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Endoscope-assisted fluorescence-guided resection allowing supratotal removal in glioblastoma surgery

Christoph Bettag, Katharina Schregel, Philip Langer, Carolina Thomas, Daniel Behme, Christine Stadelmann, Veit Rohde, and Dorothee Mielke

OBJECTIVE

Several studies have proven the benefits of a wide extent of resection (EOR) of contrast-enhancing tumor in terms of progression-free survival (PFS) and overall survival (OS) in patients with glioblastoma (GBM). Thus, gross-total resection (GTR) is the main surgical goal in noneloquently located GBMs. Complete tumor removal can be almost doubled by microscopic fluorescence guidance. Recently, a study has shown that an endoscope with a light source capable of inducing fluorescence allows visualization of remnant fluorescent tumor tissue even after complete microscopic fluorescence-guided (FG) resection, thereby increasing the rate of GTR. Since tumor infiltration spreads beyond the borders of contrast enhancement on MRI, the aim of this study was to determine via volumetric analyses of the EOR whether endoscope-assisted FG resection enables supratotal resection beyond the borders of contrast enhancement.

METHODS

The authors conducted a retrospective single-center analysis of a consecutive series of patients with primary GBM presumed to be noneloquently located and routinely operated on at their institution between January 2015 and February 2018 using a combined microscopic and endoscopic FG resection. A 20-mg/kg dose of 5-aminolevulinic acid (5-ALA) was administered 4 hours before surgery. After complete microscopic FG resection, the resection cavity was scanned using the endoscope. Detected residual fluorescent tissue was resected and embedded separately for histopathological examination. Nonenhanced and contrast-enhanced 3D T1-weighted MR images acquired before and within 48 hours after tumor resection were analyzed using 3D Slicer. Bias field–corrected data were used to segment brain parenchyma, contrast-enhancing tumor, and the resection cavity for volume definition. The difference between the pre- and postoperative brain parenchyma volume was considered to be equivalent to the resected nonenhancing but fluorescent tumor tissue. The volume of resected tumor tissue was calculated from the sum of resected contrast-enhancing tumor tissue and resected nonenhancing tumor tissue.

RESULTS

Twelve patients with GBM were operated on using endoscopic after complete microscopic FG resection. In all cases, residual fluorescent tissue not visualized with the microscope was detected. Histopathological examination confirmed residual tumor tissue in all specimens. The mean preoperative volume of brain parenchyma without contrast-enhancing tumor was 1213.2 cm3. The mean postoperative volume of brain parenchyma without the resection cavity was 1151.2 cm3, accounting for a mean volume of nonenhancing but fluorescent tumor tissue of 62.0 cm3. The mean relative rate of the overall resected volume compared to the contrast-enhancing tumor volume was 244.7% (p < 0.001).

CONCLUSIONS

Combined microscopic and endoscopic FG resection of GBM significantly increases the EOR and allows the surgeon to achieve a supratotal resection beyond the borders of contrast enhancement in noneloquently located GBM.

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Addition of intravenous N-methyl-D-aspartate receptor antagonists to local fibrinolytic therapy for the optimal treatment of experimental intracerebral hemorrhages

Ruth Thiex, Joachim Weis, Timo Krings, Sonia Barreiro, Funda Yakisikli-Alemi, Joachim M. Gilsbach, and Veit Rohde

Object

Fibrinolytic therapy with recombinant tissue plasminogen activator (rtPA) is considered a treatment option in patients with deep-seated intracerebral hemorrhage (ICH). Nevertheless, the results of animal experiments have shown that tPA exerts pleiotropic actions in the brain, including regulation of vasoactivity, amplification of calcium conductance by cleavage of the N-methyl-D-aspartate (NMDA) receptor subunit, and activation of metalloproteinases, which increase excitotoxicity, damage the blood–brain barrier, and worsen edema. The authors investigated whether the noncompetitive NMDA receptor antagonist MK801 can be used as an adjuvant therapy in combination with rtPA to attenuate the unfavorable delayed edema formation and inflammation observed following rtPA therapy in an experimental porcine model of ICH.

