Deana L. Clifford

Investigating and managing the rapid emergence of white-nose syndrome, a novel, fatal, infectious disease of hibernating bats

White-nose syndrome (WNS) is a fatal disease of bats that hibernate. The etiologic agent of WNS is the fungus Geomyces destructans, which infects the skin and wing membranes. Over 1 million bats in six species in eastern North America have died from WNS since 2006, and as a result several species of bats may become endangered or extinct. Information is lacking on the pathogenesis of G. destructans and WNS, WNS transmission and maintenance, individual and site factors that contribute to the probability of an outbreak of WNS, and spatial dynamics of WNS spread in North America. We considered how descriptive and analytical epidemiology could be used to fill these information gaps, including a four-step (modified) outbreak investigation, application of a set of criteria (Hills) for assessing causation, compartment models of disease dynamics, and spatial modeling. We cataloged and critiqued adaptive-management options that have been either previously proposed for WNS or were helpful in addressing other emerging diseases of wild animals. These include an ongoing program of prospective surveillance of bats and hibernacula for WNS, treatment of individual bats, increasing population resistance to WNS (through vaccines, immunomodulators, or other methods), improving probability of survival from starvation and dehydration associated with WNS, modifying hibernacula environments to eliminate G. destructans, culling individuals or populations, controlling anthropogenic spread of WNS, conserving genetic diversity of bats, and educating the public about bats and bat conservation issues associated with WNS.

Pathogen exposure in endangered island fox (Urocyon littoralis) populations: Implications for conservation management

Abstract Island fox (Urocyon littoralis) populations on four California Channel Islands have declined severely since 1994. Canine distemper (CDV) was suspected to be responsible for the decline of the Santa Catalina Island fox, so knowledge of infectious disease exposure in the remaining island fox populations was urgently needed. This study reviewed previous pathogen exposure in island foxes and investigated the current threat by conducting a serologic survey of foxes on all islands and sympatric feral cats on three islands from 2001 to 2003 for antibodies against canid pathogens. Before the decline, foxes had evidence of exposure to CDV, canine adenovirus (CAV), canine parvovirus (CPV), and Toxoplasma, with exposure to these five pathogens differing greatly by island. Exposure to canine coronavirus (CCV), canine herpesvirus (CHV), and Leptospira was rare. In 2001–2003, wild-born foxes had evidence of exposure to CDV (5.2–32.8%) on 5 of 6 islands, CPV (28–100%) and CAV (4.7–100%) on five islands, and Toxoplasma gondii (2.3–15.4%) on four islands. Exposure to CCV, CHV and Leptospira was less common. Sharing of infectious agents between sympatric foxes and feral cats appeared minimal, but CDV exposure was detected in two cats on Santa Catalina Island. Domestic dogs have historically been present on the islands, but it is not known if canine diseases can be maintained in fox populations without the continual presence of dogs. Targeted vaccination programs against the most virulent pathogens and continued intensive disease surveillance may help protect the critically small remaining fox populations from disease outbreaks that could threaten the success of ongoing conservation efforts.

A “One Health” Approach to Address Emerging Zoonoses: The HALI Project in Tanzania

Jonna Mazet and colleagues describe their work in the Tanzania-based HALI Project, which adopts the “One Health” approach to address emerging zoonoses and that recognizes the interconnectedness of human, animal, and environmental health.

Evolution of a transdisciplinary “One Medicine–One Health” approach to global health education at the University of California, Davis

Abstract In todays world health events in one nation or geographic area often have repercussions for the health and well-being of populations beyond that region; sometimes even globally. In recent years many factors, most notably concern about emerging infectious diseases, have contributed to an increasing appreciation of the interdependency of human, animal and ecosystem health worldwide. Integrated global approaches to improve the health of humans, animals and their shared environments are proving to be in the best interest of many countries. A special symposium and award were established in memoriam to the internationally renowned epidemiologist, Dr. Calvin W. Schwabe, who (while at the University of California, Davis) was a significant advocate of the “One Medicine” approach to public health, calling upon all health professionals, including veterinarians, to work collaboratively and comparatively to improve human health. This paper discusses the evolution of the “One Medicine” concept into a global “One Health” approach to research, training capacity and service infrastructure, focused not only on disease, but also on health at the individual, population, and ecosystem levels. Projects involving UCD faculty which attempt to integrate a One Health approach include the Health for Animals and Livelihood Improvement (HALI) Project in Tanzania, Envirovet Summer Institute, Avian Flu School and Newcastle Immunization Program in Africa, a web-based virtual global health training program, and the Calvin Schwabe One Health Project.

