Animal infections by vaccinia-like viruses in the state of ... · 1 Received on December 6, ......

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Pesq. Vet. Bras. 29(7):509-514, julho 2009

RESUMO.- [Infecções animais por vírus semelhantesao vaccínia no estado do Rio de Janeiro: uma doençaem expansão.] Neste estudo avaliou-se a presença deinfecções por vírus semelhantes ao vírus vaccínia (VACV)em gado leiteiro em 12 municípios no estado do Rio deJaneiro, ao longo dos últimos nove anos. Amostras clíni-cas foram coletadas de animais com vesículas, pústulase crostas no úbere e tetas, e da região do nariz e da cavi-dade oral de bezerros. Um teste de neutralização viral

1 Received on December 6, 2008.Accepted for publication on February 2l, 2009.

2 Laboratório de Morfologia e Morfogênese Viral, Instituto OswaldoCruz, Fiocruz, Avenida Brasil 4365, Rio de Janeiro, RJ 21040-900, Brazil.*Corresponding author: [email protected]

3 Secretaria de Agricultura, Pecuária, Pesca e Abastecimento/SEEPA,Alameda São Boaventura 770, Fonseca, Niterói, RJ 24120-191, Brazil.

4 Laboratório de Biologia e Parasitologia de Mamíferos SilvestresReservatórios, Instituto Oswaldo Cruz, Rio de Janeiro, RJ, Brazil.

Animal infections by vaccinia-like viruses in the state ofRio de Janeiro: An expanding disease1

Hermann G. Schatzmayr2*, Bruno R. Simonetti2, Danielle C. Abreu2, José P.Simonetti2, Sandra R. Simonetti2, Renata V.C. Costa3, Márcia Cristina R.

Gonçalves2, Paulo Sérgio D'Andréa4, Marconny Gerhardt4, Manuel E. VieiraSilva2, José C. Farias-Filho2 and Ortrud M. Barth2

ABSTRACT.- Schatzmayr H.G., Simonetti B.R., Abreu D.C., Simonetti J.P., SimonettiS.R., Costa R.V.V., Gonçalves M.C.R., D'Andréa P.S., Gerhardt M.., Silva M.E.V., Farias-Filho J.C. & Barth O.M. 2009. Animal infections by vaccinia-like virus in the state ofRio de Janeiro: An expanding disease. Pesquisa Veterinária Brasileira 29(7):509-514.Laboratório de Morfologia e Morfogênese Viral, Instituto Oswaldo Cruz, Fiocruz, AvenidaBrasil 4365, Rio de Janeiro, RJ 21040-900, Brazil. E-mail: [email protected]

In the present study we investigated the presence of infections by vaccinia-like virusesin dairy cattle from 12 counties in the state of Rio de Janeiro in the last 9 years. Clinicalspecimens were collected from adult animals with vesicular/pustular lesions mainly in theudder and teats, and from calves with lesions around the nose and mouth. A plaque reductionneutralization test (PRNT) was applied to search for antibodies to Orthopoxvirus; thevesicular/pustular fluids and scabs were examined by PCR, electron microscopy (EM) andby inoculation in VERO cells for virus isolation. Antibodies to Orthopoxvirus were detectedin most cases. The PCR test indicated a high nucleotide homology among the isolates andthe vaccinia viruses (VACV) used as controls. By EM, typical orthopoxvirus particles wereobserved in some specimens. The agents isolated in tissue culture were confirmed asvaccinia-like viruses by EM and PCR. The HA gene of the vaccinia-like Cantagalo/IOCvirus isolated in our laboratory was sequenced and compared with other vaccinia-likeisolates, showing high homology with the original Cantagalo strain, both strains isolated in1999 from dairy cattle. Antibodies to Orthopoxvirus were detected in one wild rodent (genusAkodon sp.) collected in the northwestern region of the state, indicating the circulation ofpoxvirus in this area. Nonetheless, PCR applied to tissue samples collected from the wildrodents were negative. Vesicular/pustular lesions in people in close contact with animalshave been also recorded. Thus, the vaccinia-like virus infections in cattle and humans inthe state seem to be an expanding condition, resulting in economic losses to dairy herdsand leading to transient incapacitating human disease. Therefore, a possible immunizationof the dairy cattle in the state should be carefully evaluated.

