Skip to main content

Advertisement

Log in

Malnutrition, assessed by the Global Leadership Initiative on Malnutrition (GLIM) criteria but not by the mini nutritional assessment (MNA), predicts the incidence of sarcopenia over a 5-year period in the SarcoPhAge cohort

  • Original Article
  • Published:
Aging Clinical and Experimental Research Aims and scope Submit manuscript

A Correction to this article was published on 13 July 2021

This article has been updated

Abstract

Background

The capacity of malnutrition screening to predict the onset of sarcopenia is unknown.

Aim

Our first objective is to explore the association between the screening of malnutrition and the incidence of sarcopenia and then, to assess the added value of the diagnosis of malnutrition to predict sarcopenia over a 5-year follow-up.

Methods

Malnutrition was screened at baseline according to the MNA short-form (MNA-SF) and long-form (MNA-LF) and was diagnosed by the GLIM definition. Sarcopenia was defined using the European Working Group on Sarcopenia in Older People (EWGSOP2) criteria. Kaplan–Meier analysis and adjusted Cox regression were performed to explore the association between nutritional status and the incidence of sarcopenia.

Results

A total of 418 participants were analyzed (median age 71.7 years (67.7 – 76.8), 60% women) for our first objective. Among them, 64 (15.3%) became sarcopenic during the follow-up period. In the adjusted model, the incidence of sarcopenia was nonsignificantly associated with the risk of malnutrition for both forms of the MNA (MNA-SF: HR of 1.68 (95% CI 0.95 – 2.99); MNA-LF: HR of 1.67 (95% CI 0.86 – 3.26)). However, among the 337 participants for which a GLIM assessment was possible and in which 46 participants became sarcopenic, malnourished subjects had a higher risk than well-nourished participants of developing sarcopenia after 5 years, with an adjusted HR of 3.19 (95% CI 1.56 – 6.50).

Conclusion

A full diagnosis of malnutrition seems more useful than a simple malnutrition screening to predict the incidence of sarcopenia over 5 years.

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

Availability of data and material

The datasets generated and/or analyzed in the current study are not publicly available due to GDPR policies and restrictions because the information could compromise the privacy of the participants. However, the data are available from the corresponding author on reasonable request.

Change history

References

  1. Landi F, Camprubi-Robles M, Bear DE et al (2019) Muscle loss: The new malnutrition challenge in clinical practice. Clin Nutr 38:2113–2120. https://doi.org/10.1016/j.clnu.2018.11.021

    Article  CAS  PubMed  Google Scholar 

  2. Goodpaster BH, Park SW, Harris TB et al (2006) The loss of skeletal muscle strength, mass, and quality in older adults: The Health, Aging and Body Composition Study. J Gerontol Ser A Biol Sci Med Sci 61:1059–1064. https://doi.org/10.1093/gerona/61.10.1059

    Article  Google Scholar 

  3. Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyère O, Cederholm T, Cooper C, Landi F, Rolland Y, Sayer AA et al (2019) Sarcopenia: Revised European consensus on definition and diagnosis. Age Ageing 48:16–31. https://doi.org/10.1093/ageing/afy169

    Article  PubMed  Google Scholar 

  4. Shafiee G, Keshtkar A, Soltani A et al (2017) Prevalence of sarcopenia in the world: A systematic review and meta- analysis of general population studies. J Diabetes Metab Disord. https://doi.org/10.1186/s40200-017-0302-x

    Article  PubMed  PubMed Central  Google Scholar 

  5. Mijnarends DM, Luiking YC, Halfens RJG et al (2018) Muscle, Health and Costs: A Glance at their Relationship. J Nutr Heal Aging 22:766–773. https://doi.org/10.1007/s12603-018-1058-9

    Article  CAS  Google Scholar 

  6. Ogawa S, Yakabe M, Akishita M (2016) Age-related sarcopenia and its pathophysiological bases. Inflamm Regen. https://doi.org/10.1186/s41232-016-0022-5

    Article  PubMed  PubMed Central  Google Scholar 

  7. Beaudart C, Zaaria M, Pasleau F et al (2017) Health Outcomes of Sarcopenia: A Systematic Review and Meta-Analysis. PLoS ONE 12:e0169548. https://doi.org/10.1371/journal.pone.0169548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Bruyère O, Beaudart C, Ethgen O et al (2019) The health economics burden of sarcopenia: a systematic review. Maturitas 119:61–69. https://doi.org/10.1016/j.maturitas.2018.11.003

