close

Вход

Забыли?

вход по аккаунту

?

Detection of pregnancy and monitoring patterns of uterine and fetal growth in the marmoset monkey (Callithrix jacchus) by real-time ultrasonography.

код для вставкиСкачать
American Journal of Primatology 361-13 (1995)
RESEARCH ARTICLES
Detection of Pregnancy and Monitoring Patterns of
Uterine and Fetal Growth in the Marmoset Monkey
(Callithrixjacchus) by Real-Time Ultrasonography
A.-K. OERKE, A. EINSPANIER, AND J.K. HODGES
Department of Reproductive Biology, German Primate Centre, Gottingen, Germany
The purpose of this study was to evaluate the potential of real-time ultrasonography for detecting and monitoring pregnancy in the common marmoset, Ultrasound was performed transabdominally on unsedated females
using a 7.5 MHz linear or intraoperative sector probe. Pregnancies were
timed using progesterone measurements in twice weekly blood samples to
determine the day of ovulation. Eight pregnancies were examined three
times a week until day 30, twice a week until day 80, and once a week until
birth. Detection of pregnancy was possible on day 15, on average, by the
appearance of a double endometrial echo indicating fluid accumulation in
the uterus. The uterine lumen thus formed was first measurable on day 21
on average. Diameter of the pregnant uterus was significantly greater
than that of the nonpregnant organ by day 38. Thereafter, the dimensions
of uterus and uterine lumen showed a similar pattern of growth until day
75, when measurements became inaccurate due to increasing uterine pliability. Embryonic development was characterized by the initial expansion of the gestation sacs and the appearance of individual embryos by day
33. Detection of heart beat a t approximately day 54 allowed confirmation
of number and viability of the embryos. With the visualization of the
skulls by day 82, it was possible to determine fetal position and to monitor
fetal growth by measurement of the biparietal diameter. All pregnancies
were of normal length (140-145 days) resulting in viable offspring. It can
be concluded that ultrasonography is suitable for detecting and monitoring pregnancy in the marmoset monkey and as a non-invasive method, has
the potential for being routinely used in this and other species of
Callitrichidae. o 1995 Wiley-Liss, Inc.
Key words: pregnancy, ultrasonography, marmoset monkey
INTRODUCTION
The common marmoset (CuZZithrixjucchus) is a small New World monkey of
the family Callitrichidae. Due to its adaptability to, and fertility in captivity, it is
widely used as an experimental animal in biomedical research and, more recently,
Received for publication February 28, 1994;revision accepted September 19,1994.
Address reprint requests to Ann-Kathrin Oerke, Department of Reproductive Biology, German Primate
Centre, Kellnerweg 4,37077 Gdttingen, Germany.
0 1995 Wiley-Liss, Inc.
2 / Oerke et al.
in conservation biology as a model for endangered species. For both research and
colony management purposes, practical and reliable methods for detecting and
monitoring pregnancy are needed.
Since female marmosets show neither menstruation nor estrus swellings and
mating occurs throughout most of pregnancy [Hearn & Lunn, 19751, there are no
reliable visible signs of reproductive status. Consequently, endocrine methods
based on either plasma or urinary hormone analysis [Chambers & Hearn, 1979;
Harlow et al., 1983; Eastman et al., 1984; Heger & Neubert, 19881have been used
for this purpose. With respect to pregnancy detection, hormone determinations can
be informative from day 16-20 onwards [Hodges et al., 1983; Hearn et al., 19881,
but require serial blood sampling and are generally time consuming and expensive
to perform. A much simpler diagnosis of pregnancy is possible by abdominal uterine palpation [Hearn & Lunn, 1975; Mitchell &Jones, 1975; Phillips & Grist, 19751
although the method can only be used with confidence four weeks after ovulation.
Neither approach, however, allows accurate staging of pregnancy and their usefulness for assessing embryonic development, and fetal growth is limited. To date,
the only opportunity to obtain this information has been from studies on material
collected during surgical and/or terminal procedures [Phillips, 1976b; Chambers &
Hearn, 1985; Smith et al., 1987; Merker et al., 1988; Moore et al., 19881. An
alternative for detecting and monitoring pregnancy, as has been proven in human
and domestic animals, is the use of real-time ultrasonography. In a non-invasive
way this technique enables direct visualization of the reproductive organs, providing immediate and reproducible results. Among non-human primates, ultrasound
has been mainly applied to macaques [Peterson et al., 1972; Sabbagha et al., 1975;
Nyland et al., 1984; Cho et al., 1987; Korte et al., 1988; Tarantal & Hendrickx,
1988a, 1988b, 1988~;
Shimizu, 1988; Conrad et al., 19891. Its potential for use with
the much smaller New World monkeys, Callitrichidae, has not been accurately
assessed. An initial attempt at using ultrasound for examination of pregnancy in
the marmoset is mentioned in Du Boulay and Wilson [19881, but details of the
study are not given.
