Kim 

et al. BMC Pulmonary Medicine (2022) 22:21

https://doi.org/10.1186/s12890-021-01816-9

RESEARCH Open Access

Comprehensive risk assessment

for hospital‑acquired pneumonia:
sociodemographic, clinical, and hospital
environmental factors associated
with the incidence of hospital‑acquired
pneumonia
Bo‑Guen Kim1†, Minwoong Kang2,3†, Jihyun Lim3, Jin Lee3,4, Danbee Kang3,4, Minjung Kim3,4, Jinhee Kim3,
Hyejeong Park3, Kyung Hoon Min5, Juhee Cho3,4* and Kyeongman Jeon1* 

Abstract 
Background:  Social and hospital environmental factors that may be associated with hospital-acquired pneumonia
(HAP) have not been evaluated. Comprehensive risk assessment for the incidence of HAP including sociodemo‑
graphic, clinical, and hospital environmental factors was conducted using national health insurance claims data.
Methods:  This is a population-based retrospective cohort study of adult patients who were hospitalized for more
than 3 days from the Health Insurance Review and Assessment Service-National Inpatient Sample data between
January 1, 2016 and December 31, 2018 in South Korea. Multivariable logistic regression analyses were conducted to
identify the factors associated with the incidence of HAP.
Results:  Among the 512,278 hospitalizations, we identified 25,369 (5.0%) HAP cases. In multivariable analysis, well-
known risk factors associated with HAP such as older age (over 70 vs. 20–29; adjusted odds ratio [aOR], 3.66; 95% con‑
fidence interval [CI] 3.36–3.99), male sex (aOR, 1.35; 95% CI 1.32–1.39), pre-existing lung diseases (asthma [aOR, 1.73;
95% CI 1.66–1.80]; chronic obstructive pulmonary disease [aOR, 1.62; 95% CI 1.53–1.71]; chronic lower airway disease
[aOR, 1.79; 95% CI 1.73–1.85]), tube feeding (aOR, 3.32; 95% CI 3.16–3.50), suctioning (aOR, 2.34; 95% CI 2.23–2.47),
positioning (aOR, 1.63; 95% CI 1.55–1.72), use of mechanical ventilation (aOR, 2.31; 95% CI 2.15–2.47), and intensive
care unit admission (aOR, 1.29; 95% CI 1.22–1.36) were associated with the incidence of HAP. In addition, poverty (aOR,
1.08; 95% CI 1.04–1.13), general hospitals (aOR, 1.54; 95% CI 1.39–1.70), higher bed-to-nurse ratio (Grade ≥ 5; aOR,

*Correspondence: [email protected]; [email protected]

†
Bo-Guen Kim and Minwoong Kang have contributed equally to this
study
1
Division of Pulmonary and Critical Care Medicine, Department
of Medicine, Samsung Medical Center, Sungkyunkwan University School
of Medicine, 81 Irwon‑ro, Gangnam‑gu, Seoul 06351, South Korea
3
Center for Clinical Epidemiology, Samsung Medical Center, Seoul, South
Korea
Full list of author information is available at the end of the article

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Kim et al. BMC Pulmonary Medicine (2022) 22:21 Page 2 of 11

1.45; 95% CI 1.32–1.59), higher number of beds per hospital room (6 beds; aOR, 3.08; 95% CI 2.77–3.42), and ward with
caregiver (aOR, 1.19; 95% CI 1.12–1.26) were related to the incidence of HAP.
Conclusions:  The incidence of HAP was associated with various sociodemographic, clinical, and hospital environ‑
mental factors. Thus, taking a comprehensive approach to prevent and treat HAP is important.
Keywords:  Epidemiology, Hospital-acquired pneumonia, Risk factors, Mortality