INDEX TERMS: Orthopoxvirus infections, PCR, neutralization test, electron microscopy, state ofRio de Janeiro.


Hermann G. Schatzmayr et al.510

Fig.1. Counties in the state of Rio de Janeiro where animalinfections have been confirmed by laboratory tests.

por redução de placas foi desenvolvido para investigar apresença de anticorpos contra Orthopoxvirus. Os fluidosde vesículas / pústulas e as crostas foram testadas porPCR, microscopia eletrônica (ME) e por inoculação emcélulas VERO para isolamento viral. Anticorpos contraOrthopoxvirus foram detectados na grande maioria dosanimais. O teste de PCR demonstrou homologia entre osvírus isolados e amostras de vírus vaccínia usados comocontroles. Na ME, partículas típicas de Orthopoxvirus fo-ram observadas em vários espécimes analisados. Os ví-rus isolados em cultivo celular foram confirmados comoOrthopoxvirus por PCR e ME. O gene HA da amostraCantagalo/IOC isolada em nosso laboratório foi seqüen-ciado e comparado com outras amostras semelhantes aovaccínia, mostrando uma alta homologia com a amostraoriginal Cantagalo, tendo sido as duas amostras isoladasem 1999 de gado leiteiro. Anticorpos para Orthopoxvirusforam detectados em um roedor silvestre do gêneroAkodon sp. coletado na região noroeste do estado, suge-rindo uma circulação de poxvírus na natureza. No entan-to, os testes de PCR aplicados a tecidos de roedores sil-vestres foram negativos. Infecções vesiculares / pustularesem humanos que mantinham contato com os animais afe-tados também foram relatadas. Assim, infecções poramostras semelhantes ao vírus VACV em bovinos e emhumanos parecem em expansão no estado, gerando per-das econômicas em animais e quadros de doençaincapacitante temporária em pacientes humanos. Dessaforma, a possibilidade da imunização do gado leiteiro noestado deve ser devidamente avaliada.

TERMOS DE INDEXAÇÃO: Infecções por Orthopoxvirus, PCR,teste de neutralização, microscopia eletrônica, estado do Riode Janeiro.

INTRODUCTIONThe family Poxviridae comprises a group of virus naturallyinfecting humans and many other vertebrate species andinsects as well. In vertebrates, these viruses cause mainlyvesicopustular infections of different degrees of severity(Schatzmayr & Azeredo-Costa 2005). The majority ofhuman poxvirus infections are zoonotic while the smallpoxvirus and Molluscum contagiosum are solely humanpathogens. Among the genera which are able to infectvertebrates, the Orthopoxvirus is the most important. Thisgenus includes smallpox virus, whose human infection waseradicated from the world in 1977; rabbitpox; vaccinia virus,which is used for vaccine preparation against smallpox;cowpox, a zoonotic virus occurring mainly in rodents inEurope and parts of Asia and monkeypox, which circulatesmainly in Africa in wild animals. This last virus was recentlyintroduced into North America by importation of pet rodents(CDC 2003).

Since 1999, orthopoxvirus infections have beenreported in the state of Rio de Janeiro (RJ) as a zoonoticdisease, involving dairy cattle and people in contact withthe affected animals (Damaso et al. 2000; Schatzmayr etal. 2000). The Cantagalo strain was characterized at

molecular level as a vaccinia-like virus that resembled thevaccinia/IOC strain used for vaccine preparation in the past(Damaso et al. 2000). Later on, other orthopoxviruses,isolated mainly in the southeastern region of the countrywere also confirmed as vaccinia-like poxviruses (Schatz-mayr et al. 2000, 2005, De Souza Trindade et al. 2003,Nagasse-Sugahara et al. 2004). The present articledescribes studies carried out in 12 counties in the north-western and Paraíba river valley regions of Rio de Janei-ro state (RJ) over the last 9 years. These studies aimed toconfirm the presence of poxviruses in skin lesions ofanimals and the presence of human infections related tothe animal disease, to characterize the circulating virusisolates and to contribute for a better understanding of theepidemiology of poxvirus infections in the state.

