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Diagnosis and treatment of urolithiasis in client-owned chelonians: 40 cases

(1987-2012)

Article  in  Journal of the American Veterinary Medical Association · September 2015

DOI: 10.2460/javma.247.6.650 · Source: PubMed

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 Diagnosis and treatment of urolithiasis
SMALL ANIMALS/

in client-owned chelonians:
EXOTIC

40 cases (1987–2012)
Krista A. Keller, DVM; Michelle G. Hawkins, VMD; E. P. Scott Weber III, VMD, MSc; Annette L. Ruby, BA;
David Sanchez-Migallon Guzman, LV, MS; Jodi L. Westropp, DVM, PhD

Objective—To calculate the prevalence of urolithiasis in client-owned chelonians examined

at a veterinary teaching hospital and to describe the clinical signs, diagnosis, and treatment
of urolithiasis in chelonians.
Design—Retrospective case series.
Animals—40 client-owned turtles and tortoises with urolithiasis.
Procedures—The medical record database of a veterinary teaching hospital was searched
from 1987 through 2012 for records of client-owned chelonians with urolithiasis. The preva-
lence of urolithiasis was calculated for client-owned chelonians examined at the hospital.
Signalment and physical examination, hematologic, biochemical, urinalysis, diagnostic im-
aging, treatment, and necropsy results were described.
Results—The mean prevalence of urolithiasis in client-owned chelonians for the study pe-
riod was 5.1 cases/100 client-owned chelonians examined. Thirty-one of the 40 chelonians
were desert tortoises. Only 5 of 40 chelonians had physical examination abnormalities as-
sociated with the urogenital tract. Surgery was performed on 17 chelonians; 5 developed
postoperative complications, and 4 of those died. Necropsy was performed on 18 cheloni-
ans, and urolithiasis contributed to the decision to euthanize or was the cause of death for
9. Uroliths from 13 chelonians were analyzed, and all were composed of 100% urate.
Conclusions and Clinical Relevance—Results indicated chelonians with urolithiasis have
various clinical signs and physical examination findings that may or may not be associated
with the urinary tract. Hematologic, biochemical, and urinalysis findings were nonspecific
for diagnosis of urolithiasis. Many chelonians died or were euthanized as a consequence
of urolithiasis, which suggested the disease should be identified early and appropriately
treated. (J Am Vet Med Assoc 2015;247:650–658)

A lthough urolithiasis is a common problem in cheloni-

ans, most of the scientific literature on the subject is
limited to case reports or case series in chelonians1–5 and
other reptile species.6–9 In reptiles, clinical signs associated
with urolithiasis include hyporexia, reduced fecal out-
put, straining to urinate or defecate, reduced mentation,
weight loss, and swelling of the hind limbs.1–10 Methods
described for treatment of urolithiasis in chelonians in-
clude cloacoscopy-assisted cloacolith removal, cystotomy
via plastronotomy, manual removal of cystoliths from the
bladder with long forceps, and cystotomy or bladder mar-
supialization by a prefemoral approach.1,2,4,10–12,a
In chelonians, most uroliths are composed of
urate,2,4,11,13,14 and 62 of 66 (93.9%) uroliths obtained
From the William R. Pritchard Veterinary Medical Teaching Hospi-
tal (Keller), Department of Medicine and Epidemiology (Hawkins,
Weber, Guzman, Westropp), and G. V. Ling Urinary Stone Analysis
Laboratory (Ruby, Westropp), School of Veterinary Medicine, Uni-
versity of California-Davis, Davis, CA 95616. Dr. Weber’s present
address is American Association for the Advancement of Science,
1200 New York Ave NW, Washington, DC 20005. Dr. Keller’s pres-
ent address is University Hills Animal Hospital, 4175 E Warren Ave,
Denver, CO 80222.
Presented as a poster at the 44th Annual American Association of Zoo
Veterinarians Conference, Oakland, Calif, October 2012.
Address correspondence to Dr. Hawkins (mghawkins@ucdavis.edu).
AST
ABBREVIATIONS
Aspartate aminotransferase
CK Creatine kinase
from tortoises and 7 of 12 uroliths obtained from tur-
tles that were analyzed at a large veterinary urolith cen-
ter were composed of urate.15 Urate calculi have also
been reported in many other species such as dogs,16,17
cats,18,19 Eurasian otters (Lutra lutra),20 North American
river otters (Lontra canadiensis),21 a northern elephant
seal (Mirounga angustirostris),22 a California sea lion
(Zalophus californicus),22 bottlenose dolphins (Tursiops
truncatus),23,24 and a blue-fronted Amazon parrot (Ama-
zona aestiva).25 In chelonians, the pathophysiology of
urate urolithiasis is postulated to be secondary to a va-
riety of causes10 and likely differs from that for humans
and dogs. However, the etiology of urate urolithiasis in
chelonians has yet to be defined.
Although methods for treatment of urolithiasis have
been described for a small number of chelonians,1,2,4,10–12
to our knowledge, a peer-reviewed retrospective study of
the diagnosis and treatment of urolithiasis in client-owned
chelonians has not been reported. The objectives of the
study reported here were to calculate the prevalence of