Introduction factors, such as hospital type, bed-to-nurse ratio, and

Hospital-acquired pneumonia (HAP) is one of the most hospital room type, would be necessary. However, stud-
common nosocomial infections [1, 2] and is associated ies on hospital environment-associated risk factors for
with significant clinical and economic burdens, such HAP are limited. Furthermore, studies excluded poverty,
as long-term hospitalization, high medical costs, and which is a strong risk factor for other infectious diseases
increased morbidity and mortality [3–7]. From stud- [12, 13]. Thus, we conducted a comprehensive risk assess-
ies conducted worldwide, its incidence ranges from five ment, including sociodemographic, clinical, and hospital
to more than 20 cases per 1000 hospital admissions and environmental factors associated with the incidence of
from 2.5 to more than 6.1 cases per 1000 patients not HAP (Fig. 1), using national health insurance claims data.
admitted to the intensive care unit (ICU) [5, 8, 9]. In
addition, previous studies have found that older age and Methods
preexisting lung diseases, such as chronic obstructive This is a population-based retrospective cohort study
pulmonary disease (COPD), asthma, and interstitial lung based on data from the Health Insurance Review and
disease, or multiple organ system disorders increased the Assessment Service-National Inpatient Sample (HIRA-
risk of HAP [6, 8]. Moreover, aspiration, intubation, and NIS). We used the HIRA-NIS in 2016, 2017, and 2018,
mechanical ventilation (MV) were risk factors for HAP which included 13% of a representative sample of all
[10, 11]. inpatients in South Korea during the study period
Considering that HAP is an exogenous infection with [14]. The inclusion criteria were men and women aged
nosocomial pathogens acquired from the hospital envi- 18 years and older, who were hospitalized for more than
ronment, evaluating hospital environment-related risk 3  days in a tertiary or general hospital. If a patient had

Fig. 1  Comprehensive risk assessment for hospital-acquired pneumonia

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 Kim et al. BMC Pulmonary Medicine (2022) 22:21 Page 3 of 11

multiple inpatient records, we only considered the first to medical students and nurses. The location of the
episode. We excluded patients who had pneumonia hospital was categorized as Seoul metropolitan, other
within 3 months before hospitalization using codes in the metropolitan areas, and provinces. In 1999, the South
10th revision of the International Classification of Dis- Korean government implemented a new staffing policy
eases (ICD). Additionally, we excluded patients who were that differentiates nursing fees for inpatients based on
admitted to the hospital from the emergency room and the bed-to-nurse ratio, from grade 1 to grade 7. The
who were suspected of community-acquired pneumonia type of hospital room was based on the number of
(CAP). The Institutional Review Board of Samsung Med- beds (patients) per room. Wards without caregivers
ical Center approved this study and waived the require- are areas where patients are cared for by nursing staff
ment for informed consent, as only de-identified data alone and caregivers do not stay at the bedside. For the
were used (SMC201912141-HE002). analysis of the type of hospital room and wards with
caregivers, special units, such as the ICU, lead shield,
Measurement and clean room, were excluded. Detailed codes for all
We used claims data to define HAP. Patients who (1) variables in the additional Additional file  1: Table  S1
underwent chest radiography, (2) were diagnosed with (see Additional file 1).
pneumonia on the same day, and (3) received antibiot-
ics during hospitalization were considered patients with Statistical analyses
HAP. Additionally, we considered patients to have HAP if The means and standard deviations or medians and
they were diagnosed with pneumonia within 3 days after interquartile ranges were used to describe the distribu-
discharge. tion of continuous variables. To compare patients with
We included information on sociodemographic char- and without HAP, a t-test for continuous variables and
acteristics, comorbidities, procedures, prescriptions, and the chi-square test for categorical variables were used.
hospital characteristics based on claim codes. We used We performed univariate and multivariate logistic
information on the type of health insurance to describe regression analyses to identify the factors associated
people living in poverty. Approximately 97.2% of the with HAP. We used the hospital as a random intercept
South Korean population was covered by the Korean in the mixed-effects logistic model. Odds ratios (ORs)
National Health Insurance (KNHI), and the remain- with 95% confidence intervals (CIs) were estimated
ing 2.8% were covered by Medical Aid, which is a pub- using the models. We performed mixed-effects logis-
lic assistance program targeted at poor individuals who tic regression using the PROC GLIMMIX procedure
are recipients of the National Basic Livelihood Security in SAS (SAS Institute, Inc., North Carolina, USA).
System based on the Medical Care Assistance Act [15]. For the multivariable model, we adjusted for age, sex,
For this study, we considered people with Medical Aid as poverty, asthma, COPD, other chronic lower respira-
people in poverty. tory diseases, CKD, anemia, tube feeding, suctioning,
Comorbidities including asthma, COPD, other positioning, surgery, MV, year of hospitalization, hos-
chronic lower respiratory diseases, chronic kidney dis- pital location, and hospital type. Additionally, we per-
ease (CKD), and anemia were defined as the presence formed a subgroup analysis for medical and surgical
of ICD-10 codes at admission and within 3  months patients. All analyses were performed using SAS (ver-
before hospitalization. Procedures of interest dur- sion 9.4; SAS Institute, Inc., North Carolina, USA). P
ing hospitalization included tube feeding, suctioning, values of less than 0.05 were used to denote statistical
positioning care, MV for more than 3  h, surgery, and significance.
ICU admissions. For hospital environment-related
variables, the type and location of the hospital, the Results
bed-to-nurse ratio, the type of hospital room, and Baseline characteristics
ward with caregivers were considered. Hospitals were Between January, 2016 and December, 2018, 542,444
classified according to their capacity based on the patients were identified. Patients with pneumonia codes
number of hospital beds and specialties, as defined 3 months before hospitalization (n = 25,398) and patients
by the Korean Health Law [16]. General hospitals are with pneumonia and suspicious symptom codes at hos-
defined as hospitals with more than 100 beds and at pitalization from the emergency room (n = 4,768) were
least seven specialty areas, and tertiary hospitals excluded; the remaining 512,278 patients were included
should have more than 500 beds with more than 20 in the final sample (Fig. 2).
specialty departments that serve as teaching hospitals

