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The Impact of Implant Location on Breast Cancer Characteristics in Previously Augmented Patients: A Systematic Literature Analysis
Journal of Cancer Prevention 2018;23:93-8
Published online June 30, 2018
© 2018 Korean Society of Cancer Prevention.

Alain Joe Azzi1, Jordan Gornitsky2, Alex Viezel-Mathieu1, and Lucie Lessard1

1Division of Plastic and Reconstructive Surgery, McGill University Faculty of Medicine, Montreal, QC, Canada, 2Department of Medicine, McGill University Faculty of Medicine, Montreal, QC, Canada
Correspondence to: Alain Joe Azzi, Division of Plastic and Reconstructive Surgery, McGill University Health Center, 1650 Cedar Avenue, Montreal, QC H3G 1A4, Canada, Tel: +1-514-934-1934 (ext. 43044), Fax: +1-514-934-8207, E-mail: alain.azzi@mail.mcgill.ca, ORCID: Alain Joe Azzi, https://orcid.org/0000-0003-3250-5305
Received March 28, 2018; Revised June 22, 2018; Accepted June 24, 2018.
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Abstract

Background

There is a paucity of data comparing the oncologic properties of breast cancer among patients previously having undergone breast augmentation in either the subglandular or subpectoral planes. The objective of the present systematic review was to evaluate whether implant location influenced the characteristics of breast tumors in previously augmented women.

Methods

A systematic literature search was performed to identify relevant articles reporting tumor characteristics in augmented patients. The search included published articles in three electronic databases; Ovid MEDLINE, EMBASE, and PubMed. Comparative studies (subglandular vs. subpectoral) were included.

Results

Analysis of data pooled from the included studies showed that subglandular implants had a higher frequency of tumors between 2 to 5 cm (26.5% vs. 9.9%, P = 0.0130). Subglandular implants also had a higher frequency of stage 2 tumors (42.9% vs. 23.7%, P = 0.0308). There was no significant difference in lymphovascular invasion between the 2 groups. These results of this systematic review suggest that the prognosis of patients undergoing augmentation is unaffected by implant location (subpectoral vs. subglandular).

Conclusions

With the absence of large randomized controlled trials, our study provides surgeons with an evidence-based reference to improve informed consent with regards to implant placement.

Keywords : Breast Implants, Breast Neoplasms, Mammography
INTRODUCTION

The demand for cosmetic breast augmentation continues to increase in the United States. According to the American Society of Aesthetic Plastic Surgeons, there were 310,444 cases of breast augmentation in 2016, representing a 206.8% annual increase in the number of procedures performed as compared to 20 years ago.1 With an approximate 12.4% lifetime risk of developing breast cancer, a significant proportion of augmented women will go on to develop breast cancer and delayed detection remains an ongoing concern.2 Numerous studies have been conducted to evaluate whether an etiologic link exists between implants and breast cancer. It has been concluded that women are not at an increased risk of developing breast carcinoma following augmentation.39 It is however well documented that the radiopaque nature of implants impairs the sensitivity of mammography, even when employing the implant displacement technique.10,11 This appears to be more pronounced when the implant is located in the subglandular plane as opposed to subpectoral.10,11 Conversely, implants have been speculated to facilitate the detection of palpable breast tumors by providing a background on which to palpate, and have also been associated with more invasive cancers.1113 The clinical significance of these findings remains unclear. While certain studies claim that women with implants have breast cancer diagnosed at a more advanced stage, other publications presented conflicting results.1419 To date, there does not exist a systematic review of the literature comparing the oncologic behavior of breast cancer between previously augmented patients in the subglandular and subpectoral planes. The objective of the present systematic review is to evaluate whether implant location (subglandular vs. subpectoral) influences the characteristics of breast tumors in previously augmented women.

