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Relation of functional capacity, strength and muscle mass in elderly women with osteopenia and osteoporosis

Abstracts

This study aimed at analyzing the association among functional ability tests, performance of knee muscles, and body composition of elderly women with low bone densities. A transverse study with 48 elderly women (aged 70.62±5.95 years) was developed, and their functional abilities were evaluated (Timed Up and Go - TUG - and Chair Stand - CST - tests), as well as their knee muscle performance (isokinetic dynamometer), their muscle mass (skeletal muscle index with BIA), and their lean mass (skin folds). The majority of the sample was active or moderately active (95.8%), was found to be overweight (68.75%), was not found to have sarcopenia (62.5%), and had average performances of 7.7 seconds in TUG and 11.21 seconds in CST. The functional ability was found to have moderate and low negative correlations with the knee muscle performance variables. Their muscle mass was found to have a low positive correlation with the power of knee extensor muscles and it was found to have no correlation with the functional ability, which was only found to have an association with the muscle performance, which reinforces how unreliable it is to use muscle mass as the single measurement for the identification of sarcopenia.

Elderly; Bone Density; Muscle Strength; Body Composition


Este estudo buscou analisar a associação entre testes de capacidade funcional, desempenho dos músculos do joelho e composição corporal de idosas com baixa densidade óssea. Foi desenvolvido um estudo transversal com 48 idosas (70,62±5,95 anos). Avaliou-se a capacidade funcional (testes Timed Up and Go - TUG e levantar e sentar na cadeira - TLS), desempenho muscular de joelho (dinamômetro isocinético), massa muscular (índice muscular esquelético com BIA) e massa magra (dobras cutâneas). A maioria da amostra era ativa ou moderadamente ativa (95,8%), apresentou sobrepeso (68,75%), ausência de sarcopenia (62,5%) e desempenho médio de 7,7 segundos no TUG e de 11,21 segundos no TLS. Observaram-se correlações negativas moderadas e baixas da capacidade funcional com as variáveis de desempenho muscular de joelho. A massa muscular apresentou correlação positiva baixa com potência de extensores de joelho e não apresentou correlação com a capacidade funcional, a qual apresentou associação somente com o desempenho muscular, reforçando a fragilidade do uso da massa muscular como medida única na identificação de sarcopenia.

Idoso; Densidade Óssea; Força Muscular; Composição Corporal


En este estudio se analizó la relación entre pruebas de capacidad funcional, el rendimiento de los músculos de la rodilla y la composición corporal de adultos mayores con baja densidad ósea. Se desarrolló un estudio transversal con 48 adultos mayores (70,62±5,95 años) para que se evalúe la capacidad funcional (test de Timed Up and Go - TUG y el de Levantarse y Sentarse en la silla - TLS), el rendimiento muscular de la rodilla (dinamómetro isocinético), la masa muscular (índice del músculo esquelético con BIA) y la masa magra (pliegues cutáneos). La mayoría de la muestra era activa o moderadamente activa (un 95,8%), presentaba sobrepeso (un 68,75%) ausencia de sarcopenia (un 62,5%) y un rendimiento medio de 7,7 segundos en el TUG y de 11,21 segundos en el TLS. Se observó moderadas y bajas correlaciones negativas en cuanto a la capacidad funcional con las variables de rendimiento muscular de la rodilla. La masa muscular mostró una baja correlación positiva con la potencia de extensores de rodilla, en cambio, no señaló una correlación con la capacidad funcional, que había demostrado relación solamente con el rendimiento muscular, lo que refuerza la fragilidad de utilización de la masa muscular como única medida para que se identifique la sarcopenia.

