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Nuclear Medicine |
1 From the Departments of Nuclear Medicine (N.G.S., T.F.H., K.D.M.S., G.K.v.S., G.W.G.) and Internal Medicine (C.T.), University Hospital Zurich, Raemistrasse 100, CH-8091 Zurich, Switzerland; and Department of Biostatistics, University of Zurich, Switzerland (B.S.). Received June 23, 2003; revision requested August 29; final revision received February 2, 2004; accepted February 16. Address correspondence to G.W.G. (e-mail: gerhard.goerres@dmr.usz.ch).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Sixty patients (mean age, 39.6 years ± 17.1 [standard deviation]) with Hodgkin disease (n = 42) or high-grade non-Hodgkin lymphoma (n = 18) were included in this retrospective study. All patients underwent PET/CT and contrast-enhanced CT within a maximum of 24 days (mean, 9.1 days ± 7.0) of each other for staging (n = 19) or first follow-up examination (n = 41). Findings were extracted from original written reports (PET/CT, contrast-enhanced CT) and compared with findings of reference standard, which included biopsy or follow-up with clinical, laboratory, or other imaging findings. For statistical analysis, sensitivity and specificity were calculated with findings of the reference standard. Agreement of both methods was determined with Cohen 
and McNemar tests on a per-patient basis.
RESULTS: For evaluation of lymph node involvement, sensitivity of PET/CT and contrast-enhanced CT was 94% and 88%, and specificity was 100% and 86%, respectively. For evaluation of organ involvement, sensitivity of PET/CT and contrast-enhanced CT was 88% and 50%, and specificity was 100% and 90%, respectively. Agreement of both methods was excellent ( = 0.84) for assignment of lymph node involvement but only fair ( = 0.50) for extranodal disease. A difference with P < .05 (McNemar test) was considered significant in regard to exclusion of disease with PET/CT, compared with contrast-enhanced CT.
CONCLUSION: PET/CT performed with nonenhanced CT is more sensitive and specific than is contrast-enhanced CT for evaluation of lymph node and organ involvement, especially regarding exclusion of disease, in patients with Hodgkin disease and high-grade non-Hodgkin lymphoma.
© RSNA, 2004
Index terms: Dual-modality imaging, PET/CT, 99.12919, 99.12963 • Hodgkin disease, CT, 99.12912 • Hodgkin disease, staging • Lymphoma, CT, 99.12912 • Lymphoma, PET, 99.12963 • Lymphoma, staging
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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With the recent introduction of in-line FDG PET with coregistered nonenhanced CT (PET/CT) scanners, a combined method of metabolic and morphologic imaging is available. PET and CT data can be acquired in the same imaging session, without the need to change the patient position between scanning with one modality and the other, to obtain coregistered images. Routinely, nonenhanced low-dose CT is used for attenuation correction, as well as image coregistration (5).
The aim of this study was to retrospectively compare the diagnostic value of coregistered PET/CT scans obtained with low-dose nonenhanced CT with those routinely obtained with contrast-enhanced CT for staging and restaging of disease in patients with Hodgkin disease or high-grade non-Hodgkin lymphoma.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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Patients fasted for at least 4 hours prior to scanning, which started 40–60 minutes after the injection of a standard dose of 370 MBq of FDG. In addition, an oral CT contrast agent (Micropaque Scanner; Guerbet, Aulnay-sous-bois, France) was administered, starting 15 minutes before the injection of FDG (6). Patients were examined in the supine position. No intravenous contrast agent was administered. An oral contrast agent was administered for all CT and PET/CT examinations. Initially, starting at the level of the head, the CT scans were acquired with the following parameters: 80 mA, 140 kV, 0.5-second tube rotation, 4.25-mm section thickness, 867-mm scan length, and 22.5-second data acquisition time. The CT scans were acquired during breath hold with the normal expiration position, and scanning included the area from the head to the pelvic floor.
Immediately following CT, a PET emission scan was acquired, with an acquisition time of 4 minutes for the emission scan per cradle position and a one-section overlap. Acquisition of scans in six cradle positions from the pelvic floor to the head resulted in an acquisition time of approximately 24 minutes. The CT data were used for attenuation correction, and images were reconstructed by using a standard iterative algorithm (ordered subset expectation maximization). The acquired images were viewed with software that provided multiplanar reformatted images of PET, CT, and fused data with linked cursors (eNtegra 3.0215; GE Medical Systems).
