9
A Prospective Study of Postoperative Surgical Site Infections in Dogs and Cats SIMONE EUGSTER, DrMedVet, PETER SCHAWALDER Prof DrMedVet, FRE ´ DE ´ RIC GASCHEN, PD, DrMedVet, Diplomate ECVIM-CA & ACVIM, and PATRICK BOERLIN, Prof DrMedVet Objective—To assess postoperative surgical site infection (SSI) rate and to identify associated predictive factors. Study Design—Prospective clinical study. Animals—Dogs and cats that had surgery (1010 interventions) during 58 weeks from April 1999 to June 2000. Methods—Data sheets were completed by clinicians. Patients were controlled for clinical evidence of SSI at suture removal. Two definitions of SSI (‘‘infection’’ and ‘‘infection/inflammation’’) were developed specifically for this study and used for statistical analysis. Logistic regression models were built in order to identify significant predictive factors for SSI. Results—Wounds with ‘‘infection/inflammation’’ occurred in 5.8% and ‘‘infected’’ wounds in 3% of patients. The outcome ‘‘infection’’ was associated with 3 major risk factors (duration of surgery, increasing number of persons in the operating room, dirty surgical site) and 1 protective factor (antimicrobial prophylaxis). The outcome ‘‘infection/inflammation’’ was associated with 6 signif- icant factors (duration of anesthesia, duration of postoperative intensive care unit stay, wound drainage, increasing patient weight, dirty surgical site, and antimicrobial prophylaxis). Conclusions—SSI frequency in companion animals is comparable with the frequency observed in human surgical patients. Several significant predictive factors for SSI in small animals surgery were identified. Clinical Relevance—Baseline information for SSI surveillance in our hospital and for comparison with other studies was defined. The factors identified may help to predict infections in surgical patients and to take adequate preventive measures for patients at risk. r Copyright 2004 by The American College of Veterinary Surgeons Key words: infection, surgery, wound, antimicrobial prophylaxis, cat, dog. INTRODUCTION N OSOCOMIAL INFECTIONS in general, and postoperative surgical site infections (SSIs) in par- ticular, are a growing concern in veterinary hospitals. Surveillance and control programs of SSI are well estab- lished in human hospitals. Despite all preventive meas- ures, it is estimated that SSI range from 2% to 5%, and remains a substantial cause of morbidity and mortality among hospitalized patients. 1–4 To our knowledge, few studies have evaluated risk factors for postoperative SSI in small animals 5–11 and most available information on risk factors associated with SSI originates from human surgical patients. Fac- tors generally considered as definite patient-associated determinants for SSI are extremes of age, morbid obesity, Address reprint requests to Dr. P. Boerlin, DrMedVet, Department of Pathobiology, University of Guelph, Guelph, ON, Canada N1G 2W1. E-mail: [email protected]. Dr. Boerlin’s current address is Department of Pathobiology, Ontario Veterinary College, University of Guelph, Canada. Submitted February 2003; Accepted June 2004 From the Divisions of Surgery and Internal Medicine, Companion Animal Hospital, Department for Clinical Veterinary Medicine and the Institute for Veterinary Bacteriology, University of Bern, Switzerland. r Copyright 2004 by The American College of Veterinary Surgeons 0161-3499/04 doi:10.1111/j.1532-950X.2004.04076.x 542 Veterinary Surgery 33:542–550, 2004

Est Prospectivo Infecciones Pos- Op 2004

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Page 1: Est Prospectivo Infecciones Pos- Op 2004

A Prospective Study of Postoperative Surgical Site Infections

in Dogs and Cats

SIMONE EUGSTER, DrMedVet, PETER SCHAWALDER Prof DrMedVet,FREDERIC GASCHEN, PD, DrMedVet, Diplomate ECVIM-CA & ACVIM, and PATRICK BOERLIN, Prof DrMedVet

Objective—To assess postoperative surgical site infection (SSI) rate and to identify associatedpredictive factors.Study Design—Prospective clinical study.Animals—Dogs and cats that had surgery (1010 interventions) during 58 weeks from April 1999 toJune 2000.Methods—Data sheets were completed by clinicians. Patients were controlled for clinical evidenceof SSI at suture removal. Two definitions of SSI (‘‘infection’’ and ‘‘infection/inflammation’’) weredeveloped specifically for this study and used for statistical analysis. Logistic regression models werebuilt in order to identify significant predictive factors for SSI.Results—Wounds with ‘‘infection/inflammation’’ occurred in 5.8% and ‘‘infected’’ wounds in 3%of patients. The outcome ‘‘infection’’ was associated with 3 major risk factors (duration of surgery,increasing number of persons in the operating room, dirty surgical site) and 1 protective factor(antimicrobial prophylaxis). The outcome ‘‘infection/inflammation’’ was associated with 6 signif-icant factors (duration of anesthesia, duration of postoperative intensive care unit stay, wounddrainage, increasing patient weight, dirty surgical site, and antimicrobial prophylaxis).Conclusions—SSI frequency in companion animals is comparable with the frequency observed inhuman surgical patients. Several significant predictive factors for SSI in small animals surgery wereidentified.Clinical Relevance—Baseline information for SSI surveillance in our hospital and for comparisonwith other studies was defined. The factors identified may help to predict infections in surgicalpatients and to take adequate preventive measures for patients at risk.r Copyright 2004 by The American College of Veterinary Surgeons

Key words: infection, surgery, wound, antimicrobial prophylaxis, cat, dog.

