Neuromuscular component of muscle quality assessment in older adults: narrative review

Authors

DOI:

https://doi.org/10.52165/kinsi.30.1.95-111

Keywords:

ageing, skeletal muscle, ultrasound sarcopenia index, phase angle, muscle quality index

Abstract

The concept of muscle quality encompasses both micro- and macroscopic aspects of muscle architecture and composition and has gained increasing attention with inclusion in the definition of sarcopenia, indicating the significance of muscle quality in evaluating muscle function and strength among older individuals. Muscle quality consists of two main components: neuromuscular and morphological and is often defined as the ratio between the two. The aim of this review is to present currently used methods for assessment of muscle quality with an emphasis on neuromuscular component in older adults. The most used methods for assessing morphological component are imaging techniques, such as magnetic resonance imaging, computed tomography, dual-energy X-ray absorptiometry and non-imaging bioimpedance analysis. In the neuromuscular component upper and lower body strength are assessed with different methods such as hand grip strength, isokinetic lower limb strength and isometric lower limb strength. Currently, there are three proposed muscle quality assessment methods for field or population studies: muscle quality index, ultrasound sarcopenia index and bioimpedance-derived phase angle. Despite the exploration of muscle quality through various assessment methods, a consensus on the most appropriate and universally applicable approach has yet to be established.

Downloads

Download data is not yet available.

References

Akamatsu, Y., Kusakabe, T., Arai, H., Yamamoto, Y., Nakao, K., Ikeue, K., Ishihara, Y., Tagami, T., Yasoda, A., Ishii, K., & Satoh-Asahara, N. (2022). Phase angle from bioelectrical impedance analysis is a useful indicator of muscle quality. Journal of Cachexia, Sarcopenia and Muscle, 13(1), 180–189. https://doi.org/10.1002/jcsm.12860

Albano, D., Messina, C., Vitale, J., & Sconfienza, L. M. (2020). Imaging of sarcopenia: old evidence and new insights. European Radiology, 30(4), 2199–2208. https://doi.org/10.1007/s00330-019-06573-2

Andreoli, A., Scalzo, G., Masala, S., Tarantino, U., & Guglielmi, G. (2009). Body composition assessment by dual-energy X-ray absorptiometry (DXA). La Radiologia Medica, 114(2), 286–300. https://doi.org/10.1007/s11547-009-0369-7

Barahona-Fuentes, G., Huerta Ojeda, Á., Romero, G. L., Delgado-Floody, P., Jerez-Mayorga, D., Yeomans-Cabrera, M.-M., & Chirosa-Ríos, L. J. (2023). Muscle Quality Index is inversely associated with psychosocial variables among Chilean adolescents. BMC Public Health, 23(1), 2104. https://doi.org/10.1186/s12889-023-16978-w

Barbat-Artigas, S., Rolland, Y., Vellas, B., & Aubertin-Leheudre, M. (2013). Muscle quantity is not synonymous with muscle quality. Journal of the American Medical Directors Association, 14(11), 852.e1-852.e7. https://doi.org/10.1016/j.jamda.2013.06.003

Barbat-Artigas, S., Rolland, Y., Zamboni, M., & Aubertin-Leheudre, M. (2012). How to assess functional status: a new muscle quality index. The Journal of Nutrition, Health & Aging, 16(1), 67–77.

Bazzocchi, A., Ponti, F., Albisinni, U., Battista, G., & Guglielmi, G. (2016). DXA: Technical aspects and application. European Journal of Radiology, 85(8), 1481–1492. https://doi.org/10.1016/j.ejrad.2016.04.004

Beaudart, C., Rolland, Y., Cruz-Jentoft, A. J., Bauer, J. M., Sieber, C., Cooper, C., Al-Daghri, N., Araujo de Carvalho, I., Bautmans, I., Bernabei, R., Bruyère, O., Cesari, M., Cherubini, A., Dawson-Hughes, B., Kanis, J. A., Kaufman, J.-M., Landi, F., Maggi, S., McCloskey, E., … Fielding, R. A. (2019). Assessment of Muscle Function and Physical Performance in Daily Clinical Practice. Calcified Tissue International, 105(1), 1–14. https://doi.org/10.1007/s00223-019-00545-w

Bohannon, R. W., Bubela, D. J., Magasi, S. R., Wang, Y. C., & Gershon, R. C. (2010). Sit-to-stand test: Performance and determinants across the age-span. Isokinetics and Exercise Science, 18(4), 235–240. https://doi.org/10.3233/IES-2010-0389

