Richard B. Chipman

Oral rabies vaccination in North America: opportunities, complexities, and challenges.

Steps to facilitate inter-jurisdictional collaboration nationally and continentally have been critical for implementing and conducting coordinated wildlife rabies management programs that rely heavily on oral rabies vaccination (ORV). Formation of a national rabies management team has been pivotal for coordinated ORV programs in the United States of America. The signing of the North American Rabies Management Plan extended a collaborative framework for coordination of surveillance, control, and research in border areas among Canada, Mexico, and the US. Advances in enhanced surveillance have facilitated sampling of greater scope and intensity near ORV zones for improved rabies management decision-making in real time. The value of enhanced surveillance as a complement to public health surveillance was best illustrated in Ohio during 2007, where 19 rabies cases were detected that were critical for the formulation of focused contingency actions for controlling rabies in this strategically key area. Diverse complexities and challenges are commonplace when applying ORV to control rabies in wild meso-carnivores. Nevertheless, intervention has resulted in notable successes, including the elimination of an arctic fox (Vulpes lagopus) rabies virus variant in most of southern Ontario, Canada, with ancillary benefits of elimination extending into Quebec and the northeastern US. Progress continues with ORV toward preventing the spread and working toward elimination of a unique variant of gray fox (Urocyon cinereoargenteus) rabies in west central Texas. Elimination of rabies in coyotes (Canis latrans) through ORV contributed to the US being declared free of canine rabies in 2007. Raccoon (Procyon lotor) rabies control continues to present the greatest challenges among meso-carnivore rabies reservoirs, yet to date intervention has prevented this variant from gaining a broad geographic foothold beyond ORV zones designed to prevent its spread from the eastern US. Progress continues toward the development and testing of new bait-vaccine combinations that increase the chance for improved delivery and performance in the diverse meso-carnivore rabies reservoir complex in the US.

Right Place, Wrong Species: A 20-Year Review of Rabies Virus Cross Species Transmission among Terrestrial Mammals in the United States

Introduction In the continental US, four terrestrial mammalian species are reservoirs for seven antigenic rabies virus variants. Cross species transmission (CST) occurs when a rabies virus variant causes disease in non-reservoir species. Methods This study analyzed national surveillance data for rabies in terrestrial mammals. The CST rate was defined as: number of rabid non-reservoir animals/number of rabid reservoir animals. CST rates were analyzed for trend. Clusters of high CST rate counties were evaluated using space-time scanning statistics. Results The number of counties reporting a raccoon variant CST rate >1.0 increased from 75 in 1992 to 187 in 2011; counties with skunk variant CST rates >1.0 remained unchanged during the same period. As of 2011, for every rabid raccoon reported within the raccoon variant region, there were 0.73 cases of this variant reported in non-reservoir animals. Skunks were the most common non-reservoir animal reported with the raccoon rabies variant. Domestic animals were the most common non-reservoir animal diagnosed with a skunk rabies virus variant (n = 1,601). Cross species transmission rates increased fastest among domestic animals. Conclusions Cross species transmission of rabies virus variants into non-reservoir animals increases the risk of human exposures and threatens current advances toward rabies control. Cross species transmission in raccoon rabies enzootic regions increased dramatically during the study period. Pet owners should vaccinate their dogs and cats to ensure against CST, particularly in regions with active foci of rabies circulation. Clusters of high CST activity represent areas for further study to better understand interspecies disease transmission dynamics. Each CST event has the potential to result in a rabies virus adapted for sustained transmission in a new species; therefore further understanding of the dynamics of CST may help in early detection or prevention of the emergence of new terrestrial rabies virus variants.

