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OCT Findings in Patients With Recanalization ofOrganized Thrombi in Coronary Arteries
Soo-Jin Kang, MD, PHD,* Masataka Nakano, MD,† Renu Virmani, MD,†Hae-Geun Song, MD,* Jung-Min Ahn, MD,* Won-Jang Kim, MD,* Jong-Young Lee, MD,*Duk-Woo Park, MD, PHD,* Seung-Whan Lee, MD, PHD,* Young-Hak Kim, MD, PHD,*Cheol Whan Lee, MD, PHD,* Seong-Wook Park, MD, PHD,* Seung-Jung Park, MD, PHD*
Seoul, Korea; and Gaithersburg, Maryland
O B J E C T I V E S The purpose of this study was to determine the angiographic and optical coherence
tomographic (OCT) characteristics of coronary lesions with recanalized thrombi.
B A C K G R O U N D Although spontaneous recanalization of thrombi has been reported pathologi-
cally, it is rarely recognized in clinical practice.
M E T H O D S Based on histopathologic features, recanalization of thrombi was defined by character-
istics on OCT.
R E S U L T S Recanalization of thrombi was identified in 6 patients (3 male, 3 female; median age 63
years; age range 54 to 72 years). Based on symptoms, 3 patients were diagnosed with unstable angina;
2 were diagnosed with stable angina; and 1, who had mitral stenosis and huge left atrial thrombi, was
diagnosed with post-infarct angina. All had normal serum concentrations of cardiac markers at
admission. Angiography showed irregular linear filling defects and haziness. Two patients with near total
occlusion had Thrombolysis In Myocardial Infarction (TIMI) flow grade 1 and collaterals, whereas 4
patients had TIMI flow grade 3 and no collaterals. All patients showed OCT findings consistent with
recanalized thrombi, which consisted of signal-rich, high backscattered septa that divided the lumen
into multiple small cavities communicating with each other. These structures, which had smooth inner
borders, created a “Swiss cheese” appearance. Percutaneous coronary intervention was performed in 5
patients with angiographic slow flow or inducible-ischemia as documented by invasive or noninvasive
stress tests. The remaining 1 patient with restored coronary flow underwent mitral valve surgery and left
atrial thrombectomy.
C O N C L U S I O N S OCT provided details on the characteristics of the organization of thrombi in both
chronic total occlusion and subtotal narrowing. Coronary lesions containing recanalized thrombi were
characterized by multiple small channels, with most showing functional significance. (J Am Coll Cardiol
Img 2012;5:725–32) © 2012 by the American College of Cardiology Foundation
From the *Department of Cardiology, University of Ulsan College of Medicine, Asan Medical Center, Seoul, Korea; and the†CVPath Institute, Inc., Gaithersburg, Maryland. This study was supported by a grant of the Korea Healthcare TechnologyR&D Project, Ministry of Health and Welfare, Republic of Korea (A102065). Dr. Virmani has served on the Speakers’ Bureauand has received research support from Terumo Corporation and St. Jude Medical. All other authors have reported they haveno relationships relevant to the contents of this paper to disclose. Neil J. Weissman, MD, served as Guest Editor for this paper.
Manuscript received December 9, 2011; revised manuscript received February 29, 2012, accepted March 19, 2012.
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Kang et al.
OCT in Recanalized Thrombi
726
lthough recanalization of coronary thrombihas been characterized pathologically, it israrely recognized in real clinical practice
(1–5). Because angiographic hazinessand filling defects are common but nonspecificfindings, it is speculated that a recanalized throm-bus is often misdiagnosed as other pathologicalconditions such as fresh thrombosis by plaquerupture/erosion, spontaneous dissection, aneurysm,or heavy calcification. Despite several case reportsaddressing neovascularization within thrombi (6–9), itsincidence and functional significance remain un-clear.
