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Pseudohypoxic Brain Swelling: Report of 2 Cases and Introduction of the Lentiform Rim Sign as Potential MRI Marker
Journal Pre-proof Pseudohypoxic Brain Swelling: report of 2 cases and introduction of the Lentiform Rim Sign as Potential MRI Marker Houman Sotoudeh, M.D., Philip R. Chapman, M.D., Ehsan Sotoudeh, M.D., Aparna Singhal, M.D., Gagandeep Choudhary, M.D., Omid Shafaat, M.D. PII:
S1878-8750(19)32633-6
DOI:
https://doi.org/10.1016/j.wneu.2019.10.018
Reference:
WNEU 13489
To appear in:
World Neurosurgery
Received Date: 20 July 2019 Revised Date:
1 October 2019
Accepted Date: 3 October 2019
Please cite this article as: Sotoudeh H, Chapman PR, Sotoudeh E, Singhal A, Choudhary G, Shafaat O, Pseudohypoxic Brain Swelling: report of 2 cases and introduction of the Lentiform Rim Sign as Potential MRI Marker, World Neurosurgery (2019), doi: https://doi.org/10.1016/j.wneu.2019.10.018. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2019 Elsevier Inc. All rights reserved.
Title page
Manuscript title: Pseudohypoxic Brain Swelling: report of 2 cases and introduction of the Lentiform Rim Sign as Potential MRI Marker
Running title: Role of imaging in PHBS/PIHV The full names and order of all authors: Houman Sotoudeh, M.D.1*, Philip R. Chapman, M.D.1, Ehsan Sotoudeh M.D.2, Aparna Singhal, M.D.1, Gagandeep Choudhary, M.D.1, Omid Shafaat, M.D.4
1. Department of Neuroradiology and Neurology, University of Alabama at Birmingham (UAB), 619 19th St S, Birmingham, AL, USA 35294
2. Department of Neuroradiology and Neurology, University of Alabama at Birmingham (UAB), 619 19th St S, Birmingham, AL, USA 35294 3. Department of Surgery, Iranian Hospital in Dubai, P.O.BOX: 2330, Al-Wasl Road, Dubai, UAE, Dubai 2330, United Arab Emirates.
4. Department of Radiology and Interventional Neuroradiology, Isfahan University of Medical Sciences, Isfahan, Iran Contact information of all co-authors: Houman Sotoudeh, M.D.: Department of Neuroradiology, University of Alabama at Birmingham (UAB); 619 19th St S, Birmingham, AL, USA 35294, JTN 333. Tel: 001(205) 8018750, office 43933 Email: [email protected]; ORCID ID: 0000-0002-5510-7062 Philip R. Chapman, M.D.: Department of Neuroradiology and Neurology, University of Alabama at Birmingham (UAB), 619 19th St S, Birmingham, AL, USA 35294 Email: [email protected]; ORCID ID: 0000-0002-9296-5672 Ehsan Sotoudeh M.D.: Department of Surgery, Iranian Hospital in Dubai, P.O.BOX: 2330, AlWasl Road, Dubai, UAE, Dubai 2330, United Arab Emirates. Email: [email protected]; ORCID ID: 0000-0002-4918-8230 Aparna Singhal, M.D.: Department of Neuroradiology, University of Alabama at Birmingham (UAB); 619 19th St S, Birmingham, AL, USA 35294 Email: [email protected];
Gagandeep Choudhary, M.D.: Department of Neuroradiology, University of Alabama at Birmingham (UAB); 619 19th St S, Birmingham, AL, USA 35294; Email: [email protected] Omid Shafaat, M.D.: Department of Radiology and radiological Sciences, Isfahan University of Medical Sciences, Hezar Jarib St, Isfahan, Iran, P.O. Box:8174673461, ORCID ID: 0000-00018793-7901
*Corresponding Author: Houman Sotoudeh, MD Assistant Professor of Neuroradiology and Neurology, Department of Neuroradiology, University of Alabama at Birmingham (UAB); 619 19th St S, Birmingham, AL, USA 35294, JTN 333. Tel: 001(205) 801-8750, office 43933 Email: [email protected]
Total number of tables and figures: Tables: 0, Figures: 4 Conflict of Interest: None Funding: None Keywords: Pseudohypoxic brain swelling; intracranial hypotension; venous cerebral congestion; postoperative intracranial hypotension; venous congestion; magnetic resonance imaging; neuroradiology
Sotoudeh 1
Pseudohypoxic Brain Swelling: report of 2 cases and introduction of the Lentiform Rim Sign as Potential MRI Marker
2 3 4
Abstract
5
Background: A rare but important complication related to otherwise uneventful brain and spine
6
surgery is becoming more recognized and more frequently reported in the medical literature.
7
This has been variably labelled as pseudohypoxic brain swelling (PHPS) or postoperative
8
hypotension-associated venous congestion (PIHV). This poorly understood condition occurs in
9
the setting of surgical intervention and is thought to be related to CSF leak or evacuation,
10
decreased intracranial pressure, and subsequent development of deep venous congestion
11
affecting the basal ganglia, thalami, and cerebellum. Clinically, patients may have global
12
neurologic deficit and outcomes range from full recovery to vegetative state or death. The
13
imaging correlate includes atypical edema, infarction, or hemorrhage and can overlap the
14
appearance of diffuse hypoxic injury, for which this condition can be mistaken both clinically
15
and radiologically. While this deep brain tissue edema can be associated with other signs of CSF
16
hypotension such as dural thickening, brain sagging, and cerebellar herniation, it can be isolated,
17
making the diagnosis challenging.
18
Case Description: We present 2 cases of unexpected clinical deterioration occurring in patients
19
with otherwise uncomplicated neurosurgery, one with craniotomy and the other with lumbar
20
spine intervention. Both patients exhibit similar appearing edema in the deep gray structures on
21
postoperative MRIs. In addition to reviewing the prior literature and imaging findings, we
22
evaluate the imaging findings to determine if there are unique features or signatures that might
23
allow differentiation of PHBS from hypoxic-ischemic encephalopathy.
24
Conclusion: The lentiform rim sign can be helpful for differentiation of PHBS versus hypoxic-
25
ischemic encephalopathy.
26 27
Keywords: Pseudohypoxic brain swelling; intracranial hypotension; venous cerebral congestion;
28
postoperative intracranial hypotension; venous congestion; magnetic resonance imaging;
29
neuroradiology 1
Sotoudeh 30 31
Introduction
32
A rare but important complication related to otherwise uneventful brain and spine surgery is
33
becoming more recognized and more frequently reported in the medical literature. This has been
34
variably labelled as pseudohypoxic brain swelling (PHBS) or postoperative hypotension-
35
associated venous congestion (PIHV).
36
described after uncomplicated brain surgery that utilized vacuum assisted CSF drainage 1. This
37
condition has also been reported after spinal surgery 2. The most common presentation of
38
PHBS/PIHV is an unexpected postoperative alteration of consciousness, seizure, and brainstem
39
dysfunction
40
related to stroke or occult hypoxic/ischemic event. The physiopathology of PHBS is still
41
controversial but it appears that rapid surgical drainage of CSF or CSF leak during surgery
42
causes sudden intracranial hypotension, brain stem sagging, venous congestion and secondary
43
venous ischemia or infarction because of shear forces involving the main intracranial deep
44
venous structures 2-9.
