Introduction Aneurysms of lenticulostriate artery (LSA) perforators are uncommon. There are few data on their natural history, and opinions differ on the treatment strategies.
Objective We report a case series and summarize the most recent literature with current treatment recommendations. We propose an anatomical classification for these entities.
Methods A retrospective review of all patients who were diagnosed with an LSA aneurysm on cerebral angiogram was performed. An extensive online literature search was performed to identify other studies reporting on the diagnosis and management of ruptured and unruptured lenticulostriate aneurysms.
Results 48 cases were identified in the literature and reviewed: 27 patients were treated surgically; five cases were treated with endovascular therapy; two cases underwent gamma knife radiosurgery; and 13 cases were managed conservatively. We classified these aneurysms into three types: type 1 describes aneurysms arising from the middle cerebral artery next to a perforating LSA; type 2 is an LSA aneurysm from which the perforating artery or arteries arise—the type 2A subtype is one in which the aneurysm neck incorporates the origin of the perforating arteries and the type 2B describes perforating arteries arising from the dome of the aneurysm; and type 3 describes a fusiform aneurysm beyond the first loop or turn of an LSA.
Conclusions LSA aneurysms are rare entities that present several treatment challenges. We have summarized the cumulative experience with these lesions and proposed a classification scheme that has treatment implications.
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Aneurysms of lenticulostriate artery (LSA) perforators are uncommon. There have only been 48 cases reported in the literature, both ruptured and unruptured. They often present as intracerebral hemorrhage (ICH) or subarachnoid hemorrhage (SAH), and have been associated with hypertension,1–4 arteriovenous malformations (AVM),5–7 systemic lupus erythematosus,8 and moyamoya disease.2 ,9–16 Due to their rarity, there are few data on their natural history, and opinions differ on the treatment strategies. A variety of treatment options have been reported. Given the paucity of information regarding these lesions, there are many questions to be answered regarding the best approach to treatment.
We report a case series from a high volume tertiary care center. We review eight cases of patients presenting with lenticulostriate aneurysms and their management and outcome. We summarize the most recent literature and current treatment recommendations, and propose an anatomical classification for these entities.
A retrospective review of all patients who were diagnosed with an LSA aneurysm on cerebral angiogram was performed over a 2 year period from December 2011 to February 2013. Five patients were identified at our institution, with an additional three provided by the Cleveland Clinic. The medical charts, conventional angiographic and non-invasive imaging data, and procedural reports were reviewed.
An extensive online literature search was performed to identify other studies reporting on the diagnosis and management of ruptured and unruptured lenticulostriate aneurysms. Online databases available through our institution, including PubMed and Medline, were searched using keywords ‘lenticulostriate aneurysm’. We reviewed angiographic data from both English and non-English studies.
Case No 1
A woman with a history of hypertension presented to the hospital after having an acute onset of the worst headache of her life, nausea, and photophobia. Her neurological examination was non-focal. A non-contrasted head CT demonstrated diffuse SAH (figure 1A). CT angiography revealed a 5 mm lobular anterior communicating artery aneurysm which was presumed to be the cause of her SAH, as well as a 3×2 mm right M1 aneurysm (figure 1B). She underwent formal angiography and coil embolization of her anterior communicating artery aneurysm, and demonstrated that the right M1 aneurysm had associated prominent LSAs arising directly from the aneurysm neck, as confirmed by aneurysmogram (figure 1C). She was ultimately discharged home with an intact neurological examination. Her unsecured LSA aneurysm is being managed conservatively, with possible planned angiographic surveillance in 1 year.
Case No 2
A man with no past medical history presented to an outside hospital with headaches. A non-contrasted head CT revealed right temporal lobe parenchymal hematoma with intraventricular extension. He was transferred to our facility for further care. On evaluation he was awake and alert with a slight left-sided pronator drift and an otherwise non-focal neurological examination. A CT angiogram was performed which demonstrated stable hematoma, but no vascular abnormality to explain his hematoma. The patient underwent formal cerebral angiography which revealed a 1 mm medial LSA aneurysm. This was felt to be the cause of the patient's intracerebral hematoma. Given the aneurysm's small size, it was not amenable to endovascular therapy, and a conservative approach was adopted with serial imaging. On hospital day 4, the patient was transferred out of the neurosciences intensive care unit and to the floor. One day later the patient was discharged home with a non-focal neurological examination. The patient underwent a repeat cerebral angiogram approximately 1 month after discharge, which demonstrated resolution of the right LSA aneurysm.
