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Healthcare-Associated Outbreaks and Pseudo-Outbreaks of Nontuberculous Mycobacteria

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Nontuberculous Mycobacterial Disease

Part of the book series: Respiratory Medicine ((RM))

Abstract

Outbreaks and pseudo-outbreaks of nontuberculous mycobacteria (NTM) have been increasingly reported worldwide. NTM thrive throughout the environment. They are commonly found in municipal and hospital water systems including hot water and chlorinated systems and cause various types of opportunistic infections in both immunocompetent and immunocompromised individuals. Most of these infectious outbreaks have exposure to water or water-based solutions as the common denominator. This chapter reviews many of the published NTM outbreaks and pseudo-outbreaks and seeks to provide guidance to the clinician and laboratory on when to suspect an NTM outbreak or pseudo-outbreak. Surveillance and control measures to prevent and mitigate these outbreaks are also described.

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References

  1. Wallace RJ Jr, Brown BA, Griffith DE. Nosocomial outbreaks/pseudo-outbreaks caused by nontuberculous mycobacteria. Annu Rev Microbiol. 1998;52:453–90.

    CAS  PubMed  Google Scholar 

  2. Brown-Elliott BA, Philley JV. Rapidly growing mycobacteria. Microbiol Spectr. 2017;5:TNM17-0027-2016.

    Google Scholar 

  3. Covert TC, Rodgers MR, Reyes AL, Stelma GN Jr. Occurrence of nontuberculous mycobacteria in environmental samples. Appl Environ Microbiol. 1999;65:2492–6.

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Williams MM, Chen T-H, Keane T, Toney N, Toney S, Armbruster CR, Butler WR, Arduino MJ. Point-of-use membrane filtration and hyperchlorination to prevent patient exposure to rapidly growing mycobacteria in the potable water supply of a skilled nursing facility. Infect Control Hosp Epidemiol. 2011;32:837–44.

    PubMed  Google Scholar 

  5. van Ingen J, Boeree MJ, Dekhuijzen PNR, van Soolingen D. Environmental sources of rapid growing nontuberculous mycobacteria causing disease in humans. Clin Microbiol Infect. 2009;15:888–93.

    PubMed  Google Scholar 

  6. Wilson RW, Steingrube VA, Böttger EC, Springer B, Brown-Elliott BA, Vincent V, Jost KC Jr, Zhang Y, Garcia MJ, Chiu SH, Onyi GO, Rossmoore H, Nash DR, Wallace RJ Jr. Mycobacterium immunogenum sp. nov., a novel species related to Mycobacterium abscessus and associated with clinical disease, pseudo-outbreaks, and contaminated metalworking fluids: an international cooperative study on mycobacterial taxonomy. Int J Syst Evol Microbiol. 2001;51:1751–64.

    CAS  PubMed  Google Scholar 

  7. Cortesia C, Lopez GJ, de Waard JH, Takiff HE. The use of quaternary ammonium disinfectants selects for persisters at high frequency from some species of non-tuberculous mycobacteria and may be associated with outbreaks of soft tissue infections. J Antimicrob Chemother. 2010;65:2574–81.

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Greendyke R, Byrd TF. Differential antibiotics susceptibility of Mycobacterium abscessus variants in biofilms and macrophages compared to that of planktonic bacteria. Antimicrob Agents Chemother. 2008;52:2019–26.

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Howard ST, Rhoades E, Recht J, Pang X, Alsup A, Kolter R, Lyons CR, Byrd TF. Spontaneous reversion of Mycobacterium abscessus from a smooth to a rough morphotype is associated with reduced expression of glycopeptidolipid and reacquisition of an invasive phenotype. Microbiology. 2006;152:1581–90.

    CAS  PubMed  Google Scholar 

  10. Schulze-Röbbecke R, Janning B, Fischeder R. Occurrence of mycobacteria in biofilm samples. Tuberc Lung Dis. 1992;73:141–4.

    Google Scholar 

  11. Sood G, Parrish N. Outbreaks of nontuberculous mycobacteria. Curr Opin Infect Dis. 2017;30:404–9.

    PubMed  Google Scholar 

  12. Galassi L, Donato R, Tortoli E, Burrini D, Santianni D, Dei R. Nontuberculous mycobacteria in hospital water systems: application of HPLC for identification of environmental mycobacteria. J Water Health. 2003;1:133–9.

    CAS  PubMed  Google Scholar 

  13. Brown-Elliott BA, Wallace RJ Jr. Clinical and taxonomic status of pathogenic nonpigmented or late-pigmenting rapidly growing mycobacteria. Clin Microbiol Rev. 2002;15:716–46.

    PubMed  PubMed Central  Google Scholar 

  14. Eid AJ, Bergari F, Sia IG, Wengenack NL, Osmon DR, Razonable RR. Prosthetic joint infection due to rapidly growing mycobacteria: report of 8 cases and review of the literature. Clin Infect Dis. 2007;45:687–94.

    PubMed  Google Scholar 

  15. Holmes GP, Bond GB, Fader RC, Fulcher SF. A cluster of cases of Mycobacterium szulgai keratitis that occurred after laser-assisted in situ keratomileusis. Clin Infect Dis. 2002;34:1039–46.

    PubMed  Google Scholar 

  16. Sampaio JL, Chimara E, Ferrazoli L, da Silva Telles MA, Del Guercio VM, Jericó ZV, Miyashiro K, Fortaleza CM, Padoveze MC, Leão SC. Application of four molecular typing methods for analysis of Mycobacterium fortuitum group strains causing post-mammaplasty infections. Clin Microbiol Infect. 2006;12:142–9.

