Bat Rabies in the United States and Canada from 1950 through 2007

9
Bat Rabies in the US and Canada CID 2008:46 (1 May) 1329 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 Fre ´de ´ ric Dallaire, 2 Mathieu Co ˆ te, 2 and Danuta M. Skowronski 3 1 Institut national de sante ´ publique du Que ´bec and 2 Universite ´ 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 2007. 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 10–29 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 1950–1989 to 6.7 per billion person-years in 1990–2007. 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 qualifie 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 char- acterizes each of the major terrestrial animal hosts. Hu- mans 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 esti- mates 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 2008. Reprints or correspondence: Dr. Gaston De Serres, Institut national de sante ´ publique du Que ´bec, 2400 d’Estimauville, Quebec, PQ, Canada, G1E 7G9 ([email protected]). Clinical Infectious Diseases 2008; 46:1329–37 2008 by the Infectious Diseases Society of America. All rights reserved. 1058-4838/2008/4609-0001$15.00 DOI: 10.1086/586745 (RPEP) that consists of a single dose of immunoglob- ulin 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 firs 90 days after exposure [3, 4]. Three principal global areas of rabies have been de- fine [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 (West- ern Europe, Canada, and the United States); and (3) rabies-free countries (mostly islands, including En- gland, 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 firs identificatio Downloaded from https://academic.oup.com/cid/article-abstract/46/9/1329/327503 by guest on 12 April 2018

Transcript of Bat Rabies in the United States and Canada from 1950 through 2007

Page 1: Bat Rabies in the United States and Canada from 1950 through 2007

Bat Rabies in the US and Canada • CID 2008:46 (1 May) • 1329

M A J O R A R T I C L E

Bat Rabies in the United States and Canadafrom 1950 through 2007: Human CasesWith and Without Bat Contact

Gaston De Serres,1 Frederic Dallaire,2 Mathieu Cote,2 and Danuta M. Skowronski3

1Institut national de sante publique du Quebec and 2Universite Laval, Quebec, and 3British 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 almostexclusively caused by the bat-variant virus.

Methods. We reviewed indigenously acquired cases of bat-variant rabies in humans in Canada and the UnitedStates from 1950 through 2007.

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 reportedno 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 10–29 years of age. The median incubation period was 7 weeks (!10 weeks in 72% of cases). The incidenceof bat-variant rabies cases increased from 2.2 per billion person-years in 1950–1989 to 6.7 per billion person-yearsin 1990–2007. 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 qualifie for rabies postexposure prophylaxis on the basis of exposure criteriaexpanded in 1995 to include bats that were in the same room as a sleeping person. The incidence of rabies forthis 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 postexposureprophylaxis 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 char-

acterizes each of the major terrestrial animal hosts. Hu-

mans 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 esti-

mates 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 published21 March 2008.

Reprints or correspondence: Dr. Gaston De Serres, Institut national de santepublique du Quebec, 2400 d’Estimauville, Quebec, PQ, Canada, G1E 7G9([email protected]).

Clinical Infectious Diseases 2008; 46:1329–37� 2008 by the Infectious Diseases Society of America. All rights reserved.1058-4838/2008/4609-0001$15.00DOI: 10.1086/586745

(RPEP) that consists of a single dose of immunoglob-

ulin 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 firs 90 days after exposure

[3, 4].

Three principal global areas of rabies have been de-

fine [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 (West-

ern Europe, Canada, and the United States); and (3)

rabies-free countries (mostly islands, including En-

gland, 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 firs identificatio

Downloaded from https://academic.oup.com/cid/article-abstract/46/9/1329/327503by gueston 12 April 2018

Page 2: Bat Rabies in the United States and Canada from 1950 through 2007

1330 • CID 2008:46 (1 May) • De Serres et al.

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 pat-

terns, 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 an-

tibody in the late 1970s and the more-recent nucleotide se-

quencing 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 un-

known or unrecognized [3, 5]. Transmission of bat-variant ra-

bies 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 fl in daylight. Those active during the day are

suspect, as are any found on the ground. The behavior dem-

onstrated by rabid bats is not always dramatically altered [4].

