Bat Rabies in the United States and Canada from 1950 through 2007: Human Cases With and Without Bat Contact

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1 MAJOR ARTICLE Bat Rabies in the United States and Canada from 1950 through 2007: Human Cases With and Without Bat Contact Gaston De Serres, 1 Frédéric Dallaire, 2 Mathieu Côte, 2 and Danuta M. Skowronski 3 1 Institut national de santé publique du Québec and 2 Université Laval, Quebec, and 3 British Columbia Centre for Disease Control, Vancouver, Canada Background. Since the 1980s, rare cases of rabies in humans in Canada and the United States have been almost exclusively caused by the bat-variant virus. Methods. We reviewed indigenously acquired cases of bat-variant rabies in humans in Canada and the United States from 1950 through Results. Of 61 cases identified, 5 occurred after organ transplantation and were excluded from further analysis. A bite was reported by 22 (39%) of the case patients, 9 (16%) had a direct contact (i.e., were touched by a bat) but no history of a bite, 6 (11%) found bats in their home (2 [4%] in the room where they slept) but reported no direct contact, and 19 (34%) reported no history of bat exposure whatsoever. With the exception of California (8 cases) and Texas (7 cases), no state or province had 13 cases. Of the case patients, 76% were men, and 40% were years of age. The median incubation period was 7 weeks (!10 weeks in 72% of cases). The incidence of bat-variant rabies cases increased from 2.2 per billion person-years in to 6.7 per billion person-years in Of 36 case patients with bat rabies described since 1990, 16 had no history of direct bat contact; 2 (13%) of the 16 would have qualified for rabies postexposure prophylaxis on the basis of exposure criteria expanded in 1995 to include bats that were in the same room as a sleeping person. The incidence of rabies for this type of exposure was 0.6 cases per billion person-years. Conclusion. The true preventable proportion of cases and the number needed to treat with rabies postexposure prophylaxis to prevent 1 case would be useful information to inform the current guidelines. Rabies is a dreaded disease. The rabies virus causes encephalitis and death in humans and in most other mammals. A distinct species-associated variant characterizes each of the major terrestrial animal hosts. Humans are not natural hosts but can become infected through contact with other rabid animals. With a single documented exception, human cases of rabies have been uniformly fatal [1]. According to the best estimates worldwide, 155,000 deaths occur annually, most of which are associated with dogs [2]. Prevention is through a protocol of rabies postexposure prophylaxis Received 12 October 2007; accepted 10 December 2007; electronically published 21 March Reprints or correspondence: Dr. Gaston De Serres, Institut national de santé publique du Québec, 2400 d Estimauville, Quebec, PQ, Canada, G1E 7G9 (gaston.deserres@ssss.gouv.qc.ca). Clinical Infectious Diseases 2008; 46: by the Infectious Diseases Society of America. All rights reserved /2008/ $15.00 DOI: / (RPEP) that consists of a single dose of immunoglobulin and 5 spaced doses of vaccine. RPEP is safe and effective; failure rates, typically associated with a delay or breach in protocol, have been estimated to range from 1 in 80,000 in developed countries to 1 in 12,000 in developing countries [3]. The reported incubation period varies from a few days to 119 years, but 75% of patients become ill in the first 90 days after exposure [3, 4]. Three principal global areas of rabies have been defined [4]. These areas are (1) countries with enzootic canine rabies (all of Asia, Latin America, and Africa); (2) countries in which canine rabies has been brought under control and wildlife rabies predominates (Western Europe, Canada, and the United States); and (3) rabies-free countries (mostly islands, including England, Australia, and Japan). In Canada and the United States, rabies is enzootic in foxes, skunks, raccoons, and bats; these animals are the only natural reservoirs in Canada and the United States. The first identification Bat Rabies in the US and Canada CID 2008:46 (1 May) 1329

2 of rabid insectivorous bats in North America was in the early 1950s. Since then, the incidence of rabies in bat populations, although known to vary according to the species, its social preferences (colony forming vs. solitary), and migratory patterns, is not known to be on the rise [3, 4]. A program of rabies immunization for domestic dogs led to a dramatic decline in human cases of canine rabies in Canada and the United States in the 1950s. In its place, the bat-variant virus has become the dominant cause of rabies in humans. The advent of the detection of anti-nucleocapsid monoclonal antibody in the late 1970s and the more-recent nucleotide sequencing applied to virus strains recovered from humans has facilitated distinction between bat-variant rabies and virus strains