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1050 JAVMA • Vol 248 • No. 9 • May 1, 2016
Zoo Animals
Bacteria of the genus Salmonella are important causes of gastrointestinal and extraintestinal dis-
ease in humans and other animals.1–3 Salmonellosis is 
a major public health problem, with an estimated 1 
million people affected annually in the United States.4 
Although most cases of disease are attributable to 
food contamination, salmonellosis acquired by con-
tact with or exposure to infected animals contributes 
to the disease burden.5–13 Salmonellosis in humans fol-
lowing contact or exposure to reptiles is associated 
with outcomes ranging from gastrointestinal illness to 
sepsis, shock, and death, which has led to recommen-
dations and legislation to reduce the risk of exposure 
or infection.14,15
Salmonella infection and carriage in reptiles 
in a zoological collection
Meredith M. Clancy dvm, mph
Meghan Davis dvm, mph, phd
Marc T. Valitutto vmd
Kenrad Nelson md
John M. Sykes IV dvm
From the Wildlife Conservation Society, Zoological 
Health Program, Bronx, NY 10460 (Clancy, Valitutto, 
Sykes); and the Bloomberg School of Public Health, Johns 
Hopkins University, Baltimore, MD 21205 (Clancy, Davis, 
Nelson). Dr. Clancy’s present address is San Diego Zoo 
Safari Park, 15500 San Pasqual Valley Rd, Escondido, CA 
92027. Dr. Valitutto’s present address is Staten Island 
Zoo, 614 Broadway, Staten Island, NY 10310.
Address correspondence to Dr. Clancy (mclancy@
sandiegozoo.org).
OBJECTIVE
To identify important subspecies and serovars of Salmonella enterica in a cap-
tive reptile population and clinically relevant risk factors for and signs of illness 
in Salmonella-positive reptiles.
DESIGN
Retrospective cross-sectional study.
ANIMALS
11 crocodilians (4 samples), 78 snakes (91 samples), 59 lizards (57 samples), 
and 34 chelonians (23 samples) at the Bronx Zoo from 2000 through 2012.
PROCEDURES
Data pertaining to various types of biological samples obtained from reptiles 
with positive Salmonella culture results and the reptiles themselves were ana-
lyzed to determine period prevalence of and risk factors for various Salmo-
nella-related outcomes.
RESULTS
Serovar distribution differences were identified for sample type, reptile phylo-
genetic family, and reptile origin and health. Salmonella enterica subsp enterica 
was the most common subspecies in Salmonella cultures (78/175 [45%]), iden-
tified across all reptilian taxa. Salmonella enterica subsp diarizonae was also 
common (42/175 [24%]) and was recovered almost exclusively from snakes (n 
= 33), many of which had been clinically ill (17). Clinically ill reptiles provided 
37% (64) of Salmonella cultures. Factors associated with an increased risk of 
illness in reptiles with a positive culture result were carnivorous diet and 
prior confiscation. Snakes had a higher risk of illness than other reptile groups, 
whereas lizards had a lower risk. Bony changes, dermatitis, and anorexia were 
the most common clinical signs.
CONCLUSIONS AND CLINICAL RELEVANCE
This study provided new information on Salmonella infection or carriage and 
associated clinical disease in reptiles. Associations identified between serovars 
or subspecies and reptile groups or clinical disease can guide management of 
Salmonella-positive captive reptiles. (J Am Vet Med Assoc 2016;248:1050–1059)
Much research has already been conducted, but 
the role of salmonellae in disease of reptiles remains 
unclear. When a reptile is exposed to the organism, 
a range of clinical outcomes is possible. Subclinical 
carriage, with intermittent shedding of salmonellae 
through feces, is common.16–18 Constant reinfection 
can occur through this shedding, making clearance of 
the pathogen challenging. This intermittent shedding 
and risk of reinfection complicate the understanding 
of epidemiology and pathophysiology of salmonello-
sis in reptiles.3,16,19 
Historically, serotyping was performed on Salmo-
nella isolates in an attempt to elucidate the course of 
disease in individuals and the epidemiology of infec-
tion in populations. This has allowed for tracking and 
tracing of outbreaks of salmonellosis by serovar. In a 
population of animals, serotyping can permit moni-
toring and longitudinal analyses, although molecular 
diagnostic methods, such as pulsed-field gel electro-
ABBREVIATIONS
CI Confidence interval
RR Relative risk
 JAVMA • Vol 248 • No. 9 • May 1, 2016 1051
Zoo Animals
phoresis, now allow for more exact epidemiological 
tracing.20
Nomenclature for the genus Salmonella has been 
constantly evolving, leading to some inconsistencies 
in the literature, particularly for subspecies of veteri-
nary importance. The genus includes 2 extant species: 
Salmonella enterica and Salmonella bongori. The 6 
subspecies of Salmonella enterica (enterica [I], sala-
mae [II], arizonae [IIIa], diarizonae [IIIb], houtenae 
[IV], and indica [VI]) are further categorized into 
serovars, with 2,637 extant serovars recognized.21,22 
Serovars are determined by phenotyping of the O 
(somatic) and H (flagellar) antigens. Certain serovars 
are associated with specific clinical syndromes, and 
although the inherent virulence of a serovar can in-
crease a bacterium’s propensity to cause disease, host 
immunity plays a large role in its pathogenicity.21,23,24 
This is of particular importance in ectothermic ani-
mals, in which ambient temperature influences me-
tabolism and immune response.19
Multiple serovars from multiple subspecies of 
S enterica have been associated with reptile-associated 
salmonellosis in humans and with subclinical carriage 
and clinical disease in reptiles.1,5,13,16,25–42 Historically 
associated with reptiles, serovars from subspecies ari-
zonae (IIIa) and diarizonae (IIIb) were once listed in 
their own genus (Arizona),29,31,42,43 and some labora-
tories fail to differentiate between these 2 subspecies 
during initial biochemical testing.23
Much published information on salmonellae in 
reptiles focuses on prevalence in routinely collected 
biological samples, point prevalence in opportunisti-
cally collected samples, or clinical illness associated 
with specific strains. Reports of associations between 
clinical disease and Salmonella carriage are uncom-
mon, but understanding the importance of positive 
Salmonella culture results in reptiles is important to 
practicing best medicine. 