MATERIALS AND METHODSClinical specimens: Vesicular and pustular fluids, scabs andblood samples from dairy cattle presenting vesicopustulardisease were received in the laboratory of Instituto OswaldoCruz for diagnosis. The specimens were originated from themunicipalities of Cantagalo, Cordeiro, Santo Antonio de Padua,Aperibé, Cambuci and Miracema in the northwestern region andValença, Barra do Piraí, Rio das Flores, Piraí, Rio Claro andResende in the Paraiba river region of the state of Rio de Janeiro(Fig.1).

In Paraiba river valley the county of Valença represents 35.5% of the farms with clinical cases, followed by Barra do Piraíwith 19.3% and Resende with 16.1%. Most of the cases occuredfrom May to August, corresponding to the dry season. Thespecimens were sent to the laboratory by animal healthauthorities for etiologic confirmation Serum samples wereobtained from most cases and skin specimens were collectedonly in acute cases. A total of 152 animal infections were studied,with 41 skin and 135 blood specimens being collected andanalyzed. Data on the cases were obtained from the owners ofthe animals and from field investigations carried out by one ofthe authors in the Paraíba river area (RVCC).

Virus isolation: specimens collected from the skin lesionswere grounded and treated with proportional volume of Eagle


Animal infections by vaccinia-like virus in the state of Rio de Janeiro: An expanding disease 511

Fig.2. Results of the PCR test for the HA gene of pox virus inagarose gel 1.5%. Result of the amplification (approx.1107bp) by PCR of the strains: 1- Cordeiro 509; 2- Cambuci; 3-Miracema; 4- Aperibé; 5- Cordeiro 510; 6- CTGV-IOC; 7-CTGV; 8- CP (VV-NYBH Wyeth); 9- CN-BIO; 10- CN-H2O;11- Ladder 123 bp.

tissue culture medium plus antibiotics. The material wasinoculated in a VERO cell strain permissive to poxvirus. Theinoculated cells were observed for cytopathic effect (CPE) andthe presence of the virus was confirmed by electron microscopy(EM) and polymerase chain reaction (PCR).

Electron microscopy: fragments of skin and vesicular fluidswere prepared for transmission EM by dilution in distilled waterand negative contrasting using PTA 1% (Brenner & Horne 1959).Observations were then made at 30,000x magnification in a ZeissElectron Microscope, model 900. Tissue culture supernatantswere contrasted and observed as described.

PCR and nucleotide sequencing: briefly, external primers(HAOUTR and HAOUTF) as previously described (Damaso2000) were applied for amplification of a segment of 1171 bp ofthe HA gene. Vaccinia-like virus strains isolated from themunicipalities of Cordeiro, Cambuci, Miracema and Aperibé andthe Cantagalo/IOC strain were included. As controls, the originalCantagalo strain and the Wyeth-NYBH vaccinia strain were alsosubmitted to PCR (Fig.2). For sequencing of a genome regionof Cantagalo/IOC strain, which has been isolated in same areaand on the same occasion as the original Cantagalo strain, twointernal primers(HAINTR and HAINTF) were used.

areas of the municipalities of Cordeiro and Cantagalo At eachcapture site, traps were set on linear transects with 20 trappingstations at 10m intervals. All transects were geographicallypositioned using the GARMINÒ GPS 12 GPS receiver, refer-enced to WGS-84 (World Geodetic System, 1984). We usedtwo types of live-traps: Sherman (H.B. Sherman Traps®, 7.62 x9.53 x 30.48cm) and Tomahawk (Tomahawk Live Traps®, 40.64x 12.70 x 12.70cm) to capture small mammals weighing up to 3kg. The bait was a mixture of banana, bacon, oats and peanutbutter. The total sampling effort was 260 trap-nights in Cordeiroand 440 trap-nights in the Paraíba do Sul locality (Cantagalo).

