Estradiol effect on anterior crural muscles-tibial bone relationship and susceptibility to injury
Abstract
The study's objective was to determine whether estradiol (E2) deficiency alters the functional relationship of muscle to bone and causes a differential increase in injury susceptibility. Ovariectomized 6-wk-old mice were administered E2 (40 micrograms. day-1. kg-1; n = 8) or the oil vehicle (n = 8) for 21 days. The anterior crural muscles of the left hindlimb were then stimulated to produce 150 maximal in vivo eccentric contractions. In vitro functional measurements were then made on the extensor digitorum longus (EDL) muscle and tibia from both the exercised and unexercised legs. The maximal isometric torque produced by the anterior crural muscles before the eccentric contraction protocol and the unexercised EDL maximal isometric tetanic force (P(0)) were higher in E2-treated mice by 18 and 14%, respectively (P < or = 0.03). Both ultimate load and stiffness for the unexercised tibia were higher by 16% in E2-treated mice (P < or = 0.03). The muscle-to-bone relationship of these measurements was unaffected by E2 status (P > or = 0.59). No evidence for increased injury susceptibility was found in either tissue from E2-deficient mice. In fact, the decrement in P(0) was only 36.9 +/- 3.8% in exercised EDL muscles from E2-deficient mice compared with 50.6 +/- 4.2% in exercised muscles from E2-treated mice (P = 0.03). Tibia stiffness was 3.9% higher in bones from exercised legs than in bones from unexercised legs (72.64 +/- 2.77 vs. 69.95 +/- 2.66 N/mm; P = 0.05) with ultimate load showing a similar trend (P = 0.07); no effect of E2 status was observed on these differences (P > or = 0.53). In conclusion, the functional relationship of bone to muscle and the susceptibility to injury in bone are not altered by the presence of E2 in ovariectomized mice; however, E2 does increase injury susceptibility in the EDL muscle.
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Functional capacity is significantly impaired immediately and for several days after 150 eccentric contractions.
“Here in this study, as with many others (34, 35, 42–44), we reaffirm that functional capacity is significantly impaired immediately, and for several days after, 150 eccentric contractions.”
From Phytoecdysteroids Accelerate Recovery of Skeletal Muscle Function Following in vivo Eccentric Contraction-Induced Injury in Adult and Old Mice (2021) · cites this paper as [43]
Cites
Perspectives: The role of changes in mechanical usage set points in the pathogenesis of osteoporosis
Frost, H. M. (1992) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.5650070303 · Cited by 264 · see citing works
Distribution of blood flow in muscles of miniature swine during exercise
Armstrong, R. B., Delp, M. D., Goljan, E. F., & Laughlin, M. H. (1987) · Journal of Applied Physiology · doi:10.1152/jappl.1987.62.3.1285 · Cited by 206 · see citing works
Self-citationPrevention of exercise-induced muscle membrane damage by oestradiol
Bär, P. R., Amelink, G. J., Oldenburg, B., & Blankenstein, M. A. (1988) · Life Sciences · doi:10.1016/0024-3205(88)90243-3 · Cited by 133 · see citing works
Cauley, J. A., Petrini, A. M., LaPorte, R. E., Sandler, R. B., Bayles, C. M., Robertson, R. J., & Slemenda, C. W. (1987) · Journal of Chronic Diseases · doi:10.1016/0021-9681(87)90062-2 · Cited by 116 · see citing works
AMELINK, G. J., KOOT, R. W., ERICH, W. B. M., VAN GIJN, J., & BÄR, P. R. (1990) · Acta Physiologica Scandinavica · doi:10.1111/j.1748-1716.1990.tb08823.x · Cited by 109 · see citing works
Exercise-induced muscle protein leakage in the rat
Amelink, G. J., & Bär, P. R. (1986) · Journal of the Neurological Sciences · doi:10.1016/0022-510x(86)90142-5 · Cited by 99 · see citing works
Edwards, M. W., Bain, S. D., Bailey, M. C., Lantry, M. M., & Howard, G. A. (1992) · Bone · doi:10.1016/8756-3282(92)90358-4 · Cited by 85 · see citing works
An apparatus to measure in vivo biomechanical behavior of dorsi- and plantarflexors of mouse ankle
Ashton‐Miller, J. A., He, Y., Kadhiresan, V. A., McCubbrey, D. A., & Faulkner, J. A. (1992) · Journal of Applied Physiology · doi:10.1152/jappl.1992.72.3.1205 · Cited by 76 · see citing works
Arnett, M. G., Rodearmel, S. J., Dennehy, C. A., Moffit, J., Lennon, A., & Schneider, C. (1994) · Medicine & Science in Sports & Exercise · doi:10.1249/00005768-199405001-00308 · Cited by 1 · see citing works
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Self-citation
- Authors
- Warren, G. L., Lowe, D. A., Inman, C. L., Orr, O. M., Hogan, H. A., Bloomfield, S. A., & Armstrong, R. B.
- Affiliations
- Texas A&M University (US)
- Venue
- Journal of Applied Physiology
- Publisher
- American Physiological Society
- Published
- 1996-05-01
- Volume
- 80
- Issue
- 5
- Pages
- 1660-1665
- ISSN
- 0161-7567 (ISSN-L)
- 8750-7587
- 1522-1601
- OpenAlex
- W2133425744
- Cited by
- 56
- References
- 9
- Citations by year
- 2026: 2 · 2024: 1 · 2023: 1 · 2022: 1 · 2021: 2 · 2018: 2 · 2017: 2 · 2016: 1 · 2015: 6 · 2014: 3 · 2013: 1 · 2012: 3
- FWCI
- 0.20
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Applied Physiology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Estrogen and related hormone effects
- Health Sciences › Medicine › Orthopedics and Sports Medicine › Bone health and osteoporosis research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Keywords
- estradiol, estrogen deficiency, ovariectomy, muscle-bone relationship, tibia, injury susceptibility, extensor digitorum longus, eccentric contraction, muscle stiffness, ultimate load, isometric torque, bone mechanical properties
- MeSH terms
- Animals, Estradiol, Female, L-Lactate Dehydrogenase, Mice, Inbred ICR, Muscle Contraction, Ovariectomy, Tibia, Mice
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