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Mosquito-borne Zoonotic Diseases CMED/EPI 526 Spring Quarter 2009 Anthony A Marfin, MD, MPH, MA State Epidemiologist Washington Department of Health April 15, 2009 University of Washington School of Public Health Overview Zoonotic diseases Definitions for vector-borne disease Role of dipterans in vector-borne diseases Japanese encephalitis serocomplex West Nile virus in North America ArboNET surveillance Mosquito-borne viruses in the blood supply Disease control Zoonoses refer to diseases & infections naturally transmitted between vertebrate animals & man with or without an arthropod intermediate (WHO, 1956) Why worry about vector-borne zoonoses? Negative impact on commerce, travel, & economies (e.g., Rift Valley fever, yellow fever) Explosive debilitating outbreaks (e.g., yellow fever) Developing nations, diseases of major public health significance (e.g., yellow fever, leishmaniasis) Preventable cause of human illness & death Human impact on environment can ↑ incidence (e.g., Japanese encephalitis) Mosquito-borne diseases that are NOT zoonotic Human is only vertebrate host Question if there is a “sylvatic” reservoir (e.g., nonhuman primate species) Examples include: • Malaria (protozoa) – Anopheles spp. • Dengue (flavivirus) – Aedes aegypti, Ae. albopictus • Filiriasis (nematode) – Aedes aegypti • Chikungunya (alphavirus) – Aedes spp. Vector-Borne Infectious Diseases Are More Complex Multiple interconnected & complex cycles Pathogens adapted to vertebrate & invertebrate species Vector interacts with host & agent Environment affects vector abundance & ability to transmit infection Multiple “host” species Commonalities of Mosquito-Borne Zoonoses Humans rarely develop high titer of pathogens in blood, CSF, or tissue (i.e., do not amplify*). Large outbreaks rare but can be explosive Clinical cases usually severe High mortality Finding source of infection (“reservoir”) important for disease control (source reduction, depopulation) * Excluding yellow fever virus Big Concepts & Definitions Unique to Vector-Borne Diseases Vector – Does not itself cause disease. Instead, vectors transmit infection by moving pathogen from one host to another. Infection generally lasts vector’s life & can kill vector. Bridging vector – Mosquito feeds on amplifying hosts & other species causing infections in other hosts. “Bridge” between one cycle & another. “Bridging” mosquito species in yellow fever “Bridging” Different Types of Hosts Amplifying host – Host (usually vertebrate) in which pathogens replicate to high levels (“titer”) leading to infection of more vectors. Reservoir hosts – Host that allows persistence of pathogen in nature when active transmission is not occurring. “Dead-end” hosts – Host that does not develop high titer of pathogens. Consequently, will not infect vectors. AKA “incidental hosts.” Definitive host – Host in which pathogen reaches “maturity” (generally applies to protozoal & nematodal infections, not viral & bacterial infections) “Advanced knowledge” of mosquito-borne zoonotic diseases Extrinsic incubation period – Time interval between infection of vector & first transmission of pathogen by vector. Transovarial transmission – Infection of eggs in ovaries of an infected female vector leading to new vector infection (“vertical transmission”) Mosquito Infection Rate (MIR) – Minimum estimate of number of infected mosquitoes. Usually expressed “per 1,000 mosquitoes.” “Over-wintering” mechanisms: Viral persistence strategies Allow re-emergence of pathogen in next year despite unfavorable environmental conditions: • Reintroduction by migratory birds • Alternate arthropod vectors • Long-term survival of infected, dormant females • Continued feeding & transmission yeararound • Chronic infection of vertebrate hosts • Transovarial transmission Factors that strongly affect pathogen transmission by mosquitoes Vector competence (ability to get infected & transmit) Extrinsic incubation period (influenced by temperature) Vector contact with critical host Population indices of vector & hosts Diurnal feeding habits of vector Pathogen replication in host (intrinsic incubation period) Host feeding preferences Vector longevity Precipitation – flooding & drought Temperature Proximity of vectors/reservoirs to human populations Dipteran Vectors of Human Disease Insects “True flies” (di + ptera = “two wings”) ~240K spp of mosquitoes, sandflies, & black flies Major insect orders for human health & economies Example: mosquitoes are primary vectors for malaria, dengue, West Nile virus, yellow fever, & multiple viruses causing encephalitis Mosquitoes, Sandflies, & Black flies (Order Diptera, Suborder Nematocera) “Primitive flies” Not common house fly Aquatic larval forms (important for control) Vectors other than mosquitoes in suborder disease: • Black flies - Onchocerca volvulus, nematode causing “river