{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,9]],"date-time":"2026-01-09T19:31:57Z","timestamp":1767987117958,"version":"3.49.0"},"reference-count":45,"publisher":"MDPI AG","issue":"14","license":[{"start":{"date-parts":[[2021,7,16]],"date-time":"2021-07-16T00:00:00Z","timestamp":1626393600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"China State Sport General Administration","award":["2013B040, 2015B039"],"award-info":[{"award-number":["2013B040, 2015B039"]}]},{"name":"Chinese Nature Science Foundation","award":["NSFC 31571219"],"award-info":[{"award-number":["NSFC 31571219"]}]},{"name":"Shanghai Jiao Tong University Zhiyuan Foundation","award":["CP2014013"],"award-info":[{"award-number":["CP2014013"]}]},{"name":"China Postdoc Scholarship Council","award":["201806230001"],"award-info":[{"award-number":["201806230001"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJERPH"],"abstract":"<jats:p>This study investigated the impact of Nordic walking on bone properties in postmenopausal women with pre-diabetes and non-alcohol fatty liver disease (NAFLD). A total of 63 eligible women randomly participated in the Nordic walking training (AEx, n = 33), or maintained their daily lifestyle (Con, n = 30) during intervention. Bone mineral content (BMC) and density (BMD) of whole body (WB), total femur (TF), femoral neck (FN), and lumbar spine (L2-4) were assessed by dual-energy X-ray absorptiometry. Serum osteocalcin, pentosidine, receptor activator of nuclear factor kappa-B ligand (RANKL) levels were analyzed by ELISA assay. After an 8.6-month intervention, the AEx group maintained their BMCTF, BMDTF, BMCL2\u22124, and BMDL2\u22124, and increased their BMCFN (p = 0.016), while the Con group decreased their BMCTF (p = 0.008), BMDTF (p = 0.001), and BMDL2\u22124 (p = 0.002). However, no significant group \u00d7 time interaction was observed, except for BMDL2\u22124 (p = 0.013). Decreased pentosidine was correlated with increased BMCWB(r = \u22120.352, p = 0.019). The intervention has no significant effect on osteocalcin and RANKL. Changing of bone mass was associated with changing of pentosidine, but not with osteocalcin and RANKL. Our results suggest that Nordic walking is effective in preventing bone loss among postmenopausal women with pre-diabetes and NAFLD.<\/jats:p>","DOI":"10.3390\/ijerph18147570","type":"journal-article","created":{"date-parts":[[2021,7,16]],"date-time":"2021-07-16T10:52:58Z","timestamp":1626432778000},"page":"7570","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":6,"title":["The Impact of Nordic Walking on Bone Properties in Postmenopausal Women with Pre-Diabetes and Non-Alcohol Fatty Liver Disease"],"prefix":"10.3390","volume":"18","author":[{"given":"Xiaming","family":"Du","sequence":"first","affiliation":[{"name":"Department of Orthopaedics, Shidong Hospital Affiliated to University of Shanghai for Science and Technology, Shanghai 200433, China"},{"name":"Exercise Translational Medicine Center, Shanghai Jiao Tong University, Shanghai 200240, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Chao","family":"Zhang","sequence":"additional","affiliation":[{"name":"Xidu Community Health Service Center of Fengxian District, Shanghai 201400, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Xiangqi","family":"Zhang","sequence":"additional","affiliation":[{"name":"Exercise Translational Medicine Center, Shanghai Jiao Tong University, Shanghai 200240, China"},{"name":"School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai 200240, China"},{"name":"School of Pharmacy, Shanghai Jiao Tong University, Shanghai 200240, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Zhen","family":"Qi","sequence":"additional","affiliation":[{"name":"Exercise Translational Medicine Center, Shanghai Jiao Tong University, Shanghai 200240, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9601-4834","authenticated-orcid":false,"given":"Sulin","family":"Cheng","sequence":"additional","affiliation":[{"name":"Exercise Translational Medicine Center, Shanghai Jiao Tong University, Shanghai 200240, China"},{"name":"School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai 200240, China"},{"name":"Faculty of Sport and Health Sciences, University of Jyv\u00e4skyl\u00e4, 40014 Jyv\u00e4skyl\u00e4, Finland"},{"name":"The Key Laboratory of Systems Biomedicine, Ministry of Education, Shanghai Center for Systems Biomedicine, Shanghai Jiao Tong University, Shanghai 200240, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Shenglong","family":"Le","sequence":"additional","affiliation":[{"name":"Exercise Translational Medicine Center, Shanghai Jiao Tong University, Shanghai 