Tuberculosis in children: gaps and opportunities

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1 Tuberculosis in children: gaps and opportunities Mark Nicol Division of Medical Microbiology and Institute for Infectious Diseases and Molecular Medicine, University of Cape Town and National Health Laboratory Service, South Africa Acknowledgement: Co-PIs on RePORT TB CHILD: Heather Zar, Jeff Starke REPORT-TB International Meeting 15 July 2016

2 Disclosures Mark Nicol has received research grants awarded to his institution from FIND, EDCTP, Wellcome Trust, BMGF and NIH, to conduct studies evaluating Xpert MTB/RIF, Ultra, LAM and other diagnostics in children.

3 Topics Natural history of infection Epidemiology Diagnostics Treatment

4 Why is TB in children important? Neglected Considered less important since non-infectious No global targets for disease reduction 6-10% of global TB burden Sentinel event: Reflects transmission from active (adult) source case Reflects failure of preventive health care Associated with high morbidity Disseminated or EPTB Rapid progression and death

5 Risk of disease following primary infection is highly age-dependent Proportion Adult-type Effusion Bronchial Ghon focus, LN TBM/miliary disease Pulmonary disease No disease <1 year 1-2 years 2-5 years 5-10 years >10 years Age at primary infection Adapted from Marais BJ, Int J Tub Lung Dis 2004

6 Research questions What is the underlying immunological basis for the striking age-related susceptibility (and resistance) to TB in children? Can we learn generic lessons from this relating to susceptibility/immunity to TB?

7 Estimates of global burden of disease are wide-ranging 200,000 new cases in 2013 Murray CJ, Lancet ,000 new cases in 2010 Dodd PJ, Lancet Global Health ,000 new cases in 2010 Jenkins HE, Lancet 2014

8 Violin plot comparing model estimates of TB cases in children to WHO reported cases (0-5 years of age) Dodd PJ, Lancet Global Health 2014

9 Research questions Why the differences between countries in expected vs. reported TB in children : Are the differences due, in part, to different application/interpretation of diagnostic criteria? Does the spectrum of illness diagnosed as TB differ from country to country (clinical, radiological)? Can we learn from these differences? What happens to children who would meet diagnostic criteria (and start treatment) in one country (e.g., South Africa) but not in other countries (e.g,. India)?

10 TB infection in children Children <5 years Children 5-15 years Sharing a household with a TB patient in 2010 Infected with M. tuberculosis in 2010 Infected with M. tuberculosis by end of million 9.7 million 2.6 million 4.9 million 6.5 million 46.9 million Developing TB in , ,000 India accounts for 27% of total burden Enormous opportunity for preventive action Dodd PJ, Lancet Global Health 2014

11 Research questions Optimal (cost-effective) strategy for contact tracing and diagnosis/prevention in different epidemiological settings Tools for prediction of children at highest risk of progression (or of adults most likely to transmit)

12 Diagnostics for childhood tuberculosis: fumbling in the dark Quandaries in diagnosing TB in children Based on clinical diagnosis, we think that culture is a poor reference standard (20-50%) microscopy is infrequently helpful (<10%) However, clinical diagnosis is unreliable chest radiography interpretation is variable clinical scoring systems seldom concur Problem for diagnosis, epidemiology, evaluation of new diagnostics and for vaccine trials

13 Interpretation of CXR is highly inconsistent Hatherill M et al. Bull World Health Organ 2010;88:

14 What do we need from a diagnostic test for children? Asymptomatic children <2 years, >10 years, or HIV-infected exposed to infectious case Symptomatic children of any age

15 What do we need from a diagnostic test for children? Asymptomatic children <2 years, >10 years, or HIV-infected exposed to infectious case Symptomatic children of any age Test for infection Predict progression High sensitivity/fair specificity Low-cost, POC Preventive therapy

16 What do we need from a diagnostic test for children? Asymptomatic children <2 years, >10 years, or HIV-infected exposed to infectious case Symptomatic children of any age Test for disease Very high sensitivity and? specificity Low-cost, POC (MDR-screen) TB Diagnosis Drug-sensitive MDR/RR TB Rapid screen for SLD resistance Detailed resistance testing for pre/xdr Treatment monitoring

17 What do we need from a diagnostic test for children? Asymptomatic children <2 years, >10 years, or HIV-infected exposed to infectious case Symptomatic children of any age Specimen collection Test for disease Very high sensitivity and? specificity Low-cost, POC (MDR-screen)

18 Appropriate specimens for diagnosis of PTB in children Sputum: expectorated/induced IS has better yield than GLA (except in mild illness) Single visit, primary care, safe (Zar HJ, Lancet 2005, Moore HA Int J TBLD 2011) GL/A Need for standardization/optimization Requires hospitalization in most cases NPA Simple to collect, lower yield (Zar HJ, Clin Infect Dis 2012) Oral swabs Stool String test Older children (Chow F. BMC ID 2006) No longer commercially available BAL No better than GL (Bell DJ Int J TBLD 2009)

