Washington University School of Medicine Digital Commons@Becker Open Access Publications 2016 Mycobacterium arupense, Mycobacterium heraklionense, and a newly proposed species, “Mycobacterium virginiense” sp. nov., but not Mycobacterium nonchromogenicum, as species of the Mycobacterium terrae complex causing tenosynovitis and osteomyelitis Ravikiran Vasireddy University of Texas Health Center at Tyler Sruthi Vasireddy University of Texas Health Center at Tyler Barbara A. Brown-Ellliott University of Texas Health Center at Tyler Nancy L. Wengenack Mayo Clinic Uzoamaka A. Eke Washington University School of Medicine in St. Louis Recommended Citation Vasireddy, Ravikiran; Vasireddy, Sruthi; Brown-Ellliott, Barbara A.; Wengenack, Nancy L.; Eke, Uzoamaka A.; Benwill, Jeana L.; Turenne, Christine; and Wallace, Richard J. Jr., ,"Mycobacterium arupense, Mycobacterium heraklionense, and a newly proposed species, “Mycobacterium virginiense” sp. nov., but not Mycobacterium nonchromogenicum, as species of the Mycobacterium terrae complex causing tenosynovitis and osteomyelitis." Journal of Clinical Microbiology.54,5. 1340-1351. (2016). https://digitalcommons.wustl.edu/open_access_pubs/4955 This Open Access Publication is brought to you for free and open access by Digital Commons@Becker. It has been accepted for inclusion in Open Access Publications by an authorized administrator of Digital Commons@Becker. For more information, please contact [email protected]. See next page for additional authors Follow this and additional works at: https://digitalcommons.wustl.edu/open_access_pubs Authors Ravikiran Vasireddy, Sruthi Vasireddy, Barbara A. Brown-Ellliott, Nancy L. Wengenack, Uzoamaka A. Eke, Jeana L. Benwill, Christine Turenne, and Richard J. Wallace Jr. This open access publication is available at Digital Commons@Becker: https://digitalcommons.wustl.edu/open_access_pubs/4955 crossmark Mycobacterium arupense, Mycobacterium heraklionense, and a Newly Proposed Species, “Mycobacterium virginiense” sp. nov., but Not Mycobacterium nonchromogenicum, as Species of the Mycobacterium terrae Complex Causing Tenosynovitis and Osteomyelitis Downloaded from Ravikiran Vasireddy,a Sruthi Vasireddy,a Barbara A. Brown-Elliott,a Nancy L. Wengenack,b Uzoamaka A. Eke,c* Jeana L. Benwill,a Christine Turenne,d* Richard J. Wallace, Jr.a Mycobacteria/Nocardia Research Laboratory, Department of Microbiology, The University of Texas Health Science Center at Tyler, Tyler, Texas, USAa; Mayo Clinic, Rochester, Minnesota, USAb; Division of Infectious Disease, Washington University in St. Louis School of Medicine, St. Louis, Missouri, USAc; Saskatchewan Disease Control Laboratory, Regina, Saskatchewan, Canadad Mycobacterium terrae complex has been recognized as a cause of tenosynovitis, with M. terrae and Mycobacterium nonchromo- genicum reported as the primary etiologic pathogens. The molecular taxonomy of the M. terrae complex causing tenosynovitis http://jcm.asm.org/ has not been established despite approximately 50 previously reported cases. We evaluated 26 isolates of the M. terrae complex associated with tenosynovitis or osteomyelitis recovered between 1984 and 2014 from 13 states, including 5 isolates reported in 1991 as M. nonchromogenicum by nonmolecular methods. The isolates belonged to three validated species, one new proposed species, and two novel related strains. The