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Abdominal Surgical Site Infection Incidence and Risk Factors in a Mexican Population

Guzmán-García, Crystell, MD; Flores-Barrientos, Oscar I., MD; Juárez-Rojop, Isela E., PhD; Robledo-Pascual, Julio C., MD; Baños-González, Manuel A., MD; Tovilla-Záratee, Carlos A., PhD; Hernández-Díaz, Yazmín, MD; González-Castro, Thelma B., PhD

Advances in Skin & Wound Care: June 2019 - Volume 32 - Issue 6 - p 1–6
doi: 10.1097/01.ASW.0000557833.80431.00

OBJECTIVE: To investigate possible predictors and prevalence of surgical site infections (SSIs) in a group of Mexican patients who underwent open abdominal surgery.

METHODS: This retrospective study included all patients (N = 755) who underwent elective or emergency open abdominal surgeries from October 2011 to March 2012.

MAIN OUTCOME MEASURE: Sociodemographic and clinical characteristics were collected through preoperative and postoperative examinations by the infection surveillance team. The relationship among variables (age, gender, body mass index, comorbidities, smoking habit, antimicrobial prophylaxis, hair removal, American Society of Anesthesiologists classification, type of operation, duration of operation, and SSI classification) was analyzed by odds ratio and χ2 tests.

MAIN RESULTS: Of the 755 patients, 91 (12%) suffered from SSI. Several variables were associated with SSI: American Society of Anesthesiologists classification (P = .001) and receiving preoperative prophylactic antimicrobials (P < .0001), among other factors. Isolated pathogens were mostly enterobacteria (60%).

CONCLUSIONS: Surveillance plays an important role in the control and prevention of SSI. Providers must implement appropriate procedures to reduce SSI after abdominal surgery.

In Tabasco, Mexico, Crystell Guzmán-García, MD, is a Doctor, Surveillance Unit for Healthcare-Associated Infections, Dr Juan Graham Casasus Hospital; Oscar I. Flores-Barrientos, MD, is a Doctor, Surveillance Unit for Healthcare-Associated Infections, Dr Juan Graham Casasus Hospital; Isela E. Juárez-Rojop, PhD, is a Researcher, Division of Health Sciences, Juárez University; Julio C. Robledo-Pascual, MD, is a Doctor, Pulmonary Service, Dr Juan Graham Casasus Hospital; Manuel A. Baños-González, MD, is Director of Teaching and Research, Dr Juan Graham Casasus Hospital; Carlos A. Tovilla-Zárate, PhD, is a Researcher, Multidisciplinary Division at Comalcalco, Juárez Autonomous University; Yazmín Hernández-Díaz, MD, is a Researcher, Multidisciplinary Division at Jalpa de Méndez, Juárez Autonomous University; and Thelma B. González-Castro, PhD, is a Research Professor, Division of Multidisciplinary Studies at Jalpa de Méndez, Juárez Autonomous University. Acknowledgments: The authors appreciate the technical support provided by the members of the Surveillance Unit for Healthcare-Associated Infections at the Dr Juan Graham Casasus Hospital. Further, they thank Mónica González Ortiz, Elizabeth Avalos Torres, and Anabel Del Valle Acosta for their excellent technical assistance. This work was supported by the Dr Juan Graham Casasus Hospital (JGC 2012-22A). The authors have disclosed no other financial relationships related to this article. Submitted May 8, 2018; accepted in revised form August 16, 2018.

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Surgical site infection (SSI) is a leading cause of adverse effects in surgical patients. Although it known that a person’s own skin flora can cause infections, SSI is currently the most common and costly healthcare-associated infection.1–3 Patients who develop an SSI are up to 60% more likely to spend time in an ICU, five times more likely to be readmitted to the hospital, and twice as likely to die compared with patients who do not develop an SSI.4,5 Moreover, SSIs prolong lengths of stay and increase healthcare costs.1

The risk of developing an SSI varies greatly according to the nature of the surgical procedure and the specific clinical characteristics of the patient undergoing that procedure.6 Several studies from around the world have shown that the rate of SSI is significantly associated with the patient’s American Society of Anesthesiologists (ASA) classification, obesity status, preoperative antimicrobial agent use, immunosuppression, use of surgical drains, use of iodine alone in skin preparation, and wound contamination, as well as smoking, diabetes mellitus, hypertension, and duration of hospital stay, among other factors.7–10 The duration of the surgical operation is also a significant parameter: only 3% of operations lasting 30 minutes or less lead to infection, whereas for operations lasting more than 6 hours, this rate increases to 18%.11 Other risk factors for SSI have been identified, such as tissue hypoxia and bleeding. However, several studies have demonstrated the efficacy of healthcare-associated infection surveillance in reducing SSIs.12

