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Clinical Neurology and Neurosurgery 116 (2014) 35– 40

Contents lists available at ScienceDirect

Clinical Neurology and Neurosurgery

jou rn al h om epage: www.elsev ier .com/ locate /c l ineuro

icrosurgical clipping of intracranial aneurysms assisted by greenndocyanine videoangiography (ICGV) and ultrasonic perivascular

icroflow probe measurement

lessandro Della Puppa ∗, Francesco Volpin, Giorgio Gioffre,riela Rustemi, Irene Troncon, Renato Scienza

epartment of Neurosurgery, Padua University Hospital, Padova, Italy

r t i c l e i n f o

rticle history:eceived 11 June 2013eceived in revised form 8 October 2013ccepted 9 November 2013vailable online 18 November 2013

eywords:ntracranial aneurysm

icro-surgerylippingreen indocyanine videoangiography

a b s t r a c t

Objectives: The purpose of this work is to assess the surgical and clinical outcome of intracranial aneurysmclipping performed combining the assistance of green indocyanine videoangiography (ICGV) and ultra-sonic perivascular microflow probe.Patients and methods: Data from patients affected with intracranial aneurysms who underwent micro-surgical clipping assisted by both techniques between May 2012 and April 2013 were retrospectivelyevaluated.Results: 26 patients with 34 aneurysms (25 unruptured) were enrolled. In a total of 11 aneurysms (32%),the vascular clip needed repositioning, since either the post-clipping microprobe assessment detecteda significant flow reduction of the explored vessels (8 cases, 23%) or ICGV identified a residual non-obliterated aneurysm (3 cases, 9%). A second clip repositioning was required in 3 cases (9%) because of

ICGV)ltrasonic perivascular microflow probe

dome remnant showed with ICGV. In all cases, final microprobe and ICGV assessments showed a completeexclusion of the aneurysm, without evidence of vascular flow impairment. Postoperatively, 1 patient (3%)presented a residual neck aneurysm. No permanent morbidity was reported.Conclusion: With the limits of our small case series, our results testify that the presented approach mayprovide high exclusion rate in the treatment of cerebral aneurysm with very low morbidity in selectedpatients.

. Introduction

The outcome of the microsurgical clipping of intracranialneurysms is strictly dependent on both the completeness ofneurysm exclusion by clip positioning and on parent or branchessels occlusion during surgery. Despite the use of innovativeechnologies and the improvement of micro-neurosurgical tech-iques, an incidence of 4–19% of aneurysm remnants is reported1–8], whilst major vessel occlusion rate has been reported asanging between 5% and 30% [1,4,9–12]. Microscope-integratedear-infrared indocyanine green videoangiography (ICGV) haseen recently applied to neurosurgery [13], and represents an

nnovation in microsurgical aneurysm clipping [14,15]. With thisechnique, a 0–14.3% rate of unexpected neck residuals [13,16–27],nd 6–7.3% of branch occlusion were reported by some authors

∗ Corresponding author at: Department of Neurosurgery, Padua University Hos-ital, Azienda Ospedaliera di Padova, via Giustiniani 2, 35128 Padova,

taly. Tel.: +39 049 8213641; fax: +39 049 8213672.E-mail address: alessandro.dellapuppa@sanita.padova.it (A. Della Puppa).

303-8467/$ – see front matter © 2013 Elsevier B.V. All rights reserved.ttp://dx.doi.org/10.1016/j.clineuro.2013.11.004

© 2013 Elsevier B.V. All rights reserved.

[16,25]. The microvascular ultrasonic flow probe is used for theintra-operative measurement of blood flow during aneurysmsurgery [28]. With this technique, no unexpected large vessel occlu-sions or strokes were evident in large series [29]. The purpose ofthis study is to assess the effectiveness and morbidity related tothe microsurgical clipping of intracranial aneurysms assisted bythe combined use of ICGV and microflow-probe.

2. Methods

2.1. Patient population

Over a period of 10 months, from May 2012 to March 2013, 94patients with intracranial aneurysms were treated at the Depart-ment of Neurosurgery of Padua University Hospital (Padova, Italy).Among these, 48 patients underwent microsurgical clipping and46 underwent endovascular treatment. Only 26 cases treated with

surgery were enrolled, in which the aneurysm size and locationenabled to safely expose both parent and branch arteries and there-fore allowed to perform both techniques. Size, location, and rupturestatus of each aneurysm were assessed with computed tomography

3 logy and Neurosurgery 116 (2014) 35– 40

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Table 1Clinical characteristics of patients (MCA, middle cerebral artery; ACA, anterior cere-bral artery; ICA, internal carotid artery; H&H, Hunt & Hess). See text for details.

