Patient Knowledge and Attitudes about Antiviral Medication and

MAJOR ARTICLE
Patient Knowledge and Attitudes about Antiviral
Medication and Vaccination for Influenza in an
Internal Medicine Clinic
Michael A. Gaglia, Jr.,1,2 Robert L. Cook,3 Kevin L. Kraemer,1 Michael B. Rothberg4
1
Division of General Internal Medicine and 2Division of General Academic Pediatrics, University of Pittsburgh, Pennsylvania; 3Departments of
Epidemiology, Biostatistics, and Medicine, University of Florida, Gainesville; and 4Division of General Medicine and Geriatrics, Tufts University,
Boston, Massachusetts
(See the editorial commentary by Linder on pages 1189–91)
Background. Despite the introduction of Centers for Disease Control and Prevention guidelines for their use,
antiviral medications for influenza remain underutilized. Our objective in this study was to describe beliefs, attitudes,
and knowledge regarding antiviral medication and vaccination for influenza among patients in an internal medicine
clinic.
Methods. We conducted a cross-sectional survey of adult patients in an internal medicine clinic from April
through June 2006.
Results. Two-hundred eighty patients completed the survey. Fifty-five percent received influenza vaccination
for the most recent influenza season. Overall antiviral knowledge was poor. Of 8 antiviral knowledge questions,
the mean percentage of correct answers was 40%; 1 (!1%) of the patients answered all questions correctly, and
47 (18%) answered all questions incorrectly. Only 37 (13%) of the patients reported calling their physician within
48 h after the onset of influenza-like symptoms. Patients with conditions associated with a high risk of complications
from influenza were no more likely than other patients to be more knowledgeable about antiviral medication, nor
were they more likely to report calling their physician within 48 h after symptom onset or to report receipt of
influenza vaccination for the previous influenza season. Only 90 (37%) of the respondents were willing to pay
1$20 for antiviral medication, although 205 (84%) were willing to pay something.
Conclusions. Patients are ill-informed about antiviral medication and its benefits, and medication costs may
present a barrier to treatment. Physicians should discuss antiviral medication with patients who are at high risk
for complications from influenza before the influenza season, and education programs for physicians and patients
should be developed.
Influenza affects 5%–20% of the population each year
[1], and influenza-related illness is responsible for
∼51,000 deaths and ∼226,000 hospitalizations each year
in the United States [2, 3]. Vaccination remains the
cornerstone of influenza control and prevention, but
antiviral medications, such as the neuraminidase inhibitors oseltamivir and zanamivir, are a key component of the most recent recommendations by the Ad-
Received 11 April 2007; accepted 9 June 2007; electronically published 28
September 2007.
Reprints or correspondence: Dr. Michael A. Gaglia, Jr., Center for Research on
Health Care, University of Pittsburgh, Ste. 600, 230 McKee Place, Pittsburgh, PA
15213 ([email protected]).
Clinical Infectious Diseases 2007; 45:1182–8
2007 by the Infectious Diseases Society of America. All rights reserved.
1058-4838/2007/4509-0009$15.00
DOI: 10.1086/522192
1182 • CID 2007:45 (1 November) • Gaglia et al.
visory Committee on Immunization Practices [4].
Specifically, the recommendations emphasize that treatment of influenza should focus on patients who are at
high risk for influenza-related complications. The neuraminidase inhibitors have assumed an even more
prominent role for 2 reasons: the emergence of widespread resistance to the M2 ion channel-blocking drugs
amantadine and rimantadine [5] and the possible role
of neuraminidase inhibitors in helping to control an
avian influenza pandemic [6].
