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. Author manuscript; available in PMC: 2020 Jul 15.
Published in final edited form as: Am J Cardiol. 2019 Apr 23;124(2):278–284. doi: 10.1016/j.amjcard.2019.04.025

Significance of Coronary Artery Calcium Found on Non-Electrocardiogram-Gated Computed Tomography During Pre-Operative Evaluation for Liver Transplant

Brian H West a, Christopher G Low b, Biraj B Bista c, Eric H Yang a, Gabriel Vorobiof a, Ronald W Busuttil d, Matthew J Budoff e, David Elashoff f,g,h, Jonathan M Tobis i, Henry M Honda a
PMCID: PMC6581589  NIHMSID: NIHMS1529943  PMID: 31122618

Abstract

Guidelines to evaluate patients for coronary artery disease (CAD) during pre-operative evaluation for orthotopic liver transplantation (OLT) are conflicting. Cardiac catheterization is not without risk in patients with end-stage liver disease. No study to date has looked at the utility of non-electrocardiogram (ECG)-gated chest computed tomography (CT) in the pre-liver transplant population. Our hypothesis was that coronary artery calcium scores (CACS) from chest CT scans ordered during the liver transplant workup, can identify patients who would benefit from invasive angiography. 953 patients who underwent coronary angiography as part of their OLT workup were considered. Charts were randomly selected and reviewed for the presence of a chest CT performed prior to coronary angiography during the OLT workup. Agatston and Weston scores were calculated. CACS results were compared to coronary angiography findings. 9 out of 54 patients were found to have obstructive coronary artery disease by angiography. ROC analysis demonstrated that an Agatston score of 251 and a Weston score of 6 maximized sensitivity and specificity for detection of obstructive coronary disease. An Agatston score < 4 or Weston score < 2 excluded the presence of obstructive CAD; using these thresholds, 13 patients (24%) or 15 patients (28%), respectively, could have theoretically avoided catheterization without missing significant CAD. In conclusion, our data identify the strength of CACS in ruling out coronary disease in patients being evaluated for OLT. Calcium scoring from non-ECG-gated CT studies may be integrated into preoperative algorithms to rule out obstructive CAD and help avoid invasive angiography in this high-risk population.

Keywords: coronary artery calcium score, orthotopic liver transplantation, preoperative evaluation, coronary artery disease, cardiac catheterization

Coronary artery disease (CAD) is an important consideration in the pre-operative evaluation of patients for orthotopic liver transplantation (OLT)1–3. However, guidelines to evaluate patients for underlying CAD during preoperative evaluation for OLT are conflicting4–6. Cardiac catheterization is not without risk in end-stage liver disease (ESLD) patients, who are often thrombocytopenic and coagulopathic7,8. It is for these reasons that liver transplant teams rely on non-invasive stress testing prior to OLT2,9,10. These tests are burdened by inaccuracies2,9. The coronary artery calcium score (CACS) has been established as a predictor of coronary artery disease, cardiovascular events, and all-cause mortality11–13, and has been incorporated into the American College of Cardiology Foundation and American Heart Association guidelines for evaluating low to intermediate-risk individuals14,15. However, only limited data are available regarding the utility of CACS in liver transplant patients. Studies have shown an association between traditional CAD risk factors and CACS in liver transplant recipients16,17. CACS have also been predictive of cardiovascular complications within one month of liver transplant18. Two studies have demonstrated an association between Agatston scores from electrocardiogram (ECG)-gated CT scans and cardiac catheterization findings in liver transplant candidates19,20. No study to date has looked at the utility of non-ECG-gated CT scans in the pre-liver transplant population, which are routinely performed to exclude pulmonary pathology or metastatic disease. Little is known about the prognostic significance of CACS from non-gated CT, though limited data has suggested it correlates well with ECG-gated studies21–23. The aim of this study was to determine the predictive value of incidental coronary artery calcium discovered on non-ECG-gated chest CT in the pre-liver transplant population. Our hypothesis was that by retrospectively evaluating CT scans ordered during the liver transplant workup, it may be possible to more accurately identify patients who would benefit from invasive angiography.

