Skip to main content

Advertisement

Log in

Linking the conventional and emerging detection techniques for ambient bioaerosols: a review

  • Review Paper
  • Published:
Reviews in Environmental Science and Bio/Technology Aims and scope Submit manuscript

Abstract

Bioaerosols are biologically originated particles present in the atmosphere that can be formed from any process involving biological materials. They comprise of both living and non-living components including organisms, dispersal methods of organisms, and excretions. Bioaerosols such as airborne bacteria, fungal spores, pollen, and others possess diverse characteristics and effects. A large gap exists in the scientific understanding of the overall physical characteristics and measurement of bioaerosols. Consequently, this review aims to devise an appropriate approach to generate more scientific knowledge of bioaerosols. In addition to comparisons and discussions about the various factors affecting bioaerosols, sampling, handling, and the application of various devised analytical techniques, this review offers insight into the current state of bioaerosol research. The review focuses on instrumental and methodical strategies to understand bioaerosol measurement. Numerous studies have investigated conventional methods, advanced methods, and real-time methods that can be applied for bioaerosol monitoring. Each method is different in terms of working principle, characteristics, sensitivity, and efficiency. For the first time, this review explains and compares different methods of conventional, offline, online, and real-time detection methods of bioaerosols based on their working principles, sensitivity, and efficiency on a single platform. This will provide a clear concept and better options for selecting the appropriate method based on the research proposal. Furthermore, recent advances are summarized, and future outlooks are emphasized for bioaerosol identification and categorization. This study also encourages developing affordable and standardized methods to avoid the inter-laboratory and sampling variability to obtain a better understanding and comparison of bioaerosol measurements worldwide. Nevertheless, this work can assist researchers in selecting appropriate methods for bioaerosol measurement and investigation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Agranovski V, Ristovski Z, Hargreaves M, Blackall PJ, Morawska L (2003) Real-time measurement of bacterial aerosols with the UVAPS: performance evaluation. J Aerosol Sci 34(3):301–317

    Article  CAS  Google Scholar 

  • Ali, S., 2010. Optical Processes in Microparticles and Nanostructures: A Festschrift Dedicated to Richard Kounai Chang on His Retirement from Yale University, 6. World Scientific

  • Amann RI, Ludwig W, Schleifer K-H (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59(1):143–169

    CAS  Google Scholar 

  • Amato P et al (2007) An important oceanic source of micro-organisms for cloud water at the Puy de Dôme (France). Atmos Environ 41(37):8253–8263

    Article  CAS  Google Scholar 

  • Arslan D, Legendre M, Seltzer V, Abergel C, Claverie J-M (2011) Distant Mimivirus relative with a larger genome highlights the fundamental features of Megaviridae. Proc Natl Acad Sci 108(42):17486–17491

    Article  CAS  Google Scholar 

  • Bauer H et al (2002) The contribution of bacteria and fungal spores to the organic carbon content of cloud water, precipitation and aerosols. Atmos Res 64(1–4):109–119

    Article  CAS  Google Scholar 

  • Bowers RM et al (2009) Characterization of airborne microbial communities at a high-elevation site and their potential to act as atmospheric ice nuclei. Appl Environ Microbiol 75(15):5121–5130

    Article  CAS  Google Scholar 

  • Bowers RM et al (2013) Seasonal variability in bacterial and fungal diversity of the near-surface atmosphere. Environ Sci Technol 47(21):12097–12106

    Article  CAS  Google Scholar 

  • Bowley HJ, Gerrard DL, Louden JD, Turrell G (2012) Practical raman spectroscopy. Springer, Berlin

    Google Scholar 

  • Brągoszewska E, Mainka A, Pastuszka JS (2017) Concentration and size distribution of culturable bacteria in ambient air during spring and winter in Gliwice: a typical urban area. Atmosphere 8(12):239

    Article  CAS  Google Scholar 

  • Bridge P, Spooner B (2001) Soil fungi: diversity and detection. Plant Soil 232(1–2):147–154

    Article  CAS  Google Scholar 

  • Brosseau LM et al (2000) Differences in detected fluorescence among several bacterial species measured with a direct-reading particle sizer and fluorescence detector. Aerosol Sci Technol 32(6):545–558

    Article  CAS  Google Scholar 

  • Burge HA (1995) Bioaerosol investigations. Bioaerosols. Lewis Publishers, Boca Raton, pp 1–23

    Google Scholar 

  • Cabredo S, Parra A, Saenz C, Anzano J (2009) Bioaerosols chemometric characterization by laser-induced fluorescence: air sample analysis. Talanta 77(5):1837–1842

    Article  CAS  Google Scholar 

  • Castillo JA, Staton SJ, Taylor TJ, Herckes P, Hayes MA (2012) Exploring the feasibility of bioaerosol analysis as a novel fingerprinting technique. Anal Bioanal Chem 403(1):15–26

    Article  CAS  Google Scholar 

  • Chen P-S, Li C-S (2005) Sampling performance for bioaerosols by flow cytometry with fluorochrome. Aerosol Sci Technol 39(3):231–237

    Article  CAS  Google Scholar 

  • Chen P-S, Li C-S (2007) Real-time monitoring for bioaerosols—flow cytometry. Analyst 132(1):14–16

    Article  CAS  Google Scholar 

  • Chi M-C, Li C-S (2007) Fluorochrome in monitoring atmospheric bioaerosols and correlations with meteorological factors and air pollutants. Aerosol Sci Technol 41(7):672–678

    Article  CAS  Google Scholar 

  • Choi J, Kang M, Jung JH (2015) Integrated micro-optofluidic platform for real-time detection of airborne microorganisms. Sci Rep 5:15983

