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Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Animals
  6. Identification of isolates
  7. Antimicrobial testing
  8. Statistics
  9. Results
  10. Staphylococcus aureus
  11. Staphylococcus intermedius
  12. Resistance trends in Staphylococcus aureus and Staph. intermedius
  13. Discussion
  14. Effects of site of isolation
  15. Effects of age and sex
  16. Acknowledgements
  17. References

Aims: This study was undertaken to investigate whether the antibiotic resistance of Staphylococcus aureus and Staph. intermedius varies with the site of isolation, sex or age of dogs. Methods and Results: A total of 867 isolates of Staph. aureus and 1339 isolates of Staph. intermedius were obtained from nose, eye, ear, reproductive extremity, urine, abscess, skin and throat isolates. Staphylococcus intermedius isolates were isolated most frequently and adult and male dogs were more common compared with juveniles and/or female dogs. Antimicrobial resistance was commonly found for penicillin G, lincomycin, tetracycline and trimethoprim-sulphamethoxazole in both Staphylococcus species. Surprisingly, we detected significant resistance to cloxacillin in male (67·1%) and female (69·4%) Staph. aureus isolates, irrespective of the anatomical site of isolation. The resistance or susceptibility of isolates of Staph. aureus from reproductive extremities and isolates of Staph. intermedius from ear, eye and abscess sites was associated with the age of the animal. Conclusions: Antimicrobial susceptibilities in Staph. aureus and Staph. intermedius often differed with regard to the site of isolation, sex and age of the animal. Significance and Impact of the Study: Increasing antimicrobial resistance in staphylococci in veterinary medicine complicates the empirical selection of antimicrobial agents. These complications reveal a continuously evolving, complicated multifactoral process of the site of isolation, sex and age of the animal.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Animals
  6. Identification of isolates
  7. Antimicrobial testing
  8. Statistics
  9. Results
  10. Staphylococcus aureus
  11. Staphylococcus intermedius
  12. Resistance trends in Staphylococcus aureus and Staph. intermedius
  13. Discussion
  14. Effects of site of isolation
  15. Effects of age and sex
  16. Acknowledgements
  17. References

Staphylococci are routinely isolated from domestic animals in veterinary clinical practice (Euzeby 1997). Besides their role as commensals on mucosal surfaces and the skin, staphylococci are often involved in a wide variety of diseases in animals (Kloos 1980). Staphylococcal infections are frequently treated with antibiotics and, consequently, antibiotic resistance and/or acquired resistance have developed (Normand et al. 2000). Staphylococcus aureus is frequently associated with suppurative infections and is recognized as a resident member of the microflora of the skin of humans and dogs (Kloos 1990). In dogs, Staph. intermedius has been considered as one of the major coagulase-positive species of Staphylococcus (Phillips and Williams 1984; Cox et al. 1988). Both Staph. intermedius and Staph. aureus have been isolated in very similar percentages from the skin and other sites (Biberstein et al. 1984).

Only a few preliminary studies have been conducted to determine whether the antibiotic susceptibility of a specific bacterium varies with (i) site of infection; (ii) sex and (iii) age of the individual (Flournoy et al. 1979; Flournoy et al. 1989; Hoekstra and Paulton 1996). The purpose of this study was to examine two common veterinary isolates, Staph. aureus and Staph. intermedius, with particular reference to three factors: (i) the antimicrobial susceptibility of Staph. aureus and Staph. intermedius isolated from various anatomical sitesin dogs to determine whether the site of isolation influences antimicrobial susceptibility for a specific bacterium (Hoekstra and Paulton 1996); (ii) the antimicrobial susceptibility of Staph. aureus and Staph. intermedius isolated from male and female dogs given the probable influence of sex in terms of virulence and antibiotic sensitivity (Picard and Goullet 1989) and (iii) the effect of age to determine whether antibiotic resistance correlated with age of the animal, as previously claimed (Lu et al. 1978).

Animals

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Animals
  6. Identification of isolates
  7. Antimicrobial testing
  8. Statistics
  9. Results
  10. Staphylococcus aureus
  11. Staphylococcus intermedius
  12. Resistance trends in Staphylococcus aureus and Staph. intermedius
  13. Discussion
  14. Effects of site of isolation
  15. Effects of age and sex
  16. Acknowledgements
  17. References

Specimens were obtained from adult and juvenile dogs of both sexes submitted to the Central Laboratory for Veterinarians (Langley, British Columbia, Canada) from veterinary clinics in the province for identification and susceptibility testing over a 6-year period (1994–1999). Animals selected for this study had no known history of prior antibiotic therapy. The bacterial isolates were identified and labelled as to source, male or female, adult (>1 year) or juvenile (<1 year) and the site ofinfection. Anatomical sites from which samples were submitted included the nose, eye, ear, reproductive extremities, urine, abscess, skin and throat.

