Accuracy of Whole-Body Diffusion-Weighted MRI (WB-DWI/MRI) in Diagnosis, Staging and Follow-Up of Gastric Cancer, in Comparison to CT: A Pilot Study.&nbsp;

doi:10.21203/rs.3.rs-99112/v1

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Accuracy of Whole-Body Diffusion-Weighted MRI (WB-DWI/MRI) in Diagnosis, Staging and Follow-Up of Gastric Cancer, in Comparison to CT: A Pilot Study.

https://doi.org/10.21203/rs.3.rs-99112/v1

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published 05 Feb, 2021

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Background: Accurate staging of patients with gastric cancer is necessary for selection of the most appropriate and personalized therapy. Computed Tomography (CT) is currently used as primary staging tool, being widely available with a relatively high accuracy for the detection of parenchymal metastases, but with low sensitivity for the detection of peritoneal metastases. Magnetic resonance imaging (MRI) with diffusion-weighted imaging (DWI) has a very high spatial and contrast resolution, suggesting a higher diagnostic performance in the detection of small peritoneal lesions. The aim of this study was to retrospectively evaluate the added value of whole-body diffusion-weighted MRI (WB-DWI/MRI) to CT for detection of peritoneal carcinomatosis (PC) and distant metastases in the preoperative staging of gastric cancer.

Methods: This retrospective study included thirty-two patients with a suspicion of gastric cancer/recurrence, who underwent WB-DWI/MRI at 1.5 Tesla, in addition to CT of thorax and abdomen. Images were evaluated by two experienced abdominal radiologists in consensus. Histopathology, laparoscopy and/or 1-year follow-up were used as reference standard.

Results: For overall tumor detection (n=32), CT sensitivity, specificity, positive predictive value (PPV) and negative predictive value (NPV) was 83.3%, 100%, 100% and 82.4% respectively. For WB-DWI/MRI these values were 100%, 92.9%, 94.7% and 100%, respectively. For staging (n=18) malignant lymph nodes and metastases, CT had a sensitivity, specificity/ PPV/ NPV of 50%/ 100%/ 100%/ 71.4%, and 15.4%/ 100%/ 100%/ 31.3% respectively. For WB-DWI/MRI, all values were 100%, for both malignant lymph nodes and metastases.

WB-DWI/MRI was significantly better than CT in detecting tumor infiltration of the mesenteric root, serosal involvement of the small bowel and peritoneal metastases for which WB-DWI/MRI was correct in 100% of these cases, CT 0%.

Conclusions: WB-DWI/MRI is highly accurate for diagnosis, staging and follow-up of patients with suspected gastric cancer. These results need to be confirmed in larger studies.

Nuclear Medicine & Medical Imaging

WB-DWI/MRI

diffusion-weighted imaging (DWI)

Magnetic Resonance Imaging (MRI)

Computed Tomography (CT)

stomach neoplasm

neoplasm metastasies

neoplasm Staging

Peritoneal neoplasms

Gastric cancer remains one of the deadliest neoplasms in the world, with a 5-year survival rate of approximately 25% for all stages [1, 2]. Once spread to the peritoneum, the 5-year survival rate drops to less than 5% [3]. Up to 40% of gastric cancer patients develop some degree of peritoneal metastases during the course of their disease [3]. After gastric cancer resection, hematogenous recurrence is most common (54%), with peritoneal disease being the second most common site of recurrence, accountable for around 43 to 45.9% [4, 5]. Other common sites of recurrence are lymph nodes (12%) and locoregional in 22% [4]. Accurate staging of all tumor locations is essential in these gastric cancer patients to select the best treatment with the highest chance of cure. As these patients have a high risk of peritoneal dissemination, an imaging technique that can detect small volume disease is needed.