200240, China"},{"name":"School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai 200240, China"},{"name":"Faculty of Sport and Health Sciences, University of Jyv\u00e4skyl\u00e4, 40014 Jyv\u00e4skyl\u00e4, Finland"},{"name":"The Key Laboratory of Systems Biomedicine, Ministry of Education, Shanghai Center for Systems Biomedicine, Shanghai Jiao Tong University, Shanghai 200240, China"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2021,7,16]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"455","DOI":"10.2147\/TCRM.S131945","article-title":"Fracture risk in patients with type 2 diabetes mellitus and possible risk factors: A systematic review and meta-analysis","volume":"13","author":"Moayeri","year":"2017","journal-title":"Ther. Clin. Risk Manag."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"931","DOI":"10.1007\/s40618-015-0342-3","article-title":"Association between nonalcoholic fatty liver disease and bone mineral density: A systematic review and meta-analysis","volume":"38","author":"Upala","year":"2015","journal-title":"J. Endocrinol. Investig."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"396545","DOI":"10.1155\/2013\/396545","article-title":"Low bone mineral density in chinese adults with nonalcoholic Fatty liver disease","volume":"2013","author":"Cui","year":"2013","journal-title":"Int. J. Endocrinol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"423","DOI":"10.1007\/s12020-012-9639-6","article-title":"Association of nonalcoholic fatty liver disease with low bone mass in postmenopausal women","volume":"42","author":"Moon","year":"2012","journal-title":"Endocrine"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"212","DOI":"10.1016\/j.jhep.2019.03.004","article-title":"Global liver disease burdens and research trends: Analysis from a Chinese perspective","volume":"71","author":"Xiao","year":"2019","journal-title":"J. Hepatol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1111\/j.1365-2265.2011.04133.x","article-title":"Regulation of glucose metabolism and the skeleton","volume":"75","author":"Ng","year":"2011","journal-title":"Clin. Endocrinol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"4106","DOI":"10.1210\/jc.2012-2045","article-title":"Serum osteocalcin is not associated with glucose but is inversely associated with leptin across generations of nondiabetic women","volume":"97","author":"Lu","year":"2012","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1817","DOI":"10.1111\/dom.13330","article-title":"Bone: Another potential target to treat, prevent and predict diabetes","volume":"20","author":"Liu","year":"2018","journal-title":"Diabetes Obes. Metab."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"358","DOI":"10.1038\/nm.3084","article-title":"Blockade of receptor activator of nuclear factor-\u03baB (RANKL) signaling improves hepatic insulin resistance and prevents development of diabetes mellitus","volume":"19","author":"Kiechl","year":"2013","journal-title":"Nat. Med."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"347","DOI":"10.1016\/j.diabet.2018.10.001","article-title":"Association between non-alcoholic fatty liver disease and bone turnover biomarkers in post-menopausal women with type 2 diabetes","volume":"45","author":"Mantovani","year":"2019","journal-title":"Diabetes Metab."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"992","DOI":"10.31616\/asj.2018.12.6.992","article-title":"Feasibility of Serum Pentosidine Level as a Potential Risk Factor for Osteoporotic Vertebral Compression Fracture","volume":"12","author":"Choi","year":"2018","journal-title":"Asian Spine J."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1013","DOI":"10.1210\/jc.2007-1270","article-title":"Serum pentosidine levels are positively associated with the presence of vertebral fractures in postmenopausal women with type 2 diabetes","volume":"93","author":"Yamamoto","year":"2008","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"439","DOI":"10.2165\/00007256-200939060-00002","article-title":"Exercise and bone mass in adults","volume":"39","author":"Fuentes","year":"2009","journal-title":"Sports Med."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"76","DOI":"10.1016\/j.amepre.2012.09.043","article-title":"Health benefits of Nordic walking: A systematic review","volume":"44","author":"Tschentscher","year":"2013","journal-title":"Am. J. Prev. Med."