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Physiology of a Microgravity Environment Selected Contribution: Effects of spaceflight during pregnancy on labor and birth at 1 G

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Abstract

The events of parturition (labor, delivery, maternal care, placentophagia, and onset of nursing) were analyzed in female Norway rats (Rattus norvegicus) flown on either 11- or 9-day-long spaceflights beginning at the approximate midpoint of their pregnancies. Each space shuttle flight landed on the 20th day of the rats' pregnancies, just 48-72 h before parturition. After spaceflight, dams were continuously monitored and recorded by time-lapse videography throughout the completion of parturition and onset of nursing (days 22 and 23). Analyses of parturition revealed that, compared with ground controls, flight dams displayed twice the number of lordosis contractions, the predominant labor contraction type in rats. The number of vertical contractions (those that immediately precede expulsion of a pup from the womb), the duration of labor, fetal wastage, number of neonates born, neonatal birth weights, placentophagia, and maternal care during parturition, including the onset of nursing, were comparable in flight and ground control dams. Our findings indicate that, with the exception of labor contractions, mammalian pregnancy and parturition remain qualitatively and quantitatively intact after spaceflight during pregnancy.
highlighted topics
Physiology of a Microgravity Environment
Selected Contribution: Effects of spaceflight
during pregnancy on labor and birth at 1 G
APRIL E. RONCA
1
AND JEFFREY R. ALBERTS
2
1
Life Sciences Division, National Aeronautics and Space Administration Ames Research Center,
Moffett Field, California 94035; and
2
Department of Psychology,
Indiana University, Bloomington, Indiana 47405
Received 3 May 2000; accepted in final form 30 May 2000
Ronca, April E., and Jeffrey R. Alberts. Selected Con-
tribution: Effects of spaceflight during pregnancy on labor
and birth at 1 G. J Appl Physiol 89: 849–854, 2000.—The
events of parturition (labor, delivery, maternal care, placen-
tophagia, and onset of nursing) were analyzed in female
Norway rats (Rattus norvegicus) flown on either 11- or 9-day-
long spaceflights beginning at the approximate midpoint of
their pregnancies. Each space shuttle flight landed on the
20th day of the rats’ pregnancies, just 48–72 h before partu-
rition. After spaceflight, dams were continuously monitored
and recorded by time-lapse videography throughout the com-
pletion of parturition and onset of nursing (days 22 and 23).
Analyses of parturition revealed that, compared with ground
controls, flight dams displayed twice the number of lordosis
contractions, the predominant labor contraction type in rats.
The number of vertical contractions (those that immediately
precede expulsion of a pup from the womb), the duration of
labor, fetal wastage, number of neonates born, neonatal birth
weights, placentophagia, and maternal care during parturi-
tion, including the onset of nursing, were comparable in
flight and ground control dams. Our findings indicate that,
with the exception of labor contractions, mammalian preg-
nancy and parturition remain qualitatively and quantita-
tively intact after spaceflight during pregnancy.
parturition; microgravity; uterus; abdominal muscle; fetus;
newborn; rat
THE VARIOUS PROCESSES COMPRISING mammalian preg-
nancy and parturition evolved within the omnipresent
context of the normal gravitational forces on Earth,
thus raising the question of whether pregnancy and
birth can be successfully sustained in the absence of
gravity. In the only previous spaceflight in which preg-
nant mammals were exposed to microgravity, rats in
late stages of pregnancy were flown on the 4.5-day
Cosmos-1514 mission in 1983 (9). After this brief flight,
four of five dams gave birth to viable litters. Parturi-
tion was not observed systematically in the Cosmos
study. Also, it is not known how longer flights might
affect physiological or behavioral responses of preg-
nant and parturient females and the process of birth.
The most common effects of spaceflight, namely, head-
ward fluid shifts, alterations in bone and calcium me-
tabolism, and muscular deconditioning (5, 8, 10), may
provide formidable obstacles to sustaining the gravid
state in space and impede the ability of mothers to give
birth.
Of particular concern are the potential effects of
spaceflight muscle deconditioning on the musculature
of pregnant dams in the days preceding parturition.
For example, expulsion of the conceptus may be com-
promised because of deconditioning of the transverse
abdominus, an antigravity muscle in tetrapods (6).
Much is known about parturition in the Norway rat
(Rattus norvegicus) (4, 14, 15). At the time of birth, the
female rat’s behavior is centered on the processes of
delivery and the products of birth, namely, the fetuses,
placentas, and birth fluids (8). The entire process be-
gins just a few hours before birth with the transition
from infrequent, low-amplitude uterine contractions to
regular, more intense contractions. This shift signals
the onset of labor (4, 15). Direct measurements of
intrauterine pressure in rats suggest that, near partu-
rition, the rat fetus is exposed to contractions ap-
proaching 20 mmHg (7). We previously described and
quantified labor and delivery in the rat using 24-h
time-lapse videography (15). Several behaviorally dis-
tinct types of uterine contractions can be observed
Address for reprint requests and other correspondence: A. E.
