Cystic Endometrial Hyperplasia and Pyometra in Three

Captive African Hunting Dogs (Lycaon pictus)

Author(s): Gwen Jankowski, D.V.M., Michael J. Adkesson, D.V.M., Dipl.
A.C.Z.M., Jennifer N. Langan, D.V.M., Dipl. A.C.Z.M., Samantha Haskins,
D.V.M., and Jamie Landolfi, D.V.M., Dipl. A.C.V.P.
Source: Journal of Zoo and Wildlife Medicine, 43(1):95-100. 2012.
Published By: American Association of Zoo Veterinarians
DOI: http://dx.doi.org/10.1638/2010-0222.1
URL: http://www.bioone.org/doi/full/10.1638/2010-0222.1

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 Journal of Zoo and Wildlife Medicine 43(1): 95–100, 2012
Copyright 2012 by American Association of Zoo Veterinarians

CYSTIC ENDOMETRIAL HYPERPLASIA AND PYOMETRA IN

THREE CAPTIVE AFRICAN HUNTING DOGS (LYCAON PICTUS)

Gwen Jankowski, D.V.M., Michael J. Adkesson, D.V.M., Dipl. A.C.Z.M., Jennifer N. Langan, D.V.M.,
Dipl. A.C.Z.M., Samantha Haskins, D.V.M., and Jamie Landolfi, D.V.M., Dipl. A.C.V.P.

Abstract: Pyometra and cystic endometrial hyperplasia are common in domestic canids and are suspected to
develop as a consequence of elevated progesterone levels. Reports of uterine pathology in exotic canids are
limited, with some speculating of association with contraception. This report describes pyometra, cystic
endometrial hyperplasia, and ovariohysterectomy in three African hunting dogs (Lycaon pictus). Ovarian corpora
lutea were detected in two of the dogs, suggesting endogenous progesterone production. One dog had a uterine
adenocarcinoma and two had ovarian granulosa cell tumors. Clinical signs included anorexia, lethargy, vulvar
discharge, polyuria, polydipsia, and abdominal distention. Diagnosis was based on clinical signs, physical
examination, bloodwork, radiography, and ultrasonography, with confirmation through histopathologic
evaluation of tissues. Cystic endometrial hyperplasia, pyometra, and uterine neoplasia have rarely been diagnosed
in exotic canids; however, they should be considered as differential diagnoses in intact bitches that present with
suspected reproductive disease.
Key words: Adenocarcinoma, African hunting dog, contraception, cystic endometrial hyperplasia, granulosa
cell tumor, Lycaon pictus, pyometra.

INTRODUCTION signs of shock.3 CEH and pyometra have been

reported in large felids and some canids in
Cystic endometrial hyperplasia (CEH) and
association with synthetic progestins such as
pyometra are often reported in domestic dogs.
melengesterol acetate (MGA) contraception.1,6,8
In dogs, CEH is the most common uterine cystic
disorder associated with pyometra.13 CEH fre- New evidence suggests CEH may occur with
quently occurs at times of chronic circulating high some frequency in exotic felids without exoge-
progesterone concentrations that predispose the nous progesterone sources.5 Progestins stimulate
uterus to ascending infection from overgrowth of growth of the uterine lining of felids and canids
normal vaginal bacterial flora, resulting in pyo- and can result in hyperplasia, pyometra, neopla-
metra. Although medical management of pyome- sia, or a combination.7 However, not all domestic
tra has been reported previously, ovariohy- canids with CEH have elevated progesterone
sterectomy (OHE) is considered the treatment of levels.3 The case series, of three African hunting
choice.3 dogs (Lycaon pictus; AHDs) from one institution,
Clinical signs of pyometra generally consist of demonstrates that cystic endometrial hyperplasia
lethargy, anorexia, vaginal discharge, and dehy- and subsequent pyometra is a clinically relevant
dration, conditions that may be seen in conjunc- medical condition in exotic canids, even in
tion with leukocytosis characterized by a left shift. patients that have not been treated with MGA.
Severe cases may result in sepsis and associated
CASE REPORTS

