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The Influence of Staff and Resident Immunization Rates on Influenza-like Illness Outbreaks in Nursing Homes
The Influence of Staff and Resident Immunization Rates on Influenza-like Illness Outbreaks in Nursing Homes Lisa R. Shugarman, PhD, Craig Hales, MD, MPH, Claude Messan Setodji, PhD, Barbara Bardenheier, MPH, MA, and Joanne Lynn, MD, MA, MS Objective: To evaluate the influence of immunization rates on the likelihood of influenza-like illness (ILI) clusters in nursing facilities. Design: Retrospective cross-sectional study. Setting: Nursing facilities in a single for-profit chain (N ⫽ 301). Participants: Nursing home residents and staff in each facility. Measurements: Resident and staff influenza immunization rates during the 2004 –2005 influenza season, indicator of ILI cluster in facility defined as 3⫹ ILI cases reported within 72 hours in close proximity within the facility, hospitalization and mortality rates for facilities reporting ILI clusters, indicator of confirmatory laboratory testing for ILI cases in facility. Results: Staff (median ⫽ 38%) and resident (median ⫽ 85%) rates of immunization did not independently predict the likelihood of an outbreak but jointly were
Influenza outbreaks in nursing homes are common and their effects can be severe. Older adults are particularly vulnerable, especially those with multiple comorbidities and functional impairment. Between 1979 and 2000, the average influenza-related hospitalization rate was 36.8 per 100,000 person-years annually; among the elderly, this rate rose to 628.6 per 100,000 personyears.1 Over 90% of deaths attributable to influenza were among the elderly as well; the average annual rate for those 65 and older was 22.1 per 100,000 person-years as compared with 3.1
RAND Corporation, Santa Monica, CA (L.R.S., C.M.S.); Centers for Disease Control and Prevention, Atlanta, GA (C.H., B.B.); RAND Corporation, Arlington, VA (J.L.). The authors had no conflicts of interest associated with the conduct of this study. Address correspondence to Lisa R. Shugarman, PhD, RAND Corporation, 1776 Main Street, PO Box 2138, Santa Monica, CA 90401-2138. E-mail: [email protected]
Copyright ©2006 American Medical Directors Association DOI: 10.1016/j.jamda.2006.06.002 562 Shugarman et al.
strong predictors. For example, facilities having greater than 55% of staff and greater than 89% of residents immunized were almost 60% less likely to have an ILI cluster (odds ratio [OR]: 0.410; 95% CI: 0.19, 0.89) compared to all others. Facilities with higher proportions of Medicaid-funded residents were less likely to have an outbreak. Each 1% increase in the proportion of residents with Medicaid was associated with a 2.5% decrease in the risk of a cluster (OR: 0.975; 95% CI: 0.956, 0.995). Bed size and staff size did not significantly influence the likelihood of an outbreak. Among facilities with outbreaks, higher vaccination rates did not predict lower rates of hospitalizations or deaths. Approximately two thirds of all ILI clusters had laboratory testing to confirm the diagnosis of influenza. Three quarters of the facilities in which outbreaks occurred and for which confirmatory tests were performed (50/67, 74.6%) had 1⫹ cases positively identified as influenza. Conclusion: Both staff and residents must have high rates of vaccination to substantially alter the rate and impact of influenza outbreaks in nursing facilities. (J Am Med Dir Assoc 2006; 7: 562–567)
per 100,000 person-years overall.2 Multiple vulnerable people requiring intimate personal care makes a nursing home environment particularly risky for outbreaks. Menec and colleagues3 reported a hospitalization rate 3 times larger for nursing home residents age 65 and older as compared with similar-aged community-based residents (31.9 versus 9.8 per 1000 population, respectively). The annualized mortality rate for nursing home residents was over 30 times larger than for similar-aged community-based residents (34.0 versus 1.04 per 1000 population, respectively).3 The Centers for Disease Control and Prevention (CDC) and others recommend influenza immunization of nursing home residents and health care workers as the primary method for preventing influenza and its complications.4 – 6 In addition, the Centers for Medicare and Medicaid Services (CMS) recently amended the Conditions of Participation to require that all long-term care facilities offer influenza immunization to their residents annually unless medically contraindicated or refused.7 Most facilities offer influenza immunizations to their residents8,9 and immunization rates for residents in the existing literature JAMDA – November 2006
range from 58.5% to 84%.8 –11 Fewer facilities offer the influenza vaccine to health care workers9 and immunization rates are generally low; published studies provide estimates ranging from 33% to 61%.8,9,12–14 Only one of these studies12 differentiated health care workers in nursing homes from other facilities. Influenza vaccine efficacy is generally high among healthy adults; approximately 86% when vaccine and virus are matched.15 Among older adults, efficacy decreases, particularly among older adults with chronic conditions and multiple comorbidities. In a recent meta-analysis of the relevant literature, effectiveness of the influenza vaccine against ILI in nursing homes was 23% and was not significant for influenza.16 Influenza immunization appears to protect against hospital admissions (vaccine efficacy: 45%, range 16% to 64%) and against all-cause mortality (vaccine efficacy: 60%, range 23% to 79%).16 Large influenza outbreaks can occur in nursing homes despite widespread immunization of residents.17 Efforts to increase influenza immunization for health care workers in nursing homes have grown in recent years, fueled by limited evidence that such efforts can help reduce virus transmission, suffering, hospitalizations, and death among nursing home residents. Potter and colleagues14 randomized long-term care hospitals to immunize health care workers during the 1994–1995 influenza season and found significant reductions in resident mortality and in ILI. Patient vaccination alone did not significantly influence mortality. In a similar randomized controlled trial conducted during the following influenza season in long-term care facilities, the overall mortality rate for patients was 13.6% in staff-immunized facilities and 22.4% in non–staff-immunized facilities (P ⬍ .05). The rate of confirmed influenza infections did not differ (5.4% in immunized facilities versus 6.7% in nonimmunized facilities, respectively; P ⫽ .055).12 To our knowledge, only the study by Potter and colleagues14 examined the effect of influenza immunization in residents in long-term care facilities, controlling for health care worker immunization. In facilities where health care workers had high rates of immunization, long-term care patients were significantly less likely to develop ILI, and the incidence of ILI was lowest when both patients and health care workers had high rates of immunization.14 The current study examines how resident and staff immunization rates are separately and jointly associated with the likelihood of an ILI cluster. We base our analyses on the theoretical model that higher rates of immunization in resident and staff populations may be protective against serious outbreaks, and we explore these relationships in a sample of nursing facilities that is larger and more geographically dispersed than that used in previous studies. METHODS Data Data for this study come from a single nursing home corporation with facilities located in many parts of the United States. A central office staff member distributed a survey to the executive director or director of nursing in 344 facilities in July 2005, asking a series of questions about each facility’s experience with ILI clusters during the flu season that had just ended (October 2004 –May 2005). ORIGINAL STUDIES