    CAS  PubMed  Google Scholar 

  17. Edens C, Liebich L, Halpin AL, Moulton-Meissner H, Eitniear S, Zgodzinski E, Vasko L, Grossman D, Perz JF, Mohr MC. Mycobacterium chelonae eye infections associated with humidifier use in an outpatient LASIK clinic – Ohio. Morb Mortal Wkly Rep. 2015;64:1177.

    Google Scholar 

  18. Ashraf MS, Swinker M, Augustino KL, Nobles D, Knupp C, Liles D, Ramsey KM. Outbreak of Mycobacterium mucogenicum bloodstream infections among patients with sickle cell disease in an outpatient setting. Infect Control Hosp Epidemiol. 2012;33:1132–6.

    PubMed  Google Scholar 

  19. Shachor-Meyouhas Y, Sprecher H, Eluk O, Ben-Barak A, Kassis I. An outbreak of Mycobacterium mucogenicum bacteremia in pediatric hematology-oncology patients. Pediatr Infect Dis J. 2011;30:30–2.

    PubMed  Google Scholar 

  20. Tagashira Y, Kozai Y, Yamasa H, Sakurada M, Kashiyama T, Honda H. A cluster of central line-associated bloodstream infections due to rapidly growing nontuberculous mycobacteria in patients with hematologic disorders at a Japanese tertiary care center: an outbreak investigation and review of the literature. Infect Control Hosp Epidemiol. 2015;36:76–80.

    PubMed  Google Scholar 

  21. Laussucq S, Baltch AL, Smith RP, Smithwick RW, Davis BJ, Desjardin EK, Silcox VA, Spellacy AB, Zeimis RT, Gruft HM, Good RC, Cohen ML. Nosocomial Mycobacterium fortuitum colonization from a contaminated ice machine. Am Rev Respir Dis. 1988;138:891–4.

    CAS  PubMed  Google Scholar 

  22. Lévy-Frébault V, David HL. Mycobacterium kansasii: drinking water contaminant of a hospital. Rev Epidemiol Sante Publique. 1983;31:11–20.

    PubMed  Google Scholar 

  23. Marshall HM, Carter R, Torbey MJ, Minion S, Tolson C, Sidjabat HE, Huygens F, Hargreaves M, Thomson RM. Mycobacterium lentiflavum in drinking water supplies, Australia. Emerg Infect Dis. 2011;17:395–402.

    PubMed  PubMed Central  Google Scholar 

  24. Kanamori H, Weber DJ, Rutala WA. Healthcare outbreaks associated with a water reservoir and infection prevention strategies. Clin Infect Dis. 2016;62:1423–35.

    PubMed  Google Scholar 

  25. Villanueva A, Calderon RV, Vargas BA, Ruiz F, Aguero S, Zhang Y, Brown BA, Wallace RJ Jr. Report on an outbreak of post-injection abscesses due to Mycobacterium abscessus, including management with surgery and clarithromycin therapy and comparison of strains by random amplified polymorphic DNA polymerase chain reaction. Clin Infect Dis. 1997;24:1147–53.

    CAS  PubMed  Google Scholar 

  26. Zhibang Y, Bixia Z, Qishan L, Lihao C, Xiangquan L, Huaping L. Large-scale outbreak of infection with Mycobacterium chelonae subsp. abscessus after penicillin injection. J Clin Microbiol. 2002;40:2626–8.

    PubMed  PubMed Central  Google Scholar 

  27. Kim H-Y, Yun Y-J, Park CG, Lee DH, Cho YK, Park BJ, Joo S-I, Kim E-C, Hur YJ, Kim B-J, Kook YH. Outbreak of Mycobacterium massiliense infection associated with intramuscular injections. J Clin Microbiol. 2007;45:3127–30.

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Tiwari TS, Ray B, Jost KC Jr, Rathod MK, Zhang Y, Brown-Elliott BA, Hendricks K, Wallace RJ Jr. Forty years of disinfectant failure: outbreak of postinjection Mycobacterium abscessus infection caused by contamination of benzalkonium chloride. Clin Infect Dis. 2003;36:954–62.

    CAS  PubMed  Google Scholar 

  29. Galil K, Miller LA, Yakrus MA, Wallace RJ Jr, Mosley DG, England B, Huitt G, McNeill MM, Perkins BA. Abscesses due to Mycobacterium abscessus linked to injection of unapproved alternative medication. Emerg Infect Dis. 1999;5:681–7.

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Phillips MS, von Reyn CF. Nosocomial infections due to nontuberculous mycobacteria. Clin Infect Dis. 2001;33:1363–74.

    CAS  PubMed  Google Scholar 

  31. Decker BK, Palmore TN. The role of water in healthcare-associated infections. Curr Opin Infect Dis. 2013;26:345–51.

    PubMed  PubMed Central  Google Scholar 

  32. Carson LA, Bland LA, Cusick LB, Favero MS, Bolan GA, Reingold AL, Good RC. Prevalence of nontuberculous mycobacteria in water supplies of hemodialysis centers. Appl Environ Microbiol. 1988;54:3122–5.

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Li T, Abebe LS, Cronk R, Bartram J. A systematic review of waterborne infections from nontuberculous mycobacteria in health care facility water systems. Int J Hyg Environ Health. 2017;229:611–20.