Ronca, Life Sciences Division, Bldg. 261, Rm 111, NASA Ames
Research Center, Moffett Field, California 94035 (E-mail:
aronca@mail.arc.nasa.gov).
The costs of publication of this article were defrayed in part by the
payment of page charges. The article must therefore be hereby
marked ‘‘advertisement’’ in accordance with 18 U.S.C. Section 1734
solely to indicate this fact.
J Appl Physiol
89: 849–854, 2000.
http://www.jap.org 849
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during labor. During a lordosis contraction, the dam
lies on her ventrum and elongates her body, often
arching her back and elevating her outstretched hind-
limbs off the ground. More than 70 lordosis contrac-
tions may be observed during a typical birth, at inter-
vals less than 35 s apart during the last hour of labor.
Lordosis contractions predominate before the birth of
the first pup and are believed to transport the concep-
tus into the lower birth canal. Vertical contractions,
observed just before the birth of a pup, consist of a
series of rapid, bilateral abdominal lifts. Rat dams
typically deliver from 8 to 12 pups over a period of
40–140 min. Elements of maternal behavior, such as
licking and retrieving, emerge when the first pup is
expelled from the womb. At birth, the mother licks the
neonate, removing its birth membranes, thereby help-
ing to initiate postnatal breathing (13). The onset of
nursing occurs soon after the last pup is born.
In the present experiment, we tested hypotheses
that mammalian pregnancy and parturition can sur-
vive exposure to sustained periods of spaceflight. On
the basis of the brief Cosmos-1514 mission, we pre-
dicted that pregnant rats flown on longer (11 and 9
day) missions would also complete their 22-day preg-
nancies and undergo vaginal deliveries but that partu-
rition would not be successful for all rat dams. The
longer period of spaceflight exposure relative to the
Cosmos mission was predicted to increase fetal losses
and reduce the number of live births. We predicted
specific effects on labor contractions at the time of
parturition, mediated via spaceflight-induced changes
in uterine contractile proteins (3) and abdominal mus-
culature (6). We also hypothesized that labor contrac-
tions would be less effective after spaceflight exposure,
possibly lengthening the birth process. We also pre-
dicted postflight behavioral changes such as reduced
appetite and lethargy and thus quantified the dams’
postflight feeding, drinking, and locomotion. Charac-
teristic maternal responses to the young during partu-
rition were analyzed to test the hypothesis that pat-
terns of maternal care would be disrupted after
spaceflight.
The data presented are derived from two spaceflight
missions jointly sponsored by National Aeronautics
and Space Administration (NASA) and National Insti-
tutes of Health (NIH) and are called the Rodent 1
(NIH.R1) and Rodent 2 (NIH.R2) missions. Ten rat
dams were flown on each mission, launched at the
approximate midpoint of pregnancy [gestational day
(GD) 9 for NIH.R1 and GD11 for NIH.R2] and landed
close to the time of parturition (GD20 of the rat’s
22-day pregnancy). The mission lengths were 11 and 9
days, respectively. The dams on each flight were
treated similarly. Continuous postflight video surveil-
lance of both NIH.R1 and NIH.R2 rat dams, including
time-lapse recordings of labor and delivery, permitted
us to replicate the parturition analyses. This was par-
ticularly important because the NIH.R1 study involved
performing a unilateral hysterectomy on each dam
soon after recovery on GD20, the major difference be-
tween the two flights. This was done so that both fetal
and neonatal samples could be obtained from each of
the NIH.R1 subjects (1).
MATERIALS AND METHODS
Subjects. Forty nulliparous, pregnant Sprague-Dawley
rats (Taconic Farms, Germantown, NY) weighing between
165 and 205 g were used. The time-bred dams were shipped
to Kennedy Space Center (KSC) on GD2 (spermatozoa posi-
tive GD1). Animals were housed in a room with controlled
lighting (6 AM to 6 PM) and temperature (22°C). Pregnant
rats were housed individually in standard vivarium cages (47
cm 26 cm 21 cm) with corncob bedding material. Rat
chow and water were available ad libitum. All animal proce-
dures adhered to NASA guidelines and the NIH Guide for the
Care and Use of Laboratory Animals. [DHHS Publication No.
(NIH) 85-23, Revised 1985, Office of Science and Health
Reports, Bethesda, MD 20892].