    Article  CAS  Google Scholar 

  • Chow JC et al (2015) Characterization of ambient PM10 bioaerosols in a California agricultural town. Aerosol Air Qual Res 15(4):1433–1447

    Article  CAS  Google Scholar 

  • Clauß M (2015) Particle size distribution of airborne microorganisms in the environment-a review. Appl Agric Forestry Res

  • Corzo CA et al (2013) Relationship between airborne detection of influenza A virus and the number of infected pigs. Vet J 196(2):171–175

    Article  Google Scholar 

  • Cox CS, Wathes CM (1995) Bioaerosols handbook. CRC Press, Boca Raton

    Google Scholar 

  • Crook B, Lacey J (1988) Enumeration of airborne micro-organisms in work environments. Environ Technol 9(6):515–520

    CAS  Google Scholar 

  • Damit B (2017) Droplet-based microfluidics detector for bioaerosol detection. Aerosol Sci Technol 51(4):488–500

    Article  CAS  Google Scholar 

  • Darwin C (1846) An account of the fine dust which often falls on vessels in the Atlantic Ocean. Q J Geol Soc 2(1–2):26–30

    Article  Google Scholar 

  • Dasgupta PK, Poruthoor SK (2002) Automated measurement of atmospheric particle composition, comprehensive analytical chemistry. Elsevier, Amsterdam, pp 161–218

    Google Scholar 

  • Deacon L et al (2009) Particle size distribution of airborne Aspergillus fumigatus spores emitted from compost using membrane filtration. Atmos Environ 43(35):5698–5701

    Article  CAS  Google Scholar 

  • DeFreez R (2009) LIF bio-aerosol threat triggers: then and now, optically based biological and chemical detection for defence V. International Society for Optics and Photonics, pp 74840H

  • Deguillaume L et al (2008) Microbiology and atmospheric processes: chemical interactions of primary biological aerosols. Biogeosci Discuss 5(1):841–870

    Article  Google Scholar 

  • Després V et al (2007) Characterization of primary biogenic aerosol particles in urban, rural, and high-alpine air by DNA sequence and restriction fragment analysis of ribosomal RNA genes. Biogeosciences 4(6):1127–1141

    Article  Google Scholar 

  • Després V et al (2012) Primary biological aerosol particles in the atmosphere: a review. Tellus B Chem Phys Meteorol 64(1):15598

    Article  Google Scholar 

  • Douwes J et al (1999) Fungal extracellular polysaccharides in house dust as a marker for exposure to fungi: relations with culturable fungi, reported home dampness, and respiratory symptoms. J Allergy Clin Immunol 103(3):494–500

    Article  CAS  Google Scholar 

  • Duchaine C et al (2001) Comparison of endotoxin exposure assessment by bioaerosol impinger and filter-sampling methods. Appl Environ Microbiol 67(6):2775–2780

    Article  CAS  Google Scholar 

  • Dungan RS, Leytem AB (2009) Qualitative and quantitative methodologies for determination of airborne microorganisms at concentrated animal-feeding operations. World J Microbiol Biotechnol 25(9):1505–1518

    Article  Google Scholar 

  • Dybwad M, Skogan G, Blatny JM (2014) Comparative testing and evaluation of nine different air samplers: end-to-end sampling efficiencies as specific performance measurements for bioaerosol applications. Aerosol Sci Technol 48(3):282–295

    Article  CAS  Google Scholar 

  • Elbert W, Taylor P, Andreae M, Pöschl U (2007) Contribution of fungi to primary biogenic aerosols in the atmosphere: wet and dry discharged spores, carbohydrates, and inorganic ions. Atmos Chem Phys 7(17):4569–4588

    Article  CAS  Google Scholar 

  • Engelhart S, Glasmacher A, Simon A, Exner M (2007) Air sampling of Aspergillus fumigatus and other thermotolerant fungi: comparative performance of the Sartorius MD8 airport and the Merck MAS-100 portable bioaerosol sampler. Int J Hyg Environ Health 210(6):733–739

    Article  Google Scholar 

  • Estillore AD, Trueblood JV, Grassian VH (2016) Atmospheric chemistry of bioaerosols: heterogeneous and multiphase reactions with atmospheric oxidants and other trace gases. Chem Science 7(11):6604–6616

    Article  CAS  Google Scholar 

  • Evanoff DD, Heckel J, Caldwell TP, Christensen KA, Chumanov G (2006) Monitoring DPA release from a single germinating bacillus s ubtilis endospore via surface-enhanced Raman Scattering Microscopy. J Am Chem Soc 128(39):12618–12619

    Article  CAS  Google Scholar 

  • Eversole JD, Roselle D, Seaver ME (1999) Monitoring biological aerosols using UV fluorescence, Air Monitoring and Detection of Chemical and Biological Agents. International Society for Optics and Photonics, pp 34–43

  • Eversole J et al (2001) Continuous bioaerosol monitoring using UV excitation fluorescence: outdoor test results. Field Anal Chem Technol 5(4):205–212

    Article  CAS  Google Scholar 

  • Fabian M, Miller S, Reponen T, Hernandez M (2005) Ambient bioaerosol indices for indoor air quality assessments of flood reclamation. J Aerosol Sci 36(5–6):763–783

    Article  CAS  Google Scholar 

  • Fabian P, McDevitt J, Houseman E, Milton D (2009) Airborne influenza virus detection with four aerosol samplers using molecular and infectivity assays: considerations for a new infectious virus aerosol sampler. J Aerosol Sci 19(5):433–441

    CAS  Google Scholar 

  • Falacy JS (2003) Detection of Erysiphe necator (Uncinula necator) with polymerase chain reaction and species-specific primers

