Abstract
Influenza illness may impact the risk of falls and fractures during acute illness due to unsteady gait or dizziness. We evaluated the association between influenza and hip fracture hospitalizations in long-stay (LS) nursing home (NH) residents.
We analyzed weekly rates of hospitalization in a retrospective cohort of LS NH residents between January 1, 2000 to December 31, 2009. Hip fracture and influenza like illness (ILI) hospitalizations were identified with Medicare fee-for-service part A claims. We evaluated unadjusted and adjusted models with the primary exposures, weekly rate of influenza-like illness hospitalizations, city-wide mortality, and NH influenza vaccination rate and primary outcome of weekly rate of hip fracture hospitalizations.
There were 9,237 incident hip fractures in the cohort. Facility wide ILI hospitalization rate was associated with the hip fracture hospitalization rate in the unadjusted (incidence rate ratio [IRR] 1.13, 95% confidence interval [CI]: 1.08, 1.17) and adjusted (IRR 1.13, 95% CI: 1.09, 1.18) analyses. City-wide influenza mortality was associated with hip fracture hospitalization rates for the unadjusted (IRR 1.03, 95% CI: 1.02, 1.04), and adjusted (IRR 1.02, 95% CI: 1.01, 1.03) analyses. NH influenza vaccination rates were not associated with changes in hip fracture hospitalization rates.
ILI hospitalizations are associated with a 13% average increase in hip fracture hospitalization risk. In a given NH week, an increase in the number ILI hospitalizations from none to two was associated with an approximate one percentage point increase in hip fracture hospitalization risk. Strategies to reduce influenza risk should be investigated to reduce hip fracture risk.
Hip fractures occur commonly (2.3 per 100-person years) in U.S. nursing homes (NH) (1). These significantly debilitating events lead to rehospitalization, functional decline, and among NH residents, a 36% risk of mortality within 6 months (2). Falls are the most common event causing hip fracture (3). Understanding factors associated with falls and hip fracture in the NH setting is important in order to inform policies aimed at tracking and preventing these devastating outcomes (4).
Influenza illness is associated with serious sequelae in NH residents, and it is possible that it contributes to fall risk. Influenza is estimated to result in an average 94,000 primary hospitalizations and 22,000–51,000 deaths annually (5–8). The symptoms of influenza illness may include severe neurologic complications such as delirium (9). Individuals may also have poor appetites in the acute illness phase leading to dehydration. This confluence of symptoms could lead to an increased risk of falling. Thus, we hypothesize acute influenza illness may represent a time of heightened risk of hip fractures for NH residents. Preventing influenza through vaccination is paramount in NHs and other congregate care environments as the course of the illness is particularly severe for the elderly with comorbid disease and is associated with increased risk of hospitalization and mortality (6,10). If influenza was associated with increased risk of hip fracture, vaccination against influenza, especially higher potency doses for older individuals, could potentially mitigate the risk of falls and hip fractures.
To our knowledge, no previous studies have examined the association between influenza illness and fracture. Therefore, our primary objective was to investigate the relationship between incident of hip fracture hospitalizations among long-stay (LS) NH residents and influenza-like illness hospitalizations. We also explored two secondary objectives: (i) To examine the variation in hip fracture rates by the residential city-wide influenza mortality rates reported by the CDC, and (ii) To identify associations between NH influenza vaccination rates and hip fracture hospitalizations.
Methods
Study Design
This study is a retrospective cohort design which analyzed weekly rates of hospitalization in NH located in one of the 122 Centers for Disease Control (122-CDC) cities in which influenza morbidity and mortality is carefully monitored. The cohort included LS NH residents enrolled in a fee-for-service Medicare program between January 1, 2000 to December 31, 2009. We constructed the cohort using a 100% sample of NH resident Medicare Part A claims (administrative claims which provide information related to hospitalization and inpatient services) linked with the Online Survey, Certification and Reporting (OSCAR) data for the facility and NH minimum data assessments (11). Only LS residents, defined as those with ≥ 100 days in the same nursing facility with no more than 10 consecutive days outside the facility, were included for analysis. The index date for each stay was the 100th day from NH admission (beginning of “long-stay”). Long stays occurring from January 1, 2000 to December 31, 2009 were included. Patients were excluded if they had (i) less than 6 months of continuous enrollment in Medicare Part A, (ii) enrolled in Medicare Advantage, or (iii) a claim for Hospice. The cohort was limited to the 122-CDC cities for which influenza mortality data were available (12). For each facility, a running count of the weekly number of LS residents, their rates of hip fractures, influenza hospitalizations and city-wide influenza deaths was determined from January 1, 2000 through December 31, 2009. Since some NHs had smaller LS populations with few events, NH were only included in the study if they operated continuously during the study period and had ≥50 LS residents for the duration of the study. A sensitivity analysis of the LS resident cutoff (no restriction, ≥75 or ≥100 every week) did not substantially change the results. However, a cutoff of 50 residents was selected to ensure a stable weekly rate of ILI or fracture hospitalization for most facilities. Our study was approved by the Brown University Institutional Review Board.
