Skip to main content

Advertisement

SpringerLink
Log in

Molecular identification and antimicrobial resistance pattern of Nocardia isolated from 14 diseased dogs and cats

  • Veterinary Microbiology - Research Paper
  • Published:
Brazilian Journal of Microbiology Aims and scope Submit manuscript

Abstract

Nocardia are ubiquitous, saprophytic and opportunistic bacteria. They cause a set of pyogenic clinical infections in animals and humans, particularly immunocompromised patients, mostly affecting the skin and respiratory tract, with refractoriness to conventional therapy. The most descriptions of nocardial infections in companion animals involve case reports, and there are scarce case series studies focused on canine and feline nocardiosis in which diagnosis has been based on molecular techniques. We investigated epidemiological aspects, clinical findings, in vitro susceptibility profile, and molecular identification of Nocardia using PCR-based method targeted 16S rRNA gene in twelve dogs and two cats. Among dogs were observed cutaneous lesions (8/12 = 67%), pneumonia (3/12 = 25%), and encephalitis (2/12 = 17%), whereas cats developed cutaneous lesions and osteomyelitis. Nocardia and canine morbillivirus coinfection was described in six dogs (6/12 = 50%). A high mortality rate (6/8 = 75%) was seen among dogs. Three dogs (3/4 = 75%) and one cat (1/2 = 50%) with systemic signs (pneumonia, encephalitis, osteomyelitis), and 83% (5/6) of dogs with a history of concomitant morbillivirus infection died. N. nova (5/12 = 42%), N. cyriacigeorgica (3/12 = 25%), N. farcinica (2/12 = 17%), N. veterana (1/12 = 8%), and N. asteroides (1/12 = 8%) species were identified in dogs, whereas N. africana and N. veterana in cats. Among the isolates from dogs, cefuroxime (12/12 = 100%), amikacin (10/12 = 83%), gentamycin (10/12 = 83%), and imipenem (10/12 = 83%) were the most effective antimicrobials, whereas cefuroxime, cephalexin, amoxicillin/clavulanic acid, imipenem, and gentamycin were efficient against isolates from cats. Multidrug resistance was observed in 36% (5/14) of isolates. We describe a variety of Nocardia species infecting dogs and cats, multidrug-resistant ones, and a high mortality rate, highlighting a poor prognosis of nocardiosis in companion animals, particularly among animals systemically compromised or coinfected by canine morbillivirus. Our study contributes to species identification, in vitro antimicrobial susceptibility profile, clinical-epidemiological aspects, and outcome of natural Nocardia-acquired infections in dogs and cats.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Data Availability

Complete epidemiological datas was presented in our tables, additional results of antimicrobial susceptibility results are available under request, and 16S rDNA sequences are available in NCBI public databank.

References

  1. Conville PS, Brown-Elliot BA, Smith T, Zelazny AM (2018) The complexities of Nocardia taxonomy and identification. J Clin Microbiol 56(e01419–17):1–10

    Google Scholar 

  2. Quinn PJ, Markey BK, Leonard FC, Fitzpatrick ES, Fanning S, Hartigan PJ (2011) Veterinary microbiology and microbial disease, 2nd edn. Wiley-Blackwell, Chichester, West Sussex, UK

    Google Scholar 

  3. Beaman BL, Beaman L (1994) Nocardia species: host-parasite relationships. Clin Microbiol Rev 7:213–264

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Ribeiro MG (2021) Nocardiosis in Animals. The Merck Veterinary Manual, 12th ed. Rahway, New Jersey, USA: Merck Publishing Group (on line version: https://www.merckvetmanual.com/generalized-conditions/nocardiosis/nocardiosisin-animals?autoredirectid=16649). Accessed 24 Sept 2021

  5. Xiao M, Pang L, Chen SC, Fan X, Zhang L, Li HX, Hou X, Cheng JW, Kong F, Zhao YP, Xu YC (2016) Accurate identification of common pathogenic Nocardia species: evaluation of a multilocus sequence analysis platform and Matrix-Assisted Laser Desorption Ionization-Time of Flight Mass Spectrometry. PLoS ONE 11:e0147487

    Article  PubMed  PubMed Central  Google Scholar 

  6. Duggal DS, Chug TD (2020) Nocardiosis: a neglected disease. Med Princ Pract 29:514–523

    Article  PubMed  PubMed Central  Google Scholar 

  7. Mehta HH, Shamoo Y (2020) Pathogenic Nocardia: a diverse genus of emerging pathogens or just poorly recognized? PLoS Pathog 16(e1008280):1–7

    Google Scholar 

  8. Genus Nocardia (2021) Available from: https://lpsn.dsmz.de/genus/nocardia. Accessed 24 Sept 2021

  9. Malik R, Krockenberger MB, Obrien CR, White JD, Foster D, Tisdall PLC, Gunew M, Carr PD, Bodell L, McCowan C, Howe J, Oakley C, Griffin C, Wigney DI, Martin P, Norris J, Hunt G, Mitchell DH, Gilpin C (2006) Nocardia infections in cats: a retrospective multi-institutional study of 17 cases. Australian Veterinary J 84:235–245

