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Hospital-onset influenza hospitalizations—United States, 2010-2011

Published:November 01, 2013DOI:https://doi.org/10.1016/j.ajic.2013.06.018

      Background

      Seasonal influenza is responsible for more than 200,000 hospitalizations each year in the United States. Although hospital-onset (HO) influenza contributes to morbidity and mortality among these patients, little is known about its overall epidemiology.

      Objective

      We describe patients with HO influenza in the United States during the 2010-2011 influenza season and compare them with community-onset (CO) cases to better understand factors associated with illness.

      Methods

      We identified laboratory-confirmed, influenza-related hospitalizations using the Influenza Hospitalization Surveillance Network (FluSurv-NET), a network that conducts population-based surveillance in 16 states. CO cases had laboratory confirmation ≤ 3 days after hospital admission; HO cases had laboratory confirmation > 3 days after admission.

      Results

      We identified 172 (2.8%) HO cases among a total of 6,171 influenza-positive hospitalizations. HO and CO cases did not differ by age (P = .22), sex (P = .29), or race (P = .25). Chronic medical conditions were more common in HO cases (89%) compared with CO cases (78%) (P < .01), and a greater proportion of HO cases (42%) than CO cases (17%) were admitted to the intensive care unit (P < .01). The median length of stay after influenza diagnosis of HO cases (7.5 days) was greater than that of CO cases (3 days) (P < .01).

      Conclusion

      HO cases had greater length of stay and were more likely to be admitted to the intensive care unit or die compared with CO cases. HO influenza may play a role in the clinical outcome of hospitalized patients, particularly among those with chronic medical conditions.

      Key Word

      Seasonal influenza is responsible for more than 200,000 hospitalizations and between 3,000 and 49,000 deaths each year in the United States
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      Estimates of deaths associated with seasonal influenza, United States, 1976-2007.
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      Influenza-associated hospitalizations in the United States.
      and poses important infection control risks and challenges to both patients and health care personnel (HCP). Although hospital-onset (HO) influenza contributes to morbidity and mortality among hospitalized patients, little is known about its overall epidemiology. Most prior reports have described outbreaks in the acute care setting among selected populations at increased risk for infection, such as immunocompromised patients or neonates.
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      We describe characteristics of adults and children with HO influenza identified during the 2010-2011 influenza season in the United States and compare them with patients hospitalized with community-onset (CO) influenza.

      Methods

      We used data from the 2010-2011 influenza season collected through the Influenza Hospitalization Surveillance Network (FluSurv-NET). FluSurv-NET is a collaborative surveillance network with participants from the Centers for Disease Control and Prevention (CDC), state and local health departments, and academic institutions that conducts population-based surveillance for laboratory-confirmed, influenza-related hospitalizations in children (persons younger than 18 years) and adults each year from October 1 to April 30. During the 2010-2011 season, FluSurv-NET covered over 80 counties in 16 states (CA, CO, CT, GA, ID, MD, MI, MN, NM, NY, OH, OK, OR, RI, TN, and UT) and included a surveillance population of approximately 7 million children and 22 million adults.

      CDC. Flu view. Available from: http://www.cdc.gov/flu/weekly/. Accessed December 12, 2012.

