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Neuroradiolog y/Head and Neck Imaging • Original Research

Kranz et al.
Imaging Signs of SIH

Neuroradiology/Head and Neck Imaging


Original Research

Time-Dependent Changes
in Dural Enhancement
Associated With Spontaneous
Intracranial Hypotension
Peter G. Kranz1 OBJECTIVE. The objective of our study was to determine whether the presence of in-
Timothy J. Amrhein dividual imaging signs of spontaneous intracranial hypotension (SIH) is correlated with in-
Kingshuk Roy Choudhury creasing duration of headache symptoms. Of particular interest is the relationship of symp-
Teerath Peter Tanpitukpongse tom duration to dural enhancement because it is the most commonly identified imaging sign
Linda Gray in patients with SIH.
MATERIALS AND METHODS. Eighty-nine patients with SIH who underwent pre-
Kranz PG, Amrhein TJ, Choudhury KR, treatment brain MRI and total-spine CT myelography and whose medical record included
American Journal of Roentgenology 2016.207:1283-1287.

­Tanpitukpongse TP, Gray L data on the duration of clinical symptoms were included in this cross-sectional retrospective
study. Brain imaging was reviewed for the presence of dural enhancement, brain sagging, and
the “venous distention” sign. CT myelograms were assessed for CSF leak. If present, a leak
was subcategorized as a high-flow or low-flow leak. Differences in headache duration be-
tween subjects with and those without individual imaging signs were compared.
RESULTS. Subjects without dural enhancement on brain MRI had a longer average du-
ration of symptoms than those with dural enhancement present (average symptom duration:
45.3 ± 59.0 [SD] vs 15.1 ± 33.0 weeks, respectively; p = 0.002). No difference in symptom du-
ration was observed between subjects whose MRI studies showed and those whose MRI stud-
ies did not show brain sagging (p = 0.10) or the venous distention sign (p = 0.21). The pres-
ence of a CSF leak on CT myelography was not associated with symptom duration (p = 0.56)
except in the subgroup of patients with low-flow leaks.
CONCLUSION. Increasing symptom duration in SIH is associated with decreased
prevalence of abnormal dural enhancement on brain MRI. Because dural enhancement is
considered a hallmark imaging feature of this condition, its absence may exacerbate the prob-
lem of underdiagnosis in chronic cases of SIH.

pontaneous intracranial hypo- tempting to establish the diagnosis of SIH be-

S tension (SIH) is an increasingly


recognized cause of chronic
headache. Diagnosis often de-
cause other imaging markers of SIH—such as
MRI evidence of brain sagging, MRI evidence
of the “venous distention” sign, and CT myelo-
pends on the detection of characteristic im- graphic evidence of CSF leak—are found less
aging abnormalities on brain MRI, the most commonly than dural enhancement and are
Keywords: brain MRI, CSF leak, CT myelography, common of which is diffuse, smooth dural therefore less reliable indicators of the disease
spontaneous intracranial hypotension
contrast enhancement on contrast-enhanced [4]. The absence of dural enhancement may
DOI:10.2214/AJR.16.16381 imaging [1, 2]. This enhancement is thought therefore increase the likelihood of misdiag-
to represent a physiologic response to CSF nosis, an already common problem in patients
Received March 14, 2016; accepted after revision volume loss whereby intracranial vascular with SIH [5]. Identifying which patients are
May 28, 2016. structures (including those within the dura) more likely to show variability in the presence
1
All authors: Department of Radiology, Duke University
are forced to dilate to compensate for the to- of dural enhancement is therefore important.
Medical Center, Box 3808, Durham, NC 27710. Address tal intracranial volume lost as a result of spi- One potential clue to the variability in du-
correspondence to P. G. Kranz (peter.kranz@duke.edu). nal CSF leakage [3]. ral enhancement may lie with the mounting
Although highly characteristic of SIH and evidence suggesting that SIH is not a static
AJR 2016; 207:1283–1287 explainable by the physiologic principles ac- process but, rather, is one in which the un-
0361–803X/16/2076–1283
companying CSF leakage, dural enhancement derlying physiology changes with time. For
is not present in approximately 20% of patients example, CSF pressure, which is often found
© American Roentgen Ray Society with SIH [4]. This fact is problematic when at- to be abnormally low in patients with the dis-

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Kranz et al.

