Publications by authors named "Laura Adamovicz"

32 Publications

BLOOD LACTATE CONCENTRATIONS IN EASTERN BOX TURTLES () FOLLOWING CAPTURE BY A CANINE SEARCH TEAM.

J Zoo Wildl Med 2021 Apr;52(1):259-267

Wildlife Epidemiology Laboratory, College of Veterinary Medicine, University of Illinois, Urbana, Illinois 61802, USA,

Studies to assess wildlife health commonly evaluate clinical pathology changes, immune responses, pathogen presence, and contaminant exposure, but novel modalities are needed to characterize the unique physiologic responses of reptiles. Lactate is an indicator of hypoperfusion and/or anaerobic respiration and can be quickly and easily measured using a point-of-care analyzer. This study evaluated baseline blood lactate concentrations in free-living eastern box turtles (, = 116) using a point of care analyzer and then determined the effect of handling time, physical examination (PE) abnormalities, and quantitative polymerase chain reaction pathogen detection ( herpesvirus 1, sp., adenovirus) on lactate concentrations. Blood lactate concentrations were higher in turtles with herpesvirus 1 ( = 11), quiet mentation, and increased packed cell volume ( < 0.05). Lactate concentrations increased between initial capture and PE, with peak values reaching 129 min after capture. Lactate at PE was positively associated with baseline lactate concentrations. Turtles with herpesvirus 1 may have alterations in blood flow, oxygen delivery, or activity patterns, driving increases in baseline lactate. Increased handling time likely leads to more escape behaviors and/or breath holding, causing turtles to undergo anaerobic metabolism and raising lactate concentrations. Overall, lactate measured by a point of care analyzer shows variability caused by capture and health factors in eastern box turtles and may be a useful adjunctive diagnostic test in this species after full methodologic validation.
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http://dx.doi.org/10.1638/2020-0071DOI Listing
April 2021

Ultraviolet Fluorescence as a Field-Applicable Screening Tool for Lesions Consistent with Ophidiomycosis in Lake Erie Watersnakes (Nerodia sipedon insularum).

J Wildl Dis 2021 04;57(2):380-385

Wildlife Epidemiology Lab, College of Veterinary Medicine, University of Illinois at Urbana-Champaign, 2001 S Lincoln Ave., Urbana, Illinois 61802, USA.

Ophidiomycosis, commonly called snake fungal disease, has been linked to significant morbidity of free-ranging snakes in North America and Europe. Diagnosis of ophidiomycosis currently requires detection of skin lesions via physical exam or characteristic histopathology as well as detection of the causative agent, Ophidiomyces ophidiicola, through quantitative (q)PCR or fungal culture of a skin swab or tissue sample. While reliable, these methods require specialized training, invasive procedures (e.g., biopsy), and several days or weeks to receive results. Additionally, screening entire populations can quickly become costly. A fast, easy-to-use, cost-efficient, and sensitive screening tool is needed to optimize conservation strategies and treatment intervention. Our objective was to investigate the association between skin fluorescence under long-wave ultraviolet (UV) light (365 nm) and the detection of Ophidiomyces ophidiicola DNA using qPCR. Fifty-eight Lake Erie watersnakes (Nerodia sipedon insularum) collected in June of 2018 and 2019 from islands in western Lake Erie, Ottawa County, Ohio, US were visually inspected for skin lesions, photographed under natural light and UV light, and swabbed for qPCR analysis. Fluorescence was highly associated with the presence of skin lesions, and the presence of at least one fluorescent skin lesion was 86% sensitive and 100% specific for identifying animals with apparent ophidiomycosis, with a positive predictive value of 100%. While we recommend performing standard diagnostics along with fluorescence, our study supports the use of visual UV fluorescence identification as a preliminary, affordable, noninvasive, and field-applicable method to screen populations for ophidiomycosis.
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http://dx.doi.org/10.7589/JWD-D-20-00013DOI Listing
April 2021

Detection of a novel herpesvirus associated with squamous cell carcinoma in a free-ranging Blanding's turtle.

J Vet Diagn Invest 2021 Mar 23;33(2):348-351. Epub 2021 Jan 23.

Wildlife Epidemiology Laboratory, College of Veterinary Medicine, University of Illinois-Urbana, IL.

The spread of both infectious and noninfectious diseases through wildlife populations is of increasing concern. Neoplastic diseases are rarely associated with population-level impacts in wildlife; however, impacts on individual health can be severe and might reflect deteriorating environmental conditions. An adult male free-ranging Blanding's turtle () originally captured in 2005 and deemed healthy, was recaptured in 2018 with a 1 × 1.5 cm intra-oral broad-based right mandibular mass. An excisional biopsy was performed, and histopathology revealed squamous cell carcinoma (SCC). Consensus herpesvirus PCR identified a novel herpesvirus (proposed name herpesvirus 2 [EBHV-2]) within the tumor. EBHV-2 shares 85% sequence homology with herpesvirus 2 (TerHV-2), a herpesvirus linked to fibropapillomas in eastern box turtles (). Virus-associated fibropapillomas have been identified in multiple marine turtle species and have had debilitating effects on their populations, but to date, virus-associated SCCs are rarely reported.
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http://dx.doi.org/10.1177/1040638721989302DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7953097PMC
March 2021

COMPARING THE EFFECTS OF LITHIUM HEPARIN AND DIPOTASSIUM ETHYLENEDIAMINETETRAACETIC ACID ON HEMATOLOGIC VALUES IN EASTERN BOX TURTLES ().

