Health Sciences University, Kanuni Research and Training Hospital, Department of Cardiovascular Surgery Trabzon, Turkey

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1 J Turgut Ozl Med Cent DOI: /jtomc ;25(1):1-6 ORIGINAL ARTICLE The role of vsculr elstogrphy nd crotid rtery intim medi thickness methods in the determintion of non-syndromic scending thorcic ortic neurysm Dogus Hemsinli 1, Htice Ayc At Korkmz 2, Gye Bki 2, Erkn Vurlkn 3, Sfiye Tub Kpln 4, Selim Kul 5, Inn Utku Turkmen 6 1 Helth Sciences University, Knuni Reserch nd Trining Hospitl, Deprtment of Crdiovsculr Surgery Trbzon, Turkey 2 Helth Sciences University, Knuni Reserch nd Trining Hospitl, Deprtment of Rdiology, Trbzon, Turkey 3 Helth Sciences University, Knuni Reserch nd Trining Hospitl, Deprtment of Otolryngology, Trbzon, Turkey 4 Helth Sciences University, Knuni Reserch nd Trining Hospitl, Deprtment of Internl Medicine, Trbzon, Turkey 5 Helth Sciences University, Ahi Evrn Reserch nd Trining Hospitl, Deprtment of Crdiology, Trbzon, Turkey 6 TED University, Deprtment of Bsic Sciences, Ankr, Turkey Abstrct Aim: The role of therosclerosis in the pthogenesis of scending thorcic ortic neurysms is still uncertin. Ultrsonic elstogrphy is new dignostic method, the use of which hs diversified considerbly in recent yers. An increse in intim medi thickness in the crotid rteries is n erly finding of therosclerosis. Our purpose ws to investigte the effect of therosclerosis in the development of scending thorcic ortic neurysms nd to be ble to recommend non-invsive nd inexpensive scnning method iming t erly dignosis. Mteril nd Methods: Thirty-three ptients with scending thorcic ortic neurysms (TAA group) nd 40 ptients with norml mesurement (control group) vlues were included in the study. The crotid rtery intim medi thicknessof crotid rteries were mesured using B mode ultrsonogrphy. Elstogrphic exmintion of the intim-medi ws then performed. Results: Body mss index, pst smoking sttus, hypertension, presence of coronry rtery disese nd hyperlipidemi were higher in the TAA group thn in the control group (p<0.05). No significnt difference ws determined between these two groups ultrsonic elstogrphy or intim medi thickness in the crotid rteries vlues (p<0.05). Conclusions: Our findings suggest tht the effect of therosclerosis in the pthogenesis of scending thorcic ortic neurysms is limited. Vsculr ultrsonic elstogrphy nd intim medi thickness determintion in the crotid rteries pper not to be effective in the evlution of scending thorcic ortic neurysms. Keywords: Aneurysm; Atherosclerosis; Intim-Medi Thickness; Vsculr Elstogrphy. INTRODUCTION Ascending thorcic ortic neurysms (TAA) generlly produce no clinicl findings before cusing crdiovsculr emergencies, such s dissection or rupture. The prehospitl mortlity rte of these emergency conditions is 40%, incresing by 1% for every hour without surgicl intervention (1,2). Despite dvnces in surgicl techniques nd periopertive cre conditions, the opertive mortlity rte is 15-30% (2). The silent course of the disese nd the lck of n effective screening method for erly dignosis mke it difficult to determine the true incidence of TAA nd to prevent cute events with ttendnt high mortlity (3,4). Dimeter mesurement lone is insufficient in the prediction of emergency events, since dissection is frequently reported in ptients with men ortic dimeter <5.0 cm, hence better mrkers re needed for more ccurte surgicl timing (1,4). Atherosclerosis plys n importnt role in the pthogenesis of numerous vsculr diseses. Despite the informtion obtined to dte, the pthophysiology of TAA nd the effect of therosclerosis on the development of neurysm re still not well understood (2,4,5). Popultion-bsed studies hve shown correltion between the severity of therosclerosis in n rteril region nd involvement of other rteries (6,8). Methods developed for the erly identifiction of rteril diseses in helthy-ppering individuls hve therefore focused on the peripherl rteries, nd prticulrly the crotid rteries (8). An increse in crotid rtery intim medi thickness (CIMT) is regrded s n erly finding of generlized therosclerosis (3,6,7). Received: Accepted: Corresponding Author: Dogus Hemsinli, Helth Sciences University, Knuni Reserch nd Trining Hospitl, Deprtment of Crdiovsculr Surgery Trbzon, Turkey, E-mil: dogushem@hotmil.com 1

