• View in gallery

    Distribution of major rabies virus variants among mesocarnivore reservoirs in the United States and Puerto Rico, 2008 to 2012. *Potential host shift event.

  • View in gallery

    Cases of rabies among wildlife in the United States, by year and species, 1983 to 2012.

  • View in gallery

    Reported cases of rabies involving raccoons, by county, 2012. Histogram represents number of counties in each category for total number of raccoons submitted for testing.

  • View in gallery

    Reported cases of rabies involving bats, by county, 2012. Histogram represents number of counties in each category for total number of bats submitted for testing.

  • View in gallery

    Reported cases of rabies involving skunks, by county, 2012. Histogram represents number of counties in each category for total number of skunks submitted for testing.

  • View in gallery

    Reported cases of rabies involving foxes, by county, 2012. Histogram represents number of counties in each category for total number of foxes submitted for testing.

  • View in gallery

    Reported cases of rabies involving cats and dogs, by county, 2012. Histogram represents number of counties in each category for total number of cats and dogs submitted for testing.

  • 1. Manning SE, Rupprecht CE, Fishbein D. Human rabies prevention—United States, 2008: recommendations of the Advisory Committee on Immunization Practices. MMWR Recomm Rep 2008; 57: 128.

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  • 2. Rupprecht CE, Briggs D, Brown CM, et al. Use of a reduced (4-dose) vaccine schedule for postexposure prophylaxis to prevent human rabies: recommendations of the advisory committee on immunization practices. MMWR Recomm Rep 2010; 59: 19.

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  • 3. Recuenco S, Eidson M, Cherry B, et al. Factors associated with endemic raccoon (Procyon lotor) rabies in terrestrial mammals in New York State, USA. Prev Vet Med 2008; 86: 3042.

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  • 4. Freuling CM, Hampson K, Selhorst T, et al. The elimination of fox rabies from Europe: determinants of success and lessons for the future. Philos Trans R Soc Lond B Biol Sci 2013; 368: 20120142.

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  • 5. Slate D, Algeo TP, Nelson KM, et al. Oral rabies vaccination in North America: opportunities, complexities, and challenges. PLoS Negl Trop Dis [serial online]. 2009; 3:e549. Available at: www.plosntds.org/article/info%3Adoi%2F10.1371%2Fjournal.pntd.0000549. Accessed Jun 1, 2013.

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  • 6. Rosatte RC, Donovan D, Allan M, et al. The control of raccoon rabies in Ontario Canada: proactive and reactive tactics, 1994–2007. J Wildl Dis 2009; 45: 772784.

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  • 7. Petersen BA, Rupprecht C. Human rabies epidemiology and diagnosis. In: Tkachev S, ed. Non-Flavivirus encephalitis. New York: InTech, 2011;247278.

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  • 8. Brown CM. Compendium of animal rabies prevention and control, 2011. National Association of State and Public Health Veterinarians, Inc. MMWR Recomm Rep 2011; 60(RR-6):117.

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  • 9. Davis AD, Dupuis M, Rudd RJ. Extended incubation period of rabies virus in a captive big brown bat (Eptesicus fuscus). J Wildl Dis 2012; 48: 508511.

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  • 10. CDC. 2012 nationally notifiable diseases and conditions and current case definitions. Atlanta: CDC, 2012.

  • 11. Ronald G, Powell J, Raj P, et al. Protocol for postmortem diagnosis of rabies in animals by direct fluorescent antibody testing: a minimum standard for rabies diagnosis in the United States. Atlanta: CDC, 2003. Available at: www.cdc.gov/rabies/pdf/rabiesdfaspv2.pdf. Accessed Aug 13, 2013.

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  • 12. Lembo T, Niezgoda M, Velasco-Villa A, et al. Evaluation of a direct, rapid immunohistochemical test for rabies diagnosis. Emerg Infect Dis 2006; 12: 310313.

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  • 13. Blanton JD, Robertson K, Palmer D, et al. Rabies surveillance in the United States during 2008. J Am Vet Med Assoc 2009; 235: 676689.

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  • 14. US Census Bureau. 2010 Census summary file. Washington, DC: US Census Bureau, 2010.

  • 15. Blanton JD, Dyer J, McBrayer J, et al. Rabies surveillance in the United States during 2011. J Am Vet Med Assoc 2012; 241: 712722.

  • 16. Blanton JD, Hanlon CA, Rupprecht CE. Rabies surveillance in the United States during 2006. J Am Vet Med Assoc 2007; 231: 540556.

  • 17. CDC. U.S-acquired human rabies with symptom onset and diagnosis abroad, 2012. MMWR Morb Mortal Wkly Rep 2012; 61: 777781.

  • 18. Christian KA, Blanton JD, Auslander M, et al. Epidemiology of rabies post-exposure prophylaxis—United States of America, 2006–2008. Vaccine 2009; 27: 71567161.

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  • 19. Knobel DL, Cleaveland S, Coleman PG, et al. Re-evaluating the burden of rabies in Africa and Asia. Bull World Health Organ 2005; 83: 360368.

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  • 20. WHO. WHO expert consultation on rabies. Second report. World Health Organ Tech Rep Ser 2013; 982: 1139.

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  • 22. Thiede H, Close NS, Koepsell J, et al. Completeness of reporting of rabies postexposure prophylaxis in King County, Washington. J Public Health Manag Pract 2008; 14: 448453.

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  • 23. Vora NM, Basavaraju SV, Feldman KA, et al. Raccoon rabies virus variant transmission through solid organ transplantation. JAMA 2013; 310: 398407.

