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Micro- and nanostructure specific X-ray tomography reveals less matrix formation and altered collagen organization following reduced loading during Achilles tendon healing

Silva Barreto, Isabella LU orcid ; Pierantoni, Maria LU ; Nielsen, Leonard C. ; Hammerman, Malin LU ; Diaz, Ana ; Novak, Vladimir ; Eliasson, Pernilla ; Liebi, Marianne LU and Isaksson, Hanna LU orcid (2024) In Acta Biomaterialia 174. p.245-257
Abstract

Recovery of the collagen structure following Achilles tendon rupture is poor, resulting in a high risk for re-ruptures. The loading environment during healing affects the mechanical properties of the tendon, but the relation between loading regime and healing outcome remains unclear. This is partially due to our limited understanding regarding the effects of loading on the micro- and nanostructure of the healing tissue. We addressed this through a combination of synchrotron phase-contrast X-ray microtomography and small-angle X-ray scattering tensor tomography (SASTT) to visualize the 3D organization of microscale fibers and nanoscale fibrils, respectively. The effect of in vivo loading on these structures was characterized in early... (More)

Recovery of the collagen structure following Achilles tendon rupture is poor, resulting in a high risk for re-ruptures. The loading environment during healing affects the mechanical properties of the tendon, but the relation between loading regime and healing outcome remains unclear. This is partially due to our limited understanding regarding the effects of loading on the micro- and nanostructure of the healing tissue. We addressed this through a combination of synchrotron phase-contrast X-ray microtomography and small-angle X-ray scattering tensor tomography (SASTT) to visualize the 3D organization of microscale fibers and nanoscale fibrils, respectively. The effect of in vivo loading on these structures was characterized in early healing of rat Achilles tendons by comparing full activity with immobilization. Unloading resulted in structural changes that can explain the reported impaired mechanical performance. In particular, unloading led to slower tissue regeneration and maturation, with less and more disorganized collagen, as well as an increased presence of adipose tissue. This study provides the first application of SASTT on soft musculoskeletal tissues and clearly demonstrates its potential to investigate a variety of other collagenous tissues. Statement of significance: Currently our understanding of the mechanobiological effects on the recovery of the structural hierarchical organization of injured Achilles tendons is limited. We provide insight into how loading affects the healing process by using a cutting-edge approach to for the first time characterize the 3D micro- and nanostructure of the regenerating collagen. We uncovered that, during early healing, unloading results in a delayed and more disorganized regeneration of both fibers (microscale) and fibrils (nanoscale), as well as increased presence of adipose tissue. The results set the ground for the development of further specialized protocols for tendon recovery.

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author
; ; ; ; ; ; ; and
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
3D organization, Fibers, Fibrils, Hierarchical tissue structure, Phase-contrast microtomography, Small-angle X-ray scattering tensor tomography
in
Acta Biomaterialia
volume
174
pages
13 pages
publisher
Elsevier
external identifiers
  • pmid:38096959
  • scopus:85180593638
ISSN
1742-7061
DOI
10.1016/j.actbio.2023.12.015
language
English
LU publication?
yes
id
b19df2ce-5905-4242-b7cc-fcc92e4e4578
date added to LUP
2024-02-13 12:03:19
date last changed
2024-04-14 22:52:12
@article{b19df2ce-5905-4242-b7cc-fcc92e4e4578,
  abstract     = {{<p>Recovery of the collagen structure following Achilles tendon rupture is poor, resulting in a high risk for re-ruptures. The loading environment during healing affects the mechanical properties of the tendon, but the relation between loading regime and healing outcome remains unclear. This is partially due to our limited understanding regarding the effects of loading on the micro- and nanostructure of the healing tissue. We addressed this through a combination of synchrotron phase-contrast X-ray microtomography and small-angle X-ray scattering tensor tomography (SASTT) to visualize the 3D organization of microscale fibers and nanoscale fibrils, respectively. The effect of in vivo loading on these structures was characterized in early healing of rat Achilles tendons by comparing full activity with immobilization. Unloading resulted in structural changes that can explain the reported impaired mechanical performance. In particular, unloading led to slower tissue regeneration and maturation, with less and more disorganized collagen, as well as an increased presence of adipose tissue. This study provides the first application of SASTT on soft musculoskeletal tissues and clearly demonstrates its potential to investigate a variety of other collagenous tissues. Statement of significance: Currently our understanding of the mechanobiological effects on the recovery of the structural hierarchical organization of injured Achilles tendons is limited. We provide insight into how loading affects the healing process by using a cutting-edge approach to for the first time characterize the 3D micro- and nanostructure of the regenerating collagen. We uncovered that, during early healing, unloading results in a delayed and more disorganized regeneration of both fibers (microscale) and fibrils (nanoscale), as well as increased presence of adipose tissue. The results set the ground for the development of further specialized protocols for tendon recovery.</p>}},
  author       = {{Silva Barreto, Isabella and Pierantoni, Maria and Nielsen, Leonard C. and Hammerman, Malin and Diaz, Ana and Novak, Vladimir and Eliasson, Pernilla and Liebi, Marianne and Isaksson, Hanna}},
  issn         = {{1742-7061}},
  keywords     = {{3D organization; Fibers; Fibrils; Hierarchical tissue structure; Phase-contrast microtomography; Small-angle X-ray scattering tensor tomography}},
  language     = {{eng}},
  pages        = {{245--257}},
  publisher    = {{Elsevier}},
  series       = {{Acta Biomaterialia}},
  title        = {{Micro- and nanostructure specific X-ray tomography reveals less matrix formation and altered collagen organization following reduced loading during Achilles tendon healing}},
  url          = {{http://dx.doi.org/10.1016/j.actbio.2023.12.015}},
  doi          = {{10.1016/j.actbio.2023.12.015}},
  volume       = {{174}},
  year         = {{2024}},
}