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Urban airborne particle exposure impairs human lung and blood Mycobacterium tuberculosis immunity
  1. Martha Torres1,
  2. Claudia Carranza1,
  3. Srijata Sarkar2,
  4. Yolanda Gonzalez1,
  5. Alvaro Osornio Vargas3,
  6. Kathleen Black4,
  7. Qingyu Meng2,
  8. Raul Quintana-Belmares5,
  9. Martha Hernandez6,
  10. Jose Juan F Angeles Garcia6,
  11. Victor Hugo Páramo-Figueroa6,
  12. Marco Antonio Iñiguez-Garcia7,
  13. Jose L Flores8,
  14. Junfeng (Jim) Zhang9,
  15. Carol R Gardner10,
  16. Pamela Ohman-Strickland11,
  17. Stephan Schwander12
  1. 1 Department of Microbiology, Instituto Nacional de Enfermedades Respiratorias, Mexico City, Mexico
  2. 2 Environmental and Occupational Health, Rutgers School of Public Health New Brunswick Campus, Piscataway, New Jersey, USA
  3. 3 Paediatrics, University of Alberta, Edmonton, Alberta, Canada
  4. 4 Environmental and Occupational Health Sciences Institute, Rutgers, The State University of New Jersey, New Brunswick, New Jersey, USA
  5. 5 Investigacion basica, Instituto Nacional de Cancerologia, Mexico City, Mexico
  6. 6 Contaminacion y salud ambiental, Instituto Nacional de Ecologia y Cambio Climatico, Coyoacan, Mexico
  7. 7 Department of Thoracic Surgery, Instituto Nacional de Enfermedades Respiratorias, Mexico City, Mexico
  8. 8 Departamento de ciencias de la salud, Universidad Autonoma Metropolitana Iztapalapa, Iztapalapa, Mexico
  9. 9 Duke Global Health Institute and Nicholas School of the Environment, Duke University, Durham, North Carolina, USA
  10. 10 Ernest Mario School of Pharmacy, Rutgers University, Piscataway, New Jersey, USA
  11. 11 Biostatistics, Rutgers School of Public Health New Brunswick Campus, Piscataway, New Jersey, USA
  12. 12 Urban-Global Public Health and Environmental and Occupational Health, Rutgers School of Public Health New Brunswick Campus, Piscataway, New Jersey, USA
  1. Correspondence to Dr Stephan Schwander, Departments of Urban-Global Public Health and Environmental and Occupational Health, Rutgers School of Public Health, Newark Campus, Newark, NJ 07102, USA; schwansk{at}sph.rutgers.edu

Abstract

Rationale Associations between urban (outdoor) airborne particulate matter (PM) exposure and TB and potential biological mechanisms are poorly explored.

Objectives To examine whether in vivo exposure to urban outdoor PM in Mexico City and in vitro exposure to urban outdoor PM2.5 (< 2.5 µm median aerodynamic diameter) alters human host immune cell responses to Mycobacterium tuberculosis.

Methods Cellular toxicity (flow cytometry, proliferation assay (MTS assay)), M. tuberculosis and PM2.5 phagocytosis (microscopy), cytokine-producing cells (Enzyme-linked immune absorbent spot (ELISPOT)), and signalling pathway markers (western blot) were examined in bronchoalveolar cells (BAC) and peripheral blood mononuclear cells (PBMC) from healthy, non-smoking, residents of Mexico City (n=35; 13 female, 22 male). In vivo-acquired PM burden in alveolar macrophages (AM) was measured by digital image analysis.

Measurements and main results In vitro exposure of AM to PM2.5 did not affect M. tuberculosis phagocytosis. High in vivo-acquired AM PM burden reduced constitutive, M. tuberculosis and PM-induced interleukin-1β production in freshly isolated BAC but not in autologous PBMC while it reduced constitutive production of tumour necrosis factor-alpha in both BAC and PBMC. Further, PM burden was positively correlated with constitutive, PM, M. tuberculosis and purified protein derivative (PPD)-induced interferon gamma (IFN-γ) in BAC, and negatively correlated with PPD-induced IFN-γ in PBMC.

Conclusions Inhalation exposure to urban air pollution PM impairs important components of the protective human lung and systemic immune response against M. tuberculosis. PM load in AM is correlated with altered M. tuberculosis-induced cytokine production in the lung and systemic compartments. Chronic PM exposure with high constitutive expression of proinflammatory cytokines results in relative cellular unresponsiveness.

  • pollution
  • tuberculosis
  • alveolar macrophages
  • particulate matter
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Footnotes

  • Contributors StS conceived the design of the work, obtained funding, acquired, analysed and interpreted the data, and drafted the manuscript. RQB, SrS, CC and YG acquired, analysed and interpreted the data. MT and SrS analysed and interpreted the data and cowrote the manuscript. Other authors contributed to the study design (AOV, JZ), sample collection (RQB, MH, JJFAG), sample analysis, data analysis and/or discussion of the study results. All authors approved this manuscript and are accountable for accuracy and integrity of all parts of the work.

  • Funding NIEHS RO1 Grant R01ES020382 (S. Schwander) and NIH-NIEHS P30 ES005022.

  • Competing interests None declared.

  • Patient consent for publication Not required.

  • Ethics approval This research protocol was approved by the Scientific and Bioethics Committee of the Instituto Nacional de Enfermedades Respiratorias Ismael Cosío Villegas in Mexico City, Mexico (INER, protocol B22-12) and Rutgers University Institutional Review Board (protocol 2012001383) in New Brunswick, NJ.

  • Provenance and peer review Not commissioned; externally peer reviewed.

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