Clinical Investigative Study

Arterial Blood Gas Analysis of Samples Directly Obtained BeyondCerebral Arterial Occlusion During Endovascular ProceduresPredicts Clinical Outcome

Alan Flores, MD, Joao Sargento-Freitas, MD, Jorge Pagola, MD, PhD, David Rodriguez-Luna, MD,Socorro Pineiro, MD, Olga Maisterra, MD, Marta Rubiera, MD, PhD, Joan Montaner, MD, PhD,Jose Alvarez-Sabin, MD, PhD, Carlos Molina, MD, PhD, Marc Ribo, MD, PhDFrom the Hospital Vall D’ Hebron, Neurology, Barcelona, Spain (AF, JP, DRL, SP, OM, MR, JM, JAS, CM, MR); Hosp Universitario Coimbra, Neurology, Coimbra, Portugal (JSF).

Keywords: ABG, endovascular, intra-arterial, stroke.

Acceptance: Received June 29, 2011,and in revised form August 12, 2011.Accepted for publication September 16,2011.

Correspondence: Address correspon-dence to Alan Flores, MD, Hospital Vall D’Hebron, Neurology, Passeig Vall DHebron number 119, Barcelona 08032,Spain. Email: alanflo2507@hotmail.com.

Conflict of Interest: None.

J Neuroimaging 2011;XX:1–5.DOI: 10.1111/j.1552-6569.2011.00667.x

A B S T R A C TReal-time intra-procedure information about ischemic brain damage degree may helpphysicians in taking decisions about pursuing or not recanalization efforts.METHODSWe studied gasometric parameters of blood samples drawn through microcatheter in16 stroke patients who received endovascular reperfusion procedures. After crossing theclot with microcatheter, blood sample was obtained from the middle cerebral artery (MCA)segment distal to occlusion (PostOcc); another sample was obtained from carotid artery(PreOcc). An arterial blood gas (ABG) study was immediately performed. We definedclinical improvement as National Institutes of Health Stroke Scale (NIHSS) decreaseof ≥4.RESULTSThe ABG analysis showed differences between PreOcc and PostOcc blood samples in meanoxygen partial pressure (Pre-PaO2: 78.9 ± 16 .3 vs 73.9 ± 14 .9 mmHg; P < .001). Patientswho presented clinical improvement had higher Post-PaO2 (81 ± 11 .4 vs 64.8 ± 14 .4mmHg; P = .025). A receiver-operator characteristic (ROC) curve determined Post-PaO2> 70 mmHg that better predicted further clinical improvement. Patients with Post-PaO2> 70 mmHg had higher chances of clinical improvement (81.8% vs 0%; P = .002) andlower disability (median mRS:3 vs 6; P = .024). In the logistic regression the onlyindependent predictor of clinical improvement was Post-PaO2 > 70 (OR: 5.21 95%CI:1.38-67.24; P = .013).CONCLUSIONDirect local blood sampling from ischemic brain is feasible during endovascular proceduresin acute stroke patients. A gradient in oxygenation parameters was demonstrated betweenpre- and post-occlusion blood samples. ABG information may be used to predict clinicaloutcome and help in decision making in the angio-suite.

IntroductionEndovascular treatment of an acute arterial occlusion is a safeand effective option in the setting of acute stroke and repre-sents a therapeutic alternative when systemic thrombolysis failsto induce recanalization or it is contraindicated.1,2 However,recent studies have shown that the high recanalization ratesachieved are not always paralleled by the expected clinicalrecovery.3

The time window for these procedures is typically set upto 6–8 hours from the symptom onset; however some studiessuggest that in selected patients this time can be successfully ex-tended.4 Before the procedure, multiparametric neuroimagingis done to see if the patients have salvageable persistent ischemicpenumbra, so that they can benefit from the interventional pro-

cedure.5 However definitive evidence about its value for triageis still lacking. Once the procedure is initiated, if recanalizationis not promptly achieved the interventionalist does not haveany source of information to take the decision about whether tocontinue the efforts to recanalize or stop the process. Pursuingrecanalization efforts at any price may lead to futile recanal-ization with no corresponding clinical improvement or, evenworse, to symptomatic hemorrhagic transformation. However,a too early termination of the procedure before recanalization isachieved may keep away from the benefits of reperfusion somepatients with not irreversibly damaged brain tissue.

