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Quick-SOFA score ≥ 2 predicts prolonged hospital stay in geriatric patients with influenza infection
YAJEM-58319; No of Pages 5 American Journal of Emergency Medicine xxx (xxxx) xxx
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American Journal of Emergency Medicine journal homepage: www.elsevier.com/locate/ajem
Quick-SOFA score ≥ 2 predicts prolonged hospital stay in geriatric patients with influenza infection Chien-Chun Yeh, MD a, Yen-An Chen, MD a, Chien-Chin Hsu, MD, PhD b,c, Jiann-Hwa Chen, MD a,d, Wei-Lung Chen, MD, PhD a,d, Chien-Cheng Huang, MD, PhD b,e,f, Jui-Yuan Chung, MD a,⁎ a
Department of Emergency Medicine, Cathay General Hospital, Taipei, Taiwan Department of Emergency Medicine, Chi-Mei Medical Center, Tainan, Taiwan Department of Biotechnology, Southern Taiwan University of Science and Technology, Tainan, Taiwan d Fu Jen Catholic University School of Medicine, Taipei, Taiwan e Department of Environmental and Occupational Health, College of Medicine, National Cheng Kung University, Tainan, Taiwan f Department of Senior Services, Southern Taiwan University of Science and Technology, Tainan, Taiwan b c
a r t i c l e
i n f o
Article history: Received 17 February 2019 Received in revised form 17 June 2019 Accepted 23 June 2019 Available online xxxx Keywords: Prolonged length of stay Emergency department Geriatric Influenza Mortality Prediction qSOFA score
a b s t r a c t Purpose: The quick Sepsis-Related Organ Failure Assessment (qSOFA) score was designed to predict mortality among sepsis patients. However, it has never been used to identify prolonged length of hospital stay (pLOS) in geriatric patients with influenza infection. We conducted this study to clarify this issue. Methods: We conducted a retrospective case-control study, including geriatric patients (aged ≥ 65 years) with influenza infection visiting the emergency department (ED) of a medical center between January 01, 2010 and December 31, 2015. The included patients were divided into two groups on the basis of their qSOFA score: qSOFA b 2, and qSOFA ≥ 2. Data regarding demographics, vital signs, qSOFA score, underlying diseases, subtypes of influenza, and outcomes were included in the analysis. We investigated the association between qSOFA score ≥ 2 and pLOS (N9 days) via logistic regression. Results: Four hundred and nine geriatric patients were included in this study with a mean age of 79.5 (standard deviation [SD], 8.3) years. The median length of stay (LOS) was 7.0 (interquartile range [IQR], 4–12) days, while the rate of pLOS (N 9 days) was 32%. The median LOS in the qSOFA ≥ 2 group, 11.0 (7–15) days, was longer than the qSOFA b 2 group, 6.0 (4–10) days (p-value b0.01). Logistic regression showed that qSOFA ≥ 2 predicts pLOS with an odds ratio of 3.78 (95% confidence interval, 2.04–6.97). Conclusion: qSOFA score ≥ 2 is a prompt and simple tool to predict pLOS in geriatric patients with influenza infection. © 2019 Published by Elsevier Inc.
1. Introduction Influenza infection is capable of causing epidemic outbreaks every year during the fall and winter. As the geriatric population is more susceptible to severe infection with more complications, prolonged length of hospital stay (pLOS) is more often seen in geriatric patients than in younger populations [1]. However, because many underlying diseases can complicate the disease course, predicting how long the patient will have to stay in the hospital seems to be difficult. It will be easier for clinical physicians to predict and identify the risk of pLOS using objective parameters.
⁎ Corresponding author at: Department of Emergency Medicine, Cathay General Hospital, 280, Sec. 4, Ren'ai Rd., Da'an Dist., Taipei City 106, Taiwan. E-mail address: [email protected] (J.-Y. Chung).
The quick Sepsis-Related Organ Failure Assessment (qSOFA) score can be useful under this situation. It was originally designed to identify non-intensive care unit (ICU) septic patients who will have prolonged ICU stay and greater risk of death. The qSOFA score comprises three parameters which can be obtained easily in clinical practice. These three parameters are blood pressure (systolic blood pressure ≤ 100 mmHg), respiratory rate (≥22 breaths per min), and level of consciousness (Glasgow coma score [GCS] b15) [2]. One point is assigned to each category if it meets the criteria. Scoring two or more points indicates increased risk of mortality and prolonged ICU stay [3]. Early recognition of pLOS patients may be beneficial in optimizing treatment plans, minimizing length of stay (LOS), hospital ward and staff allocation planning, as well as lowering the risk of other hospitalacquired infections [4]. The association between qSOFA score and pLOS in geriatric patients with influenza infection has never been reported. We believe that a successful prediction of pLOS in geriatric
https://doi.org/10.1016/j.ajem.2019.06.041 0735-6757/© 2019 Published by Elsevier Inc.
