Haversian remodeling corresponds to load frequency but not strain magnitude in the macaque (Macaca fascicularis) skeleton

Lad, Susan E.; McGraw, W. Scott; Daegling, David J.

doi:10.1016/j.bone.2019.07.027

Cited by 12 publications

(10 citation statements)

References 59 publications

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“…In comparison, strains below the 100-300 microstrain range activate bone resorption, which reduces unnecessary bone that is metabolically expensive. Low strain magnitudes acting at high frequency are also important in promoting bone formation ( 28 , 29 ). For this to occur, bone cells responsible for bone deposition and resorption must sense such changes in mechanical stimuli.…”

Section: Biomechanical Interaction Between Muscles and Bones In The Mmentioning

confidence: 99%

Muscle-Bone Crosstalk in the Masticatory System: From Biomechanical to Molecular Interactions

et al. 2021

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The masticatory system is a complex and highly organized group of structures, including craniofacial bones (maxillae and mandible), muscles, teeth, joints, and neurovascular elements. While the musculoskeletal structures of the head and neck are known to have a different embryonic origin, morphology, biomechanical demands, and biochemical characteristics than the trunk and limbs, their particular molecular basis and cell biology have been much less explored. In the last decade, the concept of muscle-bone crosstalk has emerged, comprising both the loads generated during muscle contraction and a biochemical component through soluble molecules. Bone cells embedded in the mineralized tissue respond to the biomechanical input by releasing molecular factors that impact the homeostasis of the attaching skeletal muscle. In the same way, muscle-derived factors act as soluble signals that modulate the remodeling process of the underlying bones. This concept of muscle-bone crosstalk at a molecular level is particularly interesting in the mandible, due to its tight anatomical relationship with one of the biggest and strongest masticatory muscles, the masseter. However, despite the close physical and physiological interaction of both tissues for proper functioning, this topic has been poorly addressed. Here we present one of the most detailed reviews of the literature to date regarding the biomechanical and biochemical interaction between muscles and bones of the masticatory system, both during development and in physiological or pathological remodeling processes. Evidence related to how masticatory function shapes the craniofacial bones is discussed, and a proposal presented that the masticatory muscles and craniofacial bones serve as secretory tissues. We furthermore discuss our current findings of myokines-release from masseter muscle in physiological conditions, during functional adaptation or pathology, and their putative role as bone-modulators in the craniofacial system. Finally, we address the physiological implications of the crosstalk between muscles and bones in the masticatory system, analyzing pathologies or clinical procedures in which the alteration of one of them affects the homeostasis of the other. Unveiling the mechanisms of muscle-bone crosstalk in the masticatory system opens broad possibilities for understanding and treating temporomandibular disorders, which severely impair the quality of life, with a high cost for diagnosis and management.

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Section: Biomechanical Interaction Between Muscles and Bones In The Mmentioning

confidence: 99%

Muscle-Bone Crosstalk in the Masticatory System: From Biomechanical to Molecular Interactions

et al. 2021

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“…Rabbits that process an overuse diet that includes tough and stiff hay do not have more secondary osteons or more secondary bone than conspecifics raised on a control diet of only pellets. This is surprising given that previous studies (Lad et al, 2016; Lad et al, 2019) suggest that substantial remodeling is generated by repetitive loading in the absence of high strain.…”

Section: Discussionmentioning

confidence: 80%

“…First, the answer could simply be that repetitive loading does not generate substantial remodeling activity unless strains are above a certain magnitude and that magnitude was not reached in the present experiment. This explanation seems unlikely given past results from wild samples (Lad et al, 2016; Lad et al, 2019) and given the fact that bone cells are capable of responding to low strain loads in regards to uncoupled bone formation and resorption in this model system (Franks et al, 2017; Menegaz et al, 2009; Scott et al, 2014a) and others (Gilsanz et al, 2006; Judex et al, 2007; Rubin et al, 2001; Xie et al, 2006). Second, we have assumed that if deformation occurs then microdamage will accumulate, but this could be faulty.…”

Section: Discussionmentioning

confidence: 90%

“…Interestingly, humeri of all species had more remodeling than femora despite greater peak loads in the hindlimbs compared to forelimbs. In an attempt to parse the effects of strain magnitude and cyclical loading on remodeling across the skeleton, Lad et al, (2019) found the highest incidence of remodeling in the ribs, which experience cyclical loading but very low strains compared to the limbs. Combined, these findings suggest that high strain may not be necessary for substantial remodeling to occur and that cyclical loading may be more likely to result in elevated remodeling.…”

Section: Introductionmentioning

confidence: 99%

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Bone remodeling and cyclical loading in maxillae of New Zealand white rabbits (Oryctolagus cuniculus)