Treatment of dams. Two treatment groups were used in
these experiments. For each study, 10 dams were housed in
groups of five in flight animal modules (described in Surgical
laparotomy of the NIH.R1 and NIH.R2 dams, below) and
exposed to launch, spaceflight, and landing (flight group).
Synchronous control dams (n10) were treated identically
to flight animals but were not exposed to launch, landing, or
spaceflight. These animals were run at the same gestational
ages as the flight group but with a 24-h delay relative to the
flight group to allow time for downlinking from the shuttle of
the previous day’s environmental conditions. In this way,
environmental parameters (i.e., temperature, humidity, and
exposure to augmented lighting during video recording) on-
board the shuttle could be mimicked for the synchronous
control group. The preflight (12:12 h) light-dark cycle was
maintained in the housing for both the flight and ground
groups. Before flight, dams were carefully matched according
to weight across flight and synchronous control conditions.
Maternal surgeries. All experimental dams sustained two
surgical procedures during the study (described below). On
GD7, surgical laparotomy was performed to confirm preg-
nancy and establish the number of implantation sites. Dams
were selected for inclusion in the study only if a minimum of
five embryos populated each of their paired uterine horns. On
GD20, immediately after recovery from the space shuttle, the
NIH.R1 dams (but not the NIH.R2 dams) were given a
unilateral hysterectomy under anesthesia, yielding for im-
mediate analysis of fetuses from all 10 dams (i.e., n10).
The same dams then recovered from anesthesia, completed
gestation, and underwent vaginal delivery of pups from the
remaining uterine horn, thereby providing neonates for post-
natal analyses (n10). The NIH.R2 dams were either
observed until birth (n6) or dissected on recovery (n4).
Only the dams that underwent parturition are discussed in
this report.
Surgical laparotomy of the NIH.R1 and NIH.R2 dams.
Laparotomy was conducted on flight and synchronous control
dams under aseptic conditions on GD7, the earliest day on
which implantation sites (decidual swellings) can be reliably
visualized. This procedure is described elsewhere (1). Briefly,
the dam was anesthetized with isoflurane (IsoFlo, Abbott
Labs, North Chicago, IL) vapor using a nonrebreathing ro-
dent anesthesia unit (Viking Products, Medford Lakes, NJ).
The fur overlying the abdomen of the anesthetized rat was
shaved, the skin was cleansed with antiseptic and alcohol, a
veterinary opthalmic ointment was applied, and an antibiotic
and analgesic mixture [Microcillin, Anthony Products, Arca-
dia, CA (10,000 IU) and butorphanol tartrate, Fort Dodge
Labs, Fort Dodge, IA (10 mg/kg)] was given by subcutaneous
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injection. An incision was made, beginning 2 cm cranial to
the pubis and extending cranially 2–3 cm. Each uterine horn
was gently grasped between decidual swellings and gently
externalized for close visual inspection and counts of implan-
tation site, which were recorded. The uteruses were carefully
reinserted into the abdominal cavity, after which interrupted
sutures were used to close the peritoneum and muscle layer.
The overlying skin was then closed with 9-mm wound clips.
The entire procedure lasted 10 min.
On GD8 for NIH.R1 and on GD10 for NIH.R2, the flight
and synchronous control dams were housed in groups of five
within an animal enclosure module (AEM), which is NASA’s
flight cage for group-housed adult rodents. The animal cham-
ber portion of the AEM is a stainless steel mesh cage,
23.5 35.6 21.6 cm (in Earth-gravity orientation). Food
was available in the form of food bars, each about 2.5 2.5
20 cm, which were attached to the walls of the AEM. These
foodbars are fabricated from a commercial diet (Teklad Diets,
Madison, WI) and are nutritionally complete and resistent to
spoilage. Water was available from any of four Lixit valves
that protrude from a 21 11.1 15.2 cm stainless steel box
within the AEM. With the water system and food bars in
place, the AEM is a compact volume for five pregnant rats.
Airflow through the AEM is controlled by external fans that
create a near-laminar flow moving from ceiling to floor (in
normal Earth gravity orientation); the effluent airstream
moves through the waste tray containing activated charcoal
and absorbent filter.
Unilateral hysterectomy of the NIH.R1 dams. The purpose
of the unilateral hysterectomy was to provide a sample of
fetuses soon after return from spaceflight (see Ref. 1 for
further background and discussion of the rationale). Within
3 h after recovery from spaceflight, the first flight dam was
anesthetized. Anesthesia and surgical preparations were
identical to those described for the laparotomy procedure on
GD7. The uterine horns were exteriorized by extending the
midventral abdominal incision. The uterine horn removed
was alternated across rats in each treatment group. The horn
was ligated cranially and caudally with braided silk (20,
Ethicon, Somerville, NJ) and then excised. The incision was
closed by following the procedures used for laparotomy.
