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The New England journal of medicine
01 19, 2017;376 (3): 243-253.

Transmission of Extensively Drug-Resistant Tuberculosis in South Africa.

N Sarita Shah, Sara C Auld, James C M Brust, Barun Mathema, Nazir Ismail, Pravi Moodley, Koleka Mlisana, Salim Allana, Angela Campbell, Thuli Mthiyane, Natashia Morris, Primrose Mpangase, Hermina van der Meulen, Shaheed V Omar, Tyler S Brown, Apurva Narechania, Elena Shaskina, Thandi Kapwata, Barry Kreiswirth, Neel R Gandhi
Author Information
  1. N Sarita Shah: From the Emory University Rollins School of Public Health and School of Medicine (N.S.S., S.C.A., S.A., A.C., N.R.G.) and the Centers for Disease Control and Prevention (N.S.S.) - both in Atlanta; Albert Einstein College of Medicine and Montefiore Medical Center (N.S.S., J.C.M.B., N.R.G.), Columbia University Mailman School of Public Health (B.M., T.S.B.), and the American Museum of Natural History (A.N.) - all in New York; the National Institute for Communicable Diseases, Johannesburg (N.I., H.M., S.V.O.), University of KwaZulu-Natal and National Health Laboratory Service, Durban (P. Moodley, K.M., T.M., P. Mpangase), and the South African Medical Research Council, Cape Town (N.M., T.K.) - all in South Africa; and the Public Health Research Institute, New Jersey Medical School-Rutgers University, Newark (E.S., B.K.).
  2. Sara C Auld: From the Emory University Rollins School of Public Health and School of Medicine (N.S.S., S.C.A., S.A., A.C., N.R.G.) and the Centers for Disease Control and Prevention (N.S.S.) - both in Atlanta; Albert Einstein College of Medicine and Montefiore Medical Center (N.S.S., J.C.M.B., N.R.G.), Columbia University Mailman School of Public Health (B.M., T.S.B.), and the American Museum of Natural History (A.N.) - all in New York; the National Institute for Communicable Diseases, Johannesburg (N.I., H.M., S.V.O.), University of KwaZulu-Natal and National Health Laboratory Service, Durban (P. Moodley, K.M., T.M., P. Mpangase), and the South African Medical Research Council, Cape Town (N.M., T.K.) - all in South Africa; and the Public Health Research Institute, New Jersey Medical School-Rutgers University, Newark (E.S., B.K.).
  3. James C M Brust: From the Emory University Rollins School of Public Health and School of Medicine (N.S.S., S.C.A., S.A., A.C., N.R.G.) and the Centers for Disease Control and Prevention (N.S.S.) - both in Atlanta; Albert Einstein College of Medicine and Montefiore Medical Center (N.S.S., J.C.M.B., N.R.G.), Columbia University Mailman School of Public Health (B.M., T.S.B.), and the American Museum of Natural History (A.N.) - all in New York; the National Institute for Communicable Diseases, Johannesburg (N.I., H.M., S.V.O.), University of KwaZulu-Natal and National Health Laboratory Service, Durban (P. Moodley, K.M., T.M., P. Mpangase), and the South African Medical Research Council, Cape Town (N.M., T.K.) - all in South Africa; and the Public Health Research Institute, New Jersey Medical School-Rutgers University, Newark (E.S., B.K.).
  4. Barun Mathema: From the Emory University Rollins School of Public Health and School of Medicine (N.S.S., S.C.A., S.A., A.C., N.R.G.) and the Centers for Disease Control and Prevention (N.S.S.) - both in Atlanta; Albert Einstein College of Medicine and Montefiore Medical Center (N.S.S., J.C.M.B., N.R.G.), Columbia University Mailman School of Public Health (B.M., T.S.B.), and the American Museum of Natural History (A.N.) - all in New York; the National Institute for Communicable Diseases, Johannesburg (N.I., H.M., S.V.O.), University of KwaZulu-Natal and National Health Laboratory Service, Durban (P. Moodley, K.M., T.M., P. Mpangase), and the South African Medical Research Council, Cape Town (N.M., T.K.) - all in South Africa; and the Public Health Research Institute, New Jersey Medical School-Rutgers University, Newark (E.S., B.K.).
