Handgrip Strength and Pulmonary Disease in the Elderly: What is the Link?
Tatiana Rafaela Lemos Lima1, Vívian Pinto Almeida1, Arthur Sá Ferreira1, Fernando Silva Guimarães1, Agnaldo José Lopes1,2,*
1Rehabilitation Sciences Post-Graduate Program, Augusto Motta University Center (UNISUAM), Bonsucesso, 21041-010, Rio de Janeiro, Brazil 2Post-graduate Program in Medical Sciences, School of Medical Sciences, State University of Rio de Janeiro (UERJ), Vila Isabel, 20550-170, Rio de Janeiro, Brazil
Societies in developed countries are aging at an unprecedented rate. Considering that aging is the most significant risk factor for many chronic lung diseases (CLDs), understanding this process may facilitate the development of new interventionist approaches. Skeletal muscle dysfunction is a serious problem in older adults with CLDs, reducing their quality of life and survival. In this study, we reviewed the possible links between handgrip strength (HGS)—a simple, noninvasive, low-cost measure of muscle function—and CLDs in the elderly. Different mechanisms appear to be involved in this association, including systemic inflammation, chronic hypoxemia, physical inactivity, malnutrition, and corticosteroid use. Respiratory and peripheral myopathy, associated with muscle atrophy and a shift in muscle fiber type, also seem to be major etiological contributors to CLDs. Moreover, sarcopenic obesity, which occurs in older adults with CLDs, impairs common inflammatory pathways that can potentiate each other and further accelerate the functional decline of HGS. Our findings support the concept that the systemic effects of CLDs may be determined by HGS, and HGS is a relevant measurement that should be considered in the clinical assessment of the elderly with CLDs. These reasons make HGS a useful practical tool for indirectly evaluating functional status in the elderly. At present, early muscle reconditioning and optimal nutrition appear to be the most effective approaches to reduce the impact of CLDs and low muscle strength on the quality of life of these individuals. Nonetheless, larger in-depth studies are needed to evaluate the link between HGS and CLDs.
Proinflammatory cytokines cause injury to skeletal muscles
Reduction of insulin-like growth factor I contributes to muscle dysfunction
There are interrelationships between difficult-to-control asthma, long-term asthma and decreased HGS
Sex hormones may play a role in explaining intrinsic differences in HGS between genders
Corticosteroid use negatively impacts HGS in difficult-to-control asthma
The combination of sarcopenia and obesity (sarcopenic obesity) exposes common inflammatory pathways that enhance each other
[16, 54, 86, 87]
Increased ROS production and secretion of adipokines and cytokines such as IL-6, TNF-α and mcp-1 affect skeletal muscle quality
Increased insulin resistance and dysregulation in the hypothalamic-pituitary-adrenal axis increase the risk of depression
Oxidative stress and catabolic inflammatory processes increase sarcopenia
[1, 62, 63, 70]
Mitochondrial dysfunction and accumulation of aged mitochondria damage skeletal muscle
[1, 17, 70]
The cumulative amount of corticosteroids independently predicts reduced muscle strength
[61, 62, 72, 81]
Muscle fiber disorganization and cellular metabolic changes impair metabolic demand in episodes of disease exacerbation
Physical deconditioning and long-term disease are associated with lower HGS
Mitochondrial dysfunction and ROS increase muscle fatigue
Increased energy expenditure, changes in metabolism and cachexia compromise peripheral muscles
[51, 79, 80]
Possible tumor-host interactions may cause muscle dysfunction
[49, 51, 79, 80]
Gluconeogenic precursors are crucial for maintenance of muscle function and are related to survival
The amount of skeletal muscle mass directly impacts survival
“Acute sarcopenia” secondary to hospitalization aggravates peripheral muscle performance
Lifestyle change imposed by cancer worsens HGS reduction
Table 1 Main findings that support a link between different chronic lung diseases and reduced handgrip strength in the elderly.
Figure 5. Possible mechanisms of the linkage between handgrip and pulmonary disease in the elderly.
Figure 6. Relationship between inflamm-aging, muscle function, and chronic lung disease in the elderly. While inflamm-aging can lead to damage to muscle and lung tissue, muscle can exert a protective effect on the genesis of chronic lung diseases. IL-1β = interleukin 1β; IL-6 = interleukin 6; TNF-α = tumor necrosis factor-α.
