Estimated effects of projected climate change on the basic reproductive number of the lyme disease vector ixodes scapularis

Environmental Health Perspectives

Volumn 122, Issue 6, 2014, Pages 631-638

  Ogden, Nicholas H ^a   Radojević, Milka ^a   Wu, Xiaotian ^b   Duvvuri, Venkata R ^b   Leighton, Patrick A ^c   Wu, Jianhong ^b  

^a PUBLIC HEALTH AGENCY OF CANADA   (Canada)

^b YORK UNIVERSITY   (Canada)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BASIC REPRODUCTION NUMBER; CLIMATE CHANGE; DISEASE CARRIER; GEOGRAPHIC DISTRIBUTION; HEALTH HAZARD; IXODES SCAPULARIS; LIFE CYCLE; LYME DISEASE; MODEL; MORTALITY; NONHUMAN; PRIORITY JOURNAL; RISK; SENSITIVITY ANALYSIS; SPATIOTEMPORAL ANALYSIS; SURVIVAL; TICK BORNE DISEASE; WARMING; ANIMAL; BIOLOGICAL MODEL; CANADA; FORECASTING; GROWTH, DEVELOPMENT AND AGING; HUMAN; IXODES; PARASITE VECTOR; POPULATION DYNAMICS; REPRODUCTION; TRANSMISSION; UNITED STATES; VIROLOGY;

ANIMALS; ARACHNID VECTORS; CANADA; CLIMATE CHANGE; FORECASTING; HUMANS; IXODES; LYME DISEASE; MODELS, BIOLOGICAL; POPULATION DYNAMICS; REPRODUCTION; UNITED STATES;

EID: 84899991904     PISSN: 00916765     EISSN: 15529924     Source Type: Journal    
DOI: 10.1289/ehp.1307799     Document Type: Article

References (98)

1. Anderson J.F., Duray PH, Magnarelli LA. 1987. Prevalence of Borrelia burgdorferi in white-footed mice and Ixodes dammini at Fort McCoy, Wis. J Clin Microbiol 25(8):1495-1497.
2. Barbour A.G., Fish D. 1993. The biological and social phenomenon of Lyme disease. Science 260(5114):1610-1616.
3. Bauch C.T., Lloyd-Smith JO, Coffee MP, Galvani AP. 2005. Dynamically modeling SARS and other newly emerging respiratory illnesses: past, present, and future. Epidemiology 16(6):791-801.
4. Bouchard C., Beauchamp G, Leighton PA, Lindsay R, Bélanger D, Ogden NH. 2013a. Does high biodiversity reduce the risk of Lyme disease invasion? Parasit Vectors 6(1):195; doi:10.1186/1756-3305-6-195.
5. Bouchard C., Leighton PA, Beauchamp G, Nguon S, Trudel L, Milord F., et al. 2013b. Harvested white-tailed deer as sentinel hosts for early establishing Ixodes scapularis populations and risk from vector-borne zoonoses in southeastern Canada. J Med Entomol 50(2):384-393.
6. Brownstein J.S., Holford TR, Fish D. 2005. Effect of climate change on Lyme disease risk in North America. Ecohealth 2(1):38-46.
7. Brunner J.L., Killilea M, Ostfeld RS. 2012. Overwintering survival of nymphal Ixodes scapularis (Acari: Ixodidae) under natural conditions. J Med Entomol 49(5):981-987.
8. Chowell G., Nishiura H, Bettencourt LM. 2007. Comparative estimation of the reproduction number for pandemic influenza from daily case notification data. J R Soc Interface 4(12):155-166.
9. Comin A., Klinkenberg D, Marangon S, Toffan A, Stegeman A. 2011. Transmission dynamics of low pathogenicity avian influenza infections in Turkey flocks. PLoS One. 6(10):e26935; doi:10.1371/journal.pone.0026935.
10. Degallier N., Favier C, Boulanger JP, Menkes C. 2009. Imported and autochthonous cases in the dynamics of dengue epidemics in Brazil. Rev Saude Publica 43(1):1-7.
