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Published in: BMC Musculoskeletal Disorders 1/2019

Open Access 01-12-2019 | Sarcopenia | Research article

Association of serum bone- and muscle-derived factors with age, sex, body composition, and physical function in community-dwelling middle-aged and elderly adults: a cross-sectional study

Authors: Kenta Moriwaki, Hiromi Matsumoto, Shinji Tanishima, Chika Tanimura, Mari Osaki, Hideki Nagashima, Hiroshi Hagino

Published in: BMC Musculoskeletal Disorders | Issue 1/2019

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Abstract

Background

Understanding interactions between bone and muscle based on endocrine factors may help elucidate the relationship between osteoporosis and sarcopenia. However, whether the abundance or activity of these endocrine factors is affected by age and sex or whether these factors play a causal role in bone and muscle formation and function is unclear. We aimed to evaluate the association of serum bone- and muscle-derived factors with age, sex, body composition, and physical function in community-dwelling middle-aged and elderly adults.

Methods

In all, 254 residents (97 men, 157 women) participated in this cross-sectional study conducted in Japan. The calcaneal speed of sound (SOS) was evaluated by quantitative ultrasound examination. Skeletal muscle mass index (SMI) was calculated by bioelectrical impedance analysis. Grip strength was measured using a dynamometer. Gait speed was measured by optical-sensitive gait analysis. Serum sclerostin, osteocalcin (OC), insulin-like growth factor-1 (IGF-1), myostatin, and tartrate-resistant acid phosphatase-5b (TRACP-5b) concentrations were measured simultaneously. The difference by sex was determined using t test. Correlations between serum bone- and muscle-derived factors and age, BMI, SOS, SMI, grip strength, gait speed, and TRACP-5b in men and women were determined based on Pearson’s correlation coefficients. Multiple regression analysis was performed using the stepwise method.

Results

There was no significant difference with regard to age between men (75.0 ± 8.9 years) and women (73.6 ± 8.1 years). Sclerostin was significantly higher in men than in women and tended to increase with age in men; it was significantly associated with SOS and TRACP-5b levels. OC was significantly higher in women than in men and was significantly associated with TRACP-5b levels and age. IGF-1 tended to decrease with age in both sexes and was significantly associated with SOS and body mass index. Myostatin did not correlate with any assessed variables.

