Implementation of an antimicrobial stewardship program in a veterinary medical teaching institution

Emily E. Feyes From the Department of Veterinary Preventive Medicine, The Ohio State University, Columbus, OH 43210

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Dubraska Diaz-Campos From the Department of Veterinary Clinical Sciences, The Ohio State University, Columbus, OH 43210

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Dixie F. Mollenkopf From the Department of Veterinary Preventive Medicine, The Ohio State University, Columbus, OH 43210

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Rikki L. Horne From the Department of Veterinary Medical Center, College of Veterinary Medicine, The Ohio State University, Columbus, OH 43210

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Rachel C. Soltys From the Department of Veterinary Preventive Medicine, The Ohio State University, Columbus, OH 43210

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Greg A. Ballash From the Department of Veterinary Preventive Medicine, The Ohio State University, Columbus, OH 43210

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Jessica A. Shelby From the Department of Veterinary Preventive Medicine, The Ohio State University, Columbus, OH 43210

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Erica E. Reed From the Department of Wexner Medical Center, The Ohio State University, Columbus, OH 43210., The Ohio State University, Columbus, OH 43210

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Kurt B. Stevenson From the Department of Wexner Medical Center, The Ohio State University, Columbus, OH 43210., The Ohio State University, Columbus, OH 43210

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Joshua B. Daniels From the Department of Veterinary Clinical Sciences, The Ohio State University, Columbus, OH 43210

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Jason W. Stull From the Department of Veterinary Preventive Medicine, The Ohio State University, Columbus, OH 43210

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Thomas E. Wittum From the Department of Veterinary Preventive Medicine, The Ohio State University, Columbus, OH 43210

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Abstract

Widespread use of antimicrobials in human and veterinary medicine drives the emergence and dissemination of resistant bacteria in human, animal, and environmental reservoirs. The AVMA and FDA Center for Veterinary Medicine have both taken public positions emphasizing the importance of incorporating antimicrobial stewardship in veterinary clinical settings; however, a model for implementing a comprehensive antimicrobial stewardship program in veterinary practice is not readily available.

In 2015, The Ohio State University College of Veterinary Medicine began developing a veterinary antimicrobial stewardship program modeled on existing programs in human health-care institutions and the 7 core elements of a successful hospital antimicrobial stewardship program, as defined by the CDC. The program includes comprehensive antimicrobial use guidelines, active environmental surveillance, and enhanced infection control procedures in The Ohio State University Veterinary Medical Center, along with routine monitoring and reporting of antimicrobial prescribing practices and antimicrobial susceptibility patterns of common pathogens isolated from patients and the hospital environment. Finally, programs have been developed to educate clinicians, staff, and students on antimicrobial resistance and appropriate antimicrobial prescribing practices.

The antimicrobial stewardship program has been designed to help clinicians and students confidently make judicious antimicrobial use decisions and provide them with actionable steps that can help them act as strong stewards while providing the best care for their patients. This report describes our program and the process involved in developing it, with the intent that the program could serve as a potential model for other veterinary medical institutions.

Abstract

Widespread use of antimicrobials in human and veterinary medicine drives the emergence and dissemination of resistant bacteria in human, animal, and environmental reservoirs. The AVMA and FDA Center for Veterinary Medicine have both taken public positions emphasizing the importance of incorporating antimicrobial stewardship in veterinary clinical settings; however, a model for implementing a comprehensive antimicrobial stewardship program in veterinary practice is not readily available.

In 2015, The Ohio State University College of Veterinary Medicine began developing a veterinary antimicrobial stewardship program modeled on existing programs in human health-care institutions and the 7 core elements of a successful hospital antimicrobial stewardship program, as defined by the CDC. The program includes comprehensive antimicrobial use guidelines, active environmental surveillance, and enhanced infection control procedures in The Ohio State University Veterinary Medical Center, along with routine monitoring and reporting of antimicrobial prescribing practices and antimicrobial susceptibility patterns of common pathogens isolated from patients and the hospital environment. Finally, programs have been developed to educate clinicians, staff, and students on antimicrobial resistance and appropriate antimicrobial prescribing practices.

The antimicrobial stewardship program has been designed to help clinicians and students confidently make judicious antimicrobial use decisions and provide them with actionable steps that can help them act as strong stewards while providing the best care for their patients. This report describes our program and the process involved in developing it, with the intent that the program could serve as a potential model for other veterinary medical institutions.

Introduction

Antimicrobial resistance is a critical global health concern that threatens both humans and animals, while widespread use of antimicrobials in human and veterinary medicine drives the emergence and dissemination of resistant bacteria in human, animal, and environmental reservoirs.1 The AVMA has established a policy indicating the need for veterinarians to directly address the problem of antimicrobial resistance on the basis of 5 core principles of antimicrobial stewardship in veterinary medicine.2 These core principles, together with the AVMA policy on judicious therapeutic use of antimicrobials, provide a strong philosophical basis for veterinarians to implement antimicrobial stewardship programs.3 In addition, the FDA Center for Veterinary Medicine has created a 5-year action plan supporting antimicrobial stewardship in veterinary settings.4 This plan details actions the FDA Center for Veterinary Medicine intends to support and implement to help prevent the spread of resistant bacteria and maintain the effectiveness of existing antimicrobials. These activities detailed by the AVMA and the FDA Center for Veterinary Medicine are indicators of the growing recognition of the importance of antimicrobial stewardship in veterinary medicine.