11. Diuk-Wasser MA, Hoen AG, Cislo P, Brinkerhoff R, Hamer SA, Rowland M., et al. 2012. Human risk of infection with Borrelia burgdorferi, the Lyme disease agent, in eastern United States. Am J Trop Med Hyg 86(2):320-327.
12. Dye C., Killick-Kendrick R, Vitutia MM, Walton R, Killick-Kendrick M., Harith AE, et al. 1992. Epidemiology of canine Leishmaniasis: prevalence, incidence and basic reproduction number calculated from a cross-sectional serological survey on the island of Gozo, Malta. Parasitology 105(pt 1):35-41.
13. Elliott KA. 1998. The forests of southern Ontario. Forest Chron 74(6):850-854.
14. Environment Canada. 2013. Plots and Animations. Canadian Centre for Climate Modelling and Analysis. Available: http://www.cccma.ec.gc.ca/diagnostics/canrcm4/ canrcm4.shtml [accessed 6 December 2013].
15. Estrada-Peña A, Ruiz-Fons F, Acevedo P, Gortazar C, de la Fuente J. 2013. Factors driving the circulation and possible expansion of Crimean-Congo haemorrhagic fever virus in the western Palearctic. J Appl Microbiol 114(1):278-286.
16. Ferguson N.M., Donnelly CA, Anderson RM. 2001. The foot-andmouth epidemic in Great Britain: pattern of spread and impact of interventions. Science 292(5519):1155-1160.
17. Filipe J.A., Boussinesq M, Renz A, Collins RC, Vivas-Martinez S, Grillet M.E., et al. 2005. Human infection patterns and heterogeneous exposure in river blindness. Proc Natl Acad Sci USA 102(42):15265-15270.
18. Fine P.E., Carneiro IA. 1999. Transmissibility and persistence of oral polio vaccine viruses: implications for the global poliomyelitis eradication initiative. Am J Epidemiol 150(10):1001-1021.
19. Fitzpatrick M.C., Hampson K, Cleaveland S, Meyers LA, Townsend J.P., Galvani AP. 2012. Potential for rabies control through dog vaccination in wildlife-abundant communities of Tanzania. PLoS Negl Trop Dis 6(8):e1796; doi:10.1371/journal.pntd.0001796.
20. Fraser C., Donnelly CA, Cauchemez S, Hanage WP, Van Kerkhove M.D., Hollingsworth TD, et al. 2009. Pandemic potential of a strain of influenza A (H1N1): early findings. Science 324(5934):1557-1561.
21. Gachon P., Dibike Y. 2007. Temperature change signals in northern Canada: convergence of statistical downscaling results using two driving GCMs. Int J Climatology 27(12):1623-1641.
22. Githeko A.K., Lindsay SW, Confalonieri UE, Patz JA. 2000. Climate change and vector-borne diseases: a regional analysis. Bull World Health Organ 78(9):1136-1147.
23. Githeko A.K., Ototo EN, Guiyun Y. 2012. Progress towards understanding the ecology and epidemiology of malaria in the western Kenya highlands: opportunities and challenges for control under climate change risk. Acta Trop 121(1):19-25.
24. Gran J.M., Iversen B, Hungnes O, Aalen OO. 2010. Estimating influenza-related excess mortality and reproduction numbers for seasonal influenza in Norway, 1975-2004. Epidemiol Infect 138(11):1559-1568.
25. Gubler D.J., Reiter P, Ebi KL, Yap W, Nasci R, Patz JA. 2001. Climate variability and change in the United States: potential impacts on vector-and rodent-borne diseases. Environ Health Perspect 109(suppl 2):223-233.
26. Gulenkin V.M., Korennoy FI, Karaulov AK, Dudnikov SA. 2011. Cartographical analysis of African swine fever outbreaks in the territory of the Russian Federation and computer modeling of the basic reproduction ratio. Prev Vet Med 102(3):167-174.
27. Hagmann R., Charlwood JD, Gil V, Ferreira C, do Rosário V, Smith TA 2003. Malaria and its possible control on the island of Príncipe. Malar J 2:15; doi:10.1186/1475-2875-2-15.
