Literature Review

Dural Venous Sinus Thrombosis in Patients Presenting with Blunt Traumatic Brain
Injuries and Skull Fractures: A Systematic Review and Meta-Analysis
Rakan Bokhari1,2, Eunice You2, Mohamad Bakhaidar1,2, Khalid Bajunaid5, Oliver Lasry2,3, Frederick A. Zeiler6,7,
Judith Marcoux2, Saleh Baeesa1

Key words - BACKGROUND: Dural venous sinus thrombosis (DVST) is an increasingly

- CT venography
- Dural venous sinus thrombosis
- Meta-analysis
- Prevalence
- Skull base fracture
- Traumatic brain injury
Abbreviations and Acronyms
CI: Confidence interval
CTV: Computed tomography venography
DVST: Dural venous sinus thrombosis
ICP: Intracranial pressure
NCCT: Noncontrast computed tomography
PROSPERO: International Prospective Register of
Systematic Reviews
TBI: Traumatic brain injury
From the 1Division of Neurosurgery, Department of Surgery,
Faculty of Medicine, King Abdulaziz University, Jeddah,
Saudi Arabia; Departments of 2Neurology and Neurosurgery
and 3Epidemiology, Biostatistics and Occupational Health,
Montreal Neurological Hospital and Institute, McGill
University, Montreal, Quebec; 4Department of Surgery,
Faculty of Medicine, University of Jeddah, Jeddah, Saudi
Arabia; 5Department of Surgery, Rady Faculty of Health
Sciences, University of Manitoba, Winnipeg, Manitoba,
Canada; and 6Division of Anesthesia, Addenbrooke’s
Hospital, University of Cambridge, Cambridge, United
Kingdom
To whom correspondence should be addressed:
Saleh Baeesa, M.D., F.R.C.S.C.
[E-mail: sbaeesa@kau.edu.sa]
recognized complication of blunt traumatic brain injury (TBI) and skull fractures.
However, data concerning epidemiology and clinical significance of DVST are
unclear. Determining the disease burden in patients with TBI is an important first
step to guide future studies assessing the natural course of traumatic DVST or
the effects of its treatment. Therefore, we performed to our knowledge the first
systematic review and meta-analysis evaluating the prevalence of DVST in
patients with TBI and skull fractures.
- METHODS: MEDLINE and Embase databases were systematically searched
for relevant studies published up to March 2018. All studies that assessed the
prevalence of DVST among patients with TBI who underwent a vascular imaging
study were included. The primary outcome was the presence or absence of
DVST on imaging. A random-effects meta-analysis was used to pool studies.
- RESULTS: Our systematic review yielded 638 articles, and 13 articles met
inclusion criteria. In patients with skull fractures adjacent to a venous sinus, the
prevalence was 26.2% (95% confidence interval [ 19.4%e34.4%). This elevated
risk was similar between adult (pooled estimate 23.8%; 95% CI [ 16.2%e33.5%)
and pediatric (pooled estimate 31.3%; 95% CI [ 19.1%e46.9%) populations.
- CONCLUSIONS: We found an unexpectedly high and consistent frequency of
DVST among patients with skull fractures regardless of age group or severity of
brain injury. These findings are important and highlight the need for further
understanding the natural history of DVST and providing better guidelines on its
management.

Supplementary digital content available online.

Citation: World Neurosurg. (2020) 142:495-505.
https://doi.org/10.1016/j.wneu.2020.06.117
Journal homepage: www.journals.elsevier.com/world-
neurosurgery
Available online: www.sciencedirect.com
1878-8750/$ - see front matter ª 2020 Elsevier Inc. All
rights reserved.
INTRODUCTION
Previously published series report high rates
of dural venous sinus thrombosis (DVST) in
the context of blunt traumatic brain injuries
(TBIs) and skull fractures.1-3 These findings
are in stark contrast to previous knowledge
and represent a poorly described entity in
neurotrauma.4 Because DVST manifests
with a varied clinical spectrum and may be
asymptomatic, it may go unnoticed during
the index hospitalization until subsequent
complications bring it to medical
attention.5,6 Support comes from recent
series where delayed presentation after a
prior TBI constituted a sizable portion of
inpatient cases encountered by thrombosis
specialists.7 Case reports of neglected
traumatic DVST have also implicated DVST
in delayed complications and mortality
after initially surviving the index TBI.5
Institutions have since reported on
surveillance protocols for traumatic DVST
and reported on their experiences, but the
indications for obtaining venous imaging
in these studies were variable.1-3,8-15 Other
controversies include the optimal timing
of venous imaging and whether such a
finding warrants treatment when discov-
ered. We have recently encountered a case
where a patient went on to develop a
traumatic DVST with secondary pulmo-
nary emboli despite being initially cleared
with computed tomography venography
(CTV). The outcome of anticoagulation in
this population at risk for hemorrhagic
complications is also unclear. Therefore,
we performed a systematic review of the
literature to describe what is known about
the prevalence of DVST. We also summa-
rized the patient- and imaging-related
factors that may affect its prevalence.
Another topic of interest was the reported
natural history of this finding.
MATERIALS AND METHODS
The Preferred Reporting Items for Sys-
tematic Reviews and Meta-Analyses
guidelines served as the template for

