Epidemiology and Microbiology of Surgical Wound Infections

JOURNAL OF CLINICAL MICROBIOLOGY, Feb. 2000, p. 918 922 Vol. 38, No. 2 0095-1137/00/$04.00 0 Copyright 2000, American Society for Microbiology. All Rights Reserved. Epidemiology and Microbiology of Surgical Wound Infections A. GIACOMETTI, 1 * O. CIRIONI, 1 A. M. SCHIMIZZI, 1 M. S. DEL PRETE, 1 F. BARCHIESI, 1 M. M. D ERRICO, 2 E. PETRELLI, 3 AND G. SCALISE 1 Department of Infectious Diseases, Institute of Infectious Diseases and Public Health, University of Ancona, I-60121 Ancona, 1 Department of Hygiene, Institute of Infectious Diseases and Public Health, University of Ancona, I-60100 Ancona, 2 and Department of Infectious Diseases, San Salvatore Hospital, I-60121 Pesaro, 3 Italy Received 26 July 1999/Returned for modification 27 September 1999/Accepted 13 November 1999 This study included 676 surgery patients with signs and symptoms indicative of wound infections, who presented over the course of 6 years. Bacterial pathogens were isolated from 614 individuals. A single etiologic agent was identified in 271 patients, multiple agents were found in 343, and no agent was identified in 62. A high preponderance of aerobic bacteria was observed. Among the common pathogens were Staphylococcus aureus (191 patients, 28.2%), Pseudomonas aeruginosa (170 patients, 25.2%), Escherichia coli (53 patients, 7.8%), Staphylococcus epidermidis (48 patients, 7.1%), and Enterococcus faecalis (38 patients, 5.6%). A wound is the result of physical disruption of the skin, one of the major obstacles to the establishment of infections by bacterial pathogens in internal tissues. When bacteria breach this barrier, infection can result (1, 7). The most common underlying event for all wounds is trauma. Trauma may be accidental or intentionally induced. The latter category includes hospital-acquired wounds, which can be grouped according to how they are acquired, such as surgically and by use of intravenous medical devices. Although not intentionally induced, hospital-acquired wounds can be the pressure sores caused by local ischemia, too. They are also referred as decubitus ulcers, and when such wounds become infected, they are often colonized by multiple bacterial species (7). Most wound infections can be classified into two major categories: skin and soft tissue infections, although they often overlap as a consequence of disease progression (5, 7, 8, 13). Infections of hospital-acquired wounds are among the leading nosocomial causes of morbidity and increasing medical expense. Routine surveillance for hospital-acquired wound infections is recommended by both the Centers for Disease Control and Prevention (6) and the Surgical Infection Society (2). The objectives of the present study were to identify the etiologies of surgical wound infections over the course of 6 years and characterize the antimicrobial susceptibilities of the pathogen isolates. This retrospective study included 676 patients who underwent surgical treatment (abdominal, vascular, orthopedic, and reparative surgery) during the 6-year period from May 1993 to April 1999. All patients presented signs and symptoms indicative of surgical wound infections. A definite case of surgical wound infection was defined as one in which there was any skin eruption or drainage at the surgical site that was positive for bacteria by culture within 60 days of a surgical procedure. On the other hand, a presumptive case was one in which