  5. Nazir Ismail: From the Emory University Rollins School of Public Health and School of Medicine (N.S.S., S.C.A., S.A., A.C., N.R.G.) and the Centers for Disease Control and Prevention (N.S.S.) - both in Atlanta; Albert Einstein College of Medicine and Montefiore Medical Center (N.S.S., J.C.M.B., N.R.G.), Columbia University Mailman School of Public Health (B.M., T.S.B.), and the American Museum of Natural History (A.N.) - all in New York; the National Institute for Communicable Diseases, Johannesburg (N.I., H.M., S.V.O.), University of KwaZulu-Natal and National Health Laboratory Service, Durban (P. Moodley, K.M., T.M., P. Mpangase), and the South African Medical Research Council, Cape Town (N.M., T.K.) - all in South Africa; and the Public Health Research Institute, New Jersey Medical School-Rutgers University, Newark (E.S., B.K.).
  6. Pravi Moodley: From the Emory University Rollins School of Public Health and School of Medicine (N.S.S., S.C.A., S.A., A.C., N.R.G.) and the Centers for Disease Control and Prevention (N.S.S.) - both in Atlanta; Albert Einstein College of Medicine and Montefiore Medical Center (N.S.S., J.C.M.B., N.R.G.), Columbia University Mailman School of Public Health (B.M., T.S.B.), and the American Museum of Natural History (A.N.) - all in New York; the National Institute for Communicable Diseases, Johannesburg (N.I., H.M., S.V.O.), University of KwaZulu-Natal and National Health Laboratory Service, Durban (P. Moodley, K.M., T.M., P. Mpangase), and the South African Medical Research Council, Cape Town (N.M., T.K.) - all in South Africa; and the Public Health Research Institute, New Jersey Medical School-Rutgers University, Newark (E.S., B.K.).
  7. Koleka Mlisana: From the Emory University Rollins School of Public Health and School of Medicine (N.S.S., S.C.A., S.A., A.C., N.R.G.) and the Centers for Disease Control and Prevention (N.S.S.) - both in Atlanta; Albert Einstein College of Medicine and Montefiore Medical Center (N.S.S., J.C.M.B., N.R.G.), Columbia University Mailman School of Public Health (B.M., T.S.B.), and the American Museum of Natural History (A.N.) - all in New York; the National Institute for Communicable Diseases, Johannesburg (N.I., H.M., S.V.O.), University of KwaZulu-Natal and National Health Laboratory Service, Durban (P. Moodley, K.M., T.M., P. Mpangase), and the South African Medical Research Council, Cape Town (N.M., T.K.) - all in South Africa; and the Public Health Research Institute, New Jersey Medical School-Rutgers University, Newark (E.S., B.K.).
  8. Salim Allana: From the Emory University Rollins School of Public Health and School of Medicine (N.S.S., S.C.A., S.A., A.C., N.R.G.) and the Centers for Disease Control and Prevention (N.S.S.) - both in Atlanta; Albert Einstein College of Medicine and Montefiore Medical Center (N.S.S., J.C.M.B., N.R.G.), Columbia University Mailman School of Public Health (B.M., T.S.B.), and the American Museum of Natural History (A.N.) - all in New York; the National Institute for Communicable Diseases, Johannesburg (N.I., H.M., S.V.O.), University of KwaZulu-Natal and National Health Laboratory Service, Durban (P. Moodley, K.M., T.M., P. Mpangase), and the South African Medical Research Council, Cape Town (N.M., T.K.) - all in South Africa; and the Public Health Research Institute, New Jersey Medical School-Rutgers University, Newark (E.S., B.K.).
