Fibrin‐based haemostatic agents for reducing blood loss in adult liver resection

Abdullah K Malik; Aimen O Amer; Samuel J Tingle; Emily R Thompson; Steven A White; Derek M Manas; Colin Wilson

doi:10.1002/14651858.CD010872.pub2

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Figure 1

PRISMA diagram. Date of search 20 January 2023.

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Figure 2

Risk of bias summary: review authors' judgements about each risk of bias item for each included study.

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Figure 3

Risk of bias graph: review authors' judgement about each risk of bias item presented as percentages across all included studies.

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Figure 4

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Figure 5

Fibrin‐based haemostatic agents versus non‐fibrin‐based haemostatic agents

Perioperative mortality

The Trial Sequential Analysis (TSA) showed that the diversity‐adjusted required information size (DARIS) is 18,406 participants, calculated based on the proportion of death of 4.7% in the control group; a relative risk reduction (RRR) of 20%; an alpha (type Ⅰ error) of 2%; a beta (type Ⅱ error) of 20% (power of 80%); and a diversity of 0%. The cumulative Z‐curve did not cross the conventional boundary based on the included four trials (1436 participants), nor the trial sequential monitoring boundaries of benefit and harm, suggesting that no conclusive evidence was found; hence more trials are needed. The TSA‐adjusted 95% confidence interval is 0.13 to 8.27. The x‐axis denotes the amassed versus required information size of the trial participants. The y‐axis denotes the Z values, representing the accumulating statistical information. The blue line (Z‐curve) shows the cumulative Z value. The small red lines, at the top and bottom corners, show the trial sequential boundaries for benefit or harm, representing the threshold for statistical significance in TSA. The horizontal green dotted lines show the threshold for significance in conventional meta‐analysis, at 1.96 of the Z value, corresponding to 0.05 of the P value. The red dotted lined triangular shape shows the futility boundaries and futility area in TSA.

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Analysis 1.1

Comparison 1: Fibrin‐based haemostatic agents (FBHAs) versus no intervention or placebo, Outcome 1: Perioperative mortality

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Analysis 1.2

Comparison 1: Fibrin‐based haemostatic agents (FBHAs) versus no intervention or placebo, Outcome 2: Serious adverse events

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Analysis 1.3

Comparison 1: Fibrin‐based haemostatic agents (FBHAs) versus no intervention or placebo, Outcome 3: Haemostasis within a predefined time period

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Analysis 1.4

Comparison 1: Fibrin‐based haemostatic agents (FBHAs) versus no intervention or placebo, Outcome 4: Volume of intraoperative blood loss (mL)

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Analysis 1.5

Comparison 1: Fibrin‐based haemostatic agents (FBHAs) versus no intervention or placebo, Outcome 5: Postoperative transfusion

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Analysis 1.6

Comparison 1: Fibrin‐based haemostatic agents (FBHAs) versus no intervention or placebo, Outcome 6: Reoperation

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Analysis 1.7

Comparison 1: Fibrin‐based haemostatic agents (FBHAs) versus no intervention or placebo, Outcome 7: Postoperative bile leak

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Analysis 1.8

Comparison 1: Fibrin‐based haemostatic agents (FBHAs) versus no intervention or placebo, Outcome 8: Postoperative intra‐abdominal collections

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Analysis 1.9

Comparison 1: Fibrin‐based haemostatic agents (FBHAs) versus no intervention or placebo, Outcome 9: Postoperative intra‐abdominal collections: sensitivity analysis

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Analysis 1.10

Comparison 1: Fibrin‐based haemostatic agents (FBHAs) versus no intervention or placebo, Outcome 10: Abdominal drain output (mL)

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Analysis 1.11

Comparison 1: Fibrin‐based haemostatic agents (FBHAs) versus no intervention or placebo, Outcome 11: Time to removal of abdominal drains (days)

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Analysis 1.12

Comparison 1: Fibrin‐based haemostatic agents (FBHAs) versus no intervention or placebo, Outcome 12: Operating time (minutes)

