Ultrasound Obstet Gynecol 2005; 26: 552–557 Published online in Wiley InterScience (www.interscience.wiley.com). DOI: 10.1002/uog.2587
Transvaginal sonographic features of peritoneal carcinomatosis L. SAVELLI*, P. DE IACO*, M. CECCARONI*, T. GHI*, M. CECCARINI*, R. SERACCHIOLI* and B. CACCIATORE† *Department of Obstetrics and Gynecology, University of Bologna, Italy and †Department of Obstetrics and Gynecology, University of Helsinki, Finland
K E Y W O R D S: diagnosis; ovarian cancer; peritoneal carcinomatosis; peritoneum; transvaginal sonography; ultrasound
ABSTRACT
INTRODUCTION
Objectives Peritoneal carcinomatosis involves the dissemination of intra-abdominal tumor tissue often associated with gynecological malignancies. The objective of this study was to describe the transvaginal sonographic appearance of this condition.
Peritoneal carcinomatosis is a complex clinical–pathological condition caused by the spread of neoplastic tissue in the abdominal cavity along the peritoneal surface1 . Since a palpable abdominal mass is often absent, and symptoms are non-specific, clinical diagnosis can be difficult. The main goals of diagnostic imaging techniques are the early detection and adequate staging of tumors, in order to better define the timing of surgery and facilities and equipment required. Conventional radiology often fails to detect peritoneal carcinomatosis and supplies diagnostically relevant information only when there is extensive bowel involvement2 . A more precise visualization of peritoneal and omental implants can be achieved by transabdominal ultrasound (TAS), computed tomography (CT) and magnetic resonance imaging (MRI) even if the reported diagnostic accuracy of such techniques is very variable and often unacceptably low1 – 13 . Transvaginal sonography (TVS) is the method of choice for investigating the female pelvic anatomy; it has been used in ovarian cancer screening programs14 – 17 and when associated with color or power Doppler evaluation of vascularity18 , it is a useful tool in the diagnosis of adnexal malignancies. Surprisingly, the appearance of peritoneal carcinomatosis on TVS has not been described in the scientific literature in a large study population and, as a consequence, this condition can easily be missed even by expert sonographers and physicians. In fact, it is known that, in symptom-free women undergoing an ovarian cancer screening trial, peritoneal serous papillary carcinomas, a form of peritoneal neoplastic spread not associated with pathologic ovarian enlargement, were missed by TVS19 . We therefore conducted this retrospective study
Methods The data of 60 patients with surgically and histologically proven peritoneal carcinomatosis were analyzed. Transvaginal sonograms performed within 7 days of admission to the operating theater were reevaluated in order to identify the sonographic features associated with peritoneal carcinomatosis. Results Carcinomatosis was revealed in 53/60 cases (88%) by the presence of hypoechoic nodules attached to the peritoneum and visible on transvaginal sonography (TVS). The pouch of Douglas was the site most frequently involved. Power Doppler sonography showed the presence of blood vessels in 48 (91%) of these metastases. Ascites was found in 50 (83%) women. An adnexal mass suggestive of being the primary tumor was present in only 41 women (68%). Conclusions Peritoneal carcinomatosis has typical features on TVS and, in the vast majority of cases, its genital origin can be correctly hypothesized. Power Doppler sonography strengthens the diagnosis by showing vascularity of the peritoneal implants. In a patient with a known pelvic malignancy or whenever peritoneal carcinomatosis is suspected, TVS can give useful information in order to better assess the presence and extension of metastatic nodules within the abdominal cavity. Copyright 2005 ISUOG. Published by John Wiley & Sons, Ltd.
Correspondence to: Dr L. Savelli, Department of Obstetrics and Gynecology, University of Bologna, Via Massarenti, 13, 40138 Bologna, Italy (e-mail:
[email protected]) Accepted: 15 June 2005
Copyright 2005 ISUOG. Published by John Wiley & Sons, Ltd.
ORIGINAL PAPER
Sonography of peritoneal carcinomatosis
553
to describe the preoperative TVS and Doppler findings in a large population of women with surgically and pathologically proven peritoneal carcinomatosis.