Adultos Mayores; Densidad Ósea; Fuerza Muscular; Composición Corporal


INTRODUCTION

Aging is characterized by a decline in body functions and by alterations in all body levels1. Reid KF, Fielding RA. Skeletal muscle power: a critical determinant of physical functioning in older adults. Exerc Sport Sci Rev. 2012;40(1):4-12.. Among the body composition alterations, there are highlights to the gradual increase of fat mass2. Vilaca KH, Alves NM, Carneiro JA, Ferriolli E, Lima NK, Moriguti JC. Body composition, muscle strength and quality of active elderly women according to the distance covered in the 6-minute walk test. Braz J Phys Ther. 2013;17(3):289-96. and the decreased bone and muscle mass, with a reduction in the number and size of type II muscle fibers3. Rikkonen T, Sirola J, Salovaara K, Tuppurainen M, Jurvelin JS, Honkanen R, et al. Muscle strength and body composition are clinical indicators of osteoporosis. Calcif Tissue Int. 2012;91(2):131-8.. From age 40 and on, 5% muscle mass is estimated to be lost with each decade, with a faster decline after age 654. Hairi NN, Cumming RG, Naganathan V, Handelsman DJ, Le Couteur DG, Creasey H, et al. Loss of muscle strength, mass (sarcopenia), and quality (specific force) and its relationship with functional limitation and physical disability: the Concord Health and Ageing in Men Project. J Am Geriatr Soc. 2010;58(11):2055-62., particularly in the lower limbs; that quantitative loss of transverse muscle area has been observed to contribute to muscle weakness5. Janssen I, Steven B, Heymsfield M, Robert R. Low Relative Skeletal Muscle mass (sarcopenia) in older persons is associated with functional impairment and physical disability. J Am Geriatric Soc. 2002;50:889-96. 6. Janssen I, Baumgartner RN, Ross R, Rosenberg IH, Roubenoff R. Skeletal muscle cutpoints associated with elevated physical disability risk in older men and women. Am J Epidemiol. 2004;159(4):413-21.. Those gradual mass and muscle strength losses define sarcopenia, a geriatric syndrome that is considered to be a determining factor for bone mineral density (BMD)3. Rikkonen T, Sirola J, Salovaara K, Tuppurainen M, Jurvelin JS, Honkanen R, et al. Muscle strength and body composition are clinical indicators of osteoporosis. Calcif Tissue Int. 2012;91(2):131-8., which is found to have a multifactorial etiology7. Di MM, Vallero F, Di MR, Tappero R. Prevalence of sarcopenia and its association with osteoporosis in 313 older women following a hip fracture. Arch Gerontol Geriatr. 2011;52(1):71-4. and present individuals to adverse health situations, with functional losses, dependency, social restrictions, and increased health costs and mortality8. Carmeli E, Imam B, Merrick J. The relationship of pre-sarcopenia (low muscle mass) and sarcopenia (loss of muscle strength) with functional decline in individuals with intellectual disability (ID). Arch Gerontol Geriatr. 2012;55(1):181-5..

Most studies for the prevalence of sarcopenia have used the decrease in muscle mass as the only criterion for its identification7. Di MM, Vallero F, Di MR, Tappero R. Prevalence of sarcopenia and its association with osteoporosis in 313 older women following a hip fracture. Arch Gerontol Geriatr. 2011;52(1):71-4.. However, the low muscle mass, on itself, may not be enough to recognize the risk of adverse functional results9. Patil R, Uusi-Rasi K, Pasanen M, Kannus P, Karinkanta S, Sievanen H. Sarcopenia and osteopenia among 70-80-year-old home-dwelling Finnish women: prevalence and association with functional performance. Osteoporos Int. 2013;24(3):787-96., and the functional ability investigation has been standing out among the findings regarding the association between the functional ability and the muscle performance of elderly people4. Hairi NN, Cumming RG, Naganathan V, Handelsman DJ, Le Couteur DG, Creasey H, et al. Loss of muscle strength, mass (sarcopenia), and quality (specific force) and its relationship with functional limitation and physical disability: the Concord Health and Ageing in Men Project. J Am Geriatr Soc. 2010;58(11):2055-62. 1010 . Goodpaster BH, Park SW, Harris TB, Kritchevsky SB, Nevitt M, Schwartz AV, et al. The loss of skeletal muscle strength, mass, and quality in older adults: the health, aging and body composition study. J Gerontol A Biol Sci Med Sci. 2006;61(10):1059-64.. Studies have been identifying significant associations of muscle strength and muscle power of knee extensors and flexors with the ability to stand up from a chair4. Hairi NN, Cumming RG, Naganathan V, Handelsman DJ, Le Couteur DG, Creasey H, et al. Loss of muscle strength, mass (sarcopenia), and quality (specific force) and its relationship with functional limitation and physical disability: the Concord Health and Ageing in Men Project. J Am Geriatr Soc. 2010;58(11):2055-62. 1111 . Crockett K, Ardell K, Hermanson M, Penner A, Lanovaz J, Farthing J, et al. The relationship of knee-extensor strength and rate of torque development to sit-to-stand performance in older adults. Physiother Can. 2013;65(3):229-35. and with the walking speed1212 . Garcia PA, Dias JM, Dias RC, Santos P, Zampa CC. A study on the relationship between muscle function, functional mobility and level of physical activity in community-dwelling elderly. Rev Bras Fisioter. 2011;15(1):15-22.; and the associations of torque peaks of knee extensors and flexors and the muscle work of knee extensors with the abilities to stand up and walk1313 . Pisciottano MV, Pinto SS, Szejnfeld VL, Castro CH. The relationship between lean mass, muscle strength and physical ability in independent healthy elderly women from the community. J Nutr Health Aging. 2014;18(5):554-8. 1414 . Lustosa LP, Silva JP, Coelho FM, Pereira DS, Parentoni AN, Pereira LS. Impact of resistance exercise program on functional capacity and muscular strength of knee extensor in pre-frail community-dwelling older women: a randomized crossover trial. Rev Bras Fisioter. 2011;15(4):318-24. among elderly people. Considering that, the European Working Group on Sarcopenia in Older People has suggested the following criteria for the classification of sarcopenia: reduced muscle mass and strength, with hindered ability to perform a functional activity1515 . Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, et al. Sarcopenia: European consensus on definition and diagnosis: Report of the European Working Group on Sarcopenia in Older People. Age Ageing. 2010;39(4):412-23.. Those considerations point towards the possibility for the use of physical-functional evaluation tools, not only for identifying activity limitations, but also as a feasible, valid, and reproducible alternative to infer structural and functional disabilities, which allows identifying individuals who are at a clinical risk of having/developing sarcopenia1. Reid KF, Fielding RA. Skeletal muscle power: a critical determinant of physical functioning in older adults. Exerc Sport Sci Rev. 2012;40(1):4-12..

