Skin-sparing mastectomy

Specialty bias and worldwide lack of consensus

Abstract

BACKGROUND

Skin-sparing mastectomy (SSM) is a variation of modified radical mastectomy (MRM) optimized for reconstruction. The authors attempted to determine SSM attitudes and biases within different specialties and countries throughout the world.

METHODS

The authors polled 11,485 individuals via e-mail, including members of surgical, medical, and breast oncology societies, about SSM. Respondents were directed to a survey website where data were directly entered into a database.

RESULTS

Among 1027 respondents, 19 said their knowledge was insufficient to attempt the survey. Surveys were completed by 1008 respondents (8.8%) from 52 countries, comprising 436 (43.3%) surgeons, 376 (37.3%) medical oncologists, 146 (14.5%) radiation oncologists, and 50 (5.0%) individuals from other fields. Of the respondents, 61.9% stated that SSMs are performed at their institution. However 19.1% of these believed that SSM leaves the nipple and areola intact. This perception was higher outside the U.S. (P < 0.0001). Despite knowledge by 77.8% that SSM does not have a higher local disease recurrence rate than MRM, 25.3% of these individuals did not believe the literature. This was most prevalent among radiation oncologists (48.5%), as was the belief that SSM is contraindicated in patients with ductal carcinoma in situ and invasive breast carcinoma (23.3%).

CONCLUSIONS

Despite a developing body of literature, there was variation in opinion among specialties and a lack of understanding of SSM. Many physicians were not familiar with the literature. Among those who were, skepticism was highest among radiation oncologists. Although these results were indicative of only those responding, education about SSM is needed across specialties and in other countries if the procedure is to be widely accepted. Cancer 2003. © 2003 American Cancer Society.

Over the past 30 years, breast surgery has become less invasive and disfiguring. Radical mastectomy, modified radical mastectomy, breast conservation, and sentinel lymphadenectomy are four progressive examples of this evolution. As with other trends in surgical treatment, the role of improved cosmesis has also become more significant and, in part, been driven by patient demand.

Skin-sparing mastectomy (SSM), in which the majority of a patient's natural breast skin is left in place for reconstruction, results from the continuation of these trends. Previous paradigms of breast carcinoma treatment emphasized radical resection. However, the success of breast conservation has made the need for extirpation of the uninvolved skin questionable. Despite this, modified radical mastectomies continue to be performed by removing a large ellipse of skin well beyond the nipple–areola complex and biopsy scar. In circumstances in which no reconstruction is performed such a large excision is appropriate to allow the flat adherence of skin flaps to the underlying chest wall. However, when reconstruction is performed, skin is mobilized with autologous tissue and/or an implant to fill the cutaneous defect. When skin is transferred, differences in donor skin pigmentation and texture can make this tissue transfer obvious and diminish the cosmetic result.

Since the introduction of SSM in 1991 by Toth and Lappert,1 there have been slight variations in the precise definition of the procedure,1–3 as well as its indications,1, 4, 5 although most of the literature is consistent.6–8 SSM is not yet a standard procedure for breast carcinoma. Although the body of literature on the topic has markedly increased in recent years, much confusion remains. Because we found that this controversy existed between specialties at our institution, a tertiary cancer center with a dedicated multidisciplinary breast program, we wished to determine how widespread the disparity of opinion on SSM is. As the literature develops on SSM, we also believed that it would be helpful to assess whether there are differences in opinion by specialty or geographic location. Our objectives were to understand the potential biases of future nonrandomized studies on SSM and to determine the need for educational programs to increase acceptance of this procedure.

MATERIALS AND METHODS

A unique website was established at the John Wayne Cancer Institute (Santa Monica, CA) for publication of this worldwide web-based survey. This site was created with no external links from other websites to prevent accidental browsing and completion of the survey by laypersons visiting the Institute's other web pages. The address of the web page was also made sufficiently complex to prevent individuals from guessing its location for access.

The survey was comprised of 13 multiple-choice questions and the page was programmed to allow only one answer for 12 of the 13 questions. The remaining question, regarding acceptable SSM incision types, instructed the respondent to choose “one, many, or none” of the options depicted. On completion of the survey, the respondents were instructed to press a “submit” button on the web page to enter their answers. They were informed that, once the submit button was pressed, the submission was immutable. After pressing the submit button, the page was programmed to check for answers to the 12 questions requiring one answer. Any omissions caused a dialogue box to appear. The dialogue box informed the respondent that a question was omitted and that its completion was required before submission of the survey.