Open abdominal surgeries tend to have high infection rates compared with other kinds of surgeries.13 The most common complication of open abdominal surgery is SSI, and SSI compounds patient risk of abdominal wound dehiscence and evisceration, a severe postoperative complication.14 The incidence of SSIs is related to operating conditions (eg, inadequate environmental conditions, poor infrastructure, and insufficient equipment), wound contamination (clean, clean-contaminated, contaminated, or dirty-infected), and it is also related to whether surgery was open or laparoscopic.15–18 Laparoscopic surgery can reduce the risk of SSI for most abdominal surgeries and decrease rates of SSI by simply decreasing incision length. In addition, by decreasing manipulation and surgeon contact with the incisions, infection rates may be reduced. Laparoscopy may have less impact on immune function than open surgery.19

Most extant studies on SSI risk factors were carried out in Caucasian and Asian populations.20,21 The aim of this study was to evaluate possible predictors and prevalence of SSI in a group of Mexican patients who underwent open abdominal surgery in a public hospital.

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Researchers performed a retrospective analysis of all patients who had elective or emergency abdominal surgery in the General Surgery Department at Dr Juan Graham Casasus Hospital from October 2011 to March 2012. All of the surgeries evaluated during the assessment period were classified as open surgeries. Because of the lack of equipment and supplies available to perform laparoscopic surgery, researchers could not compare the results from open surgeries to laparoscopic surgeries.

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For the purposes of this study, an SSI was considered an infection that occurred within 30 days of an operation involving no implant or within 1 year if an implant (mesh) was used. The infections were further classified as superficial incisional (infection occurred within 30 days after any operative procedure and involved only skin and subcutaneous tissue of the incision), deep incisional primary/secondary (infection occurred within 30-90 days after the operative procedure and involved deep soft tissues of the incision), or organ/space (infection occurred within 30-90 days after the operative procedure and involved any part of the body deeper than the fascial/muscle layers that was opened or manipulated during the operative procedure). This classification is based on standard definitions from the US Centers for Disease Control and Prevention for SSI.9,22,23

Antimicrobials for surgical prophylaxis were administered intravenously to those patients who were prescribed them. The appropriate duration of antimicrobial treatment was evaluated by providers in clean and clean-contaminated wounds together with patient characteristics; antimicrobial treatment for contaminated and dirty/infected wounds was continued postsurgery for up to 7 days.

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Data Collection

The following sociodemographic and clinical characteristics were recorded using a clinical survey that was applied to all patients: age, gender, ASA score, body mass index (BMI), smoking, diabetes mellitus, prophylactic antimicrobials, wound class, type of procedure, abdominal hair removal, iodine alone use, duration of surgery, surgeon, admission date, date of surgery, and discharge date.

Patients were followed from the time of admission to 30 days postoperation. After discharge, patients were monitored in the outpatient clinic.

To prevent and control infection, the surgical site was inspected by medical professionals from the Surveillance Unit for Healthcare-Associated Infections (UVIACS) starting 24 to 48 hours after surgery; the surgeons also monitored for SSI and reported to UVIACS. The UVIACS unit were informed of all microbiology culture results related to surgical wounds. These cultures were then matched to the medical chart of the patient to determine whether they were related to a surgical procedure. Next, the UVIACS unit created a database to stratify and compare the prevalence of SSIs in all open abdominal procedures. Patients were divided into two groups: those with SSIs and those without. Patients who died or who had the operation and were subsequently transferred to another hospital were excluded from the analysis.

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Ethical Statement

The study was approved by the ethics committee at the Dr Juan Graham Casasus Hospital (trial registration 2013-3501-44) and complied with the ethical standards established in the 1975 Declaration of Helsinki.

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Statistical Analysis

A multivariate analysis was performed to evaluate several known risk factors associated with the development of SSIs. The χ2 test was used to determine significant associations between predictor and outcome variables for all categorical variables; odds ratios were used to test the strength of the association between predictors. P < .05 was considered significant.

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A total of 91 SSIs were diagnosed and classified as follows: 37 (40.6%) were superficial incisional, 20 (22%) were deep incisional, and 34 (37.4%) were organ/space (P = .09). The annual SSI rate in patients undergoing abdominal surgery in the authors’ hospital was 12.05%.