INTRODUCTION

NOSOCOMIAL INFECTIONS in general, andpostoperative surgical site infections (SSIs) in par-

ticular, are a growing concern in veterinary hospitals.Surveillance and control programs of SSI are well estab-lished in human hospitals. Despite all preventive meas-ures, it is estimated that SSI range from 2% to 5%, and

remains a substantial cause of morbidity and mortalityamong hospitalized patients.1–4

To our knowledge, few studies have evaluated riskfactors for postoperative SSI in small animals5–11 andmost available information on risk factors associatedwith SSI originates from human surgical patients. Fac-tors generally considered as definite patient-associateddeterminants for SSI are extremes of age, morbid obesity,

Address reprint requests to Dr. P. Boerlin, DrMedVet, Department of Pathobiology, University of Guelph, Guelph, ON, Canada

N1G 2W1. E-mail: [email protected].

Dr. Boerlin’s current address is Department of Pathobiology, Ontario Veterinary College, University of Guelph, Canada.

Submitted February 2003; Accepted June 2004

From the Divisions of Surgery and Internal Medicine, Companion Animal Hospital, Department for Clinical Veterinary Medicine

and the Institute for Veterinary Bacteriology, University of Bern, Switzerland.

r Copyright 2004 by The American College of Veterinary Surgeons

0161-3499/04

doi:10.1111/j.1532-950X.2004.04076.x

542

Veterinary Surgery

33:542–550, 2004

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remote infection, American Society of Anesthesiologists’preoperative assessment scores (ASA scores) of � 3, andprolonged preoperative hospitalization.1–4,12–14 A clearcorrelation between the 4 categories of wound contam-ination (clean, clean-contaminated, contaminated, anddirty) and SSI rate has been reported.2,10,12,15 Predictably,infection risk increases with increasing wound contami-nation.16 However, because of wide variation in infectionrates associated with different operative procedures with-in the same wound category, it is generally accepted thata risk stratification based on wound categories alone isinsufficient.

Culver et al.3 developed a risk index score to predict asurgical patient’s risk of acquiring SSI, which performssignificantly better across a broad range of surgical pro-cedures. This risk index score ranges from 0 to 3 andresults from a number of the following risk factors: (a)ASA score of 3, 4, or 5; (b) intervention classified as eithercontaminated or dirty; (c) intervention lasting over Thours, where T depends upon the surgical procedure be-ing performed. Definite procedure-related factors associ-ated with SSI are preoperative hair removal the daybefore surgery, duration of surgery, and antibiotic proph-ylaxis.1,4,7–9,12,17,18 Several other factors have remainedcontroversial as determinants of SSI and include: diabetesmellitus, malnutrition and low serum albumin, malignan-cy, immunosuppressive therapy, steroids, multiple opera-tive procedures during the same anesthesia, tissue trauma,foreign material, drains, and emergency surgery.1,12

Our objective was to define the postoperative SSI ratein our companion animal clinic to obtain baseline infor-mation for surveillance and for comparison with otherclinics. We also wanted to identify risk factors associatedwith SSI in dogs and cats.

MATERIALS AND METHODS

Study Design

Data were systematically collected from dogs and cats thathad a surgical procedure between April 26, 1999, and June 9,2000. All interventions were included except dental and oph-thalmic surgery, which were performed in a separate buildingand under different conditions than general surgery. Felinecastration was also excluded, because they are not routine inour clinic and wound closure and postintervention follow-upare usually different from other interventions. Procedures likeesophagostomy or chest tube placement that required a smallincision but needed subsequent wound closure or were per-formed in patients subsequently hospitalized for several dayswere included. A data sheet was included within the medicalrecord of every surgical patient when the animal was preparedfor anesthesia. The 1st part of the record covering the pre- andintraoperative period was completed by an anesthesiologist ortechnician monitoring the patient during anesthesia. The at-

tending clinician completed the 2nd part of the record cov-ering the postoperative period until patient discharge. Missinginformation was obtained retrospectively from the anesthesiaprotocols and surgery reports.

