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Journal of Hospital Infection 79 (2011) 328e332

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Perioperative variables associated with surgical site infection in breast cancer surgery F.A. Angaritaa, y, S.A. Acunaa, *, y, L. Torregrosaa, b, M. Tawila, b, J. Escallonc, Á. Ruízd a

Department of Surgery, Hospital Universitario San Ignacio, Pontificia Universidad Javeriana, Bogotá, Colombia Breast and Soft Tissue Clinic, Centro Javeriano de Oncología, Bogotá, Colombia c Department of Surgery, Mount Sinai Hospital, Toronto, Ontario, Canada d Department of Clinical Epidemiology and Biostatistics, Pontificia Universidad Javeriana, Bogotá, Colombia b

a r t i c l e i n f o

s u m m a r y

Article history: Received 9 February 2011 Accepted 2 August 2011

by J.A. Child Available online xxx

Despite the fact that breast operations are usually categorized as clean procedures, higher surgical site infection (SSI) rates are reported. This study aimed to determine the perioperative variables related to SSI in breast cancer patients. Medical records of breast cancer patients undergoing surgery between January 2005 and August 2007 at a university based hospital were reviewed. Preoperative, intraoperative, and postoperative clinical data from 199 patients were extracted and analysed. Overall, the SSI rate was 19.1% (38 cases). SSI was associated with a high body mass index (P ¼ 0.001), history of diabetes mellitus (P < 0.0001), smoking (P < 0.0001), or active skin disorders (P < 0.0001). Other SSI-related variables included a tumour at an advanced clinical stage (P ¼ 0.003) and neoadjuvant therapy (P ¼ 0.003). Breastconserving operations were less frequently associated with SSI than were radical procedures (mastectomy alone and mastectomy followed by immediate reconstruction) (P ¼ 0.0001). Ó 2011 The Healthcare Infection Society. Published by Elsevier Ltd. All rights reserved.

Keywords: Breast cancer Breast surgery Surgical site infection

Introduction According to the wound classification of the Centers for Disease Control and Prevention (CDC), surgical operations on the breast are considered to be clean procedures, with a projected surgical site infection (SSI) rate of <1.5%.1 In the past, mastectomy SSI rates were reported to be 1.7e2.2%.2 Nonetheless, current published data from single centre studies are higher (1e30%).3e6 SSIs are a frequent source of postoperative morbidity not just limited to prolonged hospital stay and extra costs, but also a cause to further delay adjuvant treatment, predispose additional interventions such as debridement or abscess draining, and generate poor aesthetic results and psychological trauma.7e9 Currently available information on the risk factors for SSI in breast surgery is based primarily on a series of studies that included a large proportion of patients undergoing breast-conserving surgery (BCS).10e15 Additionally, as mastectomy rates are rising, it is important to evaluate what variables are related to this type of * Corresponding author. Address: Division of Experimental Therapeutics, Toronto General Research Institute, Room 4-425, 67 College Street, Toronto, Ontario, Canada M5G 2M1. Tel.: þ1 416 340 4800x3083; fax: þ1 416 340 3453.

E-mail address: sacuna@uhnresearch.ca (S.A. Acuna). y The first two authors contributed equally to this work.

hospital-acquired infection in a setting where locally advanced cancer is more common. The Centro Javeriano de Oncología (CJO) in Bogotá, Colombia is a national multidisciplinary cancer referral centre affiliated to Hospital Universitario San Ignacio (HUSI), a 300bed private teaching hospital. A previous study reported that 42.3% of our newly diagnosed patients had locally advanced carcinoma of the breast; accordingly these would require radical surgery after adjuvant treatment.16 Since our centre performs a significant number of mastectomies, we aimed to determine which perioperative factors may be associated with a higher probability of SSI in breast cancer surgery.

Methods Study population Procedures eligible for inclusion in this study included mastectomies and BCS performed between January 2005 and August 2007.

