ORIGINAL ARTICLE - VASCULAR NEUROSURGERY - ANEURYSM

Frequency and risk factors for postoperative aneurysm residual

after microsurgical clipping

Kathrin Obermueller

& Isabel Hostettler

& Arthur Wagner

& Tobias Boeckh-Behrens

& Claus Zimmer

Jens Gempt

& Bernhard Meyer

& Maria Wostrack

Received: 17 July 2020 / Accepted: 27 October 2020

The Author(s) 2020

Abstract

Objective Aneurysm residuals after clipping are a well-known problem, but the course of aneurysm remnants in follow-up is not

well studied. No standards or follow-up guidelines exist for treatment of aneurysm remnants. The aim of this study was to

evaluate the risk factors for postoperative aneurysm remnants and their changes during follow-up.

Methods We performed a retrospective analysis of 666 aneurysms treated via clipping in our hospital from 2006 to 2016.

Postoperative and follow-up angiographic data were analyzed for aneurysm remnants and regrowth. Clinical parameters and

aneurysm-specific characteristics were correlated with radiological results.

Results The frequency of aneurysm residuals was 12% (78/666). Aneurysms located in the middle cerebral artery (p =0.02)

showed a significantly lower risk for incomplete aneurysm occlusion. Larger aneurysms with a diameter of 11–25 mm (p =

0.005) showed a significantly higher risk for incomplete aneurysm occlusion. Five patients underwent re-clipping during the

same hospital stay. Remnants were stratified based on morphological characteristics into “dog ears” (n = 60) and “broad based”

(n = 13). The majority of the “dog ears” stayed stable, decreased in size, or vanished during follow-up. Broad-based remnants

showed a higher risk of regrowth.

Conclusions A middle cerebral artery location seems to lower the risk for the incomplete clip occlusion of an aneurysm. Greater

aneurysm size (11–25 mm) is associated with a postoperative aneurysm remnant. The majority of “dog-ear” remnants appear to

remain stable during follow-up. In these cases, unnecessarily frequent angiographic checks could be avoided. By contrast, broad-

based residuals show a higher risk of regrowth that requires close imaging controls if retreatment cannot be performe d

immediately.

Keywords Intracranial aneurysm

Aneurysm clipping

Aneurysm residual

Aneurysm remnant

Aneurysm regrowth

Abbreviations

ACA Anterior cerebral artery

DSA Digital subtraction angiography

Fig. Figure

FU Follow-up

H&H Hunt and Hess grade

ICA Internal carotid artery

ICD International Statistical Classification

of Diseases and Related Health Problems

ICG angiography Indocyanine green angiography

MCA Middlecerebralartery

PC Posterior circulation

SAH Subarachnoid hemorrhage

SD Standard deviation

Tab. Table

Introduction

The frequency of incomplete aneurysm occlusion after surgi-

cal clipping varies from 2–49% in different surgical series

[1–5, 7, 9, 12, 13, 15, 20, 24, 25, 27, 28, 31, 32]. The risk of

This article is part of the Topical Collection on Vascular Neurosurgery -

Aneurysm

* Kathrin Obermueller

kathrin.obermueller@tum.de

Department of Neurosurgery, Klinikum rechts der Isar, Technical

University Munich, Ismaninger Straße 22, 81675 Munich, Germany

Department of Neuroradiology, Klinikum rechts der Isar, Technical

University Munich, Ismaninger Straße 22, 81675 Munich, Germany

Acta Neurochirurgica

https://doi.org/10.1007/s00701-020-04639-5

rebleeding after aneurysm clipping is estimated at 1.3% and is

associated with the size of the residual rest [19]. However

clear criteria for retreatment and for follow-up controls of

aneurysm residuals have not yet been strictly defined.

Possible risk factors and potential follow-up dynamics are

essential for treatment decisions, as well a s for p atient

consultation.

