Special Article
The Efficacy and Cost Effectiveness of Vaccination against Influenza among Elderly Persons Living in the Community
N Engl J Med 1994; 331:778-784September 22, 1994
- Abstract
Background
Despite recommendations for annual vaccination against influenza, more than half of elderly Americans do not receive this vaccine. In a serial cohort study, we assessed the efficacy and cost effectiveness of influenza vaccine administered to older persons living in the community.
Methods
Using administrative data bases, we studied men and women over 64 years of age who were enrolled in a large health maintenance organization in the Minneapolis-St. Paul area. We examined the rate of vaccination and the occurrence of influenza and its complications in each of three seasons: 1990-1991, 1991-1992, and 1992-1993. Outcomes were adjusted for age, sex, diagnoses indicating a high risk, use of medications, and previous use of health care services.
Results
Each cohort included more than 25,000 persons 65 years of age or older. Immunization rates ranged from 45 percent to 58 percent. Although the vaccine recipients had more coexisting illnesses at base line than those who did not receive the vaccine, during each influenza season vaccination was associated with a reduction in the rate of hospitalization for pneumonia and influenza (by 48 to 57 percent, P ≤ 0.002) and for all acute and chronic respiratory conditions (by 27 to 39 percent, P ≤ 0.01). Vaccination was also associated with a 37 percent reduction (P = 0.04) in the rate of hospitalization for congestive heart failure during the 1991-1992 season, when influenza A was epidemic. The costs of hospitalization for all types of illness studied were lower in the vaccinated group during 1991-1992 (range of reduction, 47 to 66 percent; P<0.005) and for acute and chronic respiratory conditions and congestive heart failure in 1990-1991 (reductions of 37 percent and 43 percent, respectively; P ≤ 0.05). Direct savings per year averaged $117 per person vaccinated (range, $21 to $235), with cumulative savings of nearly $5 million. Vaccination was also associated with reductions of 39 to 54 percent in mortality from all causes during the three influenza seasons (P<0.001).
Conclusions
For elderly citizens living in the community, vaccination against influenza is associated with reductions in the rate of hospitalization and in deaths from influenza and its complications, as compared with the rates in unvaccinated elderly persons, and vaccination produces direct dollar savings. .
Media in This Article
Figure 1
Mean Number of Hospitalizations per 1000 Elderly Enrollees for Pneumonia and Influenza (Panel A), All Acute and Chronic Respiratory Conditions (Panel B), and Congestive Heart Failure (Panel C).Table 1
Base-Line Characteristics of the Study Subjects, According to Study Period and Vaccination Status.Article Activity
- Article
Influenza and its complications account for 10,000 to 40,000 excess deaths annually in the United States, of which more than 80 percent occur among the elderly1. The Advisory Committee on Immunizations Practices of the Public Health Service and others recommend that all persons 65 years of age or older receive the influenza vaccine annually2-5. Despite these recommendations, 60 percent or more of the elderly and other persons at high risk do not receive the influenza vaccine6,7. Thus, many vaccine-preventable deaths and many more vaccine-preventable hospitalizations continue to occur every year. The annual economic costs associated with influenza epidemics exceed $12 billion8.
Among the barriers to the successful delivery of vaccine to the elderly is uncertainty about the efficacy and cost effectiveness of immunization. Clinical trials of monovalent vaccines during the 1960s demonstrated that influenza vaccine reduced the incidence of influenza-like upper respiratory illnesses among residents of a large California retirement community9,10 and among elderly psychiatric inpatients11. Vaccination was also associated with a lower rate of hospitalization9. More recent observational studies have shown a reduction in influenza-associated complications and deaths among vaccinated nursing home residents12-16. Others have assessed the effectiveness of the vaccine among noninstitutionalized elderly people. Some have confirmed its efficacy, particularly during epidemic years,17-21 but others have not22,23. None of these studies evaluated the full range of complications associated with influenza,24 nor did any include the actual inpatient charges for the study subjects in calculating the cost effectiveness of vaccination. We designed a serial cohort study to assess comprehensively the efficacy and cost effectiveness of the influenza vaccine among elderly people living in the community. We evaluated the effect of vaccination on the rate of hospitalization for influenza and for complications of influenza, including pneumonia, all acute and chronic respiratory conditions, and congestive heart failure; its effect on the costs of hospitalization; and its effect on mortality rates.