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1938","DOI":"10.1177\/2047487317738592","article-title":"Nordic walking for individuals with cardiovascular disease: A systematic review and meta-analysis of randomized controlled trials","volume":"24","author":"Cugusi","year":"2017","journal-title":"Eur. J. Prev. Cardiol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1157","DOI":"10.1016\/j.pmrj.2017.06.021","article-title":"Nordic Walking for the Management of People with Parkinson Disease: A Systematic Review","volume":"9","author":"Cugusi","year":"2017","journal-title":"PM & R"},{"key":"ref_17","first-page":"e13130","article-title":"Nordic walking for women with breast cancer: A systematic review","volume":"28","author":"Torres","year":"2019","journal-title":"Eur. J. Cancer Care"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1553","DOI":"10.1589\/jpts.25.1553","article-title":"Comparison of the Effects of Walking with and without Nordic Pole on Upper Extremity and Lower Extremity Muscle Activation","volume":"25","author":"Shim","year":"2013","journal-title":"J. Phys. Ther. Sci."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Liu, W.Y., Lu, D.J., Du, X.M., Sun, J.Q., Ge, J., Wang, R.W., Wang, R., Zou, J., Xu, C., and Ren, J. (2014). Effect of aerobic exercise and low carbohydrate diet on pre-diabetic non-alcoholic fatty liver disease in postmenopausal women and middle aged men\u2014The role of gut microbiota composition: Study protocol for the AELC randomized controlled trial. BMC Public Health, 14.","DOI":"10.1186\/1471-2458-14-48"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"15952","DOI":"10.1038\/s41598-017-16159-x","article-title":"Effect of aerobic exercise and diet on liver fat in pre-diabetic patients with non-alcoholic-fatty-liver-disease: A randomized controlled trial","volume":"7","author":"Cheng","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"412","DOI":"10.1007\/BF00280883","article-title":"Homeostasis model assessment: Insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man","volume":"28","author":"Matthews","year":"1985","journal-title":"Diabetologia"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"S5","DOI":"10.1590\/S0036-36342009000700004","article-title":"The importance and relevance of peak bone mass in the prevalence of osteoporosis","volume":"51","author":"Bonjour","year":"2009","journal-title":"Salud Publica Mex."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"276","DOI":"10.1016\/j.jocd.2007.05.004","article-title":"Age-related bone mineral density, bone loss rate, prevalence of osteoporosis, and reference database of women at multiple centers in China","volume":"10","author":"Cheng","year":"2007","journal-title":"J. Clin. Densitom."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1111\/j.1600-0838.2011.01335.x","article-title":"Effect of block-periodized exercise training on bone and coronary heart disease risk factors in early post-menopausal women: A randomized controlled study","volume":"23","author":"Kemmler","year":"2013","journal-title":"Scand. J. Med. Sci. Sports"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1111\/sms.13252","article-title":"Osteogenic impact of football training in 55- to 70-year-old women and men with prediabetes","volume":"28","author":"Skoradal","year":"2018","journal-title":"Scand. J. Med. Sci. Sports"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"443","DOI":"10.1007\/s002230001180","article-title":"Efficacy of a 24-week aerobic exercise program for osteopenic postmenopausal women","volume":"67","author":"Chien","year":"2000","journal-title":"Calcif. Tissue Int."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"931","DOI":"10.1002\/jbmr.5650080805","article-title":"Effects of aerobic training on bone mineral density of postmenopausal women","volume":"8","author":"Martin","year":"1993","journal-title":"J. Bone Miner. Res."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"713","DOI":"10.1016\/j.bone.2007.06.009","article-title":"Walking intensity for postmenopausal bone mineral preservation and accrual","volume":"41","author":"Borer","year":"2007","journal-title":"Bone"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1016\/8756-3282(88)90031-2","article-title":"Brisk walking does not stop bone loss in postmenopausal women","volume":"9","author":"Cavanaugh","year":"1988","journal-title":"Bone"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"142","DOI":"10.1097\/00005768-200101000-00021","article-title":"Effects of walking poles on lower extremity gait mechanics","volume":"33","author":"Willson","year":"2001","journal-title":"Med. Sci. Sports Exerc."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"S56","DOI":"10.1007\/BF02406134","article-title":"Functional strain as a determinant for bone remodeling","volume":"36","author":"Lanyon","year":"1984","journal-title":"Calcif. Tissue Int."