Behavioral Risks for West Nile Virus Disease, Northern
Indira B. Gujral,* Emily C. Zielinski-Gutierrez,† Adrienne LeBailly,* and
*Larimer County Department of Health and Environment, Fort
Collins, Colorado, USA;
and †Centers for Disease Control and Prevention, Fort
Collins, Colorado, USA
In 2003, residents in 2 adjacent cities in northern Colorado
(Loveland and Fort
Collins) had severe outbreaks of human West
Nile virus (WNV) disease. Unexpectedly, age-adjusted neuroinvasive disease rates were higher in Loveland
(38.6 vs. 15.9 per 100,000), which had a more extensive mosquito control
program and fewer mosquitoes. A survey was conducted to assess differences in
personal protection and risk practices by each city's residents. During May and
June 2004, a random-digit dial telephone survey was conducted among adults to
assess personal protection behavioral practices used to prevent WNV infection
during the 2003 outbreak. After we adjusted for identified risk factors, Loveland
residents were 39% more likely to report seldom or never using N,N-diethyl-m-toluamide
(DEET), and ≈30% were more likely to report being outdoors during prime
mosquito-biting hours than Fort Collins
residents. Personal protective practices may directly influence rates of WNV
infection and remain important even when comprehensive community mosquito
control measures are implemented.
In the United States, the mantra familiar to public health workers and
residents living in West Nile virus (WNV)–affected areas is to practice
the 4 Ds of prevention: 1) DEET (N,N-diethyl-m-toluamide): wear an insect repellent containing DEET; 2)
dress: wear long sleeves and long pants; 3) drain: drain standing water around
the home; and 4) dusk to dawn: limit time outdoors during this time. Although
the 4 Ds have been used by many state and local health departments to promote
personal prevention, the question remains, how well do these tactics work to
In 2003, ≈30% (2,947) of human WNV cases in the United
reported in Colorado. Among
infected residents, 63 died (1). WNV transmission was
especially intense in northern Colorado,
Among county residents, 546 laboratory-confirmed cases of WNV disease,
including 63 neuroinvasive disease cases and 9 deaths
(2), occurred. Officials at the Larimer County
Department of Health and Environment noted differences in age-adjusted rates of
WNV neuroinvasive disease between the 2 largest
cities in the county. WNV neuroinvasive disease rates
were used because neuroinvasive cases are more likely
to be captured in surveillance systems because of illness severity, which often
requires hospitalization and prompt laboratory diagnosis, unlike the generally
milder West Nile fever. Furthermore, WNV neuroinvasive disease cases are typically used to draw
comparisons between geographic areas and assess rates over time (3,4). The city of Loveland
had a much higher age-adjusted rate of neuroinvasive
disease (38.6/100,000) than the city of Fort Collins
(15.9/100,000); standardized risk ratio 2.43 (95% confidence interval [CI]
1.21–4.87, p<0.01). These findings were unexpected given the ecologic
and demographic similarities of the 2 cities and a long-term comprehensive
mosquito control program in Loveland.
Among the 265,489 LarimerCounty
residents in July 2003, most lived in the cities of Fort Collins
(125,461) and Loveland (55,905) (5). Although some
limited ecologic differences exist (i.e., Loveland
water surface area is ≈2.5× greater), Fort Collins
and Loveland are largely similar.
Demographically, both cities are ≈90% white with 9% reported Hispanic
ethnicity, 8%–13% of the residents are >65 years of age, and
the annual household estimated median income is ≈$45,000 per year (5).
Figure.Culextarsalis and Cx.
pipiens density (average number collected per
trap night) and vector index (reflecting the average number of infected
mosquitoes collected per trap night)...
Loveland and Fort
Collins are both situated in a high plains ecologic
zone. The dominant WNV vector mosquito species are Culextarsalis and Cx.
During the 2003 outbreak, ≈20–40 mosquito traps were collected per
city per week by using CO2 baited Centers for Disease Control and
Prevention (CDC) miniature light traps. Mosquitoes were collected by the
Colorado Mosquito Control (Brighton, CO, USA) and the Division of
Vector-Borne Infectious Diseases at CDC (Fort Collins,
During the height of the outbreak, from July 26, 2003, to September 5, 2003,
the mean ± standard deviation number of Cx. tarsalis and Cx.
pipiens mosquitoes collected per trap night
was higher in Fort Collins (Cx. tarsalis 76 ± 62, Cx.
