The effect of urea and ammonia treatments on the survival of Salmonella spp. and Yersinia enterocolitica in pig slurry

D J Bolton, C Ivory, D.A. McDowell

    Research output: Contribution to journalArticle

    6 Citations (Scopus)

    Abstract

    Aims: The objective of this study was to investigate the survival of Salmonella and Yersinia enterocolitica strains in pig slurry and evaluate urea and ammonia as disinfection strategies.Methods and Results: Salmonella Anatum, Salmonella Derby, Salmonella Typhimurium DT19 and Y. enterocolitica bioserotypes 4, O:3, 2, O:5,27 and 1A, O:6,30 were selectively marked by insertion of the plasmid, pGLO encoding for green fluorescent protein and for ampicillin resistance. Strain cocktails were inoculated into fresh pig slurry (control), slurry treated with urea [final concentration 2% w/w, (0.33 mol-1)] and slurry treated with ammonia [final concentration 0.5% w/w, (0.3 mol l-1)] and stored at 4, 14 and 25°C. Bacterial counts were determined at regular intervals on xylose lysine deoxycholate agar (XLD), and XLD supplemented with ampicillin (01mgml1) and arabinose (06mgml1) for Salmonella and cefsulodin-irgasan-novobiocin agar (CIN) and CIN supplemented with ampicillin and arabinose for Y. enterocolitica. The pH of the control-, urea- and ammonia-treated samples ranged from 7.1 to 7.7, 8.8 to 8-9 and 8.0 to 8-3, respectively. Salmonella D4 values ranged from 2.71 to 21.29 days, D14 values from 2.72 to 11.62 days and D25 values from1.76 to 6.85 days. The equivalent D values ranges for the Y. enterocolitica strains were 3.7–19.23, 1.8–16.67 and 1.63–7.09 days, respectively. Treatment significantly (P <0.01) affected D values with control > ammonia > urea, as did incubation temperature; 4 > 14 > 25°C.Conclusions: Urea and to a lesser extent ammonia may be used to disinfect Salmonella and/or Y. enterocolitica-contaminated pig slurry, decreasing the storage time required while increasing its fertilizer value.Significance and Impact of the Study: This study presents data supporting the treatment of pig slurry to kill important zoonotic agents, thereby reducing environmental contamination, cross-infection of other animals and decreasing zoonotic disease in the food chain.
    LanguageEnglish
    Pages134-140
    JournalJournal of Applied Microbiology
    Volume114
    Issue number1
    DOIs
    Publication statusPublished - 2013

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    Yersinia enterocolitica
    pig manure
    Salmonella
    ammonia
    urea
    ampicillin
    cefsulodin
    agar
    deoxycholic acid
    novobiocin
    arabinose
    xylose
    lysine
    Salmonella Anatum
    Salmonella Derby
    cross infection
    reducing agents
    disinfection
    zoonoses
    green fluorescent protein