Preliminary identification of rodents at genus level was donein the field by external morphology, followed by confirmation bykaryotyping (De Andrade et al. 2004).

All the animals were euthanized to carry out cytogenetictechniques and collection of blood and organs for poxvirusdiagnosis, in accordance with bioethics protocols for animal use.The researchers used individual protection equipment (3M HEPAfilters, biological level 3) and other biosafety methods, followingprotocols approved by the Biosafety Committee of the OswaldoCruz Institute. The animal trapping was licensed by the BrazilianInstitute for the Environment and Renewable Natural Resources(Instituto Brasileiro do Meio Ambiente e dos Recursos NaturaisRenováveis, IBAMA), under license numbers 068/2005 and 225/2006.

Serum samples from 17 rodents were tested for antibodiesas described. Tissue fragments (liver, kidneys, lungs) were alsocollected and brought to the laboratory in liquid nitrogen,grounded and analysed by PCR and virus isolation. Alltechniques using the rodent specimens were carried out in alaboratory certified at Biosafety level 3, considering the possiblepresence of other pathogenic viruses in the wild animals.

RESULTSAnalysis of specimens collected in 12 municipalitiesconfirmed the association of orthopoxviruses with vesiculardisease in 152 animals, by at least one of the techniquesapplied. A total of 25 orthopoxviruses were isolated intissue culture and/or detected by PCR.

In Figure 2, PCR amplifications of the HA gene of fiveisolates are compared with the Cantagalo/IOC strain, theoriginal UFRJ Cantagalo strain and the Wyeth vacciniastrain. The figure shows PCR amplification of all fiveisolates, indicating homology at nucleotide level with thecontrols.

Figure 3 shows a phylogenetic analysis of the HAorthopoxvirus gene, demonstrating homology between theCantagalo/IOC and original Cantagalo strains and a closerelationship with the IOC vaccine strain, which has beenused as antigen for the serology.

Table 1 presents the results of the different methodsused to identify/characterize the viruses. Since PCR wasintroduced in our laboratory by 1995, evaluation ofsensitivity of the tests were possible only in specimenstested thereafter. In those samples in which PCR and virusisolation were carried out concomitantly, the PCR test wasmore sensitive, as expected.

Electron microscopy shows typical morphology oforthopoxvirus virions (Fig.4).

Antibody testing alone was responsible for the definitive

Sequence alignment was performed using the Clustal Wsoftware and the phylogenetic tree was constructed using theMEGA 3.1 software, by means of the neighbor joining methodunder a matrix of genetic distances established by the Kimuratwo-parameter model. The bootstrap with 1000 replications wasused to estimate the reliability of the predicted tree. The bootstrapvalues are indicated at the branch points in Figure 3.

Serology: the sera were submitted to a 50% plaque-reduction neutralization test (PRNT), using the Cantagalo/IOCstrain as the reference virus. Serum dilutions and a virussuspension containing approximately 40 plaque-forming units(pfu) in 100 microliters were incubated at 37°C for 1h in cellculture microplates, followed by addition of a suspension ofVERO cells. After 48h, the plates were stained with crystal violetand formaldehyde 1%, washed and the plaques were countedunder the microscope.

Rodent collection: small wild mammals were trapped in rural



Fig.3. Phyllogenetic analysis of Cantagalo IOC strain. Thecomparative analysis of the DNA sequences (gene HA ofOrthopoxvirus) was made using CLUSTAL software. Thephyllogenetic tree was constructed applying the neighbor-joining method (bootstrap = 1000), using the program MEGA3.1 (Molecular Evolutionary Genetics Analysis, PennsylvaniaState University). The genetic distance was obtained by theproportional distance method (two paramets model, Kimura).The reference sequences used were: Vac variants M14783,Vac ihdw AF375121, Z99051 Wyeth, RPV rev AF375118,Vac IOC AF229248, Cg IOC, CgAF229247, Vac lenAF375123, CPX 89 5 AF375086, MPV wmp AF375114.

