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CT for evaluation of pediatric oncology patients?
Clinical Imaging 39 (2015) 794–798
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Clinical Imaging journal homepage: http://www.clinicalimaging.org
Is dedicated chest CT needed in addition to PET/CT for evaluation of pediatric oncology patients? Sarah Z. Goodman, Jeremy Rosenblum, Ibrahim Tuna, Jeffrey M. Levsky, Rosanna Ricafort, Benjamin Taragin ⁎ 111 E210 Street, Bronx, NY, 10467
a r t i c l e
i n f o
Article history: Received 10 February 2015 Received in revised form 26 April 2015 Accepted 8 May 2015 Keywords: PET/CT Utilization Oncology Pediatric Imaging
a b s t r a c t Purpose: To assess the computed tomography (CT) portion of a positron emission tomography (PET)/CT, at lower dose without breath holding, as compared to diagnostic chest CT (dCTC), performed at regular dose with breath holding, and question the necessity of both for patient care in pediatric oncology. Materials and Methods: This retrospective study included 46 pediatric patients with histologically proven malignant tumors that had a total of 119 scans. Results: A total of 29 discrepancies were found between dCTC and PET/CT reports. Conclusion: In the evaluation of metastatic thoracic disease in pediatric oncology patients, the non-breath holding CT portion of PET/CT has sensitivity and specificity that approaches dCTC. © 2015 Elsevier Inc. All rights reserved.
1. Introduction In the current era of health care delivery, there is an increasing effort to minimize unnecessary radiation along with an equally important focus on proper utilization and imaging protocols. In the care of the oncology patients, radiologic imaging provides essential information on tumor stage, morphology, and presence of metastasis and has profound influence on disease management. It is standard practice at pediatric oncology centers to stage disease and to assess response to treatment for specific malignancies by performing a 18F-fluorodeoxyglucose (FDG) positron emission tomography (PET)/computed tomography (CT) of the whole body as well as diagnostic CT scans of the chest abdomen and pelvis. In the past, while CT alone was a useful tool for staging malignancies, the use of PET/CT continues to increase as it has repeatedly been shown to improve initial staging and detection of recurrence compared to CT alone [1,2]. The increased glucose metabolism and resultant FDG accumulation [3] allows localization of hypermetabolic cells while the CT portion both aids in the attenuation correction of the PET images and improves localization of positive PET findings [4,5]. However, the separate performance of diagnostic CT and PET/CT has significant drawbacks. Separate appointments for CT scanning require additional time away from school for the patient, work for the guardians, and in many cases repeat sedation. These additional factors take a toll on both the patient and family. Decreasing the number of CT scans and follow-up visits required would help to mitigate these factors and improve overall quality of life of the patients and their families. At ⁎ Corresponding author. 111 E210 Street, Bronx, NY, 10467. Tel.: +1-718-920-5213. E-mail address: btaragin@montefiore.org (B. Taragin). http://dx.doi.org/10.1016/j.clinimag.2015.05.005 0899-7071/© 2015 Elsevier Inc. All rights reserved.
our institution, the billed fee per diagnostic CT scan of the chest [diagnostic chest CT (dCTC)] scan is approximately US$300. Minimizing the number of redundant scans per patient could potentially impact health care costs substantially. The diagnostic scan may also represent an unnecessary health care expenditure. Perhaps more importantly, the additive diagnostic radiation involved in performing a separate PET/CT and diagnostic CT is concerning, especially in the care of the pediatric cancer patient. Long-term studies have shown that low-dose radiation in childhood carries a significantly increased lifetime risk of developing fatal cancer [6–9]. Recent research suggests that children are 10 times more radiosensitive than adults [10], making children more likely to develop a malignancy when compared to adults receiving an equivalent dose of radiation. Additionally, childhood cancer survivors have an increased risk of developing subsequent neoplasms due to both innate factors such as genetics, immune function, and hormone status, as well as secondary factors such as primary cancer therapy, environmental exposures, and lifestyle. The Childhood Cancer Survivor Study reported a 30-year cumulative incidence of 20.5% for all subsequent neoplasms, the risk of which remains elevated for more than 30 years from diagnosis of the primary cancer [9]. The elimination of a possible unnecessary radiation dose without compromising diagnostic efficacy [6] would better conform to the ALARA (“as low as reasonably achievable”) principle. Reducing the total number of CT studies and decreasing the number of scan “phases” are of the most powerful means of radiation reduction. With the rapid improvements of the CT component of PET/CT technology, it remains unclear if the CT performed for attenuation correction can provide additional diagnostic information [11]. While studies in adults have compared the accuracy of the CT portion of PET/CT in
S.Z. Goodman et al. / Clinical Imaging 39 (2015) 794–798
Total number of scans (119)
Of these, 9 paired scans occurred on the same day. In 47 paired scans, the PET/CT was performed prior to the dCTC, and in 63 paired scans, the dCTC occurred prior to the PET/CT.