From the Chicago Zoological and Aquatic Animal Case 1

Residency Program, University of Illinois, College of
A multiparous, 10-yr-old female AHD present-
Veterinary Medicine, Urbana, Illinois 61802, USA
(Jankowski); Chicago Zoological Society, Brookfield ed for decreased appetite and mild lethargy of 2-
Zoo, 3300 Golf Road, Brookfield, Illinois 60513, USA wk duration. The dog had been treated with
(Adkesson, Langan); University of Illinois, College of leuprolide acetate (Lupront, TAP Pharmaceuti-
Veterinary Medicine, 1008 West Hazelwood Drive, cals Inc., Deerfield, Illinois 60015, USA; 2.5 mg
Urbana, Illinois 61802, USA (Langan, Haskins); and i.m., every 28 days for the preceding 4 yr) as a
Zoological Pathology Program, University of Illinois, contraceptive agent. Physical examination and
LUMC, 2160 South First Avenue, Maywood, Illinois
radiographic findings were consistent with a
60153, USA (Landolfi). Present address (Jankowski):
Chicago Zoological Society, Brookfield Zoo, 3300 Golf distended uterus. A leukocytosis (25.1 3 103
Road, Brookfield, Illinois 60513, USA. Correspondence cells/ll; reference range, 6.5–12.7 3 103 cells/ll)4
should be directed to Dr. Jankowski (gwen.jankowski@ characterized by 6% band neutrophils was pre-
gmail.com). sent. A clinical diagnosis of pyometra was made,

95
96 JOURNAL OF ZOO AND WILDLIFE MEDICINE

and treatment with OHE was chosen. The next tra, or neoplastic metastasis was apparent on
day, OHE revealed a dilated uterus filled with radiographs, ultrasonography, or bloodwork.
purulent exudate, with multiple omental adhe- However, 3 mo later the animal was lethargic,
sions. Multiple uterine perforations resulted in with abdominal distention. Tachycardia, muffled
diffuse peritonitis. The adhered omentum was heart sounds, respiratory arrhythmia, and de-
ligated using 2-0 gut and was removed from creased lung sounds on the right were identified.
uterine serosal surfaces. Engorged uterine vessels A mild neutrophilic leukocytosis (13.7 3 103 cells/
were ligated individually and the uterine body ll; reference range, 6.5–12.7 3 103 cells/ll)4 with
using standard surgical techniques for OHE. The 1% bands was detected. Moderate bilateral pleu-
abdomen was flushed with 2 L of sterile saline ral effusion with right lung collapse and diffuse
before closure of the body wall in a continuous fluid opacity in the abdomen were evident on
pattern using 0 PDS (Ethicon Inc., Somerville, radiographs. Thoracocentesis revealed a bilateral
New Jersey 08876, USA). The subcutaneous cream-colored, purulent effusion. The abdomen
tissue and skin were closed using 2-0 Maxon was distended, and a marked fluid wave was
(United States Surgical Corp., Norwalk, Connect- palpated, but no masses were identified on
icut 06850, USA) in a continuous and cruciate ultrasonographic examination. Abdominocente-
pattern, respectively. The dog was treated with sis revealed an exudate with a large population of
amoxicillin (Pfizer Animal Health, Exton, Penn- neoplastic cells. The dog was euthanized due to
sylvania 19341, USA; 20 mg/kg i.m., b.i.d. for 5 the grave prognosis. Postmortem examination
days) and ceftazidime (GlaxoSmithKline, Re- revealed a mammary carcinoma with multicentric
search Triangle Park, North Carolina 27709, metastases and neoplastic pleural and peritoneal
USA; 28 mg/kg i.m., t.i.d. for 5 days) followed effusions. Further postmortem lesions were mild
by amoxicillin clavulanate (Clavamox, Pfizer or chronic age-related changes, or a combination,
Animal Health; 12 mg/kg p.o., b.i.d. for 20 days). of negligible clinical significance. Endometrium
Appropriate analgesia was provided postopera- of the uterine stump had mild cystic endometrial
tively. Cultures of the abdomen, uterus, and blood hyperplasia similar to that noted in the resected
isolated two strains of Escherichia coli susceptible uterus. No evidence of local or distant uterine
to amoxicillin clavulanate. neoplasia was evident at the time of necropsy.
Histologically, the uterine lumen was filled with
accumulations of neutrophils, macrophages, mu- Case 2
cus, and necrotic cellular debris. Endometrial A multiparous, 11-yr-old female AHD present-
glands were diffusely elongated with occasional ed for recheck after treatment for bacterial
branching (hyperplasia) and often markedly ec- hepatitis. The animal had been contracepted with
tatic and filled with mucus and neutrophils. The leuprolide acetate (TAP Pharmaceuticals Inc., 2.5
surrounding endometrial stroma was edematous mg i.m., every 28 days for 1 yr) at 8 yr old. On
and contained moderate to large numbers of examination, a vaginal discharge was identified,
neutrophils, plasma cells, lymphocytes, and mac- along with a leukocytosis (25.2 3 103 cells/ll;
rophages. Multifocally, inflammation extended reference range, 6.5–12.7 3 103 cells/ll)4 charac-
through the myometrium and serosa and into the terized by a mature neutrophilia (23.18 3 103
mesometrium. Serosal surfaces were covered by cells/ll; reference range, 4.9–10.3 3 103 cells/
small adherent accumulations of fibrin and neu- ll),4 leading to a clinical diagnosis of pyometra.
trophils, and there was segmental mesothelial Large populations of neutrophils and Gram-
hyperplasia. Effacing portions of the endometri- negative rods were present in the vaginal fluid.
um and underlying myometrium was a nonencap- Culture confirmed three biotypes of Pseudomonas
sulated, poorly demarcated, and infiltrative mass spp. Based on culture and sensitivity results, the
of neoplastic epithelial cells consistent with animal was placed on enrofloxacin (Baytril, Bayer
uterine adenocarcinoma. Elsewhere, a focal stro- HealthCare LLC, Animal Health Division, Shaw-
mal polyp was present in the endometrium. No nee Mission, Kansas 66201, USA; 5.3 mg/kg p.o.,
bacteria were detected in routinely or Gram- for 14 days) and after 5 days the vaginal discharge
stained sections. Four large corpora lutea were had resolved.
present in the right ovary, and both ovaries Three months later, the bitch presented with
contained granulosa cell tumors without evidence acute onset of lethargy, anorexia, and mild
of thecal involvement. diarrhea. The dog was considered to be obese
The animal was examined twice in the following (4/5 body condition score) with mild muscle
month. No evidence of peritonitis, stump pyome- wasting dorsally and a pendulous abdomen.
 JANKOWSKI ET AL.—PYOMETRA IN THREE AFRICAN HUNTING DOGS 97

