Comparison of Diffusion-Weighted Magnetic Resonance Imaging and 18F-Fluorodeoxyglucose Positron Emission Tomography/Computed Tomography for Detection of Peritoneal Carcinomatoses in Advanced Epithelial Ovarian Cancer

doi:10.21203/rs.3.rs-5014920/v1

Objectives: To compare the diagnostic accuracy of diffusion-weighted magnetic resonance imaging (DW-MRI) and 18F-fluorodeoxyglucose combined positron emission tomography combined with computed tomography(FDG-PET/CT) in detecting peritoneal carcinomatoses in advanced epithelial ovarian cancer (EOC).

Methods: This prospective study enrolled patients with stage III-IV EOC consecutively from October 2020 to February 2023. Participants underwent both DW-MRI and FDG-PET/CT. Three radiologists independently evaluated the radiological images using peritoneal cancer index (PCI) scoring systems. Clinical data, preoperative imaging assessments, and cytoreductive surgical outcomes were recorded. Univariate and multivariate analyses were performed to determine the critical regions for surgery associated with incomplete resection. The diagnostic performance of each imaging modality was calculated for each site. The interobserver agreement was assessed.

Results: Forty-eight patients were enrolled in this study. No statistically significant differences were found between the imaging modalities (p≥0.142) based on the PCI scoring evaluation system. Omental lesions extend to the hepatic flexure or splenic flexure (p=0.045, OR=20.891), and small bowel mesentery involvement (p=0.039, OR=21.814) were identified as surgically critical regions associated with incomplete resection. DW-MRI demonstrated significantly higher accuracy than FDG-PET/CT (p=0.049) in diagnosis at omental lesions extend to the hepatic flexure or splenic flexure and diaphragmatic peritoneum, with sensitivity and specificity of 0.773 and 0.792 for DW-MRI, and 0.619 and 0.696 for FDG-PET/CT, respectively. DW-MRI also showed higher interobservers agreement (k=0.654-0.782) compared to moderate agreement (k=0.515-0.745) in FDG-PET/CT.

Conclusion: DW-MRI and FDG-PET/CT were comparable in assessing the entire abdominopelvic tumor burden based on PCI scoring system. DW-MRI has an advantage in detecting omental lesions extending to the hepatic flexure or splenic flexure, which is predictive of incomplete resection.

Peritoneal carcinomatosis

Diffusion-weighted imaging

Positron-Emission Tomography computed tomography

Epithelial ovarian cancer

Cytoreductive surgery

Approximately half of patients diagnosed with advanced epithelial ovarian cancer (EOC; International Federation of Gynecology and Obstetrics [FIGO] III/IV) [1]. Multiple analyses have confirmed that women with complete resection of all visible disease have the best survival outcomes [2–4] . In this context, describing and quantifying the tumor burden are essential for planning surgical procedures, with direct impacts on surgical morbidity. The peritoneal carcinosis index (PCI) has been considered the standard for describing carcinomatosis. The commonly used PCI, described by Jacquet and Sugarbaker, is used for colorectal cancer and mesothelioma, dividing the peritoneum and intraperitoneal organs into 13 regions[5]. However, Rosendahl et al. and Sudan et al. highlighted that specific anatomic regions hold more predictive value for achieving complete resection and survival in advanced EOC[6,7]. The predictive value of the PCI score or selected regions for resectability remains controversial[8].

Currently, computed tomography (CT) is commonly used for preoperative assessments to determine tumor resectability. However, CT is not ideal for evaluating the resectability of advanced EOC in primary debulking surgery (PDS)[9,10]. Diffusion-weighted magnetic resonance imaging (DW-MRI) and 18F-fluorodeoxyglucose positron emission tomography/computed tomography (FDG-PET/CT) are both widely available. Studies have indicated high specificity and moderate sensitivity for DW-MRI and FDG-PET/CT in predicting incomplete debulking[11–14]. They may provide complementary options for detailed reporting on the distribution of peritoneal carcinomatoses. However, the evidence is not yet conclusive enough to recommend routinely incorporating DW-MRI or FDG-PET/CT into clinical practice[15].

The objective of this study is to compare the diagnostic accuracy of DW-MRI and FDG-PET/CT in identifying the PCI as recorded during surgery and critical tumor sites relevant for surgery.

