Abstract
Scrapie and chronic wasting disease (CWD) are two prion diseases of particular environmental concern as they are horizontally transmissible. Prions are shed from diseased hosts in a diverse set of biologic matrices and are present throughout the diseased host. There is strong experimental evidence that properties of soil and water can significantly affect prion sorption, resistance to degradation, persistence, replication efficiency when bound to soil, and ultimately prion infectivity. Highly sensitive and accurate detection of prion infectivity in the environment is not currently possible, severely hampering informed management of disease. A more thorough understanding of the interaction of prions with the environment in combination with robust detection methods may lead to means to reduce or eliminating prion disease in free-range and captive animal populations as well as mitigating the risk of zoonotic prion transmission.
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Acevedo P, Ruiz-Fons F, Estrada R, Márquez A, Miranda MA, Gortázar C, Lucientes J (2010) A broad assessment of factors determining Culicoides imicola abundance: modeling the present and forecasting its future in climate change scenarios. PLoS One 5:e14236
Almberg ES, Cross PC, Johnson CJ, Heisey DM, Richards BJ (2011) Modeling routes of chronic wasting disease transmission: environmental prion persistence promotes deer population decline and extinction. PLoS One 6:e19896
Atarashi R, Moore RA, Sim VL, Hughson AG, Dorward DW, Onwubiko HA, Priola SA, Caughey B (2007) Ultrasensitive detection of scrapie prion protein using seeded conversion of recombinant prion protein. Nat Methods 4:645–650
Atarashi R, Wilham JM, Christensen L, Hughson AG, Moore RA, Johnson LM, Onwubiko HA, Priola SA, Caughey B (2008) Simplified ultrasensitive prion detection by recombinant PrP conversion with shaking. Nat Methods 5:211–212
Barron RM, Campbell SL, King D, Bellon A, Chapman KE, Williamson RA, Manson JC (2007) High titers of transmissible spongiform encephalopathy infectivity associated with extremely low levels of PrPSc in vivo. J Bio Chem 282:35878–35886
Bessen RA, Marsh RF (1994) Distinct PrP properties suggest the molecular basis of strain variation in transmissible mink encephalopathy. J Virol 68:7859–7868
Blanchong JA, Samuel MD, Scribner KT, Weckworth BV, Langenberg J, Filcek KB (2008) Landscape genetics and the spatial distribution of chronic wasting disease. Biol Lett 4:130–133
Chihota CM, Gravenor MB, Baylis M (2004) Investigation of trace elements in soil as risk factors in the epidemiology of scrapie. Vet Rec 154:809–813
Cilimburg A, Monz C, Kehoe S (2000) Wildland recreation and human waste: a review of problems, practices, and concerns. Environ Manage 25:587–598
Conner MM, Miller MW (2004) Movement patterns and spatial epidemiology of a prion disease in mule deer population units. Ecol Appl 14:1870–1881
Cooke CM, Shaw G (2007) Fate of prions in soil: longevity and migration of recPrP in soil columns. Soil Bio Biochem 39:1181–1191
Cooke CM, Rodger J, Smith A, Fernie K, Shaw G, Somerville RA (2007) Fate of prions in soil: detergent extraction of PrP from soils. Environ Sci Technol 41:811–817
Davies P, Brown DR (2009) Manganese enhances prion protein survival in model soils and increases prion infectivity to cells. PLoS One 4:e7518
de Jonge LW, Kjaergaard C, Moldrup P (2004) Colloids and colloid-facilitated transport of contaminants in soils: an introduction. Vadose Zone J 3:321–325
Dexter G, Tongue SC, Heasman L, Bellworthy SJ, David A, Moore SJ, Simmons MM, Sayers AR, Simmons HA, Matthews D (2009) The evaluation of exposure risks for natural transmission of scrapie within an infected flock. BMC Vet Res 5:38