Identification of isolates

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Animals
  6. Identification of isolates
  7. Antimicrobial testing
  8. Statistics
  9. Results
  10. Staphylococcus aureus
  11. Staphylococcus intermedius
  12. Resistance trends in Staphylococcus aureus and Staph. intermedius
  13. Discussion
  14. Effects of site of isolation
  15. Effects of age and sex
  16. Acknowledgements
  17. References

After growth, staphylococcal isolates were identified according to their characteristics as outlined in Bergey's Manual of Determinative Bacteriology(Holt et al. 1994) and the Manual of Clinical Microbiology (Murray et al. 1999). Only isolates identified as Staph. aureus and Staph. intermedius were selected for this study. After growth on sheep blood agar, Staph. aureus was identified on the basis of colony characteristics, Gram stain, pigment production, acid production on d-mannitol, free coagulase and the slide test for detection of clumping factor. Colonies identified as Staph. intermedius were differentiated from Staph. aureus by lack of pigment production (Kloos and Schleifer 1975), lack of acid production from d-manniotol (Sneath 1986), lack of beta-haemolysis and variability with the slide test (Balows 1991). Similarities were discriminated using the Accu-Staph (Anachemia Science, Montreal Quebec, Canada) or API Staph. (Fisher Science, Ottawa Ontario, Canada) identification kits.

Antimicrobial testing

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Animals
  6. Identification of isolates
  7. Antimicrobial testing
  8. Statistics
  9. Results
  10. Staphylococcus aureus
  11. Staphylococcus intermedius
  12. Resistance trends in Staphylococcus aureus and Staph. intermedius
  13. Discussion
  14. Effects of site of isolation
  15. Effects of age and sex
  16. Acknowledgements
  17. References

Once samples were identified, the staphylococcal strains were tested for susceptibility to antibiotics by disc agar diffusion as previously described (Hoekstra and Paulton 1996). Discs ofantibiotics commonly used in clinical veterinary medicinefor suppurative diseases were tested: cephalothin (30 µg), chloramphenicol (30 µg), amoxicillin/clavulanic acid (30 µg), cloxacillin (5 µg), enrofloxin (5 µg), erythromycin (15 µg), penicillin G (10 U), lincomycin (2 µg), tetracycline (30 µg) and trimethoprim-sulphamethoxazole (25 µg). After measuring the zones of inhibition, the strains were classified as sensitive, intermediate or resistant to the drug according tothe literature and manufacturer (Jorgensen et al. 1999; BD,Franklin Lakes, NJ, USA).

Statistics

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Animals
  6. Identification of isolates
  7. Antimicrobial testing
  8. Statistics
  9. Results
  10. Staphylococcus aureus
  11. Staphylococcus intermedius
  12. Resistance trends in Staphylococcus aureus and Staph. intermedius
  13. Discussion
  14. Effects of site of isolation
  15. Effects of age and sex
  16. Acknowledgements
  17. References

Results are expressed as per cent resistant or susceptible and considered statistically significant for P < 0·05. For comparison between unpaired groups, the Student's t-test or Mann–Whitney test was used as appropriate. Statistical analysis using the two-factor analysis of variance was used to determine whether there was a significant difference between different sites for a specific antibiotic and a specific bacterium (Zar 1984).

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Animals
  6. Identification of isolates
  7. Antimicrobial testing
  8. Statistics
  9. Results
  10. Staphylococcus aureus
  11. Staphylococcus intermedius
  12. Resistance trends in Staphylococcus aureus and Staph. intermedius
  13. Discussion
  14. Effects of site of isolation
  15. Effects of age and sex
  16. Acknowledgements
  17. References

A total of 867 isolates of Staph. aureus and 1339 isolates of Staph. intermedius was obtained from male and female, adult and juvenile dogs from 1994 to 1999. Table 1 shows the frequency of isolation of these staphylococcal isolates according to the sex and age of the animal and anatomical site of infection.

