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Effectiveness and safety of bedaquiline-containing regimens in the treatment of MDR- and XDR-TB: a multicentre study

Sergey E. Borisov, Keertan Dheda, Martin Enwerem, Rodolfo Romero Leyet, Lia D'Ambrosio, Rosella Centis, Giovanni Sotgiu, Simon Tiberi, Jan-Willem Alffenaar, Andrey Maryandyshev, Evgeny Belilovski, Shashank Ganatra, Alena Skrahina, Onno Akkerman, Alena Aleksa, Rohit Amale, Janina Artsukevich, Judith Bruchfeld, Jose A. Caminero, Isabel Carpena Martinez, Luigi Codecasa, Margareth Dalcolmo, Justin Denholm, Paul Douglas, Raquel Duarte, Aliasgar Esmail, Mohammed Fadul, Alexey Filippov, Lina Davies Forsman, Mina Gaga, Julia-Amaranta Garcia-Fuertes, José-María García-García, Gina Gualano, Jerker Jonsson, Heinke Kunst, Jillian S. Lau, Barbara Lazaro Mastrapa, Jorge Lazaro Teran Troya, Selene Manga, Katerina Manika, Pablo González Montaner, Jai Mullerpattan, Suzette Oelofse, Martina Ortelli, Domingo Juan Palmero, Fabrizio Palmieri, Antonella Papalia, Apostolos Papavasileiou, Marie-Christine Payen, Emanuele Pontali, Carlos Robalo Cordeiro, Laura Saderi, Tsetan Dorji Sadutshang, Tatsiana Sanukevich, Varvara Solodovnikova, Antonio Spanevello, Sonam Topgyal, Federica Toscanini, Adrian R. Tramontana, Zarir Farokh Udwadia, Pietro Viggiani, Veronica White, Alimuddin Zumla, Giovanni Battista Migliori
European Respiratory Journal 2017 49: 1700387; DOI: 10.1183/13993003.00387-2017
Sergey E. Borisov
1Moscow Research and Clinical Center for TB Control, Moscow Government's Health Department, Moscow, Russian Federation
50These authors contributed equally
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Keertan Dheda
2UCT Lung Institute, Division of Pulmonology, University of Cape Town, Cape Town, South Africa
50These authors contributed equally
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Martin Enwerem
3Amity Health Consortium, Country Club Estate, Johannesburg, South Africa
50These authors contributed equally
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Rodolfo Romero Leyet
4Clinical Unit, District Clinical Specialist Team, Springbok, South Africa
50These authors contributed equally
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Lia D'Ambrosio
5World Health Organization Collaborating Centre for Tuberculosis and Lung Diseases, Maugeri Care and Research Institute, Tradate, Italy
6Public Health Consulting Group, Lugano, Switzerland
50These authors contributed equally
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Rosella Centis
5World Health Organization Collaborating Centre for Tuberculosis and Lung Diseases, Maugeri Care and Research Institute, Tradate, Italy
50These authors contributed equally
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Giovanni Sotgiu
7Clinical Epidemiology and Medical Statistics Unit, Dept of Biomedical Sciences, University of Sassari, Sassari, Italy
50These authors contributed equally
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Simon Tiberi
8Division of Infection, Royal London Hospital, Barts Health NHS Trust, London, UK
9Blizard Institute, Barts and The London School of Medicine and Dentistry, Queen Mary University of London, London, UK
50These authors contributed equally
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Jan-Willem Alffenaar
10University of Groningen, University Medical Center Groningen, Dept of Clinical Pharmacy and Pharmacology, Groningen, The Netherlands
50These authors contributed equally
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Andrey Maryandyshev
11Northern State Medical University, Arkhangelsk, Russian Federation
50These authors contributed equally
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Evgeny Belilovski
1Moscow Research and Clinical Center for TB Control, Moscow Government's Health Department, Moscow, Russian Federation
50These authors contributed equally
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Shashank Ganatra
12Dept of Respiratory Medicine, P.D. Hinduja National Hospital and MRC, Mumbai, India
50These authors contributed equally
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Alena Skrahina
13Republican Research and Practical Centre for Pulmonology and Tuberculosis, Minsk, Belarus
50These authors contributed equally
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Onno Akkerman
14University of Groningen, University Medical Center Groningen, Tuberculosis Center Beatrixoord, Haren, The Netherlands
