Retrospective study of factors associated with surgical site infection in dogs following tibial plateau leveling osteotomy

Daniel J. Lopez Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY 14850.

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Gretchen M. VanDeventer Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY 14850.

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Ursula Krotscheck Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY 14850.

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Yazdan Aryazand Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY 14850.

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Marina J. McConkey Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY 14850.

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Kei Hayashi Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY 14850.

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Rory J. Todhunter Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY 14850.

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Galina M. Hayes Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY 14850.

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Abstract

OBJECTIVE To identify risk factors associated with surgical site infection (SSI) in dogs following tibial plateau leveling osteotomy (TPLO).

DESIGN Retrospective cohort study.

ANIMALS 320 dogs that underwent unilateral or bilateral TPLO (n = 405 procedures) between 2007 and 2015 and were reexamined by a veterinarian at least once ≥ 8 weeks after the procedure.

PROCEDURES Data were extracted from medical records regarding signalment, TPLO procedure details, medical history of dermatitis, and SSI status. Logistic regression was performed to identify factors associated with SSI development.

RESULTS An SSI developed following 34 (8.4%; 95% confidence interval [CI], 6.1% to 11.5%) procedures. Prophylactic antimicrobial administration was provided following 36.8% (n = 149) of procedures. For 71 (17.5%) procedures, the dog had dermatitis at the time of surgery; 12 of these procedures involved dermatitis at the surgical site. The incidence of SSI following the 12 procedures for dogs with dermatitis at the surgical site was 16.7% (2/12 [95% CI, 3.3% to 54.3%]) and was 10.2% (6/59 [95% CI, 4.5% to 21.3%]) for dogs with dermatitis elsewhere; however, these differences in incidence were not significant. On multivariable analysis, German Shepherd Dogs (vs other breeds), meniscectomy (vs no meniscectomy), and attending surgeon having performed ≤ 20 (vs > 20) procedures during the study period were associated with increased odds of SSI.

CONCLUSIONS AND CLINICAL RELEVANCE SSI following TPLO was associated with the German Shepherd breed, meniscectomy, and surgeon. Prospective studies are needed to investigate the mechanisms underlying these associations.

Abstract

OBJECTIVE To identify risk factors associated with surgical site infection (SSI) in dogs following tibial plateau leveling osteotomy (TPLO).

DESIGN Retrospective cohort study.

ANIMALS 320 dogs that underwent unilateral or bilateral TPLO (n = 405 procedures) between 2007 and 2015 and were reexamined by a veterinarian at least once ≥ 8 weeks after the procedure.

PROCEDURES Data were extracted from medical records regarding signalment, TPLO procedure details, medical history of dermatitis, and SSI status. Logistic regression was performed to identify factors associated with SSI development.

RESULTS An SSI developed following 34 (8.4%; 95% confidence interval [CI], 6.1% to 11.5%) procedures. Prophylactic antimicrobial administration was provided following 36.8% (n = 149) of procedures. For 71 (17.5%) procedures, the dog had dermatitis at the time of surgery; 12 of these procedures involved dermatitis at the surgical site. The incidence of SSI following the 12 procedures for dogs with dermatitis at the surgical site was 16.7% (2/12 [95% CI, 3.3% to 54.3%]) and was 10.2% (6/59 [95% CI, 4.5% to 21.3%]) for dogs with dermatitis elsewhere; however, these differences in incidence were not significant. On multivariable analysis, German Shepherd Dogs (vs other breeds), meniscectomy (vs no meniscectomy), and attending surgeon having performed ≤ 20 (vs > 20) procedures during the study period were associated with increased odds of SSI.

CONCLUSIONS AND CLINICAL RELEVANCE SSI following TPLO was associated with the German Shepherd breed, meniscectomy, and surgeon. Prospective studies are needed to investigate the mechanisms underlying these associations.

The TPLO technique is commonly used for the treatment of cranial cruciate ligament disease in dogs.1 Surgical site infections are of specific concern with this procedure owing to the increased risk of infection associated with the orthopedic implants.2 The incidence of TPLO-associated infections reportedly ranges from 2.5% to 15.8%,3–10 and the incidence of implant removal because of such infections is reportedly 3.5% to 7.4%.8,9 The impacts of SSI (vs no SSI) in dogs are many, including greater postoperative pain, greater financial cost to the client, more hospital visits, and, possibly, poorer long-term outcome.11

Several risk factors have been associated with postoperative SSIs in dogs and cats, including hypotension, timing of preoperative clipping, prolonged duration of anesthesia and surgery, sex of the patient, number of personnel in the operating room, type of surgery, use of propofol for anesthetic induction, use of skin staples, and presence of concurrent endocrinopathy.2,7,12–18

Studies3,9,10,19,20 focused specifically on the TPLO technique and SSIs in dogs have revealed additional risk factors for SSI, including the type of surgical implant used, high (vs low) body weight, sexually intact male reproductive status, preoperative colonization with methicillin-resistant Staphylococcus pseudintermedius in the nares or rectum, and Bulldog (vs Airedale Terrier) breed. Reported factors with a protective association against development of a post-TPLO SSI include the use of a locking TPLO plate in dogs weighing > 50 kg (110 lb) and Labrador Retriever breed.3,21 In a multi-institutional study,20 hospital of TPLO performance was associated with SSI development, although the underlying factors were not determined. Most studies3,4,7,14,18–23 have shown that prophylactic postoperative antimicrobial administration protects against SSI development, whereas one study24 revealed no significant benefit and another study25 revealed a benefit only in conjunction with surgeon experience or procedure duration.

When a dog requiring TPLO has active dermatitis at or near the surgical site, surgeons typically recommend to owners that the dermatitis be treated and the surgery delayed until the dermatitis has resolved. However, surgeons differ in the severity of the dermatitis and proximity to the surgical site that would prompt them to suggest delaying surgery. For skin infections identified late in the course of evaluation (eg, during clipping of the surgical site when the patient is anesthetized), delaying surgery can result in an increase in the total cost to the owner and additional hospital visits, making some owners reluctant to accept such recommendations.