Table 1.  Frequency and distribution of Staphylococcus aureus and Staph. intermedius isolated from eight anatomical sites of 2206 dogs (1994–1999)
Anatomical siteStaph. aureusStaph. intermediusTotal
MAMJFAFJMAMJFAFJ
  1. MA, Adult male; MJ, juvenile male; FA, adult female; FJ, juvenile female.

Nose 36 17 62 38 85 39 35 13 325
Eye 14 16 30  5 66 35 29 22 217
Ear 67 15 46  4118 34 39 15 338
Urine 40 10 35 61 20 21 38 26 251
Reproductive 21 25 59 50 42 18 56 29 300
Abscess 53 10 52 10 48 30 37 12 252
Skin  1 16 30  7104 39102 12 311
Throat  8  2 21  6 57 28 62 28 212
Total2401113351815402443981572206

The study included more adult dogs (68·6%) than juveniles (P < 0·05) and male dogs accounted for just over half (51·5%) of all isolates. Overall, Staph. intermedius was isolated more frequently (1339 (60·7%) isolates) than Staph. aureus (867 (39·3%) isolates). In male dogs, Staph. intermedius (69·1%) was isolated more frequently (P < 0·05) than Staph. aureus (30·9%). However, there was no significant difference in the frequency of isolation of Staph. aureus (48·2%) and Staph. intermedius (51·8%) from female dogs.

Staphylococcus aureus

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Animals
  6. Identification of isolates
  7. Antimicrobial testing
  8. Statistics
  9. Results
  10. Staphylococcus aureus
  11. Staphylococcus intermedius
  12. Resistance trends in Staphylococcus aureus and Staph. intermedius
  13. Discussion
  14. Effects of site of isolation
  15. Effects of age and sex
  16. Acknowledgements
  17. References

The antimicrobial susceptibility of Staph. aureus isolates from male and female and adult and juvenile dogs is shown with anatomical site of isolation in Fig. 1.

image

Figure 1. Antimicrobial susceptibilities of Staphylococcus aureus isolated from the nose ( bsl00018), eye ( bsl00000), ear ( bsl00001), urine ( bsl00020), reproductive extremities ( bsl00023), abscess ( bsl00022), skin ( bsl00001) and throat ( bsl00003) of (a) adult male dogs (n=240); (b) juvenile male dogs (n=113); (c) adult female dogs (n=335) and (d)juvenile female dogs (n=181) from 1994 to 1999. KF, cephalexin; C, chloramphenicol; AMC, amoxicillin/clavulenic acid; OB, cloxacillin; ENO, enrofloxin; E, erythromycin; P, penicillin; MY, lincomycin; Te, tetracycline and Sxt, trimethoprim-sulphamethoxazole

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Antimicrobial resistance to at least one antimicrobial agent was frequently detected in male (91·2%) and female (95·5%) isolates and multidrug resistance (i.e. > two antimicrobial agents) was observed in 67·3% of all isolates. In both male and female dogs, resistance to cloxacillin (M, 67·1%; F, 69·4%), lincomycin (M, 79·5%; F, 77·2%), penicillin G (M, 73·8%; F, 74·5%) and trimethoprim-sulphamethoxazole (M, 74·1%; F, 74·7%) was common. The most effective antimicrobial agent in both male and female dogs was amoxicillin/clavulanic acid in ear isolates (M, 2·4%; F, 5·4%).

Table 2 shows those anatomical sites where isolates of Staph. aureus showed a greater resistance or susceptibility to antimicrobial agents than isolates from other sites. In most situations, isolates were more resistant regardless of the sex or age of the animal. For example, 94% of all isolates of Staph. aureus from the ear were resistant to trimethoprim-sulphamethoxazole, which was significantly different from all other anatomical sites (P < 0·001). However, the resistance or susceptibility of isolates from the reproductive extremities was associated with the age of the animal. Isolates from older animals were significantly more resistant to enrofloxin and susceptible to cephalothin compared with all other anatomical sites and those from younger animals were more susceptible to enrofloxin and resistant to cephalothin than isolates from other sites. Interestingly, isolates of Staph. aureus from the nose were more susceptible to penicillin G compared with isolates from all other sites.

Table 2.  Anatomical sites where Staphylococcus aureus showed a greater resistance (R) or susceptibility (S) to antimicrobial agents
 NoseThroatEarEyeReproductiveUrineAbscessSkin
  • *

    P < 0·05.

  • P < 0·01.

  • P < 0·001.

  • M, Male; F, female; A, adult; J, juvenile.