28. Hamer S.A., Tsao JI, Walker ED, Hickling GJ. 2010. Invasion of the Lyme disease vector Ixodes scapularis: implications for Borrelia burgdorferi endemicity. Ecohealth 7(1):47-63.
29. Hay S.I., Guerra CA, Tatem AJ, Atkinson PM, Snow RW. 2005. Urbanization, malaria transmission, and disease burden in Africa. Nat Rev Microbiol 3(1):81-90.
30. Heffernan J.M., Smith RJ, Wahl LM. 2005. Perspectives on the basic reproductive ratio. J R Soc Interface 2(4):281-293.
31. Hutchinson M., McKenney DW, Lawrence K, Pedlar PJ. 2009. Development and testing of Canada-wide interpolated spatial models of daily minimum-maximum temperature and precipitation for 1961-2003. J Appl Meteor Climatol 48(4):725-741.
32. Kao R.R., Leathwick DM, Roberts MG, Sutherland IA. 2000. Nematode parasites of sheep: a survey of epidemiological parameters and their application in a simple model. Parasitology 121(pt 1):85-103.
33. Kilpatrick A.M., Randolph SE. 2012. Drivers, dynamics, and control of emerging vector-borne zoonotic diseases. Lancet 380(9857):1946-1955.
34. Kitala P.M., McDermott JJ, Coleman PG, Dye C. 2002. Comparison of vaccination strategies for the control of dog rabies in Machakos District, Kenya. Epidemiol Infect 129(1):215-222.
35. Laprise R., Caya D, Bergeron G, Giguère M. 1997. The formulation of André Robert MC2 (Mesoscale Compressible Community) model. Atmos-Ocean 35(suppl 1):195-220.
36. Leighton P.A., Koffi JK, Pelcat Y, Lindsay LR, Ogden NH. 2012. Predicting the speed of tick invasion: an empirical model of range expansion for the Lyme disease vector Ixodes scapularis in Canada. J Appl Ecol 49(2):457-464.
37. 0. Comput Math Methods Med 2011:527610; doi:10.1155/2011/527610.
38. Lindsay L.R., Akwar TH, Barker IK, Reive D. 1999a. Recent Establishment of an Isolated Population of Ixodes scapularis, the Vector of Lyme borreliosis, at Point Pelee National Park, Ontario [Abstract]. PRFO Proceedings, 500. Available: http:// casiopa.mediamouse.ca/wp-content/uploads/2010/05/PRFO-1999-Proceedings-p500-Lindsay-Akwar-Barker-and-Reive-Abstract.pdf [accessed 13 February 2014].
39. Lindsay L.R., Barker IK, Surgeoner GA, McEwen SA, Gillespie TJ, Robinson J.T., et al. 1995. Survival and development of Ixodes scapularis (Acari: Ixodidae) under various climatic conditions in Ontario, Canada. J Med Entomol 32(2):143-152.
40. Lindsay L.R., Mathison SW, Barker IK, McEwen SA, Gillespie TJ, Surgeoner GA. 1999b. Microclimate and habitat in relation to Ixodes scapularis (Acari: Ixodidae) populations on Long Point, Ontario, Canada. J Med Entomol 36(3):255-262.
41. Longini I.M., Halloran ME, Nizam A, Yang Y. 2004. Containing pandemic influenza with antiviral agents. Amer J Epidemiol 159(7):623-633.
42. Lord C.C., Woolhouse ME, Barnard BJ. 1997. Transmission and distribution of virus serotypes: African horse sickness in zebra. Epidemiol Infect 118(1):43-50.
43. Martens W.J., Niessen LW, Rotmans J, Jetten TH, McMichael AJ. 1995. Potential impact of global climate change on malaria risk. Environ Health Perspect 103:458-464.
44. Massad E. 2008. The elimination of Chagas' disease from Brazil. Epidemiol Infect 136(9):1153-1164.
45. Massad E., Burattini MN, Coutinho FA Lopez, LF. 2007. The 1918 influenza A epidemic in the city of São Paulo, Brazil. Med Hypotheses 68(2):442-445.
