoperative chemotherapy in esophageal cancer. J Clin Oncol 27(30):5062–5067CrossRefPubMed
5.
go back to reference Abate E, DeMeester SR, Zehetner J et al (2010) Recurrence after esophagectomy for adenocarcinoma: defining optimal follow-up intervals and testing. J Am Coll Surg 210(4):428–435CrossRefPubMed Abate E, DeMeester SR, Zehetner J et al (2010) Recurrence after esophagectomy for adenocarcinoma: defining optimal follow-up intervals and testing. J Am Coll Surg 210(4):428–435CrossRefPubMed
6.
go back to reference Davies AR, Pillai A, Sinha P et al (2014) Factors associated with early recurrence and death after esophagectomy for cancer. J Surg Oncol 109(5):459–464CrossRefPubMed Davies AR, Pillai A, Sinha P et al (2014) Factors associated with early recurrence and death after esophagectomy for cancer. J Surg Oncol 109(5):459–464CrossRefPubMed
7.
go back to reference Dresner SM, Griffin SM (2000) Pattern of recurrence following radical oesophagectomy with two-field lymphadenectomy. Br J Surg 87(10):1426–1433CrossRefPubMed Dresner SM, Griffin SM (2000) Pattern of recurrence following radical oesophagectomy with two-field lymphadenectomy. Br J Surg 87(10):1426–1433CrossRefPubMed
8.
go back to reference Stiles BM, Salzler GG, Nasar A et al (2015) Clinical predictors of early cancer-related mortality following neoadjuvant therapy and oesophagectomy. Eur J Cardio-Thoracic Surg 48:1–6CrossRef Stiles BM, Salzler GG, Nasar A et al (2015) Clinical predictors of early cancer-related mortality following neoadjuvant therapy and oesophagectomy. Eur J Cardio-Thoracic Surg 48:1–6CrossRef
9.
go back to reference Mariette C, Balon JM, Piessen G, Fabre S, Van Seuningen I, Triboulet JP (2003) Pattern of recurrence following complete resection of esophageal carcinoma and factors predictive of recurrent disease. Cancer 97(7):1616–1623CrossRefPubMed Mariette C, Balon JM, Piessen G, Fabre S, Van Seuningen I, Triboulet JP (2003) Pattern of recurrence following complete resection of esophageal carcinoma and factors predictive of recurrent disease. Cancer 97(7):1616–1623CrossRefPubMed
10.
go back to reference Deldycke A, Van Daele E, Ceelen W, Van Nieuwenhove Y, Pattyn P (2016) Functional outcome after Ivor Lewis esophagectomy for cancer. J Surg Oncol 113(1):24–28CrossRefPubMed Deldycke A, Van Daele E, Ceelen W, Van Nieuwenhove Y, Pattyn P (2016) Functional outcome after Ivor Lewis esophagectomy for cancer. J Surg Oncol 113(1):24–28CrossRefPubMed
11.
go back to reference Derogar M, Lagergren P (2012) Health-related quality of life among 5-year survivors of esophageal cancer surgery: a prospective population-based study. J Clin Oncol 30(4):413–418CrossRefPubMed Derogar M, Lagergren P (2012) Health-related quality of life among 5-year survivors of esophageal cancer surgery: a prospective population-based study. J Clin Oncol 30(4):413–418CrossRefPubMed
12.
go back to reference Ogilvie AL, Dronfield MW, Ferguson R, Atkinson M (1982) Palliative intubation of oesophagogastric neoplasms at fibreoptic endoscopy. Gut 23(12):1060–1067CrossRefPubMedPubMedCentral Ogilvie AL, Dronfield MW, Ferguson R, Atkinson M (1982) Palliative intubation of oesophagogastric neoplasms at fibreoptic endoscopy. Gut 23(12):1060–1067CrossRefPubMedPubMedCentral
13.
