Jpn J Radiol (2014) 32:571–578 DOI 10.1007/s11604-014-0346-5
PICTORIAL ESSAY
Imaging spectrum of peritoneal carcinomatosis on FDG PET/CT Ameya D. Puranik • Nilendu C. Purandare • Archi Agrawal • Sneha Shah • Venkatesh Rangarajan
Received: 2 July 2014 / Accepted: 28 July 2014 / Published online: 14 August 2014 Ó Japan Radiological Society 2014
Abstract Recognition of patterns has always been extremely important in cross-sectional imaging. Peritoneal involvement, both primary and as dissemination from abdominopelvic malignancies, is manifested in different forms, purely because of anatomical complexity. We studied series of peritoneal involvement by 18F-fluorodeoxyglucose positron-emission tomography/computed tomography fusion imaging and derived patterns of tracer uptake on maximum intensity projection and cross-sectional fusion images. Keywords Peritoneum Ovary Colon Mesothelioma Lymphoma FDG PET/CT
Introduction The peritoneum is a thin serous membrane which encloses a large space known as the peritoneal cavity. It lines the abdominal cavity (parietal peritoneum), and supports the abdominal viscera (visceral peritoneum) [1]. Vascular and lymphatic vessels and nerves supplying the abdominal organs gain access through peritoneal folds. Omenta and mesentery are double folds of the peritoneum which enclose the bowel loops and are attached to the organs or to the posterior abdominal wall [1, 2]. Abdominopelvic malignancies have easy access to the peritoneal cavity; spread occurs via direct rupture, by intraperitoneal seeding from ascites, or by hematogenous or lymphatic routes [1]. To
A. D. Puranik N. C. Purandare A. Agrawal S. Shah V. Rangarajan (&) Department of Nuclear Medicine and Molecular Imaging, Tata Memorial Hospital, Dr E Borges Marg, Mumbai 400012, India e-mail:
[email protected]
identify peritoneal involvement, fluorodeoxyglucose positron-emission tomography/computed tomography (FDG PET/CT) is known to be more sensitive than diagnostic CT or stand alone PET [3]. Patterns of involvement are so widespread there is a possibility of missing the pathology.
Materials and methods We present nine ‘‘classical’’ cases of malignancies with peritoneal involvement, proved by use of FDG PET/CT, selected from 2400 studies over the past three years. Whole-body FDG PET/CT was performed after fasting for 6 h. Blood sugar was controlled below 170 mg/dL for diabetics. Injected activity was 222–375 MBq, depending on body weight. After an uptake time of 45–60 min, wholebody acquisition was performed by use of the GE Discovery STE BGO-based PET/CT system. The studies were analyzed by use of dedicated PET/CT fusion workstations.
Mechanism of peritoneal spread and manifestation in images Gynecological cancers Ovarian cancers (Figs. 1, 2) are primarily epithelial cancers; hence, tumor cells are easily washed off the ovary into the peritoneal circulation leading to seeding at several sites [4]. Further, the peritoneal fluid moves upwards, because of pressure gradients in the abdominal cavity. The sub-atmospheric pressure in the sub-diaphragmatic space is because the movement of the rib cage is greater than that of the diaphragm; this provides a gradient for movement of peritoneal fluid. The fluid initially enters the paracolic
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Fig. 1 A 61-year-old female underwent radical surgery in 2008 for ovarian cancer. Follow up was uneventful until the last 2 months, when she started complaining of vague abdominal pain. Serum CA 125 levels were raised. FDG PET/CT study was performed. Maximum intensity projection (MIP) image revealed foci of uptake in the
liver and abdomen (a arrows). Axial FDG PET and fused FDG PET/ CT images revealed nodular peritoneal deposits along the perihepatic space (b, d arrows). Also seen were FDG-avid mesh-like ill-defined soft tissue deposits along the greater omentum (c, e arrows)
gutters. On the left side, the phrenico-colic ligament serves as a barrier, hence fluid predominantly moves into the right paracolic gutter. It then readily ascends into the right subhepatic and subphrenic regions. Another important peritoneal fold is the greater omentum, which overlies the transverse colon and is a common site of metastatic seeding [5]. FDG PET/CT for ovarian cancers is indicated for restaging after recurrence. Although determination of CA 125 levels enables detection of early recurrence with high sensitivity, it gives no information about the location and has poor negative predictive value; FDG PET/CT reveals pelvic and extra-pelvic recurrence with good sensitivity, thereby changing subsequent management [6]. Peritoneal involvement is also seen in cervical cancers (Fig. 3). PET/CT enables sensitive monitoring of patients with locally advanced cancers subjected to radical radiotherapy [7].
