The prognostic value of thrombelastography in identifying neurosurgical patients with worse prognosis. Blood Coagul Fibrinolysis

ArticleinBlood coagulation & fibrinolysis: an international journal in haemostasis and thrombosis 22(5):416-9 · April 2011with42 Reads
Impact Factor: 1.40 · DOI: 10.1097/MBC.0b013e3283464f53 · Source: PubMed
Abstract

Coagulopathy in patients with intracranial haemorrhage or traumatic brain injury (TBI) is associated with clinical deterioration and worse outcome. Whole blood viscoelastic haemostatic assays, like thrombelastography (TEG), might aid conventional coagulation assays in identification of patients with worse prognosis. We performed a review of patients (totalling 78 patients) with primary acute intracranial haemorrhage or isolated TBI admitted to a neurointensive care unit (NICU) for more than 24 h during a period of 9 months, who had TEG analysis performed at admission. Primary outcome was all-cause 30-day mortality, whereas decline in Glasgow Coma Scale (GCS) score at 24 h after admission or death due to cerebral incarceration were secondary outcomes. Patients were defined as hypocoaguable if TEG reaction time was more than 8 min, angle less than 55° and/or maximal amplitude less than 51 mm. Patients were defined hypocoaguable according to conventional coagulation assays if international normalized ratio was more than 1.3, platelet counts less than 100×10/l and/or activated partial thromboplastine time more than 35 s. Eight patients were hypocoaguable by TEG on admission to NICU and had higher 30-day mortality (63% vs. 16%, P=0.008), more often declined in GCS (57% vs. 16%, P=0.02) and expired due to cerebral incarceration (50% vs. 6%, P=0.02). Hypocoagulability by TEG, lower admission GCS and subarachnoid haemorrhage were independently associated with higher 30-day mortality [TEG: odds ratio (OR) 14.8 (2.2-100.1), P=0.006; GCS: OR 1.3 (1.1-1.5), P=0.006; subarachnoid haemorrhage: OR: 5.3 (1.3-22.3), P=0.02]. Only two patients were hypocoaguable by both conventional coagulation assays and TEG. The current data indicate that hypocoagulability by TEG at admission to NICU predicts worse prognosis. Low concordance with conventional coagulation assays indicates that TEG might be valuable in identifying patients with clinically relevant coagulopathy.

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The prognostic value of thrombelastography in identifying
neurosurgical patients with worse prognosis
Nis A. Windeløv
a,b
, Karen-Lise Welling
c
, Sisse R. Ostrowski
a
and Pa
¨
r I. Johansson
a
Coagulopathy in patients with intracranial haemorrhage or
traumatic brain injury (TBI) is associated with clinical
deterioration and worse outcome. Whole blood viscoelastic
haemostatic assays, like thrombelastography (TEG), might
aid conventional coagulation assays in identification of
patients with worse prognosis. We performed a review of
patients (totalling 78 patients) with primary acute
intracranial haemorrhage or isolated TBI admitted to a
neurointensive care unit (NICU) for more than 24 h during a
period of 9 months, who had TEG analysis performed at
admission. Primary outcome was all-cause 30-day mortality,
whereas decline in Glasgow Coma Scale (GCS) score at
24 h after admission or death due to cerebral incarceration
were secondary outcomes. Patients were defined as
hypocoaguable if TEG reaction time was more than 8 min,
angle less than 55- and/or maximal amplitude less than
51 mm. Patients were defined hypocoaguable according to
conventional coagulation assays if international normalized
ratio was more than 1.3, platelet counts less than 100 T 10
9
/l
and/or activated partial thromboplastine time more than
35 s. Eight patients were hypocoaguable by TEG on
admission to NICU and had higher 30-day mortality (63% vs.
16%, P U 0.008), more often declined in GCS (57% vs. 16%,
P U 0.02) and expired due to cerebral incarceration (50% vs.
