Peritoneal carcinomatosis: imaging with 64-MDCT and 3T MRI with ...

Abdominal Imaging

ª Springer Science+Business Media, LLC 2011 Published online: 5 October 2011

Abdom Imaging (2012) 37:616–627 DOI: 10.1007/s00261-011-9804-z

Peritoneal carcinomatosis: imaging with 64-MDCT and 3T MRI with diffusion-weighted imaging F. Iafrate,1 M. Ciolina,1 P. Sammartino,2 P. Baldassari,1 M. Rengo,1 P. Lucchesi,1 S. Sibio,2 F. Accarpio,2 A. Di Giorgio,2 A. Laghi1 1

Department of Radiological Sciences, Oncology and Pathology, ‘‘Sapienza’’ University of Rome, Viale Regina Elena 324, 00161 Rome, Italy 2 Department of Surgery ‘‘P. Valdoni’’, ‘‘Sapienza’’ University of Rome, Rome, Italy

Abstract Peritoneal carcinomatosis is usually associated with a poor overall survival rate. Recently, introduction of more aggressive surgical treatment and intraperitoneal chemotherapy appears to significantly increase the overall survival rate for these patients. A detailed preoperative assessment of peritoneal carcinomatosis could be very challenging in the field of imaging, but a new aggressive surgical approach requires an accurate preoperative assessment of the disease. Cross-sectional imaging using CT and MRI with diffusion-weighted imaging (DWI) sequences is important for appropriate management of patients with peritoneal carcinomatosis. Appreciation of the spectrum of diagnostic patterns and pitfalls as well as different sites of involvement of peritoneal carcinomatosis using CT and DWI is crucial for appropriate surgical treatment. Key words: Ovarian cancer—Peritoneal carcinomatosis—Multidetector CT—DWI MRI

Peritoneal carcinomatosis is defined as the seeding and implantation of neoplastic cells into the peritoneal cavity and may represent the advanced and evolved stage of tumors developed in abdominal and pelvic organs [1]. Intraperitoneal seeding via ascitic fluid is one of the most important ways of peritoneal metastases spreading. Dynamics of peritoneal fluid circulation are influenced by anatomical and physiological factors like force of gravity, pressure gradient created by diaphragm during inspiration, and peristaltic motion of the intestine [2–4]. Correspondence to: F. Iafrate; email: [email protected]

Ovarian, stomach, and colorectal cancers account for almost all cases with an incidence of about 70%, 15%, and 10%, respectively [1, 5]. Peritoneal carcinomatosis is invariably associated with a poor prognosis with a mean survival of 6 months (range 1–9 months) after initial diagnosis [6]. Currently, one of the best therapeutic approach available in clinical practice includes the combination of surgery and intraperitoneal chemohyperthermia, a complex peritonectomy procedure along with hyperthermic intraperitoneal chemotherapy (HIPEC) organized into two stages: first the surgical removal of the tumoral tissue, then a ‘‘washing’’ of the abdominal cavity with chemotherapic drugs at high concentrations, in order to kill the free tumoral cells. In ovarian as well as nonovarian carcinomatosis, including cancer of the appendix and colon, maximum cytoreduction, namely, peritonectomy according to the Sugarbaker criteria [7], combined with hyperthermic intraperitoneal chemotherapy (HIPEC), is a promising locoregional treatment. That treatment offers acceptable morbidity and mortality rates and the possibility of long survival [8, 9]. HIPEC has demonstrated significantly improved survival in patients with peritoneal metastases from intra-abdominal primary cancers [6, 10, 11]. Peritoneal cancer index (PCI) has been recognized as an independent prognostic indicator for long-term outcomes influencing the likelihood of complete cytoreduction that represents another principal determinant of long-term survival [12]. Multidetector computed tomography (MDCT) and magnetic resonance imaging (MRI) with conventional and diffusion-weighted sequences are able to give accurate information on morphology, size, location of peritoneal implants, lymph node enlargement, and

