BREAST SURGERY
Antibiotic Prophylaxis and Resistance in Surgical Site Infection After Immediate Tissue Expander Reconstruction of the Breast Meghan C. McCullough, MD, Carrie K. Chu, MD, MS, Claire S. Duggal, MD, Albert Losken, MD, and Grant W. Carlson, FACS, MD Background: A recent survey of plastic surgeons showed that the majority prescribed prophylactic antibiotics after hospital discharge for breast reconstruction. There is no clinical evidence that this practice reduces surgical site infection (SSI) after immediate tissue expander breast reconstruction. Furthermore, multiple studies have suggested that current antibiotic choices may not be appropriately covering the causative organisms of SSI. Methods: An institutional breast reconstruction database from January 2005 to December 2011 was queried to identify patients undergoing immediate tissue expander reconstruction of the breast. The bacteriology of the infection, prophylactic and empiric antibiotic use, and antibiotic sensitivities were analyzed. Results: In 557 cases of immediate tissue expander breast reconstruction performed in 378 patients, SSIs were diagnosed in 50 (9.0%) cases. Two hundred patients were given oral antibiotics at discharge; 178 did not receive antibiotics. Surgical site infection developed in 12.0% of patients given oral antibiotics and in 13.5% of those not receiving antibiotics (P = 0.67). Wound culture data were obtained in 34 SSIs. Twenty-nine had positive cultures. The most common offending organisms were methicillin-sensitive (11) and methicillin-resistant (6) Staphylococcus aureus. Despite increased use of postoperative prophylaxis over the years, SSI incidence remained unchanged. However, trends toward increased resistance of SSI organisms to the preoperative and postoperative prophylaxis agents were observed. When firstgeneration cephalosporins were used as prophylaxis, SSI organisms showed resistance rates of 20.5% (preoperative cefazolin) and 54.5% (postoperative cephalexin). Conclusions: Administration of extended prophylactic antibiotics does not reduce overall risk of SSI after expander-based breast reconstruction but may inf luence antibiotic resistance patterns when infections occur. The organisms most commonly responsible for SSI are often resistant to cefazolin. Key Words: breast, reconstruction, expander, implant, mastectomy, infection, surgical site infection, antibiotics, perioperative, preoperative, postoperative, surgery, cancer, oncology (Ann Plast Surg 2014;73: 00Y00)
A
ccording to the Centers for Disease Control and the Surgical Care Improvement Project (SCIP), breast surgery is considered a clean surgical case. The current guidelines recommend a maximum of 24 hours of perioperative antibiotics.1 Patients undergoing breast surgery have been documented to have infection rates much higher than the typical 1% to 2% in clean elective surgeries, ranging from 3% to 30%.2Y7 Immediate breast reconstruction especially with
Received January 12, 2014, and accepted for publication, after revision, April 28, 2014. From the Division of Plastic Surgery, Emory University School of Medicine, Atlanta,GA. Conf licts of interest and sources of funding: none declared. Reprints: Grant W. Carlson, MD, FACS, Winship Cancer Institute, 1365C Clifton Rd, Atlanta, GA 30322. E-mail: [email protected]. Copyright * 2014 by Lippincott Williams & Wilkins ISSN: 0148-7043/14/7302Y0000 DOI: 10.1097/SAP.0000000000000275
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implants has been found to have an even higher rate of infection, up to 50%.8Y11 Implant-based breast reconstruction is the most common reconstructive technique after mastectomy for breast cancer. It is advantageous, compared with autologous reconstruction, because of the decreased morbidity, shorter operative time, and quicker recovery. However, surgical site infection (SSI) is an important complication of this technique. It is a potential cause of reconstruction failure and can have a significant impact on both patient outcomes and hospital costs. Preventing SSI in these patients is critical not only for cosmesis but also for reducing delays in adjuvant therapy. The SCIP established guidelines for antibiotic prophylaxis to reduce SSI, which include administering appropriate antibiotics within 60 minutes of incision and discontinuing them within 24 hours of surgery.1,12 Preoperative prophylaxis with a single dose of an intravenously administered antibiotic with antistaphylococcal and antistreptococcal activity has been the standard of care.1,12 The applicability of these generalized recommendations to breast reconstruction is questionable. Actual antibiotic practices are largely based on training and personal experience instead of evidence-based medicine. In a recent survey of American Society of Plastic Surgeons members, approximately 72% of plastic surgeons prescribed postoperative antibiotics for at least 1 week or until the drains were removed.9 The lack of evidence-based guidelines specific to this patient population has led to indiscriminate use of prophylactic antibiotics without clear understanding of either the bacteriology of these infections or the susceptibility of the causative bacteria to commonly used antibiotics. Inappropriate antibiotic selection and prolonged use have negative consequences including increased costs, systemic adverse effects, and growing drug resistance.12 In this study, we sought to examine the incidence and bacteriology of SSI relative to patterns of postoperative antibiotic prophylaxis after expander-based breast reconstruction.