Table 1 shows the sociodemographic characteristics and risk factors of the 755 patients studied who underwent an open abdominal surgery during the study period. Gender, BMI, albumin levels, comorbidities, and smoking showed a significant association with SSI. Similarly, study authors also explored SSI rates by ASA classification (Table 2); 3.4% of ASA I patients developed an SSI; for ASA II, 2.6% of patients developed an SSI; and ASA III to IV patients had an SSI rate of 6.0%.

Table 1

Table 1

Table 2

Table 2

In addition, researchers analyzed the relationships between the surgical procedure characteristics and patients with SSI; type of operation, wound classification, duration of operation, and type of surgery were all significantly associated with the development of an SSI. The number of people in the operating room was not significantly associated with SSI (Tables 3 and 4).

Table 3

Table 3

Table 4

Table 4

Researchers found that 358 patients (47.4%) received preoperative antimicrobial prophylaxis (Table 2). According to these data, the duration and timing of antimicrobial prophylaxis did not follow published clinical practice guidelines; doses varied according to each surgeon’s prescription. The most frequent antimicrobial prescribed was ceftriaxone, followed by amikacin. Anaerobic coverage, consisting predominantly of metronidazole, was prescribed in all cases.

Finally, by analyzing the microbiology cultures of the 91 patients diagnosed with SSI in the general surgical service, it was ascertained that 5 (5.49%) were culture negative, and 86 (94.51%) had positive bacterial growth in culture within a 48-hour incubation period. The most common isolates in order of decreasing frequency were: gram-negative bacteria such as enterobacteria, 53.84% (Escherichia coli, 39.56%); Pseudomonas aeruginosa, 17.58%; enterococcus, 8.79%; coagulase-negative Staphylococcus species, 6.49%; and Candida albicans, 3.3%.

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In this study population, SSIs occurred in 12% of the total sample (n = 91). Previous studies found that the rate of SSI was 9.5% for colonic surgery and 1.4% for cholecystectomy;24 in 2017, the French national SSI impact survey reported that the rate of SSIs was 0.82% in patients undergoing hernia surgery and 2.03% in those who have an appendectomy.25 The disparity between previous data and the results of this study highlight the importance of further investigations into the relationship between SSI and open abdominal surgery.

In this study, patients who underwent colorectal surgery had the highest SSI rates. This procedure entails the risk of wound contamination by normal flora of the digestive tract. This is relevant because if the wound is dirty and/or contaminated, SSI can ensue if bacterial exposure causes an infection. However, contaminated and dirty wounds were not left open. Instead, during the surgical procedure, the abdominal cavity and subcutaneous tissue were washed multiple times, using multiple wound drainages. The study began by establishing the risk factors associated with SSI. Most patients in this study were between 18 and 40 years old. There are reports that associate SSI with ages older than 60 years9 and identify increasing age as independent predictor of SSI. In this study, the average age of patients with SSI was 41 years old, compared with other studies on SSI in which the average patient age was 50 years.26,27 Because most of the patients in this study were younger adults, it makes sense that the rates of SSI were lower than what has been previously reported.

Women had significantly lower rates of SSI compared with men. In men, androgens have been shown to have a proinflammatory effect on wounds, impairing re-epithelialization, whereas in women estrogens have an anti-inflammatory effect, which could account for this difference.25

Most of the patients were nonsmokers, but those who were smokers were at significantly higher risk of SSI. It has been reported that a smoking habit exerts a negative effect on wound healing through impairment of tissue oxygenation.9,28 Further, comorbidities such as diabetes mellitus, high blood pressure, and obesity previously reported as risk factors29 for SSI were also found to be such in this study. Therefore, prior to undertaking any abdominal surgical procedure, clinicians should know the comorbidities present in every patient and attempt to promote behavior changes such as smoking cessation to decrease the impact these factors can have on postoperative outcomes.

The SSI rate among patients who underwent elective surgery reached 16%; SSI influences 1-year recurrence rates in hernias. However, previous studies have reported a lower frequency of SSI in elective surgeries in those patients who modify their risk factors.30 Again, clinicians must work to reduce SSIs by addressing patients’ comorbidities prior to surgery, improving antimicrobial prescribing protocols, and seeking out the most advisable surgical procedures. It is essential that patient-related factors such as losing weight, smoking cessation, and proper control of chronic diseases prior to surgery are optimized.

