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 Table of Contents  
Year : 2021  |  Volume : 5  |  Issue : 2  |  Page : 196-202

The Contribution of [18]F-fluoro-2-deoxy-glucose positron emission tomography/computed tomography to the diagnosis and staging of signet-ring cell carcinoma of the stomach

1 Department of Nuclear Medicine, Private Gaziosmanpasa Hospital, Istanbul Yeni Yüzyil University, Istanbul, Turkey
2 Clinic of Nuclear Medicine, University of Health and Sciences, Istanbul Training and Research Hospital, Istanbul, Turkey

Date of Submission17-Apr-2021
Date of Acceptance01-May-2021
Date of Web Publication16-Jun-2021

Correspondence Address:
Esra Arslan
Istanbul Egitim ve Arastırma Hastanesi, Nukleer Tıp Kliniği, Org. Nafiz Gurman Caddesi, Samatya, Kocamustafapasa, Fatih, Istanbul
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/bbrj.bbrj_60_21

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Background: Signet ring cell carcinomas (SRCC) have been among the most common histological types of gastric cancer. In recent years, [18]F-fluoro-2-deoxy-glucose positron emission tomography/computed tomography ([18]F-FDG-PET/CT) has been very useful for primary cancer staging and distant metastasis detection. In our study, the aim was to evaluate the diagnostic and predictive level of [18]F-FDG-PET/CT in SRCC. Methods: Ninetytwo patients that underwent [18]F-FDG-PET/CT procedures between 2011 and 2017 for primary staging were included in the study. The clinicopathological features and maximum standard uptake value (SUVmax) of histopathologically defined cancers were determined. Ethical approval was obtained from Istanbul Training and Research Hospital Local Ethics Committee with the date and number 04/08/2017-1048. Results: The mean age of the patients was 58.1 ± 12.2 years. Sixtythree of the patients (75.3%) were male and 29 (24.7%) were female. According to the histopathological classification, the majority of the SRCCs were poorly differentiated and were most frequently localized in the middle and lower parts of the stomach. The mean value of [18]F-FDG uptake by [18]F-FDG-PET/CT in the primary lesions was SUVmax = 9.69 ± 7.58. The mean SUVmax (SUVmax: 7.92) measured in the patient group, 60 years and older, was found to be statistically significantly higher (p = 0.038) than the value measured in the 59 years and younger group (SUVmax: 10.26). There was a statistically significant difference between the mean SUVmax of the patients aged 60 and over and under this age group (p = 0.038). A statistically significant difference was found between the group with a positive regional LN and the mean SUVmax calculated between the group with negative regional LN (p = 0.012). A statistically significant difference was found between the group with distant organ metastasis and the negative group (p = 0.008). However, no statistically significant difference was found between tumor diameter, tumor wall thickness, localization of the tumor in the stomach, presence of distant nodal metastasis, and SUVmax calculated for histological gradients of the lesions (p > 0.05). Conclusion: Due to the advances in the diagnosis and treatment of SRCC in recent years, PET/CT may contribute to the diagnosis, staging, and prognosis determination of patients. [18]F-FDG-PET/CT demonstrated high FDG uptake in SRCC lesions. The FDG SUVmax was observed to increase significantly in patients with SRCC diagnosis of regional LN and distant organ metastasis. Studies with larger patient groups are needed to detect locally advanced and metastatic cases in SRCC patients using [18]F-FDG-PET/CT.

Keywords: [18]F-fluoro-2-deoxy-glucose positron emission tomography/computed tomography, gastric cancer, signet-ring cell carcinomas

How to cite this article:
Tatar SY, Arslan E. The Contribution of [18]F-fluoro-2-deoxy-glucose positron emission tomography/computed tomography to the diagnosis and staging of signet-ring cell carcinoma of the stomach. Biomed Biotechnol Res J 2021;5:196-202

