Open Access

Molecular epidemiology of livestock rabies viruses isolated in the northeastern Brazilian states of Paraíba and Pernambuco from 2003 - 2009

  • Nobuyuki Mochizuki1,
  • Hiroyuki Kawasaki1,
  • Maria LCR Silva2,
  • José AB Afonso3,
  • Takuya Itou1Email author,
  • Fumio H Ito4 and
  • Takeo Sakai1
BMC Research Notes20125:32

DOI: 10.1186/1756-0500-5-32

Received: 22 July 2011

Accepted: 16 January 2012

Published: 16 January 2012

Abstract

Background

Limited or no epidemiological information has been reported for rabies viruses (RABVs) isolated from livestock in the northeastern Brazilian states of Paraíba (PB) and Pernambuco (PE). The aim of this study was to clarify the molecular epidemiology of RABVs circulating in livestock, especially cattle, in these areas between 2003 and 2009.

Findings

Phylogenetic analysis based on 890 nt of the nucleoprotein (N) gene revealed that the 52 livestock-derived RABV isolates characterized here belonged to a single lineage. These isolates clustered with a vampire bat-related RABV lineage previously identified in other states in Brazil; within PB and PE, this lineage was divided between the previously characterized main lineage and a novel sub-lineage.

Conclusions

The occurrences of livestock rabies in PB and PE originated from vampire bat RABVs, and the causative RABV lineage has been circulating in this area of northeastern Brazil for at least 7 years. This distribution pattern may correlate to that of a vampire bat population isolated by geographic barriers.

Background

Rabies is a fatal infectious disease that causes encephalomyelitis. In Brazil, various rabies viruses (RABVs) have been isolated from numerous animal species, including dogs, foxes, cats, and cattle, as well as from hematophagous, insectivorous, and frugivorous bats. Vampire bats, particularly Desmodus rotundus, are an important rabies vector in Latin America. Transmission from vampire bats to humans has been reported, primarily in the Amazon regions of Brazil and Peru, and a large number of cases of cattle rabies transmitted by vampire bats also have been reported in Brazil [1]. Since the introduction of a regional elimination program, the incidence of human and canine rabies in Latin America has fallen by 90% over the past 20 years. However, northeastern Brazil remains a "hotspot" for human rabies because of circulation of the virus among the dog population [2]. Carnieli Jr. et al. reported the molecular characterization and epidemiology of RABVs isolated from canids in northeastern Brazil [35], and Shoji et al. reported the genetic and phylogenetic characterization of RABVs isolated from wild fox, insectivorous bats, and livestock in Paraíba (PB) [6]. In Olinda, a city in Pernambuco (PE), 7,062 patients underwent prophylactic antirabies treatment between 2002 and 2006 [7]. Molecular and geographic analyses of livestock rabies in central and southeast Brazil revealed that RABVs isolated from livestock were related to the virus found in vampire bat populations, and this epidemiological pattern was maintained over time and space in these areas [811]. However, little or no information on the molecular epidemiology of RABVs has been reported for the virus isolated from livestock in PB and PE. The aim of the present study was to analyse the molecular epidemiology of RABVs circulating among livestock, especially cattle, in these areas between 2003 and 2009.

Results

The sequences of 890 nt PCR products, corresponding to nucleotides 89-978 of the Pasteur vaccine (PV) strain, were determined for all 52 RABV isolates. Among the 52 isolates, the nucleotide and amino acid sequence identities were 97.7-100% and 97.9-100%, respectively.

Phylogenetic analysis based on the sequences of 890 nt of the N gene revealed that the 52 RABV isolates included in this study clustered with a vampire bat-related RABV lineage; these isolates did not cluster with the dog-, fox-, or insectivorous bat-related RABVs (Figure 1). Comparison with RABVs isolated from other states in Brazil indicated that these 52 RABV isolates belonged to a single lineage; furthermore, this lineage was divided between a previously characterized main lineage (B) and a novel sub-lineage (A) consisting of several isolates located in PE. Geographical plotting showed that RABV isolates of the novel sub-lineage were derived from neighbouring areas (Figure 2). The topographical distributions of isolates from lineages A and B could not be distinguished in the areas covered by this study.
https://static-content.springer.com/image/art%3A10.1186%2F1756-0500-5-32/MediaObjects/13104_2011_Article_1353_Fig1_HTML.jpg
Figure 1

