Transcript Theodore Andreadis, Connecticut Agricultural Experiment Station

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Global Climate Change and Mosquito-Borne
Diseases
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Theodore G. Andreadis
Center for Vector Biology & Zoonotic Diseases
The Connecticut Agricultural Experiment Station
New Haven, CT
Evidence for Global Climate Change
• World climate is in a warming phase that began in the
early decades of 18th century (faster than any period in
last 1000 years) (increase of 1.5oF over past 100 yrs.)
• Sea levels have risen ~ 2-3 mm per year since 1961
• Arctic sea ice has declined by 10% per decade
• Snow cover and glaciers have diminished in both
hemispheres
• Accelerating worldwide hydrological cycle
– Increasing the intensity, frequency, and duration of droughts,
heavy precipitation events and flooding
• Predictions from United Nations Intergovernmental Panel
on Climate Change (IPCC): in next 90 years
– Global temperature will increase between 1.8 oC and 4.0 oC
– Sea levels will rise between 18 and 59 cm (up to 2 ft.)
Observed Changes in North American Extreme Climate Events
• Warmer and fewer cold days and nights
• Hotter and more frequent hot days and nights
• More frequent heat waves and warm spells
• More frequent and intense heavy downpours
and total rainfall in precipitation events
• Increases in area affected by drought
• More intense hurricanes
Why Climate Change and Mosquito-Borne Disease is a Concern
• Mosquitoes, in their role as vectors, are critical components in the
transmission cycle of many disease causing pathogens that affect hundreds of
millions of people world-wide
–
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–
–
–
–
–
–
Malaria
Dengue
Yellow Fever
Japanese Encephalitis
Chikungunya
Rift Valley Fever
Filariasis
West Nile virus
• Mosquitoes and the pathogens they transmit are directly impacted by changes
in weather and climate
– All vector-borne pathogens spend a part of their life cycle in cold-blooded
arthropods and are subject to environmental factors
– Marginal changes in temperature, humidity and rainfall can have
potentially large biological effects on disease transmission
Hypothesis:
Global warming will increase the incidence of mosquitoborne infectious diseases
Rationale:
Most mosquito-borne diseases, including Dengue, Malaria,
and Yellow Fever occur in the tropics, are weather sensitive,
and have distinct seasonal patterns
Therefore:
If warming heats up the globe, then these and other
mosquito-borne diseases will expand into new regions and
become more prevalent in areas where they already occur
However:
Climate change is only one of many factors affecting the
incidence of mosquito-borne diseases
Socioeconomic factors – human activities that impact the
local ecology are equally important and may have an equal
or greater impact
Drivers for Changes in the Status of Mosquito-Borne Diseases
Industrial &
agricultural
chemical pollution
Trade & human
movement
Invasive
mosquitoes &
pathogens
Land use, water
storage, and
irrigation
Mosquito-Borne
Diseases
Atmospheric
composition
Climate change
Weather
Urbanization
with poverty
Adapted from Sutherst , Clin. Microbiol. Rev. 2004
Increased Temperature Effects on Mosquitoes
• Can extend season when mosquitoes are
active and transfer infectious agents for
longer period of time
• Increase overwintering survival
• Shorten larval development time
• Increase adult feeding - females digest
blood more quickly and feed more frequently
• Increase adult survival at higher latitudes
• Can extend distribution range of more
tropical vector species
– Aedes aegypti
– Aedes albopictus
• Decrease survival of some species
− Increase capacity to
produce more offspring
− Increase frequency of
contact with humans or
other hosts
Bring mosquito vectors and
associated pathogens into
contact with naive human
populations that have no
immunity
Increased Temperature Effects on Mosquitoes
• Extrinsic incubation period of
pathogen is decreased in vector
at higher temperatures
Eclipse
phase
Replication
phase
– The period of time from when a
mosquito takes an infectious
bloodmeal until it transmits the
pathogen
– Pathogens inside the mosquito
