Associations of the serum albumin concentration

and Sequential Organ Failure Assessment score at

discharge with 1-year mortality in sepsis survivors:
A retrospective cohort study
Sang-Min Lee 
Seoul National University Bundang Hospital
You Hwan Jo 
(

emdrjyh@gmail.com
)
Seoul National University Bundang Hospital
Jae Hyuk Lee 
Seoul National University Bundang Hospital
Ji Eun Hwang 
Seoul National University Bundang Hospital
Inwon Park 
Seoul National University Bundang Hospital
Sumin Baek 
Seoul National University Bundang Hospital
Hwain Jeong 
Seoul National University Bundang Hospital
Young Woo Um 
Seoul National University Bundang Hospital
Hee Eun Kim 
Seoul National University Bundang Hospital

Research Article

Keywords: Sepsis, Survivors, Albumins, Sequential Organ Failure Assessment Score

Posted Date: September 6th, 2022

DOI: https://doi.org/10.21203/rs.3.rs-2019644/v1

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Abstract
Background

 This study was performed to investigate the predictors of 1-year mortality at discharge in sepsis
survivors.

Methods

 This study was a retrospective analysis of patients with sepsis and septic shock at a single centre.
Patients who survived hospitalization for sepsis or septic shock from January 2016 to December 2017
were included. Age; sex; body mass index (BMI); laboratory results such as blood cell count, C-reactive
protein (CRP) and albumin; and the Sequential Organ Failure Assessment (SOFA) score at the time of
discharge were compared between survivors and nonsurvivors at 1 year postdischarge. Multivariate
logistic regression was performed to identify the predictors of 1-year mortality.

Results

 During the study period, 725 survivors were included in the analysis, of whom 64 (8.8%) died within the
first year. Nonsurvivors were older and had a lower BMI and higher SOFA score at discharge than
survivors (P < 0.05). Among the laboratory results at discharge, haemoglobin, platelet counts and
albumin concentrations were lower in the nonsurvivors than in the survivors, whereas CRP was higher in
the nonsurvivors than in the survivors. In the multivariate logistic regression analysis, serum albumin <
2.5 mg/dl and a SOFA score ≥ 2 at discharge were identified as independent prognostic factors for 1-year
mortality (odds ratio 2.698, 95% confidential interval 1.488-4.883 for albumin < 2.5 mg/dl and 2.114,
1.204-3.814 for SOFA score ≥ 2, respectively).

Conclusions

 A low serum albumin concentration of < 2.5 mg/dL and high SOFA score of ≥ 2 at the time of discharge
were prognostic factors for 1-year mortality in sepsis survivors.

Background
Sepsis is a life-threatening organ dysfunction caused by a dysregulated host response to infection.[1] It
has been reported that 19.7% of all global deaths are related to sepsis, potentially accounting for 5.3
million deaths annually.[2, 3] Due to the risk of sepsis and the global burden, many studies have been
conducted to investigate appropriate management strategies and the prognostic factors.

Many studies have been performed to identify prognostic factors for mortality in sepsis. In previous

studies, age, sex, comorbidities, biomarkers, and severity of illness were identified as prognostic factors
for patients with sepsis.[4-9] However, most of the studies have mainly focused on short-term
mortality, such as 28- or 90-day mortality.

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There have been several studies about the long-term mortality of sepsis survivors after hospital
discharge. In a previous study, age, sex, race/ethnicity, severe comorbidities, dependency, nonsurgical
status, site of infection and organ dysfunction were reported to be associated with long-term mortality.
[10] However, this study was performed using data acquired within the patients’ first 24 hours following
admission and included only patients admitted to the intensive care unit (ICU). Another study used
various biomarker trajectories, such as highly sensitive C-reactive protein, interleukin-6, and soluble
programmed death ligand 1, but these markers are difficult to measure clinically.[11]

During the hospitalization period, a patient with sepsis undergoes many changes in his or her condition,
and at discharge, the condition of sepsis survivors is better than that during their hospitalization.
However, sepsis survivors may not recover to their presepsis health condition and continue to suffer from
various complications, which may lead to death after discharge.[12, 13] The identification of factors
related to long-term prognosis of sepsis survivors at the time of discharge would be helpful in the
management and follow-up plan of the patients and improve the prognosis. Therefore, we performed this
study to investigate the factors at the time of discharge that were related to the 1-year mortality of sepsis
survivors.

