Recovery of spaceflight-induced bone loss: Bone mineral density after
long-duration missions as fitted with an exponential function
J.D. Sibongaa,⁎, H.J. Evansb, H.G. Sungf, E.R. Spectorb, T.F. Lange, V.S. Oganovc,
A.V. Bakulinc, L.C. Shackelfordd, A.D. LeBlanca
aDivision of Space Life Sciences, Universities Space Research Association, Houston, TX, USA
bWyle Laboratories, Houston, TX, USA
cInstitute for Biomedical Problems, Russian Academy of Science, Moscow, Russia
dHuman Adaptation and Countermeasures Division, NASA Johnson Space Center (JSC), Houston, TX, USA
eDepartment of Radiology, University of California, San Francisco, San Francisco, CA, USA
fGoogle, Inc., Mountain View, CA, USA
Received 19 April 2007; revised 22 June 2007; accepted 8 August 2007
Available online 22 August 2007
The loss of bone mineral in NASA astronauts during spaceflight has been investigated throughout the more than 40 years of space travel.
bone mineraldensity(BMD), withdual-energy X-ray absorptiometry (DXA)beforeand afterflight,ofastronauts who serve onlong-duration missions
(4–6 months). We evaluated this repository of medical data to track whether there is recovery of bone mineral that was lost during spaceflight.
Our analysis was supplemented by BMD data from cosmonauts (by convention, a space traveler formally employed by the Russia Aviation and
Space Agency or by the previous Soviet Union) who had also flown on long-duration missions. Data from a total of 45 individual crew members –
a small number of whom flew on more than one mission – were used in this analysis. Changes in BMD (between 56 different sets of pre- and
postflight measurements) were plotted as a function of time (days after landing). Plotted BMD changes were fitted to an exponential mathematical
function that estimated: (i) BMD change on landing day (day 0) and (ii) the number of days after landing when 50% of the lost bone would be
recovered (“50% recovery time”) in the lumbar spine, trochanter, pelvis, femoral neck and calcaneus. In sum, averaged losses of bone mineral after
long-duration spaceflight ranged between 2% and 9% across all sites with our recovery model predicting a 50% restoration of bone loss for all
sites to be within 9 months.
© 2007 Elsevier Inc. All rights reserved.
Keywords: Cosmonauts; Astronauts; Bone densitometry; Mathematical function; Mechanical unloading
Accelerated bone loss in crew members in space is a well-
recognized effect of weightlessness on the skeletal system and a
critical risk factor for the early onset of osteoporosis after return
to Earth . Studies using calcium kinetics, site-specific bone
densitometry and bone turnover markers document a net loss of
bone mineral in the gravitationally unloaded skeleton of crew
members who had flown either on Skylab (28, 56 and 84 days)
or on long-duration missions (N4 months) aboard the Russian
Mir spacecraft and the International Space Station (ISS) [2–12].
Although calcium kinetics and bone biomarkers have been
used to characterize bone health during spaceflight, no reports
have addressed the impact of spaceflight on long-term bone
health after spaceflight, i.e., the recovery of skeletal integrity,
its nature and its time course. Since the Skylab missions of the
1970s, measurements of bone mineral and bone mineral density
had been used to evaluate the effects of spaceflight on the
skeleton [4,5,8,9]. More recently, QCT scans of long-duration
crew members were used to evaluate changes in mineral density
and in hip structure after spaceflight . The report described
Bone 41 (2007) 973–978
⁎Corresponding author. NASA, Lyndon B. Johnson Space Center, 2101
NASA Parkway, Mail Code: SK/272, Houston, TX 77058, USA. Fax: +1 281
E-mail address: firstname.lastname@example.org (J.D. Sibonga).
8756-3282/$ - see front matter © 2007 Elsevier Inc. All rights reserved.
herein expands upon QCT-measured changes in crew members
(performed immediately and at 1 year after return from ISS
mission) by evaluating the restoration of BMD in long-duration
crew members who were scanned by dual-energy X-ray absorp-
tiometry (DXA) for almost as much as 5 years postflight.
