Journal of Vascular Surgery
Volume 49, Issue 3 , Pages 623-629, March 2009

Intracranial hemorrhage after carotid endarterectomy and carotid stenting in the United States in 2005

Presented at the 2008 Vascular Annual Meeting, San Diego, Calif, June 5-8, 2008.

  • Carlos H. Timaran, MD

      Affiliations

    • Division of Vascular and Endovascular Surgery, Department of Surgery, University of Texas Southwestern Medical Center, Dallas, Tex
    • Dallas Veterans Affairs Medical Center, Dallas, Tex
    • Corresponding Author InformationReprint requests: Carlos H. Timaran, MD, University of Texas Southwestern Medical Center, 5909 Harry Hines Blvd, Dallas, TX 75390-9157
    • ,
  • Frank J. Veith, MD

      Affiliations

    • Cleveland Clinic Foundation, Cleveland, Ohio
    • ,
  • Eric B. Rosero, MD

      Affiliations

    • Division of Vascular and Endovascular Surgery, Department of Surgery, University of Texas Southwestern Medical Center, Dallas, Tex
    • ,
  • J. Gregory Modrall, MD

      Affiliations

    • Division of Vascular and Endovascular Surgery, Department of Surgery, University of Texas Southwestern Medical Center, Dallas, Tex
    • Dallas Veterans Affairs Medical Center, Dallas, Tex
    • ,
  • R. James Valentine, MD

      Affiliations

    • Division of Vascular and Endovascular Surgery, Department of Surgery, University of Texas Southwestern Medical Center, Dallas, Tex
    • ,
  • G. Patrick Clagett, MD

      Affiliations

    • Division of Vascular and Endovascular Surgery, Department of Surgery, University of Texas Southwestern Medical Center, Dallas, Tex

Received 3 July 2008; accepted 10 September 2008.

Article Outline

Background

Intracranial hemorrhage (ICH) following carotid endarterectomy (CEA) or carotid artery stenting (CAS) is a rare but potentially devastating complication. The effect of more intense dual antiplatelet therapy required for CAS on the frequency of ICH has not been established. This study was undertaken to evaluate the nationwide occurrence of ICH associated with CAS vs CEA.

Methods

The Nationwide Inpatient Sample was used to identify patients discharged after CAS and CEA during 2005. The type of revascularization and major adverse events, ie, in-hospital ICH, postprocedural stroke, and death rates, were determined by cross-tabulating specific procedural codes for CAS and CEA and diagnostic codes for carotid stenosis. Risk stratification was performed using the Charlson Comorbidity Index. Univariate and multivariate logistic regression analyses were used to assess the association between type of revascularization, comorbidities, ICH, and risk-adjusted mortality.

Results

In 2005, the estimated number of carotid revascularizations was 135,903. The vast majority of patients underwent CEA (90.4%), whereas CAS was performed in 13,093 (9.6%) patients. Most patients (92.2%) underwent treatment for asymptomatic carotid stenosis. CAS patients had higher postoperative stroke rates (2.1% vs 1.1%; P < .001) and in-hospital mortality (1.1% vs 0.6%; P < .001) than CEA patients. ICH occurred in 19 patients (0.15%) after CAS and in 20 patients (0.016%) after CEA (P < .001). CAS was identified as an independent predictor for postoperative stroke (odds ratio [OR], 1.77; 95% confidence interval [CI], 1.5-2.0; P < .001), in-hospital mortality (OR, 1.49; 95% CI, 1.2-1.8; P < .001) and ICH (OR, 5.9; 95% CI, 3.1-11.1; P < .001) after adjusting for age, gender, symptomatic status, comorbidities, admission, and hospital type using logistic regression. In-hospital mortality was 12.5% among patients developing ICH (OR, 23.2; 95% CI, 9.1-54.4; P < .001).

Conclusion

In the United States, patients undergoing CAS have not only significantly increased postoperative stroke and death rates compared with those undergoing CEA, but also a sixfold increased risk of ICH. Although ICH after CAS is extremely rare, its devastating nature and high mortality warrant further investigation to define specific risk factors, prevention, and treatment strategies.