  • Fannin K (1981) An approach to the study of environmental microbial aerosols, Water Pollution Research and Development. Elsevier, pp 1103–1119

  • Fennelly M, Sewell G, Prentice M, O’Connor D, Sodeau J (2017) The use of real-time fluorescence instrumentation to monitor ambient primary biological aerosol particles (PBAP). Atmosphere 9(1):1

    Article  CAS  Google Scholar 

  • Fergenson DP et al (2004) Reagentless detection and classification of individual bioaerosol particles in seconds. Anal Chem 76(2):373–378

    Article  CAS  Google Scholar 

  • Frohlich-Nowoisky J, Pickersgill DA, Despres VR, Poschl U (2009) High diversity of fungi in air particulate matter. Proc Natl Acad Sci U S A 106(31):12814–12819

    Article  Google Scholar 

  • Fröhlich-Nowoisky J et al (2016) Bioaerosols in the Earth system: climate, health, and ecosystem interactions. Atmos Res 182:346–376

    Article  CAS  Google Scholar 

  • Gabey A et al (2010) Measurements and comparison of primary biological aerosol above and below a tropical forest canopy using a dual channel fluorescence spectrometer. Atmos Chem Phys 10(10):4453–4466

    Article  CAS  Google Scholar 

  • Gabey A, Stanley W, Gallagher M, Kaye PH (2011) The fluorescence properties of aerosol larger than 0.8 μm in urban and tropical rainforest locations. Atmos Chem Phys 11(11):5491–5504

    Article  CAS  Google Scholar 

  • Gard E et al (1997) Real-time analysis of individual atmospheric aerosol particles: design and performance of a portable ATOFMS. Anal Chem 69(20):4083–4091

    Article  CAS  Google Scholar 

  • Genic Staphylococci P (2004) Phylogenetic considerations. Clin Microbiol Rev 17(2):840–862

    Google Scholar 

  • Gentry JW (1997) The legacy of John Tyndall in aerosol science. J Aerosol Sci 28(8):1365–1372

    Article  CAS  Google Scholar 

  • Georgakopoulos D et al (2009) Microbiology and atmospheric processes: biological, physical and chemical characterization of aerosol particles. Biogeosciences 6(4):721–737

    Article  CAS  Google Scholar 

  • Ghosh B, Lal H, Srivastava A (2015) Review of bioaerosols in indoor environment with special reference to sampling, analysis and control mechanisms. Environ Int 85:254–272

    Article  Google Scholar 

  • Gilbert Y, Duchaine C (2009) Bioaerosols in industrial environments: a review. Can J Civil Eng 36(12):1873–1886

    Article  CAS  Google Scholar 

  • Globus T, Gelmont B (2014) Biological detection with terahertz spectroscopy, bioaerosol detection technologies. Springer, Berlin, pp 241–264

    Book  Google Scholar 

  • Globus T et al (2003) THz-frequency spectroscopic sensing of DNA and related biological materials. Int J High Speed Electron Syst 13(04):903–936

    Article  CAS  Google Scholar 

  • Globus T, Khromova T, Woolard D, Gelmont B (2004) Terahertz Fourier transform characterization of biological materials in solid and liquid phases, chemical and biological standoff detection. International Society for Optics and Photonics, pp 10–19

  • Golding CG, Lamboo LL, Beniac DR, Booth TF (2016) The scanning electron microscope in microbiology and diagnosis of infectious disease. Sci Rep 6:26516

    Article  CAS  Google Scholar 

  • Gosselin MI et al (2016) Fluorescent bioaerosol particle, molecular tracer, and fungal spore concentrations during dry and rainy periods in a semi-arid forest. Atmos Chem Phys 16(23):15165–15184

    Article  CAS  Google Scholar 

  • Griffiths W, Boysan F (1996) Computational fluid dynamics (CFD) and empirical modelling of the performance of a number of cyclone samplers. J Aerosol Sci 27(2):281–304

    Article  CAS  Google Scholar 

  • Griffiths W, Stewart I, Futter S, Upton S, Mark D (1997) The development of sampling methods for the assessment of indoor bioaerosols. J Aerosol Sci 28(3):437–457

    Article  CAS  Google Scholar 

  • Gόrny RL, Dutkiewicz J, Krysinska-Traczyk E (1999) Size distribution of bacterial and fungal bioaerosols in indoor air. Ann Agric Environ Med 6:105–113

    Google Scholar 

  • Haddrell AE, Thomas RJ (2017) Aerobiology: experimental considerations, observations, and future tools. Appl Environ Microbiol 83(17)

  • Hairston PP, Ho J, Quant FR (1997) Design of an instrument for real-time detection of bioaerosols using simultaneous measurement of particle aerodynamic size and intrinsic fluorescence. J Aerosol Sci 28(3):471–482

    Article  CAS  Google Scholar 

  • Hall RJ et al (2013) Metagenomic detection of viruses in aerosol samples from workers in animal slaughterhouses. PLoS ONE 8(8):e72226

    Article  CAS  Google Scholar 

  • Han T, Mainelis G (2008) Design and development of an electrostatic sampler for bioaerosols with high concentration rate. J Aerosol Sci 39(12):1066–1078

    Article  CAS  Google Scholar 

  • Han T, An HR, Mainelis G (2010) Performance of an electrostatic precipitator with superhydrophobic surface when collecting airborne bacteria. Aerosol Sci Technol 44(5):339–348

    Article  CAS  Google Scholar 

  • Han T, Wren M, DuBois K, Therkorn J, Mainelis G (2015) Application of ATP-based bioluminescence for bioaerosol quantification: effect of sampling method. J Aerosol Sci 90:114–123

