Importance
Inappropriate antimicrobial drug use is associated with adverse events in hospitalized patients and contributes to the emergence and spread of resistant pathogens. Targeting effective interventions to improve antimicrobial use in the acute care setting requires understanding hospital prescribing practices.
Objective
To determine the prevalence of and describe the rationale for antimicrobial use in participating hospitals.
Design, Setting, and Participants
One-day prevalence surveys were conducted in acute care hospitals in 10 states between May and September 2011. Patients were randomly selected from each hospital’s morning census on the survey date. Data collectors reviewed medical records retrospectively to gather data on antimicrobial drugs administered to patients on the survey date and the day prior to the survey date, including reasons for administration, infection sites treated, and whether treated infections began in community or health care settings.
Main Outcomes and Measures
Antimicrobial use prevalence, defined as the number of patients receiving antimicrobial drugs at the time of the survey divided by the total number of surveyed patients.
Results
Of 11 282 patients in 183 hospitals, 5635 (49.9%; 95% CI, 49.0%-50.9%) were administered at least 1 antimicrobial drug; 77.5% (95% CI, 76.6%-78.3%) of antimicrobial drugs were used to treat infections, most commonly involving the lower respiratory tract, urinary tract, or skin and soft tissues, whereas 12.2% (95% CI, 11.5%-12.8%) were given for surgical and 5.9% (95% CI, 5.5%-6.4%) for medical prophylaxis. Of 7641 drugs to treat infections, the most common were parenteral vancomycin (1103, 14.4%; 95% CI, 13.7%-15.2%), ceftriaxone (825, 10.8%; 95% CI, 10.1%-11.5%), piperacillin-tazobactam (788, 10.3%; 95% CI, 9.6%-11.0%), and levofloxacin (694, 9.1%; 95% CI, 8.5%-9.7%). Most drugs administered to treat infections were given for community-onset infections (69.0%; 95% CI, 68.0%-70.1%) and to patients outside critical care units (81.6%; 95% CI, 80.4%-82.7%). The 4 most common treatment antimicrobial drugs overall were also the most common drugs used for both community-onset and health care facility–onset infections and for infections in patients in critical care and noncritical care locations.
Conclusions and Relevance
In this cross-sectional evaluation of antimicrobial use in US hospitals, use of broad-spectrum antimicrobial drugs such as piperacillin-tazobactam and drugs such as vancomycin for resistant pathogens was common, including for treatment of community-onset infections and among patients outside critical care units. Further work is needed to understand the settings and indications for which reducing antimicrobial use can be most effectively and safely accomplished.
Antimicrobial drugs have saved countless lives over the past century, and studies show that timely administration of appropriate antimicrobial therapy to severely ill, infected patients is essential to avoid infection-related morbidity and mortality.1-3 Despite the evidence supporting early, appropriate therapy, a substantial proportion of antimicrobial use in US acute care hospitals may be inappropriate, based on factors such as lack of indication or incorrect drug selection, dosing levels, or treatment duration.4-6Quiz Ref IDExposure to antimicrobial drugs is also a risk factor for the acquisition of resistant and difficult-to-treat pathogens, such as carbapenem-resistant Enterobacteriaceae7,8 and Clostridium difficile,9,10 and antimicrobial drugs are leading causes of adverse drug events.11,12 Inappropriate antimicrobial use needlessly puts patients at risk of these complications.
One aspect of a multifaceted approach to reducing antimicrobial-resistant infections is improving antimicrobial use.13,14 To improve use and reduce preventable harm in US hospitals, it is necessary to understand inpatient antimicrobial-drug–use epidemiology. There have been few large-scale efforts to define antimicrobial-drug–use epidemiology in US acute care hospitals.15-17 Studies performed in the last decade have shown that approximately 60% of adult and pediatric inpatients receive antimicrobial drugs during their hospitalizations.15,16 Significant increases in the use of piperacillin-tazobactam, carbapenems, and vancomycin in adult patients were seen in an analysis of 2002-2006 data.15 Most studies to date have used administrative data and focused on measuring the volume of antimicrobial use, without assessing the rationale for use at the patient level. We performed a multistate, acute care hospital antimicrobial-drug use prevalence survey in 2011 to determine the prevalence of inpatient antimicrobial-drug use, the most common antimicrobial drug types, and the reasons for their use.
Hospital and Patient Selection
The antimicrobial-drug use survey was performed in conjunction with a survey of health care–associated infections conducted by the Centers for Disease Control and Prevention (CDC) and the Emerging Infections Program (EIP) in California, Colorado, Connecticut, Georgia, Maryland, Minnesota, New Mexico, New York, Oregon, and Tennessee.18 The CDC deemed the survey to be a public health surveillance activity, and participating state health departments, EIP academic partners, and hospitals either approved the project in accordance with human subjects research requirements with waivers of informed consent or determined the survey was not human subjects research.
Within each EIP site’s catchment area, general acute care and children’s hospitals were stratified according to bed size. Random samples were drawn from each stratum, with a goal of engaging up to 13 small (<150 beds), 9 medium (150-399 beds), and 3 large (≥400 beds) hospitals per site. These goal numbers were based on the size distribution of all general acute care hospitals in the EIP sites, the numbers of hospitals within the selected catchment areas for the survey, and taking into account EIP site resources needed to support the survey. An alternate hospital from within the same bed-size stratum was recruited in cases for which a selected hospital declined to participate.
