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ORIGINAL ARTICLE

Prevalence of atherosclerotic stenosis of the carotid and cerebral in patients with stable or unstable coronary disease

Przemysław Puz1,2, Anetta Lasek­‑Bal1,2, Aldona Warsz­‑Wianecka1,2, Maciej Kaźmierski3 1 Department of Neurology, Medical University of Silesia, Professor Leszek Giec Upper Silesian Medical Centre, Katowice, Poland 2 School of Health Sciences in Katowice, Medical University of Silesia, Katowice, Poland 3 3rd Department of Cardiology, Medical University of Silesia, Professor Leszek Giec Upper Silesian Medical Centre, Katowice, Poland

Key words Abstract atherosclerosis, Introduction Carotid artery atherosclerosis is a recognized predictor of cardiovascular events. carotid, cerebral, The coexistence of coronary atherosclerosis and cerebrovascular disease is associated with unfavorable coronary artery clinical outcomes. disease Objectives The aim of this study was to determine the prevalence of hemodynamically and clinically significant carotid and / or cerebral artery stenosis in patients with stable and unstable coronary artery disease (CAD). Patients and methods Cardiac and neurological examinations together with coronary angiography and carotid ultrasound were performed in 241 patients, and transcranial Doppler imaging of cerebral arteries in 114. The prevalence of hemodynamically significant (ICA) stenosis, intracranial artery stenosis, and clinical signs of central nervous system ischemia were compared between patients with stable and unstable CAD. Results There was no significant difference in the prevalence of ICA stenosis (15.3% vs 19%) and intracranial artery stenosis (18% vs 16%) between patients with stable and unstable CAD. Risk fac- tors for cerebral artery stenosis included ICA stenosis (odds ratio [OR], 13.21; 95% CI, 5.93–41.89) and advanced CAD (OR, 2.38; 95% CI, 1.13–4.09), and for ischemic events within the central nervous system, ICA stenosis (OR, 1.74; 95% CI, 1.01–3.16) and intracranial artery stenosis (OR, 3.01; 95% CI, 1.66–5.57). Conclusions No differences in the prevalence of atherosclerosis of the carotid and cerebral arteries were found between patients with stable and unstable CAD in this study. Advanced CAD is one of the risk factors for hemodynamically significant cerebral artery stenosis.

Introduction Atherosclerosis is a systemic ar‑ studies, large international registries, and post‑ Correspondence to: 4-8 Przemysław Puz, MD, PhD, terial disease; however, the mechanisms under‑ mortem studies. Department of Neurology, lying the formation, development, and destabili‑ Polyvascular atherosclerosis in patients Medical University of Silesia, zation of concomitant lesions observed in arter‑ with single or multifocal clinical manifesta‑ Professor Leszek Giec Upper Silesian Medical Centre, ies of various calibers and varying reactivity pa‑ tions is associated with unfavorable clinical ul. Ziołowa 45, 40-635 Katowice, rameters remain unclear.1-3 outcomes.4-6,9 Poland, phone: +48 32 359 83 06, The involvement of arteries from different Atherosclerotic lesions in the carotid arter‑ email: [email protected] Received: March 19, 2020. vascular areas indicates a significant burden of ies and the thickness of the intima­‑media com‑ Revision accepted: April 16, 2020. the atherosclerotic process, even if patients have plex are recognized predictors of cardiovascular Published online: May 1, 2020. never experienced any clinical symptoms of ath‑ events in patients with symptomatic or asymp‑ Pol Arch Intern Med. 2020; erosclerosis. The coexistence of atherosclerosis in tomatic ischemic heart disease and of complica‑ 130 (5): 412-419 doi:10.20452/pamw.15330 the coronary arteries, carotid arteries, and oth‑ tions during coronary angiography and coronary Copyright by the Author(s), 2020 er vascular territories has been proven in clinical artery bypass graft (CABG) surgery.3,10-13

