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b r a z j i n f e c t d i s . 2 0 1 3;1 7(2):251–253

The Brazilian Journal of

INFECTIOUS DISEASESwww .e lsev i er .com/ locate /b j id

rief communication

abies in humans and non-human in the state of Pará,razilian Amazon

arcus Emanuel Barroncas Fernandesa, Lanna Jamile Corrêa da Costaa,∗,ernanda Atanaena Goncalves de Andradeb, Lucila Pereira Silvac

Instituto de Estudos Costeiros, Universidade Federal do Pará, Braganca, PA, BrazilInstituto Federal de Educacão, Ciência e Tecnologia, Tucuruí, PA, BrazilLaboratório de Raiva, Laboratório Nacional Agropecuário no Pará/LANAGRO, Belém, PA, Brazil

r t i c l e i n f o

rticle history:

eceived 24 August 2012

ccepted 7 October 2012

vailable online 9 March 2013

eywords:

razilian Amazon

umans and non-humans

a b s t r a c t

We evaluate the relationship of positive cases of rabies with the continuing expansion of

livestock production, and analyse the trends of this zoonosis in human population in the

state of Pará, Brazilian Amazon. The distribution of rabies cases was recorded between 1999

and 2004. Of 148 cases of rabies, 21% were in humans and 79% in non-human mammals.

The rapid growth in livestock numbers seems to be associated with the increase of positive

cases in bovine livestock transmitted by vampire bats. This idea is supported by positive and

significant relationship of both events in time (p < 0.01), but failed when spatial distribution

among regions of the state was considered. However, rabies cases tend to occur toward the

yssavirus

abies

northeastern of the state of Pará, where rabies cases are proportionally five times greater

than other mesoregions, suggesting that increased livestock production may influence the

increase of this zoonosis.

© 2013 Elsevier Editora Ltda. All rights reserved.

newborn mice. Positive samples were identified using mono-

abies, caused by Lyssavirus, is a disease found in humans andeveral other mammal species.1,2 Up until the mid-1990s, thetate of Pará, eastern portion of the Amazon, had the thirdighest rate of rabies cases in Brazil. According to the Brazilianealth Ministry only nine cases of rabies in humans (trans-itted by vampire bats) were recorded in Pará between 1999

nd 2002, all in the southeastern portion of the state. By con-rast, from 2003 to 2004, the number of recorded cases morehan doubled to 22, and was more widespread, ranging from

he southeast to the northeast. Therefore, the present studyas conducted primarily to assess whether positive human

nd non-human (cattle) cases of rabies were associated with

∗ Corresponding author at: Instituto de Estudos Costeiros, Universidade/n, Aldeia, Braganca, PA 68600-000, Brazil.

E-mail address: lannacorrea@yahoo.com (L.J.C. da Costa).413-8670/$ – see front matter © 2013 Elsevier Editora Ltda. All rights rttp://dx.doi.org/10.1016/j.bjid.2012.10.015

the ongoing expansion of the bovine livestock production inthe region, and to evaluate current trends in human rabiesincidence in this part of the Brazilian Amazon.

All positive human samples (n = 31) resulted from infec-tions that occurred in rural areas. The non-human group wasrepresented by cattle (n = 117). Rabies was diagnosed usingdirect immunofluorescence assays and viral isolation throughthe intracranial inoculation of the central nervous system of

Federal do Pará, Campus de Braganca, Alameda Leandro Ribeiro

clonal antibodies.The distribution of the rabies cases (human and non-

human) was recorded in the different mesoregions of

eserved.

252 b r a z j i n f e c t d i s . 2 0 1 3;1 7(2):251–253

Mesoregions1 = Lower amazon

2 = Marajó

3 = Belém

4 = Northeast

5 = Southwest

6 = Southeast

KeyHuman

Non human

1999 - 20000 50 100 200 300 400

Km

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31 2

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2001 - 2002 2003 - 2004

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’S 54º0’0’’W 51º0’0’’W 48º0’0’’W 57º0’0’’W 54º0’0’’W 51º0’0’’W 48º0’0’’W 57º0’0’’W 54º0’0’’W 51º0’0’’W 48º0’0’’W

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Fig. 1 – Positive human and non-human cases in intervals of two years, from 1999 to 2004, in the six mesoregions of the

cant correlations of human cases neither with the increase ofrabies cases in cattle (regression, F = 0.44; df = 5; p = 0.54) nor

40

35

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itive

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ine

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tock

20

15

10

58 10 12 14 16

Bovine livestock (x106)

18

y=3.461x - 22.71R2=0,86

F=25.88; p<0.01

state of Pará, eastern Brazilian Amazon.

