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Accepted Manuscript Intraoperative vascular neuromonitoring in patients with subarachnoid hemorrhage: a pilot study using combined laser-Doppler spectrophotometry Emilija Schmitz, Barbara Bischoff, M.D., Dennis Wolf, M.D., Hubert Schmitt, M.D., Ilker Y. Eyupoglu, M.D., Karl Roessler, M.D., Michael Buchfelder, M.D., Björn Sommer, M.D. PII:

S1878-8750(17)31308-6

DOI:

10.1016/j.wneu.2017.08.011

Reference:

WNEU 6261

To appear in:

World Neurosurgery

Received Date: 1 June 2017 Revised Date:

31 July 2017

Accepted Date: 1 August 2017

Please cite this article as: Schmitz E, Bischoff B, Wolf D, Schmitt H, Eyupoglu IY, Roessler K, Buchfelder M, Sommer B, Intraoperative vascular neuromonitoring in patients with subarachnoid hemorrhage: a pilot study using combined laser-Doppler spectrophotometry, World Neurosurgery (2017), doi: 10.1016/j.wneu.2017.08.011. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

ACCEPTED MANUSCRIPT Schmitz, Bischoff Intraoperative vascular neuromonitoring in patients with subarachnoid hemorrhage: a pilot study using combined laser-Doppler spectrophotometry

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Emilija Schmitz1*, Barbara Bischoff, M.D.1*, Dennis Wolf, M.D.2, Hubert Schmitt, M.D.3, Ilker

*Both authors contribute equally as first authors

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Y. Eyupoglu, M.D.1, Karl Roessler, M.D.1, Michael Buchfelder, M.D.1, Björn Sommer, M.D.1

Department of Neurosurgery, University Hospital Erlangen, Germany

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University Heart Center, Cardiology and Angiology I, Freiburg, Germany

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Department of Anesthesiology, University Hospital Erlangen, Germany

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Department of Neurosurgery, University Hospital Erlangen, Schwabachanlage 6,

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91054 Erlangen, Germany. Email: [email protected], [email protected], [email protected], [email protected],

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[email protected], [email protected] Department of Cardiology and Angiology I, University Heart Center Freiburg, Hugstetter Straße

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55, 79106 Freiburg, Germany. Email: [email protected] Department of Anesthesiology, University Hospital Erlangen, Krankenhausstraße 12, 91054

Erlangen, Germany. Email: [email protected]

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ACCEPTED MANUSCRIPT Schmitz, Bischoff

Short title: Intraoperative non-invasive vascular neuromonitoring

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Corresponding author: Björn Sommer, M.D.

Present address: Department of Neurosurgery, Paracelsus-Klinik Osnabrück, Am Natruper Holz

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69, 49076 Osnabrück, Germany; phone: +49 541 9663861; fax: +49 541 61709

Parts of this work were presented as a poster at the Annual Meeting of the German Society of Clinical Neurophysiology (DGKN) in Tübingen, Germany, on March 19, 2015, and as an electronic poster at the 84th Annual Meeting of the American Association of Neurological

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Surgeons (AANS), Chicago, Illinois, U.S.A., May 1st, 2016.

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Key words: cerebral blood flow, local microcirculation, non-invasive technique, brain ischemia

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ACCEPTED MANUSCRIPT Schmitz, Bischoff ABSTRACT Objective: Intraoperative monitoring of cerebral microcirculation in patients with subarachnoid hemorrhage

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(SAH) may predict the postoperative neurological outcome. In this pilot study, we examined the value of a novel non-invasive real-time measurement technique to detect changes in local microcirculation.

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Methods: We used the laser-Doppler spectrophotometry system „Oxygen-to-see(O2C)“ in 14 patients with SAH Hunt & Hess grade 2 to 5, who underwent microsurgical clipping of cerebral

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aneurysms. A subdural probe recorded capillary venous oxygenation (SO2), relative hemoglobin amount (rHb), blood cell velocity (velo), and blood flow (flow) in 7 mm tissue depth. Data was recorded immediately before dural closure. Additionally, we recorded somatosensory evoked potentials (SEP) with median and tibial nerve stimulation. Results were compared to

months thereafter.

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neurological performance (modified Rankin Scale) at the day of discharge from hospital and 12

Results: Patients´ functional outcome after discharge and 12 months correlated to pathological

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decreased flow and increased SO2 values. In 6 out of 8 patients, microcirculatory monitoring parameters indicated ischemia during surgery as detected by electrophysiological SEP changes

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and infarction in the postoperative CT scan. Pathological SEP results correlated closely with infarct demarcation as seen in CT. Conclusions: Our results indicate the potential benefit of intraoperative combined laser-Doppler flowmetry and spectrophotometry for the prediction of postoperative clinical outcome in this small patient sample. Larger cohort testing is required to verify our findings and show the possible merit of this novel method.

