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. 2018 Feb 3;73:177–208. doi: 10.1016/j.fm.2018.01.003

Table 3.

Survival of foodborne pathogens in manure.

Pathogen Media Concentration inoculated Experimental conditions Main findings References
Escherichia coli 0149 Slurry NS Cattle & pig slurry, Aerated & non-aerated, 18–20 °C, 6–9 °C. 10–14 W, pH (6.9–7.8) Exponential reduction during storage. At both temperatures, inactivation was faster in aerated than in non-aerated slurry batches. Munch et al., 1987
E. coli O157:H7 Bovine feces 103 & 105 cfu/g 5, 22 & 37 °C, pH (6.8–7.4) Survived for up to 70 d, depending on temperature. Wang et al., 1996
E. coli O157:H7 Manure (feces from ruminant animals) 105 - 108 cfu/g pH (7.0 - 9.0), Non aerated ovine manure, aerated ovine manure, and aerated bovine manure, 20, 4, 10, 23, 37, 45 & 70 °C, 100 d Survived for up to 21 months. Kudva et al., 1998
E. coli O26, O111, O157 Bovine feces 101, 103, 105 cfu/g 5, 15 & 25 °C Strains survived for up to 18 W depending on inoculum concentration and temperature. Fukushima et al., 1999
E. coli O157:H7 Cattle manure
Manure slurry
106–108 cfu/g Stored at 4, 20, 37 °C, pH (7.42 at the beginning, 7.10–9.47, by the end) Capable of long term survival. HimathongKham et al., 1999
E. coli O157:H7 Cattle slurry 106 cfu/g Survival in slurry from cattle fed different diets (an entire silage diet & a silage + concentrate diet) was compared. 10 °C, 84 d, pH (7.6 & 7.12) for silage and silage + concentrate respectively. Can persist in slurry for an extended time period. Approximately 3.5–5.5 log reduction in numbers in slurry from cattle fed a silage and cattle fed a silage + concentrate diet respectively over 84 d. McGee et al., 2001
E. coli 11943 (Pig) Farm yard manure NS 50 & 55 °C, 72 h Survival depended on substrate composition, moisture content & duration of incubation. Temperatures in excess of 55 °C for 2 h are required for inactivation. Turner, 2002
E. coli O157:H7 Bovine derived manure 102 - 106 cfu/g Compared the survival of laboratory grown vs bovine derived E. coli O157:H7. 40–50 °C, 50–60 °C, >60 °C, composted in lab scale bioreactors With increase in temperature, survival declined. Hess et al., 2004
E. coli O157:H7 Slaughterhouse waste
Raw & treated sewage
Bovine slurry
107 cfu/cm3 10 °C, pH (4.44–12.42) Gradual decline in cell count in all waste types, long-term storage may be an effective means of reducing pathogen loads in wastes before land application. Avery et al., 2005
E. coli O157 Pig slurries
Cattle slurries
Dirty water
106 cfu/g Laboratory controlled conditions, pH (6.20–7.70, summertime, 5.40–7.73, winter), average waste temperature- 12.4 & 4.3 °C in summer & winter respectively Slow population decline generally. More rapid decline in dirty water than in pig slurry. Season of waste deposition & storage as well as dry matter content of the wastes did not affect the rate of decline. Hutchison et al., 2005
E. coli (non O157:H7, STEC) Cow manure 106–107 cfu/g Survival compared in unturned & turned manure heaps, moisture content- 42% - 76.5% in turned heaps, 77.5%–37% in unturned heaps Capable of long term survival. Fremaux et al., 2007a
E. coli 026 Cow slurry 106 cfu/ml in 15 L of cow slurry pH (8.5–9.5), 113 d Detected for up to 3 months. Capable of survival for an extended period. Fremaux et al., 2007b
E. coli O157:H7 Dairy manure based compost 107 & 105 cfu/g pH (7.9 & 8.0), % moisture content- 63.6 & 56.5, field setting Survived at heap's surface for up to 4 months. Shepherd et al., 2007
E. coli ER2566 Dairy manure 107 cfu/g Ability of black soldier fly (Diptera stratiomyidae) to reduce counts was assessed. The effect of temperature was examined. 72 h, 23, 27, 31, 35 °C Concentrations significantly reduced in all treatments. Better reduction in cells with an increase in temperature. Liu et al., 2008
E. coli O157:H7 Dairy compost 103, 108.4 cfu/g for autoclaved and non autoclaved samples respectively 10–50% moisture levels, greenhouse conditions, ‘room’ temperature, compared sterilized and non-sterilized compost Better growth recorded when background microflora was low. Kim and Jiang 2010
E. coli O157:H7 FYM &
Slurry
107 cfu/g Aerobic and anaerobic conditions compared, 16 °C, 12 d Significantly longer survival under anaerobic conditions compared to aerobic conditions. Effect of anaerobic storage on survival more pronounced in FYM than slurry. Semenov et al., 2011