MATERIALS AND METHODS

A search of the Ovid MEDLINE, EMBASE, and PubMed databases was performed, starting from the establishment of each database to August 1st 2017. An initial search was performed using different spellings and versions of the following terms: ([“breast neoplasm”] and [“implant” or “prosthesis” or “augmentation mammoplasty” or “mammoplasty” or “alloplastic”] and [“detection” or “screening”]). A separate search was also performed using different spellings and versions of the following terms: ([“prepectoral” or “subglandular” or “retropectoral” or “subpectoral”] and [“breast neoplasms”]). Citations were limited to human studies published in the English language. Studies were included if subpectoral and subglandular implant subgroups were separated and analyzed independently with regards to cancer characteristics at presentation. The endpoints of interest were tumor size, tumor grade and lymph node involvement at diagnosis. Only comparative studies were included to reduce the risk of confounding factors. Non-human studies, case reports (< 8 patients), and review articles were excluded. Two independent reviewers assessed the eligibility of the studies using the same systematic inclusion/exclusion criteria. A total of 1,894 studies were identified and further narrowed to 135 potentially eligible studies after primary review. Studies were selected based on the relevance of the title and/or abstract of retrieved records (Fig. 1). The initial screen excluded studies with evidently irrelevant titles or abstracts. If content was unclear in the initial screen based on abstract review, a formal article review was undertaken. Potentially eligible studies were further reviewed, leading to a total of 2 eligible studies. Studies were also collected from an extensive manual Internet search and from the reference list of relevant articles, yielding one additional study. The systematic review followed the guidelines provided by the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement.20 Subglandular and subpectoral implants were compared with respect to tumor size, tumor stage, and presence of lymphovascular invasion at initial presentation for breast cancer screening. Variables were displayed as descriptive data and compared by Fisher’s exact test and chi-square analysis using IBM SPSS ver. 22 (IBM Co., Armonk, NY, USA). P-values < 0.05 were considered to be statistically significant.

RESULTS

A total of three studies met the inclusion criteria (Cho et al.,21 Douglas et al.,22 and Spear et al.23) (Table 1). Tumor size, stage and the presence of lymphovascular involvement were the only variables with enough data for comparison (Table 2). Exact carcinoma subtype (lobular vs. ductal), tumor grade, and presence of metastasis could not be compared due to incomplete or insufficient data. The following analyses were performed:

1. Tumor size

Tumor size, measured by the pathologist, was categorized into the following three categories: < 2 cm, 2 to 5 cm, and > 5 cm, based on tumor size classification in the TNM staging system.24 All 3 studies were included in the analysis with an effective sample size of 122 (Table 3). A difference in tumor sizes, trending towards statistical significance (P = 0.052) was observed between patients receiving subglandular and subpectoral implants. Subgroup analysis of data pooled from the 3 studies showed that subglandular implants were associated with a higher frequency of tumors between 2 to 5 cm (P = 0.0130). There was also a higher frequency of tumors < 2 cm in the subglandular group, with borderline statistical significance (P-value = 0.0642). There were no difference in the frequency of tumors > 5 cm.

2. Tumor stage

Tumor stage was categorized from 0 to 4, based on the TNM staging system.24 Two studies (Cho et al.21 and Spear et al.23) were included with an effective sample size of 118 (Table 4). Overall, the difference in tumor stages between both groups was not considered statistically significant (P = 0.09). Subgroup analysis of the pooled data demonstrated a higher frequency in stage 2 tumors (P = 0.0308) in the subglandular group. The remainder of the comparison demonstrated no difference in frequency between the subpectoral and subglandular groups.

3. Lymphovascular invasion

Presence of lymphovascular invasion was a binary outcome (yes or no). All 3 studies were included with an effective sample size of 126 (Table 5). Analysis of data pooled from the 3 studies demonstrated no significant difference between lymphovascular invasion and implant position (P = 0.60).

DISCUSSION

In the current review, implant location (subpectoral vs. subglandular) did not have a significant overall impact on cancer screening. Subgroup analyses demonstrated that subglandular implants had a higher frequency of tumors between 2 to 5 cm and stage 2 tumors, although no statistical significance was observed overall. There was also a difference in tumors < 2 cm, albeit not statistically significant (P = 0.0642). This finding potentially suggests that the increased distortion caused by subglandular implants may lead to delayed radiological detection of early tumors. This result however did not translate to more aggressive cancers, as there was no significant difference when comparing tumors > 5 cm, stage 3 tumors, and lymphovascular invasion between groups. These results serve to suggest that the prognosis of patients undergoing augmentation is unaffected by implant location. It is important however that patients are made aware of the inherent risk of false-negatives on mammography following augmentation,9 and counseled to undergo regular screening using both imaging and clinical examinations.