The aims of the present investigation were, therefore, (i) to evaluate the potential of ultrasonography for detecting and monitoring pregnancy in the marmoset monkey, and (ii) to provide additional information on the characteristics of
embryonic development and fetal growth in this species by use of a non-invasive
method.
METHODS
Animals
A total of eight pregnancies was examined in five marmoset monkeys. Females
lived with males either as pairs or in family groups. Four females were multiparous having had normal pregnancies resulting in viable offspring. One female was
nulliparous prior to the onset of the study. Animals were maintained in the primate facilities at the German Primate Centre under conditions described by Heistermann et al. [19931.
Timing of Pregnancy
Ovarian cycles were monitored by measurement of progesterone in blood samples taken twice a week. Plasma was assayed by a direct, non-extraction enzymeimmunoassay [Hodges et al., 19881modified by Heistermann et al. [19931.The day
of ovulation (day 0) was defined as the day before progesterone levels increased
above a value of 10 ng/ml as originally reported by Harlow et al. [1983]. The day
after ovulation (day 1) was taken to be the first day of pregnancy. Due to the
Ultrasonography of Pregnancy in the Marmoset / 3
6
Fig. 1. Diagrammatic representation of a marmoset uterus in cross section as visualized by ultrasound. 1 =
abdominal wall (arrow indicates direction of scan); 2 = uterus; 3 = endometrium; 4 = uterine lumen; 5 & 6
indicate measurements of ventro-dorsal and transverse diameter, respectively.
frequency of blood sampling however, an error of * 1day in estimating the time of
ovulation and therefore gestation age is to be expected.
Ultrasonography
Females were examined by ultrasound three times a week until day 30, twice
a week between day 30 and 80, and once a week from day 80 until birth. Ultrasonography was performed transabdominally on unsedated and unshaved animals.
In order to minimize movements during the scanning procedure, the females were
restrained on a padded frame to which they had been conditioned during a training
period prior to the study. Animals tolerated the device well and appeared relatively relaxed. Fruit or pap was offered as a reward during each examination.
Ultrasonography was carried out with a Picker CS 9000 real-time scanner
fitted with two probes operating a t a frequency of 7.5 MHz. An intraoperative
sector probe was used to provide detailed images of early pregnancy, whereas a
linear probe was preferred for surveys of late gestational stages. Examinations
took 5-10 minutes. After warmed transmission gel had been applied thickly to the
abdomen of the animal the probe was placed perpendicular to the Iong axis of the
female in the deep pelvic region and moved slowly in a cranial direction. Uterine
appearance was documented and images were printed on photopaper and recorded
on videotape. All measurements were made from cross-sections of the uterus (see
Fig. 1).Diameter (ventro-dorsal and transverse) and circumference of the uterus
were taken with internal calipers, the values of which were used by the system to
automatically calculate volume (method of ellipse) and area. Embryonic development was monitored and fetal growth recorded by regular measurements of the
transverse diameter of the skulls (biparietal diameter = BPD). Neonates were
weighed and measured for comparison with data for offspring not exposed to ultrasound during intrauterine development.
Data Analysis
Statistical comparisons between uterine measurements in pregnant and nonpregnant females were made using an unpaired t-test. A P value of <0.05 was
taken to indicate a significant difference.
4 / Oerke et al.
Fig. 2. Ultrasonogram of the uterus in a nonpregnant (a) and a n early pregnant (b)marmoset monkey. Note
the central linear echo in the nonpregnant organ in contrast to the presence of a double endometrial echo during
early pregnancy (arrows). Uterine dimensions in both (a) and (b) are 6 x 8 mm as measured in ventro-dorsal and
transverse section.
RESULTS
Detection of Pregnancy
In ultrasound images, the uterus of nonpregnant marmosets appeared as a
dark, oval structure giving a sparse echo. The nonpregnant organ was characterized by the presence of a single central bright line reflecting the close apposition
of the endometrial surface (Fig. 2a). The mean diameter of the nonpregnant uterus
during the luteal phase of the cycle was 5.7 2 1.0 mm and 8.2 & 0.8 mm as
measured in ventro-dorsal and transverse sections, respectively (n = 20 from 6
animals).