650 Scientific Reports JAVMA, Vol 247, No. 6, September 15, 2015
urolithiasis in client-owned chelonians examined at a vet-
erinary teaching hospital and to describe the clinical signs,
diagnosis, and treatment of urolithiasis in chelonians.
Materials and Methods
Case selection—The medical record database at
the William R. Pritchard Veterinary Medical Teaching
hospital was searched from January 1, 1987, through
December 31, 2012, to identify and retrieve records
of chelonians with urolithiasis. Keywords used for
the search included turtle, tortoise, urolith, urolithiasis,
cystic calculi, and bladder stone. Each of the retrieved
medical records was reviewed by 1 investigator (KAK)
to verify that the chelonian had urolithiasis. Urolithia-
sis was diagnosed on the basis of radiographic evidence
in conjunction with confirmatory results from other
diagnostic tests or direct visual observation of uroliths
(n = 32), necropsy results in the absence of any other
diagnostic test results (7), or CT results only (1). Con-
firmatory diagnostic tests included CT and coelomic
ultrasonography, and direct visual observation included
observing calculi in the urinary tract during surgery or
necropsy. Chelonians were excluded from the study
if they were not privately owned (eg, belonged to a
zoological exhibit or other public or research entity) or
urolithiasis was diagnosed on the basis of radiographic
evidence without at least 1 additional confirmatory test
result or visual observation of uroliths. Although cys-
toliths have been diagnosed in chelonians on the basis
of radiographic evidence alone,10 some of the cheloni-
ans evaluated for the study had radiographic evidence
of soft sludge in the bladder without discrete calculi;
therefore, we selected more stringent inclusion criteria
to ensure that the study population included only che-
lonians with a definitive diagnosis of urolithiasis.
Medical records review—For each chelonian, in-
formation extracted from the medical record included
signalment, clinical signs, husbandry, dietary history,
and results of all diagnostic tests or surgical proce-
dures performed. The genus and species for each che-
lonian were extrapolated on the basis of the common
name provided by the client. Sex was determined on
the basis of secondary sexual characteristics for a given
species or a history of laying eggs; the sex of juvenile
patients was frequently undetermined. When age was
unknown, the time that the animal was in the care of
its current owner was recorded. Patient dietary infor-
mation was classified into 1 of 3 categories as follows:
comprehensive dietary history that included both the
quantity and types of food offered, incomplete dietary
history in which the type but not the quantity of food
was available, or no dietary information available. Wa-
ter availability was categorized as always, intermittent,
or never or no information available. Plasma biochemi-
cal analyses and CBCs were performed at the veterinary
teaching hospital in accordance with standard methods
established by the clinical pathology laboratory. For
chelonians, standard plasma biochemical variables re-
ported included uric acid, calcium, phosphorus, glu-
cose, cholesterol, BUN, ionized calcium, total protein,
albumin, globulin, sodium, potassium, chloride, and
bile acid concentrations and AST and CK activities.
JAVMA, Vol 247, No. 6, September 15, 2015
Standard CBC variables included RBC count, hemo-
SMALL ANIMALS/
globin concentration, Hct, mean corpuscular volume,
mean corpuscular hemoglobin, mean corpuscular he-
EXOTIC
moglobin concentration, WBC count, and absolute
concentrations of heterophils, eosinophils, basophils,
lymphocytes, monocytes, and fibrinogen. For patients
that had multiple CBCs and plasma biochemical analy-
ses performed, only the results obtained closest to the
time that urolithiasis was diagnosed were evaluated.
When available, urinalysis was performed on urine
samples obtained by ultrasound-guided cystocentesis
or during cystotomy. Radiographic and CT images were
reviewed by 1 investigator (KAK), and the number and
location of calculi were recorded along with any other
abnormalities that were identified.
Calculi retrieved from the urinary tract were ana-
lyzed at the G. V. Ling Stone Analysis Laboratory at the
University of California-Davis. Uroliths were initially
analyzed by the oil immersion method of optical crys-
tallography with a polarized light microscopeb followed
by Fourier-transform infrared spectrometry with a spec-
trometerc equipped with spectroscopy softwared and kid-
ney stone library and analysis softwaree as described.26
Data analysis—The prevalence of urolithiasis in
pet chelonians that were examined at the veterinary
teaching hospital between 1987 and 2012 was calcu-
lated as the number of client-owned chelonians with
urolithiasis divided by the total number of client-
owned chelonians examined during that period. Sum-
mary statistics (mean, SD, median, and range) for CBC
and plasma biochemical variables were calculated only
for desert tortoises because they made up the majority
(31/40 [77.5%]) of the study population. Descriptive
data were provided for the other 9 chelonians.
Results
Prevalence of urolithiasis in client-owned che-
lonians—Between 1987 and 2012, 40 of 789 (5.1%)
client-owned chelonians examined at the veterinary
teaching hospital were confirmed to have urolithiasis.
This equated to a mean of 1.54 chelonians with uro-
lithiasis examined each year and a prevalence of 5.1
cases of urolithiasis/100 client-owned chelonians ex-
amined at the veterinary teaching hospital during the
26-year observation period.
Chelonians—The 40 chelonians with confirmed
urolithiasis that met the inclusion criteria for the study
included 31 (77.5%) desert tortoises (Gopherus agas-
sizii), 3 (7.5%) African spurred tortoises (Centrochelys
[Geochelone] sulcata), 2 (5%) red-eared sliders (Trache-
mys scripta elegans), 1 (2.5%) Hermann tortoise (Testudo
hermanni), 1 yellow-bellied slider (Trachemys scripta
scripta), and 1 Texas tortoise (Gopherus berlandieri); spe-
cies was not recorded for 1 tortoise. The study popula-
tion consisted of 19 (47.5%) males, 17 (42.5%) females,
and 4 (10%) juveniles for which the sex could not be
determined. When available, the mean age at the time of
examination was 26.2 years (median, 24 years; range, 6
months to 100 years). The body weight at the time of ex-
amination was available for 38 of the 40 chelonians and
ranged from 26 to 8,600 g (median, 3,875 g).
Scientific Reports 651
 Thirty of 40 (75%) chelonians were examined be- ly; however, the products used were recorded for only
cause of a single problem, whereas the remaining 10 4. Of the 40 chelonians, water was available ad libitum
(25%) chelonians were examined because of multiple for 21 (52.5%) and once or twice weekly for 2 (5%); the
SMALL ANIMALS/

problems. The most common reason for examination availability of water was not recorded for the remaining
EXOTIC

was hyporexia (n = 10 chelonians) followed by consti- 17 (42.5%).

