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1 Note: This copy is for your personal, non-commercial use only. To order presentation-ready copies for distribution to your colleagues or clients, contact us at Servet Tatli, MD Victor H. Gerbaudo, PhD Marcelo Mamede, MD, PhD Kemal Tuncali, MD Paul B. Shyn, MD Stuart G. Silverman, MD Abdominal Masses Sampled at PET/CT-guided Percutaneous Biopsy: Initial Experience with Registration of Prior PET/CT Images 1 Purpose: Materials and Methods: To establish the feasibility of performing combined positron emission tomography (PET)/computed tomography (CT)-guided biopsy of abdominal masses by using previously acquired PET/CT images registered with intraprocedural CT images. In this HIPAA-compliant institutional review board approved study, 14 patients underwent clinically indicated percutaneous biopsy of abdominal masses (mean size, 3.3 cm; range, cm) in the liver ( n = 6), presacral soft tissue ( n = 3), retroperitoneal lymph nodes ( n = 2), spleen ( n = 2), and pancreas ( n = 1). PET/CT images obtained no more than 62 days (mean, 18.3 days) before the biopsy procedure were registered with intraprocedural CT images by using image registration software. The registered images were used to plan the procedure and help target the masses. ORIGINAL RESEARCH n VASCULAR AND INTERVENTIONAL RADIOLOGY Results: Conclusion: The image registrations were technically successful in all but one patient, who had severe scoliosis. The remaining 13 biopsy procedures yielded diagnostic results, which were positive for malignancy in 10 cases and negative in three cases. PET/CT guided abdominal biopsy with use of prior PET/CT images registered with intraprocedural CT scans is feasible and may be helpful when fluorine 18 fluorodeoxyglucose avid masses that are not seen sufficiently with nonenhanced CT are sampled at biopsy. q RSNA, From the Department of Radiology, Divisions of Abdominal Imaging and Intervention (S.T., K.T., P.B.S., S.G.S.) and Nuclear Medicine (V.H.G., M.M.), Brigham and Women s Hospital, Harvard Medical School, 75 Francis St, Boston, MA Received June 22, 2009; revision requested August 5; revision received October 21; accepted November 18; fi nal version accepted January 20, Address correspondence to S.T. ( statli@partners.org ). q RSNA, 2010 Radiology: Volume 256: Number 1 July 2010 n radiology.rsna.org 305

2 Positron emission tomography (PET) is a functional imaging technique capable of interrogating the metabolic characteristics of masses ( 1 ). Inherent advantages include the early detection of malignancy, in some cases before changes are evident morphologically, and the delineation of viable malignant tissue in masses that contain nonmalignant tissue such as fibrosis ( 1 3 ). Because of its high sensitivity in the detection of malignancy, the use of PET in clinical practice has increased, particularly with the introduction of hybrid PET/computed tomography (CT) scanners ( 4 ). However, fluorine 18 fluorodeoxyglucose (FDG) uptake is not specific for malignancy. Benign causes such as inflammatory processes are also FDG avid ( 5,6 ). Therefore, percutaneous biopsy may be indicated to determine the cause of an FDG-avid mass. Nonenhanced CT often is used to guide percutaneous biopsy ( 7 ). However, some lesions detected with PET may have little or no correlative CT findings ( 8,9 ). As a result, it may not be possible to perform biopsy with PET findings alone. Nonenhanced CT guided biopsy of such lesions may lead to false-negative results because of sampling error. Furthermore, some neoplasms contain metabolically active tumor cells in only a part of the mass ( 7 ). Therefore, if PET information could be integrated into a CT-guided biopsy procedure, biopsy of more lesions could be performed and the yield of biopsy potentially could be improved ( 7 ). Such integration can be achieved manually or by using computers. Previously obtained PET/CT scans can be reviewed by the interventional radiologist, and the biopsy can be planned according to the PET/CT findings. Alternatively, image registration software can be used. With use of such software, preprocedural PET images can be registered to intraprocedural nonenhanced CT images and displayed on a single Advance in Knowledge n PET/CT-guided biopsy of abdomi- nal masses with use of previously acquired PET/CT images registered with intraprocedural CT images is feasible. screen. Thus, the purpose of this study was to establish the feasibility of performing PET/CT-guided percutaneous biopsy of abdominal masses by using previously acquired PET/CT images registered with intraprocedural CT images. Materials and Methods Study Population This prospective study was compliant with the Health Insurance Portability and Accountability Act and approved by the institutional review board at our institution. There was no industry support. Participants were selected from among patients referred to our cross-sectional interventional radiology service for clinically indicated percutaneous biopsy, and they provided written informed consent before participating in the study. Participants were aged 18 years or older and were