 

Intracranial hemorrhage (ICH) after carotid endarterectomy (CEA) occurs in 0.2% to 0.5% of cases and has primarily been attributed to hyperperfusion syndrome (HPS).1, 2, 3, 4 ICH and HPS are probably related to the preoperative loss of vascular autoregulatory mechanisms in a chronically hypoperfused cerebral hemisphere.5, 6, 7 HPS usually manifests clinically as transient focal deficits associated with ipsilateral retro-orbital headache, seizures, and only rarely ICH.5 Although hyperperfusion seems to occur to some extent in most patients after carotid revascularization, HPS develops only in 2% to 3% of patients undergoing CEA.5 Both HPS and ICH are associated with significant morbidity and mortality, and they are well-described complications of CEA.3, 5, 8

HPS and ICH have recently been described after carotid artery stenting (CAS).4, 6, 9, 10 Although HPS has similar manifestations after CAS as CEA, the overall outcomes and prognosis appear to be worse after CAS.6, 11 Furthermore, recent studies suggest a more acute onset and a relatively higher incidence of ICH after CAS, which may be greater than 5%.6, 10, 12 The potential effect of more intense dual antiplatelet therapy required for CAS13 on the frequency of ICH has not been established.

This study was undertaken to evaluate the nationwide occurrence and outcomes of ICH associated with CAS vs CEA in the United States. The objectives of this study were to compare the frequency and risk factors for ICH occurring during the same hospitalization after CAS as compared with CEA. In addition, associations between type of carotid revascularization (CAS vs CEA) and in-hospital ICH, postprocedural stroke, and death were also assessed.

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Methods 

The Nationwide Inpatient Sample (NIS) from the Healthcare Cost and Utilization Project (HCUP) was used to identify all CAS and CEA procedures performed in 2005. The NIS is the largest all-payer inpatient database in the United States.14 It represents a 20% stratified sample of inpatient admissions to US academic, community, and acute care hospitals nationwide (about 1000 hospitals in 38 states; excludes veterans affairs and other federal and prison hospitals). Typical discharge data collected include demographics, primary and 14 different secondary diagnoses, primary and 14 different secondary procedures per patient as identified by the International Classification of Diseases, 9th Revision, Clinical Modification (ICD-9-CM) codes, length of stay, charges, and outcomes. Sampling weights are provided for accurate calculations based on the complex survey design of the dataset. HCUP quality control procedures are routinely performed to confirm that data values are valid, consistent, and reliable.15 The NIS core inpatient files were used for data extraction and analysis. Because NIS data is publicly available and contains no personal identifying information, this study was exempt from institutional review board approval.

All CAS and CEA procedures performed in 2005 were identified by linking the ICD-9-CM procedural codes for CEA and CAS with a primary or secondary diagnosis of carotid stenosis. The ICD-9-CM coding system has had a specific code for CAS since 2004 (00.63). Thus, all CAS procedures performed in 2005 can be accurately identified. CEA procedures were also identified using a specific code (38.12). Symptomatic status of patients with carotid stenosis was determined according to ICD-9-CM discharge diagnosis. Patients were classified as symptomatic if discharge diagnosis was “carotid artery stenosis with stroke” or if diagnosis codes included transient ischemic attacks (TIA) or amaurosis fugax. Patients with discharge diagnosis of “carotid artery stenosis without mention of stroke” with no accompanying diagnoses for TIA or amaurosis fugax were classified as asymptomatic. Based on 15 diagnosis codes (ICD-9-CM) and the clinical classification software (CCS; Agency for Healthcare Research and Quality, Rockville, Md) coding system included in the data,16 comorbid medical conditions were defined and used further to calculate a comorbidity score based on the modified Charlson Comorbidity Index (CCI).17 The CCI is a validated measure for use with administrative data that correlates with in-hospital morbidity and mortality after surgical procedures, including elective carotid interventions.18 Each of the indicated diagnoses is assigned a weight and summed to provide a patient's total score. The CCI was further used to define two surgical-risk-based groups according to comorbidities (CCI ≤1 indicating low-risk vs CCI >1 indicating greatest comorbidity) for analyses.

