Epidemiology of rabies in bats in Texas (2001–2010)

Bonny C. Mayes Texas Department of State Health Services, Zoonosis Control Branch, MC 1956, PO Box 149347, Austin, TX 78714.

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Pamela J. Wilson Texas Department of State Health Services, Zoonosis Control Branch, MC 1956, PO Box 149347, Austin, TX 78714.

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Ernest H. Oertli Texas Department of State Health Services, Zoonosis Control Branch, MC 1956, PO Box 149347, Austin, TX 78714.

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Patrick R. Hunt Texas Department of State Health Services, Zoonosis Control Branch, MC 1956, PO Box 149347, Austin, TX 78714.

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Rodney E. Rohde Clinical Laboratory Science Program, Texas State University, San Marcos, TX 78666.

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Abstract

Objective—To obtain epidemiological information on rabies in bats in Texas.

Design—Epidemiological study.

Sample—Laboratory reports of bats that had been submitted for rabies testing in Texas from 2001 through 2010.

Procedures—Laboratory reports were reviewed to obtain information on seasonality of rabies in bats; distribution, species, and rabies virus variants of rabid bats; and human and domestic animal exposures to rabid bats.

Results—The number of rabid bats during the first 5 years of the study period remained static until a > 2-fold increase in 2006; during the subsequent 4 years, the annual number of rabid bats remained at this higher level, including a peak in 2008. The highest proportions of rabid bats were seen in late summer and early fall. The Brazilian free-tailed bat (Tadarida brasiliensis) was the most often affected species. Additionally, the rabies virus variant associated with the Brazilian free-tailed bat was the most prevalent. The percentage of rabid bats from urban areas was greater than that from rural areas. Dogs and cats were the domestic animals most frequently exposed to rabid bats. Most humans exposed to rabid bats did not report a known bite or scratch. The highest numbers of humans exposed to rabid bats were males between 11 to 15 years old.

Conclusions and Clinical Relevance—Information on the epidemiology of rabies in bats and the epidemiology of exposures to rabid bats may be useful in planning and implementing local, state, and national rabies control and prevention campaigns and in encouraging rabies vaccination of domestic animals.

Abstract

Objective—To obtain epidemiological information on rabies in bats in Texas.

Design—Epidemiological study.

Sample—Laboratory reports of bats that had been submitted for rabies testing in Texas from 2001 through 2010.

Procedures—Laboratory reports were reviewed to obtain information on seasonality of rabies in bats; distribution, species, and rabies virus variants of rabid bats; and human and domestic animal exposures to rabid bats.

Results—The number of rabid bats during the first 5 years of the study period remained static until a > 2-fold increase in 2006; during the subsequent 4 years, the annual number of rabid bats remained at this higher level, including a peak in 2008. The highest proportions of rabid bats were seen in late summer and early fall. The Brazilian free-tailed bat (Tadarida brasiliensis) was the most often affected species. Additionally, the rabies virus variant associated with the Brazilian free-tailed bat was the most prevalent. The percentage of rabid bats from urban areas was greater than that from rural areas. Dogs and cats were the domestic animals most frequently exposed to rabid bats. Most humans exposed to rabid bats did not report a known bite or scratch. The highest numbers of humans exposed to rabid bats were males between 11 to 15 years old.

Conclusions and Clinical Relevance—Information on the epidemiology of rabies in bats and the epidemiology of exposures to rabid bats may be useful in planning and implementing local, state, and national rabies control and prevention campaigns and in encouraging rabies vaccination of domestic animals.

Rabies is an acute, infectious viral disease that affects the CNS of mammals. Generally transmitted via the bite of an infected animal, rabies is nearly always fatal once there are clinical signs. During 2001 through 2010, 94% of all laboratory-confirmed cases of rabies in Texas occurred in wildlife species, with skunks and bats being the most commonly affected species. An analysis of yearly rabies reports1 revealed that bats were the most commonly infected species in Texas from 2006 through 2010. Texas has more bat species2,3 and more laboratory-confirmed rabid bats4 than any other state in the United States. For the 10-year period from 2001 through 2010, a mean of 3,107 bats/y were tested for rabies and 11% of those bats tested positive.1