Cases of immediate breast reconstruction (IBR) at the time of the primary breast surgery were recorded. Surgical operations involving dirty wounds were excluded as these were considered to be already infected and were specifically related to patients requiring emergency mastectomy for sepsis control. Patients whose final histological

0195-6701/$ e see front matter Ó 2011 The Healthcare Infection Society. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.jhin.2011.08.006

F.A. Angarita et al. / Journal of Hospital Infection 79 (2011) 328e332

report ruled out malignancy were also excluded because they were not actually breast cancer cases.

Antibiotic prophylaxis, surgery, and postoperative wound care Intravenous antibiotic prophylaxis was administered to all patients at least 45 min before the incision. Doses were adjusted for weight and repeated if the length of the procedure exceeded 2 h.

Preoperative and intraoperative preparation (e.g. hand/forearm antisepsis, cleaning and disinfection of surfaces, sterilization of surgical instruments, surgical attire, and skin preparation) were in line with CDC recommendations for SSI prevention.17 Primary oncologic breast operations were performed by one breast surgeon (L.T. or M.T.) and residents. Axillary surgical procedures such as sentinel lymph node biopsy (SLNB) and axillary lymph node dissection (ALND) were also carried out at the same time. Hair removal was standard for these procedures. IBR was carried out using either implants or autologous tissue.

Before discharge, patients were instructed on how to recognize SSI symptoms, appropriate wound care, and how to take care of portable suction devices. Patients were scheduled for follow-up with their surgeon 1e2 weeks post surgery. During that time, patients were scheduled for periodic visits to the hospital’s wound-care clinic, where a trained nurse examined and changed wound dressings.

Identification of patients with SSI Criteria for breast SSI diagnosis were established in guidelines and based upon CDC criteria.18 Stitch abscesses were not considered infections and therefore did not receive antibiotic treatment. Infections were classified as superficial or deep depending on the involvement of the fascial layer; if both superficial and deep SSIs were noted, it was diagnosed as deep. SSIs were detected either in scheduled postoperative follow-up, conducted in an outpatient setting by both breast surgeons, or in emergency department consultations, carried out by an attending general surgeon and residents. In that case, either breast surgeon was contacted and briefed.

Clinical notes were reviewed up to the first 30 days post surgery; in cases involving IBR, charts were reviewed during the first postoperative year. Note was made of which wound was infected.

Microbiological culture results were generally not available because wound swabs are not a routine procedure at our hospital, although these were done when a patient did not respond to empiric SSI treatment.

Data collection Data concerning SSI-associated variables were collected from medical charts using a standardized data-collection tool in a Microsoft Excel database (Microsoft Corp., Redmond, WA, USA).

Information gathered in the preoperative setting included: age, comorbidities, American Society of Anesthesiologists (ASA) classification, history of breast surgery, and neoadjuvant treatment.

Information on the type of surgical procedure, length of time, and estimated blood loss was extracted from the surgical record.

Histologic diagnosis, weight of tissue removed, and number of nodes excised were verified using data from the final pathology report. Postoperative follow-up data included: whether the patient was hospitalized or discharged, signs and symptoms of SSI, date of diagnosis, and treatment.

Statistical analyses Statistical analysis was performed with Stata 10.0 (StataCorp, College Station, TX, USA). Means, standard deviations, and ranges

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were used for descriptive measures. Associations between SSI and potential risk factors were calculated using Student’s t-test, chisquared test, or Fisher’s exact test when appropriate. Statistical significance was set at P < 0.05. Univariate analysis was applied to potential variables.

Results During this period, 199 breast cancer patients underwent breast surgery (Table I). Mean patient age was 54.8 13.2 years. The prevalence of diabetes mellitus, smoking, and active skin disease was 15.1%, 24.1%, and 8.0%, respectively. Approximately 60.3% of the patients had locally advanced breast cancer (N ¼ 125). Sixty-nine patients underwent neoadjuvant therapy in the following distribution: chemotherapy (76.8%), radiotherapy (11.6%), or both (11.6%); on average patients waited 45.8 10.5 days between the final neoadjuvant session and surgery.

