Interdisciplinary Perspectives on Infectious Diseases
Volume 2009 (2009), Article ID 385487, 13 pages
doi:10.1155/2009/385487
Review Article

Climate Change and Malaria in Canada: A Systems Approach

L. Berrang-Ford,1 J. D. MacLean,2 Theresa W. Gyorkos,2,3,4 J. D. Ford,1 and N. H. Ogden5

1Department of Geography, McGill University, 805 Sherbrooke Street West, Montreal, QC, H3A 2K6, Canada
2McGill University Centre for Tropical Diseases, Montreal General Hospital, Department of Medicine, McGill University, Montreal, QC, H3G 1A4, Canada
3Division of Clinical Epidemiology, McGill University Health Centre, Royal Victoria Hospital, V Building, 687 Pine Avenue West, Montreal, QC, H3A 1A1, Canada
4Department of Epidemiology, Biostatistics and Occupational Health, McGill University, Montreal, QC, H3A 1A2, Canada
5Public Health Agency of Canada and Faculté de médecine vétérinaire, Université de Montréal, CP 5000, Saint Hyacinthe, QC, J2S 7C6, Canada

Received 9 January 2008; Accepted 27 March 2008

Academic Editor: Bettina Fries

Copyright © 2009 L. Berrang-Ford et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. R. Zucker, “Changing patterns of autochthonous malaria transmission in the United States: a review of recent outbreaks,” Emerging Infectious Diseases, vol. 2, no. 1, pp. 37–43, 1996.
  2. M. Parry, O. Canziani, J. Palutikof, P. van der Linden, and C. Hanson, Eds., Climate Change 2007: Impacts, Adaptation and Vulnerability, M. Parry, O. Canziani, J. Palutikof, P. van der Linden, and C. Hanson, Eds., Working Group II Contribution to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change, Cambridge University Press, Cambridge, UK, 2007.
  3. A. J. McMichael, D. H. Campbell-Lendrum, C. F. Corvalán, et al., Eds., Climate Change and Human Health: Risks and Responses, A. J. McMichael, D. H. Campbell-Lendrum, C. F. Corvalán, et al., Eds., World Health Organization, Geneva, Switzerland, 2003.
  4. A. McMichael, D. H. Campbell-Lendrum, R. S. Kovats, et al., “Climate change,” in Comparative Quantification of Health Risks: Global and Regional Burden of Disease Due to Selected Major Risk Factors, M. Ezzati, A. Lopez, A. Rodgers, S. Vander Hoorn, and C. Murray, Eds., pp. 1543–1649, World Health Organization, Geneva, Switzerland, 2004.
  5. A. J. McMichael, R. E. Woodruff, and S. Hales, “Climate change and human health: present and future risks,” The Lancet, vol. 367, no. 9513, pp. 859–869, 2006. View at Publisher · View at Google Scholar · View at PubMed
  6. M. W. Parkes, L. Bienen, J. Breilh, et al., “All hands on deck: transdisciplinary approaches to emerging infectious disease,” EcoHealth, vol. 2, no. 4, pp. 258–272, 2005. View at Publisher · View at Google Scholar
  7. J. A. Patz and J. M. Balbus, “Methods for assessing public health vulnerability to global climate change,” Climate Research, vol. 6, no. 2, pp. 113–125, 1996. View at Publisher · View at Google Scholar
  8. P. A. Stott, D. A. Stone, and M. R. Allen, “Human contribution to the European heatwave of 2003,” Nature, vol. 432, no. 7017, pp. 610–614, 2004. View at Publisher · View at Google Scholar · View at PubMed
  9. M. van Lieshout, R. S. Kovats, M. T. J. Livermore, and P. Martens, “Climate change and malaria: analysis of the SRES climate and socio-economic scenarios,” Global Environmental Change, vol. 14, no. 1, pp. 87–99, 2004. View at Publisher · View at Google Scholar
  10. B. A. Wilcox and R. R. Colwell, “Emerging and reemerging infectious diseases: biocomplexity as an interdisciplinary paradigm,” EcoHealth, vol. 2, no. 4, pp. 244–257, 2005. View at Publisher · View at Google Scholar
  11. A. J. McMichael and R. E. Woodruff, “Detecting the health effects of environmental change: scientific and political challenge,” EcoHealth, vol. 2, no. 1, pp. 1–3, 2005. View at Publisher · View at Google Scholar
  12. S. O. Vanwambeke, E. F. Lambin, M. P. Eichhorn, et al., “Impact of land-use change on dengue and malaria in northern Thailand,” EcoHealth, vol. 4, no. 1, pp. 37–51, 2007. View at Publisher · View at Google Scholar
  13. J. N. Eisenberg, M. A. Desai, K. Levy, et al., “Environmental determinants of infectious disease: a framework for tracking causal links and guiding public health research,” Environmental Health Perspectives, vol. 115, no. 8, pp. 1216–1223, 2007.
