Could emergency admission plasma D-dimer level predict first pass effect of stent retriever thrombectomy in acute ischemic stroke?

Abstract

Background

Evidence on plasma biomarkers to identify first pass effect (FPE) in patients with acute ischemic stroke (AIS) with large vessel occlusion (LVO) treated with thrombectomy is limited.

Purpose

To evaluate whether plasma D-dimer could predict FPE.

Material and Methods

Consecutive patients with LVO who underwent first-line stent retriever thrombectomy at our center between January 2018 and August 2021 were enrolled. Patients were classified into the FPE (modified Thrombolysis in Cerebral Infarction [mTICI] ≥2c) group or non-FPE (mTICI 0–2b) group based on angiographic outcomes. Logistic regression analysis was performed to determine the predictors of FPE. The overall ability of D-dimer levels in predicting FPE was evaluated using receiver operating characteristic (ROC) curves.

Results

In total, 313 patients were included; 88 (28.1%) patients achieved FPE. Compared to those with non-FPE, patients with FPE had more diabetes mellitus history, lower D-dimer levels, higher clot burden score, a higher proportion of M1 middle cerebral artery, and a higher proportion of main stem occlusion pattern (P <0.05). After adjusting for potential variables, D-dimer levels (OR=0.81, 95% CI=0.52–0.96), clot burden score (OR=1.76, 95% CI=1.38–2.87), and main stem occlusion pattern (OR=1.85, 95% CI=1.19–2.62) remained independently associated with FPE. Based on the ROC analysis, the D-dimer as a predictor for predicting FPE presented with a specificity of 79%, a negative predictive value of 87%, and an area under the curve of 0.761.

Conclusion

Low emergency admission plasma D-dimer level is an independent predictor of FPE in patients with AIS treated with stent retriever thrombectomy.

Keywords

Stroke thrombectomy predict D-dimer outcome

Introduction

Strong evidence-based clinical trials demonstrated that endovascular thrombectomy with retrievable stents as a first-line technique has proven to be safe and effective for patients with acute ischemic stroke (AIS) with large vessel occlusion (LVO) in the anterior circulation (1,2). This thrombectomy allows multiple pass/retrieve attempts through the thrombus to achieve successful recanalization and improve clinical outcomes. First pass effect (FPE), which is defined as achieving satisfied reperfusion in a single attempt, has recently emerged as a key indicator of thrombectomy efficacy (3). Significant improvements in clinical outcomes and reductions in procedural complications have been reported in patients who have achieved FPE (4). Hence, the early identification of the predictors for FPE in clinical practice is critical to continuously improve the efficacy of this therapeutic strategy.

The aim of the present study was to investigate the association between admission plasma D-dimer levels and FPE in a single comprehensive center cohort of patients with AIS.

Material and Methods

The study protocol followed the guidelines of the World Medical Association Declaration of Helsinki and was approved by the ethics committee of our institution (ethical review no. 2021-NT-28). The requirement for informed consent was waived by the ethics committee due to the retrospective nature of the study.

Study population

Datasets of consecutive patients treated with EVT between February 2018 and August 2021 at a single stroke center were obtained from the clinical database. The patients who met the following inclusion criteria were enrolled: (i) patients diagnosed with AIS due to LVO in anterior circulation. To keep the homogeneity of the enrolled patients, we limited our study to patients with LVO in anterior circulation, including intracranial internal carotid artery occlusion (ICA) or proximal middle cerebral artery occlusion (M1 MCA) based on preoperative computed tomography (CT) angiography; (ii) age ≥18 years; (iii) EVT could be administered within 6 h after symptom onset or within 6–24 h after the onset of symptoms with the presence of large ischemic mismatch/penumbra according to CT perfusion (2); (iv) a retrievable stent was used as the primary device for endovascular thrombectomy. The exclusion criteria were as follows: (i) pre-stroke modified Rankin Scale (mRS) score >2; (ii) patients who did not undergo blood sampling for D-dimer measurement on admission; (iii) patients who received intravenous thrombolysis (IVT) before admission; (iv) patients with co-morbidities that may impact plasma D-dimer levels, such as deep vein thrombosis, pulmonary embolism, malignancy, and acute myocardial infarction; and (v) no follow-up neuroimaging available for HT evaluation. Recorded data included demographic characteristics, epidemiological data, radiologic information, procedural parameters, and follow-up neuroimaging outcomes.

