THE SPATIAL-TEMPORAL DISTRIBUTION OF DROUGHT, WETTING, AND
HUMAN CASES OF ST. LOUIS ENCEPHALITIS IN SOUTHCENTRAL FLORIDA
JEFFREY SHAMAN, JONATHAN F. DAY, AND MARC STIEGLITZ
Department of Earth and Planetary Sciences, Harvard University, Cambridge, Massachusetts; Florida Medical Entomology
Laboratory, Institute of Food and Agricultural Sciences, University of Florida, Vero Beach, Florida; Lamont-Doherty Earth
Observatory, Columbia University, Palisades, New York
Abstract. Using a dynamic hydrology model, we simulated land surface wetness conditions at 42 sites in 28 counties
in southcentral Florida from 1990 to 1998 and compared these simulations with the incidence of human cases of St. Louis
encephalitis (SLE) within these counties. Within counties, drought four months prior and wetting one-half month prior
were significantly associated with human cases of SLE. Simulated land surface wetness conditions resolved transmission
loci in both space and time, and May drought was significantly associated with the subsequent occurrence of human SLE
cases. These findings are consistent with previous results associating simulated land surface wetness conditions with the
transmission of SLE virus as measured in sentinel chickens, and support our working hypothesis that springtime drought
facilitates SLE virus amplification in mosquito and wild bird populations.
INTRODUCTION
Within Florida, four general patterns of transmission of St.
Louis encephalitis (SLE) virus to humans have been observed
since 1952.
1
During the vast majority of years, no human cases
have been reported. During some years, such as 1993, small,
focal outbreaks, usually involving fewer than 10 human cases,
were reported in various locations throughout the state. The
1993 SLE outbreak involved eight human cases from a small
area on the border of Lee and Collier Counties. Another
transmission pattern involves sporadic human cases reported
over a wider geographic area. This type of transmission was
most recently observed in 1997 when nine human SLE cases
were reported from Brevard, Charlotte, Hillsborough, Lee,
Palm Beach, and Polk Counties. Sporadic transmission of
West Nile virus to humans was also reported throughout
Florida in 2001 and 2002. The final transmission pattern is of
greatest concern: a full-blown epidemic in which hundreds or
thousands of cases, some appearing in well-defined clusters,
are reported over large parts of south Florida. The most re-
cent Florida SLE epidemic occurred in 1990 when 226 clinical
cases and as many as 30,000 infections were reported through-
out southcentral Florida. Indian River County was the epi-
center of this outbreak.
1
Recently, we found an association between antecedent
drought, coincident wetting, and transmission of SLE virus in
Indian River County Florida.
2
We used a dynamic hydrology
model
3
to hindcast mean area water table depth (WTD) in
Indian River County, and compared this model simulation to
sentinel chicken seroconversion data. Seroconversion of sen-
tinel chickens, as measured by serum assay for hemagglutina-
tion inhibition (HI) antibodies to SLE virus, has been
strongly correlated with the clinical disease in humans.
4
Using
logistic regression, we found the probability of sentinel
chicken seroconversion, i.e., transmission of SLE virus, to be
strongly associated with low WTDs 11-17 weeks prior and
higher WTDs 0-2 weeks prior.
2
A mechanism for this empirical relationship was suggested
by mosquito collection data obtained in Indian River County
from 1986 to 1991. Culex nigripalpus Theobald is the demon-
strated enzootic and epidemic vector of SLE virus in south
Florida.
5–7
Collections of Cx. nigripalpus were made in
densely vegetated “hammock” (an island of dense native veg-
etation) habitats used by this species for daytime resting.
8
During the driest conditions (low modeled WTD) preceding
heavy SLE virus transmission, Cx. nigripalpus collections dra-
matically increased.
2
Rather than indicate an increase of mos-
quito abundance, these data suggest that drought restricts Cx.
nigripalpus activity to the more humid hammock habitats.
Extreme drought periods in south Florida tend to occur dur-
ing the spring, a time when nesting wild birds also make use
of the hammocks. Thus, drought drives the mosquitoes and
birds into contact with one another. This forced interaction of
vector mosquitoes and susceptible avian amplification hosts
provides an ideal environment for the rapid epizootic ampli-
fication of SLE virus. In addition, confinement of blood fed
and gravid Cx. nigripalpus females to the hammock habitats
for extended periods forces more infected females to com-
plete the extrinsic incubation of acquired arboviruses during a
single gonotrophic cycle.
1,8
Subsequently, when the drought
ends and water resources increase, infected mosquitoes and
birds disperse and carry the virus from the hammocks. Gravid
female mosquitoes oviposit, re-feed, and if infective, they ini-
tiate the early transmission phase of the Florida SLE cycle.
Additional supporting evidence was found from wild bird
serologic data obtained during the 1990 SLE epidemic. We
showed that the presence of HI antibodies to SLE virus in
wild birds was significantly associated with modeled anteced-
ent drought, coincident wetting, and the emergence of the
Florida SLE virus vector, Cx. nigripalpus, five weeks prior.
9
Our findings suggest that three factors conspired to create the
1990 epidemic: 1) a large population of susceptible wild birds;
2) severe springtime drought, which facilitated amplification
of the SLE virus among the Cx. nigripalpus and a portion of
the wild bird population; 3) continued rainfall and wetting of
the land surface in the summer and early fall, which sustained
a large, active Cx. nigripalpus population. The continued bit-
ing and reproductive activity of Cx. nigripalpus maintained
levels of epizootic transmission throughout the summer and
early fall in Indian River County. These constant high levels
of SLE virus amplification facilitated spillover transmission to
humans throughout much of southcentral Florida.
In this study, we shift our analysis to human cases of SLE
reported throughout southcentral Florida. We hypothesize
that the spatial-temporal organization of human SLE cases in
Florida is tied to hydrologic variability. Specifically, we pro-
pose that the epidemic transmission with Indian River County
as the epicenter in 1990, the focal transmission with Lee and
Am. J. Trop. Med. Hyg., 71(3), 2004, pp. 251–261
Copyright © 2004 by The American Society of Tropical Medicine and Hygiene
251