E. Association between low handgrip strength and cardiovascular
VI. Conclusion
We demonstrated that the relative HGS is a novel biomarker for assessing the risk of CVD, and is superior to other HGS indices such as dominant or absolute HGS. We also identified a relative HGS value of 2.52 in men and 1.55 in women as the optimal cut-off point to predict CVD in Korean adults age 45 years and older. Additionally, after controlling for socioeconomic and health-related variables, we reported a strong inverse association between weak HGS, as determined by the optimal cut off derived from this study, and CVD. Our findings suggest that the measurement of HGS may add clinical utility over existing risk prediction scores. Handgrip strength is easily measured and highly reproducible in clinical practice and risk screening settings where blood sampling is not possible such as in community settings or in low and middle income countries. Especially in the elderly population, it is necessary to pay attention to their grip strength against their weight, and additional prospective or interventional studies are required to confirm the causal relationship between HGS and CVD, and to determine whether interventions in subjects with low relative HGS are effective in preventing adverse health outcomes.
74
Reference
1. Aoyama T, Asaka M, Ishijima T, Kawano H, Cao ZB, Sakamoto S, Tabata I, Higuchi M: Association between muscular strength and metabolic risk in Japanese women, but not in men. J Physiol Anthropol 30: 133-139, 2011 2. Araki A, Ito H: Diabetes mellitus and geriatric syndromes. Geriatr Gerontol
Int 9: 105-114, 2009
3. Argiles JM, Campos N, Lopez-Pedrosa JM, Rueda R, Rodriguez-Manas L:
Skeletal Muscle Regulates Metabolism via Interorgan Crosstalk: Roles in Health and Disease. J Am Med Dir Assoc 17: 789-796, 2016
4. Artero EG, Lee DC, Lavie CJ, Espana-Romero V, Sui X, Church TS, Blair SN:
Effects of muscular strength on cardiovascular risk factors and prognosis.
J Cardiopulm Rehabil Prev 32: 351-358, 2012
5. Artero EG, Lee DC, Ruiz JR, Sui X, Ortega FB, Church TS, Lavie CJ, Castillo MJ, Blair SN: A prospective study of muscular strength and all-cause mortality in men with hypertension. J Am Coll Cardiol 57: 1831-1837, 2011 6. Batsis JA, Mackenzie TA, Lopez-Jimenez F, Bartels SJ: Sarcopenia, sarcopenic obesity, and functional impairments in older adults: National Health and Nutrition Examination Surveys 1999-2004. Nutr Res 35: 1031-1039, 2015
7. Benson AC, Torode ME, Singh MA: Muscular strength and cardiorespiratory fitness is associated with higher insulin sensitivity in children and adolescents. Int J Pediatr Obes 1: 222-231, 2006
8. Byung-Taek Oh Y-SH, Jun-Young Lee, Sang-Kyun Park, Seung-Wan Hong, Young-Sung Suh, Dae-Hyun Kim: Factors Related with Hand Grip Strength in Korean Elderly Korean J Clin Geri 18: 22-29, 2017
9. Celis-Morales CA, Welsh P, Lyall DM, Steell L, Petermann F, Anderson J, Iliodromiti S, Sillars A, Graham N, Mackay DF, Pell JP, Gill JMR, Sattar N, Gray SR: Associations of grip strength with cardiovascular, respiratory, and cancer outcomes and all cause mortality: prospective cohort study of half a million UK Biobank participants. BMJ 361: k1651, 2018
75
10. Chainani V, Shaharyar S, Dave K, Choksi V, Ravindranathan S, Hanno R, Jamal O, Abdo A, Abi Rafeh N: Objective measures of the frailty syndrome (hand grip strength and gait speed) and cardiovascular mortality: A systematic review. Int J Cardiol 215: 487-493, 2016
11. Chen LK, Lee WJ, Peng LN, Liu LK, Arai H, Akishita M, Asian Working Group for S: Recent Advances in Sarcopenia Research in Asia: 2016 Update From the Asian Working Group for Sarcopenia. J Am Med Dir Assoc 17: 767 e761-767, 2016
12. Chen LK, Liu LK, Woo J, Assantachai P, Auyeung TW, Bahyah KS, Chou MY, Chen LY, Hsu PS, Krairit O, Lee JS, Lee WJ, Lee Y, Liang CK, Limpawattana P, Lin CS, Peng LN, Satake S, Suzuki T, Won CW, Wu CH, Wu SN, Zhang T, Zeng P, Akishita M, Arai H: Sarcopenia in Asia: consensus report of the Asian Working Group for Sarcopenia. J Am Med Dir Assoc 15: 95-101, 2014
