Public Veterinary Medicine: Public Health Rabies surveillance in the United States during 2012 Jessie L. Dyer, MSPH; Ryan Wallace, MPH, DVM; Lillian Orciari, MS; Dillon Hightower, BS; Pamela Yager, BS; Jesse D. Blanton, MPH 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.

T

he 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 prima-

ABBREVIATION CI

Confidence interval

ry 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 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 vari-

From the 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. 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 ([email protected]). JAVMA, Vol 243, No. 6, September 15, 2013

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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 activFigure 1—Distribution of major rabies virus variants among mesocarnivore res- ity primarily through the Public Health ervoirs in the United States and Puerto Rico, 2008 to 2012. *Potential host shift Laboratory Information System. Other event. reporting entities and USDA Wildlife Services submitted animal rabies data on a monthly or ants, vaccination of wildlife, administration of postexannual basis directly to the CDC Poxvirus and Rabies posure prophylaxis in a timely manner, and education Branch. A total of 105,328 samples were submitted for of health-care professionals and the public. Although laboratory testing, of which 102,963 were considered the number of human rabies cases has been dramatisuitable for testing. This represents a 3.1% increase cally reduced, cases continue to occur, primarily as a rein the number of animals tested for rabies, compared sult of exposure to bats.7 Appropriate risk assessment, with the number tested during 2011 (99,890). A toincluding observation and testing of animals for rabies, tal of 6,601 animals were submitted by USDA Wildcontinues to play an important role in preventing unlife Services personnel for testing with the direct rapid necessary postexposure prophylaxis after possible eximmunohistochemistry test as part of active surveilposure to rabies. A 10-day observation period is roulance efforts, accounting for 6.3% of all animals tested tinely recommended in instances of possible exposure in 2012. involving cats, dogs, or ferrets. Use of an observation The CDC rabies program requests detailed inforperiod often prevents unnecessary euthanasia of owned mation on animals submitted for rabies testing, as deanimals, specifically those that have a known history scribed.13 All states, with the exception of Oklahoma, of rabies vaccination.8 Unfortunately, data on the viral provided data on species, county, and date of testing or shedding period in other species are unavailable, makspecimen collection for all animals submitted for rabies ing immediate euthanasia and rabies testing the most testing. The vaccination status of domestic animals and results of typing of rabies virus variants isolated were prudent method for determining the necessity of postalso requested. exposure prophylaxis among persons who may have For the present report, calculations of percentages been exposed to other domestic or wildlife species with of rabid animals were based on total numbers of anirabies.8,9 Additional precautions and more extensive mals tested. Proportions presented in this report are risk assessment may be necessary following potential not representative of the incidence of rabies in these contact with bats. The Advisory Committee on Immupopulations because most animals submitted for testnization Practices recommends evaluation of all pering were selected on the basis of abnormal behavior or sons bitten by or in direct contact with bats, but also visible signs of illness or were involved in a potential recommends evaluation of persons who may have had exposure incident, biasing the selection of samples subunacknowledged contact with a bat, such as a deeply mitted for diagnostic testing. In addition, comparisons sleeping person, unattended child, mentally disabled between states should take into consideration the unperson, or intoxicated person in a room in which a bat derlying differences in submission protocols between is found.1 In instances when a bat is found in a room jurisdictions. Submission rates were calculated on the with an individual who, if asleep, would normally have basis of 2010 population data available from the US had the capacity and inclination to wake up following a Census Bureau.14 bite, careful assessment is needed, but the circumstance Geographic ranges of terrestrial rabies virus resermay not require postexposure prophylaxis. However, voirs in the United States were produced by aggregating efforts to capture the bat for rabies testing to exclude data pertaining to rabid animals collected from 2008 infection remain the most definitive way to rule out the through 2012. All maps were produced as described.13 risk of rabies transmission in these instances. Areas designated with potential host shift events signify 806

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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%). 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. 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 2—Cases of rabies among wildlife in the United States, by year and species, 1983 to 2012. JAVMA, Vol 243, No. 6, September 15, 2013

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 Vet Med Today: Public Veterinary Medicine

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Table 1—Cases of rabies in the United States, by location, during 2012. Domestic animals

