Environmental Factors and Zoonotic Pathogen Ecology in Urban Exploiter Species

Abstract

Knowledge of pathogen ecology, including the impacts of environmental factors on pathogen and host dynamics, is essential for determining the risk that zoonotic pathogens pose to people. This review synthesizes the scientific literature on environmental factors that influence the ecology and epidemiology of zoonotic microparasites (bacteria, viruses and protozoa) in globally invasive urban exploiter wildlife species (i.e., rock doves [Columba livia domestica], European starlings [Sturnus vulgaris], house sparrows [Passer domesticus], Norway rats [Rattus norvegicus], black rats [R. rattus] and house mice [Mus musculus]). Pathogen ecology, including prevalence and pathogen characteristics, is influenced by geographical location, habitat, season and weather. The prevalence of zoonotic pathogens in mice and rats varies markedly over short geographical distances, but tends to be highest in ports, disadvantaged (e.g., low income) and residential areas. Future research should use epidemiological approaches, including random sampling and robust statistical analyses, to evaluate a range of biotic and abiotic environmental factors at spatial scales suitable for host home range sizes. Moving beyond descriptive studies to uncover the causal factors contributing to uneven pathogen distribution among wildlife hosts in urban environments may lead to targeted surveillance and intervention strategies. Application of this knowledge to urban maintenance and planning may reduce the potential impacts of urban wildlife-associated zoonotic diseases on people.

This is a preview of subscription content, log in to check access.

Figure 1

References

  1. Allen SE, Boerlin P, Janecko N, Lumsden JS, Barker IK, Pearl DL, Reid-Smith RJ, Jardine C (2011) Antimicrobial resistance in generic Escherichia coli isolates from wild small mammals living in swine farm, residential, landfill, and natural environments in southern Ontario, Canada. Applied and Environmental Microbiology 77:882–888; doi: 10.1128/AEM.01111-10

    CAS  Article  PubMed  Google Scholar 

  2. Anholt H, Himsworth C, Rothenburger JL, Proctor H, Patrick DM (2014) Ear mange mites (Notoedres muris) in black and Norway rats (Rattus rattus and Rattus norvegicus) from inner-city Vancouver, Canada. Journal of Wildlife Diseases 50:104–108; doi: 10.7589/2013-02-046

    Article  PubMed  Google Scholar 

  3. Ayral F, Artois J, Zilber AL, Widén F, Pounder KC, Aubert D, Bicout DJ, Artois M (2015) The relationship between socioeconomic indices and potentially zoonotic pathogens carried by wild Norway rats: a survey in Rhône, France (2010-2012). Epidemiology and Infection 143:586-599; doi: 10.1017/S0950268814001137

    CAS  Article  PubMed  Google Scholar 

  4. Barrett MA, Bouley TA (2015) Need for enhanced environmental representation in the implementation of One Health. EcoHealth 12:212–219; doi: 10.1007/s10393-014-0964-5

    Article  PubMed  Google Scholar 

  5. Benacer D, Thong KL, Min NC, Verasahib KB, Galloway RL, Hartskeerl RA, Souris M, Zain SNM (2016) Epidemiology of human leptospirosis in Malaysia, 2004-2012. Acta Tropica 157:162–168; doi: 10.1016/j.actatropica.2016.01.031

    Article  PubMed  Google Scholar 

  6. Beninde J, Veith M, Hochkirch A (2015) Biodiversity in cities needs space: a meta-analysis of factors determining intra-urban biodiversity variation. Ecology Letters 18:581–592; doi: 10.1111/ele.12427

    Article  PubMed  Google Scholar 

  7. Bertolotti L, Kitron UD, Walker ED, Ruiz MO, Brawn JD (2008) Fine-scale genetic variation and evolution of West Nile virus in a transmission ‘hot spot’ in suburban Chicago, USA. Virology 374:381-389; doi: 10.1016/j.virol.2007.12.040

    CAS  Article  PubMed  Google Scholar 

  8. Bradley CA, Altizer S (2007) Urbanization and the ecology of wildlife diseases. Trends in Ecology and Evolution 22:95–102; doi: 10.1016/j.tree.2006.11.001

    Article  PubMed  Google Scholar 

  9. Brearley G, Rhodes J, Bradley A, Baxter G, Seabrook L, Lunney D, Liu Y, McAlpine C (2013) Wildlife disease prevalence in human-modified landscapes. Biological Reviews 88:427–442; doi: 10.1111/brv.12009