pation (5), swollen limbs (3), respiratory tract prob-
Physical examination results—During physical
lems (3), lethargy (2), not laying eggs (2), cloacal pro-
examination, only 10 of 40 (25%) chelonians had a sol-
lapse (2), and collapse, toxicosis, soft shell, dog attack,
id coelomic mass palpable in the prefemoral fossa and
being caught in a cord, wound, ulcerated feet, metal
abnormalities associated with the urogenital system
ingestion, diarrhea, nasal discharge, swollen eyes, and
were recorded for only 5 (12.5%). The most common
lack of urate production (1 each). Nine of 40 (22.5%)
abnormality identified during physical examination of
chelonians were referred to the veterinary teaching hos-
the 40 chelonians was a change in mentation (n = 15)
pital after urolithiasis was diagnosed by another veteri-
followed by nasal discharge (12), weakness (7), soft
narian, and 1 chelonian did not have any clinical signs
bones (5), wounds (5), edema (4), dehydration (3),
and urolithiasis was diagnosed during routine annual
hyperemic skin (3), evidence of previous plastronot-
physical examination. omy (3), chemosis (3), pale mucous membranes (2),
Of the 40 study chelonians, 7 (17.5%) had a com- carapacial pyramiding (2), shell lesions (2), peeling
prehensive dietary record available, 28 (70%) had an
skin (2), thickened skin (2), stomatitis (2), expiratory
incomplete dietary record, and 5 (12.5%) had no di-
wheezes (2), ocular discharge (2), and cardiac arrhyth-
etary information. Review of the diets for which data
mia, straining to defecate or urinate, yellow-colored
were available revealed that most were species appro-
urates, open-beak breathing, palpebral thickening, hy-
priate, and dietary histories included outdoor graz-
phema, and cataracts (1 each).
ing opportunities with additional mixed leafy greens,
vegetables, and fruits for the tortoises. The diets for 6 Diagnostic test results—Plasma biochemical and
chelonians were deemed inappropriate; the diets for 5 CBC results were available and summarized for 25 des-
desert tortoises were supplemented with commercially ert tortoises (Table 1). Results were compared with
available monkey or dog food, and 1 adult red-eared referent values obtained from a database for desert tor-
slider was fed dog food exclusively. Nine of 40 (22.5%) toises maintained by the International Species Informa-
chelonians were fed a dietary supplement intermittent- tion System.f Results were not available for all variables

Table 1—Summary statistics for CBC and plasma biochemical variables for 25 client-owned desert tortoises (Gopherus agassizii) with
urolithiasis that were examined at a veterinary teaching hospital between 1987 and 2012.

Referent values*
No. of No. of
Variable tortoises Mean ± SD Median (range) Range SD tortoises
RBC count (X 106 cells/µL) 13 0.65 ± 0.15 0.65 (0.43–0.98) 0.12–26 6.81 14
Hemoglobin (g/dL) 14 7.74 ± 1.19 7.5 (6.2–10.4) 4.0–9.8 1.9 7
Hct (%) 24 31.54 ± 9.89 31 (18–60.5) 10–41 7.3 39
Mean corpuscular volume (fL) 13 526.8 ± 179.45 523.3 (270.4–746.7) 267.9–2,250 505.7 13
Mean corpuscular hemoglobin (pg) 13 123.62 ± 20.5 122.5 (77.6–163) 79.7–708.3 225.3 7
Mean corpuscular hemoglobin concentration (g/dL) 14 24.7 ± 4.72 27.35 (14.6–28.9) 18–34 5.4 7
WBC count (X 103 cells/µL) 24 5.78 ± 2.75 5.55 (1–11.4) 2.4–12 2.53 35
Heterophil count (X 103 cells/µL) 24 2.47 ± 1.62 2.1 (0.23–6.79) 0.1–8.29 2.18 33
Lymphocyte count (X 103 cells/µL) 24 0.99 ± 0.73 0.91 (0.09–2.81) 0.61–6.08 1.16 33
Monocyte count (X 103 cells/µL) 24 0.28 ± 0.38 0.2 (0–1.54) 0.03–1.68 0.4 16

Eosinophil count (X 103 cells/µL) 24 0.46 ± 0.92 0.1 (0–4.56) 0.08–1.96 0.5 19
Basophil count (X 103 cells/µL) 24 0.94 ± 0.65 0.84 (0–2.75) 0.03–2.42 0.679 32
Azurophil count (X 103 cells/µL) 24 0.39 ± 0.57 0.14 (0–2.23) 0–0.76 0.25 9
Fibrinogen (mg/dL) 22 163.64 ± 126.3 100 (100–500) — — —
Uric acid (mg/dL) 24 5.48 ± 3.77 4.7 (1.5–21.6) 0.6–12.9 2.7 29
Calcium (mg/dL) 24 12.24 ± 3.55 12 (2.8–21.9) 6.0–36.6 6.2 33
Phosphorus (mg/dL) 24 3.36 ± 3.85 2.4 (1.1–21.2) 1.2–13.5 3.0 31
Glucose (mg/dL) 24 86.96 ± 29.89 84 (48–175) 33–175 37 28
Total protein (g/dL) 24 4.47 ± 1.09 4.5 (1.9–6.6) 1.2–7.7 1.4 33
Albumin (g/dL) 20 1.74 ± 0.55 1.7 (0.9–2.9) 0.4–3.0 0.6 24

Globulin (g/dL) 20 2.75 ± 0.73 2.7 (1–4.1) 1.2–4.7 0.8 24

AST (U/L) 24 178.88 ± 210.2 88 (34–593) 24–315 66 30
CK (U/L) 24 9,335.26 ± 21,289.3 2,422 (83–95,790) 52–6,945 1,783 25
Cholesterol (mg/dL) 20 156.9 ± 140.16 120 (40–727) 27–476 145 17
BUN (mg/dL) 18 15.78 ± 16.4 10 (2–57) 0–41 10 22
Ionized calcium (mmol/L) 5 1.49 ± 0.55 1.74 (0.47–2.02) — — —
Sodium (mmol/L) 11 144 ± 8.11 140 (134–156) 127–150 6 26
Potassium (mmol/L) 11 4.82 ± 1.16 4.8 (3.3–7.5) 2.2–6.6 1.1 18
Chloride (mmol/L) 11 111.2 ± 10.5 110.5 (98–134) 97–121 7 19
Bile acids (µmol/L) 2 0.5 ± 0.5 0.5 (0–1) — — —

Results were not available for all variables for all tortoises.
*Referent values were obtained from a database for desert tortoises maintained by the International Species Information System.
— = Not available.

