Abstract
Purpose:
Postoperative infection rates in the United States following breast cancer surgery range from 2–26%. Management of post-lumpectomy defects may involve simple skin closure or oncoplastic closure; however, the effect of defect repair on postoperative infection rates has not been well documented. Here we determine how oncoplastic closure of partial mastectomy defects affects postoperative infection rates and antibiotic use.
Methods:
In this retrospective single-institution study, patients undergoing lumpectomy with and without oncoplastic closure of defect were included between 2018–2020. Clinicopathologic/treatment data were collected from medical records. Patients receiving antibiotics on postoperative days 5–30 were reviewed to confirm wound infection. Associations between demographic and clinicopathologic factors and postoperative infections were analyzed.
Results:
3937 patients met eligibility criteria; 2273 (58%) had oncoplastic closure. The overall postoperative wound infection rate was 8.4% (332), and true surgical site infection was seen in 70 (1.8%) patients. On univariate analysis, age ≥60 years, diabetes, hypertension, and BMI≥30 were associated with increased breast infection. Oncoplastic closure was protective against postoperative breast infections (odds ratio [OR]0.70, p=0.040). On multivariable analysis oncoplastic closure had marginally decreased breast infection rates (OR 0.71, p=0.053); however, this was not significant. BMI≥30 was the only risk factor that remained a significant predictor of increased breast infection rates (OR1.63, p=0.021).
Conclusions:
Oncoplastic closure of lumpectomy defects had marginally significant lower rates of postoperative breast infections. As oncoplastic techniques are increasingly adopted in breast-conserving surgery, it is important to further study the protective nature of lumpectomy defect closure to reduce postoperative infection rates.
Keywords: breast cancer, surgical site infection, wound infection, antibiotics, partial mastectomy, lumpectomy
INTRODUCTION
Breast-conserving surgery followed by postoperative radiation has been shown to be equivalent to mastectomy for the local control of early breast cancer [1–3]. Breast conservation involves excision of the tumor with clear margins of normal breast tissue. Management of this tissue defect can include a simple skin closure or adding a more complex closure of lumpectomy defect, including displacement of the glandular tissue to close the dead space. This is often referred to as an oncoplastic closure, which involves tissue rearrangements and deeper closure of the defect, often resulting in improved cosmetic results. Additionally, there is evidence that closure of the lumpectomy defect’s dead space leads to lower rates of breast seromas, which have been linked to decreased postoperative infection rates [4, 5].
Breast surgery is considered a Class 1 clean case; however, surgical site infection rates after breast surgery are highly variable ranging from 2 to 26% [6–9]. The Centers for Disease Control and Prevention (CDC) in the United States has reported specific criteria that must be met for the diagnosis of surgical site infection, which must occur within 30 days of operation [10]. To be considered as a true surgical site infection, patients must present with at least one of the following: purulent drainage; positive culture; or surgical site infection requiring incisional opening by a clinician, along with either signs/symptoms of infection or formal diagnosis of a surgical site infection by a clinician [10]. Of note, this criterion excludes cellulitis as a superficial surgical site infection, which often may require treatment with antibiotics.
Postoperative infection may lead to hospitalizations, delays in adjuvant treatment, poor cosmetic results, and increased psychological burden for patients. As such, understanding risk factors and methods to reduce postoperative infections is important. However, data to evaluate the role of closure of the lumpectomy defect on postoperative infection rates are limited [7]. The aim of this study was to determine how oncoplastic closure of partial mastectomy defects affects rates of postoperative infection and postoperative antibiotic use.
