Literature Review Clinical Vasospasm After an Extended Endoscopic Endonasal Approach for Recurrent Pituitary Adenoma: Illustrative Case and Systematic Review of the Literature Eric Suero Molina1, Alberto Di Somma2, Walter Stummer1, Francesco Briganti3, Luigi Maria Cavallo4 Key words - BACKGROUND: Cerebral vasospasm causing delayed cerebral ischemia after - Cerebral vasospasm transsphenoidal surgery is a rare but life-threatening complication. Reports in the literature after extended endoscopic endonasal approach (EEEA) are scarce. Considering the progressive use of this technique during recent years, a better understanding of the potential adverse effects after this procedure is needed. The aim of this report was to systematically analyze the current literature and discuss management and causes for cerebral vasospasm after EEEA surgery. - Delayed cerebral ischemia - Extended endoscopic Abbreviations and Acronyms CSF: Cerebrospinal fluid CT: Computed tomography DSA: Digital subtraction angiography EEEA: Extended endoscopic endonasal approach ICA: Internal carotid artery MRI: Magnetic resonance imaging SAH: Subarachnoid hemorrhage TCD: Transcranial Doppler From the 1Department of Neurosurgery, University Hospital Münster, Münster, Germany; 2Department of Neurological Surgery, Hospital Clínic de Barcelona, Universidad de Barcelona, Barcelona, Spain; 3Unit of Interventional Neuroradiology, Department of Advanced Biomedical Sciences, “Federico II” University, Naples, Italy; and 4Division of Neurosurgery, Department of Neurosciences, Reproductive and Odontostomatological Sciences, Universita degli Studi di Napoli “Federico II”, Naples, Italy To whom correspondence should be addressed: Eric Suero Molina, M.D. [E-mail: eric.suero@ukmuenster.de] Supplementary digital content available online Citation: World Neurosurg. (2019) 128:29-36. https://doi.org/10.1016/j.wneu.2019.04.046 Journal homepage: www.journals.elsevier.com/worldneurosurgery Available online: www.sciencedirect.com - METHODS: We performed a systematic search of the literature according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses statement and aimed to discuss relevant risk factors for cerebral vasospasm after extended transsphenoidal surgery. - RESULTS: Thirty-four cases of delayed cerebral vasospasm after transsphenoidal surgery were identified. Among these, 4 were operated with an EEEA. We provide an extensive literature review and discuss causes and management of this delayed complication. We further present the case of a young woman who underwent resection for a large suprasellar recurrent pituitary adenoma. Surgery and initial postoperative course were uneventful. On the eighth postoperative day, the patient developed aphasia and brachiofacial paresis. Digital subtraction angiography (DSA) demonstrated cerebral vasospasm, and repeated intra-arterial nimodipine infusion was administrated. The patient recovered completely and was discharged without neurologic deficits. - CONCLUSIONS: The threshold for DSA after unexplained neurologic deteri- oration after extended transsphenoidal surgery should be low, and cerebral vasospasm should be treated early and aggressively. Surgeons performing EEEA need to consider the possibility of this delayed complication. 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved. INTRODUCTION Clinical vasospasm after transsphenoidal tumor resection is a rare but potentially devastating complication. Onset and course of symptoms of cerebral vasospasm resemble those of patients after nontraumatic subarachnoid hemorrhage (SAH). Because of a lack of specific scientific evidence, treatment and management of vasospasms after transsphenoidal surgery are performed in a similar way to nontraumatic SAH. So far, approximately 30 patients have been reported in the literature.1-3 However, almost all these patients were operated in the microscopic era, and reports of vasospasm after an extended endoscopic endonasal approach (EEEA) are rare. As extended endonasal approaches further develop, surgery is becoming more extensive, leading to more manipulation in the suprasellar space. Here, we present a case of an EEEA for resection