    Article  CAS  Google Scholar 

  10. MacNeill AL, Steeil JC, Dossin O, Hoien-Dalen PS, Maddox CW (2010) Disseminated nocardiosis caused by Nocardia abscessus in a dog. Veterinary Clin Pathol 39:381–385

    Article  Google Scholar 

  11. Condas LAZ, Ribeiro MG, Vargas AC, Yazawa K, Gonoi T, Matsuzama T, Langoni H, Melville PA, Kastelic JP, Barkema HW (2013) Molecular identification and antimicrobial susceptibility of Nocardia spp. isolated from bovine mastitis in Brazil. Vet Microbiol 167:708–712

    Article  CAS  PubMed  Google Scholar 

  12. Hilligas J, Wie EV, Barr J, Russell KE, Perry AL, Weeks BR, Zhang S (2014) Vertebral osteomyelitis and multiple cutaneous lesions in a dog caused by Nocardia pseudobrasiliensis. J Vet Intern Med 28:1621–1625

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Eroksuz Y, Gursoy NF, Karapinar T, Karabulut B, Incili CA, Yerlikaya Z, Toraman ZA, Timurkan MO, Eroksuz H (2017) Systemic nocardiosis in a dog caused by Nocardia cyriacigeorgica. BMC Vet Res 13:30

    Article  PubMed  PubMed Central  Google Scholar 

  14. Yaemsiri S, Sykes JE (2018) Successful treatment of disseminated nocardiosis caused by Nocardia veterana in a dog. J Vet Intern Med 32:418–422

    Article  CAS  PubMed  Google Scholar 

  15. Ribeiro AIT, Burema MC, Borges APS, Bruno VCM, Néspoli PEB, Colodel EM, Gouvêa FHF, Dutra V, Nakazato L, Ribeiro MG, Aguiar DM (2020) Pyogranulomatous pleuropneumonia caused by Nocardia asiatica in a dog coinfected with canine morbillivirus (canine distemper virus). Veterinary Medicine and Science 6:25–31

    Article  PubMed  Google Scholar 

  16. Ramos-Vara JA, Wu CC, Lin TL, Miller MA (2007) Nocardia tenerifensis genome identification in a cutaneous granuloma of a cat. J Vet Diagn Invest 19:577–580

    Article  PubMed  Google Scholar 

  17. Farias MR, Werner J, Ribeiro MG, Rodigheri SM, Cavalcante CZ, Chi KD, Condas LAZ, Gonoi T, Matsuzama T, Yazama K (2012) Uncommon mandibular osteomyelitis in a cat caused by Nocardia africana. BMC Vet Res 8:239

    Article  PubMed  PubMed Central  Google Scholar 

  18. Silkworth A, Cavanaugh R, Bolfa P, Becker AAMJ (2019) Cutaneous pyogranulomas associated with Nocardia jiangxiensis in a cat from the Eastern Caribbean. Tropical Medicine and Infectious Disease 4:130

    Article  PubMed  PubMed Central  Google Scholar 

  19. Sykes JE (2012) Actinomycetes and Nocardiosis. In: Greene CE (ed) Infectious diseases of the dog and cat, 4th. Elsevier Saunders, St. Louis, p 484–494

  20. Martíbez-Barricarte R (2020) Isolated nocardiosis, and unrecognized primary immunodeficiency? Front Microbiol 11:1–17

    Google Scholar 

  21. Brown-Elliott BA, Brown JM, Conville PS, Wallace RJ (2006) Clinical and laboratory features of the Nocardia spp. based on current molecular taxonomy. Clin Microbiol Rev 19:259–282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Clinical and Laboratory Standards Institute-CLSI (2020) Performance standards for antimicrobial disk and dilution susceptibility test for bacteria isolated from animals (CLSI VET 015), 5th edn. Wayne, p 25

  23. Ambaye A, Kohner PC, Wollan PC, Roberts KL, Roberts GD, Cockerill FR (1997) Comparison of agar dilution, broth microdilution, disk diffusion, E-test, and BACTEC radiometric methods for antimicrobial susceptibility testing of clinical isolates of the Nocardia asteroides complex. J Clin Microbiol 35:847–852

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, Harbarth S, Hindler JF, Kahlmeter G, Liljequist BO, Paterson DL, Rice LB, Stelling J, Struelens MJ, Vatopoulos A, Weber JT, Monnet DL (2012) Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 18:268–81

    Article  CAS  PubMed  Google Scholar 

  25. Kageyama A, Poonwan N, Yazawa K, Mikami Y, Nishimura K (2004) Nocardia asiatica sp. nov., isolated from patients with nocardiosis in Japan and clinical specimens from Thailand. Int J Syst Evol Microbiol 54:125–130