2-5
The authors prefer PHBS. The condition was first
. Clinically, patients are most often considered to have acute neurologic deficit
45 46
Radiologically, the findings include abnormal hypodensity (CT) or abnormal signal intensity
47
(MRI) involving the thalami, basal ganglia and cerebellum. These imaging findings reflect the
48
acute venous congestion and edema that occurs preferentially in these structures. The findings
49
on CT or MRI can suggest atypical arterial stroke or hypoxic-ischemic encephalopathy. However
50
vascular imaging e.g., MR angiography (MRA) and CT angiography (CTA) generally fail to
51
demonstrate pathologic findings
52
vasculature, hypoperfusion of basal ganglia, thalami, cerebellum, and telencephalon has been
53
reported in some patients using perfusion imaging 2. The bilateral symmetric involvement of the
54
deep gray structures on CT and MRI overlaps the appearance of deep venous thrombosis and
55
venous infarction. However, no venous thrombosis or obstruction has been identified. 2, 10-16.
2, 5, 8
. Despite unremarkable morphology of the brain
56 57
Diagnosis of PHBS is challenging. It is relatively rare but is becoming more recognized as case
58
reports and case series are being published. The clinical and radiologic findings are ultimately
59
nonspecific and many cases are considered to represent occult hypoxic/ischemic event. . In this
60
manuscript, we present 2 additional cases of PHBS, including the clinical presentation and 2
Sotoudeh 61
radiological findings in each case as well as a review of the literature. We also introduce a
62
potentially useful MRI marker: peripheral rim of T2/FLAIR hyperintensity along the lentiform
63
nuclei (Lentiform Rim Sign).
64 65 66 67
Case 1
68
An 81-year-old female with diabetes mellitus, atrial fibrillation, and hypertension presented with
69
exacerbation of back pain and radiculopathy and was found to have segmental lumbar stenosis.
70
The patient subsequently underwent lumbar spine surgery consisting of L3-L5 decompression
71
with internal fixation/fusion. The surgical procedure took approximately 3 hours and no
72
complications were noted during the procedure. A durotomy was not performed and there was no
73
specific finding during surgery to indicate possible CSF leak. Immediately after the surgery, the
74
patient experienced new onset of seizure activity that was treated with propofol. To exclude
75
brain infarction, the patient initially underwent brain and neck CT angiogram (CTA) and CT
76
perfusion (CTP) which were unremarkable. There was no large vessel occlusion, perfusion
77
abnormality, or evidence of intracranial hemorrhage. EEG demonstrated rhythmic appearing 1-2
78
Hz generalized sharp waves which improved with increased propofol. Although the clinical
79
presentation was concerning for hypoxic brain injury, the intraoperative record did not indicate
80
any prolonged periods of hypotension, and one episode of hypotension during a transient episode
81
of seizure was not severe or long lasting. There were no documented hypoxic events during
82
surgery and intubation procedure was uneventful.
83
Follow-up CT scan one day after the first seizure demonstrated diffuse brain edema with
84
diffuse effacement of cerebral sulci and generalized white matter hypodensity (Fig 1 A).
85
Subsequent MRI showed abnormal increased T2/fluid-attenuated inversion recovery (T2/FLAIR)
86
signal intensity in caudate heads, globous pallidum, putamen, and thalami bilaterally. Also noted
87
was a conspicuous rim of T2/FLAIR hyperintense signal lateral and inferomedial to the lentiform
88
nuclei (Fig 1 B and C arrows). There was minimal abnormal FLAIR hyperintensity in the
89
cerebellar hemispheres (Fig 1 D). Diffusion weighted images (DWI) showed no diffusion
90
restriction to indicate completed infarction or hypoxic-ischemic encephalopathy (Fig 1 E). The 3
Sotoudeh 91
patient’s condition improved after admission to intensive care unit. Follow-up brain CT 3 days
92
later showed complete resolution of diffuse brain edema (Fig 1 F). Ultimately the patient
93
recovered and transferred to skilled nursing facility with persistent cognitive deficits and
94
limitations in activities of daily living.
95 96
Case 2
97
A 72-year-old man with unremarkable past medical history presented with new onset of gait
98
instability. Initial CT scan of the head demonstrated a right-sided subdural hematoma associated
99
with mass effect and mild midline shift (Fig 2 A). On the second day of hospitalization, a right
100
frontal craniotomy and subdural evacuation was performed. In recovery, the patient developed
101
new-onset seizure activity that progressed to intractable status epilepticus. Despite extensive
102
medical regimen, status epilepticus continued and patient was ultimately placed into a medically
103
induced coma. No episode of hypotension was noted during the initial surgery or postoperative
104
period. Post-surgical brain CT showed interval development of bilateral but asymmetric
105
hypodensity in the lentiform nuclei (Fig 2 B). Subsequent MRI one day after surgery showed
106
T2/FLAIR hyperintense signal (Fig 2 C and D), diffusion restriction on DWI (Fig 2 E and F) and
107
petechial hemorrhagic changes (Fig 2 G) in lentiform nuclei. A prominent rim of T2/FLAIR
108
hyperintense signal was noted lateral and inferomedial to lentiform nuclei (Fig 2 C and D
109
arrows). On postcontrast T1 sequence no abnormal enhancement was noted (Fig 2 H). Attempts
110
to stop continuous midazolam resulted in recurrence of status epilepticus. The patient
111
subsequently developed methicillin-resistant staph aureus (MRSA) pneumonia and died.
112 113 114
Discussion and review of literature
115
PHBS is a rare condition often occurring after an uneventful brain or spinal surgical procedure
116
that can result in abrupt neurologic decline, new onset of seizure, brainstem dysfunction and can
117
lead to vegetative state or death
118
PHBS have been reported in English literature 9. The pathophysiology is poorly understood and
119
may not be completely elucidated. Most authors suggest that the phenomenon is governed by the
120
Monro-Kellie doctrine, which helps define the complex relationship between intracranial
1, 2, 8
. Based on our review of the current literature 24 cases of
4
Sotoudeh 121
pressure, CSF volume and cerebral perfusion. Presumably, a rapid reduction in CSF pressure or
122
volume during surgical procedure of the brain or spine can initiate a cascade of events including
123
inferior descent of the brain stem and compensatory increase in cerebral blood volume/venous
124
congestion. Venous congestion and inferior sagging cause shearing force over the vein of Galen
125
at the tentorium, venous congestion of deep brain structures and finally venous hemorrhagic
126
infarction in deep brain structures
127
inappropriate dural repair and suction of large CSF volume have been reported as the risk factors
128
for this condition.1, 4, 5, 8. Application of subdural or subgaleal suction has been implicated in
129
some cases as the potential causative event. PHBS has been described after extradural and
130
epicranial CSF drainage after craniotomy, spinal surgery and decompression of hydrocephalus 4.
