Pulmonary Critical Care

S EPSIS IN THE CONTEXT

OFNONVENTILATOR
HOSPITAL-ACQUIRED
PNEUMONIA

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By Karen K. Giuliano, PhD, RN, MBA and Dian Baker, PhD, RN, APRN-BC

Background Sepsis is a leading cause of mortality among

hospitalized patients and is the most expensive condi-
tion affecting the US health care system. Pneumonia is
associated with about half of sepsis cases, yet limited
research has described the incidence of sepsis in the
context of nonventilator hospital-acquired pneumonia
(NV-HAP). Persons with NV-HAP who are at risk for sep-
sis must be identified so that interventions to reduce the
burden of NV-HAP and improve outcomes among
patients with sepsis can be designed.
Objectives To determine the proportion of persons with
NV-HAP in whom sepsis develops and to describe the
demographic and clinical characteristics of persons with
NV-HAP in whom sepsis develops.
Methods In this retrospective, population-based study,
data were extracted from the National Inpatient Sample
from the 2012 Healthcare Cost and Utilization Project
dataset. International Classification of Diseases, Ninth
Revision, Clinical Modification codes were used to iden-
tify adult patients at least 18 years of age who had a stay
of at least 48 hours, had no documented diagnosis of
ventilator-associated pneumonia, and had secondary
diagnoses of both NV-HAP and sepsis, neither of which
was present on admission.
Results In the 2012 calendar year, 119 075 adults had

C E 1.0 Hour NV-HAP develop; sepsis developed in 36.3% of these

cases. Male and black patients were overrepresented in
the sample, and patients had a mean of 7 comorbid con-
This article has been designated for CE contact ditions (SD, 3.3).
hour(s). See more CE information at the end of Conclusions Sepsis in the context of NV-HAP is a key
this article. concern. Additional research is needed to identify fac-
tors associated with the development of sepsis among
patients with NV-HAP. (American Journal of Critical
©2020 American Association of Critical-Care Nurses Care. 2020;29:9-14)
doi:https://doi.org/10.4037/ajcc2020402

www.ajcconline.org AJCC AMERICAN JOURNAL OF CRITICAL CARE, January 2020, Volume 29, No. 1 9
 S
epsis is a systemic response to infection that can cause acute organ dysfunction, dis-
ability, and death.1,2 Despite focused efforts for more than a decade to curtail mortality
and morbidity, sepsis remains a significant health care challenge.3 In the United States
alone, sepsis affects 2% of all patients admitted to hospitals and has an associated
25% mortality.1,4 Furthermore, sepsis is the most expensive condition facing the US
health care system,5 with costs exceeding $23 million in 2013. In Europe and Central Asia, the
impact of sepsis is comparable to that in the United States, but East Asia and the Pacific battle
against an even higher incidence rate.6

Even with the extensive worldwide efforts to of NV-HAP and its associated morbidity and mor-
decrease sepsis, the incidence and mortality of tality are substantial, with the overall impact exceed-
sepsis are continuing to increase.6,7 Current efforts ing that of VAP.16,17 There is, therefore, a need to
remain focused on early recognition and treatment, improve understanding of sepsis in the context of