60 59
2.2. Imaging Methods
Table 1 Patient demographics Total number of patients (n=46) Male 26 Female 20 Age at first scan (years) 0–5 9 6–11 17 12–17 19 18–21 1 Total 46
24 41 53 1 119
evaluation of malignancies [12,13], the sensitivity of the lower-dose CT as an independent diagnostic tool in pediatric oncology patients compared with dCTC has not, to our knowledge, been assessed. The current study aims to measure the sensitivity and specificity of the CT portion of the PET/CT as compared to the dCTC in our pediatric oncology population at The Children’s Hospital at Montefiore. We hypothesized that the low-dose CT performed at the time of PET can provide similar diagnostic information as the dedicated chest CT. If proven correct, safe omission of the separate chest CT could result in a significant reduction in radiation as well as health care utilization without significant adverse effects in this extraordinary vulnerable population. 2. Methods and Materials 2.1. Patient Population This institutional review board approved, Health Insurance Portability and Accountability Act compliant, retrospective study included pediatric oncology patients at The Children’s Hospital of Montefiore with histologically proven malignant tumors (see Tables 1 and 2). Patients were selected through review of the Medical Center Radiology Information System database that yielded 48 patients between 01-01-2008 and 01-01-2011 who had paired scans (both dCTC and PET/CT within 4 weeks). There were 121 such paired studies in 48 patients. The population consisted of 26 boys and 22 girls age 2–17 years. Scans were obtained either for staging at initial diagnosis or for surveillance of recurrence after achieving a documented complete remission of their disease. Two patients were excluded; one was excluded because ultimately the patient was found not to have an oncologic diagnosis; the other was excluded because the imaging obtained was due to prolonged fever not for staging or surveillance of recurrence. Our study population, therefore, consisted of 46 pediatric oncology patients who had a total 119 paired scans. The patients were evaluated by 18F-FDG imaging using a combined PET/CT system (Phillips Gemini TF TOF/64-detector rows) and a single dCTC (General Electric Imaging Systems, LightSpeed VCT/64-detector rows) within 30 days.
Table 2 Malignancies included in study
Adrenocortical carcinoma Chondrosarcoma Germ cell tumor Hodgkin’s lymphoma Leiomyosarcoma Lymphoproliferative disease Nasopharyngeal carcinoma Neuroendocrine tumor Non-Hodgkin’s lymphoma Osteosarcoma Rhabdomyosarcoma Small round blue cell tumor Other Total
795
Total number of patients (n=46)
Total number of scans (n=119)
1 1 2 11 2 3 2 3 5 1 9 3 2 46
13 1 10 38 2 3 10 3 15 1 19 3 2 119
The hybrid PET/CT system used a combined multi-detector helical CT with a dedicated PET scanner. For PET/CT acquisition, the CT was acquired with a peak kilovoltage (kVp) of 120, 20–30 mAs, and a wide field of view (FOV) and was reconstructed with a slice thickness of 5 mm in lung and soft tissue windows (as per the department protocols at that time). Images were acquired without administration of oral or intravenous contrast and with the patient in free breathing with arms at side. No anesthesia or sedation was administered. PET/CT scanning was started 60 min after 18F-FDG injections. The CT scan was obtained prior to the PET scan. No procedures were performed on the day of the PET/CT prior to the study. The dCTC was performed in helical mode with a dedicated 64-slice CT scanner. The X-ray tube was operated with a kVp of 100 and slice thickness of 0.625 mm, weight-based current/time product (mAs), and standard FOV per patient dimensions. Images were reconstructed with a slice thickness of 2.5 mm in lung and soft tissue windows (as per the department protocols at that time). If chest CT was performed alone, no contrast was administered. If the chest CT was performed in conjunction with an abdomen and pelvis, CT intravenous contrast was administered. Imaging was performed with patients performing breath-holding maneuvers or suspended respiration if intubated and with arms above head. 2.3. Dose Calculations Current CT scanners provide dose information including dose length product (DLP) for each scan obtained. To best estimate the effective dose for each dCTC, we used region-specific conversion coefficients in children of various ages (1, 5, 10, and 15 years) developed by the European Commission Concerted Action on CT [14] and validated in a large survey of adult and pediatric CT doses in the UK [14,15]. They described age-specific coefficient conversion factors for different age ranges. Children from 4 months to 2 years 11 months were assigned the coefficient associated with the 1 age group, those from 3 years to 7 years 11 months were assigned the coefficient associated with the 5 age group, those from 8 years to 14 years 11 months were assigned the coefficient associated with the 10 age group, and those 15 years and older were assigned the coefficient associated with the 15 age group. These coefficients and groupings were obtained from those used by Thomas and Wang [16]. Our scanners reported DLP using a 32-cm phantom. The DLP, when available, was then multiplied by the age appropriate conversion coefficient to obtain the effective dose: effective dose=DLP×conversion coefficient (14). In accordance with the recommendations of Shrimpton et al. [14], in children b15 years of age, DLP was multiplied by a factor of 2 prior to applying the conversion factor: effective dose=DLP×conversion coefficient×2 [14]. 2.4. Image Interpretation All attending finalized reports for paired studies were collected and reviewed by the pediatric radiology fellow (IT), with 5 years of radiology experience. A scoring system and protocol for discrepant results was developed prior to review. The fellow reviewed reports from paired studies and notated all studies with positive findings. He then reviewed images from all positive paired studies and graded them as concurrent or discrepant. Paired studies with discrepant findings were then independently reviewed by a board certified pediatric radiologist (BT), with 13 years of radiology experience, and a board certified thoracic radiologist (JL), with 7 years of radiology experience. Reviewers were blinded to original reports of the discrepant studies. During discrepant