    Article  PubMed  Google Scholar 

  10. Brooks JE, Naing UH, Walton DW, Myint DS, Tun UM, Thaung U, Kyi DO (1977) Plague in small mammals and humans in Rangoon, Burma. The Southeast Asian Journal of Tropical Medicine and Public Health 8(3):335–344

    CAS  PubMed  Google Scholar 

  11. Cavanaugh DC (1971) Specific effect of temperature upon transmission of the plague bacillus by the oriental rat flea, Xenopsylla cheopis. American Journal of Tropical Medicine and Hygiene 20:264–273

    CAS  Article  PubMed  Google Scholar 

  12. Chen HX, Qiu FX, Dong BJ, Ji SZ, Li YT, Wang Y, Wang HM, Zuo GF, Tao XX, Gao SY (1986) Epidemiological studies on hemorrhagic fever with renal syndrome in China. Journal of Infectious Diseases 154:394–398; doi: 10.1093/infdis/154.3.394

    CAS  Article  PubMed  Google Scholar 

  13. Childs JE, Glass GE, Korch GW, Ksiazek TG, LeDuc JW (1992) Lymphocytic choriomeningitis virus infection and house mouse (Mus musculus) distribution in urban Baltimore. American Journal of Tropical Medicine and Hygiene 47:27–34

    CAS  Article  PubMed  Google Scholar 

  14. Childs JE, Glass GE, Korch GW, LeDuc JW (1987a) Prospective seroepidemiology of hantaviruses and population dynamics of small mammal communities of Baltimore, Maryland. American Journal of Tropical Medicine and Hygiene 37:648–662

    CAS  Article  PubMed  Google Scholar 

  15. Childs JE, Korch GW, Glass GE, LeDuc JW, Shah KV (1987b) Epizootiology of hantavirus infections in Baltimore: isolation of a virus from Norway rats, and characteristics of infected rat populations. American Journal of Epidemiology 126:55-68

    CAS  Article  PubMed  Google Scholar 

  16. Childs JE, Korch GW, Smith GA, Terry AD, LeDuc JW (1985) Geographical distribution and age related prevalence of antibody to Hantaan-like virus in rat populations of Baltimore, Maryland, USA. American Journal of Tropical Medicine and Hygiene 34:385–387

    CAS  Article  PubMed  Google Scholar 

  17. Costa F, Wunder EA, De Oliveira D, Bisht V, Rodrigues G, Reis MG, Ko AI, Begon M, Childs JE (2015) Patterns in Leptospira shedding in Norway rats (Rattus norvegicus) from Brazilian slum communities at high risk of disease transmission. PLoS Neglected Tropical Diseases 9:e0003819 (doi: 10.1371/journal.pntd.0003819)

  18. Cueto GR, Cavia R, Bellomo C, Padula PJ, Suárez OV (2008) Prevalence of hantavirus infection in wild Rattus norvegicus and R. rattus populations of Buenos Aires City, Argentina. Tropical Medicine and International Health 13:46–51; doi: 10.1111/j.1365-3156.2007.01968.x

    Article  PubMed  Google Scholar 

  19. Daszak P, Cunningham AA, Hyatt AD (2001) Anthropogenic environmental change and the emergence of infectious diseases in wildlife. Acta Tropica 78:103–16; doi: 10.1016/S0001-706X(00)00179-0

    CAS  Article  PubMed  Google Scholar 

  20. Dohoo, IR, Martin SW, Stryhn H (2009) Veterinary Epidemiological Research 2nd Edition, Charlottetown, P.E.I.: VER, Inc.

    Google Scholar 

  21. Engering A, Hogerwerf L, Slingenbergh J (2013) Pathogen-host-environment interplay and disease emergence. Emerging Microbes and Infections 2:e5 (doi: 10.1038/emi.2013.5)

  22. Estrada-Peña A, Ostfeld RS, Peterson AT, Poulin R, la Fuente J de (2014) Effects of environmental change on zoonotic disease risk: an ecological primer. Trends in Parasitology 30:205–214; doi: 10.1016/j.pt.2014.02.003

    Article  PubMed  Google Scholar 

  23. Feng AYT, Himsworth CG (2014) The secret life of the city rat: a review of the ecology of urban Norway and black rats (Rattus norvegicus and Rattus rattus). Urban Ecosystems 17:149–162; doi: 10.1007/s11252-013-0305-4

