DOI: 10.1148/rg.261055078
RadioGraphics 2006;26:143-156
© RSNA, 2006
CT and PET in Stomach Cancer: Preoperative Staging and Monitoring of Response to Therapy1
Joon Seok Lim, MD,
Mi Jin Yun, MD,
Myeong-Jin Kim, MD,
Woo Jin Hyung, MD,
Mi-Suk Park, MD,
Jin-Young Choi, MD,
Tae-Sung Kim, MD,
Jong Doo Lee, MD,
Sung Hoon Noh, MD and
Ki Whang Kim, MD
1 From the Departments of Diagnostic Radiology (J.S.L., M.J.K., M.S.P., J.Y.C., K.W.K.), Nuclear Medicine (M.J.Y., T.S.K., J.D.L.), and Surgery (W.J.H., S.H.N.), Yonsei University College of Medicine, 134 Shinchon-dong, Seodaemoon-ku, Seoul, 120–752, Republic of Korea. Presented as an education exhibit at the 2004 RSNA Annual Meeting. Received April 4, 2005; revision requested April 28 and received June 1; accepted June 13. All authors have no financial relationships to disclose.
Address correspondence to M.J.Y. (e-mail: yunmijin{at}yumc.yonsei.ac.kr).
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Abstract
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Stomach cancer is one of the leading causes of cancer mortality worldwide. Complete resection of a gastric tumor and adjacent lymph nodes represents the only potentially curative intervention. Computed tomography (CT) has remained the modality of choice for the preoperative staging of gastric cancer and for follow-up. A recently developed advanced CT technique that makes use of thin sections, optimal contrast material enhancement, and multiplanar reformation allows more accurate staging. However, CT may be limited in the identification of nonenlarged lymph node metastasis, peritoneal dissemination, and small hematogenous metastasis. Positron emission tomography (PET) with 2-[fluorine-18]fluoro-2-deoxy-D-glucose (FDG) has been recognized as a useful diagnostic technique in clinical oncology. FDG PET allows scanning of a larger volume than is possible with CT. Although FDG PET is not an appropriate first-line diagnostic procedure in the detection of stomach cancer and is not helpful in tumor staging, it may play a valuable role in the detection of distant metastases, such as those of the liver, lungs, adrenal glands, ovaries, and skeleton. FDG PET may also be helpful in the follow-up of patients undergoing chemotherapy, as it allows the identification of early response to treatment. Further studies are needed to determine the efficacy of FDG PET in the detection of local nodal metastases and peritoneal dissemination. Nevertheless, the combined use of CT and PET can be helpful in the preoperative staging of stomach cancer and in the therapeutic monitoring of affected patients.
© RSNA, 2006
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Introduction
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Stomach cancer remains the second most common cancer worldwide. In Far Eastern countries, such as Korea, China, and Japan, as well as in many developing countries, gastric cancer is the most prevalent malignant neoplasm and the leading cause of cancer death (1). In the Western world, more than 80% of patients have an advanced gastric cancer with a poor prognosis at the time of diagnosis (2).
Complete resection of a gastric tumor and adjacent lymph nodes is considered the only proved, effective curative treatment (3,4); however, the treatment of gastric cancer has become increasingly sophisticated, with therapies tailored to individual cases (2). Treatment includes a broad spectrum of therapeutic options, from endoscopic mucosal resection for selected mucosal cancers to more radical treatments for advanced cancers. Therefore, accurate preoperative staging, particularly with regard to depth of mural invasion, adjacent organ invasion, nodal involvement, and distant metastases, is vital in determining the most suitable therapy and avoiding inappropriate attempts at curative surgery. Computed tomography (CT) has been the modality of choice for pre-operative evaluation and staging in patients with gastric carcinoma. In addition, CT has been the primary tool in determining both the presence of recurrent tumors and their response to chemotherapy; however, its use is limited, particularly in the diagnosis of lymph node metastasis, peritoneal metastasis, and small hematogenous metastasis (5,6). There is a need for a better method of preoperative staging of stomach cancer. Positron emission tomography (PET) with 2-[fluorine-18]fluoro-2-deoxy-D-glucose (FDG) has been recognized as a useful diagnostic technique in clinical oncology (7), but experience with its use in evaluating stomach cancer is limited. FDG PET appears to be highly accurate in determining resectability and detecting distant metastatic disease at the time of initial diagnosis, but it may be of limited use in locoregional staging (8).
In this article, we describe the TNM (tumor-node-metastasis) staging system of stomach cancer and its clinical significance. We also discuss and illustrate the relative advantages and limitations of CT and FDG PET in pretreatment staging and in the monitoring of response to therapy. In addition, we discuss the possible benefits of combined CT and PET in this setting.
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Tumor Staging
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Tumor stages are defined according to the American Joint Committee on Cancer (AJCC) staging system (9) as follows: T1, tumor invades lamina propria or submucosa; T2, tumor invades muscularis propria or subserosa; T3, tumor penetrates serosa (visceral peritoneum) without invasion of adjacent structures; and T4, tumor invades adjacent structures. Accurate T staging is the most significant element in determining appropriate treatment plans.