Postoperative angiography is an accepted standard in most

neurosurgical departments, as it reveals residual filling of an-

eurysms or other complications, like major vessel occlusion

[13, 20, 27, 28]. In patients with completely clipped aneu-

rysms, further angiographic controls for the treated aneurysms

are considered unnecessary. However, no standards have been

established for follow-up (FU) in cases with residual aneu-

rysms after clipping. Currently, aneurysm remnants are cate-

gorized according t o their morphological characteristics.

David et al. and Raymond et al. classified aneurysm remnants

into 2 categories: “dog-ear” and “broad-based” residuals.

“Dog ears” consist of a small neck remnant between the parent

vessel and the base of the clip, wherea s the reconstructe d

parent vessel of “broad-based” remnants contains part of the

aneurysm wall [9, 29]. These differences in morphology sug-

gest different risks for regrowth and subsequent rebleeding.

Accordingly, the follow-up periods and the decision for sur-

gery should be made based on the estimated risk of rupture.

The aim of this study was to determine the frequency and

risk factors of residual aneurysm filling after aneurysm clip-

ping and to estimate the risk of regrowth of remnants in our

surgical series.

Methods

We performed a retrospective, single-center data analysis of

patients treated for intracranial aneurysm via clipping. The

analyzed data were collected from 2006 until 2016.

Patient inclusion/exclusion criteria

Based on the operational key for aneurysm clipping, the pa-

tient data were consecutively entered into the database. We

included patients with clipping for incidental aneurysms and

patients who were clipped for ruptured aneurysms. Patients

who received surgical treatment other than clipping (e.g.,

wrapping or trapping and bypass surgery) or, who did not

undergo postoperative digital subtrac tion angiography

(DSA) were excluded from the final analysis. Patients who

underwent aneurysm clipping in the context of other patholo-

gies (for example, arteriovenous malformation, or mycotic

aneurysms) were also excluded from the analysis. The local

ethics committees approved the study protocol (nb. 5020/11)

Interventions

Every patient received a four-vessel catheter DSA before and

a target vessel DSA within the first 24 h after surgery. The

decision for the treatment modality was based on interdisci-

plinary discussion between the neuroradiologist and neurosur-

geon. All surgeries were performed by three experienced vas-

cular neurosurgeons. For all incidental aneurysms, and partly

for ruptured aneurysms, patients underwent in traoperative

neuromonitoring comprising trans-cranially recorded motor

evoked potentials. Indocyanine green (ICG) angiography

was routinely conducted. If any aneurysm residual or vessel

occlusion was suspected in postoperative angiography, the

findings were discussed immediately to provide the possibility

of a prompt clip adjustment. Indications for FU angiography

in cases of residual filling without an indication for clip repo-

sitioning were discussed interdisciplinarily and were per-

formed depending on the size, shape, and general condition

of the patient.

Outcomes

The following clinical, radiological, and epidemiological data

were recorded for each patient: age, sex, preoperative neuro-

logical condition, Hunt and Hess grade, Fisher grade, aneu-

rysm location and size, number of aneurysms, number of op-

erations, postoperative neurological condition according to

the modified Rankin Scale, size of aneurysm remnant, size

of aneurysm remnant in FU angiography, and neurological

status during FU.

For the present research, postoperative DSA results were

screened for aneurysm remnants. An aneurysm remnant was

defined as an inflow of contrast medium with a minimum size

of 1 mm and visible on at least 2 projections of angiography in

the area of a previously described aneurysm. Follow-up ex-

aminations were reviewed for growth of the aneurysm rem-

nant, defined as any new inflow of contrast medium (com-

pared to postoperative angiography) that caused an enlarge-

ment of the residual. Changes in flow patterns or thrombosis

of the remnant were also evaluated.

Aneurysm remnants were divided according to classifica-

tion of David et al. and Raymond et al. into “dog-ear” rem-

nants with a small residual between the parent vessel and the

base of the clip and “broad-based” remnants, in which a larger

residual was still filling [9, 29]. The “dog-ear remnant” group

was scheduled for FU angiography depending on the remnant

size, the history of any previous subarachnoid hemorrhage

(SAH), and the general condition and age of the patient.

