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Ramazan Jabbarli, Daniela Pierscianek, Karsten Wrede, Philipp Dammann, Marc Schlamann, Michael Forsting, Oliver Müller and Ulrich Sure

OBJECTIVE

The complete clipping of a cerebral aneurysm usually warrants its sustained occlusion, while clip remnants may have far-reaching consequences. The aim of this study is to identify the risk factors for clip remnants requiring retreatment and/or exhibiting growth.

METHODS

All consecutive patients with primary aneurysm clipping performed at University Hospital of Essen between January 1, 2003, and December 31, 2013, were eligible for this study. Aneurysm occlusion was judged on obligatory postoperative digital subtraction angiography and the need for repeated vascular control. The identified clip remnants were correlated with various demographic and clinical characteristics of the patients, aneurysm features, and surgery-related aspects.

RESULTS

Of 616 primarily clipped aneurysms, postoperative angiography revealed 112 aneurysms (18%) with clip remnants requiring further control (n = 91) or direct retreatment (n = 21). Seven remnants exhibited growth during follow-up, whereas 2 cases were associated with aneurysmal bleeding. Therefore, a total of 28 aneurysms (4.5%) were retreated as clip remnants (range 1 day to 67 months after clipping). In the multivariate analysis, the need for retreatment of clip remnant was correlated with the aneurysm's initial size (> 12 mm; OR 3.22; p = 0.035) and location (anterior cerebral artery > internal carotid artery > posterior circulation > middle cerebral artery; OR 1.85; p = 0.003). Younger age with a cutoff at 45 years (OR 33.31; p = 0.004) was the only independent predictor for remnant growth.

CONCLUSIONS

The size and location of the aneurysm are the main risk factors for clip remnants requiring retreatment. Because of the risk for growth, younger individuals (< 45 years old) with clip remnants require a long-term (> 5 years) vascular follow-up.

Clinical trial registration no: DRKS00008749 (Deutsches Register Klinischer Studien)

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Philipp Dammann, Markus Barth, Yuan Zhu, Stefan Maderwald, Marc Schlamann, Mark E. Ladd and Ulrich Sure

High-resolution susceptibility weighted MR imaging at high field strength provides excellent depiction of venous structures, blood products, and iron deposits, making it a promising complementary imaging modality for cerebral cavernous malformations (CCMs). Although already introduced in 1997 and being constantly improved, susceptibility weighted imaging is not yet routine in clinical neuroimaging protocols for CCMs. In this article, the authors review the recent literature dealing with clinical and scientific susceptibility weighted imaging of CCMs to summarize its prospects and drawbacks and provide their first experience with its use in ultra–high field (7-T) MR imaging.

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Marvin Darkwah Oppong, Kathrin Buffen, Daniela Pierscianek, Annika Herten, Yahya Ahmadipour, Philipp Dammann, Laurèl Rauschenbach, Michael Forsting, Ulrich Sure and Ramazan Jabbarli

OBJECTIVE

Clinical data on secondary hemorrhagic complications (SHCs) in patients with aneurysmal subarachnoid hemorrhage (SAH) are sparse and mostly limited to ventriculostomy-associated SHCs. This study aimed to elucidate the incidence, risk factors, and impact on outcome of SHCs in a large cohort of SAH patients.

METHODS

All consecutive patients with ruptured aneurysms treated between January 2003 and June 2016 were eligible for this study. Patients’ charts were reviewed for clinical data, and imaging studies were reviewed for radiographic data. SHCs were divided into those associated with ventriculostomy and those not associated with ventriculostomy, as well as into major and minor bleeding forms, depending on clinical impact.

RESULTS

Sixty-two (6.6%) of the 939 patients included in the final analysis developed SHCs. Ventriculostomy-associated bleedings (n = 16) were independently predicted by mono- or dual-antiplatelet therapy after aneurysm treatment (p = 0.028, adjusted odds ratio [aOR] = 10.28; and p = 0.026, aOR = 14.25, respectively) but showed no impact on functional outcome after SAH. Periinterventional use of thrombolytic agents for early effective anticoagulation was the only independent predictor (p = 0.010, aOR = 4.27) of major SHCs (n = 38, 61.3%) in endovascularly treated patients. In turn, a major SHC was independently associated with poor outcome at the 6-month follow-up (modified Rankin Scale score > 3). Blood thinning drug therapy prior to SAH was not associated with SHC risk.