Initial studies found close agreement between T staging as determined with CT and pathologic T staging (10–12), but many subsequent studies have reported disappointing results (13–15). Endoscopic ultrasonography (US) is currently the most reliable method available for preoperative determination of T stage, with a diagnostic rate of 78%–93% (16,17). Botet et al (18) reported that endoscopic US had a significantly higher degree of accuracy than dynamic CT for T staging. Recently, an advanced CT technique that makes use of thin sections, optimal contrast material enhancement, and multiplanar reformation has been used for more accurate staging. In a few recent studies, advanced CT has shown promising accuracy compared with endoscopic US in T staging (19,20). However, further studies will be required to determine its efficacy in this setting.
The invasion of cancer into the gastric wall as visualized at CT has been classified as follows: In T1 and T2 lesions, invasion is limited to the gastric wall, whose outer border may be smooth (Fig 1a, 1b); in T3 lesions, the serosal contour becomes blurred, and strand-like areas of increased attenuation may be seen extending into the perigastric fat (Fig 1c); and in T4 lesions, tumor spread frequently occurs via ligamentous and peritoneal reflections to adjacent organs. The transverse colon may be invaded via the gastrocolic ligament (Fig 1d), the pancreas via the lesser sac (Fig 1e), and the liver via the gastrohepatic ligament (Fig 1f).
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Figure 1a. Stage T1–T4 gastric tumors. (a) Coronal reformatted image shows a stage T1 tumor (arrows) with focal nontransmural enhancement in the upper body. (b) Axial CT scan shows a stage T2 tumor (arrow), a localized, transmurally enhancing ulcerative mass without perigastric extension, in the lower body. (c) Coronal reformatted image shows a stage T3 tumor (arrows), with gross infiltration of the perigastric fat tissue in the antrum. (d) Axial CT scan shows a stage T4 tumor with invasion of the colon. The tumor represents an advanced cancer of the antrum and is accompanied by obliteration of the fat plane and thickening of the colonic wall (arrows). (e) Coronal reformatted image shows a stage T4 tumor (arrow) infiltrating the distal pancreatic body. (f) Axial CT scan shows a stage T4 tumor (arrows), an advanced cancer with gross infiltration of the lateral segment of the liver.
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Figure 1b. Stage T1–T4 gastric tumors. (a) Coronal reformatted image shows a stage T1 tumor (arrows) with focal nontransmural enhancement in the upper body. (b) Axial CT scan shows a stage T2 tumor (arrow), a localized, transmurally enhancing ulcerative mass without perigastric extension, in the lower body. (c) Coronal reformatted image shows a stage T3 tumor (arrows), with gross infiltration of the perigastric fat tissue in the antrum. (d) Axial CT scan shows a stage T4 tumor with invasion of the colon. The tumor represents an advanced cancer of the antrum and is accompanied by obliteration of the fat plane and thickening of the colonic wall (arrows). (e) Coronal reformatted image shows a stage T4 tumor (arrow) infiltrating the distal pancreatic body. (f) Axial CT scan shows a stage T4 tumor (arrows), an advanced cancer with gross infiltration of the lateral segment of the liver.
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Figure 1c. Stage T1–T4 gastric tumors. (a) Coronal reformatted image shows a stage T1 tumor (arrows) with focal nontransmural enhancement in the upper body. (b) Axial CT scan shows a stage T2 tumor (arrow), a localized, transmurally enhancing ulcerative mass without perigastric extension, in the lower body. (c) Coronal reformatted image shows a stage T3 tumor (arrows), with gross infiltration of the perigastric fat tissue in the antrum. (d) Axial CT scan shows a stage T4 tumor with invasion of the colon. The tumor represents an advanced cancer of the antrum and is accompanied by obliteration of the fat plane and thickening of the colonic wall (arrows). (e) Coronal reformatted image shows a stage T4 tumor (arrow) infiltrating the distal pancreatic body. (f) Axial CT scan shows a stage T4 tumor (arrows), an advanced cancer with gross infiltration of the lateral segment of the liver.
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Figure 1d. Stage T1–T4 gastric tumors. (a) Coronal reformatted image shows a stage T1 tumor (arrows) with focal nontransmural enhancement in the upper body. (b) Axial CT scan shows a stage T2 tumor (arrow), a localized, transmurally enhancing ulcerative mass without perigastric extension, in the lower body. (c) Coronal reformatted image shows a stage T3 tumor (arrows), with gross infiltration of the perigastric fat tissue in the antrum. (d) Axial CT scan shows a stage T4 tumor with invasion of the colon. The tumor represents an advanced cancer of the antrum and is accompanied by obliteration of the fat plane and thickening of the colonic wall (arrows). (e) Coronal reformatted image shows a stage T4 tumor (arrow) infiltrating the distal pancreatic body. (f) Axial CT scan shows a stage T4 tumor (arrows), an advanced cancer with gross infiltration of the lateral segment of the liver.
