Abstract
Background
The impact of glycemic status on esophageal squamous cell carcinoma (ESCC) prognosis is unclear.
Methods
A total of 623 patients who underwent curative subtotal esophagectomy for ESCC were evaluated. Diabetes was defined as a prior diagnosis of diabetes under treatment or newly diagnosed diabetes based on preoperative glycosylated hemoglobin (HbA1c) levels. Poor glycemic control was defined as HbA1c ≥ 7.0%, whereas good glycemic control was defined as HbA1c < 7.0%. The impact of glycemic status on long-term survival after esophagectomy was evaluated.
Results
Among the 623 patients, 64 (10.3%) had diabetes including 30 (4.8%) with poor glycemic control. Although diabetes did not influence patient survival, patients with poor glycemic control had worse overall and disease-specific survival compared with those with good glycemic control (P = 0.011 and 0.039, respectively). Comparing poor glycemic control with good glycemic control, the hazard ratios (HRs) for overall and disease-specific mortality were 1.91 (1.15–3.18) and 1.89 (1.02–3.49) in univariate analysis. After multivariate adjustment, poor glycemic control also had increased risk of overall and disease-specific mortality [HR 1.72 (95% CI 1.02–2.88) and 1.65 (95% CI 0.89–3.08), respectively]. Poor glycemic control did not increase the risk of overall or disease-specific mortality in patients with stages 0–II disease but significantly increased this risk in those with stages III–IV disease [HR 2.05 (1.14–3.69) and 1.95 (1.01–3.80), respectively].
Conclusions
Poor glycemic control is an independent risk factor for overall and disease-specific mortality after esophagectomy for advanced-stage ESCC.
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References
Steenland K, Nowlin S, Palu S (1995) Cancer incidence in the National Health and Nutrition Survey I. Follow-up data: diabetes, cholesterol, pulse and physical activity. Cancer Epidemiol Biomark Prev 4:807–811
Michels KB, Solomon CG, Hu FB et al (2003) Type 2 diabetes and subsequent incidence of breast cancer in the Nurses’ Health Study. Diabetes Care 26:1752–1758
Larsson SC, Orsini N, Wolk A (2005) Diabetes mellitus and risk of colorectal cancer: a meta-analysis. J Natl Cancer Inst 97:1679–1687
Inoue M, Iwasaki M, Otani T et al (2006) Diabetes mellitus and the risk of cancer: results from a large-scale population-based cohort study in Japan. Arch Intern Med 166:1871–1877
Larsson SC, Mantzoros CS, Wolk A (2007) Diabetes mellitus and risk of breast cancer: a meta-analysis. Int J Cancer 121:856–862
Friberg E, Orsini N, Mantzoros CS et al (2007) Diabetes mellitus and risk of endometrial cancer: a meta-analysis. Diabetologia 50:1365–1374
Ogunleye AA, Ogston SA, Morris AD et al (2009) A cohort study of the risk of cancer associated with type 2 diabetes. Br J Cancer 101:1199–1201
Ren HB, Yu T, Liu C et al (2011) Diabetes mellitus and increased risk of biliary tract cancer: systematic review and meta-analysis. Cancer Causes Control 22:837–847
Larsson SC, Wolk A (2011) Diabetes mellitus and incidence of kidney cancer: a meta-analysis of cohort studies. Diabetologia 54:1013–1018
Huang W, Ren H, Ben Q et al (2012) Risk of esophageal cancer in diabetes mellitus: a meta-analysis of observational studies. Cancer Causes Control 23:263–272
Kasuga M, Ueki K, Tajima N et al (2013) Report of the Japan Diabetes Society/Japanese Cancer Association Joint Committee on diabetes and cancer. Cancer Sci 104:965–976
Sasazuki S, Charvat H, Hara A et al (2013) Diabetes mellitus and cancer risk: pooled analysis of eight cohort studies in Japan. Cancer Sci 104:1499–1507
Gallagher EJ, LeRoith D (2015) Obesity and diabetes: the increased risk of cancer and cancer-related mortality. Physiol Rev 95:727–748
de Beer JC, Liebenberg L (2014) Does cancer risk increase with Hba1c, independent of diabetes? Br J Cancer 110:2361–2368
Barone BB, Yeh HC, Snyder CF et al (2008) Long-term all-cause mortality in cancer patients with preexisting diabetes mellitus: a systematic review and meta-analysis. JAMA 300:2754–2764
Campbell PT, Newton CC, Patel AV et al (2012) Diabetes and cause-specific mortality in a prospective cohort of one million US adults. Diabetes Care 35:1835–1844
Ranc K, Jorgensen ME, Friis S et al (2014) Mortality after cancer among patients with diabetes mellitus: effect of diabetes duration and treatment. Diabetologia 57:927–934
Luo J, Hendryx M, Virnig B et al (2015) Pre-existing diabetes and breast cancer prognosis among elderly women. Br J Cancer 113:827–832
