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Nuclear Medicine |
1 From the Division of Nuclear Medicine (M.T., C.C., Y.N., R.L.W.) and Department of Radiology (E.K.F., R.L.W.), Johns Hopkins Medical Institutions, 601 N Caroline St, Rm 3223A, Baltimore, MD 21287-0817. Received March 25, 2004; revision requested May 27; revision received November 25; accepted January 2, 2005. Address correspondence to R.L.W. (e-mail: rwahl{at}jhmi.edu).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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MATERIALS AND METHODS: The institutional review board allowed an exempt retrospective review of cancer PET database, and informed consent was waived. The study was HIPAA compliant. Fifty-three patients with lymphoma (20 Hodgkin and 33 non-Hodgkin; mean age, 43 years; range, 12–83 years) who underwent FDG PET/CT were included. The PET and CT images were interpreted by two nuclear medicine physicians and one radiologist, respectively, blinded to the other imaging findings. Concordant PET and CT findings were regarded as positive or negative for lymphoma. The site with discordant findings was defined as positive for disease if it was accompanied by other PET- and CT-positive sites in the same patient or was confirmed clinically (histologic examination or progressive disease). Staging results were also compared by one nuclear medicine physician.
RESULTS: Of a total of 1537 anatomic sites in 53 patients, 48 had discordant findings between PET and CT. Forty (83%) of the 48 sites had correct PET findings (31 positive, nine negative), five had correct CT findings, and three were unresolved. The 31 PET-positive and CT-negative sites accounted for 23% of all 134 true-positive PET sites. PET provided accurate staging in an incremental nine (17%, upstaging in four and downstaging in five) of 53 patients in whom CT staging was incorrect. CT provided correct upstaging in two patients.
CONCLUSION: FDG PET/CT as a combined modality may contribute substantially to lesion characterization and staging in patients with lymphoma.
© RSNA, 2005
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Positron emission tomography (PET) with the glucose analog fluorine 18 fluorodeoxyglucose (FDG) is increasingly recognized as a powerful evaluation method in the field of oncology (4–7). FDG PET enables detection of the increased glucose metabolic rate that is characteristic of most malignant cells. FDG PET has been demonstrated to be useful for the initial diagnosis and staging, for the detection of recurrence, and for the evaluation of chemotherapeutic or radiation therapeutic responses of various kinds of tumors, including lymphoma (4–7). Although not 100% accurate, FDG PET generally offers more than 85% of sensitivity and specificity in the diagnosis of malignant tumors (4–7). FDG PET now often replaces 67Ga scanning in the evaluation of lymphoma (8,9). However, FDG PET may not precisely anatomically localize lesions in the human body, since PET is a metabolic and functional imaging method that provides only limited anatomic information.
Recently, combined PET and CT scanners have emerged as a promising imaging modality and are being more routinely applied in clinical situations (10,11). The CT portion of PET/CT provides anatomic mapping images and attenuation correction data for PET, as well as traditional diagnostic information. Thus, PET/CT offers PET, CT, and high-quality fused images of both function and anatomy at the same location in the body. PET/CT allows the demonstration of pathologic FDG uptake in small lymph nodes and structures that are negative on the basis of CT size criteria. PET findings also can be truly negative for FDG uptake in inactive scar tissues that remain after treatment.
The purpose of the present study was to retrospectively compare FDG PET and CT findings at the same anatomic locations in patients with lymphoma by using a combined PET/CT scanner and to analyze the lesions on both metabolic and anatomic bases to evaluate the frequency and causes of discrepant findings between the two modalities.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Patients
Our review included imaging and clinical data from 53 patients with biopsy-proved lymphoma. The patients had been evaluated for clinical purposes with FDG PET/CT from August 2001 to April 2002 at our PET center. The initial PET/CT examination for each patient during this period was included in this study. Clinical follow-up results, including those from physical examination, blood tests, and CT or magnetic resonance (MR) imaging studies, were collected during the period of more than 1 year from each PET/CT examination. Twelve patients were examined for initial tumor staging, and 41 patients were evaluated for restaging after receiving some treatment. There were 34 male (mean age, 46 years; range, 12–83 years) and 19 female (mean age, 39 years; range, 14–72 years) patients (mean age, 43 years; age range, 12–83 years), and there were no differences in age between the male and the female patients (unpaired t test). Twenty patients had Hodgkin disease, and 33 patients had non-Hodgkin lymphoma. For the initial staging, 12 patients had undergone PET/CT examinations within 6 weeks after histopathologic confirmation (nine patients within 4 weeks), without intervening treatment. For restaging, 20 of 41 patients had undergone PET/CT examinations within 6 weeks of histopathologic confirmation (six before and 14 after the confirmation), but the interval between the examination and confirmation for the remaining 21 patients was longer. However, in this study period, 41 restaging patients were known to have lymphoma only (no other known malignancies were present). None of the 41 patients had inflammatory or infectious disease of unknown origin. Patient characteristics and information regarding treatment are listed in Table 1.