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RAKAN BOKHARI ET AL.
reporting the review. This review was
registered in the International Prospective
Register of Systematic Reviews (PROS-
PERO) (registration number
CRD42018090349), and the protocol is
available online (https://www.crd.york.ac.
uk/prospero/display_record.php?
RecordID¼90349).
Data Sources and Search Strategy
A search protocol was developed and
refined under the guidance of 2 experi-
enced librarians (Supplemental Table 1).
Two authors (R.B. and E.Y.) screened
results from MEDLINE and Embase
databases from inception to March 2018.
The title, key words, and abstract and/or
body of the text were assessed to
determine if criteria for inclusion were
met. References of included studies were
searched. Conference abstracts retrieved
were also evaluated. We attempted to
contact authors when raw data were not
presented. Unpublished data were not
pursued. The search was most recently
updated in September 2019.
The clinical question was formulated
according to the Population, Intervention,
Comparison, Outcome, and (optional)
Type framework:
 Population: Patients presenting with
TBI and skull fracture in proximity to a
dural sinus
 Intervention: Vascular imaging with
CTV or magnetic resonance venography
 Comparison (if applicable): Patients
with TBI without a skull fracture
 Outcome: Development of DVST
 Type: All study types
Eligibility Criteria
Owing to a known scarcity of randomized
controlled trials on this subject, we
included all study types regardless of
design or language that assessed the
prevalence of traumatic DVST among
patients with TBI presenting to their
institution. More specifically, we included
studies 1) that assessed traumatic DVST in
consecutive patients with TBI, 2) where
patients underwent a vascular imaging
study, and 3) that reported the total
number of patients imaged.
The definition of what constitutes sinus
obstruction can be variable and includes a
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PREVALENCE OF TRAUMATIC SINUS THROMBOSIS
spectrum from narrowing, partial filling
defect, to complete occlusion. It can also
encompass DVSTs caused by extraluminal
compression, such as by epidural hema-
tomas or bone fragments, as well as cases
caused by intraluminal thrombosis. For
the purposes of our study, we included
only cases of complete or partial intra-
luminal thrombosis. We excluded studies
exclusively reporting cases without
mention of the population denominator.
We also excluded studies that contained
nontraumatic DVST (e.g., caused by head
and neck infections) as well as cases of
extraluminal compression, as these
studies have limited applicability to our
research question. Our inclusion criteria
were intentionally left very broad to allow
for creation of subgroups of different age
groups, screening protocols, and meth-
odologic quality.
Outcomes Assessed
The primary outcome that was assessed in
this study was the presence of traumatic
DVST on imaging. In addition to standard
radiologic signs of DVST on noncontrast
computed tomography (NCCT), a specific
radiologic finding we sought to evaluate in
the context of trauma was air bubbles in
proximity to the venous sinuses origi-
nating from the adjacent mastoid air cells
or sinuses or through a penetrating
wound. Certain indirect signs of DVST,
such as hemorrhage and edema, were not
collected, as these are common findings
in the TBI population overall. Further-
more, we also sought to describe the
functional outcomes of these patients as
well as recanalization rates observed in
these studies.
We defined beforehand certain modi-
fiers that may explain observed heteroge-
neity in our analysis. These were patient
age group (<18 years of age vs. >18 years
of age), presence of fracture, presence of
fracture location (skull base vs. convexity),
timing of study (within 24 hours vs. after
24 hours), and whether radiologic (e.g.,
hyperdense sinuses, air bubbles) or
clinical (e.g., headaches, high intracranial
pressure [ICP]) features were taken into
consideration when ordering the
examinations.
Data Extraction and Quality Assessment
For each study, the following information
was collected: surname of the first author,
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LITERATURE REVIEW
year of publication, country where the
study was conducted, study setting
(trauma center vs. community-based),
study design, duration of follow-up (if re-
ported), sample size, mean (or median)
age and age range, proportion of male
participants, diagnostic test for DVST,
operational definition of the general TBI
cohort (what constituted the overall pop-
ulation as well as the high-risk cohort
considered worthwhile for DVST investi-
gation), and prevalence of each compli-
cation reported. Data were extracted using
a predesigned form. We also sought to
assess for clinically significant outcomes,
including rates of resolution and propa-
gation, as well as functional outcomes.
At the end of the extraction process,
R.B. rechecked all the data for accuracy.
Disagreements were resolved through
consensus following a discussion between
the 2 assessors. R.B. and S.B. then inde-
pendently assessed study quality using the
Newcastle-Ottawa Scale System for Cohort
Studies, which judges studies on 3 broad
perspectives: selection of study
groups (0e4 points), comparability of
groups (0e2 points), and ascertainment of
outcome of interest (0e3 points). Any
disagreement was resolved by discussion.
Statistical Analysis
Statistical analysis was performed using
point prevalence with 95% confidence
intervals (CIs). A random-effects model
was used for pooled estimates and 95%
CIs. We reported heterogeneity with the
<I>I</I>2 statistic. Assessment of pub-
lication bias was performed by inspecting
funnel plots. Significance was set at
<I>P</I> < 0.05. The meta-analyses
were carried out with Comprehensive
Meta-Analysis Version 3 (Biostat, Engle-
wood, New Jersey, USA) software.
Sensitivity analyses were conducted for
every outcome by excluding 1 study at a
time. We reported the outcome only in
instances where this resulted in a change
in the significance of the summary effect.
Higgins <I>I</I>2 test for study hetero-
geneity was used. We used the cutoff 25%,
50%, or 75% to classify heterogeneity into
low, moderate, or high heterogeneity.16
RESULTS
Our search strategy resulted in a total of
724 articles, of which 520 were found in