Video recording of labor and birth. Within several hours of
both recovery and unilateral hysterectomy (NIH.R1) or re-
covery (NIH.R2), the dams were housed singly in Plexiglas
observation cages (12.5 cm 8.5 cm 9.25 cm) lined with
corn cob bedding and placed in a vivarium. Food bars were
placed on the cage floor, and Lixit spouts were positioned
near the base of the cage to facilitate the mothers’ access to
food and water. Daily records of food bar consumption, water
intake, and body weight were maintained for the remainder
of the study. The dams were videotaped continuously begin-
ning soon after recovery until the completion of parturition
and the onset of nursing. A mirror was angled at the rear of
each observation cage to permit camera views from both the
front and rear of the cage. Cages were positioned four per
camera view. Red lighting was illuminated during the dark
phase to enable 24-h video data collection (12:1 record-to-
playback ratio).
Data analysis. Video data were analyzed by trained scor-
ers during real-time playback of the videotapes time locked to
a computerized event-scoring program (13). Briefly, the
amount of time dams spent feeding, drinking, or ambulating
was quantified with the use of this system. Interrater reli-
ability (IRR) for these measures was R
2
0.99. The number
and duration of labor contractions, number of neonates born,
placentophagia (ingestion of placenta), the total duration of
birth, maternal care (licking and handling of neonates), and
the onset of nursing were also encoded from the video record-
ings (IRR was R
2
0.98). Individual data were expressed as
litter means and analyzed with the use of ANOVA, t-tests, or
simple regression.
RESULTS
NIH.R1 and NIH.R2 dams at recovery. Because of
inclement weather, the shuttle carrying the NIH.R1
payload landed at the Hugh Dryden Flight Research
Facility (HDFRF) alternate landing site in California.
Within3hoflanding, the rats were delivered to the
payload receiving facility. The dams were then care-
fully unloaded from the AEMs, given a health exami-
nation, and weighed. Dam body weight gains at shuttle
load and unload were identical in the flight and syn-
chronous control groups (percent change from GD9 to
GD20 as follows: flight 45.7 2.0 and synchronous
control 42.4 1.7%; not significant). All of the dams
were deemed to be in good condition. Unilateral hys-
terectomy was performed on the flight group dams
without complication. Over the next several hours, the
dams showed characteristic signs of recovery from gen-
eral anesthesia and surgery.
The NIH.R2 payload landed at KSC. Within 3–4 h of
landing, the dams were given postflight health checks
and weighed. NIH.R2 dam body weight gains at shut-
tle load to unload were significantly different in the
flight and synchronous control groups [percent change
from GD11 to GD20 as follows: flight 23.8 1.0 and
synchronous control 28.6 1.0%; t(18) ⫽⫺4.1, P
0.001]. Six flight dams and six synchronous control
dams entered nest cages without manipulation.
Readaptation of flight dams to 1 G. In contrast to the
NIH.R1 dams, which received postflight surgery (i.e.,
unilateral hysterectomy), data from the NIH.R2 dams
provide an unbiased perspective of the effects of space-
flight on pregnant mothers’ behavioral readaptation to
1 G. These data are shown in Fig. 1. Results of the
time-lapse analyses are presented across three consec-
utive 12-h time intervals beginning with the dark
phase of the circadian cycle on GD20 [corresponding to
recovery (R) 12h(R12)] and ending 36 h later (at
R48), coincident with the onset of the light phase of
the cycle on GD22. This analysis revealed that flight
dams ambulated less than did synchronous control
dams [Fig. 1A; gravity F(1,10) 14.5, P0.01; New-
man-Keuls test, P0.05] but only during the dark
phase of the circadian cycle [time interval F(2,20)
12.5, P0.001; gravity time interval F(2,20) 7.5;
Newman-Keuls, P0.05]. During the light phase of
the cycle (R 24 and R 36), a floor effect was
observed that obscured potential group differences:
both flight and synchronous control dams locomoted for
less than 5% of the observation interval during the
lights-on period. Despite the reduced activity of the
flight dams during the dark phase of the cycle, the
amount of time dams spent eating and drinking was
equivalent to that of synchronous dams (Fig. 1B; grav-
ity F1), and the typical circadian rhythm of feeding
behavior was observed [time interval F(2,20) 29.3;
P0.0001].
