Abstract
BACKGROUND
Hemorrhagic stroke during pregnancy can cause devastating outcomes in women with moyamoya disease (MMD). The bleeding risk associated with choroidal anastomosis, a unique collateral manifestation of MMD, remains unknown in the context of pregnancy.
OBSERVATIONS
A 29-year-old woman with asymptomatic MMD became pregnant. She had not undergone bypass surgery, and choroidal anastomosis had developed in the right hemisphere. After an uneventful pregnancy for 34 weeks, she suddenly manifested HELLP (hemolysis, elevated liver enzymes, and low platelets) syndrome and underwent an emergency cesarean section. Although both she and her neonate remained healthy, MR angiography after delivery revealed on the choroidal anastomosis a small aneurysm, which had been absent before conception, with the possible finding of minor bleeding. After recovering from HELLP syndrome, she underwent direct bypass surgery, which resulted in the disappearance of the aneurysm and marked reduction of the choroidal anastomosis.
LESSONS
Choroidal anastomosis may carry a potential risk of aneurysm formation causing bleeding and should be carefully monitored with noninvasive imaging modalities during the antenatal and postpartum periods.
Keywords: moyamoya disease, pregnancy, intracranial hemorrhage, choroidal anastomosis, intracranial aneurysm, case report
ABBREVIATIONS: DSA = digital subtraction angiography; HDP = hypertensive disorders of pregnancy; HELLP = hemolysis, elevated liver enzymes, and low platelets; ICA = internal carotid artery; MMD = moyamoya disease; MRA = MR angiography; STS-MIP = sliding-thin-slab maximum-intensity-projection
Moyamoya disease (MMD) is a cerebrovascular disease characterized by stenosis or occlusion of the terminal portion of the internal carotid artery (ICA) and abnormal vascular networks.1,2 MMD commonly occurs in women of reproductive age2 and can cause both hemorrhagic and ischemic stroke during pregnancy, including the antenatal, intrapartum, and postpartum periods.3,4 According to single-center studies, pregnancy in MMD can safely be managed overall, especially when the pregnant women have already undergone bypass surgery.4–11 On the other hand, nationwide research has revealed a potential risk of pregnancy-associated stroke in MMD.3,12,13 Hemorrhagic stroke is more closely related to poor prognosis and fatal sequelae than ischemic stroke in pregnancy in MMD.3,10,14 Hemorrhagic stroke is prone to occur during the antepartum period, especially at or beyond 24 weeks.4 However, the mechanism of occurrence of hemorrhagic stroke during pregnancy in MMD remains unknown. Furthermore, the management for preventing perinatal hemorrhagic stroke has not been sufficiently addressed.
Choroidal anastomosis, a hemorrhage-prone collateral manifestation detected with digital subtraction angiography (DSA) and MR angiography (MRA), is attracting increasing attention as a predictor of hemorrhage in MMD.15–18 Even in asymptomatic MMD, approximately one-third of adult patients without surgery manifest choroidal anastomosis.19 Here, we describe a patient with asymptomatic MMD in whom a de novo peripheral aneurysm developed on choroidal anastomosis during the antepartum period in relation to HELLP (hemolysis, elevated liver enzymes, and low platelets) syndrome.
Illustrative Case
A 27-year-old woman who complained of chronic headache was referred to our hospital because MMD was suspected on screening MRI. She had undergone vaginal delivery of her first child and had experienced no ischemic symptoms such as transient ischemic attacks. DSA revealed severe stenosis at the terminal portion of the bilateral ICA with the development of abnormal collateral vessels (Fig. 1A), and she was diagnosed with MMD. Both DSA and sliding-thin-slab maximum-intensity-projection MRA (STS-MIP MRA) in the coronal planes revealed in the right hemisphere a positive finding of choroidal anastomosis, an anastomosis between the anterior choroidal artery and the medial end of the medullary artery (Figs. 1 left and 2A). According to the Suzuki classification, the angiographic stage was classified as stage 3 in the right hemisphere and stage 4 in the left hemisphere. She wished to receive medical treatment and regular MRI follow-ups without bypass surgery because she had experienced no ischemic symptoms.
