Global Warming and Trans-Boundary Movement of Waterborne Microbial Pathogens

  • Nicholas J. Ashbolt


Potential ramifications of climate change, as they relate to waterborne pathogens (primarily viruses, bacterial and parasitic protozoa), are the focus of this chapter. It seems clear that climate change will impact on waterborne pathogens in various ways (Rose et al. 2001), pertinent to transboundary issues are: (1) increases in intense storm events (increasing sewage/animal waste flows into waterways/aquifers) (Charron et al. 2004; Schijven and de Roda Husman 2005; Yang and Goodrich 2009; De Toffol et al. 2009; Richardson et al. 2009); (2) warmer surface water temperatures or salinity changes (for increased autochthonous pathogen growth) (Niemi et al. 2004; Koelle et al. 2005; Lebarbenchon et al. 2008); and (3) changes in food production, as most obvious in animal diseases (Lightner et al. 1997; Rapoport and Shimshony 1997), but also of concern with zoonoses and from changes in social behavior (Schwab et al. 1998; Nancarrow et al. 2008; CDC 2009a). When considering trans-boundary effects on waterborne pathogens, it is therefore the flow of pathogens in surface water (fresh and marine) and in groundwater, as well as in the varying ways water is used/reused in association with human activities (e.g., food production) that are the trans-boundary issues discussed in this chapter (examples in Table 5.1). Changes in infectious and vector-borne diseases associated with rising sea levels, losses of habitat, international travel etc. are not addressed in this chapter.


Ballast Water Parasitic Protozoan Mycobacterium Avium Diarrheal Disease Avium Complex Mycobacterium 
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  1. Ashbolt NJ, Grabow WOK, Snozzi M (2001) Indicators of microbial water quality. In: Fewtrell L, Bartram J (eds) Water quality: guidelines, standards and health risk assessment and management for water-related infectious disease. IWA, London, pp 289–315 ( Chapter 13)Google Scholar
  2. Banyai K, Bogdan A, Domonkos G, Kisfali P, Molnar P, Toth A, Melegh B, Martella V, Gentsch JR, Szucs G (2009) Genetic diversity and zoonotic potential of human rotavirus strains, 2003–2006, Hungary. J Med Virol 81:362–370CrossRefGoogle Scholar
  3. Bednarska M, Bajer A, Sinski E, Girouard AS, Tamang L, Graczyk TK (2007) Fluorescent in situ hybridization as a tool to retrospectively identify Cryptosporidium parvum and Giardia lamblia in samples from terrestrial mammalian wildlife. Parasitol Res 100:455–460CrossRefGoogle Scholar
  4. Bettelheim KA (2007) The non-O157 shiga-toxigenic (verocytotoxigenic) Escherichia coli; under-rated pathogens. Crit Rev Microbiol 33:67–87CrossRefGoogle Scholar
  5. Bharti AR, Nally JE, Ricaldi JN, Matthias MA, Diaz MM, Lovett MA, Levett PN, Gilman RH, Willig MR, Gotuzzo E, Vinetz JM (2003) Leptospirosis: a zoonotic disease of global importance. Lancet Infect Dis 3:757–771CrossRefGoogle Scholar
  6. Blinkova O, Kapoor A, Victoria J, Jones M, Wolfe N, Naeem A, Shaukat S, Sharif S, Alam MM, Angez M, Zaidi S, Delwart EL (2009) Cardioviruses are genetically diverse and cause common enteric infections in South Asian children. J Virol 83:4631–4641CrossRefGoogle Scholar
  7. Blokesch M, Schoolnik GK (2007) Serogroup conversion of Vibrio cholerae in aquatic reservoirs. PLoS Pathog 3:e81. doi: 10.1371/journal.ppat.0030081 CrossRefGoogle Scholar
  8. Bockelmann U, Dorries HH, Ayuso-Gabella MN, Salgot de Marcay M, Tandoi V, Levantesi C, Masciopinto C, Van Houtte E, Szewzyk U, Wintgens T, Grohmann E (2009) Quantitative PCR monitoring of antibiotic resistance genes and bacterial pathogens in three European artificial groundwater recharge systems. Appl Environ Microbiol 75:154–163CrossRefGoogle Scholar
  9. Broza YY, Danin-Poleg Y, Lerner L, Valinsky L, Broza M, Kashi Y (2009) Epidemiologic study of Vibrio vulnificus infections by using variable number tandem repeats. Emerg Infect Dis 15:1282–1285CrossRefGoogle Scholar
