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CLINICAL ARTICLE

Factors influencing the presence of hemiparesis in chronic


subdural hematoma
Rouzbeh Motiei-Langroudi, MD,1,2 Ron L. Alterman, MD,1 Martina Stippler, MD,1
Kevin Phan, MD, BSc, MSc, MPhil,3 Abdulrahman Y. Alturki, MBBS, MSC, FRCSC,1,4
Efstathios Papavassiliou, MD,1 Ekkehard M. Kasper, MD, PhD,5 Jeffrey Arle, MD, PhD,1
Christopher S. Ogilvy, MD,1 and Ajith J. Thomas, MD1
1
Neurosurgical Service, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts; 2Department
of Neurological Surgery, Ohio State University Wexner Medical Center, Columbus, Ohio; 3University of Sydney Westmead
Clinical School, Westmead, New South Wales, Australia; 4Department of Neurosurgery, The National Neuroscience Institute,
King Fahad Medical City, Riyadh, Saudi Arabia; and 5Division of Neurosurgery, Hamilton General Hospital, McMaster University
and Hamilton Health Sciences, Hamilton, Ontario, Canada

OBJECTIVE  Chronic subdural hematoma (CSDH) has a variety of clinical presentations, including hemiparesis. Hemi-
paresis is of the utmost importance because it is one of the major indications for surgical intervention and influences
outcome. In the current study, the authors intended to identify factors influencing the presence of hemiparesis in CSDH
patients and to determine the threshold value of hematoma thickness and midline shift for development of hemiparesis.
METHODS  The authors retrospectively reviewed 325 patients (266 with unilateral and 59 with bilateral hematomas) with
CSDH who underwent surgical evacuation, regardless of presence or absence of hemiparesis.
RESULTS  In univariate analysis, hematoma loculation, age, hematoma maximal thickness, and midline shift were sig-
nificantly associated with hemiparesis. Moreover, patients with unilateral hematomas had a higher rate of hemiparesis
than patients with bilateral hematomas. Sex, trauma history, anticoagulant and antiplatelet drug use, presence of co-
morbidities, Glasgow Coma Scale score, hematoma density characteristics on CT scan, and hematoma signal intensity
on T1- and T2-weighted MRI were not associated with hemiparesis. In multivariate analysis, the presence of loculation
and hematoma laterality (unilateral vs bilateral) influenced hemiparesis. For unilateral hematomas, maximal hematoma
thickness of 19.8 mm and midline shift of 6.4 mm were associated with a 50% probability of hemiparesis. For bilateral
hematomas, 29.0 mm of maximal hematoma thickness and 6.8 mm of shift were associated with a 50% probability of
hemiparesis.
CONCLUSIONS  Presence of loculations, unilateral hematomas, older patient age, hematoma maximal thickness, and
midline shift were associated with a higher rate of hemiparesis in CSDH patients. Moreover, 19.8 mm of hematoma
thickness and 6.4 mm of midline shift were associated with a 50% probability of hemiparesis in patients with unilateral
hematomas.
https://thejns.org/doi/abs/10.3171/2018.8.JNS18579
KEYWORDS  chronic subdural hematoma; neurologic deficit; hemiparesis; traumatic brain injury

C
hronic subdural hematoma (CSDH), a common it is one of the major indications for surgical intervention
form of intracranial hemorrhage, has a variety of and is a predictor of outcome after surgery.1,3,7,9 Therefore,
clinical presentations, including headache, deterio- defining causative factors for hemiparesis may guide treat-
ration in consciousness, and neurological deficit.3 Among ment decisions and help surgeons to avoid unnecessary
these, hemiparesis is one of the most important because conservative management in CSDH patients.

ABBREVIATIONS  CSDH = chronic subdural hematoma; GCS = Glasgow Coma Scale; MLS = midline shift; MRC = Medical Research Council Manual Muscle Testing
scale.
SUBMITTED  March 10, 2018.  ACCEPTED  August 28, 2018.
INCLUDE WHEN CITING  Published online January 11, 2019; DOI: 10.3171/2018.8.JNS18579.

©AANS 2019, except where prohibited by US copyright law J Neurosurg  January 11, 2019 1
Motiei-Langroudi et al.