Methods
Group Health, Inc., is a staff-model health maintenance organization with more than 300,000 enrollees in the Minneapolis-St. Paul area. It has 23 clinics and more than 370 salaried physicians. In 1989 Group Health initiated as a pilot program a modified version of the Minneapolis Veterans Affairs Flu Shot Program in two of its clinics25. In 1990 the program was expanded to all staff clinics. This highly successful program consisted of a standing order for nurses to offer and administer influenza vaccine to high-risk patients, walk-in influenza-vaccine clinics, use of standardized documentation forms, and mailings to patients. Since this program was begun, Group Health has been able to vaccinate more than 50 percent of its elderly enrollees against influenza.
Study Subjects
All persons 65 years of age or older who were continuously enrolled in Group Health through the vaccination season (October through December, with most doses administered by mid-November) and the following influenza season were were included in cohorts for each of three study periods: 1990-1991, 1991-1992, and 1992-1993. There were more than 25,000 elderly enrollees in each cohort. Persons who changed health plans or who died before the onset of the influenza season were excluded from the cohorts.
Influenza Seasons
The influenza seasons (the outcome periods for each cohort) were defined on the basis of influenza-surveillance data from the Minnesota Department of Health26-28. This surveillance system relies on passive reporting from schools and nursing homes, information included in the health department's standardized reportable-disease forms (disease report cards), and specimens sent to the Division of Public Health laboratories. The information is used to estimate the level of influenza activity and the specific type or types of influenza virus circulating in the state during a given year. In this study, the onset of the influenza season was defined from the date when influenza isolates were first recovered from communities in the state. For each year the influenza season was considered to extend through March.
Data Collection
Study data were obtained from Group Health's administrative data bases, which include demographic characteristics and details of the use of outpatient, inpatient, and pharmacy services by all enrollees. Base-line information was collected for the subjects in each cohort as of October 1; it included age, sex, and the number of visits to a physician during the previous year. Other information included the number of hospitalizations during the previous year (October through September), whether the patient had received pneumococcal vaccine during the previous year (code 907.32 in Current Procedural Terminology, 4th revision [CPT-4]), and whether he or she had been given a diagnosis of pneumonia in the previous year (codes 480 through 487 in the International Classification of Diseases, Ninth Revision, Clinical Modification [ICD-9-CM]). Information was also collected on whether the subject had been given the following inpatient or outpatient diagnoses for the previous year: coronary heart disease (ICD-9-CM codes 393 through 398, 410 through 414, 425, 428, and 429), chronic lung disease (ICD-9-CM codes 491 through 496 and 500 through 518), diabetes mellitus (ICD-9-CM code 250), chronic renal disease (ICD-9-CM codes 581, 582, and 585, plus the CPT-4 code for dialysis, 39.95), vasculitis or rheumatologic disease (ICD-9-CM codes 446, 710, and 714), dementia or stroke (ICD-9-CM codes 290 through 294, 331, 340, 341, 348, and 438), nonhematologic cancer (ICD-9-CM codes 140 through 199), hematologic cancer (ICD-9-CM codes 200 through 208), or the acquired immunodeficiency syndrome (ICD-9-CM codes 042 through 044). These diagnoses were selected to identify persons who had medical conditions that might increase their risk for influenza-related complications2. Influenza-vaccination status was also ascertained for each season (CPT-4 code 907.24).
Given the potential for incomplete coding of important base-line medical information, we also collected data on prescription refills during the three months preceding the immunization season and categorized them according to the therapeutic classification of the American Hospital Formulary Service. The classes of medication were chosen to reflect high-risk diagnostic categories: cardiovascular agents (codes 240000, 240400, 240800, and 241200); chemotherapeutic agents (code 100000); hormonal agents for treating diabetes (codes 682000, 682008, 682020, and 682092); immunologic agents, including steroids and agents to induce remission of rheumatologic diseases (codes 82000, 600000, 640000, and 680400); and agents for treating diseases of the respiratory tract (codes 121200 and 861600).
The outcomes we studied included hospitalizations for pneumonia and influenza (ICD-9-CM codes 480 through 487), for all acute and chronic respiratory conditions (ICD-9-CM codes 460, 462, 465, 466, 480 through 487, 490 through 496, and 500 through 518), and for congestive heart failure (ICD-9-CM code 428). These diagnoses were chosen for consistency with the previously identified categories of complications associated with influenza24. The outcome variables also included the costs of hospitalization for pneumonia and influenza, all acute and chronic respiratory conditions, and congestive heart failure and death from all causes. Because Group Health is billed for each inpatient episode, data on costs reflect actual charges for hospitalized enrollees.
