N e u r o r a d i o l o g y / H e a d a n d N e c k I m a g i n g • R ev i ew

Hacein-Bey et al.
Neuroimaging of Pregnancy and Puerperium

Neuroradiology/Head and Neck Imaging

Review
Downloaded from www.ajronline.org by 125.167.98.100 on 01/14/18 from IP address 125.167.98.100. Copyright ARRS. For personal use only; all rights reserved

FOCUS ON:

Imaging of Cerebrovascular Disease

in Pregnancy and the Puerperium
Lotfi Hacein-Bey 1,2 OBJECTIVE. The purpose of this article is to review the unique physiologic changes
Panayiotis N. Varelas 3 that characterize pregnancy and the puerperium, some that substantially affect the cerebro-
John L. Ulmer4 vascular system. Conditions that can cause neurologic deterioration and share features with
Leighton P. Mark4 preeclampsia-eclampsia include postpartum angiopathy, reversible cerebral vasoconstriction
Kesav Raghavan5 syndrome, posterior reversible encephalopathy syndrome, and amniotic fluid embolism. Oth-
er conditions not specific to this patient group include cerebral venous thrombosis, cervicoce-
James M. Provenzale 6
phalic arterial dissection, ischemic stroke, and hemorrhagic stroke, which can pose specific
Hacein-Bey L, Varelas PN, Ulmer JL, Mark LP, diagnostic and therapeutic challenges.
Raghavan K, Provenzale JM CONCLUSION. Radiologists must be familiar with the imaging findings of cerebrovas-
cular complications and pathologic entities encountered during pregnancy and the puerpe-
rium. Ongoing improvements in understanding of molecular changes during pregnancy and
the puerperium and advances in diagnostic tests should allow radiologists to continue to make
important contributions to the care of this patient population.

C
erebrovascular abnormalities of
pregnancy and the puerperium are
increasingly recognized, as evi-
denced by data from the Nation-
Keywords: cerebrovascular, MRI, postpartum, wide Inpatient Sample. These data show that
pregnancy, stroke from 1994–1995 to 2006–2007 the frequency
DOI:10.2214/AJR.15.15059
of pregnancy-related stroke hospital admis-
sions during the postpartum period increased
Received May 29, 2015; accepted after revision 83% [1], reflecting improvements in diagnos-
September 13, 2015. tic tests and increased awareness and under-
1
standing of cerebrovascular abnormalities in
Department of Medical Imaging, Sutter Health,
1500 Expo Pkwy, Sacramento, CA 95815. Address
this patient population. Radiologists should be
correspondence to L. Hacein-Bey (lhaceinbey@yahoo.com). familiar with cerebrovascular conditions en-
countered in these young, typically previously
2
Department of Radiology, UC Davis Medical Center, healthy patients, who often experience rapid
Sacramento, CA.
clinical deterioration because delay in diagno-
3
Departments of Neurology and Neurosurgery, sis and treatment can have a substantial impact
Henry Ford Hospital, Detroit, MI. on patient care. Evaluation of these patients
usually starts with unenhanced CT, which has
4
Department of Radiology, Medical College of Wisconsin, high diagnostic accuracy in detecting hemor-
Milwaukee, WI.
rhage. However, normal CT findings can delay
5
Harvard Medical School, Boston, MA. diagnosis because of a low diagnostic yield for
subtle white matter changes and inability to as-
6
Department of Radiology, Duke University Medical sess the intracranial vasculature [2]. MRI and
Center, Durham, NC.
MR angiography are both excellent first- or
second-line diagnostic modalities for this pa-
AJR 2016; 206:26–38
tient population, having high diagnostic value
0361–803X/16/2061–26 without exposure to ionizing radiation. Cere-
bral angiography may be necessary to estab-
© American Roentgen Ray Society lish certain diagnoses or to provide therapy.
Radiologists have the opportunity to play an
important role in the care of women with cere-
brovascular abnormalities during pregnancy
and the puerperal period by effectively guid-
ing diagnostic evaluation and treatment by
communicating closely with fellow clinicians
within multidisciplinary teams, properly guid-
ing and monitoring advanced imaging tests,
counseling on the use of IV contrast media,
limiting radiation exposure to the mother and
fetus, and performing life-saving therapeutic
procedures in rare, select circumstances.
Physiologic Changes of Pregnancy
and the Puerperium
Pregnancy and the puerperium are charac-
terized by a unique physiologic environment,
into which much insight has been gained in re-
cent years [3]. Plasma and total blood volumes
increase during pregnancy and may cause
blood pressure to increase. At the same time,
a gradual increase in blood and tissue estro-
gen levels stimulates the production of clotting
factors, which may increase the risk of throm-
boembolism. Toward the end of pregnancy,
increased blood and tissue concentrations of
progesterone promote venous distensibility and
affect capillary permeability, leading to water
shifts. In the postpartum period, the abrupt de-
crease in estrogen levels combined with persis-

26 AJR:206, January 2016

 Neuroimaging of Pregnancy and Puerperium

TABLE 1: Differential Diagnosis of Cerebrovascular Conditions Encountered in Pregnancy and the Postpartum Period
Rapidity of Onset
of Symptoms and
Condition Time of Occurrence Signs Clinical Presentation Imaging Findings Cerebrovascular Findings
Eclampsia Second or third trimester Gradual Seizures Cerebral edema, Normal findings, arterial
ischemia, hemorrhage spasm
Downloaded from www.ajronline.org by 125.167.98.100 on 01/14/18 from IP address 125.167.98.100. Copyright ARRS. For personal use only; all rights reserved

Reversible cerebral Postpartum Rapid Thunderclap headache Normal findings cortical Arterial spasm, dilatation,
vasoconstriction syndrome watershed infarcts, reversible
SAH
Posterior reversible Late second or third Days Headache, seizures, White matter or cortical Arterial spasm
encephalopathy syndrome trimester, postpartum encephalopathy edema or both,
typically occipital
Amniotic fluid embolism Labor Rapid Respiratory distress. Diffuse hypoxemia Normal findings
shock
Air embolism Labor Rapid Seizures, stroke, Cerebral ischemia Normal findings
coagulopathy
Cerebral venous thrombosis Third trimester Hours to weeks Ischemic stroke, Cerebral venous Venous occlusion, thrombus
hemorrhage ischemia, hemorrhage
Cervicocephalic arterial Labor Hours to weeks Headache, neurologic Ischemia, hemorrhage, Intimal dissection, double
dissection deficit SAH lumen, pseudoaneurysm
Ischemic stroke Any time, third trimester Rapid Neurologic deficit Ischemia Arterial occlusion
Arteriovenous malformation Second or third trimester, Rapid Hemorrhage, seizure, Hemorrhage Dilated arteries and veins,
rupture labor headache (­parenchymal then nidus
intraventricular then
SAH
Aneurysm rupture Labor, postpartum Rapid Prototypical thunderclap SAH Cerebral aneurysm,
headache vasospasm
Cavernoma hemorrhage Second or third trimester Rapid Seizure, neurologic Focal hemorrhage. None
deficit edema
Note—SAH = subarachnoid hemorrhage.