D-dimer measurement

D-dimer levels included in coagulation function were tested, as part of a routine laboratory testing program for all patients presenting with suspected stroke symptoms, immediately after admission. The peripheral venous blood sample was obtained from each patient into tubes harboring sodium citrate used as the anticoagulant. Plasma was separated by centrifuging the blood samples at 3000 r/min for 10 min. D-dimer levels were measured by an automated biochemical detector using a kit and immunoturbidimetry (Leadman Biochemical Co., Ltd, Beijing, China). The D-dimer levels became available within 30 min after blood sampling.

Endovascular thrombectomy

Interventional procedures were performed under local anesthesia or conscious sedation. The first-line stent retriever thrombectomy was implemented in the standard manner. An 8-Fr guiding catheter (Cordis Corporation, Miami, FL, USA) was positioned in the proximal ICA. A distal access catheter (6F Navien, Micro Therapeutics, Inc. dba ev3 Neurovascular, CA, USA; 6F Sofia PLUS Catheter, MicroVention, Terumo, CA, USA) was introduced into an 8-Fr guiding catheter, and this coaxial system was placed at the distal of the targeted ICA. The stent retriever thrombectomy was conducted with the adoption of the Solitaire AB stent retriever (6 × 30 mm or 4 × 20 mm). A microcatheter (Rebar 18/27; EV3, Irvine, CA, USA) was passed through a 0.014-inch microwire (Traxcess; MicroVention, Inc., Tustin, CA, USA) to the distal of the clot, and a retrievable stent was deployed at the clot. The stent was maintained for at least 5 min after deployment, and then the stent and microcatheter were slowly retrieved together as a whole. During retrieval of the stent system, manual negative pressure suction was continuously performed with a 50-mL syringe through the distal access catheter. Aspiration thrombectomy, combined aspiration combined with stent retriever thrombectomy, intra-arterial thrombolysis, intravenous administration of the GPIIb/IIIa inhibitor, balloon angioplasty, or stent placement, selected by the neuro interventionist, was adopted as a rescue therapy when successful recanalization failed after multiple attempts.

Evaluation of outcomes

Thrombus burden was assessed using the clot burden score (CBS) according to baseline CT angiography (CTA) (5). According to CTA, ICA occlusion extended into the MCA and or anterior cerebral artery/MCA main stem occlusion extended into the M2 branch is defined as a bifurcation occlusion, while the remaining is defined as a main stem occlusion (6). The time intervals from the groin puncture to the last angiography were calculated as procedural time. The recanalization result was evaluated by adopting the modified Thrombolysis in Cerebral Infarction (mTICI) grade. Angiographic results after the first thrombectomy attempt were recorded for final analysis. FPE was defined as mTICI ≥2c reperfusion after a single first attempt (4). The follow-up brain non-enhanced CT scan was usually performed 24 h after thrombectomy, and a repeat CT/MRI scan within 24–72 h, or immediately when clinical neurological deterioration occurred. When a hyperdense lesion without mass effect was observed on the initial follow-up CT scan after EVT, a repeat CT or MRI scan was conducted within the next 24 h, to discriminate contrast medium extravasation. Symptomatic intracranial hemorrhage (SICH) was evaluated based on the Heidelberg Bleeding Classification (7). The functional outcome was rated by the modified Rankin Scale (mRS) score at 90 days, and scores ≤2 were considered favorable functional outcomes. Two neuroradiologists who were blinded to the patient's medical information, including laboratory characteristics, independently assessed neuroimaging findings. For any disagreements between the two evaluators, another experienced neuroradiologist re-evaluated the neuroimaging and helped to achieve a final consensus.

