sciences

Case Report The Iatrogenic Development of an Anterior Cerebral during Lamina Terminalis Fenestration–Genesis, Diagnosis and Therapy: Lessons Learned

Robert Bartoš 1,2, Jan Lodin 1, Aleš Hejˇcl 1,3,4,* , Martin Sameš 1 and Filip Cihláˇr 5

1 Department of , J. E. Purkyne University, Masaryk Hospital, 401 13 Ústí nad Labem, Czech Republic; [email protected] (R.B.); [email protected] (J.L.); [email protected] (M.S.) 2 Institute of Anatomy, 1st Medical Faculty, Charles University, 128 00 Prague, Czech Republic 3 International Clinical Research Center, St. Anne’s University Hospital, 656 91 Brno, Czech Republic 4 Institute of Experimental Medicine, Academy of Sciences of the Czech Republic, 142 20 Prague, Czech Republic 5 Department of Radiology, J. E. Purkyne University, Masaryk Hospital, 401 13 Ústí nad Labem, Czech Republic; fi[email protected] * Correspondence: [email protected]; Tel.: +420-777232793; Fax: +420-477112880

 Received: 5 May 2020; Accepted: 5 June 2020; Published: 9 June 2020 

Abstract: Intracranial (PSA) are scarcely presented in the literature. We describe the case of an intracranial PSA on the right anterior cerebral artery, which developed during the complicated surgical treatment of a ruptured right middle cerebral . The pseudoaneurysm grew over time and was co-incidentally diagnosed 3 months after the original surgery. The PSA was successfully treated by coiling. In cases of vascular injuries during complicated brain surgery, the timely and careful radiological diagnosis of such a lesion is necessary to allow its fast and proper treatment and thus prevent the patient from potential risks.

Keywords: intracranial pseudoaneurysm; brain edema; external ventricular drainage; lamina terminalis

1. Introduction Intracranial pseudoaneurysms (PSA) are rare vascular entities which occur in cases of head trauma, vascular collagenopathies such as Marfan’s syndrome, , or aneurysm rupture. Furthermore, they can be iatrogenic, developing after endoscopic surgery in the sellar area, endovascular procedures of intracranial vessels, external ventricular drain insertion or even a rare case of PSA occurrence following a transcallosal approach. Generally speaking, literature concerning PSA occurrence following aneurysm surgery is, for the most part, discreetly silent. It is certainly a rare complication of these procedures. We found only three cases of pseudoaneurysm development in association with aneurysm surgery in the current literature; all three of them were treated surgically [1–3]. On the other hand, various types of endovascular therapy for PSA are available. The deconstructive treatment of a PSA by occluding the injured artery requires sufficient collateral flow [4]. Reconstructive treatment means closing the site of the injury with coils while preserving the parent artery, sometimes utilizing remodeling tools such as a balloon, a stent or a flow diverter [5,6]. The use of a stent or a flow diverter requires long-time use of anti-platelet treatment. In addition, reconstructive treatment is associated with a higher risk of recanalization of the injured site.

Brain Sci. 2020, 10, 357; doi:10.3390/brainsci10060357 www.mdpi.com/journal/brainsci Brain Sci. 2020, 10,Brain 357 Sci. 2020, 10, x FOR PEER REVIEW 2 of 7 2 of 6

