Original research

A systematic review of non-trunk basilar perforator
aneurysms: is it worth chasing the small fish?
Manuel F Granja,1 Andre Monteiro,2 Guilherme Jose Agnoletto,2 Sara Jamal,2
Eric Sauvageau,1 Amin Aghaebrahim ‍ ‍,3 Ricardo Hanel ‍ ‍2
►► Additional material is
published online only. To
view please visit the journal
online (http://​dx.d​ oi.​org/​
10.​1136neurintsurg-​2019-​
015311).
1

Lyerly Neurosurgery, Baptist
Neurological Institute,
Jacksonville, Florida, USA
2
Stroke & Cerebrovascular
Center, Baptist Medical Center
Jacksonville, Jacksonville,
Florida, USA
3
Neurological Institute, Lyerly
Neurosurgery, Baptist Medical
Center Jacksonville, Jacksonville,
Florida, USA
Correspondence to
Dr Ricardo Hanel, Stroke &
Cerebrovascular Center, Baptist
Medical Center Jacksonville,
Jacksonville, Florida 32227,
USA; r​ hanel@​lyerlyneuro.​com
Received 24 July 2019
Revised 18 September 2019
Accepted 22 September 2019

© Author(s) (or their
employer(s)) 2019. No
commercial re-use. See rights
and permissions. Published
by BMJ.
To cite: Granja MF,
Monteiro A, Agnoletto GJ,
et al. J NeuroIntervent Surg
Epub ahead of print: [please
include Day Month Year].
doi:10.1136/
neurintsurg-2019-015311

ABSTRACT
Background and purpose Non-trunk basilar
artery perforator aneurysms (BAPAs) are rare
intracranial vascular pathologies that have long been
underdiagnosed, under-reported, and under-analyzed.
We performed a systematic review of the efficacy and
safety endpoints between conservative and active
treatment approaches for non-trunk BAPAs.
Methods Major databases were analyzed for relevant
publications between 1995 and 2019. Studies comparing
the outcomes between conservative and active treatment
approaches such as coiling, stenting, clipping, liquid
embolization, and flow diversion were included.
Mortality rate, rate of permanent neurological deficit
as determined by the modified Rankin Score (mRS),
rate of second treatment occurrence, and perioperative
complication rate were also assessed.
Results A total of 24 studies, including 54 patients
with 56 non-trunk BAPAs, were included. The mean
maximum aneurysm diameter was 2.70 mm (range
1–10). A diagnosis was achieved with the initial DSA in
50.0% (27/54) of the patients. A conservative approach
was used in 16 patients while active treatment was
used in the other 38. Thirteen of 15 (86.7%) patients
in the conservative group and 27/34 (79.4%) in the
active treatment group had an mRS score 0–2. A
non-significant higher odds of a positive outcome was
observed in the conservative group (OR 1.51, 95% CI
0.50 to 4.54). The event-related mortality rate was
3.55% (3/54) with one procedure-related death in the
active treatment group.
Conclusions In patients with non-trunk BAPAs
unamenable to active treatment, conservative
approaches may result in acceptable functional outcomes
and low morbidity. Small sample sizes and underreporting of outcomes warrant further study.

the basilar trunk.2 A second classification system
aimed at standardizing angiographic descriptions
was introduced by Satti et al in 2016 (figure 1).3 In
1996, Ghogawala et al published the first case of
BAPAs,4 and since then there has been a shift from
microsurgical clipping to endovascular treatment.
However, given the rarity of this pathology, there
is not a clear understanding of the optimal management approach for BAPAs to date. A full understanding of the natural history of this condition and
clarification of the post-treatment outcomes would
provide evidence-based management protocols
for BAPAs. We conducted a systematic literature
review to collectively report and analyze previously
published data on the management of BAPAs.

