Transvaginal Gray Scale and Color Doppler Sonography in Primary Ovarian Cancer and Metastatic Tumors to the Ovary

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1 Article Transvaginal Gray Scale and Color Doppler Sonography in Primary Ovarian Cancer and Metastatic Tumors to the Ovary Juan Luis Alcázar, MD, María José Galán, MD, Carolina Ceamanos, MD, Manuel García-Manero, MD Objective. To compare gray scale and color Doppler features of primary and metastatic ovarian carcinomas. Methods. Clinical, sonographic (gray scale and color Doppler), and histopathologic data of 143 patients with primary (n = 127 adnexal masses) and metastatic (n = 34 adnexal masses) ovarian cancer were reviewed. Morphologic gray scale parameters assessed were bilaterality, tumor volume, echogenicity, and presence of septa, papillary projections, or solid areas. Color Doppler parameters were presence of blood flow, tumor blood flow location (central versus peripheral), subjective impression of blood flow amount (scanty, moderate, or abundant), lowest resistive index, lowest pulsatility index, and maximal peak systolic velocity (centimeters per second). Results. No statistical differences were found in bilaterality, tumor volume, presence of septa, papillary projections or solid areas, presence of blood flow, tumor blood flow location, subjective impression of blood flow amount, lowest resistive index, lowest pulsatility index, and maximal peak systolic velocity. Metastatic carcinomas were more frequently purely solid tumors (47% versus 26%; P =.001; likelihood ratio, 2.4; 95% confidence interval, ). Conclusions. The presence of a purely solid tumor indicates a higher probability of metastatic carcinoma than primary ovarian cancer. However, with the use of gray scale and color Doppler sonography, it is difficult to differentiate primary ovarian carcinomas from metastatic tumors to the ovary. Key words: color Doppler sonography; metastatic cancer; ovarian cancer; sonography. Abbreviations PSV, peak systolic velocity; RI, resistive index Received September 20, 2002, from the Department of Obstetrics and Gynecology, Clínica Universitaria de Navarra School of Medicine, University of Navarra, Pamplona, Spain. Revision requested October 16, Revised manuscript accepted for publication October 22, Address correspondence to Juan Luis Alcázar, MD, Department of Obstetrics and Gynecology, Clínica Universitaria de Navarra, Avenida Pio XII 36, Pamplona, Spain. W hen an ovarian tumor is identified as questionable at sonographic examination, primary ovarian cancer should be the main concern. However, about 5% to 30% of malignant ovarian tumors are metastatic tumors to the ovary. 1 The preoperative distinction between primary ovarian cancers and metastatic lesions might be of clinical relevance, because surgery is of the utmost importance in the treatment of primary ovarian cancer, given that optimal cytoreduction and accurate surgical staging are 2 of the most important prognostic factors in this disease. 2,3 However, this surgical effort in metastatic cancers to the ovary might not be worthwhile by the American Institute of Ultrasound in Medicine J Ultrasound Med 22: , /03/$3.50

2 Primary Ovarian Cancer and Metastatic Tumors to the Ovary In this study, we aimed to assess whether differences in gray scale and color Doppler features between primary ovarian cancer and metastatic tumors to the ovary exist. Materials and Methods In this retrospective study, clinical, sonographic, and pathologic data on 143 consecutive and unselected women diagnosed as having an ovarian malignancy (primary or metastatic) diagnosed and treated at our institution between January 1995 and December 2001 were reviewed. The mean age of the patients was 52.9 years (range, years). Fifty-seven women (40%) were premenopausal, and 86 (60%) were postmenopausal. Clinical data analyzed included age, menopausal status, clinical conditions, and physical examination findings. Physical examination findings were considered questionable in the presence