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Figure 1e. Stage T1–T4 gastric tumors. (a) Coronal reformatted image shows a stage T1 tumor (arrows) with focal nontransmural enhancement in the upper body. (b) Axial CT scan shows a stage T2 tumor (arrow), a localized, transmurally enhancing ulcerative mass without perigastric extension, in the lower body. (c) Coronal reformatted image shows a stage T3 tumor (arrows), with gross infiltration of the perigastric fat tissue in the antrum. (d) Axial CT scan shows a stage T4 tumor with invasion of the colon. The tumor represents an advanced cancer of the antrum and is accompanied by obliteration of the fat plane and thickening of the colonic wall (arrows). (e) Coronal reformatted image shows a stage T4 tumor (arrow) infiltrating the distal pancreatic body. (f) Axial CT scan shows a stage T4 tumor (arrows), an advanced cancer with gross infiltration of the lateral segment of the liver.
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Figure 1f. Stage T1–T4 gastric tumors. (a) Coronal reformatted image shows a stage T1 tumor (arrows) with focal nontransmural enhancement in the upper body. (b) Axial CT scan shows a stage T2 tumor (arrow), a localized, transmurally enhancing ulcerative mass without perigastric extension, in the lower body. (c) Coronal reformatted image shows a stage T3 tumor (arrows), with gross infiltration of the perigastric fat tissue in the antrum. (d) Axial CT scan shows a stage T4 tumor with invasion of the colon. The tumor represents an advanced cancer of the antrum and is accompanied by obliteration of the fat plane and thickening of the colonic wall (arrows). (e) Coronal reformatted image shows a stage T4 tumor (arrow) infiltrating the distal pancreatic body. (f) Axial CT scan shows a stage T4 tumor (arrows), an advanced cancer with gross infiltration of the lateral segment of the liver.
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Differentiation between T3 and T4 lesions is particularly important because extensive invasion of T4 lesions into adjacent structures makes surgery difficult, and with massive tumor invasion there is little possibility of resection (21). A gastric mass that abuts an adjacent organ and absence of the fat plane between the mass and the organ are suggestive of but not diagnostic for organ invasion. However, coronal or sagittal reformatted images may be helpful in making the diagnosis (Fig 1e).
PET is not helpful in T staging because it is a functional imaging modality. In primary tumor detection, variable levels of FDG uptake have been found. Gastric adenocarcinomas, such as mucinous carcinoma, signet ring cell carcinoma (Fig 2) (22), and poorly differentiated adenocarcinomas (23), tend to show significantly lower FDG uptake than do other histologic types of gastric cancer.
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Figure 2a. Signet ring cell carcinoma without significant FDG uptake in a 30-year-old woman with stomach cancer. (a) Axial CT scan shows diffuse thickening of nearly the entire gastric wall (arrowheads) due to linitis plastica. (b) Coronal PET scan shows no discernible FDG uptake in the stomach (arrows).
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Figure 2b. Signet ring cell carcinoma without significant FDG uptake in a 30-year-old woman with stomach cancer. (a) Axial CT scan shows diffuse thickening of nearly the entire gastric wall (arrowheads) due to linitis plastica. (b) Coronal PET scan shows no discernible FDG uptake in the stomach (arrows).
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Node Staging
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Under the new AJCC classification system, N staging is based on the number of positive nodes (N1, metastasis in one to six regional lymph nodes; N2, metastasis in seven to 15 lymph nodes; and N3, metastasis in more than 15 lymph nodes) (9). This approach differs from the previous classification system, which was based on anatomic nodal location.
Several studies have confirmed the superiority of number of positive nodes in the estimation of prognosis (24–27), but anatomic nodal location remains a valuable criterion (Fig 3, Table) because the D classification, a description of the extent of lymphadenectomy, is determined according to the level of lymph node dissection (D1–D4).
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Figure 3. Drawing illustrates lymph node locations according to the Japanese Research Society for Gastric Cancer (28). 1 = right paracardium, 2 = left paracardium, 3 = lesser curvature, 4 = greater curvature, 5 = suprapylorum, 6 = infrapylorum, 7 = left gastric artery, 8 = common hepatic artery, 9 = celiac artery, 10 = splenic hilum, 11 = proximal splenic artery, 12 = hepatoduodenal ligament, 13 = posterior surface of the pancreatic head, 14 = superior mesenteric vessels (SMA = superior mesenteric artery, SMV = superior mesenteric vein), 15 = middle colic vessels, 16 = abdominal aorta.
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The regional lymph nodes of the stomach are classified into four compartments according to the Japanese Research Society for Gastric Cancer (28). Compartment I includes the perigastric lymph nodes (stations 1–6). Compartment II includes lymph nodes along the left gastric artery (station 7) and common hepatic artery (station 8) (Fig 4), around the celiac axis (station 9), at the splenic hilum (station 10), and along the splenic artery (station 11). Compartment III includes lymph nodes in the hepatoduodenal ligament (station 12) (Fig 5), at the posterior aspect of the head of the pancreas (station 13) (Fig 6), and at the root of the mesentery (station 14) (Fig 6). When the cancer is located in the lower third of the stomach, lymph nodes along the splenic artery are classified as compartment III nodes. Compartment IV includes lymph nodes along the middle colic vessels (station 15) and the paraaortic lymph nodes (station 16) (Fig 7 ).