    Article  CAS  Google Scholar 

  • He Q, Yao M (2011) Integration of high volume portable aerosol-to-hydrosol sampling and qPCR in monitoring bioaerosols. J Environ Monit 13(3):706–712

    Article  CAS  Google Scholar 

  • Healy D et al (2014) Ambient measurements of biological aerosol particles near Killarney, Ireland: a comparison between real-time fluorescence and microscopy techniques. Atmos Chem Phys 14(15):8055–8069

    Article  CAS  Google Scholar 

  • Heidelberg J et al (1997) Effect of aerosolization on culturability and viability of gram-negative bacteria. Appl Environ Microbiol 63(9):3585–3588

    CAS  Google Scholar 

  • Heikkinen M, Hjelmoroos-Koski M, Haggblom M, Macher J (2005) Bioaerosols. In: LS Ruzer, NH Harley Aerosols handbook, measurement, dosimetry, and health effects. CRC Press, New York

  • Henningson EW, Ahlberg MS (1994) Evaluation of microbiological aerosol samplers: a review. J Aerosol Sci 25(8):1459–1492

    Article  Google Scholar 

  • Hernandez M et al. (2016) Chamber catalogues of optical and fluorescent signatures distinguish bioaerosol classes. Atmos Meas Tech 9(7)

  • Hirst E, Kaye PH (1996) Experimental and theoretical light scattering profiles from spherical and nonspherical particles. J Geophys Res Atmos 101(D14):19231–19235

    Article  Google Scholar 

  • Ho J (2011) Use of virtual impactor (VI) technology in biological aerosol detection. KONA Powder Part J 29:16–26

    Article  CAS  Google Scholar 

  • Ho J, Spence M, Hairston P (1999) Measurement of biological aerosol with a fluorescent aerodynamic particle sizer (FLAPS): correlation of optical data with biological data. Aerobiologia 15(4):281–291

    Article  Google Scholar 

  • Hogan C Jr et al (2005) Sampling methodologies and dosage assessment techniques for submicrometre and ultrafine virus aerosol particles. J Appl Microbiol 99(6):1422–1434

    Article  Google Scholar 

  • Hoisington AJ, Maestre JP, King MD, Siegel JA, Kinney KA (2014) Impact of sampler selection on the characterization of the indoor microbiome via high-throughput sequencing. Build Environ 80:274–282

    Article  Google Scholar 

  • Huffman J, Treutlein B, Pöschl U (2010) Fluorescent biological aerosol particle concentrations and size distributions measured with an ultraviolet aerodynamic particle sizer (UV-APS) in Central Europe. Atmos Chem Phys 10(7):3215–3233

    Article  CAS  Google Scholar 

  • Huffman J et al (2012) Size distributions and temporal variations of biological aerosol particles in the Amazon rainforest characterized by microscopy and real-time UV-APS fluorescence techniques during AMAZE-08. Atmos Chem Phys 12(24):11997–12019

    Article  CAS  Google Scholar 

  • Huffman JA et al (2013) High concentrations of biological aerosol particles and ice nuclei during and after rain. Atmos Chem Phys 13(13):6151

    Article  CAS  Google Scholar 

  • Humbal C, Gautam S, Trivedi U (2018) A review on recent progress in observations, and health effects of bioaerosols. Environ Int 118:189–193

    Article  CAS  Google Scholar 

  • Imai M et al (2012) Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets. Nature 486(7403):420

    Article  CAS  Google Scholar 

  • Jaenicke R (2005) Abundance of cellular material and proteins in the atmosphere. Science 308(5718):73

    Article  CAS  Google Scholar 

  • Jones LJ, Carballido-López R, Errington J (2001) Control of cell shape in bacteria: helical, actin-like filaments in Bacillus subtilis. Cell 104(6):913–922

    Article  CAS  Google Scholar 

  • Jonsson P, Kullander F (2014) Bioaerosol detection with fluorescence spectroscopy, bioaerosol detection technologies. Springer, Berlin, pp 111–141

    Book  Google Scholar 

  • Juozaitis A, Willeke K, Grinshpun SA, Donnelly J (1994) Impaction onto a glass slide or agar versus impingement into a liquid for the collection and recovery of airborne microorganisms. Appl Environ Microbiol 60(3):861–870

    CAS  Google Scholar 

  • Kamperman T, Trikalitis VD, Karperien M, Visser CW, Leijten J (2018) Ultrahigh-throughput production of monodisperse and multifunctional janus microparticles using in-air microfluidics. ACS Appl Mater Interfaces 10(28):23433–23438

    Article  CAS  Google Scholar 

  • Karl DM (1980) Cellular nucleotide measurements and applications in microbial ecology. Microbiol Rev 44(4):739

    CAS  Google Scholar 

  • Kaye PH, Eyles N, Ludlow I, Clark J (1991) An instrument for the classification of airborne particles on the basis of size, shape, and count frequency. Atmos Environ Part A Gen Top 25(3–4):645–654

    Article  Google Scholar 

  • Kaye PH, Alexander-Buckley K, Hirst E, Saunders S, Clark J (1996) A real-time monitoring system for airborne particle shape and size analysis. J Geophys Res Atmos 101(D14):19215–19221

    Article  Google Scholar 

  • Kaye PH et al (2005) Single particle multichannel bio-aerosol fluorescence sensor. Opt Express 13(10):3583–3593

    Article  CAS  Google Scholar 

  • Kesavan J, Hottell K (2005) Characteristics and sampling efficiencies of two bioguardian (Registered) 12.03 Aerosol samplers, Edgewood Chemical Biological Center, Aberdeen Proving Ground MD

  • Kesavan J, Sagripanti J-L (2015) Evaluation criteria for bioaerosol samplers. Environ Sci Process Impacts 17(3):638–645

