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Correlation between low handgrip strength and metabolic syndrome in older adults: a systematic review

ABSTRACT

Muscle weakness has been associated to insulin resistance and metabolic syndrome in the general population. However, it is still unclear whether this association is maintained in older adults. This study investigated correlations between low handgrip strength (HGS) and metabolic syndrome, or some of its components, in older adults through a systematic review of the literature. Searches were conducted in the Virtual Health Library Regional Portal, Scopus, Cochrane, Embase, MEDLINE/PubMed, SciELO, and Web of Science databases for relevant studies investigating muscle weakness (measured by hand dynamometer) and metabolic syndrome or its components in older adult populations, published up to September 2023. From the 2050 references initially identified, 20 studies, comprising a total of 31,264 older adults of both genders, completely met the inclusion/exclusion criteria. Eighteen studies showed that lower HGS was associated with metabolic syndrome or some of its risk factors, such as abdominal obesity, hyperglycemia, insulin resistance, dyslipidemia, or high blood pressure. Two studies found that older men with high blood pressure had increased HGS. Most studies included in this systematic review revealed a significant correlation between reduced HGS and metabolic syndrome or some of its components, especially abdominal obesity and insulin resistance. We conclude that below-average HGS can be associated with metabolic syndrome in older adults.

Keywords
Metabolic syndrome; central obesity; insulin resistance; aging; handgrip strength

INTRODUCTION

Metabolic syndrome is a combination of three or more risk factors including abdominal obesity, high blood pressure, hyperglycemia, and dyslipidemia, that increases the risk of cardiovascular disease, stroke, and diabetes, and contributes to a decline in longevity (11 Samson SL, Garber AJ. Metabolic Syndrome. Endocrinol Metab Clin North Am. 2014 Mar;43(1):1-23. doi: 10.1016/j.ecl.2013.09.009.
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2 Lakka HM, Laaksonen DE, Lakka TA, Niskanen LK, Kumpusalo E, Tuomilehto J, et al. The Metabolic Syndrome and Total and Cardiovascular Disease Mortality in Middle-Aged Men. JAMA. 2002;288(21):2709-16. doi: 10.1001/jama.288.21.2709.
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-33 Li X, Li X, Lin H, Fu X, Lin W, Li M, et al. Metabolic Syndrome and Stroke: A Meta-Analysis of Prospective Cohort Studies. J Clin Neurosci. 2017;40:34-8. doi: 10.1016/j.jocn.2017.01.018
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). The prevalence of metabolic syndrome in Brazil is high compared to that of other countries (44 de Siqueira Valadares LT, de Souza LSB, Salgado Júnior VA, de Freitas Bonomo L, de Macedo LR, Silva M. Prevalence of Metabolic Syndrome in Brazilian Adults in the Last 10 Years: A Systematic Review and Meta-Analysis. BMC Public Health. 2022;22(1):327. doi: 10.1186/s12889-022-12753-5.
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,55 McCarthy K, Laird E, O'Halloran AM, Fallon P, O'Connor D, Ortuño RR, et al. An Examination of the Prevalence of Metabolic Syndrome in Older Adults in Ireland: Findings from The Irish Longitudinal Study on Ageing (TILDA). PLoS One. 2022;17(9):e0273948. doi: 10.1371/journal.pone.0273948.
https://doi.org/10.1371/journal.pone.027...
), and evidence indicates that incidence increases with age (55 McCarthy K, Laird E, O'Halloran AM, Fallon P, O'Connor D, Ortuño RR, et al. An Examination of the Prevalence of Metabolic Syndrome in Older Adults in Ireland: Findings from The Irish Longitudinal Study on Ageing (TILDA). PLoS One. 2022;17(9):e0273948. doi: 10.1371/journal.pone.0273948.
https://doi.org/10.1371/journal.pone.027...

6 Penninx BW, Nicklas BJ, Newman AB, Harris TB, Goodpaster BH, Satterfield S, et al. Metabolic Syndrome and Physical Decline in Older Persons: Results from the Health, Aging and Body Composition Study. J Gerontol A Biol Sci Med Sci. 2009;64(1):96-102. doi: 10.1093/gerona/gln005.
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). Abnormalities, such as central obesity and hyperglycemia, are predictive of mobility limitations (66 Penninx BW, Nicklas BJ, Newman AB, Harris TB, Goodpaster BH, Satterfield S, et al. Metabolic Syndrome and Physical Decline in Older Persons: Results from the Health, Aging and Body Composition Study. J Gerontol A Biol Sci Med Sci. 2009;64(1):96-102. doi: 10.1093/gerona/gln005.
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), and have been associated with low muscle strength and worse physical performance in older adults (88 Ishii S, Tanaka T, Akishita M, Ouchi Y, Tuji T, Iijima K; Kashiwa study investigators. Metabolic Syndrome, Sarcopenia and Role of Sex and Age: Cross-Sectional Analysis of Kashiwa Cohort Study. PLoS One. 2014;9(11):e112718. doi: 10.1371/journal.pone.0112718.
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,99 Roh E, Choi KM. Health Consequences of Sarcopenic Obesity: A Narrative Review. Front Endocrinol (Lausanne). 2020;11:332. doi: 10.3389/fendo.2020.00332.
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).

Handgrip strength (HGS), measured with a handheld dynamometer, is a simple, non-invasive, and convenient tool to assess upper extremity isometric strength (1010 Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyère O, Cederholm T, et al.; Writing Group for the European Working Group on Sarcopenia in Older People 2 (EWGSOP2), and the Extended Group for EWGSOP2. Sarcopenia: Revised European Consensus on Definition and Diagnosis. Age Ageing. 2019;48(1):16-31. doi: 10.1093/ageing/afy169.
https://doi.org/10.1093/ageing/afy169...
). HGS has been shown to predict mortality in various populations of different ages (1111 Leong DP, Teo KK, Rangarajan S, Lopez-Jaramillo P, Avezum A Jr, Orlandini A, et al.; Prospective Urban Rural Epidemiology (PURE) Study investigators. Prognostic Value of Grip Strength: Findings from the Prospective Urban Rural Epidemiology (PURE) Study. Lancet. 2015;386(9990):266-73. doi: 10.1016/S0140-6736(14)62000-6.
https://doi.org/10.1016/S0140-6736(14)62...
), and cross-sectional and longitudinal relationships with cardiovascular risk, functional impairment, and multimorbidity have been described (1212 Amaral CA, Portela MC, Muniz PT, Farias ES, Araújo TS, Souza OF. Associação da Força de Preensão Manual com Morbidades Referidas em Adultos de Rio Branco, Acre, Brasil: Estudo de Base Populacional. Cad Saúde Pública. 2015;31:1313-25. doi: 10.1590/0102-311X00062214.
https://doi.org/10.1590/0102-311X0006221...

13 De Lima TR, Martins PC, Guerra PH, Santos Silva DA. Muscular Strength and Cardiovascular Risk Factors in Adults: A Systematic Review. Phys Sportsmed. 2021;49(1):18-30. doi: 10.1080/00913847.2020.1796183.
https://doi.org/10.1080/00913847.2020.17...

14 Shen C, Lu J, Xu Z, Xu Y, Yang Y. Association between Handgrip Strength and the Risk of New-Onset Metabolic Syndrome: A Population-Based Cohort Study. BMJ Open. 2020;10(10):e041384. doi: 10.1136/bmjopen-2020-041384.
https://doi.org/10.1136/bmjopen-2020-041...

15 Alkahtani S. Association between Adjusted Handgrip Strength and Metabolic Syndrome in Arab Men. Int J Environ Res Public Health. 2021;18(20):10898. doi: 10.3390/ijerph182010898.
https://doi.org/10.3390/ijerph182010898...
-1616 Ji C, Xia Y, Tong S, Wu Q, Zhao Y. Association of Handgrip Strength with the Prevalence of Metabolic Syndrome in US Adults: The National Health and Nutrition Examination Survey. Aging (Albany NY). 2020;12(9):7818-29. doi: 10.18632/aging.103097.
https://doi.org/10.18632/aging.103097...
). Recent studies have proposed normalizing HGS by body weight or body mass index (BMI) to better define subgroup-specific handgrip weakness, referred to as relative HGS as opposed to absolute HGS. Low absolute and relative HGS consistently correlate with metabolic syndrome in the general population (1717 Wen Y, Liu T, Ma C, Fang J, Zhao Z, Luo M, et al. Association between Handgrip Strength and Metabolic Syndrome: A Meta-Analysis and Systematic Review. Front Nutr. 2022;9:996645. doi: 10.3389/fnut.2022.996645.
https://doi.org/10.3389/fnut.2022.996645...
); however, there is no consensus about this correlation in the older adult population specifically.

HGS has been proposed as a biomarker of frailty and a powerful predictor of future morbidity and mortality (1818 Gómez-Campos R, Vidal Espinoza R, de Arruda M, Ronque ERV, Urra-Albornoz C, Minango JC, et al. Relationship between Age and Handgrip Strength: Proposal of Reference Values from Infancy to Senescence. Front Public Health. 2023;10:1072684. doi: 10.3389/fpubh.2022.1072684.
https://doi.org/10.3389/fpubh.2022.10726...
). HGS naturally decreases with age and is usually lower in women; however, the relationship between chronological age and HGS is nonlinear and can vary between populations (1818 Gómez-Campos R, Vidal Espinoza R, de Arruda M, Ronque ERV, Urra-Albornoz C, Minango JC, et al. Relationship between Age and Handgrip Strength: Proposal of Reference Values from Infancy to Senescence. Front Public Health. 2023;10:1072684. doi: 10.3389/fpubh.2022.1072684.
https://doi.org/10.3389/fpubh.2022.10726...
,1919 Zhang H, Lin S, Gao T, Zhong F, Cai J, Sun Y, et al. Association between Sarcopenia and Metabolic Syndrome in Middle-Aged and Older Non-Obese Adults: A Systematic Review and Meta-Analysis. Nutrients. 2018;10(3):364. doi: 10.3390/nu10030364.
https://doi.org/10.3390/nu10030364...
). Therefore, the present study aimed to systematically review the literature on the correlations between low muscular strength measured by a handheld dynamometer and metabolic syndrome, or some of its components, specifically in the older adult population.

METHODS

Protocol

Before performing the review, a protocol was created by R.A.S. and J.C.D. to define the objective, search strategy, criteria for inclusion and exclusion of studies, data to be extracted, and quality assessment. The hypothesis investigated was whether muscle weakness, as measured with a handheld dynamometer, is associated with metabolic syndrome or any of its components in older adults. This systematic review was conducted and reported according to the Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) statement (2020 Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 Statement: An Updated Guideline for Reporting Systematic Reviews. PLoS Med. 2021;18(3):e1003583. doi: 10.1371/journal.pmed.1003583.
https://doi.org/10.1371/journal.pmed.100...
).

Eligibility criteria

We included original quantitative studies that examined associations between HGS and metabolic syndrome or its risk factors. We used the following a priori criteria in the synthesis: (i) complete original articles that reported (ii) observational studies including cross-sectional, longitudinal, case-control, cohort, or prospective studies; (iii) with analysis of prevalence, correlations, and associations that allowed simultaneous control by covariables or based on regression models, with descriptive, odds ratio, and relative risk data; (iv) that reported HGS (kg) measured with a handheld dynamometer, whether on the dominant hand or both hands, expressed alone (HGS) or combined with body weight or BMI (relative HGS); (v) with metabolic syndrome or its components as outcomes (high blood pressure, elevated waist circumference, high triglycerides, low HDL cholesterol levels, high fasting blood glucose, and/or insulin resistance); which included (vi) community-dwelling older adults or clinical patients (above 60 years old) from any ethnic group.