    Cite this

    @article{c0f9d09a9a4a409c856af5f5747d4db4,
    title = "The effect of urea and ammonia treatments on the survival of Salmonella spp. and Yersinia enterocolitica in pig slurry",
    abstract = "Aims: The objective of this study was to investigate the survival of Salmonella and Yersinia enterocolitica strains in pig slurry and evaluate urea and ammonia as disinfection strategies.Methods and Results: Salmonella Anatum, Salmonella Derby, Salmonella Typhimurium DT19 and Y. enterocolitica bioserotypes 4, O:3, 2, O:5,27 and 1A, O:6,30 were selectively marked by insertion of the plasmid, pGLO encoding for green fluorescent protein and for ampicillin resistance. Strain cocktails were inoculated into fresh pig slurry (control), slurry treated with urea [final concentration 2{\%} w/w, (0.33 mol-1)] and slurry treated with ammonia [final concentration 0.5{\%} w/w, (0.3 mol l-1)] and stored at 4, 14 and 25°C. Bacterial counts were determined at regular intervals on xylose lysine deoxycholate agar (XLD), and XLD supplemented with ampicillin (01mgml1) and arabinose (06mgml1) for Salmonella and cefsulodin-irgasan-novobiocin agar (CIN) and CIN supplemented with ampicillin and arabinose for Y. enterocolitica. The pH of the control-, urea- and ammonia-treated samples ranged from 7.1 to 7.7, 8.8 to 8-9 and 8.0 to 8-3, respectively. Salmonella D4 values ranged from 2.71 to 21.29 days, D14 values from 2.72 to 11.62 days and D25 values from1.76 to 6.85 days. The equivalent D values ranges for the Y. enterocolitica strains were 3.7–19.23, 1.8–16.67 and 1.63–7.09 days, respectively. Treatment significantly (P <0.01) affected D values with control > ammonia > urea, as did incubation temperature; 4 > 14 > 25°C.Conclusions: Urea and to a lesser extent ammonia may be used to disinfect Salmonella and/or Y. enterocolitica-contaminated pig slurry, decreasing the storage time required while increasing its fertilizer value.Significance and Impact of the Study: This study presents data supporting the treatment of pig slurry to kill important zoonotic agents, thereby reducing environmental contamination, cross-infection of other animals and decreasing zoonotic disease in the food chain.",
    author = "Bolton, {D J} and C Ivory and D.A. McDowell",
    note = "Reference text: Allievi, L., Colombi, A., Calcaterra, E. and Ferrari, A. (1994) Inactivation of fecal bacteria in sewage sludge by alkaline treatment. Bioresour Technol 49,25–30. Anon. (2011) The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2009. EFSA J 9, 2090. Arrus, K.M., Holley, R.A., Ominski, K.H., Tenuta, M. and Blank, G. (2006) Influence of temperature on Salmonella survival in hog manure slurry and seasonal temperature profiles in farm manure storage reservoirs. Livest Sci 102, 226–236. Berends, B.R., Urlings, H.A., Snijders, J.M. and van Knapen, F. (1996) Identification and quantification of risk factors in animal management and transport regarding Salmonella spp. in pigs. Int J Food Microbiol 30, 37–53. Boes, J., Alban, L., Bagger, J., Mogelmose, V., Baggensen, D. L. and Olsen, J.E. (2005) Survival of Escherichia coli and Salmonella Typhimurium in slurry applied to clay soil on a Danish swine farm. Prev Vet Med 69, 213–228. Bolton, D.J., Monaghan, A., Byrne, B., Fanning, S., Sweeney, T. and McDowell, D.A. (2011) Incidence and survival of non-O157 verocytotoxigenic Escherichia coli in soil. J Appl Microbiol 111, 484–490. Bottone, E.J. (1997) Yersinia enterocolitica: the charisma continues. Clin Microbiol Rev 10, 257–276. Cardinale, E., Tall, F., Gueye, E.F., Cisse, M. and savat, G. (2004) Risk factors for Campylobacter spp. infection in Senegalese broiler-chicken flocks. Prev Vet Med 64, 15–25. Cote, C., Villeneuve, A., Lessard, L. and Quest, S. (2006) Fate of pathogenic and non-pathogenic microorganisms during storage of liquid hog manure in Quebec. Livest Sci 102, 204–210. Diez-Gonzalez, F., Jarvis, G.N., Adamovich, D.A. and Russel, J. B. (2000) Use of carbonate and alkali to eliminate Escherichia coli from dairy cattle manure. Environ Sci Technol 34, 1275–1279. Guan, T.Y. and Holley, R.A. (2003) Pathogen survival in swine manure environments and transmission of human enteric illness-a review. J Environ Qual 32, 383–392. Himathongkham, S. and Riemann, H. (1999) Destruction of Salmonella Typhimurium, Escherichia coli O157:H7 and Listeria monocytogenes in chicken manure by