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Accepted Manuscript
Fluid volume, fluid balance and patient outcome in severe sepsis
and septic shock: A systematic review
Bereket Molla Tigabu, Majid Davari, Abbas Kebriaeezadeh,
Mojtaba Mojtahedzadeh
PII:
DOI:
Reference:
S0883-9441(18)30676-2
doi:10.1016/j.jcrc.2018.08.018
YJCRC 53010
To appear in:
Journal of Critical Care
Please cite this article as: Bereket Molla Tigabu, Majid Davari, Abbas Kebriaeezadeh,
Mojtaba Mojtahedzadeh , Fluid volume, fluid balance and patient outcome in severe sepsis
and septic shock: A systematic review. Yjcrc (2018), doi:10.1016/j.jcrc.2018.08.018
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ACCEPTED MANUSCRIPT
Fluid volume, fluid balance and patient outcome in severe sepsis and septic shock: a
systematic review
Bereket Molla Tigabu1,2,3 , Majid Davari1,2 , Abbas Kebriaeezadeh1,2 , Mojtaba Mojtahedzadeh4,5
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1 Department of Pharmacoeconomics and Pharmaceutical Administration, Faculty of Pharmacy,
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International Campus, TUMS, Tehran, Iran
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2 Pharmaceutical research center, Faculty of Pharmacy, TUMS, Tehran, Iran
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3 School of Pharmacy, Haramaya University, Ethiopia
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4 Department of Clinical Pharmacy, Faculty of Pharmacy, TUMS, Tehran, Iran
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5 Sina Hospital, Division of Critical Care Medicine, Tehran, Iran
author:
and
Majid
Pharmaceutical
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Pharmacoeconomics
Dr.
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*Corresponding
Davari,
administration,
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University of medical sciences, Tehran, Iran. Email:
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mim.davari@gmail.com;
Faculty
of
Department
Pharmacy,
of
Tehran
ACCEPTED MANUSCRIPT
Abstract
Purpose: This systematic review and meta-analysis was conducted to evaluate the mortality risk
in severe sepsis and septic shock with a low and high fluid volume/balance.
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Methods: Cohort studies that compared the mortality of patients with low or high fluid
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volume/balance were included. Electronic databases: PubMed/Medline PLUS, Embase, Scopus,
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and Web of Science were searched. Patient mortality at the longest follow-up was the primary
outcome measure. The data were analyzed using STATA 14 statistical software.
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Results: The current study included fifteen studies with 31,443 severe sepsis and/or septic shock
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patients. Patients with a high fluid balance have a 70% increased risk of mortality (pooled RR:
1.70; CI: 1.20, 2.41; P=0.003). Survivors of severe sepsis and/or septic shock received higher
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fluid volume in the first three hours. However, fluid volume administered in the first 24 hours
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mortality reduction (P=0.02).
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was higher for non-survivors. Low volume resuscitation in the first 24 hours had a significant
Conclusion: High fluid balance from the first 24 hours to ICU discharge increases the risk of
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mortality in severe sepsis and/or septic shock. However, randomized clinical trials should be
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conducted to resolve the dilemma of fluid resuscitation.
Keywords: Fluid volume, fluid balance, mortality, severe sepsis, septic shock, systematic review
ACCEPTED MANUSCRIPT
Introduction
Severe sepsis and septic shock are characterized by a deficit in effective vascular volume as a
result of vasodilation, vascular leakage and third space loss (1, 2). Therefore, fluid replacement is
a core of management. Large fluid resuscitation (30ml/Kg) in the first 6 hours was recommended
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in Early Goal-Directed Therapy (1, 3). However, too much fluid has its own negative
consequences. Although positive fluid balance was found to increase mortality and time spent on
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mechanical ventilation (4-6), too little fluid may also lead to hypoperfusion and aggravate organ
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dysfunction (7). The primary goal of resuscitation is to optimize the central venous pressure to 812mmHg for non-ventilated patients and to 12-15mmHg during mechanical ventilation (1).
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Nevertheless, the optimal volume for fluid resuscitation has been debatable.
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In spite of progresses made in the development of protocols, severe sepsis and septic shock
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causes significant morbidity and mortality in the intensive care units (8, 9). Previously, two
reviews tried to address the risk of mortality with resuscitation strategy and fluid balance in
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critically ill patients (10, 11). However, both of these reviews were not specifically designed to
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deal with severe sepsis and septic shock (10, 11).
