{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,20]],"date-time":"2026-08-20T19:53:47Z","timestamp":1787255627048,"version":"build-2736575974"},"reference-count":43,"publisher":"MDPI AG","issue":"22","license":[{"start":{"date-parts":[[2022,11,11]],"date-time":"2022-11-11T00:00:00Z","timestamp":1668124800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"DoD-CDMRP","award":["W81XWH-14-SCIRP-CTA"],"award-info":[{"award-number":["W81XWH-14-SCIRP-CTA"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["JCM"],"abstract":"<jats:p>(1) Background: Resource intensive imaging tools have been employed to examine muscle and bone qualities after spinal cord injury (SCI). We tested the hypothesis that surface neuromuscular electrical stimulation (NMES) amplitude can be used to examine knee extensor muscle quality, distal femur and proximal tibia bone mineral density (BMD) in persons with SCI. (2) Methods: Seventeen persons (2 women) with chronic SCI participated in three weeks of NMES-resistance training twice weekly of 4 sets of 10 repetitions. Participants were classified according to the current amplitude (&gt;100 mA) and the number of repetitions (&gt;70 reps) of leg extension into greater (n = 8; 1 woman; group A) and lower (n = 9; 1 woman; group B) musculoskeletal qualities. Magnetic resonance imaging, dual energy x-ray absorptiometry, isometric peak torque, Modified Ashworth and Penn spasm frequency scales were conducted. (3) Results: In between group comparisons, current amplitude was lower (38\u201346%) in group A. Whole (27\u201332%; p = 0.02), absolute (26\u201333%, p = 0.02) thigh muscle and absolute knee extensor muscle cross-sectional areas (22\u201333%, p = 0.04) were greater in group A. Right distal femur (24%; p = 0.08) and proximal tibia (29%; p = 0.03) BMDs were lower in group B, and peak isometric torque (p &lt; 0.01), extensor spasticity scorers (p = 0.04) and muscle spasm scores (p = 0.002) were significantly higher in group A. Regression models revealed that amplitude of current, repetitions and body weight can accurately predict musculoskeletal qualities in persons with SCI. (4) Conclusions: Surface NMES amplitude and repetitions of leg extension differentiated between SCI survivors with greater versus lower musculoskeletal qualities. The study may shed the light on the interplay between muscle and bone in persons with SCI.<\/jats:p>","DOI":"10.3390\/jcm11226681","type":"journal-article","created":{"date-parts":[[2022,11,11]],"date-time":"2022-11-11T01:39:54Z","timestamp":1668130794000},"page":"6681","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["Employment of Neuromuscular Electrical Stimulation to Examine Muscle and Bone Qualities after Spinal Cord Injury"],"prefix":"10.3390","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-9157-6034","authenticated-orcid":false,"given":"Ashraf S.","family":"Gorgey","sequence":"first","affiliation":[{"name":"Spinal Cord Injury and Disorders Hunter Holmes McGuire VA Medical Center, Richmond, VA 23249, USA"},{"name":"Department of Physical Medicine and Rehabilitation, Virginia Commonwealth University, Richmond, VA 23284, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Refka E.","family":"Khalil","sequence":"additional","affiliation":[{"name":"Spinal Cord Injury and Disorders Hunter Holmes McGuire VA Medical Center, Richmond, VA 23249, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5072-3184","authenticated-orcid":false,"given":"Tommy W.","family":"Sutor","sequence":"additional","affiliation":[{"name":"Spinal Cord Injury and Disorders Hunter Holmes McGuire VA Medical Center, Richmond, VA 23249, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jacob A.","family":"Goldsmith","sequence":"additional","affiliation":[{"name":"Spinal Cord Injury and Disorders Hunter Holmes McGuire VA Medical Center, Richmond, VA 23249, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"David X.","family":"Cifu","sequence":"additional","affiliation":[{"name":"Department of Physical Medicine and Rehabilitation, Virginia Commonwealth University, Richmond, VA 23284, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,11,11]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1038\/s41586-018-0649-2","article-title":"Targeted neurotechnology restores walking in humans with spinal cord injury","volume":"563","author":"Wagner","year":"2018","journal-title":"Nature"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1244","DOI":"10.1056\/NEJMoa1803588","article-title":"Recovery of Over-Ground Walking after Chronic Motor Complete Spinal Cord Injury","volume":"379","author":"Angeli","year":"2018","journal-title":"N. Engl. J. Med."