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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Nontuberculous Mycobacterial Musculoskeletal Infection Cases from a
Tertiary Referral Center, Colorado, USA</title><author><name sortKey="Goldstein, Noah" sort="Goldstein, Noah" uniqKey="Goldstein N" first="Noah" last="Goldstein">Noah Goldstein</name></author><author><name sortKey="St Clair, J Benjamin" sort="St Clair, J Benjamin" uniqKey="St Clair J" first="J. Benjamin" last="St. Clair">J. Benjamin St. Clair</name></author><author><name sortKey="Kasperbauer, Shannon H" sort="Kasperbauer, Shannon H" uniqKey="Kasperbauer S" first="Shannon H." last="Kasperbauer">Shannon H. Kasperbauer</name></author><author><name sortKey="Daley, Charles L" sort="Daley, Charles L" uniqKey="Daley C" first="Charles L." last="Daley">Charles L. Daley</name></author><author><name sortKey="Lindeque, Bennie" sort="Lindeque, Bennie" uniqKey="Lindeque B" first="Bennie" last="Lindeque">Bennie Lindeque</name></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">31107224</idno><idno type="pmc">6537735</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6537735</idno><idno type="RBID">PMC:6537735</idno><idno type="doi">10.3201/eid2506.181041</idno><date when="2019">2019</date><idno type="wicri:Area/Pmc/Corpus">000944</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000944</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Nontuberculous Mycobacterial Musculoskeletal Infection Cases from a
Tertiary Referral Center, Colorado, USA</title><author><name sortKey="Goldstein, Noah" sort="Goldstein, Noah" uniqKey="Goldstein N" first="Noah" last="Goldstein">Noah Goldstein</name></author><author><name sortKey="St Clair, J Benjamin" sort="St Clair, J Benjamin" uniqKey="St Clair J" first="J. Benjamin" last="St. Clair">J. Benjamin St. Clair</name></author><author><name sortKey="Kasperbauer, Shannon H" sort="Kasperbauer, Shannon H" uniqKey="Kasperbauer S" first="Shannon H." last="Kasperbauer">Shannon H. Kasperbauer</name></author><author><name sortKey="Daley, Charles L" sort="Daley, Charles L" uniqKey="Daley C" first="Charles L." last="Daley">Charles L. Daley</name></author><author><name sortKey="Lindeque, Bennie" sort="Lindeque, Bennie" uniqKey="Lindeque B" first="Bennie" last="Lindeque">Bennie Lindeque</name></author></analytic><series><title level="j">Emerging Infectious Diseases</title><idno type="ISSN">1080-6040</idno><idno type="eISSN">1080-6059</idno><imprint><date when="2019">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Early identification and aggressive treatment are crucial for patients with these
infections. </p></div></front><back><div1 type="bibliography"><listBibl><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct></listBibl></div1></back></TEI><pmc article-type="review-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Emerg Infect Dis</journal-id><journal-id journal-id-type="iso-abbrev">Emerging Infect. Dis</journal-id><journal-id journal-id-type="publisher-id">EID</journal-id><journal-title-group><journal-title>Emerging Infectious Diseases</journal-title></journal-title-group><issn pub-type="ppub">1080-6040</issn><issn pub-type="epub">1080-6059</issn><publisher><publisher-name>Centers for Disease Control and Prevention</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">31107224</article-id><article-id pub-id-type="pmc">6537735</article-id><article-id pub-id-type="publisher-id">18-1041</article-id><article-id pub-id-type="doi">10.3201/eid2506.181041</article-id><article-categories><subj-group subj-group-type="heading"><subject>Synopsis</subject></subj-group><subj-group subj-group-type="article-type"><subject>Synopsis</subject></subj-group><subj-group subj-group-type="TOC-title"><subject>Nontuberculous Mycobacterial Musculoskeletal Infection Cases from a Tertiary Referral Center, Colorado, USA</subject></subj-group></article-categories><title-group><article-title>Nontuberculous Mycobacterial Musculoskeletal Infection Cases from a
Tertiary Referral Center, Colorado, USA</article-title><alt-title alt-title-type="running-head">Nontuberculous Mycobacterial
Infections</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Goldstein</surname><given-names>Noah</given-names></name><xref ref-type="fn" rid="FN1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>St. Clair</surname><given-names>J. Benjamin</given-names></name><xref ref-type="fn" rid="FN1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Kasperbauer</surname><given-names>Shannon H.</given-names></name></contrib><contrib contrib-type="author"><name><surname>Daley</surname><given-names>Charles L.</given-names></name></contrib><contrib contrib-type="author" corresp="yes"><name><surname>Lindeque</surname><given-names>Bennie</given-names></name></contrib><aff id="aff1">University of Colorado, Aurora, Colorado, USA (N. Goldstein, J.B. St. Clair, S.H. Kasperbauer, B. Lindeque);</aff><aff id="aff2">University of Chicago, Chicago, Illinois, USA (J.B. St. Clair);</aff><aff id="aff3">National Jewish Health, Denver, Colorado, USA (S.H. Kasperbauer, C.L. Daley)</aff></contrib-group><author-notes><corresp id="cor1">Address for correspondence: Bennie Lindeque, University of
Colorado, 12631 E 17th Ave, Academic Office 1, Rm 4602, Mailstop B202, Aurora,
CO 80045, USA; email: <email xlink:href="bennie.lindeque@ucdenver.edu">bennie.lindeque@ucdenver.edu</email></corresp></author-notes><pub-date pub-type="ppub"><month>6</month><year>2019</year></pub-date><volume>25</volume><issue>6</issue><fpage>1075</fpage><lpage>1083</lpage><abstract abstract-type="toc"><p>Early identification and aggressive treatment are crucial for patients with these
infections. </p></abstract><abstract><p>Nontuberculous mycobacteria represent an uncommon but important cause of
infection of the musculoskeletal system. Such infections require aggressive
medical and surgical treatment, and cases are often complicated by delayed
diagnosis. We retrospectively reviewed all 14 nonspinal cases of nontuberculous
mycobacterial musculoskeletal infections treated over 6 years by orthopedic
surgeons at a university-affiliated tertiary referral center. All patients
required multiple antimicrobial agents along with aggressive surgical treatment;
13 of 14 patients ultimately achieved cure. Four patients required amputation to
control the infection. Half these patients were immunosuppressed by medications
or other medical illness when they sought care at the referral center. Six cases
involved joint prostheses; all ultimately required hardware removal and
placement of an antimicrobial spacer for eradication of infection. Our findings
highlight the importance of vigilance for nontuberculous mycobacterial
musculoskeletal infection, particularly in patients who are immunosuppressed or
have a history of musculoskeletal surgery.</p></abstract><kwd-group kwd-group-type="author"><title>Keywords: </title><kwd>nontuberculous mycobacteria</kwd><kwd><italic>Mycobacterium</italic></kwd><kwd>musculoskeletal diseases</kwd><kwd>prosthesis-related infections</kwd><kwd>osteomyelitis</kwd><kwd>infectious arthritis</kwd><kwd>tuberculosis and other mycobacteria</kwd><kwd>antimicrobial resistance</kwd><kwd>Colorado</kwd><kwd>United States</kwd></kwd-group></article-meta></front><body><p>Nontuberculous mycobacteria (NTM) are opportunistic pathogens found in soil and water and
are the sources of an increasing number of infections and illness (<xref rid="R1" ref-type="bibr"><italic>1</italic></xref>,<xref rid="R2" ref-type="bibr"><italic>2</italic></xref>). Multiple recent studies have recognized this temporal
trend of increasing annual prevalence of NTM disease; current prevalence is estimated at
2.6%–10% annually (<xref rid="R1" ref-type="bibr"><italic>1</italic></xref>–<xref rid="R4" ref-type="bibr"><italic>4</italic></xref>). NTM cause a broad range of clinical manifestations,
depending on the immune competency of the host. Pulmonary disease is most common and is
often seen in immunocompetent hosts. It is difficult to estimate the prevalence of
extrapulmonary NTM infection in the United States because no system of national
surveillance and reporting exists as for tuberculosis. Reported laboratory isolation
data indicate that extrapulmonary disease may comprise up to one quarter of all NTM
infections, although the best estimates are based on data that are 1–3 decades
old. Data from the mid-1990s estimated the overall US incidence of NTM infection at
1.0%–1.8%, with ≈5% of isolates reported to the Centers for Disease
Control and Infection at that time being of extrapulmonary origin. A population-based
record review in Oregon that used data gathered during 2005–2006 found
≈22% of isolates originating from nonpulmonary specimens. Data from North
Carolina gathered during 2006–2010 showed 16%–23% of total isolates
originating from extrapulmonary specimens (<xref rid="R5" ref-type="bibr"><italic>5</italic></xref>–<xref rid="R7" ref-type="bibr"><italic>7</italic></xref>). Skin and soft tissue infections represent most
extrapulmonary NTM disease, whereas bone and joint disease is less common. With
increasing immunosuppression, NTM is more likely to manifest as disseminated disease,
possibly including bone and joint involvement.</p><p>Previous case reports and series of NTM musculoskeletal infections have focused on the
demographics, diagnosis, and treatment of patients with these difficult-to-manage
infections (<xref rid="R8" ref-type="bibr"><italic>8</italic></xref>–<xref rid="R24" ref-type="bibr"><italic>24</italic></xref>). Patients were often
immunocompetent persons who contracted an NTM disease after direct inoculation via
traumatic skin puncture (<xref rid="R25" ref-type="bibr"><italic>25</italic></xref>–<xref rid="R28" ref-type="bibr"><italic>28</italic></xref>). In a series of 29 cases from South Korea, all
patients required surgical intervention in addition to antimicrobial drugs; 3 patients
failed to respond despite aggressive treatment, and an additional 4 were lost to
follow-up. Of note, only 20 of the patients in this series received NTM-specific
antimicrobial therapy; the remainder were treated with empirical antimicrobial therapy.