Patients characteristicsTotal enrolled n. 26Age (years)

Median age 53Range 27–71

SexMale 12Female 14

Patients with multiple aneurisms 8H&H grade (n. patients)

H&H:0 17H&H:1 5H&H:2 4

WFNS grade (n. patients)0 171 72 2

Aneurysm characteristicsTotal n. 34

Ruptured 9Unruptured 25

LocationMCA 21ACA 8ICA 5

Size<7 mm 117–12 mm 1813–24 mm 5

6 A. Della Puppa et al. / Clinical Neuro

CT), CT-angiography (CTA), digital subtraction angiography imagesDSA).

.2. Intra-operative flow measurement with microflow-probe

Vascular flow measurements were performed using theicrovascular ultrasonic flow probe (Charbel Micro-flowprobe;

ransonic Systems, Inc., Ithaca, NY). This device consists of anlectronic flow detection unit and a flow sensing peri-vascularrobe. Flow measurements appear as a digital display on the detec-ion unit. In order to evaluate vascular flow, the probe uses therinciple of ultrasonic transit-time. Flow measurements in all theelevant vessels were performed before clipping, in order to obtain

baseline, and after clipping to confirm flow preservation. Accord-ng to previous experiences [29], we considered a drop >25% inost-clipping blood flow, in the context of stable end-tidal car-on dioxide (CO2) and mean arterial blood pressure values, to be

ndicative of vascular flow impairment. Consequently, when theost-clipping flow reduction was significant (i.e. more than 25%)r when ICGV was in keeping with aneurysm remnant or vascu-ar injury, the clip was immediately repositioned. Afterwards, flow

easurement was repeated, and a final ICGV control was alwayserformed.

.3. Intra-operative ICGV

Intraoperative ICGV was performed using a surgical micro-cope (OPMI® PenteroTM, The Carl Zeiss Co., Oberkochen, Germany)quipped with microscope-integrated near-infrared ICGV (Carleiss, Infrared 800TM, Meditec, Germany). Principles of ICGV guidedurgery have already been described in detail elsewhere [13].n brief, after the intravenous injection of indocyanine greenye (ICG), the operating field is illuminated with near-infrared

ight. Real-time angiographic images are displayed on a videocreen and recorded. ICGV was performed every time after floweasurement with microflow-probe. This happened in the post-

lipping phase, after evidence of preserved flow measurements wasbtained, (ICGV I) or after repositioning of clip (ICGV II). ICG-VA waslways performed after vascular flow reduction was ruled out withicroflow-probe.

.4. Pre and post-operative evaluation

Postoperative CT was performed in all patients straight afterurgery. CT-angiography was obtained within 3 months in allatients. Postoperative imaging studies were assessed by a neuro-adiologist, who was blinded to intra-operative microflow-probend ICGV findings. Clinical assessment was performed beforeurgery, then at 1st day, 1st week, and 3 months after surgery.orbidity was defined as the onset of new postoperative signs or

ymptoms after surgery.

.5. Endpoints and outcome measures

Intra-operatively, the following data were considered: (1) therequency of vascular flow impairment as detected by post-clippinglood flow measurement, defined as a 25% reduction in vascu-

ar flow; (2) the frequency of aneurysm remnant or vascular flowmpairment as detected by ICGV; (3) the rate of clip reposition-ng after intra-operative assessment with microflow-probe or ICGV.ostoperatively, we looked at the following features: (1) the cor-

elation of postoperative angiographic features, such as aneurysmac/neck exclusion and major vascular impairment, with the intra-perative findings, (2) evidence of stroke related to large vesselscclusion on postoperative imaging.

3. Results

3.1. Patients and aneurysms

26 patients (12 males and 14 females with an age rangingfrom 27 to 71 years) were treated for 34 intracranial aneurysms(see Table 1). 21 of these were located at the (middle cerebralartery) MCA, 8 at the ACA (anterior communicating artery), 5 atthe ICA (internal carotid artery). 25 aneurysms were unruptured,and 9 were ruptured. In all 17 patients with unruptured aneurysms,the neurological examination was negative. Among patients withbleeding aneurysms, 5 were admitted with a grade I SAH (H&H), 4with grade II. The aneurysms size was less than 7 mm in size in 11patients, between 7 and 12 mm in 18, and between 13 and 24 mmin 5 (Figs. 1 and 2).