At the Wildlife Conservation Society Bronx Zoo, 
reptiles have been kept in an ever-changing popula-
tion for more than a century. Salmonella spp have 
been cultured from various surveillance and diagnos-
tic biological samples from both apparently healthy 
and clinically ill animals. Given the diversity of this 
reptile population and the ability to track demograph-
ic information and health status, the Bronx Zoo pro-
vides a unique opportunity to evaluate the epidemiol-
ogy of Salmonella carriage and infection in a captive 
reptile population over several years. The purpose of 
the study reported here was to retrospectively char-
acterize S enterica isolates in this population, subspe-
cies and serovar distribution, squamate population 
prevalence, individual factors associated with clinical 
disease, and common clinical signs and outcome.
Materials and Methods
Animals and samples
The study was designed to focus on all positive 
Salmonella culture results obtained from reptiles 
housed at the Bronx Zoo from January 1, 2000, to 
December 31, 2012. Biological samples for microbial 
culture were collected by multiple methods during 
routine or diagnostic examinations of the reptiles, 
most commonly via collection of fresh fecal samples. 
All samples were shipped from the Bronx Zoo in bac-
terial transport mediaa to the Cornell University Ani-
mal Health Diagnostic Center, which is the state vet-
erinary diagnostic laboratory of New York.Microbial 
culture of fecal samples was performed by standard 
methods, often including testing for multiple enteric 
pathogens.44 Colonies with biochemical properties 
consistent with Salmonella spp were confirmed as 
salmonellae by use of an automated microbiological 
identification systemb and serogrouped via slide ag-
glutination testing. Results of these laboratory tests in-
cluded subspecies of S enterica and often serogroup 
(O antigen grouping). In the event of a positive culture 
result, samples were also sent to the National Veteri-
nary Services Laboratory for full serotyping.
Sample data sets
The study was designed in 4 portions. For the 
first portion involving overall characterization of all 
Salmonella isolates recovered from reptiles, the study 
population consisted of all samples from any reptile 
housed at the Bronx Zoo for which positive results 
of Salmonella testing were obtained from January 1, 
2000, to December 31, 2012. These data were identi-
fied through a laboratory record search at the Cornell 
University Animal Health Diagnostic Center. Informa-
tion from the Cornell University Animal Health Diag-
nostic Center and Bronx Zoo medical recordsc was 
catalogued to include reptile group, family, genus, and 
species; sample source (feces, swab specimen of solid 
organ, aspirate, or other source); and Salmonella se-
rogroup and serovar. If full serotyping had not been 
performed or was not possible, the sample was includ-
ed in the dataset with notation of lack of full typing. 
These data were analyzed for serogroup and serovar 
distribution. Reptiles from which multiple isolates 
were recovered were included. Gathered data were 
used to calculate the prevalence of positive Salmo-
nella culture results in squamate populations (lizards 
and snakes) during the study period.
The second portion of the study included charac-
terization of all individual reptiles from which salmo-
nellae had been isolated during the study period, with 
the intention of identifying individual risk factors for 
and population prevalence of positive Salmonella 
culture results. This dataset was developed from the 
laboratory records from the Cornell University Animal 
Health Diagnostic Center and evaluation of individual 
reptile records, including review of medical and zoo-
logical collection data in Bronx Zoo medical records.c 
Any reptile with an active clinical problem recorded 
in the medical record, abnormal behavior, or clinical 
signs at point of sample collection was defined as ill. All 
medical records for the 60 days prior to and following 
sample submission were reviewed by the same investi-
1052 JAVMA • Vol 248 • No. 9 • May 1, 2016
Zoo Animals
gator for consistency of clinical illness designation, and 
reptiles without medical records or husbandry notes 
were excluded from analysis. Reptile order or suborder 
(chelonian, crocodilian, lizard, and snake), family, genus, 
species, sex, age, and origin were cataloged as well as 
sample source, collection point (during the routine 30-
day quarantine period, after quarantine, or after death), 
and type (diagnostic or routine). Diet type of the vari-
ous reptile species was established on the basis of zoo-
logical collection information and the natural history 
of the species. When an individual reptile could not be 
identified via sample submission data or medical record 
review, the sample was excluded from this portion 
of the study. Individual animals that had missing data 
points (eg, sample source, collection point, or type) 
were excluded from analysis of that putative risk factor 
but were included in serotype distribution, prevalence, 
and incidence calculations.