    Article  CAS  Google Scholar 

  • Kesavan J, Schepers D, McFarland AR (2010) Sampling and retention efficiencies of batch-type liquid-based bioaerosol samplers. Aerosol Sci Technol 44(10):817–829

    Article  CAS  Google Scholar 

  • Krafft C (2010) Raman and CARS microscopy of cells and tissues, handbook of photonics for biomedical science. CRC Press, Boca Raton, pp 229–259

    Google Scholar 

  • L’Orange C, Anderson K, Sleeth D, Anthony TR, Volckens J (2015) A simple and disposable sampler for inhalable aerosol. Ann Occup Hyg 60(2):150–160

    Article  CAS  Google Scholar 

  • Lal H, Ghosh B, Srivastava A, Srivastava A (2017) Identification and characterization of size-segregated bioaerosols at different sites in Delhi. Aerosol Air Qual Res 17(6):1570–1581

    Article  CAS  Google Scholar 

  • Lee BU (2011) Life comes from the air: a short review on bioaerosol control. Aerosol Air Qual Res 11(7):921–927

    Article  Google Scholar 

  • Lee S-A et al (2004) Assessment of electrical charge on airborne microorganisms by a new bioaerosol sampling method. J Occup Environ Hyg 1(3):127–138

    Article  Google Scholar 

  • Lee J, Jang J, Akin D, Savran CA, Bashir R (2008) Real-time detection of airborne viruses on a mass-sensitive device. Appl Phys Lett 93(1):013901

    Article  CAS  Google Scholar 

  • Lee S, Choi B, Yi SM, Ko G (2009) Characterization of microbial community during Asian dust events in Korea. Sci Total Environ 407(20):5308–5314

    Article  CAS  Google Scholar 

  • Lee SH et al (2010) Identification of airborne bacterial and fungal community structures in an urban area by T-RFLP analysis and quantitative real-time PCR. Sci Total Environ 408(6):1349–1357

    Article  CAS  Google Scholar 

  • Li C-S (1999) Sampling performance of impactors for bacterial bioaerosols. Aerosol Sci Technol 30(3):280–287

    Article  Google Scholar 

  • Li M, Xu J, Romero-Gonzalez M, Banwart SA, Huang WE (2012) Single cell Raman spectroscopy for cell sorting and imaging. Curr Opin Biotechnol 23(1):56–63

    Article  CAS  Google Scholar 

  • Lim DV, Simpson JM, Kearns EA, Kramer MF (2005) Current and developing technologies for monitoring agents of bioterrorism and biowarfare. Clin Microbiol Rev 18(4):583–607

    Article  CAS  Google Scholar 

  • Lin W-H (1999) Collection efficiency and culturability of impingement into a liquid for bioaerosols of fungal spores and yeast cells. Aerosol Sci Technol 30(2):109–118

    Article  CAS  Google Scholar 

  • Lin X, Willeke K, Ulevicius V, Grinshpun SA (1997) Effect of sampling time on the collection efficiency of all-glass impingers. Am Ind Hyg Assoc J 58(7):480–488

    Article  CAS  Google Scholar 

  • Lindsley WG, Schmechel D, Chen BT (2006) A two-stage cyclone using microcentrifuge tubes for personal bioaerosol sampling. J Environ Monit 8(11):1136–1142

    Article  CAS  Google Scholar 

  • Löndahl J (2014) Physical and biological properties of bioaerosols. Bioaerosol Detection Technologies, Integrated Analytical Systems, pp 33–48

  • Macher J (1999) Developing a sampling plan. Bioaerosols Assess Control 5:1–5

    Google Scholar 

  • Madsen AM, Zervas A, Tendal K, Nielsen JL (2015) Microbial diversity in bioaerosol samples causing ODTS compared to reference bioaerosol samples as measured using Illumina sequencing and MALDI-TOF. Environ Res 140:255–267

    Article  CAS  Google Scholar 

  • Mainelis G (1999) Collection of airborne microorganisms by electrostatic precipitation. Aerosol Sci Technol 30(2):127–144

    Article  CAS  Google Scholar 

  • Mainelis G, Tabayoyong M (2010) The effect of sampling time on the overall performance of portable microbial impactors. Aerosol Sci Technol 44(1):75–82

    Article  CAS  Google Scholar 

  • Mainelis G et al (2001) Electrical charges on airborne microorganisms. J Aerosol Sci 32(9):1087–1110

    Article  CAS  Google Scholar 

  • Maliutina K, Tahmasebi A, Yu J (2018) Effects of pressure on morphology and structure of bio-char from pressurized entrained-flow pyrolysis of microalgae. Data Brief 18:422–431

    Article  Google Scholar 

  • McFarland AR et al (2010) Wetted wall cyclones for bioaerosol sampling. Aerosol Sci Technol 44(4):241–252

    Article  CAS  Google Scholar 

  • Mehta SK, Mishra S, Pierson DL (1996) Evaluation of three portable samplers for monitoring airborne fungi. Appl Environ Microbiol 62(5):1835–1838

    CAS  Google Scholar 

  • Menetrez MY et al (2007) The measurement of ambient bioaerosol exposure. Aerosol Sci Technol 41(9):884–893

    Article  CAS  Google Scholar 

  • Miaskiewicz-Peska E, Lebkowska M (2012) Comparison of aerosol and bioaerosol collection on air filters. Aerobiologia (Bologna) 28(2):185–193

    Article  Google Scholar 

  • Moon H-S, Lee J-H, Kwon K, Jung H-I (2012) Review of recent progress in micro-systems for the detection and analysis of airborne microorganisms. Anal Lett 45(2–3):113–129

