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Published in: BMC Geriatrics 1/2024

Open Access 01-12-2024 | Sarcopenia | Research

Sarcopenia in subjects with Alzheimer’s disease: prevalence and comparison of agreement between EGWSOP1, EGWSOP2, and FNIH criteria

Authors: Roberta Barone, Giulia Bramato, Valentina Gnoni, Alessia Giugno, Daniele Urso, Chiara Zecca, Salvatore Nigro, Marco Filardi, Giancarlo Logroscino

Published in: BMC Geriatrics | Issue 1/2024

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Abstract

Background

Sarcopenia is an age-related clinical syndrome characterized by the progressive loss of muscle mass and muscle strength. It appears to be closely linked to dementia, particularly Alzheimer’s disease (AD); however, its prevalence among AD patients remains unclear. In this study, we assessed differences in sarcopenia prevalence between non-demented individuals and AD patients. Moreover, we assessed sex-specific differences in sarcopenia prevalence and explored the diagnostic value of the Muscle Quality Index (MQI) for diagnosing sarcopenia among AD patients.

Method

Cross-sectional study including 145 patients with probable AD and 51 older adults with normal cognition. Sarcopenia was diagnosed according to the criteria of the European Working Group on Sarcopenia in Older People (EWGSOP1 and EWGSOP2) and of the Foundation for the National Institutes of Health (FNIH). The MQI was computed as the ratio of handgrip strength to skeletal muscle mass.

Results

No significant difference in sarcopenia prevalence was observed between AD patients and controls. Prevalence ranged from 3.4 to 23.4% in AD patients and from 2 to 11.8% in controls, depending on diagnostic criteria. Prevalence was higher using EWGSOP1 and decreased using EWGSOP2 and FNIH. Prevalence was higher in males than in females with AD. The MQI was lower in AD patients than in controls (95%CI: − 0.23, − 0.05, p < 0.001), but displayed poor diagnostic accuracy in identifying sarcopenia cases.