Human health-care institutions have placed substantial emphasis on implementation of antimicrobial stewardship programs in hospital settings.5 These programs are designed to increase awareness of antimicrobial resistance and improve antimicrobial prescribing practices. They accomplish this by emphasizing the use of the correct antimicrobial drug at the correct dosage for the correct duration to achieve the best patient outcomes while avoiding adverse events and inappropriate use of antimicrobials.6,7 Targeted environmental surveillance for resistant bacterial organisms during infectious disease outbreaks in medical settings is an important component of these programs. Passive and active surveillance are used to monitor prescribing practices and identify resistant bacteria in the patient population and hospital environment. Infectious disease physicians and pharmacists oversee these programs and provide their expertise to counsel clinicians on best practices in antimicrobial prescribing and create strategies that support judicious antimicrobial use. The primary focuses of these programs are positive clinical outcomes and quality of patient care,8 but these programs can also have financial implications for institutions. Antimicrobial stewardship programs may, for instance, provide direct financial benefits to hospitals by reducing patient duration of stay, shortening the duration of antimicrobial treatment, and reducing pharmaceutical costs while reducing the presence of multidrug-resistant bacteria in the hospital environment.8 The documented success of these programs has led the Centers for Medicare and Medicaid Services and Joint Commission on Accreditation of Healthcare Organizations to require, since 2017, that human hospitals meet defined stewardship metrics to receive federal reimbursement (Centers for Medicare and Medicaid Services) or accreditation (Joint Commission).9 Both the Centers for Medicare and Medicaid Services and Joint Commission are responsible for ensuring quality patient care and safety. Certification and accreditation by these 2 entities affect the ability of hospitals to attract patients, recruit top talent, decrease liability insurance costs, and receive third-party insurer reimbursements.10,11 These external drivers provide incentives for human health-care institutions to develop and maintain effective antimicrobial stewardship programs.

The impact of antimicrobial resistance on veterinary medicine is widespread and includes negative patient outcomes resulting from treatment failures for infections caused by drug-resistant bacteria, increased client costs, and increased risk of zoonotic transmission of multidrug-resistant bacteria to clients, veterinarians, and their staff.12 The AVMA Core Principles of Antimicrobial Stewardship urge veterinarians to “take action.”2 Unfortunately, the specific actions they should implement in the practice environment to promote antimicrobial stewardship are not obvious to most veterinarians. The OSU-CVM began developing a veterinary antimicrobial stewardship program for the OSU-VMC in 2015. This program was designed to help clinicians and students confidently make judicious antimicrobial use decisions and provide them with actionable steps intended to help them act as strong stewards while providing the best care for their patients. This report describes our program and the process involved in developing it.

OSU-VMC Antimicrobial Stewardship Program

The mission of the OSU-VMC antimicrobial stewardship program is to optimize patient care while minimizing unintended consequences of antimicrobial use, including the emergence of resistant bacteria associated with high rates of patient morbidity and mortality. An important component of this mission is to educate veterinary personnel and students about responsible antimicrobial use and the consequences of inappropriate use. Consistent with the OSU-VMC mission of providing the highest level of professional veterinary care to its patients and clients, the antimicrobial stewardship program seeks to ensure that antimicrobial treatment is based on the most appropriate drug, dosage, and duration, as determined on the basis of body site and causative agent.

At the time of our program's initiation, there were no established models for developing or instituting an antimicrobial stewardship program in a veterinary setting. We therefore chose to use an existing program from the human health-care field, specifically the antimicrobial stewardship program successfully implemented in the OSU Wexner Medical Center,13 as our initial model. Our program incorporated the 7 core elements of a successful hospital antimicrobial stewardship program, as defined by the CDC.14

These 7 core elements of stewardship are leadership commitment, accountability, drug expertise, action, tracking, reporting, and education.14 For an antimicrobial stewardship program to be successful, hospital leadership must first show a clear commitment to the program, including a commitment to providing the required financial and human resources and a willingness to publicly support the antimicrobial stewardship program. In our case, the leadership of the OSU-VMC and OSU-CVM provided this level of support from the initiation of the program and continues to champion the antimicrobial stewardship program.

Accountability and drug expertise require identification of clinical leaders who will be responsible for ensuring the effectiveness of the program and certifying improvements in antimicrobial use. In our program, both of these elements were addressed by creating an ASWG. The ASWG is a multidisciplinary group led by a clinical microbiologist, pharmacist, and epidemiologist. The group itself consists of faculty, staff, and students, including representatives from the Departments of Veterinary Preventive Medicine and Veterinary Clinical Sciences and the OSU-VMC Pharmacy. The ASWG meets regularly to monitor and discuss program status and ongoing activities, identify issues to be addressed, and determine whether any updates or changes to components of the program are needed. The ASWG is also responsible for ongoing monitoring of antimicrobial use and maintenance of the hospital antimicrobial use guidelines for the OSU-VMC.

The ASWG does not function in isolation. Clinical faculty in the OSU-VMC provided feedback on the proposed antimicrobial use guidelines prior to their publication, and the ASWG continues to regularly solicit feedback from all clinicians regarding antimicrobial use in the VMC. Additionally, the ASWG routinely receives input and feedback from a group of experienced clinicians who represent each of the OSU-VMC hospitals: companion animals, equine, and farm animals. This Senior Clinician Advisory Group provides the ASWG input on the basis of their expertise and experience in managing clinical cases and offers additional oversight regarding the use of protected antimicrobials in the OSU-VMC. The ASWG also maintains a strong collaborative relationship with ASWG personnel at the OSU Wexner Medical Center, with the working groups meeting regularly to discuss and contribute insight and experience in maintaining a successful stewardship program.

