The postoperative outcomes and oncological safety of free dermal fat graft for breast reconstruction

Introduction

Breast cancer is the second most common malignant tumor in women worldwide, with newly diagnosed cases ranking first among all types of cancer, and there is a trend towards younger age at onset (1,2). With the further development of molecular biology research, adjuvant therapy, and radiotherapy, the survival rate of breast cancer patients continues to improve. In contemporary healthcare, patients are increasingly prioritizing the maintenance of their quality of life (QoL). Therefore, in addition to disease treatment, medical care should also focus on addressing patients’ needs and enhancing their overall well-being (3,4). Breast cancer surgery has evolved from radical mastectomy to breast-conserving surgery (BCS) and nipple-areola sparing mastectomy, with the combination of immediate breast reconstruction (IBR), which has revolutionized the improvement in the cosmetic results and patients’ satisfaction (5,6). Since Kijima et al. (7) described the application of autologous free dermal fat graft (FDFG) for IBR, where fat harvested via liposuction from the abdomen, flanks, or thighs is used to fill the breast defect-this technology has gained increasing interest, particularly in patients with a high body mass index (BMI) or a history of radiation therapy (5,8). This approach not only enables single-stage surgical completion while preventing the psychological and physical trauma associated with breast loss but also effectively corrects breast contour asymmetry and enhances overall breast volume (7,9,10).

However, an investigation involving 110 hospitals in China showed that autologous breast reconstruction (ABR) only accounts for approximately one-third of breast reconstruction cases (11). The complexity of the surgery and the following complications, such as necrosis, hernia, fatty melting, and delayed incision healing, have hindered the development of the ABR (11-13). Local recurrence primarily occurs in the area surrounding the mastectomy scar, which may be associated with intraoperative tumor cell implantation. Additionally, there is a certain risk of recurrence in the ABR (13,14). Currently, no unified standard methods for screening breast reconstruction tissues have been established and there is still a lack of sufficient data on the oncological safety of FDFG for ABR. However, it has been reported that reconstructing the breast in a symmetric and cosmetic form is beneficial to patients’ psychological well-being and QoL (15,16). Breast Cancer Patient-Reported Outcomes Questionnaire (BREAST-Q) is a standardized and widely-validated patient-reported outcome measurement, designed and catalyzed by the contemporary patients-centered conception, which not solely relies on clinicians’ experience but underscores the patients’ satisfaction (17). Therefore, this study aims to explore the early stage of clinical and aesthetic outcomes of FDFG and also further evaluate the surgical efficacy by following-up study on the serum tumor markers and postoperative recurrence in patients. We present this article in accordance with the STROBE reporting checklist (available at https://gs.amegroups.com/article/view/10.21037/gs-2025-109/rc).

Methods

Study design and population

This is a retrospective study and data from patients who were in clinical staging of I, II, or IIIA breast cancer and had clear willingness for BCS were collected from the Department of Breast and Thyroid Surgery 2 of Liuzhou People’s Hospital in China between June 2015 and June 2023. The pathological stage was determined according to the 8th American Joint Committee on Cancer (AJCC) classification. The exclusion criteria were as follows: (I) patients underwent neoadjuvant therapy and failed to achieve tumor downstaging; (II) tumor location is less than 2 cm from the nipple margin or its size was over 5 cm; (III) with palpable enlarged lymph nodes in the axilla; (IV) with diffuse suspicious cancer foci or microcalcifications that cannot be removed with extensive local excision without affecting aesthetics; (V) severe internal medical conditions, including unstable angina, myocardial infarction, or cerebrovascular accidents within the last 6 months; (VI) medical conditions that would impact postoperative radiotherapy, such as previous breast or chest wall radiation or active connective tissue diseases involving the skin; (VII) pregnancy or lactation.

The FDFG group involved patients with adequate abdominal fat for grafting, estimated volume of tumor removal larger than 20% of the breast or tumor located in the upper inner quadrant, and who underwent BCS and FDFG for IBR. All the other patients who refused or were unsuitable for breast reconstruction were grouped into the traditional breast-conserving surgery (TBCS) group. This study was approved by the Ethics Committee of Liuzhou Maternity and Child Healthcare Hospital (No. 20170324068). This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. Informed consent was waived by the Ethics Committee for this retrospective study due to the exclusive use of de-identified patient data, which posed no potential harm or impact on patient care.