The submit button on the web page was programmed to send the answers directly to a custom-designed Microsoft Access database (Microsoft, Redmond, WA). This automation avoided transcription errors during data entry of responses. The database remained on a server behind a firewall and was backed up daily for data integrity and security reasons.

E-mail addresses were obtained from three published lists of major surgical, medical, and breast oncology societies. Requests of these individuals to complete the survey were made via E-mail. These requests directed the respondents to the address of the website via hyperlink, allowing them to click on the site and be directed to the survey page automatically.

No identifying data were recorded with the survey answers. An alpha level of 0.05 was considered significant.

RESULTS

Respondent Demographics

Among the E-mails sent, 11,485 had valid addresses and 1027 individuals responded. Among these, 19 sent E-mails stating that that they did not have enough knowledge to even attempt the survey. Therefore, 1008 individuals (8.8% of 11,485) completed the survey and constitute the study cohort. Among these individuals were 870 attendings (86.3%), 36 fellows (3.57%), 25 residents (2.5%), and 16 retired physicians (1.6%). The remaining 61 (6.1%) respondents comprised nurses, administrators, and physician and nonphysician scientists who classified themselves primarily by their Ph.D. degrees. Tables 1–3 show the number of respondents listed by country, specialty, and subspecialty.

Table 1. Number of Respondents, Listed by Nationality

Country	No. (%)
a Comprised 29 other countries with three or fewer respondents from each.
United States of America	712 (70.63)
Canada	30 (2.98)
Italy	27 (2.68)
Japan	19 (1.88)
Germany	16 (1.59)
Australia	14 (1.39)
France	14 (1.39)
Belgium	13 (1.29)
Brazil	13 (1.29)
Switzerland	12 (1.19)
Israel	11 (1.09)
Netherlands	11 (1.09)
Spain	11 (1.09)
Taiwan	8 (0.79)
Turkey	8 (0.79)
Argentina	7 (0.69)
Austria	7 (0.69)
United Kingdom	7 (0.69)
Greece	6 (0.60)
Mexico	6 (0.60)
New Zealand	5 (0.50)
Colombia	4 (0.40)
Egypt	4 (0.40)
Othera	44 (4.37)

Table 2. Specialty Classification of Respondents

Specialty	No. (%)
Surgeons	436 (43.25)
Medical oncologists	376 (37.30)
Radiation oncologists	146 (14.48)
Other	50 (4.96)

Table 3. Breakdown of Classification of Surgeons

Surgical subspecialty	No. (%)
Surgical oncologist	297 (68.12)
Breast surgeon	92 (21.10)
General surgeon	40 (9.17)
Plastic surgeon	5 (1.15)
Other surgeon	2 (0.46)

Knowledge of Skin-Sparing Mastectomy

Among physicians, 62.3% stated that SSM is performed at their institution. Significantly more respondents from the U.S. than from any other country replied that SSM is performed at their institutions (66.6% vs. 50.7%, P < 0.0001). Significantly more physicians at institutions at which SSM is performed knew that the nipple–areola complex was removed as part of the procedure compared with those who practice where SSM is not performed (81.7% vs. 38.0%, P < 0.0001). Among physicians, 65.2% overall knew that the nipple–areola complex is removed as part of SSM. Knowledge that the nipple and areola are excised as part of SSM was significantly less widespread among physicians outside the U.S. than within the U.S. (46.4% vs. 73.3%, P < 0.0001).

Among the six incisions presented as potentially classifiable as SSM by the literature definition, two were correct, each of which resected the nipple and areola and biopsy site, one with an axillary incision and one without. Only 16.4% of physicians chose exactly these 2 incisions, although 31.5% selected only the 1 with the axillary incision and 14.6% selected only the 1 without. Only 52.0% of physicians stated that SSM achieves an equivalent axillary lymph node dissection (ALND) and breast tissue resection, whereas 26.0% said that the ALND was equivalent, but the resection was not. Knowledge of equivalence within the oncologic specialties is shown in Figure 1.

