Introduction
Open wounds as a result of various causes are common in dogs. Naturally occurring open wounds are often contaminated with micro-organisms, and some are clinically infected.1 Infection can lead to delayed healing, highlighting the importance of prompt identification of wound-associated microbes.2 For many open wounds in dogs, specimens are collected and cultured to guide appropriate antimicrobial treatment if indicated.
Multiple different techniques for wound specimen culture have been described. Tissue biopsy has been considered the reference method of culture specimen collection in human medicine.3,4 Previously, there has been concern that swabs collect only superficial bacteria from wounds and that the swab culture results may therefore represent an inaccurate assessment of bacteria that have invaded deeper tissues.5 However, others have argued that because most wounds are contaminated by superficial bacteria, such as environmental contaminants or skin microflora, surface bacteria would be an accurate representation of the bacterial population within deeper tissues.5 In contrast to swab collection, tissue biopsy is an invasive technique that requires sedation and analgesia of the patient and appropriate training of sample collectors. Further, some wounds may not be amenable to biopsy because of location or a lack of viable tissue.
In an effort to identify the most reliable and practical method of obtaining culture specimens in human medicine, the accuracy of results of cultures of 2 specimen types, swabs and tissue biopsy specimens, have been compared.4 Results of studies that have compared the 2 sampling methods are somewhat contradictory. Results of several investigations indicate that the swab and tissue biopsy are equally effective at recovering wound-associated bacteria,6,7,8,9,10,11 whereas other studies12,13 have revealed that culturing swabs is inferior to culturing tissue biopsy specimens because fewer bacteria are recovered. In veterinary medicine, clinical evidence that would strongly favor one method over the other is lacking. To date, findings of 2 studies14,15 that were performed on traumatic horse and dog wounds indicate that there is no significant difference in culture results for swabs and tissue biopsy specimens.
The objective of the study reported here was to compare bacteriologic culture results for superficial swab (Levine technique) and tissue biopsy specimens obtained from dogs with naturally occurring open wounds. We hypothesized that use of the 2 specimen types would be equivalent with regard to culture-based isolation of wound-associated bacteria. Furthermore, we hypothesized that any disagreement in culture results between these 2 specimen types would be of low clinical importance.
Materials and Methods
Dogs
In October 2018 through November 2019, client-owned dogs of any age admitted to the Texas A&M University Veterinary Medical Teaching Hospital with an open skin wound (surface area, ≥ 1 cm2) were considered for inclusion in the study. Dogs that were known to have hematologic disorders with risk for uncontrolled bleeding or wounds that were not amenable to biopsy were excluded from the study. Each dog was only enrolled once in the study. When a dog had multiple wounds, only 1 wound was selected for inclusion. For the purpose of this study, acute and chronic wounds were defined as the wounds that were present for < 7 days or ≥ 7 days, respectively. All the dogs enrolled in this study were managed at the discretion of the attending clinician. Data collected included signalment, cause of the wound, wound location and duration, the dog’s current medications and comorbidities, date and time of specimen collection, time of submission to the laboratory, and bacteriologic culture results. Prior to sample collection, informed consent from owners was obtained for each dog included in the study. The study protocol was approved by the Texas A&M University Institutional Animal Care and Use Committee (protocol 2018-0200 CA).
Specimen collection
Wound management was performed in a routine manner. Briefly, the hair surrounding the wound was clipped; initial cleaning of intact skin was performed with 0.05% chlorhexidine diacetate solution or 4% chlorhexidine gluconate scrub, and care was taken to prevent the antiseptic solution from entering the wound. Sterile instruments, surgical caps, face masks, and sterile gloves were used by sample collectors in each case. Nonsterile surgical gowns and sterile drapes were used when deemed necessary by the attending clinician. The wound was thoroughly lavaged with copious amounts of sterile saline (0.9% NaCl) solution to allow for removal of surface contaminants and wound debris. Sterile gauze was used to blot the surface of the wound when needed. Sharp, layered debridement was performed when necessary.