    Article  Google Scholar 

  24. Gargiulo A, Russo TP, Schettini R, Mallardo K, Calabria M, Menna LF, Paia P, Pagnini U, Caputo V, Fioretti A, Dipineto L (2014) Occurrence of enteropathogenic bacteria in urban pigeons (Columba livia) in Italy. Vector Borne and Zoonotic Diseases 14:251–255; doi: 10.1089/vbz.2011.0943

    Article  PubMed  Google Scholar 

  25. Garrard J (2014) Health Sciences Literature Review Made Easy: The Matrix Method 4th Edition, Burlington: Jones and Bartlett Learning

    Google Scholar 

  26. Gasparini J, Erin N, Bertin C, Jacquin L, Vorimore F, Frantz A, Lenouvel P, Laroucau K (2011) Impact of urban environment and host phenotype on the epidemiology of Chlamydiaceae in feral pigeons (Columba livia). Environmental Microbiology 13:3186–3193; doi: 10.1111/j.1462-2920.2011.02575.x

    CAS  Article  PubMed  Google Scholar 

  27. Gasparini J, Jacquin L, Laroucau K, Vorimore F, Aubry E, Castrec-Rouëlle M, Frantz A (2014) Relationships between metals exposure and epidemiological parameters of two pathogens in urban pigeons. Bulletin of Environmental Contamination and Toxicology 92:208–212; doi: 10.1007/s00128-013-1172-7

    CAS  Article  PubMed  Google Scholar 

  28. Geigenfeind I, Vanrompay D, Haag-Wackernagel D (2012) Prevalence of Chlamydia psittaci in the feral pigeon population of Basel, Switzerland. Journal of Medical Microbiology 61:261–265; doi: 10.1099/jmm.0.034025-0

    Article  PubMed  Google Scholar 

  29. Gortazar C, Reperant LA, Kuiken T, la Fuente J de, Boadella M, Martínez-Lopez B, Ruiz-Fons F, Estrada-Peña A, Drosten C, Medley G, Ostfeld R, Peterson T, VerCauteren KC, Menge C, Artois M, Schultsz C, Delahay R, Serra-Cobo J, Roulin R, Keck F, Aguirre AA, Henttonen H, Dobson AP, Kutz S, Lubroth J, Mysterud A (2014) Crossing the interspecies barrier: opening the door to zoonotic pathogens. PLoS pathogens 10:e1004129 (doi: 10.1371/journal.ppat.1004129)

  30. Grimm NB, Faeth SH, Golubiewski NE, Redman CL, Wu J, Bai X, Briggs JM (2008) Global change and the ecology of cities. Science 319:756–760; doi: 10.1126/science.1150195

    CAS  Article  PubMed  Google Scholar 

  31. Guan P, Huang D, He M, Shen T, Guo J, Zhou B (2009) Investigating the effects of climatic variables and reservoir on the incidence of hemorrhagic fever with renal syndrome in Huludao City, China: a 17-year data analysis based on structure equation model. BMC Infectious Diseases 9:109 (doi: 10.1186/1471-2334-9-109)

  32. Halliday JEB, Knobel DL, Agwanda B, Bai Y, Breiman RF, Cleaveland S, Njenga MK, Kosoy M (2015) Prevalence and diversity of small mammal-associated Bartonella species in rural and urban Kenya. PLoS Neglected Tropical 9:e0003608 (doi: 10.1371/journal.pntd.0003608)

  33. Hathaway SC, Blackmore DK (1981) Ecological aspects of the epidemiology of infection with leptospires of the Ballum serogroup in the black rat (Rattus rattus) and the brown rat (Rattus norvegicus) in New Zealand. The Journal of Hygiene 87(3):427–436

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  34. Haydon DT, Cleaveland S, Taylor LH, Laurenson MK (2002) Identifying reservoirs of infection: a conceptual and practical challenge. Emerging Infectious Diseases 8:1468–1473; doi: 10.3201/eid0812.010317

    Article  PubMed  Google Scholar 

  35. Heddema ER, Sluis S Ter, Buys JA, Vandenbroucke-Grauls CMJE, van Wijnen JH, Visser CE (2006) Prevalence of Chlamydophila psittaci in fecal droppings from feral pigeons in Amsterdam, The Netherlands. Applied and Environmental Microbiology 72:4423–4425; doi: 10.1128/AEM.02662-05

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  36. Himsworth CG, Bai Y, Kosoy MY, Wood H, DiBernardo A, Lindsay R, Bidulka J, Tang P, Jardine C, Patrick D (2015a) An Investigation of Bartonella spp., Rickettsia typhi, and Seoul Hantavirus in Rats (Rattus spp.) from an inner-city neighborhood of Vancouver, Canada: is pathogen presence a reflection of global and local rat population structure? Vector Borne and Zoonotic Diseases 15:21–26; doi: 10.1089/vbz.2014.1657

