Transmission of chronic wasting disease in Wisconsin white-tailed deer: Implications for disease spread and management

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Jennelle, Christopher S ^a   Henaux, Viviane ^a   Wasserberg, Gideon ^b   Thiagarajan, Bala ^a   Rolley, Robert E ^c   Samuel, Michael D ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF NORTH CAROLINA AT GREENSBORO   (United States)

^c WISCONSIN DEPARTMENT OF NATURAL RESOURCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL HEALTH; ARTICLE; CHRONIC WASTING DISEASE; CONTROLLED STUDY; DEMOGRAPHY; DISEASE TRANSMISSION; FEMALE; HARVEST; INFECTION CONTROL; INFECTION RATE; MALE; NONHUMAN; POPULATION DYNAMICS; PREVALENCE; SEX DIFFERENCE; UNITED STATES; WHITE TAILED DEER; ANIMAL; DEER; TRANSMISSION; WASTING DISEASE, CHRONIC;

ANIMALS; DEER; FEMALE; MALE; PREVALENCE; WASTING DISEASE, CHRONIC; WISCONSIN;

EID: 84899082980     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0091043     Document Type: Article

References (69)

1. Ewald PW (2011) Evolution of virulence, environmental change, and the threat posed by emerging and chronic diseases. Ecol Res 26: 1017-1026. doi:10.1007/s11284-011-0874-8
2. Robinson SJ, Samuel MD, Johnson CJ, Adams M, McKenzie DI (2012) Emerging prion disease drives host selection in a wildlife population. Ecol Appl 22: 1050-1059.
3. Wobeser GA (2007) Disease in wild animals. Berlin; New York: Springer. 393 p.
4. Williams ES (2005) Chronic Wasting Disease. Vet Pathol 42: 530-549. doi:10.1354/vp.42-5-530
5. Gross JE, Miller MW (2001) Chronic wasting disease in mule deer: Disease dynamics and control. J Wildl Manag 65: 205-215. (Pubitemid 32663355)
6. Schauber EM, Woolf A (2003) Chronic wasting disease in deer and elk: A critique of current models and their application. Wildl Soc Bull 31: 610-616. (Pubitemid 37298643)
7. Miller MW, Conner MM (2005) Epidemiology of chronic wasting disease in free-ranging mule deer: spatial, temporal, and demographic influences on observed prevalence patterns. J Wildl Dis 41: 275-290. (Pubitemid 41245633)
8. Wolfe LL, Miller MW, Williams ES (2004) Feasibility of "test-and-cull" for managing chronic wasting disease in urban mule deer. Wildl Soc Bull 32: 500-505. doi:10.2193/0091-7648(2004)32[500:FOTFMC]2.0. CO;2 (Pubitemid 38946355)
9. Williams ES, Miller MW, Kreeger TJ, Kahn RH, Thorne ET (2002) Chronic wasting disease of deer and elk: A review with recommendations for management. J Wildl Manag 66: 551-563. (Pubitemid 34915216)
10. Anderson RM, May RM (1991) Infectious diseases of humans: dynamics and control. Oxford; New York: Oxford University Press. 757 p.
11. McCallum H, Barlow N, Hone J (2001) How should pathogen transmission be modelled? Trends Ecol Evol 16: 295-300. (Pubitemid 32706645)
12. Begon M, Bennett M, Bowers RG, French NP, Hazel SM, et al. (2002) A clarification of transmission terms in host-microparasite models: numbers, densities and areas. Epidemiol Infect 129: 147-153.
13. Roberts MG (1996) The Dynamics of Bovine Tuberculosis in Possum Populations, and its Eradication or Control by Culling or Vaccination. J Anim Ecol 65: 451-464.
14. Getz WM, Pickering J (1983) Epidemic Models: Thresholds and Population Regulation. Am Nat 121: 892-898. doi:10.1086/284112
15. Cross ML, Buddle BM, Aldwell FE (2007) The potential of oral vaccines for disease control in wildlife species. Vet J 174: 472-480. doi:10.1016/j.tvjl. 2006.10.005 (Pubitemid 350082696)
16. Barlow ND (1996) The ecology of wildlife disease control: Simple models revisited. J Appl Ecol 33: 303-314.
17. Miller MW, Williams ES, McCarty CW, Spraker TR, Kreeger TJ, et al. (2000) Epizootiology of chronic wasting disease in free-ranging cervids in Colorado and Wyoming. J Wildl Dis 36: 676-690.