FIG. 1.
Right internal carotid angiogram revealing choroidal anastomosis, the anastomosis between the anterior choroidal artery (arrows) and the medullary arteries (double arrows), before pregnancy (left) and after delivery with emergency cesarean section (right). Note that a tiny aneurysm on choroidal anastomosis is almost obscured by overlapping vessels (arrowhead).
FIG. 2.
Serial STS-MIP MR coronal angiograms revealing the change in choroidal anastomosis. A: Image obtained before conception, revealing choroidal anastomosis, the anastomosis between the anterior choroidal artery (arrow) and the medullary arteries (double arrow). B: Image obtained on postpartum day 2, revealing small aneurysmal formation (arrowhead) on the choroidal anastomosis. C: Image obtained 24 hours after bypass surgery, revealing bypass flow (double arrowhead) and signal reduction of choroidal anastomosis. D: Image obtained 3 years after surgery, revealing marked reduction of choroidal anastomosis with the disappearance of aneurysm.
At the age of 29 years, her pregnancy was confirmed (gravida 5 parity 1 spontaneous abortion 3). MRI and MRA performed immediately before conception had revealed no new findings. Careful pregnancy checkups by both gynecologists and neurosurgeons were indicated. Her pregnancy course was uneventful with normal blood pressure until 34 weeks of gestation. Obstetricians, anesthesiologists, and neurosurgeons held a meeting at 32 weeks of gestation, and vaginal delivery with epidural anesthesia was scheduled.
At 34 weeks 5 days of gestation, she presented to our outpatient clinic with a headache and home blood pressure readings showing systolic blood pressure exceeding 160 mm Hg. Her blood pressure was 141/85 mm Hg at the visit, and the neurological examination revealed no abnormal findings. Laboratory data revealed only a slight decrease of platelet count (145,000/μL); however, her urinalysis revealed 3+ protein, and she was admitted as an emergency to the obstetrics ward with a diagnosis of hypertensive disorders of pregnancy (HDP).
On the next day (34 weeks 6 days of gestation), laboratory data revealed acute elevation of liver enzymes (aspartate aminotransferase 360 U/L, alanine aminotransferase 269 U/L), suspected hemolysis (lactate dehydrogenase 753 U/L), and a marked decrease of platelet count (54,000/μL), and she was diagnosed with HELLP syndrome. An emergency cesarean section led to successful delivery, and both the patient and neonate remained healthy without any deficits. However, the formation of a new aneurysm was detected at the anastomosis site between the choroidal and medullary arteries by STS-MIP MRA (Fig. 2B) performed during postpartum screening on day 2. Although the patient manifested no symptoms, susceptibility-weighted imaging performed at the same time also revealed a new small low-intensity area around the aneurysm, indicating a possible intraparenchymal or intramural hematoma (Fig. 3). A head CT scan revealed no apparent intracranial hemorrhage. DSA was performed thereafter, and the aneurysm was also observed; however, it was almost obscured in 2D images by overlapping vessels (Fig. 1B). According to the Suzuki classification, the right hemisphere remained at stage 3, and no apparent disease progression was observed.
FIG. 3.
Susceptibility-weighted image revealing a new small low-intensity area around the aneurysm, indicating possible intraparenchymal or intramural hematoma.
The patient underwent direct bypass surgery (superficial temporal artery–middle cerebral artery anastomosis) for the right hemisphere to prevent subsequent hemorrhage, 3 months after delivery, following complete recovery from HELLP syndrome. The choroidal anastomosis was targeted by bypass to enhance the early preventive effect against hemorrhage. The postoperative course was uneventful. STS-MIP coronal MRA performed on day 1 revealed early reductive change of both the aneurysm and choroidal anastomosis with good patency of the bypass (Fig. 2C). The marked reduction of choroidal anastomosis and disappearance of the aneurysm were confirmed with STS-MIP coronal MRA performed 3 years after surgery (Fig. 2D). The patient has remained free from subsequent bleeding for 5 years after surgery and is grateful for having safely delivered her baby.
