One-month spaceflight compromises the bone microstructure, tissue-level mechanical properties, osteocyte survival and lacunae volume in mature mice skeletons

Maude Gerbaix,Guillaume Courbon,Guillemette Gauquelin-Koch,Delphine Farlay,Norbert Laroche,Patrick Ammann,Hélène Follet,Vasily Gnyubkin,Françoise Peyrin,Boris Shenkman,Laurence Vico,Cécile Olivier,Rachel Genthial

doi:10.1038/s41598-017-03014-2

Abstract

The weightless environment during spaceflight induces site-specific bone loss. The 30-day Bion-M1 mission offered a unique opportunity to characterize the skeletal changes after spaceflight and an 8-day recovery period in mature male C57/BL6 mice. In the femur metaphysis, spaceflight decreased the trabecular bone volume (−64% vs. Habitat Control), dramatically increased the bone resorption (+140% vs. Habitat Control) and induced marrow adiposity invasion. At the diaphysis, cortical thinning associated with periosteal resorption was observed. In the Flight animal group, the osteocyte lacunae displayed a reduced volume and a more spherical shape (synchrotron radiation analyses), and empty lacunae were highly increased (+344% vs. Habitat Control). Tissue-level mechanical cortical properties (i.e., hardness and modulus) were locally decreased by spaceflight, whereas the mineral characteristics and collagen maturity were unaffected. In the vertebrae, spaceflight decreased the overall bone volume and altered the modulus in the periphery of the trabecular struts. Despite normalized osteoclastic activity and an increased osteoblast number, bone recovery was not observed 8 days after landing. In conclusion, spaceflight induces osteocyte death, which may trigger bone resorption and result in bone mass and microstructural deterioration. Moreover, osteocyte cell death, lacunae mineralization and fatty marrow, which are hallmarks of ageing, may impede tissue maintenance and repair.

Highlights

Spaceflight sojourns induce a series of physiological adaptations in the human body that predispose astronauts to an increased risk of bone fracture after returning to Earth
Two groups were exposed to a one-month spaceflight: (i) a Flight group, which included mice killed within the day after landing; and (ii) a Flight + Rec recovery group, which included mice that were allowed to recover over 8 days
Two ground control groups were included: a Habitat Control group, which was kept under spacecraft housing conditions; and a Control group, which was kept under standard housing conditions

Summary

Introduction

Previous in-flight animal research conducted on young growing rats during relatively short-term missions (from 4 to 19 days) has considerably advanced our understanding of skeletal adaptations to spaceflight, including the mechanisms of bone loss and skeletal development in microgravity[6]. These experiments showed either deterioration in trabecular and cortical bone parameters[7,8,9,10,11] or no changes[12,13,14,15,16] depending on the animal’s age, strain levels, habitat, flight duration and the delay between landing and sample collection. Bone recovery after spaceflight is a concern because studies on spacemen[3,27] and young rats[2,28] have suggested that bone mass recovery after reambulation takes longer than the mission duration

Methods

Results

Conclusion