drying and/ or gassing with ammonia. FEMS Microbiol Lett 171, 179–182. Himathongkham, S., Bahari, S., Riemann, H. and Cliver, D. (1999a) Survival of Escherichia coli O157:H7 and Salmonella Typhimurium in cow manure and cow manure slurry. FEMS Microbiol Lett 178, 251–257. Himathongkham, S., Riemann, H., Bahari, S., Nuanualsuwan, S., Kass, P. and Cliver, D. (1999b) Survival of Salmonella Typhimurium and Escherichia coli O157:H7 in poultry manure and manure slurry at sublethal temperatures. Avian Dis 44, 853–860. Hutchinson, M.L., Walters, L.D., Moore, A. and Avery, S.M. (2005) Declines of zoonotic agents in liquid livestock wastes stored in batches on-farm. J Appl Microbiol 99, 58–65. Kadam, P.C. and Boone, D.R. (1996) Influence of pH on ammonia accumulation and toxicity in halophilic, methylotrophic methanogens. Appl Environ Microbiol 62, 4486–4492. Letourneau, V., Duchaine, C., Cote, C., Letellier, A., Topp, E. and Masse, D. (2010) Presence of zoonotic pathogens in physico-chemically characterized manures from hog finishing houses using different production systems. Bioresour Technol 101, 4048–4055. Mead, P.S., Slutsker, L., Dietz, V., McCraig, L.F., Bresse, J.S., Shapiro, C., Griffin, P.M. and Tauxe, R.V. (1999) Food related illness and death in the United Sates. Emerg Infect Dis 5, 607–625. Nesbakken, T. (2005) Yersinia enterocolitica.In Foodborne Pathogens. Microbiology and Molecular Epidemiology ed. Fratamico, P.M., Bhunia, A.K. and Smith, J.L. pp. 227–249. Wymondham, UK: Caister Academic Press. Nicholson, F.A., Groves, S.J. and Chambers, B.J. (2005) Pathogen survival during livestock manure storage and following land application. Bioresour Technol 96, 135–143. Ottoson, J., Nordin, A., von Rosen, D. and Vinneras, B. (2008) Salmonella reduction in manure by addition of urea and ammonia. Bioresour Technol 99, 1610–1615. Panetta, D.M., Powers, W.J. and Lorimor, J.C. (2005) Management strategy impacts on ammonia volatilization from swine manure. J Environ Qual 34, 1119–1130. Park, G.W. and Diez-Gonzalez, F. (2003) Utilisation of carbonate and ammonia-based treatments to eliminate Escherichia coli O157:H7 and Salmonella Typhimurium DT104 from cattle manure. J Appl Microbiol 94, 675–685. Park, J.I., Yun, Y. and Park, J.M. (2002) Long term operation of slurry bioreactor for decomposition of food wastes. Bioresour Technol 84, 101–104. Placha, I., Venglovsky, J., Saskova, N. and Svoboda, I.F. (2001) The effect of Summer and Winter seasons on the survival of Salmonella Typhimurium and indicator microorganisms during the storage of solid fraction of pig slurry. J Appl Microbiol 91, 1036–1043. Poljak, Z., Dewey, C.E., Martin, S.W., Rosendal, T., Christensen, J., Cieben, B. and Friendship, R.M. (2010) Prevalence of Yersinia enteriocolitica shedding and bioserotype distribution in Ontario finisher pig herds in 2001, 2002 and 2004. Prev Vet Med 93, 110–120. Pratt, E.V., Rose, S.P. and Keeling, A.A. (2002) Effect of ambient temperature on losses of volatile nitrogen compounds from stored laying hen manure. Bioresour Technol 84, 203–205. Smith, K.A., brewer, A.J., Dauven, A. and Wilson, D.W. (2000) A survey of the production and use of animal manures in England and Wales. I. Pig manure. Soil Use Manage 16, 124–132. Smith, K.A., brewer, A.J., Dauven, A. and Wilson, D.W. (2001) A survey of the production and use of animal manures in England and Wales. III. Cattle manures. Soil Use Manage 17,77–87. Strauch, D. and Ballarini, G. (1994) Hygienic aspects of the production and agricultural use of animal wastes. J Vet Med 41, 176–228. Van Pelt, W. and Valkenburgh, S.M. (2001) Zoonoses and zoonotic agents in humans, food, animals and feed in the Netherlands. Available at: www.keuringsdienstvanwaren.nl [Accessed 18 April 2012]. Veling, J., Wilpshaar, H., Frankena, K., Bartels, C. and Barkema, H.W. (2002) Risk factors for clinical Salmonella enterica subsp. enterica serovar Typhimurium infection on Dutch dairy farms. Prev Vet Med 54, 157–168. Vinneras, B., Bjorklund, A. and Jonsson, H. (2003) Thermal composting of faecal matter as treatment and possible disinfection method – laboratory-scale and pilot-scale studies. Bioresour Technol 88,47–54.",
    year = "2013",
    doi = "10.1111/jam.12003",
    language = "English",
    volume = "114",
    pages = "134--140",
    journal = "Journal of Applied Microbiology",
    issn = "1364-5072",
    number = "1",

