patterns of surgical treatment for women with breast cancer in relation to age
TRANSCRIPT
ORIGINAL ARTICLE
Patterns of Surgical Treatment for Women with BreastCancer in Relation to Age
Jim Wang, PhD,* James Kollias, FRACS, MD,* Margaret Boult, BSc (Hons),*Wendy Babidge, BSc (Hons), PhD,*� Helen N. Zorbas, MB, BS, FASBP,�
David Roder, PhD� and Guy Maddern, FRACS, PhD*�
*National Breast Cancer Audit, ASERNIP-S, Royal Australasian College of Surgeons, Stepney;�Department of Surgery, Adelaide University, Queen Elizabeth Hospital, Adelaide, SA; and�National Breast and Ovarian Cancer Centre, Sydney, NSW, Australia
n Abstract: Although treatment recommendations have been advocated for all women with early breast cancer regard-less of age, it is generally accepted that different treatments are preferred based on the age of the patient. The aim of thisstudy was to assess the pattern of breast cancer surgery after adjusting for other major prognostic factors in relation topatient age. Data on cancer characteristics and surgical procedures in 31,298 patients with early breast cancer reported tothe National Breast Cancer Audit between 1999 and 2006 were used for the study. There was a close association betweenage and surgical treatment pattern after adjusting for other prognostic factors, including tumor size, histologic grade, num-ber of tumors, lymph node positivity, lymphovascular invasion (LVI), and extensive intraduct component. Breast ConservingSurgery (BCS) was highest among women aged £40 years (OR = 1.140; 95% CI: 1.004–1.293) compared to women aged51–70 years (reference group). BCS was lowest in women aged >70 years (OR = 0.498, 95% CI: 0.455–0.545). Signifi-cantly more women aged £50 years underwent more than one operation for breast conservation (20.4–24.8%) comparedwith women aged >50 years (11.4–17.0%). Women aged >70 years were more likely to receive no surgical treatment, 3.5%versus 1.0–1.3% in all other age groups (£40, 41–50 51–70 years). There is an association between patient age and thetype of breast cancer surgery for women in Australia and New Zealand. Women age £40 years are more likely to undergoBCS despite having adverse histologic features and have more than one procedure to achieve breast conservation. Olderwomen (>70 years) more commonly undergo mastectomy and are more likely to receive no surgical treatment. n
Key Words: age, breast cancer, surgery
Although treatment recommendations have been
advocated for all women with early breast cancer
regardless of age, it is generally accepted that different
treatments are preferred based on the age of the
patient. The National Breast and Ovarian Cancer
Centre (NBOCC, formerly NBCC) has developed the
Clinical Practice Guidelines for Younger Women with
Breast Cancer (1), in addition to Clinical Practice
Guidelines for the Management of Early Breast Can-
cer (2) to address younger women’s particular needs.
The outcomes of Breast Conserving Surgery (BCS)
may also differ for women of different age. Many
studies have demonstrated that young women have
worse outcomes following breast-conserving therapy
with an increased risk of locoregional recurrence (3
and other references). Other age-specific consider-
ations, such as sexuality, self-esteem, quality of fam-
ily ⁄ social life and fertility can often influence
treatment choices, treatment efficacy, and safety. The
decision making process is often shared by the patient
and her surgeon.
There are age disparities in breast cancer treatment
choices in addition to other factors such as education,
income status, insurance plan, functional status, and
comorbidity (4). Age-related breast cancer pathology
may simultaneously influence treatment decisions for
women with early breast cancer. There are conflicting
reports on the age pattern of breast cancer manage-
ment. One report suggested that the overall treatment
pattern was not affected by age, except for the small
group of patients aged >70 years who had no axillary
node biopsy or dissection (5). Rao et al. (6) concluded
that elderly patients receive less aggressive treatment
Address correspondence and reprint requests to: Dr. James Kollias,
FRACS, MD, Chair of the royal Australasian College of Surgeons, Section of
Breast Surgery, Chair of the Breast Surgeons Society of Australia, New
Zealand and Clinical Director of the National Breast Cancer Audit, PO Box
553, Stepney, 5069 SA, Australia, or e-mail: [email protected].
