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Mycobacterial Taxonomy
Betty A. Forbes
Department of Pathology, Virginia Commonwealth University Medical Center, Richmond, Virginia, USA
ABSTRACT This article summarizes the most recent (since 2012) taxonomic changes
in the genus Mycobacterium. Only those mycobacteria that have been isolated from Accepted manuscript posted online 7
December 2016
human specimens are included in this summary.
Citation Forbes BA. 2017. Mycobacterial
KEYWORDS human specimens, mycobacteria, taxonomy taxonomy. J Clin Microbiol 55:380 –383. https://
doi.org/10.1128/JCM.01287-16.
Editor Colleen Suzanne Kraft, Emory University
C urrently, there are over 170 recognized species of Mycobacterium, the only genus
in the family Mycobacteriaceae. Organisms belonging to this genus are quite
diverse with respect to their ability to cause disease in humans; some are strict
Copyright © 2017 American Society for
Microbiology. All Rights Reserved.
Address correspondence to baforbes@vcu.edu.
METHODS
Only those newly recognized mycobacterial species recovered from human clinical
material and reported between January 2012 and December 2015 are summarized
here. These new species were identified using a combination of reference materials. A
valuable resource was the List of Prokaryotic Names with Standing in Nomenclature
(http://www.bacterio.net/-allnamesmr.html). In addition, a combination of reference
materials was used, including the Manual of Clinical Microbiology, 11th edition, chapters
30 through 32; the International Journal of Systematic and Evolutionary Microbiology;
and the PubMed database (http://www.ncbi.nlm.nih.gov/pubmed), using “nov. sp.
Mycobacterium” as the search term.
RESULTS
Table 1 summarizes new Mycobacterium species identified between January 2012
and December 2015. For each species, the human source(s) from which the new species
was isolated, its clinical relevance, and noteworthy growth characteristics are noted. In
addition, information on whether 16S rRNA gene sequencing identified the species is
TABLE 1 New mycobacterial species (family: Mycobacteriaceae) recovered between January 2012 and December 2015
Unique 16S
rRNA gene? If
not, gene
Scientific name (year sequence
identified) Sourcea Clinical relevance Growth characteristics alternative References
M. alsense (2015) Sputum Infection Slow grower; weak yellow pigment Yes 2, 3
on Lowenstein Jensen medium,
not Middlebrook 7H11; most
closely related to M. szulgai and
M. malmoense
M. celeriflavum (2015) Sputum Undetermined; colonizer Rapid grower; scotochromogen Yes 1, 4
(rough, pale yellow); most
closely related to M. flavescens
and M. novocastrense
M. engbaekii (2013) Urine, gastric wash fluid, Undetermined; colonizer Slow grower; most closely related Yes 1, 5
bronchial aspirate to M. terrae complex (namely, M.
hiberniae); pigmented (some
show pink photochromogenic
pigmentation)
M. fragae (2013) Sputum Undetermined; colonizer Slow grower; smooth colonies, Yes 1, 6
unpigmented; closely related to
M. celatum
“M. franklinii”b (2015) Respiratory tract, skin, Infection; colonizer Rapid grower; nonpigmented; No; rpoB, hsp65 1, 7, 8
granulomatous liver closely related to M.
lesion, central line chelonae/abscessus
infection
“M. fukienense”b (2013) Respiratory tract Undetermined; colonizer Rapid grower; nonpigmented; No; hsp65 1, 9
closely related to M.
chelonae/abscessus
M. heraklionense (2013) Respiratory: BAL and Undetermined; colonizer Slow grower; nonpigmented; Yes 1,5
sputum closely related to M. terrae
complex, namely, to M.
arupense; optimal growth temp
25–37°C
M. iranicum (2013) Sputum, BAL, CSF, hand Infection; colonizer Rapid grower; scotochromogen; Yes 1,10–14
wound, peritoneal closely related to M. gilvum
fluid
M. koreense (2012) Sputum Undetermined Slow grower; nonpigmented; Yes 1,15
included. In addition, brief summaries of case reports for some of the new species are
provided in Table 2.