RAKAN BOKHARI ET AL.
Embase and 204 were found in MEDLINE.
De-duplication resulted in 638 studies.
Thirteen studies were retained after
screening of abstracts and application of
inclusion criteria (Figure 1).
Characteristics of Included Studies
All studies were single-center studies and
conducted in hospitals with trauma
expertise. Eight were conducted in the
United States and accounted for approxi-
mately half of all patients in our pooled
analysis (704 of 1422 patients defined as
being at risk). Two studies were conducted
in China, and the remaining studies were
from Israel, Japan, and Switzerland. Of
1422 patients with skull fractures who
were identified as being at risk in their
respective studies and had undergone a
venous imaging study, 704 were from the
United States (Table 1). Risk of bias
according to the Newcastle-Ottawa Scale
is presented in Table 2. Reassuringly,
Records iden fied through
database searching
Iden fica on
(n = 724)
Records a er duplicates removed
(n = 638)
Screening
Records screened
(n = 638 )
Full-text ar cles
assessed for eligibility
(n = 30)
Eligibility
Studies included in
qualita ve synthesis
(n = 13)
Included
Studies included in
quan ta ve synthesis
(meta-analysis) of
primary outcome
(n = 13)
Figure 1. Preferred Reporting Items for Systematic Reviews and Meta-Analyses flowchart of search
strategy.
WORLD NEUROSURGERY 142: 495-505, OCTOBER 2020
PREVALENCE OF TRAUMATIC SINUS THROMBOSIS
most studies had reasonable risk of bias
(score 7/9).
Indications, Timing, and Methods of
Screening
Studies included the whole range of TBI
severity, with mild and moderate TBIs
constituting the majority of included pa-
tients (Table 3). The indication for
imaging in most studies was the
presence of a fracture in the vicinity of a
venous sinus seen on NCCT. Some
studies included clinical findings
suspicious for DVST (e.g., headache,
nausea) or NCCT findings as indications
for obtaining venous imaging.1,14,17 One
study described an unusual protocol of
ICP measurement by serial lumbar
puncture and CTV acquisition when high
ICP was detected.18 All studies used
dedicated venous imaging to assess for
DVST except 1 study in which the venous
system was assessed on computed
Addi onal records iden fied
through other sources
(n = 0)
Records excluded
(n = 608)
Full-text ar cles excluded, with
reasons
(n = 17)
Design not mee ng criteria (n=10)
Wrong primary outcome (n=7)
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LITERATURE REVIEW
tomography angiography performed for
assessment of arterial injury according to
standard criteria. CTV was the most
common modality; however, slice
thickness varied between studies.
The intervals from injury to imaging
were not accurately defined by studies, but
instead were reported as ranges without
subgrouping. All studies obtained imaging
within the first few days. The only excep-
tion was the study by Wang et al.18 that
relied on ICP elevation to obtain venous
imaging and is therefore included in the
sensitivity analysis (Table 1).
DVST Prevalence in Patients Presenting
with Blunt TBI
The overall incidence in all patients
presenting to emergency departments
with TBIs among the studies allowing
for this calculation was 4% (95% CI ¼
1.6%e9.8%; <I>I</I>2 ¼ 22.56%;
<I>P</I>  0.001) (Figure 2A).
However, when looking at the subgroup
of interest, namely, patients with skull
fractures adjacent to a venous sinus,
the prevalence is much higher
and approaches 26.2% (95% CI ¼
19.4%e34.4%; <I>P</I>  0.001). This
elevated risk was similar between adult
(pooled estimate 23.8%; 95%
CI ¼ 16.2%e33.5%; <I>P</I>  0.001)
and pediatric (pooled estimate 31.3%;
95% CI ¼ 19.1%e46.9%; <I>P</I>
 0.02) populations (Figure 2B).
We detected minimal heterogeneity
between studies in either age group
(<I>I</I>2 ¼ 0% among adult and
pediatric subgroups, respectively).
Isolating the few studies that specified
temporal bone involvement yielded the
highest pooled prevalence (pooled
estimate 40.3%; 95% CI ¼ 28.5%e
53.4%; <I>I</I>2 ¼ 10%; <I>P</I>
 0.15) (Figure 2C).
The risk was very low among studies
where it was specified that no extension to
a dural sinus was noted (0 of 19 patients in
the series by Delgado Almandoz et al.1 and
6 of 138 in the series by Li et al.15). No
cases of DVST were reported among
patients with no skull fractures in the 2
studies including 44 such patients.1,3 A
slightly higher pooled prevalence among
adults was found when including the
study by Wang et al.18 that relied on
clinical findings to obtain venous
imaging in patients with skull fractures
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Table 1. Characteristics of Included Studies
Main Total Population Total Type of Final
Age Recruitment Pattern of Fractures Included Total TBI with Venous Cases of Total Partial Extrinsic Imaging Recanalization
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Number Reference Group Period Country in Study Population Imaging tDVST tDVST tDVST Compression Study Rate

1 Adepoju and P 2009e2015 USA Mixed, including skull base (n ¼ 260 258 1 NS NS NS CTA/CTV NS
Adamo, 201710 46) and venous sinuses (n ¼ 6)
2 Benifla et al., P 2-year period Israel Mixed, but adjacent to sinus 434 41 21 15 6 NS CTV NS
201611
3 Delgado A January 1, 2000 USA Mixed, including some without 1075 195 57 31 26 NS CTV 3/5 with ACT vs.
Almandoz eJune 30, fractures but high index of 7/17 without ACT
et al., 20101 2009 suspicion
4 Fujii et al., A 2002e2008 Japan Mixed, but adjacent to sinus 97 97 15 15 0 7 CTV 4/5 without ACT
200912
5 Hersh et al., A 2004e2013 USA NS 541 113 38 NS NS 19 CTV 19/22 resolved by
201613 (A) 6 months
6 Hersh et al., P 2003e2013 USA Mixed, but adjacent to sinus 2224 41 8 5 3 14 CTV, MRV, 4/5 at last
201814 (P) or DSA follow-up
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7 Li et al., 201515 A 2011e2013 China Mixed, including some without 240 240 22 NS NS 18 CTV, MRV, NS
fractures but high index of or DSA
suspicion
8 Rischall et al., A 2006e2013 USA Mixed, but adjacent to sinus 107 107 22* NS NS 41* CTV NS
20169
9 Rivkin et al., A, P 2009e2011 USA Mixed, but adjacent to sinus 908 63 22 9 13 NS CTV in A, NS
20148 MRV in P
10 Slasky et al., A 2004e2014 USA Mixed, but adjacent to sinus 419 210 48 NS NS 78 of 210y CTV NS
20172