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1843","DOI":"10.1152\/jn.00020.2021","article-title":"Epidural spinal cord stimulation as an intervention for motor recovery after motor complete spinal cord injury","volume":"126","author":"Hachmann","year":"2021","journal-title":"J. Neurophysiol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1002\/acn3.50983","article-title":"The feasibility of using exoskeletal-assisted walking with epidural stimulation: A case report study","volume":"7","author":"Gorgey","year":"2020","journal-title":"Ann. Clin. Transl. Neurol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"373","DOI":"10.1007\/s004210050606","article-title":"Influence of complete spinal cord injury on skeletal muscle cross-sectional area within the first 6 months of injury","volume":"80","author":"Castro","year":"1999","journal-title":"Eur. J. Appl. Physiol. Occup. Physiol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"2398","DOI":"10.1152\/japplphysiol.00729.2002","article-title":"Factors influencing body composition in persons with spinal cord injury: A cross-sectional study","volume":"95","author":"Spungen","year":"2003","journal-title":"J. Appl. Physiol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"711","DOI":"10.1038\/sj.sc.3101652","article-title":"Intramuscular fat and glucose tolerance after spinal cord injury\u2014A cross-sectional study","volume":"42","author":"Elder","year":"2004","journal-title":"Spinal Cord"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"2100","DOI":"10.4103\/1673-5374.221170","article-title":"Quantification of intermuscular and intramuscular adipose tissue using magnetic resonance imaging after neurodegenerative disorders","volume":"12","author":"Ogawa","year":"2017","journal-title":"Neural Regen. Res."},{"key":"ref_9","first-page":"32","article-title":"Lower-extremity muscle atrophy and fat infiltration after chronic spinal cord injury","volume":"15","author":"Moore","year":"2015","journal-title":"J. Musculoskelet. Neuronal Interact."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"2486","DOI":"10.4103\/1673-5374.313060","article-title":"Skeletal muscle stiffness as measured by magnetic resonance elastography after chronic spinal cord injury: A cross-sectional pilot study","volume":"16","author":"Ghatas","year":"2021","journal-title":"Neural Regen. Res."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1321","DOI":"10.1007\/s00198-020-05778-2","article-title":"Bone and non-contractile soft tissue changes following open kinetic chain resistance training and testosterone treatment in spinal cord injury: An exploratory study","volume":"32","author":"Holman","year":"2021","journal-title":"Osteoporos. Int."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1591","DOI":"10.1249\/MSS.0000000000001975","article-title":"Testosterone and Resistance Training Improve Muscle Quality in Spinal Cord Injury","volume":"51","author":"Holman","year":"2019","journal-title":"Med. Sci. Sports Exerc."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"747","DOI":"10.1007\/s00198-016-3798-x","article-title":"Bone loss at the distal femur and proximal tibia in persons with spinal cord injury: Imaging approaches, risk of fracture, and potential treatment options","volume":"28","author":"Cirnigliaro","year":"2017","journal-title":"Osteoporos. Int."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1111\/j.1749-6632.2010.05806.x","article-title":"Bone and muscle loss after spinal cord injury: Organ interactions","volume":"1211","author":"Qin","year":"2010","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"261","DOI":"10.3233\/NRE-2011-0702","article-title":"The effects of spinal cord injury and exercise on bone mass: A literature review","volume":"29","author":"Dolbow","year":"2011","journal-title":"NeuroRehabilitation"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"202","DOI":"10.1080\/10790268.2004.11753748","article-title":"Risk factors for osteoporosis at the knee in the spinal cord injury population","volume":"27","author":"Garland","year":"2004","journal-title":"J. Spinal Cord Med."