Although hemiparesis is frequently seen in patients ies. The presence of membranes was further confirmed by
with CSDH and is a major determining factor for surgi- intraoperative findings. Muscle force grading was done
cal intervention and also outcome, there are still many based on the Medical Research Council Manual Muscle
aspects that are not well studied. For instance, large he- Testing scale (MRC).5 Multivariate logistic regression
matomas may be seen in patients who are neurologically analysis was performed only with variables that yielded
intact, while other patients develop deficits with smaller a p value < 0.1 in uni- and bivariate analyses. Moreover,
hematomas. Few studies have examined the clinical and probit analysis was used to determine a threshold for the
radiographic factors associated with hemiparesis in pa- development of hemiparesis based on hematoma thickness
tients with CSDH. Midline shift (MLS), observed on and MLS. Statistical analysis was performed using PASW
non–contrast-enhanced CT, 3,7,9 and decreased cerebral Statistics 18 (Predictive Analytics Software, SPSS, Inc.).
blood flow, measured with xenon CT, 2 have been sug- Statistical significance was defined as having a p value <
gested as causative factors for hemiparesis; however, 0.05.
there are as yet no definitive correlative metrics for these
factors. Despite investigative efforts to date, strong data Results
and consensus are lacking to support cutoff measure-
ment values for hematoma thickness and/or volume, Patient and Treatment Demographics
MLS magnitude, or other demographic and radiological During the study period, 325 patients (mean age 71.6
factors related to the development of hemiparesis in pa- years, range 28–98 years, M/F ratio 2.3) with CSDH who
tients with CSDH. underwent surgery were reviewed. Unilateral hematoma
Because the presence of hemiparesis in a patient pre- evacuations were performed in 266 patients and bilateral
senting with CSDH is important for decision-making evacuations in 59.
regarding conservative versus surgical treatment, we per-
formed the current study to assess if any demographic or Univariate and Bivariate Analyses of Factors Influencing
imaging data were related to the presence of hemiparesis. Hemiparesis
We employed a large database of CSDH patients treated at One hundred fifty-six patients (48%) had hemiparesis
a single large academic institution over a 10-year period to before surgery (MRC grade range 3/5 to 4/5). We first
identify those factors associated with preoperative hemi- evaluated the association of various individual clinical
paresis. We also studied the factors, if any, that influenced variables with the presence of hemiparesis. Univariate
resolution of hemiparesis after surgery. analysis showed that hematoma loculation, older patient
age, hematoma maximal thickness, and MLS were sig-
Methods nificantly associated with hemiparesis. Moreover, patients
Inclusion of Patients with unilateral hematomas exhibited a higher incidence of
hemiparesis than patients with bilateral hematomas. Sex,
Information regarding the patients included in this
study was obtained from an institutional database of con- trauma history, anticoagulant and antiplatelet drug use
secutive patients with a diagnosis of CSDH who were (including aspirin, clopidogrel, warfarin, and ticagrelor),
treated surgically between 2006 and 2016 at Beth Israel presence of comorbidities, GCS score, hematoma density
Deaconess Medical Center (Boston, MA), which is an aca- on CT (either hypodense, isodense, or mixed hyper- and
demic level I trauma tertiary care center. Patients were in- hypodense), and hematoma signal intensity on T1- or T2-
cluded regardless of their neurologic deficit/paresis status. weighted MRI were not correlated with hemiparesis (Ta-
Patients only receiving conservative management were ble 1). Maximal hematoma thickness was correlated with
not included the database and study. MLS in unilateral (r = 0.14, p = 0.02) and bilateral (r =
IRB approval was obtained for this study. 0.28, p = 0.04) hematomas.