Patients underwent surgery in the following distribution: 40.2% BCS, 51.3% for mastectomy, and 8.5% for mastectomy and IBR. Only 61.3% were hospitalized, primarily comprising patients undergoing radical surgery requiring optimized pain control. On average, patients were hospitalized for 1.6 1.9 days (range: 1e20). One patient was

Table I Study population characteristics Variable

N (%) or N SD

Age (years), average Smokinga Diabetes mellitus Active skin diseaseb Body mass index (kg/m2), average Clinical stage In situ Early Locally advanced Metastatic Neoadjuvant therapy None Chemotherapy Radiotherapy Chemoradiation therapy Preoperative haemoglobin (g/dL) (N ¼ 98)c Preoperative haematocrit (%) (N ¼ 98)c Preoperative serum glucose (mg/dL) (N ¼ 50)c Breast surgery Wire localized lumpectomy Lumpectomy Mastectomy Immediate breast reconstructiond Axillary surgery None Sentinel lymph node biopsy Axillary lymph node dissection Average number of lymph nodes (N ¼ 176) Duration of surgery (min) (N ¼ 199) Estimated intraoperative bleeding (mL) Tumour histology Ductal carcinoma in situ Invasive ductal carcinoma Invasive lobular carcinoma Mix Other

54.8 13.2 48 (24.1) 30 (15.1) 16 (8.0) 27.09 þ 4.59

a

17 (8.5) 60 (30.2) 120 (60.3) 2 (1.0) 130 (65.3) 53 (26.6) 8 (4.0) 8 (4.0) 14.08 4.3 39.9 þ 6.9 106.8 42.3 5 (2.5) 75 (37.7) 102 (51.3) 17 (8.5) 27 (13.6) 49 (24.6) 123 (61.8) 10.4 4.3 92.1 56.2 190.3 92.1 17 (8.5) 158 (79.4) 10 (5.0) 5 (2.5) 9 (4.5)

Defined as current smoking or within the past six months.

Defined as skin diseases that had been diagnosed and were currently being treated. None of the lesions involved the breast or axilla. c Data not available for every patient because these blood tests are not routinely done before surgery. Tests were done during preoperative clinic visit, one week before the surgical procedure, or in the hospital prior to surgery. Normal ranges: haemoglobin: 11e18 g/dL, haematocrit: 32e53%, and serum glucose: 65e110 mg/dL. d Breast reconstructions were distributed as follows: 10 latissimus dorsi flaps with saline implant and seven transverse rectus abdominis myocutaneous flaps. b

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hospitalized for 20 days due to postoperative complications secondary to cardiopulmonary disease. Patients with IBR were more likely to be hospitalized for more than one day (mean: 2.5 0.9 days; range: 1e4).

Thirty-eight patients had SSI within the first 30 days after surgery, generating a global SSI rate of 19.1%. All SSIs occurred in the breast surgical site (incisional primary SSI). The mean duration from surgery to diagnosis of surgical site infection was 16.6 6.5 days (range: 6e29). SSI infection rates stratified by breast procedure are summarized in Figure 1.

One patient (0.5%) was diagnosed during her original surgical admission, three patients (1.5%) were diagnosed at readmission, and the remaining 34 were diagnosed as outpatients. Thirty-five patients (92.1%) had superficial SSIs that were treated with wound irrigation, dressing changes, and oral antibiotics. Three patients were diagnosed with deep SSIs in which case they were readmitted for surgical debridement and aggressive intravenous antibiotic therapy. Two cases involved patients with IBR with a latissimus dorsi flap and saline implant, requiring removal of the latter. The other patient was a case of bilateral necrotizing fasciitis of the breast after unilateral BCS, which we previously reported.19 No patients died as a result of infection.

