Research Article ISSN 2639-8478

Cancer Science & Research

Assessment of Ultrasonic Doppler Findings in Patients with Suspicious

Preoperative Phyllodes Tumors
Ritsuko Yamada, MD. PhD.1,2,4*, Fumio Tsujimoto, MD. PhD.3, Takanori Okamura BS4, Motoki Miya-uchi,
BS4 and Masaru Sakurai BS4
1
Radio Isotope Research Institute, St. Marianna University School
of Medicine, Kawasaki, Japan.
Correspondence:
*
2
Yokohama Leaf Minatomirai Health Care Clinic, Yokohama, Ritsuko Yamada, MD., Ph.D., Radio Isotope Research Institute, St.
Japan. Marianna University School of Medicine, Kanagawa-ken, Japan,
Tel: +81-44-977-8111.
3
Department of Laboratory Medicine, St. Marianna University
School of Medicine, Kawasaki, Japan. Received: 30 January 2020; Accepted: 25 March 2020

Diagnostic Ultrasound Center, St. Marianna University School of

4

Medicine, Kawasaki, Japan.

Citation: Ritsuko Yamada, Fumio Tsujimoto, Takanori Okamura, et al. Assessment of Ultrasonic Doppler Findings in Patients with
Suspicious Preoperative Phyllodes Tumors. Cancer Sci Res. 2020; 3(1); 1-6.

ABSTRACT
Purpose: In this prospective study, patients with preoperative suspicious phyllodes tumor based on several
diagnostic imaging analyses were carried out ultrasonic color Doppler assessments. then investigated whether the
ultrasonographic evaluation is available in differentiate malignancy.

Subjects and Methods: Subjects studied were 72 patients diagnosed ultrasonographic phyllodes tumor. They were
divided into 5 groups based on pathological diagnosis of the surgical specimen or biopsy: 15 patients with benign
phyllodes tumor, borderline phyllodes tumor (12 patients), malignant phyllodes tumor (4), fibroadenoma (31),
breast cancer (10). Postoperative review was carried out, comparing ultrasonographic features included maximum
flow velocity (Vmax), minimum flow velocity (Vmin), and resistance index (RI) levels between 5 groups.

Results: Onset ages in borderline and malignant phyllodes tumors were higher than those in fibroadenomas and
breast cancers. Resistance Index (RI) levels in benign phyllodes tumors were, significantly lower than those in
malignant phyllodes tumors and breast cancers. Maximal flow velocity levels in breast cancer were significantly
higher than those in fibroadenoma, or benign phyllodes tumor (8.5+/-1.6cm/sec).

Discussion: It’s difficult to make the ultrasonographic diagnosis in phyllodes tumors which are 2 cm or less in
diameter to distinguish from fibroadenomas. Careful observation in internal echo lead irregular shaped cystic
component to the suspected diagnosis in phyllodes tumors. Giant tumors are not always malignant, however,
tumors characterized with enlarged, vascular rich, or accelerated proliferation are suspected to be malignant.

Conclusion: In this study of ultrasonic Doppler findings in phyllodes tumors, it is suggested that RI and maximal
velocity levels in benign ones are significantly low compared with those in breast cancers or malignant phyllodes
tumors. It’s already known that RI levels greater than 0.8 are the evidence of malignant invasive cancers. It’s
necessary to evaluate whether the high RI levels in a phyllodes tumor are applied as a clinical index of malignant
one. It’s considered that furthermore studies in many cases are expected to clarify the diagnostic ultrasonic Doppler
findings in phyllodes tumors whether those are malignant or not.

