usefulness of tumor blood flow imaging by intraoperative indocyanine green videoangiography in...

Peer-Review Reports

Usefulness of Tumor Blood Flow Imaging by Intraoperative Indocyanine Green

Videoangiography in Hemangioblastoma Surgery

Masato Hojo, Yoshiki Arakawa, Takeshi Funaki, Kazumichi Yoshida, Takayuki Kikuchi, Yasushi Takagi, Yoshio Araki,

Akira Ishii, Takeharu Kunieda, Jun C. Takahashi, Susumu Miyamoto

-OBJECTIVE: Hemangioblastomas remain a surgical challenge because of theirarteriovenous malformationelike character. Recently, indocyanine green (ICG)videoangiography has been applied to neurosurgical vascular surgery. The aimof this study was to evaluate the usefulness of tumor blood flow imaging byintraoperative ICG videoangiography in surgery for hemangioblastomas.

-METHODS: Twenty intraoperative ICG videoangiography procedures wereperformed in 12 patients with hemangioblastomas. Seven lesions were locatedin the cerebellum, two lesions were in the medulla oblongata, and three lesionswere in the spinal cord.

-RESULTS: Ten procedures were performed before or during dissection, and10 procedures were performed after tumor resection. ICG videoangiographycould provide dynamic images of blood flow in the tumor and its related vesselsunder surgical view. Interpretation of these dynamic images of tumor blood flowwas useful for discrimination of transit feeders (feeders en passage) and also forestimation of unexposed feeders covered with brain parenchyma. PostresectionICG videoangiography could confirm complete tumor resection and normalizedblood flow in surrounding vessels.

-CONCLUSIONS: In surgery for hemangioblastomas, careful interpretation ofdynamic ICG images can provide useful information on transit feeders andunexposed hidden vessels that cannot be directly visualized by ICG.

Key words- Hemangioblastoma- Indocyanine green videoangiography- Transit feeder- Tumor blood flow imaging

Abbreviations and AcronymsAVM: Arteriovenous malformationICG: Indocyanine greenMR: Magnetic resonancePICA: Posterior inferior cerebellar artery

Department of Neurosurgery, Kyoto UniversityGraduate School of Medicine, Kyoto, Japan

To whom correspondence should be addressed:Masato Hojo, M.D., Ph.D.[E-mail: [email protected]]

Citation: World Neurosurg. (2014).http://dx.doi.org/10.1016/j.wneu.2013.02.009

Journal homepage: www.WORLDNEUROSURGERY.org

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INTRODUCTION

Hemangioblastomas are highly vasculartumors that occur predominantly in thecerebellum and spinal cord and comprise1.5%e2.5% of intracranial and 3%e4% ofspinal tumors (1, 6, 11, 16). They mainlypresent as sporadic events, but 20%e30%ofcases are associated with vonHippel-Lindaudisease. Hemangioblastomas are histologi-cally benign tumors, and complete resectionresults in a favorable outcome. However,this tumor remains a surgical challengebecause of its arteriovenous malformation(AVM)elike character (1, 11, 16). In heman-gioblastoma surgery, it is important todistinguish between transit feeders (whichhave branches supplying the tumor) andadjacent nonfeeding arteries.Indocyanine green (ICG) video-

angiography has been recently applied to theneurosurgical field (2, 5, 10, 12, 13, 15).Previous reports have shown that intra-operative ICG videoangiography was usefulin extracranialeintracranial bypass surgeryand in the treatment of cerebral aneurysms(10, 13, 15). Here, we report the usefulness of

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tumor blood flow imaging by intraoperativeICG videoangiography in surgery forhemangioblastomas. ICG videoangiographycan provide useful information on transitfeeders (feeders en passage) and unexposedhidden vessels by careful interpretation ofdynamic images of tumor blood flow.

CLINICAL MATERIALS AND METHODS

Patient PopulationTwenty ICG videoangiography procedureswere performed in 12 patients withhemangioblastomas. The patient charac-teristics are summarized in Table 1. Themean age at the time of surgery was 47.3years (range 15e82 years). Seven lesionswere located in the cerebellum. Five ofthese 7 cerebellar lesions were cystic and2 lesions were solid. Two lesions werelocated in the medulla oblongata, and3 lesions were in the spinal cord.

