Background Despite recommendations for annual vaccination againstinfluenza, more than half of elderly Americans do not receivethis vaccine. In a serial cohort study, we assessed the efficacyand cost effectiveness of influenza vaccine administered toolder persons living in the community.
Methods Using administrative data bases, we studied men andwomen over 64 years of age who were enrolled in a large healthmaintenance organization in the Minneapolis-St. Paul area. Weexamined the rate of vaccination and the occurrence of influenzaand its complications in each of three seasons: 1990-1991, 1991-1992,and 1992-1993. Outcomes were adjusted for age, sex, diagnosesindicating a high risk, use of medications, and previous useof health care services.
Results Each cohort included more than 25,000 persons 65 yearsof age or older. Immunization rates ranged from 45 percent to58 percent. Although the vaccine recipients had more coexistingillnesses at base line than those who did not receive the vaccine,during each influenza season vaccination was associated witha reduction in the rate of hospitalization for pneumonia andinfluenza (by 48 to 57 percent, P 0.002) and for all acuteand 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 heartfailure during the 1991-1992 season, when influenza A was epidemic.The costs of hospitalization for all types of illness studiedwere lower in the vaccinated group during 1991-1992 (range ofreduction, 47 to 66 percent; P<0.005) and for acute and chronicrespiratory 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 54percent in mortality from all causes during the three influenzaseasons (P<0.001).
Conclusions For elderly citizens living in the community, vaccinationagainst influenza is associated with reductions in the rateof hospitalization and in deaths from influenza and its complications,as compared with the rates in unvaccinated elderly persons,and vaccination produces direct dollar savings. .
Influenza and its complications account for 10,000 to 40,000excess deaths annually in the United States, of which more than80 percent occur among the elderly1. The Advisory Committeeon Immunizations Practices of the Public Health Service andothers recommend that all persons 65 years of age or older receivethe influenza vaccine annually2,3,4,5. Despite these recommendations,60 percent or more of the elderly and other persons at highrisk do not receive the influenza vaccine6,7. Thus, many vaccine-preventabledeaths and many more vaccine-preventable hospitalizations continueto occur every year. The annual economic costs associated withinfluenza epidemics exceed $12 billion8.
Among the barriers to the successful delivery of vaccine tothe elderly is uncertainty about the efficacy and cost effectivenessof immunization. Clinical trials of monovalent vaccines duringthe 1960s demonstrated that influenza vaccine reduced the incidenceof influenza-like upper respiratory illnesses among residentsof a large California retirement community9,10 and among elderlypsychiatric inpatients11. Vaccination was also associated witha lower rate of hospitalization9. More recent observationalstudies have shown a reduction in influenza-associated complicationsand deaths among vaccinated nursing home residents12,13,14,15,16.Others have assessed the effectiveness of the vaccine amongnoninstitutionalized elderly people. Some have confirmed itsefficacy, particularly during epidemic years,17,18,19,20,21but others have not22,23. None of these studies evaluated thefull range of complications associated with influenza,24 nordid any include the actual inpatient charges for the study subjectsin calculating the cost effectiveness of vaccination. We designeda serial cohort study to assess comprehensively the efficacyand cost effectiveness of the influenza vaccine among elderlypeople living in the community. We evaluated the effect of vaccinationon the rate of hospitalization for influenza and for complicationsof influenza, including pneumonia, all acute and chronic respiratoryconditions, and congestive heart failure; its effect on thecosts of hospitalization; and its effect on mortality rates.
Methods
Group Health, Inc., is a staff-model health maintenance organizationwith more than 300,000 enrollees in the Minneapolis-St. Paularea. It has 23 clinics and more than 370 salaried physicians.In 1989 Group Health initiated as a pilot program a modifiedversion of the Minneapolis Veterans Affairs Flu Shot Programin two of its clinics25. In 1990 the program was expanded toall staff clinics. This highly successful program consistedof a standing order for nurses to offer and administer influenzavaccine 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 tovaccinate more than 50 percent of its elderly enrollees againstinfluenza.