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Analysis 1.13

Comparison 1: Fibrin‐based haemostatic agents (FBHAs) versus no intervention or placebo, Outcome 13: Length of hospital stay (days)

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Analysis 2.1

Comparison 2: Fibrin‐based haemostatic agents (FBHAs) versus non‐FBHAs, Outcome 1: Perioperative mortality

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Analysis 2.2

Comparison 2: Fibrin‐based haemostatic agents (FBHAs) versus non‐FBHAs, Outcome 2: Perioperative mortality: sensitivity analysis removing trials that excluded participants with cirrhosis

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Analysis 2.3

Comparison 2: Fibrin‐based haemostatic agents (FBHAs) versus non‐FBHAs, Outcome 3: Perioperative mortality: sensitivity analysis removing a trial that investigated a non‐commercial FBHA

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Analysis 2.4

Comparison 2: Fibrin‐based haemostatic agents (FBHAs) versus non‐FBHAs, Outcome 4: Serious adverse events

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Analysis 2.5

Comparison 2: Fibrin‐based haemostatic agents (FBHAs) versus non‐FBHAs, Outcome 5: Serious adverse events: sensitivity analysis removing trials that excluded participants with cirrhosis

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Analysis 2.6

Comparison 2: Fibrin‐based haemostatic agents (FBHAs) versus non‐FBHAs, Outcome 6: Time to haemostasis (minutes)

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Analysis 2.7

Comparison 2: Fibrin‐based haemostatic agents (FBHAs) versus non‐FBHAs, Outcome 7: Time to haemostasis (minutes): sensitivity analysis removing trials that excluded participants with cirrhosis

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Analysis 2.8

Comparison 2: Fibrin‐based haemostatic agents (FBHAs) versus non‐FBHAs, Outcome 8: Time to haemostasis (minutes): sensitivity analysis removing trials with extreme outliers

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Analysis 2.9

Comparison 2: Fibrin‐based haemostatic agents (FBHAs) versus non‐FBHAs, Outcome 9: Haemostasis within a predefined time period

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Analysis 2.10

Comparison 2: Fibrin‐based haemostatic agents (FBHAs) versus non‐FBHAs, Outcome 10: Haemostasis within a predefined time period: sensitivity analysis removing trials that excluded participants with cirrhosis

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Analysis 2.11

Comparison 2: Fibrin‐based haemostatic agents (FBHAs) versus non‐FBHAs, Outcome 11: Haemostasis within a predefined time period: sensitivity analysis removing trials with extreme outliers

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Analysis 2.12

Comparison 2: Fibrin‐based haemostatic agents (FBHAs) versus non‐FBHAs, Outcome 12: Volume of intraoperative blood loss (mL)

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Analysis 2.13

Comparison 2: Fibrin‐based haemostatic agents (FBHAs) versus non‐FBHAs, Outcome 13: Postoperative transfusion

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Analysis 2.14

Comparison 2: Fibrin‐based haemostatic agents (FBHAs) versus non‐FBHAs, Outcome 14: Postoperative transfusion: sensitivity analysis removing trials that excluded participants with cirrhosis

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Analysis 2.15

Comparison 2: Fibrin‐based haemostatic agents (FBHAs) versus non‐FBHAs, Outcome 15: Reoperation

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Analysis 2.16

Comparison 2: Fibrin‐based haemostatic agents (FBHAs) versus non‐FBHAs, Outcome 16: Reoperation: sensitivity analysis removing trials with extreme outliers

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Analysis 2.17

Comparison 2: Fibrin‐based haemostatic agents (FBHAs) versus non‐FBHAs, Outcome 17: Postoperative bile leak

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Analysis 2.18

Comparison 2: Fibrin‐based haemostatic agents (FBHAs) versus non‐FBHAs, Outcome 18: Postoperative bile leak: sensitivity analysis removing trials that excluded participants with cirrhosis

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Analysis 2.19

Comparison 2: Fibrin‐based haemostatic agents (FBHAs) versus non‐FBHAs, Outcome 19: Postoperative intra‐abdominal collections