The third portion of the study was designed to 
characterize antimicrobial susceptibility in recovered 
Salmonella isolates. Information was collected regard-
ing signalment, grouping, and taxa (family, genus, and 
species) of the reptile from which each isolate had been 
recovered; sample source, type, and collection point; and 
isolate antimicrobial susceptibility patterns. Because of 
changes in the panel of antimicrobials used in suscep-
tibility testing during the study period, proportions of 
susceptible samples rather than absolute numbers were 
used for analysis. Total susceptibility patterns for each 
sample were also analyzed to compare with reported 
patterns for multidrug-resistant Salmonella isolates.
The final portion of the study included evaluation 
of fecal shedding of salmonellae and prevalence of 
positive Salmonella culture results over a 5-year sub-
set of the study period (2008 to 2012). All fecal sam-
ples from reptiles during this period were evaluated 
to identify prevalence within reptile group and family.
Statistical analysis
To examine true population prevalence, squamate 
(lizard and snake) population totals were established 
per annum from 2000 through 2012, along with total 
population numbers during the study period. Squa-
mates were selected only because they contributed 
most of the Salmonella-positive samples, and the au-
thors believed this would reduce possible inaccura-
cies in chelonian population totals caused by colony 
accessions with incomplete population data and low 
numbers of positive crocodilian samples. The numera-
tor consisted of the total number of individuals with 
positive culture results, and the denominator consist-
ed of the total number of individuals in the relevant 
squamate population. Individuals from which multiple 
positive samples had been collected were counted 
only once in this calculation.
Bronx Zoo sample submission records allowed 
calculation of the prevalence of positive Salmonella 
culture results for fecal samples during the last 5 years 
of the study period (January 1, 2008, to December 31, 
2012). Calculations were made by identifying the to-
tal number of fecal samples collected from reptiles 
housed at the Bronx Zoo that were submitted for mi-
crobial culture over that period and the total number 
of fecal samples with positive Salmonella culture re-
sults over the study period. Individual reptiles from 
which multiple positive samples had been obtained 
were counted only once, and the denominator for 
prevalence calculations was the total number of fecal 
samples submitted rather than the number of individ-
ual reptiles.
In addition to prevalence calculations, binary logis-
tic regression was performed to identify risk factors for 
positive Salmonella culture results by maximum likeli-
hood, and RR and 95% CIs were computed. Binary lo-
gistic regression was also performed to evaluate serovar 
and subspecies differences. A similar approach was 
used to calculate the RR that Salmonella spp would be 
isolated from a clinically ill (vs non–clinically ill) reptile. 
Values of P < 0.05 were considered significant. Statisti-
cal softwared was used for all calculations.
Results
Overall characterization 
of Salmonella isolates
Between January 1, 2000, and December 31, 2012, 
positive results of Salmonella culture were obtained 
for 175 biological samples (4 crocodilian, 23 cheloni-
an, 57 lizard, and 91 snake) collected from 182 reptiles. 
Full serotyping was not performed or not possible for 
27 (15%) of these samples. Multiple isolates were re-
covered from 30 reptiles (22 samples), yielding a total 
of 35 isolates, with samples collected from groups of 
reptiles (rather than individuals) contributing to the 
total number of samples (175) and isolates (182). Bio-
logical sample types from which salmonellae were iso-
lated included fecal samples (117/175 [67%]) as well 
as swab or wash specimens from the cloaca (20/175 
[11%]), coelom (9/175 [5%]), gastrointestinal tract and 
liver (11/175 [6%]), and other solid organs or masses 
(18/175 [10%]).
Serovars identified via serotyping of isolates from 
samples with a positiveculture result were unevenly 
distributed among the subspecies of S enterica: 39 
enterica (I), 3 salamae (II), 6 arizonae (IIIa), 25 di-
arizonae (IIIb), and 5 houtenae (IV). Many serovars 
were identified repeatedly in the study, with only 78 
unique serovars detected. These serovars represented 
only a small percentage of extant serovars (3%), but 
the representation of each subspecies differed, with 
higher prevalences of subspecies diarizonae (IIIb; 
7%), houtenae (IV; 7%), and arizonae (IIIa; 6%). Se-
rovar distribution among subspecies of S enterica was 
significantly (P < 0.001) associated with reptile order 
or suborder and family insofar as certain subspecies 
appeared to have limited host range in this population. 
Salmonella enterica subsp enterica (I) was the most 
common (n = 78 [45%]), and S enterica subsp diarizo-
nae (IIIb) was the second most common (42 [24%]). 
Isolates of S enterica subsp diarizonae (IIIb; 42) were 
 JAVMA • Vol 248 • No. 9 • May 1, 2016 1053
Zoo Animals
mostly recovered from snakes (34 [81%]), and all 
isolates of S enterica subsp arizonae (IIIa; 10) were 
also recovered from snakes. The single most common 
serovar was Salmonella Newport (n = 10). Salmo-
nella serovar IV 43:z4,z32:– was recovered multiple 
(8) times, including 5 times from a snake described 
in a previous case report.67 Other common serovars 
include Salmonella serovars Braenderup (n = 6) and 
Montevideo, Oranienburg, and Thompson (4 each).
Characterization of all reptiles 
with positive Salmonella culture results
Samples with positive Salmonella culture results in-
cluded in the study dataset were obtained from individual 
reptiles (n = 182) representing 67 species (Table 1). The 
fact that some samples had been collected from groups 
of reptiles rather than individual reptiles contributed to a 
discrepancy between individual and sample counts. Iden-
tities could not be discerned for the reptiles from which 
8 samples with positive results were obtained; therefore, 
these samples were excluded from the second portion of 
the study, in which individual risk factors were identified.
