The American Journal of Surgery (2015) 210, 74-79

Clinical Science

Phyllodes tumors in African American women

Harvey L. Bumpers, M.D.a,*, Talaat Tadros, M.D.b,c,
Sheryl Gabram-Mendola, M.D.c,d, Monica Rizzo, M.D.c,d,
Mersadies Martin, M.D.a, Nicole Zaremba, M.D.a, Joel Okoli, M.D.c,e

a
Department of Surgery, College of Human Medicine, Michigan State University, 1200 E. Michigan
Avenue, Suite 655, Lansing, MI 48912, USA; bDepartment of Pathology Emory University School of
Medicine, Atlanta, GA, USA; cAvon Breast Center, Grady Memorial Hospital, Atlanta, GA, USA;
d
Department of Surgery, Emory University School of Medicine, Atlanta, GA, USA; eDepartment of
Surgery, Morehouse School of Medicine, Atlanta, GA, USA

KEYWORDS: Abstract
Phyllodes; BACKGROUND: Phyllodes is a rare tumor accounting for less than 1% of all breast neoplasms. Studies
Breast tumors; defining clinical predictors of malignant phyllodes (MP) are rare and inconsistent. Furthermore, MP
Cystosarcoma occurrence in African American (AA) women has never been analyzed. This study will delineate clinical
and pathologic features in AA patients that may reasonably predict the probability of malignancy.
METHODS: A retrospective study of clinical records was carried out for 50 AA patients diagnosed
with phyllodes tumors (PT) and treated between 1982 and 2012. Patients’ charts were analyzed
regarding demographics, pathology findings, and treatment.
RESULTS: The diagnosis of benign disease was made in 40 (78%), borderline in 3 (6%), and malig-
nancy in 7 (14%) patients; however, 1 patient (2%) had mixed phyllodes with ductal carcinoma in situ.
The mean age was significantly different for patients with benign disease (33 years) compared with
those with malignancy (54 years; P , .001). The average tumor size was twice as large (11.8 vs
4.1 cm; P 5 .029) and mitoses were higher with 50% of MPs having greater than 5 per 10 high power
fields. Although rare, nodal metastasis, ulceration, and multicentric disease occurred only in MP.
CONCLUSIONS: Among AA patients with phyllodes tumors, those with malignant tumors were
older and had larger tumors and higher mitotic indices than those with benign disease. AA patients also
displayed some of the more rare features of advanced disease and presented with malignancy near the
highest reported frequency.
Ó 2015 Elsevier Inc. All rights reserved.

Phyllodes tumor (PT) is a rare and unusual breast disease
representing .3% to .9% of all breast neoplasms.1 As the
name suggests, histologically, it is characterized by large
leaf-like (phyllodes) projections due to increased stromal
There were no relevant financial relationships or any sources of support
in the form of grants, equipment, or drugs.
* Corresponding author. Tel.: (517) 267-2043; fax: (517) 267-2488.
E-mail address: harvey.bumpers@hc.msu.edu
Manuscript received July 9, 2014; revised manuscript August 30, 2014
cellularity, which distinguishes it from fibroadenoma. How-
ever, this tumor historically presents considerable challenges
regarding its nomenclature, histopathologic diagnosis, clin-
ical presentation, and treatment risks of recurrence and
metastasis. Cystosarcoma phyllodes was the earliest nomen-
clature given to this tumor. The suffix ‘‘sarcoma’’ referred to
a fleshy tumor, but it is a misnomer, as there remains histo-
logic uncertainty of predicting malignancy and metastatic
potential. This disease was appropriately reassigned the
term ‘‘phyllodes tumor’’ in 1982 by the World Health

