JOURNAL OF CLINICAL MICROBIOLOGY, Feb. 2000, p.

918922
0095-1137/00/$04.000
Copyright 2000, American Society for Microbiology. All Rights Reserved.

Vol. 38, No. 2

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. DERRICO,2 E. PETRELLI,3 AND G. SCALISE1
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

Semiquantitative aerobic and anaerobic cultures were taken

routinely before (time zero [T0]), during (T1), and at the end of
(T2) 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 37C, 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 T1 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

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.
918

Downloaded from http://jcm.asm.org/ on August 17, 2015 by guest

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%).

VOL. 38, 2000

NOTES

TABLE 1. Antimicrobial susceptibilities of bacteria

isolated from surgical wounds
Organism(s)
(no. of strains)

Agentb

MIC (g/ml)a
Range

50%

90%

4256
0.25128
0.25256
32256
0.2564
0.258
0.258
0.2532
0.564

128
256
4
64
8
64
256
256
1
32
0.5
2
0.25
1
0.50
2
8
32

Escherichia coli (53)

Ampicillin
AMX-CLV
Piperacillin
Cefazolin
Ceftriaxone
Imipenem
Ciprofloxacin
Netilmicin
SXT-TMP

0.50256
0.2532
0.25256
0.25256
0.2516
0.252
0.251
0.252
0.25128

4
1
2
2
0.25
0.25
0.25
0.50
2

Ampicillin
AMX-CLV
Piperacillin
Cefazolin
Ceftriaxone
Imipenem
Ciprofloxacin
Netilmicin
SXT-TMP

2256
0.2532
0.25256
0.25256
0.254
0.254
0.254
0.258
0.5128

Ampicillin
AMX-CLV
Piperacillin
Cefazolin
Ceftriaxone
Imipenem
Ciprofloxacin
Netilmicin
SXT-TMP

4256
0.2516
0.25256
1128
0.258
0.258
0.254
0.2532
0.5128

Ampicillin
AMX-CLV
Piperacillin
Cefazolin
Ceftriaxone
Imipenem
Ciprofloxacin
Netilmicin
SXT-TMP

32256
0.25256
0.25256
64256
0.2564
0.5016
0.258
0.2564
0.5128

Ampicillin
AMX-CLV
Piperacillin
Cefazolin
Ceftriaxone
Imipenem
Ciprofloxacin
Netilmicin
SXT-TMP

1128
0.258
0.2564
2128
0.258
0.252
0.252
0.254
164

Klebsiella spp. (41)

Proteus spp. (59)

Serratia spp. (50)

Other Enterobacteriaceae (6c)

Pseudomonas aeruginosa (170)

Pseudomonas spp.d
(61)

TABLE 1Continued
%
Susceptible

20.9
76.7
72.1
0.0
69.8
95.3
90.7
93.0
95.3

128
16
64
16
2
1
0.50
1
32

66.0
96.2
94.3
90.6
100.0
100.0
100.0
100.0
90.6

64
4
8
4
0.50
0.5
0.25
0.50
4

256
16
128
32
4
4
2
4
64

43.9
92.7
73.2
61.0
100.0
100.0
92.7
100.0
90.2

32
1
2
4
1
2
0.50
0.50
4

256
16
128
32
4
4
2
8
64

32.2
100.0
71.2
52.5
100.0
100.0
91.5
93.2
59.3

256
256
8
32
16
128
256
256
4
32
2
8
0.50
4
2
8
16
128

0.0
70.0
66.0
0.0
92.0
96.0
82.0
94.0
66.0

AMX-CLV
Piperacillin
Cefazolin
Ceftazidime
Ceftriaxone
Imipenem
Ciprofloxacin
Netilmicin
SXT-TMP

8256
32
1256
8
128256 256
0.25256
2
2256
64
0.50256
2
0.5016
1
0.2564
8
4256 128

AMX-CLV
Piperacillin
Cefazolin
Ceftazidime
Ceftriaxone
Imipenem

4256
32
2256
16
128256 256
0.25256
2
1256
32
0.50256
2

256
128
256
32
128
16
16
32
256

38.8
61.8
0.0
87.0
41.8
88.8
57.6
71.8
7.6

256
128
0.0
16
128
16

31.1
65.6
93.4
67.2
83.6

Continued

MIC (g/ml)a
90%

%
Susceptible

Ciprofloxacin
Netilmicin
SXT-TMP

0.258
1
0.2532
4
8256 128

8
32
256

59.0
80.3
4.9

Acinetobacter spp.e
(42)