3, 7-9
. Perioperative volume depletion, surgical position,
131 132
The most common presentation of PHBS is brainstem dysfunction including altered mental
133
status, seizure, bradycardia, hypotension and cardiac arrest 4, which presents on imaging as
134
hypodensity (CT) and T2/FLAIR hyperintense signal (MRI) of basal ganglia, thalami and
135
cerebellum with diffuse brain swelling and effacement of cerebral sulci
136
findings ranging from normal to patchy restriction to large homogeneous zones of restriction. 2
137
Hemorrhage can occur as well, typically petechial type hemorrhage. 2 The imaging findings can
138
also overlap and mimic deep venous thrombosis
139
MRA) are usually normal but relative hypoperfusion of basal ganglia and telencephalon has been
140
described 1, 2. There is no definite treatment for this condition but intrathecal saline infusion has
141
been tried 17.
3, 5, 9
2, 5
. DWI demonstrates
. Anatomic vascular imaging (CTA and
142 143
The main differential diagnosis of PHBS is the much more common hypoxic-ischemic
144
encephalopathy which can present with the similar abnormal radiologic findings of basal ganglia
145
and thalami. At this time, there is no definite radiologic finding to differentiate these two
146
conditions based on CT or MRI. Upon review of our cases and previously published cases of
147
PHBS, we observed a prominent hyperintense rim of abnormal T2/FLAIR signal along the
148
lateral and inferomedial border of the lentiform nuclei in some case. To our knowledge, this
149
finding is unusual and not prominent in other pathologies of the basal ganglia presenting acutely.
150
We refer to this finding as the “lentiform rim sign” and found it to be conspicuous in both of the
151
current cases. We propose that this sign might be a potential useful MRI marker for this 5
Sotoudeh 152
condition. By definition, the signal of the “lentiform rim sign” must be higher than the lentiform
153
nucleus itself and the adjacent white matter on T2 and FLAIR sequences. We have
154
retrospectively observed a similar sign in some of previously published reports, although
155
conclusions are difficult in that only a few images are reviewable. Yokota et al. described a case
156
of PHBS after craniotomy for clipping the anterior communicating artery aneurysm. Their case
157
demonstrated the “lentiform rim sign”
158
spinal surgery, at least one of which appeared to demonstrate the “lentiform rim sign” 2.
159
Dickinson et al. described a case of PHBS after spinal surgery with “lentiform rim sign” in the
160
right side and hemorrhagic changes of the left lentiform nucleus 8. Van roost et al. published the
161
FLAIR image of one of their patients (patient No 14) with PHBS which showed “lentiform rim
162
sign”. In one published case by Snyder et al. this sign was also present 18.
5
. Parpaley et al. described two cases of PHBS after
163 164
To describe the “lentiform rim sign”, the deep brain venous anatomy should be reviewed. The
165
venous drainage of deep brain structures is firstly done by the medullary veins. The medullary
166
veins from the caudate nucleus constitute the “caudate vein”. The medullary vein from the basal
167
ganglia and thalami join to build the “terminal vein”. The “caudate” and ‘terminal” veins join to
168
make the “thalamostriate vein”. The “septal vein” (which receives blood from the genu of the
169
corpus callosum, septum pellucidum, and the anterior part of the caudate nucleus)
170
and “thalamostriate” veins join to build the internal cerebral vein which then drains toward the
171
vein of Galen (Fig 3). CSF hypotension and sagging of the brain likely causes deviation of these
172
deep brain veins and secondary impairment of venous derange. This theory is supported by
173
selective edema of these deep brain nuclei. Venous congestion causes selective edema in
174
structures who drained by deep veins but not peripheral brain parenchyma, which is
175
mainly drained by superficial veins. Edema between these two different venous territories causes
176
the rim of T2/FLAIR hyper-signal intensity around the lentiform nuclei the “lentiform rim sign”.
177
In severe form, these venous drainage impairments, can cause elevated venous pressure and
178
secondary venous infarction of the deep brain nuclei with diffusion restriction although diffusion
179
restriction is not as severe as arterial infarction. These venous infarcts tend to be hemorrhagic in
180
comparison to arterial infarction.
181
6
Sotoudeh 182
In
the
most
common differential diagnosis
of
this
condition,
the
hypoxic-ischemic
183
encephalopathy, in the other hand, the reason of selective involvement of deep structures is
184
higher metabolic rate of deep nuclei in comparison to peripheral white matter. In this hypoxic-
185
ischemic injury of deep nuclei, the edema is not dominant at least in acute phase so the rim of
186
T2/FLAIR hyper-signal intensity around the lentiform nuclei is not prominent (Fig 4).
187 188
A similar radiologic finding “lentiform fork sign” has been described in renal failure, uremia,
189
methanol toxicity, metabolic acidosis, mitochondrial disorders and metformin encephalopathy
190
19-27
191
involving the external capsule, external medullary lamina, internal medullary lamina and
192
internal capsule with trident morphology. In our cases, we did not observe the classical trident
193
morphology of “lentiform fork sign”. None of our cases had documented uremia, metabolic
194
acidosis or other underlying etiologies of lentiform fork sign.
. The “lentiform fork sign” represents edema and produces T2/FLAIR signal abnormality
195
Accuracy of “lentiform rim sign” for diagnosis the PHBS versus ischemic hypoxic
196
encephalopathy cannot be evaluated in this manuscript given rare incidence of PHBS. Further
197
investigation might confirm the utility of this finding.
198 199
Both of our cases presented by seizure. Seizures shortly after spinal surgeries have been reported
200
in few cases mainly in association with cerebral and cerebellar hemorrhages. It has been
201
suggested that rapid decrease of CSF pressure secondary to durotomy causes acute occlusion of
202
bridging veins and secondary cerebral/cerebellar hemorrhages. Finally, the exposure of brain to
203
hemoglobin (subdural hematoma), which has proconvulsive effects, is likely the reason for
204
seizure28, 29 . We didn’t detect evidence of intracranial hemorrhages in our first case and seizure
205
in this case was likely because of different process such as brain congestion. Although our
206
second case had subdural hematoma before craniotomy but given development of abnormal
207
signal/density, congestion and hemorrhages in the lentiform nuclei (which are not common
208
imaging findings after seizure) we believe seizure in this case was also because of venous
209
congestion and brain edema.
210
Conclusion
211
PHBS is a rare but important complication related to otherwise uneventful brain and spine
212
surgery and is becoming more recognized and more frequently reported in the medical literature. 7
Sotoudeh 213
This poorly understood condition occurs in the setting of surgical intervention and is thought to
214
be related to CSF leak or evacuation, decreased intracranial pressure, and subsequent
215
development of deep venous congestion affecting the basal ganglia, thalami, and cerebellum.
216
The clinical and imaging features can overlap those of hypoxic/ischemic event. This entity
217
should be considered in the differential of any patient that undergoes acute postoperative
218
neurologic decline and has atypical edema, mass effect, or hemorrhage involving the deep gray
219
structures. As we report, the presence of a peripheral rim of edema along the lentiform nuclei,
220
the “lentiform rim sign “may represent a potential marker for this condition.