abdominal contours. Multiple mechanisms have been proposed for peritoneal dissemination in colorectal (Fig. 4) and pancreatic (Fig. 5) cancers. It can occur from intraperitoneal tumor emboli, because of serosal penetration, or after surgical management as a result of leakage of malignant cells from lymphatic vessels or because of their dissemination during tumor dissection [8]. Cancers with predominantly mucinous histology (Fig. 6) are often a challenge in PET/CT imaging because of the absence or low concentration of the tracer [9]. In such cases, morphological features on CT and the pattern of low intensity FDG uptake should be carefully assessed. Ascites is a common manifestation of peritoneal dissemination in gastric malignancies. Sagittal MIP images typically show FDG uptake along the peritoneal lining and central photopenia, because of fluid in the abdominal cavity, which itself may be an indicator of peritoneal involvement, even before viewing cross-sectional images. The uptake pattern on axial images is typically low grade diffuse—characteristic for mucinous tumors—and can be often reported as physiological.
Abdominal malignancies MIP images provide a good indication of the possibility of peritoneal involvement by prominently revealing
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Fig. 2 A 56-year-old female diagnosed with cystadenocarcinoma of the ovary, underwent radical surgery, following which, she received adjuvant chemotherapy. Four months later, she presented with rising serum CA 125 levels, hence an FDG PET/CT study was conducted. MIP images revealed intense foci of uptake in the liver and spleen (a arrows), apparently suggestive of parenchymal metastases.
However, a sagittal fused FDG PET/CT image revealed uptake in the gastrosplenic ligament (b arrow), and coronal (c, d arrows) and axial (e, f arrows) PET and CT images indicated uptake was located in the peritoneal reflection of the liver adjacent to porta hepatis region, suggestive of peritoneal disease
Pseudomyxoma peritonei (PMP)
these manifest as intensely FDG-avid diffuse intra-peritoneal masses spreading in a sheet like fashion [13]. Although it is commonly mistaken for peritoneal carcinomatosis, appearance in images of coalescent solid contiguous masses along the peritoneal lining is characteristic of primary peritoneal mesothelioma.
PMP, which involves deposition of copious thick gelatinous material on the peritoneal surface, is primarily diagnosed radiologically. It is commonly seen in association with tumors with mucinous histology, commonly involving the appendix, followed by the gall bladder, which penetrate and rupture the peritoneal cavity [10]. It is often mistaken for post-operative collection or simple ascites, typically because of poor FDG uptake and the absence of hypermetabolism on the MIP image (Fig. 7). On CT, it is typically seen as low-attenuation masses containing abundant mucin. Poor patchy uptake within these masses is seen in areas of solid tumor, which confirms the diagnosis [11]. More importantly, pre-operative FDG PET/CT may enable prediction of pathological grade and completeness of cytoreduction, which are important prognostic factors for patients with PMP [12].
Burkitt’s lymphoma Common clinical presentation of Burkitt’s (Non-Hodgkin’s) lymphoma is fever, vomiting, and severe abdominal pain associated with intestinal obstruction or intussusception. Our case underwent laparotomy for symptomatic relief; histopathology confirmed the diagnosis. Peritoneal involvement is commonly seen in all varieties of lymphoma (Fig. 9), however diffuse peritoneal, mesenteric, and omental involvement is common with Burkitt’s type [14].