Rabies in bats has important public health implications. Of the 50 states, only Hawaii is considered rabies-free. Rabid bats have been documented in all the other 49 states. Bats are increasingly implicated as important wildlife reservoirs for rabies virus variants transmitted to humans. Typically, 2 to 3 human rabies cases occur each year in the United States; from 1995 through 2011, all except 1 indigenous case was due to a bat rabies virus variant. In most bat-associated cases of rabies in humans, bat bites were either undetected or unreported.5 A greater understanding of the epidemiology of bat rabies virus variants in Texas will be useful in the planning and implementation of rabies awareness and prevention campaigns.6 Additionally, such information is relevant to veterinarians and physicians in clinical practice when discussing rabies prevention guidelines with their clients. The purpose of the study reported here was to obtain epidemiological information on rabies in bats in Texas and the impact of rabid bats on humans and animals in the state. Specifically, the objectives were to obtain information on the prevalence of rabies in bats, including monthly variations; bat species submitted for rabies testing; virus variants associated with rabies in bats, other wildlife, and domestic animals; domestic animal exposures to rabid bats; the age and gender of humans exposed to rabid bats; and the usual routes of exposure of humans to rabid bats.

Materials and Methods

Data for the present study were obtained from laboratory reports on bats submitted for rabies testing and field investigation reports of those bats that were confirmed through laboratory testing to be positive for rabies in the state of Texas from 2001 through 2010. According to available data, approximately 83% of bats tested for rabies during this period were submitted because of concerns that they had exposed or potentially exposed a person or domestic animal to rabies. The duration of the subclinical viral shedding period in rabid bats is not known; additionally, by definition in Texas state law, bats are high-risk animals for rabies transmission. Therefore, the Texas Administrative Code7 required that any bat that had bitten or otherwise potentially exposed a human to rabies be euthanized and tested for the presence of rabies virus. Rabies case investigations were performed by personnel from the Texas Department of State Health Services Regional Zoonosis Control offices, local health departments, or local rabies control authorities. Although somewhat arbitrary, for classification purposes, bats considered to be urban were within established municipal boundaries, whereas those considered to be rural were located outside these official boundaries.

Rabies testing was performed by laboratories associated with the Texas Department of State Health Services in Austin, the El Paso City-County Health Department, the Houston Department of Health and Human Services, the San Antonio Metropolitan Health District, or the Department of Defense Veterinary Food Analysis and Diagnostic Laboratory at Fort Sam Houston (Figure 1). Submitted bat specimens were tested for rabies virus antigen by means of direct immunofluorescence microscopic examination of brain tissue impressions. Typing of rabies virus variants was performed at the Texas Department of State Health Services laboratory; antigenic analysis of specimens that tested positive for rabies virus was performed with monoclonal antibodies against the viral nucleoprotein to identify rabies virus variants.8 Atypical or unexpected results were confirmed by means of genetic analysis of the nucleoprotein sequence.9 In addition, a bioinformatic search toola was used to compare sequence data to sequences in GenBank10 to deter-mine the closest match and likely source of the virus; 18 phylogenetic lineages of rabies virus have been identified in bats in the United States.11

Figure 1—
Figure 1—

Map of Texas depicting laboratory-confirmed rabies cases in bats (2001 to 2010), major bat colonies, and rabies testing laboratories in Texas.

Citation: Journal of the American Veterinary Medical Association 243, 8; 10.2460/javma.243.8.1129

Complete information on bat species and rabies virus variant was only available on specimens submitted to the Texas Department of State Health Services rabies laboratory. Morphological characteristics, including standard measurements such as antebrachium length, were used for species determination on all bats submitted to the Texas Department of State Health Services.2,3 Bats that could not be easily identified were sent to Angelo State University, San Angelo, Tex, for species confirmation; genetic analysis was performed on those that could not be identified on the basis of morphology alone.12,13 Bat species and rabies virus variant information was only available for a small percentage of samples from the other 4 laboratories that performed rabies testing; therefore, pertaining to bat species and rabies virus variant data, only the data from the Texas Department of State Health Services rabies laboratory were included in the present study. These data represent nearly half (14,340/31,072 [46%]) of total submissions from all these laboratories and more than half (1,940/3,333 [58%]) of the total bats statewide that tested positive for rabies.