Location

Total cases Domestic Wild

Cats Cattle Dogs

Wild animals

Horses Sheep and and Other mules goats domestic* Raccoons

Bats

Skunks

Foxes

Rodents Other and wild† lagomorphs‡ Humans

% Pos 2012

2011 cases

Change (%)

AK AL AR AZ CA

6 54 131 57 252

2 9 8 0 2

4 45 123 57 249

0 4 1 0 1

0 1 3 0 0

2 4 3 0 1

0 0 1 0 0

0 0 0 0 0

0 0 0 0 0

0 33 0 0 1

0 10 22 40 226

0 0 101 13 16

4 2 0 2 6

0 0 0 2c 0

0 0 0 0 0

0 0 0 0 1

5.3 2.3 11.5 9.5 4.2

14 10 60 74 224

–57.14 440.00 118.33 –22.97 12.50

CO CT DC DE FL

183 173 60 15 109

4 5 0 4 12

179 168 60 11 97

1 3 0 3 8

1 2 0 0 0

0 0 0 0 2

0 0 0 0 2

0 0 0 1 0

2a 0 0 0 0

2 91 39 7 66

85 22 20 1 14

88 48 0 0 2

4 5 1 3 11

0 0 0 0 4d

0 2v 0 0 0

0 0 0 0 0

12.0 8.9 18.4 7.5 4.8

104 196 28 6 122

75.96 –11.73 114.29 150.00 –10.66

GA HI IA ID IL

373 0 31 23 63

38 0 5 0 0

335 0 26 23 63

24 0 1 0 0

4 0 4 0 0

7 0 0 0 0

2 0 0 0 0

0 0 0 0 0

1b 0 0 0 0

180 0 0 0 0

27 0 17 23 63

87 0 9 0 0

37 0 0 0 0

4e 0 0 0 0

0 0 0 0 0

0 0 0 0 0

14.0 0.0 2.1 6.3 1.4

370 0 25 8 51

0.81 0.00 24.00 187.50 23.53

IN KS KY LA MA

20 56 14 4 113

0 13 2 0 2

20 43 12 4 111

0 4 0 0 2

0 4 0 0 0

0 0 2 0 0

0 5 0 0 0

0 0 0 0 0

0 0 0 0 0

0 2 0 0 48

20 6 9 2 38

0 34 3 2 14

0 0 0 0 8

0 1f 0 0 1g

0 0 0 0 2w

0 0 0 0 0

1.8 4.5 1.6 0.8 4.2

33 31 17 6 118

–39.39 80.65 –17.65 –33.33 –4.24

MD ME MI MN MO

325 88 61 72 28

15 5 0 10 0

310 83 61 62 28

13 4 0 4 0

1 0 0 3 0

0 1 0 1 0

0 0 0 2 0

1 0 0 0 0

0 0 0 0 0

203 42 0 0 0

54 5 52 39 16

26 30 8 21 12

20 5 1 1 0

2h 0 0 1i 0

5x 1y 0 0 0

0 0 0 0 0

8.3 11.7 1.8 3.1 1.6

311 66 65 55 29

4.50 33.33 –6.15 30.91 –3.45

MS MT NC ND NE

2 25 434 75 59

0 3 44 23 9

2 22 390 52 50

0 0 25 6 5

0 1 7 12 3

0 1 9 0 1

0 1 2 4 0

0 0 1 1 0

0 0 0 0 0

0 0 208 0 1

2 15 28 2 13

0 7 83 50 35

0 0 68 0 1

0 0 3j 0 0

0 0 0 0 0

0 0 0 0 0

0.6 6.0 10.6 10.3 5.1

2 17 431 24 35

0.00 47.06 0.70 212.50 68.57

NH NJ NM NV NY

29 309 48 20 425

1 21 2 0 29

28 288 46 20 396

1 20 0 0 22

0 1 0 0 5

0 0 2 0 0

0 0 0 0 1

0 0 0 0 1

0 0 0 0 0

13 146 2 0 186

4 68 6 20 115

7 56 33 0 53

2 9 4 0 28

1k 0 1l 0 7m

1z 9aa 0 0 7ab

0 0 0 0 0

6.1 10.0 9.2 6.7 6.3

25 294 18 20 369

16.00 5.10 166.67 0.00 15.18

NYC OH OK OR PA

13 41 81 17 433

0 0 27 0 50

13 41 54 17 383

0 0 1 0 41

0 0 11 0 6

0 0 7 0 0

0 0 4 0 3

0 0 4 0 0

