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Analysis of Antibiotic Susceptibilities of Skin Wound Flora in Hospitalized Dermatology Patients
The Crisis of Antibiotic Resistance Has Come to the Surface
Arthur S. Colsky, PhD, MD;
Robert S. Kirsner, MD;
Francisco A. Kerdel, BSc, MBBS
Arch Dermatol. 1998;134:1006-1009.
ABSTRACT
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Background Results of an ongoing surveillance of antibiotic resistance in hospitalized dermatology patients are presented. Bacterial isolates cultured from patients with skin wounds admitted to a tertiary care dermatology inpatient unit from May 1995 through May 1996 were evaluated for resistance to commonly used antibiotics. Comparison was made with a previous survey of the same inpatient service from 1992. Our results show an alarming trend toward antibiotic resistance.
Observation In superficial skin wounds, Staphylococcus aureus constituted 77% of isolates. In leg ulcers, the frequencies of S aureus and Pseudomonas aeruginosa were approximately equal, constituting 43% and 42% of cultures, respectively. Fifty percent of S aureus isolates from leg ulcers were resistant to oxacillin, with 36% of pseudomonad isolates resistant to ciprofloxacin. In superficial wounds, oxacillin resistance in S aureus approached 25%. A comparison of antibiotic resistance profiles using data collected in 1992 for patients admitted to the same inpatient service revealed a marked increase in oxacillin and ciprofloxacin resistance in S aureus and P aeruginosa in leg ulcers, respectively (from 24% to 50% oxacillin resistance in S aureus and from 9% to 24% ciprofloxacin resistance in P aeruginosa), and superficial wounds (24% to 36% ciprofloxacin resistance in P aeruginosa).
Conclusions This study demonstrates the rapid emergence of antibiotic-resistant bacteria as a problem of growing significance in hospital dermatology and highlights the importance of local surveillance programs to aid in selecting antibiotic treatments.
INTRODUCTION
THE IMPORTANCE of antibiotic resistance in dermatologic practice is increasing. This is of no surprise since staphylococcus, an important skin pathogen, was the first human isolate shown to have acquired the ability to cleave penicillin.1 Despite this early warning, there has been an empirical tendency on the part of dermatologists to prescribe antibiotic treatments. Broad-spectrum agents with gram-positive activity are frequently chosen for skin infections and, likewise, chronic leg ulcers are often treated with quinolone antibiotics such as ciprofloxacin for pseudomonad and other gram-negative coverage. Various data, including a previous study by us,2-5 have suggested the ominous consequences of the overuse of antibiotics regarding the acquisition of antibiotic resistance. In a study published in 1993, ciprofloxacin resistance was encountered in 19% of Pseudomonas aeruginosa and 40% of Staphylococcus aureus organisms isolated from chronic leg ulcers in hospitalized dermatology patients.2 In addition, resistance of S aureus to oxacillin was encountered in 24% of leg ulcer isolates. In the present study, ongoing surveillance of the same patient base has revealed an alarming trend toward the rapid acquisition of antibiotic resistance. The crisis of antibiotic resistance has come rapidly to the (cutaneous) surface.
PATIENTS AND METHODS
A retrospective analysis of aerobic bacterial isolates was performed for patients with superficial skin wounds and leg ulcers admitted to the University of Miami dermatology inpatient service at Cedars Medical Center, Miami, Fla. The types of superficial skin wounds by dermatologic diagnosis are as follows:
Hospital charts were reviewed for consecutive patients who underwent bacterial culture for cutaneous wounds between May 1995 and May 1996. Swab cultures were processed on blood MacConkey phenylethyl alcohol thioglycolate agar. Bacterial isolates cultured at the time of hospital admission were identified. Net susceptibility and resistance profiles for commonly used antibiotics were logged for S aureus and P aeruginosa, the 2 most common bacterial isolates. Trends in antibiotic susceptibilities for these organisms were identified by comparison with values obtained in a previous surveillance study of the same patient base in 1992, including 75 patients with leg ulcers and 48 with superficial skin wounds.2 Statistical analysis was performed using a comparison of proportions. Antibiotic susceptibility testing was performed using an automated laboratory assay (Vitek method, BioMerieux Vitek Inc, Hazelwood, Mo) in the clinical microbiology laboratory of Cedars Medical Center.