Results

Annual variations in numbers of rabid bats—The total number of rabid bats in Texas from 2001 through 2010 (Figure 2) revealed a > 2-fold increase between the years 2001 and 2006, with a peak in 2008 and a positivity rate low of 9% (194/2,207) in 2001 to a positivity rate high of 12% (269/2,194) in 2004. The 5 years of the highest number of rabid bats and greatest number of bats submitted for testing were the same.

Figure 2—
Figure 2—

Number of bats submitted for rabies testing at the Houston Department of Health and Human Services (white triangles) and for all of Texas (gray triangles) from 2001 through 2010. During these years, the number of bats that tested positive for rabies (white circles) and positivity rate of bats (gray circles) are depicted.

Citation: Journal of the American Veterinary Medical Association 243, 8; 10.2460/javma.243.8.1129

Distribution of rabid bats—The latitude and longitude where each rabid bat was located was recorded, and these data were analyzed with geographic information system software and 2000 census data14 to classify rabid bats as coming from an urban or rural setting. During the 10-year period from 2001 through 2010, the percentage of rabid bats submitted from urban areas (2,626/3,333 [79%]) greatly outnumbered those from rural settings (707/3,333 [21%]).

Monthly variation in numbers of rabid bats— When data for 2001 through 2010 were combined, the numbers of rabid bats peaked slightly during April and May (Figure 3). A second, more substantial, increase in numbers of rabid bats occurred from August through October. The lowest percentage (40/1,185 [3%]) of bats tested positive for rabies in January, and the highest percentage (678/2,306 [29%]) tested positive for rabies in September.

Figure 3—
Figure 3—

Monthly distribution of total number of bats submitted for rabies testing (gray bars), number of rabid bats (black bars), and positivity rate of bats (line) in Texas from 2001 through 2010.

Citation: Journal of the American Veterinary Medical Association 243, 8; 10.2460/javma.243.8.1129

Species of rabid bats—From 2001 through 2010, 31,072 bats were received for testing at statewide laboratories; species information for the 14,340 (46%) bats that were received for testing at the Texas Department of State Health Services laboratory was recorded at the time the specimen was processed at the laboratory. Of these 14,340 bats, 97 (0.7%) could not be identified and 77 (0.5%) could only be identified to the genus level. Twenty-three bat species were received for testing; 1,940 of the 14,340 (14%) bats tested positive for rabies, and 12 bat species had at least 1 bat that tested positive for rabies (Table 1). Of the 1,940 bats that tested positive for rabies, 1,558 (80%) were identified as Brazilian (also known as Mexican) free-tailed bats (Tadarida brasiliensis) and 208 (11%) were identified as eastern red bats (Lasiurus borealis); 10 bat species were responsible for the remaining 174 (9%) cases. Of species of bats with sample sizes > 25, hoary bats (Lasiurus cinereus) had the highest mean positivity rate (55/133 [41%]) followed by Brazilian free-tailed bats (1,558/8,904 [18%]).

Table 1—

Species of bats submitted to the Texas Department of State Health Services laboratory for rabies testing from 2001 through 2010.

SpeciesTotalNo. (%) of positive test results for rabies
Pallid bat (Antrozous pallidus)*573 (5)
Jamaican fruit bat (Artibeus jamaicensis)50
Mexican long-tongued bat (Choeronycteris mexicana)20
Rafinesque's big-eared bat (Corynorhinus rafinesquii)10
Townsend's big-eared bat (Corynorhinus townsendii)30
Vampire bat (Desmodus rotundus)20
Big brown bat (Eptesicus fuscus)273 (11)
Western mastiff bat (Eumops perotis)11
Silver-haired bat (Lasionycteris noctivagans)250
Eastern red bat (Lasiurus borealis)2,263208 (9)
Hoary bat (Lasiurus cinereus)13355 (41)
Southern yellow bat (Lasiurus ega)1377 (5)
Northern yellow bat (Lasiurus intermedius)39334 (9)
Seminole bat (Lasiurus seminolus)14925 (17)
Lasiurus sp80
Southeastern myotis (Myotis austroriparius)80
Cave bat (Myotis velifer)5132 (0.4)
Yuma myotis (Myotis yumanensis)10
Myotis sp§50
Evening bat (Nycticeius humeralis)1,30432 (2)
Big free-tailed bat (Nyctinomops macrotis)120
American perimyotis (Perimyotis subflavus)2249 (4)
American parastrelle (Parastrellus hesperus)10
Egyptian fruit bat (Rousettus egypticus)10
Brazilian free-tailed bat (Tadarida brasiliensis)8,9041,558 (18)
Unable to identify972 (2)
Yellow bat (L ega or L intermedius)#641 (2)

Most of these pallid bats were part of a captive research colony at Texas A&M University.