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Rabies surveillance in the United States during 2012

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  • 1 Poxvirus and Rabies Branch, Division of High-Consequence Pathogens and Pathology, National Center for Emerging and Zoonotic Infectious Disease, CDC, 1600 Clifton Rd NE, Atlanta, GA 30333.
  • | 2 Poxvirus and Rabies Branch, Division of High-Consequence Pathogens and Pathology, National Center for Emerging and Zoonotic Infectious Disease, CDC, 1600 Clifton Rd NE, Atlanta, GA 30333.
  • | 3 Poxvirus and Rabies Branch, Division of High-Consequence Pathogens and Pathology, National Center for Emerging and Zoonotic Infectious Disease, CDC, 1600 Clifton Rd NE, Atlanta, GA 30333.
  • | 4 Poxvirus and Rabies Branch, Division of High-Consequence Pathogens and Pathology, National Center for Emerging and Zoonotic Infectious Disease, CDC, 1600 Clifton Rd NE, Atlanta, GA 30333.
  • | 5 Poxvirus and Rabies Branch, Division of High-Consequence Pathogens and Pathology, National Center for Emerging and Zoonotic Infectious Disease, CDC, 1600 Clifton Rd NE, Atlanta, GA 30333.
  • | 6 Poxvirus and Rabies Branch, Division of High-Consequence Pathogens and Pathology, National Center for Emerging and Zoonotic Infectious Disease, CDC, 1600 Clifton Rd NE, Atlanta, GA 30333.

Abstract

SUMMARY—During 2012, 49 states and Puerto Rico reported 6,162 rabid animals and 1 human rabies case to the CDC, representing a 2.1% increase from the 6,031 rabid animals and 6 human cases reported in 2011. Approximately 92% of reported rabid animals were wildlife. Relative contributions by the major animal groups were as follows: 1,953 raccoons (31.7%), 1,680 bats (27.3%), 1,539 skunks (25.0%), 340 foxes (5.5%), 257 cats (4.2%), 115 cattle (1.9%), and 84 dogs (1.4%). Compared with 2011, there was a substantial increase in the number of rabid cattle reported. One case of rabies involving a human was reported from California after the patient died abroad. The infection was determined to be a result of a rabies virus variant associated with Tadarida brasiliensis, with exposure occurring in California.

The present report provides an update on rabies epidemiology and events in the United States during 2012. Summary updates are also provided for Canada and Mexico.

Rabies is caused by neurotrophic viruses in the genus Lyssavirus. Without proper, timely medical care (eg, postexposure prophylaxis), the disease is almost always fatal. Rabies is primarily transmitted through the bite of an infected mammal, but may also be transmitted when fresh saliva from an infected animal comes into contact with a wound or mucous membranes. Postexposure prophylaxis consists of washing all bite wounds with soap and water, infiltrating the wound with rabies immunoglobulin (for persons with no history of rabies vaccination), and administering a series of 4 doses of rabies vaccine over 14 days.1,2

Since 1980, wildlife has accounted for > 90% of all rabid animals reported in the United States. The primary reservoir species are raccoons, bats, skunks, foxes, and mongooses (in Puerto Rico). Rabies virus variants associated with specific animal reservoirs primarily circulate within that species, although cross-species transmission to other mammalian species may occur. Rabies virus variants associated with mesocarnivore species (ie, raccoons, skunks, foxes, and mongooses) are associated with distinct geographic regions (Figure 1), whereas rabies virus variants associated with bat species are broadly distributed across geographic ranges associated with specific bat species. The recognized spatial boundaries of these rabies virus variants change over time as a result of many natural (eg, droughts) and anthropogenic (eg, housing development) factors affecting the corresponding reservoir species.3

Figure 1—
Figure 1—

Distribution of major rabies virus variants among mesocarnivore reservoirs in the United States and Puerto Rico, 2008 to 2012. *Potential host shift event.

Citation: Journal of the American Veterinary Medical Association 243, 6; 10.2460/javma.243.6.805

Rabies control in wildlife is a large-scale annual effort led by USDA APHIS Wildlife Services. Efforts are primarily focused on delivery of oral rabies vaccine–laden baits targeted at raccoons along the east coast of the United States. Oral vaccination of wildlife (primarily foxes and raccoons) has greatly reduced the spread of rabies in numerous countries in North America and Europe.4–6 Rabies vaccination of bats is currently not feasible and preventing human infection with bat rabies virus variants will continue to rely on secondary intervention methods such as health education, exposure prevention, and postexposure prophylaxis.

The reduction over time in the number of rabies cases involving humans in the United States has been a direct result of elimination of canine rabies virus variants, vaccination of wildlife, administration of postexposure prophylaxis in a timely manner, and education of health-care professionals and the public. Although the number of human rabies cases has been dramatically reduced, cases continue to occur, primarily as a result of exposure to bats.7 Appropriate risk assessment, including observation and testing of animals for rabies, continues to play an important role in preventing unnecessary postexposure prophylaxis after possible exposure to rabies. A 10-day observation period is routinely recommended in instances of possible exposure involving cats, dogs, or ferrets. Use of an observation period often prevents unnecessary euthanasia of owned animals, specifically those that have a known history of rabies vaccination.8 Unfortunately, data on the viral shedding period in other species are unavailable, making immediate euthanasia and rabies testing the most prudent method for determining the necessity of postexposure prophylaxis among persons who may have been exposed to other domestic or wildlife species with rabies.8,9 Additional precautions and more extensive risk assessment may be necessary following potential contact with bats. The Advisory Committee on Immunization Practices recommends evaluation of all persons bitten by or in direct contact with bats, but also recommends evaluation of persons who may have had unacknowledged contact with a bat, such as a deeply sleeping person, unattended child, mentally disabled person, or intoxicated person in a room in which a bat is found.1 In instances when a bat is found in a room with an individual who, if asleep, would normally have had the capacity and inclination to wake up following a bite, careful assessment is needed, but the circumstance may not require postexposure prophylaxis. However, efforts to capture the bat for rabies testing to exclude infection remain the most definitive way to rule out the risk of rabies transmission in these instances.