there was any skin eruption or drainage at the surgical site that was either culture negative or unresponsive to appropriate antibiotic therapy for organisms obtained on culture. * Corresponding author. Mailing address: Clinica Malattie Infettive, c/o Azienda Ospedaliera Umberto I, Piazza Cappelli, 1, 60121 Ancona, Italy. Phone: 39 71 5963467. Fax: 39 71 5963468. E-mail: cmalinf @popcsi.unian.it. Semiquantitative aerobic and anaerobic cultures were taken routinely before (time zero [T 0 ]), during (T 1 ), and at the end of (T 2 ) antibiotic therapy. For the isolation of anaerobes, specimens were inoculated onto Columbia blood agar plates enriched with hemin and menadione, incubated in an anaerobic chamber at 37 C, and examined at 48 and 96 h. Contemporaneously, specimens were Gram stained for direct examination. Altogether, 963 pre-antibiotic treatment specimens from 676 individuals were examined. One-thousand sixty bacterial strains were isolated from 614 individuals. Particularly, a single agent was identified in 271 patients, multiple agents were found in 343 patients, and no agent was identified in 62 patients. A high preponderance of aerobic bacteria was observed. Among the common pathogens were Staphylococcus aureus (191 patients, 28.2%), Pseudomonas aeruginosa (170 patients, 25.2%), Escherichia coli (53 patients, 7.8%), Staphylococcus epidermidis (48 patients, 7.1%), and Enterococcus faecalis (38 patients, 5.6%). Pure cultures most commonly yielded S. aureus (98 strains), P. aeruginosa (82 strains), and Enterobacteriaceae (102 strains). Polymicrobial infections involved a similar spectrum of pathogens and frequently involved gram-positive and gram-negative organisms, especially S. aureus together with P. aeruginosa (54 cases). Interestingly, the association between S. aureus and P. aeruginosa became increasingly more frequent, with 31 cases in the 2-year period from May 1997 to April 1999. Methicillin resistance was documented in 23 (74.2%) out of these 31 S. aureus isolates. MICs of several antimicrobial agents were determined by the broth microdilution method according to the procedures outlined by the National Committee for Clinical Laboratory Standards (9, 10). Results from cultures and susceptibility tests performed before antibiotic therapy are summarized in Table 1. Independently of culture results, antibiotic treatment was started for all patients. During treatment, 681 T 1 control specimens were obtained from 582 (95.0%) of the abovementioned 614 culture-positive (C ) individuals, while 71 specimens were obtained from 55 (88.7%) of the 62 culturenegative (C ) patients. Overall, bacterial pathogens were isolated from 131 (21.3%) C patients, while the C patients remained culture negative, with the exception of two patients positive for the presence of P. aeruginosa and Stenotrophomonas maltophilia. Finally, successive control specimens were obtained at the end of antibiotic treatment from all the 131 918