15University of Groningen, University Medical Center Groningen, Dept of Pulmonary Diseases and Tuberculosis, Groningen, The Netherlands
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Alena Aleksa
16Dept of Phthisiology, Grodno State Medical University, GRCC “Phthisiology”, Grodno, Belarus
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Rohit Amale
12Dept of Respiratory Medicine, P.D. Hinduja National Hospital and MRC, Mumbai, India
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Janina Artsukevich
16Dept of Phthisiology, Grodno State Medical University, GRCC “Phthisiology”, Grodno, Belarus
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Judith Bruchfeld
17Unit of Infectious Diseases, Dept of Medicine, Solna, Karolinska Institute, Dept of Infectious Diseases, Karolinska University Hospital, Stockholm, Sweden
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Jose A. Caminero
18Pneumology Dept, Hospital General de Gran Canaria “Dr Negrin”, Las Palmas de Gran Canaria, Spain
19MDR-TB Unit, Tuberculosis Division, International Union against Tuberculosis and Lung Disease (The Union), Paris, France
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Isabel Carpena Martinez
20General University Hospital Morales Meseguer, Murcia, Spain
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Luigi Codecasa
21TB Reference Centre, Villa Marelli Institute/Niguarda Hospital, Milan, Italy
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Margareth Dalcolmo
22Hélio Fraga Reference Center, Fiocruz/MoH, Rio de Janeiro, Brazil
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Justin Denholm
23Victorian Tuberculosis Program, Melbourne Health, Dept of Microbiology and Immunology, University of Melbourne, Peter Doherty Institute for Infection and Immunity, Melbourne, Australia
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Paul Douglas
24Health Policy and Performance Branch, Health Services and Policy Division, Dept of Immigration and Border Protection, Sydney, Australia
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Raquel Duarte
25National Reference Centre for MDR-TB, Hospital Centre Vila Nova de Gaia, Dept of Pneumology, Public Health Science and Medical Education Department, Faculty of Medicine, University of Porto, Porto, Portugal
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Aliasgar Esmail
26UCT Lung Institute, Lung Infection and Immunity Unit, Division of Pulmonology, Dept of Medicine, University of Cape Town, Groote Schuur Hospital, Cape Town, South Africa
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Mohammed Fadul
26UCT Lung Institute, Lung Infection and Immunity Unit, Division of Pulmonology, Dept of Medicine, University of Cape Town, Groote Schuur Hospital, Cape Town, South Africa
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Alexey Filippov
1Moscow Research and Clinical Center for TB Control, Moscow Government's Health Department, Moscow, Russian Federation
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Lina Davies Forsman
17Unit of Infectious Diseases, Dept of Medicine, Solna, Karolinska Institute, Dept of Infectious Diseases, Karolinska University Hospital, Stockholm, Sweden
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Mina Gaga
277th Respiratory Medicine Dept, Athens Chest Hospital, Athens, Greece
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Julia-Amaranta Garcia-Fuertes
28Bronchiectasis Unit, Respiratory Dept, Hospital Universitario Araba, Vitoria-Gasteiz, Spain
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José-María García-García
29Tuberculosis Research Programme, SEPAR, Barcelona, Spain
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Gina Gualano
30Respiratory Infectious Diseases Unit, National Institute for Infectious Diseases “L. Spallanzani”, IRCCS, Rome, Italy
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Jerker Jonsson
31National TB Surveillance Unit, Public Health Agency, Stockholm, Sweden
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Heinke Kunst
9Blizard Institute, Barts and The London School of Medicine and Dentistry, Queen Mary University of London, London, UK
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Jillian S. Lau
32Dept of Infectious Diseases, Box Hill Hospital, Victoria, Australia
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Barbara Lazaro Mastrapa
33Harry Surtie Hospital, Upington, South Africa
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Jorge Lazaro Teran Troya
33Harry Surtie Hospital, Upington, South Africa
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Selene Manga
