Importance of Soil Amendments: Survival of Bacterial Pathogens in Manure and Compost Used as Organic Fertilizers

Manan Sharma; Russell Reynnells

doi:10.1128/microbiolspec.PFS-0010-2015

Chapter 9 : Importance of Soil Amendments: Survival of Bacterial Pathogens in Manure and Compost Used as Organic Fertilizers

Authors: Manan Sharma¹, Russell Reynnells²

VIEW AFFILIATIONS HIDE AFFILIATIONS

Affiliations: 1: U.S. Department of Agriculture, Agricultural Research Service, Beltsville Area Research Center, Environmental Microbial and Food Safety Laboratory, Beltsville, MD 20705; 2: University of Maryland Eastern Shore, Department of Agriculture, Food, and Resource Science, Princess Anne, MD 21853

Content Type: Monograph

Publication Year: 2018

Book DOI: 10.1128/9781555819644

Chapter DOI: 10.1128/microbiolspec.PFS-0010-2015

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:

Importance of Soil Amendments: Survival of Bacterial Pathogens in Manure and Compost Used as Organic Fertilizers, Page 1 of 2

< Previous page | Next page > /docserver/preview/fulltext/10.1128/9781555819644/9781555817077_Chap09-1.gif /docserver/preview/fulltext/10.1128/9781555819644/9781555817077_Chap09-2.gif

Abstract:

Biological soil amendments (BSAs), including manure, compost, and compost teas (CTs), play an important role in conventional and organic agriculture. The use of these amendments can provide nutrients to soils, improving soil fertility and crop production. However, recent outbreaks of bacterial, viral, and parasitic infections associated with produce commodities over the past decade have focused more attention on agricultural inputs used to grow fresh fruits and vegetables. In response to these outbreaks, proposed rules from the U.S. Food and Drug Administration (FDA) have been issued, titled “Standards for the Growing, Harvesting, Packing and Holding of Produce for Human Consumption” Supplemental to the Proposed Rule ( 1 ). As part of these standards, the FDA has proposed specific rules and guidelines for how several BSAs can be applied to soils and fields intended to grow produce for human consumption.

Citation: Sharma M, Reynnells R. 2018. Importance of Soil Amendments: Survival of Bacterial Pathogens in Manure and Compost Used as Organic Fertilizers, p 159-175. In Thakur S, Kniel K (ed), Preharvest Food Safety. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PFS-0010-2015

Highlighted Text: Show | Hide

Full text loading...

Figures

Importance of Soil Amendments: Survival of Bacterial Pathogens in Manure and Compost Used as Organic Fertilizers

[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555819644.chap9-1,webId=/content/author/10.1128/9781555819644.chap9-1,properties={foaf_givenname=Manan, foaf_name=Manan Sharma, foaf_surname=Sharma, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555819644.chap9-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555819644.chap9-2,webId=/content/author/10.1128/9781555819644.chap9-2,properties={foaf_givenname=Russell, foaf_name=Russell Reynnells, foaf_surname=Reynnells, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555819644.chap9-aff2]]}]]

/content/10.1128/9781555819644.chap9.fig9-1

Figure 1

(A) The survival of a three-strain (TVS 353, 354, and 355), nonpathogenic (generic) E. coli inoculum in either poultry litter–amended (gEC PL), horse manure–amended (gEC HM), or unamended (gEC uA) soils over 98 days in southern Pennsylvania (Southeastern Agricultural Research and Extension Center, Pennsylvania State University, Landisville, PA). Amendments were surface applied (no till). (B) The moisture content of PL-amended soils [PL Hi(s)], HM-amended soils [HM Hi(c)], and uA soils [uA Hi(s)]. (C) The air temperature throughout the study. Values below the x-axis indicate the number of days of the study. Dashed lines indicate days when changes in E. coli populations occurred, potentially attributed to changes in either soil moisture content or temperature. The first dashed line indicates that an increase in air temperature (graph C) from days 0 to 5 corresponded to an increase in all E. coli populations in graph A; the second dashed line indicates that an increase in soil moisture content (graph B) from day 7 to day 14 corresponded to an increase in all E. coli populations; the third dashed line indicates that a decline in soil moisture content of PL Hi(s) from day 14 to day 28 resulted in a decline of E. coli populations in gEc PL. These graphs show that air temperature and soil moisture content can affect E. coli populations in soils amended with surface-applied manures more than E. coli populations in tilled in soils ( Fig. 2 ).

