Circumferential periareolar incision length as a risk factor for skin necrosis after nipple-sparing mastectomy with deep inferior epigastric perforator flap reconstruction

Abstract

Background

Nipple-sparing mastectomy (NSM) with autologous tissue reconstruction offers excellent cosmetic outcomes but can be complicated by skin necrosis. This study aimed to investigate the risk factors for skin necrosis after NSM with deep inferior epigastric perforator (DIEP) flap reconstruction, focusing on the impact of circumferential periareolar incision length.

Methods

A retrospective review of 61 patients who underwent NSM followed by DIEP flap reconstruction between 2020 and 2023 was conducted. Data on patient demographics, breast characteristics, incision type, and skin necrosis outcomes were collected.

Results

The overall rate of the mastectomy skin flap or nipple-areola complex (NAC) was 42.6%. The length of the periareolar incision was significantly associated with the incidence of skin necrosis (p = 0.035). Patients with incisions exceeding 30% of the periareolar circumference had a higher risk of necrosis (57.1%) compared to those with shorter incisions (30.3%). No significant associations were found between skin necrosis and BMI, breast ptosis, patient age, year of reconstruction, or neoadjuvant chemotherapy.

Conclusions

This study suggests that for patients undergoing NSM with DIEP flap reconstruction, a circumferential periareolar incision length exceeding 30% is associated with an increased risk of skin necrosis in the mastectomy skin flap or NAC. Surgeons should strive to minimize periareolar incision length while ensuring adequate access for flap vascular anastomosis.

Nipple-Sparing Mastectomy (NSM) Offers Well-Established Oncological Safety, Excellent Cosmetic Outcomes, Psychological Benefits, and High Satisfaction of Patient reported outcome [1–4]. NSM with implant-based reconstruction is the most commonly performed breast reconstruction procedure, but autologous tissue breast reconstruction, such as the deep inferior epigastric perforator (DIEP) flap, can provide superior aesthetic outcomes and patient satisfaction [5]. DIEP flap reconstruction is particularly suitable for patients with large or ptotic breasts, obesity, or who have undergone NSM with resection of tumor surface skin [6–9].

Skin necrosis is a serious complication that can occur in patients who undergo NSM followed by implant-based reconstruction. It can lead to implant exposure and reconstruction failure, which can have a significant impact on patient outcomes and require additional surgery. While NSM with autologous tissue reconstruction offers a safer option compared to implant-based reconstruction, it can still result in imperfect breast appearance due to mastectomy skin necrosis. This can manifest as nipple-areola discoloration and nipple loss, potentially affecting patient satisfaction [10, 11].

Previous studies have reported that skin necrosis after NSM is associated with factors such as obesity, breast ptosis, large breast volume, and incision type [11–14]. However, these studies often included only patients who underwent implant-based or both implant and autologous reconstruction. The internal thoracic vessels are the most commonly used recipient vessels in DIEP breast reconstruction. The incision design should consider the facilitation of vascular anastomosis, which is why a circumferential periareolar incision with appropriate extension is often chosen for DIEP reconstruction after NSM. The risk factors for skin necrosis after NSM with this type of incision have not been systematically studied. We hypothesize that skin necrosis after DIEP reconstruction following NSM is associated with breast ptosis, resected breast volume, and circumferential periareolar length of the NSM incision. These factors may influence the blood supply to the skin flap and increase the risk of necrosis.

Patients and methods

We conducted a retrospective review of patients who underwent NSM followed by immediate DIEP flap breast reconstruction at the department of breast, the affiliated cancer hospital of Zhengzhou university from January 2020 to December 2023. The following parameters were recorded for each patient: age, body mass index (BMI), receipt of neoadjuvant chemotherapy, year of surgery, resected breast volume, degree of breast ptosis (grades 0, 1, 2, or 3), and the proportion of the circumferential periareolar incision to the areola. The selection criteria for NSM include: The primary tumor is located outside the margin of the areola; no nipple retraction or nipple discharge; no microcalcifications in the retroareolar area; no inflammatory signs; no tumor infiltration in the retroareolar area. Patients who had a positive frozen section biopsy of the nipple-areolar complex (NAC) during surgery were excluded from this study. All patients signed informed consent for NSM and DIEP immediate breast reconstruction preoperatively. The NSM was performed by experienced oncological surgeons, with the subsequent DIEP flap reconstruction carried out by plastic surgeons. During the NSM, only the superficial layer of subcutaneous fat was preserved in the skin flap.