  14. M. Susser and E. Susser, “Choosing a future for epidemiology—II: from black box to Chinese boxes and eco-epidemiology,” American Journal of Public Health, vol. 86, no. 5, pp. 674–677, 1996.
  15. D. Waltner-Toews, Ecosystem Sustainability and Health: A Practical Approach, Cambridge University Press, Cambridge, UK, 2004.
  16. D. Waltner-Toews and J. Kay, “The evolution of an ecosystem approach: the diamond schematic and an adaptive methodology for ecosystem sustainability and health,” Ecology and Society, vol. 10, no. 1, p. 38, 2005.
  17. N. Krieger, “Theories for social epidemiology in the 21st century: an ecosocial perspective,” International Journal of Epidemiology, vol. 30, no. 4, pp. 668–677, 2001. View at Publisher · View at Google Scholar
  18. R. Few, “Health and climatic hazards: framing social research on vulnerability, response and adaptation,” Global Environmental Change, vol. 17, no. 2, pp. 281–295, 2007. View at Publisher · View at Google Scholar
  19. B. L. Turner, II, R. E. Kasperson, P. A. Matsone, et al., “A framework for vulnerability analysis in sustainability science,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 14, pp. 8074–8079, 2003. View at Publisher · View at Google Scholar · View at PubMed
  20. L. Berrang-Ford, D. Waltner-Toews, D. Charron, M. Odiit, J. McDermott, and B. Smit, “Sleeping sickness in southeastern Uganda: a systems approach,” EcoHealth, vol. 2, no. 3, pp. 183–194, 2005. View at Publisher · View at Google Scholar
  21. M. Parkes, R. Panelli, and P. Weinstein, “Converging paradigms for environmental health theory and practice,” Environmental Health Perspectives, vol. 111, no. 5, pp. 669–675, 2003.
  22. D. Waltner-Toews, J. J. Kay, C. Neudoerffer, and T. Gitau, “Perspective changes everything: managing ecosystems from the inside out,” Frontiers in Ecology and the Environment, vol. 1, no. 1, pp. 23–30, 2003. View at Publisher · View at Google Scholar
  23. B. A. Wilcox and D. J. Gubler, “Disease ecology and the global emergence of zoonotic pathogens,” Environmental Health and Preventive Medicine, vol. 10, no. 5, pp. 263–272, 2005. View at Publisher · View at Google Scholar
  24. T. Allen and T. Starr, Hierarchy: Perspectives for Ecological Complexity, University of Chicago Press, Chicago, Ill, USA, 1982.
  25. P. Checkland and J. Scholes, Soft Systems Methodology in Action, John Wiley & Sons, Chichester, UK, 1990.
  26. J. J. Kay, H. A. Regier, M. Boyle, and G. Francis, “An ecosystem approach for sustainability: addressing the challenge of complexity,” Futures, vol. 31, no. 7, pp. 721–742, 1999. View at Publisher · View at Google Scholar
  27. J. Puccia and R. Levins, Qualitative Modeling of Complex Systems, Harvard University Press, Cambridge, Mass, USA, 1985.