10.1128/9781555819644/fig9-1_thmb.gif

10.1128/9781555819644/fig9-1.gif

Figure 1

/content/10.1128/9781555819644.chap9.fig9-2

Figure 2

(A) The survival of a three-strain (TVS 353, 354, and 355), nonpathogenic (generic) E. coli inoculum in either poultry litter–amended (gEC PL), horse manure–amended (gEC HM), or unamended (gEC uA) over 98 days in soils at the Southeastern Agricultural Research and Extension Center. Amendments were tilled into soils. (B) The moisture content of tilled PL-amended [PL Hi(c)], HM-amended [HM Hi(c)], and uA soils ]uA Hi(c)]. (C) The air temperature throughout the study. Values below the x-axis indicate the number of days of the study. Dashed lines indicate days where changes in E. coli populations occurred, potentially attributed to changes in either soil moisture content or temperature. The first dashed line indicates that all E. coli populations (graph A) increased on day 5 with an increase in all soil moisture contents (graph B) from day 3 to day 5. On day 7 (no dashed line), the decline in E. coli populations between days 5 and 7 was associated with a fall in the soil moisture content of all soils. The second dashed line indicates an increase in gEC HM and gEC uA populations from day 14 to day 28, which corresponds to an increase in HM Hi(c), and uA Hi(c) soil moisture contents (no increase in gEC PL was observed). The figure illustrates that E. coli populations in tilled soils amended with manure may be less responsive to changes in air temperature and more responsive to changes in soil moisture content than E. coli in surface manure-amended soils ( Fig. 1 ).

10.1128/9781555819644/fig9-2_thmb.gif

10.1128/9781555819644/fig9-2.gif

Figure 2

(A) The survival of a three-strain (TVS 353, 354, and 355), nonpathogenic (generic) E. coli inoculum in either poultry litter–amended (gEC PL), horse manure–amended (gEC HM), or unamended (gEC uA) over 98 days in soils at the Southeastern Agricultural Research and Extension Center. Amendments were tilled into soils. (B) The moisture content of tilled PL-amended [PL Hi(c)], HM-amended [HM Hi(c)], and uA soils ]uA Hi(c)]. (C) The air temperature throughout the study. Values below the x-axis indicate the number of days of the study. Dashed lines indicate days where changes in E. coli populations occurred, potentially attributed to changes in either soil moisture content or temperature. The first dashed line indicates that all E. coli populations (graph A) increased on day 5 with an increase in all soil moisture contents (graph B) from day 3 to day 5. On day 7 (no dashed line), the decline in E. coli populations between days 5 and 7 was associated with a fall in the soil moisture content of all soils. The second dashed line indicates an increase in gEC HM and gEC uA populations from day 14 to day 28, which corresponds to an increase in HM Hi(c), and uA Hi(c) soil moisture contents (no increase in gEC PL was observed). The figure illustrates that E. coli populations in tilled soils amended with manure may be less responsive to changes in air temperature and more responsive to changes in soil moisture content than E. coli in surface manure-amended soils ( Fig. 1 ).

References

/content/book/10.1128/9781555819644.chap9

1. Food and Drug Administration . 2014. Standards for growing, harvesting, packing, and holding of produce for human consumption. FSMA Proposed Rule for Produce Safety. http://www.fda.gov/Food/GuidanceRegulation/FSMA/ucm334114.htm.[CrossRef]

2. Mikha M,, Benjamin JG . 2014. Remediation/restoration of degraded soil. II. Impact on crop production and nitrogen dynamics. Agron J 106 : 261– 272.