Measures
Hip fracture hospitalizations were identified as any primary or secondary International Classification of Diseases, 9th edition (ICD-9) diagnosis of 820.xx with or without an accompanying procedural code using Medicare Part A administrative claims (13). To avoid duplicate claims for the same fracture, hip fracture hospitalizations were not counted if a fracture occurred in the previous 100 days. An influenza like illness (ILI) hospitalization was defined as any primary or secondary ICD-9 diagnosis of 480.xx-487.xx. Following prior published work, we used hospitalizations due to influenza-like illness and pneumonia (480–487) to assess influenza severity and burden (5–8). Because the identification of influenza in individual patients is problematic without prospective laboratory testing and health evaluations, we used the CDC 122 U.S. cities data set which reports weekly counts for pneumonia and influenza deaths as a marker of city-wide influenza morbidity in which NH facilities reside (12). The CDC 122-cities mortality data is derived from vital statistics and causes of death certificates (12). Finally we ascertained the percent of residents vaccinated for influenza using the Online Survey of Certification And Reporting (OSCAR). OSCAR compiles facility level characteristics as collected by state surveyors for the purpose of certifying facilities in Medicare and Medicaid programs, and it is completed approximately every 12–18 months. For each facility week, the vaccination rate was determined by ascertaining the nearest OSCAR survey to the index week starting with the preceding week. Facilities were then divided by an influenza vaccination rate above and below 65% (the approximate median rounded to nearest 5%) with exclusion of any facility with a reported vaccination rate >100% or <15% (as implausible values). A sensitivity analysis of the vaccination rate criteria did not show significant differences by cutoff.
Statistical Analysis
The primary outcome was the weekly rate of hip fractures evaluated at the facility level in a generalized estimating equation. To adjust for potential confounding, facility level aggregated statistics from the OSCAR survey on immunizations, pharmacologic treatment, comorbid illness, and staffing were included. Individual age and gender were obtained from Medicare claim files for the eligible population and aggregated to facility. These variables were tested for inclusion in a multivariable analysis according to a backward stepwise selection strategy that required an alpha level of ≤0.1 or which substantive knowledge suggests are relevant (eg, influenza vaccination). The final adjusted model of hip fracture rates included age, sex, the total number of residents in a facility (long and short stay), percent of residents vaccinated for influenza, percent of residents with rehabilitation, ostomy, on dialysis or diagnosed with dementia, and the number of full time nursing employees per 100 residents. To account for temporal trends in hip fracture incidence, we included year as a predictor (ie, year fixed effects). Standard error calculations were adjusted for autocorrelation and within facility clustering using generalized estimating equations with robust standard errors and an exchangeable correlation matrix using the facility as the grouping variable. The primary outcome (hip fracture rate) was modeled as a Poisson distribution with a log link function which included a log offset for the number of facility LS residents per week. We modeled influenza-like illness hospitalization, city-wide mortality, and facility influenza vaccination rate as the exposure in unadjusted and multivariable adjusted models. For interpretation, the average marginal effect of increasing ILI hospitalizations from 0 to 2 per facility-week on hip fracture hospitalizations was computed, holding other covariates at their means. To adjust for differences in NHs not captured by OSCAR variables, a sensitivity analysis separately undertook a fixed effects analysis including dummy variables for each facility (or city fixed-effect for the city influenza measure) and year. A two-sided α < 0.05 was used for assessing statistical significance of the observed relationship. Analyses were performed using SAS® statistical software (version 9.4; SAS Institute Inc., Cary, NC) and STATA SE 14 (College Station, TX).
Results
Approximately 17.6 million NH residents enrolled in Medicare were evaluated with 3,750,980 LS residents evaluated for analysis. The cohort restricted to 122 cities included 624,217 LS residents across 2,923 facilities, 17% of the total LS NH population in the United States. After excluding facilities with less than 50 residents and incomplete data from 2000 to 2009, the final panel data set of weekly hospitalization rates included 455 NH with 226,814 unique residents (with one more NH excluded in the adjusted analysis for lack of OSCAR survey data). The residents were on average 79 years, 65% were women, and they accrued a mean follow-up time of 1.8 years per resident.
