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Original Scientific Article
Stage 0 to Stage III Breast Cancer in Young Women
Csaba Gajdos, MD, Paul I Tartter, MD, FACS, Ira J Bleiweiss,
MD, Carol Bodian, PhD, Steven T Brower, MD, FACS
Background: Breast cancer survival is improving because
mammography is leading to diagnosis at earlier stages of the
disease. Because young women with breast cancer rarely undergo
mammography before diagnosis, outcomes for breast cancer in young
women may not be improving. In addition to advanced stage, young
age at diagnosis is associated with biologically more aggressive
cancers with higher rates of local and distant recurrence.
Study Design: Risk factors, clinical presentations,
pathologic findings, tumor characteristics, extent of disease,
treatment, and outcomes for 101 women under age 36 treated for
breast cancer between 1989 and 1997 were compared with 631 patients
36 years and older treated by us during the same interval. Stage
IV patients were excluded.
Results: Patients younger than 36 years were more likely
to present with a palpable mass (87% versus 55%, p<0.001)
and were less likely to undergo spot localization breast biopsy
for mammographic findings (40% versus 6%, p<0.001). Patients
younger than 36 years had larger tumors (median 2.0 cm versus
1.5 cm, p<0.001), more nodal involvement (50% versus 37%,
p=0.022), more nodes involved (median 1.0 versus 0, p=0.010),
and were more likely to be diagnosed with stage II or III cancer
(60% versus 43%, overall p<0.001). Young patients' cancers
were more poorly differentiated (80% versus 44%, overall p<0.001),
estrogen receptor-negative (52% versus 31%, p<0.001), aneuploid
(70% versus 49%, p=0.013), and had higher S-phase fractions (59%
versus 29%, p=0.001). Patients less than 36 years were treated
more often with mastectomy (59% versus 22%, p<0.001) and adjuvant
chemotherapy (80% versus 54%, p<0.001) and less often with
tamoxifen (36% versus 58%, p=0.001). Cumulative 5-year local
and distant disease-free survival were significantly worse for
patients younger than 36 years (p=0.011 and p=0.044, respectively).
The higher rate of local recurrence in patients less than 36
years was from an excess number of local recurrences in patients
treated with breast conservation. After consideration for nodal
involvement, chemotherapy, and tamoxifen using the Cox proportional
hazards model, no other variable, including age, was significantly
related to local disease-free outcomes. After consideration for
tumor size and nodal involvement, no other variable was significantly
related to distant disease failure rates.
Conclusions: Patients diagnosed with breast cancer
before age 36 differ from older patients in numerous respects.
They present more often with a palpable mass rather than a mammographic
finding and their cancers are more advanced with features that
are more aggressive. Despite aggressive treatment, most commonly
with mastectomy and chemotherapy, local and distant failure rates
are higher than for patients 36 and older. The higher rate of
local recurrence in patients less than 36 years reflects an excess
number of local recurrences in patients treated with breast conservation.
The outcomes of treatment for breast
cancer are improving. Five-year disease-free survival for all
patients has risen from 75% to 85%.1 This
remarkable improvement in outcomes is attributable to earlier
detection through mammographic screening. More
than half of patients diagnosed with breast cancer by mammography
have stage 0 or I disease with prospects of cure approaching
90%.2
Because screening mammography is not recommended for women
before age 35, one would not expect survival to improve for young
women diagnosed with breast cancer. Young
women diagnosed with breast cancer before having mammography
have larger tumors with more nodal involvement and higher local
and distant recurrence rates than older women do.3-6
Several of these studies suggest that young
age is an independently significant adverse prognostic factor,4-6
although this is not a universal finding.7
Young patients' local and distant disease-free survival was
found to be inferior when compared with their older counterparts
in several early reports. There was a remarkable improvement
in the outcomes of breast cancer in the last decade because of
changing treatment modalities and earlier diagnosis, which prompted
us to examine whether young patients remain at a disadvantage
compared with their older counterparts. To address this issue
we studied 101 patients aged 35 and younger and compared them
with patients aged 36 and older. We used multivariate analysis
to evaluate whether young age alone is a significant independent
adverse prognostic factor for women with breast cancer who are
diagnosed with stage III or lesser stage diseases.
METHODS
The pathology and cancer registry records of the Mount Sinai
Medical Center from 1989 to 1997 were reviewed to identify women
under age 36 at the time of diagnosis with breast cancer. From
123 patients, 15 were excluded because surgical treatment was
not completed at Mount Sinai, 5 patients were excluded because
they had distant metastases at diagnosis, and 2 patients were
missing information about treatment. The remaining 101 patients
were compared with 631 patients older than 35 whom we treated
for breast cancer during the same interval. Stage IV patients
were excluded.