    Google Scholar 

  34. von Reyn CF, Maslow JN, Barber TW, Falkinham JO III, Arbeit RD. Persistent colonization of potable water as a source of Mycobacterium avium infection in AIDS. Lancet. 1994;343:1137–41.

    Google Scholar 

  35. Tobin-D'Angelo MJ, Blass MA, del Rio C, Halvosa JS, Blumberg HM, Horsburgh CR Jr. Hospital water as a source of Mycobacterium avium complex isolates in respiratory specimens. J Infect Dis. 2004;189:98–104.

    PubMed  Google Scholar 

  36. Lowry PW, Jarvis WR, Oberle AD, Bland LA, Silberman R, Bocchini JA Jr, Dean HD, Swenson JM, Wallace RJ Jr. Mycobacterium chelonae causing otitis media in an ear-nose-and-throat practice. N Engl J Med. 1988;319:978–82.

    CAS  PubMed  Google Scholar 

  37. Meyers H, Brown-Elliott BA, Moore D, Curry J, Truong C, Zhang Y, Wallace RJ Jr. An outbreak of Mycobacterium chelonae infection following liposuction. Clin Infect Dis. 2002;34:1500–7.

    PubMed  Google Scholar 

  38. Wenger JD, Spika JS, Smithwick RW, Pryor V, Dodson DW, Carden GA, Klontz KC. Outbreak of Mycobacterium chelonae infection associated with use of jet injectors. JAMA. 1990;264:373–6.

    CAS  PubMed  Google Scholar 

  39. Soto LE, Bobadilla M, Villalobos Y, Sifuentes J, Avelar J, Arrieta M, Ponce de Leon S. Post-surgical nasal cellulitis outbreak due to Mycobacterium chelonae. J Hosp Infect. 1991;19:99–106.

    CAS  PubMed  Google Scholar 

  40. Kuritsky JN, Bullen MG, Broome CV, Silcox VA, Good RC, Wallace RJ Jr. Sternal wound infections and endocarditis due to organisms of the Mycobacterium fortuitum complex. Ann Intern Med. 1983;98:938–9.

    CAS  PubMed  Google Scholar 

  41. Lowry PW, Beck-Sague CM, Bland LA, Aguero SM, Arduino MJ, Minuth AN, Murray RA, Swenson JM, Jarvis WR. Mycobacterium chelonae infection among patients receiving high-flux dialysis in a hemodialysis clinic in California. J Infect Dis. 1990;161:85–90.

    CAS  PubMed  Google Scholar 

  42. Bolan G, Reingold AL, Carson LA, Silcox VA, Woodley CL, Hayes PS, Hightower AW, McFarland L, Brown JW III, Petersen NJ, Favero MS, Good RC, Broome CV. Infections with Mycobacterium chelonei in patients receiving dialysis and using processed hemodialyzers. J Infect Dis. 1985;152:1013–9.

    CAS  PubMed  Google Scholar 

  43. Band JD, Ward JI, Fraser DW, Peterson NJ, Silcox VA, Good RC, Ostrey PR, Kennedy J. Peritonitis due to a Mycobacterium chelonei-like organism associated with intermittent chronic peritoneal dialysis. J Infect Dis. 1982;145:9–17.

    CAS  PubMed  Google Scholar 

  44. Carbonne A, Brossier F, Arnaud I, Bougmiza I, Caumes E, Meningaud J-P, Dubrou S, Jarlier V, Cambau E, Astagneau P. Outbreak of nontuberculous mycobacterial subcutaneous infections related to multiple mesotherapy injections. J Clin Microbiol. 2009;47:1961–4.

    PubMed  PubMed Central  Google Scholar 

  45. Jaubert J, Mougari F, Picot S, Boukerrou M, Barau G, Ali Ahmed S-A, Cambau E. A case of postoperative breast infection by Mycobacterium fortuitum associated with the hospital water supply. Am J Infect Control. 2015;43:406–8.

    PubMed  Google Scholar 

  46. Kauppinen J, Nousiainen T, Jantunen E, Mattila R, Katila ML. Hospital water supply as a source of disseminated Mycobacterium fortuitum infection in a leukemia patient. Infect Control Hosp Epidemiol. 1999;20:343–5.

    CAS  PubMed  Google Scholar 

  47. Flesner C, Deresinski S. Investigation of an outbreak of SSI due to Mycobacterium immunogenum after blepharoplasty. Am J Infect Control. 2011;39:e204–5.

    Google Scholar 

  48. Astagneau P, Desplaces N, Vincent V, Chicheportiche V, Botherel A, Maugat S, Brucker G. Mycobacterium xenopi spinal infections after discovertebral surgery: investigation and screening of a large outbreak. Lancet. 2001;358:741–51.

    Google Scholar 

  49. Kline S, Cameron S, Streifel A, Yakrus MA, Kairis F, Peacock K, Cooksey RC. An outbreak of bacteremias associated with Mycobacterium mucogenicum in a hospital water supply. Infect Control Hosp Epidemiol. 2004;25:1042–9.

    PubMed  Google Scholar 

  50. Baird SF, Taori SK, Dave J, Willocks LJ, Roddie H, Hanson M. Cluster of non-tuberculous mycobacteraemia associated with water supply in a haemato-oncology unit. J Hosp Infect. 2011;79:339–43.