VOL. 38, 2000 NOTES 919 TABLE 1. Antimicrobial susceptibilities of bacteria isolated from surgical wounds Enterobacter spp. (43) Ampicillin 4 256 128 256 20.9 AMX-CLV 0.25 128 4 64 76.7 Piperacillin 0.25 256 8 64 72.1 Cefazolin 32 256 256 256 0.0 Ceftriaxone 0.25 64 1 32 69.8 Imipenem 0.25 8 0.5 2 95.3 Ciprofloxacin 0.25 8 0.25 1 90.7 Netilmicin 0.25 32 0.50 2 93.0 SXT-TMP 0.5 64 8 32 95.3 Escherichia coli (53) Ampicillin 0.50 256 4 128 66.0 AMX-CLV 0.25 32 1 16 96.2 Piperacillin 0.25 256 2 64 94.3 Cefazolin 0.25 256 2 16 90.6 Ceftriaxone 0.25 16 0.25 2 100.0 Imipenem 0.25 2 0.25 1 100.0 Ciprofloxacin 0.25 1 0.25 0.50 100.0 Netilmicin 0.25 2 0.50 1 100.0 SXT-TMP 0.25 128 2 32 90.6 Klebsiella spp. (41) Ampicillin 2 256 64 256 43.9 AMX-CLV 0.25 32 4 16 92.7 Piperacillin 0.25 256 8 128 73.2 Cefazolin 0.25 256 4 32 61.0 Ceftriaxone 0.25 4 0.50 4 100.0 Imipenem 0.25 4 0.5 4 100.0 Ciprofloxacin 0.25 4 0.25 2 92.7 Netilmicin 0.25 8 0.50 4 100.0 SXT-TMP 0.5 128 4 64 90.2 Proteus spp. (59) Ampicillin 4 256 32 256 32.2 AMX-CLV 0.25 16 1 16 100.0 Piperacillin 0.25 256 2 128 71.2 Cefazolin 1 128 4 32 52.5 Ceftriaxone 0.25 8 1 4 100.0 Imipenem 0.25 8 2 4 100.0 Ciprofloxacin 0.25 4 0.50 2 91.5 Netilmicin 0.25 32 0.50 8 93.2 SXT-TMP 0.5 128 4 64 59.3 Serratia spp. (50) Ampicillin 32 256 256 256 0.0 AMX-CLV 0.25 256 8 32 70.0 Piperacillin 0.25 256 16 128 66.0 Cefazolin 64 256 256 256 0.0 Ceftriaxone 0.25 64 4 32 92.0 Imipenem 0.50 16 2 8 96.0 Ciprofloxacin 0.25 8 0.50 4 82.0 Netilmicin 0.25 64 2 8 94.0 SXT-TMP 0.5 128 16 128 66.0 Other Enterobacteriaceae (6 c ) Pseudomonas aeruginosa (170) Pseudomonas spp. d (61) Ampicillin 1 128 AMX-CLV 0.25 8 Piperacillin 0.25 64 Cefazolin 2 128 Ceftriaxone 0.25 8 Imipenem 0.25 2 Ciprofloxacin 0.25 2 Netilmicin 0.25 4 SXT-TMP 1 64 AMX-CLV 8 256 32 256 38.8 Piperacillin 1 256 8 128 61.8 Cefazolin 128 256 256 256 0.0 Ceftazidime 0.25 256 2 32 87.0 Ceftriaxone 2 256 64 128 41.8 Imipenem 0.50 256 2 16 88.8 Ciprofloxacin 0.50 16 1 16 57.6 Netilmicin 0.25 64 8 32 71.8 SXT-TMP 4 256 128 256 7.6 AMX-CLV 4 256 32 256 31.1 Piperacillin 2 256 16 128 65.6 Cefazolin 128 256 256 0.0 Ceftazidime 0.25 256 2 16 93.4 Ceftriaxone 1 256 32 128 67.2 Imipenem 0.50 256 2 16 83.6 Continued Acinetobacter spp. e (42) Stenotrophomonas maltophilia (8 c ) Flavimonas oryzihabitans (3 c ) TABLE 1 Continued Ciprofloxacin 0.25 8 1 8 59.0 Netilmicin 0.25 32 4 32 80.3 SXT-TMP 8 256 128 256 4.9 Ampicillin 16 256 128 256 0.0 AMX-CLV 1 128 4 32 73.8 Piperacillin 4 256 32 128 59.5 Cefazolin 32 256 256 256 0.0 Ceftriaxone 1 128 16 64 57.1 Imipenem 0.25 32 1 4 95.2 Ciprofloxacin 0.25 8 0.50 2 92.8 Netilmicin 0.25 64 4 16 92.8 SXT-TMP 4 256 32 256 52.3 Ampicillin 128 256 AMX-CLV 16 128 Piperacillin 8 128 Cefazolin 128 256 Ceftriaxone 16 128 Imipenem 32 256 Ciprofloxacin 0.50 8 Netilmicin 0.50 16 SXT-TMP 64 256 Ampicillin 4 64 AMX-CLV 0.25 4 Piperacillin 0.25 1 Cefazolin 8 128 Ceftriaxone 0.25 1 Imipenem 0.25 0.50 Ciprofloxacin 0.25 1 Netilmicin 0.25 0.50 SXT-TMP 2 32 Bacteroides spp. (9 c ) Ampicillin 32 256 AMX-CLV 0.50 4 Piperacillin 2 64 Cefazolin 64 256 Ceftriaxone 1 16 Imipenem 0.25 1 Ciprofloxacin 0.50 4 Metronidazole 0.25 8 Clindamycin 0.50 32 MS f Staphylococcus aureus (87) MR g Staphylococcus aureus (104) MS f coagulase-negative staphylococci (67) MR g coagulase-negative staphylococci (71) AMX-CLV 0.25 4 0.25 2 100.0 Piperacillin 0.50 256 32 128 70.1 Cefazolin 0.25 32 2 8 95.4 Imipenem 0.25 4 1 4 100.0 Clarithromycin 0.25 16 1 8 79.3 Ciprofloxacin 0.50 16 1 8 80.4 Netilmicin 0.25 32 2 4 96.5 Teicoplanin 0.25 4 0.50 4 100.0 Vancomycin 0.25 4 1 4 100.0 AMX-CLV 8 256 32 128 0.0 Piperacillin 32 256 128 256 0.0 Cefazolin 4 256 16 64 52.9 Imipenem 0.5 256 8 32 63.0 Clarithromycin 0.25 32 1 16 55.8 Ciprofloxacin 0.25 64 1 8 54.8 Netilmicin 0.25 64 2 16 90.4 Teicoplanin 0.25 8 1 4 100.0 Vancomycin 0.25 32 1 4 99.1 AMX-CLV 0.25 8 0.50 2 97.1 Piperacillin 1 256 16 128 67.2 Cefazolin 0.25 32 4 8 92.5 Imipenem 0.25 2 1 2 100.0 Clarithromycin 0.25 32 1 8 82.8 Ciprofloxacin 0.50 16 1 4 80.6 Netilmicin 0.25 32 2 8 94.0 Teicoplanin 0.25 4 1 2 100.0 Vancomycin 0.25 2 1 2 100.0 AMX-CLV 8 256 64 256 0.0 Piperacillin 8 256 128 256 1.4 Cefazolin 8 256 32 128 39.4 Imipenem 0.5 256 8 32 56.3 Continued on following page

