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Excess Mortality Due to Pneumonia or Influenza During Influenza Seasons Among Persons With Acquired Immunodeficiency Syndrome
Joseph C. Lin, MD;
Kristin L. Nichol, MD, MPH
Arch Intern Med. 2001;161:441-446.
ABSTRACT
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Background Anecdotal reports suggest that influenza-related morbidity may be high
among persons with acquired immunodeficiency syndrome (AIDS), but little information
is available concerning the population-level impact of influenza on mortality
in persons with AIDS.
Methods Using the Multiple Cause-of-Death data files, which contain information
on all deaths occurring in the United States each year, we calculated the
numbers of excess deaths and rates of excess death due to pneumonia or influenza
among persons with AIDS aged 13 years and older during the influenza seasons
1991-1992 through 1993-1994. For comparison, numbers of excess deaths and
excess death rates were also calculated for several other groups including
the general US population aged 13 years and older and the general US population
aged 65 years and older.
Results During the 1991-1992, 1992-1993, and 1993-1994 influenza seasons, there
were 261, 254, and 191 excess deaths due to pneumonia or influenza in persons
with AIDS and excess death rates of 19.74, 15.38, and 10.17 deaths per 10 000
persons, respectively, compared with a summer baseline period. For the same
seasons, we observed excess death rates of 1.40, 1.62, and 1.48 for the general
US population aged 13 years and older and 8.10, 9.28, and 8.54 for the general
US population aged 65 years and older. Thus, persons with AIDS had excess
death rates substantially higher than the general US population and similar
to, if not somewhat higher than, the general US population aged 65 years and
older, a group that is already targeted for annual vaccination. The findings
were similar when we compared the preinfluenza season with the influenza season.
Conclusions Persons with AIDS have significant excess mortality due to pneumonia
or influenza during influenza seasons and should be considered a high-risk
group that is targeted for the prevention of influenza.
INTRODUCTION
INFLUENZA CAUSES significant morbidity and mortality in various high-risk
groups, including persons with chronic cardiopulmonary disease, diabetes mellitus,
and advanced age and those residing in long-term care facilities. However,
there is limited information concerning the impact of influenza on morbidity
and mortality in persons with human immunodeficiency virus (HIV) infection
or acquired immunodeficiency syndrome (AIDS). Previous reports1, 2
suggested that influenza may severely compromise respiratory function and
cause prolonged duration of illness in patients with HIV infection, but, until
recently, information regarding the impact of influenza on this patient population
has been largely anecdotal.1, 2, 3, 4, 5
Because of potential for substantial benefit, the Advisory Committee on Immunization
Practices since 1987 has recommended that HIV-infected individuals receive
routine vaccination against influenza.6, 7
However, this policy has been somewhat controversial,8
and its implementation in clinical settings has not been widespread, as demonstrated
by low vaccination rates.9 Barriers to successful
vaccination efforts may include uncertainties regarding immunogenicity of
the vaccine in patients with HIV infection10, 11, 12, 13, 14, 15
and implications of possible transient increases in HIV viral load following
vaccination.13, 14, 15, 16, 17, 18, 19, 20, 21
Perhaps one of the largest influences on the poor rates of immunization has
been the persistent uncertainties concerning the magnitude of risk posed by
influenza among persons with AIDS or HIV infection. For this reason, we conducted
this study to assess influenza-related excess mortality in persons with AIDS.
METHODS
DATA SOURCE
The Multiple Cause-of-Death data files22, 23
are released annually by the National Center for Health Statistics and contain
detailed information for each of the approximately 2.2 million deaths occurring
every year in the 50 United States and the District of Columbia. Information
in the database is derived from US certificates of death and includes demographic
variables, such as age, race, sex, and geographic area, as well as cause-of-death
information. Coding of the underlying cause and contributing causes of death
for the data files is accomplished using rules established by the World Health
Organization that are applied to the information obtained from the death certificates.
This coding is increasingly automated, thus reducing or eliminating intercoder
variation. Use of information regarding not only the single underlying cause
of death, but also the contributing causes of death, can be particularly valuable
in achieving a more accurate portrayal of mortality. In some cases, deaths
are attributable to a number of concurrent disease processes for which a single
underlying cause of death insufficiently accounts for the interactions between
chronic or coexisting conditions and the immediate cause of death. Previous
publications22, 23, 24, 25, 26, 27
have described the details, potential uses, and limitations of the data files.