found at presentation to have an FDG-avid mass that either was not visible or had margins that were not clearly defined at nonenhanced CT. We also included patients with a mass that showed FDG uptake that was limited to or greater in one part of the mass. Between December 2006 and December 2007, among 553 patients who were referred to our radiology department for abdominal biopsy, 14 participants (nine women, five men; mean age, 59.6 years; age range, years) fulfilled the described criteria and were enrolled. Twelve of these patients had a known malignancy, which was cancer of the colon ( n = 4), breast ( n = 3), liver ( n = 1), or endometrium ( n = 1), or lymphoma ( n = 3). Two participants had no known malignancy. Biopsy was performed in 14 masses (mean size, 3.3 cm; Implication for Patient Care n With use of image registration software, prior PET/CT images usually can be used during biopsy to help target malignant abdominal masses that are not well seen at nonenhanced CT or contain noncancerous tissue that otherwise would reduce the yield of percutaneous biopsy. range, cm) one in each patient in the liver ( n = 6), presacral soft tissue ( n = 3), spleen ( n = 2), and pancreas ( n = 1), and in enlarged lymph nodes in the retroperitoneum ( n = 2). Two liver masses were located in segment V, and one mass each was located in segments III, IV, VI, and VII. Biopsy had been performed previously in one of the presacral soft-tissue masses at our institution and yielded inadequate material. PET/CT Imaging PET/CT was performed no more than 62 days (mean, 18.3 days) before the biopsy procedure. Patients fasted for at least 4 hours before intravenous injection of FDG (Cardinal Health, Woburn, Mass) (mean injected dose 6 standard deviation, 21.0 mci [777.0 MBq ]). PET/CT (Discovery ST; GE Medical Systems, Milwaukee, Wis) was performed a mean of 73.4 minutes (range, minutes) after the FDG injection. CT was performed with the patient supine, from the head to the proximal part of the thighs, for attenuation correction and anatomic coregistration without oral or intravenous contrast material. Imaging parameters were 140 kvp, ma, and 1.25-mm collimation, with reconstruction as 3.75-mmthick sections by using a matrix and a filtered back-projection algorithm. Immediately after CT, PET images of the same volume were obtained in two-dimensional mode for 4-minute acquisitions at each level for six to seven Published online before print /radiol Radiology 2010; 256: Abbreviations: FDG = fl uorine 18 fl uorodeoxyglucose SUV max = maximum standardized uptake value Author contributions: Guarantors of integrity of entire study, S.T., V.H.G.; study concepts/study design or data acquisition or data analysis/ interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript fi nal version approval, all authors; literature research, S.T., V.H.G., M.M., K.T., S.G.S.; clinical studies, S.T., V.H.G., M.M., S.G.S.; and manuscript editing, all authors Authors stated no fi nancial relationship to disclose. 306 radiology.rsna.org n Radiology: Volume 256: Number 1 July 2010

3 bed positions. PET images were reconstructed by using a matrix and an iterative ordered-subset expectation maximization algorithm (two iterations, 30 subsets), yielding a volume of 47 sections with a voxel size of mm. For each lesion, a maximum standardized uptake value (SUV max ) corrected for body weight (BW) was generated as follows: SUV max = ( A t 3 BW)/ A a, where A t is the concentration of radioactive activity in the tissue and A a is the administered radioactive activity. The lesional SUV max was measured as the maximal point on the axial image with the highest activity. The mean SUV max of the tumors in the study was calculated as 10.1 (range, ). No patient had surgical clips or metallic hardware adjacent to the tumor. Among the 14 masses (in 14 patients), 10 were invisible ( n = 4; two in presacral soft tissue, one in the liver, one in the spleen) or had margins that were not clearly defined ( n = 6; four in the liver, one in the spleen, one in the pancreas) on the nonenhanced CT scans. In the remaining four masses (two lymph nodes, one in the liver, and one in presacral soft tissue), the tumor was visible on the nonenhanced CT scans but showed either FDG uptake in only a part of the mass or greater uptake in one part than in another. After PET/CT, all but three patients with presacral masses were examined with diagnostic contrast material enhanced CT ( n = 9) or magnetic resonance (MR) imaging ( n = 2), the results of which were used to confirm the tumors. Tumors that were invisible with nonenhanced CT were sized by using the semiautomatic segmentation function of the registration software to calculate the largest diameter of metabolic activity ( 10 ). Biopsy Procedure All biopsy procedures were performed by three abdominal interventional radiology staff members (S.T., K.T., S.G.S., with 8, 12, and 20 years of experience, respectively) in an interventional CT suite with a CT scanner equipped with CT fluoroscopy capability (Somatom Plus 4 with CARE Vision; Siemens Medical Solutions, Forchheim, Germany). Patients were supine ( n = 9) or prone ( n = 5) during the biopsy procedure, depending on the location of the mass sampled at biopsy and the needle path identified with the PET/CT scans. A radiopaque grid (Beekley, Bristol, Conn) was placed, and initial nonenhanced CT was performed for procedure planning. No patient received intravenous contrast material during the biopsy procedure. Whole-body PET/CT images were transferred in Digital Imaging and Communications in Medicine format from the radiology department network to a separate laptop computer. A PET/CT image data set (typically 25 pairs of images) that included the mass and the surrounding anatomy was selected. The CT scanner was programmed to recognize the Internet protocol address of the laptop. Through a local area network connection, the planning CT scan (120 kvp, 120 mas, 5-mm section thickness) with a volume (typically 25 images) that matched the selected PET/CT scan data set was transferred to the laptop computer in Digital Imaging and Communications in Medicine format. An image containing the most FDG-avid portion of the mass was chosen from the PET scans, and a matching image from the intraprocedural CT scans was selected. Four structures that were visible on both the PET/CT image and the planning CT image, such as the borders of the liver and other abdominal organs, were identified and selected as landmarks. On the basis of these landmarks, the PET/ CT and intraprocedural CT images were registered by using Medical Image Processing, Analysis, and Visualization software (Biomedical Imaging Research Services Section, National Institutes of Health, Bethesda, Md) ( 10,11 ). This software is available without charge on the Internet and is compatible with several platforms, including Windows, Mac, UNIX, and Linux. The interventional radiologists who performed the procedure reviewed the registered images, and the biopsy approach was planned. The skin was marked, prepared, and draped in the usual sterile fashion. Two percent lidocaine (Hospira, Lake Forest, Ill) was used for local anesthesia, and an initial biopsy needle (E-Z-Em, Westbury, NY) was placed with use of intermittent CT fluoroscopy. CT was repeated, and the images were registered to the PET/CT images as described previously. The needles were repositioned if the needle tip was not in the most FDG-avid portion of the mass. Each registration was completed within 3 5 minutes (mean, 3.8 minutes). All patients received an intravenous sedative (midazolam, Versed, Roche, Nutley, NJ; and fentanyl citrate, Sublimaze, Hospira, Lake Forest, Ill) for conscious sedation during the procedures. Biopsy specimens were obtained by using 25-gauge needles in 10 patients; five specimens were obtained coaxially by using a 20-gauge needle, and five were obtained by using a tandem technique. In the remaining four patients, only 22-gauge needles were placed by using a tandem technique. We used fine needles because of their better overall safety profile relative to that of large needles and because fine needles are adequate most of the time ( 12,13 ). Additional large (18-gauge) needles were used in two patients in whom lymphoma was suspected. In another patient with a history of lymphoma, who was found to have a paraduodenal mass at presentation, we used only fine needles because the mass was surrounded by critical organs including blood vessels and bile ducts. Between two and eight passes (mean, 4.5 passes) were performed during each biopsy procedure. A cytotechnologist was present during all procedures to evaluate the initial specimen for adequacy. When malignant cells were not obtained initially, we obtained additional specimens to be sure that the mass was sampled adequately. After the biopsy procedure, the patients were observed for 2 6 hours and discharged. Procedure duration, defined as the time of initial planning CT to the time of postbiopsy CT, ranged from 44 to 87 minutes (mean, 62 minutes). Complications were recorded. Biopsy results were categorized as positive if malignant cells were present, with a specific diagnosis, and negative if no malignant cells were identified. The results were confirmed by means of surgery or either follow-up PET/CT or follow-up CT (mean, 21 months; range, months). Radiology: Volume 256: Number 1 July 2010 n radiology.rsna.org 307

4 Figure 1 Figure 1: Images in 73-year-old woman with history of breast and lung cancer. (a) Axial PET image shows FDG-avid focus (arrow) in left liver lobe. Posterior (1) and anterior (2) borders of liver, anterior border (3) of spine, and posterior border (4) of left kidney are marked (cursors). (b) On corresponding axial nonenhanced CT image obtained during biopsy, FDG-avid focus is not visible. (c) Image resulting from registration of a and b with use of Medical Image Processing, Analysis, and Visualization software after selection of four landmarks ( 1 4 in a ) from each image. (d) Axial CT image obtained to confi rm needle tip location. (e) Image resulting from registration of d and a shows one biopsy needle (arrow) is inside FDG-avid mass, but other needle (arrowhead) is not. Biopsy revealed metastatic breast cancer. Results The image registrations were