6%, P U 0.02). Hypocoagulability by TEG, lower admission
GCS and subarachnoid haemorrhage were independently
associated with higher 30-day mortality [TEG: odds ratio
(OR) 14.8 (2.2100.1), P U 0.006; GCS: OR 1.3 (1.11.5),
P U 0.006; subarachnoid haemorrhage: OR: 5.3 (1.322.3),
P U 0.02]. Only two patients were hypocoaguable by both
conventional coagulation assays and TEG. The current data
indicate that hypocoagulability by TEG at admission to NICU
predicts worse prognosis. Low concordance with
conventional coagulation assays indicates that TEG might
be valuable in identifying patients with clinically relevant
coagulopathy. Blood Coagul Fibrinolysis 22:000000 ß 2011
Wolters Kluwer Health | Lippincott Williams & Wilkins.
Blood Coagulation and Fibrinolysis 2011, 22:000–000
a
Section for Transfusion Medicine, Capital Region Blood Bank,
b
Department of
Anaesthesia, Centre of Head and Orthopedics and
c
Department of Neuro-
Intensive Care, Rigshospitalet, Copenhagen University Hospital, Copenhagen,
Denmark
Correspondence to Nis A. Windeløv, Section for Transfusion Medicine, Capital
Region Blood Bank, Rigshospitalet, Copenhagen University Hospital,
Blegdamsvej 9, DK-2100 Copenhagen, Denmark
Tel: +45 20653608; fax: +45 35390038; e-mail: nis.windelov@gmail.com
Received 26 August 2010 Revised 21 February 2011
Accepted 1 March 2011
Introduction
Coagulopathy in patients suffering from acute intracra-
nial haemorrhage [1] or traumatic brain injury (TBI) [2] is
associated with worse outcome, presumable due to pro-
gression in haemorrhage [3]. Coagulopathy can not only
be induced by anticoagulant medication [4] or extensive
treatment with intravenous fluids [2], but can also origin
from hyper activation of coagulation with subsequent
consumption of coagulation factors and platelets [5,6].
Coagulopathy is primarily diagnosed by measurements of
prothrombin time (PT) or International Normalized
Ratio (INR), activated partial thromboplastine time
(APTT) and/or platelet count. With increased awareness
of the importance of cellular components for haemostasis,
functional whole blood viscoelastic haemostatic assays
(VHA) such as thrombelastography (TEG) and rotational
thrombelastometry are gaining attention [7].
The aim of the present study was to evaluate the associ-
ation between TEG and conventional coagulation tests
and the predictive value of TEG for clinical deterioration
and mortality in patients with isolated primary intra-
cranial haemorrhage and/or isolated TBI when perform ed
at admission to a NICU at a tertiary referral hospital.
Method
TEG was introduced at our neurointensive care unit
(NICU) in September 2007July 2008 as a standard
laboratory test taken concurrently wi th other blood
samples upon admission to the NICU for all patients
with expected stay of more than 24 h.
Computed tomography scanning was not standardized
during the study period and direct visualization of
haemorrhage progression could not be performed.
Instead, a clinical indicator on the basis of the Glasgow
Coma Scale (GCS) Score was chosen, patients were
routinely scored by consulting anaesthesiologist and
neurosurgeon at NICU admission and approximately
24 h after admission during a pause of sedation. If GCS
were lower at 24 h compared with admission, the patient
was categorized with decline in GCS, indicating pro-
gression of insult. For patients intubated at admission
and/or at 24 h, verbal response was exempted due to score
Original article 1
0957-5235 ß 2011 Wolters Kluwer Health | Lippincott Williams & Wilkins DOI:10.1097/MBC.0b013e3283464f53
Page 1
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
CE: Madhur; MBC/200832; Total nos of Pages: 4;
MBC 200832
inaccuracy and only eye and motor response were used to
calculate a possible decline in GCS, as found valid by
Kung et al. [8]. To further access if patients expired due to
progression of insult or by secondary causes, expiration
due to cerebral incarceration was recorded.
