I n t e g r a t i ve I m a g i n g R ev i ew

Dibble et al. PET/CT of Pancreatic Neoplasms Integrative Imaging Review

CME SAM

PET/CT of Cancer Patients

FOCUS ON:

PET/CT of Cancer Patients: Part 1, Pancreatic Neoplasms

OBJECTIVE. Pancreatic cancer continues to have a poor prognosis despite impressive improvements in the outcomes of many other types of cancer, often because most pancreatic neoplasms are found to be unresectable at diagnosis. The purpose of this review is to provide an overview of pancreatic cancer and the role of modern imaging in its diagnosis and management with an emphasis on 18F-FDG PET/CT fusion imaging. CONCLUSION. Multimodality imaging is critical in the diagnosis and management of pancreatic cancer. PET/CT is increasingly viewed as a useful, accurate, and cost-effective modality in diagnosing and managing pancreatic cancer, but further studies are warranted. Early data suggest that contrast-enhanced PET/CT performed with modern PET/CT scanners yields high-resolution anatomic information for surgical and radiotherapeutic planning and functional information for whole-body staging in the care of patients with this disease.

Elizabeth H. Dibble1 Dimitrios Karantanis 2 Gustavo Mercier 1 Patrick J. Peller 3 Lisa A. Kachnic 4 Rathan M. Subramaniam1,4,5
Dibble EH, Karantanis D, Mercier G, Peller PJ, Kachnic LA, Subramaniam RM

Keywords: CT, MRI, pancreatic cancer, PET/CT DOI:10.2214/AJR.11.8182 Received November 3, 2011; accepted after revision April 5, 2012. R. M. Subramaniam was supported by a GE-AUR research fellowship, a Siemens molecular imaging research grant, and a Michael Fox Foundation research grant.
1 Department of Radiology, Boston University School of Medicine, Boston, MA. 2 Department of Molecular and Medical Pharmacology, Ahmanson Biological Imaging Division, David Geffen School of Medicine at UCLA, Los Angeles, CA. 3 4

Department of Radiology, Mayo Clinic, Rochester, MN.

Department of Radiation Oncology, Boston University School of Medicine, Boston, MA.

5

Present address: Division of Nuclear Medicine, Russell H. Morgan Department of Radiology and Radiologic Science, Johns Hopkins Medical Institutions, 601 N Caroline St, JHOC 3235, Baltimore, MD 21287. Address correspondence to R. M. Subramaniam (rsubram4@jhmi.edu).

CME/SAM This article is available for CME/SAM credit. AJR 2012; 199:952967 0361803X/12/1995952 American Roentgen Ray Society

ancreatic cancer is the 10th most common cancer in the United States but the fourth leading cause of cancer death [1]. Despite advances in the detection and treatment of other solid malignant tumors, pancreatic cancer continues to have a dismal prognosisa 5-year survival rate of 6%because the tumors are difficult to detect and are often diagnosed late in their course. The only cure is resection, but only 20% of patients present with potentially resectable lesions [2]. Even among patients with localized, resectable disease, the survival rate is only 23% [1]. Thus early detection and appropriate selection of surgical candidates are critical to the management of pancreatic cancer. In addition to aiding selection of surgical candidates, pancreatic cancer imaging helps with characterization of incidentally found lesions, initial staging, surgical and radiotherapeutic planning, assessment of treatment response, and monitoring for disease recurrence. However, the selection of an imaging modality for diagnosing and monitoring pancreatic cancers, particularly adenocarcinoma, is not uniform. CT, transabdominal ultrasound, endoscopic ultrasound [3], ERCP, MRI, MRCP, PET, and PET/CT [4] are all used in the imaging of these cancers. PET/CT is valuable in the diagnosis, staging, therapeutic assessment,

and follow-up of many solid tumors in humans [513]. This review is an overview of pancreatic neoplasms and of the role of modern imaging in the diagnosis and management of pancreatic cancer with a focus on PET/CT. Pancreatic Neoplasm Overview Classification The major pancreatic neoplasms and their key features are summarized in Table 1. Most pancreatic neoplasms are exocrine, 85% being invasive ductal adenocarcinoma [14]. Pancreatic neuroendocrine tumors, formerly called islet cell tumors, constitute 34% of pancreatic neoplasms [14] and are typically benign. Fewer than 2% of malignant pancreatic neoplasms originate from endocrine cells [15]. The other neoplasms are exocrine acinar cell neoplasms, pancreatic cystic neoplasms, and neoplasms of epithelial origin and of mixed differentiation. Presentation Pancreatic cancer is often asymptomatic in the early stages. Patients may present with obstructive jaundice, weight loss, abdominal or midback pain, or a combination of these symptoms [16]. Glucose intolerance also can be a sign of pancreatic cancer [17]. Less common presenting symptoms of obstruction include pancreatitis and gastric outlet obstruction [16]. Asymptomatic cancer can be detected incidentally

