Abstract
Summary
Osteoporosis is a health issue in postmenopausal women. Physical activity is recommended in these subjects, since it has positive effects on bone mass. Cellular mechanisms underlying this effect are still unclear. Osteogenic cells, released after physical exertion, could be a key factor in exercise-induced bone formation.
Introduction
The aim of our research was to explore if a weight-bearing and resistance exercise program could positively affect circulating osteogenic cells (OCs), markers of bone formation and quality of life (QoL) in osteopenic postmenopausal women.
Methods
We recruited 33 postmenopausal women with a T-score at lumbar spine or femoral neck between − 1 and − 2.5 SD. Anthropometric and fitness parameters, bone-remodeling markers, OCs, and QoL were evaluated at the time of enrolment, after 1-month run-in period, and after 3 months of weight-bearing and resistance exercise.
Results
After 3 months of training, the pro-collagen type 1 N-terminal peptide (P1NP) and the number of OCs were significantly increased, with no significant increase of the type 1 collagen cross-linked C-telopeptide (sCTX). We also observed a significant increase in body height, one-repetition maximum (1RM) on the pull-down lat machine and leg press, and mean VO2max. The increase of immature circulating OCs was significantly correlated with the improvement of 1RM both of the upper and lower limbs. Moreover, QoL was significantly improved with regard to pain, physical function, mental function, and general QoL. The improvement in QoL, namely in the overall score and in the pain score, was significantly correlated with the increase in height.
Conclusions
The exercise program we trialed is able to increase the markers of bone formation and the commitment of immature OCs with no significant increase in the markers of bone resorption. Our results confirm that combined weight-bearing and resistance physical activity is an effective tool to improve QoL of postmenopausal women with low bone mass.
Trial registration
NCT03195517
Similar content being viewed by others
References
Pasco JA, Sanders KM, Hoekstra FM, Henry MJ, Nicholson GC, Kotowicz MA (2005) The human cost of fracture. Osteoporos Int 16:2046–2052
WHO Scientific group (2003) Prevention and management of osteoporosis: report of WHO scientific group. Report No: WHO Technical Report Series 2003: vol. 921
Pasco JA, Seeman E, Henry MJ, Merriman EN, Nicholson GC, Kotowicz MA (2006) The population burden of fractures originates in women with osteopenia, not osteoporosis. Osteoporos Int 17:1404–1409
Koedijk JB, van Rijswijk J, Oranje WA, van den Bergh JP, Bours SP, Savelberg HH, Schaper NC (2017) Sedentary behaviour and bone health in children, adolescents and young adults: a systematic review. Osteoporos Int 28(9):2507–2519. https://doi.org/10.1007/s00198-017-4076-2
Booth FW, Laye MJ, Roberts MD (2011) Lifetime sedentary living accelerates some aspects of secondary aging. J Appl Physiol 111(5):1497–1504
Turner CH, Robling AG (2005) Mechanisms by which exercise improves bone strength. J Bone Miner Metab 23(suppl):16–22
Stubbs B, Brefka S, Denkinger MD (2015) What works to prevent falls in community-dwelling older adults? Umbrella review of meta-analyses of randomized controlled trials. Phys Ther 95(8):1095–1110
Bielemann RM, Martinez-Mesa J, Gigante DP (2013) Physical activity during life course and bone mass: a systematic review of methods and findings from cohort studies with young adults. BMC Musculoskelet Disord 14:77. https://doi.org/10.1186/1471-2474-14-77