CONCLUSIONS

SHCs present a rare sequela of SAH. Antiplatelet therapy during (but not before) SAH increases the risk of ventriculostomy-associated bleedings, but without further impact on the course and outcome of SAH. The use of thrombolytic agents for early effective anticoagulation carries relevant risk for major SHCs and poor outcome.

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Alejandro N. Santos, Laurèl Rauschenbach, Marvin Darkwah Oppong, Bixia Chen, Annika Herten, Michael Forsting, Ulrich Sure and Philipp Dammann

OBJECTIVE

Treatment indications for patients with brainstem cavernous malformations (BSCMs) remain difficult and controversial. Some authors have tried to establish classification tools to identify eligible candidates for surgery. Authors of this study aimed to validate the performance and replicability of two proposed BSCM grading systems, the Lawton-Garcia (LG) and the Dammann-Sure (DS) systems.

METHODS

For this cross-sectional study, a database was screened for patients with BSCM treated surgically between 2003 and 2019 in the authors’ department. Complete clinical records, preoperative contrast-enhanced MRI, and a postoperative follow-up ≥ 6 months were mandatory for study inclusion. The modified Rankin Scale (mRS) score was determined to quantify neurological function and outcome. Three observers independently determined the LG and the DS score for each patient.

RESULTS

A total of 67 patients met selection criteria. Univariate and multivariate analyses identified multiple bleedings (p = 0.02, OR 5.59), lesion diameter (> 20 mm, p = 0.007, OR 5.43), and patient age (> 50 years, p = 0.019, OR 4.26) as predictors of an unfavorable postoperative functional outcome. Both the LG (AUC = 0.72, p = 0.01) and the DS (AUC = 0.78, p < 0.01) scores were robust tools to estimate patient outcome. Subgroup analyses confirmed this observation for both grading systems (LG: p = 0.005, OR 6; DS: p = 0.026, OR 4.5), but the combined use of the two scales enhanced the test performance significantly (p = 0.001, OR 22.5).

CONCLUSIONS

Currently available classification systems are appropriate tools to estimate the neurological outcome after BSCM surgery. Future studies are needed to design an advanced scoring system, incorporating items from the LG and the DS score systems.

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Philipp Dammann, Karsten Wrede, Yuan Zhu, Toshinori Matsushige, Stefan Maderwald, Lale Umutlu, Harald H. Quick, Ute Hehr, Matthias Rath, Mark E. Ladd, Ute Felbor and Ulrich Sure

OBJECTIVE

Multiple cerebral cavernous malformations (CCMs) are rare lesions that occur in sporadic or familial form. Depending on the disease form, the natural history and treatment of the lesions strongly vary. Molecular analysis of an underlying germline mutation (CCM1–3) is the most sensitive screening method to distinguish between sporadic and familial cases. However, based on the different pathomechanisms that are believed to be involved in either form, significant distinctions in the CCM-associated cerebral venous angioarchitecture should be detectable. This has not been systematically studied.

METHODS

A consecutive series of 28 patients with multiple CCMs (681 total) diagnosed on 1.5-T MRI underwent genetic screening for CCM1–3 mutations and high-resolution susceptibility-weighted imaging (SWI) of the cerebral venous angioarchitecture with 7-T MRI. Imaging data were analyzed to examine the CCM-associated venous angioarchitecture. Results were correlated with findings of molecular analysis for CCM1–3 mutations.

RESULTS

Two different SWI patterns (sporadic and familial) were found. The presence of associated developmental venous anomalies correlated with negative screening for germline mutations (11 sporadic) in all cases. All patients with confirmed familial disease showed normal underlying venous angioarchitecture. Additionally, a very unusual case of a probable somatic mutation is presented.

CONCLUSIONS

The SWI results of the venous angioarchitecture of multiple CCMs correlate with sporadic or familial disease. These results are consistent with the theory that venous anomalies are causative for the sporadic form of multiple CCMs.