Conclusions

AD patients and controls show comparable sarcopenia prevalence. Sarcopenia prevalence is higher in males than females among AD patients and higher when using EWGSOP1 compared to FNIH and EWGSOP2 criteria.
Literature
2.
go back to reference Beaudart C, Zaaria M, Pasleau F, Reginster J-Y, Bruyère O. Health outcomes of sarcopenia: a systematic review and Meta-analysis. PLoS One. 2017;12:e0169548.PubMedPubMedCentralCrossRef Beaudart C, Zaaria M, Pasleau F, Reginster J-Y, Bruyère O. Health outcomes of sarcopenia: a systematic review and Meta-analysis. PLoS One. 2017;12:e0169548.PubMedPubMedCentralCrossRef
3.
go back to reference Yuan S, Larsson SC. Epidemiology of sarcopenia: prevalence, risk factors, and consequences. Metabolism. 2023;144:155533.PubMedCrossRef Yuan S, Larsson SC. Epidemiology of sarcopenia: prevalence, risk factors, and consequences. Metabolism. 2023;144:155533.PubMedCrossRef
4.
go back to reference Papadopoulou SK, Tsintavis P, Potsaki P, Papandreou D. Differences in the prevalence of sarcopenia in community-dwelling, nursing home and hospitalized individuals. A systematic review and Meta-analysis. J Nutr Health Aging. 2020;24:83–90.PubMedCrossRef Papadopoulou SK, Tsintavis P, Potsaki P, Papandreou D. Differences in the prevalence of sarcopenia in community-dwelling, nursing home and hospitalized individuals. A systematic review and Meta-analysis. J Nutr Health Aging. 2020;24:83–90.PubMedCrossRef
5.
go back to reference Waite SJ, Maitland S, Thomas A, Yarnall AJ. Sarcopenia and frailty in individuals with dementia: a systematic review. Arch Gerontol Geriatr. 2021;92:104268.PubMedCrossRef Waite SJ, Maitland S, Thomas A, Yarnall AJ. Sarcopenia and frailty in individuals with dementia: a systematic review. Arch Gerontol Geriatr. 2021;92:104268.PubMedCrossRef
6.
go back to reference Beeri MS, Leugrans SE, Delbono O, Bennett DA, Buchman AS. Sarcopenia is associated with incident Alzheimer’s dementia, mild cognitive impairment, and cognitive decline. J Am Geriatr Soc. 2021;69:1826–35.PubMedPubMedCentralCrossRef Beeri MS, Leugrans SE, Delbono O, Bennett DA, Buchman AS. Sarcopenia is associated with incident Alzheimer’s dementia, mild cognitive impairment, and cognitive decline. J Am Geriatr Soc. 2021;69:1826–35.PubMedPubMedCentralCrossRef
7.
go back to reference Lee HN, Chang YS, Wu YH, Wu CH, Wang CJ. Sarcopenia in female patients with Alzheimer’s disease are more likely to have lower levels of haemoglobin and 25-hydroxyvitamin D. Psychogeriatrics. 2020;20:858–64.PubMedCrossRef Lee HN, Chang YS, Wu YH, Wu CH, Wang CJ. Sarcopenia in female patients with Alzheimer’s disease are more likely to have lower levels of haemoglobin and 25-hydroxyvitamin D. Psychogeriatrics. 2020;20:858–64.PubMedCrossRef
8.
go back to reference Sugimoto T, Ono R, Murata S, et al. Prevalence and associated factors of sarcopenia in elderly subjects with amnestic mild cognitive impairment or Alzheimer disease. Curr Alzheimer Res. 2016;13:718–26.PubMedCrossRef Sugimoto T, Ono R, Murata S, et al. Prevalence and associated factors of sarcopenia in elderly subjects with amnestic mild cognitive impairment or Alzheimer disease. Curr Alzheimer Res. 2016;13:718–26.PubMedCrossRef
9.
go back to reference Hirose D, Hanyu H, Fukasawa R, Hatanaka H, Namioka N, Sakurai H. Frailty and sarcopenia in subjects with Alzheimer’s disease with or without cerebrovascular disease. Geriatr Gerontol Int. 2016;16:1235–6.PubMedCrossRef Hirose D, Hanyu H, Fukasawa R, Hatanaka H, Namioka N, Sakurai H. Frailty and sarcopenia in subjects with Alzheimer’s disease with or without cerebrovascular disease. Geriatr Gerontol Int. 2016;16:1235–6.PubMedCrossRef
10.
go back to reference Ogawa Y, Kaneko Y, Sato T, Shimizu S, Kanetaka H, Hanyu H. Sarcopenia and muscle functions at various stages of Alzheimer disease. Front Neurol. 2018;9:710.PubMedPubMedCentralCrossRef Ogawa Y, Kaneko Y, Sato T, Shimizu S, Kanetaka H, Hanyu H. Sarcopenia and muscle functions at various stages of Alzheimer disease. Front Neurol. 2018;9:710.PubMedPubMedCentralCrossRef
11.