0 0 0 0 0

9 2 0 0 237

3 39 3 14 63

0 0 49 0 47

0 0 1 3 26

1n 0 1° 0 5p

0 0 0 0 5ac

0 0 0 0 0

3.2 1.3 6.8 4.4 5.4

12 50 60 17 453

8.33 –18.00 35.00 0.00 –4.42

PR RI SC SD TN

73 28 137 60 48

32 2 6 21 5

41 26 131 39 43

6 2 4 2 1

2 0 2 16 0

18 0 0 0 2

6 0 0 3 2

0 0 0 0 0

0 0 0 0 0

0 9 66 0 2

0 8 25 3 10

0 8 21 36 31

0 1 18 0 0

41q 0 1r 0 0

0 0 0 0 0

0 0 0 0 0

40.3 4.9 7.1 7.4 2.5

47 28 109 40 64

55.32 0.00 25.69 50.00 –25.00

TX UT VA VT WA

683 15 597 67 9

44 0 52 5 0

639 15 545 62 9

14 0 28 3 0

9 0 15 1 0

16 0 3 0 0

4 0 4 0 0

1 0 2 1 0

0 0 0 0 0

19 0 272 30 0

331 15 20 6 9

273 0 185 26 0

13 0 52 0 0

3s 0 4t 0 0

0 0 12ad 0 0

0 0 0 0 0

6.1 3.7 13.7 16.5

1,019 7 649 28 11

–32.97 114.29 –8.01 139.29 –18.18

WI WV WY

30 68 26

0 5 2

30 63 24

0 2 1

0 0 1

0 2 0

0 1 0

0 0 0

0 0 0

0 37 0

29 4 14

1 14 10

0 4 0

0 2u 0

0 2ae 0

0 0 0

21 138 26

42.86 –50.72 0.00

1,953 31.69 13.28 1,981 –1.41

1,680 27.26 6.38 1,380 21.74

1,539 24.97 30.98 1,627 –5.41

340 5.52 18.34 427 –20.37

85 1.38 3.36 72 18.06

46 0.75 2.01 48 –4.17

1 0.02 — 6 –83.33

6,037

2.09

Total % 2012 % Pos 2012 Total 2011 % Change

6,163 100.00 6.18 6,037 2.09

519 5,643 257 115 8.42 91.56 4.17 1.87 1.04 11.22 1.07 8.67 496 5,535 303 65 4.64 1.95 –15.18 76.92

84 1.36 0.37 70 20.00

47 0.76 5.04 44 6.82

13 0.21 2.72 12 8.33

3 0.05 1.32 2 50.00

2.3 1.3 4.9 4.1 —

*Other domestic includes a2 bison; b1 llama. †Other wild includes c1 cougar, 1 ringtail; d3 bobcats, 1 not provided; e3 bobcats, 1 coyote; f1 coyote; g1 coyote; h1 deer, 1 opossum; i1 deer; j2 bobcats, 1 deer; k1 coyote; l1 coyote; m5 deer, 1 mink, 1 otter; n1 opossum; o1 bobcat; p1 bobcat, 3 deer, 1 opossum; q41 mongooses; r1 bobcat; s2 coyote, 1 deer; t1 bear, 3 bobcats; u2 bobcats. ‡Rodents and lagomorphs include v2 groundhogs; w2 groundhogs; x5 groundhogs; y1 groundhog; z1 groundhog; aa9 groundhogs; ab7 groundhogs; ac5 groundhogs; ad4 beavers, 8 groundhogs; ae2 groundhogs. — = Not applicable. NYC = New York City. Pos = Positive.

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 808

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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% JAVMA, Vol 243, No. 6, September 15, 2013

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.

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.