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Labor in flight dams. Dams from both flights began
labor at the expected time (on GD22 and GD23) with
three exceptions: two NIH.R1 flight dams and one
synchronous dam did not show signs of impending
parturition by 1500 on GD23. In accordance with pre-
determined project requirements, the neonates of these
dams were delivered by cesarean section. There was no
corresponding requirement for NIH.R2; however, ce-
sarean delivery was performed on one dam from the
flight because she appeared to be in distress during
labor. Video failure caused data from two additional
NIH.R1 control animals to be lost. We present com-
plete data from eight flight dams and seven synchro-
nous control dams for NIH.R1 and from five flight
dams and six synchronous control dams for NIH.R2.
Figure 2 shows the results of the labor analyses for
the two flights. Beginning 6 h before the birth of the
first pup and throughout parturition, NIH.R1 flight
dams exhibited over two times more lordosis contrac-
tions than did synchronous control dams [Fig. 2, solid
bars; t(13) 3.0, P0.01]. Vertical contractions were
unaffected by spaceflight [t(13) 0.50, not significant].
Although contraction numbers differed, the average
duration of lordosis contractions was identical in the
two groups (flight 19.2 2.0 s, synchronous con-
trol 19.2 2.3 s).
Precisely the same pattern of results was observed in
the NIH.R2 dams [Fig. 2, open bars; t(9) 3.9, P
0.01]. Vertical contractions did not differ across groups
(not significant).
Birth. The dams successfully delivered strong and
viable pups. Table 1 shows the number of decidual
swellings, the numbers of neonates born, neonatal
birth weights, total duration of birth, ingestion of pla-
centas (placentophagia), and maternal behavior during
parturition, as measured by licking and retrieving of
Fig. 1. Behavioral readaptation of National Institutes of Health
(NIH) Rodent 2 (NIH.R2) flight and synchronous control dams to 1 G
(n6 per condition). Locomotion (top) and eating and drinking
(bottom) across consecutive 12-h dark-light-dark periods beginning
at 6 PM on gestational day (GD) 20 [recovery (R) 12h (R 12)], at
6 AM on GD21 (R 24), and at 6 PM on GD21 (R 36). Locomotion
differed across flight and synchronous dams during the dark phase of
the circadian cycle (*P0.05); eating and drinking were identical
across the groups.
Fig. 2. Top: behavioral expression of a lordosis contraction in the
parturient rat dam. Bottom: number of lordosis contractions ob-
served in NIH Rodent 1 (NIH.R1) (n15) and NIH.R2 (n12) flight
(left) and synchronous control (right) dams. Observations antedated
the birth of the first pup by 6 h and continued until the birth of the
last pup. The number of lordosis contractions observed in flight and
synchronous dams differed from one another (*P0.05).Note:
NIH.R1 dams underwent unilateral hysterectomy before parturition.
Table 1. Number of decidual swellings, number
of neonates born, neonatal birth weights, total
duration of birth, placentophagia, and maternal care
(licking and handling) of neonates during parturition
at1Ginpregnant dams flown on the NIH.R1 and
NIH.R2 missions and synchronous control dams
NIH.R1 NIH.R2
Flight Synchronous Flight Synchronous
No. decidual
swellings 13.10.3 13.10.2 13.50.4 13.3 0.3
No. neonates born 11.80.6 11.70.6 12.50.6 13.2 0.4
Neonatal birth
weights, g 6.10.4 6.30.6 5.90.4 5.8 0.4
Birth duration,
min 57.811.9 42.12.8 97.57.9 87.3 17.3
Placentophagia,
min 12.62.6 13.11.0 13.53.1 14.0 1.3
Maternal care,
min 47.45.9 53.95.1 34.02.1 34.7 3.9
Values are means SE. Neonatal birth weights were derived from
litter averages. Birth duration data for NIH.R1 dams were affected
because of unilateral hysterectomy, resulting in neonates populating
only one uterine horn. NIH.R1 and NIH.R2, National Institutes of
Health Rodent 1 and Rodent 2.
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neonates. In contrast to our initial prediction, morbid-
ity was very low. For NIH.R1, 4 of 60 pups born to
flight dams and 1 of 58 pups born to synchronous dams
were found dead on the day of birth. For each of the
other measures, identical results were obtained for
flight and synchronous conditions. The results of the
two flights were highly consistent with each other.
DISCUSSION
The pregnant spaceflight dams returned to Earth in
good condition. For NIH.R1, weight gain of dams dur-
ing flight, particularly important to the fetuses devel-
oping in utero, was comparable to the weight gain of
ground control dams. This finding is consistent with
normal Earth gravity body weight gains seen in adult
male rats during 14-day spaceflight missions (14).
