Drug susceptibility patterns of rapidly growing mycobacteria isolated from skin and soft tissue infections in Venezuela

European Journal of Clinical Microbiology & Infectious Diseases volume 39, pages433–441(2020)Cite this article

Abstract

To our knowledge, this is the first work on drug susceptibility patterns of rapid growing mycobacteria from Latin America. The susceptibility patterns for 14 antimicrobial agents of the three most important species that cause skin infections in Venezuela were determined as follows: 63 strains belonging to Mycobacterium abscessus group, 66 strains of the Mycobacterium fortuitum group, and 13 Mycobacterium chelonae strains. The M. abscessus group strains were resistant to most antibiotics tested while M. fortuitum strains were relatively susceptible to a large number of antibiotics. We demonstrate the presence of an inducible and truncated erm(41) gene in M. abscessus group, namely M. abscessus subsp. massiliense. We show the variations in susceptibility to antimicrobial agents within and between the mycobacterial species and compare our susceptibility patterns with those reported from other countries. We conclude that the identification of mycobacteria to the species level can guide the antibiotic treatment, but that it is always important to consider drug susceptibility testing when rapidly mycobacteria are isolated.

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References

  1. 1.

    Griffiifth D, Aksamit T, Brown-Elliot B, Catanzaro A, Daley C, Gordin F et al (2007) An official ATS/IDSA statement: diagnosis, treatment, and prevention of nontuberculous mycobacterial diseases. Am J Respir Crit Care Med 175(4):367–416. https://doi.org/10.1164/rccm.200604-571ST

    CAS  Article  Google Scholar 

  2. 2.

    Song J, Sohn J, Jeong H, Cheong H, Kim W, Kim M (2006) An outbreak of post-acupuncture cutaneous infection due to Mycobacterium abscessus. BMC Infect Dis 6(6):1471–2334. https://doi.org/10.1186/1471-2334-6-6

    Article  Google Scholar 

  3. 3.

    Tang P, Walsh S, Murray C, Alterman C, Varia M, Broukhanski G et al (2006) Outbreak of acupuncture-associated cutaneous Mycobacterium abscessus infections. J Cutan Med Surg 10(4):166–169. https://doi.org/10.2310/7750.2006.00041

    Article  PubMed  Google Scholar 

  4. 4.

    Furuya Y, Paéz A, Srinivasan A, Cooksey R, Augenbraun M, Baron M (2008) Outbreak of Mycobacterium abscessus wound infections among “Lipotourists” from the United States Who underwent abdominoplasty in the Dominican Republic. Clin Infect Dis 46(8):1181–1188. https://doi.org/10.1086/529191

    Article  PubMed  Google Scholar 

  5. 5.

    Galmés-Truyols A, Giménez-Duran J, Bosch-Isabel C, Nicolau-Riutort A, Vanrell-Berga J, Portell-Arbona M et al (2011) An outbreak of cutaneous infection due to Mycobacterium abscessus associated to mesotherapy. Enferm Infecc Microbiol Clin 29(7):510–514. https://doi.org/10.1016/j.eimc.2011.03.006

    Article  PubMed  Google Scholar 

  6. 6.

    Munayco C, Grijalva C, Culqui D, Bolarte J, Suárez-Ognio L, Quispe N et al (2008) Outbreak of persistent cutaneous abscesses due to Mycobacterium chelonae after mesotherapy sessions, Lima, Peru. Rev Saude Publica 42(1):146–149. https://doi.org/10.1590/S0034-89102008000100020

    Article  PubMed  Google Scholar 

  7. 7.

    Correa N, Cataño J, Mejía G, Realpe T, Orozco B, Estrada S et al (2010) Outbreak of mesotherapy-associated cutaneous infections caused by Mycobacterium chelonae in Colombia. Jpn J Infect Dis 63(2):143–145

    PubMed  Google Scholar 

  8. 8.