Although some may become aggressive, others may simply be-

come disoriented, lose their flyin 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-in-

flicte scratch marks are !1 cm long. Such minor evidence of

contact may be difficul 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 thresh-

old for RPEP administration. In 1995, the Centers for Disease

Control and Prevention (CDC) urged “consideration of post-

exposure prophylaxis for persons potentially exposed to bats

even where a history of physical contact cannot be elicited” [9,

p. 272]. This is reflecte 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 pub-

lished previously. This report summarizes all cases of bat-var-

iant rabies identifie in humans in the United States and Can-

ada 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 ac-

quired 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 2007. 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 reflect the control of canine-variant

rabies (figu e 1A). Even recently, however, year-to-year varia-

tion 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 1979. Since 1980 and

the advent of anti-nucleocapsid monoclonal antibody detection

and nucleotide sequencing, distinct species-associated variants

were identifie in all reported human cases of rabies.

Since 1950, 61 human cases of bat-variant rabies were re-

ported 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 trans-

mission of the virus to organ transplant recipients from 2 in-

fected 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 prov-

inces, with no clear geographic clustering (figu e 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, 10–29 years). By decreasing order of fre-

quency, bat-variant rabies was diagnosed in persons aged 20–

29 years (24%), 10–19 years (18%), 40–49 years (18%), �60

Downloaded from https://academic.oup.com/cid/article-abstract/46/9/1329/327503by gueston 12 April 2018

Page 3: Bat Rabies in the United States and Canada from 1950 through 2007

Bat Rabies in the US and Canada • CID 2008:46 (1 May) • 1331

Figure 1. A, Number of human cases of indigenously acquired rabies in Canada and the United States since 1950, including cases involving organtransplantation, by type of source animal. N/A, not available. B, Number of human cases of indigenously acquired bat rabies in Canada and the UnitedStates from 1950 through 2007, excluding organ transplant cases.

years (18%) , !10 years (11%), 50–59 years (7%), and 30–39

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 figu e 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%) oc-

curred from 1990 through 2007. 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 qualifie 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 firs of

these 2 case patients (case 33), but family members had ex-

amined the child and found no evidence of a bite. After the

child’s death, the bat that had been buried was recovered and

Downloaded from https://academic.oup.com/cid/article-abstract/46/9/1329/327503by gueston 12 April 2018

Page 4: Bat Rabies in the United States and Canada from 1950 through 2007

1332

Tabl

e1.

Char

acte

rist

ics

ofth

e61

hum

anca

ses

ofin

dige

nous

lyac

quir

edba

tra

bies

inth

eU

nite

dSt

ates

and

Cana

da,1

950–

2007

.

Cas

ety

pean

dnu

mbe

rYe

ar

US

stat

eor

Can

adia

npr

ovin

ceA

ge,

year

sS

ex

Incu

batio

npe

riod,

days

Pat

ient

circ

umst

ance

san

d/or

bat-

cont

act

info

rmat

ion

[ref

eren

ce(s

)]

Dire

ctco

ntac

tby

bite

/scr

atch

()

np

22

119

51Te

xas

43F

16B

itten

onth

ele

ftfo

rear

mw

hile

obse

rvin

ga

mor

ibun

dba

t[1

5–18

]

219

53Fl

orid

a7

MU

KB

itten

seve

ralt

imes

inth

eup

per

pect

oral

regi

onby

aba

t[1

5,19

,20

]

319

58C

alifo

rnia

53F

57B

itten

ona

finge

rby

am

orib

und

bat

[16,

17,

21]

419

59W

isco

nsin

4M

22B

itten

onan

ear

bya

bat

whi

leas

leep

[16,

17]

519

70O

hio

6M

20B

itten

onth

ele

ftth

umb

bya

bat

whi

leas

leep

;rec

eive

dR

PE

Pbe

fore

onse

tof

dise

ase

and

surv

ived

[16,

17,

22,

23]

619

70S

aska

tche

wan

15M

UK

Aba

tfle

win

tohi

sfa

cean

dbi

thi

mw

hile

asle

ep;h

eth

enhe

ldth

eba

tin

his

hand

s[4

,17

,24

]

719

71N

ewJe

rsey

64M

59B

itten

onth

elo

wer

lipby

aba

t[1

6,17

,22

]

819

73K

entu

cky

26M

22B

itten

onan

ear

bya

bat

whi

leas

leep

[16,

17,

22]

919

76M

aryl

and

55F

25B

itten

ona

finge

rby

aba

t[1

6,17

,22

,25

]