develop faster in heat, increasing
transmission efficiency and the
likelihood of the disease being
spread
Transmission
Extrinsic incubation period
Infection of mosquito feeding on a viremic animal
Virus particles in blood
Digestion of blood
Spread of virus within midgut
Peritrophic Membrane
Semipermeable, non-cellular
matrix composed of chitin
and protein
Dissemination from the midgut into the hemocoel
Fat body
Salivary glands
Nervous system
Hemocoel
Virus replication in secondary tissues in body
Transmission of virus from mosquito to new host
Salivary glands
Impact of Temperature on Pathogen Development in the Mosquito Vector
Disease
Pathogen
Vector
Low Temp
High Temp
Dengue
Dengue virus
Aedes aegypti
12 days at 30 oC
7 days at 32-35 oC
Malaria
Plasmodium vivax
Anopheles gambiae
18 days at 20 oC
7 days at 30 oC
Malaria
Plasmodium falciparum
Anopheles gambiae
23 days at 20 oC
9 days at 30 oC
West Nile virus
West Nile virus
Culex pipiens
15 days at 20 oC
5 days at 30 oC
West Nile virus
West Nile virus
Culex tarsalis
20 days at 20 oC
6 days at 30 oC
Temperature Effects on Pathogens
• Changes in the distribution and length of the transmission season
– Sustained outbreaks of Malaria only occur where temperatures routinely
exceed 14-15 oC (60 oF)
– Yellow fever and Dengue fever only occur where temperatures rarely fall
below 10 oC (50 oF)
– Outbreaks of West Nile and St. Louis encephalitis viruses are associated with
above average summer temperatures
• Decreased viral replication at high temperatures
Disease
Pathogen
Vector
Min Temp
Max Temp
Malaria
P. falciparum
Anopheles
16-19 oC
33-39 oC
Malaria
P. vivax
Anopheles
14-15 oC
33-39 oC
Dengue
Dengue virus
Aedes
12 oC
Not known
Adult Survival Probability
Adult Biting Frequency
Extrinsic Incubation Period
1
50
0.3
30
20
0.8
per day
per day
Days
40
0.2
0.1
0
15
20
25
Temp
30
35
40
0
10
oC
15
20
25
Temp
30
35
40
oC
TRANSMISSION POTENTIAL
1
0.8
0.6
0.4
Plasmodium vivax
0.4
0.2
10
0
0.6
0.2
0
14 17 20 23 26 29 32 35 38 41
Temp oC
10 15
20
25
Temp
oC
30
35
40
Precipitation Effects on Mosquitoes
Increased Precipitation
Negative Impacts
• Will increase the number and
quality of larval breeding sites
• Epic rainfall events can
synchronize mosquito host
seeking and pathogen
transmission
• Associated increase in humidity
will increase mosquito survival
Positive Impact
• Excess rainfall or snow pack can
eliminate larval habitat by
flooding thus decreasing the
mosquito population
Precipitation Effects on Mosquitoes
Decreased Precipitation
Negative Impacts
• Low rainfall can create larval
habitat by causing rivers to dry
into “pools” that serve as
production sites (dry season
malaria)
• Decreased rain can increase
container-breeding mosquitoes
by forcing increased water
storage
Positive Impact
• Will generally decrease
number and quality of larval
breeding sites
Precipitation Effects on Pathogens
• Few direct effects but some data indicate that humidity affects malarial
parasite development in Anopheles mosquitoes
Relationship Between Climate Change and Mosquito-Borne
Disease: Review
Climate change may affect the incidence of mosquito-borne
diseases through its effect on four principal characteristics of
vector mosquito populations that relate to pathogen transmission1
• Geographic and Temporal Distribution: Range shifts in vector distribution that
bring mosquito vectors and disease-causing pathogens into contact with
naïve human populations
• Population Density: Changes in the population density of the mosquito vector
that result in increased frequency of contact with humans
• Prevalence of Infection by Zoonotic Pathogens: Changes in the prevalence of
pathogen infection in the reservoir host or mosquito vector population that
increase the frequency of human contact with infected mosquito vectors
• Pathogen Load: Changes in pathogen load brought about by changes in the
rates of pathogen reproduction, replication, or development in the vector
mosquito
1Adapted
from Mills et al. Environ Health Perspectives 118 (2010)
Malaria
• Africa: Increases in the incidence of malaria are strongly
associated with higher temperatures and rainfall.
• South America: Strong association between El Nino and incidence of outbreaks.