412 POLISH ARCHIVES OF INTERNAL MEDICINE 2020; 130 (5) What’s new? selected randomly due to the availability of an ul‑ trasound device in the Department of Neurology In this study, the coexistence of carotid or intracranial atherosclerosis with during their hospitalization. Primarily, there were coronary artery disease (CAD) was confirmed in more than 16% of patients. 126 patients selected; however, in the end, 114 pa‑ We did not find any significant difference in the prevalence of internal carotid tients were included into our study due to lack of artery and intracranial arterial stenoses between patients with stable CAD an appropriate acoustic window for the TCD ex‑ and those with the unstable disease. Advanced CAD was a risk factor for amination in 12 patients. the hemodynamically significant stenosis of cerebral arteries. Our findings Existing diseases and conditions commonly support a multivessel approach in patients with a single clinical manifestation considered actual and possible risk factors for stroke were determined based on recent medical of atherosclerosis. Knowledge of the site and severity of atherosclerotic lesions records and results of in­‑hospital tests. is of importance to clinicians who qualify patients for interventional treatment Heart failure, CAD, and myocardial infarction of various vascular areas, as patients with multivessel disease gain fewer were defined based on the previously described benefits. Our findings confirmed that extensive diagnostic procedures per- and established recommendations,21,22 whereas formed in patients with advanced CAD, including the examination of intracranial stroke and transient ischemic attack (TIA) were arteries, can help identify those at risk of central nervous system ischemia. defined according to the current American Stroke Association guidelines.23 All patients were eval‑ uated for risk factors for atherosclerosis, which included arterial hypertension, diabetes, obesi‑ Significant coronary artery disease (CAD) co‑ ty, lipid disorders, and nicotinism. existing with carotid stenosis in patients under‑ Unstable CAD was defined as a coronary vas‑ going interventional treatment of carotid artery cular disease causing acute coronary syndrome. stenosis (stenting or endarterectomy) is associ‑ The status of cardiac ischemia which did not lead ated with the risk of periprocedural cardiac com‑ to acute coronary syndrome was classified as sta‑ plications (myocardial infarct).14,15 ble CAD. An increase and / or decrease in cardi‑ Available data emphasizing the clinical rele‑ ac troponin levels, with at least 1 value above vance of coronary atherosclerosis, particularly the 99th percentile of the upper reference lim‑ of the asymptomatic disease, in the evaluation it, was a parameter used to confirm acute coro‑ of the prevalence of cerebral artery atherosclero‑ nary syndrome. sis and the risk for cerebral events are still scarce, The abovementioned conditions were confirmed which prompted us to investigate this area.16-18 by a neurologist, a cardiologist, or an internist. Vascular ultrasound examination with Doppler The exclusion criteria were as follows: nonath‑ color flow imaging is a modality routinely used to erosclerotic stenosis, potential causes of cere‑ assess morphological changes in the carotid ar‑ bral embolism other than atherosclerotic lesions teries and blood flow disturbances caused by ath‑ in the carotid artery (atrial fibrillation, mitral erosclerosis. Ultrasound examination of the in‑ and / or aortic valve stenosis, mechanical heart tracranial arteries can also be used as an addi‑ valve, persistent foramen ovale or another de‑ tional method to evaluate the risk of cardiovas‑ fect, interatrial septal aneurysm, cardiac myxo‑ cular events in patients with atherosclerosis.19,20 ma, or a thrombus in the left ventricle or atrium), The aim of this study was to determine carotid artery dissection or intraluminal throm‑ the prevalence of hemodynamically significant bosis visible on ultrasound and brain damage oth‑ stenosis of the carotid and / or cerebral arteries er than of vascular origin (detected on comput‑ in patients with stable and unstable CAD. ed tomography or magnetic resonance imaging An additional aim was to determine the preva‑ of the head), central nervous system (CNS) isch‑ lence of symptomatic carotid and cerebral artery emic symptoms in the area of the posterior cere‑ stenosis coexisting with CAD. bral circulation. All patients underwent coronary angiography Patients and methods The study involved according to the standard protocol.24 Based on 241 patients with CAD who were hospitalized in coronary angiography results, patients with ad‑ the 3rd Department of Cardiology at Medical Uni‑ vanced coronary lesions were identified. These versity of Silesia, Katowice, Poland. were patients who had atherosclerotic lesions In all patients, a medical history was taken and causing stenosis greater than 50% in more than a physical examination was performed, including 2 sites and those with mild atherosclerotic le‑ cardiac and neurological examinations, electro‑ sions causing stenosis greater than 50%, found cardiography, echocardiography, coronary angi‑ in 1 site or 2 sites. ography, carotid artery ultrasound, and laborato‑ Duplex Doppler ultrasound of the carotid and ry tests routinely carried out in patients admit‑ vertebral arteries was performed with the 7.5­ ted to the Department of Cardiology in order to ‑MHz linear array probe (Elegra, Siemens, Erlan‑ diagnose CAD. In 114 patients, an additional ul‑ gen, Germany) and the degree of stenosis and ath‑ trasound examination of the intracranial arter‑ erosclerotic plaque morphology was assessed. Ca‑ ies with transcranial color Doppler (TCD) imaging rotid stenosis was graded based on morphological was performed in the Department of Neurology data (B­‑mode images, color flow imaging), velocity at Medical University of Silesia, Katowice, Poland. measurements (in the stenotic and poststenotic The patients who underwent TCD imaging were segments), and collateral flow evaluated according

