Journal of Eexercise & Organ Cross Talk

The effect of exercise program combined with electrical stimulation on bone mass density (BMD) and bone turnover markers (BTMs) in postmenopausal women with osteopenia

Document Type : Original Article

Authors

1 Department of Sport Science, Azarbaijan Shahid Madani University, Tabriz, Iran.

2 Physical Medicine and Rehabilitation Research Center, Tabriz University of Medical Sciences. Tabriz, Iran

3 Department of Sport Sciences, Faculty of Educational Sciences and Psychology, Azarbaijan Shahid Madani University Tabriz/ Iran

Abstract
The aim of this study was to investigate the effects of an exercise program (EP) in combination with functional electrical stimulation (FES) on bone mass density (BMD) and bone turnover markers (BTMs) in osteopenic postmenopausal women. In this semi-experimental study, 45 women aged 61.25 ± 4.1 years who were classified as osteopenic (-2.5 < T-score < -1) were divided into three groups: 1) EP + FES, 2) EP and 3) control. The EP + FES and EP groups participated in a combined aerobic (45-60% HRR) and strength program for 90 minutes three times a week for 12 weeks. In the EP + FES group, FES with a frequency of 45 Hz and a pulse width of 300 microseconds was applied to the lumbar and hip area. Blood samples were taken at the beginning of the study and again after 12 weeks to determine BMDs. BMD was measured using dual-energy X-ray absorptiometry (DXA). After 12 weeks, cross-linked type 1 collagen C-telopeptide (sCTX) (p=0.002) and pyridinoline (PYD) (p=0.001) levels decreased significantly, while vitamin D (p=0.002), PINP/PYD ratio (p=0,032), the ALP/PYD ratio (p=0.004) and the ALP/CTX-1 ratio (p=0.010) increased significantly in both the EP+FES and EP groups compared to the control group. The EP+FES group showed a significant increase in lumbar (p=0.048) and hip BMD (p=0.038) compared to the control group. Therefore, an exercise programme in combination with FES is recommended as the preferred intervention to maintain or improve bone formation, as FES has a synergistic effect on bone health in patients with osteopenia.

What is already known on this subject?

Aerobic and resistance training can positively influence bone serum metabolism and density over the long term.

 

What this study adds?

Short-term (3 months) multi-component exercise training combined with electrical stimulation can impact bone metabolism.

Keywords

Subjects


Acknowledgements

None.

Funding

This project was supported by a research grant from …… University [grant number 1403/493]. The funder had no influence on the design and conduct of the research; the analysis, collection, management, review, and interpretation of the data; the preparation and approval of the manuscript; and the decision to submit the manuscript for publication. This work originates from a Master's thesis in exercise physiology in the Department of Sports Science.

Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

Compliance with ethical standards

Conflict of interest The authors declare that they have no conflict of interest.

Ethical approval Participation in the study was voluntary and participants could withdraw at any time. Written informed consent was obtained and the study complied with the principles of the Declaration of Helsinki and medical ethics regulations. The ethical code IR.AZARUNIV.REC.1402.010 was registered for this study.

Informed consent Participants signed an informed consent form prior to participation in the study

Author contributions

Conceptualization: A.Z., A.F.K., Y.S., A.A., S.E.; Methodology: A.Z., A.F.K., Y.S., A.A., S.E.; Software: A.Z., A.F.K., Y.S., A.A., S.E.; Validation: A.Z., A.F.K., Y.S., A.A., S.E. Formal analysis: A.Z., A.F.K., Y.S., A.A., S.E.; Investigation: A.Z., A.F.K., Y.S., A.A., S.E; Resources: A.Z., A.F.K., Y.S., A.A., S.E.; Data curation: A.Z., A.F.K., Y.S., A.A., S.E.; Writing - original draft: A.Z., A.F.K., Y.S., A.A., S.E.; Writing–review & editing: A.Z., A.F.K., Y.S., A.A., S.E.; Visualization: A.Z., A.F.K., Y.S., A.A., S.E.; Supervision: A.Z.; Project administration: A.Z.; Funding acquisition: A.Z.