The CDC's action core element of a successful hospital antimicrobial stewardship program involves implementation of specific activities intended to improve antimicrobial use. In the human health-care setting, this might include practices such as an antimicrobial time-out (systematic reevaluation 48 hours after initiation of antimicrobial administration to determine appropriateness of treatment) and prior approval requirements for certain antimicrobial drugs to ensure appropriate drug selection.14

Unfortunately, these elements have not been well-defined in veterinary medicine. The AVMA and other professional organizations, such as the American Association of Bovine Practitioners and American Association of Feline Practitioners, have provided tools15,16,17 for veterinarians to use, including a checklist of antimicrobial stewardship activities.18 However, models of the effective implementation of these tools are not readily available. To address this core element in the OSU-CVM antimicrobial stewardship program, the ASWG established comprehensive antimicrobial use guidelines intended to protect the efficacy of certain key antimicrobials for patients in the OSU-VMC, implemented active environmental surveillance for targeted resistant bacteria on the basis of recommendations from epidemiologists, and instituted enhanced infection control procedures in the OSU-VMC.

We have incorporated the elements of tracking and reporting by routinely monitoring and reporting antimicrobial prescribing practices and antimicrobial susceptibility patterns of common pathogens isolated from the OSU-VMC patient population and its environment. This includes a regular review of antimicrobial prescriptions in the OSU-VMC, annual creation of antibiograms for bacteria isolated from OSU-VMC patients, and targeted monitoring of resistant bacteria in the hospital environment. An annual report describing the program and its results was created, with annual presentations of program results at OSU-VMC section meetings and direct communication of specific findings to relevant sections and clinicians.

Finally, programs have been developed to educate clinicians, staff, and students on antimicrobial resistance and appropriate antimicrobial prescribing practices. This includes required student antimicrobial stewardship materials, antimicrobial stewardship training of new clinical residents and interns, and active engagement with clinical faculty regarding specific antimicrobial prescribing practices.

Importantly, antimicrobial stewardship programs are intended to address the judicious use of all antimicrobials (ie, antibacterial, antiviral, antifungal, and antiparasitic drugs). However, although we use the term antimicrobial in relation to our program, the program currently focuses solely on the use of antibacterial drugs in the OSU-VMC. The decision to initially direct our attention and resources toward antibacterial drugs was made on the basis of the global emergence of antibacterial resistance and the intense public scrutiny on antibacterial drug use in animals. Expansion to include other antimicrobial drugs is a future goal of our program.

Antimicrobial Use Guidelines

The OSU-VMC antimicrobial use guidelines are a compilation of evidence-based prescribing recommendations for each antimicrobial available at the OSU-VMC. These guidelines were created on the basis of pharmaceutical formulary references, current veterinary literature, and current prescribing practices within the OSU-VMC. The antimicrobial use guidelines are unique to each of the 3 hospitals in the OSU-VMC (companion animals, farm animals, and equine) and are based on the antimicrobials that are regularly used by clinicians and available in the OSU-VMC pharmacy. These guidelines are living documents that the ASWG will update every 2 years in accordance with current literature, OSU-VMC faculty feedback, and subject matter expert recommendations.

The antimicrobial use guidelines are not intended to replace the judgment of experienced clinicians in determining the best treatment for their patients. Rather, they are a tool designed to increase awareness of antimicrobial stewardship and to train future and current veterinarians in the prudent use of antimicrobials, especially by providing guidance on empirical treatment. The antimicrobial use guidelines provide species-specific antimicrobial information, including suggested drug dosages, acceptable and unacceptable drug uses, potential adverse effects, information on extralabel drug use, and available formulations in the OSU-VMC pharmacy. Reference tables and charts provide information on how to appropriately submit samples for bacterial culture, antimicrobial recommendations by species and disease condition, and common pathogenic bacterial organisms by species and body site. The antimicrobial use guidelines clearly categorize antimicrobials as unrestricted use, selective use, and protected use. Antimicrobials categorized as selective use should not be used as empirical or first-line treatment and should only be used when results of bacterial culture and antimicrobial susceptibility testing indicate that they likely will be effective. Protected-use antimicrobials are available but rarely prescribed in the OSU-VMC. These include carbapenems, vancomycin, linezolid, and piperacillin-tazobactam. These antimicrobials were classified as protected use because they should be considered a last resort in veterinary medicine and should only be used to treat life-threatening infections caused by highly resistant pathogens.19 In our hospital, we have a clear policy regarding the appropriate use of protected-use antimicrobials so that clinicians know these drugs are available when justified. Clinicians must consult with an OSU clinical microbiologist or other member of the ASWG (senior faculty member or clinical pharmacologist), bacterial culture and antimicrobial susceptibility testing must be performed and must demonstrate that no other appropriate antimicrobial option exists, testing must demonstrate susceptibility to a protected-use antimicrobial, and there must be a reasonable expectation that the disease will be effectively treated when a protected-use antimicrobial is prescribed. We classify antimicrobials in this manner to ensure medically appropriate use and to reduce the risk of further development of antimicrobial resistance. The guidelines have become a valuable educational tool and help to promote antimicrobial stewardship when treating bacterial infections in our hospital.

