A La Crosse virus case study

Invasive Species Impacting Native
Disease Dynamics: A La Crosse virus
case study
M. Camille Harris DVM, MS, PhD
Wildlife Disease Coordinator, U.S. Geological Survey
Chair, Animal Pathogens Subcommittee, Federal Interagency Committee on
Invasive Terrestrial Animals and Pathogens (ITAP)
April 1, 2016
Zika isolated from at least 16 mosquito species
“To assume that the main vector
is Ae. aegypti in areas in which
other mosquito species coexist is
naive, and could be catastrophic if
other species are found to have
important roles in Zika virus
transmission.”
Constância F J Ayres
Ayres, C.F., 2016. Identification of Zika virus
vectors and implications for control. Lancet
Infect Dis, 16: 278-279.
Slide from Monath, T.P. 2016. Virus Reservoirs and Vectors. Research Priorities to Inform Public Health and Medical Practice for Domestic Zika Virus: A
Workshop. National Academies of Sciences. Washington, DC.
http://diseasemaps.usgs.gov/mapviewer/
USGS Ecosystems Overview
Invasive
Species &
Disease
La Crosse virus (LACV)
• Family Bunyaviridae
• Genus Orthobunyavirus
• California encephalitis virus
• Negative-sense single-stranded
circular RNA virus
Aedes triseriatus
Borucki et al. 2002
La Crosse Virus & Forest Disturbance
• Temperate forest mosquito community
• LACV vectors
• LACV vertebrate hosts
• LACV prevalence
• Mosquito LACV nucleic acid detection
• Chipmunk LACV seroprevalence
Southern Appalachian Silviculture and
Biodiversity Project (SASAB)
DISTURBANCE
STAND AGE
SW
CCUT
FCON
Study Sites & Treatments
BB3
BB1
BB2
NC
Does forest disturbance influence the mosquito
community?
LACV Vectors
• Cx. pipiens
• Thompson et al. 1972
• Ae. canadensis
• Berry et al. 1986
• Nasci et al. 2000
Ae. triseriatus
Ae. japonicus
Ae. albopictus
Cx. pipiens/restuans
Ae. canadensis
Ae. vexans
• Ae. vexans
• Berry et al. 1983
Abundance of Primary LACV Vector and
Recent Invasive Decline With Disturbance
F3,380=28.1, p<0.0001
Ae. triseriatus
F3,380=20.1, p<0.0001
Ae. japonicus
Harris, MC. 2014. Forest Disturbance, Mosquito Vector Ecology and La Crosse Virus Dynamics in Southwestern Virginia
An established invasive and floodwater mosquito
increase in abundance with disturbance
F3,380=3.5, p= 0.016
F3,380=6.2, p=0.0004
Ae. albopictus
Ae. canadensis
Harris, MC. 2014. Forest Disturbance, Mosquito Vector Ecology and La Crosse Virus Dynamics in Southwestern Virginia
Culex spp. have no clear treatment preference
Ae. vexans abundance was greatest on the CCUT
F3,380=4.5, p= 0.0042
F3,380=3.2, p= 0.022
Ae. vexans
Cx. pipiens/restuans
Harris, MC. 2014. Forest Disturbance, Mosquito Vector Ecology and La Crosse Virus Dynamics in Southwestern Virginia
Does forest disturbance influence LACV
vector abundance?
• Yes but in different ways:
•
•
•
•
Ae. triseriatus and Ae. japonicus declined with disturbance
Ae. albopictus and Ae. canadensis increased with disturbance
Ae. vexans most abundant on the clearcut
Cx. pipiens/restuans – no clear treatment preference
La Crosse Virus & Forest Disturbance
• Temperate forest mosquito community
• LACV vectors
• LACV vertebrate hosts
• LACV prevalence
• Mosquito LACV nucleic acid detection
• Chipmunk LACV seroprevalence
Does forest disturbance influence LACV
detection in mosquito vectors?