The first detectable change in the ultrasound image of the uterus during pregnancy was the appearance of a double endometrial echo as the endometrial surface
began to be separated by the fluid-containing, and therefore, weakly echogenic
uterine lumen. This can be seen in Figure 2b as a double bright line separated by
a dark region in the centre. The figure provides an example of the appearance of
the uterus in a pregnant female 20 days after ovulation. The time at which a
double endometrial echo was first visible in the eight pregnancies studied ranged
between 12 and 18 days after ovulation, with a mean 2 SD of 15.2 2 2.5 days.
Changes in Uterine Measurements
The diameter of the uterus was recorded during the first 90 days of pregnancy.
Changes in the transverse dimension are shown in Figure 3a and 3b for mean and
individual data, respectively. Results for measurements in ventro-dorsal section
(mean values) are illustrated in Figure 5. No obvious increase in uterine diameter
by either measurement was discernable during the first month of pregnancy after
which the uterus displayed a continuous growth pattern. Mean values for uterine
diameter during gestation were significantly elevated over those in nonpregnant
females on day 38 in both dimensions. In general, the ventro-dorsal dimension
(Fig. 5) was smaller and showed a less pronounced increase when compared to the
transverse diameter (Fig. 3a).
As the endometrial surface began to separate during early pregnancy, a small
fluid-filled lumen within the uterus became visible (Fig. 2b). On average, the
uterine lumen was first measurable on day 21 (mean ? SD; 20.7 ? 2.3 days) with
Ultrasonography of Pregnancy in the Marmoset I 5
45
50
40
1
Mean f S.D. (n = 8 )
-
n
2
35-
v
30
-
3
25-
s
2
.,-I
k
s
20 -
15 - NP
lo-
1
I
5 01
a
I
I
I
I
I
I
I
I
I
I
I
0
10
20
30
40
50
60
70
80
90
100
50 45
o
-
Singleton
A
40 -
V
0
A
T
.
Twins
Triplets
h
g
35-
k
4
30-
A
5
V
*.
s
8
&%
Z.X&BX
n$$*Gg""
l o5 -
T
V
8".
m #
b
A
yAm
VAV
A
15 -
01
0
*llTxA
im
20 -
.rl
5
o h
.P
25-
.A
2
vn
.
A
mm
v
v
0
V
I
I
I
I
I
I
I
I
I
I
I
0
10
20
30
40
50
60
70
80
90
100
Days of pregnancy
Fig. 3. Changes in transverse uterine diameter during the first 90 days of pregnancy in the marmoset monkey.
Mean values ( * SD) of eight pregnancies are shown (a).Data have been plotted at 5-day intervals. Mean value
(t SD) for the diameter of the nonpregnant uterus (NP, ). is given for comparison. Corresponding data for
individual pregnancies are shown (b) 0 singleton, A V 0 twins, A V triplets.
6 / Oerke et al.
40
L
P)
r
17
2 5 I-
--
4
; 20
d
0
a
I
I
I
I
I
I
I
1
I
I
10
20
30
40
50
60
70
80
90
100
a
40
o
35
E
E
v
k
Singleton
A
V
0
a
A
V
.
Twins
Triplets
v
.
30
25
;20
A.
0
0
.
AA
d
.a
.
ma
15
0
E
fie
10
T
mmv
...
A
c V17vA
VA
*>aV V
mM A
ro
om I
CPA
A AV A
0)
5
A
0
v
a. 0
a ma
P)
4
El
A
I
0
0
V
0
0
.
V
OA
w a m ~ o v o
am m a P v
5
- 8 0
n worn D
n-worn
I
0
b
-
0
10
O Il
U
20
- 0
0
I
1
I
I
I
I
I
30
40
60
60
70
80
90
I
100
Days of pregnancy
Fig. 4. Changes in transverse diameter of the uterine lumen during the first 90 days of pregnancy in the
marmoset monkey. Mean values ( L SD) of eight pregnancies are shown (a).Data have been plotted at 5-day
intervals. Corresponding data for individual pregnancies are shown (b) 0 singleton, A V 0 twins, A 7 m
triplets.