Methods
Study design

A retrospective analysis of a prospectively registered database of all consecutive patients with sepsis or
septic shock was performed in an urban tertiary academic hospital. The institutional review board of
Seoul National University Bundang Hospital approved the study and granted a waiver of informed
consent (B-1909-567-111).

Study setting and population

From January 2016 to November 2017, adult patients (age ≥ 18 years) who visited the emergency
department (ED) and were diagnosed with sepsis or septic shock were initially included. Of them, patients
who died in the hospital or were discharged with a hopeless prognosis were excluded. If patients were
hospitalized more than once during the study period, only the first hospitalization data were used, and
data from subsequent hospitalizations were excluded. Patients without available data from the week
before hospital discharge were also excluded.

The Third International Consensus Definitions for Sepsis and Septic Shock (Sepsis-3) was used to define
sepsis and septic shock. Sepsis was defined as a Sequential Organ Failure Assessment (SOFA) score ≥ 2
points related to infection. Septic shock was defined as persistent hypotension in sepsis that required
vasopressors to maintain a mean arterial pressure ≥ 65 mmHg and a serum lactate concentration higher
than 2 mmol/l after fluid resuscitation.[1] Patients with sepsis or septic shock were treated according to
international guidelines for sepsis management.[1, 14]

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Measurement

Patient data at admission were collected using standardized data collection forms.[4, 15, 16] The forms
included demographic data, including age, sex, body mass index (BMI), underlying comorbidities, site of
infection, laboratory results and severity scores. In addition to the data at the time of admission, data at
the time of discharge were collected through a hospital information system. Data at the time of discharge
included body weight; laboratory results such as complete blood cell counts, albumin, and C-reactive
protein; and the SOFA score. Data closest to the time of discharge from within 1 week before discharge
were used, and patients without available data collected during that week were excluded.

The primary outcome was 1-year mortality after discharge, and medical records or a structured telephone
follow-up was used to check survival. If both methods were impossible, we checked the expunged record
of the National Health Insurance Service (NHIS). In the Republic of Korea, all citizens are obliged to
subscribe to the NHIS. The NHIS record is expunged when a person dies, has been missing for more than
5 years, or loses their nationality. We classified the expunged cases were dead and used the expunged
date as the date of death.

Statistical analysis

Continuous variables are expressed as medians with interquartile ranges (IQRs), and categorical variables
are expressed as numbers (%). Continuous variables were compared by using Student’s t test or the
Mann‒Whitney U test, as appropriate, depending on whether they were normally distributed. Categorical
variables were compared by using the χ2 test or Fisher’s exact test, as appropriate. Multivariate logistic
regression was used for analysis of the relationship between each variable at discharge and 1-year
survival, and the results were expressed as adjusted odds ratios (ORs) and 95% confidence intervals (CIs).
Age, sex, BMI, SOFA score, and variables considered to be associated with long-term prognosis, such as
white blood cell count, haemoglobin, albumin and C-reactive protein, were used in the multivariate
analysis.[9-11, 17, 18] Based on the results of multivariate analysis with continuous variables, albumin
and the SOFA score at discharge were categorized and analysed. Survival analysis for 1 year from
hospital discharge was performed with the Kaplan‒Meier survival curve and multivariate Cox
proportional hazards regression analysis. For the Kaplan‒Meier curve, the survival probability of the two
groups was analysed with the log-rank test. In the multivariate Cox proportional hazards regression
analysis, the results were expressed as adjusted hazard ratios (HRs) and 95% CIs. Receiver operating
characteristic (ROC) analysis with albumin and the SOFA score at discharge was performed. All statistical
analyses were performed using packages in R software version 4.0.5 for Windows (R Foundation for
Statistical Computing, Vienna, Austria) and GraphPad Prism 9.3.1 (GraphPad Software, La Jolla, USA). A
two-tailed p value less than 0.05 was considered statistically significant.