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Kim et al. BMC Pulmonary Medicine (2022) 22:21 Page 4 of 11

Fig. 2  Flow chart of the study participants

Among the 512,278 patients, 25,369 (5.0%) had HAP. (adjusted OR, 1.63; 95% CI 1.55–1.72) were risk factors
The characteristics of the patients with HAP are pre- for HAP (Table  2). Medical patients (adjusted OR, 2.98;
sented in Table  1. The elderly group aged 70  years and 95% CI 2.87–3.09) had a higher risk of HAP than surgi-
older had a higher rate of HAP (57.0%) than the no cal patients. Additionally, MV (adjusted OR, 2.31; 95%
HAP group (28.0%) (p < 0.001). Regarding comorbid- CI 2.15–2.47) and ICU admission (adjusted OR, 1.29;
ity, patients with HAP had a higher proportion of each 95% CI 1.22–1.36) increased the risk of HAP (Table  2).
comorbidity than those without HAP, and other chronic As the bed-to-nurse ratio grade increased, the incidence
lower respiratory diseases (23.9%) were the highest in of HAP increased (Fig.  3B). Six patients sharing one
the HAP group. In the procedures of interest during hospitalization room increased the risk of developing
hospitalization, tube feeding (18.3% vs. 2.2%), suctioning HAP (adjusted OR, 3.08; 95% CI 2.77–3.42) compared
(20.0% vs. 4.1%), positioning care (25.8% vs. 7.1%), MV with using one hospitalization room with three or fewer
(11.0% vs. 1.3%), and ICU admission (27.3% vs. 9.0%) patients. Patients hospitalized in a ward with caregivers
were more frequent in the HAP group than in the no (adjusted OR, 1.19; 95% CI 1.12–1.26) were at a higher
HAP group. risk of developing HAP than those admitted in a ward
without caregivers.
We conducted a subgroup analysis involving medical
Risk factors associated with the incidence of HAP and surgical patients (Table 3). Among surgical patients,
In multivariable analysis, old age (over 70 vs. 20–29; those aged over 70 years were at a 6.7 times higher risk of
adjusted OR, 3.66; 95% CI 3.36–3.99), male sex (adjusted HAP than those aged 20–29  years. However, ward with
OR, 1.35; 95% CI 1.32–1.39), poverty (adjusted OR, 1.08; caregivers was not a significant factor for HAP in surgical
95% CI 1.04–1.13), asthma (adjusted OR, 1.73; 95% CI patients.
1.66–1.80), COPD (adjusted OR, 1.62; 95% CI 1.53–1.71),
other chronic lower respiratory diseases (adjusted OR,
1.79; 95% CI 1.73–1.85), and CKD (adjusted OR, 1.07; Discussion
95% CI 1.00–1.14) were risk factors associated with the In this study, the incidence of HAP over 3  years was
incidence of HAP (Table 2). The OR of HAP occurrence 5.0%, and older age, male sex, asthma, COPD, other
tended to increase as the age group increased (Fig.  3A). chronic lower respiratory diseases, CKD, and poverty
The association of various comorbidities with HAP were associated with the incidence of HAP. Addition-
occurrence are detailed in Additional file  2: Table  S2 ally, clinical factors, such as tube feeding, suctioning,
(see Additional file  2). Dementia (adjusted OR, 1.32; positioning, MV, and ICU admission, increased the risk
95% CI 1.27–1.38), paraplegia and hemiplegia (adjusted of HAP. In terms of the hospital environment, hospital
OR, 1.15; 95% CI 1.05–1.25), and metastatic carcinoma type, beds-to-nurse ratio, hospital room type, and ward
(adjusted OR, 1.15; 95% CI 1.06–1.25) were associated with caregivers were associated with the incidence of
with the occurrence of HAP. HAP.
Among procedures during hospitalization, tube feeding Similar to previous studies, respiratory-related comor-
(adjusted OR, 3.32; 95% CI 3.16–3.50), suction (adjusted bidity, CKD, and age were risk factors associated with the
OR, 2.34; 95% CI 2.23–2.47), and positioning care incidence of HAP in this study [8, 17, 18]. According to