  10. California Department of Water Resources (2009) Urban water use efficiency. In: California water plan update 2009. Resource management strategies, vol 2. California Department of Water Resources, Sacramento, p 79 ( Chapter 3)
  11. Campbell-Lendrum D, Woodruff R (2006) Comparative risk assessment of the burden of disease from climate change. Environ Health Perspect 114:1935–1941Google Scholar
  12. CDC (2009a) Multistate outbreaks of Salmonella infections associated with live poultry–United States, 2007. Morb Mortal Wkly Rep 58:25–29Google Scholar
  13. CDC (2009b) Surveillance for foodborne disease outbreaks – United States, 2006. Morb Mortal Wkly Rep 58:609–636Google Scholar
  14. Charron D, Thomas M, Waltner-Toews D, Aramini J, Edge T, Kent R, Maarouf A, Wilson J (2004) Vulnerability of waterborne diseases to climate change in Canada: a review. J Toxicol Environ Health 67:1667–1677CrossRefGoogle Scholar
  15. Checkley W, Epstein LD, Gilman RH, Figueroa D, Cama RI, Patz JA, Black RE (2000) Effect of El Niño and ambient temperature on hospital admissions for diarrhoeal diseases in Peruvian children. Lancet 355:442–450Google Scholar
  16. Chung H, Sobsey MD (1993) Comparative survival of indicator viruses and enteric viruses in seawater and sediments. Water Sci Technol 27:425–428Google Scholar
  17. Colwell RR, Brayton P, Herrington D, Tall B, Huq A, Levine MM (1996) Viable but non culturable Vibrio cholerae 01 revert to a cultivable state in the human intestine. World J Microbiol Biotechnol 12:28–31CrossRefGoogle Scholar
  18. Corvalan C, Hales S, McMichael A (2005) Ecosystems and human well-being: health synthesis: a report of the Millennium Ecosystem Assessment. World Health Organization, GenevaGoogle Scholar
  19. De Toffol S, Laghari AN, Rauch W (2009) Are extreme rainfall intensities more frequent? Analysis of trends in rainfall patterns relevant to urban drainage systems. Water Sci Technol 59:1769–1776CrossRefGoogle Scholar
  20. Dillon P, Pavelic P, Page D, Beringen H, Ward J (2009) Managed aquifer recharge: an introduction. Waterlines report no 13 – February 2009. National Water Commission, Australian Government, CanberraGoogle Scholar
  21. Evison LM (1988) Comparative studies in the survival of indicator organisms and pathogens in fresh and sea water. Water Sci Technol 20:309–315Google Scholar
  22. Falkinham JO III (2009) Surrounded by mycobacteria: nontuberculous mycobacteria in the human environment. J Appl Microbiol 107:356–367CrossRefGoogle Scholar
  23. Faruque SM, Albert MJ, Mekalanos JJ (1998) Epidemiology, genetics, and ecology of toxigenic Vibrio cholerae [Review]. Microbiol Mol Biol Rev 62:1301–1314Google Scholar
  24. Fayer R (2004) Cryptosporidium: a water-borne zoonotic parasite. Vet Parasitol 126:37–56CrossRefGoogle Scholar
  25. Fenollar F, Trape JF, Bassene H, Sokhna C, Raoult D (2009) Tropheryma whipplei in fecal samples from children, Senegal. Emerg Infect Dis 15:922–924CrossRefGoogle Scholar
  26. Gillings M, Boucher Y, Labbate M, Holmes A, Krishnan S, Holley M, Stokes HW (2008) The evolution of class 1 integrons and the rise of antibiotic resistance. J Bacteriol 190:5095–5100CrossRefGoogle Scholar
  27. Gillings MR, Xuejun D, Hardwick SA, Holley MP, Stokes HW (2009) Gene cassettes encoding resistance to quaternary ammonium compounds: a role in the origin of clinical class 1 integrons? ISME J 3:209–215CrossRefGoogle Scholar
  28. Gantzer C, Dubois E, Crance JM, Billaudel S, Kopecka H, Schwartzbrod L, Pommepuy M, Le Guyader F (1998) Influence of environmental factors on the survival of enteric viruses in seawater. Oceanol Acta 21(6):983–992 (French)CrossRefGoogle Scholar
  29. Hallegraeff GM (1992) Harmful algal blooms in the Australian region. Mar Pollut Bull 25:5–8CrossRefGoogle Scholar
