Long-term changes in the density and structure of the human hip and spine after long-duration spaceflight

doi:10.1016/j.actaastro.2010.01.022

Acta Astronautica

Volume 67, Issues 1–2, July–August 2010, Pages 71-81

https://doi.org/10.1016/j.actaastro.2010.01.022 Get rights and content

Abstract

To determine the long-term effects of long-duration spaceflight, we measured bone mineral density and bone geometry of International Space Station (ISS) crewmembers using quantitative computed tomography (QCT) before launch, immediately upon their return, one year after return, and 2–4.5 years after return from the ISS. Eight crew members (7 male, 1 female, mean age 45±4 years at start of mission) who spent an average of 181 days (range 161–196 days) aboard the ISS took part in the study. Integral bone mineral density (iBMD), trabecular BMD (tBMD), bone mineral content (BMC), and vertebral cross-sectional area (CSA) were measured in the lumbar spine, and iBMD, tBMD, cortical BMD (cBMD), BMC, CSA, volume, and femoral neck section modulus were measured in the hip. Spine iBMD was 95% of the average preflight value upon return from the ISS and reached its preflight value over the next 2–4.5 years. Spine tBMD was 97% of the average preflight value upon return from the ISS and tended to decrease throughout the course of the study. Vertebral CSA remained essentially unchanged throughout the study. Hip iBMD was 91% of the preflight value upon return from the ISS and was 95% of the preflight value after 2–4.5 years of recovery. Hip tBMD was 88% of the preflight value upon return and recovered to only 93% of the preflight value after 1 year. At the 2- to 4.5-year time point, average tBMD was 88% of the preflight value. During the recovery period the total volume and cortical bone volume in the hip reached values of 114% and 110% of their preflight values, respectively. The combination of age-related bone loss, long-duration spaceflight, and re-adaptation to the 1-g terrestrial environment presumably produced these changes. These long-term data suggest that skeletal changes that occur during long-duration spaceflight persist even after multiple years of recovery. These changes have important implications for the skeletal health of crew members, especially those who make repeat trips to space.

Introduction

Bone loss has long been recognized as an important physiological problem with human spaceflight. Calcium loss from both bone and soft tissue has been observed even after relatively short missions, such as the 12.6-day Apollo 17 lunar mission [1]. This problem is more pronounced with long-duration space missions, because continued loss of bone mineral over weeks and months can lead to significant decreases in bone mineral density (BMD) of the load-bearing hip, spine, and distal tibia. Abnormally high rates of calcium loss were shown to continue during Skylab missions lasting 28–84 days [2], [3], [4], and missions to the Russian MIR orbital station lasting 4 to 6 months were shown to result in monthly BMD losses of 0.9% and 1.5% at the spine and hip, respectively [5]. These losses were confirmed by studies on the International Space Station (ISS) [6].

The time course of recovery of lost bone mineral has important implications for long-term crew health and for the success of future lunar and Mars missions. A recent report applied a mathematical model to dual-energy X-ray absorptiometry (DXA) measurements of areal BMD (aBMD) in the spine, hip and heel as performed before and after the typical missions (4–6 months) on the ISS or the Russian MIR orbital station [7]. The fitted data estimated the elapsed time, after return to earth, when substantial recovery of aBMD would be observed for those skeletal sites. Models fit to these data predicted that aBMD would return to preflight levels within 3 years. Measurements made with peripheral quantitative computed tomography (pQCT) after a 6-month MIR mission suggested that bone loss at the distal tibia persisted even after 6 months of recovery [8]. Another study, in which whole-body QCT was used to measure the density and geometry of the proximal femur, showed that the overall bone mineral content (BMC) was nearly recovered 1 year after crewmembers returned from 4- to 6-month missions aboard the ISS [9]. The recovery of BMC appeared to primarily take place through increases in bone size during the first year after the mission, as evidenced by increases in femur volume and cross-sectional area. This response could be explained by functional adaptation to increased bone strains after returning to the 1-g environment. Strains due to bending and torsion are highest at the periosteal surface, and the formation of new bone may have occurred in response to abnormally elevated strains in these locations after spaceflight-induced bone loss caused a decrease in bone stiffness [10].

To determine the long-term effects of long-duration spaceflight, we made measurements of compartmental bone mineral density and bone geometry of ISS crewmembers using QCT and DXA before launch, immediately upon their return, one year after return, and at anywhere between 2 and 4.5 years after return from 5- to 6-month missions. The purpose of this paper is to present these measurements and to interpret their implications for the long-term musculoskeletal health of ISS crew and crewmembers and the crews of future long-duration lunar and Mars missions. Data from 8 crewmembers are reported. These data represent the first volumetric measurements of human bone mineral status and bone geometry more than 1 year after return from long-duration spaceflight.

