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Incidental Findings of Pulmonary and Hilar Malignancy by Low-Resolution Computed Tomography Used in Myocardial Perfusion Imaging (FULL)
Single-photon emission computed tomography (SPECT) myocardial perfusion imaging (MPI) is a well-established technique for the evaluation of coronary artery disease (CAD).1 To improve image quality, low-resolution computed tomography (CT) is used commonly for anatomical correct and artifact attenuation during SPECT MPI.2 The low resolution, unenhanced CT images are considered low quality and are, therefore, labeled by the manufacturer as nondiagnostic. The CT portion of the MPI in many centers is used only for image fusion and attenuation correction, and these images are not routinely reviewed or reported by cardiologists.
Incidental findings by these low-resolution CT were frequent. However, clinically significant findings, including lung cancer, although relatively infrequent, were serious enough for major clinical management.3-5 Currently, there are no consensus recommendations for reviewing low-resolution CT images or the interpretation of such incidental findings during cardiac MPI.6 Clinically, low-dose CT were used for early detection and screening of lung cancer and were associated with reduced lung-cancer and any cause mortality in National Lung Screening Trial (NLST).7,8 Therefore, low-dose CT is recommended for lung cancer screening of high-risk patients by the US Preventive Service Task Force (USPSTF).9 In the veteran population, current and past smoking history are more common when compared with the general population; therefore, veterans are potentially at increased risk of lung cancer.10 In this study, we did not intend to use low-resolution CT for lung cancer screening or detection but rather to identify and report incidental findings of pulmonary/hilar malignancy detected during cardiac MPI.
Methods
The Siemens’ (Munich, Germany) Symbia Intevo Excel SPECT/CT MPI cameras with dedicated cardiac collimators were used at both the Dwight D. Eisenhower VA Medical Center (VAMC) in Leavenworth, Kansas and Colmery-O'Neil VAMC in Topeka, Kansas. The integrated CT scanner (x-ray tube current 30 to 240 mA; voltage 110 Kv with a 40 kW power generator) has the capability to image up to a 2-slice/rotation, each of 5.0 mm per slice with a scan time of about 30 seconds. The SPECT/CT gamma camera has a low energy (140 KeV), high resolution, parallel hole collimator with IQ SPECT capabilities.
The radiation dose received by the patients were expressed in dose length product (DLP), which reflects the total energy absorbed by the patient and represents integrated dose in terms of the total scan length. Additionally, each patients received 2 injections of Technetium Tc 99m sestamibi (1-day Protocol: 10 mCi rest injection, 30 mCi stress injection: 2-day Protocol for patients weighing > 350 pounds: 30 mCi at rest injection and 30 mCi at stress injection) for myocardial perfusion imaging.
All CT images and cardiac MPI findings were reviewed and reported contemporaneously by 1 of 2 experienced, board-certified radiologists who were blinded to patients’ clinical information except the indication for the cardiac stress testing. When suspicious pulmonary/hilar nodules or masses were detected, these findings and recommendations for further evaluation were conveyed to primary care provider or ordering physician via the electronic health record system.
All CT images were reviewed with cardiac MPI from September 1, 2017 to August 31, 2018. When pulmonary/hilar malignancies were identified, the health records were reviewed. Patients with known history of prior pulmonary malignancy were excluded from the study.
Results
A total of 1,098 patients underwent cardiac MPI during the study period. When the CT imaging and cardiac MPI were reviewed, incidental findings led to the diagnosis of lung cancer in 5 patients and hilar mantle cell lymphoma in 1 patient. Their clinical characteristics, CT findings, and types of malignancies for these 6 patients are summarized in the Table and Figure. Only 0.55% (6 of 1,098) patients were found to have incidental pulmonary/hilar malignancy with the cardiac evaluation low-resolution CT. Four patients with prior, known history of lung cancer were excluded from the study.
For the 6 patients found to have cancer, the average CT radiation dose during the cardiac MPI was 100 mGy-cm (range, 77 -133 mCy-cm). The subsequent chest CT with or without contrast delivered a radiation dose of 726.4 mGy-cm (range, 279.4 - 1,075 mGy-cm).
A total of 79 (7.2%) patients were found to have significant pulmonary nodules that required further evaluation; after CT examination, 32 patients had findings of benign nature and required no further follow-up; the other 47 patients are being followed according to the Fleischner Society 2017 guidelines for pulmonary nodules.11 The follow-up findings on these patients are not within the scope of this report.
Discussion
Although incidental findings on low-resolution CT during cardiac MPI are frequent, clinically significant findings are less common. However, some incidental findings may be of important clinical significance.3-5 A multicenter analysis by Coward and colleagues reported that 2.4% findings on low-resolution CT were significant enough to warrant follow-up tests, but only 0.2% were deemed potentially detrimental to patient outcomes (ie, pathology confirmed malignancies).12 Thus, the authors suggested that routine reporting of incidental findings on low-dose CT images was not beneficial.12,13
Currently, the majority of cardiac MPIs are reviewed and interpreted by nuclear cardiologists, the use of hybrid SPECT/CT for attenuation correction give rise of issue of reviewing and interpreting these CT images during cardiac MPI. Since low-dose, low-resolution CT are considered nondiagnostic, these images are not routinely and readily reviewed by cardiologists who are not trained or skilled in CT interpretations.