Reporting and Analysis

Human and animal rabies have been nationally notifiable conditions in the United States since 1944.10 In animals, rabies is diagnosed by means of the direct fluorescent antibody test. Currently more than 120 state health, agriculture, and university laboratories perform rabies diagnostic testing on a routine basis in the United States.11 In addition, targeted enhanced surveillance is conducted with the direct rapid immunohistochemistry test by USDA Wildlife Services as a component of oral rabies vaccination programs.5,12

During 2012, 13 states (Arkansas, Idaho, Maryland, Massachusetts, Michigan, New Jersey, North Dakota, Ohio, Pennsylvania, South Dakota, Vermont, Virginia, and West Virginia) transmitted electronic laboratory data for rabies diagnostic activity primarily through the Public Health Laboratory Information System. Other reporting entities and USDA Wildlife Services submitted animal rabies data on a monthly or annual basis directly to the CDC Poxvirus and Rabies Branch. A total of 105,328 samples were submitted for laboratory testing, of which 102,963 were considered suitable for testing. This represents a 3.1% increase in the number of animals tested for rabies, compared with the number tested during 2011 (99,890). A total of 6,601 animals were submitted by USDA Wildlife Services personnel for testing with the direct rapid immunohistochemistry test as part of active surveillance efforts, accounting for 6.3% of all animals tested in 2012.

The CDC rabies program requests detailed information on animals submitted for rabies testing, as described.13 All states, with the exception of Oklahoma, provided data on species, county, and date of testing or specimen collection for all animals submitted for rabies testing. The vaccination status of domestic animals and results of typing of rabies virus variants isolated were also requested.

For the present report, calculations of percentages of rabid animals were based on total numbers of animals tested. Proportions presented in this report are not representative of the incidence of rabies in these populations because most animals submitted for testing were selected on the basis of abnormal behavior or visible signs of illness or were involved in a potential exposure incident, biasing the selection of samples submitted for diagnostic testing. In addition, comparisons between states should take into consideration the underlying differences in submission protocols between jurisdictions. Submission rates were calculated on the basis of 2010 population data available from the US Census Bureau.14

Geographic ranges of terrestrial rabies virus reservoirs in the United States were produced by aggregating data pertaining to rabid animals collected from 2008 through 2012. All maps were produced as described.13 Areas designated with potential host shift events signify regions where new rabies virus variants may be emerging, as described.15

Summary data for rabies in Canada during 2012 were provided by the Center of Expertise for Rabies, Ottawa Laboratory, Fallowfield, and the Animal Health, Welfare, and Biosecurity Division, Canadian Food Inspection Agency. Summary data for rabies in Mexico during 2012 were provided by the Instituto de Salud del Estado de México.

Rabies in Wild Animals

Wild animals accounted for 91.6% (5,643) of the rabid animals reported in 2012, representing a 2.0% increase in the number of rabid wild animals reported, compared with 2011 (Figure 2). This was the first increase in the number of rabid animals reported annually since 2006.16 As has been the trend, raccoons constituted the most frequently reported rabid wildlife species (31.7%) during 2012, followed by bats (27.3%), skunks (25.0%), foxes (5.5%), other wild animals (1.4%), and rodents and lagomorphs (0.8%).

Figure 2—
Figure 2—

Cases of rabies among wildlife in the United States, by year and species, 1983 to 2012.

Citation: Journal of the American Veterinary Medical Association 243, 6; 10.2460/javma.243.6.805

Seasonal trends for wildlife species remained consistent with trends for previous years. The numbers of rabid raccoons and skunks that were reported peaked in March with a moderate second peak around August. There was a moderate peak in the number of rabid foxes around May to July, and the number of rabid bats peaked sharply in August.

Raccoons—The 1,953 rabid raccoons reported in 2012 represented a 1.4% decrease, compared with the number reported in 2011 (Table 1). Percentage of raccoons submitted for testing that were found to be rabid decreased to 13.3% from 14.5% in 2011. This was not a significant change from the 5-year average of 14.8% (95% CI, 12.9% to 16.7%). Fewer rabid raccoons were reported by 8 of the 20 eastern states, the District of Columbia, and New York City, where raccoon rabies is considered enzootic, with decreases of ≥ 10% reported from 5 localities (Ohio, 60.0% decrease; West Virginia, 49.3%; Florida, 19.5%; Massachusetts, 18.6%; and Connecticut, 12.5%). States in the northeast and mid-Atlantic region where raccoon rabies is enzootic accounted for 56.2% (1,145 cases; 17.8% decrease) of all rabid raccoons reported in 2012 (Figure 3). Southeastern states where raccoon rabies is enzootic reported 27.2% (555 cases; 1.0% increase) of all rabid raccoons. The remaining rabid raccoons were reported by states where the raccoon rabies virus variant is not enzootic, including Texas (n = 19), Colorado (2), Kansas (2), New Mexico (2), Ohio (2), California (1), and Nebraska (1). Rabies virus variant information was only available for rabid raccoons collected in areas of New Mexico and Texas where the raccoon rabies virus variant is not enzootic; these raccoons were infected with the south central skunk rabies virus variant. Overall, states in which the raccoon rabies virus variant is enzootic, excluding Tennessee and Ohio, submitted 41.0 animals/100,000 persons for rabies testing during 2012, a 7.6% increase from the 38.1 animals/100,000 persons submitted for rabies testing during 2011. Animals from states in which the raccoon rabies virus variant is enzootic, excluding Tennessee and Ohio, accounted for 64.5% of all rabid animals reported in the United States during 2012 and 88.6% of all rabid animals other than bats.

Figure 3—
Figure 3—

Reported cases of rabies involving raccoons, by county, 2012. Histogram represents number of counties in each category for total number of raccoons submitted for testing.

Citation: Journal of the American Veterinary Medical Association 243, 6; 10.2460/javma.243.6.805

Table 1—

Cases of rabies in the United States, by location, during 2012.