34Dept of Infectious Diseases, University National San Antonio Abad Cusco, Cusco, Perù
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Katerina Manika
35Pulmonary Dept, ‘G. Papanikolaou’ Hospital, Aristotle University, Thessaloniki, Greece
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Pablo González Montaner
36Pulmonology Division, Municipal Hospital F. J. Munĩz, Buenos Aires, Argentina
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Jai Mullerpattan
12Dept of Respiratory Medicine, P.D. Hinduja National Hospital and MRC, Mumbai, India
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Suzette Oelofse
26UCT Lung Institute, Lung Infection and Immunity Unit, Division of Pulmonology, Dept of Medicine, University of Cape Town, Groote Schuur Hospital, Cape Town, South Africa
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Martina Ortelli
37Pneumology Dept, University of Insubria, Varese, Italy
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Domingo Juan Palmero
36Pulmonology Division, Municipal Hospital F. J. Munĩz, Buenos Aires, Argentina
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Fabrizio Palmieri
30Respiratory Infectious Diseases Unit, National Institute for Infectious Diseases “L. Spallanzani”, IRCCS, Rome, Italy
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Antonella Papalia
38AOVV Eugenio Morelli Hospital, Reference Hospital for MDR and HIV-TB, Sondalo, Italy
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Apostolos Papavasileiou
39MDR-TB Unit, Athens Chest Hospital, Ministry of Health, Athens, Greece
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Marie-Christine Payen
40Division of Infectious Diseases, CHU Saint-Pierre, Université Libre de Bruxelles (ULB), Brussels, Belgium
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Emanuele Pontali
41Dept of Infectious Diseases, Galliera Hospital, Genoa, Italy
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Carlos Robalo Cordeiro
42Coimbra Medical School, Pneumology Dept, Coimbra University Hospital, Coimbra, Portugal
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Laura Saderi
7Clinical Epidemiology and Medical Statistics Unit, Dept of Biomedical Sciences, University of Sassari, Sassari, Italy
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Tsetan Dorji Sadutshang
43Delek Hospital, Dharamshala, India
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Tatsiana Sanukevich
16Dept of Phthisiology, Grodno State Medical University, GRCC “Phthisiology”, Grodno, Belarus
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Varvara Solodovnikova
13Republican Research and Practical Centre for Pulmonology and Tuberculosis, Minsk, Belarus
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Antonio Spanevello
44Pneumology Dept, Maugeri Care and Research Institute, Tradate, Italy
45Dept of Clinical and Experimental Medicine, University of Insubria, Varese, Italy
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Sonam Topgyal
43Delek Hospital, Dharamshala, India
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Federica Toscanini
46University Hospital San Martino, Care and Research Institute, National Institute for Cancer Research, Genoa, Italy
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Adrian R. Tramontana
47Dept of Infectious Diseases, Western Hospital, Victoria, Australia
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Zarir Farokh Udwadia
12Dept of Respiratory Medicine, P.D. Hinduja National Hospital and MRC, Mumbai, India
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Pietro Viggiani
38AOVV Eugenio Morelli Hospital, Reference Hospital for MDR and HIV-TB, Sondalo, Italy
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Veronica White
48Dept of Respiratory Medicine, Barts Healthcare NHS Trust, London, UK
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Alimuddin Zumla
49Division of Infection and Immunity, University College London and NIHR Biomedical Research Centre, UCL Hospitals NHS Foundation Trust, London, UK
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Giovanni Battista Migliori
5World Health Organization Collaborating Centre for Tuberculosis and Lung Diseases, Maugeri Care and Research Institute, Tradate, Italy
50These authors contributed equally
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  • For correspondence: giovannibattista.migliori@icsmaugeri.it
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  • FIGURE 1
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    FIGURE 1