  9. Angela Campbell: From the Emory University Rollins School of Public Health and School of Medicine (N.S.S., S.C.A., S.A., A.C., N.R.G.) and the Centers for Disease Control and Prevention (N.S.S.) - both in Atlanta; Albert Einstein College of Medicine and Montefiore Medical Center (N.S.S., J.C.M.B., N.R.G.), Columbia University Mailman School of Public Health (B.M., T.S.B.), and the American Museum of Natural History (A.N.) - all in New York; the National Institute for Communicable Diseases, Johannesburg (N.I., H.M., S.V.O.), University of KwaZulu-Natal and National Health Laboratory Service, Durban (P. Moodley, K.M., T.M., P. Mpangase), and the South African Medical Research Council, Cape Town (N.M., T.K.) - all in South Africa; and the Public Health Research Institute, New Jersey Medical School-Rutgers University, Newark (E.S., B.K.).
  10. Thuli Mthiyane: From the Emory University Rollins School of Public Health and School of Medicine (N.S.S., S.C.A., S.A., A.C., N.R.G.) and the Centers for Disease Control and Prevention (N.S.S.) - both in Atlanta; Albert Einstein College of Medicine and Montefiore Medical Center (N.S.S., J.C.M.B., N.R.G.), Columbia University Mailman School of Public Health (B.M., T.S.B.), and the American Museum of Natural History (A.N.) - all in New York; the National Institute for Communicable Diseases, Johannesburg (N.I., H.M., S.V.O.), University of KwaZulu-Natal and National Health Laboratory Service, Durban (P. Moodley, K.M., T.M., P. Mpangase), and the South African Medical Research Council, Cape Town (N.M., T.K.) - all in South Africa; and the Public Health Research Institute, New Jersey Medical School-Rutgers University, Newark (E.S., B.K.).
  11. Natashia Morris: From the Emory University Rollins School of Public Health and School of Medicine (N.S.S., S.C.A., S.A., A.C., N.R.G.) and the Centers for Disease Control and Prevention (N.S.S.) - both in Atlanta; Albert Einstein College of Medicine and Montefiore Medical Center (N.S.S., J.C.M.B., N.R.G.), Columbia University Mailman School of Public Health (B.M., T.S.B.), and the American Museum of Natural History (A.N.) - all in New York; the National Institute for Communicable Diseases, Johannesburg (N.I., H.M., S.V.O.), University of KwaZulu-Natal and National Health Laboratory Service, Durban (P. Moodley, K.M., T.M., P. Mpangase), and the South African Medical Research Council, Cape Town (N.M., T.K.) - all in South Africa; and the Public Health Research Institute, New Jersey Medical School-Rutgers University, Newark (E.S., B.K.).
  12. Primrose Mpangase: From the Emory University Rollins School of Public Health and School of Medicine (N.S.S., S.C.A., S.A., A.C., N.R.G.) and the Centers for Disease Control and Prevention (N.S.S.) - both in Atlanta; Albert Einstein College of Medicine and Montefiore Medical Center (N.S.S., J.C.M.B., N.R.G.), Columbia University Mailman School of Public Health (B.M., T.S.B.), and the American Museum of Natural History (A.N.) - all in New York; the National Institute for Communicable Diseases, Johannesburg (N.I., H.M., S.V.O.), University of KwaZulu-Natal and National Health Laboratory Service, Durban (P. Moodley, K.M., T.M., P. Mpangase), and the South African Medical Research Council, Cape Town (N.M., T.K.) - all in South Africa; and the Public Health Research Institute, New Jersey Medical School-Rutgers University, Newark (E.S., B.K.).