DOI: 10.1111/j.1524-4741.2009.00828.x
� 2009 Wiley Periodicals, Inc., 1075-122X/09The Breast Journal, Volume 16 Number 1, 2010 60–65
when compared with their younger counterparts. On
a population basis, it is not clear whether age has an
independent effect on surgical treatment. In order to
determine the possible independent effect of age on
breast cancer surgery, the data relating to patient
characteristics and treatment need to be assessed using
a multivariate analysis method. To our best knowl-
edge, there has been no such study reported for an
Australian and New Zealand population. This study
aims to assess the pattern of breast cancer surgery
after adjusting for other major prognostic factors in
relation to patient age.
SUBJECTS AND METHODS
In this study, data was obtained from the National
Breast Cancer Audit (NBCA). The database from this
audit collects data on many aspects of breast cancer
diagnosis and treatment. The NBCA uses the defini-
tion of early breast cancer as stated in the NBCC
Clinical Practice Guidelines for the Management of
Early Breast Cancer, namely, invasive tumors of not
more than 5 cm in diameter with either impalpable or
palpable but not fixed lymph nodes (LN) and with no
evidence of distant metastases. This corresponds to
tumors that are T 1-2, N 0-1, and M0 (based on 1987
UICC classification). Cases of DCIS were excluded
from this study.
Between January 1998 to December 2006, 57,100
episodes of early breast cancer in this period were
reported to the NBCA. There were 31,298 patients
with key variables, age, type, size, and grade of the
main tumor and types of surgical treatment received,
available for the analysis and included in the subse-
quent analyzes. The following categorical data items
relating to early breast cancer diagnosis, surgery, and
adjuvant therapy were used in the analysis: age at
diagnosis in years (£40, 41–50, 51–70, >70), the prin-
ciple location of the main tumor (superior ⁄ lateral,
medial ⁄ inferior, central, >1 quadrant), method of
cytological ⁄ histologic diagnosis (fine needle aspiration,
core biopsy, open biopsy), invasive tumor size (1–10,
11–20, 21–30, 31–40, 41–50 mm), tumor grades (I, II,
III according to the modified Bloom and Richardson
criteria as described by Elston and Ellis) (7), LVI
(absent, present) LN status (positive, negative), exten-
sive intraduct component (EIC, absent, present), estro-
gen receptor (positive, negative), progesterone receptor
(positive, negative), type of surgical treatment (BCS,
mastectomy).
Statistical Methodology
The four age groups were analyzed for differences
in the various diagnostic, pathological, and surgical
treatment parameters previously described using the
chi-squared test (or Fisher’s exact test where the num-
ber of cases is <5 in one cell) and ANOVA where
appropriate. A statistical significance level of p < 0.05
was used. Multivariate analysis using logistic regres-
sion was used to determine the effect of age on the
use of surgical treatment. The odds ratio and its 95%
confidential interval from the analysis were shown.
RESULTS
The Relationship Between the Age and Method of
Preoperative Diagnosis
The number of patients was 2493 in the group aged
£40 years (mean ± SD: 35.9 ± 3.9), 6,863 in the group
aged 41–50 (46.1 ± 2.8), 15,842 in the group aged
51–70 (59.7 ± 5.6), and 6,100 in the group aged >70
(78.0 ± 5.3). Table 1 illustrates the methods of preop-
erative diagnosis using cytology, core biopsy, or open
biopsy. Fine needle aspiration cytology was the com-
monest method used for preoperative diagnosis. There
was a significantly higher use of core biopsy to obtain
a preoperative diagnosis in the 50–70 year age group
and a significantly greater use of open biopsy in
women aged £40 years.
The Relationship Between Age and Breast Cancer
Pathology
Most of the cases (>95%) were unilateral breast
cancer. There was an increase in the proportion of
bilateral cancer with age (1.4% for the youngest
group, 2.2% for 41–50 group and 2.5% for 51–70
group, and 3.5% for >70 group).
No major difference was demonstrated between age
groups in their distribution of the location of the main
Table 1. Method of Preoperative Diagnosis UsingCytology or Histology
Method of
preoperative
diagnosis
Age (years)
p-value£40 (%) 41–50 (%) 51–70 (%) >70 (%)
Fine needle
aspiration cytology
60.2 54.4 50.0 59.1 <0.05
Core biopsy 43.4 48.6 52.7 40.3 <0.01
Open biopsy 15.9 14.9 13.7 8.8 <0.001
The Age Effect on Surgical Treatment Pattern of Breast Cancer • 61
tumor, particularly for those located superior ⁄ lateral
or medial ⁄ inferior (Table 2). In older patients, there
was a slight increase (p < 0.05) of tumors which were
centrally located and a decrease of tumors which were
in more than one quadrant.