According to ESMO Guidelines, outlined by Lerut et al [6], local staging with gastroscopy and Endoscopic Ultrasound (EU) should be combined with distant staging by a CT scan of the thorax and abdomen to detect metastases elsewhere in the body [6–8]. Sensitivity of CT for the evaluation of lymph node metastases is variable (62.5%-91.9%) [9], due to the lack of standard criteria for diagnosing metastatic lymph nodes [10]. Size is the most commonly used criterion to define whether or not a lymph node is metastatic. However, short-axis cut-off levels to define a metastatic lymph node vary between different studies from > 5 mm to > 10 mm. Furthermore, large lymph nodes may be inflammatory and small lymph nodes may harbor millimetric tumor metastases [11]. The accuracy of CT in detecting metastatic disease to liver and lung, according to Seevaratnam [12] is high (81%). However, a recent review of four studies revealed rather low and variable sensitivities (14.3–59.1%), with high specificities (93.3–99.8%) [13], questioning its standard use in clinical practice. Moreover, CT estimation of peritoneal cancer spread is far from optimal with a sensitivity of only 28.3% (although with a high specificity of 98.9%) [ 14], due to its limited soft tissue contrast resolution [15, 16].

Limitations of ¹⁸F-Fluoro-deoxyglucose positron emission tomography (FDG-PET/CT) are not only in the assessment of (small) lymph node involvement [17, 18], but also and especially in the estimation of peritoneal cancer spread, most profoundly in small volume disease [19, 20]. Therefore, both CT and PET/CT are not ideal for accurate staging and treatment planning [21].

Diagnostic laparoscopy is recommended for all stage IB-III, potentially resectable gastric cancer patients to exclude (PET/)CT-graphically occult metastatic disease [6–8]. A review of 15 studies reported a variable high laparoscopic sensitivity ranging from 64.3–94% [22] for the detection of peritoneal metastases, which is higher than in CT. However, laparoscopy remains an invasive surgical procedure and only provides information about structures in the peritoneal cavity. Diffusion-weighted magnetic resonance imaging (DWI/MRI) may act as a problem solver in this situation. In DWI, contrast is generated between tissues due to differences in water proton mobility. In highly cellular tissues such as tumors, water diffusion is restricted, resulting in higher signal intensity on DWI with high b values and lower apparent diffusion coefficients (ADC), compared to the normal surrounding tissue, where water molecules can move freely. Due to the high contrast resolution in DWI tumor depiction can significantly be improved, particularly for peritoneal disease [23, 24]. DWI/MRI can be used as a whole body (WB) imaging technique, for evaluation of primary tumor, lymph nodes and metastases in one single, noninvasive examination [25–28]. The aim of this study was to retrospectively evaluate the added value of whole-body diffusion-weighted MRI (WB-DWI/MRI) to CT for detection of peritoneal carcinomatosis (PC) and distant metastases in the preoperative staging of gastric cancer.

Patients

This retrospective study was approved by the institutional review board (Ethical Committee Imelda Hospital Bonheiden). Informed consent was waived. Between November 2015 and April 2019, 32 consecutive patients with suspected primary or recurrent gastric cancer underwent a WB-DWI/MRI, for diagnosis and/or assessment of operability. They all underwent a CT of the thorax and abdomen within 20 days of the MRI.

Computed tomography

Patients received oral contrast (30 ml iodinated contrast agent (Telebrix Gastro, Guerbet), 300 mg/ml, in 900 ml water), during 1 hour prior to a breath-hold CT scan of the thorax and abdomen (Somatom Force, Siemens Medical Systems, Erlangen, Germany). Images were obtained approximately 70s following intravenous iodinated contrast injection (80ml, Xenetix, Guerbet), which is the optimal timing for evaluation of the gastric tumor as well as possible hepatic metastases [10]. Images were acquired in the axial plane, and reconstructed in coronal and sagittal planes (2mm).

The following parameters were used: pitch 0.6, rotation speed 0.5 sec, 1 mm slice thickness, 0 mm slice gap and 0.6 mm collimation. A reference current of 81 mAs (thorax) and 110 mAs (abdomen) was used with automated Care Dose software.