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ACCEPTED MANUSCRIPT Schmitz, Bischoff INTRODUCTION

In neurosurgery, aneurysmatic subarachnoid hemorrhage (SAH) has a high mortality of up to

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30% despite optimal treatment.1,2 The major goal of surgical intervention is to prevent rebleeding, remove spasmogenic SAH, and, rarely, minimize mass effect either from the hemorrhage or directly from the aneurysm sac. However, surgical manipulation itself may cause

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injury of brain tissue, which remains undetectable during the operation. Ideally, brain tissue damage is detected at once to avoid further complications. Non-invasive intraoperative real-time

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monitoring techniques include registration of somatosensory-evoked potentials (SEP), motor evoked potentials (MEP), laser-Doppler flowmetry or laser-speckle imaging (LSI).3-5 These methods either report on functional (SEP, MEP) status or regional cortical blood flow; however, they do not provide information about the metabolism and perfusion/distribution of blood

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volume. We have earlier introduced a combined laser-Doppler flowmetry and tissue spectrophotometry device which is capable of continuous real-time monitoring of local cerebral microcirculation during neurosurgical procedures.7 Here, we tested whether this method can be

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used as a prognostic marker for clinical outcome in patients, who underwent surgery on patients

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suffering from aneurysmal SAH.

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ACCEPTED MANUSCRIPT Schmitz, Bischoff MATERIAL AND METHODS

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Subjects

Patient acquisition of this open, single-center, non-randomized prospective pilot study started in October 2013 at the Department of Neurosurgery, University Hospital Erlangen. The STROBE

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statement was used as a reporting guideline.8 This study complied with the laws of the Federal Republic of Germany and followed the Declaration of Helsinki. It was approved by the Ethical

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Board of the Friedrich-Alexander University of Erlangen-Nuremberg (reference number 4570). In cases where patients were not able to give written informed consent, legal representatives were set in instead.

Inclusion criteria were: a) age 18-85 years, b) subarachnoid hemorrhage due to a cerebral aneurysm of the anterior circulation, c) microsurgical clipping, d) craniotomy size >3 cm in

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diameter, e) no previous brain pathology or brain surgery. Exclusion criteria were a) decompensated renal or liver insufficiency, b) acute coronary syndrome, c) severe comorbidity

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(modified Rankin Scale (mRS) ≥3), d) pregnancy.

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Anesthesiological protocol

Patients were put under general anesthesia according to a standardized protocol. After 3 minutes of preoxygenation, general anesthesia was induced with 1-3 µg/kg fentanyl and 0.5 to 1.8 mg/kg propofol. Tracheal intubation was facilitated by the administration of 0.7 mg/kg rocuronium. Maintenance of anesthesia was performed using sevoflurane (0.3 – 2.4 Vol %). During the operation, additional doses of fentanyl and remifentanil were applied by titration. All patients were artificially ventilated (Cicero EM, Dräger Medical Deutschland GmbH, Lübeck, Germany)

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ACCEPTED MANUSCRIPT Schmitz, Bischoff with oxygen in air. Ventilation was set to maintain an arterial carbon dioxide tension of 35 – 40 mm Hg. Standard monitoring included ECG, pulse oximetry, invasive blood pressure, end-tidal carbon dioxide concentration, and body core temperature. The latter was measured with the urine

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catheter and closely kept at 36 degree Celsius by a Bair Hugger™ (3M, St. Paul, MN, U.S.A.). All anesthesiological data was recorded and processed using NarcoData (V.4.9.4.7917, latest system version update 27.04.2016, IMESO GmbH, Hüttenberg, Germany) and transferred into

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Excel table sheets for further examination (Microsoft Corporation, Redmond, WA, U.S.A.).

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Experimental setup

Surgery

CCT confirmed SAH, and digital subtraction angiography (DSA) was used to identify the

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causative brain aneurysm. Then, the patient was transferred to the operating room. Detailed preparation of the intraoperative setting is given in our previous publication.7 In short, SEPmonitoring and the O2C-device were set up simultaneously to save time. After verification of the

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quality standards of each device, SEP-monitoring started immediately after the patient´s skull was fixed in the Mayfield head clamp. After routine craniotomy and opening of the dura, a

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subdural probe of the O2C system was inserted. Depending on brain swelling and craniotomy size as well as patient´s head positioning and intraoperative recordings, the probe was placed at a location in which it did not interfere with the surgical procedure and recording of stable values was possible. After finding the right position, the probe was fixed with adhesive tape until the closure of the dura for continuous monitoring.

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ACCEPTED MANUSCRIPT Schmitz, Bischoff All patients underwent a routine presurgical protocol including anesthesiological and cardiopulmonary assessment including ECG, blood samples, recording of blood pressure, heart

as an intravenous antibiotic prophylaxis.