A phylogenetic tree based on the nucleotide sequences of the N gene. A phylogenetic tree based on the nucleotide sequences of 890 nt (bases 89-978) of the N gene was constructed using the method devised by Saitou and Nei [12]; the bootstrap probabilities of each node were calculated using 1,000 replicates. The designations BRbv, BRsp, BRgt, BRhr, BR-Pfx, and BR-DR indicate samples from Brazilian cattle, sheep, goats, horses, foxes, and vampire bats, respectively. MOKV and ABLV denote the Mokola virus and Australian bat lyssavirus, respectively. State abbreviations are as follows: PB, Paraíba; PE, Pernambuco; GO, Goiás; SP, São Paulo; RJ, Rio de Janeiro; MT, Mato Grosso; TO, Tocantins; MA, Maranhão; PA, Pará; MS, Mato Grosso do Sul. The triangle and star symbols represent the new sub-lineage (group A) and the previously reported lineage (group B), respectively.

https://static-content.springer.com/image/art%3A10.1186%2F1756-0500-5-32/MediaObjects/13104_2011_Article_1353_Fig2_HTML.jpg
Figure 2

Geographic distribution of rabies virus isolates in the Brazilian states of Paraíba and Pernambuco. (a) Map of Brazil indicating location of states pertinent to this study. State abbreviations are as follows: PB, Paraíba; PE Pernambuco; GO, Goiás; SP, São Paulo; RJ, Rio de Janeiro; MT, Mato Grosso; TO, Tocantins; MA, Maranhão; PA, Pará; MS, Mato Grosso do Sul. (b, c) Detailed geographic distribution of livestock isolates classified as genetic variants in the states of PB (b) and PE (c). The two symbols (triangle and star) correspond to the new sub-lineage and previously reported lineage, respectively, as used in Figure 1. Samples for which the geographic origin and the genetic variant are identical are illustrated using the same symbol. Brazilian maps were obtained from Brasil em Relevo - Embrapa Monitoramento por Satélite http://www.relevobr.cnpm.embrapa.br/.

Discussion

Segments of the N gene from the 52 RABV isolates, collected from PB and PE between 2003 and 2009, were sequenced and phylogenetically analysed. This N gene segment displayed greater than 97.7% nucleotide and amino acid sequence identity among these 52 RABVs. This correlation implies that the lineage has been maintained during transmission in PB and PE.

The phylogenetic analysis described here indicates that all of the livestock RABVs in PB and PE were derived from vampire bat rabies. Furthermore, the present study reveals that there are two RABV lineages that are separate from other regional Brazilian vampire bat-related RABV lineages. The first, sub-lineage A, consists of BRbv1173 (collected in PB in 2004) and another seven RABV isolates collected in PE in 2008-2009; the second, sub-lineage B, consists of isolates collected in PB in 2003-2009 and in PE in 2007-2009. Comparison among RABV isolates from multiple northern states of Brazil revealed that lineages from PB and PE were distinct from those obtained from the Maranhão (MA) state. Because of geographical barriers (mountains and rivers) between PB/PE and MA, it would be difficult for vampire bats (the prime vector for RABV) to move freely between PB/PE and MA. Geographical mapping (Figure 2) demonstrates that sub-lineage A was located mainly in high-altitude areas of PE, while sub-lineage B was widely distributed and present in both PE and PB. Thus, these two lineages seem to correlate with geographic factors and/or vampire bat populations, but do not appear to correlate with the year of isolation. Using a 203 nt segment (bases 109 to 311) of the N gene, Kobayashi et al. [8, 9] reported the existence of at least 24 RABV genetic variants among vampire bat-transmitted cases of rabies in cattle in Brazil; the distribution of several of these RABV genetic variants was found to be delimited by geographic boundaries, including mountain ranges and rivers. Our analysis (data not shown) using the same 203 nt segment reveals that the 52 RABV isolates (from PB and PE) of the present study correlate with the same PB lineage described by Kobayashi et al. These results indicate that livestock rabies has been transmitted by vampire bats in PB and PE during this study period. Furthermore, this RABV lineage seems to have been circulating in this area for at least 7 years, with transmission affected by geographic factors and resulting in dispersion of vampire bats among regional populations.

Previous reports have shown human exposure to vampire bat-transmitted rabies in northeastern Brazil, including PE [1, 7]. The present phylogenetic analysis suggests that rabies epidemics that occurred in cattle in PB and PE were transmitted by vampire bats. These RABV isolates comprised a lineage independent from that of other Brazilian isolates, with the distinction reflecting isolation from neighbouring regions by geographic factors. Thus, the vampire bat-derived rabies in this area represents an endemic disease, suggesting that the regional control of vampire bat rabies in this area may be a workable model for local elimination of human and livestock rabies.