Axillary Lymph Node Management: All patients underwent axillary lymph node dissection (ALND) or sentinel lymph node biopsy (SLNB) via a separate incision in the axilla, ensuring no interference with the primary periareolar mastectomy incision.

The criteria for assessing NSM skin ischemia were based on previous studies [15]. The definition of ischemic changes is as follows (Fig. 1): Grade 0, normal skin color of the NAC and surrounding incision area, and no NAC discoloration; Grade 1: Superficial desquamation of the anterior surface of the nipple skin, or epidermal loosening of the areola/incision margin skin. No NAC discoloration after recovery, and no clinical significance. Grade 2: Partial ischemia of the NAC, leading to partial necrosis or discoloration of the NAC. Grade 3: Partial full-thickness skin necrosis, leading to complete loss of the nipple or delayed healing of the areola/incision margin skin, formation of scars. Grade 0 and 1 changes do not affect the cosmetic appearance of the breast and are considered as no NSM skin necrosis. Grade 2 and 3 changes resulting in NAC discoloration, nipple loss, or skin scarring, are considered as NSM necrosis. All patients were evaluated 2-3weeks after surgery.

Fig. 1.

The criteria for assessing NSM skin ischemia. A: Grade 0, normal skin color of the NAC and surrounding incision area, and no NAC discoloration; B: Grade 1: Superficial desquamation of the anterior surface of the nipple skin, or epidermal loosening of the areola/incision margin skin. No NAC discoloration after recovery, and no clinical significance. C: Grade 2: Partial ischemia of the NAC, leading to partial necrosis or discoloration of the NAC. D: Grade 3: Partial full-thickness skin necrosis, leading to complete loss of the nipple or delayed healing of the areola/incision margin skin, formation of scars. Abbreviations: NSM, Nipple-Sparing Mastectomy

Breast ptosis is graded according to the position of the NAC relative to the inframammary fold (IMF). Grade 1: The NAC is at the level of the IMF. Grade 2: The NAC is below the IMF but above the lowest breast contour. Grade 3: The NAC is below the IMF and at the lowest point of the breast contour. No ptosis: The NAC is located above the IMF.

The periareolar incision with radial extension is a commonly used incision for NSM. The incision is made around the areola and extends radially outward. This incision provides good access to the chest wall vasculature for anastomosis of the recipient vessels and facilitates flap inset. The length of the radial extension depends on the size of the breast and the location of the tumor. If the tumor is located close to the skin, part of the skin over the tumor may be resected and a flap observation window may be left. Otherwise, most patients will have a small flap observation window at the incision site, while a few patients will have the incision directly sutured without an observation window.

Data were analyzed using SPSS version 22.0 (Stata Corp, College Station, Texas). One-way ANOVA was employed to identify significant correlations between continuous variables and categorical variables (such as types of incisions, study years, and complications). Positive findings from all ANOVA results were further investigated using two-sample t-tests. Chi-square analysis or Fisher’s exact test was used to examine the correlation between categorical predictive variables and outcomes. P-values between 0.1 and 0.05 were described as showing a trend towards significance, while p-values < 0.05 were considered statistically significant.