Methods

Twenty pigs were used in this study; MK801 (0.3 mg/kg) was administered to each pig intravenously immediately after hematoma induction and on the 1st and 3rd day after hematoma induction. Ten of the 20 pigs were randomly assigned to fibrinolytic therapy with rtPA (MK801–tPA group), whereas in the remaining 10 control animals (MK801 group) the hematomas were allowed to follow their natural courses of resorption. The extent of edema formation was evaluated using magnetic resonance (MR) imaging volumetry on Days 0, 4, and 10 after hematoma induction and was compared with histopathological changes found at necropsy. The mean edema volumes in these two groups were also compared with that in the group of nine pigs examined in a preceding experimental series, in which the animals’ hematomas were only treated with rtPA (tPA group).

In the 10 animals in the MK801–tPA group, the mean perihematoma edema volume on MR images had not significantly increased by Day 4 (p < 0.08) or Day 10 (p < 0.35) after hematoma induction. In the 10 animals in the MK801 group, the increase in mean perifocal edema size was significant after 4 days (p < 0.001) and nonsignificant after 10 days (p < 0.09). In the nine animals in the tPA group, the mean edema volume significantly increased by Days 4 (p < 0.002) and 10 (p < 0.03).

Conclusions

As suggested by the reduction in delayed edema volume and the inflammatory response, MK801 modifies the neurotoxic properties of rtPA but not those of blood degradation products. Possibly, fibrinolytic therapy of ICH is more beneficial if combined with agents such as MK801.

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Do we underdiagnose osteoporosis in patients with pyogenic spondylodiscitis?

Christoph Bettag, Tammam Abboud, Christian von der Brelie, Patrick Melich, Veit Rohde, and Bawarjan Schatlo

OBJECTIVE

Pyogenic spondylodiscitis affects a fragile patient population. Surgical treatment in cases of instability entails instrumentation, and loosening of this instrumentation is a frequent occurrence in pyogenic spondylodiscitis. The authors therefore attempted to investigate whether low bone mineral density (BMD)—which is compatible with the diagnosis of osteoporosis—is underdiagnosed in patients with pyogenic spondylodiscitis. How osteoporosis was treated and how it affected implant stability were further analyzed.

METHODS

Charts of patients who underwent operations for pyogenic spondylodiscitis were retrospectively reviewed for clinical data, prior medical history of osteoporosis, and preoperative CT scans of the thoracolumbar spine. In accordance with a previously validated high-fidelity opportunistic CT assessment, average Hounsfield units (HUs) in vertebral bodies of L1 and L4 were measured. Based on the validation study, the authors opted for a conservative cutoff value for low BMD, being compatible with osteoporosis ≤ 110 HUs. Baseline and outcome variables, including implant failure and osteoporosis interventions, were entered into a multivariate logistic model for statistical analysis.

RESULTS

Of 200 consecutive patients who underwent fusion surgery for pyogenic spondylodiscitis, 64% (n = 127) were male and 66% (n = 132) were older than 65 years. Seven percent (n = 14) had previously been diagnosed with osteoporosis. The attenuation analysis revealed HU values compatible with osteoporosis in 48% (95/200). The need for subsequent revision surgery due to implant failure showed a trend toward an association with estimated low BMD (OR 2.11, 95% CI 0.95–4.68, p = 0.067). Estimated low BMD was associated with subsequent implant loosening (p < 0.001). Only 5% of the patients with estimated low BMD received a diagnosis and pharmacological treatment of osteoporosis within 1 year after spinal instrumentation.

CONCLUSIONS

Relying on past medical history of osteoporosis is insufficient in the management of patients with pyogenic spondylodiscitis. This is the first study to identify a substantially missed opportunity to detect osteoporosis and to start pharmacological treatment after surgery for prevention of implant failure. The authors advocate for routine opportunistic CT evaluation for a better estimation of bone quality to initiate diagnosis and treatment for osteoporosis in these patients.

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The impact of temporary clipping during aneurysm surgery on the incidence of delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage

Vesna Malinova, Bawarjan Schatlo, Martin Voit, Patricia Suntheim, Veit Rohde, and Dorothee Mielke

OBJECTIVE

Clipping of a ruptured intracranial aneurysm requires some degree of vessel manipulation, which in turn is believed to contribute to vasoconstriction. One of the techniques used during surgery is temporary clipping of the parent vessel. Temporary clipping may either be mandatory in cases of premature rupture (rescue) or represent a precautionary or facilitating surgical step (elective). The aim of this study was to study the association between temporary clipping during aneurysm surgery and the incidence of vasospasm and delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage (aSAH) in a large clinical series.