Borga, M., West, J., Bell, J. D., Harvey, N. C., Romu, T., Heymsfield, S. B., & Leinhard, O. D. (2018). Advanced body composition assessment: From body mass index to body composition profiling. In Journal of Investigative Medicine (Vol. 66, Issue 5, pp. 887–895). BMJ Publishing Group. https://doi.org/10.1136/jim-2018-000722

Brown, W. F., Strong, M. J., & Snow, R. (1988). Methods for estimating numbers of motor units in biceps‐brachialis muscles and losses of motor units with aging. Muscle & Nerve, 11(5), 423–432. https://doi.org/10.1002/mus.880110503

Buckinx, F., & Aubertin-Leheudre, M. (2019). Relevance to assess and preserve muscle strength in aging field. In Progress in Neuro-Psychopharmacology and Biological Psychiatry (Vol. 94). Elsevier Inc. https://doi.org/10.1016/j.pnpbp.2019.109663

Buckinx, F., Croisier, J., Reginster, J., Dardenne, N., Beaudart, C., Slomian, J., Leonard, S., & Bruyère, O. (2017). Reliability of muscle strength measures obtained with a hand‐held dynamometer in an elderly population. Clinical Physiology and Functional Imaging, 37(3), 332–340. https://doi.org/10.1111/cpf.12300

Chan, O. Y. A., van Houwelingen, A. H., Gussekloo, J., Blom, J. W., & den Elzen, W. P. J. (2014). Comparison of quadriceps strength and handgrip strength in their association with health outcomes in older adults in primary care. AGE, 36(5), 9714. https://doi.org/10.1007/s11357-014-9714-4

Chen, L. K., Woo, J., Assantachai, P., Auyeung, T. W., Chou, M. Y., Iijima, K., Jang, H. C., Kang, L., Kim, M., Kim, S., Kojima, T., Kuzuya, M., Lee, J. S. W., Lee, S. Y., Lee, W. J., Lee, Y., Liang, C. K., Lim, J. Y., Lim, W. S., … Arai, H. (2020). Asian Working Group for Sarcopenia: 2019 Consensus Update on Sarcopenia Diagnosis and Treatment. Journal of the American Medical Directors Association, 21(3), 300–307. https://doi.org/10.1016/j.jamda.2019.12.012

Chianca, V., Albano, D., Messina, C., Gitto, S., Ruffo, G., Guarino, S., Del Grande, F., & Sconfienza, L. M. (2022). Sarcopenia: imaging assessment and clinical application. Abdominal Radiology, 47(9), 3205–3216. https://doi.org/10.1007/s00261-021-03294-3

Cooper, R., Hardy, R., Bann, D., Sayer, A. A., Ward, K. A., Adams, J. E., & Kuh, D. (2014). Body mass index from age 15 years onwards and muscle mass,strength, and quality in early old age: Findings from the MRC national survey of health and development. Journals of Gerontology - Series A Biological Sciences and Medical Sciences, 69(10), 1253–1259. https://doi.org/10.1093/gerona/glu039

Cruz-Jentoft, A. J., Bahat, G., Bauer, J., Boirie, Y., Bruyère, O., Cederholm, T., Cooper, C., Landi, F., Rolland, Y., Sayer, A. A., Schneider, S. M., Sieber, C. C., Topinkova, E., Vandewoude, M., Visser, M., Zamboni, M., Bautmans, I., Baeyens, J. P., Cesari, M., … Schols, J. (2019). Sarcopenia: Revised European consensus on definition and diagnosis. Age and Ageing, 48(1), 16–31. https://doi.org/10.1093/ageing/afy169

de Lucena Alves, C. P., de Almeida, S. B., Lima, D. P., Neto, P. B., Miranda, A. L., Manini, T., Vlietstra, L., Waters, D. L., Bielemann, R. M., Correa-de-Araujo, R., Fayh, A. P., & Costa, E. C. (2023). Muscle Quality in Older Adults: A Scoping Review. Journal of the American Medical Directors Association, 24(4), 462-467.e12. https://doi.org/10.1016/j.jamda.2023.02.012