    }

    The effect of urea and ammonia treatments on the survival of Salmonella spp. and Yersinia enterocolitica in pig slurry. / Bolton, D J; Ivory, C; McDowell, D.A.

    In: Journal of Applied Microbiology, Vol. 114, No. 1, 2013, p. 134-140.

    Research output: Contribution to journalArticle

    TY - JOUR

    T1 - The effect of urea and ammonia treatments on the survival of Salmonella spp. and Yersinia enterocolitica in pig slurry

    AU - Bolton, D J

    AU - Ivory, C

    AU - McDowell, D.A.

    N1 - Reference text: Allievi, L., Colombi, A., Calcaterra, E. and Ferrari, A. (1994) Inactivation of fecal bacteria in sewage sludge by alkaline treatment. Bioresour Technol 49,25–30. Anon. (2011) The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2009. EFSA J 9, 2090. Arrus, K.M., Holley, R.A., Ominski, K.H., Tenuta, M. and Blank, G. (2006) Influence of temperature on Salmonella survival in hog manure slurry and seasonal temperature profiles in farm manure storage reservoirs. Livest Sci 102, 226–236. Berends, B.R., Urlings, H.A., Snijders, J.M. and van Knapen, F. (1996) Identification and quantification of risk factors in animal management and transport regarding Salmonella spp. in pigs. Int J Food Microbiol 30, 37–53. Boes, J., Alban, L., Bagger, J., Mogelmose, V., Baggensen, D. L. and Olsen, J.E. (2005) Survival of Escherichia coli and Salmonella Typhimurium in slurry applied to clay soil on a Danish swine farm. Prev Vet Med 69, 213–228. Bolton, D.J., Monaghan, A., Byrne, B., Fanning, S., Sweeney, T. and McDowell, D.A. (2011) Incidence and survival of non-O157 verocytotoxigenic Escherichia coli in soil. J Appl Microbiol 111, 484–490. Bottone, E.J. (1997) Yersinia enterocolitica: the charisma continues. Clin Microbiol Rev 10, 257–276. Cardinale, E., Tall, F., Gueye, E.F., Cisse, M. and savat, G. (2004) Risk factors for Campylobacter spp. infection in Senegalese broiler-chicken flocks. Prev Vet Med 64, 15–25. Cote, C., Villeneuve, A., Lessard, L. and Quest, S. (2006) Fate of pathogenic and non-pathogenic microorganisms during storage of liquid hog manure in Quebec. Livest Sci 102, 204–210. Diez-Gonzalez, F., Jarvis, G.N., Adamovich, D.A. and Russel, J. B. (2000) Use of carbonate and alkali to eliminate Escherichia coli from dairy cattle manure. Environ Sci Technol 34, 1275–1279. Guan, T.Y. and Holley, R.A. (2003) Pathogen survival in swine manure environments and transmission of human enteric illness-a review. J Environ Qual 32, 383–392. Himathongkham, S. and Riemann, H. (1999) Destruction of Salmonella Typhimurium, Escherichia coli O157:H7 and Listeria monocytogenes in chicken manure by drying and/ or gassing with ammonia. FEMS Microbiol Lett 171, 179–182. Himathongkham, S., Bahari, S., Riemann, H. and Cliver, D. (1999a) Survival of Escherichia coli O157:H7 and Salmonella Typhimurium in cow manure and cow manure slurry. FEMS Microbiol Lett 178, 251–257. Himathongkham, S., Riemann, H., Bahari, S., Nuanualsuwan, S., Kass, P. and Cliver, D. (1999b) Survival of Salmonella Typhimurium and Escherichia coli O157:H7 in poultry manure and manure slurry at sublethal temperatures. Avian Dis 44, 853–860. Hutchinson, M.L., Walters, L.D., Moore, A. and Avery, S.M. (2005) Declines of zoonotic agents in liquid livestock wastes stored in batches on-farm. J Appl Microbiol 99, 58–65. Kadam, P.C. and Boone, D.R. (1996) Influence of pH on ammonia accumulation and toxicity