• 1.

    Prescott JF, 1991. Rhodococcus equi: an animal and human pathogen. Clin Microbiol Rev 4: 2034.

  • 2.

    Takai S, Tharavichitkul P, Takarn P, Khantawa B, Tamura M, Tsukamoto A, Takayama S, Yamatoda N, Kimura A, Sasaki Y, Kakuda T, Tsubaki S, Maneekarn N, Sirisanthana T, Kirikae T, 2003. Molecular epidemiology of Rhodococcus equi of intermediate virulence isolated from patients with and without acquired immune deficiency syndrome in Ching Mai, Thailand. J Infect Dis 188: 17171723.

    • Search Google Scholar
    • Export Citation
  • 3.

    Weinstock DM, Brown AE, 2002. Rhodococcus equi: an emerging pathogen. Clin Infect Dis 34: 13791385.

  • 4.

    Takai S, 1997. Epidemiology of Rhodococcus equi infections: a review. Vet Microbiol 56: 167176.

  • 5.

    Verville DT, Huicke MM, Greenfield RA, Fine DP, Kuhls TL, Slater LN, 1994. Rhodococcus equi infections of humans: 12 cases and literature review. Medicine 73: 119132.

    • Search Google Scholar
    • Export Citation
  • 6.

    Ribeiro MG, Seki I, Yasuoka K, Kakuda T, Sasaki Y, Tsubaki S, Takai S, 2005. Molecular epidemiology of virulent Rhodococcus equi from foals in Brazil: virulence plasmids of 85-kb type I, 87-kb type I, and a new variant, 87-kb type III. Comp Immunol Microbiol Infect Dis 28: 5361.

    • Search Google Scholar
    • Export Citation
  • 7.

    Takai S, Fukunga N, Ochiai S, Imai Y, Sasaki Y, Tsubaki S, Sekizaki T, 1996. Identification of intermediately virulent Rhodococcus equi isolates from pigs. J Clin Microbiol 34: 10341037.

    • Search Google Scholar
    • Export Citation
  • 8.

    Quinn PJ, Carter ME, Markey B, Carter GR, 1994. Clinical Veterinary Microbiology. London: Wolfe, 137143.

  • 9.

    Takai S, Ikeda T, Sasaki Y, Watanabe Y, Ozawa T, Tsubaki S, Sekizaki T, 1995. Identification of virulent Rhodococcus equi by amplification of gene coding for 15–17-kDa antigens. J Clin Microbiol 33: 16241627.

    • Search Google Scholar
    • Export Citation
  • 10.

    Makrai L, Kobayashi A, Matsuoka M, Sasaki Y, Kakuda T, Dénes B, Hajtós I, Révész I, Jánosi K, Fodor L, Varga J, Takai S, 2008. Isolation and characterization of Rhodococcus equi from submaxillary lymph nodes of wild boars (Sus scrofa). Vet Microbiol 131: 318323.

    • Search Google Scholar
    • Export Citation
  • 11.

    Takai S, Sasaki Y, Ikeda T, Uchida Y, Tsubaki S, Sekizaki T, 1994. Virulence of Rhodococcus equi isolates from patients with and without AIDS. J Clin Microbiol 32: 457460.

    • Search Google Scholar
    • Export Citation
  • 12.

    Makrai L, Takai S, Tamura M, Tsukamoto A, Sekimoto R, Sasaki Y, Kakuda T, Tsubaki S, Varga J, Fodor L, Solymosi N, Major A, 2002. Characterization of virulence plasmids in Rhodococcus equi isolates from foals, pigs, humans and soil in Hungary. Vet Microbiol 88: 377384.

    • Search Google Scholar
    • Export Citation
  • 13.

    Ministério da Saúde Brazil, 2007. Programa Nacional de DST/AIDS. Brasilia: Secretaria de Vigilância em Saúde. Boletim Epidemiológico DST/AIDS.

    • Search Google Scholar
    • Export Citation
  • 14.