Each hospital performed a 1-day survey that included a random sample of acute care inpatients identified from the morning census on the survey date. Large hospitals surveyed 100 patients, and small and medium hospitals surveyed either 75 patients or all eligible acute care inpatients if the census was fewer than 75 patients on the survey date. The target numbers of patients per hospital were selected to enhance the efficiency of survey planning and minimize burden to hospitals while ensuring adequate precision of health care–associated infection prevalence estimates.
Data collectors reviewed medical records on the survey date to determine whether patients may have been receiving enteral (excluding rectal), intravenous, intramuscular, or inhaled antimicrobial drugs (eMethods 1 in the Supplement) at the time of the survey, using the following screening criteria: (1) the patient was administered or was scheduled to be administered at least 1 antimicrobial drug on the survey date or the calendar day prior to the survey date; (2) the patient was a patient undergoing dialysis who received or was scheduled to receive parenteral vancomycin or an aminoglycoside during the 4 days prior to the survey date; or (3) the patient’s antimicrobial drug information was unknown or was not available at the time of the survey. Topical antimicrobials were excluded. The EIP surveillance epidemiologists retrospectively reviewed medical records of patients who met screening criteria to collect information on antimicrobial drugs given to the patient on the survey date or the calendar day prior to the survey date and parenteral vancomycin and aminoglycosides when administered during the 4 calendar days prior to the survey date to patients undergoing dialysis. Acceptable sources of antimicrobial drug administration data included electronic or paper emergency department and inpatient medication administration records and operating room flow sheets.
At the time of data collection, antimicrobial drugs were considered unique at the drug-administration route level: each antimicrobial drug could be recorded up to 2 times for a given patient if that antimicrobial drug was administered via 2 different routes at the time of the survey (eg, intravenous to oral administration transition for certain antimicrobial drugs). For each drug-route combination, data collectors recorded the rationale for use: treatment of infection, surgical prophylaxis, medical prophylaxis, a noninfection-related reason, or unknown rationale. Empirical use of antimicrobial drugs for suspected infection was considered treatment. Noninfection-related reasons for antimicrobial drug administration included treatment of conditions not primarily considered to be infectious in nature, such as erythromycin for impaired gastrointestinal motility. For antimicrobial drugs given to treat infections, data collectors identified the anatomical site of infection and the location of onset (survey hospital, other health care facility, or community) based on clinician documentation in the medical record. Although National Healthcare Safety Network (NHSN) health care–associated infection surveillance definitions were used in the health care–associated infection portion of the survey,18 they were not used in collecting data on infections for which antimicrobial drugs were given. Multiple rationales, infection sites, and onset locations could be reported for each drug.
Data analysis was performed using SAS version 9.3 (SAS Institute Inc) and OpenEpi version 3.01.19 Antimicrobial drug data were analyzed so that drugs were considered unique and distinct based on the World Health Organization (WHO) Anatomical Therapeutic Chemical fifth-level (ie, chemical substance) classification. According to this classification system, most antimicrobial drugs included in the survey were considered unique based on the chemical substance name (eg, ciprofloxacin, azithromycin, clindamycin, etc), without regard to the route of administration. However, for some antimicrobial drugs the enteral and parenteral formulations were considered distinct drugs: vancomycin, metronidazole, colistin, polymyxin B, amphotericin B, streptomycin, and neomycin.20,21 For example, a patient whose only antimicrobial drugs at the time of the survey were oral and intravenous ciprofloxacin (during an intravenous-to-oral transition day, for example) would be considered to be receiving a single antimicrobial drug because the oral and intravenous formulations of ciprofloxacin are not considered distinct from one another. By contrast, a patient whose only antimicrobial drugs at the time of the survey were oral and intravenous vancomycin would be considered to be receiving 2 antimicrobial drugs because the oral and intravenous formulations of vancomycin are considered distinct.
Antimicrobial drug data were analyzed and reported using WHO Anatomical Therapeutic Chemical fourth-level classifications (the drug subgroup, for example, fluoroquinolones) and fifth-level classifications (the chemical substance name, eg, levofloxacin). The most common individual antimicrobial drugs or drug subgroups administered in particular settings were determined on the basis of the rank order of the point estimates of the proportions of all antimicrobial drugs (or patients). The mid-P exact method was used to generate confidence intervals for antimicrobial use prevalence, defined as the number of patients receiving at least 1 antimicrobial drug divided by the total number of surveyed patients, and for other proportions. Categorical and continuous variables were compared in patients receiving or not receiving antimicrobial drugs using the χ2 and median tests, respectively. Two-sided P values <.05 were considered statistically significant.
Surveys were conducted in 183 hospitals from May to September 2011. The numbers of hospitals and patients surveyed in each EIP site have been published.18 Twenty-two of 183 hospitals (12%) were large hospitals, 68 (37%) were medium, and 93 (51%) were small. The median number of patients surveyed per hospital overall was 75 (interquartile range [IQR], 39-75). The median number of patients surveyed in large hospitals was 100 (IQR, 100-100); in medium hospitals 75 (IQR, 75-75); and in small hospitals 40 (IQR, 23-70). Of 11 282 patients, 5860 (51.9%) met antimicrobial use screening criteria; of these, 5847 (99.8%) received or were scheduled to receive antimicrobial drugs on the day of the survey or the day before the survey, and 13 (0.2%) met other criteria.
