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Resistance to fluoroquinolones and second-line injectable drugs: impact on multidrug-resistant TB outcomes

Dennis Falzon, Neel Gandhi, Giovanni B. Migliori, Giovanni Sotgiu, Helen S. Cox, Timothy H. Holtz, Maria-Graciela Hollm-Delgado, Salmaan Keshavjee, Kathryn DeRiemer, Rosella Centis, Lia D'Ambrosio, Christoph G. Lange, Melissa Bauer, Dick Menzies on behalf of the Collaborative Group for Meta-Analysis of Individual Patient Data in MDR-TB
European Respiratory Journal 2013 42: 156-168; DOI: 10.1183/09031936.00134712
Dennis Falzon
1Stop TB Dept, World Health Organization, Geneva, Switzerland
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Neel Gandhi
2Divisions of General Internal Medicine, Infectious Diseases and Epidemiology, Albert Einstein College of Medicine, New York, NY
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Giovanni B. Migliori
3World Health Organization Collaborating Centre for Tuberculosis and Lung Diseases, Fondazione S. Maugeri, Care and Research Institute, Tradate
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Giovanni Sotgiu
4Dept of Biomedical Sciences, University of Sassari, Sassari, Italy
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Helen S. Cox
5Médecins Sans Frontières, Cape Town, South Africa
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Timothy H. Holtz
6US Centers for Disease Control and Prevention, HIV/STD Research Program, Bangkok, Thailand
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Maria-Graciela Hollm-Delgado
7Montreal Chest Institute, McGill University, Montreal, QC, Canada
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Salmaan Keshavjee
8Dept of Global Health and Social Medicine, Harvard Medical School, Boston, MA
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Kathryn DeRiemer
9School of Medicine, University of California Davis, Davis, CA, USA
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Rosella Centis
3World Health Organization Collaborating Centre for Tuberculosis and Lung Diseases, Fondazione S. Maugeri, Care and Research Institute, Tradate
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Lia D'Ambrosio
3World Health Organization Collaborating Centre for Tuberculosis and Lung Diseases, Fondazione S. Maugeri, Care and Research Institute, Tradate
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Christoph G. Lange
10Clinical Infectious Diseases, Tuberculosis Center Borstel, Borstel, Germany
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Melissa Bauer
7Montreal Chest Institute, McGill University, Montreal, QC, Canada
11Dept of Epidemiology, Biostatistics, and Occupational Health, McGill University, Montreal, QC
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Dick Menzies
7Montreal Chest Institute, McGill University, Montreal, QC, Canada
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  • For correspondence: Dick.Menzies@McGill.ca
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    Figure 1–

    Treatment success among different multidrug-resistant tuberculosis (MDR-TB) patient groups. Data are presented as point estimates and 95% CI. MDR−TB+INJr: MDRTB plus resistance to amikacin/kanamycin and/or capreomycin, but susceptible to fluoroquinolones; MDR-TB+FQr: MDR-TB plus resistance to any fluoroquinolone, but susceptible to amikacin/kanamycin and/or capreomycin (at least one second-line injectable drug tested); XDR-TB: extensively drug-resistant tuberculosis (MDR-TB plus resistance to any fluoroquinolone and any second-line injectable drug (amikacin/kanamycin and/or capreomycin)).