Therefore, we developed a method to analyze this repository
of BMD data to describe the skeletal recovery of astronauts after
their return to Earth. Moreover, through cooperative agreements
with the Russian Space Agency, we obtained access to DXA
data (pre- and postflight BMD) of Russian cosmonauts who
similarly served on long-duration missions to increase the value
of this analysis. Not only did we analyze the BMD data to
determine if the crew members were able to recover their
skeletal deficits upon return to Earth, but we attempted to
understand the rate of skeletal recovery after prolonged space
habitation (typically between 4 and 6 months). This report is the
first to characterize the recovery of spaceflight-induced bone
loss over multiple years on Earth in a crew member population
of this size.
The NASA medical requirements for the health assessment of the Astronaut
Corps include the measurement of BMD to monitor skeletal integrity. Hence, the
astronaut data described herein are a subset of medical data archived by the
Office for the Longitudinal Study of Astronaut Healthat NASA-JSC. This office
operates under the JSC Committee for the Protection of Human Subjects and has
authorized the publication of these medical data.
DXA scans of crew members were conducted on a Hologic DXA
densitometer: models QDR 1000 W, 2000 or 4500 (Hologic, Inc., Waltham,
MA). All postflight scans, and analysis software, for a given subject were
performed on the identical instrument as his/her preflight scans. As documented
in the medical requirement, DXA scans of astronauts were performed as close as
possible to specified time points before and after long-duration flights. Preflight
scans are to be performed within 45 to 30 days before launch while postflight
scans are to be conducted 5 times after return to Earth: 5 days, 6 months,
12 months, 24 months and 36 months after landing. As will be discussed in
detail subsequently, DXA scans of cosmonauts are not scheduled identically to
the NASA medical requirement.
At each scan date, and on a routine monthly basis, a Hologic phantom
standard was scanned to verify proper calibration of the densitometer. Regional
scans of the lumbar spine, hip and the calcaneus were performed as well as a
whole body scan. BMD data for the pelvis were obtained from the whole body
scan [12,13], while scans of the hip yielded data for the trochanter and the
femoral neck of the proximal femur. During the 15-year period from which the
data were obtained, scans of astronauts were performed by a total of four
technicians: a primary and a back-up technician per spacecraft era (e.g., Mir or
ISS). The primary technician performed ∼90% of the total scans. To ensure
consistency in positioning, scanning and analysis, all technicians were trained
with standardized operating procedures. For cosmonaut scans, 78% of the scans
were performed by the co-author (Dr. Bakulin).
The BMD data in this report came from 45 different crew members who
served either on the Mir spacecraft or ISS. Data were obtained from 42 male
crew members and 3 female crew members (average age 43.2±5.2 years). There
was a total of 56 pre- and postflight data sets with seven long-duration crew
members participating in two missions, and two crew members serving on three
missions.BMDdatafromthese56 flights wereinitially analyzedas two separate
data sets because the data were obtained under two different protocols. Data set I
was obtained from seven NASA Mir astronauts (Group I) who flew on the
Russian spacecraft Mir between 1995 and 1998. As part of a research study of
skeletal recovery, these Mir astronauts were scanned at specific time points after
landing (5 days, 6 months, 12 months, 24 months and 36 months after return).
This research protocol of scheduled postflight DXAwas later adopted by NASA
to monitor the return of BMD to preflight status in all ISS astronauts. Data set II
was from BMD measurements conducted on a total of 39 different crew
members (Group II), which is composed of all cosmonauts, serving on Mir and
ISS, and the astronauts serving on ISS only. Table 1 outlines the number of
astronauts and cosmonauts that served on specific space crafts.
There were longitudinal measures conducted in some of the crew members
in each of the two data sets. Therefore, we used a Monte Carlo simulation (R and
Matlab) to confirm consistency in the abilities of the two sets of data to predict
recovery. Once consistency of both models for bone loss and recovery was
confirmed, the two data sets were subsequently combined for the analysis
presented in this report.