Results

A total of 61 patients who underwent successful NSM followed by DIEP breast reconstruction between January 2020 and December 2023 were included in this study. The average age of these patients was 42.2 years (ranging 31–59), with 59.0% (36/61) of the patients having a BMI of ≥ 24 kg/m². All patients had no history of smoking and had histories of childbirth. Among these patients, 10 (16.4%) received neoadjuvant chemotherapy, 9 (14.8%) were diagnosed with ductal carcinoma in situ (DCIS), and 52 had invasive carcinoma. All cases were newly diagnosed breast cancer patients; none had a history of previous partial mastectomy or radiotherapy to the breast or chest wall. 41 patients exhibited grade 2 and 3 breast ptosis, and 14 (23.0%) had a breast resection weight of > 600 g. 33 patients (54.1%) had NSM incisions that involved ≤ 30% of the periareolar circumference, while the remaining 45.9% had incisions > 30%. See Table 1 for details.

Table 1.

Patients’ characteristics with 61 patients who underwent NSM followed by DIEP flap reconstruction

Characteristics	N (%)
Age(year) Median (range)	42.2(31–59)
<40	22(36.1)
≥ 40	39(63.9)
Body mass Index (kg/m2)
<24	25(41.0)
≥ 24	36(59.0)
Year of surgery
2020–2021	19(31.1)
2022–2023	42(68.9)
Smoking
No	61(100)
Yes	0(0)
Parity
Yes	61(100)
No	0(0)
Neoadjuvant therapy
No	51(83.6)
Yes	10(16.4)
Breast ptosis
No ptosis	3(4.9)
Grade 1	17(27.9)
Grade 2	37(60.6)
Grade 3	4(6.6)
Resected breast weight
<600 g	47(77.0)
≥ 600 g	14(23.0)
Circumferential periareolar incision proportion
≤ 30%	33(54.1)
>30%	28(45.9)
Tumor characteristics
DCIS	9(14.8)
Invasive cancer	52(85.2)

Abbreviations: DCIS Ductal carcinoma in situ, DIEP Deep inferior epigastric perforator, NSM Nipple-Sparing Mastectomy

Based on the previously described criteria, Grade 0 and 1 changes were considered no NSM skin necrosis, while Grade 2 and 3 were classified as skin necrosis. Of the 61 patients who underwent NSM followed by DIEP breast reconstruction, 17 cases (27.9%) had no skin ischemia. There were 18 cases (29.5%) of Grade I skin ischemia, 21 cases (34.4%) of Grade II skin ischemia, and 5 cases (8.2%) of Grade III skin ischemia (Table 2). A total of 26 cases (42.6%) presented with skin necrosis (ischemia of Grade II/III).

Table 2.

NSM skin ischemia with 61 patients who underwent NSM followed by DIEP flap reconstruction

NSM skin ischemia	N (%)
Stage 0	17(27.9)
Stage Ⅰ	18(29.5)
Stage Ⅱ	21(34.4)
Stage Ⅲ	5(8.2)

Abbreviations: NSM Nipple-Sparing Mastectomy

The length of the periareolar incision was significantly associated with the occurrence of grade II/III necrosis. The incidence of skin necrosis was 30.3% (10/33) in patients with a periareolar incision length ≤ 30%, and 57.1% (16/28) in patients with a periareolar incision length > 30%, which was statistically significant (P = 0.035). The incidence of skin necrosis was higher in the group with breast resection weight ≥ 600 g (64.3%) than in the group with breast resection weight < 600 g (36.2%), but the difference was not statistically significant (P = 0.062). No statistically significant correlation was found between NSM skin necrosis and BMI, breast ptosis, patient age, year of reconstruction, or neoadjuvant chemotherapy (P > 0.05 for all). See Table 3 for details. Multivariate logistic regression analysis demonstrated that a periareolar incision length > 30% was significantly associated with an increased risk of NSM skin necrosis, with an odds ratio of 4.388 (95% CI: 1.189–16.193), p = 0.026 (Table 4).

Table 3.