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  • Table 1– Characteristics of multidrug-resistant tuberculosis (MDR-TB) patients with different resistance patterns of Mycobacterium tuberculosis
    MDR-TB onlyMDR-TB+INJrMDR-TB+FQrXDR-TBTotal MDR-TB cases
    Studies n2622181726
    Cases n476311304264056724
    Demographic characteristics
     Age years39.2±13.539.9±13.341.6±14.340.6±13.839.5±13.5
      Male6874686769
     HIV-infected145.11.73.711
    Clinical characteristics
     Pulmonary TB only9797969797
     Sputum-smear positive7373797974
     Cavities on chest radiography6566607766
     Extensive disease#7271787873
     Previous TB treatment¶
      None2024191630
      First-line drugs only7360645760
      Second-line drugs for MDR-TB716172710
     Had a serious adverse event during therapy2947334332
    • Data are presented as mean±sd or %, unless otherwise stated. Values shown were computed using simple pooling across all studies. Percentages were calculated on the number of patients in each group with information available. MDR-TB: multidrug-resistant TB (resistance to at least isoniazid and rifampicin); MDR-TB only: MDR-TB, but susceptible to fluoroquinolones, amikacin/kanamycin and capreomycin (at least one second-line injectable drug tested); MDR-TB+INJr: MDR-TB plus resistance to amikacin/kanamycin and/or capreomycin, but susceptible to fluoroquinolones; MDR-TB+FQr: MDR-TB plus resistance to any fluoroquinolone, but susceptible to amikacin/kanamycin and/or capreomycin (at least one second-line injectable drug tested); XDR-TB: extensively drug-resistant tuberculosis (MDR-TB plus resistance to any fluoroquinolone and any second-line injectable drug (amikacin/kanamycin and/or capreomycin)). #: Extensive disease was defined as sputum-smear positive, or cavities on chest radiography if information about sputum-smear was missing. ¶: Previous tuberculosis (TB) treatment was defined as treatment with any TB drug for ≥=1 month. Previous treatment could be with first-line drugs or with ≥2 second-line drugs for MDR. In some patients, information was only available that they had been treated previously for TB, but not whether this was with first- or second-line drugs.

  • Table 2– Resistance to anti-tuberculosis drugs by multidrug-resistant tuberculosis (MDR-TB) patient group
    MDR-TB onlyMDR-TB +INJrMDR-TB +FQrXDR-TBTotal MDR-TB cases
    Cases n476311304264056724
    Resistance
     First-line drugs
      Pyrazinamide1052 (41)556 (70)234 (58)211 (69)2053 (50)
      Ethambutol1524 (51)845 (76)296 (74)295 (81)2960 (61)
     Fluoroquinolones#00426 (100)405 (100)831 (12)
     Injectable drugs
      Streptomycin1534 (51)960 (86)226 (53)291 (78)3011 (61)
      Amikacin/kanamycin¶01042 (92)0383 (95)1425 (21)
      Capreomycin0399 (42)0104 (38)503 (16)
     Amikacin/kanamycin and capreomycin0311 (33)082 (30)393 (13)
     Amikacin/kanamycin and capreomycin and streptomycin0295 (31)068 (25)363 (12)
     Group 4 drugs
      Ethionamide/protionamide528 (19)401 (41)194 (48)212 (59)1335 (29)
      Cycloserine/terizidone125 (4)56 (5)76 (18)89 (24)346 (7)
      p-aminosalicylic acid391 (14)281 (31)125 (31)127 (43)924 (21)
    TB drugs tested+7.9±3.010.0±1.310.2±0.99.6±1.78.5±2.1
    Total number of TB drugs to which strain was resistant§
     22259 (47)0002259 (34)
     3947 (20)15 (1)19 (4)0981 (15)
     4784 (16)100 (9)66 (15)4 (1)954 (14)
     5513 (11)331 (29)101 (24)32 (8)977 (15)
     6209 (4)296 (26)118 (28)108 (27)731 (11)
     742 (1)221 (20)89 (21)105 (26)457 (7)
     89 (0.2)128 (11)25 (6)75 (19)237 (4)
     9037 (3)8 (2)46 (11)91 (1)
     ≥1002 (0.2)035 (9)37 (0.3)
    • Data are presented as n, n (%) or mean±sd. Drug-susceptibility test results for Group 5 drugs were available from very few centres and were not analysed. n (%) data are presented for the number of cases whose isolate was tested to that specific drug. All cases were tested for susceptibility to at least one fluoroquinolone (FQ) and one second-line injectable drug, but not all the other drugs. #: Most centres tested only for resistance to ofloxacin. Very few centres also tested for resistance to later-generation FQs (results of these tests are not shown). By definition, two patient groups were susceptible to FQ. ¶: Resistance to amikacin or kanamycin combined. Most centres tested for susceptibility to only one of these two drugs and considered them cross-resistant. +: Includes tests to isoniazid and rifampin, as well as to FQs and second-line injectable drugs (performed in all cases). §: In addition to isoniazid and rifampin, to which all patients were resistant, being MDR-TB. MDR-TB: multidrug-resistant tuberculosis (resistance to at least isoniazid and rifampicin); MDR-TB only: MDR-TB, but susceptible to FQs, amikacin/kanamycin and capreomycin (at least one second-line injectable drug tested); MDR-TB+INJr: MDR-TB plus resistance to amikacin/kanamycin and/or capreomycin, but susceptible to FQs; MDR-TB+FQr: MDR-TB plus resistance to any FQ, but susceptible to amikacin/kanamycin and/or capreomycin (at least one second-line injectable drug tested); XDR-TB: extensively drug-resistant tuberculosis (MDR-TB plus resistance to any FQ and any second-line injectable drug (amikacin/kanamycin and/or capreomycin)).