    Article  PubMed  Google Scholar 

  9. Cao L, Morley JE (2016) Sarcopenia Is recognized as an independent condition by an international classification of disease, tenth revision, clinical modification (ICD-10-CM) Code. J Am Med Dir Assoc 17:675–677. https://doi.org/10.1016/j.jamda.2016.06.001

    Article  PubMed  Google Scholar 

  10. Corcoran C, Murphy C, Culligan EP, Walton J, Sleator RD (2019) Malnutrition in the elderly. Sci Prog 102:171–180. https://doi.org/10.1177/0036850419854290

    Article  PubMed  Google Scholar 

  11. Hu X, Zhang L, Wang H et al (2017) Malnutrition-sarcopenia syndrome predicts mortality in hospitalized older patients. Sci Rep. https://doi.org/10.1038/s41598-017-03388-3

    Article  PubMed  PubMed Central  Google Scholar 

  12. Leij-Halfwerk S, Verwijs MH, van Houdt S et al (2019) Prevalence of protein-energy malnutrition risk in European older adults in community, residential and hospital settings, according to 22 malnutrition screening tools validated for use in adults ≥65 years: A systematic review and meta-analysis. Maturitas 126:80–89. https://doi.org/10.1016/j.maturitas.2019.05.006

    Article  PubMed  Google Scholar 

  13. Pierik VD, Meskers CGM, Van Ancum JM et al (2017) High risk of malnutrition is associated with low muscle mass in older hospitalized patients - a prospective cohort study. BMC Geriatr. https://doi.org/10.1186/s12877-017-0505-5

    Article  PubMed  PubMed Central  Google Scholar 

  14. Volkert D (2011) The role of nutrition in the prevention of sarcopenia. Wien Med Wochenschr 161:409–415. https://doi.org/10.1007/s10354-011-0910-x

    Article  PubMed  Google Scholar 

  15. Pourhassan M, Rommersbach N, Lueg G et al (2020) The impact of malnutrition on acute muscle wasting in frail older hospitalized patients. Nutrients. https://doi.org/10.3390/nu12051387

    Article  PubMed  PubMed Central  Google Scholar 

  16. Liguori I, Curcio F, Russo G et al (2018) Risk of Malnutrition Evaluated by Mini Nutritional Assessment and Sarcopenia in Noninstitutionalized Elderly People. Nutr Clin Pract 33:879–886. https://doi.org/10.1002/ncp.10022

    Article  PubMed  Google Scholar 

  17. Ramsey KA, Meskers CGM, Trappenburg MC et al (2020) Malnutrition is associated with dynamic physical performance. Aging Clin Exp Res 32:1085–1092. https://doi.org/10.1007/s40520-019-01295-3

    Article  PubMed  Google Scholar 

  18. Reginster JY, Beaudart C, Al-Daghri N et al (2021) Update on the ESCEO recommendation for the conduct of clinical trials for drugs aiming at the treatment of sarcopenia in older adults. Aging Clin Exp Res 33:3–17. https://doi.org/10.1007/s40520-020-01663-4

    Article  PubMed  Google Scholar 

  19. Robinson S, Cooper C, Aihie Sayer A (2012) Nutrition and sarcopenia: A review of the evidence and implications for preventive strategies. J Aging Res. https://doi.org/10.1155/2012/510801

    Article  PubMed  PubMed Central  Google Scholar 

  20. Tzeng PL, Lin CY, Lai TF et al (2020) Daily lifestyle behaviors and risks of sarcopenia among older adults. Arch Public Heal. https://doi.org/10.1186/s13690-020-00498-9

    Article  Google Scholar 

  21. Sieber CC (2019) Malnutrition and sarcopenia. Aging Clin Exp Res 31:793–798. https://doi.org/10.1007/s40520-019-01170-1

    Article  PubMed  Google Scholar 

  22. Cederholm T, Jensen GL, Correia MITD et al (2019) GLIM criteria for the diagnosis of malnutrition – A consensus report from the global clinical nutrition community. Clin Nutr 38:1–9. https://doi.org/10.1016/j.clnu.2018.08.002

    Article  CAS  PubMed  Google Scholar 

  23. Beaudart C, Sanchez-Rodriguez D, Locquet M et al (2019) Malnutrition as a strong predictor of the onset of sarcopenia. Nutrients. https://doi.org/10.3390/nu11122883

    Article  PubMed  PubMed Central  Google Scholar 

  24. Vellas B, Villars H, Abellan G et al (2006) Overview of the MNA® - Its history and challenges. J Nutr Heal Aging 10:456–463

