Correspondence *Cardiology Division, Gray/Bigelow 800, Massachusetts General Hospital, 55 Fruit Street, Boston, MA 02114, USA

Email ijang@partners.org

Introduction

The ability to recognize and interpret what we see in medicine, from a patient walking into the clinic to the microscopic evaluation of tissue, remains a fundamental skill. Our understanding of atherothrombotic diseases has developed from the study of postmortem specimens to the quantification of cholesterol accumulation and the dynamic processes involved in reversible endothelial dysfunction, remodeling, apoptosis and thrombotic occlusion.¹ Although stable coronary artery disease (CAD) is exemplified by large, flow-limiting plaque with a demand–supply imbalance, acute coronary syndromes frequently arise consequent to rupture of an angiographically moderate plaque with occlusive thrombus formation.² Plaques prone to rupture have certain characteristics and are often referred to as vulnerable or high-risk plaques (Figure 1). Such plaques contain a large lipid pool, often covered by a thin fibrous cap, typically less than 65 m thick.³ Increased macrophage density is also seen, especially in the shoulder regions. Since these important characteristics are microstructural changes, a high-resolution imaging method will assist in the identification of vulnerable plaques.

Figure 1 Histology of vulnerable coronary plaques seen on Movat's pentachrome staining.

(A) The lumen is substantially occluded by an eccentric plaque (magnification 40). (B) Plaque leads to concentric luminal narrowing; the asterisk indicates a focal area of lipid accumulation and the overlying cap is thin. Of note, the preserved luminal area causes detection difficulties for coronary angiography and other forms of luminography. (C) A higher-magnification image of the boxed area in B showing the lipid pool (^*) and thin fibrous cap (arrow) more clearly.

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Coronary angiography is the established imaging technique for assessment of atherosclerotic plaques, but essentially produces a two-dimensional luminogram with minimal details of the vascular wall. Despite the use of orthogonal imaging, more precise definition of the coronary plaque is not possible. Moreover, positive remodeling and diffuse disease can make localization of a normal reference segment impossible. This inability to better identify the coronary vessel pathology becomes more pressing when we consider that most vulnerable plaques are minor and nonocclusive.

New techniques have been introduced, therefore, to overcome these limitations and to facilitate identification of the vulnerable plaque. Intravascular ultrasound (IVUS) was a significant development and allowed the visualization in vivo of what was previously seen only at postmortem. Image resolution, however, remains a fundamental issue. The development of optical coherence tomography (OCT) as a complement to IVUS might overcome this major obstacle and aid in the study of coronary atherosclerotic pathophysiology. In this article, we discuss how OCT is opening new doors to our understanding of cardiovascular diseases.⁴

The technology

Most cardiologists are familiar with the principles of ultrasound imaging. An understanding of OCT technology is facilitated by analogy to that technique, although ultrasonography uses acoustic waves and OCT relies on NEAR-INFRARED ELECTROMAGNETIC RADIATION. High-resolution cross-sectional images are obtained according to the principle of LOW-COHERENCE INTERFEROMETRY (Figure 2).⁵ This technique compares the echo time delay of the reflected light to that traversing a reference path of known length, which allows precise measurement of distance. For OCT, a reference wave is combined with a sample wave and changes in the path length between the two waves enable reconstruction of reflectivity in tissue to represent depth. In addition, the intensity of the back-reflected light can be measured and quantified digitally in grayscale, enabling the creation of a digital image. Near-infrared light with a wavelength of 1300 nm is used because visible light, which has a shorter wavelength, is prone to a higher degree of scattering and absorption. Conversely, use of a wavelength that is too long will result in unacceptable absorption attenuation because of vibrational transitions in water. At 1300 nm, spatial resolution of 4–16 m is achieved with a penetration depth of 2–3 mm. This resolution compares well with the spatial resolution of 130 m and ultrasound frequency of 40 MHz achievable with IVUS. A resolution of 1 m can currently be achieved, but only with state-of-the-art lasers as light sources.⁴ Improved resolution, which might be a feasible option with OCT, is critical for the identification of high-risk plaques, because many features thought to confer risk in plaque are in the microscopic size scale. The image acquisition time for OCT is approximately 200 ms, during which time high-resolution imaging can be obtained without significant motion artefacts.