METHODS Conduct of this study was approved by the institutional review board with waiver of the requirement for written consent. A retrospective cohort analysis was performed using information from a prospectively maintained institutional database of patients who underwent immediate tissue expander breast reconstruction between January 2005 and December 2011 at Emory University Hospitals. Two surgeons performed most of the cases. Expanders were placed in a submuscular position usually with acellular dermal matrix (ADM) used as a lower pole sling. Closed suction drains were used in all reconstructions and were removed when the drain outputs were less than 30 mL every 24 hours. All patients received a single intravenous dose of antibiotics within 60 minutes before incision; this dose will be referred to as ‘‘preoperative antibiotics’’ hereafter. At discharge, postoperative prophylactic oral antibiotics (‘‘postoperative antibiotics’’) were prescribed at the discretion of the operating surgeon based on routine personal practice. No routine bias toward antibiotic use in cases of ADM existed. www.annalsplasticsurgery.com
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TABLE 1. Patient Characteristics by Postoperative SSI No All Patients Infection (n (n = 378) = 330) Age, mean, y BMI, mean, kg/m2 Obesity (BMI, Q30 kg/m2) Smoking Cancer staging* Stage 0 Stage I Stage II Stage III Stage IV Recurrent Benign Axillary surgery† None SLN biopsy Axillary lymph node dissection Radiation Chemotherapy ADM use Bilateral Postoperative antibiotic prophylaxis
Infected Reconstructions (n = 48)
P
51.4 26.2 82 (21.7%)
51.4 26.1 69 (20.9%)
51.2 27.3 13 (27.1%)
0.89 0.28 0.33
32 (8.5%)
24 (7.3%)
8 (16.7%)
0.03 0.86
81 (21.5%) 97 (25.8%) 112 (29.8%) 68 (18.1%) 6 (1.6%) 7 (1.9%) 5 (1.3%)
72 (22.0%) 84 (25.6%) 98 (29.9%) 57 (17.4%) 6 (1.8%) 6 (1.8%) 5 (1.5%)
9 (18.8%) 13 (27.1%) 14 (29.2%) 11 (22.9%) 0 (0%) 1 (2.1%) 0 (0%)
76 (20.3%) 71 (21.7%) 195 (52.0%) 169 (51.7%) 104 (27.7%) 87 (26.6%)
5 (10.4%) 26 (54.2%) 17 (35.4%)
118 (31.2%) 190 (50.3%) 300 (79.4%) 179 (47.4%) 200 (52.9%)
16 23 37 23 24
0.15
102 (30.9%) 167 (50.6%) 263 (79.7%) 156 (47.3%) 176 (53.3%)
(33.3%) (47.9%) (77.1%) (47.9%) (50.0%)
0.74 0.67 0.68 0.93 0.67
Bilateral cases given cephalexin and clindamycin, both had bilateral reconstruction, both received radiation to 1 side, and both received adjuvant chemotherapy. *One case missing cancer staging information. †Three cases missing axillary treatment. BMI indicates body mass index.
The primary end point of SSI was defined in accordance with Centers for Disease Control guidelines as purulent drainage, positive culture, peri-incisional erythema, incision deliberately opened by surgeon, and physician diagnosis of infection, such as cellulitis, for which antibiotics were prescribed. Both the administration of oral antibiotics without admission to the hospital and admission for either intravenous antibiotics or surgical intervention were considered in this study. Patients with wound dehiscence, skin f lap necrosis, implant exposure, or any other causes of expander failure were excluded, as these patients did not fit the definition of infection. For all patients who acquired infection, the timing of infection was analyzed, as were salvage measures, both antibiotic and operative. Deep wound cultures were obtained in the outpatient clinic and in the operating room. Culture sensitivities were performed where relevant. For those patients who went on to acquire infection, ‘‘empiric antibiotics’’ used to treat infection were also recorded. Potential predictors of infection such as administration of radiation and/or chemotherapy, patient age, smoking status, ADM placement, axillary dissection, and body mass index were assessed as possible confounding factors. Statistical analysis was performed using JMP v10 (Cary, NC). Fisher exact test was used for categorical variables and t tests for continuous independent variables. > was set at 0.05.
RESULTS Five hundred fifty-seven immediate tissue expander breast reconstructions were performed in 378 patients at Emory University 2
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Hospitals between January 2005 and December 2011. The mean patient age was 51.4 years (range, 27Y84 years) and the mean body mass index was 26.2 kg/m2. Additional patient and disease-related data are summarized in Table 1. Surgical site infection developed in 50 (9.0%) expander reconstructions, or 48 (12.7%) patients. There were 2 patients with bilateral infection. The median time to diagnosis of SSI was 29 days. Preoperative antibiotics were used in all cases of immediate expander reconstruction. NonYpenicillin allergic patients all received cefazolin, whereas penicillin-allergic patients received either clindamycin or vancomycin. Upon discharge, 200 (52.9%) patients were given a prescription for oral postoperative antibiotics. One hundred seventy-eight (47.1%) patients did not receive postoperative antibiotics. No significant differences were identified in demographics, comorbidities, and treatment variables between the 2 groups with and without postoperative antibiotics (Table 2). Risks of SSI were similar between patients who received postoperative antibiotics (12%) and those who did not (13.5%) (P = 0.67). Postoperative antibiotic agents and subsequent infections are detailed in Table 3. The use of postoperative antibiotics increased over the course of the study as illustrated in Figure 1. Despite this increased antibiotic use, however, incidence of infections did not decrease. In those cases that later developed infection after primary expander placement, cefazolin was used as the perioperative antibiotic in 43 (87.7%) cases, clindamycin in 6 (10.2%) cases, and vancomycin in 1 (2.0%) case. Wound culture data were submitted in 34 (68%) of the infected reconstructions. Cultures were obtained in the clinic in 7 cases and in the operating room in 27. Twenty-nine (85.3%) had growth of microorganism s including 5 (14.7%) with multiple organisms. The most common organisms cultured were methicillinsensitive Staphylococcus aureus (MSSA) (n = 11), followed by methicillin-resistant S. aureus (MRSA) (n = 6), and Staphylococcus epidermidis (n = 3) (Table 4). Staphylococcal species were responsible for 72.4% of positive cultures. TABLE 2. Patient Characteristics by Administration of Postoperative Antibiotics
Age, mean, y BMI, mean, kg/m2 Obesity (BMI, Q30 kg/m2) Smoking SSI Explantation Axillary surgery† None SLN biopsy Axillary lymph node dissection Radiation Chemotherapy ADM use Bilateral SSI
No Postoperative Antibiotics (n = 178)
Postoperative Antibiotics (n = 200)
P
50.8 26.2 38 (21.3%)
52.0 26.3 44 (22.0%)
0.31 0.87 0.88
13 (7.3%) 24 (13.5%) 14 (58.3%)
19 (9.5%) 24 (12.0%)* 14 (58.3%)
0.44 0.67 1.00 0.57
40 (22.6%) 89 (50.3%) 48 (27.1%)
36 (18.2%) 106 (53.5%) 56 (28.3%)
52 (29.2%) 92 (51.7%) 136 (76.4%) 85 (47.8%) 24 (13.5%)
66 (33.3%) 98 (49.0%) 164 (82.0%) 94 (47.0%) 24 (12.0%)
0.43 0.60 0.18 0.88 0.67
Bilateral cases given cephalexin and clindamycin, both had bilateral reconstruction, both received radiation to 1 side, and both received adjuvant chemotherapy. *Bilateral 2 patients. †Three cases missing axillary treatment. BMI indicates body mass index.
