Foxes, skunks spreading bat rabies variant in Arizona

Authorities monitoring the adapted virus during record year for rabies cases
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Foxes and skunks in northern Arizona are spreading an adapted version of a rabies virus variant associated with bats.

The state is also enduring a second consecutive record year for rabies cases in animals.

More than 200 animals in the state tested positive for rabies in the first nine months of 2009, including dozens of foxes and skunks that were infected with a bat virus variant that has adapted and spread among those terrestrial mammals. By contrast, only 176 rabid animals were discovered in all of 2008.

Trapped skunk
In response to a recent outbreak of an adapted bat rabies viral variant in terrestrial mammals, skunks in Arizona were trapped, vaccinated, and released.

Craig Levy, an epidemiologist and the manager of the vector-borne disease program for the Arizona Department of Health Services, said southern Arizona has historically had reservoirs of the gray fox rabies strain and the south-central skunk variant, and the state has multiple bat virus variants. But in 2001, the state had an unusual outbreak of rabies among skunks in Flagstaff, which is in northern Arizona.

"We never saw rabid skunks that far north in Arizona," Levy said. "So we knew something was out of whack, and we had those skunks variant-typed to find out what type of virus we were talking about.

"And it turns out that the skunks were transmitting big brown bat variant, but it was going skunk to skunk to skunk."

A scientific report in the August 2006 issue of Emerging Infectious Diseases, "Bat-associated rabies virus in skunks," states that 19 skunks in Flagstaff were confirmed to be infected with a bat-associated rabies virus variant in 2001.

"This is the largest recorded cluster of bat RABVV (rabies virus variant) infection in terrestrial mammals," the report states.

"Investigation of this novel outbreak showed evolution in action with the emergence of an RABVV that successfully adapted from Chiroptera to Carnivora."

The report also states the variant reappeared in five skunks and a fox in 2004. By late 2008, foxes were transmitting the variant to other foxes, Levy said.

"We may have some evolution occurring right before our eyes as we see a different virus variant circulating very efficiently within the wrong host," Levy said.

Rabies virus variants are genetically distinct strains, and information from the CDC indicates those variants are typically maintained in a single reservoir host species.

A 2009 circular from the U.S. Geological Survey National Wildlife Health Center, "Bat rabies and other lyssavirus infections," states that, after transmission of a variant from its reservoir host to an atypical or aberrant host species, "a dead-end infection usually results because the maladapted atypical host quickly dies before the virus can be transmitted further."

"Identification of variants that infect atypical hosts, such as humans, usually points to a particular natural reservoir host species, such as a species of carnivore or bat, as the source of human infection," the report states.

David Bergman, the state director of USDA Wildlife Services in Arizona, said a higher human population in the state, an increase in recreational activity in the state, and increased rabies awareness are connected with the record number of reported rabies cases.

Bergman said it is concerning that terrestrial wildlife is transmitting rabies near Flagstaff for the first time in 40 years.

Part of the overall rise in rabies cases is related to a normal cycle of infections, said Dr. Charles E. Rupprecht, chief of the rabies program of the national Centers for Disease Control and Prevention. But the outbreak of a bat rabies variant among terrestrial mammals in Arizona is unusual.

As people create comfortable human habitats in the desert, wildlife thrives in the same areas, Dr. Rupprecht said. Skunks are grassland animals that do not typically live in high densities in deserts, he said, but construction of golf courses near Flagstaff gave them room to thrive, and high population density likely is related to the adaptation of the rabies virus variant associated with brown bats.

The adapted variant is now demonstrating how viruses adapt and emerge, Dr. Rupprecht said. And there is a risk that, if it is truly adapted to fox species, it could spread into the Navajo Nation and cause an outbreak in unvaccinated dogs.  

Navajo Nation borders the outbreak zone

Dr. Scott C. Bender, senior tribal veterinarian for the Navajo Nation Veterinary Program, said the Navajo Nation has not identified infection with a terrestrial rabies variant in a dog since the 1940s, but the nation typically has one or two bats test positive for rabies yearly. The nation is slightly larger than West Virginia and extends into Arizona, New Mexico, and Utah.  

The Navajo Nation's border is also 10 miles from Flagstaff, and high desert country is the only barrier, Dr. Bender said. The nation's residents frequently travel to Flagstaff to adopt cats and dogs.

He and the nation's other veterinarian have frequently vaccinated dogs against rabies, and the Indian Health Service hosts an annual rabies clinic, but estimates indicate only between 5 percent and 15 percent of owned dogs on Navajo land are vaccinated.

Dr. Bender said his office has been investigating the use of oral rabies vaccines in feral and semiferal dogs as well as the use in dogs of a birth control vaccine developed for use in deer. The research has included pen and field trials of the available rabies vaccine and oral rabies vaccine baits, and at press time he expected some of the results would be presented at the International Conference on Rabies in the Americas in October in Quebec City.

Dr. Bender said it is fascinating to watch the virus's proliferation in foxes and skunks prove some theories about adaptation correct. He said it is likely similar to the time when lyssaviruses such as rabies first jumped from a bat into a terrestrial mammal.

But the fascination is accompanied by concern, Dr. Bender said, and his program is monitoring for outbreaks and performing research to reduce the risk dogs will become infected and potentially expose people to the virus. Any positive tests for the virus would be followed by a community vaccination clinic and, likely, a reduction in the feral dog population.

Outbreak centered in Flagstaff

Coconino County, the northern Arizona county that includes Flagstaff, had through early October identified 32 rabid animals, including 22 foxes and five skunks. Levy said he thinks the vast majority of the foxes and all the other animals had the big brown bat rabies virus variant.

The adapted virus is transmitted the same way as other rabies strains, and there is no indication it is more infectious, Levy said. Treatment for humans or animals exposed to the strain would be the same as for any other rabies exposure.

"It's still rabies virus and probably being transmitted by way of animal bites or saliva exposures," Levy said.

The Department of Agriculture's Wildlife Services, the Coconino County Health Department, the Arizona Department of Health Services, local animal control officials, the Arizona Game and Fish Department, and partners on Indian lands have worked together on surveillance and wildlife vaccination, Levy said.

The county health department imposed quarantine zones to make sure pets were vaccinated and people obeyed leash laws, Levy said.

Wildlife Services was involved in the distribution in July of more than 130,000 vaccine baits, mostly by air, to create herd immunity in foxes, Bergman said. The air drops of oral rabies vaccine were the first in the state, and the baits were dropped within about 15 miles of every known rabies case in the Flagstaff area.

About 110 skunks were also trapped, vaccinated, and released, Bergman said. The oral rabies vaccine baits do not work on skunks.

Increased surveillance and laboratory testing have been used to monitor the virus variant's prevalence and distribution, Levy said, and the adapted rabies virus variant appears to still be isolated to northern Arizona. Health authorities have recorded an above-average number of rabies cases in animals in the rest of the state, but Levy said, "A lot of our rabies activity in our terrestrial mammals is all driven by natural animal population fluctuation."