How to cite this URL:
Tatar SY, Arslan E. The Contribution of [18]F-fluoro-2-deoxy-glucose positron emission tomography/computed tomography to the diagnosis and staging of signet-ring cell carcinoma of the stomach. Biomed Biotechnol Res J [serial online] 2021 [cited 2022 Dec 9];5:196-202. Available from: https://www.bmbtrj.org/text.asp?2021/5/2/196/318436

  Background Top

Gastric cancer (GC) is the second most common cause of cancer-related deaths in the world. It is characterized with a poor prognosis and high mortality. Given the manifestation of late symptoms, it is frequently diagnosed at an advanced stage. Surrounding tissue invasion is an indicator of poor prognosis. In patients with distant organ metastasis, the 3-year survival is 8%, while the 5-year survival is 0%. This type of cancer is widespread throughout the world, especially in the young population in Eastern Europe, South Asia, and America.[1] Signet ring cell carcinomas (SRCC) are among the most common histological types of GC. In this cancer type, mortality decreases substantially with early diagnosis, early treatment, and follow-up. With early diagnosis, the 5-year survival rate increases up to 80%. However, many patients are diagnosed after the initiation of lymph node (LN) metastasis. Different diagnostic methods are emphasized for earlier diagnosis.[1],[2],[3],[4]

Thoracoabdominal computed tomography, endoscopy, endoscopic ultrasonography, and tumor markers are commonly used for the diagnosis and post-treatment follow-up of gastric tumors.[5] In addition to the late diagnosis of GC, one of the most important reasons affecting treatment failure is the development of recurrence in patients who are followed up. These relapses are overlooked and patients die as a result of metastasis. In addition, obtaining false-negative results in applied diagnosis and staging methods is another drawback.[5],[6] Furthermore, it is difficult to detect tumor recurrence and metastasis with these methods.[5] For this reason, accurate staging of the tumor with a good technical method in combination with follow-up is important. One of these methods, [18]F-fluoro-2-deoxy-glucose positron emission tomography/computed tomography ([18]F-FDG-PET/CT), has recently been used in the preoperative diagnosis, staging, treatment-related changes, and treatment responses in many cancer types. It is a useful method for planning radiotherapy, determining chemosensitivity, and distant metastasis. With this method, beneficial results have been obtained following the identification of tumoral tissue development in many parts of the body.

[18]F-FDG-PET/CT is based on the principle finding that malignant cells have increased glucose uptake and utilization, which can be metabolically monitored. Tumor size increase and aggressiveness have been associated with the increase in glucose uptake of tumor cells.[5],[7],[8] Different results have been obtained in studies using [18]F-FDG-PET/CT in the diagnosis and follow-up of gastric tumors. Some studies indicate that this method is more successful in restaging GCs and detecting recurrences, while other studies have reported the ability of early cancer detection. Data on SRCC, which is characterized with a worse prognosis than the other types among gastric tumors, is limited.[4],[5],[8] In our study, the use of [18]F-FDG-PET/CT was investigated to determine the diagnostic/predictive value in SRCC.

  Methods Top


Ninety-two patients with SRCC were admitted to two different Clinics of Nuclear Medicine between 2011 and 2017 and included in the study.

Positron emission tomography/computed tomography imaging

Patients whom blood glucose levels lower than 150 mg/dL after at least 6 h of fasting were admitted for the [18]F-FDG-PET/CT procedure. Standard 3.7–5.2 MBq/kg (0.1–0.2 mCi/kg) 18F-FDG intravenous injection was administered to the patients. Fortyfive-sixty minutes after injection of 18F-FDG, whole-body PET/CT imaging was obtained including the area from vertex to the upper femur at the supine position by mCT 20 ultra HD LSO PET/CT, (Siemens molecular imaging, Hoffmann Estates, Illinois, USA). The [18]F-FDG-PET/CT technique was implemented for cancer primary staging of the patients. The patients were classified as Group 1: Over 60 years old and Group 2: 59 years and younger.

Histopathological diagnosis

Sixty-six (71.7%) of the samples were obtained by endoscopic biopsy and 21 (22.8%) from gastrectomy samples. The clinicopathological features of the histopathologically defined cancer and the maximum standard uptake value (SUVmax) were compared. The mean SUVmax values were compared by dividing the tumor into two groups; smaller than 3 cm and >3 cm in diameter.