Prevalence of Antimicrobial Use
Among the 5860 patients who met antimicrobial use screening criteria, 5635 (96.2%) were confirmed to have received 1 or more antimicrobial drugs at the time of the survey. The antimicrobial use prevalence was therefore 49.9% (95% CI, 49.0%-50.9%). Although most patients receiving antimicrobial drugs were outside of critical care units (4650 patients, 82.5%; 95% CI, 81.5%-83.5%), antimicrobial drug use prevalence was higher in critical care units than in other locations (57.7%, 95% CI, 55.4%-60.0% vs 48.6%, 95% CI, 47.6%-49.6%; P < .001; Table 1).
A total of 9967 antimicrobial drug-route combinations were administered. After conforming to WHO Anatomical Therapeutic Chemical fifth-level classifications, 9865 antimicrobial drug records remained, representing 90 unique antimicrobial drugs. Of 5635 patients receiving antimicrobial drugs, 2811 (49.9%; 95% CI, 48.6%-51.2%) were receiving 1 antimicrobial drug; 1840 (32.7%; 95% CI, 31.4%-33.9%), 2 antimicrobial drugs; 682 (12.1%; 95% CI, 11.3%-13.0%), 3 antimicrobial drugs; and 302 patients (5.4%; 95% CI, 4.8%-6.0%), 4 or more antimicrobial drugs.
Patients receiving antimicrobial drugs were older, with a median age of 62 years (IQR, 44-76 years) compared with 53 years for patients not receiving antimicrobial drugs (IQR, 24-71 years; P < .001). Patients receiving antimicrobial drugs were also more likely than patients not receiving antimicrobial drugs to be men, white, in a critical care unit, and in a small hospital (eTable 1 in the Supplement).
Common Antimicrobial Drugs
Of the 9865 antimicrobial drugs used, 1388 (14.1%) were fluoroquinolones (95% CI, 13.4%-14.8%); 1213 (12.3%), parenteral glycopeptides (95% CI, 11.7%-13.0%); 1081 (11.0%), penicillin combinations (95% CI, 10.4%-11.6%); 1037 (10.5%) third-generation cephalosporins (95% CI, 9.9%-11.1%); and 983 (10.0%), first-generation cephalosporins (95% CI, 9.4%-10.6%; eTable 2 in the Supplement). Of the individual antimicrobial drugs used overall, 1212 (12%) were parenteral vancomycin (95% CI, 11.7%-12.9%); 913 (9.3%), cefazolin (95% CI, 8.7%-9.8%); 864 (8.8%), ceftriaxone (95% CI, 8.2%-9.3%); 829 (8.4%), piperacillin-tazobactam (95% CI, 7.9%-9.0%); and 768 (7.8%), levofloxacin (95% CI, 7.3%-8.3%).
Rationale for Antimicrobial Drug Use
Overall, of the 5635 patients receiving antimicrobial drugs, 4278 (75.9%; 95% CI, 74.8%-77.0%) were receiving them to treat infections; 1071 (19.0%; 95% CI, 18.0%-20.1%) for surgical prophylaxis; 388 (6.9%; 95% CI, 6.2%-7.6%) for medical prophylaxis; 40 (0.71%; 95% CI, 0.51%-0.96%) for noninfection-related reasons; and 390 (6.9%; 95% CI, 6.3%-7.6%) for no documented rationale.
The reasons for use of antimicrobial drugs in selected WHO Anatomical Therapeutic Chemical fourth-level groups are shown in eTable 3 of the Supplement. For most drug groups, infection treatment was the most common reason for use. Surgical prophylaxis was the most common reason for use of first-generation cephalosporins (72.2%; 95% CI, 69.4%-75.0%) and second generation cephalosporins (56.7%; 95% CI, 48.0%-65.1%), and medical prophylaxis was the most common reason for use of nucleoside and nucleotide antivirals (48.5%; 95% CI, 41.7%-55.4%). Of the 9865 individual antimicrobial drugs used, 7641 (77.5%; 95% CI 76.6%-78.3%) were given to treat infections, with or without other reasons for use. Eighty-three different individual antimicrobial drugs were used to treat infections. Of those 7641 treatment antimicrobial drugs used, 1229 (16.1%) were fluoroquinolones (95% CI, 15.3%-16.9%); 1104 (14.4%), parenteral glycopeptides (95% CI, 13.7%-15.3%); 1000 (13.1%), penicillin combinations (95% CI, 12.3%-13.9%); and 983 (12.9%), third-generation cephalosporins (95% CI, 12.1%-13.6%).
Surgical prophylaxis was reported as a rationale for 1199 antimicrobial drugs (12.2%; 95% CI, 11.5%-12.8%), with or without other reasons for use. Five of 35 different antimicrobial drugs accounted for more than 80% of drugs given for surgical prophylaxis: 715, cefazolin (59.6%; 95% CI, 56.8%-62.4%); 91, parenteral vancomycin (7.6%; 95% CI, 6.2%-9.2%); 77, clindamycin (6.4%; 95% CI, 5.1%-7.9%); 44, parenteral metronidazole (3.7%; 95% CI, 2.7%-4.9%); and 43, cefoxitin (3.6%; 95% CI, 2.6%-4.8%).