Most samples (148/175 [85%]) originated from 
squamates, with uneven distribution among reptile 
families and genera (Table 2). Total prevalence of posi-
tive Salmonella culture results over the study period 
for lizards was 16% (95% CI, 15% to 18%), with a high 
prevalence identified for lizards in the genera Uropla-
tus (42%) and Lialis (80%). Snakes had a similar preva-
lence of 18% (95% CI, 16% to 19%). Certain genera in 
each snake family had a high prevalence of positive 
Salmonella culture results, including Corallus (40%), 
Epicrates (29%), and Eunectes (32%) in the family Boi-
dae; Morelia (57%) in the family Pythoidae; and Agkis-
trodon (34%) and Bitis (71%) in the family Viperidae. 
No positive culture results were obtained for 2 genera 
of Boidae (Candoia and Sanzinia) and 3 genera of Py-
thonidae (Aspidites, Calabaria, and Malayopython).
With respect to fecal samples collected from 2008 
to 2012, snakes had the highest prevalence of positive 
Salmonella culture results (33%; 95% CI, 21% to 44%), 
followed by lizards (22%; 95% CI, 10% to 34%). Preva-
lence for crocodilians (8%; 95% CI, 0% to 21%) and 
chelonians (4%; 95% CI, 0% to 10%) during this period 
was considerably lower.
Characteristics of clinically ill reptiles 
with positive Salmonella culture results
Sixty-four individual reptiles had clinical illness 
at the point a Salmonella-positive specimen was col-
 Total No. of Total No. Total No.
 individuals of individuals of samples RR (95% CI) that 
 contributing samples with positive samples (total pertaining sample was from 
Reptile group (total ill) (total ill) to ill reptiles) ill reptile P value
Crocodilian 11 (0) 2 (0) 4 (0) 0.37 (0.01–5.31) 0.46
 Alligatoridae 9 (0) 1 (0) 3 (0) — —
 Crocodylidae 1 (0) 1 (0) 1 (0) — —
 
Chelonian 34 (15) 11 (5) 23 (10) 1.27 (0.12–6.54) 0.36
 Emydidae 3 (1) 3 (1) 3 (1) — —
 Geomydidae 1 (1) 1 (1) 1 (1) — —
 Testudinidae 30 (13) 8 (3) 19 (8) — —
 
Lizard 59 (16) 22 (9) 57 (6) 0.55 (0.32–0.98) 0.03
 Agamidae 10 (2) 3 (2) 6 (2) — —
 Anguidae 1 (0) 1 (0) 1 (0) — —
 Crotaphytidae 1 (1) 1 (1) 1 (1) — —
 Gekkonidae 14 (0) 4 (0) 15 — —
 Gerrhosauridae 1 (0) 1 (0) 1 (0) — —
 Helodermatidae 1 (1) 1 (1) 1 (1) — —
 Iguanidae 3 (0) 3 (0) 3 (0) — —
 Opluridae 2 (0) 1 (0) 1 (0) — —
 Pygopodidae 8 (2) 1 (1) 8 (2) — —
 Scincidae 1 (0) 1 (0) 1 (0) — —
 Varanidae 17 (6) 6 (4) 20 (7) — —
 
Snake 78 (33) 31 (20) 91 (39) 1.57 (1.03–2.39) 0.04
 Boidae 25 (12) 5 (5) 28 (11) — —
 Colubridae 17 (7) 8 (4) 19 (9) — —
 Elapidae 4 (3) 3 (2) 4 (3) — —
 Pythonidae 11 (6) 6 (3) 12 (7) — —
 Viperidae 21 (5) 9 (3) 28 (9) — —
— = Not calculated. Values of P < 0.05 were considered significant.
Table 1—Relative risk of positive Salmonella culture results for biological samples obtained from various groups of reptiles with 
versus without clinical illness at the Bronx Zoo from 2000 through 2012.
1054 JAVMA • Vol 248 • No. 9 • May 1, 2016
Zoo Animals
lected. Common clinical signs in these reptiles were 
bony changes (n = 15), dermatitis (15), anorexia (14), 
and lethargy or weakness (10). Other clinical signs in-
cluded failure to thrive (n = 8), neurologic abnormali-
ties (7), gastrointestinal parasitism (7), loss of body 
weight or condition (7), coelomic swelling or mass 
(5), dehydration (5), and gasping or other respiratory 
abnormalities (5).
Clinically ill reptiles provided 37% of all samples 
with positive culture results (61 samples from 64 indi-
viduals). Although most biological samples pertaining 
to the overall population were fecal samples collect-
ed during screening tests, the distribution of sample 
sources in the clinically ill subgroup was significantly 
(P = 0.006) differerent, with most samples having 
been obtained from other sources, such as bone biop-
sy specimens (3/61 [5%]) or abscess aspirate samples 
(6/61 [10%]), for diagnostic purposes.
Distributions of subspecies of S enterica isolated 
from clinically ill reptiles differed from those isolated 
from the overall study population. Proportions of iso-
lates belonging to each subspecies for clinically ill rep-
tiles varied (Table 3). Individual species distribution 
was generally similar to that in the overall Salmonella-
positive population.
The 2 strongest risk factors for obtaining positive 
Salmonella culture result from a clinically ill (vs non–
clinically ill) reptile were diet type and origin (Table 4). 