We excluded studies without a clear definition of metabolic syndrome components or metabolic syndrome diagnostic criteria.

Search strategy

The search was conducted in the Virtual Health Library Regional Portal, Scopus, Cochrane, Embase, MEDLINE/PubMed, SciELO, and Web of Science databases for articles published in Spanish, English, or Portuguese, until 12 March 2023. Afterward, we updated the search to include articles published until September 2023. The descriptors and related terms were searched by sectors: population (Sarcopenia, Muscle Strength, Handgrip Strength, Aged, Elderly, Senescence, Aging); interventions (Muscle Strength, Hand Dynamometer); and Outcomes (Metabolic Syndrome, Insulin Resistance, Cardiovascular Syndrome, Sarcopenia, Muscle Strength Dynamometer). The complete search strategy is fully described in the Supplementary material.

Study selection and data extraction

First, duplicate articles were discarded. Two independent authors (H.G.M.N. and A.C.B.R.J.) selected the titles and abstracts based on the eligibility criteria. Two other authors (T.G.M.N. and A.S.S.) reviewed the full texts. Interrater agreement was 87.5% (Cohen's k = 0.484). Discrepancies in the full-text screening results were discussed with a third author (J.C.D.). Disagreement was resolved by consensus meetings among all authors. We used Rayyan, a free web application that primarily supports systematic review and meta-analysis research (2121 Ouzzani M, Hammady H, Fedorowicz Z, Elmagarmid A. Rayyan – a Web and Mobile App for Systematic Reviews. Syst Rev. 2016;5(1):210. doi: 10.1186/s13643-016-0384-4.
https://doi.org/10.1186/s13643-016-0384-...
).

The following information was extracted: the first author's surname, publication year, country of study, study design, sample size, proportion of males and females, average age, HGS method, dynamometer model, metabolic syndrome outcome, and major findings associating HGS to metabolic syndrome or its components. Correlation coefficients, odds ratios, mean differences, P values, and linear regression statistics were extracted from the full-text studies for inclusion in the synthesis. All information was recorded on a standardized data collection form and checked by all authors.

Quality assessment

The methodological quality of the included studies was assessed by two authors (A.S.C. and J.C.D.) using the Appraisal tool for Cross-Sectional Studies (AXIS) (2222 Downes MJ, Brennan ML, Williams HC, Dean RS. Development of a Critical Appraisal Tool to Assess the Quality of Cross-Sectional Studies (AXIS). BMJ Open. 2016;6(12):e011458. doi: 10.1136/bmjopen-2016-011458.
https://doi.org/10.1136/bmjopen-2016-011...
). AXIS comprises 20 questions evaluating study design, methods, quality, and risk of bias in cross-sectional studies. Studies were scored according to multiple criteria with a final score ranging between 0 and 20. The score was converted into a percentage for comparability. AXIS ratings ≥75%, 50%-74%, and <50% were considered good, moderate, and poor quality, respectively (see supplementary material for scoring template and criteria).

RESULTS

Literature searches

We initially identified 2,050 potential articles. After removing duplicates and reviewing the titles and abstracts, 1,961 articles were excluded. Then, 89 articles underwent a full-text review according to the eligibility criteria. Full-text screening led to the exclusion of 69 articles. In total, 20 studies, comprising a total of 31,264 older adults of both genders, completely met the inclusion criteria and were selected for the qualitative synthesis of this systematic review. Figure 1 shows the selection process scheme.

Figure 1
Flow diagram of data search and selection.

Study characteristics

All the studies included older adults with mean age above 60 years. Two studies included very old participants (above 85 years) in separate groups (2323 Stessman J, Rottenberg Y, Fischer M, Hammerman-Rozenberg A, Jacobs JM. Handgrip Strength in Old and Very Old Adults: Mood, Cognition, Function, and Mortality. J Am Geriatr Soc. 2017;65(3):526-32. doi: 10.1111/jgs.14509.
https://doi.org/10.1111/jgs.14509...
,2424 Taekema DG, Maier AB, Westendorp RG, de Craen AJ. Higher Blood Pressure Is Associated with Higher Handgrip Strength in the Oldest Old. Am J Hypertens. 2011;24(1):83-9. doi: 10.1038/ajh.2010.185.
https://doi.org/10.1038/ajh.2010.185...
). Most studies included older adults of both genders in fairly similar proportions, except two (2525 Zhang W, Zhao Z, Sun X, Tian X. Prevalence of Metabolic Syndrome According to Absolute and Relative Values of Muscle Strength in Middle-Aged and Elderly Women. Int J Environ Res Public Health. 2021;18(17):9073. doi: 10.3390/ijerph18179073.
https://doi.org/10.3390/ijerph18179073...
,2626 Joo KC, Son DH, Park JM. Association between Relative Handgrip Strength and Insulin Resistance in Korean Elderly Men without Diabetes: Findings of the 2015 Korea National Health Nutrition Examination Survey. Korean J Fam Med. 2022;43(3):199-205. doi: 10.4082/kjfm.21.0138.
https://doi.org/10.4082/kjfm.21.0138...
). Most studies included non-institutionalized community-dwelling older adults, except two that recruited nursing home elder (2727 Escribà-Salvans A, Jerez-Roig J, Molas-Tuneu M, Farrés-Godayol P, Moreno-Martin P, Goutan-Roura E, et al. Sarcopenia and Associated Factors According to the EWGSOP2 Criteria in Older People Living in Nursing Homes: A Cross-Sectional Study. BMC Geriatr. 2022;22(1):350. doi: 10.1186/s12877-022-02827-9.
https://doi.org/10.1186/s12877-022-02827...
) and hospitalized individuals (2828 Gong H, Liu Y, Lyu X, Dong L, Zhang X. Lipoprotein Subfractions in Patients with Sarcopenia and Their Relevance to Skeletal Muscle Mass and Function. Exp Gerontol. 2022;159:111668. doi: 10.1016/j.exger.2021.111668.
https://doi.org/10.1016/j.exger.2021.111...
). Two studies included only type 2 diabetic patients (2929 Kimura T, Ushigome E, Hashimoto Y, Nakanishi N, Hamaguchi M, Asano M, et al. Home-Measured Blood Pressure Is Associated with Handgrip Strength in Patients with Type 2 Diabetes: The Kamogawa-HBP Study. J Clin Med. 2021;10(9):1913. doi: 10.3390/jcm10091913.
https://doi.org/10.3390/jcm10091913...
,3030 Leite MM, de Sousa Neto IV, Dutra MT, Funghetto SS, de Oliveira Silva A, da Silva ICR, et al. Predictive Models of Muscle Strength in Older People with Type 2 Diabetes Mellitus. Clin Interv Aging. 2023;18:1535-46. doi: 10.2147/CIA.S414620.
https://doi.org/10.2147/CIA.S414620...
) and one included female patients who visited a healthcare center for preventive purposes, without severe disease (2525 Zhang W, Zhao Z, Sun X, Tian X. Prevalence of Metabolic Syndrome According to Absolute and Relative Values of Muscle Strength in Middle-Aged and Elderly Women. Int J Environ Res Public Health. 2021;18(17):9073. doi: 10.3390/ijerph18179073.
https://doi.org/10.3390/ijerph18179073...
).

Of the 20 studies included, 17 were cross-sectional and 3 were longitudinal. Publications dates ranged from 2007 to 2023, and articles came from 11 different countries. Twelve studies were considered good and two were considered moderate by the AXIS rating. The sample size was above 2,000 in 7 studies, between 1,000 and 2,000 in 2 studies, between 500 and 1,000 in 4 studies, and below 500 in 7 studies. Characteristics of the included studies are summarized in Table 1.

Table 1
Study characteristics

Handgrip strength measures

Twelve studies used digital hand dynamometers, four used hydraulic dynamometers, and four did not state the dynamometer type. Regarding the HGS evaluation, twelve studies used absolute HGS, seven used relative HGS (normalized to body weight), and one used both. Four studies informed the cutoff values for low HGS: <30 kg for men and <20 kg for women in Bibiloni and cols. (3131 Bibiloni MDM, Karam J, Bouzas C, Aparicio-Ugarriza R, Pedrero-Chamizo R, Sureda A, et al. Association between Physical Condition and Body Composition, Nutrient Intake, Sociodemographic Characteristics, and Lifestyle Habits in Older Spanish Adults. Nutrients. 2018;10(11):1608. doi: 10.3390/nu10111608.
https://doi.org/10.3390/nu10111608...
); <28 kg for men and <18 kg for women in Chen and cols. (3232 Chen MZ, Wong MWK, Lim JY, Merchant RA. Frailty and Quality of Life in Older Adults with Metabolic Syndrome – Findings from the Healthy Older People Everyday (HOPE) Study. J Nutr Health Aging. 2021;25(5):637-44. doi: 10.1007/s12603-021-1609-3.
https://doi.org/10.1007/s12603-021-1609-...
); <30 kg for males and <20 kg for females in Lin and cols. (3333 Lin MH, Chang CY, Lu CH, Wu DM, Kuo FC, Kuo CC, et al. Association between Grip Strength and Anthropometric Characteristics in the Community-Dwelling Elderly Population in Taiwan. PLoS One. 2021;16(12):e0260763. doi: 10.1371/journal.pone.0260763.
https://doi.org/10.1371/journal.pone.026...
); and <28 kg for males and <18 kg for females in Tong and cols. (3434 Tong Q, Wang X, Sheng Y, Chen S, Lai B, Lv R, et al. Metabolic Syndrome and Its Association with Components of Sarcopenia in Older Community-Dwelling Chinese. J Biomed Res. 2022;36(2):120-6. doi: 10.7555/JBR.36.20210143.
https://doi.org/10.7555/JBR.36.20210143...
). Two studies used the EWGSOP2 (European Working Group on Sarcopenia in Older People) criteria of weak muscle strength of HGS as <27 kg for men and <16 kg for women (2727 Escribà-Salvans A, Jerez-Roig J, Molas-Tuneu M, Farrés-Godayol P, Moreno-Martin P, Goutan-Roura E, et al. Sarcopenia and Associated Factors According to the EWGSOP2 Criteria in Older People Living in Nursing Homes: A Cross-Sectional Study. BMC Geriatr. 2022;22(1):350. doi: 10.1186/s12877-022-02827-9.
https://doi.org/10.1186/s12877-022-02827...
,3535 Waqas K, Chen J, Trajanoska K, Ikram MA, Uitterlinden AG, Rivadeneira F, et al. Skin Autofluorescence, a Noninvasive Biomarker for Advanced Glycation End-Products, Is Associated with Sarcopenia. J Clin Endocrinol Metab. 2022;107(2):e793-e803. doi: 10.1210/clinem/dgab632.
https://doi.org/10.1210/clinem/dgab632...
). The Brazilian Longitudinal Study of Aging (ELSI-Brazil), a nationally representative sample of older Brazilian adults, considered muscle weakness as HGS values lower than the 20th percentile by age group and sex (3636 de Souza Moreira B, de Souza Andrade AC, Lustosa Torres J, de Souza Braga L, de Carvalho Bastone A, de Melo Mambrini JV, et al. Nationwide Handgrip Strength Values and Factors Associated with Muscle Weakness in Older Adults: Findings from the Brazilian Longitudinal Study of Aging (ELSI-Brazil). BMC Geriatr. 2022;22(1):1005. doi: 10.1186/s12877-022-03721-0.
https://doi.org/10.1186/s12877-022-03721...
). Leite and cols. considered absolute HGS as the sum of the maximum readings from both hands (3030 Leite MM, de Sousa Neto IV, Dutra MT, Funghetto SS, de Oliveira Silva A, da Silva ICR, et al. Predictive Models of Muscle Strength in Older People with Type 2 Diabetes Mellitus. Clin Interv Aging. 2023;18:1535-46. doi: 10.2147/CIA.S414620.
https://doi.org/10.2147/CIA.S414620...
).