Please cite this article as: C.-C. Yeh, Y.-A. Chen, C.-C. Hsu, et al., Quick-SOFA score≥2 predicts prolonged hospital stay in geriatric patients with influenza infection, American Journal of Emergency Medicine, https://doi.org/10.1016/j.ajem.2019.06.041
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C.-C. Yeh et al. / American Journal of Emergency Medicine xxx (xxxx) xxx
influenza patients may help optimizing medical resource utilization by re-allocating the hospital staffs and idle beds from other wards in advance of outbreak. Therefore, we conducted this study to clarify the association of pLOS with qSOFA score in geriatric influenza patients. 2. Methods 2.1. Study design, setting, and participants This study was conducted at an 800-bed university-affiliated medical center, in the capital city of Taiwan, Taipei. Approximately 55,000 patients visit the study emergency department (ED) annually; about 33% of these ED patients are elderly adults [5]. The study ED patients were managed by board-certified emergency physicians [6,7]. We included geriatric patients (age ≥ 65 years) who presented to the ED between January 1, 2010 and December 31, 2015, who fulfilled the following criteria: 1. Tympanic temperature ≥ 37.2 °C or an increase in baseline tympanic temperature ≥ 1.3 °C [6,7]; 2. Influenza infection defined as a positive influenza pharyngeal or throat swab rapid antigen-based test [3]. 2.2 Definition of variables and primary outcome. qSOFA score ≥ 2 was defined as a categorical variable, and the score was calculated according to the following three parameters: systolic blood pressure ≤ 100 mmHg, respiratory rate ≥ 22 breathes/min, and GCS b 15 [2]. Meanwhile, pLOS was defined as patients who stayed in the hospital for N9 days. In a Taiwanese study which included 17,250 hospitalized influenza-vaccinated elderly patients, an average LOS of 8.6 days was noted [8]. Another research in estimating annual influenza-associated hospitalizations in the United States by hospital discharge category, discharge type, and age group, showed an average LOS of 8,76 days in the ≥65-years-old age group [9]. 2.2. Data collection This study was conducted via retrospective chart review. Detailed information of geriatric patients in the ED was obtained who fulfilled the criteria of influenza infection; 479 geriatric ED patients met the criteria of influenza infection. Seventy patients who were lost to follow up, had missing data, or were transferred for treatment at other hospitals, were excluded. A total of 409 patients were eventually included. The included patients were divided into two groups on the basis of their qSOFA score: qSOFA b 2 (n = 360), and qSOFA ≥ 2 (n = 49). The controls to cases ratio was approximately 7.3: 1. Data regarding vital signs, demographic characteristics, influenza subtype, laboratory findings, past medical history, LOS, pLOS, qSOFA score, and 30-day mortality were collected by an emergency physician (Table 1). Any variable not recorded in the patient's medical chart was considered negative and will be excluded. 2.3. Ethical statement This study was approved by the Institutional Review Board of Cathay General Hospital and conducted according to the tenets of the Declaration of Helsinki. The need for informed consent from patients was waived because the present study was an observational study.
Table 1 Characteristics of geriatric patients with influenza in the emergency department Patient characteristics
Total patients (N = 409)
qSOFA ≥ 2 (N = 49)
qSOFA b 2 (N = 360)
p-Value
Age (mean ± SD) Age subgroup, % Young elderly (65–74 years) Moderately elderly (75–84 years) Old elderly (85 years) Gender male (%) Vital signs (mean ± SD) Glasgow coma scale SBP (mmHg)
79.5 ± 8.3
83.5 ± 7.4
79.0 ± 8.4
b0.01
30.6% 42.5%
16.3% 44.9%
32.5% 42.2%
0.02 0.72
26.9% 50.1%
38.8% 63.3%
25.3% 48.3%
0.04 0.05
13.9 ± 2.32 146.1 ± 30.5 98.8 ± 20.5
14.5 ± 1.5 147.9 ± 27.8 97.5 ± 19.2
b0.01 0.02 b0.01
21.2 ± 4.1 38.1 ± 0.9
10.0 ± 3.1 133.2 ± 44.0 108.6 ± 27.2 25.3 ± 6.6 38.1 ± 1.1
20.7 ± 3.4 38.2 ± 0.9
b0.01 0.64
39.8% 64.3% 15.8% 14.9% 25.1% 9.0% 27.1% 2.2%
44.9% 64.4% 13.3% 12.2% 20.4% 8.2% 16.3% 2.4%
38.9% 63.3% 34.7% 15.3% 23.3% 9.2% 17.8% 2.3%
0.02 0.87 b0.01 0.58 0.85 0.82 0.91 0.95
10.6 ± 5.8 12.1 ± 2.1 186.2 ± 158.8 1.6 ± 1.4 8.2 ± 10.1
13.0 ± 5.9 11.4 ± 2.0 213.1 ± 92.7 1.9 ± 1.5 11.3 ± 9.7
10.3 ± 5.7 12.4 ± 2.2 182.5 ± 165.7 1.6 ± 1.4 7.8 ± 10.2
0.02 0.01 0.21
68.0% 29.3% 2.7% 23.2%
59.2% 32.7% 8.2% 30.6%
69.2% 28.9% 1.9% 22.2%
0.16 0.59 0.01 0.20
67.5% 18.1% 8.3% 83.9% 82% 11% 32% 11.2% 7.0 (4–12)
83.7% 27.1% 9.1% 98% 91.7% 32.7% 59.2% 2.0% 11.0 (7–15) 16.7%
65.3% 20.6% 8.3% 81.9% 99.0% 8.3% 27.8% 18.1% 6.0 (4–10)
b0.01 0.31 0.91 b0.01 b0.01 b0.01 b0.01 b0.01 b0.01
4.1%
b0.01
Heart rate (/min) Respiratory rate (/min) Body temperature (°C) Medical history (%) Diabetes Hypertension Stroke Cancer Coronary artery disease Congestive heart failure COPD Dementia Laboratory data (mean ± SD) WBC count (×103/mm3) Hemoglobin (mg/dL) Platelet (×103/mm3) Serum creatinine (mg/dL) CRP (mg/dL) Influenza subtypes (%) Influenza A Influenza B Influenza A + B Vaccination Complications (%)a Pneumonia Urinary tract infection Sepsis Admission rate (%) Ordinary ward Intensive care unit LOS N 9 days Discharge Median LOS, days (IQR) 30-day mortality rate (%)
4.9%
0.21 0.03
qSOFA, quick Sepsis Related Organ Failure Assessment; SD, standard deviation; SBP, systolic blood pressure; COPD, chronic obstructive pulonary disease; WBC, white blood cell; CRP, C-reactive protein; LOS, length of hospital stay; IQR, interquartile range. a Not all the complications are listed in the table.
was used for categorical variables. The differences between skewed continuous variables, such as LOS, were analyzed via Mann Whitney U tests. Logistic regression was performed to identify pLOS among qSOFA score values of ≥ 1, ≥ 2, ≥ 3, and ≥ 4 (p value b 0.05) (Table 2). The Hosmer-Lemeshow goodness-of-fit test was performed to evaluate the reliability of the scoring system (Table 2). The sensitivity, specificity, positive predictive value, and negative predictive value for qSOFA score
2.4. Statistical analysis Statistical analysis was performed using SPSS 23.0 for Mac (SPSS Inc., Chicago, IL, USA). A power of 0.82 was calculated using G-Power 3.0 for Windows (University of Dusseldorf, Germany), which was adequate for detecting the statistical significance. Continuous data are presented as means ± standard deviation (SD). In the univariate analyses, independent samples t-test, or the Mann-Whitney-Wilcoxon test was used for continuous variables; Pearson's chi-square test or Fisher's exact test
Table 2 Prolonged length of hospital stay prediction using qSOFA score ≥ 2, identified by univariate logistic regression Score / criteria
B
Odds ratio
95% CI
p value
Hosmer-Lemeshow goodness of fit
qSOFA ≥ 2
1.32
3.78
2.04–6.97
b 0.01
0.84
qSOFA, quick Sepsis Related Organ Failure Assessment; CI, confidence interval.