J Zoo Wildl Med 2021 Jan;51(4):999-1006

Wildlife Epidemiology Laboratory, College of Veterinary Medicine, University of Illinois, Urbana, IL 61802, USA,

Anticoagulants are employed to prevent clotting and preserve cellular morphology for clinical pathology tests. Lithium heparin (LH) is the most frequently used anticoagulant in chelonians; however, dipotassium ethylenediaminetetraacetic acid (EDTA) may be superior in some species. Although eastern box turtles' () hematologic parameters are well studied, the effects of different anticoagulants on hematology in this species are unknown. This study evaluated the effects of LH and EDTA on hematologic values in free-living eastern box turtles ( = 59). Blood samples were collected from eastern box turtles in Illinois and immediately divided between LH and EDTA microtainers, and complete blood counts were performed on each sample. Grossly, plasma from EDTA blood samples was frequently and significantly hemolyzed. Blood mixed with LH had higher packed cell volume (PCV) ( = 0.04), white blood cell count (WBC) determined by Leukopet ( < 0.0001), WBC determined by blood film estimate ( < 0.0001), absolute heterophils ( = 0.007), absolute lymphocytes ( < 0.0001), and lower total solids ( < 0.0001) and absolute monocytes ( = 0.0001) than blood mixed with EDTA. All relative leukocyte counts were significantly different between the anticoagulants ( < 0.0001). EDTA apparently lysed turtle erythrocytes in this study, making it difficult to accurately count white blood cells and artificially lowering PCV. These findings demonstrate that EDTA should not be used in eastern box turtles.
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http://dx.doi.org/10.1638/2020-0109DOI Listing
January 2021

CHARACTERIZING THE EPIDEMIOLOGY OF HISTORIC AND NOVEL PATHOGENS IN BLANDING'S TURTLES ().

J Zoo Wildl Med 2020 Nov;51(3):606-617

University of Illinois Wildlife Epidemiology Laboratory, Urbana, Illinois 61802, USA,

Pathogens such as herpesviruses, spp., and frog virus 3-like ranavirus have contributed to morbidity and mortality in many species of free-living and zoo-maintained chelonians. However, their prevalence is understudied in Blanding's turtles () across North America. To assess the presence of these pathogens, Blanding's turtles were sampled in Lake County, Illinois, in 2017 ( = 213) and 2018 ( = 160). DNA from cloacal-oral swabs was assayed for four ranaviruses, three spp., two spp., herpesvirus 1 (EBHV1), and tortoise intranuclear coccidiosis (TINC) using a multiplex quantitative polymerase chain reaction (qPCR). Pathogens were most frequently detected in adult turtles ( = 25) and rarely in subadults ( = 2) or juveniles ( = 1). EBHV1 was detected in 22 individuals with no clinical signs of illness, most ( = 20) occurring in the month of May ( < 0.0001). EBHV1 cases at one study site significantly clustered within the same 0.64-km area from 17 to 22 May 2017 ( < 0.0001) and 14 to 15 May 2018 ( = 0.0006). Individuals were rarely positive for ( = 6). A novel sp. sharing high homology with other emydid spp. was detected in one turtle with nasal discharge. Neither TINC nor any ranaviruses were detected. Continued monitoring of this population and habitat may facilitate identification of risk factors for pathogen occurrence and clarify the impact of infectious diseases on Blanding's turtle conservation outcomes.
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http://dx.doi.org/10.1638/2019-0154DOI Listing
November 2020

Plasma complement activation mechanisms differ in ornate (Terrapene ornata ornata) and eastern box turtles (Terrapene carolina carolina).

J Exp Zool A Ecol Integr Physiol 2020 12 19;333(10):720-731. Epub 2020 Oct 19.

Wildlife Epidemiology Laboratory, University of Illinois College of Veterinary Medicine, Urbana, Illinois, USA.

Eastern (Terrapene carolina carolina) and ornate (Terrapene ornata ornata) box turtles have robust plasma antibacterial activity, however, the mechanism behind this activity is unknown. We used sheep red blood cell (SRBC) hemolysis assays, mannan-affinity chromatography, sodium dodecyl sulfate polyacrylamide gel electrophoresis (SDS-PAGE), and matrix-assisted laser desorption ionization time-of-flight (MALDI-TOF) to explore the mechanisms of complement activity in box turtles. Plasma from both species demonstrated volume, time, and temperature-dependent SRBC hemolysis, with significantly greater hemolytic activity in ornate box turtle plasma. Hemolytic activity was highly attenuated following treatment with heat, EDTA, and salicylaldoxime in both species, but was unchanged after treatment with methylamine and ammonium hydroxide. Two abundant mannan-binding proteins (presumed C-type lectins) were identified in eastern box turtle plasma using SDS-PAGE and MALDI-TOF, but ornate box turtles did not express either protein. Eastern box turtles appear to rely on the lectin pathway of complement activation while ornate box turtles utilize the alternative pathway. This study provides further evidence that mechanisms underlying immune function are not always conserved between closely related species. This finding may have important implications for explaining species differences in susceptibility to emerging threats such as disease, toxicants, and climate change.
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http://dx.doi.org/10.1002/jez.2423DOI Listing
December 2020

Publisher Correction: Ophidiomycosis surveillance of snakes in Georgia, USA reveals new host species and taxonomic associations with disease.

Sci Rep 2020 09 16;10(1):15362. Epub 2020 Sep 16.

Wildlife Epidemiology Laboratory, College of Veterinary Medicine, University of Illinois at Urbana-Champaign, Urbana, IL, USA.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.
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http://dx.doi.org/10.1038/s41598-020-69878-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7495465PMC
September 2020

Development and validation of a quantitative PCR assay for detection of Terrapene herpesvirus 2 in eastern box turtles (Terrapene carolina carolina).

J Virol Methods 2020 12 7;286:113968. Epub 2020 Sep 7.

Wildlife Epidemiology Laboratory, College of Veterinary Medicine, University of Illinois, 2001 S. Lincoln Ave., Urbana, IL, 61802, United States; Veterinary Diagnostic Laboratory, College of Veterinary Medicine, University of Illinois, 2001 S. Lincoln Ave., Urbana, IL, 61802, United States. Electronic address:

Herpesviruses are associated with disease in many chelonian species, resulting in pathology such as respiratory tract infection, stomatitis, conjunctivitis, hepatitis, and papillomatosis. Herpesvirus-associated fibropapillomas cause significant morbidity and mortality in marine turtles, and have been identified in an eastern box turtle (Terrapene carolina carolina) infected with Terrapene herpesvirus 2 (TerHV2). Further investigation is necessary to understand the impact of carcinogenic herpesviruses on chelonian health; however, reliable and specific methods for detection and quantitation of herpesviral load are lacking. The purpose of this study was to develop and validate a quantitative PCR assay for detection of TerHV2 in box turtles. TaqMan primer-probes were developed targeting the DNA polymerase gene. Inter- and intra-assay variability, linear range of detection, limit of detection, and specificity were assessed. The assay was highly specific for TerHV2, failing to amplify seven closely-related chelonian herpesviruses. It performed with high efficiency (slope = -3.52, R = 1, efficiency = 92.29 %), low intra-assay variability and low inter-assay variability (coefficient of variation ≤ 1.25 % at all standard dilutions). Reaction efficiency was not impacted in the presence of box turtle DNA from combined oral/cloacal swabs or whole blood. This qPCR assay has a linear range of detection from 10 to 10 viral copies per reaction and provides a valuable tool in the surveillance and characterization of TerHV2 in box turtles.
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http://dx.doi.org/10.1016/j.jviromet.2020.113968DOI Listing
December 2020

Ophidiomycosis surveillance of snakes in Georgia, USA reveals new host species and taxonomic associations with disease.