of a recurrent pituitary adenoma with delayed postoperative vasospasm, to heighten awareness for this possible complication when faced with secondary neurologic deterioration. Furthermore, we performed a systematic search of the literature to evaluate contributing factors with the goal of early identifying patients at risk. METHODS We performed a systematic literature search according to the Preferred Reporting WORLD NEUROSURGERY 128: 29-36, AUGUST 2019 Items for Systematic Reviews and MetaAnalyses statement.4 We searched the MEDLINE/PubMed database for articles published in English before November 2018 without neglecting publications of any earlier date. We searched for title and abstract using the following algorithm: “vasospasm” combined with “pituitary,” “transsphenoidal,” “macroadenoma,” “microadenoma,” “adenoma,” “craniopharyngioma,” or “transnasal.” The original search delivered 187 records, with 89 articles remaining after removal of duplicates. After excluding nonrelevant articles, 29 articles were included in the qualitative synthesis of this review.1-3,5-27 We performed a cross-reference check and included other www.journals.elsevier.com/world-neurosurgery 29 LITERATURE REVIEW ERIC SUERO MOLINA ET AL. CEREBRAL VASOSPASM AFTER EXTENDED ENDOSCOPIC ENDONASAL SURGERY Table 1. Cases of Vasospasm after EEEA from the Reviewed Literature Age Number of (years)/ Patients Sex Study 25 Pathology Classification Preoperative Intraoperative Encasement/ CSF Leak/ Suprasellar Displacement Subarachnoid Intraoperative Extension Approach of Arteries Space Opening Complications Zada et al., 2011 1 66/M PA Null-cell adenoma Yes EEEA Yes Yes n.r. Mansouri et al., 201217 1 75/M PA Null-cell adenoma Yes EEEA Yes Yes Bleeding from the (L) CV Koutourousiou et al., 201416 1 n.r. Yes EEEA n.r. n.r. n.r. Bierer et al., 20176 1 54/M Meningioma Grade I Yes EEEA Yes Yes n.r. Current study 1 23/F Rec. PA Null-cell adenoma Yes EEEA Yes Yes None n.r./elderly Meningioma CSF, cerebrospinal fluid; SAH, subarachnoid hemorrhage; M, male; PA, pituitary adenoma; EEEA, extended endoscopic endonasal approach; n.r., not reported; ACA, anterior cerebral artery; L, left, R, right; PCA, posterior cerebral artery; i.a., intra-arterial; Tc, transcranial; RH, right hemiparesis; Sc, supraclinoid; MCA, middle cerebral artery; HT, hypertension; HV, hypervolemia; EVD, external ventricular drainage; HC, hydrocephalus; GOS, Glasgow Outcome Scale; F, female; Rec., recurrent; ICA, internal carotid artery; i.v., intravenous; CV, cavernous sinus; PA, pituitary adenoma. articles when appropriate.28 We reviewed all published articles reporting cases or discussing postoperative vasospasm after endonasal transsphenoidal surgery. Patients presenting with primary pituitary apoplexy and early vasospasm were not included because of the different natural history of the disease. For further evaluation, we selected only patients having undergone EEEA. If not clearly described, a transsphenoidal approach was assumed. All procedures involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. Patient consent was acquired. For this type of systematic review, formal ethic committee consent is not required. RESULTS Among the reviewed articles, 34 cases of delayed vasospasm after transsphenoidal surgery could be identified, of which 4 were operated with an EEEA.6,16,17,25 Both meningioma (n ¼ 2) and pituitary adenoma (n ¼ 2) were reported as the underlying pathology. One patient was part of a large 30 www.SCIENCEDIRECT.com clinical series; hence, further clinical details are missing.16 From patients with available data, every patient had an intraoperative cerebrospinal fluid (CSF) leak and suffered from postoperative hematoma in the subarachnoid space. All tumors had suprasellar extension and encasement or displacement of adjacent arteries. Onset of symptoms was at a median of 8 days (range, 7e11 days). Management was mainly performed with intra-arterial vasodilatators, but also by induced hypertension and hypervolemia. All cases underwent subsequent surgery for hematoma evacuation, either transcranial6,25 or transsphenoidal.17 One patient suffered postoperative leak and