Methods

Patients who underwent coronary angiography as part of their liver transplant workup from 2006 to 2015 at a single academic medical center were retrospectively considered. At the time of OLT evaluation, the decision to proceed with angiography was based on a previously published protocol9. Charts were reviewed for coronary interventions performed, including balloon angioplasty, bare-metal stent placement, and drug eluting stent placement. Additionally, charts were reviewed for periprocedural complications, including access site and bleeding events, myocardial infarction, and stroke. Patients were included if information on both interventions and complications were available. Patients with a history of CAD and revascularization prior to liver transplant workup were excluded.

Based on a starting point selected by a random number generator, charts were reviewed for the presence of a non-ECG-gated chest CT performed prior to coronary angiography during the liver transplant workup. Based on data from ECG-gated CT scans in the ESLD population20, it was determined that a sample size of 44 patients would be required to provide 80% power to detect a difference between those with and without obstructive CAD at an α of 0.05. To account for potential dropout from incomplete medical records and/or irretrievable CT images, the minimum target sample size was set at 50 patients.

Using VitreaAdvanced® (Vital Images Inc., Minnetonka, MN), CACS were derived from these non-ECG-gated CT scans [Figure 1]. Agatston scores were calculated for the left main, left anterior descending, left circumflex, and right coronary arteries; these scores were subsequently totaled11. Absolute scores were then further categorized based on standard cutoffs that have been proven predictive of coronary disease24. Agatston scores were also adjusted for age and gender, and patients were classified into percentiles using standard protocols based on data generated from a cohort of over 35,000 patients25. Additionally, a Weston score was calculated for each vessel and summed for each patient [Figure 1]23. Weston scores have been validated against Agatston scores22 and also account for artifact23, which is common in non-ECG-gated studies. CACS results were compared to coronary angiography findings, with significant stenosis considered ≥ 50% diameter stenosis of at least one major coronary artery [Figure 2].

Figure 1:

Figure 1:

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Agatston and Weston calcium scores of LAD lesions seen on non-ECG-gated chest CT

Figure 2:

Figure 2:

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Non-ECG-gated CT coronary calcium versus angiography

Patients without obstructive coronary disease were compared to those who had obstructive coronary disease on baseline characteristics as well as absolute Agatston scores, Agatston score categories, age and gender adjusted Agatston scores, and Weston scores. The Wilcoxon rank sum test was used for continuous variables and Fisher’s exact test was used for categorical variables. Absolute Agatston scores were log transformed due to skewness.

Based on Agatston scores, a receiver operator characteristic (ROC) curve was derived and sensitivity, specificity, positive predictive value and negative predictive value were calculated. ROC analysis was also repeated using Weston scores. The area under the curve (AUC) was compared between the Agatston and Weston scores using DeLong’s test26. The Pearson correlation coefficient between Agatston scores and Weston scores was calculated.

Agatston scores were determined by one reader (BW) for all patients. Additionally, a randomly selected subset of 20 patients also had Agatston scores independently determined by a second reader (BB), to assess interreader reliability. An intra-class correlation coefficient (ICC) was calculated for these scores. Additionally, a Bland Altman plot was created to compare readers for these 20 patients and a Tukey mean difference analysis was performed to assess the degree to which the mean differences between measurements differ from zero.

Results

953 patients who underwent coronary angiography as part of their liver transplant workup from 2006 to 2015 at a single academic medical center were retrospectively considered. Of these 953 patients, 741 (78%) had intervention and complication data available. 70 of 741 patients (9.4%) had at least one coronary intervention performed during their liver transplant workup and 39 of 741 patients (5.3%) had at least one complication as a result of catheterization. The majority of these complications were bleeding events, which were seen in 23 patients. 12 patients had periprocedural myocardial infarctions and 2 patients had periprocedural strokes. 17 of the 39 patients who had complications also had interventions performed.

Review of 308 charts yielded 56 patients who had a non-ECG-gated chest CT performed prior to coronary angiography. Two of the 56 patients had CT images that could not be retrieved and were excluded. Statistical power was achieved with 54 patients included in the final analysis. The median time between the non-ECG-gated chest CT and coronary angiography was 26.5 days (IQR: 7–58 days). 9 out of these 54 patients with non-ECG-gated chest CT studies were found to have obstructive coronary artery disease; the other 45 patients did not have obstructive coronary disease.