Previous reports have shown a significant association between ASA classification and SSI,8,31 which these results also show; in particular, patients in ASA classes III and IV have an increased risk of SSIs. Clinicians should consider the patient’s ASA classification before undertaking surgery. This study did not find that a higher number of people in the operating room during surgery is an independent predictor of SSI. However, these results should be interpreted with caution because other studies32,33 have concluded that there is a statistically significant association between the number of people in the room during the operation and SSI.34 This discrepancy could be explained by the small sample size in this study; further studies are recommended for conclusive outcomes.

This study associates the duration of the operation and SSI. The longer the operation, the higher the probability a patient will acquire an infection because the time of wound exposure is longer. The authors suggest that an adequate methodology using recommendations and strategies to improve adherence to SSI prevention interventions during surgery can control SSI in the operating theater.

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Antimicrobial Therapy

Although patients whose microbiology reports showed evidence of SSI had their antimicrobial treatments modified, the authors of this study determined that patients received inadequate antimicrobial treatment not only as preoperative prophylaxis but also during the postoperative period. Providers did not prescribe antimicrobials according to best practices or the correct dosages, timing, or duration of treatment. In some cases, patients lacked the economic resources to buy the indicated antimicrobial; in others, the availability of antimicrobials in the study hospital was limited. Because of these factors, the principles of antimicrobial prophylaxis were not met.

Upon arrival to the hospital, 60% of patients presented with complicated surgical cases; these patients were more likely to have dirty wounds. Histopathologic findings of surgical specimen reports for these patients described advanced evolution of the disease (ie, gangrenous and ruptured).

This study demonstrated no significant association between SSI and patients receiving antimicrobial prophylaxis; nevertheless, preoperative prophylactic antimicrobial administration (within 1 hour before surgery) should be considered an integral part of SSI prevention. The authors recommend facilities develop antimicrobial guidelines regarding these patients.

This study’s authors observed an increasing incidence of ceftriaxone resistance in E. coli isolates responsible for SSIs. Further, the researchers observed high numbers of carbapenem-resistant and fluoroquinolone agents isolates responsible for infection, with imipenem resistance reported for E. coli and Pseudomonas isolates. These findings are relevant to individualizing recommendations for antimicrobial prophylaxis prior to surgical procedures; it is necessary to formulate specific and local guidelines for antimicrobial prophylaxis.

This hospital receives patients from several municipalities; patients often present with complicated diseases. Moreover, patients could only receive the antimicrobials available in the hospital; those infected were treated with a broad-spectrum antimicrobial. The lack of targeted antimicrobial treatment may have influenced the outcomes. Each SSI was associated with additional postoperative days in the hospital and attributable costs, depending on the infecting pathogen.

Among the bacterial species isolated from patients with SSI after abdominal surgery was a predominance of Gram-negative bacilli of gastrointestinal origin (aerobes and anaerobes) together with Gram-positive bacteria such as Staphylococcus and Enterococcus species. These findings were consistent with similar studies in which the marked diversity of potential pathogens involved in these infections highlights the risk of an inadequate treatment approach.35,36

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During this study, the authors observed noncompliance with perioperative protocols, such as changing gloves and dressings before closing by the surgeon. In addition, violations to perioperative protocols in the surgical ward were detected, related to the lack of hospital surgical materials and supplies available to care for surgical wounds, suggesting improper handling and wound contamination.

This study included SSIs detected, cultured, and managed on an outpatient basis; the actual overall SSI incidence could have been higher than reported here, because there were patients who underwent outpatient surgery and were lost to follow-up and thus were not recruited. In other words, the uncertainty around the accuracy of postdischarge surveillance has hampered researchers’ ability to get more exact SSI rates.

Finally, the sample size of the present report is small when compared with other studies reporting SSI rates for different procedures.

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There is scarce information on SSI surveillance methods in general in the Mexican population. To the authors’ knowledge, this study is the first analysis investigating the risk factors associated with SSI after open abdominal surgery in this population; these results may provide a different perspective to improve the surveillance of SSI by contributing new data to the literature, which is mostly confined to White populations.

The present study also suggests that the lack of discipline in adhering to SSI prevention protocols by surgical team members is a significant intraoperative risk factor, which could be modified by further intervention.

Finally, the findings of the present study are important because in the state of Tabasco, Mexico, hospitals do not implement antimicrobial prophylaxis policies; ideally, the outcomes of this study could encourage the development of such policies. Antimicrobial policy guidelines should be established to improve SSI control before, during, and after any abdominal surgical procedure in the Mexican population.

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abdominal surgery; antimicrobials; ASA classification; surgery; surgical site infection; surveillance

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