  28. D. Waltner-Toews, J. Kay, T. P. Murray, and C. Neudoerffer, “Adaptive methodology for ecosystem sustainability and health (AMESH): an introduction,” in Community Operational Research: Systems Thinking for Community Development, G. Midgley and A. Ochoa-Arias, Eds., Kluwer Academic Publishers, Boston, Mass, USA, 2004.
  29. Public Health Agency of Canada, “National Notifiable Diseases Online: Notifiable disease incidence by year, 1989–2004,” 2006.
  30. R. Darsie and R. Ward, Identification and Geographical Distribution of the Mosquitoes: of North America, North of Mexico, American Mosquito Control Association, Fresno, Calif, USA, 1981.
  31. R. Darsie and R. Ward, Identification and Geographical Distribution of the Mosquitoes: of North America, North of Mexico, University Press of Florida, Gainesville, Fla, USA, 2005.
  32. A. Kiszewski, A. Mellinger, A. Spielman, P. Malaney, S. E. Sachs, and J. Sachs, “A global index representing the stability of malaria transmission,” American Journal of Tropical Medicine and Hygiene, vol. 70, no. 5, pp. 486–498, 2004.
  33. R. S. Levine, A. T. Peterson, and M. Q. Benedict, “Distribution of members of Anopheles quadrimaculatus Say s.l. (Diptera: Culicidae) and implications for their roles in malaria transmission in the United States,” Journal of Medical Entomology, vol. 41, no. 4, pp. 607–613, 2004.
  34. WHO, “World Malaria Report,” 2005.
  35. W. R. Horsefall, Mosquitoes: Their Bionomics and Relation to Diseases, Ronald Press, New York, NY, USA, 1955.
  36. F. O'Rourke, “Anopheles and the problem of malaria in Canada,” Canadian Entomologist, vol. 91, no. 6, pp. 346–358, 1959.
  37. D. Wood, P. Dang, and R. Ellis, The Mosquitoes of Canada, Canadian Government Publishing Services, Ottawa, Ont, Canada, 1979.
  38. M. Baqi, K. Gamble, J. S. Keystone, and K. C. Kain, “Malaria: probably locally acquired in Toronto, Ontario,” Canadian Journal of Infectious Diseases and Medical Microbiology, vol. 9, no. 3, pp. 183–184, 1998.
  39. M. J. Eliades, S. Shah, P. Nguyen-Dinh, et al., “Malaria surveillance—United States, 2003,” Morbidity and Mortality Weekly Report, vol. 54, no. 2, pp. 25–40, 2005.
  40. S. J. Filler, J. R. MacArthur, M. Parise, et al., “Locally acquired mosquito-transmitted malaria: a guide for investigations in the United States,” Morbidity and Mortality Weekly Report, vol. 55(R13), pp. 1–9, 2006.
  41. T. H. Holtz, S. P. Kachur, J. R. MacArthur, et al., “Malaria surveillance—United States, 1998,” Morbidity and Mortality Weekly Report, vol. 50, no. 5, pp. 1–20, 2001.
  42. J. R. MacArthur, A. R. Levin, M. Mungai, et al., “Malaria surveillance—United States, 1997,” Morbidity and Mortality Weekly Report, vol. 50(SS01), no. 1, pp. 25–44, 2001.
  43. R. D. Newman, A. M. Barber, J. Roberts, T. Holtz, R. W. Steketee, and M. E. Parise, “Malaria surveillance—United States, 1999,” Morbidity and Mortality Weekly Report, vol. 51, no. 1, pp. 15–28, 2002.
  44. S. Shah, S. Filler, L. M. Causer, et al., “Malaria surveillance—United States, 2002,” Morbidity and Mortality Weekly Report, vol. 53, no. 1, pp. 21–34, 2004.