  13. Hermina van der Meulen: From the Emory University Rollins School of Public Health and School of Medicine (N.S.S., S.C.A., S.A., A.C., N.R.G.) and the Centers for Disease Control and Prevention (N.S.S.) - both in Atlanta; Albert Einstein College of Medicine and Montefiore Medical Center (N.S.S., J.C.M.B., N.R.G.), Columbia University Mailman School of Public Health (B.M., T.S.B.), and the American Museum of Natural History (A.N.) - all in New York; the National Institute for Communicable Diseases, Johannesburg (N.I., H.M., S.V.O.), University of KwaZulu-Natal and National Health Laboratory Service, Durban (P. Moodley, K.M., T.M., P. Mpangase), and the South African Medical Research Council, Cape Town (N.M., T.K.) - all in South Africa; and the Public Health Research Institute, New Jersey Medical School-Rutgers University, Newark (E.S., B.K.).
  14. Shaheed V Omar: From the Emory University Rollins School of Public Health and School of Medicine (N.S.S., S.C.A., S.A., A.C., N.R.G.) and the Centers for Disease Control and Prevention (N.S.S.) - both in Atlanta; Albert Einstein College of Medicine and Montefiore Medical Center (N.S.S., J.C.M.B., N.R.G.), Columbia University Mailman School of Public Health (B.M., T.S.B.), and the American Museum of Natural History (A.N.) - all in New York; the National Institute for Communicable Diseases, Johannesburg (N.I., H.M., S.V.O.), University of KwaZulu-Natal and National Health Laboratory Service, Durban (P. Moodley, K.M., T.M., P. Mpangase), and the South African Medical Research Council, Cape Town (N.M., T.K.) - all in South Africa; and the Public Health Research Institute, New Jersey Medical School-Rutgers University, Newark (E.S., B.K.).
  15. Tyler S Brown: From the Emory University Rollins School of Public Health and School of Medicine (N.S.S., S.C.A., S.A., A.C., N.R.G.) and the Centers for Disease Control and Prevention (N.S.S.) - both in Atlanta; Albert Einstein College of Medicine and Montefiore Medical Center (N.S.S., J.C.M.B., N.R.G.), Columbia University Mailman School of Public Health (B.M., T.S.B.), and the American Museum of Natural History (A.N.) - all in New York; the National Institute for Communicable Diseases, Johannesburg (N.I., H.M., S.V.O.), University of KwaZulu-Natal and National Health Laboratory Service, Durban (P. Moodley, K.M., T.M., P. Mpangase), and the South African Medical Research Council, Cape Town (N.M., T.K.) - all in South Africa; and the Public Health Research Institute, New Jersey Medical School-Rutgers University, Newark (E.S., B.K.).
  16. Apurva Narechania: From the Emory University Rollins School of Public Health and School of Medicine (N.S.S., S.C.A., S.A., A.C., N.R.G.) and the Centers for Disease Control and Prevention (N.S.S.) - both in Atlanta; Albert Einstein College of Medicine and Montefiore Medical Center (N.S.S., J.C.M.B., N.R.G.), Columbia University Mailman School of Public Health (B.M., T.S.B.), and the American Museum of Natural History (A.N.) - all in New York; the National Institute for Communicable Diseases, Johannesburg (N.I., H.M., S.V.O.), University of KwaZulu-Natal and National Health Laboratory Service, Durban (P. Moodley, K.M., T.M., P. Mpangase), and the South African Medical Research Council, Cape Town (N.M., T.K.) - all in South Africa; and the Public Health Research Institute, New Jersey Medical School-Rutgers University, Newark (E.S., B.K.).