Studies26,27 have shown a possible link between historical or preoperative dermatitis and postoperative SSI in humans, with a prospective study26 yielding a hazard ratio of 3.4 for deep SSIs and infection-related death independent of other factors. However, another study28 revealed no association between the bacterial load on a patient's skin before or after scrubbing and SSI development following craniotomy. Several studies7,10,16,20 have been conducted to evaluate associations between the presence of dermatitis and postoperative SSIs as secondary objectives, albeit with low case numbers. However to the authors' knowledge, no significant association between these variables has been reported in the veterinary literature. The primary objectives of the retrospective study reported here were to investigate putative risk factors for associations with SSI development following TPLO in dogs at the authors' hospital and to determine whether preoperative dermatitis was associated with increased risk of SSI development in these dogs.

Materials and Methods

Dogs

The study was designed as a retrospective cohort study involving dogs that underwent a TPLO procedure (unilateral and simultaneous or staged bilateral) at the Cornell University Hospital for Animals between March 1, 2007, and June 30, 2015. A search of the electronic medical records was performed to identify TPLO procedures performed in dogs during this period. A TPLO procedure was excluded from the study when the medical record indicated the dog had concurrently undergone additional orthopedic procedures (eg, wedge resection) or if the record lacked adequate follow-up information, defined as documented reexamination by a veterinarian at least once > 8 weeks after the procedure. A TPLO procedure was not excluded if minor soft tissue procedures, such as neutering or simple mass removal, had been concurrently performed at anatomic sites distant from the primary surgical site. All medical records and communication logs for the associated dogs were evaluated at a minimum of 1 year after the TPLO procedure. The TPLO procedures had all been performed or directly supervised by a board-certified surgeon or senior resident.

Data collection

Data pertaining to each dog were derived from the medical records and included breed, sex and reproductive status, age, date of TPLO procedure (including month, season, and year), body weight, age at time of surgery, duration of hospitalization, affected limb (left or right hind limb), whether a simultaneous bilateral procedure had been performed, interval since previous TPLO surgery (if applicable), chief surgeon, surgical resident, additional analgesia provided (eg, femoral, sciatic, or epidural blocks), surgical approach (arthrotomy or arthroscopy), condition of the cranial cruciate ligament, whether a meniscectomy had been performed, size and weight of TPLO plate, durations of anesthesia and surgery, time required to obtain postoperative radiographs, whether appropriate perioperative antimicrobials had been administered (as judged per standard guidelines19), minimum and maximum intraoperative esophageal temperature and arterial blood pressure, whether there was any medical history of skin infections, whether there was any perioperative skin infection and its location, whether an SSI developed after surgery, time to SSI development (if applicable), results of microbial culture of implants (if performed), and time to implant removal (if performed). Hypotension was defined as mean arterial blood pressure < 65 mm Hg. Hypothermia was defined as an esophageal temperature < 36.7°C (98°F).

SSI—Surgical site infections were defined in the study on the basis of criteria adapted from the CDC, excluding the associated timelines and diagnosis by physical examination alone.29 Two investigators (DJL and GMV) used these definitions and the medical record data when determining whether an SSI had developed. An SSI was categorized as superficial if it involved only skin or subcutaneous tissues at the site of the incision and met at least one of the following criteria: superficial, purulent drainage; responsible organism identified; or opening of the incision, with signs of pain, localized swelling, erythema, or heat, unless microbial culture yielded a negative result, in which case this last criterion was negated. An SSI was categorized as deep if it involved the deep soft tissue around the incision or implant and met at least one of the following criteria: deep purulent drainage, deep spontaneous dehiscence, identification of organisms via diagnostic samples obtained during surgical exploration, pyrexia (> 38°C [100.4°F]), signs of localized pain, or signs of tenderness, unless microbial culture yielded a negative result, in which case this last criterion was negated. An SSI was categorized as within an organ or space if the affected organ or space (eg, stifle joint) had been opened or manipulated during surgery and the infection met at least one of the following criteria: purulent drainage, identification of the infecting organism, or evidence of infection on gross anatomic or histologic examination.

The CDC timeframe associated with each SSI category definition was not adhered to because of the lack of a formal SSI surveillance program at our hospital and the potential delay in owners recognizing or reporting clinical signs associated with deep implant infections, such as decreased use of the limb or draining tracts. Diagnoses of SSIs made solely on the basis of findings of physical examination as performed by a surgeon or attending physician were also excluded owing to the overlap of clinical signs between inflammation and true infection, which we believed were inseparable given the retrospective data that lacked results of objective microbial culture or cytologic evaluation.

Appropriate antimicrobial administration—Appropriateness of antimicrobial administration was determined for each procedure on the basis of whether the antimicrobial (cefazolina) was administered from 1 to 60 minutes prior to the start of surgery, cefazolin was administered at a dose > 20 mg/kg (9.1 mg/1b), and cefazolin was readministered at a minimum interval of 120 minutes for the duration of the procedure.2,14,30,31 Failure to meet any of these 3 criteria was considered inadequate perioperative antimicrobial administration.

