Challenges in Preparation of Cumulative Antibiogram Reports for

Community Hospitals
Rebekah W. Moehring,a,b,c Kevin C. Hazen,d Myra R. Hawkins,b Richard H. Drew,a,b,e Daniel J. Sexton,a,b Deverick J. Andersona,b
Duke University Medical Center, Department of Medicine, Division of Infectious Diseases, Durham, North Carolina, USAa; Duke Infection Control Outreach Network and
Duke Antimicrobial Stewardship Outreach Network, Durham, North Carolina, USAb; Durham Veterans Affairs Medical Center, Department of Medicine, Division of
Infectious Diseases, Durham, North Carolina, USAc; Duke University Medical Center, Department of Pathology, Durham, North Carolina, USAd; Campbell University College
of Pharmacy and Health Sciences, Buies Creek, North Carolina, USAe

Knowledge of local antimicrobial resistance is critical for management of infectious diseases. Community hospitals compliance
with Clinical and Laboratory Standards Institute (CLSI) guidance for creation of cumulative antibiograms is uncertain. This
descriptive cohort study of antibiogram reporting practices included community hospitals enrolled in the Duke Infection Con-

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trol Outreach Network. Cumulative antibiograms from 2012 were reviewed for criteria on reporting practices and compliance
with CLSI guidelines. Microbiology personnel were sent a voluntary, electronic survey on antibiogram preparation practices.
Data were compiled using descriptive statistics. Thirty-two of 37 (86%) hospitals provided antibiograms; 26 of 37 (70%) also
provided survey responses. Twelve (38%) antibiograms specified methods used for compiling data and exclusion of duplicates.
Eight (25%) reported only species with >30 isolates. Of the 24 that did not follow the 30-isolate rule, 3 (13%) included footnotes
to indicate impaired statistical validity. Twenty (63%) reported at least 1 pathogen-drug combination not recommended for pri-
mary or supplemental testing per CLSI. Thirteen (41%) separately reported methicillin-resistant and -susceptible Staphylococcus
aureus. Complete compliance with CLSI guidelines was observed in only 3 (9%) antibiograms. Survey respondents self-assess-
ment of full or partial compliance with CLSI guidelines was 50% and 15%, respectively; 33% reported uncertainty with CLSI
guidelines. Full adherence to CLSI guidelines for hospital antibiograms was uncommon. Uncertainty about CLSI guidelines was
common. Alternate strategies, such as regional antibiograms using pooled data and educational outreach efforts, are needed to
provide reliable and appropriate susceptibility estimates for community hospitals.

F acility-specific cumulative antibiograms serve several impor-

tant purposes in the care of patients with infectious diseases.
For clinicians, knowledge of local drug resistance rates improves
with guidelines and the impact of cumulative antibiograms on
program- or facility-level decision-making.