Case No 3
A woman with a past medical history of hypertension presented to the emergency department with a sudden onset of the worst headache of her life. A non-contrasted head CT demonstrated SAH (figure 2A). On examination the patient complained of nausea and vomiting, and headaches, but had a non-focal examination. A CT angiogram showed multiple intracranial aneurysms—two arising from the anterior communicating artery, one projecting from the cavernous portion of the right internal carotid artery, a right middle cerebral artery (MCA) anterior temporal branch aneurysm, a right MCA bifurcation aneurysm, a left cavernous internal carotid artery aneurysm, and a left MCA bifurcation aneurysm. On further review, the right MCA anterior temporal branch aneurysm arose from the dorsal side of the horizontal M1 segment and was noted to incorporate a right LSA (figure 2B). Given the pattern of subarachnoid blood, the anterior communicating artery aneurysms were suspected to be the cause of her hemorrhage. She underwent embolization of both her anterior communicating artery aneurysms. She subsequently recovered from her SAH and was discharged from hospital on day 9. She underwent endovascular embolization of her right MCA bifurcation aneurysm approximately 6 months later. At that time, attempts were made to embolize the right LSA aneurysm but this was unsuccessful as the coils immediately prolapsed into the parent artery. Thus she underwent elective supraorbital craniotomy for surgical clipping.
Intraoperatively, the carotid artery was dissected distal to the terminus and then off the MCA. The anterior temporal artery branch was identified along with a 3–4 mm aneurysm associated with it. Adjacent was a large LSA. The aneurysmal neck was occluded using a Peter-Lazic (Tuttligen, Germany) bayonetted miniclip. The patient recovered well from the procedure and was discharged home the following day. Following this, the patient underwent embolization of her left-sided MCA and carotid cave aneurysms 3 months later. She was discharged home the following day with an intact neurological examination.
Case No 4
A man with a history of hypertension was referred to our institution for evaluation of multiple intracranial aneurysms found on MR angiography during workup for trigeminal neuralgia (figure 3A). He underwent formal cerebral angiography which revealed left paraophthalmic, left M2 bifurcation middle cerebral, and right M1 segment MCA aneurysms. On further review the right M1 aneurysm was found to incorporate the origin of the perforator aneurysm (figure 3B, C). The patient underwent balloon assisted embolization of the left MCA bifurcation and left paraophthalmic artery aneurysms 1 month later. He did well postprocedurally and was discharged home with a non-focal neurological examination. He returned for elective balloon assisted coiling of his right LSA aneurysm approximately 1 week later. He tolerated this well, and was discharged home on hospital day 1 at his neurological and functional baseline.
Case No 5
A woman with a history of hypertension was referred to clinic for evaluation of a basilar tip aneurysm found during workup for trigeminal neuralgia. Formal angiography revealed a basilar tip aneurysm and two M1 aneurysms. The more proximal aneurysm measured 2.5×2 mm and arose from the MCA with the LSAs remodeled around the aneurysm. The patient underwent stent assisted coiling of both aneurysms approximately 1 month later. She was discharged home at her neurological and functional baseline.
Case No 6
A man presented to an outside hospital after collapsing. CT of the head on arrival demonstrated diffuse SAH. He was transferred to our facility for further care and underwent ventriculostomy placement on arrival secondary to lethargy and mild hydrocephalus. Cerebral angiography performed on the day of admission revealed a 2 mm right-sided M1 aneurysm. An attempt to coil the aneurysm was unsuccessful and complicated by contrast extravasation from the dome. The coil attempt was aborted and he was taken to the operating room for successful microsurgical clipping of the aneurysm on post bleed day 1. His stay in the neurological intensive care unit was complicated by vasospasm that required intervention via angiography on two occasions but the patient's neurologic status improved significantly and he eventually had his ventriculostomy removed. He was discharged to a rehabilitation facility on post bleed day 15, and at the time was neurologically intact.
Case No 7
A woman with a past medical history of hypertension was initially worked up as an outpatient for her complaints of headaches and was found to have multiple intracranial aneurysms, including a right M1 aneurysm, two posterior cerebral artery aneurysms, and a basilar tip aneurysm. She had elective stent assisted coil embolization of the posterior cerebral artery aneurysms followed by stent assisted coil embolization of her M1 aneurysm in 2008. She was admitted to the neurosurgery service in December 2008 after suffering a rupture of her basilar tip aneurysm, which was subsequently coil embolized on admission. She had a ventriculostomy placed during this hospitalization, which was eventually removed and she was ultimately discharged to a rehabilitation facility.