Included Variables Multivariate Analysis of Factors Influencing Hemiparesis


The following preoperative data were recorded: sex, Multivariate analysis showed that the presence of locu-
age, history of trauma, comorbidities, anticoagulant use lation and hematoma laterality (unilateral vs bilateral)
and type, presenting Glasgow Coma Scale (GCS) score, were associated with hemiparesis (Table 2).
hematoma characteristics on imaging (laterality [bi- vs
unilateral], side, hematoma density on CT, hematoma Analysis of the Probability of Hemiparesis Based on MLS
signal intensity on MRI, maximal thickness, presence and Hematoma Maximal Thickness
of membranes and loculations, and degree of MLS), and We performed a probit analysis to examine the prob-
presence of neurological deficits (hemiparesis). ability of hemiparesis based on maximal hematoma thick-
Univariate (independent t-test), bivariate (chi-square ness and MLS. For unilateral hematomas, maximal hema-
test), and multivariate (multiple logistic regression) analy- toma thicknesses ≥ 19.8 mm and MLS ≥ 6.4 mm were as-
ses were performed to determine which, if any, of the stud- sociated with a 50% probability of hemiparesis (p < 0.001
ied factors were associated with an increased incidence and p < 0.09, respectively). For bilateral hematomas, the
of hemiparesis. Presence of both loculations (septations larger hematoma was analyzed. In patients with bilateral
which make the hematoma appear as compartmentalized) CSDH a 50% probability of hemiparesis was associated
and membranes (thin adhesions seen as a membrane with- with a maximal hematoma thickness ≥ 29.0 mm and MLS
in the hematoma) was diagnosed by preoperative CT stud- ≥ 6.8 mm (p = 0.11 and 0.04, respectively).

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Motiei-Langroudi et al.

TABLE 1. Univariate and bivariate analysis of factors influencing TABLE 2. Multivariate analysis of factors influencing hemiparesis
hemiparesis
Parameter OR 95% CI p Value
Patients Patients
Unilateral vs bilateral hematoma 1.96 1.04–3.76 0.033
With Without p
Parameter Hemiparesis Hemiparesis Value Loculation vs no loculation 2.00 1.11–3.22 0.004

Sex 0.71
 Female 47 (49.5%) 48 (50.5%)
 Male 99 (46.5%) 114 (53.5%) Discussion
Trauma history 0.43 Chronic subdural hematoma (CSDH) may present with
 No 32.4% 67.6% a variety of symptoms, including headache, nausea and
 Yes 41.5% 58.5% vomiting, deterioration in consciousness, and neurological
Comorbidity 0.58
deficits (most commonly hemiparesis).3 Along with hema-
toma volume and state of arousal, hemiparesis is a key
 No 5 (33.3%) 10 (66.7%) indication for surgical intervention. Moreover, it is an in-
 Yes 46 (43.0%) 61 (57.0%) dicator of a more critical state in CSDH.1,3,7,9 Indeed, neu-
Anticoagulant or antiplatelet use 0.99 rological status on presentation (including hemiparesis)
 No 29 (42.0%) 40 (58.0%) has been shown by some to be the single most important
 Yes 33 (42.3%) 45 (57.7%) prognostic indicator for CSDH patients.9 Brain MRI stud-
Hematoma laterality 0.02*
ies reveal signal changes in structures such as the cerebral
peduncles in patients with hemiparesis, which may pres-
 Unilateral 133 (51.4%) 126 (48.6%) age poorer surgical outcome.4 Consequently, early diagno-
 Bilateral 19 (33.3%) 38 (66.7%) sis and intervention are important in CSDH patients with