Neuraminidase inhibitors shorten the course of acute
influenza [7, 8], reduce bacterial complications of influenza [9, 10], and decrease influenza-related hospitalizations [11]. They are also cost-effective for both
treatment and prevention of influenza [12–15]. The
appropriate use of antiviral drugs for treatment of acute
influenza, however, requires education of both physi-
cians and their patients. Specifically, patients must know to
present promptly to their physician, because antiviral drugs are
not effective 148 h after onset of influenza symptoms; and
physicians must be able to rapidly diagnose influenza. The ability of physicians to diagnose influenza on clinical grounds alone
has proven to be inadequate, with physician judgment showing
a sensitivity of only 29% [16]. Physician knowledge of antiviral
drugs is also poor; only 28% of primary care physicians are
aware that antiviral drugs prevent bacterial complications of
influenza [17]. As a result, physicians prescribe antiviral medication for !20% of patients who receive a diagnosis of influenza [18, 19].
Patient knowledge and beliefs about antiviral medication are
important, because they might influence the likelihood of presenting within the 48-h window in which effective treatment
could be administered. There is a paucity of studies, however,
that address patient knowledge and attitudes regarding antiviral
medications, such as oseltamivir and zanamivir. The objectives
of this study were to describe patient knowledge and attitudes
regarding antiviral medications and to identify demographic
and clinical characteristics associated with higher levels of
knowledge regarding antiviral medication. We also sought to
examine the proportion of patients who would report calling
their physician within 48 h after the onset of influenza-like
illness. We hypothesized that patients with conditions associated with a high risk of influenza-related complications would
be more knowledgeable regarding antiviral medication and
more likely to report calling their physician within 48 h.
METHODS
Design. We distributed anonymous surveys from April
through June 2006 to a convenience sample of 400 patients at
an urban, university-affiliated general medicine clinic in Pittsburgh, Pennsylvania. Clinic staff distributed the survey to consecutive patients at check-in, as permitted by clinic patient flow,
and individual patients were free to discard the survey if they
did not wish to complete it. Information regarding patients
who did not return the survey was not available. We offered
no incentives to complete the survey. The study protocol was
approved by the University of Pittsburgh (Pittsburgh, Pennsylvania) Institutional Review Board.
Measures. We selected survey items to represent a broad
spectrum of health behaviors and attitudes that might be associated with knowledge regarding antiviral medication. Health
attitudes questions included beliefs about influenza infection
and vaccination. We selected specific health conditions to represent high-risk groups targeted for seasonal influenza vaccination by the Centers for Disease Control and Prevention:
chronic lung disease, diabetes, heart disease or stroke, chronic
kidney disease, sickle cell anemia or thalassemia, HIV infection,
history of organ transplantation, and history of malignancy [4].
Patients were considered to be at high risk for influenza complications if they had ⭓1 of the above conditions, regardless
of age.
The survey instrument consisted of the following primary
sections: demographic information, medical history, specific
health behaviors (e.g., receipt of influenza vaccination before
the most recent influenza season), knowledge regarding antiviral medication (with possible responses of “true,” “false,” and
“do not know”), attitudes toward and perceptions of antiviral
medication and influenza vaccination (likert-type scale of
strongly agree to strongly disagree), and willingness to pay for
antiviral medication. Immediately preceding the antiviral section, the survey explained that influenza infection is caused by
a virus and that antiviral medications, such as oseltamivir (Tamiflu; Roche) and zanamivir (Relenza; GlaxoSmithKline), are
used to treat it. We asked patients “When you have a cough
and fever, how long do you wait before you call the doctor?”
and offered the following choice of answers: “right away,” “1
day,” “2 days,” “12 days,” and “I usually don’t call.” We also
asked “If a medicine decreased the amount of time that you
were sick with a cough, fever, runny nose, and body aches by
1 day, how much would you be willing to pay for this medicine?” and offered the patient a choice of $0 or $10 intervals
up to $60. We also included questions pertaining to knowledge
and attitudes about avian influenza; these results will be reported elsewhere.
Clinic staff and physicians reviewed initial versions of the
survey for face validity and suggested changes for content and
clarity. The final version consisted of 34 items, was written at
an eighth grade reading level, and required 5–8 min to complete. The survey was in pen-and-paper format and was available only in English. Patients indicated responses by filling in
circles corresponding to each answer. After the surveys were
collected, we reviewed them for stray and incomplete marks
(e.g., slashes and checkmarks) and corrected them appropriately. We then scanned the surveys into a database using TELEform (Cardiff) and confirmed a 10% sample of the surveys
manually to validate the data capture process.
