Advertisement

Association between sarcopenia and diabetes: a systematic review and meta-analysis of observational studies

  • Nicola VeroneseEmail author
  • Damiano Pizzol
  • Jacopo Demurtas
  • Pinar Soysal
  • Lee Smith
  • Cornel Sieber
  • Timo Strandberg
  • Isabelle Bourdel-Marchasson
  • Alan Sinclair
  • Mirko Petrovic
  • Stefania Maggi
  • on behalf of the Special Interest Groups of Systematic Reviews and Meta-Analysis for Healthy Ageing, Diabetes, Sarcopenia of European Geriatric Medicine Society (EuGMS)
Review

Key summary points

Aim

To summarize the prevalence of diabetes in people with sarcopenia (and vice versa) through a meta-analytic approach of available observational studies.

Findings

In this work, we have presented the findings of the first full methodological systematic review and meta-analysis of observational studies exploring the relationship between diabetes and sarcopenia. Our findings overall emphasize the reciprocal relationship between diabetes and sarcopenia in terms of risk of occurrence, that is sarcopenia increases the risk of diabetes being present and vice versa.

Message

This study provides support for further research into the prognosis of people with both diabetes and sarcopenia and the value of interventional strategies in sarcopenia to minimize adverse outcomes such as premature death, hospitalization, and disability.

Abstract

Purpose

Sarcopenia and diabetes are two common conditions in older people. Some recent literature has proposed that these two conditions can be associated. However, to date, no attempt has been made to collate this literature. Therefore, we aimed to summarize the prevalence of sarcopenia in diabetes (and vice versa) and the prevalence of sarcopenia in people with diabetes complications, through a systematic review and meta-analysis.

Methods

Two authors searched major electronic databases from inception until March 2019 for case control/cross-sectional/longitudinal studies investigating sarcopenia and diabetes. The strength of the reciprocal associations between sarcopenia and diabetes was assessed through odds ratios (ORs) with 95% confidence intervals (CIs), adjusted for potential confounders, where possible.

Results

From 953 potential eligible articles, 20 were included in the systematic review, with 17 providing data for meta-analysis. Overall, 54,676 participants were included (mean age = 65.4 years). Diabetic participants had an increased prevalence of sarcopenia compared to controls (n = 10; OR = 1.635; 95% CI 1.204–2.220; p = 0.002; I2 = 67%), whilst, after adjusting for potential confounders, sarcopenia was associated with an increased odds of having diabetes (OR = 2.067; 95% CI 1.396–3.624; p < 0.0001; I2 = 0%). In 1868 diabetic participants with a complication, there was an increased prevalence of sarcopenia (OR = 2.446; 95% CI 1.839–3.254; p < 0.0001; I2 = 0%), as compared with those with no complication. Very limited data existed regarding studies with a longitudinal design.

Conclusions

Our study suggests a bidirectional association between diabetes and sarcopenia, particularly when diabetic complications are present.

Keywords

Diabetes Sarcopenia Physical performance Meta-analysis 

Notes

Funding

None to declare.

Compliance with ethical standards

Conflict of interest

The authors have not conflict of interest to declare for this work.

Ethical approval

Not required since it is a review of already published works.

Informed consent

For this type of study, formal consent is not required.

Supplementary material

41999_2019_216_MOESM1_ESM.docx (39 kb)
Supplementary material 1 (DOCX 39 kb)