0002-9610/$ - see front matter Ó 2015 Elsevier Inc. All rights reserved.
http://dx.doi.org/10.1016/j.amjsurg.2014.09.040
H.L. Bumpers et al. Phyllodes in African Americans
Organization.2 Since its first description by Muller in 1838,3
there have been a considerable number of studies designed to
delineate the various clinicopathologic features of PT that
suggest malignant or metastatic potential in these tumors
once thought to be strictly benign. Researchers have evalu-
ated histologic features such as stromal overgrowth, mitotic
activity, tumor size, and cellular atypia to predict malignant
potential.4,5 There still remains uncertainty regarding
consistent biologic behaviors of PT. Certainly, the biologic
behavior of breast cancer in African Americans (AAs) has
been understudied and under-reported. This study presents
data from a large group of AA patients with the opportunity
to evaluate biologic features and assess the malignant poten-
tial of PTs, thus making comparisons with already estab-
lished behavior mechanisms of growth and metastasis in
the general population. The purpose of this study is to
address the clinicopathologic features associated with ma-
lignant and metastatic behavior of PTs in AA women. Spe-
cific emphasis was aimed at correlating demographic,
clinical, and pathologic features. To our knowledge, this is
the first series that has examined PTs strictly in AAs.
Materials and Methods
A retrospective review of clinical records was conducted
between 1982 and 2012, identifying 62 patients diagnosed
with PTs and 1 with mixed phyllodes and Ductal carcinoma
in Situ (DCIS) at the Grady Memorial Hospital, Avon
Comprehensive Breast Center in Atlanta, Georgia. The
Grady Hospital patient population is approximately 90%
AA. The subjects of this review were obtained through a
search of the Pathology Department’s database. Patients’
charts were analyzed regarding demographics, pathology
findings, and surgical treatment. Of the 63 charts reviewed,
51 patients were AA, 3 white, 5 Hispanic, and 4 others
(American Indian [1], Asian [1], not recorded [2]). The
objective was to delineate clinical predictors of malignancy
among AA patients using pathologic correlation. Therefore,
we restricted the study population to the 51 AA patients.
Pathology findings included benign, borderline, malig-
nant (MP) phyllodes, and in one case, benign phyllodes
with a component of DCIS. Documents reviewed included
history and physicals, operative reports, pathology reports,
and all available progress notes. The hospital’s tumor
registry was used to determine final pathologic staging
(review by staff pathologist) and last hospital follow-up for
MP patients. A literature review was performed to compare
the findings in our AA patients with those of the general
population. Investigational review board approval was
received from Morehouse School of Medicine and Grady
Memorial Hospital.
Results
Forty of 50 (78%) were diagnosed with benign disease
and 7 of 50 (14%) were malignant and 3 of 50 (6%) were
75
borderline (Table 1). One patient presented with an
epithelial cancer (DCIS) arising within a benign PT. This
epithelial lesion was excluded from analysis but has been
discussed separately. The average age for patients with
benign disease was significantly different compared with
patients with malignancy, 33 years (12 to 57 years) and
54 years (43 to 69 years), respectively (P , .001). Fig. 1
illustrates the distribution by age. Ages were stratified to
reflect the occurrence of PTs in very young, premeno-
pausal, and postmenopausal women.
There was no difference in the frequency of benign
tumor location between the right and left sides, although
71% of malignant tumors occurred on the left (Table 1).
With regard to surgical management, 5 of 7 (72%) patients
with malignancy underwent total mastectomy, whereas 2 of
7 (28%) had wide excision of their tumors. The opposite
was true for benign tumors; 36 of 39 (92%) had wide exci-
sion and 3 of 39 (8%) had total mastectomies. For one
patient with benignity the procedure was not listed. Patients
with borderline tumors had wide excision; however, 1
patient refused definitive surgery after biopsy.
The mean tumor size for malignant lesions was signif-
icantly larger than that found in benign disease, 10.9 and
4.1 cm, respectively (P 5 .029). The mitotic index was
higher (2 per 10 high power fields [HPF]) in 67% compared
to benign tumors (Table 1).
Two of the 7 patients diagnosed with MP tumor, aged 67
and 69 years, had clinical or pathologic evidence of lymph
node metastasis (Table 1). The oldest patient had the high-
est mitotic index (37 mitoses per 10 HPF), which was asso-
ciated with both lymph node and pulmonary metastasis
(data not shown). Nodal metastasis (n 5 2), ulceration (n
5 1), and multicentric disease (n 5 1) were noted exclu-
sively in the MP patients. Of the 50 patients in this series,
1 presented with skin ulceration. She was diagnosed with
MP, which has been shown to occur at a higher frequency
when there is associated pain, ulceration, and rapid
growth.6,7 One patient with multicentric disease also had
a high mitotic index (7 per 10 HPF; data not shown).
The 3 patients with benign disease that underwent
mastectomies had an average tumor size of 14.3 cm (data
not shown). For those with MP who underwent wide
excision (n 5 2), their average tumor size was 2.5 cm.
The one PT with DCIS arising within it was 2.0 cm in
size and that patient underwent wide local excision.
MP patients were followed in the tumor registry. Accu-
rate follow-up information is available for the 7 patients
with MP (Table 2). The duration of follow-up ranged from
4 months to 140 months. In view of the relative rarity of
MP, statistical analysis of survival data with the Kaplan-
Meier test in our series will not be meaningful. At the
time of last follow-up by the tumor registry, 5 of 7 patients
(71%) with MP had no evidence of disease. One of 7
patients (14%) died from other causes 62 months from
the diagnosis of MP, but she had no evidence of disease.
The other 4 patients alive with no evidence of disease
had disease-free survival ranging from 43 to 140 months
76 The American Journal of Surgery, Vol 210, No 1, July 2015