3. Rees HW,, Chow L,, Zebarth B,, Xing Z,, Toner P,, Lavoie J,, Daigle J-L . 2014. Impact of supplemental poultry manure application on potato yield and soil properties on a loam soil in north-western New Brunswick. Can J Soil Sci 94 : 49– 65.[CrossRef]

4. Donovan NJ,, Saleh F,, Chan KY,, Eldridge SM,, Fahey D,, Muirhead L,, Meszaros I,, Barhcia I . 2014. Use of garden organic compost in a long-term vegetable field trial: biological soil health. Acta Hortic 1018 : 47– 55.[CrossRef]

5. CalFERT (California Food Emergency Response Team) . 2008. Investigation of the Taco John’s Escherichia coli O157:H7 outbreak associated with iceberg lettuce. California Department of Public Health, Sacramento, CA.

6. Söderström A,, Osterberg P,, Lindqvist A,, Jönsson B,, Lindberg A,, Blide Ulander S,, Welinder-Olsson C,, Löfdahl S,, Kaijser B,, De Jong B,, Kühlmann-Berenzon S,, Boqvist S,, Eriksson E,, Szanto E,, Andersson S,, Allestam G,, Hedenström I,, Ledet Muller L,, Andersson Y . 2008. A large Escherichia coli O157 outbreak in Sweden associated with locally produced lettuce. Foodborne Pathog Dis 5 : 339– 349.[PubMed][CrossRef]

7. Hutchison ML,, Walters LD,, Avery SM,, Munro F,, Moore A . 2005. Analyses of livestock production, waste storage, and pathogen levels and prevalences in farm manures. Appl Environ Microbiol 71 : 1231– 1236.[PubMed][CrossRef]

8. California Food Emergency Response Team . 2007. Investigation of an Escherichia coli O157:H7 outbreak associated with Dole pre-packaged spinach. https://www.cdph.ca.gov/pubsforms/Documents/fdb%20eru%20Spnch%20EC%20Dole032007wph.PDF.

9. Centers for Disease Control and Prevention . 2008. Multistate outbreak of Salmonella Saintpaul infections linked to raw produce (final update). http://www.cdc.gov/salmonella/2008/raw-produce-8-28-2008.html.

10. Food and Drug Administration . 2013. Environmental assessment: factors potentially contributing to the contamination of fresh whole cantaloupe implicated in a multi-state outbreak of salmonellosis. http://www.fda.gov/Food/RecallsOutbreaksEmergencies/Outbreaks/ucm341476.htm.

11. Food and Drug Administration . 2011. Environmental assessment: factors potentially contributing to the contamination of fresh whole cantaloupe implicated in a multi-state outbreak of listeriosis. http://www.fda.gov/food/recallsoutbreaksemergencies/outbreaks/ucm276247.htm.

12. Angelo KM,, Chu A,, Anand M,, Nguyen TA,, Bottichio L,, Wise M,, Williams I,, Seelman S,, Bell R,, Fatica M,, Lance S,, Baldwin D,, Shannon K,, Lee H,, Trees E,, Strain E,, Gieraltowski L, Centers for Disease Control and Prevention (CDC) . 2015. Outbreak of Salmonella Newport infections linked to cucumbers: United States, 2014. MMWR Morb Mortal Wkly Rep 64 : 144– 147.[PubMed]

13. Painter JA,, Hoekstra RM,, Ayers T,, Tauxe RV,, Braden CR,, Angulo FJ,, Griffin PM . 2013. Attribution of foodborne illnesses, hospitalizations, and deaths to food commodities by using outbreak data, United States, 1998–2008. Emerg Infect Dis 19 : 407– 415.[PubMed][CrossRef]

14. California Leafy Greens Handler Marketing Agreement . 2013. Commodity specific food safety guidelines for the production and harvest of lettuce and leafy greens. http://www.lgma.ca.gov/wp-content/uploads/2014/09/California-LGMA-metrics-08-26-13-Final.pdf.