    Article  PubMed  Google Scholar 

  37. Himsworth CG, Bidulka J, Parsons KL, Feng AYT, Tang P, Jardine CM, Kerr T, Mak S, Robinson J, Patrick DM (2013) Ecology of Leptospira interrogans in Norway Rats (Rattus norvegicus) in an inner-city neighborhood of Vancouver, Canada. PLoS Neglected Tropical Diseases 7:e2270 (doi: 10.1371/journal.pntd.0002270)

  38. Himsworth CG, Miller RR, Montoya V, Hoang L, Romney MG, Al-Rawahi GN, Kerr T, Jardine CM, Patrick DM, Tang P, Weese S (2014a) Carriage of methicillin-resistant Staphylococcus aureus by wild urban Norway rats (Rattus norvegicus). PLoS ONE 9:e87983 (doi: 10.1371/journal.pone.0087983)

  39. Himsworth CG, Patrick DM, Mak S, Jardine CM, Tang P, Weese JS (2014b) Carriage of Clostridium difficile by wild urban Norway rats (Rattus norvegicus) and black rats (Rattus rattus). Applied and Environmental Microbiology 80:1299–1305; doi: 10.1128/AEM.03609-13

    Article  PubMed  PubMed Central  Google Scholar 

  40. Himsworth CG, Zabek E, Desruisseau A, Parmley EJ, Reid-Smith R, Jardine CM, Tang P, Patrick DM (2015b) Prevalence and characteristics of Escherichia coli and Salmonella spp. in the feces of wild urban Norway and black rats (Rattus norvegicus and Rattus rattus) from an inner-city neighborhood of Vancouver, Canada. Journal of Wildlife Diseases 51:589–600; doi: 10.7589/2014-09-242

    CAS  Article  PubMed  Google Scholar 

  41. Hsieh J-W, Tung KC, Chen W-C, Lin J-W, Chien L-J, Hsu Y-M, Wang HC, Chomel BB, Chang CC (2010) Epidemiology of Bartonella infection in rodents and shrews in Taiwan. Zoonoses and Public Health 57:439–446; doi: 10.1111/j.1863-2378.2009.01234.x

    CAS  Article  PubMed  Google Scholar 

  42. Inoue K, Maruyama S, Kabeya H, Yamada N, Ohashi N, Sato Y, Yukawa M, Masuzawa T, Kawamori F, Kadosaka T, Takada N, Fujita H, Kawabata H (2008) Prevalence and genetic diversity of Bartonella species isolated from wild rodents in Japan. Applied and Environmental Microbiology 74:5086–5092; doi: 10.1128/AEM.00071-08

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  43. Jiang J-F, Zuo S-Q, Zhang W-Y, Wu X-M, Tang F, De Vlas SJ, Zhao WJ, Zhang PH, Dun Z, Wang RM, Cao WC (2008) Prevalence and genetic diversities of hantaviruses in rodents in Beijing, China. American Journal of Tropical Medicine and Hygiene 78:98–105

    CAS  PubMed  Google Scholar 

  44. Johne R, Dremsek P, Kindler E, Schielke A, Plenge-Bönig A, Gregersen H, Wessels U, Schmidt K, Rietschel W, Groschup MH, Guenther S, Heckel G, Ulrich RG (2012) Rat hepatitis E virus: geographical clustering within Germany and serological detection in wild Norway rats (Rattus norvegicus). Infection, Genetics and Evolution 12:947–956; doi: 10.1016/j.meegid.2012.02.021

    Article  PubMed  Google Scholar 

  45. Johnson S, Bragdon C, Olson C, Merlino M, Bonaparte S (2016) Characteristics of the built environment and the presence of the Norway rat in New York City: results from a neighborhood rat surveillance program, 2008-2010. Journal of Environmental Health 78:22–29

    PubMed  Google Scholar 

  46. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P (2008) Global trends in emerging infectious diseases. Nature 451:990–993; doi: 10.1038/nature06536

    CAS  Article  PubMed  Google Scholar 

  47. Klein SL, Bird BH, Nelson RJ, Glass GE (2002) Environmental and physiological factors associated with Seoul virus infection among urban populations of Norway rats. Journal of Mammalogy 83:478-488; doi: 10.1644/1545-1542(2002)083<0478:EAPFAW>2.0.CO;2