18. Wasserberg G, Osnas EE, Rolley RE, Samuel MD (2009) Host culling as an adaptive management tool for chronic wasting disease in white-tailed deer: a modelling study. J Appl Ecol 46: 457-466. doi:10.1111/j.1365-2664.2008.01576.x
19. Joly DO, Ribic CA, Langenberg JA, Beheler K, Batha CA, et al. (2003) Chronic wasting disease in free-ranging Wisconsin White-tailed Deer. Emerg Infect Dis 9: 599-601. (Pubitemid 36529521)
20. Joly DO, Samuel MD, Langenberg JA, Blanchong JA, Batha CA, et al. (2006) Spatial epidemiology of chronic wasting disease in Wisconsin white-tailed deer. J Wildl Dis 42: 578-588. (Pubitemid 44873516)
21. Grear DA, Samuel MD, Langenberg JA, Keane D (2006) Demographic Patterns and Harvest Vulnerability of Chronic Wasting Disease Infected White-Tailed Deer in Wisconsin. J Wildl Manag 70: 546-553. doi:10.2193/0022-541X(2006)70[546: DPAHVO]2.0.CO;2 (Pubitemid 43736922)
22. Osnas EE, Heisey DM, Rolley RE, Samuel MD (2009) Spatial and temporal patterns of chronic wasting disease: fine-scale mapping of a wildlife epidemic in Wisconsin. Ecol Appl 19: 1311-1322.
23. Conner MM, Miller MW (2004) Movement patterns and spatial epidemioology of a prion disease in mule deer population units. Ecol Appl 14: 1870-1881. doi:10.1890/03-5309 (Pubitemid 40020372)
24. Blanchong JA, Samuel MD, Scribner KT, Weckworth BV, Langenberg JA, et al. (2008) Landscape genetics and the spatial distribution of chronic wasting disease. Biol Lett 4: 130-133. doi:10.1098/rsbl.2007.0523 (Pubitemid 351598299)
25. Heisey DM, Osnas EE, Cross PC, Joly DO, Langenberg JA, et al. (2010) Linking process to pattern: estimating spatiotemporal dynamics of a wildlife epidemic from cross-sectional data. Ecol Monogr 80: 221-240. doi:10.1890/09-0052.1
26. Cross PC, Drewe J, Patrek V, Pearce G, Samuel MD, et al. (2009) Wildlife Population Structure and Parasite Transmission: Implications for Disease Management. In: Delahay RJ, Smith GC, Hutchings MR, editors. Management of Disease in Wild Mammals. Tokyo: Springer. pp. 9-29.
27. Magle SB, Samuel MD, Van Deelen TR, Robinson SJ, Mathews NE (2013) Evaluating spatial overlap and relatedness of white-tailed deer in a chronic wasting disease management zone. PloS One 8: e56568. doi:10.1371/journal.pone. 0056568
28. Grear DA, Samuel MD, Scribner KT, Weckworth BV, Langenberg JA (2010) Influence of genetic relatedness and spatial proximity on chronic wasting disease infection among female white-tailed deer. J Appl Ecol 47: 532-540. doi:10.1111/j.1365-2664.2010.01813.x
29. Keane DP, Barr DJ, Bochsler PN, Hall SM, Gidlewski T, et al. (2008) Chronic wasting disease in a Wisconsin white-tailed deer farm. J Vet Diagn Invest 20: 698-703.
30. Van Deelen TR, Campa III H, Hamady M, Haufler JB (1998) Migration and Seasonal Range Dynamics of Deer Using Adjacent Deeryards in Northern Michigan. J Wildl Manag 62: 205-213. (Pubitemid 28146774)
31. Van Deelen TR (1999) Deer-cedar interactions during a period of mild winters: implications for conservation of conifer swamp deeryards in the Great Lakes region. Nat Areas J 19: 263-274.
