1 3 9
ARTIGO/ARTICLE
Revista da Sociedade Br asileir a de Medicina Tr opical 3 7 ( 2 ) :1 3 9 -1 4 2 , mar-abr, 2 0 0 4
Canine rabies epidemiology in Araçatuba and neighborhood,
Northwestern São Paulo State - Brazil
Epidemiologia da raiva c anina na região de Araç atuba, Noroeste
do Estado de São Paulo - B rasil
Luzia Helena Queir oz da Silva1, César Eduar do Bissoto1, Ádna Cleia B. Delbem1, Clar a Isabel de Lucca Fer r ar i2, Sílvia Helena Ventur oli Per r i1 and Cár is Mar oni Nunes1
ABSTRACT
Ep i d e m i o lo gi c a l c h a ra c te ri sti c s o f c a n i n e ra b i e s i n th e n o rth we st re gi o n o f Sã o Pa u lo Sta te ( Ara ç a tu b a re gi o n ) , Bra zi l, f ro m 1 9 9 3 to 1 9 9 7 a re p re se n te d . Ou t o f 1 ,9 8 4 d o gs, a to ta l o f 3 5 1 ( 1 7 .7 %) we re p o si ti ve f o r ra b i e s d i a gn o si s; 8 9 % ( 3 1 2 / 351) o f the se o c c u rre d in u rb a n a re a s a n d 85% ( 266/312) o f the u rb a n po sitive c a se s we re a m o n g o wn e d do gs. The m e a n a ge o f th e ra b i d d o gs wa s 3 4 m o n th s a n d 6 1 % we re m a le . Aggre ssi ve b e h a vi o r wa s o b se rve d i n 7 7 % o f ra b i d d o gs, f o llo we d b y la c k o f c o o rdina tio n a nd pa ra lysis ( 42%) a nd 48% o f the se do gs we re re spo nsib le b iting pe o ple o r o the r a nim a ls. Info rm a tio n a b o u t va c c i n a ti o n sta tu s wa s o b ta i n e d f ro m 1 8 2 re c o rd s a n d 5 1 % o f ra b i d d o gs we re n o n - va c c i n a te d . Th e n u m b e r o f u n va c c i n a te d ra b i d d o gs i n d i c a te s a lo w va c c i n a ti o n i n d e x a n d th i s f a c to r a d d e d to th e h i gh d o g/m a n ra ti o m u st h a ve c o n tri b u te d to th e c a n i n e ra b i e s e p i zo o ti c o b se rve d i n th e stu d i e d a re a .
Ke y-words: Do gs. Ca n i n e ra b i e s. Epi de m i o lo gy. Sã o Pa u lo Sta te .
RESUMO
Sã o a p re se n ta d a s a lgu m a s c a ra c te rí sti c a s e p i d e m i o ló gi c a s d a ra i va c a n i n a n a re gi ã o d e Ara ç a tu b a , n o p e rí o d o d e 1 9 9 3 a 1 9 9 7 . De n tre 1 .9 8 4 c ã e s su b m e ti d o s a o d i a gn ó sti c o d e ra i va , 3 5 1 f o ra m p o si ti vo s se n d o q u e 8 9 % d o s c a so s ( 3 1 2 /3 5 1 ) o c o rre ra m n a zo n a u rb a n a e de ste s, 85% ( 266/312) e ra m de a n i m a i s c o m pro pri e tá ri o . As i n f o rm a ç õ e s so b re se xo e sta va m p re se n te s e m 8 3 % d a s f i c h a s e d e sta s 6 1 % e ra m d e m a c h o s. A m é d i a d e i d a d e d o s c ã e s p o si ti vo s f o i d e 3 4 m e se s. A a gre ssi vi d a d e f o i u m d o s si n to m a s m a i s c o m u m e n te o b se rva d o ( 7 7 %) , se gu i d o p o r i n c o o rd e n a ç ã o m o to ra e /o u p a ra li si a ( 42%) e 48% do s c ã e s po si ti vo s ha vi a m a gre di do pe sso a s o u o u tro s a n i m a i s. Da s 182 f i c ha s e pi de m i o ló gi c a s q u e po ssu í a m da do s de va c i n a ç ã o , 51% ( 92/182) do s c ã e s n ã o e ra m va c i n a do s. Apo n ta - se c o m o po ssí ve i s ra zõ e s pa ra o a pa re c i m e n to da e p i d e m i a n o m u n i c í p i o d e Ara ç a tu b a a b a i x a c o b e rtu ra va c i n a l d e m o n stra d a p e lo í n d i c e d e c ã e s n ã o va c i n a d o s q u e a dq u i ri ra m a do e n ç a a li a do à e le va da re la ç ã o c ã o /ho m e m ( 1:3,5) re ve la da e m e stu do a n te ri o r.