652 Scientific Reports JAVMA, Vol 247, No. 6, September 15, 2015
for all tortoises; therefore, the number of tortoises that during review of radiographic images, and the urolith

SMALL ANIMALS/
contributed to the summary statistics varied among was located in the left lobe of the bladder (n = 7), right
variables. For example, electrolyte concentrations were lobe of the bladder (2), accessory lobe of the bladder

EXOTIC
determined as part of the biochemical analysis for only (1), or in the cloaca (2). Six chelonians had multiple
11 of the 25 desert tortoises. Hematologic abnormalities calculi, all of which were located in the bladder. Other
identified in those tortoises included hemoconcentra- abnormalities observed during review of radiographic
tion (n = 3), leukopenia (2), leukocytosis (9), absolute images included long bone fractures (n = 3 cheloni-
azurophilia (4), and absolute eosinophilia or basophilia ans), diffuse osteopenia (3), gastrointestinal dilatation
(2). Review of plasma biochemical analyses revealed with gas (6), gravel in the gastrointestinal tract (1),
that 1 tortoise had severe hypocalcemia and hyper- pulmonary changes suggestive of pneumonia (1), and
phosphatemia as a result of nutritional hyperparathy- retained calcified eggs (1).
roidism. Four tortoises had AST activity increased from Thirteen of the 40 (32.5%) chelonians underwent
the upper referent value, and 4 tortoises had CK activity CT of the coelom, and uroliths were identified in all
increased from the upper referent value, 2 of which also 13 (Figure 2). Both radiographic and CT images were
had abnormally increased AST activity. One tortoise available for review for 4 chelonians, and the number
had hyperuricemia and 2 tortoises had BUN concentra- and location of uroliths visualized on the radiograph-
tions increased from the upper referent value. Four tor- ic images were in agreement with those visualized on
toises had hypernatremia, 1 tortoise had hyperkalemia, the CT images. For 2 of those chelonians, evaluation
and 1 tortoise had hyperchloremia. of the CT images provided additional information that
A CBC and plasma biochemical analysis were per- was not apparent during review of the radiographic
formed in 1 African spurred tortoise and 1 tortoise of images; noncalcified eggs were identified in one, and
unknown species, and a plasma biochemical analysis a large, hypodense liver suggestive of hepatic lipidosis
and determination of PCV were performed in anoth- was identified in the other. For the 9 chelonians that
er African spurred tortoise and 1 Texas tortoise. One did not have radiographic images available for review,
of the African spurred tortoises had a cloacolith that abnormalities identified during review of the CT im-
caused both a urinary and fecal obstruction and was ages included pulmonary infiltrates (n = 2), soft tissue
clinically dehydrated and hyperuricemic (uric acid coelomic masses (2), mineralized eggs (1), great vessel
concentration, 12.1 mg/dL; referent interval,27 2.1 to mineralization (1), and coelomic fluid (1).
10.5 mg/dL). The hematologic and biochemical results Ultrasonographic evaluation of the coelomic cav-
for the other 3 tortoises were unremarkable. ity was performed during the initial examination for 4
Urinalysis was performed for 3 desert tortoises;
urine samples for 2 of those tortoises were obtained by
ultrasound-guided cystocentesis, whereas the urine sam-
ple for the other tortoise was obtained during cystotomy.
An additional tortoise that had cystocentesis performed
only had the urine evaluated grossly and was recorded
as pale yellow in color with no additional information.
Urine specific gravity for those 3 tortoises ranged from
1.004 to 1.009 (referent interval,28,29 1.003 to 1.014). The
urinary pH (referent interval,28 8.0 to 8.5) was 8 for 2
tortoises and 5 for a male tortoise with an obstructive
cloacolith. None of the 3 tortoises had glucosuria or
ketonuria. The urine sample obtained during cystotomy
contained trace protein and 1+ hemoprotein. Analysis of
the urine sediment revealed an absence of RBCs, WBCs,
urinary casts, bacteria, lipids, and sperm for all 3 tor-
toises; however, a few transitional cells were observed in
the urine sediment for 2 of the tortoises, and 2 tortoises
had ammonium biurate crystalluria.
Radiographs were available for review for 19 of the
40 (47.5%) chelonians. Radiographic views commonly
obtained included a standard dorsoventral view and hor-
izontal-beam lateral and cranial-caudal views. When cal-
culi were visible, they typically had a radiopaque laminar
appearance and were generally located in the midcau-
dal region of the coelom and best visualized on dorso-
ventral images (Figure 1). The number of calculi in the
urinary tract region visualized on radiographic images
ranged from 0 to 4 (median, 1 calculus). One chelonian
did not have radiographic evidence of urolithiasis de- Figure 1—Dorsoventral radiographic image of a > 13-year-old
spite the observation of numerous small, rough cysto- male desert tortoise (Gopherus agassizii) that was obtained as
part of a routine annual physical examination. Notice a large
liths associated with a ruptured urinary bladder during round radiopaque lamellar structure (arrows) characteristic of a
necropsy. Twelve chelonians had 1 urolith visualized urate urolith in the left middle region of the coelom.