Additionally, scans for cosmonaut BMDs were not as numerous as those
performed on astronauts. Typically, a cosmonaut data set consisted of one
preflight session and a single session after flight. There were occasions where a
preflight session for a cosmonautpreparing for a subsequent flight also served as
a postflight time point to assess recovery from the previous flight. Analyzing the
impact of multiple flights on BMD recovery, however, was precluded by limited
Mathematical function for skeletal recovery
The change in bone mineral density that is a direct result of spaceflight was
calculated as the difference between preflight BMD measurement closest to
launch date and the first postflight BMD (i.e., closest to landing date). These
delta BMDs were expressed as a percentage of the preflight BMD. For the
measurements in this report, the first postflight scans were performed generally
within 26 days after landing (6±5 days, mean ±SD, 2–26 days range). There
was one exception of a crew member whose first postflight scan was not
performed until 116 days after landing. Changes in BMD that were derived from
multiple serial postflight scans were treated as independent measurements of
bone loss (negative change) or of bone gain (positive change). That is, a change
from a single preflight BMD was calculated for each postflight scan of the same
crew member and all changes were incorporated into the mathematical function.
Percent BMD changes were plotted as a function of time, i.e., against the
number of days after landing when the postflight BMD was measured. Because
the review of the plotted data suggested an exponential relationship between the
increase in BMD and elapsed time after landing, the data were fitted to a 2-
whereLtisthechangeinBMDdetectedattime “t”afterlanding;L0isthe change
in BMD that is a direct consequence of spaceflight (i.e., at the time of landing)
and HL (half-life) denotes the time at which 50% of the bone lost during
spaceflight has been restored.
This mathematical function estimates the loss of BMD induced by
spaceflight (L0) from a fit of all data points and describes the temporal recovery
of BMD to preflight BMD status. This recovery model – analogous to the decay
of a radioisotope – uses the “half-life” term (HL) as a metric to express the
temporal response of the skeleton. This half-life term – from here on referred to
as “50% recovery time” – was calculated for the five skeletal sites of interest
(lumbar spine, pelvis, femoral neck, trochanter and calcaneus). Spaceflight-
Mission assignments of long-duration crew members
Bone mineral density measurements were conducted in 45 different crew
members serving on a total of 56 long-duration flights during the period of
1990–2004. There were 7 flyers (all males) who flew on at least 2 mission and 2
flyers (males) who flew on 3 missions. Four of the repeat flyers studied in this
database served on both the Mir and ISS missions. Average time period between
launches of multiple flights was 1381±549 days (mean+SD) ranging between
734 and 2347 days.
974J.D. Sibonga et al. / Bone 41 (2007) 973–978
induced bone losses and 50% recovery times were compared between skeletal
sites by evaluating overlaps in error distributions.
Investigations of the influence of age, flight duration and
gender were attempted (Student t-test or Pearson correlation)
but the limited range and variability of data points failed to
show any significant effect. There was no statistically signif-
icant correlation of average % change in BMD (per month) with
age at time of launch (range of Pearson coefficient R between
−0.147 and 0.206) when evaluated for the sites of clinical
interest (pelvis, trochanter, femoral neck and lumbar spine). For
those who flew on “standard” length missions of 4–6 months,
the average flight duration was 173±24 days (range 126–
208 days). However, with the inclusion of the two crew
members that flew on atypical prolonged missions of 311 and
438 days, the average flight duration was 181±47 days. There
were only 9 crew members who flew on multiple flights; 7 of
those crew members flew on only two flights while 2 crew
members flew thrice. For these repeat flyers, the average time
period between the launches of repeat missions was 1381±
549 days (mean±SD). In Figs. 1–5, the data points representing
the second and third flights for the 9 repeat flyers are denoted as
“+” in contrast to BMD changes measured in crew members
after a single long-duration mission.
