Factors affecting survival of pathogens in soil systems – last updated 7/13/2012
Adherence/detachment of pathogens to soil particles
Attachment of most E. coli cells to soil
at the surface occurred very quickly
Ross, C.M. and A.M. Donnison. 2006. Campylobacter jejuni inactivation in New Zealand soils.
J. Appl. Microbiol. 101:1188-1197.
Fenlon, D.R., I.D. Ogden, A. Vinten, and I. Svoboda. 2000. The fate of Escherichia coli and E.
coli O157 in cattle slurry after application to land. J. Appl. Microbiol. Symp. Suppl. 88:149S156S.
Chandler, D.S. and J.A. Craven. 1978. Environmental factors affecting Escherichia coli and
Salmonella typhimurium numbers on land used for effluent disposal. Aust. J. Agric. Res. 29:577585.
Heterogeneity within the E. coli
community exists as to their attachment
strength to soil particles.
Foppen, J.W., M. van Herwerden, and J. Schijven. 2007. Transport of Escherichia coli in
saturated porous media: Dual mode deposition and intra-population heterogeneity. Water Res.
41:1743-1753.
Adherence and transport not based on
hydrophobicity nor surface charge,
however, pathogen size, including width
and shape, are dominant factors
Bolster, C.H., B.Z. Haznedaroglu, and S.L. Walker. 2009. Diversity in cell properties and
transport behavior among 12 different environmental Escherichia coli isolates. J. Environ. Qual.
38:465-472.
Ferguson, C.M., C.M. Davies, C. Kaucner, M. Krogh, J. Rodehutskors, D.A. Deere, and N.J.
Ashbolt. 2007. Field scale quantification of microbial transport from bovine feces under
simulated rainfall events. J. Wat. Hlth. 5:83-95.
Detachment of pathogen cells from soil
particles is minimal and coincides with
rainfall events
Ross, C.M. and A.M. Donnison. 2006. Campylobacter jejuni inactivation in New Zealand soils.
J. Appl. Microbiol. 101:1188-1197.
Fenlon, D.R., I.D. Ogden, A. Vinten, and I. Svoboda. 2000. The fate of Escherichia coli and E.
coli O157 in cattle slurry after application to land. J. Appl. Microbiol. Symp. Suppl. 88:149S156S.
Vinton, A.J.A., D.R. Lewis, D.R. Fenlon, K.A. Leach, R. Howard, I. Svoboda, and I. Ogden.
2002. Fate of Escherichia coli and Escherichia coli O157 in soils and drainage water following
cattle slurry application at 3 sites in southern Scotland. Soil Use Manag. 18:223-231.
Chandler, D.S. and J.A. Craven. 1978. Environmental factors affecting Escherichia coli and
Salmonella typhimurium numbers on land used for effluent disposal. Aust. J. Agric. Res. 29:577585.
Leaching or movement of pathogens
through soil is dependent on the
presence and type (solid vs liquid) of
organic matter as well as pathogen type
Forslund, A., F. Plauborg, M.N. Andersen, B. Markussen, and A. Dalsgaard. 2011. Leaching of
human pathogens in repacked soil lysimeters and contamination of potato tubers under
subsurface drip irrigation in Denmark. Water Res. 45:4367-4380.
Soupir, M.L., S. Mostaghimi, and T. Dillaha. 2010. Attachment of Escherichia coli and
enterococci to particles in runoff. J. Environ. Qual. 39:1019-1027.
Horswell, J., J. Hewitt, J. Prosser, A. Van Schaik, D. Croucher, C. Macdonald, P. Burford, P.
Susaria, P. Bickers, and T. Speir. 2010. Mobility and survival of Salmonella Typhimurium and
human adenovirus from spiked sewage sludge applied to soil columns. J. Appl. Microbiol.
108:104-114.
Hodgon, C.J., N. Bulmer, D.R. Chadwick, D.M. Oliver, A.L. Heathwaite, R.D. Fish, and M.
Winter. 2009. Establishing relative release kinetics of faecal indicator organisms from different
fecal matrices. Lett. Appl. Microbiol. 49:124-130.
Semenov, A.V., L. van Overbeek, and A.H.C. van Bruggen. 2009. Percolation and survival of
Escherichia coli O157:H7 and Salmonella enterica serovar Typhimurium in soil amended with
contaminated dairy manure or slurry. Appl. Environ. Microbiol. 75:3206-3215.