Due to that, this study aimed at analyzing the association among functional ability tests, performance of the muscles which move the knee, and the body composition of elderly women with BMDs.

METHODOLOGY

The transverse study was conducted with the approval from the Ethics Committee of Universidade Federal de Minas Gerais, and with the consent from the participants.

Elderly women of 60 years or older who had been diagnosed (≅31 months before the study or at the beginning of it) with osteopenia or osteoporosis in the L1-L4 femur segments or in the femoral neck (T-score <−1,0 DP in the bone densitometry scan) were selected in a non-randomized way from health care programs targeted at elderly people in Brazil's Distrito Federal (Federal District). Elderly women who had found to be cognitively impaired through a Mini Mental State Examination1616 . Brucki SM, Nitrini R, Caramelli P, Bertolucci PH, Okamoto IH. Sugestões para o uso do mini-exame do estado mental no Brasil. Arq Neuropsiquiatr. 2003;61(3B):777-81. (<17), elderly women who had sequelae from neurological diseases, amputations, pain complaints, and history of recent fractures in lower limbs were excluded.

The adjusted activity score (AAS) and the Human Activity Profile (HAP) were used in order to assess the physical activity level, and they allowed classifying the elderly women as inactive (AAS<53), moderately active (AAS=53-54), or active (AAS>74)1717 . Souza AC, Magalhaes LC, Teixeira-Salmela LF. Adaptação transcultural e análise das propriedades psicométricas da versão brasileira do perfil de atividade humana. Cad Saude Publica. 2006;22(12):2623-36.. Mass (kg) and body height (m) were used in order to calculate the Body Mass Index - BMI (kg/m²).

Functional ability was measured through clinical tests Timed Up and Go (TUG) and Chair Stand Test (CST). TUG has measured mobility and body balance through the time required to stand up from a chair, walk three meters as fast as possible, spin, go all the way back and sit down again1818 . Bohannon RW. Reference Values for the Timed Up and Go Test: A Descriptive Meta-Analysis. J Geriatr Phys Ther. 2006;29(2):64-8.. CST evaluated the posture control and the muscle performance of lower limbs, through the evaluation of the time required to stand up and sit on a chair for five times, as fast as possible, with the arms folded on the chest1919 . Tiedemann A, Shimada H, Sherrington C, Murray S, Lord S. The comparative ability of eight functional mobility tests for predicting falls in community-dwelling older people. Age Ageing. 2008;37(4):430-5.. Both tests were performed in sequence (with no intervals), and the times which were longer than 10 seconds in TUG1818 . Bohannon RW. Reference Values for the Timed Up and Go Test: A Descriptive Meta-Analysis. J Geriatr Phys Ther. 2006;29(2):64-8. 1818 . Bohannon RW. Reference Values for the Timed Up and Go Test: A Descriptive Meta-Analysis. J Geriatr Phys Ther. 2006;29(2):64-8. and 12 seconds in CST1919 . Tiedemann A, Shimada H, Sherrington C, Murray S, Lord S. The comparative ability of eight functional mobility tests for predicting falls in community-dwelling older people. Age Ageing. 2008;37(4):430-5. were considered as indicative of damaged functional ability.

