Prevalence of bacterial resistance in surgical wound infections in peripheral arterial surgery

Abstracts

CONTEXTO: A infecção de sítio cirúrgico é uma complicação grave da cirurgia vascular periférica. O recente aparecimento de microorganismos resistentes e agressivos gera uma nova preocupação com relação ao manejo dessas infecções. OBJETIVO: Verificar a prevalência de resistência bacteriana, a epidemiologia, os possíveis fatores associados e o padrão de resistência nas infecções de ferida operatória das cirurgias arteriais periféricas. MÉTODOS: Estudo de prevalência, envolvendo 40 pacientes portadores de infecção da ferida operatória e submetidos à cirurgia de revascularização arterial periférica no período de janeiro de 2007 a maio de 2008. RESULTADOS: Participaram do estudo pacientes com média de idade de 64,2 anos, predominantemente do sexo masculino (70%). A prevalência geral de resistência bacteriana foi 72,5%, e de multirresistência, 60%. O microorganismo mais freqüentemente isolado foi o Staphylococcus aureus (40%), sendo 11 das 16 culturas (68,7%) resistentes à oxacilina. As taxas de resistência aos principais antimicrobianos testados foram: ampicilina, 85,7%; cefalosporina, 76,9%; oxacilina, 65%; e ciprofloxacina, 62,5%. Não foi identificada resistência à vancomicina e ao imipenem. CONCLUSÕES: Os achados deste estudo sugerem que a resistência bacteriana é um problema atual e muito prevalente nas cirurgias arteriais periféricas. O Staphylococcus aureus segue sendo o principal patógeno envolvido, demonstrando altas taxas de resistência. A vancomicina e o imipenem seguem sendo as principais opções terapêuticas para esse tipo de infecção.

Infecção de ferida operatória; resistência a medicamentos; cirurgia

ORIGINAL ARTICLE

Prevalence of bacterial resistance in surgical wound infections in peripheral arterial surgery

Eduardo Lichtenfels^I; Airton D. Frankini^II; Jonas Paludo^III; Pedro A. d'Azevedo^IV

^IGraduate student, Program of Pathology, Universidade Federal de Ciências da Saúde de Porto Alegre (UFCSPA), Porto Alegre, RS, Brazil. Vascular surgeon, Complexo Hospitalar Santa Casa de Porto Alegre (CHSCPA), Porto Alegre, RS, Brazil

^IIPhD. Associate professor, Angiology and Vascular Surgery, UFCSPA, Porto Alegre, RS, Brazil. Vascular surgeon, CHSCPA, Porto Alegre, RS, Brazil

^IIIMedical student, UFCSPA, Porto Alegre, RS, Brazil

^IVPhD. Associate professor, Department of Microbiology and Parasitology, UFCSPA, Porto Alegre, RS, Brazil. Professor, Graduate Program in Pathology, UFCSPA, Porto Alegre, RS, Brazil

Correspondence

ABSTRACT

BACKGROUND: Surgical wound infection is a severe complication of peripheral vascular surgery. The recent appearance of resistant and aggressive pathogens brings new concerns related to the management of these infections.

OBJECTIVE: To verify the prevalence of bacterial resistance, epidemiology, possibly associated factors and resistance patterns in wound infections of peripheral arterial surgeries.

METHODS: Prevalence study of 40 patients with surgical wound infections submitted to peripheral arterial revascularization procedures between January 2007 and May 2008.

RESULTS: Mean age was 64.2 years, males represented 70% of all cases. The overall prevalence of bacterial resistance was 72.5% and multiresistance 60%. The commonest single cultured microorganism was the Staphylococcus aureus (40%), and 11 of 16 cultures (68.7%) were oxacillin-resistant. Prevalence of resistance to the main tested antibiotics: ampicillin 85.7%; cephalosporin 76.9%; oxacillin 65%; and ciprofloxacin 62.5%. Resistance to vancomycin and imipenem was not identified.