Primary peritoneal mesothelioma Teaching points Malignant mesothelioma is an uncommon malignant neoplasm, originating from multipotent subserosal mesenchymal cells of the pleura, peritoneum, or pericardium or the tunica vaginalis of the testes. Although most originate from the pleura, primary peritoneal tumors account for 10 % of cases [13]. On cross-sectional PET/CT imaging (Fig. 8),
Pattern recognition on FDG PET/CT helps in detecting peritoneal involvement, because these areas are difficult to target in biopsies and the possibility of false negative results is high. In such cases, attempted biopsies further hamper the imaging accuracy of CT [15]. A commonly
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Fig. 3 A 74-year-old female, who received definitive radiotherapy for cervical cancer stage IIB, presented with abdominal pain. FDG PET/CT was performed for restaging. MIP image showed discrete foci of tracer uptake in the abdomen, with a linear pattern along bilateral subdiaphragmatic spaces (a arrows). Free fluid with FDG uptake was noted in the left peri-hepatic and left subdiaphragmatic spaces. Also seen was FDG-avid soft tissue thickening along the greater omentum and paracolic gutters with free fluid interspersed
within, suggestive of peritoneal dissemination (b, d arrows). Linear band-like FDG uptake along the domes of the diaphragm and along the liver surface on MIP image was suggestive of subdiaphragmatic and perihepatic soft tissue mass-like peritoneal involvement (c, e arrows). Patchy foci of uptake on MIP image were suggestive of omental seeding. Also seen is linear uptake along the bilateral paracolic gutters, confirmed on fused FDG PET/CT to be a result of peritoneal involvement
observed pattern of peritoneal implants is the appearance of tiny nodules (Case 1), which are often missed on multi detector CT and also often misinterpreted as physiological bowel uptake. These lesions become obvious only when they coalesce to form masses (Case 2). Hypermetabolism in these nodules on PET/CT aids discovery of subtle peritoneal involvement. Typically, implants on the diaphragmatic surface appear as nodular thickening of the diaphragm (Case 1), whereas liver and splenic involvement manifest as low-attenuation masses that scallop the surface (Case 2). These lesions are sometimes seen at rare sites, for example the porta hepatis (Case 2), and may be mistaken for liver parenchymal involvement. Infiltration of omental fat is seen as nodular deposits indistinguishable from bowel loops, detection of which is made possible by FDG uptake (Case 1). FDG PET/CT is more sensitive than FDG PET and CT alone for detection of peritoneal metastases; specificity is higher than for FDG PET and equal to that for CT alone. Metabolic tracer uptake is a useful adjunct to CT findings, which can sometimes be non-specific, for example post-operative or post-intervention abdomen in an
oncological setting. CT is helpful in case of mucinous and signet ring cell histology (Cases 6, 7), in which metabolic tracer is not concentrated. For low-volume peritoneal metastases (Case 5), uptake of FDG reveals the disease process, thereby resulting in management change. Similar to CT, specific classical imaging profiles on PET MIP and cross sectional images are indicative of peritoneal carcinomatosis, as can be seen from the above cases. The closest mimic of peritoneal carcinomatosis on FDG PET/CT is tuberculous peritonitis [16], seen as diffuse abdominal FDG uptake. There are no imaging features enabling the two conditions to be distinguished. The clinical profile of the patient, histopathology, and imaging follow-up after treatment provide valuable insights leading to confirmatory diagnosis.
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Imaging patterns Patterns on PET/CT can be classified as focal nodular, diffuse, and mass-like. Diffuse uptake, when seen with
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Fig. 4 A 40-year-old male, a known case of carcinoma of the sigmoid colon, underwent sigmoid colectomy and subsequently received adjuvant chemotherapy. On follow up, serum CEA levels were raised, hence he underwent FDG PET/CT for restaging. MIP image (a) revealed diffusely increased tracer uptake in the abdomen. Axial FDG PET and fused FDG PET/CT images revealed diffuse
low-grade FDG uptake throughout the abdomen and pelvis. Illdefined stranding was noted along the greater omentum, the root of the mesentery, and the pararectal fascia, suggestive of diffuse peritoneal carcinomatosis (b–e arrows). A highlight of this case is the common cross-sectional imaging sign ‘‘omental caking’’, with diffuse low-grade FDG uptake
Fig. 5 A 57-year-old male, a case of locally advanced pancreatic adenocarcinoma, came for FDG PET/CT-based radiotherapy planning. MIP image revealed tracer uptake in a primary site in the pancreas (a thick arrow), with foci of uptake in the lower neck (thyroid nodule) and the left paracolic region (a thin arrows). Axial fused FDG PET/CT images revealed a hypodense FDG-avid peritoneal nodule in left paracolic region (b, c thin arrow), closely abutting
the bowel loops. Contrast enhanced CT enables highly accurate identification of peritoneal involvement in disseminated disease. Subcentimeter-sized localized nodules are often difficult to identify. Metabolic uptake, as seen in this case, helps reveal peritoneal spread, thus changing management from radical curative to palliative