Introduction

Eligibility criteria

Aneurysms of perforating arteries are rare intracranial vascular pathologies that have long been
underdiagnosed, under-reported, and under-analyzed. Guidance as far as an optimal treatment
strategy is lacking. The prevalence of perforator
aneurysms of the anterior circulation is less than
1%, with no more than 50 cases reported in the
literature.1 Basilar artery perforator aneurysms
(BAPAs) are an even rarer and under-reported
subtype. Categorizing these aneurysms is a challenging task; Aboukais et al described these aneurysms as those whose neck is entirely located on
a perforator artery without direct involvement of

Methods
Study design

A systematic review of PubMed, Science Direct,
and Ovid/EMBASE databases was conducted based
on the Preferred Reporting Items for Systematic
Reviews and Meta-Analyses (PRISMA) guidelines.
Key words or Medical Subject Heading (MeSH)
terms such as cerebral aneurysm, intracranial
aneurysm, basilar artery, perforator, coiling, and
conservative treatment were used in combination
with Boolean perators to maximize search sensitivity. The search was limited to studies published
between January 1995 and August 2019. Initial
screening and study selection was performed using
the Ryyan app, a web and mobile application for
systematic reviews.5 The protocol was finalized
after consensus between all authors. Two authors
independently searched publications, selected articles with valid cases, and extracted data accordingly.
Discrepancies were resolved by open discussion
between two authors.

Inclusion criteria were: (1) articles published
in English, Portuguese, and Spanish; (2) studies
reporting BAPAs, such as case reports or case series
with no minimum patient number; (3) case reports
or case series including both radiographic and clinical outcomes. BAPAs associated with the simultaneous presence of arteriovenous malformation
(AVM), as well as pseudoaneurysms, were considered as separate entities and thus were excluded
from the systematic review. Review articles, editorials, technical notes, animal studies, and cases
missing angiographic or clinical follow-ups were
also excluded. Aneurysms arising from the basilar

Granja MF, et al. J NeuroIntervent Surg 2019;0:1–6. doi:10.1136/neurintsurg-2019-015311

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Hemorrhagic Stroke

stated in the source paper; (b) rate for the presence/absence of
permanent neurological deficit, defined as mRS 3–5 or GOS
2–4; (c) aneurysm regrowth rate, defined as a new aneurysm
occurrence at the same location after an initial treatment; (d)
rate of second treatment occurrence, defined as any endovascular or open approach due to aneurysm regrowth or any other
reason; (e) spontaneous resolution rate, defined as initially documented BAPA and no subsequent evidence of the same lesion
in follow-up imaging for those patients who were approached
conservatively. Aneurysm suboptimal occlusion was defined as
any postprocedural result different from complete aneurysm
occlusion (Raymond–Roy class I). The safety endpoint was the
perioperative complication rate, defined as any neurovascular
complication in the immediate postoperative period (up to
24 hours after the procedure). Efficacy outcomes were subsequently split into favorable and unfavorable outcomes when
rough or vague descriptions of clinical outcomes were reported.

Risk of bias determination

The risk of bias was assessed by the Newcastle–Ottawa Scale
according to the proposed items by Zhao et al.6 7 Two investigators independently performed a critical appraisal to determine
the most common bias in the actual set of case reports. Studies
were considered to have a low risk of bias if they missed one of
the following: clear demographic data, severity at presentation,
active treatment effectiveness, radiological follow-up, or clinical
follow-up. Studies with a medium risk bias missed two of the
aforementioned criteria, and those considered to have a high risk
of bias had neither a complete treatment effectiveness report nor
clinical follow-up detail (see online supplementary table 1).

Figure 1 Basilar artery perforator aneurysm classification system as
described by Satti et al.
artery trunk adjacent to a perforating branch but not involving
a perforating artery (Satti type I aneurysms) were excluded from
the analysis. Satti type IIa, IIb, and III were included; Satti type
IIa aneurysms are defined as incorporating the perforating artery
origin, whereas Satti type IIb aneurysms have a perforating artery
arising from the dome of the aneurysm. Satti type III aneurysms
are fusiform lesions along the course of a perforating artery
beyond the parent vessel (figure 1).3 A specific BAPA Satti type3
was assigned when a full anatomical description and a complete
imaging set was provided by the author.