After the wound had been prepared, a swab sample was obtained for culture by the Levine technique.16 Briefly, a sterile culturette swab (BD BBL CultureSwab Collection & Transport System; Becton Dickinson) was twirled over a 1-cm2 area of the wound bed for a period of 5 seconds while applying sufficient pressure to express wound fluid or to cause minimal bleeding from the wound.16 After swabbing, the tissue biopsy specimen was obtained from an area immediately adjacent to the swabbed area. The tissue biopsy specimen was excised with a sterile 3-mm disposable biopsy punch, scalpel blade, or scissors. Aerobic bacteriologic culture of every specimen collected was performed. When clinically indicated, anaerobic bacteriologic culture of an appropriate swab (BD BBL Vacutainer Anaerobic Specimen Collector; Becton Dickinson) was also performed in the same manner. Specimens were immediately placed into individual sterile culturette tubes ((BD BBL CultureSwab Collection & Transport System and BD BBL Vacutainer Anaerobic Specimen Collector; Becton Dickinson) as appropriate for each aerobic or anaerobic culture. The exact time and date of sample collection was recorded. The culturette tubes were placed together into a specimen bag and handled in an identical manner. Specimens were either processed immediately following collection or placed in a refrigerator overnight; regardless, both specimens from a given wound were processed within 24 hours after collection.
All personnel (eg, interns, residents, or faculty members) that collected specimens had been trained in both collection techniques to enhance experimental reproducibility. Importantly, the same individual who performed the swab collection performed the tissue biopsy specimen collection.
Specimen processing
Both swab and tissue biopsy specimens were plated and processed by use of a standard bacteriologic technique in the hospital’s clinical microbiology laboratory. Identification of bacterial isolates was performed via matrix-assisted laser desorption ionization–time-of-flight mass spectrometry (MALDI-TOF MS, Microflex LT; Bruker Daltonics). Prior to testing of each specimen, the mass spectrometer was calibrated for molecular weights (range, 3,637 to 16,952 Da) with a bacterial test standard (MALDI-TOF MS, Microflex LT; Bruker Daltonics) according to the manufacturer’s recommendations. In cases where mass spectrometry failed to identify bacterial isolates, identification was achieved via conventional means involving Gram staining, assessment of colony morphology, and biochemical analyses (RapID Systems; Remel) or PCR assay of the bacterial 16S rRNA gene followed by sequencing.
Clinical interpretation
To investigate the clinical importance of any culture results that differed between the 2 specimen types, 2 board-certified veterinary surgeons (who were unaware of the specimen source) evaluated the culture results. They were asked to evaluate the culture results only, and not the wound itself. Specifically, the evaluators were provided with 2 discrepant culture results and asked to determine whether their wound management would consequently differ.
Statistical analysis
Descriptive statistics were reported, including means and SDs for continuous variables and frequency and proportion for categorical variables. A χ2 or Fisher exact test was used to analyze all categorical variables, and a Wilcoxon rank sum test was used to analyze continuous variables. Normality was assessed with the Shapiro-Wilk test; median, range, and interquartile range (IQR [25% to 75%]) were reported for nonnormally distributed data. For bacterial species present in ≥ 10% of specimens, a κ coefficient was determined to compare presence of the bacterial species in swab versus biopsy specimens. Agreement between the 2 evaluators regarding clinical importance of the 2 culture results for a given wound was assessed by calculation of a κ coefficient. Generally, κ values of 0 to 0.4 are interpreted as indicating poor agreement, values of 0.40 to 0.74 are interpreted as indicating good agreement, and values of 0.75 to 1.0 are interpreted as indicating excellent agreement.17 For all analyses, commercial statistical software (SAS 9.4; SAS Institute Inc) was used, and a value of P < 0.05 was considered significant.
Results
A total of 52 dogs were included in the study. The mean ± SD age of the dogs was 7.2 ± 0.6 years (range, 4 months to 17 years). Both sexes were equally represented; there were 26 females (23 spayed and 3 sexually intact) and 26 males (18 neutered and 8 sexually intact). Breeds included mix (n = 8), Labrador Retriever (5), Australian Shepherd (4), Chihuahua (4), pit bull–type dog (4), Border Collie (2), Jack Russell Terrier (2), Yorkshire Terrier (2), German Shepherd Dog (2), English Bulldog (2), Golden Retriever (2), Weimaraner (1), Cairn Terrier (1), Anatolian Shepherd (1), Shih Tzu (1), Wheaten Terrier (1), Blue Lacy (1), Dachshund (1), Maltese (1), Brussels Griffon (1), Great Dane (1), Giant Schnauzer (1), Greyhound (1), Lhasa Apso (1), Rat Terrier (1), and English Springer Spaniel (1). The duration of the wound was known in all cases (median duration, 3 days [range, 1 to 730 days; interquartile range, 1 to 6.5 days]). Most of the 52 wounds were acute in nature (40 [76.9%]); 12 (23%) were defined as chronic.