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Analysis 2.20

Comparison 2: Fibrin‐based haemostatic agents (FBHAs) versus non‐FBHAs, Outcome 20: Abdominal drain output (mL)

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Analysis 2.21

Comparison 2: Fibrin‐based haemostatic agents (FBHAs) versus non‐FBHAs, Outcome 21: Abdominal drain output (mL): sensitivity analysis removing trials with extreme outliers

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Analysis 2.22

Comparison 2: Fibrin‐based haemostatic agents (FBHAs) versus non‐FBHAs, Outcome 22: Time to removal of abdominal drains (days)

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Analysis 2.23

Comparison 2: Fibrin‐based haemostatic agents (FBHAs) versus non‐FBHAs, Outcome 23: Operating time (minutes)

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Analysis 2.24

Comparison 2: Fibrin‐based haemostatic agents (FBHAs) versus non‐FBHAs, Outcome 24: Length of hospital stay (days)

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Summary of findings 1. Fibrin‐based haemostatic agents versus no intervention or placebo

Fibrin‐based haemostatic agents compared with no intervention or placebo for reducing intraoperative blood loss and improving outcomes in adult liver surgery
Population: adults undergoing liver resection for cancer or benign disease Setting: liver resection unit Intervention: FBHAs applied to resection surface Comparison: haemostasis achieved through measures not including application of a topical agent (fibrin‐based or otherwise)
Outcome	*Anticipated risk difference (95% CI)**		Relative effect (95% CI)	Number of participants (RCTs)	Certainty of evidence	Comments
Outcome	Risk with no intervention	Risk with FBHAs	Relative effect (95% CI)	Number of participants (RCTs)	Certainty of evidence	Comments
Perioperative mortality Median follow‐up 1.5 months after liver resection (range 30 days to 6 months)	13 per 1000	34 per 1000 (12 to 89)	RR 2.58 (0.89 to 7.44)	782 (4)	⊕⊝⊝⊝ Very low^a,b	Defined as death, regardless of cause, occurring within 30 days of surgery in or outside hospital
Serious adverse events Median follow‐up 1.5 months after liver resection (range 30 days to 6 months)	435 per 1000	418 per 1000 (383 to 457)	RR 0.96 (0.88 to 1.05)	782 (4)	⊕⊝⊝⊝ Very low^a,b	Only 2/4 trials reported averse events according to the definition provided in ICH‐GCP 2016.
Postoperative transfusion Median follow‐up 1.5 months after liver resection (range 30 days to 6 months)	168 per 1000	175 per 1000 (129 to 235)	RR 1.04 (95% CI 0.77 to 1.40)	864 (5)	⊕⊝⊝⊝ Very low^a,b	—
Reoperation Median follow‐up 1.5 months after liver resection (range 30 days to 6 months)	7 per 1000	20 per 1000 (4 to 102)	RR 2.92 (0.58 to 14.61)	612 (2)	⊕⊝⊝⊝ Very low^a,b	—
Postoperative bile leak Median follow‐up 1.5 months after liver resection (range 30 days to 6 months)	113 per 1000	113 per 1000 (76 to 167)	RR 1.00 (0.67 to 1.48)	782 (4)	⊕⊝⊝⊝ Very low^a,b	—
*The risk in the intervention group (and its 95% CI) is based on the assumedrisk in the comparison group and the relative effect of the intervention (and its 95% CI). CI: confidence interval; FBHA: fibrin‐based haemostatic agent; RCT: randomised clinical trial; RR: risk ratio.
GRADE Working Group grades of evidence High certainty: we are very confident that the true effect lies close to that of the estimate of the effect. Moderate certainty: we are moderately confident in the effect estimate; the true effect is likely to be close to the estimate of the effect, but there is a possibility that it is substantially different. Low certainty: our confidence in the effect estimate is limited; the true effect may be substantially different from the estimate of the effect. Very low certainty: we have very little confidence in the effect estimate; the true effect is likely to be substantially different from the estimate of effect.
^a Downgraded one level for study limitations (overall high risk of bias). ^b Downgraded two levels due to serious imprecision (the optimal information size was not met (i.e. sample size < 1000), wide CIs in the result, few events, and the 95% CI includes both benefits and harms).