The remaining articles studied associations between HGS and some metabolic syndrome parameters or stratified HGS values in groups: Kawamoto and cols. correlated HGS values with metabolic syndrome parameters (3737 Kawamoto R, Ninomiya D, Kasai Y, Kusunoki T, Ohtsuka N, Kumagi T, et al. Handgrip Strength Is Associated with Metabolic Syndrome among Middle-Aged and Elderly Community-Dwelling Persons. Clin Exp Hypertens. 2016;38(2):245-51. doi: 10.3109/10641963.2015.1081232.
https://doi.org/10.3109/10641963.2015.10...
). Some studies divided the participants into quintile groups according to grip strength, grip strength/body weight, and grip strength/BMI for each sex (3838 Chun SW, Kim W, Choi KH. Comparison between Grip Strength and Grip Strength Divided by Body Weight in Their Relationship with Metabolic Syndrome and Quality of Life in the Elderly. PLoS One. 2019;14(9):e0222040. doi: 10.1371/journal.pone.0222040.
https://doi.org/10.1371/journal.pone.022...
), into quartile groups according to grip strength for sex (2323 Stessman J, Rottenberg Y, Fischer M, Hammerman-Rozenberg A, Jacobs JM. Handgrip Strength in Old and Very Old Adults: Mood, Cognition, Function, and Mortality. J Am Geriatr Soc. 2017;65(3):526-32. doi: 10.1111/jgs.14509.
https://doi.org/10.1111/jgs.14509...
,2525 Zhang W, Zhao Z, Sun X, Tian X. Prevalence of Metabolic Syndrome According to Absolute and Relative Values of Muscle Strength in Middle-Aged and Elderly Women. Int J Environ Res Public Health. 2021;18(17):9073. doi: 10.3390/ijerph18179073.
https://doi.org/10.3390/ijerph18179073...
), or into tertiles of relative HGS (T1, ≤1.387 kg/BMI; T2, 1.388-1.613 kg/BMI; and T3, ≥1.614 kg/BMI) (2626 Joo KC, Son DH, Park JM. Association between Relative Handgrip Strength and Insulin Resistance in Korean Elderly Men without Diabetes: Findings of the 2015 Korea National Health Nutrition Examination Survey. Korean J Fam Med. 2022;43(3):199-205. doi: 10.4082/kjfm.21.0138.
https://doi.org/10.4082/kjfm.21.0138...
). Kim and cols. used age-adjusted partial correlation coefficients to estimate the relationship between clinical parameters and absolute or relative HGS (3939 Kim YM, Kim S, Bae J, Kim SH, Won YJ. Association between Relative Hand-Grip Strength and Chronic Cardiometabolic and Musculoskeletal Diseases in Koreans: A Cross-Sectional Study. Arch Gerontol Geriatr. 2021;92:104181. doi: 10.1016/j.archger.2020.104181.
https://doi.org/10.1016/j.archger.2020.1...
). Kimura and cols. performed unadjusted and adjusted regression analyses for HGS and blood pressure (2929 Kimura T, Ushigome E, Hashimoto Y, Nakanishi N, Hamaguchi M, Asano M, et al. Home-Measured Blood Pressure Is Associated with Handgrip Strength in Patients with Type 2 Diabetes: The Kamogawa-HBP Study. J Clin Med. 2021;10(9):1913. doi: 10.3390/jcm10091913.
https://doi.org/10.3390/jcm10091913...
). Merchant and cols. calculated the odds ratio and beta-coefficients of individual HGS indices on risk of metabolic syndrome (4040 Merchant RA, Chan YH, Lim JY, Morley JE. Prevalence of Metabolic Syndrome and Association with Grip Strength in Older Adults: Findings from the HOPE Study. Diabetes Metab Syndr Obes. 2020;13:2677-86. doi: 10.2147/DMSO.S260544.
https://doi.org/10.2147/DMSO.S260544...
). Pérez-Souza and cols. conducted a mediation analysis to determine the indirect effect of fasting glucose levels on the relationship between abdominal obesity and relative HGS (4141 Pérez-Sousa MÁ, Del Pozo-Cruz J, Cano-Gutiérrez CA, Ferrebuz AJ, Sandoval-Cuellar C, Izquierdo M, et al. Glucose Levels as a Mediator of the Detrimental Effect of Abdominal Obesity on Relative Handgrip Strength in Older Adults. J Clin Med. 2020;9(8):2323. doi: 10.3390/jcm9082323.
https://doi.org/10.3390/jcm9082323...
).

Sayer and cols. analyzed relationships between grip strength and components of the metabolic syndrome using partial correlation coefficients and analysis of variance. Using multiple linear regression, the authors calculated sex-specific standard deviation scores for HGS and metabolic syndrome parameters and investigated the relationships between a standard deviation decrease in grip strength and each standard deviation score. Logistic regression models yielded odds ratios (and 95% confidence intervals) for each definition of the metabolic syndrome per standard deviation decrease in HGS (4242 Sayer AA, Syddall HE, Dennison EM, Martin HJ, Phillips DI, Cooper C, et al.; Hertfordshire Cohort. Grip Strength and the Metabolic Syndrome: Findings from the Hertfordshire Cohort Study. QJM. 2007;100(11):707-13. doi: 10.1093/qjmed/hcm095.
https://doi.org/10.1093/qjmed/hcm095...
). Stessman and cols. categorized HGS according to sex-specific quartiles within each age group (70, 78, 85, and 90 years) to compare old and very old populations, with low grip strength defined as the lowest quartile (0%-25%) (2323 Stessman J, Rottenberg Y, Fischer M, Hammerman-Rozenberg A, Jacobs JM. Handgrip Strength in Old and Very Old Adults: Mood, Cognition, Function, and Mortality. J Am Geriatr Soc. 2017;65(3):526-32. doi: 10.1111/jgs.14509.
https://doi.org/10.1111/jgs.14509...
). Taekema and cols. analyzed the association between blood pressure and HGS by linear regression models adjusted for gender, height, and weight (2424 Taekema DG, Maier AB, Westendorp RG, de Craen AJ. Higher Blood Pressure Is Associated with Higher Handgrip Strength in the Oldest Old. Am J Hypertens. 2011;24(1):83-9. doi: 10.1038/ajh.2010.185.
https://doi.org/10.1038/ajh.2010.185...
).

Metabolic syndrome outcomes

From the 20 studies included, six had metabolic syndrome as the primary outcome, diagnosed with criteria established by the National Cholesterol Education Program – Third Adult Treatment Panel (ATP III) (4343 Grundy SM, Cleeman JI, Daniels SR, Donato KA, Eckel RH, Franklin BA, et al.; American Heart Association; National Heart, Lung, and Blood Institute. Diagnosis and Management of the Metabolic Syndrome: An American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement. Circulation. 2005;112(17):2735-52. doi: 10.1161/CIRCULATIONAHA.105.169404.
https://doi.org/10.1161/CIRCULATIONAHA.1...
). The ATP III definition of metabolic syndrome requires three or more of the following five disorders: elevated waist circumference (>102 cm in men and >88 cm in women), hypertriglyceridemia (>150 mg/dL or reported use of triglyceride-lowering drugs), low HDL cholesterol level (<40 mg/dL in men and <50 mg/dL in women or reported use of drugs that increase HDL concentrations), high blood pressure (systolic blood pressure, SBP >130 mmHg and/or diastolic blood pressure >85 mmHg and/or pharmacological treatment), and elevated fasting glucose (>100 mg/dL and/or pharmacological treatment). Of these studies, five used ATP III adjusted for the Asian population, which considers lower cutoff points of waist circumference (>90 cm in men and >80 cm in women).

