Incomplete recovery of bone strength and trabecular microarchitecture at the distal tibia 1 year after return from long duration spaceflight

Abstract

Determining the extent of bone recovery after prolonged spaceflight is important for understanding risks to astronaut long-term skeletal health. We examined bone strength, density, and microarchitecture in seventeen astronauts (14 males; mean 47 years) using high-resolution peripheral quantitative computed tomography (HR-pQCT; 61 μm). We imaged the tibia and radius before spaceflight, at return to Earth, and after 6- and 12-months recovery and assessed biomarkers of bone turnover and exercise. Twelve months after flight, group median tibia bone strength (F.Load), total, cortical, and trabecular bone mineral density (BMD), trabecular bone volume fraction and thickness remained - 0.9% to - 2.1% reduced compared with pre-flight (p ≤ 0.001). Astronauts on longer missions (> 6-months) had poorer bone recovery. For example, F.Load recovered by 12-months post-flight in astronauts on shorter (< 6-months; - 0.4% median deficit) but not longer (- 3.9%) missions. Similar disparities were noted for total, trabecular, and cortical BMD. Altogether, nine of 17 astronauts did not fully recover tibia total BMD after 12-months. Astronauts with incomplete recovery had higher biomarkers of bone turnover compared with astronauts whose bone recovered. Study findings suggest incomplete recovery of bone strength, density, and trabecular microarchitecture at the weight-bearing tibia, commensurate with a decade or more of terrestrial age-related bone loss.

Figure 1

Tibia bone strength, density, and trabecular microarchitecture. Values are percent change from pre-flight at return (R + 0), 6-months (R + 6), and 12-months (R + 12) recovery. Dashed lines for astronauts on > 6-month missions (n = 8) and solid lines for astronauts on < 6-month missions (n = 9). Black circles connected by thick solid line indicate median group change. Shaded bars indicate least significant change. F.Load failure load, Tt.BMD total bone mineral density, Ct.BMD cortical bone mineral density, Tb.BMD trabecular bone mineral density, Tb.Th trabecular thickness, Tb.Sp trabecular separation, Conn.D connectivity density, SMI structure model index. One astronaut on a > 6-month mission did not complete the R + 12 measure (dashed, blue line). *p < 0.05 from pre-flight. Tb.Th p = 0.06 at R + 6.

Figure 2

Tibia bone strength, density, and trabecular microarchitecture by mission duration. Values are percent change from pre-flight at return (R + 0), 6-months (R + 6), and 12-months (R + 12) recovery. Dashed lines for astronauts on > 6-month missions (n = 8) and solid lines for astronauts on < 6-month missions (n = 9). Black circles connected by thick dashed line indicate median change for astronauts on > 6-month missions and black squares connected by thick solid line indicate median change for astronauts on < 6-month missions. Shaded bars indicate least significant change. F.Load failure load, Tt.BMD total bone mineral density, Ct.BMD cortical bone mineral density, Tb.BMD trabecular bone mineral density, Tb.Th trabecular thickness, Tb.Sp trabecular separation, Conn.D connectivity density, SMI structure model index. One astronaut on a > 6-month mission did not complete the R + 12 measure (dashed, blue line). *p < 0.05 from pre-flight for astronauts on > 6-month missions; ^#p < 0.05 from pre-flight for astronauts on < 6-month missions.

Figure 3

Total hip (TH), femoral neck (FN), and lumbar spine (LS) aBMD, total body mass, total body fat mass, and total body lean mass less bone mineral content. Values are percent change from pre-flight at return (R + 0), 6-months (R + 6), and 12-months (R + 12) recovery. Dashed lines for astronauts on > 6-month missions (n = 8) and solid lines for astronauts on < 6-month missions (n = 9). Black circles connected by thick solid line indicates median group change. Shaded error bars indicate least significant change. *p < 0.05 from pre-flight.

Figure 4

Biomarkers of bone turnover relative to bone recovery at pre-flight (Pre), flight days 15, 30, 60, 120, 180, and return (R + 0), 1-month (R + 1), 6-months (R + 6), and 12-months (R + 12) recovery. Median group change for astronauts who recovered (n = 8) total BMD at R + 12 are indicated by black circles connected by a thick solid line, while median group change in astronauts who did not recover (n = 9) total BMD at R + 12 are indicated by open circles connected by a thick dashed line. Colored dashed lines for astronauts on > 6-month mission and solid lines for astronauts on < 6-month mission. CTx type I collagen C-terminal cross-linked telopeptide, NTx type I collagen N-terminal cross-linked telopeptide, Sclerostin, P1NP procollagen type 1 amino-terminal propeptide, BSAP bone-specific alkaline phosphatase, Osteocalcin. Note: three astronauts on > 6-month missions did not complete CTx measures or in-flight NTX measures, and missed in-flight day 15, 60, and 120 measures for sclerostin, P1NP, BSAP, and osteocalcin. Thus, for NTx, these astronauts are indicated by an ‘x’ at pre-flight and trajectory between R + 0 and R + 12. *p < 0.05 from pre-flight for entire group. CTx, NTx, sclerostin, and osteocalcin were significantly different (p < 0.05) at all time points between astronauts who recovered tibia total BMD and astronauts whose tibia total BMD did not recover.

Figure 5

Exercise volume relative to bone recovery pre-flight, in-flight, 6-months (R + 6) and 12-months (R + 12) recovery. Median group change for astronauts who recovered (n = 8) total BMD at R + 12 are indicated by black circles connected by a thick line, while median group change in crewmembers who did not recover (n = 9) total BMD at R + 12 are indicated by open circles connected by a thick dashed line. Colored dashed lines for astronauts on > 6-month mission and solid lines for astronauts on < 6-month mission. *p < 0.05 from in-flight for entire group. ^#p < 0.05 between astronauts whose tibia total BMD recovered and astronauts whose tibia total BMD did not recover.