F. Iafrate et al.: Peritoneal carcinomatosis

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Fig. 1. Different aspects of peritoneal implants. A Axial contrast-enhanced CT scan showing solid implants (arrow) presenting as several homogenous soft-tissue nodules. B Intraoperative image of solid implants (circle). C Coronal contrast-enhanced CT image showing a cystic implant (arrow) over small bowel loops appearing hypodense due to the internal fluid

component. D Intraoperative image of cystic implants (circle). E Axial contrast-enhanced CT image showing a 4 cm implant of peritoneal carcinomatosis (arrow) presenting an oval shape and a mixed structure consisting of a mucinous cystic component and a solid irregular rounded wall showing contrast enhancement. F Intraoperative image of mixed implants (circle).

presence of ascites; results useful for disease staging, presurgical assessment and recurrent disease. In this article we review the role of 64-MDCT and MRI with diffusion-weighted sequences in peritoneal carcinomatosis imaging, the appearance of different diagnostic patterns and analysis of advantages and limits of those techniques.

administration of at least 500 mL of water 15–20 min prior to the study and intravenous administration of hyoscine butylbromide (Buscopan). CT scanning is performed in the supine position and longitudinal coverage is obtained from the diaphragm to the ischial tuberosities. The use of IV contrast medium (CM) is somewhat crucial for the assessment of peritoneal carcinomatosis. Vascular enhancement is directly influenced by the iodine delivered per second (Iodine Delivery Rate; IDR), while parenchymal enhancement is proportional to the total volume of iodine administered to the patient. These parameters should be optimized according to

Imaging method using MDCT CT is routinely performed using at least 16-row multidetector CT, better a 64-detector row CT scanner. The patient preparation includes fasting for 6 h, oral

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Fig. 2. Calcified implants. A Axial contrast-enhanced CT scan of a 76-year-old patient with ovarian cancer shows several implants of peritoneal carcinomatosis involving the greater omentum and appearing partially hyperdense due to calcifications (arrow).

patients’ characteristics, in particular lean body weight (LBW). To obtain an effective parenchymal enhancement, around 600 mg of iodine should be injected per kg of LBW. As an example, a regular man of 70 kg has around 15% of body fat, thus, his lean body weight is around 59 kg and 35.4 g of iodine (101 mL using a CM with a concentration of 350 mgI/mL) should be injected. While a male individual of the same weight but obese has around 32% of body fat, thus, only 82 mL of CM are needed (LBW: 47.6 kg; total iodine dose: 28.5 g). Vascular enhancement should also be optimized according to patient size. These values can be virtually obtained with any concentration of CM according to the following formula: IDR = ([I]/1000) 9 FR where [I] is the CM concentration (expressed in mgI/mL) and FR is the injection Flow Rate. Referring to the previous example for a man of 70 kg an IDR of 1.6 gI/s, thus, a 350 CM should be injected at 4.6 mL/s. Arterial and venous phase images of the abdomen and pelvis are, respectively, acquired 35 and 70 s after intravenous injection of CM using 1.5 collimation, 120 kV, mean tube current time-product 180 mAs, pitch 1.00. Scanning is caudocranial in the arterial phase and craniocaudal in the venous phase. Arterial phase is mandatory in case of hypervascular primary tumors and to assess or rule out vascular infiltration in case of implants located adjacent to vascular structures. Delayed phase, acquired from 8 to 10 min after contrast injection is fundamental in case of pelvic implants or retroperitoneal metastases that involve ureters occluding them or causing hydroureteronephrosis. Both axial and multiplanar reformatted images are reviewed on a workstation and threedimensional display of data could be performed to better depict peritoneal disease.

Fig. 3. Micronodular pattern in a 60-year-old woman with ovarian cancer. A Axial contrast-enhanced CT image showing tiny 4–5 mm solid implants (arrowhead) involving the mural serous layer. B Axial DW black-and-white reversed-contrast image showing the increasing contrast between lesions that appear as black spots (arrowhead), and the hyperintense normal surrounding tissue. C Intraoperative image of peritoneal implants (arrowhead).