221 222
Conflict of interest
223
All authors declare that the research was conducted in the absence of any commercial or
224
financial relationships that could be construed as a potential conflict of interest.
225 226
Author Contributions
227
HS, and PC contributed conception and design of the study; HS organized the database; HS, OS,
228
PC, and ES wrote the first draft of the manuscript. AS and GC helped us in revising and editing
229
the final manuscript. All authors contributed to manuscript revision, read and approved the
230
submitted version.
231 232
Funding
233
This research did not receive any specific grant from funding agencies in the public, commercial,
234
or not-for-profit sectors.
235 236
References
237 238 239 240 241
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2. Parpaley Y, Urbach H, Kovacs A, Klehr M, Kristof RA. Pseudohypoxic brain swelling (postoperative intracranial hypotension-associated venous congestion) after spinal surgery: report of 2 cases. Neurosurgery. 2011;68(1): E277-283. https://doi.org/10.1227/NEU.0b013e3181fead14. 3. Hadizadeh DR, Kovacs A, Tschampa H, Kristof R, Schramm J, Urbach H. Postsurgical intracranial hypotension: diagnostic and prognostic imaging findings. AJNR Am J Neuroradiol. 2010;31(1): 100-105. https://doi.org/10.3174/ajnr.A1749. 4. Moon HS, Lee SK, Kim SR, Kim SJ. Cardiac arrest due to intracranial hypotension following pseudohypoxic brain swelling induced by negative suction drainage in a cranioplasty patient: a case report. Korean J Anesthesiol. 2016;69(3): 292-295. https://doi.org/10.4097/kjae.2016.69.3.292. 5. Yokota H, Yokoyama K, Miyamoto K, Nishioka T. Pseudohypoxic brain swelling after elective clipping of an unruptured anterior communicating artery aneurysm. Clin Neurol Neurosurg. 2009;111(10): 900-903. https://doi.org/10.1016/j.clineuro.2009.08.007. 6. Mokri B. The Monro-Kellie hypothesis: applications in CSF volume depletion. Neurology. 2001;56(12): 1746-1748. https://doi.org/10.1212/wnl.56.12.1746. 7. Savoiardo M, Minati L, Farina L, et al. Spontaneous intracranial hypotension with deep brain swelling. Brain. 2007;130(Pt 7): 1884-1893. https://doi.org/10.1093/brain/awm101. 8. Dickinson J, Kroll D, Bentley J, Gustin AJ. Pseudohypoxic Brain Swelling After Elective Lumbar Spinal Surgery: Case Report. Cureus. 2018;10(4): e2454. https://doi.org/10.7759/cureus.2454. 9. Nomura M, Ota T, Ishizawa M, Yoshida S, Hara T. Intracranial Hypotension-associated Cerebral Swelling following Cranioplasty: Report of Two Cases. Asian J Neurosurg. 2017;12(4): 794-796. https://doi.org/10.4103/1793-5482.185070. 10. Fujimura M, Kameyama M, Motohashi O, Kon H, Ishii K, Onuma T. Cerebral infarction in the caudate nucleus associated with acute epidural hematoma and diffuse brain injury in a child after severe head injury. Childs Nerv Syst. 2004;20(6): 430-433. https://doi.org/10.1007/s00381-003-0884-0. 11. Giannopoulos S, Kostadima V, Selvi A, Nicolopoulos P, Kyritsis AP. Bilateral paramedian thalamic infarcts. Arch Neurol. 2006;63(11): 1652. https://doi.org/10.1001/archneur.63.11.1652. 12. Gladstone DJ, Silver FL, Willinsky RA, Tyndel FJ, Wennberg R. Deep cerebral venous thrombosis: an illustrative case with reversible diencephalic dysfunction. Can J Neurol Sci. 2001;28(2): 159-162. 13. Herrmann KA, Sporer B, Yousry TA. Thrombosis of the internal cerebral vein associated with transient unilateral thalamic edema: a case report and review of the literature. AJNR Am J Neuroradiol. 2004;25(8): 1351-1355. 14. Hoitsma E, Wilmink JT, Lodder J. Bilateral thalamic infarction may result from venous rather than arterial obstruction. J Stroke Cerebrovasc Dis. 2002;11(1): 47-50. https://doi.org/10.1053/jscd.2002.123975. 15. Karaaslan P, Pirat A, Karakayali H, Can U, Arslan G. Bilateral thalamic infarct after general anaesthesia for laparotomy: an unusual case of perioperative cryptogenic stroke. Acta Anaesthesiol Scand. 2008;52(2): 316. https://doi.org/10.1111/j.1399-6576.2007.01526.x. 16. Kumral E, Evyapan D, Balkir K, Kutluhan S. Bilateral thalamic infarction. Clinical, etiological and MRI correlates. Acta Neurol Scand. 2001;103(1): 35-42. 17. Binder DK, Dillon WP, Fishman RA, Schmidt MH. Intrathecal saline infusion in the treatment of obtundation associated with spontaneous intracranial hypotension: technical case report. Neurosurgery. 2002;51(3): 830-836; discussion 836-837. 18. Snyder KA, Clarke MJ, Gilbertson JR, Hocker SE. Prompt Recognition and Management of Postoperative Intracranial Hypotension-Associated Venous Congestion: A Case Report. Neurocrit Care. 2016;24(3): 448-453. https://doi.org/10.1007/s12028-015-0207-9. 19. Kumar G, Goyal MK. Lentiform Fork sign: a unique MRI picture. Is metabolic acidosis responsible? Clin Neurol Neurosurg. 2010;112(9): 805-812. https://doi.org/10.1016/j.clineuro.2010.06.006. 9
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20. Fernandes GC, Koltermann T, Campos L, Vedolin L, Rieder CR. Teaching NeuroImages: the lentiform fork sign: an MRI pattern of metformin-associated encephalopathy. Neurology. 2015;84(3): e15. https://doi.org/10.1212/WNL.0000000000001154. 21. da Rocha AJ, Maia AC, Jr., da Silva CJ, Sachetti SB. Lentiform fork sign in a child with dialysis disequilibrium syndrome: a transient MRI pattern which emphasizes neurologic consequence of metabolic acidosis. Clin Neurol Neurosurg. 2013;115(6): 790-792. https://doi.org/10.1016/j.clineuro.2012.07.013. 22. Grasso D, Borreggine C, Perfetto F, et al. Lentiform fork sign: a magnetic resonance finding in a case of acute metabolic acidosis. Neuroradiol J. 2014;27(3): 288-292. https://doi.org/10.15274/NRJ2014-10041. 23. Kaiwar C. Teaching NeuroImages: The lentiform fork sign: An MRI pattern of metforminassociated encephalopathy. Neurology. 2015;85(7): 655. https://doi.org/10.1212/WNL.0000000000001847. 24. Park JW, Kim SU, Choi JY, Jung JM, Kwon DY, Park MH. Reversible parkinsonism with lentiform fork sign as an initial and dominant manifestation of uremic encephalopathy. J Neurol Sci. 2015;357(1-2): 343-344. https://doi.org/10.1016/j.jns.2015.08.002. 25. Rathi M, Mudrabettu C. Lentiform fork sign in a case of end-stage renal disease. Kidney Int. 2012;82(3): 365. https://doi.org/10.1038/ki.2012.119. 26. Saini AG, Kodakkattil Sreevilasan S, Singh P, Singhi P. Lentiform fork sign due to severe metabolic acidosis. BMJ Case Rep. 2017;2017. https://doi.org/10.1136/bcr-2017-222871. 27. Sookaromdee P, Wiwanitkit V. Methanol intoxication, lentiform fork sign, plasma methanol and osmolar gap. Arq Neuropsiquiatr. 2019;77(3): 216. https://doi.org/10.1590/0004-282X20190016. 28. Chan AY, Mullin JP, Benzel E, Bingaman W. Immediate Remote Cerebellar Hemorrhage and Seizure Following Revision Lumbosacral Fusion. Cureus. 2017;9(5): e1292. https://doi.org/10.7759/cureus.1292. 29. Bowers CA, Taussky P, Duhon BS, Schmidt MH. Multiple supra- and infratentorial intraparenchymal hemorrhages presenting with seizure after massive sacral cerebrospinal fluid drainage. Spine (Phila Pa 1976). 2011;36(4): E288-291. https://doi.org/10.1097/BRS.0b013e3181f9b10f.
