Effect of fatigue loading and associated matrix microdamage on bone blood flow and interstitial fluid flow

Muir, Peter; Sample, Susannah J.; Barrett, Jennifer G.; McCarthy, Jenna; Vanderby, Ray; Markel, Mark D.; Prokuski, Laura; Kalscheur, Vicki L.

doi:10.1016/j.bone.2006.11.012

Cited by 36 publications

(41 citation statements)

References 43 publications

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“…This finding is consistent with our recent report of a displacement-dependent increase in fluoride uptake within hours after fatigue loading in the same loading model [22]. We now attribute the elevated fluoride uptake in the first 4 days to increased blood flow, due in part to increased vascularity, a conclusion consistent with the findings of Muir et al [17]. However, we do not know what the mechanical stimulus is for the displacement-dependent response we observed.…”

Section: Discussionsupporting

confidence: 92%

“…That study appears to be the first one showing that angiogenesis is critical to exercise-induced osteogenesis. Recently, Muir et al used a similar loading method as we used and reported increased bone blood flow in the first 5 days following fatigue loading [17]. Our study indicates that these changes in blood flow after fatigue loading are associated with increased periosteal vascularity, and extends the results of the previous studies by quantifying the temporospatial changes in vascularity following loading to several levels of fatigue displacement.…”

Section: Discussionsupporting

confidence: 83%

“…Despite the critical link between angiogenesis and bone formation noted above, there is little known about changes in vascularity following repetitive skeletal loading. Treadmill running in rats has been shown to stimulate increases in vascularity and trabecular bone density [15,16], and increased blood flow in bone has been reported following fatigue loading [17]. To our knowledge, these are the only reports describing quantitative vascular responses to skeletal loading.…”

Section: Introductionmentioning

confidence: 98%

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Damaging Fatigue Loading Stimulates Increases in Periosteal Vascularity at Sites of Bone Formation in the Rat Ulna

et al. 2007

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Bone formation in a variety of contexts depends on angiogenesis, however there are few reports of the vascular response to osteogenic skeletal loading. We used the rat forelimb compression model to characterize vascular changes after fatigue loading. The right forelimbs of 72 adult rats were loaded cyclically in vivo to one of four displacement levels, to produce four discrete levels of ulnar damage. Rats were euthanized 3-14 days after loading and their vasculature perfused with silicone rubber. Transverse histological sections were cut along the ulnar diaphysis. We quantified vessel number, average vessel area, total vessel area and bone area. On day 3 we observed a dramatic periosteal expansion near the ulnar midshaft, with significant increases in periosteal vascularity; total vessel area was increased 250-450% (p<0.001). Vascularity remained elevated on days 7 and 14. Vessel number and average vessel area were not correlated (p=0.09) and contributed independently to total vascular increases. Bone area was not increased on day 3, but on days 7 and 14 was increased significantly in all displacement groups (p<0.01) due to periosteal woven bone formation. Vascular and bone changes depended on longitudinal location (p<0.001), with peak increases 2 mm distal to the midshaft. Vascular and bone changes also depended on displacement level (p<0.005), with greater increases at higher levels of fatigue displacement. We conclude that skeletal fatigue loading induces a rapid increase in periosteal vascularity, followed by an increase in bone area. The angiogenic-osteogenic response is spatially coordinated and scaled to the level of the mechanical stimulus.

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Section: Discussionsupporting

confidence: 92%

Section: Discussionsupporting

confidence: 83%

Section: Introductionmentioning

confidence: 98%

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Damaging Fatigue Loading Stimulates Increases in Periosteal Vascularity at Sites of Bone Formation in the Rat Ulna

et al. 2007

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“…5,37,38 In the present Figure 4. Average microstrains calculated for tibial cortical surfaces at proximal diaphyseal (1), mid-diaphyseal (2), and distal diaphyseal (3) anatomical regions (also represented as dotted lines on tibia illustration).…”

Section: Discussionsupporting

confidence: 44%

“…Fluid flow induced by mechanical deformation is hypothesized to stimulate bone cells via mechanotransduction and initiate bone remodeling. 4,5 Parameters often overlooked in this theory are the significant stimulatory effects bone blood flow has on interstitial bone fluid flow and influences of skeletal muscle contraction on bone circulation. When muscle contracts around bone, blood vessels outside and within muscle compartments are compressed, emptying the veins, and generating pressure waves through veins and arteries toward bone capillaries.…”

mentioning

confidence: 99%

Skeletal muscle contractions uncoupled from gravitational loading directly increase cortical bone blood flow rates in vivo