Medical prophylaxis was reported as a rationale for 583 antimicrobial drugs (5.9%; 95% CI, 5.5%-6.4%), with or without other reasons for use. A total of 54 different antimicrobial drugs were administered for medical prophylaxis, although 5 antimicrobial drugs accounted for almost half of those used for medical prophylaxis: 69 (11.5%) of 583 were acyclovir (95% CI, 9.4%-14.7%); 67 (11.5%), trimethoprim-sulfamethoxazole (11.5%; 95% CI, 9.1%-14.3%); 56 (9.6%), benzylpenicillin (95% CI, 7.4%-12.2%); 51 (8.8%), fluconazole (95% CI, 6.7%-11.3%); and 32 (5.5%), azithromycin (95% CI, 3.8%-7.6%).
Fifty-seven of 69 patients receiving prophylactic acyclovir (82.6%; 95% CI, 72.3%-90.2%]) and 30 of 51 patients receiving prophylactic fluconazole (58.8%; 95% CI, 45.0%-71.7) were located in hematology/oncology, hematopoietic stem cell transplant, or solid organ transplant units. Fifty-three of 56 patients (94.6%) receiving prophylactic benzylpenicillin were in obstetrical care locations (95% CI, 86.1%-98.6%).
A noninfection-related rationale for use was reported for 41 antimicrobial drugs (0.42%; 95% CI, 0.30%-0.56%; eTable 4 in the Supplement). No rationale could be identified in the medical record for 455 antimicrobial drugs (4.6%; 95% CI, 4.2%-5.0%; eTable 5 in the Supplement).
Antimicrobial Drugs Administered to Treat Infections
Of all antimicrobial drugs used to treat infections, 2607 (34.1%) were for lower respiratory tract (95% CI, 33.1%-35.2%), 1302 (17.0%) for urinary tract infections (95% CI, 16.2%-17.9%), 1177 (15.4%) for skin and soft tissue infections (95% CI, 14.6%-16.2%), and 829 (10.8%) for gastrointestinal tract infections (95% CI, 10.2%-11.6%) and 661 (8.7%) for infections of undetermined site, including empirical therapy for suspected infection (95% CI, 8.0%-9.3%; Table 2). Of the 7641 antimicrobial drugs given to treat infections, 4154 (54.4%; 95% CI, 53.3%-55.5%) were given to treat lower respiratory tract–only infections, urinary tract–only infections, or skin and soft tissue–only infections.
Of the 7641 antimicrobial drugs given to treat infections, the most common were parenteral vancomycin (1103, 14.4%; 95% CI, 13.7%-15.2%); ceftriaxone (825, 10.8%; 95% CI, 10.1%-11.5%); piperacillin-tazobactam (788, 10.3%; 95% CI, 9.6%-11.0%); levofloxacin (694, 9.1%; 95% CI, 8.5%-9.7%); and azithromycin (390, 5.1%; 95% CI, 4.6%-5.6%). Piperacillin-tazobactam and vancomycin (parenteral or oral/enteral) ranked among the top 5 antimicrobial drugs for each of the 5 most common infection sites. Fluoroquinolones (levofloxacin or ciprofloxacin) ranked among the top 5 antimicrobial drugs for 4 of the 5 most common infection sites. Fluoroquinolones were not among the top-ranked antimicrobial drugs for treating skin and soft tissue infections (eTable 6 in the Supplement).
Most antimicrobial treatment was for community-onset infections. Of the 4278 patients receiving 7641 antimicrobial drugs to treat infections, 3058 patients (71.5%; 95% CI, 70.1%-72.8%) were receiving 5274 antimicrobial drugs (69.0%; 95% CI, 68.0%-70.1%) for community-onset infections; 1253 patients (29.3%; 95% CI, 27.9%-30.7%) were receiving 2220 antimicrobial drugs (29.1%; 95% CI, 28.0%-30.1%) for health care facility–onset infections, and 99 patients (2.3%; 95% CI, 1.9%-2.8%) were receiving 147 antimicrobial drugs (2.0%; 95% CI, 1.7%-2.3%) for infections with different onset locations, unknown onset location, or both. Treatments for community-onset and health care facility–onset infections were similar: parenteral vancomycin, ceftriaxone, piperacillin-tazobactam, and levofloxacin were among the 5 most commonly administered antimicrobial drugs for both community-onset and health care facility–onset infections (Table 3).
Parenteral vancomycin, ceftriaxone, piperacillin-tazobactam, and levofloxacin were also among the 5 most common drugs overall given to patients in critical care and non–critical care units (Table 4). These 4 drugs were among the 5 most common drugs given for community-onset infections in both critical care and non–critical care locations (excluding neonatal locations), and for health care facility–onset infections in non–critical care locations (excluding neonatal locations; Table 5). Parenteral vancomycin, piperacillin-tazobactam, and levofloxacin, but not ceftriaxone, were among the top 5 drugs given to treat health care facility–onset infections in nonneonatal critical care units. Among antimicrobial drugs given to treat only the most common infection site, community-onset lower respiratory tract infections, these 4 drugs plus azithromycin were the 5 most commonly administered both inside and outside of critical care units (eTable 7 in the Supplement). Parenteral vancomycin and piperacillin-tazobactam made up approximately 15.3% (191 of 1248; 95% CI, 13.4%-17.4%) of all antimicrobial drugs given to treat community-onset lower respiratory tract infections in nonneonatal, noncritical care units compared with 27.6% of drugs given to treat community-onset lower respiratory tract infections in nonneonatal critical care units (101 of 366; 95% CI, 23.2%-32.4%, P < .001, χ2 test).
