Elsevier

Bone

Volume 47, Issue 4, October 2010, Pages 746-755
Bone

Effect of whole-body vibration on bone properties in aging mice

https://doi.org/10.1016/j.bone.2010.07.014Get rights and content

Abstract

Recent studies suggest that whole-body vibration (WBV) can improve measures of bone health for certain clinical conditions and ages. In the elderly, there also is particular interest in assessing the ability of physical interventions such as WBV to improve coordination, strength, and movement speed, which help prevent falls and fractures and maintain ambulation for independent living. The current study evaluated the efficacy of WBV in an aging mouse model. Two levels of vibration — 0.5 and 1.5 g — were applied at 32 Hz to CB57BL/6 male mice (n = 9 each) beginning at age 18 months and continuing for 12 weeks, 30 min/day, in a novel pivoting vibration device. Previous reports indicate that bone parameters in these mice begin to decrease substantially at 18 months, equivalent to mid-fifties for humans. Micro-computed tomography (micro-CT) and biomechanical assessments were made in the femur, radius, and lumbar vertebra to determine the effect of these WBV magnitudes and durations in the aging model. Sera also were collected for analysis of bone formation and breakdown markers. Mineralizing surface and cell counts were determined histologically.

Bone volume in four regions of the femur did not change significantly, but there was a consistent shift toward higher mean density in the bone density spectrum (BDS), with the two vibration levels producing similar results. This new parameter represents an integral of the conventional density histogram. The amount of high density bone statistically improved in the head, neck, and diaphysis. Biomechanically, there was a trend toward greater stiffness in the 1.5 g group (p = 0.139 vs. controls in the radius), and no change in strength. In the lumbar spine, no differences were seen due to vibration. Both vibration groups significantly reduced pyridinoline crosslinks, a collagen breakdown marker. They also significantly increased dynamic mineralization, MS/BS. Furthermore, osteoclasts were most numerous in the 1.5 g group (p  0.05). These findings suggest that some benefits of WBV found in previous studies of young and mature rodent models may extend to an aging population. Density parameters indicated 0.5 g was more effective than 1.5 g. Serological markers, by contrast, favored 1.5 g, while biomechanically and histologically the results were mixed. Although the purported anabolic effect of WBV on bone homeostasis may depend on location and the parameter of interest, this emerging therapy at a minimum does not appear to compromise bone health by the measures studied here.

Introduction

Therapeutic whole-body vibration (WBV) has been shown to mitigate bone loss and improve neuromuscular function in certain clinical studies. Bone quality issues, in particular, are a significant concern for post-menopausal women and the aging population in general. In these groups there is increased risk of fracture primarily from repeated falls on the hip, and spontaneous vertebral body collapse as a sequela to osteoporosis. In one study, early post-menopausal women experiencing 10 min of low-level WBV (0.2 g, where 1 g = acceleration due to gravity, 9.81 m/s2) twice daily for one year showed retention of bone mineral density (BMD), whereas controls showed a loss of 2–3% [1]. Extrapolated over the full period of sharp decline for such a cohort, the finding suggests a potential for substantial improvement in the prognosis for aging bone health. This result was similar to the difference found in a study of related subjects comparing resistance training to light exercise on a WBV platform at high accelerations (2.3–5.1 g). Over six months there was a significant 1% increase in BMD in the WBV group, whereas both the control and resistance training groups were statistically unchanged, with slight mean decreases. [2].

In the elderly, WBV of 0.6–9.5 g added to a physical therapy regimen was shown in one study to improve balance as well as speed of rising from a seated position, whereas physical therapy alone did not improve these measures [3]. Similar intervention with WBV at a less elderly age also has demonstrated beneficial effects [4]. A more recent study in elderly women found that high-magnitude WBV up to 4.3 g, applied for 3 min/day for 3 months, improved movement speed, maximum excursion, and directional control [5]. At a lower magnitude of 0.3 g, however, a similar cohort recently showed no difference in excursion and control, although BMD was better retained than in controls [6]. Propensity to fall has been shown to be equally mitigated in elderly men due to either WBV for short-durations of 0.5–1 min at 6.2–16.1 g or a more rigorous exercise regimen [7]. Prevention of falls can be a significant prophylaxis against femoral neck fractures, in particular. Many study designs, notably in the field of sports science, have examined the relative effect of WBV either in direct comparison to or in combination with various exercise routines. One such study in elderly females, using a similar protocol to that of [7], found improvements in strength and counter-movement jump performance to be similar between WBV and resistance training groups [8]. This suggested that the retention of neuromuscular health in aging may not require the physical demands of a disciplined exercise regimen.