2 Although CIMT screening is not recommended for risk ssessment in crdiovsculr diseses in the most recent Europen Society of Crdiology (ESC) guideline, CIMT investigtion my nevertheless provide n opportunity for clinicins to ssess subclinicl therosclerosis in the vessel wll (8,10). Previous studies hve investigted the reltion between incresed CIMT nd vrious vsculr diseses, such s coronry rtery disese (CAD), peripherl rtery disese (PAD), intrcrnil rteril neurysms, nd bdominl ortic neurysms (AAA) (9,10,11,12). However, the number of studies concerning TAA is very smll (13). Ultrsound elstogrphy (EUS), novel dignostic technique, ws developed in recent yers on the bsis of the fct tht pthologicl processes lter tissue elsticity (14). EUS is used in the differentil dignosis of brest nd thyroid lesions, in the differentition of benign nd mlignnt lymph nodes, in the stging of heptic fibrosis, in the chrcteriztion of focl pncretic lesions, nd to differentite ctive inflmmtion nd in bowel wll lesions nd fibrotic stenosis (15-20). Our investigtion of the literture showed tht studies of EUS in the context of therosclerotic vsculr diseses hve focused on unstble plques in the crotid rteries nd on determining the risk of stroke (21,22). However, we encountered no EUS studies investigting the systemic vsculr effects of therosclerosis. This study investigted vsculr EUS nd CIMT vlues in ptients with TAA. Our im ws to investigte the effect of therosclerosis on the development of TAA nd to be ble to recommend non-invsive nd inexpensive screening method iming t erly dignosis. MATERIAL nd METHODS Study popultion: The study ws crried out with the pprovl of the locl ethicl committee ( ), nd informed consent ws obtined from the prticipnts. The records of ll ptients undergoing thorcobdominl computerized tomogrphy (CT) with contrst enhncement t the Knuni Eduction nd Reserch Hospitl, Turkey, between October 2015 nd July 2016 were exmined. Aortic dimeter mesurements were performed from the scending, rch nd descending thorcic ort nd bdominl segments. Aortic dimeter 40 mm ws regrded s neurysm. Ptients demogrphic dt, body mss index (BMI) vlues, hypertension (HT) (blood pressure 140/90 mm Hg in non-dibetic subjects, nd 130/80 mm Hg in dibetics or subjects receiving ntihypertensive therpy), hyperlipidemi (subjects with low density lipoprotein 135 mg/di or receiving lipid lowering therpy), dibetes mellitus (DM) (fsting plsm glucose 126 mg/di, nonfsting plsm glucose 200 mg/dl or subjects receiving ntidibetic drugs), presence of CAD nd cerebrovsculr disese (CVD), smoking sttus nd dt concerning drugs used were recorded. Ptients with diseses leding to structurl impirment in the vsculr wll, such s Mrfn nd Ehler Dnlos syndromes, with chronic renl filure (serum cretinine 2.0 mg/dl or receiving dilysis), bicuspid ortic vlve, dvnced regurgittion in the ortic nd/or mitrl vlve, PAD, rcus ort or descending thorcic neurysm, AAA, history of crdic nd/or ortic surgery, endovsculr intervention or neck surgery, therosclerotic plque in the crotid rtery lumen were excluded from the study. Forty ptients with mesurement vlues within norml limits were enrolled in the control group nd 33 ptients with scending thorcic ortic neurysm in the TAA group. Sonomorphologicl exmintion of both crotid rteries nd their brnches of the 73 ptients included in the study ws performed with B mode ultrsonogrphy (US), nd CIMTs were mesured. Elstogrphic exmintion of the intim medi ws subsequently performed. Rdiologicl evlution: An Aplio 500 US mchine (Toshib Medicl Systems, Co, Ltd, Ottowr, Jpn) with liner MHz trnsducers nd elstogrphy softwre ws used. All exmintions were performed by one of two rdiologists (AAK or GB) with more thn 10 yers experience of crotid Doppler sonogrphic imging nd blinded to clinicl findings, lbortory results, erly clinicl suspected differentil dignosis of neurysms nd ptients finl dignoses. Ultrsound imging: US exmintion in this study strted with gry scle imging. The ptient ws plced in supine nd slightly extended position over specil wheeled bed. B mode sonogrphic evlution strted with the bilterl common crotid rteries (CCA). Following stndrd trnsverse nd longitudinl evlution of the crotid system, we performed Doppler sonogrphic imging of the crotidl system. The right common crotid rtery ws exmined with the hed turned wy from the side of interest, nd the trnsducer ws replced so tht the ner nd fr wlls of the common crotid rtery were prllel to the trnsducer foot print, nd the lumen mesurement ws mximized in the longitudinl plne. A region 1 cm proximl to the crotid bifurction ws identified, nd the IMT of the fr wll ws evluted. The IMT mesurement ws tken from four