DISCUSSION
Accurate identification of the mycobacteria is a challenge, particularly in light of the
extraordinary number of species in the genus. It has become clear that identification of
mycobacteria based on phenotypic and culture traits is poorly reproducible, time
consuming, and lacking in sufficient discriminatory power (21). As a result, this ap-
proach to mycobacterial identification has been abandoned for the most part. Al-
though the introduction of numerous new species over recent years might seem
daunting to clinical laboratories that identify mycobacteria, accurate identification is
TABLE 2 Brief summaries of clinical case reports for new Mycobacterium species
Organism Infections Reference
M. alsense Bronchopneumonia in two 70-yr-old subjects; both responded to antimycobacterial therapy 2
“M. franklinii” Although 26 clinical isolates were obtained, medical histories were provided for only 6 7
patients; 2 patients had sinusitis, and 4 patients had lower respiratory tract symptoms; all
patients with respiratory tract symptoms had underlying pulmonary disease
M. iranicum Isolated 3 times from the hand wound of an 18-yr-old male with a history of long-term steroid 10
treatment due to renal transplantation; treated with amikacin and clinically improved
An organism grew from culture of a BAL specimen from a 60-yr-old female with pneumonia; 10
patient responded to amikacin and ciprofloxacin
Peritoneal dialysis-related peritonitis in a 68-yr-old male with diabetic nephropathy who 13
responded to appropriate antimycobacterial therapy
HIV-infected patient admitted initially with mild fever, wt loss, chronic chest pain, and 14
nonproductive cough; no AFBa smear was done; patient’s fever and chest pain remained
unchanged; after bronchoscopy, 2 of 3 BAL specimens were AFB smear positive, and 3 of 3
were culture positive for a rapidly growing mycobacterium; a standard antituberculosis
regimen was started, but patient did not improve; after 1 mo, a sputum specimen was
negative for AFB, and 1 BAL specimen was positive by microscopy and culture for M.
iranicum; patient improved rapidly on amikacin and ciprofloxacin for 3 mo
M. longobardum Osteomyelitis of the elbow in a 71-yr-old male 14
M. yongonense First description of the species and its association with pulmonary infection, from the sputum 19
of a patient with unspecified lung disease, was in South Korea
74-yr-old woman presented with fatigue, diarrhea, and wt loss; chest x-ray revealed a cavitary 20
lesion; cultures of sputum and stool grew M. yongonense; a BAL specimen was also AFB
smear positive and grew the same organism
aAFB, acid-fast bacilli.
critical for proper diagnosis and management of infections and for outbreak investi-
gation.
This need was illustrated in recent reports of serious infections in patients who had
undergone open cardiac surgery in which a contaminated heater-cooler device was
used during extracorporeal circulation. These infections, occurring in patients in Europe
and the United States, were caused by Mycobacterium chimaera, a nontuberculous
mycobacterium ubiquitous in soil and water (22). This organism is a slow-growing NTM
species included in the M. avium complex (MAC). Initially, strains of this organism were
identified by a commercial probe assay as Mycobacterium intracellulare. In-depth inves-
REFERENCES
1. Tortoli E. 2014. Microbiological features and clinical relevance of new bacterium isolated from clinical specimens. Int J Syst Evol Microbiol
species of the genus Mycobacterium. Clin Microbiol Rev 27:727–752. 65:510 –515. https://doi.org/10.1099/ijs.0.064832-0.
https://doi.org/10.1128/CMR.00035-14. 5. Tortoli E, Gitti Z, Klenk HP, Lauria S, Mannino R, Mantegani P, Mariottini A,
2. Richter E, Tortoli E, Fischer A, Hendricks O, Engel R, Hillemann D, Neonakis I. 2013. Survey of 150 strains belonging to the Mycobacterium
Schubert S, Kristiansen JE. 2007. Mycobacterium alsiense, a novel, slowly terrae complex and description of Mycobacterium engbaekii sp. nov., Myco-
growing species isolated from two patients with pulmonary disease. J bacterium heraklionense sp. nov. and Mycobacterium longobardum sp. nov.
