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Wo m e n ’s I m a g i n g • O r i g i n a l R e s e a r c h

Hassen et al.
Ultrasound of Ovarian Masses

Women’s Imaging
Original Research

Characterization of Papillary
Projections in Benign Versus
Borderline and Malignant Ovarian
Masses on Conventional and Color
W O M E N ’S
IMAGING Doppler Ultrasound
Kamel Hassen1 OBJECTIVE. The purpose of our study was to evaluate on endovaginal ultrasound the
Michel A. Ghossain2 morphologic and color Doppler characteristics of papillary projections in benign compared
Pascal Rousset 1 with borderline and malignant epithelial stromal ovarian tumors.
Catherine Sciot 1 MATERIALS AND METHODS. A total of 283 women (mean age, 52 years; age range,
Danielle Hugol 3 20–85 years) with 343 operated adnexal masses comprising 167 epithelial stromal tumors of
the ovary with 76 tumors containing papillary projections at pathology were retrospectively
Rafic Baddoura4
studied on ultrasound. We systematically evaluated the topography of the papillary
American Journal of Roentgenology 2011.196:1444-1449.

Dominique Vadrot 1 projections, the morphologic features of the largest papillary projection, and the presence or
Jean-Noël Buy 1 absence of color Doppler findings. All these findings were correlated with macroscopic and
Hassen K, Ghossain MA, Rousset P, et al. microscopic features.
RESULTS. Ultrasound detected papillary projections in 78% of tumors. Papillary
projections were disseminated in 33% of malignant, 20% of borderline, and 0% of benign
tumors (p = 0.0049). The mean size of the papillary projections was 9.6, 15.7, and 35.3 mm
in benign, borderline, and malignant tumors, respectively (p = 0.0007). An acute angle
was present in 68% of benign tumors and an obtuse angle in 40% of borderline and 89%
of malignant tumors (p = 0.0001). The surface was regular in 77% of benign tumors and
irregular in 50% of borderline and 88% of malignant tumors (p = 0.0000). Calcifications
were present only in benign tumors (18%). For papillary projections ≥ 10 mm, color flow was
present in all malignant, in 86% of borderline, and absent in all benign tumors.
CONCLUSION. Association of morphologic and vascular ultrasound findings can
Keywords: color Doppler imaging, ovarian neoplasm, highly suggest the diagnosis of benign or malignant papillary projection.
ovary, papillary projection

A
t pathology, papillary projections diagnosis [3, 4]. Papillary projections in be-
DOI:10.2214/AJR.10.5014
in an ovarian mass are considered nign cystic tumors have already been reported
Received May 18, 2010; accepted after revision diagnostic of epithelial stromal by different imaging techniques but, to our
November 29, 2010. tumor, commonly referred to as knowledge, no attempt was made to differen-
1
epithelial tumors, which can be benign, bor- tiate them from their borderline or malignant
Department of Radiology, Hôtel Dieu de Paris,
derline, or malignant [1–4]. This statement counterparts on the basis of morphologic find-
Assistance Publique des Hôpitaux de Paris, Université
Paris Descartes, 1 Pl du Parvis Notre Dame, 75004, Paris, applies to pathology because on ultrasound a ings [5, 6]. Thus, the primary purpose of this
France. Address correspondence to P. Rousset clot or any other amorphous material can sim- article was to retrospectively evaluate on ul-
(roussetpascal@gmail.com). ulate a true papillary projection. Papillary trasound a detailed analysis of the morpholog-
2
projection is defined at pathology as folding of ic findings of papillary projections in these tu-
Department of Radiology, Hôtel Dieu de France CHU,
Université Saint-Joseph, Beirut, Lebanon.
the proliferating neoplasmic epithelium mors correlated with macroscopic and micro-
growing over a central fibrovascular stromal scopic findings. We also reevaluated the color
3
Department of Pathology, Hôtel Dieu de Paris, core as opposed to more nondescript solid tis- Doppler findings previously described [5, 7, 8]
Assistance Publique des Hôpitaux de Paris, Université sue [1]. Papillary projections are mainly locat- in the differentiation of benign versus border-
Paris Descartes, Paris, France.
ed against the inner wall of the cyst (endocys- line and malignant tumors.
4
Faculty of Medicine, Hôtel Dieu de France CHU, tic papillary projections) or more rarely on the
Université Saint-Joseph, Beirut, Lebanon. septa or the outer wall of the mass (exocystic Materials and Methods
papillary projections). Although a definite di- From January 2003 to January 2009, with the ap-
AJR 2011; 196:1444–1449
agnosis of benignity versus malignancy or proval of our institutional review board that waived
0361–803X/11/1966–1444 borderline malignancy can only be made at the need to obtain patient consent, 345 consecutive
microscopy, macroscopic findings of these women (mean age, 50 years; age range, 18–85 years)
© American Roentgen Ray Society papillary projections can highly suggest the with a suspicion of an adnexal mass on a previous