    Carbonne A, Brossier F, Arnaud I, Bougmiza I, Caumes E, Meningaud J et al (2009) Outbreak of nontuberculous mycobacterial subcutaneous infections related to multiple mesotherapy injections. J Clin Microbiol 47(6):1961–1964. https://doi.org/10.1128/JCM.00196-09

    Article  PubMed  PubMed Central  Google Scholar 

  9. 9.

    Ivan M, Dancer C, Koehler A, Hobby M, Lease C (2013) Mycobacterium chelonae abscesses associated with biomesotherapy, Australia, 2008. Emerg Infect Dis 19(9):1493–1495. https://doi.org/10.3201/eid1909.120898

    Article  PubMed Central  Google Scholar 

  10. 10.

    Quiñones C, Ramalle-Gómara E, Perucha M, Lezaun M, Fernández-Vilariño E, García-Morrás P et al (2010) An outbreak of Mycobacterium fortuitum cutaneous infection associated with mesotherapy. J Eur Acad Dermatol Venereol 24(5):604–606. https://doi.org/10.1111/j.1468-3083.2009.03461.x

    Article  PubMed  Google Scholar 

  11. 11.

    Macadam S, Mehling B, Fanning A, Dufton J, Kowalewska-Grochowska K, Lennox P et al (2007) Nontuberculous mycobacterial breast implant infections. Plast Reconstr Surg 119(1):337–344. https://doi.org/10.1097/01.prs.0000244924.61968.d2

    CAS  Article  PubMed  Google Scholar 

  12. 12.

    Murillo J, Torres J, Bofill L, Ríos-Fabra A, Irausquin E, Istúriz R et al (2000) Skin and wound infection by rapidly growing mycobacteria: an unexpected complication of liposuction and liposculture. Arch Dermatol 136:1347–1352. https://doi.org/10.1001/archderm.136.11.1347

    CAS  Article  PubMed  Google Scholar 

  13. 13.

    Piquero J, Casals V, Higuera E, Yakrus M, Sikes D, de Waard J (2004) Iatrogenic Mycobacterium simiae skin infection in an immunocompetent patient. Emerg Infect Dis 10(5):969–970. https://doi.org/10.3201/eid1005.030681

    Article  PubMed  PubMed Central  Google Scholar 

  14. 14.

    Cooksey R, de Waard J, Yakrus M, Rivera I, Chopite M, Toney S et al (2004) Mycobacterium cosmeticum sp. nov., a novel rapidly growing species isolated from a cosmetic infection and from a nail salon. Int J Syst Evol Microbiol 54(6):2385–2391. https://doi.org/10.1099/ijs.0.63238-0

    CAS  Article  PubMed  Google Scholar 

  15. 15.

    Rivera-Olivero I, Guevara A, Escalona A, Oliver M, Perez-Alfonzo R, Piquero J et al (2006) Infecciones en tejidos blandos por micobacterias no tuberculosas secundarias a mesoterapia ¿cuánto vale la belleza? Enferm Infecc Microbiol Clin 24(5):302–306. https://doi.org/10.1157/13089664

    Article  PubMed  Google Scholar 

  16. 16.

    Guevara-Patiño A, Sandoval de Mora M, Farreras A, Rivera-Olivero I, Fermin D, de Waard J (2010) Soft tissue infection due to Mycobacterium fortuitum following acupunture: a case report and review of the literature. J Infect Dev Ctries 4(8):521–525. https://doi.org/10.3855/jidc.718

    Article  PubMed  Google Scholar 

  17. 17.

    Da Mata-Jardín O, Hernández-Pérez R, Corrales H, Cardoso-Leao S, de Waard J (2010) Follow-up of an outbreak of Mycobacterium abscessus soft-tissue infection associated with mesotherapy in Venezuela. Enferm Infecc Microbiol Clin 28(9):596–501. https://doi.org/10.1016/j.eimc.2009.08.003

    Article  PubMed  Google Scholar 

  18. 18.