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ICG VideoangiographyWe used an OPMI Pentero surgical micro-scope (Carl Zeiss, Co., Oberkochen,Germany) integrated with ICG video-angiography. In each procedure, ICG(8e12.5 mg) was injected into a peripheralvein as a bolus. Arterial, capillary, andvenous angiographic images could beobserved on the video screen in real time(12, 13). Images were recorded and reviewedimmediately for analysis. Recorded movieswere analyzed by FLOW800 software (CarlZeiss, Co.).

RESULTS

One to three ICG videoangiography proce-dures were performed in each operation.The timing of ICG videoangiography issummarized in Table 1. Among 20 ICGvideoangiograms, 10 procedures were per-formed before or during dissection, and 10

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Table 1. Summary of All Cases

PatientNumber

Age(Years)/Sex Location Type

Number of ICGVideoangiography

InformationObtained from ICGVideoangiography

Before TumorRemoval

After TumorRemoval

1 65/F Cerebellum Solid 1 1 3), 4), 5)

2 82/M Cerebellum Solid 2 1 1), 4), 5)

3 71/F Cerebellum Cystic 1 1 1), 4), 5)

4 28/F Cerebellum Cystic 0 1 4), 5)

5 37/M Cerebellum Cystic 0 1 4), 5)

6 32/M Cerebellum Cystic 0 1 4), 5)

7 37/F Cerebellum Cystic 1 0 1), 2)

8 48/M Medulla Solid 1 1 1), 4), 5)

9 15/F Medulla Cystic 1 1 1), 2), 4), 5)

10 68/F Spinal cord (Th9) Solid 1 1 1), 3), 4), 5)

11 54/M Spinal cord (L1) Solid 2 0 1)

12 30/M Spinal cord (L2-3) Solid 0 1 4), 5)

Information obtained from ICG videoangiography are as follows: 1) identification of feeders and drainers; 2) discriminationbetween transit feeders and adjacent non-feeding arteries; 3) estimation of unexposed feeders; 4) verification ofcomplete resection; 5) verification of normalized blood flow in surrounding vessels.

ICG, indocyanine green; M, male; F, female.

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MASATO HOJO ET AL. ICG VIDEOANGIOGRAPHY IN HEMANGIOBLASTOMA SURGERY

procedures were performed after removalof the tumor.In pre-resection studies, the feeding

arteries were visualized in six of seven cases(86%) by ICG. The tumor was visualized inall eight cases (100%), and the drainerswere visualized in seven of nine cases(78%). ICG videoangiography was availableonly for vessels visible in the surgicalfield, because ICG videoangiographycould not visualize vessels that werecovered with parenchyma. However, ICGvideoangiography could provide dynamicimages of blood flow in the tumor and itsrelated vessels under surgical view. Inter-pretation of these tumor blood flow imageswas extremely useful for discriminationbetween transit feeders and adjacent non-feeding arteries, and also for estimation ofunexposed hidden feeders. Transit feederswere filled with ICG in the early phase, andadjacent nonfeeding arteries were visual-ized by ICG in the late phase. PostresectionICG videoangiography could show thatcomplete resection had been achieved in all10 cases (100%). Moreover, normalizedblood flow in surrounding vessels could

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also be confirmed by ICG videoangiographyafter removal of the tumor in all cases.

ILLUSTRATIVE CASES

Case 1 (Patient 7)A 37-year-old woman with known von Hip-pel-Lindau disease presented with ataxia.Magnetic resonance (MR) imaging revealeda cystic lesion with a homogeneouslyenhancing mural nodule in the cerebellarhemisphere (Figure 1A). She underwentsurgery to remove the tumor. In the surgery,we could easily detect the mural noduleand the main feeding artery. However, itwas difficult to distinguish between transitfeeding arteries and adjacent nonfeedingarteries. Therefore, ICG videoangiographywas performed and the recorded movie wasanalyzed by FLOW800 software. At first, themain feeding artery was filled with ICG(Figure 1B,C, open arrowhead [1]). After4 seconds, the draining vein (open arrow [2])and the vessel indicated by arrow (3) werevisualized (Figure 1D). After 7 seconds, thevessel indicated by arrowhead (4) was filled

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with ICG (Figure 1E). The mural nodule wasvisualized underneath the thin cyst wall byICG (Figure 1E). The intensity diagramanalyzed by FLOW800 clearly showed thevariation of blood flow in these vessels(Figure 1F). These findings indicated thatthe artery indicated by arrow (3) was a transitfeeder (which had branches supplying thetumor) and that the artery indicated byarrowhead (4) was an adjacent nonfeedingartery. According to these findings, wecarefully dissected the tumor and couldcoagulate all feeders. Then,we could removethe tumor completely.

