European Journal of Radiology 84 (2015) 1569–1573
Contents lists available at ScienceDirect
European Journal of Radiology journal homepage: www.elsevier.com/locate/ejrad
Prevalence and clinical significance of extravascular incidental findings in patients undergoing CT cervico-cerebral angiography Matthew Thomas Crockett ∗ , Blathnaid Murphy 1 , Jennifer Smith 1 , Eoin Carl Kavanagh 2 Department of Radiology, Mater Misercordiae University Hospital, Dublin, Ireland
a r t i c l e
i n f o
Article history: Received 12 January 2015 Received in revised form 15 April 2015 Accepted 7 May 2015 Keywords: CT angiography CT cervico-cerebral angiography Head and neck Neuroradiology Incidental findings
a b s t r a c t Introduction: CT cervico-cerebral angiography (CTCCA) is now the first line diagnostic imaging modality for the majority of vascular pathologies of the head and neck with diagnostic value comparable to or better than traditional angiographic techniques. The aim of this study was to assess the prevalence, clinical significance and management of extravascular incidental findings detected on CTCCA. Materials and methods: A retrospective review of the CTCCA reports of 302 consecutive patients from 2009 to 2013 was undertaken. Extravascular incidental findings were classified, according to an adaptation of the CT colonography data and reporting system (CRADS), as EV1–EV4. EV1 = no incidental findings, EV2 = clinically insignificant incidental finding, EV3 = incidental finding of intermediate clinical significance, EV4 = highly clinically significant finding. Follow up of the electronic medical records of patients with EV3 or EV4 findings was undertaken to determine subsequent management. Results: Potentially clinically significant findings were demonstrated in 14.2% of patients with 8.6% of patients having a highly clinically significant finding. 4 incidental findings were confirmed to be malignant lesions and 5 required acute intervention. In addition 19% of patients with highly clinically significant incidental findings did not receive appropriate follow up. Discussion: This study has demonstrated the presence of clinically important incidental findings in a significant proportion of patients undergoing CTCCA with a significant minority of these patients not receiving follow up. A standardised method of reporting incidental findings, such as that used in this paper, would aid radiologists and referring physicians in recording and communicating these findings. © 2015 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Technological advances, including the development of multidetector row helical computed tomography (MDCT) and 3D post processing techniques, have led to multiple new clinical applications for computed tomography angiography (CTA). Whether assessing the peripheral vascular system, mesenteric vessels or pulmonary arterial system, CTA is now the first line diagnostic imaging modality for a myriad of vascular pathologies with diagnostic value comparable to or better than traditional angiographic techniques [1–4]. CTA of the head and neck, CT cervico-cerebral angiography (CTCCA) has displaced catheter directed digital subtraction
∗ Corresponding author. Tel.: +353 863669360; fax: +353 18032970. E-mail addresses: [email protected] (M.T. Crockett), [email protected] (B. Murphy), [email protected] (J. Smith), [email protected] (E.C. Kavanagh). 1 Tel.: +353 7593914; fax: +353 18032970. 2 Tel.: +353 866031274; fax: +353 18032970. http://dx.doi.org/10.1016/j.ejrad.2015.05.014 0720-048X/© 2015 Elsevier Ireland Ltd. All rights reserved.
angiography (DSA) as the initial investigation in the assessment of the majority of neurovascular pathologies [5]. Unlike DSA, in addition to assessing the head and neck vasculature, CTCCA also images adjacent structures with field of view including the lung apicies, thyroid gland, soft tissues and osseous structures of the head and neck. Consequently CTCCA has the potential to detect non vascular, “incidental” findings. Although many of these finding may be inconsequential to the patient, some may be highly clinically important such as early detection of a treatable malignancy. Previously published studies have assessed the prevalence and significance of findings incidentally identified on CT angiography of the aorta, lower limbs and pulmonary arterial system demonstrating highly significant findings in a large proportion of patients [6–8]. The results of these studies have increased awareness amongst both radiologists and referring physicians; however no similar study has been undertaken focusing on CTCCA, now one of the most commonly performed CT angiographic studies. The aim of this study was to define the prevalence, clinical significance and subsequent management of extravascular incidental findings detected on CTCCA. A more thorough knowledge of the
1570
M.T. Crockett et al. / European Journal of Radiology 84 (2015) 1569–1573
Table 1 Extra-vascular (EV) incidental findings classification system. Classification
Clinical significance
Example finding
Follow up
EV1 EV2 EV3 EV4
Normal/anatomic variant Low clinical significance Intermediate clinical significance High clinical significance
Azygous fissure Spinal degenerative disease Indeterminate thyroid nodule Lesion highly suspicious for malignancy. Pneumothorax
No follow up required No follow up required Follow up required as per clinical scenario 1. Follow up required (further imaging ± biopsy) 2. Urgent intervention required
most commonly detected clinically significant findings on CTCCA should help radiologists better define their search strategies whilst improving awareness of referring physicians and reducing potential for missed patient follow up. 2. Materials and methods A retrospective review of all CTCCA reports at a tertiary referral University hospital from November 2009 to December 2013 was conducted using the intra hospital electronic patient records system. Assessment of patient follow up was performed using the intra hospital patient record system and the National Integrated Imaging Management System (NIMIS), a nationwide PACS system covering the majority of hospitals in the state allowing capture of external patient follow up. All CTA’s at our institution were performed using a standardised protocol using a Seimens Somatom Definition 128 slice scanner. Bolus tracking software was used with a premonitoring scan centred on the aortic arch triggering the scan following administration of 80 ml of non-ionic IV contrast (Niopam 370) at a rate of 8 ml/s followed by a saline flush. FOV spanned aortic arch to skull vertex. Scan parameters consist of 6 mm collimation, 1 mm slice thickness, 1.2 pitch, kVp 120, mAs 90 (variable). Axial images were reconstructed using a medium smooth algorithm and presented for review on angiographic windows with 1 mm slice thickness. In addition axial, coronal and saggital 3D MIP images were reconstructed with 30 mm slice thickness to aid in visualisation of the intracranial arterial system. Images were viewed on a PACS workstation. Classification of incidental findings was based upon an adaptation of the CT colonography reporting and data system (C-RADS) [9,10]. Incidental findings were classified under the headings extravascular 1–4 (EV1–4). This classification system is summarised in Table 1. Studies with no incidental findings or those with