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 Figure 4—Reported cases of rabies involving bats, by county, 2012. Histogram were reported from states where raccoon rarepresents number of counties in each category for total number of bats submit- bies is enzootic. No rabid lagomorphs were ted for testing. reported during 2012. Rabies virus variants were reported for 4 of the 7 rabid coyotes reported in increase; Figure 5). A total of 51.5% of all rabid skunks 2012. This included 2 rabid coyotes infected with the were from states where the raccoon rabies virus variant south central skunk rabies virus variant (Texas), 1 is enzootic (7.0% increase). Overall, for states where coyote infected with the Arizona gray fox rabies virus skunks are the primary reservoir for rabies, 29.4 anivariant (New Mexico), and 1 coyote infected with the mals/100,000 persons were submitted for rabies testing raccoon rabies virus variant (New Hampshire). Variant during 2012, down from 30.7 animals/100,000 persons information was not reported for rabid coyotes in Georsubmitted in 2011. For states in which the primary gia (1), Kansas (1), and Massachusetts (1). terrestrial variant was south central, north central, and California skunk rabies virus variants, 26.8 aniRabies in Domestic Animals mals/100,000 persons, 39.4 animals/100,000 persons, and 15.9 animals/100,000 persons were submitted for During 2012, domestic animals accounted for 8.4% testing, respectively. (519) of all rabid animals reported, an increase of 4.6%, JAVMA, Vol 243, No. 6, September 15, 2013

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Table 2—Species of bats submitted for rabies testing in the United States during 2012. Species (common name)

No. tested

No. positive

Percentage positive

13,451 11,999 848 355 184

1,031 485 18 43 2

7.7% 4.0% 2.1% 12.1% 1.1%

Tadarida brasiliensis (Mexican free-tailed bat) Lasionycteris noctivagans (silver-haired bat) Myotis species (not further speciated) Lasiurus cinereus (hoary bat) Myotis californicus (California myotis)

177 160 69 60 55

37 8 4 29 1

20.9% 5.0% 5.8% 48.3% 1.8%

Myotis evotis (long-eared myotis) Myotis ciliolabrum (western small-footed bat) Lasiurus seminolus (Seminole bat) Myotis keenii (Keen’s myotis) Myotis yumanensis (Yuma myotis)

50 25 19 17 17

4 4 3 0 0

8.0% 16.0% 15.8% 0.0% 0.0%

Parastrellus hesperus (canyon bat) Myotis volans (long-legged myotis) Perimyotis subflavus (tri-colored bat) Lasiurus ega (southern yellow bat) Myotis austroriparius (southeastern myotis)

14 10 10 9 9

6 0 1 2 0

42.9% 0.0% 10.0% 22.2% 0.0%

Myotis septentrionalis (northern long-eared myotis) Family Molossidae (not further speciated) Myotis auriculus (southwestern myotis) Rousettus aegyptiacus (Egyptian rousette*) Myotis sodalis (Indiana bat)

8 6 6 4 3

0 3 0 0 0

0.0% 50.0% 0.0% 0.0% 0.0%

Plecotus townsendii (Townsend’s big-eared bat) Antrozous pallidus (desert pallid bat) Euderma maculatum (spotted bat) Myotis grisescens (gray myotis) Myotis leibii (small-footed myotis) Myotis thysanodes (fringed myotis)

2 1 1 1 1 1

0 0 1 0 1 0

0.0% 0.0% 100.0% 0.0% 100.0% 0.0%

27,572

1,683

6.1%

Unspeciated Eptesicus fuscus (big brown bat) Myotis lucifigus (little brown bat) Lasiurus borealis (red bat) Nycticeius humeralis (evening bat)

Total *Exotic species submitted by zoos.

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 Figure 5—Reported cases of rabies involving skunks, by county, 2012. Histogram all rabid dogs, and 16.7% (14) reportedly represents number of counties in each category for total number of skunks sub- had an unknown vaccination history; in mitted for testing. 4.8% (4), vaccinations were reportedly not up to date. Vaccination status was not provided for compared with the number reported in 2011. With the 41.7% (35) of the rabid dogs. Most of the rabid dogs in exception of cats, the number of cases of rabid animals which a rabies virus variant was reported were infected reported during 2012 was increased for all species of 810

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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.

