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Skin and Soft Tissue Infections Due to Nontuberculous Mycobacteria

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Skin and Soft Tissue Infections Due to Nontuberculous Mycobacteria Current Infectious Disease Reports (2018) 20:6 https://doi.org/10.1007/s11908-018-0611-3 SKIN, SOFT TISSUE, BONE AND JOINT INFECTIONS (N SAFDAR AND A POP-VICAS, SECTION EDITORS) Skin and Soft Tissue Infections Due to Nontuberculous Mycobacteria Elizabeth Ann Misch1 & Christopher Saddler2 & James Muse Davis3 # Springer Science+Business Media, LLC, part of Springer Nature 2018 Abstract Purpose of Review This review describes recent trends in the epidemiology of nontuberculous mycobacteria (NTM), emerging pathogens, new insights into NTM pathogenesis, and advances in diagnosis and treatment. Recent Findings Emerging pathogens include Mycobacterium chimaera and drug-resistant subspecies of Mycobacterium abscessus. Important virulence mechanisms of pathogenic NTM include the ability to alter the macrophage’spermis- siveness to intracellular bacterial growth. New diagnostic tools consist of DNA probes, gene sequencing, and matrix- assisted laser desorption ionization-time of flight. These methods allow rapid speciation of NTM species, in some cases directly from patient samples. There are few novel agents available to treat NTM, although some repurposed drugs show excellent activity. Summary The incidence of NTM infections appears to be increasing in a number of regions around the world. Molecular methods are now the diagnostic tools of choice. Discovery of novel effective agents and/or drug combinations with greater likelihood of cure, shorter treatment duration, and fewer side effects are research priorities. Keywords Nontuberculousmycobacteria .M.chimaera .Skinandsofttissue .Rapidlygrowingmycobacteria(RGM) .Molecular diagnostics Introduction and Background tuberculosis complex1 and Mycobacterium leprae, the agent of leprosy. More than 190 species have been identified Nontuberculous mycobacteria (NTM) encompass all (http://www.bacterio.net/mycobacterium.html) [1], of mycobacteria species other than those in the Mycobacterium which approximately 40 species are considered patho- genic [2]. Mycobacteria are ubiquitous in the natural and constructed environment. They can be found in all This article is part of the Topical Collection on Skin, Soft Tissue, Bone and regions of the world in soil, natural or treated water Joint Infections (including tap and shower water), and in association • * Elizabeth Ann Misch with plants, birds, fish, and other animals [3 , 4, 5, 6]. [email protected] A few species, including Mycobacterium haemophilum and Mycobacterium ulcerans, are rarely isolated from the environment [7], but this fact may reflect special 1 Division of Allergy and Infectious Disease, Department of Medicine, School of Medicine and Public Health, University of Wisconsin, growth requirements (M. haemophilum), or the extended in- Medical Foundation Centennial Building, 1685 Highland Avenue, cubation periods (M. ulcerans) needed for successful culture. 5th floor, Madison, WI 53705-2281, USA In humans, NTM are facultative intracellular pathogens. 2 Division of Allergy and Infectious Disease, Department of Medicine, They may be present as colonizers or pathogens in the respi- School of Medicine and Public Health, University of Wisconsin, ratory tract. Asymptomatic infection is probably far more Madison, WI, USA 3 Division of Infectious Disease, Department of Pediatrics, School of Medicine and Public Health, University of Wisconsin, Madison, WI, 1 M. tuberculosis complex members: M. africanum, M. bovis, M. cannetti, USA M. caprae, M. microti, M. pinnepedii,andM. tuberculosis. 6 Page 2 of 17 Curr Infect Dis Rep (2018) 20:6 frequent than disease. Antibodies against lipoarabinomannan, dissemination in immune-compromised hosts [27]. There is a glycolipid abundant in the cell wall of mycobacteria, are little evidence of person-to-person transmission of NTM, with detected in increasing numbers of healthy children after the thepossibleexceptionofM. abscessus,whichhasbeenim- age of 1 [8]. In the USA, skin test reactivity to Mycobacterium plicated in outbreaks of clonally related strains in cystic fibro- avium sensitin has been reported in 16% of adults who other- sis patients at two different centers [3•, 28, 29]. wise would have been misclassified as having latent tubercu- Mycobacteria elaborate a lipid-rich, waxy cell wall that losis infection (due to cross-reactivity of the immune response functions as a hydrophobic biofilm and allows organisms to to environmental mycobacteria and purified protein derivative adhere to hard surfaces, including pipes, drains, and tubing. (PPD)) [9]. In one survey, 33% of adults showed evidence of Biofilms inside pipes resist being physically dislodged despite prior, presumably subclinical, infection with