Historical and preoperative infections—History of dermatitis was defined for study purposes as a record of previous dermatitis, otitis externa, atopy, previous SSI, flea infestation, or owner-reported acral lick dermatitis. Perioperative dermatitis was defined as a diagnosis of dermatitis of any sort (eg, papules, pustules, or collarettes), otitis externa, or flea infestation at the time of surgery. Perioperative surgical site dermatitis was defined as dermatitis anywhere on the surgically treated limb, not including the inguinal and ventral abdominal regions, and not restricted to the draped surgical field. If dermatitis was documented on initial examination, an empirical course of antimicrobial treatment (generally cephalexin at 22 to 30 mg/kg [10 to 13.6 mg/lb], q 8 or 12 h for 2 weeks or 1 week past resolution of clinical signs) was prescribed at the discretion of the primary surgeon, and dogs were discharged from the hospital with instructions to have the dog reevaluated by either the referring veterinarian or the admitting clinician to ensure resolution of dermatitis prior to surgery. Occasionally, perioperative surgical site dermatitis was not noted until after preanesthetic sedation or anesthetic induction, at which point the supervising surgeon would have recommended delaying surgery until resolution of the dermatitis through antimicrobial treatment. However, on a case-by-case basis and dependent on the level of concern of the individual surgeon involved, some owners would have been given the option to proceed with surgery or would have requested to proceed with surgery despite active dermatitis.

Postoperative antimicrobial administration—Prophylactic postoperative antimicrobial administration was defined as the administration of antimicrobials in the immediate postoperative period, extending beyond the date of discharge from the hospital, for which no specific indication for antimicrobial use was identified in the medical record. Such practice varied within the study period. During the initial period, typical practice included prophylactic administration of antimicrobials for several days after surgery. Toward the middle to end of the study period, postoperative prophylactic antimicrobial administration was prescribed only if the dog regurgitated while anesthetized, intraoperative sterility was broken, a preoperative skin infection was present, or immediate revision of the surgery was required. No hospital guidelines for antimicrobial choice or duration were in place during the study period; therefore, duration of prophylactic antimicrobial administration was surgeon dependent. The common antimicrobial of choice was cephalexin administered at 22 to 30 mg/kg, PO, q 8 or 12 hours, for 5 days following surgery.

Statistical analysis

Continuous data were assessed for normality of distribution with the Shapiro-Wilk test. Descriptive statistics are reported as frequency (%) for categorical data, mean ± SD for normally distributed continuous data, or median (IQR) for nonnormally distributed continuous data. Data were characterized as hierarchical in structure, with nesting of procedures (the experimental unit of interest) within individual dogs when > 1 TPLO procedure was performed and recorded for the same patient. Violation of the independence assumption was controlled by means of robust variance estimation with a separate logistic regression model to evaluate associations between each hypothesized predictor variable and SSI development. Predictor variables with a P value < 0.20 were then considered for inclusion in a multivariate model.

The final multivariable model was developed by backward elimination with consideration of a causal diagram, with a cutoff for predictor variable retention of P < 0.05. Postestimation model checking was performed by use of the Hosmer-Lemeshow test together with examination of Pearson and deviance residuals. The OR for SSI in each model was calculated and is reported with its 95% CI. All statistical calculations were performed with the aid of statistical software.b

Results

Dogs

Of the 491 TPLO procedures identified, 405 procedures performed on 320 dogs met the inclusion criteria. Dogs included 171 (53.4%) females and 149 (46.6%) males; 2% of dogs of either sex were sexually intact. A total of 42 purebred dogs were represented. Dogs were most commonly classified as Labrador Retriever (n = 91 [28.4%]), mixed-breed dog (82 [25.6%]), GSD (17 [5.3%]), Golden Retriever (15 [4.7%]), and Staffordshire Bull Terrier (14 [4.4%]). Median age at initial evaluation was 5.4 years (IQR, 3.4 to 7.3 years), and median body weight at the same point was 36.6 kg (80.5 lb; IQR, 30.1 to 43.5 kg [66.2 to 95.7 lb]).

Surgical procedures

Of the 405 TPLO procedures performed, 170 were performed as a bilateral procedure in the same dog. Of these, 28 were performed during the same anesthetic event and 142 were performed during different anesthetic events. Median interval between sequential procedures on the same dog was 228 days (IQR, 105 to 442 days).

The TPLO procedures were performed with equal frequency between the left (210/405 [51.9%]) and right (195/405 [48.1%]) stifle joints, and no seasonal peaks in frequency were identified. Median number of procedures performed per year was 32 (IQR, 25 to 47), with 48.1% (195/405) performed during the years 2013 and 2014. Joint examination technique varied with patient and surgeon preference; for 21.5% (n = 87) of TPLO procedures, the joint was examined by arthroscopy, whereas the remainder involved a mini arthrotomy at the medial aspect of the stifle joint. Of the 87 procedures involving arthroscopy, 17 (20%) were converted to arthrotomy, usually for meniscectomy. Most (308/405 [76.0%]) cranial cruciate ligament tears were considered complete rather than partial. In 39.5% (160/405) of TPLO procedures, a medial meniscal tear was identified requiring meniscectomy. The odds of a medial meniscal injury were 7.3 times (OR, 7.33; 95% CI, 3.77 to 14.24; P < 0.001) as great in a joint with full versus partial cranial cruciate ligament tear.

Median duration of surgery per TPLO procedure was 135 minutes (IQR, 115 to 160 minutes). Median duration of surgical anesthesia per TPLO procedure was 280 minutes (IQR, 245 to 315 minutes). Median duration of postoperative radiographic imaging was 15 minutes (IQR, 10 to 20 minutes). Median duration of presurgical anesthesia (ie, for clipping, nerve block administration, anesthesia instrumentation, and occasional preoperative imaging) per procedure was 130 minutes (IQR, 110 to 150 minutes), representing a mean ± SD percentage of total procedure duration of 46.4 ± 7.2%.

Hypotension was recorded for dogs in 37.3% (n = 151) of TPLO procedures and hypothermia in 70.1% (284). Median minimum esophageal temperature was 36.2°C (97.2°F; IQR, 35.5° to 36.8°C [95.9° to 98.2°F]). Each additional 30 minutes of the anesthetic period was associated with a 20% increase in the odds of hypotension (OR, 1.15; 95% CI, 1.03 to 1.28; P = 0.01) and of hypothermia (OR, 1.15; 95% CI, 1.01 to 1.32; P = 0.03).