13. Chen PJ, Lin MH, Peng LN, Liu CL, Chang CW, Lin YT, Chen LK: Predicting cause-specific mortality of older men living in the Veterans home by handgrip strength and walking speed: a 3-year, prospective cohort study in Taiwan. J Am Med Dir Assoc 13: 517-521, 2012
14. Choi J, Ahn A, Kim S, Won CW: Global Prevalence of Physical Frailty by Fried's Criteria in Community-Dwelling Elderly With National Population-Based Surveys. J Am Med Dir Assoc 16: 548-550, 2015
15. Cooper R, Kuh D, Hardy R, Mortality Review G, Falcon, Teams HAS:
Objectively measured physical capability levels and mortality: systematic review and meta-analysis. BMJ 341: c4467, 2010
16. Corti MC, Guralnik JM, Salive ME, Harris T, Ferrucci L, Glynn RJ, Havlik RJ:
Clarifying the direct relation between total cholesterol levels and death from coronary heart disease in older persons. Ann Intern Med 126: 753-760, 1997
17. Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, Martin FC, Michel JP, Rolland Y, Schneider SM, Topinkova E, Vandewoude M, Zamboni M, European Working Group on Sarcopenia in Older P:
Sarcopenia: European consensus on definition and diagnosis: Report of
76
the European Working Group on Sarcopenia in Older People. Age Ageing 39: 412-423, 2010a
18. Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyere O, Cederholm T, Cooper C, Landi F, Rolland Y, Sayer AA, Schneider SM, Sieber CC, Topinkova E, Vandewoude M, Visser M, Zamboni M, Writing Group for the European Working Group on Sarcopenia in Older P, the Extended Group for E:
Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing 48: 16-31, 2019
19. Cruz-Jentoft AJ, Landi F: Sarcopenia. Clin Med (Lond) 14: 183-186, 2014 20. Cruz-Jentoft AJ, Landi F, Schneider SM, Zuniga C, Arai H, Boirie Y, Chen LK,
Fielding RA, Martin FC, Michel JP, Sieber C, Stout JR, Studenski SA, Vellas B, Woo J, Zamboni M, Cederholm T: Prevalence of and interventions for sarcopenia in ageing adults: a systematic review. Report of the International Sarcopenia Initiative (EWGSOP and IWGS). Age Ageing 43:
748-759, 2014
21. Cruz-Jentoft AJ, Landi F, Topinkova E, Michel JP: Understanding sarcopenia as a geriatric syndrome. Curr Opin Clin Nutr Metab Care 13: 1-7, 2010b 22. Dodds RM, Syddall HE, Cooper R, Kuh D, Cooper C, Sayer AA: Global
variation in grip strength: a systematic review and meta-analysis of normative data. Age Ageing 45: 209-216, 2016
23. Dong R, Wang X, Guo Q, Wang J, Zhang W, Shen S, Han P, Ma Y, Kang L, Wang M, Fu L, Jia L, Wang L, Niu K: Clinical Relevance of Different Handgrip Strength Indexes and Mobility Limitation in the Elderly Adults. J Gerontol A Biol Sci Med Sci 71: 96-102, 2016
24. Fowles J, Roy J, Clarke J, Dogra S: Are the fittest Canadian adults the healthiest? Health Rep 25: 13-18, 2014
25. Frederiksen H, Gaist D, Petersen HC, Hjelmborg J, McGue M, Vaupel JW, Christensen K: Hand grip strength: a phenotype suitable for identifying genetic variants affecting mid- and late-life physical functioning. Genet Epidemiol 23: 110-122, 2002
26. Fried LP, Tangen CM, Walston J, Newman AB, Hirsch C, Gottdiener J, Seeman T, Tracy R, Kop WJ, Burke G, McBurnie MA, Cardiovascular Health
77
Study Collaborative Research G: Frailty in older adults: evidence for a phenotype. J Gerontol A Biol Sci Med Sci 56: M146-156, 2001
27. Frontera WR, Ochala J: Skeletal muscle: a brief review of structure and function. Calcif Tissue Int 96: 183-195, 2015
28. Glasgow A, Stone TM, Kingsley JD: Resistance Exercise Training on Disease Impact, Pain Catastrophizing and Autonomic Modulation in Women with Fibromyalgia. Int J Exerc Sci 10: 1184-1195, 2017
29. Grimby G, Saltin B: The ageing muscle. Clin Physiol 3: 209-218, 1983 30. Group DS: Age- and sex-specific prevalences of diabetes and impaired
glucose regulation in 13 European cohorts. Diabetes Care 26: 61-69, 2003 31. Gubelmann C, Vollenweider P, Marques-Vidal P: Association of grip strength with cardiovascular risk markers. Eur J Prev Cardiol 24: 514-521, 2017a
32. Gubelmann C, Vollenweider P, Marques-Vidal P: No association between grip strength and cardiovascular risk: The CoLaus population-based study.