WB-DWI/MRI (table 1)

Patient preparation consisted of drinking one liter of pineapple juice during two hours prior to the examination, to minimize the high signal intensities of the bowel content on the diffusion-weighted images. Antispasmodic medication (butylhyoscine, 20 mg IV) was injected at the start of the examination to decrease bowel movement. All WB-DWI/MRI examinations were performed on a 1.5 Tesla scanner (Aera, Siemens Medical Systems, Erlangen, Germany) with multichannel phased-array surface coils and parallel imaging techniques. Diffusion-weighted images were acquired in the axial plane, free-breathing in four imaging stations (head/neck, thorax, abdomen and pelvis) at b=50 and b=1000 s/mm²(b1000), and reconstructed in the coronal plane from head to femora. Free-breathing coronal single-shot fast spin-echo T2-weighted images were acquired in the four imaging stations. Breath-hold fat-suppressed T1-weighted gradient-echo sequences after the injection of Gadolinium (Dotarem, Guerbet, Roissy, France) were acquired in the axial plane in the four imaging stations and in the coronal plane for the abdomen and pelvis.

Evaluation of imaging

All 32 patients underwent both CT and WB-DWI/MRI. CT and WB-DWI/MRI-examinations were read by two abdominal radiologists (13 years and 20 years of experience in oncological imaging) in consensus, for identification of the primary tumor, possible lymphadenopathies, peritoneal and/or distant metastases. The images were read in a random order, with a time interval of two months between the interpretation of the CT and the MRI. The readers were blinded to the results of the other imaging technique, patient history, surgical and pathological outcome.

At CT, the following criteria were used for metastatic lymph nodes: short axis diameter of >6 mm, roundness, heterogeneous contrast-enhancement and/or central necrosis. Peritoneal metastases were diagnosed in the presence of nodules on the peritoneal surface, mesentery and/or bowel wall, and/or irregular peritoneal and/or serosal thickening with enhancement. In the presence of ascites, irrespective of nodular peritoneal thickening, a suspicion for peritoneal implants was made. Distant metastases were diagnosed in the presence of malignant lesions in the liver, lungs, bones and/or other organs.

At WB-DWI/MRI, the information of b1000 diffusion-weighted images and anatomical sequences were combined. Lymph nodes with markedly higher b1000 signal intensity than the surrounding lymph nodes in combination with round and/or irregular shape and heterogeneous signal on T2 and/or post contrast images, were considered to be malignant. For diagnosing peritoneal and distant metastases the same anatomical criteria were used as in CT, in combination with contrast enhancement and/or high signal at b1000 images, not caused by T2 shine through.

For the selection of the operability of the patients, ESMO guidelines were used. Patients were considered operable in the absence of inaccessible lymph nodes, distant mesenteric, distant peritoneal and/or parenchymal metastases.

Statistical analysis

Sensitivity, specificity, positive predictive value (PPV) and negative predictive value (NPV) of CT and WB-DWI/MRI were calculated for overall tumor detection, staging of malignant lymph nodes and metastases as well as operability assessment. Reference standard for CT and MRI was histopathology, laparoscopy and/or imaging follow-up for at least 1 year. Comparison of CT and MR accuracies was performed using McNemar’s tests, with a p-value 0.05 indicating a statistically significant difference.

Patient and tumor characteristics (table 2)

The study population consisted of 22 men and 10 women, with an age range of 29-85 years. Eighteen patients were diagnosed with gastric cancer (primary cancers n=15, recurrences n=3), all were histopathologically confirmed (adenocarcinoma n=9, adenocarcinoma with signet ring cell differentiation n=9). Two patients had gastritis, 12 had a history of gastric cancer with negative follow-up examinations.

Tumor detection

Of the 15 primary cancers and 3 recurrences, WB-DWI/MRI correctly detected tumor in all these 18 patients. CT was only able to detect 15 of the 18 patients with tumor.
Twelve patients had a history of gastrectomy. CT as well as WB-DWI/MRI showed no disease recurrence. This was confirmed by a negative follow-up for at least 1 year.