Quiz Ref IDAntimicrobial drug use was common in this prevalence survey conducted in US acute care hospitals. Approximately 50% of patients were receiving antimicrobial drugs at the time of the survey, and of those, approximately 50% were receiving 2 or more antimicrobial drugs. Similar to older reports,22,23 most antimicrobial use was for infection treatment.Quiz Ref IDAlthough there were 83 different antimicrobial drugs administered to treat infections, just 4—parenteral vancomycin, piperacillin-tazobactam, ceftriaxone, and levofloxacin—made up approximately 45% of all antimicrobial drug treatment. These 4 drugs were not only the most common drugs for treating health care facility–onset infections and for treating patients in critical care units but were also the most common drugs for treating community-onset infections and patients outside of the critical care setting (Table 3 and Table 4). Additionally, approximately 54% of treatment antimicrobial drugs were given to treat lower respiratory tract, urinary tract, or skin and soft tissue infections only. Taken together, focusing stewardship efforts on these 4 drugs and 3 infection syndromes could address more than half of all inpatient antimicrobial drug use.
Parenteral vancomycin, the most common antimicrobial drug overall, was given to approximately 1 in 4 surveyed patients receiving infection treatment. The emergence of methicillin-resistant Staphylococcus aureus (MRSA) as a dominant pathogen in health care and community settings, coupled with increased awareness among health care professionals and the public, likely accounts in part for the high prevalence of vancomycin use. However, recent data suggest that the incidence of health care–associated invasive MRSA infections is declining.24 Data from the health care–associated infection component of our survey18 showed that a relatively low proportion of infections were caused by MRSA or coagulase-negative staphylococci, the most common bacteria for which vancomycin would appropriately be prescribed: 10.7% were due to S aureus, with approximately 55% of tested S aureus isolates reported to be MRSA, and 4.8% were due to coagulase-negative staphylococci. Although rates of community-associated invasive MRSA infections have improved only slightly in recent years,24 it is worth considering whether inpatient vancomycin use can be reduced in selected circumstances without compromising patient safety. Investigators have developed scoring systems and other methods to help identify patients likely to be infected with MRSA.25-27 Implementing such tools and promoting discontinuation of vancomycin therapy when diagnostic results do not indicate a need for use have the potential to reduce unnecessary prescribing.
Another area with potential for improvement is treatment of lower respiratory tract infections. The most common drugs administered for these infections in this survey, levofloxacin, azithromycin, and ceftriaxone, are consistent with current guidelines for management of community-acquired pneumonia in adults.28 However, parenteral vancomycin and piperacillin-tazobactam were also frequently used to treat lower respiratory tract infections. Although these drugs are recommended for community-acquired pneumonia treatment in selected critically ill patients,28 they made up a substantial proportion of the antimicrobial drugs given to patients in noncritical care locations to treat community-onset infections. This suggests that therapy outside critical care units may be an area for further evaluation and assessment of the need for intervention: for example, using patient risk factors and results of timely diagnostic testing to inform appropriate antibiotic selection and tailoring, and taking antibiotic time-outs6 to reassess the need for ongoing treatment. Studies have shown that antimicrobial treatment for hospitalized patients with community-acquired pneumonia can be significantly improved through stewardship interventions.29,30
Quiz Ref IDAlthough our data suggest that potential misuse of antimicrobial drugs for active infections in hospitalized patients may be common, antimicrobial drugs given only for surgical prophylaxis in our survey were largely consistent with current guidelines.31 The national Surgical Care Improvement Project has focused on improving antibiotic prophylaxis selection and discontinuing prophylaxis within 24 hours, and data on both of these performance measures indicate high levels of adherence among US acute care hospitals submitting data to the Joint Commission.32 Despite the reported high levels of compliance with these measures and data showing national progress in preventing surgical site infections related to certain types of procedures,33 there is room for improvement. Surgical site infections remain among the most common types of health care–associated infections,18 and data on their pathogens and antimicrobial resistance34 suggest the potential need to reevaluate surgical antimicrobial prophylaxis recommendations. Other studies have shown that reported adherence with individual Surgical Care Improvement Project antimicrobial prophylaxis measures was not associated with lower surgical site–infection rates35 or successful adherence to all measures,36 suggesting that addressing barriers to correct implementation of surgical site infection prevention measures may also be important.
Antimicrobials for medical prophylaxis were prescribed to a smaller population of surveyed patients than surgical prophylaxis. The most common medical prophylaxis antimicrobial drugs were drugs that are appropriately used to prevent infections in specific circumstances. We did not collect data on patients’ underlying conditions, but information about the hospital locations of patients receiving medical prophylaxis suggests these antimicrobial drugs were generally used in appropriate settings. Quiz Ref IDFor example, penicillin G is one of the recommended antimicrobial drugs for prevention of perinatal group B streptococcal disease,37 and almost 95% of all benzylpenicillin prophylaxis in this survey was administered to patients in obstetrical locations.