METHODS Data from 60 consecutive patients with a proven diagnosis of peritoneal carcinomatosis, who underwent surgery in the two participating centers (Helsinki University Hospital, Finland and Bologna University Hospital, Italy) between November 1999 and December 2002 were analyzed. Indications for TVS are given in Table 1. Four women had already been operated on for an ovarian malignancy and were subsequently referred for routine sonographic follow-up while, in the other 56 patients, the indications for TVS were as follows: suspected gynecological cancer due to a palpable adnexal mass in 34 (57%) cases, inconclusive CT examination and an elevated CA 125 serum level in 8 (13%), and non-specific abdominal symptoms (abdominal/pelvic pain, abdominal swelling, constipation) in 14 (23%). Ultrasound scans were performed within 10 days of admission to the operating theater by two experienced investigators (L. S., B. C.) using commercially available equipment with color and power Doppler capabilities (ATL HDI 5000, Philips, in Helsinki from November 1999 to August 2001 and Technos MP, Esaote, in Bologna from September 2001 to December 2002). A TVS scan of the pelvic organs was performed with a 5.0–9.0-MHz broadband endovaginal transducer and was followed by a transabdominal scan with a 3.5–5.0-MHz convex transducer, to evaluate the upper pelvis and the abdomen. All examinations were carried out in a systematic and predetermined manner, with an examination time of about 10–15 min. The first 20 patients were recruited from Helsinki and evaluated by an examiner from each center (L. S. and B. C.) in order to determine the optimal ultrasound examination procedure, which was undertaken for all subsequent examinations in both centers. The sonographic images of all the patients were reviewed, together with the surgical reports and histological diagnoses. Transvaginal scans of the pelvic organs were performed first, in longitudinal and transverse views, to evaluate the anatomy of the uterus, the ovaries and the pouch of Douglas, and were followed by a transabdominal scan to study the upper abdomen, particularly the omentum, and the parietal and visceral peritoneum. In patients who Table 1 Indications for transvaginal sonography Indication
had already undergone surgery for ovarian or uterine malignancy we investigated the empty pelvis first on a longitudinal section, keeping the bladder (easily detectable if distended by a small amount of urine) on one side of the screen, and the rectum (a tubular hyperechoic structure delimited by hypoechoic walls) on the other. In this position the transvaginal probe can be tilted from one pelvic side wall to the other maintaining a longitudinal plane. Such an examination should be integrated with a second scan, obtained by rotating the vaginal probe by 90 degrees, in order to obtain a transverse section of the pelvis. In this plane the true pelvis can be visualized from one side wall to the other, integrating the images of the longitudinal section. Diagnostic criteria suggestive of peritoneal carcinomatosis were the following: • the presence of discrete, solid hypoechoic nodules, devoid of peristaltic movements, growing on the pelvic peritoneal surfaces (Figures 1 and 2); • gross hypoechoic strands of tissue entrapping bowel loops (Figures 3 and 4); • free abdominal fluid, irrespective of its quantity and appearance (transonic or particulate); • at TAS, the visualization of a thickened and rigid omentum (Figure 5). Any solid peritoneal mass suspected of being neoplastic was evaluated by means of power Doppler ultrasonography, with a pulse repetition frequency (PRF) of 750 Hz and a wall filter of 50 Hz to detect very low-velocity blood flow. Then, pulsed Doppler ultrasonography was used in multiple samples to evaluate flow characteristics – the resistance index (RI; the ratio of the difference between peak systolic velocity and end diastolic velocity to peak systolic velocity) and the pulsatility index (PI; peak systolic velocity minus end diastolic velocity divided by mean velocity). In each case, the lowest value of the RI
Sheet-like implants Nodular implant
n (%)
Suspected gynecological cancer Inconclusive CT scan Non-specific symptoms Follow-up for ovarian cancer
34 (57) 8 (13) 14 (23) 4 (7)
Total
60 (100)
CT, computed tomography.
Copyright 2005 ISUOG. Published by John Wiley & Sons, Ltd.