JAVMA, Vol 247, No. 6, September 15, 2015 Scientific Reports 653

SMALL ANIMALS/
EXOTIC
Figure 2—Cross-sectional CT image of the tortoise in Figure 1
obtained at the level of the urinary bladder and colon. Notice a
radiopaque lamellar structure characteristic of a urate urolith in
the left ventral region of the coelom.
desert tortoises. Ultrasonography was used to facilitate
cystocentesis and diagnostic coelomocentesis in 1 tor-
toise and to facilitate cystocentesis and characterize the
stage of ovarian development to assess whether ovario-
salpingectomy could be performed in conjunction with
the cystotomy for cystolith removal in another. In the
remaining tortoises, ultrasound was performed solely
to facilitate cystocentesis in one and to evaluate the
coelom for a cause of hematochezia in another. Three
tortoises also had CT of the coelom performed, and re-
view of the ultrasonographic findings did not reveal any
information that was not revealed during review of the
CT images.
Treatment—Seventeen of 40 (43.6%) chelonians
with urolithiasis underwent surgery to remove the
uroliths. The most common surgical approach was
cystotomy via plastronotomy (n = 12) followed by
holmium:yttrium-aluminum-garnet laser lithotripsy
via a prefemoral fossa approach to the urinary bladder
(3) and endoscopic-assisted manual digital removal of
cloacoliths through the cloaca (2). During surgery, 6 of
the 17 chelonians had a pharyngostomy tube placed to
facilitate administration of postoperative medications
and nutritional support. All surgeries were performed
by faculty clinicians or residents undergoing exotic ani-
mal training under the direct supervision of a faculty
clinician. Surgical intervention was recommended for
all study chelonians, but not all clients chose to pursue
surgical intervention. The decision to perform either
cystotomy or lithotripsy for urolith removal was made
on the basis of the attending clinician’s preference.
Five of the chelonians that underwent surgery de-
veloped postoperative complications. Four years after
cystotomy via plastronotomy was performed, a desert
tortoise was examined because of a partially nonad-
hered epoxy patch and lack of plastronotomy patch
654 Scientific Reports
healing. That tortoise had complete loss of the keratin
and bone in the plastron flap created during the cys-
totomy; however, the underlying tissue was thickened
and CT evaluation revealed that there was no com-
munication with the coelomic cavity. It was success-
fully treated by placement of a new epoxy patch. Two
months after cystotomy via plastronotomy, another
desert tortoise was examined because it had not uri-
nated in 1 month. Physical examination revealed ab-
normally increased respiratory effort and a palpable
coelomic fluid wave. Ultrasonographic evaluation
of the coelom revealed a severely distended bladder,
and removal of urine by cystocentesis resulted in an
improvement in respiratory effort. The tortoise was
anesthetized, and attempts to catheterize the urinary
bladder were unsuccessful. The patient died after an-
esthesia was discontinued, and severe bladder disten-
sion and bladder wall mucinosis were observed during
necropsy. A third desert tortoise died acutely 4 days af-
ter cystotomy via plastronotomy was performed, and
the owner did not permit performance of a necropsy. A
fourth desert tortoise died 3 days after lithotripsy, and
necropsy results were indicative of acute cystitis with
evidence of disseminated intravascular coagulation. A
fifth desert tortoise was euthanized 2 days after initial
examination following repeated unsuccessful manual
attempts to remove a cloacolith via cloacoscopy, and
the owner did not permit performance of a necropsy.
Thus, 4 of 17 chelonians died following surgery for
urolith removal (2 following plastronotomy, 1 follow-
ing lithotripsy, and 1 following attempted manual re-
moval of a cloacolith).
Necropsy results—Twenty-two of the 40 (55%)
chelonians were discharged from the hospital alive, and
long-term follow-up information was unavailable for
most of those patients except for those that were exam-
ined because of postoperative complications. Necropsy
was performed on 18 of the 40 (45%) study chelonians.
The decision to euthanize or the cause of death was
associated with urolithiasis or complications following
surgery for urolith removal in 9 of those chelonians.
Two chelonians (a 51-year-old female desert tortoise
and a 57-year-old female desert tortoise) died of post-
operative complications following surgery for urolith
removal as described. A female desert tortoise that was
> 60 years old had cystoliths and was euthanized be-
cause of a uterine prolapse. A 2-year-old male African
spurred tortoise had cystoliths and was euthanized be-
cause of a cloacal prolapse. Two other desert tortoises
with cystoliths (a > 20-year-old female and a > 50-year-
old male) died secondary to complications from a rup-
tured urinary bladder and had evidence of coelomitis
with or without gastrointestinal ileus. A > 36-year-old
male desert tortoise with a cloacolith was euthanized
because of gastrointestinal obstruction and ileus. A
6-month-old female Hermann tortoise with a cloaco-
lith died secondary to chronic fecal impaction and sep-
tic coelomitis caused by a colonic perforation and also
had a thickened bladder wall and nutritional secondary
hyperparathyroidism. A female yellow-bellied slider of
unknown age was euthanized because of deteriorating
condition at home and found to have bilateral obstruc-
tive ureteroliths.
JAVMA, Vol 247, No. 6, September 15, 2015
 Of the 18 chelonians on which necropsies were
performed, 14 had cystoliths, 2 had cloacoliths, 2 had
ureteroliths, and 2 had no uroliths identified but died
or were euthanized after surgical removal of cystoliths.
One chelonian with cystoliths also had ureteroliths,
and another with cystoliths also had a cloacolith. Other
lesions identified in the urinary tracts of the 18 chelo-
nians that were necropsied included a thickened (n =
3) or necrotic (1) bladder wall, tear in the bladder wall
(2), and severe bladder distension and bladder wall
mucinosis (1), renal gout (1), membranous glomeru-
lopathy and interstitial fibrosis (1), glomerulonephritis
and interstitial fibrosis (1), and interstitial fibrosis with
mineralization (1). Abnormalities identified during
necropsy that were not associated with the urinary tract
included hepatic lipidosis (n = 18), endoparasitism (3),
pneumonic lesions (3), generalized ileus (2), colonic
obstruction secondary to calculi (2), gastric ulceration
(1), cecal foreign body (1), stomatitis (1), and sand im-
paction (1). Three chelonians had lesions consistent
with nutritional secondary hyperparathyroidism. Two
chelonians had neoplastic lesions; 1 had squamous cell
carcinoma of the plastron and adjacent fat pads, and the
other had metastatic thyroid carcinoma.
Urolith composition—Uroliths from 13 cheloni-
ans were submitted for analysis. Those uroliths were
obtained from the bladder (n = 12) or cloaca (1) dur-
ing surgery (9) or necropsy (2) or by some unrecorded
method (2). All uroliths were composed of 100% urate.
Discussion
To our knowledge, the present study was the first
to determine the prevalence of urolithiasis in a popula-
tion of chelonians and the first to evaluate a population
of client-owned chelonians with confirmed urolithia-
sis. The mean prevalence of urolithiasis (5.1 cases/100
client-owned chelonians examined) during the 26-year
observation period of the present study suggested that
the disease is fairly common in client-owned cheloni-
ans examined at our institution. In a survey30 of necrop-
sy results for tortoises that died in captivity, the preva-
lence of urolithiasis was 4.2% (6/144). The prevalence
of urolithiasis calculated for the chelonians of the pres-
ent study may be an underestimate of the true preva-
lence because of the strict inclusion criteria used for
enrollment of study subjects or may be specific to our
region or hospital and may not be valid for populations
in other geographic regions or comprised of different
chelonian species.
The majority (31/40 [77.5%]) of chelonians evalu-