  17. Elena Shaskina: From the Emory University Rollins School of Public Health and School of Medicine (N.S.S., S.C.A., S.A., A.C., N.R.G.) and the Centers for Disease Control and Prevention (N.S.S.) - both in Atlanta; Albert Einstein College of Medicine and Montefiore Medical Center (N.S.S., J.C.M.B., N.R.G.), Columbia University Mailman School of Public Health (B.M., T.S.B.), and the American Museum of Natural History (A.N.) - all in New York; the National Institute for Communicable Diseases, Johannesburg (N.I., H.M., S.V.O.), University of KwaZulu-Natal and National Health Laboratory Service, Durban (P. Moodley, K.M., T.M., P. Mpangase), and the South African Medical Research Council, Cape Town (N.M., T.K.) - all in South Africa; and the Public Health Research Institute, New Jersey Medical School-Rutgers University, Newark (E.S., B.K.).
  18. Thandi Kapwata: From the Emory University Rollins School of Public Health and School of Medicine (N.S.S., S.C.A., S.A., A.C., N.R.G.) and the Centers for Disease Control and Prevention (N.S.S.) - both in Atlanta; Albert Einstein College of Medicine and Montefiore Medical Center (N.S.S., J.C.M.B., N.R.G.), Columbia University Mailman School of Public Health (B.M., T.S.B.), and the American Museum of Natural History (A.N.) - all in New York; the National Institute for Communicable Diseases, Johannesburg (N.I., H.M., S.V.O.), University of KwaZulu-Natal and National Health Laboratory Service, Durban (P. Moodley, K.M., T.M., P. Mpangase), and the South African Medical Research Council, Cape Town (N.M., T.K.) - all in South Africa; and the Public Health Research Institute, New Jersey Medical School-Rutgers University, Newark (E.S., B.K.).
  19. Barry Kreiswirth: From the Emory University Rollins School of Public Health and School of Medicine (N.S.S., S.C.A., S.A., A.C., N.R.G.) and the Centers for Disease Control and Prevention (N.S.S.) - both in Atlanta; Albert Einstein College of Medicine and Montefiore Medical Center (N.S.S., J.C.M.B., N.R.G.), Columbia University Mailman School of Public Health (B.M., T.S.B.), and the American Museum of Natural History (A.N.) - all in New York; the National Institute for Communicable Diseases, Johannesburg (N.I., H.M., S.V.O.), University of KwaZulu-Natal and National Health Laboratory Service, Durban (P. Moodley, K.M., T.M., P. Mpangase), and the South African Medical Research Council, Cape Town (N.M., T.K.) - all in South Africa; and the Public Health Research Institute, New Jersey Medical School-Rutgers University, Newark (E.S., B.K.).
  20. Neel R Gandhi: From the Emory University Rollins School of Public Health and School of Medicine (N.S.S., S.C.A., S.A., A.C., N.R.G.) and the Centers for Disease Control and Prevention (N.S.S.) - both in Atlanta; Albert Einstein College of Medicine and Montefiore Medical Center (N.S.S., J.C.M.B., N.R.G.), Columbia University Mailman School of Public Health (B.M., T.S.B.), and the American Museum of Natural History (A.N.) - all in New York; the National Institute for Communicable Diseases, Johannesburg (N.I., H.M., S.V.O.), University of KwaZulu-Natal and National Health Laboratory Service, Durban (P. Moodley, K.M., T.M., P. Mpangase), and the South African Medical Research Council, Cape Town (N.M., T.K.) - all in South Africa; and the Public Health Research Institute, New Jersey Medical School-Rutgers University, Newark (E.S., B.K.).
PMID: 28099825 DOI: 10.1056/NEJMoa1604544