1019

77N

ova

Sco

tia62

MU

KB

itten

onhi

sle

ftha

ndw

hile

tryi

ngto

rem

ove

aba

tfr

omhi

sho

use

[4]

1119

83M

ichi

gan

5F

∼170

Par

ents

reca

lled

apo

ssib

leba

tbi

te[1

6,26

,27

]

1219

85A

lber

ta22

M∼9

0S

crat

ched

orbi

tten

inth

efa

ceby

aba

t[2

8]

1319

90Te

xas

22M

47B

itten

bya

bat

onth

erig

htin

dex

finge

r[1

6,27

,29

]

1419

91A

rkan

sas

29M

∼43

Afr

iend

said

aba

tla

nded

onth

em

outh

ofth

epa

tient

,who

kille

dit

and

disp

osed

ofit;

othe

rfr

iend

sre

calle

dse

eing

bite

son

his

thum

ban

dsc

ratc

hes

onhi

sch

est

[16,

26,

27]

1519

94W

est

Virg

inia

41M

∼94

Frie

nds

and

rela

tives

said

that

the

patie

ntsh

ota

bat

from

his

fron

tpo

rch

and

then

exam

ined

itshe

ad,

open

edits

mou

th,a

ndto

uche

dits

teet

h[1

6,27

,30

]

1620

00M

inne

sota

47M

∼54

Afr

iend

said

that

the

patie

ntha

dbe

enaw

aken

edby

aba

tth

atla

nded

onhi

srig

htha

nd;h

eki

lled

itan

dw

asbi

tten

inth

epr

oces

s;in

vest

igat

ion

ofth

eho

use

reve

aled

trac

esof

bat

activ

ities

[16,

31]

1720

02Te

nnes

see

13M

∼50

Foun

da

bat

and

brou

ght

itho

me

[16,

32]

1820

03C

alifo

rnia

66M

∼35

Bitt

enon

his

right

inde

xfin

ger

bya

bat

[16,

33]

1920

04A

rkan

sas

20M

UK

Bitt

enby

aba

tw

ithou

tfu

rthe

rin

form

atio

n;w

asth

edo

nor

ofki

dney

s,ili

acar

tery

,an

dliv

erin

case

s58

,59

,60

,an

d61

[16,

34–

36]

2020

04W

isco

nsin

15F

37B

itten

bya

bat

with

out

furt

her

info

rmat

ion;

the

only

case

ofra

bies

surv

ival

with

out

vacc

inat

ion

[1,

36]

2120

06In

dian

a10

F∼1

07B

itten

bya

bat

whi

lesl

eepi

ng;h

ada

smal

lmar

kon

her

right

arm

[16,

37]

2220

07A

lber

ta73

M18

0–27

0B

itten

bya

bat

and

kille

dit

[38]

Dire

ctco

ntac

tw

ithno

obvi

ous

bite

()

np

9

2319

94A

laba

ma

24F

UK

Freq

uent

lyre

trie

ved

dead

ordy

ing

bats

from

her

wor

kpla

ce’s

chim

ney

[9,

16]

2419

95C

alifo

rnia

27M

UK

76ba

tsw

ere

livin

gin

the

build

ing

whe

reth

epa

tient

wor

ked;

afa

mily

mem

ber

belie

ved

that

aba

tha

dla

nded

onan

dw

asbr

ushe

dof

fth

epa

tient

’sch

est

[16,

27,

39]

2519

95C

alifo

rnia

74M

UK

No

know

nex

posu

re;h

isso

nsa

idth

atth

epa

tient

som

etim

esca

ptur

edba

ts[1

6,27

,39

]

2619

97Te

xas

71M

∼61

Aw

aken

edby

aba

tth

atla

nded

onhi

ssh

ould

er[1

6,40

]

2719

97N

ewJe

rsey

32M

UK

Cap

ture

d2

bats

with

ato

wel

inhi

sho

use;

inve

stig

atio

nof

the

hous

ere

veal

edth

atup

to20

0ba

tsha

dliv

edin

the

attic

durin

gth

esu

mm

er[1

6,40

]