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PET/CT of Pancreatic Neoplasms on abdominal scans obtained for other reasons. CT scans may depict pancreatic neoplasms several months before symptoms become manifest [18]. Increasing use of imaging has led to increased detection of pancreatic abnormalities, and approximately one third of pancreatic incidentalomas turn out to be malignant [19, 20] (Fig. 1). Several rare paraneoplastic syndromes associated with pancreatic cancer have been documented. Trousseau syndrome is a wellestablished paraneoplastic syndrome associated with pancreatic adenocarcinoma that is traditionally defined as migratory thrombophlebitis but has more recently been broadened to include other coagulopathies [21 23]. Pancreatic panniculitis, or subcutaneous areas of nodular fat necrosis, is also associated with pancreatic cancer. Eighty percent of cases of panniculitis related to pancreatic cancer are associated with acinar cell carcinoma. Panniculitis usually involves the lower extremities but also occurs in the buttocks, trunk, and arms [24]. Other interesting paraneoplastic or paraneoplastic-like presenting signs of pancreatic cancer documented at least once include lower leg fasciitis associated with panniculitis [25], eczematous dermatitis [26], fibrous cutaneous hand changes [27], and plantar keratoderma [28]. Pancreatic neuroendocrine tumors present most commonly with abdominal pain; fewer than one half of cases present with endocrine disturbances [29]. Actively secreting neuroendocrine tumors that do cause endocrine disturbances include gastrinoma, which can cause Zollinger-Ellison syndrome; insulinoma, which can cause hypoglycemia; glucagonoma, which can cause diabetes mellitus and is also associated with necrolytic migratory erythema; vasoactive intestinal polypeptide tumor (VIPoma), which can cause watery diarrhea and its associated complications; and somatostatinoma, which is associated with an elevated blood glucose concentration and diarrhea [30]. There are case reports of corticotropin-secreting pancreatic neuroendocrine tumors causing Cushing syndrome [31, 32]. More than one half of all neuroendocrine tumors are carcinoid neoplasms [33], but these neoplasms are very rare in the pancreas [34]. The syndrome they cause is notable for diarrhea and flushing [34]. Hypercalcemia related to parathyroid hormonerelated peptide (PTHrP) has been reported in a PTHrP-producing neuroendocrine tumor [35], among other extremely rare pancreatic neuroendocrine tumors. Role of Multimodality Imaging in Initial Management The major goals of imaging in the initial management of pancreatic neoplasms are to characterize incidentally found lesions, assist with staging of pancreatic cancer, and assist with surgical and radiotherapeutic planning. CT is the best-validated and most widely available modality for diagnosis and initial management, but MRI, MRCP, transabdominal ultrasound, endoscopic ultrasound, ERCP, PET, and PET/CT have all been used (Table 2). The National Comprehensive Cancer Network (NCCN) provides guidelines for the imaging of pancreatic adenocarcinoma in which CT or MRI is recommended for evaluation of patients in whom pancreatic cancer or ductal dilation is clinically suspected [36]. The NCCN similarly recommends multiphasic CT or MRI to evaluate suspected pancreatic neuroendocrine tumors [37]. The American College of Radiology appropriateness criteria for selecting imaging studies are guidelines for imaging of patients with painless jaundice and palpable abdominal masses, again with CT as the most appropriate modality [38, 39]. In numerous studies in recent years, investigators have defined and compared the accuracy of various imaging modalities and techniques and elucidated areas where imaging data are inadequate. This section summarizes current imaging modalities in the initial management of pancreatic neoplasms with a focus on techniques not discussed in depth in the aforementioned established guidelines. Triple-Phase Pancreatic PET/CT Protocol The triple-phase enhanced pancreatic PET/ CT protocol (Fig. 2) is performed at our institution. The patient is given an injection of 10 mCi 18F-FDG and waits 60 minutes. Thirty minutes after injection of FDG, the patient drinks 450 mL of oral contrast barium preparation (VoLumen, E-Z-EM). The patient is scanned from skull base to midthigh according to a routine PET/CT protocol with lowdose attenuation-correction CT. CT is then performed in three phases with diagnostic parameters and contrast administration. The first, unenhanced, phase is a deep-inspiration scan of the lower chest and abdomen with the following parameters: 120 kV; automatic tube current, 150440 mA; slice thickness, 1.25 mm; pitch, 1.375. The second, arterial, phase is a scan of the same area 45 seconds after IV injection of 70 mL of ioversol (Optiray, Mallinckrodt Imaging). The third, venous, phase is a scan of the same area 70 seconds after contrast injection. Hybrid PET/CT images are generated by fusion of the PET and triple-phase CT images. Differentiating Benign From Malignant Disease Multimodality imaging can help characterize lesions as benign or malignant before or, in some benign cases, without tissue diagnosis. The pancreatic CT protocol for evaluation of suspected pancreatic cancer at our institution includes thin-slice MDCT in the unenhanced, arterial, and venous phases (Fig. 2). MRI is an acceptable alternative when patients cannot undergo CT. ERCP, endoscopic ultrasound, and MRCP are useful as adjunct modalities and when CT or MRI reveals ductal stricture but no tumor [36]. The NCCN does not provide specific recommendations regarding PET/CT, except to state that at this time PET/CT is not a substitute for highquality contrast-enhanced CT because its role is still being established [36]. Although the technology exists for combining diagnosticquality CT scans and PET images, imaging protocols are still being standardized [4]. One of the earliest uses of pancreatic PET was to differentiate chronic pancreatitis from pancreatic cancer; diffuse versus focal uptake is the differentiating characteristic in this clinical scenario [40] (Figs. 3 and 4). An early tabulated summary of FDG PET literature [41] showed a 50% change in management effect based on 26 patient studies of the use of PET for the diagnosis of pancreatic cancer in all scenarios with a weighted average sensitivity and specificity of 94% and 90% compared with 82% and 75% for CT at that time. In an early use of fusion PET/CT, Lemke et al. [42] found that fusing triple-phase MDCT with PET images improved the sensitivity of differentiating benign and malignant lesions without a significant change in specificity. PET/CT and MRI can be helpful in detecting pancreatic adenocarcinoma in patients with visually isoattenuating lesions at CT [43]. Pancreatic cancer can be differentiated from autoimmune pancreatitis with PET/CT [44, 45], potentially sparing patients unnecessary surgery. Significantly different standardized uptake values at PET/CT have been reported in malignant intraductal papillary mucinous neoplasms compared with benign lesions [46]. In a meta-analysis of 51 studies [47], PET, PET/CT, and endoscopic ultrasound were compared for usefulness in the diagnosis of all pancreatic carcinomas. The investigators found

