Research article
Diffusion-weighted magnetic resonance imaging in peritoneal carcinomatosis from suspected ovarian cancer: Diagnostic performance in correlation with surgical findings

https://doi.org/10.1016/j.ejrad.2019.108696Get rights and content

Highlights

Abstract

Purpose

Ovarian cancer (OC) is the commonest cause of death by gynaecological cancer in developed countries.

Peritoneal carcinomatosis (PC) complete debulking without residual disease of >1 cm is the best prognostic predictor in advanced OC.

PC is assessed with Computed tomography (CT). CT accuracy and cytoreduction success predictive ability are limited. PET/CT is not an imaging standard for PC.

PC shows high signal foci in Diffusion-weighted magnetic resonance imaging (DWI MRI).

We assessed the diagnostic performance (DP) and tumour burden correlation of Whole body DWI with background suppression MRI (WB-DWIBS/MRI) in PC of suspected OC using the Peritoneal Cancer Index (PCI), referring to cytoreduction surgery as the standard reference.

Method

Fifty patients with suspicion of disseminated OC underwent cytoreduction and WB-DWIBS/MRI. The PCI scores tumour burden (0–3) in 13 anatomical regions (global range of 0–39). Two radiologists (Rad1/Rad2) assessed the PCI preoperatively and with surgical findings.

We evaluated regional and global DP, the interobserver agreement (Cohen´s kappa coefficient), statistical differences (McNemar test) and tumour burden (Pearson’s test).

Results

72% (36/50) were epithelial OC and 78% (39/50) achieved complete cytoreduction. Global-PCI correlation was 0.762 (Rad1) with DP: Sensitivity 0.84, specificity 0.89, accuracy 0.89, and kappa 0.41.

Average global-PCI was 7. The pelvis and right hypochondrium showed the highest positive rate and DP, while the intestinal regions presented the lowest. Previous studies reported higher sensitivity than CT or PET/CT, although only a few used the PCI.

Conclusions

WB-DWIBS/MRI is reliable to depict, quantify and to predict complete cytoreductive surgery in OC PC.

Introduction

Ovarian cancer (OC) is the primary cause of death by gynaecological cancer in developed countries, with an annual incidence of 3412 and a 5-year prevalence in the general population of 7939 for 2017 in Spain, similar to other industrialized countries [1,2]. The most common OC histology is epithelial type, and up to 65% of patients are diagnosed at stages III and IV with peritoneal carcinomatosis (PC) and nodal dissemination, with high mortality [2,3].

The treatment of choice for OC is primary surgical cytoreduction followed by platinum-based adjuvant chemotherapy [4]. If there are no criteria against abdominal resection [5], achieving complete surgical debulking without residual disease >1 cm (R0) is the best prognostic predictor in advanced OC [5,6].Occasionally, if primary surgery cannot be performed initially [5], interval surgery after three cycles of neoadjuvant chemotherapy may be considered. Secondary cytoreduction is performed after recurrence if there is an option for R0 debulking.

Preoperative detection of irresectable disease is crucial for the selection of surgical candidates, and the detection and location of peritoneal seeding in OC is useful in the planning of accurate surgery. Laparoscopy has been proposed as a preoperative approach to tumour evaluation using the Fagotti score [7]. This system assesses eight peritoneal structures and assigns a score of 0–2. If global scoring is ≥8, then the predictive positive value (PPV) of a suboptimal surgical result is 100%. However, laparoscopy is an invasive technique, and it cannot evaluate the retroperitoneum nor the tumour posterior to the gastrosplenic ligament and in the lesser sac [8].

The peritoneal cancer index (PCI) [9] was described for PC quantification in surgical cytoreduction and hyperthermic intraperitoneal chemoperfusion (HIPEC). It is a region-wise scoring system that assesses 13 anatomic regions, each with a range of 0–3, and considers the largest lesion in each region according to the following categories: no tumour, LS0; up to 0.5 cm, LS 1; up to 5 cm, LS 2; and more than5 cm or confluent, LS 3 (Fig. 1). The PCI is calculated through the sum of all regional scores in each patient, with a total burden range of 0–39. It is used in digestive carcinomatosis candidates for cytoreduction and HIPEC, but not as often in ovarian carcinomatosis given that the only accepted prognostic factor is complete (R0) debulking, whereas HIPEC is still under discussion for advanced OC [10].