METHODS
Upon approval by the institutional review board of Memorial Sloan Kettering Cancer Center (New York, NY, USA), we queried our prospective database for female patients undergoing lumpectomy for breast cancer between 2018 and 2020 with oncoplastic closure of their partial mastectomy defect (CoD) or without oncoplastic closure of their defect (NCoD). For this cohort, CoD involved only level 1 oncoplastic techniques and were conducted solely by breast surgeons, without assistance from plastic surgery. The oncoplastic closures predominately involved primary approximation of the defects with tissue mobilization, and occasional crescent or donut mastopexies. Furthermore, our institution’s standard practice includes a separate incision for the breast and axilla The sentinel nodes were excised through the lumpectomy incision when the primary was close to the breast axillary tail. Exclusion criteria included patients lacking documentation on management of their lumpectomy defect and patients who underwent re-excision, as data on postoperative antibiotic use was recorded only from the time of the first procedure. Additionally, patients who underwent mastectomy within 3 months of initial lumpectomy were excluded. Male patients were excluded due to the limited sample size.
Clinicopathologic and treatment data were collected from an institutional tumor registry and from medical records. Demographic and clinicopathologic data included age at surgery, comorbidities, neoadjuvant treatment, histology, receptor status, clinical and pathologic tumor, and nodal stage. Surgical closure of the defect, if performed, and technique were collected from surgeon operative reports. Patient comorbidities, including cardiovascular disease (history of myocardial infarction, hypertension, hyperlipidemia, stroke, and peripheral vascular disease), renal disease, COPD, diabetes, and smoking status were collected from medical records.
At our institution, preoperative antibiotic prophylaxis is recommended for patients undergoing mastectomy, axillary lymph node dissection, or implant-based reconstruction based on previous studies investigating prophylactic antibiotic use in breast cancer surgery [11]. For patients undergoing lumpectomy, prophylactic antibiotics are not routinely recommended unless other risk factors are present [12, 13]. Antibiotic use was collected from medical records and subclassified into three categories: 1) antibiotic use from postoperative day 0–1 (defined as perioperative antibiotics); 2) antibiotic use from postoperative days 2–4 (defined as prolonged perioperative antibiotics); and 3) antibiotic use from postoperative days 5–30 (defined as postoperative antibiotics). Patients who received postoperative antibiotics were reviewed to further evaluate the reason for antibiotic prescription, type, and severity of infection. Wound infection was defined as either cellulitis or a true surgical site infection (purulent drainage, positive culture, surgical site requiring incisional opening, or signs/symptoms of infection with formal diagnosis by a clinician) based on CDC criteria [10].
Statistical analysis
Demographic and clinicopathologic data were descriptively compared between those who had and did not have postoperative breast infections (including both cellulitis and true surgical site infections as defined by the CDC). Univariate (UVA) and multivariable (MVA) logistic regression analyses were conducted to study the association of all clinicopathologic and demographic characteristics with postoperative infection. All collected variables were included in the analysis; a priori selection of variables was not done. All factors that were significant in the UVA at the type I error rate of 0.05 were included in the MVA. All statistical analyses were conducted using R 4.3 (R Foundation for Statistical Computing, Vienna, Austria).
RESULTS
Patient and treatment characteristics
A total of 3937 patients met study eligibility criteria between January 2018 and December 2020. Of those patients, 2273 (58%) had their partial mastectomy defect closed by oncoplastic repair, while 1664 (42%) did not. Most patients were White (81%), followed by Asian (10%) and Black (9.2%), and 8.2% identified as Hispanic. There was no statistically significant difference in patient age, BMI (median BMI 27), prior myocardial infarction, or stroke between patients undergoing CoD versus NCoD. The proportion of current and former smokers was slightly higher in the NCoD cohort (41.4% vs 36.5%, p = 0.016), and there was a slightly larger proportion of patients with diabetes in the CoD cohort (8.5% vs 6.1%, p = 0.003). The CoD cohort also had a significantly greater proportion of patients undergo neoadjuvant chemotherapy (14% vs 11%, p = 0.004). Perioperative antibiotics were given to 1025 patients (26%) in this study. A greater proportion of the CoD cohort received perioperative antibiotics as compared to the NCoD cohort (29% vs 22%, p < 0.001) (Table 1). However, there was no significant difference in the rate of perioperative antibiotic use in patients that developed a wound infection (cellulitis or true surgical site infection) versus those who did not (30% vs 26%, p = 0.131).
TABLE 1.
