Investigation of antimicrobial use and the impact of antimicrobial use guidelines in a small animal veterinary teaching hospital: 1995–2004

J. Scott Weese Department of Clinical Studies, Ontario Veterinary College, University of Guelph, Guelph, ON N1G 2W1, Canada.

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 DVM, DVSc, DACVIM

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Abstract

Objective—To evaluate patterns of antimicrobial use and the impact of antimicrobial use guidelines at a small animal veterinary teaching hospital.

Design—Retrospective study.

Sample Population—All antimicrobial prescriptions for dogs and cats admitted to the hospital in 1995 through 2004.

Procedure—Pharmacy records were reviewed, and antimicrobial prescriptions for all dogs and cats admitted during the study period were recorded. Amounts of individual drugs dispensed directly to the intensive care and surgical units were determined. Changes in antimicrobial use during the study period were assessed; changes in antimicrobial use patterns in 2000 through 2004 were evaluated to assess the impact of implementation of antimicrobial use guidelines in 2001.

Results—There was a significant decrease in prescriptions/1,000 admissions during the study period. From 1995 to 2004, the use of first-generation cephalosporins, fluoroquinolones, penicillins, and trimethoprim-sulfonamides decreased, whereas the use of metronidazole increased. The use of first-generation cephalosporins, fluoroquinolones, and penicillins decreased from 2000 to 2004. First-line drugs accounted for 90.7% of prescriptions during the study period. The use of third-line drugs decreased from 2000 to 2004.

Conclusions and Clinical Relevance—Characterization of antimicrobial use is an important step in defining and evaluating the prudent use of antimicrobials. Whereas the true effect of antimicrobial use guidelines is unclear, these results suggest that the guidelines may have had an effect on antimicrobial prescription patterns in this small animal veterinary teaching hospital. Analysis of objective data regarding antimicrobial use and changes in antimicrobial use patterns over time is important in veterinary practices.

Abstract

Objective—To evaluate patterns of antimicrobial use and the impact of antimicrobial use guidelines at a small animal veterinary teaching hospital.

Design—Retrospective study.

Sample Population—All antimicrobial prescriptions for dogs and cats admitted to the hospital in 1995 through 2004.

Procedure—Pharmacy records were reviewed, and antimicrobial prescriptions for all dogs and cats admitted during the study period were recorded. Amounts of individual drugs dispensed directly to the intensive care and surgical units were determined. Changes in antimicrobial use during the study period were assessed; changes in antimicrobial use patterns in 2000 through 2004 were evaluated to assess the impact of implementation of antimicrobial use guidelines in 2001.

Results—There was a significant decrease in prescriptions/1,000 admissions during the study period. From 1995 to 2004, the use of first-generation cephalosporins, fluoroquinolones, penicillins, and trimethoprim-sulfonamides decreased, whereas the use of metronidazole increased. The use of first-generation cephalosporins, fluoroquinolones, and penicillins decreased from 2000 to 2004. First-line drugs accounted for 90.7% of prescriptions during the study period. The use of third-line drugs decreased from 2000 to 2004.

Conclusions and Clinical Relevance—Characterization of antimicrobial use is an important step in defining and evaluating the prudent use of antimicrobials. Whereas the true effect of antimicrobial use guidelines is unclear, these results suggest that the guidelines may have had an effect on antimicrobial prescription patterns in this small animal veterinary teaching hospital. Analysis of objective data regarding antimicrobial use and changes in antimicrobial use patterns over time is important in veterinary practices.

Antimicrobial use and antimicrobial resistance are important topics in human and veterinary medicine. Scrutiny of antimicrobial use in both of these fields has heightened as the incidence and public awareness of antimicrobial resistance have increased. Among the general concerns are use of antimicrobials in situations in which bacterial infection is unlikely (or unlikely to develop), use of inappropriate drugs for the given situation, and administration of antimicrobials at inappropriate dosages or treatment durations.1-3 Each of these problems is of concern and requires individual evaluation and potential intervention.