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Dibble et al. overall pooled sensitivities of 88.4%, 90.1%, and 81.2% and overall pooled specificities of 83.1%, 80.1%, and 93.2% for the three techniques. Endoscopic ultrasound had the most heterogeneity in study results and was less helpful in the diagnosis of cancer in patients with a history of chronic pancreatitis. To our knowledge, in only four prospective studies [4851] has the usefulness of PET/CT in the diagnosis of pancreatic cancer been examined (Table 3). Two of the reports [48, 50] noted that management was changed and cost saved with PET/CT in certain circumstances, as in the discovery of second primary lesions. By differentiating contrast-enhanced and unenhanced PET/CT, the most recent study [51] showed a problem in summarizing the PET/CT literature: Many study reports are unclear about whether contrast material was used uniformly or at all. Contrast-enhanced imaging is expected to improve the CT component of PET/CT, resulting in superior images; however, use of contrast enhancement requires additional expertise by technical staff and by scan readers (Figs. 58). MRI is an accepted modality for imaging of patients with suspected pancreatic cancer, and MRCP is accurate in the diagnosis of biliary stones and strictures. Like ERCP, MRCP is especially useful when a mass is not seen with other imaging modalities but ductal stricture is suspected or known. As a sole technique for diagnosing pancreatic malignancy, MRCP is similar to ERCP with only 84% sensitivity and 94% specificity, according to a 2003 meta-analysis [52]. In a relatively new use, diffusion-weighted MRI (DWI) has been studied as an additional technique to help differentiate benign from malignant disease. Muhi et al. [53] reported that DWI had sensitivity and specificity of 96.2 and 98.6 in the detection of pancreatic carcinoma by three blinded radiologists. Autoimmune pancreatitis can be differentiated from pancreatic cancer with DWI [45], and significant differences in the apparent diffusion coefficients of chronic pancreatitis and pancreatic carcinoma have been found [54]. Cystic Lesions Incidentally found cystic lesions of the pancreas are a common clinical problem and present a particular challenge in differentiating benign from malignant disease. These cysts are found on approximately 2.3% of CT studies and as many as 19% of MRI studies [55]. Gastroenterology societies, pancreatology groups, and radiology groups all publish guidelines for the management of pancreatic cysts [5658]. Despite the American College of Radiology consensus publication [58] on the management of incidentally found asymptomatic pancreatic cysts, there remains considerable variability in radiologists recommendations for follow-up imaging [59, 60]. This difference may be due in part to the availability of and experience with various imaging modalities not included in the American College of Radiology guidelines. In addition, fewer studies have validated their use, although these alternative imaging modalities and techniques may eventually limit the need for the serial follow-up imaging that is currently recommended [61].

TABLE 1: Major Pancreatic Neoplasms and Their Key Features

Neoplasm Exocrine neoplasms Invasive ductal adenocarcinomas Prevalence greater in male than female patients Head and tail equally affected Symptoms are jaundice and weight loss 85% of all pancreatic neoplasms Acinar cell neoplasms Prevalence greater in male than female patients Head and tail equally affected 12% of all pancreatic neoplasms Pancreatic cystic neoplasms Serous cystic neoplasm Prevalence greater in female than male patients Head and tail equally affected 12% of all pancreatic neoplasms True cystic neoplasm Mucinous cystic neoplasm Prevalence dramatically greater in female than male patients Tail only 12% of all pancreatic neoplasms True cystic neoplasm Intrapapillary mucinous neoplasms Prevalence greater in men than women Head involved more often than tail Exocrine insufficiency, pain 35% of all pancreatic neoplasms Intraductal cystic neoplasm Epithelial and mixed differentiation neoplasms Solid-pseudopapillary neoplasm Prevalence markedly greater in female than male patients Head and tail equally affected Degenerative papillary cystic neoplasm, both solid and cystic 12% of all pancreatic neoplasms Epithelial origin Pancreatoblastoma Prevalence greater in boys than girls Head and tail equally affected Found primarily in children < 1% of all pancreatic neoplasms Neuroendocrine tumors Similar prevalence in male and female patients Head and tail equally affected Endocrine paraneoplastic syndromes 34% of all pancreatic neoplasms Features