A series of 28 cases of <italic>M. marinum</italic> musculoskeletal infections found
that 93% of cases involved fingers or hands and 87% were related to aquatic exposure;
two thirds progressed from cutaneous to invasive infection. Most cases were managed with
multiple antimycobacterial agents in addition to surgery, and the series reported a 75%
cure rate and 25% loss to follow-up. A study of 8 cases of prosthetic joint infection
(PJI) caused by rapidly growing mycobacteria found that the median interval from
prosthesis implantation to infection was 312 weeks and that all patients required either
resection and explantation of infected prostheses or chronic suppressive antimicrobial
therapy.</p><p>In these series, infections occurred throughout the musculoskeletal system but were
particularly common in the hands and spine. Identification of NTM as the causative agent
was often delayed due to the indolent course of the infection and lack of appropriate
diagnostic testing. Once identified, the infections could be treated effectively with a
combination of debridement and conventional antimycobacterial chemotherapy.</p><p>We reviewed all cases of nonspinal NTM musculoskeletal infection treated at the
University of Colorado Hospital (UCH; Aurora, CO, USA) over a 6-year period by a
multidisciplinary team of providers at UCH and National Jewish Health (NJH; Denver, CO,
USA), a renowned center for mycobacterial research and treatment that receives referrals
for difficult-to-treat NTM infections from across the United States. Our aim was to
describe the clinical characteristics and treatment outcomes of patients with NTM
musculoskeletal infections.</p><sec sec-type="materials|methods"><title>Materials and Methods</title><sec><title>Study Design</title><p>We performed a retrospective study of patients with nonspinal NTM musculoskeletal
infections treated at UCH during 2009–2015. The management of each case
was directed by an orthopedic surgeon and infectious disease physicians at UCH
and NJH. For patients with positive culture results at UCH, mycobacterial
speciation and susceptibility data were identified by ARUP Laboratories
(<ext-link ext-link-type="uri" xlink:href="https://www.aruplab.com">https://www.aruplab.com</ext-link>) using DNA sequencing or matrix-assisted
laser desorption/ionization time-of-flight mass spectrometry.</p></sec><sec><title>Case Ascertainment</title><p>We identified all cases of nonspinal NTM musculoskeletal infections treated by
orthopedic surgeons at UCH during the study period using a registry of NTM
musculoskeletal infections. We omitted spinal cases because they are handled by
a different department at UCH and so were not part of the surgeons’
personal registry. We reviewed the medical records of patients after approval
from the Institutional Review Board.</p></sec><sec><title>Data Collection</title><p>We performed our review of the medical records using a standardized case report
form. We collected demographic characteristics and data on concurrent
conditions, laboratory values, surgical intervention, antimycobacterial
chemotherapy, and outcomes.</p></sec><sec><title>Literature Review </title><p>We searched the Medline database to identify case reports and reviews of NTM
musculoskeletal infections. We used both the PubMed and Ovid access tools.</p></sec></sec><sec sec-type="results"><title>Results</title><sec><title>Patient Characteristics</title><p>Of the 14 patients in our series, 7 were receiving immunosuppressive medications
at arrival, and 5 of those had chronic autoimmune disease. Twelve patients were
referred from NJH. No predisposing host factor was identified for 6 patients.
(<xref rid="T1" ref-type="table">Table 1</xref>).</p><table-wrap id="T1" position="float"><label>Table 1</label><caption><title>Demographics of patients in retrospective study of nontuberculous
mycobacterial musculoskeletal infections, Colorado, USA*</title></caption><table frame="hsides" rules="groups"><col width="31" span="1"></col><col width="31" span="1"></col><col width="85" span="1"></col><col width="63" span="1"></col><col width="40" span="1"></col><col width="72" span="1"></col><col width="58" span="1"></col><col width="89" span="1"></col><thead><tr><th valign="bottom" align="left" scope="col" rowspan="1" colspan="1">Patient no. </th><th valign="bottom" align="center" scope="col" rowspan="1" colspan="1">Age, y/sex</th><th valign="bottom" align="center" scope="col" rowspan="1" colspan="1">Immunocompromising
conditions</th><th valign="bottom" align="center" scope="col" rowspan="1" colspan="1">Inciting or
predisposing factor(s)</th><th valign="bottom" align="center" scope="col" rowspan="1" colspan="1">Time to symptom
onset, mo</th><th valign="bottom" align="center" scope="col" rowspan="1" colspan="1">Reason care
sought</th><th valign="bottom" align="center" scope="col" rowspan="1" colspan="1">Time from symptom
onset to diagnosis, mo </th><th valign="bottom" align="center" scope="col" rowspan="1" colspan="1">Diagnostic procedure,
source of microbiologic diagnosis</th></tr></thead><tbody><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">1</td><td valign="top" align="center" rowspan="1" colspan="1">55/M</td><td valign="top" align="center" rowspan="1" colspan="1">History of lymphoma, pseudogout,
oral steroid use</td><td valign="top" align="center" rowspan="1" colspan="1">Steroid injection, left ankle</td><td valign="top" align="center" rowspan="1" colspan="1">UNK</td><td valign="top" align="center" rowspan="1" colspan="1">Osteomyelitis, septic arthritis</td><td valign="top" align="center" rowspan="1" colspan="1">12</td><td valign="top" align="center" rowspan="1" colspan="1">Tissue sample from ankle
debridement</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">2</td><td valign="top" align="center" rowspan="1" colspan="1">53/F</td><td valign="top" align="center" rowspan="1" colspan="1">None</td><td valign="top" align="center" rowspan="1" colspan="1">Pedicure</td><td valign="top" align="center" rowspan="1" colspan="1">0</td><td valign="top" align="center" rowspan="1" colspan="1">Synovitis, osteomyelitis,
cellulitis</td><td valign="top" align="center" rowspan="1" colspan="1">4</td><td valign="top" align="center" rowspan="1" colspan="1">UNK; diagnosis at another hospital
</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">3</td><td valign="top" align="center" rowspan="1" colspan="1">48/F</td><td valign="top" align="center" rowspan="1" colspan="1">None</td><td valign="top" align="center" rowspan="1" colspan="1">Second THA</td><td valign="top" align="center" rowspan="1" colspan="1">UNK</td><td valign="top" align="center" rowspan="1" colspan="1">PJI</td><td valign="top" align="center" rowspan="1" colspan="1">UNK</td><td valign="top" align="center" rowspan="1" colspan="1">Thigh fluid sampled during
I&D</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">4</td><td valign="top" align="center" rowspan="1" colspan="1">45/M</td><td valign="top" align="center" rowspan="1" colspan="1">None</td><td valign="top" align="center" rowspan="1" colspan="1">AKA</td><td valign="top" align="center" rowspan="1" colspan="1">1</td><td valign="top" align="center" rowspan="1" colspan="1">Draining wound at stump</td><td valign="top" align="center" rowspan="1" colspan="1">2</td><td valign="top" align="center" rowspan="1" colspan="1">Sample of fluid draining from AKA
stump</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">5</td><td valign="top" align="center" rowspan="1" colspan="1">64/F</td><td valign="top" align="center" rowspan="1" colspan="1">None</td><td valign="top" align="center" rowspan="1" colspan="1">Carpal tunnel release</td><td valign="top" align="center" rowspan="1" colspan="1">0</td><td valign="top" align="center" rowspan="1" colspan="1">Tenosynovitis, septic arthritis</td><td valign="top" align="center" rowspan="1" colspan="1">8</td><td valign="top" align="center" rowspan="1" colspan="1">Synovial fluid obtained during
excision of synovitis</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">6</td><td valign="top" align="center" rowspan="1" colspan="1">69/F</td><td valign="top" align="center" rowspan="1" colspan="1">Diabetes mellitus</td><td valign="top" align="center" rowspan="1" colspan="1">THA</td><td valign="top" align="center" rowspan="1" colspan="1">6</td><td valign="top" align="center" rowspan="1" colspan="1">PJI</td><td valign="top" align="center" rowspan="1" colspan="1">9</td><td valign="top" align="center" rowspan="1" colspan="1">Synovial biopsy obtained during
explantation</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">7</td><td valign="top" align="center" rowspan="1" colspan="1">23/F</td><td valign="top" align="center" rowspan="1" colspan="1">Systemic lupus erythematosus, oral
steroids, hydroxyl-chloroquine, mycophenolate mofetil</td><td valign="top" align="center" rowspan="1" colspan="1">Avascular necrosis, ankle
fusion</td><td valign="top" align="center" rowspan="1" colspan="1">3</td><td valign="top" align="center" rowspan="1" colspan="1">Septic arthritis, osteomyelitis,
skin abscesses</td><td valign="top" align="center" rowspan="1" colspan="1">1</td><td valign="top" align="center" rowspan="1" colspan="1">UNK; diagnosis at another
hospital</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">8</td><td valign="top" align="center" rowspan="1" colspan="1">57/F</td><td valign="top" align="center" rowspan="1" colspan="1">Polymyositis, oral steroids,
azathioprine, rituximab, methotrexate</td><td valign="top" align="center" rowspan="1" colspan="1">ACL repair, arthroscopy, steroid