PREVALENCE OF TRAUMATIC SINUS THROMBOSIS

11 Stiefel et al., P November 1994 Switzerland Skull base and vault, open and 131 25 8 NS NS NS CTV Residual in 1 of 7
200017 eOctober 1996 closed at last follow-up
12 Wang et al., A 2004e2005 China Mixed, but adjacent to sinus 65 NS 27 NS NS NS CTV/MRV Residual in 5 of 15
201318 at last follow-up
(delayed)
13 Wang et al., A 2006e2010 China Mixed, but adjacent to sinus 338 NS 194 NS NS NS CTV/MRV Residual in 29 of
201318 (early) 75 at last follow-
up
14 Zhao et al., A October USA Basilar skull fractures 22 13 3 3 0 1 CTA then Residual in 1 of 4
20083 eDecember MRA at last follow-up

LITERATURE REVIEW
2006

TBI, traumatic brain injury; tDVST, traumatic dural venous sinus thrombosis; P, pediatric; NS, not specified; CTA, computed tomography angiography; CTV, computed tomography venography; A, adult; ACT, anticoagulant therapy; MRV, magnetic
resonance venography; DSA, digital subtraction angiography; MRA, magnetic resonance angiography.
*Lowest possible.
y>50% compression by epidural hematoma.
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RAKAN BOKHARI ET AL.

Table 2. Newcastle-Ottawa Scale Scores for Included Studies
Selection Outcome

Newcastle- Comparability: Groups Similar for Follow-Up Long Adequacy of

Ottawa Scale Representativeness Sample Ascertainment Additional Factors (Age, Severity, Assessment Enough for Follow-Up of
Number Reference Score of Sample Size of Exposure Nonrespondents Comorbidities) of Outcome Outcomes to Occur Cohorts

1 Adepoju and 7 1 0 1 1 0 1 1 1
Adamo,
201710
2 Benifla et al., 8 1 1 1 1 0 1 1 1
201611
3 Delgado 8 1 1 1 1 0 1 1 1
Almandoz
et al., 20101
4 Fujii et al., 8 1 1 1 1 0 1 1 1
200912
5 Hersh et al., 8 1 1 1 1 0 1 1 1
201613 (adult)
6 Hersh et al., 8 1 1 1 1 0 1 1 1
201814
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(pediatric)
7 Li et al., 8 1 1 1 1 0 1 1 1
201515

PREVALENCE OF TRAUMATIC SINUS THROMBOSIS

8 Rischall et al., 8 1 1 1 1 0 1 1 1
20169
9 Rivkin et al., 8 1 1 1 1 0 1 1 1
20148
10 Slasky et al., 8 1 1 1 1 0 1 1 1
20172
12 Stiefel et al., 8 1 1 1 1 0 1 1 1
200017
13 Wang et al., 6 0 0 1 1 0 1 1 1
201318 (early)

LITERATURE REVIEW
14 Wang et al., 7 1 0 1 1 0 1 1 1
201318 (late)
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RAKAN BOKHARI ET AL. PREVALENCE OF TRAUMATIC SINUS THROMBOSIS

Table 3. Distribution of Traumatic Brain Injuries in Included Studies

Timing of TBI Severity GCS 13e15 GCS 9e12 GCS 3e8
Number Reference Study Type Imaging Definition of TBI (mean  SD) (%) (%) (%)

1 Adepoju and Retrospective NS TBI with skull fracture NS 81.4 7.8 10.8
Adamo, chart review
201710
2 Benifla et al., Retrospective In ED TBI with skull fracture NS 46 27 27
201611 chart review
3 Delgado Retrospective Within 24 Blunt trauma patients who NS NS NS NS
Almandoz chart review hours underwent imaging due to
et al., 20101 fracture or suspicion of high
ICP
4 Fujii et al., Prospective Within 72 Consecutive patients with GCS in NS NS NS
200912 study hours skull fractures thrombosis: 8 
5; GCS in
nonthrombosis:
10  4
5 Hersh et al., Retrospective NS Adult patients with 1 skull NS NS NS NS
201613 (adult) chart review fractures in the setting of
blunt trauma
6 Hersh et al., Retrospective NS Pediatric blunt trauma patients NS 56 22 22
201814 chart review who underwent neurovascular
(pediatric) imaging with CTV/MRV/DSA
7 Li et al., Retrospective Mean 3.9 Closed TBI manifesting within NS NS NS NS
201515 chart review days (range¼ 72 hours, no history of DVT/PE
6 hours e 7
days)
8 Rischall et al., Retrospective Within 48 Acute blunt trauma and skull NS NS NS NS
20169 chart review hours fracture overlying a dural
venous sinus on unenhanced
initial screening
9 Rivkin et al., Retrospective Within 48 Skull fractures involving sinus NS NS NS NS
20148 chart review hours with venography
10 Slasky et al., Retrospective NS Adult patients with 1 skull 11.7  4.5 65 9 26
20172 chart review fractures in the setting of
blunt trauma
11 Stiefel et al., Retrospective NS Pediatric patients with head NS NS NS NS
200017 chart review trauma and skull fracture
12 Wang et al., Prospective Upon clinical Adult patients with head 13.0  1.7 NS NS NS
201318 study signs of high trauma and skull fracture
(delayed) ICP crossing a sinus
13 Wang et al., Prospective Upon high ICP Adult patients with head 12.5  2.3 NS NS NS
2013 (early)18 study on routine LP trauma and skull fracture
crossing a sinus
14 Zhao et al., Prospective NS Vascular imaging done based NS 20 20 60
20083 study on Biffl criteria

TBI, traumatic brain injury; GCS, Glasgow Coma Scale; NS, nonspecified; ED, emergency department; ICP, intracranial pressure; CTV, computed tomography venography; MRV, magnetic
resonance venography; DSA, digital subtraction angiography; DVT, deep vein thrombosis; PE, pulmonary embolism; LP, lumbar puncture.