  45. H. A. Williams, J. Roberts, S. P. Kachur, et al., “Malaria surveillance—United States, 1995,” Morbidity and Mortality Weekly Report, vol. 48, no. 1, pp. 1–23, 1999.
  46. Environment Canada, “Environment Canada National Climate Data and Information Archive (1970–2003) and Canada Climate Data Online (2004–2006),” June 2007, http://climate.weatheroffice.ec.gc.ca/Welcome_e.html.
  47. CCCma, “Canadian Centre for Climate Modeling and Analysis—Models. Environment Canada,” June 2007, http://www.cccma.ec.gc.ca/models/models.shtml.
  48. J. Houghton, Y. Ding, D. J. Griggs, et al., Eds., Climate Change 2001: the Scientific Basis, J. Houghton, Y. Ding, D. J. Griggs, et al., Eds., Working Group I Contribution to the Third Assessment Report of the Intergovernmental Panel on Climate Change, Cambridge University Press, Cambridge, UK, 2001.
  49. N. H. Ogden, A. Maarouf, I. K. Barker, et al., “Climate change and the potential for range expansion of the Lyme disease vector Ixodes scapularis in Canada,” International Journal for Parasitology, vol. 36, no. 1, pp. 63–70, 2006. View at Publisher · View at Google Scholar · View at PubMed
  50. S. E. Randolph and D. J. Rogers, “Tick-borne disease systems: mapping geographic and phylogenetic space,” Advances in Parasitology, vol. 62, pp. 263–291, 2006. View at Publisher · View at Google Scholar · View at PubMed
  51. P. Reiter, “Global-warming and vector-borne disease in temperate regions and at high altitude,” The Lancet, vol. 351, no. 9105, pp. 839–840, 1998. View at Publisher · View at Google Scholar
  52. G. Fisk, “Malaria and the Anopheles mosquito in Canada,” Canadian Medical Association Journal, vol. 25, no. 6, pp. 679–683, 1931.
  53. J. McLintock and J. Iverson, “Mosquitoes and human disease in Canada,” Canadian Entomologist, vol. 107, pp. 695–704, 1975.
  54. D. F. Charron, “Potential impacts of global warming and climate change on the epidemiology of zoonotic diseases in Canada,” Canadian Journal of Public Health, vol. 93, no. 5, pp. 334–335, 2002.
  55. CATMAT, “Canadian recommendations for the prevention and treatment of malaria among international travelers,” Canadian Communicable Diseases Report, vol. 30, supplement 1, pp. 1–62, 2004.
  56. PHAC, “West Nile Virus MONITOR, Human Surveillance 2002–2006,” 2007.
  57. R. Stoppacher and S. P. Adams, “Malaria deaths in the United States: case report and review of deaths, 1979–1998,” Journal of Forensic Sciences, vol. 48, no. 2, pp. 404–408, 2003.
  58. M. Ndao, E. Bandyayera, E. Kokoskin, T. W. Gyorkos, J. D. MacLean, and B. J. Ward, “Comparison of blood smear, antigen detection, and nested-PCR methods for screening refugees from regions where malaria is endemic after a malaria outbreak in Québec, Canada,” Journal of Clinical Microbiology, vol. 42, no. 6, pp. 2694–2700, 2004. View at Publisher · View at Google Scholar · View at PubMed
  59. J. D. MacLean, A.-M. Demers, M. Ndao, E. Kokoskin, B. J. Ward, and T. W. Gyorkos, “Malaria epidemics and surveillance systems in Canada,” Emerging Infectious Diseases, vol. 10, no. 7, pp. 1195–1201, 2004.
  60. M. Ndao, E. Bandyayera, E. Kokoskin, et al., “Malaria “epidemic” in Québec: diagnosis and response to imported malaria,” Canadian Medical Association Journal, vol. 172, no. 1, pp. 46–50, 2005. View at Publisher · View at Google Scholar · View at PubMed
  61. P. Wilton, “Malaria may be on move to “tropical” Canada,” Canadian Medical Association Journal, vol. 158, no. 2, p. 160, 1998.