The OSU-VMC faculty, staff, and students have convenient and quick access to the antimicrobial use guidelines on both desktop computers and mobile devices through an online publishing website; hard copies of the antimicrobial use guidelines are available in each of the clinical departments. Students are introduced to the antimicrobial use guidelines during the second year of the professional veterinary curriculum and are officially trained on how to use them during their third year. The goal is for students to enter their fourth-year clinical rotations fully prepared to incorporate the antimicrobial use guidelines when developing treatment plans. Initial training on accessing and using the guidelines is also provided to faculty and staff. Incoming residents and interns are trained on how to access and use the guidelines during orientation. In the future, we plan to incorporate training on the guidelines during onboarding of new faculty and staff. The OSU-VMC antimicrobial use guidelines are freely available online20; the only caveat is that the guidelines are tailored to the OSU-VMC. Students are also encouraged to access this reference after graduation because included reference tables and antimicrobial information can still be applied outside the OSU-VMC to guide critical evaluation of antimicrobial prescribing choices and encourage judicious antimicrobial use. In the future, the ASWG will work with private practices in Ohio to assist in developing guidelines tailored to those individual practices. This is part of our mission to expand the antimicrobial stewardship program beyond the OSU-VMC and into the community and profession.

Prescription Drug Monitoring

Prescription drug monitoring is the process of tracking specific data on all prescriptions written for antimicrobials and other medications. These data can be used to analyze a number of important factors such as the impact of an antimicrobial stewardship program, clinician prescribing practices, and empirical or narrowed use patterns in a hospital. Tracking antimicrobial prescription data in the OSU-CVM is necessary to analyze the impact that the antimicrobial stewardship program and antimicrobial use guidelines have had on our hospitals’ prescribing practices. We used historical prescribing data from before implementation of our program to serve as a baseline for comparison with prescribing practices after implementation. Continued prescription monitoring and data analysis will be used to identify trends in OSU-VMC prescribing practices and evaluate whether these can be attributed to the antimicrobial stewardship program. Methods for this analysis are currently under development but could potentially involve retrospective record review of specific patient conditions and comparison of antimicrobial use with recommendations in the OSU-VMC antimicrobial use guidelines. Currently, use of the antimicrobial use guidelines is voluntary; however, if data show that prescribing practices could be improved, the ASWG will develop a plan to intervene in partnership with our Senior Clinician Advisory Group.

Prescription monitoring should ideally occur in real time, allowing for immediate data analysis and reporting to clinicians. Real-time data collection allows for more accurate oversight regarding prescribing of selective-use and protected-use antimicrobials. However, this type of tracking is easiest with electronic prescribing systems, which are not currently available at our hospitals. Thus, we retrospectively track prescriptions by accessing data from our electronic information system after patient charges, including charges for prescriptions, have been entered. With this process, data and information are regularly lost or overrepresented. For example, if a hospitalized patient receives antimicrobials over the course of its stay, the current system will in some situations record multiple prescriptions of a single antimicrobial for this patient.

We plan to address these monitoring challenges by creating a clinical pharmacy residency position that will be responsible for real-time monitoring of prescribing practices. In addition, we are developing an electronic antimicrobial prescription form for all the hospitals (companion animals, equine, and farm animals) in the OSU-VMC that will increase the amount of data captured. Specifically, the new form will include the following additional information: indication for antimicrobial use, results of bacterial culture and antimicrobial susceptibility testing (if applicable), antimicrobial agents administered to the patient in the past, hospitalization status and duration of stay, targeted pathogens, and infectious condition or target site. Our hope is that this expanded antimicrobial prescription form will allow pharmacists to better assist in antimicrobial selection review and provide insight into factors influencing antimicrobial use. It can also potentially serve as an additional educational tool to demonstrate and reinforce the thought processes that should occur when prescribing antimicrobials, especially antimicrobials identified as selective or protected use.

Passive Surveillance

Passive surveillance uses data generated for other purposes, such as results of bacterial culture and antimicrobial susceptibility testing. This approach is used by the ASWG to obtain data supporting clinical decision-making for empirical treatment or for initiating antimicrobial treatment while culture and susceptibility testing results are pending. Antibiograms (Tables 1 and 2) are generated with commercial softwarea from culture and susceptibility test results for patient samples submitted to the Clinical Microbiology Laboratory in the OSU-CVM. These antibiograms are reported to OSU-VMC clinicians and staff every year and help to characterize the most common pathogens causing infections in our patient populations and the susceptibility profiles of those pathogens. These data are monitored by the ASWG to assess trends and changes in susceptibility patterns. In the future, the ASWG plans to develop metrics that will allow us to assess the impact of the antimicrobial stewardship program on overall changes in resistance patterns and address any reduction in pathogen antimicrobial susceptibility. Data for protected-use antimicrobials are not included in these antibiograms because these antimicrobials should not be used for empirical treatment.

Table 1

Antibiogram for gram-positive bacteria isolated from canine and feline OSU-VMC patients in 2018.