Perioperative management

BCS consisted of the excision of the lesion with confirming a negative margin and the resected tissue was measured intra-operatively to decide the size of FDFG from the lower abdomen. Surgeons used a scalpel or scissors to remove the epidermis, followed by shaping the graft to match the contour of the recipient area. Thinning was performed at the edge of the breast area, while the part near the areola was relatively thicker to achieve a more natural appearance. The grafts were excised with a cold scalpel to a maximum thickness of 2.5 cm, weighed, and transferred to the recipient breast area. To compensate for potential volume loss, the graft size exceeded the defect volume by 10–20%. The FDFG was then implanted with its dermal side facing the pectoralis muscle surface and secured with interrupted sutures. A drainage device was placed and excessive pressure bandaging was avoided. Radiotherapy, chemotherapy, endocrine therapy or targeted therapy were determined by the results of paraffin pathology and with the breast cancer guidelines of the Chinese Society of Clinical Oncology (CSCO) after the surgery.

Follow-up and outcomes

The aesthetic outcomes were evaluated with the usage of the BREAST-Q reconstruction module and patients were asked to complete the questionnaire when it was one month after their fat grafting surgery. The BREAST-Q reconstruction includes four sections: satisfaction with breasts, psychosocial well-being, sexual well-being and physical well-being: chest. Patient scores range from 0 to 100, with higher values representing a more favorable outcome.

Patients were asked for follow-up in six months, one, and three years after surgery. Physical examinations, ultrasonography, mammography and tumor markers—cancer antigen 125 (CA125), cancer antigen 15-3 (CA15-3), carcinoembryonic antigen (CEA)—were performed for monitoring the recurrence or metastasis. Local recurrence was defined as the reappearance of tumor tissue within the same side of the chest wall where the surgery was performed, including the skin, subcutaneous tissue, and muscle in that area. Regional recurrence was defined as the spread of the tumor to lymph nodes in the same side of the body, including the axillary (armpit), internal mammary, supraclavicular or infraclavicular lymph nodes. Any recurrence in locations other than the aforementioned areas was categorized as distant metastases, meaning that the cancer had spread to other parts of the body (14).

Statistical analysis

Statistical analysis of the data was conducted using SPSS 26.0 software and figures were depicted by GraphPad Prism (version 9). Normally distributed continuous data were represented as mean ± standard deviation and compared between groups using the t-test. Categorical data were presented as frequency (percentage %) and compared using either the Chi-squared test or Fisher’s exact probability test. For non-normally distributed data, the median [Q25, Q75] was used, and group comparisons were made using the Mann-Whitney U test. Mixed effect model (REML) was applied on repeatedly measured data analysis (P<0.05 was considered statistically significant).

Results

Demographic characteristics

A total of 106 patients with age 43 [37, 49] years old and BMI 21.71 [20.29, 23.35] kg/m² were included in the study, of which 52 (49.06%) were FDFG group and 54 (50.94%) were TBCS group (Table 1). Though there were more patients with human epidermal growth factor receptor 2 (HER2)-positive breast cancer than patients with HER2-negative breast cancer in both the FDFG and TBCS group, the frequency of HER2-positive cases was significantly higher in FDFG compared with TBCS.

Surgical efficacy

The postoperative outcomes of the FDFG and TBCS group, showed that the patients undergoing FDFG had longer operation time (median 132 vs. 103 minutes, P<0.001), greater intraoperative bleeding volume (316.75±23.44 vs. 291.96±23.88 mL, P<0.001) and postoperative drainage volume (101.46±22.37 vs. 81.19±19.90 mL, P<0.001) and heavier resected breast tissue (89.9±13.82 vs. 83.20±13.00 g, P<0.001). In addition, no significant difference in the total incidence of complications was observed between the two groups with FDFG of 35.19% vs. TBCS of 34.62% (P=0.95), which included fat necrosis (9.62% vs. 7.41%, P=0.68), hemorrhage (11.54% vs. 12.96%, P=0.82), poor wound healing (11.54% vs. 9.26%, P>0.05) and infections (9.62% vs. 7.41%, P=0.70) (Table 2).