Please cite this article as: C.-C. Yeh, Y.-A. Chen, C.-C. Hsu, et al., Quick-SOFA score≥2 predicts prolonged hospital stay in geriatric patients with influenza infection, American Journal of Emergency Medicine, https://doi.org/10.1016/j.ajem.2019.06.041
C.-C. Yeh et al. / American Journal of Emergency Medicine xxx (xxxx) xxx
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Table 3 Performance of qSOFA score ≥ 2 in predicting prolonged length of hospital stay in geriatric patients with influenza infection qSOFA ≥ 2 Sensitivity Specificity Positive predictive value Negative predictive value
0.73 (0.64–0.80) 0.41 (0.36–0.47) 0.36 (0.33–0.40) 0.77 (0.71–0.82)
qSOFA, quick sepsis related organ failure assessment.
as a predictor of pLOS were also analyzed (Table 3). The distribution of LOS and patient numbers is shown in Fig. 1. The LOS of qSOFA ≥ 2 and qSOFA b 2 are compared in Fig. 2.
3. Results We included 409 patients eventually in this study with a mean age of 79.5 ± 8.3 years. The percentages of the genders were nearly equal (50.1% and 49.9% for males and females, respectively). Among the included patients, 11.2% were discharged within 1 day, and 83.9% were admitted to the ward. LOS is skewed, and the median LOS (IQR) was 7.0 (4–12) days. The rate of pLOS (N9 days) was 32%. The average systolic blood pressure, respiratory rate and GCS was 146.1 ± 30.5 mmHg, 21.2 ± 4.1 breaths/min, and 13.9 ± 2.32, respectively. The median of qSOFA score (IQR) was 0.55 (0–1). Patients in the qSOFA ≥ 2 group were significantly older (p-value b 0.01) than the qSOFA b 2 group for 83.5 ± 7.4 and 79.0 ± 8.4. For underlying diseases, patients in the qSOFA b 2 group had more ischemic stroke for 34.7%, while more diabetes mellitus was noted in the qSOFA ≥ 2 group for 44.9%. White blood cell count and C-reactive protein level were significantly higher (p-value b 0.01) in the qSOFA ≥ 2 group, for 13.0 ± 5.9 × 103/mm3, and 11.3 ± 9.7 mg/dl, compared to the qSOFA b 2 group. Complications of pneumonia and in hospital mortality were noted for 83.7% and 16.7% in the qSOFA ≥ 2 group, which were significantly higher (both p-value b 0.01) than the qSOFA b 2 group, 65.3% and 4.1%. The median (IQR) LOS in the qSOFA ≥ 2 group was longer than the qSOFA b 2 group for 11.0 (7–15) days and 6.0 (4–10) days. The significance was b0.01, analyzed via Mann Whitney U test (Table 1, Fig. 2). All patients were treated with either oseltamivir or zanamivir immediately after the diagnoses were made.
Fig. 2. Comparison of LOS between qSOFA ≥ 2 and qSOFA b 2 via the Mann Whitney U tests. (× = mean)
80
Number of patients (n)
70 60 50 40 30 20 10 0
0
1
2
3
4
5
6
7
8 9 10 11 12 Length of hospital stay (Days)
13
14
15
16
17
18
19
20
Fig. 1. Distributioln of length of stay (LOS) and patient numbers.
Please cite this article as: C.-C. Yeh, Y.-A. Chen, C.-C. Hsu, et al., Quick-SOFA score≥2 predicts prolonged hospital stay in geriatric patients with influenza infection, American Journal of Emergency Medicine, https://doi.org/10.1016/j.ajem.2019.06.041
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C.-C. Yeh et al. / American Journal of Emergency Medicine xxx (xxxx) xxx
The area under the curve (AUC) of qSOFA score predicting pLOS in geriatric patients with influenza infection was calculated for 0.64 (95% CI: 0.58–0.70). The optimal cut-off point is qSOFA score 1.5. Logistic regression revealed that the odds ratio of qSOFA ≥ 2 for pLOS was 3.78 (95% confidence interval, 2.04–6.97) (Table 2). The HosmerLemeshow goodness-of-fit test of qSOFA ≥ 2 was 0.84. The performance assessment of qSOFA ≥ 2 as a predictor of pLOS yielded: sensitivity 73%, specificity 41%, positive predictive value 36%, and negative predictive value 77% (Table 3). 4. Discussion Older patients, unlike younger populations, are more susceptible to influenza due to various reasons, such as decreased immunity and multiple underlying co-morbidities [10,11]. When geriatric patients are infected with influenza, they are prone to have much more severe symptoms and longer disease course than younger patients [1]. During the endemic season, many influenza-infected patients were admitted to the hospital for variable days and most of them were N65-years-old [12]. Predicting pLOS among geriatric patients with influenza infection in the ED may guide us to improve medical resource management, such as in the ICU and ordinary ward [13]. For those patients who were predicted to have longer hospital stays, underlying co-morbidities and medical history were crucial. Aggressive treatment strategies including early anti-viral treatment, adequate fluid status monitoring, precautions of prolonged bed-ridden complications and strict control of blood glucose level, may increase the quality of care and speed up the recovery of this group of patients, in order to free up hospital ward space during the influenza outbreak season [1,7,8]. One Indian study discovered that lower PaO2/FiO2 ratio at admission, and the presence of organ failures predicts pLOS in influenza A (H1N1) patients [5]. However, assessment of these predictors is timeconsuming. The qSOFA score was instead primarily designed to be a simple and prompt screening tool for identifying severe septic patients outside the ICU, who are more likely to have higher risk of death and spend more days in the ICU [6]. One study showed that ED patients with suspected infection with qSOFA ≥ 2 have a median hospital LOS of 111 h, compared to 74 h for the qSOFA b 2 group [7]. However, most of the studies discussed prolonged ICU stays and mortality instead of the entire hospital LOS. In this study, we discovered that an increased qSOFA score