Int J Cardiol 236: 478-482, 2017b
33. Hamer M, Stamatakis E: Screen-based sedentary behavior, physical activity, and muscle strength in the English longitudinal study of ageing. PLoS One 8: e66222, 2013
34. Hulsmann M, Quittan M, Berger R, Crevenna R, Springer C, Nuhr M, Mortl D, Moser P, Pacher R: Muscle strength as a predictor of long-term survival in severe congestive heart failure. Eur J Heart Fail 6: 101-107, 2004 35. Institute KL: User Guide for KLoSA. . 2007
36. Izawa KP, Watanabe S, Osada N, Kasahara Y, Yokoyama H, Hiraki K, Morio Y, Yoshioka S, Oka K, Omiya K: Handgrip strength as a predictor of prognosis in Japanese patients with congestive heart failure. Eur J Cardiovasc Prev Rehabil 16: 21-27, 2009
37. Jackson AW, Lee DC, Sui X, Morrow JR, Jr., Church TS, Maslow AL, Blair SN:
Muscular strength is inversely related to prevalence and incidence of obesity in adult men. Obesity (Silver Spring) 18: 1988-1995, 2010
38. Janssen I, Heymsfield SB, Wang ZM, Ross R: Skeletal muscle mass and distribution in 468 men and women aged 18-88 yr. J Appl Physiol (1985)
78 89: 81-88, 2000
39. Keevil VL, Khaw KT: Overadjustment in regression analyses: considerations when evaluating relationships between body mass index, muscle strength, and body size. J Gerontol A Biol Sci Med Sci 69: 616-617, 2014
40. Kelley GA, Kelley KS: Progressive resistance exercise and resting blood pressure : A meta-analysis of randomized controlled trials. Hypertension 35: 838-843, 2000
41. Kim CR, Jeon YJ, Jeong T: Risk factors associated with low handgrip strength in the older Korean population. PLoS One 14: e0214612, 2019 42. Kim CR, Jeon YJ, Kim MC, Jeong T, Koo WR: Reference values for hand grip
strength in the South Korean population. PLoS One 13: e0195485, 2018 43. Kim KM, Jang HC, Lim S: Differences among skeletal muscle mass indices
derived from height-, weight-, and body mass index-adjusted models in assessing sarcopenia. Korean J Intern Med 31: 643-650, 2016
44. Kishimoto H, Hata J, Ninomiya T, Nemeth H, Hirakawa Y, Yoshida D, Kumagai S, Kitazono T, Kiyohara Y: Midlife and late-life handgrip strength and risk of cause-specific death in a general Japanese population: the Hisayama Study. J Epidemiol Community Health 68: 663-668, 2014 45. Knottnerus JA, Metsemakers J, Hoppener P, Limonard C: Chronic illness in
the community and the concept of 'social prevalence'. Fam Pract 9: 15-21, 1992
46. Kronmal RA, Cain KC, Ye Z, Omenn GS: Total serum cholesterol levels and mortality risk as a function of age. A report based on the Framingham data. Arch Intern Med 153: 1065-1073, 1993
47. Lauretani F, Russo CR, Bandinelli S, Bartali B, Cavazzini C, Di Iorio A, Corsi AM, Rantanen T, Guralnik JM, Ferrucci L: Age-associated changes in skeletal muscles and their effect on mobility: an operational diagnosis of sarcopenia. J Appl Physiol (1985) 95: 1851-1860, 2003
48. Lawman HG, Troiano RP, Perna FM, Wang CY, Fryar CD, Ogden CL:
Associations of Relative Handgrip Strength and Cardiovascular Disease Biomarkers in U.S. Adults, 2011-2012. Am J Prev Med 50: 677-683, 2016 49. Lee MR, Jung SM, Kim HS, Kim YB: Association of muscle strength with
79
cardiovascular risk in Korean adults: Findings from the Korea National Health and Nutrition Examination Survey (KNHANES) VI to VII (2014-2016).