  • Table 3– Treatment outcomes by multidrug-resistant tuberculosis (MDR-TB) patient group
    Pooled treatment outcomes#MDR-TB onlyMDR-TB +INJrMDR-TB +FQrXDR-TBTotal
    Subjects476311304264056724
    Treatment success64 (57–72)56 (45–66)48 (36–60)40 (27–53)62 (54–69)
    Treatment failure or relapse4 (2–6)12 (9–15)18 (14–21)22 (15–28)7 (4–9)
    Died8 (5–11)8 (3–14)11 (3–19)15 (8–23)9 (5–12)
    Defaulted18 (12–24)16 (7–24)12 (1–23)16 (8–24)17 (11–22)
    • Data are presented as n or % (95% CI). MDR-TB: multidrug-resistant TB (resistance to at least isoniazid and rifampicin); MDR-TB only: as MDR-TB, but susceptible to fluoroquinolones, amikacin/kanamycin and capreomycin (at least one second-line injectable drug tested); MDR-TB+INJr: MDR-TB plus resistance to amikacin/kanamycin and/or capreomycin, but susceptible to fluoroquinolones; MDR-TB+FQr: MDR-TB plus resistance to any fluoroquinolone, but susceptible to amikacin/kanamycin and/or capreomycin (at least one second-line injectable drug tested); XDR-TB: extensively drug-resistant tuberculosis (MDR-TB plus resistance to any fluoroquinolone and any second-line injectable drug (amikacin/kanamycin and/or capreomycin)). #: from study level meta-analysis; column percentages do not total 100%. See the Methods section and [17] for treatment outcome definitions.

  • Table 4– Association of treatment success with patient characteristics and multidrug-resistant tuberculosis (MDR-TB) patient group
    CasesAdjusted odds of treatment success versus treatment failure/relapse/death#
    Male (versus female)¶46531.0 (0.9–1.1)
    Older age (per 10-year increment) ¶67240.8 (0.8–0.9)
    HIV infected (versus not HIV infected) ¶6150.3 (0.2–0.4)
    Extensive disease (versus not extensive) ¶47920.5 (0.4–0.6)
    Previous TB treatment¶
     None12751.0 (Reference)
     First-line drugs only44100.6 (0.5–0.8)
     First-line and second-line drugs6180.2 (0.15–0.3)
    MDR-TB patient group+
     MDR-TB only47631.0 (Reference)
     MDR+INJr11300.6 (0.5–0.7)
     MDR+FQr4260.3 (0.2–0.4)
     XDR-TB4050.2 (0.2–0.3)
    Pulmonary resection surgery performed (versus no pulmonary resection surgery)+3731.5 (0.9–2.6)
    Experienced a serious adverse event (versus no serious adverse event)+15111.0 (0.8–1.2)
    • Data are presented as n or adjusted OR (95% CI). TB: tuberculosis; MDR-TB: multidrug-resistant TB (resistance to at least isoniazid and rifampicin); MDR-TB only: MDR-TB, but susceptible to fluoroquinolones, amikacin/kanamycin and capreomycin (at least one second-line injectable drug tested); MDR-TB+INJr: MDR-TB plus resistance to amikacin/kanamycin and/or capreomycin, but susceptible to fluoroquinolones; MDR-TB+FQr: MDR-TB plus resistance to any fluoroquinolone, but susceptible to amikacin/kanamycin and/or capreomycin (at least one second-line injectable drug tested); XDR-TB: extensively drug-resistant tuberculosis (MDR-TB plus resistance to any fluoroquinolone and any second-line injectable drug (amikacin/kanamycin and/or capreomycin)). #: odds ratios of treatment success (cure and completion) versus treatment failure/relapse/death adjusted for age, sex, HIV infection, previous TB treatment, previous MDR treatment (treatment for >1 month with two or more second-line drugs) and extent of disease. See Methods and [17] for treatment outcome definitions. ¶: estimate adjusted for all other covariates (characteristics) shown. +: each of these parameters estimated separately, and adjusted for age, sex, HIV, extent of disease and previous treatment with first- or second-line TB drugs. Statistical significance is represented by bold type.