Patient demographics and preoperative comorbidities
| Characteristic | Overall (n = 3937) |
No Closure of Defect (n = 1664) |
Closure of Defect (n = 2273) |
p-value |
|---|---|---|---|---|
| Age, years, n (%) | 0.18 | |||
| < 60 | 1817 (46%) | 747 (45%) | 1070 (47%) | |
| ≥ 60 | 2119 (54%) | 916 (55%) | 1203 (53%) | |
| BMI, n (%) | 0.210 | |||
| < 25 | 1342 (34%) | 545 (33%) | 797 (35%) | |
| 25–29 | 1286 (33%) | 545 (33%) | 741 (33%) | |
| ≥ 30 | 1265 (32%) | 557 (34%) | 708 (32%) | |
| Smoking status | 0.016 | |||
| Current | 168 (4.8%) | 76 (5.4%) | 92 (4.5%) | |
| Former | 1170 (34%) | 510 (36%) | 660 (32%) | |
| Never | 2140 (62%) | 833 (59%) | 1307 (63%) | |
| Diabetes, n (%) | 295 (7.5%) | 101 (6.1 %) | 194 (8.5%) | 0.003 |
| Hypertension, n (%) | 756 (19%) | 275 (17%) | 481 (21%) | < 0.001 |
| Hyperlipidemia, n (%) | 747 (19%) | 261 (16%) | 486 (21%) | < 0.001 |
| Myocardial infarction, n (%) | 18 (0.5%) | 8 (0.5%) | 10 (0.4%) | 0.849 |
| Stroke, n (%) | 24 (0.6%) | 8 (0.5%) | 16 (0.7%) | 0.373 |
| COPD, n (%) | 35 (0.9%) | 18 (1.1%) | 17 (0.7%) | 0.271 |
| Neoadjuvant Chemotherapy, n (%) | 506 (13%) | 184 (11%) | 322 (14%) | 0.004 |
| Perioperative antibiotics, n (%) | 1025 (26%) | 370 (22%) | 655 (29%) | < 0.001 |
Bolded values indicate statistical significance; unrecorded values not included in all percentage calculations
COPD chronic obstructive pulmonary disease, BMI body mass index
The majority of cancers included in this study were tumors less than 2 cm, with clinical T1 tumors representing 64% of patients, followed by clinical T2 (17%) and Tis (17%). There was no statistically significant difference in the proportion of patients who had ductal carcinoma in situ (DCIS) versus invasive carcinoma in those with CoD versus NCoD (DCIS, 16% vs 16%, and invasive carcinoma, 84% vs 84%, respectively). Patients who had CoD were more likely to have hormone receptor-positive (HR+)/human epidermal growth factor receptor 2-positive (HER2+) cancer (10% vs 5.7%, p = 0.002). There was no difference in the proportion of node-positive (N1–3) patients undergoing CoD versus NCoD (14.7% vs 14.2%, p = 0.4) (Table 2).
TABLE 2.
Tumor histology, subtype, and pathologic nodal stage
| Characteristic | Overall (n = 3937) |
No Closure of Defect (n = 1664) |
Closure of Defect (n = 2273) |
p-value |
|---|---|---|---|---|
| Histology, n (%) | 0.907 | |||
| DCIS | 612 (16%) | 256 (16%) | 356 (16%) | |
| Invasive Carcinoma | 3303 (84%) | 1390 (84%) | 1913 (84%) | |
| Subtype, n (%) | 0.002 | |||
| HR+/HER2− | 1614 (77%) | 659 (80%) | 955 (75%) | |
| HR+/HER2+ | 176 (8.4%) | 47 (5.7%) | 129 (10%) | |
| HR−/HER2+ | 59 (2.8%) | 20 (2.4%) | 39 (3.0%) | |
| TNBC | 251 (12%) | 93 (11%) | 158 (12%) | |
| Pathologic, n (%) | 0.4 | |||
| N0 | 2703 (86%) | 1118 (86%) | 1585 (86%) | |
| N1 | 394 (13%) | 162 (13%) | 232 (13%) | |
| N2–3 | 47 (1.5%) | 15 (1.2%) | 32 (1.7%) |
Bolded values indicate statistical significance; unrecorded values not included in all percentage calculations
DCIS ductal carcinoma in situ, HR hormone receptor, HER2 human epidermal growth factor receptor 2, TNBC triple-negative breast cancer
A total of 498 (12.6%) patients received postoperative antibiotics. Of those patients, 332 (66.7%) received antibiotics for a surgical wound infection, while 166 (33.3%) patients received antibiotics for reasons not related to their surgical wound. The most common reasons for receiving antibiotics outside of a wound infection were re-excision, plastics procedure, or reoperation (113, 68%). This was followed by infections at other body sites (28, 17%) and hematomas (13, 7.8%). Patients also received postoperative antibiotics for urinary tract infections, pneumonia, and gastrointestinal infections (Table 3).