    Domestic animalsWild animals
LocationTotal casesDomesticWildCatsCattleDogsHorses and mulesSheep and goatsOther domestic*RaccoonsBatsSkunks
AK624002000000
AL5494541400033100
AR1318123133100022101
AZ5705700000004013
CA2522249101000122616
CO1834179110002a28588
CT1735168320000912248
DC6006000000039200
DE15411300010710
FL109129780220066142
GA373383352447201b1802787
HI000000000000
IA315261400000179
ID230230000000230
IL630630000000630
IN200200000000200
KS5613434405002634
KY14212002000093
LA404000000022
MA1132111200000483814
MD3251531013100102035426
ME8858340100042530
MI610610000000528
MN72106243120003921
MO2802800000001612
MS202000000020
MT253220111000157
NC4344439025792102082883
ND75235261204100250
NE5995053100011335
NH291281000001347
NJ3092128820100001466856
NM482460020002633
NV200200000000200
NY42529396225011018611553
NYC13013000000930
OH410410000002390
OK81275411174400349
OR170170000000140
PA4335038341603002376347
PR7332416218600000
RI28226200000988
SC1376131420000662521
SD60213921603000336
TN4854310220021031
TX683446391491641019331273
UT150150000000150
VA597525452815342027220185
VT6756231001030626
WA909000000090
WI300300000000291
WV6856320210037414
WY2622411000001410
Total6,1635195,64325711584471331,9531,6801,539
% 2012100.008.4291.564.171.871.360.760.210.0531.6927.2624.97
% Pos 20126.181.0411.221.078.670.375.042.721.3213.286.3830.98
Total 20116,0374965,5353036570441221,9811,3801,627
% Change2.094.641.95–15.1876.9220.006.828.3350.00–1.4121.74–5.41

Other domestic includes

2 bison

1 llama.

Other wild includes

1 cougar, 1 ringtail

3 bobcats, 1 not provided

3 bobcats, 1 coyote

1 coyote

1 coyote

1 deer, 1 opossum

1 deer

2 bobcats, 1 deer

1 coyote

1 coyote

5 deer, 1 mink, 1 otter

1 opossum

1 bobcat

1 bobcat, 3 deer, 1 opossum

41 mongooses

1 bobcat

2 coyote, 1 deer

1 bear, 3 bobcats

2 bobcats.

Rodents and lagomorphs include

2 groundhogs

2 groundhogs

5 groundhogs

1 groundhog

1 groundhog

9 groundhogs

7 groundhogs

5 groundhogs

4 beavers, 8 groundhogs

2 groundhogs.

— = Not applicable. NYC = New York City. Pos = Positive.

Bats—There were 1,680 rabid bats reported during 2012, representing a 21.7% increase from the number of rabid bats (n = 1,380) reported in 2011. In addition, the percentage of bats submitted for testing that were rabid (6.4%) was significantly higher than the average for the preceding 5 years (6.0%; 95% CI, 5.8% to 6.3%). All 48 contiguous states reported rabid bats (Figure 4). No rabid bats were reported in Alaska, Hawaii, or Puerto Rico. Seven states (Idaho, Illinois, Indiana, Mississippi, Nevada, Utah, and Washington) reported that rabid bats were the only rabid animal found in 2012. A ≥ 50% increase in the number of rabid bats was reported by 19 states (South Carolina, 525% increase; Alabama, 400%; Arkansas, 266%; Vermont, 200%; Idaho, 187%; Georgia, 170%; Wyoming, 133.3%; Utah, 114.3%; Kansas, 100%; North Dakota, 100%; New Mexico, 100%; Massachusetts, 90%; New Jersey, 89.0%; New York, 87.3%; Pennsylvania, 80%; North Carolina, 75%; Montana, 66.7%; Wisconsin, 61.1.%; Kentucky, 50%). Among the bats tested for rabies, 14,121 (51.2%) were identified beyond the taxonomic level of order (Table 2). Overall, states where bats are the only recognized reservoir for rabies submitted 19.5 animals/100,000 persons for rabies testing during 2012, up from 10.6 animals/100,000 persons submitted during 2011.

Figure 4—
Figure 4—

Reported cases of rabies involving bats, by county, 2012. Histogram represents number of counties in each category for total number of bats submitted for testing.

Citation: Journal of the American Veterinary Medical Association 243, 6; 10.2460/javma.243.6.805

Table 2—

Species of bats submitted for rabies testing in the United States during 2012.

Species (common name)No. testedNo. positivePercentage positive
Unspeciated13,4511,0317.7%
Eptesicus fuscus (big brown bat)11,9994854.0%
Myotis lucifigus (little brown bat)848182.1%
Lasiurus borealis (red bat)3554312.1%
Nycticeius humeralis (evening bat)18421.1%
Tadarida brasiliensis (Mexican free-tailed bat)1773720.9%
Lasionycteris noctivagans (silver-haired bat)16085.0%
Myotis species (not further speciated)6945.8%
Lasiurus cinereus (hoary bat)602948.3%
Myotis californicus (California myotis)5511.8%
Myotis evotis (long-eared myotis)5048.0%
Myotis ciliolabrum (western small-footed bat)25416.0%
Lasiurus seminolus (Seminole bat)19315.8%
Myotis keenii (Keen's myotis)1700.0%
Myotis yumanensis (Yuma myotis)1700.0%
Parastrellus hesperus (canyon bat)14642.9%
Myotis volans (long-legged myotis)1000.0%
Perimyotis subflavus (tri-colored bat)10110.0%
Lasiurus ega (southern yellow bat)9222.2%
Myotis austroriparius (southeastern myotis)900.0%
Myotis septentrionalis (northern long-eared myotis)800.0%
Family Molossidae (not further speciated)6350.0%
Myotis auriculus (southwestern myotis)600.0%
Rousettus aegyptiacus (Egyptian rousette*)400.0%
Myotis sodalis (Indiana bat)300.0%
Plecotus townsendii (Townsend's big-eared bat)200.0%
Antrozous pallidus (desert pallid bat)100.0%
Euderma maculatum (spotted bat)11100.0%
Myotis grisescens (gray myotis)100.0%
Myotis leibii (small-footed myotis)11100.0%
Myotis thysanodes (fringed myotis)100.0%
Total27,5721,6836.1%

Exotic species submitted by zoos.