    Article  CAS  Google Scholar 

  • Nasir Z et al (2018) A controlled study on the characterisation of bioaerosols emissions from compost. Atmosphere 9(10):379

    Article  Google Scholar 

  • Nasir ZA et al (2019) Scoping studies to establish the capability and utility of a real-time bioaerosol sensor to characterise emissions from environmental sources. Sci Total Environ 648:25–32

    Article  CAS  Google Scholar 

  • Nevalainen A, Pastuszka J, Liebhaber F, Willeke K (1992) Performance of bioaerosol samplers: collection characteristics and sampler design considerations. Atmos Environ Part A Gen Top 26(4):531–540

    Article  Google Scholar 

  • Noble CA, Prather KA (2000) Real-time single particle mass spectrometry: a historical review of a quarter century of the chemical analysis of aerosols. Mass Spectrom Rev 19(4):248–274

    Article  CAS  Google Scholar 

  • Nonnenmann M, Bextine B, Dowd S, Gilmore K, Levin J (2010) Culture-independent characterization of bacteria and fungi in a poultry bioaerosol using pyrosequencing: a new approach. J Occup Environ Hyg 7(12):693–699

    Article  CAS  Google Scholar 

  • Noris F, Siegel JA, Kinney KA (2011) Evaluation of HVAC filters as a sampling mechanism for indoor microbial communities. Atmos Environ 45(2):338–346

    Article  CAS  Google Scholar 

  • Núñez A et al (2016) Monitoring of airborne biological particles in outdoor atmosphere. Part 1: importance, variability and ratios

  • O’Connor DJ, Healy DA, Sodeau JR (2013) The on-line detection of biological particle emissions from selected agricultural materials using the WIBS-4 (Waveband Integrated Bioaerosol Sensor) technique. Atmos Environ 80:415–425

    Article  CAS  Google Scholar 

  • Pan Y-L et al (2010) Fluorescence spectra of atmospheric aerosol particles measured using one or two excitation wavelengths: comparison of classification schemes employing different emission and scattering results. Opt Express 18(12):12436–12457

    Article  CAS  Google Scholar 

  • Park J-W, Kim HR, Hwang J (2016) Continuous and real-time bioaerosol monitoring by combined aerosol-to-hydrosol sampling and ATP bioluminescence assay. Analy Chim Acta 941:101–107

    Article  CAS  Google Scholar 

  • Pathak, A.K., 2014. RECENT TRENDS IN BIO-AEROSOL STUDIES. CIBTech Journal of Microbiology, 4(3)

  • Phan HN, McFarland AR (2004) Aerosol-to-hydrosol transfer stages for use in bioaerosol sampling. Aerosol Sci Technol 38(4):300–310

    Article  CAS  Google Scholar 

  • Pillai SD, Ricke SC (2002) Review/Synthèse Bioaerosols from municipal and animal wastes: background and contemporary issues. Can J Microbiol 48(8):681–696

    Article  CAS  Google Scholar 

  • Polymenakou PN, Mandalakis M, Stephanou EG, Tselepides A (2007) Particle size distribution of airborne microorganisms and pathogens during an intense African dust event in the eastern Mediterranean. Environ Health Perspect 116(3):292–296

    Article  Google Scholar 

  • Predicala BZ, Urban JE, Maghirang RG, Jerez SB, Goodband RD (2002) Assessment of bioaerosols in swine barns by filtration and impaction. Curr Microbiol 44(2):136–140

    Article  CAS  Google Scholar 

  • Prussin AJ 2nd, Marr LC (2015) Sources of airborne microorganisms in the built environment. Microbiome 3:78

    Article  Google Scholar 

  • Prussin AJ 2nd, Marr LC, Bibby KJ (2014) Challenges of studying viral aerosol metagenomics and communities in comparison with bacterial and fungal aerosols. FEMS Microbiol Lett 357(1):1–9

    Article  CAS  Google Scholar 

  • Raisi L, Aleksandropoulou V, Lazaridis M, Katsivela E (2013) Size distribution of viable, cultivable, airborne microbes and their relationship to particulate matter concentrations and meteorological conditions in a Mediterranean site. Aerobiologia 29(2):233–248

    Article  Google Scholar 

  • Rathnayake CM et al (2017) Influence of rain on the abundance of bioaerosols in fine and coarse particles. Atmos Chem Phys 17(3):2459–2475

    Article  CAS  Google Scholar 

  • Reponen T, Hyvärinen A, Ruuskanen J, Raunemaa T, Nevalainen A (1994) Comparison of concentrations and size distributions of fungal spores in buildings with and without mould problems. J Aerosol Sci 25(8):1595–1603

    Article  CAS  Google Scholar 

  • Reponen, T., Willeke, K., Grinshpun, S., Nevalainen, A., 2011. Biological particle sampling. Aerosol measurement: principles, techniques, and applications: 549-570

  • Rinsoz T, Duquenne P, Greff-Mirguet G, Oppliger A (2008) Application of real-time PCR for total airborne bacterial assessment: comparison with epifluorescence microscopy and culture-dependent methods. Atmos Environ 42(28):6767–6774

    Article  CAS  Google Scholar 

  • Robins A (2014) Blackett Review on wide-area biological detection

  • Roux J-M, Kaspari O, Heinrich R, Hanschmann N, Grunow R (2013) Investigation of a new electrostatic sampler for concentrating biological and non-biological aerosol particles. Aerosol Sci Technol 47(5):463–471

    Article  CAS  Google Scholar 

  • Rule AM, Kesavan J, Schwab KJ, Buckley TJ (2007) Application of flow cytometry for the assessment of preservation and recovery efficiency of bioaerosol samplers spiked with Pantoea agglomerans. Enviro Sci Technol 41(7):2467–2472