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Fig. 6 A 39-year-old male, a known case of signet ring cell adenocarcinoma of the stomach, received neo-adjuvant chemotherapy, and FDG PET/ CT was conducted for assessment of response to treatment. Sagittal MIP image shows linear tracer uptake along the anterior abdominal wall (a thin arrows), with a large area of absent tracer uptake in the abdomen (a thick arrows). This corresponded to FDG uptake along the greater omentum, and gross ascites on axial fused PET and PET/CT images (b, c thin arrows) suggestive of peritoneal spread
visualization of abdominal contours, is an indication of uptake along the peritoneal linings, which is suggestive of carcinomatosis (Cases 4 and 6). MIP images provide a good indication of the possibility of peritoneal involvement by prominently highlighting abdominal contours. On fused PET/CT, the greater omentum appears as a band of fatty tissue which becomes smudged in early omental disease. There is further progression to soft tissue nodules, which then coalesce to form a thickened mass with low-grade diffuse FDG uptake which replaces the omental fat—an ‘omental cake’ (Case 4). Also, carcinomatosis in mucinous tumors can manifest as diffuse low-grade uptake in multiple collections on PET/CT, suggestive of PMP (Case 7). Diffuse intense tracer uptake with ‘‘dark’’ MIP images, as seen in our case, is classical for Burkitt’s (Case 9). Such focal patterns as prominent perihepatic or perirenal tracer uptake, or uptake along dependent areas, for example paracolic gutters or the pouch of Douglas (Cases 1, 3, 5), are strongly suggestive of peritoneal disease. Focal uptake along any of the peritoneal folds scalloping the solid organs
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often mimics parenchymal metastases (Case 2), but pattern of uptake confirms it to be in the omental folds. In addition, intense mass-like uptake of FDG along peritoneal folds in the absence of primary abdominal malignancy is suggestive of primary peritoneal neoplasm (Case 8).
Conclusion Peritoneal involvement can be either primary or from malignancies of the ovary, cervix, stomach, and other abdominal organs. Because the area of involvement can be variable and often occult, patterns must be developed for early detection. FDG PET/CT with its metabolic–morphological fusion aids identification of peritoneal disease, as illustrated in the above cases. Specific patterns of uptake—focal nodular, diffuse, or mass-like—have been derived from these cases, both on MIP and cross sectional fusion images; this could simplify diagnosis of peritoneal involvement.
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Fig. 7 A 73-year-old male underwent laparoscopic cholecystectomy for symptomatic gallstones; histopathology revealed moderately differentiated adenocarcinoma with pools of mucin. FDG PET/CT was performed for restaging. MIP image revealed diffuse colonic uptake with no abnormal tracer uptake noted elsewhere (a thin arrows). Axial fused FDG PET/CT images (b–d thin arrows)
revealed multiple hypodense low attenuation masses with poor, diffuse FDG uptake in perigastric, peri-splenic, peripancreatic spaces. Pockets of fluid were seen in the peripancreatic region (e thin arrow), with soft tissue nodules (b, e thick arrows) in the peritoneal cavity. These mucinous collections in the peritoneal spaces suggested diagnosis of pseudomyxoma peritonei
Fig. 8 A 19-year-old female presented with vague abdominal pain for two months. There were no associated symptoms. Ultrasonography revealed free fluid in the perihepatic and perirenal spaces. Because no primary site was apparent, an FDG PET/CT study was conducted. MIP image revealed intense tracer concentration along the liver margins and in the abdomen (a thin arrows), with focus of tracer uptake in the left paracolic region (a thick arrow). Coronal CT and
fused PET/CT (b, d thin arrows), and sagittal fused PET/CT (f thin arrow) images revealed intensely FDG-avid soft tissue hypodense masses in the perihepatic space contiguously extending into the perirenal space, suggestive of peritoneal origin, which was confirmed on biopsy to be a primary peritoneal mesothelioma. Another FDGavid discrete nodule was seen along the left para-rectal fascia suggestive of distant peritoneal spread (c, e thick arrow)
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Fig. 9 A four-year-old boy presented with abdominal pain for two months which progressively increased in intensity. CT study of the abdomen was suggestive of ileo-ileal intussusception. Because of high suspicion of lymphomatous involvement, the patient was referred for FDG PET/CT for baseline staging. An MIP image (a) revealed diffuse, uniformly intense tracer uptake throughout the
abdomen. Minimal ascites was noted, with no evidence of splenic involvement. Axial fused FDG PET/CT images revealed diffuse hypermetabolism throughout the peritoneal spaces and mesentery (b– e), which was confirmatory for lymphomatous involvement by nonHodgkin’s lymphoma, Burkitt’s type
Conflict of interest The authors declare that they have no conflicts of interest.
