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      Nontuberculous Mycobacterial Infections in a French Hospital: A 12-Year Retrospective Study

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          Abstract

          Background

          Nontuberculous mycobacteria (NTM) are environmental organisms associated with a range of infections. Reports of NTM epidemiology are mainly focused on pulmonary infections and isolations, and extrapulmonary infections are less frequently described.

          Methods

          We conducted a retrospective study of NTM infections at the Bordeaux University Hospital, France, between January 2002 and December 2013. We used the microbiologic component of the American Thoracic Society/Infectious Diseases Society of America's pulmonary NTM disease criteria to define cases of pulmonary NTM, and patients with isolates from a normally sterile site were classified as having extrapulmonary disease.

          Results

          In our setting, 170 patients were included. Pulmonary cases predominated (54.1%), followed by skin and soft tissue infections (22.9%), disseminated cases (10.6%), lymphadenitis (7.7%), bone and joint infections (2.9%) and the remaining 1.8% catheter-related infections. Overall, 16 NTM species were isolated. Mycobacterium avium (31.8%) and M. intracellulare (20%) were the most common species identified, followed by M. marinum (13.5%), M. kansasii (10.6%), M. xenopi (9.4%), rapidly growing mycobacteria (9.4%) and other slowly growing mycobacteria (5.3%). In general, NTM isolates were largely prevalent in people older than 50 (62.4%); patients aged 1–10 year-old exclusively yielded M. avium from lymph nodes, almost cases having being diagnosed after 2007. Among the 121 patients with complete follow-up, 78 (64.5%), 24 (19.8%), and 19 (15.7%) were cured, experienced relapse, or died, respectively.

          Conclusion

          In our study, extrapulmonary NTM infections represented almost half of cases, consisting mainly in skin and soft tissue infections. The increase lymphadenitis cases in children after 2007 could be linked to the cessation of mandatory BCG vaccination in France. We observed similar cure rates (64%) between pulmonary and extrapulmonary infections.

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          Most cited references18

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          Nontuberculous mycobacterial disease prevalence and risk factors: a changing epidemiology.

          P Cassidy, Katrina Hedberg, Ashlen Saulson … (2009)
          Nontuberculous mycobacteria (NTM) are important human pathogens, yet little is known about disease prevalence in the United States. Reports suggest prevalence has increased, particularly in women, but population-based data to substantiate this are lacking. We sought to estimate NTM disease prevalence in Oregon, and describe disease by site, species, and patient demographic characteristics. We contacted laboratories that performed mycobacterial cultures on Oregon residents in 2005-2006. For each isolate, we obtained source, collection date, species, and patient demographics. We used the microbiologic component of the American Thoracic Society/Infectious Diseases Society of America's pulmonary NTM disease criteria to define cases of pulmonary NTM, and patients with isolates from a normally sterile site were classified as having extrapulmonary disease. We identified 933 patients with > or =1 NTM isolate. Of these, 527 (56%) met the case definition (annualized prevalence, 7.2 cases per 100,000 persons). Pulmonary cases predominated (5.6 cases per 100,000 persons), followed by skin/soft-tissue cases (0.9 cases per 100,000 persons). Mycobacterium avium complex was the most common species identified in pulmonary cases (4.7 cases per 100,000 persons). Pulmonary disease prevalence was significantly higher in women (6.4 cases per 100,000 persons) than men (4.7 cases per 100,000 persons) and was highest in persons aged >50 years (15.5 cases per 100,000 persons). NTM are frequently isolated from Oregon residents; more than one-half of all isolates likely represent true disease. Pulmonary NTM is most common among elderly women, and M. avium causes most disease. Future efforts to monitor disease trends should be undertaken, and efforts made to validate the use of the ATS/IDSA microbiologic criteria alone to predict pulmonary NTM disease.
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            Nontuberculous mycobacteria in the environment.