    Silva P, Miyata M, Sato DN, Santos AC, Mendes NH, Leite CQ, 2010. Rhodococcus equi isolation from sputum of patients with suspected tuberculosis. Mem Inst Oswaldo Cruz 105: 199202.

    • Search Google Scholar
    • Export Citation
  • 15.

    Ribeiro MG, Takai S, Guazzelli A, Lara GH, Silva AV, Fernandes MC, Condas LAZ, Siqueira AK, Salerno T, 2010. Virulence genes and plasmid profiles in Rhodococcus equi isolates from domestic pig and wild boars (Sus scrofa) in Brazil. Res Vet Sci Oct 25 [Epub ahead of print].

    • Search Google Scholar
    • Export Citation
  • 16.

    Costa MM, Machado SA, Krewer CC, Fighera RA, Ilha MR, Graça DL, Vargas AP, Mattos-Guaraldi AL, 2006. Pathogenecity of Rhodococcus equi isolates from human, horse clinical and environment in immunodeficient mice. Pesqui Vet Bras 26: 167170.

    • Search Google Scholar
    • Export Citation
  • 17.

    Napoleão F, Damasco PV, Camello TC, Vale MD, Andrade AF, Hirata R Jr, Mattos-Guaraldi AL, 2005. Pyogenic liver abscess due to Rhodococcus equi in an immunocompetent host. J Clin Microbiol 43: 10021004.

    • Search Google Scholar
    • Export Citation

 

 

 

Identification of Virulence-Associated Plasmids in Rhodococcus equi in Humans with and without Acquired Immunodeficiency Syndrome in Brazil

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  • Department of Veterinary Hygiene and Public Health, School of Veterinary Medicine and Animal Science, Universidad Estadual Paulista, Botucatu, Sao Paulo, Brazil; Department of Animal Hygiene, School of Veterinary Medicine and Animal Sciences, Kitasato University, Aomori, Japan; Medicina Veterinária Preventiva, Universidade Federal de Santa Maria, Rio Grande do Sul, Brazil; Faculdade de Ciências Médicas, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, Brazil; Parasitology Research Group, Department of Biological Sciences, Feira de Santana State University, Feira de Santana, Bahia, Brazil

Virulence of Rhodococcus equi strains from 20 humans in Brazil was investigated by using a polymerase chain reaction to characterize isolates as virulent (VapA), intermediately virulent (VapB), and avirulent. Nine isolates were obtained from human immunodeficiency virus (HIV)–positive patients, six from HIV-negative patients, and five from patients of unknown status. Five isolates were VapB positive, four were VapA positive, and eleven were avirulent. Among the nine isolates from HIV-positive patients, five contained VapB plasmids and two contained VapA plasmids. Five VapB-positive isolates had the type 8 virulence plasmid. Eleven of the patients had a history of contact with livestock and/or a farm environment, and none had contact with pigs.

Rhodococcus equi is a well-recognized, gram-positive, intracellular bacterium associated with pyogranulomatous infections in humans, domestic animals, and wildlife.1 Currently, R. equi has emerged as an increasingly common opportunistic pathogen among immunocompromised human patients, particularly those infected with human immunodeficiency (HIV).2 Approximately two-thirds of patients with rhodococcosis are co-infected with HIV.3

Rhodococcus equi is widespread in soil and manure on farms, mainly in feces of foals and other herbivores.4 Inhalation and consumption of contaminated water and contact with pastures appear to be the major source of transmission this microorganism in livestock.1 However, routes of R. equi transmission for humans remain controversial, although a history of contact with livestock and farms is considered to be a risk factor.5

The virulence of R. equi has been attributed to the presence of virulence-associated antigens and plasmids. Three virulence levels of isolates are recognized: virulent, intermediately virulent, and avirulent. Virulent strains contain a large 80–90-kb plasmid that contains the gene encoding virulence-associated 15–17-kD antigen (VapA).4 These virulent isolates are recognized as the major causes of suppurative pneumonia and ulcerative enteritis in foals.6 Intermediately virulent isolates are characterized by the presence of 20-kD antigens (VapB), which are encoded by 79–100-kb plasmids. These intermediately virulent strains are commonly found in lymph nodes of pigs with and without lymphadenitis4,7 and in humans with immune system dysfunction, especially HIV-positive patients.2,3 Avirulent isolates show no evidence of vapA or vapB genes and are found in HIV-positive patients, in environments containing livestock, and in soil or sand from parks and household yards.4

The purpose of this study was to investigate virulence-associated genes (vapA and vapB) and plasmid profiles of R. equi isolates from 20 humans with and without acquired immune deficiency syndrome (AIDS) in Brazil.