Therefore, we conducted this systematic
review and meta-analysis to evaluate the mortality risk in severe sepsis and septic shock with a
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low versus high fluid volume/balance.
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Methods
This systematic review was done based on PRISMA recommendations (12) and the details of the
protocol are registered at PROSPERO (Registration number: CRD42017079560).
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Search strategy
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Bibliographic electronic databases (PubMed/Medline PLUS, Scopus, Embase, and Web of
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Science) were searched for cohort studies from January 2000 to September 2017 with the
following keywords: fluid, colloids, crystalloids, albumin, ?normal saline?, saline, ?ringer?s
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lactate?, ?lactated ringer?, volume, balance, outcome, mortality, sepsis, ?severe sepsis?, ?septic
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shock?, ?critical illness?, ?critical care?, ?intensive care? and ICU.
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Eligibility criteria
Cohort studies on adult patients with severe sepsis and/or septic shock published in the English
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language were included. High fluid volume/balance or positive fluid balance was taken as an
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intervention whereas low fluid volume/balance or negative fluid balance was the comparator.
Study selection
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Patient mortality at the longest follow-up was the primary outcome measure.
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Screening of the records based on the title and abstracts, and the selection of full text articles
based on the eligibility criteria was done by two reviewers independently. Differences between
the reviewers were settled by discussion and consensus including a third reviewer.
Data extraction
Study characteristics, patient characteristics, fluid volume, fluid balance, and outcome were
extracted by two reviewers independently, and the extracted data were cross-checked by a third
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reviewer. Mortality at different fluid volume and fluid balances were recorded at the longest
follow-up. The mean/median fluid volume was recorded for the comparator groups as reported in
the reviewed articles. However, when fluid volume/balance was reported only for quartiles, the
lowest quartile fluid volume/balance was taken as a low fluid volume/balance and the highest
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quartile fluid volume/balance was taken as a high fluid volume/balance. If the quartile volume
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was reported in a range the average of the two extremes was used during the analysis.
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Quality assessment
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Two reviewers had assessed the quality of selected studies using the Strengthening the Reporting
of Observational Studies in Epidemiology (STROBE) Statement-checklist (13) and the checklist
The overall validity of the studies was rated as complete and incomplete for
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Black (14).
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for the quality assessment of randomized and non-randomized studies developed by Downs and
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STROBE statement-checklist fulfillment. The overall quality index was calculated considering
the reporting, internal validity, bias, confounding and power of the study for the Downs and
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Statistical analysis
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Black checklist.
The pooled relative risk (RR) with 95% confidence intervals (CIs) was calculated. Statistical
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heterogeneity of the data was assessed by the Mantel-Haenszel chi-square test with a P<0.01. I2
test value > 50% was taken to indicate significant heterogeneity. The random-effects model was
used if heterogeneity was observed; otherwise, the fixed effect model was used. P <0.05 was
considered statistically significant. STATA 14 statistical software was used to analyze the result.
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Results
The database search revealed of 5191 records of which fifteen articles that fulfilled the inclusion
criteria were selected for the current review. A total of 31,443 severe sepsis and/or septic shock
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patients were analyzed. The characteristics of the included studies were shown in Table 1.
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The quality of the included studies was summarized in Table 2.
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Quality assessment
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Fluid volume and mortality
Survivors of severe sepsis and septic shock received a higher volume of fluid than non-survivors
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in the first 3 hours (2085ml vs 1600ml, P=0.007). The higher fluid volume received within the
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first 3 hours had a statistically significant association with in-hospital mortality (OR, 0.34; 95%
CI, 0.15-0.75; P= .008) (15). Survivors of septic shock received a significantly lower volume
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fluid in the first 24 hours (<5Li) (16, 17). A study on patients with negative fluid balance showed
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survivors of septic shock received a higher volume of fluid in the first 48 hours (53.7ml/Kg,
P<0.001) (18). However, this volume is less than 4 liters when a standard adult weight is
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considered. On the other hand, three studies revealed no significant relationship between the
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volume of fluid administered in the first 24 hours and patient mortality in the first 3 days, 30
days, 90 days or 365 days (19-21). Nevertheless, the cumulative number of study participants in
these three studies (n=332) (19-21) is smaller than the number of patients (n=24,561) in the
studies that showed the association (16, 17).