A significant difference in histologic tumor grade
was demonstrated according to age groups (Table 3).
Over 50% of women aged £40 years had high-grade
cancers compared with approximately 25% aged
‡50 years. In women aged 41–50 years, 36% had
high-grade tumors. There was a corresponding lower
rate of low-grade tumors in the younger age group.
The size and number of the tumor varied signifi-
cantly across the age groups. There was a trend of the
reduction in tumor size and few tumors with the
increase of age up to 70-year old. There was a signifi-
cant reduction of LN+ tumor with age. Over 40% of
the younger women had LVI presence and the propor-
tion was nearly halved in the two older groups. There
was a significant reduction in cases with the presence
of EIC from the youngest group to the oldest group
(Table 4). There was a significant increase in the rate
of estrogen receptor positive breast cancer with
increasing age. The proportion of breast cancers with
positive progesterone receptor status was significantly
less in the youngest group (Table 4).
The Relationship Between Age and Use of Surgical
Procedures
A significantly higher proportion of women aged
51–70 years underwent BCS compared with other age
groups while younger women who underwent BCS
were significantly more likely to undergo more than
one surgical procedure to obtain tumor clearance. The
proportion of women underwent breast reconstruction
after mastectomy decreased significantly with the
increase of age. Most women underwent one or more
surgical procedures although a significantly higher
proportion of women aged >70 years received no sur-
gery at all (Table 5).
The multivariate logistic regression analysis
(Table 6) shows that age was significantly associated
with the likelihood of undergoing BCS in addition to
the following variables: histologic grade, number of
Table 2. The Distribution of Principle Location ofthe Main Tumor for Different Age Groups
Location
Age (years)
p-value£40 (%) 41–50 (%) 51–70 (%) >70 (%)
Superior ⁄ lateral 64.9 66.2 65.6 62.1 NS
Medial ⁄ inferior 23.9 22.8 24.1 23.6 NS
Central 9.2 9.3 9.2 13.2 <0.05
>1 quadrant 2.0 1.7 1.1 1.0 <0.05
Table 3. Histologic Grade of the Tumor for Differ-ent Age Groups
Histologic
grades
Age (years)
p-value£40 (%) 41–50 (%) 51–70 (%) >70 (%)
1 11.4 20.2 28.9 26.7 <0.001
2 36.5 44.2 43.9 46.9 <0.001
3 52.1 35.6 27.2 26.4 <0.001
Table 4. Tumor Characteristics forDifferent Age Groups (mean + SDand%)Variable
Age
p-value£40 41–50 51–70 >70
Tumor size (mm) 20.67 + 10.84 19.31 + 10.43 17.27 + 9.91 19.82 + 10.45 <0.01
No. tumors 1.58 + 1.11 1.50 + 1.05 1.35 + 0.89 1.28 + 0.78 <0.05
LN+ 48.4% 41.2% 32.5% 36.2% <0.001
LVI presence 41.3% 30.7% 22.0% 23.0% <0.001
EIC presence 29.2% 27.2% 19.9% 13.6% <0.001
ER+ 64.4% 74.8% 79.3% 82.6% <0.001
PR+ 59.6% 70.1% 66.3% 68.0% <0.05
LVI, lymphatic vascular invasion; EIC, extensive intraduct component; ER, estrogen receptor status; PR, progesteronereceptor status.
Table 5. Utilization of the Surgical Procedures inDifferent Age Groups
Surgical procedures
Age
p-value£40 (%) 41–50 (%) 51–70 (%) >70 (%)
BCS* 53.9 56.7 62.9 53.0 <0.001
More than one BCS
procedures
24.8 20.4 17.0 11.4 <0.001
Mastectomy 44.9 42.0 36.1 43.5 <0.001
Reconstruction after
mastectomy
27.2 20.8 9.4 0.4 <0.001
No. surgical treatment 1.2 1.3 1.0 3.5 <0.001
*% BCS including one or more of the following procedures, open biopsy, CLE, re-exci-sion.