Medicine (Baltimore) 97: e13240, 2018
50. Lee SW, Kim HC, Lee HS, Suh I: Thirty-Year Trends in Mortality from Cerebrovascular Diseases in Korea. Korean Circ J 46: 507-514, 2016a 51. Lee WJ, Peng LN, Chiou ST, Chen LK: Relative Handgrip Strength Is a Simple
Indicator of Cardiometabolic Risk among Middle-Aged and Older People:
A Nationwide Population-Based Study in Taiwan. PLoS One 11: e0160876, 2016b
52. Leening MJ, Ferket BS, Steyerberg EW, Kavousi M, Deckers JW, Nieboer D, Heeringa J, Portegies ML, Hofman A, Ikram MA, Hunink MG, Franco OH, Stricker BH, Witteman JC, Roos-Hesselink JW: Sex differences in lifetime risk and first manifestation of cardiovascular disease: prospective population based cohort study. BMJ 349: g5992, 2014
53. Leong DP, Teo KK, Rangarajan S, Lopez-Jaramillo P, Avezum A, Jr., Orlandini A, Seron P, Ahmed SH, Rosengren A, Kelishadi R, Rahman O, Swaminathan S, Iqbal R, Gupta R, Lear SA, Oguz A, Yusoff K, Zatonska K, Chifamba J, Igumbor E, Mohan V, Anjana RM, Gu H, Li W, Yusuf S, Prospective Urban Rural Epidemiology Study i: Prognostic value of grip strength: findings from the Prospective Urban Rural Epidemiology (PURE) study. Lancet 386:
266-273, 2015
54. Li D, Guo G, Xia L, Yang X, Zhang B, Liu F, Ma J, Hu Z, Li Y, Li W, Jiang J, Gaisano H, Shan G, He Y: Relative Handgrip Strength Is Inversely Associated with Metabolic Profile and Metabolic Disease in the General Population in China. Front Physiol 9: 59, 2018
55. Ling CH, Taekema D, de Craen AJ, Gussekloo J, Westendorp RG, Maier AB:
Handgrip strength and mortality in the oldest old population: the Leiden 85-plus study. CMAJ 182: 429-435, 2010
56. Liu LK, Lee WJ, Chen LY, Hwang AC, Lin MH, Peng LN, Chen LK: Sarcopenia, and its association with cardiometabolic and functional characteristics in Taiwan: results from I-Lan Longitudinal Aging Study. Geriatr Gerontol Int 14 Suppl 1: 36-45, 2014
80
57. Lopez-Jaramillo P, Cohen DD, Gomez-Arbelaez D, Bosch J, Dyal L, Yusuf S, Gerstein HC, Investigators OT: Association of handgrip strength to cardiovascular mortality in pre-diabetic and diabetic patients: a subanalysis of the ORIGIN trial. Int J Cardiol 174: 458-461, 2014
58. Mainous AG, 3rd, Tanner RJ, Anton SD, Jo A: Low Grip Strength and Prediabetes in Normal-Weight Adults. J Am Board Fam Med 29: 280-282, 2016
59. Masel MC, Ostir GV, Ottenbacher KJ: Frailty, mortality, and health-related quality of life in older Mexican Americans. J Am Geriatr Soc 58: 2149-2153, 2010
60. Maslow AL, Sui X, Colabianchi N, Hussey J, Blair SN: Muscular strength and incident hypertension in normotensive and prehypertensive men. Med Sci Sports Exerc 42: 288-295, 2010
61. Mason C, Brien SE, Craig CL, Gauvin L, Katzmarzyk PT: Musculoskeletal fitness and weight gain in Canada. Med Sci Sports Exerc 39: 38-43, 2007 62. McDermott MM, Liu K, Tian L, Guralnik JM, Criqui MH, Liao Y, Ferrucci L:
Calf muscle characteristics, strength measures, and mortality in peripheral arterial disease: a longitudinal study. J Am Coll Cardiol 59: 1159-1167, 2012 63. Metter EJ, Lynch N, Conwit R, Lindle R, Tobin J, Hurley B: Muscle quality and age: cross-sectional and longitudinal comparisons. J Gerontol A Biol Sci Med Sci 54: B207-218, 1999
