Official Journal of

the British Blood Transfusion Society

Transfusion Medicine | SHORT COMMUNICATION

The application of a haemorrhage assessment tool in evaluating

control of bleeding in a pilot trauma haemorrhage trial

N. Curry,1,2 C. Foley,3 H. Wong,1,2,4 A. Mora,3 E. Curnow,3 A. Zarankaite,3 R. Hodge,3 V. Hopkins,3 A. Deary,3 J. Ray,5
P. Moss,6 M. J. Reed,7 S. Kellett,8 R. Davenport9 & S. Stanworth1,2,4
1
Department of Haematology, Oxford University Hospitals NHS Trust, Oxford, UK, 2 NIHR BRC Blood Theme, Oxford University,
Oxford, UK, 3 NHS Blood and Transplant Clinical Trials Unit, NHS Blood and Transplant, Cambridge and Bristol, UK, 4 NHS Blood and
Transplant, John Radcliffe Hospital, Oxford, UK, 5 Department of Emergency Medicine, John Radcliffe Hospital, Oxford, UK, 6 Department
of Emergency Medicine, St. George’s Hospital, London, UK, 7 Emergency Medicine Research Group Edinburgh (EMERGE), Royal
Infirmary of Edinburgh, Edinburgh, UK, 8 Department of Anaesthetics, University Hospital Southampton NHS Foundation Trust,
Southampton, UK, and 9 Centre for Trauma Sciences, Blizard Institute, Queen Mary University of London, London, UK

Received 1 May 2019; accepted for publication 6 October 2019

SUMMARY Major haemorrhage is one of the leading causes of death world-

Objectives: To determine whether it was feasible to use a
haemorrhage assessment tool (HAT) within a trauma trial and
whether the data obtained could differentiate patients who had
achieved haemostasis.
Background: Major haemorrhage is one of the leading causes of
death worldwide, affecting 40% of trauma patients. Clinical trials
evaluating haemostatic interventions often use transfusion out-
comes as a primary endpoint. Transfusion is highly dependent
on local practice, limiting its reliability as a robust, transferable
endpoint.
Methods: A 5-point HAT questionnaire was applied to partici-
pants enrolled into the EFIT-1 trial. This RCT evaluated the fea-
sibility of administering a 6 g fibrinogen concentrate to patients
with severe trauma haemorrhage.
Results: Of participants, 98% completed a HAT; 75% partici-
pants had ‘achieved haemostasis’ at the time of tool completion,
as determined by clinical acumen alone. HAT scores were able
to differentiate which participants required transfusion after 3 h.
Of participants, 56% were transfused red blood cells when they
scored 0–2, compared to 17% with HAT scores between 3 and 5.
Conclusion: This study has confirmed the feasibility of using
a HAT during the emergency care of patients suffering trauma
haemorrhage, and future studies should be conducted to deter-
mine its value as an endpoint in haemostasis studies.
Key words: haemorrhage asssessment tool, major haemor-
rhage, randomised controlled trial, trauma.
Correspondence: Dr. Nicola Curry, Oxford University Hospitals NHS
Foundation Trust, Oxford Haemophilia & Thrombosis Centre,
Churchill Hospital, OX3 7LE, UK.
Tel.: 01865 225316; fax: 01865 225608;
e-mail: nicola.curry@ouh.nhs.uk
wide. It affects up to 40% of trauma patients (Stanworth et al.,
2016) and is one of the most common causes of death in women
at the time of delivery (Say et al., 2014). Often, clinical trials
evaluating interventions to treat bleeding select transfusion end-
points (such as reduction in red cell usage) (Rahe-Meyer et al.,
2016; Collins et al., 2017) as identified in a recent systematic
review of pro-haemostatic agents (Fabes et al., 2018), and only
a few larger trials have assessed mortality (CRASH-2 trial col-
laborators, 2010; Holcomb et al., 2015; WOMAN trial Collabo-
rators, 2017; Brenner et al., 2018). However, transfusion therapy
is highly dependent on local clinical practice, which reduces its
reliability as a robust endpoint, and at best, transfusion require-
ment can be viewed as a surrogate, rather than direct, measure
of bleeding.
Control of bleeding remains an attractive and relevant end-
point but is a notoriously difficult question to standardise in a
multicentre trial and may become increasingly relevant as more
haemostasis studies are conducted. The PROPPR (Pragmatic,
Randomized Optimal Platelet and Plasma Ratios) study was
the first to use ’time to haemostasis’ as a secondary endpoint.
This study evaluated the effect of two blood transfusion ratios
on mortality in trauma haemorrhage (Holcomb et al., 2015).
Importantly, data (adjusted for multiple variables) from this trial
demonstrated that shorter times to haemostasis were reported
to be independently associated with reduced 30-day mortality
(Holcomb, 2018).
We report the use of a trial-specific haemorrhage assess-
ment tool (HAT), adapted from the tool used in PROPPR (Hol-
comb et al., 2015), within a multicentre UK trauma trial (Curry
et al., 2018). We piloted the use of this tool, with the record-
ing of a HAT score, to (i) determine whether it was feasible
to use by evaluating the numbers of HATs completed within
a trauma RCT, (ii) understand how often a participant had
achieved haemostasis and (iii) determine whether the HAT score