Percentage of susceptible isolates
Bacterial genus or species No. of isolates Amikacin Amoxicillin–clavulanic acid Ampicillin Cephalothin Cefazolin Cefovecin Cefpodoxime Chloramphenicol Clindamycin Doxycycline Enrofloxacin Erythromycin Gentamicin Marbofloxacin Minocycline Oxacillin + 2% NaCl* Penicillin Pradofloxacin Rifampin Tetracycline Trimethoprim-sulfamethoxazole
Staphylococcus aureus 12 92 75 75 75 NA 75 100 58 92 75 58 92 75 92 75 75 NA 75 100
Staphylococcus pseudintermedius (all) 220 100 58 58 58 58 58 83 49 55 58 48 71 64 57 58 65 61 55 54
S pseudintermedius (skin) 91 100 60 60 60 60 60 88 54 52 63 54 77 70 54 60 69 63 52 59
S pseudintermedius (tissue) 36 100 50 50 47 50 50 81 42 67 44 42 64 53 69 50 53 50 67 50
Staphylococcus schleiferi 24 96 46 46 46 46 46 100 100 92 29 100 79 42 100 46 46 NA 88 100
Enterococcus spp 63 IR 77 78 NA IR NA NA 92 NA 52 NA 24 IR NA 45 NA 76 NA 18 54 IR

Percentages of isolates susceptible to each antimicrobial were determined on the basis of Clinical and Laboratory Standards Institute guidelines,21 except that the Clinical and Laboratory Standards Institute recommends that data from a minimum of 30 isolates be used. Organisms with intermediate susceptibility were classified as resistant.

Susceptibility to oxacillin was used to identify and monitor methicillin-resistant Staphylococcus spp and not to determine applicability for therapeutic use.

Includes isolates from skin swab specimens (eg, swab specimens from pustules and collarettes), deep skin scrapings, skin punch biopsy specimens, and samples from draining tracts.

Includes Staphylococcus schleiferi subsp schleiferi and Staphylococcus schleiferi subsp coagulans.

Includes Enterococcus faecalis and Enterococcus faecium.

— = Not reported because β-lactamase production was not determined by the laboratory. IR = Intrinsic resistance; percentage susceptible was not reported because bacteria were considered intrinsically resistant to this antimicrobial. NA = No clinical interpretation of susceptibility was available.22,23

Table 2

Antibiogram for gram-negative bacteria isolated from canine and feline OSU-VMC patients in 2018.

Percentage of susceptible isolates
Bacterial genus or species No. of isolates Amikacin Amoxicillin–clavulanic acid Ampicillin Cefazolin Cefpodoxime Ceftazidime* Cephalexin Chloramphenicol Doxycycline Enrofloxacin Gentamicin Marbofloxacin Pradofloxacin Tetracycline Trimethoprim-sulfamethoxazole
Escherichia coli (all) 261 99 49 41 79 80 88 75 85 85 85 93 87 86 84 89
E coli (urine) 164 99 78 64 85 85 90 80 84 93 92 96 93 93 91 96
Enterobacter cloacae 21 100 IR IR IR 57 62 IR 76 62 67 91 71 NA 62 67
Klebsiella spp 23 100 52 IR 70 78 78 74 87 65 74 74 74 NA 70 74
Proteus spp 54 93 74 72 70 91 94 33 59 IR 87 85 90 83 IR 87
Pseudomonas aeruginosa 47 98 IR NA IR NA 95 NA IR IR 52 77 NA NA IR IR

Breakpoints used for interpretation of susceptibility to ceftazidime (susceptible, ≤ 8 µg/mL; intermediate, ≤ 16 µg/mL; and resistant ≥ 32 µg/mL) were the same as those used for Enterobacteriales.23

Includes isolates from urine samples obtained by clean catch or cystocentesis or from a urinary catheter.

Includes Klebsiella oxytoca and Klebsiella pneumoniae.

Includes Proteus vulgaris and Proteus mirabilis.

See Table 1 for remainder of key.

Over the past 18 months, we have used passive surveillance to monitor for changes in susceptibility patterns of pathogens recovered from OSU-VMC patients, particularly changes in susceptibility to antimicrobials classified as protected use because these antimicrobials are often the last resort for treatment of multidrug-resistant bacterial infections. Antimicrobial susceptibility data recovered through the antimicrobial stewardship program have so far been consistent with our expectations for a tertiary referral hospital. Patients referred for treatment of resistant bacterial infections have commonly been treated with 1 or more first-line antimicrobials. For example, of Escherichia coli isolates from dogs and cats treated at the OSU-VMC because of uncomplicated urinary tract infection, only 64% have been susceptible to ampicillin, a common first-line antimicrobial for empirical treatment of this type of infection. Less than 60% of all Staphylococcus isolates were susceptible to methicillin and other β-lactam antimicrobials, including first-generation cephalosporins commonly used as first-line empirical treatment for Staphylococcus pseudintermedius infections. The antibiograms developed by the OSU-VMC antimicrobial stewardship program provide clinicians objective information they can use to tailor their treatment plans to maximize successful outcomes and minimize treatment failures when using empirical treatments.

Active Environmental Surveillance

Active environmental surveillance generates new data as part of the surveillance program and involves determining the existence and extent of contamination of the hospital environment with resistant bacteria. This is a key component of the antimicrobial stewardship program and allows us to identify patterns of bacterial contamination over time and identify potential resident nosocomial (hospital-associated) pathogens.

Active surveillance for targeted resistant bacteria in the OSU-VMC environment began in January 2018 and assists us in addressing the threat of nosocomial infections and identifying and addressing environmental contamination issues quickly. Environmental sampling is performed in all 3 of the OSU-VMC's hospitals to collect data regarding the presence of bacteria of concern. Once a month, members of the ASWG use electrostatic clothsb to collect samples from surfaces subject to human and animal contact or to human contact alone. Each sample is cultured for Salmonella spp,24 extended-spectrum cephalosporin-resistant Enterobacteriaceae,25,26 carbapenem-resistant Enterobacteriales,26,27 and methicillin-resistant Staphylococcus aureus and S pseudintermedius.28 Samples are collected from > 100 sites selected on the basis of previous surveillance programs, identified as areas of concern by hospital personnel, and acknowledged as common areas of contamination for the targeted organisms. Prevalences are calculated to gauge the effectiveness of infection control and biosecurity protocols in reducing environmental contamination with resistant bacteria.