Cephalothin  R60% S89%MA S72%FA R58%MJ R56%FJ   
Penicillin GS52%*       
CloxacillinR82%*R78%*  R81%R91%  
Amoxicillin/clavulanic acid     R69%  
Enrofloxin    R61%MA R68%FA S78%MJ* S87%FJ*   
Chloramphenicol
ErythromycinR72%      R73%
Lincomycin  R93% R94%   
Tetracycline  R86%R86%    
Trimethoprim-sulphamethoxazole  R94%     

Staphylococcus intermedius

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Animals
  6. Identification of isolates
  7. Antimicrobial testing
  8. Statistics
  9. Results
  10. Staphylococcus aureus
  11. Staphylococcus intermedius
  12. Resistance trends in Staphylococcus aureus and Staph. intermedius
  13. Discussion
  14. Effects of site of isolation
  15. Effects of age and sex
  16. Acknowledgements
  17. References

The antimicrobial susceptibility of Staph. intermedius isolates from male and female and adult and juvenile dogs is shown with the anatomical site of isolation in Fig. 2.

image

Figure 2. Antimicrobial susceptibilities of Staphylococcus intermedius isolated from the nose ( bsl00018), eye ( bsl00000), ear (bsl00001), urine ( bsl00020), reproductive extremities ( bsl00023), abscess ( bsl00022), skin ( bsl00001) and throat ( bsl00003) of (a) adult male dogs (n=540); (b) juvenile male dogs (n=244); (c) adult female dogs (n=401) and(d) juvenile female dogs (n=157) from 1994 to 1999. KF, cephalexin; C, chloramphenicol; AMC, amoxicillin/clavulenic acid; OB, cloxacillin; ENO, enrofloxin; E, erythromycin; P, penicillin; MY, lincomycin; Te, tetracycline and Sxt, trimethoprim-sulphamethoxazole

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In all, 93·7% of male and 96·2% of female dogs were resistant to at least one antimicrobial agent and multidrug resistance (i.e. > two antimicrobial agents) was observed in 51·3% of all isolates. Cephalothin was the most effective antimicrobial agent in males from isolates of urine (2·0%) and abscesses (3·0%) and in females from isolates of abscesses (3·0%).

Table 3 shows those anatomical sites where isolates of Staph. intermedius showed a greater resistance or susceptibility to antimicrobial agents than isolates from other sites. In some situations, isolates were more resistant irrespective of the sex or age of the animal. For example, 45% of all isolates of Staph. intermedius from the nose were resistant to enrofloxin, which was significantly different from all other anatomical sites (P < 0·05). Like Staph. aureus, the resistance or susceptibility of some isolates of Staph. intermedius was associated with the age of the animal. Isolates from younger males were significantly (P < 0·001) more resistant to cephalothin and erythromycin in ear isolates and significantly (P < 0·001) more resistant to cloxacillin, amoxicillin/clavulanic acid and chloramphenicol in abscess isolates compared with isolates from other age groups. Isolates from older males were significantly more resistant to cloxacillin and amoxicillin/clavulanic acid in eye isolates, cephalothin in reproductive extremities and tetracycline in urine isolates compared with isolates from other age groups.

Table 3.  Anatomical sites where Staphylococcus intermedius showed a greater resistance (R) or susceptibility (S) to antimicrobial agents
 NoseThroatEarEyeReproductiveUrineAbscessSkin
  • M, Male; A, adult; J, juvenile.

  • *

    P < 0·05.

  • P < 0·01.

  • P < 0·001.

Cephalothin  R80%MJ R80%MA   
Penicillin G
CloxacillinR60%*  R85%MA  R85%MJ 
Amoxicillin/clavulanic acidR50%MA  R60%MA  R50%MJ 
EnrofloxinR45%*       
ChloramphenicolR50%MJ     R47%MJ 
ErythromycinR44%* R85%MJ     
Lincomycin
Tetracycline    S67%*R95%MAS63%* 
Trimethoprim-sulphamethoxazole

Resistance trends in Staphylococcus aureus and Staph. intermedius

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Animals
  6. Identification of isolates
  7. Antimicrobial testing
  8. Statistics
  9. Results
  10. Staphylococcus aureus
  11. Staphylococcus intermedius
  12. Resistance trends in Staphylococcus aureus and Staph. intermedius
  13. Discussion
  14. Effects of site of isolation
  15. Effects of age and sex
  16. Acknowledgements
  17. References

Differences in susceptibility were detected between Staph. aureus and Staph. intermedius. Isolates of Staph. aureus were significantly more resistant to cloxacillin (P < 0·001) and erythromycin (P < 0·05) compared with the collective sum of all Staph. intermedius isolates. We also detected a trend (P=0·53) of increased resistance to enrofloxin in Staph. aureus compared with Staph. intermedius isolates. In addition, a persistent, marked resistance (P < 0·001) of ear isolates to cephalothin was found for Staph. aureus and Staph. intermedius when compared with all anatomical sites.