The survey included questions about the number of residents and staff immunized during the season, the total number of residents in the facility during that time (including those discharged), as well as the total number of staff during that period. Each facility also reported whether or not the facility experienced an ILI cluster, defined as a cluster of three or more residents within a 72-hour period having influenza-like symptoms (sudden onset of fever or complaints of “feverishness” and at least one of the following respiratory symptoms: sore throat, runny nose, cough, or nasal congestion). For those that indicated they had at least one ILI cluster, the survey posed a series of questions regarding the total number of cases, the total number of ILI-related hospitalizations and deaths, and the total number of influenza cases tested with and confirmed by either a rapid influenza test or a nasopharyngeal swab and culture. In addition to the survey data, the nursing home corporation provided information about the bed size of each facility and the percentage of the residents who had Medicaid as the primary payor. Our analyses linked these data to the survey data. Measures We calculated the immunization rate for residents and staff separately by dividing the total of each who had documented immunization by the total number in the facility during the influenza season. For descriptive purposes, we established quartiles for resident and staff immunization rates based on the distribution for their respective rates. We also created a measure to reflect the proportion of the facility’s residents who had influenza-like illnesses by dividing the total number who had influenza-like symptoms (as defined previously) by the total number of residents. We created an indicator variable identifying facilities that reported an ILI cluster (yes/no). Among facilities with an ILI cluster, we created indicator variables to reflect any ILI-related hospitalizations or any deaths versus none. We also calculated the hospitalization and death rates from reported ILI clusters. A series of indicator variables characterized the facilities by whether or not they conducted any rapid influenza tests or nasal swab/culture tests. We created indicator variables to reflect those facilities that identified at least one positive case of the influenza virus among those that did conduct such tests. Finally, we created a set of measures to characterize the facilities by their bed size, staff size, and the proportion of residents on Medicaid. These measures controlled for variation in facility characteristics in multivariate models. We established indicator variables for each measure, reflecting facilities that were at or above the median for that measure relative to those below the median. Analysis We conducted a number of descriptive analyses, comparing the characteristics of all facilities in our sample. Among those reporting an ILI cluster, we conducted additional descriptive analyses to characterize the size and scope of the ILI cluster, and the methods for and the results of confirmatory tests in those facilities. We initially estimated logistic regression models to predict the likelihood of having an ILI cluster based on resident and Shugarman et al. 563
High Staff Immunization
High Resident/ Low Staff
High Resident/ High Staff
High Resident Immunization
Low Resident/ Low Staff
Low Resident/ High Staff
Low Resident Immunization
Resident Immunization Rate
Low Staff Immunization
Staff Immunization Rate
Fig. 1. Characteristics of facilities by immunization rates.
we had sufficient sample sizes in any single quadrant to produce stable regression parameters. We could have tested many from a theoretically infinite set of cutpoints in this analysis. However, the total facility sample size and the minimum sample size requirement we imposed limited the actual number of cutpoints tested. We fit models that tested high staff/ high resident immunization facilities against all other facilities. Any negative, statistically significant effect would suggest that facilities in the high staff/high resident immunization group would be less likely to have an ILI cluster, compared to facilities that did not reach the thresholds for both staff and resident immunization rates. This analysis was repeated for different threshold definitions of high immunization rates (eg, rates greater then 20%, 30%, 40%, and so forth) and we evaluated a diagnostic plot of the groups with statistically significant effects. RESULTS
staff immunization rates, controlling for other facility characteristics. We tested the relationship between staff and resident vaccination rates and the presence of an ILI cluster using 2 approaches. First, we tested the direct effects of continuous measures of staff and resident immunization rates on the likelihood of having an ILI cluster in logistic regression models. Then, we explored the relationship between quartiles of immunization rates and the likelihood of having an ILI cluster. We then developed a method to test the joint effect of staff and resident immunization rates on the likelihood of an ILI cluster. To find the influential immunization rate thresholds, we fit a series of multivariate logistic regression models of the likelihood of the report of an ILI cluster on the staff and resident immunization rates, adjusting for facility characteristics. We established cutpoints, defining resident and staff immunization rates above the cutpoint as “high” and at or below the cutpoint as “low” and arrayed facilities in a plot with quadrants reflecting the following immunization characteristics: high staff/high resident, high staff/low resident, low staff/high resident, and low staff/low resident (see Figure 1). The initial cutpoints were arbitrary; however, we required that each quadrant contain at least 40 facilities to ensure that
The survey was sent to 344 facilities, of which 310 responded (90.1% response rate). Of the facilities that responded, 4 were excluded because they did not report the number of residents vaccinated, 3 were excluded because they did not report the number of staff vaccinated, and 1 was excluded because the number of influenza cases reported was an extreme outlier (n ⫽ 578 influenza cases in a 124-bed facility). The resulting sample size for these analyses was 301 facilities. Table 1 presents some basic descriptive information for each facility overall and then stratified by ILI cluster status of the facility. The average facility had approximately 101 beds (standard deviation [SD]: ⫾ 41 beds), 126 residents (SD: ⫾ 85), and 94 staff (SD: ⫾ 42). The number of residents could reasonably exceed the number of beds during the influenza season because of turnover. The average facility immunization rate for residents was 78.4% (median 84.6). Staff immunization rates were substantially lower with a mean rate of 40.8% (median 37.5%). Most facility characteristics did not differ significantly by ILI cluster status, although larger facilities trended toward being more likely to report an ILI cluster. Only the percentage of the residents with Medicaid significantly differed; facilities with no ILI cluster were more likely
Table 1. Descriptive Characteristics of Nursing Facilities (N ⫽ 301) Facility Characteristics by ILI Cluster Status, Mean (SD) Facility Characteristic Bed size Staff size Residents Residents with Medicaid (%)* Resident immunization rate (%) Staff immunization rate (%) Facilities reporting an ILI cluster (%)
Mean (SD) 100.9 (40.7) 93.6 (41.7) 125.0 (84.5) 71.2 (13.9) 78.4 (20.4) 40.8 (28.7) 33.9
Median 99 88 105 73.8 84.6 37.5 —
Range
ILI Cluster (N ⴝ 102)
34–355 10–340 6–650 0–100 ⬍1–100 0–100 —
102.8 (36.5) 99.9 (40.3) 137.0 (97.3) 68.2 (17.2) 78.1 (19.7) 42.5 (26.5) —
No ILI Cluster (N ⴝ 199) 100.0 (42.8) 90.4 (42.1) 119.8 (76.7) 72.8 (11.7) 78.5 (20.8) 39.9 (29.9) —
ILI, influenza-like illness. * The means for Medicaid status of facility residents by facility ILI cluster status are significantly different (P ⫽ .012). 564 Shugarman et al.
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100.0
Resident Immunization Rates
90.0 80.0 70.0 60.0 50.0 40.0 30.0 20.0 10.0 0.0 0.0
10.0
20.0
Facilities w/ILI Cluster
30.0
40.0
50.0
60.0
70.0
80.0
90.0
100.0
Staff Immunization Rates
Facilities w/No ILI Cluster
Fig. 2. Plot of facilities by resident and staff immunization rates.