Ampicillin
AMX-CLV
Piperacillin
Cefazolin
Ceftriaxone
Imipenem
Ciprofloxacin
Netilmicin
SXT-TMP

16256 128
1128
4
4256 32
32256 256
1128
16
0.2532
1
0.258
0.50
0.2564
4
4256
32

256
32
128
256
64
4
2
16
256

0.0
73.8
59.5
0.0
57.1
95.2
92.8
92.8
52.3

Stenotrophomonas
maltophilia (8c)

Ampicillin
AMX-CLV
Piperacillin
Cefazolin
Ceftriaxone
Imipenem
Ciprofloxacin
Netilmicin
SXT-TMP

128256
16128
8128
128256
16128
32256
0.508
0.5016
64256

Flavimonas oryzihabitans (3c)

Ampicillin
AMX-CLV
Piperacillin
Cefazolin
Ceftriaxone
Imipenem
Ciprofloxacin
Netilmicin
SXT-TMP

2
128
8
4
8
8
4
4
4

100.0
70.1
95.4
100.0
79.3
80.4
96.5
100.0
100.0

128
256
64
32
16
8
16
4
4

0.0
0.0
52.9
63.0
55.8
54.8
90.4
100.0
99.1

2
128
8
2
8
4
8
2
2

97.1
67.2
92.5
100.0
82.8
80.6
94.0
100.0
100.0

256
256
128
32

0.0
1.4
39.4
56.3

Organism(s)
(no. of strains)

Agentb

Range

50%

464
0.254
0.251
8128
0.251
0.250.50
0.251
0.250.50
232

Bacteroides spp. (9c) Ampicillin

32256
AMX-CLV
0.504
Piperacillin
264
Cefazolin
64256
Ceftriaxone
116
Imipenem
0.251
Ciprofloxacin
0.504
Metronidazole 0.258
Clindamycin
0.5032
MSf Staphylococcus
aureus (87)

AMX-CLV
Piperacillin
Cefazolin
Imipenem
Clarithromycin
Ciprofloxacin
Netilmicin
Teicoplanin
Vancomycin

0.254
0.50256
0.2532
0.254
0.2516
0.5016
0.2532
0.254
0.254

0.25
32
2
1
1
1
2
0.50
1

8256 32
MRg Staphylococcus AMX-CLV
aureus (104)
Piperacillin
32256 128
Cefazolin
4256 16
Imipenem
0.5256
8
Clarithromycin 0.2532
1
Ciprofloxacin
0.2564
1
Netilmicin
0.2564
2
Teicoplanin
0.258
1
Vancomycin
0.2532
1
MS f coagulase-negative staphylococci (67)

AMX-CLV
Piperacillin
Cefazolin
Imipenem
Clarithromycin
Ciprofloxacin
Netilmicin
Teicoplanin
Vancomycin

MRg coagulase-neg- AMX-CLV

ative staphyloPiperacillin
cocci (71)
Cefazolin
Imipenem

0.258
1256
0.2532
0.252
0.2532
0.5016
0.2532
0.254
0.252

0.50
16
4
1
1
1
2
1
1

8256 64
8256 128
8256 32
0.5256
8

Continued on following page

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Enterobacter spp. (43) Ampicillin

AMX-CLV
Piperacillin
Cefazolin
Ceftriaxone
Imipenem
Ciprofloxacin
Netilmicin
SXT-TMP

919

920

NOTES

J. CLIN. MICROBIOL.
TABLE 1Continued

Organism(s)
(no. of strains)

Agentb

MIC (g/ml)a
Range

50%

90%

2
1
2
1
0.50

16
8
16
4
4

0.252
0.25128
0.258
0.252
0.2516
0.2516
0.2532
0.251
0.250.50

0.25
4
0.50
0.25
0.25
0.25
1
0.50
0.50

1
64
2
0.50
2
2
8
1
0.50

Streptococcus spp.h
(93)

AMX-CLV
Piperacillin
Cefazolin
Imipenem
Clarithromycin
Ciprofloxacin
Netilmicin
Teicoplanin
Vancomycin

Enterococcus spp.i
(48)

AMX-CLV
0.2564
Piperacillin
0.25128
Cefazolin
0.25256
Imipenem
0.2532
Clarithromycin 0.2532
Ciprofloxacin
0.5032
Netilmicin
0.2564
Teicoplanin
0.2532
Vancomycin
0.2532