of 2 may result in an approximately 4-fold risk for LOS N 9 days in the influenzainfected geriatric patients (Table 2). qSOFA score ≥ 2 also yielded a longer median LOS (11 days) than qSOFA score b 2 (6 days). qSOFA score ≥ 2 provided adequate sensitivity (73%) for early pLOS risk assessment [14]. Meanwhile, the negative predictive rate of pLOS was 77%, which indicate that 23% of the qSOFA score ≥ 2 influenza infected geriatric patients, who were initially predicted LOS b 9 days, actually had pLOS [15]. Once recognizing patients with assumed pLOS, extra works in order to hasten patients' recovery can be put into action: Firstly, selecting a more effective antiviral drug, for example Peramivir. Peramivir can be the choice of antiviral agent in such circumstances, as one study indicated that Peramivir may reduce the time to alleviation of fever [16]; Another study showed lesser adverse events (2.2% to 13.0%) and lesser complications (8.7% to 13.0%) in patients treated with Peramivir, compared with Oseltamivir [17]. Secondly, aggressive patient monitoring, for instance, checking vital signs, input output and laboratory data frequently, may assist in identification of early disease deterioration, and perhaps result in better prognosis [18]. Finally, appropriate use of medical resources, such as assigning more staffs to the influenza ward and open more wards for isolating influenza patients in order to avoid cross transmission. Good critical care requires more medical resources in the outbreak season, especially in the areas of limited medical resources. Thus, early recognition of these patients, estimation of the numbers and trends will help managing medical resources appropriately.
The major strength of this study is that it is the first study to identify the relation between qSOFA score and pLOS in geriatric ED patients with influenza infection. There are also some limitations to this study. First, due to the retrospective nature of the study, missing data are inevitable as some of the patients might be discharged or transferred to other hospitals against advice during hospitalization. Second, the overall LOS may be longer in this study, which is because the study took place in a medical center, and the patients' conditions may be more complex. Third, influenza was diagnosed by nasal or pharyngeal swab rapid antigenbased test in this study, which is a practical but not the most accurate method of diagnosing influenza, and may probably underestimate or overestimate the actual geriatric influenza infection population, due to including or excluding the false positive and false negative flu test result patients [19,20]. Fourth, the sample size of this study may not be sufficient to yield good statistical power. Subsequent studies recruiting more patients across different levels of hospitals are warranted in the future.
5. Conclusions qSOFA score ≥ 2 is a simple and prompt tool to predict a nearly 4-fold risk for pLOS among geriatric influenza patients in the ED. Early intensive monitoring and caring, early administration of effective antiviral agents, and early proper medical resources management are critical in treating geriatric influenza patients with qSOFA score ≥ 2. Further studies are warranted to validate the findings of this study. Acknowledgment Not applicable. Funding This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. Author contributions CCY, YAC, JYC, CC Hsu and CC Huang, designed and conceived this study and wrote the manuscript. JYC performed the statistical analysis. JHC and WLC provided professional suggestions and wrote the manuscript. All authors read and approved the final manuscript. References [1] Lee N, Chan PK, Choi KW, Lui G, Wong B, Cockram CS, Hui DS, Lai R, Tang JW, Sung JJ. Factors associated with early hospital discharge of adult influenza patients. [2] Singer M, Deutschman CS, Seymour CW, Shankar-Hari M, Annane D, Bauer M, et al. The third international consensus definitions for sepsis and septic shock (sepsis-3). JAMA 2016;315:801. [3] Goulden R, Hoyle MC, Monis J, et al. qSOFA, SIRS and NEWS for predicting inhospital mortality and ICU admission in emergency admissions treated as sepsis. Emerg Med J 2018;35(6):345–9 Jun. [4] Toh Hui Jin, BEng Zhen Yu Lim, MBBS Philip Yap, et al. Factors associated with prolonged length of stay in older patients. Singapore Med J 2017;58(3):134–8 Mar. [5] Chawla R, Kansal S, Chauhan M, Jain A, Jibhkate BN. Predictors of mortality and length of stay in hospitalized cases of 2009 influenza A (H1N1): experiences of a tertiary care center. Indian J Crit Care Med 2013;17:275–82. [6] Seymour CW, Liu V, Iwashyna TJ, et al Assessment of clinical criteria for sepsis. JAMA. doi:https://doi.org/10.1001/jama.2016.0288. [7] Canet Emmanuel, Taylor David McD, Khor Richard, Krishnan Vivek, Bellomo Rinaldo. qSOFA as predictor of mortality and prolonged ICU admission in Emergency Department patients with suspected infection. J Crit Care 2018;48:118–23. https://doi.org/ 10.1016/j.jcrc.2018.08.022 Dec. [Epub 2018 Aug 21]. [8] Wang Chong-Shan, Wang Shan-Tair, Lai Ching-Te, Lin Li-Jen, Lee Chien-Ting, Chou Pesus. Reducing major cause-specific hospitalization rates and shortening hospital stays after influenza vaccination. Clin Infect Dis 2004;39(11):1604–10 1 Dec. [9] Thompson WW, Shay DK, Weintraub E, et al. Influenza-associated hospitalizations in the United States. JAMA 2004;292(11):1333–40 Sep 15. [10] Freund Y, Lemachatti N, Krastinova E, et al. Prognostic accuracy of sepsis-3 criteria for in-hospital mortality among patients with suspected infection presenting to the emergency department. JAMA 2017;317(3):301–8 Jan 17.