In this paper, we describe the iatrogenic development of an anterior cerebral artery (ACA) PSA which occurred during a technically difficult procedure of aneurysm clipping, In this paper,as well we as the describe successful theconcurrent iatrogenic endovascular development treatment of the of PSA. an anterior cerebral artery (ACA) PSA which occurred during a technically difficult procedure of middle cerebral artery aneurysm clipping, 2. Case Report as well as the successful concurrent endovascular treatment of the PSA. A 49-year-old man was admitted to his local neurological department in September of 2016 with symptoms of aphasia, aggressiveness and . A computed tomography (CT) and computed 2. Case Reporttomography (CTA) were performed and showed a with hemocephalus (Fisher 4) as well as an aneurysm of the right middle cerebral artery (MCA) bifurcation A 49-year-old(M12). manDue to wasdeterioration admitted of consciousness, to his local the patient neurological was sedated, department intubated and transported in September to of 2016 with symptoms of aphasia,our neurosurgical aggressiveness department for further and confusion.treatment. After A consultation, computed the patient tomography was indicated (CT) for and computed acute surgical clipping of the aneurysm by the surgeon on duty (the first author). A standard tomography angiographypterional (CTA) and durotomy were performed were performed; and however, showed major abrain subarachnoid edema with brain hemorrhage with hemocephalusherniation (Fisher through 4) as well the craniotomy as an aneurysm was present ofand the did rightnot allow middle cisternal cerebral . artery Antiedema (MCA) bifurcation measures, including lumbar drainage of the (CSF), were unsuccessful; therefore, (M12). Due tothe deterioration surgeon decidedof to utilize consciousness, major retraction the of th patiente was in sedated,order to quickly intubated gain access and to transported to our neurosurgicalthe lamina department terminalis, foraiming further to fenestrate treatment. it. Unfortunately, After consultation, this maneuver resulted the patient in arterial was indicated for acute surgical clippingbleeding from of this the area, aneurysm which was by successfully the surgeon controlled on with duty Surgicel, (the first and fenestration author). Aof the standard pterional lamina terminalis was microsurgically performed. This resulted in sufficient CSF decompression and craniotomy andbrain durotomy relaxation, which were allowed performed; the dissection however, of the carotid major and brain Sylvian edema cisterns and with resulted brain in herniationthe through the craniotomysuccessful was present clipping of and the ruptured did not aneurysm. allow When cisternal leaving dissection. the surgical field, Antiedema the surgeon did measures, not including observe any bleeding in the anterior cerebral artery area; the original source bleeding was controlled lumbar drainagewith ofa Surgicel the cerebrospinal tamponade. A CT fluidand CTA (CSF), were performed were unsuccessful; on the first postoperative therefore, day (Figure the surgeon decided to utilize major1A) retraction and showed no of complications. the frontal lobe in order to quickly gain access to the lamina terminalis, Postoperatively, the patient developed severe , which were successfully treated aiming to fenestratepharmacologically, it. Unfortunately, including with this a one-time maneuver pharmacological resulted angioplasty in arterial with bleeding milrinone. On from the this area, which was successfullyfifth controlled postoperative with day, a Surgicel, final CTA was and performed fenestration and demonstrated of the lamina successful terminalis clipping of was the microsurgically ruptured aneurysm without any other vascular anomalies apart from a previously described small performed. Thismirror resulted aneurysm inon the su ffileftcient (Figure CSF 1B). On decompression the 18th postoperative and day, brain the patient relaxation, was transferred which allowed the dissection of theto his carotid local hospital and Sylvianfor rehabilitation cisterns in good and clinical resulted condition—Glasgow in the successful coma scale clipping 15, lucid, of the ruptured aneurysm. Whenoriented leaving to place, theperson surgical and time and field, a residual the surgeon minor left-sided did hemiparesis not observe accented any on bleeding the upper in the anterior limb. Following the transfer, the patient’s clinical condition slowly deteriorated; he became cerebral arterydisoriented area; the and original showed signs source of bradypsychia. bleeding A was follow-up controlled CT performed with 3 months a Surgicel after the tamponade. surgery A CT and CTA were performedshowed widening on the of first the ventricles postoperative as well as daya pseudoaneurysm (Figure1A) (PSA) and in showed the distal A1 no anterior complications. cerebral artery (ACA) segment (Figure 1C).

Figure 1. Clipping of a ruptured middle cerebral artery (MCA) aneurysm complicated in the Figure 1. Clippingpostoperative of course a ruptured by middle and the cerebral development artery of a pseudoaneurysm (MCA) aneurysm (PSA). (A complicated). A in the postoperative coursecomputed by tomography vasospasm angiography and the (CTA) development performed on the of first a postoperative pseudoaneurysm day shows (PSA).clips after( A). A computed tomography angiographytreating an MCA aneurysm (CTA) (left performed arrow) and a on narrowi theng first of the postoperative right A1 segment (right day arrow), shows which clips after treating an MCA aneurysm (left arrow) and a narrowing of the right A1 segment (right arrow), which eventually led to later complications. (B). Postoperatively, the patient developed a severe vasospasm (white arrows) which was successfully treated including an intra-arterial pharmacological angioplasty with milrinone. (C). Brain computed tomography (CT) performed 3 months later presenting and a suspicious PSA of the distal right A1 segment.