Statistical analysis

The continuous data were displayed as mean ± standard deviation (SD) or median (interquartile range [IQR]). Statistical tests were conducted using the Student's t-test for normally distributed continuous variables and the Mann–Whitney U test for continuous variables that did not conform to a normal distribution. The categorical data were expressed as frequencies and percentages and statistical comparisons were performed using the chi-square test. The tolerance and variance inflation factor (VIF) values were calculated to evaluate multicollinearity between variables, with tolerance <0.1 and VIF >10 considered indicative of multicollinearity. Those predictors found to be associated with FPE on univariate analysis (P <0.10) were then enrolled into the multivariate logistic regression analysis to determine independent predictors. Results were displayed as adjusted odds ratios (OR) combined with a 95% confidence interval (CI). The receiver operating characteristic (ROC) curve was utilized to determine the cutoff value of the predictor and its accuracy for the prediction of FPE. Statistical analyses were implemented employing SPSS version 26 (IBM Corp., Armonk, NY, USA) and R version 3.3.3 (R Foundation, Vienna, Austria).

Results

A total of 485 patients with AIS were treated with first-line stent retrieval thrombectomy during the study period. Finally, 313 patients (163 men [52.1%]’ mean age 69.5 ± 12.9 years) were enrolled in this analysis (Fig. 1). The median admission baseline NIHSS score was 15 (IQR = 12–21), and the median time from the stroke symptom onset to sampling was 233 min (IQR = 141–388 min). The median admission plasma D-dimer levels were 0.85 mg/L (IQR = 0.40–1.76 mg/L). Regarding the stroke etiology, there were 102 (32.6%) patients with large-artery atherosclerosis, 168 (53.7%) patients with cardioembolism, 5 (1.6%) patients with other determined causes, and 38 (12.1%) patients with undetermined causes. The median time from groin to recanalization was 76 min (IQR = 46–116 min). Ultimately, successful recanalization (mTICI 2b–3) and satisfied recanalization (mTICI 2c–3) were achieved in 254 (81.2%) and 175 (55.9%) patients, respectively. Of the included patients, 88 (28.1%) patients achieved FPE (Table 1).

Fig. 1.

Flow chart of enrolled patients. ACA, anterior cerebral artery; AMI, acute myocardial infarction; DVT, deep venous thrombosis; EVT, endovascular thrombectomy; ICA, internal carotid artery; IVT, intravenous thrombolysis; LVO, large vessel occlusion; M2/M3, second/third segment of the middle cerebral artery; mRS, modified Rankin Scale; PE, pulmonary thromboembolism; SICH, symptomatic intracranial hemorrhage.

Table 1.

Characteristics of patients between FPE and non-FPE.