Studies of high-resolution cardiac CT (including multidetector CT with contrast) suggest that incidental extracardiac findings should always be reported as there was a 0.7% incidence of previously unknown malignancies, while others have argued against “performing large field reconstructionsfor the explicit purpose of screening as it will lead to additional cost, liability and anxiety without proven benefits.”14-16 A review of incidental findings of cardiac CT by Earls suggested that all cardiac CT should be reconstructed in the maximal field of view available and images should be adequately reviewed to detect pathological findings.17 This led to an interesting discussion by Douglas and colleagues regarding the role of cardiologists and radiologists in this issue.18 Currently there is no uniform or consensus recommendations regarding incidental findings during cardiac CT imaging. Guidances range from no recommendations to optional reporting or mandatory reporting.19-23
Risk Factors for Veterans
Lung cancer is the second most common cancer and the leading cause of cancer-related death in the US.24 Smoking is the most important risk factor for lung cancer and CAD.25 Current or past smoking are more common among the veterans.10 According to a report for the US Centers for Disease Control and Prevention report, about 29.2% US veterans use tobacco products between 2010-2015, which is similar to the rate reported in 1997.26
When low-dose CT was used for lung cancer screening, it was associated with a 20.0% reduction in lung cancer mortality and a 6.7% reduction in any cause mortality.7 Currently, the US Preventive Services Task Force (USPSTF) recommends annual low-dose CT screening for lung cancer in high-risk adults that includes patients aged 55 to 80 years who have a 30-pack-year smoking history and currently smoke or have quit within the past 15 years.8
It is likely that the cardiac patients in this study might have pulmonary malignancy mortality similar to those reported in the NLST. While other studies have shown a low incidence (0.2%) of detection of malignancy by low-resolution CT during cardiac MPI,12,13 in this study we found pulmonary or hilar malignancy in 0.55% of patients.The higher incidence of malignancy in our study might be due in part to differences in the patient population studied (ie, our veterans patients have a higher proportion of current or past smoking history).10
The CT used in this study is part of the cardiac imaging process. Therefore, there was no additional radiation exposure besides that of the cardiac MPI for patients. Despite the limitations of low-resolution CT, which may miss small lesions, this study showed 0.55% incidence of incidental detection of pulmonary/hilar malignancy. This is comparable with 0.65%/year of diagnosing lung cancer using low-dose CT for lung cancer screening in NLST.8
Two of the 5 study patients who were found to have lung cancer, had quit smoking > 15 years previously and thus would not be considered as high-risk for lung cancer screening according to USPSTF guideline. These patients would not have been candidates for annual low-dose CT lung cancer screening. This study suggests that it is appropriate and necessary to review the low-resolution CT images for incidental findings during cardiac MPI.
Limitations
The study was retrospective in nature and limited by its small number of patients. The CT modality used in the study also has limitations, including low resolution, respiratory motion artifacts, and scans that did not include the entire chest area. Therefore, small and apical lesions may have been missed. However, both sets of CT at rest and after stress were reviewed to reduce or minimize the effects of respiratory motion artifacts. The true prevalence or incidence of pulmonary/hilar malignancies may have been higher than reported here. Our study population of veterans may not be representative of the general population with regards to gender (as most of our veteran patient population are of male gender, vs general population), smoking history, or lung cancer risk, thus the results should be interpreted with caution.
Conclusion
Low-resolution CTs used for attenuation correction during cardiac MPI should be routinely reviewed and interpreted by a physician or radiologist skilled in CT interpretation in order to identify incidental findings of pulmonary/hilar malignancy. This would require close collaboration between cardiologists and radiologists in the field to ensure unfragmented and high-quality patient care.
Acknowledgements
We want to thank all the staffs in cardiology and radiology department on both campuses for their dedication for our patients. Special thanks to Laura Knox, Radiation Safety Officer, Nuclear Medicine Supervisor for her technical assistance.
1. Hendel RC, Berman DS, Di Carli MF, et al. ACCF/ASNC/ACR/AHA/ASE/SCCT/SCMR/SNM 2009 appropriate use criteria for cardiac radionuclide imaging: a report of the American College of Cardiology Foundation Appropriate Use Criteria Task Force, the American Society of Nuclear Cardiology, the American College of Radiology, the American Heart Association, the American Society of Echocardiography, the Society of Cardiovascular Computed Tomography, the Society for Cardiovascular Magnetic Resonance, and the Society of Nuclear Medicine. Circulation. 2009;119(22):e561-e587.
2. Hendel RC, Corbett JR, Cullom SJ, DePuey EG, Garcia EV, Bateman TM. The value and practice of attenuation correction for myocardial perfusion SPECT imaging: a joint position statement from the American Society of Nuclear Cardiology and the Society of Nuclear Medicine. J Nucl Cardiol. 2002;9(1):135–143.
3. Coward J, Nightingale J, Hogg P. The clinical dilemma of incidental findings on the low-resolution CT images from SPECT/CT MPI studies. J Nucl Med Technol. 2016;44(3):167-172.
4. Osman MM, Cohade C, Fishman E, Wahl RL. Clinically significant incidental findings on the unenhanced CT portion of PET/CT studies: frequency in 250 patients. J Nucl Med. 2005;46(8):1352-1355.
5. Goetze S, Pannu HK, Wahl RL. Clinically significant abnormal findings on the “nondiagnostic” CT portion of low-amperage-CT attenuation-corrected myocardial perfusion SPECT/CT studies. J Nucl Med. 2006;47(8):1312-1318.
6. American College of Cardiology Foundation Task Force on Expert Consensus Documents, Mark DB, Berman DS, et al. ACCF/ACR/AHA/NASCI/SAIP/SCAI/SCCT 2010 expert consensus document on coronary computed tomographic angiography: a report of the American College of Cardiology Foundation Task Force on Expert Consensus Documents. J Am Coll Cardiol. 2010;55(23):2663-2699.
7. Diederich S, Wormanns D, Semik M, et al. Screening for early lung cancer with low-dose spiral CT: prevalence in 817 asymptomatic smokers. Radiology. 2002;222(3):773-781.
8. National Lung Screening Trial Research Team, Aberle DR, Adams AM, et al. Reduced lung-cancer mortality with low-dose computed tomographic screening. N Engl J Med. 2011;365(5):395-409.