1. Patients selection and clinical data recording

The prospective study was approved by the institutional ethics board (No. B2021324). The study consecutively enrolled patients diagnosed with advanced EOC. Patients underwent FDG-PET/CT within 4 weeks before surgery from October 2020 to February 2023. For patients for whom FDG-PET/CT indicated complete resection at PDS is unlikely, abdominopelvic MRI was performed according to a predefined protocol at our institution within 1-2 weeks before surgery. Imaging results, along with the patient's performance status and comorbidities, were assessed by a multidisciplinary team to determine whether patients would receive PDS or neoadjuvant chemotherapy with interval debulking surgery (IDS). Written informed consent was obtained from all participants. Tumor extent was assessed based on laparoscopy findings (for those treated by IDS) and PDS results, recorded by gynecologic oncologist following a standardized template. The inclusion and exclusion criteria were summarized in Figure 1.

The recorded clinical data included: age, preoperative levels of cancer antigen-125 (CA125) and human epididymis secretory protein 4 (HE4) marker, surgical staging according to the FIGO classification based on imaging (chest CT, abdominal-pelvic DW-MRI, or FDG-PET/CT) or surgical results, tissue history, and cytoreduction status (complete resection with no macroscopic residual disease; incomplete resection with any residual lesions after PDS or IDS).

2. Image Acquisition

2.1 DW-MRI acquisition.

DW-MRI examinations were performed using dedicated phased-array body and spine coils on a 3T MR systems (Discovery MR 750, GE Healthcare). Patients fasted for 4-6 hours. The conventional abdominopelvic MRI protocol included axial T1-weighted imaging (T1WI) with or without fat saturation, axial and coronal fat-suppressed T2-weighted imaging (T2WI), and contrast-enhanced T1WI using 2D Flash with fat saturation. An axial and coronal diffusion weighted imaging (DWI) was obtained with b-values of 0 and 800 or 1000 s/mm². All pulse sequences, except for the contrast-enhanced T1WI, were performed using free-breathing acquisition techniques. Respiration-triggered acquisition was employed for abdominal T2WI and DWI. An antispasmodic agent (butylscopolamine bromide, Buscopan®, 20 mg/ml, Boehringer Ingelheim) was administered. The total scan time was 35 minutes.

2.2 FDG-PET/CT acquisition.

All patients fasted for at least 6 hours and had a plasma glucose level of ≤7.0 mmol/l before intravenous injection of 18F-FDG. FDG-PET/CT scans were performed using a total-body FDG-PET/CT scanner (uEXPLORER, United Imaging Healthcare, Shanghai, China) with an axial field of view of 194 cm. Whole-body acquisition was conducted approximately 70±6 minutes after the injection of 5.5 MBq/kg of 18F-FDG. PET reconstructions were carried out using the ordered subset expectation maximization algorithm with the following parameters: time-of-flight and point spread function modeling, 3 iterations, 20 subsets, matrix of 192 × 192, a slice thickness of 1.443 mm, and a full width at half maximum of the Gaussian filter function of 3 mm.

3. Imaging interpretation

DW-MRI images were independently reviewed by three board-certified radiologists (C.S.Q, D.Y.Q and W.M.R) with 11, 15 and 7 years of experience in gynecological imaging, respectively. FDG-PET/CT images were reviewed by two nuclear physicians (L.G.B, M.X.L and L.J.J) with 11, 10 and 5 years of experience in gynecological imaging, respectively. The DW-MRI and FDG-PET/CT images were reviewed separately, with imaging observers blinded to each other's assessments and clinical findings. The assessment of selected anatomic regions and imaging PCI scores were obtained.

3.1 PCI scoring systems

The conventional PCI scoring system divides the peritoneum and intraperitoneal organs equally into 13 regions [16]. Two vertical midclavicular lines and two horizontal lines at the anterior superior iliac spines and under the costal arcs divide the peritoneal cavity into 9 areas (0-8), while the upper and lower jejunum and ileum constitute the remaining 4 areas. For each region, a lesion size score of 0-3 is assigned based on the tumor size (0 = no visible tumor; 1 = tumor < 0.5 cm; 2 = tumor 0.5-5 cm; and 3 = tumor > 5 cm). The sum (0-39) represents the conventional PCI score (Figure 2A and Supplemental Table 1).

Another PCI scoring system, with additional points for involvement of selected regions, was proposed in gynecological research[17]. This system assigns additional points to selected regions, including the left and right diaphragm, liver surface, omental lesions extending to the hepatic flexure or splenic flexure, gastrohepatic space, small bowel mesentery, peritoneal disease (localized diseases involving the peritoneum of the middle abdomen; diffused thickening of the left and right paracolic gutter peritoneum, combined with thickening of the pelvic peritoneum, and/or involving the colon), bowel infiltration, and suprarenal lymph node metastases [17]. Each region is scored as either 0 or 2 (0 = no visible tumor; 2=have any lesions). The total score (0-16) represents the selected PCI score (Figure 2B and Supplemental Table 2).

