Trabecular bone in the bird knee responds with high sensitivity to changes in load orientation

Pontzer, Herman; Lieberman, Daniel E.; Momin, E.N.; Devlin, Maureen J.; Polk, John D.; Hallgrímsson, Benedikt; Cooper, David M.L.

doi:10.1242/jeb.01971

Cited by 169 publications

(192 citation statements)

References 29 publications

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“…Here, the transfer of vertical loading forces into tensile forces while standing and walking might have prevented major age-related bone deteriorations. Hence, the ROI-specific bone loss might be the result of different mechanical loading conditions [5,7,35]. Because the distribution of compressive and tensile forces through the talus does not severely change with age, we speculate that the differently sized volumes of interest might be responsible for the greater bone loss in the body [34].…”

Section: Discussionmentioning

confidence: 97%

Bone Microarchitecture of the Talus Changes With Aging

Krause

Rupprecht

Mumme

et al. 2013

Clinical Orthopaedics &Amp; Related Research

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Background Fractures of the talus in the elderly are rare and usually result from high-impact injuries, suggesting only minor age-related bone structure changes. However, total ankle replacement failures with age often result from talar subsidence, suggesting age-related bone loss in the talus. Despite a number of histological analyses of talar microarchitecture, the effects of age and sex on talar microarchitecture changes remain poorly defined.Questions/purposes The aim of this study was to analyze changes or differences in the trabecular microarchitecture of the talus with regard to (1) age and (2) sex. Methods Sixty human tali were harvested from 30 patients at autopsy of three different age groups (20-40, 41-60, 61-80 years). The specimens were analyzed by radiography, micro-CT, and histological analysis. Given that there was no difference between the left and right talus, static histomorphometric parameters were assessed in three regions of interest of the right talus only (body, neck, head; n = 30). Results The talar body, neck, and head were affected differently by age-related changes. The greatest loss of bone volume with age was seen in the talar body (estimate: À0.239; 95% confidence interval [CI], À0.365 to À0.114; p \ 0.001). In the talar neck (estimate: À0.165; 95% CI, À0.307 to À0.023; p = 0.025), bone loss was only moderate and primarily was the result of reduction in trabecular thickness (estimate: À1.288; 95% CI, À2.449 to À0.127; p = 0.031) instead of number (estimate: À0.001; 95% CI, À0.005 to À0.003; p = 0.593). Bone structure changes were independent of sex. Conclusions Age-related bone structure changes predominantly occur in the talar body, which poses a potential risk factor for total ankle replacement loosening. The moderate changes in the talar neck might explain the persistent low incidence of talar neck fractures with age.

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Section: Discussionmentioning

confidence: 97%

Bone Microarchitecture of the Talus Changes With Aging

Krause

Rupprecht

Mumme

et al. 2013

Clinical Orthopaedics &Amp; Related Research

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“…Also, although mechanical loading can affect trabecular growth (23,46,47), direct developmental influences may not account entirely for the marked differences in trabecular density in recent modern humans and pre-Holocene hominins. It is plausible that, as sedentism became prevalent and food sources changed in the Holocene, selection pressure for robust skeletons diminished.…”