ated in the present study were desert tortoises, and this
likely represents a regional bias. Urate urolithiasis has
been reported in both free-ranging and client-owned
desert tortoises.4,10,11,14 African spurred tortoise was the
second most common species evaluated in the pres-
ent study, and urate urolithiasis has likewise been re-
ported in that species.1,2 In Europe, the most common
chelonian species affected by urolithiasis belonged to
the genera Testudo and Geochelone, which further sub-
stantiates regional differences in species that develop
urolithiasis.13,30 Interestingly, 3 aquatic turtles with
urolithiasis were included in the present study. To our
JAVMA, Vol 247, No. 6, September 15, 2015
knowledge, prior to this study, urolithiasis had been
SMALL ANIMALS/
described in only 2 aquatic chelonians,3,5 and uroliths
were not described in a large retrospective study31 of
EXOTIC
necropsy findings in aquatic chelonians. Cumulatively,
these findings indicate that, although several species
are overrepresented in the literature, many chelonian
species can develop urolithiasis.
All of the calculi analyzed in the present study
were composed of 100% urate. Although the etiology
of urolithiasis in chelonians has yet to be identified, the
pathophysiology of urate urolithiasis in chelonians is
postulated to develop secondary to a variety of causes
such as chronic dehydration, vitamin A and D deficien-
cies, and excessive intake of dietary calcium, protein, or
oxalates.10 In mammalian species, causes of urate uro-
lithiasis include hypocitraturia,24 metabolic aberrancies
associated with portosystemic shunts,19 and mutations
in the SLC2A9 gene that result in hyperuricemia and
hyperuricosuria.17 To our knowledge, many of these eti-
ologies have not been investigated in chelonians with
urolithiasis; however, chelonians process nitrogenous
wastes differently than do mammals.
In the present study, most of the chelonians were
terrestrial species that are uricotelic, which means they
excrete nitrogenous wastes in the form of uric acid.32
Uric acid is the end product of nitrogen metabolism
through a series of enzymatic reactions that involve
xanthine oxidase.33 Endogenous uric acid production
results from de novo purine synthesis and tissue ca-
tabolism. Exogenous uric acid production is dependent
on diet and is particularly high when the diet is rich in
animal protein.33 Most terrestrial chelonians typically
have a low-protein diet and should not have excessive
exogenous protein metabolism unless they are fed in-
appropriate diets, which can sometimes happen with
captive tortoises. The dietary history for 33 of the 40
(82.5%) chelonians in the present study was incom-
plete or unavailable, so although few diet abnormalities
were identified in the study population, it is possible
that some went undetected because of incomplete di-
etary histories. Clinicians should ensure that compre-
hensive dietary histories are obtained for chelonians to
aid in the elucidation of the role, if any, that diet has in
the development of urolithiasis.
In chelonians, uric acid is actively secreted by the
proximal tubules of the kidneys and excreted in the
urine.32 The form in which uric acid is excreted is de-
pendent on urine pH. When urine pH is < 5, uric acid
is present in the urine, whereas when urine pH is > 6.5,
most of the uric acid is excreted as urate or urate salts.33
Tortoises, like other herbivores, tend to have alkaline
urine,28,29 which favors the physiologic formation of
urate. Results of the present study and other case re-
ports and studies11,13–15 indicate that a high percentage
of uroliths obtained from chelonians are composed of
urate; however, uroliths should not be confused with
the normal urate material physiologically excreted by
terrestrial chelonians. Also, it is important to note that
uroliths of mixed composition or composed of struvite,
calcium phosphate, oxalate, and calcium carbonate
have also been described in chelonians.3,5,13,15,34
Unlike mammals, urine is modified in the lower uri-
nary tract of chelonians. Urine that passes through the
Scientific Reports 655
 ureters into the cloaca can flow retrograde into the blad-
SMALL ANIMALS/
der or colon, and urine in the bladder can flow retro-
grade into the colon. The epithelium of both the bladder
EXOTIC
and colon can absorb water, which results in urine con-
centration.32,35 Free-ranging desert tortoises retain urate
precipitates in the bladder until rainfall stimulates blad-
der emptying followed by imbibition of a large volume
of water.35 Thus, chronic dehydration, chronic overheat-
ing, or lack of a suitable water source might cause an
increase in water absorption from the bladder and colon,
which leads to further supersaturation and concentra-
tion of urate excreta in the bladder and might be a pre-
disposing factor for urolith formation. Twenty-one of 40
(52.5%) chelonians of the present study had free access
to water; however, 2 (5%) had only intermittent access
to water, and water availability was not indicated in the
medical records for 17 (42.5%). Although 34 of the 40
(85%) chelonians were considered desert species (des-
ert tortoises and African spurred tortoises), those spe-
cies still require water, particularly in captive situations
where a humid burrow is often not provided. In addition
to humidity, a burrow provides terrestrial desert cheloni-
ans with a cool area to escape hot daytime temperatures.
Currently, it is unknown how restricted water access
and possible chronic overheating affects the incidence
of urolithiasis in client-owned chelonians in California.
Clinicians are encouraged to obtain information about
water availability, temperature and temperature gradient
monitoring, and the availability of burrows in outdoor
enclosures when acquiring histories for chelonians.
Many of the chelonians of the present study were
examined for reasons unrelated to the urogenital sys-
tem. Although most cats with urolithiasis are examined
because of urination abnormalities,19 only 1 of the tor-
toises of the present study was examined because of
abnormal urination. Owners typically do not observe
chelonians urinate because tortoises are kept outside
when the weather is appropriate, and free-ranging des-
ert tortoises may only urinate during the rainy season
and have infrequent urination patterns, compared with
those of domestic mammals.35 Other clinical signs of
the urogenital tract (cloacal prolapse, constipation, and
egg retention) that are associated with urolithiasis1,2,10
were reported in only 5 of the 40 (12.5%) chelonians of
the present study. In this study, only 1 chelonian with-
out a history of clinical signs had urolithiasis diagnosed
during a routine annual physical examination, which
contrasted with results of another study11 in which uro-
lithiasis was diagnosed during routine physical exami-
nations of all 100 tortoises evaluated. In that study,11 1
veterinarian examined all the tortoises at a primary care
facility; however, the chelonians of the present study
were examined by various veterinarians and most were
referred to a tertiary veterinary care facility. Therefore,
all chelonians should have a routine annual examina-
tion that includes diagnostic imaging to screen for uro-
lithiasis so that the disease can be identified and treated
before it becomes an emergency situation. Further-
more, clinicians should be aware that, unlike dogs and
cats, chelonians with urolithiasis are often examined
for reasons unrelated to the urogenital system.
Few chelonians in the present study had physical
examination abnormalities specifically related to uroli-
656 Scientific Reports
thiasis. Most had musculoskeletal, respiratory, or mis-
cellaneous abnormalities. Although diagnosis of uroli-
thiasis via digital palpation of a hard structure in the pre-
femoral fossa has been described,10 only 10 of 40 (25%)
chelonians in the present study had a urolith that was
palpable through the prefemoral fossa. The surprisingly
low percentage of chelonians with a palpable calculus in
the prefemoral fossa in this study might be the result of
poor record keeping, lack of prefemoral palpation dur-
