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Non-Ventilator Associated Hospital Acquired Pneumonia (NV-HAP) Risk Among Hospitalized Veterans Before and During the COVID-19 Pandemic

  • Author Footnotes
    # Permanent (home) address: 1516 Bluemoon Drive, Longmont, CO, 80504, Cell (602) 918-0633
    Evan Carey
    Correspondence
    Corresponding Author: Evan Carey, PhD, Research Health Scientist, Research and Development, Rocky Mountain Regional VA Medical Center, Aurora, CO
    Footnotes
    # Permanent (home) address: 1516 Bluemoon Drive, Longmont, CO, 80504, Cell (602) 918-0633
    Affiliations
    Research and Development, Rocky Mountain Regional VA Medical Center, Aurora, CO

    The VA Collaborative Evaluation Center (VACE), a virtual center based at the Rocky Mountain Regional, Seattle, and Louis Stokes Cleveland VA Medical Centers; Aurora, Seattle and Cleveland, Colorado, Washington, Ohio

    Department of Biostatistics and Informatics, Colorado School of Public Health, University of Colorado Anschutz Medical Campus
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  • Hung-Yuan P. Chen
    Affiliations
    Research and Development, Rocky Mountain Regional VA Medical Center, Aurora, CO

    The VA Collaborative Evaluation Center (VACE), a virtual center based at the Rocky Mountain Regional, Seattle, and Louis Stokes Cleveland VA Medical Centers; Aurora, Seattle and Cleveland, Colorado, Washington, Ohio
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  • Dian Baker
    Affiliations
    School of Nursing, California State University, Sacramento, CA
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  • Richard Blankenhorn
    Affiliations
    Research and Development, Rocky Mountain Regional VA Medical Center, Aurora, CO

    The VA Collaborative Evaluation Center (VACE), a virtual center based at the Rocky Mountain Regional, Seattle, and Louis Stokes Cleveland VA Medical Centers; Aurora, Seattle and Cleveland, Colorado, Washington, Ohio
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  • Shannon Munro
    Affiliations
    Department of Veterans Affairs Medical Center, Salem, VA
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  • Author Footnotes
    # Permanent (home) address: 1516 Bluemoon Drive, Longmont, CO, 80504, Cell (602) 918-0633
Published:January 02, 2023DOI:https://doi.org/10.1016/j.ajic.2022.12.012

      Highlights

      • NV-HAP among hospitalized Veterans decreased steadily between 2015-2020.
      • NV-HAP rates increased by 25% among 2019-nCoV- and 108% among 2019-nCoV+ Veterans.
      • Hospitalized Veterans experienced an increased NV-HAP risk during 2019-nCoV.
      • Fundamental infection prevention and nursing care are essential to reduce NV-HAP.

      ABSTRACT

      Background

      Among hospitalized U.S. Veterans, the rate of non-ventilator associated hospital acquired pneumonia (NV-HAP) decreased between 2015-2020 then increased following the onset of 2019-nCoV (COVID-19).

      Methods

      Veterans admitted to inpatient acute care for >= 48 hours at 135 Department of Veterans Affairs Medical Centers between 2015-2021 were identified (n=1,567,275). Non-linear trends in NV-HAP incidence were estimated using generalized additive modeling, adjusted for seasonality and patient risk factors.

      Results

      The incidence rate (IR) of NV-HAP decreased linearly by 32% (95% CI: 63-74) from 10/1/2015 to 2/1/2020, translating to 337 fewer NV-HAP cases. Following the U.S. onset of the COVID-19 pandemic in February 2020, the NV-HAP IR increased by 25% (95% CI: 14-36) among Veterans without COVID-19 and 108% (95% CI: 178-245) among Veterans with COVID-19, resulting in an additional 50 NV-HAP cases and $5,042,900 in direct patient care costs 12-months post admission.

      Discussion

      This increase in NV-HAP rates could be driven by elevated risk among Veterans with COVID-19, decreased prevention measures during extreme COVID-19 related system stress, and increased patient acuity among hospitalized Veterans during the first year of the pandemic.

      Conclusions

      Basic nursing preventive measures that are resilient to system stress are needed as well as population surveillance to rapidly identify changes in NV-HAP risk.