This survey has several limitations. Because we assessed antimicrobial use over a 2-day period, longer antibiotic courses may be overrepresented relative to short courses. The survey’s restriction to 183 hospitals in 10 states limits the generalizability of the results, although to our knowledge, it is among the largest inpatient antimicrobial use evaluations in the United States to date. The survey was conducted in 2011, and it is unknown whether the prevalence or patterns of antimicrobial use are similar or different in hospitals today. Because we relied on clinician documentation rather than applying specific, objective criteria to identify infections, we may have overestimated the proportion of antimicrobial drugs given to treat infections. We also collected information on locations of infection onset rather than locations to which infections were attributed, so it is likely that some antimicrobial drugs categorized in the community-onset group were given to treat infections that were health care facility–associated but began in the community (eg, surgical site infection developing while the patient was at home recovering from surgery). This might have minimized differences between antimicrobial drugs for community-onset and health care facility–onset infections. Finally, we did not collect information on treatment duration or on patients’ diagnoses and underlying conditions and therefore were unable to determine whether antimicrobial use was correct in individual patients. We are exploring methods to evaluate the quality of antimicrobial prescribing and plan to incorporate these in future investigations.
To minimize patient harm and preserve effectiveness, it is imperative to critically examine and improve the ways in which antimicrobial drugs are used. Improving antimicrobial use in hospitals benefits individual patients and also contributes to reducing antimicrobial resistance nationally.13 The CDC has described the core elements of effective hospital antimicrobial stewardship programs.38 One of these core elements is “tracking and reporting antibiotic use and outcomes.”38 Prospective surveillance to track antimicrobial consumption is important for evaluating progress in reducing incorrect inpatient antimicrobial use.39 The NHSN recently launched an antimicrobial use reporting option to which health care facilities can electronically report monthly antimicrobial drug consumption data from different inpatient locations to facilitate risk-adjusted benchmarking and guide stewardship efforts.40 Another core element is “implementing policies and interventions to improve antibiotic use.”38 Results from this prevalence survey provide patient-level information that augments data on antimicrobial drug consumption and points to specific areas where interventions to improve antimicrobial use may be needed, such as vancomycin prescribing and respiratory infection treatment, supporting the CDC’s recommendation that every acute care hospital implement an antimicrobial stewardship program.38
In this cross-sectional evaluation of antimicrobial use in US hospitals, use of broad-spectrum antimicrobial drugs such as piperacillin-tazobactam and drugs such as vancomycin for resistant pathogens was common, including for treatment of community-onset infections and among patients outside critical care units. Further work is needed to understand the settings and indications for which reducing antimicrobial use can be most effectively and safely accomplished.
Corresponding Author: Shelley S. Magill, MD, PhD, Division of Healthcare Quality Promotion, Centers for Disease Control and Prevention, 1600 Clifton Rd, MS A-24, Atlanta, GA 30333 (smagill@cdc.gov).
Author Contributions: Dr Magill and Mr Edwards had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.
Study concept and design: Magill, Edwards, Neuhauser, Fridkin.
Acquisition, analysis, or interpretation of data: Beldavs, Dumyati, Janelle, Kainer, Lynfield, Nadle, Ray, Richards, Rodriguez, Thompson.
Drafting of the manuscript: Magill.
Critical revision of the manuscript for important intellectual content: All authors.
Statistical analysis: Magill, Edwards.
Obtained funding: Fridkin.
Administrative, technical, or material support: All authors.
Study supervision: Beldavs, Dumyati, Janelle, Kainer, Lynfield, Nadle, Ray, Richards, Rodriguez, Thompson, Fridkin.
Conflict of Interest Disclosures: All authors have completed and submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest. Dr Kainer reported that she is a board member, receives lecture and consulting fees from the Infectious Disease Consulting Corporation; and owns stock in the Infectious Disease Consulting Corporation. Dr Lynfield reported that she receives travel support from Parexel. No other disclosures were reported.
Funding/Support: The survey was supported through a cooperative agreement with the Emerging Infections Program. Funds to conduct the survey came from the CDC’s Division of Healthcare Quality Promotion, Division of Preparedness and Emerging Infections, and Office of Antimicrobial Resistance.
Role of Funders/Sponsors: The funding source was the US federal government. Federal government employees led or participated in all aspects of the survey, including design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication.
Disclaimer: The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the CDC/the Agency for Toxic Substances and Disease Registry, or the Department of Veterans Affairs.
Previous Publication: Data included in this manuscript have been previously presented in abstract and oral presentation form at Infectious Disease Week, October 17-21, 2012, San Diego, California. Pediatric data were presented in abstract and poster presentation Infectious Diseases Week, October 2-6, 2013, San Francisco, California. The results of the health care–associated infection component of the survey have been published.18 The antimicrobial use survey was described.39 Some of the data presented herein were included in the CDC report entitled “Vital Signs: Improving Antibiotic Use Among Hospitalized Patients.”6
Survey Team Members: Other members of the prevalence survey team follows: Wendy Bamberg, MD, and Julie Mullica, MPH (Colorado Department of Public Health and Environment, Denver); Richard Melchreit, MD, and Meghan Maloney, MPH (Connecticut Department of Public Health, Hartford); Lewis Perry, RN, MPH, and Nancy White, RN, BSN, CIC (Georgia Emerging Infections Program, Decatur); Lucy Wilson, MD, ScM (Maryland Department of Health and Mental Hygiene, Baltimore); Jane Harper, BSN, MS, CIC, Jean Rainbow, RN, MPH, and Linn Warnke, RN, MPH (Minnesota Department of Health, St Paul); Joan Baumbach, MD, MPH, MS (New Mexico Department of Health, Santa Fe); Cathleen Concannon, MPH, and Gail Quinlan, RN, MS, CIC (New York–Rochester Emerging Infections Program/University of Rochester Medical Center, Rochester); Margaret Cunningham, MPH, Valerie Ocampo, RN, MIPH, and Jennifer Tujo, RN, MSN, MPA, CIC (Oregon Public Health Division, Oregon Health Authority, Portland); and Matthew Crist, MD, MPH (Tennessee Department of Health, Nashville).