Delayed detection of occult breast cancers by means of mammography in previously augmented patients remains an area of ongoing concern. It has been reported in the literature that the radio-opaque nature of implants may obscure the visualization of breast tissue on mammography.9,25 The amount of glandular tissue obscured by implants varies from 22% to 83%.25 Silverstein et al.10 demonstrated that subglandular implants resulted in in reduced measurable tissue area as compared to subpectoral implants. These results were paralleled by Handel,9 who demonstrated that patients with subglandular implants had a 37% reduction in the visualized tissue area as compared to 17% in the subpectoral group. Despite utilization of Eklund’s displacement technique, minimal improvement was observed. Furthermore, in addition to implant placement, the presence of capsular contracture further obscures the image, with a reported range of 30% to 50% in Baker grades 1 to 2 and 3 to 4, respectively.9 Capsular contracture in the context of subglandular implant placement can potentially limit the sensitivity of mammography.

As a result of these factors, the sensitivity of mammography in previously augmented women with palpable tumors has been reported as reduced when compared to non-augmented women.2628 This association however is mainly based on older studies and updated prospective studies are needed due to evolution in mammography quality and implants in the past decades. Tumors in women following augmentation have been shown to be primarily detected by palpation as opposed to mammography.9,13,17 This has been explained by the smaller native breast tissue of these women as well as the implant serving as a background upon which to palpate the breast tissue. Furthermore, women undergoing cosmetic procedures may be more body conscious and therefore more likely to identify changes to their breasts.12

Whether these aforementioned factors resulting in delayed detection translate to more aggressive tumors remains inconclusive in the literature. Previous studies have shown there is no increased risk of breast cancer associated with implants and even suggested that the incidence of breast carcinoma is lower than in non-augmented women.7 Conversely, in a meta-analysis performed by Lavigne et al.,8 breast augmentation was shown to adversely affect the survival of women subsequently diagnosed with breast cancer. Patients having undergone augmentation had an overall OR of 1.26 (95% CI, 0.99–1.60) for an invasive type of breast cancer at diagnosis. The studies included in that analysis did not account for potential confounding factors and should therefore be interpreted with caution. To our knowledge, implant plane (subglandular vs. subpectoral) has not been previously compared in systematic review with regards to oncologic characteristics in breast cancer screening.

This systematic review is not without limitations. Several confounding factors may have affected the overall results. These include surgical approach, implant material, texture, size etc. Due to paucity of comparative studies, we were unable to account for these factors. Heterogeneity in mammogram machines and radiologist experience could have also affected our results. Follow-up period, mean age, and patient population also varied greatly amongst the included studies. We also acknowledge that larger randomized controlled studies are required to confirm causality.

Implant location (subpectoral vs. subglandular) does not appear to have an impact on cancer screening. Implant placement should be decided according to both patient and surgeon preference in order to achieve the desired aesthetic outcome. With the absence of meta-analyses or large randomized controlled trials, our study provides surgeons with an evidence-based reference to improve informed consent with regards to implant placement.

ACKNOWLEDGMENTS

We would like to thank Dr. Xianming Tan, Ph.D., from the Department of Biostatistics and the Lineberger Comprehensive Cancer Center in North Carolina at Chapel Hill, USA. Dr. Tan’s expertise in statistics, particularly in systematic reviews and meta-analyses, was crucial to this manuscript.

CONFLICTS OF INTEREST

No potential conflicts of interest were disclosed.