Ultrasonography of Pregnancy in the Marmoset / 7
25
-
uterus
T
o uterine lumen
20 h
1 1 5 -
v
h
4
al
10 - N P
a
1
5 -
0
I
0
10
20
30
40
I
I
I
I
I
I
50
60
70
80
90
100
Days of pregnancy
Fig. 5. Pattern of growth of the uterus (0 external diameter) and uterine lumen (0 internal diameter) as
indicated by measurements in the ventro-dorsal section during the first 90 days of pregnancy in the marmoset
monkey. Values are mean i SD (n = 8).Mean (? SD) ventro-dorsal diameter of the nonpregnant uterus (NP,
B) is given for comparison. Note relatively constant relationship between external and internal measurements,
indicating lack of change in thickness of uterine wall.
a range between day 17 and 24. Its dimension when first measurable was 1 mm in
ventro-dorsal and 2 mm in transverse section. Only slight expansion of the uterine
lumen occured until day 30 of gestation after which a progressive increase in
diameter was seen. Changes in the diameter of the uterine lumen during the first
90 days of pregnancy are shown in Figures 4a (transverse section) and 5 (ventrodorsal section).
Comparison of the growth pattern of the uterus and uterine lumen (Fig. 5)
indicates that the uterine wall maintained its thickness throughout the period
studied. In all measurements taken, an increase in variability was noted with
advancing pregnancy (see Figs. 3, 4, and 51, probably due to the increasing pliability of the uterus beyond day 70. Although data for individual animals indicate
a tendency for all dimensions recorded to be larger in triplet than in twin or
singleton pregnancies (see Figs. 3b and 4b), the data pool was too small to permit
statistical analysis. Measurements after day 90 were not possible due to the size of
the image of the uterus exceeding that of the ultrasound monitor.
Embryonic and Fetal Development
Within the first month of pregnancy, the increase in size of the uterine lumen
largely reflects the growth of the fluid-filled gestation sacs. The presence of multiple gestation sacs was notable by the appearance of fine echos representing the
interface of adjoining structures. Individual embryos first became visible on day 33
(mean ? SD; 33.2 t 3.1 days, range 28-38) and were seen as small, bright structures within the dark uterine cavity. Confirmation of the number and viability of
the embryos was possible by detection of embryonic heart beat from on average day
54 of pregnancy (mean 2 SD; 54.2 t 2.0 days, range 52-57).
8 I Oerke et al.
Fig. 6. Ultrasound image of twin fetal heads (facing left) on day 112 of pregnancy. Skulls appear of different
size due to differing positions of fetuses within the uterus.
Accurate measurement of body structures was difficult due to the usual presence of multiple embryos or fetuses. Individual fetal skulls could, however, be
identified and measured from day 82 of pregnancy (mean r SD; 81.9 f 2.8 days,
range 76-84). The image of two fetal heads on day 112 of pregnancy is given in
Figure 6. The pattern of growth of the fetal skulls as determined by measurements
of transverse diameter (biparietal diameter = BPD) is shown in Figure 7. The
initial rise in BPD appears to occur at a faster rate than that seen over the last
month of gestation. No obvious differences between BPD measurements for singleton, twin, or triplet fetuses were apparent (Fig. 7b, mean values for twins and
triplets shown). Measurements of BPD by ultrasound examination during the
week before parturition (mean f SD; 17 2 0.9 mm) compared well with those
obtained by direct measurements of neonates (mean SD; 19 2 0.6 mm).
*
DISCUSSION
The results of this study demonstrate that real-time ultrasonography is a
practical and reliable method for the early detection and monitoring of pregnancy
in the marmoset monkey. Frequent and regular scannings of pregnant females
appeared to have no influence on the progression and outcome of gestation. All
pregnancies ended in normal births producing viable offspring (1 x singleton, 3 x
twins, 4 x triplets) after gestation lengths ranging from 140 to 145 days (mean 142
days).
In the non-fertile cycle of the marmoset monkey, the uterus was characterized
by a single central bright echo as has also been described for the nonpregnant
organ in women [Callen et al., 19791 and rhesus and cynomolgus macaques [Morgan et al., 1987; Tarantal & Hendrickx, 1988a; Foster et al., 19921. The first
indication of pregnancy in the marmoset was the appearance of a double endometrial echo in the uterus on day 15 on average. Similar uterine changes forming
a thick double-line during early pregnancy in the marmoset were reported in brief
by Du Boulay and Wilson [1988] although information on the exact time at which
pregnancy diagnosis was possible was not given.
