Subido por Marco Antonio Aspron

1999 BOVINO REPRODUCCIÓN ULTRASONIDO

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Journal of Reproduction and Development, Vol. 45, No. 1, 1999
—Review—
Bovine Reproductive Ultrasonography: A Review
Abdullahi Y. RIBADU and Toshihiko NAKAO
Department of Veterinary Obstetrics and Gynecology, Rakuno Gakuen University,
582 Bunkyodai-Midorimachi, Ebetsu, Hokkaido 069-8501, Japan
Abstract. The advent of ultrasonography over a decade ago has contributed tremendously in the
field of bovine reproduction. Ultrasound imaging has shown that cattle exhibit 2 or 3 waves of
follicular development during an estrous cycle. Ultrasonography allows monitoring of individual
follicles as they grow and/or regress over time and patterns of follicular development can thus be
determined with relative precision. Other important applications of ultrasonography in bovine
reproduction includes; pregnancy diagnosis, fetal sex determination, folliculocenteses, diagnosis
of abnormalities of the reproductive organs, monitoring of treatment of ovarian cysts, monitoring
of postpartum genital resumption, ultrasound-guided centesis and male genital ultrasonography.
Recent applications of ultrasonography in bovine reproduction includes doppler ultrasonography
for genital blood flow and mammary ultrasonography. The use of ultrasonography is indispensable in most studies in which morphology (structure) and function are correlated. In this paper,
the literature pertaining to the use of ultrasonography in bovine reproduction is reviewed. The
applications and limitations of ultrasonography are highlighted. The non-invasive nature of
ultrasonography makes it an excellent clinical and research tool in bovine reproduction.
Key words: Bovine, Reproduction, Ultrasonography.
(J. Reprod. Dev. 45: 13–28, 1999)
he application of real-time B-mode ultrasonog-
T raphy to bovine reproduction has grown rapidly in the last decade. It is apparent that
ultrasonography has provided answers to a number of hitherto unanswered questions with regard
to bovine reproductive cycle and its concurrent disorders. One of the greatest advantages of
ultrasonography is that it is totally non-invasive
and so repeated examinations of an animal’s reproductive tract can be performed without
impairing its breeding potential or having adverse
effect on the conceptus. Real-time ultrasonic examination has allowed the monitoring of individual
follicles on a daily basis. It is now clearly established that the growth of follicles in bovine ovaries
occurs in a wave-like manner with two or three
Accepted for publication: September 14, 1998
Correspondence: A. Y.Ribadu
waves per estrous cycle.
Accurate early pregnancy detection can be
achieved easily and instantly through the use of
ultrasonography. Ultrasonographic fetometry allows the estimation of fetal age, assessment of
progression of fetal growth and diagnosis of pregnancy disorders. Furthermore, fetal sex can be
determined by ultrasonography.
The course of uterine involution (postpartum)
can be monitored by ultrasonography. Characteristics of uterine disorders (endometritis, pyometra,
hydrometra) have also been documented [1]. Ultrasonography has helped tremendously in the
diagnosis and differentiating the types of ovarian
cysts in cattle [2–5] and ovarian tumors [1]. The
use of ultrasonography in monitoring the response
to treatment of ovarian cysts in cattle has also been
reported [3, 6, 7].
Ultrasonically guided amnio- and allantocente-
RIBADU and NAKAO
14
ses in pregnant cows [8] and ultrasound guided
transvaginal folliculocentesis for in-vitro fertilization [9] and mammary ultrasonography [10, 11]
are other important applications of ultrasonography. The use of ultrasonography to help predict
observed oestrus in dairy cows after administration of prostaglandin has been reported recently
[12]. Currently, there is scanty of information on
the use of ultrasonography in bovine male reproduction. Ultrasonographic characteristics of bull
testes and accessory sex glands have been reported [13–15]. The potential for the use of
ultrasonography in bovine male reproduction is
enormous.
Although some review articles on bovine and
large animal ultrasonography have appeared previously [16, 17], the need to have an up-to-date
information on the rapidly growing field of bovine reproductive ultrasonography prompted this
review.
Principles of Ultrasonography
Ultrasound is defined as any sound frequency
above the the normal hearing range of the human
ear; i.e. greater than 20,000 Hz [18]. Detailed reviews of basic principles of transrectal
ultrasonography have been reported [18–21]. Briefly, ultrasonography utilizes high frequency sound
waves to produce cross sectional images of the tissues and internal organs. The sound waves are
produced by vibrations of specialized crystals (piezo-electrical crystals) housed in the ultrasound
transducer. Vibrations of the crystals are produced
by pulses of electric current. A proportion of sound
waves reflected back to the transducer is converted to electric current and displayed as an echo on
the ultrasound viewing screen. The transducer,
therefore, acts as both the sender and receiver of
echoes. The echoes are evident on the viewing
screen as varying shades of gray (black to white).
The absolute value of the acoustic impedance of
any tissue is relatively unimportant, because it is
the magnitude of the difference in acoustic impedance at tissue interface that determine the amount
of reflection of the beam [18].