Dhand NK, Eppleston J, Whittington RJ, Toribio JALML (2009) Association of farm soil characteristics with ovine Johne’s disease in Australia. Prev Vet Med 89:110–120
Epstein E, Beecher N (2005) Mad cow disease, Creuzfeld-Jakob disease, other TSEs, and biosolids. J Res Sci Technol 2:181–187
Georgsson G, Siguardson S, Brown P (2006) Infectious agent of sheep scrapie may persist in the environment for at least 16 years. J Gen Virol 87:3737–3740
Gough KC, Maddison BC (2010) Prion transmission: prion excretion and occurrence in the environment. Prion 4:275–282
Greig JR (1940) Scrapie: observation on the transmission of the disease by mediate contact. Vet J 96:203–206
Hadlow WJ, Kennedy RC, Race RE (1982) Natural infection of Suffolk sheep with scrapie virus. J Infect Dis 146:657–664
Hamir AN, Kunkle RA, Richt JA, Miller JM, Cutlip RC, Jenny AL (2005) Experimental transmission of sheep scrapie by intracerebral and oral routes to genetically susceptible Suffolk sheep in the United States. J Vet Diagn Invest 17:3–19
Hamir AN, Kunkle RA, Richt JA, Miller JM, Greenlee JJ (2008) Experimental transmission of US scrapie agent by nasal, peritoneal, and conjunctival routes to genetically susceptible sheep. Vet Pathol 45:7–11
Hinckley GT, Johnson CJ, Jacobson KT, Bartholomay C, McMahon KD, McKenzie D, Aiken JM, Pedersen JA (2008) Persistence of pathogenic prion protein during simulated wastewater treatment processes. Environ Sci Technol 42:5254–5259
Holman RC, Belay ED, Christensen KY, Maddox RA, Minino AM, Haberling DL, Hammett TA, Kochanek KD, Sejvar JJ, Schonberger LB (2010) Human prion diseases in the United States. PLoS One 5:e8521
Hunter N (2007) Scrapie: uncertainties, biology and molecular approaches. Biochim Biophys Acta 1772:619–628
Imrie CE, Korre A, Munoz-Melendez G (2009) Spatial correlation between the prevalence of transmissible spongiform diseases and British soil geochemistry. Environ Geochem Health 31:133–145
Jacobson KT, Lee S, McKenzie D, Benson CH, Pedersen JA (2009) Transport of the pathogenic prion protein through landfill materials. Environ Sci Technol 43:2022–2028
Jacobson KT, Lee S, Somerville RA, McKenzie D, Benson CH, Pedersen JA (2010) Transport of the pathogenic prion protein through soils. J Environ Qual 39:1145–1152
Johnson CJ, Phillips KE, Schramm PT, McKenzie D, Aiken JM, Pedersen JA (2006) Prions adhere to soil minerals and remain infectious. PLoS Pathog 2:296–302
Johnson CH, Pedersen JA, Chappell RJ, McKenzie D, Aiken JM (2007) Oral transmissibility of prion disease is enhanced by binding to soil particles. PLoS Pathog 3:e93
Johnson CJ, Bennett JP, Biro SM, Duque-Velasquez JC, Rodriguez CM, Bessen RA, Roke TE (2011) Degradation of the disease-associated prion protein by a serine protease from lichens. PLoS One 6:e19836
Joly DO, Samuel MD, Langenberg J, Blanchong JA, Batha CA, Rolley RE, Keane DP, Ribic CA (2006) Spatial epidemiology of chronic wasting disease in Wisconsin with-tailed deer. J Wildlife Dis 42:578–588
Kincaid AE, Bartz JC (2007) The nasal cavity is a route for prion infection in hamsters. J Virol 81:4482–4491
Kirchmayr R, Reichi HE, Schildorfer H, Braun R, Somerville RA (2006) Prion protein: detection in ‘spiked’ anaerobic sludge and degradation experiments under anaerobic conditions. Water Sci Technol 53:91–98
Kresta AE, Henke SE, Pence DB (2010) Baylisascaris procyonis in raccoons in Texas and its relationship to habitat characteristics. J Wildlife Dis 46:843–853
Krumm CE, Conner MM, Miller MW (2005) Relative vulnerability of chronic wasting disease infected mule deer to vehicle collisions. J Wildlife Dis 41:503–511
Kurt TD, Perrott MR, Wilusz CJ, Wilusz J, Supattapone S, Telling GC, Zabel MD, Hoover EA (2007) Efficient in vitro amplification of chronic wasting disease PrPres. J Virol 81:9605–9608