Keywords Introduction
Phyllodes tumor, Ultrasonic color Doppler assessment, Incidence of phyllodes tumors are rare, less than 1% of all breast
Fibroadenoma, Breast cancer, Resistance index (RI). tumors [1]. The age of onset in patients with phyllodes tumors is
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prominently higher than that in fibroadenoma. Their histological Doppler method, the velocity range is adjusted according to the
classification belongs to the mixed tumor that shows proliferation maximum flow velocity of the blood vessel starting from the initial
of the glandular epithelium and interstitial connective tissue, like value of 5 cm/s, the wall filter is set to low, the sampling volume is
that in the fibroadenoma. adjusted from the initial value 2 mm according to the blood vessel
diameter. The angle correction is set to 60 ° or less, then search
The glandular epithelial component is stretched strongly and expand, the waveform with carefully not to press the affected part. The
resulting in a foliate structure. Phyllodes tumors are divided into tracing of the blood flow waveform was carried out by automatic
3 categories, such as benign, borderline, and malignant ones [2]. measurement.
The remarkable findings of cellular heterotypic in interstitial non-
epithelial components, cell density, and mitosis make malignant We measured Vmax, Vmin and peripheral circulatory resistance
ones. However, epithelial components in malignant cases do not index RI levels in intra-tumoral vessels and, then compared among
show malignant findings [3]. 5 groups [4]. The difference of average values value between the
2 groups was tested by Mann-Whitney U test (IBM SPSS statics:
In this study, the maximum flow velocity (Vmax), the minimum test of 2 independent samples).
flow velocity (Vmin), and resistance index (RI), obtained from the
blood flow waveform analyses by pulsed Doppler method, were Examinations were conducted with patients’ approval within
evaluated in the patients with preoperative suspicious phyllodes the scope of routine examinations. All procedures were in
tumors, which had been diagnosed by various imaging analyses, accordance with the ethical standards of the respective committees
then examined the possibility as a available tool for differentiation (institutional and national) on human experimentation and with the
between benign and malignant phyllodes tumors. 1964 Declaration of Helsinki and later versions.