    CAS  Google Scholar 

  25. Guigoz Y, Vellas B (2021) Nutritional assessment in older adults: MNA® 25 years of a screening tool and a reference standard for care and research; what next ? J Nutr Health Aging. https://doi.org/10.1007/s12603-021-1601-y

    Article  PubMed  Google Scholar 

  26. Beaudart C, Reginster JY, Petermans J et al (2015) Quality of life and physical components linked to sarcopenia: The SarcoPhAge study. Exp Gerontol 69:103–110. https://doi.org/10.1016/j.exger.2015.05.003

    Article  CAS  PubMed  Google Scholar 

  27. Guigoz Y, Lauque S, Vellas BJ (2002) Identifying the elderly at risk for malnutrition the mini nutritional assessment. Clin Geriatr Med 18:737–757. https://doi.org/10.1016/S0749-0690(02)00059-9

    Article  PubMed  Google Scholar 

  28. Kaiser MJ, Bauer JM, Ramsch C et al (2009) Validation of the mini nutritional assessment short-form (MNA®-SF): a practical tool for identification of nutritional status. J Nutr Health Aging 13:782–788

    Article  CAS  Google Scholar 

  29. Nestlé Nutrition Institute Nutrition screening as easy as MNA: a guide to complete the Mini Nutiritonal Assessment (MNA) Available online: https://www.mna-elderly.com/forms/mna_guide_english.pdf (Accessed on Feb 17, 2021)

  30. Justice JN, Ferrucci L, Newman AB et al (2018) A framework for selection of blood-based biomarkers for geroscience-guided clinical trials: report from the TAME Biomarkers Workgroup. GeroScience 40:419–436. https://doi.org/10.1007/s11357-018-0042-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Adriaensen W, Matheï C, Vaes B et al (2014) Interleukin-6 predicts short-term global functional decline in the oldest old: results from the BELFRAIL study. Age (Omaha) 36:9723. https://doi.org/10.1007/s11357-014-9723-3

    Article  CAS  Google Scholar 

  32. Doi T, Shimada H, Makizako H et al (2016) Insulin-like growth factor-1 related to disability among older adults. J Gerontol Ser A Biol Sci Med Sci 71:797–802. https://doi.org/10.1093/gerona/glv167

    Article  CAS  Google Scholar 

  33. Roberts HC, Denison HJ, Martin HJ et al (2011) A review of the measurement of grip strength in clinical and epidemiological studies: Towards a standardised approach. Age Ageing 40:423–429. https://doi.org/10.1093/ageing/afr051

    Article  PubMed  Google Scholar 

  34. Vetrano DL, Landi F, Volpato S et al (2014) Association of sarcopenia with short- and long-term mortality in older adults admitted to acute care wards: Results from the CRIME study. J Gerontol Ser A Biol Sci Med Sci 69:1154–1161. https://doi.org/10.1093/gerona/glu034

    Article  Google Scholar 

  35. Steffl M, Bohannon RW, Petr M et al (2015) Relation between cigarette smoking and sarcopenia: Meta-analysis. Physiol Res 64:419–426. https://doi.org/10.33549/physiolres.932802

    Article  CAS  PubMed  Google Scholar 

  36. Dallongeville J, Maré N, Fruchart J-C et al (1998) Community and international nutrition cigarette smoking is associated with unhealthy patterns of nutrient intake: a meta-analysis. J Nutr 128:1450–1457

    Article  CAS  Google Scholar 

  37. Zadak Z, Hyspler R, Ticha A et al (2013) Polypharmacy and malnutrition. Curr Opin Clin Nutr Metab Care 16:50–55. https://doi.org/10.1097/MCO.0b013e32835b612e

    Article  CAS  PubMed  Google Scholar 

  38. Streicher M, van Zwienen-Pot J, Bardon L et al (2018) Determinants of incident malnutrition in community-dwelling older adults: A MaNuEL multicohort meta-analysis. J Am Geriatr Soc 66:2335–2343. https://doi.org/10.1111/jgs.15553

    Article  PubMed  Google Scholar 

  39. Schueren MAE, Lonterman-Monasch S, de Vries OJ et al (2013) Prevalence and determinants for malnutrition in geriatric outpatients. Clin Nutr 32:1007–1011. https://doi.org/10.1016/j.clnu.2013.05.007

    Article  Google Scholar 

  40. Tangen GG, Robinson HS (2020) Measuring physical performance in highly active older adults: associations with age and gender? Aging Clin Exp Res 32:229–237. https://doi.org/10.1007/s40520-019-01190-x

