Pulmonary immune responses to Mycobacterium tuberculosis in exposed individuals

PLoS One. 2017 Nov 10;12(11):e0187882. doi: 10.1371/journal.pone.0187882. eCollection 2017.

Abstract

Background: Blood based Interferon-(IFN)-γ release assays (IGRAs) have a poor predictive value for the development of tuberculosis. This study aimed to investigate the correlation between IGRAs and pulmonary immune responses in tuberculosis contacts in Germany.

Methods: IGRAs were performed on bronchoalveolar lavage (BAL) cells and peripheral blood from close healthy contacts of patients with culturally confirmed tuberculosis. Cellular BAL composition was determined by flow cytometry. BAL cells were co-cultured with three strains of Mycobacterium tuberculosis (Mtb) and Mtb derived antigens including Purified Protein Derivative (PPD), 6 kD Early Secretory Antigenic Target (ESAT-6) and 10 kD Culture Filtrate Protein (CFP-10). Levels of 29 cytokines and chemokines were analyzed in the supernatants by multiplex assay. Associations and effects were examined using linear mixed-effects models.

Results: There were wide variations of inter-individual cytokine levels in BAL cell culture supernatants. Mycobacterial infection and stimulation with PPD showed a clear induction of several macrophage and lymphocyte associated cytokines, reflecting activation of these cell types. No robust correlation between cytokine patterns and blood IGRA status of the donor was observed, except for slightly higher Interleukin-2 (IL-2) responses in BAL cells from IGRA-positive donors upon mycobacterial infection compared to cells from IGRA-negative donors. Stronger correlations were observed when cytokine patterns were stratified according to BAL IGRA status. BAL cells from donors with BAL IGRA-positive responses produced significantly more IFN-γ and IL-2 upon PPD stimulation and mycobacterial infection than cells from BAL IGRA-negative individuals. Correlations between BAL composition and basal cytokine release from unstimulated cells were suggestive of pre-activated lymphocytes but impaired macrophage activity in BAL IGRA-positive donors, in contrast to BAL IGRA-negative donors.

Conclusions: In vitro BAL cell cytokine responses to M. tuberculosis antigens or infection do not reflect blood IGRA status but do correlate with stronger cellular responses in BAL IGRA-positive donors. The cytokine patterns observed suggest a pre-activated state of lymphocytes and suppressed macrophage responsiveness in BAL cells from BAL IGRA-positive individuals.

MeSH terms

  • Bronchoalveolar Lavage Fluid
  • Germany
  • Humans
  • Lung / immunology*
  • Mycobacterium tuberculosis / immunology*

Grants and funding

This observational, multicentre, prospective study was carried out by the research consortium on “Pulmonary Tuberculosis – Host and Pathogen Determinants of Resistance and Disease Progression- (TB or not TB)”, funded by the German Ministry of Education and Research (BMBF, reference 01KI0784). The funder provided support in the form of salaries for one author [CH], but did not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. LvdM is the sole employee and owner of the statistics consulting company LizeStats Consulting. LizeStats Consulting provides a salary to LvdM, but did not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The specific roles of these authors are articulated in the ‘author contributions’ section.