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Ultrasound of Ovarian Masses

ultrasound or at pelvic examination were retrospec- TABLE 1:  Histology of Tumors


tively studied with endovaginal ultrasound and col-
Tumors With Papillary
or Doppler imaging.
Tumor Type No. of Patients No. of Tumors Projections at Pathology
All ultrasound studies were made by two radiolo-
gists with more than 15 and 20 years’ experience Epithelial stromal tumors 132 167 76
in gynecologic ultrasound on an ATL HDI 5000 Germ cell tumors 38 46 0
(Philps Healthcare) sonography scanner with a 5–2- Sex and stroma cell tumors 17 17 0
MHz transabdominal probe and an 8–4-MHz trans-
Endometriomas 40 56 0
vaginal probe. On color Doppler imaging, color flow
was evaluated with a pulse repetition frequency be- Functional hemorrhagic cysts 41 41 0
tween 1000 and 1500. The presence or absence of Pelvic inflammatory disease 10 11 0
Doppler flow, arterial or venous, was identified by Paraovarian cysts and hydrosalpinx 5 5 0
spectral Doppler imaging to rule out artifact.
Total 283 343 76
All gross and histologic examinations were
done by one pathologist who specialized in gyne-
cology or his assistant using the same standard- ing in a cystic portion but usually of a larger size • Its size: the largest transverse diameter (i.e., par-
ized protocol as the search for papillary projec- with a more or less round shape, homogeneous, allel to the wall or the septum) was measured.
tions and their description. or with degenerative changes (particularly necro- • The angles with the wall of the cyst: a large base of
Two hundred eighty-three women (mean age, sis). However, in some cases a clear landmark be- implantation forming an obtuse angle with the wall
52 years; age range, 20–85 years) with 343 adnex- tween papillary projection and solid tissue can be of the cyst or a short base of implantation forming
al masses underwent surgery (Table 1). Among difficult to define. In these cases, identification of an acute angle with the wall of the cyst. If the pap-
American Journal of Roentgenology 2011.196:1444-1449.