Subjects and Methods Results

From February 2006 to January 2010, 72 patients with suspicious In the preoperative ultrasonic examination, 72 patients were
phyllodes tumor were examined by preoperative ultrasonography suspected phyllodes tumor. The pathologically definite diagnoses
at St. Marianna University School of Medicine. Pathological in 72 patients were 15 benign phyllodes tumors (20.8%), 12
diagnosis of specimens by biopsy and surgery was divided into borderline phyllodes tumors (16.7%), 4 malignant phyllodes
five groups such as 15 patients with benign phyllodes tumor, tumors (5.6%), 31 fibroadenomas people (43.1%), 10 breast
12 with borderline phyllodes timor, 4 with malignant phyllodes cancers (13.8%). The breast cancers were including 1 mucinous
tumor, 31 with fibroadenomas and 10 with breast cancers. We got carcinoma and 9 ductal carcinomas.
verbal informed consent, and conducted an examination within the
scope of medical treatment. Age
The age in patients with malignant phyllodes tumor was 52.8 +/-
The statistical correlation ship was examined comparing among 11.1 year-old (average +/- standard deviation), was significantly
the definite diagnostic 5 groups, preoperative finding of B-mode higher than that in fibroadenoma (29.8 +/- 11.1 year-old, p
images and various parameters calculated from ultrasonographic <0.0005), benign phyllodes tumor (30.7 +/- 7.7 year-old, p
analyses by the pulsed Doppler methods, such as maximum blood <0.0002) and breast cancer (38.7 +/- 6.7 year-old, p <0.0132). The
flow velocity (Vmax), minimum blood flow velocity (Vmin), age in patients with borderline phyllodes tumors (44.4 +/- 7.9 years)
resistance index (RI). was significantly higher than that in fibroadenoma (p <0.0002)
and benign phyllodes tumor (p <0.0001). The age in patients with
The ultrasonic diagnostic equipments were SSA -700 (Toshiba) breast cancer was significantly higher than that in fibroadenoma (p
and EUB-8500 (Hitachi) which central frequency of the probe was <0.0198) and benign phyllodes tumor (p <0.0118).
8, 6 to 14 MHz linear electronic scanner. In B-mode examination,
we observed the shape, depth width ratio, border, boundary echo, Maximum flow velocity of intra-tumoral vessels
connective tissue spiculation, boundary line, internal echo and The Vmax of intra-tumoral blood vessels in patients with breast
posterior echo of the tumor. cancer was 16.6 +/- 1.8 cm / s (average value +/- standard
error) (Figure 1a, Figure 2), that in patients with all the kind of
The ultrasonic diagnosis of phyllodes tumor was made like those phyllodes tumor 10.3+/- 1.6 cm/s (Figure 1a, 3), and fibroadenoma
which are characterized by a slit-shaped anechoic area, an ellipsoid, 9.5+/-0.8cm/s (Figure 1a, Figure 3). The V max in patients with
lobular round, or lobular shaped low echo tumor with smooth and breast cancer was significantly higher than that in patients with
unclear border, and the internal echo is homogenous. In another fibroadenoma (p<0.0015). The Vmax in patients with malignant
cases, the internal echo are occupied mainly fascination by fibroid phyllodes tumor was 14.5+/-3.8cm/s (Figure 1a, Figure 4 and
component, however, heterogenous. Furthermore, we considered significantly lower than that in patients with breast cancer(p<0.02),
those showing internal cystic components, rather benign structure. further significantly higher than that in patients with borderline
phyllodes tumor(11.5+/-3.1 cm/s, p<0.05) (Figure 1a, Figure 5).
After confirming the blood flow wave by the color Doppler The Vmax of the benign phyllodes tumor was 8.5 +/- 1.6 cm / sec
method, the pulse Doppler method was carried out. In the pulse (Figure 1a, Figure 6).
Cancer Sci Res, 2020 Volume 3 | Issue 1 | 2 of 6
 Figure 3: Fibroadenoma organoid type in a 22 year-old patient.
a, b: Ultrasonographic findings: A space occupied lesion of 22×21×17mm in
ECD area of left breast showed clear bordered ellipsoid, and low echoic mass
with relative homogenous internal echo. The internal echo contained linear
echo with fibrous septal septal structures. This linear echo is observed when
the backscattering is enhanced in the region where the acoustic impedance
difference is large in the boundary between the duct and the fibrotic
interstitial tissue. In addition, fibrotic septum structure is rare in the inside
of fibroadenoma, and it is not seen in this case histopathology. Blood flow is
abundant. RI: 0.67, Vmax: 9.9 cm / s
c, d: Pathological features: The tumor was glandular epithelial components
rich, and also rich in blood flow,. The interstitial tissue consists of mild
proliferation of fibroblasts and dense collagenous fibers.

Figure 1: Ultrasonic pulsed Doppler finding of phyllodes tumor by

preoperative ultrasonic diagnostic examination.
a. Maximum velocity (Vmax) of intra-tumoral artery.
b. Resistance index of intra-tumoral artery.
Error bar: SE, * : p<0.05, ***: p<0.0005.

Figure 4: Malignant phyllodes tumor in a 58 year-old patient.

a, b: Ultrasonographic findings: There was a clear bordered, lobular tumor
sized more than 8 cm in right breast CD region. It contained a slit like anechoic
area. . RI: 0.68, Vmax: 18.3 cm / s.
Figure 2: Mucinous tumor, pure type, in 49 year-old patient. c, d: Pathological features: The resected tumor was sized in 9.5×9.0×8.0 mm,
a, b: Ultrasonographic finding: Lobular mass sized more than 50mm in covered with fibrous connective tissue and adipose tissue, showed yellowish-
transverse diameter, 24mm in longitudinal diameter. It showed clearer border, white and solid contents, the part of which had bleeding. Histologically, at the
and flat multiple nodular tumor Mobility with the pectoralis major was good, periphery of the tumor, there was an image of a phyllodes tumor consisting
internal echo was heterogenous, a part of anechoic area was found. There were of dilatation of lumen and mild proliferation of epithelium and proliferation
multiple small cystic area in bilateral breast. RI: 1.0, Vmax: 23.5 cm/s of breast duct-like structures and proliferation of stromal tissue. The center of
c, d: Pathological features: The tumor in the left AC region was sized 6.0 × the tumor was solid tumorous lesion consisting of fibroblast-like spindle cell
5.0 × 3.5 cm, well-defined, containing mucous in internal area, and tumor cell proliferation and somewhat myxoma-like stroma, with scattering proliferating
agglomerates with nuclear atypia are floating in a large amount of mucous cells in a mitotic stage.
The interstitial component showed especially a finding equivalent to
stored outside the cells.
myxofibrosarcoma, low grade.