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Figure 4a. Station 7 and 8 lymph node metastases in a 63-year-old man with stomach cancer. (a) Axial CT scan demonstrates a station 7 lymph node (white arrowhead) adjacent to the left gastric artery (white arrow) and a station 8 lymph node (black arrowhead) adjacent to the common hepatic artery (black arrow). The diagnosis of lymph node metastasis may be difficult if only size criteria are used. (b) Axial PET scan shows prominent FDG uptake in the corresponding station 7 (arrowhead) and station 8 (arrow) lymph nodes, a finding that suggests metastasis. Lymph node metastasis was proved at pathologic analysis.
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Figure 4b. Station 7 and 8 lymph node metastases in a 63-year-old man with stomach cancer. (a) Axial CT scan demonstrates a station 7 lymph node (white arrowhead) adjacent to the left gastric artery (white arrow) and a station 8 lymph node (black arrowhead) adjacent to the common hepatic artery (black arrow). The diagnosis of lymph node metastasis may be difficult if only size criteria are used. (b) Axial PET scan shows prominent FDG uptake in the corresponding station 7 (arrowhead) and station 8 (arrow) lymph nodes, a finding that suggests metastasis. Lymph node metastasis was proved at pathologic analysis.
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Figure 5a. Station 12 lymph node metastases in a 65-year-old man with stomach cancer. (a) Axial CT scan demonstrates an enlarged lymph node (arrowhead) in the hepatoduodenal ligament adjacent to the proper hepatic artery (arrow). (b, c) Axial (b) and coronal (c) PET scans show the lymph node (arrow) with increased FDG uptake.
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Figure 5b. Station 12 lymph node metastases in a 65-year-old man with stomach cancer. (a) Axial CT scan demonstrates an enlarged lymph node (arrowhead) in the hepatoduodenal ligament adjacent to the proper hepatic artery (arrow). (b, c) Axial (b) and coronal (c) PET scans show the lymph node (arrow) with increased FDG uptake.
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Figure 5c. Station 12 lymph node metastases in a 65-year-old man with stomach cancer. (a) Axial CT scan demonstrates an enlarged lymph node (arrowhead) in the hepatoduodenal ligament adjacent to the proper hepatic artery (arrow). (b, c) Axial (b) and coronal (c) PET scans show the lymph node (arrow) with increased FDG uptake.
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Figure 6a. Multiple station 13 and 14 lymph node metastases in a 52-year-old man with stomach cancer. (a) Axial CT scan demonstrates conglomerated station 13 lymph node metastases (black arrowheads) on the posterior surface of the pancreatic head (black arrow) and station 14 metastasis (white arrowheads) along the superior mesenteric vessel (white arrow). (b, c) Axial (b) and coronal (c) PET scans show prominent FDG uptake in the corresponding station 13 (black arrowheads in b, black arrow in c) and station 14 (white arrowheads in b, white arrow in c) lymph nodes.
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Figure 6b. Multiple station 13 and 14 lymph node metastases in a 52-year-old man with stomach cancer. (a) Axial CT scan demonstrates conglomerated station 13 lymph node metastases (black arrowheads) on the posterior surface of the pancreatic head (black arrow) and station 14 metastasis (white arrowheads) along the superior mesenteric vessel (white arrow). (b, c) Axial (b) and coronal (c) PET scans show prominent FDG uptake in the corresponding station 13 (black arrowheads in b, black arrow in c) and station 14 (white arrowheads in b, white arrow in c) lymph nodes.
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Figure 6c. Multiple station 13 and 14 lymph node metastases in a 52-year-old man with stomach cancer. (a) Axial CT scan demonstrates conglomerated station 13 lymph node metastases (black arrowheads) on the posterior surface of the pancreatic head (black arrow) and station 14 metastasis (white arrowheads) along the superior mesenteric vessel (white arrow). (b, c) Axial (b) and coronal (c) PET scans show prominent FDG uptake in the corresponding station 13 (black arrowheads in b, black arrow in c) and station 14 (white arrowheads in b, white arrow in c) lymph nodes.
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Figure 7a. Station 16 lymph node metastasis in a 55-year-old man with stomach cancer. (a) Coronal reformatted CT image demonstrates a necrotic enlarged lymph node (arrow) around the abdominal aorta. (b) Coronal PET scan shows the lymph node (arrow) with increased FDG uptake.
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Figure 7b. Station 16 lymph node metastasis in a 55-year-old man with stomach cancer. (a) Coronal reformatted CT image demonstrates a necrotic enlarged lymph node (arrow) around the abdominal aorta. (b) Coronal PET scan shows the lymph node (arrow) with increased FDG uptake.
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D1 lymphadenectomy involves the dissection of perigastric nodes attached directly to the stomach (compartment I), whereas D2 lymphadenectomy involves complete dissection of compartments I and II. The latter is the standard surgical procedure for gastric cancer in high-prevalence countries, such as Korea and Japan. D3 lymphadenectomy involves compartments I–III, whereas D4 lymphadenectomy involves dissection of all four compartments. In addition, the regional lymph nodes of stations 12p–16 are classified as distant metastases (M1) according to the new AJCC classification system. Therefore, detailed anatomic nodal descriptions based on lymph node location remain a significant component of preoperative nodal staging.