Pará between 1999 and 2004 (Fig. 1). Annual variationand different geographic regions were both evaluated withrespect to the number of rabies cases in human andnon-human by using Kruskal–Wallis’s non-parametric anal-ysis of variance (H), while linear regression (with datatransformed) was applied to describe the relationshipbetween the rabies cases (human and non-human) and live-stock production, considering annual and mesoregion varia-tions.

Between 1999 and 2004, 148 cases of rabies were recordedin Pará, of which, 31 (21%) were in humans, the remain-ing 117 (79%) in non-human mammals (cattle). The numberof non-human cases varied significantly among the six geo-graphic regions of the state (H = 9.94; df = 5; p < 0.01), withthe majority of cases being recorded in the southeast (n = 62;42%). On the other hand, no significant differences werefound in the annual variation for non-human cases (H = 2.12;df = 5; p > 0.05), although most cases have been reported in2003 and 2004. Regarding human cases there was no signif-icant differences for both annual variation and geographicregions (H = 9.8; df = 5; p = 0.07 and H = 3.05; df = 5; p = 0.69,respectively), with half of cases recorded in the Marajómesoregion.

The production of bovine livestock in the Brazilian Ama-zon basin has increased progressively since 1991. Accordingto the Pará State Department of Agriculture (SAGRI), the localbovine herd increased annually by an average of 12% dur-ing the present study period (1999–2004) totaling 73,181,447individuals, reaching the peak in 2004 (24%). Similarly, thenumbers of rabies cases in cattle have noticeably grown in

the same year (n = 62). Thus, it seems reasonable to assumethat this rapid growth in livestock numbers, mainly in 2004,may be associated with the increase in the figures of posi-tive cases of rabies in bovine livestock transmitted by vampire

bats, Desmodus rotundus. In fact, the regression analysisbetween these two events showed a positive and signifi-cant relationship in time (regression, F = 25.8; df = 5; p < 0.01– Fig. 2) supporting this hypothesis, but failed when spa-tial distribution among regions of the state was considered(regression, F = 5.63; df = 5; p = 0.07). However, it is importantto emphasize that the southeast mesoregion has a livestockten times higher than the Northeast, where the number ofrabies cases is proportionally five times greater than that ofsoutheast.

As a consequence of the increase of positive cases in cattle,one would expect a higher number of rabies cases in humansin rural areas. However, regression analysis revealed signifi-

Fig. 2 – Relationship between positive rabies cases onbovine livestock and total bovine livestock from 1999 to2004 in the state of Pará, Brazilian Amazon.

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ith the increase of total bovine livestock (regression, F = 4.44;f = 5; p = 0.10).

Rabies outbreaks in the state of Pará have occurred in ruralreas, where the majority of the human population lives inelative poverty. Most victims reported in 2004, for example,ived in thatched houses, with no electricity or other utilities,nd not close of water bodies. In most cases, information wasvailable only for the confirmed cases by governmental enti-ies and not for all clinical cases, i.e., the figures of positivendividuals were underestimated, which is a barrier to moreccurately define the trends of this disease in the Amazonegion.

Once humans dwell in the focus area of bat-transmittedabies, structural changes triggered by non-biological or socialactors make the disease emerge.3 In fact, the rabies virus

ay be spreading rapidly over wide areas within the Amazonasin and beyond, especially through intraspecies transmis-ion among bat populations,4 despite the low occurrence ofhis type of transmission.5

The association between vampire and other bats, andild bat rabies is well documented at many South Ameri-

an sites,4,6 but the lack of field surveys and monitoring ofat populations hinder the understanding of the spreadingrocess and transmission routes within the Amazon basin.dditionally, the activities of surveillance and disease controllso depend on information about the size of forested areas,opography, hydrography and land use by man,5,7 being suchactors straightly related to the livestock industry.

onflict of interest

ll authors declare to have no conflict of interest.

7

3;1 7(2):251–253 253

Acknowledgements

We thank the laboratory personnel of the Secretaria Executivade Saúde Pública do Pará (SESPA) – Núcleo de Epidemiolo-gia (NUEP), Instituto Evandro Chagas (IEC) – Departamentode Raiva, and the Agência de Defesa Agropecuária do Pará(ADEPARÁ) in the state of Pará, Brazil, who have acquired andcontributed these data over many years. We are grateful toMaura E.M. Sousa for her assistance with the figures.

e f e r e n c e s

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Chile. J Wildl Dis. 2000;36:231–40.

. Gomes MN, Monteiro AMV, Lewis N, et al. Landscape riskfactors for attacks of vampire bats on cattle in São Paulo,Brazil. Prev Vet Med. 2010;93:139–46.