    Torres-Coy J, Carrera C, Rodríguez-Castillo B, Ramírez-Murga R, Ortiz-Cáceres W, Pérez-Alfonzo R et al (2017) Mycobacterium szulgai: an unusual cause of skin and soft tissue infection after breast augmentation. Int J Dermatol 56(6):e122–e124. https://doi.org/10.1111/ijd.13605

    Article  PubMed  Google Scholar 

  19. 19.

    Ruiz-Aragón J, García-Agudo L, Flores S, Rodríguez M, Marín P, García-Martos P (2007) Susceptibilty to antimicrobial agents of rapidly growing mycobacteria. Rev Esp Quimioterap 20(4):429–432

    Google Scholar 

  20. 20.

    García-Agudo L, García-Martos P, Jesús I, Rodríguez-Iglesias M (2009) Assesment of in vitro susceptibility to antimicrobials of rapidly growing mycobacteria by E-test. Rev Med Chil 137(7):912–917

    Article  Google Scholar 

  21. 21.

    Hatakeyama S, Ohama Y, Okazaki M, Nukui Y, Moriya K (2017) Antimicrobial susceptibility testing of rapidly growing mycobacteria isolated in Japan. BMC Infect Dis 17(1):197. https://doi.org/10.1186/s12879-017-2298-8

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  22. 22.

    Pang H, Li G, Zhao X, Liu H, Wan K, Yu P (2015) Drug susceptibility testing of 31 antimicrobial agents on rapidly growing mycobacteria isolates from China. Biomed Res Int 2015:419392. https://doi.org/10.1155/2015/419392

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  23. 23.

    Park S, Kim S, Park E, Kim H, Kwon O, Chang C et al (2008) In vitro antimicrobial susceptibility of Mycobacterium abscessus in Korea. J Korean Med Sci 23(1):49–52. https://doi.org/10.3346/jkms.2008.23.1.49

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  24. 24.

    Yang S, Hsueh P, Lai H, Teng L, Huang L, Chen J et al (2003) High prevalence of antimicrobial resistance in rapidly growing mycobacteria in Taiwan. Antimicrob Agents Chemother 47(6):1958–1962. https://doi.org/10.1128/AAC.47.6.1958-1962.2003

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  25. 25.

    Huang Y, Liu M, Shen G, Lin C, Kao C, Liu P et al (2010) Clinical outcome of Mycobacterium abscessus infection and antimicrobial susceptibility testing. J Microbiol Immunol Infect 43(5):401–406. https://doi.org/10.1016/S1684-1182(10)60063-1

    CAS  Article  PubMed  Google Scholar 

  26. 26.

    Lee S, Kim J, Jeong J, Park Y, Bai G, Lee E et al (2007) Evaluation of the broth microdilution method using 2,3-diphenyl-5-thienyl-(2)-tetrazolium chloride for rapidly growing mycobacteria susceptibility testing. J Korean Med 22(5):784–790. https://doi.org/10.3346/jkms.2007.22.5.784

    CAS  Article  Google Scholar 

  27. 27.

    Heidarieh P, Mirsaeidi M, Hashemzadeh M, Feizabadi M, Bostanabad S, Nobar M et al (2016) In vitro antimicrobial susceptibility of nontuberculous mycobacteria in Iran. Microb Drug Resist 22(2):172–178. https://doi.org/10.1089/mdr.2015.0134

    CAS  Article  PubMed  Google Scholar 

  28. 28.

    Tang S, Lye D, Jureen R, Sng L, Hsu L (2015) Rapidly growing mycobacteria in Singapore, 2006-2011. Clin Microbiol Infect 21(3):236–241. https://doi.org/10.1016/j.cmi.2014.10.018

    CAS  Article  PubMed  Google Scholar 

  29. 29.

    Lee S, Yoo H, Kim S, Koh W, Kim C, Park Y et al (2014) The drug resistance profile of Mycobacterium abscessus group strains from Korea. Ann Lab Med 34(1):31–37. https://doi.org/10.3343/alm.2014.34.1.31

    Article  PubMed  Google Scholar 

  30. 30.