Novel Amdovirus in Gray Foxes

We used viral metagenomics to identify a novel parvovirus in tissues of a gray fox (Urocyon cinereoargenteus). Nearly full genome characterization and phylogenetic analyses showed this parvovirus (provisionally named gray fox amdovirus) to be distantly related to Aleutian mink disease virus, representing the second viral species in the Amdovirus genus.

Investigating and Managing the Rapid Emergence of White-Nose Syndrome, a Novel, Fatal, Infectious Disease of Hibernating Bats: White-Nose Syndrome in Bats

White-nose syndrome (WNS) is a fatal disease of bats that hibernate. The etiologic agent of WNS is the fungus Geomyces destructans, which infects the skin and wing membranes. Over 1 million bats in six species in eastern North America have died from WNS since 2006, and as a result several species of bats may become endangered or extinct. Information is lacking on the pathogenesis of G. destructans and WNS, WNS transmission and maintenance, individual and site factors that contribute to the probability of an outbreak of WNS, and spatial dynamics of WNS spread in North America. We considered how descriptive and analytical epidemiology could be used to fill these information gaps, including a four-step (modified) outbreak investigation, application of a set of criteria (Hills) for assessing causation, compartment models of disease dynamics, and spatial modeling. We cataloged and critiqued adaptive-management options that have been either previously proposed for WNS or were helpful in addressing other emerging diseases of wild animals. These include an ongoing program of prospective surveillance of bats and hibernacula for WNS, treatment of individual bats, increasing population resistance to WNS (through vaccines, immunomodulators, or other methods), improving probability of survival from starvation and dehydration associated with WNS, modifying hibernacula environments to eliminate G. destructans, culling individuals or populations, controlling anthropogenic spread of WNS, conserving genetic diversity of bats, and educating the public about bats and bat conservation issues associated with WNS.

Patterns of Natural and Human-Caused Mortality Factors of a Rare Forest Carnivore, the Fisher (Pekania pennanti) in California

Wildlife populations of conservation concern are limited in distribution, population size and persistence by various factors, including mortality. The fisher (Pekania pennanti), a North American mid-sized carnivore whose range in the western Pacific United States has retracted considerably in the past century, was proposed for threatened status protection in late 2014 under the United States Endangered Species Act by the United States Fish and Wildlife Service in its West Coast Distinct Population Segment. We investigated mortality in 167 fishers from two genetically and geographically distinct sub-populations in California within this West Coast Distinct Population Segment using a combination of gross necropsy, histology, toxicology and molecular methods. Overall, predation (70%), natural disease (16%), toxicant poisoning (10%) and, less commonly, vehicular strike (2%) and other anthropogenic causes (2%) were causes of mortality observed. We documented both an increase in mortality to (57% increase) and exposure (6%) from pesticides in fishers in just the past three years, highlighting further that toxicants from marijuana cultivation still pose a threat. Additionally, exposure to multiple rodenticides significantly increased the likelihood of mortality from rodenticide poisoning. Poisoning was significantly more common in male than female fishers and was 7 times more likely than disease to kill males. Based on necropsy findings, suspected causes of mortality based on field evidence alone tended to underestimate the frequency of disease-related mortalities. This study is the first comprehensive investigation of mortality causes of fishers and provides essential information to assist in the conservation of this species.