References

  1. 1.
    Umegaki H (2016) Sarcopenia and frailty in older patients with diabetes mellitus. Geriatr Gerontol Int 16(3):293–299Google Scholar
  2. 2.
    Karjalainen M, Tiihonen M, Kautiainen H, Saltevo J, Haanpää M, Mäntyselkä P (2018) Pain and self-rated health in older people with and without type 2 diabetes. Euro Geriatr Med 9(1):127–131Google Scholar
  3. 3.
    Ogurtsova K, da Rocha Fernandes J, Huang Y, Linnenkamp U, Guariguata L, Cho N et al (2017) IDF diabetes atlas: global estimates for the prevalence of diabetes for 2015 and 2040. Diabetes Res Clin Pract 128:40–50Google Scholar
  4. 4.
    Sinclair AJ, Abdelhafiz AH, Rodríguez-Mañas L (2017) Frailty and sarcopenia-newly emerging and high impact complications of diabetes. J Diabetes Complicat 31(9):1465–1473Google Scholar
  5. 5.
    Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F et al (2010) Sarcopenia: European consensus on definition and diagnosis: report of the European working group on sarcopenia in older people. Age Ageing 39(4):412–423.  https://doi.org/10.1093/ageing/afq034 Google Scholar
  6. 6.
    Di Francesco V, Pellizzari L, Corrà L, Fontana G (2018) The anorexia of aging: impact on health and quality of life. Geriatr Care.  https://doi.org/10.4081/gc.2018.7324 Google Scholar
  7. 7.
    Shafiee G, Keshtkar A, Soltani A, Ahadi Z, Larijani B, Heshmat R (2017) Prevalence of sarcopenia in the world: a systematic review and meta-analysis of general population studies. J Diabetes Metab Disord 16(1):21Google Scholar
  8. 8.
    Beaudart C, Zaaria M, Pasleau F, Reginster J-Y, Bruyère O (2017) Health outcomes of sarcopenia: a systematic review and meta-analysis. PLoS One 12(1):e0169548Google Scholar
  9. 9.
    Zhao Y, Zhang Y, Hao Q, Ge M, Dong B (2019) Sarcopenia and hospital-related outcomes in the old people: a systematic review and meta-analysis. Aging Clin Exp Res 31(1):5–14Google Scholar
  10. 10.
    Greene NP, Brown JL, Rosa-Caldwell ME, Lee DE, Blackwell TA, Washington TA (2018) Skeletal muscle insulin resistance as a precursor to diabetes: beyond glucoregulation. Curr Diabetes Rev 14(2):113–128Google Scholar
  11. 11.
    Leenders M, Verdijk LB, van der Hoeven L, Adam JJ, Van Kranenburg J, Nilwik R et al (2013) Patients with type 2 diabetes show a greater decline in muscle mass, muscle strength, and functional capacity with aging. J Am Med Dir Assoc 14(8):585–592Google Scholar
  12. 12.
    Park SW, Goodpaster BH, Strotmeyer ES, Kuller LH, Broudeau R, Kammerer C et al (2007) Accelerated loss of skeletal muscle strength in older adults with type 2 diabetes: the health, aging, and body composition study. Diabetes Care 30(6):1507–1512Google Scholar
  13. 13.
    Siviero P, Tonin P, Maggi S (2009) Functional limitations of upper limbs in older diabetic individuals. The Italian longitudinal study on aging. Aging Clin Exp Res 21(6):458–462Google Scholar
  14. 14.
    Wilmot EG, Edwardson CL, Achana FA, Davies MJ, Gorely T, Gray LJ et al (2012) Sedentary time in adults and the association with diabetes, cardiovascular disease and death: systematic review and meta-analysis. Diabetologia 55(11):2895–2905.  https://doi.org/10.1007/s00125-012-2677 Google Scholar
  15. 15.
    Sinclair AJ, Rodriguez-Manas L (2016) Diabetes and frailty: two converging conditions? Can J Diabetes 40(1):77–83Google Scholar
  16. 16.
    Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gøtzsche PC, Ioannidis JPA et al (2009) The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. PLoS Med 6(7):e1000100-e.  https://doi.org/10.1371/journal.pmed.1000100 Google Scholar
  17. 17.
    Stroup DF, Ja Berlin, Morton SC, Olkin I, Williamson GD, Rennie D et al (2000) Meta-analysis of observational studies in epidemiology: a proposal for reporting meta-analysis of observational studies in epidemiology (MOOSE) group. JAMA 283:2008–2012.  https://doi.org/10.1001/jama.283.15.2008 Google Scholar
  18. 18.
    Association AD. 2 (2014) Classification and diagnosis of diabetes. Diabetes care 38(Supplement_1):S8–S16.  https://doi.org/10.2337/dc15-s005 Google Scholar
  19. 19.
    Chen L-K, Liu L-K, Woo J, Assantachai P, Auyeung T-W, Bahyah KS et al (2014) Sarcopenia in Asia: consensus report of the Asian Working Group for sarcopenia. J Am Med Directors Assoc 15(2):95–101Google Scholar
  20. 20.