Among the 52 wounds, causes varied greatly, but most were animal bites (22/52 [42.3]) or surgical site infections (12 [23%]); 6 (11.5%) were penetrating wounds and 6 (11.5%) had an unknown cause. The causes of the remaining wounds were vehicular trauma (3 [5.8%]), pressure necrosis (2 [3.8%]), and gunshot (1 [1.9%]). Of the 52 wounds, 22 were located on a limb, 11 were located on the thorax or abdomen, 8 were located in the cervical region, 4 were located in the axilla, 3 were located on the head or face, 2 were located on the dorsum, 1 was located in the perianal region, and 1 was located on the tail. Specimens were collected by 21 clinicians within the institution.
Forty (76.9%) dogs had no comorbidities. The remaining 12 (23.1%) dogs were noted to have concurrent illnesses, such as mast cell tumor (n = 2), cutaneous hemangiosarcoma (1), fibroma (1), heartworm disease (1), ichthyosis (1), immune-mediated neuropathy (1), immune-mediated polyarthritis (1), metastatic apocrine gland anal sac adenocarcinoma (1), osteosarcoma (1), spinal empyema (1), and a stomach mass for which there was no histologic diagnosis (1).
Bacteriologic culture of the collected specimens yielded 34 bacterial genera and 67 bacterial species. Sample collection by swabbing and tissue biopsy resulted in 84.6% (44/52 swabs) and 76.9% (40/52 biopsy specimens) culture-positive wounds, respectively; the remaining 8 (15.3%) swabs and 12 (23.1%) biopsy specimens had no growth (Table 1). The percentage of culture-positive results did not differ significantly (P = 0.3) between specimen types. Of the 52 dogs, 24 were receiving antimicrobial treatment at the time of specimen collection. Culture results were negative for tissue biopsy specimens obtained from 12 dogs; of the 12 wounds, 10 were considered acute and 2 were considered chronic. Culture results were negative for both swabs and tissue biopsy specimens obtained from 8 dogs; of those 8 wounds, 7 were considered acute and 1 was considered chronic. None of the wound swabs yielded no growth on culture in the absence of negative culture results for the corresponding biopsy specimens. Nine of the 12 dogs for which biopsy specimen culture results were negative and 7 of 8 dogs for which biopsy specimen culture results were negative were receiving antimicrobials. With regard to the mean ± SD recovery rates of bacteria for culture-positive wounds, both the swabs and tissue biopsy specimens yielded 3.4 ± 1.8 bacterial species/wound (median, 3 bacterial species/wound; range, 1 to 9 bacterial species/wound; P = 1.0). For 16 of the 52 (30.8%) wounds, all bacterial species in a given wound were cultured from both types of specimen. However, culture of swabs from 24 (46.1%) wounds failed to recover all the bacterial species that were cultured from the respective biopsy specimens.
Bacteriologic culture results for superficial swab and tissue biopsy specimens obtained from 52 dogs with naturally occurring open skin wounds.
| Variable | No. of swab cultures (% [n = 52]) | No. of tissue biopsy specimen cultures (% [n = 52]) | No. of wounds for which the swab and biopsy specimen culture results were identical |
|---|---|---|---|
| Monomicrobial culture result | 10 (19.3) | 7 (13.5) | 2 |
| Polymicrobial culture result | 37 (71.2) | 30 (57.7) | 1 |
| Negative culture result | 8 (15.4) | 12 (23.1) | 8 |
Following routine wound preparation of 1 wound/dog, specimens were obtained with a superficial swab (Levine) technique (n = 1) and tissue biopsy (1). Specimens were similarly handled and processed by standard bacteriologic methods.
The more common bacteria (isolated from ≥ 10% of the wounds) recovered from the 52 tissue biopsy specimens were Staphylococcus pseudintermedius (n = 19 [36.5%] wounds), Streptococcus canis (7 [13.4%]), Pasteurella canis (6 [11.5%]), Escherichia coli (6 [11.5%]), and Streptococcus minor (6 [11.5%]). The more common bacteria recovered from the 52 swabs included S pseudintermedius (n = 21 [40.4%]), Enterococcus faecalis (8 [15.4%]), S canis (6 [11.5%]), Pseudomonas aeruginosa (6 [11.5%]), P canis (6 [11.5%]), E coli (6 [11.5%]), and S minor (5 [9.6%]). Among the more common bacteria cultured, there was agreement between the swab and tissue biopsy specimen culture results (Table 2).