2820

00G

eorg

ia26

MU

KTo

ldco

wor

kers

that

bats

from

the

attic

had

land

edon

him

whi

lehe

was

slee

ping

;inv

estig

atio

nre

-ve

aled

the

pres

ence

ofa

200-

bat

colo

nyin

the

attic

[16,

31]

2920

00W

isco

nsin

69M

UK

Sai

dhe

was

rem

ovin

gba

tsfr

omhi

sho

use

with

bare

hand

s2

or3

times

aye

ar;

heas

ked

cow

orke

rsif

itw

aspo

ssib

leto

acqu

irera

bies

from

anin

sect

bite

[16,

31]

3020

00C

alifo

rnia

49M

60–9

0R

emov

eda

bat

from

his

hous

e[1

6,31

]

Downloaded from https://academic.oup.com/cid/article-abstract/46/9/1329/327503by gueston 12 April 2018

Page 5: Bat Rabies in the United States and Canada from 1950 through 2007

1333

3120

06Te

xas

16M

28–4

2H

addi

rect

cont

act

with

aba

tth

atfle

win

tohi

sbe

droo

m[1

6,41

]

No

dire

ctco

ntac

t,ho

use

expo

sure

()

np

6

3219

95C

onne

ctic

ut13

F∼3

1A

bat

was

foun

din

her

hous

ew

hile

she

was

slee

ping

inan

upst

airs

bedr

oom

[16,

27,

42]

3319

95W

ashi

ngto

n4

F16

Aba

tw

asfo

und

inhe

rbe

droo

m;f

amily

mem

bers

had

exam

ined

the

chil

but

foun

dno

evid

ence

ofa

bite

;th

eba

tw

aste

sted

for

rabi

esaf

ter

the

patie

nt’s

deat

han

dw

aspo

sitiv

efo

rra

bies

[16,

27,

43]

3419

97M

onta

na65

M∼1

20A

bat

was

foun

din

his

bedr

oom

[16,

44]

3520

00Q

uebe

c9

M∼2

52

bats

wer

efo

und

ina

cabi

nw

here

the

patie

ntsl

ept;

here

port

edno

bite

but

3da

ysla

ter

show

edhi

sm

othe

ran

eryt

hem

atou

s2-

cmle

sion

onhi

sup

per

left

arm

[45]

3620

02C

alifo

rnia

28M

UK

Kill

eda

bat

inhi

sho

use;

deni

edan

ydi

rect

cont

act

with

it;in

vest

igat

ion

ofth

eho

use

reve

aled

the

pres

ence

ofa

bat

colo

nyin

the

attic

[16,

46]

3720

05M

issi

ssip

pi10

MU

KP

eopl

ere

calle

dfr

eque

ntly

seei

ngba

tsar

ound

the

patie

nt’s

hous

e;de

adba

tsw

ere

foun

dtw

ice

insi

deth

eho

use

[16,

47]

No

hist

ory

ofco

ntac

t(

)n

p19

3819

55Te

xas

UK

UK

UK

Wen

tto

Frio

Cav

ein

Texa

s;tr

ansm

issi

onth

ough

tto

beby

aero

sol[

16,1

7]

3919

56Te

xas

41M

UK

Wen

tto

Frio

Cav

ein

Texa

s;tr

ansm

issi

onth

ough

tto

beby

aero

sol[

16,1

7]

4019

59C

alifo

rnia

54M

∼30

Wen

tto

Frio

Cav

ein

Texa

s;tr

ansm

issi

onth

ough

tto

beby

aero

sol[

16,1

7]

4119

62Id

aho

11M

41U

nkno

wn

[16]

4219

78O

rego

n39

MU

KU

nkno

wn;

was

the

dono

rof

the

corn

ealt

rans

plan

tin

case

57[2

2]

4319

79K

entu

cky

45M

UK

Unk

now

n[1

6]

4419

79O

klah

oma

24M

UK

Pat

ient

was

aca

ver;

hew

ent

into

aca

vefo

rth

ela

sttim

e3

year

sea

rlier

[16]

4519

84P

enns

ylva

nia

12M

UK

No

know

nex

posu

re[1

6,27

,48

]

4619

91G

eorg

ia27

FU

KN

okn

own

expo

sure

[16,

27,

49]

4719

93N

ewYo

rk11

FU

KN

okn

own

expo

sure

[16,

27,

50]