Postoperatively, the patient developed severe vasospasms, which were successfully treated pharmacologically, including with a one-time pharmacological angioplasty with milrinone. On the fifth postoperative day, a final CTA was performed and demonstrated successful clipping of the ruptured aneurysm without any other vascular anomalies apart from a previously described small mirror aneurysm on the left (Figure1B). On the 18th postoperative day, the patient was transferred to his local hospital for rehabilitation in good clinical condition—Glasgow coma scale 15, lucid, oriented to place, person and time and a residual minor left-sided hemiparesis accented on the upper limb. Following the transfer, the patient’s clinical condition slowly deteriorated; he became disoriented and showed signs of bradypsychia. A follow-up CT performed 3 months after the surgery showed Brain Sci. 2020, 10, 357 3 of 6 widening of the ventricles as well as a pseudoaneurysm (PSA) in the distal A1 anterior cerebral artery (ACA) segment (Figure1C). We decided to treat the pathologies immediately, which necessitated the insertion of a caval filter due to deep . The following day, a ventriculo-peritoneal shunt (Certas, Medtronic) was implanted and, six days later, diagnostic angiography was performed and verified the presence of a 17 mm PSA in the distal A1 segment of the ACA (Figure2A,B). The PSA was coiled the following day (Cosmos Complex spirals into the aneurysm dome, Target Nano in the aneurysm ostium and the A1 segment of the ACA). The patency of the ipsilateral A2-3 via the anterior communicating artery was verified in the final angiogram, which also demonstrated complete occlusion of the PSA (Figure2C,D). No further neurological deficits developed following the endovascular procedure and the patient was successfully treated for suspected shunt meningitis (negative bacterial cultures) with meropenem. The patient was transferred to his local hospital and later released. Brain Sci. 2020, 10, x FOR PEER REVIEW 4 of 7

Figure 2. Diagnosis and endovascular treatment of an iatrogenic PSA of the A1 segment of the right Figure 2. Diagnosisanterior andendovascular cerebral artery (ACA). treatment(A). CT angiography of showing an iatrogenic a PSA of the right PSA A1 segment of the (arrow). A1segment of the right (B). The same PSA on a diagnostic digital substraction angiography (DSA, arrow) after implanting a anterior cerebral arteryventriculo-peritoneal (ACA). (A (VP)). CTshunt. angiography (C). An endovascular showing intervention for a the PSA PSA: of a guidewire the right in theA1 segment (arrow). (B). The same PSA onright a ACA. diagnostic (D). Angiography digital showing substraction completed coiling of angiographythe PSA and showing patency (DSA, of both arrow) A2 after implanting segments. a ventriculo-peritoneal (VP) shunt. (C). An endovascular intervention for the PSA: a guidewire in the Twenty-two months later, he was readmitted with a severe ; a CTA was performed right ACA. (D). Angiographyand did not show PSA showing recurrence completedor a subarachnoid coiling hemorrhage of thebut identified PSA and thrombosis showing of the patency of both A2 segments. straight, right sigmoid, right transverse and partial left transverse sinuses. Anticoagulation therapy was initiated and resulted in the recanalization of all sinuses, with the exception of the right transverse sinus. Afterwards, the patient and his family elected surgical clipping of the contralateral Twenty-two monthsmirror MCA later, aneurysm, he waswhich was readmitted performed by the with original a surgeon severe 11 months headache; later. The afinal CTA was performed procedure was uncomplicated (Figure 3A,C), and the patient was released with a minor organic and did not show PSApsychosyndrome, recurrence completely or self-d a subarachnoidependent, without hemiparesis. hemorrhage but identified thrombosis of the straight, right sigmoid, right transverse and partial left transverse sinuses. Anticoagulation therapy was initiated and resulted in the recanalization of all sinuses, with the exception of the right transverse sinus. Afterwards, the patient and his family elected surgical clipping of the contralateral mirror MCA aneurysm, which was performed by the original surgeon 11 months later. The final procedure was uncomplicated (Figure3A,C), and the patient was released with a minor organic psychosyndrome, completely self-dependent, without hemiparesis. Brain Sci. 2020, 10, 357 4 of 6