Conclusions

The present study indicates that occurrences of livestock rabies in PB and PE were caused by vampire bat RABVs, and that this RABV lineage has been circulating in this area of northeastern Brazil for at least 7 years. This pattern of distribution may correlate to that of a vampire bat population isolated by geographic barriers.

Methods

The 52 RABV isolates used in this study were obtained from cattle (46), sheep (3), goats (2), and horse (1), and were collected in PB and PE between 2003 and 2009 (Table 1). Brain specimens from these livestock were diagnosed as RABV-positive by an immunofluorescent antibody test and a mouse inoculation test. These study procedures were implemented in accordance with the Institutional Guidelines for Animal Experiments at the Campina Grande University under the permission (number 129/2009) of the Committee for Experimental Animals of this College. Viral RNA was extracted from the brains of livestock using the QIAamp Viral RNA Mini Kit (Qiagen, Hilden, Germany). Nucleoprotein (N) gene sequences from the Brazilian RABV isolates were amplified using RT-PCR with primers JW12 (5'-ATGTAACACCYCTACAATG-3') (position: 55-73 of PV) and N8 (5'-AGTTTCTTCAGCCATCTC-3') (position: 1585-1568 of PV), followed by hemi-nested PCR with primer pairs as follows. Primer pair A consisted of JW12 and P2 (5'-CCCATATAACATCCAACAAAGTG-3') (position: 1029-1007 of PV), and generated a 975-nt amplicon. Primer pair B consisted of P1 (5'-CTACAATGGATGCCGACAAGA-3') (position: 66-86 of PV) and N8, and generated a 1,520 nt amplicon. The nucleotide sequences of RABVs from Brazilian foxes, livestock, and hematophagous and insectivorous bats were obtained from GenBank (Table 1). Cycle sequencing, nucleotide and amino acid sequence alignments, and phylogenetic analyses were performed as previously described [13, 14]. The geographic origins of the RABV isolates sequenced from the Brazilian livestock were plotted at the municipal level of the respective federal states using MapInfo Professional GIS software (ver. 8.0, MapInfo Japan K.K., Tokyo, Japan). Brazilian maps were obtained from Brasil em Relevo - Embrapa Monitoramento por Satélite [15].
Table 1

Brazilian rabies virus isolates used in this study

Sample*1

Species

Location

State*2

Year

Lineage of PB and PE*3

Accession No.

Reference

BR-DR6

Desmodus rotundus

Laje de Muriae

RJ

1998

 

AB297633

[16]

BR-DR7

Desmodus rotundus

Itaperuna

RJ

1997

 

AB297634

[16]

BR-M1(BR-Pbt1)

Molossus sp.

Patos

PB

  

AB206414

[6]

BR-M2(BR-Pbt2)

Molossus sp.

Patos

PB

  

AB206415

[6]

BR-M3(BR-Pbt3)

Molossus sp.

Patos

PB

  

AB206416

[6]

BR-M4(BR-Pbt4)

Molossus sp.

Patos

PB

  

AB206417

[6]

BR-Pfx1

Fox

Patos

PB

2002

 

AB362483

[13]

BR-Pfx3

Fox

Patos

PB

2001

 

AB206409

[6]

BR-Pfx5

Fox

Patos

PB

2002

 

AB206411

[6]

BR-Pfx6

Fox

Patos

PB

2002

 

AB207884

[6]

BRbv30

Cattle

Morrinhos

GO

1999

 

AB083803

[17]

BRbv32

Cattle

Sao Roque

SP

1994

 

AB083805

[17]

BRbv36

Cattle

Nova Olinda

TO

1998

 

AB083809

[17]

BRbv39

Cattle

Colinas

TO

1999

 

AB083811

[17]

BRbv43

Cattle

Alto Taquari

MT

1999

 

AB083813

[17]

BRbv49

Cattle

Piraju

SP

1989

 

AB083817

[17]

BRbv50

Cattle

Corumbaiba

GO

1999

 

AB083818

[17]

BRbv55

Cattle

Montes Altos

MA

1998

 

AB675602*4

[8]

BRbv56

Cattle

Iporá

GO

1998

 

AB675603*4

[8]

BRbv76

Cattle

Xinguará

PA

2002

 

AB675604*4

[8]

BRbv80

Cattle

Ipameri

GO

2001

 

AB675605*4

[8]

BRbv103

Cattle

Nova Crixás

GO

2001

 

AB675606*4

[8]

BRbv133

Cattle

Xambioa

TO

2000

 