    Wells GA, Shea B, O’Connell D, Peterson J, Welch V, Losos M et al. The Newcastle–Ottawa Scale (NOS) for assessing the quality if nonrandomized studies in meta-analyses. http://www.ohrica/programs/clinical_epidemiology/oxfordasp). 2012:2012.  https://doi.org/10.2307/632432
  21. 21.
    Luchini CS (2017) Brendon; solmi, marco; veronese, nicola assessing the quality of studies in meta-analyses: advantages and limitations of the Newcastle Ottawa Scale. World J Meta-Anal 5:80–84Google Scholar
  22. 22.
    Higgins JPT, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21(11):1539–1558.  https://doi.org/10.1002/sim.1186 Google Scholar
  23. 23.
    Higgins JP, Altman DG, Gotzsche PC, Juni P, Moher D, Oxman AD et al (2011) The Cochrane collaboration’s tool for assessing risk of bias in randomised trials. BMJ 343:d5928.  https://doi.org/10.1136/bmj.d5928 Google Scholar
  24. 24.
    Egger M, Davey Smith G, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ (Clin Res ed) 315(September):629–634.  https://doi.org/10.1136/bmj.316.7129.469 Google Scholar
  25. 25.
    Duval S, Tweedie R (2000) Trim and fill: a simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics 56:455–463.  https://doi.org/10.1111/j.0006-341x.2000.00455.x Google Scholar
  26. 26.
    Yang R, Zhang Y, Shen X, Yan S (2016) Sarcopenia associated with renal function in the patients with type 2 diabetes. Diabetes Res Clin Pract 118:121–129.  https://doi.org/10.1016/j.diabres.2016.06.023 Google Scholar
  27. 27.
    Murata Y, Kadoya Y, Yamada S, Sanke T (2018) Sarcopenia in elderly patients with type 2 diabetes mellitus: prevalence and related clinical factors. Diabetol Int 9(2):136–142.  https://doi.org/10.1007/s13340-017-0339-6 Google Scholar
  28. 28.
    Fukuda T, Bouchi R, Takeuchi T, Nakano Y, Murakami M, Minami I et al (2017) Association of diabetic retinopathy with both sarcopenia and muscle quality in patients with type 2 diabetes: a cross-sectional study. BMJ Open Diabetes Res Care 5(1):e000404.  https://doi.org/10.1136/bmjdrc-2017-000404 Google Scholar
  29. 29.
    Freitas VP, Passos RDS, Oliveira AA, Ribeiro IJS, Freire IV, Schettino L et al (2018) Sarcopenia is associated to an impaired autonomic heart rate modulation in community-dwelling old adults. Arch Gerontol Geriatr 76:120–124.  https://doi.org/10.1016/j.archger.2018.01.006 Google Scholar
  30. 30.
    Cheng Q, Hu J, Yang P, Cao X, Deng X, Yang Q et al (2017) Sarcopenia is independently associated with diabetic foot disease. Sci Rep 7(1):8372.  https://doi.org/10.1038/s41598-017-08972-1 Google Scholar
  31. 31.
    Celiker M, Selcuk MY, Olt S (2018) Sarcopenia in diabetic nephropathy: a cross-sectional study. Romanian J Int Med Revue Roumaine de Med Interne 56(2):102–108.  https://doi.org/10.2478/rjim-2018-0003 Google Scholar
  32. 32.
    Wang T, Feng X, Zhou J, Gong H, Xia S, Wei Q et al (2016) Type 2 diabetes mellitus is associated with increased risks of sarcopenia and pre-sarcopenia in Chinese elderly. Sci Rep 6:38937.  https://doi.org/10.1038/srep38937 Google Scholar
  33. 33.
    Ma J, Hwang SJ, McMahon GM, Curhan GC, McLean RR, Murabito JM et al (2016) Mid-adulthood cardiometabolic risk factor profiles of sarcopenic obesity. Obes (Silver Spring) 24(2):526–534.  https://doi.org/10.1002/oby.21356 Google Scholar
  34. 34.
    Lim HS, Park YH, Suh K, Yoo MH, Park HK, Kim HJ et al (2018) Association between sarcopenia, sarcopenic obesity, and chronic disease in Korean elderly. J Bone Metab 25(3):187–193.  https://doi.org/10.11005/jbm.2018.25.3.187 Google Scholar
  35. 35.
    Koo BK, Roh E, Yang YS, Moon MK (2016) Difference between old and young adults in contribution of beta-cell function and sarcopenia in developing diabetes mellitus. J Diabetes Invest 7(2):233–240.  https://doi.org/10.1111/jdi.12392 Google Scholar
  36. 36.
    Kim KS, Park KS, Kim MJ, Kim SK, Cho YW, Park SW (2014) Type 2 diabetes is associated with low muscle mass in older adults. Geriatr Gerontol Int 14(Suppl 1):115–121.  https://doi.org/10.1111/ggi.12189 Google Scholar
  37. 37.
    Han P, Kang L, Guo Q, Wang J, Zhang W, Shen S et al (2016) Prevalence and factors associated with Sarcopenia in suburb-dwelling older Chinese using the asian working group for Sarcopenia definition. J Gerontol Ser A Biol Sci Med Sci 71(4):529–535.  https://doi.org/10.1093/gerona/glv108 Google Scholar
  38. 38.
    Bouchi R, Fukuda T, Takeuchi T, Nakano Y, Murakami M, Minami I et al (2017) Association of sarcopenia with both latent autoimmune diabetes in adults and type 2 diabetes: a cross-sectional study. J Diabetes Complic 31(6):992–996.  https://doi.org/10.1016/j.jdiacomp.2017.02.021 Google Scholar