tent progesterone exposure can promote capil-
lary leakage and vasogenic edema [2].
Underlying molecular changes that occur
in pregnancy and the puerperium are also be-
ing characterized with much greater specific-
ity. In the case of preeclampsia-eclampsia it
has been suspected for many years that ge-
netic susceptibility factors can trigger aber-
rations in the relation between placental and
maternal tissue, producing endothelial in-
jurants that lead to abnormal vasoactive re-
sponses [4, 5]. In preeclampsia, levels of the
soluble form of antiangiogenic molecules se-
creted by the placenta, such as fms-like tyro-
sine kinase 1 (sFlt1) and endoglin (a placen-
tal endothelial protein), are greatly elevated
[6]. Endoglin and sFlt1 interfere with the nor-
mal function of proangiogenic proteins, such
as vascular endothelial growth factor and pla-
cental growth factor (PlGF), that are neces-
sary for normal endothelial function. Over-
expression of endoglin in preeclampsia has
antiangiogenic effects by inhibiting vascular
signaling pathways, leading to increased vas-
cular permeability and hypertension [7].
A normal balance of PlGF and sFlt1 is re-
quired for normal vascular homeostasis [8].
In animal studies, elevated plasma concentra-
tions of sFlt1 are linked to all complications
related to human preeclampsia, including hy-
pertension, proteinuria, cerebral edema, he-
matologic abnormalities, and fetal growth re-
striction [9]. In humans, evidence also exists
of low levels of circulating angiogenic factors
and proangiogenic proteins in patients with
early-onset preeclampsia [10]. Furthermore,
increasing molecular and clinical evidence
suggests that postpartum angiopathy, re-
versible cerebral vasoconstriction syndrome
(RCVS), posterior reversible encephalopa-
thy syndrome (PRES), and possibly some ex-
pressions of thrombophilia all may represent
a constellation of related conditions at the ex-
treme, clinically relevant end of a continuum
of physiologic derangements related to the
preeclampsia-eclampsia spectrum [11]. As a
result, new recommendations call for use of
biomarkers such as circulating sFlt1-to-PlGF
ratios to detect preeclampsia and other condi-
tions, including RCVS and PRES [12].
Some cerebrovascular conditions that oc-
cur in the general population are also en-
countered in pregnancy and the puerperi-
um, including cerebral venous thrombosis,
cervicocephalic arterial dissections, and is-
chemic stroke. The clinical manifestations of
these conditions may be affected by the spe-
cific physiologic environment of pregnancy,
producing specific challenges affecting di-
agnostic evaluation and management. Preg-
nancy may also exacerbate preexisting neu-
rologic conditions, such as multiple sclerosis
and epilepsy. Finally, extremely uncommon
causes of neurologic deterioration are spe-
cific to pregnancy, including amniotic fluid
embolism and cerebral air embolism during
delivery (both of which are discussed in this
article), along with other conditions, such as
metastatic choriocarcinoma, neuromyelitis
optica, and Wernicke encephalopathy from
prolonged vomiting [2]. Table 1 summariz-
es clinical and radiologic findings of major
cerebrovascular conditions encountered dur-
ing pregnancy and the postpartum.
Diagnoses Specific to Pregnancy and
the Puerperium
Preeclampsia-Eclampsia
Preeclampsia, defined as the new onset
of hypertension, peripheral edema, and pro-
teinuria after at least 20 weeks of gestation

