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Locomotor training with adjuvant testosterone preserves cancellous bone and promotes muscle plasticity in male rats after severe spinal cord injury.

Abstract

Loading and testosterone may influence musculoskeletal recovery after spinal cord injury (SCI). Our objectives were to determine (a) the acute effects of bodyweight-supported treadmill training (TM) on hindlimb cancellous bone microstructure and muscle mass in adult rats after severe contusion SCI and (b) whether longer-term TM with adjuvant testosterone enanthate (TE) delivers musculoskeletal benefit. In Study 1, TM (40 min/day, 5 days/week, beginning 1 week postsurgery) did not prevent SCI-induced hindlimb cancellous bone loss after 3 weeks. In Study 2, TM did not attenuate SCI-induced plantar flexor muscles atrophy nor improve locomotor recovery after 4 weeks. In our main study, SCI produced extensive distal femur and proximal tibia cancellous bone deficits, a deleterious slow-to-fast fiber-type transition in soleus, lower muscle fiber cross-sectional area (fCSA), impaired muscle force production, and levator ani/bulbocavernosus (LABC) muscle atrophy after 8 weeks. TE alone (7.0 mg/week) suppressed bone resorption, attenuated cancellous bone loss, constrained the soleus fiber-type transition, and prevented LABC atrophy. In comparison, TE+TM concomitantly suppressed bone resorption and stimulated bone formation after SCI, produced near-complete cancellous bone preservation, prevented the soleus fiber-type transition, attenuated soleus fCSA atrophy, maintained soleus force production, and increased LABC mass. 75% of SCI+TE+TM animals recovered voluntary over-ground hindlimb stepping, while no SCI and only 20% of SCI+TE animals regained stepping ability. Positive associations between testosterone and locomotor function suggest that TE influenced locomotor recovery. In conclusion, short-term TM alone did not improve bone, muscle, or locomotor recovery in adult rats after severe SCI, while longer-term TE+TM provided more comprehensive musculoskeletal benefit than TE alone.

Authors+Show Affiliations

Research Service, Malcom Randall Department of Veterans Affairs Medical Center, North Florida/South Georgia Veterans Health System, Gainesville, FL, USA. Brain Rehabilitation Research Center, Malcom Randall Department of Veterans Affairs Medical Center, North Florida/South Georgia Veterans Health System, Gainesville, FL, USA. Division of Endocrinology, Diabetes, and Metabolism, University of Florida College of Medicine, Gainesville, FL, USA.Research Service, Malcom Randall Department of Veterans Affairs Medical Center, North Florida/South Georgia Veterans Health System, Gainesville, FL, USA. Department of Applied Physiology and Kinesiology, University of Florida, Gainesville, FL, USA.Research Service, Malcom Randall Department of Veterans Affairs Medical Center, North Florida/South Georgia Veterans Health System, Gainesville, FL, USA.Research Service, Malcom Randall Department of Veterans Affairs Medical Center, North Florida/South Georgia Veterans Health System, Gainesville, FL, USA.Research Service, Malcom Randall Department of Veterans Affairs Medical Center, North Florida/South Georgia Veterans Health System, Gainesville, FL, USA.Research Service, Malcom Randall Department of Veterans Affairs Medical Center, North Florida/South Georgia Veterans Health System, Gainesville, FL, USA.Research Service, Malcom Randall Department of Veterans Affairs Medical Center, North Florida/South Georgia Veterans Health System, Gainesville, FL, USA.Research Service, Malcom Randall Department of Veterans Affairs Medical Center, North Florida/South Georgia Veterans Health System, Gainesville, FL, USA.Research Service, Malcom Randall Department of Veterans Affairs Medical Center, North Florida/South Georgia Veterans Health System, Gainesville, FL, USA.Brain Rehabilitation Research Center, Malcom Randall Department of Veterans Affairs Medical Center, North Florida/South Georgia Veterans Health System, Gainesville, FL, USA.Divison of Orthopedics and Rehabilitation, University of Florida College of Medicine, Gainesville, FL, USA.Department of Physiological Sciences, University of Florida, Gainesville, FL, USA.National Center for the Medical Consequences of Spinal Cord Injury, James J. Peters Veterans Affairs Medical Center, Bronx, NY, USA. Departments of Medicine, Icahn School of Medicine, New York, NY, USA.National Center for the Medical Consequences of Spinal Cord Injury, James J. Peters Veterans Affairs Medical Center, Bronx, NY, USA. Departments of Medicine, Icahn School of Medicine, New York, NY, USA. Rehabilitation Medicine, Icahn School of Medicine, New York, NY, USA.Department of Physical Therapy, University of Florida, Gainesville, FL, USA.Brain Rehabilitation Research Center, Malcom Randall Department of Veterans Affairs Medical Center, North Florida/South Georgia Veterans Health System, Gainesville, FL, USA. Department of Physiological Sciences, University of Florida, Gainesville, FL, USA. Division of Neurology, University of Florida College of Medicine, Gainesville, FL, USA.Department of Physiological Sciences, University of Florida, Gainesville, FL, USA.Department of Applied Physiology and Kinesiology, University of Florida, Gainesville, FL, USA.Research Service, Malcom Randall Department of Veterans Affairs Medical Center, North Florida/South Georgia Veterans Health System, Gainesville, FL, USA.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