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Fluid balance and mortality
Eight studies reported the mortality risk of fluid balance. The average fluid balance after 24
hours was 2334.7 ml �2.9 ml for survivors and 3763.8 ml�3.0 ml for non-survivors. Micek,
et al.(22) and Sakr, et al.(23) revealed a notably low fluid balance among survivors of severe
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sepsis and/or septic shock than non-survivors at the first 24 hours and cumulative balance in
intensive care unit (ICU), respectively (P=0.003 and P<0,001, respectively) . Although Sirvent,
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et al.(24) also found remarkably high fluid balance among non-survivors at 48, 72, and 96 hours.
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The difference was not statistically significant for the first 24 hours.
Five of the reviewed studies identified fluid balance as an independent predictor of mortality.
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The study by Boyd, et al.(25) revealed that patients with a low positive fluid balance at 12 hours
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and 4th day had a lower 28-day mortality compared to those with a higher fluid balance. Four of
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these studies were included in the meta-analysis (21, 26-28). A fixed effect model was used to
calculate the pooled relative risk as there was no significant heterogeneity (P=0.389, I 2 =0.5%).
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The analysis revealed a 70% increased risk of mortality for patients with a higher positive fluid
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balance (pooled RR: 1.70; CI: 1.20, 2.41; P=0.003) (Fig 2). The Egger?s test (P=0.082) and the
shape of the funnel plot suggest no small study effect nor publication bias (Fig 3). However,
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Brotfain, E. et al.(28) presented the result by grouping the fluid balance into four groups.
Therefore, the analysis was repeated by using the group with a highest fluid balance to check the
sensitivity of the result. Similarly, the heterogeneity (P=0.382, I2 =2.2%) and the pooled relative
risk (pooled RR: 1.51; CI: 1.20, 1.90; P<0.001) were significant (Fig 4).
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Discussion
The current review revealed a positive fluid balance recognized at different times from the first
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24 hours in ICU to cumulative balance at discharge predicts mortality. Patients with a higher
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fluid balance are 1.70 times as likely to die compared to patients with a lower fluid balance. This
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result is theoretically appealing when the hemodynamics of septic patients and the associated
organ failures are considered. The inflammation-mediated injury on the glycocalyx is responsible
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for clinical effects of sepsis including edema, acute kidney injury and respiratory failure (30).
Excessive infusion of fluid aggravates glycocalyx damage, thereby further increasing tissue
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permeability and leading to poor prognosis (31). Moreover, fluid overloading can lead to atrial
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and ventricular stretching of the heart that stimulates the release of atrial and brain natriuretic
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peptides. These peptides have been found to aggravate the endothelial glycocalyx injury (32).
The treatment of sepsis attenuates the inflammatory cascade and returns fluid from the interstitia
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and third space to the central circulation. However, sepsis-related organ dysfunctions complicate
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the excretion process and associated with an increased risk of death (33-35). Therefore, the
organs involved in intravascular fluid balance (i.e. the kidneys and heart) should be optimized to
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excrete excess fluid.
The current review demonstrates that for patients with severe sepsis and septic shock, the higher
volume of fluid in the first 3 hours improves patient survival.
However, this finding was
reported in a single study. The low volume resuscitation in the first 24 hours had mortality
reduction benefit. However, Carlsen, et al.(20) and Smith, et al.(19) reported no association
between the fluid volume received in the first 24 hours and 90 days mortality of patients.
However, these studies evaluated a significantly lower number of patients as compared to the
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studies by Koonrangsesomboon, et al.(17) and Marik, et al.(16) which demonstrated the
association. Although the study by Shen, et al.(18) revealed survivors received a higher volume
of fluid than non-survivors, the study included only patients with negative fluid balance.
Therefore, it would be difficult to generalize this outcome to all septic shock patients most of
Furthermore,
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whom expected to have organ failure that leads to excessive fluid accumulation.
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the mortality reduction benefit of higher fluid volume for patients who remained in shock for
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three or more days reported by Smith, et al.(19) has a flaw. The cut-off point reported by the
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study was lower than the volume considered to be high in clinical trials (3, 36, 37).