Physical examination revealed a turgid uterus ll).4 A fluid wave and firm dorsal tubular mass,
with irregular surfaces and mucoid vaginal dis- presumed to be uterus, were present on abdom-
charge. Bloodwork was similar to the previous inal palpation. A lipoma was present on the right
presentation. Uterine enlargement was confirmed lateral thorax and a 1-cm-diameter, raised, firm
radiographically, and an OHE was performed mass was present on the ventral abdomen imme-
using the same approach as Case 1. Both uterine diately caudal to the thorax. Cytologic evaluation
horns were enlarged, fluid filled, and cystic in of a mucopurulent vaginal discharge revealed
appearance, although overt evidence of peritonitis Gram-negative rods that were confirmed by
was not present. Cultures taken from the uterus culture to be E. coli. The uterine horns were fluid
were positive for E. coli. Based on culture and filled and loculated. Abdominocentesis revealed a
sensitivity results, the dog was treated with blood-tinged milky exudate characterized by se-
ceftiofur sodium (Naxcel, Pfizer Animal Health; vere neutrophilia and intracellular Gram-negative
3.1 mg/kg i.m., s.i.d. for 5 days) and analgesics. rods. Pyometra with secondary septic peritonitis
One week later, the dog’s clinical signs had was diagnosed, and OHE with peritoneal lavage
resolved and bloodwork results had returned to was performed. Multiple sites of uterine rupture
normal. and adhesion of the surrounding omentum were
Histologically, the uterus had similar cystic present. The abdomen was lavaged with 5 L of
endometrial hyperplasia and pyometra as noted sterile saline and infused with 1 g of ceftazidime
in Case 1. In some areas of the uterus, inflamma- (GlaxoSmithKline) in 150 ml of sterile saline.
tion extended through the myometrium to the Ceftazidime (22 mg/kg i.v.) was administered
uterine serosa and mesometrium. One ovary during the procedure. The dog was weak and
contained follicular, tubo-ovarian, and subsurface disoriented for approximately 48 hr postopera-
epithelial cysts. The other ovary also contained tively. The animal was hospitalized and treated
subsurface epithelial cysts in addition to a small with enrofloxacin (Baytril, Bayer HealthCare
granulosa cell tumor without evidence of thecal LLC.; 10 mg/kg i.m., s.i.d.) and analgesics for 3
involvement. days. It was anesthetized 72 hr post-operatively
The dog developed progressive, degenerative for re-evaluation, supportive care, fine needle
joint disease of the coxofemoral joints and was aspiration of the ventral dermal abdominal mass,
euthanized 1.5 yr post-OHE. Severe degenerative and transport from the hospital to normal holding
polyarthritis, other chronic age-related changes, facilities. Enrofloxacin (10 mg/kg p.o., s.i.d.) and
and multiple apocrine gland carcinomas were anti-inflammatory drugs were administered orally
noted postmortem. No histopathologic abnor- for 14 and 7 days, respectively.
malities of the mammary or remaining uterine Histologic examination revealed uterine cystic
tissue were identified. endometrial hyperplasia and pyometra similar to
Cases 1 and 2. Both ovaries contained multiple
Case 3 large corpora lutea. Fine needle aspirate of the
A multiparous, 9-yr-old female AHD presented subcutaneous ventral abdominal mass was inter-
for acute anorexia, lethargy, and a hunched preted as a mammary carcinoma. Mass resection
appearance. Previously, one dose of leuprolide and radiographic evaluation for metastases were
acetate (Lupron, TAP Pharmaceuticals Inc.; 2.5 performed 2 wk after the dog’s initial presentation
mg/kg i.m.) followed by two 9.4-mg deslorelin for pyometra. The animal was treated with long-
implants (Suprelorin, Peptech Animal Health, acting ceftiofur crystalline-free acid (Excede,
Macquarie Park, New South Wales 2113, Aus- Pfizer Animal Health; 7 mg/kg s.c.) and anti-
tralia) for contraception placed annually for the 2 inflammatory drugs. The dog’s appetite gradually
yr immediately preceding presentation. Intermit- increased, and it progressively gained weight over
tent anorexia and vomiting had occurred over the the next 2 mo. The excised mass was mammary
previous 3 mo, but they resolved spontaneously 1 carcinoma and examined margins were free of
mo before presentation at the same time breeding neoplastic cells suggesting excision was complete.
activity was observed. At presentation, the animal Examination of the dog 2 mo later revealed no
was observed straining in lateral recumbency. clinical abnormalities or evidence of metastasis.
Bloodwork was within normal limits with the
DISCUSSION
exception of a mild leukocytosis (14.4 3 10^3 cells/
lL; reference range, 6.5–12.7 3 103 cells/ll)4 Presenting signs and results of diagnostic
characterized by a mature neutrophilia (12.67 3 testing for pyometra in AHD were consistent
103 cells/ll; reference range, 4.9–10.3 3 103 cells/ with reported signs of pyometra in domestic dogs.
98 JOURNAL OF ZOO AND WILDLIFE MEDICINE