318 319 320
Figure Legends
321
Fig 1. Non-contrast CT, one day after surgery, shows diffuse brain edema with effacement of
322
sulci and white matter hypodensity (A). MRI one day after surgery (B-E). On FLAIR and T2
323
sequence, there is mildly increased signal in lentiform nuclei, caudate and thalami in association
324
with a rim of hyper signal intensity lateral and inferomedial to the lentiform nuclei (B and C).
325
Minimal FLAIR hyper signal intensity in the cerebellum (D). No diffusion restriction to suggest
326
infarction (E). Non-contrast CT 3 day later shows complete interval resolution of brain edema
327
(F).
328 10
Sotoudeh 329
Fig 2. Initial brain CT shows right hemispheric subdural hematoma with mass effect and mild
330
midline shift-- normal density of basal ganglia (A). Post-surgical brain CT 1 day after the initial
331
CT shows postsurgical changes, right frontal pneumocephalus, and resolution of midline shift but
332
with interval development of hypodensity in basal ganglia (B). MRI 1 day after surgery (C-
333
H). T2 and FLAIR hyper signal intensity in basal ganglia with the rim of hyper signal intensity
334
lateral and inferomedial to the lentiform nuclei (arrows C and D). Diffusion restriction in the
335
lentiform nuclei, which is evident on diffusion-weighted imaging (DWI) and apparent diffusion
336
coefficient (ADC) map (E and F). Hemorrhagic changes in the lentiform nuclei causing
337
susceptibility artifact on SWI sequence (G). No visible abnormal enhancement on post-contrast
338
T1 sequence but with engorged vessels in lentiform nuclei, more prominent on the left side
339
which is felt to be engorged veins (arrows H).
340
Fig 3. Anatomic configuration of deep brain venous systems. SV: Septal Vein. C: Caudate Vein.
341
T: Terminal Vein. TS: Thalamostriate Vein. Red circle: Vein of Galen at the level of the
342
tentorium which is believed the location of venous shearing in PHBS/PIHV secondary to a rapid
343
decrease of intracranial pressure.
344 345
Fig 4. Application of “lentiform rim sign”. Top row a case of PHBS/PIHV (A-C). A rim of
346
T2/FLAIR hyper signal intensity lateral and inferomedial to the lentiform nuclei. No significant
347
diffusion restriction of deep brain structure. Bottom raw a case of hypoxic-ischemic
348
encephalopathy (D-F). No “lentiform rim sign”. More prominent diffusion restriction of deep
349
brain structures.
350
11
Abbreviations PHBS (psudohypoxic brain swelling); PIHV (postoperative intracranial hypotension-associated venous congestion); CSF (cerebrospinal fluid); CT (computed tomography); MRI (magnetic resonance imaging); CTA (CT angiography); CTP (CT perfusion); T2/FLAIR (T2/fluidattenuated inversion recovery); DWI (diffusion-weighted imaging); ADC (apparent diffusion coefficient)
Conflict of interest All authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
S1878-8750(19)32633-6
DOI:
https://doi.org/10.1016/j.wneu.2019.10.018
Reference:
WNEU 13489
To appear in:
World Neurosurgery
Received Date: 20 July 2019 Revised Date:
1 October 2019
Accepted Date: 3 October 2019
Please cite this article as: Sotoudeh H, Chapman PR, Sotoudeh E, Singhal A, Choudhary G, Shafaat O, Pseudohypoxic Brain Swelling: report of 2 cases and introduction of the Lentiform Rim Sign as Potential MRI Marker, World Neurosurgery (2019), doi: https://doi.org/10.1016/j.wneu.2019.10.018. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2019 Elsevier Inc. All rights reserved.
Title page
Manuscript title: Pseudohypoxic Brain Swelling: report of 2 cases and introduction of the Lentiform Rim Sign as Potential MRI Marker
Running title: Role of imaging in PHBS/PIHV The full names and order of all authors: Houman Sotoudeh, M.D.1*, Philip R. Chapman, M.D.1, Ehsan Sotoudeh M.D.2, Aparna Singhal, M.D.1, Gagandeep Choudhary, M.D.1, Omid Shafaat, M.D.4
1. Department of Neuroradiology and Neurology, University of Alabama at Birmingham (UAB), 619 19th St S, Birmingham, AL, USA 35294
2. Department of Neuroradiology and Neurology, University of Alabama at Birmingham (UAB), 619 19th St S, Birmingham, AL, USA 35294 3. Department of Surgery, Iranian Hospital in Dubai, P.O.BOX: 2330, Al-Wasl Road, Dubai, UAE, Dubai 2330, United Arab Emirates.