these patients, 132 had 167 ovarian epithelial stro- the echoic portion as solid tissue was retained. illary projection had an acute angle on one side and
mal tumors at pathology; 76 of 167 of these ovar- • Presence or absence of classical findings of ma- an obtuse angle on the other side, it was recorded
ian tumors had papillary projections. Papillary lignancy other than papillary projections, i.e., as having an obtuse angle. When this angle could
projections were present in 26 of 75 (35%) benign an irregular thickened septa or irregular thick- not be definitely assessed, the character of the base
tumors, 11 of 15 (73%) borderline tumors, and 39 ened wall, presence or absence of an irregu- of implantation was classified as indeterminate.
of 77 (51%) malignant tumors (Table 2). Papillary lar homogeneous or heterogeneous echogenic • The surface of the papillary projection: regular
projections were not present in nonepithelial stro- structure suggesting solid tissue [5, 9]. or irregular or indeterminate.
mal tumors at pathology (Table 1). When one or several papillary projections were • The presence or absence of calcification identified
The ultrasound examinations of the 283 women present, we systematically evaluated the following: as a hyperechoic focus with acoustic shadowing.
were reviewed by two radiologists who were blind- • The topography of the papillary projections: local-
ed to the pathologic results. They systematical- ized (< 50% of the inner surface of the cyst) or dis- Color Doppler Ultrasound
ly and retrospectively evaluated together the mass seminated (≥ 50% of the inner surface of the cyst). The presence or absence of color flow in the pap-
on contiguous sagittal and transverse still images • The morphologic features of the largest papil- illary projections (either arterial or venous as iden-
spaced 3–5 mm. Interobserver variation was re- lary projection (when multiple in a tumor, the tified by spectral Doppler ultrasound to eliminate
solved by consensus. In all 283 patients, presence largest papillary projection was considered as artifact) was reported. Spectral Doppler ultrasound
or absence of papillary projections and presence the most representative of the tumor). findings, such as resistivity index, pulsatility index,
or absence of flow in these papillary projections
were evaluated. In a second evaluation, a more de- TABLE 2:  Histology of Epithelial Stromal Tumors and Papillary Projections
tailed study as specified in the following sections
was made of tumors in which papillary projections No. of Adnexal Tumors with Papillary
were present at pathology. Histology No. of Patients Masses Projections at Pathology
Serous 33 42 25
Conventional Ultrasound Mucinous 27 27 0
For each tumor in which one or several papillary
Brenner 6 6 1
projections were detected on ultrasound and con-
firmed at pathology, we evaluated the following: Borderline serous 9 10 10
• The characteristics of the mass, whether unilat- Borderline mucinous carcinoma 5 5 1
eral or bilateral, unilocular or multilocular, and Serous carcinoma 19 32 24
its size.
Mucinous carcinoma 9 10 3
• Presence or absence of an echogenic structure
against the wall of the cyst suggesting a papillary Endometrioid carcinoma 10 13 5
projection. A papillary projection was defined on Clear cell carcinoma 4 4 3
ultrasound as a focal echoic structure against the Undifferentiated carcinoma 5 9 1
inner or outer wall or septum or protruding inside
Composite carcinomaa 5 9 3
a cystic portion or outside a mass. On the other
hand, solid tissue was defined as an echoic struc- Total 132 167 76
ture not protruding in a cystic portion or protrud- aComposite carcinoma: association of different histologic type of carcinoma in the same tumor.

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Hassen et al.

and maximum systolic velocity, were not analyzed jections in 59 tumors (22 benign, 10 border- es and thin and regular in one case. The wall
in this study because these findings have been ex- line, and 27 malignant). The size of these tu- was regular in all cases. Solid tissue was pres-
tensively studied in the literature and are of lim- mors ranged from 2.5 to 24.0 cm (mean, 8.3 ent in none of the cases. Finally, classic find-
ited value [5]. cm): 2.5 to 24.0 cm (mean, 8.4 cm) in benign ings of malignancy other than papillary projec-
tumors; 4.0 to 9.0 cm (mean, 6.2 cm) in bor- tions were present in two tumors.
Statistical Analysis derline tumors, and 4.0 to 15.0 cm (mean, 8.3 Among the 22 benign tumors with papillary
For statistical analysis, borderline and carcinoma cm) in malignant tumors. projections, 15 serous tumors were bilocular
findings were placed in one group to have enough Benign tumors were bilateral in four patients or trilocular, with thin and regular septa
values to compute the different tests. For size, we and unilateral in 14 patients. Borderline tumors and wall in all cases. Associated solid tissue
compared papillary projections < 10 mm versus pap- were bilateral in one patient and unilateral in was present in none of these cases. Classic
illary projections ≥ 10 mm. For angles, we compared eight patients. Malignant tumors were bilateral findings of malignancy other than papillary
acute angles versus obtuse and indeterminate angles. in six patients and unilateral in 15 patients. projections were present in none of 22 tumors.
For surface, we compared regular surface versus ir- Among the 27 carcinomas with papillary
regular and indeterminate surface. For location, projections, associated irregular solid tissue Detection of Papillary Projections
we compared nondisseminated versus disseminat- was observed in seven (26%) of 27 tumors; Among 343 masses of all kinds, ultrasound
ed papillary projections. The following tests were irregular thickened wall was present in two detected endocystic papillary projections in 59
performed: chi-square test with a p value of < 0.05 (7%) of 27 tumors; and septa were thickened of 76 (78%) epithelial tumors with papillary
considered statistically significant; sensitivity, spec- and irregular in two tumors, one of which projections. Among the 267 ovarian tumors
ificity, positive predictive value (PPV), negative had solid tissue. Finally, classic findings of without papillary projection at pathology, ul-
predictive value (NPV), and accuracy with evalua- malignancy other than papillary projections trasound falsely diagnosed papillary projec-
tion of the 95% CI; and multivariate analysis. were present in 10 (37%) of 27 tumors, three tions in 11/267 (4%) adnexal masses. Finally,
American Journal of Roentgenology 2011.196:1444-1449.