of at least 1 of the following: a nonmobile pelvic mass, an irregular mass, and abdominal swelling. All patients had been evaluated by transvaginal sonography with Philips P700 SE (Philips Medical Systems, Bothell, WA) and Toshiba SSA- 370A (Toshiba Medical Systems, Co, Ltd, Tokyo, Japan) systems equipped with real-time 5- to 7- MHz sector electronic array endovaginal probes with 5.0-MHz pulsed and color Doppler capabilities. The systems operate at power outputs of less than 80 mw/cm 2 in the B-mode and pulsed and color Doppler modes. All the examinations were performed by 1 author (J.L.A.) following the same methods, described previously, 5 in each case. First, the tumor volume was calculated according to the prolate ellipsoid formula (A B C , expressed in cubic centimeters). Gray scale morphologic evaluation of the adnexal mass was performed with attention to the following parameters: bilaterality, septations, papillary projections or solid areas, and echogenicity (cystic or solid [>90% of the tumor solid]). According to these parameters, tumors were classified as unilocular cysts, multilocular cysts, unilocular cysts with solid areas, multilocular cysts with solid areas, and solid. 6 After morphologic evaluation was performed, the color Doppler gate was activated for identification of vascular color signals within the tumor. If blood flow was detected, it was shown as peripheral (color signals in the tumor wall or periphery of a solid tumor) or central (blood flow detected in septa, papillary projections, solid areas, or the central part of a solid tumor). Once a vessel was identified on color Doppler imaging, the pulsed Doppler gate was activated to obtain a flow velocity waveform. The resistive index (RI = [systolic velocity diastolic velocity]/ systolic velocity) and peak systolic velocity (PSV, centimeters per second) were automatically calculated from at least 3 consecutive flow velocity waveforms. No angle correction was attempted because of the small caliber of the vessels and their tortuous course. In those tumors with more than 1 vessel, the lowest RI and highest PSV found were used for analysis. All sonographic data were collected prospectively according to predetermined methods. 5 All patients underwent surgery, and definitive histologic diagnoses were obtained. Tumors were classified according to World Health Organization definitions. 7 Malignant tumors were staged according to International Federation of Gynecology and Obstetrics criteria. 8 The Kolmogorov-Smirnov test was used to assess the normal distribution of continuous data. Continuous data were compared by 1-way analysis of variance or the Mann-Whitney U test according to their distribution. Categorical variables were compared by the χ 2 test for dichotomous variables and the Kendall τ-b test for ordinal variables. Likelihood ratios with 95% confidence intervals were calculated where appropriate. P <.05 was considered statistically significant. All statistical analyses were performed with the SPSS 9.0 statistical package (SPSS Inc, Chicago, IL). Results Eighteen patients (12.6%) had bilateral tumors, giving a total number of 161 adnexal tumors to be analyzed. One hundred thirteen women (79%) had primary ovarian cancers (serous, 62 [55%]; endometrioid, 12 [11%]; mucinous, 11 [10%]; clear cell, 4 [3.5%]; undifferentiated, 3 [2.5%]; other, 6 [5%], and low malignant potential, 15 [13%]), and 30 (21%) had metastatic tumors to the ovary (colon and rectum, 9 [30%]; breast, 7 [23%]; endometrium, 4 [13%]; stomach, 4 [13%]; leiomyosarcoma, 2 [7%]; pancreas, 1 [3%]; cholangiocarcinoma, 1 [3%]; lymphoma, 1 [3%]; and ureteral carcinoma, 1 [3%]). Tumor stages in primary ovarian cancers were as follows: stage I, 39 (34.5%); stage II, 3 (2.7%); stage III, 55 (48.7%); and stage IV, 16 (14.1%). 244 J Ultrasound Med 22: , 2003