Safety And Immunogenicity Of Ontario Rabies Vaccine Bait (Onrab) In The First Us Field Trial In Raccoons ( Procyon lotor )

Abstract In 2011, we conducted a field trial in rural West Virginia, USA to evaluate the safety and immunogenicity of a live, recombinant human adenovirus (AdRG1.3) rabies virus glycoprotein vaccine (Ontario Rabies Vaccine Bait; ONRAB) in wild raccoons (Procyon lotor) and striped skunks (Mephitis mephitis). We selected ONRAB for evaluation because of its effectiveness in raccoon rabies management in Ontario and Quebec, Canada, and significantly higher antibody prevalence rates in raccoons compared with a recombinant vaccinia-rabies glycoprotein (V-RG) vaccine, Raboral V-RG®, in US–Canada border studies. Raccoon rabies was enzootic and oral rabies vaccination (ORV) had never been used in the study area. We distributed 79,027 ONRAB baits at 75 baits/km2 mostly by fixed-wing aircraft along parallel flight lines at 750-m intervals. Antibody prevalence was significantly higher at 49.2% (n = 262) in raccoons after ONRAB was distributed than the 9.6% (n = 395) before ORV. This was the highest antibody prevalence observed in raccoons by US Department of Agriculture Wildlife Services for areas with similar management histories evaluated before and after an initial ORV campaign at 75 baits/km2 with Raboral V-RG. Tetracycline biomarker (TTCC) was significantly higher among antibody-positive raccoons after ONRAB baiting and was similar among raccoons before ORV had been conducted, an indication of vaccine-induced rabies virus–neutralizing antibody production following consumption of bait containing TTCC. Skunk sample size was inadequate to assess ONRAB effects. Safety and immunogenicity results supported replication of this field trial and led to a recommendation for expanded field trials in 2012 to evaluate safety and immunogenicity of ground-distributed ONRAB at 150 baits/km2 in residential and commercial habitats in Ohio, USA and aerially distributed ONRAB at 75 baits/km2 in rural habitats along US–Quebec border.

Arthropods of a semi-natural grassland in an urban environment: the John F. Kennedy International Airport, New York

Semi-natural grassland habitat fragments, such as those found on airports, might be important for arthropod conservation and biodiversity in urban ecosystems. The objectives of this study were to: (1) describe the arthropod communities present within the grasslands on the John F. Kennedy International Airport and (2) assess spatial and temporal variation in those arthropod communities. We collected arthropods using a vacuum sampler during 2003 and using sweep-net collection methods during 2003 and 2004. During 2003, a total of 1,467 arthropods, representing 17 orders and 68 families were found in vacuum samples. A total of 3,784 arthropods, representing 12 orders and 94 families were collected in sweep-net samples during 2003. In 2004, a total of 3,281 arthropods, representing 12 orders and 85 families were collected in sweep-net samples. Hemiptera, Orthoptera, and Diptera were the most abundant taxa, accounting for 47, 18, and 14% of all arthropods captured, respectively. We found evidence of spatial and temporal variation in arthropod abundance, in particular as noted by fluctuations in Orthoptera: Acrididae and Hemiptera: Auchenorrhyncha. Hemipteran family diversity was also influenced by habitat type. Grassland habitats on airfields, although influenced by anthropogenic factors (e.g., mowing), have the potential to provide abundant and diverse arthropod communities and might serve as a refugium for such species within urban ecosystems.

National surveillance for human and pet contact with oral rabies vaccine baits, 2001-2009.

OBJECTIVE To determine the rate and absolute number of human and pet exposures to oral rabies vaccine (ORV) bait containing liquid vaccinia rabies glycoprotein recombinant vaccine and to evaluate factors that might affect human contact with bait to modify the program and reduce human exposure to the vaccine. DESIGN Retrospective analysis of surveillance data (2001 to 2009). SAMPLE Reports on human and pet contact with ORV baits in states with ORV surveillance programs. PROCEDURES Data were collected from passive, multistate ORV surveillance systems in Alabama, Arizona, Florida, Georgia, Maine, Maryland, Massachusetts, New Hampshire, New Jersey, New York, North Carolina, Ohio, Pennsylvania, Tennessee, Texas, Vermont, Virginia, and West Virginia. Data collected included the nature of human or pet contact with bait and vaccine, the callers knowledge of the ORV bait program, local human population density, and other relevant demographic data. RESULTS All 18 states participated in the surveillance program for at least 1 year, for a combined 68 years of observation. One thousand four hundred thirty-six calls were reported, representing 3,076 found baits (6.89/100,000 baits dropped); 296 (20%) calls were related to human contact with ruptured bait, and 550 (38%) involved pet contact with the bait. Six adverse events in humans were reported, one of which required hospitalization. Fifty-nine adverse events in pets were noted, all of which were nonserious. CONCLUSIONS AND CLINICAL RELEVANCE Findings from surveillance activities have been used to improve baiting strategies and minimize human and pet contact with ORV baits. Overall, human and pet contact with ORV baits was infrequent. Surveillance has led to early identification of persons exposed to ORV and rapid intervention.