ORIGINAL ARTICLE Carotid and cerebral artery atherosclerosis in patients with CAD 413 to the combined criteria for internal carotid ste‑ The prevalence of hemodynamically signifi‑ nosis grading published by von Reutern et al.25 cant ICA stenosis, the presence of significant in‑ For the purpose of this study, internal carot‑ tracranial aortic stenosis, and clinical signs of id artery (ICA) stenosis greater than 50% was CNS ischemia (TIA, stroke) were compared be‑ considered significant. The velocity criteria for tween patients with stable CAD and those with significant ICA stenosis (>50%) were as follows: unstable CAD. peak systolic velocity greater than or equal to 120 cm/s, end diastolic velocity greater than or Statistical analysis Statistical analysis was per‑ equal to 40 cm/s, the ratio of peak systolic veloci‑ formed using the tests listed below. Basic sta‑ ty of ICA to peak systolic velocity of the common tistical parameters were calculated for interval­ carotid artery greater than or equal to 2. ‑scale variables (mean [SD], median [interquar‑ In all patients, carotid duplex Doppler ultra‑ tile range]). These variables were tested for nor‑ sound was performed by an experienced cardi‑ mality using the Shapiro–Wilk test. Numbers ologist (MK) and a neurologist (PP), who agreed and percentages were given for nominal vari‑ on the degree of stenosis. ables. Mean and median values of interval­ The intracranial arteries were examined by as‑ ‑scale variables were compared using the t test sessing the following hemodynamic parameters (for variables with normal distribution) or with TCD imaging: mean blood flow velocity in the Mann–Whitney test (for variables with dis‑ the arteries (periorbital arteries, middle cerebral tribution other than normal). Study groups were arteries, anterior cerebral arteries, posterior ce‑ compared for nominal variables using the χ2 test rebral arteries, vertebral arteries, and the bas‑ or the Fisher test, depending on the group size. ilar artery). The Pioneer 2002 TC device (EME, In order to identify risk factors for ICA steno‑ Überlingen, Germany), equipped with a 2‑MHz­ sis, intracranial artery stenosis, and CNS isch‑ pulse‑wave­ Doppler ultrasound probe, was used. emic events, univariable logistic regression anal‑ The first part of the study aimed to evaluate ysis was applied. It included risk factors for ath‑ mean blood flow velocity expressed in centime‑ erosclerosis (age, sex, arterial hypertension, di‑ ters per second and the Gosling pulsatility in‑ abetes mellitus, lipid disorders, body mass in‑ dex in the vertebral arteries, the basilar artery, dex >25 kg/m2, nicotine abuse, and heart failure) the middle, anterior, and posterior cerebral arter‑ and the presence and advancement of athero‑ ies (at the depth of 56 mm, 70 mm, and 35 mm, sclerotic lesions in the coronary vessels. Based respectively). Subjects were examined in a supine on the presence of ICA and / or intracranial ar‑ position, except for the assessment of the arter‑ tery stenosis, a univariable analysis model was ies of the vertebral­‑basilar system, which was developed to assess the cumulative risk of CNS performed in a sitting position. The middle ce‑ ischemic events in patients with comorbid ICA rebral artery (MCA) stenosis greater than 50% stenosis and intracranial arterial atherosclero‑ was diagnosed based on the following criteria: sis. Odds ratios (ORs) with 95% CIs were calcu‑ mean velocity greater than 80 cm/s, systolic ve‑ lated for the pre­‑identified independent factors. locity greater than 160 cm/s, the ratio of mean A P value less than 0.05 was considered signifi‑ velocity in the prestenotic site to mean velocity cant. Analyses were performed using the Statis‑ in the stenotic site of 1 to 2 or more, a segmental tica software, version 13.3 (Tibco Software, Inc., increase in mean velocity by 80 cm/s, the differ‑ Palo Alto, California, United States). ence between mean velocity in the corresponding The study was approved by the Bioethics Com‑ segment of the MCA on the opposite side great‑ mittee of the Medical University of Silesia (NN­ er than 30 cm/s, and the ratio of mean velocity ‑6501‑90/I/15).­ All patients were informed about in the MCA to mean velocity in ICA on the ste‑ the aim and course of the study and provided in‑ notic side greater than or equal to 2. The anteri‑ formed consent. or cerebral artery stenosis greater than 50% was diagnosed based on the following criteria: a local Results The clinical characteristics of the study increase in mean velocity with associated turbu‑ patients are presented in Table 1. lence and Doppler spectrum broadening, systol‑ Stable CAD was diagnosed in 183 patients ic velocity greater than 120 cm/s, and a segmen‑ (75.9%), and unstable CAD in 58 (24.1%). Ad‑ tal increase in mean velocity by 80 cm/s. The pos‑ vanced coronary atherosclerotic lesions (steno‑ terior cerebral artery stenosis greater than 50% sis >50% in more than 2 sites) were found in 26 was diagnosed based on the following criteria: patients (10.8%), single coronary artery stenosis a local segmental increase in mean velocity by greater than 50% in 103 (42.7%), and coronary 30% in relation to the proximal and distal seg‑ artery stenosis in 2 sites in 112 (46.5%). ments with associated turbulence and Doppler Internal carotid artery stenosis was diagnosed spectrum broadening, a segmental increase in in 39 patients (16.2%). Symptoms of CNS isch‑ mean velocity by 50 cm/s in relation to the adja‑ emia were reported in the medical history of 25 cent vessel segments.26 patients (10.4%). Transcranial color Doppler imaging was per‑ There was no significant difference in the prev‑ formed by an experienced neurosonology spe‑ alence of ICA stenosis greater than 50% between cialist (PP, accredited with the International Cer‑ patients with stable CAD and those with unsta‑ tification in Neurosonology). ble CAD. Internal carotid artery stenosis greater