© 2019 British Blood Transfusion Society doi: 10.1111/tme.12644

2 N. Curry et al.

Fig. 1. Haemorrhage assessment tool, E-FIT-1 trial. Definitions for the HAT: Q4a - this question should be posed to the trauma team leader and should
be based on the patient’s current clinical status (in the last 30 minutes); Q4b- stable BP defined as a systolic BP which is not falling and has variation of
less than 20mmHg during the 30 minutes prior to the HAT; Q4c - stable HR defined as a HR variation of less than 20 bpm when comparing the average
HR at the time of the HAT with the 30 minutes prior to the HAT; Q4d - stable urine output is defined as production of urine of at least 10mL per hour (if
the patient is an uric the answer given should be no); Q4e - decreasing lactate or base excess confirmed if the value for the most recent result is less than
the preceding sample; Q4f - rate of blood transfusion reducing is defined as the number of units (RBC, FFP, platelets and cryoprecipitate) administered
in the last 30 minutes is less than the 30 minutes preceding this time; Q5-6 -clinical opinions (where relevant) should be sought from the surgeon or
radiologist based on the current status of the patient. The HAT assessment score was measured out of 5, where a score of 5 was calculated if ‘yes’ was
given for all answers Q4b - Q4f. For Q4d - if not applicable was returned, the score given for this question was a zero.

Transfusion Medicine, 2019 © 2019 British Blood Transfusion Society

 A haemorrhage assessment tool for major traumatic bleeding 3
provided additional information when compared to simple ’clin-
ical acumen’.
METHODS
Development of tool
The HAT was based on the tool used in the PROPPR study and
used five questions aimed at recognising patients in haemor-
rhagic shock. Our HAT used the addition of two further criteria
asking: ’is the base excess or lactate improving?’ and ’is the trans-
fusion rate decreasing?’. These additional questions were devel-
oped by consensus from trauma surgeons and trauma anaes-
thesiologists who were active in trauma haemorrhage research
across Europe.
The HAT was applied to recruited patients at five major
trauma centres in the United Kingdom as part of the E-FIT-1
randomised controlled trial, which evaluated the feasibility of
administering a 6 g fibrinogen concentrate to patients with
severe trauma and major bleeding (Curry et al., 2018). Full
details of the study have been described (Curry et al., 2018).
In brief, patients were eligible if they were adults, were actively
bleeding and in haemorrhagic shock and required activation
of the major haemorrhage protocol or had already received
a transfusion of emergency red blood cells. The protocol was
approved by an independent ethics committee, the NRES Com-
mittee South Central – Oxford C (15/S3/0316) and MHRA
(25 224/0003/001–0001).
As part of the study, a HAT was completed 3 h after hos-
pital admission (Fig. 1). Figure 1 describes how to score the
tool, with a maximum score of 5 for participants who had fully
achieved haemostasis. Face-to-face education was completed
for research staff at each participating site prior to the start
of the study. Three hours was chosen following publication of
the PROPPR study data, which demonstrated that the major-
ity of deaths from trauma haemorrhage occurred within this
timeframe.
RESULTS
Patients
A total of 48 participants were enrolled in the E-FIT-1 study,
with 24 participants each in the intervention and comparator
arms. Forty-seven HATs were completed (98%) at the 3-h time
point (±60 min), 24 in the active arm and 23 in the placebo arm
(baseline characteristics Table 1). There was one missing data
point in one of the placebo arm questionnaires (lactate result not
completed). The median time of completion of the tool was 2 h
40 min (IQR: 2 h 15 to 3 h 03) from admission.
HAT score results
Of the 47 completed questionnaires, 17 participants were in the
theatre at the time of completion of the HAT, and of this group,
9 (53%) were deemed to have achieved anatomic haemostasis at
© 2019 British Blood Transfusion Society
3 h as defined by the surgeon, confirming no further bleeding
intraoperatively. Only one of the three participants being treated
in interventional radiology had achieved radiological haemosta-
sis at 3 h.
Comparing the HAT score to a question on control
of bleeding
An additional question in the tool was: ’does the trauma team feel
that haemostasis has been achieved?’. We compared the results
of this question with the 5-point HAT score. A total of 45 HAT
scores were obtained for this question and these results were
assessed (Table 2). Thirty-six participants were documented to
have ’achieved haemostasis’ by the trauma team at the point
of HAT completion (18 placebo arm, 18 active arm); within
this group, 12 participants were in the theatre at the time of
HAT completion, and 9 participants (75%) were also deemed to
have achieved surgical haemostasis. Nine participants had ’not
achieved haemostasis’ at 3 h; five of this group were in theatre,
and all surgical teams agreed that the participants were still
bleeding.
Relationship to transfusion use
Table 3 shows the participants’ transfusion requirements when
grouped by their HAT score (HAT scores of: 0–2, 3 and 4–5)
(See Fig. 1 for details on scoring). Of the 47 HAT assessments, 46
were completed in full (24 intervention arm, 22 placebo). HAT
scores were able to broadly differentiate between participants
requiring transfusion after 3 h. If the HAT score was between
0 and 2, just over half of the participants were transfused with
RBC compared to fewer than one in five of those with scores
between 3 and 5. Similar results were seen for the use of FFP. In
27 of the 47 completed HAT questionnaires (57%), urine output
data were recorded as ’not applicable’ because there were no
clinical means for determining urine output (commonly due to
no catheter sited).
Patients who failed to achieve bleeding control
More than twice as many participants deemed to have ongoing
bleeding, according to the stand-alone question, continued
to require blood components in the 3 h after the assessment
(between 3 and 6 h from admission). The majority of partic-
ipants did not require additional RBC treatment in either
study group after 3 h of admission, but for those with a
HAT question assessment recording ongoing bleeding, the
participants who received blood (n = 4) required 13 units
between 3 and 6 h (IQR: 5–21) compared to 2 units (IQR:
2–3) in the group (n = 7) where haemostasis was reported as
achieved.
DISCUSSION
This study has shown the feasibility of using a HAT during the
emergency care of trauma patients suffering with significant
Transfusion Medicine, 2019
4 N. Curry et al.

