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Urban landscapes and the transmission
of West Nile virus in Chicago, USA
Tony Goldberg1, Uriel Kitron2, Marilyn Ruiz3, Ned Walker4, Jeff Brawn3,
Gabe Hamer1,4, Tavis Anderson1, Francesco Cerutti5, Scott Loss3, Luigi
Bertolotti5, and Giuseppina Amore5,6
1 University of Wisconsin-Madison, USA
2 Emory University, USA
3 University of Illinois, USA
4 Michigan State University, USA
5 University of Torino, Italy
6 European Food Safety Authority, Parma, Italy
• Viral family: Flaviviridae
– “Japanese encephalitis antigenic complex”
– RNA genome (only ~15 kb)
• Vector-borne
– Transmitted between birds and mosquitoes
• Primarily Culex pipiens mosquitoes in the Northeast and Midwest
• Zoonotic
– Causes encephalitis in people, horses & other mammals
• Introduced into the Northeast USA in 1999 from Israel
– Spread rapidly throughout North America
West Nile virus
WNV in Chicago
• In 2002, Illinois led the
United States in numbers of
human West Nile cases.
• Chicago and surrounding
suburbs were “hot spots” of
infection.
• The Chicago area has
remained a focus of WNV
infection in humans and
birds, with infection rates
peaking in August and
September.
Smoothed Maps of Disease Cases(cases summarized by 1196 1.8 km hexagons)
WNV 2002 N=649Range 0-15 cases/cell
SLE 1975 N=231Range 0 – 7 cases/cell
A historical perspective…
• 1901: New York Times [referring to
Chicago’s 19th ward]: “dirty streets, filthy
alleys, impure water cause[d an] epidemic
of typhoid fever and malaria.”
• 1975: Outbreak of human
St. Louis encephalitis, a
virus related to WNV
• 2002: Outbreak of WNV
in humans
Seasonal “amplification” of WNV
in the Upper Midwest
Early season(mid-May to end of July)
Later season(Aug to mid-Oct)
Mosquito infection by week, Cook and
DuPaige Counties, Illinois, 2004-2008
Ruiz et al., Parasites and Vectors, in press.
Statistical associations : 2002-2006
Variable
Standardized
discriminant
function
coefficient
Means
No Cases Case(s)
Race (% White) 0.62*** 45.8% 68.3%
% Housing built 1950-59 0.44*** 15.8% 21.9%
Housing Density -0.35*** 2.41 units/km2 1.33 units/km2
Median Age 0.19*** 32.4 yrs 35.9 yrs
% Vegetated 0.13*** 17.2% 28.4%
Biodiversity index 0.09*** 0.96 1.04
In Chicago Lake Plain 0.04*** 0.82 0.64
Income -0.04*** $43,771 $55,483
Elevation range (m) -0.02*** 7.48 m 11.81 m
North Shore MAD 0.31*** 0.01 0.11
Chicago MAD -0.30*** 0.67 0.35
South Cook MAD 0.17*** 0.12 0.24
Northwest MAD -0.05*** 0.06 0.12
***Significant at 0.001 (using Wilks’ Lambda) Ruiz et al., Parasites and Vectors, in press.
Field Sites:
1 mile
1. Palos Hills - North
2. Palos Hills - South
3. Oak Lawn - Central
4. Oak Lawn - North
5. Chicago - Mt. Greenwood
6. Evergreen Park - West
7. Evergreen Park - North
8. Blue Island
9. Chicago - Ashburn East
10. Alsip
11. Burbank
12. Evergreen Cemetery
13. Wolf Wildlife Area
14. Holy Sepulchre Cemetery
15. Saint Casmir Cemetery
11 “residential”
4 “natural”
Methods: 2005-2009
transmission seasons
• Mosquito trapping
– Light traps, gravid traps, aspirators
• Bird trapping
– Mist nets
• Testing of mosquito pools and bird sera for WNV
RNA using molecular laboratory methods
• Sequencing of a portion of the WNV genome (ENV
gene) in positive samples
WNV infection in mosquitoes, 2005-2007
n ~ 60,000 mosquitoesHamer et al, 2008. VBZD 8:57-67
2005
2006
2007
Blood meal analysis
• 1,483 bloodfed mosquitoes
captured from 2005 - 2007
• 57% Culex pipiens, 19% C. restuans, 14% Aedes
vexans
• Blood meal sources identified in 1,043 (70%)
mosquitoes using Cyt B sequencing
– Failure to ID blood meals reflected advanced stage
of digestion
• For C. pipiens, 80% blood meals were avian, 16%
mammalian, 4% other (e.g. amphibian).
Hamer et al., 2009. Am J Trop Med Hyg 60:268-278.
Amplification fraction (Fi): the
fraction of West Nile virus
infectious mosquitoes resulting
from feeding on a particular
avian host.
