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. P René van Weeren
  10. Jos Malda  Is a corresponding author
  1. Department of Clinical Sciences, Faculty of Veterinary Medicine, Utrecht University, Netherlands
  2. Regenerative Medicine Utrecht, Utrecht University, Netherlands
  3. Department of Orthopedics, University Medical Centre Utrecht, Netherlands
  4. Department of Biomedical Engineering, Eindhoven University of Technology, Netherlands
  5. Department of Mathematical Sciences, University of Adelaide, Australia
  6. Division of Pathology, Department of Biomolecular Health Sciences, Faculty of Veterinary Medicine, Utrecht University, Netherlands
7 figures, 2 tables and 1 additional file

Figures

Cartilage thickness as analyzed from histological sections.

(A) Total articular cartilage thickness correlates with body mass with a negative allometric relationship (R2=0.91, a=0.28). (B) Total cartilage thickness in correlation with body mass for …

Figure 1—source data 1

Details of the cartilage samples from the aquatic and terrestrial mammals.

https://cdn.elifesciences.org/articles/80936/elife-80936-fig1-data1-v2.xlsx
Analysis of the collagen fibre orientation based on picrosirius red staining and imaging with PLM.

The collagen fibers orientation of aquatic mammals (sperm whale, A; harbor porpoise; B) appeared less organized than fiber orientation in terrestrial mammals (giraffe; C). (C) Cartilage structure in …

Figure 3 with 1 supplement
Mechanical analysis of the tissue samples.

(A) Representative stress relaxation curve of some of the tested cartilage samples (Rothschilds giraffe, porpoise and sperm whale). (B) Schematics of loading methodology: unconfined compression …

Figure 3—figure supplement 1
Stress relaxation.

(A) Initial stress relaxation appeared slower for aquatic mammals and steeper for terrestrial mammals. (B) No significant differences were observed in the phase of slow relaxation.

Figure 4 with 2 supplements
Histological staining and micro-CT analysis of the osteochondral tissues.

Safranin-O staining of histological sections of the tissue of a sperm whale (A), harbor porpoise (B) and Rothschild’s giraffe (C). Aquatic mammals (A,B) showed an abrupt transition from hyaline …

Figure 4—figure supplement 1
Examples of the analysis of tissue from additional species.

3D rendered micro-CT scans (A, C, E, G) and histological sections stained with safranin-O (B, D, F, H) of the osteochondral tissues derived of terrestrial (rat: A, B; white rhinoceros: E, F) and …

Figure 4—figure supplement 2
Lack of calcified cartilage in the sperm whale.

Safranin-O staining of histological sections of tissue of the three sperm whales (A, B, C) included in this study, highlighting the lack of the calcified cartilage layer at the cartilage-bone …

Comparison of the subchondral bone structures in the different species.

Examples of macroscopic (left) and micro-CT scans (right) of a Rothschild’s giraffe, porpoise and sperm whale. Left images show the macroscopic aspect of the humeral head of two aquatics and a …

Schematic drawings of the front extremities.

Drawings highlighting the location of the humerus (in red) of which the head (top) was sampled in this study for the sperm whale (A), harbor porpoise (B) and Rothschild’s giraffe (C).

Polarized light microscopy (PLM) analysis of collagen fiber orientation.

(A) The histological sections stained with picrosirius red were imaged, then a region of interest was selected (ROI, white frame), and the cartilage tissue was divided into deep, middle and …

Tables

Table 1
List of species included in the study.

In total tissue samples from 85 animals (34 for histological analysis, 29 for micro-CT and 20 for biomechanical analysis) were harvested for a total of 15 different species.

SpeciesAverage body mass (kg)ThicknessHistology (n)Micro-CT (n)Bio-mechanics (n)
1Rat (Rattus sp)0.260.2143-
2European Badger (Meles meles)13.20.84111
3Tufted deer (Elaphodus cephalophus)231.301--
4Indian crested porcupine (Hystrix indica)24.50.511-
5Cheetah (Acinonyx jubatus)25.50.48112
6Harbor porpoise (Phocoena phocoena)54.51.11999
7Harbor seal (Phoca vitulina)67.51.77222
8Shetland pony (Equus ferus caballus)1751.1722-
9Striped dolphin (Stenella coeruleoalba)1801.37111
10Onager (Equus hemionus)2030.8911-
8bHorse (Equus ferus caballus)5501.3822-
11Rothschild’s giraffe (Giraffa camelopardalis)10701.85212
12White rhinoceros (Ceratotherium simum)14752.1611-
13Common minke whale (Balaenoptera acutorostrata)51005.052--
14Sperm whale (Physeter macrocephalus)47.3006.51333
15Fin whale (Balaenoptera physalus)48.0007.53111
Total342920
Table 2
Overview of cartilage samples on which biomechanical tests were conducted, with average diameter and thickness per species.
SpeciesNumber of animalsNumber of samplesCartilage diameter (mm)Cartilage thickness (mm)
European Badger (Meles meles)116.41.7
Cheetah (Acinonyx jubatus)126.52.1
Rothschild’s giraffe (Giraffa camelopardalis)236.91.7
Harbor Porpoise (Phocoena phocoena)996.61.7
Harbor Seal (Phoca vitulina)227.43.7
Striped dolphin (Stenella coeruleoalba)137.61.9
Sperm whale (Physeter macrocephalus)346.38.5
Fin whale (Balaenoptera physalus)126.48.9

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