meningitis. Mortality was reported in 2 cases (Table 1).16,17 Clinical Presentation A 23-year-old woman presented to the Division of Neurosurgery, Universitá degli Studi di Napoli “Federico II” with recurrence of a nonfunctioning pituitary adenoma. The patient had undergone a transsphenoidal subtotal microscopic resection in another department 2 years prior. Subtotal removal was achieved in the first surgery. Since then, because of partial hypopituitarism, the patient required thyroid hormonal substitution and oral desmopressin (60 mg 2 times per day). Prior to admission, residual tumor from the first procedure with right-sided extension in the suprasellar space with encasement of the internal carotid artery (ICA) and displacement of the arteries of the anterior circulation was found to be progressive on magnetic resonance imaging (MRI) (Figures 1A and 1B). Ophthalmologic evaluation revealed a marked reduction in retinal sensitivity in the nasal field with beginning atrophy of the left optic nerve and a visual acuity of 6 of 10, whereas the patient was blind in her right eye. Surgical Procedure. The suprasellar region was reached endoscopically through an endonasal transplanum approach. After performing a turbinectomy on the left side, the sphenoidal sinus was opened with subsequent removal of reconstruction material from the previous surgery. The bony opening was extended to the planum sphenoidale. The limits of the bone opening were the medial opticocarotid recess on both sides and the origin of the posterior ethmoidal arteries anteriorly. The tumor could be accessed after opening the dura. The subarachnoid space was opened, and the tumor was carefully WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.04.046 LITERATURE REVIEW ERIC SUERO MOLINA ET AL. CEREBRAL VASOSPASM AFTER EXTENDED ENDOSCOPIC ENDONASAL SURGERY Table 1. Continued Postoperative Clinical Day Onset Symptoms Onset SAH Involved Vessel 8 Consciousness deterioration Yes ACA (L, R), PCA (L) 7 RH, decreased consciousness Yes Sc ICA, MCA (L) n.r. n.r. n.r. n.r. w11 days Headache 8 No A1, M1 (L, R), basilar Brachiofacial Yes paresis (L), aphasia ICA, M1, A1 (R) Therapy Duration of Cerebral Symptoms Infarction i.a. verapamil No recovery HT, HV n.r. Follow-Up Surgeries Other Complications Outcome Yes Tc hematoma evacuation - Death Yes Endoscopic hematoma evacuation, EVD HC Significant impairment, mild RH, GOS score 3 n.r. n.r. Death n.r. n.r. n.r. Antibiotics n.r. Yes i.a. þ i.v. w14 days nimodipine, HT Twice for CSF Nasoseptal flap No “obvious” leak repair necrosis, postoperative neurologic deficits leak, meningitis Yes asymptomatic. On the eighth dissected from adjacent arteries. Papavpostoperative day, a contrast-enhanced erine solution was used intraoperatively. MRI was routinely performed showing After completing the resection, no residcomplete removal of the tumor. However, it ual tumor could be observed. Reconalso demonstrated a constriction of the struction was performed using distal right ICA and proximal M1 segment periumbilical fat, a vascularized nasoof the middle cerebral artery. Remarkably, septal flap, and a mucoperichondrial the patient was asymptomatic turbinate flap. No lumbar at that time. In the evening of drain was used (Figures 2A the same day, however, the and 2B, and Video 1). The patient developed mouth postoperative course was asymmetry accompanied by initially uneventful. slurred speech and moderate Histopathologic analysis Video available at www.sciencedirect.com weakness of the upper left demonstrated a null-cell adelimb. A CT angiogram showed noma according to the latest filiform constriction of the A1 segment of World Health Organization classificathe anterior cerebral artery, and the known tion.29 The Ki67/MIB1 index was 3%, narrowing of the middle cerebral artery and without p53 mutation. ICA on the right side, indicating vasospasm. Digital subtraction angiography Postoperative Events. Prophylactic therapy (DSA) revealed severe vasospasm. Intrawith intravenous nimodipine at a rate of 0.8 arterial nimodipine (10 mg) was locally mg/h was initiated immediately after surapplied with immediate enlargement of the gery. Vital signs and