CONCLUSIONS: The findings of this study suggest that bacterial resistance is a prevalent and current problem in peripheral vascular surgeries. Staphylococcus aureus is still the most frequently involved pathogen, showing high resistance rates. Vancomycin and imipenem are still the best therapeutic options to treat these infections.

Palavras-chave: Surgical wound infection, drug resistance, surgery.

Introduction

Surgical site infection is a severe complication of peripheral vascular surgery. Surgical wound (SW) infection occurs in 0.9-22% of arterial vascular surgeries, and is around 3% in recent series.^1,2 Deep infection, which involves the wall of the operated artery or the implanted graft, occurs in 1.2-13% of arterial surgeries.^2,3 França et al., in a recent Brazilian publication, reported an incidence of synthetic graft infection in peripheral vascular surgery of 4.6%.² This type of infection is more frequent in emergency surgeries, inguinal dissections and use of vascular graft in the femoral region or in subcutaneous route. Treatment is complex, involving reoperations, use of wide-spectrum antimicrobials and prolonged hospital stay. The result is a high mortality (10-76%) and morbidity rate (amputation rates of 8-53%).^2-5

The most frequently involved microorganisms are the Staphylococcus aureus, coagulase-negative Staphylococcus, Pseudomonas sp., Escherichia coli, Enterobacter sp. and Proteus sp..^5,6 The most frequently isolated pathogen is Staphylococcus aureus (33-55%).⁷ About 25% of infections are polymicrobial.⁵ Late infections are often caused by coagulase-negative Staphylococcus , especially Staphylococcus epidermidis . The infections caused by gram-negative are very destructive and often associated with Pseudomonas aeruginosa^8,9.

The recent occurrence of resistant and aggressive strains generates a new concern over antimicrobial prophylaxis, treatment and morbidity and mortality rates. Recent data have shown that the methicillin-resistant Staphylococcus aureus (MRSA) is currently the most frequently isolated pathogen of complex and severe infections in vascular surgery, with a 40% prevalence.⁶ In a recent survey performed in the USA, a high prevalence of MRSA was shown in hospitalized patients and in those coming from the community. Prolonged prophylaxis and indiscriminate use of antimicrobials contributed to the development of bacterial resistance.^7,10

Increased incidence of multi-resistant pathogens and more aggressive strains in vascular surgeries contributes to an increase in morbidity and mortality rates,^6,9,11,12 and mortality rates of up to 75% are reported.^6,9 As a consequence, the development of more complex alternative treatments and new techniques of antimicrobial prophylaxis are necessary.¹³

This study aimed at determining the prevalence of bacterial resistance, epidemiology, possible associated factors and resistance standard of SW in peripheral arterial surgeries performed at the Vascular Surgery Service of Complexo Hospitalar Santa Casa de Porto Alegre (CHSCPA).

Methods

Patients

This prevalence study included patients submitted to peripheral arterial revascularization surgeries, with and without use of vascular graft, who developed SW infection in the postoperative period (hospital and outpatient). The procedures were performed at the Vascular Surgery Service of CHSCPA from January 2007 to May 2008.

Inclusion criteria were age over 18 years; clinical diagnosis of SW (up to 30 days after the surgery) and/or graft (up to 1 year after the surgery) infection; laboratory confirmation of the infection (culture); administration of surgical antimicrobial prophylaxis (cefazolin 1-2 g); and presence of infection defined as hospital infection (diagnosed 72 h after hospitalization and related to the procedure). All the patients included in the sample signed a consent form.

Microbiology

The collected material was comprised of SW secretion, tissue and graft fragment (if affected) with clinical diagnosis of infection. All the material was collected by the same researcher and analyzed by the same laboratory team.