Study Subjects
All persons 65 years of age or older who were continuously enrolledin Group Health through the vaccination season (October throughDecember, with most doses administered by mid-November) andthe following influenza season were were included in cohortsfor 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 onsetof 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 fromthe Minnesota Department of Health26,27,28. This surveillancesystem relies on passive reporting from schools and nursinghomes, information included in the health department's standardizedreportable-disease forms (disease report cards), and specimenssent to the Division of Public Health laboratories. The informationis used to estimate the level of influenza activity and thespecific type or types of influenza virus circulating in thestate during a given year. In this study, the onset of the influenzaseason was defined from the date when influenza isolates werefirst recovered from communities in the state. For each yearthe influenza season was considered to extend through March.
Data Collection
Study data were obtained from Group Health's administrativedata bases, which include demographic characteristics and detailsof the use of outpatient, inpatient, and pharmacy services byall enrollees. Base-line information was collected for the subjectsin each cohort as of October 1; it included age, sex, and thenumber of visits to a physician during the previous year. Otherinformation included the number of hospitalizations during theprevious year (October through September), whether the patienthad received pneumococcal vaccine during the previous year (code907.32 in Current Procedural Terminology, 4th revision [CPT-4]),and whether he or she had been given a diagnosis of pneumoniain the previous year (codes 480 through 487 in the InternationalClassification of Diseases, Ninth Revision, Clinical Modification[ICD-9-CM]). Information was also collected on whether the subjecthad been given the following inpatient or outpatient diagnosesfor the previous year: coronary heart disease (ICD-9-CM codes393 through 398, 410 through 414, 425, 428, and 429), chroniclung disease (ICD-9-CM codes 491 through 496 and 500 through518), 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 codes446, 710, and 714), dementia or stroke (ICD-9-CM codes 290 through294, 331, 340, 341, 348, and 438), nonhematologic cancer (ICD-9-CMcodes 140 through 199), hematologic cancer (ICD-9-CM codes 200through 208), or the acquired immunodeficiency syndrome (ICD-9-CMcodes 042 through 044). These diagnoses were selected to identifypersons who had medical conditions that might increase theirrisk for influenza-related complications2. Influenza-vaccinationstatus was also ascertained for each season (CPT-4 code 907.24).
Given the potential for incomplete coding of important base-linemedical information, we also collected data on prescriptionrefills during the three months preceding the immunization seasonand categorized them according to the therapeutic classificationof the American Hospital Formulary Service. The classes of medicationwere chosen to reflect high-risk diagnostic categories: cardiovascularagents (codes 240000, 240400, 240800, and 241200); chemotherapeuticagents (code 100000); hormonal agents for treating diabetes(codes 682000, 682008, 682020, and 682092); immunologic agents,including steroids and agents to induce remission of rheumatologicdiseases (codes 82000, 600000, 640000, and 680400); and agentsfor treating diseases of the respiratory tract (codes 121200and 861600).