particularly systolic A1 and M1 segments (Figures 4A and 4B). blood pressure were monitored cautiously. Also, the intravenous nimodipine infusion A routine computed tomography (CT) scan rate was raised to 1.4 mg/h, and blood performed on the first postoperative day pressure elevated. On the ninth demonstrated minor pneumocephalus in postoperative day, DSA and intra-arterial the surgical field and a hyperdensity, nimodipine (10 mg) application was compatible with a hematoma without mass repeated as response to another episode of effect, in the suprasellar space worsening of the brachiofacial palsy. MRI (Figures 3Ae3C). The patient remained WORLD NEUROSURGERY 128: 29-36, AUGUST 2019 No - Slight mouth asymmetry, no further neurologic deficit at this time revealed a region of restricted diffusion in the corona radiata and the lenticular nucleus within the basal ganglia on the right side. DSA on postoperative day 14 showed an improvement, and a further 5 mg of intra-arterial nimodipine was applied (Figures 4A and 4B). Except for slight mouth asymmetry, neurologic function recovered completely. No further complications were recorded. Follow-up MRI 3 months after surgery demonstrated the previously observed mild diffusion restriction, a complete tumor resection, and no subarachnoid blood (Figures 5Ae5C). At the last day of follow-up, no facial paresis or other neurologic symptoms could be observed. DISCUSSION In nontraumatic SAH, vasospasm leading to delayed cerebral ischemia sometimes escalating to infarction is a large cause for mortality.30 One of the first reported cases of cerebral vasospasm after transcranial tumor resection was in a pituitary adenoma.31 Clinical presentation often comprises hemiparesis and aphasia, and cranial nerve palsies, seizures, hypesthesia or paresthesia, and cognitive decline.1,3 www.journals.elsevier.com/world-neurosurgery 31 LITERATURE REVIEW ERIC SUERO MOLINA ET AL. CEREBRAL VASOSPASM AFTER EXTENDED ENDOSCOPIC ENDONASAL SURGERY Figure 1. Preoperative magnetic resonance imaging with (A) coronal and (B) sagittal sequences demonstrating the large recurrence of a null-cell pituitary adenoma with suprasellar extension, encasement of the right internal carotid artery and cavernous sinus, and displacement of the anterior cerebral artery on the left side. Figure 2. Intraoperative endoscopic imaging during an extended endoscopic endonasal transplanum approach with visualization of the (A) right optic atrophic nerve and (B) displacement of the anterior artery complex with the anterior communicating artery (asterisk) and recurrent artery of Heubner (arrow) and (C) gray-reddish appearance of the lesion. 32 www.SCIENCEDIRECT.com Opening the Subarachnoid Space Blood leakage into the subarachnoid space, as it is with nontraumatic SAH, has been strongly associated with cerebral vasospasm,32-35 and after transsphenoidal surgery blood spillage has been related to delayed constriction of vessels.22 However, vasospasm is reported to occur not solely in the immediate vicinity of the tumor bed, suggesting a multifactorial pathogenesis: the interaction of inflammation processes with blood products, specifically oxyand methemoglobin releasing free radicals in the subarachnoid cisterns, decreasing levels of endothelial nitric acid, triggering lipid peroxidation, potentially damaging endothelia, and contributing to delayed cerebral ischemia.15,36,37 Not only the occurrence of SAH per se but also the size of the hematoma is relevant,7 as reported in nontraumatic SAH stratifying patients by location and volume of leaked blood.38 Conversely, in a recent review, 61.5% of patients with delayed vasospasm did not have any intraoperative CSF leak and therefore had no blood in the subarachnoid space,3 whereas another publication reports cerebral vasospasm only in 26.7% of 15 evaluated patients with postoperative SAH after transsphenoidal surgery.15 Patients with tumor encasement of adjacent arteries on preoperative imaging are prone to develop vasospasm,39 as was the case in all reviewed patients (Table 1). Even though rare, it appears that fluid from the cystic portion of craniopharyngiomas can induce vasospasm.12,40 In