9. Moyer VA; U.S. Preventive Services Task Force. Screening for lung cancer: U.S. Preventive Services Task Force recommendation statement. Ann Intern Med. 2014;160(5):330-338.
10. McKinney WP, McIntire DD, Carmody TJ, Joseph A. Comparing the smoking behavior of veterans and nonveterans. Public Health Rep. 1997;112(3):212-218.
11. MacMahon H, Naidich DP, Goo JM, et al. Guidelines for Management of Incidental Pulmonary Nodules Detected on CT Images: From the Fleischner Society 2017. Radiology. 2017;284(1):228-243.
12. Coward J, Lawson R, Kane T, et al. Multi-centre analysis of incidental findings on low-resolution CT attenuation correction images. Br J Radiol. 2014;87(1042):20130701.
13. Coward J, Lawson R, Kane T, et al. Multicentre analysis of incidental findings on low-resolution CT attenuation correction images: an extended study. Br J Radiol. 2015;88(1056):20150555.
14. Haller S, Kaiser C, Buser P, Bongartz G, Bremerich J. Coronary artery imaging with contrast-enhanced MDCT: extracardiac findings. AJR Am J Roentgenol. 2006;187(1):105-110.
15. Flor N, Di Leo G, Squarza SA, et al. Malignant incidental extracardiac findings on cardiac CT: systematic review and meta-analysis. AJR Am J Roentgenol. 2013;201(3):555-564.
16. Budoff MJ, Gopal A. Incidental findings on cardiac computed tomography. Should we look? J Cardiovasc Comput Tomogr. 2007;1(2):97-105.
17. Earls JP. The pros and cons of searching for extracardiac findings at cardiac CT: studies should be reconstructed in the maximum field of view and adequately reviewed to detect pathologic findings. Radiology. 2011;261(2):342-346.
18. Douglas PS, Cerqueria M, Rubin GD, Chin AS. Extracardiac findings: what is a cardiologist to do? JACC Cardiovasc Imaging. 2008;1(5):682-687.
19. Holly TA, Abbott BG, Al-Mallah M, et al. Single photon-emission computed tomography. J Nucl Cardiol. 2010;17(5):941-973.
20. Dorbala S, Ananthasubramaniam K, Armstrong IS, et al. Single photon emission computed tomography (SPECT) myocardial perfusion imaging guidelines: instrumentation, acquisition, processing, and interpretation. J Nucl Cardiol. 2018;25(5):1784-1846.
21. Tilkemeier PL, Bourque J, Doukky R, Sanghani R, Weinberg RL. ASNC imaging guidelines for nuclear cardiology procedures : Standardized reporting of nuclear cardiology procedures. J Nucl Cardiol. 2017;24(6):2064-2128.
22. Dorbala S, Di Carli MF, Delbeke D, et al. SNMMI/ASNC/SCCT guideline for cardiac SPECT/CT and PET/CT 1.0. J Nucl Med. 2013;54(8):1485-1507.
23. Dilsizian V, Bacharach SL, Beanlands RS, et al. ASNC imaging guidelines/SNMMI procedure standard for positron emission tomography (PET) nuclear cardiology procedures. J Nucl Cardiol. 2016;23(5):1187-1226.
24. Jemal A, Ward EM, Johnson CJ, et al. Annual report to the nation on the status of cancer, 1975-2014, Featuring Survival. J Natl Cancer Inst. 2017;109(9):djx030.
25. US Department of Health and Human Services. The Health Consequences of Smoking: 50 Years of Progress. A Report of the Surgeon General. Atlanta, GA: US Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Health Promotion, Office on Smoking and Health; 2014. Printed with corrections, January 2014.
26. Odani S, Agaku IT, Graffunder CM, Tynan MA, Armour BS. Tobacco Product Use Among Military Veterans - United States, 2010-2015. MMWR Morb Mortal Wkly Rep. 2018;67(1):7-12.
Single-photon emission computed tomography (SPECT) myocardial perfusion imaging (MPI) is a well-established technique for the evaluation of coronary artery disease (CAD).1 To improve image quality, low-resolution computed tomography (CT) is used commonly for anatomical correct and artifact attenuation during SPECT MPI.2 The low resolution, unenhanced CT images are considered low quality and are, therefore, labeled by the manufacturer as nondiagnostic. The CT portion of the MPI in many centers is used only for image fusion and attenuation correction, and these images are not routinely reviewed or reported by cardiologists.
Incidental findings by these low-resolution CT were frequent. However, clinically significant findings, including lung cancer, although relatively infrequent, were serious enough for major clinical management.3-5 Currently, there are no consensus recommendations for reviewing low-resolution CT images or the interpretation of such incidental findings during cardiac MPI.6 Clinically, low-dose CT were used for early detection and screening of lung cancer and were associated with reduced lung-cancer and any cause mortality in National Lung Screening Trial (NLST).7,8 Therefore, low-dose CT is recommended for lung cancer screening of high-risk patients by the US Preventive Service Task Force (USPSTF).9 In the veteran population, current and past smoking history are more common when compared with the general population; therefore, veterans are potentially at increased risk of lung cancer.10 In this study, we did not intend to use low-resolution CT for lung cancer screening or detection but rather to identify and report incidental findings of pulmonary/hilar malignancy detected during cardiac MPI.
Methods
The Siemens’ (Munich, Germany) Symbia Intevo Excel SPECT/CT MPI cameras with dedicated cardiac collimators were used at both the Dwight D. Eisenhower VA Medical Center (VAMC) in Leavenworth, Kansas and Colmery-O'Neil VAMC in Topeka, Kansas. The integrated CT scanner (x-ray tube current 30 to 240 mA; voltage 110 Kv with a 40 kW power generator) has the capability to image up to a 2-slice/rotation, each of 5.0 mm per slice with a scan time of about 30 seconds. The SPECT/CT gamma camera has a low energy (140 KeV), high resolution, parallel hole collimator with IQ SPECT capabilities.