Data synthesis

Data collected included patient age, sex, presenting symptoms, subarachnoid hemorrhage (SAH), anatomical location
and severity (Fisher scale), initial imaging modality, number of
digital subtraction angiographies (DSAs) performed until actual
diagnosis, number of aneurysms per patient, and maximum
aneurysm diameter. Several treatment details were collected,
including the modality of the first active treatment (clipping,
stenting/coiling alone, stent-assisted coiling, and embolization),
treatment approach (active vs conservative), spontaneous resolution, recurrence after first treatment, second treatment modality,
incidence of periprocedural complications (3rd or 4th cranial
nerve palsy, cerebrospinal fluid leak, hemiparesis, vasospasm,
hydrocephalus, tension pneumocephalus, in-stent thrombosis),
time at follow-up when the aneurysm resolved, mortality, longest
follow-up, last documented modified Rankin Scale (mRS) score,
and permanent residual deficit.

Study endpoints

Efficacy endpoints included (a) mortality rate, defined as mRS
score of 6, Glasgow Outcome Scale (GOS) 1, or otherwise
2

Statistical analysis

Efficacy and safety endpoints were analyzed for patients with
and without active treatments in an effort to identify potential differences between the two groups. Continuous variables
are reported as means and ranges for normal distributions and
as medians with interquartile ranges for skewed distributions.
Categorical variables are presented as rates. Univariate comparisons were performed using a Fisher exact test, given the small
expected frequencies. Continuous variables were compared using
the Mann–Whitney U test or an unpaired t-test. ORs and 95%
CI for each prespecified outcome were calculated accordingly.
No particular heterogeneity or publication bias analysis was
reported because the maximum number of cases per published
series was eight.8 All statistical tests were performed using SPSS
(IBM, Armonk, New York, USA). Two-sided test results with
p<0.05 were considered statistically significant.

Results
Study selection

Out of 59 articles identified, 32 were duplicates and 15 were
excluded according to our prespecified protocol (figure 2). The
remaining 31 studies were assessed in full text and, after revision of cross references, 24 retrospective case series met our
predefined inclusion criteria and were included in the evidence
synthesis. Of the 24 included articles, 19 (79%) had a low risk
of bias,2–4 8–23 three (12%) had a medium risk of bias,24–26 and
two (8%) had a high risk of bias27 28 (see online supplementary
table 1).

Patient demographics

A total of 54 patients with 56 non-trunk BAPAs (Satti type
IIa, IIb, III)3 were included in the analysis. Patient baseline

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Hemorrhagic Stroke

the study population. Eighteen cases had a non-specified intracranial bleeding pattern. Fisher grade 3 or 4 was documented in
39.0% (21/54) of patients. All patients had a non-contrast head
CT as the first-line imaging modality. However, when considering the second-line modality, non-trunk BAPAs were identified by a CT angiogram (CTA) in 31.4% (17/54) of patients,
and in 65.0% (35/54) DSA led to a certain diagnosis. The final
imaging modality was not reported in two patients.10 Diagnosis
was achieved with the initial DSA in 50.0% (27/54) of patients,
in 41.0% (22/54) of cases by the second, and in 9.2% (5/54) by
the third. Our analysis identified aneurysm Satti type IIa in 5.5%
(3/54) of cases, type IIb in 11.1% (6/54), and type III in 63.0%
(34/54).

Treatment characteristics and outcomes

Figure 2 Flow chart of study selection.
characteristics are presented in table 1. The mean patient age
was 56.5 years (range 27–82 years) and 27.8% (15/54) were
female. The overall mean maximum aneurysm diameter was
2.70 mm (range 1–10 mm). Thirty-eight cases were actively
treated and 16 cases were managed conservatively. Patients in
the active treatment group had a significantly larger aneurysm
diameter than those in the conservative treatment group (3.32
mm vs 1.52 mm, p<0.001). At admission, 100% of patients
presented with SAH. Non-contrast head CT revealed a diffuse
bleed in 37.0% (20/54) of patients, a perimesencephalic bleed
in 18.5% (10/54), and a prepontine bleed in 11.1% (6/54) of
Table 1