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Animals
  6. Identification of isolates
  7. Antimicrobial testing
  8. Statistics
  9. Results
  10. Staphylococcus aureus
  11. Staphylococcus intermedius
  12. Resistance trends in Staphylococcus aureus and Staph. intermedius
  13. Discussion
  14. Effects of site of isolation
  15. Effects of age and sex
  16. Acknowledgements
  17. References

The prevalence and degree of antimicrobial resistance in suppurative infections in veterinary medicine are increasing worldwide (Werckenthin et al. 2001). Staphylococci have shown a frequent and rapid development and spread ofantimicrobial resistance, particularly in nosocomial infections. Unfortunately, this development has not been documented continuously in veterinary medicine. The present investigation has examined the clinical prevalence and antibiotic susceptibility of two common veterinary staphylococci, Staph. aureus and Staph. intermedius, in dogs over a 6-year period. It has shown that the site of isolation of a given bacterium may influence its antibiotic susceptibility in vitro and that antimicrobial susceptibilities of isolates from dogs may differ with the sex and age of the animal.

Effects of site of isolation

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Animals
  6. Identification of isolates
  7. Antimicrobial testing
  8. Statistics
  9. Results
  10. Staphylococcus aureus
  11. Staphylococcus intermedius
  12. Resistance trends in Staphylococcus aureus and Staph. intermedius
  13. Discussion
  14. Effects of site of isolation
  15. Effects of age and sex
  16. Acknowledgements
  17. References

The ability of staphylococci to persist in adverse environments and their extraordinary potential to develop antimicrobial resistance may contribute to resistance patterns in sites of isolation (Normand et al. 2000).

In the present study we determined that Staph. aureus andStaph. intermedius were more resistant to specific antimicrobials compared with isolates from other sites.

We identified 237 and 358 isolates of Staph. aureus from male and female dogs (irrespective of age), respectively, and 103 isolates of Staph. intermedius from the nose (irrespective of sex and age) which were resistant to cloxacillin. The pattern of susceptibility of Staphylococcus spp. from veterinary clinical specimens to synthetic penicillinase-resistant penicillins, such as cloxacillin, has not often been reported (Phillips and Williams 1984; Medleau and Blue 1988) or detectable (Kruse et al. 1996). However, a significant correlation has been reported between percentages of methicillin resistance and the usage of cloxacillin in clinical isolates of Staph. epidermidis (Lyytikainen et al. 1996) and it has been suggested that methicillin-resistant Staph. aureus (MRSA) are among those giving therapeutic problems in veterinary medicine (Jeljaszewicz et al. 2000). More importantly, it may be of greater concern that MRSA isolates detected in animal staphylococci have mostly been assumed to originate from human sources (Seguin et al. 1999; Aarestrup and Jensen 1998) where methicillin resistance is a growing problem (Witte 1999).

Resistance to penicillin, lincomycin and sulphonamides is often reported in staphylococci (Cox et al. 1984; Phillips and Williams 1984) while resistance to newer antibiotics, such as the fluoroquinolones, is to date still comparatively low (Pedersen and Wegener 1995; Werckenthin et al. 2001). However, newer broad-spectrum antibiotics, such as enrofloxin, are increasingly being used for the treatment of companion animals and resistance rates may also increase in staphylococci with their frequent use (Lloyd et al. 1999). Surprisingly, tetracycline is still an effective antimicrobial in reproductive and abscess sites (Schreiner 1984).

Our findings of increased resistance to cepthalothin in ear isolates is consistent with our previous reports (Hoekstra and Paulton 1996) and supports the continued resistance of ear isolates from dogs to cephalothin. This significant trend has not been reported in humans where cephalosporin resistance is significantly lower and ranges from 20 to 30% (Nishijima and Kurokawa 2002).