the selection of empirical antibiotics prior to return of culture and
susceptibility results. In addition, cumulative susceptibility data
are used to track changes in resistance over time, perform surveil-
lance for emergence of drug-resistant organisms, and identify ar-
eas for intervention by hospital infection prevention and antimi-
crobial stewardship programs (1). For example, the Centers for
Disease Control and Prevention includes two functions of the cu-
mulative antibiogram as core elements of hospital antimicrobial
stewardship programs: (i) tracking antimicrobial resistance and
(ii) regular reporting of information on antibiotic resistance to
relevant hospital staff (2). Cumulative antibiogram preparation
and distribution are considered an essential function of the clini-
cal microbiology laboratory (3). Antibiogram data can also im-
prove hospital antibiotic formulary decisions and local protocols
such as surgical prophylaxis or empirical treatment guidelines.
The Clinical and Laboratory Standards Institute (CLSI) first
provided guidelines for preparation of cumulative antibiograms
in 2002 and revised them in 2009 and 2014 (3, 4). However, pub-
lished data on adherence to these guidelines in community hospi-
tals are not available. Further, adherence to guidelines may be
particularly important in small, community hospitals where local
access to expertise in infectious diseases and microbiology is often
limited. The aims of this study were to (i) describe reporting prac-
tices of cumulative antimicrobial susceptibility data in a cohort of
community hospitals in the southeastern United States, (ii) deter-
mine adherence to CLSI guideline recommendations, and (iii)
describe perceptions from antibiogram preparers on compliance
MATERIALS AND METHODS
We performed a descriptive analysis of antibiogram reporting practices in
community hospitals enrolled in the Duke Infection Control Outreach
Network (DICON). DICON is a collaborative network of community
hospitals in the southeastern United States that share surveillance data on
health care-associated infection, educational materials, and consultative
services for their infection prevention programs (5). We requested cumu-
lative antibiograms that included data from calendar year 2012 from the
37 acute care hospitals participating in DICON starting in January 2013.
Of those facilities that voluntarily provided antibiograms, microbiology
laboratory directors were sent a voluntary, electronic survey on antibi-
ogram preparation knowledge and practices. The directors were asked to
delegate the survey response to the individual responsible for preparing
the facility cumulative antibiogram. Surveys were completed in
April-May 2014. Surveys were designed and distributed using Qualtrics
(Provo, UT).
Received 2 May 2015 Returned for modification 29 May 2015
Accepted 10 July 2015
Accepted manuscript posted online 15 July 2015
Citation Moehring RW, Hazen KC, Hawkins MR, Drew RH, Sexton DJ, Anderson DJ.
2015. Challenges in preparation of cumulative antibiogram reports for
community hospitals. J Clin Microbiol 53:29772982. doi:10.1128/JCM.01077-15.
Editor: B. A. Forbes
Address correspondence to Rebekah W. Moehring, rebekah.moehring@duke.edu.
Copyright 2015, American Society for Microbiology. All Rights Reserved.
doi:10.1128/JCM.01077-15

September 2015 Volume 53 Number 9 Journal of Clinical Microbiology jcm.asm.org 2977

Moehring et al.

TABLE 1 Response rates and characteristics of participating hospitals, TABLE 2 Adherence to CLSI guidelines for creation of facility
Duke Infection Control Outreach Network, 2013 cumulative antibiogramc
Hospital characteristic n % Criterion n Total no. %
DICON acute care hospitals invited to participate 37 Statement that duplicate isolates were 12 32 38
Provided 2012 antibiogram 32 86 excluded from report
Provided survey response 26 70 Reported at least 1 yr of data 30 32 94
Respondent hospital characteristicsa Reported data only when isolate n was 30 12 32 52
Location or included footnote to indicate
North Carolina 22 69 impaired interpretation due to small no.
Virginia 4 13 Separately reported MSSA and MRSAd 13 32 41
South Carolina 3 9 Provided meningitis vs. nonmeningitis 12 23 52
Georgia 2 6 susceptibilities for S. pneumoniaea
Florida 1 3 Reported only pathogen-drug test 12 32 38
Ownership combinations that are recommended for
Not for profit 23 72 routine or supplemental reportingb
Government, nonfederal 6 19 Full compliance with CLSI guidance (all six 3 32 9