Characteristics	All (n = 313)	FPE (n = 88)	Non-FPE (n = 225)	P value
Age (years)	69.5 ± 12.9	69.2 ± 11.5	69.6 ± 13.4	0.800
Male	163 (52.1)	49 (55.7)	114 (50.7)	0.425
Hypertension	192 (61.3)	56 (63.6)	136 (60.4)	0.602
Diabetes mellitus	57 (18.2)	23 (26.1)	34 (15.1)	0.039
Coronary heart disease	57 (18.2)	18 (20.5)	39 (17.3)	0.520
Atrial fibrillation	126 (40.3)	40 (45.5)	86 (38.2)	0.241
Previous stroke	37 (11.8)	10 (11.5)	27 (12.0)	0.875
Current antiplatelet	32 (10.2)	7 (8.0)	25 (11.1)	0.407
Current anticoagulant	31 (9.9)	11 (12.5)	20 (8.9)	0.336
NIHSS	15 (12–21)	15 (11–21)	16 (12–21)	0.501
ASPECTS	9 (7–9)	9 (7–9)	8 (7–9)	0.360
OTS	233 (141–388)	230 (137–383)	238 (141–403)	0.790
Plasma biomarkers
Neutrophil (10⁹/L)	4.3 (3.7–5.4)	4.1 (3.6–5.2)	4.5 (3.9–5.6)	0.336
Fibrinogen (g/L)	3.0 (2.6–3.9)	2.8 (2.4–3.5)	3.1 (2.7–4.2)	0.580
Platelet (10⁹/L)	190 (164–241)	201 (176–256)	186 (159–228)	0.298
D-dimer (mg/L)	0.85 (0.40–1.76)	0.53 (0.27–1.36)	1.12 (0.58–2.27)	<0.001
Clot burden score	6 (4–7)	7 (6–7)	5 (4–6)	0.012
Intravenous thrombolysis	99 (29.1)	30 (34.1)	61 (27.1)	0.222
Stroke etiology				0.174
LAA	102 (32.6)	28 (31.8)	74 (32.9)
Cardioembolism	168 (53.7)	52 (59.1)	116 (51.6)
Other determined	5 (1.6)	0	5 (2.2)
Undetermined	38 (12.1)	8 (9.1)	30 (13.3)
Occlusion site				0.042
ICA	90 (28.8)	18 (20.5)	72 (32.0)
M1	223 (71.2)	70 (79.5)	153 (68.0)
Occlusion pattern				<0.001
Main stem	119 (38.0)	47 (53.4)	72 (32.0)
Bifurcation occlusion	194 (62.0)	41 (46.6)	153 (68.0)
OTP (min)	302 (215–469)	290 (200–458)	307 (224–469)	0.856
PTR (min)	76 (46–116)	47 (39–65)	90 (59–128)	<0.001
Final mTICI 2b–3	254 (81.2)	88 (100)	166 (73.8)	<0.001
Final mTICI 2c–3	175 (55.9)	88 (100)	87 (38.7)	<0.001
SICH	37 (11.8)	6 (6.8)	31 (13.8)	0.086
mRS at 90 days	3 (2–5)	2 (1–4)	4 (2–5)	<0.001
mRS score ≤2 at 90 days	111 (35.5)	46 (52.3)	65 (28.9)	<0.001

Values are given as n (%), mean ± SD, or median (IQR).

ASPECTS, Alberta Stroke Program Early CT Score; FPE, first pass effect; ICA, internal carotid artery; IQR, interquartile range; LAA, large-artery atherosclerosis; M1, the first segment of middle cerebral artery; mRS, modified Rankin Scale; mTICI, modified Thrombolysis in Cerebral Infarction; NIHSS, National Institute of Health Stroke Scale; OTP, onset to groin puncture time; OTS, onset to blood sampling time; PTR, puncture to final recanalization time; SD, standard deviation; SICH, symptomatic intracranial hemorrhage.

No significant differences were found in demographic characteristics, stroke etiology, or proportion of intravenous thrombolysis between the FPE and non-FPE groups. Compared with patients in the non-FPE group, patients with FPE were more likely to have diabetes mellitus (26.1% vs. 15.1%; P = 0.039), had lower plasma D-dimer levels (0.60 vs. 0.92 mg/L; P <0.001), higher clot burden score (7 vs. 5; P = 0.012), had a higher proportion of M1 MCA (79.5% vs. 68.0%; P = 0.042), and had a higher proportion of main stem occlusion (53.4% vs. 32.0%; P <0.001). The time intervals from symptom onset to blood sampling were comparable in both groups (230 vs. 238 min; P = 0.790). The primary procedural outcomes suggested a significantly shorter median time to revascularization in the FPE group (47 vs. 90 min; P <0.001), higher final mTICI 2b–3 reperfusion (100% vs. 73.8%; P <0.001), and higher final mTICI 2c–3 reperfusion (100% vs. 38.7%; P <0.001) than that in the non-FPE group. In terms of clinical outcomes, FPE patients who suffered slightly lower SICH without a significant difference (6.8% vs. 13.8%; P = 0.086) achieved significantly better functional outcomes than non-FPE patients (52.3% vs. 28.9%; P <0.001). Fig. 2 shows the mRS score distribution (Fig. 2a), and the box plots of plasma D-dimer levels (Fig. 2b) between the FPE and non-FPE groups.