The other studies used one or more components of metabolic syndrome as outcomes: three studies evaluated blood pressure (2424 Taekema DG, Maier AB, Westendorp RG, de Craen AJ. Higher Blood Pressure Is Associated with Higher Handgrip Strength in the Oldest Old. Am J Hypertens. 2011;24(1):83-9. doi: 10.1038/ajh.2010.185.
https://doi.org/10.1038/ajh.2010.185...
,2929 Kimura T, Ushigome E, Hashimoto Y, Nakanishi N, Hamaguchi M, Asano M, et al. Home-Measured Blood Pressure Is Associated with Handgrip Strength in Patients with Type 2 Diabetes: The Kamogawa-HBP Study. J Clin Med. 2021;10(9):1913. doi: 10.3390/jcm10091913.
https://doi.org/10.3390/jcm10091913...
,4242 Sayer AA, Syddall HE, Dennison EM, Martin HJ, Phillips DI, Cooper C, et al.; Hertfordshire Cohort. Grip Strength and the Metabolic Syndrome: Findings from the Hertfordshire Cohort Study. QJM. 2007;100(11):707-13. doi: 10.1093/qjmed/hcm095.
https://doi.org/10.1093/qjmed/hcm095...
); eight studies evaluated abdominal obesity by waist circumference (2727 Escribà-Salvans A, Jerez-Roig J, Molas-Tuneu M, Farrés-Godayol P, Moreno-Martin P, Goutan-Roura E, et al. Sarcopenia and Associated Factors According to the EWGSOP2 Criteria in Older People Living in Nursing Homes: A Cross-Sectional Study. BMC Geriatr. 2022;22(1):350. doi: 10.1186/s12877-022-02827-9.
https://doi.org/10.1186/s12877-022-02827...
,3030 Leite MM, de Sousa Neto IV, Dutra MT, Funghetto SS, de Oliveira Silva A, da Silva ICR, et al. Predictive Models of Muscle Strength in Older People with Type 2 Diabetes Mellitus. Clin Interv Aging. 2023;18:1535-46. doi: 10.2147/CIA.S414620.
https://doi.org/10.2147/CIA.S414620...
,3131 Bibiloni MDM, Karam J, Bouzas C, Aparicio-Ugarriza R, Pedrero-Chamizo R, Sureda A, et al. Association between Physical Condition and Body Composition, Nutrient Intake, Sociodemographic Characteristics, and Lifestyle Habits in Older Spanish Adults. Nutrients. 2018;10(11):1608. doi: 10.3390/nu10111608.
https://doi.org/10.3390/nu10111608...
,3333 Lin MH, Chang CY, Lu CH, Wu DM, Kuo FC, Kuo CC, et al. Association between Grip Strength and Anthropometric Characteristics in the Community-Dwelling Elderly Population in Taiwan. PLoS One. 2021;16(12):e0260763. doi: 10.1371/journal.pone.0260763.
https://doi.org/10.1371/journal.pone.026...
,3636 de Souza Moreira B, de Souza Andrade AC, Lustosa Torres J, de Souza Braga L, de Carvalho Bastone A, de Melo Mambrini JV, et al. Nationwide Handgrip Strength Values and Factors Associated with Muscle Weakness in Older Adults: Findings from the Brazilian Longitudinal Study of Aging (ELSI-Brazil). BMC Geriatr. 2022;22(1):1005. doi: 10.1186/s12877-022-03721-0.
https://doi.org/10.1186/s12877-022-03721...
,3939 Kim YM, Kim S, Bae J, Kim SH, Won YJ. Association between Relative Hand-Grip Strength and Chronic Cardiometabolic and Musculoskeletal Diseases in Koreans: A Cross-Sectional Study. Arch Gerontol Geriatr. 2021;92:104181. doi: 10.1016/j.archger.2020.104181.
https://doi.org/10.1016/j.archger.2020.1...
,4141 Pérez-Sousa MÁ, Del Pozo-Cruz J, Cano-Gutiérrez CA, Ferrebuz AJ, Sandoval-Cuellar C, Izquierdo M, et al. Glucose Levels as a Mediator of the Detrimental Effect of Abdominal Obesity on Relative Handgrip Strength in Older Adults. J Clin Med. 2020;9(8):2323. doi: 10.3390/jcm9082323.
https://doi.org/10.3390/jcm9082323...
,4242 Sayer AA, Syddall HE, Dennison EM, Martin HJ, Phillips DI, Cooper C, et al.; Hertfordshire Cohort. Grip Strength and the Metabolic Syndrome: Findings from the Hertfordshire Cohort Study. QJM. 2007;100(11):707-13. doi: 10.1093/qjmed/hcm095.
https://doi.org/10.1093/qjmed/hcm095...
); four studies evaluated insulin resistance (2323 Stessman J, Rottenberg Y, Fischer M, Hammerman-Rozenberg A, Jacobs JM. Handgrip Strength in Old and Very Old Adults: Mood, Cognition, Function, and Mortality. J Am Geriatr Soc. 2017;65(3):526-32. doi: 10.1111/jgs.14509.
https://doi.org/10.1111/jgs.14509...
,2626 Joo KC, Son DH, Park JM. Association between Relative Handgrip Strength and Insulin Resistance in Korean Elderly Men without Diabetes: Findings of the 2015 Korea National Health Nutrition Examination Survey. Korean J Fam Med. 2022;43(3):199-205. doi: 10.4082/kjfm.21.0138.
https://doi.org/10.4082/kjfm.21.0138...
,3939 Kim YM, Kim S, Bae J, Kim SH, Won YJ. Association between Relative Hand-Grip Strength and Chronic Cardiometabolic and Musculoskeletal Diseases in Koreans: A Cross-Sectional Study. Arch Gerontol Geriatr. 2021;92:104181. doi: 10.1016/j.archger.2020.104181.
https://doi.org/10.1016/j.archger.2020.1...
,4141 Pérez-Sousa MÁ, Del Pozo-Cruz J, Cano-Gutiérrez CA, Ferrebuz AJ, Sandoval-Cuellar C, Izquierdo M, et al. Glucose Levels as a Mediator of the Detrimental Effect of Abdominal Obesity on Relative Handgrip Strength in Older Adults. J Clin Med. 2020;9(8):2323. doi: 10.3390/jcm9082323.
https://doi.org/10.3390/jcm9082323...
); and three studies evaluated diabetic patients (2323 Stessman J, Rottenberg Y, Fischer M, Hammerman-Rozenberg A, Jacobs JM. Handgrip Strength in Old and Very Old Adults: Mood, Cognition, Function, and Mortality. J Am Geriatr Soc. 2017;65(3):526-32. doi: 10.1111/jgs.14509.
https://doi.org/10.1111/jgs.14509...
,2929 Kimura T, Ushigome E, Hashimoto Y, Nakanishi N, Hamaguchi M, Asano M, et al. Home-Measured Blood Pressure Is Associated with Handgrip Strength in Patients with Type 2 Diabetes: The Kamogawa-HBP Study. J Clin Med. 2021;10(9):1913. doi: 10.3390/jcm10091913.
https://doi.org/10.3390/jcm10091913...
,3030 Leite MM, de Sousa Neto IV, Dutra MT, Funghetto SS, de Oliveira Silva A, da Silva ICR, et al. Predictive Models of Muscle Strength in Older People with Type 2 Diabetes Mellitus. Clin Interv Aging. 2023;18:1535-46. doi: 10.2147/CIA.S414620.
https://doi.org/10.2147/CIA.S414620...
). One study used skin autofluorescence as the primary outcome, a biomarker of advanced glycated end-products (AGE) resulting from chronic hyperglycemia, and found it inversely associated with HGS. In addition, the highest quartile of AGE biomarker comprised a significantly higher number of individuals with diabetes and weak HGS (3535 Waqas K, Chen J, Trajanoska K, Ikram MA, Uitterlinden AG, Rivadeneira F, et al. Skin Autofluorescence, a Noninvasive Biomarker for Advanced Glycation End-Products, Is Associated with Sarcopenia. J Clin Endocrinol Metab. 2022;107(2):e793-e803. doi: 10.1210/clinem/dgab632.
https://doi.org/10.1210/clinem/dgab632...
). Two studies included patients with prevalent chronic diseases, such as type 2 diabetes, hypertension, hyperlipidemia, myocardial infarction/angina, cerebrovascular accident, osteoarthritis, or osteoporosis (2929 Kimura T, Ushigome E, Hashimoto Y, Nakanishi N, Hamaguchi M, Asano M, et al. Home-Measured Blood Pressure Is Associated with Handgrip Strength in Patients with Type 2 Diabetes: The Kamogawa-HBP Study. J Clin Med. 2021;10(9):1913. doi: 10.3390/jcm10091913.
https://doi.org/10.3390/jcm10091913...
,3030 Leite MM, de Sousa Neto IV, Dutra MT, Funghetto SS, de Oliveira Silva A, da Silva ICR, et al. Predictive Models of Muscle Strength in Older People with Type 2 Diabetes Mellitus. Clin Interv Aging. 2023;18:1535-46. doi: 10.2147/CIA.S414620.
https://doi.org/10.2147/CIA.S414620...
).

Associations of low HGS with metabolic syndrome or its components

Most studies included in this systematic review found an inverse correlation between HGS and metabolic syndrome or its components. Older adult patients with insulin resistance consistently presented low HGS in different studies (2323 Stessman J, Rottenberg Y, Fischer M, Hammerman-Rozenberg A, Jacobs JM. Handgrip Strength in Old and Very Old Adults: Mood, Cognition, Function, and Mortality. J Am Geriatr Soc. 2017;65(3):526-32. doi: 10.1111/jgs.14509.
https://doi.org/10.1111/jgs.14509...
,2626 Joo KC, Son DH, Park JM. Association between Relative Handgrip Strength and Insulin Resistance in Korean Elderly Men without Diabetes: Findings of the 2015 Korea National Health Nutrition Examination Survey. Korean J Fam Med. 2022;43(3):199-205. doi: 10.4082/kjfm.21.0138.
https://doi.org/10.4082/kjfm.21.0138...
,3535 Waqas K, Chen J, Trajanoska K, Ikram MA, Uitterlinden AG, Rivadeneira F, et al. Skin Autofluorescence, a Noninvasive Biomarker for Advanced Glycation End-Products, Is Associated with Sarcopenia. J Clin Endocrinol Metab. 2022;107(2):e793-e803. doi: 10.1210/clinem/dgab632.
https://doi.org/10.1210/clinem/dgab632...
,3636 de Souza Moreira B, de Souza Andrade AC, Lustosa Torres J, de Souza Braga L, de Carvalho Bastone A, de Melo Mambrini JV, et al. Nationwide Handgrip Strength Values and Factors Associated with Muscle Weakness in Older Adults: Findings from the Brazilian Longitudinal Study of Aging (ELSI-Brazil). BMC Geriatr. 2022;22(1):1005. doi: 10.1186/s12877-022-03721-0.
https://doi.org/10.1186/s12877-022-03721...
). Sayer and cols. found that decreased HGS was associated with higher blood pressure in a population-based study of older men and women (4242 Sayer AA, Syddall HE, Dennison EM, Martin HJ, Phillips DI, Cooper C, et al.; Hertfordshire Cohort. Grip Strength and the Metabolic Syndrome: Findings from the Hertfordshire Cohort Study. QJM. 2007;100(11):707-13. doi: 10.1093/qjmed/hcm095.
https://doi.org/10.1093/qjmed/hcm095...
). On the other hand, Taekema and cols. found that higher blood pressure was associated with higher HGS only in the oldest subjects (>85 years), while in middle-aged adults, blood pressure and HGS were not significantly associated (2424 Taekema DG, Maier AB, Westendorp RG, de Craen AJ. Higher Blood Pressure Is Associated with Higher Handgrip Strength in the Oldest Old. Am J Hypertens. 2011;24(1):83-9. doi: 10.1038/ajh.2010.185.
https://doi.org/10.1038/ajh.2010.185...
). Tong and cols. found an association between high HGS and high SBP in older men (3434 Tong Q, Wang X, Sheng Y, Chen S, Lai B, Lv R, et al. Metabolic Syndrome and Its Association with Components of Sarcopenia in Older Community-Dwelling Chinese. J Biomed Res. 2022;36(2):120-6. doi: 10.7555/JBR.36.20210143.
https://doi.org/10.7555/JBR.36.20210143...
), and Kimura and cols. found that diabetic male patients with high blood pressure had higher HGS (2929 Kimura T, Ushigome E, Hashimoto Y, Nakanishi N, Hamaguchi M, Asano M, et al. Home-Measured Blood Pressure Is Associated with Handgrip Strength in Patients with Type 2 Diabetes: The Kamogawa-HBP Study. J Clin Med. 2021;10(9):1913. doi: 10.3390/jcm10091913.
https://doi.org/10.3390/jcm10091913...
).