originating in other terrestrial reservoirs; this has led to increased links with bats that may have been previously unknown or unrecognized [3, 5]. Transmission of bat-variant rabies through other terrestrial animals to humans is theoretically possible, but no such human cases have been documented [4]. A squirrel infected with bat-variant rabies was reported to have bitten a person, but RPEP was administered, and human disease did not follow [6]. Bats apply sophisticated echolocation to navigate, and healthy bats are easily able and prefer to avoid collision or other contact with humans. Bats are night creatures, and it is unusual for them to fly in daylight. Those active during the day are suspect, as are any found on the ground. The behavior demonstrated by rabid bats is not always dramatically altered [4]. Although some may become aggressive, others may simply become disoriented, lose their flying ability, and appear clumsy. Healthy juvenile bats acquiring new skills may also demonstrate such erratic behavior. Relentless attachment, particularly to the hands or heads of humans, is a clear sign of abnormality. Bat teeth are very fine, and bat bites may be undetectable as pinpoint puncture marks 1 mm in diameter. Most bat-inflicted scratch marks are!1 cm long. Such minor evidence of contact may be difficult to recall or elicit from a person dying from rabies. In the past 2 decades, most human case patients with bat-variant rabies in the United States and Canada did not report a history of a bat bite [5, 7, 8]. The recognition that indigenous cases of rabies in humans in North America are largely associated with bats and that even direct contact with bats may not be perceived has led to the lowering of the threshold for RPEP administration. In 1995, the Centers for Disease Control and Prevention (CDC) urged consideration of postexposure prophylaxis for persons potentially exposed to bats even where a history of physical contact cannot be elicited [9, p. 272]. This is reflected in guidelines published by advisory committees in the United States in 1999 and in Canada in 2002, which include scenarios in which a bat is found in the same room as a sleeping person, an unattended child, a mentally disabled person, or an intoxicated person [10, 11]. Individual case reports of bat-variant rabies have been published previously. This report summarizes all cases of bat-variant rabies identified in humans in the United States and Canada from 1950 through 2007, including those with and those without recognized bat contact. METHODS We reviewed all human cases of rabies from January 1950 through September 2007 in the United States and Canada as described in the Morbidity and Mortality Weekly Report and Canada Communicable Disease Report. The number of human cases we found with bat-variant rabies corresponds with totals published by the CDC and the Public Health Agency of Canada. Only indigenously acquired cases were considered; cases acquired elsewhere but diagnosed and treated in the United States or Canada were excluded. The incidence rate per person-year was calculated by dividing the number of cases by the sum of the populations of each year from 1950 through Population data were obtained from the US Census Bureau [12, 13] and Statistics Canada [14]. RESULTS From January 1950 through September 2007, the total number of human cases of rabies declined considerably, from a peak of 20 cases in 1952 to never more than 6 cases per year since the 1960s, which mostly reflects the control of canine-variant rabies (figure 1A). Even recently, however, year-to-year variation in the number of human cases of rabies is evident. There were 23 cases for which the source of rabies was unknown, including 21 (21%) of 102 cases from 1950 through 1959 and 2 (7%) of 29 cases from 1960 through Since 1980 and the advent of anti-nucleocapsid monoclonal antibody detection and nucleotide sequencing, distinct species-associated variants were identified in all reported human cases of rabies. Since 1950, 61 human cases of bat-variant rabies were reported in the United States (55 cases) and Canada (6 cases). A list of the characteristics and the bat-contact history of cases is presented in table 1. Five cases occurred following the transmission of the virus to organ transplant recipients from 2 infected donors; 3 of the cases involved recipients in Texas [34]. These 5 cases have been excluded from further analysis. The 56 non transplant-associated cases of bat-variant rabies were distributed across both countries in 27 states and 5 provinces, with no clear geographic clustering (figure 2). Each state or province had 3 cases, with the exception of California (8 cases) and Texas (7 cases). More than 75% of case patients were male (42 patients), and 41% (23 patients) were adolescents or young adults (age, years). By decreasing order of frequency, bat-variant rabies was diagnosed in persons aged years (24%), years (18%), years (18%), CID 2008:46 (1 May) De Serres et al.