31797423

Citation

Yarrow, Joshua F., et al. "Locomotor Training With Adjuvant Testosterone Preserves Cancellous Bone and Promotes Muscle Plasticity in Male Rats After Severe Spinal Cord Injury." Journal of Neuroscience Research, 2019.
Yarrow JF, Kok HJ, Phillips EG, et al. Locomotor training with adjuvant testosterone preserves cancellous bone and promotes muscle plasticity in male rats after severe spinal cord injury. J Neurosci Res. 2019.
Yarrow, J. F., Kok, H. J., Phillips, E. G., Conover, C. F., Lee, J., Bassett, T. E., ... Ye, F. (2019). Locomotor training with adjuvant testosterone preserves cancellous bone and promotes muscle plasticity in male rats after severe spinal cord injury. Journal of Neuroscience Research, doi:10.1002/jnr.24564.
Yarrow JF, et al. Locomotor Training With Adjuvant Testosterone Preserves Cancellous Bone and Promotes Muscle Plasticity in Male Rats After Severe Spinal Cord Injury. J Neurosci Res. 2019 Dec 4; PubMed PMID: 31797423.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Locomotor training with adjuvant testosterone preserves cancellous bone and promotes muscle plasticity in male rats after severe spinal cord injury. AU - Yarrow,Joshua F, AU - Kok,Hui Jean, AU - Phillips,Ean G, AU - Conover,Christine F, AU - Lee,Jimmy, AU - Bassett,Taylor E, AU - Buckley,Kinley H, AU - Reynolds,Michael C, AU - Wnek,Russell D, AU - Otzel,Dana M, AU - Chen,Cong, AU - Jiron,Jessica M, AU - Graham,Zachary A, AU - Cardozo,Christopher, AU - Vandenborne,Krista, AU - Bose,Prodip K, AU - Aguirre,Jose Ignacio, AU - Borst,Stephen E, AU - Ye,Fan, Y1 - 2019/12/04/ PY - 2019/08/28/received PY - 2019/10/31/revised PY - 2019/11/11/accepted PY - 2019/12/5/entrez PY - 2019/12/5/pubmed PY - 2019/12/5/medline KW - RRID:AB_1157865 KW - RRID:AB_1157897 KW - RRID:AB_138404 KW - RRID:AB_1500896 KW - RRID:AB_2099233 KW - RRID:AB_2147165 KW - RRID:AB_2235587 KW - RRID:AB_2556551 KW - RRID:AB_330924 KW - RRID:AB_60395 KW - RRID:AB_881987 KW - androgen KW - estradiol KW - exercise KW - hypogonadism KW - neuromuscular plasticity KW - osteoporosis KW - physical rehabilitation KW - regenerative rehabilitation JF - Journal of neuroscience research JO - J. Neurosci. Res. N2 - Loading and testosterone may influence musculoskeletal recovery after spinal cord injury (SCI). Our objectives were to determine (a) the acute effects of bodyweight-supported treadmill training (TM) on hindlimb cancellous bone microstructure and muscle mass in adult rats after severe contusion SCI and (b) whether longer-term TM with adjuvant testosterone enanthate (TE) delivers musculoskeletal benefit. In Study 1, TM (40 min/day, 5 days/week, beginning 1 week postsurgery) did not prevent SCI-induced hindlimb cancellous bone loss after 3 weeks. In Study 2, TM did not attenuate SCI-induced plantar flexor muscles atrophy nor improve locomotor recovery after 4 weeks. In our main study, SCI produced extensive distal femur and proximal tibia cancellous bone deficits, a deleterious slow-to-fast fiber-type transition in soleus, lower muscle fiber cross-sectional area (fCSA), impaired muscle force production, and levator ani/bulbocavernosus (LABC) muscle atrophy after 8 weeks. TE alone (7.0 mg/week) suppressed bone resorption, attenuated cancellous bone loss, constrained the soleus fiber-type transition, and prevented LABC atrophy. In comparison, TE+TM concomitantly suppressed bone resorption and stimulated bone formation after SCI, produced near-complete cancellous bone preservation, prevented the soleus fiber-type transition, attenuated soleus fCSA atrophy, maintained soleus force production, and increased LABC mass. 75% of SCI+TE+TM animals recovered voluntary over-ground hindlimb stepping, while no SCI and only 20% of SCI+TE animals regained stepping ability. Positive associations between testosterone and locomotor function suggest that TE influenced locomotor recovery. In conclusion, short-term TM alone did not improve bone, muscle, or locomotor recovery in adult rats after severe SCI, while longer-term TE+TM provided more comprehensive musculoskeletal benefit than TE alone. SN - 1097-4547 UR - https://www.unboundmedicine.com/medline/citation/31797423/Locomotor_training_with_adjuvant_testosterone_preserves_cancellous_bone_and_promotes_muscle_plasticity_in_male_rats_after_severe_spinal_cord_injury L2 - https://doi.org/10.1002/jnr.24564 DB - PRIME DP - Unbound Medicine ER -