4. Department of Radiology and Interventional Neuroradiology, Isfahan University of Medical Sciences, Isfahan, Iran Contact information of all co-authors: Houman Sotoudeh, M.D.: Department of Neuroradiology, University of Alabama at Birmingham (UAB); 619 19th St S, Birmingham, AL, USA 35294, JTN 333. Tel: 001(205) 8018750, office 43933 Email: [email protected]; ORCID ID: 0000-0002-5510-7062 Philip R. Chapman, M.D.: Department of Neuroradiology and Neurology, University of Alabama at Birmingham (UAB), 619 19th St S, Birmingham, AL, USA 35294 Email: [email protected]; ORCID ID: 0000-0002-9296-5672 Ehsan Sotoudeh M.D.: Department of Surgery, Iranian Hospital in Dubai, P.O.BOX: 2330, AlWasl Road, Dubai, UAE, Dubai 2330, United Arab Emirates. Email: [email protected]; ORCID ID: 0000-0002-4918-8230 Aparna Singhal, M.D.: Department of Neuroradiology, University of Alabama at Birmingham (UAB); 619 19th St S, Birmingham, AL, USA 35294 Email: [email protected];
Gagandeep Choudhary, M.D.: Department of Neuroradiology, University of Alabama at Birmingham (UAB); 619 19th St S, Birmingham, AL, USA 35294; Email: [email protected] Omid Shafaat, M.D.: Department of Radiology and radiological Sciences, Isfahan University of Medical Sciences, Hezar Jarib St, Isfahan, Iran, P.O. Box:8174673461, ORCID ID: 0000-00018793-7901
*Corresponding Author: Houman Sotoudeh, MD Assistant Professor of Neuroradiology and Neurology, Department of Neuroradiology, University of Alabama at Birmingham (UAB); 619 19th St S, Birmingham, AL, USA 35294, JTN 333. Tel: 001(205) 801-8750, office 43933 Email: [email protected]
Total number of tables and figures: Tables: 0, Figures: 4 Conflict of Interest: None Funding: None Keywords: Pseudohypoxic brain swelling; intracranial hypotension; venous cerebral congestion; postoperative intracranial hypotension; venous congestion; magnetic resonance imaging; neuroradiology
Sotoudeh 1
Pseudohypoxic Brain Swelling: report of 2 cases and introduction of the Lentiform Rim Sign as Potential MRI Marker
2 3 4
Abstract
5
Background: A rare but important complication related to otherwise uneventful brain and spine
6
surgery is becoming more recognized and more frequently reported in the medical literature.
7
This has been variably labelled as pseudohypoxic brain swelling (PHPS) or postoperative
8
hypotension-associated venous congestion (PIHV). This poorly understood condition occurs in
9
the setting of surgical intervention and is thought to be related to CSF leak or evacuation,
10
decreased intracranial pressure, and subsequent development of deep venous congestion
11
affecting the basal ganglia, thalami, and cerebellum. Clinically, patients may have global
12
neurologic deficit and outcomes range from full recovery to vegetative state or death. The
13
imaging correlate includes atypical edema, infarction, or hemorrhage and can overlap the
14
appearance of diffuse hypoxic injury, for which this condition can be mistaken both clinically
15
and radiologically. While this deep brain tissue edema can be associated with other signs of CSF
16
hypotension such as dural thickening, brain sagging, and cerebellar herniation, it can be isolated,
17
making the diagnosis challenging.
18
Case Description: We present 2 cases of unexpected clinical deterioration occurring in patients
19
with otherwise uncomplicated neurosurgery, one with craniotomy and the other with lumbar
20
spine intervention. Both patients exhibit similar appearing edema in the deep gray structures on
21
postoperative MRIs. In addition to reviewing the prior literature and imaging findings, we
22
evaluate the imaging findings to determine if there are unique features or signatures that might
23
allow differentiation of PHBS from hypoxic-ischemic encephalopathy.
24
Conclusion: The lentiform rim sign can be helpful for differentiation of PHBS versus hypoxic-
25
ischemic encephalopathy.
26 27
Keywords: Pseudohypoxic brain swelling; intracranial hypotension; venous cerebral congestion;
28
postoperative intracranial hypotension; venous congestion; magnetic resonance imaging;
29
neuroradiology 1
Sotoudeh 30 31
Introduction
32
A rare but important complication related to otherwise uneventful brain and spine surgery is
33
becoming more recognized and more frequently reported in the medical literature. This has been
34
variably labelled as pseudohypoxic brain swelling (PHBS) or postoperative hypotension-
35
associated venous congestion (PIHV).
36
described after uncomplicated brain surgery that utilized vacuum assisted CSF drainage 1. This
37
condition has also been reported after spinal surgery 2. The most common presentation of
38
PHBS/PIHV is an unexpected postoperative alteration of consciousness, seizure, and brainstem
39
dysfunction
40
related to stroke or occult hypoxic/ischemic event. The physiopathology of PHBS is still
41
controversial but it appears that rapid surgical drainage of CSF or CSF leak during surgery
42
causes sudden intracranial hypotension, brain stem sagging, venous congestion and secondary
43
venous ischemia or infarction because of shear forces involving the main intracranial deep
44
venous structures 2-9.
2-5
The authors prefer PHBS. The condition was first
. Clinically, patients are most often considered to have acute neurologic deficit
45 46
Radiologically, the findings include abnormal hypodensity (CT) or abnormal signal intensity
47
(MRI) involving the thalami, basal ganglia and cerebellum. These imaging findings reflect the
48
acute venous congestion and edema that occurs preferentially in these structures. The findings
49
on CT or MRI can suggest atypical arterial stroke or hypoxic-ischemic encephalopathy. However
50
vascular imaging e.g., MR angiography (MRA) and CT angiography (CTA) generally fail to
51
demonstrate pathologic findings
52
vasculature, hypoperfusion of basal ganglia, thalami, cerebellum, and telencephalon has been
53
reported in some patients using perfusion imaging 2. The bilateral symmetric involvement of the
54
deep gray structures on CT and MRI overlaps the appearance of deep venous thrombosis and
55
venous infarction. However, no venous thrombosis or obstruction has been identified. 2, 10-16.
2, 5, 8
. Despite unremarkable morphology of the brain
56 57
Diagnosis of PHBS is challenging. It is relatively rare but is becoming more recognized as case
58
reports and case series are being published. The clinical and radiologic findings are ultimately
59
nonspecific and many cases are considered to represent occult hypoxic/ischemic event. . In this
60
manuscript, we present 2 additional cases of PHBS, including the clinical presentation and 2
Sotoudeh 61
radiological findings in each case as well as a review of the literature. We also introduce a
62
potentially useful MRI marker: peripheral rim of T2/FLAIR hyperintensity along the lentiform
63
nuclei (Lentiform Rim Sign).
64 65 66 67
Case 1
68
An 81-year-old female with diabetes mellitus, atrial fibrillation, and hypertension presented with
69
exacerbation of back pain and radiculopathy and was found to have segmental lumbar stenosis.
70
The patient subsequently underwent lumbar spine surgery consisting of L3-L5 decompression
71
with internal fixation/fusion. The surgical procedure took approximately 3 hours and no
72
complications were noted during the procedure. A durotomy was not performed and there was no
73
specific finding during surgery to indicate possible CSF leak. Immediately after the surgery, the
74
patient experienced new onset of seizure activity that was treated with propofol. To exclude
75
brain infarction, the patient initially underwent brain and neck CT angiogram (CTA) and CT
76
perfusion (CTP) which were unremarkable. There was no large vessel occlusion, perfusion
77
abnormality, or evidence of intracranial hemorrhage. EEG demonstrated rhythmic appearing 1-2
78
Hz generalized sharp waves which improved with increased propofol. Although the clinical
79
presentation was concerning for hypoxic brain injury, the intraoperative record did not indicate
80
any prolonged periods of hypotension, and one episode of hypotension during a transient episode
81
of seizure was not severe or long lasting. There were no documented hypoxic events during
82
surgery and intubation procedure was uneventful.
83
Follow-up CT scan one day after the first seizure demonstrated diffuse brain edema with
84
diffuse effacement of cerebral sulci and generalized white matter hypodensity (Fig 1 A).
