Surgical Site Infection (SSI) Rates Among Patients Who Underwent Mastectomy After the Introduction of SSI Prevention Policies
Objective. To describe the results of an intervention program to reduce the rate of surgical site infection (SSI) in the breast tumor department of a referral teaching hospital for patients with cancer.
Methods. Preventive measures introduced in the Breast Tumor Department of the study hospital included the following: starting in July 2000, use of sterile technique for wound care; starting in 2001, use of closed antireflux silicone evacuation systems, use of perioperative antimicrobial prophylaxis, provision of feedback to surgeons, and remodeling of the ambulatory wound care clinic. We conducted surveillance of all patients who underwent mastectomy between February 1 and December 31, 2001, and the SSI rate was calculated. A case‐control analysis was performed for risk factors known to be associated with SSI. Results were compared with the data from 2000.
Results. The study included data on 385 surgeries. SSIs were registered in 52 (13.7%) of these 385, which was a rate 58.6% less than the 2000 infection rate (33.1%). Risk factors associated with SSI included concomitant chemotherapy and radiation therapy (OR, 3.6 [95% confidence interval {CI}, 1.9‐7.1]), surgery performed during an evening shift (OR, 1.9 [95% CI, 1.1‐3.6]), and insertion of a second drainage tube during the late postoperative period (OR, 2.8 [95% CI, 1.4‐5.7]). The mean number (± SD) of postoperative visits to the outpatient wound care clinic was reduced from 
in 2000 to 
in 2001 (
, Student's t test). The mean number of days that the evacuation systems were used was reduced from 19.0 to 16.0 days (
, Student's t test).
Conclusions. Continuous wound surveillance, along with feedback to surgeons, use of closed antireflux evacuation systems, and standardized practices in wound and drainage‐tube care, decreased by 58.6% the rate of SSI in a breast surgical department with high rates of infection.
Received November 4, 2004; accepted August 31, 2005; electronically published July 20, 2006.
Surgical site infections (SSIs) remain one of the most common causes of morbidity in the surgical patient, despite advances in surgical practice and antibiotic prophylaxis. The average cost of a surgical wound infection has proven difficult to estimate and varies depending on the type of surgical procedure, but hospital costs alone may be over US$2500.00.1‐3 The entire economic burden of SSIs is rarely taken into account, as the majority of wound infections are not diagnosed until after hospital discharge4,5; the cost to the patient in prescription charges, visits to the hospital, loss of earnings, and reduced quality of life are largely underestimated.2,3
Mastectomies have traditionally been considered clean surgical procedures; the majority of studies suggest that the infection rate in clean surgery is 5% or less.6‐8 According to the National Nosocomial Infections Surveillance System, the SSI rate for mastectomies during the past decade ranged between 2.07% and 3.9%7; however, other series have reported higher rates of infection.9‐12
In 2000, the Department of Infectious Diseases and the Breast Tumor Department at our institution (Instituto Nacional de Cancerología, Mexico City, Mexico) began an active surveillance program for SSIs that included direct observation from patient admission to surgery and until the last surgical follow‐up visit at the outpatient clinic. We identified high rates of SSI (33.0% of cases) for all types of mastectomies, and we identified the following risk factors: receipt of concomitant chemotherapy and radiation therapy (odds ratio [OR], 2.3 [95% confidence interval {CI}, 1.2‐4.3]; 
), obesity (OR, 2.3 [95% CI, 1.2‐4.6]; 
), radical surgery (OR, 3.1 [95% CI, 1.1‐8.6]; 
), placement of a surgical drainage tube for 19 days or longer (OR, 2.9 [95% CI, 1.5‐4.6]; 
), and insertion of a second drain during the late postoperative period (OR, 3.7 [95% CI, 1.8‐7.8]; 
).12 We also detected an outbreak of Pseudomonas aeruginosa SSI,13 as well as poor compliance with infection control practices and inappropriate wound management at the outpatient Wound Clinic. As a routine procedure, drainage tubes were disconnected from the system, washed with tap water, dried, and reconnected to proximal drainage tubes inserted in patients. The evacuation system used polyvinyl chloride (PVC) tubes connected to a plastic reservoir with no anti‐reflux system (Drenovac; Equipo e Instumental Médico). Doctors and nurses did not wear sterile gloves for wound care nor when handling medical supplies (gauze, clamps, and other supplies were not sterile)12; also, 2‐3 patients were evaluated simultaneously in a 20‐m2 room that had no physical barriers between patients and had no air conditioning, which favored high temperatures in the area.