  62. Statistics Canada, “Census of Canada,” 2001.
  63. I. W. Sherman, Ed., Malaria: Parasite Biology, Pathogenisis, and Protection, I. W. Sherman, Ed., ASM Press, Washington, DC, USA, 1998.
  64. M. J. Bouma and H. J. Van der Kaay, “Epidemic malaria in India and the El Niño southern oscillation,” The Lancet, vol. 344, no. 8937, pp. 1638–1639, 1994. View at Publisher · View at Google Scholar
  65. M. J. Bouma, H. E. Sondorp, and H. J. van der Kaay, “Climate change and periodic epidemic malaria,” The Lancet, vol. 343, no. 8910, p. 1440, 1994. View at Publisher · View at Google Scholar
  66. R. S. Kovats, M. J. Bouma, S. Hajat, E. Worrall, and A. Haines, “El Niño and health,” The Lancet, vol. 362, no. 9394, pp. 1481–1489, 2003. View at Publisher · View at Google Scholar · View at PubMed
  67. G. MacDonald, “The analysis of malaria epidemics,” Tropical Disease Bulletin, vol. 50, no. 10, pp. 871–892, 1954.
  68. J. Sunstrum, L. J. Elliott, L. M. Barat, E. D. Walker, and J. R. Zucker, “Probable autochthonous Plasmodium vivax malaria transmission in Michigan: case report and epidemiological investigation,” American Journal of Tropical Medicine and Hygiene, vol. 65, no. 6, pp. 949–953, 2001.
  69. IPCC, “Summary for policymakers,” in Climate Change 2007: Impacts, Adaptation and Vulnerability, M. L. Parry, O. F. Canziani, J. P. Palutikof, P. J. van der Linden, and C. E. Hanson, Eds., Working Group II Contribution to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change, pp. 7–22, Cambridge University Press, Cambridge, UK, 2007.
  70. C. F. Mantel, C. Klose, S. Scheurer, R. Vogel, A.-L. Wesirow, and U. Bienzle, “Plasmodium falciparum malaria acquired in Berlin, Germany,” The Lancet, vol. 346, no. 8970, pp. 320–321, 1995. View at Publisher · View at Google Scholar
  71. J. A. Patz and R. S. Kovats, “Hotspots in climate change and human health,” British Medical Journal, vol. 325, no. 7372, pp. 1094–1098, 2002. View at Publisher · View at Google Scholar
  72. R. S. Kovats, D. H. Campbell-Lendrum, A. J. McMichael, A. Woodward, and J. S. H. Cox, “Early effects of climate change: do they include changes in vector-borne disease?,” Philosophical Transactions of the Royal Society B, vol. 356, no. 1411, pp. 1057–1068, 2001. View at Publisher · View at Google Scholar · View at PubMed
  73. W. J. M. Martens, L. W. Niessen, J. Rotmans, T. H. Jetten, and A. J. McMichael, “Potential impact of global climate change on malaria risk,” Environmental Health Perspectives, vol. 103, no. 5, pp. 458–464, 1995. View at Publisher · View at Google Scholar
  74. W. J. Martens, T. H. Jetten, J. Rotmans, and L. W. Niessen, “Climate change and vector-borne diseases: a global modelling perspective,” Global Environmental Change, vol. 5, no. 3, pp. 195–209, 1995. View at Publisher · View at Google Scholar
  75. W. J. M. Martens, T. H. Jetten, and D. A. Focks, “Sensitivity of malaria, schistosomiasis and dengue to global warming,” Climatic Change, vol. 35, no. 2, pp. 145–156, 1997. View at Publisher · View at Google Scholar
  76. M. van Lieshout, R. S. Kovats, M. T. J. Livermore, and P. Martens, “Climate change and malaria: analysis of the SRES climate and socio-economic scenarios,” Global Environmental Change, vol. 14, no. 1, pp. 87–99, 2004. View at Publisher · View at Google Scholar
  77. S. I. Hay, G. D. Shanks, D. I. Stern, R. W. Snow, S. E. Randolph, and D. J. Rogers, “Climate variability and malaria epidemics in the highlands of East Africa,” Trends in Parasitology, vol. 21, no. 2, pp. 52–53, 2005. View at Publisher · View at Google Scholar · View at PubMed