Two patients had histopathologically confirmed gastritis. Of these, MRI was correct in 1 patient and wrongly diagnosed 1 patient as having operable gastric cancer. In both patients, CT was negative for tumor presence.

For tumor detection, WB-DWI/MRI had a sensitivity of 100%, specificity of 92.9%, PPV of 94.7% and NPV of 100% (18 TP, 13 TN, 1 FP and 0 FN). The numbers for CT were: 83.3%, 100%, 100% and 82.4% (15 TP, 14 TN, 0 FP and 3 FN), respectively. No significant difference in accuracy was found between WB-DWI/MRI and CT (96.9% vs 90.6%, p=0.32).

Staging of patients with tumor (n=18)

Lymph nodes

Eight patients were diagnosed with adenopathies (locoregional n=5, retroperitoneal n=2, paracardial n=1), 10 without. WB-DWI/MRI was correct in all patients, CT missed lymphadenopathies in 4 patients (locoregional n=3 and paracardial n=1) but correctly interpreted the other patients (sensitivity 50%, specificity 100%, PPV 100%, NPV 71.4%). WB-DWI/MRI accuracy was significantly higher than CT (100% vs 77.8%, p=0.046).

Distant metastases

Thirteen patients were diagnosed with (a combination of different) distant metastases (peritoneal n=13, bone n=2, brain n=1), 5 without. WB-DWI/MRI correctly interpreted all patients (sensitivity, specificity, PPV and NPV 100%). CT suggested possible peritoneal tumor implants in 2 patients, and failed to identify peritoneal metastases in 11 patients and as well as bone metastases in 2 patients (on a per-patient basis: sensitivity 15.4%, specificity 100%, PPV 100%, NPV 31.3% (2 TP, 5 TN, 0 FP, 11 FN), where WB-DWI/MRI was correct. Since the brain is included in the whole body DWI/MRI, 1 patient with brain metastases was detected. Accuracy on WB-DWI was significantly higher than on CT (100% vs 38.9%, p<0.001).

Operability assessment

Of the 18 patients with tumor, 10 patients turned out to be inoperable and 8 patients were operable. All three recurrences were inoperable. Two of them had peritoneal (serosal) metastases, not visible on CT, with secondary small bowel obstruction. The third patient had inaccessible retroperitoneal lymph nodes diagnosed on CT, but also peritoneal implants missed by CT.

Of the 15 primary cancers, 7 were inoperable. In 2 patients, CT suggested inoperability due to distant lymph nodes (n=2), and hydronephrosis due to possible tumoral obstruction of the distal ureter (n=1). The other 5 patients seemed operable on CT. However, they were all clearly inoperable at WB-DWI/MRI due to peritoneal metastases (n=7), brain metastases (n=1) and bone metastases (n=2). In 6 patients metastases were confirmed during follow-up imaging; in 1 patient peritoneal metastases were confirmed by histopathology during laparoscopy.

The other 8 patients were able to undergo curative surgery. These patients all seemed primarily operable on CT and WB-DWI/MRI. The added value of WB-DWI/MRI was in the detection of the primary tumor (n=3) and better delineation of the extent of the tumor (n=3). In three patients (3/8; 37.5%), WB-DWI/MRI revealed small peritoneal tumor implants on the surface of the pancreas, which were not detected by laparoscopy, though histopathologically confirmed after surgery.

Overall, the numbers for prediction of inoperability for CT were: sensitivity of 30%, specificity 100%, PPV 100% and NPV 53.3%. For WB-DWI/MRI all these values were 100%, leading to an accuracy that was significantly higher than CT (100% vs 61.1%, p=0.008).

Patients with gastric cancer/recurrence benefit from accurate diagnosis, staging and follow-up, maximizing the chance of complete resection and improved survival. The present study showed a high accuracy of WB-DWI/MRI of 96.9% for tumor detection, with only one false positive result, where a patient with gastritis was falsely interpreted as a small operable gastric cancer. Furthermore, WB-DWI/MRI was highly accurate for the prediction of inoperability (PPV 100%, NPV 100%), compared to CT (PPV 100%, NPV 53.3%). In 3 patients, WB-DWI/MRI revealed small peritoneal tumor-implants on the surface of the pancreas, not detectable with laparoscopy, suggesting higher sensitivity of WB-DWI/MRI over laparoscopy.