De Melo, T. A., Duarte, A. C. M., Bezerra, T. S., França, F., Soares, N. S., & Brito, D. (2019). The five times sit-to-stand test: Safety and reliability with older intensive care unit patients at discharge. Revista Brasileira de Terapia Intensiva, 31(1), 27–33. https://doi.org/10.5935/0103-507X.20190006

de Sousa Neto, I. V., Diniz, J. de S., Alves, V. P., Oliveira, A. R. V., de Souza Barbosa, M. P., da Silva Prado, C. R., Alencar, J. A., Vilaça E Silva, K. H. C., Silva, C. R., Ferreira, G. M. L., Garcia, D., Prestes, R. A. G. J., Melo, G. L. R., Burmann, L. L., Giuliani, F. N. G., Beal, F. L. R., Severiano, A. P., & da Cunha Nascimento, D. (2023). Field-Based Estimates of Muscle Quality Index Determine Timed-Up-and-Go Test Performance in Obese Older Women. Clinical Interventions in Aging, 18, 293–303. https://doi.org/10.2147/CIA.S399827

Dehghan, M., & Merchant, A. T. (2008). Is bioelectrical impedance accurate for use in large epidemiological studies? In Nutrition Journal (Vol. 7, Issue 1). https://doi.org/10.1186/1475-2891-7-26

Di Vincenzo, O., Marra, M., Di Gregorio, A., Pasanisi, F., & Scalfi, L. (2021). Bioelectrical impedance analysis (BIA) -derived phase angle in sarcopenia: A systematic review. Clinical Nutrition, 40(5), 3052–3061. https://doi.org/10.1016/j.clnu.2020.10.048

Distefano, G., Standley, R. A., Zhang, X., Carnero, E. A., Yi, F., Cornnell, H. H., & Coen, P. M. (2018). Physical activity unveils the relationship between mitochondrial energetics, muscle quality, and physical function in older adults. Journal of Cachexia, Sarcopenia and Muscle, 9(2), 279–294. https://doi.org/10.1002/jcsm.12272

Doherty, T. J., & Brown, W. F. (1993). The estimated numbers and relative sizes of thenar motor units as selected by multiple point stimulation in young and older adults. Muscle & Nerve, 16(4), 355–366. https://doi.org/10.1002/mus.880160404

Fragala, M. S., Kenny, A. M., & Kuchel, G. A. (2015). Muscle Quality in Aging: a Multi-Dimensional Approach to Muscle Functioning with Applications for Treatment. In Sports Medicine (Vol. 45, Issue 5, pp. 641–658). Springer International Publishing. https://doi.org/10.1007/s40279-015-0305-z

Francis, P., Toomey, C., Mc Cormack, W., Lyons, M., & Jakeman, P. (2017). Measurement of maximal isometric torque and muscle quality of the knee extensors and flexors in healthy 50‐ to 70‐year‐old women. Clinical Physiology and Functional Imaging, 37(4), 448–455. https://doi.org/10.1111/cpf.12332

Giraudo, C., Cavaliere, A., Lupi, A., Guglielmi, G., & Quaia, E. (2020). Established paths and new avenues: A review of the main radiological techniques for investigating sarcopenia. Quantitative Imaging in Medicine and Surgery, 10(8), 1602–1613. https://doi.org/10.21037/QIMS.2019.12.15

Goodpaster, B. H., Park, S. W., Harris, T. B., Kritchevsky, S. B., Nevitt, M., Schwartz, A. V, Simonsick, E. M., Tylavsky, F. A., Visser, M., & Newman, A. B. (2006). The Loss of Skeletal Muscle Strength, Mass, and Quality in Older Adults: The Health, Aging and Body Composition Study. http://biomedgerontology.oxfordjournals.org/

Hamrick, M. W., McGee-Lawrence, M. E., & Frechette, D. M. (2016). Fatty Infiltration of Skeletal Muscle: Mechanisms and Comparisons with Bone Marrow Adiposity. Frontiers in Endocrinology, 7. https://doi.org/10.3389/fendo.2016.00069

Harris-Love, M., Benson, K., Leasure, E., Adams, B., & McIntosh, V. (2018). The Influence of Upper and Lower Extremity Strength on Performance-Based Sarcopenia Assessment Tests. Journal of Functional Morphology and Kinesiology, 3(4), 53. https://doi.org/10.3390/jfmk3040053

Heymsfield, S. B., Gonzalez, M. C., Lu, J., Jia, G., & Zheng, J. (2015). Skeletal muscle mass and quality: Evolution of modern measurement concepts in the context of sarcopenia. Proceedings of the Nutrition Society, 74(4), 355–366. https://doi.org/10.1017/S0029665115000129