Fig. 4. Nodular pattern. A Coronal contrast-enhanced CT axial image showing a cystic nodular 3 cm implant at the splenic hilum (arrow). B Axial DW black-and-white reversed-contrast image confirms the presence of malignant deposit (arrow)

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clearly detectable due the high contrast-to-noise-ratio using diffusion-weighted sequences. C Intraoperative image of peritoneal implants (arrowhead).

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Imaging method using diffusionweighted imaging (DWI) MRI imaging requires state of the art high field magnet. In our personal experience, a superconducting magnet that operates at 3.0 Tesla (70 cm patient gantry, 48 cm FOV, 50 mT/m amplitude, and 200 T/m/s slew rate gradients) has been used. MRI protocol includes fasting for 6 h, oral administration of water (500 mL) and intramuscular injection of hyoscine butylbromide (Buscopan). Phased array surface coils are mandatory and now able to providing simultaneous coverage of the abdomen and pelvis. Before starting with DWI protocol, single shot T2weighted images, for both abdomen and pelvis, must be acquired to obtain morphological evaluation of peritoneal disease and to subsequently perform image fusion. For abdominal imaging, single shot T2-weighted fast images (SSFSE) in a breath-hold must be performed in the axial and coronal planes (TR/TE 2000/121, SL 5.00 mm, matrix 416 9 224, FA 90, and FOV 410 9 410). For pelvic imaging, fine resolution T2-weighted fast images (FRFSE) breathing independent must be performed in the axial, coronal, and sagittal planes (TR/TE 3875/128, SL 4.00 mm, matrix 512 9 224, FA 90, and FOV 320 9 320). Axial DWI images must be subsequently obtained using respiratory-triggered acquisitions and short TI inversion recovery-echo planar imaging sequence for fat and background suppression. Imaging parameters for DWI were as follows: DWI: TR/TE 6000/59 ms, SL 4.00 mm, matrix 80 9 128, FA 90, FOV 351 mm 9 390 mm, and b values of 0, 800, and 1000 s/mm2. Motion probing gradient pulses should be placed in the three orthogonal planes. Isotropic DWI is generated by three orthogonal-axis images. All axial source images must be provided with black-and-white reversed-contrast display, fusion images and ADC maps. All images are then reviewed on a dedicated workstation.

CT-MR appearance of peritoneal carcinomatosis Morphological aspects

Fig. 5. ‘‘Omental cake’’. A Axial contrast-enhanced CT image showing a micronodular omental thickening (arrow) with a typical stratified appearance. Malignancy tends to hide among small bowel loops. B Axial DW black-and-white reversed-contrast image demonstrates a clearly detectable region of omental nodular infiltration with low signal intensity (arrow). C Surgical specimen.

Peritoneal carcinomatosis is characterized by the presence of soft-tissue implants with different morphological features and distribution in the peritoneal cavity [13]. Radiologists should evaluate morphology and localization of each implant. At MR an CT imaging, peritoneal implants are like soft-tissue nodules that assume different characteristics according to number (solitary or multiple), shape, volume, and density or intensity without and with intravenous injection of iodinate contrast in both arterial and venous phase or in venous phase only. Three broad categories could be used to morphologically classify implants from peritoneal carcinomatosis: (1) solid


Fig. 6. ‘‘Plaque-like’’ pattern. A Axial contrast-enhanced CT image showing a ‘‘plaque-like’’ implant (arrow) over the hepatic surface appearing relatively hyopdense in comparison with surrounding parenchyma, due to the presence of a mucinous component. B Axial DW black-and-white reversed-

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contrast image shows the plaque-shape implant (arrow) presenting lobulated margins and a high restriction of water movement. C Surgical intervention confirms the plaque-like implant (arrowhead).