    CAS  PubMed  Google Scholar 

  51. Cooksey RC, Jhung MA, Yakrus MA, Butler WR, Adékambi T, Morlock GP, Williams M, Shams AM, Jensen BJ, Morey RE, Charles N, Toney SR, Jost KC Jr, Dunbar DF, Bennett V, Kuan M, Srinivasan A. Multiphasic approach reveals genetic diversity of environmental and patient isolates of Mycobacterium mucogenicum and Mycobacterium phocaicum associated with an outbreak of bacteremias at a Texas Hospital. Appl Environ Microbiol. 2008;74:2480–7.

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Livni G, Yaniv I, Samra Z, Kaufman L, Solter E, Ashkenazi S, Levy I. Outbreak of Mycobacterium mucogenicum bacteraemia due to contaminated water supply in a paediatric haematology-oncology department. J Hosp Infect. 2008;70:253–8.

    CAS  PubMed  Google Scholar 

  53. Iroh Tam P-Y, Kline S, Wagner JE, Guspiel A, Streifel A, Ward G, Messinger K, Ferrieri P. Rapidly growing mycobacteria among pediatric hematopoietic cell transplant patients traced to the hospital water supply. Pediatr Infect Dis J. 2014;33:1043–6.

    PubMed  Google Scholar 

  54. Rodriguez JM, Xie YL, Winthrop KL, Schafer S, Sehdev P, Solomon J, Jensen B, Toney NC, Lewis PF. Mycobacterium chelonae facial infections following injection of dermal filler. Asethet Surg J. 2013;33:265–9.

    Google Scholar 

  55. Brown-Elliott BA, Wallace RJ Jr, Tichindelean C, Sarria JC, McNulty S, Vasireddy R, Bridge L, Mayhall CG, Turenne C, Loeffelholz M. Five year outbreak of community- and hospital-acquired Mycobacterium porcinum infections related to public water supplies. J Clin Microbiol. 2011;49:4231–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Chadha R, Grover M, Shama A, Lakshmi A, D M, Kumar S, Mehta G. An outbreak of post-surgical wound infections due to Mycobacterium abscessus. Pediatr Surg Int. 1998;13:406–10.

    CAS  PubMed  Google Scholar 

  57. Merlani GM, Francioli P. Established and emerging waterborne nosocomial infections. Curr Opin Infect Dis. 2003;16:343–7.

    PubMed  Google Scholar 

  58. Hillebrand-Haverkort ME, Kolk AH, Kox LF, Ten Velden JJ, Ten Veen JH. Generalized Mycobacterium genavense infection in HIV-infected patients: detection of the mycobacterium in hospital tap water. Scand J Infect Dis. 1999;31:63–8.

    CAS  PubMed  Google Scholar 

  59. Conger NA, O’Connell R, Laurel V, Olivier K, Graviss EA, Williams-Bouyer N, Zhang Y, Brown-Elliott BA, Wallace RJ Jr. Mycobacterium simiae outbreak associated with a hospital water supply. Infect Control Hosp Epidemiol. 2004;25:1050–5.

    PubMed  Google Scholar 

  60. Aronson T, Holtzman A, Glover N, Boian M, Froman S, Berlin OGW, Hill H, Stelma G Jr. Comparison of large restriction fragments of Mycobacterium avium isolates recovered from AIDs and non-AIDs patients with those of isolates from potable water. J Clin Microbiol. 1999;37:1008–12.

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Baker AW, Lewis SS, Alexander BD, Chen LF, Wallace RJ Jr, Brown-Elliott BA, Isaacs PJ, Pickett LC, Patel CB, Smith PK, Reynolds JM, Engel J, Wolfe CR, Milano CA, Schroder JN, Davis RD, Hartwig MG, Stout JE, Strittholt N, Maziarz EK, Saullo JH, Hazen KC, Walczak RJ Jr, Vasireddy R, Vasireddy S, McKnight CM, Anderson DJ, Sexton DJ. Two-phase hospital-associated outbreak of Mycobacterium abscessus: investigation and mitigation. Clin Infect Dis. 2017;64:902–11.

    PubMed  PubMed Central  Google Scholar 

  62. Centers for Disease Control and Prevention. Rapidly growing mycobacterial infection following liposuction and liposculpture—Caracas, Venezuela, 1996-1998. Morb Mortal Wkly Rep. 1998;47:1065–7.

    Google Scholar 

  63. Centers for Disease Control and Prevention. Nontuberculous mycobacterial infections after cosmetic surgery—Santo Domingo, Dominican Republic, 2003-2004. Morb Mortal Wkly Rep. 2004;53:509.

    Google Scholar 

  64. del Castillo M, Palmero DJ, Lopez B, Paul R, Ritacco V, Bonvehi P, Clara L, Ambroggi M, Barrera L, Vay C. Mesotherapy-associated outbreak caused by Mycobacterium immunogenum. Emerg Infect Dis. 2009;15:357–8.

    Google Scholar 

  65. Regnier S, Cambau EM, Meningaud JP, et al. Clinical management of rapidly growing mycobacterial cutaneous infections in patients after mesotherapy. Clin Infect Dis. 2009;49:1358–64.

    PubMed  Google Scholar 

  66. van Dissel JT, Kuijper EJ. Rapidly growing mycobacteria: emerging pathogens in cosmetic procedures of the skin. Clin Infect Dis. 2009;49:1365–8.