Maddison BC, Owen JP, Bishop K, Shaw G, Rees HC, Gough KC (2010a) The interaction of ruminant PrPSc with soils is influenced by prion source and soil type. Environ Sci Technol 44:8503–8508
Maddison BC, Baker CA, Terry LA, Bellworthy SJ, Thorne L, Rees HC, Gough KC (2010b) Environmental sources of scrapie prions. J Virol 84:11560–11562
Maluquer de Motes C, Cano MJ, Torres JM, Pumarola M, Girones R (2008) Detection and survival of prion agents in aquatic environments. Wat Res 42:2465–2472
Mathiason CK, Hays SA, Powers JG, Hayes-Klug J, Langenberg J, Dahmes SH, Osborn DA, Miller KV, Warren RJ, Mason GL, Hoover EA (2009) Infectious prions in pre-clinical deer and transmission of chronic wasting disease solely by environmental exposure. PLoS One 4:e5916
Mazzola M (2002) Mechanisms of natural soil suppressiveness to soilborne diseases. Anton Leeuw Int JG 81:557–564
McBride MB (2007) Trace metals and sulfur in soils and forage of a chronic wasting disease locus. Environ Chem 4:134–139
McLeod AH, Murdoch H, Dickinson J, Dennis MJ, Hall GA, Buswell CM, Carr J, Taylor DM, Sutton JM, Raven ND (2004) Proteolytic inactivation of the bovine spongiform encephalopathy agent. Biochem Biophys Res Comm 317:1165–1170
Miller MW, Williams ES (2003) Horizontal prion transmission in mule deer. Nature 425:35–36
Miller MW, Williams ES, Hobbs NT, Wolfe LL (2004) Environmental sources of prion transmission in mule deer. Emerg Infect Dis 10:1003–1006
Miller MW, Hobbs NT, Tavener SJ (2006) Dynamics of prion disease transmission in mule deer. Ecol Appl 16:2208–2214
Nagaoka K, Yoshioka M, Shimozaki N, Yamamura T, Murayama Y, Yokoyama T, Mohri S (2010) Sensitive detection of scrapie prion protein in soil. Biochem Biophys Res Comm 397:626–630
Onisko B, Dynin I, Requena J, Silva C, Erickson M, Carter J (2007) Mass spectrometric detection of attomole amounts of the prion protein by nanoLC/MS/MS. J Am Soc Mass Spect 18:1070–1079
Pedersen JA, McMahon KD, Benson CH (2006) Prions: novel pathogens of environmental concern? J Environ Eng 132:967–969
Rhyan JC, Miller MW, Srapker TR, McCollum M, Nol P, Wolfe LL, Davis TR, Creekmore L, O’Rourke KJ (2011) Failure of fallow deer (Dama dama) to develop chronic wasting disease when exposure to a contaminated environment and infected mule deer (Odocoileus hemionus). J Wildlife Dis 47:739–744
Russo F, Johnson CJ, Johnson CJ, McKenzie D, Aiken JM, Pedersen JA (2009) Pathogenic prion protein is degraded by a manganese oxide mineral found in soils. J Gen Virol 90:275–280
Saa P, Castilla J, Soto C (2006) Ultra-efficient replication of infectious prions by automated protein misfolding cyclic amplification. J Bio Chem 281:35245–35252
Saunders SE, Bartelt-Hunt SL, Bartz JC (2008a) Prions in the environment: occurrence, fate and mitigation. Prion 2:162–169
Saunders SE, Bartz JC, Telling GC, Bartelt-Hunt SL (2008b) Environmentally-relevant forms of the prion protein. Environ Sci Technol 42:6573–6579
Saunders SE, Bartz JC, Bartelt-Hunt SL (2009a) Prion protein adsorption to soil in a competitive matrix is slow and reduced. Environ Sci Technol 43:7728–7733
Saunders SE, Bartz JC, Bartelt-Hunt SL (2009b) Influence of prion strain on prion protein adsorption to soil in a competitive matrix. Environ Sci Technol 43:5242–5248
Saunders SE, Bartz JC, VerCauteren KC, Bartelt-Hunt SL (2010) Enzymatic digestion of chronic wasting disease prions bound to soil. Environ Sci Technol 44:4129–4135
Saunders SE, Yuan Q, Bartz JC, Bartelt-Hunt SL (2011a) Effects of solution chemistry and aging time on prion protein adsorption and replication of soil-bound prions. PLoS One 6:e18752
