Abstract

Transrectal ultrasonography was performed on 10 male and 85 female African elephants (Loxodonta africana) and on 5 male and 39 female Asian elephants (Elephas maximus) in order to develop standards for assessment of reproductive health and status.

Captive and wild African males and females as well as captive Asian males and females were examined. The entire internal urogenital tract was visualized ultrasonographically by using a 3.5-MHz, a 7.5-MHz and a 10.0-MHz transducer in combination with two probe extensions specially adapted for elephant anatomy. The findings were verified by postmortem ex situ ultrasound examinations in each species. Each part of the internal urogenital tract was sonographically detectable except for main parts of the late gravid uterus (>13 mo p.c.) in females and the bulbo-urethral glands and the cranial portion of the ureters (in both sexes) and ductus deferentes in males. A variety of pathological alterations were found, but mostly in the captive population of African and Asian elephants. There was a very high incidence of uterine leiomyomas in the female genital tract of captive Asian elephants (35.9%). In contrast, wild and captive African elephants never develop leiomyomas but frequently have endometrial cysts (11.3% wild, 14.3% captive) and ovarian cysts (1.4% wild, 21.4% captive). This study presents results which indicate that transrectal ultrasonography may be used as an effective nonsurgical tool for reproductive and health assessment of elephants, which has implications for management, population control and assisted reproduction.

Introduction

Reproduction in African elephants (Loxodonta africana) and Asian elephants (Elephas maximus) is often less successful than in natural populations, inhibiting the establishment of self-sustaining captive populations.^3,11 Infertility due to reproductive disorders and mismanagement can have a devastating effect on captive breeding programs.^5,8 There is a dearth of knowledge regarding the reproductive anatomy and physiology of these both species.^2,3,6,12,14 Sonographic imaging techniques have had a beneficial impact on reproductive and veterinary studies in a wide range of domestic¹³ and wild species;^4,8 however, the feasibility of this technique as a routine diagnostic procedure in elephants has not been overly successful¹.  Some of the difficulties in viewing intra-abdominal testes, ovaries and monitoring fetal development were attributed to difficulties in positioning the instruments, and to the size and demeanor of these large pachyderms. Major anatomical obstacles during routine andrological, gynecological and obstetrical ultrasonography include locating components of the reproductive tract that in elephants lie deeply within the abdominal cavity, and the marked inclination of the axis of the proboscid pelvic inlet.¹⁵ Recently, the instrumentation for transrectal sonographic examinations in elephants has been greatly improved to overcome these obstacles.^7,9

Methods

Transrectal ultrasonography was performed on 10 male and 85 female African elephants and on 5 male (including 1 castrated individual) and 39 female Asian elephants to develop standards for assessment of reproductive health and status. This study included 5 wild male and 71 female African elephants from the Kruger National Park, Skukuza, South Africa, as well as captive African and Asian elephants kept in 19 different facilities with a variety of management systems. The age of the individuals ranged from 7–62 yr. The majority of the 139 elephants examined were in the reproductive age. The number of ultrasonographic examination/individual ranged from 1–62. However, most elephants had only one examination.

Ultrasonography was performed either in the nontranquilized captive African and Asian elephants in standing position (often chain- or chute-restraint) or in the immobilized wild African elephants (M99®, etorphine 10.0 to 15.0 mg, IM, Reckett & Coleman, Hull, UK; reversed by M50-M50^®, diprenorphine 30.0 mg, IV, Reckett & Coleman, Hull, UK), which were in lateral recumbency. Both positions were satisfactory for using the transrectal approach. After manual removal of the feces and extensive irrigation in combination with the application of ultrasound gel (Aquasonic 100®, Parker Laboratories Inc., Orange, NJ 07050 USA), the transducer was inserted into the rectum and directed carefully over the reproductive tract. The internal urogenital tract was visualized ultrasonographically by using a real-time, B-mode ultrasound scanning system (CS 9100 Oculus, Picker International GmbH, Espelkamp, D-32339, Germany ), equipped with either a 3.5-MHz, 7.5-MHz, or a 10.0-MHz transducer in combination with two different probe extensions adapted for elephant anatomy (Ultraschallkopftraeger II and III, A. Schnorrenberg Chirurgiemechanik, Woltersdorf, D-15569, Germany). These adapters were an essential part of our equipment that allowed good contact between the transducer and the rectal mucosa and could be extended to the cranial segment of the reproductive tract to view the kidneys, testes or ovaries. In addition to the main ultrasound monitor, we adapted a small monitor to a helmet that was worn by the examiner for orientation of the ultrasonogram during the procedure. Measurements were taken from the reproductive structures using the electronic caliper provided on the ultrasound unit. Actual scanning time was 15–25 min for each individual. The findings were verified by postmortem ex situ ultrasound examinations on the isolated urogenital organs in each species (63 African elephants and 6 Asian elephants).