Ascher K, Elliot SJ, Rubio GA, Glassberg MK (2017). Lung diseases of the elderly: cellular mechanisms. Clin Geriatr Med, 33:473-90.
Rosenberg IH (1989). Epidemiologic and methodologic problems in determining nutritional status of older persons: proceedings of a conference. Albuquerque, New Mexico, October 19-21, 1988. Am J Clin Nutr, 50(5 Suppl):1231-3.
Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, et al (2010). Sarcopenia: European consensus on definition and diagnosis: Report of the European Working Group on Sarcopenia in Older People. Age Ageing, 39:412-23.
Marino DM, Marrara KT, Ike D, De Oliveira ADJr, Jamami M, Di Lorenzo VA (2010). Study of peripheral muscle strength and severity indexes in individuals with chronic obstructive pulmonary disease. Physiother Res Int, 15:135-43.
Sanderson WC, Scherbov S (2014). Measuring the speed of aging across population subgroups. PLoS One, 9:e96289.
Sillanpää E, Stenroth L, Bijlsma AY, Rantanen T, McPhee JS, Maden-Wilkinson TM, et al (2014). Associations between muscle strength, spirometric pulmonary function and mobility in healthy older adults. Age, 36:9667.
Volaklis KA, Halle M, Thorand B, Peters A, Ladwig KH, Schulz H, et al (2016). Handgrip strength is inversely and independently associated with multimorbidity among older women: results from the KORA-Age study. Eur J Intern Med, 31:35-40.
Martinez CH, Diaz AA, Meldrum CA, McDonald MN, Murray S, Kinney GL, et al (2017). Handgrip strength in chronic obstructive pulmonary disease: associations with acute exacerbations and body composition. Ann Am Thorac Soc, 14:1638-645.
Celis-Morales CA, Welsh P, Lyall DM, Steell L, Petermann F, Anderson J, et al (2018). Associations of grip strength with cardiovascular, respiratory, and cancer outcomes and all causes mortality: prospective cohort study of half a million UK Biobank participants. BMJ, 361:k1651.
Albarrati AM, Gale NS, Enright S, Munnery MM, Cockcroft JR, Shale DJ (2016). A simple and rapid test of physical performance in chronic obstructive pulmonary disease. Int J Chron Obstruct Pulmon Dis, 11:1785-91.
Garcia IFF, Tiuganji CT, Simões MDSMP, Santoro IL, Lunardi AC (2017). Systemic effects of chronic obstructive pulmonary disease in young-old adults' life-space mobility. Int J Chron Obstruct Pulmon Dis, 12:2777-85.
Lopes AJ, Vigário PS, Hora AL, Deus CAL, Soares MS, Guimarães FS, et al (2018). Ventilation distribution, pulmonary diffusion and peripheral muscle endurance as determinants of exercise intolerance in elderly patients with chronic obstructive pulmonary disease. Physiol Res: [in press].
Hora AL, Guimarães FS, Menezes SLS, Soares MS, Bunn P, Lopes AJ (2018). The relationship between muscle function, lung function and quality of life in patients with chronic obstructive pulmonary disease (COPD). Isokinet Exerc Sci, 26:17-27.
Richardson WS, Wilson MC, Nishikawa J, Hayward RS (1995). The well-built clinical question: a key to evidence-based decisions. ACP J Club, 123:A12-3.
Riviati N, Setiati S, Laksmi PW, Abdullah M (2017). Factors related with handgrip strength in elderly patients. Acta Med Indones, 49:215-9.
Öztürk ZA, Türkbeyler İH, Abiyev A, Kul S, Edizer B, Yakaryılmaz FD, et al (2018). Health related quality of life and fall risk associated with age related body composition changes; sarcopenia, obesity and sarcopenic obesity. Intern Med J, 48:973-81.
Meiners S, Eickelberg O, Königshoff M (2015). Hallmarks of the ageing lung. Eur Respir J, 45:807-27.
Ito K, Mercado N (2014). STOP accelerating lung aging for the treatment of COPD. Exp Gerontol, 59:21-7.