3 Alcázar et al The mean (SD) age of patients with primary ovarian cancer was 53.7 (14.5) years compared with 49.9 (11.8) years in the group with metastatic tumors (P =.179). No differences were found for menopausal status, clinical conditions, and physical examination findings between both groups (Table 1). The median tumor volume in primary ovarian cancers (142.7 cm 3 ; interquartile range, cm 3 ) was not statistically different from that in metastatic tumors (92.3 cm 3 ; interquartile range, cm 3 ; P =.152). Bilateral masses were present in 21 primary ovarian cancers (18.6%) and 6 metastatic tumors (20%; P =.799). All patients with bilateral masses had the same histologic findings in both tumors. On gray scale sonography, metastatic tumors were more frequently solid than primary ovarian cancers (likelihood ratio, 2.4; 95% confidence interval, ; Table 2 and Figs. 1 and 2). We found 3 primary ovarian cancers that had a unilocular cyst appearance without any gross papillary projections or solid areas. In 2 of these cases, gross macroscopic pathologic examination of the surgical pieces showed small papillary projections that were missed on sonography. The estimated volumes in these cases were and 79.1 cm 3, respectively. Two cases were stage I, and 1 was stage III. All metastatic tumors (100%) had detectable blood flow compared with 119 (94%) of 127 primary ovarian cancers (P =.205). Thirty-two (94%) of 34 metastatic tumors showed central flow compared with 114 (96%) of 119 primary lesions (P =.652). No differences were found in color Doppler findings between both groups (Table 3 and Fig. 3). Discussion Accurate preoperative differential diagnosis of adnexal masses is essential for optimizing patients treatment. In primary ovarian cancer, optimal cytoreduction and accurate surgical staging are two of the most important prognostic factors of this malignancy. 2,3 However, in the case of a tumor metastatic to the ovary, such surgical effort may be not worthwhile. 4 Therefore, the possibility of discriminating preoperatively between primary and metastatic malignant ovarian tumors could be of clinical relevance when designing a surgical approach. Transvaginal sonography has been shown to be an accurate technique for discriminating between benign and malignant adnexal masses. 9,10 However, little attention has been paid to discrimination between primary and metastatic malignant ovarian tumors. We know of only 1 published study that addressed this question. Brown and coworkers 11 evaluated the role of sonography, computed tomography, and magnetic resonance imaging to differentiate between primary and secondary ovarian malignancy. Their findings suggested that only multilocularity found on sonography and magnetic resonance imaging favored the diagnosis of primary ovarian malignancy rather than a metastatic tumor to the ovary, but they concluded that it was difficult to accurately distinguish between primary and metastatic ovarian malignancy whatever the method used. 11 Table 1. Clinical Features in Primary Ovarian Cancers and Metastatic Tumors Clinical Feature Primary Ovarian Cancer Metastatic Tumors Menopausal status, n (%)* Premenopausal 41 (36) 16 (53) Postmenopausal 72 (64) 14 (47) Condition, n (%) Asymptomatic 45 (40) 14 (47) Abdominal swelling 54 (48) 11 (37) Abdominal pain 13 (11) 3 (10) Other 1 (1) 2 (6) Physical examination findings, n (%) Questionable 64 (57) 14 (47) Nonquestionable 49 (43) 16 (53) *P =.096; P =.367; P =.410. J Ultrasound Med 22: ,

4 Primary Ovarian Cancer and Metastatic Tumors to the Ovary Table 2. Gray Scale Sonographic Appearance in Primary Ovarian Cancers and Metastatic Tumors Sonographic Appearance Primary Ovarian Cancer Metastatic Tumors Unilocular cyst, n (%) 3 (2.4) 0 Multilocular cyst, n (%) 3 (2.4) 0 Unilocular cyst with solid area, n (%) 22 (17.3) 0 Multilocular cyst with solid areas, n (%) 66 (52.0) 18 (53) Solid, n (%)* 33 (26.0) 16 (47) *P =.001. Figure 1. Transvaginal gray scale sonogram of primary ovarian cancer showing a multilocular cyst with solid nodules. Figure 2. Transvaginal gray scale sonogram of a metastatic tumor to the ovary showing a purely solid pattern. Table 3. Velocimetric Parameters in Primary Ovarian Cancers and Metastatic Tumors Parameter Primary Ovarian Cancer Metastatic Tumors Lowest RI* 0.38 (0.12) 0.39 (0.10) Lowest PI 0.75 (0.99) 0.61 (0.20) Highest PSV 26.3 (18.8) 25.8 (20.5) Values in parentheses are SDs. *P =.935; P =.405; P =.905. Figure 3. Transvaginal color Doppler sonograms of primary ovarian cancer (A) and a metastatic tumor to the ovary (B). Note the similar vascular patterns: central blood flow with similar RI, pulsatility index, and PSV values. A B 246 J Ultrasound Med 22: , 2003