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image review sessions, the CT portion of the PET/CT was reviewed first and independent from the PET to prevent bias. The dCTC was then reviewed. Imaging findings on discrepant studies were reviewed and reclassified as either radiologically significant discrepancies (presence of pulmonary nodules, bony metastasis, adenopathy, and pleural effusions) or non-radiologically significant findings/discrepancies (atelectasis, posttherapy scarring, or stable nodules). Findings from these review sessions were scored on de-identified score sheets. Any persistent disagreement between attending radiologists regarding scoring of findings was resolved by panel review and discussion among all three radiologists until consensus was reached. In cases where there were true discrepancies found between the paired sets, the PET images were also reviewed and the combined findings along with contemporaneous de-identified clinical scenario were presented to an attending pediatric oncologist (RR), with 7 years of postfellowship clinical experience, for determination of clinical significance. 2.5. Data Analysis A positive finding on the unenhanced CT portion of the PET/CT was defined as true positive or false positive if the finding was confirmed or excluded, respectively, by the dCTC. A negative finding on the unenhanced CT portion of the PET/CT was defined as true negative or false negative if the finding was excluded or confirmed, respectively, on the dCTC. Performance indices of the unenhanced CT portion of the PET/CT including sensitivity specificity and positive and negative predictive values were calculated and 95% confidence intervals (95% CIs) for each parameter were calculated using an online calculator adhering to standard statistical methods. 3. Results A total of 119 PET/CT scans in 46 children with an average age at the time of the scan of 11 years (range, 2–18 years) were reviewed (see Fig. 1). Of the paired scan reports, 49 studies were normal on both
dCTC and PET/CT, 41 had concordant positive findings, and 29 were discordant (Table 3). On review of the actual image sets in the 29 discrepant pairs, 2/29 (6.9%) of the discordances had radiologically significant discrepancies, both of which were small subcentimeter nodules; 27/29 (93.1%) were determined upon review not to be of radiologic significance. A total of 13 PET/CT reports were negative, whereas dCTC reports described unchanged nodules. These nodules were all correctly noted by blinded readers in our study on review of PET/CT low-dose CT images. A total of 5 PET/CT reports were read as stable, where dCTC reports described unchanged nodules, and these nodules were all correctly noted by blinded readers in our study on review of PET/CT CT images. A total of 9 PET/CT reports were read as stable, where dCTC reports described atelectasis or posttherapy scarring, and these findings were all correctly noted by blinded readers in our study on review of PET/CT CT images. Of the two discrepant cases referred for determination of clinical significance by a pediatric oncologist, one was classified as clinically significant (Fig. 2) and one was not (Fig. 3). The discrepancy deemed not clinically significant (Fig. 2) was graded such that because this nodular density was seen intermittently on prior studies and was considered an area of itinerant atelectasis because of its intermittent disappearance and shape. The discrepancy deemed significant (Fig. 3) was graded as such because the findings of multiple nodules would require biopsy in blinded clinical review. Of note, in the real-time clinical setting, the dCTC that was performed first showed a cluster of nodules that had resolved on the subsequent PET/CT CT images. Therefore, no biopsy was performed. When comparing the unenhanced CT portion of the PET/CT to the dCTC, there were 68 true positives, 49 true negatives, 2 false negatives, and 0 false positive. The sensitivity and specificities of the unenhanced CT portion of the PET were 97.1% 95% CI (89.1–99.5) and 100% 95% CI (90.4-1), respectively. The positive predictive value of the unenhanced CT portion of the PET was 100% with a 95% CI (93.3-1) and the negative predictive value was 96.0% 95% CI (85.4–99.3).
Fig. 1. Image interpretation process.
S.Z. Goodman et al. / Clinical Imaging 39 (2015) 794–798
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Table 3 Listing of discrepant reports: Highlighted cases remained discordant after image review Scan number
Patient malignancy
PET report
Chest CT report
104 16 42 73 80 88 39 50 9 152 13 61 64 107 123 166 124 11 99 66 75 143 93 160 12 70 140 142 135 87
Lymphoma Lymphoma NC Rhabdo Rhabdo Lymphoma Rhabdo Lymphoma Lymphoma Lymphoma Rhabdo ACC NC Lymphoma Rhabdo Lymphoma Lymphoma Lymphoma Rhabdo Lymphoma NC ACC Rhabdo Lymphoma Lymphoma ACC Lymphoma Lymphoma Rhabdo Lymphoma
Normal Normal Normal Stable Stable Nodule(s) Normal Normal Nodule(s) Normal Normal Normal Stable Stable Stable Stable Nodule(s) Stable Normal Normal Normal Normal Normal Normal Normal Nodule(s) Nodule(s) Nodule(s) Nodule(s) Stable
Volume loss Nodule(s) Nodule(s) Nodule(s) Nodule(s) Stable Nodule(s) Nodule(s) Normal Nodule(s) Nodule(s) Nodule(s) Nodule(s) Nodule(s) Nodule(s) Nodule(s) Stable Nodule(s) Nodule(s) Nodule(s) Nodule(s) Lymphadenopathy Nodule(s) Lymphadenopathy Nodule(s) Normal Nodule(s) Nodule(s) Stable Nodule(s)
ACC, adrenal cortical carcinoma; Rhabdo, rhabdomyosarcoma; NC, nasopharyngeal carcinoma.
Of the 119 scans included in the study, 89 were performed prior to institutional recording of dose information. Of the DLP that was recorded in the 30 remaining scans and was categorized by patient age, the average dose for the dCTC scans was 4.99 mSv (See Table 4). 4. Discussion In a continuing effort to reduce childhood radiation exposure, this study sought to investigate whether the CT portion of PET/CT could serve a primary diagnostic role in a pediatric oncologic population. Our data demonstrate that the unenhanced CT portion may provide independent diagnostic information of different value if reviewed as a standalone diagnostic study, not as just a tool for better PET/CT interpretation. Currently, the CT portion of PET/CT in many centers is a low-dose, unenhanced study and used primarily for image localization and
Fig. 2. CT and PET/CT images of a female aged 2 years 6 months with rhabdomyosarcoma of the bladder. dCTC and PET/CT were performed on the same day. A micro-nodule (arrow) is seen on (A) dCTC in the left lower lobe (study performed during free breathing). The micro-nodule is not visualized on the free breathing CT portion of the PET/CT (B) (same anatomic level based on bronchovascular anatomy of the lung). This finding was considered a significant miss on the low-dose CT performed as part of PET/CT. However, as per the evaluation of the oncology team, this finding necessitated no additional therapy. The opacity was no longer present on subsequent imaging done for routine follow-up.