Sci Rep 2020 07 2;10(1):10870. Epub 2020 Jul 2.

Wildlife Epidemiology Laboratory, College of Veterinary Medicine, University of Illinois at Urbana-Champaign, Urbana, IL, USA.

Ophidiomycosis (snake fungal disease) is caused by the fungus Ophidiomyces ophiodiicola and threatens snake health worldwide. It has been documented throughout the eastern United States and severe cases have recently been reported in Georgia, USA. To evaluate disease distribution and prevalence in this state, 786 free-ranging snakes were examined for skin lesions consistent with ophidiomycosis and swabbed to detect O. ophiodiicola DNA using qPCR. Sampled snakes represented 34 species and 4 families; 27.5% had skin lesions, 13.3% were positive for O. ophiodiicola DNA, and 77.8% of the qPCR positive individuals had skin lesions. This is the first report of O. ophiodiicola in five of the 22 species that were qPCR positive. Multinomial logistic regression modeling indicated that Drymarchon couperi had a higher relative risk of apparent ophidiomycosis (lesions present and qPCR positive), and the best models predicting qPCR result and ophidiomycosis category included individual factors and excluded temporal and spatial factors. Phylogeny-based bipartite network analysis showed that Nerodia erythrogaster, Nerodia taxispilota, and D. couperi had the highest prevalence of apparent ophidiomycosis; this category was more prevalent in the subfamily Colubrinae and less prevalent in Natricinae. These results provide important information about ophidiomycosis epidemiology, which has implications for snake conservation.
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http://dx.doi.org/10.1038/s41598-020-67800-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7331741PMC
July 2020

Erythrocyte sedimentation rate and hemoglobin-binding protein in free-living box turtles (Terrapene spp.).

PLoS One 2020 17;15(6):e0234805. Epub 2020 Jun 17.

Wildlife Epidemiology Laboratory, University of Illinois, Urbana, Illinois, United States of America.

The acute phase response is a highly conserved reaction to infection, inflammation, trauma, stress, and neoplasia. Acute phase assays are useful for wildlife health assessment, however, they are infrequently utilized in reptiles. This study evaluated erythrocyte sedimentation rate (ESR) in eastern (Terrapene carolina carolina) and ornate box turtles (Terrapene ornata ornata) and hemoglobin-binding protein (HBP) in T. ornata. Erythrocyte sedimentation rate in 90 T. carolina and 105 T. ornata was negatively associated with packed cell volume and was greater in unhealthy turtles (p < 0.05). Female T. ornata had higher ESR values than males (p < 0.05). Measurement of ESR with a microhematocrit tube proportionally overestimated values from a commercial kit (Winpette), though both methods may retain utility with separate reference intervals. Hemoglobin-binding protein concentration in 184 T. ornata was significantly increased in adults and unhealthy turtles (p < 0.05). Erythrocyte sedimentation rate values were similar between seasons and populations, and HBP values were consistent between years, indicating that these analytes may have more stable baseline values than traditional health metrics in reptiles. This study demonstrates that ESR and HBP are promising diagnostics for health assessment in wild box turtles. Incorporating these tests into wild herptile health assessment protocols may support conservation efforts and improve ecosystem health monitoring.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0234805PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7299368PMC
August 2020

Emerging Infectious Diseases of Chelonians: An Update.

Vet Clin North Am Exot Anim Pract 2020 May;23(2):263-283

Avian and Exotic Veterinary Care, 7826 Northeast Sandy Boulevard, Portland, OR 97213, USA.

Chelonians are increasingly challenged by anthropogenic threats and disease. This article summarizes recent literature and clinical experiences regarding 4 emerging infectious diseases in turtles and tortoises: ranaviruses, cryptosporidiosis, intranuclear coccodiosis of Testudines, and Emydomyces testavorans.
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http://dx.doi.org/10.1016/j.cvex.2020.01.014DOI Listing
May 2020

Plasma antibacterial activities in ornate (Terrapene ornata) and eastern box turtles (Terrapene carolina).

J Exp Zool A Ecol Integr Physiol 2020 06 10;333(5):295-305. Epub 2020 Feb 10.

Wildlife Epidemiology Laboratory, University of Illinois College of Veterinary Medicine, Urbana, Illinois.

Chelonians are one of the most imperiled vertebrate taxa and many species are increasingly threatened by disease, however, the immune response in this group is understudied. We quantified the innate immune response of eastern (Terrapene carolina; EBT) and ornate (Terrapene ornate; OBT) box turtles using plasma antibacterial activity assays. Plasma from both species abolished or significantly reduced the growth of all eight bacterial species evaluated, including Salmonella typhimurium, Escherichia coli, Enterobacter cloacae, Citrobacter freundi, Bacillus subtilis, Staphylococcus epidermidis, and Staphylococcus aureus. Bactericidal capacity was greater in OBT compared to EBT, and OBT plasma retained high antibacterial activities at a broader temperature range (20-40°C) compared to EBT (30-40°C). Plasma antibacterial activity was abolished following treatment with heat, protease, and ethylenediaminetetraacetic acid, indicating that complement is likely responsible for the observed effects. Further characterization of the box turtle immune response may provide insight into the importance of infectious diseases for species conservation, enabling the development of more efficient and effective population management strategies.
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http://dx.doi.org/10.1002/jez.2352DOI Listing
June 2020

PREVALENCE OF BOX TURTLE ADENOVIRUS IN EASTERN BOX TURTLES () PRESENTED TO A WILDLIFE REHABILITATION CENTER IN VIRGINIA, USA.