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PET/CT of Pancreatic Neoplasms Certain characteristics of cystic lesions help distinguish them as benign versus malignant, such as mural nodules, mural irregularity, peripheral calcifications, and surrounding softtissue nonuniformity relative to the rest of the pancreas. PET/CT has been found comparable or superior to PET or CT alone in determining the presence of malignancy in cystic pancreatic lesions [62] (Fig. 9). In one study [63], PET/CT findings led to modification of the initial management strategy for one of five patients with cystic pancreatic neoplasms. False-positive findings, however, have been problematic in the imaging of cystic tumors [64]. DWI also has been used to help characterize cystic lesions of the pancreas. Wang et al. [65] found it difficult to differentiate inflammatory and neoplastic lesions (both solid and cystic) because of an overlap in apparent diffusion coefficients. In contrast, Takakura et al. [66] reported no significant difference in cancer detection between DWI and the recommended MDCT (84% versus 86%) and noted that MRI with MRCP and DWI allows characterization with a single modality without contrast administration. Staging and Surgical Planning CT, MRI, PET, PET/CT, and laparoscopic and open surgery have all been used for staging pancreatic cancer. CT is the bestvalidated modality and has been the reference standard for assessing locoregional and nodal tumor involvement at or after diagnosis. The pancreatic CT protocol of triphasic cross-sectional imaging and use of thin slices allows assessment of resectability and visualization of important vessels and anatomic relationships (Fig. 10). MRI is an acceptable alternative when patients cannot undergo CT, but it should not be considered an alternative to MDCT, when MDCT is possible, according to NCCN guidelines [36]. A 2009 study [67] comparing gadolinium-enhanced 3D gradient-echo MRCP and MDCT showed similar utility of the two methods in determination of resectability. In terms of the utility of PET, a 2001 analysis of 33 early PET studies [41] showed a combined 36% change in management effect when PET was used for initial staging. Contrast-enhanced PET/CT combines metabolic and anatomic information, and the findings can alter management strategy through prevention of unnecessary laparotomy. In a 2008 study [68], contrast-enhanced PET/CT was significantly superior to PET alone for the preoperative assessment of cancer resectTABLE 2: Advantages and Limitations of Pancreatic Cancer Imaging Techniques
Modality MRI Advantages Depiction of evidence of local extrapancreatic disease Radiation free MRCP Useful for evaluating biliary obstruction Radiation free CT Widely available Best validated PET/CT Depicts evidence of metastatic disease Clarification of equivocal CT findings Limitations Contraindicated with some metal implants and fragments High cost Contraindicated with some metal implants and fragments High cost Radiation and contrast exposure Limited usefulness in evaluation of small metastatic lesions Radiation and contrast exposure High cost

ability. PET and PET/CT both had sensitivities of 100%, but PET alone had a specificity of 44%, whereas PET/CT had 56% specificity. Contrast-enhanced PET/CT was superior to unenhanced PET/CT with a sensitivity of 96% and a specificity of 82%. A small number of patients still had unresectable tumors that were missed with all imaging methods and were diagnosed intraoperatively. In a 2009 study [50], the investigators compared PET/CT, MDCT, and MRI/MRCP and found that PET/CT had higher diagnostic accuracy than other methods, was more sensitive in the diagnosis of primary pancreatic malignancy and metastasis, and had findings that changed the management strategy in 10 of 38 cases. However, PET/CT was less sensitive than the other imaging modalities in the diagnosis of lymph node involvement. Value of FDG PET/CT in the Planning of Radiotherapy for Pancreatic Cancer Resection is the only curative treatment of pancreatic cancer, and optimal adjuvant and neoadjuvant radiotherapeutic approaches remain controversial [6972]. Patients with lesions deemed borderline resectable may be able to undergo resection after chemotherapy, radiotherapy, or both [73]. PET/CT has been suggested as potentially useful in delineating the gross tumor volume for radiotherapeutic planning (Fig. 11). Accurately defining gross tumor volume is critical given the risk to normal surrounding tissue (kidney, small bowel, liver, spinal cord, and stomach) during radiotherapy and the potential for missing the tumor in a conformal radiation field. Ford et al. [64] reviewed the role of PET/CT in radiotherapeutic planning and noted improved

delineation of tumor margins compared with that achieved with CT alone. Similarly, a single-institution study of CT versus PET/CT in the care of 14 patients undergoing radiation planning for unresectable disease showed that the addition of PET resulted in an average 30% increase in gross tumor volume in five patients owing to the incorporation of additional lymph node metastatic lesions and extension of the primary tumor beyond the volume defined with CT [74]. Although radiotherapy may improve local control and resectability rates for pancreatic cancer and PET/CT has been suggested to be useful in conformal treatment planning, improvements in overall survival with optimized radiation therapy remain to be determined. Value of FDG PET/CT in Prognosis and Management Strategy PET and PET/CT findings may play a role in prognosis, assessment of treatment response, and monitoring for cancer recurrence. Schellenberg et al. [75] found that for locally advanced unresectable pancreatic neoplasms, standardized uptake values from pretreatment PET/CT scans were prognostic of overall and progression-free survival even with control for age, presenting CA19-9 result, and single versus combination chemotherapy. Early PET studies showed that PET findings are predictive of histologic response after treatment of pancreatic cancer and that PET shows a decrease in metabolism after intraoperative radiotherapy for unresectable pancreatic cancer earlier than CT does. Thus the tumor response can be evaluated earlier and more accurately with PET than with CT [7679]. PET may also be more accurate than CT in evaluating treatment response and prognosis [80]. Kuwatani et al.

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Dibble et al. TABLE 3: Prospective Studies of PET/CT in the Diagnosis of Pancreatic Cancer
Author Heinrich et al. [48] Schick et al. [49] Kauhanen et al. [50] Buchs et al. [51] Year 2005 2008 2009 2011 n 59 46 38 42 Sensitivity (%) 89 89 85 87.9 Specificity Positive Predictive Negative Predictive (%) Value (%) Value (%) 69 74 94 55.6 91 83 94 87.9 64 82 85 55.6