Case 2 (Patient 9)A 15-year-old girl presented with headacheand nausea, and MR imaging revealeda cystic lesion with a homogeneouslyenhancing mural nodule in the medullaoblongata (Figure 2A). A cerebral angio-gram showed a highly vascularized tumorfed by the posterior inferior cerebellarartery (PICA) (Figure 2B). She underwentsurgery to remove the tumor with thepreoperative diagnosis of hemangio-blastoma. In the surgery, we carefullychecked complex vasculatures around thehighly vascular tumor, and we could detectthe main feeding artery from the PICA.After clipping this main feeding artery, ICGvideoangiography disclosed that the flow ofthe tumor was reduced (Figure 2C-F). Thedraining vein and the artery coursing alongthe upper part of the tumor were filled withICG about 3 seconds after the PICA wasvisualized (Figure 2E). In contrast, theartery coursing along the lower part of thetumor was filled with ICG about 10 secondsafter the PICA was visualized (Figure 2F).These findings indicated that the arterycoursing along the upper part of the tumorwas a transit feeding artery (which hadbranches supplying the tumor) and that theartery coursing along the lower part of thetumor was an adjacent nonfeeding artery.According to this interpretation, we care-fully dissected the upper side of the tumor,and we could detect and coagulate residualfeeding arteries. After that, we couldremove the tumor completely. Finally, ICGvideoangiography showed complete tumorresection and normalized blood flow insurrounding vessels (Figure 2G, H).

Case 3 (Patient 1)A 65-year-old woman presented withdizziness, and MR imaging revealed

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Figure 1. Magnetic resonance imaging revealed a cystic lesion with a homogeneously enhancingmural nodule (arrowhead) in the cerebellar hemisphere (A). Surgical view (B) and indocyanine green(ICG) videoangiography (CeE) at operation. At first, the main feeding artery (open arrowhead, 1) wasfilled with ICG (C). After 4 seconds, the draining vein (open arrow, 2) and the transit feeder (arrow,3) were visualized (D). After 7 seconds, the adjacent nonfeeding artery (arrowhead, 4) was filled withICG (E). The intensity diagram analyzed by FLOW800 (F) clearly showed the variation of blood flow inthese vessels (1, main feeder; 2, drainer; 3, transit feeder; 4, adjacent nonfeeding artery).

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a well-enhancing tumor in the cerebellarhemisphere (Figure 3A). A cerebral angio-gram showed a highly vascularized tumorfed by the PICA (Figure 3B). She underwentsurgery to remove the tumor with thepreoperative diagnosis of hemangio-blastoma. In the surgery, dissection of thetumor was started after the main feeding


artery was coagulated. Although bleedingoccurred during dissection, hemostasiscould be easily achieved by bipolar coagu-lation. However, soon after that, the tumorbegan to enlarge (Figure 3C). This wasassumed to be due to incomplete oblitera-tion of feeding arteries and damage tovenous drainage by coagulation. At that

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time, ICG videoangiography disclosed thatthe tumorwas graduallyfilledwith ICG fromthe rostral side of the tumor to the caudalside, which indicated that feeding arteriesremained in the rostral side of the tumor(Figure 3D-F). According to this finding, therostral side of the tumor was dissectedand residual feeding arteries could becoagulated. After that, the tumor could beremoved without further bleeding. Finally,ICG videoangiography showed no residualtumor and normalized blood flow in vesselsaround the removal cavity (Figure 3G, H).

