Coronary computed tomography in heart transplant patients: detection of significant stenosis and cardiac allograft vasculopathy,image quality,and radiation dose

Abstract

Background

Cardiac allograft vasculopathy (CAV) is an accelerated form of atherosclerosis unique to heart transplant (HTX) patients.

Purpose

To investigate the detection of significant coronary artery stenosis and CAV, determinants of image quality, and the radiation dose in coronary computed tomography angiography (CCTA) of HTX patients with 64-slice multidetector CT (64-MDCT).

Material and Methods

Fifty-two HTX recipients scheduled for invasive coronary angiography (ICA) were prospectively enrolled and underwent CCTA before ICA with intravascular ultrasound (IVUS).

Results

Interpretable CCTA images were acquired in 570 (95%) coronary artery segments ≥2 mm in diameter. Sensitivity, specificity, and positive and negative predictive values of CCTA for the detection of segments with significant stenosis (lumen reduction ≥50%) on ICA were 100%, 98%, 7.7%, and 100%, respectively. Twelve significant stenoses were located in segments with uninterpretable image quality or vessel diameter <2 mm; only one was eligible for intervention. IVUS detected CAV (maximal intimal thickness ≥0.5 mm) in 33/41 (81%) patients; CCTA and ICA identified CAV (any wall or luminal irregularity) in 18 (44%) and 14 (34%) of these 33 patients, respectively. The mean estimated radiation dose was 19.0 ± 3.4 mSv for CCTA and 5.7 ± 3.3 mSv for ICA (P < 0.001).

Conclusion

CCTA with interpretable image quality had a high negative predictive value for ruling out significant stenoses suitable for intervention. The modest detection of CAV by CCTA implied a limited value in identifying subtle CAV. The high estimated radiation dose for 64-MDCT is of concern considering the need for repetitive examinations in the HTX population.

Keywords

Computed tomography angiography cardiac transplantation

Introduction

Cardiac allograft vasculopathy (CAV) is a major cause of long-term morbidity and mortality in heart transplant (HTX) patients (1). CAV typically appears as diffuse and concentric intimal thickening affecting all parts of the coronary tree, and more infrequently as proximal focal eccentric lesions, as in atherosclerotic disease (2). Most HTX patients undergo annual invasive coronary angiography (ICA) to identify potentially significant stenosis because transplanted hearts are denervated and symptoms of myocardial ischemia often absent. The sensitivity of ICA for detecting CAV is inferior to that of intravascular ultrasound (IVUS) (3). Although IVUS is thought to be the optimal method for early detection, ICA presently serves as a screening tool to grossly detect the presence of CAV (4). Early detection of CAV has prognostic value and is a marker of long-term outcome (5,6).

Coronary computed tomography angiography (CCTA) of HTX patients can be challenging due to high heart rates with a limited response to β-blockers, increased body mass index (BMI), and the frequent manifestation of CAV in small-lumen vessels (2,7). In addition, the need for repeated examinations necessitates awareness of the radiation dose. A modest number of publications have addressed CCTA in the HTX population, and they differ regarding technical aspects and method evaluation (8,9), Only three publications have included IVUS in the evaluation of CAV detection with CCTA (10 –12).

In this prospective study, we sought to perform a comprehensive evaluation of CCTA using a 64-slice multidetector CT (64-MDCT) in a HTX population. We evaluated the detection of significant coronary artery stenosis with ICA as the standard reference and CAV with IVUS as the standard reference. We also assessed the image quality and radiation dose of CCTA.

Material and Methods

Study population

We prospectively enrolled 52 HTX patients aged ≥18 years who were scheduled for annual follow-up including ICA. The exclusion criteria were estimated creatinine clearance <50 mL/min/1.73 m², history of contrast-induced nephropathy or allergy to iodinated contrast agent, pregnancy, severe lung disease, atrial fibrillation, and severe heart failure. The study was approved by the Regional Ethics Committee and all participants provided written informed consent.

The patients’ demographics, medical histories, biochemistry, and medications were recorded during the annual follow-up. Donor data were obtained from medical records. All patients received immunosuppressive therapy as per local protocol, which consisted of maintenance therapy with prednisolone, cyclosporine, or tacrolimus, and azathioprine or mycophenolate mofetil. No cytotoxic induction therapy was given. Statins were used as standard therapy.