Pasqualini L, Leli C, Ministrini S, Schillaci G, Zappavigna RM, Lombardini R, Scarponi AM, Mannarino E (2017) Relationships between global physical activity and bone mineral density in a group of male and female students. J Sports Med Phys Fitness 57(3):238–243
Martyn-St James M, Carroll S (2009) A meta-analysis of impact exercise on postmenopausal bone loss: the case for mixed loading exercise programmes. Br J Sports Med 43(12):898–908. https://doi.org/10.1136/bjsm.2008.052704
Li WC, Chen YC, Yang RS, Tsauo JY (2009) Effects of exercise programmes on quality of life in osteoporotic and osteopenic postmenopausal women: a systematic review and meta-analysis. Clin Rehabil 23(10):888–896
Maïmoun L, Sultan C (2011) Effects of physical activity on bone remodeling. Metabolism 60(3):373–388
Theill LE, Boyle WJ, Penninger JM (2002) RANK-L and RANK: T cells, bone loss, and mammalian evolution. Annu Rev Immunol 20:795–823
Robling AG, Niziolek PJ, Baldridge LA, Condon KW, Allen MR, Alam I, Mantila SM, Gluhak-Heinrich J, Bellido TM, Harris SE, Turner CH (2008) Mechanical stimulation of bone in vivo reduces osteocyte expression of Sost/sclerostin. J Biol Chem 283(9):5866–5875
Long MW, Robinson JA, Ashcraft EA, Mann KG (1995) Regulation of human bone marrow-derived osteoprogenitor cells by osteogenic growth factors. J Clin Invest 95:881–887
Eghbali-Fatourechi GZ, Lamsam J, Fraser D, Nagel D, Riggs BL, Khosla S (2005) Circulating osteoblast-lineage cells in humans. N Engl J Med 352:1959–1966
Shirley D, Marsh D, Jordan G, McQuaid S, Li G (2005) Systemic recruitment of osteoblastic cells in fracture healing. J Orthop Res 23:1013–1021
Pirro M, Leli C, Fabbriciani GL, Manfredelli MR, Callarelli L, Bagaglia F, Scarponi AM, Mannarino E (2010) Association between circulating osteoprogenitor cell numbers and bone mineral density in postmenopausal osteoporosis. Osteoporos Int 21(2):297–306. https://doi.org/10.1007/s00198-009-0968-0
Rubin MR, Manavalan JS, Dempster DW, Shah J, Cremers S, Kousteni S, Zhou H, McMahon DJ, Kode A, Sliney J, Shane E, Silverberg SJ, Bilezikian JP (2011) Parathyroid hormone stimulates circulating osteogenic cells in hypoparathyroidism. J Clin Endocrinol Metab 96(1):176–186. https://doi.org/10.1210/jc.2009-2682
Manavalan JS, Cremers S, Dempster DW, Zhou H, Dworakowski E, Kode A, Kousteni S, Rubin MR (2012) Circulating osteogenic precursor cells in type 2 diabetes mellitus. J Clin Endocrinol Metab 97(9):3240–3250. https://doi.org/10.1210/jc.2012-1546
Bączyk G, Samborski W, Jaracz K (2016) Evaluation of the quality of life of postmenopausal osteoporotic and osteopenic women with or without fractures. Arch Med Sci 12(4):819–827
Lips P, van Schoor NM (2005) Quality of life in patients with osteoporosis. Osteoporos Int 16(5):447–455
Mayhew JL, Prinster JL, Ware JS, Zimmer DL, Arabas JR, Bemben MG (1995) Muscular endurance repetitions to predict bench press strength in men of different training levels. J Sports Med Phys Fitness 35(2):108–113
Balke B, Ware R (1959) An experimental study of physical fitness of Air Force personnel. U S Armed Forces Med J 10:675–688
Lemmink KA, Kemper HC, de Greef MH, Rispens P, Stevens M (2003) The validity of the sit-and-reach test and the modified sit-and-reach test in middle-aged to older men and women. Res Q Exerc Sport 74(3):331–336
Borg G, Hassmen P, Lagerstrom M (1987) Perceived exertion related to heart rate and blood lactate during arm and leg exercise. Eur J Appl Physiol Occup Physiol 56:679–685
Craig CL, Marshall AL, Sjostrom M, Bauman A, Booth ML, Ainsworth BE, Pratt M, Ekelund U, Yngve A, Sallis JF, Oja P (2003) International Physical Activity Questionnaire: 12-country reliability and validity. Med Sci Sports Exerc 35:1381–1395