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Fig. 7. ‘‘Mass-like’’ pattern in a 56-year-old patient with colon cancer. A Axial contrast-enhanced CT image showing a large inhomogeneous soft-tissue mass (arrow) located in the left iliac fossa. B Axial DW image shows the huge implant

(arrow) appearing as a hyperintense mass with restricted diffusion of water molecules. C Surgical intervention confirms the bulky malignant mass (arrow).

implants, (2) cystic implants, (3) mixed implants with either a solid component or a cystic component (Fig. 1). Solid implants and the solid component of mixed implants are characterized by soft tissue showing hypointensity at T2 WI, hyperintensity at DWI, and high density or relatively hypodensity at contrast-enhanced CT according to the extent of vascularization of neoplastic tissue [14]. Cystic implants and the cystic component of a mixed implant may generally correspond to necrotic or fluid areas and mucinous collections and always appear hyperintense at T2 WI, hypointense, or hyperintense at DWI according to protein component and hypodense at CT [15]. All types of implant categories

may be partially calcified showing hypointense spots at MRI and hyperdense spots at CT (Fig. 2) [14, 16]. Solid, cystic, and mixed implants may present with different patterns that depict typical aspects of peritoneal carcinomatosis.

Micronodular pattern Micronodular pattern is characterized by the presence of tiny 1–5 mm milky spots of peritoneal implants diffusely involving the tunica serosa and subserosal fat. Greater omentum, lesser omentum, and mesentery are typically involved (Fig. 3).

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Plaque-like pattern This aspect is typically found in the subdiaphragmatic spaces and is due to the confluence of multiple nodular implants. Plaques are irregular soft-tissue thickenings of inconstant extension that coat abdominal viscera and peritoneal walls usually appearing as soft tissue scalloping the liver and splenic surfaces and presenting a lower attenuation than the parenchyma on contrast-enhanced scans (Fig. 6) [18].

Mass-like pattern Mass-like pattern is typically found in the pelvis and arises from the same mechanism of ‘plaque-like’ appearance. In this case, the confluence of multiple nodular implants can lead to the formation of tissue mass which can reach sizes of several centimeters. When an individual mass is about 10 cm in diameter or larger it is called ‘‘bulky tumor’’ (Fig. 7).

Teca aspect Small bowel loops appear completely enveloped by a thickened layer of visceral peritoneum that covers the bowel loops as a sleeve. Sometimes neoplastic tissue that completely coats small bowel loops causes small bowel obstruction with consequent dilatation of proximal loops, a condition called ‘‘ileal freezing’’ (Fig. 8) [14].

Neoplastic ascites Fig. 8. ‘‘Teca Aspect’’ and small bowel obstruction. A Coronal contrast-enhanced CT image showing small bowel loops completely coated by a thickened visceral peritoneum. Neoplastic tissue has caused small bowel obstruction with consequent dilatation of proximal loops, a condition called ‘‘ileal freezing’’. B Surgical specimen showing severe dilatation of small bowel loops due to obstruction.

Nodular pattern Nodular pattern is characterized by the presence of >5 mm nodular implants diffusely involving the tunica serosa and subserosal fat (Fig. 4). Nodules may have an oval shape with rounded contours or a star-shaped appearance with spiculated margins providing a stellate pattern.

Omental cake Omental cake consists of a diffuse nodular involvement of the greater omentum in association with fibrotic tissue reaction leading to a consolidation of the omental fat that seems to be stratified (Fig. 5) [14, 17].

The presence of ascites must be very carefully checked because its presence within peritoneal cavity is usually one of the first ‘‘sign and way’’ of carcinomatosis. In patients with peritoneal carcinomatosis, an increased peritoneal fluid, or ascites is usually seen. This finding may be due to increased capillary permeability and fluid production or to obstructed lymphatic vessels and decreased absorption [17]. CT scan is acquired in the supine position and during inspiration and consequently fluid accumulates in the subdiaphragmatic spaces, paracolic gutters, and dependent peritoneal recesses. In some cases, also in advanced stages, there is only little or absent ascites.