CCTA

The participants underwent CCTA 2–4 weeks before their annual ICA. All scans were acquired using a 64-MDCT (GE Light Speed VCT; General Electric Healthcare Technologies, Milwaukee, WI, USA) using retrospective electrocardiographic (ECG) gating and the following scanning parameters: detector configuration = 64 × 0.625 mm; collimation = 40 mm; gantry rotation time = 350 ms; pitch = 0.18–0.24 (heart rate dependent); tube voltage = 120 kV; and tube current = 100–800 mAs (patient-dependent and ECG-modulated). Preceding the CCTA, a prospective ECG-triggered non-enhanced scan was obtained for coronary artery calcium (CAC) scoring.

An intravenous β-blocker was administered before the CCTA if the heart rate was >70 beats per minute (bpm) and no patient-related contraindications were present. The patients received 20 + 80 mL of contrast agent (Visipaque 320; GE Healthcare, Oslo, Norway) injected at 5 mL/s and followed by a 50-mL saline flush; the first 20 mL was a test bolus for calculation of the optimal scan delay. The maximum and minimum heart rates during the scan were recorded and the heart rate variability calculated.

Datasets were reconstructed with a slice thickness of 0.625 mm and an increment of 0.625 mm at 40%, 50%, 60%, 70%, 75%, and 80% of the R-R interval. CCTA image post-processing and calculation of the CAC score were performed on Advantage Windows 4.3 workstation (General Electric Healthcare Technologies, Milwaukee, WI, USA).

ICA and IVUS

ICA was performed following standard hospital procedures with radial artery access. A 6 F introductory sheath was used to facilitate IVUS of one major coronary artery following angiography. After intracoronary administration of 200 µg nitroglycerin, the IVUS examination was performed using a 20 MHz, 2.9 F, monorail electronic Eagle Eye Gold IVUS imaging catheter (Volcano Therapeutics, Inc., Rancho Cordova, CA, USA) and a dedicated IVUS scanner (Volcano Therapeutics). The catheter was placed as distally as possible and mechanical pullback performed from this point to the ostium. Images were acquired at a rate of 30 frames/s during pullback at a speed of 0.5 mm/s.

Analysis of stenosis

Analyses of stenosis were performed on a per-segment basis using the 16-segment classification of the American Heart Association (13) with ICA as the reference standard. Coronary artery segments with a luminal diameter ≥2 mm and image quality score >4 on CCTA were included and graded as normal or a reduction of the lumen diameter of <33%, 33–50%, or ≥50%. Significant stenosis was defined as ≥50% luminal reduction. ICA and CCTA were independently analyzed by two investigators for each modality; all readers were blinded to the results of the other modality. When a discrepancy occurred in the readers’ grading, a consensus reading was performed for each modality. When a discrepancy in stenosis grading occurred between modalities, the anatomy was validated to ensure segments matched.

CAV analysis

With IVUS, CAV was defined as a maximal intimal thickness (MIT) >0.5 mm as suggested by the American College of Cardiology clinical expert consensus document on the standards for acquisition, measurement, and reporting of IVUS studies (14). CAV was defined as any wall irregularity on CCTA and any luminal irregularity on ICA. The most severe lesion was used to classify each segment. Side branches served as anatomic landmarks to separate segments. In the absence of a side branch, the two adjacent segments were analyzed as one segment. Analyses were performed by one investigator for each of the three modalities blinded to the results of the other modalities.

Image quality

The CCTA image quality for each segment was assessed by two independent readers and scored on as: 1 = no artifacts, 2 = minor artifacts, 3 = some artifacts but interpretable, and 4 = uninterpretable (Fig. 1). A middle value was set when there was a one-step discrepancy between the readers. Disagreement regarding grade 4 or a discrepancy in two steps prompted consensus reading. Coronary segments were grouped as proximal (left main, proximal, and middle left anterior descending [LAD] and right coronary artery [RCA], and proximal and distal circumflex [CX]) and distal (distal LAD and RCA, and side branches).

Fig. 1.

Examples of CCTA image quality grading. (a) No artifacts, (b) minor artifacts, (c) some artifacts but interpretable, (d) uninterpretable.

Possible determinants of image quality investigated were BMI, heart rate, heart rate variability, CAC score, attenuation of the aortic root, and image noise. Image noise was defined as the standard deviation (SD) of the attenuation in a region of interest (100 mm²) in the aortic root at the level of the orifice of the left main coronary artery.

Radiation dose

The dose-length product (DLP) for CCTA and CAC CT, and the dose area product (DAP) for ICA was recorded and multiplied by a conversion factor of 0.014 mSv/(mGy.cm) and 0.2 mSv/(Gy.cm²) respectively, to estimate the effective dose (15,16).

