Immediate surgical mesh-free implant-based breast reconstruction with fascial flap in breast cancer patients after mastectomy

Surgical meshes are often used in retro-pectoral implant-based breast reconstruction (IBBR) to improve lower pole expansion. However, using of surgical meshes is associated with increased complications and costs. To solve this problem, we have adopted a modified fascia-based IBBR technique using fasciae of pectoral major, serratus anterior, and external oblique muscles to form a sling covering the lower pole of prosthesis since 2014. Data of 788 retro-pectoral IBBR cases, including 250 fascia-based IBBR cases (fascial group) and 538 traditional IBBR cases (control group), treated between 2014 and 2019 were retrospectively analyzed. The surgical outcomes of the fascial and control group were compared. The primary endpoint was the rate of post-operative complications requiring interventions. The secondary endpoint was the rate of explantation. The exploratory endpoint was the time from surgery to complication and explantation. The fascial group had significantly lower rates of developing major post-operative complications (1.2 vs. 6.1%, p = 0.002) and losing prostheses (1.2 vs. 4.3%, p = 0.025), as compared with the control group. The median time from surgery to complication and explantation were 61 (range, 35–115) days and 92 (range, 77–134) days for the fascial group and 35 (range, 6–239) days and 63 (range, 23–483) days for the control group, respectively. Fascia-based IBBR technique had low rates of major post-operative complications and explantation. Fascia-based IBBR technique could be considered as an alternative reconstruction method in properly selected patients.


Introduction
Mastectomy is still the standard of care for early stage breast cancer patients who are not candidates for breast-conserving surgery. Immediate breast reconstruction following skinsparing mastectomy (SSM) or nipple-sparing mastectomy (NSM), which preserves the appearance of the breast, is associated with improved aesthetic outcomes and has gained 1 3 increased popularity. Implant-based breast reconstruction (IBBR), which has fewer donor site morbidity and shorter recovery time as compared with autologous reconstruction, has become the dominant reconstruction technique [1].
Retro-pectoral placement of prosthesis is often used during IBBR to reduce post-operative visibility or palpability of the implant. To prevent cranial malposition of the prosthesis and to improve lower pole expansion, the pectoralis major muscle (PM) is often detached from its lower attachments on the ribs [2]. To fully envelope the prosthesis, surgical meshes, such as bovine pericardium, acellular dermal matrix (ADM), or titanium-coated polypropylene mesh (TCPM), are generally used to cover the inferolateral part of the prosthesis [3,4]. These materials, however, are associated with increased complications and costs [5,6]. The fasciae around the mammary gland, such as the pectoral fascia, serratus anterior fascia, and external oblique fascia, have been suggested by previous studies to act as supplementary implant coverages, showing promising preliminary results [7][8][9][10]. This technique, however, has been underestimated and there are only few reports with limited data available.
We have adopted an integrated mastectomy and IBBR technique using fascial flaps as supplementary implant coverage since 2014 at our center. An institution-wide review was performed to assess the surgical outcomes of this technique. Here, we report the surgical procedure and surgeryrelated post-operative complications of this technique, as compared with traditional retro-pectoral IBBR techniques with full-muscular or surgical mesh-assisted coverage.

Study population
A retrospective review of electronic health records was performed to identify patients who underwent NSM or SSM and IBBR, including one-stage direct-to-implant (DTI) and two-stage expander-to-implant (EI) approaches, during January 2014 and December 2019 at our center. We excluded patients without breast cancer as there were few patients who underwent mastectomy for prophylactic purpose or malignant lesions other than breast cancer at our center. Patients with follow-up time shorter than 6 months were also excluded.
This study was approved by the Institutional Review Board of Tianjin Medical University Cancer Institute and Hospital and was conducted in accordance with the Declaration of Helsinki (as revised in 2013). Because of the retrospective nature of this study, the requirement for informed consent was waived.