Association between patients’ characteristics and skin necrosis with 61 patients who underwent NSM followed by DIEP flap reconstruction

Characteristics	NSM skin ischemia N (%)		χ2	P
	Stage 0/Ⅰ	Stage Ⅱ/Ⅲ (skin necrosis)
Age(year) Median (range)
<40	15(68.2)	7(31.8)	0.643	0.200
≥ 40	20(51.3)	19(48.7)
Year of surgery
2019–2021	11(57.9)	8(42.1)	0.003	0.956
2022–2023	24(57.1)	18(42.9)
Neoadjuvant therapy
No	28(54.9)	23(45.1)	0.779	0.377
Yes	7(70.0)	3(30.0)
BMI(kg/m2)
<24	14(56.0)	11(44.0)	0.033	0.856
≥ 24	21(58.3)	15(41.7)
Resected breast weight
<600 g	30(63.8)	17(36.2)	3.487	0.062
≥ 600 g	5(35.7)	9(64.3)
Breast ptosis
Grade 0/1	13(65.0)	7(35.0)	0.707	0.400
Grade 2/3	22(53.7)	19(46.3)
Circumferential periareolar incision proportion
≤ 30%	23(69.7)	10(30.3)	4.462	0.035
>30%	12(42.9)	16(57.1)

Abbreviations: BMI Body mass index, DIEP Deep inferior epigastric perforator, NSM Nipple-Sparing Mastectomy.

Table 4.

Multivariate logistic regression analysis of risk factors for skin necrosis with 61 patients who underwent NSM followed by DIEP flap reconstruction

Characteristics	OR (92%CI)	P
Age(year) Median (range)
<40	1	0.263
≥ 40	0.263(0.066–1.049)
Year of surgery
2019–2021	1	0.922
2022–2023	0.067(0.293–3.884)
Neoadjuvant therapy
No	1	0.341
Yes	2.358(0.404–13.779)
BMI(kg/m2)
<24	1	0.436
≥ 24	1.630(0.477–5.570)
Resected breast weight
<600 g	1	0.226
≥ 600 g	2.437(0.576–10.308)
Breast ptosis
Grade 0/1	1	0.106
Grade 2/3	3.599(0.761–17.011)
Circumferential periareolar incision proportion
≤ 30%	1	0.026
>30%	4.388(1.189–16.193)

Abbreviations: BMI Body mass index, DIEP Deep inferior epigastric perforator, NSM Nipple-Sparing Mastectomy

Discussion

NSM with immediate breast reconstruction has gained increasing attention as a preferred treatment option for a growing patient population. Multiple studies have shown that NSM has comparable recurrence rates to traditional mastectomy and skin-sparing mastectomy [11, 16–19]. The focus has shifted from debating the oncological safety of NSM to determining its technical feasibility and aesthetic outcomes for the majority of patients [20–22]. Previous studies have primarily investigated the impact of different surgical incisions (periareolar, IMF, and radial) on NSM skin necrosis, and included cases that were primarily reconstructed with implants or a combination of implants and autologous tissue. Most results indicate that patients undergoing periareolar incisions have the highest risk of skin necrosis compared to other incision types [11, 13, 23–25]. Our study included a highly selected group of patients who were not ideal candidates for primary implant reconstruction. These patients either had moderate to severe breast ptosis, large breast volume, or required resection of tumor surface skin. All patients underwent NSM followed by immediate DIEP breast reconstruction. We used a periareolar and extension incision in all cases. For the first time, our study found that for patients undergoing NSM, the risk of skin necrosis was significantly increased when the periareolar incision length was ≥ 30%. This finding provides a more nuanced understanding of the impact of periareolar incision size on skin necrosis.

We selected 30% as the cutoff value for periareolar incision length based on previous research. Garwood et al. [16] demonstrated that nipple survival rates were higher and necrosis complications lower with NSM incisions crossing less than 30% of the nipple-areola complex (NAC), compared to those crossing more than 30% (periareolar NSM or NSM crossing). The NAC’s blood supply primarily relies on a dense subdermal and subcutaneous vascular network beneath and around it [26, 27]. Periareolar incisions inevitably transect or damage some of these vascular branches. As incision length increases, the cumulative number of severed vessels grows, leading to greater disruption of the periareolar vascular plexus. This forces the NAC to shift from a rich, multidirectional blood supply to a limited supply dependent on fewer remnant vessels, significantly weakening its vascular compensatory capacity. Studies indicate that when the periareolar incision length exceeds 30% of the areolar circumference, this vascular network disruption may reach a critical point, resulting in insufficient NAC perfusion and consequently increasing the risk of ischemic necrosis [16]. Longer incisions cause more severe damage to the core vascular network, thus increasingly limiting the blood flow vital for NAC viability.