Carnivores with a positive result had a significantly (P 
< 0.001) greater risk of clinical illness (RR, 4.61; 95% CI, 
2.10 to 10.10) than did noncarnivores. Confiscation was 
also associated with a significantly (P < 0.001) greater 
risk of clinical illness than were other sources of origin 
(RR, 2.03; 95% CI, 1.42 to 2.90). Snakes with a positive 
culture result had a significantly (P = 0.04) greater risk 
of clinical illness than did other reptile groups with a 
positive culture result (RR, 1.57; 95% CI, 1.03 to 2.39); 
lizards had a significantly (P = 0.03) lower risk of clini-
cal illness (RR, 0.55; 95% CI, 0.32 to 0.98).
Characterization of antimicrobial 
susceptibility patterns of Salmonella isolates
Results of full antimicrobial susceptibility testing 
were available for 116 (66%) Salmonella isolates per-
Reptile family Genus Proportion Percentage (95% CI)
Lizard 56/1,672 16 (15–18)
 Agamidae Chlamydosaurus 20/115 18 (11–25)
 Pogona 11/117 9 (4–13)
 Uromastyx 13/93 14 (7–21)
 Anguidae Ophisaurus 9/45 20 (8–32)
 Crotaphytidae Crotaphytus 63/253 25 (20–30)
 Gekkonidae Phelsuma 39/326 12 (8–16)
 Uroplatus 137/325 42 (34–50)
 Gerrhosauridae Zonosaurus 27/159 17 (11–23)Helodermatidae Heloderma 10/115 9 (4–14)
 Iguanidae Cyclura 18/92 20 (12–28)
 Sauromalus 8/190 4 (1–7)
 Opluridae Oplurus 12/146 8 (4–12)
 Pygopodidae Lialis 155/194 80 (74–86)
 Scinicidae Corucia 22/731 3 (2–4)
 Varanidae Varanus 427/2,247 19 (17–21)
 
 Snake 
 Boidae Boa 21/192 11 (7–15)
 Corallus 17/43 40 (25–55)
 Epicrates 32/112 29 (21–38)
 Eunectes 45/140 32 (25–40)
 Colubridae Drymarchon 6/67 9 (2–16)
 Elaphe 28/87 32 (22–42)
 Erpeton 7/133 5 (1–9)
 Gonyosoma 15/167 9 (5–13)
 Lampropeltis 7/43 17 (6–28)
 Leioheterodon 4/16 25 (4–46)
 Pituophis 7/48 14 (5–23)
 Elapidae Naja 7/145 5 (1–9)
 Ophiophagus 2/48 3 (0–8)
 Pythonidae Morelia 60/106 57 (50–64)
 Python 24/174 14 (9–19)
 Viperidae Agkistrodon 48/141 34 (26–42)
 Bitis 26/36 71 (57–86)
 Crotalus 31/123 25 (17–33)
 Protobothrops 3/34 9 (0–19)
 Sistrurus 2/6 33 (0–70)
Table 2—Distribution of reptiles of squamate genera (lizards [n = 59] and snakes [78]) per popu-
lation year with positive results of Salmonella culture at the Bronx Zoo from 2000 through 2012.
 JAVMA • Vol 248 • No. 9 • May 1, 2016 1055
Zoo Animals
Reptile group enterica salamae Untypable III arizonae diarizonae houtenae Other 
Crocodilian 4 (0) — — — — — 1(0)
 Alligatoridae — — — — — — — 
 Crocodylidae — — — — — — — 
 
Chelonian 16 (8) — — — 2 (0) — 3 (2)
 Emydidae 1 (0) — — — 1 (0) — 1 (1)
 Geomydidae — — — — — — 1 (1)
 Testudinidae 15 (8) — — — 1 (0) — — 
 
Lizard 28 (9) 3 (1) 6 (0) — 7 (2) 4 (0) 9 (1)
 Agamidae 4 (2) 1 (0) — — — 1 (0) —
 Anguidae — — — — — 1 (0) —
 Crotaphytidae 1 (1) — — — — — —
 Gekkonidae 1 (0) — 3 (0) — 3 (0) 2 (0) 5 (0)
 Gerrhosauridae — — — — — — 1 (0)
 Helodermatidae — 1 (1) — — — — —
 Iguanidae 2 (0) 1 (0) — — — — —
 Opluridae — — 1 (0) — 1 (0) — —
 Pygopodidae 7 (1) — — — 1 (1) — —
 Scincidae — — — — — 1 (0) —
 Varanidae 13 (5) — 2 (0) — 2 (1) — 3 (1)
 
Snake 30 (8) — 11 (9) 10 (1) 33 (17) 9 (5) 5 (3)
 Boidae 13 (3) — — 3 (0) 11 (9) 1 (0) 1 (0)
 Colubridae 5 (2) — 5 (4) 3 (0) 4 (2) — 2 (1)
 Elapidae 2 (1) — — — 3 (2) — —
 Pythonidae 2 (0) — 5 (4) — 3 (2) 1 (0) 1 (1)
 Viperidae 8 (1) — 1 (1) 4 (1) 12 (2) 7 (5) 1 (1)
— = No isolates of this subspecies recovered.
Table 3—Numbers of isolates of particular Salmonella subspecies recovered from all reptiles and from clinically ill reptiles alone 
(parentheses) at the Bronx Zoo from 2000 through 2012.