J Zoo Wildl Med 2020 Jan;50(4):769-777

Wildlife Epidemiology Lab, Departments of Veterinary Clinical Medicine and Comparative Biosciences, College of Veterinary Medicine, University of Illinois, Urbana, Illinois 61802, USA.

Eastern box turtles () are a native North American species with a declining population trend that may be attributable to habitat fragmentation, vehicle collisions, and disease. Adenoviral infections can cause significant morbidity and mortality in captive reptile populations. Adenoviruses have been documented in box turtles, but their occurrence and impact in wild populations are unknown. A disease survey was performed at The Wildlife Center of Virginia, USA, to assess the prevalence of box turtle adenovirus (BTAdV) in wild eastern box turtles and evaluate potential associations with clinical disease. Swabs from the oral cavity, including the choanal slit, and the cloaca were collected from 106 eastern box turtles from July 2015 through June 2016. The quantitative polymerase chain reaction (qPCR) primer detected both ornate box turtle adenovirus 1 and eastern box turtle adenovirus. The resulting qPCR adenovirus prevalence was 55.7% ( = 59). Most animals (99.3%) that tested positive for BTAdV had fewer than 100 viral copies/ng DNA. This study did not find a statistically significant association between cause of admission, age, sex, outcome, and BTAdV qPCR status. However, the probability of BTAdV detection was 1.5 times higher in rehabilitation turtles compared with wild turtles ( = 0.01). Albumin was significantly lower in qPCR BTAdV-positive turtles ( = 0.007). Hypoalbuminemia is not generally associated with adenovirus infections in other species, and no obvious clinical cause for this abnormality was identified. The results of this study suggest that eastern box turtles may harbor BTAdV infections at low levels and that infection is rarely associated with clinical disease, potentially identifying BTAdV as a host-adapted pathogen. Future studies should focus on this pathogen's ability to induce clinical disease and its potential impact on recovery efforts for this species.
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http://dx.doi.org/10.1638/2018-0238DOI Listing
January 2020

Characterization of sp. Infection in a midwestern state-endangered salamander () and a co-occurring common species ().

Parasitology 2020 03 8;147(3):360-370. Epub 2020 Jan 8.

Wildlife Epidemiology Lab, University of Illinois, 2001 S Lincoln Ave, Urbana, IL61802, USA.

Ichthyosporean parasites (order Dermocystida) can cause morbidity and mortality in amphibians, but their ecology and epidemiology remain understudied. We investigated the prevalence, gross and histologic appearance, and molecular phylogeny of a novel dermocystid in the state-endangered silvery salamander (Ambystoma platineum) and the co-occurring, non-threatened small-mouthed salamander (Ambystoma texanum) from Illinois. Silvery salamanders (N = 610) were sampled at six ephemeral wetlands from 2016 to 2018. Beginning in 2017, 1-3 mm raised, white skin nodules were identified in 24 silvery salamanders and two small-mouthed salamanders from five wetlands (prevalence = 0-11.1%). Skin biopsy histology (N = 4) was consistent with dermocystid sporangia, and necropsies (N = 3) identified infrequent hepatic sporangia. Parasitic 18S rRNA sequences (N = 5) from both salamander species were identical, and phylogenetic analysis revealed a close relationship to Dermotheca viridescens. Dermocystids were not identified in museum specimens from the same wetlands (N = 125) dating back to 1973. This is the first report of Dermotheca sp. affecting caudates in the Midwestern United States. Future research is needed to determine the effects of this pathogen on individual and population health, and to assess whether this organism poses a threat to the conservation of ambystomatid salamanders.
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http://dx.doi.org/10.1017/S0031182019001677DOI Listing
March 2020

Investigating the Analytical Variability and Agreement of Manual Leukocyte Quantification Methods in Eastern Box Turtles ().

Front Vet Sci 2019 12;6:398. Epub 2019 Nov 12.

Wildlife Epidemiology Laboratory, College of Veterinary Medicine, University of Illinois, Urbana, IL, United States.

Leukogram evaluation provides valuable information about inflammation, infection, and stress in free-living and zoo-maintained wildlife. While multiple protocols for quantifying leukocytes are available in reptiles, agreement between methods is infrequently described and analytical variability (including repeatability and reproducibility) has not been critically evaluated. This study addresses these knowledge gaps for two hematological methods in eastern box turtles (): Avian Leukopet (LO) and total white blood cell (WBC) estimates from blood films (EST). The objectives of this study were (1) to evaluate agreement in total WBC and individual leukocyte counts between the LO and EST methods, (2) to document repeatability (intra-assay variability) and reproducibility (inter-assay variability) for the LO method, and (3) to investigate whether biological drivers of WBC counts differ between quantification methods. Box turtles ( = 120) were sampled from five study sites in Illinois during the 2018 active season. The LO method produced significantly higher WBC counts than the EST method, and constant and proportional error was variable for each leukocyte type. The LO method demonstrated an intra-assay variability of 8.2% and an inter-assay variability of 12%, independent of biological variation. WBC counts were significantly affected by age class using both LO and EST methods, but WBC differences between locations and sexes were only observed using the LO method. These findings emphasize the importance of considering leukocyte determination method when analyzing reptilian hematology results. The inherent variability in currently available methods creates uncertainty in resulting data and highlights the need of a gold standard for reptilian WBC quantification.
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http://dx.doi.org/10.3389/fvets.2019.00398DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6861175PMC
November 2019

MORTALITY INVESTIGATION OF MONITORED EASTERN BOX TURTLES () IN CENTRAL ILLINOIS, USA, FROM 2016-18.

J Wildl Dis 2020 04 21;56(2):306-315. Epub 2019 Nov 21.

Wildlife Epidemiology Laboratory, College of Veterinary Medicine at University of Illinois, Urbana-Champaign, 2001 S Lincoln Avenue, Urbana, Illinois 61802, USA.