Palavr as-chave s: Cã e s. Ra i va c a n i n a . Epi de m i o lo gi a . Esta do de Sã o Pa u lo .
1 . Cur so de Me dic ina Ve te r inár ia do De par tame nto de Apo io , Pr o duç ão e Saude Animal da Unive r sidade Estadual de São Paulo , Ar aç atub a, SP. 2 . Lab o r ató r io de Sanidade Animal e Ve ge tal do Instituto B io ló gic o , Ar aç atub a, SP, B r asil.
Addr e ss to: Dr a. Luzia He le na Que ir o z da Silva. R. Cló vis Pe stana 7 9 3 , 1 6 0 5 0 - 6 8 0 Ar aç atub a, SP, B r asil. Te l: 5 5 1 8 3 6 2 0 - 3 2 9 8 , Fax: 5 5 1 8 3 6 2 2 - 6 4 8 7 .
E- mail: lhq silva@ fmva. une sp. b r Re c e b ido par a pub lic aç ão e m 0 1 /0 4 /2 0 0 3 Ac e ito e m 2 2 /1 2 /2 0 0 3
Canine rabies c ontinues to be a major public health problem in mo st par ts o f the wo r ld. Human r ab ies tr ansmitted b y r ab id
do gs c o r r e spo nds to 7 6 . 6 % o f the r e c o r de d c ase s in the
Ame r ic as7 and to 8 3 % o f r e giste r e d c ase s in São Paulo State ,
B razil, from 1 9 8 0 to 1 9 9 41 2. Considering that the estimated dog
po pulatio n in Latin Ame r ic a and the Car ib b e an is ab o ut 4 0 m illio n , wh ic h c o r r e s po n ds to o n e do g fo r e ve r y 8 - 1 3
inhabitants1, dogs play an important role in rabies oc c urrenc e.
During the perio d fro m 1 9 7 0 to 1 9 8 0 , B razil registered an
annual average of 2 ,4 0 0 c ases of c anine rabies6. Rabies c ontrol
me asur e s suc h as mass do g vac c inatio n c ampaigns have b e e n undertaken, resulting in a c onsiderable reduc tion in the number
o f human and do g r ab ie s c ase s ( 7 8 % and 9 0 % de c r e ase in
human and dog rabies c ases, respec tively) during the period of
1 9 8 0 to 1 9 9 0 . Ho wever, at the end o f the dec ade the inc idenc e
has inc r eased again8. Fro m 1 9 9 0 to 1 9 9 9 , B razil registered an
ave r age o f 8 7 0 .3 c ase s o f r ab ie s in do gs1 0.
In the no r thwester n r egio n o f São Paulo State an epidemic
o f c anine r ab ie s initiate d in 1 9 9 1 and disse minate d to the
1 4 0
Silva LHQ e t al
munic ipal distric ts. Dogs represented 8 7 .2 % of the total positive
animal sample s1 0. As a c o nse que nc e o f this c anine e pide mic ,
two human r ab ie s c ase s we r e r e giste r e d in Ar aç atub a and
Avanhandava, in 1 9 9 4 and 1 9 9 7 , respec tively ( Instituto Pasteur/
São Paulo, unpublished data) .
In spite of the fac t that c anine rabies epidemic s have been
reported all over the world, epidemiological descriptions are scarce3,
espec ially in Brazil. This work presents some epidemiologic al
c harac teristic s of the c anine rabies epidemic in the northwestern
region of São Paulo State, Brazil, from 1 9 9 3 to 1 9 9 7 .
MATERIAL AND METHODS
The studied area c omprises 4 2 munic ipal distric ts that sent
at le ast o ne c anine sample fo r e xaminatio n dur ing the study
pe r io d. Po sitive c ase s we r e analyze d fr o m nine munic ipal
distr ic ts o f var ying size , in the no r thwe ste r n São Paulo State ,
where a c anine rabies epidemic has been observed ( Figur e 1 ) .
RESULTS
Table 1 shows the number and percentage of examined samples
and rabies positive dogs during the studied period ac c ording to their origin. A total of 1,984 samples were evaluated and 351 ( 17.7%)
were positive by either fluorescent antibody test or mice inoculation
test. The highest percentage of positivity ( number of positive samples
from the examined samples) was observed in Rubiac ea distric t, where almost all the examined samples tested positive ( 8 8 .9 % ) .
