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Glycemic Status and Prognosis of Patients with Squamous Cell Carcinoma of the Esophagus

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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

  1. 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

    CAS  Google Scholar 

  2. 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

    Article  PubMed  Google Scholar 

  3. Larsson SC, Orsini N, Wolk A (2005) Diabetes mellitus and risk of colorectal cancer: a meta-analysis. J Natl Cancer Inst 97:1679–1687

    Article  PubMed  Google Scholar 

  4. 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

    Article  PubMed  Google Scholar 

  5. Larsson SC, Mantzoros CS, Wolk A (2007) Diabetes mellitus and risk of breast cancer: a meta-analysis. Int J Cancer 121:856–862

    Article  CAS  PubMed  Google Scholar 

  6. Friberg E, Orsini N, Mantzoros CS et al (2007) Diabetes mellitus and risk of endometrial cancer: a meta-analysis. Diabetologia 50:1365–1374

    Article  CAS  PubMed  Google Scholar 

  7. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. 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

    Article  PubMed  Google Scholar 

  9. Larsson SC, Wolk A (2011) Diabetes mellitus and incidence of kidney cancer: a meta-analysis of cohort studies. Diabetologia 54:1013–1018

    Article  CAS  PubMed  Google Scholar 

  10. 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

    Article  PubMed  Google Scholar 

  11. 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

    Article  CAS  PubMed  Google Scholar 

  12. 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

    Article  CAS  PubMed  Google Scholar 

  13. Gallagher EJ, LeRoith D (2015) Obesity and diabetes: the increased risk of cancer and cancer-related mortality. Physiol Rev 95:727–748

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. de Beer JC, Liebenberg L (2014) Does cancer risk increase with Hba1c, independent of diabetes? Br J Cancer 110:2361–2368

    Article  PubMed  PubMed Central  Google Scholar 

  15. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. 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

    Article  PubMed  PubMed Central  Google Scholar 

  17. 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

    Article  CAS  PubMed  Google Scholar 

  18. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. 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

    Article  PubMed  Google Scholar 

  20. 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

    Article  PubMed  Google Scholar 

  21. 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

    PubMed  PubMed Central  Google Scholar 

  22. Lee J, Giovannucci E, Jeon JY (2016) Diabetes and mortality in patients with prostate cancer: a meta-analysis. Springerplus 5:1548

    Article  PubMed  PubMed Central  Google Scholar 

  23. 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

    Article  CAS  PubMed  Google Scholar 

  24. Luo J, Hendryx M, Qi L et al (2016) Pre-existing diabetes and lung cancer prognosis. Br J Cancer 115:76–79

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. 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

    Article  PubMed  Google Scholar 

  26. 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

    Article  CAS  PubMed  Google Scholar 

  27. Aschner P, Beck-Nielsen H, Bennett P et al (2014) Global guideline for type 2 diabetes. Diabetes Res Clin Pract 104:1–52

    Article  Google Scholar 

  28. Sobin LH, Gospodarowicz MK, Wittekind C et al (2010) TNM classification of malignant tumours. Wiley-Blackwell, Sussex

    Google Scholar 

  29. Warburg O, Wind F, Negelein E (1927) The metabolism of tumors in the body. J Gen Physiol 8:519–530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Macheda ML, Rogers S, Best JD (2005) Molecular and cellular regulation of glucose transporter (GLUT) proteins in cancer. J Cell Physiol 202:654–662

    Article  CAS  PubMed  Google Scholar 

  31. 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

    Article  CAS  PubMed  Google Scholar 

  32. Adekola K, Rosen ST, Shanmugam M (2012) Glucose transporters in cancer metabolism. Curr Opin Oncol 24:650–654

    Article  CAS  PubMed  Google Scholar 

  33. Gatenby RA, Gawlinski ET, Gmitro AF et al (2006) Acid-mediated tumor invasion: a multidisciplinary study. Cancer Res 66:5216–5223

    Article  CAS  PubMed  Google Scholar 

  34. Brownlee M (2001) Biochemistry and molecular cell biology of diabetic complications. Nature 414:813–820

    Article  CAS  PubMed  Google Scholar 

  35. Rojas A, González I, Morales E et al (2011) Diabetes and cancer: looking at the multiligand/RAGE axis. World J Diabetes 2:108–113

    Article  PubMed  PubMed Central  Google Scholar 

  36. 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

    Article  CAS  Google Scholar 

  37. 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

    Article  PubMed  Google Scholar 

  38. 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

    Article  Google Scholar 

  39. 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

    Article  PubMed  Google Scholar 

  40. 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

    Article  PubMed  Google Scholar 

  41. 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

    Article  PubMed  Google Scholar 

  42. 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

    Article  PubMed  Google Scholar 

  43. 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

    Article  PubMed  Google Scholar 

Download references

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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Correspondence to Masayuki Watanabe.

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The authors declare that they have no conflict of interest.

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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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