Statistical analysis

Categorical variables are presented as frequency (percentage). Continuous variables are presented as mean ± SD or median (interquartile range).

The paired samples t-test was used to compare the mean image quality in proximal and distal segments and the estimated radiation dose for CCTA and ICA. The sensitivity, specificity, positive predictive value (PPV), and negative predictive value (NPV) were calculated for the detection of significant stenosis by CCTA using ICA as the reference, and for the detection of CAV by CCTA and ICA with IVUS as the reference. Linear regression analysis was used to evaluate the effects of BMI, heart rate, heart rate variability, CAC score, attenuation of the aortic root, and image noise on image quality. All statistical analyses were performed using IBM SPSS Statistics version 21 (SPSS Inc. Chicago, IL, USA). A P value <0.05 was considered significant.

Results

Two of the 52 participants had incomplete CCTA data and were excluded from further analysis, one due to a technical failure during the scan and one due to a storage failure. CCTA was performed 19.3 ± 15.9 days before ICA and IVUS. The clinical characteristics of the patients are presented in Table 1.

Table 1.

Demographics and clinical characteristics of 50 heart transplant recipients.

Characteristic
Male	43 (86%)
Age, years	49.4 ± 13.0
Body mass index (kg/mg)	26.5 ± 4.8
eGFR (mL/min/1.73 mL)	76.4 ± 17.0
Time since HTX (years)	7.4 ± 5.3
Hypertension*	31 (62%)
Diabetes mellitus	1 (2%)
Current smoker	7 (14%)
Cytomegalovirus infection	15 (30%)
Rejection^†	18 (36%)
Etiology of heart failure, coronary artery disease	19 (38%)
Etiology of heart failure, congestive cardiomyopathy	23 (46%)
Male donor	30 (64%)
Donor age (years)	34.3 ± 12.6

Data are reported as number of patients (percentage) or mean ± standard deviation as appropriate.

Hypertension defined as use of anti-hypertensive drugs.

^†Biopsy-proven rejection grade ≥ 2 and/or antibody-mediated rejection.

eGFR, estimated glomerular filtration rate as measured by the MDRD formula; HTX, heart transplant.

Detection of significant stenosis

ICA identified 695 segments. Ninety-eight (14%) of the segments were <2 mm and 27 (3.8%) segments were graded as uninterpretable by CCTA. Thus, 570 segments were included in the performance analysis of CCTA.

Of the 570 included segments, ICA identified one segment (0.2%) with significant stenosis, seven (1.2%) with 33–50% stenosis, 181 (32%) with <33% stenosis, and 381 (67%) normal segments (Table 2). CCTA correctly identified the segment with significant stenosis detected by ICA and 557 segments without significant stenosis. CCTA scored 12 segments ICA scored as <50% stenosis as ≥50% stenosis (Table 2). The sensitivity, specificity, PPV, and NPV of CCTA for the detection of segments with significant stenosis compared to ICA were 100%, 98%, 7.7%, and 100%, respectively. In the 27 segments graded as uninterpretable by CCTA, ICA identified four significant stenoses and two occlusions. Of these, only one lesion was located in a proximal segment (LAD middle segment); this was also the only significant stenosis in the study eligible for treatment. This segment was classified as uninterpretable on CCTA because one part was heavily calcified and partly outside the scan volume (Fig. 2).

Table 2.

Stenosis detection and quantification per segment by CCTA using invasive coronary angiography as the reference standard.*

	Invasive coronary angiography				Total segments (n)
	Normal	Stenosis <33%	Stenosis 33–50%	Stenosis ≥50%	Total segments (n)
CCTA
Normal	249	52	0	0	301
Stenosis <33%	123	100	2	0	225
Stenosis 33–50%	7	23	1	0	31
Stenosis ≥50%	2	6	4	1	13
Not interpretable	8	11	2	6	27
Diameter <2 mm	68	24	1	5	98

Data are number of segments.

Segments graded as normal or with the percentage reduction in lumen diameter.

Fig. 2.

CCTA of a proximal lesion in the middle segment of the left anterior descending artery. The segment was classified as uninterpretable because one part of it was heavily calcified (left image) and partly outside the scan volume (right image).

In the 98 segments with diameter <2 mm, ICA identified two significant stenoses and three occlusions.