technically successful in all but one patient, in whom severe scoliosis resulted in severe misregistration and thus the registered images could not be used to guide the biopsy procedure. The remaining 13 biopsy procedures yielded diagnostic results, which were positive for malignancy in 10 cases and negative in three cases. Of the 10 positive results for malignancy, four were metastases from the patients known primary tumors ( Fig 1 ), four were lymphoma, and two were primary liver and pancreas cancers ( Fig 2 ) (one each). There were three negative nonmalignant biopsy results: two from biopsy performed in presacral masses and one from biopsy performed in a splenic mass. Biopsy results from a 1.5-cm presacral mass (SUV max, 6.9) yielded fibrosis and necrotic tissue with- out malignant cells; the patient underwent laparotomy and surgical excision of the mass. Only hyalinized fibrous tissue with focal chronic inflammation was found. Biopsy results from a 3-cm presacral mass (SUV max, 5.8) yielded numerous neutrophils and bacteria that suggested an abscess. A repeat biopsy of the mass was performed with colonoscopy; only ulcerated mucosa with necrosis and inflammatory debris were found. The presacral mass was stable at both 6-month follow-up PET/CT and 18-month follow-up CT. The third negative biopsy result was encountered in a patient with a history of lymphoma in remission. A 3-cm, moderately FDG-avid (SUV max, 5.7) splenic mass was suggestive of lymphoma; however, biopsy results revealed only normal splenic parenchyma. With no further treatment, 24-month follow-up PET/CT revealed that the abnormality had become smaller and less FDG avid (SUV max, 3.1). There were no complications. Discussion We describe a method of and our initial experience performing PET/CT-guided biopsy by using a CT scanner and prior PET/CT images and demonstrate the feasibility of this procedure in a select group of patients. Although registration was not possible in a patient with severe scoliosis, we were able to obtain a diagnosis in the remaining 13 patients in whom we were able to perform image registration. The added value of PET can be described in two ways. First, some lesions detected with PET have little or no correlative CT findings. As a result, accurate targeting is difficult, procedures may be prolonged, and radiation exposure to the patient and health care personnel may be increased. Second, some lesions detected with PET are not homogeneously FDG avid; they are FDG avid in only one part of the mass, or FDG avidity is greater in one part of the mass. CT-guided biopsy of such masses 308 radiology.rsna.org n Radiology: Volume 256: Number 1 July 2010

5 Figure 2 Figure 2: Images obtained in 67-year-old woman with history of lymphoma, with PET/CT depicting FDG-avid focus suspected to be lymphoma adjacent to second portion of duodenum and pancreatic head. 1 = posterior border of liver, 2 = anterior border of liver, 3 = anterior border of spine, 4 = lateral border of left kidney. (a) Axial PET image from prior PET/CT scanning and (b) axial intraprocedural nonenhanced CT image were registered to form image in c. The FDG-avid focus (arrow in a ) is not clearly visible in b. (d) Axial CT image obtained to confi rm needle tip location was registered with a to form image in e, which shows needle tip (curved arrow) inside the mass (straight arrow). Biopsy revealed pancreatic adenocarcinoma. also is difficult because the biopsy might be performed in the non FDG-avid or poorly FDG-avid part of the mass and yield a false-negative result. Therefore, the information provided by PET can be used to target the metabolically active mass if there are multiple masses or the metabolically active part of a mass ( Fig 3 ). As a result, the yield of biopsy may be improved. Fusing images from two modalities requires accurate image alignment. This process is known as image registration and can be accomplished by using software algorithms ( ). Image registration has been used for many clinical applications; for example, brain images from different modalities have been registered to facilitate stereotactic biopsy of brain masses ( 16,17 ). Before the development of PET/CT scanners, registration techniques were used to combine PET and CT images that were acquired in different scan- ners at different times ( 17 ). Software registration of images from multiple modalities also has been used successfully for radiation therapy planning ( 19 ). Registered anatomic (CT, MR) and metabolic (PET) images help the radiation therapist irradiate the entire tumor while avoiding critical normal tissues ( 7,19 ). Electromagnetic navigation devices also use registration software to help track the location of needle tips and merge the location onto cross-sectional images ( 20 ). The feasibility of using these devices during image-guided interventions has been shown in phantom and animal models ( 20 ). Some of these devices can be used to register real-time ultrasonographic (US) images with a volume of previously acquired cross-sectional images such as CT scans ( 15 ). Such systems have been used to guide some interventional radiology procedures, including