TABLE 3.
Postoperative antibiotic use for reasons other than wound infection
| Reason | N (%) (n = 166) |
|---|---|
| Re-excision, plastics procedure, reoperation | 113 (68%) |
| Infection at other body site | 28 (17%) |
| Urinary tract infection | 8 (4.8%) |
| Hematoma | 13 (7.8%) |
| Pneumonia | 2 (1.2%) |
| Gastrointestinal infection | 2 (1.2 %) |
Of the 332 patients who developed a postoperative wound infection (including cellulitis), 213 (64%) were breast infections and 132 (40%) were axillary infections (Fig. 1). A true surgical site infection as defined by the CDC was seen in 70 (1.8%) patients. In those undergoing CoD, overall wound infection rates (both breast and axillary) were lower than NCoD (6.9% vs 11%, p < 0.001), and there were lower rates of breast infections in those with CoD (4.7% vs 6.8%, p = 0.010). There was no statistically significant difference in true surgical site infection as defined by the CDC in those with CoD versus NCoD (1.6% vs 2.0%, p = 0.280) (Table 4).
Fig. 1.
Overall postoperative wound infection rates.
TABLE 4.
Postoperative breast infection rates
| Characteristic | Overall (n = 3937) |
No Closure of Defect (n = 1664) |
Closure of Defect (n = 2273) |
p-value |
|---|---|---|---|---|
| Wound infection, n (%) | 332 (8.4%) | 175 (11%) | 157 (6.9%) | < 0.001 |
| Breast infection, n (%) | 213 (5.4%) | 108 (6.8%) | 105 (4.7%) | 0.010 |
| Axillary infection, n (%) | 134 (3.6%) | 78 (5.0%) | 56 (2.6%) | < 0.001 |
| True SSI, n (%) | 70 (1.8%) | 34 (2.0%) | 36 (1.6%) | 0.280 |
Bolded values indicate statistical significance; unknowns not included in all percentage calculations
SSI surgical site infection; wound infection includes breast and axillary infections.
On univariate analysis, risk factors that were associated with increased postoperative breast infections (including cellulitis) included age ≥ 60 years (odds ratio [OR] 1.48, p = 0.007), diabetes (OR 1.78, p = 0.009), hypertension (OR 1.48, p = 0.019), and BMI ≥ 30 (OR 1.88, p = 0.001). CoD was protective against developing a postoperative breast infection (OR 0.70, p = 0.040), as was neoadjuvant chemotherapy (OR 0.59, p = 0.042), when compared with NCoD. On multivariable analysis, CoD had lower breast infection rates (OR 0.71, p = 0.053); however, this was not statistically significant. BMI ≥ 30 was the only risk factor that remained a significant predictor of increased breast infection rates (OR 1.62, p = 0.021) on multivariable analysis (Table 5).
TABLE 5.
