Abstract
Spaceflight induces bone alterations with site-specific rates of bone loss according to the weight-bearing function of the bone. For the first time, this study aimed to characterize bone microarchitecture and density alterations of three ankle bones (calcaneus, navicular, and talus) of mice after spaceflight and to evaluate the impact of 8 days of Earth reambulation. Ten C57BL/6N male 4-month-old mice flew on the Bion-M1 biosatellite for 1 month; half were euthanized within 24-h of return and half after 8-days recovery on Earth. Bone microarchitecture and quality was assessed by microtomography (μCT). Whole calcaneus bone volume fraction decreased in Flight group (−6.4%, p < 0.05), and worsened in the Recovery group (−11.08%, p < 0.01), when compared to Control group. Navicular and talus trabecular bone volume fraction showed trends toward decrease in Flight and differences reached statistical significance in Recovery group (−8.16%; −8.87%, respectively; p < 0.05) when compared to Control group. At calcaneus, cortical thickness decreased in Recovery vs. Control groups (−11.69%; p < 0.01). Bone surface area, reflecting periosteal bone erosion, significantly increased in all bone sites analyzed. Qualitative analyses of 3-D bone reconstruction revealed local sites of cortical thinning and bone erosion, predominantly at articulations, muscle insertions, and ground contact bone sites. Overall, spaceflight-induced bone loss in ankle bones was site and compartment specific whilst the tissue mineral density of the remaining bone was preserved. Eight days after landing, bone status worsened as compared to immediate return.
Highlights
Our study aims to investigate the structural and density changes of the total and cortical bone, in the ankle bones of mature mice by analyzing the calcaneus, navicular, and talus after 1-month spaceflight and an 8-day recovery period post-flight
The lowest intraindividual Coefficients of variation (CV) existed for TMD of all bones; whereas, bone surface area (BS) and bone surface area normalized to bone volume (BS/BV) presented with the highest intra-individual variability for the navicular (CV = 0.5%) and the calcaneus (CV = 2%)
Thirty days of microgravity aboard the Bion-M1 mission followed by 8-day recovery induces adaptive site-specific changes in the weight bearing ankle
Summary
Across the body of research for human and rodents, it is well documented that weight-bearing bones are subjected to most adverse effects of spaceflights for both mature skeletons (Vico et al, 2000; Gerbaix et al, 2017) and growing skeletons causing retardation of matrix maturation (Morey and Baylink, 1978; Zernicke et al, 1990; Doty et al, 1992; Cavolina et al, 1997; Evans et al, 1998).Spaceflight Effects on Ankle Bonesmany non-weight bearing sites remain affected (Harrison et al, 2003; Kohler et al, 2005) to a lesser extent. Weight-bearing sites that are most commonly studied, following microgravity exposure, include the tibia (Jee et al, 1983; Collet et al, 1997; Wronski et al, 1998; Vico et al, 2000), femur (Harrison et al, 2003; Keune et al, 2015; Gerbaix et al, 2017), and the femoral neck and greater trochanter region forming the hip (Lang et al, 2004; Blaber et al, 2013). Wang et al (2015) demonstrated that in humans the navicular, in relation to its size, experiences the largest transfer of force in the foot (0.33 × body weight) From this and admitting that human and mouse ankles are comparable (Chang et al, 2016), it could be hypothesized that when unloaded the navicular may endure greatest deterioration. The observed slow bone recovery may be modulated in the ankle region, due to large involvement in the gait cycle of both mice (Mendes et al, 2015) and humans (Loudon et al, 2008)
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