414 POLISH ARCHIVES OF INTERNAL MEDICINE 2020; 130 (5) TABLE 1 Clinical characteristics of the study patients

Parameter Overall (n = 241) Stable CAD (n = 183) Unstable CAD (n = 58) P valuea Age, y Mean (SD) 68.6 (8.8) 68.9 (8.8) 67.9 (9.1) 0.47 Median (range) 69 (41–89) 69 (41–89) 67 (46–85) Female sex 69 (28.6) 51 (27.9) 18 (31) 0.64 Arterial hypertension 200 (83) 152 (83.1) 48 (82.8) 0.95 Diabetes mellitus 83 (34.4) 65 (35.5) 18 (31) 0.53 BMI Mean (SD) 28 (2.7) 27.9 (2.7) 28.9 (2.6) 0.28 Median (range) 27.5 (22.7–39.3) 27.5 (22.7–39.3) 27.9 (22.9–35.9) Lipid disorders 172 (71.4) 134 (73.2) 38 (65.5) 0.26 History of stroke / TIA 25 (10.4) 18 (9.8) 7 (12.1) 0.63 Nicotinism 123 (51) 94 (51.4) 29 (50) 0.85 LVEF >50% 173 (71.8) 129 (70.5) 44 (75.9) 0.43

Data are presented as number (percentage) unless otherwise indicated. a Comparison between patients with stable CAD and those with unstable CAD

Abbreviations: BMI, body mass index; CAD, coronary artery disease; LVEF, left ventricular ejection fraction; TIA, transient ischemic attack than 50% was found in 28 patients (15.3%) with (cumulative OR, 37.94; 95% CI, 29.82–48.29; stable CAD and in 11 (19%) with unstable CAD P <0.001). (P = 0.51). In logistic regression analysis, none of the analyzed factors turned out to be a risk fac‑ Discussion The principal findings of this study, tor for ICA stenosis. regarding the prevalence of significant stenosis Atherosclerotic stenoses of the intracranial ar‑ of the carotid and cerebral arteries in patients teries were diagnosed in 20 patients (17.6%). Of with CAD, were as follows: 1) patients with sta‑ 114 patients included into the study, 89 (78%) ble CAD and those with unstable CAD do not dif‑ were diagnosed with stable CAD, and 25 (22%) fer in the prevalence of ICA and cerebral artery with unstable CAD. There was no difference in stenosis; and 2) advanced CAD is one of the risk the prevalence of atherosclerotic intracranial ar‑ factors for atherosclerosis of the cerebral arteries. tery stenosis between patients with stable CAD Atherosclerosis is a systemic disease. There‑ and those with unstable CAD. Intracranial artery fore, the probability of comorbid arterial steno‑ atherosclerosis was found in 16 patients (18%) ses in diverse vascular territories is high. How‑ with stable CAD and in 4 (16%) with unstable ever, the level of such coexistence differs among CAD (P = 0.54) (Figure 1). studies. Polyvascular atherosclerosis was found Atherosclerosis of the intracranial arteries in 15% to 46% of patients in various studies, and was more frequent in patients with ICA steno‑ in more than 16% in our study. Such a difference sis greater than 50% (8 patients [47.1%]) than in can be explained by different study methods used those without ICA stenosis (12 patients [12.4%]); by other authors.4,6,8,27-29 Different degrees of ste‑ P = 0.005 (Figure 2). In logistic regression analysis, nosis advancement in particular arteries can be the following risk factors for intracranial athero‑ observed in every patient. Multifocal localiza‑ sclerosis were identified: ICA stenosis (OR, 13.21; tion of atherosclerosis is associated with unfa‑ 95% CI, 5.93–41.89; P = 0.009) and advanced CAD vorable long‑term­ outcomes, and the cardiovas‑ (OR, 2.38; 95% CI, 1.13–4.09; P = 0.007) (Table 2). cular risk is independently related to the number Symptoms of previous CNS ischemia were of arterial territories affected by significant ath‑ found in 18 patients (9.8%) with stable CAD and erosclerosis.4,6,8,9,18 The clinical manifestations in 7 (12.1%) with unstable CAD (P = 0.63) (Figure 3). of atherosclerosis in 1 vascular bed is often asso‑ In all patients, symptoms of CNS ischemia due to ciated with symptoms of plaque destabilization large­‑vessel atherosclerosis were seen in the area in another vascular region, as factors predispos‑ of the anterior cerebral circulation (anterior ce‑ ing to plaque ruptures can be present both local‑ rebral artery, MCA, ICA). ly and systemically.3,5 Logistic regression analysis showed that Available studies suggest that 24% of patients the factors associated with an increased risk of with CAD have atherosclerotic lesions in at least CNS ischemic events were as follows: ICA stenosis 1 additional site within the carotid, renal, and / or greater than 50% on 1 side or both sides (OR, 1.74; lower limb arteries, and the severity of stenotic 95% CI, 1.01–3.16; P = 0.03), intracranial artery lesions in the coronary arteries is associated with stenosis (OR, 3.01; 95% CI, 1.66–5.57; P = 0.03) a greater number of lesions and greater severity (Table 3). The risk of CNS ischemic events in pa‑ of lesions in another area.30 tients with comorbid ICA stenosis and intracra‑ Although the coexistence of carotid or intra‑ nial artery atherosclerosis was particularly high cranial atherosclerosis and CAD was confirmed