The strength of this review includes the precision of the clinical question restricted to severe
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sepsis and septic shock, the inclusion of both fluid volume and fluid balance, and the inclusion of
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cohort studies. This better studies the effectiveness than the efficacy of fluid therapy. This review
has several limitations. First, most of the included articles were done retrospectively. Second, the
Third, the cut-off point for the fluid volume and fluid balance used varied
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included studies.
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time points at which the fluid balance was measured and the follow-up periods vary among the
among studies. Fourth, only articles published in the English language are include. Finally, all of
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Conclusion
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the included articles are of low quality.
We cautiously conclude that high fluid balance from the first 24 hours to ICU discharge
increases the risk of mortality in severe sepsis and septic shock. Moreover, high fluid volume
resuscitation in the first 3 hours and low fluid volume therapy in the first 24 hours have survival
benefits. We, therefore, strongly recommend that randomized clinical trials should be conducted
to determine the cut-off points for fluid volume and fluid balance during fluid therapy in severe
sepsis and septic shock management.
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Authors? contributions
BMT and MD conceptualize the study, conducted the article review, do the analysis, interpreted
the results, and drafted and finalized the manuscript. AK and MM participated in the study
designed, conducted the article review and revised the manuscript. BMT, MD, AK and MM
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revised the manuscript and approved the final manuscript.
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The authors declared that they have no conflict of interest.
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Competing interests
Funding
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Not applicable
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References
Alsous F.
et al.,
2000(21)
Boyd, J.
H. et al.,
2011(25)
Patient population
Sample
size
Septic shock patients with 36
no history of dialysis
Age*
67.4
Fluid
Mortality
measured measured
24 hrsb
3 days
Septic shock patients
receiving a minimum of
5礸 norepinephrine per
minute
-
12hrs b
28 days
day 4b
28 days
PT
Authors
ED
Table1. Characteristics of included studies
H >(-500ml)
Q1-710ml
Q2-2880ml
Q3-4900ml
Q4-8150ml
Q1-1560ml
Q2-8120ml
Q3-13000ml
Q4-20500ml
L< 4.0L
H ? 4.0L
Remark
RR, 5.0; 95%
10.9;P=0.000
Septic shock
132
60
24hrsa
30-days
90-days
365-days
Smith, S.
H. et al.,
2012(19)
Septic shock
164
66
Day 1a
90-days
L< 4.0L
Days 1-3a
90-days
H > 4.0L
L<7.5L
H> 7.5L
In patients w
days or more
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Carlsen,
S.et al.,
2011(20)
Adjusted HR
0.569 (0.405
0.581 (0.414
0.762 (0.562
Adjusted HR
0.466 (0.299
0.512 (0.339
0.739 (0.503
No differenc
between the
(P=0.36), 90
365 days (P=
P=0.27
AC
778
Fluid volume/
balance
L ?(-500ml)
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Septic shock
325
S- 54.8
NS-63.0
24hrsb
Hospital
mortality
S-2959ml
NS-4374ml
Septic shock
350
65.4
24hrsb
Hospital
mortality
Q1=0-6L
Q2=6-12L
Q3=12-18L
Q4=18-24L
IP
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Micek, S.
T. et al.,
2013(22)
Sadaka, F.
et al.,
2014(26)
were associa
mortality (P=
P=0.003 (tot
survivors= 1
163
Adjusted haz
1.519 (95%
1.740 (95%
1.620 (95%
respectively
Sample
size
594
Age*
S-69
NS-74
Fluid
measured
0-3 hrsa
Mortality
measured
Hospital
mortality
M
AN
Lee, S. J. et
al.,
2014(15)
Patient
population
Severe sepsis
and septic shock
US
Authors
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Table 1. Characteristics of included studies (continued)
de Oliveira,
F. S. et al.,
2015(29)
Severe sepsis
and septic shock
Septic shock
6 hrsa
Day 4,5,6b
Hospital
mortality
116
S-57
NS-63
24-48 hrsb
Hospital
mortality
Fluid balance >
3000ml
1048
S-62
NS-56
24 hrsa
Hospital
mortality
S-3.92L
NS-4.64L
S-7.08L
NS-8.23L
S-9.88L
NS-11.43L
173
CE
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Koonrangs
esomboon,
W. et al.,
2015(17)
S-660ml
NS-880ml
S-60
NS-63
ED
Sepsis patients
in ICU
3.1-6 hrsa
S-3150ml
NS-2875ml
Negative fluid
balance
Positive fluid
balance
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Acheampo
ng, A. et
al.,
2015(27)
Fluid volume/
balance
S-2085ml
NS-1600ml
48 hrsa
72 hrs a
Remark
The higher propor
received within th
associated with de
mortality (OR, 0.3
0.75; P= .008)
P=0.09
P=0.10
A positive fluid b
independently ass
mortality (adjuste
[1.007?1.022] per
<0.001).