      KEYWORDS

      Background

      Among hospitalized U.S. Veterans, the rate of non-ventilator associated hospital acquired pneumonia (NV-HAP) decreased between 2015-2020 then increased following the onset of COVID-19.
      • Carey E
      • Blankenhorn R
      • Chen P
      • Munro S.
      Non-ventilator associated hospital acquired pneumonia incidence and health outcomes among U.S. Veterans from 2016-2020.
      This increase in NV-HAP rates could be driven by elevated risk among Veterans with COVID-19, decreased NV-HAP prevention measures during extreme COVID-19 related system stress, and increased patient acuity among hospitalized Veterans during the first year of the pandemic.

      Methods

      We identified a cohort of 1,567,275 U.S. Veterans admitted to 135 VA facilities in acute care settings between 10/1/2015 and 3/31/2021with a minimum 48-hour length of stay. Consistent with prior work,
      • Carey E
      • Chen HP
      • Baker D
      • et al.
      The association between non-ventilator associated hospital acquired pneumonia and patient outcomes among U.S. Veterans.
      transfer admissions were excluded as well as admissions with index diagnoses of acute respiratory distress, respiratory failure, respiratory arrest, asphyxia, or pneumonia indicated as present on admission (POA). The primary exposure was a positive SARS-CoV-2 test within the 28 days prior to admission date, referred to as COVID-19. The outcome of NV-HAP was identified based on International Classification of Diseases (ICD-10) codes for bacterial pneumonia indicated as not POA.
      • Carey E
      • Chen HP
      • Baker D
      • et al.
      The association between non-ventilator associated hospital acquired pneumonia and patient outcomes among U.S. Veterans.
      Patient demographics, comorbidities, exposure, and outcomes were identified using the VHA Corporate Data Warehouse (CDW).
      • Price LE
      • Shea K
      • Gephart S.
      The Veterans Affairs’ Corporate Data Warehouse: Uses and implications for nursing research and practice.
      NV-HAP incidence rates (IR) were estimated using a log linked quasi-Poisson generalized additive model with an offset for hospitalized at risk days.
      • Wood SN
      • Goude Y
      • Shaw S.
      Generalized additive models for large data sets.
      The following covariates were included a-priori for risk adjustment based on prior work: age, gender, recent diagnoses of peripheral vascular disease, chronic pulmonary disease, and cancer.
      • Carey E
      • Chen HP
      • Baker D
      • et al.
      The association between non-ventilator associated hospital acquired pneumonia and patient outcomes among U.S. Veterans.
      A cyclic cubic regression spline for admission month was included to adjust for seasonality. The trend in NV-HAP IR was estimated by a thin plate regression spline fit
      • Wood SN.
      Thin plate regression splines.
      separately for pre-COVID-19 era admissions (prior to 2/1/2020) and COVID-19 era admissions, with posterior simulations from model parameters used to identify era specific IR and the number of cases associated with that change in risk. The change in IR was summarized over two different eras: pre-COVID (10/1/2015 to 2/1/2020) and COVID-era (2/2/2020-3/31/2021). The reported change in IR and associated cases are compared to the conservative counterfactual assumption that the estimated IR at the start of each era remained constant. Additional 12-month direct medical system costs of the excess NV-HAP cases was calculated using a Monte-Carlo simulation with 10,000 replications.