go back to reference von Elm E, Altman D, Egger M, Pocock S, Gotzsche P, Vandenbroucke J (2007) The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. Lancet 370:1453–1457CrossRef von Elm E, Altman D, Egger M, Pocock S, Gotzsche P, Vandenbroucke J (2007) The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. Lancet 370:1453–1457CrossRef
14.
go back to reference Lordick F, Mariette C, Haustermans K et al (2016) Oesophageal cancer: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol. 27:50–57CrossRef Lordick F, Mariette C, Haustermans K et al (2016) Oesophageal cancer: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol. 27:50–57CrossRef
15.
go back to reference Varghese TK Jr, Hofstetter WL, Rizk NP et al (2013) The society of thoracic surgeons guidelines on the diagnosis and staging of patients with esophageal cancer. Ann Thorac Surg 96(1):346–356CrossRefPubMed Varghese TK Jr, Hofstetter WL, Rizk NP et al (2013) The society of thoracic surgeons guidelines on the diagnosis and staging of patients with esophageal cancer. Ann Thorac Surg 96(1):346–356CrossRefPubMed
16.
go back to reference Sobin L, Gospodarowicz M, Wittekind C (2009) TNM classification of malignant tumours, 7th edn. Wiley, Hoboken Sobin L, Gospodarowicz M, Wittekind C (2009) TNM classification of malignant tumours, 7th edn. Wiley, Hoboken
17.
go back to reference Kondrup J, Allison SP, Elia M, Vellas B, Plauth M (2003) ESPEN guidelines for nutrition screening 2002. Clin Nutr 22(4):415–421CrossRefPubMed Kondrup J, Allison SP, Elia M, Vellas B, Plauth M (2003) ESPEN guidelines for nutrition screening 2002. Clin Nutr 22(4):415–421CrossRefPubMed
18.
go back to reference Mandard AM, Dalibard F, Mandard JC et al (1994) Pathologic assessment of tumor regression after preoperative chemoradiotherapy of esophageal carcinoma: clinicopathologic correlations. Cancer 73(11):2680–2686CrossRefPubMed Mandard AM, Dalibard F, Mandard JC et al (1994) Pathologic assessment of tumor regression after preoperative chemoradiotherapy of esophageal carcinoma: clinicopathologic correlations. Cancer 73(11):2680–2686CrossRefPubMed
19.
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(2):205–213CrossRefPubMedPubMedCentral 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(2):205–213CrossRefPubMedPubMedCentral
20.
go back to reference Schemper M, Smith TL (1996) A note on quantifying follow-up in studies of failure time. Control Clin Trials 17:343CrossRefPubMed Schemper M, Smith TL (1996) A note on quantifying follow-up in studies of failure time. Control Clin Trials 17:343CrossRefPubMed
21.
go back to reference Zhu Z-J, Hu Y, Zhao Y-F, Chen X-Z, Chen L-Q, Chen Y-T (2011) Early recurrence and death after esophagectomy in patients with esophageal squamous cell carcinoma. Ann Thorac Surg 91(5):1502–1508CrossRefPubMed Zhu Z-J, Hu Y, Zhao Y-F, Chen X-Z, Chen L-Q, Chen Y-T (2011) Early recurrence and death after esophagectomy in patients with esophageal squamous cell carcinoma. Ann Thorac Surg 91(5):1502–1508CrossRefPubMed
22.
go back to reference van Heijl M, Sprangers MAG, de Boer AGEM et al (2010) Preoperative and early postoperative quality of life predict survival in potentially curable patients with esophageal cancer. Ann Surg Oncol 17(1):23–30CrossRefPubMed van Heijl M, Sprangers MAG, de Boer AGEM et al (2010) Preoperative and early postoperative quality of life predict survival in potentially curable patients with esophageal cancer. Ann Surg Oncol 17(1):23–30CrossRefPubMed
23.
