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The Pediatric Infectious Disease Journal • Volume 38, Number 3, March 2019 Risk Factors for Severe CAP
Patients who fulfilled all the following criteria were considered Institute Review Board at the School of Public Health, Fudan Uni-
as eligible: (1) date of admission between January 1, 2010, and versity and the Institute Review Board at SCH.
December 31, 2014; (2) between 29 days to < 5 years of age; (3)
household registered residents of Suzhou downtown area; (4) with
RESULTS
discharge diagnosis ICD-10 codes containing J09-J18 (influenza
and pneumonia) and J20-J22 (other acute lower respiratory infec- Study Subjects
tions). Basic information about demography and hospitalization A total of 185,750 records of pediatric patients at SCH from
could be directly exported from the hospital information system January 1, 2010, to December 31, 2014, were screened. Based on
database; these data included admission number, date of admission, the exclusion criteria including diagnosis, residence and previous
date of discharge, date of birth, gender, address, discharge diagno- admission within 30 days, 28,043 (15.1%) children were catego-
ses and ICD-10 codes, prognosis and medical insurance. rized as cases of CAP and enrolled into this study.
Review of individual medical charts was performed for these Of the 28,043 children with CAP, 17,501 (62.4%) were
eligible subjects by trained investigators applying a predesigned male, 20,747 (74.0%) children were < 24 months of age and
case report form. During this procedure, the detailed informa- 14,887 (53.1%) children were < 12 months of age. Age distribu-
tion, such as previous admission, gestational weeks, birth weight, tion between male and female children was significantly different
congenital heart disease, asthma, clinical symptoms at admission (χ2 = 242.6; P < 0.001). Overall, 13,160 children (46.9%) had med-
including fever (axillary temperature ≥ 37.5°C), cough, wheeze, ical insurance, and female children had greater coverage (χ2 = 14.1;
tachypnea (< 2 m, > 60 breaths/min; 2- < 12 m, > 50 breaths/min; P < 0.001). Prematurity, congenital heart diseases, low birth weight
1- < 5 y, > 40 breaths/min; ≥ 5 y, > 20 breaths/min), dyspnea and and asthma were observed in 1,718 (6.3%), 1,668 (5.9%), 1,441
chest indrawing, blood biochemical examination results (including (5.5%) and 658 (2.3%) children, respectively. There were no sig-
white blood cell count [WBC] and C-reactive protein [CRP]), chest nificant differences in prematurity, low birth weight and asthma
radiograph (CXR) results, complications (an unexpected illness, between male and female children while congenital heart disease
symptoms or consequence of the current CAP episode), therapeu- was more frequent in female children (χ2 =8.8; P = 0.003). In total,
tics (including antibiotics, antivirals, supplemental oxygen and ICU 671 (2.4%) children experienced ICU admission; male children
admission), and outcome were abstracted from the individual medi- were more likely to be transferred to ICU than female children
cal charts. The blood biochemical examination and CXRs within 72 (χ2 = 5.2; P = 0.023; Table 1).
hours before or after admission were assessed, and WBC < 5 or >
12 × 109/L, CRP > 8 mg/L, CXRs with consolidation, alveolar infil- Clinical Characteristics
trates or pleural fluid were defined as abnormal results. Among the 28,043 CAP cases, the most frequent clinical
After the medical chart review, patients without previous symptom at admission was cough, occurring in 26,427 (94.8%)
admissions for the same ICD-10 code within the last 30 days were children, followed by fever (52.9%), wheezing (37.7%) and res-
defined as CAP and enrolled into the final analysis. In this study, piratory distress symptoms (9.5%) including tachypnea, dyspnea
cured and improved prognoses were considered as fine clinical and chest indrawing. Cough occurred in over 94.0% of children in
outcome while uncured and deceased prognoses as poor clinical every age group. The incidence rate of fever significantly increased
outcome. CAP patients with treatments in the ICU during hospi- while that of respiratory distress symptoms decreased continuously
talization or poor clinical outcome at discharge were recognized with increasing age groups (Ptrend < 0.001 for both). Also, the per-
as severe CAP. centage of wheezing tended to decrease with age groups, especially
in children ≥ 6 months of age (χ2trend = 518.7; P < 0.001; Table 2).