Figure 1. Perceptions of skin-sparing mastectomy (SSM) resectional equivalency compared with modified radical mastectomy (MRM), by oncologic specialty. Shown are the percentages of each oncologic specialty that responded that SSM is equivalent to MRM with respect to both the breast parenchyma excised and the extent of the axillary dissection.

Only 7 (0.7%) respondents believed that SSM patients cannot undergo reconstruction. All but one (a surgical oncologist) of these respondents practiced outside the U.S. Another 13.4% of all respondents believed that reconstruction was either not necessary with SSM or was limited to either autologous tissue alone or implants alone (Table 4). Similar percentages of individuals overall within (49.0%) and outside the U.S. (48.0%) believed that indications for SSM were ductal carcinoma in situ (DCIS) and AJCC Stage I and II breast carcinoma (consistent with the literature). In addition, 23.3% of radiation oncologists believed that SSM was contraindicated in both invasive breast carcinoma and DCIS, whereas 14.9% of medical oncologists and 9.0% of surgical oncologists agreed.

Table 4. Knowledge Regarding Reconstruction Options for Patients Undergoing Skin-Sparing Mastectomy

Reconstruction options	Physician respondents No. (%)	Nonphysician respondents No. (%)
Can have both tissue transfer and implant reconstruction	851 (86.5)	15 (62.5)
Cannot undergo tissue transfer reconstruction and cannot have implants	7 (0.7)	0 (0)
Cannot undergo tissue transfer reconstruction but can have implants	76 (7.7)	5 (20.8)
Can undergo tissue transfer reconstruction but cannot have implants	39 (4.0)	3 (12.5)
Never needs reconstruction	11 (1.1)	1 (4.2)

Biases Regarding Skin-Sparing Mastectomy

For patients undergoing SSM, most physicians replied that they would not change their administration of radiation or adjuvant systemic therapy (62.1% and 87.8%, respectively). In contrast, 24.9% would be more aggressive with radiation, whereas only 5.6% would be more aggressive with adjuvant systemic therapy. Figure 2 details physician biases regarding treatment of patients undergoing SSM. Among radiation oncologists, 43.8% stated they would be more aggressive with radiation, whereas 9.0% of medical oncologists said they would be more aggressive with adjuvant systemic therapy.

Figure 2. Physician biases in treatment of patients who underwent skin-sparing mastectomy (SSM). Individuals surveyed were asked whether and how they would be likely to change their recommendations for administration of radiation and adjuvant systemic therapy in a patient undergoing SSM compared with modified radical mastectomy. (A) Biases regarding radiation. (B) Biases regarding adjuvant systemic therapy.

Knowledge that local disease recurrence between SSM and modified radical mastectomy (MRM) is similar was reported by 77.8% of respondents overall and by 69.3%, 70.0%, and 89.9% of radiation, medical, and surgical oncologists, respectively. Among those of each specialty who knew that local disease recurrence is similar, radiation oncologists were most skeptical of the literature (Fig. 3).

Figure 3. Literature skepticism among those knowing that local disease recurrence is not increased in skin-sparing mastectomy (SSM). Individuals were asked whether the literature shows that SSM has a higher local disease recurrence rate when compared with modified radical mastectomy (MRM). They were also asked whether, in their opinion, SSM has a higher local disease recurrence rate when compared with MRM. Numbers in the graph represent the percentage within each specialty that know, but do not believe, that the local recurrence rate is similar. The asterisk indicates that 44% of gynecologists who knew the local disease recurrence data were also skeptical.

DISCUSSION

Standard surgical practice is often quite difficult to change, as was evident when breast conservation with radiation became a valid alternative to MRM. SSM, an alternative to MRM or total mastectomy (depending on the extent of ALND performed), was first reported in 1991.1 Although technical variations have been published,5, 9 the basic description has remained relatively unchanged in the majority of the more than 60 published articles. SSM removes the nipple and areola, the skin of the biopsy site, and the skin overlying superficial tumors.1, 3, 5, 6, 8 A separate axillary incision may be made for sentinel or axillary lymphadenectomy if needed.5, 10, 11

It became evident, during tumor board discussions at the John Wayne Cancer Institute, that the safety of SSM and the details of the procedure were not universally known or accepted. We became interested in determining the level of education and skepticism among those most likely to have an interest in this topic. To do so, we queried individuals from major medical oncology, surgical oncology, and breast oncology societies because we knew that individuals of multiple disciplines and specialties were members of these societies.

