bat rabies in the united states and canada from 1950 through 2007
TRANSCRIPT
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
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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
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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
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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
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
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oman
unkn
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dise
ase
3m
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sea
rlier
[16,
27,
51]
4919
94C
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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
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ealt
rans
plan
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omca
se42
[16,
22]
5820
04Te
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50F
20–3
0R
ecip
ient
ofa
kidn
eyfr
omca
se19
[16,
34]
5920
04Te
xas
18M
20–3
0R
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ient
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kidn
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omca
se19
[16,
34]
6020
04O
klah
oma
52M
20–3
0R
ecip
ient
ofth
eliv
erfr
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[16,
34]
6120
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20–3
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ient
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ent
ofili
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tery
from
case
19[3
4]
NOTE.
RP
EP,
rabi
espo
stex
posu
repr
ophy
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s;U
K,
unkn
own.
Downloaded from https://academic.oup.com/cid/article-abstract/46/9/1329/327503by gueston 12 April 2018
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
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
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
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