anatomic variants, such as an azygous fissure, were categorised as EV1. Those with incidental findings which were of low clinical significance and did not require further follow were classified as EV2. Studies with findings of intermediate clinical significance which required further follow up depending upon the clinical scenario were classified as EV3. Those studies with findings of high clinical significance which required further imaging follow up, biopsy or urgent intervention were classified as EV4. Studies containing multiple incidental findings were classified according to the most clinically significant finding. The results of follow up imaging studies, biopsies or interventions of patients with EV3 or EV4 findings were recorded. 3. Results 302 patients underwent CTCCA over the 3 year study period from 2009 to 2013. 171 (57%) were male and 131 (43%) were female. Mean age was 61 (range 16–95 years, SD 16.9). 207 studies (69%) were performed for assessment of suspected acute ischaemic stroke. Other indications for CTCCA are listed in Table 2. 151 incidental extravascular findings were detected in 131 patients. Of these 151 incidental findings 26 (17%) were in the E4 category, 17 (11%) were in the E3 category and 87 (72%) were in the Table 2 Indication for CT cervico-cerebral angiography. Indication
Number (%)
Acute ischaemic stroke Vascular stenosis (inc. carotid disease) Vascular anomaly (inc. intracranial aneurysm) Haemorrhagic stroke Arterial dissection Vasculitis Trauma
207 (69) 26 (9) 26 (9) 15 (5) 12 (4) 8 (2) 8 (2)
Fig. 1. Axial and coronal CTA images on soft tissue windows demonstrating a heterogeneously enhancing right parotid lesion. A biopsy was subsequently undertaken confirming the presence of a pleiomorphic adenoma.
M.T. Crockett et al. / European Journal of Radiology 84 (2015) 1569–1573 Table 3 Summary of incidental extra vascular findings by EV1–4 classification. EV category
No. of findings
% study cohort
% total incidental findings
EV4 EV3 EV2 EV1
26 17 87 172
8.6% 5.6% 28.8% 57%
17% 11% 72% N/A
1571
lesions (81%) underwent further imaging with 9 undergoing subsequent biopsy. 4 lesions were positive for malignancy; 2 follicular thyroid carcinomas, 1 pleomorphic ademoma and 1 squamous cell carcinoma. 5 of the 26 EV4 incidental findings (19%) were acute findings requiring immediate intervention including a haemothorax and acute severe pulmonary oedema. 5 of the 26 EV4 findings (19%) did not undergo appropriate follow up including 3 pulmonary nodules and 2 suspicious thyroid lesions. A summary of EV3 incidental findings of intermediate clinical significance and their follow up is provided in Table 5. Of the 17 patients with EV3 incidental findings, 10 (61%) underwent follow up. This follow up consisted of further imaging studies in 8 patients (47%) and referral to subspecialty clinics in 2 patients (12%) consisting of ENT and cardiology. No patient with an EV3 incidental finding underwent biopsy. 4. Discussion
Fig. 2. Axial CTA image on soft tissue windows demonstrating a peripherally enhancing heterogenous nodule within the right lobe of the thyroid gland. This lesion was subsequently biopsied confirming the presence of a follicular thyroid carcinoma.
E2 category. Of the 302 patients included in the study, 26 (8.2%) had incidental findings of high clinical significance and 17 (5.6%) had incidental findings of intermediate clinical significance (Table 3). A summary of EV4 incidental findings of high clinical significance and their follow up is provided in Table 4. Examples of EV4 findings are provided in Figs. 1 and 2. Of the 26 EV4 incidental findings 21 (81%) were lesions suspicious for malignancy which required further follow up. 16 out of these 21
CTCCA has become the first imaging modality in the assessment of a wide range of neurovascular pathologies including acute ischaemic stroke, cervico-cerebral vascular anomalies, stenoocclusive carotid arterial disease, vascular trauma and vasculitis [5]. The most common use of CTCCA is in the assessment of ischaemic stroke. Partly due to its accuracy in identifying intraarterial thrombus and partly due to its speed of acquisition and widespread availability in the emergency setting, CTCCA has, along with non contrast CT brain, become a mainstay in the assessment of patients presenting with suspected acute ischaemic stroke [11,12]. In this setting CTCCA allows not only allows more accurate diagnosis than NCCTB alone but also allows localisation of the intraarterial thrombus and consequently guides choice of therapeutic options [13]. In line with current guidelines in 2009 our institution introduced a protocol for patients presenting with suspected acute stroke with patients undergoing a NCCTB followed by CTCCA [13]. CTCCA is performed using bolus tracking software with a field of view encompassing the aortic arch inferiorly and skull vertex superiorly [14]. The complex nature of the cervico-cerebral vascular system means that CT angiographic imaging of this region is
Table 4 Summary of EV4 findings of high clinical significance. Organ system
Finding (number)
Follow up
Outcome
Chest
Pulmonary nodule (7)
1. CT thorax 2. CT thorax 3. CT thorax 4. CT thorax 5. Not performed 6. Not performed 7. Not performed 1. CXR 2. CXR 3. CXR CT thorax CT thorax, Bronchoscopy, Bx 1. CT thorax 2. CT thorax
Resolution of nodule (likely inflammatory) Resolution of nodule (likely inflammatory) Indeterminate, continued CT follow up Hamartoma Not documented Patient deceased Not documented Instigation of medical therapy Instigation of medical therapy Instigation of medical therapy Insertion of chest drain. Squamous metaplasia, continued follow up Insertion chest drain Medical therapy
1. MRI 2. MRI, Bx MRI, Bx US, Bx 1. US 2. Not performed 3. US, Bx 4. US, Bx 5. Not performed 6. US, Bx 7. US, Bx MRI, Bx
Likely inflammatory, no biopsy Inflammatory cells. No malignancy Squamous cell carcinoma Pleiomorphic ademoma MND, no Bx Not documented Follicular carcinoma Inflammatory cells, likely benign Not documented Follicular carcinoma Inflammatory cells, likely benign Orbital pseudotumor
Acute pulmonary oedema (3)
Haemothorax (1) Paratracheal mass (1) Large pleural effusion (2) Head and neck