injection</td><td valign="top" align="center" rowspan="1" colspan="1">UNK</td><td valign="top" align="center" rowspan="1" colspan="1">Septic arthritis</td><td valign="top" align="center" rowspan="1" colspan="1">UNK</td><td valign="top" align="center" rowspan="1" colspan="1">Aspirate of left knee and right
hip</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">9</td><td valign="top" align="center" rowspan="1" colspan="1">76/M</td><td valign="top" align="center" rowspan="1" colspan="1">Nonspecific autoimmune disease, oral
steroids</td><td valign="top" align="center" rowspan="1" colspan="1">Calcium pyrophosphate deposition
disease, TKA</td><td valign="top" align="center" rowspan="1" colspan="1">0</td><td valign="top" align="center" rowspan="1" colspan="1">PJI</td><td valign="top" align="center" rowspan="1" colspan="1">2</td><td valign="top" align="center" rowspan="1" colspan="1">UNK; diagnosis at another
hospital</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">10</td><td valign="top" align="center" rowspan="1" colspan="1">58/M</td><td valign="top" align="center" rowspan="1" colspan="1">None</td><td valign="top" align="center" rowspan="1" colspan="1">Trauma, steroid injection</td><td valign="top" align="center" rowspan="1" colspan="1">12</td><td valign="top" align="center" rowspan="1" colspan="1">Septic arthritis</td><td valign="top" align="center" rowspan="1" colspan="1">19</td><td valign="top" align="center" rowspan="1" colspan="1">UNK; diagnosis at another
hospital</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">11</td><td valign="top" align="center" rowspan="1" colspan="1">77/F</td><td valign="top" align="center" rowspan="1" colspan="1">Rheumatoid arthritis, prednisone,
azathioprine</td><td valign="top" align="center" rowspan="1" colspan="1">TKA</td><td valign="top" align="center" rowspan="1" colspan="1">300</td><td valign="top" align="center" rowspan="1" colspan="1">PJI</td><td valign="top" align="center" rowspan="1" colspan="1">12</td><td valign="top" align="center" rowspan="1" colspan="1">Synovial biopsy obtained during
placement of antimicrobial spacer</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">12</td><td valign="top" align="center" rowspan="1" colspan="1">83/M</td><td valign="top" align="center" rowspan="1" colspan="1">Malnutrition, prednisone</td><td valign="top" align="center" rowspan="1" colspan="1">TKA</td><td valign="top" align="center" rowspan="1" colspan="1">168</td><td valign="top" align="center" rowspan="1" colspan="1">PJI</td><td valign="top" align="center" rowspan="1" colspan="1">8</td><td valign="top" align="center" rowspan="1" colspan="1">Tissue obtained during TKA
revision</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">13</td><td valign="top" align="center" rowspan="1" colspan="1">49/F</td><td valign="top" align="center" rowspan="1" colspan="1">None</td><td valign="top" align="center" rowspan="1" colspan="1">TKA (revision)</td><td valign="top" align="center" rowspan="1" colspan="1">14</td><td valign="top" align="center" rowspan="1" colspan="1">PJI</td><td valign="top" align="center" rowspan="1" colspan="1">2</td><td valign="top" align="center" rowspan="1" colspan="1">UNK; diagnosis at another
hospital</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">14</td><td valign="top" align="center" rowspan="1" colspan="1">24/F</td><td valign="top" align="center" rowspan="1" colspan="1">Crohn’s disease,
infliximab</td><td valign="top" align="center" rowspan="1" colspan="1">Failed IV</td><td valign="top" align="center" rowspan="1" colspan="1">0</td><td valign="top" align="center" rowspan="1" colspan="1">Cellulitis, abscess</td><td valign="top" align="center" rowspan="1" colspan="1">7</td><td valign="top" align="center" rowspan="1" colspan="1">Skin biopsy</td></tr></tbody></table><table-wrap-foot><p>*AKA, above-knee amputation; I&D, irrigation and debridement;
PJI, prosthetic joint infection, THA, total hip
arthroplasty; TKA, total knee arthroplasty; UNK, unknown.</p></table-wrap-foot></table-wrap></sec><sec><title>Clinical Presentation and Diagnosis</title><p>The patients had a wide array of sites of infection when they sought care at UCH
(5 knee, 2 hip, 1 thigh, 1 hand, 1 foot, 1 elbow, 3 with disseminated disease at
multiple sites). The diagnosis at arrival was most commonly PJI (n = 6); the
next most common diagnoses included septic arthritis (n = 5), osteomyelitis (n =
3), tendon sheath infection (n = 2), skin abscess (n = 2), cellulitis (n = 2),
and surgical-wound infection (n = 1). Several patients had complex local
infections with multiple concurrent tissue diagnoses; case-patients 1, 7, and 8
had disseminated disease at multiple sites. Each patient had undergone
<underline>></underline>1 prior procedure at the site of infection,
including 6 patients with infected prostheses, 4 with other surgical procedures,
2 with steroid injection, 1 with a failed intravenous (IV) placement, and 1 with
a cosmetic pedicure. The median interval from symptom onset to diagnosis was 7.5
months (range 1–19 months). </p><p>Of 10 patients tested, the median erythrocyte sedimentation rate (ESR) was above
the upper limit of normal (ULN) in 7 patients (70%) at arrival (ULN 15 mm/h in
men, 20 mm/h in women). C-reactive protein level was elevated in 4/14 patients
(29%) (ULN 10.0 mg/L). Blood leukocyte count was elevated in 2/14 patients (14%)
(ULN 10.1 × 10<sup>4</sup> cells/μL). All 3 laboratory tests were
within reference limits in 1 patient, and both C-reactive protein and leukocyte
levels were within reference limits in an additional 2 patients without ESR
data.</p></sec><sec><title>PJIs</title><p>Six patients arrived with PJI at the knee (4 patients) and hip (2 patients). The
interval from prosthesis implantation to symptom onset ranged from the immediate
aftermath of implantation to 25 years postimplantation; median duration was 6
months. Infected hardware was removed in all patients with PJI; the median
period from symptom onset to explantation was 8.5 months (range <3–16
months). After explantation, 2-stage revision was undertaken, first with
implantation of a temporary articulating prosthesis prepared with 1 g of
antimicrobial-loaded polymethylmethacrylate bone cement, with drug selection
based on sensitivity testing. This preparation, called an antimicrobial spacer,
was subsequently replaced with a permanent prosthesis after several months
without evidence of recurrent infection. Medication-loaded bone cement was also
used for patients requiring intramedullary nailing. Patients with PJI were also
treated with amikacin-containing calcium sulfate beads implanted within the
surgical bed (1 g of amikacin per 10 cc packet of calcium sulfate mixture).
These antimicrobial beads were used at initial explantation or when the
antimicrobial spacer was replaced with a permanent prosthesis at the discretion
of the surgeon as needed to fill dead space from aggressive debridement or the
infection itself. The precise amount of amikacin used is not always clearly
reflected in the surgical record; however, in our series, use of up to 5 g of
amikacin has been recorded. Amikacin is used for its activity against
mycobacteria and its ability to integrate with the calcium sulfate material to
form beads. Such amikacin-laden beads were also used in 2 other patients with
extensive soft-tissue involvement. A seventh patient with septic arthritis of
her native knee (case-patient 8) underwent a total knee arthroplasty that was
insufficient to eradicate the infection and ultimately required subsequent
2-stage revision.</p></sec><sec><title>Surgical Treatment</title><p>All patients required surgical treatment for control of infection, and all but 1
patient were ultimately cured by combined medical and surgical treatment. Seven
patients had <underline>></underline>1 procedure at outside hospitals before
seeking treatment at UCH. Case-patients 4 and 5 required only a single surgical
procedure at UCH for control of infection. Case-patients 6 and 12 underwent
planned 2-stage revision and required no further surgeries. The remaining 10
case-patients had initial procedures at UCH that were intended to definitively
treat infection but proved unsuccessful. Surgical treatment at UCH consisted of
aggressive debridement of infected bone and soft tissue, as well as explantation
of any infected hardware with 2-stage revision of infected prostheses. Four
patients with infections involving the knee also required placement of
intramedullary nails coated with antibiotic-loaded cement (case-patients 9, 10,
11, and 13). The median interval from initial diagnostic or therapeutic
procedure to definitive surgical treatment was 14 months (range 4–52
months) in the patients who required multiple procedures. One patient with
disseminated <italic>M. abscessus</italic> (case-patient 1) required a
debridement of the femur, partial claviculectomy, synovectomy of an ankle and a
knee, and a fasciectomy. The patient with disseminated <italic>M.
massiliense</italic> in the setting of chronic immunosuppressive therapy
(case-patient 7) required <underline>></underline>12 procedures including
multiple debridements and soft tissue excisions, removal of infected ankle
fusion hardware, and osteotomy and arthrotomy of an infected elbow with
extensive use of antimicrobial beads and bone cement. A patient with <italic>M.
intracellulare</italic> infection disseminated to the left knee and right
hip (case-patient 8) required multiple irrigations and debridements, total knee
arthroplasty with antimicrobial spacer, and subsequent implantation of a tumor
prosthesis. One patient with <italic>M. fortuitum</italic> infection
(case-patient 5) had a debridement and eventually required amputation of her
hand. One patient had cellulitis and abscess formation caused by <italic>M.
