Environment, Change and Disease: Vectorborne Zoonoses in the Americas

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Environment, Change and Disease Vector-borne
Zoonoses in the Americas

• 10th Annual New and Re-Emerging Infectious
  Disease Conference
• April 13, UIUC

Uriel Kitron University of Illinois Urbana-Champai
gn, IL, USA
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Some anthropogenic changes

• Urbanization demographics, migration,
  biodiversity
• Agricultural development crops, water
  management, migration
• Forestation Both deforestation and
  reforestation
• Global warming, other climate changes

Rate of Change is on the increase
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Monocultures

• Easy spread of pathogens
• Loss of reservoir hosts
• Species dilution (good or bad?)
• Antibiotic resistance

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Green areas in cities

• Urban lungs
• Reduction of Urban heat island effect.
• Wildlife dispersal routes, refuges
• Conservation vs. public health

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Invasion of pathogens, vectors and hosts

• Where from and Where to?
• When and How?
• Role of Anthropogenic effects
• Did (will) they become established? (Is
  transmission taking place)?

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Synathropic species(vectors and reservoir hosts
that made it)
White-tailed deer Odocoileus virginianus

• Mosquitoes Cx. pipiens - WNV
  Ae aegypti - dengue
• Sandflies leishmaniasis
• Deer Ticks and Lyme disease
• Rats Plague, Typhus

Sandfly (phlebotomus)
Culex pipiens
Aedes aegypti
Ratus ratus
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Zoonotic Vector-borne diseases (VBZD)
transmission system
Humans (domestic
animals)
What makes a good vector or a good reservoir?
Vector
Pathogen
Reservoir Host(wildlife)
Environment
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Two examples Vector borne zoonoses

• West Nile virus in Chicago - introduction,
  establishment and distribution in an urban
  area
• Chagas disease vector distribution,
  habitat modification and role of various
  zoonotic hosts

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Prerequisites for an active zoonotic VBD focus

• Vector survival
• Presence of reservoir hosts
• Pathogen transmission
• Opportunities for human/animal exposure

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4. West Nile virus Eco-epidemiology of disease
emergence in urban areas

• Develop a spatial model and risk maps based
  on
• demographic and environmental risk factors for
  WNV and SLE in birds, mosquitoes and humans
• reservoir capacity and differential effects of
  WNV on various bird species
• anthropogenic features of the urban environment
  that support Culex mosquito production,
  mosquito-bird transmission and virus
  amplification.
• Dynamics of viral transmission over space and
  time using molecular evolutionary and
  phylogeographic techniques

funded by NSF/NIH Ecology of Infectious Disease
Program
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Research Team

• Co-Investigators
• University of Illinois
• Jeff Brawn
• Tony Goldberg
• Marilyn Ruiz
• Uriel Kitron
• Michigan State University
• Edward Walker

• Collaborators
• Audubon Chicago Region
• Karen Glennemeier
• Judy Pollack
• Illinois Department of Public Health
• Constance Austin
• Linn Haramis
• Illinois State Water Survey
• Kenneth Kunkel

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West Nile Virus in Illinois

• WNV appeared in NYC during 1999 (arrived from the
  old world)
• 2001 - 123 positive bird specimens, 0 human cases
• 2002 - 884 human cases, 66 deaths, more than any
  other state that year
  (U.S. - 4,156/284)
• Over 680 cases occurred in Chicago and
  surroundings
• 2003 - 54 human cases, 1 death (U.S 9,862/264)
• 2004 - 60 human cases, 4 deaths (U.S.
  2,539/100)
• 2005 - 252 human cases, 12 deaths (U.S.
  3000/119)
• 2006 (10/26) 205 human cases, 9 deaths (U.S.
  3660/112)

2002
2003
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2002
Outbreak years were hot and dry
2005
2006
2004
2003
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Chicago
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Smoothed Map of Disease Cases summarized by
1196 1.8 km hexagons
Local Spatial Autocorrelation of Cases - LISA
statistic (Anselin)
Range 0-15 cases/cell
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WNV Human Cases with Housing Density
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• Human cases tend to be outside of the more
  densely populated urban core.
• 3 areas with most cases (circled on map)
• in the south, near Oak Lawn
• 2) in north, around Skokie
• 3) southwest of Skokie