Summary of findings 1. Fibrin‐based haemostatic agents versus no intervention or placebo

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Summary of findings 2. Fibrin‐based haemostatic agents versus non‐fibrin‐based haemostatic agents

Fibrin‐based haemostatic agents compared with non‐fibrin‐based haemostatic agents for reducing intraoperative blood loss and improving outcomes in adult liver surgery
Population: adults undergoing liver resection for cancer or benign disease Setting: clinical setting in liver resection unit Intervention: FBHAs applied to resection surface Comparison: non‐FBHAs applied to resection surface
Outcome	Anticipated risk difference (95 % CI)		Relative effect (95% CI)	Number of participants (RCTs)	Certainty of evidence	Comments
Outcome	Risk with non‐FBHAs	Risk with FBHAs	Relative effect (95% CI)	Number of participants (RCTs)	Certainty of evidence	Comments
Perioperative mortality Median follow‐up 1.25 months (range 1 to 3 months)	47 per 1000	48 per 1000 (29 to 80)	RR 1.03 (0.62 to 1.72)	1436 (11)	⊕⊝⊝⊝ Very low^a,b	Defined as death, regardless of cause, occurring within 30 days of surgery in or outside hospital
Serious adverse events Median follow‐up 1 month (range 1 to 3 months)	736 per 1000	729 per 1000 (699 to 758)	RR 0.99 (0.95 to 1.03)	1176 (9)	⊕⊕⊝⊝ Low^a,c	4 trials defined adverse events according to the Medical Dictionary for Regulatory Activities.
Postoperative transfusion Median follow‐up 1 month (range 1 to 3 months)	270 per 1000	248 per 1000 (184 to 338)	RR 0.92 (0.68 to 1.25)	599 (7)	⊕⊝⊝⊝ Very low^a,b	—
Reoperation Median follow‐up 1.5 months (range 1 to 3 months)	163 per 1000	78 per 1000 (41 to 147)	RR 0.48 (0.25 to 0.90)	358 (3)	⊕⊝⊝⊝ Very low^a,b	1 trial reported an exceptionally high rate of reoperation in both groups; this is likely to have skewed the meta‐analysis.
Postoperative bile leak Median follow‐up 1.5 months (range 1 to 3 months)	31 per 1000	36 per 1000 (19 to 69)	RR 1.15 (0.60 to 2.21)	1115 (9)	⊕⊝⊝⊝ Very low^a,b	—
*The risk in the intervention group (and its 95% CI) is based on the assumedrisk in the comparison group and the relative effect of the intervention (and its 95% CI). CI: confidence interval; FBHA: fibrin‐based haemostatic agent; RCT: randomised clinical trial; RR: risk ratio.
GRADE Working Group grades of evidence High certainty: we are very confident that the true effect lies close to that of the estimate of the effect. Moderate certainty: we are moderately confident in the effect estimate; the true effect is likely to be close to the estimate of the effect, but there is a possibility that it is substantially different. Low certainty: our confidence in the effect estimate is limited; the true effect may be substantially different from the estimate of the effect. Very low certainty: we have very little confidence in the effect estimate; the true effect is likely to be substantially different from the estimate of effect.
^a Downgraded one level for study limitations (overall high risk of bias). ^b Downgraded two levels for imprecision (few events and wide 95% CI including both benefit and harm). ^c Downgraded one level for imprecision (95% CI including both benefit and harm).