Figures
Fig. 1. Flowchart of the search criteria and strategy used for the literature review.
Tables

Overview of included studies characteristics and level of evidence

StudyYearStudy designTotal number of implantSubglandular (n)Subpectoral (n)Level of evidence
Cho et al.212017Retrospective case control9027633
Douglas et al.221991Retrospective case control8624
Spear et al.232008Retrospective case control3216164

Overall study results of included studies

VariableSubglandularSubpectoralP-value
Tumor size (cm)0.052a
 < 230 (61.2)62 (76.5)0.0642
 2–513 (26.5)8 (9.9)0.0130*
 > 52 (4.1)7 (8.6)0.3286
 Unknown4 (8.2)4 (4.9)0.4494
Tumor stage0.09b
 07 (16.7)24 (31.6)0.0796
 115 (35.7)26 (34.2)0.8704
 218 (42.9)18 (23.7)0.0308*
 32 (4.8)8 (10.5)0.2891
 40 (0)0 (0)-
Lymphovascular invasion0.60a
 Present18 (36.7)23 (28.4)0.3255
 Absent30 (61.2)55 (67.9)0.4383
 Unknown1 (2.0)3 (3.7)0.5869

Values are presented as number (%).

aFisher’s exact test was used.

bFisher’s exact test was used except for tumor stage 4.

*P < 0.05.


Tumor size characteristics

VariableTumor size (cm) (subglandular)Tumor size (cm) (subpectoral)


< 22–5> 5Unknown< 22–5> 5Unknown
Cho et al. (2017)211580445774
Douglas et al. (1991)2251002000
Spear et al. (2008)231042015100

Values are presented as number only.


Tumor stage characteristics

VariableTumor stage (subglandular)Tumor stage (subpectoral)


0123401234
Cho et al. (2017)21213110020191380
Spear et al. (2008)235272047500

Values are oresented as number only.


LV invasion characteristics

VariableLV invasion (subglandular)LV invasion (subpectoral)


PresentAbsentUnknownPresentAbsentUnknown
Cho et al. (2017)211016117433
Douglas et al. (1991)2224-11-
Spear et al. (2008)23610-511-

Values are presented as number only. LV, lymphovascular.