5 Alcázar et al On the contrary, our findings indicated that predominantly or purely solid tumors at sonographic examination were more frequently associated with metastatic malignancies, and these tumors never appeared as unilocular or multilocular cysts without solid areas or papillary projections. These results are in agreement with some previously published studies that have shown that breast metastases to the ovary 12 and Krukenberg tumors 13,14 had a solid sonographic appearance. We also found no differences in vascular features, as assessed by color Doppler sonography, between primary ovarian cancers and metastatic tumors. This is not a surprising finding, because angiogenic phenomena in metastatic tumors have been shown to be similar to those in primary carcinomas. 15 In conclusion, we found that, although distinguishing between primary and metastatic ovarian malignancies is difficult with transvaginal gray scale and color Doppler sonography, a purely or predominantly solid tumor favors the diagnosis of a metastatic tumor rather than primary ovarian cancer. References 1. Morrow CP, Curtin JP. Tumors of the ovary: soft tissue and secondary (metastatic) tumors; tumor-like conditions. In: Morrow CP, Curtin JP (eds). Synopsis of Gynecologic Oncology. 5th ed. Philadelphia, PA: Churchill Livingstone; 1998: Piver MS. Importance of proper staging in ovarian carcinoma. Clin Obstet Gynecol 1983; 10: Hacker NF, Berek JS, Lagasse LD, Nieberg RK, Elashoff RM. Primary cytoreductive surgery for epithelial ovarian cancer. Obstet Gynecol 1983; 61: Serov SF, Scully RE, Sobin LH. International Histological Classification of Tumors, No. 9: Histological Typing of Ovarian Tumors. Geneva, Switzerland: World Health Organization; Shepherd JH. Revised FIGO staging for gynaecological cancer. Br J Obstet Gynaecol 1989; 96: Lerner JP, Timor-Tritsch IE, Federman A, Abramovich G. Transvaginal ultrasonographic characterization of ovarian masses with an improved, weighted scoring system. Am J Obstet Gynecol 1994; 170: Coleman BG. Transvaginal sonography of adnexal masses. Radiol Clin North Am 1992; 30: Brown DL, Zou KH, Tempany CM, et al. Primary versus secondary ovarian malignancy: imaging findings of adnexal masses in the Radiology Diagnostic Oncology Group study. Radiology 2001; 219: Hann LE, Lui DM, Shi W, Bach AM, Selland DL, Castiel M. Adnexal masses in women with breast cancer: US findings with clinical and histopathologic correlation. Radiology 2000; 216: Shimizu H, Yamasaki M, Ohama K, Nozaki T, Tanaka Y. Characteristic ultrasonographic appearance of the Krukenberg tumor. J Clin Ultrasound 1990; 18: Cho JY, Seong CK, Kim SH. Krukenberg tumor findings at color and power Doppler US, correlation with findings at CT, MR imaging, and pathology: case reports. Acta Radiol 1998; 39: Edel MJ, Harvey JM, Papadimitriou JM. Comparison of vascularity and angiogenesis in primary invasive mammary carcinomas and in their respective axillary lymph node metastases. Clin Exp Metastasis 2000; 18: Abu-Rustum NR, Aghajanian CA, Venkatraman ES, Feroz F, Barakat RR. Metastatic breast carcinoma to the abdomen and pelvis. Gynecol Oncol 1997; 66: Alcazar JL, Ruiz-Perez ML, Errasti T. Transvaginal color Doppler sonography in adnexal masses: which parameter performs best? Ultrasound Obstet Gynecol 1996; 8: Valentin L, Sladkevicius P, Marsal K. Limited contribution of Doppler velocimetry to the differential diagnosis of extrauterine pelvic tumors. Obstet Gynecol 1994; 83: J Ultrasound Med 22: ,

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