Most ultrasound scanners used in bovine reproduction currently are B-mode (brightness modality)
real-time scanners. In B-mode ultrasonography,
the image is a two-dimensional display of dots (pix-
els), the brightness of the dots is proportional to
the amplitude of the reflected echoes returning to
the transducer. Real-time refers to the ability to
image movements (e.g. fetal heart beat or motion)
as it occurs. Dynamics of some reproductive structures or events (i.e. ovulation) could be studied by
video tape recordings of real-time ultrasound examinations.
Ultrasound scanners are equipped with transducers of varying frequencies. The most commonly
used frequencies in bovine reproduction are 3.5,
5.0 and 7.5 MHz. The higher the frequency of the
transmitted sound waves, the better the image resolution, but the shallower the depth of penetration
[2, 18]. There are two types of scanners; linear
array and sector. Linear array transducers have
piezo-electric crystals arranged in rows and as such
the image produced by linear array transducer appears rectangular. Sector transducers, on the other
hand, have only a few such crystals and the image
produced is pie-shaped corresponding to the field
of scan. Mechanical sector scanners offer multifrequency capability in a variety of scan head
design with 3.0, 5.0 and 7.5 MHz crystals in a single scan head. Because of the versatility of these
machines, they are also more expensive than linear-array systems [22]. Recent ultrasound scanners
have a wider frequency range and accept a full
line of single and dual frequency probes. Digital
image port for computer image storage is also available. Battery-powered portable ultrasound scanners
are also currently available.
Doppler ultrasonography which detects turbulence within blood vessels and direction of flow, is
also a useful diagnostic tool in bovine reproduction. The Doppler phenomenon is the change in
sound frequency of a moving object as perceived
by a stationary observer. Doppler ultrasound machines detect frequency change and, therefore,
movement which is converted to an audible signal
[23].
The major considerations in selecting an ultrasound scanner are price, resolution quality,
portability, serviceability and technical support
[24]. Other factors include memory capabilities,
remote control, transducer and cable design (I or
T), single or dual frequency probe and above all,
the use for which the machine would be put. For
routine bovine reproductive ultrasonography (early pregnancy diagnosis, pathology of the ovaries
and uterus, fetal sexing etc) a 5 MHz linear rectal
BOVINE REPRODUCTIVE ULTRASONOGRAPHY
transducer seem to be the most versatile and effective. However, a 7.5 MHz linear transducer is
recommended for follicular dynamics studies. For
transvaginal oocyte recoveries, a convex-linear
transducer gives better results.
Techniques
For transrectal or transcutaneous ultrasound
scanning in cattle, no sedation is indicated as the
procedure is totally non-invasive and well tolerated. Adequate restraint is however required and
the scanner should be placed at a sensible distance
from the cow/bull on the side opposite the operator‘s rectalling arm. All precautions that apply to
palpation per rectum are applicable to transrectal
scanning.
All feces from the rectum should be evacuated
prior to introduction of the transducer. It is often
advantageous to carry out a preliminary exploration of the topography of the reproductive tract
before commencing the ultrasonographic examination. The transducer face is lubricated with a
suitable coupling medium and is usually covered
by a lubricated plastic sleeve before insertion in a
cupped, lubricated hand through the anal opening. It is then progressed cranially along the rectal
floor to overlie the reproductive tract. The transducer face must be pressed firmly against the rectal
mucosa in order to effect ultrasound transmission
through the rectal wall into abdominal viscera. The
probe is moved across the reproductive tract in a
thorough and systemic manner [23, 25].
Basal requirements
To make an accurate diagnosis via an ultrasonographic examination, ambient lighting is
imperative. A darkroom is ideal for viewing the
monitor and helps the human eye recognize as
many shades of gray as possible. When examinations are carried out in lighted conditions, some
type of hood must be draped over the monitor to
facilitate effective gray-shade delineation [24].
Interposition of any contaminating feces will prevent ultrasound transmission and produce poor
imaging and artefactual interference. The ultrasound screen and the human eye should be at
similar level for accurate interpretation of ultrasound images.
Interpretation of ultrasound images
Interpretation of ultrasonographs of the repro-
15
ductive tract require a thorough understanding of
the composition of the images and an awareness
of the possible artifacts which can occur and lead
to a misdiagnosis. As sound waves pass through
the tissues and surrounding areas they may be
modified in a number of ways. Sound waves passing through body structures will encounter tissue
interfaces and the returning echoes will be of varying strengths and so produce a variety of images.
The ultrasonic characteristic of a tissue depends
on its ability to reflect sound waves. Liquids do
not reflect sound waves (i.e. are nonechogenic or
anechoic) and are represented on the viewing
screen as black. The ultrasonic images of liquidcontaining portions of structures such as ovarian
follicles, embryonic vesicles appear black. Dense
tissues (e.g. bone) reflect a large proportion of the
transmitted sound waves (i.e. echogenic) and is
represented on the viewing screen as light gray or
white. Various tissues and contents of the reproductive tract appear on the screen in varying shades
of gray depending upon their echogenicity [18].