    Article  Google Scholar 

  48. Korch GW, Childs JE, Glass GE, Rossi CA, LeDuc JW (1989) Serologic evidence of hantaviral infections within small mammal communities of Baltimore, Maryland: spatial and temporal patterns and host range. The American Journal of Tropical Medicine and Hygiene 41:230-40

    CAS  Article  PubMed  Google Scholar 

  49. Lau CL, Smythe LD, Craig SB, Weinstein P (2010) Climate change, flooding, urbanisation and leptospirosis: fuelling the fire? Transactions of the Royal Society of Tropical Medicine and Hygiene 104:631–638; doi: 10.1016/j.trstmh.2010.07.002

    Article  PubMed  Google Scholar 

  50. LeDuc JW, Smith GA, Pinheiro FP, Vasconcelos PF, Rosa ES, Maiztegui JI (1985) Isolation of a Hantaan-related virus from Brazilian rats and serologic evidence of its widespread distribution in South America. American Journal of Tropical Medicine and Hygiene 34:810–815

    CAS  Article  PubMed  Google Scholar 

  51. Lelu M, Muñoz-Zanzi C, Higgins B, Galloway R (2015) Seroepidemiology of leptospirosis in dogs from rural and slum communities of Los Rios Region, Chile. BMC Veterinary Research 11:31 (doi: 10.1186/s12917-015-0341-9)

  52. Mackenstedt U, Jenkins D, Romig T (2015) The role of wildlife in the transmission of parasitic zoonoses in peri-urban and urban areas. International Journal for Parasitology: Parasites and Wildlife 4:71–79; doi: 10.1016/j.ijppaw.2015.01.006

    PubMed  PubMed Central  Google Scholar 

  53. McFarlane R, Sleigh A, McMichael T (2012) Synanthropy of wild mammals as a determinant of emerging infectious diseases in the Asian-Australasian region. EcoHealth 9:24–35; doi: 10.1007/s10393-012-0763-9

    Article  PubMed  Google Scholar 

  54. McKinney ML (2006) Urbanization as a major cause of biotic homogenization. Biological Conservation 127:247–260; doi: 10.1016/j.biocon.2005.09.005

    Article  Google Scholar 

  55. Mills JN (2006) Biodiversity loss and emerging infectious disease: an example from the rodent-borne hemorrhagic fevers. Biodiversity 7:9–17; doi: 10.1080/14888386.2006.9712789

    Article  Google Scholar 

  56. Mills JN, Childs JE (1998) Ecologic studies of rodent reservoirs: their relevance for human health. Emerging Infectious Diseases 4:529–537; doi: 10.3201/eid0404.980403

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  57. Muñoz-Zanzi C, Mason M, Encina C, Gonzalez M, Berg S (2014) Household characteristics associated with rodent presence and Leptospira infection in rural and urban communities from Southern Chile. The American Journal of Tropical Medicine and Hygiene 90:497–506; doi: 10.4269/ajtmh.13-0334

    Article  PubMed  PubMed Central  Google Scholar 

  58. Murphy RG, Williams RH, Hughes JM, Hide G, Ford NJ, Oldbury DJ (2008) The urban house mouse (Mus domesticus) as a reservoir of infection for the human parasite Toxoplasma gondii: an unrecognised public health issue? International Journal of Environmental Health Research 18:177–185; doi: 10.1080/09603120701540856

    Article  PubMed  Google Scholar 

  59. Oliveira DSC, Guimarães MJB, Portugal JL, Medeiros Z (2013) The socio–demographic, environmental and reservoir factors associated with leptospirosis in an urban area of north–eastern Brazil. Annals of Tropical Medicine and Parasitology 103:149–157; doi: 10.1111/j.1863-2378.2008.01122.x

    Article  Google Scholar 

  60. Pedersen K, Clark L, Andelt WF, Salman MD (2006) Prevalence of shiga toxin-producing Escherichia coli and Salmonella enterica in rock pigeons captured in Fort Collins, Colorado. Journal of Wildlife Diseases 42:46–55; doi: 10.7589/0090-3558-42.1.46

    Article  PubMed  Google Scholar 

  61. Psaroulaki A, Antoniou M, Toumazos P, Mazeris A, Ioannou I, Chochlakis D, Christophi N, Loukaides P, Patsais A, Moschandrea I, Tselentis Y (2010) Rats as indicators of the presence and dispersal of six zoonotic microbial agents in Cyprus, an island ecosystem: a seroepidemiological study. Transactions of the Royal Society of Tropical Medicine and Hygiene 104:733–739; doi: 10.1016/j.trstmh.2010.08.005

