Wrote the paper: DS TPA KMN RBC DD JB MN CER.
The authors have declared that no competing interests exist.
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 (
Oral rabies vaccination (ORV) represents a socially acceptable methodology that may be applied on a broad geographic scale to manage the disease in specific terrestrial wildlife reservoirs, as well as in free-ranging or feral dog (
To date, ORV has been successfully applied to eliminate rabies among red foxes (
Currently, ORV use in the US remains focused on preventing raccoon (
Each ORV program is faced with multiple complexities
This paper draws largely from specific examples of contemporary wildlife rabies control programs in North America to illustrate key ecological, biological, logistical, and environmental complexities and challenges, and the initiatives taken to achieve success.
Literature searches included the use of Scopus via access through the USDA National Agricultural Library, and EBSCO Host Academic Search Premier via the University of New Hampshire's Dimond Library. Assistance in publication acquisition was provided by the USDA, Wildlife Services National Wildlife Research Center Library staff. Keyword searches included the following terms:
A broad scientific, regulatory, and management interface exists among the public health, agriculture, and wildlife management agencies responsible for specific rabies prevention and control activities in the US. Each state and federal agency has statutory authority and a public trust niche to achieve specific agency missions. As a consequence, planning, implementing, and coordinating effective rabies prevention and control necessitates inter-jurisdictional collaboration among diverse disciplines and authorities.
A national rabies management team approach has been applied in the US since 1999 to facilitate coordination of ORV programs across state and international boundaries in North America targeting specific rabies virus host reservoirs. The National Rabies Management Team is currently composed of nine smaller working groups focused on key topic areas such as surveillance, vaccine development, rabies control strategies, and research prioritization. The team meets annually to assess and discuss key issues and provides guidance for a spectrum of national wildlife rabies prevention and control goals
The signing of the North American Rabies Management Plan (NARMP) in October 2008 by representatives from Canada, Mexico, the US, and the Navajo Nation extends collaboration across national boundaries and multiple disciplines in four focus areas: communications, surveillance, control, and research. A fundamental tenet of the NARMP is that rabies prevention and control programs can be enhanced through an international collaborative framework. The formalization of this plan has spawned several proposed collaborative initiatives for 2009. Examples include a comparison of ORV performance between New Brunswick, Canada, and Maine, US, and closer coordination between border states and provinces involved in raccoon rabies control. Other examples include replication of the first ORV campaigns targeting dogs in Mexico, improved enhanced rabies surveillance along the Mexico-US border, and captive studies with the GnRH immunocontraceptive GonaCon in Mexico
Rabies surveillance is traditionally based on human or domestic animal exposure events brought to the attention of public health officials
Enhanced rabies surveillance to support ORV in the US focuses on the following types of samples: strange acting (extremely aggressive or docile) animals where no human or domestic animal exposure has been reported, road kills, animals found dead in addition to road kills, animals with injuries or lesions indicative of highly aggressive behavior, and euthanized animals from focal trapping at sites where rabid animals were recently confirmed. Not uncommonly, raccoons captured by nuisance wildlife control operators are included as enhanced rabies samples
The enhanced surveillance zone for raccoons typically extends from the areas where raccoon rabies is enzootic, through the ORV zone, to approximately 80 km into areas suspected to be free of raccoon rabies (
Substantial increases in suspect rabid animal samples under the enhanced rabies surveillance protocol often create an undue burden on state laboratories for timely diagnosis. Application of a direct rapid immunohistochemistry test (dRIT) developed at the Centers for Disease Control and Prevention (CDC) in the US
The value of enhancing rabies surveillance beyond levels typically conducted for the protection of public health was illustrated in northeast Ohio during 2007. This area is characterized by heavy commercial business and residential developments typical of suburbia (Cleveland metropolitan area). Since 2004, when rabies was first detected in this area (10 km west of the existing Appalachian ORV zone at that time), surveillance has been enhanced resulting in WS submitting 5,554 animals (through 2008) for rabies testing. In each year except 2007, rabies positive cases were detected through the public health surveillance system as well. From 2004–2006, there had been declining rabies cases, suggesting a trend toward rabies-free status in this contingency action area. In 2007, all rabies positive cases in this area were detected as a function of enhanced surveillance (
Since 16 July 2004 when raccoon rabies virus variant was first detected west of the existing oral rabies vaccination zone, 117 animals have been confirmed positive with raccoon variant within the contingency action zone. In 2007, no cases were detected via the public health surveillance system, illustrating the need for enhanced rabies surveillance.