AB675607*4

[8]

BRbv140

Cattle

Natividade

TO

2000

 

AB675608*4

[8]

BRbv141

Cattle

Nova Crixas

GO

2000

 

AB675609*4

[8]

BRbv183

Cattle

Natividade

TO

2001

 

AB675610*4

[8]

BRbv190

Cattle

Pocone

MT

2002

 

AB675611*4

[9]

BRbv192

Cattle

Nobres

MT

2002

 

AB675612*4

[8]

BRbv215

Cattle

Rosario Oeste

MT

2002

 

AB675613*4

[9]

BRbv251(BR-Pbv1)

Cattle

Patos

PB

2003

PB/PE-B

AB206423

[6]

BRbv252(BR-Pbv2)

Cattle

Patos

PB

2003

PB/PE-B

AB206424

[6]

BRbv254(BR-Pbv3)

Cattle

Patos

PB

2003

PB/PE-B

AB206425

[6]

BRbv255(BR-Pbv5)

Cattle

Patos

PB

2003

PB/PE-B

AB206426

[6]

BRbv257(BR-Pbv7)

Cattle

Patos

PB

2003

PB/PE-B

AB206427

[6]

BRbv258(BR-Pbv8)

Cattle

Patos

PB

2003

PB/PE-B

AB206428

[6]

BRbv260(BR-Pbv10)

Cattle

Patos

PB

2003

PB/PE-B

AB206429

[6]

BRbv261(BR-Pbv11)

Cattle

Patos

PB

2003

PB/PE-B

AB206430

[6]

BRbv262(BR-Pbv12)

Cattle

Patos

PB

2003

PB/PE-B

AB206431

[6]

BRbv279

Cattle

Pirapozinho

SP

2002

 

AB675614*4

[9]

BRbv312

Cattle

Paulo de Frontin

RJ

1987

 

AB675615

This study

BRbv316

Cattle

Miguel Pereina

RJ

2000

 

AB675616*4

[9]

BRbv324

Cattle

Itapecuru Mirim

MA

2004

 

AB675617*4

[9]

BRbv340

Cattle

Nossa Senhora do Livramento

MT

2004

 

AB675618*4

[9]

BRbv382

Cattle

Orizona

GO

2002

 

AB675619*4

[9]

BRbv384

Cattle

Nova América

GO

2002

 

AB675620*4

[9]

BRbv403

Cattle

Piranhas

GO

2002

 

AB675621*4

[9]

BRbv581

Cattle

Tambaú

SP

2003

 

AB675622*4

[9]

BRbv617

Cattle

Rio Claro

RJ

2004

 

AB675623*4

[9]

BRbv645

Cattle

Capinzal do Norte

MA

2004

 

AB675624*4

[9]

BRbv668

Cattle

Santo Antônio dos Lopes

MA

2005

 

AB675625*4

[9]

BRbv670

Cattle

Godofredo Viana

MA

2005

 

AB675626*4

[9]

BRbv792

Cattle

Morrinhos

GO

2002

 

AB675627*4

[9]

BRbv804

Cattle

Pilar de Goiás

GO

2005

 

AB675628*4

[9]

BRbv827

Cattle

Cocalzinho de Goiás

GO

2005

 

AB675629*4

[9]

BRbv844

Cattle

Itapaci

GO

2006

 

AB675630*4

[9]

BRbv934

Cattle

Bandeirantes

MS

2005

 

AB675631*4

[9]