Patients with “broad-base d remnants” were either re-

operated during the same hospital stay or were designated

for FU imaging. FU DSA examinations were scheduled de-

pending on the individual risk factors and remnant character-

istics regularly within a period of 3 months to 1 year after

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surgery. The mean FU in aneurysm remnants was 31 months

(SD: ± 23.3, range 2.3–93 months).

Statistical analysis

The study sample was described using means ± standard de-

viations for the continuous variables, while categorical param-

eters were depicted using absolute and relative frequencies.

Chi-squared tests and binary logistic regression were used to

test categorical variables. Continuous variables were tested

with a t test or Wilcoxon test. A p value of 0.05 was consid-

ered statistically significant. Analyses were performed utiliz-

ing R Studio Version 1.0.4 (R Studio, Boston, USA).

Results

Data collection

In 492 patients, a total of 666 ruptured and unruptured aneu-

rysms were treated between April 2006 and December 2016.

The reasons for case exclusion are listed in Fig. 1.

In 18 patients, no postoperative DSA was performed. In

this group, 11 cases had suffered a severe SAH and had died

soon after aneurysm clipping. In 3 cases, other medical cir-

cumstances (malignant disease) were treated immediately and

were judged more important than the aneurysm.

Complications during the initial angiography, with arterial

dissection in 2 and symptomatic arterial emboli in 1 case,

led to no postoperative DSA. One patient rejected postopera-

tive DSA after elective clipping.

Patient data

Patient data and data on the treated aneurysms are shown in

Tables 1 and 2.

Frequency of postoperative aneurysm remnants

Residual filling was found in 78/666 aneurysms (12%). Data

on patients with postoperative aneurysm residuals are present-

ed in Table 3.

Risk of aneurysm residuals

Binary logistic regression revealed a higher risk of an aneu-

rysm residual for aneurysms sized 11–25 mm, with an odds

ratio of 9.36 (CI 1.96–44.61; p = 0.005). A location in the

MCA showed a significantly lower risk for aneurysm resid-

uals when compared with other locations, with an odds ratio

of 0.31 (CI: 0.12–0.83; p = 0.02) (Table 4). Sex, number of

aneurysms per patient, and emergency setting of surgery

showed no significant association with postoperative aneu-

rysm residuals.

Follow-up of aneurysm remnants

Figure 2 shows the classification and early treatment of aneu-

rysm remnants. FU was available for 33/60 (55%) aneurysms

in the dog-ear group and for 7/13 (54%) in the group of broad-

700 aneurysm-clipping procedures identified

via ICD I67.1

666 aneurysm-clipping procedures

34 excluded

No postoperative DSA: 18

Surgical technique other than

clipping used: 6

Clipping not feasible: 4

No aneurysm identified: 2

Aneurysm associated with

other pathology: 5

Fig. 1 Flowchart of procedure inclusion via ICD code I67.1

Table 1 Patient data and clinical characteristics (n =492)

Parameter Value

Age at surgery mean ± SD 55.48 ± 13.1

Gender female n, (%) 343 (70)

Acute SAH n, (%) 252 (51)

Multiple aneurysms ≥ 2 n, (%) 167 (34)

SAH, subarachnoid hemorrhage

Table 2 Data on treated aneurysms (n =666)

Parameter Value

Aneurysm location n,(%)

ACA 152 (23)

ICA 140 (21)

MCA 340 (51)

PC 34 (5)

Aneurysm size n,(%)

< 3 mm 136 (20.4)

3–6 mm 306 (46.0)

7–10 mm 129 (19.4)

11–25 mm 59 (8.8)

>25mm 4(0.6)

Residual of coiled aneurysm 32 (4.8)

ACA, anterior cerebral artery; ICA, interior carotid artery; MCA, middle

cerebral artery; PC, posterior circulation

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based residuals. The mean FU was 31 months (SD: ± 23.3,

range 2.3–93 months).

The reasons for missing FU differed. In 12 cases, FU an-

giography was recommended but the patient did not attend the

FU examination. In 7 cases, the patients were in poor neuro-

logical condition and FU angiography was recommended on-

ly if the patients improved during their postoperative courses.

