ARTICLE IN PRESS

Case Studies

Young Ischemic Stroke in Association with Ovarian
Hyperstimulation Syndrome
Pawani Sachar, MBBS, MD, and Kumar Rajamani, MBBS, MD, DM

Background: Ovarian hyperstimulation syndrome (OHSS) is a serious and potentially fatal complication of medical ovarian stimulation. Uncommonly, it is associated
with thromboembolic complications with venous thrombosis being more common
than arterial thromboembolic events. We present a case of cerebral infarction in
the setting of severe OHSS secondary to in vitro fertilization treatment with no
residual neurological deficits. Materials and Methods: We also performed a review
of previously published ischemic cerebral infarction and cerebral venous sinus
thrombosis (CVST) cases associated with OHSS to evaluate common patterns in
presentations, commonly affected central nervous system sites, trends for therapeutic options in these cases, and outcomes. Conclusion: We have included 27
cases of ischemic cerebral infarction and 7 cases of CVST previously published
in English literature. We have included cases of central retinal artery occlusion
in the ischemic cerebral infarction group, and central retinal vein occlusion in the
CVST group. Mean ages of presentation were 31 ± 4.84 and 34 ± 4.90 years for ischemic cerebral infarction and CVST, respectively. Ischemic strokes commonly affect
large cortical areas with unilateral weakness, aphasia, unilateral sensory changes,
and visual field deficits being the common presentations. Middle cerebral artery
(n = 7) is the common site of vascular occlusion where vascular imaging has been
reported, followed by internal carotid artery occlusion (n = 5). OHSS cannot be
considered a direct risk for pathogenesis, but OHSS is frequently associated with
hyperviscosity, which may add to the risk factors. Key Words: Ovarian
hyperstimulation syndrome—ischemic stroke—in vitro fertilization—cerebral venous
sinus thrombosis.
© 2016 Published by Elsevier Inc. on behalf of National Stroke Association.

Case Report
A previously healthy 36-year-old right-handed Caucasian woman presented with an episode of right upper
From the Department of Neurology, Detroit Medical Center/
Wayne State University, Detroit, MI.
Received December 7, 2015; revision received April 9, 2016; accepted
April 27, 2016.
Address correspondence to Pawani Sachar, MBBS, MD, Department
of Neurology, Detroit Medical Center/Wayne State University, Detroit,
MI 48201. E-mail: pawani_sachar@yahoo.com.
1052-3057/$ - see front matter
© 2016 Published by Elsevier Inc. on behalf of National Stroke
Association.
http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2016.04.023

extremity weakness and expressive aphasia lasting for about
15-20 minutes. The patient was undergoing treatment for
infertility and had egg retrieval for in vitro fertilization
(IVF) 7 days prior to the onset of these symptoms. The
patient developed abdominal pain, nausea, malaise, and
dyspnea 2 days after egg retrieval. Abdominal ultrasound confirmed the presence of ascites and ovarian
enlargement, and the patient was diagnosed with ovarian
hyperstimulation syndrome (OHSS). Embryos were not
implanted and were frozen. The result of the neurological exam was normal on initial evaluation (National
Institutes of Health Stroke Scale score of 0). The white
blood cell count was 17 (76% neutrophils, 19% lymphocytes, 6% monocytes); platelet count, 535; hemoglobin level,

Journal of Stroke and Cerebrovascular Diseases, Vol. ■■, No. ■■ (■■), 2016: pp ■■–■■

1

ARTICLE IN PRESS
P. SACHAR AND K. RAJAMANI

2

all of which had been normal. The patient was discharged home with aspirin and simvastatin. Repeat MRA
of the head 2 months later showed improvement of the
left MCA attenuation (Fig 2B).
The patient had mild occipital headaches after discharge, which was associated with mild photophobia. The
patient did not develop any other neurological symptoms. The headaches improved spontaneously. Repeat MRA
head 3 months later showed complete resolution of the
MRA signal attenuation seen on the first study. The patient
has been symptom free for about 6 months after the initial
episode and has been taking aspirin 81 mg daily.