lesions. The disease progression in this patient likely would have been confirmed earlier with PET/CT, and the patient would have been saved the expense of two noncontributory interval CT scans. Conclusion Numerous imaging modalities are used for the diagnosis and management of pancreatic cancer. The best-validated uses of PET and PET/CT are initial staging and treatment planning. Given the poor prognosis and limited treatment options for pancreatic cancer, the greatest potential benefit is gained during this time frame. Data on the usefulness of PET and PET/CT in surgical and radiotherapeutic planning, for monitoring for treatment response and recurrent disease, and on costeffectiveness are somewhat more limited and require further study. Multimodality imaging is critical in the diagnosis and management of pancreatic cancer. As the spatial resolution of PET/CT continues to improve with the development of 16- and 64-MDCT PET/CT systems and the increasing use of contrast material, contrast-enhanced PET/CT may become the imaging test of choice in the management of pancreatic cancer, and as such continued prospective evaluation is warranted. References
1. American Cancer Society Website. Cancer facts & figures. www.Cancer.Org/research/cancerfactsfigures/index. Accessed October 19, 2011 2. Gress TM, Michl P, Pauls S. Evidence-based diagnosis and staging of pancreatic cancer. Best Pract Res Clin Gastroenterol 2006; 20:227251 3. Balci NC, Semelka RC. Radiologic diagnosis and staging of pancreatic ductal adenocarcinoma. Eur J Radiol 2001; 38:105112 4. Wong TZ, Paulson EK, Nelson RC, Patz EF Jr, Coleman RE. Practical approach to diagnostic CT combined with PET. AJR 2007; 188:622629 5. Subramaniam RM, Truong M, Peller P, Sakai O, Mercier G. Fluorodeoxyglucose-positron-emission tomography imaging of head and neck squamous cell cancer. AJNR 2010; 31:598604 6. Davison JM, Subramaniam RM, Surasi DS, Cooley T, Mercier G, Peller PJ. FDG PET/CT in patients with HIV. AJR 2011; 197:284294 7. Sacks A, Peller PJ, Surasi DS, Chatburn L, Mercier G, Subramaniam RM. Value of PET/CT in the management of primary hepatobiliary tumors, part 2. AJR 2011; 197:366; [web]W260W265 8. Sacks A, Peller PJ, Surasi DS, Chatburn L, Mercier G, Subramaniam RM. Value of PET/CT in the management of liver metastases, part 1. AJR 2011; 197:365; [web]W256W259

[81] found that PET before and after chemotherapy could be used to estimate chemotherapeutic effect and predict survival. A 2011 review of the role of FDG PET/CT in imaging of recurrent pancreatic carcinoma [82] showed that PET/CT improves evaluation of cancer recurrence in general and that, in particular, it improves evaluation of patients with elevated concentrations of tumor markers (CA19-9) and those with normal or equivocal CT findings (Fig. 12). Cost-Effectiveness of FDG PET/CT in the Management of Pancreatic Cancer Cost-effectiveness is a critical factor in determining the optimal imaging modality. In 2006, the most cost-effective and accurate means for diagnosing and staging pancreatic cancer were CT and endoscopic ultrasound [2]. This finding was based on the high cost of MRI, the limited available data on contrast-enhanced PET/CT, and the lack of evidence of the superiority of these modalities to the less expensive CT and endoscopic ultrasound. More recently, however, PET/CT has been recognized as a possible cost-saving imaging modality. Findings at PET and PET/CT for many indications, not only for pancreatic cancer, have been found to change management strategy [83], and although PET/CT has a high initial cost, it has the potential to reduce total imaging costs owing to its superior depiction of distant metastatic lesions, preventing surgery and reducing cancer imaging costs in aggregate. Heinrich et al. [48] have been one of only a few groups of investigators to examine the cost-effectiveness of PET/CT. They found that for imaging pancreatic adenocarcinoma, PET/CT was more sensitive than conventional CT for detecting distant metastasis and that the findings changed the management plans for 16% of patients with lesions deemed resectable after conventional staging. The cost-benefit analysis included the price of PET/CT, the radiotracer, fine-needle aspiration biopsy, cytologic analysis, ultrasound, CT, thoracosco-

py, and pancreatic resection, including physician fees and postoperative stay (based on costs at the authors institution for a 15-day postoperative stay based on range of 1040 days). PET/CT was reported to save an average of $62,912 for all 59 patients included in the study, or $1066 per patient. The authors further determined that limiting PET/CT to patients with lesions deemed resectable at conventional imaging would save $2844 per patient, that limiting the postoperative hospital stay to 10 days led to a savings of $430 per patient, and that using CT-guided fine-needle aspiration rather than ultrasound-guided fineneedle aspiration to confirm each distant metastatic site would still save $341 per patient. The study methods have been criticized, especially with regard to the anatomic field of CT and a lack of preresection laparoscopic exploration cost analysis [84], but the cost analysis was based on an actual standard staging protocol and resultant procedures, not theoretic scenarios, as the authors noted in a reply [85]. In a systematic review of the cost-effectiveness of the use of PET and PET/CT for all diagnoses compared with other imaging techniques and interventions, Langer [86]. concurred that PET may be cost-effective and that PET/CT may be more cost-effective than PET, although only four studies analyzing the cost-effectiveness of PET/CT have been published. Future large prospective studies are still warranted, especially with contrastenhanced PET/CT. An example of the cost-effectiveness of PET/CT occurred at our institution in 2011. A 59-year-old woman was treated for pancreatic cancer found incidentally on a CT scan. Posttreatment PET/CT (Figs. 12A and 12B) showed mild FDG uptake in the soft tissue adjacent to the left kidney that was suspicious for metastatic disease. Two follow-up CT examinations were performed to monitor the lesion and to detect recurrence of disease, but the findings were equivocal. Follow-up PET/CT several months later (Figs. 12C 12G) confirmed the presence of an enlarging perinephric metastatic lesion and new liver