Case No 8
A man who developed tremor, balance trouble, and visual disturbances was worked up by a neurologist and was found to have multiple intracranial aneurysms, including a 6 mm right MCA trifurcation, a 3.2 mm left MCA bifurcation, and a 3.3 mm left M1 aneurysm. He was taken for an elective right-sided craniotomy for successful clip of the right MCA aneurysm. Nine months later he underwent a left pterional craniotomy for elective clipping of his left-sided aneurysms. The second procedure was complicated by an M1 perforating artery occlusion and infarct that left him with dysphagia, confusion, and right-sided weakness. Hospitalization was also complicated by postoperative meningitis and bacteremia that were successfully treated with aggressive antibiotics. He was eventually discharged to a skilled nursing facility with residual right-sided deficits that are stable on the most recent follow-up, 8 years later.
Forty-eight cases were identified in the literature and reviewed. Twenty-three (48%) were male, 21 (44%) were female. Four (8%) cases did not have gender data available. Mean age was 38 (±18.5) years. Thirty-six (75%) patients presented with an intracranial hemorrhage, of which two were isolated intraventricular hemorrhages. Fifteen (31%) patients presented with SAH, 13 (30%) of which were presumed to have been caused by a ruptured LSA aneurysm. Three cases had multiple LSA aneurysms. In two cases the LSA aneurysm was discovered incidentally, one in a patient with an unruptured AVM and the second in a patient with moyamoya disease. One patient presented with ischemic strokes from a thrombosed LSA aneurysm. Another patient with superficial temporal artery to MCA bypass performed 10 years earlier was found to have an LSA aneurysm during workup for new onset gait imbalance. Six presented with hypertension, one of which was due to cocaine use. Four patients had associated AVMs. Three patients had a history of moyamoya disease or had moyamoya-like vasculature. One patient was diagnosed with a neurocytoma near the location of an LSA aneurysm. These findings are summarized in table 1.
Twenty-seven patients were treated surgically. Sixteen cases underwent clipping; five of these cases reported parent artery vessel sacrifice. Eleven patients underwent vessel clipping and aneurysm excision. One case presented with an intracranial hemorrhage which was observed but 14 days later the patient declined and was found to have a rebleed. They subsequently underwent a craniotomy for clipping and excision. Five cases were treated with endovascular therapy. Of these, three used n-butyl-2-cyanoacrylate and two used Onyx liquid embolic material (ev3, Irvine, California, USA). In one case, endovascular therapy was intended, but the lesion had disappeared on repeat angiogram. Thirteen cases were managed conservatively. Two of these cases died before any intervention could be performed. Two cases included a patient who underwent an emergent craniotomy for an intracranial hemorrhage. Delayed imaging demonstrated LSA aneurysms in both cases and were subsequently managed conservatively. One case demonstrated near complete resolution on repeat imaging 3 weeks later. Of the patients treated conservatively, seven cases demonstrated spontaneous resolution of their LSA aneurysm. Angiographic follow-up for conservatively managed patients ranged from 4 days to 2 years.
Three patients died during their hospital stay. Five patients suffered rebleeds, one of which was during initial angiography. Another patient suffered rerupture before surgical treatment. Six patients had postprocedure infarcts. One patient developed a facial droop after surgery which resolved by discharge. Two patients suffered vasospasm. One patient had enlargement of the aneurysm prior to surgical clipping. Outcome data were not consistent across the studies reviewed. Two papers reported modified Rankin Scale (mRS) data. Six patients had an mRS score of 0–2 and two patients had mRS scores of 3–6. Twenty-three (49%) patients had a good recovery, as described by the authors. Five patients had a hemiparesis which was due to their initial insult; two were discharged in a persistent vegetative state. One patient had diminished fine motor function with a persistent left gaze preference, one had persistent word finding difficulties, one patient had mild cognitive impairment, and one patient was severely disabled. Outcome data were not available in four cases.
LSA aneurysms are rare entities that present several treatment challenges. There have only been 48 cases reported in the literature (table 1).
We summarize our own experiences with these lesions and propose a classification scheme based on anatomical location and patient presentation (table 2).
