, Volume 34, Issue 4, pp 487–496 | Cite as

The abundance of urban endotoxins as measured with an impinger-based sampling strategy

  • Serena Moretti
  • Wenke Smets
  • Eline Oerlemans
  • Ronny Blust
  • Sarah LebeerEmail author
Original Paper


Endotoxins are components of Gram-negative bacteria with inherently high pro-inflammatory potential. In an urban environment, airborne endotoxins may associate with pollutants such as particulate matter, increasing the severity of the immune response by acting as a natural adjuvant to augment inflammatory respiratory disease development. Here, we present a closer look at outdoor urban endotoxins by applying a microbial-targeted collection strategy. Results from 87 samples distributed throughout the city of Antwerp ranged from 0.45 to 93.71 EU/m3, with a geometric mean of 4.49 EU/m3 and 95% confidence interval of 3.53–5.71 EU/m3. Sample collection was also coupled with the use of a Coulter counter, for which the particle count (2.5–10 μm/m3) showed a significant correlation with endotoxin concentration (R2 = 0.24; p < 0.0001; n = 64). In addition, the analysis of the cultivable bacterial colony-forming units on Reasoner’s 2A agar (expressed CFU/m3) showed to be a good indicator for airborne endotoxins (R2 = 0.57; p < 0.0001; n = 58). Moreover, identification of dominant bacterial colonies on these culture plates gave some indications on potential sources of these urban outdoor bacteria and endotoxins.


Endotoxin Urban air quality Particulate matter Lipopolysaccharides Respiratory health 



We acknowledge the valuable help of Karin Van den Bergh (SPHERE, University Antwerp, Belgium) for her assistance with the Coulter counter measurements. This research was financially supported by the University of Antwerp (BOF), EUROSA, and the Fund for Scientific Research in Flanders (KaN research Grant Number 1507114N). Serena Moretti is currently holding a Ph.D. scholarship (FWO aspirant).

Supplementary material

10453_2018_9525_MOESM1_ESM.docx (419 kb)
Supplementary material 1 (DOCX 418 kb)
10453_2018_9525_MOESM2_ESM.xlsx (16 kb)
Supplementary material 2 (XLSX 15 kb)