Summary of findings 2. Fibrin‐based haemostatic agents versus non‐fibrin‐based haemostatic agents

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Table 1. Examples of fibrin‐based haemostatic agents and their main components

Product name	Fibrinogen concentration (mg/mL)	Thrombin concentration (IU/mL)	Factor XIII concentration (U/mL)	Antifibrinolytic agent
Beriplast P (CSL Behring, Germany)	90	500	60	Bovine aprotinin: 1000 KIU/mL
Biocol (LFB, France)	127	558	11	Bovine aprotinin: 3000 KIU/mL
Bolheal (Kaketsuken Pharmaceutical, Japan)	80	250	75	Bovine aprotinin: 1000 KIU/mL
Evicel – formerly Crosseal® (Omrix Biopharmaceuticals, Israel)	70	1000	None	None
Quixil (Omrix Biopharmaceuticals, Israel)	50	1000	None	Tranexamic acid: 85 to 105 mg/mL
Tachosil (Nycomed, Switzerland)	5.5^a	2.0^b	None	None
Tisseel (Baxter, Austria)	90	500	30	Bovine aprotinin: 3000 KIU/mL
^amg/cm². ^bIU/cm². KIU: kallikrein inhibitor units.

Table 1. Examples of fibrin‐based haemostatic agents and their main components

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Comparison 1. Fibrin‐based haemostatic agents (FBHAs) versus no intervention or placebo

Outcome or subgroup title	No. of studies	No. of participants	Statistical method	Effect size
1.1 Perioperative mortality Show forest plot	4	782	Risk Ratio (M‐H, Random, 95% CI)	2.58 [0.89, 7.44]

1.2 Serious adverse events Show forest plot	4	782	Risk Ratio (M‐H, Random, 95% CI)	0.96 [0.88, 1.05]

1.3 Haemostasis within a predefined time period Show forest plot	2	172	Risk Ratio (M‐H, Random, 95% CI)	2.12 [1.65, 2.73]

1.4 Volume of intraoperative blood loss (mL) Show forest plot	3	712	Mean Difference (IV, Random, 95% CI)	101.26 [15.81, 186.71]

1.5 Postoperative transfusion Show forest plot	5	864	Risk Ratio (M‐H, Random, 95% CI)	1.04 [0.77, 1.40]

1.6 Reoperation Show forest plot	2	612	Risk Ratio (M‐H, Random, 95% CI)	2.92 [0.58, 14.61]

1.7 Postoperative bile leak Show forest plot	4	782	Risk Ratio (M‐H, Random, 95% CI)	1.00 [0.67, 1.48]

1.8 Postoperative intra‐abdominal collections Show forest plot	6	906	Risk Ratio (M‐H, Random, 95% CI)	1.01 [0.81, 1.28]

1.9 Postoperative intra‐abdominal collections: sensitivity analysis Show forest plot	5	859	Risk Ratio (M‐H, Random, 95% CI)	1.04 [0.83, 1.32]

1.10 Abdominal drain output (mL) Show forest plot	3	447	Mean Difference (IV, Random, 95% CI)	‐71.20 [‐423.54, 281.14]

1.11 Time to removal of abdominal drains (days) Show forest plot	4	822	Mean Difference (IV, Random, 95% CI)	‐0.53 [‐2.03, 0.97]

1.12 Operating time (minutes) Show forest plot	3	479	Mean Difference (IV, Random, 95% CI)	14.86 [‐0.34, 30.06]

1.13 Length of hospital stay (days) Show forest plot	3	479	Mean Difference (IV, Random, 95% CI)	‐0.15 [‐1.63, 1.33]

Comparison 1. Fibrin‐based haemostatic agents (FBHAs) versus no intervention or placebo

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Comparison 2. Fibrin‐based haemostatic agents (FBHAs) versus non‐FBHAs

Outcome or subgroup title	No. of studies	No. of participants	Statistical method	Effect size
2.1 Perioperative mortality Show forest plot	11	1436	Risk Ratio (M‐H, Random, 95% CI)	1.03 [0.62, 1.72]

2.2 Perioperative mortality: sensitivity analysis removing trials that excluded participants with cirrhosis Show forest plot	8	1142	Risk Ratio (M‐H, Random, 95% CI)	1.03 [0.58, 1.80]

2.3 Perioperative mortality: sensitivity analysis removing a trial that investigated a non‐commercial FBHA Show forest plot	10	1378	Risk Ratio (M‐H, Random, 95% CI)	0.99 [0.58, 1.70]