    PubMed  Google Scholar 

  67. Furuya EY, Paez A, Srinivasan A, Cooksey R, Augenbraun M, Baron M, Brudney K, Della-Latta P, Estivariz C, Fischer S, Flood M, Kellner P, Roman C, Yakrus M, Weiss D, Granowitz EV. Outbreak of Mycobacterium abscessus wound infections among “lipotourists” from the United States who underwent abdominoplasty in the Dominican Republic. Clin Infect Dis. 2008;46:1181–8.

    PubMed  Google Scholar 

  68. Schnabel D, Esposito DH, Gaines J, Ridpath A, Barry MA, Feldman KA, Mullins J, Burns R, Ahmad N, Nyangoma EN, Nguyen DB, Perz JF, Moulton-Meissner HA, Jensen BJ, Lin Y, Posivak-Khouly L, Jani N, Morgan OW, Brunette GW, Pritchard PS, Greenbaum AH, Rhee SM, Blythe D, Sotir M. Multistate US outbreak of rapidly growing mycobacterial infections associated with medical tourism to the Dominican Republic, 2013-2014. Emerg Infect Dis. 2016;22:1340–7.

    PubMed  PubMed Central  Google Scholar 

  69. Falsey RR, Kinzer MH, Hurst S, Kalus A, Pottinger PS, Duchin JS, Zhang J, Noble-Wang J, Shinohara MM. Cutaneous inoculation of nontuberculous mycobacteria during professional tattooing: a case series and epidemiologic study. Clin Infect Dis. 2013;57:e143–7.

    PubMed  Google Scholar 

  70. Culton DA, Lachiewicz AM, Miller BA, Miller MB, MacKuen C, Groben P, White B, Cox GM, Stout JE. Nontuberculous mycobacterial infection after fractionated CO2 laser resurfacing. Emerg Infect Dis. 2013;19:365–70.

    PubMed  PubMed Central  Google Scholar 

  71. Ivan M, Dancer C, Koehler AP, Hobby M, Lease C. Mycobacterium chelonae abscesses associated with biomesotherapy, Australia, 2008. Emerg Infect Dis. 2013;19:1493–5.

    PubMed Central  Google Scholar 

  72. Woo PCY, Leung K-W, Wong SSY, Chong KTK, Cheung EYL, Yuen K-Y. Relatively alcohol-resistant mycobacteria are emerging pathogens in patients receiving acupuncture treatment. J Clin Microbiol. 2002;40:1219–24.

    PubMed  PubMed Central  Google Scholar 

  73. Duarte RS, Lourenço MC, Fonseca Lde S, Leão SC, Amorim Ede L, Rocha IL, Coelho FS, Viana-Niero C, Gomes KM, da Silva MG, Lorena NS, Pitombo MB, Ferreira RM, Garcia MH, de Oliveira GP, Lupi O, Vilaça BR, Serradas LR, Chebato A, Marques EA, Teixeira LM, Dalcolmo M, Senna SG, Sampaio JL. Epidemic of postsurgical infections caused by Mycobacterium massiliense. J Clin Microbiol. 2009;47:2149–55.

    Google Scholar 

  74. Matsumoto CK, Chimara E, Ramos JP, Campos CED, De Suza Caldas PC, Lima KVB, Lopes ML, Duarte RS, Leão SC. Rapid tests for the detection of the Mycobacterium abscessus subsp. bolletii strain responsible for an epidemic of surgical-site infections in Brazil. Mem Inst Oswaldo Cruz, Rio de Janeiro. 2012;107:969–70.

    CAS  Google Scholar 

  75. Viana-Niero C, Lima KVB, Lopes ML, da Silva Rabello MC, Marsola LR, Brilhante VCR, Durham AM, Leão SC. Molecular characterization of Mycobacterium massiliense and Mycobacterium bolletii in isolates collected from outbreaks of infections after laparoscopic surgeries and cosmetic procedures. J Clin Microbiol. 2008;46:850–5.

    CAS  PubMed  PubMed Central  Google Scholar 

  76. Winthrop KL, Albridge K, South D, Albrecht P, Abrams M, Samuel MC, Leonard W, Wagner J, Vugia DJ. The clinical management and outcome of nail salon-acquired Mycobacterium fortuitum skin infection. Clin Infect Dis. 2004;38:38–44.

    PubMed  Google Scholar 

  77. Vugia DJ, Jang Y, Zizek C, Ely J, Winthrop KL, Desmond E. Mycobacteria in nail salon whirlpool footbaths, California. Emerg Infect Dis. 2005;11:616–8.

    Google Scholar 

  78. Winthrop KL, Abrams M, Yakrus M, Swartz I, Ely J, Gillies D, Vugia DJ. An outbreak of mycobacterial furunculosis associated with footbaths at a nail salon. N Engl J Med. 2002;346:1366–71.

    PubMed  Google Scholar 

  79. Gira AK, Reisenauer H, Hammock L, Nadiminti U, Macy JT, Reeves A, Burnett C, Yakrus MA, Toney S, Jensen BJ, Blumberg HM, Caughman SW, Nolte FS. Furunculosis due to Mycobacterium mageritense associated with footbaths at a nail salon. J Clin Microbiol. 2004;42:1813–7.

    PubMed  PubMed Central  Google Scholar 

  80. Wallace RJ Jr, Musser JM, Hull SI, Silcox VA, Steele LC, Forrester GD, Labidi A, Selander RK. Diversity and sources of rapidly growing mycobacteria associated with infections following cardiac surgery. J Infect Dis. 1989;159:708–16.