Yuan C, Rubinson DA, Qian ZR et al (2015) Survival among patients with pancreatic cancer and long-standing or recent-onset diabetes mellitus. J Clin Oncol 33:29–35
Cai H, Xu Z, Xu T et al (2015) diabetes mellitus is associated with elevated risk of mortality amongst patients with prostate cancer: a meta-analysis of 11 cohort studies. Diabetes Metab Res Rev 31:336–343
Hu D, Peng F, Lin X et al (2016) The elevated preoperative fasting blood glucose predicts a poor prognosis in patients with esophageal squamous cell carcinoma: the Fujian prospective investigation of cancer (FIESTA) Study. Oncotarget 7:65247–65256
Lee J, Giovannucci E, Jeon JY (2016) Diabetes and mortality in patients with prostate cancer: a meta-analysis. Springerplus 5:1548
Lee W, Yoon YS, Han HS et al (2016) Prognostic relevance of preoperative diabetes mellitus and the degree of hyperglycemia on the outcomes of resected pancreatic ductal adenocarcinoma. J Surg Oncol 113:203–208
Luo J, Hendryx M, Qi L et al (2016) Pre-existing diabetes and lung cancer prognosis. Br J Cancer 115:76–79
Backemar L, Djärv T, Wikman A et al (2013) The role of diabetes and other co-morbidities on survival after esophageal cancer surgery in a population-based study. Am J Surg 206:539–543
Jeppsson JO, Kobold U, Barr J et al (2002) Approved IFCC reference method for the measurement of Hba1c in human blood. Clin Chem Lab Med 40:78–89
Aschner P, Beck-Nielsen H, Bennett P et al (2014) Global guideline for type 2 diabetes. Diabetes Res Clin Pract 104:1–52
Sobin LH, Gospodarowicz MK, Wittekind C et al (2010) TNM classification of malignant tumours. Wiley-Blackwell, Sussex
Warburg O, Wind F, Negelein E (1927) The metabolism of tumors in the body. J Gen Physiol 8:519–530
Macheda ML, Rogers S, Best JD (2005) Molecular and cellular regulation of glucose transporter (GLUT) proteins in cancer. J Cell Physiol 202:654–662
Hiyoshi Y, Watanabe M, Imamura Y et al (2009) The relationship between the glucose transporter type 1 expression and F-fluorodeoxyglucose uptake in esophageal squamous cell carcinoma. Oncology 76:286–292
Adekola K, Rosen ST, Shanmugam M (2012) Glucose transporters in cancer metabolism. Curr Opin Oncol 24:650–654
Gatenby RA, Gawlinski ET, Gmitro AF et al (2006) Acid-mediated tumor invasion: a multidisciplinary study. Cancer Res 66:5216–5223
Brownlee M (2001) Biochemistry and molecular cell biology of diabetic complications. Nature 414:813–820
Rojas A, González I, Morales E et al (2011) Diabetes and cancer: looking at the multiligand/RAGE axis. World J Diabetes 2:108–113
Jiao L, Taylor PR, Weinstein SJ et al (2011) Advanced glycation end products, soluble receptor for advanced glycation end products, and risk of colorectal cancer. Cancer Epidemiol Biomark Prev 20:1430–1438
Takeuchi H, Saikawa Y, Oyama T et al (2010) Factors influencing the long-term survival in patients with esophageal cancer who underwent esophagectomy after chemoradiotherapy. World J Surg 34:277–284. doi:10.1007/s00268-009-0331-9
Booka E, Takeuchi H, Nishi T et al (2015) The impact of postoperative complications on survivals after esophagectomy for esophageal cancer. Medicine (Baltimore) 94:e1369
Baba Y, Yoshida N, Shigaki H 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 264:305–311
Yamashita K, Makino T, Miyata H et al (2016) Postoperative infectious complications are associated with adverse oncologic outcomes in esophageal cancer patients undergoing preoperative chemotherapy. Ann Surg Oncol 23:2106–2114
Martin ET, Kaye KS, Knott C et al (2016) Diabetes and risk of surgical site infection: a systematic review and meta-analysis. Infect Control Hosp Epidemiol 37:88–99
Okamura A, Watanabe M, Imamura Y et al (2017) Preoperative glycosylated hemoglobin levels predict anastomotic leak after esophagectomy with cervical esophagogastric anastomosis. World J Surg 41:200–207. doi:10.1007/s00268-016-3763-z
Lipscombe LL, Fischer HD, Austin PC et al (2015) The association between diabetes and breast cancer stage at diagnosis: a population-based study. Breast Cancer Res Treat 150:613–620
Acknowledgements
This work was supported in part by the Japan Society for the Promotion of Science (JSPS) Grant-in-Aid for Scientific Research (Grant Number 15K10122).
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Okamura, A., Watanabe, M., Imamura, Y. et al. Glycemic Status and Prognosis of Patients with Squamous Cell Carcinoma of the Esophagus. World J Surg 41, 2591–2597 (2017). https://doi.org/10.1007/s00268-017-4036-1
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DOI: https://doi.org/10.1007/s00268-017-4036-1