According to recent literature [29–32], the role of MRI in gastric cancer imaging has become more important with DWI and the calculation of ADC as a possible biomarker in diagnosis, T-staging and treatment response assessment [29]. Little is written about the role of MRI in determining metastatic gastric cancer [32]. Some studies suggest that the diagnostic performance of (DWI-)/MRI [33, 34] does not significantly differ from ¹⁸F-FDG PET/CT or CT. However, these studies contained few patients with peritoneal disease (3/49 gastric cancers) [33] and only one gastric adenocarcinoma (out of 30 different gastrointestinal malignancies) [34]. Moreover, both studies used different bowel preparation as well as different b values [33, 34].

Other studies involving tumors with different histopathology (mainly ovarian and colorectal) [15, 23, 28] showed that CT had an insufficient performance to detect PC with accuracies around 51–88%, being even higher than in our study with an accuracy of CT of 38.9%. CT especially fails in detecting tumor infiltration of the mesenteric root and serosal involvement of the small bowel with an accuracy in our study of 0%, compared to other studies where accuracies ranged from 21 to 48% [15, 23, 28, 35, 36]. DWI/MRI is known to be very good at detecting peritoneal tumor implants and implants at the small bowel wall with accuracies of 92–95% [23, 28], which is completely in line with our study (100%).

A limitation of this study is the small study population, presenting both primary and recurrent tumors. However, to our knowledge this is the first study to describe the role of WB-DWI/MRI in gastric cancer, with the confirmation that it also works on 1.5T and not only 3T.

With the results of this pilot study we can conclude that WB-DWI/MRI is a powerful one-stop imaging method in staging gastric cancer, providing all needed information about disease extent and disease location, inside and outside the abdominal cavity, to successfully determine operability. These results need to be confirmed in larger studies.

CT: Computed Tomography

MRI: Magnetic Resonance Imaging

DWI: Diffusion-weighted Imaging

WB-DWI/MRI: whole-body diffusion-weighted MRI

PC: Peritoneal carcinomatosis

FDG-PET/CT: ¹⁸F-Fluoro-deoxyglucose positron emission tomography

ADC: apparent diffusion coefficient

Ethical Approval and Consent to participate
This retrospective study was approved by the institutional review board (Ethical Committee Imelda Hospital Bonheiden, 10/12/2019, committee’s reference number 191248). Informed consent was waived.

Consent for publication

Not applicable.

Availability of supporting data

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

Competing interests

The authors declare that they have no competing interests.

Funding

Not applicable

Author’s contributions

Study concepts: SDV, VV, FDK, RD. Study design: SDV, VV, FDK, RD. Data acquisition: SDV, VV, YDB, SC, KV, TT, RD. Quality control of data: SDV, VV, YDB, RD. Data analysis and interpretation: SDV, VV, YDB, RD. Statistical analysis: SDV, FDK, RD. Manuscript preparation: SDV, FDK, RD. Manuscript editing and reviewing: all authors. All authors read and approved the final manuscript.

Acknowledgements

Not applicable

Authors’ information

¹ Department of Radiology, University Hospitals Leuven, KU Leuven, Herestraat 49, 3000 Leuven, Belgium. ²Department of Radiology, Imelda Hospital Bonheiden, Imeldalaan 9, 2820 Bonheiden, Belgium.

³ Department of Gastroenterology, Imelda Hospital Bonheiden, Imeldalaan 9, 2820 Bonheiden, Belgium. ⁴ Department of Surgery, Imelda Hospital Bonheiden, Imeldalaan 9, 2820 Bonheiden, Belgium.

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Accuracy of Whole-Body Diffusion-Weighted MRI (WB-DWI/MRI) in Diagnosis, Staging and Follow-Up of Gastric Cancer, in Comparison to CT: A Pilot Study.

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