Section snippets

Materials and methods

Eight ISS crewmembers (7 male, 1 female, mean age 45±4 years at start of mission) took part in the study to evaluate, by QCT and DXA, the changes in compartment-specific volumetric bone mineral densities and the spatial distribution of mass (e.g., geometry). These eight subjects were a subset of the larger cohort analyzed previously [6]. Informed consent was obtained from all subjects under the direction of the Institutional Review Boards at the collaborating institutions (NASA Johnson Space

Results

Table 1 provides the absolute values for all preflight measurements, and Table 2 provides measurements at each time point reported as a percent of the preflight values. Data points for each measurement and each individual are provided in Fig. 2, Fig. 3, Fig. 4, Fig. 5. Marker symbols for each individual subject are consistent for all plots.

Spine iBMD decreased in all 8 subjects during their missions (Table 2, Fig. 2). Between the return time point and the 1-year time point, spine iBMD increased

Discussion

The results of this study show that changes in bone density and structure persist even long after 5 to 6 months of living in microgravity. Measurements made with both QCT and DXA suggest that the lumbar spine fully recovers its iBMD by 2 to 4.5 years after returning to a 1-g environment. However, the tBMD of the spine remained lower than the preflight value even at the extension time point, suggesting that the recovery of BMD by the whole vertebra was not achieved through recovery of losses in

Conclusions

Missions to the ISS lasting 5- to 6- months resulted in a decrease of iBMD in the lumbar spine and proximal femur of all subjects in the study. Decreases in bone density were highest in the trabecular bone compartment. The overall bone density of the lumbar spine returned to preflight levels 2–4.5 years after the crewmembers returned to Earth, but the trabecular bone compartment demonstrated a persistent deficit in bone density in most subjects. Trabecular bone density in the femur began to

Acknowledgement

This study was funded by NASA Grant NNJ04HC7SA. The authors thank Gwenn Sandoz for assistance with this study.

Dana Carpenter, Ph.D., is an Associate Specialist in the Department of Radiology and Biomedical Imaging at the University of California, San Francisco. Dr. Carpenter obtained his B.S. in Mechanical Engineering from the Georgia Institute of Technology in 1999, his M.S. in Mechanical Engineering from Stanford University in 2002, and his Ph.D. in Mechanical Engineering from Stanford University in 2006. After working as a postdoctoral scholar for two years in the UCSF Radiology Department, Dr.

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Harlan Evans is a Principal Research Scientist at Wyle and an Assistant Professor at Baylor College of Medicine. He received a B.S. in Physics from the University of Oklahoma in 1963 and a Ph.D. in Physics from the University of Chicago in 1973. His principal research interests have been measuring bone and muscle changes caused by space flight or disuse using DXA, CT, and MRI.

Jean Sibonga is Senior Scientist at University Space Research Association (USRA) and currently serves as the Lead for the Bone Discipline in the Human Research Program at NASA Johnson Space Center. Dr. Sibonga received her B.S. in Chemistry and English (1980) from University of Puget Sound (Tacoma, Washington) and her Ph.D. in Biochemistry from Loma Linda University (1988). She has over twenty-five years of research experience in the field of mineral metabolism in such institutions as the Jerry L. Pettis VAMC (Loma Linda, CA), NASA Ames Research Center, Harvard School of Dental Medicine and the Mayo Clinic Rochester.

Thomas Lang, Ph.D., is a Professor in Residence in the University of California, San Francisco Department of Radiology and Biomedical Imaging and the UCSF/UC Berkeley Joint Bioengineering Graduate Group. He received his B.A. in Chemistry from the University of Chicago in 1983 and a Ph.D. in Chemistry from UC Berkeley in 1990. Prior to joining the UCSF faculty in 1994, he completed a postdoctoral fellowship in the UCSF Radiology Department and worked as a Nuclear Medicine Physicist at ADAC Laboratories. Dr Lang's core interest is the use of clinically available imaging modalities in the study of human musculoskeletal biology.

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Long-term changes in the density and structure of the human hip and spine after long-duration spaceflight

Abstract

Introduction

Section snippets

Materials and methods

Results

Discussion

Conclusions

Acknowledgement

Acta Astronaut.

Bone

Lancet

Bone

Bone

Bone

Calcium and phosphorus change of the Apollo 17 crew members

Nutr. Metab.

Mineral and nitrogen metabolic studies on Skylab flights and comparison with effects of earth long-term recumbency

Life Sci. Space Res.

Effect of weightlessness on mineral metabolism; metabolic studies on Skylab orbital space flights

Calcif. Tissue Res.