Figure 1 shows these c ases ac c ording to their geographic al
distribution and the percentage in each district. The highest numbers
of positive c ases, from the total detec ted c ases, were observed in the municipal districts of Birigüi ( 4 0 .2 %) and Araçatuba ( 3 7 .9 %) .
Rab ie s diagno sis was pe r fo r me d b y fluo r e sc e nt antib o dy
and mic e ino c ulatio n te sts, ac c o r ding to the Wo r ld He alth
Organization rec ommendations1 3.
Using a data base program ( Dbase 3 Plus® ) , epidemiological
file s fr o m 3 5 1 do gs with po sitive r ab ie s lab o r ato r y diagno sis wer e evaluated in that r egio n, fr o m 1 9 9 3 to 1 9 9 7 . Data o n the
origin, environment, breed, age, sex, rabies vac c ination status,
c linic al signs, aggr e ssio n and o wne r ship c o nditio ns we r e
analyze d. Unfo r tunate ly, no t all the file s c o ntaine d c o mple te info r matio n c o nc e r ning the analyze d data and in mo st o f the
c ase s it was no t po ssib le to o b tain fur the r de tails.
The c hi-squar e te st was use d fo r spe c ifie d pr o po r tio ns1 4.
40.2 37.9
3.7 1.7 2.3
Mirandó po lis Va lpa r a íso
R ub iá c e a ( 2 . 3 )
Gua r a r a pe s
Ar a ç a tub a B ila c ( 7 , 4 ) B ir igui
Coroados ( 3 .9 )
São Paul
o
Glicério ( 0.6)
Fi gu re 1 - Ma p o f Bra zi l sho wi n g Sã o Pa u lo Sta te a n d Ara ç a tu b a re gi o n ( i n de ta i l) , wi th the pe rc e n ta ge o f po si ti ve do gs i n e a c h di stri c t re la te d to the to ta l n u m b e r o f po si ti ve sa m ple s i n the who le Ara ç a tu b a re gi o n .
Ta b le 1 - Nu m b e r a n d p e rc e n ta ge o f e x a m i n e d d o gs a n d ra b i e s
p o si ti ve d i a gn o si s, a c c o rd i n g to th e o ri gi n o f m u n i c i p a l d i stri c t i n Ara ç a tu b a re gi o n f ro m 1 9 9 3 to 1 9 9 7 .
Num b e r o f Num b e r o f
Distric t e xamine d sample s po sitive sample s Po sitivity % Ar a ç a tub a 6 2 3 1 3 3 2 1 . 3 B ir igui 7 1 8 1 4 1 1 9 . 6
B ilac 5 2 2 6 4 6 . 4
Co r o a do s 6 2 1 4 2 2 . 5 Glic é r io 2 7 0 2 7 . 4 Gua r a r a pe s 4 9 1 3 2 6 . 5 Mir a n dó po lis 6 1 0 8 1 3 . 1 Rub iác e a 0 9 0 8 8 8 . 9
Valpar aíso 2 5 0 6 2 4
Oth e r s 3 5 8 0 0
Total 1 9 8 4 3 5 1 1 7 . 7
Figur e 2 pr e se nts the distr ib utio n o f all r e c o r de d po sitive
c ase s ac c o r ding to the q uar te r s o f the ye ar. The r e was a signific ant inc rease ( p < 0 .0 0 1 ) in the frequenc y of c ases during
the fir st and sec o nd quar ter s o f 1 9 9 4 .
0 5 10 15 20 25 30 35 40 45 50
1993 1994 1995 1996 1997
year
num
be
r
o
f
r
a
bi
d
do
g
s
1st quarter 2nd quarter 3rd quarter 4th quarter
Fi gu re 2 - Di stri b u ti o n o f p o si ti ve c a se s a c c o rd i n g to q u a rte rs o f ye a r, f ro m 1 9 9 3 to 1 9 9 7 .
The highe st pr o po r tio n o f do gs, c o r r e spo nding to 8 9 %
( 3 1 1 /3 5 1 ) o r iginate d fr o m ur b an ar e as, whe r e as o nly 1 1 %
( 3 9 /3 5 1 ) we r e fr o m r ur al ar e as. Amo ng the ur b an po sitive
c ases 8 5 % ( 2 6 6 /3 1 1 ) wer e o wned do gs.