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For profit 3 9
a a
Respondent hospitals contained a median of 211 beds (IQR, 129 to 279).
Definitions for adherence to CLSI guidelines were determined by six
criteria defined in a binary fashion and based on recommendations from
CLSI document M39-A3 (2009) (1, 3). Adherence to each criterion was
determined upon visual inspection of the antibiogram reports; thus, some
recommendations from CLSI could not be objectively assessed (e.g., re-
porting only final, verified results). We considered antibiograms that in-
cluded a statement indicating removal of duplicate isolates from the same
patient to be adherent to the first isolate per patient recommendation.
We considered the report to be adherent to the recommendation for time
period if it included at least 1 year of data. Reports that did not indicate
duplicate removal or time period were considered not adherent. Antibi-
ograms were considered adherent to the 30-isolate recommendation if
at least one of two criteria were met: (i) report included only species with
at least 30 isolates tested or (ii) report provided a statement to explain
impaired interpretability when the number of isolates per species was less
than 30. Antibiograms that included only pathogen-drug test combina-
tions recommended for routine or supplemental reporting in Table 1 in
CLSI M100-S23 (2013) were considered compliant with the routine test-
ing recommendation (6). Reports that separated methicillin-sensitive
from methicillin-resistant Staphylococcus aureus were deemed adherent.
Antibiograms that reported susceptibilities for Streptococcus pneumoniae
were deemed adherent if percent susceptible was reported at both men-
ingitis and nonmeningitis breakpoints. We defined full adherence as
fulfilling all six recommendations. Antibiograms that did not report S.
pneumoniae due to the 30-isolate rule were deemed to be in full adherence
if compliant with the other 5 recommendations.
Survey responses and adherence to CLSI guidance were analyzed using
descriptive statistics. All analyses were completed using Microsoft Excel
(2010). The study was deemed exempt research by the Duke University
Health System Institutional Review Board.
RESULTS
Cumulative antibiogram report analysis. Thirty-two of 37
(86%) acute care hospitals provided antibiograms (Table 1). The
formats of the 32 antibiograms varied considerably. The number
of species with percent susceptibility reported included a median
11 (interquartile range [IQR], 7.75 to 13) Gram-negative species
and 5 (IQR, 5 to 6) Gram-positive species. Only a single facility
reported Candida species susceptibilities. The median number of
isolates per facility for common species was as follows (IQRs in
parentheses): Escherichia coli, 914 (768 to 1,429); Pseudomonas
aeruginosa, 129 (88 to 184); S. aureus, 341 (206 to 615). Four
(13%) antibiograms provided unit-specific (e.g., intensive care
criteria above were met)
Reports that did not report any S. pneumoniae susceptibilities due to small isolate
numbers were deemed compliant with this element in assessment of full adherence to
CLSI guidelines.
b
Antibiograms that included only pathogen-drug test combinations recommended for
routine or supplemental reporting in Table 1 in CLSI M100-S23 (2013) were
considered compliant (6).
c
See reference 3.
d
MSSA, methicillin-susceptible Staphylococcus aureus; MRSA, methicillin-resistant
Staphylococcus aureus.
unit) susceptibility estimates. Three (9%) antibiograms separately
reported inpatient and outpatient data, 7 (22%) reported com-
bined inpatient and outpatient data, 1 included inpatient data
only, and 1 included data from inpatients plus the emergency
department. The majority (n 20, 63%) of antibiograms failed to
specify whether the reported susceptibility data included inpatient
and/or outpatient specimens. Eight (25%) reports separately pre-
sented an antibiogram compiled from urine specimens only. Ex-
tended-spectrum beta-lactamase-producing pathogens were sep-
arately reported in 15 (47%) antibiograms.
Adherence to CLSI guidance was low. Only 3 (9%) of 32 anti-
biograms achieved full adherence to the six CLSI recommenda-
tions (Table 2). Twelve (38%) antibiograms specified methods
used to compile data and exclude duplicates. Eight (25%) antibi-
ograms reported only species with 30 isolates; 3 (13%) of the 24
that did not follow the 30-isolate rule included a footnote to indi-
cate impaired ability to interpret susceptibility estimates. Twenty
(63%) antibiograms reported at least 1 pathogen-drug combina-
tion not recommended for primary or supplemental testing by the
CLSI (Table 3). The most frequently reported pathogen-drug test
combination not recommended for routine reporting was Entero-
coccus species and tigecycline (10 [31%] antibiograms). Clinically
inappropriate pathogen-drug combinations that represent seri-
ous errors were reported in 13 (41%) antibiograms (Table 3) (e.g.,
aztreonam and S. aureus). P. aeruginosa had the most commonly
reported pathogen-drug combination serious errors (e.g., ceftri-
axone). Thirteen (41%) antibiograms separately reported methi-
cillin-resistant and methicillin-susceptible S. aureus. Approxi-
mately half (12 [52%]) of the 23 facilities that reported
susceptibilities for S. pneumoniae correctly included both menin-
gitis and nonmeningitis breakpoints.
Survey results. Twenty-six (70%) of 32 facilities that submit-
ted antibiogram reports provided voluntary survey responses. The
majority of survey respondents were microbiology laboratory staff

2978 jcm.asm.org Journal of Clinical Microbiology September 2015 Volume 53 Number 9