TEG (TEG 5000; Haemoscope Corporation, Niles, Illi-
nois, USA) was performed in accordance with instructions
of the manufacture and performed within 2 h of blood
sampling. TEG parameters of reaction time, angle and
maximal amplitude and conventional coagulation data of
platelet count (XE-2100; Kyoto Sysmex, Kobe, Japan),
INR and APTT (both Q Hemostasis; Medinor, Brønshøj,
Denmark) at admission were collected from hospital
databases. Dece ased by cerebral incarceration within
30 days of admission (yes/no) and received neurosurgery
during the first 24 h after admission to NICU (yes/no)
were retrieved from hospital journals blinded to results of
TEG and conventional coagulation assays. Thirty-day
all-cause mor tality was retrieved from the Danish civil
registry. Approval from Danish data protection agency to
collect and store data was obtained.
Patients were dichotomized as hypocoaguable or nonhy-
pocoaguable by both conventional coagulation test (INR,
APTT and platelet counts) and TEG. For conventional
coagulation test, cut-off values were adopted from Wafai-
sade et al. [2] who reported that INR more than 1.3 units
(which equals a PT ratio of <70%), APTT more than 35 s
and/or platelet counts less than 100 10
9
/l was predictive
of worse outcome for patients with TBI. Cut-off values
for TEG were as reported by the manufacturer, reaction
time of more than 8 min, alpha angle less than 558 and/or
maximal amplitude of less than 51 mm, defined patients
as hypocoaguable.
TEG was not available for the staff; accordingly, TEG
values did not influence treatment. Treatment of coagulo-
pathy according to conventional coagulation assays was
performed using fresh frozen plasma (FFP) and/or platelet
concentrates. To assess if treatment confounded the associ-
ation of coagulopathy by conventional coagulation assays
and outcome, we investigated the usage of FFP and
platelet concentrates in hypocoaguable vs. nonhypocoagu-
able patients according to conventional coagulation assays.
Statistical analysis
Hypocoaguable patients were compared with nonhypo-
coaguable patients for both TEG and conventional
coagulation analysis. KolmogorovSmirnov test was per-
formed for all variables and due to nonnormalized distri-
bution of data numeric variables were reported as
medians (interquartile range) and categorical variables
by numbers (percentage). MannWhitney U-test was
performed for numerical variables and x
2
test or Fisher’s
exact test for categorical variables were appropriate.
Univariable logistic regressions with 30-day mortality
as dependent variable were performed for predefined
explanatory variables: age, GCS by admission, the diag-
nosis carrying the highest mortality in the cohort, hypo-
coagulability by conventional coagulation analysis and
hypocoagulability by TEG. Variables with P less than
0.1 was assumed to influence mortality and were included
in a multivariable logistic regression model. Data
were analysed using Statistical Package for the Social
Sciences version 17 (SPSS, IBM Corp., Somer, New York,
USA) and P less than 0.05 was considered statistically
significant.
Results
One hundred and forty patients were admitted to the
NICU during the study period due to intracranial dis-
eases with expected stay of more than 24 h. Of these
140 patients, 59 were admitted due to other reasons than
isolated primary intracranial haemorrhage and/or isolated
TBI and were therefore excluded. A further three
patients were excluded due to missing or invalid TEG
analysis, totalling 78 eligible patients. One of the
78 patients missed GCS at admission and at 24 h and
was exempted from calculations involving GCS.
The 78 patients are presented in Table 1. Eight of the
patients were hypocoaguable according to TEG at admis-
sion, whereas 16 were hypocoaguable according to conven-
tional coagulation assays, see Table 2. Only two patients
were hypocoaguable by both conventional coagulation
assays and TEG. Patients with hypocoaguable as compared
with nonhypocoaguable TEG results at admission more
frequently declined in GCS when rescored at 24 h after
admission (four of seven vs. 11 of 70, P ¼ 0.02) and had
higher 30-day mortality either due to cerebral incarceration
(four of eight vs. four of 70, P ¼ 0.02) or due to all causes
(five of eight vs. 11of 70, P ¼ 0.008), whereas this is not
found when comparing patients hypocoaguable by con-
ventional coagulation assays, Table 2.