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 Kim et al. BMC Pulmonary Medicine (2022) 22:21 Page 5 of 11

Table 1  Characteristics of the study participants (N = 512,278)

Variables No HAP (n = 486,909) HAP (n = 25,369) p value

Age group < 0.001

 20–29 35,400 (7.3) 604 (2.4)
 30–39 50,320 (10.3) 1022 (4.0)
 40–49 68,073 (14.0) 1610 (6.4)
 50–59 100,721 (20.7) 3191 (12.6)
 60–69 96,000 (19.7) 4495 (17.7)
 Over 70 136,395 (28.0) 14,447 (57.0)
Sex (male) 224,522 (46.1) 13,655 (53.8) < 0.001
Poverty (yes) 38,330 (7.9) 3122 (12.3) < 0.001
Asthma (yes) 33,331 (6.9) 4485 (17.7) < 0.001
COPD (yes) 14,412 (3.0) 2491 (9.8) < 0.001
Other chronic lower respiratory disease (yes) 52,745 (10.8) 6053 (23.9) < 0.001
CKD (yes) 18,098 (3.7) 1473 (5.8) < 0.001
Anemia (yes) 39,829 (8.2) 2723 (10.7) < 0.001
Tube feeding (yes) 10,663 (2.2) 4634 (18.3) < 0.001
Suctioning (yes) 19,773 (4.1) 5061 (20.0) < 0.001
Positioning (yes) 34,588 (7.1) 6534 (25.8) < 0.001
Surgery (yes) 189,888 (39.0) 4430 (17.5) < 0.001
Mechanical ventilation (yes) 6295 (1.3) 2785 (11.0) < 0.001
ICU admission (yes) 43,645 (9.0) 6935 (27.3) < 0.001
Location of hospital < 0.001
 Seoul metropolitan area 204,419 (42.0) 8997 (35.5)
 Other metropolitan area 142,073 (29.2) 7218 (28.5)
 Province 140,417 (28.8) 9154 (36.0)
Type of hospital < 0.001
 Tertiary 172,295 (35.4) 6344 (25.0)
 General 314,614 (64.6) 19,025 (75.0)
Bed-to-nurse ­ratio*(n = 425,953) < 0.001
 Grade 1 79,427 (19.6) 2671 (12.6)
 Grade 2 157,134 (38.3) 7564 (35.5)
 Grade 3 72,569 (17.9) 4291 (20.2)
 Grade 4 21,210 (5.2) 1441 (6.8)
 Grade ≥ 5 74,329 (18.4) 5317 (25.0)
Types of hospital rooms (n = 504,279) < 0.001
 ≤ 3 beds 44,027 (9.2) 383 (1.6)
 4 beds 68,876 (14.3) 3816 (16.2)
 5 beds 134,363 (28.0) 7096 (30.1)
 6 beds 233,445 (48.6) 12,273 (52.1)
Ward with or without ­caregiver† (n = 469,588) 0.498
 With caregivers 404,669 (90.7) 21,284 (90.8)
 Without carefgivers 41,487 (9.3) 2148 (9.2)
Year < 0.001
 2016 185,262 (38.1) 10,372 (40.9)
 2017 148,876 (30.6) 7624 (30.1)
 2018 152,771 (91.4) 7373 (29.1)

The values in the table are numbers (percentages)

CKD chronic kidney disease, COPD chronic obstructive pulmonary disease, HAP hospital-acquired pneumonia, ICU intensive care unit
*
Bed-to-nurse ratio grading is defined as follows: tertiary hospitals are divided into the following grades: grade 1 (a bed-to-nurse ratio of less than 2.0), grade 2 (a
bed-to-nurse ratio of 2.0–2.4), grade 3 (a bed-to-nurse ratio of 2.5–2.9), grade 4 (a bed-to-nurse ratio of 3.0–3.4), grade 5 (a bed-to-nurse ratio of 3.5–3.9), and grade 6
(a bed-to-nurse ratio of 4.0 or more). General hospitals are classified into the following grades: grade 1 (a bed-to-nurse ratio of less than 2.5), grade 2 (a bed-to-nurse
ratio of 2.5–2.9), grade 3 (a bed-to-nurse ratio of 3.0–3.4), grade 4 (a bed-to-nurse ratio of 3.5–3.9), grade 5 (a bed-to-nurse ratio of 4.0–4.4), grade 6 (a bed-to-nurse
ratio of 4.5–5.9), and grade 7 (a bed-to-nurse ratio of 6.0 or more)
†
Ward without caregiver is where patients are cared for by the nursing staff only, and caregivers do not stay at the bedside