Hilton, T. N., Tuttle, L. J., Bohnert, K. L., Mueller, M. J., & Sinacore, D. R. (2008). Excessive adipose tissue infiltration in skeletal muscle in individuals with obesity, diabetes mellitus, and peripheral neuropathy: Association with performance and function. Physical Therapy, 88(11), 1336–1344. https://doi.org/10.2522/ptj.20080079

Hortobágyi, T., Vetrovsky, T., Brach, J. S., van Haren, M., Volesky, K., Radaelli, R., Lopez, P., & Granacher, U. (2023). Effects of Exercise Training on Muscle Quality in Older Individuals: A Systematic Scoping Review with Meta-Analyses. In Sports Medicine - Open (Vol. 9, Issue 1). Springer Science and Business Media Deutschland GmbH. https://doi.org/10.1186/s40798-023-00585-5

Huber, F. A., Del Grande, F., Rizzo, S., Guglielmi, G., & Guggenberger, R. (2020). MRI in the assessment of adipose tissues and muscle composition: How to use it. In Quantitative Imaging in Medicine and Surgery (Vol. 10, Issue 8, pp. 1636–1649). AME Publishing Company. https://doi.org/10.21037/QIMS.2020.02.06

Hughes, V. A., Frontera, W. R., Wood, M., Evans, W. J., Dallal, G. E., Roubenoff, R., & Singh, M. A. F. (2001). Longitudinal Muscle Strength Changes in Older Adults: Influence of Muscle Mass, Physical Activity, and Health. In Journal of Gerontology: BIOLOGICAL SCIENCES Copyright (Vol. 56, Issue 5). http://biomedgerontology.oxfordjournals.org/

Jerez-Mayorga, D., Chirosa Ríos, L. J., Reyes, A., Delgado-Floody, P., Machado Payer, R., & Guisado Requena, I. M. (2019). Muscle quality index and isometric strength in older adults with hip osteoarthritis. PeerJ, 7, e7471. https://doi.org/10.7717/peerj.7471

Jiang, Z., Marriott, K., & Maly, M. R. (2019). Impact of Inter-and Intramuscular Fat on Muscle Architecture and Capacity. Critical Reviews in Biomedical Engineering, 47(6), 515–533. www.begellhouse.com

Keating, J. L., & Matyas, T. A. (1996). The Influence of Subject and Test Design on Dynamometric Measurements of Extremity Muscles. Physical Therapy, 76(8), 866–889. https://doi.org/10.1093/ptj/76.8.866a

Kilic, M. K., Kizilarslanoglu, M. C., Arik, G., Bolayir, B., Kara, O., Dogan Varan, H., Sumer, F., Kuyumcu, M. E., Halil, M., & Ulger, Z. (2017). Association of Bioelectrical Impedance Analysis–Derived Phase Angle and Sarcopenia in Older Adults. Nutrition in Clinical Practice, 32(1), 103–109. https://doi.org/10.1177/0884533616664503

Kuno, S., Katsuta, S., Inouye, T., Anno, I., Matsumoto, K., & Akisada, M. (1988). Relationship between MR relaxation time and muscle fiber composition. Radiology, 169(2), 567–568. https://doi.org/10.1148/radiology.169.2.3175009

Kuschel, L. B., Sonnenburg, D., & Engel, T. (2022). Factors of Muscle Quality and Determinants of Muscle Strength: A Systematic Literature Review. Healthcare (Switzerland), 10(10). https://doi.org/10.3390/healthcare10101937

Kyle, U., Bosaues, I., De Lorenzo, A., Deurenberg, P., Elia, M., & Gomez, J. (2004). Bioelectrical impedance analysis?part I: review of principles and methods. Clinical Nutrition, 23(5), 1226–1243. https://doi.org/10.1016/j.clnu.2004.06.004

Leblanc, A., Taylor, B. A., Thompson, P. D., Capizzi, J. A., Clarkson, P. M., Michael White, C., & Pescatello, L. S. (2015). Relationships between physical activity and muscular strength among healthy adults across the lifespan. SpringerPlus, 4(1). https://doi.org/10.1186/s40064-015-1357-0

Lenchik, L., & Boutin, R. D. (2018). Sarcopenia: Beyond Muscle Atrophy and into the New Frontiers of Opportunistic Imaging, Precision Medicine, and Machine Learning. Seminars in Musculoskeletal Radiology, 22(3), 307–322. https://doi.org/10.1055/s-0038-1641573