Hematoma CT density 0.43 hemiparesis.
 Hypodense 37 (55.2%) 30 (44.8%) Despite the apparent importance of hemiparesis in
 Isodense 34 (45.9%) 40 (54.1%) CSDH, very few studies have tried to identify imaging
  Mixed hyper- & hypodense 77 (46.4%) 89 (53.6%)
hallmarks that would predict it. In a study of 83 patients
with both unilateral and bilateral hematomas, Juković et
Hematoma T1 MRI intensity 0.35 al. found that the maximal diameter of the hematoma and
 Hypointense 1 (25.0%) 3 (75.0%) the degree of MLS measured on noncontrast CT were as-
  Mixed hypo- & isointense   1 (100.0%) 0 (0%) sociated with hemiparesis.3 Ikeda et al. employed xenon
 Isointense 4 (44.4%) 5 (55.6%) CT to measure regional cerebral blood flow (rCBF) in 38
  Mixed iso- & hyperintense 1 (100%) 0 (0%) patients with unilateral CSDH and found that while rCBF
 Hyperintense 12 (66.7%) 6 (33.3%)
was normal in all patients without hemiparesis, it was gen-
erally decreased in patients with hemiparesis, especially
Hematoma T2 MRI intensity 0.45 in the rolandic region ipsilateral to the hematoma.2 Oh et
 Isointense 4 (57.1%) 3 (42.9%) al. observed corticospinal tract degeneration on diffuse
  Mixed iso- & hyperintense 2 (100%) 0 (0%) tensor MRI in one CSDH patient whose hemiparesis did
 Hyperintense 13 (54.2%) 11 (45.8%) not resolve after surgery.6
Loculation 0.001* The present study, based on 325 patients, is to our
 Yes 84 (57.9%) 61 (42.1%)
knowledge the largest series of CSDH reported to date. In
accordance with previous studies, we found that hemato-
 No 59 (38.6%) 94 (61.4%) ma maximal thickness and midline shift were significant
Age (yrs) 74.6 ± 12.6 69.6 ± 13.4 0.03* predictors of hemiparesis in CSDH. In addition, we found
GCS score 14.3 ± 1.6 14.5 ± 1.4 0.24 for the first time that hematoma loculation and patient age
Hematoma maximal thickness 22.8 ± 5.8 18.5 ± 6.0 0.001* also predicted hemiparesis. Loculation was an indepen-
(mm) dent causative factor for hemiparesis (as shown in both
Midsagittal line shift (mm) 7.8 ± 5.4 6.0 ± 5.4 0.003* univariate and multivariate analysis). The mechanism by
which loculation may induce hemiparesis is unknown;
Values are presented as number of patients (%) or mean ± SD. however, compression of the motor cortex is certainly a
* Statistically significant. possibility. Another possible explanation is that loculated
hematomas may have higher local pressure and tension
rather than more diffusely increased pressure. Tension in
Postoperative Resolution of Hemiparesis CSDH has recently been reported to be an influencing fac-
At their final follow-up, all patients with preopera- tor in the development of hemiparesis in these patients.8
tive hemiparesis had completely recovered their muscle We also showed a higher rate of hemiparesis in unilateral
strength. Analysis showed that age, hematoma size, surgi- than bilateral hematomas, possibly due to greater hema-
cal evacuation type (burr hole drainage vs craniotomy), toma thickness and increased MLS. Finally, we found
or presence of loculations did not affect hemiparesis re- that there are different thresholds for the development of
covery after surgery (p = 0.5, 0.45, 0.79, and 0.3, respec- hemiparesis depending on hematoma thickness and MLS
tively). in unilateral and bilateral hematomas, though the analysis