2 Blood Coagulation and Fibrinolysis 2011, Vol 22 No 00
Table 1 Demographics and outcome
Number of patients 78
Age 55 (4563)
Male sex 47 (60%)
Diagnosis
Epidural haemorrhage 11 (14%)
Subdural haemorrhage 15 (19%)
Subarachnoid haemorrhage 28 (36%)
Intracerebral haemorrhage 11 (14%)
Traumatic brain injury 13 (17%)
Glasgow Coma Scale (GCS) Score
GCS upon admission to NICU 8 (414)
GCS approximately 24 h after admission to NICU 11 (715)
Decline in GCS during first 24 h in NICU 15 (19%)
Surgery
Underwent neurosurgery during first 24 h in NICU 43 (55%)
Outcome
Length of stay in NICU 8 (312)
Deceased by cerebral incarceration within 30 days of
arrival to NICU
8 (10%)
Deceased within 30 days of arrival to NICU 16 (21%)
Categorical variables stated as absolute numbers with percentage in parenthesis
and numerical values as median with interquartile range in parenthesis. NICU,
neurointensive care unit.
Page 2
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CE: Madhur; MBC/200832; Total nos of Pages: 4;
MBC 200832
Diagnosis of subarachnoid haemorrhage (diagnosis found
to carry highest 30-day mortality), lower GCS at arrival to
the NICU and hypocoagulability according to TEG, were
found to be independently associated with 30-day all-
cause mortality, see Table 3.
No difference in the use of FFP or plat elet concentrates
were found when comparing hypocoaguable with non-
hypocoaguable patients by conventional coagulation
assays [FFP: 0 (01) vs. 0 (01), P ¼ 0.69; platelet con-
centrates 0 (01) vs. 0 (00), P ¼ 0.78].
Discussion
The main finding of the present study is that a hypocoa-
guable TEG result at admission to the NICU was associ-
ated with worse outcome for patients diagnosed with TBI
and/or intracranial haemorrhage. To our knowledge, the
current study is the first to investigate the potential
prognostic value of hypocoagulability by VHA like
TEG in the neurosurgical setting, but is in alignment
with the large number of reports documenting that coa-
gulopathy is associated with progression of insul t when
computerized tomography scans were repeated [1,3] and
predictive of prolonged hospital stay, multiple organ
failure and in-hospital mortality [9,2].
It could be argued that patients hypocoaguable by TEG
had a higher tendency of haemorrhage progression fol-
lowing admission to the NICU due to diminished haemo-
static competence. This is supported by higher frequency
of patients with decline in GCS during the first 24 h after
admission and higher frequency of cerebral incarcerations
among patients with hypocoaguable TEG results when
compared with patients with nonhypocoaguable TEG
results. Alternatively, the hypocoaguable TEG result
upon admission to NICU is merely a marker of initial
haemorrhage severity with concordant higher mortality,
although in this case, we would expect a lower GCS at
admission in patients with hypocoagulability by TEG
and that the association between mortality and a hypo-
coaguable TEG result would disappear after adjusting for
admission GCS, which it was not.
Interestingly, only two out of eight patients with
hypocoagulability according to TEG had concurrent
The prognostic value of thrombelastography Windeløv et al.3
Table 2 Demographics and outcome by coagulation status
TEG
P
APTT/INR/Platelets
P
Hypocoaguable Nonhypocoaguable Hypocoaguable Nonhypocoaguable
Number of patients 8 (10%) 70 (90%) 16 (21%) 62 (79%)
Age 55 (4765) 55 (4463) 0.92 53 (4472) 55 (4562) 0.95
Male sex 6 (75%) 41 (59%) 0.37 13 (81%) 34 (55%) 0.05
Diagnosis
Epidural haemorrhage 0 (0%) 11 (16%) 4 (18%) 7 (13%)
Subdural haemorrhage 1 (13%) 14 (20%) 7 (32%) 8 (14%)
Subarachnoid haemorrhage 4 (50%) 24 (34%) 6 (27%) 22 (39%)
Intracerebral haemorrhage 1 (13%) 10 (14%) 2 (9%) 9 (16%)
Traumatic brain injury 2 (25%) 11 (16%) 0.67 3 (14%) 10 (18%) 0.38
Glasgow Coma Scale Score (GCS)
GCS at admission to NICU 6 (414) 8 (314) 0.89 7 (613) 9 (315) 0.40
GCS approximately 24 h after admission to NICU 3 (314) 11 (715) 0.14 10 (714) 11 (615) 0.34
Decline in GCS from admission to 24 h after admission 4 (57%) 11 (16%) 0.02 1 (7%) 14 (23%) 0.16
Surgery
Underwent neurosurgery during first 24 h in NICU 5 (63%) 38 (54%) 0.72 12 (75%) 31 (50%) 0.07
Outcome
Length of stay in NICU 4 (213) 8 (412) 0.25 8 (511) 7 (313) 0.28
Deceased due to cerebral incarceration within
30 days of arrival to NICU
4 (50%) 4 (6%) 0.02 0 (0%) 8 (13%) 0.20
Deceased within 30 days of arrival to NICU 5 (63%) 11 (16%) 0.008 2 (13%) 14 (23%) 0.50
Categorical variables stated as absolute numbers with percentage in parenthesis and numerical values as median with interquartile range in parenthesis. APTT, activated
partial thromboplastine time; INR, international normalized ratio; NICU, neurointensive care unit; TEG, thrombelastography.