Data analysis. Analyses and data management were performed with Stata for Windows, version 9.0 (StataCorp). Surveys with incomplete responses were excluded from analyses
of that particular incomplete response, but they were not excluded from the entire study.
We quantified knowledge of antiviral drugs by computing
the percentage of correct responses to the 8 knowledge questions; “do not know” responses were considered to be incorrect,
and questions skipped by the respondent were not counted
towards the total number of questions answered. The distribution of the percentage correct was not a normal distribution,
so we constructed a categorical variable for level of antiviral
knowledge: low (0%–33% correct), moderate (34%–66% cor-
Knowledge and Attitudes about Antivirals • CID 2007:45 (1 November) • 1183
rect) and high (67%–100% correct). We then used either the
x2 or Fisher’s exact test to examine relationships of demographic characteristics, health characteristics, health behaviors,
and attitudes with the level of antiviral knowledge. We used
multivariable ordinal logistic regression to determine independent variables associated with higher antiviral knowledge, using
a forward regression technique with a P ! .15 threshold required
for an independent variable to remain in the multivariable
model. Only variables with a P value of ⭐.20 for the x2 or
Fisher’s exact test in univariable analyses were considered for
the multivariable model. The final multivariable model only
used survey respondents who answered all demographic, clinical, and attitude questions (222 respondents).
We also used multivariable logistic regression to examine the
association of patient knowledge and beliefs with the following
outcomes: willingness to pay for antiviral medication (!$20 vs.
1$20), time to calling a physician when experiencing influenzalike symptoms (!48 h vs. 148 h), and receiving an influenza
vaccination before the previous influenza season. We used the
same P value thresholds for model entry as were used for the
antiviral knowledge level regression.
RESULTS
Of 400 patients who were offered the survey, 280 (70%) responded. The survey population was similar to the overall clinic
population with respect to sex and race and was predominantly
white (80%) and college-educated (64%; table 1). Thirty-eight
percent of respondents had at least 1 disease associated with a
high risk of influenza-related complications, as defined by the
Centers for Disease Control and Prevention [4], and 46% were
⭓50 years of age. Only 55% received influenza vaccination for
the most recent influenza season. Of interest, 2% of respondents
admitted to having a home supply of antiviral medication “just
in case.”
In multivariable logistic regression, advancing age, but not
high-risk status, was associated with current vaccination status.
A composite measure of influenza risk (the number of conditions associated with a high risk of influenza-related complications, including age ⭓65 years) also was not associated
with receipt of influenza vaccination. Patients at high risk for
influenza-related complications (stratified by age) were slightly
more likely to have received influenza vaccination for the previous influenza season (figure 1), but the association was not
statistically significant.
When asked how long they waited to call their physician
when experiencing influenza-like symptoms, only 37 (13%) of
respondents reported calling within 48 h after symptom onset.
Multivariable logistic regression showed that a history of heart
disease (OR, 3.54; 95% CI, 1.09–11.46) and taking antibiotics
often for viral-like symptoms (OR, 1.64; 95% CI, 1.05–2.57)
were significantly associated with calling ⭐48 h after onset of
1184 • CID 2007:45 (1 November) • Gaglia et al.
Table 1. Demographic characteristics of patients who responded to the influenza survey.
Characteristic
Patients
(n p 280)
Age, mean years SD
Female sex
47 15.6
190 (69)
Race/ethnicity
White
Black
219 (80)
40 (15)
Asian
Hispanic
11 (4)
6 (2)
Other
Education
College or higher
Some college
High school or less
5 (2)
177 (64)
53 (19)
47 (17)
Annual income
!$20,000
$20,001–$75,000
1$75,000
Current smoker
Comorbidity
54 (21)
118 (46)
86 (33)
39 (14)
COPD/chronic lung disease
Heart disease
35 (13)
25 (9)
Diabetes mellitus
⭓1 Disease associated with high risk of
influenza-related complications
37 (13)
Received influenza vaccination for most recent influenza season
Previously received antiviral medication
Home supply of antiviral medication
105 (38)
151 (55)
66 (25)
5 (2)
NOTE. Data are no. (%) of patients, unless otherwise indicated. COPD,
chronic obstructive pulmonary disease.
symptoms. No other high-risk conditions, separately or as a
composite, were associated with calling within this time period.