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FDG PET/CT
Whole-body FDG PET/CT was performed with a combined PET/CT scanner (Discovery LS; GE Medical Systems, Waukesha, Wis). This scanner allows the simultaneous acquisition of 35 transverse images, with an intersection spacing of 4.25 mm in one bed position for the PET images. Typically, six or more bed positions are obtained. Transverse PET resolution is approximately 4.5-mm full width at half maximum with use of the highest resolution filter. The field of view and pixel size of the reconstructed images are 50 cm and 3.91 mm, respectively. This scanner also allows multi–detector row helical CT scanning. The technical parameters used for the CT portion of PET/CT were as follows: a detector row configuration of four sections of 5-mm thickness, pitch of 6:1 (high-speed mode), gantry rotation speed of 0.8 second, table speed of 30 mm per gantry rotation, 140 kVp, and 80 mA.
After at least 4 hours of fasting, adult patients received an intravenous injection of approximately 555 MBq (15 mCi) of FDG. About 60 minutes later, CT images were acquired from the meatus of the ear to the middle of the thigh for 37 seconds without contrast material. Twenty-five patients received approximately 900 mL of oral contrast material (1.3% weight/volume barium sulfate suspension, Readi-Cat; E-Z-Em, Westbury, NY), which we started using in December 2001, in the hour before PET imaging was begun (12). A whole-body emission PET scan for the same transverse coverage was obtained with 5-minute acquisition per bed position with the scanner operating in the two-dimensional mode. Attenuation-corrected PET images with use of data from CT were reconstructed with an ordered-subset expectation maximization iterative reconstruction algorithm. The 5-mm-thick transverse CT images were reconstructed at 4.25-mm intervals to fuse with the PET images. PET, CT, and fused PET/CT images were generated for review on a computer workstation (Entegra; GE Medical Systems).
Image Analysis
FDG PET images were retrospectively interpreted by either one of two nuclear medicine physicians (M.T. and C.C., with 6 and 4 years of FDG PET experience, respectively), who were unaware of CT results; the images were then interpreted by the other nuclear medicine physician, who was also blinded to the CT results. The final diagnosis at FDG PET was made in consensus between the two observers (findings of 10 PET examinations had shown different results between the observers before consensus). Any obvious foci of FDG uptake that were increased relative to the background and not located in the areas of physiologically increased uptake were considered positive findings. Foci of FDG uptake suspicious for inflammation or infection were identified according to their shape and intensity, especially in the thoracic region. The PET findings suspected to be inflammation or infection were linear or bandlike FDG uptake extending to the periphery of the lung or mild FDG uptake in the hilum of the lung without other suspicious foci of uptake in the same patient. Equivocal FDG uptake was regarded as negative in this study. Nodular FDG uptake suspected to be physiologic uptake from the tracer distribution pattern was also recorded.
The location of positive FDG uptake was classified into the following 29 anatomic sites: 14 supradiaphragmatic regions (four cervical [right or left, upper or lower], two clavicular [right or left], two axillary [right or left], three mediastinal [anterior, upper, or lower], two hilar [right or left], and other thoracic), 10 infradiaphragmatic regions (two paraaortic [right or left], four abdominal [eg, mesenteric, right or left, upper or lower], two iliac [right or left], and two inguinal [right or left]), and five extranodal regions (spleen, bone or marrow, lung, liver, or other extranodal sites). If multiple positive findings were found at one anatomic site, the representative single largest focus of FDG uptake at the site was selected and further evaluated.
The CT images were first interpreted by one radiologist (E.K.F., 24 years of CT experience) who was blinded to the FDG PET findings. One nuclear medicine physician (M.T.) then classified the abnormal lesions into the 29 anatomic sites described earlier by reviewing the CT interpretation and the actual CT images. This procedure was performed at least 1 month after PET interpretation. Lymph nodes greater than 10 mm in the short-axis diameter were considered positive at CT. Extranodal abnormalities were evaluated according to the standard CT reading criteria as follows: area of abnormal attenuation in the spleen, bone or marrow, and liver; nodule or infiltration in the lung; and mass of soft-tissue attenuation in other extranodal sites. Equivocal findings were classified as negative. The PET and CT findings were then compared by using the one representative largest focus of FDG uptake at each anatomic site. With regard to the sites with positive findings at PET but negative findings at CT, the nuclear medicine physician recorded if the negative CT finding potentially resulted from the small size of the lesion. The sizes of visualized soft tissues or abnormalities at CT (excluding nonmalignant lesions) with positive FDG uptake were measured (M.T.) and used in the semiquantitative PET analysis.
