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Cited by 61Tuberculosis Research and EpidemiologyHIV, TB, and STIs EpidemiologyDiagnosis and treatment of tuberculosis

Disease Transmission by Patients With Subclinical Tuberculosis

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Nguyen, Hai Viet, Tiemersma, Edine, Nguyen, Nhung Viet, Nguyen, Hoa Binh, Cobelens, Frank·2023·Clinical Infectious Diseases
DOI 10.1093/cid/ciad027PMC PMC10249982
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Abstract

Background: Subclinical tuberculosis has been increasingly recognized as a separate state in the spectrum of the disease. However, evidence on the transmissibility of subclinical tuberculosis is still inconclusive. Methods: We re-analyzed the data from the 2007 combined tuberculosis prevalence and tuberculin surveys in Vietnam. Poisson regression with robust standard errors was conducted to assess the effect of clinical presentation of individuals with tuberculosis in the household on tuberculin skin test (TST) positivity among children aged 6–14 years who participated in the tuberculin survey, adjusting for child's age, smear status of the index patient, and other covariates. Results: In the multivariate analysis, we found significantly increased risks for TST positivity in children living with patients with clinical, smear-positive tuberculosis, compared with those living with individuals without tuberculosis (adjusted risk ratio [aRR]: 3.04; 95% confidence interval [CI]: 2.00–4.63) and with those living with patients with subclinical tuberculosis, adjusting for index smear status (aRR: 2.26; 95% CI: 1.03–4.96). Among children aged 6–10 years, those living with patients with clinical, smear-positive tuberculosis and those living with patients with subclinical, smear-positive tuberculosis had similarly increased risks of TST positivity compared with those living with individuals without tuberculosis (aRRs [95% CI] of 3.56 [1.91–6.62] and 3.11 [1.44–6.72], respectively). Conclusions: Our findings support the hypothesis that smear-positive subclinical tuberculosis contributes to Mycobacterium tuberculosis transmission. To eliminate tuberculosis in 2035, control strategies need to address subclinical presentations of the disease.

