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Eur J Wildl Res (2006) 52: 23–27
DOI 10.1007/s10344-005-0012-4
REVIEW
Thomas B. Hildebrandt
.
Frank Göritz
.
Robert Hermes
Ultrasonography: an important tool in captive breeding
management in elephants and rhinoceroses
Received: 15 August 2005 / Accepted: 25 August 2005 / Published online: 18 November 2005
# Springer-Verlag 2005
Abstract Nearly two decades ago, modern wildlife
medicine started to gradually use the advantages of the
non-invasive ultrasonography, which was already well es-
tablished in human and classical veterinary medicine. For
more than one decade now, the application of imaging
ultrasound for reproductive assessments and as a support-
ive tool during assisted reproduction procedures such as
artificial insemination (AI) in elephants and rhinoceroses
has dramatically improved the breeding success in captive
breeding programmes. The opportunity for identifying poten-
tial breeding candidates on the basis of their reproductive
health status is widely used for natural mating or for AI,
today. The longitudinal sonographic monitoring of patho-
logical processes on the internal female genital tract
allowed the identification of pathogenetic causes for the
rapid infertility development in older nulliparous females.
The factors causing temporary infertility in captive male
elephants and rhinoceroses were also identified by the use
of ultrasound. Today, ultrasonography is the golden stan-
dard for reproductive assessments in megavertebrates such
as elephants and rhinoceroses in captive management set-
tings and also in the wild.
Keywords Proboscidea
.
Rhinoceroses
.
Reproduction
.
Ultrasound
.
Breeding evaluation
Introduction
Over the last few decades, the elephants and rhinoceros-
es have become important icons in the saga of wildlife
conservation. Recent surveys estimate the wild Asian
(Elephas maximus) and African (Loxodonta africana) ele-
phant populations to be, at most, 50,250 and 637,600
individuals, respectively. The population estimates for the
five rhinoceros species with 3,610 black (Diceros bicornis),
11,330 white (Ceratotherium simum), 2,400 Indian (Rhinoc-
er os unicornis), 300 Sumatran (Dicero rh inus Sumatr ensis)
and 60 Javan (Rhinocer os sondaicus) are of even greater
concern.
The development and broad application of reproductive
assessment and artificial insemination (AI) techniques have
become critical to the successful breeding management of
elephants and rhinoceroses and are the top priorities of the
captive conservation programmes. Significant advances in
endocrine analyses, ultrasonographic evaluations and be-
havioural profiling have resulted in a number of remarkable
discoveries about reproductive biology in these megaverte-
brates that have led to major breakthroughs in assisted
reproduction. The development of reproductive assessment
techniques such as ultrasonography now allows zoo man-
agers to identify candidates for breeding by natural means or
by AI. These recent advances have sharpened the focus of
elephant and rhinoceros propagations and are already sig-
nificant in their impact on management and conservation.
Ultrasonography is mainly a reflection imaging tech-
nique in contrast to radiography as a transmission imaging
technique or magnetic resonance imaging (MRI) as an
emission imaging technique. Diagnostic ultrasound (2.0 to
50.0 MHz) produces a cross-sectional anatomical picture
(sonogram) of how sound waves reflect, refract and are
absorbed by different tissues. The more advanced 3D ul-
trasonography based on computerized summation of single
sonograms is generated by special volume transducers or
specific software programmes. Ultrasonography is gener-
ally non-invasive, except for the applications listed in
Fig. 1. Ultrasonic energy waves themselves can cause min-
imal bioeffects like mild tissue warming especially if colour
flow Doppler mode is used for extended periods of time
(>30 min). However, there has been no report of patient
injury or ultrasound-induced discomfort when examina-
tions were performed under the international ultrasound
safety guidelines. The necessity for animal handling and,
potentially, sedation may add invasive components to the
application of ultrasonography in non-domestic species.
The first attempt to utilize non-imaging ultrasound for a
practical application was used in an unsuccessful search for
T. B. Hildebrandt (*)
.
F. Göritz
.