Effects of age and sex

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Animals
  6. Identification of isolates
  7. Antimicrobial testing
  8. Statistics
  9. Results
  10. Staphylococcus aureus
  11. Staphylococcus intermedius
  12. Resistance trends in Staphylococcus aureus and Staph. intermedius
  13. Discussion
  14. Effects of site of isolation
  15. Effects of age and sex
  16. Acknowledgements
  17. References

The sex and age of individuals have been suggested as predisposing factors for the development of certain bacterial infections (Picard and Goullet 1989). Such data might provide useful insights into dynamic aspects of age- and sex-related processes involved in the development of antibiotic resistance.

In the present study, we found that the age of the animal was associated with different patterns of antimicrobial resistance for enrofloxin, cephalothin, chloramphenicol and tetracycline and report a unique inverse relationship for cephalothin and enrofloxin and adult and juvenile reproductive extremity isolates. The higher resistance of enrofloxin in adult dogs supports their increased use in veterinary medicine (Schwarz and Chaslus-Dancla 2001). However, the significantly lower resistance of isolates from juveniles to enrofloxin in vitro may not justify its use in vivo, given the contraindicated use of enrofloxacin in growing animals (Norrby 1991). Additionally, the frequent use of cephalosporins in younger individuals (Bergus et al. 2001) suggests that modifications in antibiotic usage patterns may have salutary effects on antimicrobial resistance patterns in adults.

Although chloramphenicol and tetracycline resistance is commonly reported in staphylococci (Schwarz and Wang 1993; Schwarz et al. 1998; Alekshun and Levy 2000), our findings of increased resistance in isolates from older animals have not been previously reported. It has even been reported that these antimicrobial agents may be more effective in adults since clinical use in juveniles is limited due to age-associated toxicity (Lewis and Reeves 1994).

Sex-related differences were also associated with antimicrobial resistance to penicillin G, tetracycline and erythromycin. Erythromycin resistance was observed in Staph. intermedius isolates in all sites of isolation for adult females compared with adult males. Other studies have reported resistance to erythromycin by Staph. intermedius (Eady et al. 1993; Pellerin et al. 1998; Boerlin et al. 2001) but have not identified sex-related differences in antimicrobial susceptibility. To our knowledge, this is the first report of sex-related differences and antimicrobial resistance in Staph. aureus and Staph. intermedius isolated from dogs. A mechanism for these sex-related associations of antimicrobial resistance still remains to be determined. Nevertheless, sex-related differences suggest consideration of sex and the bacteria isolated when prescribing antibiotics.