  • Table 5– Association of treatment success with individual drugs used in treatment by multidrug-resistant tuberculosis (MDR-TB) patient group
    MDR-TB onlyMDR-TB+INJrMDR-TB+FQrXDR-TB
    Cases# nAdjusted OR (95% CI)¶Cases# nAdjusted OR (95% CI)¶Cases# nAdjusted OR (95% CI)¶Cases# nAdjusted OR (95% CI)¶
    First-line drugs
     Pyrazinamide24801.3 (0.8–2.0)4741.2 (0.8–1.8)1710.8 (0.4–1.5)1741.1 (0.6–2.0)
     Ethambutol17940.7 (0.5–0.9)2710.8 (0.6–1.2)940.7 (0.4–1.3)931.8 (0.9–3.5)
    Injectable drugs+
     Amikacin or kanamycin225015313585
      versus no injectable drug1.9 (1.1–3.1)2.0 (0.7–5.4)0.8 (0.1–5.6)2.0 (0.5–8.7)
      versus capreomycin1.1 (0.6–1.9)1.8 (0.9–3.6)1.1 (0.2–5.9)1.2 (0.3–5.3)
      versus streptomycin1.4 (0.9–2.3)2.4 (1.1–5.0)1.1 (0.3–4.3)1.7 (0.3–7.9)
     Capreomycin only20443534109
      versus no injectable drug2.2 (1.1–4.2)0.9 (0.2–4.1)2.5 (0.9–7.0)
      versus streptomycin1.4 (0.6–3.3)0.8 (0.2–3.9)1.4 (0.1–14)
    Fluoroquinolones§
     Ofloxacin2956787197227
      versus no fluoroquinolone2.9 (1.7–4.9)2.8 (0.9–8.6)1.1 (0.5–2.4)0.7 (0.3–1.6)
      versus ciprofloxacin1.2 (0.5–3.2)1.8 (0.1–23)1.0 (0.1–19)0.2 (0.1–3.6)
    Group 4 drugs
     Ethionamide or protionamide29732.2 (1.5–3.2)6891.6 (1.0–2.4)2580.8 (0.4–1.7)2531.0 (0.5–2.1)
     Cycloserine or terizidone20071.8 (1.4–2.2)8221.7 (0.8–3.9)2920.9 (0.3–3.0)2841.3 (0.5–3.6)
     p-aminosalicylic acid13961.0 (0.8–1.3)6141.1 (0.7–1.6)2191.1 (0.6–2.3)2281.3 (0.6–3.1)
    Group 5 drugsƒ
     Any one group 5 drug versus none5610.8 (0.6–1.2)3230.9 (0.5–1.6)840.6 (0.3–1.4)951.1 (0.4–2.9)
     Two or more group 5 drugs versus one1350.5 (0.2–0.9)1110.6 (0.3–1.5)550.8 (0.3–1.8)581.2 (0.5–3.3)
    • MDR-TB: multidrug-resistant TB (resistance to at least isoniazid and rifampicin); MDR-TB only: MDR-TB, but susceptible to fluoroquinolones, amikacin/kanamycin and capreomycin (at least one second-line injectable drug tested); MDR-TB+INJr: MDR-TB plus resistance to amikacin/kanamycin and/or capreomycin, but susceptible to fluoroquinolones; MDR-TB+FQr: MDR-TB plus resistance to any fluoroquinolone, but susceptible to amikacin/kanamycin and/or capreomycin (at least one second-line injectable drug tested); XDR-TB: extensively drug-resistant tuberculosis (MDR-TB plus resistance to any fluoroquinolone and any second-line injectable drug (amikacin/kanamycin and/or capreomycin)). #: number of cases that received the drug in question and were included in the specific analysis. ¶: odds ratios of treatment success (cure and completion) versus treatment failure/relapse/death adjusted for age, sex, HIV infection, previous TB treatment, previous MDR treatment (treatment for >1 month with two or more second-line drugs) and extent of disease. If there were <50 observations no estimate was derived. See Methods and [17] for treatment outcome definitions. +: patients receiving two or more injectable drugs were excluded from this analysis. §: patients receiving two or more fluoroquinolones were excluded from this analysis. Insufficient numbers of patients received later-generation fluoroquinolones (including gatifloxacin, levofloxacin, moxifloxacin and sparfloxacin) within the MDR-TB patient groups with additional resistance, so were not analysed. ƒ: insufficient numbers of patients received specific group 5 drugs within the MDR-TB patient groups with additional resistance, so outcomes by individual group 5 drugs were not analysed. Group 5 drugs included amoxicillin/clavulanate, macrolides (azithromycin, clarithromycin and roxithromycin), clofazimine, thiacetazone, imipenem, linezolid, high-dose isoniazid and thioridazine. Statistical significance is represented by bold type.