Statistical Analysis
We estimated that a cohort of 25,000 people would give us an 85 percent chance of detecting a reduction of 35 percent in outcome events among influenza-vaccine recipients (this calculation was made with use of Power, Epicenter Software, Pasadena, Calif.). For these calculations, we assumed a vaccination rate of 55 percent, an event rate of 1 percent among unvaccinated subjects, and a two-sided alpha level of 0.05.
Student's t-tests and chi-square tests were used to conduct bivariate analyses of continuous and categorical data for each cohort. Analysis of covariance and logistic regression (with SPSS for Windows, version 6.0, SPSS, Chicago) were used to conduct multivariate analyses of the study outcomes with control for covariates and potential confounders. Cost savings associated with vaccination were calculated from the institution's perspective as direct savings during each influenza season. The costs of hospitalization for all acute and chronic respiratory conditions and for congestive heart failure were combined, and savings were calculated according to the following formulas: mean cost savings = (mean costs of hospitalization for unvaccinated subjects) - (mean costs of hospitalization for vaccine recipients) - (mean costs of influenza-vaccination program), and total cost savings = (mean cost savings) × (number of people vaccinated). The reduction in mortality among vaccine recipients was calculated from the results of the logistic regression; the adjusted odds ratio was used as an approximation of the relative risk, since outcome events were rare. The calculation was performed as follows: reduction in mortality = (1 - odds ratio) × 100 percent.
Results
There were 25,532 elderly persons in the study cohort in 1990-1991; 26,369 in 1991-1992; and 26,626 in 1992-1993. The influenza-vaccination rates were 45 percent, 58 percent, and 55 percent, respectively, in these three study periods. The base-line characteristics of the subjects in each cohort are shown in Table 1Table 1
Base-Line Characteristics of the Study Subjects, According to Study Period and Vaccination Status.. Vaccine recipients were more likely than nonrecipients to have most of the existing conditions at base line, including heart and lung disease, to have higher rates of use of health care resources in the previous year, such as visits to physicians and prescription refills, and to have a history of pneumonia. Nonrecipients of the vaccine, on the other hand, were slightly older and more likely to have been given a diagnosis of dementia or stroke. These trends were consistent among the three study cohorts. In 1991-1992, vaccine recipients were also more likely to have been hospitalized during the past year; for the other two study periods, the rates were similar in the two groups.The influenza seasons and numbers of outcome events are summarized in Table 2Table 2
Characteristics of Influenza Seasons and Numbers of Outcome Events for Each Influenza Season.. The three influenza seasons included epidemic and nonepidemic years, with varying degrees of matching between circulating virus strains and vaccine antigens. In the second season (1991-1992), influenza A was epidemic, and there was an excellent match between circulating virus strains and vaccine antigens; the first season (1990-1991) was a nonepidemic year for influenza B, with a very good match between circulating virus strains and vaccine antigens; and the third season (1992-1993) was a mixed year with early, nonepidemic influenza B (there was an excellent match between circulating strains and vaccine antigens) and late epidemic influenza A (there was a poor match between circulating strains and vaccine antigens). The total numbers of outcome events were highest during the second influenza season of the study, which was the most severe season, characterized by epidemic influenza A.The final multivariate models included influenza-vaccination status, age, sex, number of visits to a physician during the previous year, number of hospitalizations in the previous year, and number of prescription refills for each of the five therapeutic classes of medication. Also included were variables indicating whether the subject had been given a diagnosis of heart disease, lung disease, vasculitis or rheumatologic disease, or dementia or stroke as an outpatient; whether he or she had been given a diagnosis of heart disease or lung disease as an inpatient; and whether he or she had been given a diagnosis of pneumonia. A diagnosis of diabetes or neoplastic disease did not contribute significantly to the models after we included the number of refills for the corresponding therapeutic classes of medication; these variables were therefore not included in the final models. Similarly, other variables, such as pneumococcal-vaccination status, were excluded because they did not contribute significantly to the models (P>0.10 for all comparisons).