Base of tongue mass (2) Supraglottic mass (1) Parotid mass (1) Suspicious thyroid lesions (7)
Orbital mass
1572
M.T. Crockett et al. / European Journal of Radiology 84 (2015) 1569–1573
Table 5 Summary of EV3 findings of intermediate clinical significance. Organ system
Finding (number)
Follow up
Outcome
Chest
Pleural plaques (1) Pulmonary consolidation (3)
No follow up 1. CT thorax 2. CXR 3. CXR CXR No follow up Cardiology referral
Not documented Resolved, likely infective or inflammatory Resolved, likely infective or inflammatory Resolved, likely infective or inflammatory Resloved Not documented Cardiology assessment
Vocal cord nodule (1)
1. No follow up 2. No follow up 3. US 4. US 5. No follow up 6. No Follow up 7. US 8. No follow up ENT referral
Not documented Not documented Multinodular goitre Multinodular goitre Not documented Not documented Benign cyst Not documented Discharged from clinic
Expansile bony lesion mandible (1)
MRI
Fibrous dysplasia
Small pleural effusion (1) Pulmonary artery dilatation (1) Heavy coronary artery calcification (1) Head and neck
MSK
Indeterminate thyroid lesions (8)
challenging, relying on the high spatial resolution of modern MDCT as well as complex 3D post processing techniques in order to allow accurate interpretation of the large volumes of acquired data. CTCCA has demonstrated diagnostic accuracies comparable to catheter DSA [11,15]. CTCCA is also non invasive, fast and lowers radiation dose to the patient compared to DSA [5,15–18]. In addition CTCCA also assesses non vascular structures of the head, neck and upper thorax and can incidentally identify a range of extra vascular abnormalities. Whilst many of these incidentally detected abnormalities are likely to have no clinical significance, others may be highly significant and result in early diagnosis and instigation of treatment of potentially curable diseases. The aim of this study was to assess the prevalence, clinical significance and subsequent management of incidental findings detected on CTCCA. The system used to classify incidental findings in this study was based upon C-RADS, a validated system for the standardised reporting of incidental findings in CT colonography. This system was chosen because of the similarities between CTCCA and CT colonography. Although both studies are undertaken to define a specific disease process in a single organ system, both studies also collect large volumes of data on adjacent structures. Consequently extracolonic findings in CT colonography and extravascular findings in CTCCA are incidental to the primary colonic or vascular pathology. A total of 19 consultant radiologists reported the CTCCA’s over a period of 4 years from 2009 to 2013 at a single tertiary referral University teaching hospital. 3 of these consultants were neuroradiologists, the remaining 16 consultants, whilst not formally trained in neuroradiology regularly reported on head and neck imaging. Overall rates of incidental findings in this study were high with 43% of patients undergoing CTCCA having at least one incidental finding. Potentially clinically significant findings were demonstrated in 14.2% of patients with 8.6% of patients having a highly clinically significant finding. The rate of clinically significant incidental findings in this study was slightly lower than similar studies assessing incidental findings in CTA of aorta and femoral vessels and CTA of the pulmonary arterial system [6,8]. This might be expected as CTCCA has a smaller field of view and images less organs and soft tissues. The majority of highly clinically significant incidental findings were identified in the lung apices or within the thyroid gland. Of the 26 highly significant findings, 4 were confirmed to be malignant lesions and 5 required acute intervention. In addition a high proportion of patients (19%) with highly clinically significant incidental findings did not receive appropriate follow up. The reasons
for this lack of follow up were not determined in this study. No standardised system for the reporting of CTCCAs was in place for the review period of our study and it was noted that there was significant inter and intra-reporter variability in the reporting of incidental findings by radiologists. Of the clinically significant incidental findings reported, some were included within the body of the report only and some were included in the body of the report and in the final report summary/conclusion. In addition follow up imaging and management was directly suggested for some incidental findings whilst for other incidental findings no such suggestion was made with decisions on follow up imaging or management being deferred to the requesting clinician. This is a situation that likely reflects the reality of current clinical practice in the majority of centres; however it is easy to see that this situation may lead to confusion on the part of referring physicians as to the actual clinical significance of the incidental findings reported. A defined classification system for the categorisation of extravascular incidental findings in CTCCA, such as the system used in this study would aid both radiologists in recording incidental findings and referring physicians in interpreting significance of such findings, thus improving appropriateness of patient follow up and management. The data was collected as a review of CTCCA reports and CTCCA studies were not re-read for the purpose of this study. This is another limitation as some incidental findings may have been missed by the initial reporting radiologist and therefore not captured. This means that the rates of incidental findings reported in this study may actually be an underestimation of their actual prevalence. Both the intra-hospital electronic patient database and national PACS system were consulted to assess patient follow up in EV3 and EV4 categories; however it cannot be completely excluded that some patients received follow up and further management at another institution which was not captured in the results of this study and this is a further limitation of this study. 5. Conclusion This study has demonstrated the presence of extra-vascular clinically significant incidental findings in a high proportion of patients undergoing CTCCA, the majority of findings within the lung apicies and thyroid gland. A significant minority of patients with these clinically important findings did not receive appropriate follow up. It is felt that adaptation of a standardised classification and reporting system, such as the EV-RADS system used in this study, would aid
M.T. Crockett et al. / European Journal of Radiology 84 (2015) 1569–1573
both radiologists and referring physicians in recording and communicating the significance of incidental findings identified on CTCCA.