We identified 8,549 (1.7%) hip fractures and 50,938 (10.4%) ILI hospitalizations among 489,907 LS resident-years. The overall annual proportion of residents with a hip fracture hospitalization declined over time from 2.2% in 2000 to 1.6% in 2009 (14,15). Overall, we observed that influenza hospitalizations and hip fracture hospitalizations fluctuated, but both had a similar proportional increase during the winter months of December, January, and February (see Figure 1). The overall number of NH residents per facility also declined during this time (Table 1).
![Seasonal variation in hospitalizations due to influenza-like-illness (ILI) and hip fractures (2000–2009). The following figure reports the weekly risk of ILI or hip fracture hospitalization for an individual (incidence rate [IR] % per facility-week). The values are averaged across all years and plotted by month. The codes 480× and 820× refer to hospitalization billings claims for the relevant diagnoses (ILI, hip fracture).](https://oup.silverchair-cdn.com/oup/backfile/Content_public/Journal/biomedgerontology/73/12/10.1093_gerona_glx200/1/m_glx20001.jpeg?Expires=1750723534&Signature=VYRthOuO~0j4noB4U96cEaC1OUMbtc1ue89Nf3rWeQeuujL5c4QNdaHv8ps6svSLKGM3ZEveXlbKQUO5eNCQBSRDoPsDw~T1lIoJua8m2wAtwzZz9BRVWRDQyTJ5My2WZLqBnZcl55pP0koDyRJ0mDcO5xPe45vnD6Wr0PfcYlFdEOOeCU6rovIreaec3c95mcSxnZsbbGjI-KP3TZhFZBzN7o-KUfpJnmak3Cbf4ed4Imz7U4441JBh2G~PaBizfJY53Fs0XPSLIZ7jedglgqKZ~xGHrkQHA3ULi1yXxMLEQfdR0P7iu4zxHQMhHf~rDUj3svJoxTqpjrOhObTP2A__&Key-Pair-Id=APKAIE5G5CRDK6RD3PGA)
Seasonal variation in hospitalizations due to influenza-like-illness (ILI) and hip fractures (2000–2009). The following figure reports the weekly risk of ILI or hip fracture hospitalization for an individual (incidence rate [IR] % per facility-week). The values are averaged across all years and plotted by month. The codes 480× and 820× refer to hospitalization billings claims for the relevant diagnoses (ILI, hip fracture).
Distribution of Hip Fracture and P&I Hospitalizations Stratified by Calendar Year Among U.S. Long-stay Nursing Home Residents, Aged >65 y old with Medicare fee-for-service, 2000–2009
| Year | LS Person- years, Number | Hip Fracture Hosp., Number (%) | P&I Hosp., Number (%) | City P&I Mortality, per 100,000 Persons |
|---|---|---|---|---|
| 2000 | 54,232 | 1,199 (2.2) | 5,590 (10.3) | 119.5 |
| 2001 | 52,334 | 970 (1.9) | 5,371 (10.3) | 111.0 |
| 2002 | 50,830 | 1,003 (2.0) | 5,372 (10.6) | 109.6 |
| 2003 | 49,606 | 903 (1.8) | 5,253 (10.6) | 107.2 |
| 2004 | 48,459 | 798 (1.6) | 4,791 (9.9) | 105.7 |
| 2005 | 47,762 | 831 (1.7) | 5,100 (10.7) | 110.3 |
| 2006 | 47,371 | 736 (1.6) | 4,645 (9.8) | 97.2 |
| 2007 | 46,782 | 715 (1.5) | 4,817 (10.3) | 95.7 |
| 2008 | 46,161 | 652 (1.4) | 5,096 (11.0) | 107.7 |
| 2009 | 46,370 | 742 (1.6) | 4,948 (10.7) | 102.1 |
| Total | 489,907 | 8,549 (1.7) | 50,983 (10.4) |
| Year | LS Person- years, Number | Hip Fracture Hosp., Number (%) | P&I Hosp., Number (%) | City P&I Mortality, per 100,000 Persons |
|---|---|---|---|---|
| 2000 | 54,232 | 1,199 (2.2) | 5,590 (10.3) | 119.5 |
| 2001 | 52,334 | 970 (1.9) | 5,371 (10.3) | 111.0 |
| 2002 | 50,830 | 1,003 (2.0) | 5,372 (10.6) | 109.6 |
| 2003 | 49,606 | 903 (1.8) | 5,253 (10.6) | 107.2 |
| 2004 | 48,459 | 798 (1.6) | 4,791 (9.9) | 105.7 |
| 2005 | 47,762 | 831 (1.7) | 5,100 (10.7) | 110.3 |
| 2006 | 47,371 | 736 (1.6) | 4,645 (9.8) | 97.2 |
| 2007 | 46,782 | 715 (1.5) | 4,817 (10.3) | 95.7 |
| 2008 | 46,161 | 652 (1.4) | 5,096 (11.0) | 107.7 |
| 2009 | 46,370 | 742 (1.6) | 4,948 (10.7) | 102.1 |
| Total | 489,907 | 8,549 (1.7) | 50,983 (10.4) |
Note: LS = Long-stay; P&I = Pneumonia and influenza; Hosp. = Hospitalization Includes nursing homes for the Centers for Disease Control and Prevention (CDC) 122-cities. LS person-years is a summary measure to describe the total resident time in the nursing home for each year (ie, All the residents and their residence time in 2000 is equivalent to 54,232 residents each with a 1-y length of stay).