Figs. 1–5 present the plots of the BMD change, per skeletal
site, as a function of time after landing (days). Ninety-five
percent confidence limits (dashed lines) and the determination
of 50% recovery times are also depicted. Table 2 summarizes
the initial loss and 50% recovery time by skeletal region
obtained from the plots. In brief, the losses of bone density due
to spaceflight appear to be greater in the hip (femoral neck and
trochanter) and pelvis than the losses determined in the lumbar
spine and calcaneus. The confidence intervals for recovery
times for skeletal sites, however, overlapped each other indi-
cating that the rates of recovery were not significantly different
Fig. 1. Changes in BMD at the femoral neck after landing. For each postflight
BMD scan, the percentage change between postflight and preflight BMD was
plotted against the number of days after landing when the scan was performed.
The intercept of the fitted line represents the change in BMD as a direct
consequence of spaceflight (at the time of landing). Dotted lines represent 95%
confidence limits for the BMD data. Data points denoted by plus signs (vs.
diamonds) represent BMD changes measured in a flyers who have served on
multiple long-duration missions. For the femoral neck the spaceflight-induced
loss is 6.5% where 50% recovery time for the loss would occur at 211 days or
about 7 months.
Fig.2. Changesin BMDat the trochanterafter landing.Data points werederived
and plotted as described in Fig. 1. The intercept of the fitted line shows the
spaceflight-induced bone loss of 7.8% where 50% recovery time for the loss
would occur at 255 days or about 8.5 months.
Fig. 3. Changes in BMD at the pelvis after landing. Data points were derived
and plotted as described in Fig. 1. The intercept of the fitted line shows the
spaceflight-induced bone loss of 7.7% where 50% recovery time for the loss
would occur at 97 days or about 3 months.
Fig. 4. Changes in BMD at the lumbar spine after landing. Data points were
derived and plotted as described in Fig. 1. The intercept of the fitted line shows
the spaceflight-induced bone loss of 4.9% where 50% recovery time for the loss
would occur at 151 days or about 5 months.
975 J.D. Sibonga et al. / Bone 41 (2007) 973–978
between sites. Based upon the mathematical fit of postflight
scans, our recovery model estimates that recovery of half of the
bone lost in the trochanter (a clinically relevant site that
consistently displays what appears to be the greatest deficit)
occurs by 9 months.
We applied an exponential mathematical function to a data-
base of BMD measurements to describe the temporal, asymp-
totic recovery of BMD in crew members after return to Earth.
The database contained BMD data from forty-five different
crew members serving over a total of 56 long-duration flights.
There is limited documentation of BMD recovery in spaceflight
crew reported in the literature [5,10]. With imaging of eleven
Mir cosmonauts by peripheral QCT, Vico et al.  detect a
persistence of tibial BMD loss at 6 months after return sug-
gesting that the time period for recovery, if it occurs, would
exceed the duration of spaceflight exposure. Lang et al. 
document the incomplete recovery of femoral neck BMD 1 year
after flight in a QCT evaluation of the hip in 16 ISS crew
members. To supplement these reports of postflight BMD
measurements, this report is the first to use DXA BMD data
monitored over an extended postflight period, in a crew member
population of this size, to describe the recovery pattern of bone
mineral density that was lost during spaceflight.
From this mathematical fit of BMD changes during the
postflight period, we assert that most crew members who have
flown on long-duration missions (4–6 months) would return to
preflight BMD within 3 years—suggesting that the period for
recovery is greater than the duration of the mission. Our
estimate of a longer recovery period is not only supported by
previously mentioned reports on recovery [5,10] but is con-
sistent with animal models of disuse, as exemplified by Ufthoff
and Jaworksi's  report on beagles. The estimation from our
data is based upon BMD changes in the trochanter, which is the
skeletal site that consistently displays the greatest loss in BMD
in spaceflight  and flight-analog studies  and appears
(Table 2) to take the longest time to recover (albeit, not statis-
tically significant). With our mathematical fit indicating a
∼9 month 50% recovery time in the trochanter, we estimate a
substantial restoration (i.e., 15/16ths recovery at 4× the half-
life) to occur within 36 months of return.