contiguous sites t 1-mm intervls, nd the men of the four mesurements ws used for nlyses (Figur 1). Loclized structures nrrowing the rteril lumen by 1.5 mm or more were defined s therosclerotic plques (23), nd these ptients were excluded from the nlysis, since our im ws to investigte the reltionship between TAA nd CIMT elstogrphy extensively from therosclerotic plque elstogrphy. Twenty-nine ptients with therosclerotic plque in the crotid rtery lumen were lso excluded from the study. The blood flow in both crotid rteries ws observed using color Doppler US, nd blood flow prmeters of bilterl crotid rtery pek systolic velocity nd end-distolic velocity were mesured using spectrl nlysis. Elstogrphy imging nd imge nlysis: During gry scle ultrsonogrphy (US), the crotid rteries were evluted nd region of interest (ROI) for elstogrphy 2

3 ws identified. Once the elstogrphy mode is selected, the scle of colors is superimposed over the gry-scle imge. The gry-scle imge ppers on the right side of the screen nd the sonoelstogrm on the left.light compression ws pplied to the crotid rtery region in the sgittl plne using the trnsducer. At the sme time, elstogrphic imges were displyed over the B-mode imge on the monitor. Multiple elstogrphic imges were evluted nd the techniclly optiml elstogrm ws selected in order to define the elsticity score (Figur 2). Figure 1. B mode sonogrphic imge depicting crotid intimmedi mesurement (red rrow), CCA; common crotid rtery, NM; neck muscles, TV; trnsverse process of cervicl vertebrs Figure 2. Mesurement of Elstogrphy. The big white circle (red rrow) represents blood wheres smller pink one (blue rrow) represents intim medi.cca; common crotid rtery, NM; neck muscles, TV; trnsverse process of cervicl vertebrs In terms of color codes on elstogrphic imges, blue is ssocited with hrder regions, red with softer regions nd green with modertely hrder regions of the intimmedi. The elstogrphic color scle is relted to the degree of stiffness: red (soft tissue), green (intermedite stiffness), nd blue (inelstic tissue). For clssifiction, we used 4-point modified Ueno scle (15). Elsticity score (ES) I is ssocited with predominntly green color with red nd yellow mosic pttern, ES II with predominntly green color with few res of blue mosic ppernce, ES III with predominntly blue color with some res of green nd green nd blue mosic pttern, while in ES IV most of the intim medi exhibit significntly incresed stiffness, with blue color. In ddition to rel-time elstogrphic evlution, intim-medi strin cn be evluted using numericl strin vlues nd cross-checked with correltion of rdiofrequency signls. We selected two consecutive region of interest circles s trget for compring intim-medi with the ipsilterl crotid rtery for determining the control stiffness vlue. Both ROIs contined the sme mount of intim-medi nd crotid rtery. Before clculting the strin rtio we ensure tht the jugulr vein did not pper on the B-mode imge. We obtined four gry scle imges nd elstogrm nd strin mesurements for both crotid rteries. Following the exmintion we selected the most techniclly perfect imge for the evlution of crotid rtery color code grding nd stiffness. This selected elstogrm ws considered vlid. Sttisticl nlysis: Dt were nlyzed on Sttisticl Pckge for the Socil Sciences (SPSS) softwre (version 23 for Windows) (SPSS Inc., Chicgo, IL, USA). All differences ssocited with probbility of 0.05 or less were considered sttisticlly significnt. Descriptive sttistics re presented s number nd percentge nd continuous vribles s men ± stndrd devition. Ctegoricl dt were nlyzed using the chi-squre or Fisher s exct tests nd continuous vribles using the independent smples t- test. Sttisticl tests used nd p-vlues were given in detil in tble form in the results section. RESULTS Thirty-three subjects, 22 of whom were mle, were included in the TAA group nd 40 subjects, 29 mle, in the control group. Bsic chrcteristics of the study group nd comprisons thereof were shown in Tble 1. No significnt difference ws determined between the groups in terms of gender distribution, ge, current smoking sttus or presence of DM nd CVD (p>0.05). BMI, pst smoking sttus, presence of HT, hyperlipidemi nd CAD were significntly higher in the TAA group (p<0.05). As shown in Tble 2, no significnt difference ws observed between the TAA nd control groups in terms of CIMT (0.77± 0.19 vs0.71± 0.33, p=0.338) or strin rtio vlues (0.56± 0.56 vs0.70± 0.60, p=0.320). The groups ES vlues were shown in Tble 3. Since no ptients in the TAA group nd only one in the control group hd ES vlues of 4, nlysis ws performed for ES vlues of 1, 2 nd 3. Accordingly, the presence of neurysm ws found to hve no sttisticlly significnt effect on ES (2x3 Fisher s exct test p vlue: 0.721). 3