ORIGINAL ARTICLE Carotid and cerebral artery atherosclerosis in patients with CAD 415 Figure 1 Intracranial 100 artery stenosis in patients 90 with coronary artery 82 84 disease (CAD) 80

70

60 % 50

40 Patients,

30 18 20 16

10

0 Stable CAD Unstable CAD

With intracranial artery stenosis Without intracranial artery stenosis

Figure 2 Intracranial 100 87.6 artery stenosis in patients 90 with internal carotid 80 artery stenosis 70

60 52.9 47.1 50 Patients, % 40 30

20 12.4 10 0 YesNo Internal carotid artery stenosis >50%

With intracranial artery stenosis Without intracranial artery stenosis

TABLE 2 Risk factors for intracranial artery stenosis—logistic regression analysis in more than 16% of patients, we did not find a significant difference in the prevalence of ICA Parameter OR 95% CI P value and intracranial artery stenoses between patients Age 1.04 0.96–1.07 0.21 with stable CAD and those with unstable CAD. Female sex 0.85 0.36–1.57 0.81 Symptoms of CAD do not depend solely on BMI >25 kg/m2 1.13 0.85–2.61 0.15 the severity of atherosclerotic lesions in the coro‑ nary vessels. The clinical presentation of CAD de‑ Arterial hypertension 0.38 0.03–1.77 0.36 pends on the site of particular lesions in the coro‑ Diabetes mellitus 1.81 0.56–5.87 0.26 nary vessels, the development of collateral circu‑ Nicotinism 1.87 0.96–3.72 0.26 lation, atheromatous plaque morphology, the pat‑ Lipid disorders 0.97 0.55–1.76 0.17 tern and speed of its progression, its destabiliza‑ Heart failure 1.27 0.42–3.84 0.66 tion risk, comorbidities affecting pain perception, Unstable CAD 0.75 0.37–1.42 0.95 and the therapy applied. Patients with unstable CAD could be a heterogeneous group including Advanced CAD 2.38 1.13–4.09 0.007 patients with a single critical atherosclerotic le‑ ICA stenosis >50% 13.21 5.93–41.89 0.009 sion or those with advanced multivessel disease. In our study group, advanced atherosclero‑ Abbreviations: ICA, internal carotid artery; OR, odds ratio; others, see Table 1 sis of the coronary arteries was a risk factor for atherosclerosis of the intracranial arteries. This finding was similar to that reported by other authors.31 Our study confirmed that there is an increased risk of atherosclerotic lesions of the intracranial

416 POLISH ARCHIVES OF INTERNAL MEDICINE 2020; 130 (5) Figure 3 Symptoms of 100 central nervous system 90.2 87.9 90 ischemia in patients with coronary artery disease 80 (CAD) 70