References
  1. (2017). Cosmetic Surgery National Data Bank statistics. Aesthet Surg J. 37, 1-29.
    Pubmed CrossRef
  2. Howlader, N, Noone, AM, Krapcho, M, Miller, D, Bishop, K, and Kosary, CL (). SEER Cancer Statistics Review, 19752014.http://seer.cancer.gov/csr/1975_2014/
  3. Berkel, H, Birdsell, DC, and Jenkins, H (1992). Breast augmentation: a risk factor for breast cancer?. N Engl J Med. 326, 1649-1653.
    Pubmed CrossRef
  4. Brinton, LA, Lubin, JH, Burich, MC, Colton, T, Brown, SL, and Hoover, RN (2000). Breast cancer following augmentation mammoplasty (United States). Cancer Causes Control. 11, 819-27.
    Pubmed CrossRef
  5. Clark, CP, Peters, GN, and O섳rien, KM (1993). Cancer in the augmented breast. Diagnosis and prognosis. Cancer. 72, 2170-4.
    Pubmed CrossRef
  6. Deapen, DM, Pike, MC, Casagrande, JT, and Brody, GS (1986). The relationship between breast cancer and augmentation mammaplasty: an epidemiologic study. Plast Reconstr Surg. 77, 361-8.
    Pubmed CrossRef
  7. Deapen, D (2007). Breast implants and breast cancer: a review of incidence, detection, mortality, and survival. Plast Reconstr Surg. 120, 70S-80S.
    Pubmed CrossRef
  8. Lavigne, E, Holowaty, EJ, Pan, SY, Villeneuve, PJ, Johnson, KC, and Fergusson, DA (2013). Breast cancer detection and survival among women with cosmetic breast implants: systematic review and meta-analysis of observational studies. BMJ. 346, f2399.
    Pubmed CrossRef
  9. Handel, N (2007). The effect of silicone implants on the diagnosis, prognosis, and treatment of breast cancer. Plast Reconstr Surg. 120, 81S-93S.
    Pubmed CrossRef
  10. Silverstein, MJ, Handel, N, and Gamagami, P (1991). The effect of silicone-gel-filled implants on mammography. Cancer. 68, 1159-63.
    Pubmed CrossRef
  11. Silverstein, MJ, Handel, N, Gamagami, P, Waisman, E, and Gierson, ED (1990). Mammographic measurements before and after augmentation mammaplasty. Plast Reconstr Surg. 86, 1126-30.
    Pubmed CrossRef
  12. Miglioretti, DL, Rutter, CM, Geller, BM, Cutter, G, Barlow, WE, and Rosenberg, R (2004). Effect of breast augmentation on the accuracy of mammography and cancer characteristics. JAMA. 291, 442-50.
    Pubmed CrossRef
  13. Skinner, KA, Silberman, H, Dougherty, W, Gamagami, P, Waisman, J, and Sposto, R (2001). Breast cancer after augmentation mammoplasty. Ann Surg Oncol. 8, 138-44.
    Pubmed CrossRef
  14. Silverstein, MJ, Gierson, ED, Gamagami, P, Handel, N, and Waisman, JR (1990). Breast cancer diagnosis and prognosis in women augmented with silicone gel-filled implants. Cancer. 66, 97-101.
    Pubmed CrossRef
  15. Silverstein, MJ, Handel, N, Gamagami, P, Waisman, JR, Gierson, ED, and Rosser, RJ (1988). Breast cancer in women after augmentation mammoplasty. Arch Surg. 123, 681-5.
    Pubmed CrossRef
  16. Xie, L, Brisson, J, Holowaty, EJ, Villeneuve, PJ, and Mao, Y (2010). The influence of cosmetic breast augmentation on the stage distribution and prognosis of women subsequently diagnosed with breast cancer. Int J Cancer. 126, 2182-90.
  17. Birdsell, DC, Jenkins, H, and Berkel, H (1993). Breast cancer diagnosis and survival in women with and without breast implants. Plast Reconstr Surg. 92, 795-800.
    Pubmed CrossRef
  18. Deapen, D, Hamilton, A, Bernstein, L, and Brody, GS (2000). Breast cancer stage at diagnosis and survival among patients with prior breast implants. Plast Reconstr Surg. 105, 535-40.
    Pubmed CrossRef
  19. Friis, S, H철lmich, LR, McLaughlin, JK, Kj첩ller, K, Fryzek, JP, and Henriksen, TF (2006). Cancer risk among Danish women with cosmetic breast implants. Int J Cancer. 118, 998-1003.
    CrossRef
  20. Moher, D, Liberati, A, Tetzlaff, J, Altman, DG, and PRISMA Group (2010). Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int J Surg. 8, 336-41.
    Pubmed CrossRef
  21. Cho, EH, Shammas, RL, Phillips, BT, Greenup, RA, Hwang, ES, and Hollenbeck, ST (2017). Breast cancer after augmentation: oncologic and reconstructive considerations among women undergoing mastectomy. Plast Reconstr Surg. 139, 1240e-9e.
    Pubmed CrossRef
  22. Douglas, KP, Bluth, EI, Sauter, ER, McKinnon, WM, Bergeron, RB, and Merritt, CR (1991). Roentgenographic evaluation of the augmented breast. South Med J. 84, 49-54.
    Pubmed CrossRef
  23. Spear, SL, Clemens, MW, and Dayan, JH (2008). Considerations of previous augmentation in subsequent breast reconstruction. Aesthet Surg J. 28, 285-93.
    Pubmed CrossRef
  24. Array (2010). Breast. AJCC Cancer Staging Manual. New York: Springer, pp. 347-69
  25. Hayes, H, Vandergrift, J, and Diner, WC (1988). Mammography and breast implants. Plast Reconstr Surg. 82, 1-8.
    Pubmed CrossRef
  26. Silverstein, MJ, Handel, N, Gamagami, P, Gierson, ED, Furmanski, M, and Collins, AR (1992). Breast cancer diagnosis and prognosis in women following augmentation with silicone gel-filled prostheses. Eur J Cancer. 28, 635-40.
    Pubmed CrossRef
  27. Leibman, AJ, and Kruse, BD (1993). Imaging of breast cancer after augmentation mammoplasty. Ann Plast Surg. 30, 111-5.
    Pubmed CrossRef
  28. Fajardo, LL, Harvey, JA, McAleese, KA, Roberts, CC, and Granstrom, P (1995). Breast cancer diagnosis in women with subglandular silicone gel-filled augmentation implants. Radiology. 194, 859-62.
    Pubmed CrossRef


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