Among the 38 patients in the active treatment group, coiling was
the most commonly used treatment modality (39.5%, 15/38);
stenting (n=9), clipping (n=6), Onyx liquid embolization (n=1),
and flow diversion (n=5) were also utilized (table 1). Regarding
aneurysm occlusion rates, 23.7% (9/38) of patients had suboptimal occlusion after a first treatment attempt.3 8 9 16 18 21 25 Failure
to place a coil was the most common reason for an unsuccessful
first treatment attempt (18.4%, 7/38). Of the nine patients with
suboptimal occlusion, only five underwent an active second
treatment (two clipping,9 25 one wrapping,18 two stenting3 16),
three of which had an mRS 0–2 in the final follow-up. The
remaining 4/9 (44.4%) patients were managed conservatively
after the first attempt.8 13 21
Spontaneous aneurysm resolution was documented in 50.0%
(8/16) of patients in the conservative treatment group on
subsequent follow-ups and 80.0% (4/5) in whom suboptimal

Baseline patient characteristics and outcomes
Treatment approach
Conservative
(n=16)

Active (n=38)

Overall

P value

 Age, years (range)

58.7 (35–76)

55.3 (27–82)

56.5

0.830

 Female

25.0 (4/16)

29.0 (11/38)

27.8

0.767

37.5 (6/16)

39.5 (15/38)

38.9

0.892

  
CTA

25.0 (4/16)

34.2 (13/38)

31.5

0.506

  
DSA

75.0 (12/16)

60.5 (23/38)

64.8

0.309

Aneurysm identified on initial diagnostic imaging*

31.3 (5/16)

44.7 (17/38)

40.7

0.833

 Aneurysm maximum diameter, mm

1.52 (1–3)

3.32 (1.2–10)

2.70

<0.001

Demographics

Imaging features
 Fisher grade 3 or 4
 Initial diagnostic modality

Treatment modality

–

 Coiling

–

39.5 (15/38)

 Stenting

–

23.7 (9/38)

 Clipping

–

15.8 (6/38)

 Liquid embolization

–

2.60 (1/38)

 Flow diversion

–

13.2 (5/38)

Spontaneous aneurysm resolution

50.0 (8/16)

80.0 (4/5)†

57.1

0.338

mRS 0–2 at last follow-up

86.7 (13/15)

79.4 (27/34)

74.1

0.023

Data are mean (range) or % (n/N).
*No repeat imaging was required.
†Suboptimal angiographic result and second treatment attempt was not made (n=5). Fisher’s exact test for all categorical variables.
.CTA, CT angiography; DSA, digital subtraction angiography; mRS, modified Rankin Scale.

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Hemorrhagic Stroke

angiographic results were obtained but a second attempt was
not made. Five out of nine patients reported a subsequent
follow-up after an initial suboptimal treatment. The mean time
for spontaneous aneurysm resolution for the entire population
was 3.6 months (range 1–7) (n=12). A total of 49 mRS scores
were available as reported by each of the different authors. In
the conservative and active treatment groups 86.7% (13/15)
and 79.4% (27/34) had an mRS score of 0–2, respectively, indicating a non-significant higher odds of a positive outcome in
the conservative group (OR 1.51, 95% CI 0.50 to 4.54). Mean
clinical follow-up time for the whole population was 16 months

Table 2

(range 0.5–78). The overall event-related mortality rate was
3.55% (3/54)10 11 15 with one procedure-related death reported
in the active treatment group (table 2).11

Discussion
This systematic review found that both active treatment and
conservative approaches are used to treat non-trunk BAPAs with
positive outcomes. The rate of successful functional outcome
(mRS 0–2) was similar between the two groups. After consideration of the several limitations of this review, probing a

Summary of reports of non-trunk basilar perforator aneurysms

Study

Total cases (n)

Periprocedural transient Mean FU period Mortality ratio (n/ Neurological deficit mRS 0–2 at last
complications (detail, n) clinical (months) total)
during FU (deficit, n) FU (n/total)

Studies reporting conservative approach
 Park et al20
8

3

N/A

11

0/0

Hemiparesis (n=1)

3/3

2

N/A

10.5

0/0

Hemiparesis (n=1)