* 2014 Lippincott Williams & Wilkins
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TABLE 3. Postoperative Antibiotics Use and Subsequent Infection Discharge Antibiotic
Total (%)
Infection (%)
2 5 5 1 1 1 1 4 18 155 7 200 178 6 384
1 (50) 1 (20) 0 1 (100) 0 0 0 2 (50) 4 (22.2) 17 (11.0) 0 26 (13.0) 24 (13.5) 0 50 (13.0)*
Amoxicillin/clavulanate Azithromycin Trimethoprim/sulfamethoxazole Clarithromycin Cefdinir Dicloxacillin Doxycycline Ciprofloxacin Clindamycin Cephalexin Levafloxacin Discharge antibiotic total None Unknown Total *Bilateral infection, 2.
Sixteen (32%) cases of SSI resolved with antibiotics alone (oral antibiotics 12, intravenous antibiotics 4). Thirty-four (68%) infected expanders required surgical intervention. Twenty-nine (58%) expanders required explantation. Surgical salvage, consisting of washout and expander replacement, was attempted in 11 cases. Five (45.5%) cases successfully resolved the infection. Successful reconstruction was ultimately achieved in 10 of the 29 cases (delayed expander replacement 3, autologous reconstruction 7) after expander removal.
Antibiotics and Tissue Expanders
Antibiotic sensitivities were performed in the positive infected wound cultures. Retrospective comparison of the organism’s susceptibility profile with the preoperative intravenous antibiotic showed resistance to the preoperative antibiotic in 15 (51.7%) of 29 cases. The percent resistance to the preoperative antibiotic increased through the years of this study (2005, 0/1; 2006, none; 2007, 1/3; 2008, 1/4; 2009, 7/11; 2010, 3/4; and 2011, 3/6) (Fig. 2). Resistance to the postoperative prophylactic antibiotic, when administered, was observed in 8 (57.1%) of 14 cases. The proportion of infective organisms resistant to the postoperative antibiotic also increased over time (2005, none; 2006, none; 2007, 0/2; 2008, none; 2009, 4/7; 2010, 1/1; and 2011, 3/4). First-generation cephalosporins were the most commonly used agents in both the preoperative (cefazolin) and postoperative (cephalexin) prophylaxis settings. Figure 3 demonstrates the rates of SSI organism resistance to a first-generation cephalosporin for the various timings of antibiotic administration.
DISCUSSION Infectious complications of expander-based breast reconstruction are a significant cause of patient morbidity and increased hospital costs. Despite recognition of the importance of minimizing SSI after breast reconstruction, there is still no consensus regarding the utility or optimal regimen of prophylactic antibiotics. In this study, microbiological data were used to analyze the impact of extended prophylactic antibiotic use on the resistance patterns of the causative organisms of SSI. Current guidelines in antibiotic prophylaxis suggest administration of a single dose of perioperative antibiotic with cessation of further dosing beyond 24 hours after surgery. Selected agents are typically effective against gram-positive bacteria.1,12 In practice, the widespread use of extended postoperative antibiotics in expanderbased reconstruction is controversial. Phillips et al13 reviewed antibiotic usage and infection in 81 studies involving all forms of breast reconstruction. The authors found no benefit in patients who received
FIGURE 1. Discharge antibiotic use and infection rate by year. * 2014 Lippincott Williams & Wilkins
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TABLE 4. Microbiology of SSI Bacteria
Infections, n (%)
MSSA MRSA S. epidermidis Staphylococcus lugdunensis >-Hemolytic Streptococcus Corynebacterium Mycobacterium fortuitum Enterococcus Stenotrophomonas maltophilia Proteus mirabilis Serratia Pseudomonas Multiple No growth
11 6 3 1 1 1 3 2 1 1 3 2 5 5
(27.7) (17.6) (8.8) (2.9) (2.9) (2.9) (8.8) (5.8) (2.9) (2.9) (8.8) (5.4) (14.7) (14.7)
more than 24 hours of prophylactic antibiotics. Conversely, Clayton et al reviewed 250 patients undergoing breast reconstruction to determine the impact of initiating SCIP guidelines on SSI. In multivariate analysis, the authors found that those patients who did not receive postoperative antibiotics were 4.7 times as likely to develop an SSI requiring reoperation.14 Avashia et al15 also found increased rates of infection requiring expander removal (31.6% vs 7.9%) when antibiotics were discontinued after 24 hours as opposed to when they were continued for at least 48 hours. In contrast, our study shows no improvement in infection rates when postoperative antibiotics were used. Despite an increased trend in the use of postoperative antibiotics, the infection rate was unchanged over the course of the study. Moreover, when infections developed, there was a trend of increased resistance to the preoperative and postoperative prophylactic antibiotics over time. The use of antibiotics is not without complications. Other than cost, potential allergic reactions, and associated colitis, it is well documented that unnecessary or prolonged use of antibiotics can result in emergence of resistant organisms such as MRSA and vancomycin-resistant Enterococcus.16 Clayton et al14 found that those patients who did receive postoperative antibiotics, but who went on to develop SSI requiring explantation, were more likely to have gram-positive staphylococcal infections than gram-negative infections. The authors hypothesized that the use of postoperative antibiotics may have prevented gram-negative infections and selected for more resistant staphylococcal strains, but this interpretation is debatable.14 In our own experience, we observed increased resistance patterns at the same time more prophylactic postoperative antibiotics were used. Our finding that most of SSIs were caused by gram-positive organisms is consistent with the literature. Our study found staphylococcal species to be responsible for 61.7% of all cultured infections, and 72.4% of positive cultures. Methicillin-resistant S. aureus specifically accounted for 20.6% of those positive cultures. Clayton et al14 similarly found a high prevalence of MSSA, coagulase-negative Staphylococcus, and MRSA. Baumann et al17 evaluated the bacteriology of 75 tissue expander infections requiring explantation and found a high rate of skin f lora (68% of cases) as the causative organisms. Avashia et al15 in their analysis of expanderbased reconstruction with ADM, found predominantly MSSA, but also MRSA, coagulase-negative Staphylococcus, Enterococcus, Serratia, Pseudomonas, and Mycobacterium in their study sample. In a recent study by Weichman et al18 of device-based reconstructions, the most common organism cultured was S. epidermidis, followed 4