We classified PET and CT findings at each anatomic site into the following four groups: group 1, positive at PET and CT (hereafter, PET and CT positive); group 2, positive at PET and negative at CT (hereafter, PET positive and CT negative); group 3, negative at PET and positive at CT (hereafter, PET negative and CT positive); and group 4, negative at PET and CT (hereafter, PET and CT negative). According to the article by Moog et al (13), we regarded the PET- and CT-positive site as positive for the presence of lymphoma in lymphoma patients unless the site was proved to be false-positive owing to inflammation during the follow-up period of more than 1 year. We also recorded whether the PET- and CT-positive site was accompanied by other PET- and CT-positive sites in the same patient or if the PET- and CT-positive site was confirmed histopathologically in case the site was the sole abnormality in the patient. With regard to the PET-positive and CT-negative or PET-negative and CT-positive sites in lymphoma patients, a site was defined as positive for the presence of lymphoma if the site met one of the following criteria: was accompanied by other PET- and CT-positive sites in the same patient, was confirmed histopathologically, or showed progressive disease without intervening treatment in the follow-up period. Findings of corresponding diagnostic contrast material–enhanced CT examinations without intervening treatment, if any, were also collected and recorded, although the contrast-enhanced studies were performed as separate examinations. PET- and CT-negative sites were considered negative for lymphoma unless false-negative findings were suspected in the follow-up period of more than 1 year.
The Ann Arbor staging system was used (M.T., with 6 years of staging experience), which is commonly used in patients with Hodgkin disease and in those with non-Hodgkin lymphoma (14,15).
Statistical Analysis
Evaluation of the lesions was made on the basis of the anatomic site mentioned earlier. Patient-based analysis was also performed as to whether the patient had sites that had discordant findings and different staging results between PET and CT.
The difference in age between the male and female patients was analyzed with an unpaired t test. A P value of less than .05 was considered to indicate a significant difference.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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The remaining 48 sites exhibited discordant findings: 34 sites as PET positive and CT negative and 14 sites as PET negative and CT positive. The details of the sites with the discordant findings are shown in Table 2. Among the 34 PET-positive and CT-negative sites, 24 had negative CT findings because of the size criterion (>10 mm in short axis was considered positive), and all were considered to be positive for lymphoma according to the definition of positive disease in this study (Figs 1–3). Ten of the 34 sites were not depicted at CT, seven of which were considered positive for lymphoma. Although the remaining three of 10 PET-positive and CT-negative (nonvisualized) sites in two patients were given treatment after PET/CT examinations in clinical situations, they were considered undetermined in terms of the presence of lymphoma according to the definition of positive disease in this study. Twenty-five (74%) of the 34 PET-positive and CT-negative sites were located in the supradiaphragmatic region, and six (18%) and three (9%) were located in the infradiaphragmatic and extranodal regions, respectively. Twenty-three of the 34 PET-positive and CT-negative sites underwent corresponding contrast-enhanced CT examinations, and all had negative findings.
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Patient-based Analysis
There was complete agreement between PET and CT regarding anatomic sites that had positive findings in 32 (60%) of 53 patients (15 as positive and 17 as negative). In these patients, staging results were also the same between PET and CT: five patients had stage 1, four had stage 2, two had stage 3, four had stage 4, and 17 had no active disease.