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2
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Vegetation
PhysiographicRegion
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Dominant patterns in the Chicago urban landscape

• Each different colored area represents a place
  with a common set of factors related to housing,
  vegetation, socio-economics, and land use

Ruiz et al, Int'l J Health Geog 2005
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Urban Type 5, dominated by 40s and 50s housing.
Mostly white, moderate vegetation and moderate
population density. 435 cases (64) were in this
group, 2.27 cases per 10,000 people
(RRgt3.5). (All other types lt0.65
cases per 10,000)
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In hot dry years standing water with organic
matter provide habitat for Culex mosquito larvae
Area characterized by many undocumented storm
drains
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In 2005 we initiated an extensive field study of
WNV - birds, mosquitoes, virus, weather and
environment
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Site 3 Oak Lawn North
Green site Saint Casimirs Cemetery
Residential site
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Avian Host Community

• Bird Surveys
• Line transect bird surveys during May and June
• Bird Mist-netting
• 6-8 nets/morning from sunrise to noon during May
  to October
• Seropositivity of Captured Birds
• ELISA
• Virus Detection in Captured Birds - RT-PCR

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Seropositivity () of positive bird
species,southwest Chicago metropolitian area,
May-Oct, 2005
Overall Prevalence 19.9 (n 1062)
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Vector Community

• Adult Mosquito Trapping - MIR
• Light trap, gravid trap, aspirator
• Quantification of Mosquito Productivity
• Catch basins, containers
• Index of Culex Density
• Ovitraps
• Mosquito Bloodmeal Analysis

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Sharp rise in MIR, coincides with appearance of
fledging birds
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Host selectivity by vectors of West Nile virus
tying together the bird and mosquito data
Identifying the origin of the bloodmeal in
mosquitoes
In order to - Implicate vectors for
virus transmission - Identify host
feeding preferences - Identify bridge vectors

• Pi fraction of total bloodmeals from host i
  (density of species
  i/total avian density)

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Culex spp. feeding preferences

• Pi fraction of total bloodmeals from host i
  (density of species
  i/total avian density)

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Feeding preferences and vector/reservoir role in
transmission

• Culex spp. mosquitoes feed on American Robins
  opportunistically while selecting for Blue Jays
  and avoiding House Sparrows
• Robins are likely key reservoir hosts, while the
  more common sparrows much less so
• WNV detection from Culex pipiens containing
  American Robin and Human bloodmeals provides
  direct evidence of their role in transmission and
  as a bridge vector

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Molecular Epidemiology of WNV

• 1. Genetic diversity and evolution of WNV
  in Illinois, and how that compares to patterns
  across the USA. Virology 360 143-149 ,2007.
  Samples Bird and small mammals submitted to the
  Illinois Diagnostic Labs, 2002-2005
• 2. Genetic diversity, evolution, and
  spatial structure of WNV in our study area in
  Chicago. In preparation. Samples Positive
  mosquito pools and bird sera from our study in
  Chicago

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What we did

• PCR to amplify the ENV gene
• 1,575 bases, about 10 of the viral genome
• Sequencing of ENV directly from PCR products
• Population genetic analyses to quantify viral
  diversity and its apportionment
• Phylogenetic analyses to look at the rate and
  pattern of evolution of the virus

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What we found (in a nutshell)

• WNV in Illinois is genetically representative of
  WNV throughout the USA
• WNV in the USA is diversifying
• WNV in the USA is evolving at a steady rate,
  comparable to other arboviruses
• But, most of the evolution is via NEUTRAL
  mutations no evidence for positive selection.
• But, WNV-2 (our strain) has replaced NY99
• There is little geographic substructure to WNV in
  the USA
• Its pretty much a big, panmictic population, and
  you cant see evidence of any population genetic
  subdivisions corresponding to region or avian
  flyway.