19 Conventional microbiological testing is a poor reference standard Smear has very low yield 22% GL, 29% ES/IS (vs. culture reference std) Culture Cross-contamination a problem LJ<MODS<MGIT (Tran ST, PLoS ONE 2013) Paediatric-specific protocols Whitelaw A, IUATLD 2010

20 Xpert MTB/RIF: WHO recommendations Xpert should be used rather than conventional microscopy, culture and DST as the initial diagnostic test in children suspected of having MDR-TB or HIV-associated TB (strong recommendation, very low-quality evidence). as the initial diagnostic test in all children suspected of having TB (conditional recommendation acknowledging resource implications, very lowquality evidence). WHO Policy Update 2013 WHO/HTM/TB/

21 Xpert MTB/RIF accuracy for respiratory samples Pooled sensitivity for both ES/IS and GLA were 66% (single Xpert) vs. 88% adults Range in sensitivity may relate to # of comparator cultures (need for standardization) Very low sensitivity (4-15%) against clinical diagnosis in culture-negative cases WHO Policy Update 2013 WHO/HTM/TB/

22 When does Xpert assist in diagnosis? Amongst every 100 children with microbiologically proven TB in our Cape Town studies (2 x liquid culture, Xpert) X+C- X+C+ X-C

23 When does Xpert assist in diagnosis? When empiric TB treatment is common, Xpert may be less useful X+C- X+C X-C+ Empiric treatment 180

24 When does Xpert assist in diagnosis? but the use of empiric treatment is likely to vary substantially between settings X+C- X+C X-C+ Empiric treatment x

25 Xpert Ultra Additional multi-copy targets for increased sensitivity Substantially reduced limit of detection (5 cfu/ml) Equivalent to culture? Adult evaluation underway RePORT TB study (Nicol, Zar, Starke) to evaluate accuracy in children Need to evaluate with different specimen types

26 Novel diagnostics: Host biomarkers for TB Host transcriptomic signature in blood from children Discovery cohort (SA and Malawi, n=1356), validation cohort (Kenya, n=1599) 51 transcripts distinguished TB from other diseases Minimal transcript set used to generate a risk score Discovery cohort: sensitivity of 78% and specificity of 74% Validation cohort: sensitivity 83%, specificity 84% 42 transcripts distinguished TB from LTBI Sensitivity of 96% and specificity of 91% Anderson et al. NEJM 2014

27 Novel diagnostics: Host biomarkers for TB Gradient in performance of risk score Anderson et al. NEJM 2014

28 Novel diagnostics: Host biomarkers for TB TAM-TB : Detects activated TB-specific T cells by flow cytometry Portevin Lancet Infect Dis 2014

29 Research questions Advantage of collaboration: sample size, generalizability How to best use existing diagnostic tools? What specimens/combination of specimens How many specimens Optimization of specimen processing for paediatric specimens Evaluation of novel biomarkers How to deal with absence of a gold standard Differing standards of diagnosis and treatment in different countries may offer interesting opportunities

30 Role of other pathogens in pathogenesis of TB unpublished

31 Treatment considerations Wide spectrum of disease; more EPTB, severe and disseminated TB (TBM and miliary TB) Paucibacillary disease compared to adult pulmonary TB (fewer lung cavities) Treatment outcome in children generally very good provided initiated early Bacillary load and type of TB may influence effectiveness of regimens shorter regimens for children? Acknowledgement to Anneke Hesseling

32 Pharmacokinetics and dosing of first line drugs in children Limited evidence, esp. <2 years Rapid changes in PK parameters in early life Use same target concentrations as for adult TB Differences from adults Children achieve lower serum concentrations of drugs at the same mg/kg dose Children eliminate drugs faster than adults Recently revised WHO dosing guidelines

33 MDR-TB treatment

34 MDR-TB: adverse events (n = 137) Grade of AE Gr 0 Gr 1 Gr 2 Gr 3-4 Any AE (%) Joint, muscle or bone pain (1.5) 15 (10.9) Skin rashes (0.7) 33 (24.1) Itchy skin (0.7) 27 (19.7) Headache (12.4) Sleep/mood problem (0.7) 13 (9.5) Lethargy (0.7) 19 (13.9) Visual problem (3.6) Vomiting (0.7) 24 (17.5) Diarrhoea (0.7) 12 (8.8) Jaundice (0.7) 4 (2.9) Appetite/nausea (0.7) 18 (13.1) Hearing loss (n=142) 25 (17.6) Thyroxine supplementation (n=142; TSH & ft4) Seddon, Clin Infect Dis (22.5) Slide courtesy of Anneke Hesseling

35 MDR-TB treatment outcomes Outcome N = 149 (%) Cure 36 (24.2) Probable cure * 101 (67.8) Transferred out 1 (0.7) Lost to follow up 8 (5.4) Died 3 (2.0) Seddon Thorax 2013 Given good outcome, lower bacillary load, toxicities:? injectable sparing, less toxic, shorter regimen Acknowledgement: Anneke Hesseling

36 MDR-TB prevention: No WHO-recommended regimen given absence of trial data

37 Research questions PK/PD studies Short course treatment for MDR Preventive regimens for MDR contacts

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