Mortality events in eastern box turtles () threaten conservation efforts across the species range. These events are often under-diagnosed and, when observed, predictive health factors are unavailable prior to death. At Kickapoo State Park in central Illinois, USA, ranaviruses caused observed mortality events in amphibians and chelonians in 2014 and 2015. Following these outbreaks, eastern box turtles (=36) were affixed with radio transmitters and temperature data loggers to obtain repeated location and temperature data from spring 2016-spring 2018. Bimonthly, samples of blood and oral and cloacal swabs were collected to investigate health parameters (hematology and cytokine transcription) and presence of multiple pathogens. Deaths of instrumented turtles occurred in 2016 (=5), 2017 (=15), and 2018 (=2). The largest single die-off occurred in February 2017 (=7). Seventeen turtles were necropsied and multiple pathologic processes were identified, most frequently decreased adipose stores (=6). Two turtles had pathologic findings consistent with multisystemic inflammation. In addition, infectious pathogens were identified in turtles prior to death, but no single agent was associated with each mortality event. Ranavirus was not detected in any turtle. Hot spot analysis revealed spatial clustering at the center and edges of the study area for body temperature as well as for relative cytokine transcription of interleukin-1 beta, tumor necrosis factor alpha, and interleukin-10 associated with turtle death. Though no single causal factor could be identified, the information from this mortality event can direct future chelonian mortality investigations by providing baseline longitudinal data prior to death and in surviving turtles.
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April 2020

Hematology and plasma biochemistries in the Blanding's turtle (Emydoidea blandingii) in Lake County, Illinois.

PLoS One 2019 15;14(11):e0225130. Epub 2019 Nov 15.

Wildlife Epidemiology Laboratory, College of Veterinary Medicine, University of Illinois, Urbana, IL, United States of America.

Chelonians are one of the most imperiled vertebrate taxa on the planet due to changes in the environment, anthropogenic influences, and disease. Over the last two decades, conservation strategies including nest protection, head-starting and meso-predator control have been successfully adopted by the Lake County Forest Preserve District for a population of state-endangered Blanding's turtles (Emydoidea blandingii) in Illinois. Only recently have efforts expanded to assess the effects of management action on turtle health. The objectives of this study were to 1) establish reference intervals for 16 hematologic and plasma biochemical analytes in free-ranging Blanding's turtles, 2) characterize demographic and temporal drivers of clinical pathology values including age class, sex, month, and year, and 3) describe bloodwork differences between a managed (SBCP) and unmanaged (IBSP) study site. Hematology and plasma biochemistries were performed for 393 turtles from 2017-18 at two sites in the Lake Plain region. Subject or population-based reference intervals were established based on the index of individuality per American Society for Veterinary Clinical Pathology guidelines. Analytes differed by age class [packed cell volume (PCV), total solids (TS), total white blood cell counts (WBC), heterophils, lymphocytes, heterophil:lymphocyte ratio (H:L), total calcium (Ca), calcium:phosphorous (Ca:P), bile acids (BA), aspartate aminotransferase (AST)], sex [H:L, Ca, phosphorus (P), Ca:P, creatine kinase (CK)], month [eosinophils, H:L, Ca, P, uric acid (UA), AST], and year [PCV, WBC, lymphocytes, basophils, H:L, Ca, P, UA]. Several analytes also varied by site [PCV, TS, monocytes, eosinophils, P, UA, AST], suggesting that health status may be affected by habitat management or lack thereof. The results of this study provide a baseline for ongoing health assessments in this region as well as across the Blanding's turtle range.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0225130PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6857950PMC
March 2020

Assessment of hematologic and corticosterone response in free-living eastern box turtles (Terrapene carolina carolina) at capture and after handling.

Zoo Biol 2020 Jan 14;39(1):13-22. Epub 2019 Oct 14.

Institute for Conservation Medicine, Saint Louis Zoo, St. Louis, Missouri.

Hematology is a common tool for wildlife health assessments. Manual leukocyte counts are required in reptiles, however, disagreement between quantification methods has been observed in some chelonians. This study determined agreement between two methods of leukocyte quantification, eosinophilic leukopet, and blood film white blood cell (WBC) estimates, in free-living eastern box turtles (Terrapene carolina carolina). Simultaneously, we assessed the impact of handling duration on both leukocyte quantity and corticosterone levels. We collected blood at capture (<2 min from disturbance) and again before release 30-150 min later from 92 box turtles at six sites in Illinois and Tennessee. Constant and proportional error was present in the leukopet results for WBC, lymphocytes, and basophils compared to the estimate method. Both methods were in agreement for heterophils, monocytes, and eosinophils. Agreement between the methods was significantly more likely at WBC counts below 23,241/µl. All hematologic parameters were significantly higher at the final blood draw compared to the initial blood draw using both WBC determination methods, except relative eosinophil and basophil counts. Corticosterone levels varied with time, with maximum concentrations reached at 54 min postcapture, followed by a rapid return to baseline levels. Corticosterone level was not significantly associated with any hematologic parameter or sex. This study provides a framework for understanding the effects of animal handling methodology and diagnostic modality when evaluating hematologic health in box turtles.
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http://dx.doi.org/10.1002/zoo.21518DOI Listing
January 2020

FATAL RANAVIRUS INFECTION IN A GROUP OF ZOO-HOUSED MELLER'S CHAMELEONS ().

J Zoo Wildl Med 2019 Sep;50(3):696-705

Department of Molecular and Comparative Pathobiology, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA,

A group of five juvenile Meller's chameleons () experienced 100% mortality over a period of 1 mo due to ranavirus infection. The index case was found dead without premonitory signs. The three subsequent cases presented with nonspecific clinical signs (lethargy, decreased appetite, ocular discharge) and were ultimately euthanatized. The final case died after initially presenting with skin lesions. Postmortem examination revealed thin body condition in all five animals and mild coelomic effusion and petechiae affecting the tongue and kidneys of one animal. Microscopically, all animals had multifocal necrosis of the spleen, liver, and kidney; four of five animals had necrosis of the nasal cavity; and two of five had necrosis of adrenal tissue, bone marrow, and skin. Numerous basophilic intracytoplasmic inclusions were present in the liver of all animals and nasal mucosa of three of the five animals. Consensus polymerase chain reaction for herpesvirus and adenovirus were negative, whereas ranavirus quantitative polymerase chain reaction was positive. Virus isolation followed by whole genome sequencing and Bayesian phylogenetic analysis classified the isolates as a strain of frog virus 3 (FV3) most closely related to an FV3 isolate responsible for a previous outbreak in the zoo's eastern box turtle () group. This case series documents the first known occurrence of ranavirus-associated disease in chameleons and demonstrates the potential for interspecies transmission between chelonian and squamate reptiles.
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http://dx.doi.org/10.1638/2018-0044DOI Listing
September 2019

EPIDEMIOLOGY OF HERPESVIRUS 1 IN FREE-RANGING BLANDING'S TURTLES () FROM ILLINOIS.