      FluSurv-NET defines a case as (1) a resident of a preidentified geographic area (ie, a surveillance catchment area), (2) admitted to a hospital where catchment area residents receive care, (3) with a positive influenza diagnostic test ≤ 14 calendar days prior to hospital admission or any time during the current hospitalization, and (4) a hospital admission date between October 1, 2010, and April 30, 2011. Diagnostic testing for influenza was conducted at the discretion of care providers and included testing by viral culture, immunofluorescence antibody staining, reverse-transcription polymerase chain reaction testing, and rapid influenza diagnostic testing. In FluSurv-NET, the date of laboratory confirmation of influenza refers to collection date of the specimen used to confirm influenza virus infection. We considered hospitalization to represent admission to an inpatient ward of a hospital; an overnight stay was not required. Emergency room visits, regardless of duration, were not considered hospitalizations.
      We defined a CO case as any FluSurv-NET case with laboratory confirmation of influenza ≤ 3 calendar days after hospital admission. We defined a HO case as (1) any patient admitted for a nonrespiratory illness who subsequently developed fever or respiratory illness and had laboratory confirmation of influenza > 3 calendar days after hospital admission (Fig 1) or (2) any FluSurv-NET case designated by the site surveillance officer as HO, with accompanying narrative justification. HO cases eligible under criterion (2) were reviewed individually to determine final case status. For patients transferred from another hospital, we used the first hospital admission date to determine case status. We defined an indeterminate case as any FluSurv-NET case not fitting one of the above criteria for exposure setting or patients for whom the exposure setting could not be determined because of lack of available data.
      Figure thumbnail gr1
      Fig 1Identification of hospital-onset (HO), community-onset (CO), and indeterminate (IND) influenza hospitalizations in FluSurv-NET during the 2010-2011 influenza season in the United States.
      Surveillance officers at each FluSurv-NET site abstracted information from patient medical records to complete a standard case report form for all cases as part of regular surveillance activities. We compared HO cases to CO cases using the Wilcoxon rank sum test for continuous variables and the χ2 or Fisher exact test for categorical variables; α = .05 for all comparisons. We maintained case data on a secure server at CDC and performed all analyses using Microsoft Excel (Microsoft Corp, Redmond, WA) and SAS v 9.2 (SAS Institute, Cary, NC). This activity was determined by CDC to be part of routine public health practice and was not subject to Institutional Review Board approval for human research protections.