The access of the staphylococci to a wide gene pool (as is present in mixed bacterial populations on the skin and mucosal membranes) may favour the acquisition of resistance genes (Mazel and Davies 1999). Thus, increasing rates of antimicrobial resistance and the introduction of newer antimicrobial agents increase the importance of surveillance programs. Our efforts to explore the inter-relationships between antimicrobial resistance of Staph. aureus and Staph. intermedius and their site of isolation, age and sex of the dog yielded highly complex patterns of significant associations. The emergence of antibiotic resistance in the dog to newer antimicrobial agents was reported. This study once more emphasizes the need for bacterial culture with species identification and susceptibility testing of site-specific isolates in order to choose appropriate antimicrobial agents.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Animals
  6. Identification of isolates
  7. Antimicrobial testing
  8. Statistics
  9. Results
  10. Staphylococcus aureus
  11. Staphylococcus intermedius
  12. Resistance trends in Staphylococcus aureus and Staph. intermedius
  13. Discussion
  14. Effects of site of isolation
  15. Effects of age and sex
  16. Acknowledgements
  17. References
  • Aarestrup, F.M. and Jensen, N.E. (1998) Development of penicillin resistance among Staphylococcus aureus isolated from bovine mastitis in Denmark and other countries. Microbiology of Drug Resistance 4, 247256.
  • Alekshun, M.N. and Levy, S.B. (2000) Bacterial drug resistance: response to survival threats. In Bacterial Stress Responses pp. 323366. Washington, DC: ASM Press.
  • Balows, A. (1991) Manual of Clinical Microbiology, 5th edn. Washington, DC: American Society of Microbiology.
  • Bergus, G.R., Levy, S.M., Kirchner, H.L., Warren, J.J. and Levy, B.T.A. (2001) A prospective study of antibiotic use and associated infections in young children. Paediatric and Perinatal Epidemiology 15, 6167.DOI: 10.1046/j.1365-3016.2001.00326.x
  • Biberstein, E.L., Jang, S.S. and Hirsh, D.C. (1984) Species distribution of coagulase-positive staphylococci in animals. Journal of Clinical Microbiology 19, 610615.
  • Boerlin, P., Burnens, A.P., Frey, J., Kuhnert, P. and Nicolet, J. (2001) Molecular epidemiology and genetic linkage of macrolide and aminoglycoside resistance in Staphylococcus intermedius of canine origin. Veterinary Microbiology 20, 155169.
  • Cox, H.U., Hoskins, J.D., Newman, S.S., Foil, C.S., Turnwald, G.H. and Roy, A.F. (1988) Temporal study of staphylococcal species on healthy dogs. American Journal of Veterinary Research 49, 747751.
  • Cox, H.U., Hoskins, J.D., Roy, A.F., Newman, S.S. and Luther, D.G. (1984) Antimicrobial susceptibility of coagulase-positive staphylococci isolated from Louisiana dogs. American Journal of Veterinary Research 45, 20392042.
  • Eady, E.A., Ross, J.I., Tipper, J.L., Walters, C.E., Cove, J.H. and Noble, W.C. (1993) Distribution of genes encoding erythromycin ribosomal methylases and an erythromycin efflux pump in epidemiologically distinct groups of staphylococci. Journal of Antimicrobial Chemotherapy 31, 211217.
  • Euzeby, J.P. (1997) List of bacterial names with standing in nomenclature: a folder available on the internet. International Journal of Systemic Bacteriology 47, 590592.
  • Flournoy, D.J., Murray, C.K. and Vernon, A.N. (1989) A statistical analysis on the relationship of organism and site of infection to antimicrobial susceptibilities. Methods and Findings in Experimental and Clinical Pharmacology 11, 725729.
  • Flournoy, D.J., Parker, N.S. and Sackett, W.R. (1979) Variations in antimicrobial susceptibility patterns among three hospitals. Laboratory Medicine 10, 3941.
  • Hoekstra, K.A. and Paulton, R.J.L. (1996) Antibiotic sensitivity of Staphylococcus aureus and Staph. intermedius of canine and feline origin. Letters in Applied Microbiology 22, 192194.
  • Holt, J.G., Krieg, N.R., Sneathm, P.H.A., Staley, J.T. and Williams, S.T. (1994) Bergey's Manual of Determinative Bacteriology, 9th edn. Baltimore, MD: Williams and Williams.
  • Jeljaszewicz, J., Mlynarczyk, G. and Mlynarczyk, A. (2000) Antibiotic resistance in Gram-positive cocci. International Journal of Antimicrobial Agents 16, 473478.DOI: 10.1016/S0924-8579(00)00289-2
  • Jorgensen, J.H., Tunridge, J.D. and Washington, J.A. (1999) Antibacterial Susceptibility Tests: Dilution and Disk Diffusion Methods. In Manual of Clinical Microbiology, 7th edition eds Murray, P.R., Baron, E.J., Pfaller, M.A., Tenover, F.C. and Yolken, R.H. Washington, DC: American Society for Microbiology.
  • Kloos, W.E. (1980) Natural populations of the genus Staphylococcus. Annual Review of Microbiology 34, 559592.
  • Kloos, W.E. (1990) Systematics and the natural history of staphylococci. Journal of Applied Bacteriology Symposium Suppl.69, 25S37S.