920 NOTES J. CLIN. MICROBIOL. Streptococcus spp. h (93) Enterococcus spp. i (48) Anaerobic cocci (27) TABLE 1 Continued Clarithromycin 0.25 32 2 16 52.1 Ciprofloxacin 0.25 64 1 8 53.5 Netilmicin 0.25 128 2 16 91.5 Teicoplanin 0.25 32 1 4 98.6 Vancomycin 0.25 32 0.50 4 98.6 AMX-CLV 0.25 2 0.25 1 100.0 Piperacillin 0.25 128 4 64 95.7 Cefazolin 0.25 8 0.50 2 100.0 Imipenem 0.25 2 0.25 0.50 100.0 Clarithromycin 0.25 16 0.25 2 97.8 Ciprofloxacin 0.25 16 0.25 2 94.6 Netilmicin 0.25 32 1 8 93.5 Teicoplanin 0.25 1 0.50 1 100.0 Vancomycin 0.25 0.50 0.50 0.50 100.0 AMX-CLV 0.25 64 2 32 72.9 Piperacillin 0.25 128 16 128 66.6 Cefazolin 0.25 256 32 256 31.2 Imipenem 0.25 32 1 8 100.0 Clarithromycin 0.25 32 0.50 8 62.5 Ciprofloxacin 0.50 32 2 16 54.2 Netilmicin 0.25 64 4 32 68.7 Teicoplanin 0.25 32 1 4 97.9 Vancomycin 0.25 32 1 4 97.9 AMX-CLV 0.25 16 2 8 88.8 Piperacillin 0.25 64 4 16 92.6 Cefazolin 0.25 64 2 16 92.6 Imipenem 0.25 32 1 4 96.3 Clarithromycin 0.25 16 2 16 77.7 Clindamycin 0.50 64 2 16 74.1 Metronidazole 0.50 128 2 64 77.7 Teicoplanin 0.25 0.50 0.25 0.50 100.0 Vancomycin 0.25 1 0.25 1 100.0 a 50% and 90%, MICs at which 50 and 90% of the strains, respectively, are inhibited. b AMX-CLV, amoxicillin-clavulanate; SMX-TMP, sulfamethoxazole-trimethoprim. c For organism with fewer than 10 isolates, MICs at which 50 and 90% of the strains are inhibited and percentages of susceptibilities were not included. d Included Pseudomonas fluorescens (38 strains), Pseudomonas putida (22 strains), and Pseudomonas stutzeri (1 strain). e Included Acinetobacter baumannii (21 strains), Acinetobacter lwoffi (19 strains), and Acinetobacter haemolyticus (2 strains). f Methicillin-susceptible strains. g Methicillin-resistant strains. h Included Streptococcus pyogenes (2 strains), Streptococcus pneumoniae (4 strains), Streptococcus milleri (53 strains), Streptococcus sanguis (13 strains), Streptococcus mitis (8 strains), Streptococcus mitior (7 strains), and Streptococcus oralis (6 strains). i Included Enterococcus faecalis (37 strains) and Enterococcus faecium (11 strains). patients with T 1 control specimens positive for bacterial pathogens. Nineteen individuals out of these 131 patients had persistently positive culture results in spite of specific antibiotic treatment. Overall, on the basis of clinical and microbiological data, 595 (96.9%) out of 614 C individuals were classified as having definite cases of surgical wound infection, while the abovementioned 62 C patients and 19 (3.1%) out of 614 C patients were classified as having presumptive cases of surgical wound infection. The susceptibility patterns of the 1,060 bacterial strains, divided into three 2-year periods, to several antimicrobial agents are summarized in Table 2. Some consequential observations arose from the data in Table 2. More than 50% of the Enterobacteriaceae tested were resistant to ampicillin, while only a few ( 20%) were resistant to the combination of amoxicillin and clavulanate. This finding suggests that the resistance observed was due mainly to the production of -lactamase by the organisms. In addition, most isolates were susceptible to ceftriaxone but more than 50% were resistant to