NIH.R2 flight dams gained about 5% less than syn-
chronous controls, but differences were not observed in
any other measure of maternal, fetal, or neonatal out-
come after flight. Body weights of dams in the flight
and synchronous control conditions were identical at
launch for both flights. Because the NIH.R2 mission
was 2 days less in duration than the NIH.R1 mission,
one possibility is that initial postflight weight loss was
fully regained in flight on the longer 11-day mission
(NIH.R1) but not achieved by 9 days (NIH.R2). Addi-
tional studies are needed to characterize profiles of
body mass change in pregnant animals following
launch, on orbit, and on recovery from space.
The major finding of our analyses is that flight dams
had uncomplicated, successful vaginal deliveries. Par-
turition occurred at the appropriate gestational time.
Number and size of the litters were equivalent to those
of controls. Because we had noted during preflight
laparotomy the number of implantation sites in the
uterine horns of each dam on the 7th day of pregnancy,
we were also able to determine that fetal loss, i.e., the
difference between the number of implantations and
number of pups born to each dam, was equivalent
between groups. These findings were seen in both the
NIH.R1 and NIH.R2 flight groups. The correspondence
between these two data sets is striking particularly
because the NIH.R2 dams were not surgically manip-
ulated before collection of observational data.
Readaptation of flight dams to 1 G. The NIH.R2
dams provided the first systematic and continuous
observational data ever collected on the postflight re-
adaptation of rats to 1 G. The flight dams were gener-
ally less active than the synchronous control dams, as
indicated by reduced ambulation during the dark (ac-
tive) phase of the circadian cycle. There were differ-
ences in time spent eating and drinking between the
flight dams and the synchronous controls, and both
groups followed characteristic circadian fluctuations.
The postflight reduction in the locomotor activity of
dams is analogous to that of pregnant dams undergo-
ing adaptation from the normal1GonEarth to 1.5-G
hypergravity (14).
Labor after spaceflight. Labor contractions were af-
fected by spaceflight during pregnancy. The NIH.R2
dams did not receive the abdominal surgery shortly
before labor; therefore, their data are not confounded
in any way. Nevertheless, the pattern of results from
the two spaceflights was strikingly clear and reliable.
Quantification of lordosis contractions encoded dur-
ing playback of the video recordings revealed that
dams from both flights displayed dramatically more
lordosis contractions than did synchronous controls.
From the 6 h before parturition until the birth of the
last pup, flight dams had, on average, twice the num-
ber of contractions compared with controls. Despite
this difference, both the number of vertical contrac-
tions and the duration of visible labor were unaffected.
One interpretation of the increased number of con-
tractions is that the contractions were less efficacious
in the flight animals; thus additional contractions were
required to perform the work of moving fetuses
through the uterus and into the birth canal. Uterine
tissue analyzed from the NIH.R2 dams revealed reduc-
tions in connexin 43, the major gap junction protein in
myometrium (3). Uterine levels of connexin 26, located
primarily in endometrial epithelial cells, were un-
changed. It was suggested that decreased connexin 43
alters synchronization and coordination of labor con-
tractions, resulting in a requirement for more labor
contractions to complete parturition. Reports on the
histological status of the dams’ musculature provide
some insight into the consequences of spaceflight de-
conditioning on the abdominal muscles, many of which
serve postural (i.e., antigravitational) functions as well
as participate in the dramatic labor contractions.
Fejtek and Wassersug (6) reported that certain abdom-
inal muscle groups showed the kinds of decreases in
fiber diameter associated with unloading and weaken-
ing. The transverse abdominus was among those that
reflected such loss, and weakness of this muscle group
may have contributed to the requirement for additional
contractions. In contrast, the external obliques did not
show the expected atrophy. The seemingly paradoxical
differences between these abdominal muscle groups
can be resolved by combining the anatomic results with
observations of the dams’ in-flight behavior.
We analyzed video recordings of the pregnant dams
in the AEMs that were taken during flight (2). We
devised a kinematic coding scheme by which we clas-
sified and quantified the movements made by dams in
space and in the 1-G synchronous control condition.
With this analytic scheme, we found that movements
involving pitch and yaw were approximately equiva-
lent in the flight and synchronous animals. In contrast,
flight dams displayed about seven times more rolling
movements than did synchronous controls. This as-
tounding difference, we think, can be explained as a
consequence of the increased number of surfaces avail-
able in microgravity for ambulating and crawling.
Many of the movements from surface to surface involve
rolling movements along the rat’s body axis (the zaxis).
Thus, within the weightless environment of space,
the external obliques are likely to be exercised by the
mechanics of the dams’ rolling movements, the type of
activity frequently observed in microgravity but rarely
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on Earth. In contrast, the transverse abdominus mus-
cles are probably used minimally under conditions of
weightlessness, where postural control involves little
effort; hence, these muscles are not maintained as well
as they are in the synchronous controls. During expo-
sure of the pregnant females to spaceflight, decreased
uterine connexin 43 and deconditioning of the trans-
verse abdominus may have synergistically reduced the
effectiveness of uterine contractions.