Vampire bats were part of a captive colony in a zoo.

Too damaged to determine species (probably L borealis, L cinereus, L ega, L intermedius, or L seminolus).

Too damaged to determine species (probably M austroriparius, M velifer, or M yumanensis).

Fruit bat escaped from a reptile show.

Extremely damaged, decomposed, or immature.

Unable to differentiate on the basis of measurements.

Rabies virus variants—Of the 31,072 bats submitted for rabies testing during the study period, 3,333 (11%) bats tested positive for rabies (Figure 1); of the 3,333 bats, information on the rabies virus variant was available for 1,922 (58%) bats (Figure 4). Of these, 1,887 (98%) were infected with the bat rabies virus variant associated with that particular bat species; of the 1,922 bats, 33 (2%) bats had cross-species transmission (spillover) and 2 (0.1%) bats were not identified to species but the rabies virus variant was determined. The Brazilian free-tailed bat (T brasiliensis)–associated rabies virus variant was responsible for 1,549 of 1,922 (81%) cases for which a bat rabies virus variant could be identified; the rabies virus variants associated with eastern red bats (L borealis) and Seminole bats (Lasiurus seminolus) accounted for 242 of 1,922 (13%) cases. Rabies virus variants associated with other bat species accounted for the remaining 7% of cases. Of the 33 spillover cases, Lasiurus spp rabies virus variants, primarily L borealis–, L seminolus–, and L cinereus-associated rabies virus variants, accounted for the majority (26 [79%]); the T brasiliensis–associated rabies virus variant was responsible for the second highest number of spillover cases (6 [18%]). Spillover was present in more evening bats (Nycticeius humeralis) than any other bat species; 12 of the 32 (38%) positive evening bats were typed as other than N humeralis–associated rabies virus variant, primarily Lasiurus spp rabies virus variants.

Figure 4—
Figure 4—

Distribution (%) of rabies virus variants confirmed in 1,922 rabid bats identified in Texas from 2001 through 2010. The LbV and LsV (LbV/LsV) bat–associated rabies virus variants are closely related variants that are difficult to distinguish and have identical antigenic typing patterns; the Texas Department of State Health Services laboratory does not differentiate them. The LxLiV and LiV (LxLiV, LiV) bat–associated rabies virus variants are grouped in the graph; both rabies virus variants are associated with northern yellow bats and have been detected in southern yellow bats. ApV = Antrozous pallidus. EfV = Eptesicus fuscus. LbV = Lasiurus borealis. LcV = Lasiurus cinereus. LiV = Lasiurus intermedius. LsV = Lasiurus seminolus. LxLiV = Lasiurus xanthinus and Lasiurus intermedius. MspV = Associated with various Myotis spp. NhV = Nycticeius humeralis. PsV = Perimyotis subflavus. TbV = Tadarida brasiliensis.

Citation: Journal of the American Veterinary Medical Association 243, 8; 10.2460/javma.243.8.1129

Figure 5—
Figure 5—

Numbers of exposed humans (white triangles; n = 702) and domestic animals (gray triangles; 1,107) and number of rabid bats (white circles; 3,333) in Texas from 2001 through 2010.

