Skip to main content

Advertisement

Log in

Body mass index and the all-cause mortality rate in patients with type 2 diabetes mellitus

  • Original Article
  • Published:
Acta Diabetologica Aims and scope Submit manuscript

Abstract

Aims

The relationship between obesity and mortality rate among diabetic patients is a controversial topic. The aim of this study was to investigate the association between obesity and all-cause mortality risk in patients with type 2 diabetes.

Methods

In this retrospective database study, 2383 patients with type 2 diabetes, who had been registered in the Isfahan Endocrine and Metabolism Research Center, Iran, were enrolled between 1992 and 2010. The mean (SD) of diabetes duration and follow-up period was 15.5 (8.0) and 7.8 (3.9) years. The main outcome was all-cause mortality. All-cause mortality rates were calculated for the body mass index (BMI) categories of underweight, normal, overweight and class I, II and III obese. Cox proportional hazard models were used to estimate the adjusted hazard ratio for BMI as categorical variable using BMI of 18.5–24.9 kg/m2 as the reference group.

Results

The mortality rate in patients with normal weight was higher than overweight patients (59.11 vs. 33.17 per 1000 person-years). The adjusted hazard ratios of all-cause mortality were 0.82 [95%CI 0.68–0.99; P = 0.037], 0.79 [95%CI 0.61–1.02; P = 0.069], 0.71 [95%CI 0.42–1.19; P = 0.191] and 1.36 [95%CI 0.55–3.33; P = 0.507] for overweight, class I, II and III obesity, respectively. When BMI was included in the Cox model as a time-dependent variable, the U-shaped relationship between BMI and all-cause mortality did not change.

Conclusions

The results show a U-shaped association of BMI with all-cause mortality in patients with type 2 diabetes with the lowest risk observed among the overweight patients.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. International Diabetes Federation (2015) IDF diabetes atlas eB. International Diabetes Federation, Belgium

    Google Scholar 

  2. Wilson PW, Meigs JB, Sullivan L, Fox CS, Nathan DM, D’Agostino RB Sr (2007) Prediction of incident diabetes mellitus in middle-aged adults: the Framingham Offspring Study. Arch Intern Med 167(10):1068–1074. https://doi.org/10.1001/archinte.167.10.1068

    Article  PubMed  Google Scholar 

  3. Hashimoto Y, Hamaguchi M, Tanaka M, Obora A, Kojima T, Fukui M (2018) Metabolically healthy obesity without fatty liver and risk of incident type 2 diabetes: a meta-analysis of prospective cohort studies. Obesity Res Clin Pract. https://doi.org/10.1016/j.orcp.2017.12.003

    Article  Google Scholar 

  4. Bell JA, Kivimaki M, Hamer M (2014) Metabolically healthy obesity and risk of incident type 2 diabetes: a meta-analysis of prospective cohort studies. Obes Rev Off J Int Assoc Study Obes 15(6):504–515. https://doi.org/10.1111/obr.12157

    Article  CAS  Google Scholar 

  5. Kahn BB, Flier JS (2000) Obesity and insulin resistance. J Clin Investig 106(4):473–481. https://doi.org/10.1172/JCI10842

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  6. Ginsberg HN (2000) Insulin resistance and cardiovascular disease. J Clin Investig 106(4):453–458. https://doi.org/10.1172/JCI10762

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Fayh AP, Lopes AL, da Silva AM, Reischak-Oliveira A, Friedman R (2013) Effects of 5% weight loss through diet or diet plus exercise on cardiovascular parameters of obese: a randomized clinical trial. Eur J Nutr 52(5):1443–1450. https://doi.org/10.1007/s00394-012-0450-1

    Article  PubMed  CAS  Google Scholar 

  8. Meigs JB, Rutter MK, Sullivan LM, Fox CS, D’Agostino RB Sr, Wilson PW (2007) Impact of insulin resistance on risk of type 2 diabetes and cardiovascular disease in people with metabolic syndrome. Diabetes Care 30(5):1219–1225. https://doi.org/10.2337/dc06-2484

    Article  PubMed  CAS  Google Scholar 

  9. Aune D, Sen A, Prasad M, Norat T, Janszky I, Tonstad S, Romundstad P, Vatten LJ (2016) BMI and all cause mortality: systematic review and non-linear dose-response meta-analysis of 230 cohort studies with 3.74 million deaths among 30.3 million participants. Bmj 353:i2156. https://doi.org/10.1136/bmj.i2156

    Article  PubMed  PubMed Central  Google Scholar 

  10. Hansen LJ, Olivarius Nde F, Siersma V (2009) 16-year excess all-cause mortality of newly diagnosed type 2 diabetic patients: a cohort study. BMC Public Health 9:400. https://doi.org/10.1186/1471-2458-9-400