(pooled estimate 28.6%; 95% Radiologic Signs shown to have an adjacent skull fracture.
CI ¼ 18.4%e41.7%; <I>I</I>2 ¼ 0%; Only 2 studies assessed the added value of In the study by Benifla et al.,11 air bubbles
<I>P</I>  0.01) (Figure 2D). detecting air bubbles in patients already were found in similar frequency among

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 LITERATURE REVIEW
RAKAN BOKHARI ET AL. PREVALENCE OF TRAUMATIC SINUS THROMBOSIS

Figure 2. Pooled prevalence of dural venous sinus thrombosis adjacent to the venous sinus. (C) Prevalence of DVST involving
(DVST) in patients with blunt traumatic brain injury and skull the temporal bone. (D) Prevalence of DVST in fractures adjacent
fractures. (A) Overall prevalence of DVST in patients with to the venous sinus including data of Wang et al.18 TBI,
traumatic brain injury. (B) Prevalence of DVST in fractures traumatic brain injury; CI, confidence interval. (Continues)

patients with and patients without sinus
thrombosis. The study by Zhao et al.3
found adjacent air in 2 of 3 patients with
sinus thrombosis and 1 of 2 patients with
extraluminal compression (Supplemental
Table 2).
Rates of Recanalization recanalization were available for only a
Overall, no study designated recanaliza- minority of patients (Table 1). The
tion rates as their primary outcome, and majority of patients were not
significant loss to follow-up was anticoagulated given the understandable
frequently observed. Among the 6 studies hesitancy of the treating surgeons. With
reporting follow-up imaging, rates of regard to timeline of spontaneous

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 LITERATURE REVIEW
RAKAN BOKHARI ET AL. PREVALENCE OF TRAUMATIC SINUS THROMBOSIS

Figure 2. (Continued).

recanalization, it was observed up until 6
months postinjury.14
Delayed Morbidities Reported After TBI
Attributed to Traumatic DVST
The effect on outcomes attributed to DVST
was inconsistent between studies and is
confounded by the extent of the associated
cranial and extracranial injuries. As such,
we did not pool these outcomes, as they
do not allow for isolation of the effect of
traumatic DVST on the clinical course in
these patients.
DISCUSSION
This meta-analysis is the first to our
knowledge to study and pool the incidence
of traumatic DVST in the context of neu-
rotrauma. The main finding of our study
was the demonstration of an unexpectedly
high and consistent frequency of trau-
matic DVST among patients with skull
fractures regardless of age group or
severity of brain injury. We showed that
about 1 in 4 patients with a skull fracture
will be found to have a traumatic DVST.
This finding produces several questions
that need to be addressed, as the literature
provides little guidance on this seemingly
benign finding.
The occurrence of traumatic DVST in
the context of a skull fracture adjacent to a
sinus is biologically plausible. These in-
juries satisfy all 3 components of Virchow