From the Multiple Cause-of-Death data file for 1991-1994, we calculated
the number of deaths due to pneumonia or influenza each month for adolescents
and adults (ie, persons aged 13 years and older) with AIDS. Deaths were classified
as being due to pneumonia or influenza (ICD-9-CM
[International Classification of Disease, Ninth Revision,
Clinical Modification]28 codes 480-487)
if pneumonia or influenza was listed either as an underlying or contributing
cause of death in the file. Persons were classified as having AIDS if the ICD-9-CM codes consistent with AIDS surveillance case definitions
also appeared in the data file for each death. For 1991-1992, we used the
1987 case definition of AIDS29 (ICD-9-CM code 042 [AIDS] or codes 043 [AIDS-related complex] to 044
[other HIV disease], with mention of 1 or more of the AIDS clinical indicator
diseases identified by the Centers for Disease Control and Prevention [CDC]).
For the 1992-1993 and 1993-1994 influenza seasons and corresponding baseline
periods, the 1993 expanded surveillance case definition of AIDS was used.
(For the 1993 case definition, the CDC added pulmonary tuberculosis, recurrent
pneumonia, and invasive cervical cancer to the list of indicator clinical
conditions.30)
For comparison, we tabulated the number of deaths due to pneumonia or
influenza (ICD-9-CM codes 480-497) by month for all
adults and adolescents in the general US population. We also tabulated these
data for 2 additional comparison groups: the general US population 65 years
and older (a high-risk group currently targeted for annual influenza vaccination)
and the general US population aged 25 to 54 years (more than 90% of AIDS deaths
occur in this age group).
INFLUENZA SEASONS
Influenza seasons were defined using national influenza surveillance
data collected by the World Health Organization collaborating laboratories
in the United States.31, 32, 33
For each month from October to May for the years included in this study, we
identified all months for which the total number of influenza isolates was
5% or more of the season's total influenza isolates. All these months constituted
the influenza period for each study year.
BASELINE PERIODS
We used 2 baseline periods for establishing baseline pneumonia or influenza
death rates. One, the preinfluenza baseline period,
was defined as the 2 months immediately preceding the influenza season for
each study season. The other, the summer baseline period, was defined as the June through September immediately preceding each
influenza season. Because national influenza surveillance spans October through
May, data for the number of influenza isolates were not available for the
summer months. However, influenza activity is assumed to be minimal during
the summer.
CALCULATION OF EXCESS DEATHS AND DEATH RATES
We calculated excess deaths attributable to pneumonia or influenza during
each influenza season by taking the difference between those deaths occurring
each month in the influenza season and the monthly average of the preceding
baseline period. The total excess deaths for each influenza period were calculated
as the sum of the excess deaths for each month during the influenza period.
We calculated the excess deaths rates per 10 000 by dividing the total
excess deaths for each influenza season by the estimated number of living
persons according to population estimates derived from the 1990 US census34 for the general population and from estimates from
the CDC35 for persons with AIDS aged 13 years
or older in the 50 United States and the District of Columbia. We assumed
that the distribution of deaths followed a binomial distribution, and we calculated
95% confidence intervals for the death rates, as recommended by the National
Center for Health Statistics.23
RESULTS
The characteristics of adults and adolescents who died of AIDS during
the study period are shown in Table 1.
Of the persons who died, 85% to 89% were male and more than 90% were between
25 and 54 years of age. In about 15% of the persons, pneumonia or influenza
was listed as the underlying or one of the contributing causes of death.
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Table 1. Deaths in Persons With AIDS Aged 13 Years and Older*
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The influenza seasons extended from November through February for the
1991-1992 season, December through April for the 1992-1993 season, and December
through February for the 1993-1994 season. Deaths due to pneumonia or influenza
among adults and adolescents with AIDS followed a seasonal pattern, with peaks
generally occurring during the months of December and January. This pattern
paralleled the seasonal variability seen for deaths due to pneumonia or influenza
among adults and adolescents in the general US population and also followed
the seasonal pattern for positive influenza isolates in the United States
(data not shown).
During the 1991-1992, 1992-1993, and 1993-1994 influenza seasons, there
were 261, 254, and 191 excess deaths attributable to pneumonia or influenza
in persons with AIDS, respectively, compared with the summer baseline period
(Table 2). These excess deaths
corresponded to excess death rates of 19.74, 15.38, and 10.17 deaths per 10 000
adults and adolescents with AIDS. These excess death rates were 6.9 to 14.1
times higher than the excess death rates due to pneumonia or influenza observed
among adults and adolescents in the general US population and were even somewhat
higher than, although of similar magnitude to, those seen for persons 65 years
and older in the general US population (Table 2).
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Table 2. Excess Deaths and Death Rates Due to Pneumonia or Influenza
During Influenza Seasons*
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During the same influenza seasons, there were 166, 242, and 176 excess
deaths attributable to pneumonia or influenza in persons with AIDS, compared
with the preinfluenza baseline periods (Table 2, Figure 1). These
excess deaths corresponded to excess death rates of 12.56, 14.65, and 9.37
deaths per 10 000 adults and adolescents with AIDS. These excess death
rates were 8.5 to 10.3 times higher than the excess death rates due to pneumonia
or influenza observed in adults and adolescents in the general US population.