Citation: Journal of the American Veterinary Medical Association 243, 8; 10.2460/javma.243.8.1129

Over the study period, of the 5,798 laboratory-confirmed terrestrial mammal rabies cases, there were 13 (0.2%) documented cases (in none of which did the animals involved have a reported history of being previously vaccinated against rabies) of spillover of bat rabies virus variants. Five of the 13 cases occurred in cats, 4 in bovids, 2 in dogs, and 2 in ringtail cats. Three of the 4 bovine cases involved the imported vampire bat (Desmodus rotundus)–associated rabies virus variant in steers imported from Mexico. Seven of the 13 terrestrial mammal spillover species were infected with the T brasiliensis–associated rabies virus variant; there was 1 case of infection with L borealis– or L seminolus–associated rabies virus variant (these variants are antigenically indistinguishable) in a calf and 1 case of infection with the American perimyotis (Perimyotis subflavus)–associated rabies virus variant in a cat. One spillover case involving a ringtail cat was identified as a bat rabies virus variant by antigenic (monoclonal) typing, but sequencing was not performed and thus the specific bat rabies virus variant was not identified.

Exposure of domestic animals to rabid bats—From 2001 through 2010, there were 1,107 domestic animals with known exposures to rabid bats; the 3 years during this period with the highest number of exposed animals were the same as the 3 years when the greatest number of rabid bats were reported (Figure 5). Of 1,080 domestic animals identified as exposed to rabid bats for which complete data were available, 776 (72%) were dogs, 303 (28%) were cats, and 1 (0.1%) was a horse. Of the 1,080 exposed animals, 714 (66%), including 546 dogs (70% vaccination rate), 167 cats (55% vaccination rate), and the horse, were considered to be current on vaccination; of these 714 animals, 645 (90%) received a rabies vaccination and a 45-day confinement, 60 (8%) received a series of 3 rabies vaccinations and a 90-day confinement, and 9 (1%) were euthanized. Of the 1,080 animals exposed to rabid bats, the remaining 366 (34%) animals, including 230 dogs and 136 cats, were considered to be not current on vaccination (this included those animals with a vaccination history that was not appropriately documented or for which there was no history of vaccination). Of these 366 animals, 7 (2%) received a vaccination and a 45-day confinement, 259 (71%) received a series of 3 vaccinations and a 90-day confinement, and 100 (27%) were euthanized. None of the animals that received postexposure prophylaxis because of exposure to a rabid bat were reported to have developed rabies.

Exposure of humans to rabid bats—From 2001 through 2010, there were 702 humans exposed to 421 rabid bats. Multiple individuals were exposed to a single bat in approximately one-third (129) of the investigated incidents. The number of bat submissions and laboratory-confirmed bats that tested positive for rabies increased substantially from 2006 through 2010, but the number of humans exposed to rabid bats did not increase proportionately (Figure 5).

Gender was known for 699 of the exposed humans; of these, 397 (57%) were males and 302 (43%) were females. Information on age was available for 619 of the 702 humans exposed to rabid bats during these years. For males, the highest number of exposed individuals were between 11 and 15 years old (Figure 6); for females, the highest number of exposed individuals were between < 1 and 5 years of age. Individuals < 16 years of age comprised over half (317/616 [51%]) of the humans (for which age and gender were available) exposed to rabid bats. The location of the exposure was ascertained in 660 case investigations. According to information recorded by case investigators for all age groups, 353 of 660 (53%) humans were exposed to rabid bats at their residence (inside the home or in the yard), making it the most common exposure location; the second most common exposure location was at school, including child-care centers, with 167 of 660 (25%) exposures. However, 196 of 660 exposures with recorded locations occurred in males < 16 years of age, and the number of school exposures for this age group (95/196 [48%]) was greater than the number of residential exposures (67/196 [34%]) for this age group.

Figure 6—
Figure 6—

Age and gender (males, black bars; females, gray bars) distribution of 616 humans exposed to rabid bats in Texas from 2001 through 2010. Data given for 357 males and 259 females for which gender and age were known.

Citation: Journal of the American Veterinary Medical Association 243, 8; 10.2460/javma.243.8.1129

The majority of the 702 humans exposed to rabid bats did not report a known bite or scratch; 289 (41%) reported handling rabid bats and 227 (32%) did not know whether an exposure occurred (eg, individuals who woke up with a rabid bat in the same room). A known or possible bite or scratch was reported by 147 of 702 (21%) individuals. The exposure circumstances were not documented in 30 of 702 (4%) cases. The remaining 9 of 702 (1%) cases involved exposures that were indirect or questionable: 1 person reported getting bat saliva in the eye, several people were licked or bitten by their pet after the pet was exposed to a rabid bat, and 1 person reported touching a cage that housed a rabid bat. At least 619 of the 702 (88%) individuals reported as exposed to rabid bats received rabies postexposure prophylaxis, a minimum of 56 of 702 (8%) individuals did not receive postexposure prophylaxis, and documentation was lacking for the remaining 27 of 702 (4%).