Information was obtained from hospital and office records
and from patients and their families. The slides of the patients
under age 36 were reviewed by one of us (IJB). Staging
followed the criteria of the American Joint Commission on Cancer
Manual for Staging of Cancer.8 Information
was collected on age, height, weight, race, age at menarche,
pregnancies, children, age at first birth, family history of
breast cancer, smoking, clinical presentation, mammographic findings,
mode of diagnosis, histopathologic findings, tumor differentiation,
tumor size, estrogen and progesterone receptors, margins of resection,
S phase, ploidy, surgical treatment, axillary node involvement,
and adjuvant chemotherapy and radiation therapy. The last date
of followup and the date of local or distant recurrence were
recorded. The local and distant disease-free survival was calculated
from the date of the definitive operation. For estimates of local
recurrence rates patients in whom a local recurrence did not
develop were censored at the earliest of last followup or death.
Similar definitions were used for the estimates of distant disease-free
survival.
The data were analyzed using the SPSS (Statistical Package
for Social Sciences; SPSS, Inc, Chicago, IL) statistical program.
The patients were divided into two groups by age and compared.
The significance of differences in categoric variables was evaluated
using chi-square tests, and the significance of differences in
continuous variables was evaluated using Student's t-test
or Wilcoxon's rank-sum test, as appropriate. Local
and distant disease-free survival curves were calculated using
the Kaplan-Meier method.9 The significance
of differences in survival was evaluated using the Breslow test.
The Cox proportional hazards model was used to evaluate the relative
prognostic significance of each variable for both local and distant
recurrence. The influence of age at operation was allowed to
change with time because the apparent prognostic influence of
age was found to diminish during followup.
RESULTS
The patients were divided into two groups by age. The 101
patients less than 36 years ranged in age from 21 to 35 with
a mean of 32. The 631 comparison patients ranged in age from
36 to 85 with a mean of 58. Significant differences between the
two groups were noted in risk factors, clinical presentation,
pathologic findings, extent of disease, surgical and adjuvant
treatment, and outcomes.
The racial distribution of patients younger than 36 years
was significantly different from that of patients 36 years and
older (p=0.002) (Table 1). Seventy-seven percent of patients
younger than 36 years were Caucasian compared with 60% of patients
36 years and older. Patients younger than 36 years had significantly
lower body mass index (23.0 versus 26.7 kg/m2, p<0.0001) as
a consequence of both being taller (162 cm versus 159 cm, p=0.042)
and having lower body weight (62 kg versus 70 kg, p=0.001). Patients
younger than 36 years had fewer pregnancies (median 1 versus
2) and significantly fewer live births (median 1 versus 2, p<0.001)
than patients 36 years and older. A family history of breast
cancer was significantly more frequent among patients younger
than 36 years (43% versus 31%, p=0.021). Patients less than 36
years were significantly more likely to smoke (40% versus 27%,
p=0.014).
Table 1. Comparison of Patients <36 Years and >36
Years for Women Diagnosed with Stage 0 to Stage III Breast Cancer
|
|
Characteristic |
< 36 y |
> 36 y |
p Value |
|
|
n |
101 |
631 |
— |
|
Age (y) (mean) |
32 |
58 |
— |
|
(median:range) |
33:21-35 |
56:36-85 |
— |
|
Race (n) |
101 |
603 |
— |
|
Caucasian |
78 (77%) |
361 (60%) |
0.002 |
|
Hispanic |
11 (11%) |
132 (22%) |
— |
|
African American |
7 (7%) |
99 (16%) |
— |
|
Other |
5 (5%) |
11 (2%) |
— |
|
Height (cm) (mean) |
162 |
159 |
0.042 |
|
Weight (kg) (mean) |
62 |
70 |
0.001 |
|
Body mass index (kg/m2) (mean) |
23 |
26.7 |
<0.001 |
|
Age at menarche (y) (median) |
13 |
13 |
0.380 |
|
Pregnancies (median) |
1 |
2 |
0.103 |
|
Births (median) |
1 |
2 |
<0.001 |
|
Age first birth (y) (median) |
27 |
25 |
0.276 |
|
Family history breast cancer |
41/95 (43%) |
176/565 (31%) |
0.021 |
|
Smoking history |
38/96 (40%) |
135/497 (27%) |
0.014 |
|
Presentation (n) |
99 |
496 |
— |
|
Palpable mass |
86 (87%) |
273 (55%) |
<0.001 |
|
Mammographic calcium |
4 (4%) |
91 (18%) |
— |
|
Mammographic mass |
2 (2%) |
111 (22%) |
— |
|
Other |
7 (7%) |
21 (4%) |
— |
|
Mammography |
|
|
|
|
Positive/suspicious |
65/78 (83%) |
485/553 (88%) |
0.280 |
|
Diagnostic method (n) |
100 |
577 |
— |
|
Excisional biopsy |
45 (45%) |
312 (54%) |
0.154 |
|
Fine needle cytology |
50 (50%) |
229 (40%) |
— |
|
Core needle biopsy |
5 (5%) |
36 (6%) |
— |
|
Patients younger than 36 years rarely had mammography before
diagnosis and most (87%) presented with a palpable mass, which
was proved to be cancer by fine needle aspiration cytology. When
mammography was performed, usually after the diagnosis was made,
it was frequently (83%) positive. Patients 36 years and older
presented with mammographic findings significantly more frequently
(40%) and fewer presented with a palpable mass (55%). Spot localization
breast biopsy for mammographic findings was significantly more
common in the patients 36 years and older (40% versus 6%, p<0.001).
