Effects of resistance training on microcirculation of bone tissue and bone turnover markers in postmenopausal women with osteopenia or osteoporosis: A systematic review
Restricted accessResearch articleFirst published online January 30, 2025
Effects of resistance training on microcirculation of bone tissue and bone turnover markers in postmenopausal women with osteopenia or osteoporosis: A systematic review
After menopause, there is an imbalance between bone formation and resorption activity, which could lead to postmenopausal osteopenia or osteoporosis. Resistance training (RT) can induce mechanical stress on bone which is necessary for bone remodeling and angiogenic-osteogenic response. This systematic review aims to assess the effects of RT on bone microcirculation and bone turnover markers (BTMs) in postmenopausal women with osteopenia or osteoporosis.
We conducted a comprehensive search for related studies published up to April 2023 to identify eligible articles. Out of 316 articles identified, the full texts of 69 articles were screened. There is not any study which consider the effect of resistance exercises on bone microcirculation in PMOP women, but four articles aseess the effect of RT on BTMs and were reviewed. The quality of the articles was assessed by using the Physiotherapy Evidence Database (PEDro) scale.
In one study, after 6 and 12 months of RT, bone formation and bone resorption biomarkers decreased not significantly. According to another study, bone formation and resorption biomarkers increased significantly after 3-months RT. Two other studies reported increases in biomarkers of bone formation along with decreases of biomarkers in bone resorption after 6-months of RT, but these were not significant.
However, these results suggest that RT had some beneficial effects on BTMs but it is not an effective tool for modifying BTMs in women with osteoporosis or osteopenia. This may be due to the site-specific skeletal stimulation that RT provides. In addition considering the effect of RT on microcirculation of bone are important. So, there is a need for further, high-quality studies in this field.
BlackDM, RosenCJ. Postmenopausal osteoporosis. New England Journal of Medicine. 2016;374(3):254–62.
2.
WadeS, StraderC, FitzpatrickL, AnthonyM, O’MalleyC. Estimating prevalence of osteoporosis: Examples from industrialized countries. Archives of osteoporosis. 2014;9:1–10.
3.
LupsaB, InsognaK. Endocrinology and metabolism clinics of North America. Bone Health Osteoporosis. 2015;44(3):517–30.
4.
MariniS, BaroneG, MasiniA, DallolioL, BragonzoniL, LongobuccoY, et al. The effect of physical activity on bone biomarkers in people with osteoporosis: A systematic review. Front Endocrinol. 2020;11:585689.
5.
WatsonSL, WeeksBK, WeisLJ, HardingAT, HoranSA, BeckBR. High-intensity resistance and impact training improves bone mineral density and physical function in postmenopausal women with osteopenia and osteoporosis: The LIFTMOR randomized controlled trial. Journal of Bone and Mineral Research. 2018;33(2):211–20.
6.
MoreiraLDF, OliveiraMLd, Lirani-GalvãoAP, Marin-MioRV, SantosRNd, Lazaretti-CastroM. Physical exercise and osteoporosis: Effects of different types of exercises on bone and physical function of postmenopausal women. Arquivos Brasileiros de Endocrinologia & Metabologia. 2014;58:514–22.
7.
TurnerCH, RoblingAG. Designing exercise regimens to increase bone strength. Exercise and sport sciences reviews. 2003;31(1):45–50.
8.
ShojaaM, von StengelS, KohlM, SchoeneD, KemmlerW. Effects of dynamic resistance exercise on bone mineral density in postmenopausal women: A systematic review and meta-analysis with special emphasis on exercise parameters. Osteoporos Int. 2020;31(8):1427–44.
9.
KemmlerW, ShojaaM, KohlM, von StengelS. Exercise effects on bone mineral density in older men: A systematic review with special emphasis on study interventions. Osteoporosis International. 2018;29(7):1493–504.
10.