There were no significant differences in baseline clinical characteristics between patients with and without obstructive coronary disease [Table 1]. Specifically, these groups did not differ in regard to age, gender, or cardiovascular risk factors. Three patients had a history of coronary artery disease without prior revascularization. There were no significant differences in groups with regard to etiology of liver disease or Model for End-Stage Liver Disease (MELD) score. Additionally, there were no significant differences between groups in baseline INR or platelet counts.

Table 1:

Comparison of patients undergoing liver transplant workup

Variable Obstructive coronary disease Significance
p-value
No
(n=45)		 Yes
(n=9)
Age (years) 64 [59.0,67.5] 67 [53.5, 72.0] 0.59
Female 21 (47%) 3 (33%) 0.72
Hypertension 32 (71%) 6 (67%) 1.00
Hyperlipidemia 8 (18%) 4 (44%) 0.08
Diabetes mellitus 24 (53%) 5 (56%) 1.00
Smoker 15 (33%) 4 (44%) 0.70
Prior coronary artery disease* 2 (5%) 1 (11%) 0.44
Liver disease etiology:
Alcohol 7 (16%) 2 (22%)
Viral hepatitis 26 (58%) 4 (44%) 0.51
Non-alcoholic steatohepatitis 5 (11%) 0 (0%)
Other 7 (16%) 3 (33%)
MELD Score** 22.4 [9.73,32.4] 14.1 [7.9,29.5] 0.35
Creatinine** 1.35 [1.0,3.1] 1.1 [1.0,2.5] 0.68)
International normalized ratio** 1.55 [1.2,2.2] 1.4 [1.0,2.2] 0.53
Platelet count** 50.5 [30.5, 94.5] 84 [46.5, 187] 0.06
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Continuous variables were compared with the Wilcoxon rank sum test, median [inter-quartile range].

Categorical variables were compared with Fisher’s exact test, n (%).

*

Based on data for n=52 patients only.

**

Based on data for n=51 patients only.

Absolute Agatston scores were significantly higher in the group with obstructive coronary disease compared to those without obstructive disease, 311 [144, 1178.5] versus 28 [0,144.5]; p=0.003 [Table 2]. Using a standard cutoff of 40024, patients with obstructive coronary disease were more likely to test positive compared to those without obstructive disease (44% versus 11%; p=0.03) [Table 2]. Similar results were found for adjusted Agatston scores using a standard cutoff of ≥ 75th percentile27 [Table 2]. Weston scores were also significantly higher in the group with obstructive coronary disease compared to those without obstructive disease, 8 [6,10] versus 2 [0,5.5] [Table 2]. Based on standardized categories, Agatston scores were significantly higher in patients with obstructive coronary disease compared to those without obstructive disease, p= 0.006 [Table 3].

Table 2:

Calcium scores by coronary disease

Obstructive coronary disease Significance p-value
No
(n=45)		 Yes
(n=9)
Agatston score 28 [0,144.5] 311 [144,1178.5] 0.003
Agatston score positive* 5 (11%) 4 (44%) 0.03
Adjusted Agatston score positive** 10 (22%) 7 (78%) 0.003
Weston score 2 [0,5.5] 8 [6,10] 0.0005
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Continuous variables were compared with the Wilcoxon rank sum test, median [inter-quartile range].

Categorical variables were compared with Fisher’s exact test, n (%).

*

Positive > 400;

**

Positive ≥75th percentile for age and gender.

Table 3:

Agatston score category by coronary disease

Agatston Score Category Obstructive coronary disease Significance p-value
No
(n=45)		 Yes
(n=9)
0 12 0 0.006**
1–100 18 2
101–400 10 3
>400 5 4
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**

Comparison via the Wilcoxon rank sum test

ROC analysis demonstrated that an Agatston score of 251 maximized sensitivity and specificity for detection of obstructive coronary disease [Figure 3]; using this threshold, sensitivity and specificity were 78% and 87%, respectively. The positive predictive value and negative predictive value were 54% and 95%, respectively. Only two patients (3.7%) with a negative test based on Agatston score < 251 had obstructive coronary disease. Additional ROC analysis demonstrated that an Agatston score of 4 provided 100% sensitivity and a 100% negative predictive value; using this threshold, 13 patients (24%) could have avoided catheterization without missing any obstructive coronary disease.