ing physical examination because of patient size, or lack
of sensitivity of this physical examination variable. Re-
gardless, the results of the present study suggested that
the lack of physical examination abnormalities related to
the urogenital tract or a palpable mass in the prefemoral
fossa of chelonians should not preclude urolithiasis as a
differential diagnosis.
The chelonians of the present study had few hema-
tologic and biochemical abnormalities, which contrasted
with the results of another study14 in which free-ranging
desert tortoises that died because of urate urolithiasis
had substantially abnormal BUN and uric acid concen-
trations. In the present study, only 3 desert tortoises had
hyperuricemia or abnormally increased BUN concen-
trations. Failure to identify a trend for hematologic or
biochemical abnormalities in chelonians with urolithia-
sis might be associated with the low number of study
chelonians that had a CBC or plasma biochemical analy-
sis performed. Also, in chelonians, clinically normal he-
matologic and biochemical variables vary greatly on the
basis of season, sex, sexual maturity, nutrition, environ-
ment, and husbandry, which makes clinical interpreta-
tion of the data from this retrospective study difficult.
Because appropriate reference intervals for hematologic
and biochemical variables have yet to be established for
captive desert tortoises, we used values obtained from
the International Species Information System database as
referents in the present study; however, the limitations
of those values (obtained by use of multiple methodolo-
gies, without confirmation of systemic health) should be
considered.
In nonchelonian species with urolithiasis, urinaly-
sis frequently reveals hematuria, pyuria, bacteriuria, hy-
pocitraturia, crystalluria, and pH abnormalities.16,18,19,24
Urinalysis was performed for only 3 tortoises in the pres-
ent study. Microscopic evidence of blood was detected in
the urine of only 1 tortoise, and that urine sample was
obtained during surgery and might have been contami-
nated with blood. The urine pH fell within the expected
alkaline range for 2 of the 3 tortoises; however, 1 tortoise
had a urine pH of 5.0, which might have been a conse-
quence of prolonged anorexia29 or acid-base aberrations
associated with obstruction of the lower urinary tract.
Two tortoises had crystalluria, which is a common find-
ing in the urine of healthy tortoises.28,29 The paucity of
urinalysis results for the tortoises of the present study
and the lack of clinically normal urinalysis values for
chelonians limit the value of urinalysis for diagnosis of
urolithiasis in chelonian species until further informa-
tion is obtained.
Urate uroliths are not always visible on radiograph-
ic images. Uroliths were visible on radiographic images
of 143 of 159 (90%) cats with urate urolithiasis; how-
ever, many of those cats had uroliths that contained
JAVMA, Vol 247, No. 6, September 15, 2015
both urate and struvite or calcium oxalate.19 In chelo-
nians, urate uroliths have a thick laminar appearance
on radiographic images, and this laminar appearance
is presumed to be caused by the repeated deposition of
supersaturated crystalline material on the urolith.10 Of
the 19 chelonians for which radiographic images were
available for review in the present study, 18 had uro-
liths that were radiographically visible. For the chelo-
nians that had only 1 urolith identified radiographi-
cally (n = 12), that urolith was generally located in the
left lobe of the bladder (7), a finding that was in agree-
ment with the results of another study.11 Chelonian
species typically have a bilobed urinary bladder36 and
an asymmetric liver in which the right hepatic lobe
is generally larger than the left hepatic lobe. It is hy-
pothesized that the large right hepatic lobe decreases
the space available for calculus formation in the right
lobe of the bladder.36
Seventeen of the 40 chelonians of the present study
underwent surgery for urolith removal, 5 developed
postoperative complications, and 4 of those died or
were euthanized. The most common surgical procedure
performed for urolith removal in the present study and
other studies2,4,10,11 was cystotomy via plastronotomy.
Three of the 12 tortoises that underwent that procedure
developed complications, and 2 subsequently died. The
cause of bladder wall mucinosis in the tortoise that died
2 months after the plastronotomy was unknown and
might have been secondary to overactive granular cells
in the bladder epithelium that secrete mucus to protect
the epithelium from urate crystalluria.37 Other investi-
gators14 have reported that the cytoplasm of apical blad-
der epithelial cells is expanded with mucin granules in
free-ranging desert tortoises with urolithiasis. For the
tortoise of the present study, the bladder wall mucinosis
might have been induced by the presence of suture in
the bladder wall from the cystotomy or inflammation
associated with surgery and chronic urolithiasis. For the
tortoise of the present study that had a nonhealing plas-
tronotomy flap, it was theorized that failure to place a
barrier (typically bone wax) between the surgical bone
incision in conjunction with the irregular edge of the
plastronotomy incision allowed the epoxy used in the
plastron patch to leak into the surgical bone incisions
and inhibit healing.36 Clinicians considering surgical
removal of uroliths from chelonians should be aware
of potential postoperative complications. In the present
study, 2 of 12 chelonians died following cystotomy via
plastronotomy, 1 of 3 died following lithotripsy, and 1
of 2 died following digital removal of a cloacolith. Com-
plication and mortality rates for these 3 procedures may
differ for many reasons, including patient health status,
anesthesia protocol used, and surgeon experience and
comfort. To our knowledge, complication and mortal-
ity rates are not currently available for other surgical
procedures for urolith removal in chelonians such as
bladder marsupialization via a prefemoral incision.12,a
Necropsy was performed on 18 of the chelonians
of the present study, and urolithiasis contributed to the
decision to euthanize or was the cause of death for 9.
In those 9 chelonians, abnormalities identified during
necropsy were primarily associated with the urinary
tract. Those findings suggested that early diagnosis and
JAVMA, Vol 247, No. 6, September 15, 2015
treatment of urolithiasis is necessary to prevent mor-
SMALL ANIMALS/
bidity and death, and chelonian owners should be in-
formed of potential life-threatening outcomes such as
EXOTIC
tear or rupture of the bladder wall that may occur if
urolithiasis is not treated.
Results of the present study indicated that client-
owned chelonians with urolithiasis can have a variety of
clinical signs and physical examination abnormalities
that may or may not be directly referable to the urinary
tract. Hematologic, biochemical, and urinalysis find-
ings for the chelonians of this study were nonspecific
for diagnosis of urolithiasis. Many of the chelonians in
this study died or were euthanized as a consequence
of urolithiasis, which suggested that early identifica-
tion and appropriate intervention should be pursued
to correct this disease. Postoperative complications
associated with cystotomy via plastronotomy were in-
frequent and included bladder wall mucinosis and fail-
ure of plastronotomy patch healing. The acquisition of
comprehensive dietary and environmental history for
client-owned chelonians with urolithiasis is necessary
to elucidate the etiology of the disease.
a. Lamberski N, San Diego Zoo Safari Park, Escondido, Calif: Per-
sonal communication, 2014.
b. Universal polarizing microscope, Carl Zeiss Inc, Thornwood, NY.
c. Impact 410 spectrometer, Nocolet Instrument Corp, Madison, Wis.
d. OMNIC Software Suite, Nocolet Instrument Corp, Madison, Wis.
e. Therm Electron Corp, Asheville, NC.
f. ISIS Physiological Data Reference Values Project, Apple Valley,
Minn: International Species Information System (ISIS), 2010.
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From this month’s AJVR