2.4 Serious adverse events Show forest plot	9	1176	Risk Ratio (M‐H, Random, 95% CI)	0.99 [0.95, 1.03]

2.5 Serious adverse events: sensitivity analysis removing trials that excluded participants with cirrhosis Show forest plot	6	882	Risk Ratio (M‐H, Random, 95% CI)	0.99 [0.94, 1.03]

2.6 Time to haemostasis (minutes) Show forest plot	8	1093	Mean Difference (IV, Random, 95% CI)	‐1.58 [‐2.68, ‐0.49]

2.7 Time to haemostasis (minutes): sensitivity analysis removing trials that excluded participants with cirrhosis Show forest plot	5	799	Mean Difference (IV, Random, 95% CI)	‐1.77 [‐2.54, ‐1.01]

2.8 Time to haemostasis (minutes): sensitivity analysis removing trials with extreme outliers Show forest plot	7	967	Mean Difference (IV, Random, 95% CI)	‐1.86 [‐2.52, ‐1.21]

2.9 Haemostasis within a predefined time period Show forest plot	7	789	Risk Ratio (M‐H, Random, 95% CI)	1.30 [1.04, 1.62]

2.10 Haemostasis within a predefined time period: sensitivity analysis removing trials that excluded participants with cirrhosis Show forest plot	5	614	Risk Ratio (M‐H, Random, 95% CI)	1.54 [1.22, 1.94]

2.11 Haemostasis within a predefined time period: sensitivity analysis removing trials with extreme outliers Show forest plot	5	635	Risk Ratio (M‐H, Random, 95% CI)	1.11 [0.94, 1.31]

2.12 Volume of intraoperative blood loss (mL) Show forest plot	3	176	Mean Difference (IV, Random, 95% CI)	111.24 [‐102.96, 325.45]

2.13 Postoperative transfusion Show forest plot	7	599	Risk Ratio (M‐H, Random, 95% CI)	0.92 [0.68, 1.25]

2.14 Postoperative transfusion: sensitivity analysis removing trials that excluded participants with cirrhosis Show forest plot	5	423	Risk Ratio (M‐H, Random, 95% CI)	0.79 [0.56, 1.12]

2.15 Reoperation Show forest plot	3	358	Risk Ratio (M‐H, Random, 95% CI)	0.48 [0.25, 0.90]

2.16 Reoperation: sensitivity analysis removing trials with extreme outliers Show forest plot	2	242	Risk Ratio (M‐H, Random, 95% CI)	0.63 [0.12, 3.22]

2.17 Postoperative bile leak Show forest plot	9	1115	Risk Ratio (M‐H, Random, 95% CI)	1.15 [0.60, 2.21]

2.18 Postoperative bile leak: sensitivity analysis removing trials that excluded participants with cirrhosis Show forest plot	7	939	Risk Ratio (M‐H, Random, 95% CI)	1.19 [0.58, 2.44]

2.19 Postoperative intra‐abdominal collections Show forest plot	6	664	Risk Ratio (M‐H, Random, 95% CI)	0.72 [0.24, 2.21]

2.20 Abdominal drain output (mL) Show forest plot	3	296	Mean Difference (IV, Random, 95% CI)	‐212.49 [‐939.53, 514.55]

2.21 Abdominal drain output (mL): sensitivity analysis removing trials with extreme outliers Show forest plot	2	177	Mean Difference (IV, Random, 95% CI)	138.53 [66.51, 210.55]

2.22 Time to removal of abdominal drains (days) Show forest plot	4	332	Mean Difference (IV, Random, 95% CI)	0.07 [‐1.39, 1.53]

2.23 Operating time (minutes) Show forest plot	4	419	Mean Difference (IV, Random, 95% CI)	‐1.27 [‐22.73, 20.19]

2.24 Length of hospital stay (days) Show forest plot	5	503	Mean Difference (IV, Random, 95% CI)	‐0.20 [‐1.36, 0.96]

Comparison 2. Fibrin‐based haemostatic agents (FBHAs) versus non‐FBHAs

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