Case 4 (Patient 10)A 68-year-old woman presented with grad-ually worsening dysesthesias in legs. SpinalMR imaging revealed a well-enhancingintramedullary lesion at the Th 9 level(Figure 4A, B). She underwent surgery toremove the tumor with the preoperativediagnosis of spinal hemangioblastoma.After opening the dura mater, a varix-likelesion with many corkscrew-like vessels wasapparent on the dorsal surface of the spinalcord (Figure 4C). Although we carefullychecked these complex vasculatures on thespinal cord, we could not distinguishfeeding arteries from these complex cork-screw-like vessels. ICG videoangiographyshowed that the varix-like lesionwas initiallyfilled with ICG and then the corkscrew-likevessels were gradually filled with ICG(Figure 4D-F). This finding suggested thatthe varix-like lesion is the tumor and thecorkscrew-like vessels are draining veins,and that feeding arteries had not beenexposed yet. We carefully dissected thetumor and could detect the feeding arteries.After coagulation of all feeding arteries, weremoved the tumor completely (Figure 3G).ICG videoangiography showed no residualtumor and normalized blood flow in vesselsaround the removal cavity (Figure 4H).

DISCUSSION

Hemangioblastomas are highly vasculartumors that have AVM-like characters.Therefore, strategies based on the cerebro-vascular surgery are necessary for the treat-ment of this tumor (1, 11, 16). First of all,identification and elimination of feedingarteries of the tumor should be done insurgery.With diminishing blood supply, thetumor shrinks and then careful dissectionaround the tumor margin should be carriedout (1, 11, 16). It has been reported that



Figure 2. Magnetic resonance imaging revealeda cystic lesion with a homogeneously enhancingmural nodule (arrowhead) in the medullaoblongata (A). Cerebral angiogram showeda highly vascularized tumor (arrowhead) fed bythe posterior inferior cerebral artery (PICA)(B). Surgical view (C, G) and indocyanine green(ICG) videoangiography (DeF and H) at operation.After clipping the main feeding artery, ICGvideoangiography disclosed that the flow of thetumor was reduced (CeF; left is the caudal sideand right is the rostral side). The draining vein(open arrowhead) and the artery coursing alongthe upper part of the tumor (arrow, transitfeeder) were filled with ICG about 3 secondsafter the PICA (open arrow) was visualized (E). In

contrast, the artery coursing along the lower part of the tumor (arrowhead, adjacent nonfeeding artery)was filled with ICG about 10 seconds after the PICAwas visualized (F). After removal of the tumor, ICG videoangiography showed no residual tumor and normalized blood flow in vessels around the removalcavity (G, H).

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intraoperative microvascular Doppler isuseful to distinguish between the feedingarteries and draining veins of hemangio-blastomas (14). Recently, it has beenalso reported that power Doppler flowsonography is useful for surgery of heman-gioblastomas (3). However, it is notalways easy to identify all feeding arteriesand draining veins during the surgeryof hemangioblastomas, and premature


occlusion of draining veins can lead todisastrous swelling and hemorrhage of thetumor (1, 16).

Advantages and Limitations of ICGVideoangiographyRecently, intraoperative ICG video-angiography has been applied to theneurosurgical field (2, 5, 7, 10, 12, 13, 15).Previous reports have shown that ICG


videoangiography was useful duringextracranialeintracranial bypass surgeryand in the treatment of cerebral aneurysms(10, 15). Recently, the efficacy of intra-operative ICG videoangiography in thetreatment of cerebral AVMs has beenreported (12, 13). Compared with intra-operative digital subtraction angiography,ICG videoangiography can provide thesame view as a surgical one. In ICG

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Figure 3. Magnetic resonance imaging revealeda well-enhancing tumor (arrowhead) in the leftcerebellar hemisphere (A). Cerebral angiogramshowed a highly vascularized tumor (arrowhead) fedby the posterior inferior cerebral artery (PICA) (B).Surgical view (C, G) and indocyanine green (ICG)videoangiography (DeF and H) at operation. Aftercoagulation of the bleeding point, the tumor began toenlarge (C). At that time, ICG videoangiographydisclosed that the tumor was gradually filled with ICGfrom the rostral side of the tumor to the caudal side(arrows), which indicated that feeding arteries mightremain in the rostral side of the tumor (D: 3 secondsafter cerebellar circulation was visualized by ICG, E:20 seconds, F: 80 seconds after that; left is the rostralside and right is the causal side. Arrowhead showsthe draining vein, and open arrow indicates the PICA).After removal of the tumor (G), ICG videoangiographyshowed no residual tumor and normalized blood flowin vessels around the removal cavity (G, H; openarrow indicates the PICA).