Ciprandi G, Schiavetti I, Ricciardolo FLM (2018). The impact of aging on outpatients with asthma in a real-world setting. Respir Med, 136:58-64.
van Moorsel CHM (2018). Trade-offs in aging lung diseases: a review on shared but opposite genetic risk variants in idiopathic pulmonary fibrosis, lung cancer and chronic obstructive pulmonary disease. Curr Opin Pulm Med, 24:309-17.
Tran D, Rajwani K, Berlin DA (2018). Pulmonary effects of aging. Curr Opin Anaesthesiol, 31:19-23.
van Oostrom SH, Engelfriet PM, Verschuren WMM, Schipper M, Wouters IM, Boezen M, et al (2018). Aging-related trajectories of lung function in the general population: the Doetinchem Cohort Study. PLoS One, 13:e0197250.
Skloot GS (2017). The effects of aging on lung structure and function. Clin Geriatr Med, 33:447-57.
Lowery EM, Brubaker AL, Kuhlmann E, Kovacs EJ (2013). The aging lung. Clin Interv Aging, 8:1489-96.
Ohara DG, Pegorari MS, Oliveira Dos Santos NL, de Fátima Ribeiro SilvaC, MonteiroRL, Matos AP, et al (2018). Respiratory muscle strength as a discriminator of sarcopenia in community-dwelling elderly: a cross-sectional study. J Nutr Health Aging, 22:952-8.
Barabasi AL, Gulbahce N, Loscalzo J (2011). Network medicine: a network-based approach to human disease. Nat Rev Genet, 12:56-68.
Scichilone N (2017). Comorbidities of lung disease in the elderly. Clin Geriatr Med, 33:597-603.
Frohnhofen H, Hagen O (2011). Handgrip strength measurement as a predictor for successful dry powder inhaler treatment: application in older individuals with COPD. Z Gerontol Geriatr, 44:245-9.
Veiga J, Lopes AJ, Jansen JM, Melo PL (2012). Fluctuation analysis of respiratory impedance waveform in asthmatic patients: effect of airway obstruction. Med Biol Eng Comput, 50:1249-59.
Moorman JE, Akinbami LJ, Bailey CM, Zahran HS, King ME, Johnson CA, et al (2012). National surveillance of asthma: United States, 2001-2010. Vital Health Stat 3, 35:1-58.
Ida S, Kaneko R, Murata K (2018). SARC-F for screening of sarcopenia among older adults: a meta-analysis of screening test accuracy. J Am Med Dir Assoc, 19:685-9.
Matteini AM, Tanaka T, Karasik D, Atzmon G, Chou WC, Eicher JD, et al (2016). GWAS analysis of handgrip and lower body strength in older adults in the CHARGE consortium. Aging Cell, 15:792-800.
Rantanen T, Volpato S, Ferrucci L, Heikkinen E, Fried LP, Guralnik JM (2003). Handgrip strength and cause-specific and total mortality in older disabled women: exploring the mechanism. J Am Geriatr Soc, 51:636-41.
Lustosa LP, Batista PP, Pereira DS, Pereira LSM, Scianni A, Ribeiro-Samora GA (2017). Comparison between parameters of muscle performance and inflammatory biomarkers of non-sarcopenic and sarcopenic elderly women. Clin Interv Aging, 12:1183-91.
Son DH, Yoo JW, Cho MR, Lee YJ (2018). Relationship between handgrip strength and pulmonary function in apparently healthy older women. Am Geriatr Soc, 66:1367-71.
Anton SD, Woods AJ, Ashizawa T, Barb D, Buford TW, Carter CS, et al (2015). Successful aging: advancing the science of physical independence in older adults. Ageing Res Rev 24(Pt B):304-27.
Scimeca M, Centofanti F, Celi M, Gasbarra E, Novelli G, Botta A, et al (2018). Vitamin D receptor in muscle atrophy of elderly patients: a key element of osteoporosis-sarcopenia connection. Aging Dis, 9:952-64.
Pleguezuelos E, Esquinas C, Moreno E, Guirao L, Ortiz J, Garcia-Alsina J, et al (2016). Muscular dysfunction in COPD: systemic effect or deconditioning? Lung, 194:249-57.