When performing NSM followed by DIEP flap reconstruction, the incision must accommodate both the breast resection and the convenient anastomosis of the flap’s vascular pedicle to the recipient vessels (primarily the internal mammary vessels). Therefore, most NSM incisions for DIEP reconstruction consider a periareolar approach with appropriate extension. However, our research indicates that extending the periareolar incision beyond 30% can indeed affect the blood supply to the NSM flap and lead to skin necrosis. Previous studies have also shown that compared to using the thoracodorsal artery and vein as recipient vessels, using the internal mammary vessels may result in a higher rate of skin necrosis of NSM [28]. Although all NSMs in these studies utilized a superolateral radial incision, a possible explanation for this finding is that when selecting the internal mammary vessels as recipient vessels, excessive medial retraction is necessary to adequately expose the recipient site, and excessive flap retraction can also cause necrosis of the NSM flap. Although using the thoracodorsal artery as the recipient vessel can avoid a periareolar incision and instead favor a lateral radial incision or other more concealed incisions for the NSM procedure. However, the author does not recommend this approach, because the latissimus dorsi muscle flap, with the thoracodorsal vessels as its vascular pedicle, which can serve as a backup option in case of microvascular reconstruction failure. Additionally, for autologous flap reconstructions when choosing the superficial inferior epigastric artery (SIEA) flap [29], profunda artery perforator (PAP) flap [30], or lumbar artery perforator (LAP) flap [31], the vascular pedicles tend to be shorter, making the internal mammary vessels the optimal choice. All patients in our cohort underwent a circumareolar incision with radial extension. Clinical experience confirms that this incision type ensures oncologic safety during total mastectomy while effectively facilitating recipient vessel exposure for microvascular anastomosis. We believe that if the circumareolar component does not exceed 30%, it does not increase the risk of nipple-areola complex necrosis. A circumareolar (< 30%) incision with radial extension provides a valid basis for surgeons when planning incisions for NSM with immediate DIEP flap breast reconstruction.

This threshold was chosen based on clinical observation within our Asian patient cohort, considering that Asian breast volumes are generally smaller than those in Western populations. A weight exceeding 600 g represents a significantly larger breast volume in our patient demographic, which we hypothesized might be associated with increased complexity and potential for skin flap compromise. While this cutoff point is derived from local experience, it allowed us to categorize our patients meaningfully for risk factor analysis.

Several attempts to alter the incision location for autologous flap breast reconstruction following NSM have been proven to be feasible. Stolier A et al. [32] conducted a study involving 58 patients who underwent 82 NSMs for both cancer and prophylaxis, utilizing either vertical (at the 6 o’clock position) or horizontal incisions. Among these patients, 87.9% underwent autologous flap breast reconstruction (53.4% for DIEP and 34.5% for gluteal artery perforator flap), with No cases of NSM skin necrosis were reported. The authors suggested that radial incisions can better preserve the blood supply to the NSM skin, reduce skin necrosis, and perform better when using internal mammary vessels as recipient vessels. The use of endoscopic assistance and robotic techniques allows for more concealed incisions in the axilla, avoiding breast incisions and further protecting the blood supply to the NSM skin, reducing skin necrosis. If autologous flaps are selected after NSM, the thoracodorsal artery or lateral thoracic artery can be used as the recipient vessel [33, 34].