  39. 39.
    Trierweiler H, Kisielewicz G, Hoffmann Jonasson T, Rasmussen Petterle R, Aguiar Moreira C, Zeghbi Cochenski Borba V (2018) Sarcopenia: a chronic complication of type 2 diabetes mellitus. Diabetol Metab Syndrome 10:25.  https://doi.org/10.1186/s13098-018-0326-5 Google Scholar
  40. 40.
    Kreidieh D, Itani L, El Masri D, Tannir H, Citarella R, El Ghoch M (2018) Association between Sarcopenic obesity, type 2 diabetes, and hypertension in overweight and obese treatment-seeking adult women. J Cardiovasc Dev Dis 5(4):51.  https://doi.org/10.3390/jcdd5040051 Google Scholar
  41. 41.
    Cuthbertson DJ, Bell JA, Ng SY, Kemp GJ, Kivimaki M, Hamer M (2016) Dynapenic obesity and the risk of incident type 2 diabetes: the english longitudinal study of ageing. Diabetic Med 33(8):1052–1059.  https://doi.org/10.1111/dme.12991 Google Scholar
  42. 42.
    Bouchi R, Fukuda T, Takeuchi T, Minami I, Yoshimoto T, Ogawa Y (2017) Sarcopenia is associated with incident albuminuria in patients with type 2 diabetes: a retrospective observational study. J Diabetes Investig 8(6):783–787.  https://doi.org/10.1111/jdi.12636 Google Scholar
  43. 43.
    Srikanthan P, Hevener AL, Karlamangla AS (2010) Sarcopenia exacerbates obesity-associated insulin resistance and dysglycemia: findings from the National Health and Nutrition Examination Survey III. PLoS One 5(5):e10805Google Scholar
  44. 44.
    Moon S-S (2013) Low skeletal muscle mass is associated with insulin resistance, diabetes, and metabolic syndrome in the Korean population: the Korea national health and nutrition examination survey (KNHANES) 2009–2010. Endocr J 61(1):61–70Google Scholar
  45. 45.
    Handajani YS, Widjaja NT, Turana Y, Tengkawan J (2018) Diabetes mellitus, adl disability and nutrition intake: determination factors of severe Sarcopenia among elderly in urban nursing homes. Indian J Publ Health Res Dev 9(3):5–13Google Scholar
  46. 46.
    Bano G, Trevisan C, Carraro S, Solmi M, Luchini C, Stubbs B et al (2017) Inflammation and sarcopenia: a systematic review and meta-analysis. Maturitas 96:10–15.  https://doi.org/10.1016/j.maturitas.2016.11.006 Google Scholar
  47. 47.
    Cleasby ME, Jamieson PM, Atherton PJ (2016) Insulin resistance and sarcopenia: mechanistic links between common co-morbidities. J Endocrinol 229(2):R67–R81Google Scholar
  48. 48.
    Bourdel-Marchasson I, Helmer C, Fagot-Campagna A, Dehail P, Joseph PA (2007) Disability and quality of life in elderly people with diabetes. Diabetes Metab 33:S66–S74Google Scholar
  49. 49.
    Seo J, Kim S, Kim N, Baik SH, Choi DS, Choi KM (2010) Prevalence and determinant factors of Sarcopenia in patients with type 2 diabetes. Diabetes Care 33(7):1497–1499Google Scholar
  50. 50.
    Lee CG, Boyko EJ, Strotmeyer ES, Lewis CE, Cawthon PM, Hoffman AR et al (2011) Association between insulin resistance and lean mass loss and fat mass gain in older men without diabetes mellitus. J Am Geriatr Soc 59(7):1217–1224Google Scholar
  51. 51.
    Veronese N, Stubbs B, Fontana L, Trevisan C, Bolzetta F, De Rui M et al (2016) Frailty Is Associated with an increased risk of incident type 2 diabetes in the elderly. J Am Med Directors Assoc 17(10):902–907.  https://doi.org/10.1016/j.jamda.2016.04.021 Google Scholar
  52. 52.
    Guadarrama-López AL, Valdés-Ramos R, Martínez-Carrillo BE (2014) Type 2 diabetes, PUFAs, and vitamin D: their relation to inflammation. J Immunol Res 2014:860703.  https://doi.org/10.1155/2014/860703 Google Scholar
  53. 53.
    Can B, Kara O, Kizilarslanoglu MC, Arik G, Aycicek GS, Sumer F et al (2017) Serum markers of inflammation and oxidative stress in Sarcopenia. Aging Clin Exp Res 29(4):745–752Google Scholar
  54. 54.
    Kirkham FA, Bunting E, Fantin F, Zamboni M, Rajkumar C (2019) Independent association between Cardio-Ankle vascular Index and Sarcopenia in older UK adults. J Am Geriatr Soc 67(2):317–322Google Scholar
  55. 55.
    Prior SJ, Ryan AS, Blumenthal JB, Watson JM, Katzel LI, Goldberg AP (2016) Sarcopenia is associated with lower skeletal muscle capillarization and exercise capacity in older adults. J Gerontol Ser A 71(8):1096–1101Google Scholar
  56. 56.
    Kwan P (2013) Sarcopenia, a neurogenic syndrome? J Aging Res 2013:791679.  https://doi.org/10.1155/2013/791679 Google Scholar