The results of the analysis of covariance to compare the mean number of hospitalizations for pneumonia and influenza, all acute and chronic respiratory conditions, and congestive heart failure in vaccine recipients and nonrecipients are shown in Table 3Table 3
Hospitalizations per 1000 Elderly Enrollees for Pneumonia and Influenza, All Acute and Chronic Respiratory Conditions, and Congestive Heart Failure among Vaccine Recipients and Nonrecipients, According to Influenza Season. and Figure 1Figure 1Mean Number of Hospitalizations per 1000 Elderly Enrollees for Pneumonia and Influenza (Panel A), All Acute and Chronic Respiratory Conditions (Panel B), and Congestive Heart Failure (Panel C).. Vaccination against influenza was associated with significantly fewer hospitalizations for pneumonia and influenza (range of reduction, 48 to 57 percent; P ≤ 0.002 for all comparisons) and for acute and chronic respiratory conditions (range of reduction, 27 to 39 percent; P ≤ 0.01 for all comparisons) in each of the three seasons. Immunization was also associated with fewer hospitalizations for congestive heart failure during the epidemic 1991-1992 season (a 37 percent reduction; P = 0.04).The results of the analysis of covariance used to evaluate the mean costs of hospitalization for pneumonia and influenza, all acute and chronic respiratory conditions, and congestive heart failure are shown in Table 4Table 4
Mean Costs of Hospitalization for Pneumonia and Influenza, All Acute and Chronic Respiratory Conditions, and Congestive Heart Failure among Vaccine Recipients and Nonrecipients, According to Influenza Season.. The costs of hospitalizations for pneumonia and influenza, all acute and chronic respiratory conditions, and congestive heart failure were significantly lower among vaccine recipients than among unvaccinated subjects in 1991-1992 (reductions of 52 percent, 47 percent, and 66 percent, respectively; P<0.005 for all comparisons). Expenses for hospitalizations for all acute and chronic respiratory conditions and congestive heart failure were also lower among vaccine recipients in 1990-1991 (reductions, 37 percent and 43 percent, respectively; P ≤ 0.05 for both comparisons). Trends consistent with these findings, although not statistically significant, were seen in the costs of hospitalization for pneumonia and influenza in 1990-1991 and 1992-1993 and for all acute and chronic respiratory conditions in 1992-1993 as well.The cost of Group Health's influenza-vaccination program averaged $4 per person vaccinated (unpublished data). This included all costs for the vaccine, supplies, advertising and mailings, personnel to administer the vaccine, and miscellaneous administrative expenses. After subtracting the mean costs of the program, the combined direct savings in the costs of hospitalizations for all acute and chronic respiratory conditions and for congestive heart failure in 1990-1991 and 1991-1992 (the two years for which savings were statistically significant) were $114 and $235 per person vaccinated, respectively. For 1992-1993, estimated cost savings was $21 per person vaccinated, but the difference was not significant (P = 0.56). The total cumulative direct savings in hospitalizations for all acute and chronic respiratory conditions and for congestive heart failure among vaccine recipients over the three years was nearly $5 million.
In the three influenza seasons, vaccination was associated with significant decreases of 39 to 54 percent in mortality from all causes (P<0.001 for all comparisons). The adjusted odds ratios for the risk of dying among vaccine recipients as compared with nonrecipients were 0.49 (95 percent confidence interval, 0.35 to 0.70) in 1990-1991, 0.46 (95 percent confidence interval, 0.35 to 0.61) in 1991-1992, and 0.61 (95 percent confidence interval, 0.47 to 0.81) in 1992-1993. The unadjusted odds ratios were 0.57, 0.56, and 0.64, respectively.
Discussion
In this serial cohort study we found that among elderly people living in the community, vaccination against influenza was associated with less frequent hospitalizations for complications of influenza, with fewer deaths during the influenza season, and with direct savings in health care costs. These findings were consistent over three consecutive seasons among cohorts of more than 25,000 elderly men and women.
Assessments of the effect of influenza on populations have often been limited to evaluations of excess hospitalizations for pneumonia and influenza and deaths during influenza epidemics (as compared with the base-line numbers in a nonepidemic year). The impact of influenza on the elderly may be much greater than has generally been acknowledged, however. For example, not only are rates of hospitalization for pneumonia and influenza higher during the influenza season, but so also are rates of hospitalization for all acute and chronic respiratory conditions and even for congestive heart failure17,24,30-33. These effects are evident during both epidemic and nonepidemic years24. Thus, it has been suggested that studies of the effects of influenza on the elderly should evaluate all these outcomes in both epidemic and nonepidemic years24.