The outcomes we studied included hospitalizations for pneumoniaand influenza (ICD-9-CM codes 480 through 487), for all acuteand chronic respiratory conditions (ICD-9-CM codes 460, 462,465, 466, 480 through 487, 490 through 496, and 500 through518), and for congestive heart failure (ICD-9-CM code 428).These diagnoses were chosen for consistency with the previouslyidentified categories of complications associated with influenza24.The outcome variables also included the costs of hospitalizationfor pneumonia and influenza, all acute and chronic respiratoryconditions, and congestive heart failure and death from allcauses. 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 an85 percent chance of detecting a reduction of 35 percent inoutcome events among influenza-vaccine recipients (this calculationwas made with use of Power, Epicenter Software, Pasadena, Calif.).For these calculations, we assumed a vaccination rate of 55percent, 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 conductbivariate analyses of continuous and categorical data for eachcohort. Analysis of covariance and logistic regression (withSPSS for Windows, version 6.0, SPSS, Chicago) were used to conductmultivariate analyses of the study outcomes with control forcovariates and potential confounders. Cost savings associatedwith vaccination were calculated from the institution's perspectiveas direct savings during each influenza season. The costs ofhospitalization for all acute and chronic respiratory conditionsand for congestive heart failure were combined, and savingswere calculated according to the following formulas: mean costsavings = (mean costs of hospitalization for unvaccinated subjects)- (mean costs of hospitalization for vaccine recipients) - (meancosts of influenza-vaccination program), and total cost savings= (mean cost savings) x (number of people vaccinated). The reductionin mortality among vaccine recipients was calculated from theresults of the logistic regression; the adjusted odds ratiowas used as an approximation of the relative risk, since outcomeevents were rare. The calculation was performed as follows:reduction in mortality = (1 - odds ratio) x 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-vaccinationrates were 45 percent, 58 percent, and 55 percent, respectively,in these three study periods. The base-line characteristicsof the subjects in each cohort are shown in Table 1. Vaccinerecipients were more likely than nonrecipients to have mostof the existing conditions at base line, including heart andlung disease, to have higher rates of use of health care resourcesin the previous year, such as visits to physicians and prescriptionrefills, and to have a history of pneumonia. Nonrecipients ofthe vaccine, on the other hand, were slightly older and morelikely 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 havebeen hospitalized during the past year; for the other two studyperiods, the rates were similar in the two groups.
Table 1. Base-Line Characteristics of the Study Subjects, According to Study Period and Vaccination Status.
The influenza seasons and numbers of outcome events are summarizedin Table 2. The three influenza seasons included epidemic andnonepidemic years, with varying degrees of matching betweencirculating virus strains and vaccine antigens. In the secondseason (1991-1992), influenza A was epidemic, and there wasan excellent match between circulating virus strains and vaccineantigens; the first season (1990-1991) was a nonepidemic yearfor influenza B, with a very good match between circulatingvirus strains and vaccine antigens; and the third season (1992-1993)was a mixed year with early, nonepidemic influenza B (therewas an excellent match between circulating strains and vaccineantigens) and late epidemic influenza A (there was a poor matchbetween circulating strains and vaccine antigens). The totalnumbers of outcome events were highest during the second influenzaseason of the study, which was the most severe season, characterizedby epidemic influenza A.
Table 2. Characteristics of Influenza Seasons and Numbers of Outcome Events for Each Influenza Season.
The final multivariate models included influenza-vaccinationstatus, age, sex, number of visits to a physician during theprevious year, number of hospitalizations in the previous year,and number of prescription refills for each of the five therapeuticclasses of medication. Also included were variables indicatingwhether the subject had been given a diagnosis of heart disease,lung disease, vasculitis or rheumatologic disease, or dementiaor stroke as an outpatient; whether he or she had been givena 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 contributesignificantly to the models after we included the number ofrefills for the corresponding therapeutic classes of medication;these variables were therefore not included in the final models.Similarly, other variables, such as pneumococcal-vaccinationstatus, were excluded because they did not contribute significantlyto the models (P>0.10 for all comparisons).
The results of the analysis of covariance to compare the meannumber of hospitalizations for pneumonia and influenza, allacute and chronic respiratory conditions, and congestive heartfailure in vaccine recipients and nonrecipients are shown inTable 3 and Figure 1. Vaccination against influenza was associatedwith significantly fewer hospitalizations for pneumonia andinfluenza (range of reduction, 48 to 57 percent; P 0.002 forall 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 associatedwith fewer hospitalizations for congestive heart failure duringthe epidemic 1991-1992 season (a 37 percent reduction; P = 0.04).
Table 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.
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).