Discussion
Figure 1. Diffusion-weighted magnetic resonance imaging of the brain
showing acute infarction.

17.7; and hematocrit level, 52.5. Serum electrolytes were
also deranged: Na, 130; K, 4.1; CO2, 22; Cl, 100; blood
urea nitrogen, 14, and creatinine, 1.4. Total estrogens level
and total estradiol levels were 2730 and 1520 pg/mL, respectively. Repeat abdominal ultrasound showed an
enlarged liver with moderate to severe ascites. The portal
vein was patent. The patient was found to have a left
posterior insular infarction on magnetic resonance imaging
of the brain (Fig 1), and there was attenuation of the left
middle cerebral artery vasculature on magnetic resonance angiography (MRA) of the head (Fig 2). Magnetic
resonance venography of the head did not show any signs
of venous sinus or cortical vein thrombosis. Fasting lipid
profile showed a low-density lipoprotein level of 58. The
hemoglobin A1c level was 5.3. The rest of the stroke
workup including carotid duplex, 2-D echo, and
telemonitoring were normal. The patient was treated with
aggressive intravenous hydration and albumin infusions and had subsequent improvement in clinical status
and electrolyte abnormalities. Aspirin, simvastatin, and
subcutaneous heparin were started. The patient also had
hypercoagulable workup including antithrombin III, protein
C, protein S, factor V Leiden, antiphospholipid antibodies, beta-2 glycoprotein antibodies, Anti-nuclear Antibodies
(ANA), and Extractable Nuclear Antigen Antibodies (ENA),

OHSS is a serious and potentially fatal complication
of ovarian stimulation for assisted reproduction technologies. Mild forms are common and reported frequencies
for OHSS are approximately 20%-33% for mild cases, 3%6% for moderate cases, and .1%-2.0% for severe cases.
It is a broad spectrum of signs and symptoms that include
abdominal distention and discomfort, enlarged ovaries,
ascites, and other complications of enhanced vascular permeability. The pathophysiology is hypothesized to be
increased capillary permeability with the loss of fluid into
the third space, likely from overexpression of vascular
endothelial growth factor in the ovary and release of
vasoactive–angiogenic substances resulting in functional impairment of blood vessels systemically, often causing
impairment of cardiac, renal, pulmonary, and liver functions. Clinically, OHSS has been classified as mild,
moderate, severe, and critical. Thromboembolic complications are typically seen in the latter 2 forms with venous
thrombosis (64.3%) being more common than arterial
thromboembolic events (37.5%).1
Major risk factors for OHSS are previous episode of
OHSS, polycystic ovary syndrome, and younger age, which
has been reported as a possible risk factor along with
low body weight. Potential biomarkers of risk are a basal
serum anti-Müllerian hormone concentration greater than
3.3 ng/mL and an antral follicle count greater than 8. Secondary risk factors related to ovarian response are the
number of follicles (the risk rises with increasing number

Figure 2. (A and B) Magnetic resonance angiography of the brain showing narrowing of the left middle
cerebral artery with attenuated branches and followup scan 3 months later showing significant improvement.

Previous
thromboembolism

Polycystic
ovaries

Max
estradiol
level (pg/mL)

No. of
mature
follicles

Severity
of OHSS

Days to development
of stroke symptoms

Year

Mozes et al
Rizk et al
Kermode et al

1965
1990
1993

37
30
34

None
None
None

None
None
Yes

NR
NR
NR

NR
NR
NR

Severe
Severe
Severe

5 days post HCG injection
12 days post ET
9 days post ET

Inbar et al
Aurousseau et al
Cluroe et al

1994
1995
1995

22
34
40

None
None
None

Yes
None
None

NR
NR
NR

Multiple
NR
NR

None
None
Severe

7 days post HCG injection
3 days post ET transfer
6 days post ET

Aboulghar et al
Aboulghar et al
Hwang et al

1998
1998
1998

33
25
22

None
None
None

None
None
None

2100
2800
NR

12
16
NR

Moderate
Moderate
Severe

11days post ET
9 days post ET
12 days post ET

El Sadek et al
Yoshii et al
Davies et al
Worrell et al
Turkistani et al
Koo et al