Figure 2 Schematic of optical coherence tomography system.

The pulse of low-coherence light from the laser source is split 50/50 to send half the beam to the tissue sample and the other half to a reference moving mirror. Light reflected from the tissue is combined with light returning from the mirror, which moves a microscopic distance. Constructive interference results when the path length of light to the mirror and back equals that of light reflected from the tissue. The mirror position, therefore, gives a measure of the depth within the tissue sample where reflection took place.

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History and development

OCT technology was first described in the early 1990s and its clinical potential was originally recognized in ophthalmology, where it allowed precise imaging of the retina.⁶ The extension of OCT imaging to other fields followed, and current indications include the detection of neoplastic changes in Barrett's esophagus and in the skin.^{7, 8} In cardiology, the potential of OCT in the evaluation of atherosclerosis was recognized in the mid-1990s, and it began to be used for the first time in humans undergoing catheterization in 2000.^{9, 10}

OCT was first performed with modified commercially available IVUS catheters in which the core was replaced with an optic fiber and a gradient index lens with a microprism at the distal tip, resulting in a focused output beam perpendicular to the catheter axis. The mechanical properties of this catheter were similar to the 3.2 French IVUS catheter.¹¹ The OCT imaging probe still consists of a single optical fiber with a microlens and microprism at its distal end, although the probe size has been refined.¹² Proximally, the catheter was affixed to a hand-held rotational coupling unit compatible with the requirements of the catheterization lab. A 10 cc saline flush was performed through the guiding catheter immediately before imaging, which permitted clear image acquisition for 2 s.¹⁰ This need for repeated saline flushes limited its use to short, predefined segments of the coronary artery. Alternative catheter designs included optics that were incorporated into a standard 0.014 in (0.36 mm) coronary guide wire, but these imaging devices also required saline infusion to obtain a clear view of the vessel wall. New catheter designs and OCT technology are currently being developed to address this limitation.

Ex vivo validation

The characterization of human atherosclerotic plaques with OCT was first detailed in 2002 in 357 ex vivo postmortem atherosclerotic segments from 90 cadavers.¹³ This study established OCT criteria for the various plaque components and enabled the identification of the three types of histologic plaques: fibrous, fibrocalcific and lipid-rich. Fibrous plaques are characterized by homogeneous signal-rich regions. Calcification manifests as sharply delineated, homogeneous, signal-poor zones (Figure 3). Lipid pools are similarly signal-poor, but are poorly delineated with respect to the surrounding tissue. The lipid-rich plaque can be recognized, therefore, by the presence of large areas of ill-defined, signal-poor regions. With use of histology as the gold standard reference, high sensitivity and specificity have been obtained for the detection of both calcific and lipid-rich plaques (96% and 97%, and 90% and 92%, respectively).

Figure 3 In vivo optical coherence tomography images of different coronary plaque types compared with intravascular ultrasonography of the corresponding sites.

(A) Fibrous plaque: from 9 o'clock to 2 o'clock, the three-layer structure of a typical intimal hyperplasia is shown and a magnified area is shown in the box. A homogeneous, signal-rich pattern indicates fibrous plaque (F), which is partly obscured by a guide wire artefact (^*). (B) Fibrous plaque: the intravascular ultrasound image corresponding to A. (C) Calcific plaque: a signal-poor region surrounded by sharp borders represents calcific plaque, which is clearly delineated (arrows). (D) Calcific plaque: on the corresponding intravascular ultrasound image calcium is easily identified but the strong signal obscures the structure in front of the calcium deposit and a back-shadow artefact obscures that behind the deposit. (E) Lipid-rich plaque: a signal-poor region (arrow in inset) surrounded by diffuse borders and separated by a signal-rich layer (arrow heads in inset) is consistent with lipid-rich plaque. The plaque is partly obscured by a guide wire artefact (^*). (F) Lipid-rich plaque: the corresponding intravascular ultrasound image suggests a superficial echolucent region. Adapted, with permission, from reference 10 © (2002) American College of Cardiology Foundation. a, adventitia; i, intima; m, media.