Risk factors associated with postoperative breast infections
| Variables | Univariate Analysis | Multivariable Analysis | ||
|---|---|---|---|---|
| OR (95% Confidence Interval) |
p-value | OR (95% Confidence Interval) |
p-value | |
| Age ≥ 60 | 1.48 (1.11 –1.97) | 0.007 | 1.29 (0.96–1.74) | 0.090 |
| Diabetes | 1.78 (1.16–2.75) | 0.009 | 1.42 (0.90–2.26) | 0.130 |
| Hypertension | 1.48 (1.07–2.06) | 0.019 | 1.19 (0.84–1.70) | 0.300 |
| Stroke | 1.59 (0.37–6.86) | 0.500 | ||
| COPD | 0.49 (0.07–3.56) | 0.500 | ||
| Former smoker | 1.18 (0.56–2.51) | 0.800 | ||
| History of myocardial infarction | 1.01 (0.13–7.59) | >0.900 | ||
| BMI ≥ 30 | 1.88 (1.33–2.65) | 0.001 | 1.62 (1.13–2.32) | 0.021 |
| Hyperlipidemia | 0.89 (0.62–1.28) | 0.500 | ||
| Neoadjuvant chemotherapy | 0.59 (0.36–0.98) | 0.042 | 0.65 (0.39–1.08) | 0.100 |
| Perioperative Antibiotics | 1.28 (0.94–1.74) | 0.110 | ||
| Closure of defect | 0.70 (0.50–0.98) | 0.040 | 0.71 (0.51–1.00) | 0.053 |
OR odds ratio, BMI body mass index, COPD chronic obstructive pulmonary disease
DISCUSSION
In this study evaluating postoperative infection rates in patients undergoing partial mastectomy, oncoplastic closure of the defect had marginally decreased rates of postoperative breast infections. Although breast surgery is considered a Class 1 clean case, reported rates of surgical site infections are highly variable in the literature, ranging from 2% to as high as 26% [6–9]. This variability is likely a result of the inconsistent definitions of surgical site infections. The CDC has strict criteria defining a surgical site infection and specifically excludes cellulitis as a superficial surgical site infection. It is important to note that our definition of wound infection was not limited to the CDC definition of surgical site infection.
The majority of postoperative breast infections seen in this study were classifiable as cellulitis requiring antibiotics with no evidence of purulent drainage, no evidence of positive culture, and not requiring incisional opening by a clinician [10]. We report that following lumpectomy, 8.4% of patients developed postoperative wound infections, which includes cellulitis. However, only 1.8% had a true surgical site infection as defined by the CDC. Our overall postoperative wound infection rate and true surgical site infection rate closely align with a previous study performed at the Mayo Clinic, which reported a 7.3% infection rate after breast surgery when including cellulitis and a 2.7% true surgical site infection rate when excluding cellulitis per CDC guidelines [14]. We therefore redemonstrate that cellulitis following breast surgery is more common than true SSI, and excluding cellulitis cases leads to decreased reported surgical site infection rates.
The development of postoperative infections is multifactorial. Modifiable risk factors such as smoking history, obesity, and diabetes have previously been associated with increased surgical site infections in breast cancer patients [15]. A recent meta-analysis including over 2700 patients examined breast surgical site infections and found that increased age, hypertension, higher BMI, diabetes, and presence of hematoma or seroma were all associated with higher surgical site infection rates [16]. Similarly, our study demonstrated increased postoperative breast infections in patients age ≥ 60 years and with diabetes, hypertension, and BMI ≥ 30. On multivariable analysis, BMI ≥ 30 remained a significant predictor of wound infection, with CoD bordering on significance. Of note, there was no statistically significant difference in patient age or BMI in those undergoing CoD versus NCoD. Interestingly, there appeared to be a slightly larger proportion of patients with diabetes in the CoD cohort (8.5% vs 6.1%). Furthermore, perioperative antibiotic use was not associated with development of a wound infection; however, the CoD cohort had a higher rate of perioperative antibiotic use. This may be a result of the CoD group also receiving a higher rate of neoadjuvant chemotherapy or being diabetic. Our data suggest that despite these risk factors, closure of the lumpectomy defect may reduce postoperative breast infection rates.