AJR:206, January 2016 27


in a woman previously without hypertension
affects an estimated 2–8% of pregnancies
and may present as either a mild or a severe
form [13]. The physiologic mechanism of ce-
rebral edema in eclampsia is a variation of
vasogenic edema, referred to as “hydrostat-
Downloaded from www.ajronline.org by 125.167.98.100 on 01/14/18 from IP address 125.167.98.100. Copyright ARRS. For personal use only; all rights reserved
ic edema,” in which serum leakage through
capillary walls into the brain interstitium oc-
curs as a result of a combination of endothe-
lial damage, abnormal cerebrovascular auto-
regulation, and episodes of hypertension [13,
14]. The typical manifestation of preeclamp-
sia is severe throbbing headaches, sometimes
with accompanying visual symptoms such as
blurring and scotomata [13].
Eclampsia, defined as the onset of a sei-
zure in addition to preeclampsia, occurs in
0.6% of patients with mild preeclampsia and
2–3% of those with severe preeclampsia [2].
Seizures, focal neurologic deficits, altered
mental status, and coma are the most com-
mon causes of mortality in eclampsia. How-
ever, patients who are treated early and ap-
propriately tend to recover [15]. The most
common neuroradiologic findings in eclamp-
sia are cerebral edema, ischemia, and hemor-
rhage (Fig. 1). It has been suggested [13] that
the likelihood of seizures increases com-
mensurately with the amount of subcortical
and cortical fluid, as in hypertensive enceph-
alopathy. In uncommon cases, seizures may
contribute to cortical edema in eclampsia,
producing cytotoxic characteristics (i.e., re-
stricted diffusion) on DW images [16].
Reversible Cerebral Vasoconstriction Syndrome
RCVS is a cerebral angiopathy with clin-
ical manifestations of severe thunderclap
headaches, frequently photophobia, vomiting,
and blurred vision. The headaches may be ac-
companied by seizures, neurologic deficits,
and subarachnoid or parenchymal hemor-
rhage [2, 17]. The disease may present in the
puerperium (at which point it is referred to as
“postpartum angiopathy”) or outside the pu-
erperium, caused by various factors unrelat-
ed to pregnancy, such as use of pharmacologic
substances. The pathophysiologic mechanism
of RCVS is believed to consist of deranged
cerebral autoregulation in response to endo-
thelial injury, which impairs the sympathetic
perivascular network. This network is locat-
ed within the adventitia of cerebral arteries. It
supports the myogenic response of vasocon-
striction and vasodilatation and is needed to
maintain constant cerebral blood flow [18].
Call et al. [19] reported on a syndrome of
reversible cerebral segmental vasoconstric-
28 AJR:206, January 2016
Hacein-Bey et al.
tion unrelated to pregnancy in a series of four
healthy young patients who fully recovered.
Those authors suggested that the condition
they described could be a clustering form of
migraine. At about the same time, RCVS was
reported as postpartum cerebral angiopathy in
a transient syndrome of acute benign and re-
versible cerebral angiopathy occurring in the
puerperium. This process was characterized by
vasoconstriction of cerebral arteries, presumed
to be a response to acute severe hypertension
[20]. As RCVS was further characterized [21,
22], it became apparent that between 30% and
70% of cases are seen in the postpartum peri-
od, usually within a week of delivery after an
uncomplicated pregnancy. The other cases, un-
related to the puerperium, have been attributed
to medications (selective serotonin reuptake in-
hibitors, immunosuppressive drugs), cocaine,
cervicocephalic arterial dissection, and other
factors [23–25]. Hemorrhagic forms of RCVS
were initially thought to be related to the use of
vasoactive drugs such as phenylpropanolamine
[26] and cocaine [27] until it became clear that
drug ingestion was not a necessary precondi-
tion [28]. Nonetheless, RCVS outside of the
postpartum state has also been associated with
the use of bromocriptine [29] and antimigraine
vasoconstrictive medications, such as lisuride
(an ergot alkaloid derivative [30]), sumatrip-
tan, and dihydroergotamine [31].
Although RCVS is typically considered a
benign condition, results in a large series re-
ported in 2012 [12] showed poor outcomes
among postpartum women with proteinuria.
This finding suggested an association with the
preeclampsia-eclampsia complex. In those pa-
tients, angiographic findings may be initial-
ly normal. Therefore, it is possible that preg-
nancy and the postpartum period may trigger
amplification of vasoactive derangements of
RCVS [2, 17, 32, 33]. Although most patients
usually fully recover within 6–10 weeks, post-
partum patients invariably are reported to fare
worse [2, 12, 25, 32].
The distinguishing imaging feature of
RCVS is focal or multifocal constriction of
cerebral arteries, which eventually resolves
spontaneously, usually within 3 months [17].
Results of cross-sectional neuroimaging
studies are usually normal at first. However,
hemorrhage can occur and involve the brain
parenchyma, subarachnoid space, or both
(Fig. 2). Subarachnoid hemorrhage (SAH)
may be subtle, mostly visible on FLAIR im-
ages (Fig. 3). In addition, small cortical in-
farcts may be present, typically in a water-
shed distribution. Cerebral angiography
typically shows multifocal segmental arte-
rial constrictive lesions, which are the hall-
mark of RCVS and may only become con-
spicuous after the third day [22]. Cerebral
angiography has better spatial resolution
than cross-sectional techniques, such as MRI
and CT angiography (CTA) (Figs. 2 and 3),
but it shows only the arterial lumen, akin to
MR angiography, which is nonspecific [33].
MR angiography alone has been found effec-
tive in the evaluation of RCVS initially and
over time, showing persistence of vasocon-
striction after clinical recovery [33]. In one
study of patients with acute severe headache
[34], the yield of CTA for the diagnosis of
RCVS was found to be 3%, although CTA
was not compared with MR angiography or
cerebral angiography. One report [35] docu-
mented the case of a patient with headaches
and SAH whose CTA and cerebral angio-
graphic findings were normal but who had
cerebral vasoconstriction diagnosed and fol-
lowed with transcranial Doppler imaging.
Use of contrast-enhanced imaging with
high-field-strength MRI, called high-resolu-
tion MRI (Fig. 4), facilitates visualization of
the arterial wall. Images obtained with this
technique show a pattern of continuous thick-
ening throughout the arterial wall with, at
most, only a moderate degree of contrast en-
hancement. This pattern is reported to be spe-
cific for RCVS [36]. The contrast-enhancing
structures within the arterial walls in RCVS
likely represent an abnormal subadventitial
sympathetic plexus. This pattern is unlike the
dense, eccentric wall contrast enhancement
typically found in CNS vasculitis [36].
The treatment of RCVS is medical, relying
on hypervolemic therapy [37] and calcium
channel blockers [38]. Balloon angioplasty
of cerebral arteries has been used success-
fully in severe and refractory cases [39].
Posterior Reversible Encephalopathy Syndrome
PRES is characterized by rapid onset (i.e.,
usually 12–24 hours). The typical manifes-
tations are headaches, encephalopathy, sei-
zures (90% of patients), and visual distur-
bance. The neurologic presentation of PRES
has similarities to that of other conditions,
such as RCVS (because both can occur with-
out preexisting hypertension or proteinuria,
cerebral parenchymal hemorrhage, SAH, or
acute ischemic stroke) and the preeclampsia-
eclampsia complex.
The pathophysiologic mechanism that un-
derlies PRES is thought to be vasogenic ede-
ma caused by impaired cerebral autoregula-
 Neuroimaging of Pregnancy and Puerperium
tion, which typically localizes to the occipital
regions (such that 40% of patients have symp-
toms of scotomata, diplopia, visual hallucina-
tions, and blurred vision) [40]. However, as
many as 80% of patients also have edema in
other brain regions [41]. Posterior circulation
Downloaded from www.ajronline.org by 125.167.98.100 on 01/14/18 from IP address 125.167.98.100. Copyright ARRS. For personal use only; all rights reserved
arteries have fewer mural sympathetic nerves
and are thinner than other cerebral arteries,
which makes them more susceptible to en-
dothelial damage and therefore more prone
to autoregulation breakthrough with elevat-
ed pressures. As in eclampsia, resultant ce-
rebral edema is due to capillary leakage into
the interstitial space and, at least initially, is
potentially reversible [42]. Observation of an
association between PRES and neuromyeli-
tis optica (a disease in which antibodies to the
aquaporin-4 receptor have been implicated)
may help clarify the role of aquaporin water
channel membrane proteins in the develop-
ment of vasogenic edema, possibly providing
further insight into the molecular foundation
of PRES [43, 44].
The association between PRES and RCVS
(Fig. 5) has been reported [45]. Overlap be-
tween PRES and RCVS has prompted the
term “cerebral autoregulatory dysfunction syn-
drome” [46]. In addition to the commonly ac-
cepted mechanism of loss of autoregulation
leading to endothelial dysfunction, proposed
underlying vascular mechanisms include capil-
lary leakage and edema—that is, a mechanism
of cerebral overregulation in response to hyper-
tension that leads to arterial vasospasm [47].
On T2-weighted and FLAIR images, MRI
shows areas of high signal intensity involv-
ing the cortex and subcortical white matter,
predominantly in the occipital lobes [42].
DWI typically shows elevated rather than
restricted diffusion, allowing confident ex-
clusion of irreversible ischemia and guid-
ing hemodynamic medical management [48,
49] (Fig. 5). In addition, reversible restricted
diffusion has been reported in some cases,
indicating that not all regions of restricted
diffusion represent permanent infarcts [50].
Nonetheless, protracted edema and severe
endothelial injury may eventually produce
hemorrhages and permanent injuries, such
that PRES should not be thought of as a con-
sistently benign and reversible condition.
During the late second and early third tri-
mesters of pregnancy, PRES may coexist
with two rare and distinct hematologic con-
ditions, thrombotic thrombocytopenic pur-
pura (TTP) and HELLP syndrome (hemoly-
sis, elevated liver enzyme levels, low platelet
count), which have similar neurologic mani-
AJR:206, January 2016 29
festations—that is, seizures, headaches, and
neurologic deficits [2, 51]. Both conditions
are considered part of the preeclampsia-ec-
lampsia complex. Additional manifestations
of thrombotic thrombocytopenic purpu-
ra are thrombocytopenia, microangiopath-
ic hemolytic anemia, fever, and neurolog-
ic and renal dysfunction [51]. This disorder
must be promptly diagnosed; treatment con-
sists primarily of plasma exchange. HELLP
syndrome requires magnesium therapy and
rapid delivery of the infant [52]. HELLP
syndrome has also been reported as an inci-
dental finding in association with eclampsia,
arterial dissections, and stroke [53].
Amniotic Fluid Embolism
Amniotic fluid embolism is rare, with a re-
ported incidence of 2–8 per 100,000 births
[54]. However, it is the leading cause of mor-
tality during labor and the first few post-
partum hours, with reported mortality rates
ranging between 26% and 86% [55, 56]. The
first manifestation of amniotic fluid embo-
lism is respiratory distress, followed by he-
modynamic compromise if pulmonary ede-
ma and shock ensue. These findings may be
followed by cerebral hypoperfusion with the
clinical manifestations of seizures, confu-
sion, and coma. Maternal death may occur
from sudden cardiac arrest, hemorrhage due
to coagulopathy, and multiple organ failure
with acute respiratory distress syndrome.
Amniotic fluid embolism was first report-
ed in the literature by Meyer [57] in 1926,
and the pathophysiologic mechanisms re-
main incompletely understood [58]. A con-
sensus exists that the initial physiologic de-
rangement is pulmonary vasoconstriction (as
opposed to occlusion of pulmonary arteries
by amniotic fluid) with resultant pulmonary
hypertension, right-heart failure, and hypox-
emia [55, 56]. It is becoming clear that ex-
posure to insoluble fetal proteins, vasoactive
substances (primarily histamine and brady-
kinin), and procoagulants in the amniotic
fluid trigger massive endothelial activation
in predisposed patients, leading to a major
inflammatory response that can culminate
in anaphylactic shock [54–58]. No standard
diagnostic test for amniotic fluid embolism
currently exists. The finding of fetal cells in
the mother is not diagnostic because fetal
cells are often normally present in the circu-
lation of healthy pregnant women [59].
The neuroradiologic manifestations of am-
niotic fluid embolism include findings of gen-
eralized cerebral hypoxemia and ischemia due
to hypoperfusion or multiple cerebral emboli
from secondary left-heart failure or a right-to-
left shunt. Early hemorrhagic transformation
of ischemic lesions can be seen [60].
Air Embolism During Delivery
Air embolism occurs when air that enters
the myometrium during delivery reaches the
venous circulation and right ventricle, reduc-
ing cardiac output [61, 62]. During cesarean
delivery, venous air embolism is common,
seen in as many as 97% of patients, depend-
ing on patient positioning (particularly the
Trendelenburg position) and the degree of
sophistication of diagnostic tests used [62].
The most common mechanism of air embo-
lism is passage of air from ruptured veins to
the right cardiac chambers and pulmonary
artery. However, inhalational agents used in
general anesthesia (e.g., carbon dioxide, ni-
trous oxide, nitrogen, and helium) may also
cause or aggravate venous air embolism [62,
63]. Owing to hemodynamic instability, ve-
nous air embolism alone may cause seizures
or decreased consciousness during (or just
after) delivery. In addition, a severe, irre-
versible coagulopathy may occur in some pa-
tients as a result of venous air embolism [64].
Finally, if a right-to left intracardiac shunt or
a patent foramen ovale is present, passage
of air into the cerebral circulation may oc-
cur, which can cause a variety of neurolog-
ic symptoms and signs. At clinical examina-
tion, the presence of air in the retinal veins
and a so-called mill-wheel cardiac murmur
suggest the diagnosis [2].
Neuroimaging may reveal air within the
arterial system at CT, which may corre-
late with hyperintense foci on FLAIR and
T2-weighted MR images and restricted dif-
fusion on apparent diffusion coefficient
maps [65] (Fig. 6).
Diagnoses With Increased Frequency
During Pregnancy and the P ­ uerperium
Cerebral Venous Thrombosis
Pregnancy is associated with a 5- to 10-fold
increase in the risk of venous thromboembo-
lism, mostly during the final trimester [66].
Common risk factors for cerebral venous
thrombosis in pregnancy and the puerperium
include dehydration, anemia, homocystein-
emia, paraneoplastic states, traumatic deliv-
ery, cesarean delivery, and low CSF pressure
secondary to lumbar puncture for epidural
analgesia [66–68]. Patients typically present
with a headache of progressive severity and
diffuse distribution; however, thunderclap