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NCCN guidelines version 1.2011: neuroendocrine tumors. www.nccn.org/professionals/physician_gls/ pdf/neuroendocrine.pdf. Accessed October 19, 2011 38. American College of Radiology Website. ACR appropriateness criteria: clinical conditionpalpable abdominal mass. www.acr.org. Accessed October 28, 2011 39. American College of Radiology Website. ACR appropriateness criteria: clinical condition painless jaundice. www.acr.org. Accessed October 28, 2011 40. van Kouwen MC, Jansen JB, van Goor H, de Castro S, Oyen WJ, Drenth JP. FDG-PET is able to detect pancreatic carcinoma in chronic pancreatitis. Eur J Nucl Med Mol Imaging 2005; 32:399 404 41. Gambhir SS, Czernin J, Schwimmer J, Silverman DHS, Coleman RE, Phelps ME. A tabulated summary of the FDG PET literature. J Nucl Med 2001; 42(5 suppl):1S93S 42. Lemke AJ, Niehues SM, Hosten N, et al. Retrospective digital image fusion of multidetector CT and F-18-FDG PET: clinical value in pancreatic lesionsa prospective study with 104 patients. J Nucl Med 2004; 45:12791286 43. Kim JH, Park SH, Yu ES, et al. Visually isoattenuating pancreatic adenocarcinoma at dynamicenhanced CT: frequency, clinical and pathologic characteristics, and diagnosis at imaging examinations. Radiology 2010; 257:8796 44. Lee TY, Kim MH, Park do H, et al. Utility of 18F-FDG PET/CT for differentiation of autoimmune pancreatitis with atypical pancreatic imaging findings from pancreatic cancer. AJR 2009; 193:343348 45. Kamisawa T, Takum K, Anjiki H, et al. FDGPET/CT findings of autoimmune pancreatitis. Hepatogastroenterology 2010; 57:447450 46. Takanami K, Hiraide T, Tsuda M, et al. Additional value of FDG PET/CT to contrast-enhanced CT in the differentiation between benign and malignant intraductal papillary mucinous neoplasms of the pancreas with mural nodules. Ann Nucl Med 2011; 25:501510 47. Tang S, Huang G, Liu J, et al. Usefulness of 18F-FDG PET, combined FDG-PET/CT and EUS in diagnosing primary pancreatic carcinoma: a meta-analysis. Eur J Radiol 2011; 78:142150 48. Heinrich S, Goerres GW, Schafer M, et al. Positron emission tomography/computed tomography influences on the management of resectable pancreatic cancer and its cost-effectiveness. Ann Surg 2005; 242:235243 49. Schick V, Franzius C, Beyna T, et al. Diagnostic impact of F-18-FDG PET-CT evaluating solid pancreatic lesions versus endosonography, endoscopic retrograde cholangio-pancreatography with intraductal ultrasonography and abdominal ultrasound. Eur J Nucl Med Mol Imaging 2008; 35:17751785 50. Kauhanen SP, Komar G, Seppanen MP, et al. A prospective diagnostic accuracy study of (18)Ffluorodeoxyglucose positron emission tomogra-