Distribution of Hip Fracture and P&I Hospitalizations Stratified by Calendar Year Among U.S. Long-stay Nursing Home Residents, Aged >65 y old with Medicare fee-for-service, 2000–2009
| Year | LS Person- years, Number | Hip Fracture Hosp., Number (%) | P&I Hosp., Number (%) | City P&I Mortality, per 100,000 Persons |
|---|---|---|---|---|
| 2000 | 54,232 | 1,199 (2.2) | 5,590 (10.3) | 119.5 |
| 2001 | 52,334 | 970 (1.9) | 5,371 (10.3) | 111.0 |
| 2002 | 50,830 | 1,003 (2.0) | 5,372 (10.6) | 109.6 |
| 2003 | 49,606 | 903 (1.8) | 5,253 (10.6) | 107.2 |
| 2004 | 48,459 | 798 (1.6) | 4,791 (9.9) | 105.7 |
| 2005 | 47,762 | 831 (1.7) | 5,100 (10.7) | 110.3 |
| 2006 | 47,371 | 736 (1.6) | 4,645 (9.8) | 97.2 |
| 2007 | 46,782 | 715 (1.5) | 4,817 (10.3) | 95.7 |
| 2008 | 46,161 | 652 (1.4) | 5,096 (11.0) | 107.7 |
| 2009 | 46,370 | 742 (1.6) | 4,948 (10.7) | 102.1 |
| Total | 489,907 | 8,549 (1.7) | 50,983 (10.4) |
| Year | LS Person- years, Number | Hip Fracture Hosp., Number (%) | P&I Hosp., Number (%) | City P&I Mortality, per 100,000 Persons |
|---|---|---|---|---|
| 2000 | 54,232 | 1,199 (2.2) | 5,590 (10.3) | 119.5 |
| 2001 | 52,334 | 970 (1.9) | 5,371 (10.3) | 111.0 |
| 2002 | 50,830 | 1,003 (2.0) | 5,372 (10.6) | 109.6 |
| 2003 | 49,606 | 903 (1.8) | 5,253 (10.6) | 107.2 |
| 2004 | 48,459 | 798 (1.6) | 4,791 (9.9) | 105.7 |
| 2005 | 47,762 | 831 (1.7) | 5,100 (10.7) | 110.3 |
| 2006 | 47,371 | 736 (1.6) | 4,645 (9.8) | 97.2 |
| 2007 | 46,782 | 715 (1.5) | 4,817 (10.3) | 95.7 |
| 2008 | 46,161 | 652 (1.4) | 5,096 (11.0) | 107.7 |
| 2009 | 46,370 | 742 (1.6) | 4,948 (10.7) | 102.1 |
| Total | 489,907 | 8,549 (1.7) | 50,983 (10.4) |
Note: LS = Long-stay; P&I = Pneumonia and influenza; Hosp. = Hospitalization Includes nursing homes for the Centers for Disease Control and Prevention (CDC) 122-cities. LS person-years is a summary measure to describe the total resident time in the nursing home for each year (ie, All the residents and their residence time in 2000 is equivalent to 54,232 residents each with a 1-y length of stay).
The acuity of residents residing in NH facilities increased over time, including the percent on dialysis, undergoing rehabilitation, diagnosed with depression and dementia, and the percent receiving medications such as antibiotics, antianxiety and antidepressants (Table 2). The percent of residents vaccinated against influenza increased from 59.2% to 69.8% from 2000 to 2009.