Patients with a higher BMI, larger breast resection weight, or increased sternal notch-to-nipple index (SNI) are at a higher risk of skin necrosis after NSM surgery in previous studies [10, 12, 35]. Chirappapha et al. [23] found a significant correlation between the volume of resected breast tissue and NAC necrosis after NSM, and patients with breast ptosis had a trend toward a higher risk of NAC necrosis, although the difference was not statistically significant. Rusby and Gui [36] reported a higher risk of NSM necrosis in patients with larger or ptotic breasts. But no correlation was found between BMI, breast ptosis, and NSM skin necrosis in our research. Further studies with larger patient cohorts are needed to confirm these findings and investigate the relationship between breast ptosis and NAC necrosis in different patient populations and surgical techniques.

Currently, there are several research attempts to reduce skin necrosis after NSM [37–40]. Surgical delay techniques, performed before NSM, are procedures conceived to improve the blood supply to the NAC in order to overcome the ischemic risk. These surgical delay techniques can effectively restore blood supply to the NAC and reduce the occurrence of necrosis [41, 42]. The three pedicles-based nipple-sparing skin-reducing mastectomy (TP-NSSRM) technique [43] and the Internal Mammary Artery Perforator (IMP)-NSM surgical technique [44], which preserves the dominant IMP to the NAC, have also been shown to significantly reduce skin necrosis after NSM. In cases where skin necrosis does occur after NSM, hyperbaric oxygen therapy may be an effective adjunctive treatment for flap salvage [45] .

Certainly, our study has several limitations, including its single-center, retrospective design. The 30% threshold for circumareolar incision length lacks external validation, and we did not evaluate the long-term aesthetic or functional outcomes of skin necrosis. Additionally, objective assessments of NAC perfusion using methods like ICG fluorescence angiography were not performed before or after mastectomy, nor after DIEP flap anastomosis. This limits our ability to definitively determine whether skin ischemia was present prior to flap transfer or if surgical retraction and prolonged ischemia time contributed to vascular compromise. Moreover, the duration of retraction hook application to the NAC during vessel anastomosis was not quantitatively recorded, which could be a contributing factor to microcirculatory compromise. Finally, the necrosis grading was conducted early in the postoperative course (2–3 weeks), meaning that delayed manifestations like areolar depigmentation might be underreported, and comprehensive long-term aesthetic outcomes were not assessed. Furthermore, our study lacked a control group utilizing alternative incisions (e.g., inframammary fold or radial incisions). Future studies should include a larger sample size, be controlled and be conducted at multiple institutions to improve the generalizability of the findings.

Conclusion

Our findings suggest that circumareolar incisions exceeding 30% of the areolar circumference may be associated with increased risk of skin necrosis following NSM with DIEP flap reconstruction. However, due to the retrospective design, limited sample size, and lack of objective perfusion assessment and long-term follow-up for aesthetic outcomes, as well as the specific limitations noted regarding multivariate analysis, these results should be interpreted with caution. Further multicenter, prospective studies are warranted to confirm these observations and determine whether this threshold can inform surgical planning without compromising oncologic or reconstructive outcomes.

Authors’ contributions

Xuhui Guo: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Writing – original draft, Software. Xilong Gong: Formal analysis, Investigation, Methodology. Yue Yang: Resources, Validation. Lina Wang: Resources, Validation. Lei Hou: Resources, Validation. Jiao Zhang: Resources, Validation. Yajie Zhao: Resources, Validation. Jia Wang: Resources, Validation. Hao Dai: Resources, Validation. Dechuang Jiao: Resources, Validation. Zhenzhen Liu: Conceptualization, Project administration, Supervision, Validation, Writing – review & editing.

Funding

Supported by National Key Clinical Discipline Construction Project (YWB0018) and Henan Province Science and Technology Development Project (242102310102).

Data availability

The datasets during the current study are available with the corresponding authors, which can be accessed, by requesting them through email.

Declarations

Ethics approval and consent to participate

This study was approved by the Ethical Review Committee of the Affiliated Cancer Hospital of Zhengzhou University (No. 2019001). As this study had a retrospective design, the requirement for informed consent was waived by the hospital. The study was performed in accordance with the Helsinki declaration.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.