[9]
Conflicts of interest [10]
None. [11]
References [1] Met R, Bipat S, Legemate DA, Reekers JA, Koelemay MJ. Diagnostic performance of computed tomography angiography in peripheral arterial disease: a systematic review and meta-analysis. JAMA 2009;301(4):415–24. [2] Barmase M, Kang M, Wig J, Kochhar R, Gupta R, Khandelwal N. Role of multidetector CT angiography in the evaluation of suspected mesenteric ischemia. Eur J Radiol 2011;80(3):e582–7. [3] Laghi A, Iannaccone R, Catalano C, Passariello R. Multislice spiral computed tomography angiography of mesenteric arteries. Lancet 2001;358(9282):638–9. [4] Mos IC, Klok FA, Kroft LJA, Dekkers DER, Huisman OMMV. Safety of ruling out acute pulmonary embolism by normal computed tomography pulmonary angiography in patients with an indication for computed tomography: systematic review and meta-analysis. J Thromb Haemost 2009;7(9): 1491–8. [5] Delgado Almandoz JE, Romero JM, Pomerantz SR, Lev MH. Computed tomography angiography of the carotid and cerebral, circulation. Radiol Clin North Am 2010;48(2):265–81, vii–viii. [6] Naidu SG, Hara AK, Brandis AR, Stone WM. Incidence of highly important extravascular findings detected on CT angiography of the abdominal aorta and the lower extremities. AJR Am J Roentgenol 2010;194(6):1630–4. [7] Iezzi R, Cotroneo AR, Filippone A, Di Fabio F, Merlino B, Bonomo L. Extravascular incidental findings at multislice CT angiography of the abdominal aorta and lower extremity arteries: a retrospective review study. Abdom Imaging 2007;32(4):489–94. [8] Hall WB, Truitt SG, Scheunemann LP, Shah SA, Rivera MP, Parker LA, et al. The prevalence of clinically relevant incidental findings on chest computed
[12] [13]
[14]
[15]
[16]
[17]
[18]
1573
tomographic angiograms ordered to diagnose pulmonary embolism. Arch Intern Med 2009;169(21):1961–5. Zalis ME, Barish MA, Choi JR, Dachman AH, Fenlon HM, Ferrucci JT, et al. CT colonography reporting and data system: a consensus proposal. Rays 2005;236(1):3–9. McFarland EGea ACR practice guideline for the performance of CT colonography in adults. ACR practice guidelines. http://www.acr.org/∼/ media/A81531ACA92F45058A83B5281E8FE826.pdf2009 Bash S, Villablanca JP, Jahan R, Duckwiler G, Tillis M, Kidwell C, et al. Intracranial vascular stenosis and occlusive disease: evaluation with CT angiography MR angiography, and digital subtraction angiography. AJNR Am J Neuroradiol 2005;26(5):1012–21. Esteban JM, Cervera V. Perfusion CT and angio CT in the assessment of acute stroke. Neuroradiology 2004;46(9):705–15. Jauch EC, Saver JL, Adams Jr HP, Bruno A, Connors JJ, Demaerschalk BM, et al. Guidelines for the early management of patients with acute ischemic stroke: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 2013;44(3):870–947. al BJe. ACR–ASNR practice guideline for the performance and interpretation of cevicocerebral computed tomography angiography (CTA). ACR guidelines; 2009. http://www.acr.org/∼/media/ACR/Documents/PGTS/ guidelines/Cervicocerebral Angio.pdf Nguyen-Huynh MN, Wintermark M, English J, Lam J, Vittinghoff E, Smith WS, et al. How accurate is CT angiography in evaluating intracranial atherosclerotic disease? Stroke 2008;39(4):1184–8. Duffis EJ, Jethwa P, Gupta G, Bonello K, Gandhi CD, Prestigiacomo CJ. Accuracy of computed tomographic angiography compared to digital subtraction angiography in the diagnosis of intracranial stenosis and its impact on clinical decision-making. J Stroke Cerebrovasc Dis 2013;22(7):1013–7. Li Q, Lv F, Yao G, Li Y, Xie P. 64-section multidetector CT angiography for evaluation of intracranial aneurysms: comparison with 3D rotational angiography. Acta Radiol 2013 (Epub ahead of print, 2013, September 26). Zhang LJ, Wu SY, Niu JB, Zhang ZL, Wang HZ, Zhao YE, et al. Dual-energy CT angiography in the evaluation of intracranial aneurysms: image quality, radiation dose, and comparison with 3D rotational digital subtraction angiography. AJR Am J Roentgenol 2010;194(1):23–30.