The radiation dose received by the patients were expressed in dose length product (DLP), which reflects the total energy absorbed by the patient and represents integrated dose in terms of the total scan length. Additionally, each patients received 2 injections of Technetium Tc 99m sestamibi (1-day Protocol: 10 mCi rest injection, 30 mCi stress injection: 2-day Protocol for patients weighing > 350 pounds: 30 mCi at rest injection and 30 mCi at stress injection) for myocardial perfusion imaging.
All CT images and cardiac MPI findings were reviewed and reported contemporaneously by 1 of 2 experienced, board-certified radiologists who were blinded to patients’ clinical information except the indication for the cardiac stress testing. When suspicious pulmonary/hilar nodules or masses were detected, these findings and recommendations for further evaluation were conveyed to primary care provider or ordering physician via the electronic health record system.
All CT images were reviewed with cardiac MPI from September 1, 2017 to August 31, 2018. When pulmonary/hilar malignancies were identified, the health records were reviewed. Patients with known history of prior pulmonary malignancy were excluded from the study.
Results
A total of 1,098 patients underwent cardiac MPI during the study period. When the CT imaging and cardiac MPI were reviewed, incidental findings led to the diagnosis of lung cancer in 5 patients and hilar mantle cell lymphoma in 1 patient. Their clinical characteristics, CT findings, and types of malignancies for these 6 patients are summarized in the Table and Figure. Only 0.55% (6 of 1,098) patients were found to have incidental pulmonary/hilar malignancy with the cardiac evaluation low-resolution CT. Four patients with prior, known history of lung cancer were excluded from the study.
For the 6 patients found to have cancer, the average CT radiation dose during the cardiac MPI was 100 mGy-cm (range, 77 -133 mCy-cm). The subsequent chest CT with or without contrast delivered a radiation dose of 726.4 mGy-cm (range, 279.4 - 1,075 mGy-cm).
A total of 79 (7.2%) patients were found to have significant pulmonary nodules that required further evaluation; after CT examination, 32 patients had findings of benign nature and required no further follow-up; the other 47 patients are being followed according to the Fleischner Society 2017 guidelines for pulmonary nodules.11 The follow-up findings on these patients are not within the scope of this report.
Discussion
Although incidental findings on low-resolution CT during cardiac MPI are frequent, clinically significant findings are less common. However, some incidental findings may be of important clinical significance.3-5 A multicenter analysis by Coward and colleagues reported that 2.4% findings on low-resolution CT were significant enough to warrant follow-up tests, but only 0.2% were deemed potentially detrimental to patient outcomes (ie, pathology confirmed malignancies).12 Thus, the authors suggested that routine reporting of incidental findings on low-dose CT images was not beneficial.12,13
Currently, the majority of cardiac MPIs are reviewed and interpreted by nuclear cardiologists, the use of hybrid SPECT/CT for attenuation correction give rise of issue of reviewing and interpreting these CT images during cardiac MPI. Since low-dose, low-resolution CT are considered nondiagnostic, these images are not routinely and readily reviewed by cardiologists who are not trained or skilled in CT interpretations.
Studies of high-resolution cardiac CT (including multidetector CT with contrast) suggest that incidental extracardiac findings should always be reported as there was a 0.7% incidence of previously unknown malignancies, while others have argued against “performing large field reconstructionsfor the explicit purpose of screening as it will lead to additional cost, liability and anxiety without proven benefits.”14-16 A review of incidental findings of cardiac CT by Earls suggested that all cardiac CT should be reconstructed in the maximal field of view available and images should be adequately reviewed to detect pathological findings.17 This led to an interesting discussion by Douglas and colleagues regarding the role of cardiologists and radiologists in this issue.18 Currently there is no uniform or consensus recommendations regarding incidental findings during cardiac CT imaging. Guidances range from no recommendations to optional reporting or mandatory reporting.19-23
Risk Factors for Veterans
Lung cancer is the second most common cancer and the leading cause of cancer-related death in the US.24 Smoking is the most important risk factor for lung cancer and CAD.25 Current or past smoking are more common among the veterans.10 According to a report for the US Centers for Disease Control and Prevention report, about 29.2% US veterans use tobacco products between 2010-2015, which is similar to the rate reported in 1997.26
When low-dose CT was used for lung cancer screening, it was associated with a 20.0% reduction in lung cancer mortality and a 6.7% reduction in any cause mortality.7 Currently, the US Preventive Services Task Force (USPSTF) recommends annual low-dose CT screening for lung cancer in high-risk adults that includes patients aged 55 to 80 years who have a 30-pack-year smoking history and currently smoke or have quit within the past 15 years.8
It is likely that the cardiac patients in this study might have pulmonary malignancy mortality similar to those reported in the NLST. While other studies have shown a low incidence (0.2%) of detection of malignancy by low-resolution CT during cardiac MPI,12,13 in this study we found pulmonary or hilar malignancy in 0.55% of patients.The higher incidence of malignancy in our study might be due in part to differences in the patient population studied (ie, our veterans patients have a higher proportion of current or past smoking history).10
The CT used in this study is part of the cardiac imaging process. Therefore, there was no additional radiation exposure besides that of the cardiac MPI for patients. Despite the limitations of low-resolution CT, which may miss small lesions, this study showed 0.55% incidence of incidental detection of pulmonary/hilar malignancy. This is comparable with 0.65%/year of diagnosing lung cancer using low-dose CT for lung cancer screening in NLST.8
Two of the 5 study patients who were found to have lung cancer, had quit smoking > 15 years previously and thus would not be considered as high-risk for lung cancer screening according to USPSTF guideline. These patients would not have been candidates for annual low-dose CT lung cancer screening. This study suggests that it is appropriate and necessary to review the low-resolution CT images for incidental findings during cardiac MPI.