Table 1. Haemorrhage assessment results according to study arm

Active arm Placebo arm Overall

(n = 24/24) (n = 23/24)2 (n = 48)

Bleeding controlled 18 18 36
Blood pressure stable or increasing 16 18 34
Heart rate stable or maintained within normal range 18 18 36
Urine output stable or >0·5 mL kg h−11 9 9 18
Lactate or base excess level decreasing 19 17 36
Rate of blood transfusion reducing 19 20 39
Participant in theatre 10 7 17
Surgeon confirmed anatomic haemostasis 5 4 9
Participant in interventional radiology 2 1 3
Resolution of a radiological blush 1 0 1

1 Questionwas reported as not applicable/not available for 27 participants.

2 Only23 participants completed the HAT for the placebo arm.
Data are numbers.

Table 2. Characteristics of the groups according to whether the trauma team deemed them to be bleeding or not (n = 45)

Haemostasis Haemostasis not

achieved (n = 36) achieved (n = 9)
Number (%) Number (%)

Number receiving blood components at time of assessment 14 (39) 8 (89)

Blood pressure stable or increasing 30 (83) 2 (22)
Heart rate stable or maintained within normal range 32 (89) 2 (22)
Urine output stable or > 0·5 mL kg h−11 17/18 (94) 1/1 (100)
Lactate or base excess level decreasing 31 (86) 4 (44)
Rate of blood transfusion reducing 33 (92) 5 (56)
Median score (of 5) for HAT 4 0
Participant in theatre 12 5
Surgeon confirmed anatomic haemostasis 9 (75) 0 (0)
Participant in interventional radiology 2 1
Resolution of a radiological blush 0 (0) 1 (100)
Transfusion data
Number receiving RBC between 3 and 6 h 7 (19) 4 (44)
Median number of RBC units received between 3 and 6 h for whole group 0 (IQR:0–0) 0 (IQR: 0–6)
Median number of FFP units received between 3 and 6 h 0 (IQR:0–0) 2 (IQR: 0–6)