Ethics approval

Ethical approval was obtained from the Local Ethics Committee with the date and number 04/08/2017-1048.


For statistical evaluations, the Chi-square test and Fischer's exact tests were used in Statistical Package for the Social Sciences (SPSS) Version 15.0 (SPSS,IBM Company, Chicago, Illinois) commercial software. A P < 0.05 was considered statistically significant.

  Results Top

Positron emission tomography/computed tomography results in staging and demographic characteristics of the patients

Of the patients included in the study and diagnosed with SRCC, 63 (75.3%) were male and 29 (24.7%) were female. The mean age of the patients was 58.1 ± 12.2 years. The majority of the patients were between the ages of 50–70 years. There was no statistically significant difference in the comparison of the mean age of the patients by gender (P > 0.05) [Table 1].
Table 1: Distribution of patients by gender and decades

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The majority of the SRCCs was poorly differentiated, some moderately, and very few highly differentiated according to histopathological classification. Although SRCC was detected in all areas of the stomach, it was typically localized in the middle and lower parts of the stomach [Table 2].
Table 2: Distribution of lesions according to gastric localization

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SUVmax = 9.69 ± 7.58 [18]FDG uptake value was determined along with [18]F-FDG-PET/CT in primary lesions. The mean SUVmax (SUVmax: 7.92) measured in Group 1 (60 years and older [n = 44]) was 47.8% compared to 42.4% in Group 2 (59 years and below [n = 39]) with a SUVmax: 10.26 (P = 0.038).

The mean total tumor diameter was measured to be 6.25 ± 2.84. Tumor diameters were divided into two groups: <3 cm (26%) and >3 cm (74%). There was no statistically significant difference between the mean SUVmax of the two groups (P = 0.735). The mean total gastric wall thickness of the patients was found to be 3.0 ± 2.29 cm. No statistically significant correlation was found between gastric wall thickness and primary lesion mean SUVmax (r = 0.100, P = 0.735). When [18]F-FDG uptake was evaluated according to the location of the lesions in the stomach, no statistically significant difference was observed between these locations (P = 0.284). Histological grading of the lesions and the change in the primary lesion SUVmax values were not statistically significant (P = 0.946) [Table 3].
Table 3: Locations with detected pathology in positron emission tomography/computed tomography and average standard uptake value maximum values

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The mean number of LNs dissected was 30.97 ± 13.8. In cases with LN involvement, the mean axial diameter of the LN was determined to be 1.47 ± 0.99 cm. Regional LN (RLN) involvement was found to be positive in 67.4% of the lesions in total following the [18]F-FDG-PET/CT scan analysis. When RNL [18]F-FDG uptake was examined, the mean RNL SUVmax was found to be 5.7628 ± 7.10. The mean SUVmax calculated in the RLN positive group was found to be statistically significantly higher (P = 0.012) than the mean SUVmax calculated in the RLN negative group. The measured mean distant nodal metastasis LN diameter in patients with distant nodal metastasis was determined as 1.47 ± 0.67 cm. When [18]F-FDG involvement was examined for distant nodal metastasis in cases, the mean SUVmax of distant nodal metastasis was found to be 9.25 ± 9.34. Distant nodal metastasis was detected by PET/CT in 16.3% of our patients [Figure 1]; however, the change in primary lesion SUVmax values were not significanlty associated with the presence of distant nodal metastasis (P = 0.061). Distant organ metastasis was detected in 22.8% of our patients [Figure 2]. The mean SUVmax calculated in the group with positive distant metastasis was found to be significantly higher (P = 0.008) than the mean SUVmax value calculated in the negative group. The mean distant organ metastatic SUVmax value was found to be 6.62 ± 6.49 in patients with distant organ metastasis [Table 3].
Figure 1: An example of a nodal metastatic case: A 52-year-old male patient with primary tumor FDG involvement (SUVmax = 9.2) (shown with red arrow). Paraaortic metastatic lymph node (SUVmax = 12) (shown with blue arrow). PET: Positron emission tomography, CT: Computed tomography, F: Fusion, MIP: Maximum intensity projection, SUVmax: Standard uptake value maximum