International Physical Activity Questionnaire. Guidelines for data processing and analysis. Available from: https://sites.google.com/site/theipaq/9/12/15. Accessed April 2015
Lips P, Leplege A (2000) Development and validation of quality of life questionnaire for patients with vertebral fractures: Qualeffo-41. Qual Life Res 9(6a):763–766
Adami S, Gatti D, Viapiana O, Fiore CE, Nuti R, Luisetto G, Ponte M, Rossini M, BONTURNO Study Group (2008) Physical activity and bone turnover markers: a cross-sectional and a longitudinal study. Calcif Tissue Int 83(6):388–392
Mosti MP, Kaehler N, Stunes AK, Hoff J, Syversen U (2013) Maximal strength training in postmenopausal women with osteoporosis or osteopenia. J Strength Cond Res 27(10):2879–2886
Hinton PS, Nigh P, Thyfault J (2017) Serum sclerostin decreases following 12months of resistance- or jump-training in men with low bone mass. Bone 96:85–90
Janik M, Stuss M, Michalska-Kasiczak M, Jegier A, Sewerynek E (2018) Effects of physical activity on sclerostin concentrations. Endokrynol Pol 69(2):142–149. https://doi.org/10.5603/EP.a2018.0008.
Gombos GC, Bajsz V, Pék E, Schmidt B, Sió E, Molics B, Betlehem J (2016) Direct effects of physical training on markers of bone metabolism and serum sclerostin concentrations in older adults with low bone mass. BMC Musculoskelet Disord 8(17):254
Clines GA (2010) Prospects for osteoprogenitor stem cells in fracture repair and osteoporosis. Curr Opin Organ Transplant 15(1):73–78
Kuroda R, Matsumoto T, Kawakami Y, Fukui T, Mifune Y, Kurosaka M (2014) Clinical impact of circulating CD34-positive cells on bone regeneration and healing. Tissue Eng B Rev 20(3):190–199
Colaianni G, Cuscito C, Mongelli T, Oranger A, Mori G, Brunetti G, Colucci S, Cinti S, Grano M (2014) Irisin enhances osteoblast differentiation in vitro. Int J Endocrinol 2014:902186–902188. https://doi.org/10.1155/2014/902186
Carter ND, Khan KM, McKay HA, Petit MA, Waterman C, Heinonen A, Janssen PA, Donaldson MG, Mallinson A, Riddell L, Kruse K, Prior JC, Flicker L (2002) Community-based exercise program reduces risk factors for falls in 65- to 75-year-old women with osteoporosis: randomized controlled trial. CMAJ 167(9):997–1004
Chien MY, Yang RS, Tsauo JY (2005) Home-based trunk-strengthening exercise for osteoporotic and osteopenic postmenopausal women without fracture – a pilot study. Clin Rehabil 19(1):28–36
Devereux K, Robertson D, Briffa NK (2005) Effects of a water- based program on women 65 years and over: a randomized controlled trial. Aust J Physiother 51(2):102–108
Wheater G, Elshahaly M, Tuck SP, Datta HK, van Laar JM (2013) The clinical utility of bone marker measurements in osteoporosis. J Transl Med 11:201
Finnes TE, Lofthus CM, Meyer HE, Eriksen EF, Apalset EM, Tell GS, Torjesen P, Samuelsen SO, Holvik K (2014) Procollagen type 1 amino-terminal propeptide (P1NP) and risk of hip fractures in elderly Norwegian men and women. A NOREPOS study. Bone 64:1–7
Acknowledgements
Miss Helen Walsh is thanked for her editorial assistance.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. This study was approved by the Ethics Committee of Perugia University, and all study subjects signed an informed consent form to voluntarily participate in this study.
Conflicts of interest
None.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Pasqualini, L., Ministrini, S., Lombardini, R. et al. Effects of a 3-month weight-bearing and resistance exercise training on circulating osteogenic cells and bone formation markers in postmenopausal women with low bone mass. Osteoporos Int 30, 797–806 (2019). https://doi.org/10.1007/s00198-019-04908-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00198-019-04908-9