Some common artifacts include; distant enhancement (occurs when the incident sound beam strikes
the far wall of a fluid-filled structure; e.g follicle,
embryonic vesicle), refraction artifacts, specular
reflection, reverberation artifacts, acoustic shadowing [23]. A detailed review of imaging artifacts in
diagnostic ultrasound has been published [26].
Ultrasonography of Normal Ovarian
Structures
Follicles
The ultrasonographic anatomy of the ovaries of
the cow has been described in detail [3, 27–29].
Antral follicles of various sizes appear as nonechogenic structures which could be distinguished
from blood vessels in cross-section by the elongated appearance of the latter [29, 30].
There was a linear relationship between follicle
diameter measured by in vivo ultrasonography and
follicle diameter determined after slaughter [31].
Correlation coefficients of 0.7–0.9 for various sizes
of follicular structures were recorded between in
vivo ultrasonography and postmortem slicing of
excised ovaries [31–35]. These studies showed that
transrectal ultrasonography is a reliable method
for identifying and measuring follicles in bovine
ovaries. In a recent study on ultrasound echotex-
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RIBADU and NAKAO
ture of follicles and functional and endocrine status in 32 heifers [36], it was shown that the
echotexture characteristics of the ultrasound images of the follicle antrum and wall (after
ovariectomy) were correlated with the functional
and endocrine status of a follicle. Mean pixel (picture element) values (grey scale: black=0;
white=255) for the follicle wall and stroma increased progressively from the growing to
regressing phases of the dominant follicle of the
first follicular wave. Pixel heterogeneity of the antrum and wall were negatively correlated with
estradiol and estradiol:progesterone ratio in follicular fluid.
Ovarian ultrasonography has shown that the
development of bovine follicles occurs in a distinct, striking regular pattern [37]. Each wave
consists of the contemporaneous emergence of a
group (cohort) of follicles 5 mm or more in diameter. Within several days, one follicle has grown
larger than the cohort and is considered dominant
[38–41]. Ultrasonography has revealed the existence of two [32, 42, 43] or three [40, 41] follicular
waves per estrous cycle in heifers.
Each dominant follicle has a growing phase and
a static phase; each lasting for about 5–6 days. The
dominant follicle of the first wave is anovulatory.
It remains dominant for 4–5 days, and generally
by day 11 or 12 of the estrous cycle, it loses its
dominance and begins to regress which lasts for
5–7 days. In the meantime, the second wave of
follicles has been recruited and selection of the second wave dominant follicle has occurred, this
dominant follicle goes on to ovulate. In a three
wave cycle, however, this second dominant follicle regresses, making way for yet another group of
follicles, with the third dominant follicle ovulating
[43, 44]. Analysis of follicular dynamics has shown
that dominant non-ovulatory follicles remain as the
largest follicle for several days after the start of the
succeeding wave, which implied that a dominant
follicle retains morphological dominance (largest
follicle on a pair of ovaries) longer than it retains
functional dominance (ability to suppress growth
of other follicles) [45].
Ultrasonography has been used to study ovarian response to superovulation in cattle [46–49]. The
influence of a dominant follicle on the superovulatory response has been reported in heifers and cows
[50–53]. The presence of a dominant follicle seem
to have a negative influence on superovulatory re-
sponse. Thus, assessment of follicular status prior
to initiation of a superovulatory treatment may be
an important consideration. Guilbault et al. [54]
have indicated that decreased superovulatory response and embryo recovery in FSH-primed heifers
may be due to the presence of higher numbers of
follicles 7–10 mm and >10 mm prior to the initiation of the superovulatory treatment which limited
recruitment of follicles 2–3 mm during the superovulatory treatment.
Follicular dynamics in heifers and cows during
early pregnancy were investigated [55–57]. A
wave-like pattern of growth and regression of large
follicles was observed through the first 60–70 days
of pregnancy in all the studies. It was concluded
that the follicular dynamics during the first 60–70
days of pregnancy were similar to those during
non pregnancy. Bergfelt et al. [58] have reported
that the continued periodic emergence of anovulatory follicular waves in pregnant heifers was
associated with continued production of progesterone as evidenced by the continued periodic
emergence of waves in non-bred progesteronetreated heifers.
Ovulation
Determination of ovulation by ultrasound examination was reported by Larrson [59]. The ovaries
of 8 heifers were examined by ultrasonography
every 4th hour during and after estrus. Ovulation
was depicted by the absence of a preovulatory follicle that was present at a previous examination
and subsequently confirmed by the development
of corpus luteum at the same spot. The usefulness
of ultrasonography performed at 2-hourly intervals for detecting the onset of ovulation was also
demonstrated [60].
Corpora lutea
The ultrasonic characteristics of corpora lutea
(CL) has been described [5, 28, 29, 61]. Generally,
a CL is identified ultrasonically from 3 days after
ovulation. A developing CL appears on the ultrasound image as a poorly defined, irregular,
greyish-black structure with echogenic spots all
within the ovary; a mid-cycle CL is a well defined
granular, greyish echogenic structure with a demarcation line visible between it and the ovarian
stroma; in a regressing CL the demarcation line is
faint, owing to the slight difference in echogenicity between the tissues [33]. Corpora lutea with
BOVINE REPRODUCTIVE ULTRASONOGRAPHY
cavities appear as a centrally located nonechogenic area surrounded by greyish echogenic luteal
structure. The size and shape of the cavities varies
according to the cyclic stages of the CL [2, 62, 63].