      Results

      We identified 172 (2.8%) HO, 5,912 (96%) CO, and 87 (1.4%) indeterminate cases among a total of 6,171 FluSurv-NET cases during the 2010-2011 influenza season (Fig 1). The median age of HO cases was 55 years, and 84% were aged 18 years or older. The majority (90%) of HO cases had at least 1 chronic medical condition, including cardiovascular disease (40%), asthma or other chronic lung disease (40%), and metabolic disease (39%). Significantly fewer CO cases (78%) had 1 or more chronic medical conditions (Table 1). Four (2%) HO cases were newborns that had laboratory confirmation of influenza before being discharged from the maternity ward. Seventeen FluSurv-NET cases were designated by site surveillance officers as HO but had insufficient accompanying information to confirm case status; these cases were categorized as indeterminate.
      Table 1Demographic characteristics and chronic medical conditions for hospital-onset and community-onset influenza hospitalizations: FluSurv-NET sites, 2010-2011 influenza season
      Hospital onset (n = 172)Community onset (n = 5,912)P value
      Female, n (%)85 (50)3,163 (54).29
      Median age, y5452.22
      Age group, y, n (%).41
       0-422 (13)896 (15)
       5-177 (3.7)424 (7.2)
       18-4942 (24)1,437 (24)
       50-6441 (24)1,123 (19)
       65+60 (35)2,032 (34)
      Race, n (%).25
       White102 (59)3,150 (53)
       Black34 (20)1,296 (22)
       AI/AN1 (<1)48 (<1)
       Other
      Includes Asian, multiracial, and unknown race.
      21 (11)707 (12)
      Hispanic ethnicity, n (%)14/91 (15)711/3,855 (18).46
      Hospital transfer, n (%)13/171 (7.6)123/5,899 (2.1)<.01
      Nursing home resident, n (%)19/142 (14)694/4,574 (15).63
      Health care personnel, n (%)2/142 (1.4)100/4,583 (2.2).68
      Influenza vaccination, n (%)64/141 (45)2,350/5,282 (45).83
      Influenza type/subtype, n (%)
      One case had influenza A and B coinfection; 1 case had unknown type; for influenza A characterization, unknown was listed for 48 cases and was missing or other for 32 cases.
       Influenza B27 (16)978 (17).99
       Influenza A143 (84)4,866 (82)
       Influenza A (H3)58 (40)1,789 (37).15
       Influenza A (H1N1)37 (26)929 (19)
      Underlying medical condition, n (%)
      Asthma may include a diagnosis of asthma and reactive airway disease; other chronic lung diseases may include conditions such as bronchiolitis obliterans, chronic aspiration pneumonia, and interstitial lung disease; cardiovascular diseases may include conditions such as coronary heart disease, cardiac valve disorders, congestive heart failure, pulmonary hypertension, and aortic stenosis; immunosuppressive condition may include conditions such as immunoglobulin deficiency, leukemia, lymphoma, HIV/AIDS, and individuals taking immunosuppressive medications; metabolic disease may include conditions such as diabetes mellitus, thyroid dysfunction, adrenal insufficiency, and liver disease; neuromuscular disease may include conditions such as seizure disorders; obesity was either documented in the medical record or identified during patient interview or was a documented body mass index greater than 30 (kg/m2) in patients 20 years of age or older or equal to or greater than the 95th percentile of a patient's age and sex category in patients under 20 years of age. Body mass index was not calculated in pregnant women or children less than 2 years of age; renal diseases may include conditions such as acute or chronic renal failure, nephrotic syndrome, glomerulonephritis, and impaired creatinine clearance.
      153 (89)4,630 (78)<.01
       Asthma24 (14)1,159 (20).065
       Other chronic lung disease44 (26)1,113 (19)<.026
       Cardiovascular disease67 (39)1,743 (30)<.01
       Metabolic disease64 (37)1,672 (28)<.011
       Renal disease38 (22)707 (12)<.01
       Neuromuscular disease12 (7.0)376 (6.3).74
       Immunosuppressive condition34 (20)622 (11)<.01
       Obesity or morbid obesity45/156 (32)1,368/4,032 (34).62
      Pregnant, n (%)2 (1.2)236 (4).069
      AI/AN, American Indian/Alaskan native.
      Includes Asian, multiracial, and unknown race.
      One case had influenza A and B coinfection; 1 case had unknown type; for influenza A characterization, unknown was listed for 48 cases and was missing or other for 32 cases.