    Article  CAS  PubMed  Google Scholar 

  26. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  27. Beaman BL, Sugar AM (1983) Nocardia in naturally acquired and experimental infections in animals. J Hygiene 91:303–419

    Article  Google Scholar 

  28. Luque R, Astorga C, Tarradas B (2002) Nocardia otitidiscaviarum infection in a cat. Veterinary Record 151:488

    CAS  PubMed  Google Scholar 

  29. Ajello L, Walker WW, Dungworth DL, Brumfield GL (1961) Isolation of Nocardia brasiliensis from a cat with a review of its prevalence and geographic distribution. J Am Veterinary Med Assoc 138:370–376

    CAS  Google Scholar 

  30. Ribeiro MG, Salerno T, Mattos-Guaraldi ALD, Camello TCF, Langoni H, Siqueira AK, Paes AC, Fernandes MC, Lara GHB (2008) Nocardiosis: an overview and additional report of 28 cases in cattle and dogs. Rev Inst Med Trop Sao Paulo 50:177–185

    Article  PubMed  Google Scholar 

Download references

Funding

This study is funded by the São Paulo Research Foundation (Fapesp, Protocols 2008/56037–1 and 2009/53494–5). Márcio Garcia Ribeiro received support for research productivity fellowship (PQ-1D) from the National Council for Scientific and Technological Development (CNPq, protocol 310345/2020–0), Brazil.

Author information

Authors and Affiliations

  1. Faculdade de Medicina Veterinária, UniBrasil Centro Universitário, Curitiba, PR, Brasil

    Larissa Anuska Zeni Condas & Guilherme Borges Bond

  2. Faculdade de Medicina Veterinária e Zootecnia, Departamento de Produção Animal e Medicina Veterinária Preventiva, UNESP, Botucatu, SP, Brasil

    Larissa Anuska Zeni Condas, Amanda Keller Siqueira, Tatiana Salerno & Márcio Garcia Ribeiro

  3. Faculdade de Medicina Veterinária, Pontifícia Universidade Católica do Paraná, Curitiba, PR, Brasil

    Marconi Rodrigues de Farias & Kung Darh Chi

  4. Laboratório de Histopatologia Veterinária Werner & Werner, Curitiba, Brasil

    Juliana Werner

  5. Faculdade de Medicina Veterinária, Universidade Federal de Santa Maria, Santa Maria, RS, Brasil

    Agueda Castagna de Vargas

  6. Medical Mycology Research Center, Chiba University, Chiba, Japan

    Tohru Gonoi

  7. University of Nagasaki, Nagasaki, Japan

    Tetsuhiro Matsuzawa

Authors
  1. Larissa Anuska Zeni Condas
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marconi Rodrigues de Farias
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Amanda Keller Siqueira
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tatiana Salerno
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kung Darh Chi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Juliana Werner
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Agueda Castagna de Vargas
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Guilherme Borges Bond
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Tohru Gonoi
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Tetsuhiro Matsuzawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Márcio Garcia Ribeiro
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

The authors contributed to the study review, data collection, and material preparation. The conception of the study was elaborated by Dr. Marcio Garcia Ribeiro. Material preparation and data collection were performed by Marcio Garcia Ribeiro, Agueda Castagna de Vargas, Marconi Rodrigues de Farias, Kung Dahr Chi, and Larissa Anuska Zeni Condas. Laboratorial molecular identification, antimicrobial pattern, histopathological, and description were analyzed by Katsukiyo Yazawa, Tetsuhiro Matsuzawa, Tohru Gonoi, Amanda Keller Siqueira, Tatiana Salerno, Juliana Werner, and Larissa Anuska Zeni Condas. All authors contributed to the written manuscript, with complementary review and editing of Guilherme Borges Bond. All authors read and approved the manuscript.

Corresponding author

Correspondence to Larissa Anuska Zeni Condas.

Ethics declarations

Ethics approval

This study was conducted under the Ethics Committee on Animal Use (CEUA) guidelines of the School of Veterinary Medicine and Animal Sciences, São Paulo University-UNESP, Botucatu, SP, Brazil (protocol number 169/2014).

Consent to participate/Consent for publication

All authors of this paper are aware of the study developed, participated in thesis review, and contributed to the conclusions obtained in the study, further agreeing to its publication.

Competing interests

The authors declare no competing interests.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Responsible Editor: Mariana X Byndloss

Place where the study was developed: Departmento de Produção Animal e Medicina Veterinária Preventiva, UNESP, Botucatu, SP, Brasil.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Condas, L.A.Z., de Farias, M.R., Siqueira, A.K. et al. Molecular identification and antimicrobial resistance pattern of Nocardia isolated from 14 diseased dogs and cats. Braz J Microbiol 54, 1287–1294 (2023). https://doi.org/10.1007/s42770-023-00968-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42770-023-00968-6

Keywords

Search

Navigation