            Joseph Falkinham (2002)
            It is likely that the incidence of infection by environmental opportunistic mycobacteria will continue to rise. Part of the rise will be caused by the increased awareness of these microbes as human pathogens and improvements in methods of detection and culture. Clinicians and microbiologists will continue to be challenged by the introduction of new species to the already long list of mycobacterial opportunists (see Table 3). The incidence of infection will also rise because an increasing proportion of the population is aging or subject to some type of immunosuppression. A second reason for an increase in the incidence of environmental mycobacterial infection is that these microbes are everywhere. They are present in water, biofilms, soil, and aerosols. They are natural inhabitants of the human environment, especially drinking water distribution systems. Thus, it is likely that everyone is exposed on a daily basis. It is likely that certain human activities can lead to selection of mycobacteria. Important lessons have been taught by study of cases of hypersensitivity pneumonitis associated with exposure to metalworking fluid. First, the implicated metalworking fluids contained water, the likely source of the mycobacteria. Second, the metalworking fluids contain hydrocarbons (e.g., pine oils) and biocides (e.g., morpholine) both of which are substrates for the growth of mycobacteria [53,193]. Third, outbreak of disease followed disinfection of the metalworking fluid [136,137]. Although the metalworking fluid was contaminated with microorganisms, it was only after disinfection that symptoms developed in the workers. Because mycobacteria are resistant to disinfectants, it is likely that the recovery of the mycobacteria from the metalworking fluid [137] was caused by their selection. Disinfection may also contribute, in part, to the persistence of M avium and M intracellulare in drinking water distribution systems [33,89,240]. M avium and M intracellulare are many times more resistant to chlorine, chloramine, chlorine dioxide, and ozone than are other water-borne microorganisms [141,236]. Consequently, disinfection of drinking water results in selection of mycobacteria. In the absence of competitors, even the slowly growing mycobacteria can grow in the distribution system [33]. It is likely that hypersensitivity pneumonitis in lifeguards and therapy pool attendants [139] is caused by a similar scenario.
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              Impact of genotypic studies on mycobacterial taxonomy: the new mycobacteria of the 1990s.

              Enrico Tortoli (2003)
              The advancement of genetic techniques has greatly boosted taxonomic studies in recent years. Within the genus Mycobacterium, 42 new species have been detected since 1990, most of which were grown from clinical samples. Along with species for which relatively large numbers of strains have been reported, some of the new species of mycobacteria have been detected rarely or even only once. From the phenotypic point of view, among the new taxa, chromogens exceed nonchromogens while the numbers of slowly and rapidly growing species are equivalent. Whereas conventional identification tests were usually inconclusive, an important role was played by lipid analyses and in particular by high-performance liquid chromatography. Genotypic investigations based on sequencing of 16S rRNA gene have certainly made the most important contribution. The investigation of genetic relatedness led to the redistribution of the species previously included in the classically known categories of slow and rapid growers into new groupings. Within slow growers, the intermediate branch related to Mycobacterium simiae and the cluster of organisms related to Mycobacterium terrae have been differentiated; among rapid growers, the group of thermotolerant mycobacteria has emerged. The majority of species are resistant to isoniazid and, to a lesser extent, to rifampin. Many of the new species of mycobacteria are potentially pathogenic, and there are numerous reports of their involvement in diseases. Apart from disseminated and localized diseases in immunocompromised patients, the most frequent infections in immunocompetent people involve the lungs, skin, and, in children, cervical lymph nodes. The awareness of such new mycobacteria, far from being a merely speculative exercise, is therefore important for clinicians and microbiologists.
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                Author and article information