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by S. aureus, although overall they found equivalence in their study between gram-positive and gram-negative infections. In keeping with the emergence of more gram-negative infections, Mukhtar et al19 reviewed SSI after nonreconstructive breast surgery. They found 28.1% of their cultures to be S. aureus but 18.8% to be Escherichia coli. Although certain microbial trends have emerged among these multiple studies, the diversity of the bacteriologic findings suggests unique microbial profiles among individual institutions. Our study found substantial resistant rates of 20% to 54% to first-generation cephalosporins used in preoperative and postoperative prophylaxis (Fig. 3). Baumann et al17 reported a greater than 65% resistance to cefazolin in 75 positive wound cultures after tissue expander reconstruction. Weichman et al18 evaluated SSI after 43 implant-based breast reconstructions to examine bacterial resistance patterns. Postoperative prophylactic antibiotics were routinely administered. They found a 40% resistance of infecting organisms to cefazolin. Given these repeated findings confirming the poor activity of cefazolin against the causative organisms of SSI in breast reconstruction, multiple authors have suggested alternative antibiotic regimens when SSI develops. Feldman et al20 found a very high incidence of MRSA infections in their review of 31 SSIs and suggested vancomycin as empiric antibiotic therapy. Weichman et al recommend that if patients are amenable to oral antibiotics, f luoroquinolones should be used. If patients are not amenable to oral therapy, they suggest IV therapy be initiated with vancomycin in addition to either imipenem or gentamycin.18 This retrospective review is subject to inherent limitations. Cohorts were nonrandomized with potential selection for treatment with preventive postoperative antibiotics. However, no routine preference for antibiotics based on any patient or technical variables existed; rather, individual surgeon practice usually dictated antibiotic use. Sampling is biased toward more severe infections from which cultures were collected, likely underestimating the incidence of infections that responded to outpatient empiric oral antibiotics. Additionally, not all traditionally associated factors with infection were analyzed; for example, drain data and expander volumes were not evaluated. Multiple surgeons performed operations with technical variation. The small number of culture-positive SSI with relevant susceptibility studies limits definitive conclusion regarding the impact of prophylaxis on bacterial resistance.
FIGURE 2. For cases of SSI, percentage of cultured organisms resistant to the administered preoperative intravenous antibiotic by year. * 2014 Lippincott Williams & Wilkins
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Antibiotics and Tissue Expanders
FIGURE 3. For cases of SSI, susceptibility and resistance patterns of first-generation cephalosporin by timing of administration (‘‘Prophylactic cefazolin’’ was administered within 1 hour before surgical incision, ‘‘Postoperative cephalexin’’ was administered after surgery in preventive fashion, and ‘‘Empiric cefazolin’’ was administered postoperatively when SSI was suspected or diagnosed before availability of culture data).
In conclusion, administration of extended prophylactic antibiotics does not reduce risk of SSI after expander-based breast reconstruction, but may inf luence antibiotic resistance patterns when infections occur. The organisms most commonly responsible for SSI have become often resistant to first-generation cephalosporins. Future directions may include improved preoperative surveillance and tailored antiseptic or antibacterial prophylaxis.
10.
11. 12.
REFERENCES 1. Mangram AJ, Horan TC, Pearson ML, et al. Guideline for prevention of surgical site infection, 1999. Hospital Infection Control Practices Advisory Committee. Infect Control Hosp Epidemiol. 1999;20:250Y278; quiz 279Y80.
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2. Beatty JD, Robinson GV, Zaia JA, et al. A prospective analysis of nosocomial wound infection after mastectomy. Arch Surg. 1983;118:1421Y1424.
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3. Chen J, Gutkin Z, Bawnik J. Postoperative infections in breast surgery. J Hosp Infect. 1991;17:61Y65. 4. D’Amico DF, Parimbelli P, Ruffolo C. Antibiotic prophylaxis in clean surgery: breast surgery and hernia repair. J Chemother. 2001;13:108Y111. 5. Hall JC, Hall JL. Antibiotic prophylaxis for patients undergoing breast surgery. J Hosp Infect. 2000;46:165Y170. 6. Rotstein C, Ferguson R, Cummings KM, et al. Determinants of clean surgical wound infections for breast procedures at an oncology center. Infect Control Hosp Epidemiol. 1992;13:207Y214. 7. Tejirian T, DiFronzo LA, Haigh PI. Antibiotic prophylaxis for preventing wound infection after breast surgery: a systematic review and metaanalysis. J Am Coll Surg. 2006;203:729Y734. 8. Acuna SA, Angarita FA, Escallon J, et al. Determining the use of prophylactic antibiotics in breast cancer surgeries: a survey of practice. BMC Surg. 2012;12:18. 9. Phillips BT, Wang ED, Mirrer J, et al. Current practice among plastic surgeons of antibiotic prophylaxis and closed-suction drains in breast reconstruction:
* 2014 Lippincott Williams & Wilkins
15.
16. 17.
18.