At CT, positive nodes are identified on the basis of size, shape, and enhancement pattern (ie, more than 8–10 mm along the short axis, nearly round shape, central necrosis, and marked or heterogeneous enhancement) (29–31). There is a strong correlation between the existence of metastatic nodal involvement and these criteria. In addition, CT can provide anatomic information about metastatic nodes (Figs 3, 4a, 5a, 6a, 7a; Table). Nodal assessment of compartments III and IV is particularly important because the metastatic nodes of stations 12p–16 (M1 nodes) cannot be removed with routine D2 dissection. Metastatic nodal involvement of these distant areas may be detected and localized with CT. However, CT has a major limitation in that it cannot help detect cancerous involvement of normal-size nodes and cannot help distinguish between reactive hyperplasia and metastatic enlargement.
FDG PET, which has the capacity to show changes in metabolism, could conceivably be used to overcome this limitation of anatomic imaging. However, PET is less sensitive than CT in the detection of lymph node metastasis in compartments I and II, mainly due to its poor spatial resolution, which makes it unhelpful in discriminating between lymph nodes and the primary tumor (32). However, the presence of metastatic perigastric lymph nodes may not be important in planning surgical extent, since these nodes would be removed at the time of surgery.
Detection of lymph node metastases in compartments III and IV can change the extent of lymph node dissection or may preclude unnecessary surgery. Metastases at these sites would theoretically be easier to identify at PET because they are located away from the primary lesion (Figs 5b, 5c, 6b, 6c, 7b). In other words, the relatively low spatial resolution of PET does not adversely affect the detection of these metastases because they are remote from the primary tumor or from areas of intense FDG uptake. To our knowledge, there has been no published report about the efficacy of PET in the diagnosis of these distant lymph node metastases. Lymph node assessment for metastatic spread remains a challenge with PET.
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Metastasis Staging
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Solid Organ Metastasis
Solid organ metastasis is uncommon in primary gastric cancers at the time of initial diagnosis, but its detection is important in treatment planning. Hematogenous metastases from gastric carcinoma most commonly involve the liver because the stomach is drained by the portal vein (Figs 8, 9) (3,6). Other less common sites of hematogenous spread include the lungs, adrenal glands, and skeleton. In the case of ovarian metastasis (Krukenberg tumor) (Fig 10), three possible pathways have been considered: peritoneal dissemination, lymphatic spread, and hematogenous spread (33).
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Figure 8a. Multiple hepatic metastases in a 58-year-old man with stomach cancer. (a) Portal venous phase CT scan shows multiple metastatic nodules in both hepatic lobes. (b) Axial PET scan shows multiple nodules with prominent FDG uptake in the liver.
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Figure 8b. Multiple hepatic metastases in a 58-year-old man with stomach cancer. (a) Portal venous phase CT scan shows multiple metastatic nodules in both hepatic lobes. (b) Axial PET scan shows multiple nodules with prominent FDG uptake in the liver.
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Figure 9a. Small hepatic metastases in a 54-year-old man with stomach cancer. (a) Portal venous phase CT scans show four metastatic nodules (arrowheads), none of which is easily discernible. (b) Axial PET scans more clearly depict the nodules (arrowheads). (c) Axial superparamagnetic iron oxide–enhanced gradient-recalled echo T2*-weighted magnetic resonance images (repetition time msec/echo time msec = 120/10, 30° flip angle) help confirm the presence of all four metastatic nodules (arrowheads).
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Figure 9b. Small hepatic metastases in a 54-year-old man with stomach cancer. (a) Portal venous phase CT scans show four metastatic nodules (arrowheads), none of which is easily discernible. (b) Axial PET scans more clearly depict the nodules (arrowheads). (c) Axial superparamagnetic iron oxide–enhanced gradient-recalled echo T2*-weighted magnetic resonance images (repetition time msec/echo time msec = 120/10, 30° flip angle) help confirm the presence of all four metastatic nodules (arrowheads).
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Figure 9c. Small hepatic metastases in a 54-year-old man with stomach cancer. (a) Portal venous phase CT scans show four metastatic nodules (arrowheads), none of which is easily discernible. (b) Axial PET scans more clearly depict the nodules (arrowheads). (c) Axial superparamagnetic iron oxide–enhanced gradient-recalled echo T2*-weighted magnetic resonance images (repetition time msec/echo time msec = 120/10, 30° flip angle) help confirm the presence of all four metastatic nodules (arrowheads).
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Figure 10a. Krukenberg tumor in a 34-year-old woman with stomach cancer. (a) CT scan shows a mixed cystic-solid tumor (arrows) in the pelvis. (b) Axial PET scan demonstrates the tumor (arrows) with increased FDG uptake. Metastatic involvement of the ovary was proved at histologic analysis of the gross specimen.
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Figure 10b. Krukenberg tumor in a 34-year-old woman with stomach cancer. (a) CT scan shows a mixed cystic-solid tumor (arrows) in the pelvis. (b) Axial PET scan demonstrates the tumor (arrows) with increased FDG uptake. Metastatic involvement of the ovary was proved at histologic analysis of the gross specimen.