In human medicine, a variety of strategies for controlling or changing patterns of antimicrobial use have been attempted. These include development of clinical practice guidelines, education of physicians and patients, restriction of available antimicrobials, use of antimicrobial order forms, feedback activities, monitoring of prescription patterns, use of antimicrobial rotation programs, and requiring approval of use of certain drugs.1,4-8 Positive impacts on prescribing practices have been reported with some programs, resulting in benefits such as decreases in overall antimicrobial use, use of targeted antimicrobials, costs, and antimicrobial resistance1,4,7,9-11; however, the relative effect of individual factors is unclear.

Comparatively, there is less objective information regarding antimicrobial use in companion animal medicine, although it is likely that the aforementioned issues for human medicine also apply. Prescott et al12 evaluated antimicrobial use in dogs at the OVC-VTH as part of a study of changes in antimicrobial resistance of certain pathogens. In the period from 1990 to 1999, increased enrofloxacin use was identified and was associated with increased enrofloxacin resistance among Staphylococcus intermedius isolates obtained from dogs.12 A study13 of prescriptions for antimicrobials at a small animal teaching hospital in Finland revealed that 22% of dogs (n = 5,918) were treated with antimicrobials, that β-lactam antimicrobials were most commonly administered, and that prescription of fluoroquinolones was uncommon. A study14 of antimicrobial use in dogs and cats that was based on wholesaler's statistics revealed that β-lactam antimicrobials were the most commonly prescribed antimicrobials in Sweden, whereas trimethoprim-sulfonamide was most commonly used in Norway. Detailed antimicrobial use data are required to better understand how antimicrobials are used in small animal veterinary medicine, provide objective data for interpreting risks of antimicrobial resistance, and establish a baseline from which to assess measures taken to reduce antimicrobial use.

In veterinary medicine, a variety of professional bodies have developed basic guidelines of antimicrobial treatment.15,16 Although these are potentially effective educational tools, such general policies do not provide specific guidance regarding appropriate use of specific antimicrobials or classes of antimicrobials, either in general terms or specific situations. At the practice level, specific antimicrobial use guidelines are uncommon; Prescott et al12 reported that only 3 of 21 veterinary teaching hospitals in the United States and Canada had policies for the use of drugs such as amikacin, imipenem, and vancomycin. Recently, the American College of Veterinary Internal Medicine recommended that veterinarians classify antimicrobials used in their practice into primary, secondary, and tertiary categories.a To the author's knowledge, the potential impact of antimicrobial use guidelines has not been evaluated in veterinary medicine.

On the basis of anecdotal concerns regarding antimicrobial prescription patterns in the small animal clinic of the OVC-VTH, particularly the frequency of use of fluoroquinolones and imipenem, antimicrobial use guidelines were developed by the institutional Infection Control Committee in 2001. Different antimicrobials were placed into use classes (designated first-line, second-line, and third-line drugs; Appendix), and general recommendations regarding antimicrobial use were established. In 2003, a policy to restrict the use of vancomycin was implemented. The objectives of the study reported here were to evaluate patterns of antimicrobial use and the impact of antimicrobial use guidelines on prescription issuance at the OVC-VTH.

Materials and Methods

Pharmacy records at the OVC-VTH Small Animal Clinic generated during 1995 through 2004 were searched for drug dispensing data. All antimicrobial prescriptions dispensed to clients for individual animals (dogs and cats) that involved drugs that were orally or parenterally administered were recorded. Multiple prescriptions for the same antimicrobial for an individual animal for the same disease process were considered to be a single use. Data were evaluated in terms of antimicrobial class or the individual antimicrobial when only one of a particular class was used. Additionally, drugs were classified into use categories as defined in the OVC-VTH antimicrobial use guidelines. For each drug class and use category, the number of prescriptions per year, the number of prescriptions/1,000 admissions per year, and prescriptions as a percentage of total prescriptions issued yearly were calculated.

Whereas most situations in which antimicrobials were administered involved the issuance of individual prescriptions, some animals received antimicrobials that were dispensed directly to surgical or intensive care units. Total amount (in milligrams) of each antimicrobial dispensed to each of those hospital areas was also determined and calculated on the basis of total use/1,000 admissions per year. Total cost of antimicrobials dispensed to the surgical and intensive care units was calculated for each year of the study on the basis of cost charged to clients for each drug in 2005.