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Ultimately, our goal is to be able to explain and
predict
2005 outbreak
Mosquito pool WNV test results
Human WNV cases, 10/3/2005 185/197 in greater
Chicago
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Weekly 2005 mosquito infection rate by watershed
and cases of human illness in Cook and DuPage
County, Illinois. Human illness cases are
preliminary data and should not be considered
authoritative.
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Weekly 2005 mosquito infection rate by watershed
and cases of human illness in Cook and DuPage
County, Illinois. Human illness cases are
preliminary data and should not be considered
authoritative.
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Trying to understand processes and
interactionsbehind the clustering patterns

• Ecological
• Weather, landscape, housing, and catch basins
• Mosquito and bird habitat suitability
• Mosquito/bird/virus interactions
• Socioeconomic
• Lifestyle
• Race, income, access to health care
• Mosquito Abatement Districts
• Control methods
• Personal protection

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5. Eco-Epidemiology of Chagas Disease in
northwest Argentina

• Ricardo Gurtler, Carla Cecere, Univ. of Buenos
  Aires, Argentina
• Joel Cohen, Rockefeller University, NY
• Cinthia Spillman National Vector Control
  Program, Argentina
• Ellen Dotson, CDC, Atlanta
• Pierre Dujardin, CNRS-IRD, France
• Marta Lauricella, Instituto Fatala Chabén,
  Argentina
• Uriel Kitron, Univ. of Illinois

Supported by NIH/NSF Ecology of Infectious
Disease Program
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Chagas Disease(American trypanosomiasis)

• Zoonosis caused by protozoan trypanosoma cruzi.
• Only in the Americas.
• Only infects mammals.
• 10-18 million people infected,
• 30 affected by heart disease.
• Most infections initially asymptomatic, progress
  to chronic.
• Main routes of infection
• Vector-borne triatomine bugs
• Congenital
• Blood transfusion (concern in US)
• NO VACCINE.
• No effective drugs for chronics.
• Control through insecticide spraying
• and screening of blood donnors.

T. Cruzi in blood
Swollen Eye, 5 of cases
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Chagas disease

• In terms of public health and economic
  impact, American trypanosomiasis (Chagas'
  disease) is the most important parasitic
  infection in Latin America"

Geographic distribution determined by presence
of efficient vectors
Life cycle of Trypanosoma cruzi
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Complexity of transmission cycles of T. cruzi
Zeledón R. CIBA Foundation Symposium, 1974.
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Study area in Northern Argentina, part of the
Gran Chaco of Argentina, Bolivia, Paraguay and
Brazil

Departamento Moreno
Santiago del Estero Province
Amama
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Semi-arid area Mean annual temp. of 22º C
Dry Chaco
Thorn forest of Quebracho and Algarrobo
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The rural landscape of forest and savannah is
undergoing rapid change - Cattle and Soybean
introduction.
Soy boom in South America may be bust for
environment, Miami Herald  - Dec 24, 2004
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Cattle operation and soybean cultivation by
large landowners result in
further deforestation, fencing of large areas,
Labor migration and displacement of livestock
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STUDY AREA, 2002
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Typical Compound with home and multiple
peridomestic structures
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Peridomestic Structures refuge for bugs
Pig corral
Storeroom
Goat corral
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Insecticide spraying is the main control strategy

Big problem - reinfestation of houses by
triatomine bugs from peridomestic and sylvatic
sources
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Control is hard, time consuming, has to be
repeated and is based on ongoing surveillance
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Mapping and geostatistical tools
Sketch maps made in the field during 1993-2002
Ikonos Satellite imagery (1-4m2)
Digital map for each village
Joining of attribute data to a GIS file
Clusters of high infestation and potential
sources of community reinfestation
SPATIAL STATISTICS
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Chagas disease study

• Vector studies - Reinfestation by triatomine bugs
• Reservoir studies infection and infectiousness
  of domestic animals
• Sylvatic studies of wildlife and bugs
• Scale of study and heterogeneity

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Reinfestation by T. infestans (5 years
post-spraying)
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Gi(d) local spatial statistic

• Gi(d) ?j Wij(d) xj
• ?j xj
• Wij(d) is a spatial weights matrix with
• values of one for all links within
• distance d of a given I
• Concern about multiple comparisons
• (need to adjust significant z value)

We used Gi(d) to detect local and focal
clustering of infestations (number of bugs per
structure)
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FOCAL ANALYSIS OF REINFESTATION IN AMAMÁ
Primary source of T. infestans 1993
Subsequent infestations were clustered around an
initial focus at a distance of 450 mts.
Potential secondary sources fell within the
range of the clustering around the primary
source.
Cecere et al. 2005. Am. J. Trop. Med. Hyg.,
71(6) 803810.
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Moving upscale - Including other
villages. Internal and external sources of
reinfestation.
Trinidad
Mercedes
External sources Villages not sprayed and
located within 1,500 m of the treated villages.
Cecere et al. EID, 2006
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RECOMENDATION
An effective control program on the community
level would entail residual spraying with
insecticides of the colonized site and all sites
within a radius of 450 m, and all communities
within 1,500 m of the target community in order
to prevent the subsequent propagation of T.
infestans
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Chagas disease study