      Results

      Hospitalized Veterans in this cohort have a high burden of clinical comorbidities documented in the year prior to admission across all eras reported (table 1). Most demographics and comorbidities are similar across eras except race and diagnosis of dementia. Veterans with COVID-19 are more likely to be Caucasian and have documented dementia in the previous year compared with COVID negative Veterans or those Veterans hospitalized prior to the onset of COVID-19.
      Table 1Select patient traits stratified by era: pre-COVID-19 era, post-COVID-19 era COVID±, and post-COVID-19 era COVID –. Continuous variables are summarized by mean (standard deviation) and categorical variables are summarized by count (percent). Standardized mean differences (SMD) are presented to identify imbalance across groups, with SMD0.1 bolded.
      VariablePre-COVID Era AdmissionsCOVID Era COVID- AdmissionCOVID Era COVID+ AdmissionSMD
      Total unique index admissions1,290,056258,19719,022
      Demographics
      Age, mean (SD)   70.34 (12.23)    69.35 (12.56)69.84 (13.79)0.052
        Age<40   29,825 (2.3)    7,957 (3.1)789 (4.1)
       40<=Age<50   40,649 (3.2)    9,750 (3.8)698 (3.7)
       50<=Age<65   276,189 (21.4)    59,065 (22.9)3,948 (20.8)
       65<=Age<75   513,448 (39.8)    99,891 (38.7)6,758 (35.5)
        75<=Age   429,945 (33.3)    81,534 (31.6)6,829 (35.9)
      Male Gender, N (%)1,223,645 (94.9)244,232 (94.6)17,996 (94.6)0.008
      Race, N (%)
        Caucasian   910,275 (70.6)176,715 (68.4)11,736 (61.7)0.125
        African American   288,384 (22.4)    61,501 (23.8) 5,725 (30.1)0.118
        American Indian   12,729 (1.0)    2,643 (1.0) 216 (1.1)0.01
        Asian   5,927 (0.5)    1,452 (0.6) 106 (0.6)0.01
        Pacific Islander   11,798 (0.9)    2,553 (1.0) 198 (1.0)0.009
        Unknown   69,810 (5.4)    15,085 (5.8) 1,198 (6.3)0.025
      Ethnicity, N (%)
        Hispanic Latino   81,919 (6.4)    15,989 (6.2) 1,365 (7.2)0.026
        Not Hispanic Latino1,121,149 (86.9)216,121 (83.7)15,762 (82.9)0.075
        Unknown   86,988 (6.7)    26,087 (10.1) 1,895 (10.0)0.081
      Clinical Comorbidities in 1 year prior to admission
      Myocardial infarction, N (%)   121,686 (9.4)    28,037 (10.9) 1,925 (10.1)0.032
      Congestive heart failure, N (%)   329,174 (25.5)    71,160 (27.6) 5,039 (26.5)0.031
      Peripheral vascular disease, N (%)   265,363 (20.6)    58,923 (22.8) 3,798 (20.0)0.046
      Cerebrovascular disease, N (%)   185,820 (14.4)    41,296 (16.0) 3,155 (16.6)0.04
      Dementia, N (%)   104,663 (8.1)    22,567 (8.7) 2,676 (14.1)0.127
      Chronic pulmonary disease, N (%)   387,765 (30.1)    77,572 (30.0) 5,569 (29.3)0.011
      Connective tissue disease, N (%)   27,392 (2.1)    5,643 (2.2) 414 (2.2)0.003
      Peptic Ulcer disease, N (%)   30,974 (2.4)    6,979 (2.7) 374 (2.0)0.033
      Mild Liver Disease, N (%)   173,865 (13.5)    38,341 (14.8) 2,438 (12.8)0.039
      Diabetes without comp, N (%)   525,240 (40.7)    106,913 (41.4) 8,516 (44.8)0.055
      Diabetes with comp, N (%)   309,360 (24.0)    70,686 (27.4) 5,536 (29.1)0.077
      Hemiplegia paraplegia, N (%)   59,071 (4.6)    9,867 (3.8) 685 (3.6)0.033
      Renal disease, N (%)   308,349 (23.9)    68,926 (26.7) 5,478 (28.8)0.074
      Cancer, N (%)   261,231 (20.2)    54,604 (21.1) 3,157 (16.6)0.078
      Severe liver disease, N (%)   36,936 (2.9)    8,362 (3.2) 502 (2.6)0.024
      Metastatic solid tumor   60,909 (4.7)    13,766 (5.3) 717 (3.8)0.05
      AIDS   12,924 (1.0)    2,694 (1.0) 197 (1.0)0.003
      Charlson index, mean (SD)   3.46 (3.04)    3.73 (3.20) 3.64 (3.21)0.057
      The NV-HAP IR decreased linearly by 32% (95% CI: 63-74) between 10/1/2015 and 2/1/2020, representing 338 (95% CI: 263 - 412) fewer cases of NV-HAP in this cohort. Compared to the conservative assumption that NV-HAP risk would remain constant following 2/2/2020, the observed NV-HAP IR increased by 24.8% (95% CI:14.6-35.8) among COVID-19 negative Veterans and by 108.4% (95% CI:78-144.8) among COVID-19 positive Veterans, representing an additional 50 (95% CI: 27-74) NV-HAP cases. Figure 2 summarizes these trends. Prior work estimated the additional 12-month direct medical costs of a single NV-HAP case is $100,858.61(SD=310),
      • Carey E
      • Chen HP
      • Baker D
      • et al.
      The association between non-ventilator associated hospital acquired pneumonia and patient outcomes among U.S. Veterans.
      thus we estimate these cases represent an additional $5,045,259 (95% CI: 2,707,708-7,363,787) in direct health system costs over one year post admission.