  78. A. Githeko and W. Ndegwa, “Predicting malaria epidemics in the Kenyan highlands using climate data: a tool for decision makers,” Global Change & Human Health, vol. 2, no. 1, pp. 54–63, 2001. View at Publisher · View at Google Scholar
  79. P. Martens, R. S. Kovats, S. Nijhof, et al., “Climate change and future populations at risk of malaria,” Global Environmental Change, vol. 9, pp. S89–S107, 1999. View at Publisher · View at Google Scholar
  80. C. Thomas, “Malaria: a changed climate in Africa?,” Nature, vol. 427, no. 6976, pp. 690–691, 2004. View at Publisher · View at Google Scholar · View at PubMed
  81. C. J. Thomas, G. Davies, and C. E. Dunn, “Mixed picture for changes in stable malaria distribution with future climate in Africa,” Trends in Parasitology, vol. 20, no. 5, pp. 216–220, 2004. View at Publisher · View at Google Scholar · View at PubMed
  82. J. Small, S. J. Goetz, and S. I. Hay, “Climatic suitability for malaria transmission in Africa, 1911–1995,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 26, pp. 15341–15345, 2003. View at Publisher · View at Google Scholar · View at PubMed
  83. P. H. Martin and M. G. Lefebvre, “Malaria and climate: sensitivity of malaria potential transmission to climate,” Ambio, vol. 24, no. 4, pp. 200–207, 1995.
  84. W. J. M. Martens, L. W. Niessen, J. Rotmans, T. H. Jetten, and A. J. McMichael, “Potential impact of global climate change on malaria risk,” Environmental Health Perspectives, vol. 103, no. 5, pp. 458–464, 1995. View at Publisher · View at Google Scholar
  85. D. J. Rogers and S. E. Randolph, “The global spread of malaria in a future, warmer world,” Science, vol. 289, no. 5485, pp. 1763–1766, 2000. View at Publisher · View at Google Scholar · View at PubMed
  86. K. G. Kuhn, D. H. Campbell-Lendrum, B. Armstrong, and C. R. Davies, “Malaria in Britain: past, present, and future,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 17, pp. 9997–10001, 2003. View at Publisher · View at Google Scholar · View at PubMed
  87. D. Charron, D. Waltner-Toews, and A. Maarouf, “A synopsis of known and potential diseases and parasites associated with climate change,” Ministry of Natural Resources, Ontario Forest Research Institute, Sault Ste. Marie, Ont, Canada, 2003.
  88. Environment Canada, “Climate Change Scenarios Network,” August 2007, http://www.ccsn.ca/index-e.html.
  89. NR-CAN, “Natural Resources Canada, The Atlas of Canada: Climate change,” August 2007, http://atlas.nrcan.gc.ca/site/english/maps/climatechange#potentialimpacts.
  90. P. R. Epstein, “West nile virus and the climate,” Journal of Urban Health, vol. 78, no. 2, pp. 367–371, 2001. View at Publisher · View at Google Scholar · View at PubMed
  91. P. R. Epstein, “Climate change and emerging infectious diseases,” Microbes and Infection, vol. 3, no. 9, pp. 747–754, 2001. View at Publisher · View at Google Scholar
  92. P. Gosselin, G. Lebel, S. Rivest, and M. Douville-Fradet, “The integrated system for public health monitoring fo West Nile virus (ISPHM-WNV): a real-time GIS for surviellance and decision-making,” International Journal of Health Geographics, vol. 4, article 21, pp. 1–12, 2005. View at Publisher · View at Google Scholar · View at PubMed
  93. Health Canada, “Canadian Climate Change and Health Vulnerability Assessment,” 2007, Government of Canada: Ottawa, Canada.