• Climate modeling shows that global warming will likely enlarge the potential range
of Anopheles vectors and thus can expect increased expansion of disease
Dengue
• Africa: Increase in incidence associated with increased humidity
• Asia: Many countries experienced high activity associated with
1998 El Nino
• Climate warming may increase area of land suitable Aedes aegypti
and slight increase in temperature could result in epidemics
• Epidemics in the
America's have
been linked to the
reestablishment
of Ae. aegypti
• Key West, FL –
outbreak in 2009
• 22 locally
acquired cases in
Florida in 2013
Dengue
Aedes aegypti
Chikungunya Virus
• Previously confined to central Africa but
during the last century has expanded into
more temperate regions
• Africa: 2004 epidemic in Kenya associated
with unseasonably dry conditions and
inadequate socioeconomic conditions
– Unsafe domestic water storage
– Shortened extrinsic incubation period in
Aedes aegypti
• A single mutation in viral genome facilitated
adaptation to Aedes albopictus played a
major role in expansion from Africa in 2005
• Expansion into northern Italy associated
with unusually warm dry summer in 2007
• With expansion of Ae. albopictus and Ae.
aegypti could expect more epidemics
Chikungunya Virus
• Emerging mosquito-borne alpha virus
• Principal vectors: Aedes aegypti and Aedes
albopictus
• Characterized by acute fever and severe joint
pain
• Name derives from a Makonde word meaning
“that which bends up” – refers to contorted
posture associated with severe joint pain
• First identified in Tanzania in 1952
• Caused small sporadic outbreaks in Africa
and Asia through the 1960’s and 1970’s
• Since 2004 has expanded its geographic
range causing unprecedented epidemics in
Africa, Asia, Europe and the Caribbean
Transmission Cycles
Sylvatic Enzootic Cycle
Ae. taylori
Ae. furcifer
Ae. africanus
Ae. luteocephalus
Urban Epidemic Cycle
Ae. aegypti
Ae. albopictus
Aedes aegypti
• Most important vector in urban areas
• Develop moderate virus titers 104 pfu
• Adult females prefer to feed on
humans – aggressive day biter
• Often take several partial blood meals
during a single gonotrophic cycle
• Oviposit in artificial containers as
preferred larval sites
• Rest inside houses with ready access
to human hosts
• Distribution limited to tropical and
subtropical climates
Aedes albopictus
• Active in urban, suburban and rural
environments
• Competent vectors that develop
moderate virus titers 104 pfu
• Aggressive human day biter but also
feeds on other animals
• Oviposit in artificial containers as
preferred larval sites
• Long-lived (4-8 weeks)
• Produce drought and cold resistant
eggs
• More temperate distribution than Ae.
aegypti
Recent Reemergence of Chikungunya Virus
• Epidemic began in Kenya in 2004
and spread into islands in the
Indian Ocean causing ~ 500,000
cases (2005-2006)
• Spread to India via infected air
travelers causing an epidemic
(2006-2009) with >1.5 million cases
• Introduced into northern Italy in
2007 by an infected traveler from
India causing > 200 cases
• Subsequently spread through
southeast Asia and islands in the
Pacific Ocean (2007-2008), > 5
million people sickened
• 2010 introduced into southeastern
France by an infected traveler from
India (2 local cases)
2007
2010
2008
2005
2007
2008
2004
2005 - 2006
• A single mutation in viral genome (amino acid in E2
protein) facilitated adaptation to Aedes albopictus
(increased infectivity) played a major role in
expansion from Africa
Introduction of Chikungunya Virus into the Caribbean
• The first locally acquired human cases
in the Americas occurred in October
2013 on the island of Saint Martin and
were reported by the Pan American
Health Organization in December 2013
Introduction of Chikungunya Virus into the Caribbean
• The first locally acquired human cases
in the Americas occurred in October
2013 on the island of Saint Martin and
were reported by the Pan American
Health Organization in December 2013
• During the next 6 months > 400,000
confirmed and probable cases were
reported throughout other Caribbean
Islands (17 countries or territories)
Introduction of Chikungunya Virus into the Caribbean
• The first locally acquired human cases
in the Americas occurred in October
2013 on the island of Saint Martin and
were reported by the Pan American