Results
Characteristics of the study population

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  During the study period, there were 1,125 eligible patients with sepsis. Among these patients, 203
(18%) died in the hospital or were discharged with a hopeless prognosis, and 922 survived to hospital
discharge. Patients who were hospitalized more than once (n = 63) and patients without available data
from the week before discharge (n = 134) were excluded. Finally, 725 patients who survived to hospital
discharge were included in the final analysis. Among them, 64 patients (8.8%) died within one year (Fig.
1).

   The median age of the patients was 75 (65-81) years, and there were 396 male patients (54.6%). The
baseline characteristics at admission of the survivors and the nonsurvivors are presented in Table 1.
Compared to the survivors, the nonsurvivors were older and had a lower BMI. Comorbidities were not
different between the survivors and the nonsurvivors. Patients with respiratory tract infections
had a lower survival rate. Of the laboratory results, nonsurvivors had lower haemoglobin and albumin
concentrations than survivors. The nonsurvivors had longer hospital lengths of stay and higher
SOFA scores than the survivors (Table 1).

   Patient characteristics at discharge are presented in Table 2. BMI, white blood cell count, haemoglobin,
albumin, creatinine, CRP concentrations and SOFA score were decreased and platelet count was
increased at the time of discharge compared with initial values at admission (Additional file 1: Table S1).
At the time of discharge, BMI, haemoglobin, platelets and albumin were lower, and CRP and
SOFA scores were higher in the nonsurvivors than in the survivors (Table 2).

 Multivariate analysis

   In the multivariate logistic regression analysis with all variables considered to be continuous variables,
low albumin at discharge (OR 0.360, 95% CI 0.181-0.708) and a high SOFA score at discharge (OR 1.209,
95% CI 1.042-1.400) were identified as prognostic factors for 1-year mortality (Additional file 1: Table S2).
Based on these results, albumin concentration at discharge was divided into two groups: albumin ≥ 2.5
mg/dl and < 2.5 mg/dl. In sepsis survivors, the median albumin concentration was 2.9 (2.5-3.2) mg/dl,
and a cut-off of 2.5 mg/dl of albumin was selected based on clinically significant hypoalbuminemia.[19]
The SOFA score at discharge was divided into two groups: SOFA score ≥ 2 and < 2.[1] In multivariate
logistic regression with albumin and the SOFA score as categorical variables, albumin < 2.5 mg/dl and
SOFA score ≥ 2 were identified as prognostic factors for 1-year mortality (OR 2.698, 95% CI 1.488-4.883
for albumin < 2.5 mg/dl and OR 2.114, 95% CI 1.204-3.814 for SOFA score ≥ 2, respectively) (Table 3).

   During the 1-year follow-up period after hospital discharge, albumin < 2.5 mg/dl at discharge
had an approximately 2.5-fold higher risk for death in a year (HR 2.553, 95% CI 1.483-4.395). A SOFA
score ≥ 2 at discharge was associated with an approximately 2.0-fold higher risk for death in a year (HR
2.038, 95% CI 1.188-3.494) (Fig. 2). The Kaplan‒Meier curve showed that albumin < 2.5 mg/dl at
discharge and a SOFA score ≥ 2 points at discharge increased mortality over the first year (P < 0.05, Fig.
3a and 3b).

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   In the ROC analysis, the area under the curve (AUC) was 0.720 (95% CI 0.653-0.787) for albumin and
0.659 (95% CI 0.589-0.730) for the SOFA score. There was no significant difference in the AUC of the two
curves (p = 0.147, Fig. 4).

Discussion
 In this study, with sepsis survivors, inflammatory markers such as white blood cell counts and C-reactive
protein concentration were decreased at discharge compared to those at admission. In addition, the
albumin concentration and the SOFA score also decreased. In the multivariate analysis, the serum
albumin concentration and the SOFA score at discharge were predictors of 1-year mortality in patients
who survived to hospital discharge with sepsis or septic shock.