of which had papillary projections < 10 mm. ultrasound detected papillary projections with
Results Among the 10 borderline tumors with pap- a sensitivity of 78%, a specificity of 96%, a
Characteristics of the Mass illary projections, the tumors were unilocular PPV of 84%, an NPV of 94%, and an accuracy
Among the 76 tumors with papillary pro- in seven, multilocular in two, and bilocular in of 92%). The morphologic findings of detected
jections, ultrasound detected papillary pro- one. Septa were thick and irregular in two cas- papillary projections are shown in Table 3.

TABLE 3:  Morphologic Findings of Papillary Projections in Benign, Borderline, and Malignant Tumors
No. of Lesions Performance Value
Tumor Characteristic Benign (n = 22) Borderline (n = 10) Malignant (n = 27) Odds Ratio (95% CI) p
Size (mm) 7.46 (1.89–29.43) 0.0007
≤5 7 2 2
6–9 6 1 1
10–14 4 0 1
15–19 4 4 0
≥ 20 mm 1 3 23
Angle 11.07 (2.51–48.84) 0.0001
Acute 15 5 1
Obtuse 3 4 24
Indeterminate 4 1 2
Surface 12.33 (2.68–56.60) 0.0000
Regular 17 5 3
Irregular 1 4 21
Indeterminate 4 1 3
Dissemination ND 0.0049
Not disseminated 22 8 18
Disseminated 0 2 9
Calcificationa
Present 4 0 0
Absent 18 10 27
Note—ND = odds ratio could not be estimated because no benign lesion had disseminated papillary projections but the p value was significant.
aThe number of calcifications was too small to compute the chi-square test.

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A B C
Fig. 1—40-year-old woman with malignant papillary projections in serous cystadenocarcinoma.
A, Endovaginal ultrasound image shows 7-cm cystic ovarian mass containing endocystic papillary projections, largest one > 2 cm, with broad base of implantation
forming obtuse angle with inner wall and irregular surface. Cystic content is uniformly low echoic.
B, Color Doppler ultrasound image shows large vessels at base of papillary projection.
C, Photograph of surgical specimen shows multiple papillary projections, some of which are confluent. Scale is cm.

Among the 76 tumors with papillary pro- and one functional cyst, accumulation of mu- of 100%, NPV of 76%, and an accuracy of
jections at pathology, papillary projections cin in one mucinous cystadenoma, a small por- 88%. Color flow was absent in all papillary
were not detected on ultrasound in 17 (22%) tion of normal parenchyma protruding in a se- projections < 10 mm whether benign, bor-
of 76 tumors: four benign, 12 malignant, rous cyst, a small echogenic portion in a der- derline, or malignant (Figs. 1–3).
moid cyst, and a tubal fold in a hydrosalpinx For the assessment of tumors containing
American Journal of Roentgenology 2011.196:1444-1449.