The list of selected results for the univariate analysis is shown in Table II. Discussion SSI was diagnosed in 19.1% of our study population. Although the observed SSI incidence was higher than what is typically expected for clean procedures, it was within the range of what is reported by different breast cancer surgery groups worldwide (4e41%).2,4e6,20e26 This wide range of results is secondary to the following study characteristics: type of procedures (cosmetic and non-cosmetic), SSI definition, population, and the length of follow-up time. The manner in which cases are collected also determines the reported infection rate because studies that rely on self-reporting without providing post-hospital discharge surveillance systems most likely underestimate true infection rates.27 A prospective study showed much higher SSI rates after axillary dissection than the w2% rate normally reported for this procedure.28 The type of surgical procedure determines the SSI rate; lower rates are reported to occur following BCS, while radical surgery with or without reconstructive surgery is more likely to be associated with

120 P = 0.0001 No. of procedures

100 80 60 40 20 0

BCS

Mastectomy Mastectomy + IBR Surgical procedure

Figure 1. Surgical site infection (SSI) rates stratified by surgical procedure. Grey bars: uninfected; black bars: surgical site infection. Breast-conserving surgeries (BCS) had the lowest SSI rate (3.8%); both mastectomy alone and mastectomy and immediate breast reconstruction (IBR) were more likely to be associated with SSI (SSI rate 29.4% and 29.4%, respectively) (P ¼ 0.0001).

Table II Comparison of variables between surgical site breast infection and uninfected patients Uninfected wounds (N ¼ 161)

Variable

Surgical site infection (N ¼ 38)

Age (years)a Body mass index (kg/m2) <25 25e30 >30 Diabetes mellitus ASA score I II III Current smoking or within the past 6 months Active skin disorder prior to surgery Neoadjuvant therapy Previous breast surgery in the same breast, within the last year Type of surgery Breast conserving Radical Histology type In situ Invasive Clinical stage In situ Early Locally advanced Metastatic Mean duration of surgery (min)a Estimated mean blood loss during surgery (mL)a Mean incision size (cm)a Weight of tissue removed (g)a Axillary procedure None Sentinel lymph node biopsy Axillary lymph node dissection Drain in situ

57.7 10.9

54.1 13.6

4 (10.5%) 19 (50.0%) 15 (39.5%) 21 (55.3%)

62 (38.5%) 70 (43.5%) 29 (18.0%) 9 (5.6%)

4 (10.5%) 11 (28.9%) 23 (60.5%) 32 (84.2%)

51 88 22 16

(31.7%) (54.7%) (13.7%) (9.9%)

P-value

NS 0.001

<0.0001 <0.0001

<0.0001

12 (31.6%)

2 (1.2%)

<0.0001

21 (55.3%) 6 (15.8%)

48 (29.8%) 26 (16.1%)

0.003 NS

3 (7.9%) 35 (92.1%)

77 (47.8%) 84 (52.2%)

<0.0001

0.05 0 38 (100.0%)

17 (10.6%) 144 (89.4%)

0 6 (15.8%) 32 (84.2%) 0 101.3 51.9

18 (11.2%) 56 (34.8%) 84 (52.2%) 3 (1.9%) 89.9 57.1

208.8 103.2

185.9 89.1

NS

11.5 3.8 470.9 401.1

10.3 4.3 390.8 317.2

NS NS NS

9 (23.7%) 2 (5.3%) 27 (71.0%) 27 (71.1%)

25 40 96 94

(15.5%) (24.8%) (59.6%) (58.4%)

0.003

NS

NS

ASA, American Society of Anesthesiologists; NS, non-significant. a Mean SD.

SSI.4,11,13,14,23,28e36 The current study also found a tendency for radical surgery to be significantly more associated with infection (29.4% vs 3.8%, P ¼ 0.0001). The more extensive surgical resection needed for advanced tumours probably accounts for the association between radical breast surgery and wound infection.20 Prolonged breast surgery increases the infection rate, but high volumes of estimated blood loss during breast operation is not a risk factor for SSI.37,38 We found no direct association between duration of surgery, blood loss, incision size, and amount of tissue excised with SSI. Breast cancer is an important variable associated with SSI. Infection rates are higher in patients with breast cancer when compared to non-cancer patients who undergo similarly extensive operations (e.g. breast reduction surgery).38 SSI in patients with implant-based reconstruction is frequently reported. Women who undergo oncological surgery and IBR have an infection rate of up to 53%, whereas non-cancer patients undergoing the same reconstructive procedure average an SSI rate of 2.5%.39 Suction drainage through drains in situ reduces the incidence of seroma. At our centre, women who undergo radical breast cancer surgery and/or axillary node dissection have routinely been discharged one day after surgery with a J-VACÒ drain in situ in the mastectomy and axilla cavity. Twenty-seven patients (13.6%) with