The isokinetic muscle performance was evaluated through the following measurements: torque peak to body mass (Newton-meter/body mass); work to body mass (Joule/body mass) at 60°/s (5 maximum repetitions); average power (Watts) at 180°/s (15 maximum repetitions) of knee flexors and extensors in the dominant lower limb (preferred for kicking) through a Biodex System 4 Pro(r) isokinetic dynamometer, using concentric contractions. The backrest of the dynamometer was fixed at 85°, the rotational axis of the device was aligned with the lateral epicondyle of the femur, the lever pillow was fixed three centimeters above the lateral malleolus, and the range of motion was set to 85°. The tests were performed according to the manufacturer's specifications, also considering the familiarization at the day of the test with the isokinetic exercise in a maximum and two submaximum repetitions, with correction for gravity, and 120-second rest between test speeds2020 . Drouin JM, Valovich-mcLeod TC, Shultz SJ, Gansneder BM, Perrin DH. Reliability and validity of the Biodex system 3 pro isokinetic dynamometer velocity, torque and position measurements. Eur J Appl Physiol. 2004;91(1):22-9..

Lean mass was estimated based on the averages of the three thickness measurements of biceps, triceps, subscapularis, midaxillary, pectoral, suprailiac, abdominal, thigh, and mid-calf skin fold sites2121 . Guedes DP. Composição corporal: princípios, técnicas e aplicações. 2 ed. Londrina: APEF; 1994., in the right hemibody, in order to calculate body fat percentage based on the prediction equation by Jackson et al.2222 . Jackson AS, Pollock ML, Ward A. Generalized equations for predicting body density of women. Med Sci Sports Exerc. 1980;12(3):175-81.. The lean mass percentage and its value in kilograms were calculated based on the body fat percentage. That lean mass measurement was collected from part of the sample (20 elderly women). The skeletal muscle mass index (SMMI) was obtained for the whole sample (48 elderly women) through Bioelectric Impedance (BIA) using the equation proposed by Janssen et al.2323 . Janssen I, Heymsfield SB, Baumgartner RN, Ross R. Estimation of skeletal muscle mass by bioelectrical impedance analysis. J Appl Physiol. 2000;89(2):465-71., which calculates absolute skeletal muscle mass (kg) as divided by the squared height (m²), which allows adjusting non-muscle components (bone, fat, and organs)5. Janssen I, Steven B, Heymsfield M, Robert R. Low Relative Skeletal Muscle mass (sarcopenia) in older persons is associated with functional impairment and physical disability. J Am Geriatric Soc. 2002;50:889-96.:

Muscle Mass: [(h2/r x 0.401) + (s x 3.825) + (i x -0.071)] + 5.102

h = height in cm; r = resistance in Ohm;

s = sex 0 for women; a = age in years.

That equation uses the resistance measurement from BIA, as collected through the tetrapolar body composition analyzer Maltron BF-900(r), and it consists in the imperceptible passage of low-intensity (500-800µÄ) and high frequency (50kHz) electric current through the body. During the evaluation, the elderly women lay on their backs, with the red electrodes being placed under the articular lines of the wrist and ankle, and the black electrodes on the third metacarpal bone (hand) and on the second metatarsal bone (foot) of the right hemibody6. Janssen I, Baumgartner RN, Ross R, Rosenberg IH, Roubenoff R. Skeletal muscle cutpoints associated with elevated physical disability risk in older men and women. Am J Epidemiol. 2004;159(4):413-21.. SMMI (kg/m²) allowed the indication of severe (≤5.75), moderate (5.76-6.75), or absent sarcopenia (≥6.76)1515 . Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, et al. Sarcopenia: European consensus on definition and diagnosis: Report of the European Working Group on Sarcopenia in Older People. Age Ageing. 2010;39(4):412-23..

Firstly, the data regarding age, medications used, bone densitometry, and HAP were collected at volunteers' houses. In the same week, in the Movement Laboratory, the following order of evaluations was conducted, with one-minute resting periods between each: body mass and height measurements; functional tests; isokinetic evaluation; skin fold thickness; and BIA. The compliance with the recommendations regarding the body impedance test were not monitored (excessive water intake, alcohol and coffee consumption in the previous 24 hours, and emptying of the bladder 30 minutes before the test)2424 . Maltron BF-900(r). Operating Manual. 1998. U.K., Maltron Internacional LTD. Disponivel em: http://maltronint.com/products/bf900.php
http://maltronint.com/products/bf900.php...
.