Eighteen R. equi isolates were obtained from 18 patients admitted to hospitals in four states in Brazil over a 10-year period (1997–2007). We reviewed records concerning epidemiologic factors (sex, age, and history of contact with domestic animals and/or farms), primary site of infection, major clinical signs, and other laboratory diagnoses (particularly antibodies against HIV and other debilitating diseases). Two strains were isolated from asymptomatic farm workers. Unfortunately, some epidemiologic details and outcomes were not available or were not identified in certain cases, especially for HIV-positive patients. All strains were isolated by culturing on sheep blood agar incubated aerobically for 3 days at 37°C. Rhodocoddus equi isolates were classified according to conventional methods8 and analyzed by using a polymerase chain reaction (PCR).2

Isolation of plasmid DNA was obtained by using an alkaline lysis method with some modifications as described elsewhere.2 Specific DNAs for PCR amplification were determined according to reported sequences of the vapA (15–17-kD antigen) and vapB (20-kD antigen) genes (GenBank accession nos. D212361 and D44469).

Plasmid DNA was digested with restriction endonucleases Eco RI, Eco T22I, and Hind III.7,9 Samples of plasmid were separated by electrophoresis on a 1.0% agarose gel, stained with ethidium bromide, and examined under ultraviolet light. Primer 1 (5′-GACTCTTCACAAGACGGT-3′) and primer 2 (5′-TAGGCGTTGTGCCAGCTA-3′) were used to identify virulent isolates (vapA gene) on the basis of amplification of the expected 569–552-basepair product. Primer 3 (5′-AACGTAGTCGCGGTGAGAA-3′) and primer 4 (5′-ACCGAGACTTGAGCGACTA-3′) were used to identify intermediately virulent (vapB gene) isolates by using the expected 1,066–1,048-basepair product.9 The PCR amplification was carried out using 10 μL of the DNA preparation in a 50-μL reaction containing 10 mM Tris-HCl (pH 8.3 at 25°C), 50 mM KCl, 1.5 mM MgCl2, 0.2 mM each deoxynucleotide triphosphate, 1 mM primer (each), and 2.5 units of Taq DNA polymerase.2 Samples were subjected to 30 cycles of amplification: denaturation for 90 seconds at 94°C, annealing for 1 minute at 55°C, and extension for 2 minutes at 72°C.9

The virulent ATCC 33701 strain (equine origin), intermediately virulent strains (human and pig origin), and other representative R. equi strains for various plasmid types were used as reference strains. Corresponding plasmid profiles and virulence levels of reference strains have been described.2,6,7,9,10 Statistical analysis was conducted by using the chi-square test (Epi Info version 6.4; Centers for Disease Control and Prevention, Atlanta, GA), and P < 0.05 was considered significant.

Epidemiologic, diagnostic, and virulence plasmid profile findings for the 20 R. equi strains isolated from symptomatic and asymptomatic patients are shown in Table 1. Of 20 patients, 6 were men (patients 5, 16, 17, 18, 19, and 20), and the sexes of the remaining patients were unknown. Three patients (patients 17, 19, and 20) were 31–40 years of age, 4 (patients 5, 14, 16, and 18) were 41–50 years of age, and the ages of other patients were unknown.