Figure 3:

Figure 3:

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ROC analysis for obstructive coronary disease

ROC analysis demonstrated that a Weston score of 6 maximized sensitivity and specificity for detection of obstructive coronary disease [Figure 3]; using this threshold, sensitivity and specificity were 89% and 76%, respectively. The positive predictive value and negative predictive value were 42% and 97%, respectively. Only one patient (1.9%) with a negative test based on Weston score < 6 had obstructive coronary disease. Additional ROC analysis demonstrated that a Weston score of 2 provided 100% sensitivity and a 100% negative predictive value; using this threshold, 15 patients (28%) could have avoided catheterization without missing any obstructive coronary disease.

ROC analysis showed the AUC for the Agatston score was 0.82 (95% CI 0.66–0.98) and the AUC for the Weston score was 0.86 (95% CI 0.74–0.99) [Figure 3]; this difference was not statistically significant (p = 0.256). It should be noted that the Weston score did have a slightly higher AUC compared to the Agatston score, suggesting a trend towards better performance in identifying obstructive coronary disease in this population.

There was a strong, positive correlation between Agatston scores and Weston scores for all patients (r = 0.93) [Figure 4]. There was a positive correlation for Agatston scores between both readers (ICC = 0.98). Additionally, by Bland-Altman analysis, there was no significant difference between readers in terms of Agatston scores (p = 0.38)

Figure 4:

Figure 4:

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Agatston score versus Weston score

Discussion

This study demonstrated the predictive value of incidental coronary artery calcium discovered on non-ECG-gated CT in patients undergoing pre-operative evaluation for liver transplant. It also demonstrated that Agatston scores can be applied to non-ECG-gated studies in this population. Additionally, this study showed that Weston scores approximated Agatston scores in predicting obstructive coronary disease. Our results suggest that coronary calcium scoring may be an important addition to the risk stratification of liver transplant candidates.

The most recent recommendations from The American Heart Association and the American College of Cardiology Foundation suggest noninvasive stress testing based on cardiovascular risk factor assessment for patients without active cardiac disease4. However, guidelines from the American Association for the Study of Liver Diseases and the American Society of Transplantation recommend noninvasive cardiac testing for all adults undergoing liver transplant workup5. Alternatively, many cardiologists advocate for invasive angiography in patients with more than two cardiac risk factors prior to listing for OLT6.

Data on cardiac catheterization in ESLD patients raise concerns about safety. Studies have demonstrated higher rates of complications, such as major bleeding and pseudoaneurysm formation, in patients with liver failure compared with control patients undergoing left heart catheterization8. Additionally, the interventional cardiology community recommends the use of special considerations in these patients, such as prophylactic platelet and/or fresh frozen plasma transfusions as well as smaller vascular sheaths7.

In our subgroup of 741 patients with catheterization outcomes data, 22 of 671 (3.3%) who underwent diagnostic angiography and 17 of 70 (24.3%) who had interventions performed experienced complications. These figures are higher than average for all patients who undergo diagnostic and interventional cardiac catheterization, respectively28,29. Although the majority of the complications seen in our population were bleeding events (59% of patient complications), which may be regarded as relatively benign, treatment can be complex in liver transplant candidates due to underlying thrombocytopenia and coagulopathy.

To avoid potential complications, liver transplant teams have turned to pharmacologic stress testing in OLT candidates. In one study of 389 patients undergoing pre-operative evaluation prior to OLT, DSE and SPECT had sensitivities of 9% and 57%, respectively, for perioperative cardiac events2. Similar results were seen in a larger (n=473) study which focused on the use of SPECT imaging in the pre-liver transplant evaluation: We demonstrated a sensitivity of only 62% for adenosine and 35% for regadenoson SPECT, in diagnosing severe CAD and concluded that SPECT was a poor screening test in the pre-OLT population9.