The statistical analyses were processed in SPSS 16.0 software. The data distribution normality was confirmed through Kolmogorov-Smirnov test; Pearson product-moment correlation coefficient was used, and a 5% significance level was considered.

RESULTS

48 elderly women were evaluated (70.62±5.95 years), of which most were considered as active, moderately active (95.8%)1717 . Souza AC, Magalhaes LC, Teixeira-Salmela LF. Adaptação transcultural e análise das propriedades psicométricas da versão brasileira do perfil de atividade humana. Cad Saude Publica. 2006;22(12):2623-36., and overweight (68.75%) (WHO classification) (Table 1).

Table 1
Clinical and demographic characteristics of the sample (n = 48)

The characteristics related to functional ability, mass, and muscle performance are in Table 2. Most subjects were found to have good performances in TUG (95.8%; average of 7.7 seconds) and in the Chair Stand Test (77.1%, average of 11.21 seconds), and 62.5% of elderly women were found to have SMMIs higher or equal to 6.76kg/m².

Table 2
Functional ability, muscle performance and mass of the sample (n=48)

In the correlation analyses (Table 3), TUG was found to have a high positive correlation with CST, moderate negative correlations with the work from knee extensors and with the level of physical activity; and low negative correlations with the remaining muscle performance variables. CST was found to have moderate negative correlations with the power from knee flexors and with the physical activity level, and low negative correlations with the remaining muscle performance variables. SMMI was found to have a low correlation, albeit positive, with the power from knee extensors. A moderate positive correlation (r=0.662; p=0.001) was found to exist between the two lean mass evaluation measurements, as well as low positive correlations between the physical activity level and all muscle performance variables.