  • Table 6– Association of treatment success with the number of effective drugs used in the intensive and continuation phases of treatment by the multidrug-resistant tuberculosis (MDR-TB) patient group
    Number of drugsMDR-TB onlyMDR-TB+INJrMDR-TB+FQrXDR-TB
    Cases nAdjusted OR# (95% CI)Cases nAdjusted OR# (95% CI)Cases nAdjusted OR# (95% CI)Cases nAdjusted OR# (95% CI)
    Intensive phase¶
     ≤2451.0 (reference)291.0 (reference)101.0 (reference)241.0 (reference)
     3621.1 (0.5–2.3)271.7 (0.5–5.2)321.0 (reference)471.0 (reference)
     41651.9 (1.0–3.7)831.3 (0.5–3.1)491.6 (0.7–3.8)461.9 (0.8–4.3)
     52961.7 (0.8–3.8)1371.2 (0.4–3.4)351.4 (0.3–6.4)361.8 (0.5–6.6)
     ≥63801.0 (0.5–1.8)1201.3 (0.5–3.3)271.1 (0.4–2.9)204.9 (1.4–16.6)
    Continuation phase+
     ≤2771.0 (reference)461.0 (reference)351.0 (reference)271.0 (reference)
     31335.9 (3.1–11.0)3312.2 (3.4–44)272.5 (0.8–7.4)323.3 (1.3–8.5)
     42396.0 (2.8–13.1)1013.7 (1.7–8.2)273.1 (0.5–21.1)286.1 (1.4–26.3)
     ≥52334.7 (2.7–8.1)1003.1 (1.7–6.0)202.3 (0.7–7.2)172.3 (0.7–7.6)
    • MDR-TB: multidrug-resistant TB (resistance to at least isoniazid and rifampicin); MDR-TB only: MDR-TB, but susceptible to fluoroquinolones, amikacin/kanamycin and capreomycin (at least one second-line injectable drug tested); MDR-TB+INJr: MDR-TB plus resistance to amikacin/kanamycin and/or capreomycin, but susceptible to fluoroquinolones; MDR-TB+FQr: MDR-TB plus resistance to any fluoroquinolone, but susceptible to amikacin/kanamycin and/or capreomycin (at least one second-line injectable drug tested); XDR-TB: extensively drug-resistant tuberculosis (MDR-TB plus resistance to any fluoroquinolone and any second-line injectable drug (amikacin/kanamycin and/or capreomycin)). #: odds ratios of treatment success (cure and completion) versus treatment failure/relapse/death adjusted for age, sex, HIV infection, previous TB treatment, previous MDR treatment (treatment for >1 month with two or more second-line drugs) and extent of disease. See Methods and [17] for treatment outcome definitions. ¶: the initial part of a course of treatment during which an injectable drug is given. +: the period immediately following the initial phase when no injectable drug is given. Only 18 studies provided information regarding drug susceptibility testing and the number of drugs in the intensive phase, while only 15 of these described the number of drugs in the continuation phase. Statistical significance is represented by bold type.