Breast-Q outcome

The results of Breast-Q-based cosmetic outcomes are shown in Table 3. All the patients completed the survey and submitted valid answers one month after the surgery. The FDFG group reported more favorable outcomes with significantly higher scores in satisfaction with the breasts (mean score 75 vs. 67, P=0.02) and psychosocial well-being (mean score 73 vs. 65, P=0.72) in comparison. There were no significant differences in physical well-being: chest (mean score 80 vs. 78, P=0.044) and sexual well-being (mean score 50 vs. 48, P=0.19) between the two groups.

Recurrence

The follow-up from the operation was for 3 years, and Table 4 presents the recurrence evaluation during this period. The total 3-year survival rate was 80.19%. There were no significant differences in the survival rate curve (Figure 1, Mantel-Cox analysed the curves of two groups with P=0.83), local recurrence rate (TBCS =27.78% vs. FDFG =26.92%, P=0.92), regional recurrence rate (TBCS =11.11 vs. FDFG =5.77%, P=0.32) and distant metastases rate (TBCS =11.11% vs. FDFG =13.46%, P=0.71) between the two groups (Table 4). Figure 2 shows the results of the serum CA125, CA15-3 and CEA before and after the surgery, respectively. The mixed effect model suggested that no group effect but time effect (P<0.001) and group-time interactive effect (P=0.006) were significant in the tumor markers. Generally, the amount of tumor markers decreased dramatically once the surgery was performed with CA125 from the mean value of 46.81 to 36.11 U/mL, CA15-3 from 42.99 to 35.08 U/mL and CEA from 43.33 to 34.47 mg/mL and continued to decrease during the follow-up period in FDFG patients (Figure 3). However, an increase in patients’ CA125 levels was observed, with an average rise from 33.13 to 34.19 U/mL over the course of the past two years (Figure 3, P=0.02).

Figure 1 Comparison of postoperative survival rate curve in the TBSC and FDFG groups. FDFG, free dermal fat graft; TBCS, traditional breast-conserving surgery.

Figure 2 Comparison of tumor markers in TBCS and FDFG patients. CA125, cancer antigen 125; CA15-3, cancer antigen 15-3; CEA, carcinoembryonic antigen; FDFG, free dermal fat graft; TBCS, traditional breast-conserving surgery.

Figure 3 The trend of tumor marker in FDFG patients during the follow-up. *, P<0.05; **, P<0.01; ***, P<0.001; ****, P<0.0001. CA125, cancer antigen 125; CA15-3, cancer antigen 15-3; CEA, carcinoembryonic antigen; FDFG, free dermal fat graft.

Discussion

In this study, we compared the outcomes of FDFG breast reconstruction with TBCS in patients diagnosed with breast cancer at early stages. Our findings reveal several important insights. The insignificant disparities in complication rates are reassuring and underscore the safety profile of FDFG breast reconstruction in comparison to traditional TBCS. However, nearly one-third of the FDFG patients were subjected to postoperative complications in this study, which is relatively high in contrast with the average reported complication rate of 8.4% in patients undergoing autologous fat grafting (AFG) (15). Fat necrosis was identified as the most common complications with up to 50% occurrence reported by Shamoun et al. (16), but in another pooled study consisting of 160 patients the prevalence of fat necrosis is 6.2% and it has been demonstrated that the incidence of complications are associated with the volume of the grafting fat (18,19). Kijima et al. (12,20) and our previous study also identified the weight and the thickness of FDFG as independent influencing factors (21). The observation of a higher complication rate associated with higher graft volume or weight in the study presents an intriguing avenue for discussion. This phenomenon can be attributed to several factors, with the most prominent being the challenges related to vascular supply and oxygen diffusion within the transplanted fat tissue. This issue is further exacerbated in the central region of the fat globule, leading to a higher risk of necrosis. However, in contrast, adipocytes located in the peripheral layer tend to survive better due to processes such as imbibition and revascularization. This finding underscores the paramount importance of surgical technique in achieving favorable outcomes, potentially outweighing the influence of the processing system used for the graft (19).