19. 20.
experience, evidence, and implications for postoperative care. Ann Plast Surg. 2011;66:460Y465. Alderman AK, Wilkins EG, Kim HM, et al. Complications in postmastectomy breast reconstruction: two-year results of the Michigan Breast Reconstruction Outcome Study. Plast Reconstr Surg. 2002;109:2265Y2274. Pittet B, Montandon D, Pittet D. Infection in breast implants. Lancet Infect Dis. 2005;5:94Y106. Fry DE. Surgical site infections and the surgical care improvement project (SCIP): evolution of national quality measures. Surg Infect (Larchmt). 2008;9:579Y584. Phillips BT, Bishawi M, Dagum AB, et al. A systematic review of antibiotic use and infection in breast reconstruction: what is the evidence? Plast Reconstr Surg. 2013;131:1Y13. Clayton JL, Bazakas A, Lee CN, et al. Once is not enough: withholding postoperative prophylactic antibiotics in prosthetic breast reconstruction is associated with an increased risk of infection. Plast Reconstr Surg. 2012; 130:495Y502. Avashia YJ, Mohan R, Berhane C, et al. Postoperative antibiotic prophylaxis for implant-based breast reconstruction with acellular dermal matrix. Plast Reconstr Surg. 2013;131:453Y461. Monroe S, Polk R. Antimicrobial use and bacterial resistance. Curr Opin Microbiol. 2000;3:496Y501. Baumann D, Viola G, Selber J. Emerging trends in infectious complications in tissue expander reconstruction: are the causative bacteria evolving? In Proceedings of the 91st Annual Meeting of the American Association of Plastic Surgeons. 2012. San Francisco, CA. Weichman KE, Levine SM, Wilson SC, et al. Antibiotic selection for the treatment of infectious complications of implant-based breast reconstruction. Ann Plast Surg. 2013;71:140Y143. Mukhtar RA, Throckmorton AD, Alvarado MD, et al. Bacteriologic features of surgical site infections following breast surgery. Am J Surg. 2009;198:529Y531. Feldman EM, Kontoyiannis DP, Sharabi SE, et al. Breast implant infections: is cefazolin enough? Plast Reconstr Surg. 2010;126:779Y785.
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5
Antibiotic Prophylaxis and Resistance in Surgical Site Infection After Immediate Tissue Expander Reconstruction of the Breast Meghan C. McCullough, MD, Carrie K. Chu, MD, MS, Claire S. Duggal, MD, Albert Losken, MD, and Grant W. Carlson, FACS, MD Background: A recent survey of plastic surgeons showed that the majority prescribed prophylactic antibiotics after hospital discharge for breast reconstruction. There is no clinical evidence that this practice reduces surgical site infection (SSI) after immediate tissue expander breast reconstruction. Furthermore, multiple studies have suggested that current antibiotic choices may not be appropriately covering the causative organisms of SSI. Methods: An institutional breast reconstruction database from January 2005 to December 2011 was queried to identify patients undergoing immediate tissue expander reconstruction of the breast. The bacteriology of the infection, prophylactic and empiric antibiotic use, and antibiotic sensitivities were analyzed. Results: In 557 cases of immediate tissue expander breast reconstruction performed in 378 patients, SSIs were diagnosed in 50 (9.0%) cases. Two hundred patients were given oral antibiotics at discharge; 178 did not receive antibiotics. Surgical site infection developed in 12.0% of patients given oral antibiotics and in 13.5% of those not receiving antibiotics (P = 0.67). Wound culture data were obtained in 34 SSIs. Twenty-nine had positive cultures. The most common offending organisms were methicillin-sensitive (11) and methicillin-resistant (6) Staphylococcus aureus. Despite increased use of postoperative prophylaxis over the years, SSI incidence remained unchanged. However, trends toward increased resistance of SSI organisms to the preoperative and postoperative prophylaxis agents were observed. When firstgeneration cephalosporins were used as prophylaxis, SSI organisms showed resistance rates of 20.5% (preoperative cefazolin) and 54.5% (postoperative cephalexin). Conclusions: Administration of extended prophylactic antibiotics does not reduce overall risk of SSI after expander-based breast reconstruction but may inf luence antibiotic resistance patterns when infections occur. The organisms most commonly responsible for SSI are often resistant to cefazolin. Key Words: breast, reconstruction, expander, implant, mastectomy, infection, surgical site infection, antibiotics, perioperative, preoperative, postoperative, surgery, cancer, oncology (Ann Plast Surg 2014;73: 00Y00)
A
ccording to the Centers for Disease Control and the Surgical Care Improvement Project (SCIP), breast surgery is considered a clean surgical case. The current guidelines recommend a maximum of 24 hours of perioperative antibiotics.1 Patients undergoing breast surgery have been documented to have infection rates much higher than the typical 1% to 2% in clean elective surgeries, ranging from 3% to 30%.2Y7 Immediate breast reconstruction especially with
Received January 12, 2014, and accepted for publication, after revision, April 28, 2014. From the Division of Plastic Surgery, Emory University School of Medicine, Atlanta,GA. Conf licts of interest and sources of funding: none declared. Reprints: Grant W. Carlson, MD, FACS, Winship Cancer Institute, 1365C Clifton Rd, Atlanta, GA 30322. E-mail: [email protected]. Copyright * 2014 by Lippincott Williams & Wilkins ISSN: 0148-7043/14/7302Y0000 DOI: 10.1097/SAP.0000000000000275
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& Volume 73, Number 2, August 2014
implants has been found to have an even higher rate of infection, up to 50%.8Y11 Implant-based breast reconstruction is the most common reconstructive technique after mastectomy for breast cancer. It is advantageous, compared with autologous reconstruction, because of the decreased morbidity, shorter operative time, and quicker recovery. However, surgical site infection (SSI) is an important complication of this technique. It is a potential cause of reconstruction failure and can have a significant impact on both patient outcomes and hospital costs. Preventing SSI in these patients is critical not only for cosmesis but also for reducing delays in adjuvant therapy. The SCIP established guidelines for antibiotic prophylaxis to reduce SSI, which include administering appropriate antibiotics within 60 minutes of incision and discontinuing them within 24 hours of surgery.1,12 Preoperative prophylaxis with a single dose of an intravenously administered antibiotic with antistaphylococcal and antistreptococcal activity has been the standard of care.1,12 The applicability of these generalized recommendations to breast reconstruction is questionable. Actual antibiotic practices are largely based on training and personal experience instead of evidence-based medicine. In a recent survey of American Society of Plastic Surgeons members, approximately 72% of plastic surgeons prescribed postoperative antibiotics for at least 1 week or until the drains were removed.9 The lack of evidence-based guidelines specific to this patient population has led to indiscriminate use of prophylactic antibiotics without clear understanding of either the bacteriology of these infections or the susceptibility of the causative bacteria to commonly used antibiotics. Inappropriate antibiotic selection and prolonged use have negative consequences including increased costs, systemic adverse effects, and growing drug resistance.12 In this study, we sought to examine the incidence and bacteriology of SSI relative to patterns of postoperative antibiotic prophylaxis after expander-based breast reconstruction.