Fig. 3. Illustration of influential thresholds associated with reduced likelihood of ILI cluster.
to have a larger proportion of Medicaid-eligible residents. Among the 301 facilities in this sample, 102 (33.9%) reported an ILI cluster. Figure 2 presents a scatter plot of the resident and staff immunization rates. The dark circles reflect facilities that reported an ILI cluster and the open circles represent facilities that did not report an ILI cluster. Table 2 describes the size and scope of ILI clusters in those facilities that reported an ILI cluster. The average ILI cluster included just over 15 residents experiencing influenza-like symptoms. The average number of hospitalizations and deaths were 2.2 and less than 1 per facility, respectively. The hospitalization rate per 100 ILI cases was 13.7; the death rate per 100 ILI cases was 4.5. About one third of all facilities reporting an ILI cluster performed no confirmatory tests of residents with influenza-like symptoms. Of those facilities that performed at least one test (n ⫽ 67), 50 (74.6%) had at least one positive test and 17 (25.4%) had no positive tests. As described above, we tested the association of the direct effects of staff and resident immunization rates as both continuous measures and in quartiles. We estimated models with each immunization rate, both with and without controlling for the other immunization rate, as well as with and without facility characteristics (e.g., bed size, staff size, and percent of residents covered by Medicaid). We found no significant association between these direct effects and the likelihood of an ILI cluster in any of these models (data not shown). Figure 3 presents the same plot of staff and resident immu-
nization rates presented in Figure 2 overlaid by an illustration of an influential threshold of staff and resident immunization rates. We found that facilities that had achieved a staff immunization rate greater than 55% and a resident immunization rate greater than 89% (represented by the shaded region) were significantly less likely to report an ILI cluster than those that had rates less than or equal to these thresholds. Table 3 presents the results of logistic regressions testing the effect of this threshold on the likelihood of having an ILI cluster alone and controlling for facility characteristics. In the unadjusted model, staff and resident immunization rates greater than 55% and 89%, respectively, were almost 60% less likely to experience an ILI cluster than were facilities that had lower immunization rates for either or both of staff and residents (OR: 0.41, 95% CI: 0.19, 0.89). Controlling for facility characteristics further reduced the odds of having an ILI cluster in facilities with high immunization rates in both staff and residents, although the difference between the adjusted and unadjusted models was not substantial. Similar to the descriptive analyses (Table 1), the only facility characteristic that was significant in the multivariate model was whether the facility had Medicaid rates above the median for all facilities. Facilities with an above-median Medicaid rate were half as likely to have an ILI cluster as those with lower percentages of residents on Medicaid. We also tested the facility characteristics in their continuous form and found similar results (data not shown).
Table 2. Characteristics of Facilities With Reported Influenza-Like Illness (ILI) Cluster (N ⫽ 102)
Number of residents in ILI cluster Number of ILI-related hospitalizations Hospitalization rate* Number of ILI-related deaths Death ratea Facilities performing confirmatory tests (%)
Mean (SD)
Median
Range
15.2 (12.7) 2.2 (3.9) 13.7 0.84 (2.4) 4.5 65.7
10.5 0 — 0 — —
3–60 0–23 — 0–14 — —
* Rate reported per 100 ILI cases. ORIGINAL STUDIES
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Table 3. Illustration of Logistic Regression Model Predicting the Likelihood of an ILI Cluster
Resident immunization rate: ⬎89% Staff immunization rate: ⬎55% Bed size† Staff size† % Residents with Medicaid†
Unadjusted OR (95% CI)
Adjusted OR (95% CI)
0.41 (0.19–0.89)*
0.39 (0.17–0.87)*
— — —
0.86 (0.40–1.86) 1.84 (0.86–3.94) 0.50 (0.30–0.84)
ILI, influenza-like cluster; OR, odds ratio; 95% CI, 95% confidence interval. * The odds ratios presented here refer to facilities with the combination of a resident immunization rate greater than 89% and a staff immunization rate greater than 55%. † Indicator variables reflecting facility characteristics greater than the median value of that characteristic.
We evaluated all the possible thresholds, by whole percentages, that met our criterion that at least 40 facilities be included in the comparison groups to ensure we could produce stable estimates. The unadjusted ORs for the thresholds tested ranged from 0.37 (95% CI: 0.16 – 0.87) for staff immunization rates greater than 65% and resident immunization rates greater than 90% to 0.44 (95% CI: 0.20 – 0.95) for staff immunization rates greater than 57% and resident immunization rates greater than 89%. Clearly, higher resident and staff immunization rates had a larger protective effect, although the differences were not substantial between the largest and smallest significant effect. DISCUSSION This study found a strong association between higher rates of both resident and staff influenza immunizations and the reduced likelihood of an ILI cluster in the nursing home. This finding offers new evidence that increasing resident immunization rates alone is not likely to have a significant impact on influenza outbreaks in long-term care facilities. However, the joint effort to increase resident and staff influenza immunization rates can substantially reduce the suffering and death associated with influenza. In nursing facilities, a strong motivating force is the desire to avoid the disruption and despair of many residents and staff being sick at the same time, and many residents dying close together. One third of nursing home facilities in this study experienced an ILI cluster, despite a relatively high median resident influenza immunization rate and a median staff immunization rate in the same range as the national average for health care facilities. The resident immunization rate alone was not a statistically significant predictor of the occurrence of an ILI cluster, given the range of immunization rates in our study. We were unable to validate that immunization of residents had an impact on rates of ILI or ILI-related hospitalizations. Nursing home staff immunization rates also did not, on their own, predict the occurrence of an ILI cluster or influenza-related hospitalizations and deaths. In the only study we identified that tested this same relationship,12 the authors found that staff immunization rates did not influence the likelihood of an outbreak; however, this and other previous studies have indicated an association between higher staff immunization rates and decreased resident influenza-related mortality.12,14,16 566 Shugarman et al.