Skunks—There was a 5.4% decrease in the number of rabid skunks reported (1,539) during 2012, compared with the number reported during 2011. The percentage of skunks submitted for rabies testing that were found to be rabid increased significantly (31.0%) from the previous 5-year average (26.8%; 95% CI, 25.0% to 28.5%). Seven of the 22 states where skunk rabies virus variants are enzootic reported a ≥ 50% increase during 2012 (Colorado, 282.6% increase; North Dakota, 177.8%; New Mexico, 135.7%; Nebraska, 105.6%; Arkansas, 90.6%; South Dakota, 80.0%; and Michigan, 60%). Illinois and Indiana did not report any rabid skunks and have not done so since 2005 and 2007, respectively. States in which the south central skunk rabies virus variant is enzootic reported 35.0% of all rabid skunks (a 12.2% decrease), and states in which the north central skunk rabies virus variant is enzootic reported 10.0% of all rabid skunks (a 1.2% decrease); 1.0% of all rabid skunks were reported with the California skunk rabies virus variant (a 0.3% increase; Figure 5). A total of 51.5% of all rabid skunks were from states where the raccoon rabies virus variant is enzootic (7.0% increase). Overall, for states where skunks are the primary reservoir for rabies, 29.4 animals/100,000 persons were submitted for rabies testing during 2012, down from 30.7 animals/100,000 persons submitted in 2011. For states in which the primary terrestrial variant was south central, north central, and California skunk rabies virus variants, 26.8 animals/100,000 persons, 39.4 animals/100,000 persons, and 15.9 animals/100,000 persons were submitted for testing, respectively.

Figure 5—
Figure 5—

Reported cases of rabies involving skunks, by county, 2012. Histogram represents number of counties in each category for total number of skunks submitted for testing.

Citation: Journal of the American Veterinary Medical Association 243, 6; 10.2460/javma.243.6.805

Foxes—There were 340 rabid foxes reported during 2012, which represented a 20.4% decrease, compared with the number reported in 2011. The percentage of foxes submitted for testing that were rabid (18.3%) was significantly lower than the average for the preceding 5 years (24.7%; 95% CI, 21.7% to 27.7%). Most rabid foxes (300 [88.2%]) were reported from states where raccoon rabies is enzootic (Figure 6). For the 80 rabid foxes for which the rabies virus variant was typed, most infections were attributed to raccoon rabies virus variants (55 [68.7%]). Additional infections among rabid foxes were associated with the south central skunk rabies virus variant (17 [21.3%]), the north central skunk rabies virus variant (1 [1.3%]), and an insectivorous bat rabies virus variant (1 [1.3%]). Four (5.0%) rabid foxes were reportedly infected with the arctic fox rabies virus variant, and 2 (2.5%) were infected with the Arizona gray fox rabies virus variant. A cluster of 3 rabid foxes was reported from southern Oregon during 2012 within a geographic range designated as a potential host shift area since 2010. Rabies virus variant typing was available for 2 of these foxes, 1 from Jackson county and 1 from Josephine county. These foxes were infected with the distinctly different rabies virus variant associated with Myotis spp. No animals infected with the Texas gray fox rabies virus variant were reported during 2012.

Figure 6—
Figure 6—

Reported cases of rabies involving foxes, by county, 2012. Histogram represents number of counties in each category for total number of foxes submitted for testing.

Citation: Journal of the American Veterinary Medical Association 243, 6; 10.2460/javma.243.6.805

Other wild animals—Puerto Rico reported 41 rabid mongooses during 2012, a 17.1% increase from the 35 cases reported in 2011. Other reported rabid wildlife included 16 bobcats (Lynx rufus), 12 deer (presumably Odocoileus virginianus), 7 coyotes (Canis latrans), 3 opossums (Didelphis virginiana), 1 bear (Ursus spp), 1 cougar (Puma concolor), 1 mink (Neovison vison), 1 otter (presumably Lontra canadensis), and 1 ringtail (Bassariscus astutus). Rabid rodents reported in 2012 included 42 groundhogs (Marmota monax) and 4 beavers (Castor canadensis), all of which were reported from states where raccoon rabies is enzootic. No rabid lagomorphs were reported during 2012. Rabies virus variants were reported for 4 of the 7 rabid coyotes reported in 2012. This included 2 rabid coyotes infected with the south central skunk rabies virus variant (Texas), 1 coyote infected with the Arizona gray fox rabies virus variant (New Mexico), and 1 coyote infected with the raccoon rabies virus variant (New Hampshire). Variant information was not reported for rabid coyotes in Georgia (1), Kansas (1), and Massachusetts (1).

Rabies in Domestic Animals

During 2012, domestic animals accounted for 8.4% (519) of all rabid animals reported, an increase of 4.6%, compared with the number reported in 2011. With the exception of cats, the number of cases of rabid animals reported during 2012 was increased for all species of domestic animals, compared with the number reported during 2011. Five states and Puerto Rico reported more than half of the rabid domestic animals in 2012: Virginia (n = 52), Pennsylvania (50), North Carolina (44), Texas (44), Georgia (38), and Puerto Rico (32).

Dogs—Eighty-four rabid dogs were reported during 2012, representing a 20.0% increase from the number reported during 2011 (Figure 7). Most rabid dogs were reported from Puerto Rico (n = 18 [21.4%]), Texas (16 [19.1%]), North Carolina (9 [10.7%]), Georgia (7 [8.3%]), and Oklahoma (7 [8.3%]). Overall, the percentage of dogs submitted for rabies testing that were rabid (0.4%) was significantly higher, compared with the preceding 5-year average (0.3%; 95% CI, 0.28% to 0.32%). Vaccination status was reported for 58.3% (n = 49) of all rabid dogs. No known vaccination history was reported for 36.9% (n = 31) of all rabid dogs, and 16.7% (14) reportedly had an unknown vaccination history; in 4.8% (4), vaccinations were reportedly not up to date. Vaccination status was not provided for 41.7% (35) of the rabid dogs. Most of the rabid dogs in which a rabies virus variant was reported were infected with the south central skunk rabies virus variant (26 [72.2%]), followed by the raccoon rabies virus variant (5 [13.8%]), north central skunk rabies virus variant (4 [11.1%]), and arctic fox rabies virus variant (1 [2.7%]). Variant information was not reported for rabid dogs in Puerto Rico (18), North Carolina (9), Georgia (7), Florida (2), Arkansas (2), Kentucky (2), West Virginia (2), Alaska (1), Alabama (1), California (1), Montana (1), Nebraska (1), and Virginia (1).