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Intravoxel incoherent motion MRI for the differentiation between mass forming chronic pancreatitis and pancreatic carcinoma. Invest Radiol 2011; 46:5763 55. Macari M, Finn ME, Bennett GL, et al. Differentiating pancreatic cystic neoplasms from pancreatic pseudocysts at MR imaging: value of perceived internal debris. Radiology 2009; 251:7784 56. Tanaka M, Chari S, Adsay V, et al. International consensus guidelines for management of intraductal papillary mucinous neoplasms and mucinous cystic neoplasms of the pancreas. Pancreatology 2006; 6:1732 57. Simeone DM. SSAT/AGA/ASGE state of the art conference on cystic neoplasms of the pancreas. J Gastrointest Surg 2008; 12:14751477 58. Berland LL. The American College of Radiology strategy for managing incidental findings on abdominal computed tomography. Radiol Clin North Am 2011; 49:237243 59. Macari M, Megibow AJ. Focal cystic pancreatic lesions: variability in radiologists recommendations for follow-up imaging. Radiology 2011; 259: 2023 60. Di Muzio N, Broggi S, Passoni P, et al. PET/CT guided helical tomotherapy in patients with locally advanced pancreatic cancer. Radiother Oncol 2005; 76(suppl 2):S165S166 61. Berland LL, Silverman SG, Gore RM, et al. Managing incidental findings on abdominal CT: white paper of the ACR incidental findings committee. J Am Coll Radiol 2010; 7:754773 62. Tann M, Sandrasegaran K, Jennings SG, Skandarajah A, McHenry L, Schmidt CM. Positronemission tomography and computed tomography of cystic pancreatic masses. Clin Radiol 2007; 62:745751 63. Pery C, Meurette G, Ansquer C, Frampas E, Regenet N. Role and limitations of (18)F-FDG positron emission tomography (PET) in the management of patients with pancreatic lesions. Gastroenterol Clin Biol 2010; 34:465474 64. Ford EC, Herman J, Yorke E, Wahl RL. (18)FFDG PET/CT for image-guided and intensitymodulated radiotherapy. J Nucl Med 2009; 50:16551665 65. Wang Y, Chen ZM, Yaghmai V, et al. Diffusionweighted MR imaging in pancreatic endocrine tumors correlated with histopathologic characteristics. J Magn Reson Imaging 2011; 33:10711079 66. Takakura K, Sumiyama K, Munakata K, et al. Clinical usefulness of diffusion-weighted MR imaging for detection of pancreatic cancer: comparison with enhanced multidetector-row CT. Abdom Imaging 2011; 36:457462 67. Park HS, Lee JM, Choi HK, Hong SH, Han JK, Choi BI. Preoperative evaluation of pancreatic cancer: comparison of gadolinium-enhanced dynamic MRI with MR cholangiopancreatography versus MDCT. J Magn Reson Imaging 2009; 30:586595 68. Strobel K, Heinrich S, Bhure U, et al. Contrastenhanced F-18-FDG PET/CT: 1-stop-shop imaging for assessing the resectability of pancreatic cancer. J Nucl Med 2008; 49:14081413 69. [No authors listed]. Further evidence of effective adjuvant combined radiation and chemotherapy following curative resection of pancreatic cancer. Gastrointestinal Tumor Study Group. Cancer 1987; 59:20062010 70. Klinkenbijl JH, Jeekel J, Sahmoud T, et al. Adjuvant radiotherapy and 5-fluorouracil after curative resection of cancer of the pancreas and periampullary region: phase III trial of the EORTC Gastrointestinal Tract Cancer Cooperative Group. Ann Surg 1999; 230:776782 71. Neoptolemos JP, Dunn JA, Stocken DD, et al. Adjuvant chemoradiotherapy and chemotherapy in resectable pancreatic cancer: a randomised controlled trial. Lancet 2001; 358:15761585 72. Neoptolemos JP, Stocken DD, Friess H, et al. A randomized trial of chemoradiotherapy and chemotherapy after resection of pancreatic cancer. N Engl J Med 2004; 350:12001210 73. Crane CH, Varadhachary G, Wolff RA, Pisters PW, Evans DB. The argument for pre-operative chemoradiation for localized, radiographically resectable pancreatic cancer. Best Pract Res Clin Gastroenterol 2006; 20:365382 74. Topkan E, Yavuz AA, Aydin M, Onal C, Yapar F, Yavuz MN. Comparison of CT and PET-CT based planning of radiation therapy in locally advanced pancreatic carcinoma. J Exp Clin Cancer Res 2008; 27:41 75. Schellenberg D, Quon A, Minn AY, et al. 18Fluorodeoxyglucose PET is prognostic of progressionfree and overall survival in locally advanced pancreas cancer treated with stereotactic radiotherapy. Int J Radiat Oncol Biol Phys 2010; 77:14201425 76. Rose DM, Delbeke D, Beauchamp RD, et al. 18Fluorodeoxyglucose-positron emission tomography in the management of patients with suspected pancreatic cancer. Ann Surg 1999; 229:729 737; discussion 737738 77. Higashi T, Sakahara H, Torizuka T, et al. Evaluation of intraoperative radiation therapy for unresectable pancreatic cancer with FDG PET. J Nucl Med 1999; 40:14241433 78. Maisey NR, Webb A, Flux GD, et al. FDG-PET in the prediction of survival of patients with cancer of the pancreas: a pilot study. Br J Cancer 2000; 83:287293 79. Yoshioka M, Sato T, Furuya T, et al. 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Impact of positron emission tomography/computed tomography and positron emission tomography (PET) alone on expected management of patients with cancer: initial results from the National Oncologic PET Registry. J Clin Oncol 2008; 26:21552161 84. Goh BK. Positron emission tomography/computed tomography influences on the management of resectable pancreatic cancer and its cost-effectiveness. Ann Surg 2006; 243:709710 85. Heinrich S, Schafer M, Clavien PA. Positron emission tomography/computed tomography influences on the management of resectable pancreatic cancer and its cost-effectiveness. (letter) Ann Surg 2006; 243:710 86. Langer A. A systematic review of PET and PET/ CT in oncology: a way to personalize cancer treatment in a cost-effective manner? BMC Health Serv Res 2010; 10:283

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Fig. 177-year-old man with incidental finding of pancreatic lesion at routine 2-year imaging follow-up of laryngeal cancer. A and B, Coronal maximum-intensity-projection (A) and axial (B) PET images show increased uptake in area of pancreas (arrow, B). C and D, Axial CT (C) and corresponding PET/CT (D) images show 2-cm poorly marginated low-attenuation mass at junction of body and tail of pancreas with moderate FDG uptake (arrow, D). Distal pancreas and spleen resection yielded pancreatic ductal carcinoma and multiple negative peripancreatic lymph nodes.

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Fig. 255-year-old man with pancreatic adenocarcinoma. AF, Unenhanced (A), arterial (C), and venous (E) phase CT images and corresponding fused FDG PET/CT (B, D, and F) images show appearance during triple-phase contrast-enhanced pancreatic PET/CT protocol.

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Fig. 367-year-old man with jaundice and vague abdominal pain due to autoimmune pancreatitis. ERCP revealed diffuse irregular narrowing of main pancreatic duct. A and B, Coronal maximum-intensity-projection (A) and axial PET (B) images show moderate diffuse increased FDG accumulation in pancreas (percutaneous drainage tube is present in common bile duct and passes to outside drainage bag). C, Axial CT image shows diffusely enlarged pancreas and mild prominence in pancreatic head with distinct mass formation. D, Fused axial PET/CT image shows relatively homogeneous increased activity throughout pancreas (maximum standardized uptake value, 5.1). Serum assays revealed elevated antinuclear antibody, rheumatoid factor, and antilactoferrin antibody levels. Treatment with corticosteroids produced prompt remission.

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Fig. 462-year-old man undergoing chemotherapy for metastatic lung cancer with idiopathic pancreatitis causing severe upper abdominal pain that radiates to back. ERCP showed diffuse irregular narrowing of main pancreatic duct without site of obstruction. Metastatic nodes were present adjacent to pancreatic head. A and B, Coronal maximum-intensity-projection (A) and axial PET (B) images show moderate diffuse increased FDG accumulation in pancreas. C, Axial CT scan shows diffusely enlarged pancreas. D, Axial fused PET/CT scan shows moderate diffuse increased FDG accumulation and enlarged pancreas. Symptoms resolved with supportive treatment.