The percentage of samples from human-only contact surfaces (eg, computer keyboards, door handles, telephones, and automated prescription-dispensing machines) positive for antimicrobial-resistant organisms in our hospital (19.8%) has been similar to the percentage of samples from human and animal contact surfaces that have been positive (25.5%). We commonly recover Enterobacteriaceae (E coli, Klebsiella spp, and Enterobacter spp) resistant to extended-spectrum cephalosporins (496/2,016 [24.6%] samples) from the OSU-VMC environment, which is expected for any hospital where use of β-lactam antimicrobials is common. Over a period of 19 months, recovery of Salmonella spp and carbapenem-resistant Enterobacteriales remained low in our hospital environment (16/2,016 [0.7%] and 15/2,016 [0.8%], respectively). Recovery of methicillin-resistant Staphylococcus organisms during this period was < 20% for 16 of those 19 months.

To maintain a successful antimicrobial stewardship program, effective infection control measures, such as isolation protocols, clearly defined cleaning and disinfection procedures, and promotion of proper hand-hygiene practices, must be in place. The active environmental surveillance component of our antimicrobial stewardship program complements the OSU-VMC Infection Control Program by generating data that allow us to identify and address environmental contamination issues before they become a problem. In fact, these data helped to identify and address potential nosocomial infections on 2 occasions since we began active environmental surveillance. However, we do not yet have a defined process for real-time detection of potential nosocomial outbreaks. Our consistently low recovery of resistant organisms from the hospital environment is an indicator of the effectiveness of our existing cleaning and disinfection protocols and biosecurity measures. We believe it is normal to find some resistant organisms in the patient-contact areas of the hospital owing to the nature of our patient population. However, our recovery rates of resistant organisms from human-only contact surfaces indicated a need to improve our hand-hygiene practices and reevaluate cleaning and disinfection protocols for these surfaces. These data are now supporting the implementation of a new hand-hygiene campaign throughout the OSU-VMC.

Education

The ASWG has incorporated an educational component into the antimicrobial stewardship program efforts to increase student, faculty, and staff awareness of antimicrobial stewardship and veterinary medicine's role in the reduction of antimicrobial resistance. One of the primary objectives of our program has been to train future veterinarians in responsible antimicrobial use and prescribing practices. Our goal is for new graduates to bring their knowledge of antimicrobial stewardship with them into private practices and other institutions, engaging even more people in the fight against antimicrobial resistance. Multiple strategies have been used to address education, including implementing an online education program on responsible antimicrobial use, widely disseminating the antimicrobial use guidelines, and providing training on the antimicrobial stewardship program and antimicrobial use guidelines to incoming interns and residents during their orientation. The ASWG is working to help students develop an intrinsic motivation to become good antimicrobial stewards, as opposed to relying solely on the extrinsic motivation of the OSU-VMC antimicrobial stewardship program during their fourth year. Developing this intrinsic motivation involves incorporating stewardship training prior to the clinical year. Teaching materials supporting responsible antimicrobial use have already been incorporated into the second and third years of the professional curriculum at OSU-CVM. These include lectures, assignments, and quizzes focused on clinical decision-making regarding antimicrobial use and antimicrobial stewardship in practice. Plans for introducing these concepts in the first year of the professional curriculum are currently in development. Once the curriculum is in place for all 4 years of training, the ASWG will shift its focus to assessing the impact of this training. Surveys and assessments evaluating student understanding of these topics will be administered before and after delivery of antimicrobial stewardship program training to determine knowledge uptake and overall retention.

Future Expansion of the Antimicrobial Stewardship Program

The ASWG recognizes the need for stewardship practices beyond the academic community, and we intend to help address this need in the coming years. In 2020, the OSU-CVM launched the BuckeyeASP. This is a 3-year certification program that will provide antimicrobial stewardship resources and expertise to veterinarians throughout Ohio and actively engage them in the fight against antimicrobial resistance. Private veterinary practices (including companion animal, equine, large animal, mixed animal, and specialty practices) will voluntarily participate and work with the ASWG to tailor the OSU-CVM antimicrobial stewardship program to fit their individual practice needs. This includes adapting the OSU-CVM antimicrobial use guidelines to each hospital's antimicrobial use practices and drug inventory, establishing an achievable passive surveillance program for antimicrobial prescribing, establishing a passive surveillance program for results of bacterial culture and antimicrobial susceptibility testing, developing an active environmental surveillance program for each clinic, and training staff on how to collect surveillance samples. Partner clinics will work with OSU-VMC pharmacists, veterinary epidemiologists, and clinical microbiologists to analyze generated data, evaluate antimicrobial prescribing practices, perform antimicrobial resistance risk assessments, and develop or improve practice biosecurity and infection control programs. The ASWG recognizes that financial restraints serve as a roadblock to the development of antimicrobial stewardship programs in private practice. We believe that partnering with private practices through this program can help practitioners defer the cost of building a program while receiving subsidized active surveillance bacterial culture and susceptibility testing, free phone consultations, and free training activities and materials. Additionally, the ASWG is developing a website for the program where practitioners will be able to access surveillance data, compare their antimicrobial use practices with the practices of other hospitals in their area, and download client handouts discussing antimicrobial stewardship and the program. There will be a section on the website for clients who wish to learn more about the program and how it benefits their family and pets.