The presence or size of central fluid-filled cavity
affected neither the plasma progesterone secretion
nor subsequent reproductive performance [34].
These structures represent a normal variation of
CL in bovine.
Kähn and Ludlow [64] compared palpation per
rectum and transrectal ultrasonography (with a 5
MHz transducer) with ovarian dissection for identifying mid-cycle CL and obtained a sensitivity of
85% for both methods. Complete agreement was
reported between in-vivo ultrasonography and postmortem slicing of ovaries for identification of CL
and the presence of CL with cavities [61]. Pieterse
et al. [33] reported that the sensitivity and predictive value of palpation for detecting mid-cycle CL
were 83.3% and 73.2% and those of transvaginal
ultrasonography (with a 5 MHz transducer) were
80.6% and 85.3%, respectively. In another study,
Ribadu et al. [5] compared the evaluation of midcycle CL by palpation per rectum, ultrasonography
(with 7.5 MHz transducer) and plasma progesterone concentration and obtained a sensitivity,
specificity and positive predictive value of palpation as 85%, 95.7% and 89.7%, respectively.
Ultrasonography had a sensitivity of 95%, a specificity of 100% and a positive predictive value of
100%.
Quirk et al. [65] stated that decreases in the size
of the CL in heifers coincided with decreases in
the plasma concentrations of progesterone. Sprecher et al. [66] obtained a correlation coefficient of
0.68 between milk progesterone measured by radioimmunoassay and luteal diameter measured by
ultrasonography. Song-Chang et al. [67] also reported a significant correlation between CL size
(as determined by ultrasonography) and milk
progesterone concentration in 16 dairy cows. Kastelic et al. [68] concluded that an ultrasonographic
assessment of CL was a viable alternative to measurement of plasma progesterone concentration for
the evaluation of luteal function. It should be noted however, that even though a high correlation
exists between the CL diameter measured by ultrasound and plasma progesterone concentration
during most days of the estrous cycle; the correlation was absent during the last few days of the
estrous cycle when sharp decline of progesterone
17
concentration was not accompanied by a commensurate decrease in CL size as visualized by
ultrasonography [5, 69]. A similar trend was observed by Kamimura et al. [34] who reported that
the estimated volume of corpus luteum (by ultrasonography) and plasma progesterone
concentration in early postpartum cows increased
with similar profiles during the luteal growth but
decreased more slowly than the fall in plasma
progesterone level during luteal regression.
Ultrasonography of the Uterus during the
Estrous Cycle
The ultrasonic anatomy of the uterine horn has
been described [29, 32]. The ultrasound image of
the uterus showed a distinctly echogenic structure
with different layers of the uterine horn reflected
by differing echotextures. The echotexture of the
endometrium was characterized by the presence
of non-specular reflections with dark and bright
signals seen within the ultrasound image of the
endometrium.
The changes in the morphology of the uterus
during the estrous cycle has been characterized ultrasonically in 22 Holstein heifers monitored during
58 interovulatory intervals [70]. The ultrasonographic appearance of the uterus was influenced
by the stage of the estrous cycle. Uterine echotexture was characteristically dark during the follicular
phase (estrus) reflecting an extensive degree of edema of the endometrium. The uterine horns were
maximally curled during luteal dominance but
were less curled during follicular dominance.
Ultrasonographic Detection of Pregnancy
The early and accurate diagnosis of pregnancy
in cattle is essential for the maintenance of high
levels of reproductive efficiency. Chaffaux et al.
[71] first reported the use of real-time ultrasonography to diagnose pregnancy in cattle. Using a 3.5
MHz transducer, they observed irregularly shaped
nonechogenic structures in the lumen of the uterus from day 28 post-insemination. Later, several
authors [72–81] reported on the use of ultrasonography to diagnose pregnancy in cattle.
Pierson and Ginther [72] using a 5 MHz transducer, reported the presence of discrete
18
RIBADU and NAKAO
nonechogenic areas within the uterus at days 12
and 14. The changes in the ultrasonographic appearance of the bovine conceptus from time of first
detection of the embryo proper (day 20) to day 60
of pregnancy was reported [75]. The embryo was
seen initially as a small echogenic line on day 20.
By days 22 to 30, the embryo had a prominent Cshape. Boyd et al. [82], using a 7.5 MHz transducer
in 22 Friesian dairy cows reported that the conceptus was tentatively observed at day 13 within the
vesicle. The vesicle suddenly enlarged at day 19
and the heart beat was detected in the embryo at
day 22.
Tentative early pregnancy diagnosis (before detection of an embryo proper) was based on the
finding of discrete, nonechogenic structure or line
within the uterine lumen but must be subsequently confirmed by the progressive elongation of the
nonechogenic area and eventual detection of embryo proper. Definitive diagnosis was unreliable
before day 18 using a 5 MHz transducer [83] and
before day 16 using a 7.5 MHz transducer [84].