Limitations
The study was retrospective in nature and limited by its small number of patients. The CT modality used in the study also has limitations, including low resolution, respiratory motion artifacts, and scans that did not include the entire chest area. Therefore, small and apical lesions may have been missed. However, both sets of CT at rest and after stress were reviewed to reduce or minimize the effects of respiratory motion artifacts. The true prevalence or incidence of pulmonary/hilar malignancies may have been higher than reported here. Our study population of veterans may not be representative of the general population with regards to gender (as most of our veteran patient population are of male gender, vs general population), smoking history, or lung cancer risk, thus the results should be interpreted with caution.
Conclusion
Low-resolution CTs used for attenuation correction during cardiac MPI should be routinely reviewed and interpreted by a physician or radiologist skilled in CT interpretation in order to identify incidental findings of pulmonary/hilar malignancy. This would require close collaboration between cardiologists and radiologists in the field to ensure unfragmented and high-quality patient care.
Acknowledgements
We want to thank all the staffs in cardiology and radiology department on both campuses for their dedication for our patients. Special thanks to Laura Knox, Radiation Safety Officer, Nuclear Medicine Supervisor for her technical assistance.
Single-photon emission computed tomography (SPECT) myocardial perfusion imaging (MPI) is a well-established technique for the evaluation of coronary artery disease (CAD).1 To improve image quality, low-resolution computed tomography (CT) is used commonly for anatomical correct and artifact attenuation during SPECT MPI.2 The low resolution, unenhanced CT images are considered low quality and are, therefore, labeled by the manufacturer as nondiagnostic. The CT portion of the MPI in many centers is used only for image fusion and attenuation correction, and these images are not routinely reviewed or reported by cardiologists.
Incidental findings by these low-resolution CT were frequent. However, clinically significant findings, including lung cancer, although relatively infrequent, were serious enough for major clinical management.3-5 Currently, there are no consensus recommendations for reviewing low-resolution CT images or the interpretation of such incidental findings during cardiac MPI.6 Clinically, low-dose CT were used for early detection and screening of lung cancer and were associated with reduced lung-cancer and any cause mortality in National Lung Screening Trial (NLST).7,8 Therefore, low-dose CT is recommended for lung cancer screening of high-risk patients by the US Preventive Service Task Force (USPSTF).9 In the veteran population, current and past smoking history are more common when compared with the general population; therefore, veterans are potentially at increased risk of lung cancer.10 In this study, we did not intend to use low-resolution CT for lung cancer screening or detection but rather to identify and report incidental findings of pulmonary/hilar malignancy detected during cardiac MPI.
Methods
The Siemens’ (Munich, Germany) Symbia Intevo Excel SPECT/CT MPI cameras with dedicated cardiac collimators were used at both the Dwight D. Eisenhower VA Medical Center (VAMC) in Leavenworth, Kansas and Colmery-O'Neil VAMC in Topeka, Kansas. The integrated CT scanner (x-ray tube current 30 to 240 mA; voltage 110 Kv with a 40 kW power generator) has the capability to image up to a 2-slice/rotation, each of 5.0 mm per slice with a scan time of about 30 seconds. The SPECT/CT gamma camera has a low energy (140 KeV), high resolution, parallel hole collimator with IQ SPECT capabilities.
The radiation dose received by the patients were expressed in dose length product (DLP), which reflects the total energy absorbed by the patient and represents integrated dose in terms of the total scan length. Additionally, each patients received 2 injections of Technetium Tc 99m sestamibi (1-day Protocol: 10 mCi rest injection, 30 mCi stress injection: 2-day Protocol for patients weighing > 350 pounds: 30 mCi at rest injection and 30 mCi at stress injection) for myocardial perfusion imaging.
All CT images and cardiac MPI findings were reviewed and reported contemporaneously by 1 of 2 experienced, board-certified radiologists who were blinded to patients’ clinical information except the indication for the cardiac stress testing. When suspicious pulmonary/hilar nodules or masses were detected, these findings and recommendations for further evaluation were conveyed to primary care provider or ordering physician via the electronic health record system.
All CT images were reviewed with cardiac MPI from September 1, 2017 to August 31, 2018. When pulmonary/hilar malignancies were identified, the health records were reviewed. Patients with known history of prior pulmonary malignancy were excluded from the study.
Results
A total of 1,098 patients underwent cardiac MPI during the study period. When the CT imaging and cardiac MPI were reviewed, incidental findings led to the diagnosis of lung cancer in 5 patients and hilar mantle cell lymphoma in 1 patient. Their clinical characteristics, CT findings, and types of malignancies for these 6 patients are summarized in the Table and Figure. Only 0.55% (6 of 1,098) patients were found to have incidental pulmonary/hilar malignancy with the cardiac evaluation low-resolution CT. Four patients with prior, known history of lung cancer were excluded from the study.
For the 6 patients found to have cancer, the average CT radiation dose during the cardiac MPI was 100 mGy-cm (range, 77 -133 mCy-cm). The subsequent chest CT with or without contrast delivered a radiation dose of 726.4 mGy-cm (range, 279.4 - 1,075 mGy-cm).
A total of 79 (7.2%) patients were found to have significant pulmonary nodules that required further evaluation; after CT examination, 32 patients had findings of benign nature and required no further follow-up; the other 47 patients are being followed according to the Fleischner Society 2017 guidelines for pulmonary nodules.11 The follow-up findings on these patients are not within the scope of this report.