85
Subsequent MRI showed abnormal increased T2/fluid-attenuated inversion recovery (T2/FLAIR)
86
signal intensity in caudate heads, globous pallidum, putamen, and thalami bilaterally. Also noted
87
was a conspicuous rim of T2/FLAIR hyperintense signal lateral and inferomedial to the lentiform
88
nuclei (Fig 1 B and C arrows). There was minimal abnormal FLAIR hyperintensity in the
89
cerebellar hemispheres (Fig 1 D). Diffusion weighted images (DWI) showed no diffusion
90
restriction to indicate completed infarction or hypoxic-ischemic encephalopathy (Fig 1 E). The 3
Sotoudeh 91
patient’s condition improved after admission to intensive care unit. Follow-up brain CT 3 days
92
later showed complete resolution of diffuse brain edema (Fig 1 F). Ultimately the patient
93
recovered and transferred to skilled nursing facility with persistent cognitive deficits and
94
limitations in activities of daily living.
95 96
Case 2
97
A 72-year-old man with unremarkable past medical history presented with new onset of gait
98
instability. Initial CT scan of the head demonstrated a right-sided subdural hematoma associated
99
with mass effect and mild midline shift (Fig 2 A). On the second day of hospitalization, a right
100
frontal craniotomy and subdural evacuation was performed. In recovery, the patient developed
101
new-onset seizure activity that progressed to intractable status epilepticus. Despite extensive
102
medical regimen, status epilepticus continued and patient was ultimately placed into a medically
103
induced coma. No episode of hypotension was noted during the initial surgery or postoperative
104
period. Post-surgical brain CT showed interval development of bilateral but asymmetric
105
hypodensity in the lentiform nuclei (Fig 2 B). Subsequent MRI one day after surgery showed
106
T2/FLAIR hyperintense signal (Fig 2 C and D), diffusion restriction on DWI (Fig 2 E and F) and
107
petechial hemorrhagic changes (Fig 2 G) in lentiform nuclei. A prominent rim of T2/FLAIR
108
hyperintense signal was noted lateral and inferomedial to lentiform nuclei (Fig 2 C and D
109
arrows). On postcontrast T1 sequence no abnormal enhancement was noted (Fig 2 H). Attempts
110
to stop continuous midazolam resulted in recurrence of status epilepticus. The patient
111
subsequently developed methicillin-resistant staph aureus (MRSA) pneumonia and died.
112 113 114
Discussion and review of literature
115
PHBS is a rare condition often occurring after an uneventful brain or spinal surgical procedure
116
that can result in abrupt neurologic decline, new onset of seizure, brainstem dysfunction and can
117
lead to vegetative state or death
118
PHBS have been reported in English literature 9. The pathophysiology is poorly understood and
119
may not be completely elucidated. Most authors suggest that the phenomenon is governed by the
120
Monro-Kellie doctrine, which helps define the complex relationship between intracranial
1, 2, 8
. Based on our review of the current literature 24 cases of
4
Sotoudeh 121
pressure, CSF volume and cerebral perfusion. Presumably, a rapid reduction in CSF pressure or
122
volume during surgical procedure of the brain or spine can initiate a cascade of events including
123
inferior descent of the brain stem and compensatory increase in cerebral blood volume/venous
124
congestion. Venous congestion and inferior sagging cause shearing force over the vein of Galen
125
at the tentorium, venous congestion of deep brain structures and finally venous hemorrhagic
126
infarction in deep brain structures
127
inappropriate dural repair and suction of large CSF volume have been reported as the risk factors
128
for this condition.1, 4, 5, 8. Application of subdural or subgaleal suction has been implicated in
129
some cases as the potential causative event. PHBS has been described after extradural and
130
epicranial CSF drainage after craniotomy, spinal surgery and decompression of hydrocephalus 4.
3, 7-9
. Perioperative volume depletion, surgical position,
131 132
The most common presentation of PHBS is brainstem dysfunction including altered mental
133
status, seizure, bradycardia, hypotension and cardiac arrest 4, which presents on imaging as
134
hypodensity (CT) and T2/FLAIR hyperintense signal (MRI) of basal ganglia, thalami and
135
cerebellum with diffuse brain swelling and effacement of cerebral sulci
136
findings ranging from normal to patchy restriction to large homogeneous zones of restriction. 2
137
Hemorrhage can occur as well, typically petechial type hemorrhage. 2 The imaging findings can
138
also overlap and mimic deep venous thrombosis
139
MRA) are usually normal but relative hypoperfusion of basal ganglia and telencephalon has been
140
described 1, 2. There is no definite treatment for this condition but intrathecal saline infusion has
141
been tried 17.
3, 5, 9
2, 5
. DWI demonstrates
. Anatomic vascular imaging (CTA and
142 143
The main differential diagnosis of PHBS is the much more common hypoxic-ischemic
144
encephalopathy which can present with the similar abnormal radiologic findings of basal ganglia
145
and thalami. At this time, there is no definite radiologic finding to differentiate these two
146
conditions based on CT or MRI. Upon review of our cases and previously published cases of
147
PHBS, we observed a prominent hyperintense rim of abnormal T2/FLAIR signal along the
148
lateral and inferomedial border of the lentiform nuclei in some case. To our knowledge, this
149
finding is unusual and not prominent in other pathologies of the basal ganglia presenting acutely.
150
We refer to this finding as the “lentiform rim sign” and found it to be conspicuous in both of the
151
current cases. We propose that this sign might be a potential useful MRI marker for this 5
Sotoudeh 152
condition. By definition, the signal of the “lentiform rim sign” must be higher than the lentiform
153
nucleus itself and the adjacent white matter on T2 and FLAIR sequences. We have
154
retrospectively observed a similar sign in some of previously published reports, although
155
conclusions are difficult in that only a few images are reviewable. Yokota et al. described a case
156
of PHBS after craniotomy for clipping the anterior communicating artery aneurysm. Their case
157
demonstrated the “lentiform rim sign”
158
spinal surgery, at least one of which appeared to demonstrate the “lentiform rim sign” 2.
159
Dickinson et al. described a case of PHBS after spinal surgery with “lentiform rim sign” in the
160
right side and hemorrhagic changes of the left lentiform nucleus 8. Van roost et al. published the
161
FLAIR image of one of their patients (patient No 14) with PHBS which showed “lentiform rim
162
sign”. In one published case by Snyder et al. this sign was also present 18.
5
. Parpaley et al. described two cases of PHBS after
163 164
To describe the “lentiform rim sign”, the deep brain venous anatomy should be reviewed. The
165
venous drainage of deep brain structures is firstly done by the medullary veins. The medullary
166
veins from the caudate nucleus constitute the “caudate vein”. The medullary vein from the basal
167
ganglia and thalami join to build the “terminal vein”. The “caudate” and ‘terminal” veins join to
168
make the “thalamostriate vein”. The “septal vein” (which receives blood from the genu of the
169
corpus callosum, septum pellucidum, and the anterior part of the caudate nucleus)
170
and “thalamostriate” veins join to build the internal cerebral vein which then drains toward the
171
vein of Galen (Fig 3). CSF hypotension and sagging of the brain likely causes deviation of these
172
deep brain veins and secondary impairment of venous derange. This theory is supported by
173
selective edema of these deep brain nuclei. Venous congestion causes selective edema in
174
structures who drained by deep veins but not peripheral brain parenchyma, which is
175
mainly drained by superficial veins. Edema between these two different venous territories causes
176
the rim of T2/FLAIR hyper-signal intensity around the lentiform nuclei the “lentiform rim sign”.