1998
1998
1999
2001
2001
2002

24
26
33
34
34
33

None
None
None
None
None
None

None
None
None
None
None
None

3000
NR
NR
2663
NR
NR

34
NR
NR
NR
NR
NR

Severe
Severe
Moderate
Mild
Moderate
Severe

6 days post ET
NR
NR
7 days post ET
NR
14 days post ET

Elford et al

2002

28

None

None

3132

NR

Severe

7 days post ET

Di Micco et al

2003

32

None

None

3800

NR

Moderate

NR

Togay-Isikay et al

2004

27

None

None

NR

NR

Severe

12 days post IUI

Demirol et al
Giner et al
Marti et al
Bartkova et al

2007
2007
2008
2008

21
35
34
31

None
None
None
None

None
None
None
None

2118
NR
NR
1440

16
NR
NR
NR

None
Severe
Moderate
Severe

2 days post HCG injection
NR
3 days post ET
9 days post ET

Qazi et al
Song et al

2008
2008

30
31

None
None

None
Yes

NR
4300

NR
NR

Severe
Severe

NR
NR

Jing et al
Gervasi et al
Current case

2011
2012
2013

30
34
36

None
None
None

None
Yes
None

4267
NR
1520

13
NR

Severe
Severe
Severe

7 hours post ET
7 days post HCG injection
8 days post HCG injection

Stroke symptoms
Left hemiplegia, coma
Left hemiplegia, left hemisensory loss, left hemianopsia
Right hemiplegia, right hemisensory loss, right
hemianopsia, aphasia, left-sided Horner seizure
Headache, nausea, amnesia, dysarthria
Left hemiplegia
Left hemiplegia, left hemisensory loss, right gaze deviation,
left tongue deviation, lethargy
Left hemiparesis
Left hemiparesis, seizure
Left hemiparesis, left facial weakness, left hemisensory
loss, dysarthria
Right hemiparesis
Left hemiparesis, dysarthria,
Left hemiparesis, headache
Right hemiparesis, aphasia
Left unilateral visual loss
Left hemiparesis, Left visual field deficit, right gaze
preference, left hemineglect, dysarthria
Left hemiplegia, left facial weakness, dysarthria,
drowsiness
Right hemiplegia, right facial weakness, right visual field
deficit
Sensory loss left face, right hemisory loss, ataxia, Horner
syndrome, nystagmus
Right hemisensory loss, aphasia, disorientation
Right hemiparesis, aphasia
Left visual loss
Left hemiparesis, left facial weakness, right head deviation,
left sided gaze palsy, drowsiness
Left hemiparesis, dysarthria
Left hemiparesis, left facial weakness, left visual field
deficit, nystagmus
Right hemisensory loss, aphasia, disorientation, dizziness
Right hemiparesis, aphasia
Right upper extremity weakness, aphasia
(continued on next page)

ARTICLE IN PRESS

Author

Age
(years)

ISCHEMIC STROKE ASSOCIATED WITH OHSS

Table 1. Ischemic cerebral infarction cases

3

Area of cerebral
infarction on imaging

Author
Mozes et al

NR

Rizk et al
Kermode et al

Right MCA territory
Left frontal and parietal

Inbar et al
Right temporoparietal
Aurousseau et al NR

Left extracranial ICA
occlusion with
intracranial extension
No abnormalities
NR

Other sites of
thrombosis
None

None
Right internal
iliac vein
No abnormalities
None
Right ICA dissection and None
thrombosis
NR
None
NR
None
NR
None
Right MCA occlusion
Myxomatous mitral valve
Left choroidal artery
None
occlusion
Right ICA occlusion
None