Table 3
Correlation among studied variables

DISCUSSION

In this study, the three muscle performance parameters evaluated (torque peak, work, and muscle power) were found to have similar associations with standing up, sitting down, and fast walking activities, which corroborates findings in the literature4. Hairi NN, Cumming RG, Naganathan V, Handelsman DJ, Le Couteur DG, Creasey H, et al. Loss of muscle strength, mass (sarcopenia), and quality (specific force) and its relationship with functional limitation and physical disability: the Concord Health and Ageing in Men Project. J Am Geriatr Soc. 2010;58(11):2055-62. 1111 . Crockett K, Ardell K, Hermanson M, Penner A, Lanovaz J, Farthing J, et al. The relationship of knee-extensor strength and rate of torque development to sit-to-stand performance in older adults. Physiother Can. 2013;65(3):229-35. 1313 . Pisciottano MV, Pinto SS, Szejnfeld VL, Castro CH. The relationship between lean mass, muscle strength and physical ability in independent healthy elderly women from the community. J Nutr Health Aging. 2014;18(5):554-8. 2525 . Puthoff ML, Nielsen DH. Relationships among impairments in lower-extremity strength and power, functional limitations, and disability in older adults. Phys Ther. 2007;87(10):1334-47.. Several studies have also evaluated the relationships among those variables in community elderly people, and found a strong correlation between the muscle performance in the lower limbs with the decreased mobility in walking activities4. Hairi NN, Cumming RG, Naganathan V, Handelsman DJ, Le Couteur DG, Creasey H, et al. Loss of muscle strength, mass (sarcopenia), and quality (specific force) and its relationship with functional limitation and physical disability: the Concord Health and Ageing in Men Project. J Am Geriatr Soc. 2010;58(11):2055-62. 1212 . Garcia PA, Dias JM, Dias RC, Santos P, Zampa CC. A study on the relationship between muscle function, functional mobility and level of physical activity in community-dwelling elderly. Rev Bras Fisioter. 2011;15(1):15-22. 1313 . Pisciottano MV, Pinto SS, Szejnfeld VL, Castro CH. The relationship between lean mass, muscle strength and physical ability in independent healthy elderly women from the community. J Nutr Health Aging. 2014;18(5):554-8. 2525 . Puthoff ML, Nielsen DH. Relationships among impairments in lower-extremity strength and power, functional limitations, and disability in older adults. Phys Ther. 2007;87(10):1334-47. 2626 . Buchman AS, Wilson RS, Boyle PA, Tang Y, Fleischman DA, Bennett DA. Physical activity and leg strength predict decline in mobility performance in older persons. J Am Geriatr Soc. 2007;55(10):1618-23., and in activities regarding going up and down stairs8. Carmeli E, Imam B, Merrick J. The relationship of pre-sarcopenia (low muscle mass) and sarcopenia (loss of muscle strength) with functional decline in individuals with intellectual disability (ID). Arch Gerontol Geriatr. 2012;55(1):181-5. 2626 . Buchman AS, Wilson RS, Boyle PA, Tang Y, Fleischman DA, Bennett DA. Physical activity and leg strength predict decline in mobility performance in older persons. J Am Geriatr Soc. 2007;55(10):1618-23., with the reduced performance for standing up and sitting down4. Hairi NN, Cumming RG, Naganathan V, Handelsman DJ, Le Couteur DG, Creasey H, et al. Loss of muscle strength, mass (sarcopenia), and quality (specific force) and its relationship with functional limitation and physical disability: the Concord Health and Ageing in Men Project. J Am Geriatr Soc. 2010;58(11):2055-62. 8. Carmeli E, Imam B, Merrick J. The relationship of pre-sarcopenia (low muscle mass) and sarcopenia (loss of muscle strength) with functional decline in individuals with intellectual disability (ID). Arch Gerontol Geriatr. 2012;55(1):181-5. 1111 . Crockett K, Ardell K, Hermanson M, Penner A, Lanovaz J, Farthing J, et al. The relationship of knee-extensor strength and rate of torque development to sit-to-stand performance in older adults. Physiother Can. 2013;65(3):229-35. 2525 . Puthoff ML, Nielsen DH. Relationships among impairments in lower-extremity strength and power, functional limitations, and disability in older adults. Phys Ther. 2007;87(10):1334-47. and the possibility of falling2727 . Antero-Jacquemin JS, Santos P, Garcia PA, Dias RC, Dias JMDD. Comparação da função muscular isocinética dos membros inferiores entre idosos caidores e não caidores. Fisioter Pesq. 2012;19(1):32-8.. Pisciottano et al.1313 . Pisciottano MV, Pinto SS, Szejnfeld VL, Castro CH. The relationship between lean mass, muscle strength and physical ability in independent healthy elderly women from the community. J Nutr Health Aging. 2014;18(5):554-8. observed that the 1-unit increase in the torque peak of knee extensors was associated with a 0.01-second improvement in individual capacities in TUG. However, unlike this study, some others pointed out that muscle power explained, in a more consistent way than muscle strength, the variation in functional limitations in relatively more intense tasks1111 . Crockett K, Ardell K, Hermanson M, Penner A, Lanovaz J, Farthing J, et al. The relationship of knee-extensor strength and rate of torque development to sit-to-stand performance in older adults. Physiother Can. 2013;65(3):229-35. 2525 . Puthoff ML, Nielsen DH. Relationships among impairments in lower-extremity strength and power, functional limitations, and disability in older adults. Phys Ther. 2007;87(10):1334-47., a fact which has been linked to reduced nerve impulses, to the fact that elderly people are not very familiarized with knee extension in isokinetic dynamometers1111 . Crockett K, Ardell K, Hermanson M, Penner A, Lanovaz J, Farthing J, et al. The relationship of knee-extensor strength and rate of torque development to sit-to-stand performance in older adults. Physiother Can. 2013;65(3):229-35., and to the more dynamic and dependent characteristics, regarding both the force production and the contraction speed in those daily activities2525 . Puthoff ML, Nielsen DH. Relationships among impairments in lower-extremity strength and power, functional limitations, and disability in older adults. Phys Ther. 2007;87(10):1334-47. 2525 . Puthoff ML, Nielsen DH. Relationships among impairments in lower-extremity strength and power, functional limitations, and disability in older adults. Phys Ther. 2007;87(10):1334-47..