R. Hermes
Institute for Zoo and Wildlife Research,
Alfred-Kowalke-Straβe 17,
10315 Berlin, Germany
e-mail: hildebrand@izw-berlin.de
the sunken “Titanic” in the North Atlantic in 1912. Ul-
trasound was routinely applied in the 1940s in World War
II, as a non-imaging Doppler technique for military pur-
poses (Sound Navigation and Ranging, SONAR). The first
medical application of ultrasonographic techniques was
developed for soft tissue characterization in humans in the
1950s (Donald et al. 1958). Subsequently, there has been a
dramatic development of imaging ultrasound, which has
been used in a wide range of applications in many fields of
human and veterinary medicine (DuBolay and Wilson
1988). This image modality allows non-surgical, transcu-
taneous and transrectal approaches for explorating of to-
pography and monitoring of biological and diagnosing of
pathological processes in humans and animals.
In 1991, Adams et al. described the first use of ultra-
sonography in rhinoceroses and elephants. Special acces-
sories and protocols were developed over the next few
years to increase the efficacy of ultrasound in these mega-
vertebrates (Hildebrandt et al. 2000a). Since 1993, the
Institute for Zoo and Wildlife (IZW) research team has
performed more than 3,000 individual ultrasound exam-
inations in approximately 400 elephants and more than 150
reproductive assessments in more than 70 rhinoceroses
under different management settings and in the wild.
In megavertebrates, the application is mainly limited to
transcutaneous and transrectal ultrasound. However, the
use of ultrasonography offers new opportunities in these
species to evaluate parts of internal organ systems and
joints which are inaccessible by other means (e.g. con-
ventional/digital radiography, magnetic resonance, endo/
arthroscopy) due to the enormous size and the location and
dimension of the organs. Additionally, in contrast to other
imaging procedures, clinical ultrasonography has several
advantages: (1) it is safe due to minimal bioeffects and
therefore repeatable; (2) it provides real-time information;
(3) it generates high-resolution characterization of soft
tissue and bone surface as well as morphometrics of
organs, implants or other foreign bodies; (4) it produces
sectional images and 3D reconstructions of tissues and
organ structures; (5) it permits examining motion and di-
rection (heartbeat, vascular flow, fetal movement); (6) it
operates economically efficient; (7) it facilitates document-
ing and preserving data on storable media; and (8) it is
portable and compatible with zoo and field conditions.
In general, only approximately 15% of all ultrasound
applications in elephants are performed transcutaneously
compared to 85% transrectal applications. In rhinoceroses,
the transcutaneous approach is limited to only 5% of the
applications such as monitoring of mammary gland de-
velopment in pregnant rhinoceroses. The cause for this
difference in utilization of these two application forms in
these pachyderms is due to the anatomy of the integu-
ment and the restricted penetration depth of commercially
available systems (max. average depth=220 mm). Trans-
cutaneous approach is predominantly used for obstetrics
(late-term pregnancy), orthopedics, cardiology, dentistry,
ophthalmology and for the visualization of cranial abdom-
inal organs and mammary gland development and function.
Transrectal examinations already stated above require a
higher level of patient preparation and specific customized
ultrasound accessories to overcome the anatomical obsta-
cles of the adult elephant. Nevertheless, transrectal ultra-
sound is an ideal tool for imaging the urogenital system,
rectal wall, intestinal loops, peritoneal–abdominal cavity,
and early to mid-term pregnancies (Fig. 2). Furthermore,
the transrectal approach has the added advantage of
improved coupling with the rectal wall, which allows for
the use of a variety of transducers with different fre-
quencies ranging from 2.0 to 10.0 MHz compared to
transcutaneous ultrasound that can only be performed with
a low-frequency probe (e.g. 4–2 MHz) (Hildebrandt et al.
1997). Therefore, more diagnostic information is available
from the detailed imaging generated by transrectal ultra-
sound. For this specific application, the commercial ul-
trasound system has been modified to incorporate special
features, including probe and cable extensions and a mon-
itor helmet with video glasses.
Reproductive disorders are the main obstacle for suc-
cessful captive management plans (Hermes et al. 2004;
transabdominal
transcorneal
transpalpebral
intercostal
transcutaneous
ultrasonography
SURFACE
transrectal
transintestinal
transduodenal
transcloacal
intranasal
transoesophageal
intrapharyngeal
intrabronchial
non-invasive
endosonography
transurethral
intrauterine
INSIDE
intravasal
intracardial
intraabdominal
invasive
endosonography
intravasal
intracardial
intraabdominal
invasive
endosonography
intrasalpingenous
transvaginal
Fig. 1 Overview of the ultra-
sound applications in mammals.