    Article  PubMed  PubMed Central  Google Scholar 

  11. Zoppini G, Verlato G, Leuzinger C, Zamboni C, Brun E, Bonora E, Muggeo M (2003) Body mass index and the risk of mortality in type II diabetic patients from Verona. Int J Obes Relat Metab Disord J Int Assoc Study Obes 27(2):281–285. https://doi.org/10.1038/sj.ijo.802199

    Article  CAS  Google Scholar 

  12. Eeg-Olofsson K, Cederholm J, Nilsson PM, Zethelius B, Nunez L, Gudbjornsdottir S, Eliasson B (2009) Risk of cardiovascular disease and mortality in overweight and obese patients with type 2 diabetes: an observational study in 13,087 patients. Diabetologia 52(1):65–73. https://doi.org/10.1007/s00125-008-1190-x

    Article  PubMed  CAS  Google Scholar 

  13. Carnethon MR, De Chavez PJ, Biggs ML, Lewis CE, Pankow JS, Bertoni AG, Golden SH, Liu K, Mukamal KJ, Campbell-Jenkins B, Dyer AR (2012) Association of weight status with mortality in adults with incident diabetes. JAMA 308(6):581–590. https://doi.org/10.1001/jama.2012.9282

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Jackson CL, Yeh HC, Szklo M, Hu FB, Wang NY, Dray-Spira R, Brancati FL (2014) Body-mass index and all-cause mortality in US adults with and without diabetes. J Gen Intern Med 29(1):25–33. https://doi.org/10.1007/s11606-013-2553-7

    Article  PubMed  Google Scholar 

  15. Logue J, Walker JJ, Leese G, Lindsay R, McKnight J, Morris A, Philip S, Wild S, Sattar N, Scottish Diabetes Research Network Epidemiology G (2013) Association between BMI measured within a year after diagnosis of type 2 diabetes and mortality. Diabetes Care 36(4):887–893. https://doi.org/10.2337/dc12-0944

    Article  PubMed  PubMed Central  Google Scholar 

  16. Zhao W, Katzmarzyk PT, Horswell R, Wang Y, Li W, Johnson J, Heymsfield SB, Cefalu WT, Ryan DH, Hu G (2014) Body mass index and the risk of all-cause mortality among patients with type 2 diabetes mellitus. Circulation 130(24):2143–2151. https://doi.org/10.1161/circulationaha.114.009098

    Article  PubMed  PubMed Central  Google Scholar 

  17. Kwon Y, Kim HJ, Park S, Park YG, Cho KH (2017) Body mass index-related mortality in patients with type 2 diabetes and heterogeneity in obesity paradox studies: a dose-response meta-analysis. PLoS ONE 12(1):e0168247. https://doi.org/10.1371/journal.pone.0168247

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Tobias DK, Pan A, Jackson CL, O’Reilly EJ, Ding EL, Willett WC, Manson JE, Hu FB (2014) Body-mass index and mortality among adults with incident type 2 diabetes. N Engl J Med 370(3):233–244. https://doi.org/10.1056/NEJMoa1304501

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  19. Esteghamati A, Larijani B, Aghajani MH, Ghaemi F, Kermanchi J, Shahrami A, Saadat M, Esfahani EN, Ganji M, Noshad S, Khajeh E, Ghajar A, Heidari B, Afarideh M, Mechanick JI, Ismail-Beigi F (2017) Diabetes in Iran: prospective analysis from first nationwide diabetes report of national program for prevention and control of diabetes (NPPCD-2016). Sci Rep 7(1):13461. https://doi.org/10.1038/s41598-017-13379-z

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. Statistical C, Of Iran (2011) Selected finding of the 2011 national population and housing census. https://www.amar.org.ir/Portals/1/Iran/census-2.pdf

  21. American Diabetes Association (2000) Screening for type 2 diabetes. Diabetes Care 23(Suppl 1):S20–S23

    Google Scholar 

  22. Garvey WT, Mechanick JI, Brett EM, Garber AJ, Hurley DL, Jastreboff AM, Nadolsky K, Pessah-Pollack R, Plodkowski R, Reviewers of the AACEOCPG (2016) American Association of Clinical Endocrinologists and American College of Endocrinology comprehensive clinical practice guidelines for medical care of patients with obesity. Endocr Pract Off J Am Coll Endocrinol Am Assoc Clin Endocrinol 22(Suppl 3):1–203. https://doi.org/10.4158/EP161365.GL

    Article  Google Scholar 

  23. Perloff D, Grim C, Flack J, Frohlich ED, Hill M, McDonald M, Morgenstern BZ (1993) Human blood pressure determination by sphygmomanometry. Circulation 88(5 Pt 1):2460–2470

    Article  PubMed  CAS  Google Scholar 

  24. Royston P, Ambler G, Sauerbrei W (1999) The use of fractional polynomials to model continuous risk variables in epidemiology. Int J Epidemiol 28(5):964–974

    Article  PubMed  CAS  Google Scholar 

  25. Royston P, Sauerbrei W (2008) Multivariable model-building: a pragmatic approach to regression analysis based on fractional polynomials for modelling continuous variables, vol 777. Wiley, London