Nursing Home Characteristics Over Time (n = 455 facilities, 2000–2009)
| Year | Total Residents | Antibiotics | Infl. Vacc. | Antianxiety | Antidepressants | Restraints | Rehab. | Dialysis | Dementia | Overall Ulcer Frequency >10% | Nursing FTE/100 Residents |
|---|---|---|---|---|---|---|---|---|---|---|---|
| 2000 | 202 | 6.2 | 59.2 | 6.8 | 15.9 | 10.2 | 12.8 | 1.4 | 43.1 | 25.3 | 18.1 |
| 2001 | 200 | 6.2 | 62.6 | 6.8 | 17.0 | 9.7 | 12.6 | 1.4 | 44.3 | 28.2 | 17.8 |
| 2002 | 200 | 6.6 | 63.6 | 6.8 | 18.0 | 9.1 | 13.5 | 1.6 | 44.4 | 26.9 | 18.0 |
| 2003 | 200 | 6.8 | 64.3 | 6.9 | 19.3 | 7.9 | 15.0 | 1.8 | 44.9 | 22.2 | 18.3 |
| 2004 | 200 | 6.8 | 63.4 | 7.1 | 20.3 | 7.1 | 15.9 | 1.9 | 45.8 | 24.7 | 18.7 |
| 2005 | 199 | 6.5 | 63.5 | 7.3 | 21.1 | 6.7 | 16.4 | 2.0 | 46.9 | 25.3 | 18.9 |
| 2006 | 199 | 6.6 | 65.9 | 7.5 | 21.7 | 6.5 | 17.4 | 2.0 | 46.8 | 24.9 | 19.1 |
| 2007 | 198 | 6.8 | 68.5 | 7.8 | 22.2 | 5.6 | 18.8 | 2.1 | 46.9 | 22.0 | 19.4 |
| 2008 | 196 | 6.8 | 68.7 | 8.3 | 22.3 | 4.6 | 19.4 | 2.1 | 46.8 | 21.6 | 19.9 |
| 2009 | 195 | 6.7 | 69.8 | 8.7 | 22.3 | 3.9 | 20.3 | 2.2 | 46.7 | 15.4 | 20.6 |
| Year | Total Residents | Antibiotics | Infl. Vacc. | Antianxiety | Antidepressants | Restraints | Rehab. | Dialysis | Dementia | Overall Ulcer Frequency >10% | Nursing FTE/100 Residents |
|---|---|---|---|---|---|---|---|---|---|---|---|
| 2000 | 202 | 6.2 | 59.2 | 6.8 | 15.9 | 10.2 | 12.8 | 1.4 | 43.1 | 25.3 | 18.1 |
| 2001 | 200 | 6.2 | 62.6 | 6.8 | 17.0 | 9.7 | 12.6 | 1.4 | 44.3 | 28.2 | 17.8 |
| 2002 | 200 | 6.6 | 63.6 | 6.8 | 18.0 | 9.1 | 13.5 | 1.6 | 44.4 | 26.9 | 18.0 |
| 2003 | 200 | 6.8 | 64.3 | 6.9 | 19.3 | 7.9 | 15.0 | 1.8 | 44.9 | 22.2 | 18.3 |
| 2004 | 200 | 6.8 | 63.4 | 7.1 | 20.3 | 7.1 | 15.9 | 1.9 | 45.8 | 24.7 | 18.7 |
| 2005 | 199 | 6.5 | 63.5 | 7.3 | 21.1 | 6.7 | 16.4 | 2.0 | 46.9 | 25.3 | 18.9 |
| 2006 | 199 | 6.6 | 65.9 | 7.5 | 21.7 | 6.5 | 17.4 | 2.0 | 46.8 | 24.9 | 19.1 |
| 2007 | 198 | 6.8 | 68.5 | 7.8 | 22.2 | 5.6 | 18.8 | 2.1 | 46.9 | 22.0 | 19.4 |
| 2008 | 196 | 6.8 | 68.7 | 8.3 | 22.3 | 4.6 | 19.4 | 2.1 | 46.8 | 21.6 | 19.9 |
| 2009 | 195 | 6.7 | 69.8 | 8.7 | 22.3 | 3.9 | 20.3 | 2.2 | 46.7 | 15.4 | 20.6 |
Note: Data from the OSCAR surveys. Each facility reports the % of residents with certain conditions, medications. Each cell corresponds to the mean reported value (eg, % of residents) across all facilities, ulcer frequency is the % of facilities with >10% ulcer rate. FTE = Full time employee; Infl. Vacc. = Influenza vaccination rate; Rehab. = Patients undergoing rehabilitation care.
Data not shown but evaluated in models: % with ostomy, % with depression, other FTE’s/100 residents (physicians etc.)