Although resident and staff immunization rates independently showed no effect on the occurrence of an ILI cluster, our analysis identified an interaction between resident and staff immunization rates. For example, nursing homes with a resident immunization rate greater than 89% and a staff immunization rate greater than 55% were 60% less likely to experience an ILI cluster, compared with nursing homes that did not achieve these rates in both residents and staff. Although previous studies have demonstrated a significant association between facility size and outbreak status,10,18 facility characteristics were generally not informative in the current analysis. However, facilities with a higher proportion of residents on Medicaid were significantly less likely to experience an ILI cluster. The reason for this association probably warrants further consideration. This study demonstrated a significant association between immunization practices and the risk of an ILI cluster despite a poor match between the 2004 –2005 influenza vaccine composition and the prevalent strains circulating in the United States during that season. Influenza A (H3N2) predominated during the 2004 –2005 influenza season. Of the influenza A (H3N2) subtypes that were antigenically characterized by the Centers for Disease Control and Prevention, 78% were A/California/7/2004-like, an antigenically similar component that was not present in the 2004 –2005 influenza vaccine.19 Several factors limit the internal and external validity of this study. The survey was sent to facilities during the summer to collect data on the previous influenza season, introducing the possibility of recall bias. These facilities came from a single nursing home company, and thus the findings may not be generalizable to other facilities. However, we had a very high survey response rate (90.1%) and the facilities were characterized by a wide distribution of bed size and geographic location, reflecting the greater heterogeneity found across all facilities. Facilities reported data on resident and staff immunization rates, ILI cases, hospitalizations, deaths, and laboratory results based on their own data collection mechanisms, which may have differed from facility to facility. Although the cohort limits confidence in generalization, the facilities in a single company will have the advantages of shared information systems, data collection mechanisms, and definitions of staff. Thus, the reporting process across these facilities was likely to be more homogeneous, compared to a randomly selected group of independent facilities or facilities from difJAMDA – November 2006
ferent companies. In addition, we enhanced consistency in reporting by giving respondents a standard definition of an ILI cluster. This project did not address the question of whether family visitors, volunteers, and others who frequent the nursing home environment are also important vectors, and whether their immunization status is important. Finally, this project reported findings in just 1 year, and other years could have differences arising from severity of influenza, matching of influenza type with immunization contents, and other factors. CONCLUSION Influenza outbreaks continue to occur in nursing homes despite high immunization rates of their residents. In this study, only nursing homes with higher rates of both resident and staff immunization saw a significantly reduced risk of experiencing an ILI cluster. These findings suggest that, in addition to achieving a high immunization rate for residents, immunization of health care workers is a necessary part of a strategy to reduce risk of an ILI cluster in nursing homes. Calls for increasing immunization rates in health care workers have been made on the basis that it improves safety and efficacy in health service provision and that health care workers have a legal and ethical duty to get immunized.20 The recent proposal by the Joint Commission on Accreditation of Health Care Organizations to require efforts to ensure immunization of health care workers21 and the educational material provided to long-term care facilities by the Medicare Quality Improvement Community (MedQIC)22 are examples of implementation of this insight. Assuming that it is confirmed in future work, more forceful requirements, or public information about the facility’s rates, might be wise policy. Future research might replicate this study in a larger sample of facilities on a prospective basis, over multiple years, and might also further explore the association of facility characteristics such as the proportion of residents on Medicaid with the likelihood of an influenza outbreak. The authors thank Kelly Sand, Bill Kubat, Keith Krein, and Barbara Baylis for their advice and technical assistance. This study was funded in part by the Centers for Disease Control and Prevention (CDC) (5U01IP000034-02). This manuscript was reviewed and approved of by the CDC. REFERENCES 1. Thompson WW, Shay DK, Weintraub E, et al. Influenza-associated hospitalizations in the United States. JAMA 2004;292(11):1333–1340. 2. Thompson WW, Shay DK, Weintraub E, et al. Mortality associated with influenza and respiratory syncytial virus in the United States. JAMA 2003;289(2):179 –186. 3. Menec VH, MacWilliam L, Aoki FY. Hospitalizations and deaths due to respiratory illnesses during influenza seasons: A comparison of community residents, senior housing residents, and nursing home residents. J Gerontol A Biol Sci Med Sci 2002;57(10):M629 – 635. 4. Harper SA, Fukuda K, Uyeki TM, Cox NJ, Bridges CB. Prevention and control of influenza. Recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep 2005;54(RR-8): 1– 40.
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5. Pearson ML, Bridges CB, Harper SA. Influenza vaccination of healthcare personnel: Recommendations of the Healthcare Infection Control Practices Advisory Committee (HICPAC) and the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep 2006;55(RR2):1–16. 6. Talbot TR, Bradley SE, Cosgrove SE, Ruef C, Siegel JD, Weber DJ. Influenza vaccination of healthcare workers and vaccine allocation for healthcare workers during vaccine shortages. Infect Control Hosp Epidemiol 2005;26(11):882– 890. 7. Department of Health and Human Services, Centers for Medicare and Medicaid Services. 42 CFR Part 483, Medicare and Medicaid Programs: Condition of Participation: Immunization Standard for Long-Term Care Facilities. Federal Register 2005;70(194):58833–58852. 8. Nichol KL, Grimm MB, Peterson DC. Immunizations in long-term care facilities: Policies and practice. J Am Geriatr Soc 1996;44(4):349 – 355. 9. Zadeh MM, Buxton Bridges C, Thompson WW, Arden NH, Fukuda K. Influenza outbreak detection and control measures in nursing homes in the United States. J Am Geriatr Soc 2000;48(10):1310 –1315. 10. Arden N, Monto AS, Ohmit SE. Vaccine use and the risk of outbreaks in a sample of nursing homes during an influenza epidemic. Am J Public Health 1995;85(3):399 – 401. 11. Bardenheier B, Shefer A, McKibben L, Roberts H, Bratzler D. Characteristics of long-term-care facility residents associated with receipt of influenza and pneumococcal vaccinations. Infect Control Hosp Epidemiol 2004;25(11):946 –954. 12. Carman WF, Elder AG, Wallace LA, et al. Effects of influenza vaccination of health-care workers on mortality of elderly people in long-term care: A randomised controlled trial. Lancet 2000;355(9198):93–97. 13. King WD, Woolhandler SJ, Brown AF, et al. BRIEF REPORT: Influenza Vaccination and Health Care Workers in the United States. J Gen Intern Med Jan 20 2006. 14. Potter J, Stott DJ, Roberts MA, et al. Influenza vaccination of health care workers in long-term-care hospitals reduces the mortality of elderly patients. J Infect Dis 1997;175(1):1– 6. 15. Bridges CB, Thompson WW, Meltzer MI, et al. Effectiveness and costbenefit of influenza vaccination of healthy working adults: A randomized controlled trial. JAMA 2000;284(13):1655–1663. 16. Jefferson T, Rivetti D, Rivetti A, Rudin M, Di Pietrantonj C, Demicheli V. Efficacy and effectiveness of influenza vaccines in elderly people: A systematic review. Lancet 2005;366(9492):1165–1174. 17. Drinka PJ, Gravenstein S, Krause P, Schilling M, Miller BA, Shult P. Outbreaks of influenza A and B in a highly immunized nursing home population. J Fam Pract 1997;45(6):509 –514. 18. Patriarca PA, Weber JA, Parker RA, et al. Risk factors for outbreaks of influenza in nursing homes. A case-control study. Am J Epidemiol 1986;124(1):114 –119. 19. Update: Influenza activity—United States and worldwide, 2004 – 05 season. MMWR Morb Mortal Wkly Rep 2005;54(25):631– 634. 20. Poland GA, Tosh P, Jacobson RM. Requiring influenza vaccination for health care workers: seven truths we must accept. Vaccine 2005;23(17– 18):2251–2255. 21. Joint Commission on Accreditation of Healthcare Organizations. Proposed Standards for Immunization of Staff, Students, Volunteers, and Licensed Independent Practitioners Against Influenza. Available at: http://www.jointcommission.org/NR/rdonlyres/3207FFDF-C540-40FD8901-55AEFD764F03/0/influenza_immunization_stds_fr.pdf. Accessed March 27, 2006. 22. Medicare Quality Improvement Community (MedQIC). Immunizations Toolkit. Available at: http://www.medqic.org/dcs/ContentServer?cid⫽ 1105558764854&pagename⫽Medqic%2FMQTools%2FToolTemplate& parentName⫽Topic&c⫽MQTools. Accessed March 23, 2006.