Active pathogen motility within soil
matrix is influenced by nutrient
availability such that densities in
rhizosphere soil will be greater than bulk
soil when nutrients are limiting in bulk
soil.
Guber, A.K., J.S. Karns, Y.A. Pachepsky, A.M. Sadeghi, J.S. Van Kessel, and T.H. Dao. 2007.
Comparison of release and transport of manure-borne Escherichia coli and enterococci under
grass buffer conditions. Lett. Appl. Microbiol. 44:161-167.
Kearney, T.E., M.J. Larkin, and P.N. Levett. 1993. The effect of slurry storage and anaerobic
digestion on survival of pathogenic bacteria. J. Appl. Bacteriol. 74:86-93.
Semenov, A.V., L. van Overbeek, and A.H.C. van Bruggen. 2009. Percolation and survival of
Escherichia coli O157:H7 and Salmonella enterica serovar Typhimurium in soil amended with
contaminated dairy manure or slurry. Appl. Environ. Microbiol. 75:3206-3215.
Habteselassie, M., M. Bischoff, E. Blume, B. Applegate, B. Reuhs, S. Brouder, and R.F. Turco.
2008. Environmental controls on the fate of Escherichia coli in soil. Water Air Soil Pollut.
190:143-155.
Compiled by Marilyn Erickson, Center for Food Safety, University of Georgia
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Page 1
Factors affecting survival of pathogens in soil systems – last updated 7/13/2012
Role of soil moisture in pathogen survival
In general, survival of microorganisms
is greater in moist environments than
dry environments but will depend on the
type of pathogen, pathogen
concentration, storage temperature, and
presence of indigenous competitive
microflora.
Ongeng, D., C. Muyanja, A.H. Geeraerd, D. Springael, and J. Ryckeboer. 2011. Survival of
Escherichia coli O157:H7 and Salmonella enterica serovar Typhimurium in manure and manureamended soil under tropical climatic conditions in sub-Saharan Africa. J. Appl. Microbiol.
110:1007-1022.
Leifert, C., K. Ball, N. Volakakis, and J.M. Cooper. 2008. Control of enteric pathogens in readyto-eat vegetable crops in organic and 'low input' production systems: a HACCP-based approach.
J. Appl. Microbiol. 105:931-950.
Lang, N.L. and S.R. Smith. 2007. Influence of soil type, moisture content and biosolids
application on the fate of Escherichia coli in agricultural soil under controlled laboratory
conditions. J. Appl. Microbiol. 103:2122-2131.
Holley, R.A., K.M. Arrus, K.H. Ominsky, M. Tenuta, and G. Blank. 2006. Salmonella survival in
manure-treated soils during simulated seasonal temperature exposure. J. Environ. Qual. 35:11701180.
Davies, C.M., N. Altavilla, M. Krogh, C.M. Ferguson, D.A. Deere, and N.J. Ashbolt. 2005.
Environmental inactivation of Cryptosporidium oocysts in catchment soils. J. Appl. Microbiol.
98:308-317.
Jenkins, M.B., D.D. Bowman, E.A. Fogarty, and W.C. Ghiorse. 2002. Cryptosporidium parvum
oocyst inactivation in three soil types at various temperatures and water potentials. Soil Biol.
Biochem. 34:1101-1109.
Kato, S., M.B. Jenkins, E.A. Fogarty, and D.D. Bowman. 2002. Effects of freeze-thaw events on
the viability of Cryptosporidium parvum oocysts in soil. J. Parasitol. 88:718-722.
Dowe, M.J., E.D. Jackson, J.G. Mori, and C.R. Bell. 1997. Listeria monocytogenes survival in
soil and incidence in agricultural soils. J. Food Prot. 60:1201-1207.
Chandler, D.S. and J.A. Craven. 1978. Environmental factors affecting Escherichia coli and
Salmonella typhimurium numbers on land used for effluent disposal. Aust. J. Agric. Res. 29:577585.
Role of soil temperature in pathogen survival
Soil temperatures are often cooler than
optimum growth temperature of many
enteric bacterial pathogens, however,
increasing soil temperatures generally
result in decreased pathogen survival
due to an increased endogenous
predatory activity in the soil
Lang, N.L., M.D. Bellett-Travers, and S.R. Smith. 2007. Field investigations on the survival of
Escherichia coli and presence of other enteric microorganisms in biosolids-amended agricultural
soil. J. Appl. Microbiol. 103:1868-1882.