METHODS

Seven hundred seventy-eight patients who underwent surgical aneurysm treatment after aSAH were retrospectively included in the study. In addition to surgical parameters, the authors recorded transcranial Doppler (TCD) sonography–documented vasospasm (TCD-vasospasm, blood flow acceleration > 120 cm/sec), delayed ischemic neurological deficits (DINDs), and delayed cerebral infarction (DCI). Multivariate binary logistic regression analysis was applied to assess the association between temporary clipping, vasospasm, DIND, and DCI.

RESULTS

Temporary clipping was performed in 338 (43.4%) of 778 patients during aneurysm surgery. TCD sonographic flow acceleration developed in 370 (47.6%), DINDs in 123 (15.8%), and DCI in 97 (12.5%). Patients with temporary clipping showed no significant increase in the incidence of TCD-vasospasm compared with patients without temporary clipping (49% vs 48%, respectively; p = 0.60). DINDs developed in 12% of patients with temporary clipping and 18% of those without temporary clipping (p = 0.01). DCI occurred in 9% of patients with temporary clipping and 15% of those without temporary clipping (p = 0.02). The need for rescue temporary clipping was a predictor for DCI; 19.5% of patients in the rescue temporary clipping group but only 11.3% in the elective temporary clipping group had infarcts (p = 0.02). Elective temporary clipping was not associated with TCD-vasospasm (p = 0.31), DIND (p = 0.18), or DCI (p = 0.06).

CONCLUSIONS

Temporary clipping did not contribute to a higher rate of TCD-vasospasm, DIND, or DCI in comparison with rates in patients without temporary clipping. In contrast, there was an association between temporary clipping and a lower incidence of DINDs and DCI. There is no reason to be hesitant in using elective temporary clipping if deemed appropriate.

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Assessment of tissue permeability by early CT perfusion as a surrogate parameter for early brain injury after subarachnoid hemorrhage

Vesna Malinova, Bogdan Iliev, Ioannis Tsogkas, Veit Rohde, Marios-Nikos Psychogios, and Dorothee Mielke

OBJECTIVE

The severity of early brain injury (EBI) after aneurysmal subarachnoid hemorrhage (aSAH) correlates with delayed cerebral ischemia (DCI) and outcome. A disruption of the blood-brain barrier is part of EBI pathophysiology. The aim of this study was to assess tissue permeability (PMB) by CT perfusion (CTP) in the acute phase after aSAH and its impact on DCI and outcome.

METHODS

CTP was performed on day 3 after aSAH. Qualitative and quantitative analyses of all CTP parameters, including PMB, were performed. The areas with increased PMB were documented. The value of an early PMB increase as a predictor of DCI and outcome according to the modified Rankin Scale (mRS) grade 3 to 24 months after aSAH was assessed. Possible associations of increased PMB with the Subarachnoid Hemorrhage Early Brain Edema Score (SEBES) and with early perfusion deficits, as radiographic EBI markers, were evaluated.

RESULTS

A total of 69 patients were enrolled in the study. An increased PMB on early CTP was detected in 10.1% (7/69) of all patients. A favorable outcome (mRS grade ≤ 2) occurred in 40.6% (28/69) of all patients. DCI was detected in 25% (17/69) of all patients. An increased PMB was a predictor of DCI (logistic regression, p = 0.03) but not of outcome (logistic regression, p = 0.40). The detection of increased PMB predicted DCI with a sensitivity of 25%, a specificity of 94%, a positive predictive value of 57%, and a negative predictive value of 79% (chi-square test p = 0.03). Early perfusion deficits were seen in 68.1% (47/69) of the patients, a finding that correlated with DCI (p = 0.005) but not with the outcome. No correlation was found between the SEBES and increased PMB.

CONCLUSIONS

Changes in PMB can be detected by early CTP after aSAH, which correlates with DCI. Future studies are needed to evaluate the time course of PMB changes and their interaction with therapeutic measures.