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Kim et al. BMC Pulmonary Medicine (2022) 22:21 Page 6 of 11

a study conducted at a 1,000-bed hospital, patients aged professionals associated with better quality care than
over 60 years had a 2.8-fold higher risk of HAP than those those of general hospitals [27, 28]. Additionally, the
aged below 60  years [19]. While approximately half of bed-to-nurse ratio, which is one of the quality indica-
patients with HAP are aged below 60 years [20], evidence tors for nursing care, was associated with the incidence
on how age is associated with increased risk of HAP in of HAP. Patients who stayed in hospitals with grade 4
patients aged below 60 years is limited. In this study, we and 5 bed-to-nurse ratios had a 1.4-fold higher risk of
found a linear association between age and the incidence HAP than those in the hospital with a grade 1 bed-to-
of HAP. Compared with patients aged 20–29 years, those nurse ratio. According to the literature, nursing quality
in their 30 s, 40 s, and 50 s had 1.25-, 1.31-, and 1.60-fold and time have a direct impact on patient outcomes and
higher risks, respectively. the incidence of hospital-acquired infection [29–31].
Poverty and infectious diseases interact in complex A study found that a higher proportion of total hours
ways [21], and poverty is a well-known risk factor for of nursing care provided by registered nurses was
community-acquired pneumonia [12, 13]. According 0.59 times lower than the incidence of HAP in medi-
to previous studies, poor individuals have a higher risk cal patients [30]. Nurses would be able to spend more
of community-acquired pneumonia as they are more time and effort with fewer patients when they had to
likely to have uncontrolled chronic diseases and less care less patients.
likely to have sufficient medical resources and access to To the best of our knowledge, no study has investigated
care, resulting in longer hospital stays and higher mor- the relationship between the type of hospital room and
tality [13, 22, 23]. In this study, patients in poverty had incidence of HAP. We found that the risk of HAP was
a slightly higher risk of HAP than those not in poverty. approximately three times higher in patients who stayed
In South Korea, through the KNHI, all registered citizens in rooms with more than four beds than that in those
have access to care, and few health inequalities exist in who stayed in rooms with three or fewer beds. According
South Korea [24]. Therefore, poverty might have a greater to a meta-analysis, using a single-patient room reduced
impact on the incidence of HAP in patients in other healthcare-associated colonization of multidrug-resist-
countries where there are larger differences in access to ant pathogens by 0.52 times and bacteremia rate by 0.64
healthcare. times compared with using a multiple-patient room [32].
Studies have suggested that HAP is more commonly Patients who stay in single-patient rooms would have a
observed in medical patients than in surgical patients [8, lower risk of HAP as they have reduced direct or indirect
20], and we had similar findings. This might be because contact with the reservoir compared with those who stay
patients who are hospitalized for surgery would have suf- in multiple-patient rooms.
ficient health status to receive surgery than those who As a caregiver who is not a specialist revealed prob-
are hospitalized for medical problems [25]. However, this lems in the quality of care, infection, and safety, the
does not mean that surgical patients do not have the risk need for fundamental alternatives for private nursing
of HAP. Approximately one-fifth of patients with HAP has been raised [33, 34]. Then, it was believed that the
in this study were surgical patients and had different provision of specialized nurses contributed to reducing
risk factors for HAP. Older age had a greater impact on the incidence of HAP by minimizing various infection
the incidence of HAP in surgical patients than in medi- issues caused by the immature and inconsistent qual-
cal patients. Compared with patients aged 20–29  years ity of care from nonprofessional caregivers [34]. How-
(among surgical patients), those aged over 70 years were ever, no study has evaluated this issue. In South Korea,
at a 6.7-fold higher risk of HAP, which was much higher wards without caregivers were implemented in 2013.
than that in medical patients. Clinicians should pay more We found that patients who stayed in a ward with a car-
attention to older patients undergoing surgery to prevent egiver had a 1.19-fold higher risk of HAP than those
and manage HAP. who were cared for only by nurses. It might be impor-
In this study, the incidence of HAP in tertiary hos- tant to educate caregivers and patients regarding hand
pitals was 3.5%, whereas that in general hospitals was hygiene and other preventive behaviors to reduce the
5.7%. Similarly, the incidence of HAP in hospitals in risk of HAP. Moreover, providing care by nurses with-
Seoul was 4.2%; however, the incidence of HAP in out caregivers to patients who have a relatively higher
the province was 6.1%. This difference could be due risk of HAP would be necessary.
to differences in health resource access and quality of This study had some limitations. First, HAP defined
patient care [26]. Tertiary hospitals would have a bet- by claim codes has limited accuracy and validity. In this
ter hygiene environment and better trained healthcare study, we tried to use an operational definition of HAP