Turkistani et al
Koo et al

Central retinal artery occlusion NR
Right MCA territory
Right MCA occlusion

None
None

Elford et al

Left MCA territory

Left MCA occlusion

None

Di Micco et al
Togay-Isikay
et al
Demirol et al
Giner et al

NR
Bilateral PICA territory

Left ICA occlusion
Left vertebral occlusion

None
None

Left MCA territory
Left parietal, left lenticular
nucleus, right caudate
Left thalamus

Left MCA occlusion
NR

None
See below

Central retinal artery
occlusion
Left MCA occlusion
Carotid atherosclerosis
No abnormalities

None

Yoshii et al

Marti et al
Bartkova et al
Qazi et al
Song et al
Jing et al
Gervasi et al

Left basal ganglia
Right MCA territory
Right MCA territory, left
cerebellum
Left MCA territory
Left fronto-temporal-occipital

Current case

Left insula

NR
None
Left distal ICA occlusion Intracardiac thrombus

Left MCA occlusion
NR
Left MCA occlusion

None
None
None

Maternal outcome

Fetal outcome

Treatment

NR

Death

No pregnancy

Mechanical
thrombectomy

NR
NR

Term delivery
No pregnancy

Aspirin
NR

None
None

Recovery
Residual motor and speech
deficits
Recovery
Recovery

No pregnancy
Aspirin
Therapeutic abortion Heparin

NR
None
None
None
None

Death
Recovery
Recovery
Residual motor deficits
Recovery

No pregnancy
No pregnancy
No pregnancy
Therapeutic abortion
No pregnancy

Temporary elevation of TAT
and D-dimer, temporary
reduction of protein S

Recovery

Therapeutic abortion NR

None
Mildly decreased protein S

Recovery
Residual motor and speech
deficits
NR
Residual motor deficits

NR
Spontaneous
miscarriage
Preterm labor
Therapeutic abortion

None
Low protein S and high IgM
anticardiolipin antibodies
None

Residual motor, visual, and Normal vaginal
sensory deficits
delivery
None
Improvement, not specified No pregnancy
Activated protein C resistance, Residual motor deficits
NR
factor V Leiden mutation
None
Recovery
No pregnancy
Antiphospholipid antibody
Recovery
No pregnancy
syndrome
None
Residual visual deficits
No pregnancy

None
None
Temporarily low protein S and
antithrombin III
None
homozygosity
Left ventricular thrombus, MTHF reductase variant
tetralogy of Fallot
None
None

Recovery
Recovery
Residual motor and speech
deficits
Residual unknown deficits
NR
Recovery

NR
Heparin
Heparin
NR
Heparin- > aspirin

NR
tPA, heparin> warfarin
Heparin
NR
intra-arterial tPA,
dalteparin
Heparin- > aspirin
Heparin, aspirin

Aspirin, warfarin
Anticoagulation,
not specified
Heparin- > warfarin> aspirin
Term delivery
Heparin- > aspirin
No pregnancy
Heparin, aspirin
Therapeutic abortion Heparin- > aspirin
NR
NR

Ozagrel, aspirin
NR

No pregnancy

Aspirin, heparin

Abbreviations: ET, embryo transfer; HCG, human chorionic gonadotrophin; ICA, internal carotid artery; IUI, Intra-uterine Insemination; MCA, middle cerebral artery; MTHF, methylenetetrahydrofolate; NR, not reported; OHSS, ovarian
hyperstimulation syndrome; PICA, posterior inferior cerebellar artery; tPA, tissue plasminogen activator.