It is believed that closure of a partial mastectomy defect by glandular displacement may decrease rates or the size of postoperative seroma development, one of the most common sequalae of breast surgery. Therefore, reduction in seroma rates with lumpectomy defect closure may explain the reduction in postoperative infections [17]. A study from Cambridge University (Cambridge, United Kingdom) by Mukesh et al. evaluated postoperative infection rates after breast cancer excision by reviewing evidence of a seroma on axial computed tomography images at the time of radiotherapy planning. Of the 648 included patients, they reported the overall rate of postoperative infection was 19.7% and that postoperative infection was more common in patients with seromas (26% vs 16%, p = 0.004) [5]. Similar studies in mastectomy patients, including those undergoing immediate reconstruction, have shown that seroma formation after mastectomy is associated with increased postoperative infections, and that closing the dead space following a mastectomy reduces the rate of seroma formation [18, 19]. These findings, along with the current findings in this study, suggest that oncoplastic closure of the dead space leads to decreased seroma formation, and thus decreased surgical site infections following breast surgery.
Additionally, a study from the University of Florida College of Medicine (Gainesville, FL) by Indelicato et al. demonstrated similar findings when examining the incidence of postoperative infection based on lumpectomy closure technique. This study included 580 patients undergoing breast-conserving surgery for early-stage breast cancer and reported an overall rate of infection of 7.7%. Their results demonstrated that postoperative infection occurred less frequently in those with full-thickness closure of their lumpectomy site as compared to those with superficial closure (5.7% vs 11.7%, p = 0.009) [7]. This study further supports that closure of the defect may be protective against postoperative seroma formation and infection.
Strengths and limitations
The limitations of our study include its retrospective design and therefore the possibility that it underestimates postoperative wound infection rates. There was also potential for selection bias, as the decision for closure of the partial mastectomy defect was left to the discretion of the surgeon. Although it is suspected that the decreased postoperative infection rates may be related to decreased incidence or size of seroma development, seroma characteristics were not reported in this study.
Conclusions
Our study suggests that closure of the partial mastectomy defect by glandular displacement and level 1 oncoplastic techniques may result in lower rates of postoperative breast infections, including cellulitis and superficial surgical site infections. BMI was the major predictor of post-lumpectomy breast infection. While age, diabetes, and hypertension were significant on univariate analysis, they were not significant on multivariable analysis. Closure of the lumpectomy defect appears to remain protective against postoperative infection. These results support the continued use of oncoplastic closure in breast-conserving surgery and encourage further studies evaluating postoperative breast infection rates.
Synopsis:
Here we find that closure of lumpectomy defects resulted in marginally significant lower rates of postoperative breast infections. We conclude that BMI ≥ 30 was a significant predictor of increased postoperative breast infections.
Acknowledgments and Funding Information:
The preparation of this study was supported in part by NIH/NCI Cancer Center Support Grant P30 CA008748 to Memorial Sloan Kettering Cancer Center. The funding source had no role in the collection, analysis, and interpretation of data; in the writing of the report; and in the decision to submit the article for publication. This study was presented in poster format at the 25th Annual Meeting of the American Society of Breast Surgeons, April 10–14, 2024, in Orlando, FL. Fifth author Dr. Monica Morrow reports receipt of speaking honoraria from Merck; all other authors have no conflicts of interest to disclose. All procedures performed in studies involving human participants were in accordance with the ethical standards of our Institutional Review Board. This article does not contain any studies with animals performed by any of the authors, has not been published before, is not under consideration for publication anywhere else, and has been approved for publication by all co-authors.
Abbreviations and Acronyms
- CDC
Centers for Disease Control and Prevention
- CoD
closure of their partial mastectomy defect
- NCoD
without closure of partial mastectomy defect
- UVA
univariate
- MVA
multivariable
- DCIS
ductal carcinoma in situ
- HR+
hormone receptor positive
- HER2
human epidermal growth factor receptor 2
- OR
odds ratio
Footnotes
Prior Presentation: This study was presented in poster format at the 25th Annual Meeting of the American Society of Breast Surgeons, April 10–14, 2024, Orlando, FL.
Data Availability:
The data used in this study are available from the corresponding author upon reasonable request.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The data used in this study are available from the corresponding author upon reasonable request.