Trabecular bone adapts to long-term cyclic loading by increasing stiffness and normalization of dynamic morphometric rates

Lambers, Floor M.; Koch, Kathleen; Kuhn, Gisela; Ruffoni, Davide; Weigt, Claudia; Schulte, Friederike A.; Müller, Ralph

doi:10.1016/j.bone.2013.04.016

Cited by 49 publications

(48 citation statements)

References 38 publications

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“…We agree that inferences for humanlike hand use among australopiths referred to by Almécija et al are neither "unprecedented nor unexpected" (1). However, the inferences we can now make, based on the trabecular bone distribution and the well-accepted concept that trabeculae remodel in response to habitual load during an individual's lifetime (4,5), are much stronger than they and others have been able to make based on external morphology of hand bones alone.…”

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confidence: 61%

Response to Comment on “Human-like hand use in Australopithecus africanus ”

Skinner

Stephens

Tsegai

et al. 2015

Science

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Almécija and colleagues claim that we apply a simplified understanding of bone functional adaptation and that our results of human-like hand use in Australopithecus africanus are not novel. We argue that our results speak to actual behavior, rather than potential behaviors, and our functional interpretation is well supported by our methodological approach, comparative sample, and previous experimental data.A lmécija et al.(1) challenge our conclusions on three points: (i) we do not give sufficient credence to published studies on the external morphology of australopith hand bones that are consistent with precision grip capabilities; (ii) we overstate the evidence for a form-function signal in trabecular bone; and (iii) our comparative sample and analyses do not support differences in trabecular patterning between humans and extant apes. Their critique suffers from a lack of recognition that (i) our study provides evidence for hand postures actually adopted by australopiths, rather than those they were potentially capable of; (ii) we base our conclusions on the three-dimensional distribution of trabecular bone throughout the epiphysis rather than on particular measures of subregions of trabecular structure; and (iii) our comparative sample, which includes stone toolusing Taï chimpanzees, indicates that humans have a distinctive trabecular pattern that is shared with Neandertals and Australopithecus africanus (2).We do not claim that our results "refute the previously existing hypothesis that human-like manipulation preceded systematized stone tool manufacture" (1); to the contrary, we state that our results are consistent with the use of "forceful hand grips for any number of manipulative behaviors" (2). Almécija et al.(1) refer to previous studies (mainly their own) based on the relative lengths and external morphology of hand bones that "have provided compelling evidence for padto-pad precision grasping before the widespread occurrence of flaked stone tools" (1) and that australopiths and earlier hominins "were likely capable of human-like manipulation" (1). We agree; however, Almécija et al.(1) fail to acknowledge that our results are novel because they reflect (i) actual behavior, rather than the capability for particular behaviors and (ii) forceful pad-to-pad precision grasping, which is what separates human dexterity from that of other primates (3). The asymmetric distribution of trabecular bone within the base of the thumb and metacarpal heads in humans, Neandertals, and A. africanus (and the absence of this pattern in apes) provides evidence for habitual, forceful opposition of the thumb to the fingers. We agree that inferences for humanlike hand use among australopiths referred to by Almécija et al. are neither "unprecedented nor unexpected" (1). However, the inferences we can now make, based on the trabecular bone distribution and the well-accepted concept that trabeculae remodel in response to habitual load during an individual's lifetime (4, 5), are much stronger than they and others have been able to...

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supporting

confidence: 61%

Response to Comment on “Human-like hand use in Australopithecus africanus ”

Skinner

Stephens

Tsegai

et al. 2015

Science

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“…Previous studies into trabecular bone formation in response to strain have demonstrated an in vivo correlation in a mouse model between bone strain and trabecular bone formation. 27,28 Results from the current study demonstrate that 2.2-12.1% of the total bone in the compressively loaded samples was experiencing between 1000 and 3000 le. This increased to 4.3-17.4% when just the bone surface was examined.…”