Caulkins

Ebramzadeh

Winet

2008

Journal Orthopaedic Research

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The direct and indirect effects of muscle contraction on bone microcirculation and fluid flow are neither well documented nor explained. However, skeletal muscle contractions may affect the acquisition and maintenance of bone via stimulation of bone circulatory and interstitial fluid flow parameters. The purposes of this study were to assess the effects of transcutaneous electrical neuromuscular stimulation (TENS)-induced muscle contractions on cortical bone blood flow and bone mineral content, and to demonstrate that alterations in blood flow could occur independently of mechanical loading and systemic circulatory mechanisms. Bone chamber implants were used in a rabbit model to observe real-time blood flow rates and TENS-induced muscle contractions. Video recording of fluorescent microspheres injected into the blood circulation was used to calculate changes in cortical blood flow rates. TENS-induced repetitive muscle contractions uncoupled from mechanical loading instantaneously increased cortical microcirculatory flow, directly increased bone blood flow rates by 130%, and significantly increased bone mineral content over 7 weeks. Heart rates and blood pressure did not significantly increase due to TENS treatment. Our findings suggest that muscle contraction therapies have potential clinical applications for improving blood flow to cortical bone in the appendicular skeleton. Keywords: bone blood flow; bone; muscle; bone healing A large body of evidence supports the premise that skeletal muscle contractions affect the acquisition and maintenance of bone mass. In general, muscle contraction loading of bone is not independent of physical activity or body weight forces, however, isolated contractions apply greater loads than do gravitational forces associated with weight and contribute to over 70% of the bending moments placed on bone. 1Animal models for disuse osteoporosis demonstrated that maintenance of muscle contraction within castimmobilized limbs via electrical stimulation resulted in a decreased rate of bone loss compared to nonstimulated immobilized animals.2,3 In tail-suspended rats, lowfrequency electrically stimulated contractions of the hindlimb muscles prevented bone loss compared to nonstimulated animals and further resulted in elevated periosteal and cancellous bone formation rates.3 Disuse created by casting rabbit hindlimbs with the ankle in plantarflexion caused a faster, more intensive rate of bone loss than casting with 908 joint angles.2 Plantarflexion was thought to inhibit contraction power of the calf muscles, thus reducing mechanical loading to the immobilized tibia. These findings support the hypothesis that skeletal muscle contractions play a significant role in bone homeostasis and adaptation. However, the specific mechanism remains unclear.Popular models for regulation of bone adaptation involve fluid flow. Fluid flow induced by mechanical deformation is hypothesized to stimulate bone cells via mechanotransduction and initiate bone remodeling. 4,5 Parameters often overlooked ...

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Systemic effects of ulna loading in male rats during functional adaptation

Sample

Collins

Wilson

et al. 2010

Journal of Bone and Mineral Research

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Functional skeletal adaptation is thought to be a local phenomenon controlled by osteoctyes. However, the nervous system also may have regulatory effects on adaptation. The aim of this study was to determine the effects of loading of a single bone on adaptation of other appendicular long bones and whether these responses were neuronally regulated. Young male Sprague-Dawley rats were used. The right ulna was loaded to induce a modeling response. In other rats, a second regimen was used to induce bone fatigue with a mixed modeling/remodeling response; a proportion of rats from each group received brachial plexus anesthesia to induce temporary neuronal blocking during bone loading. Sham groups were included. Left and right long bones (ulna, humerus, tibia, and femur) from each rat were examined histologically 10 days after loading. In fatigue- and sham-loaded animals, blood plasma concentrations of TNF-α, RANKL, OPG, and TRAP5b were determined. We found that loading the right ulna induced an increase in bone formation in distant long bones that were not loaded and that this effect was neuronally regulated. Distant effects were most evident in the rats that received loading without bone fatigue. In the fatigue-loaded animals, neuronal blocking induced a significant decrease in plasma TRAP5b at 10 days. Histologically, bone resorption was increased in both loaded and contralateral ulnas in fatigue-loaded rats and was not significantly blocked by brachial plexus anesthesia. In young, growing male rats we conclude that ulna loading induced increased bone formation in multiple bones. Systemic adaptation effects were, at least in part, neuronally regulated. © 2010 American Society for Bone and Mineral Research.

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Effect of fatigue loading and associated matrix microdamage on bone blood flow and interstitial fluid flow

Cited by 36 publications

References 43 publications

Damaging Fatigue Loading Stimulates Increases in Periosteal Vascularity at Sites of Bone Formation in the Rat Ulna

Damaging Fatigue Loading Stimulates Increases in Periosteal Vascularity at Sites of Bone Formation in the Rat Ulna

Skeletal muscle contractions uncoupled from gravitational loading directly increase cortical bone blood flow rates in vivo

Systemic effects of ulna loading in male rats during functional adaptation

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