Muscle mass was not found to be correlated with functional ability, and it was found to have a low positive correlation with the average power of knee extensors and negative correlations with the remaining muscle performance variables in elderly women. Such results corroborate the results from Hairi et al.4. Hairi NN, Cumming RG, Naganathan V, Handelsman DJ, Le Couteur DG, Creasey H, et al. Loss of muscle strength, mass (sarcopenia), and quality (specific force) and its relationship with functional limitation and physical disability: the Concord Health and Ageing in Men Project. J Am Geriatr Soc. 2010;58(11):2055-62., who also found an association between the quadriceps muscle strength and functional limitation, and no relationship between the latter and muscle mass, which suggests that muscle strength would be the factor which could best determine the limitations in activities regarding walking, standing up, and sitting down. Conversely, some authors5. Janssen I, Steven B, Heymsfield M, Robert R. Low Relative Skeletal Muscle mass (sarcopenia) in older persons is associated with functional impairment and physical disability. J Am Geriatric Soc. 2002;50:889-96. 6. Janssen I, Baumgartner RN, Ross R, Rosenberg IH, Roubenoff R. Skeletal muscle cutpoints associated with elevated physical disability risk in older men and women. Am J Epidemiol. 2004;159(4):413-21. 2828 . Shin H, Panton LB, Dutton GR, Ilich JZ. Relationship of Physical Performance with Body Composition and Bone Mineral Density in Individuals over 60 Years of Age: A Systematic Review. J Aging Res. 2011;23:1-14. 3131 . Taekema DG, Gussekloo J, Maier AB, Westendorp RG, de Craen AJ. Handgrip strength as a predictor of functional, psychological and social health. A prospective population-based study among the oldest old. Age Ageing. 2010;39(3):331-7. pointed out that higher muscle mass influenced better physical performances2828 . Shin H, Panton LB, Dutton GR, Ilich JZ. Relationship of Physical Performance with Body Composition and Bone Mineral Density in Individuals over 60 Years of Age: A Systematic Review. J Aging Res. 2011;23:1-14. and that low lean mass was related to functional disability5. Janssen I, Steven B, Heymsfield M, Robert R. Low Relative Skeletal Muscle mass (sarcopenia) in older persons is associated with functional impairment and physical disability. J Am Geriatric Soc. 2002;50:889-96. 6. Janssen I, Baumgartner RN, Ross R, Rosenberg IH, Roubenoff R. Skeletal muscle cutpoints associated with elevated physical disability risk in older men and women. Am J Epidemiol. 2004;159(4):413-21., dependency in daily activities,3131 . Taekema DG, Gussekloo J, Maier AB, Westendorp RG, de Craen AJ. Handgrip strength as a predictor of functional, psychological and social health. A prospective population-based study among the oldest old. Age Ageing. 2010;39(3):331-7. and decreased mobility3030 . Launer LJ, Harris T, Rumpel C, Madans J. Body mass index, weight change, and risk of mobility disability in middle-aged and older women. The epidemiologic follow-up study of NHANES I. JAMA. 1994;271(14):1093-8.. However, in the physiological aging process, decreased muscle mass may not play a significant role in the diminished functional ability and muscle performance, as that reduction in performance is due to multiple factors9. Patil R, Uusi-Rasi K, Pasanen M, Kannus P, Karinkanta S, Sievanen H. Sarcopenia and osteopenia among 70-80-year-old home-dwelling Finnish women: prevalence and association with functional performance. Osteoporos Int. 2013;24(3):787-96.. The decline in muscle strength may be more related to neural alterations, which are more characterized by the increased co-activation of antagonist muscles, and reduced recruitment speed and synchronization of motor unit activation than by the hypotrophy of muscle fibers, which may significantly contribute to functional alterations1111 . Crockett K, Ardell K, Hermanson M, Penner A, Lanovaz J, Farthing J, et al. The relationship of knee-extensor strength and rate of torque development to sit-to-stand performance in older adults. Physiother Can. 2013;65(3):229-35.. Those results reinforce the idea that the isolated use of muscle mass as a criterion to define sarcopenia may not be adequate for all age ranges, taking into account that, in the elderly, the relationship between muscle mass and physical-functional ability has not shown to be linear1313 . Pisciottano MV, Pinto SS, Szejnfeld VL, Castro CH. The relationship between lean mass, muscle strength and physical ability in independent healthy elderly women from the community. J Nutr Health Aging. 2014;18(5):554-8..