Anaerobic cocci
(27)

AMX-CLV
Piperacillin
Cefazolin
Imipenem
Clarithromycin
Clindamycin
Metronidazole
Teicoplanin
Vancomycin

0.2516
0.2564
0.2564
0.2532
0.2516
0.5064
0.50128
0.250.50
0.251

2
16
32
1
0.50
2
4
1
1
2
4
2
1
2
2
2
0.25
0.25

32
128
256
8
8
16
32
4
4
8
16
16
4
16
16
64
0.50
1

52.1
53.5
91.5
98.6
98.6
100.0
95.7
100.0
100.0
97.8
94.6
93.5
100.0
100.0
72.9
66.6
31.2
100.0
62.5
54.2
68.7
97.9
97.9
88.8
92.6
92.6
96.3
77.7
74.1
77.7
100.0
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 T1 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

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Clarithromycin 0.2532
Ciprofloxacin
0.2564
Netilmicin
0.25128
Teicoplanin
0.2532
Vancomycin
0.2532

%
Susceptible

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 T0 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, 1012, 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

Organism(s) (no. of strains)
b

Agenta

% of strains showing resistance

May 1993April 1995

May 1995April 1997

May 1997April 1999

Ampicillin
AMX-CLV
Piperacillin
Cefazolin
Ceftriaxone
Imipenem
Ciprofloxacin
Netilmicin
SXT-TMP

53.1
16.3
10.2
51.0
10.2
6.1
16.3
14.3
36.7

56.1
18.4
11.2
53.1
15.3
7.1
20.4
13.3
35.7

57.1
18.1
12.4
53.3
17.1
9.5
24.8
17.6
40.9

Pseudomonas aeruginosa (170c)

AMX-CLV
Piperacillin
Cefazolin
Ceftazidime
Ceftriaxone
Imipenem
Ciprofloxacin
Netilmicin
SXT-TMP

56.1
12.2
100.0
14.6
56.1
9.7
19.5
12.2
87.8

52.9
17.6
100.0
13.7
58.8
15.7
31.4
15.7
94.1

57.7
23.1
100.0
20.5
64.1
21.8
39.7
17.9
96.1

Staphylococcus aureus (191d)

Methicillin
AMX-CLV
Piperacillin
Cefazolin
Imipenem
Clarithromycin
Ciprofloxacin
Netilmicin
Teicoplanin
Vancomycin

55.3
21.3
42.5
25.5
14.9
19.1
25.5
12.8
0.0
0.0

47.0
19.7
36.4
24.2
13.6
19.7
24.2
15.1
1.5
1.5

60.2
26.9
46.1
28.2
21.8
27.0
33.3
20.5
1.3
1.3

Coagulase-negative staphylococci (138e)

Methicillin
AMX-CLV
Piperacillin
Cefazolin
Imipenem
Clarithromycin
Ciprofloxacin
Netilmicin
Teicoplanin
Vancomycin

42.4
18.2
33.3
24.2
12.1
21.2
24.2
9.1
0.0
0.0

47.9
20.8
39.6
20.8
14.6
25.0
29.2
12.5
2.1
2.1

59.6
26.3
47.4
29.8
22.8
28.1
35.1
17.5
1.7
1.7

Streptococcus spp. (93f)

AMX-CLV
Piperacillin
Cefazolin
Imipenem
Clarithromycin
Ciprofloxacin
Netilmicin
Teicoplanin
Vancomycin

7.1
7.1
10.7
0.0
10.7
17.8
14.3
0.0
0.0

8.6
11.4
14.3
0.0
14.3
20.0
22.8
0.0
0.0

6.6
10.0
13.3
0.0
13.3
23.3
20.0
0.0
0.0

Enterococcus spp. (48g)

AMX-CLV
Piperacillin
Cefazolin
Imipenem
Clarithromycin
Ciprofloxacin
Netilmicin
Teicoplanin
Vancomycin

9.1
18.2
36.4
9.1
36.4
54.5
45.4
0.0
0.0

7.1
14.3
35.7
7.1
42.8
50.0
42.8
0.0
7.1

13.0
13.0
34.8
8.7
39.1
56.5
43.5
4.3
4.3

AMX-CLV, amoxicillin-clavulanate; SMX-TMP, sulfamethoxazole-trimethoprim.

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.
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.
b
c

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Enterobacteriaceae (252 )

922

NOTES

J. CLIN. MICROBIOL.
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