Lad

Anderson

Cortese

et al. 2021

The Anatomical Record

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Mammalian feeding behaviors are altered when mechanically challenging (e.g., tough, stiff) foods require large bite forces or prolonged mastication. Bony responses to high bite forces are well‐documented for the mammalian skull, but osteogenesis due to cyclical loading, caused by repetitive chewing, is more poorly understood. Previous studies demonstrate that cyclical loading results in greater bone formation in the rabbit masticatory apparatus and in substantial Haversian remodeling in primate postcrania. Here we assess the relationship between cyclical loading and remodeling in the rabbit maxilla. Twenty male New Zealand white rabbits (Oryctolagus cuniculus) were raised on either an overuse or control diet (10 per group) for 48 weeks, beginning at weaning onset. The control group was raised on a diet of rabbit pellets (E = 29 MPa, R = 1031 J/m2), whereas the overuse group ate rabbit pellets and hay, which has high stiffness (E = 3336 MPa) and toughness (R = 2760 J/m2) properties. Hay requires greater chewing investment (475 chews/g) and longer chewing durations (568 s/g) than pellets (161 chews/g and 173 s/g), therefore causing cyclical loading of the jaws. Remodeling was measured as osteon population density (OPD), percent Haversian bone (%HAV), and osteon cross‐sectional area (On.Ar). The only significant difference found was greater On.Ar in the alveolar region of the maxilla (p < 0.001) in the overuse group. The hypothesis that cyclical loading engenders Haversian remodeling in the developing maxilla is not supported. The continuation of modeling throughout the experimental duration may negate the need for remodeling as newly laid bone tends to be more compliant and resistant to crack propagation.

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“…Skedros et al (2013) collated secondary osteon size and bone volume data for the rib and various lower limb bones (femora, metatarsals, calcanei, radii, humeri, metacarpals) from a range of human and non-human animals including deer (O. hemionus, O. virginianus), sheep (O. aries), elk (C. elaphus), and black bear (U. americanus) (see Table 1 in Skedros et al 2013 for full details of specimens), to find that bone histological markers and Stewart et al ASI 2020 R2 4 volume did not consistently follow the expectation that metabolic homeostasis is preferentially maintained at the rib. However, rib tissue in the macaque (Macaca fascicularis), when compared against the femur, tibia, and fibula (Lad et al 2019); and in archeological human remains when contrasted against femur, tibia, humerus, metacarpal, occipital bone, pelvis, clavicle, radius, and thoracic vertebrae samples (Fahy et al 2017), did show microscopic evidence for high remodeling trends intra-skeletally. To the best of our knowledge, no studies have yet used histology to evaluate rib vascularity intra-skeletally in a macropod model adapted to habitual bipedal hopping.…”

Section: Introductionmentioning

confidence: 97%

Intra-skeletal vascular density in a bipedal hopping macropod with implications for analyses of rib histology

2021

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Human ribs are thought to be less affected by mechanical strain at the microscopic level than limb bones, implying that rib remodeling better reflects bone physiological homeostasis. Here, we test the hypothesis that rib tissue will be well vascularized and thus enhance susceptibility to metabolic influence. An intra-skeletal comparison of bone vascular canal density was conducted using a macropod animal model adapted to bipedal habitual hopping. The right humerus, ulna, radius, femur, tibia, fibula, a mid-thoracic and upper-thoracic rib of an eastern grey kangaroo (Macropus giganteus) were sectioned at the midshaft, from which histological sections were prepared. Bone vascularity from a maximum of 12 mm 2 of sub-periosteal parallel-fibred and lamellar bone was recorded, resulting in a total of 2,047 counted vessels. Vascular canal density data were corrected by cortical width, maximum length, and midshaft circumference robusticity indices computed for each bone. The fibula consistently had the highest vascular canal density, even when corrected for maximum length, cortical width and midshaft circumference robusticities. This was followed by the mid-and upperthoracic ribs. Vascularity differences between bones were relatively consistent whether vascular canal density was controlled for by cortical width or midshaft circumference robusticities. Vascular canal density and robusticity indices were also positively and negatively correlated (p < 0.05). Results confirm that the ribs are well vascularized, which facilitates bone metabolic processes such as remodeling, but the fibula also appears to be a well vascularized bone. Future research investigating human bone metabolism will benefit from examining thoracic rib or fibula samples.

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Haversian remodeling corresponds to load frequency but not strain magnitude in the macaque (Macaca fascicularis) skeleton

Cited by 12 publications

References 59 publications

Muscle-Bone Crosstalk in the Masticatory System: From Biomechanical to Molecular Interactions

Muscle-Bone Crosstalk in the Masticatory System: From Biomechanical to Molecular Interactions

Bone remodeling and cyclical loading in maxillae of New Zealand white rabbits (Oryctolagus cuniculus)

Intra-skeletal vascular density in a bipedal hopping macropod with implications for analyses of rib histology

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