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RAKAN BOKHARI ET AL.
triad for venous thrombosis19: injury of the
endothelial lining with exposure of
thrombogenic subendothelial tissue;
increased coagulability in the context of
TBI20 and at times polytrauma; and
sluggish flow by compressing skull
fragments, epidural hematomas, or
applied cervical collars. This provides a
rationale for the observed remarkably
high prevalence of traumatic DVST in
these patients and across studies,
especially patients with petrous temporal
bone fractures; as these tend to imply
the transmission of significant kinetic
energy to the skull base.1-3,14
However, as one would expect from the
pathophysiology of disease, the occur-
rence of traumatic DVST is not instanta-
neous. The radiologic screening protocol
should therefore address not only who
should be scanned but also when. Our
initial protocol was to clear the dural si-
nuses with CTV acquired as expeditiously
and as safely possible. This may be done
immediately on presentation or after
emergent surgery, which is similar to
practice patterns reported by others
(Table 3). In cases where imaging
demonstrated no sinus thrombosis, we
would then consider the patient cleared
without further follow-up surveillance.
This procedure was re-evaluated after
encountering the case of missed traumatic
DVST with pulmonary emboli after
initial clearance that we described
earlier. Although the possibility of missing
lesions with early screening was alluded
to by previous authors,1,9,18 no
recommendations to overcome this
limitation were made. Our experience
lends further support to the concern that
very early imaging risks missing future
asymptomatic DVST, which is not
inconsequential.5,7
In attempting to define patients with
the highest risk and highest yield for
screening, we find rates of traumatic DVST
to be similar between adults and children.
However, fractures involving the skull base
or petrous temporal bones were associated
with the highest rates of traumatic DVST
of approximately 40% (Figure 2D),
probably a result of higher forces
necessary to generate those fractures or
due to the close proximity of several
dural venous sinuses, which therefore
increase the likelihood of being crossed
by a fracture. We theorize that the more
WORLD NEUROSURGERY 142: 495-505, OCTOBER 2020
PREVALENCE OF TRAUMATIC SINUS THROMBOSIS
forceful nature of the inciting injury in
these patients leads to more severe
traumatic brain injuries, an independent
cause for hypercoagulability.21,22
We did not find sufficient evidence to
guide the optimal timing to screen pa-
tients with TBI, as timing of venous im-
aging in series was vague with no
individual patient data available. We did,
however, find support for the notion that
the sensitivity of imaging increases with
time, which is true even beyond 30 days
from the insult.9 Our current protocol is to
image patients at risk for DVST at an
interval of 5e7 days, as it is unlikely that
therapeutic anticoagulation will be
administered earlier in the asymptomatic
or mildly symptomatic trauma patient,
and the reviewed literature provides
some evidence that the yield increases
with time. Significant clinical
manifestations compatible with traumatic
DVST, such as malignant brain edema
and uncontrolled ICP, would necessitate
earlier imaging. Obtaining mixed-phase
computed tomography arteriography/CTV
in a delayed fashion at 7 days also allows
for follow-up of any incidental arterial in-
juries noted on presentation.23 Delayed
imaging has the added utility of
documenting contusion stability before
therapeutic anticoagulation,24 which is
unlikely to be started in the first few
days when risk of hemorrhage is
highest.25 We found no NCCT imaging
findings to be superior to the finding of
a fracture, especially one adjacent to a
venous sinus. We thought air bubbles
would be an appealing adjunct for a
missed temporal bone fracture given the
proximity of air cells in the region, but
no studies lend support to this notion.
The interest in this finding may
progressively diminish with
improvements in CT resolution causing a
decrease in the numbers of missed
fractures, and its utility away from air
cells is limited.
Specific attention should be given to
avoid mimickers of sinus thrombosis, as
they may result in unnecessary anti-
coagulation in the context of normal vari-
ants of hypoplasia or prominent arachnoid
granulations. Distinguishing true throm-
bosis from sinus occlusion caused by a
compressing extradural hematoma can be
very difficult and with significant risks in
the event of misdiagnosis.26 Special care
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LITERATURE REVIEW
should be exercised when considering
this diagnosis in the presence of an
adjacent epidural hematoma, and repeat
imaging after diminution of the epidural
bleed may be warranted to confirm the
diagnosis before treatment initiation.
Whether investigating for thrombo-
philia in patients with traumatic DVST is
warranted remains to be determined. We
were unable to identify any studies in our
review investigating the association be-
tween thrombophilia and DVST, but it is
biologically plausible, and further research
may be needed given the limited evalua-
tion of this risk factor.27 Furthermore, no
study collected information on
antiplatelet or anticoagulant use and
international normalized ratio values
among included patients, so no
comment can be made on the protective
effect or on the role of reversal in DVST
development.
Optimal management of an otherwise
fit-for-discharge patient with mild TBI and
a skull fracture traversing a sinus is also
unclear, as traumatic DVST is not exclu-
sive to severe injuries. Given reports of
morbidity and mortality following
discharge of such patients,5,7 discharge
after initial CTV/magnetic resonance
venography with appropriate counseling
along with delayed follow-up imaging ap-
pears justified. Good quality evidence is
sorely needed, as these imaging studies
are costly and not without risk. They are
also, in the case of an asymptomatic
patient, detecting a finding of unclear
clinical significance, unknown natural
history, and without available guidelines
on management. We believe that
thrombus propagation, embolization, or
lack of recanalization at 4e6 weeks would
constitute an appropriate indication for
anticoagulant therapy until further evi-
dence is provided by appropriately
designed prospective observational and
interventional studies.
The need for treating a symptomatic
DVST, even in the presence of secondary
hematomas, is well established and is the
current recommendation of the American
Heart Association, American Stroke Asso-
ciation, and European Federation of
Neurological Societies.28,29 Treatment
prevents clot propagation and possible
embolization, alleviates symptoms, helps
control secondary elevated ICP, and
decreases the chance of venous
503