It must be noted that the data obtained from this survey can only be said to represent the respondents themselves. Generalizations to any particular group may be difficult, especially as a minority of those polled responded. However, the data offer a glimpse of the education level and SSM biases of physicians and nonphysicians involved in oncology and represent the only such assessment to date. Some individuals replied that their knowledge was insufficient to attempt the survey, but it may be assumed that the majority of those who did choose to respond perceived their knowledge to be sufficient to answer the questions. Regardless, we have demonstrated that accurate knowledge of SSM is not universal and that biases against the procedure exist. This may be important for interpreting future nonrandomized studies on SSM and disseminating information about this useful technique.

Many reports do not demonstrate an increase in the local disease recurrence rate for SSM compared with MRM (Table 5). Despite this, we found significant skepticism, which was most prominent among radiation oncologists. Within the surgical community, however, the decreasing skepticism from general surgeon to surgical oncologist, breast surgeon, and then plastic surgeon mimics the more intense focus on this procedure by each of these respective specialties. It should be noted, however, that only five plastic surgeons responded. The responses regarding skepticism are also consistent with the finding that the plastic surgery literature contains the majority of articles on SSM because SSM was first described by plastic surgeons.1

Table 5. Published Skin-Sparing Mastectomy Series that Consist of more than 100 Procedures and more than 3 Years of Follow-Up that Analyzed Local Disease Recurrence Rates

Series	No. of SSM	SSM local disease recurrence (%)	Follow-up (mos)
SSM: skin-sparing mastectomy; DCIS: ductal carcinoma in situ.
Carlson et al. (2003)17	565	5.5	61.6
Newman et al. (1998)18	372	6.2	50
Carlson et al. (1997)6	327	4.8	41.3
Spiegel and Butter (2003)19	177 invasive, 44 DCIS	5.6 invasive, 0 DCIS	117.6 overall, 126 DCIS
Medina-Franco et al. (2002)15	173	4.5	73
Kroll et al. (1999)20	114	7.0	66
Kroll et al. (1997)21	104	6.7	67.2

Published articles have assessed specialty differences and practice patterns12, 13 for varying procedures and fields, although none exist for SSM to date. Most of these assessments deal with one country's or region's attitudes without global comparisons. We have found that there is significantly greater awareness on the part of physicians within the U.S. regarding the definition and indications for SSM. It is unclear whether this is because the overwhelming majority of articles published on the subject originated in the U.S. or because of the higher prevalence of the procedure within the U.S.

SSM has been consistently demonstrated to have an equivalent recurrence rate to MRM.3, 14–17 The skepticism expressed by the radiation and medical oncologists involved the equivalency of resection as well as the indications and disease recurrence rate. These biases may be a reflection of the dearth of literature on the subject published by investigators in those fields. In a literature search at the time of this writing for the term “skin-sparing mastectomy,” only 9 of 68 articles were published in nonsurgical journals and none of them were found in radiation or medical oncology journals.

One of the more surprising findings of the current study was that only a small percentage of physicians correctly identified the two incisions encompassed by descriptions in the majority of the SSM literature. Many physicians did know that at least one or both of these were correct SSM incisions. However, many are unaware that a separate axillary incision, in itself, does not change the classification of the mastectomy as “skin-sparing.”2, 3, 5, 10, 11 Many also do not know the incision types used in the SSM procedure. The third most common incision type selected by physicians was a single inframammary incision with no nipple, areolar, or biopsy site resection.

These results demonstrate that although substantial increases in publications on SSM have occurred in recent years, knowledge of this subject is spotty. Many physicians are not aware of the details of the procedure and, among those who are, many are biased against it. Radiation oncologists are the most skeptical, followed by medical oncologists. Finally, SSM does not appear to be performed as frequently outside the United States where there is more awareness of the procedure.

Acknowledgements

The authors extend their sincere thanks to Chris Herlong for his database and web page programming expertise, Karen Hirsch for her website graphic arts talents, and Cynthia Ye for her assistance with the statistical data.