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 Kim et al. BMC Pulmonary Medicine (2022) 22:21 Page 7 of 11

Table 2  Factors associated with the incidence of hospital-acquired pneumonia

Characteristics Univariable Multivariable
OR (95% CI) Adjusted OR (95% CI)

Age group
 20–29 Reference Reference
 30–39 1.25 (1.13–1.38) 1.25 (1.13–1.39)
 40–49 1.42 (1.29–1.56) 1.31 (1.19–1.45)
 50–59 1.91 (1.75–2.09) 1.60 (1.47–1.75)
 60–69 2.91 (2.67–3.17) 2.11 (1.93–2.31)
 Over 70 6.22 (5.73–6.76) 3.66 (3.36–3.99)
Sex (male) 1.36 (1.32–1.39) 1.35 (1.32–1.39)
Poverty (yes) 1.45 (1.39–1.51) 1.08 (1.04–1.13)
Asthma (yes) 2.83 (2.73–2.93) 1.73 (1.66–1.80)
COPD (yes) 3.60 (3.44–3.77) 1.62 (1.53–1.71)
Other chronic lower respiratory disease (yes) 2.56 (2.48–2.64) 1.79 (1.73–1.85)
CKD (yes) 1.71 (1.62–1.81) 1.07 (1.00–1.14)*
Anemia (yes) 1.42 (1.36–1.48) 1.04 (1.00–1.10)†
Tube feeding (yes) 11.25 (10.82–11.71) 3.32 (3.16–3.50)
Suction (yes) 7.15 (6.89–7.42) 2.34 (2.23–2.47)
Positioning (yes) 4.71 (4.57–4.86) 1.63 (1.55–1.72)
Surgery (no) 2.76 (2.67–2.85) 2.98 (2.87–3.09)
Mechanical ventilation (yes) 11.40 (10.85–11.98) 2.31 (2.15–2.47)
ICU admission (yes) 4.22 (4.09–4.35) 1.29 (1.22–1.36)
Location of hospital
 Seoul metropolitan area Reference Reference
 Other metropolitan area 1.09 (1.05–1.14) 1.16 (1.06–1.26)
 Province 1.40 (1.35–1.45) 1.20 (1.11–1.31)
Type of hospital
 Tertiary Reference Reference
 General 1.53 (1.37–1.69) 1.54 (1.39–1.70)
Bed-to-nurse ­ratio‡ (n = 425,953)
 Grade 1 Reference Reference
 Grade 2 1.12 (1.03–1.23) 1.16 (1.06–1.27)
 Grade 3 1.36 (1.24–1.50) 1.31 (1.19–1.44)
 Grade 4 1.59 (1.42–1.78) 1.42 (1.26–1.59)
 Grade ≥ 5 1.62 (1.49–1.77) 1.45 (1.32–1.59)
Type of hospital room (n = 504,279)
 ≤ 3 beds Reference Reference
 4 beds 5.38 (4.83–5.99) 3.26 (2.92–3.64)
 5 beds 6.08 (5.48–6.76) 3.34 (3.00–3.72)
 6 beds 5.10 (4.60–5.65) 3.08 (2.77–3.42)
Ward with or without c­ aregiver§ (n = 469,588)
 With caregivers 1.09 (1.03–1.14) 1.19 (1.12–1.26)
 Without caregivers Reference Reference