4819

93Te

xas

82M

UK

No

know

nex

posu

re;n

oba

tfo

und,

but

the

attic

coul

dha

vebe

enac

cess

ible

from

the

outs

ide;

aco

wliv

ing

onth

epa

tient

’sfa

rmdi

edfr

oman

unkn

own

dise

ase

3m

onth

sea

rlier

[16,

27,

51]

4919

94C

alifo

rnia

44M

UK

No

know

nex

posu

re[1

6,27

,52

]

5019

94Te

nnes

see

42F

UK

No

know

nex

posu

re[9

,16

]

5119

96K

entu

cky

42F

UK

No

know

nex

posu

re[1

6,27

,53

]

5219

96M

onta

na49

MU

KN

okn

own

expo

sure

;som

etim

essa

wba

tsou

tsid

ehi

sw

orkp

lace

[16,

27,

53]

5319

97W

ashi

ngto

n64

MU

KN

okn

own

expo

sure

[16,

44]

5419

98Vi

rgin

ia29

MU

KN

okn

own

expo

sure

;som

eco

-inm

ates

repo

rted

havi

ngse

enba

tsou

tsid

e[1

6,54

]

5520

02Io

wa

20M

UK

No

know

nex

posu

re[1

6,55

]

5620

03B

ritis

hC

olum

bia

52M

UK

No

know

nex

posu

re;t

hepa

tient

had

told

rela

tives

that

heha

dbe

enar

ound

bats

inab

ando

ned

cabi

nsin

the

prev

ious

year

[56]

Org

antr

ansp

lant

atio

n(

)n

p5

5719

78Id

aho

37F

30R

ecip

ient

ofa

corn

ealt

rans

plan

tfr

omca

se42

[16,

22]

5820

04Te

xas

50F

20–3

0R

ecip

ient

ofa

kidn

eyfr

omca

se19

[16,

34]

5920

04Te

xas

18M

20–3

0R

ecip

ient

ofa

kidn

eyfr

omca

se19

[16,

34]

6020

04O

klah

oma

52M

20–3

0R

ecip

ient

ofth

eliv

erfr

omca

se19

[16,

34]

6120

04Te

xas

55F

20–3

0R

ecip

ient

ofa

segm

ent

ofili

acar

tery

from

case

19[3

4]

NOTE.

RP

EP,

rabi

espo

stex

posu

repr

ophy

laxi

s;U

K,

unkn

own.

Downloaded from https://academic.oup.com/cid/article-abstract/46/9/1329/327503by gueston 12 April 2018

Page 6: Bat Rabies in the United States and Canada from 1950 through 2007

1334 • CID 2008:46 (1 May) • De Serres et al.

Figure 2. Geographic distribution and number of human cases of bat rabies in Canada and the United States from 1950 through 2007, excludingcases 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 identifie 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 180–270 days (case 22). The onset of symp-

toms occurred before 10 weeks in 18 (72%) of the 25 case

patients (table 1 and figu e 3). The diagnosis of rabies was

considered for the firs 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 in-

cidence 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 1950–1989 to 6.7 cases per billion

person-years in 1990–2007 (table 2 and figu e 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 as-

sumption 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 1950–1959, 0.5 cases per billion

person-years in 1960–1969, and 4.6 cases per billion person-

years in 1970–1979 (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 inci-

dence for this type of exposure was 0.6 cases per billion person-

years. 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 non-

domesticated animals is more difficul 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

Downloaded from https://academic.oup.com/cid/article-abstract/46/9/1329/327503by gueston 12 April 2018

Page 7: Bat Rabies in the United States and Canada from 1950 through 2007

Bat Rabies in the US and Canada • CID 2008:46 (1 May) • 1335

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.

Table 2. Incidence rate and number of human cases of bat rabies in the United States and Canada, excluding cases involvingorgan transplantation, by decade and type of contact.