Six studies showed that reduced HGS was associated with metabolic syndrome (2525 Zhang W, Zhao Z, Sun X, Tian X. Prevalence of Metabolic Syndrome According to Absolute and Relative Values of Muscle Strength in Middle-Aged and Elderly Women. Int J Environ Res Public Health. 2021;18(17):9073. doi: 10.3390/ijerph18179073.
https://doi.org/10.3390/ijerph18179073...
,3232 Chen MZ, Wong MWK, Lim JY, Merchant RA. Frailty and Quality of Life in Older Adults with Metabolic Syndrome – Findings from the Healthy Older People Everyday (HOPE) Study. J Nutr Health Aging. 2021;25(5):637-44. doi: 10.1007/s12603-021-1609-3.
https://doi.org/10.1007/s12603-021-1609-...
,3737 Kawamoto R, Ninomiya D, Kasai Y, Kusunoki T, Ohtsuka N, Kumagi T, et al. Handgrip Strength Is Associated with Metabolic Syndrome among Middle-Aged and Elderly Community-Dwelling Persons. Clin Exp Hypertens. 2016;38(2):245-51. doi: 10.3109/10641963.2015.1081232.
https://doi.org/10.3109/10641963.2015.10...
,3838 Chun SW, Kim W, Choi KH. Comparison between Grip Strength and Grip Strength Divided by Body Weight in Their Relationship with Metabolic Syndrome and Quality of Life in the Elderly. PLoS One. 2019;14(9):e0222040. doi: 10.1371/journal.pone.0222040.
https://doi.org/10.1371/journal.pone.022...
,4040 Merchant RA, Chan YH, Lim JY, Morley JE. Prevalence of Metabolic Syndrome and Association with Grip Strength in Older Adults: Findings from the HOPE Study. Diabetes Metab Syndr Obes. 2020;13:2677-86. doi: 10.2147/DMSO.S260544.
https://doi.org/10.2147/DMSO.S260544...
,4242 Sayer AA, Syddall HE, Dennison EM, Martin HJ, Phillips DI, Cooper C, et al.; Hertfordshire Cohort. Grip Strength and the Metabolic Syndrome: Findings from the Hertfordshire Cohort Study. QJM. 2007;100(11):707-13. doi: 10.1093/qjmed/hcm095.
https://doi.org/10.1093/qjmed/hcm095...
). Chen and cols. included only participants with metabolic syndrome. The authors found a higher prevalence of reduced HGS in the metabolic syndrome frail, who were also older, with an increased prevalence of diabetes and low HDL compared to that of metabolic syndrome robust participants (3232 Chen MZ, Wong MWK, Lim JY, Merchant RA. Frailty and Quality of Life in Older Adults with Metabolic Syndrome – Findings from the Healthy Older People Everyday (HOPE) Study. J Nutr Health Aging. 2021;25(5):637-44. doi: 10.1007/s12603-021-1609-3.
https://doi.org/10.1007/s12603-021-1609-...
). Zhang and cols. found a higher prevalence of metabolic syndrome in women with low relative HGS (2525 Zhang W, Zhao Z, Sun X, Tian X. Prevalence of Metabolic Syndrome According to Absolute and Relative Values of Muscle Strength in Middle-Aged and Elderly Women. Int J Environ Res Public Health. 2021;18(17):9073. doi: 10.3390/ijerph18179073.
https://doi.org/10.3390/ijerph18179073...
). Chun and Kawamoto found inverse correlations between relative HGS and metabolic syndrome (3737 Kawamoto R, Ninomiya D, Kasai Y, Kusunoki T, Ohtsuka N, Kumagi T, et al. Handgrip Strength Is Associated with Metabolic Syndrome among Middle-Aged and Elderly Community-Dwelling Persons. Clin Exp Hypertens. 2016;38(2):245-51. doi: 10.3109/10641963.2015.1081232.
https://doi.org/10.3109/10641963.2015.10...
,3838 Chun SW, Kim W, Choi KH. Comparison between Grip Strength and Grip Strength Divided by Body Weight in Their Relationship with Metabolic Syndrome and Quality of Life in the Elderly. PLoS One. 2019;14(9):e0222040. doi: 10.1371/journal.pone.0222040.
https://doi.org/10.1371/journal.pone.022...
). Merchant and cols. and Sayer and cols. found that relative HGS was associated with decreased odds of having metabolic syndrome (4040 Merchant RA, Chan YH, Lim JY, Morley JE. Prevalence of Metabolic Syndrome and Association with Grip Strength in Older Adults: Findings from the HOPE Study. Diabetes Metab Syndr Obes. 2020;13:2677-86. doi: 10.2147/DMSO.S260544.
https://doi.org/10.2147/DMSO.S260544...
,4242 Sayer AA, Syddall HE, Dennison EM, Martin HJ, Phillips DI, Cooper C, et al.; Hertfordshire Cohort. Grip Strength and the Metabolic Syndrome: Findings from the Hertfordshire Cohort Study. QJM. 2007;100(11):707-13. doi: 10.1093/qjmed/hcm095.
https://doi.org/10.1093/qjmed/hcm095...
). However, Tong and cols. found a positive correlation between HGS and metabolic syndrome in older men (3434 Tong Q, Wang X, Sheng Y, Chen S, Lai B, Lv R, et al. Metabolic Syndrome and Its Association with Components of Sarcopenia in Older Community-Dwelling Chinese. J Biomed Res. 2022;36(2):120-6. doi: 10.7555/JBR.36.20210143.
https://doi.org/10.7555/JBR.36.20210143...
).

Chun and cols. analyzed the relationship between HGS and relative HGS (grip strength/body weight or grip strength/BMI) and metabolic syndrome using the data of 1,273 men and 1,436 women aged 60-80 years. Absolute HGS was not associated with metabolic syndrome, whereas relative HGS measures were inversely associated with metabolic syndrome in both sexes. Between relative HGS measures tested, HGS divided by body weight was better associated with metabolic syndrome (3838 Chun SW, Kim W, Choi KH. Comparison between Grip Strength and Grip Strength Divided by Body Weight in Their Relationship with Metabolic Syndrome and Quality of Life in the Elderly. PLoS One. 2019;14(9):e0222040. doi: 10.1371/journal.pone.0222040.
https://doi.org/10.1371/journal.pone.022...
).

Eight studies found consistent associations between central obesity and muscle weakness measured by HGS (2727 Escribà-Salvans A, Jerez-Roig J, Molas-Tuneu M, Farrés-Godayol P, Moreno-Martin P, Goutan-Roura E, et al. Sarcopenia and Associated Factors According to the EWGSOP2 Criteria in Older People Living in Nursing Homes: A Cross-Sectional Study. BMC Geriatr. 2022;22(1):350. doi: 10.1186/s12877-022-02827-9.
https://doi.org/10.1186/s12877-022-02827...
,2929 Kimura T, Ushigome E, Hashimoto Y, Nakanishi N, Hamaguchi M, Asano M, et al. Home-Measured Blood Pressure Is Associated with Handgrip Strength in Patients with Type 2 Diabetes: The Kamogawa-HBP Study. J Clin Med. 2021;10(9):1913. doi: 10.3390/jcm10091913.
https://doi.org/10.3390/jcm10091913...
,3030 Leite MM, de Sousa Neto IV, Dutra MT, Funghetto SS, de Oliveira Silva A, da Silva ICR, et al. Predictive Models of Muscle Strength in Older People with Type 2 Diabetes Mellitus. Clin Interv Aging. 2023;18:1535-46. doi: 10.2147/CIA.S414620.
https://doi.org/10.2147/CIA.S414620...
,3333 Lin MH, Chang CY, Lu CH, Wu DM, Kuo FC, Kuo CC, et al. Association between Grip Strength and Anthropometric Characteristics in the Community-Dwelling Elderly Population in Taiwan. PLoS One. 2021;16(12):e0260763. doi: 10.1371/journal.pone.0260763.
https://doi.org/10.1371/journal.pone.026...
,3535 Waqas K, Chen J, Trajanoska K, Ikram MA, Uitterlinden AG, Rivadeneira F, et al. Skin Autofluorescence, a Noninvasive Biomarker for Advanced Glycation End-Products, Is Associated with Sarcopenia. J Clin Endocrinol Metab. 2022;107(2):e793-e803. doi: 10.1210/clinem/dgab632.
https://doi.org/10.1210/clinem/dgab632...
,3636 de Souza Moreira B, de Souza Andrade AC, Lustosa Torres J, de Souza Braga L, de Carvalho Bastone A, de Melo Mambrini JV, et al. Nationwide Handgrip Strength Values and Factors Associated with Muscle Weakness in Older Adults: Findings from the Brazilian Longitudinal Study of Aging (ELSI-Brazil). BMC Geriatr. 2022;22(1):1005. doi: 10.1186/s12877-022-03721-0.
https://doi.org/10.1186/s12877-022-03721...
,3939 Kim YM, Kim S, Bae J, Kim SH, Won YJ. Association between Relative Hand-Grip Strength and Chronic Cardiometabolic and Musculoskeletal Diseases in Koreans: A Cross-Sectional Study. Arch Gerontol Geriatr. 2021;92:104181. doi: 10.1016/j.archger.2020.104181.
https://doi.org/10.1016/j.archger.2020.1...
,4141 Pérez-Sousa MÁ, Del Pozo-Cruz J, Cano-Gutiérrez CA, Ferrebuz AJ, Sandoval-Cuellar C, Izquierdo M, et al. Glucose Levels as a Mediator of the Detrimental Effect of Abdominal Obesity on Relative Handgrip Strength in Older Adults. J Clin Med. 2020;9(8):2323. doi: 10.3390/jcm9082323.
https://doi.org/10.3390/jcm9082323...
). Kim and cols. showed that relative HGS was inversely correlated with waist circumference and insulin resistance and the authors reported a direct correlation between HGS and HDL cholesterol levels (3939 Kim YM, Kim S, Bae J, Kim SH, Won YJ. Association between Relative Hand-Grip Strength and Chronic Cardiometabolic and Musculoskeletal Diseases in Koreans: A Cross-Sectional Study. Arch Gerontol Geriatr. 2021;92:104181. doi: 10.1016/j.archger.2020.104181.
https://doi.org/10.1016/j.archger.2020.1...
). High odds ratio for various chronic diseases in the lowest relative HGS tertile were observed for both sexes, while high odds for hyperlipidemia was observed only in women (3939 Kim YM, Kim S, Bae J, Kim SH, Won YJ. Association between Relative Hand-Grip Strength and Chronic Cardiometabolic and Musculoskeletal Diseases in Koreans: A Cross-Sectional Study. Arch Gerontol Geriatr. 2021;92:104181. doi: 10.1016/j.archger.2020.104181.
https://doi.org/10.1016/j.archger.2020.1...
). Pérez-Sousa and cols. showed that waist circumference and higher levels of fasting glucose were inversely correlated with relative HGS (4141 Pérez-Sousa MÁ, Del Pozo-Cruz J, Cano-Gutiérrez CA, Ferrebuz AJ, Sandoval-Cuellar C, Izquierdo M, et al. Glucose Levels as a Mediator of the Detrimental Effect of Abdominal Obesity on Relative Handgrip Strength in Older Adults. J Clin Med. 2020;9(8):2323. doi: 10.3390/jcm9082323.
https://doi.org/10.3390/jcm9082323...
).

Sayer and cols. found that decreased HGS was associated with increased waist circumference and high triglyceride levels, high blood pressure, hyperglycemia, and insulin resistance (4242 Sayer AA, Syddall HE, Dennison EM, Martin HJ, Phillips DI, Cooper C, et al.; Hertfordshire Cohort. Grip Strength and the Metabolic Syndrome: Findings from the Hertfordshire Cohort Study. QJM. 2007;100(11):707-13. doi: 10.1093/qjmed/hcm095.
https://doi.org/10.1093/qjmed/hcm095...
). Joo and cols. also reported an increased prevalence of insulin resistance among the lower HGS subjects (2626 Joo KC, Son DH, Park JM. Association between Relative Handgrip Strength and Insulin Resistance in Korean Elderly Men without Diabetes: Findings of the 2015 Korea National Health Nutrition Examination Survey. Korean J Fam Med. 2022;43(3):199-205. doi: 10.4082/kjfm.21.0138.
https://doi.org/10.4082/kjfm.21.0138...
). Gong and cols. used lipoproteins as primary outcomes and found an inverse correlation between HGS and triglycerides and other lipoprotein subfractions (2828 Gong H, Liu Y, Lyu X, Dong L, Zhang X. Lipoprotein Subfractions in Patients with Sarcopenia and Their Relevance to Skeletal Muscle Mass and Function. Exp Gerontol. 2022;159:111668. doi: 10.1016/j.exger.2021.111668.
https://doi.org/10.1016/j.exger.2021.111...
).

