DINTRE NIVELELE SCAZUTE DE BILIRUBINA SERICA SI CRESTEREA GROSIMII COMPLEXULUI INTIMA-MEDIA LA NIVELUL ARTEREI CAROTIDE
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1 ASOCIEREA DINTRE NIVELELE SCAZUTE DE BILIRUBINA SERICA SI CRESTEREA GROSIMII COMPLEXULUI INTIMA-MEDIA LA NIVELUL ARTEREI CAROTIDE Germaine Săvoiu 1, Corina Şerban 1, Lavinia Noveanu 2, O. Fira-Mlădinescu 1, Anca Tudor 3, Roxana Popescu 4, Danina Muntean 1, Doina Verdeş 4, Georgeta Mihalaş 2 1- DEPARTAMENTUL DE FIZIOPATOLOGIE; 2- DEPARTAMENTUL DE FIZIOLOGIE; 3- DEPARTAMENTUL DE INFORMATICĂ; 4- DEPARTAMENTUL DE BIOLOGIE CELULARA, UNIVERSITATEA DE MEDICINĂ ŞI FARMACIE VICTOR BABEŞ TIMIŞOARA, THE ASSOCIATION BETWEEN LOW SERUM BILIRUBIN LEVELS AND INCREASED CAROTID INTIMA-MEDIA THICKNESS Abstract. Carotid intima-media thickness (IMT) is a predictor for the development and progression of atherosclerosis. Oxidative modification of human low density lipoprotein (LDL) has been implicated in plaque formation in blood vessels leading to atherogenesis. Bilirubin prevents oxidative modification of LDL and may protect from atherosclerosis and arterial hypertension. The aim of this study was to analyze the association between low serum bilirubin levels with carotid intima-media thickness in a group of 73 patients. Carotid intima-media thickness was measured by means of high-resolution vascular ultrasound. All the patients were clinically and paraclinically investigated. We have determined the levels of triglycerides, total cholesterol, HDL-cholesterol and serum bilirubin levels. We used the Friedewald formula to estimate serum LDL-cholesterol levels. Carotid IMT was increased, 1.05 ± 0.02 mm. We noticed low serum levels of total bilirubin (0.67 ± 0.08 mg/dl), direct bilirubin (0.20 ± 0.05 mg/dl) and indirect bilirubin (0.47 ± 0.07 mg/dl). The statistically analysis done with Pearson s test indicated inverse correlations between low serum total bilirubin, direct bilirubin and indirect bilirubin levels and carotid intima-media thickness. Oxidation of LDL is implicated in plaque formation in blood vessels leading to atherogenesis, and there is evidence that prevention of this oxidation reduces the incidence of coronary heart disease. In this study we have shown that lower serum bilirubin concentrations are independently and inversely associated with carotid intima-media thickness. Bilirubin, via its antioxidant potential, has antiatherogenic properties and might be a new potential therapeutic target in cardiovascular diseases. Key words: bilirubin, intima-media thickening, atherosclerosis Introducere Dezvoltarea aterosclerozei implica cateva reactii oxidative precum formarea oxigenului, a radicalilor peroxil, oxidarea lipidelor si mai ales a lipoproteinelor cu densitate scazuta (Mylonas si Kouretas, 1999). Intelegerea procesului patogenic al aterosclerozei a condus la ideea ca antioxidantii au rol important in prevenirea aterosclerozei si a altor boli. Din moment ce modificarea oxidativa a LDL rezulta din peroxidarea lipidelor, apa si antioxidantii solubili ar putea avea un rol in prevenirea aestei modificari (Vitek si colab.; 2002). In alte studii s-a sugerat ca antioxidantii precum vitamina E sau flavonoidele protejeaza LDL de modificarea oxidativa, ceea ce ar putea avea un rol important in procesul aterogenetic si inflamator, protejand organismul de ateroscleroza si boala coronariana ischemica (Breimer si colab.; 1995). Pe baza studiilor in vitro efectuate pe animale, este general recunoscut ca bilirubina este o substanta antioxidanta