Rodent models commonly have indicated a qualified anabolic response, in which WBV often induces increased bone formation rate and remodeling, but at restricted anatomical sites. The quality of the bone improves selectively, and the degree to which signaling is sustained is equivocally reported. For instance, a 5-week study in adult mice subjected to 1 g of WBV resulted in an increase in the ratio of bone volume to tissue volume (BV/TV) of 43% in the proximal tibia [9]. Yet there was no difference in BV/TV in the femoral condyles, distal femoral metaphysis, proximal femur, or L5 vertebral body. Mineralizing surface was found in a study of adult BALB mice to increase 75% in the proximal tibia trabecular metaphysis due to WBV of 0.3 g, but was effectively unchanged in the epiphysis [10]. Periosteal and bone marrow area also increased with WBV, along with type I and especially type II muscle fiber area. Recently, a study comparing adult to aged BALB/c mice showed that WBV increased bone mineral content (BMC) in the lower leg at a low-amplitude WBV of 0.3 g in both ages, but only in the adult mice at a high-amplitude WBV of 1.0 g [11]. This appears to be the first report on the effect of WBV in an aging model.

Current literature suggests a provisional consensus is building toward low-amplitude, high-frequency vibration as the most effective and least invasive form for therapeutic stimulation. This combination is thought to approximate the subtle in vivo stress of nominal basal twitch in some muscles. The less-is-more movement has extended down to nano-intensity levels, in which bone strains as low as 10 micro-strain (1 part in 100,000) have been shown to effect an anabolic response [10]. Certainly, high-amplitude vibration has unwanted consequences when chronically applied, as noted by a generation of studies correlating low back pain and other ailments to occupational vibration [12], [13], [14]. Such high-amplitude vibration also is often found in efficacy studies from the sports and exercise science field. The recent application of WBV to the health care population, however, normally operates at a categorically lower level of stimulation, as this less invasive realm has proven to be effective in some areas, as well, while it enhances safety.

The goal of the current study was to bridge the low- and medium-amplitude protocols of recent investigations in determining the degree to which WBV can influence the aging process of the skeleton, which normally is associated with significant bone loss. The two vibration amplitudes have been shown to be well tolerated clinically and in rodents. The model was C57BL/6 male mice, which are available at advanced age and provide an efficient means to stimulate and assay a statistically useful sample size. WBV was applied by a novel vibration device operating on a single pivot axis. This design produces a continuum of acceleration across the vibrating surface, allowing multiple acceleration magnitudes to be applied simultaneously for a given frequency through varying displacement amplitudes. The analysis of the study focused on both established and new measurement tools for characterizing morphological, structural, and biomechanical changes in the femur, radius, and spine of the experimental groups, along with serological markers and histological parameters.

Section snippets

Specimens

C57BL/6 male mice were obtained from Harlan Sprague Dawley, Inc. (Indianapolis, IN) at 17 months of age, and allowed 1 month to acclimate to our facility until the starting age of the study at 18 months. Initial mean weight was 28.1 g. Three groups of 9 mice each were formed, with 3 mice housed in each 11 × 7-inch cage and fed ad libidum. One group received 0.5 g at 32 Hz for 30 min/day, 5 day/week, for 3 months (LOW). A second group received 1.5 g at 32 Hz for the same period (HIGH). A third group was not

Monitoring

Mean weight of the CTRL and HIGH groups changed by less than 0.1 g over the 3-month course of the study, while that of the LOW group was reduced by 0.3 g (not significant; NS). Food intake followed a similar pattern in all three groups, with slight fluctuation in the first few weeks, then stable consumption for the duration of the study. One mouse from the CTRL group had to be euthanized due to an infection surrounding the eye. No behavioral changes were readily evident either due to aging or as

Discussion

This study aimed to further establish the degree to which whole-body vibration influences bone health, in this case in an aging population. Based on lifespan, the 18-month starting age of the mice was equivalent to the human age of mid-fifties. The ending age of 21 months was equivalent to mid-sixties in humans. The study sought, furthermore, to differentiate between conventionally low and medium acceleration amplitudes, as a considerable disparity still exists in the range of vibrational forces

Acknowledgments

This work was financially supported by the Medical College of Georgia School of Medicine, Department of Orthopaedic Surgery and Section of Plastic Surgery. The authors wish to thank: 1) Greg White, MCG Laboratory Equipment Services, for machining expertise and mechanical design consultation; 2) Eddie Estochen, Savannah River National Laboratory, for accelerometer testing support; and 3) David H. Pashley, DMD, MCG School of Dentistry, for mechanical testing resources.

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