26 August 2013: Clinical Research
Arterial distensibility in patients with ruptured and unruptured intracranial aneurysms: Is it a predisposing factor for rupture risk?
Abdurrahim Dusak ABCDEFG , Kaan Kamasak ABCDEFG , Cemil Goya ABCDEFG , Mehmet E. Adin ABCDEFG , Mehmet A. Elbey ABCDEFG , Aslan Bilici ABCDEFG
DOI: 10.12659/MSM.889032
Med Sci Monit 2013; 19:703-709
Abstract
BACKGROUND: A risk factor assessment that reliably predicts whether patients are predisposed to intracranial aneurysm (IA) rupture has yet to be formulated. As such, the clinical management of unruptured IA remains unclear. Our aim was to determine whether impaired arterial distensibility and hypertrophic remodeling might be indicators of risk for IA rupture.
MATERIAL AND METHODS: The study population (n=49) was selected from consecutive admissions for either unruptured IA (n=23) or ruptured IA (n=26) from January to December 2010. Hemodynamic measures were taken from every patient, including systolic and diastolic blood pressure using a sphygmomanometer. Unruptured IA and ruptured IA characteristics, including aneurysmal shape, size, angle, aspect ratio, and bottleneck factor, were measured and calculated from transverse brain CT angiography images. With ultrasound, the right common carotid artery intima-media thickness was measured, as well as the lumen diameter during systole and diastole. Arterial wall strain, distensibility, stiffness index, and elastic modulus were calculated and compared between patients with unruptured IAs and ruptured IAs. A p-value less than 0.05 was considered statistically significant.
RESULTS: General demographic data did not differ between patients with unruptured IAs and ruptured IAs. Greater mean intima-media thickness (p=0.013), mean stiffness index (p=0.044), and mean elastic modulus (p=0.026) were observed for patients with ruptured IAs. Moreover, mean strain (p=0.013) and mean distensibility (p=0.024) were decreased in patients with ruptured IAs.
CONCLUSIONS: Patients with ruptured IAs demonstrated decreased arterial distensibility and increased intima-media thickness at the level of the carotid arteries. By measuring these parameters via ultrasound, it may be possible to predict whether patients with existing IAs might rupture and hemorrhage into the subarachnoid space.
Keywords: Cerebral Angiography, carotid intima-media thickness, Cerebral Arteries - ultrasonography, elastic modulus, Hemodynamics, Intracranial Aneurysm - pathology, Risk Factors, Turkey - epidemiology, Vascular Stiffness
Background
Population-based and autopsy studies report that the incidence of intracranial aneurysms (IAs) may be as high as 10% and peaks in the sixth decade of life. Females with a family history of IA are especially at risk [1–3]. Subarachnoid hemorrhages (SAHs) due to ruptured IAs account for 10% and 40% of deaths before hospitalization and after a 1-month hospital stay, respectively [1,4]. More than 35% of patients with SAH develop major neurological deficits preceding hospital discharge, even if they demonstrated favorable Glasgow Coma Scores [5–8]. Although it is easier to detect unruptured IAs with various imaging modalities, it is difficult to predict if or when they will rupture, which poses a dilemma for both patients and physicians [9–11].
Acquired and hereditary risk factors contribute to the multifactorial etiology of unruptured IA, including sex, hypertension, atherosclerosis, alcohol consumption, and smoking [12]. Parameters utilized for rupture assessment include aneurysm size, shape, and location, in addition to angle and flow hemodynamics [13–18]. Cumulative arterial wall deterioration as a result of constant remodeling characterized by degeneration and inflammatory cell infiltration lead to IA rupture and subsequent SAH [19,20]. Altered arterial wall elastic properties and hypertrophic remodeling might predispose IAs to rupture [21–23]. Arterial wall elasticity and intima-media thickness can be estimated non-invasively via ultrasound to indirectly evaluate arterial wall strength [24–26]. We hypothesized that hypertrophic intimal remodeling and impaired elastic properties detected in the right carotid artery might co-occur with IA rupture and thus may predict an impending IA rupture.
Material and Methods
BLOOD PRESSURE MEASUREMENT:
Maximum blood pressure (BPmax) was the systolic BP and minimum blood pressure (BPmin) was the diastolic BP. Blood pressure was measured from the right brachial artery with a sphygmomanometer (Omron HEM 705CP, Colson) after a 10-minute resting period. Heart rate and BP were measured just before ultrasound examination, and within the first 3 days following IA rupture to avoid falsely elevated BPs from SAH-induced vasospasm.