      Discussion

      Following several years of decreased incidence of NV-HAP among Veterans hospitalized in acute care settings, there was an increase in NV-HAP following the onset of the COVID-19 pandemic among all hospitalized Veterans. The highest risk was among the COVID-19 positive Veterans. The CDC reported that after years of decline from 2015-2020, U.S. hospitals experienced a rise in monitored hospital acquired infections (HAI) during COVID-19.
      • Weiner-Lastinger LM
      • Pattabiraman V
      • Konnor RY
      • et al.
      The impact of coronavirus disease 2019 (COVID-19) on healthcare-associated infections in 2020: A summary of data reported to the National Healthcare Safety Network.
      NV-HAP is not a required CMS metric but carries a higher morbidity and mortality than other HAI.
      • Munro SC
      • Baker D
      • Giuliano KK
      • et al.
      Nonventilator hospital-acquired pneumonia: A call to action: Recommendations from the National Organization to Prevent Hospital-Acquired Pneumonia (NOHAP) among nonventilated patients.
      To our knowledge, this is the first published report of changes in NV-HAP risk associated with the onset of COVID-19 among all hospitalized Veterans in a national healthcare system.
      The observed increase in NV-HAP risk among all patients during the COVID era is likely multifactorial. Prevention strategies are essential to mitigate NV-HAP risk, yet increased clinical workload seen during the COVID-19 pandemic may have limited completion of fundamental nursing care (e.g., early mobility programs, consistent oral care, aspiration precautions, see table 2) to prevent NV-HAP.
      • Sugg HVR
      • Russell AM
      • Morgan LM
      • et al.
      Fundamental nursing care in patients with the SARS-CoV-2 virus: results from the “COVID-NURSE” mixed methods survey into nurses’ experiences of missed care and barriers to care.
      Other barriers include wearing personal protective equipment which impacts communication and the ability to get needed supplies to the bedside without cross-contamination. Among patients with COVID-19 infections, increased NV-HAP risk could be due to changes in the lower respiratory tract microbiome, disruption of the immune response, and synergism seen during COVID-19 infection.
      • Mirzaei R
      • Goodarzi P
      • Asadi M
      • et al.
      Bacterial co-infections with SARS-CoV-2.
      Increase in NV-HAP risk could also be associated with placing patients in the prone position (to improve oxygenation) as well as having the diagnosis of dementia, which increases the risk of microaspiration leading to development of secondary bacterial pneumonia.
      • Povoa P
      • Martin-Loeches I
      • Nseir S.
      Secondary pneumonias in critically ill patients with COVID-19: Risk factors and outcomes.
      Table 2Nursing interventions to reduce the risk of hospital acquired pneumonia in non-ventilated patients
      Nursing interventionRecommendations
      Oral hygieneComplete an oral care assessment and report any signs of active infection (e.g., abscess, candidiasis). Provide consistent oral care including toothbrushing a minimum of twice daily and dentures/ partials care nightly.
      • Munro SC
      • Baker D
      • Giuliano KK
      • et al.
      Nonventilator hospital-acquired pneumonia: A call to action: Recommendations from the National Organization to Prevent Hospital-Acquired Pneumonia (NOHAP) among nonventilated patients.
      Use a suction toothbrush for patients at risk for aspiration.
      Early mobilityFollow standardized mobility protocols including passive range of motion, turning in bed, and early and frequent ambulation depending on the physical capabilities of the patient initiated within 24 hours of admission.
      • Munro SC
      • Baker D
      • Giuliano KK
      • et al.
      Nonventilator hospital-acquired pneumonia: A call to action: Recommendations from the National Organization to Prevent Hospital-Acquired Pneumonia (NOHAP) among nonventilated patients.
      Nasogastric-tube careAdhere to standardized process for placement and management of nasogastric tubes and provision of ongoing staff education and skills testing.
      • Munro SC
      • Baker D
      • Giuliano KK
      • et al.
      Nonventilator hospital-acquired pneumonia: A call to action: Recommendations from the National Organization to Prevent Hospital-Acquired Pneumonia (NOHAP) among nonventilated patients.
      Aspiration precautionsFacilitate dysphagia screening in high-risk patients and evaluation by speech and language pathologists, provide modified diets and feeding strategies for patients with abnormal swallowing, assist with head of bed elevation (“up to eat”).
      • Munro SC
      • Baker D
      • Giuliano KK
      • et al.
      Nonventilator hospital-acquired pneumonia: A call to action: Recommendations from the National Organization to Prevent Hospital-Acquired Pneumonia (NOHAP) among nonventilated patients.
      For the patient at high-risk for aspiration use a suction toothbrush for oral care.
      Turn, cough, deep breathing exercises, incentive spirometry, and chest physiotherapyFollow local healthcare facility policy.
      • Munro SC
      • Baker D
      • Giuliano KK
      • et al.
      Nonventilator hospital-acquired pneumonia: A call to action: Recommendations from the National Organization to Prevent Hospital-Acquired Pneumonia (NOHAP) among nonventilated patients.
      Routine handwashingDecontaminate hands before and after contact with patients and when visibly soiled.
      Influenza, covid-19, and pneumococcal vaccination for patients and healthcare personnelAdminister vaccinations following CDC guidelines and facility policy.
      Patient, family and/or caregiver educationDiscuss prevention strategies to reduce the risk of NV-HAP with patients and their family/caregivers.
      • Munro SC
      • Baker D
      • Giuliano KK
      • et al.
      Nonventilator hospital-acquired pneumonia: A call to action: Recommendations from the National Organization to Prevent Hospital-Acquired Pneumonia (NOHAP) among nonventilated patients.
      Beyond prevention efforts, implementation of NV-HAP monitoring via automated electronic surveillance may serve as a cornerstone of a strong infection prevention program. Previous studies on electronic surveillance of NV-HAP have demonstrated high sensitivity, negative predictive value, and accuracy along with a significantly reduced workload associated with manual chart audits.
      • Munro SC
      • Baker D
      • Giuliano KK
      • et al.
      Nonventilator hospital-acquired pneumonia: A call to action: Recommendations from the National Organization to Prevent Hospital-Acquired Pneumonia (NOHAP) among nonventilated patients.
      If such a system were in place at the onset of the COVID-19 pandemic, the increase in NV-HAP risk would have been identified sooner.
      Limitations of this analysis include the use of ICD-10 code-based definitions for NV-HAP which are prone to variability across settings and use of administrative data-based definitions for other variables. The exclusion of transfer patients to ensure the onset of NV-HAP diagnosis as well as the use of Veteran based demographics (higher proportion male and Caucasian) may limit generalizability to other health systems. The data reflects the VA demographic which is primarily made up of Caucasian Non-Hispanic males over age 50 which may limit external reliability.