Surgical Preparation

The same aseptic preparation protocol was used for allpatients. After induction, surgical sites were clipped andscrubbed for 5 minutes with a povidone iodine detergent, thenthe patient was moved from the induction room to the op-erating room, and the surgical site was sprayed with a povi-done iodine solution just before draping. Patients had surgeryin one of 2 surgical suites: 1 suite equipped with a single sur-gery table was reserved for clean procedures, and the othersuite had 2 surgical tables where both clean and non-cleanprocedures were performed. Interventions not requiring en-tirely sterile conditions were occasionally performed in theinduction room. Cefalexin (20mg/kg intravenously; Rile-xines, Virbac, Carros, France) was administered prophylac-tically at induction for most clean and clean-contaminatedprocedures. Additional doses were administered every 3 hoursuntil the end of surgery. If infection was present (proceduresclassified as contaminated or dirty), antimicrobial agents spe-cific for that infection were administered.

Preparation of the surgeon and assistants included scrub-bing for 5 minutes with a 4% chlorhexidine detergent andwearing sterile impervious disposable paper gowns, latex sur-gical gloves, masks, and caps. Operating room personnel woremasks, caps, and washable cotton gowns at all times.

Data Collection

Recorded patient-related data was: dog or cat, sex (male,male castrated, female, female spayed), age in years (age o1year was coded as 0), body weight (kg), nutritional status(subjectively classified as obese, normal, thin, or cachectic),case origin (referred or directly admitted to the clinic), pre-operative hospital stay, and entire hospital stay in days. Pro-cedure data recorded were: interval preparation surgery inminutes (duration between time aseptic preparation was fin-ished and time of the 1st incision), duration of surgery inminutes (interval between 1st skin incision and final closure),type of anesthesia (general or local), patient ASA score (thisscore is representative of the patients physical status beforesurgery and ranges from 1 to 5, with 1 being an otherwisehealthy young patient and 5 being a moribund patient notexpected to survive surgery more than 1 day,19 emergency(yes/no), daytime (surgery performed during emergency hoursor during normal hospital working hours), traumatic insult(yes/no), number of surgical procedures performed on thesame patient during one anesthesia, operating room, maxi-mum number of persons in the room during surgery, presenceof students (yes/no), wound category (clean, clean-contami-nated, contaminated, dirty) classified by the attending surgeonaccording to the criteria established by the National ResearchCouncil (1964),20 placement of implant (yes/no), placement ofdrain (yes/no; drains were mostly open drains covered with a

543EUGSTER ET AL.

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sterile bandage inserted in a dedicated additional incision),presence of other disease which could potentially influencewound healing (e.g., endocrinopathy, neoplasia, polytrauma)or infection (either clearly purulent infection or infectionsconfirmed by bacteriological analysis) at a remote site (yes/no), use of pre- and intraoperative prophylactic antimicrobialagents from 2 hours before 1st skin incision to wound closure(yes/no), antimicrobial therapy before or after the procedure(yes/no, excluding pre- and intraoperative prophylactic anti-biotic administration), administration of dexamethasone dur-ing perioperative period (yes/no), duration of postoperativestay in the intensive care unit (ICU) in days (durations ofo24hours for routine postoperative recovery were not consideredas stay in the ICU), duration of anesthesia in minutes (intervalbetween induction to extubation).

Outcome

A hospital surgeon examined the patients at suture removalfor clinical evidence of inflammation or SSI. If the animal leftthe clinic before suture removal, the referring veterinarian wasinformed about the study and received a detailed list of criteriafor SSI evaluation. The hospital clinician or the referring vet-erinarian was contacted directly or by telephone to obtaininformation about the wound condition at suture removal. Ifthe referring veterinarian did not remove the sutures, theowner was contacted and interviewed directly by the principalinvestigator. Signs of infection registered for the local woundarea were redness, swelling, pain, heat, serous wound drain-age, purulent wound drainage, wound dehiscence, abscessa-tion, and fistulation.

Definition of SSI

Various definitions have been used for postoperative SSI inveterinary medicine.5–11 Therefore, based on the signs of in-fection listed above, we used 2 different definitions for post-operative SSI matched as closely as possible to those reportedpreviously. A wound was classified as ‘‘infected’’ if purulent

drainage, an abscess, or a fistula was recorded. A wound wasclassified as ‘‘infected/inflamed’’ when it was ‘‘infected’’ orwhen � 3 of the following signs were present simultaneously:redness, swelling, pain, heat, serous discharge, and wounddehiscence. Rectal temperature measurements during thepostoperative period were not included in these 2 definitions,because this variable was frequently not recorded. Moreover,2 previous veterinary studies did not detect an associationbetween increased postoperative rectal temperature and de-velopment of a local SSI.10,11