A B C
Fig. 1—57-year-old man with positional headache. Brain imaging reveals common imaging abnormalities associated with spontaneous intracranial hypotension.
A, Abnormal diffuse, smooth dural enhancement (arrowheads) is seen on axial contrast-enhanced T1-weighted image.
B, MR image shows “venous distention” sign (arrow), whereby borders of dominant transverse venous sinus are convex, rather than normal concave configuration, and
result in rounded appearance of sinus.
C, MR image shows brain sagging with downward sloping of third ventricular floor, narrowing of suprasellar cistern, and descent of mammillary bodies (arrow) to level of
dorsum sella.
American Journal of Roentgenology 2016.207:1283-1287.

ease, has been shown to rise with time even by Schievink et al. [8] and whose pretreatment icate of added qualification in neuroradiology and
if CSF leakage is ongoing [6]. Similarly, brain MRI studies were available in our institu- extensive experience in treating patients with SIH.
clinical symptoms often change with time as tion’s PACS were identified. All subjects under- The presence of principal brain MRI signs of
well, and many patients experience a reduc- went CT myelography as part of their workup [9]. SIH (i.e., dural enhancement, brain sagging, and
tion in the stereotypical orthostatic compo- The duration of each patient’s clinical symptoms the venous distention sign) (Fig. 1) was assessed
nent of their headaches, which may evolve was determined from the clinical history record- using previously described criteria [4]. Dural en-
into nonorthostatic headaches [7]. Whether ed in the electronic medical record; assessment of hancement was graded as follows: absent, abnor-
the imaging features of SIH, including dural the duration of headache symptoms, including a mal enhancement without dural thickening, or ab-
enhancement, also change with time remains specific starting date if possible, is part of the his- normal enhancement with dural thickening. The
an unexplored question. tory obtained from patients at our institution us- presence of pituitary engorgement was not as-
The primary purpose of this investigation ing a standardized pretreatment questionnaire. sessed because we think that this sign is too sub-
was to determine whether dural enhance- Ten of these 99 patients (10%) were excluded be- jective for reproducible analysis and is of lesser
ment on MRI in patients with SIH is corre- cause information about the duration of their clin- diagnostic significance in SIH.
lated with an increasing duration of clinical ical symptoms was not available in the medical CT myelograms were designated as showing
headache symptoms. We also sought to de- record, resulting in a final study cohort of 89 sub- evidence of CSF leak if contrast material was seen
termine whether other imaging signs of SIH jects. Of these remaining subjects, 83 (93%) un- outside the thecal sac. Leaks were further subcat-
such as MRI evidence of brain sagging, MRI derwent pretreatment brain MRI performed with egorized as high-flow leaks or low-flow leaks us-
evidence of the venous distention sign, and and without IV contrast material, and six (7%) un- ing the following previously described criteria: A
CT myelographic evidence of CSF leak vary derwent unenhanced brain MRI only. Brain MRI leak was defined as a high-flow leak if leaked con-
with symptom duration. protocols varied on a case-by-case basis because trast material was seen spreading over more than
almost all pretreatment brain imaging examina- one vertebral level and as a low-flow leak if leaked
Materials and Methods tions were performed at outside centers; howev- contrast material was seen spreading over one ver-
This investigation is a retrospective cross-sec- er, the brain MRI examinations typically included tebral level or less [10].
tional study of patients with SIH. Subjects were axial fast spin-echo (FSE) unenhanced and con-
identified from a database search of patients with trast-enhanced T1-weighted images and either Statistical Analysis
SIH treated at our institution between January FSE or spoiled gradient-recalled coronal contrast- Differences in symptom duration between sub-
2006 and October 2014 that was performed as part enhanced T1-weighted images. jects for whom individual brain MRI signs of SIH
of a separate investigation examining the relation- were present or absent were compared using a
ship between the imaging signs of SIH and CSF Image Analysis two-sided t test. For subjects with abnormal du-
pressure [4]. This study was approved by our local The imaging studies were reviewed by a board- ral enhancement, differences in symptom duration
institutional review board and is compliant with certified radiologist who was in the second year of based on the degree of dural abnormality were
HIPAA regulations. a neuroradiology fellowship to determine if the im- compared using the Mann-Whitney test. For CT
aging signs of SIH were present or absent. If the myelographic findings, a two-sided t test was used
Subjects imaging findings for a patient were thought to be to compare symptom duration between subjects
A total of 99 subjects who met the crite- equivocal, the imaging studies were reviewed by a with a CSF leak and those without a CSF leak.
ria for SIH according to the criteria proposed second board-certified radiologist who has a certif- A one-way ANOVA was used to further compare

