Publications by authors named "Matthew C Allender"

106 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

First Report of Ophidiomycosis in a Free-Ranging California Kingsnake (Lampropeltis californiae) in California, USA.

J Wildl Dis 2021 01;57(1):246-249

Wildlife Epidemiology Lab, University of Illinois College of Veterinary Medicine, 2001 S Lincoln Avenue, Urbana, Illinois 61802, USA.

Ophidiomycosis (snake fungal disease) is an emerging threat to snake health worldwide. We report a case of disseminated ophidiomycosis in a California kingsnake (Lampropeltis californiae) from Plymouth, Amador County, California, US, which is the first report of the disease in this species and in a free-ranging snake in California.
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http://dx.doi.org/10.7589/JWD-D-20-00006DOI Listing
January 2021

Shell Lesions Associated With Infection in Freshwater Aquatic Turtles.

Vet Pathol 2021 May 12;58(3):578-586. Epub 2021 Feb 12.

70154University of Illinois at Urbana-Champaign, Brookfield, IL, USA.

A newly described onygenalean fungus, , has been isolated from ulcerative shell and skin lesions of freshwater aquatic chelonians. To investigate the shell lesions associated with infection and determine if any lesional features were unique to . , tissues from turtles housed in zoological institutions ( = 45) in the United States and free-living turtles ( = 5) submitted for diagnostic biopsy or necropsy were examined. Free-living turtles were from geographically distinct habitats in Florida ( = 1) and Washington ( = 4) at the time of sampling. Histologic shell sections were evaluated for the presence or absence of specific lesional features. Infection with was evaluated in all cases by screening GMS (Grocott-Gomori's methenamine silver)-stained histologic sections for the presence of morphologically consistent fungi and by quantitative PCR (polymerase chain reaction) on representative frozen tissue or formalin-fixed paraffin-embedded sections. Additionally, culture was performed for 15 cases with available fresh/frozen tissue. In total, there were 17 PCR-confirmed cases, 29 cases with morphologically consistent fungi on GMS-stained sections, and 21 cases of shell lesions without histologic or molecular evidence of infection. Epithelial inclusion cysts, defined as cystic structures within the dermis lined by keratinized stratified squamous epithelium and containing necrotic bone and keratin debris, were significantly ( < .01) associated with infection. Other significantly associated shell lesions included squamous metaplasia, hyperkeratosis, inflammation, and osteonecrosis ( < .05). This study identified characteristic shell lesions associated with infection. Further studies to prove causality are needed.
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http://dx.doi.org/10.1177/0300985820985217DOI Listing
May 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

Use of a Multimodal, Peer-to-Peer Learning Management System for Introduction of Critical Clinical Thinking to First-Year Veterinary Students.

J Vet Med Educ 2021 Apr 11;48(2):170-180. Epub 2021 Jan 11.

Veterinary medical students need multiple thinking strategies, particularly critical thinking. We used a multimedia, peer review learning management system (CGScholar) to introduce a series of complex, realistic, case-based e-learning modules to help introduce critical thinking to 422 first-year veterinary students through instructor-designed clinical cases. Students developed and published on the CGScholar platform an analysis of a case and conducted anonymous peer reviews of each other's drafts. Instructors selected desirable characteristics of a student's activity to track and provide automatic feedback to students via an analytics dashboard and aster plot that allowed visualization of progress. The dashboard also enabled instructors to view the entire class's performance, highlighting students whose performance was lagging. Online interactions were supplemented by case-specific face-to-face workshop sessions. Our goal was to address the following questions: Does the addition of multimedia to a work (one's own or others') enhance people's ability to understand and convey the material? Does peer review (of one's own and others' work) lead to improvements in the writer's own work? Does the peer review process enhance the writer's understanding of what constitutes high-quality literature evidence? An anonymous student survey showed that experience was significantly more positive in the second and third year of implementation after inclusion of explicit guidance on the use of the rubric for peer review. Overall, 67% of students thought inclusion of multimedia enhanced their ability to communicate and 52% agreed multimedia enhanced their ability to understand their peers' analyses, but students were split on benefits to their understanding of high-quality literature.
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http://dx.doi.org/10.3138/jvme.2019-0029DOI Listing
April 2021

The effect of topical lidocaine on intradermal testing in atopic dogs.