 No. (%) of all No. (%) of ill
Factor Individuals individuals RR (95% CI) P value
Origin 
 Dealer 49 (27) 15 (31) 0.80 (0.08–4.6) 0.45
 Confiscation 38 (21) 23 (63) 2.03 (1.5–3.1) < 0.001
 Captivity 35 (19) 12 (34) 1.10 (0.6–1.4) 0.72
 Private donation 38 (21) 10 (29) 0.70 (0.4–1.2) 0.23
 Wild 4 (2) 1 (25) — —
 Unknown 18 (10) 3 (17) — —
 
Point of sample collection 
 Quarantine 88 (48) 24 (28) 0.64 (0.3–0.8) 0.04
 After quarantine 54 (30) 28 (54) 1.66 (1.2–2.9) 0.006
 Unknown 40 (22) 12 (30) — —
 
Diet type 
 Carnivore 130 (71) 58 (46) 4.61 (1.8–8.4) < 0.001
 Omnivore 7 (4) 3 (43) — —
 Insectivore 15 (8) 3 (20) — —
 Herbivore 30 (17) 0 (0) 0.030 (0.0–0.5) 0.01
 
Sample type 
 Fecal 136 (75) 31 (48) 0.32 (0.2–0.5) < 0.001
 Nonfecal 46 (25) 33 (52) 3.57 (2.2–4.5) < 0.001
For calculations of RR, the referent group was the group of reptiles lacking the indicated factor. 
See Table 2 for remainder of key.
Table 4—Associations of various factors with clinical illness (vs no clinical illness) in reptiles with 
positive Salmonella culture results at the Bronx Zoo from 2000 through 2012.
1056 JAVMA • Vol 248 • No. 9 • May 1, 2016
Zoo Animals
taining to 121 reptiles. Antimicrobial resistance was 
uncommon, with a mean of > 90% of isolates suscep-
tible to most antimicrobials (Table 5). Only 7 isolates 
were multidrug resistant, with resistance to penicillins 
and cephalosporins; partial resistance to tetracyclines, 
ticarcillin, gentamicin, and trimethoprim-sulfamethox-
azole; and intermediate resistance to enrofloxacin and 
orbifloxacin. These isolates had similar antimicrobial 
susceptibility patterns, with 5 isolates pertaining to 
specimens collected within the same 5-month period, 
all of which were from confiscated chelonians in the 
family Testudinidae. Four of the 5 isolates were iden-
tified as Salmonella Potsdam, constituting the only 
representatives of this serovar in the study. Each of 
the 4 isolates originated from different members of 
a group of Chelonians of genus Pyxis that had been 
confiscated at the same time. The fifth isolate in this 
cluster was identified as Salmonella Newport and had 
been recovered from a group sample from Burmese 
star tortoises (Geochelone platynota).
Two additional isolates of multidrug-resistant Sal-
monella spp had similar but not identical susceptibili-
ty patterns. Both had been cultured from fecal samples 
obtained from apparently healthy reptiles, and both 
were recovered > 1 year after the original cluster of 
5 multidrug-resistant isolates had been identified. One 
isolate was from an emerald monitor (Varanus pras-
nius), and serotyping was not possible. The second 
was from a Western diamondback rattlesnake (Crota-
lus atrox) and was typed as Salmonella Muenchen.
Discussion
Salmonella carriage or infection was prevalent in 
both apparently healthy animals and clinically ill cap-
tive reptiles at the Bronx Zoo in the present study. The 
percentage of cultures from reptiles with clinical signs 
of disease that yielded salmonellae (37%) was higher 
than expected. Although S enterica serovars were as-
sociated with clinical illness in this particular reptile 
population, its role as a primary pathogen remains 
unclear.
The ability of salmonellae to serve as primary 
pathogens in snakes has been established.3,19,29,34,35,45–47 
For reptiles with positive Salmonella culture results 
in the present study, some of the clinical signs most 
commonly observed were consistent with those of 
other studies17,19 and of the established clinical signs 
of salmonellosis in reptiles, such as bony changes, 
weight loss, and lethargy. Other clinical signs, such as 
dermatitis and gastrointestinal parasitism, may have 
been related to debilitation, which is common in ill 
reptiles. Although nearly two-thirds of all biological 
samples with a positive culture result had been ob-
tained from apparently healthy reptiles, the number of 
ill individuals with positive Salmonella culture results 
was considerable.
Because the present study focused on reptiles 
with positive Salmonella culture results rather than 
on all reptiles at the Bronx Zoo, analyses to identify 
risk factors for Salmonella carriage could not be per-
formed, but risk factors associated with (vs without) 
clinical illness at the point of a positive culture result 
could be and were identified. Reptile group (with an 
increased risk for snakes and decreased risk for liz-
ards), diet type, and origin and source and collection 
point of biological samples were all important. Many 
of these risk factors were clinically relevant. 
A confiscated reptile with a positive Salmonella 
culture result was more likely to be ill than a noncon-
fiscated reptile. Confiscated reptiles housed at the 
Bronx Zoo often come from illegal trade and arrive 
dehydrated and otherwise compromised. Dehydration 
can reinitiate shedding of salmonellae in chelonian 
species.43 Whether this shedding results from altera-
tions in immune function or directly from changes in 
the gastrointestinal tract that result from dehydration 
is undetermined but may be important in other rep-
tile groups and in the Bronx Zoo reptile population. 