Fig. 3. CT and PET/CT images of a different female aged 2 years 6 months with nasal rhabdomyosarcoma, and dCTC was performed 5 days prior to the PET/CT. A cluster of nodules (arrow) is seen on (A) dCTC at the level of the liver (study performed during free breathing). The nodules are not visualized on the free breathing CT portion of the PET/CT (B) (same anatomic level based on bronchovascular anatomy of the lung). This finding was considered a significant miss on the low-dose CT performed as part of PET/CT. A repeat dCTC performed 1 week later with prone imaging demonstrated resolution of the finding.
attenuation correction. However, additional diagnostic information can be added through independent readings of the unenhanced CT portion of PET/CT. For example, in a study examining the unenhanced CT portion of 18F-fluoride PET/CT in patients with known malignancies, there were clinically significant findings in 27.2% of patients when the CT portion was read independently. Many of these findings included small pulmonary nodules [17]. Our study further supports this notion that, in pediatric patients with the unenhanced CT portion of PET/CT with a sensitivity of 97.1% and a specificity of 100%, it performs almost as well as dCTC. In our study, many of the discrepant reports were attributable to stylistic reporting differences. This fact is exemplified by the number of true discrepancies (2), found after dedicated review of the images, which was significantly lower than the number of discrepant reports (29). Blinded review of both studies from the falsely discrepant 27 pairs revealed that 13 paired reports were discrepant only in regard to differences in description of unchanged nodules, 5 regarding categorization of stable findings, and 9 report omissions of apparent but not significant findings. Both of our study’s true discrepancies occurred in patients with soft tissue sarcomas. A retrospective study that investigated the effectiveness of FDG-PET/CT in the diagnosis of local recurrence and distant metastases of malignant bone and soft tissue sarcomas in children found that, while FDG-PET/CT was highly sensitive (100%) for detection of local recurrence, it had lower sensitivity (77%) for the detection of distant metastases, such as those in the lungs [18]. Our results suggest re-examination of these findings. While these malignancies can be more aggressive than many of the others included in this study, a separate dCTC may not be warranted in this population if low-dose CT performed with PET performs as equally. Historically at our institution, the CT portion of the PET/CT was reviewed by the nuclear medicine attending physician and radiology residents but not routinely read by a pediatric radiologist specializing in cross-sectional image interpretation. Our results have caused us to review our current imaging protocols allowing for CT review at the time of the performance of PET/CT. If the CT is deemed diagnostic without any findings, we now endeavor, in specific patients with known stable disease and non-aggressive histology, to contact clinicians and discuss canceling possibly redundant imaging. Prior studies had shown that the use of CT intravenous contrast in PET/ CT has been associated with an overestimation of the standardized uptake value after CT-based attenuation correction of PET data [19,20]. Therefore, our institution’s protocol is to perform PET/CT without contrast. Newer publications have dispelled this potential pitfall [21,22]. This potential change in protocol, namely intravenour contrast administration during PET/CT, locally and perhaps nationally if standardized could make the CT of the PET/CT even closer to diagnostic CT accuracy. Administration of contrast may also allow for simultaneous acquisition of abdominal and pelvic CT scans that currently are performed separately. Continuing hardware and software improvements in the PET/CT scanners will allow changes in current technique that would provide
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Table 4 Effective dose for dCTC Age
Number of scans
DLP mean
DLP range
SD
Conversion coefficient
Mean effective dose (mSv)
Range of effective dose (mSv)
SD
1 5 10 15
5 12 11 2
151.84 158.56 310.05 178.20
48.47–233.57 64.44–287.95 155.37–555.98 113.45–242.95
66.35 58.86 139.60 91.57
0.026 0.018 0.013 0.014
3.95 3.37 7.70 2.50
1.26–6.07 2.10–5.82 3.94–14.45 1.59–3.40
1.73 1.22 3.84 1.28
better image resolution. These include optimized FOV, modulating tube current, reconstruction algorithms, and decreased slice thickness all of which likely would result in improved lesion conspicuity even at the dose used for PET/CT scanning. Most of these options are already incorporated into state-of-the-art, low-dose CT scanners but many PET/CT scanners have not yet been updated. Our findings suggest that there may be a concurrent cost saving and radiation reduction effect that should encourage updating older scanners. Additionally, newer PET/CT scanners with faster acquisition time of the CT images will allow pediatric PET/CT to be performed without artifacts from breathing motion, a previously reported limitation in using the CT images from the PET/CT [23]. Current understanding of the harmful effects of diagnostic radiation motivates us to comply as best possible with the ALARA principle. Reducing the total number of CT studies is of the most powerful means of radiation reduction. Indeed, even the lay press [24] has highlighted double scanning of the chest as often inappropriate. We feel that our results and subsequent change in practice should be an impetus for this possible change in current resource utilization and clinical protocols. Our study had multiple limitations including our population and overall scan frequency. Our study comprised 119 paired scans that occurred in only 46 patients. Additionally, the overall incidence of new pulmonary disease in our population was low. Furthermore, some individual patients in our study received a disproportionate number of scans, for example, 1 patient with adrenocortical carcinoma had 13 paired scans during our study timeframe. This caused bias in our results and precludes us from confirming whether our findings were histology specific or patient specific. Lastly, the our study population that included multiple tumor histologies and uneven distribution of patients within the different diagnosis limits our conclusions. Larger studies would be helpful in proving the trends seen in our study. Since, in our study, the chest CT portion of PET/CT has sensitivity and specificity that approaches dCTC, we feel that additional multi-center collaboration is warranted to determine which patient subsets do not need both tests. If implemented at our institution, this protocol would result in a per incidence savings of US$300 and 4.99 mSv. Local interdepartmental collaboration as well as national interdisciplinary dialog between radiologists, oncologists, and nuclear medicine physicians is necessary to optimize future oncologic follow-up imaging protocols and algorithms. In particular, the CT portion of a PET/CT can be used in place of a dCTC when routine follow-up protocols indicate that a PET is necessary. Such collaboration may obviate repeat imaging in select cases. This could improve patient care, decrease overall health care cost, and lower patient’s diagnostic radiation dose.