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Philipp Dammann, Karsten Wrede, Ramazan Jabbarli, Salome Neuschulte, Katja Menzler, Yuan Zhu, Neriman Özkan, Oliver Müller, Michael Forsting, Felix Rosenow and Ulrich Sure

OBJECTIVE

The aim of this study was to determine seizure outcome, functional outcome, and the withdrawal of antiepileptic drugs (AEDs) after conservative or surgical treatment of patients with new-onset cavernoma-related epilepsy (CRE).

METHODS

The authors conducted a retrospective comparative observational study of 79 consecutive patients, each with a single sporadic cerebral cavernous malformation (CCM) and new-onset CRE.

RESULTS

Forty-one patients underwent initial surgery (IS), and 38 patients underwent initial conservative (IC) treatment. Of those in the latter group, 19 underwent delayed surgical (DS) treatment. At the last follow-up, 88%, 32%, and 79% of patients in the respective groups had been seizure free for at least 2 years (International League Against Epilepsy [ILAE] Class 1; IS vs IC, p < 0.0001) and 78%, 8%, and 58%, respectively, had been off AEDs (IS vs IC, p < 0.0001). The cumulative probability of staying seizure free (ILAE Class 1) during a 5-year period was 73% (mean seizure-free follow-up 49.8 ± 2.7 months, 95% CI 44.4–55.1 months) for the IS group, 22% (mean 31.8 ± 3.6 months, 95% CI 24.8–38.8 months) for the IC group, and 68% (mean 48.6 ± 4.3 months, 95% CI 40.1–57.1 months) for the DS group (IS vs IC p < 0.001). Long-term operative morbidity was 3%, and long-term morbidity in the conservatively treated group was also 3%.

CONCLUSIONS

Patients with CCM and new-onset CRE who underwent IS treatment showed better results in seizure control and the discontinuation of AEDs than the conservatively treated patients. Operative morbidity was comparable to the morbidity from symptomatic CCM hemorrhage in the conservative group. Half of the patients who started with conservative treatment underwent subsequent surgical treatment; however, a longer duration of epilepsy prior to surgery did not worsen postoperative seizure outcome.

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Philipp Dammann, Annika Herten, Alejandro N. Santos, Laurèl Rauschenbach, Bixia Chen, Marvin Darkwah Oppong, Börge Schmidt, Michael Forsting, Christoph Kleinschnitz and Ulrich Sure

OBJECTIVE

The object of this study was to assess outcome after surgery for brainstem cavernous malformations (BSCMs) using functional, health-related quality of life (HRQOL), and psychological surveys to analyze the interrelation of these measurements, and to compare HRQOL and anxiety and depression scores with those in a healthy population.

METHODS

The authors performed a cross-sectional outcome study of all patients surgically treated for BSCM in their department between January 1, 2003, and December 31, 2019. They assessed functional outcome via the modified Rankin Scale (mRS), health-related quality of life (HRQOL) via the SF-36 and 9-item Life Satisfaction Questionnaire (LISAT-9), cranial nerve and brainstem function using a questionnaire, symptom-based psychological outcome via the Hospital Anxiety and Depression Scale (HADS), and timepoint of a return to previous employment. They analyzed the correlation between absolute (mRS score ≤ 2) and relative (postoperative deterioration in initial mRS score) outcome endpoints and the interrelation of the outcome measures and performed a comparison of HRQOL and HADS scores with findings in a healthy population.

RESULTS

Seventy-four patients were eligible for inclusion in the study. HRQOL was impaired after surgery for BSCM compared to that in a healthy population. This impairment was substantial in patients with an unfavorable functional outcome (mRS > 2) but was also present in those with a favorable outcome (mRS ≤ 2) in selected domains. Psychological impairment was negligible in patients with a favorable outcome and grave in those with an unfavorable outcome. LISAT-9 results revealed that brainstem and cranial nerve symptoms reduce satisfaction mainly in self-care abilities for both unfavorable and favorable outcome patients. Among the brainstem and cranial nerve symptoms, balance impairment showed the most significant impact on HRQOL. Absolute outcome endpoints were superior to relative outcome endpoints in reflecting impairment in HRQOL after surgery.

CONCLUSIONS

The study data can improve patient counseling and decision-making in BSCM treatment and may function as a benchmark. The authors report outcomes after BSCM surgery in high detail, emphasizing the specific impact of cranial nerve and brainstem symptoms on HRQOL. When reporting BSCM surgery outcome, absolute outcome endpoints should be applied.