pipiens 31.5 ± 13.2,) than in Loveland (Cx. tarsalis 43
± SD 34, Cx. pipiens
7 ± 1) (Figure). On the basis of 7,037 mosquitoes tested
(4,999 Cx. tarsalis
and 2,038 Cx. pipiens),
the WNV infection rates (estimated number of mosquitoes infected/1,000 tested)
were approximately equivalent in the 2 cities during that period (Cx. tarsalis
14.7 in Fort Collins, 12.8 in Loveland; Cx. pipiens 25.9 in Fort Collins, 21.2 in Loveland). A
vector index was calculated to estimate the average number of WNV-infected
mosquitoes collected per trap night (i.e., summation of the product of the
average number Culex mosquitoes collected
per trap night and the proportion infected for each species). More WNV-infected
mosquitoes were present in Fort Collins
than in Loveland (Figure)
(CDC, unpub. data). This finding was consistent with
mosquito control efforts occurring during that period; Loveland had an
integrated mosquito control program in place since 1986, and Fort Collins
reacted to the outbreak by implementing an emergency mosquito control program
later in the outbreak (mid-August through early September).
health officials encouraged residents to "Fight the Bite,"
specifically, to practice the 4 Ds of prevention. The difference in
age-adjusted rates of WNV neuroinvasive disease
between the 2 cities was unexpected because Fort Collins
residents were exposed to a larger number of WNV-infected mosquitoes. To understand
the differences in rates of neuroinvasive disease in
the 2 cities, LarimerCounty
health officials commissioned a survey to assess city residents' knowledge,
attitudes, and beliefs about WNV and to measure reported personal protective
practices during the 2003 WNV season. The purpose of this study was to increase
our understanding of the role of individual preventive measures by assessing
post hoc the behavioral practices among residents of Fort
Collins and Loveland.
From May 4 to June 7, 2004,
the Survey Research Unit of the Colorado Department of Public Health and
Environment in Denver performed a
random-digit-dial telephone survey among residents of Fort
Collins and Loveland.
The survey was developed by the Larimer County Department of Health and
Environment, CDC, and the Colorado Department of Public Health and Environment.
The survey consisted of 42 questions; 27 (64.0%) questions were specifically
related to WNV, and 15 (36.0%) questions concerned demographic information.
Questions were derived from the 2003 Colorado Behavioral Risk Factor
Surveillance System, local agency staff, and a survey conducted by the
Mississippi Department of Health (7,8).
All households with telephones in Fort Collins
and Loveland were eligible for
inclusion. One adult >18 years of age who lived within the city
limits of Fort Collins or Loveland from July through August 2003 was randomly
selected from each household to participate. Each phone number in the sample
was called <15 times, with at least 3 attempts in the evening, 3
during the day, and 3 on the weekend until the total number of desired
completed interviews was obtained. Interviews were conducted in either English
or Spanish. All interviews were completed by using Computer-Assisted Telephone
Interviewing software (Sawtooth Technologies, Northbrook,
The exposure factor of interest was residence (Fort
Collins vs. Loveland).
Outcomes were based on self-reported WNV preventive practices during the 2003
outbreak. Five outcomes were used: DEET repellent use (DEET was the only insect
repellent active ingredient recommended in 2003); draining standing water;
dressing in long clothing (pants and long-sleeved shirts); minimizing hours
outside from dusk to dawn on weekends; and minimizing hours outside from dusk
to dawn on weekdays. Outcome variables were dichotomized as follows: DEET and
dress (sometimes, nearly always, or always vs. seldom or never); drain (yes vs.
no); dusk to dawn on weekends (<2 h vs. 3–40 h outside); and dusk
to dawn on weekdays (<5 h vs. 6–60 h outside).
Explanatory variables investigated included sex, age, ethnicity, income,
education, owning an air-conditioner or swamp cooler, WNV risk perception, and
awareness of a local mosquito control program. Variables were classified as
follows: sex (male and female); age in years (18–44 and >45);
ethnicity (non-Hispanic and Hispanic); income in US dollars (<$25,000,
$25,000–50,000, and >$50,000); education (a high school diploma or
less and college or higher); an air-conditioner or swamp cooler in home (yes
and no); risk perception (very worried, somewhat worried, and not worried about
getting sick from WNV); and awareness of a mosquito control program in city of
residence (yes and no).
Analysis was conducted by using anonymized data. A
Z test was used to identify statistically significant (p<0.05) differences
in the proportion of residents reporting selected characteristics. Five
unconditional logistic regression models were used to estimate the odds of each
outcome among Fort Collins and Loveland
residents while adjusting for identified risk factors. Models were built by
using purposeful selection, a 5-step method for selecting variables based on
both biologic importance and statistical significance. As outlined by Hosmer and Lemeshow (9), the 5 steps of purposeful selection are 1) test for univariate significance (p<0.25); 2) build the
multivariate model (p<0.05); 3) test for confounding; 4) assess continuous
variables for linearity; and, 5) test for effect modification and include
interaction terms that are both significant (p<0.05) and biologically
plausible. Model fit was determined by using the Hosmer–Lemeshow goodness-of-fit test (9).