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Motiei-Langroudi et al.

in patients with bilateral hematomas is less reliable due a series of patients including both nonsurgical and surgi-
to the small sample size. Among patients with unilateral cal patients. This requirement, nonetheless, needs a larger
hematomas, we found that hematoma maximal thick- study involving multiple practices. Another issue with
ness of approximately 20 mm and midline shift of 6 mm the current study is that we did not evaluate the effect of
were associated with a 50% probability of hemiparesis. CSDH duration prior to surgery on hemiparesis, as longer
One prior study also noted different thresholds of MLS durations may cause higher rates of hemiparesis. Although
for hemiparesis in unilateral and bilateral CSDHs (10 mm we showed that the presence of loculations (as an indicator
and 4.5 mm, respectively).3 Our results, based on a larger of hematoma chronicity) is associated with a higher rate of
patient database, showed that lower thresholds should be hemiparesis, we could not directly assess the time factor.
taken into account when managing CSDH patients. Of To evaluate this variable, the exact time of CSDH onset
note, imaging factors like hematoma size and MLS are should be determined through CT imaging studies before
not the only factors determining the need for surgery, as surgery, which is not done in all patients. Future studies
other factors such as severity of symptoms (headache for focusing on this issue may be helpful for clarification.
instance), neurological status, hematoma progression in
subsequent CTs, etc. should also be considered. As such, Conclusions
surgery may be considered for a smaller hematoma with
lower shifts if clinically indicated. On the other hand, in The results of our study showed that the presence of
many practices larger hematomas (more than 15 or 20 mm loculations, unilateral hematomas, older patient age, he-
maximal thickness) are frequently indicated for surgery matoma maximal thickness, and MLS are associated with
based only on their size, regardless of neurological status a higher rate of hemiparesis in CSDH. Among these vari-
and presence of paresis. ables, only hematoma loculation and laterality remained
Although hemiparesis resolution after surgery was not as significant predictors in multivariate analysis. More-
the main outcome of the current study, we failed to show over, 19.8 mm of hematoma thickness and 6.4 mm of MLS
an effect for age, hematoma size, presence of loculations, are associated with a 50% probability of hemiparesis in
surgical evacuation type, or other factors to predict hemi- unilateral hematomas.
paresis resolution. The main reasons for this observation
could be the following: 1) all patients improved after sur- Acknowledgments
gery; 2) the initial MRC hemiparesis grade before surgery We thank Ms. Patricia Baum, BSc, for her help with this study.
was 4/5 or 3/5 at most in our series; and 3) a large number
of patients (52%) were neurologically intact (MRC grade
5/5). All of these factors contributed to the fact that the References
improvement in motor scale after surgery yielded small   1. Adhiyaman V, Asghar M, Ganeshram KN, Bhowmick BK:
numbers (ranging from 0 to 2), resulting in a statistical- Chronic subdural haematoma in the elderly. Postgrad Med J
ly negative analysis. More studies focusing only on the 78:71–75, 2002
  2. Ikeda K, Ito H, Yamashita J: Relation of regional cerebral
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address this issue. Surg Neurol 33:87–95, 1990
Our study was aimed at investigating patient and imag-   3. Juković MF, Stojanović DB: Midline shift threshold value for
ing factors related to the development of hemiparesis and hemiparesis in chronic subdural hematoma. Srp Arh Celok
was not designed to answer the question of whether to de- Lek 143:386–390, 2015
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tive management, which is more extensively investigated Kernohan’s notch phenomenon in chronic subdural hema-
toma: MRI findings. J Clin Neurosci 14:989–992, 2007
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gate a question about an important presentation of CSDH, Pearls. Treasure Island, FL: StatPearls Publishing, 2018
which has both decision-making and prognostic value. As (http://www.ncbi.nlm.nih.gov/books/NBK436008/) [Ac-
such, our results cannot directly suggest thresholds for cessed October 2, 2018]
surgery based on imaging or patient factors. This question   6. Oh SI, Kim MJ, Oh KP, Kim HY, Kim SH, Kim HJ: Tractog-
remains unanswered until a later date. raphy of persistent ipsilateral hemiparesis following subdural
hematoma. Can J Neurol Sci 40:601–602, 2013
  7. Sucu HK, Gelal F, Gökmen M, Ozer FD, Tektaş S: Can
Limitations midline brain shift be used as a prognostic factor to predict
The major limitation of the current study is its retro- postoperative restoration of consciousness in patients with
spective design. Nevertheless, the relatively large sample chronic subdural hematoma? Surg Neurol 66:178–182, 2006
size in a group of consecutively treated patients allows   8. Tomita Y, Yamada SM, Yamada S, Matsuno A: Subdural ten-
for statistically reliable observations to be made that may sion on the brain in patients with chronic subdural hematoma
serve as a focus of future prospective studies. One other is related to hemiparesis but not to headache or recurrence.
World Neurosurg 119:e518–e526, 2018
major limitation is that our series is a surgical series and   9. van Havenbergh T, van Calenbergh F, Goffin J, Plets C: Out-
all patients were included if they underwent surgery. A come of chronic subdural haematoma: analysis of prognostic
study including all patients presenting with CSDH, re- factors. Br J Neurosurg 10:35–39, 1996
gardless of treatment option, would be more appropriate
to answer the questions raised in this study. Specifically,
any recommendations for surgical intervention instead of Disclosures
conservative management would be more appropriate in The authors report no conflict of interest concerning the materi-

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Motiei-Langroudi et al.

als or methods used in this study or the findings specified in this analysis: Motiei-Langroudi, Phan. Administrative/technical/mate-
paper. rial support: Thomas. Study supervision: Thomas, Stippler.

Author Contributions Correspondence


Conception and design: Thomas, Motiei-Langroudi. Acquisition Ajith J. Thomas: Beth Israel Deaconess Medical Center, Harvard
of data: Motiei-Langroudi. Analysis and interpretation of data: Medical School, Boston, MA. athomas6@bidmc.harvard.edu.
Motiei-Langroudi, Phan. Drafting the article: Motiei-Langroudi.
Critically revising the article: Thomas, Motiei-Langroudi, Alter-
man, Stippler, Alturki, Papavassiliou, Kasper, Arle, Ogilvy.
Reviewed submitted version of manuscript: all authors. Statistical

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