marinum</italic> (case-patient 14) requiring a wide excision of the soft
tissue around her elbow. One patient with a hip-prosthetic infection caused by
<italic>M. abscessus</italic> (case-patient 3) required hemipelvectomy due
to the progressive spread of the infection despite >1 year of intravenous
therapy, prosthetic hip explantation, and multiple debridements (<xref rid="T2" ref-type="table">Table 2</xref>).</p><table-wrap id="T2" position="float"><label>Table 2</label><caption><title>Surgical treatment of patients with nontuberculous mycobacterial
musculoskeletal infections, Colorado, USA*</title></caption><table frame="hsides" rules="groups"><col width="32" span="1"></col><col width="37" span="1"></col><col width="60" span="1"></col><col width="54" span="1"></col><col width="94" span="1"></col><col width="67" span="1"></col><col width="45" span="1"></col><col width="49" span="1"></col><col width="41" span="1"></col><thead><tr><th rowspan="2" valign="bottom" align="left" scope="col" colspan="1">Patient
no.</th><th rowspan="2" valign="bottom" align="center" scope="col" colspan="1">Site</th><th rowspan="2" valign="bottom" align="center" scope="col" colspan="1">Previous
surgeries</th><th rowspan="2" valign="bottom" align="center" scope="col" colspan="1">Symptom
onset to first surgery, mo</th><th valign="bottom" colspan="2" align="center" scope="colgroup" rowspan="1">Surgeries for control of infection at UCH<hr></hr></th><th rowspan="2" valign="bottom" align="center" scope="col" colspan="1">Time
between surgeries, mo</th><th rowspan="2" valign="bottom" align="center" scope="col" colspan="1">First
visit to definitive procedure, mo</th><th rowspan="2" valign="bottom" align="center" scope="col" colspan="1">Length of
follow-up, mo</th></tr><tr><th valign="bottom" colspan="1" align="center" scope="colgroup" rowspan="1">First procedure(s)</th><th valign="bottom" align="center" scope="col" rowspan="1" colspan="1">Definitive
procedure</th></tr></thead><tbody><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">1<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">Multiple joints† <hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">Multiple I&Ds, below-knee
amputation<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">UNK<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">I&D, excision of soft-tissue
masses, debridement, synovectomy, amikacin bead implantation
<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">Wide excision of right
calf<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">36<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">22<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">7<hr></hr></td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">2<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">Left foot<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">Debridement, amputation L 5th toe,
nodule excision<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">2<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">Debridement of dorsum of left
foot<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">Excisional debridement of left
foot<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">17<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">14<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">60<hr></hr></td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">3<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">Left hip (PJI)<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">UNK<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">UNK<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">Debridement and polyethylene
exchange<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">Hemi-pelvectomy<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">31<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">38<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">14<hr></hr></td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">4<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">Left thigh<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">None<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">18<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">NA<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">Above-knee amputation stump
revision<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">NA<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">14<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">1<hr></hr></td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">5<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">Right hand<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">None<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">9<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">NA<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">Amputation of right hand and
forearm<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">NA<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">3<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">37<hr></hr></td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">6<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">Right hip (PJI)<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">None<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">9<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">Resection arthroplasty, tobramycin
cement spacer<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">Revision THA<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">4<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">6<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">49<hr></hr></td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">7<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">Multiple joints‡<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">I&D<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">1<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">Hardware removal, I&D, amikacin
bead implantation, arthrotomy and osteotomy with amikacin
cement, soft-tissue excisions<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">Excisional debridement of left
forearm and right foot with amikacin bead
placement§<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">51<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">51<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">2<hr></hr></td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">8<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">Left knee, right hip<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">None<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">UNK<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">I&D, amikacin cement
spacer<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">TKA with tumor prosthesis,
gentamicin cement, amikacin beads<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">7<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">8<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">48<hr></hr></td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">9<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">Left knee (PJI)<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">Explant with antimicrobial spacer,
I&D<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">4<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">I&D, explantation, tobramycin
spacer, intramedullary nail with tobramycin cement, revision of
spacer<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">Revision TKA with tobramycin cement
and amikacin beads<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">20<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">12<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">20<hr></hr></td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">10<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">Left knee<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">Arthroscopic meniscectomy, synovial
biopsy, aspirations, arthroscopic synovectomy<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">2<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">Radical synovectomy, amikacin bead
implantation, resection arthroplasty, knee-spanning
intramedullary nail with tobramycin cement<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">TKA with tumor prosthesis and
tobramycin cement<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">40<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">12<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">4<hr></hr></td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">11<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">Right knee (PJI)<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">None<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">12<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">Explantation, amikacin spacer,
I&D, intramedullary nail with amikacin cement<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">Revision TKA with gentamicin cement
and amikacin beads<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">7<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">11<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">17<hr></hr></td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">12<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">Left knee (PJI)<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">I&D, polyethylene
exchange<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">0<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">Explantation, gentamicin cement
spacer<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">Revision TKA with tobramycin cement
and amikacin beads<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">12<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">5<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">20<hr></hr></td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">13<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">Right knee (PJI)<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">Explant, I&D, antimicrobial
spacers<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">3<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">Revision TKA, I&D,
intramedullary nail with amikacin cement<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">Revision TKA with amikacin cement
and amikacin beads<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">14<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">6<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">1<hr></hr></td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">14</td><td valign="top" align="center" rowspan="1" colspan="1">Right elbow</td><td valign="top" align="center" rowspan="1" colspan="1">None</td><td valign="top" align="center" rowspan="1" colspan="1">8</td><td valign="top" align="center" rowspan="1" colspan="1">Wide excision of right forearm,
nodule excision</td><td valign="top" align="center" rowspan="1" colspan="1">Wide excision of right forearm</td><td valign="top" align="center" rowspan="1" colspan="1">4</td><td valign="top" align="center" rowspan="1" colspan="1">10</td><td valign="top" align="center" rowspan="1" colspan="1">47</td></tr></tbody></table><table-wrap-foot><p>*I&D, irrigation and debridement; NA, not applicable;
PJI, prosthetic joint infection, THA, total hip
arthroplasty; TKA, total knee arthroplasty; UNK,
unknown.
†Infection was present in patient’s left
thigh and knee, and right talus, ankle joint, and subtalar
joint.
‡Infection was present in patient’s left
elbow, buttock, forearm, calf, right ankle and thigh, and both feet.
§Because this patient is in treatment for chronic
disseminated infection, definitive procedure is defined as the most
recent surgical procedure.</p></table-wrap-foot></table-wrap></sec><sec><title>Histopathology and Microbiology</title><p>The species of NTM responsible for the musculoskeletal infection was known or
identified in each patient. All patients had tissue specimens taken for culture
during their procedure(s) at UCH. Eight patients had microbiologic diagnoses of
NTM infection before transfer to UCH, and 6 of these patients were
culture-negative at the time of surgery at UCH (case-patients 1, 2, 4, 8, 9, and
13). Antimicrobial therapy was initiated at outside hospitals in 6 of the 8
patients who came to UCH with established microbiologic diagnoses; the other 2
patients were referred directly to infectious diseases specialists at UCH, NJH,
or both for treatment. </p><p>Seven patients were infected with a rapidly growing mycobacterial species,
whereas the remaining 7 were infected with slowly growing species (<xref rid="T1" ref-type="table">Table 1</xref>). Ten patients had intraoperative
biopsy specimens demonstrating granuloma formation, but only 2 of these had
evidence of acid-fast bacilli on direct microscopy. Eight of 14 patients had
intraoperative cultures that grew NTM, with speciation consistent with prior
data when available. All patients had visual evidence of infection at the time
of operation. One patient who had <italic>M. marinum</italic> worked at a pet
store that sold fish and aquariums and frequently submerged her hands and arms
in the water, and her infection originated at a failed IV site. In the 5
patients with <italic>M. avium</italic> complex, 3 had speciation available that
identified <italic>M. intracellulare</italic>.</p></sec><sec><title>Antimicrobial Treatment</title><p>All patients were treated with combination antimycobacterial chemotherapy (<xref rid="T3" ref-type="table">Table 3</xref>) determined on the basis of
antimicrobial drug sensitivities (<xref ref-type="local-data" rid="SD1">Appendix</xref> Table) and recommendations from NJH. Thirteen of 14
patients were receiving antimycobacterial therapy at the time of surgery based
on previous culture and drug susceptibility test results. Antimicrobial therapy
was not administered around the time of surgery for case-patient 7 because of
adverse effects from these medications. </p><table-wrap id="T3" position="float"><label>Table 3</label><caption><title>Microbiology and antimicrobial treatment of patients with
nontuberculous mycobacterial musculoskeletal infections, Colorado,
USA*</title></caption><table frame="hsides" rules="groups"><col width="31" span="1"></col><col width="68" span="1"></col><col width="98" span="1"></col><col width="81" span="1"></col><col width="58" span="1"></col><col width="99" span="1"></col><col width="45" span="1"></col><thead><tr><th valign="bottom" align="left" scope="col" rowspan="1" colspan="1">Patient no.</th><th valign="bottom" align="center" scope="col" rowspan="1" colspan="1">Species</th><th valign="bottom" align="center" scope="col" rowspan="1" colspan="1">Oral therapy
(duration, mo)</th><th valign="bottom" align="center" scope="col" rowspan="1" colspan="1">Intravenous therapy
(duration, mo)</th><th valign="bottom" align="center" scope="col" rowspan="1" colspan="1">Total duration of
therapy, mo</th><th valign="bottom" align="center" scope="col" rowspan="1" colspan="1">Time from last
surgery to cessation of antimicrobial therapy, mo</th><th valign="bottom" align="center" scope="col" rowspan="1" colspan="1">Outcome</th></tr></thead><tbody><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">1</td><td valign="top" align="center" rowspan="1" colspan="1"><italic>M. abscessus</italic></td><td valign="top" align="center" rowspan="1" colspan="1">Azithromycin (24)</td><td valign="top" align="center" rowspan="1" colspan="1">Tigecycline + amikacin + imipenem
(24)</td><td valign="top" align="center" rowspan="1" colspan="1">24</td><td valign="top" align="center" rowspan="1" colspan="1">0</td><td valign="top" align="center" rowspan="1" colspan="1">Cured</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">2</td><td valign="top" align="center" rowspan="1" colspan="1"><italic>M. abscessus</italic></td><td valign="top" align="center" rowspan="1" colspan="1">Azithromycin + linezolid (6)</td><td valign="top" align="center" rowspan="1" colspan="1">Amikacin + imipenem (6)</td><td valign="top" align="center" rowspan="1" colspan="1">6</td><td valign="top" align="center" rowspan="1" colspan="1">0</td><td valign="top" align="center" rowspan="1" colspan="1">Cured</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">3</td><td valign="top" align="center" rowspan="1" colspan="1"><italic>M. abscessus</italic></td><td valign="top" align="center" rowspan="1" colspan="1">Azithromycin + clofazimine (20)</td><td valign="top" align="center" rowspan="1" colspan="1">Imipenem + amikacin (15)</td><td valign="top" align="center" rowspan="1" colspan="1">20</td><td valign="top" align="center" rowspan="1" colspan="1">0</td><td valign="top" align="center" rowspan="1" colspan="1">Cured</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">4</td><td valign="top" align="center" rowspan="1" colspan="1"><italic>M. abscessus</italic></td><td valign="top" align="center" rowspan="1" colspan="1">Azithromycin + clofazimine (14)</td><td valign="top" align="center" rowspan="1" colspan="1">Cefoxitin + amikacin (8)</td><td valign="top" align="center" rowspan="1" colspan="1">14</td><td valign="top" align="center" rowspan="1" colspan="1">0</td><td valign="top" align="center" rowspan="1" colspan="1">Cured</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">5</td><td valign="top" align="center" rowspan="1" colspan="1"><italic>M. fortuitum</italic></td><td valign="top" align="center" rowspan="1" colspan="1">Moxifloxacin (2)</td><td valign="top" align="center" rowspan="1" colspan="1">Imipenem (2)</td><td valign="top" align="center" rowspan="1" colspan="1">2</td><td valign="top" align="center" rowspan="1" colspan="1">1</td><td valign="top" align="center" rowspan="1" colspan="1">Cured</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">6</td><td valign="top" align="center" rowspan="1" colspan="1"><italic>M. fortuitum</italic></td><td valign="top" align="center" rowspan="1" colspan="1">Doxycycline + ciprofloxacin +
trimethoprim/ sulfamethoxazole (5)</td><td valign="top" align="center" rowspan="1" colspan="1">Amikacin (3)</td><td valign="top" align="center" rowspan="1" colspan="1">5</td><td valign="top" align="center" rowspan="1" colspan="1">3</td><td valign="top" align="center" rowspan="1" colspan="1">Cured</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">7</td><td valign="top" align="center" rowspan="1" colspan="1"><italic>M. massiliense</italic></td><td valign="top" align="center" rowspan="1" colspan="1">Azithromycin, linezolid (4)</td><td valign="top" align="center" rowspan="1" colspan="1">Cefoxitin, tigecycline, linezolid,
amikacin, azithromycin (4)</td><td valign="top" align="center" rowspan="1" colspan="1">4†</td><td valign="top" align="center" rowspan="1" colspan="1">NA</td><td valign="top" align="center" rowspan="1" colspan="1">Treatment failure</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">8</td><td valign="top" align="center" rowspan="1" colspan="1"><italic>M.