Bacterioscopic examination, Gram stain, culture exam and antibiogram were performed in all cases. Screen and identification of Staphylococcus epidermidis were performed using the susceptibility test to desferrioxamine and fosfomycin, with disc diffusion in Muller-Hinton Agar plates.¹⁴ The susceptibility test to antimicrobials was performed using the disc diffusion technique placed on Muller-Hinton Agar plates, according to the Clinical and Laboratory Standards Institute (CLSI).¹⁵ The bacterial inoculum was prepared using the same concentration of a 0.5 McFarland standard suspension. The plates remained 16-18 h in a greenhouse, with temperature ranging between +35 and -2º C. Interpretation of the diameter in inhibition zones was performed according to CLSI recommendations.¹⁵ The following antimicrobial discs were used: gram-positive cocci - vancomycin 30 µg, oxacillin 1 µg, erythromycin 15 µg, clindamycin 2 µg, ciprofloxacin 5 µg, sulfamethoxazole 25 µg, chloramphenicol 30 µg and gentamicine 10 µg; gram-negative bacili - ampicillin 10 µg, first- (cefazolin), second- (cefoxitin) and fourth-generation (cefepime) cephalosporins, ciprofloxacin 5 µg, gentamicine 10 µg, sulfamethoxazole 25 µg and imipenem.

Evaluation of susceptibility and resistance to antimicrobials was performed through analysis of inhibitory halos, defined according to CLSI criteria. Multi-resistance was defined as resistance to three or more classes of antimicrobials.

Statistical analysis

Data analysis started as a descriptive statistics with distribution of simple and relative frequencies using contingency tables. Fisher's exact test was used to investigate a possible association between bacterial resistance to antimicrobials and qualitative variables, in 2 x 2 tables. The data received a statistical treatment using the software Statistical Package for the Social Sciences (SPSS), version 11.5, in which, a significance level (alpha) of 5% was adopted for decision criteria, and between 5-10% for borderline significance.

Results

Patients' demographic characteristics

Forty patients with SW infection after peripheral arterial surgery were analyzed during the study. The patients' mean age was 64.2 years, and the male gender was predominant (70%). The patients' demographic data are summarized in Table 1. There was no significant difference between the groups with infection by resistant and non-resistant microorganisms as to population characteristics.

Patients' surgical characteristics

Mean preoperative hospital stay was 8.9 (SD = 8.5) days. Therapeutic antimicrobials were used in 27.5% of cases in the preoperative period. The most frequent type of surgery was femoropopliteal bypass (35%), followed by aortobifemoral bypass (27.5%). Twenty-nine patients (72.5%) with infection had a vascular graft. SW infection topography had the following order of frequency: inguinal, 67.5% (23.1% bilateral); lower limb, 30%; and abdomen, 2.5%. The most frequent type of infection, according to Szilagyi classification,¹⁶ was degree II or incisional (60%). Graft exposure (degree III) was observed in 10% of cases. The main surgical data are shown in Table 2. Preoperative mean hospital stay was significantly higher in patients with infection due to resistant microorganisms.

Microbiology

Gram-positive cocci accounted for 65% of infections. The most frequent microorganism in SW infections was the Staphylococcus aureus, present in 40% of cases. Complete microbiological analysis is shown in Table 3.

Bacterial resistance

Overall prevalence of bacterial resistance was 72.5%. Multi-resistance was observed in 60% of cases. The oxacillin-resistant Staphylococcus aureus had a 68.7% resistance rate. The oxacillin-resistant Staphylococcus aureus alone had overall prevalence of 27.5%. Resistance rates according to isolated microorganism are shown in Table 3. Prevalence rates of resistance to antimicrobials were ampicillin, 85.7%; first-generation cephalosporin, 76.9%; oxacillin, 65%; ciprofloxacin, 62.5%; erythromycin, 61.5%; clindamycin, 61.5%; sulfamethoxazole, 60%; chloramphenicol, 57.7%; gentamicine, 52.5%; second-generation cephalosporin, 50%; and fourth-generation cephalosporin, 21.4%. There was no resistance to vancomycin or imipenem. The resistance pattern of assessed samples is shown in Table 4.