headache may be the presenting feature [69].
The location and extent of thrombosis within
dural sinuses dictate the clinical presentation,
which can include dizziness; nausea; papill-
edema; motor, sensory, or visual disturbanc-
es; psychiatric manifestations; lethargy; and
Downloaded from www.ajronline.org by 125.167.98.100 on 01/14/18 from IP address 125.167.98.100. Copyright ARRS. For personal use only; all rights reserved
coma [70]. PRES has been reported in asso-
ciation with dural sinus thrombosis [71]. Rap-
id clinical deterioration can occur if cerebral
venous thrombosis is not treated, either from
venous infarction or extension of thrombus
into the deep venous system.
When cerebral venous thrombosis occurs
during pregnancy, especially during the first
trimester, an underlying hypercoagulable
state is usually present, most often factor V
Leiden deficiency [70]. However, most oc-
currences (75%) are seen in the postpartum
period, and usually no underlying coagulop-
athy is found. Postpartum patients have bet-
ter outcomes than pregnant patients [71].
CT shows a clearly identifiable high-attenua-
tion thrombus within a large dural sinus in only
approximately 30% of cases (Fig. 7). More
commonly, the thrombosed dural sinus causes
only a small increase in CT attenuation, mak-
ing diagnosis difficult [72]. Contrast-enhanced
MRI with the inclusion of MR venography and
susceptibility-weighted imaging is the imag-
ing study of choice (Fig. 7) for diagnosing du-
ral sinus thrombosis [73]. If unenhanced MRI
alone is used, an important pitfall exists be-
cause thrombus in the early stage of evolution
may appear isointense to brain on T1-weighted
images and hypointense on T2-weighted imag-
es (Fig. 7), mimicking normal flow [74]. Time-
resolved CTA is reported to have high accu-
racy in depicting dural sinus and cortical vein
thrombosis and the compensatory venous col-
lateral pathways needed to guide thrombolytic
therapy [75]. Cerebral angiography is general-
ly reserved for cases in which a neurointerven-
tional procedure is needed to treat a thrombus
that is causing rapid neurologic decline.
Cervicocephalic Arterial Dissection
Arterial dissection of the cervicocephalic
arteries is an increasingly recognized cause
of stroke among young and middle-aged per-
sons [76]. In a large multihospital study, ex-
tracranial vertebral artery dissection was
identified, after eclampsia, as the most com-
mon cause of ischemic stroke during preg-
nancy [77]. Risk factors remain largely
unclear, with the exception of known con-
nective tissue disorders and abnormal neck
movements [78]. However, an association
with RCVS in postpartum patients has been
30 AJR:206, January 2016
Hacein-Bey et al.
suggested [79]. Cervicocephalic arterial dis-
sections have also been reported in associa-
tion with cerebral venous thrombosis [80].
A characteristic appearance is seen on un-
enhanced T1-weighted MR images, namely,
that of a crescentic rim of high signal inten-
sity within the arterial wall and narrowing of
the arterial lumen [81]. The hyperintense ap-
pearance is caused by blood in the methemo-
globin stage. However, this finding may not be
present in the first few days after the onset of
dissection, that is, while blood is still in the
deoxyhemoglobin stage (Fig. 8). A number of
pitfalls in the diagnosis of dissection can be
seen at CTA, MRI, and MR angiography [82].
Ischemic Stroke
The earliest reported incidence of isch-
emic carotid territory stroke in pregnant or
puerperal women was five cases per 100,000
deliveries in a Scottish cohort [83]. Later, the
incidence of stroke among pregnant and pu-
erperal women was estimated to be 13 times
that of nonpregnant women of comparable
age [84], although it was suggested that some
of the patients described in that cohort likely
had cerebral venous thrombosis [85]. Results
of yet another study [85] suggested that the
postpartum state rather than pregnancy was
associated with increased risk of cerebral
infarction and hemorrhage. The topic is ex-
tensive and has been reviewed [86]. In brief,
the findings in that review were as follows:
whereas stroke mortality rates in the gener-
al population have decreased over 4 decades,
the rate among pregnant women has not sub-
stantially changed; approximately 90% of
maternal strokes occur at delivery or in the
postpartum period; and intracranial hemor-
rhage is the leading cause of maternal stroke
death, many of those cases being associated
with preeclampsia or eclampsia.
During pregnancy, the radiologic diag-
nosis of acute ischemic stroke relies heavily
on DWI, which may show restricted diffu-
sion in ischemic brain tissue within minutes
of stroke onset [87]. Assessment of the is-
chemic penumbra with either perfusion
CT or contrast-enhanced MRI is generally
avoided during pregnancy but can be rou-
tinely performed when the stroke occurs
postpartum [87]. Although both endovas-
cular therapy [88] and IV thrombolysis [89]
have been used in the management of strokes
occurring during the third trimester of preg-
nancy, treatment effectiveness is not estab-
lished at this time, and overall complication
rates remain fairly high.
Hemorrhagic Stroke
Cardiac output increases 60% by the end
of the second trimester, but blood volume
and arterial pressure increase progressively
throughout pregnancy to reach their highest
values at term. In addition, various molecu-
lar changes affect endothelial, capillary, and
smooth-muscle function, such that in predis-
posed patients intracranial hemorrhage is an
important cause of morbidity and mortal-
ity. Cerebral arteriovenous malformations
(AVMs), intracranial aneurysms, and caver-
nomas are the most common lesions related
to cerebral hemorrhage.
Cerebral AVM rupture is considered the
second most common cause of cerebral hem-
orrhage during pregnancy and the postpar-
tum period, after eclampsia [90]. The risk
of hemorrhage from a cerebral AVM during
pregnancy has been estimated at approxi-
mately 3.5%. It was therefore concluded that
pregnancy is not a risk factor for hemorrhage
from previously unruptured AVMs [91].
For AVMs that bleed during pregnancy,
the risk of rerupture during the same preg-
nancy remains poorly understood, although
it has been reported to be 27% [92], hyper-
tension being the most important indepen-
dent risk factor for repeat hemorrhage from
ruptured AVMs [93]. Ruptured AVMs most
commonly cause intracerebral hemorrhage
followed by intraventricular hemorrhage
and uncommonly SAH, all easily identi-
fied with CT or MRI [94]. Pial AVMs, the
most common type, are abnormal connec-
tions between arteries and veins with an in-
tervening vascular tangle (nidus) of variable
size, which is embedded within (but separate
from) brain parenchyma but without a true
capillary bed. The AVM nidus and enlarged
feeding arteries and draining veins may be
readily visible with CT, CTA, and MRI. Ear-
ly venous drainage is best evaluated with ce-
rebral angiography, which remains the refer-
ence standard [95].
Although classically reported to rupture
during labor [90], cerebral aneurysms have a
low rupture rate during pregnancy, and most
are reported to rupture in the postpartum
period. In a large study conducted with the
Nationwide Inpatient Sample of the Health-
care Cost and Utilization Project, Agency for
Healthcare Research and Quality, pregnan-
cy-related admissions for women 15 to 44
years old between 1995 and 2008 revealed
a rate of SAH of 5.8 per 100,000 deliveries,
more than one-half of the cases of SAH oc-