Many confiscated reptiles in the present study devel-oped disease associated with a positive Salmonella 
culture result years after the related sample had been 
collected, although reptiles in the quarantine period, 
regardless of origin, had a decreased risk of illness. 
These findings suggested that the factors underlying 
the association between confiscation and increased 
risk of illness at point of a positive culture result were 
more complex than simply immune alterations caused 
by transport and stress or that transport and its associ-
ated stressors may have more lasting effects on reptil-
ian immune function than suspected.
Other environmental factors, including diet and 
housing, have been identified as potential risk factors 
for Salmonella shedding by reptiles.26,34,37,48 Carnivo-
rous diet had a close association with illness at the 
point of a positive culture result in the reptiles of the 
present study. Snakes, a reptile group with an increased 
Antimicrobial Percentage susceptible*
β-Lactams 
 Penicillins 93.1–94.8
 Cephalosporins 28.4–98.6
 Potentiated β-lactams 94.0–94.8
 
Aminoglycosides 96.6–100
Fluoroquinolones 83.5–100
Tetracyclines 91.3–100
Sulfonamides 76.2–96.6
Macrolides 0.0
 
Lincomycin 0.0
Chloramphenicol 97.1
Carboxypenem 99.1
Rifamycin 0.0
*Reported ranges pertain to multiple antimicrobials within a given 
class.
Table 5—Percentage of all Salmonella isolates (n = 116) recov-
ered from reptiles at the Bronx Zoo from 2000 through 2012 
with susceptibility to various antimicrobials.
 JAVMA • Vol 248 • No. 9 • May 1, 2016 1057
Zoo Animals
risk for illness at time of a positive Salmonella culture 
result relative to other groups, are obligate carnivores. 
Other carnivorous reptiles, such as varanid lizards, had 
a relatively high proportion of ill individuals with a 
positive culture result, whereas most herbivorous liz-
ard families had a relatively low proportion. Previous 
studies37,48 in which mice and other dietary sources 
were investigated as a potential origin for salmonellae 
in reptiles revealed a lack of a direct association. 
Enclosure size and usage are other husbandry 
variables that have not been well explored but could 
contribute to the risk of reinfection in captive settings. 
Enclosure characteristics were not investigated for as-
sociations with outcome in the present study, and the 
risk for reinfection because of environmental contami-
nation or housing with a Salmonella carrier could be 
expected to increase the risk of Salmonella expo-
sure. Enclosure characteristics were inconsistently re-
corded to allow assessment, which represents a study 
limitation. Future studies should include comparison 
of captive and natural environments and evaluation of 
enclosure and other husbandry variables.
In other studies29–31,34,36,37,45,49–54 of captive rep-
tile populations, prevalence estimates for Salmonella 
carriage have differed widely (2% to 55% in cheloni-
ans, < 5% in crocodilians, 36% to 84% in lizards, 28% 
to 100% in snakes, and 22% to 76% in entire reptile 
populations). In the present study, the prevalence of 
positive Salmonella culture results was lower in liz-
ards (16.5%) and snakes (17.5%) than in the aforemen-
tioned studies. Numerous possible explanations exist 
for these discrepancies, including true differences in 
prevalence among captive populations and differenc-
es in testing methods and sensitivities.55 In the pres-
ent study, the same testing methods were used consis-
tently throughout the sample collection period.
Husbandry factors, such as whether a natural or 
captive climate is provided, have been hypothesized to 
be risk factors for Salmonella carriage and reinfection. 
One study48 revealed that reptiles from an arid natural 
environment may be more susceptible to reinfection 
when housed in a less arid captive enclosure. A similar 
pattern was not identified in the present study. Snake 
genera with the highest prevalence of positive Salmo-
nella culture results were largely semiaquatic, most 
notably in the families Boidae (Corallus, Epicrates, and 
Eunectes) and Viperidae (Agkistrodon and Bitis). Not 
all semiaquatic or tropical species had a high preva-
lence; the aquatic genus Erpeton and tropical genus 
Gonyosoma both had a relatively low prevalence. Mul-
tiple genera of lizards naturally found in arid climates 
(Heloderma, Oplurus, Pogona, and Sauromalus) had 
the lowest prevalence of positive Salmonella culture 
results. No similar environmental or natural history fac-
tor was identified between the 2 lizard genera with the 
highest prevalence (the arboreal tropical Uroplatus 
and the ground-dwelling temperate Lialis).
Serovar distribution among the subspecies of 
S enterica in the present study was uneven, with a 
higher prevalence of serovars from subspecies diari-
zonae (IIIb), houtenae (IV), and arizonae (IIIa) than 
from other subspecies. Although subspecies arizonae 
(IIIa) has already been identified in reptile species, 
particularly snakes,3,29,45,56 and numerous serovars 
of S enterica subsp enterica (I) have been isolated 
from all reptile groups,25,26,29,33,51,52,54,57–62 particularly 
turtles,15,43,53,63,64 the high prevalence of serovars from 
subspecies diarizonae (IIIb) and houtenae (IV) in 
the present study was unique. These 2 serovars were 
important in this study population, particularly when 
considering the likelihood of serovars of these sub-
species to be associated with illness.24,28,30,37,38,50,62,65 
Serovars from S enterica subsp enterica (I), the most 
common subspecies associated with human dis-
ease,4,21,66 were identified in samples from all reptile 
taxa in the present study. Many of the Salmonella en-
terica serovars linked to reptile-associated salmonel-
losis in humans were also identified in the reptiles, 
including serovars Pomona, Poona, Typhimurium, 
I 4,[5],12:i:–, and IV 44:z24,z23:–.8,18,25,61 Distribution 
of serovars among O antigen serogroups was similar 
to that in another study16 in which certain O antigen 
serogroups, particularly serogroups other than B and 
D, were evaluated for an association with reptiles.
