Shear stress and atherosclerosis. Frank Gijsen Department of Biomedical Engineering and Cardiology ErasmusMC Rotterdam

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1 Shear stress and atherosclerosis in human coronary arteries Frank Gijsen Department of Biomedical Engineering and Cardiology ErasmusMC Rotterdam

2 Shear stress and atherosclerosis in human coronary arteries Plaque distribution in human coronary arteries Shear stress modulates plaque composition in human coronaries Location of plaque rupture in human coronary arteries (prelim!)

3 Shear stress Shear stress (SS): V h F SS = force per unit area = viscosity x shear rate = η x V/h

4 Shear stress (in a straight tube)

5 Shear stress (in a straight tube) u(r) SS = η x V/ r V r

6 Shear stress (in a straight tube) D = diameter of the tube η = viscosity of fluid Q = flow V = mean velocity = Q /0.25πD 2 shear stress: SS = η 8V/D

7 Shear stress (in a straight tube) Coronary circulation: D = 3.0 mm APV = 0.15 m/s SS = 0.6 Pa Magnitude SS very low (1 Pa): no direct mechanical impact

8 Shear stress (in arteries) Poiseuille can be useful, but: arteries are not straight tubes - bend - stenosis - bifurcations flow in arteries is not steady blood is not Newtonian Steinman et al. 1999

9 Questions?

10 Atherosclerosis Classification by Stary: Circulation 1992, 85(1): A definition of the intima of human arteries and of its atherosclerosis-prone regions Circulation 1994, 89(5): A definition of initial, fatty streak, and intermediate lesions of atherosclerosis Circulation 1995, 92(5): A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis.

11 Atherosclerosis

12 Atherosclerosis

13 Atherosclerosis

14 Atherosclerosis

15 Vulnerable plaques AHA classification by Stary did not relate atherosclerosis to sudden death. Extension of the scheme provided by Virmani (ATVB 2000, 20, ) Vulnerable plaques are characterized by necrotic core (covered by) thin fibrous cap (infiltrated by) macrophages Histological data provided by Renu Virmani Nissen et al.,am J Cardiol 2002

16 Atherosclerosis Rupture of vulnerable plaque is responsible for majority of acute myocarial infarctions and stroke. No significant lumen narrowing, so patients are often asymptomatic!

17 Questions?

18 Shear stress and atherosclerosis Magnitude SS very low (1 Pa) but is has a strong impact on the endothelium!

19 Shear stress and atherosclerosis Malek et al. JAMA 1999

20 Shear stress and atherosclerosis In the presence of risk factors, low shear stress is one of the key factors in localizing early atherosclerosis. Vanderlaan, ATVB 2004

21 Remodeling in atherosclerosis Nissen et al.,am J Cardiol 2002

22 Transition: is plaque burden limiting? lumen area [mm 2 ] plaque area media bounded area = plaque burden (%) Glagov et.al. NEJM 1987

23 Progression of atherosclerosis low shear stress high shear stress lipid influx

24 Shear stress and advanced atherosclerosis flow low high smooth muscle cells low shear stress blood flow cap high shear stress lipid core high low macrophages Slager et Dirksen al., Nature et al., Clinical Circulation Practice, 98 05

25 Slager et al., Nature Clinical Practice, vol2, #8 and vol2, #9, Shear stress and atherosclerosis

26 Questions?

27 Plaque distribution in human coronary artery bifurcations assessed with MSCT Alina van der Giessen 1, Jolanda Wentzel 1, Bob Mijboom 2, Nico Mollet 3, Frans van de Vosse 4, Ton van der Steen 1, Pim de Feyter 2,3 and Frank Gijsen 1 Departments of 1 Biomedical Engineering, 2 Cardiology, 3 Radiology, ErasmusMC Rotterdam 4 Department of Biomedical Engineering, Eindhoven University of Technology The Netherlands

28 Shear stress near bifurcations Prosi - J. Biomech. 04 low high SS shear stress

29 Hypothesis Plaque will preferentially be located in low shear stress regions in human coronary bifurcations If plaques are present at high shear stress regions, a plaque will be found in the adjacent low shear stress region as well Aim: In-vivo non-invasive assessment of plaque distribution near bifurcations with multi-slice computed tomography (MSCT).

30 MSCT coronary angiography MSCT angiography: Non-invasive (or better: minimally invasive) Plaque visible 3D

31 MSCTA specifications Siemens Somatom Sensation 64-slice scanner Temporal resolution: 164 ms In plane resolution: 0.3 mm Slice thickness: 0.4 mm Mollet - Circulation 04

32 Patients & Bifurcations Patients Elected for coronary angiography HR < 65 bpm during scanning 1 2 Bifurcations 1 Left main Left anterior descending artery & Circumflex 2 Left anterior descending artery First diagonal Trifurcations are excluded Heavily calcified arteries are excluded

33 Extract bifurcation

34 Select cross-section mm 3 4

35 Determine plaque in segments I IV II III III II IV I Segment Shear Stress I - - II - III + IV ++

36 Numbers # patients bifurcation 1 LAD LCx LAD D1 start 37 HR 65 bpm 28 bifurcation 2 Trifurcation Calcium A total of 65 (== 260 segments ) cross-sections is analyzed