15. National Organic Program . Soil fertility and crop nutrient management practice standard. 7 C.F.R. 205.203.

16. Tomato Best Practices Manual . 2007. A guide to tomato good agricultural practices (T-GAP) and tomato best management practices (T-BMP) 2007. http://fvreports.freshfromflorida.com/5G_TomBPM.pdf.

17. Avery LM,, Hill P,, Killham K,, Jones DL . 2004. Escherichia coli O157 survival following the surface and sub-surface application of human pathogen contaminated organic waste to soil. Soil Biol Biochem 36 : 2101– 2103.[CrossRef]

18. Franz E,, Semenov AV,, Termorshuizen AJ,, de Vos OJ,, Bokhorst JG,, van Bruggen AHC . 2008. Manure-amended soil characteristics affecting the survival of E. coli O157:H7 in 36 Dutch soils. Environ Microbiol 10 : 313– 327.[PubMed][CrossRef]

19. Harris LJ,, Berry ED,, Blessington T,, Erickson M,, Jay-Russell M,, Jiang X,, Killinger K,, Michel FC,, Millner P,, Schneider K,, Sharma M,, Suslow TV,, Wang L,, Worobo RW . 2013. A framework for developing research protocols for evaluation of microbial hazards and controls during production that pertain to the application of untreated soil amendments of animal origin on land used to grow produce that may be consumed raw. J Food Prot 76 : 1062– 1084.[PubMed][CrossRef]

20. Hutchison ML,, Walters LD,, Avery SM,, Synge BA,, Moore A . 2004. Levels of zoonotic agents in British livestock manures. Lett Appl Microbiol 39 : 207– 214.[PubMed][CrossRef]

21. Nyberg KA,, Ottoson JR,, Vinnerås B,, Albihn A . 2014. Fate and survival of Salmonella Typhimurium and Escherichia coli O157:H7 in repacked soil lysimeters after application of cattle slurry and human urine. J Sci Food Agric 94 : 2541– 2546.[PubMed][CrossRef]

22. Gessel PD,, Hansen NC,, Goyal SM,, Johnston LJ,, Webb J . 2004. Persistence of zoonotic pathogens in surface soil treated with different rates of liquid pig manure. Appl Soil Ecol 25 : 237– 243.[CrossRef]

23. Bezanson G,, Delaquis P,, Bach S,, McKellar R,, Topp E,, Gill A,, Blais B,, Gilmour M . 2012. Comparative examination of Escherichia coli O157:H7 survival on romaine lettuce and in soil at two independent experimental sites. J Food Prot 75 : 480– 487.[PubMed][CrossRef]

24. Gutiérrez-Rodríguez E,, Gundersen A,, Sbodio AO,, Suslow TV . 2012. Variable agronomic practices, cultivar, strain source and initial contamination dose differentially affect survival of Escherichia coli on spinach. J Appl Microbiol 112 : 109– 118.[PubMed][CrossRef]

25. Whyte C,, Cotton CP,, Hashem F,, Sharma M,, Millner P . 2014. Irrigation, manure, and soil type influences on survival and persistence of non-pathogenic E. coli and E. coli O157:H7 in a greenhouse environment. Poster P1-129, International Association for Food Protection Annual Meeting, Indianapolis, IN, 3–6 August.

26. Brennan FP,, Abram F,, Chinalia FA,, Richards KG,, O’Flaherty V . 2010. Characterization of environmentally persistent Escherichia coli isolates leached from an Irish soil. Appl Environ Microbiol 76 : 2175– 2180.[PubMed][CrossRef]

27. van Hoek AH,, Aarts HJM,, Bouw E,, van Overbeek WM,, Franz E . 2013. The role of rpoS in Escherichia coli O157 manure-amended soil survival and distribution of allelic variations among bovine, food and clinical isolates. FEMS Microbiol Lett 338 : 18– 23.[PubMed][CrossRef]