Cases per billion person-years (no. of cases)

Bat-variant rabies

Direct contact No direct contact

Period Population With bite No biteHouse

exposureNo history

of exposure TotalUnknown source and

rabies variant Total

1950–1959 1,802,584,987 2.2 (4) 0 (0) 0 (0) 1.7 (3) 3.9 (7) 11.6 (21) 15.5 (28)1960–1969 2,119,911,320 0 (0) 0 (0) 0 (0) 0.5 (1) 0.5 (1) 0 (0) 0.5 (1)1970–1979 2,379,524,923 2.5 (6) 0 (0) 0 (0) 1.3 (3) 3.8 (9) 0.8 (2) 4.6 (11)1980–1989 2,627,534,011 0.8 (2) 0 (0) 0 (0) 0.4 (1) 1.1 (3) 0 (0) 1.1 (3)1990–1999 2,904,437,968 1.0 (3) 1.7 (5) 1.0 (3) 3.1 (9) 6.9 (20) 0 (0) 6.9 (20)2000–2007 2,507,594,847 2.8 (7) 1.6 (4) 1.2 (3) 0.8 (2) 6.4 (16) 0 (0) 6.4 (16)Total 14,341,588,056 1.5 (22) 0.6 (9) 0.4 (6) 1.3 (19) 3.9 (56) 1.6 (23) 5.5 (79)

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 identi-

ficatio of the bat variant among persons with unrecognized

exposure. This and the increased concern about bat rabies gen-

erally make it difficul to comment on temporal trends. Rabies

in humans is dramatic in its clinical presentation and is ac-

companied 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 sus-

pected 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 profes-

sional bat handlers [57]. In Mexico, 2–3 human cases of bat

rabies were identifie 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 beneficia to

emphasize through public messages the importance of main-

Downloaded from https://academic.oup.com/cid/article-abstract/46/9/1329/327503by gueston 12 April 2018

Page 8: Bat Rabies in the United States and Canada from 1950 through 2007

1336 • CID 2008:46 (1 May) • De Serres et al.

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 fin a bat in

the room or an adult witnesses a bat in the room with a pre-

viously unattended child, mentally disabled person, or intox-

icated person)” [10, p. 8]. Only 2 (13%) of the 16 case patients

since 1990 who reported no direct contact had possible ex-

posure while sleeping and, thus, would have qualifie for RPEP

had this been recognized as sufficien 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 infor-

mation to inform the current guidelines. In that context, eval-

uation of the frequency of different types of bat contact and

the potentially at-risk but undeclared exposures in a represen-

tative sample of the population may be worthwhile.

Acknowledgments

Financial support. Ministere de la sante et des services sociaux duQuebec.

Potential conflict of interest. All authors: no conflicts

References

1. Willoughby RE Jr, Tieves KS, Hoffman GM, et al. Survival after treat-ment of rabies with induction of coma. N Engl J Med 2005; 352:2508–14.

2. World Health Organization. Rabies. 2006. Available at: http://www.who.int/mediacentre/factsheets/fs099/en/. Accessed 18 March2008.

3. Bleck TP, Rupprecht CE. Rabies. In: Richman DD, Whitley RJ, HaydenFG, eds. Clinical virology. New York: Churchill Livingstone, 1997:879–97.

4. Brass DA. Rabies in bats—natural history and public health implica-tions. Ridgefield CT: Livia Press, 1994.

5. Messenger SL, Smith JS, Rupprecht CE. Emerging epidemiology of bat-associated cryptic cases of rabies in humans in the United States. ClinInfect Dis 2002; 35:738–47.

6. Webster WA, Casey GA, Charlton KM. Rabies in a squirrel. Can VetJ 1988; 29:1015.

7. Smith JS, Seidel HD. Rabies: a new look at an old disease. Prog MedVirol 1993; 40:82–106.

8. Smith JS. New aspects of rabies with emphasis on epidemiology, di-agnosis, and prevention of the disease in the United States. Clin Mi-crobiol Rev 1996; 9:166–76.

9. Centers for Disease Control and Prevention. Human rabies—Alabama,Tennessee, and Texas, 1994. MMWR Morb Mortal Wkly Rep 1995;44:269–72.

10. Centers for Disease Control and Prevention. Human rabies preven-tion—United States, 1999: recommendations of the Advisory Com-mittee on Immunization Practices (ACIP). MMWR Recomm Rep1999; 48(RR-1):1–21.

11. National Advisory Committee on Immunization, Public Health Agencyof Canada. Canadian immunization guide. 7th ed. Ottawa, Canada:Public Works and Government Services, 2006:285–97.

12. 2006 Population estimates. Vol. 2007. US Census Bureau, PopulationEstimates Program, 2007.