Conclusions

Sclerostin was significantly associated with sex, age, and bone metabolism, although there was no discernable relationship between serum sclerostin levels and muscle function. There was no obvious relationship between OC and muscle parameters. This study suggests that IGF-1 is an important modulator of muscle mass and function and bone metabolism in community-dwelling middle-aged and elderly adults.
Literature
1.
go back to reference Lewiecki EM, Watts NB. New guidelines for the prevention and treatment of osteoporosis. South Med J. 2009;102:175–9.CrossRef Lewiecki EM, Watts NB. New guidelines for the prevention and treatment of osteoporosis. South Med J. 2009;102:175–9.CrossRef
2.
go back to reference Matsumoto H, Tanimura C, Tanishima S, Osaki M, Noma H, Hagino H. Sarcopenia is a risk factor for falling in independently living Japanese older adults: a 2-year prospective cohort study of the GAINA study. Geriatr Gerontol Int. 2017;17:2124–30.CrossRef Matsumoto H, Tanimura C, Tanishima S, Osaki M, Noma H, Hagino H. Sarcopenia is a risk factor for falling in independently living Japanese older adults: a 2-year prospective cohort study of the GAINA study. Geriatr Gerontol Int. 2017;17:2124–30.CrossRef
3.
go back to reference Miyakoshi N, Hongo M, Mizutani Y, Shimada Y. Prevalence of sarcopenia in Japanese women with osteopenia and osteoporosis. J Bone Miner Metab. 2013;31:556–61.CrossRef Miyakoshi N, Hongo M, Mizutani Y, Shimada Y. Prevalence of sarcopenia in Japanese women with osteopenia and osteoporosis. J Bone Miner Metab. 2013;31:556–61.CrossRef
4.
go back to reference Wu CH, Yang KC, Chang HH, Yen JF, Tsai KS, Huang KC. Sarcopenia is related to increased risk for low bone mineral density. J Clin Densitom. 2013;16:98–103.CrossRef Wu CH, Yang KC, Chang HH, Yen JF, Tsai KS, Huang KC. Sarcopenia is related to increased risk for low bone mineral density. J Clin Densitom. 2013;16:98–103.CrossRef
5.
go back to reference Morse A, McDonald MM, Kelly NH, Melville KM, Schindeler A, Kramer I, Kneissel M, van der Meulen MC, Little DG. Mechanical load increases in bone formation via a sclerostin-independent pathway. J Bone Miner Res. 2014;29:2456–67.CrossRef Morse A, McDonald MM, Kelly NH, Melville KM, Schindeler A, Kramer I, Kneissel M, van der Meulen MC, Little DG. Mechanical load increases in bone formation via a sclerostin-independent pathway. J Bone Miner Res. 2014;29:2456–67.CrossRef
6.
go back to reference Ke HZ, Richards WG, Li X, Ominsky MS. Sclerostin and Dickkopf-1 as therapeutic targets in bone diseases. Endocr Rev. 2012;33:747–83.CrossRef Ke HZ, Richards WG, Li X, Ominsky MS. Sclerostin and Dickkopf-1 as therapeutic targets in bone diseases. Endocr Rev. 2012;33:747–83.CrossRef
7.
go back to reference Amrein K, Amrein S, Drexler C, Dimai HP, Dobnig H, Pfeifer K, Tomaschitz A, Pieber TR, Fahrleitner-Pammer A. Sclerostin and its association with physical activity, age, gender, body composition, and bone mineral content in healthy adults. J Clin Endocrinol Metab. 2012;97:148–54.CrossRef Amrein K, Amrein S, Drexler C, Dimai HP, Dobnig H, Pfeifer K, Tomaschitz A, Pieber TR, Fahrleitner-Pammer A. Sclerostin and its association with physical activity, age, gender, body composition, and bone mineral content in healthy adults. J Clin Endocrinol Metab. 2012;97:148–54.CrossRef
8.
go back to reference Szulc P, Boutroy S, Vilayphiou N, Schoppet M, Rauner M, Chapurlat R, Hamann C, Hofbauer LC. Correlates of bone microarchitectural parameters and serum sclerostin levels in men: the STRAMBO study. J Bone Miner Res. 2013;28:1760–70.CrossRef Szulc P, Boutroy S, Vilayphiou N, Schoppet M, Rauner M, Chapurlat R, Hamann C, Hofbauer LC. Correlates of bone microarchitectural parameters and serum sclerostin levels in men: the STRAMBO study. J Bone Miner Res. 2013;28:1760–70.CrossRef