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Fig. 552-year-old woman with hypoglycemic episodes and increasing back pain and history glucagon-secreting pancreatic neuroendocrine tumor treated with resection of primary tumor and left hepatic lobe. AC, Coronal maximum-intensity-projection (A), axial PET (B), and fused axial PET/CT (C) images show 2.5-cm mass in head of pancreas with mild FDG uptake (arrow, C). D, Axial CT scan shows hypoenhancing pancreatic head lesion. E, T1-weighted fat-suppressed MR image shows lesion. F, Octreotide SPECT/CT scan shows intense 111In-octreotide accumulation in pancreatic head mass (arrow). G, T1-weighted fat-suppressed contrast-enhanced MR image shows hyperenhancing pancreatic head mass (arrow). Biopsy confirmed recurrent glucagon-secreting pancreatic neuroendocrine tumor.

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Fig. 664-year-old woman with pancreatic adenocarcinoma, acholic stools, and jaundice. A, T2-weighted selective partial inversion recovery MR image shows pancreatic head mass (arrow) with obstruction. B, Axial contrast-enhanced CT image shows heterogeneously enhancing necrotic solid mass (arrow) in pancreatic head. C, Axial contrast-enhanced fused PET/CT image shows intense hypermetabolic activity (arrow) corresponding to mass in B.

Fig. 772-year-old man with pancreatic lymphoma, epigastric discomfort, and fatigue. Upper gastrointestinal endoscopic findings were normal. AC, Coronal maximum-intensity-projection (A) and axial PET (B and C) images show intense FDG uptake in pancreas. D and E, Axial CT images show 2.5-cm hypoenhancing pancreatic mass (arrow, D) and spleen for PET/CT comparison. F and G, Axial fused PET/CT images show 2.5-cm uncinate mass with intense FDG uptake (maximum standardized uptake value, 8.9) and moderate diffuse activity in spleen (arrow, G) that suggested lymphoma. Fine-needle aspiration of pancreatic mass and bone marrow biopsy yielded follicular non-Hodgkin lymphoma.

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Fig. 870-year-old man with history of hairy cell leukemia initially diagnosed 4 years earlier and treated with splenectomy and chemotherapy. Follow-up CT showed 3.2 2.7 cm mass in body of pancreas. A, Coronal maximum-intensity-projection image shows moderate diffuse activity in bone marrow of axial and proximal appendicular skeleton. B, Axial PET image shows increased uptake in pancreatic head (arrow). C and D, Axial CT (C) and corresponding PET/CT (D) images show 3.2-cm mass (arrow, D) in head of pancreas with moderate FDG uptake (maximum standardized uptake value, 5.0). Pancreatic mass and bone marrow biopsies confirmed diagnosis of recurrent hairy cell leukemia.

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Fig. 946-year-old man with abdominal pain due to pancreatic adenocarcinoma. AD, Coronal maximum-intensity-projection (A), coronal contrast-enhanced fused PET/CT (B), and axial contrast-enhanced fused PET/CT (C and D) images show hypermetabolic activity and mass (arrow, C and D) in head and neck of pancreas without evidence of metastatic disease. Biliary stent is in place. E and F, Axial contrast-enhanced CT images show cystic lesion (arrow, F). Cystic areas are likely pseudocysts.

Fig. 1058-year-old man with 6 weeks of painless jaundice; ultrasound showed pancreatic abnormality. A and B, Coronal arterial (A) and venous (B) phase CT images show heterogeneously enhancing mass (blue arrow, A) in head of pancreas encasing hepatic artery and dilatation of common bile (yellow arrow, A) and pancreatic (red arrow, A) ducts.

Fig. 1162-year-old man with known inoperable T2N0M0 adenocarcinoma of the pancreas undergoing staging scanning for radiotherapeutic planning. A, Axial CT image shows head of pancreas with indwelling stent. B, Same axial slice as A fused with FDG PET scan obtained for staging. PET enables radiation oncologist to more easily discern gross tumor volume (inner outline), for which 50 Gy in 25 daily fractions is prescribed, whereas clinical target volume (outer outline) encompassing locoregional nodal basins receives 45 Gy in 25 fractions through dose painted intensity-modulated technique.

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Fig. 1259-year-old woman with history of pancreatic adenocarcinoma found incidentally on CT scan. A and B, Contrast-enhanced axial CT (A) and contrast-enhanced axial fused PET/CT (B) images obtained immediately after therapy show mild FDG uptake in soft tissue adjacent to left kidney (arrow, B) that was suspicious for metastatic disease. CG, Follow-up coronal maximum-intensity-projection (C), axial contrast-enhanced CT (D and E), and axial contrast-enhanced fused PET/CT images (F and G) scans obtained several months after A and B confirm presence of enlarging perinephric metastatic lesion and new liver lesion (arrows, F and G). Two interval CT scans between the PET/CT scans were noncontributory.

F O R YO U R I N F O R M AT I O N

This article is part of a self-assessment module (SAM). Please also refer to PET/CT of Cancer Patients: Part 2, Deformable Registration Imaging Before and After Chemotherapy for Radiation Treatment Planning in Head and Neck Cancer, which can be found on page 968. Each SAM is composed of two journal articles along with questions, solutions, and references, which can be found online. You can access the two articles at www.ajronline.org, and the questions and solutions that comprise the Self-Assessment Module by logging on to www.arrs.org, clicking on AJR (in the blue Publications box), clicking on the article name, and adding the article to the cart and proceeding through the checkout process. The American Roentgen Ray Society is pleased to present these SAMs as part of its commitment to lifelong learning for radiologists. Continuing medical education (CME) and SAM credits are available in each issue of the AJR and are free to ARRS members. Not a member? Call 1-866-940-2777 (from the U.S. or Canada) or 703-729-3353 to speak to an ARRS membership specialist and begin enjoying the benefits of ARRS membership today!

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