Nursing Home Characteristics Over Time (n = 455 facilities, 2000–2009)
| Year | Total Residents | Antibiotics | Infl. Vacc. | Antianxiety | Antidepressants | Restraints | Rehab. | Dialysis | Dementia | Overall Ulcer Frequency >10% | Nursing FTE/100 Residents |
|---|---|---|---|---|---|---|---|---|---|---|---|
| 2000 | 202 | 6.2 | 59.2 | 6.8 | 15.9 | 10.2 | 12.8 | 1.4 | 43.1 | 25.3 | 18.1 |
| 2001 | 200 | 6.2 | 62.6 | 6.8 | 17.0 | 9.7 | 12.6 | 1.4 | 44.3 | 28.2 | 17.8 |
| 2002 | 200 | 6.6 | 63.6 | 6.8 | 18.0 | 9.1 | 13.5 | 1.6 | 44.4 | 26.9 | 18.0 |
| 2003 | 200 | 6.8 | 64.3 | 6.9 | 19.3 | 7.9 | 15.0 | 1.8 | 44.9 | 22.2 | 18.3 |
| 2004 | 200 | 6.8 | 63.4 | 7.1 | 20.3 | 7.1 | 15.9 | 1.9 | 45.8 | 24.7 | 18.7 |
| 2005 | 199 | 6.5 | 63.5 | 7.3 | 21.1 | 6.7 | 16.4 | 2.0 | 46.9 | 25.3 | 18.9 |
| 2006 | 199 | 6.6 | 65.9 | 7.5 | 21.7 | 6.5 | 17.4 | 2.0 | 46.8 | 24.9 | 19.1 |
| 2007 | 198 | 6.8 | 68.5 | 7.8 | 22.2 | 5.6 | 18.8 | 2.1 | 46.9 | 22.0 | 19.4 |
| 2008 | 196 | 6.8 | 68.7 | 8.3 | 22.3 | 4.6 | 19.4 | 2.1 | 46.8 | 21.6 | 19.9 |
| 2009 | 195 | 6.7 | 69.8 | 8.7 | 22.3 | 3.9 | 20.3 | 2.2 | 46.7 | 15.4 | 20.6 |
| Year | Total Residents | Antibiotics | Infl. Vacc. | Antianxiety | Antidepressants | Restraints | Rehab. | Dialysis | Dementia | Overall Ulcer Frequency >10% | Nursing FTE/100 Residents |
|---|---|---|---|---|---|---|---|---|---|---|---|
| 2000 | 202 | 6.2 | 59.2 | 6.8 | 15.9 | 10.2 | 12.8 | 1.4 | 43.1 | 25.3 | 18.1 |
| 2001 | 200 | 6.2 | 62.6 | 6.8 | 17.0 | 9.7 | 12.6 | 1.4 | 44.3 | 28.2 | 17.8 |
| 2002 | 200 | 6.6 | 63.6 | 6.8 | 18.0 | 9.1 | 13.5 | 1.6 | 44.4 | 26.9 | 18.0 |
| 2003 | 200 | 6.8 | 64.3 | 6.9 | 19.3 | 7.9 | 15.0 | 1.8 | 44.9 | 22.2 | 18.3 |
| 2004 | 200 | 6.8 | 63.4 | 7.1 | 20.3 | 7.1 | 15.9 | 1.9 | 45.8 | 24.7 | 18.7 |
| 2005 | 199 | 6.5 | 63.5 | 7.3 | 21.1 | 6.7 | 16.4 | 2.0 | 46.9 | 25.3 | 18.9 |
| 2006 | 199 | 6.6 | 65.9 | 7.5 | 21.7 | 6.5 | 17.4 | 2.0 | 46.8 | 24.9 | 19.1 |
| 2007 | 198 | 6.8 | 68.5 | 7.8 | 22.2 | 5.6 | 18.8 | 2.1 | 46.9 | 22.0 | 19.4 |
| 2008 | 196 | 6.8 | 68.7 | 8.3 | 22.3 | 4.6 | 19.4 | 2.1 | 46.8 | 21.6 | 19.9 |
| 2009 | 195 | 6.7 | 69.8 | 8.7 | 22.3 | 3.9 | 20.3 | 2.2 | 46.7 | 15.4 | 20.6 |
Note: Data from the OSCAR surveys. Each facility reports the % of residents with certain conditions, medications. Each cell corresponds to the mean reported value (eg, % of residents) across all facilities, ulcer frequency is the % of facilities with >10% ulcer rate. FTE = Full time employee; Infl. Vacc. = Influenza vaccination rate; Rehab. = Patients undergoing rehabilitation care.
Data not shown but evaluated in models: % with ostomy, % with depression, other FTE’s/100 residents (physicians etc.)
The primary and secondary outcomes are summarized in Table 3. The mean number of hip fracture hospitalizations and ILI hospitalizations per facility-week was 0.04 and 0.22, respectively. Influenza hospitalizations were associated with hip fracture hospitalizations in the unadjusted (incidence rate ratio [IRR] 1.12, 95% confidence interval [CI]: 1.08, 1.18), adjusted (IRR 1.13, 95% CI: 1.08, 1.17) and fixed effects analysis (IRR 1.13, 95% CI: 1.08, 1.18). An increase in the number of ILI hospitalizations per week from none to two was associated with an increased mean number of hip fracture hospitalizations per week from 0.03 to 0.04 (approximate 1 percentage-point increase). City-wide deaths due to influenza and pneumonia were also associated with a small increase in hip fracture hospitalization rates for the unadjusted (IRR 1.03, 95% CI: 1.01–1.04), and adjusted analysis (IRR 1.02, 95% CI: 1.01, 1.03) but not fixed-effects analysis (IRR 1.00, 95% CI: 0.99, 1.02).