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Clinical Imaging journal homepage: http://www.clinicalimaging.org
Is dedicated chest CT needed in addition to PET/CT for evaluation of pediatric oncology patients? Sarah Z. Goodman, Jeremy Rosenblum, Ibrahim Tuna, Jeffrey M. Levsky, Rosanna Ricafort, Benjamin Taragin ⁎ 111 E210 Street, Bronx, NY, 10467
a r t i c l e
i n f o
Article history: Received 10 February 2015 Received in revised form 26 April 2015 Accepted 8 May 2015 Keywords: PET/CT Utilization Oncology Pediatric Imaging
a b s t r a c t Purpose: To assess the computed tomography (CT) portion of a positron emission tomography (PET)/CT, at lower dose without breath holding, as compared to diagnostic chest CT (dCTC), performed at regular dose with breath holding, and question the necessity of both for patient care in pediatric oncology. Materials and Methods: This retrospective study included 46 pediatric patients with histologically proven malignant tumors that had a total of 119 scans. Results: A total of 29 discrepancies were found between dCTC and PET/CT reports. Conclusion: In the evaluation of metastatic thoracic disease in pediatric oncology patients, the non-breath holding CT portion of PET/CT has sensitivity and specificity that approaches dCTC. © 2015 Elsevier Inc. All rights reserved.
1. Introduction In the current era of health care delivery, there is an increasing effort to minimize unnecessary radiation along with an equally important focus on proper utilization and imaging protocols. In the care of the oncology patients, radiologic imaging provides essential information on tumor stage, morphology, and presence of metastasis and has profound influence on disease management. It is standard practice at pediatric oncology centers to stage disease and to assess response to treatment for specific malignancies by performing a 18F-fluorodeoxyglucose (FDG) positron emission tomography (PET)/computed tomography (CT) of the whole body as well as diagnostic CT scans of the chest abdomen and pelvis. In the past, while CT alone was a useful tool for staging malignancies, the use of PET/CT continues to increase as it has repeatedly been shown to improve initial staging and detection of recurrence compared to CT alone [1,2]. The increased glucose metabolism and resultant FDG accumulation [3] allows localization of hypermetabolic cells while the CT portion both aids in the attenuation correction of the PET images and improves localization of positive PET findings [4,5]. However, the separate performance of diagnostic CT and PET/CT has significant drawbacks. Separate appointments for CT scanning require additional time away from school for the patient, work for the guardians, and in many cases repeat sedation. These additional factors take a toll on both the patient and family. Decreasing the number of CT scans and follow-up visits required would help to mitigate these factors and improve overall quality of life of the patients and their families. At ⁎ Corresponding author. 111 E210 Street, Bronx, NY, 10467. Tel.: +1-718-920-5213. E-mail address: btaragin@montefiore.org (B. Taragin). http://dx.doi.org/10.1016/j.clinimag.2015.05.005 0899-7071/© 2015 Elsevier Inc. All rights reserved.
our institution, the billed fee per diagnostic CT scan of the chest [diagnostic chest CT (dCTC)] scan is approximately US$300. Minimizing the number of redundant scans per patient could potentially impact health care costs substantially. The diagnostic scan may also represent an unnecessary health care expenditure. Perhaps more importantly, the additive diagnostic radiation involved in performing a separate PET/CT and diagnostic CT is concerning, especially in the care of the pediatric cancer patient. Long-term studies have shown that low-dose radiation in childhood carries a significantly increased lifetime risk of developing fatal cancer [6–9]. Recent research suggests that children are 10 times more radiosensitive than adults [10], making children more likely to develop a malignancy when compared to adults receiving an equivalent dose of radiation. Additionally, childhood cancer survivors have an increased risk of developing subsequent neoplasms due to both innate factors such as genetics, immune function, and hormone status, as well as secondary factors such as primary cancer therapy, environmental exposures, and lifestyle. The Childhood Cancer Survivor Study reported a 30-year cumulative incidence of 20.5% for all subsequent neoplasms, the risk of which remains elevated for more than 30 years from diagnosis of the primary cancer [9]. The elimination of a possible unnecessary radiation dose without compromising diagnostic efficacy [6] would better conform to the ALARA (“as low as reasonably achievable”) principle. Reducing the total number of CT studies and decreasing the number of scan “phases” are of the most powerful means of radiation reduction. With the rapid improvements of the CT component of PET/CT technology, it remains unclear if the CT performed for attenuation correction can provide additional diagnostic information [11]. While studies in adults have compared the accuracy of the CT portion of PET/CT in
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Total number of scans (119)
Of these, 9 paired scans occurred on the same day. In 47 paired scans, the PET/CT was performed prior to the dCTC, and in 63 paired scans, the dCTC occurred prior to the PET/CT.