cefazolin. Most P. aeruginosa isolates were susceptible to piperacillin, ceftazidime, and imipenem, although a gradual emergence of resistance to these -lactams has been observed. In addition, only a few isolates were resistant to netilmicin, while a severe decrease in ciprofloxacin activity has been noted in the last few years. In this study S. aureus was the most common cause of surgical wound infections. Methicillin resistance was documented in 104 (54.4%) of 191 S. aureus isolates. Although amoxicillinclavulanate, cefazolin, and imipenem were shown to be active in vitro against more than 60% of the isolates, according to National Committee for Clinical Laboratory Standards recommendations, the methicillin-resistant staphylococci were considered resistant to all -lactams, including penicillins, cephalosporins, -lactam -lactamase inhibitor combinations, and carbapenems, since these agents may be clinically ineffective against such organisms. Enterococci, a frequent cause of infection in surgical wounds, were isolated from 48 patients. Nearly all of the 38 Enterococcus faecalis isolates were susceptible in vitro to glycopeptides (Table 1) and gentamicin (data not shown). In contrast, most of the strains were resistant to cefazolin. Finally, good in vitro activities were shown by amoxicillin-clavulanate and imipenem. Anaerobic species (36 strains) were isolated from 21 distinct patients. Overall, the anaerobic gram-positive cocci (27 isolates) were susceptible to all the drugs tested, while the gramnegative isolates (nine Bacteroides spp. strains) were shown to be resistant to ampicillin and cefazolin. Epidemiological data about the emergence of antibiotic resistance were drawn by dividing the susceptibility patterns of the T 0 isolates on the basis of the microbiological results obtained during three 2-year periods (Table 2). The susceptibility data collected in this study suggest that some antibiotics would have very limited usefulness for the prophylaxis or the empirical treatment of wound infections. For instance, most of the gram-negative isolates were found to be resistant to ampicillin and cefazolin while the majority of staphylococcal strains were resistant to methicillin. These are remarkable data, since virtually all the patients received first- or second-generation cephalosporins as antibiotic prophylaxis. Overall, a progressive variation in causative pathogens and resistance patterns has been observed throughout the study. In fact, the susceptibility to antibiotics constantly decreased while multiresistant Pseudomonas and staphylococcal strains were isolated with increasing frequency. According to literature data, perioperative prophylaxis can decrease the incidence of wound infection (2, 3, 6, 7, 10 12, 14, 16). Cefazolin is the most used agent for surgical prophylaxis in our hospitals but can be ineffective against the increasingly common wound pathogens methicillin-resistant S. aureus, methicillin-resistant coagulase-negative staphylococci, P. aeruginosa, and other species of gramnegative rods. The inappropriate usage of antimicrobials in surgical perioperative prophylaxis is still a problem, and a close collaboration between surgeons and microbiologists is needed (4, 15). On the basis of our results, antimicrobial agents or drug combinations with wider spectra of activity and stronger resistance to enzymatic degradation are desirable for perioperative prophylaxis or treatment of surgical infection.