A wide variation in the levels of accuracy for
pregnancy diagnosis (70–100%) has been reported
by several authors [76, 77, 83, 85–88]. The level of
accuracy depends on factors like; the type of ultrasound equipment used (sector or linear), transducer
frequency (3.5, 5.0 or 7.5 MHz), stage of gestation
and the experience of the operator. Generally, a 5
MHz or 7.5 MHz transducer tends to provide more
reliable results than does a 3.0 MHz transducer for
early pregnancy diagnosis. However, the reliable
period of for pregnancy diagnosis with a positive
predictive value of over 95% varies between days
20 and 42 postbreeding [17].
The use of ultrasonography for pregnancy diagnosis has no detrimental effect on either the dam
or the fetus. In a recent study, Baxter and Ward
[80] showed that the use of ultrasound scanners
for early pregnancy diagnosis (at 30 to 40 days of
gestation) did not increase the rate of fetal loss.
The advantages of using ultrasonography for pregnancy diagnosis are that the presence of an embryo
can be detected earlier than by palpation per rectum and that direct physical manipulation of the
gravid reproductive tract is unnecessary with ultrasonography. Thus, the risk of inducing
embryonic mortality is greatly reduced [89].
Fetal Sex Determination by Ultrasonography
Fetal sex determination has several implications
in the animal breeding industry. The gender of
fetuses can be detected by visualization of the location of the genital tubercle [90] or the scrotum
and mammary glands [91]. The most appropriate
time of ultrasonographic sex determination is 55
to 60 days of gestation and the technique can be
accurate even under farm conditions [92].
In another study, Viana and Marx [93] used ultrasonography to determine the sex of bovine
fetuses between 60th -90th day of pregnancy in
716 embryo recipient cows and heifers. Verification tests on calves born revealed a correct
diagnosis of 96.3%. It was concluded that this technique offers a new tool for the management of cattle
industry. It should be emphasized however, that
ultrasonic identification of the genital tubercle or
the scrotum and mammary glands for sexing purposes requires considerable experience.
Ultrasonographic Fetometry
Although a cow’s calving date can be predicted
with reasonable precision from a knowledge of service date (whether AI or supervised natural
mating), it is however difficult when cows are run
together with a bull, mating is frequently not observed and the dates of service may be unknown.
Accurate estimate of calving dates could be a good
management tool as cows can be rationed more
precisely in late pregnancy to achieve the appropriate level of body condition at calving [94].
Management at calving could also be eased if cows
could be grouped according to their expected calving dates.
Estimation of fetal age, monitoring of fetal
growth across time and diagnosis of pregnancy disorders can be performed by ultrasonographic
fetometry. Growth curves of fetal structures based
on ultrasonographic fetometry have been reported
[95, 96]. Kähn [96] described in detail the sonographic fetometry of fetuses in 19 pregnant heifers.
A total of 485 examinations were carried out between 2 to 10 months of pregnancy. The organs
evaluated included eyeball, brain case, stomach,
trunk, ribs, metacarpal diaphysis, os ilium and os
ischii, scrotum and umbilical cord. For determina-
BOVINE REPRODUCTIVE ULTRASONOGRAPHY
tion of the size of organs, the transducer was manipulated so that the largest sonographic section
of the structure was obtained on the screen. Regression and correlation coefficients of fetal
structures were calculated depending on days of
gestation. It was concluded that intra-uterine development of the bovine fetus and its gestational
age may be judged from the size of its organs and
parts of the body.
Ultrasonographic fetometry has been shown to
provide a precise estimation of gestational age and
prediction of calving dates [94]. In a study of 300
pregnant beef cows between 35 and 125 days of
gestation, Wright et al. [94] reported the mean difference between the actual and predicted calving
dates as 0.9 ± 9.0 S.D (days). It was concluded that
the accuracy and precision of the prediction of calving date were sufficient to be of benefit in the
management of cows in late pregnancy and at calving.
19
by day 28–40 postpartum based on ultrasonographic assessment. The difference in the mean day of
completion of uterine involution may be attributed to differences in sample sizes, parity and level
of management.
Ultrasonographic evaluation of uterine involution in 11 Swedish cows with retained fetal
membranes [99] revealed accumulation of snowy
fluid and thickening of the endometrium and uterine walls in all cows. In a recent study, Torres et
al. [100] monitored uterine involution in 33 dairy
cows and reported that uterine involution was completed at 4 weeks postpartum in cows with normal
puerperium (n=12) but was delayed in 23.8% of
cows with abnormal puerperium (n=21).
These studies have demonstrated that ultrasonography is a useful tool in monitoring the
progress and completion of uterine involution.
Ultrasonographic Diagnosis of Ovarian and
Uterine Abnormalities
Ultrasonography of Postpartum Uterus
Serial ultrasonographic assessment of bovine
postpartum uterine involution has shown that total uterine diameter and endometrial thickness
decreased over time to reach a static size at completion of uterine involution.