Advances in high-resolution imaging modalities,such as intravascular ultrasound (IVUS) and opticalcoherence tomography (OCT), have provided newinsights into evolving thrombotic lesions (6–9). Asangiographic haziness does not always signify afresh thrombus, intravascular imaging is necessaryto differentiate the causative mechanisms in vivoand may provide information allowing an appropri-ate treatment approach specific to the underlyingetiology. We have assessed the morphological charac-
teristics on angiography, IVUS, and OCTof coronary lesions with spontaneous recan-alization of thrombi.
M E T H O D S
Angiographic analysis. From July 2010 toSeptember 2011, OCT was performed in
71 patients. Recanalization of organized thrombias found in 6 patients on the basis of OCTndings. Qualitative and quantitative angiographiceasurements were performed using standard tech-
iques with automated edge-detection algorithmsCAAS-5, Pie-Medical, Maastricht, the Nether-ands) at the angiographic analysis center of theardioVascular Research Foundation, Seoul, Korea
10,11).OCT imaging and analysis. Before February 2011,OCT images were acquired by an occlusive tech-nique using a commercially available system forintracoronary imaging and a 0.019-in ImageWire(LightLab Imaging, Westford, Massachusetts) be-fore IVUS imaging. The artery was cleared of bloodby continuous flushing with iodixanol 370 (Visi-paque, GE Health Care, Cork, Ireland) at a flowrate of 3.0 ml/s (12). Since March 2011, OCTimages were acquired by a nonocclusive techniquewith a C7XR system (DragonFly catheter andC7XR, LightLab Imaging). Based on previous
und
histopathologic studies, recanalization or neovascu- m
larization of thrombi was defined as multiple chan-nels divided by thin septa with or without commu-nication with each other (3–8). Calcification wasdefined as a well-delineated, signal-poor regionwith sharp borders (13). Fresh thrombi were de-fined as masses �250 �m in diameter protrudingnto the vessel lumen and discontinuous from theurface of the vessel wall. Red thrombi were defineds high-backscattering protrusions with signal-freehadowing, and white thrombi as signal-rich, lowackscattering projections into the lumen (14–17).he OCT analysis was performed by 2 independentbservers (S.J.K. and H.G.S.).
IVUS imaging and analysis. IVUS imaging was per-ormed after OCT imaging and after intracoronarydministration of 0.2 mg nitroglycerin using motor-zed transducer pullback (0.5 mm/s) and a commercialcanner (Boston Scientific/SCIMED, Minneapolis,
innesota), consisting of a rotating 40 MHz trans-ucer within a 3.2-F imaging sheath. Using comput-rized planimetry (EchoPlaque 3.0, Indec Systems,
ountain View, California), off-line quantitativeVUS analysis was performed in a core laboratory athe Asan Medical Center. External elastic membranend minimal lumen areas were measured at the lesionite and reference segments (18).
R E S U L T S
Clinical characteristics. Based on the OCT findings,ecanalization of organized thrombi was identifiedn 6 patients. The median age of the patients was 63ears (range 54 to 72 years) and 3 were female. Fiveatients had no history of previous percutaneousoronary intervention or coronary bypass surgery.nly 1 patient (Patient #6) showed in-stent reste-
osis after drug-eluting stent implantation 4 yearsarlier.
Table 1 summarizes the history and clinicalresentation of the 6 patients. Three patients, withecently developed or aggravated angina symptomsor 1 to 8 weeks before admission, were diagnosedith unstable angina. Two patients presented with
table angina, and 1 patient (Patient #4) with mitraltenosis and huge left atrial thrombi 5 weeks afteron–ST-segment elevation myocardial infarctionas diagnosed with post-infarct angina. All 6 pa-
ients were admitted through the out-patient de-artment. At admission, none had resting chestain or presented with acute myocardial infarction.heir serum concentrations of creatine kinase-
A B B R E V I A T I O N S
A N D A C R O N YM S
IVUS � intravascular ultraso
OCT � optical coherence
yocardial band and troponin were normal.