Phase 1 of the BuckeyeASP, currently in progress, involves partnerships with the OSU Dublin Veterinary Medical Center (an orthopedic surgery facility with limited specialty services and an urgent care service) and the OSU Marysville Large Animal Services Ambulatory Clinic. These affiliate hospitals function more as private specialty (Dublin) and general (Marysville) practices than tertiary referral centers. Partnering with them provides experience with private diagnostic laboratories (for patient submissions) and a range of practice management software. Lessons learned during this first phase will be used to better adapt the BuckeyeASP to function efficiently when introduced into additional private veterinary practices. Phase 2 of the program involves partnerships with interested private practices in the Columbus Metropolitan area; phase 3 extends the program into practices throughout Ohio. Enrollment in phase 2 will be limited to 3 to 5 practices during the first year. This controlled enrollment will provide the ASWG with an understanding of the time and resources necessary to serve each practice. Phase 2 will also allow the ASWG to receive feedback on the program and how it can be improved to better serve practices in the future. Feedback will be solicited from all practices upon full program implementation to continually improve the program and better integrate antimicrobial stewardship into veterinary practice.

Participation in the BuckeyeASP will be promoted by the OSU-CVM as a quality indicator for Ohio veterinary practices, demonstrating to veterinary clients that participating practices are committed to and promote responsible antimicrobial use. This program can serve as a model for moving stewardship practices beyond principles and into actions in veterinary private practice facilities. The BuckeyeASP is aligned with the community outreach and engagement goal of OSU-CVM's strategic plan.29

Conclusions

Veterinarians take an oath to protect animal and public health. Therefore, we are obligated to engage in the fight against antimicrobial resistance by acting as stewards of antimicrobial drugs. Recently, many veterinary organizations have encouraged incorporating the theories and principles of antimicrobial stewardship into clinical veterinary education and practice. Unfortunately, veterinary practitioners do not have effective models readily available to aid in translating theory into practice. The OSU-CVM's ASWG designed an antimicrobial stewardship program that puts these principles and concepts of stewardship into action while focusing on educating future veterinarians about judicious antimicrobial use. Additionally, the ASWG continues to work with our human hospital counterpart to grow and improve our program while also reaching out to the community. The BuckeyeASP will move stewardship into private practice, empowering veterinary practitioners to provide exceptional care to patients while preserving medically important antimicrobial drugs and preventing the development of antimicrobial resistance. We hope this model can be adapted by other veterinary medical centers or institutions that are considering establishing their own antimicrobial stewardship programs and incorporating antimicrobial stewardship into their curriculum, practice, and community and professional outreach.

Acknowledgments

Financial support for this program was provided by the OSU Infectious Disease Institute and OSU-CVM Infectious Disease Signature Program.

The authors thank Drs. Julie Byron, Margaret Mudge, and Jeff Lakritz for their service on the Senior Clinician Advisory Group.

Footnotes

a.

Sensititre SWIN Epidemiology Module, Thermo Fisher Scientific, Waltham, Mass.

b.

Swiffer, Procter & Gamble, Cincinnati, Ohio.

Abbreviations

ASWG

Antimicrobial Stewardship Working Group

BuckeyeASP

Buckeye Antimicrobial Stewardship Program

OSU

Ohio State University

OSU-CVM

Ohio State University College of Veterinary Medicine

OSU-VMC

Ohio State University Veterinary Medical Center

References

  • 1.

    Boerlin P, White DG. Antimicrobial resistance and its epidemiology. In: Giguère S, Prescott JF, Dowling PM, eds. Antimicrobial therapy in veterinary medicine. 5th ed. Ames, Iowa: John Wiley and Sons Inc, 2013;2743.

    • Search Google Scholar
    • Export Citation
  • 2.

    AVMA. Antimicrobial stewardship definition and core principles. Available at: www.avma.org/resources-tools/avma-policies/antimicrobial-stewardship-definition-and-core-principles. Accessed Feb 14, 2020.

    • Search Google Scholar
    • Export Citation
  • 3.

    AVMA. Judicious therapeutic use of antimicrobials. Available at: www.avma.org/resources-tools/avma-policies/judicious-therapeutic-use-antimicrobials. Accessed Feb 14, 2020.

    • Search Google Scholar
    • Export Citation
  • 4.

    US FDA Center for Veterinary Medicine. Supporting antimicrobial stewardship in veterinary settings: goals for fiscal years 2019–2023. Washington, DC: US FDA Center for Veterinary Medicine, 2018.

    • Search Google Scholar
    • Export Citation
  • 5.

    Fishman N, Society for Healthcare Epidemiology of America, Infectious Diseases Society of America. Policy statement on antimicrobial stewardship by the Society for Healthcare Epidemiology of America (SHEA), the Infectious Diseases Society of America (IDSA), and the Pediatric Infectious Diseases Society (PIDS). Infect Control Hosp Epidemiol 2012;33:322327.

    • Search Google Scholar
    • Export Citation
  • 6.

    Federico F. The five rights of medication administration. Available at: www.ihi.org/resources/Pages/ImprovementStories/FiveRightsofMedicationAdministration.aspx. Accessed Feb 14, 2020.

    • Search Google Scholar
    • Export Citation
  • 7.

    Grissinger M. The five rights: a destination without a map. P&T 2010;35:542.

  • 8.