Contents lists available at ScienceDirect
European Journal of Radiology journal homepage: www.elsevier.com/locate/ejrad
Prevalence and clinical significance of extravascular incidental findings in patients undergoing CT cervico-cerebral angiography Matthew Thomas Crockett ∗ , Blathnaid Murphy 1 , Jennifer Smith 1 , Eoin Carl Kavanagh 2 Department of Radiology, Mater Misercordiae University Hospital, Dublin, Ireland
a r t i c l e
i n f o
Article history: Received 12 January 2015 Received in revised form 15 April 2015 Accepted 7 May 2015 Keywords: CT angiography CT cervico-cerebral angiography Head and neck Neuroradiology Incidental findings
a b s t r a c t Introduction: CT cervico-cerebral angiography (CTCCA) is now the first line diagnostic imaging modality for the majority of vascular pathologies of the head and neck with diagnostic value comparable to or better than traditional angiographic techniques. The aim of this study was to assess the prevalence, clinical significance and management of extravascular incidental findings detected on CTCCA. Materials and methods: A retrospective review of the CTCCA reports of 302 consecutive patients from 2009 to 2013 was undertaken. Extravascular incidental findings were classified, according to an adaptation of the CT colonography data and reporting system (CRADS), as EV1–EV4. EV1 = no incidental findings, EV2 = clinically insignificant incidental finding, EV3 = incidental finding of intermediate clinical significance, EV4 = highly clinically significant finding. Follow up of the electronic medical records of patients with EV3 or EV4 findings was undertaken to determine subsequent management. Results: Potentially clinically significant findings were demonstrated in 14.2% of patients with 8.6% of patients having a highly clinically significant finding. 4 incidental findings were confirmed to be malignant lesions and 5 required acute intervention. In addition 19% of patients with highly clinically significant incidental findings did not receive appropriate follow up. Discussion: This study has demonstrated the presence of clinically important incidental findings in a significant proportion of patients undergoing CTCCA with a significant minority of these patients not receiving follow up. A standardised method of reporting incidental findings, such as that used in this paper, would aid radiologists and referring physicians in recording and communicating these findings. © 2015 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Technological advances, including the development of multidetector row helical computed tomography (MDCT) and 3D post processing techniques, have led to multiple new clinical applications for computed tomography angiography (CTA). Whether assessing the peripheral vascular system, mesenteric vessels or pulmonary arterial system, CTA is now the first line diagnostic imaging modality for a myriad of vascular pathologies with diagnostic value comparable to or better than traditional angiographic techniques [1–4]. CTA of the head and neck, CT cervico-cerebral angiography (CTCCA) has displaced catheter directed digital subtraction
∗ Corresponding author. Tel.: +353 863669360; fax: +353 18032970. E-mail addresses: [email protected] (M.T. Crockett), [email protected] (B. Murphy), [email protected] (J. Smith), [email protected] (E.C. Kavanagh). 1 Tel.: +353 7593914; fax: +353 18032970. 2 Tel.: +353 866031274; fax: +353 18032970. http://dx.doi.org/10.1016/j.ejrad.2015.05.014 0720-048X/© 2015 Elsevier Ireland Ltd. All rights reserved.
angiography (DSA) as the initial investigation in the assessment of the majority of neurovascular pathologies [5]. Unlike DSA, in addition to assessing the head and neck vasculature, CTCCA also images adjacent structures with field of view including the lung apicies, thyroid gland, soft tissues and osseous structures of the head and neck. Consequently CTCCA has the potential to detect non vascular, “incidental” findings. Although many of these finding may be inconsequential to the patient, some may be highly clinically important such as early detection of a treatable malignancy. Previously published studies have assessed the prevalence and significance of findings incidentally identified on CT angiography of the aorta, lower limbs and pulmonary arterial system demonstrating highly significant findings in a large proportion of patients [6–8]. The results of these studies have increased awareness amongst both radiologists and referring physicians; however no similar study has been undertaken focusing on CTCCA, now one of the most commonly performed CT angiographic studies. The aim of this study was to define the prevalence, clinical significance and subsequent management of extravascular incidental findings detected on CTCCA. A more thorough knowledge of the
1570
M.T. Crockett et al. / European Journal of Radiology 84 (2015) 1569–1573
Table 1 Extra-vascular (EV) incidental findings classification system. Classification
Clinical significance
Example finding
Follow up
EV1 EV2 EV3 EV4
Normal/anatomic variant Low clinical significance Intermediate clinical significance High clinical significance
Azygous fissure Spinal degenerative disease Indeterminate thyroid nodule Lesion highly suspicious for malignancy. Pneumothorax
No follow up required No follow up required Follow up required as per clinical scenario 1. Follow up required (further imaging ± biopsy) 2. Urgent intervention required
most commonly detected clinically significant findings on CTCCA should help radiologists better define their search strategies whilst improving awareness of referring physicians and reducing potential for missed patient follow up. 2. Materials and methods A retrospective review of all CTCCA reports at a tertiary referral University hospital from November 2009 to December 2013 was conducted using the intra hospital electronic patient records system. Assessment of patient follow up was performed using the intra hospital patient record system and the National Integrated Imaging Management System (NIMIS), a nationwide PACS system covering the majority of hospitals in the state allowing capture of external patient follow up. All CTA’s at our institution were performed using a standardised protocol using a Seimens Somatom Definition 128 slice scanner. Bolus tracking software was used with a premonitoring scan centred on the aortic arch triggering the scan following administration of 80 ml of non-ionic IV contrast (Niopam 370) at a rate of 8 ml/s followed by a saline flush. FOV spanned aortic arch to skull vertex. Scan parameters consist of 6 mm collimation, 1 mm slice thickness, 1.2 pitch, kVp 120, mAs 90 (variable). Axial images were reconstructed using a medium smooth algorithm and presented for review on angiographic windows with 1 mm slice thickness. In addition axial, coronal and saggital 3D MIP images were reconstructed with 30 mm slice thickness to aid in visualisation of the intracranial arterial system. Images were viewed on a PACS workstation. Classification of incidental findings was based upon an adaptation of the CT colonography reporting and data system (C-RADS) [9,10]. Incidental findings were classified under the headings extravascular 1–4 (EV1–4). This classification system is summarised in Table 1. Studies with no incidental findings or those with