0 10 20 30 40
Killdeer
Song Sparrow
Eastern Bluebird
House Wren
Brown Thrasher
Common Yellowthroat
Willow Flycatcher
Mourning Dove
Eastern Towhee
Swainson's Thrush
Cooper's Hawk
Swamp Sparrow
House Sparrow
Common Canary
Scarlet Tanager
Northern Cardinal
American Kestrel
House Finch
Blue Jay
American Robin
Hamer et al., 2009. Am J Trop
Med Hyg 60:268-278.
Robins!
• Robins in suburban Chicago:– Abundant
• Second only to house sparrows
– Preferred by Culex pipiens• House sparrows are avoided
• Kilpatrick et al., 2006 (Proc Roy Soc Lond B, 273:2327-33).– Washington DC and Maryland (5 urban sites in 2004)
– Robins preferred, house sparrows avoided
– Describe robins as a WNV “super spreader”
Week
Birds in mist nets
Avian seroprevalence
Avian viremia
Culex IR
Human cases
Role of Hatch-Year Birds
Hamer et al. (2008), VBDZ 8:57-67
“Smoking gun” mosquito
Date Species Bloodmeal ID
7/20/05 Cx. pipiens House sparrow
8/19/05 Cx. pipiens American Robin
8/20/05 Cx. pipiens American Robin
9/7/05 Cx. pipiens Human
Blood meal analysis on individual Culex pipiens that were
also positive for WNV by PCR
Hamer et al., 2008 Journal of Medical Entomology, 45: 125-128.
* Note: 84% of mammalian blood meals were human!
Culex pipiens
• “Northern house mosquito”
• Distribution: urban temperate zones worldwide
• Feeding habits: mostly birds, sometimes
mammals
• Breeding habitats: small pools of stagnant water
with organic material
“Coincidence model” of WNV amplification in Chicago
Urban civil engineering
Robin population dynamics
Summer weather patterns
WNV meningitis/encephalitis human cases
Viral evolution
• Sequencing WNV ENV gene in
positive samples
– 1,575 bases, most variable in WNV genome
• ~500 WNV ENV sequences to
date
– 3% birds, 97% mosquitoes
– 68% from residential sites, 32% from
natural sites
WNV nucleotide diversity in Culex mosquitoes by site
type, 2005-2007
Amore et al., Proc Roy Soc Lond Ser B, in press.
Year Site type N π (%) SE (%) Difference*
2005 Residential 76 0.37 0.022
p < 0.001 Natural 52 0.26 0.050
All 128 0.33 0.016
2006 Residential 59 0.45 0.023
p = 0.003 Natural 21 0.42 0.037
All 80 0.44 0.019
2007 Residential 38 0.50 0.039
p = 0.107 Natural 8 0.46 0.063
All 46 0.50 0.035
* Difference between residential and natural sites within the same year
WNV evolutionary rate
• Rate for WNV in Illinois,
2002-2005:
– 0.85 X (± 0.02) 10-3
substitutions per site per year
• Rate for WNV in Chicago
area, 7/21/05 - 10/4/05:
– 8.2 (± 2.8) X 10-3
substitutions per site per year
Bertolotti et al., Virology 360:143-149 and 374:381-389
A possible
explanation for:
• Higher viral genetic
diversity in mosquitoes
from residential sites
than from natural sites
• Spatial heterogeneity in
mosquito infection rates
• Higher evolutionary
rates within
transmission seasons
than between seasons
Conclusions
• Key hosts (robins) and vectors (C. pipiens) interact
with climate and the urban built environment (catch
basins) to spur local transmission and amplification
of WNV.
– “Hot spots within hot spots”
• Possible role of urban microclimate
– Higher viral diversity in residential than in “natural” areas
– Higher evolutionary rates in the summer than across years
– First documented example of a link between urbanization
and viral evolution.
– Implications for climate change?
Co - PIs
University of Illinois
Jeff Brawn
Marilyn Ruiz
Michigan State University
Ned Walker
Gabe Hamer
Emory University
Uriel Kitron
Collaborators, students, post-docs
Students and Post-Docs
Gabe Hamer, Luigi Bertolotti, Giusi Amore, John
Andrews, Scott Loss, Anna Schothoeffer, Jane
Messina, Laura Tomassone, Laura Hickman, Tavis
Anderson, Luis Chavez, Robert Smith, Christina
Newman, Bethany Krebs
Collaborators
Mike Ward, Steve Bolin, Bryan Epperson, Kirk
Klassing, Chris Small
Audubon Chicago Region
Karen Glennemeier
Judy Pollack
Illinois Department of Public Health
Constance Austin, Linn Haramis
Illinois State Water Survey
Kenneth Kunkel
Chicago Department of Public Health
South Cook County Mosquito Abatement District
Municipalities
Oak Lawn, Palos Hills, Burbank, Evergreen Park,
Alsip, Cities of Blue Island and Chicago
Acknowledgments
Funding through NSF/NIH EID
Program; Award No. EF-0429124
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