P. SACHAR AND K. RAJAMANI

Davies et al
Worrell et al

Right MCA territory
Cortical area, not specified
Left parieto-occipital
Right MCA territory
Left basal ganglia and corona
radiata
Right internal capsular,
bilateral corona radiata,
bilateral parietal, right
occipital
Right MCA territory
Left MCA territory infarction

Coagulation
abnormalities

ARTICLE IN PRESS

Cluroe et al
Aboulghar et al
Aboulghar et al
Hwang et al
El Sadek et al

Vascular imaging
findings

(continued)

4

Table 1.

OHSS

Days to development
of stroke symptoms

Waterstone et al
Tang et al
Ou et al
Edris et al

1992
2000
2003
2007

29
34
29
38

None
None
None
None

None
None
None
None

NR
5668
3707
3346

2
NR
7
16

Severe
Severe
Moderate
Severe

12 days post HCG injection
14 days post ET
9 days post ET
4 days post ET

Lee et al
Santoro et al

2008
2009

36
31

None
None

None
None

NR
NR

NR
NR

None
Moderate

NR
NR

Man et al

2011

42

None

None

2616

NR

Severe

1 day post HCG injection

Vascular imaging
findings

Waterstone et al

NR

Right transverse sinus,
internal cerebral
vein, vein of Galen
Cortical vein

Tang et al

Left frontal
hemorrhagic
infarction

Ou et al

Right frontal, left
frontoparietal

Superior sagittal sinus

Edris et al

Periventricular
white matter

Lee et al

None

Santoro et al

NR

Man et al

Right frontal

Superior sagittal sinus,
transverse sinus,
cortical veins
Central retinal vein
occlusion
Rectal sinus,
transverse venous
sinus
Superior sagittal sinus,
right cortical veins

Other sites of
thrombosis

Coagulation
abnormalities

Stroke symptoms
Left hemiplegia, seizure, coma
Right hand weakness, seizure
Left hemiplegia, seizures
Headache, lethargy, confusion,
neck pain
Right visual loss
Hemiparesis unknown side,
headache, visual complains
Left hemiparesis, headache

Maternal
outcome

Fetal outcome

Treatment

None

NR

Residual motor
deficits

Spontaneous
miscarriage

Heparin- > warfarin

Inferior vena cava,
right common iliac,
left femoral and left
external iliac
None

No abnormalities

Recovery

Therapeutic
abortion

Heparin- > warfarin

Temporarily low
protein S

Residual motor
deficits, seizures

Term delivery

None

No abnormalities

Recovery

No pregnancy

Mechanical
thrombectomy,
urokinase- >
heparin
Heparin- > warfarin

None

No abnormalities

NR

NR

NR

None

G20210A prothrombin
mutation

Recovery

NR

Heparin- > warfarin

None

No abnormalities

NR

NR

Heparin

Abbreviations: ET, embryo transfer; HCG, human chorionic gonadotrophin; NR, not reported; OHSS, ovarian hyperstimulation syndrome.

ARTICLE IN PRESS

Year

Author

Polycystic
ovaries

No. of
mature
follicles

Author

Area of cerebral
infarction on
imaging

Previous
thromboembolism

Max
estradiol
level (pg/mL)

Age
(years)