RAKAN BOKHARI ET AL.
infarctions.30-32 Traumatic DVSTs are
different in that the associated hematomas
are potentially unrelated to the venous
lesions, but rather a result of the cranial
trauma and are at risk of expansion even
with prophylactic doses of anticoagulants.
Whether asymptomatic traumatic DVST
merits treatment remains to be deter-
mined. On one hand, a patient of ours and
other reports provide evidence suggesting
that treatment is worthwhile to avoid
embolic complications and delayed
complications, such as venous hyperten-
sion and secondary arteriovenous fis-
tulas.5-7,33 On the other hand, series have
reported spontaneous recanalization in
the majority (>80%) of these clots
(Table 1), which approximates the
recanalization rates of spontaneous DVST
with anticoagulation.7,31 In addition,
anticoagulation therapy is not benign in
the setting of a polytrauma patient with
increased risk for cerebral and extracranial
hemorrhage.
Decision making and informed consent
for treatment necessitate a thorough un-
derstanding of the natural history, which
remains enigmatic and unaddressed in the
literature. One can make the argument
that an 80% resolution rate in a pathology
with such a high incidence may still result
in a significant absolute residual number
of DVSTs in the population, as skull
fractures are not uncommon. We are
therefore in dire need of studies that allow
a proper risk-benefit analysis and a better
understanding of the natural history of
DVST, which remains unclear.16
Limitations
Several points in our meta-analysis need to
be addressed. First, the major limitation
regarding the conclusion of this article is
that we summarize the frequency of an
entity that is of undetermined clinical
significance. The natural history of trau-
matic DVST remains unclear, with reports
citing it as a self-limiting phenomenon
with some reporting spontaneous recana-
lization rates of 80%, which approximate
the recanalization rates of DVST with
anticoagulation.31 This may be due to a
natural history that differs from that of
spontaneous DVST or due to confusion
with sinus compression from focal
epidural hematomas that may mimic the
appearance of sinus thrombosis.26 We
believe this lack of consensus on its
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PREVALENCE OF TRAUMATIC SINUS THROMBOSIS
significance as well as the description of
a consistently high incidence are major
strengths in our paper, as this implies
feasibility of patient recruitment for
prospective observational or even
interventional studies. The high
incidence rate also explains why this
predominately benign phenomenon can
still be a significant concern.
Second, many studies did not provide
the exact interval from presentation to
diagnosis. This prevents conclusions from
being made in this study for one particular
interval over another. This should be
addressed in future studies.
Third, head injury can lead to sinus
thrombosis via other mechanisms, such as
cerebrospinal fluid leak and subsequent
meningitis.34,35 We excluded studies that
included sepsis as the cause for DVST,
but studies reliant on radiologic data
may have erroneously included them.
However, most series selected patients
sufficiently early that this concern is not
major.
Fourth, we are limited by our reliance
on retrospective institutional small series
to offer a conclusion on the necessity, or
lack thereof, for anticoagulation in this
setting. Whether the risk-benefit balance
tilts toward observation or anticoagulation
needs to be answered by prospective
studies, which to the best of our
knowledge are unavailable.
Fifth, publication bias is a potential
concern; however, this topic is of suffi-
cient interest that this should not be of
major concern. Our analysis demonstrates
lack of evidence that further publication
may change the conclusion of this article
(Supplemental Figure 1). Selection bias is
also an issue, as the sickest patients with
multiorgan failure may be deemed too
sick to receive intravenous contrast or
may ultimately die before imaging
acquisition. Very severely injured patients
can also die before study acquisition, but
this should cause a prevalence lower
than if these were included.
CONCLUSIONS
Further understanding of asymptomatic
sinus thrombosis in the setting of TBI is
warranted. Our study is important because
it is the first to examine and pool the
incidence of DVST in the context of
neurotrauma. The pooled incidence in this
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2020.06.117
LITERATURE REVIEW
meta-analysis was found to be consistently
high across studies, regardless of age
groups, yet little is known about the
natural history of traumatic DVST.
Although it has been linked to serious
delayed complications, no clear imaging-
or patient-related factors have been eluci-
dated, and better understanding of who is
at risk for thrombus propagation and
complication occurrence is warranted.
Furthermore, we believe that the first step
in the proper description of the natural
history of this disease is designing a
protocol that would result in the best
acquisition rates. Given the lack of sup-
port in the literature, we propose
screening with CTV in hospitalized trauma
patients at 3e5 days, which is the earliest
we would feel comfortable initiating ther-
apeutic anticoagulation in this patient
population for an asymptomatic finding. A
repeat delayed imaging study during
subsequent follow up may be the most
suitable study for patients with mild TBI
who can be discharged after a short period
of observation. While the value of this
finding remains to be determined, and
well-conducted prospective studies
continue to be needed, these findings
provide a good basis for future studies and
allow for appropriate sample size
calculations.
ACKNOWLEDGMENTS
We thank McGill University Health Centre
librarians Tara Landry and Alex Amar for
their assistance in helping us with devel-
oping and refining our search strategy.
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Conflict of interest statement: The authors declare that the
article content was composed in the absence of any
commercial or financial relationships that could be construed
as a potential conflict of interest.
Received 29 February 2020; accepted 16 June 2020
Citation: World Neurosurg. (2020) 142:495-505.
https://doi.org/10.1016/j.wneu.2020.06.117
Journal homepage: www.journals.elsevier.com/world-
neurosurgery
Available online: www.sciencedirect.com
1878-8750/$ - see front matter ª 2020 Elsevier Inc. All
rights reserved.
505
 LITERATURE REVIEW
RAKAN BOKHARI ET AL. PREVALENCE OF TRAUMATIC SINUS THROMBOSIS

SUPPLEMENTARY DATA

Supplemental Table 1. Search strategies

On the topic of Dural venous sinus thrombosis in patients with TBI or skull fracture
On 3/13/2018

Ovid MEDLINE and Epub Ahead of Print, In-Process and Other Non-Indexed Citations, Ovid
MEDLINE Daily (1946 to Present)

# Searches Results
1 Brain Injuries/ 49,904
2 Brain Injuries, Traumatic/ 2125
3 Brain Concussion/ 6487
4 Brain Contusion/ 29
5 exp *Brain/in 3000
6 Head Injuries, Closed/ 2921
7 (tbi or mtbi).tw,kf. 21,320
8 (trauma* adj2 (brain or head) adj2 injur*).tw,kf. 31,084
9 concuss*.tw,kf. 7233
10 exp Skull Fractures/ 20,614
11 ((skull* or calvaria*) adj2 fractur*).tw,kf. 3486
12 neurotrauma*.tw,kf. 1651
13 Craniocerebral Trauma/ 21,124
14 1 or 2 or 3 or 4 or 5 or 6 or 7 or 8 or 9 or 10 or 11 or 12 or 13 112,997
15 sinus.hw. and Thrombosis/ 323
16 exp Sinus Thrombosis, Intracranial/ 3344
17 dural* ve* sinus*.tw,kf. 413
18 cerebr* ve* sinus*.tw,kf. 912
19 sinus* thromb*.tw,kf. 3796
20 15 or 16 or 17 or 19 5426
21 14 and 20 174
22 Phlebography/ 12,220
23 ((comput* tomograph* or magnet* resonan*) adj2 (phlebograph* or venograph*)).tw,kf. 933
24 22 or 23 12,823
25 14 and 24 50
26 21 or 25 205
27 remove duplicates from 26 204
28 from 27 keep 1e204 204

Embase 1974 to 2018 March 12

# Searches Results
1 exp brain injury/ 158,272
2 (tbi or mtbi).tw,kw. 35,199
3 (trauma* adj2 (brain or head) adj2 injur*).tw,kw. 45,888
4 concuss*.tw,kw. 9407

Continues

505.E1 www.SCIENCEDIRECT.com WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2020.06.117