Table 1

Epidemiologic, diagnostic, and virulence plasmid profile findings for Rhodococcus equi strains isolated from 20 symptomatic and asymptomatic humans, Brazil, 1997–2007*

Patient no.Animal or farm contactMajor clinical signDiagnostic cultureUnderlying conditionVirulence plasmid profile (type)
1UnknownPneumoniaBronchial washHIV positiveVapB (type 8)
2FarmPneumoniaLung fragmentHIV positiveVapA (87-kb type I)
3Equine and farmPneumoniaBronchial washHIV positiveVapB (type 8)
4UnknownPneumoniaBronchial washHIV positiveVapB (type 8)
5EquineHepatitis, enteritis, and weight lossHepatic fragmentHIV negative, alcoholism, and hepatitisAvirulent
6UnknownPneumoniaBronchial washUnknownAvirulent
7UnknownPneumoniaBronchial washHIV negativeAvirulent
8Equine, bovine, and farmPneumoniaBronchial washHIV positiveVapA (85-kb type I)
9UnknownPneumoniaBronchial washUnknownAvirulent
10EquinePneumoniaBronchial washUnknownAvirulent
11UnknownPneumoniaBronchial washUnknownAvirulent
12UnknownPneumoniaBronchial washUnknownAvirulent
13BovinePneumoniaBronchial washHIV positiveAvirulent
14UnknownPneumoniaBronchial washHIV positiveVapB (type 8)
15FarmPneumoniaBronchial washHIV positiveAvirulent
16Equine, bovine, and farmPneumoniaBronchial washHIV negativeVapA (87-kb type I)
17Equine, bovine, and farmWeight loss and gastroenteritisSwab under a fingernailHIV negative and alcoholismAvirulent
18UnknownHepatitis and cutaneous lesionBlood and cutaneous fragmentHIV positive and hepatitisVapB (type 8)
19FarmAsymptomaticNasal swabHIV negativeVapA (87-kb type I)
20FarmAsymptomaticNasal swabHIV negativeAvirulent

HIV = human immunodeficiency virus; Vap = virulence-associated protein; VapB = intermediately virulent; VapA = virulent.

Nine patients were HIV positive, which was defined as the presence of antibodies against HIV in serum samples. Among HIV-positive patients, one had also hepatitis. Six patients were not infected with HIV, and the HIV status of the five remaining patients was unknown. One HIV-negative patient had a history of alcoholism and hepatitis, and another HIV-negative patient had a history of alcoholism as an underlying condition.

The major clinical sign identified in 15 (75.0%) patients was pneumonia. Rhodococcus equi was isolated from bronchial washes (14 patients), nasal mucosa (2 patients), lung fragment (1 patient), hepatic fragment (1 patient), blood and cutaneous fragments (1 patient), and the fingernail region (1 patient).

Eleven patients (55.0%) had history of contact with livestock and/or farms. Contact exclusively with a farm environment was reported by four (20.0%) patients, and contact with only equines or bovines were reported by two (10.0%) patients and one (5.0%) patient, respectively. For nine patients, the date of contact with a farm environment or livestock was unknown. No patients had a history of contact with pigs or pig breeders.

Virulence plasmid analysis of the 20 R. equi isolates showed the presence of 5 (25.0%) intermediately virulent, 4 (20.0%) virulent, and 11 (55.5%) avirulent isolates. Among the four VapA isolates, three had the 87-kb type I plasmid and 1 had the 85-kb type I plasmid. For two isolates with a VapA plasmid profile from patients who had a history of equine contact, one isolate contained the 85-kb type I plasmid and the other isolate contained the 87-kb type I plasmid.

Of nine strains isolated from HIV-positive patients, five contained the vapB gene, two contained the vapA gene, and two did not contain either the vapA or the vapB gene. Plasmid profiles of the five intermediately virulent isolates were characterized as type 8, and plasmids with intermediate virulence was significantly associated with an HIV-positive diagnosis (P < 0.001). The presence of the vapA or vapB genes was also significantly associated with HIV-positive patients (P = 0.0124). Among the 20 patients, 11 had avirulent isolates, accounting for 2 HIV-positive patients, 2 HIV-negative patients, and 2 HIV-negative patients with a history of alcoholism and/or hepatitis. The five remaining patients had an unknown history of HIV infection or other debilitating diseases.