Abstract

BACKGROUND: Drug-resistant tuberculosis threatens recent gains in the treatment of tuberculosis and human immunodeficiency virus (HIV) infection worldwide. A widespread epidemic of extensively drug-resistant (XDR) tuberculosis is occurring in South Africa, where cases have increased substantially since 2002. The factors driving this rapid increase have not been fully elucidated, but such knowledge is needed to guide public health interventions.
METHODS: We conducted a prospective study involving 404 participants in KwaZulu-Natal Province, South Africa, with a diagnosis of XDR tuberculosis between 2011 and 2014. Interviews and medical-record reviews were used to elicit information on the participants' history of tuberculosis and HIV infection, hospitalizations, and social networks. Mycobacterium tuberculosis isolates underwent insertion sequence (IS)6110 restriction-fragment-length polymorphism analysis, targeted gene sequencing, and whole-genome sequencing. We used clinical and genotypic case definitions to calculate the proportion of cases of XDR tuberculosis that were due to inadequate treatment of multidrug-resistant (MDR) tuberculosis (i.e., acquired resistance) versus those that were due to transmission (i.e., transmitted resistance). We used social-network analysis to identify community and hospital locations of transmission.
RESULTS: Of the 404 participants, 311 (77%) had HIV infection; the median CD4+ count was 340 cells per cubic millimeter (interquartile range, 117 to 431). A total of 280 participants (69%) had never received treatment for MDR tuberculosis. Genotypic analysis in 386 participants revealed that 323 (84%) belonged to 1 of 31 clusters. Clusters ranged from 2 to 14 participants, except for 1 large cluster of 212 participants (55%) with a LAM4/KZN strain. Person-to-person or hospital-based epidemiologic links were identified in 123 of 404 participants (30%).
CONCLUSIONS: The majority of cases of XDR tuberculosis in KwaZulu-Natal, South Africa, an area with a high tuberculosis burden, were probably due to transmission rather than to inadequate treatment of MDR tuberculosis. These data suggest that control of the epidemic of drug-resistant tuberculosis requires an increased focus on interrupting transmission. (Funded by the National Institute of Allergy and Infectious Diseases and others.).

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Grants

  1. T32 HL116271/NHLBI NIH HHS
  2. P30 AI050409/NIAID NIH HHS
  3. P30 AI051519/NIAID NIH HHS
  4. R01 AI089349/NIAID NIH HHS
  5. K23 AI083088/NIAID NIH HHS
  6. UL1 TR000454/NCATS NIH HHS
  7. UL1 TR001073/NCATS NIH HHS
  8. R01 AI087465/NIAID NIH HHS
  9. K24 AI114444/NIAID NIH HHS

MeSH Term

AIDS-Related Opportunistic Infections
Adolescent
Adult
Antitubercular Agents
CD4 Lymphocyte Count
Child
Extensively Drug-Resistant Tuberculosis
Female
HIV Infections
Humans
Male
Middle Aged
Mycobacterium tuberculosis
Phylogeny
Polymorphism, Single Nucleotide
Prospective Studies
Social Support
South Africa
Tuberculosis, Multidrug-Resistant
Young Adult

Chemicals

Antitubercular Agents
Journal Article Research Support, N.I.H., Extramural
Article has an altmetric score of 632

Word Cloud

Created with Highcharts 10.0.0tuberculosisparticipantstreatmentXDRSouthAfricatransmissionHIVinfectioncases404usedanalysisdueMDRepidemicdrug-resistantincreasedKwaZulu-Natalsequencinginadequateieresistance1BACKGROUND:Drug-resistantthreatensrecentgainshumanimmunodeficiencyvirusworldwidewidespreadextensivelyoccurringsubstantiallysince2002factorsdrivingrapidincreasefullyelucidatedknowledgeneededguidepublichealthinterventionsMETHODS:conductedprospectivestudyinvolvingProvincediagnosis20112014Interviewsmedical-recordreviewselicitinformationparticipants'historyhospitalizationssocialnetworksMycobacteriumisolatesunderwentinsertionsequenceIS6110restriction-fragment-lengthpolymorphismtargetedgenewhole-genomeclinicalgenotypiccasedefinitionscalculateproportionmultidrug-resistantacquiredversustransmittedsocial-networkidentifycommunityhospitallocationsRESULTS:31177%medianCD4+count340cellspercubicmillimeterinterquartilerange117431total28069%neverreceivedGenotypic386revealed32384%belonged31clustersClustersranged214exceptlargecluster21255%LAM4/KZNstrainPerson-to-personhospital-basedepidemiologiclinksidentified12330%CONCLUSIONS:majorityareahighburdenprobablyratherdatasuggestcontrolrequiresfocusinterruptingFundedNationalInstituteAllergyInfectiousDiseasesothersTransmissionExtensivelyDrug-ResistantTuberculosis

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