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European Heart Journal Advance Access originally published online on November 6, 2007
European Heart Journal 2008 29(1):38-44; doi:10.1093/eurheartj/ehm507
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Published on behalf of the European Society of Cardiology. All rights reserved. © The Author 2007. For permissions please email: journals.permissions@oxfordjournals.org

Relationship between longitudinal morphology of ruptured plaques and TIMI flow grade in acute coronary syndrome: a three-dimensional intravascular ultrasound imaging study

Atsushi Tanaka1,*, Kenei Shimada2, Masashi Namba3, Tsunemori Sakamoto4, Yasuhiro Nakamura3, Yukio Nishida4, Junichi Yoshikawa2 and Takashi Akasaka1

1 Department of Cardiovascular Medicine, Wakayama Medical University, 811-1, Kimiidera, Wakayama 641-8510, Japan
2 Osaka Ekisaikai Hospital, Osaka, Japan
3 Ishikiri-seiki Hospital, Higashiosaka, Japan
4 Baba Memorial Hospital, Sakai, Japan

Received 3 November 2006; revised 28 September 2007; accepted 12 October 2007; online publish-ahead-of-print 6 November 2007.

* Corresponding author. Tel: +81 73 447 2300, Fax: +81 73 446 0631. Email: m4497147{at}msic.med.osaka-cu.ac.jp


   Abstract
Top
 Abstract
Introduction
 Methods
 Results
 Discussion
 References
 
Aims: In this study, we investigated the relationship between longitudinal morphology reconstructed from pre-intervention intravascular ultrasound (IVUS) images and thrombolysis in myocardial infarction (TIMI) flow grade at initial angiograms in the acute phase of acute coronary syndrome (ACS).

Methods and results: Our patient population comprised 72 ACS patients in whom we obtained successful reconstructed longitudinal images. On the basis of the site of the maximum aperture of rupture in the longitudinally reconstructed IVUS images, patients were divided into three groups: plaques with rupture in the proximal shoulder (proximal type; n = 28), mid-portion (mid-type; n = 18), and distal shoulder (distal type; n = 26) of the plaque. There were no differences in terms of coronary risk factors or the angiographic findings. The proximal-type group more frequently showed TIMI 0 on initial angiogram (proximal type, 86%; mid-type, 50%; and distal type, 31%; P = 0.002). A multivariable logistic regression model revealed that the presence of a proximal-type rupture correlated with the presentation of ST-elevation myocardial infarction (P = 0.019; odds ratio, 8.12; 95% CI, 1.404–49.996).

Conclusions: Longitudinal morphological features in a ruptured plaque may affect the formation of obstructive thrombus in ACS. Our results suggest that longitudinal morphology may be an important determinant of coronary artery occlusion.

Key Words: Plaque • Thrombus • Imaging • Angiography


   Introduction
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 Abstract
 Introduction
Methods
 Results
 Discussion
 References
 
Plaque rupture and secondary thrombus formation play key roles in the onset of acute coronary syndrome (ACS).1 Many post mortem and in vivo studies have addressed in cross-section the morphology of plaque rupture.2–10 It is suggested that coronary flow is closely related to obstructive thrombus formation and that the longitudinal morphology of plaque rupture also affects the coronary flow. We have previously reported that pre-intervention intravascular ultrasound (IVUS) can accurately identify lesion morphology, including the features of plaque rupture, in acute myocardial infarction (AMI).11,12 In this study, our aim was to investigate the relationship between longitudinal lesion morphology and thrombolysis in myocardial infarction (TIMI) flow grade on initial angiograms in the acute phase of ACS.


   Methods
Top
 Abstract
 Introduction
 Methods
Results
 Discussion
 References
 
Subjects
Our population was drawn from 131 consecutive first-episode ACS patients (with or without ST-segment elevation) who were admitted to Baba Memorial Hospital from September 2003 to December 2005 and underwent pre-intervention IVUS within 24 h of admission. We found plaque ruptures at culprit sites in 74 (56%) of these patients. At this point, we constructed three-dimensional IVUS images of the culprit vessels and excluded two patients in whom we were unable to obtain adequate longitudinal IVUS images. In this way, we ultimately arrived at a population of 72 ACS patients who were enrolled in the study.

This study complies with the Declaration of Helsinki. The protocol for the study was approved by the Ethics Committee of Baba Memorial Hospital. We also obtained written informed consent from all participants prior to initial coronary angiography.