The multivariable analysis included age, sex, poverty, asthma, COPD, other chronic lower respiratory diseases, CKD, anemia, tube feeding, suctioning, positioning,
surgery, mechanical ventilation, ICU admission, year of hospitalization, location of the hospital, and type of hospital
CI confidence interval; CKD, chronic kidney disease; COPD, chronic obstructive pulmonary disease; HAP, hospital-acquired pneumonia; ICU, intensive care unit; OR,
odds ratio
*
p = 0.03
†
p = 0.08
‡
Bed-to-nurse ratio grading was defined as follows: tertiary hospitals were divided into the following grades: grade 1 (a bed-to-nurse ratio of less than 2.0), grade 2 (a
bed-to-nurse ratio of 2.0–2.4), grade 3 (a bed-to-nurse ratio of 2.5–2.9), grade 4 (a bed-to-nurse ratio of 3.0–3.4), grade 5 (a bed-to-nurse ratio of 3.5–3.9), and grade 6
(a bed-to-nurse ratio of 4.0 or more). General hospitals are classified into the following grades: grade 1 (a bed-to-nurse ratio of less than 2.5), grade 2 (a bed-to-nurse
ratio of 2.5–2.9), grade 3 (a bed-to-nurse ratio of 3.0–3.4), grade 4 (a bed-to-nurse ratio of 3.5–3.9), grade 5 (a bed-to-nurse ratio of 4.0–4.4), grade 6 (a bed-to-nurse
ratio of 4.5–5.9), and grade 7 (a bed-to-nurse ratio of 6.0 or more)
§
In wards without caregivers, only the nursing staff takes care of the patients, and caregivers do not stay at the bedside

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Kim et al. BMC Pulmonary Medicine (2022) 22:21 Page 8 of 11

Fig. 3  The odds ratio of hospital-acquired pneumonia incidence according to A age and B bed-to-nurse ratio

that fitted the definition of existing guidelines, but we included only the first hospitalization in the analy-
we cannot exclude misclassification of HAP. Further- sis. This approach may underrepresent the hospitali-
more, diagnoses based on claims can differ from clini- zations of high-risk patients, such as elderly patients
cal diagnose. The HIRA database, however, is routinely or patients with multiple comorbidities, who are more
audited, and the data are considered reliable and have likely to have multiple hospitalizations.
been used in numerous peer-reviewed publications Despite these limitations, this nationwide study
[35, 36]. Second, as the HIRA database includes claims revealed the HAP incidence rate and identified factors
for the entire hospital admission period, it was not associated with the incidence of HAP. This study con-
able to establish the temporal relationship among the firmed the evidence on factors well-known in existing
factors. For example, while MV is a well-known risk studies [8, 37] and additionally found that sociodemo-
factor for HAP, patients might have MV due to HAP graphic and hospital environmental factors might be
rather than vice-versa. Further longitudinal observa- related to the incidence of HAP.
tional studies are necessary to confirm this finding.
Third, our results may not be generalizable to other Conclusions
countries with different healthcare systems. Lastly, the The incidence of HAP was associated with various soci-
patient samples in the HIRA dataset included linked odemographic, clinical, and hospital environmental fac-
data to claims accumulated over a year-long cycle, but tors. Taking a comprehensive approach to prevent and
patient data could not be linked across years. There- manage HAP is important. Thus, health professionals
fore, it is not possible to conduct research that requires should work with various stakeholders, such as hospital
long-term follow-up of patients with our data. In the management personnel and policymakers, to develop
case of repeated hospitalizations within the same year, strategies to reduce HAP.

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 Kim et al. BMC Pulmonary Medicine (2022) 22:21 Page 9 of 11

Table 3  Odds ratios (95% confidence intervals) for risk factor with hospital-acquired pneumonia during hospitalization in medical and
surgical patients
Characteristics Medical Surgical
Adjusted OR (95% CI) Adjusted OR (95% CI)