  • Kloos, W.E. and Schleifer, K.H. (1975) Simplified scheme for routine identification of human Staphylococcus species. Journal of Clinical Microbiology 1, 8288.
  • Kruse, H., Hofshagen, M., Thoresen, S.I., Bredal, W.P., Vollset, I. and Soli, N.E. (1996) The antimicrobial susceptibility of Staphylococcus species isolated from canine dermatitis. Veterinary Research Communications 20, 205214.
  • Lewis, D.A. and Reeves, D.S. (1994) Antibiotics at the extremes of age: choices and constraints. Journal of Antimicrobial Chemotherapy 34 (Suppl. A), 1118.
  • Lloyd, D.H., Lamport, A.I., Noble, W.C. and Howell, S.A. (1999) Fluoroquinolone resistance in Staphylococcus intermedius. Veterinary Dermatology 10, 249252.
  • Lu, Y.S., Ringler, D.H. and Park, J.S. (1978) Characterization of Pasteurella multocida isolates from the nares of healthy rabbits with pneumonia. Laboratory Animal Science 28, 691697.
  • Lyytikainen, O., Vaara, M., Jarviluoma, E., Rosenqvist, K., Tiittanen, L. and Valtonen, V. (1996) Increased resistance among Staphylococcus epidermidis isolates in a large teaching hospital over a 12-year period. European Journal of Clinical Microbiology and Infectious Diseases 15, 133138.
  • Mazel, D. and Davies, J. (1999) Antibiotic resistance in microbes. Cellular and Molecular Life Sciences 56, 742754.
  • Medleau, L. and Blue, J.L. (1988) Frequency and antimicrobial susceptibility of Staphylococcus spp. isolated from feline skin lesions. Journal of American Veterinary Medical Association 193, 10801081.
  • Murray, P.R., Baron, E.J., Pfaller, M.A., Tenover, F.C. and Yolken, R.H. (1999) Manual of Clinical Microbiology, 7th edn. Washington, DC: American Society for Microbiology.
  • Nishijima, S. and Kurokawa, I. (2002) Antimicrobial resistance of Staphylococcus aureus isolated from skin infections. International Journal of Antimicrobial Agents 19, 241243.
  • Normand, E.H., Gibson, N.R., Reid, S.W., Carmichael, S. and Taylor, D.J. (2000) Antimicrobial-resistance trends in bacterial isolates from companion animal community practice in the UK. Preventative Veterinary Medicine 46, 267278.
  • Norrby, S.R. (1991) Side-effects of quinolones: comparisons between quinolones and other antibiotics. European Journal of Clinical Microbiology and Infectious Diseases 10, 378383.
  • Pedersen, K. and Wegener, H.C. (1995) Antimicrobial susceptibility and rRNA gene restriction patterns among Staphylococcus intermedius from healthy dogs and from dogs suffering from pyoderma or otitis externa. ACTA Veterinaria Scandinavica (Copenhagen) 36, 335342.
  • Pellerin, J.L., Bourdeau, P., Sebbag, H. and Person, J.M. (1998) Epidemio-surveillance of antimicrobial compound resistance of Staphylococcus intermedium clinical isolates from canine pyodermas. Comparative Immunology, Microbiology and Infectious Diseases 21, 115133.DOI: 10.1016/S0147-9571(97)00026-X
  • Phillips, W.E. Jr and Williams, B.J. (1984) Antimicrobial susceptibility patterns of canine Staphylococcus intermedius isolates from veterinary clinical specimens. American Journal of Veterinary Research 45, 23762379.
  • Picard, B. and Goullet, P. (1989) Correlation between electrophoretic types B1 and B2 of carboxylesterase B and sex of patients in Escherichia coli urinary tract infections. Epidemiology and Infection 103, 97103.
  • Schreiner, A. (1984) Use of lindamycin in lower respiratory tract infections. Scandinavian Journal of Infectious Diseases (Supp) 43, 5661.
  • Schwarz, S. and Chaslus-Dancla, E. (2001) Use of antimicrobials in veterinary medicine and mechanisms of resistance. Veterinary Research 32, 201225.
  • Schwarz, S., Roberts, M.C., Werckenthin, C., Pang, Y. and Lange, C. (1998) Tetracycline resistance in Staphylococcus spp. from domestic animals. Veterinary Microbiology 63, 217227.
  • Schwarz, S. and Wang, Z. (1993) Tetracycline resistance in Staphylococcus intermedius. Letters in Applied Microbiology 17, 8891.
  • Seguin, J.C., Walker, R.D., Caron, J.P., Kloos, W.E., George, C.G., Hollis, R.J., Jones, R.N. and Pfaller, M.A. (1999) Methicillin-resistant Staphylococcus aureus outbreak in a veterinary teaching hospital: potential human-to-animal transmission. Journal of Clinical Microbiology 37, 14591463.
  • Sneath, P.H.A. (1986) Bergey's Manual of Systematic Bacteriology. Vol.2, pp. 10151050. Baltimore, MD: Williams and Wilkins.
  • Werckenthin, C., Cardoso, M., Martel, J.-L. and Schwarz, S. (2001) Antimicrobial resistance in staphylococci from animals with particular reference to bovine Staphylococcus aureus and porcine Staphylococcus hyicus, and canine Staphylococcus intermedius. Veterinary Research 32, 341362.
  • Witte, W. (1999) Antibiotic resistance in gram-positive bacteria: epidemiological aspects. Journal of Antimicrobial Chemotherapy 44 (Suppl. A), 19.DOI: 10.1093/jac/44.suppl_1.1
  • Zar, J.H. (1984) Biostatistical Analysis, 2nd edn. Englewood Cliffs NJ: Prentice Hall.