64. Minneci C, Mello AM, Mossello E, Baldasseroni S, Macchi L, Cipolletti S, Marchionni N, Di Bari M: Comparative study of four physical performance measures as predictors of death, incident disability, and falls in unselected older persons: the insufficienza Cardiaca negli Anziani Residenti a Dicomano Study. J Am Geriatr Soc 63: 136-141, 2015
65. Morley JE, Abbatecola AM, Argiles JM, Baracos V, Bauer J, Bhasin S, Cederholm T, Coats AJ, Cummings SR, Evans WJ, Fearon K, Ferrucci L, Fielding RA, Guralnik JM, Harris TB, Inui A, Kalantar-Zadeh K, Kirwan BA, Mantovani G, Muscaritoli M, Newman AB, Rossi-Fanelli F, Rosano GM, Roubenoff R, Schambelan M, Sokol GH, Storer TW, Vellas B, von Haehling S, Yeh SS, Anker SD, Society on Sarcopenia C, Wasting Disorders Trialist W:
81
Sarcopenia with limited mobility: an international consensus. J Am Med Dir Assoc 12: 403-409, 2011
66. Nair KS: Aging muscle. Am J Clin Nutr 81: 953-963, 2005
67. Newman AB, Haggerty CL, Goodpaster B, Harris T, Kritchevsky S, Nevitt M, Miles TP, Visser M, Health A, Body Composition Research G: Strength and muscle quality in a well-functioning cohort of older adults: the Health, Aging and Body Composition Study. J Am Geriatr Soc 51: 323-330, 2003 68. Newman AB, Simonsick EM, Naydeck BL, Boudreau RM, Kritchevsky SB,
Nevitt MC, Pahor M, Satterfield S, Brach JS, Studenski SA, Harris TB:
Association of long-distance corridor walk performance with mortality, cardiovascular disease, mobility limitation, and disability. JAMA 295: 2018-2026, 2006
69. Nofuji Y, Shinkai S, Taniguchi Y, Amano H, Nishi M, Murayama H, Fujiwara Y, Suzuki T: Associations of Walking Speed, Grip Strength, and Standing Balance With Total and Cause-Specific Mortality in a General Population of Japanese Elders. J Am Med Dir Assoc 17: 184 e181-187, 2016
70. Ntuk UE, Celis-Morales CA, Mackay DF, Sattar N, Pell JP, Gill JMR:
Association between grip strength and diabetes prevalence in black, South-Asian, and white European ethnic groups: a cross-sectional analysis of 418 656 participants in the UK Biobank study. Diabet Med 34: 1120-1128, 2017
71. Ong HL, Abdin E, Chua BY, Zhang Y, Seow E, Vaingankar JA, Chong SA, Subramaniam M: Hand-grip strength among older adults in Singapore: a comparison with international norms and associative factors. BMC Geriatr 17: 176, 2017
72. Pescatello LS, Franklin BA, Fagard R, Farquhar WB, Kelley GA, Ray CA, American College of Sports M: American College of Sports Medicine position stand. Exercise and hypertension. Med Sci Sports Exerc 36: 533-553, 2004
73. Rantanen T, Masaki K, Foley D, Izmirlian G, White L, Guralnik JM: Grip strength changes over 27 yr in Japanese-American men. J Appl Physiol (1985) 85: 2047-2053, 1998
82
74. Reginster JY, Cooper C, Rizzoli R, Kanis JA, Appelboom G, Bautmans I, Bischoff-Ferrari HA, Boers M, Brandi ML, Bruyere O, Cherubini A, Flamion B, Fielding RA, Gasparik AI, Van Loon L, McCloskey E, Mitlak BH, Pilotto A, Reiter-Niesert S, Rolland Y, Tsouderos Y, Visser M, Cruz-Jentoft AJ:
Recommendations for the conduct of clinical trials for drugs to treat or prevent sarcopenia. Aging Clin Exp Res 28: 47-58, 2016