curring postpartum [96]. A 2013 study [97]
 Neuroimaging of Pregnancy and Puerperium
showed a 1.4% risk of aneurysm rupture
during pregnancy and 0.05% during deliv-
ery, both figures lower than for the general
nonpregnant female population. In patients
with aneurysmal SAH, CTA has reported
specificity rates of 96–98% (90–94% for an-
Downloaded from www.ajronline.org by 125.167.98.100 on 01/14/18 from IP address 125.167.98.100. Copyright ARRS. For personal use only; all rights reserved
eurysms smaller than 3 mm and as high as
100% for aneurysms larger than 4 mm) and
sensitivity rates of 96–98% [98]. MR angi-
ography performed with 3D time-of-flight
technique is highly sensitive to patient mo-
tion, which is particularly hard to control in
patients with SAH [99].
Contrast-enhanced MR angiography per-
formed with accelerated parallel imaging is
reported to have higher sensitivity than time-
of-flight imaging, similar to that of high-reso-
lution CTA [100]. However, gadolinium may
not be administered during pregnancy. The
reference standard for the diagnosis of cere-
bral aneurysms, ruptured or not, remains ce-
rebral angiography [101]. There is agreement
that management during pregnancy should be
the same as otherwise, either with endovas-
cular [102] or open surgical [103] technique.
Cavernomas, also called cerebral cavern-
ous malformations, are the most commonly
diagnosed cerebral vascular malformations,
with a prevalence estimated between 100 and
500 cases per 100,000 population [104]. Cav-
ernoma may occur either sporadically, de-
fined as an isolated lesion in a patient without
a family history of the lesion, or as a familial
form in which there are multiple lesions. The
estimated hemorrhagic risk in the familial
form may be as low as 0.6% per year and per
lesion [105]. Although the effects of pregnan-
cy, the postpartum state, and hormonal thera-
py remain poorly understood and the source
of much controversy [106], the risk of symp-
tomatic hemorrhage from a cavernoma during
pregnancy does not appear to be increased or
to contraindicate vaginal delivery [107]. Most
cavernomas are asymptomatic and incidental-
ly discovered at MRI, on either T2-weighted
or gradient-echo images [108, 109]. Suscepti-
bility-weighted imaging has become the stan-
dard diagnostic test for cavernoma [110].
The addition of dynamic contrast-en-
hanced quantitative perfusion to suscepti-
bility-weighted imaging may be the most
sensitive radiologic method for detecting cav-
ernomas and may become a useful biomarker
for monitoring natural history and response
to therapy [111]. When symptomatic, cav-
ernomas typically present with seizures or
hemorrhage, which can produce neurologic
deficits or severe headaches [109, 112].
AJR:206, January 2016 31
In a pregnant woman presenting with sei-
zures, the diagnosis of eclampsia is by far
the first consideration, followed by PRES,
CVT, and RCVS [2]. In case of a first hemor-
rhage from a cavernoma, MRI findings may
be atypical, suggesting a tumor or some oth-
er lesion, by revealing a soft-tissue mass sur-
rounded with fresh blood without evidence
of old hemorrhagic products (Fig. 9).
Conclusion
Radiologists must be familiar with the im-
aging findings of cerebrovascular complica-
tions and pathologic conditions encountered
during pregnancy and the puerperium. On-
going improvements in understanding of
molecular changes during pregnancy and
the puerperium and advances in diagnostic
tests should allow radiologists to continue to
make important contributions to the care of
this patient population.
References
1. Kuklina EV, Tong X, Bansil P, et al. Trends in
pregnancy hospitalizations that included a stroke
in the United States from 1994 to 2007: reasons
for concern? Stroke 2011; 42:2564–2570
2. Edlow JA, Caplan LR, O’Brien K, Tibbles CD.
Diagnosis of acute neurological emergencies in
pregnant and post-partum women. Lancet Neurol
2013; 12:175–185
3. Sidorov EV, Feng W, Caplan LR. Stroke in pregnant
and postpartum women. Expert Rev C ­ ardiovasc
Ther 2011; 9:1235–1247
4. Roberts JM. Endothelial dysfunction in pre-
eclampsia. Semin Reprod Endocrinol 1998;
16:5–15
5. Roberts JM, Cooper DW. Pathogenesis and ge-
netics of pre-eclampsia. Lancet 2001; 357:53–56
6. Mijal RS, Holzman CB, Rana S, et al. Mid-preg-
nancy levels of angiogenic markers as indicators
of pathways to preterm delivery. J Matern Fetal
Neonatal Med 2012; 25:1135–1141
7. Levine RJ, Lam C, Qian C, et al. CPEP Study
Group. Soluble endoglin and other circulating
antiangiogenic factors in preeclampsia. N Engl J
Med 2006; 355:992–1005
8. Maynard SE, Min JY, Merchan J, et al. Excess
placental soluble fms-like tyrosine kinase 1
(sFlt1) may contribute to endothelial dysfunction,
hypertension, and proteinuria in preeclampsia.
J Clin Invest 2003; 111:649–658
9. Lu F, Longo M, Tamayo E, et al. The effect of over-
expression of sFlt-1 on blood pressure and the oc-
currence of other manifestations of preeclampsia in
unrestrained conscious pregnant mice. Am J Obstet
Gynecol 2007; 196:396.e1–396.e7
10. Noori M, Donald AE, Angelakopoulou A, et al. Pro-
spective study of placental angiogenic factors and
maternal vascular function before and after pre-
eclampsia and gestational hypertension. ­Circulation
2010; 122:478–487
11. Rana S, Powe CE, Salahuddin S, et al. Angio-
genic factors and the risk of adverse outcomes in
women with suspected preeclampsia. C ­ irculation
2012; 125:911–919
12. Fugate JE, Ameriso SF, Ortiz G, et al.
Variable presentations of postpartum angiopathy.
Stroke 2012; 43:670–676
13. Fletcher JJ, Kramer AH, Bleck TP, Solenski NJ.
Overlapping features of eclampsia and postpartum
angiopathy. Neurocrit Care 2009; 11:199–209
14. Duley L, Meher S, Abalos E. Management of
pre-eclampsia. BMJ 2006; 332:463–468
15. Sibai BM. Diagnosis, prevention, and manage-
ment of eclampsia. Obstet Gynecol 2005;
105:402–410
16. Ginzburg VE, Wolff B. Headache and seizure on
postpartum day 5: late postpartum eclampsia.
CMAJ 2009; 180:425–428
17. Calabrese LH, Dodick DW, Schwedt TJ, Singhal
AB. Narrative review: reversible cerebral vaso-
constriction syndromes. Ann Intern Med 2007;
146:34–44
18. Aukes AM, de Groot JC, Aarnoudse JG, Zeeman
GG. Brain lesions several years after eclampsia.
Am J Obstet Gynecol 2009; 200:504.e1–504.e5
19. Call GK, Fleming MC, Sealfon S, et al. Revers-
ible cerebral segmental vasoconstriction. Stroke
1988; 19:1159–1170
20. Bogousslavsky J, Despland PA, Regli F,
­Dubuis PY. Postpartum cerebral angiopathy: revers-
ible vasoconstriction assessed by transcranial Dop-
pler ultrasounds. Eur Neurol 1989; 29:102–105
21. Neudecker S, Stock K, Krasnianski M. Call-
Fleming postpartum angiopathy in the puerperi-
um: a reversible cerebral vasoconstriction syn-
drome. Obstet Gynecol 2006; 107:446–449
22. Ducros A, Boukobza M, Porcher R, et al. The clin-
ical and radiological spectrum of reversible cere-
bral vasoconstriction syndrome: a prospective se-
ries of 67 patients. Brain 2007; 130:3091–3101
23. Ducros A, Bousser MG. Reversible cerebral
vasoconstriction syndrome. Pract Neurol 2009;
9:256–267
24. Sattar A, Manousakis G, Jensen MB. Sys-
tematic review of reversible cerebral vasocon-
striction syndrome. Expert Rev Cardiovasc Ther
2010; 8:1417–1421
25. Ducros A, Fiedler U, Porcher R, et al.
Hemorrhagic manifestations of reversible cere-
bral vasoconstriction syndrome: frequency, fea-
tures, and risk factors. Stroke 2010; 41:2505–2511
26. Maher LM, Peterson PL, Dela-Cruz C.
Postpartum intracranial hemorrhage and phenyl-
propanolamine use. Neurology 1987; 37:1686