Other studies have mentioned that the absent correlation between mass and muscle performance in the elderly may be explained through the altered muscle quality3232 . Newman AB, Haggerty CL, Goodpaster B, Harris T, Kritchevsky S, Nevitt M, et al. Strength and muscle quality in a well-functioning cohort of older adults: the Health, Aging and Body Composition Study. J Am Geriatr Soc. 2003;51(3):323-30., as defined by the functional application of muscle strength in relation to the muscle mass amount3333 . Barbat-Artigas S, Rolland Y, Zamboni M, Aubertin-Leheudre M. How to assess functional status: a new muscle quality index. J Nutr Health Aging. 2012;16(1):67-77., with the decreased strength occurring first, and in a quicker fashion as compared to the decreased mass1010 . Goodpaster BH, Park SW, Harris TB, Kritchevsky SB, Nevitt M, Schwartz AV, et al. The loss of skeletal muscle strength, mass, and quality in older adults: the health, aging and body composition study. J Gerontol A Biol Sci Med Sci. 2006;61(10):1059-64.. That phenomenon may have taken place in this study sample that comprised more active, younger, and non-sarcopenic elderly women, for whom the onset of the muscle performance physiological decline is not necessarily being accompanied by diminished muscle mass. Contributing to this analysis in this study, unlike the remaining main variables (functional ability and muscle strength), the muscle mass measurement was not related to the subjects' physical activity levels. Furthermore, the literature points towards a strong association between a lower muscle quality and higher functional limitations in daily activities4. Hairi NN, Cumming RG, Naganathan V, Handelsman DJ, Le Couteur DG, Creasey H, et al. Loss of muscle strength, mass (sarcopenia), and quality (specific force) and its relationship with functional limitation and physical disability: the Concord Health and Ageing in Men Project. J Am Geriatr Soc. 2010;58(11):2055-62., reduced walking speed, balance deficit2929 . Villareal DT, Banks M, Siener C, Sinacore DR, Klein S. Physical frailty and body composition in obese elderly men and women. Obes Res. 2004;12(6):913-20., and decreased muscle performance2. Vilaca KH, Alves NM, Carneiro JA, Ferriolli E, Lima NK, Moriguti JC. Body composition, muscle strength and quality of active elderly women according to the distance covered in the 6-minute walk test. Braz J Phys Ther. 2013;17(3):289-96. 3. Rikkonen T, Sirola J, Salovaara K, Tuppurainen M, Jurvelin JS, Honkanen R, et al. Muscle strength and body composition are clinical indicators of osteoporosis. Calcif Tissue Int. 2012;91(2):131-8.. Also, considering that most elderly women in this study were found to be overweight, the reduced muscle quality may also be a consequence of the altered body composition that arises from the increased fat-free mass2. Vilaca KH, Alves NM, Carneiro JA, Ferriolli E, Lima NK, Moriguti JC. Body composition, muscle strength and quality of active elderly women according to the distance covered in the 6-minute walk test. Braz J Phys Ther. 2013;17(3):289-96. 2929 . Villareal DT, Banks M, Siener C, Sinacore DR, Klein S. Physical frailty and body composition in obese elderly men and women. Obes Res. 2004;12(6):913-20. and through the infiltration of fat into the muscles3434 . Visser M, Goodpaster BH, Kritchevsky SB, Newman AB, Nevitt M, Rubin SM, et al. Muscle mass, muscle strength, and muscle fat infiltration as predictors of incident mobility limitations in well-functioning older persons. J Gerontol A Biol Sci Med Sci. 2005;60(3):324-33..

The sample was not calculated in this study, nor was the intake of water, alcohol, or coffee was controlled, and the emptying of bladders were not supervised either before the body impedance tests were taken. Such limitations hinder the internal validity of the study; however, the findings regarding significant positive and moderate correlations among bioimpedance and lean mass measurements that were obtained through the thickness of skin folds showed how reliable the body impedance evaluation and the SMMI calculation were. In order to improve the robustness of results, future studies are recommended to separate samples by age ranges, before correlation analyses can be conducted.

Thus, taking into account that no linear relationships were found among muscle mass and applied functional tests, the muscle performance of knee extensors and flexors seems to have a more important role than muscle mass by itself1313 . Pisciottano MV, Pinto SS, Szejnfeld VL, Castro CH. The relationship between lean mass, muscle strength and physical ability in independent healthy elderly women from the community. J Nutr Health Aging. 2014;18(5):554-8. for the preservation of abilities regarding walking, standing up, or sitting down4. Hairi NN, Cumming RG, Naganathan V, Handelsman DJ, Le Couteur DG, Creasey H, et al. Loss of muscle strength, mass (sarcopenia), and quality (specific force) and its relationship with functional limitation and physical disability: the Concord Health and Ageing in Men Project. J Am Geriatr Soc. 2010;58(11):2055-62., for elderly women with low BMDs. Therefore, the muscle performance is suggested to be the parameter that is prioritized in the clinical practice for the investigation of functional limitations in elderly women, once the use of muscle mass as the only parameter may not be the most adequate way to define sarcopenia. Considering the correlation among the isokinetic variables and the TUG and CST tests, and the quicker, easier, and more inexpensive application of functional ability measurements may enable tracing the physical-functional risks that are related to sarcopenia.

CONCLUSION

In conclusion, the association between functional ability and muscle performance was the only one observed, and its relationship with muscle mass was not found to be true. The latter, in turn, was found to be inversely related to muscle strength. Those findings reinforce how unreliable it is to use muscle mass as the single measurement for the identification of sarcopenia.

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  • 2
    A study developed in the Movement Laboratory of Universidade de Brasília (UnB) - Brasília (DF), Brasil.

Publication Dates

  • Publication in this collection
    Apr-Jun 2015

History

  • Received
    Mar 2014
  • Accepted
    May 2015
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