The most commonly reported signs in domestic consist of low to high doses of estrogens, increase
dogs are anorexia, lethargy, vulvar discharge, and the risk of pyometra by approximately 6%.15
abdominal distention.3 A fluid-distended uterus Progesterones are suggested to directly stimulate
visible on radiographic or ultrasonographic ex- hyperplasia of the endometrium and uterine
amination is strongly suggestive of pyometra.3,12 secretions, providing optimal conditions for bac-
Hyperproteinemia, hyperglobulinemia, and leu- terial growth. Exogenous progestins cause histo-
kocytosis characterized by a left shift are the most logic changes in the endometrial lining similar to
common bloodwork changes present in domestic CEH and especially are seen with use of MGA
dogs.3 Hyperproteinemia and hyperglobulinemia and medroxyprogesterone.10 Progestin treatments
are presumed to result from chronic antigenic have been shown to increase risk of pyometra in
stimulation, but they were not present in the exotic felids and domestic dogs.8,10 Synthetic
AHD, which may result from exhaustion or progestins have more potent effects than endog-
inadequate production of inflammatory globulins. enous progesterone because they clear more
The leukocytic profile of Cases 1 and 2 was slowly and have a higher affinity for the recep-
similar to those of most domestic dogs (severe tors.6 The frequency of CEH and pyometra also
leukocytosis and neutrophilia 6 a left shift). The increase with age and decreased parity.8,10
youngest female (Case 3) presented with a very All three AHD were multiparous dams that had
mild leukocytosis and neutrophilia without a left not been treated with progestins but had been
shift, which may result from the lack of appropri- treated for a period of ,5 yr with gonadotropin-
ate inflammatory response or the result of a releasing hormone (GnRH) agonists (deslorelin
profound neutrophilic response in the uterus implants, leuprolide acetate injections, or both).
and abdomen resulting in early leukocytosis The dogs developed CEH and pyometra within 1–
followed by depletion. As many as 25% of 5 yr of GnRH treatment. GnRH agonists do not
pyometra cases in domestic dogs may present potentiate progestins, but before suppressing
with normal leukograms.14 Blood profiles may not estrus they may have a stimulatory effect, causing
reflect the level of pathologic change and should a short spike in sexual hormone production
be interpreted in conjunction with clinical signs during one ovulatory cycle. Although corpora
and other exam findings. Escherichia coli was lutea were present in Cases 1 and 3, progesterone
isolated from all three cases and is the most assays run on frozen, banked serum were rela-
common isolate from uterine cultures in domestic tively low (2–3 ng) in each case. The brevity with
dogs with pyometra. An antibiotic-resistant Pseu- which the animals were treated with GnRH
domonas spp. was cultured from Case 2; Pseudo- agonists and the delayed onset of clinical signs
monas spp. and fecal pathogens are not after contraceptive treatment in Cases 1 and 2
uncommon in cases of pyometra.10 There are suggests it is less likely that contraception played
instances when OHE may not be immediately a significant role in the development of CEH and
selected for the treatment of a pyometra (e.g., pyometra in these AHD; however, the low levels
valuable breeding animals, compromised patients of serum progesterone and lack of exogenous
that are poor surgical candidates). Medical man- progesterone sources suggest other predisposing
agement may be attempted in such situations, as factors may have played an important role. Some
with Case 2, where initial management consisted studies have indicated that an exaggerated re-
of antibiotic therapy based on culture and sensi- sponse to progesterone, even in low levels, may
tivity results. Additional therapies intended to result in similar risks as sustained high levels of
decrease progesterone-associated effects also progesterone.14 Efforts including vaginal epitheli-
would be appropriate; in domestic dogs, prosta- al cytology and progesterone assays to identify
glandins, dopamine agonists (e.g., cabergoline and during which stage of the reproductive cycle each
bromocriptine), or antiprogesterones (e.g., agle- dog presented, may have been helpful in identify-
pristone) may be of benefit.14 ing potential etiologies or risk factors.
Both exogenous progestins and estrogens have Up to 50% of dogs with ovarian granulosa cell
been implicated as predisposing factors for the tumors develop CEH.3,12 The granulosa cell
development of pyometra in canids and felids.10 tumors and the presence of corpora lutea in Cases
Estrogens are suggested to potentiate the effects 1 and 2 may have potentiated the development of
of progesterone on the endometrium and relax the CEH and pyometra. Cases 1 and 2 were both
cervix, allowing bacteria to enter the uterus. In greater than 9 yr old, and old age is a recognized
domestic dogs, abortogenic treatments such as risk factor for development of CEH in domestic
estradiol-cypionate or diethylstilbestrol, which dogs.3,12
 JANKOWSKI ET AL.—PYOMETRA IN THREE AFRICAN HUNTING DOGS 99