One study used skin autofluorescence as the primary outcome, a biomarker of advanced glycated end-products (AGE) resulting from chronic hyperglycemia, and found it inversely associated with HGS. Also, the highest quartile of AGE biomarker contained a significantly higher number of individuals with diabetes and weak HGS (3535 Waqas K, Chen J, Trajanoska K, Ikram MA, Uitterlinden AG, Rivadeneira F, et al. Skin Autofluorescence, a Noninvasive Biomarker for Advanced Glycation End-Products, Is Associated with Sarcopenia. J Clin Endocrinol Metab. 2022;107(2):e793-e803. doi: 10.1210/clinem/dgab632.
https://doi.org/10.1210/clinem/dgab632...
).

DISCUSSION

This systematic review identified 20 studies investigating associations between muscle strength measured with a handheld dynamometer and the occurrence of metabolic syndrome or some of its components in older adults. Most studies found consistent correlations between lower HGS and metabolic syndrome or its risk factors in older adults. Among metabolic syndrome components, high blood pressure was the only one that correlated with stronger handgrip in the older adults (2424 Taekema DG, Maier AB, Westendorp RG, de Craen AJ. Higher Blood Pressure Is Associated with Higher Handgrip Strength in the Oldest Old. Am J Hypertens. 2011;24(1):83-9. doi: 10.1038/ajh.2010.185.
https://doi.org/10.1038/ajh.2010.185...
).

This qualitative synthesis indicates that low HGS in older adults is significantly associated with metabolic syndrome and with some of its components, except hypertension. In a recent nationwide cross-sectional study in Korea with 77,991 participants, high relative HGS was significantly associated with reduced risk of hypertension in adult and middle-aged (4444 Park JH, Lim NK, Park HY. Relative Handgrip Strength Is Inversely Associated with Hypertension in Consideration of Visceral Adipose Dysfunction: A Nationwide Cross-Sectional Study in Korea. Front Physiol. 2022;13:930922. doi: 10.3389/fphys.2022.930922.
https://doi.org/10.3389/fphys.2022.93092...
). Thus, maintaining high relative HGS may be associated with protective benefits against hypertension in the long term. However, some studies included in this systematic review showed that a higher blood pressure was associated with higher HGS, especially in older diabetic men (2929 Kimura T, Ushigome E, Hashimoto Y, Nakanishi N, Hamaguchi M, Asano M, et al. Home-Measured Blood Pressure Is Associated with Handgrip Strength in Patients with Type 2 Diabetes: The Kamogawa-HBP Study. J Clin Med. 2021;10(9):1913. doi: 10.3390/jcm10091913.
https://doi.org/10.3390/jcm10091913...
) and in very old Caucasian subjects (>85 years) (2424 Taekema DG, Maier AB, Westendorp RG, de Craen AJ. Higher Blood Pressure Is Associated with Higher Handgrip Strength in the Oldest Old. Am J Hypertens. 2011;24(1):83-9. doi: 10.1038/ajh.2010.185.
https://doi.org/10.1038/ajh.2010.185...
). Evidence indicates that in the very old adults, higher blood pressure may be protective because it is associated with preservation of renal function (4545 van Bemmel T, Woittiez K, Blauw GJ, van der Sman-de Beer F, Dekker FW, Westendorp RG, et al. Prospective Study of the Effect of Blood Pressure on Renal Function in Old Age: The Leiden 85-Plus Study. J Am Soc Nephrol. 2006;17(9):2561-6. doi: 10.1681/ASN.2005090902.
https://doi.org/10.1681/ASN.2005090902...
), better cognition (4646 Nilsson SE, Read S, Berg S, Johansson B, Melander A, Lindblad U. Low Systolic Blood Pressure Is Associated with Impaired Cognitive Function in the Oldest Old: Longitudinal Observations in a Population-Based Sample 80 Years and Older. Aging Clin Exp Res. 2007;19(1):41-7. doi: 10.1007/BF03325209.
https://doi.org/10.1007/BF03325209...

47 Euser SM, van Bemmel T, Schram MT, Gussekloo J, Hofman A, Westendorp RG, et al. The Effect of Age on the Association Between Blood Pressure and Cognitive Function Later in Life. J Am Geriatr Soc. 2009;57(7):1232-7. doi: 10.1111/j.1532-5415.2009.02264.x.
https://doi.org/10.1111/j.1532-5415.2009...
-4848 Molander L, Gustafson Y, Lövheim H. Low Blood Pressure Is Associated with Cognitive Impairment in Very Old People. Dement Geriatr Cogn Disord. 2010;29(4):335-41. doi: 10.1159/000289821.
https://doi.org/10.1159/000289821...
), and muscular strength, conditions that significantly depend on vascular function. The increased vascular resistance with aging was speculated to require greater blood pressure to maintain tissue perfusion and prevent further damage to ischemic peripheral organs, such as skeletal muscles (2424 Taekema DG, Maier AB, Westendorp RG, de Craen AJ. Higher Blood Pressure Is Associated with Higher Handgrip Strength in the Oldest Old. Am J Hypertens. 2011;24(1):83-9. doi: 10.1038/ajh.2010.185.
https://doi.org/10.1038/ajh.2010.185...
,3434 Tong Q, Wang X, Sheng Y, Chen S, Lai B, Lv R, et al. Metabolic Syndrome and Its Association with Components of Sarcopenia in Older Community-Dwelling Chinese. J Biomed Res. 2022;36(2):120-6. doi: 10.7555/JBR.36.20210143.
https://doi.org/10.7555/JBR.36.20210143...
).

The age-related decline in muscle mass and function is one of the most prevalent health problems in older adults, with a high rate of adverse outcomes (4949 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. doi: 10.1186/s40200-017-0302-x.
https://doi.org/10.1186/s40200-017-0302-...
). Pathological changes to this vital metabolically active tissue can profoundly affect older adults. According to the 2019 Sarcopenia Consensus, patients that have below-average HGS can be classified as "probable sarcopenia" and need further muscle evaluation to confirm the diagnosis. Sarcopenia has been associated with acute and chronic disease states, increased insulin resistance, fatigue, falls, and mortality (5050 Walston JD. Sarcopenia in Older Adults. Curr Opin Rheumatol. 2012;24(6):623-7. doi: 10.1097/BOR.0b013e328358d59b.
https://doi.org/10.1097/BOR.0b013e328358...
,5151 Murai J, Nishizawa H, Otsuka A, Fukuda S, Tanaka Y, Nagao H, et al. Low Muscle Quality in Japanese Type 2 Diabetic Patients with Visceral Fat Accumulation. Cardiovasc Diabetol. 2018;17(1):112. doi: 10.1186/s12933-018-0755-3.
https://doi.org/10.1186/s12933-018-0755-...
), and is a powerful predictor of late-life disability (5252 Fielding RA, Vellas B, Evans WJ, Bhasin S, Morley JE, Newman AB, et al. Sarcopenia: An Undiagnosed Condition in Older Adults. Current Consensus Definition: Prevalence, Etiology, and Consequences. International Working Group on Sarcopenia. Am Med Dir Assoc. 2011;12(4):249-56. doi: 10.1016/j.jamda.2011.01.003.
https://doi.org/10.1016/j.jamda.2011.01....
,5353 Rantanen T, Guralnik JM, Foley D, Masaki K, Leveille S, Curb JD, et al. Midlife Hand Grip Strength as a Predictor of Old Age Disability. JAMA. 1999;281(6):558-60. doi: 10.1001/jama.281.6.558.
https://doi.org/10.1001/jama.281.6.558...
). Metabolic syndrome and sarcopenia adversely affect the quality of life and contribute to increased frailty, weakness, dependence, morbidity, and mortality, all conditions that have been associated with aging and reduced HGS (66 Penninx BW, Nicklas BJ, Newman AB, Harris TB, Goodpaster BH, Satterfield S, et al. Metabolic Syndrome and Physical Decline in Older Persons: Results from the Health, Aging and Body Composition Study. J Gerontol A Biol Sci Med Sci. 2009;64(1):96-102. doi: 10.1093/gerona/gln005.
https://doi.org/10.1093/gerona/gln005...
,1818 Gómez-Campos R, Vidal Espinoza R, de Arruda M, Ronque ERV, Urra-Albornoz C, Minango JC, et al. Relationship between Age and Handgrip Strength: Proposal of Reference Values from Infancy to Senescence. Front Public Health. 2023;10:1072684. doi: 10.3389/fpubh.2022.1072684.
https://doi.org/10.3389/fpubh.2022.10726...
,5454 Volaklis KA, Halle M, Meisinger C. Muscular Strength as a Strong Predictor of Mortality: A Narrative Review. Eur J Intern Med. 2015;26(5):303-10. doi: 10.1016/j.ejim.2015.04.013.
https://doi.org/10.1016/j.ejim.2015.04.0...
). Patients with metabolic syndrome and sarcopenia at the same time have a higher risk of severe health events than those with either metabolic syndrome or sarcopenia (5555 Batsis JA, Villareal DT. Sarcopenic Obesity in Older Adults: Aetiology, Epidemiology and Treatment Strategies. Nat Rev Endocrinol. 2018;14(9):513-37. doi: 10.1038/s41574-018-0062-9.
https://doi.org/10.1038/s41574-018-0062-...
,5656 Kobayashi M, Ogawa S, Tayama J, Sagara I, Takeoka A, Bernick P, et al. Intra-Abdominal Fat Accumulation Is an Important Predictor of Metabolic Syndrome in Young Adults. Medicine (Baltimore). 2020;99(37):e22202. doi: 10.1097/MD.0000000000022202.
https://doi.org/10.1097/MD.0000000000022...
).