3 Figure 1. A, Number of human cases of indigenously acquired rabies in Canada and the United States since 1950, including cases involving organ transplantation, by type of source animal. N/A, not available. B, Number of human cases of indigenously acquired bat rabies in Canada and the United States from 1950 through 2007, excluding organ transplant cases. years (18%),!10 years (11%), years (7%), and years (4%). Of the 56 case patients, 31 (55%) had direct contact with a bat: 22 reported being bitten, and 9 had direct contact (i.e., were touched by a bat) but reported no history of a bite (table 1 and figure 1B). The remaining 24 case patients (43%) did not have recognized direct contact with a bat: 6 found bats in their home (2 while sleeping) and 19 reported no history of bat exposure whatsoever. Of the 12 case patients with a history of a bat in their bedroom (cases 4, 5, 6, 8, 16, 21, 26, 28, 31, 33, 34, and 35), 3 had no direct contact, 5 were bitten, and 4 were awakened by a bat having landed on them. Of the 56 cases not associated with organ transplantation, 36 (64%) occurred from 1990 through Of these 36 cases since 1990, 16 involved no history of direct contact with a bat; 2 (13%) of the 16 case patients would have qualified for RPEP on the basis of exposure criteria expanded in 1995 to include bats that were in the same room as a sleeping person. Among the 6 cases involving pediatric patients!10 years of age (cases 2, 4, 5, 11, 33, and 35), only 2 occurred since 1990 (cases 33 and 35). A bat was found in the room of the first of these 2 case patients (case 33), but family members had examined the child and found no evidence of a bite. After the child s death, the bat that had been buried was recovered and Bat Rabies in the US and Canada CID 2008:46 (1 May) 1331

4 Table 1. Characteristics of the 61 human cases of indigenously acquired bat rabies in the United States and Canada, Case type and number Year US state or Canadian province Age, years Sex Incubation period, days Patient circumstances and/or bat-contact information [reference(s)] Direct contact by bite/scratch ( n p 22 ) Texas 43 F 16 Bitten on the left forearm while observing a moribund bat [15 18] Florida 7 M UK Bitten several times in the upper pectoral region by a bat [15, 19, 20] California 53 F 57 Bitten on a finger by a moribund bat [16, 17, 21] Wisconsin 4 M 22 Bitten on an ear by a bat while asleep [16, 17] Ohio 6 M 20 Bitten on the left thumb by a bat while asleep; received RPEP before onset of disease and survived [16, 17, 22, 23] Saskatchewan 15 M UK A bat flew into his face and bit him while asleep; he then held the bat in his hands [4, 17, 24] New Jersey 64 M 59 Bitten on the lower lip by a bat [16, 17, 22] Kentucky 26 M 22 Bitten on an ear by a bat while asleep [16, 17, 22] Maryland 55 F 25 Bitten on a finger by a bat [16, 17, 22, 25] Nova Scotia 62 M UK Bitten on his left hand while trying to remove a bat from his house [4] Michigan 5 F 170 Parents recalled a possible bat bite [16, 26, 27] Alberta 22 M 90 Scratched or bitten in the face by a bat [28] Texas 22 M 47 Bitten by a bat on the right index finger [16, 27, 29] Arkansas 29 M 43 A friend said a bat landed on the mouth of the patient, who killed it and disposed of it; other friends recalled seeing bites on his thumb and scratches on his chest [16, 26, 27] West Virginia 41 M 94 Friends and relatives said that the patient shot a bat from his front porch and then examined its head, opened its mouth, and touched its teeth [16, 27, 30] Minnesota 47 M 54 A friend said that the patient had been awakened by a bat that landed on his right hand; he killed it and was bitten in the process; investigation of the