Fig. 2.

(a) mRS distribution (P <0.001) and (b) box plots of plasma D-dimer levels (P <0.001) between the FPE group and non-FPE group. FPE, first pass effect; mRS, modified Rankin Scale.

Finally, the tolerance was >0.1, and VIF was significantly <10 for the predictors, indicating no multicollinearity in the models (Table 2). In the univariate analysis, D-dimer, diabetes mellitus, M1 MCA occlusion, clot burden score, and main stem occlusion pattern were significantly associated with FPE (P <0.05) (Table 3). After adjusting for potential variables, multivariable logistic regression analysis also found that D-dimer levels (adjusted common OR [acOR] = 0.81; 95% confidential interval [CI] = 0.52–0.96; P = 0.015), clot burden score (acOR = 1.76; 95% CI = 1.38–2.87; P = 0.031), and main stem occlusion pattern (acOR = 1.85; 95% CI = 1.19–2.62; P <0.001) were significantly associated with FPE. Based on the ROC curve, the optimal cutoff value of D-dimer as a predictor for predicting FPE was 0.97 mg/L, which showed a sensitivity of 79.3% and a specificity of 87.4%, a negative predictive value of 85.1%, and had an area under the curve of 0.761 (Fig. 3).

Fig. 3.

Receiver operating characteristic curve was utilized to evaluate the predictive ability of emergency admission plasma D-dimer levels for first pass effect (area under the curve = 0.761).

Table 2.

The tolerance and VIF for multicollinearity between variables.

Characteristics	Tolerance	VIF
D-dimer	0.826	1.114
Diabetes mellitus	0.941	1.068
Clot burden score	0.863	1.312
M1 MCA occlusion	0.907	1.152
Main stem	0.916	1.098

MCA, middle cerebral artery; VIF, variance inflation factor.

Table 3.

Unadjusted and adjusted ORs of the association of patient characteristics with FPE (n = 313).

Variables	Unadjusted OR (95% CI)	Unadjusted P value	Adjusted OR (95% CI)	Adjusted P value
D-dimer	0.72 (0.41–0.91)	0.001	0.81 (0.52–0.96)	0.015
Diabetes mellitus	1.69 (1.09–2.62)	0.038	1.36 (0.89–2.32)	0.120
Clot burden score	1.82 (1.27–3.23)	0.012	1.76 (1.38–2.87)	0.031
M1 MCA occlusion	1.38 (1.02–3.30)	0.044	1.24 (0.95–3.09)	0.071
Main stem	1.98 (1.24–3.47)	<0.001	1.85 (1.19–2.62)	<0.001

CI, confidence interval; FPE, first pass effect; MCA, middle cerebral artery; OR, odds ratio.

Discussion

To our knowledge, no publication has reported the association between emergency admission D-dimer levels and FPE in patients with AIS treated with thrombectomy. The present study suggested that low D-dimer levels were significantly associated with FPE after stent thrombectomy and that independent correlations persisted after adjusting for potential factor interference.