The consequence of presenting more often with a palpable mass
as opposed to mammographic findings is that patients younger
than 36 years were diagnosed with breast cancer when it was significantly
more advanced (p<0.001) (Table 2). Patients less than 36 years
had significantly larger invasive tumors (median 2 cm versus
1.5 cm, p<0.001), were more likely to have nodal involvement
(50% versus 38%, p=0.022), and had more nodes involved (median
1.0 versus 0, p=.010). The majority of patients younger than
36 years were diagnosed with stage II or III disease, but the
majority of patients 36 years and older were diagnosed with stage
0 or I (p < 0.001).
Table 2. Pathologic Findings of Patients <36 Years and
> 36 Years for Women with Stage 0 to Stage III Breast
Cancer
|
|
|
< 36 y |
> 36 y |
p Value |
|
|
Histopathology (n) |
101 |
539 |
— |
|
Infiltrating ductal |
84 (83%) |
417 (77%) |
0.337 |
|
Infiltrating lobular |
5 (5%) |
43 (8%) |
— |
|
Ductal carcinoma in situ |
12 (12%) |
79 (15%) |
— |
|
Tumor differentiation (n) |
73 |
450 |
— |
|
Well |
3 (4%) |
41 (9%) |
<0.001 |
|
Moderate |
12 (16%) |
213 (47%) |
— |
|
Poor |
58 (80%) |
196 (44%) |
— |
|
Tumor size (cm) (median)* |
2.0 |
1.5 |
<0.001 |
|
n |
89 |
504 |
— |
|
0–2 cm |
48 (54%) |
359 (71%) |
— |
|
2.1–5 cm |
32 (36%) |
110 (22%) |
0.005 |
|
> 5.1 cm |
9 (10%) |
35 (7%) |
— |
|
Estrogen-positive |
44/92 (48%) |
349/507 (69%) |
<0.001 |
|
Progesterone-positive |
35/92 (38%) |
277/493 (56%) |
0.001 |
|
Aneuploid |
28/40 (70%) |
110/225 (49%) |
0.013 |
|
High S phase |
20/34 (59%) |
59/203 (29%) |
0.001 |
|
Node-positive† |
44/89 (51%) |
145/413 (35%) |
0.023 |
|
Involved nodes (median)† |
1.0 |
0 |
0.010 |
|
Margins |
|
|
|
|
Close/involved |
21/101 (21%) |
68/423 (16%) |
0.025 |
|
Stage (n) |
101 |
538 |
|
|
0 |
12 (12%) |
79 (15%) |
|
|
I |
28 (28%) |
225 (42%) |
<0.001 |
|
II |
47 (47%) |
214 (40%) |
|
|
III |
14 (14%) |
20 (4%) |
|
|
Surgery (n) |
101 |
606 |
|
|
Breast conservation |
41 (41%) |
473 (78%) |
<0.001 |
|
Mastectomy |
60 (59%) |
133 (22%) |
|
|
Neoadjuvant chemotherapy |
11/101 (11%) |
26/631 (4%) |
0.004 |
|
Postoperative chemotherapy |
75/94 (80%) |
338/631 (54%) |
<0.001 |
|
Tamoxifen |
21/58 (36%) |
282/485 (58%) |
0.001 |
|
Radiation therapy |
45/84 (54%) |
482/631 (76%) |
<0.001 |
|
* Size of invasive component.
