RESEARCH PAPER
Airborne virus sampling: Efficiencies of samplers and their detection limits for infectious bursal disease virus (IBDV)
 
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1
Wageningen UR Livestock Research, Wageningen, The Netherlands
 
2
Department of Agricultural and Biosystems Engineering, Iowa State University, USA
 
3
Animal Health Service (GD), Deventer, The Netherlands
 
4
Farm Technology Group, Wageningen University, The Netherlands
 
5
Quantitative Veterinary Epidemiology, Wageningen University, The Netherlands
 
 
Corresponding author
Andre J.A. Aarnink   

Wageningen UR Livestock Research, Wageningen, The Netherlands
 
 
Ann Agric Environ Med. 2014;21(3):464-471
 
KEYWORDS
ABSTRACT
Introduction:
The airborne transmission of infectious diseases in livestock production is increasingly receiving research attention. Reliable techniques of air sampling are crucial to underpin the findings of such studies. This study evaluated the physical and biological efficiencies and detection limits of four samplers (Andersen 6-stage impactor, all-glass impinger “AGI-30”, OMNI-3000 and MD8 with gelatin filter) for collecting aerosols of infectious bursal disease virus (IBDV).

Material and Methods:
IBDV aerosols mixed with a physical tracer (uranine) were generated in an isolator, and then collected by the bioaerosol samplers. Samplers’ physical and biological efficiencies were derived based on the tracer concentration and the virus/tracer ratio, respectively. Detection limits for the samplers were estimated with the obtained efficiency data.

Results:
Physical efficiencies of the AGI-30 (96%) and the MD8 (100%) were significantly higher than that of the OMNI-3000 (60%). Biological efficiency of the OMNI-3000 (23%) was significantly lower than 100% (P<0.01), indicating inactivation of airborne virus during sampling. The AGI-30, the Andersen impactor and the MD8 did not significantly inactivate virus during sampling. The 2-min detection limits of the samplers on airborne IBDV were 4.1 log10 50% egg infective dose (EID50) m-3 for the Andersen impactor, 3.3 log10 EID50 m-3 for the AGI-30, 2.5 log10 EID50 m-3 for the OMNI-3000, and 2.9 log10 EID50 m-3 for the MD8. The mean half-life of IBDV aerosolized at 20°C and 70% was 11.9 min.

Conclusions:
Efficiencies of different samplers vary. Despite its relatively low sampling efficiency, the OMNI-3000 is suitable for use in environments with low viral concentrations because its high flow rate gives a low detection limit. With the 4 samplers investigated, negative air samples cannot guarantee virus-free aerial environments, which means that transmission of infectious agents between farms may still occur even when no virus has been detected.

 
REFERENCES (46)
1.
Gloster J, Champion HJ, Sorensen JH, Mikkelsen T, Ryall DB, Astrup P, et al. Airborne transmission of foot-and-mouth disease virus from Burnside Farm, Heddonon-the-Wall, Northumberland, during the 2001 epidemic in the United Kingdom. Vet Rec. 2003; 152(17): 525–533.
 
2.
Mikkelsen T, Alexandersen S, Astrup P, Champion HJ, Donaldson AI, Dunkerley FN, et al. Investigation of airborne foot-and-mouth disease virus transmission during low-wind conditions in the early phase of the UK 2001 epidemic. Atmos Chem Phys. 2003; 3(6): 2101–2110.
 
3.
Gloster J, Alexandersen S. New directions: Airborne transmission of Foot-and-mouth disease virus. Atmos Environ. 2004; 38(3): 503–505.
 
4.
Hugh-Jones M, Allan WH, Dark FA, Harper GJ. The evidence for the airborne spread of Newcastle disease. J Hyg. 1973; 71(2): 325–39.
 
5.
Kristensen CS, Botner A, Takai H, Nielsen JP, Jorsal SE. Experimental airborne transmission of PRRS virus. Vet Microbiol. 2004; 99(3/4): 197–202.
 
6.
Kitching RP, Thrusfield MV, Taylor NM. Use and abuse of mathematical models: an illustration from the 2001 foot and mouth disease epidemic in the United Kingdom. Rev Sci Tech Off Int Epiz. 2006; 25(1): 293–311.
 
7.
Zhen S, Li K, Yin L, Yao M, Zhang H, Chen L, et al. 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. 2009; 40(6): 503–513.
 