  1. Allen, J., Bartlett, K., Graham, M., & Jackson, P. (2011). Ambient concentrations of airborne endotoxin in two cities in the interior of British Columbia, Canada. Journal of Environmental Monitoring, 13(3), 631–640. Scholar
  2. Alwis, K. U., & Milton, D. K. (2006). Recombinant factor C assay for measuring endotoxin in house dust: Comparison with LAL, and (1 → 3)-β-d-glucans. American Journal of Industrial Medicine, 49(4), 296–300.CrossRefGoogle Scholar
  3. Bowers, R. M., McCubbin, I. B., Hallar, A. G., & Fierer, N. (2012). Seasonal variability in airborne bacterial communities at a high-elevation site. Atmospheric Environment, 50, 41–49. Scholar
  4. Bowers, R. M., McLetchie, S., Knight, R., & Fierer, N. (2011a). Spatial variability in airborne bacterial communities across land-use types and their relationship to the bacterial communities of potential source environments. The ISME Journal, 5(4), 601–612.CrossRefGoogle Scholar
  5. Bowers, R. M., Sullivan, A. P., Costello, E. K., Collett, J. L., Knight, R., & Fierer, N. (2011b). Sources of bacteria in outdoor air across cities in the midwestern United States. Applied and Environmental Microbiology, 77(18), 6350–6356. Scholar
  6. Cheng, J. Y., Hui, E. L., & Lau, A. P. (2012a). Bioactive and total endotoxins in atmospheric aerosols in the Pearl River Delta region, China. Atmospheric Environment, 47, 3–11.CrossRefGoogle Scholar
  7. Cheng, J. Y. W., Hui, E. L. C., & Lau, A. P. S. (2012b). Bioactive and total endotoxins in atmospheric aerosols in the Pearl River Delta region, China. Atmospheric Environment, 47, 3–11. Scholar
  8. Degobbi, C., Saldiva, P. H. N., & Rogers, C. (2011). Endotoxin as modifier of particulate matter toxicity: A review of the literature. Aerobiologia, 27(2), 97–105. Scholar
  9. Duchaine, C., Thorne, P. S., Mériaux, A., Grimard, Y., Whitten, P., & Cormier, Y. (2001). Comparison of endotoxin exposure assessment by bioaerosol impinger and filter-sampling methods. Applied and Environmental Microbiology, 67(6), 2775–2780.CrossRefGoogle Scholar
  10. Dybwad, M., Skogan, G., & Blatny, J. M. (2014). Comparative testing and evaluation of nine different air samplers: End-to-end sampling efficiencies as specific performance measurements for bioaerosol applications. Aerosol Science and Technology, 48(3), 282–295.CrossRefGoogle Scholar
  11. Gordon, T., Galdanes, K., & Brosseau, L. (1992). Comparison of sampling media for endotoxin-contaminated aerosols. Applied Occupational and Environmental Hygiene, 7(7), 472–477.CrossRefGoogle Scholar
  12. Griffin, D. W., Gonzalez, C., Teigell, N., Petrosky, T., Northup, D. E., & Lyles, M. (2011). Observations on the use of membrane filtration and liquid impingement to collect airborne microorganisms in various atmospheric environments. Aerobiologia, 27(1), 25–35.CrossRefGoogle Scholar
  13. Heinrich, J., Pitz, M., Bischof, W., Krug, N., & Borm, P. J. A. (2003). Endotoxin in fine (PM2.5) and coarse (PM2.5–10) particle mass of ambient aerosols. A temporo-spatial analysis. Atmospheric Environment, 37(26), 3659–3667. Scholar
  14. Hyvärinen, A., Martikainen, P., & Nevalainen, A. (1991). Suitability of poor medium in counting total viable airborne bacteria. Grana, 30(2), 414–417.CrossRefGoogle Scholar
  15. Imrich, A., Ning, Y. Y., Koziel, H., Coull, B., & Kobzik, L. (1999). Lipopolysaccharide priming amplifies lung macrophage tumor necrosis factor production in response to air particles. Toxicology and Applied Pharmacology, 159(2), 117–124.CrossRefGoogle Scholar
  16. Jones, A. M., & Harrison, R. M. (2004). The effects of meteorological factors on atmospheric bioaerosol concentrations—A review. Science of the Total Environment, 326(1), 151–180.CrossRefGoogle Scholar
  17. Lane, D. J. (1991). 16S/23S rRNA sequencing (Nucleic acid techniques in bacterial systematics). New York: Wiley.Google Scholar
  18. Liebers, V., Raulf-Heimsoth, M., & Brüning, T. (2008). Health effects due to endotoxin inhalation (review). Archives of Toxicology, 82(4), 203–210. Scholar
  19. Maron, P. A., Mougel, C., Lejon, D. P. H., Carvalho, E., Bizet, K., Marck, G., et al. (2006). Temporal variability of airborne bacterial community structure in an urban area. Atmospheric Environment, 40(40), 8074–8080. Scholar
  20. Menetrez, M., Foarde, K., Esch, R., Schwartz, T., Dean, T., Hays, M., et al. (2009). An evaluation of indoor and outdoor biological particulate matter. Atmospheric Environment, 43(34), 5476–5483.CrossRefGoogle Scholar
  21. Miller, S. I., Ernst, R. K., & Bader, M. W. (2005). LPS, TLR4 and infectious disease diversity. Nature Reviews Microbiology, 3(1), 36–46.CrossRefGoogle Scholar