Vet Dermatol 2021 Apr 8;32(2):139-e31. Epub 2021 Jan 8.

Department of Veterinary Clinical Medicine, University of Illinois Veterinary Teaching Hospital, 1008 West Hazelwood Drive, Urbana, IL, 61802, USA.

Background: Intradermal testing (IDT) most often requires sedation. Topical lidocaine offers an adjunct or alternative to sedation.

Hypothesis/objectives: We hypothesized that topical lidocaine would significantly reduce reactions to intradermal injections and that atopic dogs treated with topical lidocaine would have similar results with IDT to atopic dogs tested without topical lidocaine.

Animals: Fifteen client-owned atopic dogs.

Methods: In Part I, a 5% lidocaine patch, 5% lidocaine cream and a control with no active ingredients were compared. The lowest pain score during intradermal injection was established in six atopic dogs. Fifteen atopic dogs were enrolled in Part II, and lidocaine cream (found to be most effective in Part 1) was applied randomly to a single side of the thorax. An IDT was performed on each side of the chest. Subjective and objective scores of the control and lidocaine treatment sides were compared 15 and 30 min post-injection.

Results: The 5% lidocaine cream had the greatest reduction in pain score associated with intradermal injection. There were no significant differences in mean wheal diameter for any evaluated allergen at any time point between the control and lidocaine-treated sides. There was high agreement between the two groups when assessing the subjective score for all but one allergen.

Conclusions And Clinical Importance: Topical lidocaine may be used as adjunctive analgesia during IDT with caution in interpretation of subjective house dust scoring. Lidocaine cream appeared to reduce pain score and may allow reduction in concurrent sedation.
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http://dx.doi.org/10.1111/vde.12923DOI Listing
April 2021

Temperature affects the host hematological and cytokine response following experimental ranavirus infection in red-eared sliders (Trachemys scripta elegans).

PLoS One 2020 29;15(10):e0241414. Epub 2020 Oct 29.

Wildlife Epidemiology Laboratory, College of Veterinary Medicine at University of Illinois, Urbana-Champaign, Illinois, United States of America.

Pathogen-host interactions are important components of epidemiological research, but are scarcely investigated in chelonians. Red-eared sliders (Trachemys scripta elegans), are recognized as a model for frog virus-3 infection (FV3), a ranavirus in the family Iridoviridae that infects multiple classes of ectothermic vertebrates. Previous challenge studies observed differences in disease outcome based on environmental temperature in this species, but the host response was minimally evaluated. We challenged red-eared sliders with an FV3-like ranavirus at both 28°C and 22°C. We monitored several host response variables for 30 days, including: survival (binary outcome and duration), clinical signs, total and differential leukocytes, and select cytokine transcription in the buffy coat (IL-1β, TNFα, IFYg, IL-10). After 30 days, 17% of challenged turtles survived at 28°C (Median survival time [MST]: 15 days, range: 10-30 days) and 50% survived (MST: 28.5 days, range: 23-30 days) at 22°C (range 23-30 days). The most common clinical signs were injection site swelling, palpebral swelling, and lethargy. The heterophil/lymphocyte ratio at 22°C and interleukin-1 beta (IL1β) transcription at both 22°C and 28°C were significantly greater on days 9, 16, and 23 in FV3 challenged groups. Tumor necrosis factor alpha and interleukin-10 were transcribed at detectable levels, but did not display significant differences in mean relative transcription quantity over time. Overall, evidence indicates an over-robust immune response leading to death in the challenged turtles. FV3 remains a risk for captive and free-ranging chelonian populations, and insight to host/pathogen interaction through this model helps to elucidate the timing and intensity of the host response that contribute to mortality.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0241414PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7595395PMC
December 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

Comparison of isoflurane, sevoflurane, and desflurane as inhalant anesthetics in prairie rattlesnakes ().

J Am Vet Med Assoc 2020 Nov;257(9):945-949

Objective: To characterize induction and recovery characteristics of 3 commonly used inhalant anesthetics in prairie rattlesnakes (): isoflurane, sevoflurane, and desflurane.

Animals: 12 healthy adult prairie rattlesnakes.