of Influenza Hospitalization Versus None on the Occurrence of Hip Fracture Hospitalizations Among U.S. Long-stay Nursing Home Residents ≥65 years old Under a Series of Models, 2000–2009
| Model | Incidence Rate Ratioa (95% CI) | ||||
|---|---|---|---|---|---|
| Nb (facility) | Nb (facility by week) | Unadjusted | Adjusted | Fixed-Effects | |
| Influenza hospitalizations | 454 | 208,412 | 1.12 (1.08–1.18) | 1.13 (1.08–1.17) | 1.13 (1.08–1.18) |
| City-wide influenza mortality | 454 | 195,653c | 1.03 (1.01–1.04) | 1.02 (1.01–1.03) | 1.00 (0.99–1.02) |
| Influenza vaccination rate ≥ 65% | 454 | 208,412 | 0.98 (0.93–1.04) | 0.98 (0.92–1.04) | 0.99 (0.92–1.06) |
| Model | Incidence Rate Ratioa (95% CI) | ||||
|---|---|---|---|---|---|
| Nb (facility) | Nb (facility by week) | Unadjusted | Adjusted | Fixed-Effects | |
| Influenza hospitalizations | 454 | 208,412 | 1.12 (1.08–1.18) | 1.13 (1.08–1.17) | 1.13 (1.08–1.18) |
| City-wide influenza mortality | 454 | 195,653c | 1.03 (1.01–1.04) | 1.02 (1.01–1.03) | 1.00 (0.99–1.02) |
| Influenza vaccination rate ≥ 65% | 454 | 208,412 | 0.98 (0.93–1.04) | 0.98 (0.92–1.04) | 0.99 (0.92–1.06) |
Note: Interpretable as a relative change (ie, 1.2, 20%).
Sample used in adjusted analysis
City-wide influenza death rate was missing for 6% of sample.
Covariate adjusted includes: Year fixed effects, resident gender, age, facility antibiotic use, influenza vaccination, percent of residents with rehabilitation, ostomy, or dialysis care, the percent of residents diagnosed with depression and dementia, and the no of nursing FTE per 100 residents.
Fixed effects includes fixed effect terms for each year and facility without adjustment for any specific covariate.
of Influenza Hospitalization Versus None on the Occurrence of Hip Fracture Hospitalizations Among U.S. Long-stay Nursing Home Residents ≥65 years old Under a Series of Models, 2000–2009
| Model | Incidence Rate Ratioa (95% CI) | ||||
|---|---|---|---|---|---|
| Nb (facility) | Nb (facility by week) | Unadjusted | Adjusted | Fixed-Effects | |
| Influenza hospitalizations | 454 | 208,412 | 1.12 (1.08–1.18) | 1.13 (1.08–1.17) | 1.13 (1.08–1.18) |
| City-wide influenza mortality | 454 | 195,653c | 1.03 (1.01–1.04) | 1.02 (1.01–1.03) | 1.00 (0.99–1.02) |
| Influenza vaccination rate ≥ 65% | 454 | 208,412 | 0.98 (0.93–1.04) | 0.98 (0.92–1.04) | 0.99 (0.92–1.06) |
| Model | Incidence Rate Ratioa (95% CI) | ||||
|---|---|---|---|---|---|
| Nb (facility) | Nb (facility by week) | Unadjusted | Adjusted | Fixed-Effects | |
| Influenza hospitalizations | 454 | 208,412 | 1.12 (1.08–1.18) | 1.13 (1.08–1.17) | 1.13 (1.08–1.18) |
| City-wide influenza mortality | 454 | 195,653c | 1.03 (1.01–1.04) | 1.02 (1.01–1.03) | 1.00 (0.99–1.02) |
| Influenza vaccination rate ≥ 65% | 454 | 208,412 | 0.98 (0.93–1.04) | 0.98 (0.92–1.04) | 0.99 (0.92–1.06) |
Note: Interpretable as a relative change (ie, 1.2, 20%).
Sample used in adjusted analysis
City-wide influenza death rate was missing for 6% of sample.
Covariate adjusted includes: Year fixed effects, resident gender, age, facility antibiotic use, influenza vaccination, percent of residents with rehabilitation, ostomy, or dialysis care, the percent of residents diagnosed with depression and dementia, and the no of nursing FTE per 100 residents.
Fixed effects includes fixed effect terms for each year and facility without adjustment for any specific covariate.