Somatosensory potential (SEP) monitoring

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rate, and classification according to the ASA-rating system. Every patient received 2g cefazolin

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After fixing the skull in the Mayfield clamp, we set up the SEP monitoring (Nicolet Endeavor CR or Viking IV-P, Viasis Healthcare, Pennsylvania, U.S.A.) which took between 8 to 10

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minutes. Bilateral median nerve stimulation at the wrist or posterior tibial nerve stimulation at the ankle was applied (intensity 20-25 mA, duration 200 µs, rate 5.1 Hz, Table 1). The nonaffected hemisphere was used as an additional reference for interpretation of pathological SEP parameters. Subdermal recording electrodes were placed on the three scalp sides (C3´, C4´, Cz´)

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according to the international 10-20 system, with a reference electrode at Fz and a ground electrode at the forehead. Settings of the data processing were: bandpass filter 30 to 300 Hz, sensitivity 7 µV, 200 sweep averages. Taking into account the interindividual variability of the

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limb length, the distance from the site of SEP stimulation to the greater tubercule of the humerus or the greater trochanter of the femur was determined. When SEP parameters were stable, we

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started surgery.

Postoperative Course

After surgery, patients were monitored in our ICU. We defined neurological outcome using the modified Rankin Scale (mRS) to assess the clinical status at the time of discharge and 12 months after surgery. Outcome measures also included surgery-related morbidity and mortality. All

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ACCEPTED MANUSCRIPT Schmitz, Bischoff patients were treated in accordance with the clinical routine guidelines of our department, which included vasospasm therapy using hypertensive and hypervolemic therapy as well as administration of intravenous nimodipine when vasospasm was diagnosed intraoperatively or

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due to transcranial Doppler ultrasound or neurological deterioration which led to cerebral angiography over a time span of 14 days.

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Intraoperative vascular neuromonitoring

The techniques of tissue spectrophotometry and laser-Doppler flowmetry are combined in one

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device to assess local capillary-venous microcirculation. The O2C system and the measurement principle have been described in detail previously.7,9,10 In short, the laser-Doppler flowmeter measures relative blood cell velocity (velo) and blood flow (flow) using the Doppler principle and sending light waves of the near-infrared (NIR) spectrum with a wavelength of 830 nm.

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Tissue oxygen saturation (SO2) and relative hemoglobin content (rHb) are measured by the backscattering-spectroscopy system. Since light is absorbed completely if the vessel diameter exceeds 100 µm, these values represent mainly the capillary-venous tissue compartment.11 The

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laser-Doppler flowmeter has a sampling rate of 40 Hz, the spectrophotometer of 2 Hz. The O2C flat probe LFX25 was used in this study. Although this combined optical system has

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been proved to measure reliable and valid parameters under standardized conditions,7 it has not been tested in human brain tissue against absolute, quantitative values. As the absolute quantity of hemoglobin, blood cell velocity and blood flow cannot be determined because the calculation of the scattering coefficient or the phase is not possible, the manufacturer used arbitrary units (AU) to describe the pseudo-quantitative features of these values.

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ACCEPTED MANUSCRIPT Schmitz, Bischoff Intraoperative data acquisition A detailed description of routine setup for using the O2C probe is given in our recent publication.7 In this series, we chose representative data samples immediately after dura opening

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and before closure of the dura. The exact location of the probe depended on the vulnerability of the cortex, the degree of brain swelling, cardiopulmonary status and severity of SAH. In general, the recording site was chosen 1-2 cm away from the Sylvian fissure either on the frontal or

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temporal lobe (Fig. 1). After the initial ambient light correction and visual verification of stable parameters and normal NIR spectrum, continuous real-time monitoring was started after

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approximately 30 seconds. The inbuilt ambient light correction automatically calibrated the spectra according to changes of surrounding light conditions every 5 seconds. Data samples were taken over a time period of 60 seconds immediately after opening of the dura.

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Statistical analysis

For all metric dependent variables we chose median values with one standard deviation (SD) for statistical calculation. Dependent variables of the O2C-system included “SO2”, “rHb”, “velo”

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and “flow”. In our previous study with 20 subjects,7 we calculated the upper and lower limit of normal, baseline values using 2 SD above or below the median value of each variable. In this

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trial, values above or below the previously obtained baseline values (median ± 2SD) were considered as “pathologic”. To measure the impact of anesthesiological parameters, we included bladder temperature, systolic/diastolic blood pressure (BP_sys, BP_dia), mean arterial blood pressure (MAP), heart rate (HR), fraction of inspired oxygen (FiO2), end-tidal partial carbon dioxide pressure (CO2_end), hemoglobin oxygenation saturation (SaO2), standard base excess (SBE), actual base excess (ABE), hemoglobin (Hb), bicarbonate, hematocrit (HCT),

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ACCEPTED MANUSCRIPT Schmitz, Bischoff temperature-corrected partial carbon dioxide and oxygen pressure (pCO2 (T), pO2 (T)), and oxygen content of blood (CaO2) into our descriptive statistics. Furthermore, we calculated Spearman´s rank correlation coefficient (rs) for correlation analysis with O2C parameters.

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Independent variables were dichotomized and included functional outcome (“good” = mRS≤2, “poor” mRS≥3), congruency of CT scan pathology with pathological O2C-result (yes/no), SEP monitoring results congruent with the obtained microcirculatory parameters (yes/no). To identify

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a normal distribution of all metric variables, a Shapiro-Wilk test, histogram, and investigation of kurtosis and skewness was performed. We used a Fisher´s exact test to determine effects of not

reached when the P-value was