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Please cite this article as: C.-C. Yeh, Y.-A. Chen, C.-C. Hsu, et al., Quick-SOFA score≥2 predicts prolonged hospital stay in geriatric patients with influenza infection, American Journal of Emergency Medicine, https://doi.org/10.1016/j.ajem.2019.06.041
Contents lists available at ScienceDirect
American Journal of Emergency Medicine journal homepage: www.elsevier.com/locate/ajem
Quick-SOFA score ≥ 2 predicts prolonged hospital stay in geriatric patients with influenza infection Chien-Chun Yeh, MD a, Yen-An Chen, MD a, Chien-Chin Hsu, MD, PhD b,c, Jiann-Hwa Chen, MD a,d, Wei-Lung Chen, MD, PhD a,d, Chien-Cheng Huang, MD, PhD b,e,f, Jui-Yuan Chung, MD a,⁎ a
Department of Emergency Medicine, Cathay General Hospital, Taipei, Taiwan Department of Emergency Medicine, Chi-Mei Medical Center, Tainan, Taiwan Department of Biotechnology, Southern Taiwan University of Science and Technology, Tainan, Taiwan d Fu Jen Catholic University School of Medicine, Taipei, Taiwan e Department of Environmental and Occupational Health, College of Medicine, National Cheng Kung University, Tainan, Taiwan f Department of Senior Services, Southern Taiwan University of Science and Technology, Tainan, Taiwan b c
a r t i c l e
i n f o
Article history: Received 17 February 2019 Received in revised form 17 June 2019 Accepted 23 June 2019 Available online xxxx Keywords: Prolonged length of stay Emergency department Geriatric Influenza Mortality Prediction qSOFA score
a b s t r a c t Purpose: The quick Sepsis-Related Organ Failure Assessment (qSOFA) score was designed to predict mortality among sepsis patients. However, it has never been used to identify prolonged length of hospital stay (pLOS) in geriatric patients with influenza infection. We conducted this study to clarify this issue. Methods: We conducted a retrospective case-control study, including geriatric patients (aged ≥ 65 years) with influenza infection visiting the emergency department (ED) of a medical center between January 01, 2010 and December 31, 2015. The included patients were divided into two groups on the basis of their qSOFA score: qSOFA b 2, and qSOFA ≥ 2. Data regarding demographics, vital signs, qSOFA score, underlying diseases, subtypes of influenza, and outcomes were included in the analysis. We investigated the association between qSOFA score ≥ 2 and pLOS (N9 days) via logistic regression. Results: Four hundred and nine geriatric patients were included in this study with a mean age of 79.5 (standard deviation [SD], 8.3) years. The median length of stay (LOS) was 7.0 (interquartile range [IQR], 4–12) days, while the rate of pLOS (N 9 days) was 32%. The median LOS in the qSOFA ≥ 2 group, 11.0 (7–15) days, was longer than the qSOFA b 2 group, 6.0 (4–10) days (p-value b0.01). Logistic regression showed that qSOFA ≥ 2 predicts pLOS with an odds ratio of 3.78 (95% confidence interval, 2.04–6.97). Conclusion: qSOFA score ≥ 2 is a prompt and simple tool to predict pLOS in geriatric patients with influenza infection. © 2019 Published by Elsevier Inc.
1. Introduction Influenza infection is capable of causing epidemic outbreaks every year during the fall and winter. As the geriatric population is more susceptible to severe infection with more complications, prolonged length of hospital stay (pLOS) is more often seen in geriatric patients than in younger populations [1]. However, because many underlying diseases can complicate the disease course, predicting how long the patient will have to stay in the hospital seems to be difficult. It will be easier for clinical physicians to predict and identify the risk of pLOS using objective parameters.
⁎ Corresponding author at: Department of Emergency Medicine, Cathay General Hospital, 280, Sec. 4, Ren'ai Rd., Da'an Dist., Taipei City 106, Taiwan. E-mail address: [email protected] (J.-Y. Chung).
The quick Sepsis-Related Organ Failure Assessment (qSOFA) score can be useful under this situation. It was originally designed to identify non-intensive care unit (ICU) septic patients who will have prolonged ICU stay and greater risk of death. The qSOFA score comprises three parameters which can be obtained easily in clinical practice. These three parameters are blood pressure (systolic blood pressure ≤ 100 mmHg), respiratory rate (≥22 breaths per min), and level of consciousness (Glasgow coma score [GCS] b15) [2]. One point is assigned to each category if it meets the criteria. Scoring two or more points indicates increased risk of mortality and prolonged ICU stay [3]. Early recognition of pLOS patients may be beneficial in optimizing treatment plans, minimizing length of stay (LOS), hospital ward and staff allocation planning, as well as lowering the risk of other hospitalacquired infections [4]. The association between qSOFA score and pLOS in geriatric patients with influenza infection has never been reported. We believe that a successful prediction of pLOS in geriatric
https://doi.org/10.1016/j.ajem.2019.06.041 0735-6757/© 2019 Published by Elsevier Inc.