An influenza vaccination rate ≥65% was not associated with hip fracture hospitalization rates for the unadjusted (IRR 0.98, 95% CI: 0.93, 1.04), adjusted (IRR 0.98, 95% CI: 0.92, 1.04) or fixed effects analysis (IRR 0.99, 95% CI: 0.93, 1.06).
Discussion
This cohort study sought to determine if weekly hospitalization rates for ILI were associated with weekly hip fracture hospitalization in NHs. We observed a statistically significant positive association between influenza hospitalizations and hip fractures. An increase in the number of NH ILI hospitalizations per week from none to two was associated with an approximate one percentage point increase in the number of hip fracture hospitalizations per week.
Previous studies of morbidity and mortality due to influenza have primarily focused on respiratory disease health outcomes (5,6,9). However, nonrespiratory adverse health consequences of influenza have also been identified including: acute myocardial infarction (AMI) and congestive heart failure exacerbations (16–18). We observed a significant association between influenza hospitalizations and hip fracture hospitalizations after accounting for the number of LS residents, facility characteristics, and other quality markers. City-wide deaths due to influenza were also associated with an increase in hip fracture hospitalizations but not in models adjusted for differences in city, facility. Our findings are consistent with a recent study that found an 26% increased risk of fracture following weeks with high influenza infection burden (19). If influenza does increase risk of hip fracture then vaccination against influenza could ameliorate risk, and there remains room for improvement in NH vaccination rates (20). However, we did not observe a lower incidence of hip fracture in facilities with high vaccination rates. Vaccination rates were determined through the OSCAR survey and were only updated approximately annually. A more precise measurement of vaccination status in individuals may help evaluate its effectiveness in preventing hip fractures (if a true causal relationship exists). The association between influenza and hip fractures could be due to a heightened risk for falls among residents with symptomatic influenza. Another possible explanation is that influenza illness in one patient or group of patients necessitates greater nursing care and attention which leads to decreased monitoring for another group of patients at risk for falls. We recommend caution in interpreting our findings in a causal framework: we evaluated weekly rates of hip and ILI hospitalizations, without accounting for which event occurred first in an individual patient. It is also possible that hip fracture may predispose to influenza infection due to debilitation and exposure to nosocomial infections (21).
Our definition of influenza is based on Medicare claims, and it could include many hospitalizations not actually due to influenza viral illness. Definitions which include laboratory-confirmed influenza illness or definitively timing illness events would better account for these limitations. Although not statistically significant, we observed a similar trend for city-wide ILI mortality suggesting that our definition of influenza hospitalization is reflective of influenza disease. Second, although models were adjusted for age, gender, % with dementia, % undergoing rehabilitation, nursing resources, and evaluated medication use (antipsychotics and antidepressants), we did not have a precise measure of functional status or severity of illness, and it remains possible that these factors in part explain our findings. Additionally, our findings are limited to NH with >50 LS residents in 122 U.S. cities from 2000 to 2009 due to datasource limitations, and may not be generalizable to more recent years and all locations.
We view our findings as important to highlight the potential for influenza illness as a contributor to increased hip fracture risk. Although the incidence ratios were modest, NHs are a reservoir for influenza illness during the winter, such that the absolute number of hip fractures associated with influenza in the United States is substantial but this analysis still represents a substantial percentage (6%) of all LS NH residents. A longitudinal cohort analysis to evaluate the temporal relationship between influenza illness and risk of hip fracture with patients matched on functional status, comorbidities, and facility level characteristics is needed to better characterize the association between influenza and hip fracture. Further research could also focus on potential mitigation strategies (ie, vaccinations, rehydration, or delirium interventions) (22).
Conclusion
We observe a significant association between influenza hospitalizations and hospitalizations for hip fracture among LS NH residents. In a given NH week, an increase in the number ILI hospitalizations from none to two was associated with an approximate one percentage point increase in the risk of a hip fracture hospitalization. Further in-depth study could help characterize the causal relationship between the two events and whether increased surveillance or high-potency vaccination against influenza should be investigated as an additional strategy to reduce hip fracture risk.
Funding
This work was supported by the National Institute of Health (NIH), National Institute on Aging (NIA), #1R01AG045441-01A1, the Agency for Healthcare Research and Quality (AHRQ; 5K12HS022998-02, R01 HS018462), and Office of Academic Affiliations, Department of Veterans Affairs.
Conflict of Interest
V.M. holds stock of unknown value in PointRight, Inc. an information services company providing advice and consultation to various components of the long term care and post acute care industry, including suppliers and insurers. In addition, V.M. Chairs the Independent Quality Committee for HRC Manor Care, Inc., a nursing home chain and serves as chair of a Scientific Advisory Committee for NaviHealth, a post-acute care service organization. The authors have no financial conflicts of interest to disclose.