Two studies have demonstrated relationships between ECG-gated CT scans and cardiac catheterization findings in OLT candidates19,20. These studies used only Agatston scores to evaluate patients and were limited in terms of sample size. Data from coronary computed tomography angiography (CTA) have shown a prognostic value similar to DSE and carries the additional risk of contrast dye10. In addition, CTA needs to be gated and can be difficult to obtain in ESLD patients who are often tachycardic. The ability to use non-ECG gated CT exams would facilitate obtaining important non-invasive information about CAD in the ESLD population.

Our data confirm the strength of calcium scoring in ruling out coronary disease in patients being evaluated for OLT. By lowering the threshold for considering a patient to be positive to an Agatston score of 4 or a Weston score of 2, we predicted non-obstructive coronary disease with 100% certainty in our population. This would have prevented 13 (24%) or 15 (28%) catheterizations, based on Agatston or Weston scores, respectively. Using this calcium screen threshold could thereby prevent complications from invasive angiography.

Many liver transplant candidates undergo non-gated, non-contrast chest CT during their workup. We found that 56 of the 308 (18.1%) patients randomly reviewed for this study had a non-gated chest CT ordered within six months of angiography. The most common reason for this was staging for HCC. However, other reasons included history of obstructive or parenchymal pulmonary disease, screening for lung cancer, concern for pulmonary infection, evaluation for pulmonary hypertension or arteriovenous shunt, and to follow up abnormalities on chest x-ray or pulmonary function testing. A limitation of this study includes the potential bias regarding CAD risk introduced by the subgroup of transplant candidates undergoing chest CT. Limited data does suggest similar rates of mild to moderate CAD and pre-operative revascularization in liver transplant candidates with HCC versus those without HCC30.

Other limitations of this study include its retrospective nature and the biases inherent in this design. The associations we found are only hypothesis generating and suggest a need for randomized, prospective studies in the future. Additionally, this study was relatively limited in terms of sample size analyzed due to the retrospective nature of the design and frequency with which non-gated CT was performed during the pre-catheterization time interval. Fortunately, the sample size obtained did fulfill our power requirement and demonstrated a significant difference in coronary calcium between ESLD patients with and without obstructive CAD.

Another specific limitation involves the interpretation of non-gated CT using criteria designed for gated studies. The chest imaging obtained in this study was for non-cardiac purposes and not part of a protocol for cardiac risk stratification, and thus it is difficult to estimate the true prevalence of coronary calcification in OLT candidates. Moreover, many of the images did contain motion artifact, which can falsely elevate the Agatston score. A strength of this study was also including the semi-quantitative Weston score, which is less subject to motion artifact; this may be one of the reasons that the Weston score outperformed the Agatston score in our study. Additional data is needed comparing these scores in non-ECG-gated studies.

Future studies should evaluate whether the addition of a calcium score impacts the preoperative evaluation of liver transplant candidates. The Agatston and Weston score cutoffs established in this paper can be used to prospectively risk stratify patients for angiography. Ultimately, calcium scoring may be integrated into preoperative algorithms to rule out obstructive disease and help to avoid invasive angiography in this high-risk population.

Acknowledgments

We would like to thank the UCLA Specialty Training and Advanced Research (STAR) program for support of this project. This project was funded by NIH grant 5T32HL007895–19 and we would like to thank Dr. James N. Weiss (PI) for his support. We would also like to thank Dr. Tristan Grogan for his help with the statistical analysis on this project. We would like to thank Dr. Stephanie Guo for her pulmonary expertise. We would like to thank Dr. Janet Sinsheimer and Dr. Douglas Bell for their insight into and advice about this project. The research described was supported by NIH/National Center for Advancing Translational Science (NCATS) UCLA CTSI Grant Number UL1TR001881.

Grants, contracts, other financial support:

Brian H. West-NIH grant 5T32HL007895–19; PI: Dr. James N. Weiss

Matthew J. Budoff – Grant support from the NIH and General Electric

Footnotes

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