an animal experiment, Kamal et al.12 reported an onset of vasospasm 4 days after its instillation in the femoral vessel of rats. Spasmogenic Substances Vasoactive substances liberated from pituitary tumor or the hypothalamohypophyseal region (e.g., endothelin, angiotensin or lipid metabolites),41-43 or influencing intracellular calcium levels, have been discussed in the context of delayed cerebral ischemia.44 Hypothalamic damage or dysfunction caused by sympathetic activation with liberation of catecholamines can lead to secretion of spasmogenic factors.45-49 Others propose that hypothalamic dysfunction can induce polyuria WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.04.046 LITERATURE REVIEW ERIC SUERO MOLINA ET AL. CEREBRAL VASOSPASM AFTER EXTENDED ENDOSCOPIC ENDONASAL SURGERY leading to hypovolemia and vessel construction.7,50 Larger tumors with suprasellar extension could be adjacent to the hypothalamus, making this region vulnerable for injury. Although we deliberately dismissed cases initially presenting with pituitary apoplexy, it merits mention that secreting substances from necrotic pituitary tissue and blood can be vasoactive and lead to cerebral ischemia.9,51-54 However, these patients usually present with an earlier onset of symptoms. Figure 3. (A) Postoperative computed tomography imaging on the first postoperative day demonstrating suprasellar hematoma and small pneumocephalus (B) sagittal and (C) coronal T1 without contrast postoperative magnetic resonance imaging on the eighth postoperative day demonstrating suprasellar hematoma and small pneumocephalus with only mild mass effect. Electrolyte and Fluid Disorders Because of known diabetes insipidus prior to surgery, our patient received desmopressin regularly. No fluid disorder was observed postoperatively. Nevertheless, fluids need to be strictly controlled in this type of patients because diabetes insipidus after dehydration and volume contraction have also been reported to cause vasospasm.2,55 Fluid disorders might lead to microcirculation disturbances as a consequence of electrolyte imbalance and hypovolemia.12 Cerebral salt wasting syndrome and hyponatremia are known risk factors for vasospasm in nontraumatic SAH,56 and similar reports have shown comparable events after transsphenoidal surgery.15 Timing After transsphenoidal surgery, a recent review indicated a mean onset of 8 days postoperatively.1,2 Another older review described 20 cases where the mean time of onset of symptomatic vasospasm ranged from 3 to 13 days postoperatively.26 In our reviewed series, the mean onset time was 8 days (range, 7e11 days). In the cases reviewed in this article, 1 patient developed vasospasm even after 11 days, where the underlying etiology was most probably meningitis after postoperative CSF leak. Meningitis8,14 and postoperative CSF leak3 have been previously associated with cerebral vasospasm after transsphenoidal surgery. Figure 4. Digital subtraction angiography demonstrating (A) narrowing of the distal internal carotid artery and proximal M1 and A1 segment on the eighth postoperative day and (B) regression of vasospasm on postoperative day 14 with only slight residual of vasoconstriction in the M1 segment of the right middle cerebral artery. WORLD NEUROSURGERY 128: 29-36, AUGUST 2019 Management Induced hypertension and prophylaxis with the calcium-antagonist nimodipine are well acknowledged therapies.38,39 However, nimodipine, as a vasodilatator, leads to hypotension, which should be carefully monitored in these patients. www.journals.elsevier.com/world-neurosurgery 33 LITERATURE REVIEW ERIC SUERO MOLINA ET AL. CEREBRAL VASOSPASM AFTER EXTENDED ENDOSCOPIC ENDONASAL SURGERY Figure 5. Follow-up magnetic resonance imaging 3 months after surgery with complete tumor resection in (A) coronal and (B) sagittal T1 contrast-enhanced sequences and (C) mild diffusion restriction in the territory of the corona radiata without presence of subarachnoid hemorrhage. Reducing periods of hypotension before and after surgery, predominantly in elderly arteriosclerotic patients, seems furthermore to be favorable.51 Oral as opposed to intravenous nimodipine