  • Table 7– Association between the duration of treatment and treatment success by multidrug-resistant tuberculosis (MDR-TB) patient group
    MDR-TB onlyMDR-TB+INJrMDR-TB+FQrXDR-TB
    Cases nAdjusted OR# (95%CI)Cases nAdjusted OR# (95%CI)Cases nAdjusted OR# (95%CI)Cases nAdjusted OR# (95%CI)
    Duration of intensive phase¶ months
     1–4.019241.0 (reference)991.0 (reference)331.0 (reference)551.0 (reference)
     4.1–6.52742.8 (0.8–9.7)823.2 (0.8–13.6)410.9 (0.2–4.5)416.1 (0.6–62)
     6.6–9.02443.1 (1.1–8.3)799.8 (1.9–49)360.6 (0.1–4.1)3771.0 (5.2–200)
     9.1–20.03472.1 (0.9–5.1)1554.1 (1.5–11.2)550.4 (0.1–2.0)775.1 (1.2–21)
    Total duration of treatment months
     6.0–15.04431.0 (reference)2791.0 (reference)541.0 (reference)871.0 (reference)
     15.1–20.021713.6 (1.7–7.9)2603.1 (1.0–9.1)472.4 (0.4–14.3)792.0 (0.3–11.7)
     20.1–25.04845.9 (3.0–11.5)2027.7 (3.8–15.7)602.1 (0.7–6.5)615.5 (1.7–17.6)
     25.1–30.01472.8 (1.2–6.9)656.0 (2.3–15.6)244.1 (0.9–19.4)215.8 (1.3–25.1)
     30.1–36.0611.8 (0.6–5.6)172.9 (0.7–12.2)131.1 (0.2–5.2)101.3 (0.2–7.8)
    • MDR-TB: multidrug-resistant TB (resistance to at least isoniazid and rifampicin); MDR-TB only: MDR-TB, but susceptible to fluoroquinolones, amikacin/kanamycin and capreomycin (at least one second-line injectable drug tested); MDR-TB+INJr: MDR-TB plus resistance to amikacin/kanamycin and/or capreomycin, but susceptible to fluoroquinolones; MDR-TB+FQr: MDR-TB plus resistance to any fluoroquinolone, but susceptible to amikacin/kanamycin and/or capreomycin (at least one second-line injectable drug tested); XDR-TB: extensively drug-resistant tuberculosis (MDR-TB plus resistance to any fluoroquinolone and any second-line injectable drug (amikacin/kanamycin and/or capreomycin)). #: Odds ratios of treatment success versus treatment failure or relapse adjusted for age, sex, HIV infection, previous TB treatment, previous MDR treatment (treatment for >1 month with two or more second-line drugs) and extent of disease. See Methods and [17] for treatment outcome definitions. ¶: The initial part of a course of treatment during which an injectable drug is given.

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Resistance to fluoroquinolones and second-line injectable drugs: impact on multidrug-resistant TB outcomes
Dennis Falzon, Neel Gandhi, Giovanni B. Migliori, Giovanni Sotgiu, Helen S. Cox, Timothy H. Holtz, Maria-Graciela Hollm-Delgado, Salmaan Keshavjee, Kathryn DeRiemer, Rosella Centis, Lia D'Ambrosio, Christoph G. Lange, Melissa Bauer, Dick Menzies
European Respiratory Journal Jul 2013, 42 (1) 156-168; DOI: 10.1183/09031936.00134712

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Resistance to fluoroquinolones and second-line injectable drugs: impact on multidrug-resistant TB outcomes
Dennis Falzon, Neel Gandhi, Giovanni B. Migliori, Giovanni Sotgiu, Helen S. Cox, Timothy H. Holtz, Maria-Graciela Hollm-Delgado, Salmaan Keshavjee, Kathryn DeRiemer, Rosella Centis, Lia D'Ambrosio, Christoph G. Lange, Melissa Bauer, Dick Menzies
European Respiratory Journal Jul 2013, 42 (1) 156-168; DOI: 10.1183/09031936.00134712
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