  30. Hardwick SA, Stokes HW, Findlay S, Taylor M, Gillings MR (2008) Quantification of class 1 integron abundance in natural environments using real-time quantitative PCR. FEMS Microbiol Lett 278:207–212CrossRefGoogle Scholar
  31. Jay MT, Cooley M, Carychao D, Wiscomb GW, Sweitzer RA, Crawford-Miksza L, Farrar JA, Lau DK, O’Connell J, Millington A, Asmundson RV, Atwill ER, Mandrell RE (2007) Escherichia coli O157:H7 in feral swine near spinach fields and cattle, central California coast. Emerg Infect Dis 13:1908–1911CrossRefGoogle Scholar
  32. Kawaguchi K, Matsuo J, Osaki T, Kamiya S, Yamaguchi H (2009) Prevalence of Helicobacter and Acanthamoeba in natural environment. Lett Appl Microbiol 48:465–471CrossRefGoogle Scholar
  33. Keath NA, Brown RR (2009) Extreme events: being prepared for the pitfalls with progressing sustainable urban water management. Water Sci Technol 59:1271–1280CrossRefGoogle Scholar
  34. King CW, Webber ME (2008) The water intensity of the plugged-in automotive economy. Environ Sci Technol 42:4305–4311CrossRefGoogle Scholar
  35. Koelle K, Pascual M, Yunus M (2005) Pathogen adaptation to seasonal forcing and climate change. Proceedings in biological science 272:971–977CrossRefGoogle Scholar
  36. Kozak GK, Boerlin P, Janecko N, Reid-Smith RJ, Jardine C (2009) Antimicrobial resistance in Escherichia coli isolates from swine and wild small mammals in the proximity of swine farms and in natural environments in Ontario, Canada. Appl Environ Microbiol 75:559–566CrossRefGoogle Scholar
  37. Kracman B, Martrin R, Sztajnbok P (2001) The Virginia pipeline: Australia’s largest water recycling project. Water Sci Technol 43(10):35–42Google Scholar
  38. Kváč M, Květoňová D, Sak B, Ditrich O (2009) Cryptosporidium pig genotype II in immunocompetent man. Emerg Infect Dis 15:982–983CrossRefGoogle Scholar
  39. Lathrop S, Edge K, Bareta J (2009) Shiga toxin-producing Escherichia coli, New Mexico, USA, 2004–2007. Emerg Infect Dis 15:1289–1291Google Scholar
  40. Lau HY, Ashbolt NJ (2009) The use of Acanthamoeba as a tool for understanding Legionella pathogenesis: implications for drinking water. J Appl Microbiol 107:368–378CrossRefGoogle Scholar
  41. Lebarbenchon C, Brown SP, Poulin R, Gauthier-Clerc M, Thomas F (2008) Evolution of pathogens in a man-made world. Mol Ecol 17:475–484CrossRefGoogle Scholar
  42. Lightner DV, Redman RM, Poulos BT, Nunan LM, Mari JL, Hasson KW (1997) Risk of spread of penaeid shrimp viruses in the Americas by the international movement of live and frozen shrimp. Rev Sci Tech 16:146–160Google Scholar
  43. Lipp EK, Huq A, Colwell RR (2002) Effects of global climate on infectious disease: the cholera model. Clin Microbiol Rev 15:757–770CrossRefGoogle Scholar
  44. Lipp EK, Rodrigues-Palacios C, Rose JB (2001) Occurrence and distribution of the human pathogen Vibrio vulnificus in a subtropical Gulf of Mexico estuary. Hydrobiologiea 460:165–173CrossRefGoogle Scholar
  45. Mattison K, Shukla A, Cook A, Pollari F, Friendship R, Kelton D, Bidawid S, Farber JM (2007) Human Noroviruses in swine and cattle. Emerg Infect Dis 13:1184–1188CrossRefGoogle Scholar
  46. McCarthy SA, Khambaty FM (1994) International dissemination of epidemic Vibrio cholerae by cargo ship ballast and other nonpotable waters. Appl Environ Microbiol 60:2597–2601Google Scholar
  47. McMichael A, Campbell-Lendrum DH, Kovats RS, Edwards S, Wilkinson P, Wilson T et al (2004) Climate change. In: Ezzati M, Lopez A, Rodgers A, Murray C (eds) Comparative quantification of health risks: global and regional burden of disease due to selected major risk factors. World Health Organization, Geneva, pp 1543–1649Google Scholar
  48. McNeill AR (ed) (1985) Microbiological water quality criteria: a review for Australia. Australian water resource council technical report no 85. Australian Government Publishing Service, Canberra, 561 pagesGoogle Scholar
  49. Millennium Assessment Board (2005) Living beyond our means: natural assets and human well-being, Millennium Ecosystem Assessment.