Among the 20 patients, clinical outcome was known only for four patients. Among these patients, cure was observed in 2 patients (patients 5 and 16), and disease was fatal in 2 patients (patients 2 and 19).

The first recognized case of human rhodococcosis was reported in 1967. Only 12 new cases were described in 15 years after this initial report.5 In contrast, a substantial increase in the number of reported human cases has occurred in recent decades worldwide, mainly as co-infection with HIV.2,11,12

In Latin America, approximately 1.6 million persons are infected with HIV. The Brazilian Ministry of Health reported 474,273 cases of AIDS during 1980–2007. The disease was fatal in 28,609 persons in Brazil during 1983–2003.13 Despite implementation of control strategies and treatment protocols against HIV/AIDS in Brazil, deaths of HIV–positive patients co-infected with R. equi have been observed.14 However, little information is available in Brazil about virulence plasmid profiles of R. equi isolates from humans.1517

Intermediately virulent strains of R. equi are predominantly identified in HIV-positive patients,2 the lymph nodes of pigs with and without lymphadenitis,7,12 and, more recently, in lymph nodes of wild boars (Sus scrofa) in Hungary10 and Brazil.15 Furthermore, virulent R. equi strains also have been described in HIV-negative human patients.11 Despite similarities of virulence-associated plasmid profiles of R. equi reported for humans, pigs, and wild boars, the role of these animal species in transmission of the microorganism to humans is controversial.10,12 In addition, the history of contact between persons infected with R. equi and domestic pig breeders, or an environment in which pigs are present is unclear.15 Evidence supports the hypothesis that consumption of pork products or undercooked pork may be a probable route of R. equi infection in humans in some countries.2

Rhodococcus equi infections in pigs and wild boars are restricted mainly to the lymphatic system, and are predominantly found in submaxillary lymph nodes.7,10 A recent investigation of R. equi strains from lymph nodes of domestic pigs and wild boars in Brazil showed that the VapB type 8 plasmid is the most common virulence type.15 Distinct 79–100 kb plasmids associated with expression of VapB in R. equi isolated from humans have been described in different countries and involve mainly types 1, 4, 7,2 and 5.12 Ours results indicate the exclusive presence of the type 8 plasmid among intermediately virulent isolates from humans. Interestingly, this predominant type 8 VapB plasmid has not been reported in cases of human rhodococcosis. Thus, to our knowledge, the present report is the first description of HIV-positive patients infected with R. equi containing the VapB type 8 plasmid. None of the patients in our study had a history of contact with pigs or pig products. However, the fact that the type 8 virulence plasmid is found in humans, pigs, and wild boars in Brazil provides information about the source and route of R. equi infections in humans in this country.

For humans, exposure to soil contaminated with equine manure has been suggested as a route of transmission of virulent strains.3,11 The virulence of 41 R. equi isolates from foals in Brazil showed that all isolates were VapA positive: 33 strains contained the 87-kb type I plasmid, 6 contained the 85-kb type I plasmid, and 2 contained proposed new variants.6 Our results showed the same types of VapA (87-kb type I and 85-kb type I) in four patients, including those with and without AIDS. In addition, some of these patients had a history of contact with equines and/or farm environments. This circumstantial evidence suggests that exposure to equines and their environment may play an important role in cases of human rhodococcosis in Brazil.

Although our study focused on virulence-associated plasmid profiles of R. equi, some epidemiologic aspects of the cases were evaluated, in addition to contact between persons and livestock and/or farm environments. No sex or age predispositions have been found to be determinants of human rhodococcosis.1 In the present study, six patients were men 30–50 years of age. This finding is consistent with results of other studies, which have also identified similar frequencies of rhodococcosis in men 30–50 years of age,5,14 indicating an occupational risk of human infection by R. equi, particularly to immunocompromised patients exposed to livestock or farm environments.1,11

The clinical manifestation of R. equi in humans is diverse, although pulmonary infections are present in approximately 80% of cases.3 In the current study, R. equi was also isolated predominantly from pulmonary infections. Interestingly, two of our field strains were isolated from asymptomatic farm workers, one from the nasal mucosa and one from the fingernail region. This result provides further evidence that contact with soil or manure in contaminated farms or inhalation of the pathogen in dry or warm regions that facilitate aerosolization represent a risk factor for R. equi infections in humans.1,4,5,11

Surveillance studies concerning virulence plasmid profiles of R. equi isolates from humans and domestic animals in different geographic areas are needed to determine the role of animals in transmission of the pathogen to humans, particularly because of the opportunistic behavior of this bacterium in immunocompromised patients.