62 • wang ET AL.
cancers, tumor size, tumor location, the EIC presence
(yes or no), and LN status (+ or )). After adjusting
for these factors, compared with the group aged 51–
70 years (the reference group), the group aged
£40 years had a significantly increased likelihood of
receiving BCS (OR = 1.14, 95% CI: 1.004–1.293)
while the group aged >70 years had only half the
chance of receiving BCS (OR = 0.498, 95% CI:
0.455–0.545).
DISCUSSION
The results of this study demonstrate consistent dif-
ferences between the age groups in the early diagnosis,
cancer pathological characteristics, and the surgical
treatment received. After adjusting for cancer patho-
logical characteristics, age is independently associated
with the surgical treatment pattern in women with
breast cancer.
As expected, the breast cancers of younger women
had adverse histologic features including increased
tumor size, tumor number, higher histologic grades,
more LN involvement, more frequent LVI, and EIC.
These features suggest a higher rate of loco-regional
recurrence and worse survival for young women with
early breast cancer than older women which have
been confirmed by previous studies (8–11). There was
a significant increase in the rate of estrogen receptor
positive breast cancer in the older groups while the
proportion of progesterone receptor positive was sig-
nificantly higher only in the group aged >70 years. A
higher prevalence of simultaneous bilateral breast can-
cer was seen in women of older age groups. This
relates to the higher sensitivity of mammography for
older women (12,13). Another study reported that age
was a minor determinant of mammographic sensitivity
in women aged 40 years or older (14). There was no
difference between women aged 51–70 years and
those aged >70 years in tumor histologic grade, preva-
lence of LN+, and LVI although tumor size was signif-
icantly larger in women aged >70 years.
The clinical impact of the Breast Screen Australia
and Breast Screen Aotearoa Program in New Zealand
was demonstrated in the higher use of core biopsy in
the diagnosis of breast cancer in women aged 50–
70 years. Previous studies have demonstrated an
increase in preoperative cancer diagnosis with the use
of core biopsy compared with fine needle aspiration
(15,22 #1487). The use of open biopsy for breast can-
cer diagnosis was highest for women aged <40 years.
Although the reason for this may involve discrepant
results in the triple test, particularly in relation to
breast imaging, the increased use of core biopsy in this
group may lead to a reduced need for open biopsy.
The need to preserve the breast is more important
for young women. Higher rates of adjustment prob-
lems, body image issues, and depression have been
previously shown for younger women having mastec-
tomy (16). The preference of younger women for BCS
was also demonstrated by the strong age-related pat-
tern that they were more likely to undergo more than
one procedure to obtain resection margins or one or
two conservative procedures prior to mastectomy. In
the study population, one in four younger women
underwent more than one procedure. This may reflect
a more conservative approach by breast surgeons to
preserve breast aesthetic outcome with the first proce-
dure. Previous studies have shown that young women
tended to have smaller volumes of breast tissue
resected, more often extending to surgical margins at
re-excision (17).
Improvements in preoperative local staging to
determine the extent of cancer in the breast in younger
women is likely to improve surgical outcomes and
reduce the need for multiple operations. The relatively
low sensitivity of mammography in the dense breast is
a detriment to surgeons planning breast conserving
procedures in young women. Recent studies have
suggested that MRI has a much greater sensitivity and
can accurately assess the extent of breast cancer in
women with dense breasts (18–20). It is anticipated
that breast MRI will have a place in preoperative stag-
ing of breast cancer for young women in the near
Table 6. Multivariate logistic regression analyzesfor likelihood of BCS
OR 95% CI for OR p-value
Age (years) £40 1.140 1.004 1.293 <0.05
41–50 1.082 0.996 1.176 NS
51–70 1
>70 0.498 0.455 0.545 <0.01
Tumor size 0.942 0.939 0.946 <0.05
Histologic grade 1 1
Histologic grade 2 0.898 0.826 0.977 <0.05
Histologic grade 3 0.875 0.798 0.960 <0.01
No. tumors 1 1
No. tumors 2 0.329 0.293 0.370 <0.001
No. tumors 3+ 0.161 0.142 0.183 <0.001
EIC present, no 1
EIC present, yes 0.461 0.425 0.500 <0.01
LN) 1
LN+ 0.736 0.685 0.789 <0.01
EIC, extensive intraduct component; LN, lymph node.Significant values shown in bold.
The Age Effect on Surgical Treatment Pattern of Breast Cancer • 63
future. Diagnostic core biopsy can also accurately pro-
file the primary tumor in breast cancer patients
(21,22), and should be used more often in younger
women in order to provide more precise information
on breast cancer histologic characteristics.
