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.

Seasonal temperature in Chicago

Distribution

of human

WNV cases

in the

greater

Chicago

area, 2002

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.

Inside the “hot spot”

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”

“Natural” site

“Residential” site

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

Spatial variation in mosquito infection rates within the

“hot spot” area, 2005-2008

1 km

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

Catch basins

Catch basins: a key factor?

“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