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"330","DOI":"10.1111\/j.1365-2362.1990.tb01865.x","article-title":"Longitudinal study of bone mineral content in the lumbar spine, the forearm and the lower extremities after spinal cord injury","volume":"20","author":"Bohr","year":"1990","journal-title":"Eur. J. Clin. Investig."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"410","DOI":"10.1007\/s00774-014-0602-x","article-title":"Zoledronic acid administration failed to prevent bone loss at the knee in persons with acute spinal cord injury: An observational cohort study","volume":"33","author":"Bauman","year":"2015","journal-title":"J. Bone Miner. Metab."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"543","DOI":"10.1080\/10790268.2008.11753650","article-title":"Five-year longitudinal bone evaluations in individuals with chronic complete spinal cord injury","volume":"31","author":"Garland","year":"2008","journal-title":"J. Spinal Cord Med."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"939","DOI":"10.1016\/j.pmrj.2013.05.006","article-title":"Femoral bone marrow adiposity and cortical bone cross-sectional areas in men with motor complete spinal cord injury","volume":"5","author":"Gorgey","year":"2013","journal-title":"PM&R"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1016\/j.bone.2004.10.012","article-title":"Deteriorated geometric structure and strength of the midfemur in men with complete spinal cord injury","volume":"36","author":"Modlesky","year":"2005","journal-title":"Bone"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"889","DOI":"10.1007\/s001980070049","article-title":"Quantitative computed tomography in the evaluation of spinal osteoporosis following spinal cord injury","volume":"11","author":"Liu","year":"2000","journal-title":"Osteoporos. Int."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"252","DOI":"10.1016\/j.jocd.2021.11.003","article-title":"Prediction of Distal Femur and Proximal Tibia Bone Mineral Density from Total Body Dual Energy X-ray Absorptiometry Scans in Persons with Spinal Cord Injury","volume":"25","author":"Ghatas","year":"2022","journal-title":"J. Clin. Densitom."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"161","DOI":"10.3233\/NRE-130941","article-title":"Differences in current amplitude evoking leg extension in individuals with spinal cord injury","volume":"33","author":"Gorgey","year":"2013","journal-title":"NeuroRehabilitation"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"526","DOI":"10.1186\/s13063-019-3560-8","article-title":"Skeletal muscle hypertrophy and attenuation of cardio-metabolic risk factors (SHARC) using functional electrical stimulation-lower extremity cycling in persons with spinal cord injury: Study protocol for a randomized clinical trial","volume":"20","author":"Gorgey","year":"2019","journal-title":"Trials"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"2631","DOI":"10.1089\/neu.2018.6136","article-title":"Low-Dose Testosterone and Evoked Resistance Exercise after Spinal Cord Injury on Cardio-Metabolic Risk Factors: An Open-Label Randomized Clinical Trial","volume":"36","author":"Gorgey","year":"2019","journal-title":"J. Neurotrauma"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1007\/s42600-020-00061-z","article-title":"Neuromuscular fatigue detection by mechanomyography in people with complete spinal cord injury","volume":"36","author":"Krueger","year":"2020","journal-title":"Res. Biomed. Eng."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"987","DOI":"10.1038\/s41393-018-0079-x","article-title":"Estimates of the precision of regional and whole body composition by dual-energy X-ray absorptiometry in persons with chronic spinal cord injury","volume":"56","author":"Gorgey","year":"2018","journal-title":"Spinal Cord"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"714","DOI":"10.4103\/1673-5374.206634","article-title":"MRI analysis and clinical significance of lower extremity muscle cross-sectional area after spinal cord injury","volume":"12","author":"Gorgey","year":"2017","journal-title":"Neural Regen. Res."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"366","DOI":"10.1055\/s-0044-102133","article-title":"Validation of Anthropometric Muscle Cross-Sectional Area Equation after Spinal Cord Injury","volume":"39","author":"Wade","year":"2018","journal-title":"Int. J. Sports Med."