LSA aneurysms have been described in the presence of moyamoya-like vasculature,2 ,9–16 AVM,5–7 and hypertension1–3 but most cases are idiopathic. Almost all present with intracranial hemorrhage in relatively young healthy patients (median 39 years of age). Seven cases have been reported in the pediatric literature, of which two were associated with an underlying AVM.5 ,6 ,17–21 Most cases have been treated with open surgical clipping or excision but increasingly less invasive treatment options are becoming available, such as endovascular embolization9 ,11 ,13 ,22 and gamma knife radiosurgery.23 Conservative management has also been described, with angiographic resolution or near resolution of the aneurysm.1 ,10 ,24 ,25
Patients presenting with spontaneous intracranial hemorrhage should undergo vascular imaging. One prospective study of 80 patients with ICH found that angiography identified structural lesions in 74% of patients <50 years of age, and 83% in normotensive patients in this age group.26 Zhu et al27 found that the yield of angiography (CT based or formal) was significantly higher in patients at or below the age of 45 years and without pre-existing hypertension who presented with putaminal, thalamic, posterior fossa, or lobar hemorrhages. Formal angiography may provide several advantages over CT based angiography, such as higher resolution and the ability to plan for future treatments, especially if endovascular therapy is being considered. Given the small size of LSA aneurysms, they may not appear on CT angiograms. At high volume centers, high quality cerebral angiography can be performed with minimal risk to the patient and in a timely manner.
We propose a classification scheme based on anatomical location of LSA aneurysms visualized on cerebral angiography (figure 4). Type 1 describes aneurysms arising from the dorsal MCA next to a perforating LSA but not incorporating the perforator. This type is distinguished from an anterior temporal artery aneurysm, which arises from the ventral surface of the MCA alongside the origin of the anterior temporal artery. Type 2 is an LSA aneurysm from which the perforating artery or arteries arise. We propose two subtypes, one in which the aneurysm neck incorporates the origin of the perforating arteries (type 2A) and a second subtype in which the perforating arteries arise from the dome of the aneurysm (type 2B). Type 3 describes a fusiform aneurysm beyond the first loop or turn of an LSA. Even with high resolution magnified biplanar two-dimensional and three-dimensional angiography, it is often times difficult to discern the exact relationship of an LSA aneurysm to the neighboring perforators. In these instances, we have found that selective microcatheter selection of the aneurysm to perform aneurysmography is helpful to interrogate the anatomy of the lesion.
Type 1 aneurysms are rarely reported in the literature. This is likely due to the fact that most of these aneurysms arise from the MCA and are classified as proximal M1 aneurysms and are not recognized as separate entities. Unfortunately, angiographic data were not available in all of the cases reviewed, and thus we were only able to identify examples from our own case series. We report three cases of type 1 aneurysms from our own experiences (case Nos 1, 7, 8). Treatment of these lesions can lead to significant neurological sequelae, as demonstrated in case No 8. The most commonly described proximal LSA aneurysms are those classified as type 2 and usually also present with SAH due to their proximity to the MCA. All three cases described in the literature presented with SAH, and one patient suffered vasospasm, a feared complication of SAH.2 ,17 ,28 All three patients with type 2 aneurysms were treated surgically. In one case the aneurysm was excised and the other two underwent clipping. Both patients who had their aneurysms clipped suffered basal ganglia infarcts, but both recovered with either improvement of symptoms or full recovery described. This suggests that surgical treatment is a viable option for these lesions. Type 3 aneurysms are the typical Charcot–Bouchard aneurysms associated with hypertension and usually present with intraparenchymal hemorrhages, most commonly in the area of the basal ganglia, as well as intraventricular hemorrhage. These lesions arise in association with moyamoya-like vasculature, as the collateral vessels that develop cause dilation of the small LSA perforators. In one case, a type 3 LSA aneurysm was reported in a patient who had undergone superficial temporal artery to MCA bypass 12 years previously.12 The hemorrhages caused by type 3 LSA aneurysms can be dangerous due to the mass effect exerted on surrounding brain tissue with subsequent risk of herniation and death. However, hemorrhages from these types are less likely to result in acute hydrocephalus and delayed cerebral vasospasm. We have summarized our schema and treatment recommendations in table 3.