Figure 7—
Figure 7—

Reported cases of rabies involving cats and dogs, by county, 2012. Histogram represents number of counties in each category for total number of cats and dogs submitted for testing.

Citation: Journal of the American Veterinary Medical Association 243, 6; 10.2460/javma.243.6.805

Cats—Cats accounted for most of the rabid domestic animals (257 [49.9%]) reported during 2012, despite a 15.2% decrease in the number of rabid cats, compared with the number reported during 2011. The percentage of cats submitted for testing that were rabid (1.1%) was not significantly different, compared with the preceding 5-year average (1.0%; 95% CI, 0.9% to 1.2%). Rabies vaccination status was reported for 18.6% of the rabid cats. Most of the rabid cats were reported from states in which the raccoon rabies virus variant is enzootic (Pennsylvania, 15.6%; Virginia, 11.0%; North Carolina, 9.5%; New Jersey, 9.5%; Georgia, 9.1%). Twenty states, the District of Columbia, and New York City reported no rabid cats. Rabies virus variant typing was performed for 92 (35.0%) rabid cats reported during 2012. Most of these cats were infected with the raccoon rabies virus variant (72 [78.3%]), with the remainder infected with the south central skunk variant (15 [16.3%]) and the north central skunk variant (5 [5.4%]).

Other domestic animals—A total of 115 rabid cattle were reported during 2012, representing a 76.9% increase from the number reported during 2011. The percentage of cattle submitted for rabies testing that were found to be rabid (8.7%) was significantly increased, compared with the preceding 5-year average (5.6%; 95% CI, 5.1% to 6.2%). Most of the rabid cattle were reported from South Dakota (16 [14.0%]), Virginia (15 [13.0%]), North Dakota (12 [10.4%]), Oklahoma (11 [9.6%]), Texas (9 [7.8%]), and North Carolina (7 [6.1%]). The number of rabid horses and mules increased 6.8% (n = 47) during 2012, compared with the number reported during 2011 (44). The percentage of horses and mules submitted for rabies testing that were found to be rabid (5.0%) was significantly increased, compared with the preceding 5-year average (4.2%; 95% CI, 3.4% to 4.9%). The 5 states and territories with the greatest number of rabid horses and mules were Puerto Rico (6 [12.8%]), Kansas (5 [10.6%]), North Dakota (4 [8.5%]), Oklahoma (4 [8.5%]), and Texas (4 [8.5%]). The number of rabid sheep and goats reported during 2012 (13) increased by 8.3%, compared with the number reported during 2011. Other rabid domestic animals reported included 2 bison from Colorado and a llama from Georgia.

Rabies in Humans

Samples from 33 humans from 23 states were submitted to the CDC for rabies testing during 2012, representing a 26.8% decrease from the number for 2011. One case of human rabies was confirmed in 2012 (Table 3). Thirty-one cases of human rabies have been reported in the United States since 2003. Most human patients with domestically acquired rabies were males (14 [70.0%]), and the median age of infected human patients was 38.8 years.

Table 3—

Cases of rabies in humans in the United States and Puerto Rico, 2003 through June 2013, by circumstances of exposure and rabies virus variant

Date of onsetDate of deathReporting stateAge (y)SexExposure*Rabies virus variant
10 Feb 0310 Mar 03VA25MUnknownRaccoon, eastern United States
28 May 035 Jun 03PR64MBite-Puerto RicoDog/mongoose, Puerto Rico
23 Aug 0314 Sep 03CA66MBiteBat, Ln
9 Feb 0415 Feb 04FL41MBite-HaitiDog, Haiti
27 Apr 043 May 04AR20MBite (organ donor)Bat, Tb
25 May 0431 May 04OK53MLiver transplantBat, Tb
27 May 0421 Jun 04TX18MKidney transplantBat, Tb
29 May 049 Jun 04TX50FKidney transplantBat, Tb
2 Jun 0410 Jun 04TX55FArterial transplantBat, Tb
12 Oct 04SurvivedWI15FBiteBat, unknown
19 Oct 0426 Oct 04CA22MUnknown-El SalvadorDog, El Salvador
27 Sep 0527 Sep 05MS10MContactBat, unknown
4 May 0612 May 06TX16MContactBat, Tb
30 Sep 062 Nov 06IN10FBiteBat, Ln
15 Nov 0614 Dec 06CA11MBite-PhilippinesDog, Philippines
19 Sep 0720 Oct 07MN46MBiteBat, unknown
16 Mar 0818 Mar 08CA16MBite-MexicoFox, Tb related
19 Mar 0830 Nov 08MO55MBiteBat, Ln
25 Feb 09SurvivedTX17FContactBat, unknown
5 Oct 0920 Oct 09IN43MUnknownBat, Ps
20 Oct 0911 Nov 09MI55MContactBat, Ln
23 Oct 0920 Nov 09VA42MContact-IndiaDog, India
2 Aug 1021 Aug 10LA19MBite-MexicoBat, Dr
24 Dec 1010 Jan 11WI70MUnknownBat, Ps
30 Apr 11SurvivedCA8FUnknownUnknown
30 Jun 1120 Jul 11NJ73FBite-HaitiDog, Haiti
14 Aug 1121 Aug 11NY25MContact-AfghanistanDog, Afghanistan
Sep 11Oct 11MA40MContact-BrazilDog, Brazil
3 Dec 1119 Dec 11SC46FUnknownTb
Dec 11Jan 12MA63MContactMy sp
6 Jul 1231 Jul 12CA34MBiteBat, Tb
31 Jan 1327 Feb 13MD49MKidney transplantRaccoon, eastern United States
21 Aug 111 Sep 11NC20MContactRaccoon, eastern United States
16 May 1311 Jun 13TX28MUnknown-GuatemalaDog, Guatemala

Data for exposure history are reported when plausible information was reported directly by the patient (if lucid or credible) or when a reliable account of an incident consistent with rabies virus exposure (eg, dog bite) was reported by an independent witness (usually a family member). Exposure histories are categorized as bite, contact (eg, waking to find bat on exposed skin) but no known bite was acknowledged, or unknown (ie, no known contact with an animal was elicited during case investigation).