60 59
2.2. Imaging Methods
Table 1 Patient demographics Total number of patients (n=46) Male 26 Female 20 Age at first scan (years) 0–5 9 6–11 17 12–17 19 18–21 1 Total 46
24 41 53 1 119
evaluation of malignancies [12,13], the sensitivity of the lower-dose CT as an independent diagnostic tool in pediatric oncology patients compared with dCTC has not, to our knowledge, been assessed. The current study aims to measure the sensitivity and specificity of the CT portion of the PET/CT as compared to the dCTC in our pediatric oncology population at The Children’s Hospital at Montefiore. We hypothesized that the low-dose CT performed at the time of PET can provide similar diagnostic information as the dedicated chest CT. If proven correct, safe omission of the separate chest CT could result in a significant reduction in radiation as well as health care utilization without significant adverse effects in this extraordinary vulnerable population. 2. Methods and Materials 2.1. Patient Population This institutional review board approved, Health Insurance Portability and Accountability Act compliant, retrospective study included pediatric oncology patients at The Children’s Hospital of Montefiore with histologically proven malignant tumors (see Tables 1 and 2). Patients were selected through review of the Medical Center Radiology Information System database that yielded 48 patients between 01-01-2008 and 01-01-2011 who had paired scans (both dCTC and PET/CT within 4 weeks). There were 121 such paired studies in 48 patients. The population consisted of 26 boys and 22 girls age 2–17 years. Scans were obtained either for staging at initial diagnosis or for surveillance of recurrence after achieving a documented complete remission of their disease. Two patients were excluded; one was excluded because ultimately the patient was found not to have an oncologic diagnosis; the other was excluded because the imaging obtained was due to prolonged fever not for staging or surveillance of recurrence. Our study population, therefore, consisted of 46 pediatric oncology patients who had a total 119 paired scans. The patients were evaluated by 18F-FDG imaging using a combined PET/CT system (Phillips Gemini TF TOF/64-detector rows) and a single dCTC (General Electric Imaging Systems, LightSpeed VCT/64-detector rows) within 30 days.
Table 2 Malignancies included in study
Adrenocortical carcinoma Chondrosarcoma Germ cell tumor Hodgkin’s lymphoma Leiomyosarcoma Lymphoproliferative disease Nasopharyngeal carcinoma Neuroendocrine tumor Non-Hodgkin’s lymphoma Osteosarcoma Rhabdomyosarcoma Small round blue cell tumor Other Total
795
Total number of patients (n=46)
Total number of scans (n=119)
1 1 2 11 2 3 2 3 5 1 9 3 2 46
13 1 10 38 2 3 10 3 15 1 19 3 2 119
The hybrid PET/CT system used a combined multi-detector helical CT with a dedicated PET scanner. For PET/CT acquisition, the CT was acquired with a peak kilovoltage (kVp) of 120, 20–30 mAs, and a wide field of view (FOV) and was reconstructed with a slice thickness of 5 mm in lung and soft tissue windows (as per the department protocols at that time). Images were acquired without administration of oral or intravenous contrast and with the patient in free breathing with arms at side. No anesthesia or sedation was administered. PET/CT scanning was started 60 min after 18F-FDG injections. The CT scan was obtained prior to the PET scan. No procedures were performed on the day of the PET/CT prior to the study. The dCTC was performed in helical mode with a dedicated 64-slice CT scanner. The X-ray tube was operated with a kVp of 100 and slice thickness of 0.625 mm, weight-based current/time product (mAs), and standard FOV per patient dimensions. Images were reconstructed with a slice thickness of 2.5 mm in lung and soft tissue windows (as per the department protocols at that time). If chest CT was performed alone, no contrast was administered. If the chest CT was performed in conjunction with an abdomen and pelvis, CT intravenous contrast was administered. Imaging was performed with patients performing breath-holding maneuvers or suspended respiration if intubated and with arms above head. 2.3. Dose Calculations Current CT scanners provide dose information including dose length product (DLP) for each scan obtained. To best estimate the effective dose for each dCTC, we used region-specific conversion coefficients in children of various ages (1, 5, 10, and 15 years) developed by the European Commission Concerted Action on CT [14] and validated in a large survey of adult and pediatric CT doses in the UK [14,15]. They described age-specific coefficient conversion factors for different age ranges. Children from 4 months to 2 years 11 months were assigned the coefficient associated with the 1 age group, those from 3 years to 7 years 11 months were assigned the coefficient associated with the 5 age group, those from 8 years to 14 years 11 months were assigned the coefficient associated with the 10 age group, and those 15 years and older were assigned the coefficient associated with the 15 age group. These coefficients and groupings were obtained from those used by Thomas and Wang [16]. Our scanners reported DLP using a 32-cm phantom. The DLP, when available, was then multiplied by the age appropriate conversion coefficient to obtain the effective dose: effective dose=DLP×conversion coefficient (14). In accordance with the recommendations of Shrimpton et al. [14], in children b15 years of age, DLP was multiplied by a factor of 2 prior to applying the conversion factor: effective dose=DLP×conversion coefficient×2 [14]. 2.4. Image Interpretation All attending finalized reports for paired studies were collected and reviewed by the pediatric radiology fellow (IT), with 5 years of radiology experience. A scoring system and protocol for discrepant results was developed prior to review. The fellow reviewed reports from paired studies and notated all studies with positive findings. He then reviewed images from all positive paired studies and graded them as concurrent or discrepant. Paired studies with discrepant findings were then independently reviewed by a board certified pediatric radiologist (BT), with 13 years of radiology experience, and a board certified thoracic radiologist (JL), with 7 years of radiology experience. Reviewers were blinded to original reports of the discrepant studies. During discrepant