75. Robinson SM, Jameson KA, Batelaan SF, Martin HJ, Syddall HE, Dennison EM, Cooper C, Sayer AA, Hertfordshire Cohort Study G: Diet and its relationship with grip strength in community-dwelling older men and women: the Hertfordshire cohort study. J Am Geriatr Soc 56: 84-90, 2008 76. Rosenberg IH: Sarcopenia: origins and clinical relevance. J Nutr 127:
990S-991S, 1997
77. Rosenberg IH: Sarcopenia: origins and clinical relevance. Clin Geriatr Med 27: 337-339, 2011
78. Rosero-Bixby L, Dow WH: Predicting mortality with biomarkers: a population-based prospective cohort study for elderly Costa Ricans. Popul Health Metr 10: 11, 2012
79. Ruiz JR, Sui X, Lobelo F, Morrow JR, Jr., Jackson AW, Sjostrom M, Blair SN:
Association between muscular strength and mortality in men: prospective cohort study. BMJ 337: a439, 2008
80. Sanford A, Morley JE: Are the new guidelines for cholesterol and hypertension age friendly? J Am Med Dir Assoc 15: 373-375, 2014
81. Sayer AA, Syddall HE, Dennison EM, Martin HJ, Phillips DI, Cooper C, Byrne CD, Hertfordshire C: Grip strength and the metabolic syndrome: findings from the Hertfordshire Cohort Study. QJM 100: 707-713, 2007
82. Schatz IJ, Masaki K, Yano K, Chen R, Rodriguez BL, Curb JD: Cholesterol and all-cause mortality in elderly people from the Honolulu Heart Program:
a cohort study. Lancet 358: 351-355, 2001
83. Schisterman EF, Faraggi D, Reiser B, Hu J: Youden Index and the optimal threshold for markers with mass at zero. Stat Med 27: 297-315, 2008 84. Strand BH, Cooper R, Bergland A, Jorgensen L, Schirmer H, Skirbekk V,
Emaus N: The association of grip strength from midlife onwards with
all-83
cause and cause-specific mortality over 17 years of follow-up in the Tromso Study. J Epidemiol Community Health 70: 1214-1221, 2016 85. Studenski SA, Peters KW, Alley DE, Cawthon PM, McLean RR, Harris TB,
Ferrucci L, Guralnik JM, Fragala MS, Kenny AM, Kiel DP, Kritchevsky SB, Shardell MD, Dam TT, Vassileva MT: The FNIH sarcopenia project: rationale, study description, conference recommendations, and final estimates. J Gerontol A Biol Sci Med Sci 69: 547-558, 2014
86. UnitedNations. World Population Ageing 2015 2015
87. Vellas B, Fielding RA, Bens C, Bernabei R, Cawthon PM, Cederholm T, Cruz-Jentoft AJ, Del Signore S, Donahue S, Morley J, Pahor M, Reginster JY, Rodriguez Manas L, Rolland Y, Roubenoff R, Sinclair A, Cesari M:
Implications of ICD-10 for Sarcopenia Clinical Practice and Clinical Trials:
Report by the International Conference on Frailty and Sarcopenia Research Task Force. J Frailty Aging 7: 2-9, 2018
88. Volaklis KA, Halle M, Koenig W, Oberhoffer R, Grill E, Peters A, Strasser B, Heier M, Emeny R, Schulz H, Ladwig KH, Meisinger C, Thorand B:
Association between muscular strength and inflammatory markers among elderly persons with cardiac disease: results from the KORA-Age study. Clin Res Cardiol 104: 982-989, 2015
89. Wang CP, Lorenzo C, Espinoza SE: Frailty Attenuates the Impact of Metformin on Reducing Mortality in Older Adults with Type 2 Diabetes. J Endocrinol Diabetes Obes 2, 2014
90. WHO (2016). Technical Package for Cardiovascular Disease Management in Primary Health Care. In Geneva, Switzerland: World Health Organization.