Leong, D. P., Teo, K. K., Rangarajan, S., Lopez-Jaramillo, P., Avezum, A., Orlandini, A., Seron, P., Ahmed, S. H., Rosengren, A., Kelishadi, R., Rahman, O., Swaminathan, S., Iqbal, R., Gupta, R., Lear, S. A., Oguz, A., Yusoff, K., Zatonska, K., Chifamba, J., … Yusuf, S. (2015). Prognostic value of grip strength: findings from the Prospective Urban Rural Epidemiology (PURE) study. The Lancet, 386(9990), 266–273. https://doi.org/10.1016/S0140-6736(14)62000-6

Lord, S. R., Murray, S. M., Chapman, K., Munro, B., & Tiedemann, A. (2002). Sit-to-Stand Performance Depends on Sensation, Speed, Balance, and Psychological Status in Addition to Strength in Older People. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences, 57(8), M539–M543. https://doi.org/10.1093/gerona/57.8.M539

Lustgarten, M. S., & Fielding, R. A. (2011). Assessment of analytical methods used to measure changes in body composition in the elderly and recommendations for their use in phase II clinical trials. The Journal of Nutrition, Health & Aging, 15(5), 368–375. https://doi.org/10.1007/s12603-011-0049-x

Lynch, N. A., Metter, E. J., Lindle, R. S., Fozard, J. L., Tobin, J. D., Roy, T. A., Fleg, J. L., & Hurley, B. F. (1999). Muscle quality. I. Age-associated differences between arm and leg muscle groups. Journal of Applied Physiology, 188–194. https://doi.org/https://doi.org/10.1152/jappl.1999.86.1.188

Marusic, U., Narici, M., Simunic, B., Pisot, R., & Ritzmann, R. (2021). Nonuniform loss of muscle strength and atrophy during bed rest: a systematic review. Journal of Applied Physiology, 131(1), 194–206. https://doi.org/10.1152/japplphysiol.00363.2020

McKinnon, N. B., Connelly, D. M., Rice, C. L., Hunter, S. W., & Doherty, T. J. (2017). Neuromuscular contributions to the age-related reduction in muscle power: Mechanisms and potential role of high velocity power training. Ageing Research Reviews, 35, 147–154. https://doi.org/10.1016/j.arr.2016.09.003

McKinnon, N. B., Montero-Odasso, M., & Doherty, T. J. (2015). Motor unit loss is accompanied by decreased peak muscle power in the lower limb of older adults. Experimental Gerontology, 70, 111–118. https://doi.org/10.1016/j.exger.2015.07.007

Metter, E. J., Conwit, R., Tobin, J., & Fozard, J. L. (1997). Age-Associated Loss of Power and Strength in the Upper Extremities in Women and Men. Journal of Gerontology: BIOLOGICAL SCIENCES, 52(5). https://academic.oup.com/biomedgerontology/article/52A/5/B267/617501

Minetto, M. A., Busso, C., Gamerro, G., Lalli, P., Massazza, G., & Invernizzi, M. (2021). Quantitative assessment of volumetric muscle loss: Dual-energy X-ray absorptiometry and ultrasonography. In Current Opinion in Pharmacology (Vol. 57, pp. 148–156). Elsevier Ltd. https://doi.org/10.1016/j.coph.2021.02.002

Misic, M. M., Rosengren, K. S., Woods, J. A., & Evans, E. M. (2007). Muscle Quality, Aerobic Fitness and Fat Mass Predict Lower-Extremity Physical Function in Community-Dwelling Older Adults. Gerontology, 53(5), 260–266. https://doi.org/10.1159/000101826

Moore, A. Z., Caturegli, G., Metter, E. J., Makrogiannis, S., Resnick, S. M., Harris, T. B., & Ferrucci, L. (2014). Difference in muscle quality over the adult life span and biological correlates in the baltimore longitudinal study of aging. Journal of the American Geriatrics Society, 62(2), 230–236. https://doi.org/10.1111/jgs.12653

Naimo, M. A., Varanoske, A. N., Hughes, J. M., & Pasiakos, S. M. (2021). Skeletal Muscle Quality: A Biomarker for Assessing Physical Performance Capabilities in Young Populations. In Frontiers in Physiology (Vol. 12). Frontiers Media S.A. https://doi.org/10.3389/fphys.2021.706699