Please cite this article as: C.-C. Yeh, Y.-A. Chen, C.-C. Hsu, et al., Quick-SOFA score≥2 predicts prolonged hospital stay in geriatric patients with influenza infection, American Journal of Emergency Medicine, https://doi.org/10.1016/j.ajem.2019.06.041
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influenza patients may help optimizing medical resource utilization by re-allocating the hospital staffs and idle beds from other wards in advance of outbreak. Therefore, we conducted this study to clarify the association of pLOS with qSOFA score in geriatric influenza patients. 2. Methods 2.1. Study design, setting, and participants This study was conducted at an 800-bed university-affiliated medical center, in the capital city of Taiwan, Taipei. Approximately 55,000 patients visit the study emergency department (ED) annually; about 33% of these ED patients are elderly adults [5]. The study ED patients were managed by board-certified emergency physicians [6,7]. We included geriatric patients (age ≥ 65 years) who presented to the ED between January 1, 2010 and December 31, 2015, who fulfilled the following criteria: 1. Tympanic temperature ≥ 37.2 °C or an increase in baseline tympanic temperature ≥ 1.3 °C [6,7]; 2. Influenza infection defined as a positive influenza pharyngeal or throat swab rapid antigen-based test [3]. 2.2 Definition of variables and primary outcome. qSOFA score ≥ 2 was defined as a categorical variable, and the score was calculated according to the following three parameters: systolic blood pressure ≤ 100 mmHg, respiratory rate ≥ 22 breathes/min, and GCS b 15 [2]. Meanwhile, pLOS was defined as patients who stayed in the hospital for N9 days. In a Taiwanese study which included 17,250 hospitalized influenza-vaccinated elderly patients, an average LOS of 8.6 days was noted [8]. Another research in estimating annual influenza-associated hospitalizations in the United States by hospital discharge category, discharge type, and age group, showed an average LOS of 8,76 days in the ≥65-years-old age group [9]. 2.2. Data collection This study was conducted via retrospective chart review. Detailed information of geriatric patients in the ED was obtained who fulfilled the criteria of influenza infection; 479 geriatric ED patients met the criteria of influenza infection. Seventy patients who were lost to follow up, had missing data, or were transferred for treatment at other hospitals, were excluded. A total of 409 patients were eventually included. The included patients were divided into two groups on the basis of their qSOFA score: qSOFA b 2 (n = 360), and qSOFA ≥ 2 (n = 49). The controls to cases ratio was approximately 7.3: 1. Data regarding vital signs, demographic characteristics, influenza subtype, laboratory findings, past medical history, LOS, pLOS, qSOFA score, and 30-day mortality were collected by an emergency physician (Table 1). Any variable not recorded in the patient's medical chart was considered negative and will be excluded. 2.3. Ethical statement This study was approved by the Institutional Review Board of Cathay General Hospital and conducted according to the tenets of the Declaration of Helsinki. The need for informed consent from patients was waived because the present study was an observational study.
Table 1 Characteristics of geriatric patients with influenza in the emergency department Patient characteristics
Total patients (N = 409)
qSOFA ≥ 2 (N = 49)
qSOFA b 2 (N = 360)
p-Value
Age (mean ± SD) Age subgroup, % Young elderly (65–74 years) Moderately elderly (75–84 years) Old elderly (85 years) Gender male (%) Vital signs (mean ± SD) Glasgow coma scale SBP (mmHg)
79.5 ± 8.3
83.5 ± 7.4
79.0 ± 8.4
b0.01
30.6% 42.5%
16.3% 44.9%
32.5% 42.2%
0.02 0.72
26.9% 50.1%
38.8% 63.3%
25.3% 48.3%
0.04 0.05
13.9 ± 2.32 146.1 ± 30.5 98.8 ± 20.5
14.5 ± 1.5 147.9 ± 27.8 97.5 ± 19.2
b0.01 0.02 b0.01
21.2 ± 4.1 38.1 ± 0.9
10.0 ± 3.1 133.2 ± 44.0 108.6 ± 27.2 25.3 ± 6.6 38.1 ± 1.1
20.7 ± 3.4 38.2 ± 0.9
b0.01 0.64
39.8% 64.3% 15.8% 14.9% 25.1% 9.0% 27.1% 2.2%
44.9% 64.4% 13.3% 12.2% 20.4% 8.2% 16.3% 2.4%
38.9% 63.3% 34.7% 15.3% 23.3% 9.2% 17.8% 2.3%
0.02 0.87 b0.01 0.58 0.85 0.82 0.91 0.95
10.6 ± 5.8 12.1 ± 2.1 186.2 ± 158.8 1.6 ± 1.4 8.2 ± 10.1
13.0 ± 5.9 11.4 ± 2.0 213.1 ± 92.7 1.9 ± 1.5 11.3 ± 9.7
10.3 ± 5.7 12.4 ± 2.2 182.5 ± 165.7 1.6 ± 1.4 7.8 ± 10.2
0.02 0.01 0.21
68.0% 29.3% 2.7% 23.2%
59.2% 32.7% 8.2% 30.6%
69.2% 28.9% 1.9% 22.2%
0.16 0.59 0.01 0.20
67.5% 18.1% 8.3% 83.9% 82% 11% 32% 11.2% 7.0 (4–12)
83.7% 27.1% 9.1% 98% 91.7% 32.7% 59.2% 2.0% 11.0 (7–15) 16.7%
65.3% 20.6% 8.3% 81.9% 99.0% 8.3% 27.8% 18.1% 6.0 (4–10)
b0.01 0.31 0.91 b0.01 b0.01 b0.01 b0.01 b0.01 b0.01
4.1%
b0.01
Heart rate (/min) Respiratory rate (/min) Body temperature (°C) Medical history (%) Diabetes Hypertension Stroke Cancer Coronary artery disease Congestive heart failure COPD Dementia Laboratory data (mean ± SD) WBC count (×103/mm3) Hemoglobin (mg/dL) Platelet (×103/mm3) Serum creatinine (mg/dL) CRP (mg/dL) Influenza subtypes (%) Influenza A Influenza B Influenza A + B Vaccination Complications (%)a Pneumonia Urinary tract infection Sepsis Admission rate (%) Ordinary ward Intensive care unit LOS N 9 days Discharge Median LOS, days (IQR) 30-day mortality rate (%)
4.9%
0.21 0.03
qSOFA, quick Sepsis Related Organ Failure Assessment; SD, standard deviation; SBP, systolic blood pressure; COPD, chronic obstructive pulonary disease; WBC, white blood cell; CRP, C-reactive protein; LOS, length of hospital stay; IQR, interquartile range. a Not all the complications are listed in the table.
was used for categorical variables. The differences between skewed continuous variables, such as LOS, were analyzed via Mann Whitney U tests. Logistic regression was performed to identify pLOS among qSOFA score values of ≥ 1, ≥ 2, ≥ 3, and ≥ 4 (p value b 0.05) (Table 2). The Hosmer-Lemeshow goodness-of-fit test was performed to evaluate the reliability of the scoring system (Table 2). The sensitivity, specificity, positive predictive value, and negative predictive value for qSOFA score
2.4. Statistical analysis Statistical analysis was performed using SPSS 23.0 for Mac (SPSS Inc., Chicago, IL, USA). A power of 0.82 was calculated using G-Power 3.0 for Windows (University of Dusseldorf, Germany), which was adequate for detecting the statistical significance. Continuous data are presented as means ± standard deviation (SD). In the univariate analyses, independent samples t-test, or the Mann-Whitney-Wilcoxon test was used for continuous variables; Pearson's chi-square test or Fisher's exact test
Table 2 Prolonged length of hospital stay prediction using qSOFA score ≥ 2, identified by univariate logistic regression Score / criteria
B
Odds ratio
95% CI
p value
Hosmer-Lemeshow goodness of fit
qSOFA ≥ 2
1.32
3.78
2.04–6.97
b 0.01
0.84
qSOFA, quick Sepsis Related Organ Failure Assessment; CI, confidence interval.