RESULTS
A retrospective microbiologic analysis of bacterial wound cultures performed on hospitalized dermatology patients with superficial skin wounds and leg ulcers revealed 194 who had undergone skin wound culture over a 13-month period; charts of these persons were included in the study. The dominant culture composition was as follows:
Table 1 shows the susceptibility patterns of S aureus isolates from patients with leg ulcers. High-level antibiotic resistance was encountered for most agents evaluated. Only one culture (non–methicillin-resistant) was resistant to vancomycin, although the isolate was not retained and this result was unable to be further confirmed. Results of the evaluation of pseudomonad isolates in leg ulcers are also presented in Table 1. Most isolates were sensitive to ticarcillin and gentamicin, and only 1 culture showed resistance to the third-generation cephalosporin ceftazidime.
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Table 1. Antibiograms for Staphylococcus aureus and Pseudomonas aeuginosa in Leg Ulcers*
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A similar analysis was performed for S aureus and P aeruginosa isolates from superficially wounded skin. Table 2 shows the prevalence of antibiotic resistance for staphylococcal cultures. Resistance to tetracycline was encountered in only 6.8% (7/103) of S aureus isolates and all cultures were sensitive to vancomycin. For P aeruginosa, antibiotic resistance in superficial wounds is also presented in Table 2.
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Table 2. Antibiograms for Staphylococcus aureus and Pseudomonas aeruginosa in Superficial Wounds*
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To evaluate trends in antibiotic resistance, a comparison of antibiotic resistance profiles was made using data collected in 1992 for patients admitted to the same inpatient service.2 As shown in Figure 1, there is a marked increase in antibiotic resistance in S aureus isolates. In the previous study, while only 24% and 9% of S aureus isolates were resistant to oxacillin in leg ulcers and superficial wounds, respectively, present data show an increase to 50% (P .05) and 24% (P.06) for the same respective wounds. Similarly, ciprofloxacin resistance has more than doubled in superficial wounds, from 9% to 21% (P.05), while showing a more modest increase in leg ulcers. A marked increase in ciprofloxacin resistance was also seen for P aeruginosa in leg ulcers (Figure 1, C). Currently, 36% of isolates are resistant vs 24% (P.11) resistance in 1992.
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Antibiotic resistance trends for Staphylococcus aureus cultured from leg ulcers (A) and superficial skin wounds (B) and for Pseudomonas aeruginosa cultured from leg ulcers (C): comparison of current antibiograms with those measured in 1992.10
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COMMENT
Our results of research in hospitalized dermatology patients show an alarming trend toward antibiotic resistance.
A comparison of antibiotic susceptibilities of S aureus and P aeruginosa in this survey with those determined in the previous analysis shows the emergence of alarming trends in antibiotic resistance. Resistance of both organisms to ciprofloxacin and of S aureus to oxacillin in both wound types studied were either statistically significant or within limits of a trend toward significance. Particularly striking was the marked increase in oxacillin resistance that occurred over an approximate 4-year period. A doubling of oxacillin resistance was noted in S aureus cultured from leg ulcers when compared with the 1992 survey. Presently, 50% of isolates are resistant to oxacillin compared with 24% previously. This finding can be further appreciated by comparison with the hospital antibiogram, which shows 40% prevalence of oxacillin resistance in S aureus isolates from all sources and which is largely reflective of nosocomial pathogens. In contrast, oxacillin resistance in our leg ulcer population was measured in cultures obtained at the time of admission and may represent an evolving flora rather than dominant nosocomial spread. Even more ominous is a comparison of oxacillin resistance in S aureus cultured from superficial skin wounds. Whereas previously only 9% of isolates were resistant, present data show resistance in 24% of cultures—almost triple in occurrence. The marked increase in oxacillin resistance seen in S aureus from leg ulcers may be due in part to the chronic nature of the wound and frequent antibiotic exposure. Many of these patients have been receiving long-term treatment, including prior hospital admissions as well as multiple courses of antibiotic therapy in the outpatient setting.
The prevalence of S aureus strains resistant to other commonly used antibiotics has also increased markedly. In cultures isolated from leg ulcers, S aureus resistance to most antibiotic agents surveyed has become increasingly prominent. High-level resistance to ciprofloxacin by P aeruginosa in our patient population has also emerged. Our data exceed resistance prevalences reported in national surveillance studies. In a survey of quinolone resistance in 25 US hospitals, overall resistance of P aeruginosa to ciprofloxacin was found to be 7.8%.6 In a European study, ciprofloxacin-resistant P aeruginosa was encountered in 13% of isolates.7 Similar prevalence data for ciprofloxacin-resistant P aeruginosa in multicenter analyses have been published.8-11 Therefore, the greater prominence of ciprofloxacin resistance encountered in our inpatient population cannot be explained solely on the basis of hospital environment or level of care. Rather, our data may reflect trends in dermatologic infections and may be associated with more frequent prescribing of ciprofloxacin by community dermatologists. Moreover, patients with P aeruginosa infections in chronic leg ulcers are frequently treated with ciprofloxacin empirically, which provides a selective pressure for the emergence of resistance to this antibiotic.
