Research Article: The impact of bipedal mechanical loading history on longitudinal long bone growth

Date Published: February 7, 2019

Publisher: Public Library of Science

Author(s): Adam D. Foster, Costin Daniel Untaroiu.

http://doi.org/10.1371/journal.pone.0211692

Abstract

Longitudinal bone growth is accomplished through a process where proliferating chondrocytes produce cartilage in the growth plate, which ultimately ossifies. Environmental influences, like mechanical loading, can moderate the growth of this cartilage, which can alter bone length. However, little is known about how specific behaviors like bipedalism, which is characterized by a shift in body mass (mechanical load), to the lower limbs, may impact bone growth. This study uses an experimental approach to induce bipedal behaviors in a rodent model (Rattus norvegicus) over a 12-week period using a treadmill-mounted harness system to test how rat hindlimbs respond to the following loading conditions: 1) fully loaded bipedal walking, 2) partially loaded bipedal walking, 3) standing, 4) quadrupedal walking, and 5) no exercise control. These experimental conditions test whether mechanical loading from 1) locomotor or postural behaviors, and 2) a change in the magnitude of load can moderate longitudinal bone growth in the femur and tibia, relative to controls. The results demonstrate that fully loaded bipedal walking and bipedal standing groups showed significant differences in the percentage change in length for the tibia and femur. When comparing the change from baseline, which control for body mass, all bipedal groups showed significant differences in tibia length compared to control groups. However, there were no absolute differences in bone length, which suggests that mechanical loads from bipedal behaviors may instead be moderating changes in growth velocity. Implications for the relationship between bipedal behaviors and longitudinal bone growth are discussed.

Partial Text

Longitudinal bone growth results from a process where proliferating chondrocytes produce hypertrophic chondrocytes that are aligned with the long axis of the bone. Growth velocity (length/time) is primarily driven by the rate of production of hypertrophic chondrocytes. Proliferative processes that occur between primary and secondary ossification centers (also referred to as the growth plate) form the epiphyses of bones and are responsible for long bone growth throughout adolescence [1]. Cartilaginous regions that make up the diaphysis and epiphysis of the bone ossify over time at a rate that is closely linked with phylogeny [2]. However, there are a number of intrinsic and environmental factors that can modify longitudinal bone growth that are important for explaining intraspecific variation in bone length.

Female Sprague-Dawley rats (Rattus norvegicus; Harlan, Indianapolis, IN, USA) were acquired at three weeks of age (the youngest age available from the vendor) and were allowed one week of acclimation. Rats were housed in a temperature and humidity controlled room using a 12-hour day-night light cycle. All rats were allowed ad libitum access to food and water and were group housed in cages (3 rats per cage) containing wood shaving bedding and a PVC tube. Cages were standard laboratory polycarbonate rat pans (19” x 10-1/2” x 8”) and were not equipped with an exercise wheel or any other method of enrichment. Exercise procedures, which occurred outside of the cage environment, were conducted during the light cycle.

There were significant differences among the experimental groups for the amount of hindlimb loading, calculated as the mean percentage of body mass experienced by the hindlimbs for each rat for each 60 minute experimental period, over the 12-week experiment (F[41,2] = 110.1, p<0.001). A follow-up Fisher’s LSD post-hoc test found significant differences in pairwise comparisons between all three groups (p<0.001; Fig 2). The mean loading amount experienced by the fully loaded bipedal group was 90.2% (±7.2% [SD]) of body mass, the partially loaded group experienced 54.5% (± 8.9% [SD]) of body mass, and the standing group experienced 78.5% (± 8.2% [SD]) of body mass. There were no measured hindlimb loads for the quadrupedal control group because loading was measured via a hanging scale, which measures the amount of body mass offset by a vertical force on the torso (see Methods). The purpose of this study was to explore how bipedal locomotor and postural mechanical loads may moderate longitudinal bone growth in an animal model. This study used five different experimental groups to test the independent effects of a postural and locomotor shift to bipedal behaviors and the dose-dependent effects of force magnitude. While the study design cannot characterize the mechanical forces applied to bones (i.e., tension, compression, shear, etc.), it does offer insight into how bone growth is impacted by the average loading amounts experienced by the hindlimbs. The mechanical loading applied to animal hindlimbs was consistent (as measured by average values across all experimental days) and occurred during crucial growth periods of the tibia in the rat [32]. Ultimately, there were no absolute differences in length for the femur and tibia. However, there were significant differences in the percentage change in length for the fully loaded bipedal walking and bipedal standing groups when compared to both control groups, which appears to start a process of leveling off from weeks 9 to 12. This result is consistent with previous work which suggests that longitudinal bone growth in rat tibiae undergo rapid, logarithmic growth through 64 days of age. After this point, growth begins to slow with no detected growth after 20 weeks [32]. At weeks 9 to 12 of the experiment, the rats in this study are approximately 84 to 105 days of age (rats were 4 weeks of age [28 days] at the start of the experiment), which is consistent with growth rates in Horton et al. [32]. Because there were no differences in absolute values, but significant differences seen in measures of relative change, these bipedal mechanical loads may be altering growth velocity. However, the final bone length is still strongly influenced by genetics.   Source: http://doi.org/10.1371/journal.pone.0211692

 

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