METHODS Conduct of this study was approved by the institutional review board with waiver of the requirement for written consent. A retrospective cohort analysis was performed using information from a prospectively maintained institutional database of patients who underwent immediate tissue expander breast reconstruction between January 2005 and December 2011 at Emory University Hospitals. Two surgeons performed most of the cases. Expanders were placed in a submuscular position usually with acellular dermal matrix (ADM) used as a lower pole sling. Closed suction drains were used in all reconstructions and were removed when the drain outputs were less than 30 mL every 24 hours. All patients received a single intravenous dose of antibiotics within 60 minutes before incision; this dose will be referred to as ‘‘preoperative antibiotics’’ hereafter. At discharge, postoperative prophylactic oral antibiotics (‘‘postoperative antibiotics’’) were prescribed at the discretion of the operating surgeon based on routine personal practice. No routine bias toward antibiotic use in cases of ADM existed. www.annalsplasticsurgery.com
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
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TABLE 1. Patient Characteristics by Postoperative SSI No All Patients Infection (n (n = 378) = 330) Age, mean, y BMI, mean, kg/m2 Obesity (BMI, Q30 kg/m2) Smoking Cancer staging* Stage 0 Stage I Stage II Stage III Stage IV Recurrent Benign Axillary surgery† None SLN biopsy Axillary lymph node dissection Radiation Chemotherapy ADM use Bilateral Postoperative antibiotic prophylaxis
Infected Reconstructions (n = 48)
P
51.4 26.2 82 (21.7%)
51.4 26.1 69 (20.9%)
51.2 27.3 13 (27.1%)
0.89 0.28 0.33
32 (8.5%)
24 (7.3%)
8 (16.7%)
0.03 0.86
81 (21.5%) 97 (25.8%) 112 (29.8%) 68 (18.1%) 6 (1.6%) 7 (1.9%) 5 (1.3%)
72 (22.0%) 84 (25.6%) 98 (29.9%) 57 (17.4%) 6 (1.8%) 6 (1.8%) 5 (1.5%)
9 (18.8%) 13 (27.1%) 14 (29.2%) 11 (22.9%) 0 (0%) 1 (2.1%) 0 (0%)
76 (20.3%) 71 (21.7%) 195 (52.0%) 169 (51.7%) 104 (27.7%) 87 (26.6%)
5 (10.4%) 26 (54.2%) 17 (35.4%)
118 (31.2%) 190 (50.3%) 300 (79.4%) 179 (47.4%) 200 (52.9%)
16 23 37 23 24
0.15
102 (30.9%) 167 (50.6%) 263 (79.7%) 156 (47.3%) 176 (53.3%)
(33.3%) (47.9%) (77.1%) (47.9%) (50.0%)
0.74 0.67 0.68 0.93 0.67
Bilateral cases given cephalexin and clindamycin, both had bilateral reconstruction, both received radiation to 1 side, and both received adjuvant chemotherapy. *One case missing cancer staging information. †Three cases missing axillary treatment. BMI indicates body mass index.
The primary end point of SSI was defined in accordance with Centers for Disease Control guidelines as purulent drainage, positive culture, peri-incisional erythema, incision deliberately opened by surgeon, and physician diagnosis of infection, such as cellulitis, for which antibiotics were prescribed. Both the administration of oral antibiotics without admission to the hospital and admission for either intravenous antibiotics or surgical intervention were considered in this study. Patients with wound dehiscence, skin f lap necrosis, implant exposure, or any other causes of expander failure were excluded, as these patients did not fit the definition of infection. For all patients who acquired infection, the timing of infection was analyzed, as were salvage measures, both antibiotic and operative. Deep wound cultures were obtained in the outpatient clinic and in the operating room. Culture sensitivities were performed where relevant. For those patients who went on to acquire infection, ‘‘empiric antibiotics’’ used to treat infection were also recorded. Potential predictors of infection such as administration of radiation and/or chemotherapy, patient age, smoking status, ADM placement, axillary dissection, and body mass index were assessed as possible confounding factors. Statistical analysis was performed using JMP v10 (Cary, NC). Fisher exact test was used for categorical variables and t tests for continuous independent variables. > was set at 0.05.