Procedures: In a randomized crossover design, snakes underwent anesthetic induction with 5% isoflurane, 8% sevoflurane, or 18% desflurane, with a washout period of ≥ 7 days between anesthetic events. Anesthetic depth parameters were recorded throughout induction and recovery, including time to loss and return of righting reflex, muscle tone, ability to intubate, response to pressure, and time to return to spontaneous respiration. Every 5 minutes throughout the anesthetic procedures, heart rate, respiratory rate, and percentage expired anesthetic gas were recorded.

Results: No snakes died during the study. Sevoflurane anesthesia resulted in anesthetic gas avoidance behavior in snakes during induction and had the significantly longest recovery time to extubation and time to return of pressure response, compared with the other inhalant anesthetics. Anesthesia with isoflurane resulted in a significantly longer time to return of righting reflex, compared with sevoflurane or desflurane. No significant difference was noted in time to loss of pressure response among the 3 anesthetic gases. Desflurane anesthesia resulted in the significantly quickest loss of righting reflex among the anesthetic protocols; despite this, 4 of 12 desflurane anesthetized snakes did not achieve an anesthetic plane deep enough for intubation.

Conclusions And Clinical Relevance: Isoflurane and sevoflurane, but not desflurane, inhalation anesthesia resulted in consistent and predictable loss of righting reflex and induction of anesthesia deep enough to allow intubation in snakes.
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http://dx.doi.org/10.2460/javma.257.9.945DOI Listing
November 2020

Ophidiomycosis, an emerging fungal disease of snakes: Targeted surveillance on military lands and detection in the western US and Puerto Rico.

PLoS One 2020 8;15(10):e0240415. Epub 2020 Oct 8.

Naval Facilities Engineering Command Southwest, San Diego, CA, United States of America.

Wildlife disease surveillance and pathogen detection are fundamental for conservation, population sustainability, and public health. Detection of pathogens in snakes is often overlooked despite their essential roles as both predators and prey within their communities. Ophidiomycosis (formerly referred to as Snake Fungal Disease, SFD), an emergent disease on the North American landscape caused by the fungus Ophidiomyces ophiodiicola, poses a threat to snake population health and stability. We tested 657 individual snakes representing 58 species in 31 states from 56 military bases in the continental US and Puerto Rico for O. ophiodiicola. Ophidiomyces ophiodiicola DNA was detected in samples from 113 snakes for a prevalence of 17.2% (95% CI: 14.4-20.3%), representing 25 species from 19 states/territories, including the first reports of the pathogen in snakes in Idaho, Oklahoma, and Puerto Rico. Most animals were ophidiomycosis negative (n = 462), with Ophidiomyces detected by qPCR (n = 64), possible ophidiomycosis (n = 82), and apparent ophidiomycosis (n = 49) occurring less frequently. Adults had 2.38 times greater odds than juveniles of being diagnosed with ophidiomycosis. Snakes from Georgia, Massachusetts, Pennsylvania, and Virginia all had greater odds of ophidiomycosis diagnosis, while snakes from Idaho were less likely to be diagnosed with ophidiomycosis. The results of this survey indicate that this pathogen is endemic in the eastern US and identified new sites that could represent emergence or improved detection of endemic sites. The direct mortality of snakes with ophidiomycosis is unknown from this study, but the presence of numerous individuals with clinical disease warrants further investigation and possible conservation action.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0240415PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7544097PMC
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

EVALUATION OF THE INTER- AND INTRAINDIVIDUAL AGREEMENT OF A PODODERMATITIS SCORING MODEL IN GREATER FLAMINGOS ().