3.2. Intra-operative assessment (see Table 2)

3.2.1. Flow measurementThe use of the flow probe was feasible in all the vessels of

interest. A total of 82 measurements were performed: 34 wereobtained at basal flow before clipping, and 34 after clip position-ing; 11 procedures were performed after clip re-positioning, onthe basis of the flow measurements findings – distal vessel flowlower than 75% of basal flow, 8 cases – and/or of the ICGV data –residual aneurysm neck or dome – 3 cases. No flow reductions wererecorded after first (11 cases) or second (3 cases) clip re-positioning.Finally, 8 out of 48 measurements showed a flow reduction >25%(16%).

3.2.2. ICGV

A total of 37 ICGV were performed. 26 of these were obtained

at basal time after clip positioning, and 11 after clip repositioningon the basis of the information gathered from flow measurement(significant blood flow reduction was found in 8 cases, 6 MCA, 1

A. Della Puppa et al. / Clinical Neurology and Neurosurgery 116 (2014) 35– 40 37

Fig. 1. Patient with left unruptured internal carotid artery bifurcation aneurysm. After clip positioning (a), flow reduction >25% at left A1 is detected with microflow probe( raphy

Iwpov

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b). Thus, clip is repositioned (c) and no remnants are visualized with video-angiog

CA and 1 ACA aneurysms) or from ICGV (residual aneurysm neck

as found in 3 cases, 2 MCA and 1 ACA aneurysms). After clip re-ositioning in 3 cases ICGV showed a neck remnant. Finally, 6 outf 37 procedures showed a neck-dome remnant (16%). No cases ofascular flow impairment were reported.

ig. 2. Patient with left unruptured middle cerebral artery bifurcation (a). No flow reductc). Thus second clip is positioned.

.

3.2.3. Clip repositioning

In 11 out of 34 clipped aneurysms (32%), clip needed to be repo-

sitioned. In 8 cases (23%) because the post-clipping microprobeassessment detected a significant flow reduction of the exploredvessels, and in 3 cases (9%) because ICGV identified a residual

ions are detected (b) but aneurismal remnant is identified with video-angiography

38 A. Della Puppa et al. / Clinical Neurology and Neurosurgery 116 (2014) 35– 40

Table 2Intra-operative data. Flow measurement: flow reduction > or <25% at microvascular ultrasonic flow probe assessment. Aneurysm remnant at indocyanine green videoan-giography (ICGV) assessment. (n): number of patients. See text for details.

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on-obliterated aneurysm. A second clip repositioning wasequired in 3 cases (27% of repositioned clips, 9% of total) becausef dome remnant showed with ICGV.

.3. Postoperative assessment

CT-angio scan was performed within three months after surgeryn all patients, while 18 patients underwent also DSA. In no caseneurysm dome remnants were observed. One case of neck residualas reported. In no cases vascular impairment or large vessel-

elated strokes were observed. Finally, no transient or permanentigns or symptoms related to vascular damage were reported. Noadiological findings of stroke related to large vessels occlusion onostoperative imaging were reported. Patients with unrupturedneurysm presented an uneventful postoperative course. Patientsith bleeding aneurysms completely recovered in all cases within

months (GOS 5).

. Discussion

The aim of treating aneurysms through microsurgical clippings to occlude the aneurysmal sac while preserving blood flow inarent and branch arteries. Many authors suggest that even theost experienced surgeons should not rely on simple observation

f the field through the operating microscope to establish whether vascular clip can be considered well positioned [1,4,9–11,30]. Inhe past, this concept led to the need of introducing new intra-perative assessment tools, in order to make clipping safer in termsf patients’ outcome. Some authors suggested the use of intraoper-tive intracranial Doppler to obtain flow measurements [9,31,32].owever, this technique, despite its easy use, has been proved to

ave several limitations and audio Doppler signals used to detectow reduction during aneurysm surgery are subjective methods,nd can be insufficient or deceptive [30]. Many authors recom-end the routine or selected use of intraoperative angiography in