2 foarte importanta (Mayer, 2000). Alte studii au sugerat sugerat ca bilirubina actioneaza ca un antioxidant fiziologic important deoarece sinteza sa este indusa de stresul exidativ si poate proteja impotriva aterosclerozei, bolii arteriale coronariene si inflamatiei (Siow si colab.; 1999). Studii anterioare au demonstrat ca exista corelatii inverse intre prezenta bolii cardiovasculare si nivelul bilirubinei totale serice (Hopkins si colab.;1996, Schwertner si colab.; 1994). In plus, nivelul de bilirubina se coreleaza invers cu cativa factori de risc ai bolii cardiovasculare, printre care fumatul, nivelul crescut de LDL-colesterol, diabetul, si obezitatea, dar este direct proportionala cu HDL-colesterolul (Madhavan si colab.; 1997). Efectele bilirubinei asupra riscului de boala cardiovasculara sunt evidente la barbati, dar neclare la femei (Hunt si colab.; 2001). Grosimea intimei mediei arterei carotide IMT măsurată noninvaziv prin ultrasonografie este folosită ca un marker pentru boala aterosclerotică şi este direct asociată cu un risc crescut de boală cardiovasculară (Davis si colab.; 2001). Pentru a descoperi mai multe despre rolul statusului endoteliului vascular in stadiile precoce ale aterosclerozei, am analizat relatia dintre IMT masurat la nivelul arterei carotide si nivelele scazute de bilirubina serica la un grup de 73 de pacienti. Material si metode Am selectat un numar de 73 de subiecti, 52 barbati si 21 de femei pe baza nivelelor de bilirubina serica totala, in absenta unei boli sistemice, renale, hepatice. Un alt criteriu de selectie a fost varsta pacientilor, care a fost cuprinsa intre 30 si 40 de ani. S-au facut cel putin 3 determinari ale bilirubinei serice totale, in decurs de 6 luni. Studiul a fost realizat in conformitate cu Declaratia de la Helsinki si a fost obtinut consimtamantul scris al fiecarui pacient. Am efectuat la fiecare pacient examen clinic complet si fiecare individ a completat, voluntar, un chestionar pentru identificarea factorilor de risc cardiovasculari care a cuprins: date personale (varsta, sex), istoricul de diabet sau hipertensiune si fumatul. A fost masurata de asemenea tensiunea arteriale sistolica la acesti pacienti. Au fost recoltate probe de sange prin punctie venoasa dimineata, dupa un post nocturn de minim 8 ore. Colesterolul seric toral (CT), trigliceridele (TG) si HDL-colesterolul au fost masurate prin metode enzimatice standard. S-au calculat concentratiile plasmatice de LDLcolesterol prin formula lui Friedewald: LDL (mg/dl) = [TC (mg/dl) TG (mg/dl) / 5] HDL C (mg/dl). Grosimea intima-medie (IMT) este un marker al aterosclerozei subclinice la nivelul arterelor carotide. Toţi pacienţii au fost evaluaţi cu ajutorul unui sistem de operare B-mode de rezoluţie înaltă cu transductor liniar cu frecvenţa de 10 MHz. Pentru obţinerea unei imagini de calitate distanţa focală optimă a fost de mm, frecvenţa optimă a cadrelor de 25 Hz şi s- au efectuat setări de amplificare pentru a elimina artefactele intraluminale minime. Amplificarea compensatorie a fost în jur de 60 db. De asemenea, s-au făcut ajustări pentru obţinerea unei luminozităţi simetrice a peretelui apropiat cât şi a celui depărtat, scăzând în caz de necesitate amplificarea în partea mijlocie a câmpului, pentru evitarea artefactelor intraluminale. Segmentele pereţilor arteriali au fost evaluate longitudinal, perpendicular pe raza ultrasunetului, cu vizualizarea clară a ambilor pereţi pentru a permite măsurarea diametrului, conform Consensului de la Mannheim. Se recomandă incidenţa laterală deoarece aceasta oferă cea mai bună vedere a câmpului mijlociu, nivel la care rezoluţia este mai mare decât în câmpul alăturat sau îndepărtat. IMT se măsoară de preferinţă la nivelul peretelui 45