and one borderline. In the four benign tu-


mors, the size of papillary projections was falsely considered as an ovarian cyst. Color papillary projections ≥ 10 mm, color Doppler
≤ 2 mm. These four tumors were unilocular flow was absent in all these 11 echoic struc- findings were absent in nine of nine (100%)
cysts with a thin wall and without solid tis- tures falsely considered as papillary projection. benign tumors. Conversely, color Doppler
sue, so that these tumors were preoperative- findings were present in 24 of 24 malignant
ly considered benign tumors. In the one bor- Morphologic Findings of Papillary Projections tumors and in six of seven borderline tu-
derline and 12 malignant tumors, endocystic Morphologic findings and topography of the mors, with sensitivity of 97% (95% CI, 83.3–
papillary projections could not be visualized largest papillary projection assessed in 59 tu- 99.9%), specificity of 100% (95% CI, 66.4–
in 12 tumors in which the size of papillary mors (22 benign, 10 borderline, 27 malignant) 100%), PPV of 100%, NPV of 90%, and an
projections was ≤ 2 mm and in one tumor (Figs. 1–3) showed that dissemination, size, accuracy of 97%.
in which the size was 5 mm; moreover, in wide angle, and irregular surface were indica-
these 13 tumors, exocystic papillary projec- tive of malignancy (p values in Table 3). Cal- Multivariate Analysis
tions with size ≤ 5 mm were invisible in six cification was indicative of benign lesions, but Three variables were dropped from the
tumors. It must be noted that in all these 13 we did not have sufficient data to compute the multivariate analysis because they were ful-
cases, malignant irregular solid tissue was chi-square test. ly predictive of the outcome of interest—that
present, and therefore these cases were con- is, malignancy (presence of color Doppler
sidered malignant preoperatively. Color Doppler Findings in Papillary Projections flow in the papillary projection and dissemi-
Among the 267 ovarian tumors with­out Color Doppler findings were present in 30 nation of papillary projections ≥ 50% of the
papillary projection at pathology, papillary of 37 borderline and malignant tumors and surface) or benignity (presence of calcifica-
projections on ultrasound were falsely iden- absent in all 22 benign tumors, with sensi- tions in the papillary projection). Therefore,
tified in 11 (4%) of 267 cases. These cases tivity of 81% (95% CI, 64.8–92.0%), speci- we performed a logistic regression test with
were related to a clot in six endometriomas ficity of 100% (95% CI, 84.6–100%), PPV malignancy as the binary dependent variable,

Fig. 2—20-year-old woman with serous


cystadenoma.
A and B, Endovaginal color Doppler ultrasound image
(A) and photograph of surgical specimen (B) show
4-cm ovarian cyst with small group of four papillary
projections, measuring less than 5 mm at base of
implantation. Papillary projections form acute angle
with inner wall of cyst. No color flow is detected in
papillary projections. Scale is cm.
A B

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Hassen et al.

A B C
Fig. 3—58-year-old woman with serous cystadenoma.
A, Endovaginal ultrasound image discloses right cystic ovarian mass of 6 cm containing 2.5-cm endocystic papillary projection with broad base of implantation and
obtuse angle.
B, Color Doppler ultrasound image shows no vessel is detected in this papillary projection, which measured greater than 1 cm.
C, Photograph of surgical specimen shows that papillary projection seen on ultrasound corresponds to group of gathered small endocystic benign papillary projections.
Scale is cm.

and three independent binary variables signif- pecially tubal fold in a hydrosalpinx, can also or malignant masses [1, 3, 4]. However, there
icantly associated with malignancy in univar- be confused with an endocystic papillary pro- is an overlap of sizes, and our data outline the
iate analysis were included in the model: size jection. No color flow was detected in these problem of choosing a threshold. If a thresh-
American Journal of Roentgenology 2011.196:1444-1449.