In the remaining 21 patients (40% of 53 patients), there was disagreement between PET and CT with regard to the sites with positive findings (Table 2). Fourteen and seven patients had more positive sites at PET and CT, respectively. The 14 patients with more positive sites at PET consisted of five patients at initial staging and nine patients at restaging. The seven patients with more positive sites at CT were patients who underwent PET/CT for restaging. The PET-positive and CT-negative finding provided correct upstaging in four of the 14 patients having more positive sites at PET. No change of staging was observed in eight of the 14 patients. Two of the 14 patients had inconclusive staging results because of unresolved PET-positive and CT-negative findings, although they were treated on the basis of PET staging results. In the seven patients with more positive sites at CT, the PET-negative and CT-positive finding provided correct upstaging results in two patients and incorrect overstaging results in five patients (Table 3).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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A main finding in our study was that PET provided accurate results in 40 (83%) of the 48 sites with discordant findings between PET and CT, and that the 40 sites included 31 sites (78%) with PET-positive and CT-negative findings. The 31 sites accounted for 23% of all 134 PET-positive sites, which were considered to be lymphoma lesions according to the definition of positive disease in this study. It is not uncommon that small lesions can represent malignancy. Although we clearly could not compare all PET findings with histopathologic results, false-positive results due to inflammation would be rare according to the published data, with histopathologic verification in various sizes of lymphoma lesions (13,17–19). In this study, we regarded each PET-positive and CT-negative site as a true-positive PET finding only when the site met one of the following criteria, which we believe is generally accepted in clinical situations: (a) the site was accompanied by multiple PET and CT–positive sites in the same patient, (b) the site itself was confirmed histopathologically, or (c) the site exhibited progressive disease in the follow-up period without intervening treatment.
For lung cancer, Gupta et al (20) demonstrated that FDG PET was 80% sensitive and 95% specific in detecting lymph node metastases of less than 10 mm in size. Their data support our observation in this study. It has been recognized for many years that CT evaluation is not sensitive for foci of tumor that are less than 10 mm in diameter, but no alternative methods for the size criteria have been consistently adopted to date. Since PET/CT provides both metabolic and morphologic information for each lesion, new criteria for diagnosing small foci of malignancy may be proposed with this modality. However, careful comparison of PET findings and histopathologic results and/or follow up is obviously needed to firmly establish such criteria.
In 21 (40%) of 53 patients, disagreement at the sites with positive findings was observed between PET and CT. This disagreement affected staging results in 11 patients. PET allowed upstaging in four patients by depicting small or nonvisualized lesions that were negative at CT, and it allowed downstaging in five patients by exhibiting no abnormal FDG uptake in the posttreatment scar tissues, which were suspected to be positive at CT. CT, on the other hand, allowed accurate staging in two patients, who had no PET findings in the posttreatment soft tissues. These results clearly reflect the characteristics of both imaging modalities.
Although PET is useful in staging or restaging of lymphoma, in some instances it fails to depict small tumor foci because of its limited spatial resolution. FDG PET also has potential disadvantages in depicting positive lesions in the brain or urinary tract and/or nearby regions and in differentiating inflammatory lesions that are not accompanied by characteristic shape or clinical symptoms. In these situations, CT is expected to provide additional information to PET for the proper treatment of patients. At this point, PET/CT allows routine acquisition of both PET and CT images without difficulty at the same location in the body. This is important in terms of comparison of both types of images. PET/CT may also reduce the time for imaging examinations, since it is a single examination and is faster than separate PET and CT examinations. Repeat examinations could be conducted more easily with PET/CT in lymphoma, which requires whole-body evaluation after treatment or during the follow-up period.
In this study, a PET-negative and CT-positive finding was observed in relatively large lesions in seven patients who had history of treatment. Five of the seven patients were considered to have nonviable scar tissue according to clinical information, including follow-up imaging results. PET exhibited accurate findings in most such settings. Although a negative PET finding after treatment does not necessarily mean the absence of viable malignant cells, as shown in the two patients in this study, patients with such findings have been shown to have a better prognosis than patients with positive FDG uptake (3,21,22). Separate PET and CT images may be sufficient for assessing these large abnormalities. However, in cases of CT abnormalities with modest FDG uptake, which are frequently observed in posttreatment situations, PET/CT would be more useful for follow-up than separate PET and CT examinations. Precise localization of FDG uptake is desired for these purposes. Wahl et al (23) reported that glucose metabolic changes preceded morphologic changes during effective chemotherapy in breast cancer patients. The careful comparison of both PET and CT findings during treatment could be of interest for better understanding of the disease status in patients with lymphoma.
Findings of this study also suggest the potential advantages of PET/CT images over PET and CT images obtained on separate occasions. PET/CT allowed localization of nodelike FDG uptake in brown fat tissues on CT images in six patients. This finding has also recently been reported by Hany et al (24) and others (25). Before PET/CT was widely available, the foci of FDG uptake might have been misinterpreted as positive for tumor. Definite localization of FDG uptake to fat was possible with use of CT images obtained at the same location as PET and fused PET/CT images. PET and CT images acquired separately may provide enough information for this assessment, but fusion of the images at the same location would require a special technique and more time. Similarly, the small positive lymph nodes may have been given a less confident diagnosis if PET and CT images were acquired with separate scanners. In many instances in this study, PET/CT clearly demonstrated FDG uptake in small lymph nodes of less than 1 cm in size. With regard to PET/CT and PET alone, the former has been shown to be better for lesion detection and diagnostic confidence than the latter in studies dealing with many cancer patients (26,27). We believe that combined PET/CT would also be better in lesion detection and diagnostic confidence, especially in small lesions, than separate PET and CT, based on the results of this study. Further study is required to conclusively prove this point, and these studies are ongoing.