 Challenges in Preparing Antibiograms

TABLE 3 Number of antibiograms reporting pathogen-drug test combinations that are not recommended by CLSI for routine or supplemental
reporting
No. reporting antimicrobial susceptibility testa

Amp-sulbactam

Erythromycin
Moxifloxacin

Clindamycin
Meropenem

Tetracycline
Ceftazidime
Cefuroxime

Ceftriaxone
Cefotaxime

Tigecycline

Quin-dalfo
Aztreonam

TMP/SMX
Imipenem

Rifampin
Cefoxitin
Pip-Tazo
Pathogen
Enterococcus spp. 1 1 10 5 3 1 2
S. aureus 1 1 1 1 3 8 2
S. pneumoniae 1
Enterobacteriaceae 9
Acinetobacter spp. 1 6 1
P. aeruginosa 2 1 5 3 8 4 2 2 1
Stenotrophomonas 1

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a
Numbers indicate the number of facility antibiograms (of 32 participating facilities) reporting this pathogen-drug test combination as percent susceptible on their cumulative
antibiogram. Overall, 20 (64%) of 32 antibiograms contained at least one pathogen-drug combination not recommended for routine or supplemental reporting. Gray shading
indicates combinations considered to be serious errors. Thirteen (41%) of 32 antibiograms contained at least one serious error. Abbreviations: Amp-sulbactam,
ampicillin-sulbactam; Pip-Tazo, piperacillin-tazobactam; TMP/SMX, trimethoprim-sulfamethoxazole; Quin-dalfo, quinupristin-dalfopristin.

members; approximately half were senior technologists or team used self-reported, voluntary surveys to assess compliance with
leaders (Table 4). Vitek 2 and MicroScan were the most com- specific CLSI recommendations (7, 8, 10). A survey of laboratory
monly utilized automated antimicrobial susceptibility testing directors at 494 U.S. acute care hospitals in 2004 reported 60% of
platforms. Individuals most frequently involved in antibiogram responders in compliance with annually compiling, updating, and
preparation included microbiology technologists (19 [90%]) and distributing a facility antibiogram (8). The self-reported compli-
clinical pharmacists (10 [48%]); infectious disease-trained phar- ance rates in a 2009 survey of pharmacy directors in the University
macists (5 [24%]) and infectious disease physicians (2 [10%]) Health Consortium were favorable (10). Respondents reported
were less commonly involved. Approximately a third (6 [30%]) of publishing at least annually (98%), eliminating duplicates (89%),
respondents indicated that no committee formally or routinely not including surveillance cultures (83%), and including at least
reviewed the antibiogram report at their facility. The majority (16 30 isolates for each organism (64%) (10). Studies that assessed
[84%]) of respondents indicated that they were unaware or un- compliance by direct inspection of antibiograms showed lower
certain of any change in facility-level decisions that had occurred adherence than those that used self-reported compliance (9, 11).
as a result of antibiogram results. Survey respondents self-assess- Direct inspection of antibiograms in our study revealed not
ment of full or partial compliance with CLSI guidelines was 50% only low guideline compliance but also that some facility antibi-
and 15%, respectively. Over a third (7 [35%]) of respondents re- ograms contained serious errors of clinically inappropriate patho-
ported uncertainty or unfamiliarity with CLSI guidance. gen-drug combinations. Similarly, Zapantis et al. examined 209
antibiograms and found that a number of reports included inap-
DISCUSSION propriate pathogen-drug combinations (e.g., Klebsiella pneu-
This study highlights limited adherence to CLSI guidelines for moniae and ampicillin) or unlikely percent susceptibility results
cumulative antibiograms, unfamiliarity with these guidelines, and (11). A longitudinal study evaluated the effect of statewide educa-
the perceived limited effect that antibiogram reports have on fa- tional outreach efforts by reviewing cumulative antibiogram re-
cility-level decision making in our community hospital cohort. ports from 86 hospitals in Michigan (9). Serious errors in antibi-
The incidence of antibiotic-resistant pathogens varies geographi- ograms were defined as improbable or impossible percent
cally. Therefore, clinicians must understand rates of resistance in susceptibility results or the reporting of misleading or inappropri-
local populations in order to best manage empirical treatment of ate pathogen-drug combinations. The percentage of antibiograms
infectious diseases. The facility antibiogram is the primary tool with serious errors decreased over time (59% to 19%). Serious
that provides this important information. However, the facility errors in antibiograms could result in medical errors if antibi-
antibiogram may prove to be an unstandardized, ignored, and at ograms are used to make clinical decisions. These serious errors
times clinically inappropriate representation of antibiotic resis- suggest that antibiograms were not thoroughly reviewed for accu-
tance. racy and clinical relevance. Further, these errors may potentially
Our study demonstrated that fewer than 1 in 10 hospitals had represent a limited knowledge of clinical microbiology among an-
full compliance with CLSI guidelines for cumulative antibi- tibiogram preparers and reviewers.
ograms. Antibiogram reports were heterogeneous in both format The current study is unique in that it combines direct inspec-
and approach. Our study also revealed problems with a lack of tion of antibiogram reports with survey responses, which provides
documentation of the method of antibiogram preparation (e.g., insight into perceptions from antibiogram preparers in addition
specifying time period, outpatient versus inpatient, and duplicate to evaluations of guideline compliance. A third of survey respon-
removal). Prior published surveys of antibiogram preparation dents reported uncertainty or unfamiliarity with CLSI guidance.
practices have also shown variability in report format and limited The majority of respondents indicated that they were unaware of
uptake of CLSI guidelines (79). Several prior investigators have any change in facility policy or decision making that had occurred