The mechanisms of muscle weakness associated with metabolic syndrome are not completely clear but are related to inflammation and insulin resistance (5757 Buchmann N, Fielitz J, Spira D, König M, Norman K, Pawelec G, et al. Muscle Mass and Inflammation in Older Adults: Impact of the Metabolic Syndrome. Gerontology. 2022;68(9):989-98. doi: 10.1159/000520096.
https://doi.org/10.1159/000520096...
). Recent evidence indicates a link between loss of muscle mass and insulin resistance and an increased prevalence of metabolic syndrome in adults with sarcopenia (1919 Zhang H, Lin S, Gao T, Zhong F, Cai J, Sun Y, et al. Association between Sarcopenia and Metabolic Syndrome in Middle-Aged and Older Non-Obese Adults: A Systematic Review and Meta-Analysis. Nutrients. 2018;10(3):364. doi: 10.3390/nu10030364.
https://doi.org/10.3390/nu10030364...
,5858 Nishikawa H, Asai A, Fukunishi S, Nishiguchi S, Higuchi K. Metabolic Syndrome and Sarcopenia. Nutrients. 2021;13(10):3519. doi: 10.3390/nu13103519.
https://doi.org/10.3390/nu13103519...
,5959 Kim SH, Jeong JB, Kang J, Ahn DW, Kim JW, Kim BG, et al. Association between Sarcopenia Level and Metabolic Syndrome. PLoS One. 2021;16(3):e0248856. doi: 10.1371/journal.pone.0248856.
https://doi.org/10.1371/journal.pone.024...
). Insulin resistance causes a reduction in glycogen and protein synthesis and an acceleration of protein degradation (5858 Nishikawa H, Asai A, Fukunishi S, Nishiguchi S, Higuchi K. Metabolic Syndrome and Sarcopenia. Nutrients. 2021;13(10):3519. doi: 10.3390/nu13103519.
https://doi.org/10.3390/nu13103519...
). Reduced skeletal muscle mass also contributes to insulin resistance, increases lipolysis, the release of free fatty acids from adipose tissue, and inhibits the growth hormone (GH)-insulin like growth factor 1 (IGF1) axis (6060 Denisenko YK, Kytikova OY, Novgorodtseva TP, Antonyuk MV, Gvozdenko TA, Kantur TA. Lipid-Induced Mechanisms of Metabolic Syndrome. J Obes. 2020;2020:5762395. doi: 10.1155/2020/5762395.
https://doi.org/10.1155/2020/5762395...
,6161 Kalyani RR, Corriere M, Ferrucci L. Age-Related and Disease-Related Muscle Loss: The Effect of Diabetes, Obesity, and Other Diseases. Lancet Diabetes Endocrinol. 2014;2(10):819-29. doi: 10.1016/S2213-8587(14)70034-8.
https://doi.org/10.1016/S2213-8587(14)70...
). Stessman and cols. investigated older adult patients with type 2 diabetes mellitus and found a consistent association between diabetes mellitus and low HGS (2323 Stessman J, Rottenberg Y, Fischer M, Hammerman-Rozenberg A, Jacobs JM. Handgrip Strength in Old and Very Old Adults: Mood, Cognition, Function, and Mortality. J Am Geriatr Soc. 2017;65(3):526-32. doi: 10.1111/jgs.14509.
https://doi.org/10.1111/jgs.14509...
). Previous studies have indicated that insulin resistance and alterations in glucose homeostasis are associated with decaying muscle strength (6262 Atlantis E, Martin SA, Haren MT, Taylor AW, Wittert GA; Members of the Florey Adelaide Male Ageing Study. Inverse Associations between Muscle Mass, Strength, and the Metabolic Syndrome. Metabolism. 2009;58(7):1013-22. doi: 10.1016/j.metabol.2009.02.027.
https://doi.org/10.1016/j.metabol.2009.0...

63 Kaur P, Bansal R, Bhargava B, Mishra S, Gill H, Mithal A. Decreased Handgrip Strength in Patients with Type 2 Diabetes: A Cross-Sectional Study in a Tertiary Care Hospital in North India. Diabetes Metab Syndr. 2021;15(1):325-9. doi: 10.1016/j.dsx.2021.01.007.
https://doi.org/10.1016/j.dsx.2021.01.00...
-6464 Park SW, Goodpaster BH, Lee JS, Kuller LH, Boudreau R, de Rekeneire N, et al.; Health, Aging, and Body Composition Study. Excessive Loss of Skeletal Muscle Mass in Older Adults with Type 2 Diabetes. Diabetes Care. 2009;32(11):1993-7. doi: 10.2337/dc09-0264.
https://doi.org/10.2337/dc09-0264...
). Insulin resistance is a central abnormality in the metabolic syndrome, and muscle mass and strength are strong protective factors independent of insulin resistance and abdominal fat accumulation (6262 Atlantis E, Martin SA, Haren MT, Taylor AW, Wittert GA; Members of the Florey Adelaide Male Ageing Study. Inverse Associations between Muscle Mass, Strength, and the Metabolic Syndrome. Metabolism. 2009;58(7):1013-22. doi: 10.1016/j.metabol.2009.02.027.
https://doi.org/10.1016/j.metabol.2009.0...
,6565 Cheung CL, Nguyen US, Au E, Tan KC, Kung AW. Association of Handgrip Strength with Chronic Diseases and Multimorbidity: A Cross-Sectional Study. Age (Dordr). 2013;35(3):929-41. doi: 10.1007/s11357-012-9385-y.
https://doi.org/10.1007/s11357-012-9385-...
). Therefore, current literature and the qualitative synthesis of this systematic review indicate that improving muscle strength may have wider advantages than previously appreciated regarding the attenuation of the impact of metabolic syndrome in the older adult population.

Older adults have a higher risk of developing sarcopenic obesity, a condition characterized by an important reduction in lean body mass associated with central obesity (5555 Batsis JA, Villareal DT. Sarcopenic Obesity in Older Adults: Aetiology, Epidemiology and Treatment Strategies. Nat Rev Endocrinol. 2018;14(9):513-37. doi: 10.1038/s41574-018-0062-9.
https://doi.org/10.1038/s41574-018-0062-...
,6666 Dominguez LJ, Barbagallo M. The Cardiometabolic Syndrome and Sarcopenic Obesity in Older Persons. J Cardiometab Syndr. 2007;2(3):183-9. doi: 10.1111/j.1559-4564.2007.06673.x.
https://doi.org/10.1111/j.1559-4564.2007...

67 Gao Q, Mei F, Shang Y, Hu K, Chen F, Zhao L, et al. Global Prevalence of Sarcopenic Obesity in Older Adults: A Systematic Review and Meta-Analysis. Clin Nutr. 2021;40(7):4633-41. doi: 10.1016/j.clnu.2021.06.009.
https://doi.org/10.1016/j.clnu.2021.06.0...
-6868 Zamboni M, Mazzali G, Fantin F, Rossi A, Di Francesco V. Sarcopenic Obesity: A New Category of Obesity in the Elderly. Nutr Metab Cardiovasc Dis. 2008;18(5):388-95. doi: 10.1016/j.numecd.2007.10.002.
https://doi.org/10.1016/j.numecd.2007.10...
). Sarcopenic obesity has a greater impact on metabolic diseases and cardiovascular-associated mortality than either sarcopenia or obesity alone (99 Roh E, Choi KM. Health Consequences of Sarcopenic Obesity: A Narrative Review. Front Endocrinol (Lausanne). 2020;11:332. doi: 10.3389/fendo.2020.00332.
https://doi.org/10.3389/fendo.2020.00332...
,6969 Powell-Wiley TM, Poirier P, Burke LE, Després JP, Gordon-Larsen P, Lavie CJ, et al.; American Heart Association Council on Lifestyle and Cardiometabolic Health; Council on Cardiovascular and Stroke Nursing; Council on Clinical Cardiology; Council on Epidemiology and Prevention; and Stroke Council. Obesity and Cardiovascular Disease: A Scientific Statement from the American Heart Association. Circulation. 2021;143(21):e984-e1010. doi: 10.1161/CIR.0000000000000973.
https://doi.org/10.1161/CIR.000000000000...
,7070 Chung JY, Kang HT, Lee DC, Lee HR, Lee YJ. Body Composition and Its Association with Cardiometabolic Risk Factors in the Elderly: A Focus on Sarcopenic Obesity. Arch Gerontol Geriatr. 2013;56(1):270-8. doi: 10.1016/j.archger.2012.09.007.
https://doi.org/10.1016/j.archger.2012.0...
). The lipid overflow from the expanded adipose tissue leads to increased fat deposition in skeletal muscle, which may result in the development of muscle insulin resistance and a decrease in muscle mass (7171 Meex RCR, Blaak EE, van Loon LJC. Lipotoxicity Plays a Key Role in the Development of Both Insulin Resistance and Muscle Atrophy in Patients with Type 2 Diabetes. Obes Rev. 2019;20(9):1205-17. doi: 10.1111/obr.12862.
https://doi.org/10.1111/obr.12862...

72 Cartwright MJ, Tchkonia T, Kirkland JL. Aging in Adipocytes: Potential Impact of Inherent, Depot-Specific Mechanisms. Exp Gerontol. 2007;42(6):463-71. doi: 10.1016/j.exger.2007.03.003.
https://doi.org/10.1016/j.exger.2007.03....
-7373 Cree MG, Newcomer BR, Katsanos CS, Sheffield-Moore M, Chinkes D, Aarsland A, et al. Intramuscular and Liver Triglycerides Are Increased in the Elderly. J Clin Endocrinol Metab. 2004;89(8):3864-71. doi: 10.1210/jc.2003-031986.
https://doi.org/10.1210/jc.2003-031986...
). Moreover, visceral fat significantly increases the risk of insulin resistance, metabolic syndrome, and cardiovascular diseases (6060 Denisenko YK, Kytikova OY, Novgorodtseva TP, Antonyuk MV, Gvozdenko TA, Kantur TA. Lipid-Induced Mechanisms of Metabolic Syndrome. J Obes. 2020;2020:5762395. doi: 10.1155/2020/5762395.
https://doi.org/10.1155/2020/5762395...
,7474 Westphal SA. Obesity, Abdominal Obesity, and Insulin Resistance. Clin Cornerstone. 2008;9(1):23-9; discussion 30-1. doi: 10.1016/s1098-3597(08)60025-3.
https://doi.org/10.1016/s1098-3597(08)60...
). More recent data highlight abdominal obesity, as determined by waist circumference, as a cardiovascular disease risk marker that is independent of BMI (6969 Powell-Wiley TM, Poirier P, Burke LE, Després JP, Gordon-Larsen P, Lavie CJ, et al.; American Heart Association Council on Lifestyle and Cardiometabolic Health; Council on Cardiovascular and Stroke Nursing; Council on Clinical Cardiology; Council on Epidemiology and Prevention; and Stroke Council. Obesity and Cardiovascular Disease: A Scientific Statement from the American Heart Association. Circulation. 2021;143(21):e984-e1010. doi: 10.1161/CIR.0000000000000973.
https://doi.org/10.1161/CIR.000000000000...
). The five studies included in this review that used waist circumference as an outcome found significant correlations between abdominal obesity and low HGS in older adults (3131 Bibiloni MDM, Karam J, Bouzas C, Aparicio-Ugarriza R, Pedrero-Chamizo R, Sureda A, et al. Association between Physical Condition and Body Composition, Nutrient Intake, Sociodemographic Characteristics, and Lifestyle Habits in Older Spanish Adults. Nutrients. 2018;10(11):1608. doi: 10.3390/nu10111608.
https://doi.org/10.3390/nu10111608...
,3333 Lin MH, Chang CY, Lu CH, Wu DM, Kuo FC, Kuo CC, et al. Association between Grip Strength and Anthropometric Characteristics in the Community-Dwelling Elderly Population in Taiwan. PLoS One. 2021;16(12):e0260763. doi: 10.1371/journal.pone.0260763.
https://doi.org/10.1371/journal.pone.026...
,3939 Kim YM, Kim S, Bae J, Kim SH, Won YJ. Association between Relative Hand-Grip Strength and Chronic Cardiometabolic and Musculoskeletal Diseases in Koreans: A Cross-Sectional Study. Arch Gerontol Geriatr. 2021;92:104181. doi: 10.1016/j.archger.2020.104181.
https://doi.org/10.1016/j.archger.2020.1...
,4141 Pérez-Sousa MÁ, Del Pozo-Cruz J, Cano-Gutiérrez CA, Ferrebuz AJ, Sandoval-Cuellar C, Izquierdo M, et al. Glucose Levels as a Mediator of the Detrimental Effect of Abdominal Obesity on Relative Handgrip Strength in Older Adults. J Clin Med. 2020;9(8):2323. doi: 10.3390/jcm9082323.
https://doi.org/10.3390/jcm9082323...
,4242 Sayer AA, Syddall HE, Dennison EM, Martin HJ, Phillips DI, Cooper C, et al.; Hertfordshire Cohort. Grip Strength and the Metabolic Syndrome: Findings from the Hertfordshire Cohort Study. QJM. 2007;100(11):707-13. doi: 10.1093/qjmed/hcm095.
https://doi.org/10.1093/qjmed/hcm095...
). Finally, reduced HGS was also associated with dyslipidemia in three studies included; low HGS was associated with hypertriglyceridemia (3737 Kawamoto R, Ninomiya D, Kasai Y, Kusunoki T, Ohtsuka N, Kumagi T, et al. Handgrip Strength Is Associated with Metabolic Syndrome among Middle-Aged and Elderly Community-Dwelling Persons. Clin Exp Hypertens. 2016;38(2):245-51. doi: 10.3109/10641963.2015.1081232.
https://doi.org/10.3109/10641963.2015.10...
,4242 Sayer AA, Syddall HE, Dennison EM, Martin HJ, Phillips DI, Cooper C, et al.; Hertfordshire Cohort. Grip Strength and the Metabolic Syndrome: Findings from the Hertfordshire Cohort Study. QJM. 2007;100(11):707-13. doi: 10.1093/qjmed/hcm095.
https://doi.org/10.1093/qjmed/hcm095...
) and with low HDL levels (3737 Kawamoto R, Ninomiya D, Kasai Y, Kusunoki T, Ohtsuka N, Kumagi T, et al. Handgrip Strength Is Associated with Metabolic Syndrome among Middle-Aged and Elderly Community-Dwelling Persons. Clin Exp Hypertens. 2016;38(2):245-51. doi: 10.3109/10641963.2015.1081232.
https://doi.org/10.3109/10641963.2015.10...
,3939 Kim YM, Kim S, Bae J, Kim SH, Won YJ. Association between Relative Hand-Grip Strength and Chronic Cardiometabolic and Musculoskeletal Diseases in Koreans: A Cross-Sectional Study. Arch Gerontol Geriatr. 2021;92:104181. doi: 10.1016/j.archger.2020.104181.
https://doi.org/10.1016/j.archger.2020.1...
). These results indicate that HGS may be a useful tool to detect sarcopenic obesity and metabolic syndrome in older adults (7575 Bohannon RW. Grip Strength: An Indispensable Biomarker for Older Adults. Grip Strength: An Indispensable Biomarker for Older Adults. Clin Interv Aging. 2019;14:1681-91. doi: 10.2147/CIA.S194543.
https://doi.org/10.2147/CIA.S194543...
).