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Figure 3. Clipping of an unruptured left M2 aneurysm. (A). Intraoperative view of the left unruptured Figure 3. ClippingM2 aneurysm. of an ( unrupturedB). Intraoperative left view M2 after aneurysm. successful clipping (A). the Intraoperative M2 aneurysm. (C). viewCTA after of final the left unruptured M2 aneurysm.treatment: (B). Intraoperative a clip of a ruptured view right afterM12 bifurcations successful (arrow), clipping coiling of the the right M2 distal aneurysm. A1 (full white (C). CTA after final treatment: a cliparrowhead) of a ruptured and a clip of right unruptur M12ed left bifurcations M2 (empty arrowhead). (arrow), coiling of the right distal A1 (full white arrowhead)3. Discussion and a clip of unruptured left M2 (empty arrowhead). Iatrogenic pseudoaneurysms can occur as rare complications of several neurosurgical 3. Discussion procedures, including transsphenoidal surgery [7,8], external ventricular drain insertion [9,10] or stereotactic radiosurgery of cerebellopontine angle lesions [11,12]. The genesis of these lesions during Iatrogenicopen pseudoaneurysms neurosurgical procedures can is occursparsely as discussed rare complications in the literature, perhaps of several due to their neurosurgical rarity or procedures, including transsphenoidaldue to the fact that they surgery are traumatic [7,8], events external for the operating ventricular surgeons, drain not suitable insertion for publishing. [9,10 ] or stereotactic Dunn et al. [13] describe the development of a pericallosal artery PSA a year after the radiosurgery oftranscallosal cerebellopontine surgery of an optic angle glioma lesions in a child. [11 The,12 PSA]. was The later genesis resected, ofand thesethe artery lesions wall during open neurosurgicaldefect procedures was repaired is sparselyusing a graft discussed from the superfic in theial temporalis literature, artery. perhaps However, duethis report to their does rarity or due to the fact that theynot depict are traumatic PSA formation events during a for primarily the operating vascular procedure—aneurysm surgeons, not clipping. suitable A historical for publishing. description of such a situation is presented by Cosgrove et al. 1983 [1], who describe the formation Dunn et al.and [ 13rupture] describe of a pseudoaneurysm the development in close proxim of a pericallosality to a clipped arteryanterior PSAcommunicating a year afterartery the transcallosal surgery of ananeurysm optic glioma 21 days inafter a the child. primary The surgical PSA proc wasedure. later According resected, to the andauthors, the the artery primary wall defect was procedure was in no way complicated; however, they suggest possible trauma to a small branch of repaired usingthe a graftACA or from direct thetrauma superficial to the ACA during temporalis intraoperative artery. . However, The PSA this was report successfully does not depict PSA formation duringtreated a surgically primarily via an vascular additional procedure—aneurysmclip. Eleven years later, Rowed clipping.et al. [2] presented A historical a case of description of iatrogenic trauma to the (ACI) during the clipping of a ruptured aneurysm of such a situationthe isbasilar presented and superior by cerebell Cosgrovear artery et angle. al. 1983 The traumatic [1], who ACI describe lesion spontaneously the formation stopped and rupture of a pseudoaneurysmbleeding in and close was therefore proximity not directly to a clippedtreated duri anteriorng the primary communicating procedure. This scenario artery most aneurysm 21 days after the primaryresembles surgical our own procedure. case. Eight days According after the primary to the procedure, authors, the rupture the primary of a related procedure ACI was in no pseudoaneurysm occurred and a revision procedure requiring the sacrifice of the ACI was way complicated;performed. however, This unfortunately they suggest resulted in possible a permanen traumat neurological to deficit. a small In hindsight, branch the ofauthors the ACA or direct trauma to thesuggest ACA duringmore careful intraoperative observation of the hypotension. trauma site as well The as preventive PSA wasly suturing successfully the damaged treated surgically artery wall. The surgical treatment, however, led to a permanent neurological deficit which via an additionalemphasizes clip. the Eleven role of endovascular years later, therapy Rowed as the first-line et al. treatment [2] presented of such a PSA a unless case a ofbypass iatrogenic trauma to the internalis carotidneeded. artery (ACI) during the clipping of a ruptured aneurysm of the basilar and A more recent case report is presented by Shoja et al. [3], who describe the formation of a PSA superior cerebellar18 days artery after the angle. uncomplicated The traumatic surgical clipping ACI of lesionan anterior spontaneously communicating artery stopped (AComA) bleeding and was therefore not directlyaneurysm, treatedwhich was during preceded theby an primary unsuccessful procedure. coiling attempt. This A temporary scenario clip most was used resembles our own case. Eight daysduring after the thesurgical primary procedure. procedure, The PSA formed the agai rupturen on the AComA of a related but in an ACI opposite pseudoaneurysm direction to occurred the original aneurysm (superior direction). An attempted endovascular procedure was unsuccessful, and a revisionand procedure the PSA was requiring finally treated the surgically sacrifice with of a c thelip via ACI the original was performed. approach. The authors This unfortunately suggest resulted in a permanentseveral neurological possible