Figure 1 Transvaginal sagittal scan of the pouch of Douglas showing several solid hypoechoic neoplastic implants growing on the peritoneal surface. They appear as nodular or sheet-like non-peristaltic masses attached to the peritoneum. The presence of ascitic fluid clearly outlines such metastases.
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Figure 2 The same patient as in Figure 1: power Doppler ultrasonography reveals several blood vessels arising from the underlying peritoneum, branching within the hypoechoic tissue. This feature confirms the neoplastic nature of the nodules, ruling out the presence of blood clots or debris.
Neoplastic bridges
Bowel
Figure 3 Transvaginal scan of the true pelvis showing bowel loops encircled and entrapped by thick hypoechoic tissue.
and the PI was registered. Digital ultrasound images were recorded and stored on a hard disk for subsequent review and analysis.
RESULTS Clinical characteristics of the study population and histological origin of peritoneal carcinomatosis are reported in Tables 1 and 2. Sixty patients (mean age 61 years, range 36–81) fulfilled the inclusion criteria of a surgically and histologically proven diagnosis of peritoneal carcinomatosis. Twenty-five of the women (42%) were premenopausal, 35 (58%) postmenopausal. Serum CA 125 levels were assessed in 58 women; they were over 35 IU/ml in 55 (95%) of them (mean 1299 IU/mL, range 18–13 720). Sonographic characteristics of the patients are summarized in Table 3. Single or diffuse peritoneal lesions were
Copyright 2005 ISUOG. Published by John Wiley & Sons, Ltd.
Figure 4 Transvaginal scan showing peritoneal implants connecting the small bowel to the pelvic side wall.
found in 53 (88%) women. These appeared as nodular or sheet-like hypoechoic structures, attached to the pelvic peritoneum and devoid of peristaltic movements. The smallest peritoneal implant seen on TVS was 5 mm high and 5 mm wide. The pouch of Douglas was the site most frequently involved and easily evaluated by means of TVS. In 48/53 (91%) of these cases, irregular and randomly dispersed blood vessels suggestive of malignancy were identified by power Doppler within the hypoechoic tissue. The mean PI was 0.80 ± 0.2 (range 0.45–1.20) and the mean RI was 0.60 ± 0.2 (range 0.29–0.86). In 5/53 (9%) cases power Doppler ultrasonography revealed absence of blood flow or only scarce vascular traces within the peritoneal implants. There were four cancers of ovarian origin (three serous papillary, one undifferentiated) and one endometrial serous papillary cancer accompanied by small and flat peritoneal implants. In fifteen cases (25%), peritoneal metastases were seen to involve the bowel walls; these appeared as thick hypoechoic bridges. Such peritoneal lesions kinking or entrapping small bowel loops could be distinguished quite easily from the intestinal content, which usually appears bright owing to the presence of air and fecal material of mixed echogenicity. In all cases in which peritoneal metastases were detected at TVS in the pelvis, surgery confirmed their presence, location and aspect. Cul-de-sac fluid, suggestive of ascites, was found in 50 (83%) cases. It appeared as anechoic in 38 women and hypoechoic (small punctate echoes floating in the fluid) in 12. In 41 (68%) women, a complex adnexal mass of 3–10 cm suggestive of a gynecological malignancy was seen. Vascularization was detected by power Doppler ultrasonography within the mass in 39 (95%) women. Pulsed Doppler ultrasonography revealed low impedance to flow; the mean PI was 0.8 ± 0.2 (range, 0.40–1.2) and mean RI was 0.50 ± 0.1 (range, 0.35–0.60). In
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Sonography of peritoneal carcinomatosis
555 Table 3 Sonographic characteristics of the patients Present/absent Peritoneal metastases
Vascularization of the metastases Involvement of bowel loops Fluid in the cul-de-sac
Adnexal mass suggestive of gynecological malignancy Vascularization of the mass Thickened and rigid omentum (‘omental cake’) Vascularization of the omental cake
n (%)
Present Nodular only Sheet-like only Both Absent Present Absent Present Absent Present Anechoic Hypoechoic Absent
53/60 (88) 36/53 (68) 4/53 (8) 13/53 (24) 7/60 (12) 48/53 (91) 5/53 (9) 15/60 (25) 45/60 (75) 50/60 (83) 38/50 (76) 12/50 (24) 10/60 (17)
Present* Absent Present Absent Present Absent
41/60 (68) 19/60 (32) 39/41 (95) 2/41 (5) 26/60 (43) 34/60 (57)
Present Absent
18/26 (69) 8/26 (31)
*Mean diameter 6 cm, range 3–10 cm.