4 Tble 1. Anlysis of the study popultion Control group (n=40) TAA group (n=33) P vlue Gender (% of mles) b Age (yers) BMI (kg/m 2 ) Smokers (%) b Pst smokers (%) b Hypertension (%) b Hyperlipidemi (%) c Dibetes mellitus (%) c CAD (%) b CVD (%) c TAA: Ascending Thorcic Aortic Aneurysms, BMI: Body Mss Index, CAD: Coronry Artery Disese, CVD: Cerebrovsculr Disese, Independent smples t-test, b Chi squre test, c Fisher s exct test Tble 2. CIMT nd strin rtio vlues CIMT nd strin rtio vlues in the control nd neurysm groups Control group (n=40) TAA group (n=33) P vlue CIMT (Men±SD) 0.71± ± Strin rtio 0.70± ± (Men±SD) CIMT: Crotid Intim Medi Thickness, TAA: Ascending Thorcic Aortic Aneurysms, SD: Stndrd devition Independent Smples t-test, Tble 3. Elsticity score vlues Elsticity score vlues in the control nd neurysm groups d ES 1 n (%) ES 2 n (%) ES 3 n (%) ES 4 n (%) Totl n (%) Control group 17 (42.5) 17 (42.5) 5(12.5) 1 (2.5) 40(100.0) TAA group 11 (33.3) 17(51.5) 5 (15.2) 0 (0.0) 33 (100.0) ES: Elsticity score, TAA: Ascending Thorcic Aortic Aneurysms d 2x3 Fisher s exct test p vlue: ES 4 is omitted nd then d 2x3 Fisher s exct is pplied DISCUSSION The study findings my be summrized s follows: i) high BMI, pst history of smoking nd the incidence of hyperlipidemi, HT nd CAD were higher in the ptients with TAA thn in the control group. ii) No difference ws determined between the TAA nd control groups in terms of CIMT vlues. iii) No difference ws determined between the TAA nd control groups in terms of EUS vlues. iv) No correltion ws determined between IMT nd EUS vlues. In greement with the literture, therosclerotic risk fctors such s high BMI, smoking, hyperlipidemi nd HT were higher in the TAA group thn in the control group in this study (2-5). Atherosclerosis in ortic neurysms is closely ssocited with incresed medil degenertion nd ortic dissection (24). The frgmenttion of elstic fibers constitutes significnt prt of the thorcic ortic remodeling process tht ccompnies ging. Clcific nd therosclerotic lesions hve been reported to ccompny this frgmenttion involved in the pthogenesis of neurysm (25). Atherosclerosis begins dmging the rteril wll by cusing symptomtic chnges. Erly therosclerotic chnges in the rteril wll progress rpidly to severe lesions under the effect of crdiovsculr risk fctors (9,10,25). Currently Doppler US or ngiogrphy re generlly used for the evlution of rteril diseses. However, these techniques provide no informtion bout pthologicl chnges in the rteril wll prior to the formtion of lesions. The evlution of intim medi thickness (IMT) using US ws developed in order to be ble to investigte the wlls of superficil rteries such s the crotid in detiled nd non-invsive mnner. The ltest ESC guideline does not recommend CIMT for crdiovsculr disese risk ssessment (8). Nonetheless, numerous studies hve reported tht CIMT is vluble technique for evluting systemic therosclerosis in the erly period (3,9-11,13). Using this method, the dmge cused by therosclerosis in the rteril wll cn be evluted even in the bsence of lesion cusing chnges in the lumen (3). CIMT vlues hve been shown to be comptible with histologicl findings of therosclerosis (26). Studies hve described CIMT s non-invsive, rpid, esily repetble, economicl nd useful method of determining therosclerosis in the erly period (9,11,12,27,28). Although the reltion between CIMT nd vrious therosclerotic vsculr diseses such s CAD, PAD nd CVD hs been clerly reveledthe findings of studies investigting CIMT in neurysml diseses re inconsistent (9-12). One study reported tht CIMT vlues in ptients with AAA nd PAD incresed t similr rte to those of helthy volunteers (29). Studies mintining the opposite, however, hve reported similr CIMT vlues in ptients with AAA to those in helthy volunteers but significntly lower vlues thn those in ptients with PAD (10,30). Authors reporting lower CIMT vlues in AAAs compred to PAH hve interpreted those findings s mening tht therosclerosis is bsic pthologicl fctor in the development of PAH, but tht its effect in the development of neurysm is limited. They lso stted tht therosclerosis is only one component of the complex pthophysiologicl mechnisms in the development of neurysm. Our review of the literture reveledonly one study investigting CIMT in TAA. Hung t l. compred the men CIMT vlues of 52 ptients with TAA nd 29-member control group. They determined significntly lower CIMT vlues in the TAA group, independently of therosclerotic risk fctors (ge, BMI, gender, fmily history, smoking, dyslipidemi, rce, DM nd HT) compred to the control group (0.50±0.13mm vs 0.60±0.11 mm, p= ). Those uthors therefore suggested tht the presence of TAA significntly reduces the development of systemic therosclerosis. In ddition, they reported tht proneurysml genetic muttions provided protection ginst therosclerosis nd tht it ws importnt for these mechnisms to be understood in order to develop 4