Fluctuation of soil temperatures leads to
increased metabolic stress and decreased
survival of pathogens
Ongeng, D., C. Muyanja, J. Ryckeboer, D. Springael, and A.H. Geeraerd. 2011. Kinetic modelbased prediction of the persistence of Salmonella enterica serovar Typhimurium under tropical
agricultural field conditions. J. Appl. Microbiol. 110:995-1006.
Lang, N.L., M.D. Bellett-Travers, and S.R. Smith. 2007. Field investigations on the survival of
Escherichia coli and presence of other enteric microorganisms in biosolids-amended agricultural
soil. J. Appl. Microbiol. 103:1868-1882.
Semenov, A.V., A.H.C. van Bruggen, L. van Overbeek, A.J. Termorshuizen, and A.M. Semenov.
2007. Influence of temperature fluctuations on Escherichia coli O157:H7 and Salmonella
enterica serovar Typhimurium in cow manure. FEMS Microbiol. Ecol. 60:419-428.
Kupriyanov, A.A., N.N. Kunenkova, A.H.C. van Bruggen, and A.M. Semenov. 2009.
Translocation of bacteria from animal excrements to soil and associated habitats. Eurasian Soil
Sci. 42:1263-1269.
Natvig, E.E., S.C. Ingham, B.H. Ingham, L.R. Cooperband, and T.R. Roper. 2002. Salmonella
enterica serovar Typhimurium and Escherichia coli contamination of root and leaf vegetables
grown in soils with incorporated bovine manure. Appl. Environ. Microbiol. 68:2737-2744.
Olson, M.E., J. Goh, M. Phillips, N. Guselle, and T.A. McAllister. 1999. Giardia cyst and
Cryptosporidium oocyst survival in water, soil, and cattle feces. J. Environ. Qual. 28:1991-1996.
Role of sunlight in pathogen survival in soils
Contribution of sunlight to pathogen
inactivation is dependent on season and
soil depth
Palacios, M.P., P. Lupiola, M.T. Tejedor, E. Del-Nero, A. Pardo, and L. Pita. 2001. Climatic
effects on Salmonella survival in plant and soil irrigated with artificially inoculated wastewater:
preliminary results. Wat. Sci. Technol. 43(12):103-108.
Palacios, M.P., P. Lupiola, M.T. Tejedor, E. Del-Nero, A. Pardo, and L. Pita. 2001. Climatic
effects on Salmonella survival in plant and soil irrigated with artificially inoculated wastewater:
preliminary results. Wat. Sci. Technol. 43(12):103-108.
Compiled by Marilyn Erickson, Center for Food Safety, University of Georgia
Downloaded from the website: A Systems Approach for Produce Safety: A Research Project Addressing Leafy Greens found at:
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Page 2
Factors affecting survival of pathogens in soil systems – last updated 7/13/2012
Gerba, C.P., and G. Britton. 1984. Microbial pollutants: Their survival and transport pattern to
groundwater. In: Britton, G., C.P. Gerbva (eds). Groundwater pollution microbiology. Wiley,
New York, pp. 39-54.
Survival of pathogens in soil as a function of the pathogen type and initial load
Protozoan parasites are the most
resistant to inactivation in soil followed
by enteroviruses and then enteric
bacterial pathogens
Survival times within soil systems
increase when the initial load of
contamination is larger
Some non-O157 serotypes were
generally more persistent (e.g.
O145:H28) and some were generally
less persistent (e.g. O113:H4 and
O6:H8).
Possession of Shiga toxins and intimin
in E. coli O157:H7 did not appear to
play an important role in its survival in
soils
Gale, P. 2005. Land application of treated sewage sludge: quantifying pathogen risks from
consumption of crops. J. Appl. Microbiol. 98:380-396.
Arthurson, V., A. Sessitsch, and L. Jäderlund. 2011. Persistence and spread of Salmonella
enterica serovar Weltevreden in soil and on spinach plants. FEMS Microbiol. Ecol. 314:67-74.
Ongeng, D., C. Muyanja, J. Ryckeboer, A.H. Geeraerd, and D. Springael. 2011. Rhizosphere
effect on survival of Escherichia coli O157LH7 and Salmonella enterica serovar Typhimurium in
manure-amended soil during cabbage (Brassica oleracea) cultivation under tropical field
conditions in sub-Saharan Africa. Int. J. Food Microbiol. 149:133-142.