VOL. 38, 2000 NOTES 921 TABLE 2. Susceptibility patterns of the most frequently isolated bacteria Agent a % of strains showing resistance May 1993 April 1995 May 1995 April 1997 May 1997 April 1999 Enterobacteriaceae (252 b ) Ampicillin 53.1 56.1 57.1 AMX-CLV 16.3 18.4 18.1 Piperacillin 10.2 11.2 12.4 Cefazolin 51.0 53.1 53.3 Ceftriaxone 10.2 15.3 17.1 Imipenem 6.1 7.1 9.5 Ciprofloxacin 16.3 20.4 24.8 Netilmicin 14.3 13.3 17.6 SXT-TMP 36.7 35.7 40.9 Pseudomonas aeruginosa (170 c ) AMX-CLV 56.1 52.9 57.7 Piperacillin 12.2 17.6 23.1 Cefazolin 100.0 100.0 100.0 Ceftazidime 14.6 13.7 20.5 Ceftriaxone 56.1 58.8 64.1 Imipenem 9.7 15.7 21.8 Ciprofloxacin 19.5 31.4 39.7 Netilmicin 12.2 15.7 17.9 SXT-TMP 87.8 94.1 96.1 Staphylococcus aureus (191 d ) Methicillin 55.3 47.0 60.2 AMX-CLV 21.3 19.7 26.9 Piperacillin 42.5 36.4 46.1 Cefazolin 25.5 24.2 28.2 Imipenem 14.9 13.6 21.8 Clarithromycin 19.1 19.7 27.0 Ciprofloxacin 25.5 24.2 33.3 Netilmicin 12.8 15.1 20.5 Teicoplanin 0.0 1.5 1.3 Vancomycin 0.0 1.5 1.3 Coagulase-negative staphylococci (138 e ) Methicillin 42.4 47.9 59.6 AMX-CLV 18.2 20.8 26.3 Piperacillin 33.3 39.6 47.4 Cefazolin 24.2 20.8 29.8 Imipenem 12.1 14.6 22.8 Clarithromycin 21.2 25.0 28.1 Ciprofloxacin 24.2 29.2 35.1 Netilmicin 9.1 12.5 17.5 Teicoplanin 0.0 2.1 1.7 Vancomycin 0.0 2.1 1.7 Streptococcus spp. (93 f ) AMX-CLV 7.1 8.6 6.6 Piperacillin 7.1 11.4 10.0 Cefazolin 10.7 14.3 13.3 Imipenem 0.0 0.0 0.0 Clarithromycin 10.7 14.3 13.3 Ciprofloxacin 17.8 20.0 23.3 Netilmicin 14.3 22.8 20.0 Teicoplanin 0.0 0.0 0.0 Vancomycin 0.0 0.0 0.0 Enterococcus spp. (48 g ) AMX-CLV 9.1 7.1 13.0 Piperacillin 18.2 14.3 13.0 Cefazolin 36.4 35.7 34.8 Imipenem 9.1 7.1 8.7 Clarithromycin 36.4 42.8 39.1 Ciprofloxacin 54.5 50.0 56.5 Netilmicin 45.4 42.8 43.5 Teicoplanin 0.0 0.0 4.3 Vancomycin 0.0 7.1 4.3 a AMX-CLV, amoxicillin-clavulanate; SMX-TMP, sulfamethoxazole-trimethoprim. b Includes 49, 98, and 105 strains collected between May 1993 and April 1995, May 1995 and April 1997, and May 1997 and April 1999, respectively. c Includes 41, 51, and 78 strains collected between May 1993 and April 1995, May 1995 and April 1997, and May 1997 and April 1999, respectively. d Includes 47, 66, and 78 strains collected between May 1993 and April 1995, May 1995 and April 1997, and May 1997 and April 1999, respectively. e Includes 33, 48, and 57 strains collected between May 1993 and April 1995, May 1995 and April 1997, and May 1997 and April 1999, respectively. f Includes 28, 35, and 30 strains collected between May 1993 and April 1995, May 1995 and April 1997, and May 1997 and April 1999, respectively. g Includes 11, 14, and 23 strains collected between May 1993 and April 1995, May 1995 and April 1997, and May 1997 and April 1999, respectively.

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