Please cite this article as: C.-C. Yeh, Y.-A. Chen, C.-C. Hsu, et al., Quick-SOFA score≥2 predicts prolonged hospital stay in geriatric patients with influenza infection, American Journal of Emergency Medicine, https://doi.org/10.1016/j.ajem.2019.06.041
C.-C. Yeh et al. / American Journal of Emergency Medicine xxx (xxxx) xxx
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Table 3 Performance of qSOFA score ≥ 2 in predicting prolonged length of hospital stay in geriatric patients with influenza infection qSOFA ≥ 2 Sensitivity Specificity Positive predictive value Negative predictive value
0.73 (0.64–0.80) 0.41 (0.36–0.47) 0.36 (0.33–0.40) 0.77 (0.71–0.82)
qSOFA, quick sepsis related organ failure assessment.
as a predictor of pLOS were also analyzed (Table 3). The distribution of LOS and patient numbers is shown in Fig. 1. The LOS of qSOFA ≥ 2 and qSOFA b 2 are compared in Fig. 2.
3. Results We included 409 patients eventually in this study with a mean age of 79.5 ± 8.3 years. The percentages of the genders were nearly equal (50.1% and 49.9% for males and females, respectively). Among the included patients, 11.2% were discharged within 1 day, and 83.9% were admitted to the ward. LOS is skewed, and the median LOS (IQR) was 7.0 (4–12) days. The rate of pLOS (N9 days) was 32%. The average systolic blood pressure, respiratory rate and GCS was 146.1 ± 30.5 mmHg, 21.2 ± 4.1 breaths/min, and 13.9 ± 2.32, respectively. The median of qSOFA score (IQR) was 0.55 (0–1). Patients in the qSOFA ≥ 2 group were significantly older (p-value b 0.01) than the qSOFA b 2 group for 83.5 ± 7.4 and 79.0 ± 8.4. For underlying diseases, patients in the qSOFA b 2 group had more ischemic stroke for 34.7%, while more diabetes mellitus was noted in the qSOFA ≥ 2 group for 44.9%. White blood cell count and C-reactive protein level were significantly higher (p-value b 0.01) in the qSOFA ≥ 2 group, for 13.0 ± 5.9 × 103/mm3, and 11.3 ± 9.7 mg/dl, compared to the qSOFA b 2 group. Complications of pneumonia and in hospital mortality were noted for 83.7% and 16.7% in the qSOFA ≥ 2 group, which were significantly higher (both p-value b 0.01) than the qSOFA b 2 group, 65.3% and 4.1%. The median (IQR) LOS in the qSOFA ≥ 2 group was longer than the qSOFA b 2 group for 11.0 (7–15) days and 6.0 (4–10) days. The significance was b0.01, analyzed via Mann Whitney U test (Table 1, Fig. 2). All patients were treated with either oseltamivir or zanamivir immediately after the diagnoses were made.
Fig. 2. Comparison of LOS between qSOFA ≥ 2 and qSOFA b 2 via the Mann Whitney U tests. (× = mean)
80
Number of patients (n)
70 60 50 40 30 20 10 0
0
1
2
3
4
5
6
7
8 9 10 11 12 Length of hospital stay (Days)
13
14
15
16
17
18
19
20
Fig. 1. Distributioln of length of stay (LOS) and patient numbers.
Please cite this article as: C.-C. Yeh, Y.-A. Chen, C.-C. Hsu, et al., Quick-SOFA score≥2 predicts prolonged hospital stay in geriatric patients with influenza infection, American Journal of Emergency Medicine, https://doi.org/10.1016/j.ajem.2019.06.041
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C.-C. Yeh et al. / American Journal of Emergency Medicine xxx (xxxx) xxx
The area under the curve (AUC) of qSOFA score predicting pLOS in geriatric patients with influenza infection was calculated for 0.64 (95% CI: 0.58–0.70). The optimal cut-off point is qSOFA score 1.5. Logistic regression revealed that the odds ratio of qSOFA ≥ 2 for pLOS was 3.78 (95% confidence interval, 2.04–6.97) (Table 2). The HosmerLemeshow goodness-of-fit test of qSOFA ≥ 2 was 0.84. The performance assessment of qSOFA ≥ 2 as a predictor of pLOS yielded: sensitivity 73%, specificity 41%, positive predictive value 36%, and negative predictive value 77% (Table 3). 4. Discussion Older patients, unlike younger populations, are more susceptible to influenza due to various reasons, such as decreased immunity and multiple underlying co-morbidities [10,11]. When geriatric patients are infected with influenza, they are prone to have much more severe symptoms and longer disease course than younger patients [1]. During the endemic season, many influenza-infected patients were admitted to the hospital for variable days and most of them were N65-years-old [12]. Predicting pLOS among geriatric patients with influenza infection in the ED may guide us to improve medical resource management, such as in the ICU and ordinary ward [13]. For those patients who were predicted to have longer hospital stays, underlying co-morbidities and medical history were crucial. Aggressive treatment strategies including early anti-viral treatment, adequate fluid status monitoring, precautions of prolonged bed-ridden complications and strict control of blood glucose level, may increase the quality of care and speed up the recovery of this group of patients, in order to free up hospital ward space during the influenza outbreak season [1,7,8]. One Indian study discovered that lower PaO2/FiO2 ratio at admission, and the presence of organ failures predicts pLOS in influenza A (H1N1) patients [5]. However, assessment of these predictors is timeconsuming. The qSOFA score was instead primarily designed to be a simple and prompt screening tool for identifying severe septic patients outside the ICU, who are more likely to have higher risk of death and spend more days in the ICU [6]. One study showed that ED patients with suspected infection with qSOFA ≥ 2 have a median hospital LOS of 111 h, compared to 74 h for the qSOFA b 2 group [7]. However, most of the studies discussed prolonged ICU stays and mortality instead of the entire hospital LOS. In this study, we discovered that an increased qSOFA score of 2 may result in an approximately 4-fold risk for LOS N 9 days in the influenzainfected geriatric patients (Table 2). qSOFA score ≥ 2 also yielded a