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The most common finding on electrocardiogra-phy was T-wave inversion, observed in 4 (67%)patients, whereas Q-wave was seen in only 1 pa-tient. Regional wall motion abnormalities of thetarget vessel territory were observed in 4 patients(67%). The results of noninvasive and invasivestress tests are shown in Table 1.Angiographic and grayscale IVUS. The involved ves-sel was the left anterior descending artery in 2patients and the right coronary artery in 4 patients.All lesions presented with multiple speckled stain-ing of contrast or filling defects with irregular
Table 1. Clinical Characteristics, Cases 1 Through 6
Patient # Sex/AgeClinical Presentation
at Admission
1 F/72 Chest pain during exercise8 months previously;aggravated symptomsfor 1 month
Un
2 M/63 5-year history of angina;aggravated chest painfor 1 week
Un
3 F/54 New onset of prolongedchest pain for 4 weeks
Un
4 F/63 Non-STEMI 5 weeksearlier; mitral stenosiswith LA thrombi atrialfibrillation
Ol
5 M/55 Effort-related chest painfor 1 year
Sta
6 M/73 s/p DES implantation4 years earlier;recurrent angina 1 yearearlier
Sta
DES � drug-eluting stent(s); ECG � electrocardiogram; Echo � echocardiograpelevation myocardial infarction.
Table 2. Angiographic Findings
Findings 1 2
Lesion site RCA RCA
Lesion length, mm 29.3 19.5
Diameter stenosis, % 65 42
TIMI flow grade 3 3
Collaterals None None
Visible thrombi � �
Plaque rupture � �
Haziness or filling defect � �
Calcification � �
Dissection � �
Minus symbols indicate negative findings; plus symbols indicate positive findin
LAD � left anterior descending artery; RCA � right coronary artery; TIMI � Thromlumen border. In each, the lumen included multiplelinear structures mimicking a spontaneous dissec-tion. Three patients showed only a mild degree ofangiographic stenosis (diameter stenosis �50%).Angiography showed irregular linear filling defectand haziness. Two patients with near total occlu-sion had Thrombolysis In Myocardial Infarction(TIMI) flow grade 1 and collateral vessels, whereasthe other 4 patients had TIMI flow grade 3 and nocollateral vessels (Table 2).
Pre-procedural IVUS was performed in 4 of the6 patients and showed multiple cavities of variable
agnosis Risk Factors Noninvas
le angina Hypertension,hyperlipidemia
ECG: Q-wave in II, III,Echo: inferoposteriorThallium: partially revsevere perfusion d
le angina Smoking, hypertension,hyperlipidemia
ECG: T-wave inversioEcho: inferoposteriorFFR at maximal hype
le angina None ECG: T-wave inversiolateral leads
Thallium: partially revdefect in apical sepmid anteroseptum
Echo: akinesia of ante
yocardialrction
Hypertension ECG: T-wave inversioEcho: severe mitral st
(5 � 3 cm), hypokinferior wall, EF 50
angina Hypertension,hyperlipidemia,smoking
Thallium: reversible, lin apical septum a
ECG and Echo: norma
angina Diabetes mellitus ECG: T-wave inversioEcho: normal finding
F � ejection fraction; FFR � fractional flow reserve; LA � left atrial; s/p � status p
Patient #
3 4 5
LAD RCA LAD
65.0 20.4 15.9
36 41 100
3 3 1
None None From RCA
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bolysis In Myocardial Infarction.J A C C : C A R D I O V A S C U L A R I M A G I N G , V O L . 5 , N O . 7 , 2 0 1 2
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Kang et al.
OCT in Recanalized Thrombi
728
size at the lesion site. There was vigorous bloodspeckling suggesting severe blood stasis in thelumen. The IVUS also revealed free-floating, hugeintraluminal thrombi in 3 patients. All had mark-edly dilated vessels (external elastic membrane di-ameter �5.0 mm) with positive remodeling at thelesion segment and angiographic haziness.OCT findings. On OCT, all patients with recana-lized thrombi showed signal-rich, high backscat-
Figure 1. Histology and OCT Illustrations of Recanalization With
(A) The old lumen is occupied by an organized thrombus (black arwell endothelialized (red asterisks). (B) The signal-poor, darker tissu(OCT) corresponds to a proteoglycan-rich area (red arrows). Converand collagen, as well as being brighter on OCT (black arrow).