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  1. [1]World Health Organization. Global tuberculosis report 2021. Geneva, Switzerland: WHO Press, 2022.
  2. [2]Glynn JR, Guerra-Assunção JA, Houben RM, et al Whole genome sequencing shows a low proportion of tuberculosis disease is attributable to known close contacts in rural Malawi. PLoS One 2015; 10: e0132840. PMC4504505 26181760
  3. [3]McCreesh N, White RG. An explanation for the low proportion of tuberculosis that results from transmission between household and known social contacts. Sci Rep 2018; 8: 5382. 29599463 PMC5876383
  4. [4]Drain PK, Bajema KL, Dowdy D, et al Incipient and subclinical tuberculosis: a clinical review of early stages and progression of infection. Clin Microbiol Rev 2018; 31: e00021-18. PMC6148193 30021818
  5. [6]Richards AS, Sossen B, Emery JC, et al The natural history of TB disease—a synthesis of data to quantify progression and regression across the spectrum. medRxiv 2022 [ Preprint]. Available from: 10.1101/2021.09.13.21263499. · DOI
  6. [7]World Health Organization. WHO guidelines approved by the guidelines review committee. Systematic screening for active tuberculosis: principles and recommendations. Geneva, Switzerland: World Health Organization, 2013. 25996015
  7. [8]Stuck L, van Haaster AC, Kapata-Chanda P, Klinkenberg E, Kapata N, Cobelens F. How “subclinical” is subclinical tuberculosis? An analysis of national prevalence survey data from Zambia. Clin Infect Dis 2022; 75: 842– 8. 34984431 PMC9477454
  8. [9]Wurie FB, Lawn SD, Booth H, Sonnenberg P, Hayward AC. Bioaerosol production by patients with tuberculosis during normal tidal breathing: implications for transmission risk. Thorax 2016; 71: 549– 54. 26917579
  9. [10]Williams CM, Abdulwhhab M, Birring SS, et al Exhaled Mycobacterium tuberculosis output and detection of subclinical disease by face-mask sampling: prospective observational studies. Lancet Infect Dis 2020; 20: 607– 17. 32085847 PMC7191268
  10. [11]Esmail H, Dodd PJ, Houben R. Tuberculosis transmission during the subclinical period: could unrelated cough play a part? Lancet Respir Med 2018; 6: 244– 6. 29595504
  11. [12]Hoa NB, Sy DN, Nhung NV, Tiemersma EW, Borgdorff MW, Cobelens FGJ. National survey of tuberculosis prevalence in Viet Nam. Bull World Health Organ 2010; 88: 273– 80. 20431791 PMC2855599
  12. [14]Hoa NB, Cobelens FG, Sy DN, Nhung NV, Borgdorff MW, Tiemersma EW. First national tuberculin survey in Viet Nam: characteristics and association with tuberculosis prevalence. Int J Tuberc Lung Dis 2013; 17: 738– 44. 23676155
  13. [15]Nguyen HT, Bui DD, Nguyen CV, et al Tuberculosis epidemiology in six provinces of Vietnam after the introduction of the DOTS strategy. Int J Tuberc Lung Dis 2006; 10: 963– 9. 16964785
  14. [16]Tran BN, Quy HT, Qui NC, Nguyen LT, Dinh SN, Cobelens F. Decrease in risk of tuberculosis infection despite increase in tuberculosis among young adults in urban Vietnam. Int J Tuberc Lung Dis 2010; 14: 289– 95. 20132619
  15. [17]Nguyen HB, Tiemersma EW, Dinh SN, et al Household expenditure and tuberculosis prevalence in VietNam: prediction by a set of household indicators. Int J Tuberc Lung Dis 2011; 15: 32– 7. 21276293
  16. [19]Knol MJ, Le Cessie S, Algra A, Vandenbroucke JP, Groenwold RH. Overestimation of risk ratios by odds ratios in trials and cohort studies: alternatives to logistic regression. CMAJ 2012; 184: 895– 9. 22158397 PMC3348192
  17. [20]Asadi L, Croxen M, Heffernan C, et al How much do smear-negative patients really contribute to tuberculosis transmissions? Re-examining an old question with new tools. EClinicalMedicine 2022; 43: 101250. PMC8743225 35036885
  18. [21]Tostmann A, Kik SV, Kalisvaart NA, et al Tuberculosis transmission by patients with smear-negative pulmonary tuberculosis in a large cohort in the Netherlands. Clin Infect Dis 2008; 47: 1135– 42. 18823268
  19. [22]Ku C, Dodd PJ. Forecasting the impact of population ageing on tuberculosis incidence. PLoS One 2019; 14: e0222937. PMC6759178 31550293
  20. [23]Kendall EA. When infections don't reflect infectiousness: interpreting contact investigation data with care. Clin Infect Dis 2021; 73: e3456-e8. PMC7454347 32770232
  21. [24]Horby P, Pham QT, Hens N, et al Social contact patterns in Vietnam and implications for the control of infectious diseases. PLoS One 2011; 6: e16965. PMC3038933 21347264
  22. [25]Berkel GM, Cobelens FG, de Vries G, Draayer-Jansen IW, Borgdorff MW. Tuberculin skin test: estimation of positive and negative predictive values from routine data. Int J Tuberc Lung Dis 2005; 9: 310– 6. 15786896
  23. [26]Hernández-Garduño E, Cook V, Kunimoto D, Elwood RK, Black WA, FitzGerald JM. Transmission of tuberculosis from smear negative patients: a molecular epidemiology study. Thorax 2004; 59: 286– 90. 15047946 PMC1763818
  24. [27]Jones-López EC, Acuña-Villaorduña C, Ssebidandi M, et al Cough aerosols of Mycobacterium tuberculosis in the prediction of incident tuberculosis disease in household contacts. Clin Infect Dis 2016; 63: 10– 20. 27025837 PMC5006106
  25. [28]Patterson B, Wood R. Is cough really necessary for TB transmission? Tuberculosis (Edinburgh, Scotland) 2019; 117: 31– 5. 31378265 PMC6688829
  26. [29]Asadi S, Wexler AS, Cappa CD, Barreda S, Bouvier NM, Ristenpart WD. Aerosol emission and superemission during human speech increase with voice loudness. Sci Rep 2019; 9: 2348. 30787335 PMC6382806
  27. [30]Yousaf N, Monteiro W, Matos S, Birring SS, Pavord ID. Cough frequency in health and disease. Eur Respir J 2013; 41: 241– 3. 23277523
  28. [31]Field SK, Escalante P, Fisher DA, Ireland B, Irwin RS. Cough due to TB and other chronic infections: cHEST guideline and expert panel report. Chest 2018; 153: 467– 97. 29196066 PMC6689101
  29. [32]Emery JC, Dodd PJ, Banu S, et al Estimating the contribution of subclinical tuberculosis disease to transmission—an individual patient data analysis from prevalence surveys. medRxiv 2022 [ Preprint]. Available from: 10.1101/2022.06.09.22276188. PMC10727500 38109277 · DOI

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Authors
Nguyen, H. V., Tiemersma, E., Nguyen, N. V., Nguyen, H. B., & Cobelens, F.
Affiliations
  • Amsterdam Institute for Global Health and Development (NL)
  • KNCV TB Plus (NL)
  • Vietnam National Tuberculosis Program , Ha Noi , Vietnam
Corresponding author
Nguyen, Hai Viet
ORCID
Venue
Clinical Infectious Diseases
Publisher
Oxford University Press (OUP)
Published
2023-01-20
Volume
76
Issue
11
Pages
2000-2006
ISSN
  • 1058-4838 (ISSN-L)
  • 1537-6591
DOI
10.1093/cid/ciad027
PMC
PMC10249982
OpenAlex
W4317567508
Cited by
61
References
3
Citations by year
2026: 13 · 2025: 19 · 2024: 22 · 2023: 7
FWCI
12.63
Type
journal article
Language
en
Open access
Licence
Locations
  • Clinical Infectious Diseases (publishedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • Pure Amsterdam UMC (acceptedVersion, cc-by)
Topics
  • Health Sciences › Medicine › Infectious Diseases › Tuberculosis Research and Epidemiology
  • Social Sciences › General Social Sciences › HIV, TB, and STIs Epidemiology
  • Health Sciences › Medicine › Surgery › Diagnosis and treatment of tuberculosis
Keywords
subclinical tuberculosis, tuberculosis transmission, household transmission, smear-positive tuberculosis, children, Mycobacterium tuberculosis, tuberculosis control, Vietnam
MeSH terms
Child, Humans, Mycobacterium tuberculosis, Surveys and Questionnaires, Risk Factors, Tuberculin, Tuberculin Test, Tuberculosis, Tuberculosis, Pulmonary

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