    Article  CAS  Google Scholar 

  • Russell SC et al (2004) Toward understanding the ionization of biomarkers from micrometer particles by bio-aerosol mass spectrometry. J Am Soc Mass Spectrom 15(6):900–909

    Article  CAS  Google Scholar 

  • Ryškevič N et al (2010) Concept design of a UV light-emitting diode based fluorescence sensor for real-time bioparticle detection. Sensors Actuators B Chem 148(2):371–378

    Article  CAS  Google Scholar 

  • Sahu A, Grimberg SJ, Holsen TM (2005) A static water surface sampler to measure bioaerosol deposition and characterize microbial community diversity. J Aerosol Sci 36(5–6):639–650

    Article  CAS  Google Scholar 

  • Sengupta A, Laucks M, Dildine N, Drapala E, Davis E (2005a) Bioaerosol characterization by surface-enhanced Raman spectroscopy (SERS). J Aerosol Sci 36(5–6):651–664

    Article  CAS  Google Scholar 

  • Sengupta A, Laucks ML, Davis EJ (2005b) Surface-enhanced Raman spectroscopy of bacteria and pollen. Appl Spectrosc 59(8):1016–1023

    Article  CAS  Google Scholar 

  • Seshadri S, Han T, Krumins V, Fennell DE, Mainelis G (2009) Application of ATP bioluminescence method to characterize performance of bioaerosol sampling devices. J Aerosol Sci 40(2):113–121

    Article  CAS  Google Scholar 

  • Sharma Ghimire P et al (2016) Insight into enzymatic degradation of corn, wheat, and soybean cell wall cellulose using quantitative secretome analysis of Aspergillus fumigatus. J Proteome Res 15(12):4387–4402

    Article  CAS  Google Scholar 

  • Shintani H, Taniai E, Miki A, Kurosu S, Hayashi F (2004) Comparison of the collecting efficiency of microbiological air samplers. J Hosp Infect 56(1):42–48

    Article  CAS  Google Scholar 

  • Sivaprakasam V, Huston AL, Scotto C, Eversole JD (2004) Multiple UV wavelength excitation and fluorescence of bioaerosols. Opt Express 12(19):4457–4466

    Article  CAS  Google Scholar 

  • Smets W, Moretti S, Denys S, Lebeer S (2016) Airborne bacteria in the atmosphere: presence, purpose, and potential. Atmos Environ 139:214–221

    Article  CAS  Google Scholar 

  • Stetzenbach LD (2007) Introduction to aerobiology, Manual of Environmental Microbiology, Third Edition. American Society of Microbiology, pp 925–938

  • Suess DT, Prather KA (1999) Mass spectrometry of aerosols. Chem Rev 99(10):3007–3036

    Article  CAS  Google Scholar 

  • Svensson T (2016) Airborne microorganisms. A methodology to examine viability of bioaerosols. http://lup.lub.lu.se/student-papers/record/8884293

  • Szponar B, Larsson L (2001) Use of mass spectrometry for characterising microbial communities in bioaerosols. Ann Agric Environ Med 8(2):111–117

    CAS  Google Scholar 

  • Taiwo AM, Beddows DC, Shi Z, Harrison RM (2014) Mass and number size distributions of particulate matter components: comparison of an industrial site and an urban background site. Sci Total Environ 475:29–38

    Article  CAS  Google Scholar 

  • Tan M, Shen F, Yao M, Zhu T (2011) Development of an automated electrostatic sampler (AES) for bioaerosol detection. Aerosol Sci Technol 45(9):1154–1160

    Article  CAS  Google Scholar 

  • Tang, J.W., 2009. The effect of environmental parameters on the survival of airborne infectious agents. Journal of the Royal Society Interface: rsif20090227

  • Taylor PE, Flagan RC, Valenta R, Glovsky MM (2002) Release of allergens as respirable aerosols: a link between grass pollen and asthma. J Allergy Clin Immunol 109(1):51–56

    Article  Google Scholar 

  • Terzieva S et al (1996) Comparison of methods for detection and enumeration of airborne microorganisms collected by liquid impingement. Appl Environ Microbiol 62(7):2264–2272

    CAS  Google Scholar 

  • Thompson MW, Donnelly J, Grinshpun SA, Juozaitis A, Willeke K (1994) Method and test system for evaluation of bioaerosol samplers. J Aerosol Sci 25(8):1579–1593

    Article  CAS  Google Scholar 

  • Tobias HJ et al (2005) Bioaerosol mass spectrometry for rapid detection of individual airborne Mycobacterium tuberculosis H37Ra particles. Appl Environ Microbiol 71(10):6086–6095

    Article  CAS  Google Scholar 

  • Tripathi A et al (2009) Bioaerosol analysis with Raman chemical imaging microspectroscopy. Anal Chem 81(16):6981–6990

    Article  CAS  Google Scholar 

  • Trunov M, Trakumas S, Willeke K, Grinshpun SA, Reponen T (2001) Collection of bioaerosol particles by impaction: effect of fungal spore agglomeration and bounce. Aerosol Sci Technol 35(1):617–624

    Article  CAS  Google Scholar 

  • Tseng C-C, Li C-S (2005) Collection efficiencies of aerosol samplers for virus-containing aerosols. J Aerosol Sci 36(5–6):593–607

    Article  CAS  Google Scholar 

  • Unterwurzacher V et al (2018) Validation of a quantitative PCR based detection system for indoor mold exposure assessment in bioaerosols. Environmental Science: Processes & Impacts

  • Van Duyne RP (1979) Laser excitation of Raman scattering from adsorbed molecules on electrode surfaces. Chem Biochem Appl Lasers 4:101