Ultrasonographic evaluation of the diameter and
shape of the postpartum uterus, echotexture and
layers of the uterine wall and intraluminal fluid
accumulation has been reported in cows [97]. Uterine involution was completed at approximately 40
days based on ultrasonic assessment of uterine horn
diameters. Kamimura et al. [ 34] also monitored
the progress of uterine involution by twice-weekly
ultrasonography in 40 Holstein cows and reported
completion of uterine involution by 41.5 days postpartum.
Uterine involution in 15 Charolais cows were
monitored by Santos et al. [98] using an ultrasound
scanner at 3 day intervals from 8 to 40 days after
calving. For cows with a normal parturition, uterine involution was completed an average of 28.12
± 55 days after calving vs 32.75 ± 1.13 days for
cows with dystocia. There were highly significant
differences between cows with dystocia and those
calving normally in the time taken for involution
of the uterine horns. Taking the above studies
together, uterine involution seem to be completed
Ovarian cysts
Ovarian cysts is an important cause of infertility
in cattle. It is characterized by the presence of one
or more follicular structures larger than 25 mm in
diameter for 10 or more days in the absence of a
corpus luteum [101]. Ovarian cysts are either follicular (thin-walled) or luteal (thick-walled). The
difficulties of differentiating accurately between
follicular and luteal cysts by palpation per rectum
is well documented [102–106]. It is pertinent to
distinguish follicular cysts from luteal cysts accurately as the approach to treatment may differ
depending on the diagnosis. Ultrasonography provides a method of accurately differentiating the
types of cysts. The ultrasound appearance of follicular and luteal cysts have been documented [1,
3–5, 107–110]. By ultrasonography, a follicular cyst
appeared as a uniformly nonechogenic ovarian
structure >25 mm in diameter with a wall <3 mm
thick. Luteal cysts, on the other hand, appeared as
nonechogenic structure >25 mm in diameter with
grey patches within the antrum or along the inner
cyst wall and a wall thickness >3 mm. It is necessary to distinguish luteal cysts from cystic corpus
luteum as the latter is not pathological. For clear
differentiation between the two, various criteria
must be considered which include; overall size,
shape of the cavity, thickness of the luteinized wall
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RIBADU and NAKAO
and echogenicity of the interior area. Cystic corpora lutea are usually no larger than 3 cm in
diameter and the wall is about 5–10 mm thick.
Corpora lutea are rarely spherical usually presenting an oval shape on the screen. The image of the
cavities depend on direction of the ultrasound
beam and is either circular or oval. The fluidfilled cavities of CL only seldom present reflections
more often being homogeneous and near-black,
whereas reflections are frequently observed in
luteal cysts [1, 5].
Ultrasonography has proved to be useful in monitoring the dynamics of experimental ovarian cyst
formation following the administration of steroids
in heifers and cows [111–114]. Cyst turnover in
spontaneous occurring ovarian cysts in cows [115]
was also monitored.
The ultrasound appearance of ovarian tumor
have been reported [1, 116]. A compact, highly
echogenic image interrupted by nonechogenic
blood vessels was observed in a cow with granulosa cell tumor [1].
Ovarian cysts after treatment
Prior to the introduction of ultrasonography, assessment of luteinization of follicular cysts
following therapy was performed by palpation per
rectum. However, incorrect assessment of luteinization of follicular cysts by palpation per rectum
after treatment has been a problem [117, 118]. Ultrasonography is an effective tool for monitoring
the response of cystic ovaries to therapy. Edmondson et al. [3] first reported the use of ultrasound to
monitor the response of cystic ovaries following
treatment. In a cow treated with gonadotropic releasing hormone, the cyst wall increased in
thickness from 2 mm to 6 mm over a two week
period.
In a study on the use of ultrasound and progesterone profile to monitor the response of ovarian
follicular cysts in 5 cows treated with gonadotropic releasing hormone, Ribadu et al. [6] have
observed ultrasound changes after treatment which
included; clouding of the uniformly nonechogenic
antrum of cysts, luteinization of cysts wall, reduction in cyst size (resolution) and/or development
of 1–4 corpora lutea on the ovary bearing the cyst
or on the contralateral ovary. Multiple ovulation
occasionally occur following GnRH therapy of ovarian follicular cysts.
Treatment of cows with ovarian cysts (follicular
or luteal) with progesterone releasing intravaginal
device (PRID) or gonadotropic releasing hormone
(GnRH) did not seem to have any immediate effect on either follicular or luteal cysts, but
consistently resulted in estrus and ovulation; with
subsequent CL formation as monitored by ultrasonography. Treatment of luteal cysts with
prostaglandin caused marked decreases in cyst size
with rough echotexture of the luteinized rim of
the cyst within 2–4 days and the formation of new
CL within 1 week after treatment [7]. Ohnami et
al. [119] also monitored the response of ovarian
cysts in 9 cows treated with GnRH analogue. Ultrasonography detected doughnut-like luteal
structures after treatment which would not have
been detected by palpation per rectum alone. Subsequent hormone measurement confirmed the
luteal structures were fully functional.