of the papillary projection (using a threshold false-positive cases, but this is not sufficient old < 10 mm was chosen for benignity, there
of 10 mm or more), angle within the cyst (ob- to exclude papillary projections because color would be 13 (59%) of 22 benign, three (30%)
tuse or indeterminate versus acute), and as- flow may be absent in benign, borderline, and of 10 borderline, and three (11%) of 27 car-
pect of the surface of the papillary projection even small malignant papillary projections. cinomas. However, in these three cases of
(irregular or indeterminate versus regular). On the other hand, although not present in this malignant tumors, the small papillary pro-
Using a backward approach, only size ≥ 10 series, tubal folds in a hydrosalpinx or protru- jections were associated with solid irregular
mm and irregular or indeterminate surface sion of normal ovarian parenchyma may show tissue, and these tumors would be correct-
remained significant predictors of malignan- exceptional color flow. ly classified as malignant on the basis of the
cy, with odds ratios (95% CI) as 8.35 (1.85– Although all patients with a cyst containing solid irregular tissue. The problem would be
37.61) and 13.46 (3.15–57.52), respectively. papillary projections will likely undergo sur- with the three borderline tumors. If a thresh-
Because color Doppler flow was negative gical removal of the cyst [2], preoperative as- old ≤ 5 mm was chosen, there would be still
in all 19 subjects with size of papillary projec- sessment of a tumor or a papillary projection a problem with two borderline tumors. If a
tions < 10 mm, we looked more specifically at as benign, borderline, or malignant is funda- threshold > 20 mm was chosen for malignan-
this subgroup. None had a dissemination ≥ 50% mental, particularly in young women. This cy, papillary projections would be found in
of the surface. The presence of one of the two will help the surgeon to decide the type of 23 (85%) of 27 malignant tumors, in three
remaining characteristics, i.e., irregular sur- surgery (cystectomy, ovariectomy, or adnex- (30%) of 10 borderline tumors, and in only
face and an obtuse angle, was more common ectomy) and the surgical approach (laparos- one (5%) of 22 benign tumors.
in the presence of malignancy, with odds ratios copy or laparotomy through Pfannenstiel The angle of the papillary projection with
of 4.15 (0.42–40.79) and 1.21 (0.12–11.99), re- or midline incision). the wall could not be assessed as acute or ob-
spectively, although not statistically significant. Although several scoring systems and tuse in seven (12%) of 59 tumors. In the other
models for masses containing papillary pro- cases, an acute angle was more common in be-
Discussion jections have been suggested to character- nign tumors and an obtuse angle in malignant
As has already been reported, papillary ize papillary projections [12, 13], this study tumors, whereas no significant difference was
projections can be missed on ultrasound shows that on conventional ultrasound, topog- found in borderline tumors (Table 3).
[10] and MRI [2], mainly because of their raphy, size, and morphologic findings corre- As reported by Krigman et al. [1], the lin-
small size (< 5 mm). Papillary projections lated with macroscopic findings, and presence ing of the surface of benign papillary pro-
can also be missed because of their exocys- or absence of color flow can be used to char- jections is usually smooth, whereas papillary
tic location, as in six (8%) of the 76 cases in acterize papillary projections. projections of malignant tumors have high-
our study; however, in these cases, these exo- Benign epithelial tumors have fewer papil- ly irregular angular margins. These findings
cystic papillary projections were associated lary projections than borderline or malignant could not be clearly defined in eight (14%)
with endocystic papillary projections. masses [1, 3, 4, 14]. In our study, dissemi- of 59 tumors in our series. As for the angle
On the contrary, echogenic structures nated papillary projections (covering ≥ 50% in the other cases, there was a difference for
against the inner wall of the cyst can be false- of the surface of the tumor) were present in benign and malignant tumors but not for bor-
ly considered as papillary projections [11]. In 0% of benign, 25% of borderline, and 50% derline (Table 3).
our study, the main source of false-positive of malignant tumors. Although calcifications have been reported
findings was amorphous material, essentially At pathology, benign epithelial tumors show in carcinoma at pathology [1], calcifications of
clots; however, vascularized structures, es- smaller papillary projections than borderline a sufficient size to be detected on ultrasound

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Ultrasound of Ovarian Masses

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