3 îndepărtat. În cazul peretelui apropiat, IMT trebuie măsurat separat de IMT de la nivelul peretelui îndepărtat. De-a lungul a minim 10 mm de segment arterial, se obţine o imagine de calitate prin măsurători seriate. O valoare de peste 1 mm a fost considerata anormala. In figura 1 am exemplificat determinarea grosimii intima-media carotidiana, intr-o sectiune longitudinala la nivelul arterei carotide comune. Figura1. Sectiune longitudinala la nivelul arterei carotide comune Am masurat nivelul de bilirubina serica totala prin metode colorimetrice standard.toate valorile numerice au fost exprimate ca valoare medie ± deviaţie standard. Analiza statistică a fost făcută folosind testul Pearson s pentru corelaţii şi testul t-student pentru valori pereche. Valorile de probabilitate p < 0.05 au fost considerate semnificative. Toate analizele statistice au fost efectuate folosind programul Excell Microsoft Office Rezultate Datele demografice, factorii de risc cardiovasculari traditionali si masuratorile IMT carotidian sunt exemplificate in tabelul I. Subiectii au fost predominant barbati si majoritatea dintre ei au fost supraponderali. 10% dintre subiecti erau fumatori si aveau istoric de hipertensiune.valoarea medie a masurarilor IMT la nivelul carotidei a fost 1,05 ± 0,02 mm. Nivelele de bilirubina au fost scazute: bilirubina serica totala 0,67 ± 0,08 mg/dl, biliubina directa 0,20 ± 0,05 mg/dl si nivelul de bilirubina indirecta 0,47 ± 0,07 mg/dl. Tabel I. Caracteristicile subiectilor studiati (n = 73) Caracteristici Medie ± deviatie standard Varsta (ani) 30 ± 10 Presiune arteriala 111,7 ± 16,06 sistolica (mm Hg) Presiune arteriala 72,42 ± 10,71 diastolica (mm Hg) Colesterol total (mg/dl) 176,32 ± 29,2 Trigliceride (mg/dl) 180,79 ± 72,05 LDL colesterol (mg/dl) 108,6 ± 22,55 HDL colesterol (mg/dl) 33,24 ± 7,99 Fumator 10% Fost fumator 8% In urma analizei rezultatelor, am observat o corelatie inversa, puternica si semnificativa intre IMT la nivelul arterei carotide si bilirubina totala (α=0.001) (figura 2). TB r=-0.81 IMT p<0.001 Figura 2-Corelatie intre IMT si bilirubina totala 46
4 In figura 3 am prezentat corelatia dintre IMT carotidian si bilirubina directa care a fost inversa, slaba si semnificativa (α=0.05) la grupul de subiecti investigati de noi DB r=-0.35 p=0.047 IMT Figura 3-Corelatie intre IMT si bilirubina directa Corelatia dintre IMT masurat la nivelul arterei carotide si bilirubina indirecta a fost inversa, medie si semnificativa (α=0.01) (figura 4) IB r=-0.45 p=0.007 IMT Figura 4-Corelatia dintre IMT si bilirubina indirecta 47
5 Discutii IMT masurat la nivelul arterei caroride, care este o metoda neinvaziva imagistica recomandata de American Heart Association pentru evaluarea riscului cardiovascular, este un marker al aterosclerozei foarte cunoscut (Greenland si colab.; 2001). Creşterea IMT se corelează cu factorii de risc cardio-vasculari şi cu severitatea aterosclerozei coronariene, această creştere fiind de asemenea un factor predictiv pentru evenimentele cardio-vasculare ulterioare, din cadrul grupurilor populaţionale (Raitakari si colab.; 2003). In cateva studii s-a descoperit ca diferite forme circulante ale bilirubinei sunt puternic antioxidante si toate formele de bilirubina protejeaza LDL impotriva peroxidarii (Strocker, 1987). Nu se stiu foarte multe despre asocierea bilirubinei totale cu boala cardiovasculara. Schwertner si colaboratorii au fost primii care au observat o corelatie inversa semnificativa intre concentratia plasmatica a bilirubinei serice totale si prevalenta bolii cardiovasculare (Schwertner si colab.;1994). Bilirubina se pare ca de asemenea protejeaza eritrocitele si miocitele ventriculare cand sunt expuse actiunii radicalilor liberi de