8.
Mainelis G, Berry D, Reoun An H, Yao M, DeVoe K, Fennell DE, et al. Design and performance of a single-pass bubbling bioaerosol generator. Atmos Environ. 2005; 39(19): 3521–3533.
 
9.
Yao M, Mainelis G. Analysis of portable impactor performance for enumeration of viable bioaerosols. J Occup Environ Hyg. 2007; 4(7): 514–524.
 
10.
Engelhart S, Glasmacher A, Simon A, Exner M. Air sampling of Aspergillus fumigatus and other thermotolerant fungi: Comparative performance of the Sartorius MD8 airport and the Merck MAS-100 portable bioaerosol sampler. J Hyg. 2007; 210(6): 733–739.
 
11.
Thorne PS, Kiekhaefer MS, Whitten P, Donham KJ. Comparison of bioaerosol sampling methods in barns housing swine. Appl Environ Microbiol. 1992; 58(8): 2543–2551.
 
12.
Thompson MW, Donnelly J, Grinshpun SA, Juozaitis A, Willeke K. Method and test system for evaluation of bioaerosol samplers. J Aerosol Sci. 1994; 25(8): 1579–1593.
 
13.
Tseng CC, Li CS. Collection efficiencies of aerosol samplers for virus-containing aerosols. J Aerosol Sci. 2005; 36(5–6): 593–607.
 
14.
Yao MH, Mainelis G. Effect of physical and biological parameters on enumeration of bioaerosols by portable microbial impactors. J Aerosol Sci. 2006; 37(11): 1467–1483.
 
15.
Xu Z, Wu Y, Shen F, Chen Q, Tan M, Yao M. Bioaerosol science, technology, and engineering: Past, present, and future. Aerosol Sci Tech. 2011; 45(11): 1337–1349.
 
16.
Oliveira CJB, Carvalho LFOS, Garcia TB. Experimental airborne transmission of Salmonella Agona and Salmonella Typhimurium in weaned pigs. Epidemiol Infect. 2006; 134(1): 199–209.
 
17.
Zhao Y, Aarnink AJA, Groot Koerkamp PWG, Hagenaars TJ, Katsma WEA, de Jong MCM. Detection of airborne Campylobacter with three bioaerosol samplers for alarming bacteria transmission in broilers. Biol Eng T. 2011; 3(4): 177–186.
 
18.
Seedorf J. Emissions and dispersion of livestock-related biological aerosols: An overview. In: Dustconf J. How to Improve Air Quality. Maastricht 2007.
 
19.
VDI 4251 Part1: Measurement of airborne microorganisms and viruses in ambient air – Planning of plant-related ambient air measurements – Plume measurement. Verein Deutscher Ingenieure, Editor 2007.p.58.
 
20.
Wang P. A single hit model of polymicrobial sepsis: Cecal ligation and puncture. Sepsis 1998; 2(3): 227–233.
 
21.
Andersen AA. New sampler for the collection, sizing, and enumeration of viable airborne particles. J Bacteriol. 1958; 76(5): 471–484.
 
22.
Zhao Y, Aarnink AJA, Cambra-Lopez M, Fabri T. Viral shedding and emission of airborne infectious bursal disease virus from a broiler room. Br Poultry Sci 2013 (in press); doi: 10.1080/00071668.2012.762505.
 
23.
Spearman C. The method of right and wrong cases (constant stimuli) without Gauss’s formulae. Brit J Psychol. 1908; 2(3): 227–242.
 
24.
Hoekstra JA. Estimation of the LC50, a review. Environmetrics 1991; 2(2): 139–152.
 
25.
Schuijffel DF, Van Empel PCM, Pennings A, Van Putten JPM, Nuijten PJM. Successful selection of cross-protective vaccine candidates for Ornithobacterium rhinotracheale infection. Infect Immun. 2005; 73(10): 6812–6821.
 
26.
Marangon S, Busani L. The use of vaccination in poultry production . Rev Sci Tech Off Int Epiz. 2007; 26(1): 265–274.
 
27.
Zhao Y, Aarnink AJA, Doornenbal P, Huynh TTT, Groot Koerkamp PWG, Landman WJ, et al. Investigation of the efficiencies of bioaerosol samplers for collecting aerosolized bacteria using a fluorescent tracer. II: Sampling efficiency, and half-life time . Aerosol Sci Tech. 2011; 45(3): 432–442.
 