Variants of the rabies virus associated with terrestrial animals in the United States and Puerto Rico are identified with the names of the reservoir animal (eg, dog or raccoon), followed by the name of the most definitive geographic entity (usually the country) from which the variant has been identified. Variants of the rabies virus associated with bats are identified with the names of the species of bats in which they have been found to be circulating. Because information regarding the location of the exposure and the identity of the exposing animal is almost always retrospective and much information is frequently unavailable, the location of the exposure and the identity of the animal responsible for the infection are often limited to deduction.

Dr = Desmodus rotundus. Ln = Lasionycteris noctivagans. My sp = Myotis sp. Ps = Perimyotis subflavus. Tb = Tadarida brasiliensis.

In July 2012, a 34-year-old male US citizen presented to a hospital in Iraq with right arm spasticity, anxiety, and malaise. After hospitalization, the patient's status quickly deteriorated into a coma. At the family's request, the patient was transferred to Zurich, Switzerland, on July 29; the patient died on July 31. A diagnosis of rabies was confirmed by means of fluorescent antibody testing of brain tissue at the Swiss Rabies Center on August 22, and samples of brain tissue submitted to the CDC confirmed a rabies virus variant associated with the insectivorous Mexican free-tailed bat (Tadarida brasiliensis).17 During the patient's infectious period, case investigations revealed that the patient had traveled on 8 international flights and visited 4 medical facilities. A total of 59 contacts with the patient were identified, and 23 of these individuals received rabies postexposure prophylaxis.17 During the investigation, an acquaintance of the patient reported that the patient had been seen touching a bat and had pulled his hand back as if bitten. This case represents the first report of rabies acquired in the United States with symptoms development, medical management, and diagnosis abroad.

Rabies in Canada and Mexico

Canada reported 142 laboratory-confirmed cases of rabies during 2012, a 23.4% increase from the number reported during 2011. Most of the rabid animals were wildlife (119 [83.8%]). The remaining rabid animals consisted of cats and dogs (18 [12.7%]) and livestock (4 [2.8%]). There was also 1 case (0.7%) of rabies in a human. The number of animals submitted to the Canadian Food Inspection Agency for diagnostic testing decreased 16.1%, from 4,589 in 2011 to 3,851 in 2012. In addition to animals submitted to the Canadian Food Inspection Agency for testing, several provincial ministries undertook active wildlife rabies surveillance testing during 2012; no rabid animals were identified. No rabid raccoons have been reported in Canada since 2008. One rabid wolf was reported in Canada in 2012. Numbers of rabid skunks, bats, and cats decreased by 23.9%, 4.3%, and 50.0%, respectively. During 2012, there was a northern epizootic in both arctic and red foxes, which accounted for a 156.0% increase (41 cases reported in 2012, compared with 16 cases reported in 2011) in the number of rabid foxes and an increase of 800% (16 cases reported in 2012, compared with 2 cases reported in 2011) in the number of rabid dogs. In the human rabies case, the patient, a Haitian national, presented in Toronto with symptoms upon returning from the Dominican Republic. Sequence analysis showed similarities to previously isolated Haitian canine rabies virus variants.a

Mexico reported 12 laboratory-confirmed cases of canine rabies involving the canine rabies virus variant during 2012, a 47% decrease from the number reported during 2011. Nine cases occurred in southeast Mexico (6 in Chiapas and 3 in the Yucatan). Probable causes include a high number of stray dogs and low canine vaccine coverage rates. Three cases occurred in the center of Mexico (2 in Mexico State and 1 in Querataro). The cases in Mexico State occurred in areas with new settlements and inadequate health care. The case in Querataro was an imported case originating in a market. Molecular results showed high similarities to isolates from the same region (Chiapas isolates showed 98% similarity to an isolate obtained from a Yucatan dog in 2002; Yucatan isolates showed 98% similarity to an isolate obtained from a Yucatan dog in 1998; Mexico State and Queretaro isolates showed 100% similarity to isolates from Mexico State in 2005).

Discussion

Since 2006, the CDC has annually requested information on all animals submitted for rabies testing. The number of animals submitted for rabies testing increased by 2.27% in 2012, compared with the number submitted in 2011. Despite this increase, the number of animals submitted for testing in 2012 was decreased, compared with the preceding 5-year average (111,477; 95% CI, 102,849 to 120,105). Laboratory testing of animals suspected to be rabid remains a critical public health function. Ruling out rabies reduces the number of individuals receiving postexposure prophylaxis unnecessarily, which in turn reduces the number of adverse events and the health-care costs related to rabies exposures.18

Rabies remains a global international burden. Although the true burden of rabies remains unknown, current estimates are that more than 55,000 persons die of rabies each year, mostly in Asia and Africa.19,20 The elimination of rabies will require a large-scale, global effort. As can be seen with the human cases in the United States and Canada, advances in international travel now necessitate collaboration among multiple countries and investigators to determine the source of exposure and other individuals who may be at risk.21