Almstedt, H. C., Grote, S., Korte, J. R., Beaudion, S. P., Shoepe, T. C., Strand, S., & Tarleton, H. P. J. B. r. (2016). Combined aerobic and resistance training improves bone health of female cancer survivors. Bone Rep, 5, 274-279. https://doi.org/210.1016/j.bonr.2016.1009.1003.
Alp, A. (2013). Effects of Aerobic Exercise on Bone-Specific Alkaline Phosphatase and Urinary CTX Levels in Premenopausal Women. Turk J Phys Med Rehabil, 59(4), 310-313. https://doi.org/310.4274/tftr.93546.
Aragão, F. A., Karamanidis, K., Vaz, M. A., Arampatzis, A., & kinesiology. (2011). Mini-trampoline exercise related to mechanisms of dynamic stability improves the ability to regain balance in elderly. J of electromyography, 21(3), 512-518. https://doi.org/510.1016/j.jelekin.2011.1001.1003.  
Armengol, M., Zoulias, I. D., Gibbons, R. S., McCarthy, I., Andrews, B. J., Harwin, W. S., & Holderbaum, W. (2022). The effect of Functional Electrical Stimulation-assisted posture-shifting in bone mineral density: case series-pilot study. Spinal Cord Ser Cases, 8(1), 60. https://doi.org/10.1038/s41394-41022-00523-41399.
Banfi, G., Lombardi, G., Colombini, A., & Lippi, G. (2010). Bone metabolism markers in sports medicine. Sports Med, 40(8), 697-714. https://doi.org/610.2165/11533090-000000000-000000000.
Barry, D. W., & Kohrt, W. M. (2007). Acute effects of 2 hours of moderate-intensity cycling on serum parathyroid hormone and calcium. Calcif Tissue Int, 80(6), 359-365. https://doi.org/310.1007/s00223-00007-09028-y.
BeDell, K. K., Scremin, A. E., Perell, K. L., Kunkel, C. F., & rehabilitation. (1996). Effects of functional electrical stimulation-induced lower extremity cycling on bone density of spinal cord-injured patients1. Am J Phys Med Rehabil, 75(1), 29-34. https://doi.org/10.1097/00002060-199601000-199600008.
Behrens, M., Müller, K., Kilb, J.-I., Schleese, L., Herlyn, P. K., Bruhn, S., . . . Fischer, D.-C. (2017). Modified step aerobics training and neuromuscular function in osteoporotic patients: a randomized controlled pilot study. Arch Orthop Trauma Surg, 137(2), 195-207. https://doi.org/110.1007/s00402-00016-02607-00405.
Camacho, P. M., & Lopez, N. A. (2008). Use of biochemical markers of bone turnover in the management of postmenopausal osteoporosis. Clin Chem Lab Med, 46(10), 1345-1357. https://doi:1310.1515/CCLM.2008.1310.
Çay, V., Buyukyazi, G., Ulman, C., Taneli, F., Doğru, Y., Tıkız, H., . . . Keskinoğlu, P. (2018). Effects of aerobic plus explosive power exercises on bone remodeling and bone mineral density in young men. Turk Biyokim Derg, 43(1), 40-48. https://doi.org/10.1515/tjb-2016-0130.
Çergel, Y., Topuz, O., Alkan, H., Sarsan, A., & Sabir Akkoyunlu, N. (2019). The effects of short-term back extensor strength training in postmenopausal osteoporotic women with vertebral fractures: comparison of supervised and home exercise program. Arch Osteoporos, 14(1), 1-8. https://doi.org/10.1007/s11657-11019-10632-z.
Cheng, X., & Zhao, C. (2023). The correlation between serum levels of alkaline phosphatase and bone mineral density in adults aged 20 to 59 years. Medicine, 102(32), e34755. https://doi:34710.31097/MD.0000000000034755.  
Civil, R., Dolan, E., Swinton, P. A., Santos, L., Varley, I., Atherton, P. J., . . . Sale, C. (2023). P1NP and β-CTX-1 responses to a prolonged, continuous running bout in young healthy adult males: a systematic review with individual participant data meta-analysis. Sports Med Open, 9(1), 85. https://doi.org/10.1186/s40798-40023-00628-x.
Dizdar, M., Irdesel, J. F., Dizdar, O. S., & Topsaç, M. (2018). Effects of balance-coordination, strengthening, and aerobic exercises to prevent falls in postmenopausal patients with osteoporosis: a 6-month randomized parallel prospective study. J Aging Phys Act, 26(1), 41-51. https://doi.org/10.1123/japa.2016-0284.
