Skip to main content

Prions in the Environment

  • Chapter
  • First Online:

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.

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   229.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   299.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   299.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Bessen RA, Marsh RF (1994) Distinct PrP properties suggest the molecular basis of strain variation in transmissible mink encephalopathy. J Virol 68:7859–7868

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Cilimburg A, Monz C, Kehoe S (2000) Wildland recreation and human waste: a review of problems, practices, and concerns. Environ Manage 25:587–598

    Article  PubMed  Google Scholar 

  • Conner MM, Miller MW (2004) Movement patterns and spatial epidemiology of a prion disease in mule deer population units. Ecol Appl 14:1870–1881

    Article  Google Scholar 

  • Cooke CM, Shaw G (2007) Fate of prions in soil: longevity and migration of recPrP in soil columns. Soil Bio Biochem 39:1181–1191

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Davies P, Brown DR (2009) Manganese enhances prion protein survival in model soils and increases prion infectivity to cells. PLoS One 4:e7518

    Article  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Epstein E, Beecher N (2005) Mad cow disease, Creuzfeld-Jakob disease, other TSEs, and biosolids. J Res Sci Technol 2:181–187

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Gough KC, Maddison BC (2010) Prion transmission: prion excretion and occurrence in the environment. Prion 4:275–282

    Article  PubMed  CAS  Google Scholar 

  • Greig JR (1940) Scrapie: observation on the transmission of the disease by mediate contact. Vet J 96:203–206

    Google Scholar 

  • Hadlow WJ, Kennedy RC, Race RE (1982) Natural infection of Suffolk sheep with scrapie virus. J Infect Dis 146:657–664

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Hunter N (2007) Scrapie: uncertainties, biology and molecular approaches. Biochim Biophys Acta 1772:619–628

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Kincaid AE, Bartz JC (2007) The nasal cavity is a route for prion infection in hamsters. J Virol 81:4482–4491

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Mazzola M (2002) Mechanisms of natural soil suppressiveness to soilborne diseases. Anton Leeuw Int JG 81:557–564

    Article  CAS  Google Scholar 

  • McBride MB (2007) Trace metals and sulfur in soils and forage of a chronic wasting disease locus. Environ Chem 4:134–139

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Miller MW, Williams ES (2003) Horizontal prion transmission in mule deer. Nature 425:35–36

    Article  PubMed  CAS  Google Scholar 

  • Miller MW, Williams ES, Hobbs NT, Wolfe LL (2004) Environmental sources of prion transmission in mule deer. Emerg Infect Dis 10:1003–1006

    Article  PubMed  Google Scholar 

  • Miller MW, Hobbs NT, Tavener SJ (2006) Dynamics of prion disease transmission in mule deer. Ecol Appl 16:2208–2214

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Pedersen JA, McMahon KD, Benson CH (2006) Prions: novel pathogens of environmental concern? J Environ Eng 132:967–969

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Saunders SE, Bartelt-Hunt SL, Bartz JC (2008a) Prions in the environment: occurrence, fate and mitigation. Prion 2:162–169

    Article  PubMed  Google Scholar 

  • Saunders SE, Bartz JC, Telling GC, Bartelt-Hunt SL (2008b) Environmentally-relevant forms of the prion protein. Environ Sci Technol 42:6573–6579

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Saunders SE, Bartelt-Hunt SL, Bartz JC (2012a) Occurrence, tranmission and zoonotic potential of chronic wasting disease. Emerg Infect Dis 18:369–376

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Siguardson S (1991) Epidemiology of scrapie in Iceland. In: Bradley R, Savey M, Marchant B (eds) Sub-acute spongiform encephalopathies. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Smith CB, Booth CJ, Pedersen JA (2011) Fate of prions in soil: a review. J Environ Qual 40:449–461

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Taylor DM (1999) Inactivation of prions by physical and chemical means. J Hosp Infect 43:S69–S76

    Article  PubMed  Google Scholar 

  • Walter WD, Walsh DP, Farnsworth ML, Winkelman DL, Miller MW (2011) Soil clay content underlies prion infection odds. Nat Commun 2:200

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

Download references

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).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shannon L. Bartelt-Hunt Ph.D. .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer Science+Business Media New York

About this chapter

Cite this chapter

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

Download citation

Publish with us

Policies and ethics