MuellerS, GosauM, WendlC, PrantlL, WiggermannP, ReichertT, et al. Postoperative evaluation of microvascularization in mandibular reconstructions with microvascular flaps–First results with a new perfusion software for contrast-enhanced sonography (CEUS). Clinical Hemorheology and Microcirculation. 2012;52(2-4):187–96.
11.
MüllerS, GosauM, StrobelD, GehmertS, MoralisA, ReichertT, et al. Assessment of bone microcirculation by contrast-enhanced ultrasound (CEUS) and [18F]-positron emission tomography/computed tomography in free osseous and osseocutaneus flaps for mandibular reconstruction: Preliminary results. Clinical Hemorheology and Microcirculation. 2011;49(1-4):115–28.
12.
VogtMT, CauleyJA, KullerLH, NevittMC. Bone mineral density and blood flow to the lower extremities: The study of osteoporotic fractures. Journal of Bone and Mineral Research. 1997;12(2):283–9.
13.
AlagiakrishnanK, JubyA, HanleyD, TymchakW, SclaterA. Role of vascular factors in osteoporosis. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences. 2003;58(4):M362–M6.
14.
SaranU, PiperniSG, ChatterjeeS. Role of angiogenesis in bone repair. Archives of Biochemistry and Biophysics. 2014;561:109–17.
15.
RamasamySK, KusumbeAP, SchillerM, ZeuschnerD, BixelMG, MiliaC, et al. Blood flow controls bone vascular function and osteogenesis. Nature Communications. 2016;7(1):13601.
16.
HongoM, ItoiE, SinakiM, MiyakoshiN, ShimadaY, MaekawaS, et al. Effect of low-intensity back exercise on quality of life and back extensor strength in patients with osteoporosis: A randomized controlled trial. Osteoporosis International. 2007;18(10):1389–95.
17.
RoghaniT, TorkamanG, MovassegheS, HedayatiM, GooshehB, BayatN. Effects of short-term aerobic exercise with and without external loading on bone metabolism and balance in postmenopausal women with osteoporosis. Rheumatology international. 2013;33(2):291–8.
18.
DelmasP, EastellR, GarneroP, SeibelM, StepanJ, Foundation CoSAotIO. The use of biochemical markers of bone turnover in osteoporosis. Osteoporosis International. 2000;11(6):S2.
19.
GombosGC, BajszV, PékE, SchmidtB, SióE, MolicsB, et al. Direct effects of physical training on markers of bone metabolism and serum sclerostin concentrations in older adults with low bone mass. BMC Musculoskeletal Disorders. 2016;17(1):1–8.
20.
LópezB, QuerejetaR, VaroN, GonzálezA, LarmanM, Martínez UbagoJL, et al. Usefulness of serum carboxy-terminal propeptide of procollagen type I in assessment of the cardioreparative ability of antihypertensive treatment in hypertensive patients. Circulation. 2001;104(3):286–91.
21.
NishizawaY, OhtaH, MiuraM, InabaM, IchimuraS, ShirakiM, et al. Guidelines for the use of bone metabolic markers in the diagnosis and treatment of osteoporosis edition). Journal of bone and mineral metabolism. 2013;31:1–15.
22.
VincentKR, BraithRW. Resistance exercise and bone turnover in elderly men and women. Medicine & Science in Sports & Exercise. 2002;34(1):17–23.
23.
PasqualiniL, MinistriniS, LombardiniR, BagagliaF, PaltricciaR, PippiR, 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. Osteoporosis International. 2019;30(4):797–806.
24.
TheillLE, BoyleWJ, PenningerJM. RANK-L and RANK: T cells, bone loss, and mammalian evolution. Annual Review of Immunology. 2002;20(1):795–823.
25.
YamatoTP, DevezaLA, MaherCG. Exercise for osteoarthritis of the knee (PEDro synthesis). British Journal of Sports Medicine. 2016;50(16):1013–4.
26.
De MortonNA. The PEDro scale is a valid measure of the methodological quality of clinical trials: A demographic study. Australian Journal of Physiotherapy. 2009;55(2):129–33.