Dr. Bell, N. H., Godsen, R. N., Henry, D. P., Shary, J., Epstein, S., & research, m. (1988). The effects of muscle‐building exercise on vitamin D and mineral metabolism. J Bone Miner Res, 3(4), 369-374. https://doi.org/310.1002/jbmr.5650030402.
Dror, N., Carbone, J., Haddad, F., Falk, B., Klentrou, P., & Radom-Aizik, S. (2021). Different Sclerostin Response to Cycling and Running at the Same Exercise Intensity. Mapping Intimacies, 1-12. https://doi.org/10.21203/rs.21203.rs-191530/v191531.
Ella, D. S. (2024). THE EFFECT OF EXERCISE ON VITAMIN D METABOLISM AND THE ROLE OF ADIPOSE TISSUE. University of Bath, Student thesis: Doctoral Thesis, 1-299. https://purehost.bath.ac.uk/ws/portalfiles/portal/341345186/329298039_Redacted.pdf
Elnaggar, R. K., Mahmoud, W. S., Moawd, S. A., & Azab, A. R. (2021). Impact of core stability exercises on bone mineralization and functional capacity in children with polyarticular juvenile idiopathic arthritis: a randomized clinical trial. Clin Rheumatol, 40(1), 245-253. https://doi.org/210.1007/s10067-10020-05219-10069.
Elsayyad LK, S. A., Almehmadi M, Gharib AF, El Askary A, Alsayad T, Muhsen A, Allam H. (2021 ). Effect of Exercise-Induced Lipolysis on Serum Vitamin D Level in Obese Children: A Clinical Controlled Trial. Open Access Maced J Med Sci, 9(B), 1596-1601. https://doi.org/10.3889/oamjms.2021.7707
Farajtabar Behrestaq, S. (2023). Comparison of the Levels of Bone Metabolic Markers between Young Female Basketball Players and Non-Athlete Females. mljgoums, 17(1), 47-53. https://doi.org/10.61186/mlj.61117.61181.61147.
Frotzler, A., Coupaud, S., Perret, C., Kakebeeke, T. H., Hunt, K. J., Donaldson, N. d. N., & Eser, P. (2008). High-volume FES-cycling partially reverses bone loss in people with chronic spinal cord injury. J Bone Miner Res, 43(1), 169-176. https://doi.org/10.1016/j.bone.2008.03.004
Garnero, P., Sornay‐Rendu, E., Chapuy, M. C., Delmas, P. D., & research, m. (1996). Increased bone turnover in late postmenopausal women is a major determinant of osteoporosis. J Journal of bone, 11(3), 337-349. doi: https://doi.org/10.1002/jbmr.5650110307
Gombos, G. C., 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 Musculoskeletal Disord, 17, 254. https://doi.org/210.1186/s12891-12016-11109-12895.
Gómez-Cabello, A., Ara, I., González-Agüero, A., Casajús, J., & Vicente-Rodriguez, G. (2012). Effects of training on bone mass in older adults: a systematic review. Sports Med, 42(4), 301-325. https://doi.org/310.2165/11597670-000000000-000000000.
Gorgey, A. S., Venigalla, S., Deitrich, J. N., Ballance, W. B., Carter, W., Lavis, T., & Adler, R. A. (2025). Electrical stimulation paradigms on muscle quality and bone mineral density after spinal cord injury. J Osteoporosis International, 36(6), 1039-1051. doi: https://doi.org/10.1007/s00198-025-07482-5
Guo, S., Dai, X., Chen, X., Zhao, G., Xue, Y., Zhang, C., . . . Shi, Y. (2022). Effect of transcutaneous electrical acupoint stimulation on bone loss for patients with foot and ankle fracture: a pragmatic randomized controlled trial. Am J Transl Res, 14(11), 8191-8203. https://doi.org/8110.1136/bmjopen-2021-056691.
Haryono, I. R., Tulaar, A., Sudoyo, H., Purba, A., Abdullah, M., Jusman, S. W., . . . Ibrahim Ilyas, E. I. (2017). Comparison of the effects of walking and bench-step exercise on osteocalcin and ctx-1 in post-menopausal women with osteopenia. J Musculoskelet Res, 20(02), 1750012. https://doi.org/1750010.1751142/S0218957717500129.
Hemmati, E., Mirghafourvand, M., Mobasseri, M., Shakouri, S. K., Mikaeli, P., Farshbaf-Khalili, A., & Promotion, H. (2021). Prevalence of primary osteoporosis and low bone mass in postmenopausal women and related risk factors. J Educ Health Promot, 10(1), 204. https://doi.org/210.4103/jehp.jehp_4945_4120.