A large-scale trap-vaccinate-release (TVR) operation was conducted near Cleveland, Ohio, in 2008 and resulted in the hand vaccination of 4,196 raccoons and the brainstem testing of 138 raccoons and 77 skunks. The TVR zone consisted of 185 cells (1 km2 in size) and was delineated from raccoon variant rabies cases confirmed in the Contingency Action ORV zone in 2007 (
Raccoon rabies was first described in Florida in the 1940s
During the 1990s, coordinated operational raccoon rabies control programs in the US expanded from small scale projects in five states (Florida, Massachusetts, Maryland, New Jersey, New York) to include portions of 16 states by 2005
Obviously, lower indices to population immunity connote a greater risk of ORV zone compromise and a reduced ability to sustain effective programs, highlighting the need for improved or new baits and vaccines and strategy refinements. Frequent spillover of raccoon rabies virus variant into the striped skunk
In the US, a contingency action has continued in northeast Ohio since 2004, when raccoon rabies emerged 10 km west of the established ORV zone
Contingency actions are an integral component of rabies management strategies in meso-carnivores to address local emergencies that may arise during normal ORV operations. However, such actions are labor intensive and wrought with logistical and environmental challenges that mandate careful coordination with the attendant high cost per unit area treated in comparison to regularly planned ORV campaigns. Comprehensive economic analysis of the benefits and costs associated with the 2008 contingency action in Ohio are in progress and will be compared to earlier reported estimates from Ontario that suggest the costs are approximately 2.5 times greater than ORV for a similar area
Key among the many challenges implicit in rabies control is the pervasiveness of the translocation of raccoons and other meso-carnivores
Adaptive methods for enhanced effectiveness in rabies control require attention to a broad range of research needs. These include ecology of reservoir species, an understanding of target and non-target species foraging behaviors, community dynamics of the meso-carnivore complex, bait uptake relative to a suite of species-specific spatio-temporal variables, and model development to support ORV decision making. Chief among these is the need for improved or new baits and vaccines that lead to enhanced field performance in raccoons and other species to reduce dependency on contingency actions and allow a shift in focus toward elimination strategies. This need is driven in part by rabies virus spillover and establishment among several sympatric meso-carnivores in North America
Notable examples of this dilemma have been documented in Alaska and Canada, where arctic fox rabies virus variant has spilled over into other animals, such as dogs and red foxes
In Ontario, field trials were conducted recently with a human adenovirus recombinant vaccine (ONRAB) developed with the intent that its strategic use will facilitate the elimination of the fox rabies foci maintained by skunks in southern Ontario
Tetracycline has had a long history as a biomarker in wildlife management, including extensive use in evaluating bait uptake in ORV campaigns
In 2001, apparent spillover of big brown bat rabies virus variant resulted in 19 documented cases in skunks near Flagstaff, indicative of transmission among skunks
The cost effectiveness of the shifting paradigm toward controlling rabies in meso-carnivore reservoirs should and will receive continual scrutiny. To date, studies of the benefits and costs have concluded that under specific assumptions and scenarios, ORV is a viable rabies management alternative
Concerns linger among some wildlife managers over potentially negative consequences from rabies control to species of conservation concern
Establishment of a rabies management team composed of a coalition of diverse expertise from the public health-agriculture-wildlife management interface has been critical to facilitate coordination among rabies control programs targeting meso-carnivores in the US. The NARMP has established a continental framework that extends collaboration and coordination, capacity for rabies communications, surveillance, control, and research among Canada, Mexico, and the US. Enhanced surveillance as a complement to public health surveillance has improved decision-making capability regarding allocation of rabies control resources, including contingency actions to address emergencies, as illustrated in Ohio. Raccoon rabies has not spread appreciably since ORV intervention has expanded in the eastern US, yet rabies virus neutralizing antibody levels in raccoon populations as an index to immune buffers in existing ORV zones point to the need for improved or new baits, oral vaccines, and strategy refinements. Achieving advances that lead to improved field performance should allow for a more aggressive movement of ORV zones into raccoon enzootic areas. Measureable successes beyond containment would be expected to enhance program sustainability toward the goal of broader scale elimination of raccoon rabies and ultimately other meso-carnivore rabies virus variants. Economic analyses will remain integral to ORV planning and as a means to characterize successes in costs and benefits. Conservation concerns related to control programs cannot be ignored and require additional study to better understand the role of rabies and other diseases on the population dynamics of meso-carnivores, such as the raccoon.
ORV represents a socially acceptable methodology that has helped eliminate canine rabies from the US, and restricted the distribution of raccoon, arctic fox, and gray fox variants of rabies in North America.
An international rabies management team composed of experts from the public health-agriculture-wildlife management interface has been vital to the establishment of viable rabies control programs in North America.
ORV in the US remains focused on the raccoon variant of rabies, while work continues to contain and eliminate the gray fox rabies variant in west Texas, and prevent canine rabies from re-emerging into the US from Mexico.
Advances in enhanced rabies surveillance that relies largely on a direct rapid immunohistochemistry test have led to improved real-time management decisions for meso-carnivore rabies reservoir species in the US.
ORV-related dog research in the southwestern US has potentially broad application in developing countries, where most of the 55,000 human rabies cases per year occur as the result of dog bites.
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We thank staff in the CDC Rabies Program for their laboratory contributions, due diligence, and diagnostic expertise, especially R. Franka, L. Greenberg, F. Jackson, I. Kuzmin, X. Ma, L. Orciari, O. Urozova, A. Velasco, and P. Yager. We also thank WS field staff working on rabies management programs in the following states: AL, AZ, CA, FL, GA, KS, KY, LA, MA, ME, MD, MI, MS, NH, NJ, NY, NC, OH, PA, TN, TX, VT, VA, WV, and WY for their technical skills and dedication, especially R. Hromack, T. Keller, J. Hoblet, J.P. Seman, C. Wellman, and B. Bjorklund. In addition, we would like to extend our gratitude to all the state public health departments that support enhanced rabies surveillance via testing specimens. Finally, we thank S. O'Dee with the Ohio Department of Health and P. Canac-Marquis and J. Mainguy with the Québec Ministère des Ressources naturelles et de la Faune for their contributions to this paper.
The findings and conclusions in this report are those of the authors and do not necessarily represent the views of their institutions.