Section: Discussionmentioning

confidence: 86%

An Experimental and Computational Investigation of Bone Formation in Mechanically Loaded Trabecular Bone Explants

et al. 2015

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Understanding how bone marrow multipotent stromal cells (MSCs) contribute to new bone formation and remodeling in vivo is of principal importance for informing the development of effective bone tissue engineering strategies in vitro. However, the precise in situ stimuli that MSCs experience have not been fully established. The shear stress generated within the bone marrow of physiologically loaded samples has never been determined, but could be playing an important role in the generation of sufficient stimulus for MSCs to undergo osteogenic differentiation. In this study fluid structure interaction (FSI) computational models were used in conjunction with a bioreactor which physiologically compresses explanted trabecular bone samples to determine whether MSCs can be directly stimulated by mechanical cues within the bone marrow. Experimentally loaded samples were found to have greater osteogenic activity, as verified by bone histomorphometry, compared to control static samples. FSI models demonstrated a linear relationship between increasing shear stress and decreasing bone volume. The FSI models demonstrated that bone strain, not marrow shear stress, was likely the overall driving mechanical signal for new bone formation during compression. However, the shear stress generated in the models is within the range of values which has been shown previously to generate an osteogenic response in MSCs.

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“…Thanks to the development of X‐ray computed microtomography, 3D trabecular architecture could be extensively studied in birds (e.g., Bishop et al, ; Doube, Kłosowski, Wiktorowicz‐Conroy, Hutchinson, & Shefelbine, ; Fajardo, Hernandez, & O'Connor, ; Pontzer et al, ) and mammals (e.g., many orders [Doube et al, ], bovids [Mittra, Rubin, & Qin, , Sode, Burghardt, Nissenson, & Majumdar, ], lagomorphs [Marchand, Chen, Buschmann, & Hoemann, , van der Meulen et al, ], primates [Barak, Lieberman, Raichlen, et al, , Cunningham & Black, , Kivell, Skinner, Lazenby, & Hublin, , Lazenby, Skinner, Kivell, & Hublin, , Sode et al, ], rodents [Carlson, Lublinsky, & Judex, , Lambers et al, , Sode et al, ], sciuromorphs [Mielke et al, ], suids [Ben‐Zvi, Reznikov, Shahar, & Weiner, ], and xenarthrans [Amson et al, ]). In comparison, 3D trabecular architecture of nonavian reptiles has received little attention.…”

Section: Introductionmentioning

confidence: 99%

Trabecular architecture in the humeral metaphyses of non‐avian reptiles (Crocodylia, Squamata and Testudines): Lifestyle, allometry and phylogeny

Plasse

Amson

Bardin

et al. 2019

Journal of Morphology

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The lifestyle of extinct tetrapods is often difficult to assess when clear morphological adaptations such as swimming paddles are absent. According to the hypothesis of bone functional adaptation, the architecture of trabecular bone adapts sensitively to physiological loadings. Previous studies have already shown a clear relation between trabecular architecture and locomotor behavior, mainly in mammals and birds. However, a link between trabecular architecture and lifestyle has rarely been examined. Here, we analyzed trabecular architecture of different clades of reptiles characterized by a wide range of lifestyles (aquatic, amphibious, generalist terrestrial, fossorial, and climbing). Humeri of squamates, turtles, and crocodylians have been scanned with microcomputed tomography. We selected spherical volumes of interest centered in the proximal metaphyses and measured trabecular spacing, thickness and number, degree of anisotropy, average branch length, bone volume fraction, bone surface density, and connectivity density. Only bone volume fraction showed a significant phylogenetic signal and its significant difference between squamates and other reptiles could be linked to their physiologies. We found negative allometric relationships for trabecular thickness and spacing, positive allometries for connectivity density and trabecular number and no dependence with size for degree of anisotropy and bone volume fraction. The different lifestyles are well separated in the morphological space using linear discriminant analyses, but a cross‐validation procedure indicated a limited predictive ability of the model. The trabecular bone anisotropy has shown a gradient in turtles and in squamates: higher values in amphibious than terrestrial taxa. These allometric scalings, previously emphasized in mammals and birds, seem to be valid for all amniotes. Discriminant analysis has offered, to some extent, a distinction of lifestyles, which however remains difficult to strictly discriminate. Trabecular architecture seems to be a promising tool to infer lifestyle of extinct tetrapods, especially those involved in the terrestrialization.

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Trabecular bone adapts to long-term cyclic loading by increasing stiffness and normalization of dynamic morphometric rates

Cited by 49 publications

References 38 publications

Response to Comment on “Human-like hand use in Australopithecus africanus ”

Response to Comment on “Human-like hand use in Australopithecus africanus ”

An Experimental and Computational Investigation of Bone Formation in Mechanically Loaded Trabecular Bone Explants

Trabecular architecture in the humeral metaphyses of non‐avian reptiles (Crocodylia, Squamata and Testudines): Lifestyle, allometry and phylogeny

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