Statistical Analysis Overall, 21,898 (78.1%) children had abnormal CXR find-
Continuous variables are described as the mean with stand- ings (radiologic evidence of pneumonia), 9,387 (34.3%) children
ard deviation or as the median with interquartile range, categorical were examined with abnormal WBC and 6,895 (25.3%) children
variables as numbers and percentages. χ2 test was used to compare with abnormal CRP level. There was a tendency for abnormal
the demographic profile and clinical characteristics. χ2 trend test CXR findings to be more frequently observed in younger children
was used to verify the age trend of these features. Univariate and while abnormal CRP level in older children (Ptrend < 0.001 for all;
multivariate analyses were conducted to explore potential risk fac- Table 2).
tors for ICU admission and poor clinical outcome among children When considering all children enrolled, 1,403 (5.0%) devel-
hospitalized with CAP. Gender, age, underlying conditions (includ- oped at least 1 complication; convulsion or shock was the most
ing congenital heart disease, asthma and prematurity), symptoms at common complication (n = 530 [1.9%]). The incidence of compli-
admission, blood biochemical examination and CXR results were cation was higher among children ≥ 12 months old when compared
included into the logistic regression model to explore risk factors with younger children. In addition, 1.0% of children developed
for requiring ICU care during hospitalization. Variables above plus heart failure, 0.8% respiratory failure, 0.7% meningitis or encepha-
complications and therapeutics were taken as independent variables litis and septicemia, 0.4% other pulmonary diseases (including pul-
into the regression model to explore risk factors for poor outcome at monary edema, empyema, atelectasis and emphysema) and 0.3%
discharge. However, there existed some multicollinearity between hydrothorax. Except for septicemia and other pulmonary diseases,
cough and antibiotics, and oxygen treatment and ICU admission, the incidence of other complications was significantly different
so we excluded cough and oxygen treatment in the final regression across age groups. It was observed that younger children were
model. All statistical tests were 2-tailed, with a significance level of more likely to develop respiratory failure and heart failure while
0.05. All statistical analyses were conducted with SPSS software hydrothorax and convulsion or shock were more frequent in older
(version 22.0, IBM, Armonk, NY). children (Ptrend < 0.001 for all; Table 2).
Antibiotics were prescribed to 26,673 children (95.3%),
Ethics Statement antivirals to 17,935 children (64.1%) and supplemental oxygen
As a retrospective study reviewing medical records, there was given to 1,861 children (6.7%). A total of 671 children (2.4%)
was no personal identifier and no patient contact involved, and an needed to be cared for in the ICU, and the majority were very young
informed consent was exempted. The study was approved by the children: 403 patients < 6 months old (60.1%) and 524 patients <
Copyright © 2018 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
Shan et al The Pediatric Infectious Disease Journal • Volume 38, Number 3, March 2019
n % n % n % χ2 P
Age
29 d to < 6 mo 8922 31.8 5758 32.9 3164 30.0 242.6 < 0.001
6 mo to < 12 mo 5965 21.3 4040 23.1 1925 18.3
12 mo to < 24 mo 5860 20.9 3662 20.9 2198 20.8
24 mo to < 60 mo 7296 26.0 4041 23.1 3255 30.9
Medical insurance
Yes 13,160 46.9 8061 46.1 5099 48.4 14.1 < 0.001
No 14,883 53.1 9440 53.9 5443 51.6
Underlying condition*
Prematurity 1718 6.3 1107 6.5 611 6.0 3.3 0.069
CHD 1668 5.9 984 5.6 684 6.5 8.8 0.003
LBW 1441 5.5 871 5.3 570 5.8 2.2 0.134
Asthma 658 2.3 414 2.4 244 2.3 0.1 0.785
Referral to ICU
Yes 671 2.4 447 2.6 224 2.1 5.2 0.023
No 27,981 97.6 17,014 97.4 10,296 97.9
*CHD means “congenital heart disease”; LBW means “low birth weight,” which was defined as birth weight < 2500 g.