  Many studies have investigated prognostic factors for sepsis, but most of the studies investigated
prognostic factors for one or three months of follow-up.[5, 9, 20, 21] There have been some studies of
long-term mortality in sepsis. In a study of sepsis survivors who were admitted to 192 critical care units,
variables obtained within 24 hours of the index hospitalization were analysed.[10] In this study, age, male
sex, one or more severe comorbidities, prehospitalization dependency, and nonsurgical status were
identified as risk factors for long-term mortality. In a study of immune responses, many biomarkers were
measured at 5 time points from the index admission.[11] In this study, persistent elevation of
inflammatory and immunosuppressive biomarkers was associated with worse long-term outcomes.[11] In
another study of sepsis survivors, laboratory data obtained within 24 hours of ICU admission were
analysed, and a lower serum albumin concentration was a predictor of short-term and long-term mortality
in patients with septic shock.[22]

The present study has several differences compared to previous studies. First, we focused on long-term
survival, not short-term survival. Sepsis survivors suffer from various organ injuries during
hospitalization, and these injuries could influence the long-term prognosis after discharge. Therefore, the
present study was performed because we thought that identification of the factors related to long-term
outcomes at the time of discharge would be helpful for the treatment and follow-up plans of sepsis
survivors after discharge. Second, although there have been a few studies about long-term mortality in
sepsis survivors, most of the studies used variables at the time of admission rather than at discharge.
However, the initial variables reflect the patients’ condition at the time of admission, so they are likely to
be more relevant to short-term outcomes than long-term outcomes. Therefore, we used variables at the
time of discharge that were measured after the completion of acute treatment. Third, this study included
patients admitted to both the ICU and general wards. The criteria for admission to the ICU may differ from
hospital to hospital. Since this study included sepsis patients admitted to the general wards as well as
the ICUs, we could include all sepsis patients compared to studies of only ICU patients. Last, the present
study did not include various biomarkers that can be measured only in the laboratory but included those
that could be easily measured in clinical practice.

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In the present study, serum albumin concentration and the SOFA score at discharge were identified as
prognostic factors for long-term survival in patients with sepsis. In the present study, most of the
laboratory results were improved at discharge compared to at admission and were almost
within the normal range (Additional file 1: Table S1). However, the albumin concentration at discharge did
not improve; rather, it decreased compared to that at admission. The decreased albumin concentration
might be due to the dilution effect caused by fluid therapy and albumin leakage by the increased vascular
permeability that occurs during sepsis.[23, 24] The albumin concentration has been reported as a
prognostic factor for short-term and long-term mortality in patients with sepsis.[22, 25, 26] Patients with
malnutrition have a high risk of death in the ICU, and serum albumin concentration is a nutritional marker.
[27] In addition, albumin could act as an antioxidant and a transporter for hormones or signalling
molecules and inhibit platelet aggregation.[19] Therefore, hypoalbuminemia would be associated with
long-term survival.

    The SOFA score is a tool used to measure organ dysfunction in critically ill patients, and a high SOFA
score is known to be related to severity and poor outcome. Sepsis-3 also uses a change in SOFA score of
2 or more as an important diagnostic criterion.[1] In a previous study on the long-term survival of sepsis,
the SOFA score at admission was identified as a prognostic factor, and the SOFA score at discharge was
identified as a prognostic factor in the present study.[10] In the present study, the median SOFA score
decreased from 6 (4-8) at admission to 1 (0-3) at discharge. However, 330 patients (45.5%) still had a
SOFA score of 2 or higher at discharge. This suggests that organ dysfunction remains chronic for many
sepsis patients, and a SOFA score of 2 or higher at discharge was associated with long-term mortality.

   This study has several limitations. First, the present study was a retrospective analysis at a single
centre. Therefore, these results might be difficult to generalize to other institutions. Second, long-term
mortality from sepsis is known to be associated with inflammation and immune function.[11] However,
our study did not measure biomarkers of the immune response. Instead, this study used commonly
available variables. Finally, in some patients, the date of death was estimated based on the date the
National Health Insurance Service record was expunged. It is possible that the health insurance was
cancelled not because of death but because of other reasons, such as disappearance or a loss of
nationality, although this would have a negligible effect.

