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      A Century of Tuberculosis Epidemiology in the Northern and Southern Hemisphere: The Differential Impact of Control Interventions

      research-article
      1 , 2 , 3 , * , 4 , 1 , 5 , 6
      PLoS ONE
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          Abstract

          Background

          Cape Town has one of the highest TB burdens of any city in the world. In 1900 the City of Cape Town, New York City and London had high mortality of tuberculosis (TB). Throughout the 20th century contemporaneous public health measures including screening, diagnosis and treatment were implemented in all three settings. Mandatory notification of TB and vital status enabled comparison of disease burden trajectories.

          Methods

          TB mortality, notification and case fatality rates were calculated from 1912 to 2012 using annual TB notifications, TB death certifications and population estimates. Notification rates were stratified by age and in Cape Town by HIV status (from 2009 onwards).

          Results

          Pre-chemotherapy, TB mortality and notification rates declined steadily in New York and London but remained high in Cape Town. Following introduction of combination chemotherapy, mean annual case fatality dropped from 45–60% to below 10% in all three settings. Mortality and notification rates subsequently declined, although Cape Town notifications did not decline as far as those in New York or London and returned to pre-chemotherapy levels by 1980. The proportional contribution of childhood TB diminished in New York and London but remained high in Cape Town. The advent of the Cape Town HIV-epidemic in the 1990s was associated with a further two-fold increase in incidence. In 2012, notification rates among HIV-negatives remained at pre-chemotherapy levels.

          Conclusions

          TB control was achieved in New York and London but failed in Cape Town. The TB disease burden trajectories started diverging before the availability of combination chemotherapy in 1952 and further diverged following the HIV epidemic in 1990. Chemotherapy impacted case fatality but not transmission, evidenced by on-going high childhood TB rates. Currently endemic TB results from high on-going transmission, which has been exacerbated by the HIV epidemic. TB control will require reducing transmission, which is inexorably linked to prevailing socio-economic factors.

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          Most cited references16

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          The population dynamics and control of tuberculosis.

          More than 36 million patients have been successfully treated via the World Health Organization's strategy for tuberculosis (TB) control since 1995. Despite predictions of a decline in global incidence, the number of new cases continues to grow, approaching 10 million in 2010. Here we review the changing relationship between the causative agent, Mycobacterium tuberculosis, and its human host and examine a range of factors that could explain the persistence of TB. Although there are ways to reduce susceptibility to infection and disease, and a high-efficacy vaccine would boost TB prevention, early diagnosis and drug treatment to interrupt transmission remain the top priorities for control. Whatever the technology used, success depends critically on the social, institutional, and epidemiological context in which it is applied.
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            Studies on the treatment of tuberculosis undertaken by the British Medical Research Council tuberculosis units, 1946-1986, with relevant subsequent publications.

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              Changing prevalence of tuberculosis infection with increasing age in high-burden townships in South Africa.

              Crowded townships of Cape Town, South Africa, where human immunodeficiency virus (HIV) prevalence and tuberculosis (TB) notification rates are among the highest in the world. To determine age-specific prevalence rates of latent tuberculosis infection (LTBI) among HIV-negative individuals, and the annual risk and force of infection during childhood and adolescence. A cross-sectional survey using a standardised tuberculin skin test (TST) in HIV-negative individuals aged 5-40 years. A TST diameter of > or =10 mm was defined as indicative of LTBI. Among 1061 individuals, only 4.7% had low-grade TST responses of 1-9 mm. However, the proportions of individuals with TST > or =10 mm increased from 28.0% in the 5-10 year age stratum to 88.0% in the 31-35 year age stratum. The mean annual risk of infection was 3.9% up to 5 years of age. The estimated force of infection (the rate of acquisition of LTBI among the residual pool of non-infected individuals) increased throughout childhood to a maximum of 7.9% per year at age 15 years. Extremely high rates of infection in childhood and adolescence result in very high LTBI prevalence rates in young adults who are most at risk of acquiring HIV infection. This may be an important factor fuelling the high rates of HIV-associated TB in southern Africa.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                19 August 2015
                2015
                : 10
                : 8
                : e0135179
                Affiliations
                [1 ]Desmond Tutu HIV Centre, Institute of Infectious Disease and Molecular Medicine, University of Cape Town, Cape Town, South Africa
                [2 ]Department of Global Health, Academic Medical Center, University of Amsterdam, Amsterdam Institute for Global Health and Development, Amsterdam, the Netherlands
                [3 ]Department of Internal Medicine, School of Medicine, Makerere University College of Health Sciences, Kampala, Uganda
                [4 ]Department of Epidemiology, Boston University School of Public Health, Boston, Massachusetts, United States of America
                [5 ]Department of Medicine, University of Cape Town, Cape Town, South Africa
                [6 ]Department of Clinical Research, Faculty of Infectious & Tropical Diseases, London School of Hygiene & Tropical Medicine, London, United Kingdom
                University of Cape Town, SOUTH AFRICA
                Author notes

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

                Conceived and designed the experiments: SH RW. Performed the experiments: SH RW. Analyzed the data: SH RW. Contributed reagents/materials/analysis tools: SH RW. Wrote the paper: SH CRH RW.

                Article
                PONE-D-15-17528
                10.1371/journal.pone.0135179
                4545605
                26288079
                c1c81381-36e3-46b6-a16c-3bca04bfc558

                This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication

                History
                : 22 April 2015
                : 17 July 2015
                Page count
                Figures: 4, Tables: 1, Pages: 13
                Funding
                This work was supported by the European Union [Marie Curie International Outgoing Fellowship for Career Development PIOF-GA-2012-332311 to SH], the Swiss National Science Foundation [PBSKP3_145774 to SH], the National Institutes of Health [R01AI058736-02, R01AI093269-02, U01AI069924-02 and U01A1069519 to RW, U01AI100805 to CRH], and the South African Medical Research Council [MRC-RFA-UFSP-01-2013/CCAMP to RW]. The funding bodies had no role in study design, data analysis, or write-up.
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