Coronary angiography
In all patients, coronary angiography was performed using a 6F Judkins-type catheter via the femoral approach. All patients received an intravenous bolus injection of 10 000 IU of heparin and intracoronary isosorbide dinitrate (2 mg) before angiography.

Coronary angiograms were reviewed separately by two independent observers (M.N. and T.S.) who unaware of the IVUS findings. Perfusion degree was evaluated according to TIMI criteria13 and collaterals were graded according to Rentrop’s classification,14 with good collateral flow defined as Grade 2 or 3.

Intravascular ultrasound imaging protocol
After completion of diagnostic coronary angiography, and before any intervention, all patients were evaluated with IVUS. The IVUS catheter (3.2F Ultra cross, 30 MHz, or 2.9F Atlantis, 40 MHz, Boston Scientific Corporation/SCIMED, Maple Grove, MN, USA) was carefully advanced distal to the lesion under fluoroscopic guidance. It was then pulled back automatically from the distal portion at 0.5 mm/s, facilitating the observation of the lesion. IVUS images were recorded on S-VHS video for off-line analysis.

The images were digitalized and analysed with commercially available software for longitudinal reconstructive IVUS image analysis (Netra IVUS, ScImage Inc., Los Altos, CA, USA). While pulling back the catheter, we manually infused a contrast medium suitable for IVUS imaging,11 carefully observing the lesion.

Intravascular ultrasound image analysis
The longitudinal morphological features detected using IVUS images were interpreted by two independent experienced observers (A.T. and K.S.) who unfamiliar with the angiographic and clinical data. Evaluation of two-dimensional lesion morphology and other measurements during IVUS was done according to the American College of Cardiology Clinical Expert Consensus Document on Standards for Acquisition, Measurement and Reporting of Intravascular Ultrasound Studies (IVUS).15 A lipid pool-like image was defined as a pooling of low-echoic material or echolucent material covered with a high-echoic layer.12 Incidence of lesion external elastic membrane-cross-sectional area (EEM-CSA) larger than the proximal reference EEM-CSA was defined as positive remodelling. We defined IVUS plaque rupture lesions as follows1: lesions with fissure/dissection2 or lesions without fissure/dissection but in which injection of saline or contrast medium confirmed a communication between the plaque and the coronary artery lumen.16

Longitudinal images were classified using the following criteria:

  • Proximal-type rupture: the centre of the largest ‘aperture’ of the ruptured plaque is located within one-third of the distance from the proximal edge of the ruptured plaque.
  • Distal-type rupture: the centre of largest ‘aperture’ of the ruptured plaque exists is located within one-third of the distance from the distal edge of the ruptured plaque.
  • Mid-type rupture: all other rupture types including cases where no main ‘aperture’ could be identified.
To assess the validity of this classification, Observer 1 (A.T.) repeated the analysis one month after initial assessment and also compared the results to find the agreement with that of Observer 2 (K.S.).

Representative examples of each type of rupture are shown in Figure 1. Using these classification criteria for the longitudinal morphological features of ruptured plaques, the patients were divided into three groups: a proximal-type (n = 28), a distal-type (n = 26) and a mid-type (n = 18) group.


Figure 1
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  		Figure 1 Representative three-dimensional intravascular ultrasound images of each longitudinal rupture type. (A) A proximal-type rupture. The aperture of a ruptured plaque is open-wide against the direction of coronary flow like an alligator waiting for its prey (white arrow). (B) A mid-type rupture. The aperture of a ruptured plaque open at the centre of the plaque. The contents of the ruptured plaque have been washed out and a large ulceration cavity is visible (white arrow). (C) A distal-type rupture. The aperture of a ruptured plaque open along the direction of the coronary flow. The flap of the rupture has been suppressed by the flow and the aperture of the rupture minimized (white arrow)

 
High-sensitive C-reactive protein assay
Blood samples were centrifuged, and serum removed and stored at –80° until assay could be performed. High-sensitive C-reactive protein (hs-CRP) was analysed using a commercially available testing kit (N-Latex CRP II, Dade Behring Marburg Gmbh, Marburg, Germany).

Statistical analysis
Statistical analysis was performed using StatView 5.0J (Abacus Concept, Inc.). The results are expressed as mean ± SD for continuous variables. Times from onset to angiography are expressed in mean and interquartile ranges.