Surgical technique
The surgical technique of fascia-based IBBR was a modified version of previously described methods [7][8][9][10][11]. Under general anesthesia with paralysis, patients were placed on the operating table in the supine position with the ipsilateral arm abducted approximately 75°. The borders of the breast were delineated on the skin. A NSM or SSM was performed to remove the mammary gland, taking care not to disturb the circummammary ligament during the operation [12]. The placement and size of the incision were at the discretion of the surgeons. Our preference is the lateral or superolateral approach, which is an excellent option for removing the breast gland while performing retro-areolar biopsy intraoperatively. During mastectomy, cares should be taken to preserve the superficial pectoral fascia (PF), especially the inferolateral part of it. Tumescence could be used to increase the sub-glandular space and facilitate the separation of the deep layer of superficial fascia of the breast from PF. After completion of mastectomy, the integrity of PF was examined to determine whether fascia-based IBBR was feasible. Patients who were not suitable for fascia-based IBBR could be offered with other techniques of IBBR. Axillary lymph node sampling was performed in a separated axillary incision.
An L-shaped incision of PF was then made parallel to the lateral border of PM and the inframammary fold (IMF) (Fig. 1a). The distances between the incision and the borders of PM and IMF varied, depending on the expected volume of the prosthesis that would be implanted, with the most commonly used distances being 5 cm medially from the lateral border of PM and 6 cm cranially from IMF. Tumescence could be applied to increase the space between PF and PM, and a sharp dissection with a scalpel was performed to separate PF from PM caudally to about 1 cm to 2 cm below IMF and laterally to the border of PM (Fig. 1b). The lateral dissection was then turned naturally to the lateral chest wall, elevating the fasciae of serratus anterior muscle and external oblique muscle, which are continuous with PF (Fig. 1c). To be noted, due to the variation of the levels of IMF in different patients, sometimes a small region of the ipsilateral anterior rectus sheath might be incorporated into the caudal part of the conjoined fascia. A continuous fascial flap that could mimic a surgical mesh was thus created (Fig. 1d).
A submuscular dissection in the space between PM and pectoralis minor was then performed. Medially, the dissection proceeded to the lateral border of the sternum. Precautions should be taken not to disrupt the intercostal branches of internal mammary vessels and the attachments of PM on the sternal border. Caudally, all of the attachments of PM were carefully freed from the ribs (Fig. 1e).
An implant or expander was then inserted into the subpectoral space and adjusted to ensure its placement in proper position (Fig. 1a). Two suction drains were placed into the subpectoral implant pocket and the subcutaneous plane, respectively. The free edge of the fascia was then approximated to the inferolateral border of PM with 3-0 Vicryl sutures to create a "hand-in-glove" fit between the implant and the fascia (Fig. 1f).
IBBRs using traditional retro-pectoral IBBR techniques, with full-muscular coverage or surgical mesh-assisted coverage, which were chosen as the control group, were performed at the preference of individual treating surgeon. The primary type of surgical mesh used in this group of patients was bovine pericardium.

Data collection
The demographic and clinicopathological characteristics, treatments in neoadjuvant and adjuvant settings, types of mastectomies, and post-operative complications of the included patients were retrieved from inpatient and outpatient charts. According to the guidelines for breast cancer follow-up at our institute, patients were followed up every 3 months in the first 2 years after surgery. Patients who failed to present after surgery were contacted via telephone or mail. Patients without follow-up information or with follow-up time less than 6 months were excluded. The time point and types of post-operative complications, if happened, were recorded for further analyses. Data were collected in December 2020. Data analysis was performed from January, 2021, to March, 2021.

Statistical analysis
The main purpose of this study was to evaluate the feasibility and safety of the fascia-based IBBR technique. We compared the surgical outcomes of patients in the fascial group to those of patients in the control group. The primary endpoint of interest was the rate of surgery-associated complications requiring medical or surgical interventions. Capsular contracture was not deemed as a surgery-associated complication in this study. Previous studies had suggested that anterior, and external oblique is formed. View from lateral side before the inferior attachments of PM are detached from the ribs. e Inferior attachments of PM on the ribs are detached. A dual-planar implant coverage composed superiorly of PM and inferolaterally of the conjoined fascia is formed. f An implant is inserted into the subpectoral space and the free edges of PM and the conjoined fascia are sutured together the cumulative rate of capsular contracture would increase as time went by and most cases of capsular contracture occurred within the first year following surgery. [13] Therefore, we explored separately the rate of capsular contracture treating with surgical intervention within the first 12 months following surgery. The secondary endpoint was the rate of explantation due to surgery-associated complications. The exploratory endpoint was the time intervals from surgery to complication and explantation.
Continuous variables were analyzed using the t test or Mann-Whitney U test, and categorical variables were analyzed using the Chi-square test or Fisher's exact test. The multivariate logistic regression model was used to adjust the associations between IBBR techniques and the development of post-operative complications. Clinicopathological characteristics including age, body mass index (BMI), type of mastectomy, neoadjuvant and adjuvant therapies, type of prosthesis, and initial volume of prosthesis were included as adjusting factors. Patients with bilateral breast cancer were deemed to be two individual cases and analyzed separately in the statistical analyses. Statistical analyses were performed using SPSS, version 22.0 for Windows (IBM Corporation). A two-sided p value < 0.05 indicated statistical significance.