CAV detection

IVUS was performed in 42 patients, but one IVUS dataset was lost due to a storage failure. A total of 134 segments were defined in the remaining 41 patients. All of the segments were identified in the corresponding CCTA and ICA examinations. CAV was detected by IVUS in 33 (81%) patients and 74 (55%) segments. Of the 33 patients confirmed by IVUS to have CAV, CCTA and ICA detected 18 (44%) and 14 (34%) cases of CAV, respectively. Of the 74 (55%) segments proven by IVUS to be affected by CAV, 50 (68%) were identified by CCTA and 49 (66%) by ICA (Table 3).

Table 3.

Detection of cardiac allograft vasculopathy (CAV) by CCTA and invasive coronary angiography (ICA) with intravascular ultrasound (IVUS) as the reference standard.

	CCTA detection of CAV		ICA detection of CAV
	Segments	Patients	Segments	Patients
True positive	50	18	49	14
True negative	41	6	36	7
False positive	19	2	24	1
False negative	24	15	25	19
Sensitivity (%)	68	55	66	42
Specificity (%)	68	75	60	88
Positive predictive value (%)	73	90	67	93
Negative predictive value (%)	63	29	59	27

Data are number or percentage as appropriate.

Image quality

The maximum heart rate during CCTA was 75.9 ± 10.0 bpm, the heart rate scan variability was 1 (range = 0–20) bpm, and 40 (80%) patients were given β-blockers, reducing the heart rate by 14 ± 8 bpm. The Agatston coronary calcium score was 1.5 (range = 0–457). Attenuation of the aortic root was 341 ± 66 Hounsfield units (HU) and image noise 28.1 ± 5.8 HU. The mean image quality score per patient was 2.26 ± 0.40. A significant difference was found in the mean quality score between proximal and distal segments (2.03 ± 0.42 vs. 2.66 ± 0.50; P < 0.001). A total of 27 segments in 15 patients were graded as uninterpretable (seven proximal, 20 distal). The image quality on a per segment basis is presented in Table S1 online.

Linear regression analysis revealed an inverse association between image quality and CAC (P = 0.006). For the distal segments, CAC (P = 0.009) and image noise (P = 0.013) were inversely related to image quality (Table S2).

Radiation dose

The DLP for CCTA was 1356 ± 246 mGy.cm and the estimated radiation dose 19.0 ± 3.4 mSv. The scan for CAC scoring had a DLP of 89 ± 16 mGy.cm and an estimated radiation dose of 1.2 ± 0.22 mSv. The DAP for ICA was 28.6 ± 16.4 Gy.cm² and the estimated radiation dose 5.7 ± 3.3 mSv. The estimated radiation dose for CCTA was significantly higher compared with ICA, P < 001.

Discussion

In the present study, CCTA with interpretable image quality had a high NPV for ruling out significant stenosis suitable for percutaneous coronary intervention (PCI). The value of CCTA for detecting CAV as assessed by IVUS was modest and similar to ICA. The high estimated radiation dose for the 64-MDCT is concerning, as HTX patients undergo repeated examinations.

Allograft transplant vasculopathy is one of the most important causes of death after the first year following HTX (1). The total atherosclerotic burden in a HTX patient is a composite of donor-mediated disease, CAV, and de novo atherosclerosis. Although CAV and atherosclerosis each have some typical features (2), the two entities are difficult to differentiate by morphology and distribution (17). ICA provides a planar two-dimensional silhouette of the vessel lumen but is inferior to IVUS in detecting CAV (3). IVUS provides high-resolution cross-sectional images of the arterial wall, enabling the detection of discrete, diffuse CAV at an early stage. Early detection of CAV has prognostic value as a marker of the long-term outcome after HTX (5,6). PCI is performed for suitable discrete lesions, and ICA screening is recommended to detect lesions (4).

Due to its high NPV, CCTA is an effective, non-invasive alternative to ICA for the detection of significant stenosis in the non-transplanted population (18). CCTA has been proposed to be superior to ICA in detecting CAV due to its ability to visualize the coronary wall (9,19). The high NPV found in our study supports CCTA as a non-invasive alternative in a HTX population serving as a gatekeeper for ICA. Other publications addressing the detection of significant stenosis in HTX patients by equivalent (12,20,21) or superior equipment (256-MDCT or dual-source CT) (20,22,23) have reported similarly high NPV (98–100%).

Nevertheless, 4.5% of the segments had uninterpretable image quality and another 14% of the segments with a vessel diameter <2 mm were not evaluated in our study. The number of excluded segments is comparable to other studies (0–19%) (10,12,20 –23). However, most of the excluded segments in our study were in the periphery of the coronary tree, where potential significant lesions are usually unsuitable for revascularization. This was confirmed by the proximal location of the single significant stenosis treated in our study. It should be noted, though, that CAV often affects distal segments of the coronary tree, where CCTA is hampered by limited spatial resolution and image noise.