Linear regression analysis was used to evaluate changes in antimicrobial use over the entire study period; for the period from 2000 through 2004, analysis was performed as a measure of the effect of the antimicrobial use guidelines that were implemented in 2001. A value of P < 0.05 was considered significant. Analyses were performed by use of a statistical software package.b

Results

Overall antimicrobial prescriptions—During 1995 through 2004, 21,152 antimicrobial prescriptions were written for 99,400 dogs and cats. Among the years of the study period, there was no significant change in total prescriptions per year; however, there was a significant (P = 0.011) increase in yearly admissions during the study period. Accordingly, there was a decrease (P = 0.007) in total prescriptions/1,000 admissions over the study period, from a maximum value of 234.9 prescriptions/1,000 admissions in 1999 to a minimum value of 168.4 prescriptions/1,000 admissions in 2004 (Table 1).

Table 1—

Antimicrobial use at a small animal veterinary teaching hospital during 1995 through 2004, expressed as the number of prescriptions/1,000 admissions. In addition to changes in prescription issuance that occurred during the entire study period, changes that occurred in 2000 through 2004 were also assessed to evaluate the effect of implementation of antimicrobial use guidelines in 2001.

Antimicrobial or antimicrobial classYearChange between 1995 and 2004 (%)P valueChange between 2000 and 2004 (%)P valueUse in 2004 (%)*
199519961997199819992000 200220032004
First-generation cephalosporins82.787.879.376.970.581.474.670.552.152.3−370.002−360.01131.1
Second-generation cephalosporins0.71.70.33.13.22.71.22.02.22.2+2140.290−190.9571.3
Third-generation cephalosporins0.81.62.10.81.10.91.91.40.90.6−250.492−330.3650.4
Aminoglycosides2.21.52.92.70.95.83.93.13.84.1+860.091+290.3422.5
Carbapenems1.30.91.01.72.61.91.10.81.00.5−620.402−730.0530.3
Chloramphenicol1.01.12.71.42.70.20.70.40.30.3−700.093+500.6700.2
Fluoroquinolones16.413.811.820.120.916.913.113.87.27.8−520.031−540.0274.6
Glycopeptides0000.100000.2000.46700.5590
Lincosamides5.18.912.610.16.18.010.412.812.08.6+690.261+80.7445.1
Macrolides4.63.61.10.81.01.31.074.42.03.1−330.808+1380.3511.8
Metronidazole5.214.114.611.517.913.621.727.626.320.6+2940.003+510.35712.2
Penicillins53.137.228.029.822.723.019.817.415.311.9−780.002−480.0017.1
Potentiated penicillins26.137.434.333.054.346.239.237.842.839.1+500.205−150.40823.2
Tetracyclines5.99.210.817.214.713.511.89.710.97.9+340.931−410.0344.7
Trimethoprim-sulfonamide23.411.115.517.516.414.911.68.910.89.5−330.015−360.1195.6
No. of prescriptions/1,000 admissions228.6229.7217.1226.7234.9230.3212.1210.7187.7168.4−260.007−270.005NA
No. of admissions9,9469,0899,0368,7878,5509,50610,15511,44611,31411,571+160.011+220.031NA

Value represents the percentage of total prescriptions for the year.

NA = Not applicable.

The most commonly prescribed drug in each year of the study was cephalexin, a first-generation cephalosporin. In 1996 through 2004, amoxicillinclavulanic acid was the second most common drug, followed by amoxicillin; the order of prescription frequency of these 2 drugs was reversed in 1995.

Changes in antimicrobial class or drug prescription—There were significant changes in antimicrobial class prescriptions during the study period and following implementation of antimicrobial use guidelines in 2001 (Table 1). In the period from 1995 through 2004, use of metronidazole increased, whereas prescription of first-generation cephalosporins, fluoroquinolones, penicillins, and trimethoprim-sulfonamides decreased. In 2000 through 2004, the period influenced by implementation of antimicrobial use guidelines in 2001, there were significant decreases in the use of fluoroquinolones, penicillins, and tetracyclines; albeit not significant (P = 0.053), there was also a decrease in imipenem use.