Discussion
Although incidental findings on low-resolution CT during cardiac MPI are frequent, clinically significant findings are less common. However, some incidental findings may be of important clinical significance.3-5 A multicenter analysis by Coward and colleagues reported that 2.4% findings on low-resolution CT were significant enough to warrant follow-up tests, but only 0.2% were deemed potentially detrimental to patient outcomes (ie, pathology confirmed malignancies).12 Thus, the authors suggested that routine reporting of incidental findings on low-dose CT images was not beneficial.12,13
Currently, the majority of cardiac MPIs are reviewed and interpreted by nuclear cardiologists, the use of hybrid SPECT/CT for attenuation correction give rise of issue of reviewing and interpreting these CT images during cardiac MPI. Since low-dose, low-resolution CT are considered nondiagnostic, these images are not routinely and readily reviewed by cardiologists who are not trained or skilled in CT interpretations.
Studies of high-resolution cardiac CT (including multidetector CT with contrast) suggest that incidental extracardiac findings should always be reported as there was a 0.7% incidence of previously unknown malignancies, while others have argued against “performing large field reconstructionsfor the explicit purpose of screening as it will lead to additional cost, liability and anxiety without proven benefits.”14-16 A review of incidental findings of cardiac CT by Earls suggested that all cardiac CT should be reconstructed in the maximal field of view available and images should be adequately reviewed to detect pathological findings.17 This led to an interesting discussion by Douglas and colleagues regarding the role of cardiologists and radiologists in this issue.18 Currently there is no uniform or consensus recommendations regarding incidental findings during cardiac CT imaging. Guidances range from no recommendations to optional reporting or mandatory reporting.19-23
Risk Factors for Veterans
Lung cancer is the second most common cancer and the leading cause of cancer-related death in the US.24 Smoking is the most important risk factor for lung cancer and CAD.25 Current or past smoking are more common among the veterans.10 According to a report for the US Centers for Disease Control and Prevention report, about 29.2% US veterans use tobacco products between 2010-2015, which is similar to the rate reported in 1997.26
When low-dose CT was used for lung cancer screening, it was associated with a 20.0% reduction in lung cancer mortality and a 6.7% reduction in any cause mortality.7 Currently, the US Preventive Services Task Force (USPSTF) recommends annual low-dose CT screening for lung cancer in high-risk adults that includes patients aged 55 to 80 years who have a 30-pack-year smoking history and currently smoke or have quit within the past 15 years.8
It is likely that the cardiac patients in this study might have pulmonary malignancy mortality similar to those reported in the NLST. While other studies have shown a low incidence (0.2%) of detection of malignancy by low-resolution CT during cardiac MPI,12,13 in this study we found pulmonary or hilar malignancy in 0.55% of patients.The higher incidence of malignancy in our study might be due in part to differences in the patient population studied (ie, our veterans patients have a higher proportion of current or past smoking history).10
The CT used in this study is part of the cardiac imaging process. Therefore, there was no additional radiation exposure besides that of the cardiac MPI for patients. Despite the limitations of low-resolution CT, which may miss small lesions, this study showed 0.55% incidence of incidental detection of pulmonary/hilar malignancy. This is comparable with 0.65%/year of diagnosing lung cancer using low-dose CT for lung cancer screening in NLST.8
Two of the 5 study patients who were found to have lung cancer, had quit smoking > 15 years previously and thus would not be considered as high-risk for lung cancer screening according to USPSTF guideline. These patients would not have been candidates for annual low-dose CT lung cancer screening. This study suggests that it is appropriate and necessary to review the low-resolution CT images for incidental findings during cardiac MPI.
Limitations
The study was retrospective in nature and limited by its small number of patients. The CT modality used in the study also has limitations, including low resolution, respiratory motion artifacts, and scans that did not include the entire chest area. Therefore, small and apical lesions may have been missed. However, both sets of CT at rest and after stress were reviewed to reduce or minimize the effects of respiratory motion artifacts. The true prevalence or incidence of pulmonary/hilar malignancies may have been higher than reported here. Our study population of veterans may not be representative of the general population with regards to gender (as most of our veteran patient population are of male gender, vs general population), smoking history, or lung cancer risk, thus the results should be interpreted with caution.
Conclusion
Low-resolution CTs used for attenuation correction during cardiac MPI should be routinely reviewed and interpreted by a physician or radiologist skilled in CT interpretation in order to identify incidental findings of pulmonary/hilar malignancy. This would require close collaboration between cardiologists and radiologists in the field to ensure unfragmented and high-quality patient care.
Acknowledgements
We want to thank all the staffs in cardiology and radiology department on both campuses for their dedication for our patients. Special thanks to Laura Knox, Radiation Safety Officer, Nuclear Medicine Supervisor for her technical assistance.
1. Hendel RC, Berman DS, Di Carli MF, et al. ACCF/ASNC/ACR/AHA/ASE/SCCT/SCMR/SNM 2009 appropriate use criteria for cardiac radionuclide imaging: a report of the American College of Cardiology Foundation Appropriate Use Criteria Task Force, the American Society of Nuclear Cardiology, the American College of Radiology, the American Heart Association, the American Society of Echocardiography, the Society of Cardiovascular Computed Tomography, the Society for Cardiovascular Magnetic Resonance, and the Society of Nuclear Medicine. Circulation. 2009;119(22):e561-e587.
2. Hendel RC, Corbett JR, Cullom SJ, DePuey EG, Garcia EV, Bateman TM. The value and practice of attenuation correction for myocardial perfusion SPECT imaging: a joint position statement from the American Society of Nuclear Cardiology and the Society of Nuclear Medicine. J Nucl Cardiol. 2002;9(1):135–143.
3. Coward J, Nightingale J, Hogg P. The clinical dilemma of incidental findings on the low-resolution CT images from SPECT/CT MPI studies. J Nucl Med Technol. 2016;44(3):167-172.