37 Presence of plaque In 96% of the patients one or more crosssection contained plaque 51% of the segments shear stress % 72% contained plaque 31% 38% Mean angle of the plaque 165 appearance is 165 epicard

38 Plaque configurations 10/11 plaque in I or II No plaque in IV No plaque in facing parts 20/21 plaque in I or II /20 plaque in I and II I shear stress ++ III IV II

39 Plaque at carina (segment 4) Only 1/15 cross-sections where plaque is found at the carina conflicts with the grow hypothesis I shear stress ++ III IV II

40 Conclusion Plaques grow circumferential from low shear stress regions into high shear stress carina, because: Most plaques in low shear stress regions Early plaques (involving 1 part) where not found at the, atheroprotective, high shear stress carina In more advanced plaques (involving 2 or 3 part), the low shear stress regions are most affected If plaque is present at the high shear stress carina adjacent low shear stress regions also contain plaque, indicating that plaques grow circumferentially

41 Questions?

42 The fifth international symposium on Organized by F. Gijsen, A. Horrevoets and J. Wentzel Hilton Hotel, Rotterdam, The Netherlands April,

43 Shear stress modulates plaque composition in human coronary arteries in vivo Frank Gijsen, Jolanda Wentzel, Johannes Schaar, Pim de Feyter, Anton van der Steen and Patrick Serruys Departments of Biomedical Engineering and Interventional Cardiology, Erasmus Medical Center, Rotterdam, The Netherlands.

44 Shear stress and atherosclerosis low shear stress high shear stress continuous influx lipids

45 Slager et al., Nature Clinical Practice 2005, vol 2, #8 and #9.

46 Shear stress and atherosclerosis 448 carotid arteries : 16% had ulcers Number of ulcerations Proximal of most stenotic site Distal of most stenotic site 63 (68%) 29 (32%) de Weert, Groen et al. submitted

47 Shear stress and atherosclerosis Shear stress is an important regulating factor in vascular biology: vascular remodeling in healthy arteries key localizing factor in early atherosclerosis important de-stabilizing effect on composition in late atherosclerosis Aim: To investigate the relationship between shear stress and plaque composition in human coronary arteries

48 Methods: plaque composition IVUS at 100 mmhg (t 1, P 1 ) processing (t 2, P 2 ) Strain map IVUS at 95 mmhg

49 Methods: plaque composition Smooth muscle cells Macrophages 3.0 3, , ,0 Strain (%) Strain (%) 1,5 1,0.5, ,0 none minor medium heavy none minor medium heavy Schaar et al., Circulation, vol #8, 2003

50 index follow up

51 high ANGUS 3D wall thickness ANGUS + CFD 3D shear stress ANGUS + palpo 3D strain data At index and at 6 months follow up low

52 Methods: plaque definition ANGUS data normalized wall thickness (wt norm ) : wt norm = 0.2 U S T S flow D U: upstream T: throat S: shoulders D: downstream

53 shear stress strain 31 plaques in 13 coronary arteries were analyzed. S U T S S U T S D D average normalized shear 3 stress # strain [%] # # # # 0.25 low medium high shear stress

54 average normalized shear stress average shear stress [Pa] # U T S D average strain [%] # U T S D

55 U S T S strain [%] D shear stress [Pa] 29 out of 31 plaques showed a positive relationship between shear stress and strain S U T S D

56 Results: shear stress vs strain 0.75 # strain [%] # # low medium high shear stress Accepted for publication in the American Journal of Physiology.

57 Discussion and conclusions (1) Shear stress is low downstream of a plaque, but the complex 3D shape of human coronary arteries does not allow to predict shear stress distribution in other plaque regions. Lower strain values can be observed downstream of a plaque, which agrees with the observation that at those locations more SMC are present. Other plaque locations show a heterogenuous strain distribution. The plaque regions exposed to the highest shear stress reveal increased strain values, indicating that shear stress might have an impact on plaque composition in the more advanced phases of the disease.

58 wall thickness shear stress strain index strain fup Final number: 16 plaques in 7 patients strain

59 Results: location vs strain strain U T S D

60 Results: shear stress vs strain # strain

61 Discussion and conclusions (2) Follow-up studies are difficult! Changes in strain -and thus plaque composition- over a six month period are small. No significant changes in plaque composition can be found if we look at different plaque regions. However, those plaque regions exposed to highest shear stress levels show an increase in strain, confirming our hypothesis that high shear stress might be involved in destabilizing advanced atherosclerotic plaques.

62 Acknowledgements Bioengineering lab: Jolanda Wentzel Harald Groen Alina van der Giessen Frits Mastik Ton van der Steen Department of Radiology: Nico Mollet Aad van der Lugt Wiro Niessen Department of Interventional Cardiology Johannes Schaar Patrick Serruys Pim de Feyter

63 The fifth international symposium on Organized by F. Gijsen, A. Horrevoets and J. Wentzel Hilton Hotel, Rotterdam, The Netherlands April,

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