2/2

 Daruwalla et al15

1

N/A

0.5

1/1

NR

0/1

 Aboukais et al2

1

N/A

6.5

0/0

NR

3/3

 Buell et al11

3

N/A

35

0/0

No

3/3

 Sahu et al22

2

N/A

NR

NR

NR

NR

12

1

N/A

12

0/0

No

1/1

3

N/A

6

1/3

(n=1), non-specified

1/3

 Forbrig et al

 Chau et al

 Bhogal et al10

Studies reporting active treatment
 Ghogawala et al4

1

3rd cranial nerve palsy

6

0/0

No

1/1

 Hamel et al18

1

Tension pneumocephalus

7

0/0

Ataxia

0/1

26

3

No

NR

0/0

No

3/3

 Mathieson et al25

1

CSF leak and
hydrocephalus

NR

0/0

Amnesia

1/1

 Deshaies et al16

1

No

6

0/0

No

1/1

 Chen et al14

2

No

21

0/0

Lower extremity
weakness (n=1)

2/2

 Nyberg et al28

 Sanchez-Mejia et al

2

No

9

0/0

NR

NR

9

1

Hemiparesis

20

0/0

Hemiparesis (n=1)

0/1

 Ding et al17

1

Dysarthria, lethargy,
severe quadriparesis,
R-facial nerve palsy

NR

0/0

Severe disability

0/1

 Chalouhi et al27

1

No

6

0/0

No

1/1

1

Vasospasm, 3rd cranial
nerve palsy

12

0/0

No

1/1

 Apok et al

 Gross et al

24

 Sivakanthan et al23

1

No

6

0/0

No

1/1

13

2

No

6

0/0

No

1/1

 Peschillo et al21

2

Hemiparesis, in-stent
thrombosis* (n=2)

21

0/0

Upper extremity
monoparesis (n=1)

2/2

 Forbrig et al8

6

Hemiparesis, vasospasm,
hydrocephalus (n=3)

30.5

0/0

Hemiparesis (n=2)

5/6

 Buell et al11

4

NR

32

1/4

(n=3), non-specified

2/4

 Sahu et a22

2

No

7.5

0/0

No

2/2

 Satti et al3

1

Vessel dissection and 4th
cranial nerve palsy (n=1)

7

0/0

No

1/1

 Lockwood et al19

1

Vasospasm

5

0/0

No

1/1

1

No

6

0/0

No

1/1

3

No

6

0/0

(n=3), non-specified

3/4

 Chavent et al

 Chau et al

12

 Bhogal et al10
*Reversed with tirofiban.
FU, follow-up; NR, not reported.

4

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significantly higher benefit in terms of functional outcome for
any of the specific modalities included in the active treatment
group (ie, coiling, stenting, clipping, liquid embolization, and
flow diversion) seems to be elusive. However, the data compiled
in this review provide enlightening facts about these uncommon
lesions. We found that (1) a maximum aneurysm diameter of
≥3.32 mm was significantly associated with an active approach;
(2) 41% of patients required a second DSA in order to achieve a
certain diagnosis; (3) suboptimal occlusion rates can be observed
in up to 23.7% of patients after an active treatment modality
is provided; and (4) failure to place a coil is the most common
reason for an unsuccessful first treatment attempt.
As a framework for future studies, Satti et al proposed a
distinctive BAPA classification system where type I aneurysms
are defined as lesions arising from the basilar artery trunk adjacent to a perforating branch but not involving a perforating
artery.3 This rare type of aneurysm can be found in up to
2.1% of patients among overall aneurysm locations.3 Whether
this new classification system translates into differential treatment strategies is yet to be elucidated. Trunk BAPAs are often
described and compared along with non-trunk BAPAs. Nevertheless, trunk BAPAs have been subclassified into four different
categories based on imaging findings, including acute dissecting
aneurysms, segmental ectasia, chronic mural bleeding ectasia,
and saccular.29 Saccular aneurysms seem to be stable over time
with little or no change in size. However, segmental ectasia and
chronic dissecting aneurysms are characterized by increasing
size and carry a risk of SAH, especially in men with positive
vascular risk factors, and require prompt intervention.29 Type I
trunk BAPAs were excluded from this review based on their high
complexity, heterogeneity, different natural history, and uncertainty regarding best treatment modality. AVM-related basilar
artery aneurysms were also considered a separate and secondary
entity and were therefore excluded from the present systematic
review.
Typically, non-trunk BAPAs are angiographically occult,
requiring three-dimensional rotational angiography for final
diagnosis. Indeed, only one-third of non-trunk BAPAs included
in this review were diagnosed after a second-line CTA and 50%
after a single DSA. Other authors have reported performing up
to three conventional angiograms before a final diagnosis was
achieved, raising serious concerns regarding under-diagnosis.21
The introduction of improved microcatheter/microware technologies to the neurointervention armamentarium has allowed
endovascular management of trunk and non-trunk BAPAs as
a first-line treatment approach. Peschillo et al retrospectively
analyzed results of three patients diagnosed with trunk Satti type
I BAPAs treated with flow diversion. Long-term outcomes for
all patients were acceptable and the following periprocedural
complications were described: 2/3 patients experienced in-stent
thrombosis and 1/3 experienced intracranial hemorrhage.21
Although initial series of flow diverters in the posterior circulation reported high morbidity and mortality rates, most of these
series included giant or fusiform aneurysms.30 31 Recently, the
use of a single long flow diverter instead of multiple telescoped
devices as well as adequate compliance with antiplatelet regimens have shown considerable efficacy and safety in the treatment of intracranial aneurysms of the vertebrobasilar system.32 33
On the other hand, non-trunk Satti type II BAPAs have been
successfully managed after placement of lower-metal coverage
stents (ie, Enterprise and Neuroform stents). However, we
cannot state whether these results were due to a favorable
balance between adequate metal coverage and low risk of perforator occlusion or to natural history of spontaneous aneurysm