Changes in prescription of antimicrobial use classes—Among prescriptions for antimicrobials issued yearly during the study period, the proportion (mean ± SD) that related to first-line drugs was 90.7 ± 1.7% (range, 88.4% to 93.6%); second- and third-line drugs accounted for 8.7 ± 1.6% (range, 5.8% to 10.7%) and 0.6 ± 0.2% (range, 0.3% to 1.0%), respectively. There was a significant decrease in prescription of first-line drugs/1,000 admissions during the period from 1995 to 2004 and a decrease in the use of both first- and third-line drugs from 2000 through 2004 (Table 2). Vancomycin was administered to 1 dog in 1998 and to 2 dogs in 2003.

Table 2—

Prescriptions issued (No. of prescriptions/1,000 admissions) for antimicrobials (by use groups) at a small animal veterinary teaching hospital during 1995 through 2004. In addition to changes in prescription issuance that occurred during the entire study period, changes that occurred in 2000 through 2004 were also assessed to evaluate the effect of implementation of antimicrobial use guidelines in 2001.

Antimicrobial use groupYearChange between 1995 and 2004 (%)P valueChange between 2000 and 2004 (%)P valueUse in 2004 (%)*
199519961997199819992000 200220032004
First-line207214207207219216201192179158−24< 0.001−270.00192
Second-line23.319.317.025.026.222.917.020.211.113.2−420.075−420.0857.6
Third-line1.310.881.01.812.571.891.080.791.140.52−600.112−720.0120.3

First-line group = Drugs to be used in the absence of or pending results of bacteriologic culture and antimicrobial susceptibility testing.

Second-line group = Drugs to be used on the basis of results of bacteriologic culture and antimicrobial susceptibility testing in vitro and because of the lack of any appropriate first-line drug options. Third-line group = Drugs to be used only to treat serious infections with bacteria that have known resistance to first- and second-line drugs but that are susceptible to a third-line drug.

See Table 1 for remainder of key.

Direct dispensing of antimicrobials to the surgical and intensive care units—There were no changes in the number of units (milligrams) of cefazolin, cefoxitin, ampicillin, clindamycin, or enrofloxacin dispensed to the surgical or intensive care units/1,000 admissions from 1995 through 2004; however, from 2000 through 2004, there were significant decreases in ampicillin and cefazolin use (P = 0.048 and 0.02, respectively). There was no significant (P = 0.253) increase in cost of drugs dispensed to surgical and intensive care units from 1995 through 2004 (Can $16,108 vs $20,850, respectively); from 2000 through 2004, there was a significant (P = 0.016) decrease in this cost (Can $26,312 vs $20,850, respectively).

Discussion

The present study involved analysis of data regarding antimicrobial use in a small animal veterinary teaching hospital during a 10-year period. The author is not aware of other published studies that have evaluated data collected from such an extended period and believes that the study of this report is the first to evaluate the impact of antimicrobial use guidelines in a veterinary situation.

A variety of methods are available for evaluating antimicrobial use patterns, all of which have limitations. In human studies, DDD is the standard for reporting antimicrobial use trends.17 Calculation of DDD is based on the total volume of antimicrobial administered and the dosing regimen, which usually involves a standard weight per person. Because the weight ranges among dogs and cats are wide, DDD may be more difficult to apply accurately in many veterinary species.14 However, DDD could be used in veterinary settings if a standardized body weight was accurately defined for the intended study group and there were no differences in antimicrobial use patterns among animals of different sizes. Another potential limitation of DDD in veterinary hospital–based studies is the somewhat common practice, at least in the OVC-VTH, of discharging animals and providing their owners with antimicrobials for use in the treatment of their pets at home. In these situations, the calculated DDD would overrepresent in-hospital antimicrobial use. In some veterinary studies,13,14 the total mass of drug or number of prescriptions issued has been used to evaluate antimicrobial use. In the present study, both of the latter methods were applied. Prescription numbers were used for the main part of the study because these data provided the most accurate assessment of antimicrobial use at the individual animal prescription level. Total drug amounts dispensed to the surgical and intensive care units, although not useful for evaluating drug use at the individual animal level, were used for further comparison of antimicrobial uses and to ensure apparent changes in prescription patterns were not the result of a change in the manner in which antimicrobials were dispensed during hospitalization.