With the aim of decreasing the rate of SSI after mastectomy, the following sequenced prevention measures were introduced: starting in July 2000, use of sterile technique for wound care; and starting in 2001, use of closed, antireflux, silicone evacuation systems, use of perioperative antimicrobial prophylaxis, provision of feedback to surgeons, and remodeling of the ambulatory wound care clinic to establish physical barriers between patients and to provide air conditioning. Table 1 gives a detailed description of the interventions. This article describes the effect of introducing preventive measures in our Breast Tumor Department, which had high rates of wound complications. We also discuss our experience with continuous surveillance for SSIs and use of standard sterile procedure for wound and drainage‐tube care.
Methods
Background and Interventions
Between February 1, 2001, and December 31, 2001, all breast surgeries for cancer performed at the Instituto Nacional de Cancerologia were registered. This is a 150‐bed, national referral teaching hospital for adult patients with cancer, where more than 3,000 surgeries are performed annually. Mastectomies represent more than 10% of all procedures performed at the institution.
Patients Management and Surveillance
Patients were operated on by the same surgical team and managed according to the standard protocol of care; follow‐up included daily medical‐chart review, microbiology reports, and rounds at the patients’ bedside. After discharge from the hospital, one physician who was part of the study team conducted direct observation along with the surgeon once or twice per week, until the last surgical follow‐up visit at the outpatient clinic. Data on the appearance of the wound and the amount and characteristics of material drained from the wound were collected at each visit on a standardized form. All patients were followed up for at least 30 days, as previously described for the year 2000.12 A sample for culture was obtained if infection was suspected because of pain or tenderness, localized swelling, redness or heat, purulent drainage from a superficial or deep incision, fever (temperature, 38°C or higher), or suspicion of an infected wound by the surgeon. SSI was classified according to the Centers for Disease Control and Prevention definitions for surgical infection.14
Statistical Analysis
Data collected were introduced into a database (with Paradox 9 software; Corel). Patient variables studied included age, body mass index, duration of hospitalization (preoperative and postoperative hospital stay), type of mastectomy undergone, history of smoking (past or current, and if current, whether the patient had avoided smoking in the 72 hours prior to surgery), presence of diabetes mellitus, presence of hypertension, previous receipt of chemotherapy and radiation therapy, American Society of Anesthesiologists physical status (ASA) score, surgical shift during which surgery had been performed, prophylactic and postoperative antibiotic therapy received, receipt of immediate breast reconstruction, and occurrence of other wound complications, such as flap necrosis, dehiscence, epidermolysis, and hematoma or seroma formation.
We also conducted case‐control analysis to verify whether the data for the patient and operation were similar to those reported in 2000. Case patients were defined as those with SSI, and control subjects were patients who underwent a mastectomy who were free of infection by day 30 after surgery. Case and control patients were all selected from the same population (ie, patients who underwent mastectomy in 2001).
For analysis, the number of SSIs per 100 surgeries was calculated. The frequencies of hematomas, seromas, epidermolysis, and dehiscence were also calculated. The Student's t test, the Mann‐Whitney U test, and the χ2 test for proportions were used for analysis (with Stata software for Windows; Stata), as appropriate. To test the association between the occurrence of SSI and possible risk factors, we estimated odds ratios and 95% confidence intervals (with Epi Info 6 software; Centers for Disease Control and Prevention). A P value of <.05 was considered statistically significant. Results were compared with results for 2000.
Results
During the 11‐month surveillance period, 385 patients who had undergone mastectomy were monitored, and 379 (98.4%) completed the follow‐up. Fifty‐two surgical infections were registered: 40 (76.9%) were superficial incisional infections and 12 (23.1%) were deep incisional infections. The median time from surgery to SSI diagnosis was 25.0 days (range, 6‐58 days). Monthly rates of wound infection for 2000 and 2001 are shown in Figure 1.
Figure 1. Monthly rates of surgical site infection (SSI) among patients who underwent mastectomy at the study hospital, 2000‐2001.
Forty‐eight patients developed 1 SSI, and 2 patients developed 2 wound infections. Cultures were performed for 42 infections (80.7%). The bacteria most frequently isolated from infected wounds were as follows: Staphylococcus aureus (6 infections), Klebsiella species (6), E. cloacae (5), Citrobacter species (4), S. epidermidis (3), Pseudomonas aeruginosa (2), Serratia species (2), and Escherichia coli (2). Other bacteria were isolated from 6 infections, and cultures were negative for pathogens in 6 infections. Bacteria isolated from the infected wounds differed little from the bacteria isolated before the study, except for P. aeruginosa, which was more common during the previous year (2000, comparison group), when an outbreak was detected.13 Klebsiella species were more commonly isolated in the present series.