  50. Moulin-Schouleur M, Reperant M, Laurent S, Bree A, Mignon-Grasteau S, Germon P, Rasschaert D, Schouler C (2007) Extraintestinal pathogenic Escherichia coli strains of avian and human origin: link between phylogenetic relationships and common virulence patterns. J Clin Microbiol 45:3366–3376CrossRefGoogle Scholar
  51. Myers ML, Panicker G, Bej AK (2003) PCR detection of a newly emerged pandemic Vibrio parahaemolyticus O3:K6 pathogen in pure cultures and seeded waters from the Gulf of Mexico. Appl Environ Microbiol 69:2194–2200CrossRefGoogle Scholar
  52. Nancarrow BE, Leviston Z, Po M, Porter NB, Tucker DI (2008) What drives communities’ decisions and behaviours in the reuse of wastewater. Water Sci Technol 57:485–491CrossRefGoogle Scholar
  53. Niemi G, Wardrop D, Brooks R, Anderson S, Brady V, Paerl H, Rakocinski C, Brouwer M, Levinson B, McDonald M (2004) Rationale for a new generation of indicators for coastal waters. Environ Health Perspect 112:979–986CrossRefGoogle Scholar
  54. Niklasson B, Hörnfeldt B, Lundman B (1998) Could myocarditis, insulin-dependent diabetes mellitus and Guillain-Barré‚ syndrome be caused by one or more infectious agents carried by rodents? Emerg Infect Dis 4:187–193CrossRefGoogle Scholar
  55. Okum DA (2002) Water reuse introduces the need to integrate both water supply and wastewater management at local and regulatory levels. Water Sci Technol 46(6–7):273–280Google Scholar
  56. Oron G, Armon R, Mandelbaum R, Manor Y, Campos C, Gillerman L, Salgot M, Gerba C, Klein I, Enriquez C (2001) Secondary wastewater disposal for crop irrigation with minimal risks. Water Sci Technol 43(10):139–146Google Scholar
  57. Prüss-Üstün A, Bos R, Gore F, Bartram J (2008) Safer water, better health. World Health Organization, GenevaGoogle Scholar
  58. Rapoport E, Shimshony A (1997) Health hazards to the small ruminant population of the Middle East posed by the trade of sheep and goat meat. Rev Sci Tech 16:57–64Google Scholar
  59. Rasko DA, et al. (2008) The pangenome structure of Escherichia coli: comparative genomic analysis of E. coli commensal and pathogenic isolates. J Bacteriol 190:6881–6893Google Scholar
  60. Rathjen D, Cullen P, Ashbolt N, Cunliffe D, Langford J, Listowski A, McKay J, Priestley T, Radcliffe J (2003) Recycling water for our cities. Report to Prime Minister’s Science, Engineering and Innovation Council (PMSEIC), 28th November 2003. Federal Government of Australia, CanberraGoogle Scholar
  61. Richardson HY, Nichols G, Lane C, Lake IR, Hunter PR (2009) Microbiological surveillance of private water supplies in England – the impact of environmental and climatefactors on water quality. Water Res 43:2159–2168CrossRefGoogle Scholar
  62. Robertson LJ (2009) Giardia and Cryptosporidium infections in sheep and goats: a review of the potential for transmission to humans via environmental contamination. Epidemiol Infect 137:913–921CrossRefGoogle Scholar
  63. Rosario K, Nilsson C, Lim YW, Ruan Y, Breitbart M (2009) Metagenomic analysis of viruses in reclaimed water. Environ Microbiol. doi: 10.1111/j.1462-2920.2009.01964.x Google Scholar