The decrease in antimicrobial prescription rates/1,000 admissions (which adjusts for changes in caseload) during the study period was interesting and could have been associated with a variety of factors. Increased awareness of concerns regarding overuse of antimicrobials, as a result of the guidelines introduced at the OVC-VTH in 2001 and information from other sources, may have impacted treatment decisions at the hospital in terms of whether antimicrobial treatment was indicated and which drug was chosen. Other factors should also be considered, including change in caseload distribution, particularly if such a change involved an increase in elective, nonsurgical cases that would be less likely to require antimicrobials. Although specific information regarding the distribution of cases in the OVC-VTH Small Animal Clinic was not available, there was no indication that any such changes occurred during the study period. Another factor that required consideration was a change in the manner in which antimicrobials were dispensed. Because drugs dispensed directly to the surgical or intensive care units were not recorded for individual use, this method of dispensing required scrutiny. However, the lack of a concurrent increase in antimicrobials dispensed directly to these hospital areas as antimicrobial prescriptions decreased confirmed that changes in the mechanism of antimicrobial delivery within the OVC-VTH were not a confounding influence.

In addition to decreasing overall use of antimicrobials, decreased use of certain classes of drugs is an important objective in prudent antimicrobial use. In the present study, the decrease in use of fluoroquinolones, the overall decrease in use of drugs classified as third-line agents, and the suggestion of a decrease in carbapenem use were encouraging. Additionally, the fact that these decreases occurred from 2000 through 2004, the period concurrent with implementation of antimicrobial use guidelines, suggests that these guidelines may have, at least in part, been a contributing factor. In human medicine, excessive fluoroquinolone use has been associated with emergence of antimicrobial resistance, treatment failure, increased patient morbidity rates, and increased costs.18-20 As a result, there are increasing calls to restrict the use of fluoroquinolones in humans to situations in which alternative treatments have failed, patients are allergic to other drug options, or multidrug-resistant infection is present.8,18,21 Concerns regarding excessive or inappropriate use of fluoroquinolones in veterinary medicine have also been expressed.22,23 Similarly, inappropriate carbapenem use has been associated with increased antimicrobial resistance in human hospitals, particularly resulting in emergence of multidrug-resistant Pseudomonas aeruginosa and Acinetobacter baumannii.1 The high cost of drugs such as carbapenems, compared with the costs of alternative agents, is an added concern in human medicine,1 and the changes in antimicrobial prescription patterns determined in the present study would presumably have resulted in decreased costs to clients.

The effects of changes in antimicrobial use on patient illness and death were not assessed. However, it is important to note that studies24,25 in humans have revealed beneficial effects on patient mortality and morbidity rates associated with implementation of antimicrobial use guidelines or restrictions.

The true effect of the antimicrobial use guidelines at the OVC-VTH is impossible to determine objectively. When the guidelines were implemented, descriptive materials were circulated to the hospital clinicians but there was little formal education and enforcement.

Rather, much of the implementation was based on informal monitoring and discussion by certain interested clinicians. It is possible that, concurrent with guideline development, there was increased awareness regarding prudent antimicrobial use that also impacted antimicrobial selection. Other possible reasons for changes in antimicrobial prescription rates are not readily apparent.

In the present study, it was also encouraging that vancomycin—a critically important antimicrobial in human medicine and a drug for which antimicrobial resistance is an emerging concern—was used rarely. The OVC-VTH vancomycin restriction policy states that it may only be used to treat life-threatening infections involving bacteria for which multidrug resistance and in vitro susceptibility to vancomycin have been determined, and in situations in which no other antimicrobials are appropriate, and when permission of 2 designated Infection Control Committee members has been granted. The effects of this policy on vancomycin usage are unclear. Use of vancomycin has never been denied under this program, but it is possible that in certain situations in which vancomycin might otherwise have been used, the establishment of this program resulted in clinicians choosing other antimicrobials instead of attempting to obtain permission to administer vancomycin.

The predominance of prescriptions for cephalexin and amoxicillin-clavulanic acid, which accounted for 54% of prescriptions in 2004, is similar to findings of a study13 of antimicrobial prescriptions issued for Finnish dogs. In contrast, another study14 of antimicrobial use in dogs and cats revealed the predominance of penicillin use in Sweden and trimethoprim-sulfonamide use in Norway. In those 2 studies,13,14 fluoroquinolone use was uncommon, comprising 2.8% of prescriptions for dogs in Finland and 2.4% and 1.0% of the total mass of antimicrobials sold in Sweden and Norway, respectively. In the present study, fluoroquinolones comprised 8.9% of prescriptions in 1999 and perceived overuse of this drug class both at the OVC-VTH and in small animal practice as a whole was one of the main reasons for development of antimicrobial use guidelines at the hospital.