Open surgery has been the mainstay of treatment for LSA aneurysms and remains a good option in patients with symptomatic hematomas or in cases where endovascular therapy has failed. For type III aneurysms, this involves a craniotomy with excision of the aneurysm and sacrifice of the parent LSA. These operations can be technically challenging due to the depth of the LSA within the brain parenchyma, especially for vessels arising proximally along the MCA. Additionally, the LSAs are small vessels and can be in close proximity to the MCA. Image guided surgery has been reported with good results and could be considered for planning, especially in cases where the anatomy is distorted due to an underlying hematoma.5 ,29 In one series by Gandhi et al,2 three of six surgically treated patients underwent LSA sacrifice at the time of surgery as the aneurysm was fusiform and could not be excluded from the parent artery. Two of these three patients had basal ganglia infarcts on postoperative head CTs; however these infarcts did not cause neurological deficits. All three of these patients had a good outcome (mRS score of 1 or 2) at discharge. The neurological deficits suffered by these patients were related to their initial insult rather than basal ganglia infarcts, as they did not develop any new neurological symptoms postoperatively, suggesting that sacrifice of the distal LSA is well tolerated. Two of the three cases had angiographic data that were reviewable, and the LSA aneurysms were classified as type 3. Eddleman et al surgically treated a type 2A aneurysm and the patient subsequently suffered a left basal ganglia ischemic stroke. The patient developed postoperative facial droop and upper extremity weakness which resolved 1 week after clipping.28 It is possible that in type 3 aneurysms, which are located distally along the LSA, sacrifice of the parent artery would be better tolerated, as there is less territory supplied by more distal segments of the artery. In the event of these types presenting with ICH with a resulting neurologic deficit, it may also be expected that LSA sacrifice would be better tolerated. From our own experiences, occlusion of a proximal perforator during surgery for clipping of a type 1 aneurysm was complicated by profound postoperative neurological deficits (case No 8).
Endovascular therapy is becoming increasingly reported as a treatment option for LSA aneurysms. Several cases have been reported using n-butyl-2-cyanoacrylate and Onyx to sacrifice the parent LSA in order to treat the aneurysm.6 ,9 ,11 ,13 ,22 Three of five cases treated in this manner did not have any evidence of basal ganglia infarct postprocedurally. In one report, the authors described significant injury after endovascular injury but did not provide any details.6 In some cases endovascular therapy is attempted but unsuccessful. Commonly cited reasons are an acute angle of the LSA relative to the parent MCA, small caliber of the LSA, making it difficult to cannulate the vessel with microcatheters, or unwillingness to sacrifice the parent LSA.2 ,12 ,23 ,28–30 As the LSAs supply the basal ganglia, care should be taken before sacrificing these vessels. Endovascular treatment allows for evaluation of the vascular territory supplied by individual LSAs through injection of amobarbital injection or test occlusion with subsequent intraprocedural neurological examination.11 Patients with moyamoya-like blood vessels deserve special consideration as their vasculature can be frail and susceptible to damage. Recently, flow diversion devices have gained popularity for the treatment of difficult aneurysms. One case series of basilar perforator artery aneurysms treated with overlapping flow diverters has been described.31 Nonetheless, there is insufficient evidence regarding the treatment of perforator aneurysms with these devices to draw any conclusions.
Gamma knife radiosurgery has been well described for the treatment of AVM. A report by Lan et al23 describes the use of gamma knife to treat a ruptured distal LSA aneurysm. Although the authors report obliteration of the LSA aneurysm, the efficacy of gamma knife in treating LSA aneurysms is difficult to assess as there are reports of spontaneous angiographic resolution of these lesions when treated conservatively. Additionally, it can take up to 2 years for obliteration of the lesion, and in the interim patients may be at increased risk of rerupture. It is important to note that in this case radiotherapy did not seem to negatively impact on the patient's outcome.
Twenty-three patients had a good recovery and five patients died of their injury. From our experience, six of eight patients had a good recovery from their lesions with minimal residual symptoms. Of the two who had persistent neurological deficits, one was due to an SAH caused by rupture of an unrelated basilar tip aneurysm (case No 7) and another was caused by a postoperative perforator stroke. In both cases the outcome was good, with an mRS score of 2. This suggests that LSA aneurysms do not have the same mortality as those found in other locations. The main cause of initial death in SAH is due to vasospasm or acute hydrocephalus, and in the case of LSA aneurysms a minority of cases presented with SAH (31%). The danger from these lesions comes from the mass effect caused by intracranial hematomas. In some cases the mass effect can lead to hydrocephalus and subsequent mortality. Small hemorrhages in the absence of coagulopathies are usually managed conservatively if the lesion is not life threatening. However, most aneurysms are treated either endovascularly or surgically, and thus it is difficult to estimate the risk of rerupture for LSA aneurysms. Of the cases that reruptured prior to surgery, all patients had significant mortality or death.2 ,4 ,32 Given this finding, it is reasonable to treat these aneurysms as quickly as possible.
LSA aneurysms are rare entities that present several treatment challenges. We have summarized the cumulative experience with these lesions and proposed a classification scheme that has treatment implications.
We would like to thank Emma Vought for providing illustrations.
Contributors Each author listed should receive authorship credit based on material contribution to the article, revision of the article, and final approval of this article for submission to this journal.
Competing interests None.
Ethics approval The study was approved by the Medical University of South Carolina.
Provenance and peer review Not commissioned; externally peer reviewed.
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