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Imaging Signs of SIH

200.0 t test p = 0.002 200.0 t test p = 0.010 200.0 t test p = 0.021


Symptom Duration (wk)

Symptom Duration (wk)

Symptom Duration (wk)


50.0 50.0 50.0

20.0 20.0 20.0

5.0 5.0 5.0

2.0 2.0 2.0


1.0 1.0 1.0
0.5 0.5 0.5

Absent Present Absent Present Absent Present


Dural Enhancement Brain Sagging Venous Distention Sign

A B C
Fig. 2—Box-and-whisker plots comparing symptom duration in patients with spontaneous intracranial hypotension (SIH) and brain MRI signs suggestive of SIH. Upper
and lower lines of boxes show first and third quartiles, respectively. Middle lines in boxes show median. Whiskers show minimum and maximum values, excluding
outliers.  = outliers.
A–C, Box-and-whisker plots show symptom duration in SIH patients with and in those without brain MRI signs of SIH. Brain MRI signs of SIH that were evaluated include
dural enhancement (A), brain sagging (B), and “venous distention” sign (C).

symptom duration on the basis of leak subtype nal study cohort, the mean age was 47.7 ± hancement was associated with a longer du-
(i.e., no leak, high-flow leak, low-flow leak). The 13.9 (SD) years (range, 18–83 years). Sixty ration of symptoms than the presence of dural
Fisher exact test was used to compare the preva- patients (67%) were female subjects, and 29 enhancement (average symptom duration,
American Journal of Roentgenology 2016.207:1283-1287.

lence of dural enhancement in patients who had patients (33%) were male subjects. A prior 45.3 ± 59.0 vs 15.1 ± 33.0 weeks, respectively;
received a prior epidural blood patch with that in blood patch had been attempted in 36 sub- p = 0.002). For subjects with abnormal dural
patients who had not. Analysis was performed us- jects (40%), whereas 53 subjects (60%) had enhancement, a subgroup analysis based on
ing statistical and computing software (R, version not been treated previously. The prevalence the degree of abnormality (i.e., abnormal en-
3.0.2, The R Foundation); p values of < 0.05 were of dural enhancement was not significant- hancement alone vs abnormal enhancement
considered to be statistically significant. ly different in the subgroup of patients who plus dural thickening) was not associated
had received prior blood patch (89%) com- with a significant difference in symptom du-
Results pared with the subgroup of those who had ration (p = 0.58). No difference in symptom
The mean duration of headache symptoms not (77%) (p = 0.25). duration was found between subjects showing
was 20.5 months (range, 9 days–240 months; Comparisons of symptom duration in pa- and those not showing brain sagging on brain
SD, 40.0 months). The distribution was tients with and those without brain MRI signs MRI (p = 0.10) or between subjects showing
skewed, however, with subjects having symp- of SIH are shown in Figure 2. Significant dif- and those not showing the venous distention
tom duration of less than 1 year accounting ferences in symptom duration were observed sign on brain MRI (p = 0.21).
for 67% of the population. As a result, the between subjects with dural enhancement on Of the 89 subjects, 37 (42%) showed no
median duration of symptoms was only 6.0 brain MRI compared with those without du- CSF leak, 45 (51%) had a high-flow leak, and
months (95% CI, 3.5–8.0 months). In the fi- ral enhancement. The absence of dural en- seven (8%) had a low-flow leak on CT my-

200.0 t test p = 0.56 200.0 ANOVA p = 0.003


Symptom Duration (wk)

Symptom Duration (wk)

50.0 50.0

20.0 20.0

5.0 5.0

2.0 2.0
1.0 1.0
0.5 0.5

Absent Present No Leak High-Flow Leak Low-Flow Leak


Leak on CT Myelography CT Myelography Findings

A B
Fig. 3—Box-and-whisker plots comparing symptom duration and CT myelography findings in patients with spontaneous intracranial
hypotension. Upper and lower lines of boxes show first and third quartiles, respectively. Middle lines in boxes show median. Whiskers
show minimum and maximum values, excluding outliers.  = outliers.
A, Box-and-whisker plot shows symptom duration in patients with and in those without CSF leak on CT myelography.
B, Box-and-whisker plot shows symptom duration in patients with CSF leak on CT myelography by subtype of CSF leak identified. Leak
was defined as high-flow leak if leaked contrast material was seen spreading over more than one vertebral level and as low-flow leak
if leaked contrast material was seen spreading over one vertebral level or less [10].