Contrast-enhanced CT was performed in different hospitals. All were equipped with helical CT scanners: a single-section unit (Sele; Picker/Elscint, Hamburg, Germany) and two multisection units (Emotion Dual Slice CT, Siemens, Erlangen, Germany; Somatom Volume Zoom, Siemens). The CT scanners were either single- or multisection scanners, and imaging of the neck, thorax, abdomen, and pelvis was performed according to the guidelines of the American College of Radiology, with acquisition of contiguous sections of 5-mm thickness. In all patients, data acquisition included the same anatomic regions from the neck to the pelvic floor as were included in PET/CT scans. All contrast-enhanced CT examinations were performed with an intravenous injection of 120–200 mL of contrast medium. All CT images were displayed as transverse sections.
PET/CT and contrast-enhanced CT data were acquired within a maximum of 24 days (mean, 9.1 days ± 7.0) of each other. The mean clinical follow-up for the confirmation of findings at PET/CT or contrast-enhanced CT that were negative was 9.3 months ± 2.5.
Imaging and Pathologic Finding Analysis
The information about possible or evident pathologic findings described in original written reports of PET/CT and contrast-enhanced CT results was used to perform statistical analysis (N.G.S., B.S.). All pathologic findings as reported with PET/CT were directly compared with findings reported with contrast-enhanced CT for the assignment of the anatomic localization of lymph node involvement and the identification of organ infiltration by two readers (N.G.S., G.W.G.). Only when discrepant findings between PET/CT and contrast-enhanced CT were reported were the images viewed again by two readers in consensus. Both readers were board-certified nuclear medicine physicians and radiologists (T.F.H., G.W.G.) with more than 2 years of experience in interpretation of PET/CT scans and 8 years of experience in interpretation of contrast-enhanced CT scans. This allowed assessment if a lesion was missed with one imaging method.
All pathologic findings described in the original written reports were ranked to assign the probability of lymphoma involvement of a given lesion on PET/CT and contrast-enhanced CT scans, separately, with the following grading scale: 0 (no lymphoma), 1 (possible lymphoma), or 2 (evident lymphoma involvement). In addition, a consensus was reached about whether a lesion corresponded to lymph node or organ involvement due to lymphoma. The findings of PET/CT and contrast-enhanced CT were compared with histologic findings, if available (restaging in seven of 41 patients, staging in 13 of 19 patients). Clinical follow-up was investigated in all 60 patients at a mean of 9.3 months ± 2.5 after imaging (N.G.S.). The standard of reference was preferably biopsy, if available, or follow-up, which included clinical, laboratory, or other imaging (plain radiography, magnetic resonance [MR] imaging, bone scintigraphy) findings.
In regard to change in treatment, retrospective analysis of the patient’s chart was performed to determine whether the treatment was based on PET/CT or contrast-enhanced CT findings. In addition, the treating oncologist (N.G.S.) was contacted to determine whether treatment decisions were based on contrast-enhanced CT or PET/CT findings.
Statistical Analysis
Sensitivity and specificity were calculated on the basis of the true-positive and true-negative findings as described in the same anatomic region (N.G.S. and B.S.). Statistical analysis was performed with software (StatView, version 5.0.1; SAS Institute, Cary, NC). The agreement of PET/CT and contrast-enhanced CT findings was assessed separately for lymph node and organ involvement with the statistic. The agreement was determined, with values as follows: 0–0.20, very poor; 0.21–0.40, poor; 0.41–0.60, fair; 0.61–0.80, good; and 0.81–1.00, excellent.
The following regions were used for the anatomic assignment of lymph node involvement to measure the agreement between the methods: neck, mediastinum, axilla, abdomen, retroperitoneal space, and groin. Organ involvement was assessed for the lung, liver, spleen, gastrointestinal tract, and bone marrow.