longer median LOS (11 days) than qSOFA score b 2 (6 days). qSOFA score ≥ 2 provided adequate sensitivity (73%) for early pLOS risk assessment [14]. Meanwhile, the negative predictive rate of pLOS was 77%, which indicate that 23% of the qSOFA score ≥ 2 influenza infected geriatric patients, who were initially predicted LOS b 9 days, actually had pLOS [15]. Once recognizing patients with assumed pLOS, extra works in order to hasten patients' recovery can be put into action: Firstly, selecting a more effective antiviral drug, for example Peramivir. Peramivir can be the choice of antiviral agent in such circumstances, as one study indicated that Peramivir may reduce the time to alleviation of fever [16]; Another study showed lesser adverse events (2.2% to 13.0%) and lesser complications (8.7% to 13.0%) in patients treated with Peramivir, compared with Oseltamivir [17]. Secondly, aggressive patient monitoring, for instance, checking vital signs, input output and laboratory data frequently, may assist in identification of early disease deterioration, and perhaps result in better prognosis [18]. Finally, appropriate use of medical resources, such as assigning more staffs to the influenza ward and open more wards for isolating influenza patients in order to avoid cross transmission. Good critical care requires more medical resources in the outbreak season, especially in the areas of limited medical resources. Thus, early recognition of these patients, estimation of the numbers and trends will help managing medical resources appropriately.
The major strength of this study is that it is the first study to identify the relation between qSOFA score and pLOS in geriatric ED patients with influenza infection. There are also some limitations to this study. First, due to the retrospective nature of the study, missing data are inevitable as some of the patients might be discharged or transferred to other hospitals against advice during hospitalization. Second, the overall LOS may be longer in this study, which is because the study took place in a medical center, and the patients' conditions may be more complex. Third, influenza was diagnosed by nasal or pharyngeal swab rapid antigenbased test in this study, which is a practical but not the most accurate method of diagnosing influenza, and may probably underestimate or overestimate the actual geriatric influenza infection population, due to including or excluding the false positive and false negative flu test result patients [19,20]. Fourth, the sample size of this study may not be sufficient to yield good statistical power. Subsequent studies recruiting more patients across different levels of hospitals are warranted in the future.
5. Conclusions qSOFA score ≥ 2 is a simple and prompt tool to predict a nearly 4-fold risk for pLOS among geriatric influenza patients in the ED. Early intensive monitoring and caring, early administration of effective antiviral agents, and early proper medical resources management are critical in treating geriatric influenza patients with qSOFA score ≥ 2. Further studies are warranted to validate the findings of this study. Acknowledgment Not applicable. Funding This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. Author contributions CCY, YAC, JYC, CC Hsu and CC Huang, designed and conceived this study and wrote the manuscript. JYC performed the statistical analysis. JHC and WLC provided professional suggestions and wrote the manuscript. All authors read and approved the final manuscript. References [1] Lee N, Chan PK, Choi KW, Lui G, Wong B, Cockram CS, Hui DS, Lai R, Tang JW, Sung JJ. Factors associated with early hospital discharge of adult influenza patients. [2] Singer M, Deutschman CS, Seymour CW, Shankar-Hari M, Annane D, Bauer M, et al. The third international consensus definitions for sepsis and septic shock (sepsis-3). JAMA 2016;315:801. [3] Goulden R, Hoyle MC, Monis J, et al. qSOFA, SIRS and NEWS for predicting inhospital mortality and ICU admission in emergency admissions treated as sepsis. Emerg Med J 2018;35(6):345–9 Jun. [4] Toh Hui Jin, BEng Zhen Yu Lim, MBBS Philip Yap, et al. Factors associated with prolonged length of stay in older patients. Singapore Med J 2017;58(3):134–8 Mar. [5] Chawla R, Kansal S, Chauhan M, Jain A, Jibhkate BN. Predictors of mortality and length of stay in hospitalized cases of 2009 influenza A (H1N1): experiences of a tertiary care center. Indian J Crit Care Med 2013;17:275–82. [6] Seymour CW, Liu V, Iwashyna TJ, et al Assessment of clinical criteria for sepsis. JAMA. doi:https://doi.org/10.1001/jama.2016.0288. [7] Canet Emmanuel, Taylor David McD, Khor Richard, Krishnan Vivek, Bellomo Rinaldo. qSOFA as predictor of mortality and prolonged ICU admission in Emergency Department patients with suspected infection. J Crit Care 2018;48:118–23. https://doi.org/ 10.1016/j.jcrc.2018.08.022 Dec. [Epub 2018 Aug 21]. [8] Wang Chong-Shan, Wang Shan-Tair, Lai Ching-Te, Lin Li-Jen, Lee Chien-Ting, Chou Pesus. Reducing major cause-specific hospitalization rates and shortening hospital stays after influenza vaccination. Clin Infect Dis 2004;39(11):1604–10 1 Dec. [9] Thompson WW, Shay DK, Weintraub E, et al. Influenza-associated hospitalizations in the United States. JAMA 2004;292(11):1333–40 Sep 15. [10] Freund Y, Lemachatti N, Krastinova E, et al. Prognostic accuracy of sepsis-3 criteria for in-hospital mortality among patients with suspected infection presenting to the emergency department. JAMA 2017;317(3):301–8 Jan 17.
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Please cite this article as: C.-C. Yeh, Y.-A. Chen, C.-C. Hsu, et al., Quick-SOFA score≥2 predicts prolonged hospital stay in geriatric patients with influenza infection, American Journal of Emergency Medicine, https://doi.org/10.1016/j.ajem.2019.06.041