Of the 421 rabid bats involved in human exposures, the majority (263/421 [62%]) of these bats were encountered outside, whereas 121 of 421 (29%) were encountered inside buildings. Investigation reports indicated that pets were responsible for transporting 32 of the 421 (8%) bats into home environments. The location of 37 of 421 (9%) rabid bats involved in these exposures was not documented. Only 57 of 421 (14%) of the rabid bats involved in human exposures were reportedly flying when the exposure occurred; 245 of 421 (58%) bats were down and appeared to be sick or injured, and 76 of 421 (18%) were dead. Information regarding the physical state of the remaining 43 of 421 (10%) bats was not provided.

The 702 human exposures to 421 rabid bats occurred in 82 of the 254 counties in Texas. Of the rabid bats associated with exposures, 196 (47%) were located in 4 counties: Travis County (81 [19%]), Williamson County (54 [13%]), Harris County (34 [8%]), and Bexar County (27 [6%]).

In addition to these data on humans exposed to rabid bats, it was determined that 208 additional humans were potentially exposed to 163 bats that were submitted for testing but could not be determined to be positive or negative for rabies because they were either decomposed or destroyed on arrival at the laboratory. Of those 208 humans, at least 138 (66%) received postexposure prophylaxis (44 [21%] did not receive postexposure prophylaxis and 26 [13%] did not have the postexposure prophylaxis status indicated); similar to exposures to rabid bats, the majority of exposures to decomposed or destroyed bats was in males (135 [65%]) and in the age group of < 16 years (125 [60%]).

Discussion

Brazilian free-tailed bats comprised the majority (80%) of bats tested from 2001 through 2010. The high positivity rate (18%) in this species explains the high mean positivity rate (11%) during the study period. Similarly, several states having large populations of Brazilian free-tailed bats report 10% to 15% laboratory rabies positivity rates for bats on their state public health or similar informational websites. Some of the largest colonies and most dense groupings of bats in Texas occur within urban settings. One such example is the Congress Avenue Bridge15 colony in Austin, Tex (Figure 1); 1.5 million Brazilian free-tailed bats live under the bridge, which is a major tourist attraction. Where there are substantial numbers of bats residing in areas with large populations of humans and domestic animals, there will be more encounters with bats and thus larger numbers submitted for rabies testing. Brazilian free-tailed bats are considered to be a gregarious and synanthropic species, which could contribute to a higher potential for contact with humans. Species that roost in more conspicuous areas visible to humans are also more likely to have contact with humans and be submitted for rabies testing.16 During the study period, the highest proportion of rabid bats was detected in late summer and early fall, followed by a slight increase in spring, consistent with what has been described in another report.16 Bats in the United States, both migratory and nonmigratory, are most active during summer and early fall; during this time, bats engage in swarming and prepare for migration or hibernation, and young bats are weaning and starting to fly.17 The slight increase in rabid bats in spring is probably due primarily to the large influx of Brazilian free-tailed bats to summer maternity colonies from their winter hibernacula; the densest concentrations of this species are found in Texas, where they congregate in innumerable maternity colonies, each of which consists of millions of individuals.15

The number of bat submissions drastically increased in 2006. The mean number of bats tested at the Houston Department of Health and Human Services rabies laboratory prior to 2006 was 773/y; approximately 2,800 were tested there in 2006.1 A teenager from Humble, Tex, a suburb of Houston, died of rabies on May 12, 2006.18 The publicity surrounding the case undoubtedly resulted in an increase in awareness of rabies in bats and therefore bat submissions (approx 93% of the bats submitted to the Houston lab in 2006 were received after May 12). Following the teenager's death, the Regional Zoonosis Control office in Houston and the Houston Department of Health and Human Services rabies laboratory were inundated with phone calls from concerned citizens. Prior to the teenager's death, most animal control agencies would only submit bats involved in pet or human exposures; after the media coverage and resulting heightened concern about bats and rabies, most animal control agencies in the Houston area started submitting all bats, regardless of exposure circumstances.b,c