anatomic variants, such as an azygous fissure, were categorised as EV1. Those with incidental findings which were of low clinical significance and did not require further follow were classified as EV2. Studies with findings of intermediate clinical significance which required further follow up depending upon the clinical scenario were classified as EV3. Those studies with findings of high clinical significance which required further imaging follow up, biopsy or urgent intervention were classified as EV4. Studies containing multiple incidental findings were classified according to the most clinically significant finding. The results of follow up imaging studies, biopsies or interventions of patients with EV3 or EV4 findings were recorded. 3. Results 302 patients underwent CTCCA over the 3 year study period from 2009 to 2013. 171 (57%) were male and 131 (43%) were female. Mean age was 61 (range 16–95 years, SD 16.9). 207 studies (69%) were performed for assessment of suspected acute ischaemic stroke. Other indications for CTCCA are listed in Table 2. 151 incidental extravascular findings were detected in 131 patients. Of these 151 incidental findings 26 (17%) were in the E4 category, 17 (11%) were in the E3 category and 87 (72%) were in the Table 2 Indication for CT cervico-cerebral angiography. Indication
Number (%)
Acute ischaemic stroke Vascular stenosis (inc. carotid disease) Vascular anomaly (inc. intracranial aneurysm) Haemorrhagic stroke Arterial dissection Vasculitis Trauma
207 (69) 26 (9) 26 (9) 15 (5) 12 (4) 8 (2) 8 (2)
Fig. 1. Axial and coronal CTA images on soft tissue windows demonstrating a heterogeneously enhancing right parotid lesion. A biopsy was subsequently undertaken confirming the presence of a pleiomorphic adenoma.
M.T. Crockett et al. / European Journal of Radiology 84 (2015) 1569–1573 Table 3 Summary of incidental extra vascular findings by EV1–4 classification. EV category
No. of findings
% study cohort
% total incidental findings
EV4 EV3 EV2 EV1
26 17 87 172
8.6% 5.6% 28.8% 57%
17% 11% 72% N/A
1571
lesions (81%) underwent further imaging with 9 undergoing subsequent biopsy. 4 lesions were positive for malignancy; 2 follicular thyroid carcinomas, 1 pleomorphic ademoma and 1 squamous cell carcinoma. 5 of the 26 EV4 incidental findings (19%) were acute findings requiring immediate intervention including a haemothorax and acute severe pulmonary oedema. 5 of the 26 EV4 findings (19%) did not undergo appropriate follow up including 3 pulmonary nodules and 2 suspicious thyroid lesions. A summary of EV3 incidental findings of intermediate clinical significance and their follow up is provided in Table 5. Of the 17 patients with EV3 incidental findings, 10 (61%) underwent follow up. This follow up consisted of further imaging studies in 8 patients (47%) and referral to subspecialty clinics in 2 patients (12%) consisting of ENT and cardiology. No patient with an EV3 incidental finding underwent biopsy. 4. Discussion
Fig. 2. Axial CTA image on soft tissue windows demonstrating a peripherally enhancing heterogenous nodule within the right lobe of the thyroid gland. This lesion was subsequently biopsied confirming the presence of a follicular thyroid carcinoma.
E2 category. Of the 302 patients included in the study, 26 (8.2%) had incidental findings of high clinical significance and 17 (5.6%) had incidental findings of intermediate clinical significance (Table 3). A summary of EV4 incidental findings of high clinical significance and their follow up is provided in Table 4. Examples of EV4 findings are provided in Figs. 1 and 2. Of the 26 EV4 incidental findings 21 (81%) were lesions suspicious for malignancy which required further follow up. 16 out of these 21
CTCCA has become the first imaging modality in the assessment of a wide range of neurovascular pathologies including acute ischaemic stroke, cervico-cerebral vascular anomalies, stenoocclusive carotid arterial disease, vascular trauma and vasculitis [5]. The most common use of CTCCA is in the assessment of ischaemic stroke. Partly due to its accuracy in identifying intraarterial thrombus and partly due to its speed of acquisition and widespread availability in the emergency setting, CTCCA has, along with non contrast CT brain, become a mainstay in the assessment of patients presenting with suspected acute ischaemic stroke [11,12]. In this setting CTCCA allows not only allows more accurate diagnosis than NCCTB alone but also allows localisation of the intraarterial thrombus and consequently guides choice of therapeutic options [13]. In line with current guidelines in 2009 our institution introduced a protocol for patients presenting with suspected acute stroke with patients undergoing a NCCTB followed by CTCCA [13]. CTCCA is performed using bolus tracking software with a field of view encompassing the aortic arch inferiorly and skull vertex superiorly [14]. The complex nature of the cervico-cerebral vascular system means that CT angiographic imaging of this region is
Table 4 Summary of EV4 findings of high clinical significance. Organ system
Finding (number)
Follow up
Outcome
Chest
Pulmonary nodule (7)
1. CT thorax 2. CT thorax 3. CT thorax 4. CT thorax 5. Not performed 6. Not performed 7. Not performed 1. CXR 2. CXR 3. CXR CT thorax CT thorax, Bronchoscopy, Bx 1. CT thorax 2. CT thorax
Resolution of nodule (likely inflammatory) Resolution of nodule (likely inflammatory) Indeterminate, continued CT follow up Hamartoma Not documented Patient deceased Not documented Instigation of medical therapy Instigation of medical therapy Instigation of medical therapy Insertion of chest drain. Squamous metaplasia, continued follow up Insertion chest drain Medical therapy
1. MRI 2. MRI, Bx MRI, Bx US, Bx 1. US 2. Not performed 3. US, Bx 4. US, Bx 5. Not performed 6. US, Bx 7. US, Bx MRI, Bx
Likely inflammatory, no biopsy Inflammatory cells. No malignancy Squamous cell carcinoma Pleiomorphic ademoma MND, no Bx Not documented Follicular carcinoma Inflammatory cells, likely benign Not documented Follicular carcinoma Inflammatory cells, likely benign Orbital pseudotumor
Acute pulmonary oedema (3)
Haemothorax (1) Paratracheal mass (1) Large pleural effusion (2) Head and neck