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but preventive strategies have not been as aggressively NV-HAP. Identification of persons with NV-HAP
deployed. Although the US Centers for Disease Con- who are at risk for sepsis is necessary to design
trol and Prevention recognizes the fundamental interventions to reduce the burden of NV-HAP
benefits of prevention-oriented strategies,8 preven- and improve outcomes among those with sepsis.
tion of sepsis through prevention of infection, To better understand the incidence and impact
particularly hospital-acquired infection, remains a of sepsis among persons with NV-HAP, we conducted
clinical challenge. a retrospective, population-based study in which we
The most common type of infection leading to analyzed data from the National Inpatient Sample
sepsis is pneumonia, including community-acquired (NIS) from the 2012 Healthcare Cost and Utilization
pneumonia and hospital-acquired pneumonia.4,9 Project (HCUP) data set. The purpose of this study
Hospital-acquired pneu- was to determine the proportion of individuals with
The risk of sepsis asso- monia comprises both
ventilator-associated
NV-HAP in whom sepsis develops and to describe
the demographic and clinical characteristics of per-
ciated with nonventilator pneumonia (VAP) and sons with NV-HAP who have sepsis develop.
nonventilator hospital-
hospital-acquired pneu- acquired pneumonia Methods
monia continues to be (NV-HAP). Ventilator This study is part of our hospital-acquired pneu-
use is a risk factor for monia prevention initiative program of research.19-23
underappreciated. hospital-acquired pneu- The institutional review board at the principal inves-
monia,10,11 and the use tigator’s institution granted this secondary analysis
of evidence-based prevention strategies has led to project exempt status.
significant decreases in VAP incidence.12-15 Unfortu-
nately, in comparison with VAP, NV-HAP has been Data Source
inadequately studied and underreported; thus, the Data were extracted from the HCUP NIS data set.
risk of sepsis associated with NV-HAP continues to The data extraction process is shown in the Figure.
be underappreciated.16-20 In spite of recent reduc- The HCUP NIS data set is a public-use data set that
tions in VAP incidence, data still indicate that 50% supports analyses on US hospital trends. The HCUP
of sepsis cases are associated with pneumonia.1 is a partnership of federal and state health care agen-
Moreover, emerging data suggest that the incidence cies and the Agency for Healthcare Research and
Quality.24 The NIS is the largest all-payer, inpatient
care database of the United States, with a 20% strati-
About the Authors fied sample of all inpatient discharges from commu-
Karen K. Giuliano is an associate professor, The Institute
for Applied Life Sciences and College of Nursing, Uni- nity hospitals (excluding rehabilitation and long-term
versity of Massachusetts, Amherst. Dian Baker is a pro- acute care hospitals). Forty-four states participate in
fessor, School of Nursing, California State University,
Sacramento, California.
HCUP, representing more than 96% of the US popu-
lation. As required for use of the NIS dataset, data use
Corresponding author: Karen K. Giuliano, PhD, RN, MBA,
PO Box 391, Mirror Lake, NH 03853 (email: kkgiuliano96
agreement training was completed by the principal
@gmail.com). investigator (April 27, 2015; HCUP-318K72CUW).

10 AJCC AMERICAN JOURNAL OF CRITICAL CARE, January 2020, Volume 29, No. 1 www.ajcconline.org
 US National Inpatient
Sample from 2012
N = 7 296 968
Healthcare Cost and Utilization
Project data set

n = 6 142 968
Adult patients * 18 years old
(1 154 464 excluded)

NV-HAP: pneumonia as secondary

diagnosis not present on admission,
n = 119 075
stay at least 48 hours, no diagnosis of
ventilator-associated pneumonia

NV-HAP with sepsis n = 43 252

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Figure Extraction of nonventilator hospital-acquired pneumonia (NV-HAP) cases.