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drains in situ developed SSI, a rate close to the 17e33% incidence reported in other studies.20,22 Our data showed that having drains in situ was not related to SSI. In the literature, there are conflicting reports on this point, and other individual studies do show a statistical correlation whereas a systematic review of the literature reported no direct association.40 In 83% of microbiologically confirmed breast infection cases, SSI is reported to be caused by the same bacteria previously isolated from the drainage fluid and that bacterial colonization of the drain was independently associated with a higher SSI incidence.22 This phenomenon is due to a combination of disrupted lymphatic drainage and a prolonged length of time of drains in the cavity.20 Typically in patients with prolonged drainage in situ, infections may occur due to contaminations of drainage tube opening and improper or untimely dressing change. The total duration of drains in situ in our cohort was unavailable because they were usually removed in the wound clinic and this information was not registered.

Radiotherapy affects wound healing because it increases fibrosis, decreases vascularity, and impairs leucocyte function, explaining why 25e41% of patients exposed to preoperative irradiation develop SSI.23,24 In our cohort, neoadjuvant was significantly associated with SSI (55.3% vs 29.8%, P ¼ 0.003) probably owing to the radiotherapy component, as neoadjuvant chemotherapy without radiation therapy does not increase the risk of SSI.4 Although experimental studies performed in animals have shown decreased wound strength after the administration of pre- or postoperative chemotherapy, clinical studies fail to show similar results.4,41 Time elapsed between chemotherapy and surgery seems to have no significant impact on surgical outcomes.42 Additionally, adjuvant chemotherapy may be delayed up to 10 days as a result of SSI.43 In this cohort, mastectomy alone and when followed by IBR had the highest SSI rates (29.4% and 29.4%, respectively) when compared to BCS (3.75%). The morbidity associated with this technique ranges from 15 to 52%, yet the individual effect of IBR is unclear.44,45 In another study,46 where the SSI rate was 5.9%, the only statistically significant predictor of SSI was to have received adjuvant radiation therapy. Neoadjuvant chemotherapy did not increase the risk of major surgical complications following IBR.47 The concern with reconstructive patients is whether or not the initiation of chemotherapy will be delayed. Mortenson et al. found an increased incidence of wound complications in patients who underwent IBR compared with non-reconstructed patients (8.3% vs 22.3%, P ¼ 0.02), with no delay in the initiation of adjuvant therapy.48 The aim of this study was to determine what patient and surgical characteristics were associated with SSI developing in breast cancer patients. Variables related to SSI were those indicative of locally advanced tumours, which generally required neoadjuvant therapy and radical procedures, as well as patients with significant comorbidities. Indeed there are other perioperative variables that were not included in this study (e.g. oxygenation level during surgery and number of residents operating) that may have had an impact on our SSI rate. Overall, our study supports the fact that SSI post-breast cancer surgery is more common than expected, and breast surgeons should keep this, and the patient characteristics identified in this study, in mind.

While there are sufficient data to suggest that targeted antibiotic prophylaxis reduces SSIs in those undergoing nonreconstructive breast cancer surgeries, there is little published on SSI prevention practice outside the operating room.49 This has motivated us to work toward creating an effective breast surgery SSI prevention plan at our hospital. In the outpatient clinic potential interventions include a formal surveillance tracking system, stricter control of comorbidities, promotion of meticulous hand hygiene, and standardized wound control in order to improve the quality of care delivered to patients undergoing breast cancer surgery.

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Conflict of interest statement None declared.

Funding source This project was funded by the Breast and Soft Tissue Clinic, Pontificia Universidad Javeriana.

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