5 protective therpeutic strtegies ginst therosclerosis (13). In contrst to Hung et l. during comprison of CIMT vlues between the groups in our study, therosclerotic risk fctors, known to ply n importnt role in the etiology of TAA, were not excluded. In greement with the informtion in the literture, smoking, HT nd hyperlipidemi levels in the TAA group were significntly higher thn those in the control group (4,5). We ttributed the men CIMT vlues in our TAA group being 0.27 mm higher thn the ptients with TAA in Hung et l. s study to this. In conclusion, the bsence of sttisticlly significnt difference between CIMT vlues in our TAA nd control groups suggested tht therosclerosis plys limited role in the pthogenesis of TAA, nd our findings support those of Hung et l. The EUS technique ws first introduced by Ophir et l. in 1991 (14). This is non-invsive US technique tht mesures the degree of hrdness of tissues. It clcultes the response to compression of the distnce between two points determined in the longitudinl plin in the tissue under investigtion. The im is to give n ide of tissue hrdness. For exmple, mlignnt formtions re generlly hrd nd do not respond to compression, while benign formtions nd norml tissues re softer nd permit compression.tissues cn be evluted ccording to their strin rtio nd strin pttern. The strin rtio is obtined by dividing the hrdness (strin) of the surrounding norml tissue by the degree of hrdness of the investigted tissue. Scoring systems evluting lesion hrdness re generlly used for the strin pttern (14-20). The rteril wlls of ptients with generlized therosclerosis re observed to lose elsticity nd softness during crdiovsculr surgicl procedures. We therefore hypothesized tht EUS might be useful in the ssessment of vsculr diseses whose etiopthogenesis involves therosclerosis. However, our review of the literture reveled no EUS studies investigting the systemic effects of therosclerosis in vsculr diseses. Studies on this subject hve generlly focused on being ble to identify risk of stroke nd unstble plque rupture in the crotid rtery (21,22). In our study we determined no significnt difference in terms of EUS vlues between the TAA nd control groups. We lso observed no correltion between the CIMT vlues we obtined nd the EUS findings. These findings suggested tht, like CIMT, EUS is not method tht cn be used in the evlution of therosclerotic vsculr diseses. There re number of limittions to this study. First, there is no stndrd method of ssessing CIMT. Studies hve mesured the crotid rtery nd internl crotid rteries from vrious points bsed on crotid rtery bifurction. In ddition, different methods such s tking the highest from bilterl mesurements or men vlues hve been employed. This mkes it difficult to estblish working method nd to compre previous studies (9,10). Second, there is no screening technique for determining cuses of neurysm of genetic origin, such s Mrfn nd Ehler- Dnlos syndromes. However, these syndromes re very rre nd re seen in young ptients. The possibility of their ffecting our study popultion is therefore very low (9). Third, there re no previous EUS studies of the systemic vsculr effects of therosclerosis. There is therefore no stndrd defined method for evluting the crotid rteries for this purpose using EUS. CONCLUSION In conclusion, our findings suggest tht the effect of therosclerosis in the pthogenesis of TAA is limited. CIMT is n importnt method in the evlution of systemic therosclerosis in the erly period. However, it ppers to hve no efficcy in the ssessment of TAA. On the other hnd, our findings suggest tht EUS cnnot be used s screening technique in the erly ssessment of TAA. Wider rnging studies with broder levels of prticiption re now needed to illuminte the complex mechnisms underlying the development of TAA. 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