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Because metastatic hepatic lesions are usually hypovascular, the optimal CT strategy is helical scanning during the portal venous phase of enhancement (Fig 8a). This technique improves lesion conspicuity by increasing the attenuation of normal liver tissue (34). Occasionally, rim enhancement of a hypoattenuating metastasis can be seen. Krukenberg tumors are often large and bilateral and manifest as adnexal solid masses with heterogeneous contrast material enhancement (Fig 10a) (3).
The major advantage of FDG PET over anatomic imaging modalities is its capacity to help detect distant solid organ metastases. Metastases to the liver, lungs, adrenal glands, and ovaries can be readily identified at FDG PET. A recent meta-analysis by Kinkel et al (35) showed that FDG PET is the most sensitive noninvasive imaging modality for the diagnosis of hepatic metastases from colorectal, gastric, and esophageal cancers.
Theoretically, a small liver metastasis may be missed at CT but well seen at FDG PET, with its high target-to-background ratio (Fig 9b). Another advantage of PET is the ability to scan a larger volume (generally from skull base to pelvis with whole-body PET) than is possible with routine abdominopelvic CT.
Distant Lymph Node Metastasis
In the staging of gastric cancer, involvement of the supraclavicular lymph nodes, compartment III lymph nodes, and compartment IV lymph nodes is considered distant metastasis rather than nodal metastasis and precludes curative surgery.
Routine abdominopelvic CT can help localize significantly enlarged lymph nodes in compartments III and IV (Figs 5a, 6a, 7a). However, as mentioned earlier, CT cannot help detect cancerous involvement of normal-size nodes or help distinguish between reactive hyperplasia and metastatic enlargement. Furthermore, extraabdominal lymph node metastasis cannot be evaluated with abdominopelvic CT.
The more significant metastases in compartments III and IV (ie, remote from the primary tumor) may be easily detected with PET (Figs 5b, 5c, 6b, 6c, 7b). Extraabdominal lymph node metastasis can also be detected with PET, which allows whole-body imaging (Fig 11). Furthermore, as was said earlier, the relatively low spatial resolution of PET does not adversely affect the detection of these metastatic lesions because they are remote from the primary lesion.
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Figure 11a. Supraclavicular lymph node metastasis in a 44-year-old woman with stomach cancer. (a) Chest CT scan shows bilateral supraclavicular lymph nodes (arrows) less than 1 cm in diameter. (b, c) Axial (b) and coronal (c) PET scans show the lymph nodes (arrows) with increased FDG uptake. Metastatic involvement was confirmed at needle aspiration biopsy.
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Figure 11b. Supraclavicular lymph node metastasis in a 44-year-old woman with stomach cancer. (a) Chest CT scan shows bilateral supraclavicular lymph nodes (arrows) less than 1 cm in diameter. (b, c) Axial (b) and coronal (c) PET scans show the lymph nodes (arrows) with increased FDG uptake. Metastatic involvement was confirmed at needle aspiration biopsy.
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Figure 11c. Supraclavicular lymph node metastasis in a 44-year-old woman with stomach cancer. (a) Chest CT scan shows bilateral supraclavicular lymph nodes (arrows) less than 1 cm in diameter. (b, c) Axial (b) and coronal (c) PET scans show the lymph nodes (arrows) with increased FDG uptake. Metastatic involvement was confirmed at needle aspiration biopsy.
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Peritoneal Metastasis
Peritoneal metastasis is an extremely unfavorable prognostic factor. The existence of peritoneal metastases implies that the disease is incurable. Pre-operative knowledge of peritoneal metastasis in patients with gastric adenocarcinoma is important in planning the surgical procedure. Such knowledge allows the surgeon to decide whether surgery is likely to be potentially curative or palliative in nature and to avoid performing an unnecessary laparotomy.
CT remains the modality of choice for the pre-operative diagnosis of peritoneal carcinomatosis. However, peritoneal carcinomatosis is often detected only intraoperatively because of the limited capability of CT (36). However, the recent advent of a new scanning technique that makes use of thin-section collimation and multiplanar reformation may improve the detection of peritoneal metastasis.
Ascites is one of the most common findings with these tumors. Other CT findings accompanying peritoneal metastasis include a nodular, plaque-like or infiltrative soft-tissue lesion in the peritoneal fat or on the peritoneal surface; parietal peritoneal thickening or enhancement; and small bowel wall thickening or distortion (Figs 12a, 13a, 14a, 14b, ) (37,38).
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Figure 12a. Peritoneal metastasis in a 38-year-old man with stomach cancer. (a) CT scan shows small metastatic nodules in the omentum (arrows) and enhanced peritoneal thickening (arrowheads). Peritoneal metastasis was confirmed at histologic analysis of ascitic fluid obtained with fine-needle aspiration. (b) Coronal PET scan shows diffuse FDG uptake throughout the entire abdomen and pelvis. The uptake obscures normal, discrete visceral outlines (arrows).
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Figure 12b. Peritoneal metastasis in a 38-year-old man with stomach cancer. (a) CT scan shows small metastatic nodules in the omentum (arrows) and enhanced peritoneal thickening (arrowheads). Peritoneal metastasis was confirmed at histologic analysis of ascitic fluid obtained with fine-needle aspiration. (b) Coronal PET scan shows diffuse FDG uptake throughout the entire abdomen and pelvis. The uptake obscures normal, discrete visceral outlines (arrows).