A total of 3 2 4 files had information about the breed of the
animals and 2 8 0 c orresponded to mongrel dogs ( 8 6 % ) . Eighty
three percent ( 2 9 2 /3 5 1 ) of the files had information about sex and
1 4 1 Revista da So ciedade Br asileir a de Medicina Tr o pical 3 7 :1 3 9 - 1 4 2 , mar- abr, 2 0 0 4
Table 2 shows information regarding age, which was obtained
fr o m 2 0 8 files ( 5 9 % o f the to tal) . The median age o f the r ab id dogs was 3 4 months and the highest age frequenc y was 2 4 to 4 8
mo nths c o r r e spo nding to 2 6 % ( p < 0 .0 0 1 ) , 1 2 to 2 4 mo nths
and 6 to 1 2 mo nths, b o th with 1 7 .3 % o c c ur r enc e.
DISCUSSION
In the last few years urban rabies control in Brazil and specifically
in the northwestern São Paulo State region was undertaken mostly by mass immunization c ampaigns besides laboratory diagnosis of
suspected rabid animals. In the five years prior to the rabies epidemic,
vaccination coverage in Araçatuba region had reached 8 0 .0 % of the
total estimated dog population ( approximately 1 5 ,0 0 0 dogs) ,
considering a dog-to-person ratio 1 : 8 -1 31, which is usually used as
a basis in many American countries. However, the dog-to-person
ratio observed in this region was 1 :3 .5 indicating that possibly, the
real coverage was below this estimation5. Consequently, urban rabies
outbreaks appeared in many municipal districts of the region,
particularly in Araçatuba contributing to the epidemic progression
towards the East, reaching a total distance of 1 5 2 km1 0.
The inc r e ase in the numb e r o f c ase s o b se r ve d dur ing the
fir st and se c o nd quar te r s o f 1 9 9 4 o c c ur r e d j ust afte r the fir st human r ab ie s c ase r e giste r e d in Januar y 1 9 9 4 in Ar aç atub a.
This might have c ontributed to the inc reased number of samples
sent fo r rabies diagno sis. In additio n, the large number o f free
r o aming do gs and the po o r c aptur e se r vic e allo we d a r apid disseminatio n o f r abies vir us amo ng the do g po pulatio n.
In the urban areas o f these distric ts, where the highest
c onc entration of dogs is rec orded, our results show that most of
the rabid dogs were owned. However, they were c ertainly not
r e str aine d whe n o utdo o r s, whic h is a c o mmo n c usto m in
developing c ountries2.
The highest perc entage o f po sitive male do gs ( 6 1 % ) might
b e due to the fac t that when fr ee r o aming females ar e i n he a t,
fights will be more numerous and the roaming range will expand
a n d a ls o b e c a us e th e y us ua lly de fin e th e ir te r r ito r y a n d
c hallenge any dog whic h does not belong to their group1. Similar
results were desc ribed in Mexic o3 and the United States2 where
authors desc ribed the highest perc entage of positive rabies c ases
o c c urring in males.
Concerning the age distribution of positive dogs, the highest frequenc ies were observed between 6 and 4 8 months, whic h
corresponds to 6 0 .6 % of the cases, probably because of the lack of
vaccination or immune response. Eng et a l3 observed that the highest
frequency of rabid dogs in Mexico was between 6 and 1 2 month of
age when they had a great mass of unvaccinated dogs. In the present study, aggressiveness was observed in 7 7 % of the cases that had
information on clinical signs while the same symptom was observed
in 2 9 .3 % of rabid dogs in United States2. The high percentage of dogs
showing aggressiveness in our study, is related to the high frequency
( 4 7 .6 %) of dogs that had bitten humans or other animals. It should be emphasized that 6 1 .7 % of the aggressors were owned, and only
4 6 % were vaccinated against rabies. These observations reflect the carelessness of the owners, mainly concerning vaccination and
allowing their pets to roam freely on the streets.
Re po r ts o f r ab ie s in vac c inate d do gs e spe c ially amo ng yo unge r animals that have a highe r susc e ptib ility to infe c tio n
and pr o b ab ly do no t have an ade quate se r o c o nve r sio n and
pr o tec tio n3 is quite c o mmo n b ut, in o ur study, this pr o po r tio n
c o r r e spo nde d to 4 9 % , whic h me ans that almo st half o f the
Ta b le 2 - Nu m b e r a n d p e rc e n ta ge o f d o gs w i th p o si ti ve ra b i e s d i a gn o si s, a c c o rd i n g to th e i r a ge i n Ara ç a tu b a re gi o n f ro m 1 9 9 3 to 1 9 9 7 .
