Experimental Acute Exposure to Thirdhand Smoke and Changes in the Human Nasal Epithelial Transcriptome: A Randomized Clinical Trial

JAMA Netw Open. 2019 Jun 5;2(6):e196362. doi: 10.1001/jamanetworkopen.2019.6362.

Abstract

Importance: No previous studies have shown that acute inhalation of thirdhand smoke (THS) activates stress and survival pathways in the human nasal epithelium.

Objective: To evaluate gene expression in the nasal epithelium of nonsmoking women following acute inhalation of clean air and THS.

Design, setting, and participants: Nasal epithelium samples were obtained from participants in a randomized clinical trial (2011-2015) on the health effects of inhaled THS. In a crossover design, participants were exposed, head only, to THS and to conditioned, filtered air in a laboratory setting. The order of exposures was randomized and exposures were separated by at least 21 days. Ribonucleic acid was obtained from a subset of 4 healthy, nonsmoking women.

Exposures: By chance, women in the subset were randomized to receive clean air exposure first and THS exposure second. Exposures lasted 3 hours.

Main outcomes and measures: Differentially expressed genes were identified using RNA sequencing with a false-discovery rate less than 0.1.

Results: Participants were 4 healthy, nonsmoking women aged 27 to 49 years (mean [SD] age, 42 [10.2] years) with no chronic diseases. A total of 389 differentially expressed genes were identified in nasal epithelium exposed to THS, while only 2 genes, which were not studied further, were affected by clean air. Enriched gene ontology terms associated with stress-induced mitochondrial hyperfusion were identified, such as respiratory electron transport chain (q = 2.84 × 10-3) and mitochondrial inner membrane (q = 7.21 × 10-6). Reactome pathway analysis identified terms associated with upregulation of DNA repair mechanisms, such as nucleotide excision repair (q = 1.05 × 10-2). Enrichment analyses using ingenuity pathway analysis identified canonical pathways related to stress-induced mitochondrial hyperfusion (eg, increased oxidative phosphorylation) (P = .001), oxidative stress (eg, glutathione depletion phase II reactions) (P = .04), and cell survival (z score = 5.026).

Conclusions and relevance: This study found that acute inhalation of THS caused cell stress that led to the activation of survival pathways. Some responses were consistent with stress-induced mitochondrial hyperfusion and similar to those demonstrated previously in vitro. These data may be valuable to physicians treating patients exposed to THS and may aid in formulating regulations for the remediation of THS-contaminated environments.

Publication types

  • Randomized Controlled Trial
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Adult
  • Air Pollutants / adverse effects*
  • Cell Death / physiology
  • Cell Survival / physiology
  • Cross-Over Studies
  • DNA Repair / physiology
  • Environmental Exposure / adverse effects
  • Female
  • Gene Expression / physiology
  • Healthy Volunteers
  • Humans
  • Middle Aged
  • Nasal Mucosa / physiology*
  • Smoke / adverse effects*
  • Stress, Physiological / physiology
  • Tobacco Smoke Pollution / adverse effects
  • Transcriptome / physiology*

Substances

  • Air Pollutants
  • Smoke
  • Tobacco Smoke Pollution