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Endoscope-assisted visualization of 5-aminolevulinic acid fluorescence in surgery for brain metastases

Christoph Bettag, Abdelhalim Hussein, Bawarjan Schatlo, Alonso Barrantes-Freer, Tammam Abboud, Veit Rohde, and Dorothee Mielke

OBJECTIVE

Fluorescence-guided resection of cerebral metastases has been proposed as an approach to visualize residual tumor tissue and maximize the extent of resection. Critics have argued that tumor cells at the resection margins might be overlooked under microscopic visualization because of technical limitations. Therefore, an endoscope, which is capable of inducing fluorescence, has been applied with the aim of improving exposure of fluorescent tumor tissue. In this retrospective analysis, authors assessed the utility of endoscope assistance in 5-aminolevulinic acid (5-ALA) fluorescence–guided resection of brain metastases.

METHODS

Between June 2013 and December 2016, a standard 20-mg/kg dose of 5-ALA was administered 4 hours prior to surgery in 26 patients with suspected single brain metastases. After standard neuronavigated microsurgical tumor resection, a microscope capable of inducing fluorescence was used to examine tumor margins. The authors classified the remaining fluorescence into 3 grades (0 = none, 1 = weak, and 2 = strong). Endoscopic assistance was employed if no or only weak fluorescence was visualized at the resection margins under the microscope. Endoscopically identified fluorescent tissue at the margins was resected and evaluated separately via histological examination to prove or disprove tumor infiltration.

RESULTS

Under the microscope, weakly fluorescent tissue was seen at the margins of the resection cavity in 15/26 (57.7%) patients. In contrast, endoscopic inspection revealed strongly fluorescent tissue in 22/26 (84.6%) metastases. In 11/26 (42.3%) metastases no fluorescence at the tumor margins was detected by the microscope; however, strong fluorescence was visualized under the endoscope in 7 (63.6%) of these 11 metastases. In the 15 metastases with microscopically weak fluorescence, strong fluorescence was seen when using the endoscope. Neither microscopic nor endoscopic fluorescence was found in 4/26 (15.4%) cases. In the 26 patients, 96 histological specimens were obtained from the margins of the resection cavity. Findings from these specimens were in conjunction with the histopathological findings, allowing identification of metastatic infiltration with a sensitivity of 95.5% and a specificity of 75% using endoscope assistance.

CONCLUSIONS

Fluorescence-guided endoscope assistance may overcome the technical limitations of the conventional microscopic exposure of 5-ALA–fluorescent metastases and thereby increase visualization of fluorescent tumor tissue at the margins of the resection cavity with high sensitivity and acceptable specificity.

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Early whole-brain CT perfusion for detection of patients at risk for delayed cerebral ischemia after subarachnoid hemorrhage

Vesna Malinova, Karoline Dolatowski, Peter Schramm, Onnen Moerer, Veit Rohde, and Dorothee Mielke

OBJECT

This prospective study investigated the role of whole-brain CT perfusion (CTP) studies in the identification of patients at risk for delayed ischemic neurological deficits (DIND) and of tissue at risk for delayed cerebral infarction (DCI).

METHODS

Forty-three patients with aneurysmal subarachnoid hemorrhage (aSAH) were included in this study. A CTP study was routinely performed in the early phase (Day 3). The CTP study was repeated in cases of transcranial Doppler sonography (TCD)–measured blood flow velocity (BFV) increase of > 50 cm/sec within 24 hours and/or on Day 7 in patients who were intubated/sedated.

RESULTS

Early CTP studies revealed perfusion deficits in 14 patients, of whom 10 patients (72%) developed DIND, and 6 of these 10 patients (60%) had DCI. Three of the 14 patients (21%) with early perfusion deficits developed DCI without having had DIND, and the remaining patient (7%) had neither DIND nor DCI. There was a statistically significant correlation between early perfusion deficits and occurrence of DIND and DCI (p < 0.0001). A repeated CTP was performed in 8 patients with a TCD–measured BFV increase > 50 cm/sec within 24 hours, revealing a perfusion deficit in 3 of them (38%). Two of the 3 patients (67%) developed DCI without preceding DIND and 1 patient (33%) had DIND without DCI. In 4 of the 7 patients (57%) who were sedated and/or comatose, additional CTP studies on Day 7 showed perfusion deficits. All 4 patients developed DCI.