• Vector studies - Reinfestation by triatomine bugs
• Reservoir studies infection and infectiousness
  of domestic animals,
• Sylvatic studies of wildlife and bugs
• Scale of study and heterogeneity

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Relative contribution to transmission ofdogs
cats humans14 5 1
3.5 yrs mean life expectancy

• Index based on multiplying
• Host-specific blood meal indices
• Host prevalence of infectiousness
• Host infectiousness to bugs

Gurtler et al, Parasitology, 2006
Also, chickens, goats, opossums, skunks
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Abundance and spatial distribution of T.
guasayana were positively associated with the
local density and spatial distribution of goats.
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Chagas disease study

• Vector studies - Reinfestation by triatomine bugs
• Reservoir studies infection and infectiousness
  of domestic animals
• Sylvatic studies of wildlife and bugs
• Scale of study and heterogeneity

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505 sylvatic mammals trapped between 2002-2004
1 INFECTED SKUNKS (N 92)
8 INFECTED OPOSSUMS (N 42)
All 4 opossum infected by parasite lineage i. The
only skunk infected had parasite lineage iic.
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Decline in age-specific prevalence of t. Cruzi in
opossums didelphis albiventris after 12 years of
surveillance ( ) relative to pre-spraying
prevalence ( )
1988-1991 (Schweigmann et al., 1999)
?8.2/month
2002-2004
?1.2/month
Ceballos et al., Acta Trop.98 286296, 2006.
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• (iii) changes in landscape over two decades since
  1990
• gt Extensive deforestation probably resulted in
• - reduced number of refuges for opossums and
  bugs
• - increased number of predators (foxes) and
  skunks.
• ? refuges ? opossums ? rate of contact
  bugs-opossums ?
• ? ? transmission
• Complex links and interactions between
• sylvatic, peridomestic and domestic bug
  infestation and parasite transmission need to be
  considered.

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Chagas disease study

• Vector studies - Reinfestation by triatomine bugs
• Reservoir studies infection and infectiousness
  of domestic animals
• Sylvatic studies of wildlife and bugs
• Scale of study and heterogeneity

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Heterogeneity at various levels

• Bug abundance at domestic and peri-domestic site,
  community and department levels
• Host infection 'infected households', 'infected
  communities'
• Host infectivity to bugs 'Superspreaders'
• Spatial distribution of infected dogs within and
  among villages gt 'Hotspots of transmission'.
• Complex sylvatic/peridomestic/domestic
  interactions of host, vectors, parasites and the
  environment
• gt VERY FOCAL TRANSMISSION function of
  epidemiological, entomological, parasitological,
  demographic, socio-economic and environmental
  factors

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Project is a true Interdisciplinary collaboration
between UBA, UIUC, CDC, Rockefeller and Natl
Vector Control Programme and includes a strong
training component
Cardinal MV, Levin M, Grijalva E, Kitron U,
Dieter R, Cortinas R, Ceballos LA, Gürtler RE,
Petrocco F, Gurevitz JM, Vazquez-Prokopec GM.
Amamá, July 2003
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b. Some general points re environment and disease

• Movement of people/animals to zoonotic disease
  areas and movement of pathogens to susceptible
  human/animal populations.
• Deforestation (reforestation), agricultural
  practices and urbanization (landscape/land use).
• Risk and protection associated with large
  monocultures and loss of biodiversity (cash
  crops, intensive animal production,
  megalopolises)

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b. Some general points (cont'd)

• What is the role of green areas in urban
  settings?
• Issues of conservation vs. public health
• Haves and Have nots (South vs. North,
  Developed vs. Under-developed, Low vs. High
  socioeconomic status)

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And let us not forget communication and the media
Africa Africa's Blight is in the Environment
http//allafrica.com/stories/200704021765.html En
vironmental factors alone account for 25 to 45
percent of bad health in the world but it is
becoming progressively clear that the environment
is a health factor.