    Article  PubMed  Google Scholar 

  41. Locquet L, Bruyère O, Lengelé L et al (2021) Relationship between smoking and the incidence of sarcopenia: the SarcoPhAge cohort. Public Health. https://doi.org/10.1016/j.puhe.2021.01.017

    Article  PubMed  Google Scholar 

  42. Tombaugh TN, McIntyre NJ (1992) The mini-mental state examination: a comprehensive review. J Am Geriatr Soc 40:922–935. https://doi.org/10.1111/j.1532-5415.1992.tb01992.x

    Article  CAS  PubMed  Google Scholar 

  43. Taylor HL, Jacobs DR, Schucker B et al (1978) A questionnaire for the assessment of leisure time physical activities. J Chronic Dis 31:741–755. https://doi.org/10.1016/0021-9681(78)90058-9

    Article  CAS  PubMed  Google Scholar 

  44. McHugh ML (2012) Lessons in biostatistics interrater reliability: the kappa statistic. Biochem Medica 22:276–282

    Article  Google Scholar 

  45. Remelli F, Vitali A, Zurlo A et al (2019) Vitamin D deficiency and sarcopenia in older persons. Nutrients. https://doi.org/10.3390/nu11122861

    Article  PubMed  PubMed Central  Google Scholar 

  46. Beaudart C, Locquet M, Touvier M et al (2019) Association between dietary nutrient intake and sarcopenia in the SarcoPhAge study. Aging Clin Exp Res 31:815–824. https://doi.org/10.1007/s40520-019-01186-7

    Article  PubMed  Google Scholar 

  47. Rondanelli M, Faliva M, Monteferrario F et al (2015) Novel insights on nutrient management of sarcopenia in elderly. Biomed Res Int. https://doi.org/10.1155/2015/524948

    Article  PubMed  PubMed Central  Google Scholar 

  48. Abiri B, Vafa M (2019) Nutrition and sarcopenia: A review of the evidence of nutritional influences. Crit Rev Food Sci Nutr 59:1456–1466. https://doi.org/10.1080/10408398.2017.1412940

    Article  PubMed  Google Scholar 

  49. Cruz-Jentoft AJ, Kiesswetter E, Drey M et al (2017) Nutrition, frailty, and sarcopenia. Aging Clin Exp Res 29:43–48. https://doi.org/10.1007/s40520-016-0709-0

    Article  PubMed  Google Scholar 

  50. Nascimento CM, Ingles M, Salvador-Pascual A et al (2019) Sarcopenia, frailty and their prevention by exercise. Free Radic Biol Med 132:42–49. https://doi.org/10.1016/j.freeradbiomed.2018.08.035

    Article  CAS  PubMed  Google Scholar 

  51. Robinson SM, Reginster JY, Rizzoli R et al (2018) Does nutrition play a role in the prevention and management of sarcopenia? Clin Nutr 37:1121–1132. https://doi.org/10.1016/j.clnu.2017.08.016

    Article  CAS  PubMed  Google Scholar 

  52. Mithal A, Bonjour JP, Boonen S et al (2013) Impact of nutrition on muscle mass, strength, and performance in older adults. Osteoporos Int 24:1555–1566. https://doi.org/10.1007/s00198-012-2236-y

    Article  CAS  PubMed  Google Scholar 

  53. Simsek H, Meseri R, Sahin S et al (2019) Prevalence of sarcopenia and related factors in community-dwelling elderly individuals. Saudi Med J 40:568–574. https://doi.org/10.15537/smj.2019.6.23917

    Article  PubMed  PubMed Central  Google Scholar 

  54. Alexandre T, Duarte YA, Santos JLF (2018) Prevalence and associated factors of sarcopenia, dynapenia, and sarcodynapenia in community-dwelling elderly in são paulo – sabe study. Rev Bras Epidemiol. https://doi.org/10.1590/1980-549720180009.supl.2

    Article  Google Scholar 

  55. Wu C-H, Chen K-T, Hou M-T et al (2014) Prevalence and associated factors of sarcopenia and severe sarcopenia in older Taiwanese living in rural community: The Tianliao Old People study 04. Geriatr Gerontol Int 14:69–75. https://doi.org/10.1111/ggi.12233

    Article  PubMed  Google Scholar 

  56. Conzade R, Phu S, Vogrin S et al (2019) Changes in nutritional status and musculoskeletal health in a geriatric post-fall care plan setting. Nutrients. https://doi.org/10.3390/nu11071551