Ibeneme, S., Uzoho, A., Ibeneme, G., & Nna, E. (2015). Effects of aerobic exercises on bone-specific alkaline phosphatase and pyridinoline as markers of bone turnover in women at post-menopause. Physiotherapy, 101(1), e1564. https://doi.org/1510.1016/j.physio.2015.1503.1564.
Kim, A.-R., Lee, S.-E., Shim, Y.-J., & Choi, S.-W. (2022). The Effect of 6-Month Complex Exercise on Serum Bone Metabolism: Focused on the Elderly over 75 Years Old. Applied Sciences, 12(22), 11373. https://doi.org/11310.13390/app122211373.
Lai, C.-H., Chang, W., Chan, W. P., Peng, C.-W., Shen, L.-K., Chen, J., & Chen, S.-C. (2010a). Effects of functional electrical stimulation cycling exercise on bone mineral density loss in the early stages of spinal cord injury. J Journal of rehabilitation medicine, 42(2), 150-154. https://doi.org/10.2340/16501977-0499
Lai, C.-H., Chang, W. H.-S., Chan, W. P., Peng, C.-W., Shen, L.-K., Chen, J.-J. J., & Chen, S.-C. (2010b). Effects of functional electrical stimulation cycling exercise on bone mineral density loss in the early stages of spinal cord injury. J Rehabil Med, 42(2), 150-154. https://doi.org/110.2340/16501977-16500499.
Linhares, D. G., Borba-Pinheiro, C. J., Castro, J. B. P. d., Santos, A. O. B. d., Santos, L. L. d., Cordeiro, L. d. S., . . . Health, P. (2022). Effects of multicomponent exercise training on the health of older women with osteoporosis: a systematic review and meta-analysis. Int J Environ Res Public Health, 19(21), 14195. https://doi.org/14110.13390/ijerph192114195.
Mineiro, L., Zeigelboim, B. S., dos Santos, C. F., da Rosa, M. R., Valderramas, S. R., & Gomes, A. R. S. (2024). Effects of Exercise for Older Women with Osteoporosis: A Systematic Review. Molecular & Cellular Biomechanics, 21, 117. https://doi.org/110.62617/mcb.v62621.62117.
Nahas-Neto, J., Cangussu, L., Orsatti, C., Bueloni-Dias, F., Poloni, P., Schmitt, E., & Nahas, E. (2018). Effect of isolated vitamin D supplementation on bone turnover markers in younger postmenopausal women: a randomized, double-blind, placebo-controlled trial. Osteoporos Int, 29(5), 1125-1133. https://doi.org/1110.1007/s00198-00018-04395-y.
Pasqualini, L., Ministrini, S., Lombardini, R., Bagaglia, F., Paltriccia, R., Pippi, R., . . . E, M. (2019). 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(4), 797-806. https://doi.org/710.1007/s00198-00019-04908-00199.
Perić, D., Kovačev-Zavišić, B., Međedović, B., Romanov, R., Ahmetović, Z., Novaković-Paro, J., & Dimitrić, M. (2018). Physical activity and bone turnover in women with osteopenia. Vojnosanitetski pregled, 75(9), 875-883. https://doi.org/810.2298/VSP160303003P.
Rezaei, N., Torkaman, G., MOVASSEGHE, S., Hedayati, M., & Bayat, N. (2012). The comparison of 6-week resistance training and pulsed electromagnetic field on TALP, CA, P, cortisol, and anthropometric parameters in osteoporotic postmenopausal women. IJEM, 14(4), 380-391. http://ijem.sbmu.ac.ir/article-381-1325-en.html.
Riaz, S., Shakil Ur Rehman, S., Hassan, D., & Hafeez, S. (2024). Gamified Exercise with Kinect: Can Kinect-Based Virtual Reality Training Improve Physical Performance and Quality of Life in Postmenopausal Women with Osteopenia? A Randomized Controlled Trial. j Sensors, 24(11), 3577. https://doi.org/3510.3390/s24113577Riaz.
Schini, M., Vilaca, T., Gossiel, F., Salam, S., & Eastell, R. (2023). Bone turnover markers: basic biology to clinical applications. Endocr Rev, 44(3), 417-473. https://doi:410.1210/endrev/bnac1031.
Shen, C.-L., Williams, J. S., Chyu, M.-C., Paige, R. L., Stephens, A. L., Chauncey, K. B., . . . Yeh, J. K. (2007). Comparison of the effects of Tai Chi and resistance training on bone metabolism in the elderly: a feasibility study. Am J Chin Med, 35(3), 369-381. https://doi.org/310.1142/S0192415X07004898.