The primary outcome endpoint of this cross-sectional population-based study was the occurrence of in-hospital ICH and death after carotid revascularization procedures, ie, ICH and/or deaths that occur after CEA or CAS during the same hospitalization. All instances of ICH occurring in patients undergoing CEA and CAS during the same hospitalization were identified using appropriate specific ICD-9-CM codes (432, 432.0, 432.9, 430). In addition, the occurrence of postoperative stroke was also assessed. Postoperative stroke was defined as an ICD-9-CM secondary diagnostic code of “postoperative stroke (997.02)”. Postoperative death was defined as any death occurring during the same hospitalization. Mortality data was available directly from the dataset, which is entered as died during hospitalization and is coded from disposition of patient. Weighted analyses for predictors of in-hospital ICH, stroke, and death included demographic data, symptomatic status, preoperative comorbidities, and risk stratification, which were based on the comorbidity index, and hospital characteristics.

Descriptive statistics for categorical variables are presented as relative frequencies (percents), which were compared with χ2 test (χ2 for independent groups, two-tailed P value). Continuous variables were expressed as medians and interquartile ranges and compared with nonparametric tests. In-hospital ICH, stroke, and death rates were adjusted for patient age, gender, symptomatic status, and CCI for risk-stratification using multivariate stepwise logistic regression analyses. Findings were considered statistically significant if the resulting P value was less than .05 for the primary and secondary endpoints (in-hospital ICH, postoperative stroke, and death). Multivariate odds ratios (OR) are reported with 95% confidence intervals (CI). Nationwide estimates and weighted data analyses were obtained using population-based procedures specific to the unique NIS sample design. SAS version 9.1 (SAS Institute, Cary, NC) was used for data analyses.

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Results 

The estimated number of carotid revascularizations performed nationwide in 2005 was 135,903. Most patients underwent CEA (n = 122,984; 90.4%), whereas CAS was only performed in 13,093 (9.6%) patients. Of these, 76.5% were elective carotid procedures. Patient characteristics and comorbidities according to type of carotid revascularization are listed in Table I. Most patients (92.2%) underwent treatment for asymptomatic carotid stenosis. Among patients with symptomatic stenosis, 58% had TIA and 42% had stroke listed as principal or secondary diagnoses.

Table I. Clinical characteristics of patients undergoing CAS and CEA in 2005
CASCEAP value
(n = 13,093)(n = 122,984)
Median age, year (IQR)72(64-78)72(65-78).72⁎
Female gender, %37.842.6<.001†
Symptomatic carotid stenosis, %9.67.7.24
Comorbidities, %
Hypertension69.176.0<.001†
Diabetes mellitus28.429.3.042†
Chronic lung disease17.621.2<.001†
Previous myocardial infarction11.211.7.117
Congestive heart failure11.77.6<.001†
Renal failure5.03.5<.001†
Charlson comorbidity index, median (IQR)1(1-3)1(0-2)<.001⁎
Teaching hospital, %65.940.4<.001†
Elective admission, %66.077.8<.001†

CAS, Carotid artery stenting; CEA, carotid endarterectomy; IQR, interquartile range.

⁎Mann-Whitney U test.

†χ2 analysis.

Patients undergoing CAS had a significantly greater prevalence of congestive heart failure and renal failure, whereas patients undergoing CEA had a greater prevalence of hypertension and chronic lung disease (Table I). Overall, CAS patients had a higher surgical risk profile according to the comorbidity index (32.8% with CCI ≥2 vs 29% in the CEA group; P < .001). The percentage of octogenarians was significantly higher in the CAS group compared with the CEA group (21.2% vs 19.7%; P < .001). The median length of stay among patients undergoing CAS (median, 1 day; interquartile range [IQR], 1-2 days) was significantly shorter compared with patients undergoing CEA (median, 1 day; IQR, 1-3 days; P < .001). A higher proportion of CAS procedures were classified as nonelective admissions (34% vs 22.2%), and more were performed in teaching hospitals (65.9% vs 40.4%) compared with CEA procedures.

Acute ICH during the same hospitalization occurred in 19 patients (0.15%) undergoing CAS and in 20 patients (0.016%) undergoing CEA (P < .001). In-hospital mortality was 12.5% among patients developing ICH (OR, 23.2; 95% CI, 9.1-54.4; P < .001). Among patients that developed ICH and underwent CAS, 5 of 19 (26%) died during the same hospitalization, whereas no deaths occurred among 20 patients that developed ICH and underwent CEA.