Table 3 Variables associated with 30-day mortality
Univariable regressions OR (95% CI) x
2
P
Age (per year) 1.0 (1.01.0) 0.06 0.81
GCS upon admission to the NICU (per reduced point) 1.2 (1.01.3) 5.7 0.03
Subarachnoid haemorrhage 2.9 (0.99.0) 3.5 0.06
Hypocoaguable according to INR, APTT and/or platelet count 0.5 (0.12.4) 0.9 0.49
Hypocoaguable according to TEG 8.9 (1.842.9) 7.7 0.006
Multivariable regression of variables with P < 0.1 OR (95% CI) x
2
P
GCS upon admission to the NICU (per reduced point) 1.3 (1.11.5) 9.6 0.006
Subarachnoid haemorrhage 5.3 (1.322.3) 5.6 0.02
Hypocoaguable according to TEG 14.8 (2.2100.1) 8.8 0.006
Odds ratio (OR) with 95% confidence interval (95% CI). APTT, activated partial thromboplastine time; GCS, Glasgow coma scale score; INR, international normalized ratio;
NICU, neurointensive care unit; TEG, thrombelastography.
Page 3
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CE: Madhur; MBC/200832; Total nos of Pages: 4;
MBC 200832
coagulopathy according to INR, APTT and/or platelet
counts. With the association of hypocoagulability by
TEG and worse outcome in mind, the approach to blood
coagulation monitoring of TEG might prove a valuable
addition to the existing coagulation assays in identifying
patients at risk of worse outcome and could, if confirmed
in larger and prospectively gathered material, prompt
for targeted early intervention to ensure haemostatic
competence.
In the current study, patients hypocoaguable by conven-
tional coagulation assays (INR, APTT and platelet count)
did not receive more units of FFP and platelet concen-
trates during stay, did not decline in GCS during the first
24 h after admission to the NICU and hypocoagulability
according to these assays was not associated with
mortality.
The present study has limitations inherent to its retro-
spective nature and we cannot establish a cause and
effect relationship. Furthermore, the study originated
from a single centre and even though intern validity
may be high, external validity may be limited and cut-
off values for TEG should be determined locally. Finally,
the study is of limited size with inherent risk of both
types I and II errors. The current findings compel for a
larger prospective study to clarify the role of TEG in the
neurosurgical setting.
Conclusion
Hypocoagulability by TEG at admission to the NICU
was associated with clinical deterioration and worse out-
come. Low concordance with conventional coagulation
assays indicate that TEG might be valuable in identify-
ing patients with clinically rel evant coagulopathy.