Bolton, D.J., C.M. Byrne, J.J. Sheridan, D.A. McDowell, and I.S. Blair. 1999. The survival
characteristics of a non-toxigenic strain of Escherichia coli O157:H7. J. Appl. Microbiol.
86:407-411.
Ma, J., A.M. Ibekwe, X. Yi, H. Wang, A. Yamazaki, D.E. Crowley, and C.-H. Yang. 2011.
Persistence of Escherichia coli O157:H7 and its mutants in soils. PLoS One 6:e23291.
Role of plant type on pathogen survival
Root exudates may account for the
different survival patterns of pathogens
in soil systems cultivating different
crops
Houlden, A., T.M. Timms-Wilson, M.J. Day, and M.J. Bailey. 2008. Influence of plant
developmental stage on microbial community structure and activity in the rhizosphere of three
field crops. FEMS Microbiol. Ecol. 65:193-201.
Islam, M., M.P. Doyle, S.C. Phatak, P. Millner, and X. Jiang. 2005. Survival of Escherichia coli
O157:H7 in soil and on carrots and onions grown in fields treated with contaminated manure
composts or irrigation water. Food Microbiol. 22:63-70.
Islam, M., J. Morgan, M.P. Doyle, and X. Jiang. 2004. Fate of Escherichia coli O157:H7 in
manure compost-amended soil and on carrots and onions grown in an environmentally controlled
growth chamber. J. Food Prot. 67:574-578.
Ibekwe, A., P.M. Watt, P.J. Shouse, and C.M. Grieve. 2004. Fate of Escherichia coli O157:H7 in
irrigation water on soils and plants as validated by culture method and real-time PCR. Can. J.
Microbiol. 50:1007-1014.
Marschner, P., D. Crowley, and C.H. Yang. 2004. Development of specific rhizosphere bacterial
communities in relation to plant species, nutrition and soil type. Plant Soil 261:199-208.
Gagliardi, J.V. and J.S. Karns. 2002. Persistence of Escherichia coli O157:H7 in soil and on plant
roots. Environ. Microbiol. 4(2):89-96.
Haichar, F.Z., C. Marol, O. Berge, J.I. Rangel-Castro, J.I. Prosser, J. Balesdent, T. Heulin, and
W. Achouak. 2008. Plant host habitat and root exudates shape soil bacterial community structure.
ISME J. 2:1221-1230.
Maloney, P.E., A.H.C. van Bruggen, and S. Hu. 1997. Bacterial community structure in relation
to the carbon environments in lettuce and tomato rhizospheres and in bulk soil. Microbial
Ecology 34:109-117.
Ongeng, D., C. Muyanja, J. Ryckeboer, A.H. Geeraerd, and D. Springael. 2011. Rhizosphere
effect on survival of Escherichia coli O157LH7 and Salmonella enterica serovar Typhimurium in
manure-amended soil during cabbage (Brassica oleracea) cultivation under tropical field
conditions in sub-Saharan Africa. Int. J. Food Microbiol. 149:133-142.
Role of indigenous soil microflora on pathogen survival
Contribution of indigenous soil
microflora is based on systems where
their levels have been reduced through
chemical or physical treatments
Ibekwe, A.M., S.K. Papiernik, C.M. Grieve, and C.-H. Yang. 2010. Influence of fumigants on
soil microbial diversity and survival of E. coli O157:H7. J. Environ. Sci. Hlth. Part B 45:416426.
van Elsas, J.D., P. Hill, A. Chroňáková, M. Grekova, Y. Topalova, D. Elhottová, and V.
Krištůfek. 2007. Survival of genetically marked Escherichia coli O157:H7 in soil as affected by
soil microbial community. The ISME J. 1:204-214.
You, Y., S.C. Rankin, H.W. Aceto, C.E. Benson, J.D. Toth, and Z. Dou. 2006. Survival of
Salmonella enterica serovar Newport in manure and manure-amended soils. Appl. Environ.
Microbiol. 72:5777-5783.
Compiled by Marilyn Erickson, Center for Food Safety, University of Georgia
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Page 3
Factors affecting survival of pathogens in soil systems – last updated 7/13/2012
Both enhancement and inhibition of
colonization of enteric pathogen
colonization in soil have been observed
with individual soil organisms
It is advocated that an increased
proportion of oligotrophic organisms in
soil (capable of surviving in low carbon
environments) would increase the
competitive pressure on enteric
pathogens and thus inactivation would
be faster under those conditions.