For 138 (34.1%; including 8 simultaneous bilateral procedures in 4 dogs) TPLO procedures, the provided intraoperative antimicrobial treatment was deemed inappropriate. For 149 (36.8%) procedures, a prophylactic course of antimicrobials had been administered after surgery.

Incidence of SSI

An SSI developed following 34 (8.4%; 95% CI, 6.1% to 11.5%) TPLO procedures. Of these 34 SSIs, 14 (41%) were classified as superficial, 18 (53%) as deep (5 with concurrent joint space involvement), and 2 (6%) as involving the joint space alone. Infections were noted a median of 21 days (IQR, 14 to 61 days) after surgery. Staphylococcus pseudintermedius, the most common organism recovered via microbial culture, was identified in 8 dogs (24% of SSIs), including 1 dog with methicillin-resistant S pseudintermedius. For 18 (53%) TPLO procedures resulting in an SSI, implant removal was a component of management, which was performed a median of 118 days (IQR, 93 to 302 days) after the initial surgery.

Concurrent infection status

One hundred fifty-five (38.3%) TPLO procedures were performed in dogs with historical dermatitis. Of these procedures, 11 (7.1%; 95% CI, 3.9% to 12.4%) were followed by an SSI. Seventy-one (17.5%) procedures were performed on dogs with concurrent dermatitis anywhere on the body, of which 59 (14.6% of all procedures) were performed on dogs with dermatitis anywhere but at the surgical site and 12 (3.0% of all procedures) were performed on dogs with dermatitis at the surgical site specifically. The incidence of SSI was 10.2% (6/59; 95% CI, 4.5% to 21.3%) for dogs with generalized dermatitis and 16.7% (2/12; 95% CI, 3.3% to 54.3%) for dogs with dermatitis specifically at the surgical site. These cases of SSI involved either dogs with dermatitis that had not completely resolved despite treatment or dogs with owners who elected to move forward with TPLO despite discussion about increased potential for SSI development. The incidence of SSI for dogs with generalized or surgical site dermatitis was higher than that for dogs with no perioperative dermatitis (26/334 [7.8%]), but this difference was not significant (P = 0.49).

Univariable associations with SSI development

Univariable analysis revealed that breed was significantly (P < 0.001) associated with SSI development. When dogs were categorized by whether they were a Labrador Retriever, mixed-breed dog, GSD, Golden Retriever, Staffordshire Bull Terrier, or other breed, the lowest risk group was Staffordshire Bull Terriers (1 SSI/22 procedures). German Shepherd Dogs had 14 times the odds of SSI, compared with Staffordshire Bull Terriers, and approximately 9 times the odds of SSI, compared with all other breeds (Table 1).

Table 1—

Variables identified via univariable logistic regression for consideration in a multivariable model* of factors associated with development of an SSI following TPLO procedures (n = 405) in 320 dogs.

VariableOR95% CIP value
GSD (vs other) breed9.213.66–23.18< 0.01
Body weight (kg)1.021.01 – 1.040.04
Surgery in June, July, or August (vs other months)2.020.97–4.210.06
Procedure duration (h)1.421.02–1.970.04
Mean arterial blood pressure < 65 (vs ≥ 65) mm Hg1.030.99–1.070.13
Postoperative antimicrobials given (vs not given)0.500.22–1.140.10
Attending surgeon performed ≤ 20 (vs > 20) procedures3.921.68–9.16< 0.01
Medial meniscal tear requiring meniscectomy (vs no such tear)2.071.03–4.150.04
Arthroscopy and arthrotomy performed (vs not performed)2.470.67–9.060.17

Variables were considered for the multivariable model if the P value was ≤ 0.20.

The risk of SSI was associated with the surgeon (n = 12) performing the procedure (P = 0.02). The number of procedures performed by each surgeon ranged from 1 to 163. When surgeons were grouped by the number of procedures they performed during the study period, surgeons who performed ≤ 20 procedures each (n = 9; SSI rate, 21% [8/39]) had a significantly (P < 0.01) higher odds of SSI in their patients than surgeons who performed > 20 procedures each (3; SSI rate, 7.1% [26/366]; Table 1). The surgeon who performed the largest number of surgeries had a mean procedure duration that was 21 minutes briefer (P < 0.001) than that for the other surgeons; that surgeon's SSI rate was 6.7% (11/163).

Procedures for dogs with a medial meniscal tear requiring meniscectomy were approximately twice as likely to be followed by an SSI as were procedures involving no such tears (Table 1). Risk of SSI development also increased with increasing body weight and procedure duration. Other variables considered for inclusion in the multivariable model (with a value of P < 0.20) were TPLO procedures performed in the summer months, mean arterial blood pressure < 65 mm Hg, postoperative antimicrobial administration, and arthroscopy with conversion to arthrotomy.

Multivariable model

The final multivariable model contained the variables GSD breed (OR, 9.72; 95% CI, 3.76 to 25.15; P < 0.001), presence of a medial meniscal tear requiring meniscectomy (OR, 2.49; 95% CI, 1.20 to 5.18; P = 0.02), and performance of the procedure by a surgeon who had contributed ≤ 20 procedures to the study sample (OR, 2.96; 95% CI, 1.21 to 7.25; P = 0.02). The value for the area under the receiver operating characteristic curve (0.71) of this model indicated good discrimination, with adequate model fit (Hosmer-Lemeshow test, P = 0.58).

Discussion

The purpose of the retrospective cohort study reported here was to identify risk factors associated with SSI development in dogs following TPLO. We were particularly interested in the relationship between historical or preoperative dermatitis and outcome. The incidence of SSI was 8.4%, which is within the reported range of 2.5% to 15.8%.3–10 Dog breed, attending surgeon, and medial meniscal tear requiring meniscectomy were each independently associated with SSI development in the final multivariable model.