The tumor, node, and metastasis (TNM) stages for the 385 patients at the time of surgery were as follows: in situ stage, 4 patients (1.03%); stage I, 19 patients (4.9%); stage IIA, 69 patients (17.9%); stage IIB, 67 patients (17.4%); stage IIIA, 65 patients (16.9%); stage IIIB, 44 patients (11.4%), and stage IV, 20 patients (5.2%). These proportions were similar to the TNM stages described for the previous year (2000). Two patients had Paget disease diagnosed, and 1 patient had phyllodes diagnosed. Ninety‐four patients (24.4%) had a biopsy performed at another institution and an unavailable pathology report; thus, TNM staging was incomplete at the time of surgery.
The mean age (± SD) of case patients was 
years, and that of control patients was 
years (P, not significant). Diabetes mellitus, receipt of neoadjuvant chemotherapy, immediate breast reconstruction, receipt of antibiotic prophylaxis, ASA score, duration of surgery, and duration of hospital stay were not associated with infection. Variables shown to be associated with infection were as follows: preoperative chemotherapy and radiation therapy (OR, 3.6 [95% CI, 1.9‐7.2]; 
), surgery performed during the afternoon or evening shift (OR, 1.9 [95% CI, 1.1‐3.6]; 
), and need for reinsertion of a drainage tube during the late postoperative period (ie, 2‐3 weeks after surgery) (OR, 2.8 [95% CI, 1.3‐5.7]; 
). Results of univariate analysis are shown in Table 2.
The mean duration of surgery (±SD) was 
minutes for case patients and 
minutes for noninfected patients (P, not significant). The mean duration of hospital stay for case patients was 
days and that for control patients was 
days (P, not significant); these findings are very similar to those of previous studies.
In addition to SSI, we monitored other wound‐related complications. Epidemolysis occurred in 19.5% of patients, flap necrosis occurred in 18.2%, dehiscence occurred in 10.1%, seromas occurred in 20.8%, and hematomas occurred in 2.1%. Rates of these complications were similar to those observed for the study performed in 2000, except for epidermolysis, which decreased from 37.4% of patients to 19.5%.
Data on drainage tube type, duration of drainage tube placement, and average number of visits to the outpatient wound care clinic were compared with the results of the study performed in 2000.12 In 2001, the mean time (±SD) that a drainage tube remained in place was 
days, compared with 
days in 2000 (
, Student's t test). Similarly, the mean number of visits (±SD) to the outpatient wound care clinic was reduced from 
visits in 2000 to 
in 2001 (
, Student's t test). Savings related to direct costs of ambulatory wound care were approximately US$8,500.00 for 9 months. We did not find significant differences in the wound infection rate between drainage tube types; however, seromas were less common in patients with the silicone evacuation system with flat tubes (Biovac; Biometrix). Details about the duration of placement and the types of drainage tube used are given in Table 3, along with data on infections and seroma formation for the drainage tube types.
Discussion
Surveillance of SSIs is costly in human resources and time. Surveillance of postoperative patients has become a difficult task with changes in surgical practice, such as shortened duration of postoperative stay, greater numbers of outpatient procedures, and the increased use of laparoscopic surgery, but there is no doubt that surveillance of SSIs has been shown to be a powerful prevention tool if data are collected, analyzed, and used appropriately.15
The prospective surveillance program for SSIs at the Breast Tumor Department of our institution allowed us to characterize the frequency of and the risk factors associated with SSI among patients who underwent mastectomy in 2000.12 Starting in July 2000, we introduced sequenced preventive measures (Table 1) and observed the effects of these measures by means of the same surveillance method (ie, direct observation) at the outpatient clinic, in conjunction with the surgeons. All patients were followed up for at least 30 days, and no changes were observed in the intensity of surveillance or the variables studied. As shown in Figure 1, the preventive intervention program decreased the rate of SSI; this decrease occurred gradually and was greater during the second half of 2001. Overall, the number of SSIs decreased by more than 50% from 2000 to 2001.