Conclusion
A low serum albumin concentration of < 2.5 mg/dL and high SOFA score of ≥ 2 at the time of discharge
were prognostic factors for 1-year mortality in sepsis survivors.

Abbreviations
BMI: Body mass index

CRP: C-reactive protein

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SOFA: Sequential Organ Failure Assessment

ICU: Intensive care unit

ED: Emergency department

NHIS: National Health Insurance Service

IQR: Interquartile range

OR: Odds ratio

CI: Confidence interval

HR: Hazard ratio

ROC: Receiver operating characteristic

AUC: Area under the curve

Declarations
Ethics approval and consent to participate

The institutional review board of Seoul National University Bundang Hospital approved the study and
granted a waiver of informed consent (B-1909-567-111).

Consent for publication

 Not applicable.

Availability of data and materials

 The datasets analysed during the current study are available from the corresponding author on
reasonable request.

Competing interests

 The authors have no conflicts of interest to declare.

Funding

 Not applicable.

 Authors’ contributions

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S-ML and YHJ conceived and designed this study. S-ML, YHJ, JHL, JEH, IP, SB, HJ, YWU and HEK
collected and managed the data. S-ML and YHJ analysed the data. IP provided advice for data analysis.
S-ML drafted the manuscript, and YHJ revised it. S-ML assumes responsibility for the paper as a whole.
All authors read and approved the final manuscript.

Acknowledgements

 None

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Tables
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Table 1. Baseline characteristics at admission of the survivors and the nonsurvivors at 1 year

Page 11/17
Variable Total Survivors Nonsurvivors p
value
(n = 725) (n = 661) (n = 64)

Age, years 75.0 (65.0-81.0) 75.0 (65.0-81.0) 80.0 (71.0-84.0) 0.002

Male, n (%) 396 (54.6) 357 (54.0) 39 (60.9) 0.352

Body mass index, kg/m2 21.5 (18.6-24.1) 21.6 (18.8-24.2) 19.3 (16.7-23.0) 0.002

Comorbidities        

Hypertension 379 (52.3) 347 (52.5) 32 (50.0) 0.802

Diabetes mellitus 238 (32.8) 214 (32.4) 24 (37.5) 0.488

 Neurologic diseases 277 (38.2) 245 (37.1) 32 (50.0) 0.058

 Congestive heart failure 2 (0.3) 2 (0.3) 0 (0.0) 1.000

 Chronic lung disease 90 (12.4) 79 (12.0) 11 (17.2) 0.310

 Chronic renal failure 40 (5.5) 35 (5.3) 5 (7.8) 0.578

 Malignancy 125 (17.2) 114 (17.2) 11 (17.2) 1.000

Site of infection, n (%)        

 Respiratory 347 (47.9) 306 (46.4) 41 (64.1) 0.007

 Genitourinary 174 (24.0) 165 (25.0) 9 (14.1) 0.051

 Abdominal 143 (19.7) 133 (20.1) 10 (15.6) 0.388

 Musculoskeletal 24 (3.3) 22 (3.3) 2 (3.1) 1.000

 Others 36 (5.0) 34 (5.1) 2 (3.1) 0.762

Laboratory results        

 White blood cells, 109/L 11.6 (7.9-16.9) 11.7 (7.9-16.9) 11.3 (7.8-18.9) 0.793

 Haemoglobin, g/dL 11.6 (10.0-13.0) 11.6 (10.1-13.0) 11.2 (9.0-12.6) 0.035

 Platelets, 109/L 179.0 (120.0- 177.0 (120.0- 202.5 (128.0- 0.476

256.0) 255.0) 266.5)

