Comparative forefoot trabecular bone architecture in extant hominids

Griffin, Nicole L.; D’Août, Kristiaan; Ryan, Timothy M.; Richmond, Brian G.; Ketcham, Richard A.; Постнов, А. А.

doi:10.1016/j.jhevol.2010.06.006

Cited by 67 publications

(102 citation statements)

References 41 publications

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“…The three main hypotheses proposed to explain the relatively gracile skeleton of contemporary humans include: (i) a reduction in physical activity because of increased sedentism and reliance on culture (1-6, 41), (ii) selection for systemic reduction of bone mass in modern humans (14,16), and (iii) attenuation of strain imposed upon trabecular bone because of larger joint surface areas (12,13). The morphological differences between the highly mobile foragers and relatively sedentary village agriculturalists clearly point to physical activity as a major determinant of bone mass in the hip joint.…”

Section: Discussionmentioning

confidence: 99%

“…Alternatively, it has been suggested that the low bone-volume fraction observed in human thoracic vertebrae and the first and second metatarsals are the result of systemic physiological differences between humans and apes (14,16). These studies do not suggest the mechanism or the function of this systemic gracility, but one potential explanation may be selection for increased tissue economy in hominins (5,(33)(34)(35).…”

Section: Significancementioning

confidence: 99%

“…The etiology of this relative gracility remains uncertain, and this uncertainty hinders the development of strategies for mitigating fracture risk and morbidity. The progressive gracilization of the Homo postcranial skeleton was originally detected in cortical bone structure (1, 2), but has now been demonstrated in the trabecular bone microstructure of joints (12,14,(16)(17)(18)(19), where osteoporotic fracture risk is highest (20). Most notably, in an analysis of thoracic vertebral bodies, Cotter et al (12) found that young adult humans have significantly lower trabecular bone volume fraction (BV/TV) and thinner vertebral shells than similarly sized apes.…”

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confidence: 99%

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Gracility of the modernHomo sapiensskeleton is the result of decreased biomechanical loading

Ryan

Shaw

2014

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

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162

195

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The postcranial skeleton of modern Homo sapiens is relatively gracile compared with other hominoids and earlier hominins. This gracility predisposes contemporary humans to osteoporosis and increased fracture risk. Explanations for this gracility include reduced levels of physical activity, the dissipation of load through enlarged joint surfaces, and selection for systemic physiological characteristics that differentiate modern humans from other primates. This study considered the skeletal remains of four behaviorally diverse recent human populations and a large sample of extant primates to assess variation in trabecular bone structure in the human hip joint. Proximal femur trabecular bone structure was quantified from microCT data for 229 individuals from 31 extant primate taxa and 59 individuals from four distinct archaeological human populations representing sedentary agriculturalists and mobile foragers. Analyses of mass-corrected trabecular bone variables reveal that the forager populations had significantly higher bone volume fraction, thicker trabeculae, and consequently lower relative bone surface area compared with the two agriculturalist groups. There were no significant differences between the agriculturalist and forager populations for trabecular spacing, number, or degree of anisotropy. These results reveal a correspondence between human behavior and bone structure in the proximal femur, indicating that more highly mobile human populations have trabecular bone structure similar to what would be expected for wild nonhuman primates of the same body mass. These results strongly emphasize the importance of physical activity and exercise for bone health and the attenuation of age-related bone loss. trabecular bone | gracilization | human evolution | biomechanics | mobility C ompared with other hominoids and extinct hominin species, more recent humans possess relatively gracile postcranial skeletons (1-9). One of the consequences of this gracility in contemporary humans is an increased fracture risk associated with age-related bone loss and osteoporosis [hip fractures alone are projected to reach 6.26 million per year globally by 2050 (10)] (11-15). The etiology of this relative gracility remains uncertain, and this uncertainty hinders the development of strategies for mitigating fracture risk and morbidity. The progressive gracilization of the Homo postcranial skeleton was originally detected in cortical bone structure (1, 2), but has now been demonstrated in the trabecular bone microstructure of joints (12,14,(16)(17)(18)(19), where osteoporotic fracture risk is highest (20). Most notably, in an analysis of thoracic vertebral bodies, Cotter et al. (12) found that young adult humans have significantly lower trabecular bone volume fraction (BV/TV) and thinner vertebral shells than similarly sized apes. Griffin et al. (16) also found significantly lower BV/TV in the human first and second metatarsal heads compared with hominoid primates. The results of these studies are corroborated by work on the hominoid...

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Section: Discussionmentioning

confidence: 99%

Section: Significancementioning

confidence: 99%

mentioning

confidence: 99%

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Gracility of the modernHomo sapiensskeleton is the result of decreased biomechanical loading

Ryan

Shaw

2014

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

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162

195

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“…Anisotropy in particular appears to be related to principal loading direction (42). Work to date suggests that in some anatomical regions, such as metatarsal heads, humans are characterized by higher degrees of anisotropy (36), but in others, such as metacarpal heads, humans and apes have comparable degrees of anisotropy (32). In both these cases, modern human joints are consistently low in TBF (32,36).…”

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.

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142

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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“…Comparative studies characterizing the microarchitecture of trabecular bone have consistently found that humans have a lower bone volume fraction (BV/TV) than chimpanzees. Whether in the humeral head (Shaw and Ryan, 2012;Scherf et al, 2013), first metacarpal head (Lazenby et al, 2011), thoracic vertebra (Cotter et al, 2011), femoral head (Shaw and Ryan, 2012), calcaneal body (Maga et al, 2006), talar body (DeSilva and Devlin, 2012), or medial metatarsal heads (Griffin et al, 2010), humans consistently possess lower BV/TV than chimpanzees. Under the Achilles tendon insertion, however, we found a trend towards slightly higher BV/TV in humans than in chimpanzees, though this trend was not statistically significant.…”

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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Comparative forefoot trabecular bone architecture in extant hominids

Cited by 67 publications

References 41 publications

Gracility of the modernHomo sapiensskeleton is the result of decreased biomechanical loading

Gracility of the modernHomo sapiensskeleton is the result of decreased biomechanical loading

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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