27. Mercado A, Johnson G Jr, Calver D, Sokol RJ. Co-
caine, pregnancy, and postpartum intracerebral
hemorrhage. Obstet Gynecol 1989; 73:467–468
28. Geocadin RG, Razumovsky AY, Wityk RJ,
et al. Intracerebral hemorrhage and postpartum ce-
rebral vasculopathy. J Neurol Sci 2002; 205:29–34
Downloaded from www.ajronline.org by 125.167.98.100 on 01/14/18 from IP address 125.167.98.100. Copyright ARRS. For personal use only; all rights reserved
29. Janssens E, Hommel M, Mounier-Vehier F, et al.
Postpartum cerebral angiopathy possibly due to
bromocriptine therapy. Stroke 1995; 26:128–130
30. Roh JK, Park KS. Postpartum cerebral an-
giopathy with intracerebral hemorrhage in a patient
receiving lisuride. Neurology 1998; 50:1152–1154
31. Granier I, Garcia E, Geissler A, et al. Postpartum
cerebral angiopathy associated with the adminis-
tration of sumatriptan and dihydroergotamine: a
case report. Intensive Care Med 1999; 25:532–534
32. Fugate JE, Wijdicks EF, Parisi JE, et al.
Fulminant postpartum cerebral vasoconstriction
syndrome. Arch Neurol 2012; 69:111–117
33. Chen SP, Fuh JL, Wang SJ, et al. Magnetic reso-
nance angiography in reversible cerebral vasocon-
striction syndromes. Ann Neurol 2010; 67:648–656
34. Alons IM, van den Wijngaard IR, Verheul
RJ, et al. The value of CT angiography in patients
with acute severe headache. Acta Neurol Scand
2015; 131:164–168
35. Bittel B, Husmann K. A case report of thunder-
clap headache with subarachnoid hemorrhage
and negative angiography: a review of Call-
Fleming syndrome and the use of transcranial
Dopplers in predicting morbidity. J Vasc Interv
Neurol 2011; 4:5–8
36. Obusez EC, Hui F, Hajj-Ali RA, et al. High-
resolution MRI vessel wall imaging: spatial and
temporal patterns of reversible cerebral vasocon-
striction syndrome and central nervous system vas-
culitis. AJNR 2014; 35:1527–1532
37. Akins PT, Levy KJ, Cross AH, et al. Postpartum
cerebral vasospasm treated with hypervolemic ther-
apy. Am J Obstet Gynecol 1996; 175:1386–1388
38. Ursell MR, Marras CL, Farb R, et al. Re-
current intracranial hemorrhage due to postpar-
tum cerebral angiopathy: implications for man-
agement. Stroke 1998; 29:1995–1998
39. Song JK, Fisher S, Seifert TD, et al. Postpartum
cerebral angiopathy: atypical features and treat-
ment with intracranial balloon angioplasty.
­Neuroradiology 2004; 46:1022–1026
40. Weiner CP. The clinical spectrum of pre-
eclampsia. Am J Kidney Dis 1987; 9:312–316
41. McKinney AM, Short J, Truwit CL, et al. Poste-
rior reversible encephalopathy syndrome: inci-
dence of atypical regions of involvement and im-
aging findings. AJR 2007; 189:904–912
42. Schwartz RB, Jones KM, Kalina P, et al.
Hypertensive encephalopathy: findings on CT,
MR imaging, and SPECT imaging in 14 cases.
AJR 1992; 159:379–383
32 AJR:206, January 2016
Hacein-Bey et al.
43. Magaña SM, Matiello M, Pittock SJ, et al. Poste-
rior reversible encephalopathy syndrome in neu-
romyelitis optica spectrum disorders. Neurology
2009; 72:712–717
44. Cheng C, Jiang Y, Chen X, et al. Clinical,
radiographic characteristics and immunomodu-
lating changes in neuromyelitis optica with ex-
tensive brain lesions. BMC Neurol 2013; 13:72
45. Singhal AB. Postpartum angiopathy with revers-
ible posterior leukoencephalopathy. Arch Neurol
2004; 61:411–416
46. Garg RK, Malhotra HS, Patil TB, ­ Agrawal
A. Cerebral-autoregulatory dysfunction syn-
drome. BMJ Case Rep 2013; 2013:bcr2013201592
47. Morriss MC, Twickler DM, Hatab MR, et al.
Cunningham FG. Cerebral blood flow and crani-
al magnetic resonance imaging in eclampsia and
severe preeclampsia. Obstet Gynecol 1997;
89:561–568
48. Bartynski WS, Boardman JF. Catheter angi-
ography, MR angiography, and MR perfusion in
posterior reversible encephalopathy syndrome.
AJNR 2008; 29:447–455
49. Schaefer PW. Diffusion-weighted imaging as a
problem-solving tool in the evaluation of patients
with acute stroke like syndromes. Top Magn
­Reson Imaging 2000; 11:300–309
50. Benziada-Boudour A, Schmitt E, Kremer
S, et al. Posterior reversible encephalopathy syn-
drome: a case of unusual diffusion-weighted MR
images. J Neuroradiol 2009; 36:102–105
51. Martin JN Jr, Bailey AP, Rehberg JF, et al.
Thrombotic thrombocytopenic purpura in 166
pregnancies: 1955–2006. Am J Obstet Gynecol
2008; 199:98–104
52. Burrus TM, Wijdicks EF, Rabinstein AA.
Brain lesions are most often reversible in acute
thrombotic thrombocytopenic purpura. N ­ eurology
2009; 73:66–70
53. Borelli P, Baldacci F, Vergallo A, et al. Bilateral
thalamic infarct caused by spontaneous vertebral
artery dissection in pre-eclampsia with HELLP
syndrome: a previously unreported association.
J Stroke Cerebrovasc Dis 2012; 21:914.e9–914.e10
54. Ito F, Akasaka J, Koike N, et al. Inci-
dence, diagnosis and pathophysiology of amni-
otic fluid embolism. J Obstet Gynaecol 2014;
34:580–584
55. Gist RS, Stafford IP, Leibowitz AB, Beilin Y.
Amniotic fluid embolism. Anesth Analg 2009;
108:1599–1602
56. Busardo FP, Gulino M, Di Luca NM, et
al. Not only a clinical nightmare: amniotic fluid
embolism in court. Curr Pharm Biotechnol 2014;
14:1195–1200
57. Meyer JR. Embolia pulmonar amnio caseosa.
Bras Med 1926; 2:301–303
58. Rath WH, Hoferr S, Sinicina I. Amniotic
fluid embolism: an interdisciplinary challenge:
epidemiology, diagnosis and treatment. Dtsch
Arztebl Int 2014; 111:126–132
59. Brass SD, Copen WA. Neurological disorders in
pregnancy from a neuroimaging perspective.
­Semin Neurol 2007; 27:411–424
60. Stawicki SP, Papadimos TJ. Challenges in
managing amniotic fluid embolism: an up-to-date
perspective on diagnostic testing with focus on
novel biomarkers and avenues for future research.
Curr Pharm Biotechnol 2014; 14:1168–1178
61. Muth CM, Shank ES. Gas embolism. N Engl J
Med 2000; 342:476–482
62. Lew TW, Tay DH, Thomas E. Venous air
embolism during cesarean section: more com-
mon than previously thought. Anesth Analg 1993;
77:448–452
63. Kim CS, Liu J, Kwon JY, et al. Venous air
embolism during surgery, especially cesarean de-
livery. J Korean Med Sci 2008; 23:753–761
64. Moningi S, Kulkarni D, Bhattacharjee S.
Coagulopathy following venous air embolism: a
disastrous consequence—a case report. Korean J
Anesthesiol 2013; 65:349–352
65. Lynn AM, Yang MJ, Wang PH, et al.
Postpartum eclampsia with cerebral air embo-
lism. Taiwan J Obstet Gynecol 2013; 52:431–434
66. Lanska DJ, Kryscio RJ. Risk factors for pe-
ripartum and postpartum stroke and intracranial
venous thrombosis. Stroke 2000; 31:1274–1282
67. Cantu-Brito C, Arauz A, Aburto Y, et al. Cere-
brovascular complications during pregnancy and
postpartum: clinical and prognosis observations
in 240 Hispanic women. Eur J Neurol 2011;
18:819–825
68. Coutinho JM, Ferro JM, Canhão P, et al.
Cerebral venous and sinus thrombosis in women.
Stroke 2009; 40:2356–2361
69. Stam J. Thrombosis of the cerebral veins and si-
nuses. N Engl J Med 2005; 352:1791–1798
70. Masuhr F, Mehraein S, Einhaupl K. Cere-
bral venous and sinus thrombosis. J Neurol 2004;
251:11–23
71. Petrovic BD, Nemeth AJ, McComb EN, Walker
MT. Posterior reversible encephalopathy syn-
drome and venous thrombosis. Radiol Clin North
Am 2011; 49:63–80
72. Saposnik G, Barinagarrementeria F, Brown
RD Jr, et al.; American Heart Association Stroke
Council and the Council on Epidemiology and Pre-
vention. Diagnosis and management of cerebral
venous thrombosis: a statement for healthcare pro-
fessionals from the American Heart Association/
American Stroke Association. Stroke 2011;
42:1158–1192
73. Ganeshan D, Narlawar R, McCann C, et al. Cere-