Jou et al. [120] monitored the ovarian response
in cows with follicular cysts treated with GnRH
followed by prostaglandin 10–12 days later (n=15)
and saline followed by prostaglandin 10–12 days
later (control; n=17) and reported no significant
difference in the time from treatment to detection
of the first CL or cyst disappearance in the 2 groups.
Although the success rates following GnRH therapy of ovarian cysts varied amongst the various
studies quoted above, the visualization by ultrasonography of cyst luteinization and, or the
presence of CL in cows after treatment showed
that in responding cases evidence of therapeutic
success could be confirmed quickly [6]. Ultrasonography is thus, a useful tool for monitoring the
response of ovarian cysts to treatment.
Uterine abnormalities
The usefulness of ultrasonography in diagnosing pathological conditions of the uterus has been
reported [1, 121]. Uterine abnormalities recognised during ultrasonography included endometritis,
pyometra, fetal maceration and fetal mummification. Ultrasonographic appearance of inflammatory
conditions of the uterus were characterized by distended lumen filled to varying degrees with
partially echogenic, diffuse, flaky reflections. The
degree of echogenicity depended on the consistency of the fluid. When the uterine content was very
thick and full of leucocytes and tissue debris; the
echogenicity resembled that of uterine wall [1]. In
fetal maceration, the fetal bones were identified as
echogenic structures in the uterine lumen suspend-
BOVINE REPRODUCTIVE ULTRASONOGRAPHY
ed in nonechogenic fetal fluids with a thickened
uterine wall. Fetal mummification, on the other
hand, appeared as poorly defined mass (fetal mummy) with complete absence of uterine fluids.
These studies have indicated that, ultrasonography is an effective tool for diagnosing and studying
uterine abnormalities in cows.
Although the use of ultrasonography in diagnosis of hydrometra in sheep and goats have been
fairly documented [122–125], there is scanty information on its application in bovine.
Ultrasonography may be helpful in diagnosis of
hydrometra and mucometra in cattle.
Ultrasonographic Folliculocentesis
Ultrasound-guided transvaginal oocyte aspiration is helpful in obtaining ova from clinically
infertile, but valuable cows for in-vitro fertilization.
In this way, the genetic potential of such donor
cows could be propagated.
Pieterse et al. [9] described a technique for the
repeated collection of bovine oocytes using transvaginal ultrasound guided aspiration during the
normal estrous cycle and after stimulation with
PMSG in 10 cows. A total of 36 transvaginal procedures were performed during which 54 oocytes
were recovered from 197 follicles.
Moyo and Dobson [126] using a 7.5 MHz linear
array ultrasound transducer collected oocytes from
5 cows superovulated with ovine follicle stimulating hormone (oFSH). From 124 follicles punctured,
oocyte recovery rate of 48% was recorded. In another study [127], an oocyte recovery rate of 50–70%
has been reported in cows.
In a study on the development of oocytes derived from the first dominant follicles of beef cows,
Otoi et al. [128] monitored follicle development in
26 Japanese black beef cows by daily ultrasonography from day of estrus (day 0) until the first
dominant follicle was aspirated. It was observed
that the percentage of oocytes from first dominant
follicles that developed to blastocysts tended to
decrease with increasing follicular diameter and
estrous cycle days. Also, recovery of oocytes by
transvaginal ultrasound-guided follicle aspiration
once or twice a week for up to 12 weeks in heifers
did not affect subsequent response to superovulation and embryo recovery or the occurrence of
estrus[129]. Ooe et al. [130] showed that ultra-
21
sound-guided transvaginal oocyte aspiration can
be performed repeatedly and safely at different
phases of the estrous cycle and stages of gestation
in pregnant cows.
In addition to collection of oocytes for in vitro
fertilization, ultrasound guided folliculocentesis
also allows the collection of follicular fluid for hormonal studies [131].
Ultrasound Guided Amnio- and
Allantocentesis
Amniocentesis is the collection of fetal amniotic
fluid. The interactions between the fetus and the
dam may be studied through the technique of amnio and allantocentesis. Specific objectives of
amniocentesis includes; correlation of changes in
biochemical constituents with gestational age, early determination of fetal sex by cytological analysis
and as a source of fetal cells for the determination
of prenatal transgenesis.
Transvaginal ultrasound guided amnio and allantocentesis has been reported in 7 Dutch Friesian
cows [8]. The pregnant uterus was rectally positioned against the puncture needle which was
mounted on the intravaginally inserted ultrasound
transducer (sector). It was shown that amniotic
and allantoic fluid could be obtained in most ultrasound guided attempts and one fetus was
carried to term even after repeated (weekly) amnio and allantocenteses. The risks of fetal deaths
resulting from repeated punctures of the pregnant uterus (due to excessive manipulation and
bacterial contamination) in a large percentage of
animals limits the application of this procedure in
routine pregnancy evaluation. However, collection of fetal amniotic fluid using ultrasound-guided
transvaginal technique seem to be promising. In a
recent study, Garcia and Salaheddine [132] have
described the technical aspects of a safe and reliable ultrasound-guided transvaginal method of
amniotic fluid collection from heifers (n=93) with
day 79 to 90 bovine conceptuses using a very fine
aspiration needle. Collection of amniotic fluid samples was successful in 88 out of 93 (94.6%) attempts,
and no complications of pregnancy losses were recorded as consequence of the procedure.