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4 Blood Coagulation and Fibrinolysis 2011, Vol 22 No 00
Page 4
    • "Since this monitoring is able to be performed at bedside and repeatedly, we can observe a state of coagulopathy in real time. These values were associated with the clinical outcome in TBI patients [17,18]. In another report, tranexamic acid was administered as antifibrinolytic therapy for the acute phase of trauma expected to cause massive hemorrhage in adults [19]. "
    [Show abstract] [Hide abstract] ABSTRACT: Careful course observation is necessary for cases of mild to moderate traumatic brain injury even when disturbed consciousness is mild on admission. This is because delayed enlargement of hematoma and progression of cerebral swelling may occur and result in an emergency craniotomy. Here, we investigated coagulopathy and abnormal fibrinolysis as a predictive factor of “deterioration requiring surgery” in mild to moderate traumatic brain injury.Patients and methodsSixty-one patients with mild to moderate (Glasgow Coma Scale (GCS) score 9–15) traumatic brain injury were admitted between June 2009 and October 2010. There were 54 subjects in the study, excluding those treated with oral antiplatelet agents and anticoagulants. Patients were classified into those with deterioration requiring surgery [op(+)] or those without deterioration requiring surgery [op(−)]. This was based on whether surgical treatment was performed for hematoma expansion, and exacerbated consciousness level within 3 days after admission. Age, GCS score on admission and blood test findings (platelet count, PT-INR, APTT, fibrinogen, FDP, and d-dimer) on admission were compared.ResultsThe op(+) and op(−) groups comprised 7 (13.0%) and 47 patients (87.0%), respectively. Platelet counts (24.8 vs 18.5 × 104/μl) were decreased, and PT-INR (1.0 vs 1.2) was higher in the op(+) group. Specially, APTT (28.6 vs 39.1 s), FDP (28.9 vs 112.9 μg/ml), and d-dimer (17.3 vs 69.6 μg/ml) values were significantly higher in the op(+) group.Conclusions Coagulopathy and abnormal fibrinolysis, which are measurable in routine medical practice, is associated with deterioration requiring surgery in mild to moderate traumatic brain injury, indicating that careful course observation is necessary.
    Full-text · Article · Oct 2014 · Clinical Neurology and Neurosurgery
    • " diagnosed at admission in general ICU patients and associated with a higher rate of ventilator treatment, higher rate of renal replacement therapy and higher use of blood products. It was also found to be an independent risk factor associated with a more than 3 times increased risk of death within 30 days in these patients (Johansson et al. 2010). Windeløv et al. (2011) showed that neurosurgical patients with hypocoagulation detected by TEG have a worse prognosis and thus TEG has a predictive value in this group of patients. Another recent human study reported a sensitivity of 95.2% and a specificity of 81% for a novel thromboelastographic score to identify overt DIC resulting in a hypocoagulable state"
    [Show abstract] [Hide abstract] ABSTRACT: Thromboelastography (TEG) is a viscoelastic, whole blood‐based assay that integrates information from both the cellular and soluble components of coagulation, providing a global evaluation of the haemostatic system. This contrasts with the conventional coagulation assays (i.e. platelet count, prothrombin time [PT], activated partial thromboplastin time [aPTT] and fibrinogen concentration [FIB]), which only provide information about one component (e.g. clotting factors in the case of PT and aPTT) of the haemostatic process, requiring the combination of several assays for a complete evaluation of haemostasis. Thromboelastography is an old technology that has been used in human medicine for over 50 years. However, it is relatively new in veterinary medicine and has only been applied to horses in the last 5 years. Clinical applications in human medicine include diagnosis and monitoring of coagulopathies. Currently, extensive research is being carried out to expand the use of TEG in dogs and cats. Therefore, it is expected that the use of this technique will also further expand in horses in the near future. To date, the available studies in the equine species have evaluated TEG in healthy horses, horses with gastrointestinal disease, septic foals, horses with exercise‐induced pulmonary haemorrhage (EIPH) and a filly with Glanzmann's thrombasthenia. The main objective of this review is to introduce the TEG technique to equine clinicians, providing information on how the TEG functions, blood sample collection and processing, variables measured and their interpretations, normal reference values and areas of potential clinical application.
    Full-text · Article · Dec 2012 · Equine Veterinary Education
    • "There have been few studies linking the severity of TBI with platelet function [12, 14]. However, a correlation between a GCS <8 and a reduced viscoelastic strength of the thrombus has recently been described [18, 19]. In addition, there is a weak correlation between platelet dysfunction and death due to TBI in multisystem trauma [20]. "
    Full-text · Article · Sep 2012 · Journal of the American College of Surgeons
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