    Book  Google Scholar 

  26. Dekker FW, de Mutsert R, van Dijk PC, Zoccali C, Jager KJ (2008) Survival analysis: time-dependent effects and time-varying risk factors. Kidney Int 74(8):994–997. https://doi.org/10.1038/ki.2008.328

    Article  PubMed  Google Scholar 

  27. Zaccardi F, Dhalwani NN, Papamargaritis D, Webb DR, Murphy GJ, Davies MJ, Khunti K (2017) Nonlinear association of BMI with all-cause and cardiovascular mortality in type 2 diabetes mellitus: a systematic review and meta-analysis of 414,587 participants in prospective studies. Diabetologia 60:240–248. https://doi.org/10.1007/s00125-016-4162-6

    Article  PubMed  Google Scholar 

  28. Flegal KM, Kit BK, Orpana H, Graubard BI (2013) Association of all-cause mortality with overweight and obesity using standard body mass index categories: a systematic review and meta-analysis. JAMA 309(1):71–82. https://doi.org/10.1001/jama.2012.113905

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Hainer V, Aldhoon-Hainerová I (2013) Obesity paradox does exist. Diabetes care 36(Suppl 2):S 276–S 281. https://doi.org/10.2337/dcs13-2023

    Article  Google Scholar 

  30. Tseng CH (2013) Obesity paradox: differential effects on cancer and noncancer mortality in patients with type 2 diabetes mellitus. Atherosclerosis 226(1):186–192. https://doi.org/10.1016/j.atherosclerosis.2012.09.004

    Article  PubMed  CAS  Google Scholar 

  31. Ross R, Bradshaw AJ (2009) The future of obesity reduction: beyond weight loss. Nat Rev Endocrinol 5(6):319–325. https://doi.org/10.1038/nrendo.2009.78

    Article  PubMed  Google Scholar 

  32. Fadini GP, Boscaro E, de Kreutzenberg S, Agostini C, Seeger F, Dimmeler S, Zeiher A, Tiengo A, Avogaro A (2010) Time course and mechanisms of circulating progenitor cell reduction in the natural history of type 2 diabetes. Diabetes Care 33(5):1097–1102. https://doi.org/10.2337/dc09-1999

    Article  PubMed  PubMed Central  Google Scholar 

  33. Song X, Jousilahti P, Stehouwer CD, Soderberg S, Onat A, Laatikainen T, Yudkin JS, Dankner R, Morris R, Tuomilehto J, Qiao Q (2015) Cardiovascular and all-cause mortality in relation to various anthropometric measures of obesity in Europeans. Nutr Metab Cardiovasc Dis NMCD 25(3):295–304. https://doi.org/10.1016/j.numecd.2014.09.004

    Article  PubMed  CAS  Google Scholar 

  34. Kuk JL, Katzmarzyk PT, Nichaman MZ, Church TS, Blair SN, Ross R (2006) Visceral fat is an independent predictor of all-cause mortality in men. Obesity (Silver Spring, Md) 14(2):336–341. https://doi.org/10.1038/oby.2006.43

    Article  Google Scholar 

  35. Schenkeveld L, Magro M, Oemrawsingh RM, Lenzen M, de Jaegere P, van Geuns RJ, Serruys PW, van Domburg RT (2012) The influence of optimal medical treatment on the ‘obesity paradox’, body mass index and long-term mortality in patients treated with percutaneous coronary intervention: a prospective cohort study. BMJ Open 2:e000535. https://doi.org/10.1136/bmjopen-2011-000535

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We would like to thank Mr. Majid Abyar for technical computer assistance and all the patients for participation in this study.

Funding

The study was funded by Isfahan Endocrine and Metabolism Research Center, Isfahan University of Medical Sciences, Isfahan, Iran.

Author information

Authors and Affiliations

Authors

Contributions

Dr. Rezvan Salehidoost designed the study, wrote the manuscript and contributed to discussion. Dr. Asieh Mansouri contributed to the statistical analysis and interpretation of data. Prof. Massoud Amini contributed to conducting the research, interpreting the data and reviewed the manuscript. Dr. Sima Aminorroaya contributed to writing the manuscript and discussion. Prof. Ashraf Aminorroaya contributed to conducting the research, interpreting the data and reviewed the manuscript.

Corresponding authors

Correspondence to Massoud Amini or Ashraf Aminorroaya.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. The study was approved by the Ethics Committee of the Isfahan University of Medical Sciences.

Informed consent

Informed consent was obtained from all patients for precipitation and registration.

Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

Additional information

Managed by Antonio Secchi.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Salehidoost, R., Mansouri, A., Amini, M. et al. Body mass index and the all-cause mortality rate in patients with type 2 diabetes mellitus. Acta Diabetol 55, 569–577 (2018). https://doi.org/10.1007/s00592-018-1126-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00592-018-1126-y

Keywords

Navigation