Comparative performance of three sampling techniques to detect airborne Salmonella species in poultry farms
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Universitat Politècnica de València. Institute of Animal Science and Technology, Valencia, Spain
Instituto Valenciano de Investigaciones Agrarias. Centro de Tecnología Animal, Segorbe, Castellón, Spain
Iowa State University. Department of Agricultural and Biosystems Engineering, Iowa, USA
Universitat Politècnica de València. Department of Biotechnology, Valencia, Spain
Instituto Valenciano de Investigaciuones Agrarias. Centro de Tecnología Animal. Polígono la Esperanza N 100, 12400 Segorbe, Spain.
Universitat Politècnica de València. Institute of Animal Science and Technology, Valencia, Spain.
Ann Agric Environ Med. 2014;21(1):15-24
Sampling techniques to detect airborne Salmonella species (spp.) in two pilot scale broiler houses were compared. Broilers were inoculated at seven days of age with a marked strain of Salmonella enteritidis. The rearing cycle lasted 42 days during the summer. Airborne Salmonella spp. were sampled weekly using impaction, gravitational settling, and impingement techniques. Additionally, Salmonella spp. were sampled on feeders, drinkers, walls, and in the litter. Environmental conditions (temperature, relative humidity, and airborne particulate matter (PM) concentration) were monitored during the rearing cycle. The presence of Salmonella spp. was determined by culture-dependent and molecular methods. No cultivable Salmonella spp. were recovered from the poultry houses’ surfaces, the litter, or the air before inoculation. After inoculation, cultivable Salmonella spp. were recovered from the surfaces and in the litter. Airborne cultivable Salmonella spp. Were detected using impaction and gravitational settling one or two weeks after the detection of Salmonella spp. in the litter. No cultivable Salmonella spp. were recovered using impingement based on culture-dependent techniques. At low airborne concentrations, the use of impingement for the quantification or detection of cultivable airborne Salmonella spp. is not recommended. In these cases, a combination of culture-dependent and culture-independent methods is recommended. These data are valuable to improve current measures to control the transmission of pathogens in livestock environments and for optimising the sampling and detection of airborne Salmonella spp. in practical conditions.
Dungan RS. Board-invited review: Fate and transport of bioaerosols associated with livestock operations and manures. J Anim Sci. 2010; 88: 3693–3706.
Bonlokke JH, Meriaux A, Duchaine C, Godbout S, Cormier Y. Seasonal variations in work-related health effects in swine farm workers. Ann Agric Environ Med. 2009; 16: 43–52.
Donham KJ, Cumro D, Reynolds SJ, Merchant JA. Dose-response relationships between occupational aerosol exposures and cross-shift declines of lung function in poultry workers: Recommendations for exposure limits. J Occup Environ Med. 2000; 42: 260–269.
Zucker BA, Trojan S, Muller W. Airborne gram-negative bacterial flora in animal houses. J Vet Med B Infect Dis Vet Public Health. 2000; 47: 37–46.
Seedorf J, Hartung J, Schroder M, Linkert KH, Phillips VR, Holden MR, et al. Concentrations and emissions of airborne endotoxins and microorganisms in livestock buildings in Northern Europe. J Agr Eng Res. 1998; 70: 97–109.
Radon K, Schulze A, Ehrenstein V, van Strien RT, Praml G, Nowak D. Environmental exposure to confined animal feeding operations and respiratory health of neighboring residents. Epidemiol. 2007; 18: 300–308.
Cox CS, Wathes C. Bioaerosols handbook. C CRC Press. Boca Raton, Florida, U.S.A, 1995.
Adell E, Moset V, Zhao Y, Cerisuelo A, Cambra-López M. Concentración, distribución espacial y por tamaño de bacterias aerobias mesófilas en el aire de granjas de broilers. ITEA-Información técnica económica agraria. 2011; 107: 77–93.
Cambra-López M, Aarnink AJA, Zhao Y, Calvet S, Torres AG. Airborne particulate matter from livestock production systems: A review of an air pollution problem. Environ Pollut. 2010; 58: 1–17.
Nimmermark S, Lund V, Gustafsson G, Eduard W. Ammonia, dust and bacteria in welfare-oriented systems for laying hens. Ann Agric Environ Med. 2009; 16: 103–113.
Just N, Duchaine C, Baljit S. An aerobiological perspective of dust in cage-housed and floor-housed poultry operations. J Occup Med Toxicol. 2009; 4: 13.
Andersson AM, Weis N, Rainey F, Salkinoja-Salonen MS. Dust-borne bacteria in animal sheds, schools and children’s day care centres. J Appl Microbiol. 1999; 86: 622–634.
Curtis SE, Drummond JG, Kelley KW, Grunloh DJ, Meares VJ, Norton HW, Jensen AH. Diurnal and annual fluctuations of aerial bacterial and dust levels in enclosed swine houses. J Anim Sci. 1975; 41: 1502–1511.