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1080\/10790268.2010.11689669","article-title":"Relationship of spasticity to soft tissue body composition and the metabolic profile in persons with chronic motor complete spinal cord injury","volume":"33","author":"Gorgey","year":"2010","journal-title":"J. Spinal Cord Med."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"96","DOI":"10.1038\/sj.sc.3102087","article-title":"Spasticity may defend skeletal muscle size and composition after incomplete spinal cord injury","volume":"46","author":"Gorgey","year":"2008","journal-title":"Spinal Cord"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"569","DOI":"10.1038\/s41393-018-0063-5","article-title":"Intra-rater and inter-rater reliability of the Penn Spasm Frequency Scale in People with chronic traumatic spinal cord injury","volume":"56","author":"Mills","year":"2018","journal-title":"Spinal Cord"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"373","DOI":"10.1682\/JRRD.2011.04.0076","article-title":"Insulin growth factors may explain relationship between spasticity and skeletal muscle size in men with spinal cord injury","volume":"49","author":"Gorgey","year":"2012","journal-title":"J. Rehabil. Res. Dev."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"482","DOI":"10.1152\/japplphysiol.00895.2004","article-title":"Time course of molecular responses of human skeletal muscle to acute bouts of resistance exercise","volume":"98","author":"Bickel","year":"2005","journal-title":"J. Appl. Physiol."},{"key":"ref_36","first-page":"175","article-title":"Wolff\u2019s Law and bone\u2019s structural adaptations to mechanical usage: An overview for clinicians","volume":"64","author":"Frost","year":"1994","journal-title":"Angle Orthod."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1080","DOI":"10.2340\/16501977-0469","article-title":"Spasticity and bone density after a spinal cord injury","volume":"41","author":"Lofvenmark","year":"2009","journal-title":"J. Rehabil. Med."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"453","DOI":"10.5312\/wjo.v11.i10.453","article-title":"Long-term effect of intrathecal baclofen treatment on bone health and body composition after spinal cord injury: A case matched report","volume":"11","author":"Ifon","year":"2020","journal-title":"World J. Orthop."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"2166","DOI":"10.1016\/j.apmr.2013.06.016","article-title":"Electrically induced resistance training in individuals with motor complete spinal cord injury","volume":"94","author":"Ryan","year":"2013","journal-title":"Arch. Phys. Med. Rehabil."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1359\/jbmr.0301208","article-title":"Trabecular bone microarchitecture is deteriorated in men with spinal cord injury","volume":"19","author":"Modlesky","year":"2004","journal-title":"J. Bone Miner. Res."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"554","DOI":"10.1016\/j.jocd.2019.07.012","article-title":"Bone Mineral Density Testing in Spinal Cord Injury: 2019 ISCD Official Position","volume":"22","author":"Morse","year":"2019","journal-title":"J. Clin. Densitom."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"106102","DOI":"10.1016\/j.cct.2020.106102","article-title":"The design of a randomized control trial of exoskeletal-assisted walking in the home and community on quality of life in persons with chronic spinal cord injury","volume":"96","author":"Spungen","year":"2020","journal-title":"Contemp. Clin. Trials"},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Gorgey, A.S., Goldsmith, J.A., Khalil, R.E., Liu, X.-H., Pan, J., Cardozo, C., and Adler, R.A. (Eur. J. Appl. Physiol., 2022). Predictors of muscle hypertrophy responsiveness to electrically evoked resistance training after spinal cord injury, Eur. J. Appl. Physiol., in press.","DOI":"10.1007\/s00421-022-05069-0"}],"container-title":["Journal of Clinical Medicine"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2077-0383\/11\/22\/6681\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T01:14:19Z","timestamp":1760145259000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2077-0383\/11\/22\/6681"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,11,11]]},"references-count":43,"journal-issue":{"issue":"22","published-online":{"date-parts":[[2022,11]]}},"alternative-id":["jcm11226681"],"URL":"https:\/\/doi.org\/10.3390\/jcm11226681","relation":{},"ISSN":["2077-0383"],"issn-type":[{"value":"2077-0383","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,11,11]]}}}