46. May R.M., Gupta S, McLean AR. 2001. Infectious disease dynamics: What characterizes a successful invader? Philos Trans R Soc Lond B Biol Sci 356(1410):901-910.
47. McFarlane NA Scinocca JF, Lazare M, Harvey R, Verseghy D, Li J. 2005. The CCCma Third Generation Atmospheric General Circulation Model (AGCM3). CCCMA, Internal Report. Available: http://www.cccma.ec.gc.ca/papers/ jscinocca/AGCM3_report.pdf [accessed 6 August 2013].
48. Meehl G.A., Boer GJ, Covey C, Latif M, Stouffer RJ. 2000. The Coupled Model Intercomparison Project (CMIP). Bull Amer Meteor Soc 81(2):313-318.
49. Mills C.E., Robins JM, Lipsitch M. 2004. Transmissibility of 1918 pandemic influenza. Nature 432(7019):904-906.
50. Mordecai E.A., Paaijmans KP, Johnson LR, Balzer C, Ben-Horin T, de Moor E, et al. 2013. Optimal temperature for malaria transmission is dramatically lower than previously predicted. Ecol Lett 16(1):22-30.
51. Morecroft M.D., Taylor ME, Oliver HR. 1998. Air and soil microclimates of deciduous woodland compared to an open site. Agric For Meteorol 90(2):141-156.
52. Morin X., Chuine I. 2006. Niche breadth, competitive strength and range size of tree species: a trade-off based framework to understand species distribution. Ecol Lett 9(2):185-195.
53. Morshed M.G., Scott JD, Fernando K, Mann RB, Durden LA. 2003. Lyme disease spirochete, Borrelia burgdorferi endemic at epicenter in Rondeau Provincial Park, Ontario. J Med Entomol. 40(1):91-94.
54. Mossong J., Muller CP. 2000. Estimation of the basic reproduction number of measles during an outbreak in a partially vaccinated population. Epidemiol Infect 124(2):273-278.
55. Mukandavire Z., Liao S, Wang J, Gaff H, Smith DL, Morris JG Jr. 2011. Estimating the reproductive numbers for the 2008-2009 cholera outbreaks in Zimbabwe. Proc Natl Acad Sci USA 108(21):8767-8772.
56. Music B., Caya D. 2007. Evaluation of the hydrological cycle over the Mississippi river basin as simulated by the Canadian Regional Climate Model (CRCM). J Hydrometeorol 8(5):969-988.
57. Nakicenovic N., Swart R. 2000. Special Report on Emissions Scenarios: A Special Report of Working Group III of the Intergovernmental Panel on Climate Change. Cambridge UK:Cambridge University Press.
58. Natural Resources Canada. 2013. Additions and Deletions of Forest Area. Available: http://www.nrcan.gc.ca/ forests/canada/sustainable-forest-management/criteriaindicators/ 13233 [accessed 6 December 2013].
59. 0 from early epidemic growth data. Int J Environ Res Public Health 7(1):291-302.
60. Nishiura H. 2010b. Time variations in the generation time of an infectious disease: implications for sampling to appropriately quantify transmission potential. Math Biosci Eng 7(4):851-869.
61. Ogden N.H., Barker IK, Beauchamp G, Brazeau S, Charron DF, Maarouf A., et al. 2006a. Investigation of ground level and remote-sensed data for habitat classification and prediction of survival of Ixodes scapularis in habitats of southeastern Canada. J Med Entomol 43(2):403-414.
62. Ogden N.H., Bigras-Poulin M, O'Callaghan CJ, Barker IK, Kurtenbach K., Lindsay LR, et al. 2007. Vector seasonality, host infection dynamics and fitness of pathogens transmitted by the tick Ixodes scapularis. Parasitology 134(2):209-227.
63. Ogden N.H., Bigras-Poulin M, O'Callaghan CJ, Barker IK, Lindsay L.R., Maarouf A, et al. 2005. A dynamic population model to investigate effects of climate on geographic range and seasonality of the tick Ixodes scapularis. Int J Parasitol 35(4):375-389.