    Global distribution of multidrug-resistant and extensively drug-resistant tuberculosis cases treated with regimens containing bedaquiline, 2009–2016. n=428 cases in 25 study sites (online supplementary table S1).

  • FIGURE 2
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    FIGURE 2

    Median (interquartile range) values of the Friderica-corrected QT interval (QTcF) and its temporal trends in the cohort in the initial 12 weeks of treatment. Few patients underwent ECG after week 12.

  • FIGURE 3
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    FIGURE 3

    Sputum smear and culture conversion rates of 428 culture-confirmed multidrug-resistant tuberculosis patients exposed to bedaquiline-containing regimens.

Tables

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  • TABLE 1

    Demographic, epidemiological and clinical characteristics of 428 culture-confirmed multidrug-resistant tuberculosis (MDR-TB) patients exposed to bedaquiline-containing regimens

    Age years35 (27–44)
    Male263/428 (61.5)
    Body weight at admission kg56 (47–65)
    Height cm169 (160–176)
    Migrant45/428 (10.5)
    Employed110/413 (26.6)
    Prisoner23/413 (5.6)
    Pregnant1/133 (0.8)
    Thyroid disease12/413 (2.9)
    Heart disease40/318 (12.6)
    Pre-existing ECG abnormality13/318 (4.1)
    Alcoholism132/363 (36.4)
    Drug abuse75/413 (18.2)
    Methadone use0/318 (0.0)
    Diabetes26/413 (6.3)
    HIV infection testing425/428 (99.3)
    HIV-positive94/425 (22.1)
    CD4 count at baseline cells·mm-3269 (168–470)
    Nadir CD4+ cell count cells·mm-3222 (160–402)
    Antiretroviral therapy exposure92/94 (97.9)
    Prior anti-TB therapy334/428 (78.0)
    Prior courses of treatment lasting >1 month n2 (1–2)
    Prior TB treatment outcome
     Success68/263 (25.9)
     Cure41/263 (15.6)
     Completion27/263 (10.3)
     Default35/263 (13.3)
     Transfer out20/263 (7.6)
     Failure140/263 (53.2)
    Pulmonary surgery55/423 (13.0)
    Previous MDR-TB169/317 (53.3)
    Pulmonary involvement426/428 (99.5)
    Extrapulmonary involvement11/428 (2.6)
    Radiology involvement
     Cavitary lesion81/331 (24.5)
     Bilateral pulmonary with cavitary lesions147/331 (44.4)
     Bilateral pulmonary56/331 (16.9)
     Noncavitary nonbilateral pulmonary47/331 (14.2)
    Sputum smear positive305/423 (72.1)
    Sputum culture positive421/428 (98.4)
    Drug resistance
     Streptomycin185/196 (94.4)
     Ethambutol186/240 (77.5)
     Pyrazinamide145/206 (70.4)
     Fluoroquinolones267/414 (64.5)
     Amikacin131/295 (44.4)
     Capreomycin127/305 (41.6)
     Kanamycin179/302 (59.3)
     Ethionamide135/226 (59.7)
     Cycloserine20/163 (12.3)
     Para-aminosalicylic acid70/196 (35.7)
     Linezolid4/38 (10.5)
     Rifabutin32/35 (91.4)
    XDR-TB195/428 (45.6)
    MDR- or XDR-TB contacts105/411 (25.6)
    Hospital stay days179 (92–280)
    • Data are presented as median (interquartile range) or n/N (%). XDR-TB: extensively drug-resistant tuberculosis.

  • TABLE 2

    Safety and tolerability profile of bedaquiline-containing regimens in a cohort of 428 culture-confirmed multidrug-resistant tuberculosis patients

    Interruption of bedaquiline51/428 (11.9)
    Interruption of bedaquiline due to adverse events25/428 (5.8)
    Adverse events presumably due to bedaquiline80/213 (19.4)
    Bedaquiline restarted if interrupted25/69 (36.2)
    Total bedaquiline exposure days168 (86–180)
    Creatinine >1.4×ULN91/411 (22.1)
    Lipase >1.6×ULN1/239 (0.4)
    ALT >3×ULN92/413 (22.3)
    Bilirubin >2×ULN47/413 (11.4)
    Albumin g·dL−136 (30–40)
    Potassium <3.4 or >5.6 mmol·L−198/412 (23.8)
    Magnesium <0.59 mmol·L−121/199 (10.6)
    Calcium <1.75 mmol·L−123/302 (7.6)
    Adverse effects
     Nausea130/413 (31.5)
     Peripheral neuropathy96/412 (23.3)
     Otovestibular toxicity96/412 (23.3)
     Vomiting87/411 (21.2)
     Anaemia86/412 (20.9)
     Arthralgia84/412 (20.4)
     Skin rash63/412 (15.3)
     Diarrhoea56/412 (13.6)
     Renal failure47/413 (11.4)
     Thrombocytopenia41/413 (9.9)
     Neutropenia40/413 (9.7)
     Lymphocytopenia40/413 (9.7)
     QT prolongation24/248 (9.7)
     Hypothyroidism38/410 (9.3)
     Psychiatric disorder29/413 (7.0)
     Tendinopathy18/413 (4.4)
     Optic neuropathy10/413 (2.4)
     Deep vein thrombosis7/412 (1.7)
     Pancreatitis4/318 (1.3)
     Hallucinations2/411 (0.5)
     Stroke1/318 (0.3)
    • Data are presented as n/N (%) or median (interquartile range). ULN: upper limit of normal; ALT: alanine-transaminase.