ACKNOWLEDGMENTS:

We thank the Núcleo de Coleção de Microrganismos do Instituto Adolfo Lutz de São Paulo, Brazil, for assistance.

  • 1.

    Prescott JF, 1991. Rhodococcus equi: an animal and human pathogen. Clin Microbiol Rev 4: 2034.

  • 2.

    Takai S, Tharavichitkul P, Takarn P, Khantawa B, Tamura M, Tsukamoto A, Takayama S, Yamatoda N, Kimura A, Sasaki Y, Kakuda T, Tsubaki S, Maneekarn N, Sirisanthana T, Kirikae T, 2003. Molecular epidemiology of Rhodococcus equi of intermediate virulence isolated from patients with and without acquired immune deficiency syndrome in Ching Mai, Thailand. J Infect Dis 188: 17171723.

    • Search Google Scholar
    • Export Citation
  • 3.

    Weinstock DM, Brown AE, 2002. Rhodococcus equi: an emerging pathogen. Clin Infect Dis 34: 13791385.

  • 4.

    Takai S, 1997. Epidemiology of Rhodococcus equi infections: a review. Vet Microbiol 56: 167176.

  • 5.

    Verville DT, Huicke MM, Greenfield RA, Fine DP, Kuhls TL, Slater LN, 1994. Rhodococcus equi infections of humans: 12 cases and literature review. Medicine 73: 119132.

    • Search Google Scholar
    • Export Citation
  • 6.

    Ribeiro MG, Seki I, Yasuoka K, Kakuda T, Sasaki Y, Tsubaki S, Takai S, 2005. Molecular epidemiology of virulent Rhodococcus equi from foals in Brazil: virulence plasmids of 85-kb type I, 87-kb type I, and a new variant, 87-kb type III. Comp Immunol Microbiol Infect Dis 28: 5361.

    • Search Google Scholar
    • Export Citation
  • 7.

    Takai S, Fukunga N, Ochiai S, Imai Y, Sasaki Y, Tsubaki S, Sekizaki T, 1996. Identification of intermediately virulent Rhodococcus equi isolates from pigs. J Clin Microbiol 34: 10341037.

    • Search Google Scholar
    • Export Citation
  • 8.

    Quinn PJ, Carter ME, Markey B, Carter GR, 1994. Clinical Veterinary Microbiology. London: Wolfe, 137143.

  • 9.

    Takai S, Ikeda T, Sasaki Y, Watanabe Y, Ozawa T, Tsubaki S, Sekizaki T, 1995. Identification of virulent Rhodococcus equi by amplification of gene coding for 15–17-kDa antigens. J Clin Microbiol 33: 16241627.

    • Search Google Scholar
    • Export Citation
  • 10.

    Makrai L, Kobayashi A, Matsuoka M, Sasaki Y, Kakuda T, Dénes B, Hajtós I, Révész I, Jánosi K, Fodor L, Varga J, Takai S, 2008. Isolation and characterization of Rhodococcus equi from submaxillary lymph nodes of wild boars (Sus scrofa). Vet Microbiol 131: 318323.

    • Search Google Scholar
    • Export Citation
  • 11.

    Takai S, Sasaki Y, Ikeda T, Uchida Y, Tsubaki S, Sekizaki T, 1994. Virulence of Rhodococcus equi isolates from patients with and without AIDS. J Clin Microbiol 32: 457460.

    • Search Google Scholar
    • Export Citation
  • 12.