go back to reference Mal F, Perniceni T, Levard H, Denet C, Validire P, Gayet B (2005) Pre-operative predictive factors of early recurrence after resection of adenocarcinoma of the esophagus and cardia. Gastroenterol Clin Biol 29(12):1275–1278CrossRefPubMed Mal F, Perniceni T, Levard H, Denet C, Validire P, Gayet B (2005) Pre-operative predictive factors of early recurrence after resection of adenocarcinoma of the esophagus and cardia. Gastroenterol Clin Biol 29(12):1275–1278CrossRefPubMed
24.
go back to reference Kosugi S-I, Kanda T, Yajima K, Ishikawa T, Hatakeyama K (2011) Risk factors that influence early death due to cancer recurrence after extended radical esophagectomy with three-field lymph node dissection. Ann Surg Oncol 18(10):2961–2967CrossRefPubMed Kosugi S-I, Kanda T, Yajima K, Ishikawa T, Hatakeyama K (2011) Risk factors that influence early death due to cancer recurrence after extended radical esophagectomy with three-field lymph node dissection. Ann Surg Oncol 18(10):2961–2967CrossRefPubMed
25.
go back to reference Yoshida N, Baba Y, Shigaki H et al (2016) Risk factors of early recurrence within 6 months after esophagectomy following neoadjuvant chemotherapy for resectable advanced esophageal squamous cell carcinoma. Int J Clin Oncol 21(6):1071–1078 Epub 2016 Jun 2 CrossRefPubMed Yoshida N, Baba Y, Shigaki H et al (2016) Risk factors of early recurrence within 6 months after esophagectomy following neoadjuvant chemotherapy for resectable advanced esophageal squamous cell carcinoma. Int J Clin Oncol 21(6):1071–1078 Epub 2016 Jun 2 CrossRefPubMed
26.
go back to reference Lagarde SM, Reitsma JB, Maris AKD et al (2008) Preoperative prediction of the occurrence and severity of complications after esophagectomy for cancer with use of a nomogram. Ann Thorac Surg 85(6):1938–1945CrossRefPubMed Lagarde SM, Reitsma JB, Maris AKD et al (2008) Preoperative prediction of the occurrence and severity of complications after esophagectomy for cancer with use of a nomogram. Ann Thorac Surg 85(6):1938–1945CrossRefPubMed
27.
go back to reference Lerut T, Moons J, Coosemans W et al (2009) Postoperative complications after transthoracic esophagectomy for cancer of the esophagus and gastroesophageal junction are correlated with early cancer recurrence: role of systematic grading of complications using the modified Clavien classification. Ann Surg 250(5):798–807CrossRefPubMed Lerut T, Moons J, Coosemans W et al (2009) Postoperative complications after transthoracic esophagectomy for cancer of the esophagus and gastroesophageal junction are correlated with early cancer recurrence: role of systematic grading of complications using the modified Clavien classification. Ann Surg 250(5):798–807CrossRefPubMed
28.
go back to reference Stratton RJ, Elia M (2006) Deprivation linked to malnutrition risk and mortality in hospital. Br J Nutr 96(5):870–876CrossRefPubMed Stratton RJ, Elia M (2006) Deprivation linked to malnutrition risk and mortality in hospital. Br J Nutr 96(5):870–876CrossRefPubMed
29.
go back to reference Mariette C, De Botton ML, Piessen G (2012) Surgery in esophageal and gastric cancer patients: what is the role for nutrition support in your daily practice? Ann Surg Oncol 19(7):2128–2134CrossRefPubMed Mariette C, De Botton ML, Piessen G (2012) Surgery in esophageal and gastric cancer patients: what is the role for nutrition support in your daily practice? Ann Surg Oncol 19(7):2128–2134CrossRefPubMed
30.