91. Wijndaele K, Duvigneaud N, Matton L, Duquet W, Thomis M, Beunen G, Lefevre J, Philippaerts RM: Muscular strength, aerobic fitness, and metabolic syndrome risk in Flemish adults. Med Sci Sports Exerc 39: 233-240, 2007
92. Willems SM, Wright DJ, Day FR, Trajanoska K, Joshi PK, Morris JA, Matteini AM, Garton FC, Grarup N, Oskolkov N, Thalamuthu A, Mangino M, Liu J, Demirkan A, Lek M, Xu L, Wang G, Oldmeadow C, Gaulton KJ, Lotta LA, Miyamoto-Mikami E, Rivas MA, White T, Loh PR, Aadahl M, Amin N, Attia
84
JR, Austin K, Benyamin B, Brage S, Cheng YC, Cieszczyk P, Derave W, Eriksson KF, Eynon N, Linneberg A, Lucia A, Massidda M, Mitchell BD, Miyachi M, Murakami H, Padmanabhan S, Pandey A, Papadimitriou I, Rajpal DK, Sale C, Schnurr TM, Sessa F, Shrine N, Tobin MD, Varley I, Wain LV, Wray NR, Lindgren CM, MacArthur DG, Waterworth DM, McCarthy MI, Pedersen O, Khaw KT, Kiel DP, Consortium GA-ToF, Pitsiladis Y, Fuku N, Franks PW, North KN, van Duijn CM, Mather KA, Hansen T, Hansson O, Spector T, Murabito JM, Richards JB, Rivadeneira F, Langenberg C, Perry JRB, Wareham NJ, Scott RA: Large-scale GWAS identifies multiple loci for hand grip strength providing biological insights into muscular fitness. Nat Commun 8: 16015, 2017
93. Williams MA, Haskell WL, Ades PA, Amsterdam EA, Bittner V, Franklin BA, Gulanick M, Laing ST, Stewart KJ, American Heart Association Council on Clinical C, American Heart Association Council on Nutrition PA, Metabolism: Resistance exercise in individuals with and without cardiovascular disease: 2007 update: a scientific statement from the American Heart Association Council on Clinical Cardiology and Council on Nutrition, Physical Activity, and Metabolism. Circulation 116: 572-584, 2007 94. Won CW, Kim S: Use of Frailty in Deciding Clinical Treatment Goals for Chronic Disease in Elderly Patients in the Community. J Am Med Dir Assoc 17: 967-969, 2016
95. Wu Y, Wang W, Liu T, Zhang D: Association of Grip Strength With Risk of All-Cause Mortality, Cardiovascular Diseases, and Cancer in Community-Dwelling Populations: A Meta-analysis of Prospective Cohort Studies. J Am Med Dir Assoc 18: 551 e517-551 e535, 2017
96. Xu L, Hao YT: Effect of handgrip on coronary artery disease and myocardial infarction: a Mendelian randomization study. Sci Rep 7: 954, 2017
97. Yang EJ, Lim S, Lim JY, Kim KW, Jang HC, Paik NJ: Association between muscle strength and metabolic syndrome in older Korean men and women:
the Korean Longitudinal Study on Health and Aging. Metabolism 61: 317-324, 2012
98. Yates T, Zaccardi F, Dhalwani NN, Davies MJ, Bakrania K, Celis-Morales CA,
85
Gill JMR, Franks PW, Khunti K: Association of walking pace and handgrip strength with all-cause, cardiovascular, and cancer mortality: a UK Biobank
Gill JMR, Franks PW, Khunti K: Association of walking pace and handgrip strength with all-cause, cardiovascular, and cancer mortality: a UK Biobank