resolution as seen in 50.0% of the cases in the group who underwent a conservative approach. Multiple interventions and staged
approaches may also be expected when treating non-trunk
BAPAs. Every time a first treatment attempt was unsuccessful,
mostly due to failure to place a coil, a second treatment was not
attempted, especially in those cases where the initial maximum
aneurysm diameter was <2.5 mm, which raises questions
about the indication and benefit of any active treatment in this
subgroup of patients.8 9 13 18 25 This review demonstrated that
up to 24% of patients had a suboptimal occlusion rate after an
initial treatment attempt; however, 66% of those had a favorable
mRS score at final follow-up.
This systematic review has several limitations. There was
significant under-reporting of objective scales regarding aneurysm occlusion grades; hence, criteria for reintervention after
any degree of recanalization was not well defined. All the
included articles were retrospective studies. In addition, small
sample sizes and under-reporting of functional outcomes among
the conservative approach limit the scope of these results. A
heterogeneous body of evidence on diagnostic methods, occlusion rates, clinical outcomes, and periprocedural complication
rates preclude any robust conclusion favoring a specific treatment modality.
In conclusion, case reports and case series on either active
treatment modalities and conservative approaches can be found
across the literature for the treatment of BAPAs. In this contemporary systematic review, conservative approaches may result in
acceptable functional outcomes and low morbidity in patients
not amenable to active treatment. Small sample sizes and
under-reporting of outcomes warrant further study to explore
the effects of individual treatment strategies on BAPAs.
Twitter Amin Aghaebrahim @drnimajax
Contributors MFG: manuscript design, writing, editing, and statistical analysis.
AM: data gathering, editing, and statistical analysis. GJA, SJ, ES, AA: manuscript
writing, editing. RH: original idea, manuscript writing, and editing.
Funding The authors have not declared a specific grant for this research from any
funding agency in the public, commercial or not-for-profit sectors.
Disclaimer RH is a consultant and scientific advisor for Microvention, Stryker, and
Covidien.
Competing interests RH is a consultant for Medtronic, Stryker, Codman, and
MicroVention. The remaining authors have nothing to disclose.
Patient consent for publication Not required.
Provenance and peer review Not commissioned; externally peer reviewed.
ORCID iDs
Amin Aghaebrahim http://​orcid.​org/​0000-​0002-​9126-​2932
Ricardo Hanel http://​orcid.​org/​0000-​0001-​7195-​5806

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Granja MF, et al. J NeuroIntervent Surg 2019;0:1–6. doi:10.1136/neurintsurg-2019-015311

J NeuroIntervent Surg: first published as 10.1136/neurintsurg-2019-015311 on 9 October 2019. Downloaded from http://jnis.bmj.com/ on October 13, 2019 at University of Otago. Protected
by copyright.

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