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Kranz et al.

elography. Comparisons of symptom dura- positional component of the headache alto- fects of CSF volume depletion over time and
tion related to CT myelographic findings are gether and transformation into chronic daily result in a decrease in the dilatation of blood
shown in Figure 3. Although there was no headache [7, 11]. The headache pattern may vessels within the dura, as necessitated by
overall difference in symptom duration be- evolve into a so-called “second-half-of-the- the Monro-Kellie doctrine. This decreased
tween patients with no leak and those with day” headache in which the orthostatic com- vasodilatation manifests as a decrease in du-
a leak (p = 0.56), there was a significant dif- ponent is evident only over a longer period of ral enhancement on MRI.
ference (p = 0.003) when the data were seg- time upright [12] despite ongoing CSF leak- Our investigation also found that the like-
mented by leak subtype. Based on a one-way age detectable on CT myelography. Thus, as lihood of finding a CSF leak on CT myelog-
ANOVA analysis, the duration of symp- the clinical symptoms become less clearly in- raphy was independent of symptom dura-
toms of subjects with high-flow leaks was dicative of a diagnosis of SIH, the likelihood tion except in patients with low-flow leaks.
shorter relative to baseline (i.e., the no-leak of suggestive imaging abnormalities may also Therefore, in general, it cannot be conclud-
group), but this difference was not statistical- decrease, further hindering diagnosis. ed that the decreased prevalence of dural en-
ly significant (p = 0.17). However, subjects The observation that the prevalence of du- hancement with time is caused by spontane-
with low-flow leaks were symptomatic 40.9 ral enhancement changes with time contrib- ous cessation of CSF leaks. With regard to
weeks (mean) longer than baseline (no-leak utes to the growing body of evidence that the the low-flow leaks, it is possible that some
group), a difference that was highly statisti- physiology associated with SIH is not static of the subjects in our study cohort had leaks
cally significant (p = 0.01). and that various compensatory mechanisms that initially started out as more rapid but
may contribute to variations in the clinical that slowed over time because of partial con-
Discussion and imaging presentation of the condition tainment of the leak.
Our investigation shows that the dural over time. Defining these changes and how Because there is no single test that func-
enhancement seen in patients with SIH be- to detect them could lead to improvements in tions as the reference standard for the diag-
American Journal of Roentgenology 2016.207:1283-1287.

comes less prevalent over time after the onset the management of patients currently diag- nosis of SIH, the decreased prevalence of
of symptoms. The mean duration of headache nosed with SIH and could potentially lead to hallmark imaging signs such as dural en-
symptoms for subjects with dural enhance- a further broadening of the diagnostic crite- hancement poses challenges for diagnosing
ment present was 15.1 weeks compared with ria as more variation is recognized. SIH in patients who present for evaluation
45.3 weeks for those with no dural enhance- Evidence of physiologic compensatory later in the course of their symptoms. This
ment. Conversely, other less common imag- mechanisms in SIH has been suggested by diagnosis is doubly challenging if the clini-
ing findings including brain sagging and the several prior observations. First, SIH is as- cal symptoms also are changing with time.
venous distention sign do not show similar sociated with identifiable anatomic changes It is possible, perhaps even likely, that some
time-dependent variability, but these signs in the caliber of the veins in the intracrani- patients diagnosed with other chronic head-
are less frequently found in SIH overall. The al compartment and within the spinal canal; ache syndromes such as new daily persistent
presence or absence of a CSF leak on CT my- these changes are consistent with the tenets headache actually suffer from an occult pre-
elography was not associated with differences of the Monro-Kellie doctrine that requires sentation of SIH. These patients may exhib-
in symptom duration in general, with the ex- the vascular space to expand as the CSF vol- it different clinical or imaging features than
ception of the low-flow subtype of leaks. ume decreases [3]. Second, CSF pressure subjects with so-called “classic,” or stereo-
These findings have implications when is only weakly correlated with other objec- typical, presentations of SIH. Defining how
considering the diagnosis of SIH, particular- tive indicators of CSF volume depletion such broad the disease spectrum may be and de-
ly in patients with symptoms of longer dura- as brain imaging findings of venous disten- fining how to best establish the diagnosis in
tion. Dural enhancement is the single most tion and brain sagging and is not significant- these patients remain important avenues for
common imaging sign found in patients with ly correlated with dural enhancement or CT future investigation.
SIH [4] and therefore is often relied on as a myelographic evidence of CSF leakage [4]. Limitations of this study include our loca-
major indicator of the condition. Failure to These observations point to the influence of tion at a tertiary referral center, which could
account for the time-dependent decrease in compensatory physiologic processes that can have the potential to introduce spectrum
the prevalence of dural enhancement could help maintain CSF pressure in some patients bias. However, most of our subjects had not
potentially contribute to underdiagnosis, despite ongoing CSF volume loss. Finally, been treated elsewhere previously, and thus
which is already a known problem [5]. Spe- CSF pressure in patients with SIH shows a our sample would likely be representative of
cifically, patients with chronic SIH whose statistically significant increase with the in- SIH patients in general. We do not have ret-
imaging studies no longer show dural en- creasing duration of symptoms indepen- rospective data regarding headache severi-
hancement would be less likely to be recog- dent of the presence or absence of CT my- ty, which could be a theoretic covariate that
nized as suffering from the condition. elographically detectable CSF leakage, again could change with time. However, there are
This problem of underdiagnosis could suggesting that the physiologic changes in- no data, to our knowledge, to suggest that the
be further compounded by the fact that the duced by SIH vary in a manner that is par- severity of headache influences the imaging
headache phenotype in SIH also can change tially time-dependent [6]. signs of SIH such as dural enhancement.
with chronicity, evolving from positional The observation of time-dependent chang- In conclusion, we found that dural en-
headaches into nonspecific headache symp- es in dural enhancement in this current inves- hancement is less likely to be present as
toms that are less stereotypical of the condi- tigation further reinforces this body of evi- symptom duration increases in patients with
tion. These changes may result in decreasing dence. Specifically, our results suggest that SIH. As a result, SIH may be less likely to be
headache severity or the disappearance of the compensatory mechanisms mitigate the ef- diagnosed accurately in patients with long-