Univariate analysis revealed that patients in the CAS group had a 77% increased risk of postoperative stroke, compared to patients undergoing CEA (OR, 1.77; 95% CI, 1.3-2.4; P < .001). Patients undergoing CAS also had significantly higher postoperative stroke rates (2.1% vs 1.1%; P < .001) and in-hospital mortality (1.1% vs 0.6%; P < .001) than CEA patients. Combined stroke and death rates were also higher after CAS compared with CEA (2.8% vs 1.5%; P < .001).

Stratified analyses according to symptomatic status and type of carotid revascularization revealed that all 19 instances of ICH after CAS occurred in asymptomatic patients. Alternatively, among patients undergoing CEA, 5 cases of ICH occurred in symptomatic patients and 15 in asymptomatic patients. Symptomatic patients undergoing CAS had higher postoperative stroke rates (5% vs 2.6%) and in-hospital mortality (4.6% vs 1.4%) compared with patients undergoing CEA (P < .001). Similarly, asymptomatic patients in the CAS group had higher postoperative stroke rates (1.8% vs 1%; P < .001) and in-hospital mortality (0.7% vs 0.5%; P = .002) than those in the CEA group.

Multivariate logistic regression analysis revealed that patients undergoing CAS had a sixfold increased risk of ICH compared to those undergoing CEA after adjusting for age, gender, symptomatic status, comorbidity index, admission, and hospital type (OR, 5.9; 95% CI, 3.1-11.1; P < .001). Other independent predictors for ICH included increasing patient age, female gender, comorbidity index, renal failure, hypertension, and nonelective admission (Table II). Multivariate logistic regression models also revealed that CAS was associated with a 1.8-fold increased risk of postoperative stroke compared with CEA after adjusting for age, gender, symptomatic status, comorbidities, admission, and hospital type (OR, 1.77; 95% CI, 1.5-2.0; P < .001).

Table II. Independent predictors of intracranial hemorrhage and death after carotid interventions⁎
CoefficientOdds Ratio†95% Confidence IntervalP value
Intracranial hemorrhage
CAS (vs CEA)1.7545.903.1-11.1<.001
Age0.0551.021.01-1.02.003
Charlson comorbidity index0.2981.351.1-1.7.005
Nonelective admission2.68514.705.8-37.2<.001
Female gender1.5014.491.8-11.4.002
Hypertension0.6881.991.1-3.9.044
Renal failure1.7425.712.4-13.5<.001
In-hospital mortality
CAS (vs CEA)0.3981.491.2-18<.001
Age0.0131.011.01-1.02.001
Charlson comorbidity index0.3121.371.3-1.4<.001
Nonelective admission1.4054.073.5-4.7<.001
Female gender0.2481.281.1-1.5.001
Renal failure0.6511.921.5-2.4<.001
Symptomatic carotid stenosis0.6291.881.6-2.2<.001
Intracranial hemorrhage1.3884.011.5-10.9.007

CEA, carotid endarterectomy; CAS, carotid artery stenting.

⁎Variables with a P value <.25 in the univariate analysis and those known to be important and possible confounding factors were entered into the multivariate logistic regression models and selected by forward stepwise selection if P value <.05 (P < .001 for models).

ICH was identified as an independent predictor for in-hospital mortality by multivariate regression analysis (OR, 4.01; 95% CI, 1.5-10.9; P < .001). CAS was also independently associated with a 1.5-fold increased risk of in-hospital mortality compared with CEA (OR, 1.49; 95% CI, 1.2-1.8; P < .001). Increasing patient age, female gender, CCI, renal failure, symptomatic disease, and nonelective admission were also identified as independent predictors of in-hospital mortality by stepwise logistic regression (Table II).

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Discussion 

This nationwide population-based study indicates that patients who undergo CAS have not only significantly higher stroke and death rates compared with those undergoing CEA, but also significantly increased risk of ICH. The US national statistics also specifically demonstrate that CAS-related ICH is associated with significantly increased risk of in-hospital mortality compared with ICH associated with CEA. These results suggest that CEA is safer than CAS in patients with increased risk of ICH. Further studies are necessary to identify markers of increased risk for ICH among patients requiring carotid interventions.