% 60 50 Patients, 40 30 20 9.8 12.1 10 0 Stable CAD Unstable CAD

With central nervous system ischemia Without central nervous system ischemia

TABLE 3 Risk factors for symptoms of central nervous system ischemia—logistic for myocardial infarction during, and even af‑ regression analysis ter, interventional treatment of the carotid ar‑ teries. Therefore, we must look for asymptom‑ P Parameter OR 95% CI value atic CAD in patients with carotid stenosis.14,15 Age 1.05 0.94–1.09 0.28 Musiałek et al14 proposed a novel carotid revas‑ Female sex 0.52 0.27–1.95 0.71 cularization decision­‑making model with coro‑ BMI >25 m/kg2 1.06 0.62–1.98 0.71 nary angiography before stenting to prevent cor‑ Arterial hypertension 0.25 0.02–1.67 0.17 onary complications in the perioperative period. The findings of our study support such a multi‑ Diabetes mellitus 0.49 0.13–1.97 0.56 vessel approach in patients with 1 clinical man‑ Nicotinism 0.4 0.20–1.13 0.34 ifestation of atherosclerosis. It would be rea‑ Lipid disorders 1.51 0.78–2.85 0.92 sonable to broaden the scope of diagnostic pro‑ Heart failure 1.22 0.71–2.16 0.96 cedures in patients with CAD in order to assess Unstable CAD 0.51 0.21–1.23 0.85 the condition of the carotid and cerebral arter‑ ies, which would optimize the therapeutic strat‑ Advanced CAD 1.04 0.29–3.73 0.94 egy and help prevent stroke. To know the site ICA stenosis >50% 1.74 1.01–3.16 0.03 and severity of atherosclerotic lesions is of im‑ Intracranial artery stenosis 3.01 1.66–5.57 0.03 portance to clinicians who qualify patients for interventional treatment of various vascular Abbreviations: see Tables 1 and 2 areas, as patients with multivessel disease gain fewer benefits.33 In clinical practice, our findings confirmed that extensive diagnostic work­‑up performed in pa‑ arteries in patients with ICA stenosis and a dis‑ tients with advanced CAD, including the exami‑ tinct cumulative risk of CNS ischemic events in nation of the intracranial arteries, can help iden‑ patients with both these pathologies. The pres‑ tify patients at risk of CNS ischemia. ence of such tandem stenoses is relevant not only because it influences the disease risk but also in Limitations Our study had the following limita‑ terms of selecting the most suitable intervention‑ tions: 1) lack of TCD imaging results in the entire al treatment method. study group (the examination was performed in From a clinical point of view, it is of key im‑ almost a half of the patients); including only sub‑ portance to determine the risk of CNS ischemic jects who underwent TCD imaging would affect events in patients with advanced CAD and carot‑ the sample size and lower the quality of performed id artery stenosis before CABG, as different treat‑ search for associations; 2) different numbers of ment strategies can be applied (simultaneous or patients with stable and unstable CAD (a smaller staged carotid endarterectomy / CABG or carotid number of those with unstable CAD)—it also lim‑ artery stenting / CABG).32 The risk of CNS isch‑ ited the difference in the number of TCD examina‑ emic events depends not only on the degree of tions in both groups. It did not affect the results, as ICA stenosis and the presence of bilateral ICA ste‑ the percentage of patients with unstable CAD was nosis but also, as found in our study, on the pres‑ similar, that is 24%, in the entire group and 22% ‑ence of intracranial artery stenosis. in patients who underwent TCD imaging. Te per On the other hand, asymptomatic CAD co‑ centage of patients undergoing TCD imaging was existing with carotid stenosis is a risk factor proportional in those with stable and unstable CAD