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 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 [10.6%]), North Dakota (4 [8.5%]), Oklaand dogs submitted for testing. homa (4 [8.5%]), and Texas (4 [8.5%]). The number of rabid sheep and goats reported with the south central skunk rabies virus variant (26 during 2012 (13) increased by 8.3%, compared with [72.2%]), followed by the raccoon rabies virus variant the number reported during 2011. Other rabid domes(5 [13.8%]), north central skunk rabies virus variant (4 tic animals reported included 2 bison from Colorado [11.1%]), and arctic fox rabies virus variant (1 [2.7%]). and a llama from Georgia. Variant information was not reported for rabid dogs in Puerto Rico (18), North Carolina (9), Georgia (7), Rabies in Humans Florida (2), Arkansas (2), Kentucky (2), West Virginia (2), Alaska (1), Alabama (1), California (1), Montana Samples from 33 humans from 23 states were (1), Nebraska (1), and Virginia (1). submitted to the CDC for rabies testing during 2012, representing a 26.8% decrease from the number for Cats—Cats accounted for most of the rabid do2011. One case of human rabies was confirmed in 2012 mestic animals (257 [49.9%]) reported during 2012, (Table 3). Thirty-one cases of human rabies have been JAVMA, Vol 243, No. 6, September 15, 2013

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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 onset

Date of death

Reporting state Age (y) Sex Exposure*

10 Feb 03 28 May 03 23 Aug 03

10 Mar 03 5 Jun 03 14 Sep 03

VA PR CA

25 64 66

M M M

Unknown Bite-Puerto Rico Bite

Raccoon, eastern United States Dog/mongoose, Puerto Rico Bat, Ln

9 Feb 04 27 Apr 04 25 May 04 27 May 04 29 May 04 2 Jun 04

15 Feb 04 3 May 04 31 May 04 21 Jun 04 9 Jun 04 10 Jun 04

FL AR OK TX TX TX

41 20 53 18 50 55

M M M M F F

Bite-Haiti Bite (organ donor) Liver transplant Kidney transplant Kidney transplant Arterial transplant

Dog, Haiti Bat, Tb Bat, Tb Bat, Tb Bat, Tb Bat, Tb

12 Oct 04 19 Oct 04

Survived 26 Oct 04

WI CA

15 22

F M

Bite Bat, unknown Unknown-El Salvador Dog, El Salvador

27 Sep 05

27 Sep 05

MS

10

M

Contact

Bat, unknown

4 May 06 30 Sep 06 15 Nov 06

12 May 06 2 Nov 06 14 Dec 06

TX IN CA

16 10 11

M F M

Contact Bite Bite-Philippines

Bat, Tb Bat, Ln Dog, Philippines

19 Sep 07

20 Oct 07

MN

46

M

Bite

Bat, unknown

16 Mar 08 19 Mar 08

18 Mar 08 30 Nov 08

CA MO

16 55

M M

Bite-Mexico Bite

Fox, Tb related Bat, Ln

25 Feb 09 5 Oct 09 20 Oct 09 23 Oct 09

Survived 20 Oct 09 11 Nov 09 20 Nov 09

TX IN MI VA

17 43 55 42

F M M M

Contact Unknown Contact Contact-India

Bat, unknown Bat, Ps Bat, Ln Dog, India

2 Aug 10 24 Dec 10

21 Aug 10 10 Jan 11

LA WI

19 70

M M

Bite-Mexico Unknown

Bat, Dr Bat, Ps

30 Apr 11 30 Jun 11 14 Aug 11 Sep 11 3 Dec 11 Dec 11

Survived 20 Jul 11 21 Aug 11 Oct 11 19 Dec 11 Jan 12

CA NJ NY MA SC MA

8 73 25 40 46 63

F F M M F M

Unknown Bite-Haiti Contact-Afghanistan Contact-Brazil Unknown Contact

Unknown Dog, Haiti Dog, Afghanistan Dog, Brazil Tb My sp

6 Jul 12

31 Jul 12

CA

34

M

Bite

Bat, Tb

31 Jan 13 21 Aug 11 16 May 13

27 Feb 13 1 Sep 11 11 Jun 13

MD NC TX

49 20 28

M M M

Kidney transplant Contact Unknown-Guatemala

Raccoon, eastern United States Raccoon, eastern United States Dog, Guatemala

Rabies virus variant†

*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.

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. 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 812

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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 JAVMA, Vol 243, No. 6, September 15, 2013

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 JAVMA, Vol 243, No. 6, September 15, 2013

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 wholesalerspecific 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. Vet Med Today: Public Veterinary Medicine

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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 ad814

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dition, 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. a.

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

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