Our study was designed specifically to take these issues into account. We assessed the effectiveness of influenza vaccine with respect to a broad range of influenza-associated complications, including pneumonia and influenza, acute and chronic respiratory conditions, and congestive heart failure in both epidemic and nonepidemic years. We were thus able to assess the effectiveness of influenza vaccine in reducing the number of hospitalizations and health care costs for each of these disease categories. We found that the vaccine was beneficial in both epidemic and nonepidemic years; however, its efficacy was greatest during the 1991-1992 season, when influenza A was epidemic and when there was an excellent match between the vaccine and circulating viral strains.
Our findings corroborate the results in three recent case-control studies that demonstrated the efficacy of influenza vaccine among noninstitutionalized elderly people; these studies used more limited outcome measures than did our study and assessed fewer base-line risk characteristics among patients19-21. All three studies showed reductions of 30 to 45 percent in the rate of hospitalization for pneumonia and influenza during selected epidemic years. The investigators in one study also measured hospitalizations for all acute and chronic respiratory conditions and found reductions of 15 to 34 percent among vaccine recipients; they also found reductions of 27 to 30 percent in mortality from all causes19. We observed decreases of 48 to 57 percent in the rate of hospitalization for pneumonia and influenza, decreases of 27 to 39 percent in the rate of hospitalization for all acute and chronic respiratory conditions, and decreases of 39 to 54 percent in mortality from all causes. Influenza and its complications are major health problems among elderly people. Undoubtedly, influenza often goes unrecognized as a precipitating factor in the deaths of many elderly people.
It has been suggested that vaccinating elderly persons against influenza is more cost effective than many other preventive and therapeutic interventions, such as the pneumococcal vaccine, screening for cervical cancer, treatment of lipid disorders, and coronary-artery bypass surgery34-36. In some situations, vaccination against influenza has been shown to produce cost savings -- or at least potential savings -- that depend on the level of efficacy of the vaccine, vaccination coverage rates, the population's risk profile, the cost of the vaccine, and whether future medical costs for additional years of life gained were included in the calculations21,34-40. The direct cost savings attributable to vaccination in our study totaled almost $5 million and averaged $117 for each of the 41,418 people immunized during the three years we studied. This figure is higher than other estimates of savings produced by the influenza vaccine. Previous studies probably underestimated cost savings by failing to include reductions in the costs of hospitalization for congestive heart failure and acute and chronic respiratory conditions other than pneumonia and influenza or by assuming that the vaccine had benefits only during epidemic years. In our study we may also have underestimated cost savings attributable to vaccination against influenza, since we did not include estimates of savings due to the decreased use of outpatient health care resources.
The strengths of our study include the use of the cohort design, the strongest of all noninterventional or observational study designs,41 and the large samples with high proportions of vaccine recipients. The inclusion of data from three consecutive influenza seasons also reduced the likelihood of spurious conclusions.
A limitation of observational studies, including those that use administrative data sets, is the difficulty of performing adequate risk adjustment in multivariate analyses42. Without the randomization of study subjects that is usually performed in a clinical trial, the chance is greater that there will be important unmeasured differences between the study groups that might influence the study outcome. In our study, we collected extensive information on base-line risk factors for hospitalization and death from influenza-associated complications so as to allow adequate adjustment for risk factors including age, a history of heart or lung disease, previous hospitalization,1,17,43 and other conditions that are indications for vaccination, such as diabetes, neoplastic disease, and immunosuppression2. We included information from several sources, including inpatient, outpatient, and medication data, in the patients' risk profile. We also collected information on the intensity of the patients' previous use of health care resources. Because these variables were included in our multivariate analyses, we were able to assess the independent contribution of vaccination against influenza to the outcome events.
Recently Medicare added vaccination against influenza to its list of reimbursable services for the 31 million elderly people in this country. With clear and striking evidence of the effectiveness of the vaccine in reducing hospitalizations and deaths and in producing direct cost savings, providers and patients alike should take steps to ensure that people at high risk receive the influenza vaccine each year. Few, if any, other preventive interventions for adults match these benefits.
Presented in part at the national meeting of the Society of General Internal Medicine, Washington, D.C., April 28, 1994.
Supported in part by a grant from Connaught Laboratories.
We are indebted to John Krystosek for obtaining the study data and to Andrew Nelson for his support and encouragement of this project.
Source Information
From the Veterans Affairs Medical Center and the University of Minnesota Medical School (K.L.N.), the Hennepin County Medical Center (K.L.M.), and Group Health, Inc. (J.W., T.V.S.) -- all in Minneapolis.
Address reprint requests to Dr. Nichol at the Section of General Internal Medicine, Veterans Affairs Medical Center, 1 Veterans Dr., Minneapolis, MN 55417.
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