27.
WaltmanN, KupzykKA, FloresLE, MackLR, LappeJM, BilekLD. Bone-loading exercises versus risedronate for the prevention of osteoporosis in postmenopausal women with low bone mass: A randomized controlled trial. Osteoporosis International. 2022:1–12.
28.
LineroC, ChoiSJ. Effect of blood flow restriction during low-intensity resistance training on bone markers and physical functions in postmenopausal women. J Exerc Sci Fitness. 2021;19(1):57–65.
29.
MostiMP, KaehlerN, StunesAK, HoffJ, SyversenU. Maximal strength training in postmenopausal women with osteoporosis or osteopenia. The Journal of Strength & Conditioning Research. 2013;27(10):2879–86.
30.
BasatH, EsmaeilzadehS, EskiyurtN. The effects of strengthening and high-impact exercises on bone metabolism and quality of life in postmenopausal women: A randomized controlled trial. Journal of Back and Musculoskeletal Rehabilitation. 2013;26(4):427–35.
31.
RotheR, SchulzeS, NeuberC, HauserS, RammeltS, PietzschJ. Adjuvant drug-assisted bone healing: Part III–Further strategies for local and systemic modulation. Clinical Hemorheology and Microcirculation. 2019;73(3):439–88.
32.
RotheR, SchulzeS, NeuberC, HauserS, RammeltS, PietzschJ. Adjuvant drug-assisted bone healing: Part I–Modulation of inflammation. Clinical Hemorheology and Microcirculation. 2019;73(3):381–408.
33.
RotheR, SchulzeS, NeuberC, HauserS, RammeltS, PietzschJ. Adjuvant drug-assisted bone healing: Part II–Modulation of angiogenesis. Clinical Hemorheology and Microcirculation. 2019;73(3):409–38.
34.
RyanAS, GeS, BlumenthalJB, SerraMC, PriorSJ, GoldbergAP. Aerobic exercise and weight loss reduce vascular markers of inflammation and improve insulin sensitivity in obese women. Journal of the American Geriatrics Society. 2014;62(4):607–14.
35.
KlentrouP, SlackJ, RoyB, LadouceurM. Effects of exercise training with weighted vests on bone turnover and isokinetic strength in postmenopausal women. Journal of aging and physical activity. 2007;15(3):287–99.
36.
KaraarslanS, BüyükyaziG, TaneliF, UlmansC, TikizC, GümüşerG, et al. Effects of different intensity resistance exercise programs on bone turnover markers, osteoprotegerin and receptor activator of nuclear factor kappa? Ligand in Post-Menopausal Women. Turk Klinikleri J Med Sci. 2010;30(1):123–34.
37.
MoreiraLDF, FronzaFCAO, dos SantosRN, TeixeiraLR, KruelLFM, Lazaretti-CastroM. High-intensity aquatic exercises (HydrOS) improve physical function and reduce falls among postmenopausal women. Menopause. 2013;20(10):1012–9.
38.
RezaeiN, TorkamanG, MovassegheS, HedayatiM, BayatN. The comparison of 6-week resistance training and pulsed electromagnetic field on TALP, CA, P, cortisol, and anthropometric parameters in osteoporotic postmenopausal women. 2012.
39.
AraziH, SamadpourM, EghbaliE. The effects of concurrent training (aerobic-resistance) and milk consumption on some markers of bone mineral density in women with osteoporosis. BMC Women’s Health. 2018;18(1):1–9.
40.
TorresA, CruzM, GarciaC, CazarezB, ChenZ, editors. Bone turnover markers responses to acute resistance exercise in postmenopausal women. International Journal of Exercise Science: Conference Proceedings. 2022.
41.
StableyJN, MoningkaNC, BehnkeBJ, DelpMD. Exercise training augments regional bone and marrow blood flow during exercise. Medicine and Science in Sports and Exercise. 2014;46(11):2107.