  • TABLE 3

    Treatment outcome and conversion rates of culture-confirmed multidrug-resistant tuberculosis (MDR-TB) patients exposed to bedaquiline-containing regimens and treatment outcomes of MDR-TB patients starting their treatment with bedaquiline-containing regimens before December 31, 2014

    Bedaquiline-containing regimenBedaquiline-containing regimen started before December 31, 2014
    Patients n428130
    Sputum smear conversion 30 days206/324 (63.6)
    Sputum culture conversion 30 days117/389 (30.1)
    Sputum smear conversion 60 days257/317 (81.1)
    Sputum culture conversion 60 days213/376 (56.7)
    Sputum smear conversion 90 days265/310 (85.5)
    Sputum culture conversion 90 days298/370 (80.5)
    Sputum smear conversion at the end of treatment126/140 (90.0)
    Sputum culture conversion at the end of treatment191/208 (91.8)
    Time to sputum smear conversion days4 (30–60)
    Time to sputum culture conversion days60 (33–90)
    Treatment outcome
     Success176/247 (71.3)100/130 (76.9)
     Cure154/247 (62.4)86/130 (66.2)
     Completion22/247 (8.9)14/130 (10.8)
     Death33/247 (13.4)8/130 (6.2)
     Default18/247 (7.3)6/130 (4.6)
     Failure19/247 (7.7)16/130 (12.3)
     Transfer out1/247 (0.4)
    Duration of treatment after MDR-TB diagnosis months18 (10–22)
    Body weight at end of treatment kg61.9±13.9
    • Data are presented as n/N (%), median (interquartile range) or mean±sd, unless otherwise stated.

  • TABLE 4

    Treatment outcomes of 428 culture-confirmed multidrug resistant (MDR-) and extensively drug-resistant tuberculosis (XDR-TB) patients exposed to bedaquiline-containing regimens in different settings and stratified by cohort

    AfricaEastern EuropeOther settings2008–20092010–20112012–2014
    Total cohort11385499121
     Success73 (64.6)65 (76.5)38 (77.6)5 (55.6)95 (78.5)
     Cure73 (64.6)54 (63.5)27 (55.1)5 (55.6)81 (66.9)
     Completion11 (12.9)11 (22.5)0 (0.0)14 (11.6)
     Death27 (23.9)3 (3.5)3 (6.1)2 (22.2)6 (5.0)
     Default9 (8.0)8 (9.4)1 (2.0)2 (22.2)4 (3.3)
     Failure3 (2.7)9 (10.6)7 (14.3)0 (0.0)16 (13.2)
     Transfer out1 (0.9)
    MDR-TB623927
     Success36 (58.1)28 (71.8)22 (81.5)
     Cure36 (58.1)20 (51.3)11 (40.7)
     Completion8 (20.5)11 (40.7)
     Death17 (27.4)3 (7.7)1 (3.7)
     Default7 (11.3)3 (7.7)1 (3.7)
     Failure1 (1.6)5 (12.8)3 (11.1)
     Transfer out1 (1.6)
    XDR-TB514622
     Success37 (72.6)37 (80.4)16 (72.7)
     Cure37 (72.6)34 (73.9)16 (72.7)
     Completion3 (6.5)
     Death10 (19.6)2 (9.1)
     Default2 (3.9)5 (10.9)
     Failure2 (3.9)4 (8.7)4 (18.2)
     Transfer out
    • Data are presented as n or n (%).