To evaluate the difference in probability assignment between the two imaging modalities, we separately analyzed the data in regard to the standard of reference (true-positive and true-negative results according to the standard of reference). We applied the McNemar test separately in these two groups, with a confidence level of 95% (a difference with P < .05 was considered significant). Furthermore, the McNemar test according to sex (male or female patients) and histologic findings (Hodgkin disease or non-Hodgkin lymphoma) was used to determine a significant difference between these subgroups (N.G.S., G.W.G., B.S.). All tests were performed on a per-patient basis, and hence, dependency or clustering did not occur. With the McNemar test, the P value after Bonferroni correction was calculated as .05/6 = .008.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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In a total of 41 patients who underwent imaging with both modalities for restaging, lymph node involvement was found in 11 patients with PET/CT and in 13 patients with contrast-enhanced CT (Table 2). Concordant lymph node involvement was reported in seven patients. In four patients, PET/CT depicted additional nodal involvement. In two of these patients, increased FDG uptake was histologically confirmed as nodal involvement. In a third patient, PET/CT depicted a suspicious lymph node that was not histologically or cytologically confirmed. In the fourth patient, a mesenteric bulk considered as stable disease at contrast-enhanced CT (1-year follow-up after the completion of chemotherapy) revealed increased FDG uptake at PET/CT. Two false-negative lesions were found at PET/CT: First, a paraaortic lymph node shown on contrast-enhanced CT images revealed no FDG uptake and was missed on the nonenhanced CT image at PET/CT. Second, subcarinal lymph node involvement with Hodgkin disease in a 3.8-cm-diameter enlarged lymph node was not depicted on PET/CT images but was identified on contrast-enhanced CT scans and was proved at biopsy. In 24 patients, no nodal involvement was detected with both imaging modalities. In an additional four patients, contrast-enhanced CT depicted lymph nodes suspicious for lymphoma involvement. All patients remained without further evidence of recurrent lymphoma during clinical follow-up, and findings were considered false-positive.
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Organ Involvement
In 15 of 19 patients who underwent PET/CT and contrast-enhanced CT for staging purposes, no organ involvement was reported (Figure). In three patients, extranodal disease was reported at PET/CT (one patient each had bone invasion, spleen infiltration, and a combination of both). Bone involvement was confirmed at bone scintigraphy, MR imaging, and additional radiography. This confirmation led to an upgrading of the stage of the disease. The spleen involvement was confirmed after 10 months at follow-up PET/CT, which showed progression of the disease. In all three patients, the PET/CT findings were considered to be true-positive (Table 3). In one patient, at contrast-enhanced CT for staging, findings indicated additional small-bowel involvement. These findings led to an adaptation of treatment, and thus, findings were considered true-positive at contrast-enhanced CT and correspondingly false-negative at PET/CT. No false-positive findings were reported with PET/CT and contrast-enhanced CT for staging (Table 3).
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In five patients, seven extranodal lesions were depicted with contrast-enhanced CT that were not depicted at PET/CT. In four patients, pathologic lung infiltration was found with contrast-enhanced CT, and in one patient, involvement of the liver, spleen, and bone marrow was described. These lung lesions, usually described as patchy areas of opacity, were considered to correspond to lymphoma. However, at clinical evaluation with follow-up contrast-enhanced CT, findings were normal in all four patients, thus confirming the results with true-negative PET/CT scans. In the patient with liver, spleen, and bone marrow involvement depicted with contrast-enhanced CT, findings at PET/CT were negative and clinical follow-up with contrast-enhanced CT after 4 months revealed no pathologic findings or clinical signs of recurrence. In these five patients with erroneously suspected extranodal lymphoma at contrast-enhanced CT, the treatment did not change, and all contrast-enhanced CT findings were considered false-positive (Table 3).
The sensitivity and specificity for extranodal involvement on a per-patient basis were 88% (seven of eight) and 100% (52 of 52) for PET/CT and 50% (four of eight) and 90% (47 of 52) for contrast-enhanced CT, respectively. The McNemar test for the probability assignment of suspicious lesions revealed no significant difference between both imaging methods, with P = .07 for the exclusion of pathologic organ involvement and P = .37 for the assignment of organ involvement with Hodgkin disease and high-grade non-Hodgkin lymphoma.
On the basis of findings at PET/CT for staging, treatment was changed in three (16%) patients, and on the basis of contrast-enhanced CT findings, it was changed in one (5.2%) patient. For the restaging examinations, PET/CT revealed additional findings that led to a change of treatment in six (15%) patients, and contrast-enhanced CT revealed additional findings that led to an adaptation of treatment in one (2.4%) patient.