subjective probabilities and economic modelling. Health Technol Assess. 2013;17:1–323. Delbeke D, Martin WH. FDG PET and PET/CT for colorectal cancer. Methods Mol Biol. 2011;727:77–103. Berger KL, Nicholson SA, Dehdashti F, Siegel BA. FDG PET evaluation of mucinous neoplasms: correlation of FDG uptake with histopathologic features. AJR Am J Roentgenol. 2000; 174:1005–8. Hossain J, Malabarey T, al-Mofleh I, Hawass NE, Ismail AH. Clinical and radiological features of pseudomyxoma peritonei. J R Soc Med. 1989;82:600–2. Harshen R, Jyothirmayi R, Mithal N. Pseudomyxoma peritonei. Clin Oncol (R Coll Radiol). 2003;15:73–7. Passot G, Glehen O, Pellet O, Issac S, Tychyj C, Mohamed F, et al. Pseudomyxoma peritonei: role of 18F-FDG PET in preoperative evaluation of pathological grade and potential for complete cytoreduction. Eur J Surg Oncol. 2010;36:315–23. Levy AD, Arna´iz J, Shaw JC, Sobin LH. From the archives of the AFIP: primary peritoneal tumors: imaging features with pathologic correlation. Radiographics. 2008;28:583–607. Biko DM, Anupindi SA, Hernandez A, Kersun L, Bellah R. Childhood Burkitt lymphoma: abdominal and pelvic imaging findings. AJR Am J Roentgenol. 2009;192:1304–15. De Gaetano AM, Calcagni ML, Rufini V, Valenza V, Giordano A, Bonomo L. Imaging of peritoneal carcinomatosis with FDG PET-CT: diagnostic patterns, case examples and pitfalls. Abdom Imaging. 2009;34:391–402. Takalkar AM, Bruno GL, Reddy M, Lilien DL. Intense FDG activity in peritoneal tuberculosis mimics peritoneal carcinomatosis. Clin Nucl Med. 2007;32:244–6.
8.
References 1. Coakley FV, Hricak H. Imaging of peritoneal and mesenteric disease: key concepts for the clinical radiologist. Clin Radiol. 1999;54:563–74. 2. Healy JC, Reznek RH. The peritoneum, mesenteries and omenta: normal anatomy and pathological processes. Eur Radiol. 1998;8:886–900. 3. Dirisamer A, Schima W, Heinisch M, Weber M, Lehner HP, Haller J, et al. Detection of histologically proven peritoneal carcinomatosis with fused 18F-FDG-PET/MDCT. Eur J Radiol. 2009;69:536–41. 4. Wang E, Ngalame Y, Panelli MC, Nguyen-Jackson H, Deavers M, Mueller P, et al. Peritoneal and subperitoneal stroma may facilitate regional spread of ovarian cancer. Clin Cancer Res. 2005;11:113–22. 5. Pannu HK, Bristow RE, Montz FJ, Fishman EK. Multidetector CT of peritoneal carcinomatosis from ovarian cancer. Radiographics. 2003;23:687–701. 6. Nougaret S, Addley HC, Colombo PE, Fujii SS, Al Sharif SS, Tirumani SH, et al. Ovarian carcinomatosis: how the radiologist can help plan the surgical approach. Radiographics. 2012;32:1775–800. 7. Meads C, Auguste P, Davenport C, Malysiak S, Sundar S, Kowalska M, et al. Positron emission tomography/computerised tomography imaging in detecting and managing recurrent cervical cancer: systematic review of evidence, elicitation of
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9.
10.
11. 12.
13.
14.
15.
16.