13. Historical national population estimates. Vol. 2007. US Census Bureau,Population Estimates Program, 2000.

14. Estimated population of Canada, 1605 to present. Vol. 2007. StatisticsCanada, 2007.

15. Enright JB. Bats, and their relation to rabies. Annu Rev Microbiol1956; 10:369–92.

16. Zoonosis Control Branch. Rabies in humans in USA 1950–present.Austin, TX: Texas Department of State Health Services, 2007.

17. Constantine DG. House bat management. Jamestown, ND: NorthernPrairie Wildlife Research Center, 2006.

18. Sulkin SE, Greve MJ. Human rabies caused by bat bite. Tex State JMed 1954; 50:620–1.

19. Venters HD, Hoffert WR, Schatterday JE, Hardy AV. Rabies in bats inFlorida. Am J Pub Health 1954; 44:182–5.

20. Scatterday JE. Bat rabies in Florida. J Am Vet Med Assoc 1954; 124:125.

21. Humphrey GL, Kemp GE, Wood EG. A fatal case of rabies in a womanbitten by an insectivorous bat. Public Health Rep 1960; 75:317–26.

22. Anderson LJ, Nicholson KG, Tauxe RV, Winkler WG. Human rabiesin the United States, 1960 to 1979: epidemiology, diagnosis, and pre-vention. Ann Intern Med 1984; 100:728–35.

23. Hattwick MA, Weis TT, Stechschulte CJ, Baer GM, Gregg MB. Recoveryfrom rabies: a case report. Ann Intern Med 1972; 76:931–42.

24. Dempster G, Grodumas EI, Bayatpour M, Zbitnew A. A human caseof unsuspected rabies in Saskatchewan diagnosed by virus isolation.Can J Public Health 1972; 63:215–8.

25. Centers for Disease Control and Prevention. Human rabies—Mary-land. MMWR Morb Mortal Wkly Rep 1976; 25:235–6.

26. Centers for Disease Control and Prevention. Human rabies—Michigan.MMWR Morb Mortal Wkly Rep 1983; 32:159–60.

27. Noah DL, Drenzek CL, Smith JS, et al. Epidemiology of human rabiesin the United States, 1980 to 1996. Ann Intern Med 1998; 128:922–30.

28. Rabies in Canada in 1985. Can Med Assoc J 1987; 136:1277–80.29. Centers for Disease Control and Prevention. Human rabies—Texas,

1990. MMWR Morb Mortal Wkly Rep 1991; 40:132–3.30. Centers for Disease Control and Prevention. Human rabies—West Vir-

ginia, 1994. MMWR Morb Mortal Wkly Rep 1995; 44:86–7.31. Centers for Disease Control and Prevention. Human rabies—Califor-

nia, Georgia, Minnesota, New York, and Wisconsin, 2000. MMWRMorb Mortal Wkly Rep 2000; 49:1111–5.

32. Centers for Disease Control and Prevention. Human rabies—Tennes-see, 2002. MMWR Morb Mortal Wkly Rep 2002; 51:828–9.

Downloaded from https://academic.oup.com/cid/article-abstract/46/9/1329/327503by gueston 12 April 2018

Page 9: Bat Rabies in the United States and Canada from 1950 through 2007

Bat Rabies in the US and Canada • CID 2008:46 (1 May) • 1337

33. Centers for Disease Control and Prevention. Human death associatedwith bat rabies—California, 2003. MMWR Morb Mortal Wkly Rep2004; 53:33–5.

34. Srinivasan A, Burton EC, Kuehnert MJ, et al. Transmission of rabiesvirus from an organ donor to four transplant recipients. N Engl J Med2005; 352:1103–11.

35. Centers for Disease Control and Prevention. Investigation of rabiesinfections in organ donor and transplant recipients—Alabama, Ar-kansas, Oklahoma, and Texas, 2004. MMWR Morb Mortal Wkly Rep2004; 53:586–9.

36. Centers for Disease Control and Prevention. Update: investigation ofrabies infections in organ donor and transplant recipients—Alabama,Arkansas, Oklahoma, and Texas, 2004. MMWR Morb Mortal WklyRep 2004; 53:615–6.

37. Centers for Disease Control and Prevention. Human rabies—Indianaand California, 2006. MMWR Morb Mortal Wkly Rep 2007; 56:361–5.