Table 1 Characteristic of phyllodes tumors in African American women

Characteristic Benign (n 5 40) Borderline (n 5 3) Malignant (n 5 7) P value*
Average age (y) 33 30 52 .0002
Laterality .020
Right 19 2 2
Left 20 1 5
Not noted 1
Surgical management
Mastectomy, n (%) 3 (8) d 5 (71)
Wide excision, n (%) 36 (92) 2 (67) 2 (29)
Biopsy only, n (%) d 1 (33)
Not noted 1
Tumor characteristics .02 (all groups)
Mean size (cm) 4.1 5.5 10.9 .01 (BP vs MP)
6SD 5.0 5.7 8.0 NS (BP vs BLP)
Mitoses (per 10 high power fields)†
0–2 30 0 2
3–5 0 2 2
.5 0 0 3
Not available 1 1
Nodal metastasis (1) d d 2
Ulceration d d 1
Multicentric d d 1
BLP 5 borderline phyllodes tumor; BP 5 benign phyllodes tumor; MP 5 malignant phyllodes tumor; NS 5 not significant; SD 5 standard deviation.
*Significance of the distribution was calculated by performing student t test (unpaired) for BP vs MP and BLP vs MP. One-way analysis of variance was
used to compare all 3 groups.
†
Phyllodes tumors with DCIS had 0 mitoses but were not included because they were phyllodes mixed with epithelial malignancy.