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    Supplementary table S1 ERJ-00387-2017_Supplementary_table_S1

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    Onno Akkerman ERJ-00387-2017_Akkerman

    Luigi Codecasa ERJ-00387-2017_Codecasa

    M-C. Payen ERJ-00387-2017_Payen

    E. Pontali ERJ-00387-2017_Pontali

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Vol 49 Issue 5 Table of Contents
European Respiratory Journal: 49 (5)
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Effectiveness and safety of bedaquiline-containing regimens in the treatment of MDR- and XDR-TB: a multicentre study
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Effectiveness and safety of bedaquiline-containing regimens in the treatment of MDR- and XDR-TB: a multicentre study
Sergey E. Borisov, Keertan Dheda, Martin Enwerem, Rodolfo Romero Leyet, Lia D'Ambrosio, Rosella Centis, Giovanni Sotgiu, Simon Tiberi, Jan-Willem Alffenaar, Andrey Maryandyshev, Evgeny Belilovski, Shashank Ganatra, Alena Skrahina, Onno Akkerman, Alena Aleksa, Rohit Amale, Janina Artsukevich, Judith Bruchfeld, Jose A. Caminero, Isabel Carpena Martinez, Luigi Codecasa, Margareth Dalcolmo, Justin Denholm, Paul Douglas, Raquel Duarte, Aliasgar Esmail, Mohammed Fadul, Alexey Filippov, Lina Davies Forsman, Mina Gaga, Julia-Amaranta Garcia-Fuertes, José-María García-García, Gina Gualano, Jerker Jonsson, Heinke Kunst, Jillian S. Lau, Barbara Lazaro Mastrapa, Jorge Lazaro Teran Troya, Selene Manga, Katerina Manika, Pablo González Montaner, Jai Mullerpattan, Suzette Oelofse, Martina Ortelli, Domingo Juan Palmero, Fabrizio Palmieri, Antonella Papalia, Apostolos Papavasileiou, Marie-Christine Payen, Emanuele Pontali, Carlos Robalo Cordeiro, Laura Saderi, Tsetan Dorji Sadutshang, Tatsiana Sanukevich, Varvara Solodovnikova, Antonio Spanevello, Sonam Topgyal, Federica Toscanini, Adrian R. Tramontana, Zarir Farokh Udwadia, Pietro Viggiani, Veronica White, Alimuddin Zumla, Giovanni Battista Migliori
European Respiratory Journal May 2017, 49 (5) 1700387; DOI: 10.1183/13993003.00387-2017

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Effectiveness and safety of bedaquiline-containing regimens in the treatment of MDR- and XDR-TB: a multicentre study
Sergey E. Borisov, Keertan Dheda, Martin Enwerem, Rodolfo Romero Leyet, Lia D'Ambrosio, Rosella Centis, Giovanni Sotgiu, Simon Tiberi, Jan-Willem Alffenaar, Andrey Maryandyshev, Evgeny Belilovski, Shashank Ganatra, Alena Skrahina, Onno Akkerman, Alena Aleksa, Rohit Amale, Janina Artsukevich, Judith Bruchfeld, Jose A. Caminero, Isabel Carpena Martinez, Luigi Codecasa, Margareth Dalcolmo, Justin Denholm, Paul Douglas, Raquel Duarte, Aliasgar Esmail, Mohammed Fadul, Alexey Filippov, Lina Davies Forsman, Mina Gaga, Julia-Amaranta Garcia-Fuertes, José-María García-García, Gina Gualano, Jerker Jonsson, Heinke Kunst, Jillian S. Lau, Barbara Lazaro Mastrapa, Jorge Lazaro Teran Troya, Selene Manga, Katerina Manika, Pablo González Montaner, Jai Mullerpattan, Suzette Oelofse, Martina Ortelli, Domingo Juan Palmero, Fabrizio Palmieri, Antonella Papalia, Apostolos Papavasileiou, Marie-Christine Payen, Emanuele Pontali, Carlos Robalo Cordeiro, Laura Saderi, Tsetan Dorji Sadutshang, Tatsiana Sanukevich, Varvara Solodovnikova, Antonio Spanevello, Sonam Topgyal, Federica Toscanini, Adrian R. Tramontana, Zarir Farokh Udwadia, Pietro Viggiani, Veronica White, Alimuddin Zumla, Giovanni Battista Migliori
European Respiratory Journal May 2017, 49 (5) 1700387; DOI: 10.1183/13993003.00387-2017
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