intracellulare</italic></td><td valign="top" align="center" rowspan="1" colspan="1">Azithromycin + ethambutol +
rifabutin (14)</td><td valign="top" align="center" rowspan="1" colspan="1">Amikacin (8)</td><td valign="top" align="center" rowspan="1" colspan="1">14</td><td valign="top" align="center" rowspan="1" colspan="1">1</td><td valign="top" align="center" rowspan="1" colspan="1">Cured</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">9</td><td valign="top" align="center" rowspan="1" colspan="1">MAC, speciation unavailable</td><td valign="top" align="center" rowspan="1" colspan="1">Azithromycin + clofazimine +
ethambutol + rifampin (39)</td><td valign="top" align="center" rowspan="1" colspan="1">Amikacin (2)</td><td valign="top" align="center" rowspan="1" colspan="1">39</td><td valign="top" align="center" rowspan="1" colspan="1">11</td><td valign="top" align="center" rowspan="1" colspan="1">Cured</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">10</td><td valign="top" align="center" rowspan="1" colspan="1"><italic>M.
intracellulare</italic></td><td valign="top" align="center" rowspan="1" colspan="1">Azithromycin + rifampin +
clofazimine + ethambutol (27)</td><td valign="top" align="center" rowspan="1" colspan="1">Amikacin (5)</td><td valign="top" align="center" rowspan="1" colspan="1">27</td><td valign="top" align="center" rowspan="1" colspan="1">7</td><td valign="top" align="center" rowspan="1" colspan="1">Cured</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">11</td><td valign="top" align="center" rowspan="1" colspan="1"><italic>M.
intracellulare</italic></td><td valign="top" align="center" rowspan="1" colspan="1">Azithromycin + moxifloxacin +
ethambutol (9)</td><td valign="top" align="center" rowspan="1" colspan="1">None</td><td valign="top" align="center" rowspan="1" colspan="1">9</td><td valign="top" align="center" rowspan="1" colspan="1">5</td><td valign="top" align="center" rowspan="1" colspan="1">Cured</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">12</td><td valign="top" align="center" rowspan="1" colspan="1">MAC, speciation unavailable</td><td valign="top" align="center" rowspan="1" colspan="1">Azithromycin + ethambutol + rifampin
(7)</td><td valign="top" align="center" rowspan="1" colspan="1">None</td><td valign="top" align="center" rowspan="1" colspan="1">7</td><td valign="top" align="center" rowspan="1" colspan="1">3</td><td valign="top" align="center" rowspan="1" colspan="1">Cured</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">13</td><td valign="top" align="center" rowspan="1" colspan="1"><italic>M. gordonae</italic></td><td valign="top" align="center" rowspan="1" colspan="1">Azithromycin + trimethoprim/
sulfamethoxazole + ethambutol (16)</td><td valign="top" align="center" rowspan="1" colspan="1">Amikacin (2)</td><td valign="top" align="center" rowspan="1" colspan="1">16</td><td valign="top" align="center" rowspan="1" colspan="1">2</td><td valign="top" align="center" rowspan="1" colspan="1">Cured</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">14</td><td valign="top" align="center" rowspan="1" colspan="1"><italic>M. marinum</italic></td><td valign="top" align="center" rowspan="1" colspan="1">Azithromycin + ciprofloxacin
(14)</td><td valign="top" align="center" rowspan="1" colspan="1">Imipenem (10)</td><td valign="top" align="center" rowspan="1" colspan="1">14</td><td valign="top" align="center" rowspan="1" colspan="1">10</td><td valign="top" align="center" rowspan="1" colspan="1">Cured</td></tr></tbody></table><table-wrap-foot><p>*All bacteria are <italic>Mycobacterium</italic> spp. MAC,
<italic>Mycobacterium avium</italic> complex.
†Patient elected to discontinue antimicrobial treatment
after experiencing intolerable side effects from multiple medications,
despite ongoing disseminated infection.</p></table-wrap-foot></table-wrap><p>Amikacin-related toxicity occurred in 3 patients. Ototoxicity occurred in 2
patients: case-patient 1 reported hearing loss after 9 months of parenteral
amikacin and within 1 month of implantation of amikacin beads, and case-patient
6 experienced tinnitus after 3 months of parenteral amikacin. Kidney injury
occurred in case-patient 7 after 3 months of parenteral amikacin and 1 month
after implantation of amikacin beads (creatinine level increased from 0.71 to
2.37 mg/dL). Tigecycline was also discontinued in case-patient 7 due to
intractable nausea and vomiting within 2 days of initiation, and cefoxitin was
discontinued due to fever within 3 days of treatment. Clofazimine also caused
intractable nausea and vomiting upon initiation in this patient and was
discontinued after 1 month. Apart from case-patient 1, who experienced permanent
hearing loss, toxicity resolved with discontinuation of medications. Two
patients with <italic>M. avium</italic> complex infection did not receive
amikacin due to history of <italic>C. difficile</italic> infection
(case-patients 10 and 11). </p><p>The median duration of antimicrobial chemotherapy was 14 months (range
2–39 months). Among the 7 patients with rapidly growing NTM, the median
duration was 6 months. The median duration was longer in patients with
slow-growing NTM, at 14 months. Twelve patients received injectable
antimicrobial drugs as part of their treatment regimen, whereas 2 patients had
oral therapy alone. The median duration of therapy with injectable agents was 5
months; rapidly growing strains were treated for a median of 6 months and
slow-growing strains for a median of 5 months. The median duration of
antimicrobial drug therapy after definitive surgery was 2 months. Patients
infected with slow-growing NTM received a more protracted course of
postoperative antimicrobial therapy, with a median duration of 5 months,
compared with <1 month in patients infected with rapidly growing strains.</p></sec><sec><title>Outcomes</title><p>During the follow-up period after surgical intervention (median duration 20
months, range 1–60 months), 13/14 patients did not develop clinical or
microbiological relapse and were cured. One (case-patient 7) had clinical and
microbiological relapse and was deemed to have failed treatment; the first
relapse occurred 2 months after the first surgery to control the infection. The
relapse, a disseminated infection distant from the original surgical site, was a
likely result of the patient receiving multiple immunosuppressive medications to
control systemic lupus erythematosus. She required 12 surgical procedures within
the first year and subsequently required ≈1 procedure/year for control of
chronic disseminated infection over the next 3 years, primarily in the form of
debridement and excision of soft tissue mass. Of note, this patient chose to
forgo antimicrobial therapy after the first 4 months of treatment because of
intolerable side effects from multiple medications. Two instances of
microbiologic relapse were documented for this patient.</p></sec></sec><sec sec-type="discussion"><title>Discussion</title><p>We present a series of cases of NTM musculoskeletal infections requiring surgical
intervention and antimycobacterial chemotherapy that were managed at UCH and NJH
over a 6-year period. NTM musculoskeletal infections have been reported in the
literature sporadically due to their rare occurrence; 2 previous case series
documented 29 cases over 13 years in South Korea (<xref rid="R27" ref-type="bibr"><italic>27</italic></xref>) and 8 cases of PJI by NTM over 4 decades at the
Mayo Clinic in the United States (<xref rid="R26" ref-type="bibr"><italic>26</italic></xref>). In a 6-year period, we have identified 14
case-patients treated at our institutions with unique characteristics, in comparison
to previous studies (<xref rid="R25" ref-type="bibr"><italic>25</italic></xref>–<xref rid="R28" ref-type="bibr"><italic>28</italic></xref>). Specifically, the cases we report indicate the
importance of a low threshold for suspicion and testing for NTM in any patient who
has an unidentified musculoskeletal infection, particularly with evidence of
granuloma formation on pathology. Furthermore, for all of our case-patients, NTM
infections developed at the site of a prior procedure (prosthetic joint or other
intervention), raising the concept of early culture for mycobacteria in conjunction
with or after negative results from conventional bacterial culture.</p><p>One of the most notable findings from the 3 previous case series studying NTM
musculoskeletal infections was that, in all studies, the overwhelming majority of
the patients were immunocompetent (<xref rid="R26" ref-type="bibr"><italic>26</italic></xref>–<xref rid="R28" ref-type="bibr"><italic>28</italic></xref>). In contrast, half the patients in our study
were immunosuppressed as a result of either an underlying medical condition or a
medication used to treat rheumatologic disease. While this may be a manifestation of
the relationship between UCH and NJH, our report highlights the importance of
hypervigilance for possible NTM in immunocompromised patients with musculoskeletal
infections. The most severely immunocompromised patients in our series
(case-patients 1, 7, and 8) had disseminated infection. Immunocompromised patients
with a history of musculoskeletal surgery should receive a mycobacterial workup as a
component of their care.</p><p>Another crucial aspect of our case series is the observation that 10/14 cases
occurred at the site of a previous musculoskeletal surgery and 6 of these cases
involved a joint prosthesis. Moreover, all 14 cases were preceded by an invasive
procedure at the initial site of infection. In all but 3 of our surgery-associated
cases, the onset of symptoms occurred <underline>></underline>3 months after the
preceding surgical procedure, suggesting hematogenous spread, possibly due to
transient mycobacteremia, with seeding of surgically altered tissue as the likely
mechanism of inoculation. This mechanism is particularly likely in case-patients 1,
7, 8, 11, and 12, which comprise 3 cases of disseminated infection in severely
immunocompromised patients and 2 late prosthetic joint infections with more than a
decade between initial prosthetic joint surgery and eventual infection. The previous
report from South Korea noted a minority of periprosthetic infections, but most
cases were related to trauma or iatrogenic injections rather than surgery (<xref rid="R27" ref-type="bibr"><italic>27</italic></xref>). </p><p>The report from the Mayo Clinic focused on PJIs but noted only 8 cases over 4 decades
(<xref rid="R26" ref-type="bibr"><italic>26</italic></xref>). A recent series of
6 cases of chronic trauma– or intervention-related joint infection not
responding to empiric therapy reported no cases of periprosthetic NTM infection
(<xref rid="R29" ref-type="bibr"><italic>29</italic></xref>). Our relatively
rapid accumulation of surgery-related cases over a 6-year period is due to the
relationship between UHC and NJH and NJH’s high volume of NTM cases; we
cannot generalize this trend to the general US population, given the unique referral
characteristics of our patient population. It is possible that improvements in
detection and identification of NTM infections may contribute to this increased case
volume, as has been suggested to explain the increasing incidence and prevalence of
pulmonary NTM (<xref rid="R30" ref-type="bibr"><italic>30</italic></xref>).