J Zoo Wildl Med 2020 Jun;51(2):379-384

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

Pododermatitis is an important cause of morbidity and mortality in flamingos under human care; management and treatment options vary widely based on subjective assessment from veterinarians or animal care staff (ACS). The objective of this study was to evaluate the agreement of pododermatitis severity scores assigned by veterinarians, ACS, and veterinary students when given a standardized rubric. Twenty-four greater flamingos () from a single zoo-managed flock were evaluated over time for pododermatitis. The individual feet of each bird were imaged, blinded, randomized, and scored for hyperkeratosis, fissures, nodules, papillomatous growth, and overall subjective score by seven evaluators (three veterinary specialists, two ACS, and two veterinary students) using a previously established flamingo pododermatitis scoring rubric. Interindividual reliability between evaluators and intraindividual agreement among specialists was determined. Reliable interindividual agreement was seen for fissures (Krippendorff's α [KA] = 0.807) between all seven evaluators, whereas the other individual lesions had very low reliability. Between the specialists, fissures had low interindividual reliability (KA = 0.782). Two specialists had strong intraindividual agreement for fissure score and one specialist had strong intraindividual agreement for overall subjective score (Cohen's κ [CK] 0.8-0.9, < 0.01). Hyperkeratosis, papillomatous growth, nodules, and overall subjective score had low to moderate inter- and intraindividual reliability or agreement (KA, 0.06-0.49; CK, 0.02-0.8). In conclusion, the current scoring method for flamingo pododermatitis does not supply a reliable method for tracking foot health based on images alone across timepoints, except for fissures. Further analysis of the scoring system being used during a physical examination is warranted.
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http://dx.doi.org/10.1638/2019-0219DOI Listing
June 2020

PROGNOSTIC INDICATORS FOR SURVIVAL OF ORPHANED EASTERN GRAY SQUIRRELS ().

J Zoo Wildl Med 2020 Jun;51(2):275-279

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

The eastern grey squirrel (EGS), , is a tree squirrel native to the eastern United States. This species commonly presents to wildlife medical clinics for a variety of human-related injuries including confrontations with road traffic and pet predation. The purpose of this study was to assess initial examination findings as prognostic indicators for survival in EGS. The medical record database of the University of Illinois Wildlife Medical Clinic was searched from January 2012 through December 2018 for records of EGS weighing <300 g. The squirrels were identified as survivors (individuals surviving, released, or transferred to a rehabilitator within 72 hr of intake) or nonsurvivors (individuals euthanized or dying within 72 hr of intake after receiving medical care). Presenting weight, health status, method of feeding, and singleton versus group presentation were categorically recorded for each case. The data were modeled using a series of candidate logistic regression models fitted using the generalized linear model. An information theoretical approach determined the best fit model. A total of 955 EGS were included in this study. Factors that predicted a nonsurvivor status included EGSs that presented with any health system abnormality (odds ratio [OR], 4.81; 95% confidence interval [CI], 3.34-6.72), EGSs that presented between December and May (OR, 1.60; 95% CI, 1.12-2.27) rather than between June and November, and individuals with neurologic signs (OR, 2.61; 95% CI, 1.51-4.51) compared with EGSs without neurologic signs. Despite not being included in the final model, the presence of respiratory signs (OR, 3.43; 95% CI, 2.41-4.89) and diarrhea (OR, 4.01; 95% CI, 1.59-10.09) were significantly associated with a higher likelihood of nonsurvival status. Wildlife medical clinics and rehabilitation centers may use this information by initiating more aggressive therapies or instituting distinct euthanasia protocols for EGS that present with body system abnormalities, particularly neurologic clinical signs, and those that present in the winter months.
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http://dx.doi.org/10.1638/2019-0124DOI Listing
June 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

Circulating nutrient concentrations in free-ranging Humboldt penguins (Spheniscus humboldti) in Punta San Juan, Peru.

Zoo Biol 2020 Jul 29;39(4):246-256. Epub 2020 Mar 29.

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

Free-ranging Humboldt penguin (HP, Spheniscus humboldti) populations are under pressure from resource competition with industrial fisheries, habitat loss, and El Niño Southern Oscillation events. Foraging patterns for this top marine predator change during periods of aberrant oceanographic conditions and scarce fish stock numbers. These radical dietary fluctuations can lead to poor fertility, early embryonic death, poor hatchability, suppressed immune function, high chick mortality, and illness. To understand the variability of nutrient status in reproductive seasons, we measured select circulating nutrient concentrations (fat-soluble vitamins A, D, E, and carotenoids, fatty acids, amino acids, minerals, and electrolytes) of 105 HP at Punta San Juan, Peru during the first reproductive seasons of 2007 and 2008. We determined significant differences in nutrient status between sexes, years of sampling, and reproductive stages. Males (4.5 ± 0.38 kg) weighed more than females (4.0 ± 0.29 kg) and exhibited higher concentrations of vitamin A (0.71 ± 0.11 vs. 0.61 ± 0.12 µg/ml) and docosahexaenoic acid (6.70 ± 1.61 vs. 5.65 ± 1.59%). Males also displayed lower concentrations of β-carotene (0.01 ± 0.01 vs. 0.012 ± 0.001 µg/ml) and phosphorus (3.43 ± 0.83 vs. 4.40 ± 1.66 mg/dl). Comparison between the 2 years showed most circulating amino acid concentrations were higher in 2007. Significant differences in circulating amino acids and vitamins were also noted between different reproductive stages. These results demonstrate concentrations of nutrients can vary due to the physiological state of the animal, as well as the overall dynamics of their marine ecosystem habitat.
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http://dx.doi.org/10.1002/zoo.21540DOI Listing
July 2020