Cancer Sci Res, 2020 Volume 3 | Issue 1 | 3 of 6

Figure 5: Border-line phyllodes tumor in a 48 year-old patient. patients with breast cancer.
a, b: Ultrasonographic findings: A lobular ellipsoid tumor of size 37 × 24
× 18 mm was observed in the 8 o’clock direction of the right breast and a Pathological diagnoses of breast cancer cases were 2 cases of
slit-shaped anechoic area was observed in the internal echo. Blood flow is papillotubular carcinoma, 2 cases of solid-tubular carcinoma, 2
abundant, RI: 0.61, Vmax: 6.4 cm / s.
cases of scirrhous carcinoma, 1 case of spindle cell carcinoma, 1
c, d: Pathological features: The clear bordered tumor was low density in
medullary carcinoma and 2 cases of mucinous carcinoma.
cells, however the nuclear fission feature was slightly higher at 5/10 HPF
(high power field).
Discussion
The phyllodes tumor is a solid tumor with a cystoid part including
macroscopic lobular protrusions, which shows, resembling
fibroadenoma, a hard and boundary clear lobular ellipsoid shape
developing inflatable and it’s color is pale white to yellow-brown.
While a part of fibroadenomas are accompanied by degeneration,
necrosis, infarction, and bleeding, phyllodes tumors are abundant
with the interstitial components and cellular components and the
tumor occasionally has a huge diameter of more than 5 cm [1].

Mammography findings of phyllodes tumors, as the other diagnostic

imaging analyses, showed equal to high concentration of circular or
lobular mass with clear border lining. The ultrasonic preoperative
diagnosis of phyllodes tumor was carried out based on findings
such as slit shaped anechoic area, clear border-lined smooth
surfaced ellipsoid or lobular round or lobular low echoic legion,
Figure 6: Benign phyllodes tumor hemorrhage in a23 year-old patient.
which internal echo was homogenous, while those containing large
a, b: Ultrasonographic findings: The lobular ellipsoid tumor sized in 47 sized, amount of fibrous fascination structure with heterogeneous
× 46 × 27 mm in the left breast E region was clear bordered, smooth internal echo. Furthermore, internal cystic components can be a
marginal. The internal echoes are relatively low, and showed slit-like sign of the relatively benign structured tumor [5]. As a tumor with
structures. Blood flow entering the mass was relatively abundant. RI: 0.36 less than 2 cm in diameter is especially difficult to distinguish
- 0.67, Vmax: 3.4 - 14.8 cm / s. from a fibroadenoma, we carefully observed the internal echo,
c, d: Pathological features: The mass was white, solid, and clear bordered. and if there is an irregular shaped cystic component, we suspect
The edematous fibrous interstitial tissue around the duct was proliferated it a phyllodes tumor. Although the large tumor may sometimes be
accompanied by depression of the duct. The cell density was low and the benign, but we usually considered it malignant rumor to be large,
nuclear fission images was also 0-1 / 10 HPF. blood flow rich and show rapid proliferation [6,7].