TABLE 2. Clinical Characteristics of Children Hospitalized with CAP by Age Group [n(%)]
Symptoms at admission†
Cough 26,427 (94.8) 8415 (94.6) 5691 (95.8) 5465 (94.0) 6856 (94.5) 1.832 0.176
Fever 14,659 (52.9) 1886 (21.5) 3201 (54.3) 3973 (68.6) 5599 (77.4) 5378.9 < 0.001
Wheezing 10,514 (37.7) 3456 (38.9) 3106 (52.3) 2323 (40.0) 1629 (22.5) 518.7 < 0.001
Respiratory distress 2649 (9.5) 1291 (14.5) 516 (8.7) 426 (7.3) 416 (5.7) 372.5 < 0.001
Diagnostic tests‡
Abnormal CXR 21,898 (78.1) 7331 (82.2) 4692 (78.7) 4458 (76.1) 5417 (74.2) 161.9 < 0.001
Abnormal WBC 9387 (34.3) 2668 (30.5) 2320 (39.8) 1957 (34.3) 2442 (34.4) 14.1 < 0.001
CRP (> 8 mg/L) 6895 (25.3) 1156 (13.3) 1227 (21.2) 1592 (28.0) 2920 (41.0) 1631.0 < 0.001
Complications§ 1403 (5.0) 392 (4.4) 218 (3.7) 354 (6.0) 439 (6.0) 37.1 < 0.001
Convulsion or shock 530 (1.9) 62 (0.7) 86 (1.4) 174 (3.0) 208 (2.9) 132.2 < 0.001
Heart failure 279 (1.0) 168 (1.9) 46 (0.8) 37 (0.6) 28 (0.4) 93.1 < 0.001
Respiratory failure 219 (0.8) 123 (1.4) 36 (0.6) 31 (0.5) 29 (0.4) 50.6 < 0.001
Meningitis or encephalitis 202 (0.7) 43 (0.5) 30 (0.5) 64 (1.1) 65 (0.9) 16.5 < 0.001
Septicemia 191 (0.7) 69 (0.8) 39 (0.7) 38 (0.6) 45 (0.6) 1.4 0.231
Other pulmonary diseases 111 (0.4) 34 (0.4) 20 (0.3) 24 (0.4) 33 (0.5) 0.7 0.405
Hydrothorax 78 (0.3) 9 (0.1) 5 (0.1) 14 (0.2) 50 (0.7) 48.9 < 0.001
Therapeutics¶
Antibiotics 26,673 (95.3) 8468 (95.1) 5677 (95.3) 5523 (94.5) 7005 (96.3) 6.5 0.011
Antivirals 17,935 (64.1) 5345 (60.0) 3876 (65.1) 3868 (66.2) 4846 (66.6) 79.2 < 0.001
Oxygen treatment 1861 (6.7) 1087 (12.2) 300 (5.0) 254 (4.3) 220 (3.0) 551.5 < 0.001
ICU admission 671 (2.4) 403 (4.5) 121 (2.0) 77 (1.3) 70 (1.0) 232.08 < 0.001
Prognosis
Cured 1076 (3.8) 300 (3.4) 231 (3.9) 272 (4.6) 273 (3.7) 21.3 < 0.001
Improved 26,608 (94.9) 8467 (94.9) 5651 (94.7) 5525 (94.3) 6965 (95.5)
Uncured 338 (1.2) 146 (1.6) 76 (1.3) 60 (1.0) 56 (0.8)
Deceased 21 (0.1) 9 (0.1) 7 (0.1) 3 (0.1) 2 (0.0)
*The information of certain variables of some cases is missing, so the detailed information about sample sizes is as follows, fever: 27,691 (98.7%), other symptoms at admission:
27,900 (99.5%), WBC: 27,364 (97.6%), CRP: 27,264 (97.2%), antivirals: 27,976 (99.8%), other therapeutics: 27,981 (99.8%), others: 28,043 (100.0%).