Several surveillance methods with various degrees of sensitivity have been reviewed for detection of infected wounds,16,17 but the most precise and reliable method for SSI surveillance is one that includes examination of the wound and gathering of information from medical records (ie, reading of the surgical notes and culture results). An SSI surveillance program must be sufficiently sensitive to identify cases of wound infection diagnosed after patient hospital discharge.18
The number of SSIs observed during 2000 was clearly higher than the reported rate.7,9‐11 Mastectomy is classified as a clean procedure; thus, SSI rates should not be higher than 5%,7 but in studies that have exclusively included patients with cancer, the rate of infection does tend to be higher.9‐11 In patients with advanced stage of cancer, wound complications are even more frequent.12,19‐20 In our series, 45.7% of patients had an advanced stage of cancer, so more‐radical procedures with concomitant chemotherapy and radiation treatment were more common, which probably contributed to a higher rate of wound complications, because chemotherapy and radiation treatment were strongly associated with SSI (OR, 3.6 [95% CI, 1.9‐7.1]).
Determining which of the intervention measures introduced had a greater effect on the decrease of SSIs is difficult, but at least 3 of the strategies were demonstrated to be efficacious. Surveillance for SSI with provision of feedback to surgeons is a powerful prevention tool15 and has been shown to decrease the incidence of surgical infections in various studies.21‐23 The latter finding is probably related to the fact that surgeons are more aware of the best surgical technique and perioperative patient care.7
As shown in Table 1, we modified the practices for wound and drainage‐tube care. In July 2000, as a result of the outbreak investigation, sterile technique for wound and drainage tube care was introduced. Later, in January 2001, evacuation systems were also changed. As reported previously,12 the drainage systems used had PVC tubes, which were frequently converted to open drainage tubes 10‐14 days after surgery. It was also a frequent practice to disconnect tube drains from the reservoir, clean them with tap water to remove fibrin clots, and reattach them to the evacuation system, which practices are clearly inappropriate. PVC tubes are also more rigid and may increase damage to tissues. Guidelines have strongly recommended that an evacuation system be used only if necessary, and, if used, it should always be a closed system.24 A radical change in the use of closed, silicone evacuation systems helped to improve infection control practices and decreased SSI rates. As shown in Table 3, use of a closed, antireflux, silicone evacuation system with flat tubes (Biovac) also diminished the rate of seroma formation (
). Use of sterile technique for wound and drainage‐tube care during the postoperative period should be strongly encouraged, because the drainage tube breaks the skin barrier and constitutes a bridge between the external environment and the patient's tissue.
In June 2001, in accordance with best practices for perioperative antibiotic prophylaxis, we decided that patients who had undergone mastectomy should receive antibiotic prophylaxis for no more than 24 hours. As a routine procedure, surgeons chose to continue prophylaxis until all drainage tubes were removed, despite the fact that evidence does not support this practice.25 In mid‐2001, explicit stop orders were given, and continuous monitoring of antibiotic prescription practices was instituted.
Inappropriate surgical antimicrobial prophylaxis continues to be a major problem in most hospitals. Inappropriate use of antimicrobial agents not only adds to the cost of medical care, but it also increases selective pressure for bacterial resistance in healthcare facilities.15 According to Burke,26 cost savings and improved infection control rates have been shown to accrue with appropriate use of surgical antimicrobial prophylaxis. In our series, in 2000, the cost of unnecessary antibiotics per patient was approximately US$20.82; in the same period in 2001, this cost diminished to US$4.47. For the group of all patients, net cost savings realized by elimination of unnecessary antibiotic therapy was US$5000.00.
The risk factors found to be associated with SSI in 2001 were similar to those reported for the previous year, during which variables related to use of drainage tubes and concomitant chemotherapy and radiation treatment were associated with SSI. In the 2001 series, the hospital shift during which surgery was performed was also studied as a possible risk factor for SSI. As shown in Table 2, performance of surgery during an evening shift increased the risk of infection by nearly 2‐fold. This finding could be related to less supervision by staff surgeons and senior residents. In the literature, a relationship has been reported between greater expertise and occurrence of fewer wound complications.27,28
In summary, the prospective surveillance program at the Breast Tumor Department of our institution and the establishment of preventive measures decreased the SSI rate by 58.6% in 2001. The program also improved infection control and antibiotic prescription practices and reduced the cost of medical care. The 58.6% reduction in the SSI rate observed during 2001 was maintained throughout 2002.
Acknowledgment
In August 2002, GlaxoSmithKline Foundation (Mexico) gave this research an award for Best Original Clinical Research Project submitted to the “XIII Premio Nacional de Investigación de la Fundación GlaxoSmithKline.”
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Presented in part: 4th Panamerican Meeting Association on Infection Control and Hospital Epidemiology in Cancún, México, November 2002.