It is important, however, to note that skeletal recovery is
highly variable among crew members. As displayed in figures
of postflight BMD changes, some crew members recover within
the first year after return while others do not recover until much
later. Factors that contribute to this variability in recovery are
likely to include nutrition [15,16], skeletal muscle recondition-
ing  and genetics [18,19]; some of these factors may delay
the ability and motivation of crew members to become ambu-
latory and thus mechanically load their skeletons. It is inter-
esting to note that two of the three outliers for BMD loss in the
proximal femur (greater than a 15% deficit in femoral neck and
trochanter) were older than the average age of, or in space
longer than the average duration for, long-duration crew
members; the missions corresponding to these outliers also
represented their first long-duration flight. There was a regional
BMD measurement of the femoral neck that appeared to reflect
deficits in excess of 15%; this hip scan was performed on a
repeat flyer at R+116 days. However, this data point was
beyond the confidence limits of our mathematical fit (Fig. 1)
and the review of subsequent postflight BMD data for this crew
member suggested further that the BMD deficit at 116 days was
A recent presentation by Keyak et al.  relates changes in
DXA areal BMD after flight with reductions in hip strength in
of QCT hip scans. By extrapolation from Keyak's data, we can
suggest that the losses of N15% in the trochanter and femoral
neck, as seen in our database, could lead to an average reduction
in strength of 21.9% with fall loads and 27.1% with axial loads
(with stance). These observed reductions, in a crew member
population with an average age of 43 years, are similar to or
exceed the age-related strength reductions determined with a
cross-sectional comparison to elderly, post-menopausal white
females (strength losses of 24.4% with falls and 6.9% with
stance) . Thus, the reductions in DXA areal BMD translate
Fig. 5. Changes in BMD at the calcaneus after landing. Data points were derived
and plotted as described in Fig. 1. The intercept of the fitted line shows the
spaceflight-induced bone loss of 2.9% where 50% recovery time for the loss
would occur at 163 days or about 5 months.
Summary of fitted data per skeletal site
Skeletal siteLoss (L0) at landing % 50% recovery time (days)
6.8 (5.7, 7.9)
7.8 (6.8, 8.8)
7.7 (6.5, 8.9)
4.9 (3.8, 6.0)
2.9 (2.0, 3.8)
211 (129, 346)
255 (173, 377)
97 (56, 168)
151 (72, 315)
163 (67, 395)
The percentage of preflight BMD loss (L0) at the time of landing and the “50%
recovery time” are listed per skeletal site. Fifty percent recovery time represents
the number of days after landing at which there is a restoration of half of the
bone mineral lost during spaceflight. The L0 and recovery times were
determined from BMD data fitted to a 2-parameter exponential function for
recovery of skeletal BMD after landing: Lt=L0⁎exp[ln(0.5)⁎t/HL]. Confidence
limits (95%) for the fitted values are provided in parentheses. The intercept for
the fitted data (L0) (Figs. 1–5) represents BMD loss as a direct consequence of
976 J.D. Sibonga et al. / Bone 41 (2007) 973–978
to a much greater reduction in the ability of the hip to withstand
applied loads and suggest that crew members are at an increased
risk for hip fracture during the first 3 years after return, and
possibly much longer.
Risk factors that contribute to bone loss in crew members
should also be considered to evaluate their influence on recov-
ery. Collectively, future studies will not only need to evaluate
how bone metabolism responds to changes in mechanical
loading (at the molecular, cellular and tissue level) but how
changes in skeletal mass and structure correlate with changes in
muscle forces, with expression of skeletally relevant genes and
with nutrient uptake in this crew member population.
All models have limitations. However, we chose to develop a
useful recovery model to study the skeleton's re-adaptation to
gravitational forces – after a prolonged exposure to weight-
lessness – by using all available data from every DXA scans
performed after spaceflight during a 15-year period. Only some
of the data in this report was from a research investigation (Data
set I) which was/is always conducted on crew member volun-
teers. Hence, we also included medical data from the NASA
Astronaut Corps in this analysis. Medical evaluations, however,
were restricted to specific times periods before launch and after
landing, and there was insufficient time to allow for replicate
measures. For a human study, we measured a low number of
crew members since there are at most two long-duration mis-
sions flown per year with only 2–3 crew members per mission.