†Respiratory distress symptoms including tachypnea, dyspnea and chest indrawing.
‡CXR: chest radiograph; WBC: white blood cell count; CRP: C-reactive protein. Abnormal CXR was defined as the presence of consolidation, alveolar infiltrates and/or pleural
fluid; abnormal WBC means that WBC was < 5 or > 12 × 109/L.
§Other pulmonary diseases including pulmonary edema, empyema, atelectasis and emphysema.
¶Oxygen treatment here included nasal catheter oxygen inhalation, supplemental oxygen through face mask and extracorporeal membrane oxygenation but no oxygen atomization.
12 months old (78.1%). With increasing age, the rate of antiviral Exploring Potential Risk Factors
use gradually increased, while oxygen treatment and ICU admis- For this study, referral to the ICU was considered as a
sion decreased (Ptrend < 0.001 for all; Table 2). measure of severe CAP. Univariate analysis revealed that male
At discharge, the great majority of the children were children and younger children were more likely to be referred
improved or cured (98.7%), while 338 children (1.2%) were still to the ICU. Also, children with congenital heart disease, prema-
not cured, and 21 children (0.1%) were deceased. The differences turity, respiratory distress symptoms at admission and abnor-
across age groups were statistically significant (P < 0.001; Table 2). mal WBC and CRP results were at higher risk for more severe
Copyright © 2018 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
The Pediatric Infectious Disease Journal • Volume 38, Number 3, March 2019 Risk Factors for Severe CAP
illness. Multivariable logistic regression (controlling for other We classified the prognoses of those patients who were not
variables) revealed that children with CAP younger than 12 cured or who were deceased at discharge into “poor clinical out-
months of age more frequently developed severe CAP compared come”; other prognoses were categorized into “fine clinical out-
with those ≥ 24 months of age (OR = 4.19). Congenital heart come.” We found from multivariate analysis that children under 2
disease (OR = 3.03), prematurity (OR = 1.99), abnormal WBC years of age were at higher risk to suffer poor clinical outcome than
(OR = 1.27) and abnormal CRP level (OR = 2.20), and respira- others, so were children with congenital heart diseases (OR = 2.59),
tory distress at admission (OR = 12.10) increased the risk of abnormal WBC (OR = 1.68), abnormal CRP level (OR = 1.49), any
developing severe CAP. However, children with cough at admis- complications (OR = 2.55) and ICU admission(OR = 8.87). How-
sion had lower risk to be cared for in ICU (OR = 0.28). And there ever, children with wheezing at admission (OR = 0.61), abnormal
was no relationship between gender, asthma, fever or wheezing at CXR findings (OR = 0.75), receiving antibiotics (OR = 0.42) and
admission, abnormal CXR findings and the requirement of ICU antivirals (OR = 0.72) therapeutics were more likely to be more
admission (Table 3). healthy at discharge (Table 4).