bral venous thrombosis: a pictorial review. Eur J
Radiol 2010; 74:110–116
 Neuroimaging of Pregnancy and Puerperium
74. Hinman JM, Provenzale JM. Hypointense
thrombus on T2-weighted MR imaging: a poten-
tial pitfall in the diagnosis of dural sinus throm-
bosis. Eur J Radiol 2002; 41:147–152
75. Ono Y, Abe K, Suzuki K, et al. Usefulness of 4D-
CTA in the detection of cerebral dural sinus oc-
Downloaded from www.ajronline.org by 125.167.98.100 on 01/14/18 from IP address 125.167.98.100. Copyright ARRS. For personal use only; all rights reserved
clusion or stenosis with collateral pathways.
­Neuroradiol J 2013; 26:428–438
76. Schievink WI. Spontaneous dissection of
the carotid and vertebral arteries. N Engl J Med
2001; 344:898–906
77. Sharshar T, Lamy C, Mas JL; Stroke in Pregnan-
cy Study Group. Incidence and causes of strokes
associated with pregnancy and puerperium: a
study in public hospitals of Ile de France. Stroke
in Pregnancy Study Group. Stroke 1995; 26:930–
936
78. Rubinstein SM, Peerdeman SM, van Tulder
MV, et al. A systematic review of the risk factors for
cervical artery dissection. Stroke 2005; 36:1575–1580
79. Arnold M, Camus-Jacqmin M, Stapf C, et al.
Postpartum cervicocephalic artery dissection.
Stroke 2008; 39:2377–2379
80. Ostrovskiy D, Hacein-Bey L, Varelas PN,
Heverly DN. Simultaneous postpartum cerebral
venous thrombosis and cervico-cephalic arterial
dissections. Cerebrovasc Dis 2003; 16:301–303
81. Lévy C, Laissy JP, Raveau V, et al. Carotid and
vertebral artery dissections: three-dimensional
time-of-flight MR angiography and MR imaging
versus conventional angiography. Radiology
1994; 190:97–103
82. Provenzale JM, Sarikaya B, Hacein-Bey L,
Wintermark M. Causes of misinterpretation of
cross-sectional imaging studies for dissection of
the craniocervical arteries. AJR 2011; 196:45–52
83. Cross JN, Castro PO, Jennett WB. Cere-
bral strokes associated with pregnancy and the
puerperium. BMJ 1968; 3:214–218
84. Wiebers DO. Ischemic cerebrovascular complica-
tions of pregnancy. Arch Neurol 1985; 42:1106–1113
85. Kittner SJ, Stern BJ, Feeser BR, et al.
Pregnancy and the risk of stroke. N Engl J Med
1996; 335:768–774
86. Foo L, Bewley S, Rudd A. Maternal death
from stroke: a thirty year national retrospective
review. Eur J Obstet Gynecol Reprod Biol 2013;
171:266–270
87. Wintermark M, Sanelli PC, Albers GW, et al. Im-
aging recommendations for acute stroke and
transient ischemic attack patients: a joint state-
AJR:206, January 2016 33
ment by the American Society of Neuroradiolo-
gy, the American College of Radiology and the
Society of NeuroInterventional Surgery. J Am
Coll Radiol 2013; 10:828–832
88. Murugappan A, Coplin WM, Al-Sadat AN,
et al. Thrombolytic therapy of acute ischemic stroke
during pregnancy. Neurology 2006; 66:768–770
89. Mantoan Ritter L, Schüler A, Gangopadhyay R,
et al. Successful thrombolysis of stroke with in-
travenous alteplase in the third trimester of preg-
nancy. J Neurol 2014; 261:632–634
90. Mas JL, Lamy C. Stroke in pregnancy and
the puerperium. J Neurol 1998; 245:305–313
91. Horton JC, Chambers WA, Lyons SL, Adams
RD, Kjellberg RN. Pregnancy and the risk of
hemorrhage from cerebral arteriovenous malfor-
mations. Neurosurgery 1990; 27:867–871
92. Sadasivan B, Malik GM, Lee C, Ausman
JI. Vascular malformations and pregnancy. Surg
Neurol 1990; 33:305–313
93. Langer DJ, Lasner TM, Hurst RW, Flamm
ES, Zager EL, King JT Jr. Hypertension, small size,
and deep venous drainage are associated with risk of
hemorrhagic presentation of cerebral arteriovenous
malformations. Neurosurgery 1998; 42:481–486
94. Mohr JP, Kejda-Scharler J, Pile-Spellman J.
Diagnosis and treatment of arteriovenous malforma-
tions. Curr Neurol Neurosci Rep 2013; 13:324
95. Geibprasert S, Pongpech S, Jiarakongmun P,
Shroff MM, Armstrong DC, Krings T. Radiologic
assessment of brain arteriovenous malformations:
what clinicians need to know. RadioGraphics 2010;
30:483–501
96. Bateman BT, Olbrecht VA, Berman MF,
Minehart RD, Schwamm LH, Leffert LR. Peri-
partum subarachnoid hemorrhage: nationwide
data and institutional experience. Anesthesiology
2012; 116:324–333
97. Kim YW, Neal D, Hoh BL. Cerebral aneurysms
in pregnancy and delivery: pregnancy and deliv-
ery do not increase the risk of aneurysm rupture.
Neurosurgery 2013; 72:143–149; discussion, 150
98. McKinney AM, Palmer CS, Truwit CL,
Karagulle A, Teksam M. Detection of aneurysms by
64-section multidetector CT angiography in patients
acutely suspected of having an intracranial aneurysm
and comparison with digital subtraction and 3D rota-
tional angiography. AJNR 2008; 29:594–602
99. Bernstein MA, Huston J 3rd, Lin C, Gibbs GF,
Felmlee JP. High-resolution intracranial and cervi-
cal MRA at 3.0T: technical considerations and ini-
tial experience. Magn Reson Med 2001; 46:955–962
100. Nael K, Villablanca JP, Mossaz L, et al. 3-T con-
trast-enhanced MR angiography in evaluation of
suspected intracranial aneurysm: comparison with
MDCT angiography. AJR 2008; 190:389–395
101. Hacein-Bey L, Provenzale JM. Current imaging
assessment and treatment of intracranial aneu-
rysms. AJR 2011; 196:32–44
102. Meyers PM, Halbach VV, Malek AM, et al. En-
dovascular treatment of cerebral artery aneu-
rysms during pregnancy: report of three cases.
AJNR 2000; 21:1306–1311
103. Kataoka H, Miyoshi T, Neki R, Yoshimatsu J,
Ishibashi-Ueda H, Iihara K. Subarachnoid hem-
orrhage from intracranial aneurysms during
pregnancy and the puerperium. Neurol Med Chir
(Tokyo) 2013; 53:549–554
104. Labauge P, Denier C, Bergametti F, Tournier-
Lasserve E. Genetics of cavernous angiomas.
Lancet Neurol 2007; 6:237–244
105. Labauge P, Brunerau L, Laberge S, Houtteville
JP. Prospective follow-up of 33 asymptomatic pa-
tients with familial cerebral cavernous malfor-
mations. Neurology 2001; 57:1825–1828
106. Stapf C, Hervé D. From cavern-dwellers to caver-
noma science: towards a new philosophy of cere-
bral cavernous malformations. Stroke 2008;
39:3129–3130
107. Kalani MY, Zabramski JM. Risk for symptomatic
hemorrhage of cerebral cavernous malformations
during pregnancy. J Neurosurg 2013; 118:50–55
108.
Wurm G, Fellner FA. Implementation of T2*-
weighted MR for multimodal image guidance in ce-
rebral cavernomas. Neuroimage 2004; 22:841–846
109. Lehnhardt FG, von Smekal U, Ruckriem B, et al.
Value of gradient-echo magnetic resonance imag-
ing in the diagnosis of familial cerebral cavernous
malformation. Arch Neurol 2005; 62:653–658
110. de Champfleur NM, Langlois C, Ankenbrandt
WJ, et al. Magnetic resonance imaging evalua-
tion of cerebral cavernous malformations with
susceptibility-weighted imaging. Neurosurgery
2011; 68:641–647; discussion, 647–648
111. Mikati AG, Tan H, Shenkar R, et al. Dynamic
permeability and quantitative susceptibility: re-
lated imaging biomarkers in cerebral cavernous
malformations. Stroke 2014; 45:598–601
112. Hoeldtke NJ, Floyd D, Werschkul JD, Calhoun
BC, Hume RF. Intracranial cavernous angioma
initially presenting in pregnancy with new-onset
seizures. Am J Obstet Gynecol 1998; 178:612–613
(Figures start on next page)
 Fig. 1—30-year-old woman at 24th week of pregnancy with subarachnoid hemorrhage as complication of
Hacein-Bey
eclampsia. Axial FLAIR MR imageetshows
al. subarachnoid blood in right posterior frontal and parietal sulci (short
arrows) and subtle edema involving underlying cortex (long arrows).
Downloaded from www.ajronline.org by 125.167.98.100 on 01/14/18 from IP address 125.167.98.100. Copyright ARRS. For personal use only; all rights reserved