† Ductal carcinoma in situ.
In addition to being larger with more nodal involvement, young
patients' tumors tended to be more aggressive. Their cancers
were more poorly differentiated (80% versus 44%, p < 0.001),
more likely to be estrogen receptor-negative (52% versus 31%,
p < 0.001), more likely to be aneuploid (70% versus 49%, p
= 0.013), and more likely to have high S phase (59% versus 29%,
p = 0.001).
The majority (59%) of patients younger than 36 years were
treated with mastectomy but the majority (78%) of patients 36
years and older were treated with breast conservation (p <
0.001). Breast conservation was accompanied by radiation therapy
for all patients younger than 36 years and for 90% of the patients
36 years and older. Adjuvant chemotherapy was more frequently
used in patients younger than 36 years (80% versus 54%, p <
0.001) and tamoxifen was more frequently used in patients 36
years and older (36% versus 58%, p = 0.001).
Patients younger than 36 years fared worse than patients 36
years and older (Table 3). Patients younger than 36 years had
a significantly higher rate of both local recurrence and distant
metastases. The cumulative 5-year local recurrence-free survival
was 87% for patients younger than 36 years compared with 91%
of patients 36 years and older (p = 0.011) (Table 3; Fig. 1).
The higher rate of local recurrence in patients younger than
36 years was from an excess number of local recurrences in patients
treated with breast conservation. The cumulative 5-year local
recurrence-free survival for the 39 patients younger than 36
years treated with breast conservation was 87% compared with
94% in the 346 patients 36 years and older (p=0.036). This difference
was not attributable to a higher rate of positive margins, involved
nodes, or larger tumor size among patients younger than 36 years.
Table 3. Local and Distant Disease-Free Survival
|
|
Age |
n |
Recurred |
Cumulative 5-year recurrence-free survival |
p Value* |
|
|
Local Recurrence |
|
|
|
|
|
< 36 y |
95 |
11 |
87% |
0.011 |
|
> 36 y |
471 |
29 |
91% |
|
|
Distant Recurrence |
|
< 36 y |
97 |
13 |
84% |
0.044 |
|
> 36 y |
470 |
46 |
85% |
|
|
*p value is from the Breslow test comparing the
Kaplan-Meier survival curves.
Figure 1. Five-year cumulative survival free of local
recurrence for women under age 36 and for women ages 36 and older.
The cumulative 5-year distant disease-free survival was 84%
for patients younger than 36 years compared with 85% for patients
36 years and older (p=0.044) (Table 3; Fig. 2). This is statistically
significant because a difference in distant disease-free survival
was observed early on, but there was little difference in cumulative
survival at 5 years.
Figure 2. Five-year cumulative survival free of distant
metastases for women under age 36 and for women ages 36 and older.
Cox regression was used to evaluate the significance of age
as a prognostic factor after controlling for all other variables
potentially related to survival. Because the prognostic influence
of young age at diagnosis appeared to diminish during followup,
the estimated influence of age was allowed to change with time.
Nodal involvement (p<0.001; relative risk [RR]: 1.19; 95%
confidence limit [CL]: 1.11 to 1.28), chemotherapy (p=0.016;
RR: 0.38; 95% CL: 0.13 to 1.07), and tamoxifen (p=0.040; RR:
1.60; 95% CL: 1.00 to 2.55) were significantly related to local
disease-free survival. After consideration for nodal involvement,
chemotherapy, and tamoxifen, no other variable was significantly
related to local disease-free outcomes. Tumor size (p<0.001;
RR: 1.03; 95% CL: 1.01 to 1.04) and nodal involvement (p<0.001;
RR: 1.17; 95% CL: 1.09 to 1.24) were significantly related to
distant disease-free survival. After consideration for tumor
size and nodal involvement no other variable was significantly
related to distant disease-free outcomes. The results were similar
when the influence of age was considered as constant over time.
DISCUSSION
Many of the differences we noted between patients younger
than 36 years and 36 years and older reflect age differences
of the general population. Young breast cancer patients are taller,
thinner, and smoke more because young people in the general population
are taller, thinner, and smoke more, not because these factors
are associated with early onset breast cancer. The differences
in reproductive history we noted also may reflect changes in
the reproductive pattern of the US population.
