Background: Recent years have witnessed growing concerns about the possible
adverse effects of implants on breast cancer diagnosis and treatment. Numerous
reports describe how implants might interfere with mammography and impair
the ability to detect cancer. Several publications document the diminished
sensitivity of mammography in augmented patients with palpable tumors. However,
epidemiologic studies comparing stage of disease at time of diagnosis in
augmented and nonaugmented women are equivocal. The purpose of this study
was to review the authors’ experience with a large number of breast cancer
patients to determine whether implants impair early diagnosis or adversely affect
prognosis.
Methods: The authors reviewed their prospective database, which contains
detailed information on 3953 nonaugmented and 129 augmented breast cancer
patients. Various parameters of the two groups were compared and differences
were analyzed using appropriate statistical methodology.
Results:
The authors’ data reveal that augmented patients present with a statistically
greater frequency of palpable lesions, have a slightly greater risk of
invasive tumors, and have an increased likelihood of axillary lymph node metastases.
Despite this, there was no statistically significant difference in stage of
disease between augmented and nonaugmented patients; mean tumor size,
recurrence rates, and breast cancer-specific survival were virtually identical in
both groups.
Conclusions: Based on these findings, the authors conclude that despite the
diminished sensitivity of mammography in women with implants, augmented
and nonaugmented patients are diagnosed at a similar stage and have a comparable
prognosis. While implants may impair mammography, they appear to
facilitate detection of palpable breast cancers on physical examination. (Plast.
Reconstr. Surg. 118: 587, 2006.)
Breast enlargement surgery is popular in the
United States; it is estimated that more
than 334,000 women underwent elective
augmentation in 2004.1 Carcinoma of the breast
is also common, with an estimated annual incidence
of more than 267,000 new cases (including
both invasive and noninvasive tumors).2 A
woman in the United States now has a 1 in 7
(13.4 percent) lifetime risk of developing breast
cancer. Based on these statistics, it can be projected
that nearly 45,000 women undergoing
augmentation each year will develop breast cancer
at some time during their lives.
There does not appear to be an etiologic link
between implants and breast tumors. Numerous
studies show that the rate of breast cancer is not
increased among augmented women,3–9 and
some studies actually demonstrate lower than
expected rates.10–12 However, because a large
number of augmented women eventually will
develop breast cancer, there have been persistent
concerns about possible adverse effects of
implants on cancer detection and treatment.13,14
There is substantial literature to suggest that
implants can interfere with mammography.15–18
Likewise, several clinical studies document an
increased rate of false-negative mammograms in
augmented patients with palpable tumors.19–22
However, when it comes to determining whether
implants actually result in cancer being diagnosed
at a more advanced stage, the findings are
equivocal. Some studies indicate that augmented
breast cancer patients are diagnosed with more
advanced cancers than nonaugmented
patients,16,23,24 while other studies indicate that
the stage of disease is virtually identical in the
two groups.5,8,25–27
We have collected data pertaining to a large
number of augmented and nonaugmented
breast cancer patients treated over a 23-year period.
Our data reveal that augmented breast cancer
patients are diagnosed more frequently with
palpable tumors, have a lower incidence of in
situ lesions, and have a greater likelihood of
positive axillary lymph nodes. However, tumor
size is virtually identical in both groups, there is
no significant difference in stage of disease at
time of diagnosis, and prognosis appears to be
similar in both groups. The finding that significantly
more augmented patients present with
palpable cancers, while the lesions are the same
size as those in nonaugmented women, suggests
that implants may actually facilitate detection of
breast tumors on physical examination.
PATIENTS AND METHODS
This study comprised a consecutive series of
cancer patients treated between 1981 and 2004 at
two multidisciplinary breast centers. A total of 4082 breast cancer
patients were treated; 3953 cancers occurred in
nonaugmented women and 129 occurred in augmented
patients. All patients were entered into a
prospective database, which included, among
other information, tumor palpability, size of the
primary tumor (measured at the time of surgical
excision), nuclear grade, the presence or absence
of lymphovascular invasion, and axillary lymph
node status. Breast cancer recurrence and mortality
rates were also carefully tracked. Mammograms
were reviewed (when available) to compare
the sensitivity of mammography in augmented
and nonaugmented patients with palpable lesions.