house revealed traces of bat activities [16, 31] Tennessee 13 M 50 Found a bat and brought it home [16, 32] California 66 M 35 Bitten on his right index finger by a bat [16, 33] Arkansas 20 M UK Bitten by a bat without further information; was the donor of kidneys, iliac artery, and liver in cases 58, 59, 60, and 61 [16, 34 36] Wisconsin 15 F 37 Bitten by a bat without further information; the only case of rabies survival without vaccination [1, 36] Indiana 10 F 107 Bitten by a bat while sleeping; had a small mark on her right arm [16, 37] Alberta 73 M Bitten by a bat and killed it [38] Direct contact with no obvious bite ( n p 9 ) Alabama 24 F UK Frequently retrieved dead or dying bats from her workplace s chimney [9, 16] California 27 M UK 76 bats were living in the building where the patient worked; a family member believed that a bat had landed on and was brushed off the patient s chest [16, 27, 39] California 74 M UK No known exposure; his son said that the patient sometimes captured bats [16, 27, 39] Texas 71 M 61 Awakened by a bat that landed on his shoulder [16, 40] New Jersey 32 M UK Captured 2 bats with a towel in his house; investigation of the house revealed that up to 200 bats had lived in the attic during the summer [16, 40] Georgia 26 M UK Told coworkers that bats from the attic had landed on him while he was sleeping; investigation revealed the presence of a 200-bat colony in the attic [16, 31] Wisconsin 69 M UK Said he was removing bats from his house with bare hands 2 or 3 times a year; he asked coworkers if it was possible to acquire rabies from an insect bite [16, 31] California 49 M Removed a bat from his house [16, 31] 1332

5 Texas 16 M Had direct contact with a bat that flew into his bedroom [16, 41] No direct contact, house exposure ( n p 6 ) Connecticut 13 F 31 A bat was found in her house while she was sleeping in an upstairs bedroom [16, 27, 42] Washington 4 F 16 A bat was found in her bedroom; family members had examined the chil but found no evidence of a bite; the bat was tested for rabies after the patient s death and was positive for rabies [16, 27, 43] Montana 65 M 120 A bat was found in his bedroom [16, 44] Quebec 9 M 25 2 bats were found in a cabin where the patient slept; he reported no bite but 3 days later showed his mother an erythematous 2-cm lesion on his upper left arm [45] California 28 M UK Killed a bat in his house; denied any direct contact with it; investigation of the house revealed the presence of a bat colony in the attic [16, 46] Mississippi 10 M UK People recalled frequently seeing bats around the patient s house; dead bats were found twice inside the house [16, 47] No history of contact ( n p 19 ) Texas UK UK UK Went to Frio Cave in Texas; transmission thought to be by aerosol [16, 17] Texas 41 M UK Went to Frio Cave in Texas; transmission thought to be by aerosol [16, 17] California 54 M 30 Went to Frio Cave in Texas; transmission thought to be by aerosol [16, 17] Idaho 11 M 41 Unknown [16] Oregon 39 M UK Unknown; was the donor of the corneal transplant in case 57 [22] Kentucky 45 M UK Unknown [16] Oklahoma 24 M UK Patient was a caver; he went into a cave for the last time 3 years earlier [16] Pennsylvania 12 M UK No known exposure [16, 27, 48] Georgia 27 F UK No known exposure [16, 27, 49] New York 11 F UK No known exposure [16, 27, 50] Texas 82 M UK No known exposure; no bat found, but the attic could have been accessible from the outside; a cow living on the patient s farm died from an unknown disease 3 months earlier [16, 27, 51] California 44 M UK No known exposure [16, 27, 52] Tennessee 42 F UK No known exposure [9, 16] Kentucky 42 F UK No known exposure [16, 27, 53] Montana 49 