Although FDFG is associated with longer operation time, increased intraoperative bleeding, and greater postoperative drainage volumes, the cosmetic outcomes observed were notably positive. The majority of patients undergoing FDFG in our study reported that the results met or exceeded their expectations, a finding consistent with previous studies (12,20,22,23). The findings of the present study demonstrate a concurrence with the conclusions of previous investigations that have demonstrated that FDFG provides a higher level of patient satisfaction in relation to breast reconstruction (16). Furthermore, the strong link between cosmetic outcomes and psychological well-being in breast cancer patients underscores the significance of successful reconstructive procedures. Research has shown that patients undergoing IBR not only benefit from the physical restoration but also experience significant improvements in self-esteem, body image, and overall emotional health (4,9). These improvements extend across all psychosocial dimensions, including reduced anxiety, depression, and social isolation, which are critical factors in the post-cancer recovery process. In our study, FDFG patients similarly exhibited higher scores in psychosocial well-being, suggesting that the cosmetic satisfaction derived from FDFG contributes directly to better mental health and overall life satisfaction. This preference further highlights the potential of FDFG to not only meet aesthetic expectations but also provide deeper psychological benefits. Given the intertwined nature of physical appearance and emotional recovery, FDFG emerges as a highly valuable option for patients seeking a holistic improvement in their post-reconstruction QoL, addressing both aesthetic and psychological dimensions of well-being.

One of the paramount concerns in the field of breast reconstruction is the oncological safety of the procedure. In our study, no significant differences in the survival rate curve, recurrence rate or distant metastases rate between the FDFG and TBCS groups. A mixed-effects model analysis revealed that there was no significant group effect on these tumor markers, but the time effect and group-time interactive effect were significant. Generally, the tumor marker levels decreased dramatically postoperatively and continued to decline during the follow-up period in FDFG patients. This trend aligns with the successful treatment of breast cancer. These findings are reassuring, suggesting that FDFG does not compromise the oncological safety of breast cancer treatment. A number of clinical research comparing oncological outcomes in BCS followed by AFG have found neither an increased risk of recurrence nor a different survival rate, while some studies indicate a higher risk of recurrence in patients with FDFG (16,17,24-26). A study reported that the local recurrence rate of 9.4% in the FDFG group was significantly higher than that in the TBCS groups (1.9%) (27). It’s worth noting that patients’ CA125 levels increased slightly between the last two years in our study. Palacios Huatuco et al. reported that a patient who showed elevated levels of CA15-3 was diagnosed with metastasis 15 years after the mastectomy and IBR (28). The patient is free of disease 4 years after surgery. Therefore, this clinical significance may require further research with a longer follow-up period.

Our study contributes to the growing body of research on breast cancer treatment and reconstruction options. The high patient satisfaction rates with FDFG suggest that it can be a valuable technique in addressing the aesthetic concerns of patients undergoing breast cancer surgery. Importantly, our findings affirm the oncological safety of FDFG in the short term, providing confidence in its use as a reconstructive option. However, there are some limitations in our study. The current analysis is restricted to Breast-Q questionnaire assessments conducted only at the 1-month postoperative time point. This relatively short follow-up period primarily captures patients’ immediate postoperative satisfaction, which may not fully reflect long-term outcomes. Subsequent research could benefit from a prolonged follow-up (1–3 years) to systematically assess the sustainability of patient satisfaction regarding surgical efficacy. Additionally, as a retrospective study, there are inherent limitations in controlling for confounding factors. A propensity score evaluation was not conducted to mitigate the impact of unintended bias on the trial results. Therefore, prospective randomized controlled trials may be necessary in the future to further validate the findings. Long-term follow-up studies are needed to confirm the durability of aesthetic outcomes and to continue monitoring for oncological safety.

Conclusions

In conclusion, our study underscores the potential benefits of FDFG breast reconstruction, particularly in achieving high patient satisfaction without compromising oncological safety in the early postoperative period. While further research is needed to address the questions raised by our findings, this study contributes to the ongoing efforts to improve the QoL and outcomes for breast cancer patients undergoing reconstructive surgery.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://gs.amegroups.com/article/view/10.21037/gs-2025-109/rc

Data Sharing Statement: Available at https://gs.amegroups.com/article/view/10.21037/gs-2025-109/dss

Peer Review File: Available at https://gs.amegroups.com/article/view/10.21037/gs-2025-109/prf

Funding: This study was supported by Clinical Research of Breast-conserving Surgery Combined with Free Dermal-Fat Flap Transplantation for Breast Cancer (No. Z20170474).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://gs.amegroups.com/article/view/10.21037/gs-2025-109/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. This study was approved by the Ethics Committee of Liuzhou Maternity and Child Healthcare Hospital (No. 20170324068). This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. Informed consent was waived by the Ethics Committee for this retrospective study due to the exclusive use of de-identified patient data, which posed no potential harm or impact on patient care.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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