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Figure 2: An example of a multiple organ metastatic case: A 68-year-old male patient with primary tumor FDG involvement with gastric corpus location (SUVmax = 7.6) (shown with red arrow). Liver metastasis (shown with blue arrow). Multiple bone-bone marrow metastasis (shown with green arrow). PET: Positron emission tomography, CT: Computed tomography, F: Fusion, MIP: Maximum intensity projection, SUVmax: Standard uptake value maximum

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  Discussion Top

GC ranks second among cancer-related deaths. In addition to early diagnosis, the implementation of a useful method for the determination of tumor structures, staging, and treatment follow-up are needed to increase survival and decreases mortality.[1] Recently, [18]FDG-PET/CT has been used successfully as a noninvasive method in the diagnosis, treatment, follow-up and staging of many tumor tissues in the body.[9],[10] Studies on the precision of this method in GCs have not been adequately examined.[4],[11],[12] SRC of the stomach is the second-most common GC and has a poor prognosis. There are few studies on the pre- and post-operative use of [18]FDG-PET/CT method for this type of cancer. Studies indicate that because a mucinous substance is highly secreted in SRCC, the false positivity increases and the sensitivity of [18]FDG-PET/CT method decreases. Therefore, the implementation of [18]FDG-PET/CT method in this cancer type is considered with suspicion. However, opposing information has been garnered about the effectiveness of this method in gastric tumors.[4],[8],[12] Therefore, our study has the potential to shed light on the literature regarding the use of the [18]FDG-PET/CT technique in SRCC.

In the diagnosis of SRCC of the stomach, small lesions as well as errors that may arise from sampling, deep localization of metastases, and proximity to large vessels or organs make tissue sampling difficult. There are also similar limitations in revealing cancer recurrence. The ideal imaging method for early detection of recurrences of these cancers is not well documented. The general accuracy of magnetic resonance imaging (MRI) and CT in tumor detection in gastric tumors varies between 43% and 82%, respectively. They can accurately detect LN involvement in a wide range of 25%–86%. CT is also insufficient to detect the extent of the disease.[13],[14],[15],[16] Ultrrasonography and MRI have been used to detect relapses, but limitations in restaging are well known. Endoscopic examinations cannot detect extraluminal recurrence, and recurrence cannot be localized with tumor markers.[13],[17] In their study, Xu et al. emphasized that patients with negative endoscopy should be re-evaluated with PET/CT.[5] Therefore, more sensitive methods will decrease the mortality of patients and increase survival. In the study of Yeung et al., PET/CT showed 93% sensitivity, 100% specificity, and 95% diagnostic accuracy.[18] These values suggested that the [18]FDG-PET/CT method could be used in the diagnosis, staging, treatment, and follow-up of GC for nodal and systemic metastasis.[10] For the PET/CT method, it has been reported that [18]F-FDG uptake imaging may be low and evaluated as false-negative for some cancer types including signet ring cell carcinoma.[19],[20]

The high value of SUVmax in the [18]FDG-PET/CT method increases the reliability of this method for diagnosis. Pak et al. stated in their study that high SUVmax values gave statistically significant results together with tumor aggressiveness.[8] Lee et al. stated that [18]F-FDG uptake of tumor tissue is an independent and very important prognostic factor.[12] In our study, we found SUVmax = 9.69 ± 7.58 [18]F-FDG uptake in tumor tissue. A few studies for SRCC have reported low SUVmax values and low sensitivity. Pak et al. found the SUVmax value obtained from the patients as 3.8 in their study.[8] Nakamoto et al. found low sensitivity in the implementation of PET for SRCC patients in their study; however, they stated that the number of patients in their study was sufficient. However, they emphasized that it is useful for detecting recurrent GC.[4] Chen et al. reported the SUVmax value as 6.34 in their study on patients with GC.[21] Lee et al. reported the SUVmax value as 7.4 in SRCC patients in their study, which consisted of a large group of patients (preoperative patients).[12] The high SUVmax values found are the main reason why the [18]F-FDG-PET/CT technique is recommended for prognosis prediction of GC, post-surgery, survival determination, and treatment follow-up.[22],[23] The high SUVmax value we found in our study supports the appropriateness of this method for staging patients with SRCC, evaluating their response to treatment, and detecting their recurrence.