Different imaging techniques are used in preoperative PC assessment and describe several dissemination patterns [11,12], although no imaging tool is capable of predicting the success of a R0 resection. Computed tomography (CT) is the elective technique for abdominal imaging and, when using a dedicated protocol, CT correlates well with the surgical PCI [13]. CT is recommended for staging and follow up in gynaecological malignancies by the American College of Radiology (ACR) and National Comprehensive Cancer Network (NCCN) guidelines. The accuracy of CT for PC in OC and its capability for predicting the success of cytoreductive surgery is limited, although when evaluated with CA-125 levels it may predict prognosis [14,15]. Positron emission tomography CT with 18-fluorodeoxyglucose (PET/CT) can be considered for systemic evaluation of gynaecological malignancies, although it is not yet established as a reference standard for PC depiction [16]. Conventional MRI is useful in peritoneal carcinomatosis [17], however its diagnostic performance (DP) is inferior to PET/CT [18,19] and similar to CT [20]. Diffusion-weighted imaging (DWI) is obtained using high-energy short-time MR radiofrequency pulses, where the b value expresses the strength of potentiation in diffusion. Using high b values (b max≥ 1000), DWI provides a very high signal intensity of structures with water movement restriction and almost no signal from other anatomical structures. Dynamic contrast-enhanced imaging and DWI improve the capability of tumour pelvic recurrence characterisation [21], and the addition of high b DWI to routine MRI raises the DP for peritoneal metastases [[22], [23], [24], [25]]. Finally, whole body DWI with background suppression MRI (WB-DWIBS/MRI) combines high b DWI with conventional imaging of the entire body for anatomical referencing and characterisation of findings [26].

This study aimed to assess the DP and tumour burden correlation of WB-DWIBS/MRI in PC from suspected OC using the PCI, referring to cytoreduction surgery as the standard reference.

Section snippets

Study design

This is an observational, prospective, single-institution, non-comparative, DP study of WBMRI/DWIBS versus the pathologically-proven surgical standard of reference. Institutional review board approval was obtained, and all patients signed written informed consent.

Study population

Inclusion criteria included suspected diagnosis of a primary or recurrent ovarian carcinoma according to raised CA-125 levels and imaging findings. Exclusion criteria were claustrophobia, known renal impairment (creatinine >1.5 mg/dl

Clinical results

A total of 50 patients were selected for this study. Peritoneal seeding in 13 PCI regions was pathologically confirmed after surgery (Fig. 1). Table 2 shows the clinical outcome. Surgery was delayed in some patients due to acute comorbidities (acute infections, renal impairment and others).

Almost all the patients (94%, 47/50) presented with primary gynaecological disease; 88% (44/50) were primary gynaecological malignancies and 76% (38/50) were of ovarian origin, while the histology was

Discussion

This prospective study evaluated DP and tumour burden quantification using WB-DWIBS/MRI in suspected ovarian PC, comparing the imaging PCI with the surgical PCI in patients undergoing primary or secondary cytoreduction. Patients who received interval debulking surgery after three cycles of chemotherapy were excluded from the study, given that tumour necrosis and bleeding might be a source of false positives [28].

Secondary cytoreduction is a different clinical situation, in that recurrence in

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

We thank H. Nikki March, PhD, from Edanz Group (www.edanzediting.com/ac) for editing a draft of this manuscript and David Gutiérrez Pérez, BS in Mathematics, for the initial design of this study.

References (42)

  • B. Li et al.

    Diagnostic value of whole-body diffusion-weighted magnetic resonance imaging for detection of primary and metastatic malignancies: a meta-analysis

    Eur. J. Radiol.

    (2014)
  • ...
  • L.A. Torre et al.

    Ovarian cancer statistics, 2018

    CA: Cancer J. Clin.

    (2018)
  • Kurman, Robert J., 2014. International Agency for Research on Cancer, World Health Organization, WHO classification of...
  • T. Thigpen

    The if and when of surgical debulking for ovarian carcinoma

    N. Engl. J. Med.

    (2004)
  • D. Querleu et al.

    European Society of Gynaecological Oncology (ESGO) guidelines for ovarian cancer surgery

    Int. J. Gynecol. Cancer

    (2017)
  • I. Vergote et al.

    Neoadjuvant chemotherapy or primary surgery in stage IIIC or IV ovarian cancer

    N. Engl. J. Med.

    (2010)
  • A. Fagotti et al.

    Prospective validation of a laparoscopic predictive model for optimal cytoreduction in advanced ovarian carcinoma

    Am. J. Obstet. Gynecol.

    (2008)
  • S. Nougaret et al.

    Ovarian carcinomatosis: how the radiologist can help plan the surgical approach

    Radiographics

    (2012)
  • P.H. Sugarbaker

    Review of a personal experience in the management of carcinomatosis and sarcomatosis

    Jpn. J. Clin. Oncol.

    (2001)
  • S. González-Moreno et al.

    Imaging of peritoneal carcinomatosis

    Cancer J.

    (2009)
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