These were all patients who had suffered a severe SAH. In 4

dog-ear cases, FU angiography was not recommended

because of the small size of the aneurysm remnant. In 9 cases,

a FU recommendation was not specified at discharge.

Follow-up of dog-ear remnants and broad-based remnants

Table 5 shows the course of dog-ear residuals during FU.

The major par t of the dog-ear residuals stayed stable, de-

creased in size, or closed during FU (94%). An increase in

size was recorded in two cases.

During FU, two of the broad-based aneurysms increased in

size, one decreased, and none closed spontaneously. The num-

ber of broad-bas ed aneurysms i n FU was small ( n =7)

(Table 6). Figures 3 and 4 show typical DSA findings of a

dog ear and a broad-based aneurysm residual.

Treatment of aneurysm residuals during follow-up

All aneurysm remnants with increasing size were treated (2 in

the dog-ear group, 2 in the broad-based group). The 2 progres-

sive dog-ear residuals were treated 1 year after clipping by

coiling and stent-assisted coiling. The progressive broad-

based residuals were treated via clipping in one case at 6

months after the first surgery and by coiling in the other case

at 1 year after surgery.

Two broad-based aneurysm residuals were treated irrespec-

tive of the residual growth during the FU. In 1 case, the broad-

based residual of a paraophthalmic aneurysm was treated with

a flow diverter 6 months postoperatively. In another case, a

paraophthalmic ICA aneurysm was clipped and postoperative

angiography revealed a small remnant. Early second surgery

was performed, but a postoperative DSA still showed an an-

eurysm residual. One year later, the aneurysm residual was

treated with stent-assisted coiling and showed no further

growth during FU.

Fig. 2 Flowchart of aneurysm residuals

Table 4 Factors associated with postoperative aneurysm residuals. The

factor positively associated with postoperative aneurysm residuals is

aneurysm size 11–25 mm. The location of the “MCA” aneurysm is asso-

ciated with a reduced risk for postoperative aneurysm residuals. (Binary

logistic regression)

Parameter OR (95%CI) p

Aneurysm location

ACA 0.67 (0.24–1.84) 0.44

ICA 1.35 (0.51–3.61) 0.55

MCA 0.31 (0.12–0.83) 0.02

Aneurysm size n (%)

< 3 mm 0.98 (0.19–4.99) 0.98

3–6 mm 2.04 (0.46–9.12) 0.35

7–10 mm 4.23 (0.95–20.60) 0.06

11–25 mm 9.36 (1.96–44.61) 0.005

>25mm 4.46(0.37–66.74) 0.28

Surgery in acute phase 0.67 (0.38–1.16) 0.16

ACA, anterior cerebral artery; ICA, interior carotid artery; MCA, middle

cerebral artery

Table 3 Data on aneurysms with residual filling in postoperative DSA

(n = 78). The percentage is based on the total number of operated patients

in the respective subgroup

Parameter Value

Aneurysm location n, (% of the entire subgroup)

ACA (n =152) 18(11)

ICA (n =140) 28(20)

MCA (n =340) 25(7)

PC (n =34) 8(24)

Aneurysm size n,(%)

< 3 mm (n = 136) 7 (5)

3–6mm(n =306) 28(9)

7–10 mm (n =129) 23(17)

11–25 mm (n = 59) 18 (31)

>25mm(n = 4) 1 (25)

Residual of coiled aneurysm (n =32) 2(6)

ACA, anterior cerebral artery; ICA, interior carotid artery; MCA, middle

cerebral artery; PC, posterior circulation

Acta Neurochir

Discussion

In the current study, we analyzed the risk factors for aneurysm

remnants after microsurgical clipping and the course of aneu-

rysm remnants in FU. Postoperative angiography revealed a

rate of 12% for residual aneurysm filling in clipped aneurysms

in our series. These data are consistent with other published

studies, as the frequency of residual filling of aneurysms after

clipping is reported to range from 2.3 to 19.3%. One series

from Korea revealed an incidence of residual filling of even

49% when controlled with 3D angiography and defining a

remnant size from 1 mm onward [1–5, 7, 9, 12, 13, 15, 20,

24, 25, 27, 28, 31, 32]. Our series confirms the need for early

postoperative angiography to certify the success of the surgery

and, in the c ase of remn ants, to ensure that FU or further

therapy can be scheduled appropriately. The necessit y for

postoperative angiography has been discussed previously [8,

10, 12], and this procedure remains the absolute standard for

control after aneurysm surgery.