  64. Rose JB, Epstein PR, Lipp EK, Sherman BH, Bernard SM, Patz JA (2001) Climate variability and change in the United States: potential impacts on water- and foodborne diseases caused by microbiologic agents. Environ Health Perspect 109:211–221CrossRefGoogle Scholar
  65. Rutjes SA, Lodder WJ, Lodder-Verschoor F, van den Berg HH, Vennema H, Duizer E, Koopmans M, de Roda Husman AM (2009) Sources of hepatitis E virus genotype 3 in The Netherlands. Emerg Infect Dis 15:381–387CrossRefGoogle Scholar
  66. Schijven JF, de Roda Husman AM (2005) Effect of climate changes on waterborne disease in The Netherlands. Water Sci Technol 51:79–87Google Scholar
  67. Schwab KJ, Neill FH, Estes MK, Metcalf TG, Atmar RL (1998) Distribution of Norwalk virus within shellfish following bioaccumulation and subsequent depuration by detection using RT-PCR. J Food Prot 61:1674–1680Google Scholar
  68. Singh RB, Hales S, de Wet N, Raj R, Hearnden M, Weinstein P (2001) The influence of climate variation and change on diarrheal disease in the Pacific Islands. Environ Health Perspect 109:155–159CrossRefGoogle Scholar
  69. Tang YZ, Dobbs FC (2007) Green autofluorescence in dinoflagellates, diatoms, and other microalgae and its implications for vital staining and morphological studies. Appl Environ Microbiol 73:2306–2313CrossRefGoogle Scholar
  70. Thomas V, Loret JF, Jousset M, Greub G (2008) Biodiversity of amoebae and amoebae-resisting bacteria in a drinking water treatment plant. Environ Microbiol 10:2728–2745CrossRefGoogle Scholar
  71. Toomey N, Monaghan A, Fanning S, Bolton D (2009) Transfer of antibiotic resistance marker genes between lactic acid bacteria in model rumen and plant environments. Appl Environ Microbiol 75:3146–3152CrossRefGoogle Scholar
  72. Victoria JG, Kapoor A, Li L, Blinkova O, Slikas B, Wang C, Naeem A, Zaidi S, Delwart E (2009) Metagenomic analyses of viruses in stool samples from children with acute flaccid paralysis. J Virol 83:4642–4651CrossRefGoogle Scholar
  73. WHO (2003) Emerging issues in water and infectious disease. World Health Organization, GenevaGoogle Scholar
  74. WSAA (2008) WSAA report card 2007/2008. Performance of the Australian urban water industry and projections for the future. Water Services Association of Australia Ltd, MelbourneGoogle Scholar
  75. Yang YJ, Goodrich JA (2009) Timing and prediction of climate change and hydrological impacts: periodicity in natural variations. Environ Geol 57:1065–1078Google Scholar
  76. Zahid MS, Udden SM, Faruque AS, Calderwood SB, Mekalanos JJ, Faruque SM (2008) Effect of phage on the infectivity of Vibrio cholerae and emergence of genetic variants. Infect Immun 76:5266–5273CrossRefGoogle Scholar
  77. Zell R, Krumbholz A, Wutzler P (2008) Impact of global warming on viral diseases: what is the evidence? Curr Opin Biotechnol 19:652–660CrossRefGoogle Scholar

Copyright information

© Springer 2010

Authors and Affiliations

  1. 1.National Exposure Research LaboratoryU.S. Environmental Protection AgencyCincinnatiUSA

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