Women aged >70 years were least likely to undergo
BCS compared to those aged 51–70 years despite
having histologic features that suggested suitability for
breast conservation. Furthermore, they were about
three times more likely to receive no surgical treat-
ment comparing with other age groups. Reasons for
this may include greater patient acceptance of mastec-
tomy, avoiding radiotherapy due to inconvenience and
radiation sequelae, simplifying treatment, and a differ-
ent understanding of information about treatment
efficacy of various surgical treatment options. Our
findings are consistent with recent studies regarding
the breast cancer treatment pattern in older women
(6). Older women (>70-year old) were less likely to
undergo axillary surgery (p < 0.001) (5). Another
study reported a lower frequency of adjuvant therapy
use among women over 65 years of age (23). The
guideline adherence was markedly lower for elderly
patients (24). The seemingly lower level of treatment
received by older women is an important issue requir-
ing further study. The complex interaction between
age, overall heath status, and living function compli-
cates the planning and outcomes of surgery. One
study in the USA population comprising Hispanic,
black, and non-Hispanic white women showed that
there are racial and age disparities in breast cancer
treatment in addition to the effect of education,
income status, insurance plan, functional status, and
comorbidity (4).
The inverse association between the use of BCS and
age is not fully consistent with the current recommen-
dation in the clinical guidelines in Australia and New
Zealand for breast cancer treatment and care. The
guidelines for all women stated: where appropriate,
women should be offered a choice of either BCS fol-
lowed by radiotherapy or mastectomy, as there is no
difference in the rate of survival or distant metastasis
(1). The guidelines also highlighted the need of
informing patients that body image is better preserved
with BCS (level I evidence). On the other hand, in the
guidelines for younger women with early breast can-
cer, it is noted that there are inadequate data about
optimal local treatment in the very young but limited
evidence suggests that age younger than 35 years is
associated with increased risk of recurrence after
breast conserving treatment, and also possibly follow-
ing mastectomy (2). It is possible that, either through
the zeal of the treating team or through patient
choice, preservation of the breast in younger women
may be used injudiciously and may jeopardize local
cancer control. Adequate surgery is fundamental to
the optimal treatment of breast cancer. A recent study
has demonstrated that the risk of death from breast
cancer was significantly higher if loco-regional treat-
ment was inadequate despite adjuvant treatments (25).
Although young age is currently not considered to be
a contraindication to breast conserving treatment, it
may signify a higher risk of ipsilateral breast tumor
recurrence (26), and require more aggressive surgical
resection and careful attention to margin status. As an
isolated loco-regional recurrence is a potentially cur-
able condition, patients treated with breast conserva-
tion, and diagnosed with breast cancer at a young age
should be monitored closely to detect local recurrence
at an early stage. If breast conservation cosmetic
issues assume importance, oncoplastic methods of
breast volume replacement or breast volume displace-
ment are methods that surgeons may employ to
improve outcomes. Further research is required in this
area.
This study has used data submitted over the last
8 years by breast surgeons in Australia and New
Zealand. One previous study has shown that over
this period of time, the use of BCS has not changed
significantly either overall (27), or for younger
women using multivariate models (28). In the multi-
variate logistic regression analysis, we have checked
and ensured that assumptions underlying the logistic
modeling, such as a lack of co-linearity, were satis-
fied. The variables which were not statistically signifi-
cant in the model have been dropped. A major
drawback of the present study is the lack of data
relating to patient participating in decision-making
process. Therefore, using the currently available data
in assessing the link between age and treatment can-
not elucidate the reasons for different treatment pat-
terns in women of different age. This study can only
illustrate the treatment pattern rather than identify
age as a factor influencing treatment. Complex inter-
actions between patient preference, breast cancer pre-
sentation, and treatment options by the surgeon may
at least partially explain some of the results reported
in this study.
In conclusion, this study demonstrates that there is
an independent association between patient age and
64 • wang ET AL.
the type of breast cancer surgery received by breast
cancer women in Australia and New Zealand. Women
age £40 years are more likely to undergo BCS despite
having adverse histologic features and often have
more than one procedure to achieve breast conserva-
tion. Older women (>70 years) more commonly
undergo mastectomy and are more likely to receive no
surgical treatment.
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The Age Effect on Surgical Treatment Pattern of Breast Cancer • 65