Fig.4. Orthopoxvirus particle observed using electron microscopytechnique in bovine specimen.

Fig.5. Lesions observed in the udder (A, B, C), in calf tongue(D) and nose (E).

Table 1. Laboratorial results of the specimens frombovines suspected of poxvirus infection in 12 counties of

the state of Rio de Janeiro, 1999-2007

Positive samples Negative samples

RT-PCR test 22 09Vírus isolation 13 14Electron microscopy 16 09Neutralization test 100 30

diagnostic in most cases, being sera dilutions >1/10accepted as positive In some animals, titers as high as1280 were observed. Antibodies to orthopoxviruses weredetected at dilution of 1/20 in three subsequent antibodytitration tests in the serum of one rodent genus (Akodon

sp.) out of 17 animals collected in the same week.Nonetheless, no virus could be detected in tissues by virusisolation or PCR in any of the rodents collected.

The lesions in the adult cattle were observed in theudder and teats and in the lips and around the noses ofcalves. In one calf which was positive by PCR andneutralizing antibodies, lesions were detected also in thetongue (Fig.5).

Typically, after the vesicle/pustular stage, the mem-brane covering the lesion dried and pelt off, leaving abloody painful wound, sometimes reaching large areas inthe teats (Fig.5). The evolution of the vesicle to the com-plete healing took about 3 to 4 weeks.

Human cases were observed in workers in directcontact with affected animals, yet no human-to-humantransmission was reported. In more than 80% of thepatients only lesions in the hands and fingers wereobserved. Almost all patients could not attend their nor-mal activities during the disease. Most patients (97.3% of22) recorded pain in the lesions, fever and lymph nodeswelling, headache, sudoresis and prostration. Theincubation period, after the first contact with the infectedanimals was of 5 to 7 days and the clinical disease lastedabout 3 weeks. Cases of poxvirus infection in humans andcattle had been confirmed at other municipalities but sofar have not been confirmed at laboratory level.

DISCUSSIONOrthopoxvirus infections in human and animals have beendescribed in several countries (Lum et al. 1967, Mesquita& Schatzmayr 1969, Topciu et al. 1976, Schatzmayr et al.2000, 2005). Nagasse-Sugahara et al. (2004), studying74 cases of a vesicular human disease in the Paraíba rivervalley in the state of São Paulo, indicated the circulationof poxviruses in the area.

In Brazil, the smallpox vaccination in rural areas hasbeen carried out farm-by-farm. Careless handling of the


Animal infections by vaccinia-like virus in the state of Rio de Janeiro: An expanding disease 513

live vaccine - containing virus titers as high as 108 infectiousparticles per mililiter - possibly allowed the disseminationof the vaccine virus in nature. It is very likely that vaccineviruses had been introduced in nature in different occasions.Although smallpox vaccination was discontinued in thecountry in the 70s, vaccinia-like viruses have been isolatedfrom animals confirming that vaccinia-like virus arecirculating in the country, a fact already accepted by theinternational literature (Regnery 2007).

In the state of Rio de Janeiro, animal and humanpoxvirus infections have been repeatedly described alongthe years (Silva & Moraes 1961, Mesquita & Schatzmayr1969, De Souza et al. 2003, Costa et al 2007, Donatele etal. 2007, Simonetti et al 2007). In this article, the clinicallesions observed in the animals confirmed observationsof these authors. Vesicles occurred in the udder, particularlyin the teats, with coalescence of vesicles resulting in largevesicular lesions that erupted and became covered byscabs. Permanent udder lesions were observed as well asmastitis, which resulted in economic losses, besides thereduction in milk production.

The lesions in the tongue of one calf suggest the pre-sence of virus in the oral cavity and probably the salivacould transmit the virus by direct contact with other animalsin the herd. Nevertheless, this observation deserves furtherstudies.The disease was transmitted only to calvessuckling in infected mothers, but not in those drinking milkin tanks, suggesting that transmission occurred only bydirect contact.