In our study, the SUVmax value (SUVmax: 7.92) in the Group 1 was found to be significantly higher (P = 0.038) than the SUVmax value Group 2. Similarly, in the studies of Pak et al., the SUVmax values of the group over 60 years old were found to be higher than those below the age of 60; this data were not statistically significant.[8] In the study of Chen et al., a significant difference was found between two different age groups, similar to our study.[21] The SUVmax values we obtained in our study were higher in this age group than in both studies. The reason for this was that the patients included in the study were diagnosed at an advanced stage and were not diagnosed at an early stage.

In our study, no statistically significant difference was found between tumor diameter, tumor wall thickness, localization of the tumor in the stomach, histological grading of lesions, and SUVmax values (P > 0.05). Although SUVmax values of tumor stage, invasion, depth, and LN invasion determined in the study of Pak et al. were lower than the values in our study, they found it to be statistically significant.[8] Chen et al. reported statistical significance for tumor depth, histological grading, and SUVmax values in their study. The SUVmax value reported in that study was lower than in our study.[21] Özkan et al. emphasized that the use of [18]F-FDG PET/CT method in tumor classification in gastric tumors can be successful. They stated that [18]F-FDG-PET/CT can be used successfully in postoperative and preoperative evaluation of GCs.[24] However, it has been emphasized that [18]F-FDG-PET/CT has limited place in histological grading because it determines the functional status of the tissue.[25] Therefore, National Comprehensive Cancer Network Guidelines recommended the clinical use of this method in advanced tumors and in the postoperative follow-up of patients.[22] Lee et al. in a large-scale study stated that the [18]F-FDG-PET/CT method could be used for the evaluation of preoperative patients based on the results of patients who were followed in their posttreatment prognoses using the [18]F-FDG-PET/CT method; although its place in diagnosis was limited. In the same study, they reported that this method can provide information about patient prognosis while determining the depth of the lesion.[12] The findings we obtained in our study led us to postulate that the location of [18]F-FDG-PET/CT in the tumoral tissue and the depth of the tissue have no significance.

The presence of distant metastasis in GCs provides important information about cancer curability.[26] Dissection of LN metastases, which is an indicator of this, can provide beneficial information when performed together with gastrectomy. Therefore, accurate detection of LN metastasis is important.[10] In our study, the mean SUVmax value in the group with positive LN metastasis was found to be statistically higher (P = 0.012) compared to the negative group. However, the presence of distant nodal metastasis and SUVmax values of the primary lesion did not show a statistically significant relationship (P = 0.061). In previous studies, SUVmax values determined in groups with and without LN metastasis were found to be lower than the values in our study, and no statistically significant relationship was found between the two groups.[8],[19] The [18]F-FDG-PET/CT method is superior in showing LNs compared to other radiological methods because it provides both metabolic and morphological information. The indicator of malignancy in CT is only the size of the LN, whereas in [18]F-FDG-PET/CT, the LN metabolism (related to the [18]F-FDG uptake density of the primary tumor) and size are evaluated together. This provides both metabolic and morphological information. Therefore, it is stated that [18]F-FDGPET/CT performance is good when evaluating LN metastases.[25] Incompatibility in distant and near LN metastases varies according to the number of different differentiated cells in metastases. Therefore, there is generally no correlation between [18]F-FDG uptake densities of LNs and [18]F-FDG uptake intensities of other distant metastases. The diagnostic value of the [18]F-FDG method in LN involvement varies according to the tumor tissue and the initial stage of the disease. This could be the underlying reason for the incompatibility detected in both metastatic tissues in our study. However, this finding is not very important as it cannot contribute to the treatment of patients, because distant metastasis does not have a determining role in surgery. The important aspect is to detect near LN metastases. Studies emphasize that the [18]F-FDG-PET/CT method is quite successful in detecting near LN metastasis.[12],[25] Therefore, the false negativity value of the [18]F-FDG-PET/CT method is quite low, as it shows increased activity involvement in the LN depending on the metabolic density, regardless of the size of the LNs.