Only patients with infiltrating ductal carcinoma,
infiltrating lobular carcinoma, ductal carcinoma
in situ, and lobular carcinoma in situ were
included for the purposes of the current study
(unusual tumors, such as angiosarcomas and lymphomas,
were excluded). A total of 3922 nonaugmented
patients and 129 augmented cancer patients
were included in the final analysis.
The data were evaluated by comparing various
parameters of the two groups. Statistical significance
was determined using several methods as
appropriate: comparison of the groups on average
tumor size was done with t tests on independent
groups; comparison of survival until recurrence
and survival until death was done using log-rank
tests from Kaplan-Meier survival analysis; and analysis
of counts and percentages was done with chisquare
tests.
RESULTS
The mean age at time of diagnosis was 53.5
years (range, 22 to 95 years) in nonaugmented
women and 46.8 years (range, 29 to 71 years) in
augmented patients (Table 1). In the augmented
group, for cases where data were available (n =
104), implants were present for a mean period of
10.45 years (range, 0.5 to 37 years) before cancer
diagnosis. In cases where information regarding
the degree of capsular contracture was available (n
= 106), 30 percent were Baker grade I, 40 percent
were grade 2, 22 percent were grade 3, and 8
percent were grade 4.
The distribution of cancers by histologic type
was similar in both groups (Table 2). A significantly
higher percentage of augmented patients
presented with palpable tumors (75 percent compared
with 54 percent, p < 0.0001) (Table 3).
There was a slightly lower incidence of early, in situ
lesions in augmented patients (27 percent compared
with 33 percent) and a greater incidence of
positive axillary lymph nodes (invasive cancers
only) in augmented patients (46 percent compared
with 35 percent). However, there was no
statistically significant difference in stage of disease
between the two groups (Table 4). The percentage
of patients (invasive cancers only) with
lymphovascular involvement was essentially the
same in augmented and nonaugmented patients.
Likewise, there was no difference in nuclear grade
between the two groups.
For purposes of comparing tumor size in augmented
and nonaugmented women, only patients
with infiltrating ductal lesions were considered.
Infiltrating ductal tumors were the type most commonly
encountered, and measurements of these
lesions were the most reliable. Among the 3922
nonaugmented patients, there were 2235 infiltrating
ductal cancers and the average tumor size was
23.8mm.Among120 augmented cancer patients, 86
had infiltrating ductal lesions with an average size of
23.2 mm (no significant difference) (Table 5).
Mammograms were available for 87 of the augmented
patients with palpable lesions. The mammogram
failed to reveal an abnormality in 36
cases, for a false-negative rate of 41.4 percent.
Mammograms were available for 1741 of the nonaugmented
women with palpable cancers and did
not visualize the tumor in 153 women, yielding a
false-negative rate of 8.8 percent. The difference
was significant (p < 0.0001) (Table 6).
Breast cancer recurrence rates and breast cancer-
specific mortality rates were compared between
the two groups. Among 3922 nonaugmented
cancer patients there have been 764
recurrences (19.5 percent), and among 129 augmented
patients there have been 19 recurrences
(14.7 percent), a difference that is not significant
(p = 0.4932) (Table 7). The Kaplan-Meier analysis
of cancer recurrence is illustrated in Figure 1.
Death from breast cancer occurred in 412 nonaugmented
patients (10.5 percent) and 13 augmented
patients (10.1 percent), again a nonsignificant
difference (p = 0.6523) (Table 8).
Kaplan-Meier analysis of breast cancer-specific survival
is depicted in Figure 2.