Base of tongue mass (2) Supraglottic mass (1) Parotid mass (1) Suspicious thyroid lesions (7)
Orbital mass
1572
M.T. Crockett et al. / European Journal of Radiology 84 (2015) 1569–1573
Table 5 Summary of EV3 findings of intermediate clinical significance. Organ system
Finding (number)
Follow up
Outcome
Chest
Pleural plaques (1) Pulmonary consolidation (3)
No follow up 1. CT thorax 2. CXR 3. CXR CXR No follow up Cardiology referral
Not documented Resolved, likely infective or inflammatory Resolved, likely infective or inflammatory Resolved, likely infective or inflammatory Resloved Not documented Cardiology assessment
Vocal cord nodule (1)
1. No follow up 2. No follow up 3. US 4. US 5. No follow up 6. No Follow up 7. US 8. No follow up ENT referral
Not documented Not documented Multinodular goitre Multinodular goitre Not documented Not documented Benign cyst Not documented Discharged from clinic
Expansile bony lesion mandible (1)
MRI
Fibrous dysplasia
Small pleural effusion (1) Pulmonary artery dilatation (1) Heavy coronary artery calcification (1) Head and neck
MSK
Indeterminate thyroid lesions (8)
challenging, relying on the high spatial resolution of modern MDCT as well as complex 3D post processing techniques in order to allow accurate interpretation of the large volumes of acquired data. CTCCA has demonstrated diagnostic accuracies comparable to catheter DSA [11,15]. CTCCA is also non invasive, fast and lowers radiation dose to the patient compared to DSA [5,15–18]. In addition CTCCA also assesses non vascular structures of the head, neck and upper thorax and can incidentally identify a range of extra vascular abnormalities. Whilst many of these incidentally detected abnormalities are likely to have no clinical significance, others may be highly significant and result in early diagnosis and instigation of treatment of potentially curable diseases. The aim of this study was to assess the prevalence, clinical significance and subsequent management of incidental findings detected on CTCCA. The system used to classify incidental findings in this study was based upon C-RADS, a validated system for the standardised reporting of incidental findings in CT colonography. This system was chosen because of the similarities between CTCCA and CT colonography. Although both studies are undertaken to define a specific disease process in a single organ system, both studies also collect large volumes of data on adjacent structures. Consequently extracolonic findings in CT colonography and extravascular findings in CTCCA are incidental to the primary colonic or vascular pathology. A total of 19 consultant radiologists reported the CTCCA’s over a period of 4 years from 2009 to 2013 at a single tertiary referral University teaching hospital. 3 of these consultants were neuroradiologists, the remaining 16 consultants, whilst not formally trained in neuroradiology regularly reported on head and neck imaging. Overall rates of incidental findings in this study were high with 43% of patients undergoing CTCCA having at least one incidental finding. Potentially clinically significant findings were demonstrated in 14.2% of patients with 8.6% of patients having a highly clinically significant finding. The rate of clinically significant incidental findings in this study was slightly lower than similar studies assessing incidental findings in CTA of aorta and femoral vessels and CTA of the pulmonary arterial system [6,8]. This might be expected as CTCCA has a smaller field of view and images less organs and soft tissues. The majority of highly clinically significant incidental findings were identified in the lung apices or within the thyroid gland. Of the 26 highly significant findings, 4 were confirmed to be malignant lesions and 5 required acute intervention. In addition a high proportion of patients (19%) with highly clinically significant incidental findings did not receive appropriate follow up. The reasons
for this lack of follow up were not determined in this study. No standardised system for the reporting of CTCCAs was in place for the review period of our study and it was noted that there was significant inter and intra-reporter variability in the reporting of incidental findings by radiologists. Of the clinically significant incidental findings reported, some were included within the body of the report only and some were included in the body of the report and in the final report summary/conclusion. In addition follow up imaging and management was directly suggested for some incidental findings whilst for other incidental findings no such suggestion was made with decisions on follow up imaging or management being deferred to the requesting clinician. This is a situation that likely reflects the reality of current clinical practice in the majority of centres; however it is easy to see that this situation may lead to confusion on the part of referring physicians as to the actual clinical significance of the incidental findings reported. A defined classification system for the categorisation of extravascular incidental findings in CTCCA, such as the system used in this study would aid both radiologists in recording incidental findings and referring physicians in interpreting significance of such findings, thus improving appropriateness of patient follow up and management. The data was collected as a review of CTCCA reports and CTCCA studies were not re-read for the purpose of this study. This is another limitation as some incidental findings may have been missed by the initial reporting radiologist and therefore not captured. This means that the rates of incidental findings reported in this study may actually be an underestimation of their actual prevalence. Both the intra-hospital electronic patient database and national PACS system were consulted to assess patient follow up in EV3 and EV4 categories; however it cannot be completely excluded that some patients received follow up and further management at another institution which was not captured in the results of this study and this is a further limitation of this study. 5. Conclusion This study has demonstrated the presence of extra-vascular clinically significant incidental findings in a high proportion of patients undergoing CTCCA, the majority of findings within the lung apicies and thyroid gland. A significant minority of patients with these clinically important findings did not receive appropriate follow up. It is felt that adaptation of a standardised classification and reporting system, such as the EV-RADS system used in this study, would aid
M.T. Crockett et al. / European Journal of Radiology 84 (2015) 1569–1573
both radiologists and referring physicians in recording and communicating the significance of incidental findings identified on CTCCA.