Similar to the comparison to the summer baseline period, these rates were
even somewhat higher than those seen for the general US population 65 years
and older (Table 2).
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Excess death rates due to pneumonia or influenza during influenza
seasons compared with preinfluenza baseline periods. Shown are the excess
death rates per 10 000 for the 1991-1992, 1992-1993, and 1993-1994 influenza
seasons for the general US population 13 years and older and 65 years and
older and for persons with acquired immunodeficiency syndrome (AIDS) aged
13 years and older.
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The general US population aged 25 to 54 years was selected as an additional
comparison group as more than 90% of AIDS deaths in our study occurred in
this age group. We found that the excess death rate from pneumonia or influenza
was 81 to 155 times higher among adults and adolescents with AIDS than for
the general US population aged 25 to 54 years compared with the summer baseline
period. Similarly, when using the preinfluenza period as the baseline, we
found that the excess death rate for adults and adolescents with AIDS was
106 to 161 times higher than that of the general US population aged 25 to
54 years (Table 2).
COMMENT
We have shown that adults and adolescents with AIDS have substantial
excess mortality due to pneumonia or influenza during influenza seasons. The
excess death rates from influenza or pneumonia per 10 000 persons are
comparable to if not greater than those for the general US population 65 years
and older, a high-risk group that is already targeted for routine annual influenza
vaccination.
Previous studies have attempted to define the impact of influenza or
influenza-related illnesses on morbidity and mortality in persons with HIV
infection. In one case report2 of a child with
HIV infection and one case series1 describing
6 HIV-infected patients from whom influenza virus was isolated, the authors
suggested that patients with HIV infection may experience more severe respiratory
complications and prolonged duration of illness. In one study36
that examined hospital use for patients with AIDS in the state of New York,
the authors noted that the length of hospital stay was 2.8, 1.1, and 2.4 days
longer in January (typically when influenza-related morbidity and mortality
peaks nationwide) compared with June during 3 consecutive years, but they
made no comment concerning the frequency of hospitalization, reasons for admission,
or rates of death. Recently, Neuzil et al37
demonstrated increased hospitalization rates for cardiopulmonary causes during
influenza season in women with HIV infection. This retrospective population-based
cohort study of women enrolled in the Medicaid program for the state of Tennessee
demonstrated influenza-related excess morbidity in patients with HIV infection.
Of all women with high-risk chronic conditions, the risk attributable to influenza
was shown to be highest among those with HIV infection. This study estimated
the hospitalization rate for influenza-related illnesses to be 300 per 10 000
women with HIV infection. According to their estimates, women with HIV infection
were 50 to 75 times more likely to be hospitalized for influenza-related morbidity
compared with women aged 15 to 64 years who were without high-risk chronic
conditions. Our study augments these findings by defining influenza-associated
excess mortality for the entire US adolescent and adult population with AIDS.
Other investigators have used several different types of baseline periods
to estimate excess outcome rates associated with influenza. These periods
have included summer months,37, 38, 39, 40, 41
peri-influenza periods,37 and nonepidemic influenza
seasons with low rates of influenza activity as defined by relatively flat
curves for mortality due to pneumonia and influenza.42, 43
Because the choice of baseline period can influence the calculated rates of
excess events, we adapted methods from several previous studies and used 2
different baseline periods in our study. As expected, the use of 2 different
baseline periods resulted in somewhat differing point estimates for excess
mortality rates but identical conclusions regarding the substantially increased
risk among persons with AIDS compared with the general US population.
We used both underlying and contributing causes of death to estimate
the total number of deaths due to pneumonia or influenza. According to Barker
and Mullooly,44 up to one half or more of pneumonia-associated
deaths may be attributed to underlying chronic medical conditions on death
certificates. Consistent with these findings, our estimated number of excess
death due to pneumonia or influenza based on both underlying and contributing
causes of death are approximately twice those obtained if only deaths with
pneumonia or influenza as the underlying cause were included (data not shown).
The resulting excess mortality rates of 1.1 to 1.6 deaths per 10 000
that we calculated for adults and adolescents in the general US population
are similar to those reported by other investigators. For example, Kavet,45 in assessing the impact of 3 influenza epidemics
during the 1960s, estimated mortality rates of 1.0 to 2.5 per 10 000
persons in the general population. He estimated that in 21% to 37% of these
deaths the underlying cause of death was pneumonia or influenza. Barker and
Mullooly46 reported 1.2 excess deaths due to
pneumonia or influenza per 10 000 members of the Kaiser Permanente health
maintenance organization in Portland, Ore, for the 1968-1969 and 1972-1973
influenza epidemics. During the 1977-1978 influenza epidemic in Houston, Tex,
Glezen47 reported a mortality rate due to acute
respiratory disease among persons aged 20 years and older of 2.26 per 10 000.