majority of isolates (20/26, or 77%) belonged to two recently described species: Myco- bacterium arupense (10 isolates, or 38%) and Mycobacterium heraklionense (10 isolates, or 38%). Three isolates (12%) had 100% sequence identity to each other by 16S rRNA and 99.3 to 100% identity by rpoB gene region V sequencing and represent a previ- ously undescribed species within the M. terrae complex. There were no isolates of M. terrae or M. nonchromogenicum, including among the five isolates reported in 1991. The 26 isolates were susceptible to clarithromycin (100%), rifabutin (100%), ethambu- on May 31, 2016 by Washington University in St. Louis tol (92%), and sulfamethoxazole or trimethoprim-sulfamethoxazole (70%). The current study suggests that M. arupense, M. heraklionense, and a newly proposed species (“M. virginiense” sp. nov.; proposed type strain MO-233 [DSM 100883, CIP 110918]) within the M. terrae complex are the major causes of tenosynovitis and osteomyelitis in the United States, with little change over 20 years. Species identification within this complex requires sequencing methods. ycobacterium terrae complex (MTC) was first characterized ture sequence for members of the MTC compared to other slowly Min 1981 by the International Working Group in Mycobacte- growing mycobacteria (37, 38). He also characterized several new rial Taxonomy (IWGMT). The initial MTC consisted of two non- species in the complex, including Mycobacterium heraklionense chromogenic slowly growing species: M. terrae and Mycobacte- and Mycobacterium engbaekii (1). rium nonchromogenicum (1, 2). Phenotypic separation within the The greater availability of DNA sequencing (59) has resulted in group was often difficult, and molecular methods were not avail- a “boom” of new species of MTC, beginning with Mycobacterium able, making establishment of species pathogenicity uncertain (3). hiberniae (39). An additional eight new species have been validly The complex is recognized as an environmental contaminant published since 2006: Mycobacterium arupense (28), Mycobacte- of sputum and a cause of tenosynovitis and osteomyelitis primar- rium kumamotonense (36), Mycobacterium heraklionense (1), My- ily of the fingers and wrist (3–35). Whether one or more members cobacterium senuense (40), Mycobacterium minnesotense (41), My- of the complex are true respiratory pathogens has not been estab- lished (1, 22). The first published case report of tenosynovitis caused by the MTC was by Hirata and Tomiyama in 1976 (4). There have been Received 28 January 2016 Returned for modification 16 February 2016 Accepted 1 March 2016 approximately 34 additional case reports published since then, Accepted manuscript posted online 9 March 2016 identified using nonmolecular methods (3–25), with 14 cases Citation Vasireddy R, Vasireddy S, Brown-Elliott BA, Wengenack NL, Eke UA, identified using molecular methods (26–28, 30–36)(Tables 1 and Benwill JL, Turenne C, Wallace RJ, Jr. 2016. Mycobacterium arupense, 2). With the exception of four isolates of M. arupense, including Mycobacterium heraklionense, and a newly proposed species, “Mycobacterium the original description of M. arupense (28), details of the methods virginiense” sp. nov., but not Mycobacterium nonchromogenicum, as species of the and/or explicitly stating a 100% 16S rRNA gene sequence identity Mycobacterium terrae complex causing tenosynovitis