ULTRASOUND EXAMINATION:
Ultrasound examinations were performed for patients with ruptured IAs within the first 3 days of rupture to avoid SAH induced vasospasm and following DSA. Specifically, the Aplio XG scanner equipped with a 10 MHz linear array transducer (Toshiba Medical Systems, Tokyo, Japan) was used. A pulse repetition frequency of 3 kHz with an automatic cutoff filter ranging from 1 to 3 kHz was utilized. M-mode ultrasound was performed at a speed of 50 mm/sec.
The right common carotid artery (CCA) was examined while the patient assumed the supine position with slight head elevation. The transducer was positioned parallel to the CCA such that the lumen’s diameter was maximized in the longitudinal plane. Maximum (Dmax) and minimum (Dmin) internal lumen diameters were measured at 1 to 2 cm proximal to the CCA bifurcation in magnified M-mode during systole and diastole. Intima-media thickness measurements were taken at this same location, but were derived in B-mode.
ELASTIC PROPERTIES:
Arterial elastic properties, including distensibility, strain, stiffness index, and elastic modulus, were measured to determine the stress on the right CCA wall during diastole and systole [27,28]. Strain was defined as the percent change in CCA artery lumen diameter during systole and diastole. The following calculations were performed to determine the aforementioned measures:
STATISTICS:
Statistical Package for the Social Sciences for Windows (SPSS ver. 18, Chicago, IL, USA) software was used to analyze all data. Descriptive parameters were expressed as the mean ± the standard deviation or via percentages. Variations between groups were compared with the Mann-Whitney U test. Correlation analyses were performed with the Spearman test. A
Results
A comparison between unruptured IA and ruptured IA groups in terms of demographics and aneurysm characteristics is provided in Table 1. There were no differences in age, sex, and heart rate between groups. Patients with unruptured IA had a mean age of 47.1±12.0 years, with ages that ranged from 26 to 68 years. Patients with ruptured IA had a mean age of 48.6±11.5 years, ranging from 31 to 67 years. Unruptured IA and ruptured IA characteristics included shape, size, angle, aspect ratio, and bottleneck factor. For the entire study population, unruptured IA and ruptured IA locations included the internal carotid artery (ICA) in 14% of cases, the anterior communicating artery (ACoA) in 20% of cases, the middle cerebral artery (MCA) in 41% of cases, and the vertebral and basilar arteries (V-B) in 25% of of cases (Figures 1 and 2).
The unruptured IA group exhibited a decreased mean CCA intima-media thickness at 0.52±0.12 cm
Discussion
LIMITATIONS:
The study sample size was small, lacked a healthy control group, and no long-term follow-up was performed. However, all study subjects ultimately received surgical or interventional treatment.
Conclusions and Future Perspectives
Our findings demonstrate that patients with ruptured IAs exhibit impaired CCA wall distensibility and increased intima-media thickness, which suggests hypertrophic remodeling. Thus, determining CCA distensibility and intima-media thickness might be useful in determining whether an IA may rupture in the future. To better determine whether CCA elastic properties predispose patients to IA rupture, a larger prospective study design might be more informative, as the development of rupture may be correlated with changes in these factors over time. It is our hope that developing a set of predictive parameters for IA rupture will guide clinical management so to prevent complications such as subarachnoid hemorrhage.
References
1. Rinkel GJ, Djibuti M, Algra A, van Gijn J, Prevalence and risk of rupture of intracranial aneurysms: a systematic review: Stroke, 1998; 29; 251-56, pmid: 9445359
2. Loewenstein JE, Gayle SC, Duffis EJ, The natural history and treatment options for unruptured intracranial aneurysms: Int J Vasc Med, 2012; 2012; 898052, pmid: 22500236
3. Oh SY, Kwon JT, Park YS, Clinical features of acute subdural hematomas caused by ruptured intracranial aneurysms: J Korean Neurosurg Soc, 2011; 50; 6-10, pmid: 21892397
4. You SH, Kong DS, Kim JS, Characteristic features of unruptured intracranial aneurysms: predictive risk factors for aneurysm rupture: J Neurol Neurosurg Psychiatry, 2010; 81; 479-84, pmid: 19726404