Risk factors for incomplete aneurysm occlusion

A greater aneurysm size (11–25 mm) was associated with

incomplete surgical occlusion. Jabbarli et al. described similar

results for aneurysms sized > 12 mm and an association with a

higher risk for a clip remnant [18].

The location of the aneurysm is considered important for

the occurrence of an aneurysm remnant, as the risk of aneu-

rysm remnants seem to be greater for paraophthalmic, anterior

communicating artery, and basilar artery aneurysms [18, 27,

32]. Our series revealed a lower risk for aneurysm residuals

following clipping of MCA aneurysms, in agreement with

previously described findings and reflecting the technically

easier accessibility as compared to paraophthalmic and poste-

rior circulation aneurysms [21, 28].

Direct intraoperative catheter angiography within a hybrid

operating room is described as potentially beneficial for the

occlusion rates of the aneurysms [22, 26]. However, in our

series, only 5 patients underwent early clip revision surgery.

This was primarily due to the technically difficult

configuration of the aneurysm; therefore, it could not be

avoided with the use of intraoperative DSA.

Angiographic and clinical follow-up of aneurysm remnants

In our series, the major part of dog-ear residuals remained

stable, decreased in size, or vanished during the FU.

Therefore, foregoing angiographic controls might be justified,

particularly in patients without risk factors such as a previous

history of SAH, hereditary or de novo aneurysms, hypertonus,

or smoking. A younger age should also be regarded as a po-

tential risk factor because of the previously reported increased

risk of regrowth of aneurysm residuals in patients under 45

years old [18].

In 2004, Akyüz et al. performed a long-term angiographic

FU (median 46.6 months) of 166 clipped aneurysms, with 7

residuals (4.2%), using the Sindou residual grading system.

They reported 5 small neck residuals and 2 with a broader

residual. One case of regrowth was recorded in a small rem-

nant and led to reoperation, but no cases of regrowth occurred

among the larger remnants. These surgeons also had one case

of spontaneous thrombosis of a small remnant but experienced

no cases of rebleeding during FU. They concluded that small

aneurysm remnants may stay stable [3].

The FU of broad-based aneurysms in our series was incom-

plete, but it revealed a high rate of regrowth (28%). This was

also observed by David et al., who noted aneurysm regrowth

in 3 out of 4 cases [9]. Only one broad-based residual de-

creased in size during FU, but it did not close completely.

Broad-based residuals seem to have a high risk of regrowth

and should be scheduled for FU, as the need for retreatment

seems to occur frequently. Furthermore, the CARAT study

revealed a size-dependent risk of rebleeding in clipped and

coiled aneurysms [19].

In treated aneurysms after SAH, the risk of rehemorrhage

has been estimated as 0.11–0.21% in the first year for coiled

aneurysms and 0.0–0.03% for clipped aneurysms [10, 19]. In

our series, no case of rebleeding occurred in the incompletely

clipped aneurysms within the F U of a maximum o f 93

months. David et al. estimated the risk of rebleeding in aneu-

rysms with postoperative remnants as 1.5% per year [9]. A

series of 715 surgically treated patients reported by Feuerberg

Table 5 Behavior of dog-ear re-

siduals in follow-up (n =33)

Stable size in

Decreased size in

Closed in

Increased in

size

Number of aneurysm residuals n,

(%)

22 (67) 3 (9) 6(18) 2 (6)

Table 6 Behavior of broad-based

residuals in follow-up (n =7)

Stable size in FU Decreased size in FU Increased in size

Number of aneurysm residuals n, (%) 4 (60) 1 (14) 2 (28)

Acta Neurochir

et al. revealed a risk of rebleeding in aneurysm residuals of

0.38–0.79% per year, leading to a discussion of whether this

risk of rebleeding might justify the risk of reoperation [15].