  94. D. Lemmen and F. Warren, Eds., Climate Change Impacts and Adaptation: A Canadian Perspective, D. Lemmen and F. Warren, Eds., Natural Resources Canada (NR-CAN), Ottawa, Canada, 2007.
  95. C. B. Bradley, M. H. Zaki, D. G. Graham, et al., “Probable locally acquired mosquito transmitted Plasmodium vivax infection—Suffolk County, New York, 1999,” Morbidity and Mortality Weekly Report, vol. 49, no. 22, pp. 495–298, 2000.
  96. R. Bradley, “Past global changes and their significance for future,” Quarternary Science Reviews, vol. 19, no. 1–5, pp. 391–402, 2000. View at Publisher · View at Google Scholar
  97. D. L. Smith, F. E. McKenzie, R. W. Snow, and S. I. Hay, “Revisiting the basic reproductive number for malaria and its implications for malaria control,” PLoS Biology, vol. 5, no. 3, pp. 531–542, 2007. View at Publisher · View at Google Scholar · View at PubMed
  98. K. C. Kain, M. A. Harrington, S. Tennyson, and J. S. Keystone, “Imported malaria: prospective analysis of problems in diagnosis and management,” Clinical Infectious Diseases, vol. 27, no. 1, pp. 142–149, 1998. View at Publisher · View at Google Scholar
  99. S. W. Lindsay and W. J. M. Martens, “Malaria in the African highlands: past, present and future,” Bulletin of the World Health Organization, vol. 76, no. 1, pp. 33–45, 1998.
  100. A. Schoepke, R. Steffen, and N. Gratz, “Effectiveness of personal protection measures against mosquito bites for malaria prophylaxis in travelers,” Journal of Travel Medicine, vol. 5, no. 4, pp. 188–192, 1998. View at Publisher · View at Google Scholar
  101. P. Martens and L. Hall, “Malaria on the move: human population movement and malaria transmission,” Emerging Infectious Diseases, vol. 6, no. 2, pp. 103–109, 2000.
  102. P. Muentener, P. Schlagenhauf, and R. Steffen, “Imported malaria (1985–1995): trends and perspectives,” Bulletin of the World Health Organization, vol. 77, no. 7, pp. 560–566, 1999.
  103. Statistics Canada, “Immigrant population by place of birth and period of immigration (2001 Census),” June 2007, http://www40.statcan.ca/l01/cst01/demo24a.htm.
  104. Statistics Canada, “Tourism Statistical Digest,” 2001, Catalogue N. 87-403-XIE.
  105. R. Slinger, A. Giulivi, M. Bodie-Collins, et al., “Transfusion-transmitted malaria in Canada,” Canada Communicable Disease Report, vol. 25, no. 6, pp. 53–62, 1999.
  106. M. J. Bouma, C. Dye, and H. J. van der Kaay, “Falciparum malaria and climate change in the northwest frontier province of Pakistan,” American Journal of Tropical Medicine and Hygiene, vol. 55, no. 2, pp. 131–137, 1996.
  107. NOAA, “El Niño. National Oceanic and Atmospheric Administration,” April 2007, http://www.pmel.noaa.gov/tao/elnino/nino-home.html.
  108. J. de Zulueta, S. M. Mujtaba, and I. H. Shah, “Malaria control and long-term periodicity of the disease in Pakistan,” Transactions of the Royal Society of Tropical Medicine and Hygiene, vol. 74, no. 5, pp. 624–632, 1980. View at Publisher · View at Google Scholar
  109. P. Bloland, “Drug Resistance in Malaria, WHO Document WHO/CDS/CSR/DRS/2001.4,” Department of Communicable Disease Surveillance and Response, World Health Organization, May 2007, http://www.who.int/csr/resources/publications/drugresist/malaria.pdf.