N., Bondu, J. D., Thomas, N., & Paul, T. V. (2016). Bone turnover markers: Emerging tool in the management of osteoporosis. Indian J Endocrinol Metab, 20(6), 846-852. https://doi:810.4103/2230-8210.192914.
Shin S, H. N., Rhee Y. . (2024). A randomized controlled trial of the effect of raloxifene plus cholecalciferol versus cholecalciferol alone on bone mineral density in postmenopausal women with osteopenia. JBMR Plus., 8(7), ziae073. https://doi.org/010.1093/jbmrpl/ziae1073.
Shu, J., Tan, A., Li, Y., Huang, H., & Yang, J. (2022). The correlation between serum total alkaline phosphatase and bone mineral density in young adults. BMC Musculoskeletal Disord, 23(1), 467. https://doi.org/410.1186/s12891-12022-05438-y.
Shuai, C., Yang, W., Peng, S., Gao, C., Guo, W., Lai, Y., & Feng, P. (2018). Physical stimulations and their osteogenesis-inducing mechanisms. Int J Bioprint, 4(2), 138. https://doi.org/110.18063/IJB.v18064i18062.18138.
Skrypnik, D., Ratajczak, M., Karolkiewicz, J., Mądry, E., Pupek-Musialik, D., Hansdorfer-Korzon, R., . . . Bogdański, P. (2016). Effects of endurance and endurance–strength exercise on biochemical parameters of liver function in women with abdominal obesity. Biomed Pharmacother, 80, 1-7. https://doi.org/10.1016/j.biopha.2016.1002.1017.
Sözen, T., Özışık, L., & Başaran, N. Ç. (2017). An overview and management of osteoporosis. Eur J Rheumatol, 4(1), 46-56. https://doi:10.5152/eurjrheum.2016.5048
Stunes, A. K., Brobakken, C. L., Sujan, M. A. J., Aagård, N., Brevig, M. S., Wang, E., . . . Mosti, M. P. (2022). Acute effects of strength and endurance training on bone turnover markers in young adults and elderly men. Front Endocrinol (Lausanne), 13, 915241. https://doi.org/915210.913389/fendo.912022.915241.
Tariq, S., Tariq, S., Lone, K. P., & Khaliq, S. (2019). Alkaline phosphatase is a predictor of Bone Mineral Density in postmenopausal females. Pak J Med Sci, 35(3), 749-733. https://doi.org/710.12669/pjms.12635.12663.12188.
Uadia, P., Orumwensodia, K., Arainru, G., Agwubike, E., & Akpata, C. (2016). Effect of physical and flexibility exercise on plasma levels of some liver enzymes and biomolecules of young Nigerian adults. Trop J Nat Prod Res, 15(2), 421-425. https://doi.org/410.4314/tjpr.v4315i4312.4328.
Ureńa, P., Ferreira, A., Kung, V. T., Morieux, C., Simon, P., Ang, K. S., . . . de Vernejoul, M. C. (1995). Serum pyridinoline as a specific marker of collagen breakdown and bone metabolism in hemodialysis patients. J Bone Miner Res, 10(6), 932-939. https://doi:910.1002/jbmr.5650100614.
Vincent, K. R., & Braith, R. W. (2002). Resistance exercise and bone turnover in elderly men and women. Med Sci Sports Exerc, 34(1), 17-23. https://doi.org/10.1097/00005768-200201000-200200004.
Wen, H., Huang, T., Li, T., Chong, P., & Ang, B. (2017). Effects of short-term step aerobics exercise on bone metabolism and functional fitness in postmenopausal women with low bone mass. Osteoporos Int, 28(2), 539-547. https://doi.org/510.1007/s00198-00016-03759-00194.
Zhang, J., & Cao, Z. (2022). Exercise: A Possibly Effective Way to Improve Vitamin D Nutritional Status. Nutrients, 14(13), 2652. https://doi.org/2610.3390/nu14132652.
Zhang, W., Luo, Y., Xu, J., Guo, C., Shi, J., Li, L., . . . Kong, Q. (2023). The Possible Role of Electrical Stimulation in Osteoporosis: A Narrative Review. Medicina, 59(1), 121. https://doi.org/110.3390/medicina59010121.
Zhong, M. (2022). Effect of Core Muscle Strength Training Combined with Taijiquan on Bone Mineral Density Measured by Quantitative CT Scanning in the Elderly. Scanning, 6942081. https://doi.org/6942010.6941155/6942022/6942081.
Volume 5, Issue 2
Spring 2025
Pages 48-58

  • Receive Date 28 April 2025
  • Revise Date 02 June 2025
  • Accept Date 04 June 2025