Narici, M., McPhee, J., Conte, M., Franchi, M. V., Mitchell, K., Tagliaferri, S., Monti, E., Marcolin, G., Atherton, P. J., Smith, K., Phillips, B., Lund, J., Franceschi, C., Maggio, M., & Butler-Browne, G. S. (2021). Age-related alterations in muscle architecture are a signature of sarcopenia: the ultrasound sarcopenia index. Journal of Cachexia, Sarcopenia and Muscle, 12(4), 973–982. https://doi.org/10.1002/jcsm.12720

Newman, A. B., Haggerty, C. L., Goodpaster, B., Harris, T., Kritchevsky, S., Nevitt, M., Miles, T. P., & Visser, M. (2003). Strength and Muscle Quality in a Well-Functioning Cohort of Older Adults: The Health, Aging and Body Composition Study. In J Am Geriatr Soc (Vol. 51).

Nordez, A., Jolivet, E., Südhoff, I., Bonneau, D., de Guise, J. A., & Skalli, W. (2009). Comparison of methods to assess quadriceps muscle volume using magnetic resonance imaging. Journal of Magnetic Resonance Imaging, 30(5), 1116–1123. https://doi.org/10.1002/jmri.21867

Norman, K., Wirth, R., Neubauer, M., Eckardt, R., & Stobäus, N. (2015). The Bioimpedance Phase Angle Predicts Low Muscle Strength, Impaired Quality of Life, and Increased Mortality in Old Patients With Cancer. Journal of the American Medical Directors Association, 16(2), 173.e17-173.e22. https://doi.org/10.1016/j.jamda.2014.10.024

Nowicka, M., Górska, M., Edyko, K., Szklarek-Kubicka, M., Kazanek, A., Prylińska, M., Niewodniczy, M., Kostka, T., & Kurnatowska, I. (2022). Association of Physical Performance, Muscle Strength and Body Composition with Self-Assessed Quality of Life in Hemodialyzed Patients: A Cross-Sectional Study. Journal of Clinical Medicine, 11(9), 2283. https://doi.org/10.3390/jcm11092283

Overend, T. J., Cunningham, D. A., Paterson, D. H., & Lefcoe, M. S. (1992). Thigh composition in young and elderly men determined by computed tomography. Clinical Physiology, 12(6), 629–640. https://doi.org/10.1111/j.1475-097X.1992.tb00366.x

Pišot, R., Narici, M. V., Šimunič, B., De Boer, M., Seynnes, O., Jurdana, M., Biolo, G., & Mekjavič, I. B. (2008). Whole muscle contractile parameters and thickness loss during 35-day bed rest. European Journal of Applied Physiology, 104(2), 409–414. https://doi.org/10.1007/s00421-008-0698-6

Ploutz-Snyder, L. L., Manini, T., Ploutz-Snyder, R. J., & Wolf, D. A. (2002). Functionally Relevant Thresholds of Quadriceps Femoris Strength. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences, 57(4), B144–B152. https://doi.org/10.1093/gerona/57.4.B144

Pons, C., Borotikar, B., Garetier, M., Burdin, V., Salem, D. Ben, Lempereur, M., & Brochard, S. (2018). Quantifying skeletal muscle volume and shape in humans using MRI: A systematic review of validity and reliability. PLoS ONE, 13(11). https://doi.org/10.1371/journal.pone.0207847

Power, G. A., Dalton, B. H., Behm, D. G., Vandervoort, A. A., Doherty, T. J., & Rice, C. L. (2010). Motor Unit Number Estimates in Masters Runners. Medicine & Science in Sports & Exercise, 42(9), 1644–1650. https://doi.org/10.1249/MSS.0b013e3181d6f9e9

Pus, K., Paravlic, A. H., & Šimunič, B. (2023). The use of tensiomyography in older adults: a systematic review. Frontiers in Physiology, 14. https://doi.org/10.3389/fphys.2023.1213993

Radaelli, R., Botton, C. E., Wilhelm, E. N., Bottaro, M., Lacerda, F., Gaya, A., Moraes, K., Peruzzolo, A., Brown, L. E., & Pinto, R. S. (2013). Low- and high-volume strength training induces similar neuromuscular improvements in muscle quality in elderly women. Experimental Gerontology, 48(8), 710–716. https://doi.org/10.1016/j.exger.2013.04.003