    Wallace RJ, Brown-Elliott B, Ward S, Crist C, Mann L, Wilson R (2001) Activities of linezolid against rapidly growing mycobacteria. Antimicrob Agents Chemother 45(3):764–767. https://doi.org/10.1128/AAC.45.3.764-767.2001

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  31. 31.

    Telenti A, Marchesi F, Balz M, Bally F, Böttger E, Bodmer T (1993) Rapid identification of mycobacteria to the species level by polymerase chain reaction and restriction enzyme analysis. J Clin Microbiol 31(2):175–178

    CAS  Article  Google Scholar 

  32. 32.

    da Costa A, Lopes M, Furlaneto I, de Sousa M, Lima K (2010) Molecular identification of nontuberculous mycobacteria isolates in a Brazilian mycobacteria reference laboratory. Diagn Microbiol Infect Dis 68(4):390–394. https://doi.org/10.1016/j.diagmicrobio.2010.07.019

    CAS  Article  PubMed  Google Scholar 

  33. 33.

    Nash K, Brown-Elliott B, Wallace RJ (2009) A novel gene, erm(41), confers inducible macrolide resistance to clinical isolates of Mycobacterium abscessus but is absent from Mycobacterium chelonae. Antimicrob Agents Chemother 53(4):1367–1376. https://doi.org/10.1128/AAC.01275-08

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  34. 34.

    Wallace RJ, Brown-Elliott B, Wilson R, Mann L, Hall L, Zhang Y et al (2004) Clinical and laboratory features of Mycobacterium porcinum. J Clin Microbiol 42(12):5689–5697. https://doi.org/10.1128/JCM.42.12.5689-5697.2004

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  35. 35.

    Woods GL, Browm-Elliot BA, Conville PS et al (2011) Susceptibility Testing of Mycobacteria, Nocardiae, and other aerobic actinomycetes; Approved Standard- Second edition, CLSI document M24-A2. Clinical and Laboratory Standards Institute (CLSI), Wayne ISBN 1-56238-746-4, ISSN 0273-3099

    Google Scholar 

  36. 36.

    Wallace RJ, Brown-Elliot B, Crist C, Mann L, Wilson R (2002) Comparison of the in vitro activity of the glycylcline tigecycline (formerly GAR-936) with those of tetracycline, minocycline, and doxycycline against isolates of nontuberculous mycobacteria. Antimicrob Agents Chemother 46(10):3164–3167. https://doi.org/10.1128/AAC.46.10.3164-3167.2002

    CAS  Article  PubMed  Google Scholar 

  37. 37.

    Huang C, Wu M, Chen H, Huang W (2018) In vitro activity of aminoglycosides, clofazimine, d-cycloserine and dapsone against 83 Mycobacterium avium complex clinical isolates. J Microbiol Immunol Infect 51(5):636–643. https://doi.org/10.1016/j.jmii.2017.05.001

    CAS  Article  PubMed  Google Scholar 

  38. 38.

    Kim H, Kim B, Kook Y, Yun Y, Shin J, Kim B et al (2010) Mycobacterium massiliense is differentiated from Mycobacterium abscessus and Mycobacterium bolletii by erythromycin ribosome methyltransferase gene (erm) and clarithromycin susceptibility patterns. Microbiol Immunol 54(6):347–353. https://doi.org/10.1111/j.1348-0421.2010.00221.x

    CAS  Article  PubMed  Google Scholar 

  39. 39.

    Bastian S, Veziris N, Roux A, Brossier F, Gaillard J, Jarlier V et al (2011) Assessment of clarithromycin susceptibility in strains belonging to the Mycobacteium abscessus group by erm(41) and rrl sequencing. Antimicrob Agents Chemother 55(2):775–781. https://doi.org/10.1128/AAC.00861-10

    CAS  Article  PubMed  Google Scholar 

  40. 40.