4. Surgical evaluation

Following each PDS and exploratory laparotomy, the surgeon recorded findings using a standardized form, noting the location and size of any disease present. If complete resection seemed doubtful, an exploratory laparotomy was conducted. During this procedure, the abdominal and pelvic cavities were systematically evaluated to assess the extent and size of the disease.

5. Statistical analysis

Statistical analysis was performed using SPSS statistical software (V26.0; IBM, Armonk, NY) and MedCalc (version 20.215; MedCalc Software Ltd, Ostend, Belgium). According to previous results, we anticipate a sensitivity of 80% and 90% for DW-MRI and FDG-PET/CT, and we set alpha at 0.05 and power at 0.80[15]. The sample size is 41. The diagnostic performances of the two imaging modalities in different anatomic regions were evaluated using receiver operating characteristic (ROC) curves, from which sensitivity and specificity were calculated. The areas under the ROC curves were compared between the two imaging methods. The inter-observer agreement for each region were compared by Fleiss Kappa. The agreement between the entire imaging PCIs and the PCIs confirmed by surgery was assessed using Bland-Altman statistics and correlation matrices. The difference between DW-MRI and FDG-PET/CT in assessing the two PCI scoring system was compared using Student's paired t-test or Mann-Whitney U test. Univariate analysis was conducted to compare clinical factors, entire surgery PCI, and different region carcinomatoses between complete and incomplete resection groups after PDS. Variables with p-value ＜0.05 were included in the multivariate models. Multivariate logistic regression analysis with forward stepwise elimination was conducted to identify factors associated with incomplete resection. All tests were two-sided, with statistically significant at a p-value < 0.05.

1. Patients

This prospective study consecutively enrolled 48 patients with advanced EOC, with a median age of 55 years (range: 49-66 years). Thirty-three underwent PDS, 12 underwent IDS and exploratory laparotomy, and 3 declined further treatment after exploratory laparotomy. The patient characteristics are summarized in Table 1.

Of the 35 patients (77.78%) who achieved complete resection, 26 patients in the PDS group and 9 patients in the IDS group. The remaining 10 patients (22.22%) who did not achieve complete resection，included 7 from the PDS group and 3 from the IDS group. The residual tumor distribution was summarized in Table 2.

2. The comparison of DW-MRI and FDG-PET/CT diagnostic accuracy in selected anatomic regions with surgery correlation

The quality of DW-MRI and FDG-PET/CT images was evaluated in all patients and regions. There were significant differences observed in the diaphragmatic peritoneum (p=0.017, Figure 3) and omental lesions extending to the hepatic flexure or splenic flexure (p=0.049, Figure 4). No statistically significant differences were detected in other regions between the two imaging modalities (p≥0.114). The comparison of the two imaging modalities diagnostic accuracy in selected anatomic regions was summarized in Table 3.

3. The comparison of PCI_surgery and PCI_ imaging

Forty-three percent (21/48) of patients were underestimated in the conventional PCI scoring system by either DW-MRI or FDG-PET/CT. Seventy-one percent（34/48）and 73% (35/48) were underestimated in the selected regions PCI scoring system by DW-MRI and FDG-PET/CT respectively. The mean differences in the conventional PCI scoring system (PCI_surgery - PCI_imaging) were 0.958 (CI: -4.556, 6.472) for DW-MRI and 1.574 (CI: -4.288, 7.437) for FDG-PET/CT. In selected regions, the mean differences (PCI_surgery - PCI_imaging) were 2.478 (CI: -3.463, 8.421) for DW-MRI and 2.188 (CI: -5.187, 9.562) for FDG-PET/CT (Figure 5). The correlation between DW-MRI and surgical result was 0.901 for conventional scoring system and 0.738 for the selected region PCI score system (both p<0.0001). The correlation between FDG-PET/CT and surgical result was 0.887 for conventional PCI score system and 0.594 for selected region PCI score system (both p<0.0001). There was no statistically significant difference between the imaging modalities in assessing the two PCI scoring systems (p=0.142 and p=0.614).

4. The clinical and regional carcinomatoses that related to the surgical residual disease

In the PDS group, 7 of the 33 patients had residual disease after PDS. Significant differences (p≤0.014) were observed in the PCI scores between the two groups. In the univariate analyses, there were significant differences in specific regional carcinomatoses between the two groups, including lesions in the hepatogastric space, omental lesions extending to the hepatic flexure or splenic flexure, small bowel mesentery, and peritoneal disease. In the multivariate analysis, only omental lesions extending to the hepatic flexure or splenic flexure (OR (odd ratio) =20.891; p=0.045) and small bowel mesentery involvement (OR=21.843; p=0.039) remained as independent significant variables associated with incomplete resection (Table 4; Figure 6).