Martin WT, Zhang Y, Willson P, Archer TP, Kinahan C, Barber EM. Bacterial and fungal flora of dust deposits in a pig building. Occup Environ Med. 1996; 53: 484–487.
WHO. (2011). World Health Organization. Health topics. Salmonella. (acces: 2012.06.12).
Blaser MJ, Newman LS. A review of human salmonellosis.1. Infective dose. Rev Infect Dis. 1982; 4: 1096–1106.
Davies RH, Breslin M. Observations on Salmonella contamination of commercial laying farms before and after cleaning and disinfection. Vet Rec. 2003; 152: 283–287.
Marin C, Hernandiz A, Lainez M. Biofilm development capacity of Salmonella strains isolated in poultry risk factors and their resistance against disinfectants. Poult Sci. 2009; 88: 424–431.
Chinivasagam HN, Tran L, Maddock L, Gale A, Blackall PJ. Mechanically ventilated broiler sheds: a possible source of aerosolized Salmonella, Campylobacter, and Escherichia coli. Appl Environ Microbiol. 2009; 75: 7417–7425.
Davies, R. H., and M. Breslin. Persistence of Salmonella Enteritidis Phage Type 4 in the environment and arthropod vectors on an empty free-range chicken farm. Environ Microbiol. 2003; 5: 79–84.
Mallinson ET, De Rezende CE, Tablante NL, Carr LE, Joseph SW. A management technique to identify prime locations of Salmonella contamination on broiler and layer farms. J Appl Poultry Res. 2000; 9: 364–370.
Wales A, Breslin M, Davies R. Semiquantitative assessment of the distribution of Salmonella in the environment of caged layer flocks. J Appl Microbiol. 2006; 101: 309–318.
Davis M, Morishita TY. Relative ammonia concentrations, dust concentrations, and presence of Salmonella species and Escherichia coli inside and outside commercial layer facilities. Avian Dis. 2005; 49(1): 30–35.
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.
Blackall PJ, Chinivasagam HN, Ristovski Z. Evaluating risks posed by pathogen and dust emissions from meat chicken sheds. Rural Industries Research and Development Corporation, Australia, 2010.
Eriksson E, Aspan A. Comparison of culture, ELISA and PCR techniques for Salmonella detection in faecal samples for cattle, pig and poultry. BMC Vet Res. 2007; 3: 21.
Gradel KO, Jorgensen JC, Andersen JS, Corry JEL. Laboratory heating studies with Salmonella spp. and Escherichia coli in organic matter, with a view to decontamination of poultry houses. J Appl Microbiol. 2003; 94: 919–928.
Adell E, Moset V, Zhao Y, Jiménez-Belenguer A, Cerisuelo A, Cambra-López M, Detection of airborne Salmonella spp. in poultry farms using impingement: culture-dependent vs. culture-independent methods. In: Proceedings of the 9th International Livestock Environment Symposium (ILES IX). Paper No. 1300. M. Cambra-Lopez, E.F. Wheeler, D. J. Moura, K. Janni, and R.S. Gates (eds.). St. Joseph, Mich.: ASABE.
Peccia J, Hernandez M. Incorporating polymerase chain reaction-based identification, population characterization, and quantification of microorganisms into aerosol science: A review. Atmos Environ. 2006; 40: 3941–3961.
Calvet, S., F. Estellés, M. Cambra-López, A. G. Torres, and H. Van den Weghe. The influence of broiler activity, growth rate and litter on carbon dioxide balances for the determination of ventilation flow rates in broiler production. Poult Sci. 2011; 90: 2449–2458.
ISO 6579:2002. Microbiology of food and animal feeding stuffs. Horizontal methods for the detection of Salmonella spp. International Organization for Standardization, Geneve,Switzerland.
AOAC International. Official methods of analysis of AOAC international. Official Method 945.18. Cereals Adjuncts, 17th ed. 2nd revision. 2003. Association of Analytical Communities, Gaithersburg, MD, USA.
Thorne PS, Kiekhaefer MS, Whitten P, Donham KJ. Comparison of bioaerosol sampling methods in barns housing swine. Appl Environ Microbiol. 1992; 58: 2543–2551.
Aabo S, Rasmussen OF, Rossen L, Sorensen PD, Olsen JE. Salmonella Identification by the Polymerase Chain-Reaction. Mol. Cell. Probes. 1993; 7: 171–178.
SAS. SAS User’s Guide: Statistics. Cary NC. USA, SAS Institute Inc. 2001.
Buttner M, Stetzenbach L. Evaluation of four aerobiological sampling methods for the retrieval of aerosolized pseudomonas syringae. Appl Environ Microbiol. 1991; 57: 1268–1270.