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image review sessions, the CT portion of the PET/CT was reviewed first and independent from the PET to prevent bias. The dCTC was then reviewed. Imaging findings on discrepant studies were reviewed and reclassified as either radiologically significant discrepancies (presence of pulmonary nodules, bony metastasis, adenopathy, and pleural effusions) or non-radiologically significant findings/discrepancies (atelectasis, posttherapy scarring, or stable nodules). Findings from these review sessions were scored on de-identified score sheets. Any persistent disagreement between attending radiologists regarding scoring of findings was resolved by panel review and discussion among all three radiologists until consensus was reached. In cases where there were true discrepancies found between the paired sets, the PET images were also reviewed and the combined findings along with contemporaneous de-identified clinical scenario were presented to an attending pediatric oncologist (RR), with 7 years of postfellowship clinical experience, for determination of clinical significance. 2.5. Data Analysis A positive finding on the unenhanced CT portion of the PET/CT was defined as true positive or false positive if the finding was confirmed or excluded, respectively, by the dCTC. A negative finding on the unenhanced CT portion of the PET/CT was defined as true negative or false negative if the finding was excluded or confirmed, respectively, on the dCTC. Performance indices of the unenhanced CT portion of the PET/CT including sensitivity specificity and positive and negative predictive values were calculated and 95% confidence intervals (95% CIs) for each parameter were calculated using an online calculator adhering to standard statistical methods. 3. Results A total of 119 PET/CT scans in 46 children with an average age at the time of the scan of 11 years (range, 2–18 years) were reviewed (see Fig. 1). Of the paired scan reports, 49 studies were normal on both
dCTC and PET/CT, 41 had concordant positive findings, and 29 were discordant (Table 3). On review of the actual image sets in the 29 discrepant pairs, 2/29 (6.9%) of the discordances had radiologically significant discrepancies, both of which were small subcentimeter nodules; 27/29 (93.1%) were determined upon review not to be of radiologic significance. A total of 13 PET/CT reports were negative, whereas dCTC reports described unchanged nodules. These nodules were all correctly noted by blinded readers in our study on review of PET/CT low-dose CT images. A total of 5 PET/CT reports were read as stable, where dCTC reports described unchanged nodules, and these nodules were all correctly noted by blinded readers in our study on review of PET/CT CT images. A total of 9 PET/CT reports were read as stable, where dCTC reports described atelectasis or posttherapy scarring, and these findings were all correctly noted by blinded readers in our study on review of PET/CT CT images. Of the two discrepant cases referred for determination of clinical significance by a pediatric oncologist, one was classified as clinically significant (Fig. 2) and one was not (Fig. 3). The discrepancy deemed not clinically significant (Fig. 2) was graded such that because this nodular density was seen intermittently on prior studies and was considered an area of itinerant atelectasis because of its intermittent disappearance and shape. The discrepancy deemed significant (Fig. 3) was graded as such because the findings of multiple nodules would require biopsy in blinded clinical review. Of note, in the real-time clinical setting, the dCTC that was performed first showed a cluster of nodules that had resolved on the subsequent PET/CT CT images. Therefore, no biopsy was performed. When comparing the unenhanced CT portion of the PET/CT to the dCTC, there were 68 true positives, 49 true negatives, 2 false negatives, and 0 false positive. The sensitivity and specificities of the unenhanced CT portion of the PET were 97.1% 95% CI (89.1–99.5) and 100% 95% CI (90.4-1), respectively. The positive predictive value of the unenhanced CT portion of the PET was 100% with a 95% CI (93.3-1) and the negative predictive value was 96.0% 95% CI (85.4–99.3).
Fig. 1. Image interpretation process.
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Table 3 Listing of discrepant reports: Highlighted cases remained discordant after image review Scan number
Patient malignancy
PET report
Chest CT report
104 16 42 73 80 88 39 50 9 152 13 61 64 107 123 166 124 11 99 66 75 143 93 160 12 70 140 142 135 87
Lymphoma Lymphoma NC Rhabdo Rhabdo Lymphoma Rhabdo Lymphoma Lymphoma Lymphoma Rhabdo ACC NC Lymphoma Rhabdo Lymphoma Lymphoma Lymphoma Rhabdo Lymphoma NC ACC Rhabdo Lymphoma Lymphoma ACC Lymphoma Lymphoma Rhabdo Lymphoma
Normal Normal Normal Stable Stable Nodule(s) Normal Normal Nodule(s) Normal Normal Normal Stable Stable Stable Stable Nodule(s) Stable Normal Normal Normal Normal Normal Normal Normal Nodule(s) Nodule(s) Nodule(s) Nodule(s) Stable
Volume loss Nodule(s) Nodule(s) Nodule(s) Nodule(s) Stable Nodule(s) Nodule(s) Normal Nodule(s) Nodule(s) Nodule(s) Nodule(s) Nodule(s) Nodule(s) Nodule(s) Stable Nodule(s) Nodule(s) Nodule(s) Nodule(s) Lymphadenopathy Nodule(s) Lymphadenopathy Nodule(s) Normal Nodule(s) Nodule(s) Stable Nodule(s)
ACC, adrenal cortical carcinoma; Rhabdo, rhabdomyosarcoma; NC, nasopharyngeal carcinoma.
Of the 119 scans included in the study, 89 were performed prior to institutional recording of dose information. Of the DLP that was recorded in the 30 remaining scans and was categorized by patient age, the average dose for the dCTC scans was 4.99 mSv (See Table 4). 4. Discussion In a continuing effort to reduce childhood radiation exposure, this study sought to investigate whether the CT portion of PET/CT could serve a primary diagnostic role in a pediatric oncologic population. Our data demonstrate that the unenhanced CT portion may provide independent diagnostic information of different value if reviewed as a standalone diagnostic study, not as just a tool for better PET/CT interpretation. Currently, the CT portion of PET/CT in many centers is a low-dose, unenhanced study and used primarily for image localization and
Fig. 2. CT and PET/CT images of a female aged 2 years 6 months with rhabdomyosarcoma of the bladder. dCTC and PET/CT were performed on the same day. A micro-nodule (arrow) is seen on (A) dCTC in the left lower lobe (study performed during free breathing). The micro-nodule is not visualized on the free breathing CT portion of the PET/CT (B) (same anatomic level based on bronchovascular anatomy of the lung). This finding was considered a significant miss on the low-dose CT performed as part of PET/CT. However, as per the evaluation of the oncology team, this finding necessitated no additional therapy. The opacity was no longer present on subsequent imaging done for routine follow-up.