9.
go back to reference Garnero P, Sornay-Rendu E, Munoz F, Borel O, Chapurlat RD. Association of serum sclerostin with bone mineral density, bone turnover, steroid and parathyroid hormones, and fracture risk in postmenopausal women: the OFELY study. Osteoporos Int. 2013;24:489–94.CrossRef Garnero P, Sornay-Rendu E, Munoz F, Borel O, Chapurlat RD. Association of serum sclerostin with bone mineral density, bone turnover, steroid and parathyroid hormones, and fracture risk in postmenopausal women: the OFELY study. Osteoporos Int. 2013;24:489–94.CrossRef
10.
go back to reference Invernizzi M, Carda S, Rizzi M, Grana E, Squarzanti DF, Cisari C, Molinari C, Reno F. Evaluation of serum myostatin and sclerostin levels in chronic spinal cord injured patients. Spinal Cord. 2015;53:615–20.CrossRef Invernizzi M, Carda S, Rizzi M, Grana E, Squarzanti DF, Cisari C, Molinari C, Reno F. Evaluation of serum myostatin and sclerostin levels in chronic spinal cord injured patients. Spinal Cord. 2015;53:615–20.CrossRef
11.
go back to reference Lee AJ, Hodges S, Eastell R. Measurement of osteocalcin. Ann Clin Biochem. 2000;37 ( Pt 4:432–46.CrossRef Lee AJ, Hodges S, Eastell R. Measurement of osteocalcin. Ann Clin Biochem. 2000;37 ( Pt 4:432–46.CrossRef
12.
go back to reference Tsuchiya Y, Sakuraba K, Ochi E. High force eccentric exercise enhances serum tartrate-resistant acid phosphatase-5b and osteocalcin. J Musculoskelet Neuronal Interact. 2014;14:50–7.PubMed Tsuchiya Y, Sakuraba K, Ochi E. High force eccentric exercise enhances serum tartrate-resistant acid phosphatase-5b and osteocalcin. J Musculoskelet Neuronal Interact. 2014;14:50–7.PubMed
14.
go back to reference Lombardi G, Di Somma C, Vuolo L, Guerra E, Scarano E, Colao A. Role of IGF-I on PTH effects on bone. J Endocrinol Investig. 2010;33:22–6. Lombardi G, Di Somma C, Vuolo L, Guerra E, Scarano E, Colao A. Role of IGF-I on PTH effects on bone. J Endocrinol Investig. 2010;33:22–6.
15.
go back to reference Barbieri M, Ferrucci L, Ragno E, Corsi A, Bandinelli S, Bonafe M, Olivieri F, Giovagnetti S, Franceschi C, Guralnik JM, Paolisso G. Chronic inflammation and the effect of IGF-I on muscle strength and power in older persons. Am J Physiol Endocrinol Metab. 2003;284:E481–7.CrossRef Barbieri M, Ferrucci L, Ragno E, Corsi A, Bandinelli S, Bonafe M, Olivieri F, Giovagnetti S, Franceschi C, Guralnik JM, Paolisso G. Chronic inflammation and the effect of IGF-I on muscle strength and power in older persons. Am J Physiol Endocrinol Metab. 2003;284:E481–7.CrossRef
16.
go back to reference Hofmann M, Halper B, Oesen S, Franzke B, Stuparits P, Tschan H, Bachl N, Strasser EM, Quittan M, Ploder M, Wagner KH, Wessner B. Serum concentrations of insulin-like growth factor-1, members of the TGF-beta superfamily and follistatin do not reflect different stages of dynapenia and sarcopenia in elderly women. Exp Gerontol. 2015;64:35–45.CrossRef Hofmann M, Halper B, Oesen S, Franzke B, Stuparits P, Tschan H, Bachl N, Strasser EM, Quittan M, Ploder M, Wagner KH, Wessner B. Serum concentrations of insulin-like growth factor-1, members of the TGF-beta superfamily and follistatin do not reflect different stages of dynapenia and sarcopenia in elderly women. Exp Gerontol. 2015;64:35–45.CrossRef
17.
go back to reference Volpato S, Bianchi L, Cherubini A, Landi F, Maggio M, Savino E, Bandinelli S, Ceda GP, Guralnik JM, Zuliani G, Ferrucci L. Prevalence and clinical correlates of sarcopenia in community-dwelling older people: application of the EWGSOP definition and diagnostic algorithm. J Gerontol A Biol Sci Med Sci. 2014;69:438–46.CrossRef Volpato S, Bianchi L, Cherubini A, Landi F, Maggio M, Savino E, Bandinelli S, Ceda GP, Guralnik JM, Zuliani G, Ferrucci L. Prevalence and clinical correlates of sarcopenia in community-dwelling older people: application of the EWGSOP definition and diagnostic algorithm. J Gerontol A Biol Sci Med Sci. 2014;69:438–46.CrossRef
