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Title: The multiscale structural and mechanical effects of mouse supraspinatus muscle unloading on the mature enthesis

Abstract

The musculoskeletal system is sensitive to its loading environment; this is of particular concern under conditions such as disuse, paralysis, and extended-duration space flight. Although structural and mechanical changes to tendon and bone following paralysis and disuse are well understood, there is a pressing need to understand how this unloading affects the bone-tendon interface (enthesis); the location most prone to tears and injury. Here, we therefore elucidated these effects of unloading in the entheses of adult mice shoulders that were paralyzed for 21 days by treatment with botulinum toxin A. Unloading significantly increased the extent of mechanical failure and was associated with structural changes across hierarchical scales. At the millimeter scale, unloading caused bone loss. At the micrometer scale, unloading decreased bioapatite crystal size and crystallographic alignment in the enthesis. At the nanometer scale, unloading induced compositional changes that stiffened the bioapatite/collagen composite tissue. Mathematical modeling and mechanical testing indicated that these factors combined to increase local elevations of stress while decreasing the ability of the tissue to absorb energy prior to failure, thereby increasing injury risk. These first observations of the multiscale effects of unloading on the adult enthesis provide new insight into the hierarchical features of structure andmore » composition that endow the enthesis with increased resistance to failure.« less

Authors:
ORCiD logo [1];  [2];  [3];  [4];  [5];  [6]; ORCiD logo [7]
  1. Univ. of Connecticut, Storrs, CT (United States). Dept. of Biomedical Engineering
  2. Washington Univ., St. Louis, MO (United States). Dept. of Orthopaedic Surgery
  3. Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
  4. Washington Univ., St. Louis, MO (United States). Dept. of Physics
  5. Washington Univ., St. Louis, MO (United States). Dept. of Earth and Planetary Science
  6. Washington Univ., St. Louis, MO (United States). Dept. of Mechanical Engineering and Materials Science
  7. Columbia Univ., New York, NY (United States). Dept. of Orthopedic Surgery, and Dept. of Biomedical Engineering
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22); National Institutes of Health (NIH)
OSTI Identifier:
1505164
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Acta Biomaterialia
Additional Journal Information:
Journal Volume: 83; Journal Issue: C; Journal ID: ISSN 1742-7061
Publisher:
Acta Materialia, Inc.
Country of Publication:
United States
Language:
English
Subject:
Biomechanics; Enthesis; Paralysis; Rotator cuff; Shoulder; Structure; Unloading

Citation Formats

Deymier, Alix C., Schwartz, Andrea G., Cai, Zhounghou, Daulton, Tyrone L., Pasteris, Jill D., Genin, Guy M., and Thomopoulos, Stavros. The multiscale structural and mechanical effects of mouse supraspinatus muscle unloading on the mature enthesis. United States: N. p., 2018. Web. doi:10.1016/j.actbio.2018.10.024.
Deymier, Alix C., Schwartz, Andrea G., Cai, Zhounghou, Daulton, Tyrone L., Pasteris, Jill D., Genin, Guy M., & Thomopoulos, Stavros. The multiscale structural and mechanical effects of mouse supraspinatus muscle unloading on the mature enthesis. United States. doi:10.1016/j.actbio.2018.10.024.
Deymier, Alix C., Schwartz, Andrea G., Cai, Zhounghou, Daulton, Tyrone L., Pasteris, Jill D., Genin, Guy M., and Thomopoulos, Stavros. Wed . "The multiscale structural and mechanical effects of mouse supraspinatus muscle unloading on the mature enthesis". United States. doi:10.1016/j.actbio.2018.10.024.
@article{osti_1505164,
title = {The multiscale structural and mechanical effects of mouse supraspinatus muscle unloading on the mature enthesis},
author = {Deymier, Alix C. and Schwartz, Andrea G. and Cai, Zhounghou and Daulton, Tyrone L. and Pasteris, Jill D. and Genin, Guy M. and Thomopoulos, Stavros},
abstractNote = {The musculoskeletal system is sensitive to its loading environment; this is of particular concern under conditions such as disuse, paralysis, and extended-duration space flight. Although structural and mechanical changes to tendon and bone following paralysis and disuse are well understood, there is a pressing need to understand how this unloading affects the bone-tendon interface (enthesis); the location most prone to tears and injury. Here, we therefore elucidated these effects of unloading in the entheses of adult mice shoulders that were paralyzed for 21 days by treatment with botulinum toxin A. Unloading significantly increased the extent of mechanical failure and was associated with structural changes across hierarchical scales. At the millimeter scale, unloading caused bone loss. At the micrometer scale, unloading decreased bioapatite crystal size and crystallographic alignment in the enthesis. At the nanometer scale, unloading induced compositional changes that stiffened the bioapatite/collagen composite tissue. Mathematical modeling and mechanical testing indicated that these factors combined to increase local elevations of stress while decreasing the ability of the tissue to absorb energy prior to failure, thereby increasing injury risk. These first observations of the multiscale effects of unloading on the adult enthesis provide new insight into the hierarchical features of structure and composition that endow the enthesis with increased resistance to failure.},
doi = {10.1016/j.actbio.2018.10.024},
journal = {Acta Biomaterialia},
issn = {1742-7061},
number = C,
volume = 83,
place = {United States},
year = {2018},
month = {10}
}

Journal Article:
Free Publicly Available Full Text
This content will become publicly available on October 17, 2019
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