DISCUSSION
The key to early detection of breast cancer is
routine mammographic screening of asymptomatic
women.28,29 It has been well established that
occult breast cancers, lesions too small to be palpated
on physical examination but identifiable on
mammograms, have a very high cure rate.30–32 Because
of the effectiveness of mammography in
detecting early breast cancer, the American Cancer
Society recommends annual mammographic
screening of all women age 40 and older.2
Silicone gel-filled and saline-filled implants
are “radio-opaque” compared with breast tissue
(which has a radiological profile similar to fat).33
As a result, breast implants cast a shadow on
mammograms.22,34 It has long been known that
this implant shadow has the possibility of obscuring
an early breast cancer.35–37 To overcome this
impediment, various recommendations have been
made, including the use of displacement (Eklund
technique) mammography in conjunction with
conventional compression mammography in an
effort to visualize more of the breast.21,37–39 However,
even with vigilant techniques, it is likely that
mammographic screening will be impaired to
some extent in women with implants.17,18,40
Typically, mammography is highly sensitive for
detecting breast lesions. In nonaugmented
women with palpable breast cancer, mammography
reveals the tumor in more than 90 percent of
cases and has a false-negative rate below 10 percent.
However, repeated studies in augmented patients
with palpable cancers reveal diminished sensitivity
of mammography with a significantly
increased rate of false-negative examinations.19–22
Our current data add additional support to this
finding, revealing that among women with palpable
cancers the false-negative mammography rate
was 41.4 percent in those with implants, compared
with only 8.8 percent in nonaugmented patients.
Because implants have the potential to obscure
lesions on mammography, and because of
the increased rate of “false-negative” mammograms
in augmented patients with palpable tumors,
there has been persistent concern that augmented
breast cancer patients are diagnosed with
more advanced disease.13,14,20 However, published
studies examining the stage of disease at time of
diagnosis are equivocal.
We previously reported that among our breast
cancer population, augmented women were diagnosed
at a comparatively advanced stage.16,20 Others
have reported similar observations. In the Multicenter
Study,23 Brinton et al. found that
augmented cancer patients had a lower incidence
of in situ and local disease and a higher rate of
axillary nodal metastases and distant spread than
nonaugmented patients. Similarly, Karanas and
associates24 reported a low rate of early lesions
(stages 0 and 1) and a relatively high rate of advanced
disease (stages 3 and 4) in augmented
patients with breast cancer. On the other hand,
there are numerous reports suggesting that the
stage of disease at diagnosis is equivalent in augmented
and nonaugmented women.5,8,25–27 Our
updated observations tend to support the conclusion
that the stage of disease is similar in both
groups at time of diagnosis. Likewise, our series
confirms, as others have reported, that augmented
patients are not a higher risk of cancer recurrence
or death.25,27,41–45
Our data do not reveal a significant difference
in tumor size, lymph node status, stage of disease,
or prognosis between augmented and nonaugmented
patients. However, breast cancers were
palpable at the time of diagnosis significantly
more often in augmented women (75 percent
compared with 54 percent). Since the size of the
lesion is virtually identical in the two groups, one
explanation might be that the presence of an implant
actually facilitates palpation of the tumor.
Others have suggested that the augmented breast
may be easier to examine,14 and there are several
reasons why this hypothesis is reasonable.
Palpation of a breast lesion is dependent on
feeling the abnormality and distinguishing it from
surrounding normal breast tissue. This task is much
more difficult in women with large breasts and deep
tumors, because the lesion simply is not as accessible
to the palpating fingers. It is widely acknowledged
that breast implants compress breast parenchyma
and, over time, cause atrophy of tissue. It is not
unusual to observe that the parenchymal envelope
in augmented patients has been reduced to a thickness
of just a few centimeters, particularly when implants
have been present for many years. In our
population of augmented cancer patients, implants
had been present for an average period of 10.45
years before diagnosis. This is certainly ample time
for the prosthesis to have caused tissue compression,
thinning, and atrophy (Fig. 3).