Statistical Methods

All statistical analyses were performed using computersoftware (Statistix for Windowss, Analytical Software,Tallahassee, FL, and MedCalc 5s, MedCalc Software, Mar-iakerke, Belgium). When animals had several interventions atdifferent dates, each intervention was recorded as a separatesurgery and the interventions were considered independentlyfor statistical evaluation. Associations between qualitativevariables were tested using w2 tests or Fisher’s exact tests asappropriate. Associations of quantitative data with the out-comes (‘‘infection’’ and ‘‘infection/inflammation’’) were testedusing Mann–Whitney rank sum test. The Armitage test fortrend was used for the analysis of associations between ASAscores or wound categories and outcomes. A logistic regres-sion analysis was performed using a manual stepwise back-ward elimination procedure starting with all the risk factorshaving a P-value � 25% in the univariate analysis. The elim-ination procedures were stopped when the P-value for allvariables in the model was o10%. The Walter’s hierarchicalcoding method was used for the ordinal variables ASA scoresand wound category.21 To maximize the power of the un-ivariate analyses, all available subjects for which the corre-sponding dependent and independent variables had beenrecorded were used. Consequently, the number of patientsanalyzed and reported in the results section may vary fromone variable to another (Tables 1–3). For the multivariateanalyses, only patients with complete data records for the

Table 1. Distribution of Patients and Intervention Characteristics (Qualitative)

Species (n¼ 945) (%) Cats: 29.7 Dogs: 70.3

Sex (n¼ 944) (%) Females: 28.6 Spayed females: 21.6 Males: 33.6 Castrated males: 16.2

Nutritional status (n¼ 836) (%) Obese: 13.4 Normal: 81.0 Thin: 5.3 Cachectic: 0.4

Origin (n¼ 945) (%) Direct: 35.6 Referred: 64.4

Emergency hours intervention (n¼ 836) (%) Yes: 9.2 No: 90.8

Traumatic insult (n¼ 836) (%) Yes: 32.4 No: 67.6

ASA score (n¼ 814) (%) 1: 25.9 2: 38.8 3: 25.8 4 and 5: 9.5

Other disease (n¼ 836) (%) Yes: 16.7 No: 83.3

Wound category (n¼ 836) (%) Clean: 70.8 Clean–contaminated: 13.4 Contaminated: 10.4 Dirty: 5.4

Type of anesthesia (n¼ 836) (%) General: 99.8 Local: 0.2

Implant (n¼ 836) (%) Yes: 33.9 No: 66.1

Drain (n¼ 834) (%) Yes: 8.3 No: 91.7

Operation room (n¼ 836) (%) Clean room: 39.8 Second room: 57.1 Induction room: 3.1

Undergraduate students (n¼ 833) (%) Present: 50.7 Absent: 49.3%

Preoperative antimicrobial treatment (n¼ 834) (%) Yes: 25.1 No: 74.9

Antimicrobial prophylaxis (n¼ 836) (%) Yes: 93.2 No: 6.8

Postoperative antimicrobial treatment (n¼ 835) (%) Yes: 77.5 No: 22.5

Immunosuppression or cytostatics (n¼ 836) (%) Yes: 8.3 No: 91.7

544 SURGICAL SITE INFECTIONS IN DOGS AND CATS

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variables used at the start of the backward elimination pro-cedure were used for the analysis.

RESULTS

Patient Population

Data from 1010 procedures performed on 735 animalswere studied. Complete records including data on signs ofinflammation or infection were obtained from 712(70.5%) interventions. The distribution of the variablesrecorded and used for statistical analysis (Tables 1 and 2)and use of antimicrobial agents (Table 3) are provided.

SSIs and Associated Factors

Suture removal was performed by a hospital surgeon(52% of patients), referring veterinarian (38%), or theowner (10%). Surgical sites were classified as ‘‘infected/inflamed’’ (55 of 946; 5.8%) or as ‘‘infected’’ (28; 3.0%)Variables having an association with the development ofSSI are listed in Table 4. Factors significantly associatedwith ‘‘infection/inflammation’’ (Po.05) had the sametrend for ‘‘infections,’’ but mostly at a non-significantlevel. This lack of power most probably resulted from therelatively low number of cases with ‘‘infection.’’ Heavierbody weight was significantly associated with postoper-ative SSI in dogs (P¼ .009) but not in cats. A significant

increase for risk of infection with increasing wound con-tamination in the ‘‘infection/inflammation’’ group wasobserved (Table 5). A similar trend was visible for the‘‘infected’’ wounds but because of the low number ofpositive cases (n¼ 23), this association was not statisti-cally significant. An increasing ASA score was alsosignificantly associated with both ‘‘infection’’ and ‘‘infec-tion/inflammation’’ (Table 6). Pre- and postoperative ad-ministrations of antimicrobials were associated with anincreased frequency of SSI. Antimicrobial prophylaxisseemed to give some protection against surgical woundinfections but the very low numbers of animals withoutprophylaxis together with the relatively low frequency ofinfection did not result in a statistically significant effectat the univariate level.