E. coli O157:H7 (Fresh) dairy compost 107 cfu/g Moisture- 40/50%, 50, 55 & 60 °C Initial moisture levels in compost affects inactivation. Survival for 72, 48 & 24 h in compost with 40% moisture & 72, 24, 24 h in compost with 50% moisture at 50, 55 & 60 °C. Singh et al., 2011
Salmonella (Thompson, Typhimurium, Senftenberg) Litter & dry droppings 1010 cfu/g Effect of ammonia on survival rate was assessed. Moisture % by wt (0–22.0), pH (6.3–8.65) Death rates increased with increase in aw. addition of ammonia accelerated the death rates. Turnbull and Snoeyenbos, 1973
Salmonella Dublin (HWS5I, 859/65, 2415)
Typhimurium (2337/65, A665)
Stanley (S8o4/7)
Choleraesuis (SI346/72)
Choleraesuis var Kunzedorf (S140/72)
Cattle slurry 105, 106 cfu/g pH (7.5) 5, 10, 20 & 30 °C Survived for up to 132 d at 5 °C. Jones, 1976
S. Typhimurium 0035 Cattle slurry 107 cfu/ml 135 d, 4 & 17 °C Reduction in viable numbers during slurry storage period. Kearney et al., 1993
Salmonella Infantis a Fresh slurry 104 cfu/g The effect of aeration on survival was investigated- in laboratory experiemnts and in farm scale slurry tanks. ‘Room temperature’, 6–39.4 °C Sensitive to aeration, exponential decline in aerated slurry within 2–5 W Heinonen-Tanski et al., 1998
Salmonellaa Spent pig litter (partially decomposed pig manure + sawdust) NS Effect of composting on elimination of Salmonella was investigated. Moisture content- 60%, 91 d Temperature has an effect on the elimination of Salmonella from the spent litter. Temperature from 64 to 67 °C sufficiently killed the pathogens during windrow composting. Tiquia et al., 1998
Salmonella Typhimurium Cattle manure
Manure slurry
106–108 cfu/g Stored at 4, 20, 37 °C, pH (7.42 at the beginning, 7.10–9.47, by the end) Population reduction time ranged from 6 d to 3W in manure & 2 d to 5 W in manure slurry HimathongKham et al., 1999
Salmonella Typhimurium, Agona, Hadar, Oranienburg Hog manure 107 cfu/mL 4, 25, 37 °C, ≤ 16 months, pH (7–7.5) Cell numbers declined during storage. At 4 °C, survival was >300 d. Arrus et al., 2006
Salmonella Newport Dairy manure 107.12 cfu/g Used 2 strains- MDR & DS strains, 184 d, pH (6.7), moisture content- 86% Below the detection limit of the direct plating method You et al., 2006
S. Newport Sewage sludge 109 cfu/g 43 h of composting, 60 C, No viable cells detected after composting. Wiley and Westerberg, 1969
Salmonella spp. Dairy compost 101 cfu/g Autoclaved and non-autoclaved compost compared, moisture levels of 10–50% Increase in population within 3 d in autoclaved compost at 40% moisture. No growth in non-autoclaved compost observed. Kim and Jiang 2010
Salmonella Typhimurium FYM & slurry 107 cfu/g Aerobic and anaerobic conditions compared, 16 °C, 12 d No significant difference in survival under aerobic & anaerobic conditions Semenov et al., 2011
Listeria monocytogenes Cattle slurry 108 cfu/ml 84 d, 4/17 °C Decline in viable numbers is temperature dependent. More rapid decline was observed at 17 °C than at 4 °C. Kearney et al., 1993
L. monocytogenes Cattle slurry 106 cfu/g pH (6.9) moisture 12.1% Decline at similar rates during summer and winter. Hutchison et al., 2004
L. monocytogenes Dairy compost 101 cfu/g Initial moisture levels of 10–50%, greenhouse conditions, Increase in population in compost with initial moisture content of 30%. Detected for up to 28 d in all seasons. Temperature, light intensity and moisture affected growth potential & survival. Kim and Jiang, 2010
Campylobacter jejuni Cattle slurry 104 cfu/ml 112 d, 4/17 °C, Storage period was insufficient to reduce viable numbers. Kearney et al., 1993
C. jejuni Biosolids 106, 107, 108 cfu/g 5, 22, 38, 49.5 °C, 62d, pH (5.5–6.3), 3 batches, Cells were sensitive to temperature, Ahmed and Sorensen 1995
C. jejuni Pig slurries
Cattle slurries
Dirty waters
106 cfu/g Laboratory controlled conditions, pH (6.20–7.70, summertime, 5.40–7.73, winter), average waste temperature- 12.4 & 4.3 °C in summer & winter respectively Rapid population decline, not affected by season of waste deposition and storage. Hutchison et al., 2005
Yersinia enterocolitica Cattle slurry 109 cfu/ml 142 d, stored at 4/17 °C Anaerobic digestion had little effect in reducing the viable numbers. Kearney et al., 1993
Y. enterocolitica Biosolids 108, 109 MPN/100g 5, 22, 38, 49.5 °C, aerobic & anaerobic conditions, 62 d Destruction at all temperature profiles, but destruction improved with increase in temperature. Oxygen did not have a significant impact on survival Ahmed and Sorensen, 1995

Key: M- Months, FYM- Farm Yard Manure, h-hours, vs-versus, d-day(s), NS-Not specified.