18.
go back to reference White TA, LeBrasseur NK. Myostatin and sarcopenia: opportunities and challenges - a mini-review. Gerontology. 2014;60:289–93.CrossRef White TA, LeBrasseur NK. Myostatin and sarcopenia: opportunities and challenges - a mini-review. Gerontology. 2014;60:289–93.CrossRef
19.
go back to reference Yarasheski KE, Bhasin S, Sinha-Hikim I, Pak-Loduca J, Gonzalez-Cadavid NF. Serum myostatin-immunoreactive protein is increased in 60-92 year old women and men with muscle wasting. J Nutr Health Aging. 2002;6:343–8.PubMed Yarasheski KE, Bhasin S, Sinha-Hikim I, Pak-Loduca J, Gonzalez-Cadavid NF. Serum myostatin-immunoreactive protein is increased in 60-92 year old women and men with muscle wasting. J Nutr Health Aging. 2002;6:343–8.PubMed
20.
go back to reference Burch PM, Pogoryelova O, Palandra J, Goldstein R, Bennett D, Fitz L, Guglieri M, Bettolo CM, Straub V, Evangelista T, Neubert H, Lochmuller H, Morris C. Reduced serum myostatin concentrations associated with genetic muscle disease progression. J Neurol. 2017;264:541–53.CrossRef Burch PM, Pogoryelova O, Palandra J, Goldstein R, Bennett D, Fitz L, Guglieri M, Bettolo CM, Straub V, Evangelista T, Neubert H, Lochmuller H, Morris C. Reduced serum myostatin concentrations associated with genetic muscle disease progression. J Neurol. 2017;264:541–53.CrossRef
21.
go back to reference Bergen HR 3rd, Farr JN, Vanderboom PM, Atkinson EJ, White TA, Singh RJ, Khosla S, LeBrasseur NK. Myostatin as a mediator of sarcopenia versus homeostatic regulator of muscle mass: insights using a new mass spectrometry-based assay. Skelet Muscle. 2015;5:21.CrossRef Bergen HR 3rd, Farr JN, Vanderboom PM, Atkinson EJ, White TA, Singh RJ, Khosla S, LeBrasseur NK. Myostatin as a mediator of sarcopenia versus homeostatic regulator of muscle mass: insights using a new mass spectrometry-based assay. Skelet Muscle. 2015;5:21.CrossRef
22.
go back to reference Morissette MR, Stricker JC, Rosenberg MA, Buranasombati C, Levitan EB, Mittleman MA, Rosenzweig A. Effects of myostatin deletion in aging mice. Aging Cell. 2009;8:573–83.CrossRef Morissette MR, Stricker JC, Rosenberg MA, Buranasombati C, Levitan EB, Mittleman MA, Rosenzweig A. Effects of myostatin deletion in aging mice. Aging Cell. 2009;8:573–83.CrossRef
23.
go back to reference Matsumoto H, Hagino H, Osaki M, Tanishima S, Tanimura C, Matsuura A, Makabe T. Gait variability analysed using an accelerometer is associated with locomotive syndrome among the general elderly population: the GAINA study. J Orthop Sci. 2016;21:354–60.CrossRef Matsumoto H, Hagino H, Osaki M, Tanishima S, Tanimura C, Matsuura A, Makabe T. Gait variability analysed using an accelerometer is associated with locomotive syndrome among the general elderly population: the GAINA study. J Orthop Sci. 2016;21:354–60.CrossRef
24.
go back to reference Tanimura C, Matsumoto H, Tokushima Y, Yoshimura J, Tanishima S, Hagino H. Self-care agency, lifestyle, and physical condition predict future frailty in community-dwelling older people. Nurs Health Sci. 2017. Tanimura C, Matsumoto H, Tokushima Y, Yoshimura J, Tanishima S, Hagino H. Self-care agency, lifestyle, and physical condition predict future frailty in community-dwelling older people. Nurs Health Sci. 2017.
25.
go back to reference Tanishima S, Hagino H, Matsumoto H, Tanimura C, Nagashima H. Association between sarcopenia and low back pain in local residents prospective cohort study from the GAINA study. BMC Musculoskelet Disord. 2017;18:452.CrossRef Tanishima S, Hagino H, Matsumoto H, Tanimura C, Nagashima H. Association between sarcopenia and low back pain in local residents prospective cohort study from the GAINA study. BMC Musculoskelet Disord. 2017;18:452.CrossRef