    De Groote M, Huitt G (2006) Infections due to rapidly growing mycobacteria. Clin Infect Dis 42(12):1756–1763. https://doi.org/10.1086/504381

    Article  PubMed  Google Scholar 

  41. 41.

    Hwang T, Dotsenko S, Jafarov A, Weyer K, Falzon D, Lunte K et al (2014) Safety and availability of clofazimine in the treatment of multidrug and extensively drug-resisitant tuberculosis: analysis of published guidance and meta-analysis of cohort studies. BMJ Open 4(1):e004143. https://doi.org/10.1136/bmjopen-2013-004143

    Article  PubMed  PubMed Central  Google Scholar 

  42. 42.

    Wallace RJ, Dukart G, Brown-Elliott B, Griffith D, Scerpella E, Marshall B (2014) Clinical experience in 52 patients witth tigecycline-containing regimens for salvage treatment of Mycobacterium abscessus and Mycobacterium chelonae infections. J Antimicrob Chemother 69(7):1945–1953. https://doi.org/10.1093/jac/dku062

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  43. 43.

    Nie W, Duan H, Huang H, Lu Y, Chu N (2015) Species identification and clarithromycin susceptibility testing of 278 clinical nontuberculous mycobacteria isolates. Biomed Res Int 2015:506598. https://doi.org/10.1155/2015/506598

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  44. 44.

    Christianson S, Grierson W, Kein D, Tyler A, Wolfe J, Sharma M (2016) Time to detection of inducible macrolide resistance in Mycobacterium abscessus subspecies and its association with the Erm(41) sequevar. PLoS One 11(8):e0158723. https://doi.org/10.1371/journal.pone.0158723

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  45. 45.

    Li B, Yang S, Chu H, Zhang Z, Liu W, Luo L et al (2017) Relationship between antibiotic susceptibility and genotype in Mycobacterium abscessus clinical isolates. Front Microbiol 14(8):1739. https://doi.org/10.3389/fmicb.2017.01739

    Article  Google Scholar 

  46. 46.

    Rubio M, March F, Garrigó M, Moreno C, Español M, Coll P (2015) Inducible and acquired clarithromycin resistance in the Mycobacterium abscessus complex. PLoS One 10(10):e0140166. https://doi.org/10.1371/journal.pone.0140166

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  47. 47.

    Hanson K, Slechta E, Muir H, Barker A (2014) Rapid molecular detection of inducible macrolide resistance in Mycobacterium chelonae and M. abscessus strains: a replacement for 14 day susceptibility testing? J Clin Microbiol 52(5):1705–1707. https://doi.org/10.1128/JCM.03464-13

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  48. 48.

    Esteban J, Martín-de-Hijas N, García-Almeida D, Bodas-Sánchez A, Gadea I, Fernández-Roblas R (2009) Prevalence of erm methylase genes in clinical isolates of non-pigmented, rapidly growing mycobacteria. Clin Microbiol Infect 15(10):919–923. https://doi.org/10.1111/j.1469-0691.2009.02757.x

    CAS  Article  PubMed  Google Scholar 

  49. 49.

    Ali S, Khan F, Fisher M (2007) Catheter-related bloodstream infection caused by Mycobacterium mageritense. J Clin Microbiol 45(1):273. https://doi.org/10.1128/JCM.01224-06

    Article  PubMed  Google Scholar 

  50. 50.

    Gira A, Reisenauer A, Hammock L, Nadiminti U, Macy J, Reeves A et al (2004) Furunculosis due to Mycobacterium mageritense associated with footbaths at a nail salon. J Clin Microbiol 42(4):1813–1817. https://doi.org/10.1128/JCM.42.4.1813-1817.2004

    Article  PubMed  PubMed Central  Google Scholar 

  51. 51.