The double echo reflects the separation of the endometrial surfaces presumably caused, a t least initially, by an accumulation of maternally derived secretions. Since implantation in the marmoset does not commence before day 11after
20
-
18
-
14
-
12
-
10
-
16
Ei
-E
Ultrasonography of Pregnancy in the Marmoset / 9
n
k
8 -
6 4 2 0 '
70
I
I
I
I
I
I
I
I
80
90
100
110
120
130
140
150
18 16 14 12 Ei
Ei 10 20
8
0
; . ; *
0
0
0
.
n
k
D
8 -
0
0
8
.
. *
0
0
5
Neonates
0
0
Singleton n = l
Twins
n=3
Triplets
n=4
0
0
0
O
0
6 -
1
0
0
4 2 0 '
b
I
I
I
I
I
I
I
1
80
90
100
110
120
130
140
150
70
Days of pregnancy
Fig. 7. Changes in biparietal diameter (BPD) of fetal marmoset skulls between day 80 of pregnancy and birth.
Mean values (+ SD) for eight pregnancies are demonstrated (a). Data for singleton (0)
and mean values for
are shown (b).The last point in each graph is the BPD of neonates.
twins (0)and triplets
(m)
10 / Oerke et al.
ovulation [Moore et al., 19851, and an early post-attachment blastocyst has a total
diameter of less than 1mm [Summers et al., 19931, ultrasonographic visualization
of the conceptus a t this early stage is unlikely.
In other primates an accumulation of fluid in the early pregnant uterus leads
to comparable ultrasonograms. In rhesus and cynomolgus macaques the initial
indication of pregnancy is an irregularity of the central linear echo [Tarantal &
Hendrickx, 1988al followed by the appearance of intrauterine fluid [Tarantal,
19921. The early pregnant uterus of Macaca fascicularis shows changes in endometrial echogenicity, swelling of the central line [Conrad et al., 19891,and a lumen
detectable as a dark gap [Korte et al., 19881. In other studies in macaque monkeys,
however, the presence of a gestation sac at around day 20 is reported as being the
first sign of pregnancy visible by ultrasound [Nyland et al., 1984; Cho et al., 1988;
Shimizu, 19881.
Based on the present results, prenatal development in the marmoset monkey
as followed by ultrasonography can be conveniently divided into three phases:
expansion of the gestation sacs, embryonic development, and fetal growth. The
period represented by the expansion of the gestation sacs is associated with further
accumulation of intrauterine fluid and can be seen by ultrasound as an increased
separation of the endometrial surfaces. Although it is possible to identify gestation
sacs from day 21 onwards, their number cannot be accurately determined a t this
stage. Repeated scannings during this first phase of pregnancy indicate a gradual
increase in the size of the uterine lumen whilst the external dimensions of the
organ remain relatively constant. The time a t which an increase in mean uterine
diameter can be determined (i.e., between day 33 and 38) approximates to that at
which pregnancy diagnosis is first possible by abdominal palpation [Hearn &
Lunn, 1975; Mitchell & Jones, 1975; Phillips & Grist, 19751.
The embryos themselves become visible by ultrasonography between day 28
and 38 of pregnancy. This can be taken to represent the start of the second gestational phase which appears to include all stages of embryonic development described by Phillips [1976b] and Merker et al. [1988]. Although the embryos can be
clearly seen within the uterus, details of embryonic structures are not possible to
monitor by ultrasound at this stage. A notable event, however, is the onset of the
heart beat on day 54, on average, which is important in allowing confirmation of
the number of individual embryos. Since, according to histological sections, the
heart in the marmoset is not fully developed until day 60170 [Phillips, 1976b;
Merker et al., 19881it would thus appear that the onset of the heart beat precedes
the completion of anatomical development of the organ. From a diagnostic point of
view, detection of heart beat is of importance in providing the first reliable indication of embryonic viability and also being useful as a routine check throughout
the course of gestation.
Although embryonic development cannot be monitored in sufficient detail to
enable staging of pregnancy, changes in uterine size provide useful information in
this regard. As illustrated in Figure 5, the diameters of the uterus and uterine
lumen display similar, regular growth curves between days 35 and 90. Since,
however, both measurements show an increase in variability after about day 75,
the most reliable time for using ultrasonographical measurements of the uterus for
staging pregnancy would be within the period 35-75 days gestation. Earlier studies using transabdominal palpation described similar patterns of uterine growth to
those obtained here [Hearn & Lunn, 1975; Mitchell 8z Jones, 1975; Phillips &
Grist, 19751. Direct comparison of uterine dimensions obtained by ultrasound and
transabdominal palpation with respect to the stage of pregnancy is however difficult due to the use of varying methods for monitoring time of ovulationlconception.