Another hypothetical way that implants could
facilitate palpation of tumors is by providing a
smooth, uniform platform upon which the lesion
is more easily appreciated. When the nonaugmented
breast is palpated, there are underlying
structures, such as the bone and cartilage comprising
the sternum and ribs; these tissues have a
firm, lumpy consistency. These textural irregularities
may make it more difficult to determine
whether an abnormality is present. In augmented
patients, the breast parenchyma lies atop an implant,
which has a uniform consistency and a
smooth surface. This homogeneous background
provides a uniform substrate upon which the
denser, irregular tumor mass may be felt more
readily.
Many patients who have had implants for a
prolonged period of time develop clinically significant
capsular contracture. This decreases the
compliance of the implant and results in the surrounding
breast tissue being stretched over a relatively
immobile, rigid surface. While capsular
contracture has been shown to impair mammography,
when the thinned out breast tissue is
stretched over a rigid, uniform underlying structure
(the implant encased in a contracted capsule),
this might actually facilitate palpation of
abnormalities.
CONCLUSIONS
There are numerous studies suggesting that
implants obscure mammographic visualization of
the breast. There are also data demonstrating that
implants reduce the sensitivity of mammography
in patients with palpable lesions. In our review of
a large series of augmented and nonaugmented
breast cancer patients, we found that tumors were
palpable significantly more often in augmented
patients and that women with implants had a significantly
higher rate of false-negative mammograms.
Despite this, tumor size was virtually identical
in both groups, with similar results for stage
of disease, recurrence rates, and breast cancerspecific
survival. These findings suggest that tumors
of equal size may be more easily palpated in
augmented patients, and this beneficial effect may
compensate for the potential impairment of mammography.
Because of the possible adverse effect of implants
on visualization of breast tissue, screening
mammography may not be appropriate in augmented
patients. In most cases, a diagnostic
mammogram should be obtained, even in
asymptomatic patients. Ideally, physical and
mammographic findings should be correlated.
Any palpable abnormalities should be studied
with ultrasound. In appropriate cases, magnetic
resonance imaging should be considered as an
adjunct. While many questions about cancer in
the augmented breast remain unanswered, our
most recent findings suggest that in the typical
clinical setting augmented and nonaugmented
breast cancer patients are diagnosed at a similar
stage and have a comparable prognosis.
ACKNOWLEDGMENTS
The authors acknowledge the contributions of Rita
Engelhardt, Dr.P.H., and Jeffrey Gornbein, Dr.P.H.,
Department of Biomathematics, UCLA, who assisted in data
analysis.
DISCLOSURE
Neither Dr. Handel nor Dr. Silverstein has any
commercial associations that might pose or create a conflict
of interest with information presented in this article.
Specifically, neither Dr. Handel nor Dr. Silverstein has
any consultancies, stock ownership or other equity interests,
patent licensing arrangements, or payments of stipends
for conducting or publicizing the study described
in the article. Dr. Handel personally paid the expenses
related to carrying out this study.
REFERENCES
1. American Society for Aesthetic Plastic Surgery. The American
Society for Aesthetic Plastic Surgery 2004 Cosmetic Surgery National
Data Bank Statistics. American Society for Aesthetic
Plastic Surgery, 2005.
2. American Cancer Society. Breast Cancer Facts & Figures 2003-
2004.: American Cancer Society, 2003.
3. Berkel, H., Birdsell, D. C., and Jenkins, H. Breast augmentation:
A risk factor for breast cancer. N. Engl. J. Med. 326:
1649, 1982.
4. Deapen, D. M., Pike, M. C., Casagrande, J. T., et al. The
relationship between breast cancer and augmentation mammoplasty:
An epidemiologic study. Plast. Reconstr. Surg. 77:
361, 1986.
5. Clark, C. P., III, Peters, G. N., and O’Brien, K. M. Cancer in
the augmented breast: Diagnosis and prognosis. Cancer 72:
2170, 1993.
6. Brinton, L. A., Malone, K. E., Coates, R. J., et al. Breast
enlargement and reduction: Results from a breast cancer
case-control study. Plast. Reconstr. Surg. 97: 269, 1996.