    Article  PubMed  PubMed Central  Google Scholar 

  57. Shafiee G, Heshmat R, Ostovar A et al (2020) Comparison of EWGSOP-1and EWGSOP-2 diagnostic criteria on prevalence of and risk factors for sarcopenia among Iranian older people: the Bushehr Elderly Health (BEH) program. J Diabetes Metab Disord 19:727–734. https://doi.org/10.1007/s40200-020-00553-w

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Locquet M, Beaudart C, Petermans J et al (2019) EWGSOP2 versus EWGSOP1: Impact on the prevalence of sarcopenia and its major health consequences. J Am Med Dir Assoc 20:384–385. https://doi.org/10.1016/j.jamda.2018.11.027

    Article  PubMed  Google Scholar 

  59. Cederholm T, Barazzoni R, Austin P et al (2017) ESPEN guidelines on definitions and terminology of clinical nutrition. Clin Nutr 36:49–64. https://doi.org/10.1016/j.clnu.2016.09.004

    Article  CAS  PubMed  Google Scholar 

  60. Cederholm T, Bosaeus I, Barazzoni R et al (2015) Diagnostic criteria for malnutrition - An ESPEN Consensus Statement. Clin Nutr 34:335–340. https://doi.org/10.1016/j.clnu.2015.03.001

    Article  CAS  PubMed  Google Scholar 

  61. Power L, Mullally D, Gibney ER et al (2018) A review of the validity of malnutrition screening tools used in older adults in community and healthcare settings – A MaNuEL study. Clin Nutr ESPEN 24:1–13. https://doi.org/10.1016/j.clnesp.2018.02.005

    Article  PubMed  Google Scholar 

  62. Schueren MAE, Keller H, Cederholm T et al (2020) Global Leadership Initiative on Malnutrition (GLIM): Guidance on validation of the operational criteria for the diagnosis of protein-energy malnutrition in adults. Clin Nutr 39:2872–2880. https://doi.org/10.1016/j.clnu.2019.12.022

    Article  Google Scholar 

  63. Yeung SSY, Chan RSM, Kwok T et al (2020) Malnutrition according to GLIM criteria and adverse outcomes in community-dwelling chinese older adults: a prospective analysis. J Am Med Dir Assoc. https://doi.org/10.1016/j.jamda.2020.09.029

    Article  PubMed  Google Scholar 

  64. McLeod JC, Stokes T, Phillips SM (2019) Resistance exercise training as a primary countermeasure to age-related chronic disease. Front Physiol. https://doi.org/10.3389/fphys.2019.00645

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Funding

M.L. is supported by a fellowship from the FNRS (Fonds National de la Recherche Scientifique de Belgium—FRSFNRS—http://www.frs-fnrs.be).

Author information

Authors and Affiliations

Authors

Contributions

Conceptualization, O.B., C.B., and J.-Y.R.; methodology, L.L., O.B., and M.L.; software, L.L.; validation, L.L., O.B., M.L., C.B. and J.-Y.R.; formal analysis, L.L.; investigation, L.L., M.L. and C.B.; resources, O.B. and J.-Y.R.; data curation, L.L., M.L., and C.B.; writing—original draft preparation, L.L.; writing—review and editing, L.L., M.L., O.B., and C.B.; supervision, O.B. and J.-Y.R. All authors have read and agreed to the published version of the manuscript.

Corresponding author

Correspondence to Laetitia Lengelé.

Ethics declarations

Conflicts of interest

The authors declare no conflict of interest.

Ethics approval

The guidelines of the Declaration of Helsinki were followed, and the present study was approved by the ethics committee of the University of Liege Teaching Hospital (reference 2012/277), with two amendments in 2015 and 2018.

Consent to participate and consent for publication

Informed consent was obtained from all participants involved in the study.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

In the original publication of the article was wrongly published. The correct title is “Malnutrition, assessed by the Global Leadership Initiative on Malnutrition (GLIM) criteria but not by the mini nutritional assessment (MNA), predicts the incidence of sarcopenia over a 5-year period in the SarcoPhAge cohort".

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lengelé, L., Bruyère, O., Beaudart, C. et al. Malnutrition, assessed by the Global Leadership Initiative on Malnutrition (GLIM) criteria but not by the mini nutritional assessment (MNA), predicts the incidence of sarcopenia over a 5-year period in the SarcoPhAge cohort. Aging Clin Exp Res 33, 1507–1517 (2021). https://doi.org/10.1007/s40520-021-01880-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40520-021-01880-5

Keywords

Navigation