Although the canine rabies virus variant has been eliminated from the United States, management of human exposures to wildlife remains critical. Most human rabies cases that occur in the United States are due to bat exposures that were either unrecognized or were not considered serious enough to seek medical attention. In states where only bat rabies virus variants are found, submission rates for rabies testing are significantly lower than in states in which raccoon and skunk rabies virus variants are enzootic. This may relate to differences in the perception of rabies risk in areas where only bats are reportedly rabid, as rates of postexposure prophylaxis are also lower in these areas of the United States.18,22 However, any mammal is capable of acquiring and transmitting rabies infection. Therefore, it is important for public health advocates to continue educational outreach efforts regarding the risk of rabies from contact with wildlife, regardless of the reservoir species. Appropriate risk assessment and judicious application of postexposure prophylaxis remain an important focus of rabies education for health-care providers in the United States. During the fall of 2012, the CDC was notified by Sanofi Pasteur that the company would be restricting supplies of Imovax rabies vaccine to orders for postexposure prophylaxis only. During this time, only the Novartis RabAvert vaccine was available for preexposure vaccination through wholesalers in the United States. Both manufacturers remained in contact with the CDC and the FDA regarding supply levels during this time. Stakeholders, including state health department representatives, monitored reports of difficulties in obtaining supplies and projected usage rates to ensure preventative actions could be taken before a true shortage could occur. Despite difficulties in ordering the vaccine and some regional wholesaler-specific shortages, supplies continued to meet demand throughout 2012, and no specific changes in recommendations or further ordering restrictions were implemented. This situation and more severe situations in the past 5 years continue to illustrate the need to closely monitor rabies vaccine supplies. Improved risk assessments, including animal observation and testing where possible, along with better national surveillance of human rabies postexposure prophylaxis are needed to improve the use of rabies biologics and to better understand the epidemiology of rabies.

2013 Rabies Update

Three human rabies cases were reported in the United States during the first half of 2013. In February 2013, a man presented to a Maryland emergency department with right hip pain. He developed encephalitis and hypersalivation and died after 22 days of hospitalization. Samples obtained 5 days prior to the patient's death were submitted to the CDC, and rabies was confirmed. The infecting virus was typed as a rabies virus variant associated with raccoons. No known exposures to animals were elicited during the patient investigation. However, the patient had received a kidney transplant from a deceased donor approximately 17 months before the onset of rabies. The deceased donor had presented to an emergency department in Florida in August 2011 with nausea, vomiting, and upper extremity paresthesia. He was admitted after developing seizures and an altered mental status requiring sedation and intubation and was declared brain-dead 17 days after illness onset. Given that the patient had a history of consuming raw fish, the presumed diagnosis at the time of death was severe acute gastroenteritis. Organs were harvested and transplanted into 4 recipients. Testing of banked samples from the donor confirmed a diagnosis of rabies, with rabies virus–specific antibodies identified in serum and rabies virus RNA identified in postmortem CNS tissue. Sequence analysis found > 99.9% identity between the rabies virus isolate from the donor and the isolate from the Maryland recipient. On further investigation, the donor was identified as an active hunter and raccoon trapper. The 3 remaining organ recipients were identified and provided postexposure prophylaxis and have remained healthy.23

In June 2013, the Texas State Health Department notified the CDC of a suspected case of rabies involving a 28-year-old Guatemalan resident who had been detained by US authorities. The diagnosis was confirmed by the CDC, and the infecting virus was typed as a canine variant found in Central America. The patient was apprehended while crossing the US border and developed anxiety and difficulty swallowing while in a detainment center. The patient was transferred to a hospital, where he developed pneumomediastinum, fever, abdominal pain, and, eventually, encephalitis and respiratory failure. Contact investigations identified more than 500 detainees who were potentially housed with the patient during his infectious period, of which 68 were considered to have a moderate or high risk of close contact. The CDC coordinated with Immigration and Customs Enforcement to perform follow-up risk assessments for contacts still detained in the United States and contacted the Pan American Health Organization to notify countries to which other contacts had been returned.

Rabies vaccine supply concerns, which began in September 2012, continued through spring and early summer 2013. However, by June, both manufacturers were supplying rabies vaccine without restrictions. In an effort to increase awareness of rabies vaccine supply concerns, the CDC has established a website with updates on rabies vaccine and immune globulin supply concerns (www.cdc.gov/rabies/resources/availability.html). In addition, a subscription service is available that allows the public to subscribe to email alerts when updates have been posted to the rabies website. Currently, more than 80,000 persons have subscribed to receive these updates, allowing for rapid distribution of vaccine supply and other rabies alerts.

Despite > 2 years without any reports of rabid animals infected with the Texas gray fox variant, a rabid cow with this variant was reported from central Texas in 2013. Enhanced surveillance and oral rabies vaccination have been instituted around the region where this case was identified. Adequate and reasonable surveillance levels to identify the elimination of rabies virus variants from wildlife populations have not been established. Additional efforts are needed to establish standards that will be flexible and based on reservoir species and environmental considerations as efforts continue toward elimination of wildlife rabies virus variants.

ABBREVIATIONS

CI

Confidence interval

a.

Fehlner-Gardiner C, Center of Expertise for Rabies, Ottawa, ON, Canada: Personal communication, 2013.

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Contributor Notes

Use of trade names and commercial sources is for identification only and does not imply endorsement by the US Department of Health and Human Services. The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the CDC.

The authors thank the state and territorial health and agriculture departments and laboratories for their contributions of rabies surveillance data and human case investigations, especially Laura Robinson of the Texas Department of Health and Darlene Bhavnani of the CDC Division of Global Migration and Quarantine. The authors also thank N. Kuzmina and A. Velasco-Villa for assistance with diagnostic testing and viral typing; Kim Knight-Picketts and Christine Fehlner-Gardiner from the Center of Expertise for Rabies, Ottawa Laboratory, Fallowfield, and from the Animal Health, Welfare and Biosecurity Division, Canadian Food Inspection Agency, for providing 2012 summary data for Canada; and Fernando Vargas Pino from the Instituto de Salud del Estado de México for providing 2012 canine rabies summary data for Mexico.

This article has not undergone peer review.

Address correspondence to Mr. Blanton (asi5@cdc.gov).