    PubMed  Google Scholar 

  81. Robicsek F, Daugherty HK, Cook JW, Selle JG, Masters TN, O’Bar PR, Fernandez CR, Mauney CU, Calhoun DM. Mycobacterium fortuitum epidemics after open-heart surgery. J Thor Cardiovasc Surg. 1978;75:91–6.

    CAS  Google Scholar 

  82. Hoffman PC, Fraser DW, Robiesek F, O'Bar PR, Mauney CU. Two outbreaks of sternal wound infections due to organisms of the Mycobacterium fortuitum complex. J Infect Dis. 1981;143:533–42.

    CAS  PubMed  Google Scholar 

  83. Hector JSR, Pang Y, Mazurek GH, Zhang Y, Brown BA, Wallace RJ Jr. Large restriction fragment patterns of genomic Mycobacterium fortuitum DNA as strain-specific markers and their use in epidemiologic investigation of four nosocomial outbreaks. J Clin Microbiol. 1992;30:1250–5.

    CAS  PubMed  PubMed Central  Google Scholar 

  84. Vukovic D, Parezanovic V, Savid B, Dakic I, Laban-Nestorovic S, Ilic S, Cirkovic I, Stepanovic S. Mycobacterium fortuitum endocarditis associated with cardiac surgery, Serbia. Emerg Infect Dis. 2013;19:517–9.

    PubMed  PubMed Central  Google Scholar 

  85. Strabelli TMV, Siciliano RF, Castelli JB, Demarchi LMMF, Cardoso Leão S, Viana-Niero C, Miyashiro K, Sampaio RO, Grinberg M, Uip DE. Mycobacterium chelonae valve endocarditis resulting from contaminated biological prostheses. J Infect. 2010;60:467–73.

    CAS  PubMed  Google Scholar 

  86. Nagpal A, Wentink JE, Berbari EF, Aronhalt KC, Wright AJ, Krageschmidt DA, Wengenack NL, Thompson RI, Tosh PK. A cluster of Mycobacterium wolinskyi surgical site infection at an academic medical center. Infect Control Hosp Epidemiol. 2014;35:1169–75.

    PubMed  Google Scholar 

  87. Dupont C, Terru D, Aguilhon S, Frapier J-M, Paquis M-P, Morquin D, Lamy B, Godreuil S, Parer S, Lotthé A, Jumas-Bilak E, Romano-Bertrand S. Source-case investigation of Mycobacterium wolinskyi cardiac surgical site infection. J Hosp Infect. 2016;93:235–9.

    CAS  PubMed  Google Scholar 

  88. Lyman MM, Grigg C, Kinsey CB, Keckler MS, Moulton-Meissner H, Cooper E, Soe MM, Noble-Wang J, Longenberger A, Walker SR, Miller JR, Perz JF, Perkins KM. Invasive nontuberculous mycobacterial infections among cardiothoracic surgical patients exposed to heater-cooler devices. Emerg Infect Dis. 2017;23:796–805.

    PubMed  PubMed Central  Google Scholar 

  89. Kohler P, Kuster SP, Bloemberg G, Schulthess B, Frank M, Tanner FC, Rössle M, Böni C, Falk V, Wilhelm MJ, Sommerstein R, Achermann Y, Ten Oever J, Debast SB, Wolfhagen MJHM, Bravo Bruinsma GJB, Vos MC, Bogers A, Serr A, Beyersdorf F, Sax H, Böttger EC, Weber R, van Ingen J, Wagner D, Hasse B. Healthcare-associated prosthetic heart valve, aortic vascular graft, and disseminated Mycobacterium chimaera infections subsequent to open heart surgery. Eur Heart J. 2015;36:2745–53.

    PubMed  Google Scholar 

  90. Sax H, Bloemberg G, Hasse B, Sommerstein R, Kohler P, Achermann Y, Rössle M, Falk V, Kuster SP, Böttger EC, Weber R. Prolonged outbreak of Mycobacterium chimaera infection after open-chest heart surgery. Clin Infect Dis. 2015;61:67–75.

    PubMed  Google Scholar 

  91. Marra AR, Diekema DJ, Edmond MB. Mycobacterium chimaera infections associated with contaminated heater-cooler devices for cardiac surgery: outbreak management. Clin Infect Dis. 2017;65:669–74.

    PubMed  Google Scholar 

  92. Perkins KM, Lawsin A, Hasan NA, Strong M, Halpin AL, Rodger RR, Moulton-Meissner H, Crist MB, Schwartz S, Mardens J, Daley CL, Salfinger M, Perz JF. Notes from the field: Mycobacterium chimaera contamination of heater-cooler devices used in cardiac surgery – United States. MMWR Morb Mortal Wkly Rep. 2016;65:1117–8.

    PubMed  Google Scholar 

  93. Centers for Disease Control and Prevention. CDC advises hospitals to alert patients at risk for contaminated heater-cooler devices used during cardiac surgery. https://emergency.cec.gov/han/han00397.asp. 2016.

  94. Centers for Disease Control and Prevention. Non-tuberculous Mycobacterium (NTM) infections and heater-cooler devices interim practical guidance: Updated October 27, 2015. In: Services HaH, editor; 2015. Department of Health and Human Services, Centers for Disease Control and Prevention. https://www.cdc.gov/HAI/pdfs/outbreaks/CDC-Notice-Heater-Cooler-Units-final-clean.pdf

  95. Aitken ML, Limaye A, Pottinger P, Whimbey E, Goss GH, Tonelli MR, Cangelosi GA, Ashworth M, Olivier KN, Brown-Elliott BA, Wallace RJ Jr. Respiratory outbreak of Mycobacterium abscessus subspecies massiliense in a lung transplant and cystic fibrosis center. Letter to the Editor. Am J Respir Crit Care Med. 2012;185:231–3.