Birth and maternal care of neonates after spaceflight.
Although more contractions may have been required
for parturition in the flight group, this difference did
not affect the duration or temporal patterns of birth.
The flight dams appeared to be competent mothers.
Maternal licking and handling of neonates during par-
turition and the consumption of birth fluids and mem-
branes (i.e., placentophagia) were indistinguishable in
flight and synchronous control dams. Within3hof
birth, mammary tissue was visually inspected and
mammary gland metabolic activity was analyzed (11).
These studies indicated that the dams’ were physiolog-
ically prepared for lactation.
In conclusion, the NIH.R1 and NIH.R2 spaceflight
experiments provide a convincing database for the fea-
sibility of studying mammalian development under
spaceflight conditions. It appears that the latter half of
the dams’ pregnancy and the offsprings’ gestation can
withstand the novel challenge of microgravity condi-
tions. The maternal-fetal system is superbly adaptable
indeed, for it can adjust to conditions never before
sustained during ontogenesis anytime or anywhere on
Earth.
One of the most surprising findings from the space
shuttle studies was the dams’ ability to have successful
vaginal delivery following spaceflight deconditioning
for most of the second half of the pregnancy. It must be
recognized, however, that the pregnant rats were not
immune to the deconditioning effects of space. They
showed the typical profile of postural and locomotor
signs of postflight muscle weakening. Moreover, there
was clearly a difference in their labor contractions,
indicating that we must be vigilant in future ventures,
particularly with exposures of longer duration.
Observational data of the rats’ in-flight behavior
provided insights important to understanding space-
flight effects on the bodies of dams as well as identify-
ing potential concerns for newborns. Labor contrac-
tions during birth provide an important source of
perinatal stimulation that promotes breathing and or-
ganized suckling in the neonate (13). Maternal effects
on offspring are potentially significant interpretive is-
sues that should be considered in future studies involv-
ing mammalian development under altered gravity
conditions.
We acknowledge Regina Abel, Michael Armbruster, Karen Cabell,
Cheryl Galvani, Kieu Lam, Nicole Mills, Erika Roldan, and David
Tanner for assistance with data collection and analysis. We thank
Joe Calabrese, Debra Reiss-Bubenheim, Paula Dumars, Carol El-
land, Nichola Hawes, Dana Leonard, Vera Vizar, Sharon Yavrom,
and other members of the science support team at KSC, HDFRF, and
NASA Ames Research Center. We acknowledge the crews of the
STS-66 and STS-70 flights, especially mission specialist J. T. Tan-
ner. We also thank the anonymous reviewers of this manuscript for
their critical comments.
This work was supported by NASA Grants NCC2-870 and
NAS121-10-40 and by National Institute of Mental Health Grants
MH-46485 and MH-28355.
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854 SPACEFLIGHT AND BIRTH
Downloaded from journals.physiology.org/journal/jappl (181.214.033.138) on August 26, 2021.
... Space flight litters had similar birth weights compared with all control groups when weights for female and male pups were analysed separately 34 . During labour, the flight dams had about twice as many lordosis contractions (which occur before the birth of the first pup) than synchronous controls, whilst the number of vertical contractions, which occur just before the expulsion of the pup from the vagina, did not differ 35 . ...
... The somatic granulosa and theca cells of the ovulated follicle then undergo a process called luteinization to become the corpus luteum, which synthesizes progesterone to prepare the uterus for implantation should conception occur 111 . In the NIH.R2 study [35][36][37] , 4 of 10 dams per group were euthanized 3 h after landing on GD 20, whereas the remaining 6 were allowed to give birth (GD 22-23) and were euthanized 3 h after delivery 36,37 . Fetal mass at GD 20 did not differ between the groups 37 . ...
... Fetal mass at GD 20 did not differ between the groups 37 . Maternal weight gain from GD 11 to GD 20 differed among the groups, with lower weight gain in the flight group than in the synchronous and no surgery vivarium controls (the percent maternal weight gain for NIH.R2 dams was reported differently in two different publications: 34.1 ± 1.6% and 46.5 ± 1.9% increases in weight for flight and synchronous controls, respectively 37 , and 23.8 ± 1.0% and 28.6 ± 1.0% increases for flight and synchronous controls, respectively 35 ). For flight and synchronous controls, Burden et al. 37 reported birth weights of 5.6 ± 0.1 g and 6.2 ± 0.1 g, respectively, and Ronca and Alberts 35 reported birth weights of 5.9 ± 0.4 g and 5.8 ± 0.4 g, respectively. ...