CONCLUSIONS

Whole-brain CTP on Day 3 after aSAH allows early and reliable identification of patients at risk for DIND and tissue at risk for DCI. Additional CTP investigations, guided by TCD–measured BFV increase or persisting coma, do not contribute to information gain.

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Intracerebral Hematoma Lysis

Veit Rohde and Uzma Samadani

Object

Currently no adequate surgical treatment exists for spontaneous intracerebral hemorrhage (ICH). Implantable polymers can be used effectively to deliver therapeutic agents to the local site of the pathological process, thus reducing adverse systemic effects. The authors report the use of stereotactically implanted polymers loaded with tissue plasminogen activator (tPA) to induce lysis of ICH in a rabbit model.

Methods

Ethylene vinyl acetate (EVAc) polymers were loaded with bovine serum albumin (BSA) only or with BSA plus tPA. In vitro pharmacokinetic (three polymers) and thrombolysis (12 polymers) studies were performed. For the in vivo study, 12 rabbits were fixed in a stereotactic frame, and 0.2 ml of clotted autologous blood was injected into the right frontal lobe parenchyma. After 20 minutes, control BSA polymers were stereotactically implanted at the hemorrhage site in six rabbits, and experimental BSA plus tPA polymers were implanted in six rabbits. Animals were killed at 3 days, and blood clot volume was assessed.

The pharmacokinetic study showed release of 146 ng of tPA over 3 days. The tPA activity correlated with in vitro thrombolysis. In the in vivo study, the six animals treated with tPA polymers had a mean (±standard error of the mean [SEM]) thrombus volume of 1.43 ±0.29 mm3 at 3 days, whereas the six animals treated with blank (BSA-only) polymers had a mean (±SEM) thrombus volume of 19.99 ±3.74 mm3 (p <0.001).

Conclusions

Ethylene vinyl acetate polymers release tPA over the course of 3 days. Stereotactic implantation of tPA-loaded EVAc polymers significantly reduced ICH volume. Polymers loaded with tPA may be useful clinically for lysis of ICH without the side effects of systemic administration of tPA.

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Spontaneous adrenal hemorrhage: a little-known complication of intracranial tumor surgery

Case report

Angelika Gutenberg, Bettina Lange, Bastian Gunawan, Joerg Larsen, Wolfgang Brück, Veit Rohde, and Raphaela Verheggen

✓ Nontraumatic adrenal hemorrhage in adults is uncommon and unexpected in the context of intracranial surgery. The authors report on a patient in whom hemodynamically relevant retroperitoneal bleeding developed within hours after an otherwise uneventful operation for a falcine meningioma. In this brief report they seek to draw attention to this rare but life-threatening complication, because rapid diagnosis can be life-saving.

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Intraosseous ultrasonography to determine the accuracy of drill hole positioning prior to the placement of pedicle screws: an experimental study

Laboratory investigation

Sven Rainer Kantelhardt, Jörg Larsen, Volker Bockermann, Wolfgang Schillinger, Alf Giese, and Veit Rohde

Object

Dorsal fixation with rods and pedicle screws (PSs) is the most frequently used surgery to correct traumatic and degenerative instabilities of the human spine. Prior to screw placement, screw holes are drilled along the vertebral pedicles. Despite the use of a variety of techniques, misplacement of screw holes, and consequently of the PSs, is a common problem. The authors investigated the usefulness of an intraspinal, intraosseous ultrasonography technique to determine the accuracy of drill hole positioning.

Methods

An endovascular ultrasound transducer was used for the intraluminal scanning of bore holes in trabecular bovine bone, 12 pedicle drill holes in cadaveric human spine, and 4 pedicle drill holes in a patient undergoing thoracic spondylodesis. Seven of the experimental bore holes in the cadaveric spine were placed optimally (that is, inside the pedicle) and 5 were placed suboptimally (breaching the medial or lateral cortical surface of the pedicle). Computed tomography scans were obtained in the patient and cadaveric specimen after the procedure.

Results

The image quality achieved in examinations of native bovine bone tissue, the formalin-fixed human spine specimen, and human vertebrae in vivo was equal. The authors endosonographically identified correct intrapedicular and intravertebral positions as well as poor (cortex breached) placement of drill holes.

Conclusions

Intraosseous ultrasonography is a promising technique for the investigation of PS holes prior to screw implantation, and may add to the safety of PS placement.