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1949","DOI":"10.1097\/00005768-200011000-00020","article-title":"Musculoskeletal responses to high- and low-intensity resistance training in early postmenopausal women","volume":"32","author":"Bemben","year":"2000","journal-title":"Med. Sci. Sports Exerc."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"701","DOI":"10.1089\/jwh.1998.7.701","article-title":"The effect of a specific strength-development exercise on bone mineral density in perimenopausal and postmenopausal women","volume":"7","author":"Danz","year":"1998","journal-title":"J. Womens Health"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"203","DOI":"10.2114\/jpa.22.203","article-title":"Effects of physical training on bone mineral density and bone metabolism","volume":"22","author":"Shibata","year":"2003","journal-title":"J. Physiol. Anthropol. Appl. Hum. Sci."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Wochna, K., Nowak, A., Huta-Osiecka, A., Sobczak, K., Kasprzak, Z., and Leszczy\u0144ski, P. (2019). Bone Mineral Density and Bone Turnover Markers in Postmenopausal Women Subjected to an Aqua Fitness Training Program. Int. J. Environ. Res. Public Health, 16.","DOI":"10.3390\/ijerph16142505"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1038\/nature01658","article-title":"Osteoclast differentiation and activation","volume":"423","author":"Boyle","year":"2003","journal-title":"Nature"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"524","DOI":"10.1016\/j.exger.2011.02.005","article-title":"Effects of resistance and aerobic exercise on physical function, bone mineral density, OPG and RANKL in older women","volume":"46","author":"Marques","year":"2011","journal-title":"Exp. Gerontol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"226","DOI":"10.1016\/j.archger.2013.03.014","article-title":"Response of bone mineral density, inflammatory cytokines, and biochemical bone markers to a 32-week combined loading exercise programme in older men and women","volume":"57","author":"Marques","year":"2013","journal-title":"Arch. Gerontol. Geriatr."},{"key":"ref_39","first-page":"178","article-title":"Do walking programs affect C-reactive protein, osteoprotegerin and soluble receptor activator of nuclear factor-kappa \u03b2 ligand?","volume":"34","author":"Esen","year":"2009","journal-title":"T\u00fcrk Biyokim. Derg."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"320","DOI":"10.1007\/s11914-016-0332-1","article-title":"Advanced Glycation End Products, Diabetes, and Bone Strength","volume":"14","author":"Yamamoto","year":"2016","journal-title":"Curr. Osteoporos. Rep."},{"key":"ref_41","first-page":"650","article-title":"Advanced glycation end products affect growth and function of osteoblasts","volume":"29","author":"Franke","year":"2011","journal-title":"Clin. Exp. Rheumatol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"286","DOI":"10.1007\/s00223-012-9641-2","article-title":"Advanced glycation end products (AGEs), but not high glucose, inhibit the osteoblastic differentiation of mouse stromal ST2 cells through the suppression of osterix expression, and inhibit cell growth and increasing cell apoptosis","volume":"91","author":"Okazaki","year":"2012","journal-title":"Calcif. Tissue Int."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"166","DOI":"10.1196\/annals.1433.044","article-title":"Pentosidine effects on human osteoblasts in vitro","volume":"1126","author":"Sanguineti","year":"2008","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"5691","DOI":"10.1074\/jbc.M610536200","article-title":"Non-enzymatic glycation of bone collagen modifies osteoclastic activity and differentiation","volume":"282","author":"Valcourt","year":"2007","journal-title":"J. Biol. Chem."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1007\/s10654-012-9674-x","article-title":"Association between bone mineral density and type 2 diabetes mellitus: A meta-analysis of observational studies","volume":"27","author":"Ma","year":"2012","journal-title":"Eur. J. Epidemiol."}],"container-title":["International Journal of Environmental Research and Public Health"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1660-4601\/18\/14\/7570\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T06:31:25Z","timestamp":1760164285000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1660-4601\/18\/14\/7570"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,7,16]]},"references-count":45,"journal-issue":{"issue":"14","published-online":{"date-parts":[[2021,7]]}},"alternative-id":["ijerph18147570"],"URL":"https:\/\/doi.org\/10.3390\/ijerph18147570","relation":{},"ISSN":["1660-4601"],"issn-type":[{"value":"1660-4601","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,7,16]]}}}