A B C
Fig. 2—28-year-old woman with postpartum angiopathy who presented with severe headaches, obtundation, and right-sided weakness 1 week after delivery.
A, Unenhanced head CT image shows subarachnoid blood in left Sylvian fissure (long arrow) and bilateral basal ganglia hemorrhages (short arrows).
B, FLAIR MR image shows basal ganglia hemorrhages (short arrows) and subarachnoid hemorrhage (long arrows) as regions of hyperintense signal abnormality.
C, Cerebral angiogram shows discrete focal narrowing of anterior division branch of right middle cerebral artery (arrows).

Fig. 3—31-year-old woman

with reversible cerebral
vasoconstriction syndrome who
presented with 3-day history of
severe headache beginning 1 day
after normal delivery. She fully
recovered within 2 weeks.
A, Axial FLAIR image at level of
centrum semiovale shows small
focus of subarachnoid blood
(arrow) in mesial parietal sulcus.
B, Catheter angiogram shows
discrete irregularities involving
distal left parietal branches of
middle cerebral artery (arrows).
A B

34 AJR:206, January 2016

 Neuroimaging of Pregnancy and Puerperium
Downloaded from www.ajronline.org by 125.167.98.100 on 01/14/18 from IP address 125.167.98.100. Copyright ARRS. For personal use only; all rights reserved

A B C
Fig. 4—26-year-old woman 1 week postpartum with clinical diagnosis of reversible cerebral vasoconstriction syndrome. Example of high-resolution MRI of vessel wall.
(Courtesy of Hui FK, Cleveland Clinic, Cleveland, OH)
A, Time-of-flight MR angiogram shows multiple irregularities and stenoses of both anterior and middle cerebral arteries (arrows).
B, Axial contrast-enhanced high-resolution fat-suppressed T1-weighted MR image at level of origin of middle cerebral artery shows subtle regions of contrast
enhancement of arterial walls (arrows) corresponding to abnormalities in A.
C, MR angiogram obtained 2 weeks after B, after ICU management and considerable clinical improvement, shows resolution (arrows) of stenoses.

A B C

Fig. 5—30-year-old woman with both posterior

reversible encephalopathy syndrome and reversible
cerebral vasoconstriction syndrome.
A, Axial FLAIR MR image shows area of high signal
intensity (arrows) in right occipital and temporal
cortex.
B, DW image corresponding to A shows area of
abnormal high signal intensity (arrows).
C, Apparent diffusion coefficient map shows that
regions corresponding to abnormalities (arrows) in B
are not due to restricted diffusion.
D, Catheter angiogram of right internal carotid artery
shows multiple stenoses (arrows).
E, Catheter angiogram of left vertebral artery shows
additional abnormalities (arrows). Within 3 weeks,
after management in ICU, patient made full recovery.
D E

AJR:206, January 2016 35

 Hacein-Bey et al.
Downloaded from www.ajronline.org by 125.167.98.100 on 01/14/18 from IP address 125.167.98.100. Copyright ARRS. For personal use only; all rights reserved

A B C
Fig. 6—29-year-old woman who became unresponsive after generalized seizure 8 hours after uncomplicated cesarean delivery of her first child.
A, Unenhanced CT image of brain shows air in right carotid terminus (solid arrow) and anterior communicating artery (open arrow).
B, Axial T2-weighted MR image obtained immediately after CT shows area of high signal intensity (arrows) in basal ganglia.
C, DW image from same imaging study as B shows that most of anterior portion of basal ganglia (arrows) does not show diffusion abnormality and does not represent
acute infarction but may, instead, represent vasogenic edema. In contrast, posterior part of basal ganglia shows shine-through phenomenon consistent with more
pronounced vasogenic edema. Patient, who also had signs of posterior reversible encephalopathy syndrome and pituitary apoplexy (not shown), made near-complete
recovery with aggressive medical management. (Reprinted with permission from [65])

A B

Fig. 7—34-year-old woman with dural sinus

thrombosis 2 weeks postpartum.
A, Unenhanced brain CT image shows increased
attenuation in right sigmoid sinus (arrows).
B, Axial T2-weighted MR image shows area of
low signal intensity (arrows) in right sigmoid sinus
consistent with early thrombus stage, which can be
mistaken for normally flowing blood.
C, Axial unenhanced T1-weighted MR image
shows area of high signal intensity (arrows) in right
sigmoid sinus. In conjunction with low-signal-
intensity appearance of thrombus in B, findings are
consistent with thrombus in stage of intracellular
methemoglobin.
D, Coronal contrast-enhanced T1-weighted MR
image shows filling defect (arrow) in right sigmoid
sinus, consistent with thrombus.
C D

36 AJR:206, January 2016

 Neuroimaging of Pregnancy and Puerperium

Fig. 8—38-year-old woman 5 days postpartum with

severe right-sided neck pain and headaches due to
multiple arterial dissections and venous thrombosis.
Downloaded from www.ajronline.org by 125.167.98.100 on 01/14/18 from IP address 125.167.98.100. Copyright ARRS. For personal use only; all rights reserved

Patient has evidence of fibromuscular dysplasia.

A, Axial diffusion-weighted MR image shows small
right cerebellar infarct (arrow).
B, Axial T2-weighted MR image shows right
cerebellar infarct (arrowhead), thickening of right
carotid arterial wall (short arrow) consistent with
dissection, and thrombus in left jugular vein (long
arrow).
C, Anteroposterior cerebral angiogram of right
internal carotid artery shows pseudoaneurysm
(arrow) consistent with dissection.
D, Anteroposterior cerebral angiogram of right
vertebral artery shows two pseudoaneurysms
(arrows).

A B

C D

AJR:206, January 2016 37

 Hacein-Bey et al.

Fig. 9—29-year-old woman who was 7 months

pregnant when she experienced generalized tonic-
clonic seizure from first hemorrhagic event caused by
left hippocampal cavernoma.
A, Axial T1-weighted MR image shows hyperintense
rim of recent hemorrhage consistent with
intracellular methemoglobin (arrowhead) around
isointense round cavernoma (arrow).
Downloaded from www.ajronline.org by 125.167.98.100 on 01/14/18 from IP address 125.167.98.100. Copyright ARRS. For personal use only; all rights reserved

B, Axial T2-weighted MR image shows moderately

hyperintense rim of hemorrhage (arrowhead) and
hypointense round cavernoma with blood products
(arrow) of older age.

A B

38 AJR:206, January 2016