26.
go back to reference Coulson J, Bagley L, Barnouin Y, Bradburn S, Butler-Browne G, Gapeyeva H, Hogrel JY, Maden-Wilkinson T, Maier AB, Meskers C, Murgatroyd C, Narici M, Paasuke M, Sassano L, Sipila S, Al-Shanti N, Stenroth L, Jones DA, McPhee JS. Circulating levels of dickkopf-1, osteoprotegerin and sclerostin are higher in old compared with young men and women and positively associated with whole-body bone mineral density in older adults. Osteoporos Int. 2017. Coulson J, Bagley L, Barnouin Y, Bradburn S, Butler-Browne G, Gapeyeva H, Hogrel JY, Maden-Wilkinson T, Maier AB, Meskers C, Murgatroyd C, Narici M, Paasuke M, Sassano L, Sipila S, Al-Shanti N, Stenroth L, Jones DA, McPhee JS. Circulating levels of dickkopf-1, osteoprotegerin and sclerostin are higher in old compared with young men and women and positively associated with whole-body bone mineral density in older adults. Osteoporos Int. 2017.
27.
go back to reference Gaudio A, Pennisi P, Bratengeier C, Torrisi V, Lindner B, Mangiafico RA, Pulvirenti I, Hawa G, Tringali G, Fiore CE. Increased sclerostin serum levels associated with bone formation and resorption markers in patients with immobilization-induced bone loss. J Clin Endocrinol Metab. 2010;95:2248–53.CrossRef Gaudio A, Pennisi P, Bratengeier C, Torrisi V, Lindner B, Mangiafico RA, Pulvirenti I, Hawa G, Tringali G, Fiore CE. Increased sclerostin serum levels associated with bone formation and resorption markers in patients with immobilization-induced bone loss. J Clin Endocrinol Metab. 2010;95:2248–53.CrossRef
28.
go back to reference Hamrick MW, McNeil PL, Patterson SL. Role of muscle-derived growth factors in bone formation. J Musculoskelet Neuronal Interact. 2010;10:64–70.PubMedPubMedCentral Hamrick MW, McNeil PL, Patterson SL. Role of muscle-derived growth factors in bone formation. J Musculoskelet Neuronal Interact. 2010;10:64–70.PubMedPubMedCentral
29.
go back to reference Hamrick MW. A role for myokines in muscle-bone interactions. Exerc Sport Sci Rev. 2011;39:43–7.CrossRef Hamrick MW. A role for myokines in muscle-bone interactions. Exerc Sport Sci Rev. 2011;39:43–7.CrossRef
30.
go back to reference Kanazawa I, Notsu M, Miyake H, Tanaka K, Sugimoto T. Assessment using serum insulin-like growth factor-I and bone mineral density is useful for detecting prevalent vertebral fractures in patients with type 2 diabetes mellitus. Osteoporos Int. 2018. Kanazawa I, Notsu M, Miyake H, Tanaka K, Sugimoto T. Assessment using serum insulin-like growth factor-I and bone mineral density is useful for detecting prevalent vertebral fractures in patients with type 2 diabetes mellitus. Osteoporos Int. 2018.
31.
go back to reference Hitachi K, Nakatani M, Tsuchida K. Myostatin signaling regulates Akt activity via the regulation of miR-486 expression. Int J Biochem Cell Biol. 2014;47:93–103.CrossRef Hitachi K, Nakatani M, Tsuchida K. Myostatin signaling regulates Akt activity via the regulation of miR-486 expression. Int J Biochem Cell Biol. 2014;47:93–103.CrossRef
Metadata
Title
Association of serum bone- and muscle-derived factors with age, sex, body composition, and physical function in community-dwelling middle-aged and elderly adults: a cross-sectional study
Authors
Kenta Moriwaki
Hiromi Matsumoto
Shinji Tanishima
Chika Tanimura
Mari Osaki
Hideki Nagashima
Hiroshi Hagino
Publication date
01-12-2019
Publisher
BioMed Central
Published in
BMC Musculoskeletal Disorders / Issue 1/2019
Electronic ISSN: 1471-2474
DOI
https://doi.org/10.1186/s12891-019-2650-9

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