Age group
 20–29 Reference Reference
 30–39 1.26 (1.13–1.40) 1.32 (0.97–1.80)
 40–49 1.26 (1.14–1.40) 1.90 (1.44–2.52)
 50–59 1.53 (1.39–1.68) 2.37 (1.81–3.09)
 60–69 2.01 (1.83–2.20) 3.19 (2.45–4.15)
 Over 70 3.34 (3.06–3.66) 6.70 (5.17–8.70)
Sex, male 1.33 (1.29–1.37) 1.47 (1.37–1.57)
Poverty, yes 1.03 (0.99–1.08) 1.45 (1.31–1.60)
Asthma, yes 1.77 (1.69–1.85) 1.41 (1.27–1.58)
COPD, yes 1.70 (1.60–1.80) 1.20 (1.05–1.37)
Other chronic lower respiratory disease, yes 1.86 (1.79–1.93) 1.34 (1.22–1.47)
CKD, yes 1.00 (0.93–1.07) 1.34 (1.16–1.54)
Anemia, yes 1.01 (0.96–1.07) 1.20 (1.08–1.35)
Tube feeding, Yes 3.01 (2.84–3.20) 4.21 (3.82–4.64)
Suction, Yes 2.40 (2.25–2.55) 2.10 (1.92–2.31)
Positioning care, Yes 1.71 (1.61–1.81) 1.48 (1.34–1.63)
Mechanical ventilation, Yes 1.76 (1.61–1.93) 2.06 (1.85–2.29)
ICU admission 1.05 (0.99–1.12) 2.40 (2.17–2.67)
Location of hospital
 Seoul metropolitan area Reference Reference
 Other metropolitan area 1.16 (1.06–1.27) 1.11 (1.02–1.21)
 Province 1.17 (1.08–1.27) 1.42 (1.31–1.54)
Type of hospital
 Tertiary Reference Reference
 General 1.60 (1.45–1.77) 1.27 (1.18–1.37)
Bed-to-nurse ­ratio* (n = 425,953)
 Grade1 Reference Reference
 Grade2 1.22 (1.11–1.34) 1.09 (0.92–1.29)
 Grade3 1.34 (1.21–1.48) 1.27 (1.05–1.54)
 Grade4 1.42 (1.26–1.60) 1.46 (1.13–1.88)
 Grade ≥ 5 1.43 (1.29–1.58) 1.71 (1.44–2.04)
Hospitalization room (n = 504,279)
 ≤ 3 beds Reference Reference
 4 beds 3.22 (2.86–3.62) 3.65 (2.63–5.09)
 5 beds 3.22 (2.87–3.61) 3.91 (2.82–5.41)
 6 beds 3.06 (2.74–3.42) 3.53 (2.55–4.87)
Ward with or without ­caregiver† (n = 469,588)
 With caregivers 1.17 (1.10–1.25) 1.15 (0.98–1.34)
 Without caregivers Reference Reference
Year
 2016 1.30 (1.19–1.42) 1.27 (1.17–1.37)
 2017 1.17 (1.01–1.27) 1.09 (1.00–1.19)
 2018 Reference Reference

Multivariable analysis was including age, sex, poverty, asthma, COPD, other chronic lower respiratory diseases, CKD, anemia, tube feeding, suctioning, positioning,
surgery, mechanical ventilation, ICU admission, year of hospitalization, location of hospital, and type of hospital
CI confidence interval; CKD, chronic kidney disease; COPD, chronic obstructive pulmonary disease; HAP, hospital-acquired pneumonia; ICU, intensive care unit; OR,
odds ratio
*
Bed-to-nurse ratio grade is defined as follows: tertiary hospitals are divided into the following grades: grade 1 (a bed-to-nurse ratio of less than 2.0), grade 2 (a

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Kim et al. BMC Pulmonary Medicine (2022) 22:21 Page 10 of 11

Table 3  (continued)
bed-to-nurse ratio of 2.0–2.4), grade 3 (a bed-to-nurse ratio of 2.5–2.9), grade 4 (a bed-to-nurse ratio of 3.0–3.4), grade 5 (a bed-to-nurse ratio of 3.5–3.9), and grade 6
(a bed-to-nurse ratio of 4.0 or more). General hospitals are classified into the following grades: grade 1 (a bed-to-nurse ratio of less than 2.5), grade 2 (a bed-to-nurse
ratio of 2.5–2.9), grade 3 (a bed-to-nurse ratio of 3.0–3.4), grade 4 (a bed-to-nurse ratio of 3.5–3.9), grade 5 (a bed-to-nurse ratio of 4.0–4.4), grade 6 (a bed-to-nurse
ratio of 4.5–5.9), and grade 7 (a bed-to-nurse ratio of 6.0 or more)
†
Ward without caregiver is where patients are cared for by the nursing staff only, and caregivers do not stay at the bedside

4
Abbreviations  Department of Clinical Research Design and Evaluation, SAIHST, Sungk‑
CI: Confidence interval; CKD: Chronic kidney disease; COPD: Chronic obstruc‑ yunkawan University, 115 Irwon‑ro, Gangnam, Seoul 06335, South Korea.
5
tive lung disease; HAP: Hospital-acquired pneumonia; HIRA-NIS: Health insur‑  Division of Pulmonary, Allery, and Critical Care Medicine, Department of Inter‑
ance review and assessment service-national inpatient sample; ICU: Intensive nal Medicine, Korea University Guro Hospital, Seoul, South Korea.
care unit; IQR: Interquartile range; MV: Mechanical ventilation; SD: Standard
deviation; OR: Odds ratio; VAP: Ventilator-associated pneumonia. Received: 22 September 2021 Accepted: 24 December 2021

Supplementary Information
The online version contains supplementary material available at https://​doi.​
org/​10.​1186/​s12890-​021-​01816-9.
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