The light bars represent influenza-vaccine recipients, and the dark bars nonrecipients. The data have been adjusted for the base-line risk factors listed in the text. P values are for the comparisons between the groups within each influenza season; NS denotes not significant.
The results of the analysis of covariance used to evaluate themean costs of hospitalization for pneumonia and influenza, allacute and chronic respiratory conditions, and congestive heartfailure are shown in Table 4. The costs of hospitalizationsfor pneumonia and influenza, all acute and chronic respiratoryconditions, and congestive heart failure were significantlylower among vaccine recipients than among unvaccinated subjectsin 1991-1992 (reductions of 52 percent, 47 percent, and 66 percent,respectively; P<0.005 for all comparisons). Expenses forhospitalizations for all acute and chronic respiratory conditionsand congestive heart failure were also lower among vaccine recipientsin 1990-1991 (reductions, 37 percent and 43 percent, respectively;P 0.05 for both comparisons). Trends consistent with thesefindings, although not statistically significant, were seenin the costs of hospitalization for pneumonia and influenzain 1990-1991 and 1992-1993 and for all acute and chronic respiratoryconditions in 1992-1993 as well.
Table 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 cost of Group Health's influenza-vaccination program averaged$4 per person vaccinated (unpublished data). This included allcosts for the vaccine, supplies, advertising and mailings, personnelto administer the vaccine, and miscellaneous administrativeexpenses. After subtracting the mean costs of the program, thecombined direct savings in the costs of hospitalizations forall acute and chronic respiratory conditions and for congestiveheart failure in 1990-1991 and 1991-1992 (the two years forwhich savings were statistically significant) were $114 and$235 per person vaccinated, respectively. For 1992-1993, estimatedcost savings was $21 per person vaccinated, but the differencewas not significant (P = 0.56). The total cumulative directsavings in hospitalizations for all acute and chronic respiratoryconditions and for congestive heart failure among vaccine recipientsover the three years was nearly $5 million.
In the three influenza seasons, vaccination was associated withsignificant decreases of 39 to 54 percent in mortality fromall causes (P<0.001 for all comparisons). The adjusted oddsratios for the risk of dying among vaccine recipients as comparedwith 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 confidenceinterval, 0.47 to 0.81) in 1992-1993. The unadjusted odds ratioswere 0.57, 0.56, and 0.64, respectively.
Discussion
In this serial cohort study we found that among elderly peopleliving in the community, vaccination against influenza was associatedwith less frequent hospitalizations for complications of influenza,with fewer deaths during the influenza season, and with directsavings in health care costs. These findings were consistentover three consecutive seasons among cohorts of more than 25,000elderly men and women.
Assessments of the effect of influenza on populations have oftenbeen limited to evaluations of excess hospitalizations for pneumoniaand influenza and deaths during influenza epidemics (as comparedwith the base-line numbers in a nonepidemic year). The impactof influenza on the elderly may be much greater than has generallybeen acknowledged, however. For example, not only are ratesof hospitalization for pneumonia and influenza higher duringthe influenza season, but so also are rates of hospitalizationfor all acute and chronic respiratory conditions and even forcongestive heart failure17,24,30,31,32,33. These effects areevident during both epidemic and nonepidemic years24. Thus,it has been suggested that studies of the effects of influenzaon the elderly should evaluate all these outcomes in both epidemicand nonepidemic years24.
Our study was designed specifically to take these issues intoaccount. We assessed the effectiveness of influenza vaccinewith respect to a broad range of influenza-associated complications,including pneumonia and influenza, acute and chronic respiratoryconditions, and congestive heart failure in both epidemic andnonepidemic years. We were thus able to assess the effectivenessof influenza vaccine in reducing the number of hospitalizationsand health care costs for each of these disease categories.We found that the vaccine was beneficial in both epidemic andnonepidemic years; however, its efficacy was greatest duringthe 1991-1992 season, when influenza A was epidemic and whenthere was an excellent match between the vaccine and circulatingviral strains.