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In addition to the characterization of the basic anatomy of the arterial wall, OCT has also been shown to both detect and quantify the number of macrophages in atherosclerotic plaques.¹⁴ Twenty-six lipid-rich atherosclerotic coronary arteries were evaluated using OCT within 72 h of death and compared with immunohistologic stains of the corresponding segments. A good correlation (r = 0.84, P <0.0001) was reported between OCT and histologic measurements of fibrous cap macrophage density. At a threshold of 10% for macrophage content, sensitivity and specificity of OCT were both greater than 90% for the detection of macrophages within atherosclerotic plaques (Figure 4). This ability of OCT to detect macrophages is due to the direct correlation of strong back deflections to macrophage density within atherosclerotic caps.

Figure 4 Low and high magnification of optical coherence tomography and corresponding histology images.

(A) and (B) Optical coherence tomography with macrophages showing as areas of high-intensity signal beneath the intima. (C) and (D) Corresponding histology findings for A and C, showing CD68 immunoperoxidase staining. Arrows indicated macrophage accumulation. MAC, macrophage accumulation.

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Classically, thin-cap fibrous atheroma manifests as a thin signal-rich band (representing the fibrous cap) overlying a large signal-poor region. OCT is able, therefore, to precisely characterize the histologic features of the vulnerable plaque: a large lipid pool, a thin fibrous cap (65 m), and macrophages near the fibrous cap.^{1, 15, 16}

Human studies

Plaque characterization

Among patients presenting with the various clinical coronary syndromes, OCT has been shown to provide detailed in vivo characterization of coronary plaque morphology (Figure 5A, B).¹⁷ In this study, patients with recent acute ST-segment elevation myocardial infarction, acute coronary syndromes (including non-ST-segment elevation myocardial infarction and unstable angina), and stable angina pectoris, underwent coronary angiography and concurrent OCT imaging. Patients with an acute coronary event had discernible plaque characteristics compared with patients with stable angina pectoris. In particular, there was a higher frequency of thin cap fibroatheroma (defined as plaques with lipid content in 2 quadrants on cross-sectional analysis and fibrous cap thickness of 65 m) among patients with ST-segment elevation myocardial infarction and acute coronary syndromes than among patients with stable angina (72%, 50% and 20%, respectively; P = 0.012). This study affirmed that OCT is capable of providing detailed coronary microstructure in patients. This information will ultimately lead to a better understanding of the mechanisms of coronary artery disease.

Figure 5 Selected optical coherence tomography images of clinically relevant atherosclerosis-related situations.

(A) An irregular, homogeneous material adherent to the vessel wall is consistent with a thrombus. (B) Plaque disruption (arrows) in a patient with an acute coronary event. Adherent thrombus (T) is also present. (C) Intravascular ultrasound image of a stented coronary artery. (D) Optical coherence tomography image corresponding to C. Although intravascular ultrasound documents a well-deployed stent, the detailed structure between stent struts is not well visualized. By contrast, optical coherence tomography clearly shows tissue prolapse between stent struts (12–3 o'clock), in which low signal intensity suggests a plaque with a large lipid content. Adapted, with permission, from references 40–42 © (2001, 2002, 2003) Lippincott, Williams & Wilkins.