When asked how much they were willing to pay for antiviral
medication that would shorten the duration of influenza-like
symptoms by 1 day (figure 2), 205 (84%) of the respondents
were willing to pay something, but only 90 (37%) were willing
to pay 1$20. According to multivariable logistic regression analysis, willingness to pay 1$20 for antiviral medication was associated with an annual income 1$75,000 (OR, 1.94; 95% CI,
1.23–3.05), belief that antiviral medication are scarce (OR, 2.19;
95% CI, 1.18–4.07), calling a physician within 48 h after influenza symptom onset (OR, 2.64; 95% CI, 1.05–6.68), and
taking “leftover” antibiotics for influenza-like symptoms (OR,
2.82; 95% CI, 1.01–7.84); the belief that one does not need
medication to recover from influenza was associated with less
willingness to pay (OR, 0.34; 95% CI, 0.17–0.66).
The mean percentage of correct responses to 8 antiviral
knowledge questions was 40% (table 2). One respondent (!1%)
answered all questions correctly, and 47 (18%) answered all
Figure 1. Receipt of influenza vaccination for the most recent influenza season, by age and risk group. High-risk group, patients at high risk for
influenza and influenza-related complications; low-risk group, patients at low risk for influenza and influenza-related complications.
questions incorrectly. Among respondents who answered all 8
knowledge questions (252 respondents), 40 (15%) answered
“do not know” to all 8 questions. Thirty percent knew that
antiviral medications only work if they are taken during the
first 48 h of symptoms. A significant percentage (96 respondents; 37%) believed that influenza vaccination can cause influenza; more than one-half of the respondents were worried
that there is not enough antiviral medication (133 respondents;
52%) or influenza vaccine (131 respondents; 51%) in the
United States. Approximately one-third of the respondents believed that they did not need medication to recover from influenza; there was no difference between patients at high risk
for complications and other patients in this regard.
Multivariable ordinal logistic regression analysis indicated
that 3 variables were significantly associated with a higher degree of antiviral knowledge: college education or higher (OR,
1.99; 95% CI, 1.37–2.91), the belief that influenza vaccination
is effective (OR, 1.94; 95% CI, 1.07–3.52), and the belief that
one does not need medication to recover from influenza (OR,
2.55; 95% CI, 1.41–4.60). Black race (OR, 0.39; 95% CI, 0.17–
0.90) and the belief that influenza vaccination causes influenza
(OR, 0.54; 95% CI, 0.30–0.96) were associated with lower antiviral knowledge.
CONCLUSIONS
We found that overall knowledge regarding antiviral medication
was poor. We also found that patients with conditions asso-
ciated with a high risk of influenza complications were no more
likely than patients without such conditions to report receipt
of influenza vaccination for the most recent influenza season
or to report calling their physician within 48 h after the onset
of influenza-like symptoms; in addition, patients with highrisk conditions were not more willing than others to pay 1$20
for antiviral medication. Perhaps most importantly, however,
patients with conditions associated with a high risk of complications from influenza were not more knowledgeable regarding antiviral medication; this was contrary to our initial
hypothesis.
Neuraminidase inhibitors are effective in decreasing the
length of illness and in preventing hospitalizations and bacterial
complications in patients with influenza who are at high risk
for complications [10, 11]. Furthermore, such treatment is endorsed by Centers for Disease Control and Prevention guidelines. Two potential barriers to treatment with antiviral drugs
are patient knowledge and the relatively high cost of the medications. Knowledge deficits are important because of the limited window of effectiveness for the neuraminidase inhibitors.