Observed agreement (κ coefficient with 95% confidence interval [CI]) for bacteria that were most frequently cultured (ie, recovered from ≥ 10% of the 52 wounds) from swab and tissue biopsy specimens obtained from the 52 dogs in Table 1.
| Bacteria | Observed agreement (%) | κ | 95% CI |
|---|---|---|---|
| Enterococcus faecalis | 90.4 | 0.56 | 0.2–0.92 |
| Escherichia coli | 92.3 | 0.62 | 0.26–0.98 |
| Pasteurella canis | 92.3 | 0.62 | 0.26–0.98 |
| Pseudomonas aeruginosa | 94.2 | 0.69 | 0.36–1.0 |
| Staphylococcus pseudintermedius | 84.6 | 0.67 | 0.47–0.88 |
| Streptococcus canis | 94.2 | 0.74 | 0.45–1.0 |
| Streptococcus minor | 94.2 | 0.69 | 0.36–1.0 |
κ Values of 0 to 0.4 were interpreted as indicating poor agreement, values of 0.40 to 0.74 were interpreted as indicating good agreement, and values of 0.75 to 1.0 were interpreted as indicating excellent agreement.
Culture results for swab and tissue biopsy specimens were identical in 11 of the 52 (21.2%) wounds; in culture, 8 wounds yielded no growth and the remaining 3 wounds yielded ≥ 1 bacterial species (Table 1). The observed agreement for negative culture results was 92% (48/52 wounds; κ coefficient, 0.75 [95% CI, 0.5 to 0.9]). All wounds for which swab culture results were negative also had negative biopsy specimen culture results. However, there were 4 wounds from which biopsy specimens were culture negative and the respective swabs were culture positive (each with a single organism). The organisms isolated from those swabs were Aeromonas hydrophilia, Pasteurella sp, S canis, and Enterococcus faecium. Considering only these 4 dogs, 1 had a chronic wound and 3 had acute wounds, 2 were receiving antimicrobials and 2 were not, and 2 had no concurrent illness and 2 did have concurrent illness (1 dog had a mast cell tumor and hemangiosarcoma and 1 dog had a stomach mass [for which there was no histologic diagnosis]).
With regard to the treatment choices of the 2 culture results evaluators, overall agreement in clinical judgment was noted in 40 of 52 (76.9%) cases (κ coefficient, 0.38 [95% CI, 0.08 to 0.69]). For 33 of the 52 (63.5%) wounds, both evaluators agreed that the dogs would be similarly treated despite the difference in culture results for the 2 specimen types. In contrast, for 7 (13.5%) dogs with discrepant culture results, both observers would agreeably choose a different treatment plan based on the differing culture results. For 12 (23.1%) wounds for which the culture results for the 2 types of specimen differed, only 1 evaluator would have chosen a different treatment plan on the basis of the 2 results.
Discussion
The study of the present report investigated culture results for specimens of dog wounds collected by 1 of 2 methods: swabbing (Levine technique) and tissue biopsy. The study findings supported our hypothesis that superficial swabs and tissue biopsy specimens of dog wounds are equally suitable for culture of wound-associated bacteria. For both techniques, recovery of clinical isolates was effective, with a mean culture yield for each specimen type of 3.4 species/wound. The swab and biopsy specimen culture results were identical for 21.2% (11/52) of the wounds.
Although the difference was not significant, swab culture had a higher bacterial recovery rate than that of biopsy specimen culture (85% vs 77%), which was consistent with findings of a previous study.15 In that study of 52 dogs (1 wound/dog), there were higher numbers of culture-positive wounds; 94.2% of wound swabs and 86.5% of biopsies specimens yielded positive culture results. Enrollment of only dogs with clinically infected wounds could account for the higher number of positive cultures observed in that study.
Although the culture-positive results in the present study were often not identical, culture of each specimen type commonly resulted in recovery of S pseudintermedius, S canis, P canis, E coli, and S minor at a similar frequency. Of the remaining bacteria isolated, E faecalis and P aeruginosa were noticeably more frequently recovered by cultures of swabs. Overall, these findings were consistent with those of previous studies,18,19,20 in which these bacteria were most commonly isolated from dog wounds and surgical site infections, with S pseudintermedius being the most prevalent bacterium. Of note, the bacteria recovered by culture of swabs or tissue biopsy specimens in the present study were also commonly isolated from human wounds, regardless of the specimen type, in another study.9 Moreover, 62% (37/60) of bacteria recovered in cultures of swabs and tissue biopsy specimens from diabetic foot ulcers in human patients were identical.7 Results of the present study also indicated that for 30.8% (16/52) of wounds, the swab culture resulted in isolation of additional bacteria, compared with the results of biopsy specimen culture. The latter finding was consistent with the previous human study7 in which culture of swabs resulted in isolation of additional bacteria, compared with findings for biopsy specimen cultures, in 20% (12/60) of patients.