Microcatheter access to the distal aspect of the clot is usu-ally performed during the procedures either to perform an an-giogram of the distal branches6 or to deploy retrieving devices.7

Copyright ◦C 2011 by the American Society of Neuroimaging 1

Fig 1. The site of pre- and post-occlusion blood sampling. MCA =middle cerebral artery. ICA = internal carotid artery.

Prior studies have shown that it is possible to get beyond the oc-cluding clot and evaluate the distal segment of this.8 Accessingthe arterial lumen beyond the occlusion brings the opportunityto draw blood samples directly from the ischemic core. Theanalysis of this blood may offer intra-procedural informationabout several parameters and biomarkers that could be usedto determine the status of the brain at risk and decide whetherto continue or stop the procedure. We performed a pilot studyconsistent with an immediate arterial blood gas (ABG) analysisof blood samples simultaneously obtained in the arterial seg-ments before and beyond the occluding clot during endovascu-lar procedures and correlated the results with different outcomeparameters.

MethodsConsecutive patients with acute stroke, in anterior circulationstroke syndromes within 8 hours of the time of onset, withangiographically proven distal internal carotid artery (ICA) orproximal middle cerebral artery (MCA) occlusions undergo-ing endovascular procedures, were studied. At patient arrivalto the emergency department a complete evaluation was doneby the neurologist on call, including a ultrasound evaluation(transcranial Doppler [TCD]).9 Early ischemic signs on cranialcomputed tomography (CT) scan were quantified by the Al-berta stroke program early CT score (ASPECTS).10 Eligiblepatients were treated with intravenous tissue plasminogen ac-tivator (tPA) before intra-arterial (IA) procedure. Patients witha persistent arterial occlusion at the end of intravenous (IV)-tPA infusion or with contraindications to receive IV-tPA weretreated with endovascular procedures. When clinical status al-lowed, a conscious sedation protocol avoiding intubation waspreferred. Heparin was administered following femoral arterypuncture as a 2000-3000 units IV bolus. Only patients with an-giographically documented terminal internal carotid artery ormiddle cerebral artery occlusion were included in the study.Typically, once the arterial occlusion was angiographically

Table 1. Measurements Obtained in the Pre- and Post-OcclusionSamples

Pre-occlusion Post-occlusion P value

PH 7.38 ± .07 7.38 ± .7 .386CO2 partial pressure 37.6 ± 10.2 38.6 ± 7.8 .413pO2 partial pressure 78.9 ± 16.3 73.9 ± 14.9 .007HCO3− 22.2 ± 3.5 22.1 ± 3.2 .798O2 saturation 94.3 ± 3.9 93.2 ± 4.4 .003Na+ 137.6 ± 3.9 136.5 ± 6.2 .363K+ 3.6813 ± .7 3.78 ± .6 .465Ca++ 3.9 ± .5 4.1 ± .4 .285Cl− 106.6 ± 4.1 103.8 ± 4.6 .068Anion gap 12.5 ± 2.7 19.8 ± 21.8 .198Glucose (mg/dL) 136.4 ± 29.2 137.2 ± 33 .836

Bold denote statistical significance.

confirmed, a 2.9/2.7-French tapered microcatheter (Progreat;Terumo, Spain) was advanced through the guiding catheterto the proximal aspect of the clot. Then attempts to cross thethrombus with the microcatheter were made. Once the inter-ventionalist considered that the tip of the microcatheter was inthe arterial lumen ahead of the occluding clot, 1 mL of blood(post-occlusion sample: PostOcc) was drawn through the micro-catheter with a 2.5 mL syringe. Then a microcatheter contrastinjection was performed to verify the position of the micro-catheter tip and the patency of the distal arterial branches. Atthis point another 1 mL blood sample from the internal carotidartery was obtained from the guiding catheter (pre-occlusionsample: PreOcc) (Fig 1). Both blood samples were tagged andan immediate ABG analysis was performed (Rapidpoint 400blood gas analyzer; Bayer, Leverkusen, Germany); the mea-sured parameters are shown in Table 1. When blood did notreflow from the microcatheter the interventionalist could ad-vance and reposition the tip of the catheter or exclude thepatient from the study.