Case Identification stay, total hospital charges, operating room procedure

The 2012 HCUP NIS data set allows extraction (yes/no), admission and discharge transfer status,
of principal diagnosis and up to 24 secondary diag- and in-hospital mortality.
noses based on the International Classification of Dis-
eases, Ninth Revision, Clinical Modification (ICD-9-CM) Statistical Analyses
diagnosis codes. In addition, HCUP includes a present- Descriptive statistics were used to summarize
on-admission indicator to distinguish between med- the characteristics of NV-HAP cases with sepsis. All
ical conditions that are present when patients enter statistical analyses were performed using SPSS v23.0.
the hospital and those that occur during the hospi-
tal stay. To identify cases of NV-HAP with data avail- Results
able in HCUP, we queried the database for adult In the 2012 calendar year, 133 595 adults in the
patients at least 18 years of age who had a stay of HCUP NIS database had a secondary diagnosis of
at least 48 hours; had no diagnosis of VAP; and had pneumonia. After excluding cases with a length of stay
secondary diagnoses of both NV-HAP and sepsis, less than 48 hours, we obtained a sample of 119 075
neither of which was present on admission. NV-HAP cases (see Figure). Sepsis developed in 36.3%
Consistent with the HCUP Clinical Classifica- of these cases. Descriptive data are shown in the Table.
tions Software recommendations,24 NV-HAP cases The amount of missing data was 4% for race and less
were identified using the following ICD-9-CM codes: than 1% for all other variables.
480.80, 481.00, 482.00, 482.10, 482.20, 482.39,
482.41, 482.42, 482.82, 482.83, 483.80, 484.60, Discussion
484.70, and 486.00.25 Given that hospital-acquired Our goal was to add to the body of knowledge
pneumonia is defined as pneumonia that occurs describing sepsis within the context of NV-HAP. In
more than 48 hours after hospital admission,10 we the current study, 36.3% of patients with NV-HAP had
excluded cases in which pneumonia occurred less sepsis develop. This pro-
than 48 hours after hospital admission. Sepsis portion is comparable to Sepsis developed in
cases were identified by ICD-9-CM codes 995.91 the proportion of patients
and 995.92. with VAP who have sepsis 36.3% of 119 075 cases
Demographic and Clinical Characteristics
develop, which previous
reports26,27 have indicated
of nonventilator hospital-
Data describing the demographic and clinical ranges from 37% to 50%. acquired pneumonia.
characteristics of each case were extracted from the Because NV-HAP usually
database. These characteristics included age, sex, occurs outside of the intensive care unit and occurs
race, number of chronic conditions, elective versus more often in medical than in surgical patients,
nonelective hospital admission, length of hospital the sepsis risk associated with NV-HAP may be

www.ajcconline.org AJCC AMERICAN JOURNAL OF CRITICAL CARE, January 2020, Volume 29, No. 1 11
 Table
Descriptive characteristics of 43 252 patients with
nonventilator hospital-acquired pneumonia and sepsis
Male patients and black patients were overrepre-
Characteristic Valuea sented in the current sample of individuals with
Age, mean (SD), y 66.4 (16.3) NV-HAP and sepsis in comparison to the popula-
Male sex 52.9 (22 874) tion demographic characteristics of the United States
Race (n = 41 525) as a whole.31 This finding is consistent with previous
White 67.9 (28 191) reports of a higher incidence of sepsis among male
Black 15.3 (6374) patients1 and black patients.32,33 Similarly, patients
Hispanic 9.4 (3907)
in the current sample had a mean of 7 comorbid
Asian or Pacific Islander 3.4 (1396)
Native American 0.7 (286) conditions (SD, 3.3), a finding that is supported by
Other 3.3 (1371) previous research suggesting a positive association
Chronic conditions (n = 43 252) between chronic disease burden and risk of sepsis.2
Number of conditions, mean (SD) 7.4 (3.2) The results of this study indicate that sepsis in
Elective versus nonelective hospital admission (n = 43 146) the context of NV-HAP is a significant concern, per-
Patients who did not elect for hospital admission 92.7 (40 084) haps particularly among individuals who are male,
Patients who elected for hospital admission 7.1 (3062)
identify as black, or have multiple chronic health