go back to reference Demura T, Okuno T, Miwa T, Iritani O, Nakano H, Yamamoto J, et al. Sarcopenia and decline in appendicular skeletal muscle mass are associated with hypoperfusion in key hubs of central autonomic network on 3DSRT in older adults with progression of normal cognition to Alzheimer’s disease. Geriatr Gerontol Int. 2023;23:16–24.PubMedCrossRef Demura T, Okuno T, Miwa T, Iritani O, Nakano H, Yamamoto J, et al. Sarcopenia and decline in appendicular skeletal muscle mass are associated with hypoperfusion in key hubs of central autonomic network on 3DSRT in older adults with progression of normal cognition to Alzheimer’s disease. Geriatr Gerontol Int. 2023;23:16–24.PubMedCrossRef
12.
go back to reference Cruz-Jentoft AJ, Baeyens JP, Bauer JM, et al. Sarcopenia: European consensus on definition and diagnosis: report of the European working group on sarcopenia in older people. Age Ageing. 2010;39:412–23.PubMedPubMedCentralCrossRef Cruz-Jentoft AJ, Baeyens JP, Bauer JM, et al. Sarcopenia: European consensus on definition and diagnosis: report of the European working group on sarcopenia in older people. Age Ageing. 2010;39:412–23.PubMedPubMedCentralCrossRef
13.
go back to reference Cruz-Jentoft AJ, Bahat G, Bauer J, et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing. 2019;48:16–31.PubMedCrossRef Cruz-Jentoft AJ, Bahat G, Bauer J, et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing. 2019;48:16–31.PubMedCrossRef
14.
go back to reference Studenski SA, Peters KW, Alley DE, et al. The FNIH sarcopenia project: rationale, study description, conference recommendations, and final estimates. J Gerontol A Biol Sci Med Sci. 2014;69:547–58.PubMedPubMedCentralCrossRef Studenski SA, Peters KW, Alley DE, et al. The FNIH sarcopenia project: rationale, study description, conference recommendations, and final estimates. J Gerontol A Biol Sci Med Sci. 2014;69:547–58.PubMedPubMedCentralCrossRef
15.
go back to reference Goodpaster BH, Park SW, Harris TB, Kritchevsky SB, Nevitt M, Schwartz AV, et al. The loss of skeletal muscle strength, mass, and quality in older adults: the health, aging and body composition study. J Gerontol A Biol Sci Med Sci. 2006;61:1059–64.PubMedCrossRef Goodpaster BH, Park SW, Harris TB, Kritchevsky SB, Nevitt M, Schwartz AV, et al. The loss of skeletal muscle strength, mass, and quality in older adults: the health, aging and body composition study. J Gerontol A Biol Sci Med Sci. 2006;61:1059–64.PubMedCrossRef
16.
go back to reference Barbat-Artigas S, Rolland Y, Zamboni M, Aubertin-Leheudre M. How to assess functional status: a new muscle quality index. J Nutr Health Aging. 2012;16:67–77.PubMedCrossRef Barbat-Artigas S, Rolland Y, Zamboni M, Aubertin-Leheudre M. How to assess functional status: a new muscle quality index. J Nutr Health Aging. 2012;16:67–77.PubMedCrossRef
18.
go back to reference American Psychiatric Association. Diagnostic and statistical manual of mental disorders. 5th edition. Arlington, VA; 2013.CrossRef American Psychiatric Association. Diagnostic and statistical manual of mental disorders. 5th edition. Arlington, VA; 2013.CrossRef
19.
go back to reference Filardi M, Barone R, Bramato G, Nigro S, Tafuri B, Frisullo ME, et al. The relationship between muscle strength and cognitive performance across Alzheimer’s disease clinical continuum. Front Neurol. 2022;13:833087.PubMedPubMedCentralCrossRef Filardi M, Barone R, Bramato G, Nigro S, Tafuri B, Frisullo ME, et al. The relationship between muscle strength and cognitive performance across Alzheimer’s disease clinical continuum. Front Neurol. 2022;13:833087.PubMedPubMedCentralCrossRef
20.
go back to reference Weiner MW, Veitch DP, Aisen PS, Beckett LA, Cairns NJ, Green RC, et al. The Alzheimer’s Disease Neuroimaging Initiative 3: continued innovation for clinical trial improvement. Alzheimers Dement. 2017;13:561–71.PubMedCrossRef Weiner MW, Veitch DP, Aisen PS, Beckett LA, Cairns NJ, Green RC, et al. The Alzheimer’s Disease Neuroimaging Initiative 3: continued innovation for clinical trial improvement. Alzheimers Dement. 2017;13:561–71.PubMedCrossRef
21.
go back to reference Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics. 1977;33:159–74.PubMedCrossRef Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics. 1977;33:159–74.PubMedCrossRef
22.
go back to reference Perneczky R, Wagenpfeil S, Komossa K, Grimmer T, Diehl J, Kurz A. Mapping scores onto stages: mini-mental state examination and clinical dementia rating. Am J Geriatr Psychiatry. 2006;14:139–44.PubMedCrossRef Perneczky R, Wagenpfeil S, Komossa K, Grimmer T, Diehl J, Kurz A. Mapping scores onto stages: mini-mental state examination and clinical dementia rating. Am J Geriatr Psychiatry. 2006;14:139–44.PubMedCrossRef