Jiang, X., J. Morgan, and M.P. Doyle. 2002. Fate of Escherichia coli O157:H7 in manureamended soil. Appl. Environ. Microbiol. 68:2605-2609.
Cooley, M.B., W.G. Miller, and R.E. Mandrell. 2003. Colonization of Arabidopsis thaliana with
Salmonella enterica and enterohemorrhagic Escherichia coli O157:H7 and competition by
Enterobacter asburiae. Appl. Environ. Microbiol. 69:4915-4926.
Semenov, A.V., E. Franz, L. van Overbeek, A.J. Termorshulzen, and A.H.C. van Bruggen. 2008.
Estimating the stability of Escherichia coli O157:H7 survival in manure-amended soils with
different management histories. Environ. Microbiol. 10:1450-1459.
Role of indigenous soil macrofauna on pathogen survival
Soil macrofauna, such as nematodes and
flagellates, are capable of ingesting and
digesting enteric pathogens although it
does not ensure complete elimination of
the pathogen
Kenney, S.J., G.O. Anderson, P.L. Williams, P.D. Millner, and L.R. Beuchat. 2005. Persistence
of Escherichia coli O157:H7, Salmonella Newport, and Salmonella Poona in the gut of a freeliving nematode, Caenorhabditis elegans, and transmission to progeny and uninfected
nematodes. Int. J. Food Microbiol. 101:227-236.
Erickson, M.C., M. Islam, C. Sheppard, J. Liao, and M.P. Doyle. 2004. Reduction of Escherichia
coli O157:H7 and Salmonella enterica serovar Enteritidis in chicken manure by larvae of the
black soldier fly. J. Food Prot. 67:685-690.
Huamanchay, O., L. Genzlinger, M. Iglesias, and Y.R. Ortega. 2004. Ingestion of
Cryptosporidium oocysts by Caenorhabditis elegans. J. Parasitol. 90:1176-1178.
Role of management practices on pathogen survival in soil
Fumigation of contaminated soils
decreased populations of enteric
pathogens
Ibekwe, A.M., S.K. Papiernik, C.M. Grieve, and C.-H. Yang. 2010. Influence of fumigants on
soil microbial diversity and survival of E. coli O157:H7. J. Environ. Sci. Hlth. Part B 45:416426.
Ibekwe, A.M., C.M. Grieve, S.K. Papiernik, and D-H. Yang. 2009. Persistence of Escherichia
coli O157:H7 on the rhizosphere and phyllosphere of lettuce. Lett. Appl. Microbiol. 49:784-790.
Application of essential oils to soils
decreases populations of enteric
pathogens
Weed management practices have not
been shown to increase the risk of
pathogen survival
Ca(OH)2 can be used to inactivate
pathogens in soil but the pH must
remain above 11 for at least 7 days
while a high manure: soil ratio will tend
to neutralize the pH and increase the risk
of Salmonella regrowth.
Ibekwe, A.M., C.M. Grieve, M. Grieve, and C-H. Yang. 2007. Survival of Escherichia coli
O157:H7 in soil and on lettuce after soil fumigation. Can. J. Microbiol. 53:623-635.
van Elsas, J.D., P. Hill, A. Chroňáková, M. Grekova, Y. Topalova, D. Elhottová, and V.
Krištůfek. 2007. Survival of genetically marked Escherichia coli O157:H7 in soil as affected by
soil microbial community. The ISME J. 1:204-214.
Yossa, N., J. Patel, P. Millner, and M. Lo. 2011. Inactivation of Salmonella in organic soil by
cinnamaldehyde, eugenol, ecotrol, and sporran. Foodborne Path. Dis. 8:311-317.
Yossa, N., J. Patel, P. Millner, and Y.M. Lo. 2010. Antimicrobial activity of essential oils against
Escherichia coli O157:H7 in organic soil. Food Control 21:1458-1465.
Fischer-Arndt, M., D. Neuhoff, L. Tamm, and U. Kopke. 2010. Effects of weed management
practices on enteric pathogen transfer into lettuce (Lactuca sativa var. capitata). Food Control
21:1004-1010.
Nyberg, K.A., B. Vinneras, S.S. Lewerin, E. Kjellberg, and A. Albihn. 2011. Treatment with
Ca(OH)2 for inactivation of Salmonella Typhimurium and Enterococcus faecalis in soil
contaminated with infected horse manure. J. Appl. Microbiol. 110:1515-1523.
Compiled by Marilyn Erickson, Center for Food Safety, University of Georgia
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Page 4