Several other statistically non-significant trends werealso apparent. For instance, the duration of the postop-erative stay in the ICU, as well as duration of patientsurgical preparation, of surgery, and anesthesia seemedassociated with higher frequencies of postoperative SSI.The number of persons in the operating room and thepresence of another disease can be considered similarly.Finally, duration of postoperative hospitalization andtotal hospitalization were both significantly associatedwith postoperative ‘‘infections/inflammation’’ at the un-ivariate level (Po.030). Median duration of postopera-tive stay with no infection was 2 days (mean 3 days; 1stquartile, 1 day; 3rd quartile, 4 days), whereas median

Table 2. Distribution of Patients and Intervention Characteristics (Quantitative)

Median (Average) Minimum–Maximum 1st–3rd Quartiles

Age of dogs in years (n¼ 659) 5.0 (5.1) 0.1–15.0 2.0–8.0

Age in years for cats (n¼ 270) 2.0 (3.4) 0.2–17.0 1.0–5.0

Weight of dogs in kg (n¼ 621) 27.0 (25.7) 1.2–85.0 11.0–35.0

Weight of cats in kg (n¼ 249) 4.0 (3.9) 1.2–9.0 3.0–4.5

Duration of preparation in minutes (n¼ 834) 20 (22) 0–245 15–25

Duration of surgical intervention in minutes (n¼ 835) 90 (98) 7–380 60–130

Duration of anesthesia in minutes (n¼ 869) 165 (171) 20–480 115–220

Number of simultaneous surgical procedures (n¼ 872) 1 (1.1) 1–6 1–1

Number of persons in operation room (n¼ 759) 5 (5.5) 2–18 4–6

Duration of preoperative stay in days (n¼ 835) 1 (1.6) 0–29 0–1

Duration of postoperative stay in days (n¼ 820) 2 (3.2) 0–30 1–4

Duration of stay in ICU in days (n¼ 832) 1 (1.2) 0–17 0–1

Duration of hospital stay in days (n¼ 820) 3 (4.7) 0–41 1–6

Time between surgical intervention and suture removal in days (n¼ 930) 11 (11.5) 2–29 10–12

Table 3. Use of Antimicrobial Agents in Relation with Wound Category

Antimicrobial Use

Wound Category

Clean Clean–Contaminated Contaminated Dirty

Preoperative 15.6% (n¼ 590) 28.6% (n¼ 112) 60.9% (n¼ 87) 71.1% (n¼ 45)

Perioperative (prophylaxis) 92.2% (n¼ 592) 96.4% (n¼ 112) 95.4% (n¼ 87) 93.3% (n¼ 45)

Postoperative 69.7% (n¼ 591) 92.9% (n¼ 112) 98.9% (n¼ 87) 100% (n¼ 45)

n, number of patients in the corresponding category with available data on antimicrobial use.

545EUGSTER ET AL.

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duration of postoperative stay for patients with an ‘‘in-fection’’ or with ‘‘infection/inflammation’’ was 4 days(mean 6 days; 1st quartile, 1 day; 3rd quartile 8 days for‘‘infection’’ and mean 7 days; 1st quartile, 1 day; 3rdquartile, 10 days; for ‘‘infection/inflammation’’). No as-sociation or trend was observed between development ofSSI in animals and the other factors studied.

Multivariate Analysis

A 1st multivariate model was built for the outcome‘‘infection’’ using the starting variables indicated in Table4 and the 712 interventions with complete data sets for

these variables. Animal species was forced into the model(kept in the model at all stages of the procedure despitelack of statistical significance) because it was consideredan important factor with strong influences on the char-acteristics of the surgical interventions. The ASA scoreswere also forced into the model because in human med-icine they are known to be a major risk indicator fordevelopment of SSI. The variables remaining at the endof the backward elimination procedure and the corre-sponding odds ratios for the final model are listed inTable 7. Ninety-seven percent of the cases were correctlyclassified by this model and the Hosmer–Lemeshow sta-tistic was 3.76 (P¼ .88), thus indicating a good fit of themodel to the actual observations.

A 2nd multivariate model was built for the outcome‘‘infection/inflammation’’ using the starting variables list-ed in Table 1 and the 778 interventions with completedata sets for these variables. As for the 1st model, theanimal species and ASA scores were forced into themodel. Despite their lack of significance at the univariatelevel, antimicrobial prophylaxis and personnel were alsoincluded as starting variables for the backward elimina-tion procedure, because of their high significance in the

Table 4. Factors Associated with Postoperative Surgical Site Infections

(Univariate Level)

P-Value

Infection�Infection/

Inflammation�

Weight in dogs (risk)w .051k .009kWeight in cats (risk)w .436k .127kSurgical site category (see Table 5)z .161k .002kASA score (see Table 3)y .043k .050kOther simultaneous disease/infection (risk)z .223k .303