Figure 5 Transabdominal scan in a patient with surgically and pathologically proven neoplastic involvement of the omentum. (a) Gray-scale image showing a thickened and rigid omentum (‘omental cake’), outlined by the anechoic ascitic fluid. (b) Power Doppler ultrasonography reveals vascular traces within the thickened omentum. Table 2 Histologic origin of peritoneal carcinomatosis Origin
n (%)
Ovary Stomach Tube Pancreas Peritoneum Endometrium Breast Colon
40 (67) 7 (12) 5 (8) 3 (5) 2 (3) 1 (2) 1 (2) 1 (2)
Total
60 (100)
19 (32%) women, no adnexal mass or other sign of a bulky gynecological tumor was found either at TVS or at surgery.
Copyright 2005 ISUOG. Published by John Wiley & Sons, Ltd.
In 26 patients (43%), the use of TAS revealed the presence of a thickened and rigid omentum, known as the ‘omental cake’. Power Doppler ultrasonography showed the presence of blood vessels within the omentum in 18 cases (69%). In seven cases, free fluid in the abdominal cavity, indicative of ascites, was the only sonographic abnormality found in patients with peritoneal carcinomatosis. At surgery, small flat pelvic implants of 1–5 mm in diameter were seen growing on the mesothelial surfaces. In four women bulky masses were present only in the upper abdomen, attached to the mesenteric root, the omentum, and the spleen.
DISCUSSION Correct early identification of peritoneal carcinomatosis is crucial to identify women who would benefit from prompt neoadjuvant chemotherapy, in order to avoid unnecessary exploratory laparotomies and incomplete debulking surgeries20 . Unfortunately, the diagnosis of peritoneal carcinomatosis is difficult even for a skilled sonographer when the peritoneal dissemination of cancer cells is not accompanied by the presence of a bulky adnexal mass. In fact, it has been reported that, in ovarian cancer screening programs based on TVS, peritoneal carcinomatosis can easily be missed, perhaps because the transvaginal sonographic features of this condition have not yet been described19 . We have demonstrated that in the vast majority of patients with peritoneal carcinomatosis, it is possible to visualize solid peritoneal implants at TVS. These showed two distinct features, appearing either as nodular,
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Figure 6 Transvaginal scan of a peritoneal metastasis located deep in the pelvis, behind the uterus. Although ascitic fluid is absent, the small implant is visible on TVS. Power Doppler ultrasonography shows several tiny vessels arising from the peritoneum and entering the mass.
hypoechoic lesions attached to the peritoneum or as sheetlike, diffuse masses, eventually leading to the covering of the entire pelvis. The close proximity to the rectouterine space and the high-frequency probes available nowadays permit images of very high quality to be obtained and thus even small peritoneal implants can be visualized. Moreover, the presence of free fluid in the pelvis clearly outlines any solid peritoneal nodule, allowing easier detection on TVS. On CT, the diagnosis of peritoneal carcinomatosis is prompted by the visualization of ascites and gross thickening of the parietal peritoneum, which may be late signs of neoplastic spread21 . It is known that the pouch of Douglas is the primary site of ascitic pooling and metastatic growth deriving from an abdominal tumor22 . Therefore pelvic metastases are likely to be found here at a very early stage of the disease, and thus could be visible at TVS if the sonographer is aware of their appearance. Power Doppler ultrasonography has been proven to be highly efficient in showing blood vessels within neoplastic tissue18 . Thus, its use can help in differentiating true metastases from blood clots and debris, which at times can be difficult to distinguish by conventional grayscale B-mode sonography. In the present study, power Doppler ultrasonography clearly demonstrated blood flow in 91% of the metastatic implants in both the parietal and the visceral peritoneum. Blood vessels with an irregular vascular architecture appeared to arise from the underlying peritoneum (Figures 2 and 6). Pulsed Doppler analysis of the waves obtained from vessels within the metastases revealed a wide range of PI and RI values. This could be explained by the variable biological conditions and clonal selection of the lesions, accounting for different speeds of growth and invasive potential.