Health Organization in December 2013
• During the next 6 months > 400,000
confirmed and probable cases were
reported throughout other Caribbean
Islands (17 countries or territories)
• Infected travelers originating from the
island countries carried the virus around
the region leading to local transmission
in Central, South and North America
Chikungunya in the Americas
800
37 countries
747,721 reported cases
35
700
30
600
25
500
20
400
15
300
10
200
5
100
0
0
Dec
Jan
Feb
Mar
Apr
May
Month
Jun
Jul
Aug
Sep
Cases, Suspected and Confirmed (thousands)
Countries and Territories with Local Transmission
40
Introduction of Chikungunya Virus into the Caribbean
• The first locally acquired human cases
in the America’s occurred in October
2013 on the island of Saint Martin and
were reported by the Pan American
Health Organization in December 2013
• During the next 6 months > 100,000
confirmed and probable cases were
reported throughout other Caribbean
Islands (17 countries or territories)
• Infected travelers originating from the
island countries carried the virus around
the region leading to local transmission
in Central, South and North America
• To date > 1.2 million suspected or
confirmed locally acquired cases have
been reported in 43 countries (150
deaths) with imported cases throughout
the Americas
Florida
11
Caribbean
Islands
203,556
Puerto Rico
20,073
Dominican
Republic
499,000
Guatemala
473
El Salvador
123,229
Haiti
64,709
Nicaragua
542
Costa Rica
1
Panama
32
Venezuela
7,400
Guyana
76
Suriname
1,210 French Guiana
7,870
Columbia
22,372
Brazil
173
Chikungunya Virus in the United States
• CDC data show that from 2006 –
2013 an average of 28 cases/year
(range 5 - 65) of Chikungunya virus
disease were identified in travelers
visiting or traveling to the US from
affected areas, mostly Asia
• As of February 10, 2015, a total of
2,481 laboratory confirmed cases
have been reported in the US (98%
in travelers from the Caribbean)
• Florida: 11 locally acquired cases
Number Cases
Connecticut
31
Maine
6
Massachusetts
158
Broward - 1
New Hampshire
22
Miami-Dade - 2
New Jersey
171
Palm Beach - 4
New York
740
St Lucie - 4
Pennsylvania
96
Rhode Island
49
Vermont
3
Origin of Chikungunya Virus in the Caribbean
• The CHICK virus strain circulating
in the Americas belongs to the
Asian genotype and is most
closely related to strains isolated
from Indonesia, Thailand and the
Philippines
• Supports the idea that a single
strain was introduced from Asia
• Ae. aegypti and Ae. albopictus
are competent vectors of the
Asian strain
East, Central, South Africa
• Asian strain infects Ae. aegypti
more efficiently
• No evidence supporting a
substantive role of Ae. albopictus
in epidemic transmission of the
Asian strain
Leparc-Goffart et al. 2014 Lancet 383:514
Lanciotti & Valadere 2014 EID 20:1400
• The current epidemic in the Americas is being
driven by Ae. aegypti and not Ae. albopictus
Chikungunya Virus: Assessing the Threat in the Americas
• The virus is spreading uncontrolled in the
Caribbean
DENGUE
• Will likely spread throughout Latin America
and portions of South America wherever
Ae. aegypti occurs similar to Dengue
• Most of the population is naïve, setting the
stage for major epidemics: hundreds of
millions of people at risk
• There could be potential for the virus to
establish an enzootic monkey – human
cycle as occurred with Yellow Fever
• No vaccine is currently available
• Prospects for control in Latin and South
America are not good!
2013
2.4 million cases
773 in US (49 locally acquired)
Areas with recent Dengue transmission
Areas infested with Aedes aegypti
Chikungunya Virus: Assessing the Threat in the US
• The virus strain is the old Asian lineage that
does not infect Ae. albopictus as efficiently
• Most transmission in the Americas will occur
via Ae. aegypti which should limit geographic
spread, particularly to temperate climates
where this mosquito does not normally occur
• The capacity for Ae. albopictus to transmit the
Asian strain provides potential for local
transmission in the continental US where Ae.
albopictus is common
• Don’t know what role Ae. albopictus will play in
spreading the virus in more temperate regions
• If a mutation occurs in the currently circulating
strain, the US will be at greater risk
• “It would be a game changer!”