As the PCI and critical anatomic sites with carcinomatoses in predicting incomplete resection for the patients with advanced EOC has been valued, the accurately noninvasive assessment of tumor burden before surgery become more and more important in clinical setting[6,8]. However, the certainty of the evidence was insufficient to advise routine addition of FDG-PET/CT or DW-MRI to clinical practice[15]. In this prospective single-center study, we compared the diagnostic accuracy of DW-MRI and FDG-PET/CT in preoperative assessment of PCIs and selected anatomic sites in patients who need further identify the tumor burden to optimize treatment selection.

Both DW-MRI and FDG-PET/CT were found to underestimate the total PCI as determined during surgery. The modalities were more likely to underestimate the PCI in selected regions than the conventional PCI (~70% vs. 43.75%), indicating that accurately identify the critical anatomic sites before surgery still challenging. Though the correlation between PCI_DW-MRI and PCI_surgery was stronger than that between PCI_FDG-PET/CT and PCI_surgery (r=0.738-0.901 vs. 0.587-0.887), the two imaging modalities showed comparable diagnostic abilities, which is consistent with previous studies[18,19].

When examining peritoneal metastases region by region, DW-MRI demonstrated significantly higher accuracy than FDG-PET/CT in detecting lesions in the diaphragmatic peritoneum and omental lesions extending to the hepatic flexure or splenic flexure. Both of the two imaging modalities showed moderate inter-observer agreement, excepted for FDG-PET/CT in detecting lesions in the omental lesions extending to the bowl. One reason may be that DW-MRI is more sensitive in detecting mesenteric or serosal involvement due to the high signal intensity of lesions on high b-value images compared to the suppressed background signal [20,21]. Another reason may be the designed examination protocol for DW-MRI, which involves coronal scanning combined with respiratory triggering. This offers advantages for visualizing the diaphragmatic peritoneum and omental lesions extending to the hepatic flexure or splenic flexure, which are more challenging to detect on axial images.

Note that 80% to 90% of residual disease is found in the small intestine with mesentery and/or in the hepatoduodenal ligament, both in our cohort and in previous studies [9,18,22]. Previous studies emphasize DW-MRI’s diagnostic capability in detecting small bowel lesions[23]. However, we found no advantage of DW-MRI over FDG-PET/CT in detecting lesions involving the small bowel mesentery and the hepatoduodenal ligament. The two imaging modalities demonstrated similar diagnostic efficiency and consistence among observers. Lesions, particularly those smaller than 0.5cm, involving the small intestine with mesentery and the hepatoduodenal ligament, remain challenging for preoperative diagnosis.

Our study has some limitations. First, we did not compare DW-MRI and FDG-PET/CT against MDCT, which is more commonly used in clinical setting. However, the aim of this study is to identify the additional benefits of DWI-MRI and FDG-PET/CT in identifying critical anatomic sites that CT may not good at. Previous studies have shown that these imaging modalities typically offer better specificity and sensitivity than MDCT[14,23–25]. Second, the prospective nature and the focus of the study led to missing surgical details for three patients, and selected bias is evident. Lastly, this is a single-center study, and the results have not been further validated by multicenter trials. Strengths include the homogeneity of the patients, standardized surgeries performed by two certified gynecologic cancer surgeons at a single center, and perioperative PCI evaluations conducted. However, patient homogeneity could also be seen as a limitation，as it complicates the generalization of our findings to other centers.

DW-MRI and FDG-FDG-PET/CT were comparable in assessing the total abdominopelvic tumor burden using PCI score system. The imaging PCI often underestimated the true extent of peritoneal dissemination. The DW-MRI showed superior performance to FDG-PET/CT in assessing critical disease regions corresponding to the small bowel mesentery and omental lesions extending to the hepatic flexure or splenic flexure, which was independently predictive of incomplete resection.

Author Contribution

•Jian-Jun Zhou and Meng-Su Zeng contributed equally to guarantee this study.•Song-Qi Cai and Jian-Feng Huang contributed equally to the study design, data acquirement and manuscript editing. As a result, they are listed as joint first authors of this article.•Funding acquisition: Song-Qi Cai, Yu-Qin Ding.•Investigation: all authors.•Resources: all authors.•Writing—review & editing: all authors.