Figure 2. Angiographic and OCT Findings in Patient #1 and Pat
In both Patient #1 (A to C) and Patient #2 (D to F), angiography (Aof the right coronary artery (black arrows). Intravascular ultrasonog(red asterisks). Optical coherence tomography (OCT) (C, F) showed
central lumen (white asterisk). The “Swiss cheese” appearance suggesttered septa dividing the lumen into multiple smallcavities that communicated with each other (Fig. 1).The thin septa had smooth inner borders, and themultiple holes had a “Swiss cheese” appearance.The deeper portion contained signal-poor, darkertissue, corresponding to a proteoglycans-rich areawith or without neovascularization on histology. Incontrast, the areas near the lumen tended to bebrighter, suggesting a relatively higher content of
hrombi
heads). The surface of septa of recanalized spaces are smooth andthe deeper portion observed on optical coherence tomography, the areas near the lumen tend to be rich in smooth muscle cells
#2
showed multiple filling defects and haziness in the mid portiony (B, E) showed multiple cavities filled with blood specklingltiple small channels, divided by thin septa, surrounding a larger
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OCT in Recanalized Thrombi
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smooth muscle cells and collagen. The angio-graphic, IVUS, and OCT findings of the 6 patientsare shown in Figures 2 to 5. Fresh or organizinghrombi with signal attenuation were present in thereas adjacent to the lesion in 3 patients, whereasCT-defined calcification was not observed. Thereas no definitive evidence of plaque rupture orissection as a nidus of thrombotic occlusion.
Revascularization. Treatment strategy was based onhe functional significance of stenosis. All 3 patientsho underwent thallium scans (Patients #1, #3, and5) showed reversible or partially reversible perfu-ion defects in the corresponding territories, and 1Patient #2) showed a reduced fractional flow re-erve of 0.65. These 4 patients with documentednducible ischemia underwent percutaneous coro-ary intervention, with drug-eluting stents success-ully implanted. In addition, a drug-eluting stentas implanted in Patient 6, who was diagnosedith total in-stent restenosis and angiographic slowow. There was symptomatic improvement in allatients after treatment. The remaining patientPatient #4) with restored coronary flow underwentitral valve surgery and left atrial thrombectomy.
Figure 3. Angiographic and OCT Findings in Patient #3
(A) Intraluminal filling defects accompanied by a long flaplike strucicking a spontaneous dissection. (B, C) On optical coherence tomogdeeper portion (white arrows), represent neovascularization within
(D) The lesion was successfully treated by placement of Nobori stents.D I S C U S S I O N
Three major findings were observed in coronarylesions with recanalization of organized thrombi:1) common angiographic findings such as multipleirregular filling defects and intraluminal hazinesswere not specific for recanalization; 2) on OCT, therecanalization of organized thrombi was character-ized by multiple small channels divided by thinsepta communicating with each other; and 3) de-spite the neovascularization process, most of theselesions were functionally significant.
Previous histopathologic studies found thatolder coronary thrombi undergo organization orrecanalization to form a few large or several smalllumens. Neovascularization is of variable sizes,endothelium-lined vascular channels within thethrombus, supported by a small amount of con-nective tissue (1–5). One-third of patients withthrombotic occlusion were reported to have somedegree of recanalization, as confirmed by pathol-ogy (3,19). Although recanalization of thrombiwas not infrequent in histopathologic studies(1,3,19), it was reported to be rare when assessed
in the entire left anterior descending artery (black arrows), mim-hy (OCT), multiple channels (red asterisks), with darker tissue in aanized thrombi. A disrupted septum is visible (white arrowhead).
