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________________________________________ Global Climate Change and Mosquito-Borne Diseases _____________________________________________________________ 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 – – – – – – – – 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