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Table1 Patient demographics and clinical data
	Median/N	Range/N%
Age(years)	55	(49-66)
Primary tumor site
ovary	44	91.7%
fallopian tube	3	6.2%
primary peritoneal	1	2.1%
Histology
high grade serous adenocarcinoma	43	89.6%
low grade serous adenocarcinoma	1	2.1%
clear cell adenocarcinoma	4	8.3%
CA125(U/ml)	890	（393-1698）
HE4(pmol/L)	384.5	(157.5-747.25)
Treatment for the primary diagnosed advanced high-grade ovarian cancer+
PDS	33	73.3%
IDS	12	26.7%

CA125，cancer antigen-125；HE4, human epididymis secretory protein 4

+3 patients underwent exploratory laparotomy but declined to have further treatment

Table 2 Cytoreduction status and the residual tumor distribution

PDS, primary debulking surgery; IDS, interval debulking surgery

Table 3 DW-MRI and FDG-PET/CT diagnostic performance in selected anatomic regions
Region	DW-MRI					FDG-PET/CT				p (DW-MRI vs. PET/CT)
Region	Sensitivity		Specificity	ROC area	k（95%CI）	Sensitivity	Specificity	ROC area	k（95%CI）	p (DW-MRI vs. PET/CT)
Diaphragmatic peritoneum	0.903	0.592		0.910	0.782（0.671,0.867）	0.645	0.917	0.781	0.745（0.619,0.843）	0.005*
Liver lesions	0.631	0.862		0.747	0.757（0.635,0.850）	0.526	0.724	0.625	0.712（0.576,0.820）	0.114
Lesions in the hepatogastric space	0.423	0.92		0.683	0.756（0.634,0.849）	0.550	0.875	0.713	0.635（0.474,0.769）	0.406
Omental lesions extend to the hepatic flexure or splenic flexure	0.773	0.792		0.772	0.645（0.491,0.773）	0.619	0.696	0.657	0.515（0.330,0.683）	0.049*
Small bowel mesentery involvement	0.577	0.810		0.693	0.634（0.473,0.768）	0.630	0.714	0.684	0.671（0.5240.792）	0.603
Peritoneal disease	0.714	0.963		0.823	0.864（0.786,0.918）	0.667	0.840	0.765	0.725（0.583,0.834）	0.401
Bowel infiltration	0.524	0.833		0.679	0.704（0.565,0.814）	0.524	0.875	0.699	0.826（0.732,0.895）	0.804
Suprarenal lymph node metastases Suprarenal	0.842	0.957		0.899	0.912（0.745,1.00）	0.895	0.833	0.864	0.934（0.769,1.00）	0.507

ROC, receiver operating characteristic; CI, confidence interval

*a significant difference was found in this item

Table 4 The univariate and multivariate analyses in PDS group
	Univariate analysis		Multivariate analysis
	OR (95% CI)	p	OR (95% CI)	p
Age(years)	1.042（0.964, 1.126）	0.304	……	……
CA125(U/ml)	1.000(0.999,1.000)	0.456	……	……
HE4(pmol/L)	1.000(0.999,1.000)	0.729	……	……
Diaphragmatic peritoneum(Y/N)	6.750(0.750,60.760)	0.089	……	……
Liver lesions(Y/N)	1.780(0.843,3.754)	0.130	……	……
Lesions in the hepatogastric space(Y/N)	3.464(1.430,8.393)	0.006	……	……
Omental lesions extend to the hepatic flexure or splenic flexure (Y/N)	27.000(2.886,252.624)	0.004	20.891（1.077,405.288）	0.045
Small bowel mesentery involvement(Y/N)	33.000(3.462,314.533)	0.002	21.843（1.175,406.170）	0.039
Peritoneal disease(Y/N)	41.400(4.23,405.216)	0.001	13.146（0.722,239.449）	0.082
Bowel infiltration (Y/N)	0.867(0.204, 3.676)	0.833	……	……
Suprarenal lymph node metastases Suprarenal(Y/N)	1.018(0.220,4.720)	0.982	……	……
Conventional PCI	1.410(1.121,1.774)	0.003	……	……
Selected regions PCI	1.175(1.033,1.336)	0.014	……	……

PDS, primary debulking surgery; OR, odd ratio; CI, confidence interval; CA125, cancer antigen-125; HE4, human epididymis secretory protein 4

No competing interests reported.

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Comparison of Diffusion-Weighted Magnetic Resonance Imaging and 18F-Fluorodeoxyglucose Positron Emission Tomography/Computed Tomography for Detection of Peritoneal Carcinomatoses in Advanced Epithelial Ovarian Cancer

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