7. Kern, K. A., Flannery, J. T., and Kuehn, P. G. Carcinogenic
potential of silicone breast implants: A Connecticut statewide
study. Plast. Reconstr. Surg. 100: 737, 1997.
8. Friis, S., McLaughlin, J. K., Mellemkjaer, L., et al. Breast implants
and cancer risk in Denmark. Int. J. Cancer 71: 956, 1997.
9. McLaughlin, J. K., Nyren, O., Blot, W. J., et al. Cancer risk
among women with cosmetic breast implants: A populationbased
cohort study in Sweden. J. Natl. Cancer Inst. 90: 156, 1998.
10. Su, C. W., Dreyfuss, D. A., and Krizek, A. Silicone implants
and the inhibition of cancer. Plast. Reconstr. Surg. 96: 513,
1995.
11. Deapen, D. M., Bernstein, L., and Brody, G. S. Are breast
implants anticarcinogenic? A 14-year follow-up of the LA study. Plast. Reconstr. Surg. 99: 1346, 1997.
12. Hoshaw, S. J., Klein, P. J., Clark, B. D., et al. Breast implants
and cancer: Causation, delayed detection, and survival. Plast.
Reconstr. Surg. 107: 1393, 2001.
13. Jakubietz, M. G., Janis, J. E., Jakubietz, R. G., and Rohrich, R. J.
Breast augmentation: Cancer concerns andmammography—A
literature review. Plast. Reconstr. Surg. 113: 117, 2004.
14. Jakub, J. W., Ebert, M. D., Cantor, A., et al. Breast cancer
in patients with prior augmentation: Presentation, stage,
and lymphatic mapping. Plast. Reconstr. Surg. 114: 1737,
2004.
15. Rintala, A. E., and Svinhufvud, U. M. Effect of augmentation
mammaplasty on mammography and thermography. Plast.
Reconstr. Surg. 54: 390, 1974.
16. Silverstein, M. J., Handel, N., Gamagami, P., et al. Breast
cancer in women after augmentation mammaplasty. Arch.
Surg. 123: 681, 1988.
17. Silverstein, M. J., Handel, N., and Gamagami, P. The effect
of silicone gel-filled implants on mammography. Cancer 68 (5
Suppl.): 1159, 1991.
18. Handel, N., Silverstein, M. J., Gamagami, P., Jensen, J. A., and
Collins, A. Factors affecting mammographic visualization of
the breast after augmentation mammaplasty. J.A.M.A. 268:
1913, 1992.
19. Douglas, K. P., Bluth, E. I., Sauter, E. R., et al. Roentgenographic
evaluation of the augmented breast. South. Med. J. 84:
49, 1991.
20. Silverstein, M. J., Handel, N., Gamagami, P., et al. Breast
cancer diagnosis and prognosis in women following augmentation
with silicone gel-filled prostheses. Eur. J. Cancer 28:
635, 1992.
21. Leibman, A. J., and Kruse, B. D. Imaging of breast cancer
after augmentation mammaplasty. Ann. Plast. Surg. 30: 111,
1993.
22. Fajardo, L. L., Harvey, J. A., McAleese, K. A., Roberts, C. C.,
and Granstrom, P. Breast cancer diagnosis in women with
subglandular silicone gel filled augmentation implants. Radiology
194: 859, 1995.
23. Brinton, L. A., Lubin, J. H., Burich, M. C., et al. Breast cancer
following augmentation mammaplasty. Cancer Causes Control
11: 819, 2000.
24. Karanas, Y. L., Leong, D. S., Da Lio, A., et al. Surgical treatment
of breast cancer in previously augmented patients.
Plast. Reconstr. Surg. 111: 1078, 2003.
25. Birdsell, D. C., Jenkins, H., and Berkel, H. Breast cancer
diagnosis and survival in women with and without breast
implants. Plast. Reconstr. Surg. 92: 795, 1993.
26. Cahan, A. C., Ashikari, R., Pressman, P., et al. Breast cancer
after breast augmentation with silicone implants. Ann. Surg.
Oncol. 2: 121, 1995.