Ultrasonography of Pregnancy in the Marmoset / 11
Nevertheless, the data as shown here tend to confirm the findings of Hearn and
Lunn [19751 and Mitchell and Jones [19751, whereas the values given by Phillips
and Grist [19751possibly overestimate the actual stage of gestation. The dificulty
of obtaining reliable uterine measurements between day 70 and 90 as experienced
in the present study using ultrasound, is also reported for transabdominal palpation [Mitchell & Jones, 1975; Phillips & Grist, 19751. Whilst the increasing softness and pliability of the uterus is clearly an important factor, the results presented here indicate that the number of embryos is also likely to be an additional
source of inter-individual variation. Since, however, the data pool in the present
investigation was limited, the extent of this variation and relevance in practical
terms could not be assessed.
Little difference was found between the information obtained from measurements of ventro-dorsal and transverse dimensions. Combined measurements of the
uterus and uterine lumen in both planes would, however, be likely to result in a
more reliable assessment of stage of pregnancy, than by determination of any
single parameter. The calculation of area or volume did not, in our experience,
provide useful additional information, and manual tracking of circumference contains a high degree of error and is not recommended.
Coincident with the end of the period of embryonic development, which according to Phillips [1976b] and Merker et al. (19881 occurs at around day 80, the
fetal skulls become visible by ultrasound. This represents the beginning of the
third ultrasonographically determined phase of prenatal development. The time at
which heads can be detected appears to precede the onset of ossification, since in an
earlier radiological study by Phillips [1976al, skeletal formation was first noted at
around day 110. Mitchell and Jones [1975] and Phillips and Grist [1975] were able
to transabdominally palpate heads between day 90 and 120, the same period during which differentiation of singleton from twin and triplet pregnancies using this
method was reported by Hearn and Lunn [19751. Although other body parts also
become easier to distinguish by ultrasonography after day 90, the presence of
multiple fetuses usually causes difficulties in monitoring individual structures.
The skulls, however, provide reliable information about fetal number and position
in the uterus. Movements of the fetal heads provide an additional means of confirming fetal viability. Based on the measurements of the biparietal diameter
(BPD); fetal age and delivery are predictable, although a decrease in accuracy
must be accepted due to a less pronounced growth of the skulls from day 120
onwards. This tendency is also indicated by the ultrasound data published by Du
Boulay and Wilson [19881, whereas Chambers and Hearn [ 19851, using material
collected at hysterectomy, found a continuous increase in the width of the fetal
heads until birth. For corresponding pregnancy stages the head size as measured
by abdominal palpation [Phillips & Grist, 19751in general, appears to be smaller.
Dimensions of the heads in neonates in this study, however, were comparable to
fetal BPD measurements in the week before birth.
CONCLUSIONS
1. Ultrasonography is a practical and reliable non-invasive method for detecting and monitoring pregnancy in Callithrix jacchus and can be safely applied in
longitudinal studies.
2. Detection of pregnancy is possible as early as 12 days after ovulation (day 15
on average) i.e., from the time of implantation onwards.
3. Pregnancy can be staged most accurately between days 35 and 75 by measurements of external and internal uterine diameters.
12 / Oerke et al.
4. Monitoring of fetal growth is reliable by measurements of the biparietal
diameter from around day 80.
ACKNOWLEDGMENTS
Special thanks to Dorothea Blank and Cornelia Casper for looking after the
animals and helping during all of the examinations. Dr. Michael Heistermann is
gratefully acknowledged for advice with the progesterone assay.
REFERENCES
Callen, P.W.; De Martini, W.J.; Filly, R.A.
The central uterine cavity echo: A useful
anatomic sign in the ultrasonographic
evaluation of the female pelvis. RADIOLOGY 131:187-190,1979.
Chambers, P.L.; Hearn, J.P. Peripheral
plasma levels of progesterone, oestradiol
17p, oestrone, testosterone, androstenedione and chorionic gonadotrophin during
Dregnancy in the marmoset monkey, Caliithyix jrkchus. JOURNAL OF REPRODUCTION AND FERTILITY 56:23-32.
1979.
Chambers, P.L.; Hearn, J.P. Embryonic, foetal and placental development in the common marmoset (Callithrix jacchus). JOURNAL OF ZOOLOGY, LONDON (A) 207:
545-561,1985.