    Article  Google Scholar 

  • Van Wuijckhuijse A et al (2005) Matrix-assisted laser desorption/ionisation aerosol time-of-flight mass spectrometry for the analysis of bioaerosols: development of a fast detector for airborne biological pathogens. J Aerosol Sci 36(5–6):677–687

    Article  CAS  Google Scholar 

  • Vanhee LM, Nelis HJ, Coenye T (2009) Detection and quantification of viable airborne bacteria and fungi using solid-phase cytometry. Nat Protoc 4(2):224–231

    Article  CAS  Google Scholar 

  • Verboket PE, Borovinskaya O, Meyer N, Günther D, Dittrich PS (2014) A new microfluidics-based droplet dispenser for ICPMS. Anal Chem 86(12):6012–6018

    Article  CAS  Google Scholar 

  • Verreault D, Moineau S, Duchaine C (2008) Methods for sampling of airborne viruses. Microbiol Mol Biol Rev 72(3):413–444

    Article  CAS  Google Scholar 

  • Wang Z, Reponen T, Grinshpun SA, Górny RL, Willeke K (2001) Effect of sampling time and air humidity on the bioefficiency of filter samplers for bioaerosol collection. J Aerosol Sci 32(5):661–674

    Article  CAS  Google Scholar 

  • Wang CH et al (2015) Field evaluation of personal sampling methods for multiple bioaerosols. PLoS ONE 10(3):e0120308

    Article  CAS  Google Scholar 

  • Welker M, Moore ER (2011) Applications of whole-cell matrix-assisted laser-desorption/ionization time-of-flight mass spectrometry in systematic microbiology. Syst Appl Microbiol 34(1):2–11

    Article  CAS  Google Scholar 

  • Willeke K, Lin X, Grinshpun SA (1998) Improved aerosol collection by combined impaction and centrifugal motion. Aerosol Sci Technol 28(5):439–456

    Article  CAS  Google Scholar 

  • Woodward RM (2004) Terahertz technology in biological and chemical sensing for defence, Optically Based Biological and Chemical Sensing for Defence. International Society for Optics and Photonics, pp. 341–353

  • Wu Y et al (2015) MS2 virus inactivation by atmospheric-pressure cold plasma using different gas carriers and power levels. Appl Environ Microbiol 81(3):996–1002

    Article  CAS  Google Scholar 

  • Xu Z, Yao M (2011) Analysis of culturable bacterial and fungal aerosol diversity obtained using different samplers and culturing methods. Aerosol Sci Technol 45(9):1143–1153

    Article  CAS  Google Scholar 

  • Xu Z et al (2011) Bioaerosol science, technology, and engineering: past, present, and future. Aerosol Sci Technol 45(11):1337–1349

    Article  CAS  Google Scholar 

  • Yamamoto N, Nazaroff WW, Peccia J (2014) Assessing the aerodynamic diameters of taxon-specific fungal bioaerosols by quantitative PCR and next-generation DNA sequencing. J Aerosol Sci 78:1–10

    Article  CAS  Google Scholar 

  • Yao M (2018) Reprint of bioaerosol: a bridge and opportunity for many scientific research fields. J Aerosol Sci 119:91–96

    Article  CAS  Google Scholar 

  • Yao M, Mainelis G (2006) Utilization of natural electrical charges on airborne microorganisms for their collection by electrostatic means. J Aerosol Sci 37(4):513–527

    Article  CAS  Google Scholar 

  • Yao M, Mainelis G (2007) Analysis of portable impactor performance for enumeration of viable bioaerosols. J Occup Environ Hyg 4(7):514–524

    Article  Google Scholar 

  • Yoo K, Yoo H, Lee JM, Shukla SK, Park J (2018) Classification and regression tree approach for prediction of potential hazards of urban airborne bacteria during asian dust events. Sci Rep 8(1):11823

    Article  CAS  Google Scholar 

  • Yoon KY, Park CW, Byeon JH, Hwang J (2010) Design and application of an inertial impactor in combination with an ATP bioluminescence detector for in situ rapid estimation of the efficacies of air controlling devices on removal of bioaerosols. Environ Sci Technol 44(5):1742–1746

    Article  CAS  Google Scholar 

  • Zamengo L, Barbiero N, Gregio M, Orrù G (2009) Combined scanning electron microscopy and image analysis to investigate airborne submicron particles: a comparison between personal samplers. Chemosphere 76(3):313–323

    Article  CAS  Google Scholar 

  • Zhao, Y. et al., 2011. Investigation of the efficiencies of bioaerosol samplers for collecting aerosolized bacteria using a fluorescent tracer. I: Effects of non-sampling processes on bacterial culturability. Aerosol Science and Technology, 45(3): 423-431

  • Zhen S et al (2009) A comparison of the efficiencies of a portable BioStage impactor and a reuter centrifugal sampler (RCS) high flow for measuring airborne bacteria and fungi concentrations. J Aerosol Sci 40(6):503–513

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We acknowledge the support provided by the National Natural Science Foundation of China (41630754, 41721091) and the State Key Laboratory of Cryospheric Science (SKLCS-ZZ-2018). Prakriti Sharma Ghimire is supported by a PIFI Fellowship from the Chinese Academy of Sciences (PIFI2018PC20021). Lekhendra Tripathee acknowledges the Chinese Academy of Science for international Young staff support under PIFI (2020FYC0001) program.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shichang Kang.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sharma Ghimire, P., Tripathee, L., Chen, P. et al. Linking the conventional and emerging detection techniques for ambient bioaerosols: a review. Rev Environ Sci Biotechnol 18, 495–523 (2019). https://doi.org/10.1007/s11157-019-09506-z

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11157-019-09506-z

Keywords

Navigation