Rauzzino et al. determined a relatively high risk of rebleeding

in aneurysm remnants. Surgery in 312 aneurysms led to a

remnant rate of 4.2% (n = 13). Only 4 of these remnants were

not treated immediately after initial surgery. All 4 of these

remaining aneurysm remnants became symptomatic within 2

years: 3 with a new SAH and 1 because of a local mass effect

[28]. Configuration of the remnants was not further specified

in this study.

Furthermore, radiation exposure, periprocedural complica-

tions, and costs should also be factored into the decision for

invasive angiographic controls. The development of less in-

vasive but adequate imaging procedures with lower radiation

exposure for the patient, such as metal artifact reduced MRI,

would be desirable. However, even the most recent, newly

developed MRI sequences are not able to suppress the artifacts

so strongly to be able to determine the fine differences in size

or configuration of the neck remnant [16]. The MRI is nowa-

days much more useful in checking untreated aneurysms or in

excluding de novo formations in predisposed patients.

CT angiography (CT-A) is less invasive and has been com-

pared to classical DSA in different studies. The sensitivity for

detection of postoperative aneurysm remnants varied between

50–100% comparing CT-A to DSA [6, 11, 14, 23, 30, 33, 34].

The precision of the CT-A strongly decreases with the usage

of multiple clips, in cases with posterior circulation aneurysms

and in small remnants.

Sagara et al. came to the conclusion that the usage of mul-

tiple clips is an indication for 3D DSA [30]. Bharatha et al.

reported a sensitivity of 88% for the detection of aneurysm

remnants after clipping when comparing DSA to CT-A,

whereas the sensitivity for a small neck remnant (mean size

1 mm) was only 20% [6].

Dundar et al. compared traditional DSA to subtraction CT-A

and came to the conclusion that DSA remains the gold standard

as residuals < 3 mm are not reliably examined with CT-A [14].

In our opinion and according to previous publications, CT-A

might be suitable, for long-term follow-up controls when DSA

controls were initially stable and CT-A quality is good [17].

Study limitations

One limitation of our study is its retrospective data collection.

Furthermore, FU is not available for almost half the patients

with incompletely occluded aneurysms, either due to the poor

clinical condition of certain SAH patients or due to the esti-

mated low-risk factors based on patient’s postoperative angi-

ography and medical history. This may obscure the true data

Fig. 4 a Preoperative DSA of an Acoma aneurysm in a patient with SAH

H&H II; b postoperative DSA 1 showed a broad-based aneurysm residual

and the patient underwent revision surg ery on the same d ay; c

postoperative DSA 2 demonstrates now complete occlusion of the resid-

ual, which was achieved by placement of further clips

Fig. 3 a Preoperative DSA

demonstrating an incidental

paraophthalmic ICA aneurysm

which was scheduled for clipping;

b postoperative DSA reveals

small dog-ear residual. This pa-

tient was scheduled for follow-up

DSA, which showed a stable

result

Acta Neurochir

concerning growth dynamics of incompletely occluded

aneurysms.

Conclusions

MCA aneurysms appear to have a lower risk for postoperative

aneurysm residuals than is observed for an aneurysm in other

locations. A large part of dog-ear residuals appear to remain

stable, decrease in size, or close during FU. Management of

aneurysm remnants should consider individual risk factors

and the remnant configuration.

Funding Open Access funding enabled and organized by Projekt DEAL.

Compliance with ethical standards

Conflict of interest The authors declare that they have no conflict of

interest.

Ethical approval All procedures performed in studies involving human

participants were in accordance with the ethical standards of the institu-

tional and/or national research committee and with the 1964 Helsinki

declaration and its later amendments or comparable ethical standards.

Open Access This article is licensed under a Creative Commons

Attribution 4.0 International License, which permits use, sharing, adap-

tation, distribution and reproduction in any medium or format, as long as

you give appropriate credit to the original author(s) and the source, pro-

vide a link to the Creative Commons licence, and indicate if changes were

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