Independently of the obtained blood gas results interven-tionalists tried to achieve recanalization with repeated local3–5 mg tPA injections (to a maximum of 20 mg), mechanicalclot disruption with the guidewire and/or the Merci, Solitaire,or Trevo retrievers according to their preferences and patientcharacteristics. The predefined protocol, approved by the lo-cal ethics committee, indicates procedure termination whenrecanalization is achieved or at 6 hours from symptoms onset.Timing of all procedural steps was recorded. Recanalizationwas assessed with the Thrombolysis in Myocardial Infarction(TIMI) grading score11 at the end of the procedure. For anal-ysis purposes we considered successful recanalization a TIMIscore ≥ 2 (eg, TIMI 2 Perfusion with incomplete or slow dis-tal branch filling TIMI 3 Full perfusion with filling of all distalbranches, including the MCA arterial segments M3,412).

Neurological status was assessed by a certified neurologiston patient’s arrival, at 24 hours and at 7 days or discharge usingthe National Institutes of Health Stroke Scale13 (NIHSS). Wedefined clinical improvement as NIHSS decrease ≥4 points atdischarge or at 7 day.

A 24-hour CT scan determined the presence of hemor-rhage, and infarct volume was measured using the ABC/2

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Table 2. Patients Characteristics at Baseline

All patients Post-Occ PaO2 > 70 Post-Occ PaO2 < 70n = 16 n = 11 n = 5 P

Age 77.8 ± 7.6 77.5 ± 8.8 78.6 ± 4.6 .81Gender (female) 7 (43.7%) 7 (63.6%) 0 .07Hypertension 11(68.75) 8(72.2%) 3 (60%) .51Diabetes mellitus 0 0 0Baseline-NIHSS (median-IQR) 19.5(6) 20(3) 16(5)Glucose (mg/dL) 102.7 ± 39.2 103.6 ± 42.4 99 ± 31.1 .89Systolic BP (mmHg) 142.5 ± 26.6 136.6 ± 22.2 162.4 ± 35.5 .15Diastolic BP (mmHg) 73.9 ± 11.1 73 ± 10.9 77 ± 13.7 .61Occluded vessel (ICA/MCA) 3/13 2/10 1/3 .41Good pial collateral (score 1-2) 6/11∗ 3/6 3/5 0,32ASPECTS score 10(1) 10(1.5) 10(.5) .60Time to blood sample (minutes) 233.8 ± 92.3 225.2 ± 107.2 257.5 ± 20.6 .57

NIHSS = National Institutes of Health Stroke Scale; BP = b Blood pressure; ICA = internal carotid artery; IQR = interquartile range; MCA = middle cerebral artery;ASPECTS = Alberta Stroke Program early CT Score.∗Total patient’s with pial collateral measure.

formula.14,15 Symptomatic hemorrhage was defined as CT doc-ument hemorrhage that was temporally related to deteriorationin the patient’s clinical condition in the judgment of the clini-cal investigator.16 Modified Rankin scale17 was used to assessclinical outcome at 90 days. We defined clinical good outcomeas mRS between 0 and 2. The baseline clinical characteristicswere collected prospectively.

Statistical Analysis

Descriptive and frequency statistical analyses were obtainedand comparisons were made using the SPSS 15.0 statisticalpackage (SPSS, Inc., Chicago, IL). Statistical significance forintergroup differences was assessed by the Pearson χ2 or theFisher exact test for categorical variables, and the Student’s t testand ANOVA for continuous variables. To assess differences inblood gas between pre- and post-occlusion samples a paired-samples t test was performed.