64. Ogden N.H., Bouchard C, Kurtenbach K, Margos G, Lindsay LR, Trudel L., et al. 2010. Active and passive surveillance and phylogenetic analysis of Borrelia burgdorferi elucidate the process of Lyme disease risk emergence in Canada. Environ Health Perspect 118:909-914; doi:10.1289/ ehp.0901766.
65. Ogden N.H., Lindsay LR, Beauchamp G, Charron D, Maarouf A, O'Callaghan CJ, et al. 2004. Investigation of relationships between temperature and developmental rates of tick Ixodes scapularis (Acari: Ixodidae) in the laboratory and field. J Med Entomol 41(4):622-633.
66. Ogden N.H., Lindsay LR, Leighton P. 2013. Predicting the rate of invasion of the agent of Lyme disease, Borrelia burgdorferi in North America. J Appl Ecol 50(2):510-518.
67. Ogden N.H., Lindsay LR, Morshed M, Sockett PN, Artsob H. 2009. The emergence of Lyme disease in Canada. CMAJ 180(12):1221-1224.
68. Ogden N.H., Maarouf A, Barker IK, Bigras-Poulin M, Lindsay LR, Morshed M.G., et al. 2006b. Climate change and the potential for range expansion of the Lyme disease vector Ixodes scapularis in Canada. Int J Parasitol 36(1):63-70.
69. Ogden N.H., St-Onge L, Barker IK, Brazeau S, Bigras-Poulin M, Charron D.F., et al. 2008. Risk maps for range expansion of the Lyme disease vector, Ixodes scapularis, in Canada now and with climate change. Int J Health Geogr 7:24; doi:10.1186/1476-072X-7-24.
70. Padmanabha H., Durham D, Correa F, Diuk-Wasser M, Galvani A. 2012. The interactive roles of Aedes aegypti super-production and human density in dengue transmission. PLoS Negl Trop Dis 6(8):e1799; doi:10.1371/journal. pntd.0001799.
71. Patz J.A., Martens WJ, Focks DA, Jetten TH. 1998. Dengue fever epidemic potential as projected by general circulation models of global climate change. Environ Health Perspect 106:147-153.
72. Pinho S.T., Ferreira CP, Esteva L, Barreto FR, Morato e Silva V.C., et al. 2010. Modelling the dynamics of dengue real epidemics. Philos Transact A Math Phys Eng Sci 368(1933):5679-56793.
73. 0) for measles viruses observed in recent outbreaks lower than in the pre-vaccination era? [Letter]. Euro Surveill 17(31):22.
74. Poletti P., Messeri G, Ajelli M, Vallorani R, Rizzo C, Merler S. 2011. Transmission potential of Chikungunya virus and control measures: the case of Italy. PLoS One 6(5):e18860; doi:10.1371/journal.pone.0018860.
75. Pourbohloul B., Ahued A, Davoudi B, Meza R, Meyers LA, Skowronski D.M., et al. 2009. Initial human transmission dynamics of the pandemic (H1N1) 2009 virus in North America. Influenza Other Respir Viruses 3(5):215-222.
76. Quinnell R.J., Courtenay O, Garcez L, Dye C. 1997. The epidemiology of canine Leishmaniasis: transmission rates estimated from a cohort study in Amazonian Brazil. Parasitology 115(pt 2):143-156.
77. Reiter P. 2001. Climate change and mosquito-borne disease. Environ Health Perspect 109(suppl 1):141-161.
78. Reiter P., Thomas CJ, Atkinson PM, Hay SI, Randolph SE, Rogers D.J., et al. 2004. Global warming and malaria: a call for accuracy. Lancet Infect Dis 4(6):323-324.
79. Reithinger R., Espinoza JC, Davies CR. 2003. The transmission dynamics of canine American cutaneous leishmaniasis in Huánuco, Peru. Am J Trop Med Hyg 69(5):473-480.
80. Rogers D.J., Randolph SE. 2000. The global spread of malaria in a future, warmer world. Science 289(5485):1763-1766.
81. Santman-Berends IM, Stegeman JA, Vellema P, van Schaik G. 2013. Estimation of the reproduction ratio (R0) of bluetongue based on serological field data and comparison with other BTV transmission models. Prev Vet Med 108(4):276-284.