M UK No known exposure; sometimes saw bats outside his workplace [16, 27, 53] Washington 64 M UK No known exposure [16, 44] Virginia 29 M UK No known exposure; some co-inmates reported having seen bats outside [16, 54] Iowa 20 M UK No known exposure [16, 55] British Columbia 52 M UK No known exposure; the patient had told relatives that he had been around bats in abandoned cabins in the previous year [56] Organ transplantation ( n p 5 ) Idaho 37 F 30 Recipient of a corneal transplant from case 42 [16, 22] Texas 50 F Recipient of a kidney from case 19 [16, 34] Texas 18 M Recipient of a kidney from case 19 [16, 34] Oklahoma 52 M Recipient of the liver from case 19 [16, 34] Texas 55 F Recipient of a segment of iliac artery from case 19 [34] NOTE. RPEP, rabies postexposure prophylaxis; UK, unknown. 1333

6 Figure 2. Geographic distribution and number of human cases of bat rabies in Canada and the United States from 1950 through 2007, excluding cases involving organ transplantation. Provinces and states with no cases are in white. tested positive for rabies. The second case patient had no known bat bite but showed his mother a 2-cm erythematous lesion on his upper arm 3 days after he slept in a cabin where 2 bats had been found. The lesion was not identified as a bat bite at the time. The remaining 4 pediatric cases occurred before 1990, and all 4 case patients had a history of bat bite. Among the 25 persons with a discrete history of bat exposure, under the assumption that the infection was caused by that recognized exposure, the incubation period varied from 16 days (cases 1 and 33) to days (case 22). The onset of symptoms occurred before 10 weeks in 18 (72%) of the 25 case patients (table 1 and figure 3). The diagnosis of rabies was considered for the first time at autopsy in only 6 (11%) of the cases (cases 11, 15, 18, 29, 34, and 38). Excluding the 5 transplant-associated cases, the overall incidence rate of bat rabies in humans was 3.9 cases per billion person-years, with similar rates in the United States and Canada (3.9 and 4.4 cases per billion person-years, respectively). The incidence of bat-variant rabies cases increased from 2.2 cases per billion person-years in to 6.7 cases per billion person-years in (table 2 and figure 1B). It is likely that a proportion of the 23 cases occurring from 1950 through 1979 with no known source of exposure and an uncharacterized rabies virus were caused by the bat variant. Under the assumption that all cases were caused by bat rabies, the overall incidence would be 5.5 cases per billion person years, with 15.5 cases per billion person-years in , 0.5 cases per billion person-years in , and 4.6 cases per billion personyears in (table 2). From 1990 through 2007, there were 2 case patients for whom the only known exposure was the presence of a bat in the room where they slept. The incidence for this type of exposure was 0.6 cases per billion personyears. During the same period, there were 11 cases (2.0 cases per billion person-years) with no recognized or reported history of contact. DISCUSSION Rabies in humans in the United States and Canada remains dreaded but rare. With the near elimination of human cases caused by canine rabies, bats have become the animal source of the greatest concern. This is in part because of frequent opportunities for interaction through shared urban and rural distribution and because controlling enzootic rabies in nondomesticated animals is more difficult than in domesticated animals, as seen in the successful control of canine rabies achieved through immunization of dogs. Overall since 1950, we found an incidence rate of bat rabies 1334 CID 2008:46 (1 May) De Serres et al.