Because 5-point Likert scales can place persons in
the middle category (10), final unconditional
logistic regression models were retested to determine if similar results would
be found between models in which the response "sometimes" was
included in the opposite category (seldom and never). Statistical analyses were
performed by using SAS version 9.1 software (SAS, Cary, NC, USA).
Among the 3,739 county households identified, 1,230 were sampled. Of these,
256 (20%) refused sampling 11 (1.1%) terminated the interview before it was
completed, 6 (0.9%) had a language barrier, and 957 (78%) were surveyed. Fort
Collins residents included 424 (44.3%) of those
interviewed. Survey demographics reflect the general populations of Loveland
and Fort Collins (5).
Among those surveyed, significant (p<0.05) differences were found between
Fort Collins and Loveland residents by sex, age group, income, education, and
ownership of an air-conditioner or swamp cooler. Compared with Loveland
survey participants, more residents of Fort Collins
were female, younger (18–44 years of age), had a higher income
(>$50,000), educated (more than a high school diploma), and reported no
air-conditioner or swamp cooler in the home (Table
Significant differences (p<0.05) between Fort Collins and Loveland
residents were observed for those reporting DEET use and those spending time
outdoors from dusk to dawn on both weekends and weekdays (Table
2). The proportion of persons who reported seldom or never using DEET was
higher among Loveland residents
than among Fort Collins residents.
Likewise, a higher proportion of Loveland
residents reported spending >2 h outdoors from dusk to dawn on weekends and
spending >5 h outdoors from dusk to dawn on weekdays.
Five unconditional multivariate logistic regression models were built to
test for an association between city of residence and reported WNV preventive
behavior. The drain model was omitted after careful review of the survey
question deemed it too vague for a meaningful interpretation. This was
unfortunate because draining water from around a residence may reduce exposure
to mosquito-breeding sites.
When we adjusted for sex, age, and risk perception, Loveland residents were
39% (95% confidence interval [CI] 1.04–1.76) more likely to report that
they seldom or never used DEET than Fort Collins residents (Table
3). Among residents surveyed about DEET use, persons >45 years of age
were 62% (95% CI 1.21–2.18) more likely to report seldom or never using
DEET than younger respondents. Persons who were not worried about WNV were 4×
(95% CI 2.90–7.51) more likely to report that they seldom or never used
DEET than persons who sometimes, nearly always, or always worried about WNV.
Similar results were obtained when the model was tested with the sometimes
response included in the seldom or never group.
After we adjusted for identified risk factors, no statistically significant
difference was observed between Fort Collins
and Loveland residents who reported
seldom or never wearing long clothes to protect against mosquitoes. However,
persons who reported that they were not worried about getting sick from WNV
were 2.5× (95% CI 1.25–5.28) more likely to report not wearing protective
clothing. Similar results were obtained when the sometimes response was
included in the seldom or never response group.
Participants were surveyed regarding amount of time spent outdoors from dusk
to dawn during the week and on weekends. Compared with the Fort Collins
residents, Loveland survey participants were 35% (95% CI 1.01–1.82) more
likely to report spending >5 h outdoors during the week from dusk to dawn
when adjustments were made for sex, age, education, and income. The model also
held a statistically significant and plausible interaction term; males earning
<$25,000 per year were more likely to report spending >5 h outside from
dusk to dawn during the week.
Compared with Fort Collins
residents, Loveland residents were
30% (95% CI 1.00–1.74) more likely to report spending >2 h outdoors
from dusk to dawn on weekends when adjustments were made for sex, age, and risk
perception. Similarly, persons who reported they were somewhat worried or not
worried about getting sick from WNV were 68% and >2× as likely (95% CI
1.07–2.65 and 1.31–3.51), respectively, to report spending >2 h
outdoors from dusk to dawn on weekends than persons very worried about getting
sick from WNV.
During the 1999 WNV outbreak on Staten Island, New York, a serosurvey conducted by Mostashari
et al. found the highest seroprevalence of WNV among
persons who spent >2 h outdoors from dusk to dawn; persons were even more
likely to be seropositive if they reported never
using a repellent containing DEET (11). In a recent
national study, 40% of survey participants reported using a repellent
containing DEET and draining standing water, 29% avoided perceived areas with mosquitoes,
28% avoided being outdoors from dusk to dawn, and 27% wore long sleeved-shirts
and long pants to avoid bites (12).