Localization The localization of peritoneal implants is extremely important for the presurgical and pretreatment evaluation of peritoneal carcinomatosis. Radiologists must specify every site of peritoneal carcinomatosis to provide a staging as precise as possible. The best rule is to carefully check the surface of the bodies covered by the peritoneal layer, all peritoneal ligaments, and surrounding peritoneal spaces. To obtain a precise evaluation of

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Fig. 9. Involvement of mesenteric root. A Coronal contrastenhanced CT scan showing neoplastic involvement of the mesenteric root, which appears retracted (arrow) with sub-

sequent attraction of small bowel loops (curved arrow). B Surgical image shows multiple tiny nodules of carcinomatosis (arrowhead) diffusely involving the mesenteric root.

peritoneal carcinomatosis and to map peritoneal implants, some radiologists commonly use the evaluation system proposed by Sugarbaker that allows to calculate the Peritoneal Cancer Index (PCI) according to size, location, and number of lesions. It consists of subdividing the abdomen into 12 abdomino-pelvic areas (9 areas + 4 relating to small bowel) and assigning a score from 0 to 3 to each specific areas according with lesions’ size reaching a maximum score of 39 [20]. In the upper mesocolic space, peritoneal implants can frequently involve hepatic and splenic surfaces and hila that might be associated with intraparenchymal infiltration. The gastric surface, lesser omentum, and its parts formed by the gastro-hepatic and gastro-duodenal ligaments are frequently involved by peritoneal implants. Tumors can be recognized in the gallbladder fossa and over the gallbladder surface, over the falciform ligament, frenocolic ligament, gastro-splenic ligament, and gastrocolic ligament [14, 17]. Visceral peritoneum over small bowel loops and colonic surface can be involved by malignant tissue, causing eventually bowel distortion, bowel wall thickening, and bowel obstruction. The presence of pathology involving the Treitz ligament, small bowel, and mesenteric root is crucial for preoperative staging because it is used as an exclusion criterion of surgical intervention (Fig. 9). Also the mesentery, right, and left paracolic gutters, ileocecal region and appendix must be carefully checked. In the pelvis, pertitonal implants can be found over pelvic organs as the uterus, ovaries, urinary bladder

dome, rectum and rectovesical pouch or rectouterine pouch (pouch of Douglas) [21]. Some neoplastic nodules may involve the abdominal wall or retroperitoneal space. Neoplastic cells reach these sites through direct infiltration from the abdominal cavity or through metastatic hematogenous or lymphatic diffusion. In particular, subcutaneous metastases in the periumbilical area have been widely described and known as Sister Mary Joseph’s nodules (Fig. 10).

Role of CT and DW imaging CT is able to give accurate preoperative or pretreatment information on morphology, size, location of peritoneal implants, lymph node enlargement and presence of ascites [15, 22]. Recently, the accuracy of computed tomography in the diagnosis of peritoneal metastases has improved primarily due to the introduction of spiral CT and secondarily to a greater awareness of imaging findings in peritoneal disease [15, 18]. Previous studies showed an overall sensitivity and specificity of >16-detector row CT in the detection on peritoneal deposits ranging, respectively, from 60% to 93% [16, 23] and from 96% to 100% [16, 19]. Multidetector CT has several advantages: it can be performed rapidly and relatively easily, it is free from misregistration artifacts, thin sections provide the detection of subcentimeter implants, and a large volume of tissue can be obtained [14, 16]. CT examination allows exploration of the entire abdomen, especially certain sites that are difficult to


Fig. 10. Sister Mary Joseph’s Nodule indicates a periumbilical subcutaneous metastasis form peritoneal carcinomatosis. A Axial contrast-enhanced CT shows a solid nodule (arrow) appearing to involve the greater omentum, linea alba and subcutaneous tissue. B Surgical specimen of periumbilical node (arrow).

evaluate at surgery. These sites are represented by the diaphragm, splenic hilum, stomach, lesser sac, liver, mesenteric root, and the paraaortic nodes [14, 24]. Detection of lesions at these sites and in other abdominopelvic regions is clinically helpful to develop scoring systems for predicting the success of surgery, like the PCI, proposed by Sugarbaker and to eventually determine if patients are candidates for neoadjuvant chemotherapy prior to surgery [25–30]. In particular, axial images enable evaluation of the lesser omentum, mesenteric root, falciform ligament, gallbladder fossa, bowel wall, hepatic hilum, and splenic hilum. The use of multiplanar reformatted images, like coronal ones, allow a better evaluation of paracolic gutters, extent of omental disease, and number and location of implants over the hepatic and splenic surface. Sagittal reformatted images allow assessment of the vaginal cuff, cul-de-sac, peritoneal surface of the bladder, and rectosigmoid colon [17].