reasons deficit. for PSA In hindsight, formation, incl theuding authors trauma suggestduring the more first endovascular careful observation of the procedure, residual aneurysm after clipping or ischemia of the artery wall due to the obliteration of trauma site as wellthe vasa as vasorum preventively by the surgical suturing clip. The the authors damaged consider artery direct wall.trauma Theto the surgical AComA or treatment, its however, led to a permanentbranches neurological to be the least probable deficit explanation which of emphasizes PSA formation. Our the case role is perhaps of endovascular most similar to therapy as the first-line treatment of such a PSA unless a bypass is needed. A more recent case report is presented by Shoja et al. [3], who describe the formation of a PSA 18 days after the uncomplicated surgical clipping of an anterior communicating artery (AComA) aneurysm, which was preceded by an unsuccessful coiling attempt. A temporary clip was used during the surgical procedure. The PSA formed again on the AComA but in an opposite direction to the original aneurysm (superior direction). An attempted endovascular procedure was unsuccessful, and the PSA was finally treated surgically with a clip via the original approach. The authors suggest several possible reasons for PSA formation, including trauma during the first endovascular procedure, residual aneurysm after clipping or ischemia of the artery wall due to the obliteration of the vasa vasorum by the surgical clip. The authors consider direct trauma to the AComA or its branches to be the least probable explanation of PSA formation. Our case is perhaps most similar to the case described by Rowed et al., involving PSA formation as a direct surgical complication, which thankfully resulted in a good outcome for the patient due to the effective endovascular treatment of the PSA [14,15]. It is Brain Sci. 2020, 10, 357 5 of 6 necessary to accent the fact that, in our case, reaching the lamina terminalis in conditions of extreme brain edema was a critical step in achieving sufficient brain relaxation and thus successful clipping of the ruptured aneurysm. Unlike the above mentioned case reports, the development of a PSA was thankfully diagnosed as a coincidental finding on a follow-up CT, not by rupture of the lesion. This resulted in timely endovascular treatment which allowed the successful treatment of the lesion with minimum neurological morbidity. Our department represents a medium-volume center in treating cerebral (400 aneurysms within 8 years). This is the first time such a case has occurred, and it has led to a paradigm shift in our approach when performing the surgical clipping of a ruptured brain aneurysm in conditions of severe brain edema. We believe this will be beneficial to future patients who are treated in similar conditions. In cases of suspected injury to an arterial vessel, large or small, extreme care must be taken to visualize, control and treat the suspected lesion by means of clip or suture. Tamponade in combination with local hemostatic agents is not a sufficient treatment strategy. In cases where such treatment is not possible, an early diagnosis must be obtained after the treatment of vasospasms, as these can delay PSA formation. We prefer CTA from digital substraction angiography (DSA) in order to avoid the 1% risk of a neurological deficit associated with angiographic assessment [16]. Nonetheless, a following endovascular procedure is then the treatment method of choice. In cases where the surgeon predicts severe brain edema on the basis of preoperative CT scans, the preoperative insertion of an external ventricular drain should be considered in cases with sufficient ventricle width. Insertion of a lumbar drain may not be sufficient in such cases. As a last resort, in cases of brain edema which is unresponsive to conventional antiedema therapy (hyperventilation, osmotherapy, lumbar drain), an emergent external ventricular drain may be inserted from the superior part of the pterional craniotomy [17], via the Park’s, Paine’s or Hyun´s point, rather than risking brain trauma by attempting to reach the lamina terminalis directly.

4. Conclusions The occurrence of an intracranial PSA after the surgical repair of an aneurysm is a rare complication. In cases of extensive perioperative brain edema which is unresponsive to regular management (osmotherapy, lumbar drain, hyperventilation), emergent external ventricular drain (EVD) implantation, rather than a direct approach to the lamina terminalis, should be attained in order to avoid vascular lesion complications. In case of any suspicion, targeted diagnostic steps such as repeated CTA are to be performed in order to confirm the development of a PSA, which would facilitate early treatment.

Author Contributions: R.B. performed the surgical treatment of the patient and wrote the manuscript. J.L. participated in writing the paper and most of its editing. A.H. treated the patient, collected the data and wrote the manuscript. F.C. performed the angiography part of the study, edited the manuscript. M.S. treated the patient, supervised the whole manuscript, performed final review and editing. All authors have read and agreed to the published version of the manuscript. Funding: This research was funded by a grant No. 17-32872A from the Czech Health Research Council (AZV CR),ˇ by the project no. LQ1605 from the National Program of Sustainability II (MEYS CR) and by the project FNUSA-ICRC no. CZ.1.05/1.1.00/02.0123 (OP VaVpI). Conflicts of Interest: The authors declare no conflict of interest.

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