Fig. 3. CT and PET/CT images of a different female aged 2 years 6 months with nasal rhabdomyosarcoma, and dCTC was performed 5 days prior to the PET/CT. A cluster of nodules (arrow) is seen on (A) dCTC at the level of the liver (study performed during free breathing). The nodules are not visualized on the free breathing CT portion of the PET/CT (B) (same anatomic level based on bronchovascular anatomy of the lung). This finding was considered a significant miss on the low-dose CT performed as part of PET/CT. A repeat dCTC performed 1 week later with prone imaging demonstrated resolution of the finding.
attenuation correction. However, additional diagnostic information can be added through independent readings of the unenhanced CT portion of PET/CT. For example, in a study examining the unenhanced CT portion of 18F-fluoride PET/CT in patients with known malignancies, there were clinically significant findings in 27.2% of patients when the CT portion was read independently. Many of these findings included small pulmonary nodules [17]. Our study further supports this notion that, in pediatric patients with the unenhanced CT portion of PET/CT with a sensitivity of 97.1% and a specificity of 100%, it performs almost as well as dCTC. In our study, many of the discrepant reports were attributable to stylistic reporting differences. This fact is exemplified by the number of true discrepancies (2), found after dedicated review of the images, which was significantly lower than the number of discrepant reports (29). Blinded review of both studies from the falsely discrepant 27 pairs revealed that 13 paired reports were discrepant only in regard to differences in description of unchanged nodules, 5 regarding categorization of stable findings, and 9 report omissions of apparent but not significant findings. Both of our study’s true discrepancies occurred in patients with soft tissue sarcomas. A retrospective study that investigated the effectiveness of FDG-PET/CT in the diagnosis of local recurrence and distant metastases of malignant bone and soft tissue sarcomas in children found that, while FDG-PET/CT was highly sensitive (100%) for detection of local recurrence, it had lower sensitivity (77%) for the detection of distant metastases, such as those in the lungs [18]. Our results suggest re-examination of these findings. While these malignancies can be more aggressive than many of the others included in this study, a separate dCTC may not be warranted in this population if low-dose CT performed with PET performs as equally. Historically at our institution, the CT portion of the PET/CT was reviewed by the nuclear medicine attending physician and radiology residents but not routinely read by a pediatric radiologist specializing in cross-sectional image interpretation. Our results have caused us to review our current imaging protocols allowing for CT review at the time of the performance of PET/CT. If the CT is deemed diagnostic without any findings, we now endeavor, in specific patients with known stable disease and non-aggressive histology, to contact clinicians and discuss canceling possibly redundant imaging. Prior studies had shown that the use of CT intravenous contrast in PET/ CT has been associated with an overestimation of the standardized uptake value after CT-based attenuation correction of PET data [19,20]. Therefore, our institution’s protocol is to perform PET/CT without contrast. Newer publications have dispelled this potential pitfall [21,22]. This potential change in protocol, namely intravenour contrast administration during PET/CT, locally and perhaps nationally if standardized could make the CT of the PET/CT even closer to diagnostic CT accuracy. Administration of contrast may also allow for simultaneous acquisition of abdominal and pelvic CT scans that currently are performed separately. Continuing hardware and software improvements in the PET/CT scanners will allow changes in current technique that would provide
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Table 4 Effective dose for dCTC Age
Number of scans
DLP mean
DLP range
SD
Conversion coefficient
Mean effective dose (mSv)
Range of effective dose (mSv)
SD
1 5 10 15
5 12 11 2
151.84 158.56 310.05 178.20
48.47–233.57 64.44–287.95 155.37–555.98 113.45–242.95
66.35 58.86 139.60 91.57
0.026 0.018 0.013 0.014
3.95 3.37 7.70 2.50
1.26–6.07 2.10–5.82 3.94–14.45 1.59–3.40
1.73 1.22 3.84 1.28
better image resolution. These include optimized FOV, modulating tube current, reconstruction algorithms, and decreased slice thickness all of which likely would result in improved lesion conspicuity even at the dose used for PET/CT scanning. Most of these options are already incorporated into state-of-the-art, low-dose CT scanners but many PET/CT scanners have not yet been updated. Our findings suggest that there may be a concurrent cost saving and radiation reduction effect that should encourage updating older scanners. Additionally, newer PET/CT scanners with faster acquisition time of the CT images will allow pediatric PET/CT to be performed without artifacts from breathing motion, a previously reported limitation in using the CT images from the PET/CT [23]. Current understanding of the harmful effects of diagnostic radiation motivates us to comply as best possible with the ALARA principle. Reducing the total number of CT studies is of the most powerful means of radiation reduction. Indeed, even the lay press [24] has highlighted double scanning of the chest as often inappropriate. We feel that our results and subsequent change in practice should be an impetus for this possible change in current resource utilization and clinical protocols. Our study had multiple limitations including our population and overall scan frequency. Our study comprised 119 paired scans that occurred in only 46 patients. Additionally, the overall incidence of new pulmonary disease in our population was low. Furthermore, some individual patients in our study received a disproportionate number of scans, for example, 1 patient with adrenocortical carcinoma had 13 paired scans during our study timeframe. This caused bias in our results and precludes us from confirming whether our findings were histology specific or patient specific. Lastly, the our study population that included multiple tumor histologies and uneven distribution of patients within the different diagnosis limits our conclusions. Larger studies would be helpful in proving the trends seen in our study. Since, in our study, the chest CT portion of PET/CT has sensitivity and specificity that approaches dCTC, we feel that additional multi-center collaboration is warranted to determine which patient subsets do not need both tests. If implemented at our institution, this protocol would result in a per incidence savings of US$300 and 4.99 mSv. Local interdepartmental collaboration as well as national interdisciplinary dialog between radiologists, oncologists, and nuclear medicine physicians is necessary to optimize future oncologic follow-up imaging protocols and algorithms. In particular, the CT portion of a PET/CT can be used in place of a dCTC when routine follow-up protocols indicate that a PET is necessary. Such collaboration may obviate repeat imaging in select cases. This could improve patient care, decrease overall health care cost, and lower patient’s diagnostic radiation dose.
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