J Zoo Wildl Med 2019 Sep;50(3):547-556

Department of Pathobiology, College of Veterinary Medicine, University of Illinois at Urbana-Champaign, Urbana, IL 61802, USA.

Herpesvirus infections have been associated with high morbidity and mortality in populations of captive emydid chelonians worldwide, but novel herpesviruses have also recently been identified in apparently healthy free-ranging emydid populations. Blanding's turtle (), an endangered species in Illinois, has experienced range-wide declines because of habitat loss, degradation, and fragmentation. A novel herpesvirus, herpesvirus 1 (EBHV1), was identified in Blanding's turtles in DuPage County, IL, in 2015. Combined oral-cloacal swabs were collected from radio transmitter-fitted and trapped ( = 54) turtles multiple times over the 2016 activity season. In addition, swabs were collected at a single time point from trapped and incidentally captured ( = 84) Blanding's turtles in DuPage ( = 33) and Lake ( = 51) counties over the same field season. Each sample was tested for EBHV1 using quantitative polymerase chain reaction (qPCR). EBHV1 was detected in 15 adult females for an overall prevalence of 10.8% ( = 15/138; 95% confidence interval [CI]: 6.2-17.3%). In radio transmitter-fitted females, there was a significantly higher prevalence of EBHV1 DNA in May (23.8%, = 10/42) than June (3.6%, = 1/28), July (0%, = 0/42), August (0%, = 0/47), or September (7.7%, = 3/39) (odds ratio: 12.19; 95% CI: 3.60-41.30). The peak in May corresponds to the onset of nesting and may be associated with increased physiologic demands. Furthermore, all positive turtles were qPCR negative in subsequent months. There were no clinical signs associated with EBHV1 detection. This investigation is the critical first step to characterizing the implications of EBHV1 for Blanding's turtle population health and identifying management changes that may improve sustainability.
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http://dx.doi.org/10.1638/2018-0074DOI Listing
September 2019

BODY CONDITION OF EASTERN BOX TURTLES () EVALUATED BY COMPUTED TOMOGRAPHY.

J Zoo Wildl Med 2019 Jun 13;50(2):295-302. Epub 2019 Jun 13.

Department of Veterinary Clinical Medicine, University of Illinois College of Veterinary Medicine, Urbana, IL 61802, USA.

Conservation efforts determining the health status of individuals can aid in assessing population health and sustainability. Body condition was determined in 65 free-ranging Eastern box turtles () from four locations in Vermilion County, Illinois, in the months of May, July, and September 2014, 2015, and 2016 using computed tomography (CT). Physical examinations were performed to determine morphometric measurements, and CT scans measured body fat. Twenty-three linear models were constructed to determine which morphometric measurements best correlated to fat content. The top two models of body fat included a relationship between mass and carapace width. Fat increases as both mass and carapace width increase. CT, while impractical for daily use, improved on previous methods of measuring body condition and created a calculation that can be applied broadly to Eastern box turtles. By understanding how measurements of mass and carapace width correlate to body condition, practitioners, researchers, and conservationists can evaluate chelonians with increased confidence in the accuracy of their assessment.
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http://dx.doi.org/10.1638/2018-0201DOI Listing
June 2019

DETECTION OF SP. IN INDOCHINESE BOX TURTLES ().

J Zoo Wildl Med 2019 03;50(1):254-257

Wildlife Epidemiology Laboratory, College of Veterinary Medicine, University of Illinois, Urbana, IL 61802, USA.

species are important pathogens of captive and free-ranging chelonians. Bourret's box turtle () is a critically endangered species of Indochinese box turtle in the family Geoemydidae. Four privately owned wild-caught Bourret's box turtles were presented for clinical evaluation for anorexia and lethargy following shipment from a reptile wholesaler 3 wk prior. Choanal-cloacal swabs of two of the turtles were positive for sp. by polymerase chain reaction. Sequencing of the 16S rRNA gene and 16S-23S rRNA intergenic spacer was 99% homologous to an unclassified sp. previously documented in free-ranging and captive North American species of the family Emydidae. The potential of sp. to induce disease in Bourret's box turtles is unknown. Global trade in live reptiles is believed to have facilitated this potential expansion of host range.
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http://dx.doi.org/10.1638/2018-0091DOI Listing
March 2019

EFFECTS OF OXYGEN AND ISOFLURANE ANESTHESIA ON HEMOLYMPH GAS ANALYSIS AND RIGHTING REFLEX OF ASIAN FOREST () AND DICTATOR SCORPIONS ().

J Zoo Wildl Med 2019 03;50(1):111-122

Wildlife Epidemiology Laboratory, Department of Veterinary Clinical Medicine, College of Veterinary Medicine, University of Illinois at Urbana-Champaign, Urbana, IL 61802, USA.

Large arachnids are commonly managed under professional care, and anesthesia is occasionally required for physical examination and diagnostic and therapeutic procedures. Anesthetic responses and hemolymph gas analysis have been studied previously in spiders, but scorpions have yet to be investigated. This study measured hemolymph gas values with an i-STAT point of care blood gas analyzer in healthy adult Asian forest scorpions ( = HL, = 8) and dictator scorpions ( = PD, = 12) breathing: 1) room air (RA), 2) 100% oxygen for 10 min in a chamber (OX), and 3) 5% isoflurane and oxygen (ISO) in a chamber until induction or loss of righting reflex. All scorpions recovered without complications, and there were no cartridge failures. Analysis of hemolymph gas values revealed that pH was lower in OX compared with RA and ISO and was lower in PD compared with HL scorpions. The partial pressure of carbon dioxide did not differ between inhaled gases but was higher in PD compared with HL. The partial pressure of oxygen (pO) was higher in ISO compared with OX, and both were higher than when breathing RA. Despite a lack of species difference in pO, PD had a more dramatic increase in pO in ISO compared with HL (significant species and inhalant interaction). PD had a significantly shorter induction time than HL, but recovery time (return of righting reflex) did not differ between species. Subjectively, HL exhibited rough inductions compared with PD, characterized by violent whole-body and tail movements. The unexpected increase in pO in ISO compared with OX, along with the species-specific differences and anesthetic effects, emphasizes the unique respiratory physiology of scorpions and demonstrates that further species-specific studies of anesthetics are warranted.
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http://dx.doi.org/10.1638/2018-0173DOI Listing
March 2019

TISSUE ENZYME ACTIVITIES IN FREE-LIVING EASTERN BOX TURTLES ().

