Skip to main page content
Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2018 Jul 5;6:e5156.
doi: 10.7717/peerj.5156. eCollection 2018.

Trabecular Bone Patterning in the Hominoid Distal Femur

Affiliations
Free PMC article

Trabecular Bone Patterning in the Hominoid Distal Femur

Leoni Georgiou et al. PeerJ. .
Free PMC article

Abstract

Background: In addition to external bone shape and cortical bone thickness and distribution, the distribution and orientation of internal trabecular bone across individuals and species has yielded important functional information on how bone adapts in response to load. In particular, trabecular bone analysis has played a key role in studies of human and nonhuman primate locomotion and has shown that species with different locomotor repertoires display distinct trabecular architecture in various regions of the skeleton. In this study, we analyse trabecular structure throughout the distal femur of extant hominoids and test for differences due to locomotor loading regime.

Methods: Micro-computed tomography scans of Homo sapiens (n = 11), Pan troglodytes (n = 18), Gorilla gorilla (n = 14) and Pongo sp. (n = 7) were used to investigate trabecular structure throughout the distal epiphysis of the femur. We predicted that bone volume fraction (BV/TV) in the medial and lateral condyles in Homo would be distally concentrated and more anisotropic due to a habitual extended knee posture at the point of peak ground reaction force during bipedal locomotion, whereas great apes would show more posteriorly concentrated BV/TV and greater isotropy due to a flexed knee posture and more variable hindlimb use during locomotion.

Results: Results indicate some significant differences between taxa, with the most prominent being higher BV/TV in the posterosuperior region of the condyles in Pan and higher BV/TV and anisotropy in the posteroinferior region in Homo. Furthermore, trabecular number, spacing and thickness differ significantly, mainly separating Gorilla from the other apes.

Discussion: The trabecular architecture of the distal femur holds a functional signal linked to habitual behaviour; however, there was more similarity across taxa and greater intraspecific variability than expected. Specifically, there was a large degree of overlap in trabecular structure across the sample, and Homo was not as distinct as predicted. Nonetheless, this study offers a comparative sample of trabecular structure in the hominoid distal femur and can contribute to future studies of locomotion in extinct taxa.

Keywords: Functional morphology; Hominoid; Locomotion; Trabecular bone.

Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Figure 1
Figure 1. Comparison of knee posture during different habitual locomotor activities in great apes (A–B) and humans (C–D).
(A) Great ape knee posture in maximum knee flexion (∼50°) during climbing (Isler, 2005). (B) Great ape knee posture at toe-off (∼120°) during terrestrial knuckle-walking (Finestone et al., 2018). (C) Human knee posture at toe-off (∼145°). (D) Human knee posture at heel-strike (∼160°). These were selected depending on when GRF is highest. In this study, all great apes are considered to show similar degrees of knee flexion during quadrupedal walking, as demonstrated by Finestone et al. (2018) and during climbing, but it should be noted that Gorilla has been shown to use a less flexed knee posture during vertical climbing compared with Pan (Isler, 2005).
Figure 2
Figure 2. Processing steps of a Gorilla specimen, showing a parasagittal view through the lateral condyle.
(A) Segmented microCT scan. (B) Inner trabecular area. (C) Trinary mask representing inner air, outer air and trabecular structure, as well as the 3D background grid. (D) BV/ TV distribution within this slice (scaled to its own data range).
Figure 3
Figure 3. Partitioning of the lateral condyle into sub-regions in a Pan specimen.
(A) Selection of condyle. (B) Separation into quarters, including the distal (bottom, right), posteroinferior (bottom, left) and posterosuperior (top, left). The anterosuperior quadrant (top, right) was not analysed. The medial condyle was partitioned in the same way.
Figure 4
Figure 4. Pan BV/TV distribution.
(A) Anterior view. (B) Inferior view. (C) Posterior view. (D) Lateral condyle. (E) Medial condyle. (F–J) Specimen MPITC 15001. (F) Anterior view. (G) Inferior view. (H) Posterior view. (I) Lateral condyle. (J) Medial condyle. (K-O) Specimen MPITC 11786. (K) Anterior view. (L) Inferior view. (M) Posterior view. (N) Lateral condyle. (O) Medial condyle. (P–T) Specimen MPITC 11793. (P) Anterior view. (Q) Inferior view. (R) Posterior view. (S) Lateral condyle. (T) Medial condyle. (U–Y) Specimen MPITC 11778. (U) Anterior view. (V) Inferior view. (W) Posterior view. (X) Lateral condyle. (Y) Medial condyle. All specimens are from the right side. In anterior and inferior views the medial condyle is on the right. In the posterior view the medial condyle is on the left. The location of the parasagittal slice through each condyle is indicated above and the main areas of interest are outlined. Individuals are scaled to the same data range.
Figure 5
Figure 5. Gorilla BV/TV distribution.
(A–E) Specimen M95. (A) Anterior view. (B) Inferior view. (C) Posterior view. (D) Lateral condyle. (E) Medial condyle. (F–J) Specimen M300. (F) Anterior view. (G) Inferior view. (H) Posterior view. (I) Lateral condyle. (J) Medial condyle. (K–O) Specimen M372. (K) Anterior view. (L) Inferior view. (M) Posterior view. (N) Lateral condyle. (O) Medial condyle. (P-T) Specimen M798. (P) Anterior view. (Q) Inferior view. (R) Posterior view. (S) Lateral condyle. (T) Medial condyle. (U–Y) Specimen M856. (U) Anterior view. (V) Inferior view. (W) Posterior view. (X) Lateral condyle. (Y) Medial condyle. All specimens are from the right side. In anterior and inferior views the medial condyle is on the right. In the posterior view the medial condyle is on the left. The location of the parasagittal slice through each condyle is indicated above and the main areas of interest are outlined. Individuals are scaled to the same data range.
Figure 6
Figure 6. Pongo BV/TV distribution.
(A–E) Specimen ZSM 1909 0801. (A) Anterior view. (B) Inferior view. (C) Posterior view. (D) Lateral condyle. (E) Medial condyle. (F–J) Specimen ZSM 1907 0660. (F) Anterior view. (G) Inferior view. (H) Posterior view. (I) Lateral condyle. (J) Medial condyle. (K–O) Specimen ZSM 1973 0270. (K) Anterior view. (L) Inferior view. (M) Posterior view. (N) Lateral condyle. (O) Medial condyle. (P–T) Specimen ZSM 1907 0483. (P) Anterior view. (Q) Inferior view. (R) Posterior view. (S) Lateral condyle. (T) Medial condyle. (U–Y) Specimen ZSM 1907 0633B. (U) Anterior view. (V) Inferior view. (W) Posterior view. (X) Lateral condyle. (Y) Medial condyle. All specimens are from the right side. In anterior and inferior views the medial condyle is on the right. In the posterior view the medial condyle is on the left. The location of the parasagittal slice through each condyle is indicated above and the main areas of interest are outlined. Individuals are scaled to the same data range. Captive specimens are not included in the figure but can be found in the Supplemental Files.
Figure 7
Figure 7. Homo BV/TV distribution.
(A–E) Specimen Campus 66. (A) Anterior view. (B) Inferior view. (C) Posterior view. (D) Lateral condyle. (E) Medial condyle. (F–J) Specimen Campus 36. (F) Anterior view. (G) Inferior view. (H) Posterior view. (I) Lateral condyle. (J) Medial condyle. (K–O) Specimen Campus 72. (K) Anterior view. (L) Inferior view. (M) Posterior view. (N) Lateral condyle. (O) Medial condyle. (P–T) Specimen Campus 86. (P) Anterior view. (Q) Inferior view. (R) Posterior view. (S) Lateral condyle. (T) Medial condyle. (U–Y) Specimen Campus 81. (U) Anterior view. (V) Inferior view. (W) Posterior view. (X) Lateral condyle. (Y) Medial condyle. All specimens are from the right side. In anterior and inferior views the medial condyle is on the right. In the posterior view the medial condyle is on the left. The location of the parasagittal slice through each condyle is indicated above and the main areas of interest are outlined. In Homo the slice is angled as it follows the orientation of the condyles and runs through the centre of each condyle. Individuals are scaled to the same data range.
Figure 8
Figure 8. Bone volume fraction (BV/TV) and degree of anisotropy (DA) results for each region and taxon.
(A) BV/TV in the lateral condyle. (B) BV/TV in the medial condyle. (C) DA in the lateral condyle. (D) DA in the medial condyle. Regions (outlined) and taxa are displayed below.
Figure 9
Figure 9. Trabecular number (Tb.N), separation (Tb.Sp) and thickness (Tb.Th) results for each region and taxon.
(A) Tb.N in the lateral condyle. (B) Tb.N in the medial condyle. (C) Tb.Sp in the lateral condyle. (D) TB.Sp in the medial condyle. (E) Tb.Th in the lateral condyle. (F) Tb.Th in the medial condyle. Regions (outlined) and taxa are displayed below. Taxa are presented in order of body mass (Pan the smallest; Gorilla the largest) to better visualise any patterns potentially associated with body size.
Figure 10
Figure 10. Results of principal components analysis of three trabecular variables (Tb.N, Tb.Sp. and DA) in all analysed regions.
PC1 is mainly driven by variation in trabecular separation, while PC2 is driven primarily by degree of anisotropy (also see Table S2 for loadings).
Figure 11
Figure 11. Inferior index for BV/TV and DA.
(A) BV/TV. (B) DA. Index >1 indicates higher BV/TV or DA in the distal region, whereas index <1 indicates higher values in the posteroinferior region.
Figure 12
Figure 12. Posterior index for BV/TV and DA.
(A) BV/TV. (B) DA. Index >1 indicates higher BV/TV or DA values in the posteroinferior region, whereas index <1 indicates higher values in the posterosuperior region.

Similar articles

See all similar articles

Cited by 1 article

References

    1. Ahrens J, Geveci B, Law C. ParaView: an end-user tool for large data visualization. In: Hansen CD, Johnson CR, editors. Visualization Handbook. Burlington: Butterworth-Heinemann; 2005. pp. 717–731.
    1. Alexander RMN. Characteristics and advantages of human bipedalism. In: Rayner JMV, Wooton RJ, editors. Biomechanics in Evolution. Cambridge: Cambridge University Press; 1991. pp. 225–266.
    1. Alexander RMN. Bipedal animals, and their differences from humans. Journal of Anatomy. 2004;204(5):321–330. doi: 10.1111/j.0021-8782.2004.00289.x. - DOI - PMC - PubMed
    1. Anderson FC, Pandy MG. Static and dynamic optimization solutions for gait are practically equivalent. Journal of Biomechanics. 2001;34(2):153–161. doi: 10.1016/s0021-9290(00)00155-x. - DOI - PubMed
    1. Ankel-Simons F. Primate Anatomy: An Introduction. Burlington: Academic Press; 2007.

Grant support

This research was supported by a 50th Anniversary Research Scholarship, University of Kent (Leoni Georgiou), European Research Council Starting Grant 336301 (Matthew M Skinner, Tracy L Kivell), and the Max Planck Society (Matthew M Skinner, Tracy L Kivell). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

LinkOut - more resources

Feedback