Minimum flow velocity of intra-tumoral blood vessel As a result, in the diagnosis by the ultrasonic B-mode method
The Vmin of the intra-tumoral vessels in patients with fibroadenoma and the color Doppler method (R1), 43.0% of 72 patients with
was 3.5 +/- 1.2 cm / s, that in patients with benign phyllodes tumor ultrasonographic phyllodes tumors were those with fibroadenomas,
3.9 +/- 0.6 cm / s, that in patients with borderline phyllodes tumor 43.0% were phyllodes tumors, and 13.9% were breast cancer.
4.3 +/- 1.1 cm / s, 3.7 +/- 2.1 cm / s(malignant phyllodes tumor), 2.9 Forty percent of patients with breast cancer are classified as special
+/- 0.9 cm / s (breast cancer), and the Vmin showed no significant type, in this time we showed a case of mucinous carcinoma. A
difference among the groups. fibroadenoma is easy to be misdiagnosed as a phyllodes tumor in
preoperative ultrasonography, and a fibroadenoma is easy to be
Resistance Index (RI) misdiagnosed as a mucinous carcinoma, therefore a mucinous
The RI of intra-tumoral vessels was 0.80 +/- 0.09 (mean +/- carcinoma is easy to be misdiagnosed as a phyllodes tumor
standard error) ( breast cancer), 0.619 +/- 0.024 (all the kind of [8,9]. We studied that the pulsed Doppler method is useful as a
phyllodes tumor ), 0.61 +/- 0.02 ( fibroadenoma), and the RI in diagnostic support mean. In the ultrasonic pulse Doppler method,
patients with breast cancer was significantly higher than that in the pulsatility index (PI) is defined as the value obtained by
patients with phyllodes tumor (p <0.0158) and fibroadenoma (p dividing the difference between Vmin and Vmax by the average
<0.0093). blood flow velocity Vmean per a heartbeat. That is, the value
changes depending on the heart rate. In addition, it may be a factor
The RI in patients with malignant phyllodes tumor was 0.79 +/- to increase an error that PI values measurements are necessary to
0.05, and was significantly higher than those in patients with trace the waveform manually. These are reason why we did not use
benign phyllodes tumors (0.55 +/- 0.04 (p <0.05), borderline PI, but RI. The, Vmax and Vmin values were also measured as a
phyllodes tumors (0.62 +/- 0.03 (p <0.05), and fibroadenomas (p detectable marker. As a result, it was shown that RI is significantly
<0.005) (Figure 1b). The RI in patients with malignant phyllodes higher in malignant phyllodes tumors and breast cancers than in
tumor showed no significant difference compared with that in fibroadenomas, benign phyllodes tumors, and borderline phyllodes
Cancer Sci Res, 2020 Volume 3 | Issue 1 | 4 of 6
tumors. In addition, breast cancers showed that the highest flow a high value. On the other hand, in fibroadenomas and benign
rate was significantly higher than malignant phyllodes tumors. phyllode tumors, although vascular hyperplasia is observed, they
keep anatomical structure, and neoplastic changes in surrounding
As described above, the study of B-mode ultrasonic phyllodes interstitial tissues are poor and do not significantly effect on blood
tumor was carried out pulsed Doppler measurement and calculated flow velocities. There is no increase in blood flow as much as
Vmax and RI. As a result, RI levels in B-mode phyllodes tumor breast cancer, and the blood flow waveform shows relatively low
are rather lower than those in breast cancers. The ultrasonographic in systole, relatively high in diastolic.
comparison between phyllodes tumors and fibroadenomas is not
available, and the additional information of V max and RI in vain. Although malignant phyllodes tumor is rare and is not well
known about its blood flow dynamics, but pathologically does
It is suggested that Vmax and RI obtained by pulse Doppler not contain elastic fiber, surrounding interstitial tissues are not so
method may be useful B-mode ultrasonic phyllodes tumors for hard as breast cancer, which is the reason why PI and RI levels
distinguishing among malignant, borderline and benign tumors. of malignant phyllodes tumors are intermediate values between
Chao et al. [9] demonstrated that the diagnosis of phyllodes tumors those of fibroadenoma and breast cancer. The blood flow volume
by ultrasonic B-mode is based on lobular tumor with the smooth increase followed by an increases of Vmax values in patients with
surface, lower internal echo, heterogenous internal echo without malignant phyllodes tumors may be shown so much as those with
calcification. In addition, 51.4% of patients show more than 0.7 RI breast cancers.
levels, and 51.4% of patients show more than 15 cm / s of Vmax.
The diagnoses of breast tumors are usually carried out by ultrasonic
Park HL, et al. [10] reported that phyllodes tumors show the round B-mode examination based on the other clinical findings, such as
to ellipsoid tumors without calcification, and with heterogenous age, inspection and palpation findings, mammography findings,
and cystoid internal echo by ultrasonic B-mode scanning, then etc. Taking it into account how the traditional diagnostic methods
the vacuum-assisted biopsy was carried out. They demonstrated a by B-mode scanning can be, it’s an important point that additional
conclusion that a long-term follow-up and observation is necessary technique of pulsed Doppler methods may improve diagnostic
even if they were benign phyllodes tumors. ability or not.