Overall, the sensitivity and specificity for lymph node and organ involvement on a per-patient basis were 93% (37 of 40) and 100% (80 of 80) for PET/CT and 80% (32 of 40) and 89% (71 of 80) for contrast-enhanced CT, respectively. The McNemar test for the comparison of the probability assignment of suspicious lesions between PET/CT and contrast-enhanced CT indicated a significant difference for the exclusion of pathologic organ or lymph node involvement (P = .004) and no significant difference for the assignment of pathologic involvement (P = .11).
There were no significant differences in regard to assignment between the imaging modalities according to sex (male patients, P = .58; female patients, P = 1.0) or histologic findings (Hodgkin disease, P = .42; non-Hodgkin lymphoma, P = .68).
The value as a measure for agreement between PET/CT and contrast-enhanced CT revealed that the agreement between the methods was excellent for lymph node staging and restaging examinations. However, only a poor to fair agreement was found for evaluation of extranodal disease (Table 4).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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Currently, contrast-enhanced CT is the first-line imaging modality in Hodgkin disease and non-Hodgkin lymphoma, which allows the detection of morphologic abnormalities such as lymph node enlargement or changes in contrast enhancement that suggest organ manifestation. However, disease in normal-sized lymph nodes and in spleen and bone marrow is less well depicted (7). In several studies, the role of FDG PET for pretreatment as well as posttreatment evaluation of Hodgkin disease and non-Hodgkin lymphoma has been evaluated (1–4,8–12). PET imaging with FDG showed no difference in depiction of nodal and extranodal disease compared with conventional morphologic staging methods (3,10). In addition, reliable assessment of bone marrow disease was achieved. On the basis of these findings, we have translated these procedures into clinical routine procedures, with FDG PET imaging as an adjunct to morphologic imaging with contrast-enhanced CT in staging and restaging of lymphoma. Correspondingly, a combination of both methods as a single-step examination would simplify diagnostic imaging in patients with lymphoma.
In our study, the statistic revealed excellent agreement between PET/CT and contrast-enhanced CT for the delineation of lymph node involvement, independent of the purpose of the examination for staging or restaging. Basically, pathologic uptake in lymph nodes of any size was regarded as lymph node involvement in PET/CT images. With coregistration of PET and CT images, correct localization of uptake is easily achievable even though only a low-dose nonenhanced CT scan was used for coregistration. These findings confirm previous results from CT studies, which did not reveal any significant difference in the detection of mediastinal lymph nodes with nonenhanced and enhanced CT (13–15).
Several false-positive contrast-enhanced CT findings were reported in regard to lymph node involvement at restaging examinations. Particularly, the remaining soft-tissue densities on contrast-enhanced CT images that were regarded as persistent disease reflect the delayed morphologic response to successful therapy, and follow-up CT scans in these patients revealed normal results after a time. In these cases, PET/CT findings confirmed the absence of active tumor tissue with delineation of soft-tissue masses and without evidence of FDG uptake corresponding to scar tissue. At PET/CT, no false-positive results in regard to lymph node involvement were described. This is in contrast to findings in previous reports with descriptions of a rather high rate of false-positive findings at PET, since inflammatory lesions may demonstrate increased FDG uptake (16). However, the use of coregistered structural information increases the specificity of lesion characterization (17).
In contrast, only a fair agreement was found for the assessment of organ involvement. The main cause for this disagreement could be found in the rather large number of false-positive findings at contrast-enhanced CT, when lung opacities were interpreted as lymphoma. In four patients, pulmonary involvement was reported with contrast-enhanced CT but was considered a false-positive finding, since spontaneous resolution of these opacities without therapy was seen at follow-up examinations. Fundamentally important for staging is the detection of bone marrow involvement, which was described in three patients. In two patients, this involvement was seen exclusively on PET/CT images and was confirmed with additional imaging. In contrast, at contrast-enhanced CT, bone infiltration was incorrectly reported in one patient. This confirms the limitations of contrast-enhanced CT to identify limited skeletal involvement (7).