administration has been favored in the treatment of aneurysmal SAH. However, its actual value in preventing cerebral vasospasm remains uncertain.57 As a matter of fact, despite nimodipine being started on postoperative day 1, our patient still developed vasospasm on the eighth day. The reasons for such complications remain unclear. Even though evidence on hypervolemia does not support its benefit in the prophylaxis of vasospasm in nontraumatic SAH because of its vast complications (e.g., pulmonary edema58,59), even modern case reports describe hypervolemia as a possible management option.9,17,18 More invasive therapies include balloon 34 www.SCIENCEDIRECT.com angioplasty7,10,60 and intra-arterial nimodipine/papaverine applications. Doses reported for papaverine during intra-arterial injection ranged from 160 to 300 mg,15,19 whereas nimodipine was dosed at 2e10 mg.20 Further controlled trials are needed to prove its efficacy.20 In this context, von der Brelie et al.61 reported that single injections provide less complications compared with the continuous intraarterial application of nimodipine. Additionally, balloon angioplasty should be carefully considered because injured or irradiated vessels are vulnerable and can potentially rupture.41 Symptomatic cerebral vasospasm may be preventable. Transcranial Doppler (TCD) is a well-acknowledged method for the diagnosis and monitoring for vasospasm.62 The discussed cases in this article identified common risk factors; therefore, elective daily TCD should be carried out in patients with large sellar tumors with suprasellar extension and encasement or displacement of arteries, aggressive manipulation of suprasellar vessels during surgery, postoperative SAH, intra- and postoperative CSF leak, and/or postoperative meningitis. Induced hypertension could prevent manifest vasospasm, when detected early. It merits mention that several cases presented vasospasm in the supraclinoid ICA,3,7,17 which is not typically sound out during traditional TCD; hence, a transorbital evaluation of distal ICA flow should be considered.63 Furthermore, the threshold for initiating DSA after transsphenoidal surgery and unexplained neurologic deterioration should be low. It has to be stressed that while Eseonu et al.3 reported on transsphenoidal surgery of both microsurgical and endoscopic approaches, our case focused primarily on EEEA and the discussion of the occurrence of vasospasm after the surgical procedure. In the presented case, even though prophylaxis with nimodipine was given, the patient developed symptomatic vasospasm. A TCD performed on a daily basis could have perhaps provided further information to adjust the postoperative management (e.g., blood pressure management) in our patient. Limitations The small number of patients discussed in this article is a limitation. Publication bias is a further problem because severe cases are more frequently published than minor ones. Furthermore, not all information available in the reviewed articles was as detailed as needed. Similarly, approaches were not always precisely described; therefore, we might have missed relevant articles. CONCLUSIONS Mechanisms of vasospasm after transsphenoidal surgery are still poorly understood. Cerebral vasospasm can potentially lead to a high morbidity and mortality in patients. The threshold for DSA after unexplained neurologic deterioration after transsphenoidal surgery should be low, and cerebral vasospasm should be addressed early and aggressively. Surgeons performing EEEA need to consider WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.04.046 LITERATURE REVIEW ERIC SUERO MOLINA ET AL. the possibility complication. of this CEREBRAL VASOSPASM AFTER EXTENDED ENDOSCOPIC ENDONASAL SURGERY delayed REFERENCES 1. Alzhrani G, Sivakumar W, Park MS, Taussky P, Couldwell WT. Delayed complications after transsphenoidal surgery for pituitary adenomas. World Neurosurg. 2018;109:233-241. 2. Alotaibi NM, Lanzino G. Cerebral vasospasm following tumor resection. J Neurointerv Surg. 2013; 5:413-418. transsphenoidal surgery for pituitary tumors. Pituitary. 2013;16:260-269. 16. 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