blindness” • Deer flies - Francisella tularensis (tularemia, “rabbit fever”) • Phlebotamine sandflies – Toscana, SFF Sicily, & SFF Naples viruses (Phlebovirus, Bunyaviridae) • Biting midges – Blue tongue virus (Orbivirus, Reoviridae) & other diseases of livestock Infectious Disease Transmission: The “Epi-Triangle” Agent “Vectors” Viruses Bacteria Protozoans Nematodes Mosquitoes Sand fly Hosts Vertebrates – Humans, horses, rodents, birds, & reptiles Environment Temperature, humidity, rainfall Mosquitoes, Sandflies & Human Disease Infectious Disease Agents Vector genera Virus Bacterial Protozoal Anopheles Onyong-n’yong (Alphavirus) ?? Plasmodium (Malaria) Aedes / Ochlerotatus (Stegomyia) Yellow fever & Dengue (Flavivirus) Chikungunya virus (Alphavirus) Francisella tularensis* ?? Culex West Nile virus Japanese encephalitis virus St. Louis encephalitis virus Francisella tularensis* ?? Phelbotomus & Lutzomyia Sandfly Fever (Phlebovirus) Bartonella (Oroya Fever) Leishmania (Kala Azar) * Mechanical transfer of bacteria Today’s Discussion Infectious Disease Agents Vector genera Virus Anopheles Aedes/Ochlerotatus (Stegomyia) Culex Phelbotomus Japanese encephalitis serocomplex (Flaviviruses) Bacterial Protozoal Japanese encephalitis serocomplex (14 viruses) Viruses that cause human encephalitis • Japanese encephalitis virus • West Nile virus (Variant: Kunjin) • St. Louis encephalitis virus • Murray Valley encephalitis virus (Variant: Alfuy) • Rocio virus • Ilheus virus • Bussuquara virus (?) Viruses that do not cause human encephalitis but may cause animal infections/illnesses • Usutu (?), Cacipacore, Koutango, Yaounde, & Stratford viruses Commonality of Viruses in JE Serocomplex Human infections: • Most asymptomatic • Small number of rash-fever or febrile illness cases • < 1% associated with central nervous system illness • Very low virus titer in human serum & CSF: No human-mosquito-human transmission No human-to-human transmission Surface Envelope protein similar across complex Culex mosquitoes are vectors Amplifying hosts: Birds • JE & MVE – Ardeid birds In JE, pigs also serve as amplifying hosts • WNV & SLE – Passerine birds “…West Nile virus was first isolated in 1937 from the blood of a febrile woman in the West Nile province of Uganda…” West Nile Virus Epidemics Endemic transmission with periodic epidemics First recorded epidemic: Israel, 1951-1954 & 1957 France – 1962 South Africa – 1974 • Massive (~75K), 1 case of encephalitis reported Romania – 1996 Italy – 1998 Russia – 1999 • ↑ rate of WNND, ↑ case fatality rate West Nile Virus Approximate Geographic Range in 1998 1999: 1st WNV outbreak in North America New York City, June – October 1999 Initially, two separate investigations • Epizootic beginning June 1999 • Epidemic beginning August 1999 Begins with the “astute clinician…” • Veterinary & medical clinicians • Tracey McNamara, Bronx Zoo • Debbie Asnis, Flushing Hospital Links between investigations established in September 1999 West Nile Virus, New York City, 1999, Timeline June & July 1999: • Epizootic begins, dead crow reports • Veterinarian (Flushing/Brooklyn) finds crows with signs of nervous system disorders • No human illnesses identified (retrospective review) August 1999: • Epizootic: Bronx zoo birds die (~8/25). Samples to NYS Department of Environmental Conservation (DEC) • Epidemic begins in 1st week 8/2 – First human infection (retrospective) 8/12 – First case admitted to Flushing hospital 8/23 – 5th case admitted, Hospital contacts NYC-DOH 8/31 – Samples arrive at NYS-DOH lab WNV in NYC in 1999 September 1999: • Epizootic: Avian samples to USGS & USDA. Unidentified virus isolated. Connecticut: Virus isolated from crow brain Isolates sent to CDC • Epidemic: 9/1 NYS-DOH lab: Antibody to Flavivirus (SLE?) 9/3 CDC DVBID confirms SLE; NYC starts vector control Autopsy samples to UC Irvine Late September 1999 – Investigations come together • Virus identified as Flavivirus by CDC (WNV-like) & UC Irvine (Kunjin) • Repeat serology, high-titer antibody against WNV • Complete sequence identifies West Nile virus from birds/humans • WNV identified from mosquitoes collected in NYC NYC 1999 isolate essentially identical to 1998 isolate from Israel (Epidemic transmission) (Low level, zoonotic transmission) Lanciotti et al. 1999. Origin of the West Nile virus responsible for an outbreak of encephalitis in the northeastern U.S. Science 286:2333-337. WNV in NYC in 1999 October 1999: • Equine outbreak on Long Island reported • WNV-positive dead crow found in Baltimore Jan-Feb 2000: • WNV found in overwintering dormant female Cx. pipiens in NYC WNV transmission (Eastern U.S.) Culex quinquefasciatus Enzootic vector Culex pipiens Enzootic vector (Maintenance/Amplification) Amplifying hosts Primary Enzootic Cycle WNV transmission Enzooticvector vector Enzootic Incidental hosts Humans Horses Other mammals Bridge vectors* Amplifying hosts Cx