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Figure 4. Spinal magnetic resonance imaging revealed a well-enhancing intramedullary lesion(arrowhead) at the Th 9 level (A, B). Surgical view (C, G) and indocyanine green (ICG)videoangiography (DeF and H) at operation. After opening the dura mater, a varix-like lesion(arrowhead) with many corkscrew-like vessels (arrows) was apparent on the dorsal surface of thespinal cord. ICG videoangiography showed that the varix-like lesion was initially filled with ICG (D) andthen corkscrew-like vessels were gradually filled with ICG (E, F), suggesting that the varix-like lesionwas the tumor and corkscrew-like vessels were draining veins but not feeding arteries (D: 3 secondsafter cerebellar circulation was visualized by ICG, E: 10 seconds, F: 20 seconds after that; left is therostral side and right is the caudal side). After the tumor was removed, ICG videoangiography showedno residual tumor and normalized blood flow in vessels around the removal cavity (G, H).

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videoangiography, all images are inte-grated into the operative view. Therefore, itis very easy to interpret the results and tohave a comprehensive anatomic orienta-tion. This is one of the great advantages ofintraoperative ICG videoangiography.Furthermore, ICG videoangiography isa simple, easy, and safe method that can bemade available in a matter of minutes andcan be easily repeated. It is not necessary forthe surgeons to interrupt the operation forICG videoangiography.


However, ICG videoangiography has thelimitation that it is available only for vesselsvisible in the surgical field (13). ICG video-angiography cannot visualize vessels that arecovered with parenchyma. In the operationofdeep-seated lesions, it isnot easy to clearlyvisualize vessels around the lesion. Insurgery for a nodular hemangioblastomawith a large cyst, the main difficulty is tolocate the nodule hidden behind the whitecyst wall. In case 1 (patient 7), the muralnodule was visualized underneath the thin


cyst wall by ICG (Figure 1E). However, ourdata cannot demonstrate whether ICG vid-eoangiography can visualize such a lesionhidden behind the white cyst wall, althougha hemangioblastoma can be visualizedunderneath adhesive scar tissue by ICG (4).In contrast, ICG fluorescence can penetratethe duramater, and so cortical vessels can beevaluated before opening of the dura mater(5). In patient 2, we removed a solid cere-bellar hemangioblastoma that was attachedto the tentorium via an occipital trans-tentorial approach. In the surgery, we per-formed ICG videoangiography beforeincising the tentorium in order to locate thetumor. However, the tumor could not bevisualized underneath the tentoriumby ICG.ICG fluorescence cannot penetrate thetentorium.

Lessons Learned from ICGVideoangiography in AVM SurgeryIn surgery for AVMs, ICG video-angiography can visualize the superficialnidus and drainers, but cannot visualizethe feeders, nidus, and drainers that arecovered with parenchyma (13). However,ICG videoangiography can provide imagesof dynamic flow changes in the nidus afterclipping or coagulating of feeders underthe operative microscopic view (13). Insurgery for hemangioblastomas, the sameeffects of ICG videoangiography are ex-pected as in surgery for AVMs. ICG vid-eoangiography can visualize vascular-richtumors, feeders and drainers like AVMs.However, although the nidi of AVMs aredemonstrated as vascular tangles by ICG,hemangioblastomas are visualized ashomogenously hyperfluorescent masses byICG, because hemangioblastomas have nointervening parenchyma within the lesion.

Usefulness of Dynamic Flow Images ofICG Videoangiography inHemangioblastoma SurgeryICG videoangiography can provide imagesofflowdynamics in the tumorunder surgicalview. In hemangioblastoma surgery, it isimportant to distinguish between transitfeeding arteries (which have branchessupplying the tumor) and adjacent non-feeding arteries. In our series, we coulddistinguish between transit feeders andadjacent nonfeeding arteries by dynamicICG images. Based on the timing of ICGfilling of drainers, we can distinguishbetween these vessels as follows. At first,

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main feeding arteries are filled with ICGbefore drainers are visualized by ICG. Next,transit feeders are filled with ICG at almostthe same time as drainers. Last, adjacentnonfeeding arteries are visualized severalseconds after drainers are filled with ICG.We could also estimate the unexposedfeeding arteries when the tumor wereenlarged due to the damage of venousdrainage, and we could successfully detectthe residual feedingarteries and could totallyremove the tumor without damage to thesurrounding brain. ICG videoangiographycan provide useful information on unex-posed vessels by careful interpretation offlowdynamic imagesof the tumor. This kindof use of ICG videoangiography is consid-ered very helpful in surgery for hemangio-blastomas. Unlike in the surgery for AVMs,ICG videoangiography after tumor removalis not so useful in the surgery for heman-gioblastomas, because a careful circumfer-ential dissection can ensure the totalremoval of the tumor.