Additional Contributions: We thank the staff and patients in each hospital that participated in phases 2 and 3 of the survey. We also thank our colleagues in the EIP sites and at the CDC who contributed to this effort and the following individuals, who received compensation for their work as CDC or EIP site employees or contractors are acknowledged for their contributions to survey coordination, data collection, and data entry: Deborah Godine, RN, CIC, and Celeste Prothro, RN, MPH (California Emerging Infections Program, Oakland); Laura McAllister-Hollod, MPH (Centers for Disease Control and Prevention, Atlanta, Georgia); Cindy Gross, MT (ASCP), SM, CIC, and Dee Higgins, RN, BSN (Georgia Emerging Infections Program, Decatur); Patricia Lawson, RN, MS, MPH, CIC, LaToya Forrester, MPH, and Malorie Givan, MPH (Maryland Department of Health and Mental Hygiene, Baltimore); Emily Hallberg, MPH (Minnesota Department of Health, St Paul); Monear Makvandi, MPH (New Mexico Department of Health, Santa Fe); Barbara Mooney, BSMB, BSMT (ASCP), CIC (Infection Control Consultants of New Mexico, consultant through HealthInsight New Mexico, Albuquerque); Jennifer Salazar, LPN (HealthInsight New Mexico, Albuquerque); Rebecca Tsay, MPH, MLS, and Anita Gellert, RN (New York–Rochester Emerging Infections Program/University of Rochester Medical Center, Rochester, NY); and Ellen Borchers, MSN, RN, Daniel Muleta, MD, MPH, Loretta Moore-Moravian, RN/BSN, COHN-S/CM, and Dana Jackson, RN, BSN (Tennessee Department of Health, Nashville).
Correction: This article was corrected on October 7, 2014, to include a link to eTable 7 in the Supplement.
1.Gaieski
DF, Mikkelsen
ME, Band
RA,
et al. Impact of time to antibiotics on survival in patients with severe sepsis or septic shock in whom early goal-directed therapy was initiated in the emergency department.
Crit Care Med. 2010;38(4):1045-1053.
PubMedGoogle ScholarCrossref 2.Iregui
M, Ward
S, Sherman
G, Fraser
VJ, Kollef
MH. Clinical importance of delays in the initiation of appropriate antibiotic treatment for ventilator-associated pneumonia.
Chest. 2002;122(1):262-268.
PubMedGoogle ScholarCrossref 3.Garey
KW, Rege
M, Pai
MP,
et al. Time to initiation of fluconazole therapy impacts mortality in patients with candidemia: a multi-institutional study.
Clin Infect Dis. 2006;43(1):25-31.
PubMedGoogle ScholarCrossref 4.Castle
M, Wilfert
CM, Cate
TR, Osterhout
S. Antibiotic use at Duke University Medical Center.
JAMA. 1977;237(26):2819-2822.
PubMedGoogle ScholarCrossref 5.Hecker
MT, Aron
DC, Patel
NP, Lehmann
MK, Donskey
CJ. Unnecessary use of antimicrobials in hospitalized patients: current patterns of misuse with an emphasis on the antianaerobic spectrum of activity.
Arch Intern Med. 2003;163(8):972-978.
PubMedGoogle ScholarCrossref 6.Fridkin
S, Baggs
J, Fagan
R,
et al; Centers for Disease Control and Prevention (CDC). Vital signs: improving antibiotic use among hospitalized patients.
MMWR Morb Mortal Wkly Rep. 2014;63(9):194-200.
PubMedGoogle Scholar 7.Swaminathan
M, Sharma
S, Poliansky Blash
S,
et al. Prevalence and risk factors for acquisition of carbapenem-resistant Enterobacteriaceae in the setting of endemicity.
Infect Control Hosp Epidemiol. 2013;34(8):809-817.
PubMedGoogle ScholarCrossref 8.Marchaim
D, Chopra
T, Bhargava
A,
et al. Recent exposure to antimicrobials and carbapenem-resistant Enterobacteriaceae: the role of antimicrobial stewardship.
Infect Control Hosp Epidemiol. 2012;33(8):817-830.
PubMedGoogle ScholarCrossref 9.Srigley
JA, Brooks
A, Sung
M, Yamamura
D, Haider
S, Mertz
D. Inappropriate use of antibiotics and
Clostridium difficile infection.
Am J Infect Control. 2013;41(11):1116-1118.
PubMedGoogle ScholarCrossref 10.Polgreen
PM, Chen
YY, Cavanaugh
JE,
et al. An outbreak of severe
Clostridium difficile-associated disease possibly related to inappropriate antimicrobial therapy for community-acquired pneumonia.
Infect Control Hosp Epidemiol. 2007;28(2):212-214.
PubMedGoogle ScholarCrossref 11.Bates
DW, Cullen
DJ, Laird
N,
et al; ADE Prevention Study Group. Incidence of adverse drug events and potential adverse drug events: implications for prevention.
JAMA. 1995;274(1):29-34.