fluid balance mor
the 24th and the 4
diagnosis were in
associated with hi
3.14; 95% CI, 1.1
Non-survivors ha
higher median cu
at 24, 48, and 72 h
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Table 1. Characteristics of included studies (continued)
Authors
Sirvent, J.M.
et al.,
2015(24)
Patient
population
Severe sepsis
and septic shock
Sample
size
42
Age*
S-58.9
NS-66.9
Fluid
measured
24 hrsb
Mortality
measured
28-days
mortality
48 hrsb
Sepsis patients
in ICU
296
G1-61.08
G2-63.79
G3-63.23
G4-61.51
At ICU
discharge b
Marik, P. et
al., 2017(16)
Severe sepsis
and septic shock
23,513
NMV,NS Day 1a
h-67.5
Hospital
mortality
Hospital
mortality
AN
US
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Brotfain, E.
et al.,
2016(28)
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96 hrsb
Shen, Y. F. et
al., 2017(18)
Sepsis (critically
ill)
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Sepsis patients
in ICU
1,808
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Sakr, Y. et
al., 2017(23)
4440ml
S-59.3
NS-69.3
5459ml
Cumulative
balance in
ICUb
48 hrs a
Non-survivors had h
positive fluid balanc
hours (P=0.02,P=0.0
respectively)
ICU
mortality
S-354ml
NS-3680ml
hospital
mortality
S-53.7ml/Kg
NS-48.3ml/Kg
The positive cumulat
found to be an indepe
ICU mortality (OR, 1
1.06; P < .001; and in
(OR, 1.06; 95% CI, 1
Low volume resuscit
associated with a sm
reduction in mortality
(95% CI ?1.0%, ?0.4
However, in patients
volume resuscitation
mortality increased b
2.5%; p = 0.0003) fo
above 5 L.
P<0.001
Fluid intake was stat
(P<0.001)
mean/median a fluid volume, b fluid balance, G-group, H-higher fluid balance/volume, L-lower fluid
balance/volume, MV- mechanical ventilation, NMV-no mechanical ventilation, NSh- no shock, NS-non-survivors,
Q-quartile, Sh- shock, S-survivors
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*
2,068
3618ml
3889ml
M
MV,NSh
-65.3
NMV,Sh
-68.5
MV,Sh66.3
62
Remark
T
72 hrsb
Fluid volume/
balance
S-1710.4ml
NS-3153.5ml
S-1791.6ml
NS-4394.3ml
S-1128.1ml
NS-5401.6ml
S-4612.6ml
NS-6678.6ml
< 10 L
10-20 L
20-30 L
>30L
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Table2. Quality assessment
2
3
3
3
3
0
0
0
0
0
0
0
0
0
0
2
3
3
3
3
0
0
0
0
0
0.52
0.59
0.70
0.70
0.67
T
1
1
3
3
3
3
3
2
2
3
3
3
3
3
3
IP
9
9
10
10
9
3
3
2
2
3
3
3
3
3
3
US
9
7
10
9
9
8
9
8
8
9
Quality
index,
total/27
0.59
0.59
0.59
0.59
0.63
0.56
0.59
0.56
0.56
0.63
ED
M
Alsous F. et al., 2000(21)
Boyd, J. H. et al., 2011(25)
Carlsen, S.et al., 2011(20)
Smith, S. H. et al., 2012(19)
Micek, S. T. et al., 2013(22)
Sadaka, F. et al., 2014(26)
Lee, S. J. et al., 2014(15)
Acheampong, A. et al., 2015(27)
de Oliveira, F. S. et al., 2015(29)
Koonrangsesomboon., W. et al ,
2015(17)
Sirvent, J.M. et al., 2015(24)
Brotfain, E. et al., 2016(28)
Marik, P. et al., 2017(16)
Sakr, Y. et al., 2017(23)
Shen, Y. F. et al., 2017(18)
External
validity,
3 points
1
3
2
2
2
1
1
1
1
2
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Reporting,
10 points
Downs and Black checklist
Bias, 7 Confounding,
Power,
points 6 points
1 point
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Included studies
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CE
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1.