Rift Valley Fever
• Africa: Activity follows periods of heavy rain which coincide with
sea surface temperature anomalies in equatorial Pacific and Indian Oceans
• East Africa: Outbreaks are associated with exceptionally high rainfall amounts
that flood grassland depressions “dambos” and support Aedes and Culex
mosquitoes. Terminate with end of rainy season
Indian
Ocean
Regions reporting
large outbreaks
Regions at risk
Relationship Between Climate Variation and Mosquito-Borne Disease: Current
Observations and Future Expectations
ROSS RIVER VIRUS
• Australia: Epidemics occur after unusually heavy rain and flooding.
• Climatological models show that a rise in sea level with greater
rainfall and flooding could significantly increase virus activity.
RRV infections 2006-07
West Nile Virus
• United States
• The weather in New York during the spring
and summer of 1999, when the virus was
presumably introduced, was particularly
warm and humid, creating conditions that
favored intensive mosquito breeding and
efficient virus transmission
West Nile Virus
• United States
• Since 1999 the largest outbreaks of human
disease have been associated with warm
wet winters and springs followed by hot dry
summers which resemble some general
circulation model projections for climate
change over much of the US
• Currently experiencing earlier reemergence
in spring and more rapid amplification in the
summer that may be associated with early
“heat waves”
2012
United States
Northeast
Total Cases
Fatalities
5,387
243 (4.5%)
259
17 (6.5%)
EEE Activity - Northeastern US
• Unprecedented northward
expansion into new regions where
the virus had been historically rare
or previously unknown
EEE Human cases
1965-2001
2003-2014
ME
VT
NH
NY
• Experiencing a sustained
resurgence of activity within longstanding foci
(51 cases, 20 fatalities)
MA
CT
RI
NJ
EEE Human cases
1965-2001
2003-2014
Armstrong & Andreadis NEJM 2013
1.5 / yr
4.5 / yr
Resurgence
Mosquito Species Range Expansions?
New State Records since 2005
Increased abundance
and distribution
Predicted Aedes albopictus range
expansion in the northeastern US
under two climate change
scenarios
Moderate increase in CO2
High increase in CO2
Expansion and abundance
associated with higher winter
temperatures and precipitation
(snowfall)
Rochlin I, Ninivaggi DV, Hutchinson ML, Farajollahi A (2013) Climate change and range expansion of the Asian Tiger Mosquito (Aedes albopictus) in
northeastern USA: implications for public health practitioners. PLoS ONE 8(4): e60874. doi:10.1371/journal.pone.0060874
Distribution of Aedes albopictus in Connecticut
2006
2010
2011
2012
Distribution of Anopheles crucians in Connecticut
2000-03
2004-07
2008-11
2012
Summary
• The greatest effects of climate change on transmission of
vector-borne diseases are likely to be observed at the
temperature extremes of the range of temperatures at
which transmission occurs
– Increased pathogen transmission efficiency
– Increased vector-host contact
– Shortened extrinsic incubation period
• The effects are likely to be expressed in many ways
– Short-term epidemics
– Long-term gradual changes in disease trends
Concluding Thoughts
• “The natural history of mosquito-borne diseases are
complex and the interplay of climate, ecology and
vector biology defies simplistic analysis” (Reiter, Environ Health Per 2001)
• The recent resurgence of many of these diseases is a major cause for concern,
but climate variability is only one factor
• Other principal determinants include local politics, economics and human activities
– Demographic changes (population growth, migration, urbanization)
– Societal changes (inadequate housing, water deterioration, migration)
– Changes in public health policy (decreased resources for surveillance, prevention and
vector control)
– Insecticide and drug resistance
– Deforestation
– Irrigation systems and dams
Concluding Thoughts
• Adaptations to climate change and variability will largely depend on the level
of health infrastructure in the affected regions
• We really don’t know how projected climate change will affect the complex
ecosystems required to maintain these mosquito-borne diseases
• More research is needed to better understand the influence of weather and
climate on these pathogens in their natural transmission cycles
• Assessments that integrate global climate scenario-based analyses with local
demographic and environmental factors will be needed to guide
comprehensive, long-term preventive health measures