Results

Each part of the internal urogenital tract was sonographically detectable, except for main parts of the late gravid uterus (>13 mo p.c.) in females and the bulbo-urethral glands and the cranial portion of the ureters (in both sexes) and ductus deferentes in males (Table 1). The use of all three ultrasound transducers in combination with the two adapters was necessary to get optimal information about the urogenital organs. The quality of the ultrasonographic images of each probe was evaluated on the basis of the following criteria: overview, detail, and surface of the organ examined (Table 1). This knowledge concerning the appearance of healthy genital structures was necessary for clear recognition of pathological alterations. Ultrasonography was used to detect the following pathological alterations listed in Table 2.

Table 1. Comparison of the efficiency of three transducers in the ultrasonographic imaging of elephant urogenital tracts

*= this type of transducer did not fit in an adapter
+++ = excellent
++ = good
+= insufficient
-= impossible

Table 2. Pathological findings detected by transrectal ultrasonography in wild and captive elephants

*= in comparison to the normal age-related development
** = caused by a surgical castration
( ) = brackets contain total number of individuals investigated

Discussion

Assessment of the reproductive capacity of an individual is based on the health of the internal genital tract. It is therefore important to detect pathological alterations of the inner genital tract and to determine the importance or influence they may have on reproductive performance before forming breeding groups.⁸

Generally, exotic animals show signs of diseases or disorders very late in their progression. Sonographic examination of the urogenital organs may provide useful criteria to appraise the fitness or breeding potential of an individual. Detection of subclinical changes in these organs indicates that a clinically apparent metabolic disorder may occur under the physiological burden of breeding activity and pregnancy, which could have possible lethal consequences for mother and/or fetus.

There was a very high incidence of uterine leiomyomas in the female genital tract of captive Asian elephants (35.9%). In contrast, wild and captive African elephants never develop leiomyomas, but frequently have endometrial cysts (11.3% wild, 14.3% captive) and ovarian cysts (1.4% wild, 21.4% captive). These findings correlated with a postmortem study between 1975 and 1995 of approximately 30,000 exotic mammal cases at the Institute for Zoo Biology and Wildlife Research Berlin, and the Smithsonian Institution, Washington DC, in which leiomyomas were found in the uterus, cervix, and vagina in 14 species of exotic mammals. These animals originated from the Smithsonian's National Zoological Park (NZP) and from multiple zoos in Europe. This study indicated a very high necropsy prevalence of genital tract leiomyomas in Asian elephants as compared to other species.¹⁰

Findings regarding the general health of the animal and those specific to the genital tract should be considered in order to make appropriate decisions regarding which animals to breed.^4,8 This study presents results that indicate that transrectal ultrasonography may be used as an effective nonsurgical tool for reproductive and health assessment of elephants, which has implications for management, population control and assisted reproduction.

Acknowledgments

The authors are grateful for assistance from the staffs at the following institutions: Circus Frankello; Circus Sarrasani; Circus Scholl; Dickerson Park Zoo; Fort Worth Zoo; Indianapolis Zoo; Knoxville Zoo; Kruger National Park Board; National Zoological Park; Pittsburgh Zoo; private zoo (Virginia); Ringling Bros. and Barnum & Bailey Circus; St. Louis Zoo; Tierpark Carl Hagenbeck, Hamburg; Woodland Park Zoo; Zoo Wroclaw; Zoological Garden, Berlin; Zoological Garden, Münster; Zoological Garden, Erfurt; Zoo Zürich.

Financial support was provided in part by the Institute for Zoo Biology and Wildlife Research, Berlin and the Smithsonian Institution Short Term Visitor Program. The work on the wild African elephants was supported by a grant of the Society for Technical Collaboration, Germany.

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