oxigen (Wu si colab.; 1991). De asemenea s-a sugerat ca nivele crescute de bilirubina plasmatica ar putea reduce riscul aterogen (Wu si colab.; 1991). Desi mecanismele prin care anumite concentratii de bilirubina protejeaza impotriva aterosclerozei si bolii cardiovasculare raman a fi clarificate, ar putea fi posibil ca in viitor, concentrtia de bilirubina sa devina un index al aterosclerozei (Greenland si colab.; 2001). In acest studiu noi am observat ca la subiectii cu concentratii scazute ale nivelului de bilirubina serica, valoarea IMT masurat la nivelul arterei carotide este crescuta. Aceasta observatie este importanta, deoarece, putem trage concluzia ca subiectii cu nivel scazut de bilirubina serica au risc crescut de aterscleroza, in stadii precoce de viata. Concluzii Cresterea grosimii intima-media carotidiene la subiecti tineri, cu nivele scazute de bilirubina serica totala, sugereza ca, acestia sunt predispusi sa dezvolte precoce ateroscleroza si boala cardiovasculara. Asadar, putem considera nivelul bilirubinei serice un marker independent al bolii cardiovasculare. Bibliografie Breimer LH, Wannamethee G, Ebrahim S, Shaper AG. Serum bilirubin and risk of ischemic heart disease in middle-aged British men. Clin Chem 1995;41: Davis PH, Dawson JD, Riley WA, Lauer RM. Carotid intimal medial thickness is related to cardiovascular risk factors measured from childhood through middle age. The Muscatine Study. Circulation 2001; 104: Greenland P, Smith SC, Grundy SM. Improving coronary heart disease risk assessment in asemptomatic people role of traditional risk factors and noninvasive cardiovascular tests. Circulation 2001;104: Hopkins PN, Wu LL, Hunt SC, James BC, Vincent GM, Williams RR. Higher serum bilirubin is associated with decreased risk for early familial coronary artery disease. Arterioscler Thromb Vasc Biol 1996;16: Hunt SC, Kronenberg F, Eckfeldt JH, Hopkins PN, Myers RH, Heiss G. Association of plasma bilirubin with coronary heart disease and segregation of bilirubin as a major gene trait: the NHLBI family heart study. Atherosclerosis 2001;154: Madhavan M, Wattigney WA, Srinivasan SR, Berenson GS. Serum bilirubin distribution and its relation to cardiovascular risk in children and young adults. Atherosclerosis 1997;131: Mayer M. Association of serum bilirubin concentrations with risk of coronary artery disease. Clin Chem 2000;46:
6 Mylonas C, Kouretas D. Lipid peroxidation and tissue damage. In Vivo 1999;13: Raitakari, O.T., M. Juonala, M. Kähönen, L. Taittonen, T. Laitinen, N. Mäki-Torkko, M.J. Järvisalo, M. Uhari, E. Jokinten, T. Rönnemaa, H.K. Åkerblom, J. Viikari, Cardiovascular risk factors in childhood and carotid artery intima-media thickness in adulthood: The cardiovascular risk in young finns study, JAMA, 2003, 290, Schwertner HA, Jackson WG, Tolan G. Association of low serum concentration of bilirubin with increased risk of coronary artery disease. Clin Chem 1994;40: Siow RC, Sato H, Mann GE. Heme oxygenase-carbon monoxide signalling pathway in atherosclerosis: anti-atherogenic actions of bilirubin and carbon monoxide? Cardiovasc Res 1999;41: Strocker R, Yamamoto Y, McDonagh AF, Glazer AN, Ames BN. Bilirubin is an antioxidant of possible physiological importance. Science 1987;235: Vitek L, Jirsa Jr M, Brodanova M, et al. Gilbert syndrome and ischemic heart disease: a protective effect of elevated bilirubin concentrations. Atherosclerosis 2002;160: Wu TW, Wu J, Li RK, Mickle D, Carey D. Albumin-bound bilirubins protect human ventricular myocytes against oxyradical damage. Biochem Cell Biol 1991;69:
Received: March 2008; in final form May 2008.
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