The overrepresentation of Caucasians among patients younger
than 36 years in our study may reflect changes in the populations
our institution serves. The hospital borders East Harlem, populated
by African Americans and Hispanics, and New York's Upper East
Side, the most affluent section of New York City. Because the
population of East Harlem is younger than the population of the
Upper East Side, one would expect overrepresentation of African
Americans and Hispanics among the young breast cancer patients.
The racial differences we observed also
may be a consequence of the lower incidence of breast cancer
in African Americans and Hispanics10-12
except that, for unexplained reasons, populations with higher
rates of breast cancer do not have earlier age of onset of the
disease.10,11
The patients younger than 36 years in our study rarely had
mammography before diagnosis. Almost all
young patients are diagnosed with breast cancer after presenting
with a palpable mass.7,13,14 Mammography
is not recommended for asymptomatic women under 35 because the
high density of the breast tissue and the low incidence of cancer
limit the yield. When mammography was performed on women younger
than 36 years in our study, the malignancy was often visible.
Mammography should be used after the diagnosis is made in young
women to evaluate the contralateral breast and assess the extent
of disease on the affected side if breast conservation is entertained.
Presentation with a palpable mass increases the likelihood
of diagnosis by fine needle aspiration cytology.7 Unfortunately
a consequence of presenting with a palpable mass is that the
cancer tends to be larger and more advanced. Breast
cancers of young patients are larger with more nodal involvement
than breast cancers in older patients.3-6,15
Young patients' cancers also are more
poorly differentiated and more likely to be estrogen receptor-negative.3,5,6,16 Flow cytometry demonstrates that these cancers
are more often aneuploid and the high S-phase fractions indicate
that they are growing more rapidly than cancers in older patients.16
The surgical treatment of breast cancer in young women is
shifting away from mastectomy toward greater use of breast conservation.7
The majority of young patients are still treated with mastectomy
at our institution and the majority of older patients receive
breast conservation. Geographic differences
in mastectomy rates exist within the United States and even greater
differences exist among different countries.17-19
Some studies report higher rates of breast conservation in younger
patients than in older patients.3,6,15
High rates of breast conservation lead
to higher rates of local recurrence among young patients than
among older patients.4,5,7,14,20 Anderson
and coworkers7 noted that the rate of local recurrence among
young patients doubled as breast conservation rates rose from
1% to 14% between 1969 and 1989 at their institution. Patients
younger than 36 years in our study had higher rates of local
recurrence than patients 36 years and older only if they had
been treated with breast conservation. The proportion of patients
younger than 36 years who recurred after mastectomy was the same
as the proportion of patients 36 years and older recurring after
mastectomy. We and others3-7 could not attribute the higher rate
of local recurrence after breast conservation in young patients
to larger tumor size, a higher rate of positive margins, or to
more involved nodes.
The adverse prognostic indices of cancers in young women adversely
affect outcomes. In all available studies of patients younger
than 36, rates of distant metastases are higher and survival
is lower than for older women.3-6,14 Controversy surrounds the
question of whether age alone, after consideration of other poor
prognostic features of cancers in young women, is a significant
independent prognostic variable. In our study, as in others',3
after consideration for tumor size and nodal involvement, age
younger than 36 was not a significant independent prognostic
factor. In other studies the poor prognosis of patients younger
than 36 could not be attributed to the association of young age
with other prognostic variables.4-6
Women under age 36 diagnosed with breast cancer differ from
their older counterparts in numerous respects. The diagnosis
of breast cancer is more often made by fine needle aspiration
cytology of a palpable mass. They rarely have had mammograms
before diagnosis. In our study a surprising number of cancers
were visible on mammography. As in other studies, cancers of
women under 36 were larger, more poorly differentiated, more
often estrogen receptor-negative, aneuploid, and had higher S-phase
fractions than cancers of older women.
Acknowledgment:
We would like to thank Dennis Timony (Cancer Registry Manager)
for his assistance.
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No competing interests declared.
Received July 21, 1999; Revised November 19, 1999; Accepted
January 4, 2000.
From the Departments of Department of Surgery (Gajdos, Brower),
The Mount Sinai Medical Center, New York, NY, USADepartment of
Pathology (Bleiweiss), The Mount Sinai Medical Center, New York,
NY, USAand Department of Biomathematical Sciences (Bodian), The
Mount Sinai Medical Center, New York, NY, USA and the Department
of Surgery (Tartter), St Luke's Roosevelt Hospital, New York,
NY, USA.
Correspondence address: Paul I Tartter, MD, The Comprehensive
Breast Center, 425 West 59th St, 7A, New York, NY 10019.
JACS |