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OCT has been used to investigate the hypothesis that increased systemic or multifocal arterial inflammation is an independent risk factor for acute coronary events.¹⁸ OCT imaging of 225 plaques from 49 patients revealed an increase in both multifocal and local macrophage densities in patients presenting with an acute coronary event. This work also showed that macrophage concentrations were higher focally at rupture sites and at the surface of plaques in culprit lesions of acute patients. By elucidating the focal and generalized inflammatory features found in patients with different clinical presentations, this study expanded our understanding of coronary artery disease and provided evidence supporting both the vulnerable plaque and vulnerable patient hypotheses.^{19, 20}

Current limitations of oct

OCT needs a blood-free imaging field because red blood cells scatter light. The required saline flushes limit scan times to approximately 2 s per flush, and restrict the length of vessel segments that can be imaged. Other new technologies employing balloon occlusion for a static saline column, or continuous saline flush, may allow for scanning of longer vessel segments. This approach results in transient ischemia, however, which might not be tolerated. Conversely, the presence of side branches could affect clearing of the blood field. Index matching is another possible solution and is based on the hypothesis that the predominant source of scattering in blood is the difference in refractive index between the cytoplasm of erythrocytes and serum. Hence, setting the refractive index of serum at a value similar to the cytoplasm could substantially reduce scattering.²⁴ A possible future alternative approach is isovolumic replacement of blood with an optically transparent hemoglobin-based blood substitute, which has been tested in mouse myocardium.²⁵

While conventional OCT systems have a sampling rate of just 4–16 frames/s, new technology—termed optical frequency domain imaging (OFDI)—has been developed that allows high-speed acquisition and real-time imaging, which reduces motion artefacts and allows screening of larger tissue volumes.²⁶ This technology will probably replace older OCT systems as it increases sensitivity while using a lower power source. The limited depth range of OCT remains a limitation, however. Reliable delineation of morphologic structures is currently restricted to a radius of 3–4 mm. Visualization of the complete plaque is not, therefore, possible, especially when the catheter is not immediately adjacent to the vessel wall. This problem has been solved by two techniques: the first, termed autoranging, adaptively adjusts the OCT system optics to follow the lumen of the arterial wall;²⁷ the second, use of OFDI systems, will allow greater depth range than conventional OCT. The penetration depth of OCT is a fundamental limitation that is based on the sensitivity of the device. In conventional OCT systems, this penetration depth ranges from 1–3 mm, dependent on tissue type. Evaluation of pathologies beyond the internal elastic lamina is difficult, meaning that OCT is unlikely to be used as a stand-alone tool for the assessment of processes such as remodeling. Most features of coronary arteries relevant to plaque vulnerability are, however, superficial and readily evaluated by OCT. Finally, while detailed anatomic visualization is achieved by this technique, its ability to provide physiologic and functional information has not yet been demonstrated in human coronary arteries.

OCT shares the same inherent limitations of all intravascular imaging modalities, which include the risks associated with an invasive procedure (Table 1). Local tissue heating is a theoretical concern but has not been observed to be a problem in the studies done so far. The future incorporation of OFDI, which employs a lower power source, should also help to protect against tissue heating. Population screening is not possible, therefore, and only local information is obtainable despite the increased acceptance that atherosclerosis is a systemic disease involving multiple vascular beds. In addition, because of cardiac motion and the uncertainty of precise catheter localization, repeat sampling of the same site is difficult. No local therapy is yet established and these invasive diagnostic techniques remain, therefore, largely in the realm of research.

Table 1 Comparison of current invasive imaging methods.

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Future technical developments

The introduction of fluorescence probes that emit in the near-infrared region have opened up a vista for in vivo molecular imaging.²⁸ In this region, photons are absorbed minimally by tissues and, therefore, allow improved penetration and safe delivery of optical powers. The use of near-infrared dyes with absorption characteristics within the OCT source spectrum may enhance contrast and further improve the information attainable at depth.^{29, 30} Such dyes could include new-generation nanoparticles with improved optical properties and reduced susceptibility to chemical and thermal denaturation. Additionally, the use of near-infrared absorbing nanoparticles could potentially serve as thermal therapy.³¹ This combination of biophotonics and nanotechnology offer the feasibility of new strategies in the detection and therapy of atherosclerotic disease.