TABLE 3. Potential Risk Factors for ICU Admission Among Children Hospitalized with CAP
Non-ICU ICU
Admission Admission
COR AOR
Factors n % n % (95% CI) (95% CI) P
Gender (male) 17,014 97.4 447 2.6 1.21 (1.03–1.42) 1.18 (0.99–1.41) 0.069
Age
24 mo to < 60 mo 7207 99.0 70 1.0 1.00 1.00
12 mo to < 24 mo 5770 98.7 77 1.3 1.37 (0.99–1.90) 1.41 (1.00–2.00) 0.053
6 mo to < 12 mo 5833 98.0 121 2.0 2.14 (1.59–2.87) 1.93 (1.38–2.69) < 0.001
29 d to < 6 mo 8500 95.5 403 4.5 4.88 (3.78–6.30) 4.19 (3.10–5.66) < 0.001
Underlying condition
Prematurity 1625 95.0 85 5.0 2.41 (1.91–3.04) 1.99 (1.55–2.57) < 0.001
CHD 1527 91.8 137 8.2 4.33 (3.57–5.26) 3.03 (2.43–3.79) < 0.001
Asthma 646 98.3 11 1.7 0.69 (0.38–1.26) 1.29 (0.68–2.44) 0.439
Symptoms at admission
Cough 25,829 97.9 556 2.1 0.26 (0.21–0.32) 0.28 (0.21–0.36) < 0.001
Fever 14,381 98.2 257 1.8 0.56 (0.47–0.65) 0.74 (0.60–0.91) 0.054
Wheezing 10,233 97.4 268 2.6 1.10 (0.95–1.30) 1.25 (1.04–1.51) 0.017
Respiratory distress 2290 86.6 355 13.4 12.33 (10.53–14.44) 12.10 (8.96–16.36) < 0.001
Diagnostic tests
Abnormal CXR 21,326 97.5 543 2.5 1.19 (0.98–1.45) 1.24 (1.00–1.55) 0.056
Abnormal WBC 9098 97.0 278 3.0 1.39 (1.19–1.62) 1.27 (1.07–1.51) 0.006
CRP (> 8 mg/L) 6672 96.9 213 3.1 1.44 (1.22–1.70) 2.20 (1.79–2.70) < 0.001
TABLE 4. Potential Risk Factors for Poor Clinical Outcome Among Children Hospitalized with CAP
Fine Poor
Outcome Outcome
Gender (male) 17,280 98.7 221 1.3 0.96 (0.78–1.19) 0.96 (0.77–1.28) 0.760
Age
24 mo to < 60 mo 7238 99.2 58 0.8 1.00 1.00
12 mo to < 24 mo 5797 98.9 63 1.1 1.36 (0.95–1.94) 1.65 (1.08–2.51) 0.021
6 mo to < 12 mo 5882 98.6 83 1.4 1.76 (1.26–2.47) 1.96 (1.29–2.97) 0.001
29 d to < 6 mo 8767 98.3 155 1.7 2.21 (1.63–2.99) 1.59 (1.06–2.40) 0.025
Underlying condition
Prematurity 1694 98.6 24 1.4 1.23 (0.81–1.87) 0.87 (0.54–1.42) 0.579
CHD 1594 95.6 74 4.4 4.25 (3.30–5.52) 2.59 (1.86–3.62) < 0.001
Asthma 657 99.8 1 0.2 0.12 (0.02–0.82) 0.27 (0.04–1.96) 0.196
Symptoms at admission
Fever 14,502 98.9 157 1.1 0.72 (0.59–0.90) 0.75 (0.56–1.01) 0.056
Wheezing 10,422 99.1 92 0.9 0.58 (0.46–0.74) 0.61 (0.46–0.81) 0.001
Respiratory distress 2576 97.2 73 2.8 2.55 (1.96–3.31) 1.04 (0.72–1.51) 0.834
Diagnostic tests
Abnormal CXR 21647 98.9 251 1.1 0.65 (0.52–0.81) 0.75 (0.57–1.00) 0.049
Abnormal WBC 9225 98.3 162 1.7 1.77 (1.43–2.19) 1.68 (1.31–2.16) < 0.001
CRP (> 8 mg/L) 6788 98.4 107 1.6 1.44 (1.14–1.81) 1.49 (1.12–1.99) 0.006
Having complications 1315 93.7 88 6.3 6.51 (5.09–8.33) 2.55 (1.80–3.61) < 0.001
Therapeutics
Antibiotics 26,357 98.8 316 1.2 0.38 (0.27–0.53) 0.42 (0.27–0.65) < 0.001
Antivirals 17,760 99.0 175 1.0 0.54 (0.44–0.66) 0.72 (0.56–0.92) 0.009
ICU admission 582 86.7 89 13.3 15.49 (12.02–19.96) 8.87 (6.07–12.98) < 0.001
Copyright © 2018 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
Shan et al The Pediatric Infectious Disease Journal • Volume 38, Number 3, March 2019
Copyright © 2018 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
The Pediatric Infectious Disease Journal • Volume 38, Number 3, March 2019 Risk Factors for Severe CAP
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