Dellinger RP, Levy MM, Rhodes A, Annane D, Gerlach H, Opal SM, et al. Surviving Sepsis
Campaign: international guidelines for management of severe sepsis and septic shock, 2012. Intensive
care medicine. 2013;39(2):165-228.
2.
Cawcutt KA, Peters SG, editors. Severe sepsis and septic shock: clinical overview and update on
management. Mayo Clinic Proceedings; 2014: Elsevier.
3.
Rivers E, Nguyen B, Havstad S, Ressler J, Muzzin A, Knoblich B, et al. Early goal -directed therapy
in the treatment of severe sepsis and septic shock. New England Journal of Medicine.
2001;345(19):1368-77.
4.
Barmparas G, Liou D, Lee D, Fierro N, Bloom M, Ley E, et al. Impact of positive fluid balance on
critically ill surgical patients: a prospective observational study. Journal of critical care. 2014;29(6):93641.
5.
Flori HR, Church G, Liu KD, Gildengorin G, Matthay MA. Positive fluid balance is associated with
higher mortality and prolonged mechanical ventilation in pediatric patients with acute lung injury.
Critical care research and practice. 2011;2011.
6.
Rosenberg AL, Dechert RE, Park PK, Bartlett RH. Review of a large clinical series: association of
cumulative fluid balance on outcome in acute lung injury: a retrospective review of the ARDSnet tidal
volume study cohort. Journal of intensive care medicine. 2009;24(1):35-46.
7.
Semler MW, Rice TW. Sepsis Resuscitation: Fluid Choice and Dose. Clinics in chest medicine.
2016;37(2):241.
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PT
ED
M
AN
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8.
Fleischmann C, Scherag A, Adhikari NK, Hartog CS, Tsaganos T, Schlattmann P, et al. Assessment
of global incidence and mortality of hospital-treated sepsis. Current estimates and limitations. American
journal of respiratory and critical care medicine. 2016;193(3):259-72.
9.
Vincent J-L, Marshall JC, 補mendys-Silva SA, Fran鏾is B, Martin-Loeches I, Lipman J, et al.
Assessment of the worldwide burden of critical illness: the intensive care over nati ons (ICON) audit. The
Lancet Respiratory Medicine. 2014;2(5):380-6.
10.
Silversides JA, Major E, Ferguson AJ, Mann EE, McAuley DF, Marshall JC, et al. Conservative fluid
management or deresuscitation for patients with sepsis or acute respiratory distress s yndrome following
the resuscitation phase of critical illness: a systematic review and meta-analysis. Intensive care
medicine. 2017;43(2):155-70.
11.
Malbrain ML, Marik PE, Witters I, Cordemans C, Kirkpatrick AW, Roberts DJ, et al. Fluid overload,
de-resuscitation, and outcomes in critically ill or injured patients: a systematic review with suggestions
for clinical practice. Anaesthesiology intensive therapy. 2014;46(5):361-80.
12.
Moher D, Liberati A, Tetzlaff J, Altman DG, Group P. Preferred reporting ite ms for systematic
reviews and meta-analyses: the PRISMA statement. PLoS medicine. 2009;6(7):e1000097.
13.
Vandenbroucke JP, Von Elm E, Altman DG, G鴗zsche PC, Mulrow CD, Pocock SJ, et al.
Strengthening the Reporting of Observational Studies in Epidemiology (STROBE): explanation and
elaboration. PLoS medicine. 2007;4(10):e297.
14.
Downs SH, Black N. The feasibility of creating a checklist for the assessment of the
methodological quality both of randomised and non-randomised studies of health care interventions.
Journal of Epidemiology & Community Health. 1998;52(6):377-84.
15.
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Patients with a high fluid balance have a 70% increased risk of mortality.
Survivors of severe sepsis and/or septic shock received higher fluid volume in the first
three hours.
Non-survivors received higher volume of fluid in the first 24 hours
Low volume resuscitation in the first 24 hours had a significant mortality reduction
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