ablation ( 21 ). Image registration of separately acquired anatomic and functional images performed by using computer software is more accurate than is visual coregistration, particularly in parts of the body that do not move with respiration, such as the brain ( 16 ). Image registration algorithms can be classified as rigid (linear) or nonrigid (elastic) ( 14,15 ). The rigid image registration used in our study is the oldest registration algorithm and is widely available ( 7,14,15 ). It is fast and particularly applicable to lesions in the retroperitoneum and pelvis because they typically do not change their location relative to the adjacent bone structures. However, rigid registration techniques are prone to errors when registering deformable organs, particularly those adjacent to the diaphragm that can change location and shape because of patient movement, respiration, or cardiac motion ( 14,16,18 ). Nonrigid algorithms can accommodate deformable organs Radiology: Volume 256: Number 1 July 2010 n radiology.rsna.org 309

6 Figure 3 Figure 3: Images obtained in 74-year-old woman with history of breast cancer, with PET/CT depicting FDG-avid focus in liver. 1 = posterior border of liver, 2 = anteromedial border of liver, 3 = left lateral abdominal wall, 4 = posterior spinous process of spine. (a) Axial PET image from prior PET/CT scanning and (b) axial intraprocedural CT image were registered to form image in c. The mass (arrow in a ) accumulated FDG heterogeneously and was not clearly visible in b. (d) Axial CT image obtained to confi rm needle tip location was registered with a to form image in e, which shows tip of one needle (arrow) in the most metabolically active portion of the mass. Biopsy revealed metastatic breast cancer. that move, facilitating accurate image registration. However, clinically available nonrigid algorithms require powerful computers and are too labor and time intensive to implement during interventional procedures ( 22,23 ). Despite the limitations of rigid registration algorithms, we were able to register PET and CT images of masses in the liver and spleen for successful biopsy of these lesions. Our registration algorithm required that matching landmarks be defined manually on both intraprocedural CT and PET/CT images. Manual matching results in more accurate registration than does matching performed automatically with computers ( 15 ). However, manual matching is more time-consuming, and, thus, its real-time use during interventional procedures is not possible. PET/CT does not have to be performed at the same institution or on a scanner from the same manufacturer as the interventional CT scanner. As long as the data set is in Digital Imaging and Communications in Medicine format, the software can be used to perform the registration. Since PET/CT usually is performed with the patient supine, registration can be challenging if a patient s position needs to be altered during the biopsy procedure. Depending on the patient s degree of rotation from the supine position during the biopsy, the PET/CT images need to be rotated manually to match the intraprocedural CT images. Our study was limited in that it included a small number of patients and no control group. Also, we did not assess the accuracy of the registrations. However, our aim was to describe the technique and demonstrate the clinical feasibility of PET/CT-guided biopsy with use of prior PET/CT image registration. PET/CT images can also be used to guide percutaneous biopsy in a PET/CT scanner ( 24 ). However, the advantage of our approach is that in patients who have undergone diagnostic PET/CT, an additional FDG injection and its attendant cost and radiation exposure is avoided. If a mass is not well visualized with nonenhanced CT, intravenous contrast material can be administered during CT-guided biopsy. This commonly used method, however, is limited because contrast material enhancement of some masses (eg, hepatocellular carcinoma) may be transient and insufficient to guide the entire length of the procedure ( 25 ). US or MR imaging guidance also can be used to perform biopsy of masses that are not visible with nonenhanced CT. However, some masses are not visible with US. MR imaging typically requires special wide-bore or open-configuration imaging units. Furthermore, these modalities still may be limited in their depiction of the neoplastic part of masses that also contain nonneoplastic parts. Finally, PET/CT has some known shortcomings. FDG activity may not be detectable in small (eg,, 5 mm) tumors or in tumors recently treated with chemotherapy that prevents FDG uptake by cancer cells ( 7 ). Also FDG avidity can be a false-positive result due to infection or inflammation ( 26 ). In conclusion, PET/CT-guided biopsy of abdominal masses with use of prior PET/CT images registered with intraprocedural CT scans is feasible. This technique can be particularly helpful when biopsy is performed in masses that are FDG avid but not well visualized with nonenhanced CT and in masses that have 310 radiology.rsna.org n Radiology: Volume 256: Number 1 July 2010

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