This study and others highlight the rapid emergence of antibiotic-resistant bacteria as a problem of growing significance in dermatology.2, 11-13 While national databases contain limited information on this problem, the importance of local trends cannot be overstated.14-18 Antibiotic prescribing habits differ markedly not only in different regions of the world but also within local communities. For example, the widespread use of ciprofloxacin to treat leg ulcer infections in local dermatologic practice may be at the root of the precipitous increase in ciprofloxacin resistance encountered in our inpatient surveillance. Furthermore, as managed care programs restrict the ability to choose agents, prescribing patterns can differ markedly between health care delivery systems bound by formulary constraints. Therefore, as illustrated herein, data on antimicrobial resistance patterns must be monitored with particular attention to local trends. Only then will directed intervention programs be effective in stemming the rapid evolution of antibiotic-resistant bacteria.
AUTHOR INFORMATION
Accepted for publication April 2, 1998.
This study was supported in part by the Department of Dermatology and Cutaneous Surgery, University of Miami, Miami, Fla.
Corresponding author: Francisco A. Kerdel, BSc, MBBS, University of Miami School of Medicine, Department of Dermatology and Cutaneous Surgery, 1600 NW 10th Ave, Miami, FL 33136.
From the Department of Dermatology and Cutaneous Surgery, University of Miami School of Medicine, Miami, Fla.
REFERENCES
1. Rammelkamp CH, Maxon T. Resistance of Staphylococcus aureus to the action of penicillin. Proc Soc Exp Biol Med. 1942;51:386.
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2. Teng P, Falanga V, Kerdel FA. The microbiological evaluation of leg ulcers and infected dermatoses in patients requiring hospitalization. Wounds. 1993;5:133-136.
3. Kunin CM. Resistance to antimicrobial drugs: a worldwide calamity. Ann Intern Med. 1993;118:557-561.
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4. Jones RN. Impact of changing pathogens and antimicrobial susceptibility patterns in the treatment of serious infections in hospitalized patients. Am J Med. 1996;100(suppl):3S-12S.
5. Brown KS. Pharmaceutical and biotech firms taking on drug-resistant microbes. Scientist. 1996;10:1.
6. Thornsberry C. Susceptibility of clinical bacterial isolates to ciprofloxacin in the United States. Infection. 1994;22(suppl 2):S80-S89.
7. Kresken M, Hafner D, Mittermayer H, et al. Prevalence of fluoroquinolone resistance in Europe. Infection. 1994;22(suppl 2):S90-S98.
8. Gold HS, Moellering RC. Antimicrobial-drug resistance. N Engl J Med. 1996;335:1445-1453.
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9. New project launched to track antibiotic resistance. Am J Hosp Pharm. 1994;51:2874.
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10. Murray BE. Can antibiotic resistance be controlled? N Engl J Med. 1994;330:1229-1230.
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11. Brook I, Frazier EH, Yeager JK. Microbiology of infected atopic dermatitis. Int J Dermatol. 1996;35:791-793.
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12. Schwartz R, Das-Young LR, Ramirez-Ronda C, Frank E. Current and future management of serious skin and skin-structure infections. Am J Med. 1996;100(suppl):90S-95S.
13. Gonzalez A, Schachner LA, Cleary T, et al. Pyoderma in childhood. Adv Dermatol. 1989;4:127.
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14. Stratton CW, Ratner H, Johnston PE, Schaffner W. Focused microbiologic surveillance by a specific hospital unit as a sensitive means of defining antimicrobial resistance problems. Diagn Microbiol Infect Dis. 1992;15(suppl):11S-18S.
15. Thornsberry C, Yee C. Comparative activity of eight antimicrobial agents against clinical bacterial isolates from the United States, measured by two methods. Am J Med. 1996;100(suppl):26S-38S.
16. Jones RN, Kehrberg EN, Erwin ME, Anderson SC, and The Fluoroquinolone Resistance Group. Prevalence of important pathogens and antimicrobial activity of parenteral drugs at numerous medical centers in the United States, I: study on the threat of emerging resistance: real or perceived? Diagn Microbiol Infect Dis. 1994;19:203-215.
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17. Neu HC, Duma RJ, Jones RN, et al. Antibiotic resistance: epidemiology and therapeutics. Diagn Microbiol Infect Dis. 1992;15:53S-60S.
18. Ballow CH, Schentag JJ. Trends in antibiotic utilization and bacterial resistance: report of the National Nosocomial Resistance Surveillance Group. Diagn Microbiol Infect Dis. 1992;1:37S-42S.
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