Cho, F.; Narita, H.; Ono, T.; Honjo, S. Early
pregnancy diagnosis by the ultrasonographical device and observation of fetal
growth in cynomolgus monkeys (Macaca
fascicularis). EXPERIMENTAL ANIMAL
36:223-228, 1987.
Conrad, S.H.; Sackett, G.P.; Burbacher, T.M.
Diagnosis of early pregnancy by ultrasound in Mucacu fascicularis. JOURNAL
OF MEDICAL PRIMATOLOGY 18:143154, 1989.
Du Boulay, G.H.; Wilson, O.L. Diagnosis of
pregnancy and disease by ultrasound in exotic species. SYMPOSIA OF THE ZOOLOGICAL SOCIETY LONDON 60:135150, 1988.
Eastman, S.-A.K., Makawiti, D.W.; Collins,
W.P.; Hodges, J.K. Pattern of excretion of
urinary steroid metabolites during the ovarian cycle and pregnancy in the marmoset
monkey. JOURNAL OF ENDOCRINOLOGY 102:19-26,1984.
Foster, W.G.; Stals, S.I.; McMahon, A. A prospective analysis of endometrial cycle
changes by ultrasound in the female cynomolgus monkey. JOURNAL OF MEDICAL
PRIMATOLOGY 21:30-34,1992.
Harlow, C.R.; Gems, S.; Hodges, J.K.;
Hearn, J.P. The relationship between
plasma progesterone and the timing of ovulation and early embryonic development in
the marmoset monkey (Callithrix jacchus).
JOURNAL OF ZOOLOGY, LONDON 201:
273-282,1983.
Hearn, J.P.; Hodges, J.K.; Gems, S . Early
secretion of chorionic gonadotrophin by
marmoset embryos in vivo and in vitro.
JOURNAL OF ENDOCRINOLOGY 119:
249-255, 1988.
Hearn, J.P.; Lunn, S.F. The reproductive biology of the marmoset monkey, Callithrix
jacchus. BREEDING SIMIANS FOR DEVELOPMENTAL BIOLOGY. LABORATORY ANIMAL HANDBOOKS 6:igi202, 1975.
Heger, W.; Neubert, D. Monitoring of ovulation and pregnancy by measuring steroids
in the urine of marmosets. Pp. 71-82 in
NON HUMAN PRIMATESDEVELPOMENTAL BIOLOGY AND TOXICOLOGY. D. Neubert; H.-J. Merker; A.G. Hendrickx, eds. WierdBerlin, Ueberreuther
Wissenschaft, 1988.
Heistermann, M.; Tari, S.; Hodges, J.K.
Measurements of faecal steroids for monitoring ovarian function in New World primates, Callithrichidae. JOURNAL OF REPRODUCTION AND FERTILITY 99:243251, 1993.
Hodges, J.K.; Henderson, C.; Hearn, J.P. Relation between ovarian and placental steroid production during early pregnancy in
the marmoset monkey (Callithrix jacchus).
JOURNAL OF REPRODUCTION AND
FERTILITY 69:613-621,1983.
Hodges, J.K.; Green, D.I.; Cottingham, P.G.;
Sauer, M.J.; Edwards, C.; Lightman, S.L.
Induction of luteal regression in the marmoset monkey (Callithrix jucchus) by a gonadotrophin-releasing hormone antagonist
and the effects on subsequent follicular development. JOURNAL OF REPRODUCTION AND FERTILITY 82:743-752,1988.
Korte, R.; Vogel, F.; Osterburg, I. Determination of pregnancy in Macaca fascicularis
by use of ;ltrasonography. Pp..101-107 in
NON HUMAN PRIMATESDEVELOPMENTAL BIOLOGY AND TOXICOLOGY. D. Neubert; H . J . Merker; A.G. Hendrickx, eds. WiedBerlin, Ueberreuther
Wissenschaft, 1988.
Merker, H.-J.; Sames, K.; Csato, W.; Heger,
W.; Neubert, D. The embryology of Callithrix jucchus. Pp. 217-239 in NON HUMAN PRIMATEELDEVELOPMENTAL
BIOLOGY AND TOXICOLOGY. D. Neu-
Ultrasonography of Pregnancy in the Marmoset / 13
bert; H.-J. Merker; A.G. Hendrickx, eds.
WiedBerlin, Ueberreuther Wissenschaft,
1988.
Mitchell, S.J.; Jones, S.M. Diagnosis of pregnancy in marmosets (Callithrix jucchus)
LABORATORY ANIMALS 9:49-56,1975.