Informed Consent
The necessary informed consent was obtained in this study.
Discussion
Observations
The present case report describes the sudden emergence of an aneurysm on choroidal anastomosis, confirmed by serial radiological images before and after HELLP syndrome. As of this writing, this is the first report to confirm de novo aneurysm formation on choroidal anastomosis during pregnancy in MMD. We found only one Japanese article describing a ruptured choroidal artery aneurysm in a pregnant woman with MMD;20 however, their case did not undergo a radiological assessment before pregnancy because she had not been diagnosed with MMD.
The relationship between choroidal anastomosis and hemorrhagic stroke has rarely been addressed in the context of pregnancy in MMD, probably due to little recognition of choroidal anastomosis. Accordingly, we reviewed 11 articles (12 events) illustrating hemorrhagic stroke in pregnant women with MMD, in which DSA results of sufficient quality were available (Table 1).10,20–29 Interestingly, choroidal anastomosis was attributable to hemorrhage in 8 of 12 events (66.7%). This suggests the potential impact of choroidal anastomosis on hemorrhagic stroke in pregnancy.
TABLE 1.
Summary of the literature on hemorrhagic stroke in pregnant women with MMD with DSA results of sufficient quality
| Case No. | Authors & Year | Age (yrs) | Hemorrhage Site | Choroidal Anastomosis | Responsible Vessel | Wk of Onset | Complication | Surgical Treatment (wks) | Mode of Delivery (wks) | Outcome* |
|---|---|---|---|---|---|---|---|---|---|---|
| 1 | Hashimoto et al., 198822 | 24 | IVH (atrium) | Positive | ChA | 2–23 | None | Bypass (24–27) | VD (39–42) | GR |
| 2 | Shimamoto et al., 199426 | 23 | IVH | Positive | ChA | 30 | None | EVD (30) | CS (30) | VS |
| 3 | Newman & Al-Memar, 199825 | 37 | IVH | Positive | ChA | 30 | None | EVD (30) | VD (34) | GR |
| 4 | Nakai et al., 200221 | 29 | IVH (atrium) | Positive | ChA | 14 | None | None | NA |
D |
| 5 (lt) | Kim et al., 200424 | 26 | IVH (unknown) | Positive | ChA | 28 | None | EVD (28) | VD (30) | GR |
| 5 (rt) | Kim et al., 200424 | 31 | Parieto-occipital lobe | Positive | ChA | 27 | None | Evacuation (27) | VD (35) | MD |
| 6 | Mehrkens et al., 200623 | 25 | IVH (atrium) | Positive | ChA (w/ AN) | 24 | None | EVD (24) | CS (36) | MD |
| 7 | Murakami et al., 201420 | 32 | Atrium, temporal lobe | Positive | ChA (w/ AN) | 24 | None | Evacuation (24); embolization (24) | CS (37) | GR |
| 8 | Liu et al., 201410 | 40 | IVH | Negative | LSA | 40 | None | EVD (40) | NA | NA |
| 9 | Sun et al., 200027 | 36 | Frontal lobe | Negative | ND† | 31 | HDP | Evacuation (31) | CS (31) | D |
| 10 | Williams et al., 200028 | 36 | Frontal lobe | Negative | ND† | 34 | HDP | Evacuation (34) | CS (34) | D |
| 11 | Kakogawa et al., 201129 | 29 | Temporal lobe | Negative | ND† | 39 | HELLP | Evacuation (39) | CS (39) | SD |
AN = aneurysm; ChA = choroidal anastomosis; CS = cesarean section; EVD = external ventricular drainage; IVH = intraventricular hemorrhage; LSA = lenticulostriate anastomosis; NA = not applicable; ND = not determined; VD = vaginal delivery.
* Glasgow Outcome Scale: D = death; GR = good recovery; MD = moderate disability; SD = severe disability; VS = vegetative state.
† Not determined due to hematoma removal before angiography.