in halophilic, methylotrophic methanogens. Appl Environ Microbiol 62, 4486–4492. Letourneau, V., Duchaine, C., Cote, C., Letellier, A., Topp, E. and Masse, D. (2010) Presence of zoonotic pathogens in physico-chemically characterized manures from hog finishing houses using different production systems. Bioresour Technol 101, 4048–4055. Mead, P.S., Slutsker, L., Dietz, V., McCraig, L.F., Bresse, J.S., Shapiro, C., Griffin, P.M. and Tauxe, R.V. (1999) Food related illness and death in the United Sates. Emerg Infect Dis 5, 607–625. Nesbakken, T. (2005) Yersinia enterocolitica.In Foodborne Pathogens. Microbiology and Molecular Epidemiology ed. Fratamico, P.M., Bhunia, A.K. and Smith, J.L. pp. 227–249. Wymondham, UK: Caister Academic Press. Nicholson, F.A., Groves, S.J. and Chambers, B.J. (2005) Pathogen survival during livestock manure storage and following land application. Bioresour Technol 96, 135–143. Ottoson, J., Nordin, A., von Rosen, D. and Vinneras, B. (2008) Salmonella reduction in manure by addition of urea and ammonia. Bioresour Technol 99, 1610–1615. Panetta, D.M., Powers, W.J. and Lorimor, J.C. (2005) Management strategy impacts on ammonia volatilization from swine manure. J Environ Qual 34, 1119–1130. Park, G.W. and Diez-Gonzalez, F. (2003) Utilisation of carbonate and ammonia-based treatments to eliminate Escherichia coli O157:H7 and Salmonella Typhimurium DT104 from cattle manure. J Appl Microbiol 94, 675–685. Park, J.I., Yun, Y. and Park, J.M. (2002) Long term operation of slurry bioreactor for decomposition of food wastes. Bioresour Technol 84, 101–104. Placha, I., Venglovsky, J., Saskova, N. and Svoboda, I.F. (2001) The effect of Summer and Winter seasons on the survival of Salmonella Typhimurium and indicator microorganisms during the storage of solid fraction of pig slurry. J Appl Microbiol 91, 1036–1043. Poljak, Z., Dewey, C.E., Martin, S.W., Rosendal, T., Christensen, J., Cieben, B. and Friendship, R.M. (2010) Prevalence of Yersinia enteriocolitica shedding and bioserotype distribution in Ontario finisher pig herds in 2001, 2002 and 2004. Prev Vet Med 93, 110–120. Pratt, E.V., Rose, S.P. and Keeling, A.A. (2002) Effect of ambient temperature on losses of volatile nitrogen compounds from stored laying hen manure. Bioresour Technol 84, 203–205. Smith, K.A., brewer, A.J., Dauven, A. and Wilson, D.W. (2000) A survey of the production and use of animal manures in England and Wales. I. Pig manure. Soil Use Manage 16, 124–132. Smith, K.A., brewer, A.J., Dauven, A. and Wilson, D.W. (2001) A survey of the production and use of animal manures in England and Wales. III. Cattle manures. Soil Use Manage 17,77–87. Strauch, D. and Ballarini, G. (1994) Hygienic aspects of the production and agricultural use of animal wastes. J Vet Med 41, 176–228. Van Pelt, W. and Valkenburgh, S.M. (2001) Zoonoses and zoonotic agents in humans, food, animals and feed in the Netherlands. Available at: www.keuringsdienstvanwaren.nl [Accessed 18 April 2012]. Veling, J., Wilpshaar, H., Frankena, K., Bartels, C. and Barkema, H.W. (2002) Risk factors for clinical Salmonella enterica subsp. enterica serovar Typhimurium infection on Dutch dairy farms. Prev Vet Med 54, 157–168. Vinneras, B., Bjorklund, A. and Jonsson, H. (2003) Thermal composting of faecal matter as treatment and possible disinfection method – laboratory-scale and pilot-scale studies. Bioresour Technol 88,47–54.