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Influenza outbreaks in nursing homes are common and their effects can be severe. Older adults are particularly vulnerable, especially those with multiple comorbidities and functional impairment. Between 1979 and 2000, the average influenza-related hospitalization rate was 36.8 per 100,000 person-years annually; among the elderly, this rate rose to 628.6 per 100,000 personyears.1 Over 90% of deaths attributable to influenza were among the elderly as well; the average annual rate for those 65 and older was 22.1 per 100,000 person-years as compared with 3.1
RAND Corporation, Santa Monica, CA (L.R.S., C.M.S.); Centers for Disease Control and Prevention, Atlanta, GA (C.H., B.B.); RAND Corporation, Arlington, VA (J.L.). The authors had no conflicts of interest associated with the conduct of this study. Address correspondence to Lisa R. Shugarman, PhD, RAND Corporation, 1776 Main Street, PO Box 2138, Santa Monica, CA 90401-2138. E-mail: [email protected]
Copyright ©2006 American Medical Directors Association DOI: 10.1016/j.jamda.2006.06.002 562 Shugarman et al.
strong predictors. For example, facilities having greater than 55% of staff and greater than 89% of residents immunized were almost 60% less likely to have an ILI cluster (odds ratio [OR]: 0.410; 95% CI: 0.19, 0.89) compared to all others. Facilities with higher proportions of Medicaid-funded residents were less likely to have an outbreak. Each 1% increase in the proportion of residents with Medicaid was associated with a 2.5% decrease in the risk of a cluster (OR: 0.975; 95% CI: 0.956, 0.995). Bed size and staff size did not significantly influence the likelihood of an outbreak. Among facilities with outbreaks, higher vaccination rates did not predict lower rates of hospitalizations or deaths. Approximately two thirds of all ILI clusters had laboratory testing to confirm the diagnosis of influenza. Three quarters of the facilities in which outbreaks occurred and for which confirmatory tests were performed (50/67, 74.6%) had 1⫹ cases positively identified as influenza. Conclusion: Both staff and residents must have high rates of vaccination to substantially alter the rate and impact of influenza outbreaks in nursing facilities. (J Am Med Dir Assoc 2006; 7: 562–567)
per 100,000 person-years overall.2 Multiple vulnerable people requiring intimate personal care makes a nursing home environment particularly risky for outbreaks. Menec and colleagues3 reported a hospitalization rate 3 times larger for nursing home residents age 65 and older as compared with similar-aged community-based residents (31.9 versus 9.8 per 1000 population, respectively). The annualized mortality rate for nursing home residents was over 30 times larger than for similar-aged community-based residents (34.0 versus 1.04 per 1000 population, respectively).3 The Centers for Disease Control and Prevention (CDC) and others recommend influenza immunization of nursing home residents and health care workers as the primary method for preventing influenza and its complications.4 – 6 In addition, the Centers for Medicare and Medicaid Services (CMS) recently amended the Conditions of Participation to require that all long-term care facilities offer influenza immunization to their residents annually unless medically contraindicated or refused.7 Most facilities offer influenza immunizations to their residents8,9 and immunization rates for residents in the existing literature JAMDA – November 2006
range from 58.5% to 84%.8 –11 Fewer facilities offer the influenza vaccine to health care workers9 and immunization rates are generally low; published studies provide estimates ranging from 33% to 61%.8,9,12–14 Only one of these studies12 differentiated health care workers in nursing homes from other facilities. Influenza vaccine efficacy is generally high among healthy adults; approximately 86% when vaccine and virus are matched.15 Among older adults, efficacy decreases, particularly among older adults with chronic conditions and multiple comorbidities. In a recent meta-analysis of the relevant literature, effectiveness of the influenza vaccine against ILI in nursing homes was 23% and was not significant for influenza.16 Influenza immunization appears to protect against hospital admissions (vaccine efficacy: 45%, range 16% to 64%) and against all-cause mortality (vaccine efficacy: 60%, range 23% to 79%).16 Large influenza outbreaks can occur in nursing homes despite widespread immunization of residents.17 Efforts to increase influenza immunization for health care workers in nursing homes have grown in recent years, fueled by limited evidence that such efforts can help reduce virus transmission, suffering, hospitalizations, and death among nursing home residents. Potter and colleagues14 randomized long-term care hospitals to immunize health care workers during the 1994–1995 influenza season and found significant reductions in resident mortality and in ILI. Patient vaccination alone did not significantly influence mortality. In a similar randomized controlled trial conducted during the following influenza season in long-term care facilities, the overall mortality rate for patients was 13.6% in staff-immunized facilities and 22.4% in non–staff-immunized facilities (P ⬍ .05). The rate of confirmed influenza infections did not differ (5.4% in immunized facilities versus 6.7% in nonimmunized facilities, respectively; P ⫽ .055).12 To our knowledge, only the study by Potter and colleagues14 examined the effect of influenza immunization in residents in long-term care facilities, controlling for health care worker immunization. In facilities where health care workers had high rates of immunization, long-term care patients were significantly less likely to develop ILI, and the incidence of ILI was lowest when both patients and health care workers had high rates of immunization.14 The current study examines how resident and staff immunization rates are separately and jointly associated with the likelihood of an ILI cluster. We base our analyses on the theoretical model that higher rates of immunization in resident and staff populations may be protective against serious outbreaks, and we explore these relationships in a sample of nursing facilities that is larger and more geographically dispersed than that used in previous studies. METHODS Data Data for this study come from a single nursing home corporation with facilities located in many parts of the United States. A central office staff member distributed a survey to the executive director or director of nursing in 344 facilities in July 2005, asking a series of questions about each facility’s experience with ILI clusters during the flu season that had just ended (October 2004 –May 2005). ORIGINAL STUDIES
The survey included questions about the number of residents and staff immunized during the season, the total number of residents in the facility during that time (including those discharged), as well as the total number of staff during that period. Each facility also reported whether or not the facility experienced an ILI cluster, defined as a cluster of three or more residents within a 72-hour period having influenza-like symptoms (sudden onset of fever or complaints of “feverishness” and at least one of the following respiratory symptoms: sore throat, runny nose, cough, or nasal congestion). For those that indicated they had at least one ILI cluster, the survey posed a series of questions regarding the total number of cases, the total number of ILI-related hospitalizations and deaths, and the total number of influenza cases tested with and confirmed by either a rapid influenza test or a nasopharyngeal swab and culture. In addition to the survey data, the nursing home corporation provided information about the bed size of each facility and the percentage of the residents who had Medicaid as the primary payor. Our analyses linked these data to the survey data. Measures We calculated the immunization rate for residents and staff separately by dividing the total of each who had documented immunization by the total number in the facility during the influenza season. For descriptive purposes, we established quartiles for resident and staff immunization rates based on the distribution for their respective rates. We also created a measure to reflect the proportion of the facility’s residents who had influenza-like illnesses by dividing the total number who had influenza-like symptoms (as defined previously) by the total number of residents. We created an indicator variable identifying facilities that reported an ILI cluster (yes/no). Among facilities with an ILI cluster, we created indicator variables to reflect any ILI-related hospitalizations or any deaths versus none. We also calculated the hospitalization and death rates from reported ILI clusters. A series of indicator variables characterized the facilities by whether or not they conducted any rapid influenza tests or nasal swab/culture tests. We created indicator variables to reflect those facilities that identified at least one positive case of the influenza virus among those that did conduct such tests. Finally, we created a set of measures to characterize the facilities by their bed size, staff size, and the proportion of residents on Medicaid. These measures controlled for variation in facility characteristics in multivariate models. We established indicator variables for each measure, reflecting facilities that were at or above the median for that measure relative to those below the median. Analysis We conducted a number of descriptive analyses, comparing the characteristics of all facilities in our sample. Among those reporting an ILI cluster, we conducted additional descriptive analyses to characterize the size and scope of the ILI cluster, and the methods for and the results of confirmatory tests in those facilities. We initially estimated logistic regression models to predict the likelihood of having an ILI cluster based on resident and Shugarman et al. 563
High Staff Immunization
High Resident/ Low Staff
High Resident/ High Staff
High Resident Immunization
Low Resident/ Low Staff
Low Resident/ High Staff
Low Resident Immunization
Resident Immunization Rate
Low Staff Immunization
Staff Immunization Rate
Fig. 1. Characteristics of facilities by immunization rates.