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standing SIH given the importance placed on 56:1746–1748 Bousser MG, Goadsby PJ. Diagnostic criteria for
brain imaging in the diagnostic evaluation of 4. Kranz PG, Tanpitukpongse TP, Choudhury KR, headache due to spontaneous intracranial hypoten-
the condition. Further investigation of the Amrhein TJ, Gray L. Imaging signs in spontaneous sion: a perspective. Headache 2011; 51:1442–1444
time-dependent changes in the clinical pre- intracranial hypotension: prevalence and relation- 9. Kranz PG, Gray L, Taylor JN. CT-guided epidural
sentation and physiologic changes accompa- ship to CSF pressure. AJNR 2016; 37:1374–1378 blood patching of directly observed or potential
nying SIH is warranted. 5. Schievink WI. Misdiagnosis of spontaneous intracra- leak sites for the targeted treatment of spontaneous
nial hypotension. Arch Neurol 2003; 60:1713–1718 intracranial hypotension. AJNR 2011; 32:832–838
References 6. Kranz PG, Tanpitukpongse TP, Choudhury KR, 10. Kranz PG, Luetmer PH, Diehn FE, Amrhein TJ,
1. Pannullo SC, Reich JB, Krol G, Deck MD, Posner Amrhein TJ, Gray L. How common is normal ce- Tanpitukpongse TP, Gray L. Myelographic tech-
­
JB. MRI changes in intracranial hypotension. rebrospinal fluid pressure in spontaneous intra- niques for the detection of spinal CSF leaks in sponta-
Neurology 1993; 43:919–926 cranial hypotension? Cephalalgia 2015 Dec 17 neous intracranial hypotension. AJR 2016; 206:8–19
2. Fishman RA, Dillon WP. Dural enhancement and [Epub ahead of print] 11. Mokri B. Spontaneous CSF leaks: low CSF vol-
cerebral displacement secondary to intracranial 7. Mokri B. Spontaneous low pressure, low CSF vol- ume syndromes. Neurol Clin 2014; 32:397–422
hypotension. Neurology 1993; 43:609–611 ume headaches: spontaneous CSF leaks. H ­ eadache 12. Leep Hunderfund AN, Mokri B. Second-half-of-
3. Mokri B. The Monro-Kellie hypothesis: applica- 2013; 53:1034–1053 the-day headache as a manifestation of spontane-
tions in CSF volume depletion. Neurology 2001; 8. Schievink WI, Dodick DW, Mokri B, Silberstein S, ous CSF leak. J Neurol 2012; 259:306–310
American Journal of Roentgenology 2016.207:1283-1287.

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