Temporal Variation in Terrestrial Invertebrate Consumption by Laughing Gulls in New York

Abstract Laughing gulls (Larus atricilla) are commonly found in many areas of North America and little is known about their diet, particularly in coastal-urban interfaces where gull-aircraft collisions can be a serious concern. The objective of this study was to describe and quantify the consumption of terrestrial invertebrates by laughing gulls at a coastal-urban interface in the northeastern United States. We examined the stomach contents of laughing gulls (n  =  1053) collected during wildlife damage management operations at John F. Kennedy International Airport during the summers of 2003 and 2004. Terrestrial invertebrates consumed by laughing gulls represented 2 taxonomic phyla, 4 classes, 15 orders and 40 families. Beetles (Coleoptera) and ants (Hymenoptera) were the most common terrestrial invertebrates consumed by laughing gulls. We found evidence of temporal (i.e., monthly) variation in the frequency of occurrence of terrestrial insects in laughing gull diets. Laughing gull gender and age did not influence the frequency of occurrence of terrestrial insects in gull diets. Terrestrial environments (e.g., areas of turfgrass) appear to provide important foraging locations and food resources for laughing gulls in coastal-urban areas. This information is important for developing effective management approaches to reduce human-gull conflicts, such as gull-aircraft collisions at coastal airports.

Evaluation of immune responses in dogs to oral rabies vaccine under field conditions

During the 20th century parenteral vaccination of dogs at central-point locations was the foundation of successful canine rabies elimination programs in numerous countries. However, countries that remain enzootic for canine rabies have lower infrastructural development compared to countries that have achieved elimination, which may make traditional vaccination methods less successful. Alternative vaccination methods for dogs must be considered, such as oral rabies vaccine (ORV). In 2016, a traditional mass dog vaccination campaign in Haiti was supplemented with ORV to improve vaccination coverage and to evaluate the use of ORV in dogs. Blisters containing live-attenuated, vaccine strain SPBNGAS-GAS were placed in intestine bait and distributed to dogs by hand. Serum was collected from 107 dogs, aged 3-12 months with no reported prior rabies vaccination, pre-vaccination and from 78/107 dogs (72.9%) 17 days post-vaccination. The rapid florescent focus inhibition test (RFFIT) was used to detect neutralizing antibodies and an ELISA to detect rabies binding antibodies. Post-vaccination, 38/41 (92.7%) dogs that received parenteral vaccine had detectable antibody (RFFIT >0.05 IU/mL), compared to 16/27 (59.3%, p < 0.01) dogs that received ORV or 21/27 (77.8%) as measured by ELISA (>40% blocking, p < 0.05). The fate of 291 oral vaccines was recorded; 283 dogs (97.2%) consumed the bait; 272 dogs (93.4%) were observed to puncture the blister, and only 14 blisters (4.8%) could not be retrieved by vaccinators and were potentially left in the environment. Pre-vaccination antibodies (RFFIT >0.05 IU/mL) were detected in 10/107 reportedly vaccine-naïve dogs (9.3%). Parenteral vaccination remains the most reliable method for ensuring adequate immune response in dogs, however ORV represents a viable strategy to supplement existing parental vaccination campaigns in hard-to-reach dog populations. The hand-out model reduces the risk of unintended contact with ORV through minimizing vaccine blisters left in the community.