Clin Microbiol 45:3837–3839. https://doi.org/10.1128/JCM.01097-07. Int J Syst Evol Microbiol 63:401–411. https://doi.org/10.1099/ijs.0.038737-0.
3. Tortoli E, Richter E, Borroni E, Cabibbe AM, Capitolo E, Cittaro D, Engel R, 6. Ramos JP, Campos CE, Caldas PC, Ferreira NV, da Silva MV, Redner P,
Hendricks O, Hillemann D, Kristiansen JE, Mariottini A, Schubert S, Cirillo Campelo CL, Vale SF, Barroso EC, Medeiros RF, Montes FC, Galvao TC,
DM. 2016. Mycobacterium alsense sp. nov., a scotochromogenic slow Tortoli E. 2013. Mycobacterium fragae sp. nov., a non-chromogenic
grower isolated from clinical respiratory specimens. Int J Syst Evol species isolated from human respiratory specimens. Int J Syst Evol
Microbiol 66:450 – 456. https://doi.org/10.1099/ijsem.0.000744. Microbiol 63:2583–2587. https://doi.org/10.1099/ijs.0.046862-0.
4. Shahraki AH, Cavusoglu C, Borroni E, Heidarieh P, Koksalan OK, Cabibbe 7. Simmon KE, Brown-Elliott BA, Ridge PG, Durtschi JD, Mann LB, Slechta
AM, Hashemzadeh M, Mariottini A, Mostafavi E, Cittaro D, Feizabadi MM, ES, Steigerwalt AG, Moser BD, Whitney AM, Brown JM, Voelkerding KV,
Lazarevic D, Yaghmaei F, Molinari GL, Camaggi A, Tortoli E. 2015. Myco- McGowan KL, Reilly AF, Kirn TJ, Butler WR, Edelstein PH, Wallace RJ, Jr,
bacterium celeriflavum sp. nov., a rapidly growing scotochromogenic Petti CA. 2011. Mycobacterium chelonae-abscessus complex associated
with sinopulmonary disease, northeastern USA. Emerg Infect Dis 17: chromogenic species closely related to Mycobacterium triviale. Int J Syst
1692–1700. https://doi.org/10.3201/eid1709.101667. Evol Microbiol 62:1289 –1295. https://doi.org/10.1099/ijs.0.033274-0.
8. Lourenço Nogueira C, Simmon KE, Chimara E, Cnockaert M, Carlos 16. Hong SK, Sung JY, Lee HJ, Oh MD, Park SS, Kim EC. 2013. First case of
Palomino J, Martin A, Vandamme P, Brown-Elliott BA, Wallace R, Jr, Mycobacterium longobardum infection. Ann Lab Med 33:356 –359.
Cardoso Leao S. 2015. Mycobacterium franklinii sp. nov., a species closely https://doi.org/10.3343/alm.2013.33.5.356.
related to members of the Mycobacterium chelonae-Mycobacterium ab- 17. Kim BJ, Hong SH, Kook YH, Kim BJ. 2014. Mycobacterium paragordonae
scessus group. Int J Syst Evol Microbiol 65:2148 –2153. https://doi.org/ sp. nov., a slowly growing, scotochromogenic species closely related to
10.1099/ijs.0.000234. Nogueira). Mycobacterium gordonae. Int J Syst Evol Microbiol 64:39 – 45. https://
9. Zhang YY, Li YB, Huang MX, Zhao XQ, Zhang LS, Liu WE, Wan KL. 2013. doi.org/10.1099/ijs.0.051540-0.
Novel species including Mycobacterium fukienense sp. is found from 18. Kim BJ, Hong SH, Yu HK, Park YG, Jeong J, Lee SH, Kim SR, Kim K, Kook
tuberculosis patients in Fujian Province, China, using phylogenetic anal- YH, Kim BJ. 2013. Mycobacterium parakoreense sp. nov., a slowly growing
ysis of Mycobacterium chelonae/abscessus complex. Biomed Environ Sci non-chromogenic species related to Mycobacterium koreense, isolated
26:894 –901. from a human clinical specimen. Int J Syst Evol Microbiol 63:2301–2308.