Our findings corroborate the results in three recent case-controlstudies that demonstrated the efficacy of influenza vaccineamong noninstitutionalized elderly people; these studies usedmore limited outcome measures than did our study and assessedfewer base-line risk characteristics among patients19,20,21.All three studies showed reductions of 30 to 45 percent in therate of hospitalization for pneumonia and influenza during selectedepidemic years. The investigators in one study also measuredhospitalizations for all acute and chronic respiratory conditionsand found reductions of 15 to 34 percent among vaccine recipients;they also found reductions of 27 to 30 percent in mortalityfrom all causes19. We observed decreases of 48 to 57 percentin the rate of hospitalization for pneumonia and influenza,decreases of 27 to 39 percent in the rate of hospitalizationfor all acute and chronic respiratory conditions, and decreasesof 39 to 54 percent in mortality from all causes. Influenzaand its complications are major health problems among elderlypeople. Undoubtedly, influenza often goes unrecognized as aprecipitating factor in the deaths of many elderly people.
It has been suggested that vaccinating elderly persons againstinfluenza is more cost effective than many other preventiveand therapeutic interventions, such as the pneumococcal vaccine,screening for cervical cancer, treatment of lipid disorders,and coronary-artery bypass surgery34,35,36. In some situations,vaccination against influenza has been shown to produce costsavings -- or at least potential savings -- that depend on thelevel of efficacy of the vaccine, vaccination coverage rates,the population's risk profile, the cost of the vaccine, andwhether future medical costs for additional years of life gainedwere included in the calculations21,34,35,36,37,38,39,40. Thedirect cost savings attributable to vaccination in our studytotaled almost $5 million and averaged $117 for each of the41,418 people immunized during the three years we studied. Thisfigure is higher than other estimates of savings produced bythe influenza vaccine. Previous studies probably underestimatedcost savings by failing to include reductions in the costs ofhospitalization for congestive heart failure and acute and chronicrespiratory conditions other than pneumonia and influenza orby assuming that the vaccine had benefits only during epidemicyears. In our study we may also have underestimated cost savingsattributable to vaccination against influenza, since we didnot include estimates of savings due to the decreased use ofoutpatient health care resources.
The strengths of our study include the use of the cohort design,the strongest of all noninterventional or observational studydesigns,41 and the large samples with high proportions of vaccinerecipients. The inclusion of data from three consecutive influenzaseasons also reduced the likelihood of spurious conclusions.
A limitation of observational studies, including those thatuse administrative data sets, is the difficulty of performingadequate risk adjustment in multivariate analyses42. Withoutthe randomization of study subjects that is usually performedin a clinical trial, the chance is greater that there will beimportant unmeasured differences between the study groups thatmight influence the study outcome. In our study, we collectedextensive information on base-line risk factors for hospitalizationand death from influenza-associated complications so as to allowadequate adjustment for risk factors including age, a historyof heart or lung disease, previous hospitalization,1,17,43 andother conditions that are indications for vaccination, suchas diabetes, neoplastic disease, and immunosuppression2. Weincluded 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 variableswere included in our multivariate analyses, we were able toassess the independent contribution of vaccination against influenzato the outcome events.
Recently Medicare added vaccination against influenza to itslist of reimbursable services for the 31 million elderly peoplein this country. With clear and striking evidence of the effectivenessof the vaccine in reducing hospitalizations and deaths and inproducing direct cost savings, providers and patients alikeshould take steps to ensure that people at high risk receivethe influenza vaccine each year. Few, if any, other preventiveinterventions for adults match these benefits.
Supported in part by a grant from Connaught Laboratories.
We are indebted to John Krystosek for obtaining the study dataand to Andrew Nelson for his support and encouragement of thisproject.
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. Presented in part at the national meeting of the Society of General Internal Medicine, Washington, D.C., April 28, 1994.
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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