Microstructural differences in the osteochondral unit of terrestrial and aquatic mammals

  1. Irina AD Mancini
  2. Riccardo Levato
  3. Marlena M Ksiezarczyk
  4. Miguel Dias Castilho
  5. Michael Chen
  6. Mattie HP van Rijen
  7. Lonneke L IJsseldijk
  8. Marja Kik
  9. René van Weeren
  10. Jos Malda  Is a corresponding author
  1. Utrecht University, Netherlands
  2. University Medical Center Utrecht, Netherlands
  3. Eindhoven University of Technology, Netherlands
  4. University of Adelaide, Netherlands

Abstract

During evolution, animals have returned from land to water, adapting with morphological modifications to life in an aquatic environment. We compared the osteochondral units of the humeral head of marine and terrestrial mammals across species spanning a wide range of body weights, focusing on microstructural organization and biomechanical performance. Aquatic mammals feature cartilage with essentially random collagen fiber configuration, lacking the depth-dependent, arcade-like organization characteristic of terrestrial mammalian species. They have a less stiff articular cartilage at equilibrium with a significantly lower peak modulus, and at the osteochondral interface do not have a calcified cartilage layer, displaying only a thin, highly porous subchondral bone plate. This totally different constitution of the osteochondral unit in aquatic mammals reflects that accommodation of loading is the primordial function of the osteochondral unit. Recognizing the crucial importance of the microarchitecture-function relationship is pivotal for understanding articular biology and, hence, for the development of durable functional regenerative approaches for treatment of joint damage, which are thus far lacking.

Data availability

Data generated or analysed during this study are included in the manuscript and supporting file; Source Data files have been provided for Figure 1.

Article and author information

Author details

  1. Irina AD Mancini

    Department of Clinical Sciences, Utrecht University, Utrecht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  2. Riccardo Levato

    Department of Clinical Sciences, Utrecht University, Utrecht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  3. Marlena M Ksiezarczyk

    Department of Orthopedics, University Medical Center Utrecht, Utrecht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  4. Miguel Dias Castilho

    Department of Biomedical Engineering, Eindhoven University of Technology, Eindhoven, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  5. Michael Chen

    5Department of Mathematical Sciences, University of Adelaide, Adelaide, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  6. Mattie HP van Rijen

    Department of Orthopedics, University Medical Center Utrecht, Utrecht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  7. Lonneke L IJsseldijk

    Department of Biomolecular Health Sciences, Utrecht University, Utrecht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7288-9118
  8. Marja Kik

    Department of Biomolecular Health Sciences, Utrecht University, Utrecht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  9. René van Weeren

    Department of Clinical Sciences, Utrecht University, Utrecht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6654-1817
  10. Jos Malda

    Department of Orthopedics, University Medical Center Utrecht, Utrecht, Netherlands
    For correspondence
    j.malda@umcutrecht.nl
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9241-7676

Funding

European Commission (3099622 (FP7))

  • Irina AD Mancini
  • René van Weeren
  • Jos Malda

Dutch Arthritis Society (LLP12 and LLP22)

  • Riccardo Levato
  • Miguel Dias Castilho
  • René van Weeren
  • Jos Malda

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

© 2023, Mancini et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Irina AD Mancini
  2. Riccardo Levato
  3. Marlena M Ksiezarczyk
  4. Miguel Dias Castilho
  5. Michael Chen
  6. Mattie HP van Rijen
  7. Lonneke L IJsseldijk
  8. Marja Kik
  9. René van Weeren
  10. Jos Malda
(2023)
Microstructural differences in the osteochondral unit of terrestrial and aquatic mammals
eLife 12:e80936.
https://doi.org/10.7554/eLife.80936

Share this article

https://doi.org/10.7554/eLife.80936

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