Pearson correlation coefficient was used to determine cor-relations between blood gases and other continuous variables.When indicated, Mann-Whitney U and Spearman tests wereused. To calculate the sensitivity and specificity of biomarkersto predict clinical improvement, a receiver-operator character-istic (ROC) curve was configured. A logistic regression analysiswas performed to determine factors that could be consideredindependent predictors of favorable outcome. P < .05 was con-sidered statistically significant.

ResultsA total of 16 patients were included in this pilot study, meanage 78.5 ± 7 .5 years, median NIHSS 20 (interquartile range IR:16-21). Six (37.5%) patients received IV-tPA treatment beforeendovascular procedure. The median pre-IA procedure AS-PECTS score was 10 (IR: 9-10). Other baseline parameters areshown in Table 2. The mean time from symptom onset to groinpuncture was 209 ± 135 minutes. On the initial angiogram 12(75%) patients had a middle cerebral artery occlusion and 4(25%) a terminal internal carotid artery occlusion. The meantime from symptom onset to blood sampling was 233 ± 92minutes. Recanalization was achieved in 11 patients (68.9%:

TIMI 2a 18.8%, TIMI 2b 18.8%, TIMI3 31.3%), and meantime to recanalization was 322 ± 169 minutes. The mean in-farct volume on the 24 hours follow-up CT scan was 164 ± 169cc; 1 patient (6.3%) had a symptomatic hemorrhagic transfor-mation. At discharge/7 days the median NIHSS was 16 (IR:4-30), and 9 patients (56.3%) presented a clinical improvement.At three months median mRS was 4 (IR: 1-6) and 31.2% hadmRS ≤ 1.

The ABG analysis showed differences between PreOcc andPostOcc blood samples in mean oxygen partial pressure (Pre-PaO2 78.9 ± 16 .3 vs Post-PaO2 73.9 ± 14 .9; P < .001) andmean oxygen saturation (Pre-Sat O2 9 4.3 ± 3 .9% vs Post-SatO2 93.2 ± 4 .4%; P < .001). The other measured parametersdid not show statistically significant differences between PreOccand PostOcc samples (Table 1).

Neither Post-PaO2 (r =− .16; P = .68) nor Post-SatO2(r =− .08; P = .75) were correlated with the elapsed time fromsymptom onset to blood sampling. The ASPECT score on thepre-procedure CT-scan was correlated neither to Post-PaO2(r =− .1; P = .73) nor to Post-Sat O2 (r =− .09; P = .75). Con-versely, the final infarct volume was correlated with Post-PaO2(r =− .62, P = .019) and Post-SatO2 (r = − .69, P = .006) butnot with time to recanalization (r =− 1.17; P = .61).

We did not find a correlation between the presence of GoodPial Collateral and the Post-PaO2 (P = .97).

Patients who presented a neurological improvement had ahigher Post-PaO2 (81 ± 11 .4 vs 64.8 ± 14 .4 mmHg; P =.025) and a higher Post-SatO2 (95.5% vs 90.2%; P = .01).A receiver operating characteristic curve determined the cutpoints: Post-PaO2 > 70 mmHg and Post-Sat O2 > 92% thatbetter predicted further clinical improvement (100% sensitiv-ity, 71% specificity). Patients with Post-PaO2 > 70 mmHg orPost-SatO2 > 92% had higher chances of clinical improve-ment (81.8% vs 0%; P = .002), lower infarct volumes (66cc vs340.5; P = .003) and lower disability at 3 months (median mRS3 vs 6; P = .024) (Fig 2). Among patients with Post-PaO2 >

70 mmHg, if recanalization was achieved, 87.5% achieveda clinical improvement. The patient who presented a symp-tomatic intracranial hemorrhagic (SICH) presented a Post-PaO2 of 54.6 mmHg and a Post-SatO2 of 88.9%.

Flores et al: ABG in Blood Samples Beyond the Occlusion 3

Fig 2. Differences in different outcomes according to post-occlusion oxygen partial pressure. NIHSS = National Institutes of Health StrokeScale. ∗P < .05.

Among all baseline variables only Post-PaO2 > 70 (P < .01),Post-Sat92 > 92 (P < .01), and the presence of an MCA occlu-sion (as compared to terminal ICA; P = .01) were associatedwith clinical improvement. In the logistic regression model af-ter adjusting by age and admission NIHSS, Post-PaO2 > 70emerged as the only independent predictor of clinical improve-ment (OR: 5.21 95% CI:1.38-67.24; P = .013).