RESULTS Five hundred fifty-seven immediate tissue expander breast reconstructions were performed in 378 patients at Emory University 2
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Hospitals between January 2005 and December 2011. The mean patient age was 51.4 years (range, 27Y84 years) and the mean body mass index was 26.2 kg/m2. Additional patient and disease-related data are summarized in Table 1. Surgical site infection developed in 50 (9.0%) expander reconstructions, or 48 (12.7%) patients. There were 2 patients with bilateral infection. The median time to diagnosis of SSI was 29 days. Preoperative antibiotics were used in all cases of immediate expander reconstruction. NonYpenicillin allergic patients all received cefazolin, whereas penicillin-allergic patients received either clindamycin or vancomycin. Upon discharge, 200 (52.9%) patients were given a prescription for oral postoperative antibiotics. One hundred seventy-eight (47.1%) patients did not receive postoperative antibiotics. No significant differences were identified in demographics, comorbidities, and treatment variables between the 2 groups with and without postoperative antibiotics (Table 2). Risks of SSI were similar between patients who received postoperative antibiotics (12%) and those who did not (13.5%) (P = 0.67). Postoperative antibiotic agents and subsequent infections are detailed in Table 3. The use of postoperative antibiotics increased over the course of the study as illustrated in Figure 1. Despite this increased antibiotic use, however, incidence of infections did not decrease. In those cases that later developed infection after primary expander placement, cefazolin was used as the perioperative antibiotic in 43 (87.7%) cases, clindamycin in 6 (10.2%) cases, and vancomycin in 1 (2.0%) case. Wound culture data were submitted in 34 (68%) of the infected reconstructions. Cultures were obtained in the clinic in 7 cases and in the operating room in 27. Twenty-nine (85.3%) had growth of microorganism s including 5 (14.7%) with multiple organisms. The most common organisms cultured were methicillinsensitive Staphylococcus aureus (MSSA) (n = 11), followed by methicillin-resistant S. aureus (MRSA) (n = 6), and Staphylococcus epidermidis (n = 3) (Table 4). Staphylococcal species were responsible for 72.4% of positive cultures. TABLE 2. Patient Characteristics by Administration of Postoperative Antibiotics
Age, mean, y BMI, mean, kg/m2 Obesity (BMI, Q30 kg/m2) Smoking SSI Explantation Axillary surgery† None SLN biopsy Axillary lymph node dissection Radiation Chemotherapy ADM use Bilateral SSI
No Postoperative Antibiotics (n = 178)
Postoperative Antibiotics (n = 200)
P
50.8 26.2 38 (21.3%)
52.0 26.3 44 (22.0%)
0.31 0.87 0.88
13 (7.3%) 24 (13.5%) 14 (58.3%)
19 (9.5%) 24 (12.0%)* 14 (58.3%)
0.44 0.67 1.00 0.57
40 (22.6%) 89 (50.3%) 48 (27.1%)
36 (18.2%) 106 (53.5%) 56 (28.3%)
52 (29.2%) 92 (51.7%) 136 (76.4%) 85 (47.8%) 24 (13.5%)
66 (33.3%) 98 (49.0%) 164 (82.0%) 94 (47.0%) 24 (12.0%)
0.43 0.60 0.18 0.88 0.67
Bilateral cases given cephalexin and clindamycin, both had bilateral reconstruction, both received radiation to 1 side, and both received adjuvant chemotherapy. *Bilateral 2 patients. †Three cases missing axillary treatment. BMI indicates body mass index.
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TABLE 3. Postoperative Antibiotics Use and Subsequent Infection Discharge Antibiotic
Total (%)
Infection (%)
2 5 5 1 1 1 1 4 18 155 7 200 178 6 384
1 (50) 1 (20) 0 1 (100) 0 0 0 2 (50) 4 (22.2) 17 (11.0) 0 26 (13.0) 24 (13.5) 0 50 (13.0)*
Amoxicillin/clavulanate Azithromycin Trimethoprim/sulfamethoxazole Clarithromycin Cefdinir Dicloxacillin Doxycycline Ciprofloxacin Clindamycin Cephalexin Levafloxacin Discharge antibiotic total None Unknown Total *Bilateral infection, 2.
Sixteen (32%) cases of SSI resolved with antibiotics alone (oral antibiotics 12, intravenous antibiotics 4). Thirty-four (68%) infected expanders required surgical intervention. Twenty-nine (58%) expanders required explantation. Surgical salvage, consisting of washout and expander replacement, was attempted in 11 cases. Five (45.5%) cases successfully resolved the infection. Successful reconstruction was ultimately achieved in 10 of the 29 cases (delayed expander replacement 3, autologous reconstruction 7) after expander removal.
Antibiotics and Tissue Expanders
Antibiotic sensitivities were performed in the positive infected wound cultures. Retrospective comparison of the organism’s susceptibility profile with the preoperative intravenous antibiotic showed resistance to the preoperative antibiotic in 15 (51.7%) of 29 cases. The percent resistance to the preoperative antibiotic increased through the years of this study (2005, 0/1; 2006, none; 2007, 1/3; 2008, 1/4; 2009, 7/11; 2010, 3/4; and 2011, 3/6) (Fig. 2). Resistance to the postoperative prophylactic antibiotic, when administered, was observed in 8 (57.1%) of 14 cases. The proportion of infective organisms resistant to the postoperative antibiotic also increased over time (2005, none; 2006, none; 2007, 0/2; 2008, none; 2009, 4/7; 2010, 1/1; and 2011, 3/4). First-generation cephalosporins were the most commonly used agents in both the preoperative (cefazolin) and postoperative (cephalexin) prophylaxis settings. Figure 3 demonstrates the rates of SSI organism resistance to a first-generation cephalosporin for the various timings of antibiotic administration.