And while DXA scans were a medical requirement for NASA
astronauts, NASA had minimal oversight to BMD measure-
ments of cosmonaut volunteers. Scans for cosmonaut BMDs, as
previously mentioned, were not as numerous as those per-
formed on astronauts. Finally, there are strict regulations on
reporting identifiable medical data. It could be possible to
identify a crew member by his/her data simply by associating
BMD with flight duration, gender, age, ethnicity or nationality.
In light of these constraints, this mathematical fit of postflight
data makes optimal use of all available measurements of BMD
in individuals exposed to spaceflight.
Initially, there was some concern regarding the fact that the
BMD database contained two distinct data sets of BMD. These
data sets represented different numbers of crew members (n=7
vs. 39) and were generated under different protocols. The re-
search data from Group I were more systematically obtained
with longitudinal measurements during a postflight period of a
small number of individuals (n=7); the data from Group II,
but were limited in the number of postflight scans performed per
crew member. Both data sets, moreover, contained serial mea-
data sets, we were able to establish consistency between the two
recovery models of fitted data by a Monte Carlo simulation; this
enabled us to fit all available changes in BMD into our mathe-
matical function thereby optimizing its utility to predict of
Another limitation of the recovery model lay in its inability
to evaluate the influence of previous flights on skeletal recov-
ery. In Data set II there were 49 sets of preflight and postfight
scans available from the 39 crew members (Group II) because
of nine crew members who flew on multiple missions. As
previously mentioned, two of those same nine crew members
flew on three missions each and one astronaut in Group II had
previously flown on a Mir mission (Group I). There was an
average elapsed period of 1381±549 days (774–2347 days)
between repeat flights. Because of the small number of repeat
flyers in our database, as well as the limited variation in flight
durations, it was not possible to account for the impact of both
multiple missions or of mission duration on a crew member's
spaceflight-induced bone loss or on BMD recovery.
A regression analysis has been conducted by our Russian co-
author who analyzed BMD of L1–L4 from fourteen cosmo-
nauts who have served on multiple missions of 5.5–11 months
duration. In a previously conducted analysis by our co-author,
Oganov reports the results of multiple regression analysis of
variables from an earlier flight to predict BMD changes in a
subsequent flight. In brief, there is a significant correlation
(R=0.627) of bone loss in the first flight, combined with the
bone restoration before the second flight, with BMD change in
the second flight; there was only a slight improvement when
baseline bone mineral density for the first flight was added as a
third independent variable (R=0.632) . Further study is
warranted; investigations that address bone phenotypes that
may serve as predictive indices for bone loss during and recov-
ery after spaceflight are currently in progress by our Russian
Finally, DXA measurement of BMD alone is no longer
considered a sufficient surrogate for bone strength . With
the results of this study, we do not assert that the restoration of
bone mass in crew members implies a restoration of bone
strength particularly since DXA measurement of areal BMD
fails to take into account bone geometry or material properties
which all together or combination could influence fracture
In summary, a two-parameter exponential function was
applied to serial BMD measurements of 45 crew members who
served on a total of 56 long-duration spaceflight missions
(N4 months). The recovery model, based upon a fit of data
points (approximately 62–119) over 5 regional sites, provided a
numerical estimate for the length of time to restore 50% of bone
lost during spaceflight. The results indicate that deficits in BMD
are gradually restored after return to Earth, and the recovery
model estimates that restoration of BMD would be expected to
occur within 3 years after return for most crew members. This
investigation addresses a fundamental issue of how bone mass
responds to changes in skeletal loading. These results would
have an additional relevance to patient populations that are
subjected to prolonged periods of immobilization and to the
skeleton's capacity to recover.
The authors would like to express their appreciation to Dr.
Victor Schneider (NASA Headquarters) without whose efforts
Funding: T.Lang, Contract NAS-9-99055 Grant NNJ04HC7SA
from NASA Johnson Space Center.
977 J.D. Sibonga et al. / Bone 41 (2007) 973–978
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