No complication related blood sampling was observed.

DiscussionOur study shows that microcatheter-driven analysis of bloodsamples obtained beyond the arterial occlusion during en-dovascular recanalization procedures in acute stroke patientsis safe and feasible. Moreover, the immediate gasometric anal-ysis shows significant differences in oxygen-related parametersbetween pre- and post-occlusion blood samples. The identifica-tion of this gradient in blood oxygen supports the theory thatthe obtained measures reflect the degree of hypoperfusion ormisery perfusion beyond the occluding clot.

The expected correlations between “post-occlusion oxy-genation status” and the total time of ischemia or the collateralflow state could not be confirmed in this study. A possible expla-nation would be that collateral circulation was not consistentlystudied in all patients and also the differences in tolerance ormetabolism in ischemic conditions between patients.

To date, the best noninvasive method to map and quantifythe oxygen extraction fraction (OEF) in the ischemic brain tis-sue has been positron emission tomography (PET), which is notreadily accessible in clinical routine. PET studies have shownthat within the penumbra the OEF increases from about 40%

under normal conditions to about 90% during hypoperfusion.However, during brain ischemia, the OEF measured by PETdid not prove to be a reliable predictor of tissue viability.18 TheABG analysis of blood samples obtained in the ischemic arearepresents in fact an invasive method to determine oxygen-related parameters at the lesion site. In our study, a high oxy-gen concentration determined as a partial oxygen pressure >

70 mmHg emerged as a powerful predictor of further in-hospitalclinical improvement, being also associated with a smaller finalinfarct volume, clinical improvement, and a significant lowerNIHSS at discharge.

If these results are confirmed this method could help thetreating physicians in taking decisions in the angio-suite duringintra-arterial treatments. In the acute management of stroke sev-eral approaches have been studied to determine the presenceof savable ischemic brain tissue in order to select the best can-didates to receive revascularization treatments. Particularly CTor MRI multiparametric neuroimaging are being widely usedfor this purpose.19,20 However once the decision to perform anendovascular procedure is made if recanalization is not rapidlyachieved the interventionalists have little data about whetherit is safe and effective to pursue the recanalization efforts. Thislack of information may lead to a too early procedure termina-tion before recanalization is achieved avoiding clinical recoveryin some cases or to futile efforts challenging the patient’s safetyand unnecessarily increasing the costs in others. Previous stud-ies have pointed the detection of a good angiographic collateralflow as a possible marker of good outcome.21,22 Scales quantify-ing this collateral flow have been created,22,23 however their useas decision making tools still needs to be validated. Our studyshows a novel approach to determine the degree of ischemia

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in the brain at risk during the intra-arterial procedure. Thefeasibility of accessing with the microcatheter the arterial seg-ment beyond the occlusion to inject either contrast agents6 oroxygenated blood24 has been previously described. Our studydemonstrates now that once the microcatheter reaches the distalaspect of the clot it can also be used to obtain blood samples thatcan be analyzed in a few minutes offering valuable information.

Our study confirms the possibility to obtain and investigateblood biomarkers beyond the arterial occlusion. We chose tomeasure ABG parameters because determination can be imme-diately done. However, this novel approach opens the door tofuture investigations of different biomarkers that can be mea-sured in these blood samples directly obtained at the core of theischemic tissue. In the future, a combination of angiographicand biochemical parameters may be extremely useful in de-cision making in the angio-suite especially when consideringexpanding the therapeutic window.

A postOcc blood sample could not be obtained in all thepatients. This could be due to the clot burden, composition, orextent in some cases or to excessive vessel tortuosity in othercases.

ConclusionDirect local blood sampling from ischemic brain is feasible dur-ing endovascular procedures in acute stroke patients. A gradientin oxygenation parameters was demonstrated between pre- andpost-occlusion blood samples. ABG information may be usedto predict clinical outcome and help in decision making in theangio-suite.

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