Kaymaz D, Candemir İÇ, Ergün P, Demir N, Taşdemir F, Demir P (2018). Relation between upper-limb muscle strength with exercise capacity, quality of life and dyspnea in patients with severe chronic obstructive pulmonary disease. Clin Respir J, 12:1257-63.
Jones SE, Maddocks M, Kon SS, Canavan JL, Nolan CM, Clark AL, et al (2015). Sarcopenia in COPD: prevalence, clinical correlates and response to pulmonary rehabilitation. Thorax, 70:213-8.
Limpawattana P, Inthasuwan P, Putraveephong S, Boonsawat W, Theerakulpisut D, Sawanyawisuth K (2018). Sarcopenia in chronic obstructive pulmonary disease: a study of prevalence and associated factors in the Southeast Asian population. Chron Respir Dis, 15:250-7.
Jaitovich A, Barreiro E (2018). Skeletal muscle dysfunction in chronic obstructive pulmonary disease: what we know and can do for our patients. Am J Respir Crit Care Med, 198:175-86.
Byun MK, Cho EN, Chang J, Ahn CM, Kim HJ (2017). Sarcopenia correlates with systemic inflammation in COPD. Int J Chron Obstruct Pulmon Dis, 12:669-75.
Burtin C, Ter Riet G, Puhan MA, Waschki B, Garcia-Aymerich J, Pinto-Plata V, et al (2016). Handgrip weakness and mortality risk in COPD: a multicentre analysis. Thorax, 71:86-7.
Gale NS, Albarrati AM, Munnery MM, Hubbard RE, Tal-Singer R, Cockcroft JR, et al (2018). Frailty: a global measure of the multisystem impact of COPD. Chron Respir Dis, 15:347-55.
Cortopassi F, Celli B, Divo M, Pinto-Plata V (2015). Longitudinal changes in handgrip strength, hyperinflation, and 6-minute walk distance in patients with COPD and a control group. Chest, 148:986-94.
Cheung CL, Nguyen US, Au E, Tan KC, Kung AW (2013). Association of handgrip strength with chronic diseases and multimorbidity: a cross-sectional study. Age, 35:929-41.
Stene GB, Helbostad JL, Amundsen T, Sørhaug S, Hjelde H, Kaasa S, et al (2015). Changes in skeletal muscle mass during palliative chemotherapy in patients with advanced lung cancer. Acta Oncol, 54:340-8.
Shachar SS, Williams GR, Muss HB, Nishijima TF (2016). Prognostic value of sarcopenia in adults with solid tumours: a meta-analysis and systematic review. Eur J Cancer, 57:58-67.
Barata AT, Santos C, Cravo M, Vinhas MD, Morais C, Carolino E, et al (2017). Handgrip dynamometry and Patient-Generated Subjective Global Assessment in patients with nonresectable lung cancer. Nutr Cancer, 69:154-8.
Dowman L, McDonald CF, Hill CJ, Lee A, Barker K, Boote C, et al (2016). Reliability of the hand held dynamometer in measuring muscle strength in people with interstitial lung disease. Physiotherapy, 102:249-55.
Kapella MC, Larson JL, Covey MK, Alex CG (2011). Functional performance in chronic obstructive pulmonary disease declines with time. Med Sci Sports Exerc, 43:218-24.
Stenholm S, Rantanen T, Heliövaara M, Koskinen S (2008). The mediating role of C-reactive protein and handgrip strength between obesity and walking limitation. J Am Geriatr Soc, 56:462-9.
Haarmann H, Folle J, Nguyen XP, Herrmann P, Heusser K, Hasenfuß G, et al (2017). Impact of non-invasive ventilation on sympathetic nerve activity in chronic obstructive pulmonary disease. Lung, 195:69-75.
Lopes AJ, de Melo PL (2016). Brazilian studies on pulmonary function in COPD patients: what are the gaps? Int J Chron Obstruct Pulmon Dis, 11:1553-67.
Lopes AJ, Mafort TT (2014). Correlations between small airway function, ventilation distribution, and functional exercise capacity in COPD patients. Lung, 192:653-9.