Animals from one of the farms with vesicular/pustulardisease were negative to Orthopoxvirus by all laboratorytechniques applied. Other agents causing vesiculardisease like parapoxviruses might have been involved intheses cases as already described in sheep in the state(Barth et al. 2005).

Our PCR results showed that the viruses recoveredfrom sick animals match with the Cantagalo strain,confirming that vaccinia-like virus strains circulating in thestate are close related to the original Cantagalo strain(Fig.2, lanes 1-7). This strain has been demonstrated tobe, at molecular level, similar to the strain used for vaccinepreparation at the Oswaldo Cruz Institute (Damaso et al.2000).

In other nearby counties, vesicular/pustular diseaseshave also been described in dairy cattle, suggesting thatthe virus is present in large areas of the state. A surveillancesystem has been established at Paraíba valley and othermunicipalities are being monitored. According toinformations obtained from local residents, similar episodesof vesicular disease have been observed in the Paraíbavalley, along the last years and even just after the smallpoxmass vaccination campaign, about forty years ago.

The presence of antibodies to orthopoxvirus in just onewild rodent of genus Akodon is not enough to confirm thepresence of virus circulation in rodents in the state.However this hypothesis is well supported, since the firstvaccinia-like virus isolated in the country in nature was

present in the whole blood from a rodent (Oryzomys sp.)in the Amazon region (Fonseca et al. 1998). Cotia virus,also a poxvirus was isolated in a sentinel rodent in thestate of São Paulo (Lopes et al. 1965, Ueda et al. 1978),confirming that this group is circulating in arthropods inthe country.

These data support that further field studies are neededfor confirming the possible role of wild rodents as reservoirsfor orthopoxviruses in the state. In this sense, a recentreview emphasized the capacity of orthopoxviruses toadapt to new animal species (Regnery 2007). Field studiesare needed for confirming the possible role of reservoirslike wild rodents and vectors, which might be related topoxviruses transmission in the state.

According to the data obtained over the years,Orthopoxvirus infections seem to be spreading in the stateof Rio de Janeiro and should be considered a newemerging zoonotic disease. This disease may causetemporary incapacitating human disease that may be moresevere in immunosuppressed individuals. In dairy cattle,such infections cause important economic losses, due toreduction in milk production and permanent lesions on theudder. Therefore, the possibility of immunization of dairycattle against poxviruses should be carefully evaluated.

Acknowledgements.- To all the professionals and animal owners whocollaborated in obtaining the specimens and the epidemiological data.Financial support: CNPq (Proc.472.332/2006-0), FAPERJ (Proc.E-26/171.152/2005) and Oswaldo Cruz Foundation.

REFERENCESBarth O.M., Majerowicz S., Romijn P.C., Silva R.C.F., Costa C.H.C.,

Otavio J.R., Pires A.R. & Schatzmayr H.G. 2005. Occurrence ofparapoxvirus infections in ovine flocks in the state of Rio de Janeiro.Virus Rev. Res. 10:23-26.

Brenner S. & Horne R.W. 1959. A negative staining method for high-resolution electron microscopy of viruses. Biochim. Biophsys. Acta34:103-104.

Centers for Disease Control and Prevention 2003. Multistate outbreakof monkeypox - Illinois, Indiana and Wisconsin. J. Am. Med. Assoc.290 (Jul.2):30-31.

Costa R.V.C., Simonetti B.R., Abreu D.C., Simonetti J.P., GonçalvesM.C.R., Silva M.E.V., Brust L.A.C., Barth O.M. & Schatzmayr H.G.2007. Animal infections by vaccinia-like virus in the state of Rio deJaneiro:2-Paraiba river valley. Virus Rev. Res. 12:37-42.

Damaso C.R.A., Esposito J.J., Condit R.C. & Moussatché N. 2000. Anemergent poxvirus from humans and cattle in Rio de Janeiro state:Cantagalo virus may derive from Brazilian smallpox vaccine. Virology277:439-449.

De Andrade A.F.B., Bonvicino C.R., Briani D.C. & Kasahara S. 2004.Karyologic diversification and phylogenetic relationships of the genusThalpomys (Rodentia, Sigmodontidae). Acta Theriologica 49:181-189.