Radaelli, R., Taaffe, D. R., Newton, R. U., Galvão, D. A., & Lopez, P. (2021). Exercise effects on muscle quality in older adults: a systematic review and meta-analysis. Scientific Reports, 11(1). https://doi.org/10.1038/s41598-021-00600-3

Reed, R. L., Pearlmutter, L., Yochum, K., Meredith, K. E., & Mooradian, A. D. (1991). The Relationship between Muscle Mass and Muscle Strength in the Elderly. Journal of the American Geriatrics Society, 39(6), 555–561. https://doi.org/10.1111/j.1532-5415.1991.tb03592.x

Ribeiro, A. S., Picoloto, A., Nunes, J. P., Bezerra, E. S., Schoenfeld, B. J., & Cyrino, E. S. (2022). Effects of Different Resistance Training Loads on the Muscle Quality Index in Older Women. Journal of Strength and Conditioning Research, 36(5), 1445–1449. https://doi.org/10.1519/JSC.0000000000003667

Rice, C. L., Cunningham, D. A., Paterson, D. H., & Lefcoe, M. S. (1989). Arm and leg composition determined by computed tomography in young and elderly men. Clinical Physiology, 9(3), 207–220. https://doi.org/10.1111/j.1475-097X.1989.tb00973.x

Roman, W. J., Fleckenstein, J., Stray-Gundersen, J., Alway, S. E., Peshock, R., & Gonyea, W. J. (1993). Adaptations in the elbow flexors of elderly males after heavy-resistance training. Journal of Applied Physiology, 74(2), 750–754. https://doi.org/10.1152/jappl.1993.74.2.750

Ryan, A. S., Buscemi, A., Forrester, L., Hafer-Macko, C. E., & Ivey, F. M. (2011). Atrophy and intramuscular fat in specific muscles of the thigh: Associated weakness and hyperinsulinemia in stroke survivors. Neurorehabilitation and Neural Repair, 25(9), 865–872. https://doi.org/10.1177/1545968311408920

Saragat, B., Buffa, R., Mereu, E., De Rui, M., Coin, A., Sergi, G., & Marini, E. (2014). Specific bioelectrical impedance vector reference values for assessing body composition in the Italian elderly. Experimental Gerontology, 50, 52–56. https://doi.org/10.1016/j.exger.2013.11.016

Sardinha, L. B. (2018). Physiology of exercise and phase angle: another look at BIA. European Journal of Clinical Nutrition, 72(9), 1323–1327. https://doi.org/10.1038/s41430-018-0215-x

Schenkman, M., Hughes, M. A., Samsa, G., & Studenski, S. (1996). The Relative Importance of Strength and Balance in Chair Rise by Functionally Impaired Older Individuals. Journal of the American Geriatrics Society, 44(12), 1441–1446. https://doi.org/10.1111/j.1532-5415.1996.tb04068.x

Selberg, O., Burchert, W., Graubner, G., Wenner, C., Ehrenheim, C., & Müller, M. J. (1993). Determination of Anatomical Skeletal Muscle Mass by Whole Body Nuclear Magnetic Resonance. In Human Body Composition (pp. 95–97). Springer US. https://doi.org/10.1007/978-1-4899-1268-8_22

Sergi, G., De Rui, M., Veronese, N., Bolzetta, F., Berton, L., Carraro, S., Bano, G., Coin, A., Manzato, E., & Perissinotto, E. (2015). Assessing appendicular skeletal muscle mass with bioelectrical impedance analysis in free-living Caucasian older adults. Clinical Nutrition, 34(4), 667–673. https://doi.org/10.1016/j.clnu.2014.07.010

Sergi, G., Trevisan, C., Veronese, N., Lucato, P., & Manzato, E. (2016). Imaging of sarcopenia. European Journal of Radiology, 85(8), 1519–1524. https://doi.org/10.1016/j.ejrad.2016.04.009

Šimunič, B., Degens, H., Rittweger, J., Narici, M., Mekjavić, I. B., & Pišot, R. (2011). Noninvasive estimation of myosin heavy chain composition in human skeletal muscle. Medicine and Science in Sports and Exercise, 43(9), 1619–1625. https://doi.org/10.1249/mss.0b013e31821522d0

Šimunič, B., Koren, K., Rittweger, J., Lazzer, S., Reggiani, C., Rejc, E., Pišot, R., Narici, M., & Degens, H. (2019). Tensiomyography detects early hallmarks of bed-rest-induced atrophy before changes in muscle architecture. J Appl Physiol, 126, 815–822. https://doi.org/10.1152/japplphysiol.00880.2018.-In