82. Scinocca J.F., McFarlane NA, Lazare M, Li J, Plummer D. 2008. The CCCma third generation AGCM and its extension into the middle atmosphere. Atmos Chem Phys Discuss 8(2):7883-7930.
83. Scott J.D., Fernando K, Durden LA, Morshed MG. 2004. Lyme disease spirochete, Borrelia burgdorferi, endemic in epicenter at Turkey Point, Ontario. J Med Entomol 41(2):226-230.
84. Service MW. 1997. Mosquito (Diptera: Culicidae) dispersal-the long and short of it. J Med Entomol 34(3):579-588.
85. Smith D.L., McKenzie FE, Snow RW, Hay SI. 2007. Revisiting the basic reproductive number for malaria and its implications for malaria control. PLoS Bio. 5(3):e42; doi:10.1371/journal. pbio.0050042.
86. Stadler T., Kouyos R, von Wyl V, Yerly S, Böni J, Bürgisser P, et al. 2012. Estimating the basic reproductive number from viral sequence data. Mol Biol Evol 29(1):347-357.
87. Stegeman A., Bouma A, Elbers AR, de Jong MC, Nodelijk G, de Klerk F, et al. 2004. Avian influenza A virus (H7N7) epidemic in the Netherlands in 2003: course of the epidemic and effectiveness of control measures. J Infect Dis 190(12):2088-2095.
88. Tanser F.C., Sharp B, le Sueur D. 2003. Potential effect of climate change on malaria transmission in Africa. Lancet 362(9398):1792-1798.
89. Truscott J., Fraser C, Cauchemez S, Meeyai A, Hinsley W, Donnelly C.A., et al. 2012. Essential epidemiological mechanisms underpinning the transmission dynamics of seasonal influenza. J R Soc Interface 9(67):304-312.
90. Tuite A.R., Greer AL, Whelan M, Winter AL, Lee B, Yan P, et al. 2010. Estimated epidemiologic parameters and morbidity associated with pandemic H1N1 influenza. CMAJ 182(2):131-136.
91. Vynnycky E., Trindall A, Mangtani P. 2007. Estimates of the reproduction numbers of Spanish influenza using morbidity data. Int J Epidemiol 36(4):881-889.
92. Watson T.G., Anderson RC. 1976. Ixodes scapularis Say on white-tailed deer (Odocoileus virginianus) from Long Point, Ontario. J Wildl Dis 12(1):66-71.
93. White L., Wallinga J, Finelli L, Reed C, Riley S, Lipsitch M, et al. 2009. Estimation of the reproductive number and the serial interval in early phase of the influenza A/H1N1 pandemic in the USA. Influenza Other Respir Viruses 3(6):267-276.
94. Wood C.L., Lafferty KD. 2013. Biodiversity and disease: a synthesis of ecological perspectives on Lyme disease transmission. Trends Ecol Evol 28(4):239-247.
95. Wu X., Duvvuri VR, Lou Y, Ogden NH, Pelcat Y, Wu J. 2013. Developing a temperature-driven map of the basic reproductive number of the emerging tick vector of Lyme disease Ixodes scapularis in Canada. J Theor Biol 319:50-61.
96. Xiao Y., Tang S, Zhou Y, Smith RJ, Wu J, Wang N. 2013. Predicting the HIV/AIDS epidemic and measuring the effect of mobility in mainland China. J Theor Biol 317:2712-85.
97. Yang Y., Sugimoto JD, Halloran ME, Basta NE, Chao DL, Matrajt L., Potter G, et al. 2009. The transmissibility and control of pandemic influenza A (H1N1) virus. Science 326(5953):729-733.
98. Zhang Z., Chen D, Ward MP, Jiang Q. 2012. Transmissibility of the highly pathogenic avian influenza virus, subtype H5N1 in domestic poultry: a spatio-temporal estimation at the global scale. Geospat Health 7(1):135-143.