32. Dunkley L, Cattet MRL (2003) A comprehensive review of the ecological and human social effects of artificial feeding and baiting of wildlife. Saskatoon, Saskatchewan: Canadian Cooperative Wildlife Health Centre.
33. Wisconsin Department of Natural Resources (2010) Wisconsin's chronic wasting disease response plan: 2010-2025. Madison, Wisconsin.
34. Keane DP, Barr DJ, Keller JE, Hall SM, Langenberg JA, et al. (2008) Comparison of retropharyngeal lymph node and obex region of the brainstem in detection of chronic wasting disease in white-tailed deer (Odocoileus virginianus). J Vet Diagn Invest 20: 58-60. (Pubitemid 352843941)
35. Caswell H (2001) Matrix population models: construction, analysis, and interpretation. 2nd ed. Sunderland, Mass: Sinauer Associates. 722 p.
36. Oli MK, Venkataraman M, Klein PA, Wendland LD, Brown MB (2006) Population dynamics of infectious diseases: A discrete time model. Ecol Model 198: 183-194. doi:10.1016/j.ecolmodel.2006.04.007 (Pubitemid 44287183)
37. Klepac P, Caswell H (2011) The stage-structured epidemic: linking disease and demography with a multi-state matrix approach model. Theor Ecol 4: 301-319. doi:10.1007/s12080-010-0079-8
38. Rudolf VHW, Antonovics J (2005) Species coexistence and pathogens with frequency-dependent transmission. Am Nat 166: 112-118. doi:10.1086/430674 (Pubitemid 40886778)
39. Potapov A, Merrill E, Pybus M, Coltman D, Lewis MA (2013) Chronic wasting disease: Possible transmission mechanisms in deer. Ecol Model 250: 244-257. doi:10.1016/j.ecolmodel.2012.11.012
40. Hilborn R, Mangel M (1997) The Ecological Detective: Confronting Models with Data. Princeton: Princeton University Press. 330 p.
41. Burnham KP, Anderson DR (1998) Model selection and inference: a practical information-theoretic approach. New York: Springer-Verlag. 353 p.
42. McKay MD, Beckman RJ, Conover WJ (1979) Comparison of Three Methods for Selecting Values of Input Variables in the Analysis of Output from a Computer Code. Technometrics 21: 239-245. doi:10.1080/00401706.1979.10489755 (Pubitemid 9452235)
43. Manache G, Melching CS (2004) Sensitivity Analysis of a Water-Quality Model Using Latin Hypercube Sampling. J Water Resour Plan Manag 130: 232-242. doi:10.1061/(ASCE)0733-9496(2004)130:3(232) (Pubitemid 38571090)
44. Robinson SJ, Samuel MD, Rolley R, Shelton P (2013) Using landscape epidemiological models to understand factors affecting the distribution of chronic wasting disease in the Midwestern USA. Landsc Ecol 28: 1923-1935.
45. Holsman RH, Petchenik J (2006) Predicting Deer Hunter Harvest Behavior in Wisconsin's Chronic Wasting Disease Eradication Zone. Hum Dimens Wildl 11: 177-189. doi:10.1080/10871200600669916
46. Storm DJ, Samuel MD, Rolley RE, Shelton P, Keuler NS, et al. (2013) Deer density and disease prevalence influence transmission of chronic wasting disease in white-tailed deer. Ecosphere 4: 10. doi:10.1890/ES12-00141.1
47. Farnsworth ML, Wolfe LL, Hobbs NT, Burnham KP, Williams ES, et al. (2005) Human land use influences chronic wasting disease prevalence in mule deer. Ecol Appl 15: 119-126. doi:10.1890/04-0194 (Pubitemid 40263573)