There were limitations to our study. First, we did not compare PET and CT findings with histopathologic results in many lesions. Thus, we defined the status of "positive for malignancy" based on the concept that is generally accepted in clinical situations to treat lymphoma patients. PET- and CT-positive sites were regarded as positive unless a false-positive finding was suspected during the follow-up of more than 1 year. All PET- and CT-positive sites in this study were accompanied either by other PET- and CT-positive sites in the same patient or by histopathologic confirmation. In the sites with discordant findings between PET and CT, positive lesions were required to meet at least one of the following criteria: (a) be accompanied by other PET- and CT-positive sites in the same patient, (b) be confirmed histopathologically, and (c) show progressive disease without intervening treatment in the follow-up period. This lack of histopathologic correlation is a common problem in lymphoma imaging studies in general and is frequently seen in clinical situations, especially in a posttreatment state, since lymphoma is a systemic malignant disease and we cannot evaluate all of the lesions histopathologically.
Second, intravenous contrast material was not used for the CT images of this study. Although intravenous contrast material has recently been reported to be applicable in the CT portion of PET/CT (12), this study, as an initial evaluation of PET/CT in lymphoma, included patients examined from August 2001 to April 2002, when the effect of intravenous contrast material on attenuation-corrected PET data was not clarified. However, in all patients who underwent corresponding contrast-enhanced CT without intervening treatment in this study, contrast-enhanced CT also showed negative findings in the PET-positive and CT-negative sites. We used oral contrast material in about half of the patients. The issue should be resolved soon whether PET/CT requires both intravenous and oral contrast material even after dedicated contrast-enhanced CT is performed.
Third, the current used in the CT portion of PET/CT was considerably lower than that used in dedicated CT examinations in adults. The low current recommended by the manufacturer was used to reduce radiation exposure to the whole body but may degrade the image quality of CT, especially in large patients. However, as far as we experienced, no PET-positive and CT-negative sites turned out to be CT-positive even at dedicated contrast-enhanced CT.
In conclusion, this study demonstrated that PET provided findings considered to be accurate according to our study criteria in 40 (83%) of the 48 sites with discordant findings between PET and CT, and that the 40 sites included 31 (78%) sites with PET-positive and CT-negative findings, which accounted for 23% of all 134 true-positive PET sites. FDG PET resulted in an accurate staging (based on our study criteria) in an incremental 17% (nine of 53) of patients in whom CT staging was incorrect. FDG PET/CT may contribute substantially to accurate lesion characterization and staging in patients with lymphoma by clearly depicting small pathologic lymph nodes or by accurately excluding residual disease activity in posttreatment scar tissues.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Abbreviations: FDG = fluorine 18 fluorodeoxyglucose
R.L.W. has received honoraria from GE Healthcare and has a research contract with GE, has received honoraria from CTMI (Siemens), Cardinal Health, and Philips.
Author contributions: Guarantor of integrity of entire study, R.L.W.; study concepts, M.T., R.L.W.; study design, M.T., Y.N., R.L.W.; literature research, M.T., Y.N.; clinical studies, C.C., E.K.F., R.L.W.; data acquisition, C.C., E.K.F., R.L.W.; data analysis/interpretation, M.T., C.C., Y.N.; statistical analysis, M.T., Y.N.; manuscript preparation, M.T., R.L.W.; manuscript definition of intellectual content, C.C., Y.N., E.K.F., R.L.W.; manuscript editing, R.L.W.; manuscript revision/review and final version approval, all authors
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References |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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This article has been cited by other articles:
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  M. Tatsumi, J. H. Miller, and R. L. Wahl 18F-FDG PET/CT in Evaluating Non-CNS Pediatric Malignancies J. Nucl. Med., December 1, 2007; 48(12): 1923 - 1931. [Abstract] [Full Text] [PDF]
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 P. Seam, M. E. Juweid, and B. D. Cheson The role of FDG-PET scans in patients with lymphoma Blood, November 15, 2007; 110(10): 3507 - 3516. [Abstract] [Full Text] [PDF]
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