23.
go back to reference Fernandes LV, Paiva AEG, Silva ACB, de Castro IC, Santiago AF, de Oliveira EP, et al. Prevalence of sarcopenia according to EWGSOP1 and EWGSOP2 in older adults and their associations with unfavorable health outcomes: a systematic review. Aging Clin Exp Res. 2022;34:505–14.PubMedCrossRef Fernandes LV, Paiva AEG, Silva ACB, de Castro IC, Santiago AF, de Oliveira EP, et al. Prevalence of sarcopenia according to EWGSOP1 and EWGSOP2 in older adults and their associations with unfavorable health outcomes: a systematic review. Aging Clin Exp Res. 2022;34:505–14.PubMedCrossRef
24.
go back to reference Locquet M, Beaudart C, Petermans J, Reginster J-Y, Bruyère O. EWGSOP2 versus EWGSOP1: impact on the prevalence of sarcopenia and its major health consequences. J Am Med Dir Assoc. 2019;20:384–5.PubMedCrossRef Locquet M, Beaudart C, Petermans J, Reginster J-Y, Bruyère O. EWGSOP2 versus EWGSOP1: impact on the prevalence of sarcopenia and its major health consequences. J Am Med Dir Assoc. 2019;20:384–5.PubMedCrossRef
25.
go back to reference Pagotto V, Silveira EA. Applicability and agreement of different diagnostic criteria for sarcopenia estimation in the elderly. Arch Gerontol Geriatr. 2014;59:288–94.PubMedCrossRef Pagotto V, Silveira EA. Applicability and agreement of different diagnostic criteria for sarcopenia estimation in the elderly. Arch Gerontol Geriatr. 2014;59:288–94.PubMedCrossRef
26.
go back to reference Sosowska N, Pigłowska M, Guligowska A, Sołtysik B, Kostka T. Comparison of agreement between several diagnostic criteria of sarcopenia in community-dwelling older adults. J Frailty Aging. 2022;11:33–9.PubMed Sosowska N, Pigłowska M, Guligowska A, Sołtysik B, Kostka T. Comparison of agreement between several diagnostic criteria of sarcopenia in community-dwelling older adults. J Frailty Aging. 2022;11:33–9.PubMed
27.
go back to reference Chen Y, Zhan Y, Wang H, Zhang H, Cai Y, Wang L, et al. Mediating effect of lower extremity muscle strength on the relationship between mobility and cognitive function in Chinese older adults: a cross-sectional study. Front Aging Neurosci. 2022;14:984075.PubMedPubMedCentralCrossRef Chen Y, Zhan Y, Wang H, Zhang H, Cai Y, Wang L, et al. Mediating effect of lower extremity muscle strength on the relationship between mobility and cognitive function in Chinese older adults: a cross-sectional study. Front Aging Neurosci. 2022;14:984075.PubMedPubMedCentralCrossRef
28.
go back to reference Castillo EM, Goodman-Gruen D, Kritz-Silverstein D, Morton DJ, Wingard DL, Barrett-Connor E. Sarcopenia in elderly men and women: the rancho Bernardo study. Am J Prev Med. 2003;25:226–31.PubMedCrossRef Castillo EM, Goodman-Gruen D, Kritz-Silverstein D, Morton DJ, Wingard DL, Barrett-Connor E. Sarcopenia in elderly men and women: the rancho Bernardo study. Am J Prev Med. 2003;25:226–31.PubMedCrossRef
29.
go back to reference Patel HP, Syddall HE, Jameson K, Robinson S, Denison H, Roberts HC, et al. Prevalence of sarcopenia in community-dwelling older people in the UK using the European working group on sarcopenia in older people (EWGSOP) definition: findings from the Hertfordshire cohort study (HCS). Age Ageing. 2013;42:378–84.PubMedPubMedCentralCrossRef Patel HP, Syddall HE, Jameson K, Robinson S, Denison H, Roberts HC, et al. Prevalence of sarcopenia in community-dwelling older people in the UK using the European working group on sarcopenia in older people (EWGSOP) definition: findings from the Hertfordshire cohort study (HCS). Age Ageing. 2013;42:378–84.PubMedPubMedCentralCrossRef
30.
go back to reference Landi F, Liperoti R, Fusco D, Mastropaolo S, Quattrociocchi D, Proia A, et al. Prevalence and risk factors of sarcopenia among nursing home older residents. J Gerontol A Biol Sci Med Sci. 2012;67:48–55.PubMedCrossRef Landi F, Liperoti R, Fusco D, Mastropaolo S, Quattrociocchi D, Proia A, et al. Prevalence and risk factors of sarcopenia among nursing home older residents. J Gerontol A Biol Sci Med Sci. 2012;67:48–55.PubMedCrossRef
31.