PubMedGoogle ScholarCrossref 15.Pakyz
AL, MacDougall
C, Oinonen
M, Polk
RE. Trends in antibacterial use in US academic health centers: 2002 to 2006.
Arch Intern Med. 2008;168(20):2254-2260.
PubMedGoogle ScholarCrossref 16.Gerber
JS, Newland
JG, Coffin
SE,
et al. Variability in antibiotic use at children’s hospitals.
Pediatrics. 2010;126(6):1067-1073.
PubMedGoogle ScholarCrossref 17.Huttner
B, Jones
M, Huttner
A, Rubin
M, Samore
MH. Antibiotic prescription practices for pneumonia, skin and soft tissue infections and urinary tract infections throughout the US Veterans Affairs system.
J Antimicrob Chemother. 2013;68(10):2393-2399.
PubMedGoogle Scholar 18.Magill
SS, Edwards
JR, Bamberg
W,
et al; Emerging Infections Program Healthcare-Associated Infections and Antimicrobial Use Prevalence Survey Team. Multistate point-prevalence survey of health care-associated infections.
N Engl J Med. 2014;370(13):1198-1208.
PubMedGoogle ScholarCrossref 19.Dean
AG, Sullivan
KM, Soe
MM. OpenEpi: Open Source Epidemiologic Statistics for Public Health, version 3.01.
www.OpenEpi.com. Accessed January 29, 2014.
22.Shapiro
M, Townsend
TR, Rosner
B, Kass
EH. Use of antimicrobial drugs in general hospitals, II: analysis of patterns of use.
J Infect Dis. 1979;139(6):698-706.
PubMedGoogle ScholarCrossref 24.Dantes
R, Mu
Y, Belflower
R,
et al; Emerging Infections Program–Active Bacterial Core Surveillance MRSA Surveillance Investigators. National burden of invasive methicillin-resistant
Staphylococcus aureus infections, United States, 2011.
JAMA Intern Med. 2013;173(21):1970-1978.
PubMedGoogle Scholar 25.Zilberberg
MD, Chaudhari
P, Nathanson
BH,
et al. Development and validation of a bedside risk score for MRSA among patients hospitalized with complicated skin and skin structure infections.
BMC Infect Dis. 2012;12:154.
PubMedGoogle ScholarCrossref 26.Shorr
AF, Myers
DE, Huang
DB, Nathanson
BH, Emons
MF, Kollef
MH. A risk score for identifying methicillin-resistant
Staphylococcus aureus in patients presenting to the hospital with pneumonia.
BMC Infect Dis. 2013;13(1):268.
PubMedGoogle ScholarCrossref 27.Jinno
S, Chang
S, Donskey
CJ. A negative nares screen in combination with absence of clinical risk factors can be used to identify patients with very low likelihood of methicillin-resistant
Staphylococcus aureus infection in a Veterans Affairs hospital.
Am J Infect Control. 2012;40(9):782-786.
PubMedGoogle ScholarCrossref 28.Mandell
LA, Wunderink
RG, Anzueto
A,
et al. Infectious Diseases Society of America/American Thoracic Society consensus guidelines on the management of community-acquired pneumonia in adults.
Clin Infect Dis. 2007;44(suppl 2):S27-S72.
PubMedGoogle ScholarCrossref 29.Avdic
E, Cushinotto
LA, Hughes
AH,
et al. Impact of an antimicrobial stewardship intervention on shortening the duration of therapy for community-acquired pneumonia.
Clin Infect Dis. 2012;54(11):1581-1587.
PubMedGoogle ScholarCrossref 30.Schouten
JA, Hulscher
ME, Trap-Liefers
J,
et al. Tailored interventions to improve antibiotic use for lower respiratory tract infections in hospitals: a cluster-randomized, controlled trial.
Clin Infect Dis. 2007;44(7):931-941.
PubMedGoogle ScholarCrossref 31.Bratzler
DW, Dellinger
EP, Olsen
KM,
et al; American Society of Health-System Pharmacists; Infectious Disease Society of America; Surgical Infection Society; Society for Healthcare Epidemiology of America. Clinical practice guidelines for antimicrobial prophylaxis in surgery.
Am J Health Syst Pharm. 2013;70(3):195-283.
PubMedGoogle ScholarCrossref 34.Berríos-Torres
SI, Yi
SH, Bratzler
DW,
et al. Activity of commonly used antimicrobial prophylaxis regimens against pathogens causing coronary artery bypass graft and arthroplasty surgical site infections in the United States, 2006-2009.
Infect Control Hosp Epidemiol. 2014;35(3):231-239.
PubMedGoogle ScholarCrossref 35.Stulberg
JJ, Delaney
CP, Neuhauser
DV, Aron
DC, Fu
P, Koroukian
SM. Adherence to surgical care improvement project measures and the association with postoperative infections.
JAMA. 2010;303(24):2479-2485.
PubMedGoogle ScholarCrossref 36.Hawkins
RB, Levy
SM, Senter
CE,
et al. Beyond surgical care improvement program compliance: antibiotic prophylaxis implementation gaps.
Am J Surg. 2013;206(4):451-456.
PubMedGoogle ScholarCrossref 39.Fridkin
SK, Srinivasan
A. Implementing a strategy for monitoring inpatient antimicrobial use among hospitals in the United States.
Clin Infect Dis. 2014;58(3):401-406.
PubMedGoogle ScholarCrossref