Detection of distant organ metastasis in GC is important for the treatment plan.[25] The mean SUVmax value calculated in the group with positive distant metastasis of our patients was found to be statistically significantly higher (P = 0.008) compared to the group with negative distant metastasis. Nakamoto et al. found that the [18]F-FDG-PET/CT method was successful in many parts of the body for detecting metastases and recurrences in gastric tumors (except for some exceptional locations).[4] Kinkel et al. and Lim et al. stated that the most sensitive method in distant organ metastasis is the [18]F-FDG-PET/CT method.[25],[26] Lee et al. stated that patients who were negative for [8]F-FDG intake had almost no relapses compared to the positive group.[12] This information supports our determination of the SUVmax values of our patients with distant organ metastasis, which were higher than the group with no distant organ metastasis. At the same time, this method allows scanning of a large area of the body at the same time. Thus, it is thought that this method can detect small metastases, which may be missed using CT imaging.

Total gastrectomy is preferred for cancers detected in the middle and lower part of the stomach. Cancers developed in this region may cause more recurrence and LN metastasis compared to other parts of the stomach.[10],[13],[14] Most of the SRCC types detected in the patients in our study were poorly differentiated according to the histopathological classification. Tumoral tissue was found most frequently in the middle and lower part of the stomach in most of the patients. Studies have shown that SRCC generally shows low differentiation.[13],[14] In the study of Pak et al., it was determined that the gastric localization of SRCC was mostly in the lower part.[8] Chen et al. reported that they detected stomach cancers in the lower part of the stomach.[21]

In some studies, it was stated that the [18]F-FDG-PET/CT method does not have adequate performance for detecting GCs due to its low sensitivity in detecting tumoral tissue. However, in the study of Pak et al., one of the few studies conducted for SRCC, the use of [18]F-FDG-PET/CT may be useful in determining tumor aggressiveness and prognosis in advanced stage tumors.[8] Nakamoto et al. reported that the use of the [18]F-FDG-PET/CT method in gastric tumors has a high sensitivity and is at least as useful as invasive interventions in diagnosis.[4] Yun et al. stated that this method shows high specificity in detecting recurrences in GC.[13],[14] Lime et al. stated that the best use for [18]F-FDG PET/CT method in re-evaluating local growth and reactivation states would be valuable.[25]

The increase in uptake of [18]F-FDG into cells due to the increased metabolic activity in the tissue, the evaluation of inflammation in the surgical area, and reactive changes in the mediastinal LNs as false-positive results are the missing aspects of the [18]F-FDG PET/CT method.[27]

  Conclusion Top

Advances made in the diagnosis and treatment of SRCC in recent years, the 18F-FDG-PET/CT method may contribute to the diagnosis, staging, and prognosis determination of patients. In our study, we found a high uptake of 18F-FDG in the tumor-detected tissue regions of SRCC patients. We suggest that this method significantly detects regional LN and organ metastases in patients with SRCC, as well as scanning a large part of the body. The use of the 18F-FDG-PET/CT method in the diagnosis of SRCC patients has led to the conclusion that it will be useful for the clinician in determining tumor aggressiveness, particularly in the diagnosis and treatment of patients that will receive surgery and chemotherapy. However, further studies with larger study groups should be conducted in order to obtain safer results in local, advanced or metastatic cases of SRCC with low uptake of 18F-FDG.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

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Conflicts of interest

The authors declare that none of the authors have any competing interests.

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Kieran G Foley, Will Coomer, Bernadette Coles, Kevin M Bradley
The British Journal of Radiology. 2022;
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