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Figure 13a. Peritoneal metastasis in a 34-year-old woman with stomach cancer. (a) Axial contrast material–enhanced CT scan shows a peritoneal implant (arrows) in the left pelvic peritoneum. (b) Axial PET scan shows a discrete focus of increased FDG uptake (arrow) in the same location.
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Figure 13b. Peritoneal metastasis in a 34-year-old woman with stomach cancer. (a) Axial contrast material–enhanced CT scan shows a peritoneal implant (arrows) in the left pelvic peritoneum. (b) Axial PET scan shows a discrete focus of increased FDG uptake (arrow) in the same location.
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Figure 14a. Peritoneal metastasis from poorly differentiated adenocarcinoma (confirmed at endoscopic biopsy) in a 59-year-old man with stomach cancer. (a) Coronal reformatted CT image shows omental infiltration (arrows). (b) Coronal reformatted CT image demonstrates ascitic fluid (*) and parietal peritoneal thickening (arrows), findings that suggest peritoneal metastasis. (c) Coronal PET scan demonstrates slightly increased bowel uptake in the abdomen without obscuration of visceral outlines. Differentiation between normal physiologic bowel uptake and tumor seeding is difficult.
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Figure 14b. Peritoneal metastasis from poorly differentiated adenocarcinoma (confirmed at endoscopic biopsy) in a 59-year-old man with stomach cancer. (a) Coronal reformatted CT image shows omental infiltration (arrows). (b) Coronal reformatted CT image demonstrates ascitic fluid (*) and parietal peritoneal thickening (arrows), findings that suggest peritoneal metastasis. (c) Coronal PET scan demonstrates slightly increased bowel uptake in the abdomen without obscuration of visceral outlines. Differentiation between normal physiologic bowel uptake and tumor seeding is difficult.
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Figure 14c. Peritoneal metastasis from poorly differentiated adenocarcinoma (confirmed at endoscopic biopsy) in a 59-year-old man with stomach cancer. (a) Coronal reformatted CT image shows omental infiltration (arrows). (b) Coronal reformatted CT image demonstrates ascitic fluid (*) and parietal peritoneal thickening (arrows), findings that suggest peritoneal metastasis. (c) Coronal PET scan demonstrates slightly increased bowel uptake in the abdomen without obscuration of visceral outlines. Differentiation between normal physiologic bowel uptake and tumor seeding is difficult.
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The use of CT in the identification of peritoneal metastases is limited by its varying sensitivities, which depend on factors such as (a) the size, location, and morphologic features of the tumor deposit; (b) the presence of ascites; (c) the paucity of intraabdominal fat; and (d) the adequacy of bowel enhancement (39,40). A few studies have reported that FDG PET has greater sensitivity than CT in the evaluation of peritoneal carcinomatosis in various abdominal malignancies (41–43). Two patterns of FDG uptake are known to be indicators of peritoneal metastasis: (a) diffuse uptake spreading uniformly throughout the abdomen and pelvis, obscuring visceral outlines (normal serpiginous pattern of the large and small bowel and physiologic hepatic and splenic uptake) (Fig 12b) (43,44); and (b) discrete foci of uptake located randomly and anteriorly within the abdomen or dependently within the pelvis and unrelated to solid viscera or nodal stations (Fig 13b) (43). However, the utility of PET has remained controversial. Small peritoneal seeding nodules may be missed due to the low resolution of PET. In addition, FDG uptake by gastric cancers varies depending on cell differentiation. Several investigators have reported that mucinous and signet ring cell carcinomas, as well as poorly differentiated adenocarcinomas, showed significantly less FDG uptake than did other histologic types of gastric cancer (22,23). The same pattern might be expected with peritoneal metastasis (Fig 14c).
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Recurrent Disease and Evaluation of Response to Therapy
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Although tumor recurrence has a poor prognosis (6), early identification is helpful because it may allow patients with minimal adenopathy or small recurrent masses to respond better to chemotherapy or radiation therapy (45). The routes of spread of recurrent disease are thought to include contiguous invasion, lymphatic spread, hematogenous spread, and peritoneal dissemination.
CT is the primary tool for the investigation of suspected recurrence due to its widespread availability and relatively low cost (Figs 15a , 16a). However, CT often cannot help differentiate treatment-induced morphologic changes from tumor recurrence (Fig 15a). Recurrence at the gastric stump or anastomosis manifests as non-specific localized bowel wall thickening at CT. Potential sources of erroneous interpretation include improperly distended bowel loops, surgical plication, bowel adhesion, and reflux gastritis (34). Furthermore, response to treatment is evaluated on the basis of size measurements obtained with CT, which are potentially inaccurate or impossible to obtain because most of the gastric tumor is not measurable.