Several observational studies have revealed that the incidence of postoperative ICH among patients undergoing CEA is in the range of 0.2% to 0.7%.1, 2, 3, 4 In contrast, the reported incidence of ICH after CAS has not been well established. Although large series of patients undergoing CAS report similarly low rates between 0.4% and 0.7%, smaller series with fewer than 100 cases reveal ICH rates as high as 5%.4, 6, 9, 10, 12, 19, 20 Our results revealed significant differences in ICH rates after CAS and CEA, with significantly higher risk of acute ICH after CAS. Of note, our data is restricted to ICH that occurred during the same hospitalization after carotid interventions. Because most episodes of ICH after CEA are related to HPS and occur several days after the intervention, the true incidence of this complication after carotid interventions is not reported in this study. Unfortunately, follow-up information cannot be obtained because the NIS dataset is thoroughly de-identified and restricted to inpatient data.

ICH after carotid interventions has usually been attributed to HPS.5 A second type of acute ICH has also been described.6, 12 In contrast to the delayed form associated with HPS, acute ICH occurs after a short postprocedural time course and resembles hypertensive ICH. It is usually fatal. Coutts et al6 were the first to emphasize the distinction between the early and delayed types of HPS and ICH occurring after both CEA and CAS. In their series, three categories of HPS could be differentiated: two occurred within a few hours after the carotid intervention whereas the “classic” delayed type of presentation occurred days after the procedure. The two early types include acute focal edema and acute ICH. The respective outcomes were significantly different: acute edema was associated with favorable outcome whereas acute ICH was typically fatal. Buhk et al12 have further suggested that acute ICH resembles hypertensive ICH and appears to be more frequent after CAS. Large observational studies have further demonstrated that the onset of HPS peaks on postoperative day 6 in patients undergoing CEA and within 12 hours in those undergoing CAS.4 Our results are consistent with these observations and suggest that acute ICH is significantly more frequent after CAS compared to CEA.

The difference in timing of ICH between the two carotid interventions cannot be easily explained. Distal cerebral embolization and subsequent ICH in areas of infarction may account for the increased risk of acute ICH after CAS. Several observational studies have in fact revealed that release of atherosclerotic fragments from carotid plaque occurs during virtually all CAS procedures and that a high proportion of stented carotid lesions continue to release embolic material after the procedure.20, 21, 22 These embolic episodes occur more frequently after CAS than after CEA.23 Superimposed cerebral reperfusion can lead to hemorrhagic transformation of the areas of infarction.5 However, because ICH is not necessarily associated with impaired autoregulation of cerebral blood flow under these circumstances, it cannot be attributed to HPS.

CAS frequently induce bradycardia and hypotension secondary to catheter instrumentation of the carotid bulb.24, 25, 26 Balloon inflation and stent placement are responsible for the direct stimulation of the carotid baroreceptors, which in turn may result in neuronal responses manifested as hemodynamic depression.27 Bradycardia is primarily related to increased parasympathetic discharges, whereas hypotension is caused by inhibition of the sympathetic tone. Hemodynamic depression has been associated with significant morbidity and mortality if not resolved expeditiously.28, 29, 30 Cerebral ischemia secondary to hemodynamic depression may occur more frequently during CAS compared with CEA resulting in severe endothelial injury secondary to hyperperfusion and reperfusion, thereby increasing the risk of ICH in the early postoperative period.5 A direct association between hemodynamic depression and ICH, however, has not been demonstrated.

Although acute hemorrhagic transformation of recent cerebral infarctions may account for the higher incidence of early ICH after CAS compared with CEA, pre-existing ischemic stroke has not consistently been associated with either HPS or ICH after carotid interventions. In our study, patients with symptomatic carotid stenosis and those presenting with ischemic stroke did not have an increased risk of ICH. A serious limitation of this study, however, is defining symptomatic status using ICD-9-CM codes. Significant undercoding and under-reporting that frequently occurs with administrative datasets may result in underestimation of the true frequency of symptomatic carotid stenosis in this study.

Subarachnoid hemorrhage has been reported to occur more frequently after CAS compared to CEA.4, 6, 9, 10 In the NIS dataset, however, no instances of subarachnoid hemorrhage were reported after neither CAS nor CEA, probably because of undercoding. Although undercoding is an inherent limitation of most administrative datasets, it probably occurs at a similar frequency after both CAS and CEA. Future studies are needed to define the true incidence and clinical significance of subarachnoid hemorrhage after carotid interventions.