ICG Videoangiography for SpinalHemangioblastomasIn surgery for spinal hemangioblastomas, itis very important to identify feeding arteriesand draining veins from complex vascula-tures on the spinal cord (6, 9). Hwang et al.reported a case of spinal hemangioblastomatreated using intraoperative ICG video-angiography (4). In this report, ICG video-angiography clearly revealed a residualhemangioblastoma underneath adhesivescar tissue.Murakami et al. reported anothercase of spinal hemangioblastoma (8). In thisreport, ICG videoangiography revealeda feeding artery from the posterior spinalartery, and after this feeding artery wascoagulated, the tumor was totally removed.In our case, careful analysis of images ofICG videoangiography allowed us to esti-mate feeding arteries that had not beenexposed. In surgery for spinal hemangio-blastomas, dynamic ICG images of tumorblood flow can also provide useful


information on unexposed vessels coveredwith parenchyma.

CONCLUSION

In surgery for hemangioblastomas, ICGvideoangiography can provide useful infor-mation on discrimination between transitfeeders and adjacent nonfeeding arteries bycareful interpretation of dynamic flowimages under the surgicalmicroscopic view.Interpretation of tumor blood flow can alsobe useful for estimating unexposed hiddenfeeding arteries and draining veins thatcannot be directly visualized by ICG.

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2. Ferroli P, Acerbi F, Albanese E, Tringali G,Broggi M, Franzini A, Broggi G: Application ofintraoperative indocyanine green angiography forCNS tumors: results on the first 100 cases. ActaNeurochir Suppl 109:251-257, 2011.

3. Glasker S, Shah MJ, Hippchen B, Neumann HP, vanVelthoven V: Doppler-sonographically guidedresection of central nervous system hemangio-blastomas. Neurosurgery 68:267-275, 2011 [discus-sion 274-275].

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7. Murai Y, Adachi K, Matano F, Tateyama K,Teramoto A: Indocyanin green videoangiographystudy of hemangioblastomas. Can J Neurol Sci 38:41-47, 2011.

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8. Murakami T, Koyanagi I, Kaneko T, Iihoshi S,Houkin K: Intraoperative indocyanine green video-angiography for spinal vascular lesions: case report.Neurosurgery 68:241-245, 2011 [discussion 245].

9. Oppenlander ME, Spetzler RF: Advances in spinalhemangioblastoma surgery. World Neurosurg 74:116-117, 2010.

10. Raabe A, Nakaji P, Beck J, Kim LJ, Hsu FP,Kamerman JD, Seifert V, Spetzler RF: Prospectiveevaluation of surgical microscope-integrated intra-operative near-infrared indocyanine green video-angiography during aneurysm surgery. J Neurosurg103:982-989, 2005.

11. Rachinger J, Buslei R, Prell J, Strauss C: Solidhaemangioblastomas of the CNS: a review of 17consecutive cases. Neurosurg Rev 32:37-47, 2009[discussion 47-48].

12. Takagi Y, Kikuta K, Nozaki K, Sawamura K,Hashimoto N: Detection of a residual nidus bysurgical microscope-integrated intraoperativenear-infrared indocyanine green videoangiographyin a child with a cerebral arteriovenous malfor-mation. J Neurosurg 107:416-418, 2007.

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Conflict of interest statement: The authors declare that thearticle content was composed in the absence of anycommercial or financial relationships that could be construedas a potential conflict of interest.

Received 31 July 2012; accepted 1 February 2013

Citation: World Neurosurg. (2014).http://dx.doi.org/10.1016/j.wneu.2013.02.009

Journal homepage: www.WORLDNEUROSURGERY.org

Available online: www.sciencedirect.com

1878-8750/$ - see front matter ª 2014 Elsevier Inc.All rights reserved.




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