BRbv1169

Cattle

Patos

PB

2004

PB/PE-B

AB623080

This study

BRbv1170

Cattle

Santa Terezinha

PB

2004

PB/PE-B

AB623081

This study

BRbv1172

Cattle

São José do Bonfim

PB

2004

PB/PE-B

AB623082

This study

BRbv1173

Cattle

Itaporanga

PB

2004

PB/PE-A

AB623083

This study

BRbv1174

Cattle

São Vicente do Seridó

PB

2004

PB/PE-B

AB623084

This study

BRbv1176

Cattle

Patos

PB

2005

PB/PE-B

AB623085

This study

BRbv1177

Cattle

Santa Luzia

PB

2005

PB/PE-B

AB623086

This study

BRbv1179

Cattle

Areal

PB

2006

PB/PE-B

AB623087

This study

BRbv1181

Cattle

Monteiro

PB

2006

PB/PE-B

AB623089

This study

BRbv1182

Cattle

Junco do Seridó

PB

2006

PB/PE-B

AB623090

This study

BRbv1183

Cattle

São José do Sabugi

PB

2006

PB/PE-B

AB623091

This study

BRbv1184

Cattle

Santa Luzia

PB

2006

PB/PE-B

AB623092

This study

BRbv1186

Cattle

Patos

PB

2007

PB/PE-B

AB623093

This study

BRbv1187

Cattle

Patos

PB

2007

PB/PE-B

AB623094

This study

BRbv1190

Cattle

Areal

PB

2007

PB/PE-B

AB623096

This study

BRbv1193

Cattle

Patos

PB

2007

PB/PE-B

AB623097

This study

BRbv1194

Cattle

São José do Bonfim

PB

2007

PB/PE-B

AB623098

This study

BRbv1197

Cattle

São José do Bonfim

PB

2007

PB/PE-B

AB623099

This study

BRbv1198

Cattle

Brejinho

PE

2007

PB/PE-B

AB623106

This study

BRbv1199

Cattle

Patos

PB

2008

PB/PE-B

AB623100

This study

BRbv1200

Cattle

Patos

PB

2008

PB/PE-B

AB623101

This study

BRbv1201

Cattle

Patos

PB

2008

PB/PE-B

AB623102

This study

BRbv1204

Cattle

Patos

PB

2008

PB/PE-B

AB623103

This study

BRbv1206

Cattle

Patos

PB

2008

PB/PE-B

AB623104

This study

BRbv1207

Cattle

Patos

PB

2009

PB/PE-B

AB623105

This study

BRbv1209

Cattle

Vitória de Santo Antão

PE

2008

PB/PE-B

AB623107

This study

BRbv1210

Cattle

Venturosa

PE

2008

PB/PE-A

AB623108

This study

BRbv1211

Cattle

Pedra

PE

2008

PB/PE-A

AB623109

This study

BRbv1212

Cattle

Venturosa

PE

2008

PB/PE-A

AB623110

This study

BRbv1213

Cattle

Garanhuns

PE

2008

PB/PE-A

AB623111

This study

BRbv1214

Cattle

Venturosa

PE

2008

PB/PE-A

AB623112

This study

BRbv1215

Cattle

Paranatama

PE

2008

PB/PE-B

AB623113

This study

BRbv1216

Cattle

Venturosa

PE

2008

PB/PE-A

AB623114

This study

BRbv1217

Cattle

Belo Jardim

PE

2008

PB/PE-B

AB623115

This study

BRbv1218

Cattle

Belo Jardim

PE

2009

PB/PE-B

AB623116

This study

BRbv1219

Cattle

Lajedo

PE

2009

PB/PE-B

AB623117

This study

BRbv1220

Cattle

Garanhuns

PE

2009

PB/PE-A

AB623118

This study

BRgt249(BR-Pgt1)

Goat

Patos

PB

2003

PB/PE-B

AB206437

[6]

BRgt1205

Goat

São Mamede

PB

2008

PB/PE-B

AB623077

This study

BRhr31

Horse

Ipora

GO

1998

 

AB083804

[17]

BRhr1196

Horse

Patos

PB

2007

PB/PE-B

AB623076

This study

BRsp250(BR-Psp1)

Sheep

Patos

PB

2003

PB/PE-B

AB206438

[6]

BRsp1171

Sheep

Santa Terezinha

PB

2004

PB/PE-B

AB623078

This study

BRsp1203

Sheep

Patos

PB

2008

PB/PE-B

AB623079

This study

*1 Names in parentheses are designations from Shoji et al. (2006)

*2 State abbreviations are as follows: PB Paraíba, PE Pernambuco, GO Goiás, SP São Paulo, RJ Rio de Janeiro, MT Mato Grosso, TO Tocantins, MA Maranhão, PA Pará, MS Mato Grosso do Sul

*3 Lineages are based on the phylogenetic tree of Figure 1

*4 We determined extra sequences in this study

Declarations

Acknowledgements

This work was supported in part by a Grant-in-Aid for the Academic Frontier Project for Private Universities from the Ministry of Education, Culture, Sports, Science, and Technology of Japan.

Authors’ Affiliations

(1)
Nihon University Veterinary Research Center, Nihon University
(2)
Academic Unit of Veterinary Medicine, Center of Health and Rural Technology, Federal University of Campina Grande
(3)
Bovine Clinic, Federal Rural University of Pernambuco, Campus of Garanhuns
(4)
Department of Preventive Veterinary Medicine and Animal health, Faculty of Veterinary Medicine and Zootechny, University of São Paulo

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© Mochizuki et al; licensee BioMed Central Ltd. 2012

This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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