Regardless, infections in our study were more likely to occur at the site of a
previous orthopedic surgery and in <underline>></underline>4 cases led to severe
complications requiring partial or full amputation, with 1 patient requiring
hemipelvectomy. Three of these patients were infected with <italic>M.
abscessus</italic> and 1 with <italic>M. fortuitum</italic>. <italic>M.
abscessus</italic> is highly drug resistant and therefore responds poorly to
antimicrobial therapy. It is difficult to ascertain if these amputations could have
been avoided with earlier diagnosis and aggressive surgical therapy. In several
cases, patients with long delays in diagnosis ultimately required amputation; almost
one third of patients in our series required amputation.</p><p>Given the importance in identifying NTM musculoskeletal infections in the
immunocompromised or those with prior surgery, it is unfortunate that our data did
not identify more substantial diagnostic criteria based upon inflammatory markers.
Whereas the ESR in our patients was usually elevated, the C-reactive protein and
leukocyte counts were typically normal. The patient who failed treatment had one of
the highest ESRs in our patient group, nearly double the median value of 38 at
intake, perhaps because of her chronic autoimmune condition.</p><p>All patients had positive mycobacterial cultures at time of initial diagnosis.
Thirteen of 14 patients were receiving mycobacterial therapy at the time of surgery
at our institution and only half of them were persistently positive for
mycobacterial growth despite ongoing symptoms and intraoperative observation of
sinus tract formation and suppuration. We are familiar with this phenomenon, and
therefore do not require a positive culture to define failure of therapy. If a
patient has ongoing signs of infection while receiving effective antimicrobial drugs
(based on drug sensitivity testing), then they need more aggressive resection of
infected tissue. The 3 patients with PJI and rapidly growing NTM infection all
required prolonged courses of IV and oral antimicrobial therapy. One of the 3
patients with <italic>M. avium</italic> complex–related PJI also required 2
months of concomitant IV amikacin. All patients with PJIs required explantation of
the infected hardware followed by antimicrobial spacer placement for
<underline>></underline>3 months in addition to ongoing postoperative oral or
intravenous antimicrobial therapy to achieve a successful outcome. In
<underline>></underline>5 cases, microbiologic diagnosis of mycobacterial
infection was only confirmed during the initial surgical intervention, and in each
of these cases, prior or subsequent surgeries were required for ultimate control of
infection. Ultimately, the fact that 10/14 cases required multiple surgeries for
control of infection with long intervals from onset of symptoms and initial seeking
of care to identification of the infectious agent and finally definitive surgical
treatment underscores the need for early identification and aggressive treatment of
NTM infection.</p></sec><sec sec-type="supplementary-material"><title></title><supplementary-material content-type="local-data" id="SD1"><caption><title>Appendix</title><p>Additional information about nontuberculous mycobacterial musculoskeletal
infections, Colorado, USA. </p></caption><media mimetype="application" mime-subtype="excel" xlink:href="18-1041-Techapp-s1.xlsx" xlink:type="simple" id="d35e1370" position="anchor"></media></supplementary-material></sec></body><back><fn-group><fn fn-type="citation"><p><italic>Suggested citation for this article</italic>: Goldstein N, St. Clair JB,
Kasperbauer SH, Daley CL, Lindeque B. Nontuberculous mycobacterial
musculoskeletal infection cases from a tertiary referral center, Colorado, USA.
Emerg Infect Dis. 2019 Jun [<italic>date cited</italic>]. <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3201/eid2506.181041">https://doi.org/10.3201/eid2506.181041</ext-link></p></fn><fn id="FN1"><label>1</label><p>These first authors contributed equally to this article.</p></fn></fn-group><bio id="d35e1388"><p>Dr. Goldstein is a graduate of the University of Colorado School of Medicine, Aurora,
CO. He will begin his residency in psychiatry at the University of North Carolina in
July 2019. </p></bio><ref-list><title>References</title><ref id="R1"><label>1. </label><mixed-citation publication-type="journal"><string-name><surname>Prevots</surname><given-names>DR</given-names></string-name>,
<string-name><surname>Shaw</surname><given-names>PA</given-names></string-name>,
<string-name><surname>Strickland</surname><given-names>D</given-names></string-name>,
<string-name><surname>Jackson</surname><given-names>LA</given-names></string-name>,
<string-name><surname>Raebel</surname><given-names>MA</given-names></string-name>,
<string-name><surname>Blosky</surname><given-names>MA</given-names></string-name>, <etal>et al.</etal><article-title>Nontuberculous mycobacterial lung disease prevalence at four
integrated health care delivery systems.</article-title><source>Am J Respir Crit Care Med</source>.
<year>2010</year>;<volume>182</volume>:<fpage>970</fpage>–<lpage>6</lpage>.
<pub-id pub-id-type="doi">10.1164/rccm.201002-0310OC</pub-id><pub-id pub-id-type="pmid">20538958</pub-id></mixed-citation></ref><ref id="R2"><label>2. </label><mixed-citation publication-type="journal"><string-name><surname>Adjemian</surname><given-names>J</given-names></string-name>,
<string-name><surname>Olivier</surname><given-names>KN</given-names></string-name>,
<string-name><surname>Seitz</surname><given-names>AE</given-names></string-name>,
<string-name><surname>Holland</surname><given-names>SM</given-names></string-name>,
<string-name><surname>Prevots</surname><given-names>DR</given-names></string-name>. <article-title>Prevalence of
nontuberculous mycobacterial lung disease in U.S. Medicare
beneficiaries.</article-title><source>Am J Respir Crit Care Med</source>.
<year>2012</year>;<volume>185</volume>:<fpage>881</fpage>–<lpage>6</lpage>.
<pub-id pub-id-type="doi">10.1164/rccm.201111-2016OC</pub-id><pub-id pub-id-type="pmid">22312016</pub-id></mixed-citation></ref><ref id="R3"><label>3. </label><mixed-citation publication-type="journal"><string-name><surname>Al-Houqani</surname><given-names>M</given-names></string-name>,
<string-name><surname>Jamieson</surname><given-names>F</given-names></string-name>,
<string-name><surname>Mehta</surname><given-names>M</given-names></string-name>,
<string-name><surname>Chedore</surname><given-names>P</given-names></string-name>,
<string-name><surname>May</surname><given-names>K</given-names></string-name>,
<string-name><surname>Marras</surname><given-names>TK</given-names></string-name>. <article-title>Aging, COPD, and
other risk factors do not explain the increased prevalence of pulmonary
<italic>Mycobacterium avium</italic> complex in Ontario.</article-title><source>Chest</source>.
<year>2012</year>;<volume>141</volume>:<fpage>190</fpage>–<lpage>7</lpage>.
<pub-id pub-id-type="doi">10.1378/chest.11-0089</pub-id><pub-id pub-id-type="pmid">21724552</pub-id></mixed-citation></ref><ref id="R4"><label>4. </label><mixed-citation publication-type="journal"><string-name><surname>Spaulding</surname><given-names>AB</given-names></string-name>,
<string-name><surname>Lai</surname><given-names>YL</given-names></string-name>,
<string-name><surname>Zelazny</surname><given-names>AM</given-names></string-name>,
<string-name><surname>Olivier</surname><given-names>KN</given-names></string-name>,
<string-name><surname>Kadri</surname><given-names>SS</given-names></string-name>,
<string-name><surname>Prevots</surname><given-names>DR</given-names></string-name>, <etal>et al.</etal><article-title>Geographic distribution of nontuberculous mycobacterial species
identified among clinical isolates in the United States,
2009–2013.</article-title><source>Ann Am Thorac Soc</source>.
<year>2017</year>;<volume>14</volume>:<fpage>1655</fpage>–<lpage>61</lpage>.
<pub-id pub-id-type="doi">10.1513/AnnalsATS.201611-860OC</pub-id><pub-id pub-id-type="pmid">28817307</pub-id></mixed-citation></ref><ref id="R5"><label>5. </label><mixed-citation publication-type="journal"><string-name><surname>Griffith</surname><given-names>DE</given-names></string-name>,
<string-name><surname>Aksamit</surname><given-names>T</given-names></string-name>,
<string-name><surname>Brown-Elliott</surname><given-names>BA</given-names></string-name>,
<string-name><surname>Catanzaro</surname><given-names>A</given-names></string-name>,
<string-name><surname>Daley</surname><given-names>C</given-names></string-name>,
<string-name><surname>Gordin</surname><given-names>F</given-names></string-name>, <etal>et al.</etal>; <collab>ATS
Mycobacterial Diseases Subcommittee</collab>; <collab>American Thoracic
Society</collab>; <collab>Infectious Disease Society of America</collab>.
<article-title>An official ATS/IDSA statement: diagnosis, treatment, and
prevention of nontuberculous mycobacterial diseases.</article-title><source>Am J Respir Crit Care Med</source>.
<year>2007</year>;<volume>175</volume>:<fpage>367</fpage>–<lpage>416</lpage>.
<pub-id pub-id-type="doi">10.1164/rccm.200604-571ST</pub-id><pub-id pub-id-type="pmid">17277290</pub-id></mixed-citation></ref><ref id="R6"><label>6. </label><mixed-citation publication-type="journal"><string-name><surname>Smith</surname><given-names>GS</given-names></string-name>,
<string-name><surname>Ghio</surname><given-names>AJ</given-names></string-name>,
<string-name><surname>Stout</surname><given-names>JE</given-names></string-name>,
<string-name><surname>Messier</surname><given-names>KP</given-names></string-name>,
<string-name><surname>Hudgens</surname><given-names>EE</given-names></string-name>,
<string-name><surname>Murphy</surname><given-names>MS</given-names></string-name>, <etal>et al.</etal><article-title>Epidemiology of nontuberculous mycobacteria isolations among
central North Carolina residents, 2006-2010.</article-title><source>J Infect</source>.
<year>2016</year>;<volume>72</volume>:<fpage>678</fpage>–<lpage>86</lpage>.