(mean, 105 months). The one patient with unknown status
of disease with regard to MP had synchronous adenocarci-
noma of the vaginal cuff and died 12 months after diagnosis
and treatment of MP. The patient with high-grade MP and
pulmonary metastasis expired 4 months after diagnosis.
Comments
It is well documented that differences exist for AA
women diagnosed with breast cancer, contributing to the
poorer survival (41%) for this group of patients compared
with Caucasians.8 PT is a rare neoplasm with more
Figure 1 Age distribution of phyllodes tumors in African
American women.
unpredictable behavior. There has been no appreciable
change in the frequency of occurrence of PT during the
years (1982 to 2012) included in this study. It has remained
approximately 1% of all breast tumors and 2% to 3% of the
fibroepithelial breast neoplasms.9 Our findings report some
of the best insights into the racial prevalence of these
tumors and the level of malignant transformation and
morbidity that accompanies them. Although the number
of patients in this study is small relative to studies for
epithelial-derived breast cancers, in comparing the litera-
ture, it is of considerable size for PTs from a single institu-
tion and is very large for AA women.
The AA patients in our study with MP were significantly
older than those with benign tumors, 54 vs 33 years. The
literature seems to be inconsistent on this issue. Buchanan10
agreed with our findings that MP occurred more frequently
in older patients, whereas others11,12 reported no difference
in frequency relative to age. It is unknown if these patients
had a delay in diagnosis, as is so often the case in AA
patients with epithelial breast cancers.8 Epithelial breast
cancers usually start as very early stages of malignancy
and progress with time. The literature has shown that PTs
can transform to MP.13–15 Certainly, a long delay in diag-
nosis could result in increased malignancy in older AA
women. We found no lateralization for benign PT, although
50% more MP occurred on the left side. There was no
rational explanation for this difference except sample size.
There was a significant correlation between large tumor
size and malignancy in our patients. Although there are
H.L. Bumpers et al. Phyllodes in African Americans
Table 2 Survival for patients with malignant phyllodes tumors
Patient number Age (y) Treatment
1 43 Wide excision
2 57 Wide excision
3 47 Total mastectomy
4 47 Total mastectomy
5 46 Total mastectomy
6 67 Total mastectomy
7 69 Total mastectomy
NED 5 No evidence of disease.
supporting and conflicting arguments regarding size in
predicting malignancy,16,17 this was more clearly delin-
eated in the cases of AA women, as has been seen with
recurrence of PT in Hispanic women.18 Malignant phyl-
lodes were almost 3 times larger than benign PT
(10.9 cm vs 4.1 cm; P 5 .029). Both large tumor size
and malignant pathology led to an increased rate of mastec-
tomies in the MP patients. Features documented to occur
with rarity in the general population of patients with MP
were found in our group of AA women. There is general
agreement among most series that the highest frequency
of MP is about 25%, and in our study, the rate of malignant
transformation in 16% of AA women was near the higher
end of the spectrum.
Most reports of axillary lymph node metastasis in
phyllodes indicate occurrence with a frequency of
approximately 2%.19–22 Even when 10% of cases present
with clinical adenopathy, only 1% are pathologically
affected.23,24 We found axillary lymph node metastasis
in 2 (4%) of our patients, and this corresponded to a
rate of 29% of the 7 patients with MP. Four MP patients
underwent axillary node dissection, and large tumor size
was a common feature (range, 12 to 23 cm). This is higher
than the series noted previously but probably not signifi-
cantly different. Because malignant phyllodes usually
spread hematogenously,14 metastases often present as
distant disease as opposed to disease within regional
lymph nodes. In malignant phyllodes that are extremely
large tumors, there appears to be no role for elective axil-
lary lymph node dissection. In a series in which PTs were
malignant, extremely large, or recurrent, Chen et al25 per-
formed modified radical mastectomies for 42 of their 172
patients. They found nodal involvement in 0% of those
patients. It is very rare that PT patients will present
with distant metastasis. MP occurs in about 10% to 30%
of all PT and metastasis occurs in 10% to 30% of those
patients. In this study, 14% (1) of our MP patients was
found to have lung metastasis at the time of presentation.
In the 3 patients with distant metastases reported in
Chen’s series, lungs were the only site in 2 cases, and
lungs occurred with bone in the other case. The high fre-
quency of presentation with late-stage disease in AA
women is similar to the racial disparity that is seen with
77
Duration of
follow-up (mo) Cancer status Vital status
140 NED Alive
62 NED Deceased
43 NED Alive
125 NED Alive
111 NED Alive
12 Unknown; vaginal cuff cancer Deceased
4 Pulmonary metastases Deceased
epithelial breast cancers. It has been well documented
that most distant metastases from MP are in the lungs,
bone, and abdominal viscera.19,26,27
An even rarer event is the development of an epithelial
cancer within a PT.28 In one of our cases in this series, there
was a finding of an intraductal carcinoma in the phyllodes
with no MP stromal transformation. According to reports,
this has occurred approximately 30 times worldwide28
and only 7 times in the in the English literature.29 After
resection of these cancers, cure usually results. The high