Copyright 2005 ISUOG. Published by John Wiley & Sons, Ltd.
Savelli et al. It has been reported that contrast enhanced parietal implants on CT can also be found in inflammatory diseases of the peritoneum such as tubercular peritonitis23 . These conditions may cause similar thickening of the peritoneum with hyperemia similar to that found in our patients at TVS. Thus, a clinical differential diagnosis may occasionally benefit from chest radiography and a tuberculin skin test, together with maintenance of a high index of suspicion in populations at risk for tuberculosis24 . Ascites was the second most frequent sign of peritoneal carcinomatosis, seen on TVS in 50 (83%) patients. Its presence can easily be detected by TVS because the pouch of Douglas is the first site of collection of freely movable fluid in the abdominal cavity. In eight women, the presence of ascites and elevated serum CA 125 levels raised the suspicion of peritoneal carcinomatosis, even in the absence of sonographically visible peritoneal metastases. It seems reasonable that the abdominal spread of cancer cells is a continuous process which is not detectable on TVS at the earliest stages before the growth of solid peritoneal implants. For this reason we believe that, when intraperitoneal tumor spread is minimal, false negative results can be expected with any imaging technique. In such cases, immunohistochemical staining combined with conventional cytological analysis of the ascitic fluid drained by percutaneous or transvaginal puncture may confirm the presence of malignant cells in the ascitic fluid25 . An adnexal mass with malignant sonographic features was detected in only 41 patients (68%); surgery confirmed the absence of a bulky pelvic tumor in the remaining patients. Thus, 19 women were diagnosed as having peritoneal carcinomatosis even in the absence of a pelvic tumor suggestive of being the origin of the neoplasm. We believe it is important to stress this fact because a gynecologist can be asked to evaluate patients with peritoneal carcinomatosis in the case of the erroneous clinical suspicion of a mass of gynecologic origin; moreover, peritoneal carcinomatosis can develop from ovarian cancer in which the ovaries are of normal size, as in the case of peritoneal serous papillary carcinoma19 . In this study, peritoneal carcinomatosis could be identified on TVS in 88% of the cases. However, the diagnosis can be reinforced by the detection, on TAS, of a grossly abnormal and thickened omentum, known as the ‘omental cake’, which is due to the metastatic colonization of the omentum by tumor cells10 . As a consequence, the omentum appears rigid, thickened and floating in the ascites (Figure 5). Therefore, we suggest completing the examination with a transabdominal scan, which can show the extension of ascites, a thickened omentum and solid nodules attached to the anterior parietal peritoneum. In our study, power Doppler ultrasonography was able to reveal vascularity within the thick omentum in 18/26 cases (69%). Nowadays, transvaginal sonography is the initial imaging technique in female patients with abdominal and
Ultrasound Obstet Gynecol 2005; 26: 552–557.
Sonography of peritoneal carcinomatosis pelvic symptoms. It is used in several centers worldwide as a screening tool in women at high risk for ovarian cancer. Despite the heterogeneity of the study group and the descriptive nature of our study, we found that peritoneal carcinomatosis is visible on TVS if the operator is aware of the spectrum of findings and their subtle manifestations. Proper knowledge of the appearance of peritoneal implants would allow the physician to diagnose or at least suspect the presence of a disease which has metastasized to the peritoneum and, in the majority of cases, to assess the gynecological origin of the neoplasm. Further ongoing studies, aimed at evaluating the sensitivity, specificity and positive and negative predictive values of TVS will confirm the diagnostic accuracy of such techniques in detecting peritoneal carcinomatosis, especially in comparison with other imaging techniques.
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