Nowadays, imaging predictors of FPE in patients with AIS treated with thrombectomy have been extensively investigated, such as thrombus density, clot perviousness, thrombus enhancement sign, and thrombus burden score (8 –10). Unlike in blood biomarkers where publication remains scarce. D-dimer is a soluble fibrin degradation product, that acts as an objective measurement of blood biomarker characteristics and has been widely used in the diagnosis of systemic thrombotic diseases (11 –14). It is known that when a thrombus forms in the systemic circulation, with time, D-dimer levels may increase due to in activation of the thrombotic/fibrinolytic conditions (11,15). Furthermore, the origin and development of a clot follows a definitive chronology (15); as time goes by, a clot is further compacted by the water-hammer influence of systemic blood pressure (16), and finally, a mature clot rich in fibrin is developed (16,17). It can be concluded that the concentration of fibrin indicates the age of the clot. The clot characteristic is a critical factor in endovascular thrombectomy (18,19). Fibrin-rich clots decrease successful recanalization rates of stent retrievable thrombectomy due to their low deformability, high static friction, and steady state when deploying a retrievable stent (18 –20). Because the fibrin-rich clot is too rigid to be embedded, it has a greater tendency to “slip” over the dense clot during stent retrieval (21). In contrast, the red blood cell-rich clot is easier to recanalize than the fibrin-rich clot (22), probably because the red blood cell-rich clot is younger and more easily deformed than a fibrin-rich clot, allowing stent struts to penetrate into the clot more easily. In the present study, no significant difference was found in the time from symptom onset to blood sampling between the two groups. Thence, thrombus formation in the circulation system of non-FPE patients may occur before the onset of stroke symptoms, resulting in more mature clots, richer fibrin, and higher levels of D-dimer. A previous study also showed that higher admission D-dimer levels were a predictor of differentiating embolic from intracranial atherosclerosis-related in patients with LVO (23).

In addition, high D-dimer levels may represent thrombus volume in the occluded artery in patients with AIS (13). In view of this, previous literature has reported that admission D-dimer levels have recently emerged as a novel predictor of the presence of LVO in AIS. In patients with AIS, elevated D-dimer levels on admission may be associated with enhanced activation of the fibrinolytic system in occluded intravascular clot and a larger clot volume may lead to a significant elevation. Thence, as a reason why high D-dimer levels could predict FPE failure in stent retrievable thrombectomy, we consider it represents the larger volume of the clot in the occluded artery, the number of multiple passes of the stent retriever, and the potential incidence of distal embolism may be greater.

The CTA-based clot burden score is an objective and easily accessible semi-quantitative imaging parameter, and previous studies have demonstrated that the clot burden score is significantly associated with thrombus length, thrombolytic recanalization rate, and clinical outcomes (5). The present study found that a higher clot burden score (acOR = 1.76; 95% CI = 1.38–2.87) was significantly associated with FPE. After vessel occlusion, the static frictional force exists between the thrombus and the vessel wall. The larger the clot burden, the larger the contact area between the thrombus and the vessel wall, and the greater the corresponding frictional force, so it is difficult to remove the thrombus during stent retrieval (24). Second, there may be a mismatch between the stent and the thrombus length when the thrombus burden is too large, and the thrombus may be fragmented when the stent is retrieved (25). Clinical practice reports that bifurcation occlusion has been a challenge for thrombectomy even when different rescue treatments are proposed (26,27). Consistent with previous studies (26,27), the main stem occlusion pattern (acOR = 1.85; 95% CI = 1.19–2.62) was also significantly related with FPE in this study. When the thrombus extends into the bifurcation, the thrombus is not completely trapped by the stent and retrieval of the stent may result in displacement of the thrombus or fragmentation of the embolus into the distal branch (27). In addition, occlusion involves bifurcation, with a high percentage of embolic stroke etiologies (19). Because the embolic stroke clot is too rigid to be embedded, it has a greater tendency to “slip” over the dense clot during stent retrieval (21).

The present study has some limitations. First, bias exists inherent to the retrospective study design nature, but the relatively large sample size and adjusted multivariate logistic regression analysis reduce the impact of bias and made the conclusions more reliable. Second, we did not analyze thrombus composition, but this is due to the purpose of this study to focus on plasma biomarkers and the inherent limitation of the prediction delay existing in the thrombus composition. Nevertheless, we assessed clot burden score, occlusion pattern, and stroke etiology, among others.

In conclusion, a low emergency admission plasma D-dimer level was associated with FPE in patients treated with stent retriever thrombectomy. The plasma D-dimer levels are readily obtained at an early time point on emergency department arrival, and thus may facilitate the predetermination of thrombectomy strategies before EVT.

Footnotes

Acknowledgments

We would like to thank all authors for providing assistance during the preparation of this manuscript.

Declaration of conflicting interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.

ORCID iD

Wen-wei Tang

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