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angiographically (4). Because of poor resolution,oronary “luminography” has been unable to dif-erentiate multiple vascular channels from moreommon pathological conditions causing angio-raphic haziness (3,9,20). Although IVUS pro-ides cross-sectional images of atheroscleroticlaque and vessel walls, its relatively low resolu-ion limits proper diagnosis and accurate tissueharacterization. Because of its better resolution,CT can clarify the etiology of angiographic
mbiguity and potentially guide an optimal ther-peutic approach.
All 6 of our patients showed multiple linearfilling defects on coronary angiography mimickingspontaneous dissection. Although neovasculariza-tion is based on pathological diagnosis, OCTclearly demonstrated the unique features of recana-lized thrombi in vivo, described as a Swiss cheese–like or spider web–like appearance. These findingssuggest that the organization of thrombi is eithercomplete or ongoing (7–9). Figure 1 illustrates the
athological findings of recanalized thrombi thatere similar to the OCT findings.Although the functional significance of recanali-
ation of organized thrombi has been unclear,revious studies have reported that blood flowhrough recanalized channels is insufficient. Be-ause the growth of vascular channels takes several
Figure 4. Angiographic and OCT Findings in Patient #4 and Pat
In both patients, (A to C) Patient #4 and (D to F) Patient #5, (A, D)with luminal haziness. (B, C, E, F) Optical coherence tomography (Osepta, as well as protruding intraluminal thrombi with attenuation
eeks or months (5,21,22), the role of recanaliza-
ion in the restoration of blood flow may bensignificant, especially soon after infarction. Weound that angiographic diameter stenosis variedrom 36% to 100%. Irrespective of the degree ofngiographic stenosis, all patients who underwentnvasive or noninvasive functional tests had induc-ble ischemia revealed. Despite the recanalization,he stenosis remained functionally significant inost of our patients, and it is also suggested by an
utopsy study that recanalized thrombi may beesponsible for terminal coronary events (2). How-ver, it remains unclear how recanalization affectsarly and long-term prognosis after myocardialnfarction; therefore, more investigations are defi-itely needed in this matter.
Study limitations. As a limitation of retrospectiveobservation, the general incidence of thrombus withrecanalization or the accuracy of angiographic find-ings was not shown. Also, the accuracies of gray-scale IVUS with 40 MHz and 20 MHz catheters inidentifying thrombi were not compared in thestudy. Because the sample size of this study wassmall and there was no histological confirmation,our observations cannot be generalized. More-over, we could not determine the possible causesof initial thrombotic occlusion, such as plaquerupture or spontaneous dissection, as a nidus for
#5
iography showed multiple irregular filling defects (black arrows)showed many channels with smooth inner border of multiplete arrows).
ient
angCT)
thrombus formation. The presence of clinical
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plaque rupture or focal dissection may be ob-scured by organized thrombi or other structures.In addition, the entry site of a dissection isusually small and may not show re-entry into thetrue lumen. Finally, the composition of the extra-cellular matrix including its collagen/proteoglycancontent depends on duration of thrombus, location,and other factors, and this small study did notaddress the various stages of evolving thrombi over
Figure 5. Angiographic and OCT Findings in Patient #6
(A) In-stent restenosis with total occlusion (black arrows) in Patientities (red asterisks) and suspicious thrombi (white arrows). (C, D) Owithin huge thrombi (red asterisks).
ized coronary stenoses: histopatho-6. Cho JM, Raffel O
CJ, Jang IK. Spont
C O N C L U S I O N S
An OCT evaluation provided details on the charac-teristics of the evolution of thrombi. Recanalization ofthese thrombi was characterized by multiple smallchannels, with most showing functional significance.
Reprint requests and correspondence: Dr. Seung-JungPark, Professor of Medicine, Asan Medical Center,388-1 Poongnap-dong, Songpa-gu, Seoul 138-736,
(B) Grayscale intravascular ultrasonography showing multiple cav-al coherence tomography (OCT) showing neovascularization
time. South Korea. E-mail: sjpark@amc.seoul.kr.
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Key Words: angiographichaziness y optical coherencetomography y recanalized
hrombi.