Patients must be aware of both the potential benefit of treatment in terms of decreasing morbidity and the need to present
for treatment as early as possible. We found that patients at
high risk for influenza-related complications are largely unaware of the benefits of antiviral medication. Except for patients
with heart disease (for whom the effect was small), patients
with high-risk conditions were not more likely than patients
Knowledge and Attitudes about Antivirals • CID 2007:45 (1 November) • 1185
Figure 2. Percentage of patients willing to pay for antiviral medication to treat influenza, by cost of medication
without high-risk conditions to call within the 48 h window.
Indeed, only 13% of all respondents stated they would call
within the appropriate time frame.
The knowledge deficit in our sample group was not limited
to antiviral medication, as evidenced by the 37% of respondents
who believed that influenza vaccination causes influenza. This
percentage is higher than that reported in a recent Medicare
Current Beneficiary Survey [20], conducted in 2001–2002, in
which ∼20% of respondents refused influenza vaccination because of the belief that it would cause influenza. A large proportion of respondents (63%) were unaware that antiviral medications are ineffective against bacteria, demonstrating that a
significant number of patients continue to misunderstand the
difference between viral and bacterial illness. This is consistent
with previous studies, which found a 21%–55% prevalence of
the false belief that antibiotics are effective for viral upper respiratory illnesses [21–23]. We also found that patients with
high-risk conditions who are !50 years of age continue to be
undervaccinated, with only 30% of respondents in our study
reporting recent influenza vaccination. This is in agreement
with national data, which reveal that only 26% of adults aged
18–49 years who are at high risk for influenza complications
have received a recent influenza vaccination [4]. This is troubling, because antiviral therapy is, at best, an adjunct strategy;
influenza vaccination remains the keystone of influenza prevention and control.
Even if patients receive a correct diagnosis within 48 h after
1186 • CID 2007:45 (1 November) • Gaglia et al.
onset, patients will not benefit from therapy unless they are
willing to pay for it. We found that only approximately onethird of patients are willing to pay 1$20 for antiviral medication,
which is a common level of copayment for brand-only medications. Even fewer patients (!10%) are willing to pay the
retail cost of the medication (∼$80 for a 5-day course [24]).
It is unclear if the expense of antiviral medication contributes
to the dearth of patients at high risk for influenza complications
who are treated with antiviral drugs; in our study, patients at
high risk for influenza complications were not more willing
than other patients to pay for antiviral medication. Physician
attitudes are also a likely factor in the relatively low use of
antiviral drugs; a recent study showed that 40% of primary
care physicians believe that influenza is self-limited and does
not require treatment [17].
In addition, our study demonstrates that, regardless of their
knowledge level, a majority of patients are worried about shortages of both antiviral medication and influenza vaccine. A small
number of patients even reported hoarding antiviral drugs.
There is a relative lack of data regarding how patients think
and behave regarding such shortages (whether real or perceived). One study found a spike in antiviral medication sales
in New York City in the fall of 2006, before the influenza season
began [25]; another study found that almost one-half of infectious diseases consultants had been asked by family or friends
for a neuraminidase inhibitor prescription specifically for stockpiling purposes [26]. The motivations for such behavior are
Table 2. Knowledge and attitudes regarding antiviral medication.
No. (%) of patients
Question (correct response)
Antiviral medicines work for a cold (false)
Antiviral medicines only work if you take them in the first 48 h of the flu (true)
Antiviral
Antiviral
Antiviral
Antiviral
medicines can also be taken to prevent the flu (true)
medicines decrease the amount of time you are sick with the flu (true)
medicines can sometimes cause the flu (false)
medicine usually has side effects, like nausea or dizziness (false)
Antiviral medicines are available over the counter (false)
Antiviral medicines also work against bacteria (false)
True
False
Do not know
37 (14)
79 (30)
116 (44)
37 (14)
109 (42)
147 (56)
(24)
(57)
(19)
(30)
89 (35)
18 (7)
102 (39)
23 (9)
106
95
111
158
16 (6)
14 (5)
152 (58)
63
147
49
79
(41)
(37)
(42)
(61)
93 (36)
151 (58)
95 (37)
Strongly
agree/agree
Neutral
Strongly disagree/
disagree
The flu shot protects you from the flu
The flu shot can cause bad side effects, like fever and rash
179 (69)
125 (49)
47 (18)
84 (33)
34 (13)
48 (19)
The flu shot can cause the flu
My own body can fight off the flu without help from medicine
I am worried there is not enough antiviral medicine in this country for everyone
I am worried there is not enough flu vaccine in this country for everyone
96
96
133
131
65
82
77
77
96
80
46
48
unclear, although fears of a future influenza pandemic are likely
to be a key factor.