Most Mosquito LACV Detections on FCON
6
LACV Detected in 6 of 1,595 Vector Pools
χ2=9.7, d.f.=3, p=0.02
5
4
3
2
1
0
CCON
FCON
CCUT
SW
Treatment
Harris, MC. 2014. Forest Disturbance, Mosquito Vector Ecology and La Crosse Virus Dynamics in Southwestern Virginia
LACV Detected in Accessory Vectors Only
Ae. japonicus
Cx. pipiens/restuans
Ae. vexans
Ae. triseriatus
3 LACV+ Pools
452
2 LACV+ Pools
375
1 LACV+ Pool
65
0 LACV+ Pools
590
Harris, MC. 2014. Forest Disturbance, Mosquito Vector Ecology and La Crosse Virus Dynamics in Southwestern Virginia
Invasive Mosquitoes and LACV
Photo Credit: CDC Public Health Image Library
Invasive Mosquitoes and LACV
• Vector Competence & TOT
• Hughes et al. 2006
• Field LACV Detections & Isolations
• Gerhardt et al. 2001
• Lambert et al. 2010
• Westby et al. 2011; 2015
Invasive Mosquitoes and LACV
• Vector Competence
• Sardelis et al. 2002
• Field LACV detections & isolations
• Harris et al. 2015
• Detection in eggs
• Westby et al. 2015
Photo Credit: CDC Public Health Image Library
Harris et al. 2015. Detection and isolation of La Crosse virus in field-collected Aedes japonicus japonicus (Diptera: Culicidae) in the Appalachian Region,
USA. Emerging Infectious Diseases. 21(4): http://dx.doi.org/10.3201/eid2104.140734
Harris et al. 2015. Detection and isolation of La Crosse virus in field-collected Aedes japonicus japonicus (Diptera: Culicidae) in the Appalachian Region,
USA. Emerging Infectious Diseases. 21(4): http://dx.doi.org/10.3201/eid2104.140734
Harris et al. 2015. Detection and isolation of La Crosse virus in field-collected Aedes japonicus japonicus (Diptera: Culicidae) in the Appalachian Region,
USA. Emerging Infectious Diseases. 21(4): http://dx.doi.org/10.3201/eid2104.140734
Harris et al. 2015. La Crosse virus field detection and vector competence of Culex mosquitoes. American Journal of Tropical Medicine & Hygiene. 93(3):
461-467. doi:10.4269/ajtmh.14-0128
LACV & Culex Mosquitoes
• Both Cx. restuans and Cx. pipiens were susceptible to
infection
• Based on salivary expectorate, their ability to transmit LACV
was poor in comparison to Ae. triseriatus
• Nutritionally-stressed Cx. restuans larvae were significantly
more likely to disseminate and transmit LACV
Cx. pipiens/restuans
Does forest disturbance influence LACV
detection in mosquito vectors?
• Most mosquito LACV detections were on undisturbed treatments
• All LACV detections were in accessory vectors
Summary
• Mosquito vector populations were affected by forest disturbance in
different ways
• The primary LACV vector declined with disturbance
• Mosquito LACV detection declined with disturbance
• LACV was only detected in accessory vectors
LACV Risk and Forest
Disturbance
• Ae. triseriatus abundance and
mosquito LACV detections were
greatest in undisturbed forest
• Suspect greatest LACV vertical
transmission
• Greatest risk to humans
• Complicated by multiple vectors
• Other vertical transmitters
• Link between mosquito community
ecology and vector-borne disease
dynamics needs to be explored
Acknowledgements
• Dana Hawley, Sally Paulson, Francois Elvinger, XJ Meng, Robert Jones
• Co-Authors: Bryan L. Brown, Bryan Jackson, Dorian Jackson, Fan Yang, Steven Zink, Laura
Kramer, Eric Dotseth, Paul Marek
• SASAB Researchers (esp. Travis Belote, Carola Haas), Jesse Overcash (USFS)
• Lab: Laila Kirkpatrick, Jennifer Miller, Kevin Myles, Noah Thrope, Kylie Perkins, Lindsey
McAlexander, Genevieve Dudzinsky, Courtney Scarborough, Bryan Tims, Andrew Luna, Dee
Petit, Sean Kelly, Alexander Ciota
• Field: Nate Lambert, Allen Patton, RJ Wilding, Jake Bova, Bonnie Fairbanks, Cari Lynn Squibb
• CDC: Amy Lambert, Jason Velez, Olga Kosoy, Marvin Godsey, Robert Lanciotti, Roger Nasci
• VT: Jack Cranford, Bryan Jackson, Nancy Troyano, Jake Bova, Fan Yang, James Adelman,
Cassandra Nunez, Sahnzi Moyers, Ariel Leon, Laura Schoenle Thomas, Michelle Jusino, Vicki
Garci, Olya Milenkaya
Thank you!