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Receipt or not of operating room procedure (n = 43 252)
conditions. Additional research is needed to identify
Patients who did not undergo an operating room procedure 78.8 (34 061)
Patients who underwent an operating room procedure 21.2 (9191) factors associated with the development of sepsis
Patient’s preadmission setting (n = 43 018) among patients with NV-HAP and to design and
Another acute care facility 8.3 (3605) test interventions aimed at the prevention and
Another type of health care facility 7.3 (3156) early recognition and treatment of sepsis in this
A non–health care setting 83.8 (36 257) patient population.
Patient transfer disposition at discharge (n = 43 241)
To a different acute care facility 3.8 (1654)
Limitations
To another type of health care facility 39.4 (17 029)
To a non–health care setting 56.8 (24 558) While the sampling strategy of using ICD-9
In-hospital mortality (n = 43 241) 20.5 (8847) codes to identify the NV-HAP cases has been used
a Values are percentage (number) of patients unless otherwise indicated in first
in previous research,19,25 variations in the accuracy
column. of administratively coded data (ACD) have been
well-documented.34,35 Data indicate that currently
used ACD, specifically ICD-9 coding, may have lim-
underappreciated.16,19 Additionally, it is possible that ited and variable accuracy for the identification and
recognition and treatment of NV-HAP for patients surveillance of hospital-acquired infection. In a recent
admitted with another principal diagnosis may be study36 conducted at 47 acute care hospitals in Cali-
delayed, further increasing their risk for sepsis as fornia, researchers looked at both traditional surveil-
well as other related complications. This notion is lance and claims-based surveillance for surgical site
further strengthened by findings from published infection. These researchers found that the overall
research on rapid response teams, in which data sensitivity for traditional surveillance was 50% whereas
support respiratory compromise as the most com- that of claims-based surveillance was 84%, and that
mon reason for deterioration in a patient’s condi- surveillance using both ICD-9 and ICD-10 codes
tion and initiation of the rapid response team.28-30 provided a standardized approach.36 Nevertheless,
In our descriptive review of patient characteris- given that the identification of surgical site infection
tics, we found a high need for postdischarge care in can occur in either the acute care setting before dis-
another health care facility for NV-HAP patients with charge or in the outpatient setting where the surveil-
sepsis, with a total of 17 029 lance process is less defined, these findings may have
patients with NV-HAP and limited applicability for the acute care infection sur-
Sepsis in the context of sepsis requiring additional veillance used to identify NV-HAP.
care in a health care facility
nonventilator hospital- upon hospital discharge.
Because of the secondary nature of our analyses
and the use of ACD, we were unable to confirm that
acquired pneumonia is a These findings are consis- all cases included in our analyses were correctly clas-
tent with previous research sified. Thus, we were unable to identify the impact of
significant concern. and provide evidence to any incorrectly clasified cases in our sample because
highlight that hospital- they would be the result of a coding error. One exam-
based length of stay and total charges represent ple is related to our exclusion of patients with a VAP
only a portion of the total economic impact of diagnosis. In doing so, it is possible that we may
sepsis following NV-HAP.25 have eliminated some of the most severe NV-HAP

12 AJCC AMERICAN JOURNAL OF CRITICAL CARE, January 2020, Volume 29, No. 1 www.ajcconline.org
cases, that is, those patients who had NV-HAP 6. Mariansdatter SE, Eiset AH, Søgaard KK, et al. Differences
in reported sepsis incidence according to study design: a
develop, required mechanical ventilation, and literature review. BMC Med Res Methodol. 2016;16:1-13.
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the prevalence and outcomes of infection in intensive care
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sure that the patients in this important group were 8. US Centers for Disease Control. Prevention status report,
healthcare associated infection. https://wwwn.cdc.gov/psr/
all correctly classified, and this may potentially NationalSummary/NSHAI.aspx. Published 2016.
have resulted in an underestimation of the inci- 9. Ranieri VM, Thompson BT, Barie PS, et al. Drotrecogin alfa
(activated) in adults with septic shock. N Engl J Med. 2012;
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of our sample.37,38 10. Kalil AC, Metersky ML, Klompas M, et al. Management of
adults with hospital-acquired and ventilator-associated
All things considered, because ACD is the pneumonia: 2016 clinical practice guidelines by the Infec-
approach currently used by US hospitals for pay- tious Diseases Society of America and the American Tho-
racic Society. Clin Infect Dis. 2016;63:e61-e111.
ment, ACD will continue to serve as the common 11. Magill SS, Edwards JR, Bamberg W, et al. Multistate point-
benchmark for health care–associated infection prevalence survey of health care–associated infections. N
Engl J Med. 2014;370:1198-1208.
surveillance and payment until better methods can 12. El-Solh AA. Association between pneumonia and oral care
be developed and assessed.36 The transition in US in nursing home residents. Lung. 2011;189:173.