DISCUSSION Infectious complications of expander-based breast reconstruction are a significant cause of patient morbidity and increased hospital costs. Despite recognition of the importance of minimizing SSI after breast reconstruction, there is still no consensus regarding the utility or optimal regimen of prophylactic antibiotics. In this study, microbiological data were used to analyze the impact of extended prophylactic antibiotic use on the resistance patterns of the causative organisms of SSI. Current guidelines in antibiotic prophylaxis suggest administration of a single dose of perioperative antibiotic with cessation of further dosing beyond 24 hours after surgery. Selected agents are typically effective against gram-positive bacteria.1,12 In practice, the widespread use of extended postoperative antibiotics in expanderbased reconstruction is controversial. Phillips et al13 reviewed antibiotic usage and infection in 81 studies involving all forms of breast reconstruction. The authors found no benefit in patients who received
FIGURE 1. Discharge antibiotic use and infection rate by year. * 2014 Lippincott Williams & Wilkins
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Annals of Plastic Surgery
McCullough et al
TABLE 4. Microbiology of SSI Bacteria
Infections, n (%)
MSSA MRSA S. epidermidis Staphylococcus lugdunensis >-Hemolytic Streptococcus Corynebacterium Mycobacterium fortuitum Enterococcus Stenotrophomonas maltophilia Proteus mirabilis Serratia Pseudomonas Multiple No growth
11 6 3 1 1 1 3 2 1 1 3 2 5 5
(27.7) (17.6) (8.8) (2.9) (2.9) (2.9) (8.8) (5.8) (2.9) (2.9) (8.8) (5.4) (14.7) (14.7)
more than 24 hours of prophylactic antibiotics. Conversely, Clayton et al reviewed 250 patients undergoing breast reconstruction to determine the impact of initiating SCIP guidelines on SSI. In multivariate analysis, the authors found that those patients who did not receive postoperative antibiotics were 4.7 times as likely to develop an SSI requiring reoperation.14 Avashia et al15 also found increased rates of infection requiring expander removal (31.6% vs 7.9%) when antibiotics were discontinued after 24 hours as opposed to when they were continued for at least 48 hours. In contrast, our study shows no improvement in infection rates when postoperative antibiotics were used. Despite an increased trend in the use of postoperative antibiotics, the infection rate was unchanged over the course of the study. Moreover, when infections developed, there was a trend of increased resistance to the preoperative and postoperative prophylactic antibiotics over time. The use of antibiotics is not without complications. Other than cost, potential allergic reactions, and associated colitis, it is well documented that unnecessary or prolonged use of antibiotics can result in emergence of resistant organisms such as MRSA and vancomycin-resistant Enterococcus.16 Clayton et al14 found that those patients who did receive postoperative antibiotics, but who went on to develop SSI requiring explantation, were more likely to have gram-positive staphylococcal infections than gram-negative infections. The authors hypothesized that the use of postoperative antibiotics may have prevented gram-negative infections and selected for more resistant staphylococcal strains, but this interpretation is debatable.14 In our own experience, we observed increased resistance patterns at the same time more prophylactic postoperative antibiotics were used. Our finding that most of SSIs were caused by gram-positive organisms is consistent with the literature. Our study found staphylococcal species to be responsible for 61.7% of all cultured infections, and 72.4% of positive cultures. Methicillin-resistant S. aureus specifically accounted for 20.6% of those positive cultures. Clayton et al14 similarly found a high prevalence of MSSA, coagulase-negative Staphylococcus, and MRSA. Baumann et al17 evaluated the bacteriology of 75 tissue expander infections requiring explantation and found a high rate of skin f lora (68% of cases) as the causative organisms. Avashia et al15 in their analysis of expanderbased reconstruction with ADM, found predominantly MSSA, but also MRSA, coagulase-negative Staphylococcus, Enterococcus, Serratia, Pseudomonas, and Mycobacterium in their study sample. In a recent study by Weichman et al18 of device-based reconstructions, the most common organism cultured was S. epidermidis, followed 4
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by S. aureus, although overall they found equivalence in their study between gram-positive and gram-negative infections. In keeping with the emergence of more gram-negative infections, Mukhtar et al19 reviewed SSI after nonreconstructive breast surgery. They found 28.1% of their cultures to be S. aureus but 18.8% to be Escherichia coli. Although certain microbial trends have emerged among these multiple studies, the diversity of the bacteriologic findings suggests unique microbial profiles among individual institutions. Our study found substantial resistant rates of 20% to 54% to first-generation cephalosporins used in preoperative and postoperative prophylaxis (Fig. 3). Baumann et al17 reported a greater than 65% resistance to cefazolin in 75 positive wound cultures after tissue expander reconstruction. Weichman et al18 evaluated SSI after 43 implant-based breast reconstructions to examine bacterial resistance patterns. Postoperative prophylactic antibiotics were routinely administered. They found a 40% resistance of infecting organisms to cefazolin. Given these repeated findings confirming the poor activity of cefazolin against the causative organisms of SSI in breast reconstruction, multiple authors have suggested alternative antibiotic regimens when SSI develops. Feldman et al20 found a very high incidence of MRSA infections in their review of 31 SSIs and suggested vancomycin as empiric antibiotic therapy. Weichman et al recommend that if patients are amenable to oral antibiotics, f luoroquinolones should be used. If patients are not amenable to oral therapy, they suggest IV therapy be initiated with vancomycin in addition to either imipenem or gentamycin.18 This retrospective review is subject to inherent limitations. Cohorts were nonrandomized with potential selection for treatment with preventive postoperative antibiotics. However, no routine preference for antibiotics based on any patient or technical variables existed; rather, individual surgeon practice usually dictated antibiotic use. Sampling is biased toward more severe infections from which cultures were collected, likely underestimating the incidence of infections that responded to outpatient empiric oral antibiotics. Additionally, not all traditionally associated factors with infection were analyzed; for example, drain data and expander volumes were not evaluated. Multiple surgeons performed operations with technical variation. The small number of culture-positive SSI with relevant susceptibility studies limits definitive conclusion regarding the impact of prophylaxis on bacterial resistance.
FIGURE 2. For cases of SSI, percentage of cultured organisms resistant to the administered preoperative intravenous antibiotic by year. * 2014 Lippincott Williams & Wilkins
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Antibiotics and Tissue Expanders
FIGURE 3. For cases of SSI, susceptibility and resistance patterns of first-generation cephalosporin by timing of administration (‘‘Prophylactic cefazolin’’ was administered within 1 hour before surgical incision, ‘‘Postoperative cephalexin’’ was administered after surgery in preventive fashion, and ‘‘Empiric cefazolin’’ was administered postoperatively when SSI was suspected or diagnosed before availability of culture data).
In conclusion, administration of extended prophylactic antibiotics does not reduce risk of SSI after expander-based breast reconstruction, but may inf luence antibiotic resistance patterns when infections occur. The organisms most commonly responsible for SSI have become often resistant to first-generation cephalosporins. Future directions may include improved preoperative surveillance and tailored antiseptic or antibacterial prophylaxis.
10.
11. 12.
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