M. avium [10]. high flow rates. Because of their biofilm-forming ability, en- In adults, NTM are most frequently associated with lung dis- vironmental mycobacteria are highly resistant to decontami- ease. In children, lymphadenitis is the most common disease nation with standard antiseptics and biocides, including chlor- manifestation and comprises 75 to 85% percent of total infections hexidine and glutaraldehyde [30–34]. As a result, mycobacte- [11, 12]. Other disease presentations include skin and soft tissue rial species are frequently found even in hospital environ- infection, tenosynovitis, septic arthritis, osteomyelitis, or keratitis ments and have been associated with outbreaks of nosocomial [3•, 13, 14]. Disseminated disease involving the blood, central infections following surgery or cosmetic procedures [35, 36, nervous system, or other dispersed sites can occur, particularly 37•, 38, 39, 40]. Clustered cases have also been reported from for more virulent species, such as M. avium and M. abscessus [5]. non-hospital settings, including tattoo parlors (M. chelonae, Immune-compromised hosts, including patients with ad- M. fortuitum); fish markets (M. marinum); and nail salons vanced HIV infection, organ or stem cell transplantation, and (M. chelonae, M. fortuitum, M. abscessus)[41–46]. individuals with Mendelian susceptibility to mycobacterial In contrast to M. tuberculosis, treatment regimens for NTM disease (MSMD), are also at greater risk of disseminated dis- infections have not been extensively studied in clinical trials. ease due to NTM [5, 15]. The latter individuals carry autoso- For most species, there are no standard regimens and our mal or X-linked mutations in genes within the interferon-gam- understanding of the role of antibiotic susceptibility testing ma/IL-12 immune response pathway [15]. Several naturally is incomplete [47]. Treatment decisions are thus largely based occurring polymorphism in TLR1 and TLR2, invariant recep- on case studies and expert opinion published in guidelines [3•, tors on the surface of immune cells that recognize bacterial 48–52]. Some emerging pathogens, such as M. abscessus,are lipopeptides, have also been associated with altered suscepti- highly drug-resistant and cannot be treated with typical bility to M. tuberculosis or M. leprae in human populations agents, which include macrolides, fluoroquinolones, amino- [16–20]. These data suggest that there are likely other com- glycosides, cefoxitin, imipenem, sulfamethoxazole, and tetra- mon variants in immune response genes that modulate human cyclines (other than tigecycline) [53]. Table 1 summarizes the susceptibility to clinically important NTMs via complex in- clinical presentation, notable features, and treatment of select- heritance (non-Mendelian) patterns. ed NTMs that cause SSTIs. Skin and soft tissue infections are the most common pre- sentation for the rapid-growing species Mycobacterium fortuitum, M. abscessus,andM. chelonae [3•]. Certain slow- Recent Epidemiology growing species of mycobacteria, namely Mycobacterium marinum, M. ulcerans, M. chimaera,andM. haemophilum, An accurate estimate of the burden of NTM disease in the are also more frequently associated with skin disease [3•, general population is limited by the fact that infections are 21–23]. However, virtually any species can localize to the skin not reportable in most countries, including the USA [3•, 51]. or soft tissues. Clinically, lesions may appear as papules, pus- Available evidence suggests, however, that NTM pulmonary tules, nodules, abscesses, panniculitis, folliculitis, or plaques. disease is increasing in North America, much of Europe, New They are typically erythematous or violaceous, but not warm. Zealand, Australia, and tertiary centers in East Asia [81•, 82]. Lesions may later become ulcerated [7]. Infection may present Data from China, India, and Africa are far from complete [81•, with a “sporotrichoid” pattern of spread, tracking along sub- 83, 84]. In the USA, the annual rate of pulmonary disease is cutaneous lymphatics from the site of inoculation proximally. currently 5–10/100,000 [81•]. Several US studies have shown This pattern is particularly classical for M. marinum cutaneous increases in the frequency of NTM infection [85•, 86, 87•]. disease [21, 24]. Skin and soft tissue infection (SSTI) may In the past, 75 to 80% of reported NTM disease represented follow minor trauma and inadvertent inoculation, such as oc- pulmonary infection [3•]. It is unclear whether this distribution curs when the skin is punctured by wood splinters, fish spines, is stable or changing. One single center series from a university or needles [21]. Infections can also arise through accidental hospital in France, for example, reported that pulmonary infec- contamination of surgical or open wounds [24–26]. Finally, tions made up only 54%
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