The reason for the increase in metronidazole use in the present study is unclear. An outbreak of nosocomial Clostridium difficile–associated diarrhea was encountered in 2001,26 accounting for a predictable increase in metronidazole use at the OVC-VTH that year. However, the increase continued after the outbreak abated. It is possible that the outbreak created more awareness of nosocomial C difficile–associated diarrhea, resulting in earlier or more frequent treatment of animals, including animals with infections that might otherwise have been self-limiting and would have remained untreated in the past.

Any evaluation of antimicrobial use must consider the study group. The study of this report involved dogs and cats at a tertiary care veterinary teaching hospital, at which the population of animals is more likely to have severe disease, receive frequent antimicrobial administration prior to referral, receive more frequent applications of invasive devices (ie, IV catheters and urinary catheters), or be immunocompromised (drug or disease induced); furthermore, a veterinary teaching hospital is likely to be an animal, human, and environmental reservoir of nosocomial pathogens. Presumably, the likelihood of antimicrobial resistance would be greater at a veterinary teaching hospital, compared with primary care veterinary clinics, because of the skewed nature of the caseload; nevertheless, drugs designated as first-line comprised > 90% of prescriptions.

Although results of the present study were encouraging, this assessment evaluated only 1 component of prudent antimicrobial use. The investigation focused on characterization of overall prescription patterns and changes of these patterns over time and in response to antimicrobial use guideline implementation. Other aspects such as indications for antimicrobial treatment in individual animals, the use of results of bacteriologic culture and antimicrobial susceptibility testing as the basis of antimicrobial selection, and proper duration of treatment were not evaluated and require equal attention.

As concerns regarding antimicrobial resistance intensify and there is increasing scrutiny of antimicrobial use in veterinary medicine, it is important for veterinarians to take measures to ensure that antimicrobials are used prudently. Periodic reviews of antimicrobial use in hospitals and clinics, similar to that performed in the study of this report, can be used to identify changes in patterns of prescription issuance and allow for earlier intervention to rectify undesirable shifts in drug use, if required. The results of the present study also suggest that development of antimicrobial use guidelines specifically for use in an individual hospital or clinic can have a positive effect on prudent antimicrobial use therein.

OVC-VTH

Ontario Veterinary College Veterinary Teaching Hospital

DDD

Defined daily dose

a.

Morley P, Animal Population Health Institute, Fort Collins, Colo: Personal communication, 2005.

b.

InStat 3.0, GraphPad Software Inc, San Diego, Calif.

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Appendix 1

Appendix 1

Overview of OVC-VTH Small Animal Clinic antimicrobial use guidelines.

First-line drugs
To be used in the absence of or pending results of bacteriologic culture and antimicrobial susceptibility testing.
 Penicillins: penicillin G, amoxicillin, or ampicillin
 Potentiated penicillins: amoxicillin-clavulanic acid
 First-generation cephalosporins: cefazolin or cephalexin
 Second-generation cephalosporins: cefoxitin
 Aminoglycosides: gentamicin
 Trimethoprim-sulfonamide
 Tetracyclines: tetracycline or doxycycline
 Lincosamides: clindamycin
 Metronidazole
 Macrolides: erythromycin or tylosin
Second-line drugs
To be used on the basis of results of bacteriologic culture and antimicrobial susceptibility testing in vitro and because of the lack of any appropriate first-line drug options.
 Cloxacillin
 Piperacillin
 Ticarcillin
 Amikacin or tobramycin
 Fluoroquinolones
 Other cephalosporins
 Other potentiated penicillins
Third-line drugs
To be used only to treat serious infections with bacteria that have known resistance to first- and second-line drugs but that are susceptible to a third-line drug.
 Carbapenems
 Vancomycin (use directed by vancomycin policy guidelines)
 Other drugs not listed above but which have been used in veterinary species
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