Age ( mo nths) Nu m b e r %
< 3 1 0 4 . 8
3 - 6 2 5 1 2 . 0
6 - 1 2 3 6 1 7 . 3
1 2 - 2 4 3 6 1 7 . 3 2 4 - 4 8 5 4 2 6 . 0 4 8 - 7 2 2 0 9 . 6 7 2 - 9 6 1 1 5 . 3 9 6 - 1 2 0 1 0 4 . 8
> 1 2 0 6 2 . 9
Total 2 0 8 1 0 0 . 0
Concerning clinical findings, 2 3 % of the files did not contain any
information. From a total of 2 6 9 animals for which at least one sign
was reported, aggressiveness was the most frequent sign ( 7 7 %)
followed by lameness and limb paralysis ( 4 2 %) , change in voice ( 3 0 %) and jaw paralysis with excessive salivation ( 2 6 %) . Lethargy
was reported in only 1 1 % of the dogs. Most of the files ( 9 7 %) ,
contained information about aggression and in 4 8 % ( 1 6 2 /3 4 0 ) of
the cases, rabid dogs had bitten a human or other animal. Ninety one percent ( 1 4 8 /1 6 2 ) of these aggressors were owned dogs.
Dur ing the analyze d pe r io d, do gs we r e r e spo nsib le fo r
the transmission of rabies to 2 1 herbivores inc luding 1 2 c attle ,
6 horses, 2 pigs and 1 sheep, 1 9 % of whic h ( 4 /2 1 ) c orresponded
to animals kept in ur b an ar eas.
Vac c inatio n status was info r me d in 5 2 % ( 1 8 2 /3 5 1 ) o f the files and 5 1 % ( 9 2 /1 8 2 ) of these dogs, had never been vac c inated
against rabies.
Figur e 3 pr esents the distr ib utio n o f r ab id do gs ac c o r ding
to age and vac c inatio n status. The highest per c entage o f r ab id
vac c inated dogs was 5 0 .0 % and oc c urred between the age of 1 2 and 2 4 mo nths as we ll as in do gs o ve r te n ye ar s o ld.
Fr o m a to tal o f 1 8 2 r e giste r s that had info r matio n ab o ut
va c c ina tio n s ta tus , 5 4 r a b id do gs ( 2 9 . 6 % ) we r e o wne d,
aggressive and unvac c inated against rabies.
0 10 20 30 40 50 60
num
be
r
of
ra
bid
dogs
<3 3 - <6 6 - <12 12 - <24 24 - <48 48 - <72 72 - <96 96 - <120 >120
age (month)
vaccinated total
1 4 2
r ab id do gs had b e e n vac c inate d at le ast o nc e . Rab ie s vac c ine
used fo r B razilian do g vac c inatio n c ampaigns is an inac tivated suc kling mouse brain vac c ine, tested for potenc y by Ministry of
Agr ic ultur e , using Hab e l te st4 with a minimum tite r o f 1 06 .0
LD5 0 /0 .0 3 ml ( 5 0 % Lethal Doses) . Among the vac c inated dogs,
the highest perc entage of rabies oc c urred in those aged between 1 2 and 2 4 months ( 5 0 % ) emphasizing the observations already
made in an earlier study that only after rec eiving three or more
do se s o f vac c ine s in mass c ampaigns, o ve r c o nse c utive ye ar s,
the animals will present adequate and durable rabies antibodies
le ve ls1 1. Sim ila r r e s ults s h o win g th e b e n e fits o f s e ve r a l
vac c inatio ns o n the antib o dy tite r s we r e r e po r te d b y Se ghaie r
e t a l9. To b e tte r disc uss the se data, mo r e info r matio n is nec essary about the time between the last vac c ination and death, the age o f fir st vac c inatio n and the numb e r o f do se s r e c e ive d
during their lifetime, unfo rtunately ho wever, suc h info rmatio n
is no t availab le in lo c al r ec o r ds.
Our findings sho w the ne c e ssity o f inte nsifying c o ntr o l
measures, population health educ ation, spec ially referring to responsible ownership, whic h involves adequate vac c ination and
restric ting pets from street roaming, in addition to daily c are.
We c o nside r that this k ind o f r e po r t is im po r tant fo r
epidemio lo gic al surveys and c an help to mo dify rabies c o ntro l
me asur e s and c o ntr ib ute to a b e tte r unde r standing o f the dynamic s o f ur ban do g po pulatio ns.
ACKNOWLEDGEMENTS
To UNESP Veterinary Hospital Pathology Servic e for nec ropsy
o f do gs. To Cr istiano de Car valho fo r the pr e par atio n o f the
samples and Devani Mariano Pinheiro for c are of the laboratory
mic e . To Dr. Flo r anc e Clique t fr o m AFSSA-Nanc y ( Fr anc e ) fo r the var io us suggestio ns r egar ding this manusc r ipt.
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