Saunders SE, Shikiya RA, Langenfeld KA, Bartelt-Hunt SL, Bartz JC (2011b) Replication efficiency of soil-bound prions varies with soil type. J Virol 85:5476–5482
Saunders SE, Bartz JC, VerCauteren KC, Bartelt-Hunt SL (2011c) An enzymatic treatment of soil-bound prions effectively inhibits replication. Applied and Environmental Microbiology 77:4313–4317
Saunders SE, Bartelt-Hunt SL, Bartz JC (2012a) Occurrence, tranmission and zoonotic potential of chronic wasting disease. Emerg Infect Dis 18:369–376
Saunders SE, Bartz JC, Bartelt-Hunt SL (2012b) Soil-mediated prion transmission: is local soil-type a key determinant of prion disease incidence? Chemos 87:661–667
Scherbel C, Richner R, Groschup MH, Mueller-Hellwig S, Scherer S, Dietrich R, Maertlbauer E, Gareis M (2006) Degradation of scrapie associated prion protein (PrPSc) by the gastrointestinal microbiota of cattle. Vet Res 37:695–703
Scherbel C, Pichner R, Groschup MH, Mueller-Hellwig S, Scherer S, Dietrich R, Maertlbauer E, Gareis M (2007) Infectivity of scrapie prion protein PrPSc following In vitro digestion with bovine gastrointestinal microbiota. Zoo Public Health 54:185–190
Seidel B, Thomzig A, Buschmann A, Groschup MH, Peters R, Beekes M, Terytze K (2007) Scrapie agent (strain 263 K) can transmit disease via the oral route after persistence in soil over years. PLoS One 2(5):e435
Sharp A, Pastor J (2011) Stable limit cycles and the paradox of enrichment in a model of chronic wasting disease. Ecol Appl 21:1024–1030
Siguardson S (1991) Epidemiology of scrapie in Iceland. In: Bradley R, Savey M, Marchant B (eds) Sub-acute spongiform encephalopathies. Kluwer Academic Publishers, Dordrecht
Sigurdson CJ, Williams ES, Miller MW, Spraker TR, O’Rourke KI, Hoover EA (1999) Oral transmission and early lymphoid tropism of chronic wasting disease PrPSc in mule deer fawns (Odecoileus hemionus). J Gen Virol 80:2757–2764
Silveira JR, Raymond GJ, Hughson AG, Race RE, Sim VL, Hayes SF, Caughey B (2005) The most infectious prion protein particles. Nature 437:257–261
Smith CB, Booth CJ, Pedersen JA (2011) Fate of prions in soil: a review. J Environ Qual 40:449–461
Stevens KB, Del Rio Vilas VJ, Guitian J (2009) Classical sheep scrapie in Great Britain: spatial analysis and identification of environmental and farm-related risk factors. BMC Vet Res 5:33
Tamgüney G, Miller MW, Wolfe LL, Sirochman TM, Glidden DV, Palmer CP, Lemus A, DeArmond SJ, Pruisner SB (2009) Asymptomatic deer excrete infectious prions in faeces. Nature 461:529–532
Taylor DM (1999) Inactivation of prions by physical and chemical means. J Hosp Infect 43:S69–S76
Walter WD, Walsh DP, Farnsworth ML, Winkelman DL, Miller MW (2011) Soil clay content underlies prion infection odds. Nat Commun 2:200
Wild MA, Hobbs NT, Graham MS, Miller MW (2011) The role of predation in disease control: a comparison of selective and nonselective removal on prion disease dynamics in deer. J Wildlife Dis 47:78–79
Yoshioka M, Miwa T, Horii H, Takata M, Yokoyama T, Nishizawa K, Watanabe M, Shinagawa M, Murayama Y (2007) Characterization of a proteolytic enzyme derived from a Bacillus strain that effectively degrades prion protein. J Appl Microbiol 102:509–515
Acknowledgments
This work was supported by National Science Foundation (CBET-1149242) and the Nation Center for Research Resources (P20 RR0115635-6, C06 RR17417-01 and G200RR024001).
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Bartelt-Hunt, S.L., Bartz, J.C., Saunders, S.E. (2013). Prions in the Environment. In: Zou, WQ., Gambetti, P. (eds) Prions and Diseases. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-5338-3_6
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DOI: https://doi.org/10.1007/978-1-4614-5338-3_6
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