Qualitative data are presented as n (%). Continuous variables have been compared using the one-way ANOVA test, and categorical data with the {chi}2 test. Time from onset to angiography was compared using the Kruskal–Wallis test. The agreement between intra-observer and inter-observer results was assessed using kappa statistics. A multivariable logistic regression model was used to determine predictors of ST-elevation MI. Independent variables included in the model were age, gender, history of systemic hypertension, history of diabetes mellitus, history of hypercholesterolemia, hs-CRP, time from onset to angiography, superficial calcium, arterial remodelling, plaque volume, ulceration cavity volume, and longitudinal structural form. All statistical tests were two-sided. In addition, because of the explanatory nature of the study, experimental type I errors were not considered. A P-value of <0.05 was considered statistically significant.


   Results
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 Abstract
 Introduction
 Methods
 Results
Discussion
 References
 
Patient characteristics
The patient characteristics of each group are summarized in Table 1. There were no differences in terms of age, sex, or classic coronary risk factors among the three groups. ST-elevation MI was observed more frequently in the proximal-type group than in the other two groups (P = 0.03). Hs-CRP was similar in each group.


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  		Table 1 Patient characteristics

 
Angiographic results
Angiographic findings are summarized in Table 2. There were no significant differences in the angiographic findings, nor were there any differences in time from onset to angiography in the three groups. However, the frequency of patients with TIMI 0 at initial angiography did differ in the three groups. As can be seen in Figure 2, the proximal-type group more frequently showed TIMI 0 on initial angiogram (proximal type, 86%; mid-type, 50%; and distal type, 31%, P = 0.002).


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  		Table 2 Angiographical findings

 

Figure 2
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  		Figure 2 Frequency of each TIMI flow grade in each rupture group. Proximal-type ruptures more frequently presented TIMI 0 flow grade while there was even distribution of TIMI flow grades among our distal-type rupture patients

 
Intravascular ultrasound findings
Coronary artery rupture sites were successfully observed in all patients with IVUS without any serious procedural complications. Our pre-intervention IVUS findings are summarized in Table 3. In our longitudinal classification analysis, both intra- and inter-observer agreement was 97% ({kappa} = 0.96; 95% CI, 0.90–1.0) . We observed proximal-type ruptures in 28 (39%) patients, mid-type ruptures in 18 (25%) patients, and distal-type ruptures in 26 (36%) patients. The mid-type ruptures presented with significantly larger ulceration cavities than the other types of rupture (proximal type, 1.8 ± 2 mm3; mid-type, 6.7 ± 9 mm3; and distal type 3.1 ± 5 mm3; P = 0.01).


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  		Table 3 Pre-intervention IVUS findings for culprit lesions

 
Multivariable analysis for presentation with ST-elevation myocardial infarction
We compared age, sex, coronary risk factors, history of pre-infarction angina, CRP, time from onset to angiography, lesion location, good collateral flow, arterial remodelling, and superficial calcium etc. between ST-elevation MI and non-ST-elevation MI subjects. However, there were no significant predictive factors for ST-elevation MI and non-ST-elevation MI. Therefore, we included only clinically meaningful factors for ST-elevation MI in our multivariable models. Since the result of a likelihood ratio test between lesions with and without a longitudinal morphology factor (as a three-level factor) was statistically significant (P = 0.01), we included longitudinal morphology as a factor in this model as a pair-wise comparison.

Our multivariable logistic regression model revealed that the presence of a proximal-type rupture alone correlated with presentation with ST-elevation MI (P = 0.019; odds ratio, 8.12; 95% CI, 1.404–49.996). These data are summarized in Table 4.


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  		Table 4 Multivariable logistic regression model for ST-elevation myocardial infarction

 

   Discussion
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 Abstract
 Introduction
 Methods
 Results
 Discussion
References
 
Longitudinal morphology and coronary flow in acute coronary syndrome
To the best of our knowledge, few in vivo studies have dealt with the relationship between the longitudinal structural form of plaque rupture and coronary flow in patients with ACS.17 Seimiya et al. found that proximal plaque rupture was observed more frequently in AMI than in unstable angina.

Previous studies from cross-sectional views have suggested that plaque rupture occurs most frequently at the point where the fibrous cap is thinnest and most heavily infiltrated by macrophage foam cells. These rupture-related macrophages are activated, indicating ongoing inflammation at the site of plaque disruption. Macrophages are capable of degrading the extracellular matrix by phagocytosis or by secreting proteolytic enzymes such as plasminogen activators and the family of matrix metalloproteinases that may weaken the fibrous cap, predisposing it to rupture.18

In vitro studies indicate that low endothelial shear stress up-regulates the genetic and molecular responses leading to the initiation and progression of atherosclerosis, and promotes inflammation and formation of other features characteristic of vulnerable plaques.19,20 After plaque rupture, the contents of the lipid core that appear in the plaque rupture, most probably the most thrombogenic components of the plaque, are exposed to coronary flow and thrombus formation ensues.21

In this study, all 72 patients presented with plaque rupture and we observed no differences in CRP that might reflect the intensity of the inflammatory response, or in the cross-sectional IVUS parameters among our three groups. Initially, the inflammatory process towards plaque rupture and catastrophic cascade after rupture may occur equally in all patients. However, in our patients, only the presence of a proximal-type rupture correlated with the presentation of ST-elevation MI.