A fundamental limitation of the present study was that the data were usually obtained from passive surveillance submissions. Some submitting facilities only send bats for rabies testing if humans or domestic animals have been exposed, or potentially exposed, to them. Others will submit bats simply for surveillance purposes. Shipping supplies and fees are expensive, so more nonexposure-related submissions tend to come from areas in close proximity to the rabies testing laboratories where specimens can be hand delivered. Bias is introduced in that bats submitted for testing are often dead or debilitated when they are encountered and are thus more likely to be rabid. Data availability was another issue; the amount of information recorded by investigators varied from region to region. In addition, a database alteration between 2007 and 2008 resulted in some changes in the type of data collected.

The Texas Department of State Health Services rabies laboratory was the only testing facility that routinely identified all bats received for testing. This provides an incomplete representation of bat species submitted for rabies testing and rabies prevalence in statewide bat submissions; nonetheless, these data are valuable. These bats have been very useful for evaluating changes in chiropteran distributions in Texas, and many new county records and range extensions have been documented.3,13 Bats with a solitary nature, such as hoary bats, roost in locations where they are not likely to interact with humans. The higher positivity rate in these bats could be explained by the concept that they are more likely to contact humans and be apparent if they have clinical signs of rabies.16

Antigenic or molecular typing was performed for over half of the bats that tested positive for rabies, and spillover was present in < 2% of these cases; 26 of 33 (79%) cases were due to Lasiurus spp rabies virus variants, primarily L borealis– or L seminolus–associated and L cinereus–associated rabies virus variants. Evening bats are known to inhabit a large variety of roosts and readily use many types of trees as roosting sites,3 so the high rate of spillover in this species may be due to the higher probability that other species may be sharing the same roosts, especially tree-roosting lasiurine bats.

Spillover of vampire bat–associated rabies virus variants into cattle is common in Latin America. Spillover of insectivorous bat–associated rabies virus variants into terrestrial mammals is unusual and generally an isolated event. However, adaptation of bat rabies virus variants to terrestrial mammals occurred in Flagstaff, Ariz, in 2001.19 The rabies-typing data from the Texas Department of State Health Services have been useful for monitoring the changes in rabies reservoirs and rabies virus variants in Texas over time and have been used for determining vaccine bait drop zones for the Oral Rabies Vaccination Program targeting certain terrestrial mammals.20 Tracking this typing information facilitates recognition of novel rabies virus variants and spillover events.

The 5 cats and 2 dogs that died of bat rabies virus variants during this study period did not have a history of being previously vaccinated against rabies. Rabies infections in terrestrial mammals can result from a bat bite or bat ingestion. Domestic cats that are allowed to roam freely outdoors will readily prey on grounded bats and have a tendency to deliver their victims to their owner's residences. Keeping cats current on their rabies vaccinations and confining them indoors will help protect cats and their owners.21 Texas state law requires that cats and dogs be vaccinated against rabies; we found 70% dog-owner compliance and 55% cat-owner compliance.

According to the Texas Administrative Code, domestic animals that have been exposed to a rabid animal must either be euthanized or provided postexposure prophylaxis. For an animal that is not current on vaccination against rabies (animals that had never been previously vaccinated are also included in this category), postexposure prophylaxis consists of immediate vaccination, confinement for 90 days, and booster vaccinations during the third and eighth weeks of confinement. For an animal that is current on vaccination against rabies, postexposure prophylaxis consists of immediate vaccination and confinement for 45 days.22 By definition in state law, to be considered current on vaccination, an animal must have been vaccinated with a rabies vaccine licensed by the USDA for the species at or after the minimum age requirement and the recommended route of administration for that vaccine must have been used, at least 30 days must have lapsed since the initial vaccination, and the time elapsed since the most recent vaccination must not have exceeded the recommended interval for booster vaccination as established by the manufacturer.7 Variances in how postexposure prophylaxis was handled (eg, why some animals that were considered to be current on vaccination received a series of 3 vaccinations and a 90-day confinement period instead of 1 vaccination and a 45-day confinement period) could have stemmed from multiple variables, such as interpretation of what constitutes an exposure, standard operating procedures of local rabies control authorities, and vaccination requirements in city and county ordinances, which may be at a stricter level than state law (eg, a city may require annual vaccination even if a vaccine with a longer duration of immunity was administered to the animal). The data indicating that, of domestic animals exposed to rabid bats, only 1% of those that were current on vaccination were euthanized, compared with 27% of those considered to be not current on vaccination, reinforce the importance of keeping domestic animals current on vaccination against rabies.