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Extended travel in deep space poses potential hazards to the reproductive function of female and male astronauts, including exposure to cosmic radiation, microgravity, increased gravity (hypergravity), psychological stress, physical stress and circadian rhythm disruptions. This Review focuses on the effects of microgravity, hypergravity and cosmic radiation. Cosmic radiation contains protons, helium nuclei and high charge and energy (HZE) particles. Studies performed on Earth in which rodents were exposed to experimentally generated HZE particles have demonstrated a high sensitivity of ovarian follicles and spermatogenic cells to HZE particles. Exposure to microgravity during space flight and to simulated microgravity on Earth disrupts spermatogenesis and testicular testosterone synthesis in rodents, whereas the male reproductive system seems to adapt to exposure to moderate hypergravity. A few studies have investigated the effects of microgravity on female reproduction, with findings of disrupted oestrous cycling and in vitro follicle development being cause for concern. Many remaining data gaps need to be addressed, including the effects of microgravity, hypergravity and space radiation on the male and female reproductive tracts, hypothalamic–pituitary regulation of reproduction and prenatal development of the reproductive system as well as the combined effects of the multiple reproductive hazards encountered in space.
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Oxidative stress has been implicated in the pathophysiology of numerous terrestrial disease processes and associated with morbidity following spaceflight. Furthermore, oxidative stress has long been considered a causative agent in adverse reproductive outcomes. The purpose of this review is to summarize the pathogenesis of oxidative stress caused by cosmic radiation and microgravity, review the relationship between oxidative stress and reproductive outcomes in females, and explore what role spaceflight-induced oxidative damage may have on female reproductive and developmental outcomes.
... Space-flown pregnant rats gave birth at the expected time; however, they exhibited twice as many 'lordosis' contractions during labor coupled with decreased uterine myometrial connexin 43 (gap junction) protein expression relative to controls, suggesting changes to the uterine smooth musculature tone with exposure to microgravity. However, the duration of labor, maternal weight gain, miscarriage/stillbirth rate, litter size, neonatal birthweight, placentophagia, and maternal care patterns were not significantly different from ground controls [40,41]. Importantly, NIH.R1 and R2 offspring were flown for the second half of the rats' gestational period, after organogenesis was complete, and returned to Earth for parturition. ...
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Outer space is an extremely hostile environment for human life, with ionizing radiation from galactic cosmic rays and microgravity posing the most significant hazards to the health of astronauts. Spaceflight has also been shown to have an impact on established cancer hallmarks, possibly increasing carcinogenic risk. Terrestrially, women have a higher incidence of radiation-induced cancers, largely driven by lung, thyroid, breast, and ovarian cancers, and therefore, historically, they have been permitted to spend significantly less time in space than men. In the present review, we focus on the effects of microgravity and radiation on the female reproductive system, particularly gynecological cancer. The aim is to provide a summary of the research that has been carried out related to the risk of gynecological cancer, highlighting what further studies are needed to pave the way for safer exploration class missions, as well as postflight screening and management of women astronauts following long-duration spaceflight.
... To date, studies of ovarian function and fertility in mice exposed to microgravity during NASA Space Shuttle flights were of short duration (<12 days) and, importantly, all included the effects of live reentry prior to collection of tissues and analysis of animal behavior 3,7 . Similarly, pregnant female rats flown on Cosmos 1514 (1982), NASA-NIH Rodent (R)1 (STS-66 in 1994), and NASA-NIH R2 (STS-70 in 1995) were of short duration (4.5-11 days) and had live animal return [8][9][10] . Notably, in the pregnant rats no effects of spaceflight on healthy and atretic ovarian antral follicle populations, fetal wastage in utero, plasma concentrations of progesterone and luteinizing hormone (LH) or pituitary content of follicle stimulating hormone (FSH) were noted 8 . ...
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The contents of this book are: Physiological Adaptation to Space Flight: Overall Adaptation to Space Flight and Implications; The Neurovestibular System; Performance; The Cardiopulmonary System; Nutrition; Bone and Mineral Metabolism; Hematology, Immunology, Endocrinology, and Biochemistry; Microgravity: Stimulations and Analogs; Health Maintenance of Space Crewmemebers: Medical Evaluation for Astronaut Selection and Longitudinal Studies; Biomedical Training of Space Crews; Ground-Based Medical Programs; Countermeasures to Space Deconditioning; Medical Problems of Space Flight: Toxic Hazards in Space Operations; Radiation Exposure Issues and Medical Care and Health Maintenance in Flight.
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