salinarius Cx nigripalpus Ochlerotatus sollicitans Oc taeniorhynchus Aedes vexans Ae albopictus Cx tarsalis * Epidemic potential What About Crows? High mortality throughout region Short time from infection to death Intermediate virus titer Unlikely to be amplifying host driving epidemic & epizootic Unlikely to be reservoir host allowing seasonal persistence “I love the smell of malathion in the morning” West Nile Virus Human Illness <1% infections West Nile neuroinvasive disease(WNND) Encephalitis, meningitis, myelitis Increased risk with age & co-morbid conditions Reportable condition 10 -30% infections West Nile fever (WNF) No “overt” CNS involvement WNF (10-30%) Fever, rash, headache, myalgia, arthralgia Not a reportable condition 70-90% infections Asymptomatic infection Not reportable condition Same virus / antibody kinetics WN Life-longAsymptomatic immunity (70-90%) Potentialinfection problem for blood banking & organ donation Clinical Spectrum of WNV Illness: Revised WN Meningitis WN Fever WN Encephalitis WN “Poliomyelitis” Inflammatory Neuropathy Radiculopathy / plexopathy Surveillance for mosquito-borne zoonoses • Weather conditions (temperature & precipitation • Wild-bird population: • Sick/dead birds – test for virus (WNV, Usutu) • Healthy birds – test for antibodies • Sentinel chicken flocks – test for antibodies • Mosquito collections – test for virus • Horses – encephalitis – test for antibodies • Human illnesses • Viremic blood donors (WNV) WNV Disease Surveillance http://diseasemaps.usgs.gov/ 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 West Nile Virus Neuroinvasive Disease Cases in United States (by year) Regional epidemics WNND Cases 3000 Average = 1295/yr 2500 2000 1500 1000 2007 2006 2005 2004 2003 2002 2001 2008* (*As of 11/18/2008) 2000 0 1999 500 First Reported WNV Activity by State, 1999-2008 1999 2000 2001 2002 2003 2004 Average Annual Incidence of WNND, by County, U.S., 2004-2007 Human WNV Cases in Washington State, 2006-2008 Whatcom Okanogan Skagit Stevens Island Snohomish Clallam Chelan Jefferson Kitsap Grays Mason Harbor Thurston Pacific Wahkiakum Pend Oreille Ferry San Juan Douglas King (1 human) Pierce (2 humans) Kittitas Lewis Yakima (2 humans) Cowlitz Skamania Clark (1 human) Lincoln Spokane Grant Adams Whitman Franklin Garfield Benton Walla Columbia Walla Asotin Klickitat WNV-infected human identified in county Culex tarsalis • • • • • “The” vector of irrigated lands in arid west Efficient WNV transmitter in lab Long distance flier Feed equally on birds & mammals High infection rates in 2003 Estimated Number of WNV Infections & Fever Cases, U.S., 1999-2008 Reports of WNV fever vary widely WNND best indicator of WNV transmission among humans 11,807 cases of neuroinvasive disease in 10 years Based on serosurveys: • 140 WNV infections per 1 WNND case 140 x 11,807 WNND = ~1.65 million infections • 28 WNV fever cases per 1 WNND case 28 x 11,807 WNND = ~331,000 WNV fever West Nile Virus - The most widespread of the JE serocomplex flaviviruses Transmission of WNV Without Mosquitoes Viremia Concentration WNV-CNS tissue Serum & CSF IgM Ab IgG & Nt Ab Infection Illness onset Incubation: 2-15 days D4 – D6 illness 1Y after illness D14 – D21 illness Surveillance for Asymptomatic WNViremic Blood Donors 23 transfusion-associated WNV infections identified in 2002 Beginning 2003, all blood donations screened using NAT “Presumed Viremic Donors” (PVD) reported to state health departments which report cases to ArboNET WNV Transfusion- & TransplantationAssociated Disease 2002-2008, 32 transfusion (TFX)-associated WNV illnesses reported Last documented TFX-associated cases in 2006 2002-2008, 7 transplantation-associated WNV illnesses reported • 4 cases in 2002, 3 cases in 2005 Last documented TFX-associated cases in 2005 Disease Control Strategies to prevent arboviral infections Alter environment: • Reduce mosquito breeding habitats • Screen windows/doors Kill mosquitoes: • Larvicide/ Bacillus thuringienis applications • Aerial spraying (“adulticide”) • Tailor to habits of specific vector • Mosquito fish & copepods Humans & personal protection: • Restrict outdoor activity at dawn & dusk • Wear long-length clothing • Mosquito repellant use Human-Driven Ecological Changes That Alter Incidence of Mosquito-Borne Zoonoses Deforestation Large-scale water projects Global climate change Urbanization Industrial agriculture practices Industrial animal husbandry practices Widespread use of pesticides Water pollution Introduction of exotic species Tendency towards monoculture Environmental Change & Potential Changes to Mosquito-Borne Zoonotic Diseases Increase amplifying hosts • Example: Hog farms that ↑ Japanese encephalitis virus transmission in Southeast Asia • Example: Rice monoculture in peri-urban areas of SE Asian cities Increase vector species • Example: Irrigation practices that ↑ West Nile virus transmission in CO & NE