De Souza Trindade G., Fonseca F.G., Marques J.T., Nogueira M.L.,Mendes L.C., Borges A.S., Peiro J.R., Pittuco A.M., Bonjardin C.A.,Ferreira P.C. & Kroon E.G. 2003. Araçatuba virus: A vaccinia likevirus associated with infection in humans and cattle. Emerg. Infect.Dis. 9:155-160.

Donatele D.M., Travassos C.E.P.F., Leite J.A. & Kroon E.G. 2007. Epi-demiologia da poxvirose bovina no Estado do Espírito Santo, Brasil.Braz. J. Vet. Res. Anim. Sci. 44:275-282.



Fonseca F.G., Lanna M.C.S., Campos M.A.S., Kitajima E.W., PerezJ.N., Golgher R.R., Ferreira P.C.P. & Kroon E.G. 1998. Morphologicaland molecular characterization of the poxvirus BeAn 58058. Arch.Virol. 143:1171-1186.

Lopes O.S., Lacerda J.P.G., Fonseca I.E.M., Castro D.P., Forattini O.P.& Rabello E.X. 1965. Cotia virus: New agent isolated from sentinelmice in São Paulo, Brazil. Am. J. Trop. Med. Hyg. 14:156-157.

Lum G.S., Soriano F., Trejos A. & Lierena J. 1967. Vaccinia epidemicand epizootic in El Salvador. Am. J. Trop. Med. Hyg. 16:332-338.

Mesquita J.A. & Schatzmayr H.G. 1969. Estudos laboratoriais de infec-ções humanas e de bovinos com vírus do grupo pox. Revta Soc. Bras.Med. Trop. 3:171-175.

Nagasse-Sugahara T.K., Kisielius J.J., Ueda-Ito M., Curti S.P., FigueiredoC.A. & Cruz A.S. 2004. Human vaccinia-like virus outbreaks in SãoPaulo and Goiás States, Brazil: Virus detection, isolation andidentification. Revta Inst. Med. Trop. São Paulo 46:315-322.

Regnery R.L. 2007. Poxvirus and passive quest for novel hosts. Curr.Top. Microbiol. Immunol 315:345-361.

Schatzmayr H.G. & Costa E.A. 2005. Poxvirus, p.1936-1944. In: CouraJ.R. (Ed.), Dinâmica das Doenças Infecciosas e Parasitárias. EditoraGuanabara, Rio de Janeiro.

Schatzmayr H.G., Lemos E.R., Mazur C., Schubach A., Majerowicz S.,Rozental T., Schubach M.C., Bustamante M.C. & Barth O.M. 2000.Detection of poxviruses associated with human cases in the state ofRio de Janeiro: A preliminary report. Mem. Inst. Oswaldo Cruz 95:625-627.

Schatzmayr H.G., Romijin P.C., Barreto D.F., Silva E.E., Farias-FilhoJ.C., Tavares A.F.A. & Barth O.M. 2005. An outbreak of vesicopustulardisease in humans and dairy cattle in the state of Rio de Janeiro.Virus Rev. Res. 10:61-63.

Silva P.L. & Moraes L.T. 1961. Nota sobre a ocorência da varíola bovi-na no estado do Rio de Janeiro. 1 Estudo da doença no município deTrês Rios. Veterinária, Rio de J., 14:31-35.

Simonetti B.R., Abreu D.C., Simonetti J.P., Gonçalves M.C.R., SilvaM.E.V., Barth O.M. & Schatzmayr H.G. 2007. Animal infections byvaccinia-like viruses in the state of Rio de Janeiro:1-Northwesternregion. Virus Rev. Res. 12:32-36.

Topciu V., Luca I., Moldovan E., Stoianovici V., Plavosin L. & Milin D.1976. Transmission of vaccinia virus from vaccinated milkers to cattle.Virology 27:279-282.

Ueda Y., Tsuruhara K.R. & Tagaya T. 1978. Studies on Cotia virus: Anunclassified poxvirus. J. Gen. Virol. 40:263-276.

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