27. Deapen, D., Hamilton, A., Bernstein, L., and Brody, G. S.
Breast cancer stage at diagnosis and survival among patients
with prior breast implants. Plast. Reconstr. Surg. 105:
535, 2000.
28. Bedwani, R., Vana, J., Mettlin, C., et al. Management and
survival of female patients with “minimal” breast cancer.
Cancer 47: 2769, 1981.
29. Schwartz, G. F., Feig, S. A., and Patchefsky, A. S. Clinicopathologic
correlations and significance of clinically occult
mammary lesions. Cancer 41: 1147, 1978.
30. Koscielny, S., Tubiana, M., Le, M. G., et al. Breast cancer:
Relationship between the size of the primary tumor and the
probability of metastatic dissemination. Br. J. Cancer 49: 709,
1984.
31. Fentiman, I. S., Cuzick, J., Millis, R. R., et al. Which patients
are cured of breast cancer? Br. Med. J. 289: 1108, 1984.
32. Rosen, P. P., Groshen, P. E., Kinne, D. W., and Hellman, S.
Pathological prognostic factors in stage I (T1,N0, M0) and
stage II (T1, N1, M0) breast carcinoma: A study of 644
patients with median follow-up of 18 years. J. Clin. Oncol. 7:
1239, 1989.
33. Gumucio, C. A., Pin, P., Young, V. L., et al. The effect of
breast implants on the radiographic detection of microcalcification
and soft-tissue masses. Plast. Reconstr. Surg. 84: 772,
1989.
34. Monsees, B. S., and Destouet, J. M. Mammography in aesthetic
and reconstructive breast surgery. Perspect. Plast. Surg.
5: 103, 1991.
35. Hayes, H., Jr., Vandergrift, J., and Diner, W. Mammography
and breast implants. Plast. Reconstr. Surg. 92: 209, 1993.
36. Carlson, G. W., Curley, S. A., Martin, J. E., et al. The detection
of breast cancer after augmentation mammaplasty. Plast.
Reconstr. Surg. 91: 837, 1993.
37. Skinner, K. A., Silbermann, H., Dougherty, W., et al. Breast
cancer after augmentation mammaplasty. Ann. Surg. Oncol.
8: 138, 2001.
38. Eklund, G. W., Busby, R. C., Miller, S. H., et al. Improved
imaging of the augmented breast. A.J.R. Am. J. Roentgenol.
151: 469, 1988.
39. Leibman, A. J. Breast cancer: Mammographic and sonographic
findings after augmentation mammaplasty. Radiology
174: 195, 1990.
40. Silverstein, M. J., Handel, N., Gamagami, P., Waisman, E.,
and Gierson, E. D. Mammographic measurements before
and after augmentation mammaplasty. Plast. Reconstr. Surg.
86: 1126, 1990.
41. McLaughlin, J. K., Nyren, O., Blot, W. J., et al. Cancer risk
among women with cosmetic breast implants: A populationbased
cohort study in Sweden. J. Natl. Cancer Inst. 90: 156,
1998.
42. Park, A. J., Chetty, U., and Watson, A. C. H. Silicone breast
implants and breast cancer. Breast 7: 22, 1998.
43. Petit, J. Y., Le, M., Rietjens, M., et al. Does long-term exposure
to gel-filled silicone implants increase the risk of relapse after
breast cancer? Tumori 84: 525, 1998.
44. Joseph, E., Wells, K. E., Anastasi, G. W., Reintgen, D. S.,
and Cox, C. E. Survival from breast carcinoma after augmentation
mammaplasty. In Proceedings of the 67th Annual
Scientific Meeting of the American Society of Plastic and Reconstructive
Surgeons, the Plastic Surgery Educational Foundation,
and the American Society of Maxillofacial Surgeons., October 3-7, 1998.
45. Georgiade, G. S., Riefkohl, R., Cox, E., et al. Long-term
clinical outcome of immediate reconstruction after mastectomy.
Plast. Reconstr. Surg. 76: 415, 1985.