ISCHEMIC STROKE ASSOCIATED WITH OHSS

Table 2. Venous cerebral infarction cases

5

ARTICLE IN PRESS
P. SACHAR AND K. RAJAMANI

6

of follicles >20 over 10 mm in diameter) and high (or
rapidly rising) serum estradiol concentration. In 1 study,
the incidence of OHSS in women with preovulatory serum
estradiol concentrations greater than 3500 pg/mL or greater
than 6000 pg/mL was 1.5% and 38%, respectively. The
commonly affected sites are the deep extremity veins, the
internal jugular vein, and the subclavian vein. Mozes et al
reported a fatal case of ischemic stroke associated with
severe OHSS in 1965,2 and there have been several other
reports of ischemic cerebral infarction and cerebral venous
sinus thrombosis (CVST) since then. We present another
case of cerebral infarction in the setting of OHSS with
no residual neurological deficits. We also performed a
review of previously published ischemic cerebral infarction and CVST cases to evaluate common patterns in
presentations, commonly affected central nervous system
sides, trends for therapeutic options in these cases, and
outcomes.
We have included 27 cases of ischemic cerebral
infarction1-25 and 7 cases of CVST26-32 previously published in English literature (Tables 1, 2). We have included
cases of central retinal artery occlusion in the ischemic
cerebral infarction group and central retinal vein occlusion in the CVST group. The mean ages of presentation
were 31 ± 4.84 and 34 ± 4.90 years for ischemic cerebral
infarction and CVST, respectively. Ischemic strokes commonly affect large cortical areas with unilateral weakness,
aphasia, unilateral sensory changes, and visual field deficits being the common presentations. The middle cerebral
artery (n = 7) is the common site of vascular occlusion
where vascular imaging has been reported, followed by
internal carotid artery occlusion (n = 5). Posterior circulation is rarely affected with only 1 reported case of
vertebral occlusion.19 Ischemic strokes usually occur in
association with moderate–severe OHSS (~85%), but there
has been 1 case reported with mild OHSS and 3 cases
without OHSS. These cases without OHSS happened also
after IVF or ovulation induction without any determined etiology. By contrast, venous sinus thrombosis has
always been associated with moderate–severe OHSS. The
maximum serum estradiol level reported is 2831 ± 1000 pg/
mL in ischemic strokes and 3834 ± 1304 pg/mL in CVST.
The exposure to higher levels of estrogens in the
women with other potential risk factors is the likely
pathogenesis in these cases. In fact, other concomitant
hypercoagulable risk factors have been found in 7 cases
of ischemic strokes and in 2 cases of CVST. The true prevalence of hypercoagulable risk factors in these patients
is difficult to estimate due to small numbers and as
some of the case reports have not reported any testing
for them.
It is difficult to definitely draw conclusions as very few
of the reported cases of OHSS with ischemic stroke and
CVST in our review were found to have concomitant coagulation abnormalities, primarily because of lack of
hypercoagulability testing in the majority of the cases.

Out of 22 cases of ischemic stroke, 2 patients had mild
protein S deficiency; 1 patient had protein S deficiency
along with high anticardiolipin antibodies; 1 patient had
protein C resistance along with factor V Leiden mutation; and 1 patient had antiphospholipid antibody
syndrome. In patients with CVST and OHSS, 1 patient
had temporarily low protein S deficiency and another
patient had a G20210A prothrombin gene mutation. Because
thromboembolic complications are relatively rare, routine
screening for thrombophilia in women planning to undergo
ovarian stimulation is not recommended. It is debatable
whether women with an underlying known thrombophilia should receive prophylaxis or not prior to ovulation
induction to prevent thromboembolic complications. OHSS
is frequently associated with hyperviscosity, which may
add to the risk factors. As there have been such few reports
of high prevalence of inherited thrombophilias in patients with OHSS,33,34 whether it is cost effective to screen
all women undergoing ovarian stimulation for these conditions is debatable.35 We will suggest, though, a detailed
discussion with the patients planning for IVF or ovulation induction who may have known risk factors.
Therapeutic options have been varied in the past with
no particular trends. Two patients were treated with intravenous tissue plasminogen activator without any
significant complications. All ischemic strokes in the acute
setting should be treated with thrombolytics and/or mechanical intervention as per American Heart Association
guidelines.36 Secondary stroke prophylaxis in these cases
is debatable. Previously antiplatelets, warfarin, and heparin
products have been used in various regimens. Our patient
has done well with only aspirin, and we will recommend an individualized approach on a case-to-case basis.
About 48% of the ischemic stroke patients experienced
complete recovery and 7% (n = 2) of the patients died.
This outcome can be considered relatively good considering that most of these patients had large hemispheric
strokes.

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