Patient characteristics and treatment
A total of 788 cases including 770 Chinese female patients (18 patients with bilateral mastectomies and reconstructions) were included in this study. There were 250 cases in the fascial group and 538 cases in the control group.
Baseline characteristics of the included patients are shown in Table 1. The median age and BMI of the patients included in this study were 41 (range 21-63) years and 22.7 (range 16.9-28.3), respectively. There were no statistically significant differences regarding age and BMI between the fascial and control group. Significantly more patients in the Most of the included cases received NSM and DTI reconstruction. Compared with those in the control group, more patients in the fascial group received NSM (86.0 vs. 78.1%, p = 0.009) as well as two-stage EI reconstruction (17.2 vs. 5.2%, p < 0.001). The mean initial volume of the prostheses was significantly lower in the fascial group compared with that in the control group (246.7 vs. 273.9 ml, p < 0.001).
In the adjuvant setting, more patients in the fascial group received radiation therapy (18.0 vs. 10.8%, p = 0.005) while more patients in the control group received chemotherapy (61.6 vs. 78.6%, p < 0.001).

Complications
As shown in Table 2, 3 and 33 cases developed surgeryrelated complications requiring intervention in the fascial group and control group, respectively. Three cases in the fascial group and twenty-three cases in the control group lost implant due to complications. Cases in the fascial group had significantly lower probability of developing complications as compared with those in the control group (6.1 vs. 1.2%, p = 0.002). In line with this, cases in the control group had a higher rate of implant removal than those in the fascial group (4.3 vs. 1.2%, p = 0.025). Skin cellulitis and wound dehiscence were the most common types of complication in the whole population treated with IBBR. Among 787 cases with follow-up time more than 12 months, 0.8% (2) and 0.4% (2) of the cases in the fascial group and control group developed capsular contracture requiring surgical intervention within the first year after surgery, respectively (p = 0.596).

Time to complication and time to explantation
By December 31, 2020, the median follow-up time were 31 (range, 13-79) months and 33 (range, 11-84) months for the fascial and control group, respectively. The median time from surgery to complication were 61 (range, 35-115) days for the fascial group and 35 (range, 6-239) days for the control group. The median time from surgery to explantation were 92 (range, 77-134) days for the fascial group and 63 (range, 23-483) days for the control group.