1 Question was reported as not applicable/not available for 27 participants.

trauma haemorrhage. Very high rates of completion were
observed for participants who were alive at the 3-h time point.
Three quarters of all participants had haemorrhage control
achieved by 3 h. The results of the study-specific HAT appeared
to be able to distinguish between those still actively bleeding
and those no longer bleeding. Patients with a score of 0–2 were
three times as likely to receive a transfusion of either RBC or
FFP in the 3 h following the assessment.
The HAT, when compared to clinical acumen alone – i.e. ask-
ing a simple question (does the trauma team feel the patient
has achieved haemostasis?) – provided very similar results. The
HAT score and the trauma team leader’s assessment concurred
in more than three quarters of all cases, suggesting that clin-
ical judgement in this small group appears to be reliable as
a scoring method. These data suggest that the HAT may be
better utilised to find risk of ongoing bleeding as it appears
to differentiate those patients requiring an ongoing transfusion
need rather than determining whether a patient has achieved
haemostasis.
It has not been possible to determine whether any of the single
parameters within the HAT are sensitive to detecting cessation
of bleeding due to the small sample size. The question regarding
urine output, which was included in our HAT tool, was not
answered in 27 of 47 cases. This was due to the emergency nature
of the study and reflected the short timeframe within which
the HAT was completed. Future adaptations of this HAT would
benefit from reviewing this parameter.
When compared to the PROPPR study, the findings from
our HAT appear consistent. In the PROPPR study, the median
time to haemostasis was 105 min (IQR, 64–179 min) in the

Transfusion Medicine, 2019 © 2019 British Blood Transfusion Society

 A haemorrhage assessment tool for major traumatic bleeding 5

Table 3. Haemorrhage assessment tool scores and transfusion requirement (n = 46)

RBC units from RBC units FFP units from FFP units
HAT score admission to 3 h between 3 and 6 h admission to 3 h between 3 and 6 h

0–2 (n = 9) 12 (6–23) 3–18 (100%) 2 (0–6) 0–24 (56%) 8 (6–16) 2–15 (100%) 0 (0–6) 0–12 (44%)
3 (n = 8) 2 (1–3) 0–8 (87·5%) 0 (0–0) 0–2 (12·5%) 2 (1·5–4·5) 0–8 (87·5%) 0 (0–0) 0–1 (12·5%)
4 and 5 (n = 29) 3 (2–5) 0–12 (86%) 0 (0–0) 0–4 (17%) 3 (1–6) 0–13 (76%) 0 (0–0) 0–4 (10%)

Data are presented as median and IQR for units of RBC or FFP, followed by the range of units.
The data in % represent the proportion of the group in receipt of a transfusion.

intervention arm compared to 100 min (IQR, 56–181 min)
in the comparator arm, (P = 0·44). There was a signifi-
cantly greater number of participants in the 1:1:1 arm who
achieved anatomic haemostasis (86·1%) compared to the 1:1:2
group (78·1%, P = 0·006). The results from our single-point
study showed a similar result, such that 75% of patients had
achieved haemostasis at 3 h. Time to haemostasis would be
a more ideal data point to collect but does require significant
research resources, which was undertaken as a continuous
one-to-one follow-up in the US study for every participant
in that study, allowing a definitive time to haemostasis to be
recorded.
There are limitations to this study, most notably the small
sample size. Furthermore, the majority of the participants in this
study were deemed to have achieved haemostasis by the 3-h time
point, limiting the comparisons that could be made between
actively and non-actively bleeding patients. Future studies would
need to apply the HAT tool at a much earlier time point, perhaps
at 1 h after admission to hospital. The tool itself appeared to
perform no better than clinical acumen, likely reflecting the
automatic use of many of the HAT parameters by clinicians
within their decision-making. As such, a HAT may only ever
be used in the clinical trial setting. This study did not set out
to evaluate the relationship between the HAT score and other
clinical outcome data (i.e. ICU admission, length of stay or
mortality), and these relationships would be worth exploring in
larger studies.
Validated bleeding assessment tools are available that have
been designed to look at either the baseline bleeding risk for
patients considered to have an inherited bleeding disorder (i.e.
International Society for Thrombosis and Hemostasis Bleed-
ing Assessment Tool (ISTH BAT) (Rodeghiero et al., 2010))
or to see how much bleeding has already occurred following
a clinical bleeding episode (World Health Organization bleed-
ing assessment tool (Kaufman et al., 2015)). No tool has been
validated and used contemporaneously to assess ’cessation of
bleeding’.
The results of our study and the PROPRR trial findings sug-
gest that HATs can be completed within highly complex major
haemorrhage RCTs, which may have value as endpoints in
haemostasis clinical studies.
ACKNOWLEDGMENTS
The trial was funded by CSL Behring.
N. C. and S. S. designed the study, wrote the protocol, analysed
data and wrote the manuscript. C. F. led the CTU running of the
trial, analysed data and wrote the manuscript. H. W., A. M., R.
H., V. H. and A. D. conducted the study; conducted CTU trial
work; and read and approved the final manuscript. E. C. and A.
Z. designed and conducted the statistical analysis for the trial and
wrote and approved the final manuscript. J. R., P. M., M. J. R., S. Z.
and R. D. led recruitment at sites and read and approved the final
manuscript. All authors read and approved the final manuscript.
CONFLICT OF INTEREST
The authors have no competing interests.

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