Reducing Impacts of Double-Crested Cormorants to Natural Resources in Central New York: A Review of a Collaborative Research, Management, and Monitoring Program

Abstract. Double-crested Cormorants (Phalacrocorax auritus) have used central New York waters for breeding and stopover habitats during migration since 1984. In response to public concern over Oneida Lake, the United States Department of Agriculture Wildlife Services and the New York State Department of Environmental Conservation initiated an integrated research, management and monitoring program aimed at mitigating cormorant impacts to fisheries and other natural resources in 1998. The history of this program was reviewed and efforts to reduce negative impacts of the Double-crested Cormorant population in central New York described. Management was successful, as demonstrated by a substantial decrease in cormorant use of Oneida Lake during spring, summer and fall seasons, and the apparent recovery of certain sportfish populations. Research identified cormorant movement patterns within and among water bodies and documented cormorant responses to hazing and other management techniques. The cormorant management program in central New York was intended to keep cormorant use of Oneida Lake at a level that prevents unsustainable impacts to fisheries populations.

Field Studies Evaluating Bait Acceptance and Handling by Dogs in Navajo Nation, USA

Mass parenteral vaccination remains the cornerstone of dog rabies control. Oral rabies vaccination (ORV) could increase vaccination coverage where free-roaming dogs represent a sizeable segment of the population at risk. ORV’s success is dependent on the acceptance of baits that release an efficacious vaccine into the oral cavity. A new egg-flavored bait was tested alongside boiled bovine intestine and a commercially available fishmeal bait using a hand-out model on the Navajo Nation, United States, during June 2016. A PVC capsule and biodegradable sachet were tested, and had no effect on bait acceptance. The intestine baits had the highest acceptance (91.9%; 95% confidence interval (CI), 83.9–96.7%), but the fishmeal (81.1%; 95% CI, 71.5–88.6%) and the egg-flavored baits (77.4%; 95% CI, 72.4–81.8%) were also well accepted, suggesting that local bait preference studies may be warranted to enhance ORV’s success in other areas where canine rabies is being managed. Based on a dyed water marker, the delivery of a placebo vaccine was best in the intestine baits (75.4%; 95% CI, 63.5–84.9%), followed by the egg-flavored (68.0%; 95% CI, 62.4–73.2%) and fishmeal (54.3%; 95% CI, 42.9–65.4%) baits. Acceptance was not influenced by the supervision or ownership, or sex, age, and body condition of the dogs. This study illustrates that a portion of a dog population may be orally vaccinated as a complement to parenteral vaccination to achieve the immune thresholds required to eliminate dog rabies.

Management and modeling approaches for controlling raccoon rabies: The road to elimination

Rabies is an ancient viral disease that significantly impacts human and animal health throughout the world. In the developing parts of the world, dog bites represent the highest risk of rabies infection to people, livestock, and other animals. However, in North America, where several rabies virus variants currently circulate in wildlife, human contact with the raccoon rabies variant leads to the highest per capita population administration of post-exposure prophylaxis (PEP) annually. Previous rabies variant elimination in raccoons (Canada), foxes (Europe), and dogs and coyotes (United States) demonstrates that elimination of the raccoon variant from the eastern US is feasible, given an understanding of rabies control costs and benefits and the availability of proper tools. Also critical is a cooperatively produced strategic plan that emphasizes collaborative rabies management among agencies and organizations at the landscape scale. Common management strategies, alone or as part of an integrated approach, include the following: oral rabies vaccination (ORV), trap-vaccinate-release (TVR), and local population reduction. As a complement, mathematical and statistical modeling approaches can guide intervention planning, such as through contact networks, circuit theory, individual-based modeling, and others, which can be used to better understand and predict rabies dynamics through simulated interactions among the host, virus, environment, and control strategy. Strategies derived from this ecological lens can then be optimized to produce a management plan that balances the ecological needs and program financial resources. This paper discusses the management and modeling strategies that are currently used, or have been used in the past, and provides a platform of options for consideration while developing raccoon rabies virus elimination strategies in the US.