    CAS  PubMed  Google Scholar 

  96. Bryant JM, Grogono DM, Rodriguez-Rincon D, Everall I, Brown KP, Moreno P, Verma D, Hill E, Drijkoningen J, Gilligan P, Esther CR, Noone PG, Giddings O, Bell SC, Thomson R, Wainwright CE, Coulter C, Pandey S, Wood ME, Stockwell RE, Ramsay KA, Sherrard LJ, Kidd TJ, Jabbour N, Johnson GR, Knibbs LD, Morawska L, Sly PD, Jones A, Bilton D, Laurenson I, Ruddy M, Bourke S, Bowler ICJW, Chapman SJ, Clayton A, Cullen M, Daniels T, Dempsey O, Denton M, Desai M, Drew RJ, Edenborough F, Evans J, Folb J, Humphrey H, Isalska B, Jensen-Fangel S, Jönsson B, Jones AM, Katzenstein TL, Lillebaek T, MacGregor G, Mayell S, Millar M, Modha D, Nash EF, O’Brien C, O’Brien D, Ohri C, Pao CS, Peckham D, Perrin F, Perry A, Pressler T, Prtak L, Qvist T, Robb A, Rodgers H, Schaffer K, Shafi N, van Ingen J, Walshaw M, Watson D, West N, Whitehouse J, Haworth CS, Harris SR, Ordway D, Parkhill J, Floto RA. Emergence and spread of a human-transmissible multidrug-resistant nontuberculous mycobacterium. Science. 2016;354:751–7.

    CAS  PubMed  PubMed Central  Google Scholar 

  97. Bryant JM, Grogono DM, Greaves D, Foweraker J, Roddick I, Inns T, Reacher M, Haworth CS, Curran MD, Harris SR, Peacock SJ, Parkhill J, Floto RA. Whole-genome sequencing to identify transmission of Mycobacterium abscessus between patients with cystic fibrosis: a retrospective cohort study. Lancet. 2013;381:1551–60.

    CAS  PubMed  PubMed Central  Google Scholar 

  98. Tettelin H, Davidson RM, Agrawal S, Aitken ML, Shallom S, Hasan NA, Strong M, de Moura VCN, De Groote MA, Duarte RS, Hine E, Parankush S, Su Q, Daugherty SC, Fraser CM, Brown-Elliott BA, Wallace RJ Jr, Holland SM, Sampaio EP, Olivier KN, Jackson M, Zelazny AM. High-level relatedness among Mycobacterium abscessus subsp. massiliense strains from widely separated outbreaks. Emerg Infect Dis. 2014;20:364–71.

    PubMed  PubMed Central  Google Scholar 

  99. Floto RA, Olivier KN, Saiman L, Daley CL, Herrmann J-L, Nick JA, Noone PG, Bilton D, Corris P, Gibson RL, Hempstead SE, Koetz K, Sabadosa KA, Sermet-Gaudelus I, Smyth AR, van Ingen J, Wallace RJ, Winthrop KL, Marshall BC, Haworth CS. US Cystic Fibrosis Foundation and European Cystic Fibrosis Society consensus recommendations for the management of non-tuberculous mycobacteria in individuals with cystic fibrosis. Thorax. 2016;71:i1–i22.

    PubMed  Google Scholar 

  100. Chroneou A, Zimmerman SK, Cook S, Willey S, Eyre-Kelly J, Zias N, Shapiro DS, Beamis JF, Craven DE. Molecular typing of Mycobacterium chelonae isolates from a pseudo-outbreak involving an automated bronchoscope washer. Infect Control Hosp Epidemiol. 2008;29:1088–90.

    PubMed  Google Scholar 

  101. Scorzolini L, Mengoni F, Mastroianni CM, Baldan R, Cirillo DM, De Giusti M, Vullo V. Pseudo-outbreak of Mycobacterium gordonae in a teaching hospital: importance of strictly following decontamination procedures and emerging issues concerning sterilization. New Microbiol. 2016;39:25–34.

    CAS  PubMed  Google Scholar 

  102. LaBombardi VJ, O’Brien AM, Kislak JW. Pseudo-outbreak of Mycobacterium fortuitum due to contaminated ice machines. Am J Infect Control. 2002;30:184–6.

    PubMed  Google Scholar 

  103. Wang S-H, Mangino JE, Stevenson K, Yakrus MA, Cooksey R, Butler WR, Healy M, Wise MG, Schlesinger LS, Pancholi P. Characterization of “Mycobacterium paraffinicum” associated with a pseudo-outbreak. J Clin Microbiol. 2008;46:1850–3.

    CAS  PubMed  PubMed Central  Google Scholar 

  104. Maloney S, Welbel S, Daves B, Adams K, Becker S, Bland L, Arduino M, Wallace RJ Jr, Zhang Y, Buck G, Risch P, Jarvis W. Mycobacterium abscessus pseudoinfection traced to an automated endoscope washer: utility of epidemiologic and laboratory investigation. J Infect Dis. 1994;169:1166–9.

    CAS  PubMed  Google Scholar 

  105. Fraser V, Wallace RJ Jr. Nontuberculous mycobacteria. In: Mayhall CG, editor. Hospital epidemiology and infection control. Baltimore, MD: Williams & Wilkins; 1996. p. 1224–37.