31.
go back to reference Mele A, Mehta P, Slanetz PJ et al (2017) Breast-conserving surgery alone for ductal carcinoma in situ: factors associated with increased risk of local recurrence. Ann Surg Oncol 24(5):1221–1226CrossRefPubMed Mele A, Mehta P, Slanetz PJ et al (2017) Breast-conserving surgery alone for ductal carcinoma in situ: factors associated with increased risk of local recurrence. Ann Surg Oncol 24(5):1221–1226CrossRefPubMed
32.
go back to reference Rink M, Furberg H, Zabor EC et al (2013) Impact of smoking and smoking cessation on oncologic outcomes in primary non-muscle-invasive bladder cancer. Eur Urol 63(4):724–732CrossRefPubMed Rink M, Furberg H, Zabor EC et al (2013) Impact of smoking and smoking cessation on oncologic outcomes in primary non-muscle-invasive bladder cancer. Eur Urol 63(4):724–732CrossRefPubMed
33.
go back to reference Shui IM, Wong C-J, Zhao S et al (2016) Prostate tumor DNA methylation is associated with cigarette smoking and adverse prostate cancer outcomes. Cancer 122(14):2168–2177CrossRefPubMedPubMedCentral Shui IM, Wong C-J, Zhao S et al (2016) Prostate tumor DNA methylation is associated with cigarette smoking and adverse prostate cancer outcomes. Cancer 122(14):2168–2177CrossRefPubMedPubMedCentral
34.
go back to reference Lee KWK, Pausova Z (2013) Cigarette smoking and DNA methylation. Front Genet 17(4):132 Lee KWK, Pausova Z (2013) Cigarette smoking and DNA methylation. Front Genet 17(4):132
35.
go back to reference Kaz AM, Grady WM, Stachler MD, Bass AJ (2015) Genetic and epigenetic alterations in Barrett’s esophagus and esophageal adenocarcinoma. Gastroenterol Clin North Am 44(2):473–489CrossRefPubMedPubMedCentral Kaz AM, Grady WM, Stachler MD, Bass AJ (2015) Genetic and epigenetic alterations in Barrett’s esophagus and esophageal adenocarcinoma. Gastroenterol Clin North Am 44(2):473–489CrossRefPubMedPubMedCentral
36.
go back to reference Zheng Y, Cao X, Wen J et al (2015) Smoking affects treatment outcome in patients with resected esophageal squamous cell carcinoma who received chemotherapy. PLoS ONE 10(4):e0123246CrossRefPubMedPubMedCentral Zheng Y, Cao X, Wen J et al (2015) Smoking affects treatment outcome in patients with resected esophageal squamous cell carcinoma who received chemotherapy. PLoS ONE 10(4):e0123246CrossRefPubMedPubMedCentral
37.
go back to reference Hamano R, Miyata H, Yamasaki M et al (2011) Overexpression of miR-200c induces chemoresistance in esophageal cancers mediated through activation of the Akt signaling pathway. Clin Cancer Res 17(9):3029–3038CrossRefPubMed Hamano R, Miyata H, Yamasaki M et al (2011) Overexpression of miR-200c induces chemoresistance in esophageal cancers mediated through activation of the Akt signaling pathway. Clin Cancer Res 17(9):3029–3038CrossRefPubMed
38.
go back to reference Yoshioka A, Miyata H, Doki Y et al (2008) The activation of Akt during preoperative chemotherapy for esophageal cancer correlates with poor prognosis. Oncol Rep 19(5):1099–1107PubMed Yoshioka A, Miyata H, Doki Y et al (2008) The activation of Akt during preoperative chemotherapy for esophageal cancer correlates with poor prognosis. Oncol Rep 19(5):1099–1107PubMed
Metadata
Title
Locoregional Tumor Extension and Preoperative Smoking are Significant Risk Factors for Early Recurrence After Esophagectomy for Cancer
Authors
Styliani Mantziari
Pierre Allemann
Michael Winiker
Nicolas Demartines
Markus Schäfer
Publication date
01-07-2018
Publisher
Springer International Publishing
Published in
World Journal of Surgery / Issue 7/2018
Print ISSN: 0364-2313
Electronic ISSN: 1432-2323
DOI
https://doi.org/10.1007/s00268-017-4422-8

Other articles of this Issue 7/2018

World Journal of Surgery 7/2018 Go to the issue