5. Beck J, Rohde S, Berkefeld J, Size and location of ruptured and unruptured intracranial aneurysms measured by 3-dimensional rotational angiography: Surg Neurol, 2006; 65; 18-25, pmid: 16378842
6. Terzidou C, Dalianis G, Zacharaki F, Ocular symptomatology, management, and clinical outcome of a giant intracranial aneurysm: Case Report Med, 2012; 2012; 643965
7. White PM, The detection and management of unruptured intracranial aneurysms: Brain, 2000; 123; 205-21, pmid: 10648430
8. Beck J, Rohde S, el Beltagy M, Difference in configuration of ruptured and unruptured intracranial aneurysms determined by biplanar digital subtraction angiography: Acta Neurochir, 2003; 145; 861-65, pmid: 14577007
9. Yoshimoto Y, Wakai S, Cost-effectiveness analysis of screening for asymptomatic, unruptured intracranial aneurysms. A mathematical model: Stroke, 1999; 30; 1621-27, pmid: 10436111
10. Wanke I, Doerfler A, Dietrich U, Endovascular treatment of unruptured intracranial aneurysms: AJNR Am J Neuroradiol, 2002; 23; 756-61, pmid: 12006272
11. Costalat V, Sanchez M, Ambard D, Biomechanical wall properties of human intracranial aneurysms resected following surgical clipping: J Biomech, 2011; 44; 2685-91, pmid: 21924427
12. Luukkonen TM, Pöyhönen M, Palotie A, A balanced translocation truncates Neurotrimin in a family with intracranial and thoracic aortic aneurysm: J Med Genet, 2012; 49; 621-29, pmid: 23054244
13. Amenta PS, Yadla S, Campbell PG, Analysis of nonmodifiable risk factors for intracranial aneurysm rupture in a large, retrospective cohort: Neurosurgery, 2012; 70; 693-99, pmid: 21904261
14. Nader-Sepahi A, Casimiro M, Sen J, Kitchen ND, Is aspect ratio a reliable predictor of intracranial aneurysm rupture?: Neurosurgery, 2004; 54; 1343-47, pmid: 15157290
15. Clarke G, Mendelow AD, Mitchell P, Predicting the risk of rupture of intracranial aneurysms based on anatomical location: Acta Neurochir, 2005; 147; 259-63, pmid: 15662565
16. Lall RR, Eddleman CS, Bendok BR, Batjer HH, Unruptured intracranial aneurysms and the assessment of rupture risk based on anatomical and morphological factors: sifting through the sands of data: Neurosurg Focus, 2009; 26; E2, pmid: 19408998
17. Hoh BL, Sistrom CL, Firment CS, Bottleneck factor and height-width ratio: association with ruptured aneurysms in patients with multiple cerebral aneurysms: Neurosurgery, 2007; 61; 716-22, pmid: 17986932
18. Raij L, Gonzalez-Ochoa AM, Vascular compliance in blood pressure: Curr Opin Nephrol Hypertens, 2011; 20; 457-64, pmid: 21738031
19. Jayaraman T, Paget A, Shin YS, TNF-alpha-mediated inflammation in cerebral aneurysms: a potential link to growth and rupture: Vasc Health Risk Manag, 2008; 4; 805-17, pmid: 19065997
20. Tulamo R, Frösen J, Junnikkala S, Complement activation associates with saccular cerebral artery aneurysm wall degeneration and rupture: Neurosurgery, 2006; 59; 1069-76, pmid: 17016232
21. Sakata N, Takebayashi S, Shimizu K, A case of segmental mediolytic arteriopathy involving both intracranial and intraabdominal arteries: Pathol Res Pract, 2002; 198; 493-97, pmid: 12234069
22. Giannarelli C, Bianchini E, Bruno RM, Local carotid stiffness and intimamedia thickness assessment by a novel ultrasound-based system in essential hypertension: Atherosclerosis, 2012; 223; 372-77, pmid: 22727194
23. Rogowicz-Frontczak A, Araszkiewicz A, Pilacinski S, Carotid intima-media thickness and arterial stiffness in type 1 diabetic patients with and without microangiopathy: Arch Med Sci, 2012; 8; 484-90, pmid: 22852004
24. Bjällmark A, Lind B, Peolsson M, Ultrasonographic strain imaging is superior to conventional non-invasive measures of vascular stiffness in the detection of age-dependent differences in the mechanical properties of the common carotid artery: Eur J Echocardiogr, 2010; 11; 630-36, pmid: 20338957
25. Maltete D, Bellien J, Cabrejo L, Hypertrophic remodeling and increased arterial stiffness in patients with intracranial aneurysms: Atherosclerosis, 2010; 211; 486-91, pmid: 20452592
26. Karwowski W, Naumnik B, Szczepański M, Myśliwiec M, The mechanism of vascular calcification – a systematic review: Med Sci Monit, 2012; 18(1); RA1-11, pmid: 22207127