28. Franz E,, van Hoek AHAM,, Bouw E,, Aarts HJM . 2011. Variability of Escherichia coli O157 strain survival in manure-amended soil in relation to strain origin, virulence profile, and carbon nutrition profile. Appl Environ Microbiol 77 : 8088– 8096.[PubMed][CrossRef]

29. Bhagwat AA,, Tan J,, Sharma M,, Kothary M,, Low S,, Tall BD,, Bhagwat M . 2006. Functional heterogeneity of RpoS in stress tolerance of enterohemorrhagic Escherichia coli strains. Appl Environ Microbiol 72 : 4978– 4986.[PubMed][CrossRef]

30. Duffitt AD,, Reber RT,, Whipple A,, Chauret C . 2011. Gene expression during survival of Escherichia coli O157:H7 in soil and water. Int J Microbiol 2011 : 1– 12.[PubMed][CrossRef]

31. Kandror O,, DeLeon A,, Goldberg AL . 2002. Trehalose synthesis is induced upon exposure of Escherichia coli to cold and is essential for viability at low temperatures. Proc Natl Acad Sci USA 99 : 9727– 9732.[PubMed][CrossRef]

32. Zhang Q,, Yan T . 2012. Correlation of intracellular trehalose concentration with desiccation resistance of soil Escherichia coli populations. Appl Environ Microbiol 78 : 7407– 7413.[PubMed][CrossRef]

33. Graham L,, Wright D,, Hashem F,, Cotton C,, Collins A,, White K,, Stonebraker R,, Sharma M,, Millner P . 2014. The effect of manure application method on the persistence of Escherichia coli in manure-amended soils in southeastern Pennsylvania. Poster P1-131, International Association for Food Protection Annual Meeting, Indianapolis, IN, 3–6 August.

34. Schwarz KR,, Sidhu JPS,, Pritchard DL,, Li Y,, Toze S . 2014. Decay of enteric microorganisms in biosolids-amended soil under wheat ( Triticum aestivum) cultivation. Water Res 59 : 185– 197.[PubMed][CrossRef]

35. Lang NL,, Bellett-Travers MD,, Smith SR . 2007. Field investigations on the survival of Escherichia coli and presence of other enteric micro-organisms in biosolids-amended agricultural soil. J Appl Microbiol 103 : 1868– 1882.[PubMed][CrossRef]

36. Gibbs RA,, Hu CJ,, Ho GE,, Unkovich I . 1997. Regrowth of faecal coliforms and salmonellae in stored biosolids and soil amended with biosolids. Water Sci Technol 35 : 269– 275.[CrossRef]

37. Berry ED,, Wells JE,, Bono JL,, Woodbury BL,, Kalchayanand N,, Norman KN,, Suslow TV,, López-Velasco G,, Millner PD . 2015. Effect of proximity to a cattle feedlot on Escherichia coli O157:H7 contamination of leafy greens and evaluation of the potential for airborne transmission. Appl Environ Microbiol 81 : 1101– 1110.[PubMed][CrossRef]

38. Oni RA,, Sharma M,, Buchanan RL . 2015. Survival of Salmonella spp. in dried turkey manure and persistence on spinach leaves. J Food Prot 78 : 1791– 1799.[PubMed][CrossRef]

39. Wichmann F,, Udikovic-Kolic N,, Andrew S,, Handelsman J . 2014. Diverse antibiotic resistance genes in dairy cow manure. MBio 5 : e01017-13.[PubMed][CrossRef]

40. Marti R,, Scott A,, Tien Y-C,, Murray R,, Sabourin L,, Zhang Y,, Topp E . 2013. Impact of manure fertilization on the abundance of antibiotic-resistant bacteria and frequency of detection of antibiotic resistance genes in soil and on vegetables at harvest. Appl Environ Microbiol 79 : 5701– 5709.[PubMed][CrossRef]

41. Udikovic-Kolic N,, Wichmann F,, Broderick NA,, Handelsman J . 2014. Bloom of resident antibiotic-resistant bacteria in soil following manure fertilization. Proc Natl Acad Sci USA 111 : 15202– 15207.[PubMed][CrossRef]

