Translocation of black carbon particles to human intestinal tissue

Abstract

Background: Evidence is accumulating that elevated levels of particulate air pollution, including black carbon, have been linked to gastrointestinal disorders and a lower intestinal bacterial richness and diversity. One of the hypothesized underlying mechanisms is the absorption of air pollution-related particles from the gastrointestinal tract.

Methods: We visualized and quantified black carbon particles via white light generation under femtosecond-pulsed laser illumination in ileum and colon biopsies of five human patients. The biodistribution was assessed in three different layers (i.e., mucosa, submucosa, and muscularis propria).

Findings: Black carbon particles could be identified in all three tissue layers of the ileum and colon biopsies of five participants (two men and three women; mean ± standard deviation age, 76.40 ± 7.37 years), and their carbonaceous nature was confirmed via emission fingerprinting. The median (±SD) black carbon load was borderline statistically significantly higher in the ileum compared to the colon (1.21 × 10⁵ ± 1.68 × 10⁴ particles/mm³ versus 9.34 × 10⁴ ± 1.33 × 10⁴ particles/mm³; p = 0.07) and was driven by a difference in black carbon load in the submucosa layer (p = 0.01). Regarding the three tissue layers, loads were higher in the submucosa, compared with the mucosa (ileum: +76%, p < 0.0001; colon: +70%, p = 0.0001) and muscularis propria (ileum: +88%, p < 0.0001; colon: +88%, p < 0.0001). In ileum, loads were borderline higher in the mucosa versus muscularis propria (p = 0.09).

Interpretation: This explorative study provides real-life evidence that black carbon particles can reach the intestinal tissue and accumulate in different intestinal tissue layers. These findings support further research into how particulate air pollution directly affects gastrointestinal health.

Funding: Thessa Van Pee holds a doctoral fellowship from the Research Foundation Flanders (FWO), grant number: 11C7421N. Tim Nawrot is a Methusalem grant holder.

Keywords: Black carbon; Colon; Ileum; Translocation.

Fig. 1

Histology of the intestine. Representative images of (A) all intestinal layers and a detail of the (B) mucosa, (C) submucosa, and (D) muscularis propria. Paraffin-embedded 5 μm sections were stained with hematoxylin and eosin and imaged at × 2.5 and × 10 magnifications.

Fig. 2

Evidence of black carbon particles in different intestinal regions: (A) mucosa, (B) submucosa, and (C) muscularis propria. White light generation originating from black carbon particles (white, indicated with a white arrow) under femtosecond pulsed laser illumination (excitation 810 nm) was observed. Images represent the overlap of the two-photon autofluorescence of the tissue (green, emission 450–650 nm) and second harmonic generation of collagen (red, emission 400–410 nm). Scale bar: 10 μm.

Fig. 3

Boxplot representing the (A) average number of black carbon particles per mm³ ileum or colon tissue, or (B) the average number of black carbon particles per mm³ stratified per tissue layer: mucosa, submucosa, and muscularis propria. Violin boxes span from the lowest to the highest value, with the horizontal line inside the box representing the median value. n = 5. ∗indicates p-value ≤0.05 and indicates p-value ≤0.10.