[9]
Conflicts of interest [10]
None. [11]
References [1] Met R, Bipat S, Legemate DA, Reekers JA, Koelemay MJ. Diagnostic performance of computed tomography angiography in peripheral arterial disease: a systematic review and meta-analysis. JAMA 2009;301(4):415–24. [2] Barmase M, Kang M, Wig J, Kochhar R, Gupta R, Khandelwal N. Role of multidetector CT angiography in the evaluation of suspected mesenteric ischemia. Eur J Radiol 2011;80(3):e582–7. [3] Laghi A, Iannaccone R, Catalano C, Passariello R. Multislice spiral computed tomography angiography of mesenteric arteries. Lancet 2001;358(9282):638–9. [4] Mos IC, Klok FA, Kroft LJA, Dekkers DER, Huisman OMMV. Safety of ruling out acute pulmonary embolism by normal computed tomography pulmonary angiography in patients with an indication for computed tomography: systematic review and meta-analysis. J Thromb Haemost 2009;7(9): 1491–8. [5] Delgado Almandoz JE, Romero JM, Pomerantz SR, Lev MH. Computed tomography angiography of the carotid and cerebral, circulation. Radiol Clin North Am 2010;48(2):265–81, vii–viii. [6] Naidu SG, Hara AK, Brandis AR, Stone WM. Incidence of highly important extravascular findings detected on CT angiography of the abdominal aorta and the lower extremities. AJR Am J Roentgenol 2010;194(6):1630–4. [7] Iezzi R, Cotroneo AR, Filippone A, Di Fabio F, Merlino B, Bonomo L. Extravascular incidental findings at multislice CT angiography of the abdominal aorta and lower extremity arteries: a retrospective review study. Abdom Imaging 2007;32(4):489–94. [8] Hall WB, Truitt SG, Scheunemann LP, Shah SA, Rivera MP, Parker LA, et al. The prevalence of clinically relevant incidental findings on chest computed
[12] [13]
[14]
[15]
[16]
[17]
[18]
1573
tomographic angiograms ordered to diagnose pulmonary embolism. Arch Intern Med 2009;169(21):1961–5. Zalis ME, Barish MA, Choi JR, Dachman AH, Fenlon HM, Ferrucci JT, et al. CT colonography reporting and data system: a consensus proposal. Rays 2005;236(1):3–9. McFarland EGea ACR practice guideline for the performance of CT colonography in adults. ACR practice guidelines. http://www.acr.org/∼/ media/A81531ACA92F45058A83B5281E8FE826.pdf2009 Bash S, Villablanca JP, Jahan R, Duckwiler G, Tillis M, Kidwell C, et al. Intracranial vascular stenosis and occlusive disease: evaluation with CT angiography MR angiography, and digital subtraction angiography. AJNR Am J Neuroradiol 2005;26(5):1012–21. Esteban JM, Cervera V. Perfusion CT and angio CT in the assessment of acute stroke. Neuroradiology 2004;46(9):705–15. Jauch EC, Saver JL, Adams Jr HP, Bruno A, Connors JJ, Demaerschalk BM, et al. Guidelines for the early management of patients with acute ischemic stroke: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 2013;44(3):870–947. al BJe. ACR–ASNR practice guideline for the performance and interpretation of cevicocerebral computed tomography angiography (CTA). ACR guidelines; 2009. http://www.acr.org/∼/media/ACR/Documents/PGTS/ guidelines/Cervicocerebral Angio.pdf Nguyen-Huynh MN, Wintermark M, English J, Lam J, Vittinghoff E, Smith WS, et al. How accurate is CT angiography in evaluating intracranial atherosclerotic disease? Stroke 2008;39(4):1184–8. Duffis EJ, Jethwa P, Gupta G, Bonello K, Gandhi CD, Prestigiacomo CJ. Accuracy of computed tomographic angiography compared to digital subtraction angiography in the diagnosis of intracranial stenosis and its impact on clinical decision-making. J Stroke Cerebrovasc Dis 2013;22(7):1013–7. Li Q, Lv F, Yao G, Li Y, Xie P. 64-section multidetector CT angiography for evaluation of intracranial aneurysms: comparison with 3D rotational angiography. Acta Radiol 2013 (Epub ahead of print, 2013, September 26). Zhang LJ, Wu SY, Niu JB, Zhang ZL, Wang HZ, Zhao YE, et al. Dual-energy CT angiography in the evaluation of intracranial aneurysms: image quality, radiation dose, and comparison with 3D rotational digital subtraction angiography. AJR Am J Roentgenol 2010;194(1):23–30.