Enright PL, Kronmal RA, Manolio TA, Schenker MB, Hyatt RE (1994). Respiratory muscle strength in the elderly: correlates and reference values. Cardiovascular Health Study Research Group. Am J Respir Crit Care Med, 149(2 Pt 1):430-8.
Cortopassi F, Divo M, Pinto-Plata V, Celli B (2011). Resting handgrip force and impaired cardiac function at rest and during exercise in COPD patients. Respir Med, 105:748-54.
García-Lucio J, Peinado VI, de Jover L, Del Pozo R, Blanco I, Bonjoch C, et al (2018). Imbalance between endothelial damage and repair capacity in chronic obstructive pulmonary disease. PLoS One, 13:e0195724.
Miranda NADF, Goulart CDL, Silva ABE, Cardoso DM, Paiva DN, Trimer R, et al (2018). Does peripheral arterial occlusive disease influence muscle strength and exercise capacity in COPD patients? J Vasc Bras, 16:285-92.
Hanada M, Sakamoto N, Ishimatsu Y, Kakugawa T, Obase Y, Kozu R, et al (2016). Effect of long-term treatment with corticosteroids on skeletal muscle strength, functional exercise capacity and health status in patients with interstitial lung disease. Respirology, 21:1088-93.
Gea J, Bàdenes D, Balcells E (2018). Nutritional abnormalities and muscle dysfunction in idiopathic pulmonary fibrosis. Arch Bronconeumol, 54:545-6.
Agustí A, Edwards LD, Rennard SI, MacNee W, Tal-Singer R, Miller BE, et al (2012). Persistent systemic inflammation is associated with poor clinical outcomes in COPD: a novel phenotype. PLoS One, 7:e37483.
Agusti A, Barbera JA, Wouters EF, Peinado VI, Jeffery PK (2013). Lungs, bone marrow, and adipose tissue: a network approach to the pathobiology of chronic obstructive pulmonary disease. Am J Respir Crit Care Med, 188:1396-406.
Kovacs EJ, Boe DM, Boule LA, Curtis BJ (2017). Inflammaging and the lung. Clin Geriatr Med, 33:459-71.
Stenholm S, Tiainen K, Rantanen T, Sainio P, Heliövaara M, Impivaara O, et al (2012). Long-term determinants of muscle strength decline: prospective evidence from the 22-year mini-Finland follow-up survey. J Am Geriatr Soc, 60:77-85.
Kang MJ, Shadel GS (2016). A mitochondrial perspective of chronic obstructive pulmonary disease pathogenesis. Tuberc Respir Dis, 79:207-13.
Al-Obaidi S1, Al-Sayegh N, Nadar M (2014). Smoking impact on grip strength and fatigue resistance: implications for exercise and hand therapy practice. J Phys Act Health, 11:1025-31.
Bueno M, Lai YC, Romero Y, St Croix CM, Kamga C, Corey C, et al (2015). PINK1 deficiency impairs mitochondrial homeostasis and promotes lung fibrosis. J Clin Invest, 125:521-38.
Even B, Fayad-Kobeissi S, Gagliolo JM, Motterlini R, Boczkowski J, Foresti R, et al (2018). Heme oxygenase-1 induction attenuates senescence in chronic obstructive pulmonary disease lung fibroblasts by protecting against mitochondria dysfunction. Aging Cell, 17:e12837.
Shimokata H, Shimada H, Satake S, Endo N, Shibasaki K, Ogawa S, et al (2018). Chapter 2: Epidemiology of sarcopenia. Geriatr Gerontol Int, 18(Suppl 1):13-22.
Kozu R, Jenkins S, Senjyu H (2014). Evaluation of activity limitation in patients with idiopathic pulmonary fibrosis grouped according to Medical Research Council dyspnea grade. Arch Phys Med Rehabil, 95:950-5.
Welch C, K Hassan-Smith Z, A Greig C, M Lord J, A Jackson T (2018) Acute sarcopenia secondary to hospitalization: an emerging condition affecting older adults. Aging Dis, 9:151-64.
Sosa P, Alcalde-Estevez E, Plaza P, Troyano N, Alonso C, Martínez-Arias L, et al (2018) Hyperphosphatemia promotes senescence of myoblasts by impairing autophagy through ILK overexpression, a possible mechanism involved in sarcopenia. Aging Dis, 9:769-84.