Pathogen Surveillance and Detection of Ranavirus () in Translocated Gopher Tortoises ().

J Wildl Dis 2020 07 13;56(3):679-683. Epub 2020 Feb 13.

Warnell School of Forestry and Natural Resources, University of Georgia, 180 E Green St., Athens, Georgia 30602, USA.

Emerging pathogens may pose additional threats to already vulnerable populations of chelonians, such as gopher tortoises (). In response to a mortality event on a translocation site in northwest Florida, US during 2013-15, 13 gopher tortoises were necropsied and their tissues were screened for 12 pathogens, including , , and -like ranavirus (FV3). The DNA of FV3 was detected via quantitative PCR in the gastrointestinal tract of three tortoises. Subsequently, pathogen surveillance was performed on whole blood and oral-cloacal swab samples of live translocated tortoises from two different enclosures within the site (=68), rehabilitated tortoises from the site (=18), and tortoises prior to release on site (=35) during 2015-17. spp. were present in all groups and years of live tortoises tested. The DNA of FV3 was detected in 15 individuals both with and without clinical signs of disease in 2016. We recaptured 20 tortoises and captured an additional 20 tortoises in 2017 for surveillance, yet FV3 DNA was no longer detected, even in those that had previously tested positive (=7). The results of this study contribute to the epidemiology of ranavirus in chelonians and suggests that gopher tortoises could be reservoirs for FV3. We recommend that the status of infection should be included for health screens for gopher tortoises in translocation programs.
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http://dx.doi.org/10.7589/2019-02-053DOI Listing
July 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

OBJECTIVE GAIT ANALYSIS IN HUMBOLDT PENGUINS () USING A PRESSURE-SENSITIVE WALKWAY.

J Zoo Wildl Med 2020 Jan;50(4):910-916

Chicago Zoological Society, Brookfield Zoo, Brookfield, IL 60513, USA.

Assessment of pododermatitis, osteoarthritis, and other causes of lameness in penguins can be challenging. Subjective gait analysis using visual observation and response to analgesic therapy can be affected by observer variation and caregiver placebo bias. A pressure-sensitive walkway (PSW), however, allows for objective gait analysis and assessment of analgesic therapeutic response. In this study, a 3-m-long PSW was used to analyze gait in 21 adult Humboldt penguins (). Medical record reviews and comprehensive examinations were performed on all penguins; five penguins were considered abnormal, with either right-sided ( = 3) or bilateral historical lameness-causing disease ( = 2) and were analyzed separately from the normal data set. All penguins walked across the PSW four times and gait parameters (step and stride distances and velocities, maximum force, impulse, and peak pressure) were calculated for each foot in each penguin. Statistical comparisons were made between right and left feet, sexes, and normal and abnormal penguins for each gait parameter. Among normal penguins, there were no significant differences between feet or sex. Left step width was shorter in abnormal penguins than that of normal penguins. Study results established baseline values for Humboldt penguins. This will allow objective monitoring of progression and response to therapy in penguin lameness cases, both current and future. The data also provide a foundation to compare gait parameters with other penguin populations and species.
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http://dx.doi.org/10.1638/2019-0054DOI Listing
January 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

PROGNOSTIC INDICATORS FOR SURVIVAL OF ORPHANED NEONATAL AND JUVENILE EASTERN COTTONTAIL RABBITS (): 1,256 CASES (2012-17).

J Wildl Dis 2020 07 2;56(3):523-529. Epub 2020 Jan 2.

Department of Veterinary Clinical Sciences, College of Veterinary Medicine, University of Illinois, 2001 S Lincoln Avenue, Urbana, Illinois 61802, USA.