aneurysm surgery, which is thought to be the “gold standard” indisplaying aneurysm neck residuals or vascular flow impairment[1,4,10–12,33–36]. Nevertheless, this procedure cannot be per-formed routinely at most Institutions, is expensive, time consumingand requires a well trained staff. Furthermore, the intra-operativeangiographical detection of vascular occlusion may exceed thetime limit before irreversible ischemia occurs. In recent years, twonew intra-operative assessment tools have been described: bloodflow measurement using an ultrasonic perivascular flow probe andICGV. The first procedure has been described by Charbel and col-leagues [28]. Flow measurement gives real time information aboutflow variations, and therefore assists clip positioning by providingan immediate proof that flow in parent and distal branches is pre-served. Its main disadvantage is that it does not supply informationregarding residual aneurysm remnants, which are reported in up to8% of cases [1,3,11]. In addition to this, it does not provide informa-tion about small vessel such as perforating arteries. The use of ICGVwas introduced by Raabe et al., who then reported a 90% correspon-dence of intra-operative ICGV findings with postoperative DSA. Thismethod allows a real time visualization of blood flow and it is afairly simple procedure. It does not entail the removal of the micro-scope away from the operatory field, and perforating arteries can bevisualized as well [13,17]. As regards larger ICGV studies, a residualaneurysm neck rate of 0–14.3% [13,16–26] and branch occlusion of6–7.3% have been reported [16,25]. The main disadvantages are thevisual restriction in the limits of the microscope field view, whichis narrow when compared with DSA, and the surface-restricted,bi-dimensional perspective it provides. Bearing in mind the limita-tions of flow probe and ICGV, we considered trying to improve theireffectiveness by combining them during surgery: after verifyingthrough micro flow probe the presence of a viable distal blood flow

after clipping, ICGV can give information as whether the aneurysmsac is completely excluded. Two other studies comparing intravas-cular monitoring technologies during aneurysm surgery have beenreported [18,19]. Gruber and colleagues compared the value of

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A. Della Puppa et al. / Clinical Neuro

CGV derived information with data from microvascular Doppleronography, intraoperative DSA, electrophysiological monitoringr in selected cases additional neuroendoscopy. Intra-operative clipeposition was needed in 24% of cases. Fisher et al. has describedhe utilization of microvascular Doppler sonography (qualitativeutput) and ICGV in aneurysm surgery, revealing a 4% branch occlu-ion and a 6% neck remnants. Conversely, no studies describing floweasurement using an ultrasonic perivascular flow probe and ICGV

ombined intra-operative assistance have been reported in litera-ure. Unfortunately, the design of our study cannot define how these of the ultrasonic microflow probe in conjunction with ICG-VAight affect outcomes. However, the high rate of clip replacement

n our patients could be the key to interpret the promising results ofhe present approach. Indeed, our approach led to intra-operativelip replacement in 32% of cases and in 23% of cases a compro-ised blood flow was specifically detected by the microprobe floweasurement. In our study, ICG video-angiography was used after

ow probe measurement to detect aneurysm sac residuals. Thisappened in 9% of patients, leading to clip repositioning. A sec-nd clip repositioning was required in 3 cases (9%) because ofome remnant showed with ICGV. We report no case of vascularow impairment, no large vessel-related stroke and no transitoryr permanent signs or symptoms related to vascular damage. Weeport only one case of aneurysm neck residual (3%). Final morbid-ty related to clipping was 0%. A limit in our data is that patients

ere not consecutively enrolled. In fact, only 26 out of 48 patientsho underwent clipping in the same period were monitored with

oth techniques and were consequently enrolled in the study. How-ver, we emphasize that, in our opinion, the present approach cane safely performed only in selected patients according to differ-nt factors such as size and location of aneurysm, brain slackness,AH grade. Thus, we should bear in mind that the morbidity rateeported in our study could be influenced by such selection criteria.ur work is a retrospective study on selected patients, since the usef this combined intra-operative assistance was feasible only whenneurysm and patient features enabled wide and safe exposure ofarent and branch arteries and aneurysm sac in the operating field.owever, our study testifies as, in selected cases, microsurgicallipping can safely achieve a high occlusion rate (close to 100%).

. Conclusions

With the limits of this small series, our results testify thatombining ICGV (green indocyanine videoangiography) and ultra-onic perivascular microflow probe in microsurgical clipping, mayrovide high exclusion rate of cerebral aneurysm with very loworbidity.

onflict of interest

The authors report no conflict of interests concerning the mate-ials or methods used in this study or the findings specified in thisaper.

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