Moore, H.D.M.; Gems, S.; Hearn, J.P. Early
implantation stages in the marmoset monkey (Callithrixjucchus). THE AMERICAN
JOURNAL OF ANATOMY 172:265-278,
1985.
Morgan, P.M.; Hutz, R.J.; Kraus, E.M.;
Cormie, J.A.; Bavister, B.D. Ultrasonographic assessment of the endometrium in
rhesus monkeys during the normal menstrual cycle. BIOLOGY OF REPRODUCTION 36~463-469,1987.
Nyland, T.G.; Hill, D.E.; Hendrickx, A.G.;
Farver, T.B.; McGahan, J.P.; Henrickson,
R.; Anderson, J.; Phillips, H.E. Ultrasonic
assessment of fetal growth in the nonhuman primate (Macucu muluttu). JOURNAL OF CLINICAL ULTRASOUND 12:
387-395,1984.
Peterson, E.N.; Hutchinson, D.L.; Sabbagha,
R.E.; Royal, J.S.; Levitt, M.J . Sonography
and amniocentesis as predictors of gestational age and fetal growth in the rhesus
monkey. AMERICAN JOURNAL OF OBSTETRICS AND GYNECOLOGY 1 1 4
883-889, 1972.
Phillips, I.R. Skeletal development in the
foetal and neonatal marmoset (Cullithrix
jucchus). LABORATORY ANIMALS 10:
317-333, 1976a.
Phillips, I.R. THE EMBRYOLOGY OF THE
COMMON MARMOSET (Callithriz jucC ~ U S ) .ADVANCES IN ANATOMY, EMBRYOLOGY AND CELL BIOLOGIE 52/5.
Springer Verlag, Berlin/Heidelberg/New
York, 1976b.
Phillips, I.R.; Grist, S.M. The use of transabdominal palpation to determine the course
of pregnancy in the marmoset (Callithrix
jucchus). JOURNAL OF REPRODUCTION AND FERTILITY 43:103-108,1975.
Sabbagha, R.E.; Turner, J.H.; Chez, R.A. Sonar biparietal diameter growth standards
in the rhesus monkey. AMERICAN JOURNAL OF OBSTETRICS AND GYNECOLOGY 121:371-374,1975.
Shimizu, K. Ultrasonic assessment of pregnancy and fetal development in three species of macaque monkeys. JOURNAL OF
MEDICAL PRIMATOLOGY 17:247-256,
1988.
Smith, C.A.; Moore, H.D.M.; Hearn, J.P. The
ultrastructure of early implantation in the
marmoset monkey (Cullithriz jacchus).
ANATOMY AND EMBRYOLOGY 175:
399-410, 1987.
Summers, P.M.; Taylor, C.T.; Miller, M.W.
Requirement of inner cell mass for efficient
chorionic gonadotrophin secretion by blastocysts of common marmosets (Callithrix
jacchus). JOURNAL OF REPRODUCTION AND FERTILITY 97:321-327,1993.
Tarantal, A.F. Sonographic assessment of
nongravid female macaques (Mucucu muluttu and Mucuca fasciculuris). JOURNAL
OF MEDICAL PRIMATOLOGY 21:308315,1992.
Tarantal, A.F.; Hendrickx, A.G. Use of ultrasound for early pregnancy detection in
the rhesus and cynomolgus macaque
(Mucaca mulatta and Macaca fuscicularis).
JOURNAL OF MEDICAL PRIMATOLOGY 17~105-112, 1988a.
Tarantal, A.F.; Hendrickx, A.G. Prenatal
growth in the cynomolgus and rhesus
macaque (Macaca fascicularis and Mucuca
mulatta): A comparison by ultrasonography. AMERICAN JOURNAL OF PRIMATOLOGY 151309-323, 198813.
Tarantal, A.F.; Hendrickx, A.G. The use of
ultrasonography for evaluating pregnancy
in macaques. Pp. 92-99 in NON HUMAN
PRIMATESDEVELOPMENTAL BIOLOGY AND TOXICOLOGY. D. Neubert;
H . J . Merker; A.G. Hendrickx, eds. Wied
Berlin, Ueberreuther Wissenschaft, 1 9 8 8 ~ .
Документ
Категория
Без категории
Просмотров
3
Размер файла
805 Кб
Теги
pregnancy, detection, growth, ultrasonography, marmoset, callithrix, monitoring, jacchus, times, patterns, monkey, real, fetal, uterine
1/--страниц
Пожаловаться на содержимое документа