Discussion

The recent occurrence of resistant and aggressive strains generates a new concern over antimicrobial prophylaxis, treatment and morbidity and mortality rates within the context of medicine and peripheral vascular surgery.¹⁷ The importance of bacterial resistance lies in the fact that it has become much prevalent in hospital institutions,^18,19 accounts for the lack of antimicrobial treatment,²⁰ can be disseminated, causing a public health problem²¹ and increases costs regarding antimicrobial therapy and patient treatment.²² Increased incidence of multi-resistant pathogens and more aggressive strains in vascular surgeries contributes to an increase in morbidity and mortality rates,^6,9,11,12 and mortality rates of up to 75% are reported.^6,9

The main factors involved in the development of SW infection are bacterial, wound and the patient's own factors. Many pathogens have certain components that increase their virulence, such as the Staphylococcus aureus biofilm. Local factors include surgical material, surgical technique, graft implantation, and local complications (more frequent in the inguinal region). Factors associated with the patient are age, malnutrition, obesity, neoplasms, and trauma, among others.^23-27 Elderly patients have higher risk due to skin and subcutaneous tissue atrophy.²⁸ Among risk factors for vascular graft infections, in addition to those previously mentioned, are bacterial contamination of the graft, surgery involving the inguinal region, grafts in extra-anatomical position, prolonged preoperative hospital stay, emergency surgery, prolonged surgical time, associated gastrointestinal surgery, and arterial reoperation.^3,29 In this study the patients had high mean age and predominance of male gender. All the patients had comorbidities, most of them were multiple. The most frequent associated diseases were hypertension, ischemic heart disease and diabetes mellitus, besides smoking. The main factors related to the development of infection were identified, but there was no association between comorbidities or gender and prevalence of bacterial resistance. The patients that developed infections caused by resistant microorganisms had longer preoperative hospital stay (Table 2), which can be related to increased infection rates and prevalence of bacterial resistance.³⁰ Use of vascular grafts, in this study, was not associated with infection due to resistant microorganism. All the patients submitted to surgery, either with or without graft, were submitted to preoperative antimicrobial prophylaxis, judicious surgical technique, and intensive perioperative care. In agreement with the literature, the most frequent infection topography was the inguinal region (67.5%), despite not having any significant difference between studied groups.

Type of surgery also influences risk of infection;^28,31 however, the relationship with development of infection due to resistant organism is not known. The most frequent surgeries in this study were femoropopliteal and aortobifemoral bypass. Type of surgery was not associated with prevalence of bacterial resistance, but iliofemoral revascularization in anatomical position showed a tendency to protection against infection due to resistant bacteria in the statistical analysis. Resistant infections showed higher frequency by infrainguinal bypasses and extra-anatomical bypasses (Table 2).

Recent data have showed that the MRSA is currently the most frequently isolated pathogen in complex and severe infections in vascular surgery (40%).⁶ The most severe infections, incisional and with vascular graft exposure, showed a higher prevalence of resistant microorganisms in our study, but with no statistical difference. In general, incisional infection was the most frequent (60%) (Table 2).

The most frequently involved bacteria are the Staphylococcus aureus, coagulase-negative Staphylococcus, Pseudomonas sp., Escherichia coli, Enterobacter sp. and Proteus sp..^5,6,9 The most common pathogen is the Staphylococcus aureus (33-55%).⁷ Cowie et al. showed that the MRSA is the second most frequent microorganism (21%) in infections in patients submitted to vascular surgery.¹¹ The most prevalent microorganism causing infection in our study was the Staphylococcus aureus (37.9%), followed by coagulase-negative Staphylococcus (20.7%). Many authors report the Staphylococcus epidermidis as one of the main microorganisms related to hospital infections¹⁴ and especially SW infection in vascular surgery,^5,6,9,32-36 as well as its association with high rates of antimicrobial resistance.^32,34 In this study, however, the tests to identify Staphylococcus epidermidis were all negative. Our data conform a high prevalence of coagulase-negative Staphylococcus and a high rate of this type of antimicrobial resistance in this type of infection, but it does not identify the Staphylococcus epidermidis as one of main pathogens involved (Table 3).