We suspect that antegrade coronary flow causes the flap of the ruptured plaque in the proximal-type rupture to ‘roll up’ back across the rupture site, extending the ‘aperture’ of the ruptured plaque across the plaque. More of the thrombogenic contents of the lipid core are then exposed to coronary flow, compared with other rupture types. This wider exposure of the plaque contents may result in more rapid thrombus formation and even total occlusion of the coronary artery.

We also found that the volume of the ulceration cavity (taken as the volume of washed-away plaque contents) was largest in mid-type ruptures. This finding raises the possibility that rapid thrombus formation arises not only from the wider exposure of the plaque contents but also on the rolled-up flap itself, which may disturb coronary flow in proximal-type ruptures.

However, antegrade coronary flow can suppress the rolling-back of the flap in distal-type ruptures. In these, the aperture of the ruptured plaque may be smaller than that in proximal-type ruptures, meaning that thrombus formation may occur more slowly. Furthermore, coronary flow may flush away the plaque contents. In patients with a distal-type rupture, thrombus formation after plaque rupture may therefore be dependent on not only exposure of the plaque contents but also on a number of other variables, including platelet activity,22 blood viscosity,23 haemodynamic shear stress,24 and/or time from onset to angiography.9 The fact that the number of patients presenting each of the TIMI flow grades was similar in our distal group supports our hypothesis.

Clinical implications
Although we enrolled symptomatic ACS patients presenting with plaque rupture in this study, the presence of a proximal-type rupture alone correlated with the presentation with ST-elevation MI. We reported in a recent study that multiple plaque rupture occurs in 23% of first AMI patients.25 Several studies also have demonstrated multiple plaque rupture in the entire coronary tree and adjacent to the culprit lesion and many ruptured plaques do not cause clinical events.26,27 We hypothesize that the longitudinal location of the plaque rupture may determine whether the plaque rupture leads to serious clinical events as a result of occlusion of the coronary artery.

Our results show the importance of longitudinal morphology to understand plaque rupture. Some IVUS studies have raised the possibility of detecting vulnerable plaques using not only two-dimensional images but by stress mapping in longitudinal views or three-dimensional tissue characterization.28–30 Our results suggest that we should pay more attention to the three-dimensional structural form of plaque rupture to further our understanding of the aetiology of ACS.

Study limitations
There can be said to be a number of limitations associated with the present study. We excluded patients with poor three-dimensional IVUS images. The size of our study population was also admittedly, relatively small. Lesions containing small ruptured plaques may have been misread as non-ruptured plaques. Although the structure of plaque rupture is very complex in three-dimensional images, in this study, we have only used a simple classification taken from the longitudinal view. There is of course the possibility that the initial passage of the IVUS catheter may damage the shoulder of the plaque, and this damage is more likely to occur at the proximal shoulder than at the distal one.

Also, an occluded artery is devoid of pressure and undergoes elastic recoil with a marked reduction in all volumetric measurements; therefore, positive remodelling and its assessment can be substantially influenced by either the presence or the absence of physiological pressure in the artery. According to our criteria, plaque ruptures with larger ulcerations and cavities may often be assigned to the mid-type class. Therefore, we must concede that our identification of larger ulceration cavities in our mid-type group may be partly because of our definition of the rupture types. Also, thrombus exists at the culprit site in the acute phase of ACS and it is difficult for IVUS to distinguish thrombus from plaques. In our patients, the ulceration cavity volume was smaller than that in a previous study by Goessl et al.31 We speculate that this difference may be because of dissimilarities in our relative patient populations and selection policies. There is a possibility that the plaque volumes reported in this study have misrepresented actual plaque volumes.

Conflict of interest: none declared.


   References
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 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 

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A. Tanaka, T. Imanishi, H. Kitabata, T. Kubo, S. Takarada, T. Tanimoto, A. Kuroi, H. Tsujioka, H. Ikejima, S. Ueno, et al.
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