      Asthma may include a diagnosis of asthma and reactive airway disease; other chronic lung diseases may include conditions such as bronchiolitis obliterans, chronic aspiration pneumonia, and interstitial lung disease; cardiovascular diseases may include conditions such as coronary heart disease, cardiac valve disorders, congestive heart failure, pulmonary hypertension, and aortic stenosis; immunosuppressive condition may include conditions such as immunoglobulin deficiency, leukemia, lymphoma, HIV/AIDS, and individuals taking immunosuppressive medications; metabolic disease may include conditions such as diabetes mellitus, thyroid dysfunction, adrenal insufficiency, and liver disease; neuromuscular disease may include conditions such as seizure disorders; obesity was either documented in the medical record or identified during patient interview or was a documented body mass index greater than 30 (kg/m2) in patients 20 years of age or older or equal to or greater than the 95th percentile of a patient's age and sex category in patients under 20 years of age. Body mass index was not calculated in pregnant women or children less than 2 years of age; renal diseases may include conditions such as acute or chronic renal failure, nephrotic syndrome, glomerulonephritis, and impaired creatinine clearance.
      Among HO cases, the median date of influenza confirmation by diagnostic test was hospital day 7 (range, 4-101). The median hospital length of stay (LOS) after influenza diagnosis for HO cases (7.5 days) was significantly longer than that of CO cases (3 days). Of 72 (42%) HO cases admitted to the intensive care unit during their hospitalization, 46 (27%) required mechanical ventilation; both proportions were significantly greater than those observed among CO cases (Table 2). Among cases for which information was available, a significantly greater proportion of HO cases either died during hospitalization (16%), compared with CO cases (2.9%), or were discharged to a long-term care facility (LTCF) (35%) compared with CO cases (16%). Significantly more HO cases (7.6%) were transferred from another hospital compared with CO cases (2.1%). Significantly fewer HO cases (64%) received treatment with influenza antiviral medications during hospitalization than did CO cases (72%) (Table 2).
      Table 2Clinical course and treatment for hospital-onset and community-onset influenza hospitalizations: FluSurv-NET sites, 2010-2011 influenza season
      Hospital onset (n = 172)Community onset (n = 5,912)P value
      Intensive care unit admission, n (%)72/171 (42)1,021/5,894 (17)<.01
      Mechanical ventilation, n (%)46/171 (27)465/5,894 (7.9)<.01
      Antiviral treatment, n (%)110/171 (64)4,255/5,903 (72).026
      Pneumonia, n (%)56 (33)1,828 (31).65
      Acute respiratory distress syndrome, n (%)14 (8.1)189 (3.2)<.01
      Died, n (%)27/171 (16)170/5,894 (2.9)<.01
      Discharged home, n (%)91/140 (65)4,704/5,595 (84)<.01
      Discharged to long-term care facility/hospice, n (%)49/140 (35)874/5,595 (16)<.01
      Median length of stay (range), days7 (4-101)3 (0-164)<.01
      Median length of stay after influenza test (range), days7.5 (0-66)3 (0-164)<.01
      HO cases were identified in 15 of 16 FluSurv-NET sites and ranged from 0% to 7% of all influenza-associated hospitalizations at each site. Connecticut reported 30 HO cases, the largest number among all sites, representing 17% of all HO cases identified, whereas Idaho reported the fewest number (1), excluding Oklahoma, which did not identify an HO case during the surveillance period (Fig 2). Overall, 140 (81%) HO and 4,008 (68%) CO cases were identified using a reverse-transcription polymerase chain reaction diagnostic test, respectively (P < .01).
      Figure thumbnail gr2
      Fig 2Number of hospital-onset influenza hospitalizations (percent of all influenza hospitalizations) identified in FluSurv-NET by state during the 2010-2011 influenza season (n = 172).
      Thirty-five of 49 (71%) HO cases discharged to a LTCF after hospitalization were not LTCF residents prior to hospitalization. This is significantly higher than the proportion of CO cases (334/874, 38%) discharged to an LCTF who were not LTCF residents prior to hospitalization (P < .01). Among patients with influenza A virus infection, significantly more HO cases were hospitalized with influenza A (H3N2) virus than influenza A (H1N1) virus compared with CO cases (Table 1).