    Stevenson KB, Balada-Llasat J, Bauer K, et al. The economics of antimicrobial stewardship: the current state of the art and applying the business case model. Infect Control Hosp Epidemiol 2012;33:389397.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9.

    Thompson CA. Antimicrobial stewardship in hospitals to become national requirement. Am J Health Syst Pharm 2016;73:11121116.

  • 10.

    Centers for Medicare and Medicaid Services. The Hospital Value-Based Purchasing (VBP) Program. Available at: www.cms.gov/Medicare/Quality-Initiatives-Patient-Assessment-Instruments/Value-Based-Programs/HVBP/Hospital-Value-Based-Purchasing. Accessed Apr 16, 2020.

    • Search Google Scholar
    • Export Citation
  • 11.

    The Joint Commission. Why achieve accreditation? Available at: www.jointcommission.org/accreditation-and-certification/become-accredited/why-achieve-accreditation/. Accessed Apr 16, 2020.

    • Search Google Scholar
    • Export Citation
  • 12.

    Guardabassi L, Prescott JF. Antimicrobial stewardship in small animal veterinary practice: from theory to practice. Vet Clin North Am Small Anim Pract 2015;45:361376.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13.

    The Ohio State University College of Medicine. ASP frequently asked questions. Available at: medicine.osu.edu/departments/pharmacy/asp/introfaq. Accessed Apr 16, 2020.

    • Search Google Scholar
    • Export Citation
  • 14.

    Pollack LA, Srinivasan A. Core elements of hospital antibiotic stewardship programs from the Centers for Disease Control and Prevention. Clin Infect Dis 2014;59(suppl 3):S97S100.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15.

    AVMA. Antimicrobial use in veterinary practice. Available at: www.avma.org/antimicrobial-use-veterinary-practice. Accessed Dec 13, 2019.

    • Search Google Scholar
    • Export Citation
  • 16.

    American Association of Bovine Practitioners. Key elements for implementing antimicrobial stewardship plans in bovine veterinary practices working with beef and dairy operations. Available at: aabp.org/resources/AABP_Guidelines/AntimicrobialStewardship-7.27.17.pdf. Accessed Feb 14, 2020.

    • Search Google Scholar
    • Export Citation
  • 17.

    American Association of Feline Practitioners. Basic guidelines of judicious therapeutic use of antimicrobials. Available at: catvets.com/public/PDFs/PracticeGuidelines/Guidelines/2014AntimicrobialsGuidelines%20AAHA_AAFP.pdf. Accessed Feb 14, 2020.

    • Search Google Scholar
    • Export Citation
  • 18.

    AVMA. Veterinary checklist for antimicrobial stewardship. Available at: www.avma.org/sites/default/files/2020–06/Veterinary-Checklist-Antimicrobial-Stewardship.pdf. Accessed Dec 13, 2019.

    • Search Google Scholar
    • Export Citation
  • 19.

    World Health Organization. Critically important antimicrobials for human medicine; 6th revision. Available at: apps.who.int/iris/bitstream/handle/10665/312266/9789241515528-eng.pdf?ua=1. Accessed Dec 9, 2019.

    • Search Google Scholar
    • Export Citation
  • 20.

    The Ohio State University. OSU VMC antimicrobial use guidelines. Available at: ohiostate.pressbooks.pub/osuvmcabxuse/. Accessed Sep 1, 2020.

    • Search Google Scholar
    • Export Citation
  • 21.

    Clinical and Laboratory Standards Institute. Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals. CLSI supplement VET08. 4th ed. Wayne, Pa: Clinical and Laboratory Standards Institute, 2018.

    • Search Google Scholar
    • Export Citation
  • 22.

    Clinical and Laboratory Standards Institute. Analysis and presentation of cumulative antimicrobial susceptibility test data; approved guideline. CLSI document M39–A4. 4th ed. Wayne, Pa: Clinical and Laboratory Standards Institute, 2014.

    • Search Google Scholar
    • Export Citation
  • 23.

    Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing. CLSI supplement M100. 30th ed. Wayne, Pa: Clinical and Laboratory Standards Institute, 2020.

    • Search Google Scholar
    • Export Citation
  • 24.

    Ruple-Czerniak A, Bolte DS, Burgess BA, et al. Comparison of two sampling and culture systems for detection of Salmonella enterica in the environment of a large animal hospital. Equine Vet J 2014;46:499502.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25.

    Adams RJ, Kim SS, Mollenkopf DF, et al. Antimicrobial-resistant Enterobacteriaceae recovered from companion animal and livestock environments. Zoonoses Public Health 2018;65:519527.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26.

    Mathys DA, Mollenkopf DF, Van Balen JC, et al. β-Lactam and fluoroquinolone-resistant Enterobacteriaceae recovered from the environment of human and veterinary tertiary care hospitals. Vector Borne Zoonotic Dis 2018;18:620623.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27.

    Adams RJ, Mathys DA, Mollenkopf DF, et al. Carbapenemase-producing Aeromonas veronii disseminated in the environment of an equine specialty hospital. Vector Borne Zoonotic Dis 2017;17:439442.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28.

    van Balen J, Kelley C, Nava-Hoet RC, et al. Presence, distribution, and molecular epidemiology of methicillin-resistant Staphylococcus aureus in a small animal teaching hospital: a year-long active surveillance targeting dogs and their environment. Vector Borne Zoonotic Dis 2013;13:299311.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29.

    The Ohio State University. Be the model. Available at: vet.osu.edu/about-college/strategic-plan. Accessed Sep 1, 2020.

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