Interestingly, in their study of the influence of sampling method on bacteriologic culture results for 52 dogs with infected wounds, Concannon et al15 found that culture of biopsy specimens resulted in less bacterial yield (mean culture yield, 1.87 bacterial species/wound) than culture of swabs (mean culture yield, 2.29 bacterial species/wound). In the present study, cultures of the 2 types of specimen yielded the same number of bacteria (mean culture yield, 3.4 bacterial species/wound), but the swab cultures resulted in negative results less frequently, albeit not significantly, than did the biopsy specimen cultures. Both our study and that of Concannon et al15 used the Levine swab technique and similar methods for tissue biopsy specimen collection. In the present study, bacteriologic cultures were performed in-house, and specimens were plated within 24 hours after collection. In the previous study,15 specimens were obtained at 1 of 3 hospitals, transported, and plated within 48 hours after collection. Moreover, the swabs were stored in agar gel culturettes, and the tissue biopsy specimens were stored in sterile vacutainer with 1 drop of sterile saline solution. That sample handling differed from that used in the present study, wherein specimens for culture were handled identically (ie, swabs and tissue biopsy specimens were placed within the same type of culturette tube). It is possible that the differences in handling technique were the reason that the culture yields for both swab and tissue biopsy specimens in the present study were greater than findings in the previous study.15 Moreover, the mean culture yield in the present study was greater, despite the fact that more wounds with negative culture results were included. It is possible that differences in sample handling impacted the culture results.
Another difference between the study by Concannon et al15 and the present study was the population of dogs. Concannon et al15 enrolled only dogs with clinically infected wounds, and the present study included dogs with an open wound with or without clinical signs of infection. Therefore, the present study included more specimens that yielded negative culture results. Interestingly, Concannon et al15 reported that specimens collected by all methods from 2 wounds had negative culture results. In that investigation and the present study, all wounds for which the swabs yielded negative culture results had negative culture results for the tissue biopsy specimens. Although broad-reaching conclusions cannot be made from this information because of the limited number of cases, the importance of negative culture results for swabs obtained by use of the Levine technique should not be underrated.
Although the clinical relevance of the types of bacteria cultured from each specimen could not be evaluated in the present study, we determined that the culture result differences for specimens collected by the 2 sampling techniques would not result in large differences in treatment. Similarly, Concannon et al15 concluded that culture technique did not greatly influence the antimicrobial selection made by clinicians. In the present study, at least 1 of the 2 evaluators reported that, clinically, they would have administered the same treatment even in the face of different culture results for 45 of 52 dogs. It seems likely that a difference in culture results between the 2 types of specimen would not result in a change in clinical management for most dogs with skin wounds. However, it is important to note that these determinations were made solely on basis of the culture results provided and that the evaluators were unaware of the clinical status of any of the dogs and their wounds, which may have affected the evaluators’ treatment recommendations.
The present study was limited to assessment of swabs obtained with the Levine technique, and the data cannot be directly used to infer the effectiveness of other swab collection techniques. The Levine technique has been shown to be the most effective swab collection technique in human medicine.8,21,22 Although the Levine technique has been shown to be an effective swab collection technique in veterinary medicine,15 that technique has not been compared with other methods of swabbing in veterinary patients. Additionally, the present study was based on qualitative analysis of the bacteria recovered rather than a semiquantitative approach. Future studies to quantitatively analyze culture results may be warranted. Specimen collection was performed by a diverse group of house officers and senior clinicians, all of whom were trained prior to specimen collection. Furthermore, specimens were obtained from various canine wounds rather than a single wound type (eg, surgical site infections or bite wounds only). Collectively, these facts could be considered limitations of the present study, but in the authors’ opinion, they strengthen the clinical importance of the study findings because the swab technique could be appropriately implemented in a diverse population of wounds by personnel with various levels of clinical expertise. Overall, results of the present study indicated that a swab collected with the Levine technique is a reliable, noninvasive alternative to collection of a tissue biopsy specimen for culture to identify the bacterial population of canine wounds. Furthermore, a negative culture result obtained from a swab collected with the Levine technique should be considered of high clinical relevance.
Acknowledgments
This study was funded by a GINN Research Grant (Texas A&M).
The authors certify that they have no affiliations with or involvement in any organization or entity with any financial or nonfinancial interest in the subject matter or materials discussed in this manuscript.
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