The strength of this systematic review is in the broad search strategy adopted, which was conducted in several different databases. The main limitation was not conducting a meta-analysis owing to the heterogeneity of metabolic syndrome outcomes and data analysis of the included studies. However, the qualitative synthesis of the included studies allowed us to conclude that most studies found a clear correlation between low HGS and metabolic syndrome or some of its components, especially abdominal fat and insulin resistance.

In conclusion, most studies examined in this systematic review revealed significant correlations between reduced HGS and metabolic syndrome or some of its components in older adults, especially abdominal obesity and insulin resistance. These results corroborate previous findings that below-average HGS is a proper indicator of health outcomes in the older adult population and supports the use of HGS in clinical settings as a predictor of adverse outcomes related to metabolic syndrome in older people.

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SUPPLEMENTARY MATERIAL:

1) The full mapping terms for the search strategy divided by sectors.

For the population:

DECS terms: (Sarcopenia OR Sarcopenias OR "Força Muscular" OR "Fuerza Muscular" OR "Inibição Muscular Artrogênica") AND (Mãos OR mão OR Mano) OR ("Fuerza de la Mano" OR "Força da Mão" OR "Aperto de Mão" OR Empunhadura) AND (Idoso OR Idosos OR Idosas OR Idosa OR "Pessoa de Idade" OR "Pessoas de Idade") AND (Idoso OR Idosos OR Idosas OR Idosa OR "Pessoa de Idade" OR "Pessoas de Idade").

MESH terms: (Sarcopenia) OR (Sarcopenia) OR (Muscle Strength) OR (Strength, Muscle) OR (Muscle Inhibition) OR (Muscle Inhibitions) AND (Hand) OR (hands) / (Hand Strength) OR (Hand Strengths) OR (Strength, Hand) OR (Strengths, Hand) OR (Grip) OR (Grips) OR (Grasp) OR (Grasps) AND (Aged OR Elderly OR senescence OR aging).

For the interventions:

DECS terms: Dinamômetro de Força Muscular OR "Dinamómetro de Fuerza Muscular".

MESH terms: (Muscle Strength Dynamometer) OR (Dynamometer, Muscle Strength) OR (Dynamometers, Muscle Strength) OR (Muscle Strength Dynamometers) OR (Dynamometer) OR (Dynamometers).

For the outcomes:

DECS terms: "Síndrome Metabólica" OR "Síndrome Metabólico" / (Síndrome Metabólica) OR (Síndrome Metabólico).

MESH terms: "Metabolic Syndrome" OR "Metabolic Syndromes" OR "Syndrome, Metabolic" OR "Syndromes, Metabolic" OR "Metabolic Syndrome X" OR "Insulin Resistance Syndrome X" OR "Syndrome X, Metabolic" OR "Syndrome X, Insulin Resistance" OR "Metabolic X Syndrome" OR "Syndrome, Metabolic X" OR "X Syndrome, Metabolic" OR "Dysmetabolic Syndrome X" OR "Syndrome X, Dysmetabolic" OR "Reaven Syndrome X" OR "Syndrome X, Reaven" OR "Metabolic Cardiovascular Syndrome" OR "Cardiovascular Syndrome, Metabolic" OR "Cardiovascular Syndromes, Metabolic" OR "Syndrome, Metabolic Cardiovascular" / (Metabolic Syndrome) OR (Metabolic Syndromes) OR (Syndrome, Metabolic) OR (Syndromes, Metabolic) OR (Metabolic Syndrome X) OR (Insulin Resistance Syndrome X) OR (Syndrome X, Metabolic) OR (Syndrome X, Insulin Resistance) OR (Metabolic X Syndrome) OR (Syndrome, Metabolic X) OR (X Syndrome, Metabolic) OR (Dysmetabolic Syndrome X) OR (Syndrome X, Dysmetabolic) OR (Reaven Syndrome X) OR (Syndrome X, Reaven) OR (Metabolic Cardiovascular Syndrome) OR (Cardiovascular Syndrome, Metabolic) OR (Cardiovascular Syndromes, Metabolic) OR (Syndrome, Metabolic Cardiovascular) ((Metabolic Syndrome) OR (Metabolic Syndromes) OR (Syndrome, Metabolic) OR (Syndromes, Metabolic) OR (Metabolic Syndrome X) OR (Insulin Resistance Syndrome X) OR (Syndrome X, Metabolic) OR (Syndrome X, Insulin Resistance) OR (Metabolic X Syndrome) OR (Syndrome, Metabolic X) OR (X Syndrome, Metabolic) OR (Dysmetabolic Syndrome X) OR (Syndrome X, Dysmetabolic) OR (Reaven Syndrome X) OR (Syndrome X, Reaven) OR (Metabolic Cardiovascular Syndrome) OR (Cardiovascular Syndrome, Metabolic) OR (Cardiovascular Syndromes, Metabolic) OR (Syndrome, Metabolic Cardiovascular) AND (english[Filter] OR portuguese[Filter] OR spanish[Filter])) AND ((((Sarcopenia) OR (Sarcopenia) OR (Muscle Strength) OR (Strength, Muscle) OR (Muscle Inhibition) OR (Muscle Inhibitions)) AND ((Hand) OR (hands))) AND ((Muscle Strength Dynamometer) OR (Dynamometer, Muscle Strength) OR (Dynamometers, Muscle Strength) OR (Muscle Strength Dynamometers) OR (Dynamometer) OR (Dynamometers))) ((((Hand Strength) OR (Hand Strengths) OR (Strength, Hand) OR (Strengths, Hand) OR (Grip) OR (Grips) OR (Grasp) OR (Grasps)) AND (Aged OR Elderly OR senescence OR aging)) AND ((Muscle Strength Dynamometer) OR (Dynamometer, Muscle Strength) OR (Dynamometers, Muscle Strength) OR (Muscle Strength Dynamometers) OR (Dynamometer) OR (Dynamometers)) AND (english[Filter] OR portuguese[Filter] OR spanish[Filter])) AND ((Metabolic Syndrome) OR (Metabolic Syndromes) OR (Syndrome, Metabolic) OR (Syndromes, Metabolic) OR (Metabolic Syndrome X) OR (Insulin Resistance Syndrome X) OR (Syndrome X, Metabolic) OR (Syndrome X, Insulin Resistance) OR (Metabolic X Syndrome) OR (Syndrome, Metabolic X) OR (X Syndrome, Metabolic) OR (Dysmetabolic Syndrome X) OR (Syndrome X, Dysmetabolic) OR (Reaven Syndrome X) OR (Syndrome X, Reaven) OR (Metabolic Cardiovascular Syndrome) OR (Cardiovascular Syndrome, Metabolic) OR (Cardiovascular Syndromes, Metabolic) OR (Syndrome, Metabolic Cardiovascular) AND (english[Filter] OR portuguese[Filter] OR spanish[Filter])).

2) Critical appraisal tool to assess the quality of cross-sectional studies (AXIS)

Reference: AXIS, Appraisal Tool for Cross-Sectional Studies (Downes et al., 2016).

Table 1 Number of articles attending criteria 1. Were the aims/objectives of the study clear? 2. Was the study design appropriate for the stated aim(s)? 3. Was the sample size justified? 4. Was the target/reference population clearly defined? (Is it clear who the research was about?) 5. Was the sample frame taken from an appropriate population base so that it closely represented the target/reference population under investigation? 6. Was the selection process likely to select subjects/participants that were representative of the target/reference population under investigation? 7. Were measures undertaken to address and categorise non-responders? 8. Were the risk factor and outcome variables measured appropriate to the aims of the study? 9. Were the risk factor and outcome variables measured correctly using instruments/measurements that had been trialled, piloted or published previously? 10. Is it clear what was used to determined statistical significance and/or precision estimates? (eg, p values, CIs) 11. Were the methods (including statistical methods) sufficiently described to enable them to be repeated? 12. Were the basic data adequately described? 13. Does the response rate raise concerns about non-response bias? 14. If appropriate, was information about non-responders described? 15. Were the results internally consistent? 16. 1Were the results for the analyses described in the methods, presented? 17. Were the authors' discussions and conclusions justified by the results? 18. Were the limitations of the study discussed? 19. Were there any funding sources or conflicts of interest that may affect the authors' interpretation of the results? 20. Was ethical approval or consent of participants attained?
Table 2
AXIS score of the articles included in the qualitative synthesis
3) Cohen's Kappa statistics

Results of the inter-rater evaluation of the first screening, comparing the agreement between the two pairs of raters.

% of agreement: 87.47913188647746%

Cohen's k: 0.48399434891974746

Moderate agreement

Publication Dates

  • Publication in this collection
    07 June 2024
  • Date of issue
    2024

History

  • Received
    01 Jan 2023
  • Accepted
    07 Feb 2024
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