    Makrai L, Takai S, Tamura M, Tsukamoto A, Sekimoto R, Sasaki Y, Kakuda T, Tsubaki S, Varga J, Fodor L, Solymosi N, Major A, 2002. Characterization of virulence plasmids in Rhodococcus equi isolates from foals, pigs, humans and soil in Hungary. Vet Microbiol 88: 377384.

    • Search Google Scholar
    • Export Citation
  • 13.

    Ministério da Saúde Brazil, 2007. Programa Nacional de DST/AIDS. Brasilia: Secretaria de Vigilância em Saúde. Boletim Epidemiológico DST/AIDS.

    • Search Google Scholar
    • Export Citation
  • 14.

    Silva P, Miyata M, Sato DN, Santos AC, Mendes NH, Leite CQ, 2010. Rhodococcus equi isolation from sputum of patients with suspected tuberculosis. Mem Inst Oswaldo Cruz 105: 199202.

    • Search Google Scholar
    • Export Citation
  • 15.

    Ribeiro MG, Takai S, Guazzelli A, Lara GH, Silva AV, Fernandes MC, Condas LAZ, Siqueira AK, Salerno T, 2010. Virulence genes and plasmid profiles in Rhodococcus equi isolates from domestic pig and wild boars (Sus scrofa) in Brazil. Res Vet Sci Oct 25 [Epub ahead of print].

    • Search Google Scholar
    • Export Citation
  • 16.

    Costa MM, Machado SA, Krewer CC, Fighera RA, Ilha MR, Graça DL, Vargas AP, Mattos-Guaraldi AL, 2006. Pathogenecity of Rhodococcus equi isolates from human, horse clinical and environment in immunodeficient mice. Pesqui Vet Bras 26: 167170.

    • Search Google Scholar
    • Export Citation
  • 17.

    Napoleão F, Damasco PV, Camello TC, Vale MD, Andrade AF, Hirata R Jr, Mattos-Guaraldi AL, 2005. Pyogenic liver abscess due to Rhodococcus equi in an immunocompetent host. J Clin Microbiol 43: 10021004.

    • Search Google Scholar
    • Export Citation

Author Notes

*Address correspondence to Márcio Garcia Ribeiro, Universidade Estadual Paulista Júlio de Mesquita Filho, Faculdade de Medicina Veterinária e Zootecnia, Departamento de Higiene Veterinária e Saúde Pública, CP 560, CEP 18618-970, Botucatu, Sao Paulo, Brazil. E-mail: mgribeiro@fmvz.unesp.br

Financial support: This study was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo, Brazil (grant no. 06/50406–0).

Authors' addresses: Márcio Garcia Ribeiro, Universidade Estadual Paulista Júlio de Mesquita Filho, Faculdade de Medicina Veterinária e Zootecnia, Departamento de Higiene Veterinária e Saúde Pública, CP 560, CEP 18618-970, Botucatu, Sao Paulo, Brazil, E-mail: mgribeiro@fmvz.unesp.br. Shinji Takai, Ryoko Ohno, and Hajime Okano, Department of Animal Hygiene, School of Veterinary Medicine and Animal Sciences, Kitasato University, Towada-Shi, Aomori, 034-8628, Japan, E-mail: takai@vmas.kitasato-u.ac.jp. Agueda Castagna de Vargas, Centro de Ciências Rurais, Departamento de Medicina Veterinária Preventiva, Universidade Federal de Santa Maria, CEP 97105-900, Santa Maria, Rio Grande do Sul, Brazil, E-mail: agueda.vargas@gmail.com. Ana Luiza Mattos-Guaraldi and Thereza Cristina Ferreira Camello, Faculdade de Ciências Médicas, Universidade do Estado do Rio de Janeiro, Avenida 28 de Setembro, 87, 3° Andar, CEP 20.551-030, Rio de Janeiro, Brazil, E-mails: aguaraldi@gmail.com and camello@unisys.com.br. Aristeu Vieira da Silva, Departamento de Ciências Biológicas, Universidade de Feira de Santana, Rodovia Transnordestina, s/n, CEP 44.036-900, Feira de Santana, Bahia, Brazil, E-mail: aristeuvsilva@gmail.com.

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