No significant association was identified between medical history of dermatitis and SSI development. Although point estimates of SSI incidence in the subgroups of dogs with perioperative dermatitis at the surgical site (16.7%) or elsewhere on the body (10.2%) were higher than in dogs with no perioperative dermatitis (7.8%), these differences were not significant. The number of dogs within these subgroups was small, allowing for the possibility of a type II error. We therefore recommend additional investigation into the influence of perioperative dermatitis on SSI in dogs undergoing TPLO, given that this variable could affect the surgeon's decision-making process and subsequent recommendations to owners.

The finding that the GSD breed had almost 10 times the odds of developing an SSI relative to other breeds was consistent with the findings of another retrospective study,32 in which GSDs were at increased odds of developing complications following TPLO. The GSD breed reportedly has the largest total number of inherited defects.33,34 Many of these defects are immune-mediated disorders, including inflammatory conditions such as atopic dermatitis.35 German Shepherd Dogs may be genetically predisposed to SSI, regardless of dermatitis status at the time of TPLO. Further investigation of factors that increase the risk of postoperative SSI in this breed is warranted. No significant association with SSI development was identified for other breeds, such as Labrador Retrievers or Bulldogs, as identified in previous studies.3,20

To the authors' knowledge, the present study represents the first study to show that attending surgeon was a risk factor for SSI development in veterinary patients. When surgeons were categorized by the number of procedures they performed during the study period, those who performed ≤ 20 procedures each were nearly 4 times as likely to have a procedure resulting in an SSI as were surgeons who performed > 20 procedures. The surgeons in the > 20 procedures group were all permanent board-certified orthopedic faculty with several years of experience working in a familiar operating-room environment. Conversely, the surgeons in the other group were a mix of final-year residents, newly qualified surgeons in clinical instructor positions, or experienced board-certified orthopedic surgeons fulfilling temporary locum positions. Thus, the procedure contribution rate may have acted as a proxy variable either for surgeon inexperience or unfamiliarity with their operating-room environment. It would appear intuitive that either or both of these factors might have contributed to increased risk of surgical trauma or intraoperative contamination, and additional research in these areas might be enlightening. In previous studies,36,37 the risk of a breach in asepsis by incidents such as glove perforation varied among surgeons, and such breaches increased the likelihood of SSI. A similar surgeon-related influence on SSIs has been reported in human medicine.38 Breaches in asepsis were not reliably documented in the medical records used for the present study, so this variable could not be specifically explored for an association with SSI development. A significant association was identified between SSI and hospital where the procedure was performed in another veterinary study,20 and this finding could be partly explained by the involvement of different surgeons in procedures, although this possibility was not directly evaluated. Because TPLO technique in the present study was not standardized, with many components of specific technique and pre- and postoperative care left to the discretion of the attending surgeon, the identified surgeon effect was likely a proxy for 1 or more specific variables, such as specific beliefs and preferences regarding delaying surgery for dogs with existing dermatitis. Investigation of individual surgical methods in a prospective study design may better identify both detrimental and protective surgical-related techniques that can influence SSI development in dogs following TPLO.

Meniscal tears are a common comorbidity associated with cranial cruciate ligament tears, as shown by 39.5% of dogs in the present study requiring a meniscectomy. Dogs with complete cranial cruciate ligament tears had 7.3 times the odds of requiring a meniscectomy, compared with the odds for dogs with partial tears, which is similar to previously reported data.39,40 In humans, meniscal tears cause an inflammatory cascade that results in the development of osteoarthritis.41 Meniscal disease alone or meniscectomy may increase the risk of SSI development. Meniscectomy involves more instruments and more manipulation of the joint to allow exposure of the damaged tissue than TPLO alone, resulting in more opportunities for breaks in asepsis. In the authors' experience, dogs with meniscal disease often have a longer duration of cranial cruciate rupture and attendant joint inflammation than dogs with only partial cranial cruciate ligament tears and functionally intact menisci. Chronic inflammation could influence immunity and opportunities for infection within the stifle joint; however, most SSIs in the present study were limited to the deep surgical tissues around the TPLO plate and not to the joint space itself.

Prophylactic antimicrobial administration following surgery was not significantly associated with SSI development in the present study, although a protective effect has been identified in previous studies.3,4,7,14,18–23 Nonetheless, in the absence of convincing evidence to the contrary, we recommend targeted prophylactic antimicrobial treatment following surgery for dogs at risk or suspected to be at risk of SSI, such as GSDs, dogs with complete cranial cruciate ligament rupture and meniscal tears, or dogs with perioperative dermatitis.

Limitations of the study reported here included selection bias and its retrospective nature. One element of selection bias was the fact that dogs that underwent surgery despite dermatitis generally had mild dermatitis, and dogs with severe dermatitis had surgery delayed until their signs resolved. Given the lack of active, contemporaneously acquired follow-up information, the true incidence of SSI was likely higher than that captured in the medical records. Prospective studies involving an SSI surveillance program would be necessary to capture the true SSI incidence rate. In addition, preoperative dermatitis was diagnosed largely on the basis of physical examination findings, with cytologic evaluation performed only sporadically to confirm the diagnosis. Diagnostic cytologic evaluation or bacterial culture would ideally have been performed to definitively diagnose preoperative dermatitis. Reliance on retrospective review of medical records also likely introduced measurement error in that a surgeon's failure to document certain variables did not always mean those variables did not exist for a given patient. Furthermore, the lack of standardized criteria for recording of dermatitis or severity of dermatitis, together with inability to reliably retrospectively capture all dogs for which surgery had been delayed owing to dermatitis, likely impaired our ability to assess associations between SSI development and dermatitis or surgeon.