42. Cernicchiaro N,, Cull CA,, Paddock ZD,, Shi X,, Bai J,, Nagaraja TG,, Renter DG . 2013. Prevalence of Shiga toxin-producing Escherichia coli and associated virulence genes in feces of commercial feedlot cattle. Foodborne Pathog Dis 10 : 835– 841.[PubMed][CrossRef]

43. Cernicchiaro N,, Renter DG,, Cull CA,, Paddock ZD,, Shi X,, Nagaraja TG . 2014. Fecal shedding of non-O157 serogroups of Shiga toxin-producing Escherichia coli in feedlot cattle vaccinated with an Escherichia coli O157:H7 SRP vaccine or fed a Lactobacillus-based direct-fed microbial. J Food Prot 77 : 732– 737.[PubMed][CrossRef]

44. Luedtke BE,, Bono JL,, Bosilevac M . 2014. Evaluation of a real time PCR assay for the detection and enumeration of enterohemorrhagic Escherichia coli directly from cattle feces. J Microbiol Methods 105 : 72– 79.[PubMed][CrossRef]

45. Millner PD, . 2009. Manure management, p 79– 104. In Sapers GM,, Solomon EB,, Matthews KR (ed), The Produce Contamination Problem. Academic Press, New York.[CrossRef]

46. Millner PD . 2014. Pathogen disinfection technologies, metrics, and regulations for recycled organics used in horticulture. Acta Hortic 1018 : 621– 630.[CrossRef]

47. Mylavarapu RS,, Zinati GM . 2009. Improvement of soil properties using compost for optimum parsley production in sandy soils. Sci Hortic (Amsterdam) 120 : 426– 430.[CrossRef]

48. Gandolfi I,, Sicolo M,, Franzetti A,, Fontanarosa E,, Santagostino A,, Bestetti G . 2010. Influence of compost amendment on microbial community and ecotoxicity of hydrocarbon-contaminated soils. Bioresour Technol 101 : 568– 575.[PubMed][CrossRef]

49. Farrell M,, Griffith GW,, Hobbs PJ,, Perkins WT,, Jones DL . 2009. Microbial diversity and activity are increased by compost amendment of metal-contaminated soils. FEMS Microbiol Lett 71 : 94– 105.[PubMed][CrossRef]

50. Reynnells RE . 2013. Comparison of pathogen detection methods in compost and compost characteristics as potential predictors of pathogen regrowth. Master’s thesis, University of Maryland, College Park, MD. http://drum.lib.umd.edu/handle/1903/14819.

51. Berry ED,, Millner PD,, Wells JE,, Kalchayanand N,, Guerni MN . 2013. Fate of naturally occurring Escherichia coli O157:H7 and other zoonotic pathogens during minimally managed bovine feedlot manure composting processes. J Food Prot 76 : 1308– 1321.[PubMed][CrossRef]

52. Ingram DT . 2009. Assessment of foodborne pathogen survival during production and pre-harvest application of compost and compost tea. Ph.D. dissertation, University of Maryland, College Park, MD. http://drum.lib.umd.edu/bitstream/1903/9137/1/Ingram_umd_0117E_10231.pdf.

53. Brinton WF Jr,, Storms P,, Blewett TC . 2009. Occurrence and levels of fecal indicators and pathogenic bacteria in market-ready recycled organic matter composts. J Food Prot 72 : 332– 339.[PubMed]

54. Wichuk KM,, McCartney D . 2007. A review of the effectiveness of current time-temperature regulations on pathogen inactivation during composting. J Environ Eng Sci 6 : 572– 586.[CrossRef]

55. Shepherd MW Jr,, Liang P,, Jiang X,, Doyle MP,, Erickson MC . 2010. Microbiological analysis of composts produced on South Carolina poultry farms. J Appl Microbiol 108 : 2067– 2076.[PubMed]