In general, the prevalence of significant disease is low in all studies on HTX patients (0–3%) (10,12,20 –23). This likely reflects participant selection, as registry data indicate that 30% of the patients are diagnosed with CAV within five years and 50% within ten years after transplantation (1). One obviously important selection factor is renal function, as renal insufficiency is an exclusion criterion for our and the abovementioned studies. According to registry data, a total of 45% of the patients have abnormal creatinine at five years post transplantation and 12% have creatinine ≥2.5 mg/dL (220 µmol/L) (1). Hence, reduced kidney function probably excluded older transplants with more severe CAV from the study.

CCTA had a modest detection rate for CAV, as assessed by IVUS, and at the same level as ICA. Only one previous study evaluated both CCTA and ICA with IVUS-detected CAV. In 20 patients, Gregory (10) found that CCTA using 64-MDCT detected 39 (70%) of 56 segments with CAV, whereas ICA only detected six (11%) segments. Though the ability of CCTA to detect CAV was comparable in our study, the ability of ICA to detect CAV was markedly greater in our study. Schepis (24) evaluated the detection of CAV by dual-source CT using IVUS as the gold standard in 30 patients and found a slightly higher detection rate (35/41 segments, 85%). This may reflect the improved performance of high-end equipment.

In the regression analysis the only significant determinant of image quality was CAC. Mittal found a tendency, but not a significant trend, towards worsening image quality with increasing CAC score (21). In several publications on CCTA in non-transplant populations, CAC significantly reduced the image quality (25 –27).

Radiation exposure is a concern in the HTX population due to repeated examinations and the increased risk of cancer caused by prolonged immunosuppression. The estimated radiation dose in our study was high despite the use of ECG-synchronized tube current modulation. Recent studies by Mittal (21) and Barthélémy (20) reported equivalent radiation doses for 64-MDCT of 17.5 ± 6.9 mSv and 17.8 ± 5.5 mSv, respectively. The high heart rate in HTX patients often prevents the use of dose-lowering techniques or renders them less effective (28). Prospective ECG-triggered sequential scanning is one of the most effective dose-saving strategies (28 –31) but has been limited to heart rates <60–65 bpm (32 –34). With the newest high-end scanners, prospective ECG-triggering can be used in heart rates up to 75 bpm (35,36) or higher (37). Thus, a greater proportion of the HTX population could benefit from this dose-reducing approach. Furthermore, the use of tube voltages below 120 kV reduces radiation exposure (38,39). Novel iterative reconstruction algorithms have demonstrated significant dose reduction with preserved image quality when using lower tube current in CCTA studies in the general population (40,41).

New high-end equipment with faster gantry rotation and either dual source or wide detector, will probably perform at a markedly lower dose and with a higher image quality in the small caliber vessels than a 64-MDCT (20,22), and should, if available, be utilized when examining HTX patients.

Limitations of the present study were the limited number of patients and few significant stenoses. The high frequency of chronic renal impairment reduces the number of available patients and causes selection bias. We chose not to include segments <2 mm to ensure valid results. Inclusion of smaller segments could have increased the number of evaluated peripheral coronary segments in the study. Nitroglycerin was not administered before CCTA. It is possible that its use could have increased the number of included segments and improved the quality of the examinations (42).

In conclusion, CCTA with interpretable image quality had a high NPV for ruling out significant stenoses suitable for PCI, supporting a role as a gatekeeper for ICA in a HTX population. The detection of IVUS-defined CAV by CCTA was modest and at the same level as ICA, implying a limited value of CCTA in detecting subtle CAV. The high estimated radiation dose for 64-MDCT is of concern considering the need for repetitive examinations, and new high-end equipment should preferably be used when examining HTX patients.

Footnotes

Acknowledgements

The authors thank professor Lars Gullestad for his contribution in the planning of the study and in the revision of the manuscript, Satish Arora for his advice on intravascular ultrasound, radiographer Joanna Kristiansen for her contribution in the planning of and for performing the coronary CT angiographies, radiographer Ingrid Erikstad for doing the analysis of the IVUS examinations, and Leiv Sandvik for statistical advice.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: The work received financial support from the South-Eastern Norway Regional Health Authority, unrestricted grants from Inger and John Fredriksen’s Cardiac Research Fund, and Professor Frimann-Dahl’s Fund.

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