ORIGINAL ARTICLE Carotid and cerebral artery atherosclerosis in patients with CAD 417 (48% vs 43%); 3) only stroke and TIA were treated 6 Przewłocki T, Kabłak­‑Ziembicka A, Kozanecki A, et al. Polyvascular ex- tracoronary atherosclerotic disease in patients with coronary artery disease. as symptoms of CNS ischemia. We did not investi‑ Kardiol Pol. 2009; 67: 978-984. gate other possible manifestations of CNS ischemia 7 Iwakiri T, Yano Y, Sato Y, et al. Usefulness of carotid intima­‑media thick- (eg, impairment of cognitive functions) and “silent” ness measurement as an indicator of generalized atherosclerosis: findings from autopsy analysis. Atherosclerosis. 2012; 225: 359-362.  ischemic events revealed in neuroimaging studies. 8 Vlajinac HD, Marinkovic JM, Maksimovic MZ, et al. The prevalence of In accordance with the assumption and purpose polyvascular disease in patients with carotid artery disease and peripheral of the study, we analyzed acute symptomatic in‑ artery disease. Kardiol Pol. 2019; 77: 926-934.  cidents caused by atherosclerosis during the pre‑ 9 Musialek P, Montauk L, Saugnet A, et al. The cardio­‑vascular future of panvascular medicine: the basics. Kardiol Pol. 2019; 77: 899-901.  ceding 6 months (based on the definition adopt‑ 10 Steinvil A, Sadeh B, Bornstein NM, et al. Impact of carotid atheroscle- ed in guidelines by researchers and experts). It is rosis on the risk of adverse cardiac events in patients with and without cor- impossible to assess the onset of silent strokes; 4) onary disease. Stroke. 2014; 45: 2311-2317.  lack of subanalysis of patients divided according to 11 Nonin S, Iwata S, Sugioka K, et al. Plaque surface irregularity and cal- cification length within carotid plaque predict secondary events in patients the site of atherosclerotic lesions in the coronary with coronary artery disease. Atherosclerosis. 2017; 256: 29-34.  vessels and the number of affected coronary ves‑ 12 Gacoń J, Przewlocki T, Podolec J, et al. The role of serial carotid intima­ sels. It did not affect the results of the study, al‑ ‑media thickness assessment as a surrogate marker of atherosclerosis con- trol in patients with recent myocardial infarction. Postepy Kardiol Interwen- though such an analysis would increase its value; cyjnej. 2019; 15: 74-80.  5) lack of multivariable logistic regression analy‑ 13 Gacoń J, Przewłocki T, Podolec J, et al. Prospective study on the prog- sis to identify potential independent risk factors nostic value of repeated carotid intima­‑media thickness assessment in pa- tients with coronary and extra coronary steno­‑occlusive arterial disease. Pol for intracranial artery stenosis and CNS ischemia Arch Intern Med. 2019; 131: 12-21.  syndrome. Undoubtedly, this analysis would en‑ 14 Musialek P, Mazurek A, Trystula M, et al. Novel PARADIGM in carot- hance the value of our study. id revascularization: prospective evaluation of All­‑comer peRcutaneous cA- rotiD revascularization in symptomatic and Increased­‑risk asymptomatic ca- rotid artery stenosis using CGuardTM MicroNet­‑covered embolic prevention Conclusions No differences between the preva‑ stent system. EuroIntervention. 2016; 12: e658­‑e670.  lence of atherosclerosis of the carotid and cere‑ 15 Pieniazek P, Musialek P, Kablak­‑Ziembicka A, et al. Carotid artery stent- ing with patient- and lesion­‑tailored selection of the neuroprotection sys- bral arteries between patients with stable and un‑ tem and stent type: early and 5­‑year results from a prospective academ- stable CAD were found in this study. ic registry of 535 consecutive procedures (TARGET­‑CAS). J Endovasc Ther. 2008; 15: 249-262.  A total of 16% to 20% of study patients with un‑ 16 Kim MJ, Song H, Oh SY, et al. Assessment of stroke and concomi- stable CAD had atherosclerotic stenosis of the ca‑ tant cerebrovascular disease with heart disease requires invasive treatment: rotid or cerebral arteries. However, in the major‑ analysis of 249 consecutive patients with heart disease. Thorac Cardiovasc Surg. 2014; 62: 317-323.  ity of patients, stenosis was asymptomatic. 17 Amarenco P, Lavallée PC, Labreuche J, et al. Coronary artery disease Advanced CAD is one of the risk factors for and risk of major vascular events after cerebral infarction. Stroke. 2013; 44: hemodynamically significant cerebral artery 1505-1511.  stenosis. 18 Musiałek P, Grunwald IQ. How asymptomatic is “asymptomatic” carot- id stenosis. Pol Arch Intern Med. 2017; 127: 718-719.  19 Tegeler CH, Crutchfield K, Katsnelson M, et al. Transcranial Dop- Article information pler velocities in a large, healthy population. J Neuroimaging. 2013; 23: 466-472.  