4. Osman MM, Cohade C, Fishman E, Wahl RL. Clinically significant incidental findings on the unenhanced CT portion of PET/CT studies: frequency in 250 patients. J Nucl Med. 2005;46(8):1352-1355.
5. Goetze S, Pannu HK, Wahl RL. Clinically significant abnormal findings on the “nondiagnostic” CT portion of low-amperage-CT attenuation-corrected myocardial perfusion SPECT/CT studies. J Nucl Med. 2006;47(8):1312-1318.
6. American College of Cardiology Foundation Task Force on Expert Consensus Documents, Mark DB, Berman DS, et al. ACCF/ACR/AHA/NASCI/SAIP/SCAI/SCCT 2010 expert consensus document on coronary computed tomographic angiography: a report of the American College of Cardiology Foundation Task Force on Expert Consensus Documents. J Am Coll Cardiol. 2010;55(23):2663-2699.
7. Diederich S, Wormanns D, Semik M, et al. Screening for early lung cancer with low-dose spiral CT: prevalence in 817 asymptomatic smokers. Radiology. 2002;222(3):773-781.
8. National Lung Screening Trial Research Team, Aberle DR, Adams AM, et al. Reduced lung-cancer mortality with low-dose computed tomographic screening. N Engl J Med. 2011;365(5):395-409.
9. Moyer VA; U.S. Preventive Services Task Force. Screening for lung cancer: U.S. Preventive Services Task Force recommendation statement. Ann Intern Med. 2014;160(5):330-338.
10. McKinney WP, McIntire DD, Carmody TJ, Joseph A. Comparing the smoking behavior of veterans and nonveterans. Public Health Rep. 1997;112(3):212-218.
11. MacMahon H, Naidich DP, Goo JM, et al. Guidelines for Management of Incidental Pulmonary Nodules Detected on CT Images: From the Fleischner Society 2017. Radiology. 2017;284(1):228-243.
12. Coward J, Lawson R, Kane T, et al. Multi-centre analysis of incidental findings on low-resolution CT attenuation correction images. Br J Radiol. 2014;87(1042):20130701.
13. Coward J, Lawson R, Kane T, et al. Multicentre analysis of incidental findings on low-resolution CT attenuation correction images: an extended study. Br J Radiol. 2015;88(1056):20150555.
14. Haller S, Kaiser C, Buser P, Bongartz G, Bremerich J. Coronary artery imaging with contrast-enhanced MDCT: extracardiac findings. AJR Am J Roentgenol. 2006;187(1):105-110.
15. Flor N, Di Leo G, Squarza SA, et al. Malignant incidental extracardiac findings on cardiac CT: systematic review and meta-analysis. AJR Am J Roentgenol. 2013;201(3):555-564.
16. Budoff MJ, Gopal A. Incidental findings on cardiac computed tomography. Should we look? J Cardiovasc Comput Tomogr. 2007;1(2):97-105.
17. Earls JP. The pros and cons of searching for extracardiac findings at cardiac CT: studies should be reconstructed in the maximum field of view and adequately reviewed to detect pathologic findings. Radiology. 2011;261(2):342-346.
18. Douglas PS, Cerqueria M, Rubin GD, Chin AS. Extracardiac findings: what is a cardiologist to do? JACC Cardiovasc Imaging. 2008;1(5):682-687.
19. Holly TA, Abbott BG, Al-Mallah M, et al. Single photon-emission computed tomography. J Nucl Cardiol. 2010;17(5):941-973.
20. Dorbala S, Ananthasubramaniam K, Armstrong IS, et al. Single photon emission computed tomography (SPECT) myocardial perfusion imaging guidelines: instrumentation, acquisition, processing, and interpretation. J Nucl Cardiol. 2018;25(5):1784-1846.
21. Tilkemeier PL, Bourque J, Doukky R, Sanghani R, Weinberg RL. ASNC imaging guidelines for nuclear cardiology procedures : Standardized reporting of nuclear cardiology procedures. J Nucl Cardiol. 2017;24(6):2064-2128.
22. Dorbala S, Di Carli MF, Delbeke D, et al. SNMMI/ASNC/SCCT guideline for cardiac SPECT/CT and PET/CT 1.0. J Nucl Med. 2013;54(8):1485-1507.
23. Dilsizian V, Bacharach SL, Beanlands RS, et al. ASNC imaging guidelines/SNMMI procedure standard for positron emission tomography (PET) nuclear cardiology procedures. J Nucl Cardiol. 2016;23(5):1187-1226.
24. Jemal A, Ward EM, Johnson CJ, et al. Annual report to the nation on the status of cancer, 1975-2014, Featuring Survival. J Natl Cancer Inst. 2017;109(9):djx030.
25. US Department of Health and Human Services. The Health Consequences of Smoking: 50 Years of Progress. A Report of the Surgeon General. Atlanta, GA: US Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Health Promotion, Office on Smoking and Health; 2014. Printed with corrections, January 2014.
26. Odani S, Agaku IT, Graffunder CM, Tynan MA, Armour BS. Tobacco Product Use Among Military Veterans - United States, 2010-2015. MMWR Morb Mortal Wkly Rep. 2018;67(1):7-12.
1. Hendel RC, Berman DS, Di Carli MF, et al. ACCF/ASNC/ACR/AHA/ASE/SCCT/SCMR/SNM 2009 appropriate use criteria for cardiac radionuclide imaging: a report of the American College of Cardiology Foundation Appropriate Use Criteria Task Force, the American Society of Nuclear Cardiology, the American College of Radiology, the American Heart Association, the American Society of Echocardiography, the Society of Cardiovascular Computed Tomography, the Society for Cardiovascular Magnetic Resonance, and the Society of Nuclear Medicine. Circulation. 2009;119(22):e561-e587.