Discussion
In this study, we evaluated the feasibility of harvesting autologous fascia as supplementary implant coverage during immediate retro-pectoral IBBR. Our data showed that the fascia-based retro-pectoral IBBR technique was associated with promising results, with significantly lower rates of postoperative complication and explantation as compared with those of traditional retro-pectoral IBBR techniques. To our knowledge, this is the largest study evaluating the surgical outcomes of fascia-based IBBR technique to date.
Although pre-pectoral IBBR has resurged in popularity in recent years, retro-pectoral IBBR remains a useful technique [14]. While pre-pectoral IBBR harbors the advantage of leaving the pectoralis muscle untouched and offering better cosmetic outcomes in properly selected patients, its success is highly dependent on a well-perfused skin flap following mastectomy. For cases with a threatened mastectomy flap, retro-pectoral IBBR technique is a wise alternative. However, cranial malposition and unsatisfied lower pole expansion are often encountered following retro-pectoral placement of prosthesis. To solve this problem, retro-pectoral IBBRs are routinely performed using dual-plane technique, which comprises detachment of PM from ribs and incorporating supplementary soft tissue or surgical mesh as an inferolateral coverage [2,15]. Surgical meshes, such as ADM, TCPM, and bovine pericardium, however, are associated with increased complications and costs [5,6,16], which could prevent some patients from considering IBBR, especially in regions where breast reconstruction is not covered by insurance. During the past decades, some surgeons have proposed the usage of fasciae around the mammary gland, such as the pectoral fascia, serratus anterior fascia, external oblique fascia, or a conjoined fascia as an alternative sling during prosthetic breast reconstruction [7][8][9][10][11]17], which have rendered encouraging preliminary results [7,18,19]. The results of our study align with these studies and confirm the feasibility and safety of incorporating fascial flap into IBBR as a supplementary prosthetic coverage. Specifically, our results showed that fascia-based procedure was associated with significantly lower rates for developing major post-operative complications, as compared with the traditional retro-pectoral IBBR techniques. This might derive from the autologous and well-vascularized nature of the fascial flap. Indeed, when traditional retro-pectoral IBBR techniques were divided into full-muscular and mesh-assisted subgroups according to the implant coverage used, we found that fascia-based technique had similar risk of complications as full-muscular technique, which also incorporated autologous and well-vascularized muscular tissues as prosthetic coverage. On the other hand, surgical mesh-assisted technique was associated with significantly higher risk of post-operative complications when compared with that of full-muscular technique.
Even though with the advantage of reduced risk of complications, the fascia-based IBBR technique faces several challenges, which might have limited its application in clinical practice. First, this technique is highly dependent on well preservation of the fascial flaps around the corpus mammae during mastectomy, which is especially challenging in patients with low BMI index, as indicated in previous studies [11,20]. Second, the innate limitations relating to the maximal available surface of fascia that could be harvested imply that this technique is optimal for patients with breasts of small to medium size and without significant ptosis. As shown in our study, the mean initial volume of prostheses  [7,18,19,21]. Nevertheless, we have found in our practice that patients with proportional breast size to their body size and habitus generally had sufficient fascial flaps as supplementary prosthetic coverage after mastectomy. Third, this technique could also be challenging when mastectomy and reconstruction procedure are performed separately by oncological and plastic surgeons, which are often the case in some regions around the world. Excessive oncological dissection might cause iatrogenic injury to the fascial flap or jeopardize their blood supply, which could increase the risk of complications. Nonetheless, the fascia-based IBBR technique remains a valuable alternative method for breast reconstruction, especially in DTI setting. Surgical mesh-sparing approach could significantly reduce the overall cost, which has been proved in previous study [22]. Furthermore, fascia-based technique has a lower rate of post-operative complications, which means a reduced revision rate and less additional costs. Moreover, fascia-based IBBR technique might be more tolerable to post-operative radiation therapy, as compared with traditional IBBR techniques. As shown in this study, adjuvant radiation therapy was associated with an increased rate of post-operative complications, which aligns with a previous study that has also showed the reverse impact of adjuvant radiation on implant-based reconstruction [23]. As shown above, although about 18% of patients in the fascial group received adjuvant radiation therapy, there were few cases in this group who developed major post-operative complications. Further studies comparing the rates of postradiation complications between fascia-based and traditional IBBR techniques in patients who are treated with adjuvant radiation therapy are thus warranted. The rate of severe capsular contracture within the first year after surgery was also relatively low in patients within the fascial group. All these results suggest that using of fascia-based IBBR technique can achieve reliable outcomes in properly selected patients.
Our study has several limitations. As a non-randomized retrospective study, we were unable to control some imbalances of baseline characteristics. Also, we did not compare the cosmetic outcomes between fascia-based and traditional IBBR technique as patients-reported outcomes regarding the reconstructed breast might change over time [24]. On the other hand, the oncological soundness of preserving PF remains a concern to some oncologists [25], even though many surgeons have opted for preservation of this fascia to reduce the risk of implant extrusion [26]. To elucidate these questions, a prospective cohort study is now undergoing in our center to evaluate the oncological and cosmetic outcomes of fascia-based IBBR technique.
In conclusion, the results of this study prove that fascia-based IBBR technique is a feasible, reliable, and valid method for post-mastectomy reconstruction in breast cancer patients. This technique is a valuable alternative IBBR technique in properly selected patients, i.e., those with small-to medium-sized and non-ptotic breasts.
Author contributions A-XC: data collection and analysis, manuscript writing. XC: data collection. YY: data collection. XW: data collection, manuscript editing. BZ: project development, manuscript editing. X-CC: project development, data management, and manuscript editing.
Funding This work was supported by the National Natural Science Foundation of China (No. 81502300, NO. 82172827, and NO. 82172835) and Tianjin Key Medical Disciplines (Specialty) Construction Project (TJYXZDXK-009A).

Availability of data and material
The datasets of the current study are available from the corresponding author on reasonable request.

Declarations
Conflict of interest Ao-Xiang Chen, Xiao Chen, Yue Yu, Xin Wang, Bin Zhang, and Xu-Chen Cao have no conflict of interest to declare.
Ethical approval This study was conducted in accordance with the current guidelines for good and sound research practice (including the 1964 Helsinki declaration and its later amendments) after approval from The Ethic Committee of Tianjin Medical University Cancer Institute and Hospital. As a retrospective study, there was no testing or manipulation of the patient's standard of care. For this type of study, formal consent is not required.