Section: Discussionmentioning

confidence: 99%

Recent origin of low trabecular bone density in modern humans

Chirchir

Kivell

Ruff

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

133

168

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Humans are unique, compared with our closest living relatives (chimpanzees) and early fossil hominins, in having an enlarged body size and lower limb joint surfaces in combination with a relatively gracile skeleton (i.e., lower bone mass for our body size). Some analyses have observed that in at least a few anatomical regions modern humans today appear to have relatively low trabecular density, but little is known about how that density varies throughout the human skeleton and across species or how and when the present trabecular patterns emerged over the course of human evolution. Here, we test the hypotheses that (i) recent modern humans have low trabecular density throughout the upper and lower limbs compared with other primate taxa and (ii) the reduction in trabecular density first occurred in early Homo erectus, consistent with the shift toward a modern human locomotor anatomy, or more recently in concert with diaphyseal gracilization in Holocene humans. We used peripheral quantitative CT and microtomography to measure trabecular bone of limb epiphyses (long bone articular ends) in modern humans and chimpanzees and in fossil hominins attributed to Australopithecus africanus, Paranthropus robustus/ early Homo from Swartkrans, Homo neanderthalensis, and early Homo sapiens. Results show that only recent modern humans have low trabecular density throughout the limb joints. Extinct hominins, including pre-Holocene Homo sapiens, retain the high levels seen in nonhuman primates. Thus, the low trabecular density of the recent modern human skeleton evolved late in our evolutionary history, potentially resulting from increased sedentism and reliance on technological and cultural innovations. trabecular bone | human evolution | gracilization | Homo sapiens | sedentism O bligate bipedalism-a defining feature of humans that distinguishes us from our closest living relatives, the African apes-has transformed the human skeleton. Among these unique features are long lower limbs with large joint surfaces. These large joint surfaces help distribute loads over a larger surface area and thus are better at resisting the high forces incurred during locomotion on two limbs instead of four (1-5). Early African Homo erectus at 1.8-1.5 Ma had enlarged lower limb joint surfaces (1, 3) and a larger stature (6) and body mass (7, 8) than many earlier hominins, and this pattern often is considered to reflect the emergence of a more modern human-like body plan (1, 3, 5, 6, 9; but also see ref. 7).Recent modern human (Holocene Homo sapiens) skeletons also appear to be gracile as compared with earlier hominins (10-14). Here, "gracilization" refers to the reduction in strength and bone mass relative to body mass inferred from osseous tissue and overall bone size and has been studied mainly using diaphyseal cortical bone cross-sections (10-16). Although the relationship between mechanical loading during life and bone strength is likely to be complex (17), there is much evidence that increased mechanical loading leads to increases in relative ...

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“…Alternatively, if our model for how the Achilles tendon loads calcaneal trabecular bone is correct, then our findings contradict some predictions of Wolff's "Law." Although many have found evidence for trabecular bone adaptation to changes in diet and hormones (Hodgkinson et al, 1978;Reeve et al, 1980;Devlin et al, 2010), and loading (Pontzer et al, 2006;Barak et al, 2011), others (Fajardo et al, 2007;Ryan and Walker, 2010;Shaw and Ryan, 2012;DeSilva and Devlin, 2012) have found the relationship between trabecular bone and inferred mechanical loading in primates to be more complicated. Although trabecular bone clearly is responsive to a variety of factors, Achilles tendon length may not affect trabecular properties as we had predicted.…”

Section: Discussionmentioning

confidence: 99%

The Effect of the Achilles Tendon on Trabecular Structure in the Primate Calcaneus

Kuo

DeSilva

Devlin

et al. 2013

The Anatomical Record

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Humans possess the longest Achilles tendon relative to total muscle length of any primate, an anatomy that is beneficial for bipedal locomotion. Reconstructing the evolutionary history of the Achilles tendon has been challenging, in part because soft tissue does not fossilize. The only skeletal evidence for Achilles tendon anatomy in extinct taxa is the insertion site on the calcaneal tuber, which is rarely preserved in the fossil record and, when present, is equivocal for reconstructing tendon morphology. In this study, we used high-resolution three-dimensional microcomputed tomography (micro-CT) to quantify the microstructure of the trabecular bone underlying the Achilles tendon insertion site in baboons, gibbons, chimpanzees, and humans to test the hypothesis that trabecular orientation differs among primates with different tendon morphologies. Surprisingly, despite their very different Achilles tendon lengths, we were unable to find differences between the trabecular properties of chimpanzee and human calcanei in this specific region. There were regional differences within the calcaneus in the degree of anisotropy (DA) in both chimpanzees and humans, though the patterns were similar between the two species (higher DA inferiorly in the calcaneal tuber). Our results suggest that while trabecular bone within the calcaneus varies, it does not respond to the variation of Achilles tendon morphology across taxa in the way we hypothesized. These results imply that internal bone architecture may not be informative for reconstructing Achilles tendon anatomy in early hominins. Anat Rec, 296:1509Rec, 296: -1517Rec, 296: , 2013. V C 2013 Wiley Periodicals, Inc.

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Trabecular bone in the bird knee responds with high sensitivity to changes in load orientation

Cited by 169 publications

References 29 publications

Bone Microarchitecture of the Talus Changes With Aging

Bone Microarchitecture of the Talus Changes With Aging

Recent origin of low trabecular bone density in modern humans

The Effect of the Achilles Tendon on Trabecular Structure in the Primate Calcaneus

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