27. Selzer RH, Mack WJ, Lee PL, Improved common carotid elasticity and intima-media thickness measurements from computer analysis of sequential ultrasound frames: Atherosclerosis, 2001; 154; 185-93, pmid: 11137099
28. van‘t Veer M, Buth J, Merkx M, Biomechanical properties of abdominal aortic aneurysms assessed by simultaneously measured pressure and volume changes in humans: J Vasc Surg, 2008; 48; 1401-7, pmid: 18771885
29. Godia EC, Madhok R, Pittman J, Carotid artery distensibility: a reliability study: J Ultrasound Med, 2007; 26; 1157-65, pmid: 17715309
30. Tóth M, Nádasy GL, Nyár I, Are there systemic changes in the arterial biomechanics of intracranial aneurysm patients?: Pflugers Arch, 2000; 439; 573-78, pmid: 10764217
31. Greene ER, Lanphere KR, Sharrar J, Roldan CA, Arterial distensibility in systemic lupus erythematosus: Med Biol Soc, 2009; 2009; 1109-12
32. Boutouyrie P, Germain DP, Fiessinger JN, Increased carotid wall stress in vascular Ehlers-Danlos syndrome: Circulation, 2004; 109; 1530-35, pmid: 15007000
33. Groth M, Forkert ND, Buhk JH, Comparison of 3D computer-aided with manual cerebral aneurysm measurements in different imaging modalities: Neuroradiology, 2013; 55; 171-78, pmid: 23007858
34. Rohde S, Lahmann K, Beck J, Fourier analysis of intracranial aneurysms: towards an objective and quantitative evaluation of the shape of aneurysms: Neuroradiology, 2005; 47; 121-26, pmid: 15688203
35. Foutrakis GN, Yonas H, Sclabassi RJ, Saccular aneurysm formation in curved and bifurcating arteries: AJNR Am J Neuroradiol, 1999; 20; 1309-17, pmid: 10472991
36. Vlak MH, Rinkel GJ, Greebe P, Trigger factors for rupture of intracranial aneurysms in relation to patient and aneurysm characteristics: J Neurol, 2012; 259; 1298-302, pmid: 22186848
37. Pierot L, Barbe C, Spelle L, Endovascular treatment of very small unruptured aneurysms: rate of procedural complications, clinical outcome, and anatomical results: Stroke, 2010; 41; 2855-59, pmid: 21030707
38. Evrengul H, Tanriverdi H, Kilic ID, Aortic stiffness and flow-mediated dilatation in normotensive offspring of parents with hypertension: Cardiol Young, 2012; 22; 451-56, pmid: 22348859
39. van Laake LW, Vainas T, Dammers R, Systemic dilation diathesis in patients with abdominal aortic aneurysms: a role for matrix metalloproteinase-9?: Eur J Vasc Endovasc Surg, 2005; 29; 371-77, pmid: 15749037
40. Wilson KA, Lee AJ, Lee AJ, The relationship between aortic wall distensibility and rupture of infrarenal abdominal aortic aneurysm: J Vasc Surg, 2003; 37; 112-17, pmid: 12514586
41. Wilson KA, Lindholt JS, Hoskins PR, The relationship between abdominal aortic aneurysm distensibility and serum markers of elastin and collagen metabolism: Eur J Vasc Endovasc Surg, 2001; 21; 175-78, pmid: 11237793
42. Gaál EI, Salo P, Kristiansson K, Intracranial aneurysm risk locus 5q23.2 is associated with elevated systolic blood pressure: PLoS Genet, 2012; 8; e1002563, pmid: 22438818
43. Zapolski T, Wysokiński A, Left atrium volume index is influenced by aortic stiffness and central pulse pressure in type 2 diabetes mellitus patients: a hemodynamic and echocardiographic study: Med Sci Monit, 2013; 19; 153-64, pmid: 23458774
44. Orlova IA, Nuraliev EY, Yarovaya EB, Ageev FT, Prognostic value of changes in arterial stiffness in men with coronary artery disease: Vasc Health Risk Manag, 2010; 6; 1015-21, pmid: 21127698
45. van de Putte EM, Uiterwaal CS, Bots ML, Is chronic fatigue syndrome a connective tissue disorder? A cross-sectional study in adolescents: Pediatrics, 2005; 115; 415-22
46. Mizuguchi Y, Oishi Y, Miyoshi H, Impact of statin therapy on left ventricular function and carotid arterial stiffness in patients with hypercholesterolemia: Circ J, 2008; 72; 538-44, pmid: 18362422
47. Celik T, Iyisoy A, Kursaklioglu H, Impaired aortic elastic properties in young patients with prehypertension: Blood Press Monit, 2006; 11; 251-55, pmid: 16932034
48. Seth S, Goyal NK, Jagia P, Carotid intima-medial thickness as a marker of disease activity in Takayasu’s arteritis: Int J Cardiol, 2006; 108; 385-90, pmid: 15970340
49. Mattace-Raso FU, van den Meiracker AH, Bos WJ, Arterial stiffness, cardiovagal baroreflex sensitivity and postural blood pressure changes in older adults: the Rotterdam Study: J Hypertens, 2007; 25; 1421-26, pmid: 17563564
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