Clinical efficacy of hydrocodone-acetaminophen

and tramadol for control of postoperative pain
in dogs following tibial plateau leveling osteotomy
Marian E. Benitez et al

September 2015
Objective—To evaluate clinical efficacy of hydrocodone-acetaminophen and tramadol for treatment
of postoperative pain in dogs undergoing tibial plateau leveling osteotomy (TPLO). See the midmonth issues
Animals—50 client-owned dogs.
of JAVMA
Procedures—Standardized anesthetic and surgical protocols were followed. Each patient was
randomly assigned to receive either tramadol hydrochloride (5 to 7 mg/kg, PO, q 8 h; tramadol group) for the expanded
or hydrocodone bitartrate–acetaminophen (0.5 to 0.6 mg of hydrocodone/kg, PO, q 8 h; hydrocodone
group) for analgesia after surgery. The modified Glasgow composite measure pain scale was used table of contents
to assess signs of postoperative pain at predetermined intervals by an investigator who was blinded
to treatment group. Scoring commenced with the second dose of the assigned study analgesic. for the AJVR
Pain scores and rates of treatment failure (ie, dogs requiring rescue analgesia according to a
predetermined protocol) were compared statistically between groups.
or log on to
Results—12 of 42 (29%; 5/19 in the hydrocodone-acetaminophen group and 7/23 in the tramadol avmajournals.avma.org
group) dogs required rescue analgesic treatment on the basis of pain scores. Median pain score for
the hydrocodone group was significantly lower than that of the tramadol group 2 hours after the for access
second dose of study analgesic. The 2 groups had similar pain scores at all other time points. to all the abstracts.
Conclusions and Clinical Relevance—Overall, differences in pain scores between dogs that
received hydrocodone-acetaminophen or tramadol were minor. The percentage of dogs with
treatment failure in both groups was considered unacceptable. (Am J Vet Res 2015;76:755–762)

658 Scientific Reports JAVMA, Vol 247, No. 6, September 15, 2015

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