    PY - 2013

    Y1 - 2013

    N2 - Aims: The objective of this study was to investigate the survival of Salmonella and Yersinia enterocolitica strains in pig slurry and evaluate urea and ammonia as disinfection strategies.Methods and Results: Salmonella Anatum, Salmonella Derby, Salmonella Typhimurium DT19 and Y. enterocolitica bioserotypes 4, O:3, 2, O:5,27 and 1A, O:6,30 were selectively marked by insertion of the plasmid, pGLO encoding for green fluorescent protein and for ampicillin resistance. Strain cocktails were inoculated into fresh pig slurry (control), slurry treated with urea [final concentration 2% w/w, (0.33 mol-1)] and slurry treated with ammonia [final concentration 0.5% w/w, (0.3 mol l-1)] and stored at 4, 14 and 25°C. Bacterial counts were determined at regular intervals on xylose lysine deoxycholate agar (XLD), and XLD supplemented with ampicillin (01mgml1) and arabinose (06mgml1) for Salmonella and cefsulodin-irgasan-novobiocin agar (CIN) and CIN supplemented with ampicillin and arabinose for Y. enterocolitica. The pH of the control-, urea- and ammonia-treated samples ranged from 7.1 to 7.7, 8.8 to 8-9 and 8.0 to 8-3, respectively. Salmonella D4 values ranged from 2.71 to 21.29 days, D14 values from 2.72 to 11.62 days and D25 values from1.76 to 6.85 days. The equivalent D values ranges for the Y. enterocolitica strains were 3.7–19.23, 1.8–16.67 and 1.63–7.09 days, respectively. Treatment significantly (P <0.01) affected D values with control > ammonia > urea, as did incubation temperature; 4 > 14 > 25°C.Conclusions: Urea and to a lesser extent ammonia may be used to disinfect Salmonella and/or Y. enterocolitica-contaminated pig slurry, decreasing the storage time required while increasing its fertilizer value.Significance and Impact of the Study: This study presents data supporting the treatment of pig slurry to kill important zoonotic agents, thereby reducing environmental contamination, cross-infection of other animals and decreasing zoonotic disease in the food chain.

    AB - Aims: The objective of this study was to investigate the survival of Salmonella and Yersinia enterocolitica strains in pig slurry and evaluate urea and ammonia as disinfection strategies.Methods and Results: Salmonella Anatum, Salmonella Derby, Salmonella Typhimurium DT19 and Y. enterocolitica bioserotypes 4, O:3, 2, O:5,27 and 1A, O:6,30 were selectively marked by insertion of the plasmid, pGLO encoding for green fluorescent protein and for ampicillin resistance. Strain cocktails were inoculated into fresh pig slurry (control), slurry treated with urea [final concentration 2% w/w, (0.33 mol-1)] and slurry treated with ammonia [final concentration 0.5% w/w, (0.3 mol l-1)] and stored at 4, 14 and 25°C. Bacterial counts were determined at regular intervals on xylose lysine deoxycholate agar (XLD), and XLD supplemented with ampicillin (01mgml1) and arabinose (06mgml1) for Salmonella and cefsulodin-irgasan-novobiocin agar (CIN) and CIN supplemented with ampicillin and arabinose for Y. enterocolitica. The pH of the control-, urea- and ammonia-treated samples ranged from 7.1 to 7.7, 8.8 to 8-9 and 8.0 to 8-3, respectively. Salmonella D4 values ranged from 2.71 to 21.29 days, D14 values from 2.72 to 11.62 days and D25 values from1.76 to 6.85 days. The equivalent D values ranges for the Y. enterocolitica strains were 3.7–19.23, 1.8–16.67 and 1.63–7.09 days, respectively. Treatment significantly (P <0.01) affected D values with control > ammonia > urea, as did incubation temperature; 4 > 14 > 25°C.Conclusions: Urea and to a lesser extent ammonia may be used to disinfect Salmonella and/or Y. enterocolitica-contaminated pig slurry, decreasing the storage time required while increasing its fertilizer value.Significance and Impact of the Study: This study presents data supporting the treatment of pig slurry to kill important zoonotic agents, thereby reducing environmental contamination, cross-infection of other animals and decreasing zoonotic disease in the food chain.

    U2 - 10.1111/jam.12003

    DO - 10.1111/jam.12003

    M3 - Article

    VL - 114

    SP - 134

    EP - 140

    JO - Journal of Applied Microbiology

    T2 - Journal of Applied Microbiology

    JF - Journal of Applied Microbiology

    SN - 1364-5072

    IS - 1

    ER -