Our survey has several limitations. First, we used an unvalidated instrument, because no validated instruments to measure
antiviral knowledge or attitudes were available. We did, however, test the instrument for face validity and content prior to
administration. Second, although the questions appear to capture straightforward attitudes and beliefs, patient knowledge
and attitudes are not static and could vary temporally on the
basis of future events regarding seasonal and pandemic influenza. Indeed, this is evidenced by the recent emergence of
neuraminidase-resistant strains of both human and avian influenza [27–29]. Any beliefs or hoarding behavior could certainly change if drug resistance became more widespread. Similarly, the actual behavior of respondents might differ from the
behavior reported in the survey. Third, our study was limited
to only 1 specific population in a clinic; one would anticipate
even lower knowledge scores, however, if this survey were applied to a population with lower education and socioeconomic
status. Future studies of this type would benefit from the use
of a broader sample of geographic areas and clinic types. Fourth,
we did not have data available for patients who were given the
survey but did not return it; this could have possibly introduced
bias.
Our results raise 2 issues: how to identify patients more
effectively before the 48-h treatment window expires and how
to manage the increased volume of patients with nonspecific
viral symptoms that would result. Diagnosis of influenza remains difficult [16, 30], and rapid testing has not gained universal acceptance [17]; therefore, practical strategies for both
(37)
(37)
(52)
(51)
(25)
(32)
(30)
(30)
(37)
(31)
(18)
(19)
screening and diagnosis are sorely needed. Future studies
should focus on educational interventions for patients and physicians, emphasizing the benefits of antiviral medication for
patients at high risk for influenza complications and the importance of early presentation. We also found that the false
belief that influenza vaccination causes influenza was associated
with lower knowledge of antiviral drugs; this suggests that education should emphasize the importance of influenza vaccination, as well. Studies are also needed to identify the best way
to triage patients with influenza-like symptoms who might benefit from antiviral treatment, to avoid overburdening the health
care system. Lastly, studies of fears regarding antiviral medication shortages and hoarding of antiviral medications are also
lacking.
Despite evidence that antiviral medications can decrease the
morbidity associated with influenza, physicians have been slow
to adopt their use. Our study provides a preliminary understanding of patient perceptions and knowledge regarding antiviral medications and their relation to beliefs regarding influenza and influenza vaccination. We found multiple barriers to
optimal detection and treatment of influenza, including poor
knowledge of influenza in general, a low percentage of patients
reporting that they would call within the first 48 h of illness,
and a lack of willingness to pay for antiviral medication. This
gap between patient and physician must be bridged with improved patient (and physician) education, more efficient efforts
in triage and diagnosis, and a focus on patients who are at high
risk for influenza and its complications. The challenge influenza
poses to the individual physician demands a paradigm shift in
the clinical approach to viral illness. Patients at high risk for
Knowledge and Attitudes about Antivirals • CID 2007:45 (1 November) • 1187
influenza and its complications should be viewed with more
urgency when they present with influenza-like symptoms, and
heath care systems must redouble their efforts to increase influenza vaccination rates in patients who are at high risk for
complications from influenza.
13.
14.
15.
Acknowledgments
We thank Deborah Naglieri-Prescod, for her help with formatting the
survey, and Cecelia Stafford, for help distributing the surveys.
Financial support. M.A.G.’s research is supported in part by a Health
Resources and Services Administration training grant in primary care
research.
Potential conflicts of interest. All authors: no conflicts.
16.
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