Bernardi G et al. [11] diagnosed as a phyllodes tumor the case of Some of Vmax, Vmin and RI values show statistically significant
which smooth marginal round shaped tumors with posterior echo differences among breast cancers, phyllodes tumors, and
enhancement or attenuation by ultrasonic B-mode scanning, and fibroadenomas, however it’s unknown how they contribute to
intra-tumoral vessels by color-Doppler methods. They reported diagnostic ability. It is necessary to verify whether these values
that it was difficult to discriminate whether it is malignant one or are clinically effective or not, whether diagnostic ability can be
not. improved by successfully combining with B-mode diagnosis, or
whether these techniques can be available to malignant phyllodes
Mishra SP et al. [12] used ultrasound diagnosis and defined the tumor. It needs to followed up by increasing the number of subjects.
phyllodes tumors that show the smooth marginal round or lobular
tumors with heterogenous internal echo and fascination structure, In this study, we examined whether malignancy of phyllodes
including higher values of RI, PI, Vmax. tumor can be judged by pulsed Doppler findings as a preliminary
trial, however further examination is expected in future cases.
In addition, Hayashi et al. [13] reported that PI and RI were high
in malignant breast tumors,. Okuno et al. [14] measured PI and Conclusion
RI using ultrasonic Doppler method to differentiate between In this study of ultrasonic Doppler findings in phyllodes tumors,
breast cancer and benign tumors, then proposed that it frequently it is suggested that RI and maximal velocity levels in benign
happens to be the malignant tumors with more than 1.3 of PI and ones are significantly low compared with those in breast cancers
more than 0.74 of RI. or malignant phyllodes tumors. It’s already known that RI levels
greater than 0.8 are the evidence of malignant invasive cancers.
In these papers, they demonstrated that PI and RI have overlapping It’s necessary to evaluate whether the high RI levels in a phyllodes
parts between benign and malignant ones, so the B-mode scanning tumor are applied as a clinical index of malignant one. It’s
are inevitable for the confirmed diagnoses. The wave form of breast considered that furthermore studies in many cases are expected
cancers are higher themselves, because pathological features of to clarify the diagnostic ultrasonic Doppler findings in phyllodes
intra-tumoral blood vessels in breast cancers proliferated among tumors whether those are malignant or not.
hard fibrous interstitial tissues, and deficiency of elastic fibers,
then showed an increase of blood flow volume. Human rights statements and informed consent
Examinations were conducted with patients’ approval within the
As a result, although higher flow velocity is shown during systole, scope of routine examinations. All procedures were in accordance
the reflux pressure in diastole is low and the flow velocity is low. with the ethical standards of the respective committees (institutional
Therefore, the blood flow waveform becomes sharp and RI shows and national) on human experimentation and with the 1964
Cancer Sci Res, 2020 Volume 3 | Issue 1 | 5 of 6
Declaration of Helsinki and later versions. The institutional review 1089-1097.
board (IRB)/ Ethics Committee of Yokohama Leaf Minatomirai 7. Bernardi G, Cavallaro G, Indinnimeo M, et al. Usefulness of
Health Care Clinic has ruled that approval was not required for this ultrasounds in the management of breast phyllodes tumors. G
retrospective study. Chir. 2012; 33: 81-85.
8. Jalaguler-Coudray A, Thomassin-Piana J. Solid masses What
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© 2019 Ritsuko Yamada, et al. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License

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