10. Shojaei H, Daley C, Gitti Z, Hashemi A, Heidarieh P, Moore ER, Naser AD, https://doi.org/10.1099/ijs.0.045070-0.
19. Kim BJ, Math RK, Jeon CO, Yu HK, Park YG, Kook YH, Kim BJ. 2013.
Russo C, van Ingen J, Tortoli E. 2013. Mycobacterium iranicum sp. nov., a
Mycobacterium yongonense sp. nov., a slow-growing non-chromogenic
rapidly growing scotochromogenic species isolated from clinical speci-
species closely related to Mycobacterium intracellulare. Int J Syst Evol
mens on three different continents. Int J Syst Evol Microbiol 63:
Microbiol 63:192–199. https://doi.org/10.1099/ijs.0.037465-0.
1383–1389. https://doi.org/10.1099/ijs.0.043562-0.
20. Tortoli E, Mariottini A, Pierotti P, Simonetti TM, Rossolini GM. 2013.
11. Tan JL, Ng HF, Wee WY, Ang MY, Wong GJ, Ngeow YF, Choo SW. 2013.
Mycobacterium yongonense in pulmonary disease, Italy. Emerg Infect Dis
First whole-genome sequence of Mycobacterium iranicum, a newly re-
19:1902–1904.
ported mycobacterial species. Genome Announc 1:e00732-13. https:// 21. Springer B, Stockman L, Teschner K, Roberts GD, Böttger EC. 1996.
doi.org/10.1128/genomeA.00732-13. Two-laboratory collaborative study on identification of mycobacteria:
12. Balakrishnan N, Tortoli E, Engel SL, Breitschwerdt EB. 2013. Isolation of a molecular versus phenotypic methods. J Clin Microbiol 34:296 –303.
novel strain of Mycobacterium iranicum from a woman in the United States. 22. Perkins KM, Lawsin A, Hasan NA, Strong M, Halpin AL, Rodger RR, Moulton-
J Clin Microbiol 51:705–707. https://doi.org/10.1128/JCM.02560-12. Meissner H, Crist MB, Schwartz S, Marders J, Daley CL, Salfinger M, Perz JF.
13. Inagaki K, Mizutani M, Nagahara Y, Asan M, Masamoto D, Sawada O, 2016. Mycobacterium chimaera contamination of heater-cooler devices used
Aono A, Chikamatsu K, Mitarai S. 2016. Successful treatment of perito- in cardiac surgery—United States. MMWR Morb Mortal Wkly Rep 65:
neal dialysis-related peritonitis due to Mycobacterium iranicum. Intern 1117–1118. https://doi.org/10.15585/mmwr.mm6540a6.
Med 55:1929 –1931. https://doi.org/10.2169/internalmedicine.55.5219. 23. Tortoli E, Rindi L, Garcia MJ, Chiaradonna P, Dei R, Garzelli C, Kroppen-
14. Hashemi-Shahraki A, Azarpira S, Shojaei H, Hashemzadeh M, Tortoli E. 2013. stedt RM, Lari N, Mattei R, Mariottini A, Mazzarelli G, Murcia MI, Nanetti
Mycobacterium iranicum infection in HIV-infected patient, Iran. Emerg Infect A, Piccoli P, Scarparo C. 2004. Proposal to elevate the genetic variant
Dis 19:1696–1697. https://doi.org/10.3201/eid1910.130658. MAC-A, included in the Mycobacterium avium complex, to species rank
15. Kim BJ, Jeong J, Lee SH, Kim SR, Yu HK, Park YG, Kim KJ, Kook YH, Kim as Mycobacterium chimaera sp. nov. Int J Syst Evol Microbiol 54:
BJ. 2012. Mycobacterium koreense sp. nov., a slowly growing non- 1277–1285. https://doi.org/10.1099/ijs.0.02777-0.