Pregnancy diagnosis in wild canids using a commercially available relaxin assay

Accurate detection of pregnancy is a useful tool in zoo management and husbandry, conservation breeding programs and research settings. Our study evaluated the ability of a commercial relaxin hormone assay used in domestic dogs (ReproCHEK(TM)) to accurately detect pregnancy through plasma analysis in two wolf and two fox species. The relaxin assay detected all of the pregnancies greater than 25 days gestation for island foxes, fennec foxes, gray wolves, and Mexican gray wolves. For island foxes, three negative relaxin results were attributed to using the test earlier postconception than manufacturer recommendation (before day 20). Five other negative results were found for females estimated at 15-25 days gestation, spanning the early and intermediate period (21-30 days gestation) when relaxin may be detected but less reliably. There were no false-positive results in nonmated negative control animals. Relaxin assay results were highly correlated with ultrasound results and the intra-assay replicate agreement was 100%. Our results show that the ReproCHEK(TM) commercial relaxin assay is a minimally invasive and reliable method for pregnancy detection in these wild species when used after 25 days gestation and might be applied to other canids as well. Furthermore, this assay is easy to run and requires no specialized equipment, making it extremely useful for zoo and field research applications. Zoo Biol 27:406-413, 2008. (c) 2008 Wiley-Liss, Inc.

Pathology and epidemiology of ceruminous gland tumors among endangered santa catalina island foxes (Urocyon littoralis catalinae) in the channel Islands, USA

In this study, we examined the prevalence, pathology, and epidemiology of tumors in free-ranging island foxes occurring on three islands in the California Channel Islands, USA. We found a remarkably high prevalence of ceruminous gland tumors in endangered foxes (Urocyon littoralis catalinae) occurring on Santa Catalina Island (SCA)—48.9% of the dead foxes examined from 2001–2008 had tumors in their ears, and tumors were found in 52.2% of randomly-selected mature (≥ 4 years) foxes captured in 2007–2008, representing one of the highest prevalences of tumors ever documented in a wildlife population. In contrast, no tumors were detected in foxes from San Nicolas Island or San Clemente Island, although ear mites (Otodectes cynotis), a predisposing factor for ceruminous gland tumors in dogs and cats, were highly prevalent on all three islands. On SCA, otitis externa secondary to ear mite infection was highly correlated with ceruminous gland hyperplasia (CGH), and tumors were significantly associated with the severity of CGH, ceruminous gland dysplasia, and age group (older foxes). We propose a conceptual model for the formation of ceruminous gland tumors in foxes on SCA that is based on persistent, ubiquitous infection with ear mites, and an innate, over exuberant inflammatory and hyperplastic response of SCA foxes to these mites. Foxes on SCA are now opportunistically treated with acaricides in an attempt to reduce mite infections and the morbidity and mortality associated with this highly prevalent tumor.

Serum chemistry, hematologic, and post-mortem findings in free-ranging bobcats (Lynx rufus) with notoedric mange.

Abstract:  Notoedric mange was responsible for a population decline of bobcats (Lynx rufus) in 2 Southern California counties from 2002–2006 and is now reported to affect bobcats in Northern and Southern California. With this study we document clinical laboratory and necropsy findings for bobcats with mange. Bobcats in this study included free-ranging bobcats with mange (n = 34), a control group of free-ranging bobcats without mange (n = 11), and a captive control group of bobcats without mange (n = 19). We used 2 control groups to evaluate potential anomalies due to capture stress or diet. Free-ranging healthy and mange-infected bobcats were trapped or salvaged. Animals were tested by serum biochemistry, complete blood count, urine protein and creatinine, body weight, necropsy, and assessment for anticoagulant rodenticide residues in liver tissue. Bobcats with severe mange were emaciated, dehydrated, and anemic with low serum creatinine, hyperphosphatemia, hypoglycemia, hypernatremia, and hyperchloremia, and sometimes septicemic when compared to control groups. Liver enzymes and leukocyte counts were elevated in free-ranging, recently captured bobcats whether or not they were infested with mange, suggesting capture stress. Bobcats with mange had lower levels of serum cholesterol, albumin, globulin, and total protein due to protein loss likely secondary to severe dermatopathy. Renal insufficiency was unlikely in most cases, as urine protein:creatinine ratios were within normal limits. A primary gastrointestinal loss of protein or blood was possible in a few cases, as evidenced by elevated blood urea nitrogen, anemia, intestinal parasitism, colitis, gastric hemorrhage, and melena. The prevalence of exposure to anticoagulant rodenticides was 100% (n = 15) in bobcats with mange. These findings paint a picture of debilitating, multisystemic disease with infectious and toxic contributing factors that can progress to death in individuals and potential decline in populations.