we had sufficient sample sizes in any single quadrant to produce stable regression parameters. We could have tested many from a theoretically infinite set of cutpoints in this analysis. However, the total facility sample size and the minimum sample size requirement we imposed limited the actual number of cutpoints tested. We fit models that tested high staff/ high resident immunization facilities against all other facilities. Any negative, statistically significant effect would suggest that facilities in the high staff/high resident immunization group would be less likely to have an ILI cluster, compared to facilities that did not reach the thresholds for both staff and resident immunization rates. This analysis was repeated for different threshold definitions of high immunization rates (eg, rates greater then 20%, 30%, 40%, and so forth) and we evaluated a diagnostic plot of the groups with statistically significant effects. RESULTS
staff immunization rates, controlling for other facility characteristics. We tested the relationship between staff and resident vaccination rates and the presence of an ILI cluster using 2 approaches. First, we tested the direct effects of continuous measures of staff and resident immunization rates on the likelihood of having an ILI cluster in logistic regression models. Then, we explored the relationship between quartiles of immunization rates and the likelihood of having an ILI cluster. We then developed a method to test the joint effect of staff and resident immunization rates on the likelihood of an ILI cluster. To find the influential immunization rate thresholds, we fit a series of multivariate logistic regression models of the likelihood of the report of an ILI cluster on the staff and resident immunization rates, adjusting for facility characteristics. We established cutpoints, defining resident and staff immunization rates above the cutpoint as “high” and at or below the cutpoint as “low” and arrayed facilities in a plot with quadrants reflecting the following immunization characteristics: high staff/high resident, high staff/low resident, low staff/high resident, and low staff/low resident (see Figure 1). The initial cutpoints were arbitrary; however, we required that each quadrant contain at least 40 facilities to ensure that
The survey was sent to 344 facilities, of which 310 responded (90.1% response rate). Of the facilities that responded, 4 were excluded because they did not report the number of residents vaccinated, 3 were excluded because they did not report the number of staff vaccinated, and 1 was excluded because the number of influenza cases reported was an extreme outlier (n ⫽ 578 influenza cases in a 124-bed facility). The resulting sample size for these analyses was 301 facilities. Table 1 presents some basic descriptive information for each facility overall and then stratified by ILI cluster status of the facility. The average facility had approximately 101 beds (standard deviation [SD]: ⫾ 41 beds), 126 residents (SD: ⫾ 85), and 94 staff (SD: ⫾ 42). The number of residents could reasonably exceed the number of beds during the influenza season because of turnover. The average facility immunization rate for residents was 78.4% (median 84.6). Staff immunization rates were substantially lower with a mean rate of 40.8% (median 37.5%). Most facility characteristics did not differ significantly by ILI cluster status, although larger facilities trended toward being more likely to report an ILI cluster. Only the percentage of the residents with Medicaid significantly differed; facilities with no ILI cluster were more likely
Table 1. Descriptive Characteristics of Nursing Facilities (N ⫽ 301) Facility Characteristics by ILI Cluster Status, Mean (SD) Facility Characteristic Bed size Staff size Residents Residents with Medicaid (%)* Resident immunization rate (%) Staff immunization rate (%) Facilities reporting an ILI cluster (%)
Mean (SD) 100.9 (40.7) 93.6 (41.7) 125.0 (84.5) 71.2 (13.9) 78.4 (20.4) 40.8 (28.7) 33.9
Median 99 88 105 73.8 84.6 37.5 —
Range
ILI Cluster (N ⴝ 102)
34–355 10–340 6–650 0–100 ⬍1–100 0–100 —
102.8 (36.5) 99.9 (40.3) 137.0 (97.3) 68.2 (17.2) 78.1 (19.7) 42.5 (26.5) —
No ILI Cluster (N ⴝ 199) 100.0 (42.8) 90.4 (42.1) 119.8 (76.7) 72.8 (11.7) 78.5 (20.8) 39.9 (29.9) —
ILI, influenza-like illness. * The means for Medicaid status of facility residents by facility ILI cluster status are significantly different (P ⫽ .012). 564 Shugarman et al.
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100.0
Resident Immunization Rates
90.0 80.0 70.0 60.0 50.0 40.0 30.0 20.0 10.0 0.0 0.0
10.0
20.0
Facilities w/ILI Cluster
30.0
40.0
50.0
60.0
70.0
80.0
90.0
100.0
Staff Immunization Rates
Facilities w/No ILI Cluster
Fig. 2. Plot of facilities by resident and staff immunization rates.