      Conclusions

      Healthcare systems should strengthen plans to prioritize infection prevention efforts and basic nursing care that includes NV-HAP prevention measures (e.g., early mobility programs, oral care, aspiration precautions) for all hospitalized patients that are resilient to extreme system stress. In addition to a focus on preventive measures, population surveillance is needed to rapidly identify changes in NV-HAP risk. Accurate and efficient NV-HAP surveillance informs and quantifies the impact of prevention initiatives and helps healthcare systems develop practical strategies to reduce HAIs including NV-HAP. Since prevention of NV-HAP improves patient safety and quality of life, saves lives, and reduces cost, strategies to reduce NV-HAP risk should be designed with resilience to significant system stress such as the COVID-19 pandemic.

      Uncited Link

      Figure 1
      Figure 1:
      Figure 1Population flow chart summarizing the inclusion/exclusion criteria
      Figure 2:
      Figure 2Time trends of NV-HAP incidence with pre/post COVID-19 onset, and separate curves for COVID-19± patients post COVID-19 onset

      Declaration of Competing Interest

      The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

      Acknowledgments

      All authors have completed and submitted the International Committee of Medical Journal Editors form for disclosure of potential conflicts of interest. All potential conflicts of interest were disclosed.
      The VA Quality Enhancement Research Initiative (QUERI) program of the VHA Health Services Research and Development Service and the Diffusion of Excellence Initiative funded this approved non-research evaluation (VHA program guide 1200.21) through grant PEC-19-306 conducted under the authority of the VHA Office of Nursing Services.
      The findings and conclusions in this article are those of the authors and do not necessarily reflect those of the U.S. Government or any of its agencies. This material is the result of work supported with resources and the use of facilities at the Cleveland-Denver-Seattle VA Collaborative Evaluation Center and the Department of Veterans Affairs Medical Center in Salem, VA.

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