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Intravenous injection of contrast material may also assess the enhancement degree of masses [30], depict relationship of nodules to viscera and blood vessels as it would appear at surgery and show them especially using three-dimensional display of the data. MDCT imaging of peritoneal carcinomatosis can be compromised by the small size of cancer implants. CT sensitivity tends to reduce to 7–50% when malignant peritoneal deposits have a low volume measuring less than 1 cm [24, 26, 29]. On the contrary, DWI has been shown to improve sensitivity for minute hypercellular implants of peritoneal malignant tissue due to increased contrast between the hyperintense spot of malignant tissue and around hypointense normal tissue [31–33]. Another disadvantage of CT is the identification of neoplastic implants in challenging anatomic sites. The reported per-site sensibility of CT for the localization of peritoneal implants is only 25–37% [28]. In a study by Low et al., the association of DWI and traditional MR sequence seems to improve the accuracy for disease detection in 15 of 16 anatomic sites [34]. DWI, providing signal suppression from surrounding ascites, bowel contents and fat, increases the contrast-to-noise-ratio. That enhances detectability of peritoneal implants located in some abdominal sites usually difficult to evaluate using MDCT due to the complexity of anatomic relationships. Most of these sites are the right and left subdiaphragmatic space, hepatic hilum, small bowel wall, colonic wall, falciform ligament, gallbladder fossa, Treitz ligament, mesenteric root, uterine surface, and the bladder dome [34, 35]. DWI seems to improve detection of malignant deposits in most of these abdominal areas and in particular permit better assessment disease involving the mesenteric root, Treitz ligament, small bowel wall, and hepatic hilum (Fig. 11). Evaluation of these three sites is somewhat crucial to definitely exclude patients’ candidacy for surgery. Disadvantages of DWI are mainly related to the low spatial resolution and some possible pitfalls. The diffusion-weighted is fundamentally a T2-weighted sequence with fat suppression. Therefore, tissues presenting long T2 relaxation time, such as cysts or post-surgery edema, may appear hyperintense on high b value images due to high freedom of movement of water molecules, a phenomenon called ‘‘T2 shine through’’. This effect can cause a misinterpretation and increase of false positive findings when high b value images are analyzed without aid of ADC map. High signal intensity on the ADC map argues for T2 shine through effect, while low value of intensity is associated with a real restriction of water diffusion [22]. As mentioned earlier, the increased cell density on DWI permits recognition of neoplastic tissues due to restriction of water movement represented by hyperintensity on high b value and low signal on ADC map. However, some types of tumor such mucinous ones and


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well differentiated adenocarcinomas have a lower cell density and therefore may appear hypointense on high b values [36]. Some densely cellular tissue, like fibrosis, bowel mucosa, endometrium, and normal lymph nodes present a restricted diffusion appearing hyperintense in DWI with low ADC values. Necrosis and abscesses also have high values in DWI sequences with high b values but generally present higher values on the ADC map [37].

Conclusion CT and DWI are accurate and complementary diagnostic tools to recognize and report in detail spread of peritoneal disease offering a map of neoplastic implants, and an accurate calculation of PCI score with final aim to plan the optimal patient treatment. References

Fig. 11. Challenging anatomic site. A Axial contrasted-enhanced CT image showing a soft-tissue nodule (arrow) adjacent to the portal vein, near the hepatic hilum. In this area, peritoneal implants are more difficult to detect because they tend to hide between vascular structures and the bile duct. B Axial DW image allows a clearer detection of peritoneal implant (arrowhead) that appears as a high signal intensity nodule. C At axial DW black-and-white reversedcontrast image, pertitoneal implant (arrowhead) appears as a low signal intensity nodule.

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