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.

I

n 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 prevent infection?

In 2003, ≈30% (2,947) of human WNV cases in the

United States were reported in Colorado. Among infected

residents, 63 died (1). WNV transmission was especially

intense in northern Colorado, including Larimer County.

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 Larimer County 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).

Loveland and Fort Collins are both situated in a high

plains ecologic zone. The dominant WNV vector mosquito species are Culex tarsalis and Cx. pipiens (6). During

the 2003 outbreak, ≈20–40 mosquito traps were collected

Behavioral Risks for West Nile Virus

Disease, Northern Colorado, 2003 

Indira B. Gujral,* Emily C. Zielinski-Gutierrez,† Adrienne LeBailly,* and Roger Nasci†

Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 13, No. 3, March 2007 419

*Larimer County Department of Health and Environment, Fort

Collins, Colorado, USA; and †Centers for Disease Control and

Prevention, Fort Collins, Colorado, USA
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 VectorBorne Infectious Diseases at CDC (Fort Collins, CO,

USA). 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).

Larimer County 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,

Larimer County 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.

Methods

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, IL, USA).

The exposure factor of interest was residence (Fort

Collins vs. Loveland). Outcomes were based on selfreported 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

RESEARCH

420 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 13, No. 3, March 2007

Figure. Culex tarsalis and Cx. pipiens density (average number

collected per trap night) and vector index (reflecting the average

number of infected mosquitoes collected per trap night), Fort

Collins and Loveland, Colorado, July 26, 2003 through September

5, 2003. 
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).

Results

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 1).

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 mosquitobreeding 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

Behavioral Risks for West Nile Virus Disease

Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 13, No. 3, March 2007 421
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.

Discussion

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 duskto-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 proRESEARCH

422 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 13, No. 3, March 2007
portion 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 Larimer County,

biting pressure from the nuisance mosquito Aedes vexans

(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

Behavioral Risks for West Nile Virus Disease

Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 13, No. 3, March 2007 423
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 behaviors.

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.

Acknowledgments

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 Colorado

State University. 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.

References

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Address for correspondence: Indira B. Gujral, 1415 Crestmore Pl, Fort

Collins, CO 80521, USA; email: indiragujral0214@msn.com

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Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 13, No. 3, March 2007 425

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