177
In severe form, these venous drainage impairments, can cause elevated venous pressure and
178
secondary venous infarction of the deep brain nuclei with diffusion restriction although diffusion
179
restriction is not as severe as arterial infarction. These venous infarcts tend to be hemorrhagic in
180
comparison to arterial infarction.
181
6
Sotoudeh 182
In
the
most
common differential diagnosis
of
this
condition,
the
hypoxic-ischemic
183
encephalopathy, in the other hand, the reason of selective involvement of deep structures is
184
higher metabolic rate of deep nuclei in comparison to peripheral white matter. In this hypoxic-
185
ischemic injury of deep nuclei, the edema is not dominant at least in acute phase so the rim of
186
T2/FLAIR hyper-signal intensity around the lentiform nuclei is not prominent (Fig 4).
187 188
A similar radiologic finding “lentiform fork sign” has been described in renal failure, uremia,
189
methanol toxicity, metabolic acidosis, mitochondrial disorders and metformin encephalopathy
190
19-27
191
involving the external capsule, external medullary lamina, internal medullary lamina and
192
internal capsule with trident morphology. In our cases, we did not observe the classical trident
193
morphology of “lentiform fork sign”. None of our cases had documented uremia, metabolic
194
acidosis or other underlying etiologies of lentiform fork sign.
. The “lentiform fork sign” represents edema and produces T2/FLAIR signal abnormality
195
Accuracy of “lentiform rim sign” for diagnosis the PHBS versus ischemic hypoxic
196
encephalopathy cannot be evaluated in this manuscript given rare incidence of PHBS. Further
197
investigation might confirm the utility of this finding.
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Both of our cases presented by seizure. Seizures shortly after spinal surgeries have been reported
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in few cases mainly in association with cerebral and cerebellar hemorrhages. It has been
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suggested that rapid decrease of CSF pressure secondary to durotomy causes acute occlusion of
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bridging veins and secondary cerebral/cerebellar hemorrhages. Finally, the exposure of brain to
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hemoglobin (subdural hematoma), which has proconvulsive effects, is likely the reason for
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seizure28, 29 . We didn’t detect evidence of intracranial hemorrhages in our first case and seizure
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in this case was likely because of different process such as brain congestion. Although our
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second case had subdural hematoma before craniotomy but given development of abnormal
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signal/density, congestion and hemorrhages in the lentiform nuclei (which are not common
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imaging findings after seizure) we believe seizure in this case was also because of venous
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congestion and brain edema.
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Conclusion
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PHBS is a rare but important complication related to otherwise uneventful brain and spine
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surgery and is becoming more recognized and more frequently reported in the medical literature. 7
Sotoudeh 213
This poorly understood condition occurs in the setting of surgical intervention and is thought to
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be related to CSF leak or evacuation, decreased intracranial pressure, and subsequent
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development of deep venous congestion affecting the basal ganglia, thalami, and cerebellum.
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The clinical and imaging features can overlap those of hypoxic/ischemic event. This entity
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should be considered in the differential of any patient that undergoes acute postoperative
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neurologic decline and has atypical edema, mass effect, or hemorrhage involving the deep gray
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structures. As we report, the presence of a peripheral rim of edema along the lentiform nuclei,
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the “lentiform rim sign “may represent a potential marker for this condition.
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Conflict of interest
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All authors declare that the research was conducted in the absence of any commercial or
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financial relationships that could be construed as a potential conflict of interest.
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Author Contributions
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HS, and PC contributed conception and design of the study; HS organized the database; HS, OS,
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PC, and ES wrote the first draft of the manuscript. AS and GC helped us in revising and editing
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the final manuscript. All authors contributed to manuscript revision, read and approved the
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submitted version.
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Funding
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This research did not receive any specific grant from funding agencies in the public, commercial,
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or not-for-profit sectors.
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References
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Figure Legends
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Fig 1. Non-contrast CT, one day after surgery, shows diffuse brain edema with effacement of
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sulci and white matter hypodensity (A). MRI one day after surgery (B-E). On FLAIR and T2
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sequence, there is mildly increased signal in lentiform nuclei, caudate and thalami in association
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with a rim of hyper signal intensity lateral and inferomedial to the lentiform nuclei (B and C).
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Minimal FLAIR hyper signal intensity in the cerebellum (D). No diffusion restriction to suggest
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infarction (E). Non-contrast CT 3 day later shows complete interval resolution of brain edema
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(F).
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Fig 2. Initial brain CT shows right hemispheric subdural hematoma with mass effect and mild
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midline shift-- normal density of basal ganglia (A). Post-surgical brain CT 1 day after the initial
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CT shows postsurgical changes, right frontal pneumocephalus, and resolution of midline shift but
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with interval development of hypodensity in basal ganglia (B). MRI 1 day after surgery (C-
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H). T2 and FLAIR hyper signal intensity in basal ganglia with the rim of hyper signal intensity
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lateral and inferomedial to the lentiform nuclei (arrows C and D). Diffusion restriction in the
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lentiform nuclei, which is evident on diffusion-weighted imaging (DWI) and apparent diffusion
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coefficient (ADC) map (E and F). Hemorrhagic changes in the lentiform nuclei causing
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susceptibility artifact on SWI sequence (G). No visible abnormal enhancement on post-contrast
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T1 sequence but with engorged vessels in lentiform nuclei, more prominent on the left side
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which is felt to be engorged veins (arrows H).
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Fig 3. Anatomic configuration of deep brain venous systems. SV: Septal Vein. C: Caudate Vein.
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T: Terminal Vein. TS: Thalamostriate Vein. Red circle: Vein of Galen at the level of the
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tentorium which is believed the location of venous shearing in PHBS/PIHV secondary to a rapid
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decrease of intracranial pressure.
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Fig 4. Application of “lentiform rim sign”. Top row a case of PHBS/PIHV (A-C). A rim of
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T2/FLAIR hyper signal intensity lateral and inferomedial to the lentiform nuclei. No significant
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diffusion restriction of deep brain structure. Bottom raw a case of hypoxic-ischemic
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encephalopathy (D-F). No “lentiform rim sign”. More prominent diffusion restriction of deep
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brain structures.
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11
Abbreviations PHBS (psudohypoxic brain swelling); PIHV (postoperative intracranial hypotension-associated venous congestion); CSF (cerebrospinal fluid); CT (computed tomography); MRI (magnetic resonance imaging); CTA (CT angiography); CTP (CT perfusion); T2/FLAIR (T2/fluidattenuated inversion recovery); DWI (diffusion-weighted imaging); ADC (apparent diffusion coefficient)
Conflict of interest All authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.