J Zoo Wildl Med 2019 03;50(1):45-54

Wildlife Epidemiology Laboratory, University of Illinois, Urbana, IL 61802, USA.

Plasma biochemical enzymes are commonly assayed as part of a diagnostic evaluation for zoological species, but their interpretation is complicated by a lack of knowledge about tissue of origin in many reptiles. This study evaluated tissue specificity of six biochemical enzymes (alanine aminotransferase [ALT], aspartate aminotransferase [AST], alkaline phosphatase [ALP], creatine kinase [CK], gamma-glutamyl transferase [GGT], and glutamate dehydrogenase [GLDH]) in 10 tissues (skeletal muscle, cardiac muscle, lung, liver, gallbladder, pancreas, gastrointestinal tract, kidney, spleen, and reproductive tract) from 10 free-living eastern box turtles (). CK activity was highest in skeletal muscle, cardiac muscle, and gastrointestinal tract; GLDH and ALT activities were highest in liver, kidney, and gallbladder; ALP and GGT activities were elevated in kidney and gastrointestinal tract; and AST was relatively nonspecific, with significantly higher activity in the cardiac muscle, liver, kidney, skeletal muscle, and gallbladder compared to other tissues ( < 0.05). These results serve as a first step toward improving clinical interpretation of plasma biochemistry panels in box turtles.
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http://dx.doi.org/10.1638/2018-0079DOI Listing
March 2019

Venous blood gas in free-living eastern box turtles () and effects of physiologic, demographic and environmental factors.

Conserv Physiol 2018 25;6(1):coy041. Epub 2018 Jul 25.

Wildlife Epidemiology Lab, Department of Veterinary Clinical Medicine 2001 S. Lincoln Ave., Urbana, IL 61802, USA.

Sustainable wildlife populations depend on healthy individuals, and the approach to determine wellness of individuals is multifaceted. Blood gas analysis serves as a useful adjunctive diagnostic test for health assessment, but it is uncommonly applied to terrestrial reptiles. This study established reference intervals for venous blood gas panels in free-living eastern box turtles (, = 102) from Illinois and Tennessee, and modeled the effects of environmental and physiologic parameters on each blood gas analyte. Blood gas panels included pH, partial pressure of oxygen (pO), partial pressure of carbon dioxide (pCO), total carbon dioxide (TCO), bicarbonate (HCO), base excess (BE) and lactate. Candidate sets of general linear models were constructed for each blood gas analyte and ranked using an information-theoretic approach (AIC). Season, packed cell volume (PCV) and activity level were the most important predictors for all blood gas analytes ( < 0.05). Elevations in PCV were associated with increases in pCO and lactate, and decreases in pH, pO, HCO, TCO and BE. Turtles with quiet activity levels had lower pH and pO and higher pCO than bright individuals. pH, HCO, TCO and BE were lowest in the summer, while pCO and lactate were highest. Overall, blood pH was most acidic in quiet turtles with elevated PCVs during summer. Trends in the respiratory and metabolic components of the blood gas panel tended to be synergistic rather than antagonistic, demonstrating that either (1) mixed acid-base disturbances are common or (2) chelonian blood pH can reach extreme values prior to activation of compensatory mechanisms. This study shows that box turtle blood gas analytes depend on several physiologic and environmental parameters and the results serve as a baseline for future evaluation.
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http://dx.doi.org/10.1093/conphys/coy041DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6059089PMC
July 2018

Investigation of multiple mortality events in eastern box turtles (Terrapene carolina carolina).

PLoS One 2018 5;13(4):e0195617. Epub 2018 Apr 5.

Zoological Pathology Program, University of Illinois College of Veterinary Medicine, Urbana, Illinois, United States of America.

Wildlife mortality investigations are important for conservation, food safety, and public health; but they are infrequently reported for cryptic chelonian species. Eastern box turtles (Terrapene carolina carolina) are declining due to anthropogenic factors and disease, and while mortality investigations have been reported for captive and translocated individuals, few descriptions exist for free-living populations. We report the results of four natural mortality event investigations conducted during routine health surveillance of three Illinois box turtle populations in 2011, 2013, 2014, and 2015. In April 2011, over 50 box turtles were found dead and a polymicrobial necrotizing bacterial infection was diagnosed in five survivors using histopathology and aerobic/anaerobic culture. This represents the first reported occurrence of necrotizing bacterial infection in box turtles. In August 2013, paired histopathology and qPCR ranavirus detection in nine turtles was significantly associated with occupation of moist microhabitats, identification of oral plaques and nasal discharge on physical exam, and increases in the heterophil count and heterophil to lymphocyte ratio (p < 0.05). In July 2014 and 2015, ranavirus outbreaks reoccurred within a 0.2km radius of highly-disturbed habitat containing ephemeral ponds used by amphibians for breeding. qPCR ranavirus detection in five individuals each year was significantly associated with use of moist microhabitats (p < 0.05). Detection of single and co-pathogens (Terrapene herpesvirus 1, adenovirus, and Mycoplasma sp.) was common before, during, and after mortality events, but improved sample size would be necessary to determine the impacts of these pathogens on the occurrence and outcome of mortality events. This study provides novel information about the causes and predictors of natural box turtle mortality events. Continued investigation of health, disease, and death in free-living box turtles will improve baseline knowledge of morbidity and mortality, identify threats to survival, and promote the formation of effective conservation strategies.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0195617PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5886585PMC
July 2018

Development and validation of a quantitative PCR assay for detection of Emydoidea herpesvirus 1 in free-ranging Blanding's turtles (Emydoidea blandingii).

J Virol Methods 2018 04 31;254:40-45. Epub 2018 Jan 31.

Wildlife Epidemiology Laboratory, Department of Veterinary Clinical Medicine, College of Veterinary Medicine, University of Illinois at Urbana-Champaign, Urbana, IL 61802, USA.