go back to reference Shafiee G, Keshtkar A, Soltani A, Ahadi Z, Larijani B, Heshmat R. Prevalence of sarcopenia in the world: a systematic review and meta- analysis of general population studies. J Diabetes Metab Disord. 2017;16:21.PubMedPubMedCentralCrossRef Shafiee G, Keshtkar A, Soltani A, Ahadi Z, Larijani B, Heshmat R. Prevalence of sarcopenia in the world: a systematic review and meta- analysis of general population studies. J Diabetes Metab Disord. 2017;16:21.PubMedPubMedCentralCrossRef
32.
go back to reference Dennison EM, Sayer AA, Cooper C. Epidemiology of sarcopenia and insight into possible therapeutic targets. Nat Rev Rheumatol. 2017;13:340–7.PubMedCrossRef Dennison EM, Sayer AA, Cooper C. Epidemiology of sarcopenia and insight into possible therapeutic targets. Nat Rev Rheumatol. 2017;13:340–7.PubMedCrossRef
33.
go back to reference Yang L, Smith L, Hamer M. Gender-specific risk factors for incident sarcopenia: 8-year follow-up of the English longitudinal study of ageing. J Epidemiol Community Health. 2019;73:86–8.PubMedCrossRef Yang L, Smith L, Hamer M. Gender-specific risk factors for incident sarcopenia: 8-year follow-up of the English longitudinal study of ageing. J Epidemiol Community Health. 2019;73:86–8.PubMedCrossRef
34.
go back to reference Gheller BJF, Riddle ES, Lem MR, Thalacker-Mercer AE. Understanding age-related changes in skeletal muscle metabolism: differences between females and males. Annu Rev Nutr. 2016;36:129–56.PubMedCrossRef Gheller BJF, Riddle ES, Lem MR, Thalacker-Mercer AE. Understanding age-related changes in skeletal muscle metabolism: differences between females and males. Annu Rev Nutr. 2016;36:129–56.PubMedCrossRef
35.
go back to reference Tay L, Ding YY, Leung BP, Ismail NH, Yeo A, Yew S, et al. Sex-specific differences in risk factors for sarcopenia amongst community-dwelling older adults. Age (Dordr). 2015;37:121.PubMedCrossRef Tay L, Ding YY, Leung BP, Ismail NH, Yeo A, Yew S, et al. Sex-specific differences in risk factors for sarcopenia amongst community-dwelling older adults. Age (Dordr). 2015;37:121.PubMedCrossRef
36.
go back to reference Yang J, Jiang F, Yang M, Chen Z. Sarcopenia and nervous system disorders. J Neurol. 2022;269:5787–97.PubMedCrossRef Yang J, Jiang F, Yang M, Chen Z. Sarcopenia and nervous system disorders. J Neurol. 2022;269:5787–97.PubMedCrossRef
37.
go back to reference Brown WF. A method for estimating the number of motor units in thenar muscles and the changes in motor unit count with ageing. J Neurol Neurosurg Psychiatry. 1972;35:845–52.PubMedPubMedCentralCrossRef Brown WF. A method for estimating the number of motor units in thenar muscles and the changes in motor unit count with ageing. J Neurol Neurosurg Psychiatry. 1972;35:845–52.PubMedPubMedCentralCrossRef
38.
go back to reference Fulle S, Protasi F, Di Tano G, Pietrangelo T, Beltramin A, Boncompagni S, et al. The contribution of reactive oxygen species to sarcopenia and muscle ageing. Exp Gerontol. 2004;39:17–24.PubMedCrossRef Fulle S, Protasi F, Di Tano G, Pietrangelo T, Beltramin A, Boncompagni S, et al. The contribution of reactive oxygen species to sarcopenia and muscle ageing. Exp Gerontol. 2004;39:17–24.PubMedCrossRef
40.
go back to reference Maggio M, Lauretani F, Ceda GP. Sex hormones and sarcopenia in older persons. Curr Opin Clin Nutr Metab Care. 2013;16:3–13.PubMed Maggio M, Lauretani F, Ceda GP. Sex hormones and sarcopenia in older persons. Curr Opin Clin Nutr Metab Care. 2013;16:3–13.PubMed
41.
go back to reference Dent E, Woo J, Scott D, Hoogendijk EO. Toward the recognition and management of sarcopenia in routine clinical care. Nat Aging. 2021;1:982–90.PubMedCrossRef Dent E, Woo J, Scott D, Hoogendijk EO. Toward the recognition and management of sarcopenia in routine clinical care. Nat Aging. 2021;1:982–90.PubMedCrossRef
Metadata
Title
Sarcopenia in subjects with Alzheimer’s disease: prevalence and comparison of agreement between EGWSOP1, EGWSOP2, and FNIH criteria
Authors
Roberta Barone
Giulia Bramato
Valentina Gnoni
Alessia Giugno
Daniele Urso
Chiara Zecca
Salvatore Nigro
Marco Filardi
Giancarlo Logroscino
Publication date
01-12-2024
Publisher
BioMed Central
Published in
BMC Geriatrics / Issue 1/2024
Electronic ISSN: 1471-2318
DOI
https://doi.org/10.1186/s12877-024-04890-w

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