                Contributors
                Olivier Neyrolles: Role: Editor
                Journal
                Journal ID (nlm-ta): PLoS One
                Journal ID (iso-abbrev): PLoS ONE
                Journal ID (publisher-id): plos
                Journal ID (pmc): plosone
                Title: PLoS ONE
                Publisher: Public Library of Science (San Francisco, CA USA )
                ISSN (Electronic): 1932-6203
                Publication date (Electronic): 13 December 2016
                Publication date Collection: 2016
                Volume: 11
                Issue: 12
                Electronic Location Identifier: e0168290
                Affiliations
                [1 ]Service de maladies infectieuses et tropicales, Centre Hospitalier Universitaire de Bordeaux, Bordeaux, France
                [2 ]Laboratoire de Bactériologie, Centre Hospitalier Universitaire de Bordeaux, Bordeaux, France
                [3 ]Université de Bordeaux, Infections humaines à mycoplasmes et à chlamydiae, Bordeaux, France
                [4 ]INRA, Infections humaines à mycoplasmes et à chlamydiae, Bordeaux, France
                [5 ]Service de médecine interne, Centre Hospitalier Universitaire de Bordeaux, Bordeaux, France
                [6 ]Service de pneumologie, Centre Hospitalier Universitaire de Bordeaux, Bordeaux, France
                [7 ]Service de dermatologie, Centre Hospitalier Universitaire de Bordeaux, Bordeaux, France
                [8 ]Service de chirurgie plastique, reconstructrice et esthétique -brulés- chirurgie de la main, Centre Hospitalier Universitaire de Bordeaux, Bordeaux, France
                Institut de Pharmacologie et de Biologie Structurale, FRANCE
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                • Conceptualization: HD MD.

                • Data curation: PB HD OP.

                • Formal analysis: PB HD OP.

                • Investigation: PB HD OP.

                • Methodology: PB HD MD.

                • Project administration: MD.

                • Resources: PB OP FAD CC DN GW JP P. Morlat P. Mercié JT MSD PP MD.

                • Supervision: MD.

                • Validation: HD MD.

                • Visualization: PB HD OP MD.

                • Writing – original draft: PB HD OP FAD.

                • Writing – review & editing: PB HD OP MD.

                Article
                Publisher ID: PONE-D-16-36450
                DOI: 10.1371/journal.pone.0168290
                PMC ID: 5154556
                PubMed ID: 27959960
                SO-VID: 5655bba0-a95c-4128-b577-c0553b1f9e83
                Copyright © © 2016 Blanc et al
                License:

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                Date received : 10 September 2016
                Date accepted : 29 November 2016
                Page count
                Figures: 0, Tables: 3, Pages: 12
                Funding
                The authors received no specific funding for this work.
                Categories
                Subject: Research Article
                Subject: Biology and Life Sciences
                Subject: Organisms
                Subject: Bacteria
                Subject: Actinobacteria
                Subject: Mycobacterium Avium Complex
                Subject: Biology and Life Sciences
                Subject: Organisms
                Subject: Bacteria
                Subject: Actinobacteria
                Subject: Nontuberculous Mycobacteria
                Subject: Medicine and Health Sciences
                Subject: Pulmonology
                Subject: Respiratory Infections
                Subject: Medicine and Health Sciences
                Subject: Infectious Diseases
                Subject: Soft Tissue Infections
                Subject: Medicine and Health Sciences
                Subject: Pharmacology
                Subject: Drugs
                Subject: Antimicrobials
                Subject: Antibiotics
                Subject: Biology and Life Sciences
                Subject: Microbiology
                Subject: Microbial Control
                Subject: Antimicrobials
                Subject: Antibiotics
                Subject: Medicine and Health Sciences
                Subject: Dermatology
                Subject: Skin Infections
                Subject: Medicine and Health Sciences
                Subject: Infectious Diseases
                Subject: Skin Infections
                Subject: Medicine and Health Sciences
                Subject: Surgical and Invasive Medical Procedures
                Subject: Biopsy
                Subject: Medicine and Health Sciences
                Subject: Surgical and Invasive Medical Procedures
                Custom metadata
                Data Availability All relevant data are within the paper and its Supporting Information files.

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                ScienceOpen disciplines: Uncategorized

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