Regardless of these limitations, the present study revealed several risk factors for SSI in dogs following TPLO that had not been previously reported, including effect of surgeon and need for meniscectomy. The point estimates of SSI incidence in the subgroups of dogs with perioperative dermatitis were interesting and warrant further investigation. Prospective studies are warranted to investigate the effect of tailoring management protocols to dogs with established or suspected risk factors for SSI.

ABBREVIATIONS

CI

Confidence interval

GSD

German Shepherd Dog

IQR

Interquartile range (25th to 75th percentile)

SSI

Surgical site infection

TPLO

Tibial plateau leveling osteotomy

Footnotes

a.

Apotex Corp, Weston, Fla.

b.

Stata, version 13, Stata Corp, College Station, Tex.

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    • Search Google Scholar
    • Export Citation
  • 6. Etter SW, Ragetly GR, Bennett RA, et al. Effect of using triclosan-impregnated suture for incisional closure on surgical site infection and inflammation following tibial plateau leveling osteotomy in dogs. J Am Vet Med Assoc 2013;242:355358.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7. Frey TN, Hoelzler MG, Scavelli TD, et al. Risk factors for surgical site infection-inflammation in dogs undergoing surgery for rupture of the cranial cruciate ligament: 902 cases (2005–2006). J Am Vet Med Assoc 2010;236:8894.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8. Gallagher AD, Mertens WD. Implant removal rate from infection after tibial plateau leveling osteotomy in dogs. Vet Surg 2012;41:705711.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9. Savicky R, Beale B, Murtaugh R, et al. Outcome following removal of TPLO implants with surgical site infection. Vet Comp Orthop Traumatol 2013;26:260265.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10. Thompson AM, Bergh MS, Wang C, et al. Tibial plateau levelling osteotomy implant removal: a retrospective analysis of 129 cases. Vet Comp Orthop Traumatol 2011;24:450456.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11. Nicoll C, Singh A, Weese JS. Economic impact of tibial plateau leveling osteotomy surgical site infection in dogs. Vet Surg 2014;43:899902.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12. Beal MW, Brown DC, Shofer FS. The effects of perioperative hypothermia and the duration of anesthesia on postoperative wound infection rate in clean wounds: a retrospective study. Vet Surg 2000;29:123127.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13. Brown DC, Conzemius MG, Shofer F, et al. Epidemiologic evaluation of postoperative wound infections in dogs and cats. J Am Vet Med Assoc 1997;210:13021306.

    • Search Google Scholar
    • Export Citation
  • 14. Eugster S, Schawalder P, Gaschen F, et al. A prospective study of postoperative surgical site infections in dogs and cats. Vet Surg 2004;33:542550.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15. Heldmann E, Brown DC & Shofer F. The association of propofol usage with postoperative wound infection rate in clean wounds: a retrospective study. Vet Surg 1999;28:256259.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16. Mayhew PD, Freeman L, Kwan T, et al. Comparison of surgical site infection rates in clean and clean-contaminated wounds in dogs and cats after minimally invasive versus open surgery: 179 cases (2007–2008). J Am Vet Med Assoc 2012;240:193198.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17. Nicholson M, Beal M, Shofer F, et al. Epidemiologic evaluation of postoperative wound infection in clean-contaminated wounds: a retrospective study of 239 dogs and cats. Vet Surg 2002;31:577581.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18. Verwilghen D & Singh A. Fighting surgical site infections in small animals: are we getting anywhere? Vet Clin North Am Small Anim Pract 2015;45:243276.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19. Nazarali A, Singh A, Weese JS. Perioperative administration of antimicrobials during tibial plateau leveling osteotomy. Vet Surg 2014;43:966971.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20. Nazarali A, Singh A, Moens NM, et al. Association between methicillin-resistant Staphylococcus pseudintermedius carriage and the development of surgical site infections following tibial plateau leveling osteotomy in dogs. J Am Vet Med Assoc 2015;247:909916.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21. Solano MA, Danielski A, Kovach K, et al. Locking plate and screw fixation after tibial plateau leveling osteotomy reduces postoperative infection rate in dogs over 50 kg. Vet Surg 2015;44:5964.

    • Search Google Scholar
    • Export Citation
  • 22. Pratesi A, Moores AP, Downes C, et al. Efficacy of postoperative antimicrobial use for clean orthopedic implant surgery in dogs: A prospective randomized study in 100 consecutive cases. Vet Surg 2015;44:653660.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23. Whittem TL, Johnson AL, Smith CW, et al. Effect of perioperative prophylactic antimicrobial treatment in dogs undergoing elective orthopedic surgery. J Am Vet Med Assoc 1999;215:212216.

    • Search Google Scholar
    • Export Citation
  • 24. Aiken MJ, Hughes TK, Abercromby RH, et al. Prospective, randomized comparison of the effect of two antimicrobial regimes on surgical site infection rate in dogs undergoing orthopedic implant surgery. Vet Surg 2015;44:661667.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25. Vasseur PB, Levy J, Dowd E, et al. Surgical wound infection rates in dogs and cats. Data from a teaching hospital. Vet Surg 1988;17:6064.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26. Faraday N, Rock P, Lin EE, et al. Past history of skin infection and risk of surgical site infection after elective surgery. Ann Surg 2013;257:150154.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27. Lim CT, Tan KJ, Kagda F, et al. Implant infection caused by dermatitis: a report of two cases. J Orthop Surg (Hong Kong) 2007;15:365367.

  • 28. Cronquist AB, Jakob K, Lai L, et al. Relationship between skin microbial counts and surgical site infection after neurosurgery. Clin Infect Dis 2001;33:13021308.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29. Centers for Disease Control and Prevention. Surgical Site Infection (SSI) Event. Available at: www.cdc.gov/nhsn/pdfs/pscmanual/9pscssicurrent.pdf. Accessed Jul 1, 2016.