HELLP syndrome might be a clue as to the possible mechanism of aneurysm formation in the present case. HELLP syndrome is considered one of the manifestations of HDP, caused by endothelial dysregulation and inflammation.30 Kakogawa et al. reported a case of a pregnant woman with MMD complicated with both hemorrhagic stroke and HELLP syndrome.29 They speculated that hypertension, systemic hemodynamic change, and cerebral vasospasm might cause the bleeding. We consider that endothelial dysfunction and inflammation could also cause aneurysm formation on the fragile site of choroidal anastomosis, and such formation might be one of the possible mechanisms of hemorrhagic stroke during pregnancy in MMD. Tiny aneurysms formed on choroidal anastomosis could be overlooked with 2D DSA because of obscuration by overlapping vessels.
In view of devastating outcomes related to hemorrhagic stroke during pregnancy, it is important to assess the presence or absence of choroidal anastomosis with optimal imaging modalities before pregnancy for women with known MMD. Several studies have revealed that choroidal anastomosis is a strong predictor for hemorrhagic stroke.15,16 More importantly, choroidal anastomosis can be reduced by bypass surgery.31 Several studies including a systematic review have suggested that prior bypass surgery is associated with fewer neurological events in women with MMD.8,11,32 Prophylactic bypass surgery might be considered especially for women both with the desire for childbirth and who develop choroidal anastomosis considering the high prevalence of HDP reported in MMD.4,5 Careful monitoring of choroidal anastomosis, if present, should be considered with noninvasive imaging modalities such as STS-MIP MRA33 during the antenatal and postpartum periods.
While our close collaboration among obstetricians, anesthesiologists, and neurosurgeons led to a successful outcome in the present case, the optimal management strategy and its timing for de novo choroidal artery aneurysms remain unclear. Wiedmann et al. suggested the efficacy of prompt endovascular treatment for ruptured choroidal artery aneurysms.34 Murakami et al. also reported a pregnant woman with MMD, who experienced a ruptured choroidal artery aneurysm and was successfully treated by endovascular treatment.20 On the other hand, our previous study suggests that early reduction of choroidal anastomosis can occur immediately after direct bypass, especially when the anastomosis is to be bypassed.35 The mechanism of and treatment strategy for aneurysms on choroidal anastomosis remain unknown because of the limited number of studies; further studies are required to resolve this issue.
Serial imaging in the present case revealed that the aneurysm on the choroidal anastomosis developed during pregnancy; however, the direct association between aneurysm formation and pregnancy remains unclear. Further studies investigating the effects of pregnancy on choroidal anastomosis are required.
Lessons
The present case report suggests the potential risk of de novo aneurysm formation associated with choroidal anastomosis during pregnancy in MMD. If choroidal anastomosis is present, it should be carefully monitored with noninvasive imaging modalities such as STS-MIP MRA during the antenatal and postpartum period.
Disclosures
Dr. Funaki reported grants from consigned research fund from Nihon Medi-Physics outside the submitted work. Dr. Arakawa reported grants from Philips, Otsuka, Chugai, Nihon Medi-Physics, Daiichi Sankyo, Stryker, Eisai, Japan Blood Products Organization, Ono Pharmaceutical, Taiho Pharma, Sumitomo Dainippon Pharma, Astellas Pharma, Incyte Biosciences, and Servier; and personal fees from Nippon Kayaku, Novocure, UCB Japan, Ono Pharmaceutical, Brainlab, Merck, Chugai, Eisai, Daiichi Sankyo, Carl Zeiss, Nihon Medi-Physics, and Stryker outside the submitted work.
Author Contributions
Conception and design: Funaki, Yokochi. Acquisition of data: Funaki, Chihara. Analysis and interpretation of data: all authors. Drafting the article: Funaki, Yokochi, Chihara. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Funaki. Administrative/technical/material support: Tatsumi.
Correspondence
Takeshi Funaki: Kyoto University Graduate School of Medicine, Kyoto, Japan. tfunaki@kuhp.kyoto-u.ac.jp.
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