28.
Burton NC, Grinshpun SA, Reponen T. Physical collection efficiency of filter materials for bacteria and viruses . Ann Occup Hyg. 2007; 51(2): 143–151.
 
29.
Tang JW. The effect of environmental parameters on the survival of airborne infectious agents. J R Soc Interface. 2009; 6(S6): 737–746.
 
30.
Zhao Y, Aarnink AJA, Dijkman R, Teun F, de Jong MCM, Groot Koerkamp PWG. Effect of temperature, relative humidity, absolute humidity and evaporation potential on survival of airborne Gumboro vaccine virus. Appl Environ Microbiol. 2012; 78(4): 1048–1054.
 
31.
Reponen T, Willeke K, Ulevicius V, Grinshpun SA, Donnelly J. Techniques for dispersion of microorganisms into air. Aerosol Sci Tech. 1997; 27(3): 405–421.
 
32.
Zhao Y, Aarnink AJA, de Jong MCM, Ogink NWM, Groot Koerkamp PWG. Effectiveness of multi-stage scrubbers in reducing emissions of air pollutants from pig houses. T ASABE. 2011; 54(1): 285–293.
 
33.
Lundholm IM. Comparison of methods for quantitative determinations of airborne bacteria and evaluation of total viable counts. Appl Environ Microbiol. 1982; 44(1): 179–183.
 
34.
Zhao Y, Aarnink AJA, Doornenbal P, Huynh TTT, Groot Koerkamp PWG, de Jong MCM, et al. 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 Sci Tech. 2011; 45(3): 423–431.
 
35.
Terzieva S, Donnelly J, Ulevicius V, Grinshpun SA, Willeke K, Stelma GN, et al. Comparison of methods for detection and enumeration of airborne microorganisms collected by liquid impingement. Appl Environ Microbiol. 1996; 62(7): 2264–2272.
 
36.
Nevalainen A, Pastuzska J, Liebhaber F, Willeke K. Performance of bioaerosol samplers: collection characteristics and sampler design considerations. Atmos Environ. 1992; 26A(4): 531–540.
 
37.
Kesavan JS, Schepers DR. Characteristics and sampling efficiencies of OMNI 3000 aerosol samplers. Edgewood Chemical Biological Center, Maryland 2006.
 
38.
Burton NC, Adhikari A, Grinshpun SA, Hornung R, Reponen T. The effect of filter material on bioaerosol collection of Bacillus subtilis spores used as a Bacillus anthracis simulant. J Environ Monitor. 2005; 7(5): 475–480.
 
39.
Lin XJ, Willeke K, Ulevicius V, Grinshpun SA. Effect of sampling time on the collection efficiency of all-glass impingers . Am Ind Hyg Assoc J. 1997; 58(7): 480–488.
 
40.
Stewart SL, Grinshpun SA, Willeke K, Terzieva S, Ulevicius V, Donnelly J. Effect of impact stress on microbial recovery on an agar surface . Appl Environ Microbiol. 1995; 61(4): 1232–1239.
 
41.
Landman WJM, van Eck JHH. Aerosolization of Newcastle disease vaccine virus and Enterococcus faecalis. Avian Dis. 2001; 45(3): 684–687.
 
42.
Sattar SA, Ijaz MK, Johnson-Lussenburg CM, Springthorpe VS. Effect of relative humidity on the airborne survival of Rotavirus SA11. Appl Environ Microbiol. 1984; 47(4): 879–881.
 
43.
Larson EW, Dominik JW, Slone TW. Aerosol stability and respiratory infectivity of Japanese B encephalitis virus. Infect Immun. 1980; 30(2): 397–401.
 
44.
Spackman E, Senne DA, Myers TJ, Bulaga LL, Garber LP, Perdue ML, et al. Development of a real-time reverse transcriptase PCR assay for type A influenza virus and the avian H5 and H7 hemagglutinin subtypes. J Clin Microbiol. 2002; 40(9): 3256–3260.
 
45.
Tumpey TM, Basler CF, Aguilar PV, Zeng H, Solórzano A, Swayne DE, et al. Characterization of the reconstructed 1918 Spanish influenza pandemic virus. Science. 2005; 310(5745): 77–80.
 
46.
Tompkins SM, Lo CY, Tumpey TM, Epstein SL. Protection against lethal influenza virus challenge by RNA interference in vivo . PNAS. 2004; 101(23): 8682–8686.
 
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