Blanding's turtles (Emydoidea blandingii), an endangered species in Illinois, have experienced range-wide declines because of habitat degradation and fragmentation, predation, and road mortality. While ongoing studies are crucial to a thorough understanding of the natural history and demographics in these disjointed Illinois populations, infectious disease threats have been largely unevaluated. Herpesvirus outbreaks have been associated with high morbidity and mortality in populations of captive tortoises and turtles worldwide, including the family Emydidae (pond and box turtles). However, novel herpesviruses including Terrapene herpesvirus 1, Emydid herpesvirus 1 and 2, and Glyptemys herpesvirus 1 and 2, have recently been identified in apparently healthy free-ranging freshwater turtles. In 2015, 20 free-ranging Blanding's turtles in DuPage County, Illinois were screened for a herpesvirus using consensus PCR. A novel herpesvirus species (Emydoidea herpesvirus 1; EBHV1) was identified in two animals and shared a high degree of sequence homology to other freshwater turtle herpesviruses. Two quantitative real-time PCR assays, using EBHV1 primer-1 and primer-2, were developed to target an EBHV1-specific segment of the DNA-dependent DNA polymerase gene and validated. Both assays performed with high efficiency (slope = -3.2; R = 1), low intra-assay variability, and low inter-assay variability (coefficient of variation <2% at all dilutions). However, EBHV1 primer-2 displayed less variation and was selected to test clinical samples and five closely related herpesvirus control samples. Results indicate that this assay is specific for EBHV1, has a linear range of detection from 10 to 10 viral copies per reaction, and can categorically detect as few as 1 viral copy per reaction. This qPCR assay provides a valuable diagnostic tool for future characterization of EBHV1 epidemiology.
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http://dx.doi.org/10.1016/j.jviromet.2018.01.006DOI Listing
April 2018

DETECTION OF RANAVIRUS USING BONE MARROW HARVESTED FROM MORTALITY EVENTS IN EASTERN BOX TURTLES ( TERRAPENE CAROLINA CAROLINA).

J Zoo Wildl Med 2017 12;48(4):1210-1214

The causes of free-living chelonian mortality events are often unknown because of infrequent recovery of remains and rapid postmortem decomposition. This study describes a technique to harvest bone marrow and detect frog virus 3-like ranavirus (FV3) using quantitative polymerase chain reaction in skeletonized eastern box turtles ( Terrapene carolina carolina) ( N = 87), and assesses agreement with concurrent perimortem samples ( N = 14). FV3 was detected in bone marrow samples from 12 turtle shells (14%). Three of 14 turtles had detectable FV3 loads in both bone marrow and perimortem samples, two turtles had detectable FV3 in bone marrow only, and nine turtles tested FV3 negative in both bone marrow and concurrent perimortem samples. There was substantial agreement between FV3 testing of bone marrow and other tissues ( κ = 0.658). Harvesting bone marrow from shells is easily performed and can serve as a means for biologists and wildlife veterinarians to improve postmortem surveillance for systemically distributed pathogens, including FV3.
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http://dx.doi.org/10.1638/2017-0098.1DOI Listing
December 2017

DETECTION OF COPATHOGENS IN FREE-RANGING EASTERN BOX TURTLES ( TERRAPENE CAROLINA CAROLINA) IN ILLINOIS AND TENNESSEE.

J Zoo Wildl Med 2017 12;48(4):1127-1134

Conservation efforts are investigating the impact of diseases within a species of interest, including prevalence and transmission and morbidity and mortality rates. However, the majority of these studies focus solely on the characteristics of a single pathogen. Recently, the role of copathogens has been reported to impact disease susceptibility and mortality. To that effect, a survey was conducted including 318 eastern box turtles ( Terrapene carolina carolina) from populations in Illinois and Tennessee in 2014 and 2015. Blood samples and oral swabs were collected for quantitative polymerase chain reaction (qPCR) of 15 different pathogens performed in a multiplex format using Fluidigm array technology. Four pathogens were found with varying qPCR prevalence: ranavirus (FV3; n = 2, 0.6%), Terrapene herpesvirus 1 (TerHV1; n = 129, 40.7%), box turtle Mycoplasma sp. (BT Myco; n = 14, 4.6%), and box turtle adenovirus (BT Adv1; n = 18, 11%). Thirteen pathogens were not identified in any sample, including Mycoplasma agassizii, M. testudineum, Salmonella enteriditis, S. typhmirium, Borrelia burgdorferi, Anaplasma phagocyophilum, tortoise intranuclear coccidia, Ambystoma tigrinum virus, Bohle iridovirus, Epizootic hematopoietic necrosis virus, and testudinid herpesvirus 2. Copathogen occurrence was rare but was observed in eight individuals with TerHV1-BT Myco detection and two animals with TerHV1-Adv1. Significant differences were observed in pathogen detection across season (TerHV1, BT Adv1, BT Myco, and TerHV1-Myco) and year (TerHV1, BT Adv1, and TerHV1-Myco). The results of this survey highlight that a single pathogen model may not adequately explain pathogen dynamics and that conservation efforts need to be aimed at detecting multiple pathogens in order to fully characterize population health.
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http://dx.doi.org/10.1638/2017-0148R.1DOI Listing
December 2017

BIOCHEMISTRY PANEL REFERENCE INTERVALS FOR JUVENILE GOLDFISH (CARASSIUS AURATUS).

J Zoo Wildl Med 2017 09;48(3):776-785

Reference intervals for diagnostic tests are vitally important for clinical decision making. Despite the popularity of pet goldfish (Carassius auratus), reference intervals have not been generated for routine biochemistry panel analytes in this species. This study establishes de novo reference intervals for packed cell volume and total solids, using 47 apparently healthy immature goldfish, and for 11 common chemistry panel analytes (albumin, aspartate aminotransferase, calcium, creatine kinase, globulin, blood glucose, sodium, potassium, phosphorous, total protein, and uric acid) using 39 immature goldfish. Robust reference intervals were generated following recommendations of the American Society for Veterinary Clinical Pathology. Linear regression was used to demonstrate a statistically significant relationship between body weight and calcium, albumin, total protein, potassium, packed cell volume, and total solids. The results of this study serve as a useful baseline for future reference interval generation in goldfish.
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http://dx.doi.org/10.1638/2015-0287.1DOI Listing
September 2017