Some approaches are not prac-
ticable for megavertebrates like
elephants and rhinoceroses
Fig. 2 Transrectal 3D-sonogram (7–5 MHz) of a 168-day-old
elephant fetus. The 3D-mode allows the visualization of the fetal eye
(EY), trunk (TR), front and hind legs (LE), as well as part of the
placenta (PL) and the uterus (UT). Bar=20 mm
24
Hildebrandt et al. 2005). So far, none of the captive
elephant and rhinoceros propagation programmes reached
the level of being self-sustaining (Hermes at el. 2004;
Olson and Wiese 2000; Wiese 2000; Wiese and Willis
2004). The consequence is that imports from the range
countries are necessary for the zoo populations. In general,
reproductive pathologies in female elephants and rhi-
noceroses mainly involve changes in the internal genital
organs, primarily uterine tumours (leiomyomas), endome-
trial cysts and ovarian cysts (Fig. 3). There is a higher
incidence of genital tract leiomyomas in Asian compared to
African species, whereas ovarian cysts occur frequently in
African but rarely in Asian species (Hildebrandt and Göritz
1995, 1999; Hildebrandt et al. 2000b, 2003a; Montali et al.
1997; Hermes et al. 2001). Cystic endometrial degenera-
tion has been found in all species (Agnew et al. 2004;
Hildebrandt et al. 1997). These pathologies in an advanced
stage affect reproduction dramatically. Ovarian cysts have
been associated with acyclicity in elephants and rhinoc-
eroses (Brown et al. 1999;Hermesetal.2004;Hermesetal.
2005b). It is now known that the incidence of these
reproductive disorders increases with age and is greater in
nulliparous than in similarly aged parous individuals
(Hermes et al. 2004; Hildebrandt et al. 2000b). An ad-
ditional reproductive disorder complex in elephants is the
high percentage of more than 50% dystocia cases in older
primiparous cows (>20 years old) resulting in stillborn
calves and in about 5% of the cases in the death of the cow
due to retained conceptus and intoxication (Hildebrandt et
al. 2003b; Lange at el. 1999;Schaftenaar1996). The use of
ultrasonography during a dystocia treatment can optimize
the medical intervention and therefore helps save the life of
the cow (Schaftenaar et al. 2001). These findings suggest
that breeding elephants and rhinoceroses at a young age
(before onset of pathogenesis) should be a high priority, and
that females should be assessed periodically by ultrasound
and longitudinal hormonal analyses (usually progesterone)
to assess reproductive fitness.
Male elephant infertility appears to be related to poor
semen quality and low libido rather than any specific ana-
tomical abnormality. To date, evaluating circulating tes-
tosterone has been a non-informative index for diagnosing
gonadal dysfunction. Rather, ultrasonography remains the
most reliable method of assessing breeding potential in bull
elephants. Transrectal ultrasound assessments combined
with manual semen collection (Hildebrandt et al. 2000c;
Schmitt and Hildebrandt 1998) were performed in more
than 100 bull elephants. In that process, the morphology
and functionality of the entire urogenital tract have been
characterized, including testes and accessory sex organs as
well as the sperm parameters (Hildebrandt et al. 1998,
2000c, 2003a). Most bulls were non-breeders even those
exposed to females. Percentage of reproductive tract pathol-
ogies detected by ultrasound was low (14%), however,
even in older animals. In contrast, semen quality varied
markedly, and sperm motility often was less than 50%. In-
terestingly, more than half of the ‘ infertile’ bulls appeared
to be in social situations where they were subordinate to
older cows or other bulls. Thus, although many of these
bulls could serve as semen donors, they inconsistently
produce good quality ejaculates that could have resulted
from physiological disorder(s), behavioural problems or
perhaps suboptimal semen collection methods. Regardless,
periodic ultrasound examinations combined with semen
collection have been recommended as routine management
tools to monitor the reproductive value of bull elephants.
Despite profound differences in social systems of el-
ephants and rhinoceroses, unsuitable social environments
have similar impact on reproductive performance of male
rhinoceroses showing long-term detrimental effects on
fertility and resulting in 50% of the male captive population
being subfertile or infertile (Seror et al. 2002; Hermes et
al. 2005a). Ultrasonography of the accessory sex glands
combined with semen collections by using electro-ejacu-
lation in white rhinoceroses documented that semen quality
is associated with group size and social rank (Hermes et al.