Antimicrobial pretreatment (risk)z .038k .131kPre- and intraoperative antimicrobial

prophylaxis (protective)z.202k .377k

Antimicrobial postoperative treatment (risk)z .266 .028kOperating roomz .080k .332

Number of persons present during

intervention (risk)w.107k .824k

Duration of patient preparation (risk)w .114k .152kDuration of anesthesia (risk)w .251 .193kDuration of surgical intervention (risk)w .160k .183kDuration of postoperative stay in ICU (risk)w .542 .079kPlacement of a drain (risk)z .100k o.001k

ASA, anesthesiologists’ preoperative assessment.�For definition, see Materials and Methods section.

wMann–Whitney test.

zw2-test.yArmitage test for trend.

zFisher’s exact test; Only variables with P-values equal or smaller than

.25 are included in the list.

kThese variables were used as starting variables for the backward

elimination procedures in the logistic regression models.

Table 5. Percentage of Wounds with Signs of Infection in Relation to

Wound Categories

Clean

(%)

Clean-

Contaminated

(%)

Contami-

nated

(%)

Dirty

(%) P-Valuew

Infection� 2.0 3.5 4.6 6.7 .161

Infection/inflammation� 4.9 4.5 9.1 17.8 .002

�For definition, see Materials and Methods.

wP-value obtained with Armitage test for trend.

Table 6. Percentage of Infections in Relation to ASA Scores

ASA Scores

P-ValuewI

(%)

II

(%)

III

(%)

IV

(%)

V

(%)

Infection� 1.5 2.9 3.4 5.6 0.0 .043

Infection/inflammation� 4.4 5.6 7.9 8.3 0.0 .050

ASA, anesthesiologists’ preoperative assessment.�For definitions, see Materials and Methods.

wP-value obtained with Armitage test for trend using the categories

I–V (since only one case had a score of V, the categories IV and V were

pooled together).

Table 7. Variables Associated with Surgical Site ‘‘Infections’’ in a

Logistic Regression Model

Predictor

Odds Ratio

(95% CI) P-Value

Duration of surgical intervention

(minutes)

1.01 (1.00–1.02)� .001

Number of persons present

during intervention

1.30 (1.03–1.64)� .026

Dirty wound 5.56 (1.39–22.24 .015

Antimicrobial prophylaxis 0.15 (0.03–0.88) .035

The variables animal species and anesthesiologists’ preoperative as-

sessment scores were forced into the model but remained non-significant

at the end of the elimination procedure and are not shown in this table.�For each additional minute of surgical intervention, the animal is

1.01 times more likely to have an ‘‘infection’’ and for each additional

person in the operating room, the animal is 1.3 times more likely to have

an ‘‘infection.’’

546 SURGICAL SITE INFECTIONS IN DOGS AND CATS

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1st model. The remaining variables and the correspond-ing odds ratios for the final model at the end of the pro-cedure are summarized in Table 8. The Hosmer–Lemeshow statistic for this model was 9.64 (P¼ .29)and is indicative of a not completely satisfactory fit of themodel to the actual observations; however, 94% of thecases were correctly classified by this model.

DISCUSSION

Infection Rate

The 5.8% rate for surgical sites identified as ‘‘infected/inflamed,’’ we found, is similar to previous reports.6,7,9,10

Using a case definition including purulent discharge andsigns of local inflammation, Vasseur et al.10 reported aninfection rate of 5.1% in a retrospective study. If weconsider only surgical sites with an ‘‘infection,’’ our in-fection rate was 3.0%, which is lower than 5.5% reportedin a prospective study by Brown et al.7 using a similardefinition (wounds with purulent discharge). Similarly,the infection rate observed here for clean-contaminatedwounds is lower than reported by Nicholson et al.9 Thesediscrepancies are probably indicative of different patientpopulations and/or of different inclusion criteria, or of apossible bias introduced by patients with incompleterecords in our study.

Risk and Protection Factors for SSIs

To control for confounding effects between the nu-merous variables studied at the univariate level, multi-variate logistic regression models were built for the2 outcomes ‘‘infection’’ and ‘‘obvious infection.’’ Usingthis comprehensive approach, important changes were

observed in the predictive value of different potential riskand protective factors. ASA scores were forced into thesemodels, because they represent definite predictive indica-tors for SSI in humans and are part of a relatively ac-curate risk stratification index system for SSI in humansurgery across a broad range of surgical procedures.1,3,22

Moreover, results from our univariate analysis showedthat an increasing ASA score was significantly related toa higher risk for both ‘‘infection’’ and ‘‘infection/inflam-mation.’’ Four major predictive variables for SSI wereidentified in our logistic regression model when using thedefinition of ‘‘infection’’ as an outcome.