The results of this study suggest that differences in WNV neuroinvasive disease rates may be due, in part, to lower
use of repellents containing DEET and greater dusk-to-dawn outdoor exposure
among Loveland residents. These findings support the benefit of promoting
personal prevention approaches, particularly by using effective insect
repellents and reducing exposure to mosquitoes during prime-biting hours.
An alternative explanation for the differences in neuroinvasive
disease rates among Loveland and Fort
Collins residents may be unexplained ecologic
differences that influence the risk for infection. Loveland
has a greater proportion of water surface area than Fort
Collins, a difference that has been hypothesized to
influence mosquito populations, local bird populations, and human behavior.
However, on the basis of vector indices for 6 weeks of entomologic data
collected during the height of the 2003 outbreak, more WNV-infected mosquitoes
were present in Fort Collins than
in Loveland. This finding was
predictable, given that Fort Collins
implemented an emergency mosquito control program late in the WNV season.
Many results of this study are consistent with those of previous reports.
Older persons and those not worried about WNV infection were more likely to
report seldom or never using a repellent containing DEET (12,13). Similarly, persons with lower incomes
reported practicing fewer preventive behavioral measures. This finding was
evident in the dusk-to-dawn weekday model in which an interaction term
appeared; men with the lowest income levels were more likely to be outdoors
during the week from dusk to dawn. This result seems plausible given that
weekday workers have less control over outdoor exposure than nonworking hours
during the weekend and may specifically capture those engaged in agricultural
or landscaping work. No differences between Fort Collins
and Loveland residents were
observed for those reporting seldom or never wearing long clothes, which is not
surprising, given that few people use this strategy (12).
Although explanatory variables help identify the proportion of surveyed
persons not following the 4 Ds of prevention, they do not explain why Loveland
residents were less likely to practice personal prevention behavioral measures.
Loveland residents may have had
less knowledge of these prevention strategies.
However, this was unlikely, given widespread WNV educational efforts in both
cities and local and state media coverage of the outbreak. Furthermore, bivariate analysis of reported risk perception indicates
that both Fort Collins and Loveland
residents perceived very similar risks for WNV infection.
Perceived risk for disease was a consistent factor in the multivariate
models. Persons who were not worried about WNV were more likely to report
seldom or never using a repellent with DEET, not wearing long clothes, and
spending more time outdoors from dusk to dawn on the weekend. As noted by other
authors (14–16), risk perception is only one
of many factors that directly contribute to practicing preventive behavioral
measures. For example, environmental triggers may play a role. In a model
proposed by Zielinski-Gutierrez and Hayden, a person's experience with their
environment (i.e., seeing mosquitoes, getting bitten, or both) is one of the
most immediate triggers for taking protective action (17).
This was true for residents in Mississippi
who in 2003 reported feeling a mosquito bite as the most important reason for
taking precautions against mosquito bites (8). During
the outbreak in LarimerCounty,
biting pressure from the nuisance mosquito Aedesvexans (Fort Collins,
39.6/trap night), and Loveland
(22.6/trap night) along with Culex sp. may
have prompted residents to use repellent and practice other avoidance
strategies. Environmental triggers, such as biting pressure, may explain why Fort
Collins and Loveland
residents responded similarly to a general question on risk perception
regarding WNV but reported differences in preventive behaviors.
This possibility raises a related question, "Did Loveland residents
choose to rely on the city's control program instead of practicing individual
preventive measures?" Loveland
residents may have been less likely to have applied personal preventive
measures (the 4 Ds of prevention) given their reliance on the long-standing
community mosquito control program. Although difficult to establish with any
certainty, this prospect suggests the need to promote integrated prevention
with both community and individual actions complementing each another. Future
research should assess the multiple factors that contribute to risk perception
and address the human-environmental interactions that influence protective
Although this study is limited by recall and reporting bias because the
survey was conducted 8 months after the outbreak, these information biases are
most likely nondifferential since recall and
reporting would likely be similar among both Loveland
and Fort Collins residents. The
results of this study reinforce use of personal protection efforts even in
areas with strong community mosquito control measures and suggest that these
personal measures may influence disease rates. Furthermore, study results
suggest that persons residing in a city with greater mosquito-biting pressure,
as measured by a vector index, were more likely to take preventive measures
than persons in a community with less biting pressure. Future studies are
warranted to understand the effects of human-environment interactions to derive
the greatest benefit from community and personal efforts to reduce disease and
death from WNV.
We thank Alyson Shupe, Becky Rosenblatt, David Withum, and Brad Biggerstaff for
their assistance during the study.
Ms Gujral is a doctoral candidate in the
Department of Environmental Health and Radiological Sciences at ColoradoStateUniversity.
This work was conducted while she worked as a WNV health educator at the
Larimer County Department of Health and Environment in the summer of 2005.
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