56. Patel JR,, Yossa I,, Macarisin D,, Millner P . 2015. Physical covering for control of Escherichia coli O157:H7 and Salmonella spp. in static and windrow composting processes. Appl Environ Microbiol 81 : 2063– 2074.[PubMed][CrossRef]

57. Erickson MC,, Liao J,, Jiang X,, Doyle MP . 2014. Inactivation of pathogens during aerobic composting of fresh and aged dairy manure and different carbon amendments. J Food Prot 77 : 1911– 1918.[PubMed][CrossRef]

58. Reynnells R,, Ingram DT,, Roberts C,, Stonebraker R,, Handy ET,, Felton G,, Vinyard BT,, Millner PD,, Sharma M . 2014. Comparison of U.S. Environmental Protection Agency and U.S. Composting Council microbial detection methods in finished compost and regrowth potential of Salmonella spp. and Escherichia coli O157:H7 in finished compost. Foodborne Pathog Dis 11 : 555– 567.[PubMed][CrossRef]

59. Paniel N,, Rousseaux S,, Gourland P,, Poitrenaud M,, Guzzo J . 2010. Assessment of survival of Listeria monocytogenes, Salmonella Infantis and Enterococcus faecalis artificially inoculated into experimental waste or compost. J Appl Microbiol 108 : 1797– 1809.[PubMed][CrossRef]

60. Pietronave S,, Fracchia L,, Rinaldi M,, Martinotti MG . 2004. Influence of biotic and abiotic factors on human pathogens in a finished compost. Water Res 38 : 1963– 1970.[PubMed][CrossRef]

61. Soares HM,, Cardenas B,, Weir D,, Switzenbaum MS . 1995. Evaluating pathogen regrowth in biosolids compost. Biocycle 36 : 70– 76.

62. Kim J,, Shepherd MW Jr,, Jiang X . 2009. Evaluating the effect of environmental factors on pathogen regrowth in compost extract. Microb Ecol 58 : 498– 508.[PubMed][CrossRef]

63. Ingram DT,, Millner PD . 2007. Factors affecting compost tea as a potential source of Escherichia coli and Salmonella on fresh produce. J Food Prot 70 : 828– 834.[PubMed]

64. Kannangara T,, Forge T,, Dang B . 2006. Effects of aeration molasses, kelp, compost type, and carrot juice on the growth of Escherichia coli in compost teas. Compost Sci Util 14 : 40– 47.[CrossRef]

65. Sidhu J,, Gibbs RA,, Ho GE,, Unkovich I . 2001. The role of indigenous microorganisms in suppression of Salmonella regrowth in composted biosolids. Water Res 35 : 913– 920.[PubMed][CrossRef]

66. Millner PD,, Powers KE,, Enkiri NK,, Burge WD . 1987. Microbially mediated growth suppression and death of Salmonella in composted sewage sludge. Microb Ecol 14 : 255– 265.[PubMed][CrossRef]

67. Islam M,, Doyle MP,, Phatak SC,, Millner P,, Jiang X . 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.[PubMed][CrossRef]

68. Islam M,, Morgan J,, Doyle MP,, Phatak SC,, Millner P,, Jiang X . 2004. Fate of Salmonella enterica serovar Typhimurium on carrots and radishes grown in fields treated with contaminated manure composts or irrigation water. Appl Environ Microbiol 70 : 2497– 2502.[PubMed][CrossRef]

Tables

Importance of Soil Amendments: Survival of Bacterial Pathogens in Manure and Compost Used as Organic Fertilizers

/content/10.1128/9781555819644.chap9.tab9-1

TABLE 1

Guidance and proposed rules by organizations and federal agencies in the United States on the application of biological soil amendments to agricultural fields intended to grow selected fruit and vegetable crops

TABLE 1

/content/10.1128/9781555819644.chap9.tab9-2

TABLE 2

Change in inoculated E. coli populations in manure-amended soils in large pots in a greenhouse environment after weekly irrigation events

TABLE 2

Change in inoculated E. coli populations in manure-amended soils in large pots in a greenhouse environment after weekly irrigation events