Campos-Obando N, Lahousse L, Brusselle G, Stricker BH, Hofman A, Franco OH, et al (2018) Serum phosphate levels are related to all-cause, cardiovascular and COPD mortality in men. Eur J Epidemiol: [in press].
Dubé BP, Laveneziana P (2018) Effects of aging and comorbidities on nutritional status and muscle dysfunction in patients with COPD. J Thorac Dis, 10(Suppl 12):S1355-66.
de Blasio F, Di Gregorio A, de Blasio F, Bianco A, Bellofiore B, Scalfi L (2018). Malnutrition and sarcopenia assessment in patients with chronic obstructive pulmonary disease according to international diagnostic criteria, and evaluation of raw BIA variables. Respir Med, 134:1-5.
Lis CG, Gupta D, Lammersfeld CA, Markman M, Vashi PG (2012). Role of nutritional status in predicting quality of life outcomes in cancer: a systematic review of the epidemiological literature. Nutr J, 11:27.
Guerra RS, Fonseca I, Pichel F, Restivo MT, Amaral TF (2014). Handgrip strength cutoff values for undernutrition screening at hospital admission. Eur J Clin Nutr, 68:1315-21.
Schakman O, Kalista S, Barbé C, Loumaye A, Thissen JP (2013). Glucocorticoid-induced skeletal muscle atrophy. Int J Biochem Cell Biol, 45:2163-72.
Decramer M, de Bock V, Dom R (1996). Functional and histologic picture of steroid-induced myopathy in chronic obstructive pulmonary disease. Am J Respir Crit Care Med, 153(6 Pt 1):1958-64.
Bowyer SL, LaMothe MP, Hollister JR (1985). Steroid myopathy: incidence and detection in a population with asthma. J Allergy Clin Immunol, 76(2 Pt 1):234-42.
Mafort TT, Rufino R, Costa CH, Lopes AJ (2016). Obesity: systemic and pulmonary complications, biochemical abnormalities, and impairment of lung function. Multidiscip Respir Med, 11:28.
Leite Ribeiro TE, Costa de Freitas SilvaE, Silveira de MenesesSL, Lopes AJ (2009). Correlation of clinical findings with functional parameters in elderly asthma patients. Rev Port Pneumol, 15:1029-41.
Akishita M, Kozaki K, Iijima K, Tanaka T, Shibasaki K, Ogawa S, et al (2018). Chapter 1: Definitions and diagnosis of sarcopenia. Geriatr Gerontol Int, 18(Suppl 1):7-12.
Xiao J, Cain A, Purcell SA, Ormsbee MJ, Contreras RJ, Kim JS, et al (2018). Sarcopenic obesity and health outcomes in patients seeking weight loss treatment. Clin Nutr ESPEN, 23:79-83.
Strasser B, Volaklis K, Fuchs D, Burtscher M (2018). Role of dietary protein and muscular fitness on longevity and aging. Aging Dis, 9:119-32.
Pedersen B Muscles and their myokines (2011). J Exp Biol, 214(Pt 2):337-46.
Febbraio MA, Pedersen BK (2002). Muscle-derived interleukin-6: mechanisms for activation and possible biological roles. FASEB J, 16:1335-47.
Pleguezuelos E, Guirao L, Moreno E, Samitier B, Ortega P, Vila X, et al (2018). Ischiocrural strength may be a better prognostic marker than quadriceps strength in COPD. Lung, 196:665-8.
Mohamed-Hussein AAR, Makhlouf HA, Selim ZI, Gamaleldin Saleh W (2018). Association between hand grip strength with weaning and intensive care outcomes in COPD patients: a pilot study. Clin Respir J, 12:2475-9.
Neves RS, Lopes AJ, Menezes SLS, Lima TRL, Ferreira AS, Guimarães FS (2017). Hand grip strength in healthy young and older Brazilian adults: development of a linear prediction model using simple anthropometric variables. Kinesiology, 49:208-16.
Arai H, Wakabayashi H, Yoshimura Y, Yamada M, Kim H, Harada A (2018). Chapter 4: Treatment of sarcopenia. Geriatr Gerontol Int, 18(Suppl 1):28-44.