Fig. 3. Illustration of influential thresholds associated with reduced likelihood of ILI cluster.
to have a larger proportion of Medicaid-eligible residents. Among the 301 facilities in this sample, 102 (33.9%) reported an ILI cluster. Figure 2 presents a scatter plot of the resident and staff immunization rates. The dark circles reflect facilities that reported an ILI cluster and the open circles represent facilities that did not report an ILI cluster. Table 2 describes the size and scope of ILI clusters in those facilities that reported an ILI cluster. The average ILI cluster included just over 15 residents experiencing influenza-like symptoms. The average number of hospitalizations and deaths were 2.2 and less than 1 per facility, respectively. The hospitalization rate per 100 ILI cases was 13.7; the death rate per 100 ILI cases was 4.5. About one third of all facilities reporting an ILI cluster performed no confirmatory tests of residents with influenza-like symptoms. Of those facilities that performed at least one test (n ⫽ 67), 50 (74.6%) had at least one positive test and 17 (25.4%) had no positive tests. As described above, we tested the association of the direct effects of staff and resident immunization rates as both continuous measures and in quartiles. We estimated models with each immunization rate, both with and without controlling for the other immunization rate, as well as with and without facility characteristics (e.g., bed size, staff size, and percent of residents covered by Medicaid). We found no significant association between these direct effects and the likelihood of an ILI cluster in any of these models (data not shown). Figure 3 presents the same plot of staff and resident immu-
nization rates presented in Figure 2 overlaid by an illustration of an influential threshold of staff and resident immunization rates. We found that facilities that had achieved a staff immunization rate greater than 55% and a resident immunization rate greater than 89% (represented by the shaded region) were significantly less likely to report an ILI cluster than those that had rates less than or equal to these thresholds. Table 3 presents the results of logistic regressions testing the effect of this threshold on the likelihood of having an ILI cluster alone and controlling for facility characteristics. In the unadjusted model, staff and resident immunization rates greater than 55% and 89%, respectively, were almost 60% less likely to experience an ILI cluster than were facilities that had lower immunization rates for either or both of staff and residents (OR: 0.41, 95% CI: 0.19, 0.89). Controlling for facility characteristics further reduced the odds of having an ILI cluster in facilities with high immunization rates in both staff and residents, although the difference between the adjusted and unadjusted models was not substantial. Similar to the descriptive analyses (Table 1), the only facility characteristic that was significant in the multivariate model was whether the facility had Medicaid rates above the median for all facilities. Facilities with an above-median Medicaid rate were half as likely to have an ILI cluster as those with lower percentages of residents on Medicaid. We also tested the facility characteristics in their continuous form and found similar results (data not shown).
Table 2. Characteristics of Facilities With Reported Influenza-Like Illness (ILI) Cluster (N ⫽ 102)
Number of residents in ILI cluster Number of ILI-related hospitalizations Hospitalization rate* Number of ILI-related deaths Death ratea Facilities performing confirmatory tests (%)
Mean (SD)
Median
Range
15.2 (12.7) 2.2 (3.9) 13.7 0.84 (2.4) 4.5 65.7
10.5 0 — 0 — —
3–60 0–23 — 0–14 — —
* Rate reported per 100 ILI cases. ORIGINAL STUDIES
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Table 3. Illustration of Logistic Regression Model Predicting the Likelihood of an ILI Cluster
Resident immunization rate: ⬎89% Staff immunization rate: ⬎55% Bed size† Staff size† % Residents with Medicaid†
Unadjusted OR (95% CI)
Adjusted OR (95% CI)
0.41 (0.19–0.89)*
0.39 (0.17–0.87)*
— — —
0.86 (0.40–1.86) 1.84 (0.86–3.94) 0.50 (0.30–0.84)
ILI, influenza-like cluster; OR, odds ratio; 95% CI, 95% confidence interval. * The odds ratios presented here refer to facilities with the combination of a resident immunization rate greater than 89% and a staff immunization rate greater than 55%. † Indicator variables reflecting facility characteristics greater than the median value of that characteristic.
We evaluated all the possible thresholds, by whole percentages, that met our criterion that at least 40 facilities be included in the comparison groups to ensure we could produce stable estimates. The unadjusted ORs for the thresholds tested ranged from 0.37 (95% CI: 0.16 – 0.87) for staff immunization rates greater than 65% and resident immunization rates greater than 90% to 0.44 (95% CI: 0.20 – 0.95) for staff immunization rates greater than 57% and resident immunization rates greater than 89%. Clearly, higher resident and staff immunization rates had a larger protective effect, although the differences were not substantial between the largest and smallest significant effect. DISCUSSION This study found a strong association between higher rates of both resident and staff influenza immunizations and the reduced likelihood of an ILI cluster in the nursing home. This finding offers new evidence that increasing resident immunization rates alone is not likely to have a significant impact on influenza outbreaks in long-term care facilities. However, the joint effort to increase resident and staff influenza immunization rates can substantially reduce the suffering and death associated with influenza. In nursing facilities, a strong motivating force is the desire to avoid the disruption and despair of many residents and staff being sick at the same time, and many residents dying close together. One third of nursing home facilities in this study experienced an ILI cluster, despite a relatively high median resident influenza immunization rate and a median staff immunization rate in the same range as the national average for health care facilities. The resident immunization rate alone was not a statistically significant predictor of the occurrence of an ILI cluster, given the range of immunization rates in our study. We were unable to validate that immunization of residents had an impact on rates of ILI or ILI-related hospitalizations. Nursing home staff immunization rates also did not, on their own, predict the occurrence of an ILI cluster or influenza-related hospitalizations and deaths. In the only study we identified that tested this same relationship,12 the authors found that staff immunization rates did not influence the likelihood of an outbreak; however, this and other previous studies have indicated an association between higher staff immunization rates and decreased resident influenza-related mortality.12,14,16 566 Shugarman et al.