Occurrence of multiresistant bacteria, such as the methicillin-resistant Staphylococcus aureus and, more rarely, vancomycin, and coagulase-negative quinolone-resistant Staphylococcus have been recently observed. The SENTRY program showed a 16.7% incidence of methicillin-resistant Staphylococcus aureus .³⁷ The same program, in 2003, showed an increase in 29.2-36.0% in resistance rates involving coagulase-negative Staphylococcus in Latin America.³⁸ Brazilian data have showed rates of oxacillin resistance ranging between 64-80% for coagulase-negative Staphylococcus .^39,40 Multiresistance was found in 59.9% of Staphylococcus aureus isolated from hospitalized patients.⁹ Naylor et al., in a multi-center study evaluating complex and graft infections in Great Britain and Ireland, found a 40% prevalence of methicillin-resistant Staphylococcus aureus in complex SW infections and 33% in graft infections.⁶ Taylor et al. reported that gram-positive microorganisms are the main responsible for infection in vascular surgeries (60.9%); the Staphylococcus aureus is the most frequent pathogen (60.8%), and the MRSA is the most prevalent isolated microorganism (57.5%).¹² The same authors also found that SW is the main MRSA site (54.8%).¹² Our study found a high rate of bacterial resistance (72.5%) and multiresistance (60%), which corroborates data from the recent literature on the increase in bacterial resistance in this group of surgical patients. In addition, the Staphylococcus aureus, the most frequent microorganism in this study, had a 68.7% resistance rate, and the oxacillin-resistant Staphylococcus aureus alone had prevalence of 27.5%.

The spectrum of resistant phenotypes ranges from susceptibility to all beta-lactamic antibiotics (4.1%) to resistance to five non-beta-lactamic antibiotics (2.4%). The phenotypes with most frequent resistance among hospital organisms are multiresistance to ciprofloxacin, erythromycin and clindamycin (47.6%) resistance to ciprofloxacin and erythromycin (13.7%), and multiresistance to ciprofloxacin, erythromycin, clindamycin and gentamicine (8.3%). As to patterns of bacterial resistance, there was high prevalence of resistance to beta-lactamic antibiotics (ampicillin, cephalosporins and oxacillin), as well as high rates of resistance to ciprofloxacin, clindamycin and sulfamethoxazole. There was no case of resistance to sulfamethoxazole in the tested group (gram-positive), neither to imipenem (gram-negative). Double and multiple resistance rates were also high, well above 50% (Table 4).

The limitations of this study include those inherent to a cross-sectional design, such as absence of follow-up, analysis of prevalence rates and convenience sample obtained consecutively. The small sample of this study reflects the low incidence of SW infection in peripheral arterial surgeries.

The findings of this study suggest that bacterial resistance is a current and much prevalent problem in peripheral arterial surgeries. Similarly, there were high rates of multiresistance and resistance patterns, involving some of the main antimicrobials used in prophylaxis and treatment of SW infections. Among the factors that could be associated with infection due to resistant bacteria, only preoperative hospital stay time was significantly higher in this group. The most frequent pathogen was the Staphylococcus aureus, which showed high rates of resistance. On the other hand, vancomycin and imipenem are still the best therapeutic options for the treatment of these infections. We suggest wider studies, follow-up of patients for a better evaluation of associated factors and outcome in these patients.

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Publication Dates

• Publication in this collection
  08 Dec 2008
• Date of issue
  Sept 2008

History

• Received
  29 June 2008
• Accepted
  30 July 2008