    • Search Google Scholar
    • Export Citation
  • 30. Bratzler DW, Dellinger EP, Olsen KM, et al. Clinical practice guidelines for antimicrobial prophylaxis in surgery. Surg Infect (Larchmt) 2013;14:73156.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31. Marcellin-Little DJ, Papich MG, Richardson DC, et al. Pharmacokinetic model for cefazolin distribution during total hip arthroplasty in dogs. Am J Vet Res 1996;57:720723.

    • Search Google Scholar
    • Export Citation
  • 32. Coletti TJ, Anderson M, Gorse MJ, et al. Complications associated with tibial plateau leveling osteotomy: a retrospective of 1,519 procedures. Can Vet J 2014;55:249254.

    • Search Google Scholar
    • Export Citation
  • 33. Asher L, Diesel G, Summers JF, et al. Inherited defects in pedigree dogs. Part 1: disorders related to breed standards. Vet J 2009;182:402411.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 34. Summers JF, Diesel G, Asher L, et al. Inherited defects in pedigree dogs. Part 2: disorders that are not related to breed standards. Vet J 2010;183:3945.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 35. Tengvall K, Kierczak M, Bergvall K, et al. Genome-wide analysis in German Shepherd Dogs reveals association of a locus on CFA 27 with atopic dermatitis. PLoS Genet 2013;9:e1003475.

    • Search Google Scholar
    • Export Citation
  • 36. Misteli H, Weber WP, Reck S, et al. Surgical glove perforation and the risk of surgical site infection. Arch Surg 2009;144:553558.

  • 37. Meakin LB, Gilman OP, Parsons KJ, et al. Colored indicator undergloves increase the detection of glove perforations by surgeons during small animal orthopedic surgery: a randomized controlled trial. Vet Surg 2016;45:709714.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 38. Hellinger WC, Heckman MG, Crook JE, et al. Association of surgeon with surgical site infection after liver transplantation. Am J Transplant 2011;11:18771884.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 39. Hayes GM, Langley-Hobbs SJ, Jeffery ND. Risk factors for medial meniscal injury in association with cranial cruciate ligament rupture. J Small Anim Pract 2010;51:630634.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 40. Corr SA & Brown C. A comparison of outcomes following tibial plateau levelling osteotomy and cranial tibial wedge osteotomy procedures. Vet Comp Orthop Traumatol 2007;20:312319.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 41. Edd SN, Giori NJ, Andriacchi TP. The role of inflammation in the initiation of osteoarthritis after meniscal damage. J Bio mech 2015;48:14201426.

    • Search Google Scholar
    • Export Citation

Contributor Notes

Address correspondence to Dr. Hayes (gmh59@cornell.edu).

Dr. VanDeventer's present address is Boundary Bay Veterinary Speciality Hospital, Unit 204, 20434 64 Ave, Langley, BC V2Y IN4, Canada.

Dr. Aryazand's present address is Veterinary Medical Center of Long Island, 75 Sunrise Hwy North Service Rd, West Islip, NY 11795.

Drs. Lopez and VanDeventer contributed equally to this work.

  • 1. Slocum B, Slocum TD. Tibial plateau leveling osteotomy for repair of cranial cruciate ligament rupture in the canine. Vet Clin North Am Small Anim Pract 1993;23:777795.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2. Turk R, Singh A, Weese JS. Prospective surgical site infection surveillance in dogs. Vet Surg 2015;44:28.

  • 3. Fitzpatrick N, Solano MA. Predictive variables for complications after TPLO with stifle inspection by arthrotomy in 1000 consecutive dogs. Vet Surg 2010;39:460474.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4. Gatineau M, Dupuis J, Planté J, et al. Retrospective study of 476 tibial plateau levelling osteotomy procedures. Rate of subsequent ‘pivot shift’, meniscal tear and other complications. Vet Comp Orthop Traumatol 2011;24:333341.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5. Pacchiana PD, Morris E, Gillings SL, et al. Surgical and postoperative complications associated with tibial plateau leveling osteotomy in dogs with cranial cruciate ligament rupture: 397 cases (1998–2001). J Am Vet Med Assoc 2003;222:184193.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6. Etter SW, Ragetly GR, Bennett RA, et al. Effect of using triclosan-impregnated suture for incisional closure on surgical site infection and inflammation following tibial plateau leveling osteotomy in dogs. J Am Vet Med Assoc 2013;242:355358.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7. Frey TN, Hoelzler MG, Scavelli TD, et al. Risk factors for surgical site infection-inflammation in dogs undergoing surgery for rupture of the cranial cruciate ligament: 902 cases (2005–2006). J Am Vet Med Assoc 2010;236:8894.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8. Gallagher AD, Mertens WD. Implant removal rate from infection after tibial plateau leveling osteotomy in dogs. Vet Surg 2012;41:705711.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9. Savicky R, Beale B, Murtaugh R, et al. Outcome following removal of TPLO implants with surgical site infection. Vet Comp Orthop Traumatol 2013;26:260265.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10. Thompson AM, Bergh MS, Wang C, et al. Tibial plateau levelling osteotomy implant removal: a retrospective analysis of 129 cases. Vet Comp Orthop Traumatol 2011;24:450456.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11. Nicoll C, Singh A, Weese JS. Economic impact of tibial plateau leveling osteotomy surgical site infection in dogs. Vet Surg 2014;43:899902.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12. Beal MW, Brown DC, Shofer FS. The effects of perioperative hypothermia and the duration of anesthesia on postoperative wound infection rate in clean wounds: a retrospective study. Vet Surg 2000;29:123127.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13. Brown DC, Conzemius MG, Shofer F, et al. Epidemiologic evaluation of postoperative wound infections in dogs and cats. J Am Vet Med Assoc 1997;210:13021306.