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13. Eom JS, Lee M-S, Chun H-K, et al. The impact of a ventila-
health care from ICD-9 to ICD-10 and the increased tor bundle on preventing ventilator-associated pneumonia:
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14. Lim K-P, Kuo S-W, Ko W-J, et al. Efficacy of ventilator-
should provide improvements in the coding accu- associated pneumonia care bundle for prevention of
racy for ACD. ventilator-associated pneumonia in the surgical inten-
sive care units of a medical center. J Microbiol Immunol
Infect. 2015;48:316-321.
Conclusions 15. Viana WN, Bragazzi C, Couto de Castro JE, et al. Ventilator-
associated pneumonia prevention by education and two
In the past decade, evidence-based care practices, combined bedside strategies. Int J Qual Health Care. 2013;
including early mobilization, head-of-bed elevation, 25:308-313.
16. Davis J, Finley E. The breadth of hospital-acquired pneumo-
judicious use of proton-pump inhibitor medications, nia: non-ventilated versus ventilated patients in Pennsylva-
and standardized oral care, have reduced the inci- nia. Pa Patient Saf Advis. 2012;9:99-105.
17. DiBiase LM, Weber DJ, Sickbert-Bennett EE, et al. The growing
dence of VAP.39-41 However, because the risk of importance of non-device-associated healthcare-associated
NV-HAP has been underappreciated, patients who infections: a relative proportion and incidence study at an
academic medical center, 2008-2012. Infect Control Hosp
are not undergoing mechanical ventilation do not Epidemiol. 2014;35:200-202.
routinely receive care to prevent hospital-acquired 18. Micek ST, Chew B, Hampton N, et al. A case-control study
assessing the impact of nonventilated hospital-acquired
pneumonia. Clearly, additional research is needed pneumonia on patient outcomes. Chest. 2016;150:1008-1014.
to translate the achievements of VAP prevention into 19. Quinn B, Baker DL, Cohen S, et al. Basic nursing care to
prevent nonventilator hospital-acquired pneumonia. J Nurs
evidence-based strategies for NV-HAP prevention. Scholarsh. 2014;46:11-19.
20. Baker D, Quinn B, Ewan V, Giuliano K. Sustaining quality
ACKNOWLEDGMENT improvement: long-term reduction of non-ventilator hospital-
acquired pneumonia. J Nurs Care Qual. 2019; 34(3):223-229.
Mining of the HCUP database to create the dataset for
21. Giuliano KK. Nonventilator hospital-acquired pneumonia: where
analyses was provided by Albert Taylor, PhD. All statisti- do we go from here? Am J Infect Control. 2018;46(6):729-730.
cal analyses using SPSS were performed by Preston L. 22. Giuliano KK. Nonventilator hospital-acquired pneumonia:
Reed, PhD, statistical consultant, and reviewed by Karen epidemiology to support prevention strategies. Am J Infect
K. Giuliano, PhD, RN, and Dian Baker, PhD, RN. We would Control. 2018;46(7):847-848.
also like to acknowledge Barbara Quinn, MSN, RN, for 23. Giuliano KK, Baker D, Quinn B. The epidemiology of non-
her ongoing contributions to our collective program of ventilator hospital-acquired pneumonia in the United States.
NV-HAP research. Am J Infect Control. 2018;46(3):322-327.
24. Healthcare Cost and Utilization Project. NIS Database Docu-
mentation. https://www.hcup-us.ahrq.gov/db/nation/nis
FINANCIAL DISCLOSURES /nisdbdocumentation.jsp. Published 2013. Accessed Octo-
None reported. ber 9, 2019.
25. Thompson DA, Makary MA, Dorman T, et al. Clinical and
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tion following colon surgery and abdominal hysterectomy

C E 1.0 Hour Category A

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following objectives:
1. Describe the incidence of nonventilator hospital-acquired pneumonia (NV-HAP) in US health care.
2. Discuss the incidence of sepsis in the context of NV-HAP.
3. List the prevention strategies that have been successful in reducing ventilator-associated pneumonia.
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