Šimunič, B., Pišot, R., Rittweger, J., & Degens, H. (2018). Age-related slowing of contractile properties differs between power, endurance, and nonathletes: A tensiomyographic assessment. Journals of Gerontology - Series A Biological Sciences and Medical Sciences, 73(12), 1602–1608. https://doi.org/10.1093/gerona/gly069

Sjostrom, L., Kvist, H., Cederblad, A., & Tylen, U. (1986). Determination of total adipose tissue and body fat in women by computed tomography, 40K, and tritium. American Journal of Physiology-Endocrinology and Metabolism, 250(6), E736–E745. https://doi.org/10.1152/ajpendo.1986.250.6.E736

Skelton, D. A., Greig, C. A., Davies, J. M., & Young, A. (1994). Strength, Power and Related Functional Ability of Healthy People Aged 65-89 Years. In Age and Ageing (Vol. 23). http://ageing.oxfordjournals.org/

Steihaug, O. M., Gjesdal, C. G., Bogen, B., & Ranhoff, A. H. (2016). Identifying low muscle mass in patients with hip fracture: Validation of bioelectrical impedance analysis and anthropometry compared to dual energy X-ray absorptiometry. The Journal of Nutrition, Health & Aging, 20(7), 685–690. https://doi.org/10.1007/s12603-016-0686-1

Taaffe, D. R., Duret, C., Wheeler, S., & Marcus, R. (1999). Once-weekly resistance exercise improves muscle strength and neuromuscular performance in older adults. Journal of the American Geriatrics Society, 47(10), 1208–1214. https://doi.org/10.1111/j.1532-5415.1999.tb05201.x

Tognon, G., Malmros, V., Freyer, E., Bosaeus, I., & Mehlig, K. (2015). Are segmental MF-BIA scales able to reliably assess fat mass and lean soft tissue in an elderly Swedish population? Experimental Gerontology, 72, 239–243. https://doi.org/10.1016/j.exger.2015.10.004

Torriani, M., Townsend, E., Thomas, B. J., Bredella, M. A., Ghomi, R. H., & Tseng, B. S. (2012). Lower leg muscle involvement in Duchenne muscular dystrophy: An MR imaging and spectroscopy study. Skeletal Radiology, 41(4), 437–445. https://doi.org/10.1007/s00256-011-1240-1

Uemura, K., Yamada, M., & Okamoto, H. (2019). Association of bioimpedance phase angle and prospective falls in older adults. Geriatrics & Gerontology International, 19(6), 503–507. https://doi.org/10.1111/ggi.13651

van den Helder, J., Verreijen, A. M., van Dronkelaar, C., Memelink, R. G., Engberink, M. F., Engelbert, R. H. H., Weijs, P. J. M., & Tieland, M. (2022). Bio-Electrical Impedance Analysis: A Valid Assessment Tool for Diagnosis of Low Appendicular Lean Mass in Older Adults? Frontiers in Nutrition, 9. https://doi.org/10.3389/fnut.2022.874980

Watanabe, Y., Yamada, Y., Fukumoto, Y., Ishihara, T., Yokoyama, K., Yoshida, T., Miyake, M., Yamagata, E., & Kimura, M. (2013). Echo intensity obtained from ultrasonography images reflecting muscle strength in elderly men. Clinical Interventions in Aging, 8, 993–998. https://doi.org/10.2147/CIA.S47263

Wirth, R., Volkert, D., Rösler, A., Sieber, C. C., & Bauer, J. M. (2010). Bioelectric impedance phase angle is associated with hospital mortality of geriatric patients. Archives of Gerontology and Geriatrics, 51(3), 290–294. https://doi.org/10.1016/j.archger.2009.12.002

Yamada, Y., Buehring, B., Krueger, D., Anderson, R. M., Schoeller, D. A., & Binkley, N. (2016). Electrical Properties Assessed by Bioelectrical Impedance Spectroscopy as Biomarkers of Age-related Loss of Skeletal Muscle Quantity and Quality. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences, glw225. https://doi.org/10.1093/gerona/glw225

Published

2025-02-14

How to Cite

Puš, K., & Šimunič, B. (2025). Neuromuscular component of muscle quality assessment in older adults: narrative review. Kinesiologia Slovenica: Scientific Journal on Sport, 30(1), 95-111. https://doi.org/10.52165/kinsi.30.1.95-111