    Google Scholar 

  106. Fraser V, Zuckerman G, Clouse RE, O’Rourke S, Jones M, Klasner J, Murray P. A prospective randomised trial comparing manual and automated endoscope disinfection methods. Infect Control Hosp Epidemiol. 1993;14:353–89.

    Google Scholar 

  107. Fraser VJ, Jones M, Murray PR, Medoff G, Zhang Y, Wallace RJ Jr. Contamination of flexible fiberoptic bronchoscopes with Mycobacterium chelonae linked to an automated bronchoscope disinfection machine. Am Rev Respir Dis. 1992;145:853–5.

    CAS  PubMed  Google Scholar 

  108. Zlojtro M, Jankovic M, Samarzija M, Zmak L, Jankovic VK, Obrovac M, Jakopovic M. Nosocomial pseudo-outbreak of Mycobacterium gordonae associated with a hospital’s water supply contamination: a case series of 135 patients. J Water Health. 2015;13:125–30.

    PubMed  Google Scholar 

  109. Guimarães T, Chimara E, do Prado GV, Ferrazoli L, Carvalho NG, Simeão FC, de Souza AR, Costa CA, Viana Niero C, Brianesi UA, di Gioia TR, Gomes LM, Spadão FS, Silva MD, de Moura EG, Levin AS. Pseudooutbreak of rapidly growing mycobacteria due to Mycobacterium abscessus subsp. bolletii in a digestive and respiratory endoscopy unit caused by the same clone as that of a countrywide outbreak. Am J Infect Control. 2016;44:e221–6.

    PubMed  Google Scholar 

  110. Lai KK, Brown BA, Westerling JA, Fontecchio SA, Zhang Y, Wallace RJ Jr. Long-term laboratory contamination by Mycobacterium abscessus resulting in two pseudo-outbreaks: recognition with use of random amplified polymorphic DNA (RAPD) polymerase chain reaction. Clin Infect Dis. 1998;27:169–75.

    CAS  PubMed  Google Scholar 

  111. Bignardi GE, Barrett SP, Hinkins R, Jenkins PA, Rebec MP. False-positive Mycobacterium avium-intracellulare cultures with the Bactec 460 TB system. J Hosp Infect. 1994;26:203–10.

    CAS  PubMed  Google Scholar 

  112. Bettiker RL, Axelrod PI, Fekete T, St. John K, Truant A, Toney S, Yakrus MA. Delayed recognition of a pseudo-outbreak of Mycobacterium terrae. Am J Infect Control. 2006;34:343–7.

    PubMed  Google Scholar 

  113. Zhang Y, Yakrus MA, Graviss EA, Williams-Bouyer N, Turenne C, Kabani A, Wallace RJ Jr. Pulsed-field gel electrophoresis study of Mycobacterium abscessus isolates previously affected by DNA degradation. J Clin Microbiol. 2004;42:5582–7.

    CAS  PubMed  PubMed Central  Google Scholar 

  114. Sampaio JLM, Junior DN, de Freitas D, Höfling-Lima AL, Miyashiro K, Alberto FL, Leão SC. An outbreak of keratitis caused by Mycobacterium immunogenum. J Clin Microbiol. 2006;44:3201–7.

    CAS  PubMed  PubMed Central  Google Scholar 

  115. Zhang Y, Rajagopalan M, Brown BA, Wallace RJ Jr. Randomly amplified polymorphic DNA PCR for comparison of Mycobacterium abscessus strains from nosocomial outbreaks. J Clin Microbiol. 1997;35:3132–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  116. Sampaio JL, Viana-Niero C, de Freitas D, Höfling-Lima AL, Leão SC. Enterobacterial repetitive intergenic consensus PCR is a useful tool for typing Mycobacterium chelonae and Mycobacterium abscessus isolates. Diagn Microbiol Infect Dis. 2006;55:107–18.

    CAS  PubMed  Google Scholar 

  117. Brown-Elliott BA, Wallace RJ Jr. Nontuberculous mycobacteria. In: Mayhall CG, editor. Hospital epidemiology and infection control. 4th ed. Philadelphia: Lippincott Williams & Wilkins; 2012. p. 593–608.

    Google Scholar 

  118. Hung JH, Huang YH, Chang TC, Tseng SH, Shih MH, Wu JJ, Huang FC. A cluster of endophthalmitis caused by Mycobacterium abscessus after cataract surgery. J Microbiol Immunol Infect. 2016;49:799–803.

    PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Microbiology, Mycobacteria/Nocardia Research Laboratory, The University of Texas Health Science Center, Tyler, TX, USA

    Barbara A. Brown-Elliott

  2. Department of Microbiology, Mycobacteria/Nocardia Laboratory, The University of Texas Health Science Center, Tyler, TX, USA

    Richard J. Wallace Jr.

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  1. Barbara A. Brown-Elliott
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Correspondence to Barbara A. Brown-Elliott .

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  1. Professor of Medicine, University of Texas Health Science Center, Tyler, TX, USA

    David E. Griffith

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Brown-Elliott, B.A., Wallace, R.J. (2019). Healthcare-Associated Outbreaks and Pseudo-Outbreaks of Nontuberculous Mycobacteria. In: Griffith, D. (eds) Nontuberculous Mycobacterial Disease. Respiratory Medicine. Humana Press, Cham. https://doi.org/10.1007/978-3-319-93473-0_18

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