The Multiple Cause-of-Death data files are derived from death certificates.
The use of these and other files based on death certificate data is standard
for tracking national mortality trends,48 including
influenza-associated excess mortality.49, 50
It is believed that more than 99% of deaths occurring in the United States
are registered.23 However, several limitations
of death certificate data deserve comment and necessitate interpreting our
study results with some caution. Previous studies51, 52
have suggested that 9% to 12% of death certificates fail to mention AIDS as
the underlying or contributing cause of death among persons with known AIDS.
Therefore, it is possible that we underestimated the number of deaths occurring
among persons with AIDS. This possible underestimation may explain why our
estimates of the total number of deaths due to AIDS were on average 11.5%
lower than those estimated by the CDC.35 Such
an underestimation of deaths would most likely have resulted in an underestimation
of the excess death rates due to pneumonia and influenza that we reported.
In addition, death certificates may not list pneumonia or influenza even when
they were a cause of death. In one study,44
16% of death certificates for persons who died of pneumonia or influenza did
not mention pneumonia or influenza. If it occurred, underreporting pneumonia
and influenza on death certificates during the years of this study would probably
also have resulted in underestimation of excess death rates. The presence
of an AIDS diagnosis, especially among persons with pulmonary opportunistic
infections, may also have contributed to a detection bias leading to more
frequent listing of pulmonary infections, such as bacterial pneumonias, on
the death certificate than might be seen in the general population. However,
if present, such a bias was probably most relevant in establishing the baseline
rate of death due to pneumonia or influenza. We found no evidence of seasonal
variability in the listing of pulmonary opportunistic infections as underlying
or contributing causes of death among persons with AIDS (data not shown).
Thus, our use of excess death rates above the baseline rate likely minimized
the impact of any detection bias.
Another limitation of the present study is that it encompasses years
that predate the advent of highly active antiretroviral therapy, which was
not widely used to treat persons with HIV infection in the United States until
1996. Since the introduction of highly active antiretroviral therapy, morbidity
and mortality from HIV disease and various associated opportunistic infections
have decreased significantly.53 Therefore,
it is unclear whether the magnitude of risk that we identified in this study
will be present in future years.
Our findings suggest that the magnitude of influenza-related excess
mortality in persons with AIDS is comparable to, if not greater than, that
seen among the general US population aged 65 years and older, a high-risk
group targeted for annual influenza vaccination. Although various reports13, 14, 15, 16, 17, 18, 19, 20, 21
have provided conflicting results of whether influenza vaccination transiently
increases HIV viral load after immunization, the clinical relevance of this
short-lived phenomenon is unclear. To our knowledge, no detriment in clinical
outcome has ever been shown to be associated with this transient viremia.
Questions also persist concerning the efficacy of vaccination in a patient
population characterized by defects in cellular and humoral immunity. However,
until recently assessments of vaccine efficacy10, 11, 12, 13, 14, 15
have been based on laboratory measurements of antibody response, as opposed
to clinical measurements of the protection that vaccination provides. One
double-blind, placebo-controlled trial54 in
patients with AIDS and HIV infection showed that influenza vaccination was
associated with a 93% efficacy against laboratory-confirmed infection and
a 100% efficacy against symptomatic illness. Even in the subgroups of participants
with CD4 counts less than 200/µL, 20% of those who received the vaccine
vs 50% of those who received placebo experienced respiratory symptoms.
CONCLUSIONS
In this study, adults and adolescents with AIDS had substantial excess
mortality due to pneumonia or influenza during influenza seasons. The mortality
risk attributable to influenza in this population was comparable to that of
the general US population 65 years or older. In the absence of any clear evidence
to suggest that influenza vaccination is clinically harmful to persons with
HIV infection and AIDS and in light of new information demonstrating protective
efficacy provided by vaccination, our findings support recommendations for
annual vaccination of persons with AIDS.
AUTHOR INFORMATION
Accepted for publication August 24, 2000.
From the Medicine Service and Center for Chronic Disease Outcomes Research,
Veterans Affairs Medical Center and the Department of Medicine, University
of Minnesota Medical School, Minneapolis.
Corresponding author and reprints: Kristin L. Nichol, MD, MPH, Medicine
Service, Veterans Affairs Medical Center (111), 1 Veterans Dr, Minneapolis,
MN 55417 (e-mail: nicho014{at}tc.umn.edu).
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