In the present study, age, comorbidity index, hypertension, renal failure, female gender, and nonelective admission, in addition to CAS, were identified as independent predictors of ICH after carotid interventions. Previous studies have demonstrated similar risk factors for ICH after both CEA and CAS.4, 9 Of note, an association between hypertension and an increased risk of HPS and ICH after carotid interventions have consistently been reported. In our series, hypertension was associated with a twofold increased risk of acute ICH after carotid interventions. Aggressive treatment of hypertension in patients at high-risk for HPS has been shown to effectively reduce the risk of ICH after CEA.8 More recently, a similar approach in patients undergoing CAS has resulted in a lower incidence of HPS and ICH.31 These studies underscore the importance of treating hypertension in patients undergoing carotid interventions to reduce the risk of postprocedural ICH.

In the present study, the mortality rates were significantly higher in patients with ICH after carotid interventions compared with those that did not develop this complication. These results are consistent with previous reports of poor prognoses for ICH after both CAS and CEA.4, 19 In our series, 26% of patients that developed acute ICH and underwent CAS died during the same hospitalization, whereas no deaths occurred among patients that developed ICH after CEA. Thus, ICH after CAS was associated with a 34-fold increased risk of in-hospital mortality (OR, 33.9; 95% CI, 12-95; P < .001). We acknowledge that the absence of death among patients that developed ICH after CEA may be explained by undercoding or by late occurrence of ICH and HPS after CEA. As noted above, the incidence of delayed ICH is not known as only in-hospital major adverse events are available within the NIS dataset.

Although the present study includes the nationwide experience with carotid interventions performed in the United States in 2005, several important limitations should be acknowledged. First, miscoded and missing data can occur in large administrative datasets, such as the NIS. However, potential undercoding and misclassifications would have occurred without bias toward either of the two procedure groups. Second, the NIS dataset only includes in-hospital ICH, stroke, and death rates, which may erroneously be considered too low compared with the usually reported 30-day rates of major adverse events after carotid interventions. Third, the role of dual antiplatelet therapy on the incidence of ICH after CAS could not be assessed in our study as this information was not available. Patients undergoing CAS, however, usually receive dual antiplatelet therapy as opposed to those undergoing CEA. The possible role of dual antiplatelet therapy in patients undergoing CAS as a possible etiology factor for the higher incidence of ICH after CAS compared with CEA is further supported by previous studies revealing a higher incidence of ICH with the use of dual antiplatelet therapy as opposed to aspirin alone in high-risk neurologic patients.32 Again, it is unfortunate that the type of antiplatelet therapy in patients undergoing carotid interventions is not recorded in the NIS dataset. Finally, anatomic, lesion, procedural, and other patient and treatment characteristics, such as withholding antihypertensive medications prior to CAS, that could be explored as possible predictors of ICH are not available in the NIS dataset. Given these limitations, case-and-effect relationships based on the results of this study cannot be drawn. Future studies assessing their effects on the incidence and outcomes of ICH after carotid interventions are needed.

In conclusion, patients undergoing CAS in the United States have not only significantly increased postoperative stroke and death rates compared with those undergoing CEA, but also a sixfold increased risk of ICH. CEA may in fact be safer than CAS in patients with increased risk of ICH. Further studies are necessary, however, to identify patient and lesion characteristics that increase the risk of ICH among patients requiring carotid interventions. Although ICH after CAS is extremely rare, its devastating nature and high mortality warrant further investigation to define specific risk factors and to determine prevention and treatment strategies.

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Author contributions 


Conception and design: WS, TP, UM, AV

Analysis and interpretation: KB, SR, EG, WS

Data collection: KB, SR, TP, AV

Writing the article: KB, SR, AV, TP, WS

Critical revision of the article: WS, AV, UM

Final approval of the article: WS, AV, TP, UM

Statistical analysis: KB, SR, EG

Obtained funding: Not applicable

Overall responsibility: WS, KB, TP

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 Competition of interest: none.

PII: S0741-5214(08)01676-5

doi:10.1016/j.jvs.2008.09.064

Journal of Vascular Surgery
Volume 49, Issue 3 , Pages 623-629, March 2009

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