 Albumin, g/dL 3.0 (2.6-3.4) 3.1 (2.6-3.5) 2.8 (2.4-3.2) <0.001

 Creatinine, mg/dL 1.2 (0.9-2.0) 1.2 (0.8-1.9) 1.5 (1.0-2.2) 0.063

 C-reactive protein, mg/dL 12.4 (6.3-19.2) 12.4 (6.3-19.2) 12.3 (6.8-19.6) 0.900

SOFA score at admission 6.0 (4.0-8.0) 6.0 (4.0-8.0) 7.0 (5.0-9.0) 0.092

Hospital length of stay, days 12.0 (8.0-18.5) 12.0 (8.0-18.0) 15.0 (10.0-23.0) 0.017

Page 12/17
 Admitted to intensive care unit, 245(33.8) 219 (33.1) 26 (40.6) 0.284
n (%)

Values are expressed as medians (interquartile range) or numbers (%) as appropriate. The p value is from
Student’s t test or the Mann‒Whitney U test for continuous variables and the χ2 test or Fisher’s exact test
for categorical variables, as appropriate.

SOFA, Sequential Organ Failure Assessment

Table 2. Characteristics at discharge of sepsis survivors according to the 1-year mortality

Variable Total Survivors Nonsurvivors p value

(n = 725) (n = 661) (n = 64)

Body mass index, 21.2 (18.3-23.7) 21.3 (18.6-23.8) 19.1 (16.7-22.2) 0.002
kg/m2

Laboratory results        

 White blood cells, 109/L 7.5 (5.7-10.0) 7.4 (5.7-9.9) 8.5 (6.0-10.2) 0.092

 Haemoglobin, g/dL 10.6 (9.6-11.8) 10.6 (9.7-11.8) 10.1 (9.1-10.8) 0.001

 Platelets, 109/L 246.0 (171.0- 248.0 (175.0- 212.5 (150.5- 0.010

345.0) 353.0) 270.0)

 Albumin, g/dL 2.9 (2.5-3.2) 2.9 (2.6-3.2) 2.5 (2.2-2.8) <0.001

 Creatinine, mg/dL 0.7 (0.5-0.9 0.7 (0.5-0.9) 0.7 (0.5-1.2) 0.266

 C-reactive protein, 2.5 (1.2-4.9) 2.3 (1.1-4.9) 3.7 (2.2-6.5) 0.001

mg/dL

SOFA score 1.0 (0.0-3.0) 1.0 (0.0-2.0) 2.0 (1.0-4.0) <0.001

Values are expressed as medians (interquartile range).

 SOFA, Sequential Organ Failure Assessment

Table 3. Multivariate logistic regression analysis for 1-year mortality

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 Variables Odds ratio 95% Confidence interval p value

Age 1.024 1.000-1.051 0.065

Male 0.802 0.454-1.399 0.441

Body mass index 0.943 0.876-1.013 0.116

White blood cell 1.020 0.950-1.087 0.566

Haemoglobin 0.881 0.712-1.078 0.228

C-reactive protein 1.052 0.978-1.126 0.156

       

Albumin ≥ 2.5 mg/dL Reference    

Albumin < 2.5 mg/dL 2.698 1.488-4.883 0.001

SOFA score < 2 Reference    

SOFA score ≥ 2 2.114 1.204-3.814 0.011

Body mass index, white blood cells, haemoglobin, albumin, C-reactive protein and SOFA score were
measured at the time of discharge. The albumin and SOFA scores were analysed by dichotomizing the
patients around the respective cut-offs of 2.5 mg/dL and 2.

 SOFA, Sequential Organ Failure Assessment

Figures

Figure 1

Flow diagram of included patients.

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Figure 2

Multivariate Cox proportional analysis for 1 year mortality.

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Figure 3

Kaplan‒Meier survival curves.

 In the log-rank test, the two groups showed a significant difference (p < 0.001, both a and b).

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Figure 4

Receiver operating characteristic curves of albumin concentration and SOFA score at discharge.

The area under the curve (95% confidence interval) of albumin was 0.720 (0.653-0.787), and that of the
SOFA score was 0.659 (0.589-0.730), with p < 0.0001. There was no significant difference in the AUC of
the two curves in the bootstrap test (p = 0.147).

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