One exciting development is the possibility of physiologic evaluation in addition to anatomic information. Currently, the commercial Doppler-based JoMetrics FloWire® system (Volcano Corporation, Rancho Cordova, CA, USA), allows flow measurements at the distal wire tip and is an established tool in determining the significance of an intermediate lesion and also in the assessment of intervention results.³² Light from a moving particle is Doppler shifted when compared with that from a stationary particle, and thus the direction and velocity of blood flow can be determined. Distinct and complementary information on the physiology of blood flow at the plaque site can hence be gathered. The detection of blood flow with OCT in human skin has recently been demonstrated and a prototype catheter has been described.^{33, 34} The use of this capability could extend the application of OCT in interventional cardiology by adding the ability to obtain both anatomic and physiologic measurements to the interventionist's armamentarium.

Information on the biomechanical properties of the plaque beyond that of structural imaging may also be obtained with OCT. These data are especially relevant given that many plaque ruptures are asymptomatic. A better understanding of which vulnerable plaques result in acute coronary syndromes is critical to determining the optimum treatment of this disease. Elastography is the estimation of biomechanical properties of a tissue using imaging techniques. Because abnormal tissues typically have different biomechanical properties from normal tissues, elastography can be used for the monitoring of pathologic states such as the abnormal weakening of vessel walls. Ultrasound and magnetic resonance elastography are well described, but OCT elastography has been evaluated only for coronary diagnosis.^{35, 36, 37}

The principal advantage of OCT elastography is its high spatial resolution, which allows a precise characterization of the biomechanical properties of tissues. Studies have confirmed the feasibility of this approach, albeit in an ex vivo setting with phantom models.^{38, 39}

Although OCT imaging remains largely a research tool, we expect greater use in routine coronary angiography with the publication of data substantiating its use in the broader population. The introduction of 0.014 in (0.36 mm), wire-based systems will facilitate its use in intervention. The future incorporation of physiologic measurements is expected to improve the preference of OCT over IVUS or pressure or Doppler wire methods because additional information can be obtained without incurring the cost of using separate equipment. We envisage that OCT will complement emerging noninvasive methods such as multidetector CT or MRI, which might in future serve as primary prevention measures in high-risk individuals. OCT might also prove useful in follow-up population screenings with risk-scoring systems or measurement of biomarkers in asymptomatic people at risk of a cardiac event. The patient can then be evaluated further by the use of a variety of noninvasive imaging techniques and ultimately proceed to OCT to better define vulnerable lesions with a view to primary prevention.

Conclusion

OCT is a rapidly evolving technique. Currently it allows detailed structural analysis of the coronary vessel including coronary plaque characterization at the preselected locations. In the future, though, it should be able to provide not only detailed information of the vessel wall over a long segment, but also additional complementary information on flow dynamics and microscopic biomechanical properties. Evolving combined OCT-fluorescence methods and nanoparticle markers could further expand its potential. The combination of all these technologies will allow us to identify vulnerable plaques and lead to therapy that will save lives as well as potentially lower healthcare costs.

Acknowledgments

We thank our research staff at the Cardiovascular Clinical Research Office, and nurses and technologists at the cardiac catheterization laboratories of the Massachusetts General Hospital, MA, USA. Funding for work described was provided by the Center for Integration of Medicine and Innovative Technology, the National Institutes of Health and through a generous gift from Mr and Mrs John and Marilee Polmonari. AF Low is the recipient of a Health Manpower Development Program Fellowship funded by the Ministry of Health, Singapore.

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Subject areas under which this article appears: Imaging and other investigations | Vascular disease