Carrique-Mas JJ, Davies RH. Sampling and bacteriological detection of Salmonella in poultry and poultry premises: a review. Rev Sci Tech OIE. 2008; 27(3): 665–677.
Davies RH, Wray C. Persistence of Salmonella enteritidis in poultry units and poultry food. Br Poult Sci. 1996; 37: 589–596.
Al Homidan A, Robertson JF, Petchey AM. Effect of environmental factors on ammonia and dust production and broiler performance. Br Poult Sci. 1998; 39, 9–10.
Feddes JJ, Emmanuel EJ, Zuidhoft MJ. Broiler performance, body weight variance, feed and water intake, and carcass quality at different stocking densities. Poult Sci. 2002; 81: 774–779.
Tang JW. The effect of environmental parametres on the survival of airborne infectious agents. J Roy Soc Interface. 2009; 6, 737–746.
Zhao Y, Aarnink AJA, De Jong MCM, Ogink NWM, Koerkamp PWGG. Effectiveness of multi-stage scrubbers in reducing emissions of air pollutants from pig houses. Trans ASABE. 2011; 54: 285–293.
Cambra-Lopez M, Hermosilla T, Lai HTL, Aarnink AJA, Ogink NWM. Particulate matter emitted from poultry and pig houses: source identification and quantification. Trans ASABE. 2011; 54: 629–642.
Hayes JR, Car LE,Mallinson ET, Douglas LW, Joseph SW. Characterization of water activity and moisture content to the population distribution of Salmonella spp. in comercial poutry houses. Poult Sci. 2000; 79: 1557–1561.
Lin XJ, Reponen T, Willeke K, Wang Z, Grinshpun SA, Trunov M. Survival of airborne microorganisms during swirling aerosol collection. Aerosol Sci Technol. 2000; 32: 184.
Grinshpun SA, Willeke K, Ulevicius V, Juozaitis A, Terzieva S, Donnelly J, Stelma GN, Brenner KP. Effect of impaction, bounce and reaerosolization on the collection efficiency of impingers. Aerosol Sci Technol. 1997; 26: 326–342.
Brooks JP, McLaughlin MR, Scheffler B, Miles DM. Microbial and antibiotic resistant constituents associated with biological aerosols and poultry litter within a commercial poultry house. Sci Total Environ. 2010; 408(20): 4770–4777.
Gupte AR, de Rezende CLE, Joseph SW. Induction and resuscitation of viable but nonculturable Salmonella enterica serovar typhimurium DT104. Appl Environ Microbiol. 2003; 69: 6669–6675.
Qasem JA, Al Mouqati S, Rajkumar G. Comparison of DNA probe, PCR amplification, ELISA and culture methods for the rapid detection of Salmonella in poultry. In: Makkar H, Viljoen G, editors. Applications of Gene-Based Technologies for Improving Animal Production and Health in Developing Countries. Springer Netherlands; 2005, 529–541.
Lever MS, Williams A. Cross-infection of chicks by airborne transmission of Salmonella enteritidis PT4. Lett Appl Microbiol. 1996; 23(5): 347–349.
Chi MC, Li C-H. Analysis of bioaerosols from chicken houses by culture and non-culture method. Aerosol Sci Technol. 2006; 40, 1071–1079.
Gast RK, Mitchell BW, Holt PS. Evaluation of culture media for detecting airborne Salmonella enteritidis collected with an electrostatic sampling device from the environment of experimentally infected laying hens. Poult Sci. 2004; 83: 1106–1111.
Kwon YM, Woodward CL, Pillai SD, Pena J, Corrier DE, Byrd JA, Ricke SC. Litter and aerosol sampling of chicken houses for rapid detection of Salmonella typhimurium contamination using gene amplification. J Ind Microbiol Biotechnol. 2000; 24: 379–382.
Alvarez A, Buttner M, Stetzenbach L. PCR for bioaerosol monitoring: sensitivity and environmental interference. Appl Environ Microbiol. 1995; 61: 3639–3644.
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. 2011; 3: 177–186.
Hospodsky D, Yamamoto N, Peccia J. Accuracy, precision, and method detection limits of quantitative PCR for airborne bacteria and fungi. Appl Environ Microbiol. 2010; 76: 7004–7012.
Keer JT, Birch L. Molecular methods for the assessment of bacterial viabiliy. J Microbiol Meth. 2003; 53: 175–183.
Stojek NM, Wojcik-Fatla A, Dutkiewicz J. Efficacy of the detection of Legionella in hot and cold water samples by culture and PCR. II. Examination of native samples from various sources. Ann Agric Environ Med. 2012; 19: 295–298.
Kothary MH, Babu US. Infective dose of foodborne pathogens in volunteers: A review. J Food Safety. 2001; 21: 49–68.
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