Copyright information

© European Geriatric Medicine Society 2019

Authors and Affiliations

  • Nicola Veronese
    • 1
    Email author
  • Damiano Pizzol
    • 2
  • Jacopo Demurtas
    • 3
  • Pinar Soysal
    • 4
  • Lee Smith
    • 5
  • Cornel Sieber
    • 6
  • Timo Strandberg
    • 7
    • 8
  • Isabelle Bourdel-Marchasson
    • 9
    • 10
  • Alan Sinclair
    • 11
  • Mirko Petrovic
    • 12
  • Stefania Maggi
    • 1
  • on behalf of the Special Interest Groups of Systematic Reviews and Meta-Analysis for Healthy Ageing, Diabetes, Sarcopenia of European Geriatric Medicine Society (EuGMS)
  1. 1.National Research Council, Neuroscience InstitutePaduaItaly
  2. 2.Operational Research UnitDoctors with AfricaDar es SalaamMozambique
  3. 3.Primary Care DepartmentAzienda USL Toscana Sud EstGrossetoItaly
  4. 4.Department of Geriatric MedicineBezmialem Vakif UniversityIstanbulTurkey
  5. 5.The Cambridge Centre for Sport and Exercise SciencesAnglia Ruskin UniversityCambridgeUK
  6. 6.Institute for Biomedicine of Ageing (IBA)Friedrich-Alexander-Universität Erlangen-Nürnberg (FAU)NurembergGermany
  7. 7.University of Helsinki, Clinicum and Helsinki University HospitalHelsinkiFinland
  8. 8.Center for Life Course Health ResearchUniversity of OuluOuluFinland
  9. 9.CNRS, University of Bordeaux, RMSBBordeauxFrance
  10. 10.Pôle de Gérontologie Clinique, CHU de BordeauxBordeauxFrance
  11. 11.Diabetes Frail Ltd and King’s CollegeLondonUK
  12. 12.Department of Internal Medicine and Paediatrics, Section of GeriatricsGhent UniversityGhentBelgium

Personalised recommendations