    Wallace RJ, Brown-Elliot B, Hall L, Roberts G, Wilson R, Mann L et al (2002) Clinical and laboratory features of Mycobacterium mageritense. J Clin Microbiol 40(8):2930–2935. https://doi.org/10.1128/JCM.40.8.2930-2935.2002

    CAS  Article  PubMed  Google Scholar 

  52. 52.

    Fernández-Roblas R, Martín-de-Hijas N, Fernández-Martínez A, García-Almeida D, Gadea I, Esteban J (2008) In vitro activities of tigecycline and 10 other antimicrobials against nonpigmented rapidly growing mycobacteria. Antimicrob Agents Chemother 52(11):4184–4186. https://doi.org/10.1128/AAC.00695-08

    CAS  Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We acknowledge the significant contributions of laboratory staff of “Diagnósticos Especiales” at Instituto Nacional de Higiene “Rafael Rangel” and the laboratory staff of Laboratory of Tuberculosis at Instituto de Biomedicina. We also acknowledge to special contributions of María Fernanda González Barrios, Margarita Monzón García and Ismar Rivera Olivero.

Funding

This work was financially supported by the research program of the research coordination of “Gerencia de Docencia e Investigación” and “Gerencia de Diagnóstico y Vigilancia” of Instituto Nacional de Higiene “Rafael Rangel”, the FONACIT Project Number 2012001149 and FUNDAIM (Fundacion para la Investigacion en Micobacterias).

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Affiliations

  1. Postgrado de Biología, Universidad Simón Bolívar, Caracas, Venezuela

    Omaira Da Mata-Jardín & Margarita Rodríguez

  2. Laboratorio de Diagnósticos Especiales, Departamento de Bacteriología, Instituto Nacional de Higiene “Rafael Rangel”, Caracas, Venezuela

    Omaira Da Mata-Jardín, Alejandro Angulo & Sandra Fernández-Figueiras

  3. Departamento de Tuberculosis, Servicio Autónomo Instituto de Biomedicina “Dr. Jacinto Convit”, Universidad Central de Venezuela, Caracas, Venezuela

    Jacobus H de Waard

  4. One Health Research Group, Facultad de Ciencias de la Salud, Universidad de Las Américas, Quito, Ecuador

    Jacobus H de Waard

Authors
  1. Omaira Da Mata-Jardín
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  2. Alejandro Angulo
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  3. Margarita Rodríguez
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  4. Sandra Fernández-Figueiras
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  5. Jacobus H de Waard
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Contributions

Omaira Da Mata-Jardín was responsible for the laboratory experiments, the analysis, the interpretation of the results and drafted initial manuscript. This manuscript is part of her PhD thesis presented at the “Universidad Simón Bolívar” in Caracas, Venezuela. Alejandro Angulo participated in carrying out laboratory techniques. Margarita Rodríguez, Sandra Fernández-Figueiras and de Jacobus H Waard conceived, designed and supervised the study and provided significant guidance on the development of the manuscript.

Corresponding author

Correspondence to Omaira Da Mata-Jardín.

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Ethical approval and Informed consent

The strains in this study were isolated for routine diagnosis purpose in the years 2007 and 2012 in the “Tuberculosis Laboratory” at Insituto de Biomedicina “Dr. Jacinto Convit” and Instituto Nacional de Higiene “Rafael Rangel.” For this study, bacterial strains were coded, handled blindly without the possibility to disclose patient’s identity, identified to species level, and submitted for drug resistance testing. No clinical or personal data of the patients have been used for this publication.

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Da Mata-Jardín, O., Angulo, A., Rodríguez, M. et al. Drug susceptibility patterns of rapidly growing mycobacteria isolated from skin and soft tissue infections in Venezuela. Eur J Clin Microbiol Infect Dis 39, 433–441 (2020). https://doi.org/10.1007/s10096-019-03740-7

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Keywords

  • Rapidly growing mycobacteria
  • Venezuela
  • Antimicrobial susceptibility
  • Mycobacterium abscessus
  • Mycobacterium chelonae
  • Mycobacterium fortuitum