Although resident and staff immunization rates independently showed no effect on the occurrence of an ILI cluster, our analysis identified an interaction between resident and staff immunization rates. For example, nursing homes with a resident immunization rate greater than 89% and a staff immunization rate greater than 55% were 60% less likely to experience an ILI cluster, compared with nursing homes that did not achieve these rates in both residents and staff. Although previous studies have demonstrated a significant association between facility size and outbreak status,10,18 facility characteristics were generally not informative in the current analysis. However, facilities with a higher proportion of residents on Medicaid were significantly less likely to experience an ILI cluster. The reason for this association probably warrants further consideration. This study demonstrated a significant association between immunization practices and the risk of an ILI cluster despite a poor match between the 2004 –2005 influenza vaccine composition and the prevalent strains circulating in the United States during that season. Influenza A (H3N2) predominated during the 2004 –2005 influenza season. Of the influenza A (H3N2) subtypes that were antigenically characterized by the Centers for Disease Control and Prevention, 78% were A/California/7/2004-like, an antigenically similar component that was not present in the 2004 –2005 influenza vaccine.19 Several factors limit the internal and external validity of this study. The survey was sent to facilities during the summer to collect data on the previous influenza season, introducing the possibility of recall bias. These facilities came from a single nursing home company, and thus the findings may not be generalizable to other facilities. However, we had a very high survey response rate (90.1%) and the facilities were characterized by a wide distribution of bed size and geographic location, reflecting the greater heterogeneity found across all facilities. Facilities reported data on resident and staff immunization rates, ILI cases, hospitalizations, deaths, and laboratory results based on their own data collection mechanisms, which may have differed from facility to facility. Although the cohort limits confidence in generalization, the facilities in a single company will have the advantages of shared information systems, data collection mechanisms, and definitions of staff. Thus, the reporting process across these facilities was likely to be more homogeneous, compared to a randomly selected group of independent facilities or facilities from difJAMDA – November 2006
ferent companies. In addition, we enhanced consistency in reporting by giving respondents a standard definition of an ILI cluster. This project did not address the question of whether family visitors, volunteers, and others who frequent the nursing home environment are also important vectors, and whether their immunization status is important. Finally, this project reported findings in just 1 year, and other years could have differences arising from severity of influenza, matching of influenza type with immunization contents, and other factors. CONCLUSION Influenza outbreaks continue to occur in nursing homes despite high immunization rates of their residents. In this study, only nursing homes with higher rates of both resident and staff immunization saw a significantly reduced risk of experiencing an ILI cluster. These findings suggest that, in addition to achieving a high immunization rate for residents, immunization of health care workers is a necessary part of a strategy to reduce risk of an ILI cluster in nursing homes. Calls for increasing immunization rates in health care workers have been made on the basis that it improves safety and efficacy in health service provision and that health care workers have a legal and ethical duty to get immunized.20 The recent proposal by the Joint Commission on Accreditation of Health Care Organizations to require efforts to ensure immunization of health care workers21 and the educational material provided to long-term care facilities by the Medicare Quality Improvement Community (MedQIC)22 are examples of implementation of this insight. Assuming that it is confirmed in future work, more forceful requirements, or public information about the facility’s rates, might be wise policy. Future research might replicate this study in a larger sample of facilities on a prospective basis, over multiple years, and might also further explore the association of facility characteristics such as the proportion of residents on Medicaid with the likelihood of an influenza outbreak. The authors thank Kelly Sand, Bill Kubat, Keith Krein, and Barbara Baylis for their advice and technical assistance. This study was funded in part by the Centers for Disease Control and Prevention (CDC) (5U01IP000034-02). This manuscript was reviewed and approved of by the CDC. REFERENCES 1. Thompson WW, Shay DK, Weintraub E, et al. Influenza-associated hospitalizations in the United States. JAMA 2004;292(11):1333–1340. 2. Thompson WW, Shay DK, Weintraub E, et al. Mortality associated with influenza and respiratory syncytial virus in the United States. JAMA 2003;289(2):179 –186. 3. Menec VH, MacWilliam L, Aoki FY. Hospitalizations and deaths due to respiratory illnesses during influenza seasons: A comparison of community residents, senior housing residents, and nursing home residents. J Gerontol A Biol Sci Med Sci 2002;57(10):M629 – 635. 4. Harper SA, Fukuda K, Uyeki TM, Cox NJ, Bridges CB. Prevention and control of influenza. Recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep 2005;54(RR-8): 1– 40.
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5. Pearson ML, Bridges CB, Harper SA. Influenza vaccination of healthcare personnel: Recommendations of the Healthcare Infection Control Practices Advisory Committee (HICPAC) and the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep 2006;55(RR2):1–16. 6. Talbot TR, Bradley SE, Cosgrove SE, Ruef C, Siegel JD, Weber DJ. Influenza vaccination of healthcare workers and vaccine allocation for healthcare workers during vaccine shortages. Infect Control Hosp Epidemiol 2005;26(11):882– 890. 7. Department of Health and Human Services, Centers for Medicare and Medicaid Services. 42 CFR Part 483, Medicare and Medicaid Programs: Condition of Participation: Immunization Standard for Long-Term Care Facilities. Federal Register 2005;70(194):58833–58852. 8. Nichol KL, Grimm MB, Peterson DC. Immunizations in long-term care facilities: Policies and practice. J Am Geriatr Soc 1996;44(4):349 – 355. 9. Zadeh MM, Buxton Bridges C, Thompson WW, Arden NH, Fukuda K. Influenza outbreak detection and control measures in nursing homes in the United States. J Am Geriatr Soc 2000;48(10):1310 –1315. 10. Arden N, Monto AS, Ohmit SE. Vaccine use and the risk of outbreaks in a sample of nursing homes during an influenza epidemic. Am J Public Health 1995;85(3):399 – 401. 11. Bardenheier B, Shefer A, McKibben L, Roberts H, Bratzler D. Characteristics of long-term-care facility residents associated with receipt of influenza and pneumococcal vaccinations. Infect Control Hosp Epidemiol 2004;25(11):946 –954. 12. Carman WF, Elder AG, Wallace LA, et al. Effects of influenza vaccination of health-care workers on mortality of elderly people in long-term care: A randomised controlled trial. Lancet 2000;355(9198):93–97. 13. King WD, Woolhandler SJ, Brown AF, et al. BRIEF REPORT: Influenza Vaccination and Health Care Workers in the United States. J Gen Intern Med Jan 20 2006. 14. Potter J, Stott DJ, Roberts MA, et al. Influenza vaccination of health care workers in long-term-care hospitals reduces the mortality of elderly patients. J Infect Dis 1997;175(1):1– 6. 15. Bridges CB, Thompson WW, Meltzer MI, et al. Effectiveness and costbenefit of influenza vaccination of healthy working adults: A randomized controlled trial. JAMA 2000;284(13):1655–1663. 16. Jefferson T, Rivetti D, Rivetti A, Rudin M, Di Pietrantonj C, Demicheli V. Efficacy and effectiveness of influenza vaccines in elderly people: A systematic review. Lancet 2005;366(9492):1165–1174. 17. Drinka PJ, Gravenstein S, Krause P, Schilling M, Miller BA, Shult P. Outbreaks of influenza A and B in a highly immunized nursing home population. J Fam Pract 1997;45(6):509 –514. 18. Patriarca PA, Weber JA, Parker RA, et al. Risk factors for outbreaks of influenza in nursing homes. A case-control study. Am J Epidemiol 1986;124(1):114 –119. 19. Update: Influenza activity—United States and worldwide, 2004 – 05 season. MMWR Morb Mortal Wkly Rep 2005;54(25):631– 634. 20. Poland GA, Tosh P, Jacobson RM. Requiring influenza vaccination for health care workers: seven truths we must accept. Vaccine 2005;23(17– 18):2251–2255. 21. Joint Commission on Accreditation of Healthcare Organizations. Proposed Standards for Immunization of Staff, Students, Volunteers, and Licensed Independent Practitioners Against Influenza. Available at: http://www.jointcommission.org/NR/rdonlyres/3207FFDF-C540-40FD8901-55AEFD764F03/0/influenza_immunization_stds_fr.pdf. Accessed March 27, 2006. 22. Medicare Quality Improvement Community (MedQIC). Immunizations Toolkit. Available at: http://www.medqic.org/dcs/ContentServer?cid⫽ 1105558764854&pagename⫽Medqic%2FMQTools%2FToolTemplate& parentName⫽Topic&c⫽MQTools. Accessed March 23, 2006.
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