    Article  PubMed  Google Scholar 

  62. Reisen WK, Barker CM, Carney R, Lothrop HD, Wheeler SS, Wilson JL, Madon MB, Takahashi R, Carroll B, Garcia S, Fang Y, Shafii M, Kahl N, Ashtari S, Kramer V, Glaser C, Jean C (2006) Role of corvids in epidemiology of West Nile virus in southern California. Journal of Medical Entomology 43:356–367

    Article  PubMed  Google Scholar 

  63. Reisen WK, Lothrop HD, Wheeler SS, Kennsington M, Gutierrez A, Fang Y, Garcia S, Lothrop B (2008) Persistent West Nile virus transmission and the apparent displacement St. Louis encephalitis virus in southeastern California, 2003-2006. Journal of Medical Entomology 45:494–508

    PubMed  PubMed Central  Google Scholar 

  64. Romero-Vivas CME, Cuello-Pérez M, Agudelo-Flórez P, Thiry D, Levett PN, Falconar AKI (2013) Cross-sectional study of Leptospira seroprevalence in humans, rats, mice, and dogs in a main tropical sea-port city. The American Journal of Tropical Medicine and Hygiene 88:178–183; doi: 10.4269/ajtmh.2012.12-0232

    Article  PubMed  PubMed Central  Google Scholar 

  65. Sacristán C, Esperón F, Herrera-León S, Iglesias I, Neves E, Nogal V, Muño MJ, Torre A (2014) Virulence genes, antibiotic resistance and integrons in Escherichia coli strains isolated from synanthropic birds from Spain. Avian Pathology 43:172–175; doi: 10.1080/03079457.2014.897683

    Article  PubMed  Google Scholar 

  66. Sargeant JM, O’Connor AM, Dohoo IR, Erb HN. STROBE-Vet Statement. https://strobevet-statement.org/. Accessed November 9, 2016

  67. Satterthwaite D (2003) The links between poverty and the environment in urban areas of Africa, Asia, and Latin America. Annals of the American Academy of Political and Social Science 590:73–92; doi: 10.1177/0002716203257095

    Article  Google Scholar 

  68. Taylor PJ, Arntzen L, Hayter M, Iles M, Frean J, Belmain S (2008) Understanding and managing sanitary risks due to rodent zoonoses in an African city: beyond the Boston Model. Integrative Zoology 3:38–50; doi: 10.1111/j.1749-4877.2008.00072.x

    Article  PubMed  Google Scholar 

  69. United Nations, Department of Economic and Social Affairs, Population Division (2015) World Urbanization Prospects: The 2014 Revision, New York: United Nations. https://esa.un.org/unpd/wup/. Accessed November 2, 2016

  70. Widén F, Ayral F, Artois M, Olofson AS, Lin J (2014) PCR detection and analyzis of potentially zoonotic Hepatitis E virus in French rats. Virology Journal 11:90 (doi: 10.1186/1743-422X-11-90)

  71. Yokoyama E, Maruyama S, Kabeya H, Hara S, Sata S, Kuroki T, Yamamoto T (2007) Prevalence and genetic properties of Salmonella enterica serovar typhimurium definitive phage type 104 isolated from Rattus norvegicus and Rattus rattus house rats in Yokohama City, Japan. Applied and Environmental Microbiology 73:2624–2630; doi: 10.1128/AEM.02465-06

    CAS  Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

J. Rothenburger’s research is supported by the following: Natural Sciences and Engineering Research Council Alexander Graham Bell Canada Graduate Scholarship-Doctoral, Canadian Federation of University Women Dr. Margaret McWilliams Pre-Doctoral Fellowship, Imperial Order Daughters of the Empire War Memorial Scholarship, Ontario Veterinary College Graduate Student Fellowship and the University of Guelph Dean’s Tri-Council Scholarship. The authors wish to thank the two anonymous reviewers for their insightful comments.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Jamie L. Rothenburger.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 118 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Rothenburger, J.L., Himsworth, C.H., Nemeth, N.M. et al. Environmental Factors and Zoonotic Pathogen Ecology in Urban Exploiter Species. EcoHealth 14, 630–641 (2017). https://doi.org/10.1007/s10393-017-1258-5

Download citation

Keywords

  • Columba livia domestica
  • Disease ecology
  • Mus
  • Passer domesticus
  • Rattus
  • Zoonoses