Contribution statement PP collected data, performed analysis, and drafted the paper. AL­‑B conceived the study concept, designed the analy- 20 Poi MJ, Echeverria A, Lin PH. Contemporary management of patients sis, and supervised the study. AW­‑W analyzed data and performed literature with concomitant coronary and carotid artery disease. World J Surg. 2018; search. MK contributed to study planning and data collection. All authors ed- 42: 272-282.  ited and approved the final version of the manuscript. 21 Thygesen K, Alpert JS, Jaffe AS, et al; Executive Group on behalf of Conflict of interest None declared. the Joint European Society of Cardiology (ESC)/American College of Car- diology (ACC)/American Heart Association (AHA)/World Heart Federa- Open access This is an Open Access article distributed under the terms tion (WHF) Task Force for the Universal Definition of Myocardial Infarction. of the Creative Commons Attribution­‑NonCommercial­‑ShareAlike 4.0 Inter- Fourth universal definition of myocardial infarction (2018). Circulation. 2018; national License (CC BY­‑NC­‑SA 4.0), allowing third parties to copy and re- 138: e618­‑e651. distribute the material in any medium or format and to remix, transform, and build upon the material, provided the original work is properly cited, distrib- 22 Ponikowski P, Voors A, Anker S, et al. ESC Guidelines for the diagno- uted under the same license, and used for noncommercial purposes only. For sis and treatment of acute and chronic heart failure. Kardiol Pol. 2016; 74: commercial use, please contact the journal office at [email protected]. 1037-1147. How to cite Puz P, Lasek­‑Bal A, Warsz­‑Wianecka A, Kaźmierski M. Prev- 23 Sacco R, Kasner S, Broderick J, et al. An updated definition of stroke alence of atherosclerotic stenosis of the carotid and cerebral arteries in pa- for the 21st century. Stroke. 2013; 44: 2064-2089.  tients with stable or unstable coronary artery disease. Pol Arch Intern Med. 24 Smith S, Feldman T, Hirshfeld J, et al. ACC/AHA/SCAI 2005 guide- 2020; 412-419. doi:10.20452/pamw.15330 lines update for percutaneous coronary intervention. Circulation. 2006; 113: 166-286.  References 25 von Reutern GM, Goertler MW, Bornstein NM, et al. Grading carotid stenosis using ultrasonic methods. Stroke. 2012; 43: 916-921.  1 Gepner AD, Young R, Delaney JA, et al. Comparison of coronary artery 26 Zhao L, Barlinn K, Sharma VK, et al. Velocity criteria for intracranial ste- calcium presence, carotid plaque presence, and carotid intima­‑media thick- nosis revisited: an international multicenter study of transcranial Doppler and ness for cardiovascular disease prediction in the Multi­‑Ethnic Study of Ath- digital subtraction angiography. Stroke. 2011; 42: 3429-3434.  erosclerosis. Circ Cardiovasc Imaging. 2015; 8: e002262.  27 Vranic H, Hadzimehmedagic A, Haxibeqiri­‑Karabdic I, et al. Critical ca- 2 Sigala F, Oikonomou E, Antonopoulos AS, et al. Coronary versus carotid rotid artery stenosis in coronary and non­‑coronary patients – frequency of artery plaques. Similarities and differences regarding biomarkers morpholo- risk factors. Med Arch. 2017; 71: 110-114.  gy and prognosis. Curr Opin Pharmacol. 2018; 39: 9-18.  28 Kazum S, Eisen A, Lev EI, et al. Prevalence of carotid artery disease 3 Schneider A, Gawęcka J, Minczykowski A, et al. Arterial structure and among ambulatory patients with coronary artery disease. Isr Med Assoc function in patients with acute coronary syndrome after 1­‑year treatment. J. 2016; 18: 100-103. Pol Arch Intern Med. 2017: 127: 184-189.  29 LeBlanc S, Bibeau K, Bertrand OF, et al. Carotid versus coronary athero- 4 Bhatt D, Steg P, Ohman E, et al. International prevalence, recognition and sclerosis burdens in acute compared with chronic symptomatic coronary ar- treatment of cardiovascular risk factors in outpatients with atherothrombo- tery disease. Can J Physiol Pharmacol. 2017; 95: 878-887.  sis. JAMA. 2006; 295: 180-189.  30 Imori Y, Akasaka T, Ochiai T, et al. Co­‑existence of carotid artery dis- 5 Musialek P, Tracz W, Tekieli L, et al. Multimarker approach in discrimi- ease, renal artery stenosis, and lower extremity peripheral arterial disease nating patients with symptomatic and asymptomatic atherosclerotic carot- in patients with coronary artery disease. Am J Cardiol. 2014; 113: 30-35.  id artery stenosis. J Clin Neurol. 2013; 9: 165-175. 

418 POLISH ARCHIVES OF INTERNAL MEDICINE 2020; 130 (5) 31 Gibson AO, Blaha MJ, Arnan MK, et al. Coronary artery calcium and in- cident cerebrovascular events in an asymptomatic cohort. The MESA Study. JACC Cardiovasc Imaging. 2014; 7: 1108-1115.  32 Dzierwa K, Pieniazek P, Musialek P, et al. Treatment strategies in severe symptomatic carotid and coronary artery disease. Med Sci Monit. 2011; 17: 191-197.  33 Srinivasan K, Ravikumar S, Chandra SR, et al. Cerebral and coronary vasculature in disease associations and dissociations in the South Indian population. J Neurosci Rural Pract. 2017; 8: 352-356. 

ORIGINAL ARTICLE Carotid and cerebral artery atherosclerosis in patients with CAD 419