Information regarding serovar contributes only par-
tially to evaluations of the epidemiology of Salmonella 
infection or carriage. Serotyping remains common in 
veterinary medicine, although alternative techniques 
that rely on genetic rather than phenotypic characteriza-
tion20 may provide more valuable epidemiological data 
in a collection such as the reptiles in the study reported 
here. Such evaluation was not possible given the avail-
able study data, but use of these techniques in a prospec-
tive study may further contribute to our understanding. 
The relatively low period prevalence of positive 
Salmonella culture results in the present study, com-
pared with point prevalence estimates from other 
studies involving similar reptiles, could be attributed 
to opportunistic rather than routine testing. Frequency 
of sample collection changed substantially in the last 5 
years of the study as the frequency of quarantine test-
ing decreased at the Bronx Zoo. Prevalence estimates 
reported here may also have been imprecise because of 
the retrospective population counts, which may have 
introduced a minimal degree of inaccuracy, and group 
sample collection, whereby 2 or more individuals could 
have contributed feces to a single sample. Pooled fecal 
samples are often used in reptile prevalence studies to 
reduce the frequency of sample collection and testing, 
but such collection methods can reduce the accuracy 
of calculations in that only 1 individual from the group 
could have been shedding salmonellae but the positive 
result would represent the whole group. Selection bias 
may have influenced the lower risk of a fecal sample 
from a quarantined, clinically ill (vs non–clinically ill) 
reptile yielding a positive Salmonellaculture result, giv-
en that samples were more likely to be collected from 
a source or particular individual if illness was observed.
The veterinary literature14,64 currently recommends 
against treatment of Salmonella infection or carriage 
in reptiles unless a reptile is clinically ill. At the Bronx 
Zoo, antimicrobial treatment has been directed by anti-
1058 JAVMA • Vol 248 • No. 9 • May 1, 2016
Zoo Animals
microbial susceptibility results, but empirical treatment 
of a clinically ill reptile before results are received often 
included ceftazidime (a first-line antimicrobial in reptile 
medicine not included in the antimicrobial susceptibili-
ty panel), amikacin, or enrofloxacin. Antimicrobial treat-
ment has not been highly successful for most ill reptiles 
at the Bronx Zoo or in the literature.3,46 A Taylor’s cantil 
(Agkistrodon bilineatus taylori) with osteomyelitis 
that was treated with amikacin delivered via osmotic 
pump reportedly had cessation but not reversal of le-
sions for the 10-month treatment period, and the dis-
ease recurred when treatment stopped.67 Antimicrobial 
resistance occurs in salmonellae, although multidrug 
resistance was uncommon in the present study be-
yond the expected pattern for gram-negative bacteria 
of resistance to clindamycin, erythromycin, penicillin, 
and rifampin. Overinterpretation of resistance patterns 
is possible when interpreters fail to consider the char-
acteristics of the gram-negative bacteria and family En-
terobacteriaceae.54,56,59,68
Findings of the present study underscored the im-
portance of salmonellae as potential pathogens in cap-
tive reptile collections. Salmonella spp were detected 
in a third of all snake fecal samples and in biological 
samples from 15% to 20% of squamates. Clinical illness 
was evident in a third of reptiles with positive Salmo-
nella culture results. Even though these data supported 
the notion that salmonellae are a typical component of 
reptilian intestinal flora, the detected period prevalence 
was higher than predicted for this captive population. 
Certain risk factors for illness associated with positive 
Salmonella culture results were identified, including 
snake suborder, carnivorous diet, and confiscation, but 
these factors did not account for all reptiles at risk for 
developing clinical illness. The difficulties in identifying 
high-risk reptiles, coupled with the insidious nature of 
this pathogen, prevent a complete understanding of 
the epidemiology of Salmonella infection or carriage 
in reptile collections. Careful assessment of husbandry 
factors should be considered in future investigations of 
risk factors for Salmonella carriage and disease, which 
would be best performed in a prospective study with a 
similar setting. Treatment of salmonellosis in reptiles is 
often unsuccessful but should be guided by results of 
antimicrobial susceptibility testing.
Acknowledgments
This manuscript represents a portion of a capstone project 
submitted by Dr. Clancy to the Johns Hopkins Bloomberg School of 
Public Health as partial fulfillment of the requirements for a Master 
of Public Health degree.
Presented in abstract form at the 45th Annual Meeting of the 
American Association of Zoo Veterinarians, Salt Lake City, October 2013.
The authors thank Jean Lay and Dr. Kimberly Rainwater for 
data collection and collation, Dr. Shelley Rankin for subject-matter 
expertise, and Dr. Pat McDonough for sample testing and initial data 
compilation.
Footnotes
a. BBL Port-A-Cul specimen collection and transport products, 
Becton Dickinson, Franklin Lakes, NJ.
b. Sensititre automated microbiology system A80 panel, TREK Di-
agnostic Systems, Cleveland, Ohio.
c. MedARKS, International Species Information System, Bloom-
ington, Minn.
d. Stata, version 12, StataCorp, College Station, Tex.
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