Our results concur with studies of human SSI, whereduration of intervention represents an important riskfactor.1,3,4,22 In our model risk of ‘‘infection’’ increased1.01 times for each additional minute of surgery, whichcorresponds to doubling the risk of infection approxi-mately every 70 minutes. Relatively similar results werereported in another prospective veterinary study wherethe risk for postoperative wound infection was estimatedto double if the procedure took 90 minutes comparedwith a surgical time of 60 minutes.7 However, anotherreport did not find any significant association betweendevelopment of an infection and duration of the inter-vention.11 The lower sample size (112 patients) comparedwith our study (712) and Brown et al. (1255) may havecontributed to this lack of significance. Thus, duration ofsurgical intervention must be regarded as an importantpredictive factor for SSI not only in human, but also insmall animal surgery.

For each additional person in the surgical suite, therisk of SSI was 1.3 times higher. Reports on this factorare sparse, and it is not explicitly reported as a major riskfactor for SSI. To our knowledge, no other veterinarystudy has examined this variable. It is possible that thenumber of persons in the operating room could be anindicator of another risk factor, although except forASA-scores, no correlation with other variables recordedwas observed. Because ASA-scores were forced into themultivariate models, their effect was accounted for andwould not be expected to be additionally reflected againin the number of persons in the operating room. In ad-dition, no clear trend was visible between the type ofinterventions associated with large or small numbers ofpersons in the room, and the effect of surgery complexityis partially accounted for in our final model by the du-ration of the operation. Finally, the consequences of anincreasing number of persons on contamination of thewound in a clean surgical suite with numerous asepticmanipulations are quite obvious.4,23 Therefore, a limita-tion on personnel in the operating room is still a validrecommendation for a reduction of SSI frequency.4

The presence of a surgical site classified as ‘‘dirty’’ wasa highly predictive risk factor for ‘‘infection’’ as well as

Table 8. Variables Associated with Postoperative Surgical site ‘‘Infec-

tion/Inflammation’’ in a Logistic Regression Model

Predictor

Odds Ratio

(95% CI) P-Value

Dirty wound 3.56 (1.27–9.98) .016

Antimicrobial prophylaxis 0.26 (0.09–0.82) .021

Duration of anesthesia (minutes) 1.004 (1.00–1.01)� .067

Duration of postoperative

stay in ICU (days)

1.16 (1.03–1.30)� .011

Presence of drain 2.64 (1.05–6.65) .039

Weight of animal (kg) 1.03 (1.01–1.05)� .014

The variables animal species and anesthesiologists’ preoperative as-

sessment scores were forced into the model but remained non-significant

at the end of the elimination procedure and are not shown in this table.�For each additional minute of anesthesia, the animal is 1.004 times

more likely to have an ‘‘infection/inflammation,’’ for each additional day

spent in the intensive care unit, the animal is 1.16 times more likely to have

an ‘‘infection/inflammation,’’ and for each additional kilogram of weight,

the animal is 1.03 more likely to have an ‘‘infection/inflammation.’’

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for ‘‘infection/inflammation’’ in our multivariate analy-ses. No association between postoperative SSI and theother wound classes was identified with the multivariateregression model. Nevertheless, univariate analysis dem-onstrated an increasing surgical site class as a significantrisk factor for ‘‘infection/inflammation’’ and showed aclear but not significant trend for ‘‘infection.’’ Our resultsare in full agreement with previous human and veterinarydata with regard to this risk factor,2,10,12 but, as previ-ously discussed, risk stratification based on wound cat-egories alone remains a moderately predictive factor forSSI because of its failure to account for intrinsic patientrisk.3, 7,10,24

Despite the relatively small number of patients notadministered antimicrobials in our study, the multivariatestatistical models for ‘‘infection’’ as well as for ‘‘infection/inflammation’’ showed that pre- and intraoperative an-timicrobial prophylaxis represents an important protec-tive factor against SSI. Patients administeredantimicrobial prophylaxis were on average 6–7 times lesslikely to develop SSI than patients without prophylaxis.Administration of prophylactic antibiotics seems routinefor clean-contaminated procedures and for most cleaninterventions in human surgery.14,18 The objective ofprophylactic treatment is to reduce intraoperative bacte-rial contamination below the critical level needed to in-duce an infection and is not intended to preventpostoperative contamination.

In their guidelines for prevention of SSI, Mangramet al.14 recommend the use of pre- and intraoperativeantimicrobial prophylaxis for all clean-contaminated pro-cedures and for clean procedures when SSI would be amajor threat for the patient, as well as for those proce-dures where a prosthetic joint or any intravascular pros-thetic material will be inserted. Few studies on use ofantimicrobial prophylaxis for clean procedures have beenreported in veterinary medicine. Vasseur et al.10 reporteda significantly lower infection rate if prophylactic antibi-otics were administrated and surgical duration exceeded90 minutes, but not for a shorter surgical time. For elec-tive orthopedic surgery, Whittem et al.11 also reported asignificantly higher infection rate in dogs administeredsaline solution rather than prophylactic antibiotics 30minutes before surgery. In another prospective reportwith a standardized protocol for perioperative adminis-tration of antimicrobial agents, no significant associationbetween administration of antimicrobial prophylaxis andthe SSI rate was identified.7 However, as mentionedabove, the populations under investigation in these stud-ies may differ substantially, in particular with respect topatients with clean surgical sites.