42.
KusumbeAP, RamasamySK, AdamsRH. Coupling of angiogenesis and osteogenesis by a specific vessel subtype in bone. Nature. 2014;507(7492):323–8.
43.
MatsuzakiH, WohlGR, NovackDV, LynchJA, SilvaMJ. Damaging fatigue loading stimulates increases in periosteal vascularity at sites of bone formation in the rat ulna. Calcified Tissue International. 2007;80:391–9.
44.
TongX, ChenX, ZhangS, HuangM, ShenX, XuJ, et al. The effect of exercise on the prevention of osteoporosis and bone angiogenesis. BioMed Research International. 2019;2019(1):8171897.
45.
TurnerCH, RoblingAG. Mechanisms by which exercise improves bone strength. Journal of Bone and Mineral Metabolism. 2005;23:16–22.
46.
TongX, ChenX, ZhangS, HuangM, ShenX, XuJ, et al. The effect of exercise on the prevention of osteoporosis and bone angiogenesis. BioMed Research International. 2019;2019.
47.
WazzaniR, PalluS, BourzacC, AhmaïdiS, PortierH, JaffréC. Physical activity and bone vascularization: A way to explore in bone repair context?Life. 2021;11(8):783.
48.
KuoT-R, ChenC-H. Bone biomarker for the clinical assessment of osteoporosis: Recent developments and future perspectives. Biomarker Research. 2017;5(1):1–9.
49.
GlendenningP, ChubbSP, VasikaranS. Clinical utility of bone turnover markers in the management of common metabolic bone diseases in adults. Clin Chim Acta. 2018;481:161–70.
50.
GarneroP, HausherrE, ChapuyMC, MarcelliC, GrandjeanH, MullerC, et al. Markers of bone resorption predict hip fracture in elderly women: The EPIDOS Prospective Study. Journal of Bone and Mineral Research. 1996;11(10):1531–8.
51.
JhaS, WangZ, LaucisN, BhattacharyyaT. Trends in media reports, oral bisphosphonate prescriptions, and hip fractures – An ecological analysis. Journal of Bone and Mineral Research. 2015;30(12):2179–87.
52.
BembenDA, FettersNL, BembenMG, NabaviN, KohET. Musculoskeletal responses to high- and low-intensity resistance training in early postmenopausal women. Medicine and Science in Sports and Exercise. 2000;32(11):1949–57.
53.
OladapoBI, IsmailSO, KayodeJF, IkumapayiOM. Piezoelectric effects on bone modeling for enhanced sustainability. Materials Chemistry and Physics. 2023;305:127960.
54.
ChoplinRH, LenchikL, WuertzerS. A practical approach to interpretation of dual-energy X-ray absorptiometry (DXA) for assessment of bone density. Current Radiology Reports. 2014;2:1–12.
55.
AtmacaA, GedikO. Effects of alendronate and risedronate on bone mineral density and bone turnover markers in late postmenopausal women with osteoporosis. Advances in therapy. 2006;23:842–53.
56.
HongAR, KimSW. Effects of resistance exercise on bone health. Endocrinology and Metabolism. 2018;33(4):435–44.
57.
RubinC. Regulation of bone mass by mechanical strain magnitude. Calcif Tissue Int. 1988;37:441–7.
58.
HsiehYF, TurnerCH. Effects of loading frequency on mechanically induced bone formation. Journal of Bone and Mineral Research. 2001;16(5):918–24.
59.
OteroM, EsainI, González-SuarezÁM, GilSM. The effectiveness of a basic exercise intervention to improve strength and balance in women with osteoporosis. Clinical Interventions in Aging. 2017;12:505.
60.
WatsonSL, WeeksBK, WeisLJ, HoranSA, BeckBR. Heavy resistance training is safe and improves bone, function, and stature in postmenopausal women with low to very low bone mass: Novel early findings from the LIFTMOR trial. Osteoporosis International. 2015;26(12):2889–94.