RIBADU and NAKAO
22
Mammary Ultrasonography
Ultrasonography has important applications in
the bovine mammary glands. Ultrasound studies
have characterized not only the normal ultrasonographic appearance of the mammary glands and
teats but also some pathologic lesions of the mammary glands.
Cartee et al. [10] examined the udders and teats
of 4 cows (in-vitro in a water bath) and 3 live cows
and found no difference in the ultrasonographic
appearance of the mammary glands. Teats appeared as hypoechoic structures with anechoic
lumens while the papillary ducts appeared as a
thin anechoic area within folds of the inner teat
layer. Ultrasonography detected the presence of a
hypoechoic mass in a cow that was examined because of obstructed milk flow from a quarter.
In a further study [11], ultrasonic tomography
was applied to evaluate the teat morphology and
its use in preventing bovine mastitis.
Ultrasonography of the Male Reproductive
System
The establishment of normal ultrasonic parameters for testicular dimensions and characterization
of normal ultrasonic appearance are necessary to
allow studies on degenerative and pathological
conditions of the bovine testicle. Transcutaneous
ultrasonic imaging has been used to characterize
the ultrasonic morphology of the testicles of the
bull [13, 14]. The normal bull testicle was reported
as being homogeneous and moderately echogenic.
The head and tail of the epididymis were easily
identified on all testes, but the epididymal body
and ductus (vas) deferens were difficult to identify. Ultrasonic measurement of testicles was
correlated with testicular circumference, weight
and volume but not with scrotal circumference
[133]. Ultrasonic scanning of the bovine testicle
was found to have no detrimental effect on reproductive capacity (semen characteristics, testicular
dimensions and consistency) after exposure to a 3min scan with a 5.0 MHz transducer [134].
Recently, Bailey et al. [135] compared the reliability of caliper and ultrasonographic
measurements of testicular length and width invivo in 10 bulls. The data demonstrated the
reliability of using caliper and ultrasonographic
imaging for measurements of testicular length and
width. However, calipers were easier to use and
demonstrated a higher degree of accuracy for measurement of testicular length. It was concluded
that ultrasonography offers no added advantage
over that of calipers for measuring the length of
the in-vivo testicles except when only a width measurement is desired.
The ultrasonic anatomy of the accessory sex
glands of the bull has been described [15]. Transrectal ultrasonography was used to measure the
vesicular glands, ampullae and bulbourethral
glands. Ultrasonic measurements were found to
be repeatable in individual bulls over time and it
was concluded that the anatomic relationships and
organ dimensions were accurately imaged by ultrasonography.
Ultrasonography revealed testicular lesions in 95
bulls following in vitro injection of testes with crystalline, metallic or aqueous solutions [136].
Mickelson et al. [137] described the characteristic
ultrasonographic changes in a bull with seminal
vesiculitis. The changes observed included; increased glandular size, loss of normal lobular
structure, increased glandular volume and the presence of bright fibrous tissue within the hyperechoic
glandular parenchyma. Anderson et al. [138] used
doppler ultrasonography and positive contrast cavernosography to evaluate a persistent penile
hematoma in a bull. A wide scope exists for the
use of ultrasonography in male reproduction.
Conclusions
The use of ultrasonography has allowed accurate monitoring of ovarian follicular development
in heifers and postpartum cows on a daily basis in
a non-invasive manner. This has contributed immensely to the understanding of follicular
dynamics during the estrous cycle, early gestation
and the postpartum period. In the areas of pregnancy diagnosis, fetal sex determination,
folliculocenteses, amnio and allantocentesis, reproductive tract pathology, monitoring of normal and
abnormal postpartum interval, diagnosis and evaluation of treatment of ovarian cysts, mammary
ultrasonography, male reproduction; ultrasonography has proved to be a useful clinical and
research tool. Ultrasonography is quite helpful for
BOVINE REPRODUCTIVE ULTRASONOGRAPHY
individuals who are inexperienced in palpation per
rectum as palpation skills are acquired quickly
while at the same time making accurate diagnosis
via ultrasonography.
One of the greatest constraints limiting the widespread use of ultrasonography in bovine
reproduction is the high cost of the ultrasound machine. It is hoped that with the availability of
several types of scanners (from different manufacturers) and improvements in the quality of
scanners, the price may be affordable to a large
number of veterinarians and research scientists and
this will enhance its application in clinical as well
as research studies of bovine reproduction.
It must be emphasized that the use of ultrasonog-
23
raphy requires some skills. Such skills are usually
obtained during university training or through attendance at continuous professional development
(CPD) courses organized for such purposes. Furthermore, experience can be gained through the
use of the ultrasound scanner repeatedly.
Acknowledgements
The authors wish to express their appreciation
to Japan Society for the Promotion of Science (JSPS)
for the award of a Postdoctoral Fellowship (for foreign researchers) to A.Y. Ribadu.
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