Although pyometra and CEH have been thor- when treating cases of pyometra. Despite the low
oughly documented in exotic felids5,7,8 and domes- rate of metastasis, biopsy of surrounding tissues
tic dogs,3,10 both have been reported infrequently and adjacent lymph nodes in conjunction with
in exotic canids. In a survey of necropsy results in diagnostic imaging of other organs may be
the captive red wolf (Canis rufus), CEH was valuable when evaluating AHD with pyometra.
present in 2 of 19 female wolves, one of which Further investigation is needed to determine the
progressed to pyometra.1 Pyometra and CEH incidence of reproductive lesions in exotic canids.
were reported in a maned wolf (Chrysocyon
brachyurus) along with a granulosa cell tumor of Acknowledgments: We thank the animal care
the ovary.9 A review of reproductive lesions in and veterinary staff at the Chicago Zoological
exotic canids conducted by the Association of Society/Brookfield Zoo (Chicago, Illinois, USA).
Zoos & Aquariums’ (AZA) Wildlife Contracep-
tion Center Health Surveillance Program found LITERATURE CITED
that endometrial hyperplasia (53%), hydrometra
1. Acton, A. E., L. Munson, and W. T. Waddell.
(33%), and adenomyosis (25%) were the most
2000. Survey of necropsy results in captive red wolves
frequently observed lesions.6 Endometrial hyper-
(Canis rufus), 1992–1996. J. Zoo Wildl. Med. 31: 2–8.
plasia was present in 40% and pyometra in 10% of 2. Chun, R., and L. Garrett. 2005. Urogenital and
canids never treated with MGA.6 All eight AHD mammary gland tumors. In: Ettinger, S. J., and E. C.
in the AZA study had endometrial hyperplasia; Feldman (eds.). Textbook of Veterinary Internal Med-
six were graded as advanced or severe and five icine: Diseases of the Dog and Cat, 6th ed. W. B.
were treated with MGA.6 Five of the six severe Saunders Co., Philadelphia, Pennsylvania. Pp. 784–
cases had been treated with MGA.6 The propor- 795.
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canid species, although the difference was not hyperplasia/pyometra complex and infertility in female
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Textbook of Veterinary Internal Medicine: Diseases of
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England. 2001. Cystic endometrial hyperplasia/pyo-
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progesterones, specifically MGA, but the impact J. Reprod. Fertil. Suppl. 57: 395–406.
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