  22. Morgenstern, V., Carty, C. L., Gehring, U., Cyrys, J., Bischof, W., & Heinrich, J. (2005). Lack of spatial variation of endotoxin in ambient particulate matter across a German metropolitan area. Atmospheric Environment, 39(36), 6931–6941. Scholar
  23. Mueller-Anneling, L., Avol, E., Peters, J. M., & Thorne, P. S. (2004). Ambient endotoxin concentrations in PM10 from Southern California. Environmental Health Perspectives, 112(5), 583–588.CrossRefGoogle Scholar
  24. Nilsson, S., Merritt, A., & Bellander, T. (2011). Endotoxins in urban air in Stockholm, Sweden. Atmospheric Environment, 45(1), 266–270.CrossRefGoogle Scholar
  25. Ryan, P. H., Bernstein, D. I., Lockey, J., Reponen, T., Levin, L., Grinshpun, S., et al. (2009). Exposure to traffic-related particles and endotoxin during infancy is associated with wheezing at age 3 years. American Journal of Respiratory and Critical Care Medicine, 180(11), 1068–1075. Scholar
  26. Rylander, R. (2006). Endotoxin and occupational airway disease. Current opinion in Allergy and Clinical Immunology, 6(1), 62–66.CrossRefGoogle Scholar
  27. Schins, R. P. F., Lightbody, J. H., Borm, P. J. A., Shi, T., Donaldson, K., & Stone, V. (2004). Inflammatory effects of coarse and fine particulate matter in relation to chemical and biological constituents. Toxicology and Applied Pharmacology, 195(1), 1–11. Scholar
  28. Smets, W., Moretti, S., Denys, S., & Lebeer, S. (2016). Airborne bacteria in the atmosphere: Presence, purpose, and potential. Atmospheric Environment, 139, 214–221. Scholar
  29. Spaan, S., Doekes, G., Heederik, D., Thorne, P. S., & Wouters, I. M. (2008a). Effect of extraction and assay media on analysis of airborne endotoxin. Applied and Environmental Microbiology, 74(12), 3804–3811. Scholar
  30. Spaan, S., Heederik, D. J., Thorne, P. S., & Wouters, I. M. (2007). Optimization of airborne endotoxin exposure assessment: Effects of filter type, transport conditions, extraction solutions, and storage of samples and extracts. Applied and Environmental Microbiology, 73(19), 6134–6143.CrossRefGoogle Scholar
  31. Spaan, S., Schinkel, J., Wouters, I. M., Preller, L., Tielemans, E., Nij, E. T., et al. (2008b). Variability in endotoxin exposure levels and consequences for exposure assessment. Annals of Occupational Hygiene, 52(5), 303–316. Scholar
  32. Tager, I. B., Lurmann, F. W., Haight, T., Alcorn, S., Penfold, B., & Hammond, S. K. (2010). Temporal and spatial patterns of ambient endotoxin concentrations in Fresno, California. Environmental Health Perspectives, 118(10), 1491–1496. Scholar
  33. Thorne, P. S., Bartlett, K. H., Phipps, J., & Kulhankova, K. (2003). Evaluation of five extraction protocols for quantification of endotoxin in metalworking fluid aerosol. Annals of Occupational Hygiene, 47(1), 31–36.Google Scholar
  34. Thorne, P. S., Perry, S. S., Saito, R., O’Shaughnessy, P. T., Mehaffy, J., Metwali, N., et al. (2010). Evaluation of the Limulus amebocyte lysate and recombinant factor C assays for assessment of airborne endotoxin. Applied and Environmental Microbiology, 76(15), 4988–4995. Scholar
  35. Traversi, D., Alessandria, L., Schilirò, T., & Gilli, G. (2011). Size-fractionated PM10 monitoring in relation to the contribution of endotoxins in different polluted areas. Atmospheric Environment, 45(21), 3515–3521.CrossRefGoogle Scholar
  36. Turner, S., Pryer, K. M., Miao, V. P., & Palmer, J. D. (1999). Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis. Journal of Eukaryotic Microbiology, 46(4), 327–338.CrossRefGoogle Scholar
  37. Vaïtilingom, M., Amato, P., Sancelme, M., Laj, P., Leriche, M., & Delort, A.-M. (2010). Contribution of microbial activity to carbon chemistry in clouds. Applied and Environmental Microbiology, 76(1), 23–29. Scholar
  38. VMM. (2011). Comparative PM10 and PM2.5 measurements in Flanders, 2010 campaign (Depot number: D/2011/6871/022). Flemish Environmental Agency, Section Air. Philippe D’Hondt (Ed.). Available at Accessed 3 July 2018.
  39. Wheeler, A. J., Dobbin, N. A., Lyrette, N., Wallace, L., Foto, M., Mallick, R., et al. (2011). Residential indoor and outdoor coarse particles and associated endotoxin exposures. Atmospheric Environment, 45(39), 7064–7071. Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Environmental Ecology and Applied Microbiology (ENdEMIC), Department of Bioscience EngineeringUniversity of AntwerpAntwerpBelgium
  2. 2.Systemic Physiological and Ecotoxicological Research (SPHERE), Department of BiologyUniversity of AntwerpAntwerpBelgium

Personalised recommendations