The association of ‘‘dirty’’ surgical sites and antimi-crobial prophylaxis with the outcome ‘‘infection/inflam-mation’’ in our 2nd logistic regression model were slightly

weaker than in the 1st model. This reflects the fact thatthe case definition for ‘‘infection/inflammation’’ wasprobably less specific than the case definition for ‘‘infec-tion.’’ Duration of anesthesia rather than duration ofsurgery was significantly associated with the outcome inthe 2nd model. Because both variables are clearly corre-lated (Pearson’s correlation coefficient¼ 0.86), it may bedifficult to decipher the exact role of each factor. Ourresults related to duration of anesthesia are in closeagreement with those of Beal et al.5 and coworkers wherethere was a 30% increase in risk of SSI in clean woundsfor each additional hour of anesthesia. There are someobvious biological reasons for the role of a prolongedanesthesia as a predisposing factor for SSI. These includeperioperative hypothermia leading to impairment ofphagocytic function, and hypotension or hypoxia, whichmay result in reduced perfusion and oxygenation ofwound tissue with similar consequences and diminishedtissue regeneration.14,25,26

In our study, 3.1% of the patients hospitalized in ICUdeveloped an ‘‘infection’’ and 6.1% developed an ‘‘infec-tion/inflammation.’’ From the 2nd logistic regressionmodel for each additional day spent in ICU, patientswere 1.16 times more likely to develop an ‘‘infection/in-flammation.’’ In human hospitals � 20% of nosocomialinfections occur in ICUs, and surgical ICU patients are atthe greatest risk.27 One study yielded an SSI rate of 1% ofadmissions in ICU patients whereas in an earlier studySSI rate was 16.6%, both higher than the overall humanSSI rate (2–5%).27,28 Because of the debilitation of ICUpatients and increased contamination pressure by oftenmultiresistant microorganisms through invasive devices,nosocomial infections are a general problem in ICUs.Such problems are already present in veterinary ICUsand may have to be controlled more tightly in veterinarymedicine also.29,30 Use of a drain is associated with anincreased risk of wound infection because foreign mate-rials reduce the number of microorganisms required forinfection by 10,000-fold.14,31,32 However, drains are also asource of local inflammation, which may have been clas-sified as ‘‘infection/inflammation’’ in our study. There-fore, any association of drain and infection identified herehas to be interpreted with caution and may be less strongthan suggested by an odds ratio of 2.6.

Heavier animals were seemingly significantly more atrisk for infection than smaller animals. Previous humanand veterinary studies have reported that morbid obesityand malnutrition predispose to SSI.1,4,10,14 However, thenutritional status of our patients was not associated withinfection and does not account for an association be-tween weight and ‘‘infection/inflammation.’’ Possible dif-ferences in behavior between large and small breeds ormore frequent inflammation signs in large breeds (mis-interpreted as infection) because of a more intense

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mechanical stress on surgical wounds in these heavy,stronger animals may be responsible for the observed as-sociation between weight and ‘‘infection/inflammation.’’

Some variables significantly associated with the devel-opment of infection in the univariate analysis were theincreasing duration of postoperative hospital stay andshortening of the interval between surgery and suture re-moval. These factors are clear indicators of the increasedcare needed by patients with SSI and of the associatedcosts.

Our results allow a 1st estimation of the SSI rate in ourcompanion animal hospital and are broadly comparablewith data reported from other veterinary hospitals. Wewere able to define some highly predictive factors for SSIin dogs and cats. The logistic regression models we de-veloped may represent a useful tool for surgeons in mak-ing decisions on the necessity of additional preventivemeasures in patients at a high risk for developing post-operative SSI. Surveillance programs should be imple-mented to follow the evolution of nosocomial infectionsin veterinary medicine. Our methodology using chart re-views and postdischarge surveillance has been shown asone of the most effective methods for detection of SSI inhuman hospitals.33 However, it is very tedious, labor in-tensive, and difficult to implement for routine surveil-lance, particularly in veterinary medicine. Unfortunately,surveillance based on microbial analysis submissions ismuch less sensitive. Thus, an approach between effectivesurveillance using simplified charts combined with elec-tive microbial analysis specifically adapted to veterinaryclinics still needs to be found. Our study represents anadditional step in this direction.

ACKNOWLEDGMENTS

The authors wish to thank all clinicians and technicians of

the Companion Animal Hospital, who patiently completed

the data record sheets during the study. We are also very

thankful to S. McEwen and R. Reid-Smith for reading the

manuscript and for their helpful suggestions.

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