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Figure 15a. Local tumor recurrence following subtotal gastrectomy in a 63-year-old man. (a) Axial contrast-enhanced CT scan shows mild gastric wall thickening (arrows) at an anastomotic site. This finding was misinterpreted as a postoperative change (possibly plication-induced fibrotic change or reflux gastritis). (b) Axial PET scan shows prominent increased FDG uptake (arrows) in the anastomotic site. Cancer recurrence was proved at histologic analysis of tissue obtained at endoscopic biopsy.
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Figure 15b. Local tumor recurrence following subtotal gastrectomy in a 63-year-old man. (a) Axial contrast-enhanced CT scan shows mild gastric wall thickening (arrows) at an anastomotic site. This finding was misinterpreted as a postoperative change (possibly plication-induced fibrotic change or reflux gastritis). (b) Axial PET scan shows prominent increased FDG uptake (arrows) in the anastomotic site. Cancer recurrence was proved at histologic analysis of tissue obtained at endoscopic biopsy.
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Figure 16a. Suspected tumor recurrence in a 44-year-old woman with stomach cancer. (a, b) Axial contrast-enhanced CT scan (a) and PET scan (b) obtained prior to chemotherapy show prominent diffuse gastric wall thickening (arrows in a) with prominent FDG uptake (arrow in b). (c) Follow-up PET scan obtained approximately 5 months after chemotherapy shows markedly decreased FDG uptake in the stomach (arrow). (d) Follow-up CT scan obtained 3 months later demonstrates obstruction of a pyloric stent (arrow), a finding that suggests residual tumor. A radical subtotal gastrectomy was performed for palliation, but no residual tumor was detected in the resected specimen.
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Figure 16b. Suspected tumor recurrence in a 44-year-old woman with stomach cancer. (a, b) Axial contrast-enhanced CT scan (a) and PET scan (b) obtained prior to chemotherapy show prominent diffuse gastric wall thickening (arrows in a) with prominent FDG uptake (arrow in b). (c) Follow-up PET scan obtained approximately 5 months after chemotherapy shows markedly decreased FDG uptake in the stomach (arrow). (d) Follow-up CT scan obtained 3 months later demonstrates obstruction of a pyloric stent (arrow), a finding that suggests residual tumor. A radical subtotal gastrectomy was performed for palliation, but no residual tumor was detected in the resected specimen.
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Figure 16c. Suspected tumor recurrence in a 44-year-old woman with stomach cancer. (a, b) Axial contrast-enhanced CT scan (a) and PET scan (b) obtained prior to chemotherapy show prominent diffuse gastric wall thickening (arrows in a) with prominent FDG uptake (arrow in b). (c) Follow-up PET scan obtained approximately 5 months after chemotherapy shows markedly decreased FDG uptake in the stomach (arrow). (d) Follow-up CT scan obtained 3 months later demonstrates obstruction of a pyloric stent (arrow), a finding that suggests residual tumor. A radical subtotal gastrectomy was performed for palliation, but no residual tumor was detected in the resected specimen.
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Figure 16d. Suspected tumor recurrence in a 44-year-old woman with stomach cancer. (a, b) Axial contrast-enhanced CT scan (a) and PET scan (b) obtained prior to chemotherapy show prominent diffuse gastric wall thickening (arrows in a) with prominent FDG uptake (arrow in b). (c) Follow-up PET scan obtained approximately 5 months after chemotherapy shows markedly decreased FDG uptake in the stomach (arrow). (d) Follow-up CT scan obtained 3 months later demonstrates obstruction of a pyloric stent (arrow), a finding that suggests residual tumor. A radical subtotal gastrectomy was performed for palliation, but no residual tumor was detected in the resected specimen.
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FDG PET delineates the glucose metabolism of tissue, which is commonly elevated in tumor and low in scar tissue (Fig 15b). Thus, equivocal CT findings that are suggestive of tumor recurrence can be accurately characterized with FDG PET. However, PET may be limited in screening for recurrent tumors because of low FDG uptake in signet ring cell carcinoma and mucinous carcinoma, lack of adequate spatial resolution for the detection of small peritoneal nodules, and marked variability among patients in terms of physiologic peritoneal uptake (46).
It is hoped that response to treatment will be apparent much earlier at PET than at CT, allowing early changes in treatment for unresponsive tumors. Several recent reports involving patients with gastric cancer have demonstrated that response to preoperative chemotherapy can be predicted with FDG PET early in the course of therapy (Fig 16b, 16c) (47,48). Promising results have also been shown in studies of patients with various other tumors (49,50).
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Conclusions
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In the past, CT has been the imaging modality of choice for the preoperative staging of gastric cancer and the follow-up of affected patients. However, FDG PET may be superior to anatomic imaging modalities in the detection of distant metastases and significant nodal metastases. In addition, FDG PET may play a valuable role in monitoring response to therapy in patients who undergo surgery or chemotherapy. Therefore, the combined use of CT and PET can be helpful in preoperative staging and therapeutic monitoring in patients with stomach cancer.
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Footnotes
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Abbreviations: AJCC = American Joint Committee on Cancer, FDG = 2-[fluorine-18]fluoro-2-deoxy-D-glucose
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References
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- Whelan SL, Parkin DM, Masuyer E, eds. Trends in cancer incidence and mortality. Lyon, France: IARC Scientific Publications, 1993.
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Abstract
Introduction