      Discussion

      We used data from a multicenter, national surveillance system in the United States to describe the prevalence of laboratory-confirmed HO influenza during an influenza season. We found 2.8% of all patients hospitalized with influenza in FluSurv-NET during the 2010-2011 season to be HO cases. This result falls within the range of previous surveillance studies of health care-associated influenza that reported rates from 2.0% to 7.0% among adult or all hospitalized patients with influenza.
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      Influenza virus infection in patients already hospitalized for other conditions may contribute to poorer clinical outcomes, increase the use of health care resources in hospitals, and add to the annual burden of influenza in the United States.
      Demographic characteristics of HO cases were similar to CO cases, but chronic medical conditions were more frequently identified in HO cases. The reason for this difference is unclear. Because persons with chronic medical conditions are known to be at increased risk for complications from influenza,
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      these patients may have been closely monitored for onset of influenza-like illness while hospitalized, resulting in increased testing for influenza and increased case detection. Regardless of the reason, close attention should be given to hospitalized patients at increased risk for influenza complications, including persons with chronic medical conditions, and influenza testing and early antiviral treatment is strongly encouraged for hospitalized patients developing new or worsening symptoms of acute respiratory illness.
      The clinical course of HO cases was remarkable for greater LOS, greater proportion with intensive care unit admission, greater proportion requiring mechanical ventilation, and greater proportion dying or discharged to a LTCF compared with CO cases. Elderly patients and patients with multiple chronic medical conditions (some of which may place them at increased risk for influenza complications) tend to have longer hospital stays compared with younger patients and those with fewer chronic medical conditions.
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      patients with chronic conditions that predispose them to influenza complications may be at risk for acquisition of influenza because of increased LOS and at risk for influenza complications because of their chronic medical conditions. Although we could not estimate the contribution that influenza made to poor patient outcomes, influenza virus infection in an already debilitated patient population may have contributed to the increased measures of illness severity seen in HO cases. Previous studies have described HO influenza virus infections resulting in severe, prolonged, and fatal disease among immunocompromised patients
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      that at least 87% of cases with symptom onset 1.5 days or later after admission acquired their infections nosocomially. If diagnostic testing were delayed to fall outside the 3-day period, misclassification is possible, although most immunocompetent adults shed virus for ≤ 7 days.
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      Thus, it is reasonable to conclude that misclassification would have occurred in only a minority of HO cases. Moreover, it is likely that the majority of HO cases we identified were not only HO but also hospital-acquired cases of influenza because our case definition generally precluded other sources of acquisition. Second, we were unable to ascertain the temporal relationship between case status and measures describing the clinical course of patients. Notably, greater illness severity and LOS among HO cases may not be a result of influenza; rather, HO influenza may have resulted from a greater LOS, which itself may have been due to an unrelated factor, such as a chronic medical condition. Third, our findings likely underestimate the number of influenza-associated hospitalizations, including HO cases, because the decision to perform influenza diagnostic testing on patients admitted to FluSurv-NET hospitals is based on the clinical judgment of medical care providers, and not all patients with influenza may have been identified. Because the sensitivity and positive predictive value of clinical signs and symptoms for the diagnosis of influenza among patients hospitalized for nonrespiratory related illnesses are reported to be low,
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      clinicians may have been less likely to test patients presenting with minor or atypical influenza signs and symptoms. Finally, because clinicians may be inclined to reserve influenza testing for patients who are severely ill or medically fragile, our findings may also over-represent cases with more severe illness (because of influenza or due to a chronic medical condition).
      To prevent both HO and CO influenza, the Advisory Committee on Immunization Practices recommends annual seasonal influenza vaccination for all persons ≥ 6 months of age.
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      Vaccination of HCP is an important step in preventing health care transmission of influenza, but vaccination rates among HCP remain suboptimal, despite strong Advisory Committee on Immunization Practices and National Committee for Quality Assurance recommendations that all HCP should be vaccinated annually against influenza.
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      In addition to vaccination, diagnostic testing for influenza among hospitalized patients with respiratory illness is recommended, as well as early administration of antiviral medications for patients suspected to have influenza. To prevent and control HO influenza, health care facilities should also implement appropriate transmission-based isolation precautions for patients with suspected or confirmed influenza, manage ill HCP appropriately, and employ facility-wide environmental and engineering infection control measures.

      Prevention strategies for seasonal influenza in healthcare settings. Available from: http://www.cdc.gov/flu/professionals/infectioncontrol/healthcaresettings.htm. Accessed October 30, 2012.

      Siegel JD, Rhinehart E, Jackson M, Chiarello L. Guideline for isolation precautions: preventing transmission of infectious agents in healthcare settings. 2007. Available from: http://www.cdc.gov/ncidod/dhqp/pdf/isolation2007.pdf. Accessed September 1, 2012.

      Although they comprised a small proportion of all influenza-associated hospitalizations in FluSurv-NET during the 2010-2011 season, the 172 cases in this report provide a useful preliminary description of the epidemiology of HO influenza in the United States. They also describe the additional burden that HO influenza may impose on health care facilities and hospitalized patients, especially those with chronic medical conditions. Whether or not HO influenza leads directly to poor outcomes among hospitalized patients merits further investigation in a more comprehensive study that can evaluate the relative risk of severe outcomes associated with influenza in HO compared with CO cases. Physicians should be aware of influenza as a potential HO infection during influenza season and of the possibility of severe illness, particularly among patients at increased risk for complications from influenza.

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