<pub-id pub-id-type="doi">10.1016/j.jinf.2016.03.008</pub-id><pub-id pub-id-type="pmid">26997636</pub-id></mixed-citation></ref><ref id="R7"><label>7. </label><mixed-citation publication-type="journal"><string-name><surname>Cassidy</surname><given-names>PM</given-names></string-name>,
<string-name><surname>Hedberg</surname><given-names>K</given-names></string-name>,
<string-name><surname>Saulson</surname><given-names>A</given-names></string-name>,
<string-name><surname>McNelly</surname><given-names>E</given-names></string-name>,
<string-name><surname>Winthrop</surname><given-names>KL</given-names></string-name>. <article-title>Nontuberculous
mycobacterial disease prevalence and risk factors: a changing
epidemiology.</article-title><source>Clin Infect Dis</source>.
<year>2009</year>;<volume>49</volume>:<fpage>e124</fpage>–<lpage>9</lpage>.
<pub-id pub-id-type="doi">10.1086/648443</pub-id><pub-id pub-id-type="pmid">19911942</pub-id></mixed-citation></ref><ref id="R8"><label>8. </label><mixed-citation publication-type="journal"><string-name><surname>Booth</surname><given-names>JE</given-names></string-name>,
<string-name><surname>Jacobson</surname><given-names>JA</given-names></string-name>,
<string-name><surname>Kurrus</surname><given-names>TA</given-names></string-name>,
<string-name><surname>Edwards</surname><given-names>TW</given-names></string-name>. <article-title>Infection of
prosthetic arthroplasty by <italic>Mycobacterium fortuitum.</italic> Two
case reports.</article-title><source>J Bone Joint Surg Am</source>.
<year>1979</year>;<volume>61</volume>:<fpage>300</fpage>–<lpage>2</lpage>.
<pub-id pub-id-type="doi">10.2106/00004623-197961020-00029</pub-id><pub-id pub-id-type="pmid">422622</pub-id></mixed-citation></ref><ref id="R9"><label>9. </label><mixed-citation publication-type="journal"><string-name><surname>Horadam</surname><given-names>VW</given-names></string-name>,
<string-name><surname>Smilack</surname><given-names>JD</given-names></string-name>,
<string-name><surname>Smith</surname><given-names>EC</given-names></string-name>.
<article-title><italic>Mycobacterium fortuitum</italic> infection after
total hip replacement.</article-title><source>South Med J</source>.
<year>1982</year>;<volume>75</volume>:<fpage>244</fpage>–<lpage>6</lpage>.
<pub-id pub-id-type="doi">10.1097/00007611-198202000-00036</pub-id><pub-id pub-id-type="pmid">7058374</pub-id></mixed-citation></ref><ref id="R10"><label>10. </label><mixed-citation publication-type="journal"><string-name><surname>Heathcock</surname><given-names>R</given-names></string-name>,
<string-name><surname>Dave</surname><given-names>J</given-names></string-name>,
<string-name><surname>Yates</surname><given-names>MD</given-names></string-name>.
<article-title><italic>Mycobacterium chelonae</italic> hip
infection.</article-title><source>J Infect</source>.
<year>1994</year>;<volume>28</volume>:<fpage>104</fpage>–<lpage>5</lpage>.
<pub-id pub-id-type="doi">10.1016/S0163-4453(94)94533-0</pub-id><pub-id pub-id-type="pmid">8163823</pub-id></mixed-citation></ref><ref id="R11"><label>11. </label><mixed-citation publication-type="journal"><string-name><surname>Pring</surname><given-names>M</given-names></string-name>,
<string-name><surname>Eckhoff</surname><given-names>DG</given-names></string-name>.
<article-title><italic>Mycobacterium chelonae</italic> infection
following a total knee arthroplasty.</article-title><source>J Arthroplasty</source>.
<year>1996</year>;<volume>11</volume>:<fpage>115</fpage>–<lpage>6</lpage>.
<pub-id pub-id-type="doi">10.1016/S0883-5403(96)80170-7</pub-id><pub-id pub-id-type="pmid">8676110</pub-id></mixed-citation></ref><ref id="R12"><label>12. </label><mixed-citation publication-type="journal"><string-name><surname>Luque</surname><given-names>AE</given-names></string-name>,
<string-name><surname>Kaminski</surname><given-names>D</given-names></string-name>,
<string-name><surname>Reichman</surname><given-names>R</given-names></string-name>,
<string-name><surname>Hardy</surname><given-names>D</given-names></string-name>; <collab>Amneris E. Luque,
Dorothy Kaminski</collab>. <article-title><italic>Mycobacterium
szulgai</italic> osteomyelitis in an AIDS patient.</article-title><source>Scand J Infect Dis</source>.
<year>1998</year>;<volume>30</volume>:<fpage>88</fpage>–<lpage>91</lpage>.
<pub-id pub-id-type="doi">10.1080/003655498750002376</pub-id><pub-id pub-id-type="pmid">9670366</pub-id></mixed-citation></ref><ref id="R13"><label>13. </label><mixed-citation publication-type="journal"><string-name><surname>Breda</surname><given-names>L</given-names></string-name>, <string-name><surname>de
Michele</surname><given-names>G</given-names></string-name>,
<string-name><surname>Nozzi</surname><given-names>M</given-names></string-name>, <string-name><surname>De
Sanctis</surname><given-names>S</given-names></string-name>, <string-name><surname>Di
Marzio</surname><given-names>D</given-names></string-name>,
<string-name><surname>Chiarelli</surname><given-names>F</given-names></string-name>. <article-title>Non-tuberculous
mycobacterial osteomyelitis: an unusual cause of hip pain in immunocompetent
children.</article-title><source>Rheumatol Int</source>.
<year>2009</year>;<volume>29</volume>:<fpage>1487</fpage>–<lpage>9</lpage>.
<pub-id pub-id-type="doi">10.1007/s00296-009-0844-4</pub-id><pub-id pub-id-type="pmid">19156420</pub-id></mixed-citation></ref><ref id="R14"><label>14. </label><mixed-citation publication-type="journal"><string-name><surname>Wang</surname><given-names>S-X</given-names></string-name>,
<string-name><surname>Yang</surname><given-names>C-J</given-names></string-name>,
<string-name><surname>Chen</surname><given-names>Y-C</given-names></string-name>,
<string-name><surname>Lay</surname><given-names>C-J</given-names></string-name>,
<string-name><surname>Tsai</surname><given-names>C-C</given-names></string-name>. <article-title>Septic
arthritis caused by <italic>Mycobacterium fortuitum</italic> and
<italic>Mycobacterium abscessus</italic> in a prosthetic knee joint:
case report and review of literature.</article-title><source>Intern Med</source>.
<year>2011</year>;<volume>50</volume>:<fpage>2227</fpage>–<lpage>32</lpage>.
<pub-id pub-id-type="doi">10.2169/internalmedicine.50.5610</pub-id><pub-id pub-id-type="pmid">21963746</pub-id></mixed-citation></ref><ref id="R15"><label>15. </label><mixed-citation publication-type="journal"><string-name><surname>Garcia</surname><given-names>DC</given-names></string-name>,
<string-name><surname>Sandoval-Sus</surname><given-names>J</given-names></string-name>,
<string-name><surname>Razzaq</surname><given-names>K</given-names></string-name>,
<string-name><surname>Young</surname><given-names>L</given-names></string-name>. <article-title>Vertebral
osteomyelitis caused by <italic>Mycobacterium
abscessus.</italic></article-title><source>BMJ Case Rep</source>.
<year>2013</year>;<volume>2013</volume>(<issue>aug07
1</issue>):<elocation-id>cr2013009597</elocation-id>. <pub-id pub-id-type="doi">10.1136/bcr-2013-009597</pub-id><pub-id pub-id-type="pmid">23925676</pub-id></mixed-citation></ref><ref id="R16"><label>16. </label><mixed-citation publication-type="journal"><string-name><surname>Suy</surname><given-names>F</given-names></string-name>,
<string-name><surname>Carricajo</surname><given-names>A</given-names></string-name>,
<string-name><surname>Grattard</surname><given-names>F</given-names></string-name>,
<string-name><surname>Cazorla</surname><given-names>C</given-names></string-name>,
<string-name><surname>Denis</surname><given-names>C</given-names></string-name>,
<string-name><surname>Girardin</surname><given-names>P</given-names></string-name>, <etal>et al.</etal><article-title>Infection due to <italic>Mycobacterium
thermoresistibile</italic>: a case associated with an orthopedic
device.</article-title><source>J Clin Microbiol</source>.
<year>2013</year>;<volume>51</volume>:<fpage>3154</fpage>–<lpage>6</lpage>.
<pub-id pub-id-type="doi">10.1128/JCM.00925-13</pub-id><pub-id pub-id-type="pmid">23843483</pub-id></mixed-citation></ref><ref id="R17"><label>17. </label><mixed-citation publication-type="journal"><string-name><surname>Bakhsh</surname><given-names>WR</given-names></string-name>,
<string-name><surname>Mesfin</surname><given-names>A</given-names></string-name>.
<article-title><italic>Mycobacterium kansasii</italic> infection of the
spine in a patient with sarcoidosis: a case report and literature
review.</article-title><source>J Surg Orthop Adv</source>.
<year>2014</year>;<volume>23</volume>:<fpage>162</fpage>–<lpage>5</lpage>.
<pub-id pub-id-type="doi">10.3113/JSOA.2014.0162</pub-id><pub-id pub-id-type="pmid">25153815</pub-id></mixed-citation></ref><ref id="R18"><label>18. </label><mixed-citation publication-type="journal"><string-name><surname>Hazara</surname><given-names>AM</given-names></string-name>,
<string-name><surname>Edey</surname><given-names>M</given-names></string-name>,
<string-name><surname>Roy</surname><given-names>A</given-names></string-name>,
<string-name><surname>Bhandari</surname><given-names>S</given-names></string-name>. <article-title>Rapidly growing
non-tuberculous mycobacterial infection in a renal transplant patient after
alemtuzumab induction.</article-title><source>Transpl Infect Dis</source>.
<year>2014</year>;<volume>16</volume>:<fpage>847</fpage>–<lpage>52</lpage>.
<pub-id pub-id-type="doi">10.1111/tid.12269</pub-id><pub-id pub-id-type="pmid">25040696</pub-id></mixed-citation></ref><ref id="R19"><label>19. </label><mixed-citation publication-type="journal"><string-name><surname>Kato</surname><given-names>S</given-names></string-name>,
<string-name><surname>Murakami</surname><given-names>H</given-names></string-name>,
<string-name><surname>Demura</surname><given-names>S</given-names></string-name>,
<string-name><surname>Yoshioka</surname><given-names>K</given-names></string-name>,
<string-name><surname>Hayashi</surname><given-names>H</given-names></string-name>,
<string-name><surname>Yokogawa</surname><given-names>N</given-names></string-name>, <etal>et al.</etal><article-title>Vertebral osteomyelitis caused by <italic>Mycobacterium
abscessus</italic> surgically treated using antibacterial
iodine-supported instrumentation.</article-title><source>Case Rep Orthop</source>.