7 Figure 3. Incubation period of indigenously acquired human cases of bat rabies with a history of a bat bite (black), direct contact with no bite (gray), or the presence of a bat in the house without direct contact (white), excluding cases involving organ transplantation. in humans of 3.9 cases per billion person-years, with similar rates in the United States and Canada. The introduction of anti-nucleocapsid monoclonal antibody detection at the end of the 1970s led to improved species attribution and the identification of the bat variant among persons with unrecognized exposure. This and the increased concern about bat rabies generally make it difficult to comment on temporal trends. Rabies in humans is dramatic in its clinical presentation and is accompanied by cardinal features. Nevertheless, the diagnosis may be missed; in this series, 11% (6) of the cases of bat rabies were diagnosed postmortem, and it is possible that additional cases without an autopsy performed were missed. The extent of this underestimation is impossible to determine but is likely to be higher among those cases without recognized and suspected exposure history. Although rabies is also enzootic among bats in Europe, only 5 human cases of bat rabies have been described there, 2 of which occurred in nonvaccinated professional bat handlers [57]. In Mexico, 2 3 human cases of bat rabies were identified per year since 2000, although the trend as a proportion of all human cases of rabies has been increasing in recent years [58]. For the rest of Latin America, data are fragmentary, but some cases have been reported [59 62]. Among reported case patients, young-adult and adolescent males seem to predominate. They may practice activities that increase their exposure risk or may be less inclined to seek medical attention or prophylaxis should a contact, even a bite, occur. For this group in particular, it would be beneficial to emphasize through public messages the importance of main- Table 2. Incidence rate and number of human cases of bat rabies in the United States and Canada, excluding cases involving organ transplantation, by decade and type of contact. Direct contact Period Population With bite No bite Cases per billion person-years (no. of cases) Bat-variant rabies No direct contact House exposure No history of exposure Total Unknown source and rabies variant ,802,584, (4) 0 (0) 0 (0) 1.7 (3) 3.9 (7) 11.6 (21) 15.5 (28) ,119,911,320 0 (0) 0 (0) 0 (0) 0.5 (1) 0.5 (1) 0 (0) 0.5 (1) ,379,524, (6) 0 (0) 0 (0) 1.3 (3) 3.8 (9) 0.8 (2) 4.6 (11) ,627,534, (2) 0 (0) 0 (0) 0.4 (1) 1.1 (3) 0 (0) 1.1 (3) ,904,437, (3) 1.7 (5) 1.0 (3) 3.1 (9) 6.9 (20) 0 (0) 6.9 (20) ,507,594, (7) 1.6 (4) 1.2 (3) 0.8 (2) 6.4 (16) 0 (0) 6.4 (16) Total 14,341,588, (22) 0.6 (9) 0.4 (6) 1.3 (19) 3.9 (56) 1.6 (23) 5.5 (79) Total Bat Rabies in the US and Canada CID 2008:46 (1 May) 1335

8 taining a safe distance from bats, avoiding the handling of bats, and minimizing opportunities for contact with bats. Primary preventive measures include education and the barring of bats from human dwellings by sealing openings as small as 2 cm and by placing screens on windows. Professional bat-control advice may be necessary where human dwellings are already inhabited with bats. Although effective, secondary prevention through immediate wound washing and RPEP requires that exposure has been both recognized and brought to the attention of public health personnel. Given the frequently cryptic nature of bat contact, this is clearly not always possible. Among the 56 human case patients with bat rabies described in this series, nearly half had no history of direct contact, and one-third had no known or reported bat exposure at all. The recollection of bite incidents can affect the analysis, and these cases were likely caused by an unrecognized bite and salivary contamination, as opposed to aerosol exposure. Since 1999, RPEP recommendations have been broadened in the hopes of preventing additional cases among persons with unrecognized bat contact, including persons who were in the same room as the bat and who might be unaware that a bite or direct contact had occurred (e.g., 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) [10, p. 8]. Only 2 (13%) of the 16 case patients since 1990 who reported no direct contact had possible exposure while sleeping and, thus, would have qualified for RPEP had this been recognized as sufficient exposure. Although the remainder may also have had qualifying contact that was not elicited before illness or death, other types of exposure outside the eligibility criteria for RPEP may have been responsible. The true preventable proportion of cases and the number needed to treat with RPEP to prevent 1 case would be useful information to inform the current guidelines. In that context, evaluation of the frequency of different types of bat contact and the potentially at-risk but undeclared exposures in a representative sample of the population may be worthwhile. Acknowledgments Financial support. Ministère de la santé et des services sociaux du Québec. Potential conflicts of interest. All authors: no conflicts. References 1. Willoughby RE Jr, Tieves KS, Hoffman GM, et al. Survival after treatment of rabies with induction of coma. N Engl J Med 2005; 352: World Health Organization. Rabies Available at: Accessed 18 March Bleck TP, Rupprecht CE. Rabies. In: Richman DD, Whitley RJ, Hayden FG, eds. 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