Orphaned eastern cottontail rabbits (ECRs; ) often present to wildlife clinics within their geographic range and require considerable dedication of time and resources. The objective of this analytical cross-sectional study was to assess initial examination findings to be used as prognostic indicators for orphaned neonatal and juvenile ECRs. The medical records of the University of Illinois Wildlife Medical Clinic were searched for ECRs presenting between 2012 and 2018. This criterion identified 1,256 ECRs that were then classified as survivors (survived and released) or as nonsurvivors (euthanized or natural death) within 72 h of admission. Presenting weight, body system abnormalities, hydration status, intervention prior to presentation, and singleton versus group presentation were categorically recorded for each individual ECR. The data were modeled using a series of logistic regression models fitted using the general linear model. Individuals were significantly more likely to be nonsurvivors if they presented as singletons (<0.0001), presented with moderate/severe (<0.001) or mild integumentary signs (=0.0261), presented with multi-organ disease (<0.001), presented with neurologic signs (<0.0003), or had treatment provided prior to presentation (=0.031). Factors that did not predict survival status in ECRs included body weight =0.210), presence of respiratory signs (=0.674), and presence of dehydration (=0.356). These findings may be used at wildlife medical clinics to make triage criteria for euthanasia as well as dedicate limited funds and labor to cases with the best prognosis for survival.
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http://dx.doi.org/10.7589/2019-06-146DOI Listing
July 2020

Hepatic CT attenuation differs in three species of freshwater turtles and hepatic Hounsfield units increase with folliculogenesis in wild Blanding's turtles (Emydoidea blandingii).

Vet Radiol Ultrasound 2020 Mar 20;61(2):181-189. Epub 2019 Dec 20.

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

Freshwater turtle species are suffering from anthropocentric-caused population declines, making preservation of professionally managed populations increasingly important. Turtles under professional care have an increased risk to develop hepatic lipidosis, potentially resulting in early death. Computed tomography can provide an antemortem screening for increased fatty liver composition. A goal of this prospective analytical cross-sectional study was to assess the hepatic attenuation measured as Hounsfield units (HU) in a wild population of a freshwater turtle species, and then compare hepatic HU to freshwater turtles under professional care. Ninety-five wild Blanding's turtles (BT; Emydoidea blandingii) as well as 10 Vietnamese Pond turtles (VPT; Mauremys annamensis) and six Northern Snake-Necked turtles (NSNT; Chelodina oblonga) under professional care underwent CT with quantification of hepatic HU. Hepatic HU were correlated to serum chemistry findings and the presence of follicles was recorded in BT. The mean (±SD) hepatic attenuation for 95 wild BT was 97.5 HU ±9.6. There were significant differences in hepatic attenuation among VPT, NSNT, and BT, with median HU values (range) of 5.39 HU (-6.45 to 61.50), 71.74 HU (59.44-94.49), and 95.43 HU (74.41-124.56), respectively. Aspartate aminotransferase (AST) values had a weak negative correlation to HU with a coefficient of -0.85 (P < .001). The hepatic attenuation was significantly higher for individuals undergoing folliculogenesis (P = .007). The decreased HU values were significantly negatively correlated with AST values. Findings supported the use of CT as an aid for guiding future management practices in freshwater turtles.
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http://dx.doi.org/10.1111/vru.12827DOI Listing
March 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

Determination of Thiafentanil in Plasma Using LC-MS.

J Chromatogr Sci 2019 Dec;58(1):1-4

Wildlife Pharmaceuticals Inc., 1230 West Ash, Windsor, CO, USA.

A new method of analysis has been developed and validated for the determination of thiafentanil in plasma. After protein precipitation, samples were separated on an XBridge BEH C18 column and quantified using mass spectrometry. The mobile phase was a mixture of water with 0.1% formic acid and acetonitrile with 0.1% formic acid (90:10). The standard curve ranged from 0.1 to 25 ng/mL. Intra- and Inter-assay variability for thiafentanil was less than 10%, and the average recovery was greater than 95%. The lower limit of quantification was 0.1 ng/mL. This is the first validated method for thiafentanil analysis in plasma.
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http://dx.doi.org/10.1093/chromsci/bmz098DOI Listing
December 2019

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