and osteomyelitis. J Clin Microbiol 54:1340–1351. doi:10.1128/JCM.00198-16. to recognized species for the remaining cases with molecular iden- Editor: G. A. Land tifications have been absent (Table 2). Address correspondence to Ravikiran Vasireddy, [email protected]. An excellent history and species update of the M. terrae com- * Present address: Uzoamake A. Eke, Infectious Diseases Consultants of Detroit, plex based on multigene sequencing targets was published by Tor- Southfield, Michigan, USA; Christine Turenne, St. Boniface Hospital, Diagnostic toli et al. (1). He noted that the presence of a two nucleotide Services Manitoba, Winnipeg, MB, Canada. insertion in helix 18 of the 16S rRNA gene (bp ϳ430 to 500; Copyright © 2016, American Society for Microbiology. All Rights Reserved. hypervariable region B or region V3) provided a consistent signa- 1340 jcm.asm.org Journal of Clinical Microbiology May 2016 Volume 54 Number 5 Mycobacterium terrae Species Causing Tenosynovitis TABLE 1 Characteristics and species designations of 35 previously reported cases of tenosynovitis due to the M. terrae complex without molecular species identificationa Local Granulomatous AFB Location/yr of No. Age/sex Site of tenosynovitis Diagnosis or risk factor(s)s steroid Surgery inflammation smear Species Reference publication 1 65/M Right foot (ankle) Farmer; NA ϩ NA NA NA M. nonchromogenicum 4 Japan/1976 2 20/M Left forefinger, wrist NA ϩϩ ϩ ϩM. terrae 5 Texas/1978 3 23/M Left index finger Puncture from fish fin ϩϩ ϩ ϪM. terrae 6 NA/1979 4 57/M Knee RA ϩ NA NA ? M. terrae 7 NA/1981 5 66/F Right index finger Puncture from blackberry Ϫϩ ϩ ϩM. terrae 8 NA/1981 thorn Downloaded from 6 60/M Left hand, forearm Puncture from wooden Ϫϩ ϩ ϪM. terrae 9 NA/1983 splinter 7 47/F Right 4th and 5th Puncture from straight pin ϩϩ ϩ ϪM. terrae 10 NA/1983 fingers, palm, thumb 8 72/M left forearm, right 5th Puncture wound Ϫϩ ϩ ϪM. terrae 11 France/1984 finger, right thumb 9 75/M Left index finger Arteritis ϩϩ ϩ ϪM. terrae 12 NA/1985 10 NA Knee NA ϩ NA NA NA M. terrae 13 France/1987 11 54/M Right 3rd finger, PIP Puncture from fish fin ϩϩ ϩ ϩM. terrae 14 NA/1988 http://jcm.asm.org/ joint 12 55/M Right 3rd finger, Puncture from fish fin ϪϪ NA Ϫ M. terrae 14 NA/1988 MCP joint 13 41/F Hand, wrist Renal transplant ϩ NA NA NA M. terrae 15 NA/1988 14 58/F Right, 3rd finger Nurse ϩϩ ϩ ϪM. terrae 16 Sweden/1989 15 28/F Right, 2nd finger Lab technician Ϫϩ Ϫ ϪM. terrae 16 Sweden/1989 16 71/F Right, 2nd finger Retired ϩϩ Ϫ ϪM. terrae 16 Sweden/1989 17 47/F Right 3rd finger Cook ϩϩ ϩ ϪM. terrae 16 Sweden/1989 18 31/F Right, 2nd finger Office worker ϩϩ ϩ ϪM. terrae 16 Sweden/1989 19 38/F Right, 3rd finger Lab technician ϩϩ ϩ ϪM. terrae 16 Sweden/1989 on May 31, 2016 by Washington University in St. Louis 20 48/M 3rd finger NA ? ϩ ??M. terrae 17 NA/1989 21 63/F Wrist Gardener NA NA NA NA M. terrae 18 NA/1990 22 58/F Right index finger Gardening, cook (case 1) Ϫϩ ϩ ϪM. nonchromogenicum 3 Maine/1991 23 60/M Left wrist Meat cutter (case 2) Ϫϩ ϩ ϪM. nonchromogenicum 3 Illinois/1991 24 59/M Left wrist Maintenance work (case 3) Ϫϩ ϩ ϪM. nonchromogenicum 3 Florida/1991 25 62/F Right middle finger NA (case 4) Ϫϩ ϩ ϪM. nonchromogenicum 3 Texas/1991 26 40/M Left hand, thumb Dermatomyositis on ϩϩ ϩ ϪM. nonchromogenicum 3 Florida/1991 steroids (case 5) 27 40/F Right 5th finger Fishing, gardening, prior Ϫϩ ϩ NA M.