 LITERATURE REVIEW
RAKAN BOKHARI ET AL. PREVALENCE OF TRAUMATIC SINUS THROMBOSIS

Supplemental Table 1. Continued

Embase 1974 to 2018 March 12
5 exp skull fracture/ 23,881
6 ((skull* or calvaria*) adj2 fractur*).tw,kw. 4206
7 (cranio?cerebr* trauma* or neurotrauma*).tw,kw. 4578
8 1 or 2 or 3 or 4 or 5 or 6 or 7 197,522
9 exp cerebral sinus thrombosis/ 7398
10 dural* ve* sinus*.tw,kw. 537
11 sinus* thromb*.tw,kw. 5334
12 9 or 10 or 11 9233
13 phlebography/or magnetic resonance venography/ 17,346
14 ((comput* tomograph* or magnet* resonan*) adj2 (venograph* or phlebograph*)).tw,kw. 1272
15 13 or 14 17,630
16 8 and 12 406
17 8 and 15 175
18 16 or 17 524
19 remove duplicates from 18 520
20 (“13152568” or “13240151” or “14084295” or “14167088” or “14192735” or “14199710” or 186
“14243489” or “5922427” or “5958240” or “5633799” or “5612537” or “5699612” or “5674803”
or “5478767” or “5552040” or “5090948” or “22046652” or “5133588” or “5569399” or
“5136335” or “5058725” or “4662417” or “4120705” or “5027895” or “5030509” or “5083089”
or “4662418” or “4344711” or “4662415” or “4585606” or “4422865” or “4529151” or
“1205403” or “1078303” or “590222” or “882905” or “283925” or “723388” or “360435” or
“749992” or “732920” or “461795” or “7351570” or “6752736” or “7167369” or “7067596” or
“6860864” or “6142618” or “6828227” or “6888641” or “6394995” or “3892357” or “3002108”
or “3903542” or “3484839” or “3484556” or “3580156” or “3059214” or “2735572” or
“2621681” or “2817667” or “2234228” or “1893320” or “1744302” or “1796733” or “2043915”
or “1822590” or “1995822” or “1436410” or “1523298” or “8440287” or “8465369” or
“8413812” or “8474644” or “8154543” or “8745787” or “8873095” or “8907010” or “8684142”
or “8851086” or “9324517” or “9146838” or “9716187” or “9537663” or “9672457” or
“9588564” or “9647307” or “24525817” or “10201757” or “10098226” or “10836118” or
“11086800” or “10927903” or “10770246” or “11326560” or “12172938” or “12435960” or
“11933750” or “12356221” or “14743123” or “12576036” or “12701266” or “12488376” or
“12748104” or “15628581” or “15007604” or “14605837” or “15286895” or “14975431” or
“15069261” or “15519881” or “15232248” or “14749592” or “15330829” or “15176564” or
“15462367” or “15262747” or “15168052” or “15920426” or “16195674” or “16133767” or
“16382251” or “16808219” or “16494173” or “16703896” or “17621510” or “17880557” or
“18053865” or “18955626” or “18382983” or “17822873” or “18603838” or “18260793” or
“19326975” or “19359906” or “18787197” or “19636678” or “19509620” or “19084283” or
“19343268” or “19882841” or “19632499” or “19468680” or “20169891” or “20139533” or
“20720085” or “20209407” or “20413766” or “20593983” or “20065786” or “20127265” or
“21416310” or “21389895” or “21397144” or “21633606” or “21986442” or “22551588” or
“23008364” or “23904040” or “23748465” or “23921849” or “23588984” or “23522289” or
“23644533” or “23307334” or “24728440” or “23708934” or “24285968” or “23403479” or
“22381814” or “25267989” or “24589805” or “27169046” or “24573982” or “25111001” or
“26150078” or “25274619” or “27169076” or “25893912” or “26092532” or “26136327” or
“25675020” or “27150321” or “27153380” or “26653366” or “27840921” or “27907955” or
“27399454” or “27440521” or “27165903” or “26358702” or “27902676” or “29027868” or
“28732458” or “28576515” or “28495232” or “28458953” or “27942920” or “28623115” or
“28448419” or “28780405” or “29350373” or “29243974” or “29363350”).pm.
21 19 not 20 434

TBI, traumatic brain injury.

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 LITERATURE REVIEW
RAKAN BOKHARI ET AL. PREVALENCE OF TRAUMATIC SINUS THROMBOSIS

Supplemental Table 2. Noncontrast Computed Tomography Findings in Included

Studies
Radiologic Findings

Air Bubbles in Vicinity of

Sinus with versus without
Number Reference Hyperdense Sinus Sinus Thrombosis

1 Adepoju and Adamo, 201710 NA NA

11
2 Benifla et al., 2016 8/21 vs. 1/20 6/21 vs. 9/20
3 Delgado Almandoz et al., 20101 NA NA
12
4 Fujii et al., 2009 NA NA
5 Hersh et al., 201613 (adult) NA NA
6 Hersh et al., 201814 (pediatric) 1/7 (worrisome NCCT findings) NA
vs. 6/24
(based on fracture location)
7 Li et al., 201515 NA NA
8 Rischall et al., 20169 NA NA
36
9 Rivkin et al., 2014 NA NA
10 Slasky et al., 20172 NA NA
17
11 Stiefel et al., 2000 4/8 in DVST vs. 0 in remainder NA
18
12 Wang et al., 2013 (early) NA NA
13 Wang et al., 201318 (late) NA NA
3
14 Zhao et al., 2008 NA 2/4 vs. 1/2

We included only the findings of hyperdense sinus sign and air bubbles in the vicinity of the dural sinus, as all other
radiologic signs, such as hemorrhage and white matter hypodensity, are confounded by the associated brain trauma. We
compared the rate of air bubbles in patients with and without sinus thrombosis.
NA, Not available; NCCT, Noncontrast computed tomography; DVST, dural venous sinus thrombosis.

Funnel Plot of Standard Error by Logit event rate

0.0

0.5
Standard Error

1.0

1.5

2.0

-3 -2 -1 0 1 2 3

Logit event rate

Supplemental Figure 1. Funnel plot.

505.E3 www.SCIENCEDIRECT.com WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2020.06.117