2. Hendel RC, Corbett JR, Cullom SJ, DePuey EG, Garcia EV, Bateman TM. The value and practice of attenuation correction for myocardial perfusion SPECT imaging: a joint position statement from the American Society of Nuclear Cardiology and the Society of Nuclear Medicine. J Nucl Cardiol. 2002;9(1):135–143.
3. Coward J, Nightingale J, Hogg P. The clinical dilemma of incidental findings on the low-resolution CT images from SPECT/CT MPI studies. J Nucl Med Technol. 2016;44(3):167-172.
4. Osman MM, Cohade C, Fishman E, Wahl RL. Clinically significant incidental findings on the unenhanced CT portion of PET/CT studies: frequency in 250 patients. J Nucl Med. 2005;46(8):1352-1355.
5. Goetze S, Pannu HK, Wahl RL. Clinically significant abnormal findings on the “nondiagnostic” CT portion of low-amperage-CT attenuation-corrected myocardial perfusion SPECT/CT studies. J Nucl Med. 2006;47(8):1312-1318.
6. American College of Cardiology Foundation Task Force on Expert Consensus Documents, Mark DB, Berman DS, et al. ACCF/ACR/AHA/NASCI/SAIP/SCAI/SCCT 2010 expert consensus document on coronary computed tomographic angiography: a report of the American College of Cardiology Foundation Task Force on Expert Consensus Documents. J Am Coll Cardiol. 2010;55(23):2663-2699.
7. Diederich S, Wormanns D, Semik M, et al. Screening for early lung cancer with low-dose spiral CT: prevalence in 817 asymptomatic smokers. Radiology. 2002;222(3):773-781.
8. National Lung Screening Trial Research Team, Aberle DR, Adams AM, et al. Reduced lung-cancer mortality with low-dose computed tomographic screening. N Engl J Med. 2011;365(5):395-409.
9. Moyer VA; U.S. Preventive Services Task Force. Screening for lung cancer: U.S. Preventive Services Task Force recommendation statement. Ann Intern Med. 2014;160(5):330-338.
10. McKinney WP, McIntire DD, Carmody TJ, Joseph A. Comparing the smoking behavior of veterans and nonveterans. Public Health Rep. 1997;112(3):212-218.
11. MacMahon H, Naidich DP, Goo JM, et al. Guidelines for Management of Incidental Pulmonary Nodules Detected on CT Images: From the Fleischner Society 2017. Radiology. 2017;284(1):228-243.
12. Coward J, Lawson R, Kane T, et al. Multi-centre analysis of incidental findings on low-resolution CT attenuation correction images. Br J Radiol. 2014;87(1042):20130701.
13. Coward J, Lawson R, Kane T, et al. Multicentre analysis of incidental findings on low-resolution CT attenuation correction images: an extended study. Br J Radiol. 2015;88(1056):20150555.
14. Haller S, Kaiser C, Buser P, Bongartz G, Bremerich J. Coronary artery imaging with contrast-enhanced MDCT: extracardiac findings. AJR Am J Roentgenol. 2006;187(1):105-110.
15. Flor N, Di Leo G, Squarza SA, et al. Malignant incidental extracardiac findings on cardiac CT: systematic review and meta-analysis. AJR Am J Roentgenol. 2013;201(3):555-564.
16. Budoff MJ, Gopal A. Incidental findings on cardiac computed tomography. Should we look? J Cardiovasc Comput Tomogr. 2007;1(2):97-105.
17. Earls JP. The pros and cons of searching for extracardiac findings at cardiac CT: studies should be reconstructed in the maximum field of view and adequately reviewed to detect pathologic findings. Radiology. 2011;261(2):342-346.
18. Douglas PS, Cerqueria M, Rubin GD, Chin AS. Extracardiac findings: what is a cardiologist to do? JACC Cardiovasc Imaging. 2008;1(5):682-687.
19. Holly TA, Abbott BG, Al-Mallah M, et al. Single photon-emission computed tomography. J Nucl Cardiol. 2010;17(5):941-973.
20. Dorbala S, Ananthasubramaniam K, Armstrong IS, et al. Single photon emission computed tomography (SPECT) myocardial perfusion imaging guidelines: instrumentation, acquisition, processing, and interpretation. J Nucl Cardiol. 2018;25(5):1784-1846.
21. Tilkemeier PL, Bourque J, Doukky R, Sanghani R, Weinberg RL. ASNC imaging guidelines for nuclear cardiology procedures : Standardized reporting of nuclear cardiology procedures. J Nucl Cardiol. 2017;24(6):2064-2128.
22. Dorbala S, Di Carli MF, Delbeke D, et al. SNMMI/ASNC/SCCT guideline for cardiac SPECT/CT and PET/CT 1.0. J Nucl Med. 2013;54(8):1485-1507.
23. Dilsizian V, Bacharach SL, Beanlands RS, et al. ASNC imaging guidelines/SNMMI procedure standard for positron emission tomography (PET) nuclear cardiology procedures. J Nucl Cardiol. 2016;23(5):1187-1226.
24. Jemal A, Ward EM, Johnson CJ, et al. Annual report to the nation on the status of cancer, 1975-2014, Featuring Survival. J Natl Cancer Inst. 2017;109(9):djx030.
25. US Department of Health and Human Services. The Health Consequences of Smoking: 50 Years of Progress. A Report of the Surgeon General. Atlanta, GA: US Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Health Promotion, Office on Smoking and Health; 2014. Printed with corrections, January 2014.
26. Odani S, Agaku IT, Graffunder CM, Tynan MA, Armour BS. Tobacco Product Use Among Military Veterans - United States, 2010-2015. MMWR Morb Mortal Wkly Rep. 2018;67(1):7-12.