The data from this study indicated that most humans exposed to rabid bats did not report a known bite or scratch. Recently published data seem to indicate that transmission of rabies virus can occur from minor, seemingly unimportant, or unrecognized bites from bats.5 In all instances of potential human exposures involving bats, the bat in question should be safely collected, if possible, and submitted for rabies diagnosis. Rabies postexposure prophylaxis is recommended for all persons with bite, scratch, or mucous membrane exposure to a bat, unless the bat is available for testing and there is no evidence of rabies. Rabies postexposure prophylaxis should be considered for persons who were in the same room as a bat and who might be unaware that a bite or direct contact had occurred (eg, a sleeping person awakens to find a bat in the room or an adult witnesses a bat in the room with a previously unattended child, mentally disabled person, or intoxicated person) and rabies cannot be ruled out by testing the bat. The period of rabies virus shedding in bats is unknown; therefore, during the 10-year period of this study, Texas law required that bats, defined in Texas law as being high-risk animals for rabies, be euthanized and tested rather than confined and observed if they had bitten or otherwise potentially exposed a human. Unnecessary administration of postexposure prophylaxis can be avoided by the timely and proper submission of specimens for testing as demonstrated by the decomposed and destroyed bat specimen data. However, even if a specimen appears to be decomposed or badly damaged, it should still be submitted for testing; the laboratory should be the entity to determine the testing viability and status.

The difficulty of obtaining the true description of potential human exposure is evident in the field investigations conducted on the incidents described in the present report. Concern by adolescents that they will be in trouble for their actions, conflicting statements by individuals and associated peers, and uncooperative attitudes for a variety of reasons often make documentation and risk management a challenge. Gathering information pertaining to logistics and demographics related to human exposures to rabid bats provides a valuable public health service. For example, data from this study revealed that males < 16 years of age formed a group with the greatest amount of exposure, particularly in the school environment. Furthermore, according to census data,23,24 there is almost equal distribution between male versus female populations of the younger age groups; therefore, these data support our findings that younger males have a higher exposure rate to rabid bats. With this target group in mind, the Texas Department of State Health Services Zoonosis Control Branch initiated a rabies awareness and prevention poster contest for school children to enhance their awareness of rabies, including the value of rabies vaccinations for domestic animals, how to take preventive measures to avoid being exposed to rabies, and what to do if you think you or your pet have been exposed. In its educational efforts, the Zoonosis Control Branch also has stressed the importance of safely capturing or collecting and submitting for rabies testing any bat with which there could have been a potential exposure to humans or domestic animals.

Although an effective vaccine is available, the cost and anxiety of rabies postexposure prophylaxis are substantial. This descriptive review reveals that location, age group, and gender may be associated with risk of exposure to rabid bats. For pets, exposures result in 2 choices: vaccination along with confinement and observation for an extended period or euthanization.22 Neither option is desirable to the animal or the owner. For exposed children and adults, the postexposure experience is traumatic as well. Public health interventions that promote the reduction of exposure to potential rabies transmission by limiting contact with potentially rabid animals are more cost-effective than treatment.6 Additionally, endeavors toward educating the public about the need to submit a bat for rabies testing if it has been involved in a potential exposure scenario play an important role in rabies prevention efforts. By understanding the epidemiology of rabid bat exposures, focused mitigation efforts are possible.

a.

BLAST, National Center for Biotechnology Information, National Institutes of Health, Bethesda, Md. Available at: blast.ncbi.nlm.nih.gov/. Accessed Oct 3, 2012.

b.

Johnson G, Texas Department of State Health Services, Zoonosis Control Branch, Houston, Tex: Personal communication, 2013.

c.

Turner C, Houston Department of Health and Human Services, Bureau of Laboratory Services, Houston, Tex: Personal communication, 2013.

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