2005a). Reproductive ageing processes and tumour devel-
Fig. 3 Transrectal sonogram (4–2 MHz) of an ovary (OV)
containing an ovarian cyst (CY). The cyst can be clearly distinguished
from a follicular structure by the presence of a prominent wall (WA).
Ovarian cysts are often combined with acyclicity in adult elephants.
The rectal wall (RE) appears as a moderately echoic strip at the top
of the sonogram. Bar=20 mm
Fig. 4 Transcutaneous sonogram (4–2 MHz) generated through the
inguinal skin (SK) of the cigar-shaped testis (TE) in an approx. 40-
year-old white rhinoceros bull affected by a medium-sized seminoma
and fibrosis (FI) in the testicular parenchyma. The malignant tumour
(TU) appeared hypoechoic and had a spherical structure. Bar=20 mm
25
opment in the genital tract play only a minor role in male
rhinoceroses. In the Indian and the white rhinoceros, pro-
gressive changes in testicular morphology attributable to
ageing occur in males older than 15 years of age.
Different from the females, this ageing process does not
overtly affect functional reproductive parameters as older
males prove to be the best semen donors despite con-
siderable testicular fibrosis (Endo et al. 1996; Hermes et al.
2005a). In contrast to frequent neoplastic processes in the
female genital tract, testicular tumours in a male rhinoceros
are rare findings (Fig. 4). The establishment of a social
hierarchy and low-grade fighting may involve sustained
testicular trauma. The subsequent exposure of spermatozoa
and seminal fluid to the surrounding testicular tissue induce
seminoma development (Portas et al. 2005). Despite
seminomas fast-growing character, the fertilizing potential
of affected males may remain high until in the advanced
stage of tumour growth.
Conclusions
This short review has endeavoured to provide credible
applications of the value of ultrasonography as a practical
diagnostic tool in elephants and rhinoceroses. The technol-
ogy still is vastly underutilized, and its many advantages
(non-invasiveness, reproducible real-time images, cross-
sectional images of tissues/organs and ability to measure
morphometry) certainly argue for more widespread use. In
the field of embryology alone, real-time ultrasonography
expands our ability to study embryonic development, uter-
ine and ovarian function in ways that are impossible using
conventional techniques.
Applying ultrasound to the systematic examination will
undoubtedly help find new solutions to current physiological
problems. But it will also promote the technology and
provoke the design of new and more specialized, species-
specific instruments. Continued miniaturization of complete
high-end ultrasound systems and development of probes
with compact, contoured shapes will improve the imaging
possibilities and increase the amount of diagnostic informa-
tion extractable from ultrasonography. Many new systems
offer colour flow imaging that allows direct evaluation of
blood vessel architecture in reproductive organs. This is a
promising area of research, providing insight into the marked
changes related to seasonality, maturation, sexual activity
and pregnancy or tumour development. 3D ultrasonography
also will further expand our ability to characterize repro-
ductive soundness while facilitating a better understanding
of complex physiological processes and creating near life-
like images.
A high priority is to incorporate this technology into
more comprehensive, integrated investigations involving
multiple scientific disciplines. Successful collaborations al-
ready exist, especially collaborations amongst ultraso-
nography specialists, endocrinologists and behaviourists.
Such scholarly partnerships will create new databases, help-
ing to develop mitigating treatments for overcoming repro-
ductive failure. It is the hope of the authors that more
scientists and zoo veterinarians will accept the challenge of
conducting integrated studies that cross-discipline for the
pleasure of pure scientific discovery as well as for developing
practical solutions to managing elephant and rhinoceros
species. Ultimately, our goal is to understand the reproduc-
tion biology and physiology of these megavertebrates in the
hopes of improving management to establish or maintain
self-sustaining populations, both in situ and ex situ.
Acknowledgements The authors dedicate this article to Professor
Christian Pitra for his upcoming 65th birthday in 2006. The new field
of reproduction management including the development of assisted
reproduction technologies for non-domestic species was originally
inspired and started by Christian Pitra at the Institute for Zoo and
Wildlife Research before his heart discovered evolutionary genetics.
T. B. H. would like to thank personally my former teacher and mentor
for his ideas and support which had an important impact on my own
professional career.
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