38. Centers for Disease Control and Prevention. Human rabies—Alberta,Canada, 2007. MMWR Morb Mortal Wkly Rep 2008; 57:197–200.

39. Centers for Disease Control and Prevention. Human rabies—Califor-nia, 1995. MMWR Morb Mortal Wkly Rep 1996; 45:353–6.

40. Centers for Disease Control and Prevention. Human rabies—Texas andNew Jersey, 1997. MMWR Morb Mortal Wkly Rep 1998; 47:1–5.

41. Centers for Disease Control and Prevention. Confirmatio of humanrabies infection in Texas. Atlanta, GA: Centers for Disease Control andPrevention, 2006.

42. Centers for Disease Control and Prevention. Human rabies—Con-necticut, 1995. MMWR Morb Mortal Wkly Rep 1996; 45:207–9.

43. Centers for Disease Control and Prevention. Human rabies—Wash-ington, 1995. MMWR Morb Mortal Wkly Rep 1995; 44:625–7.

44. Centers for Disease Control and Prevention. Human rabies—Montanaand Washington, 1997. MMWR Morb Mortal Wkly Rep 1997; 46:770–4.

45. Turgeon N, Tucci M, Deshaies D, et al. Human rabies in Montreal,Quebec—October, 2000. Can Commun Dis Rep 2000; 26:209–10.

46. Centers for Disease Control and Prevention. Human rabies—Califor-nia, 2002. MMWR Morb Mortal Wkly Rep 2002; 51:686–8.

47. Centers for Disease Control and Prevention. Human rabies—Missis-sippi, 2005. MMWR Morb Mortal Wkly Rep 2006; 55:207–8.

48. Centers for Disease Control and Prevention. Human rabies—Penn-sylvania. MMWR Morb Mortal Wkly Rep 1984; 33:633–5.

49. Centers for Disease Control and Prevention. Human rabies—Texas,Arkansas, and Georgia, 1991. MMWR Morb Mortal Wkly Rep 1991;40:765–9.

50. Centers for Disease Control and Prevention. Human rabies—NewYork, 1993. MMWR Morb Mortal Wkly Rep 1993; 42:799–80.

51. Centers for Disease Control and Prevention. Human rabies—Texas andCalifornia, 1993. MMWR Morb Mortal Wkly Rep 1994; 43:93–6.

52. Centers for Disease Control and Prevention. Human rabies—Califor-nia, 1994. MMWR Morb Mortal Wkly Rep 1994; 43:455–8.

53. Centers for Disease Control and Prevention. Human rabies—Kentuckyand Montana 1996. MMWR Morb Mortal Wkly Rep 1997; 46:397–400.

54. Centers for Disease Control and Prevention. Human rabies—Virginia,1998. MMWR Morb Mortal Wkly Rep 1999; 48:95–7.

55. Centers for Disease Control and Prevention. Human rabies—Iowa,2002. MMWR Morb Mortal Wkly Rep 2003; 52:47–8.

56. Parker R, McKay D, Hawes C, et al. Human rabies, British Columbia—January 2003. Can Commun Dis Rep 2003; 29:137–8.

57. Bourhy H, Dacheux L, Strady C, Mailles A. Rabies in Europe in 2005.Euro Surveill 2005; 10:213–6.

58. Nadin-Davis SA, Loza-Rubio E. The molecular epidemiology of rabiesassociated with chiropteran hosts in Mexico. Virus Res 2006; 117:215–26.

59. Nadin-Davis SA, Torres G, de los Angeles Ribas M, et al. A molecularepidemiological study of rabies in Cuba. Epidemiol Infect 2006; 134:1313–24.

60. Badilla X, Perez-Herra V, Quiros L, et al. Human rabies: a reemergingdisease in Costa Rica? Emerg Infect Dis 2003; 9:721–3.

61. da Rosa ES, Kotait I, Barbosa TF, et al. Bat-transmitted human rabiesoutbreaks, Brazilian Amazon. Emerg Infect Dis 2006; 12:1197–202.

62. Goncalves MA, Sa-Neto RJ, Brazil TK. Outbreak of aggressions andtransmission of rabies in human beings by vampire bats in northeasternBrazil. Rev Soc Bras Med Trop 2002; 35:461–4.

Downloaded from https://academic.oup.com/cid/article-abstract/46/9/1329/327503by gueston 12 April 2018