On a per-patient basis, overall performance of both imaging modalities was not different in the assignment of disease. PET/CT seems to perform better in exclusion of disease, which represents a higher diagnostic confidence to exclude initial disease or recurrence.
A limitation of PET is that small lesions can be missed. In one patient, the thickening of a small-bowel loop indicated lymphoma involvement on contrast-enhanced CT images. This lesion was not visible on FDG PET images. Correct interpretation of abdominal FDG uptake can be difficult, because FDG uptake can be physiologically increased in small and large bowel (18).
PET/CT had a greater effect on therapeutic decision making in our patients with Hodgkin disease and high-grade non-Hodgkin lymphoma than did conventional contrast-enhanced CT. In nine patients, PET/CT revealed relevant additional lesions in lymph nodes and organs at staging and restaging examinations. In contrast, only in two patients did contrast-enhanced CT reveal additional lesions, and this revelation led to a change of clinical management. In one of these two patients, a mediastinal mass was identified on a contrast-enhanced CT scan but was not reported with PET/CT, although retrospectively this mass was clearly identified on the nonenhanced CT image at PET/CT. This case illustrates the importance of careful interpretation of the nonenhanced CT scan independent from information of the PET scan.
An essential advantage of PET/CT imaging over PET imaging alone is the ability to use CT data for attenuation correction of emission data in the reconstruction of PET images. This allows reduction of total data acquisition time to less than 25 minutes per patient (19). If necessary, after completion of scanning, contrast-enhanced CT can be performed in any desired location and can be used for image fusion. However, our data suggest that PET/CT performed with low-dose CT and without intravenous contrast media is sufficient in staging and restaging of disease in patients with Hodgkin disease and high-grade non-Hodgkin lymphoma.
This study had several shortcomings. Mainly, the retrospective nature of this study may have introduced a bias in the data. The patient population was heterogeneous and rather small. Furthermore, the technique of contrast-enhanced CT was not standardized, since data acquisition was performed at different institutions. In addition, the time sequence of PET/CT and contrast-enhanced CT data acquisition was not randomized, and nonstandardized written reports as the basis of analysis could have reduced the clinical importance of our results. Our standard of reference included clinical patient follow-up information obtained at biopsy, from clinical and/or laboratory reports, and at imaging with other techniques. Only a few patients had histologic verification of the specific suspected pathologic findings. This is a known limitation from previous studies in which the performance of imaging methods was compared in lymphoma patients. However, the aim of this study was to determine whether the two selected imaging modalities were able to depict viable tumor tissue and to give correct information for staging and restaging, thus representing the setting in clinical routine.
Overall, the sensitivity and specificity for lymph node and organ infiltration of non-Hodgkin lymphoma and Hodgkin disease analyzed on a per-patient basis were better for PET/CT compared with contrast-enhanced CT. The agreement of both methods was excellent in regard to the status of disease of lymph nodes ( = 0.84) but only fair for extranodal disease ( = 0.50). A significant difference was found in regard to exclusion of disease with PET/CT compared with contrast-enhanced CT. Because of identified shortcomings, future prospective studies are needed for evaluation of the role of PET/CT in the diagnostic work-up and treatment of patients with Hodgkin disease and high-grade non-Hodgkin lymphoma.
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FOOTNOTES |
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Authors stated no financial relationship to disclose.
Abbreviation: FDG = fluorodeoxyglucose
Author contributions: Guarantors of integrity of entire study, N.G.S., G.W.G.; study concepts, N.G.S., T.F.H., C.T., G.W.G.; study design, N.G.S., G.W.G.; literature research, N.G.S., G.W.G.; clinical studies, T.F.H., K.D.M.S., G.W.G.; data acquisition, N.G.S., C.T.; data analysis/interpretation, N.G.S., T.F.H., G.W.G.; statistical analysis, N.G.S., G.W.G., B.S.; manuscript preparation, N.G.S., T.F.H., G.K.v.S., G.W.G.; manuscript definition of intellectual content and revision/review, all authors; manuscript editing, N.G.S., T.F.H., G.W.G.; manuscript final version approval, T.F.H., G.W.G., N.G.S., B.S.
N.G.S. and T.F.H. contributed equally to this work.
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTS DISCUSSIONREFERENCES |
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