    • Search Google Scholar
    • Export Citation
  • 14. Eugster S, Schawalder P, Gaschen F, et al. A prospective study of postoperative surgical site infections in dogs and cats. Vet Surg 2004;33:542550.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15. Heldmann E, Brown DC & Shofer F. The association of propofol usage with postoperative wound infection rate in clean wounds: a retrospective study. Vet Surg 1999;28:256259.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16. Mayhew PD, Freeman L, Kwan T, et al. Comparison of surgical site infection rates in clean and clean-contaminated wounds in dogs and cats after minimally invasive versus open surgery: 179 cases (2007–2008). J Am Vet Med Assoc 2012;240:193198.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17. Nicholson M, Beal M, Shofer F, et al. Epidemiologic evaluation of postoperative wound infection in clean-contaminated wounds: a retrospective study of 239 dogs and cats. Vet Surg 2002;31:577581.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18. Verwilghen D & Singh A. Fighting surgical site infections in small animals: are we getting anywhere? Vet Clin North Am Small Anim Pract 2015;45:243276.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19. Nazarali A, Singh A, Weese JS. Perioperative administration of antimicrobials during tibial plateau leveling osteotomy. Vet Surg 2014;43:966971.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20. Nazarali A, Singh A, Moens NM, et al. Association between methicillin-resistant Staphylococcus pseudintermedius carriage and the development of surgical site infections following tibial plateau leveling osteotomy in dogs. J Am Vet Med Assoc 2015;247:909916.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21. Solano MA, Danielski A, Kovach K, et al. Locking plate and screw fixation after tibial plateau leveling osteotomy reduces postoperative infection rate in dogs over 50 kg. Vet Surg 2015;44:5964.

    • Search Google Scholar
    • Export Citation
  • 22. Pratesi A, Moores AP, Downes C, et al. Efficacy of postoperative antimicrobial use for clean orthopedic implant surgery in dogs: A prospective randomized study in 100 consecutive cases. Vet Surg 2015;44:653660.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23. Whittem TL, Johnson AL, Smith CW, et al. Effect of perioperative prophylactic antimicrobial treatment in dogs undergoing elective orthopedic surgery. J Am Vet Med Assoc 1999;215:212216.

    • Search Google Scholar
    • Export Citation
  • 24. Aiken MJ, Hughes TK, Abercromby RH, et al. Prospective, randomized comparison of the effect of two antimicrobial regimes on surgical site infection rate in dogs undergoing orthopedic implant surgery. Vet Surg 2015;44:661667.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25. Vasseur PB, Levy J, Dowd E, et al. Surgical wound infection rates in dogs and cats. Data from a teaching hospital. Vet Surg 1988;17:6064.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26. Faraday N, Rock P, Lin EE, et al. Past history of skin infection and risk of surgical site infection after elective surgery. Ann Surg 2013;257:150154.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27. Lim CT, Tan KJ, Kagda F, et al. Implant infection caused by dermatitis: a report of two cases. J Orthop Surg (Hong Kong) 2007;15:365367.

  • 28. Cronquist AB, Jakob K, Lai L, et al. Relationship between skin microbial counts and surgical site infection after neurosurgery. Clin Infect Dis 2001;33:13021308.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29. Centers for Disease Control and Prevention. Surgical Site Infection (SSI) Event. Available at: www.cdc.gov/nhsn/pdfs/pscmanual/9pscssicurrent.pdf. Accessed Jul 1, 2016.

    • Search Google Scholar
    • Export Citation
  • 30. Bratzler DW, Dellinger EP, Olsen KM, et al. Clinical practice guidelines for antimicrobial prophylaxis in surgery. Surg Infect (Larchmt) 2013;14:73156.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31. Marcellin-Little DJ, Papich MG, Richardson DC, et al. Pharmacokinetic model for cefazolin distribution during total hip arthroplasty in dogs. Am J Vet Res 1996;57:720723.

    • Search Google Scholar
    • Export Citation
  • 32. Coletti TJ, Anderson M, Gorse MJ, et al. Complications associated with tibial plateau leveling osteotomy: a retrospective of 1,519 procedures. Can Vet J 2014;55:249254.

    • Search Google Scholar
    • Export Citation
  • 33. Asher L, Diesel G, Summers JF, et al. Inherited defects in pedigree dogs. Part 1: disorders related to breed standards. Vet J 2009;182:402411.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 34. Summers JF, Diesel G, Asher L, et al. Inherited defects in pedigree dogs. Part 2: disorders that are not related to breed standards. Vet J 2010;183:3945.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 35. Tengvall K, Kierczak M, Bergvall K, et al. Genome-wide analysis in German Shepherd Dogs reveals association of a locus on CFA 27 with atopic dermatitis. PLoS Genet 2013;9:e1003475.

    • Search Google Scholar
    • Export Citation
  • 36. Misteli H, Weber WP, Reck S, et al. Surgical glove perforation and the risk of surgical site infection. Arch Surg 2009;144:553558.

  • 37. Meakin LB, Gilman OP, Parsons KJ, et al. Colored indicator undergloves increase the detection of glove perforations by surgeons during small animal orthopedic surgery: a randomized controlled trial. Vet Surg 2016;45:709714.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 38. Hellinger WC, Heckman MG, Crook JE, et al. Association of surgeon with surgical site infection after liver transplantation. Am J Transplant 2011;11:18771884.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 39. Hayes GM, Langley-Hobbs SJ, Jeffery ND. Risk factors for medial meniscal injury in association with cranial cruciate ligament rupture. J Small Anim Pract 2010;51:630634.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 40. Corr SA & Brown C. A comparison of outcomes following tibial plateau levelling osteotomy and cranial tibial wedge osteotomy procedures. Vet Comp Orthop Traumatol 2007;20:312319.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 41. Edd SN, Giori NJ, Andriacchi TP. The role of inflammation in the initiation of osteoarthritis after meniscal damage. J Bio mech 2015;48:14201426.

    • Search Google Scholar
    • Export Citation

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