<year>2014</year>;<volume>2014</volume>:<elocation-id>197061</elocation-id>.
<pub-id pub-id-type="doi">10.1155/2014/197061</pub-id><pub-id pub-id-type="pmid">25544922</pub-id></mixed-citation></ref><ref id="R20"><label>20. </label><mixed-citation publication-type="journal"><string-name><surname>Nguyen</surname><given-names>HH</given-names></string-name>,
<string-name><surname>Fadul</surname><given-names>N</given-names></string-name>,
<string-name><surname>Ashraf</surname><given-names>MS</given-names></string-name>,
<string-name><surname>Siraj</surname><given-names>DS</given-names></string-name>. <article-title>Osteomyelitis
infection of <italic>Mycobacterium marinum:</italic> a case report and
literature review.</article-title><source>Case Rep Infect Dis</source>.
<year>2015</year>;<volume>2015</volume>:<elocation-id>905920</elocation-id>.
<pub-id pub-id-type="doi">10.1155/2015/905920</pub-id><pub-id pub-id-type="pmid">25664190</pub-id></mixed-citation></ref><ref id="R21"><label>21. </label><mixed-citation publication-type="journal"><string-name><surname>Sharma</surname><given-names>VK</given-names></string-name>,
<string-name><surname>Pai</surname><given-names>G</given-names></string-name>,
<string-name><surname>Deswarte</surname><given-names>C</given-names></string-name>,
<string-name><surname>Lodha</surname><given-names>R</given-names></string-name>,
<string-name><surname>Singh</surname><given-names>S</given-names></string-name>,
<string-name><surname>Kang</surname><given-names>LW</given-names></string-name>, <etal>et al.</etal><article-title>Disseminated <italic>Mycobacterium avium</italic> complex
infection in a child with partial dominant interferon gamma receptor 1
deficiency in India.</article-title><source>J Clin Immunol</source>.
<year>2015</year>;<volume>35</volume>:<fpage>459</fpage>–<lpage>62</lpage>.
<pub-id pub-id-type="doi">10.1007/s10875-015-0173-1</pub-id><pub-id pub-id-type="pmid">26054576</pub-id></mixed-citation></ref><ref id="R22"><label>22. </label><mixed-citation publication-type="journal"><string-name><surname>Silva</surname><given-names>JT</given-names></string-name>,
<string-name><surname>López-Medrano</surname><given-names>F</given-names></string-name>,
<string-name><surname>Fernández-Ruiz</surname><given-names>M</given-names></string-name>,
<string-name><surname>San-Juan</surname><given-names>R</given-names></string-name>,
<string-name><surname>Ruiz-Cano</surname><given-names>MJ</given-names></string-name>,
<string-name><surname>Delgado</surname><given-names>JF</given-names></string-name>, <etal>et al.</etal><article-title><italic>Mycobacterium abscessus</italic> pulmonary infection
complicated with vertebral osteomyelitis in a heart transplant recipient:
case report and literature review.</article-title><source>Transpl Infect Dis</source>.
<year>2015</year>;<volume>17</volume>:<fpage>418</fpage>–<lpage>23</lpage>.
<pub-id pub-id-type="doi">10.1111/tid.12381</pub-id><pub-id pub-id-type="pmid">25816889</pub-id></mixed-citation></ref><ref id="R23"><label>23. </label><mixed-citation publication-type="journal"><string-name><surname>Wood</surname><given-names>BR</given-names></string-name>,
<string-name><surname>Buitrago</surname><given-names>MO</given-names></string-name>,
<string-name><surname>Patel</surname><given-names>S</given-names></string-name>,
<string-name><surname>Hachey</surname><given-names>DH</given-names></string-name>,
<string-name><surname>Haneuse</surname><given-names>S</given-names></string-name>,
<string-name><surname>Harrington</surname><given-names>RD</given-names></string-name>.
<article-title><italic>Mycobacterium avium</italic> complex
osteomyelitis in persons with human immunodeficiency virus: case series and
literature review.</article-title><source>Open Forum Infect Dis</source>.
<year>2015</year>;<volume>2</volume>:<elocation-id>ofv090</elocation-id>.
<pub-id pub-id-type="doi">10.1093/ofid/ofv090</pub-id><pub-id pub-id-type="pmid">26180837</pub-id></mixed-citation></ref><ref id="R24"><label>24. </label><mixed-citation publication-type="journal"><string-name><surname>Kuntz</surname><given-names>M</given-names></string-name>,
<string-name><surname>Seidl</surname><given-names>M</given-names></string-name>,
<string-name><surname>Henneke</surname><given-names>P</given-names></string-name>. <article-title>Osteomyelitis
because of <italic>Mycobacterium xenopi</italic> in an immunocompetent
child.</article-title><source>Pediatr Infect Dis J</source>.
<year>2016</year>;<volume>35</volume>:<fpage>110</fpage>–<lpage>3</lpage>.<pub-id pub-id-type="pmid">26418244</pub-id></mixed-citation></ref><ref id="R25"><label>25. </label><mixed-citation publication-type="journal"><string-name><surname>Marchevsky</surname><given-names>AM</given-names></string-name>,
<string-name><surname>Damsker</surname><given-names>B</given-names></string-name>,
<string-name><surname>Green</surname><given-names>S</given-names></string-name>,
<string-name><surname>Tepper</surname><given-names>S</given-names></string-name>. <article-title>The
clinicopathological spectrum of non-tuberculous mycobacterial osteoarticular
infections.</article-title><source>J Bone Joint Surg Am</source>.
<year>1985</year>;<volume>67</volume>:<fpage>925</fpage>–<lpage>9</lpage>.
<pub-id pub-id-type="doi">10.2106/00004623-198567060-00015</pub-id><pub-id pub-id-type="pmid">4019542</pub-id></mixed-citation></ref><ref id="R26"><label>26. </label><mixed-citation publication-type="journal"><string-name><surname>Eid</surname><given-names>AJ</given-names></string-name>,
<string-name><surname>Berbari</surname><given-names>EF</given-names></string-name>,
<string-name><surname>Sia</surname><given-names>IG</given-names></string-name>,
<string-name><surname>Wengenack</surname><given-names>NL</given-names></string-name>,
<string-name><surname>Osmon</surname><given-names>DR</given-names></string-name>,
<string-name><surname>Razonable</surname><given-names>RR</given-names></string-name>. <article-title>Prosthetic joint
infection due to rapidly growing mycobacteria: report of 8 cases and review
of the literature.</article-title><source>Clin Infect Dis</source>.
<year>2007</year>;<volume>45</volume>:<fpage>687</fpage>–<lpage>94</lpage>.
<pub-id pub-id-type="doi">10.1086/520982</pub-id><pub-id pub-id-type="pmid">17712751</pub-id></mixed-citation></ref><ref id="R27"><label>27. </label><mixed-citation publication-type="journal"><string-name><surname>Park</surname><given-names>JW</given-names></string-name>,
<string-name><surname>Kim</surname><given-names>YS</given-names></string-name>,
<string-name><surname>Yoon</surname><given-names>JO</given-names></string-name>,
<string-name><surname>Kim</surname><given-names>JS</given-names></string-name>,
<string-name><surname>Chang</surname><given-names>JS</given-names></string-name>,
<string-name><surname>Kim</surname><given-names>JM</given-names></string-name>, <etal>et al.</etal><article-title>Non-tuberculous mycobacterial infection of the musculoskeletal
system: pattern of infection and efficacy of combined surgical/antimicrobial
treatment.</article-title><source>Bone Joint J</source>.
<year>2014</year>;<volume>96-B</volume>:<fpage>1561</fpage>–<lpage>5</lpage>.
<pub-id pub-id-type="doi">10.1302/0301-620X.96B11.33427</pub-id><pub-id pub-id-type="pmid">25371475</pub-id></mixed-citation></ref><ref id="R28"><label>28. </label><mixed-citation publication-type="journal"><string-name><surname>Johnson</surname><given-names>MG</given-names></string-name>,
<string-name><surname>Stout</surname><given-names>JE</given-names></string-name>. <article-title>Twenty-eight
cases of <italic>Mycobacterium marinum</italic> infection: retrospective
case series and literature review.</article-title><source>Infection</source>.
<year>2015</year>;<volume>43</volume>:<fpage>655</fpage>–<lpage>62</lpage>.
<pub-id pub-id-type="doi">10.1007/s15010-015-0776-8</pub-id><pub-id pub-id-type="pmid">25869820</pub-id></mixed-citation></ref><ref id="R29"><label>29. </label><mixed-citation publication-type="journal"><string-name><surname>Gundavda</surname><given-names>MK</given-names></string-name>,
<string-name><surname>Patil</surname><given-names>HG</given-names></string-name>,
<string-name><surname>Agashe</surname><given-names>VM</given-names></string-name>,
<string-name><surname>Soman</surname><given-names>R</given-names></string-name>,
<string-name><surname>Rodriques</surname><given-names>C</given-names></string-name>,
<string-name><surname>Deshpande</surname><given-names>RB</given-names></string-name>. <article-title>Nontuberculous
mycobacterial infection of the musculoskeletal system in immunocompetent
hosts.</article-title><source>Indian J Orthop</source>.
<year>2017</year>;<volume>51</volume>:<fpage>205</fpage>–<lpage>12</lpage>.
<pub-id pub-id-type="doi">10.4103/0019-5413.201718</pub-id><pub-id pub-id-type="pmid">28400668</pub-id></mixed-citation></ref><ref id="R30"><label>30. </label><mixed-citation publication-type="journal"><string-name><surname>Johnson</surname><given-names>MM</given-names></string-name>,
<string-name><surname>Odell</surname><given-names>JA</given-names></string-name>. <article-title>Nontuberculous
mycobacterial pulmonary infections.</article-title><source>J Thorac Dis</source>.
<year>2014</year>;<volume>6</volume>:<fpage>210</fpage>–<lpage>20</lpage>.<pub-id pub-id-type="pmid">24624285</pub-id></mixed-citation></ref></ref-list></back></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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