48. Halls LK (1984) White-tailed deer: ecology and management. Harrisburg, PA: Stackpole Books. 870 p.
49. Habib TJ, Merrill EH, Pybus MJ, Coltman DW (2011) Modelling landscape effects on density-contact rate relationships of deer in eastern Alberta: Implications for chronic wasting disease. Ecol Model 222: 2722-2732. doi:10.1016/j.ecolmodel.2011.05.007
50. Brown P, Gajdusek D (1991) Survival of scrapie virus after 3 years' interment. The Lancet 337: 269-270. doi:10.1016/0140-6736(91)90873-N
51. Johnson CJ, Phillips KE, Schramm PT, McKenzie D, Aiken JM, et al. (2006) Prions Adhere to Soil Minerals and Remain Infectious. PLoS Pathog 2: e32. doi:10.1371/journal.ppat.0020032
52. Miller MW, Williams ES, Hobbs NT, Wolfe LL (2004) Environmental Sources of Prion Transmission in Mule Deer. Emerg Infect Dis 10: 1003-1006. doi:10.3201/eid1006.040010 (Pubitemid 38697690)
53. Miller MW, Hobbs NT, Tavener SJ (2006) Dynamics of prion disease transmission in mule deer. Ecol Appl 16: 2208-2214. (Pubitemid 44917580)
54. 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. doi:10.1371/journal.pone.0019896
55. Fenichel EP, Horan RD (2007) Gender-Based Harvesting in Wildlife Disease Management. Am J Agric Econ 89: 904-920. doi:10.1111/j.1467-8276.2007.01025.x (Pubitemid 47506068)
56. Kjær LJ, Schauber EM, Nielsen CK (2008) Spatial and Temporal Analysis of Contact Rates in Female White-Tailed Deer. J Wildl Manag 72: 1819-1825. doi:10.2193/2007-489
57. Silbernagel ER, Skelton NK, Waldner CL, Bollinger TK (2011) Interaction among deer in a chronic wasting disease endemic zone. J Wildl Manag 75: 1453-1461. doi:10.1002/jwmg.172
58. Richards SA (2008) Dealing with overdispersed count data in applied ecology. J Appl Ecol 45: 218-227. doi:10.1111/j.1365-2664.2007.01377.x
59. Palmer MV, Waters WR, Whipple DL (2004) Shared feed as a means of deer-todeer transmission of Mycobacterium bovis. J Wildl Dis 40: 87-91. (Pubitemid 39026757)
60. Oyer AM, Mathews NE, Skuldt LH (2007) Long-Distance Movement of a White-Tailed Deer Away From a Chronic Wasting Disease Area. J Wildl Manag 71: 1635-1638. doi:10.2193/2006-381
61. Long ES, Diefenbach DR, Rosenberry CS, Wallingford BD, Grund MD (2005) Forest cover influences dispersal distance of white-tailed deer. J Mammal 86: 623-629. doi:10.1644/1545-1542(2005)86[623:FCIDDO]2.0.CO;2 (Pubitemid 40802358)
62. Lang KR, Blanchong JA (2012) Population genetic structure of white-tailed deer: Understanding risk of chronic wasting disease spread. J Wildl Manag 76: 832-840. doi:10.1002/jwmg.292
63. Robinson SJ, Samuel MD, Lopez DL, Shelton P (2012) The walk is never random: subtle landscape effects shape gene flow in a continuous white-tailed deer population in the Midwestern United States. Mol Ecol 21: 4190-4205. doi:10.1111/j.1365-294X.2012.05681.x
64. Potapov A, Merrill E, Lewis MA (2012) Wildlife disease elimination and density dependence. Proc R Soc B Biol Sci 279: 3139-3145. doi:10.1098/rspb.2012. 0520
65. Roseberry JL, Woolf A (1991) A Comparative Evaluation of Techniques for Analyzing White-Tailed Deer Harvest Data. Wildl Monogr 117: 3-59.
66. Gaillard J-M, Festa-Bianchet M, Yoccoz NG (1998) Population dynamics of large herbivores: variable recruitment with constant adult survival. Trends Ecol Evol 13: 58-63. doi:10.1016/S0169-5347(97)01237-8 (Pubitemid 28081008)
67. Williams ES, Young S (1980) Chronic wasting disease of captive mule deer: a spongiform encephalopathy. J Wildl Dis 16: 89-98.
68. Walter WD, Walsh DP, Farnsworth ML, Winkelman DL, Miller MW (2011) Soil clay content underlies prion infection odds. Nat Commun 2: 200. doi:10.1038/ncomms1203
69. Bolker BM (2008) Ecological models and data in R. Princeton, N.J: Princeton University Press. 396 p.