cure rate probably occurs because the cancer is usually
completely excised because of its isolation within the phyl-
lodes. Although an intraductal tumor is reported here, infil-
trating ductal carcinomas arising within phyllodes have
also been reported with similarly high frequency of
cure.30 Tumor morbidities such as ulcerations and multi-
centricity are not commonly documented with PT, but
they were apparent in our group of patients, and only
among those with MP. AA women appear to have more
morbid disease even when the breast malignancy is
phyllodes.
Although the differentiation between benign and malig-
nant phyllodes tumor based on tissue morphology is
difficult and the risk of recurrence and metastasis is
uncertain, there are certain clinicopathologic features in
this series that represent possible predictors of malignant
potential. Patients with malignant tumors are generally
older and present with larger lesions. In addition, higher
mitotic indices correlated with an increased propensity for
more advance disease, regional lymph node metastasis, and
even distant spread of disease. Most recently, the pathologic
subclassification of PT has been modified.31This classifica-
tion recognizes benignity, borderline, and malignancy, with
borderline representing a low-grade malignancy. Benign
PTs have fewer than 2 mitoses per 10 HPF and only modest
cellular overgrowth and uniform stromal proliferation.
Borderline PTs have 2 to 5 mitoses per 10 HPF, microscop-
ically invasive borders, and moderate stromal cellularity.
MP typically has more than 5 mitoses per 10 HPF, invasive
borders, marked hypercellularity, and extensive stromal
proliferation. Of note in our series, the patient with
37 mitoses per 10 HPF had pulmonary metastasis. Those
patients with 7 or more mitoses per 10 HPF were not
78
only more likely to have malignancy but also their disease
had a more aggressive biological behavior. This was
evident in that those patients with high mitoses presented
with axillary lymph node involvement, ulcerations, or mul-
ticentricity. By current definitions, 7 mitoses per 10 HPF
represents high-grade disease. Stromal overgrowth has
been correlated with malignancy but usually fails to meet
the criteria as an isolated finding.25,32 This AA population
had a distribution of benign, borderline, and malignant
phyllodes that was 78%, 6%, and 14%, respectively.
Belkacemi et al33 reviewed a database of 443 cases of phyl-
lodes occurring over a period from 1971 to 2003, and they
noted the distribution in their population was 64% benign,
18% borderline, and 18% malignant. Patients in our study
compared favorably to theirs. It is important to distinguish
those patients with malignancy because adjuvant therapy
may be needed and close follow-up will be necessary.
Surgery is the standard of treatment for PT, including
malignancy. Preventing recurrences dictates that the mar-
gins of resection must be free. It is a general consensus that
margins should be greater than 1 cm, and breast conserva-
tion is the rule when free margins can be achieved with
acceptable cosmesis.10,20,26,34 Distant metastasis does not
occur as a result of local recurrences.35 It has also been rec-
ommended that if initial resection fails to give adequate
margins or there is local recurrence and repeated
re-excision can be done, then mastectomy becomes a last
resort.20,29 Even very small tumors have a high recurrence
with poor margins of resection. In this study, the 3 patients
with benign PT that underwent mastectomies had large
tumors (average, 14.3 cm). Total mastectomies were
reasonable treatments as not only can recurrence be high,
as previously noted, but also the risk of malignancy may
be elevated as well because in our AA patients, larger
tumors correlated with malignancy. In those patients who
had local excision for tumors that turned out to be malig-
nant (n 5 2), the average size was 2.5 cm. All margins
were free. Past recommendations of mastectomy for MP
of this size have been reversed because resection with
free margins has low recurrence. Although radiation and
chemotherapy have been used as adjuvant therapies, the
critical importance of margin-free resection must be under-
scored. In our study, 2 patients with MP and negative mar-
gins received adjuvant therapy after surgery. One was
treated with chemotherapy and radiation for a tumor that
was 13 cm and contained 13 mitoses per 10 HPF. The other
patient treated with adjuvant radiation had a 17-cm tumor
with 37 mitoses per 10 HPF. It has been suggested that
there is a role for radiation for patients with large tumors
or positive margins on resection,33,36,37 although there has
been a lack of consistency regarding recommendations
for adjuvant radiation therapy. Chemotherapy, usually the
regimen used for sarcoma, has been used with malignant
and metastatic disease with little to no effectiveness.7,38,39
As a result, there has been no defined role for radiation
or chemotherapy in malignant phyllodes.
The American Journal of Surgery, Vol 210, No 1, July 2015
Conclusions
AA patients with phyllodes present with tumors that
appear to be more aggressive since all the morbid features
that accompany malignancy were found in our group of
patients. There were clinicopathologic findings, which
indicated that (1) patients with malignant tumors are older
and have larger tumors, (2) patients with ulcerated tumors
or palpable axillary lymph nodes all had malignancy and
more aggressive disease, and (3) higher mitotic indices
represented MP and thus correlated with more locoregional
disease and distant metastasis.
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