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Moehring et al.

TABLE 4 Survey responses regarding practices for preparation of cumulative antibiogram

Response No. of responses (total, 26) % of respondentsa
Survey respondent role
Senior technologist or team leader 12 48
Medical laboratory or microbiology technologist 4 16
Director or manager of microbiology 4 16
Microbiologist 3 12
Pharmacist 1 4
Infection preventionist 1 4
No response 1

Site of microbiology lab

Onsite 24 96
Referral lab 1 4
No response 1

Automated antimicrobial susceptibility test system

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Vitek 2 13 52
MicroScan 10 40
Vitek 2 8
No response 1

Antimicrobial stewardship program

Formal program present 16 76
No formal program 5 24
No response 5

Individual involved in antibiogram prepna

Microbiology technologist 19 90
Clinical pharmacist 10 48
Infectious disease pharmacist 5 24
Pharmacy director 3 14
Infectious disease physician 2 10
No response 5

Hospital group or committee that formally reviews the antibiograma

Pharmacy and therapeutics 8 40
Infection prevention committee 5 25
Antimicrobial stewardship 5 25
Not formally reviewed 6 30
Other group in the pharmacy department 3 15
No response 6

Method of antibiogram disseminationa

Pocket card 10 48
Facility intranet 9 43
Hard copies in patient care areas 4 19
Integrated into facility handbooks 1 5
Uncertain 2 10
No response 5

Which of following changes occurred as result of antibiogram reviewa

Revision of order sets and clinical guidelines for infectious diseases 1 5
Preoperative prophylaxis choices adjusted 0 0
Formulary additions, deletions, or revisions 3 16
Uncertain of any resulting change 16 84
Other 1 5
No response 7

Perceived compliance with CLSI M39 (2009)

Fully compliant 10 50
Partially compliant 3 15
Not compliant 0 0
Uncertain or unfamiliar with guidance 7 35
No response 6
a
Select all that apply questions allowed multiple responses possible from the same respondent. Thus, totals and percent may exceed 26 and 100%, respectively.

2980 jcm.asm.org Journal of Clinical Microbiology September 2015 Volume 53 Number 9


as a result of antibiogram data. A large proportion reported that
no formal review of antibiogram data occurred. These responses
plus the presence of serious clinical errors in study antibiograms
are further evidence of the absence of formal, multidisciplinary
review.
This study is focused on antibiogram preparation practices in
smaller, community hospitals in the southeastern United States.
We have observed that such hospitals face specific barriers to ef-
fective antibiogram preparation, such as limited microbiology or
informatics personnel dedicated to the task, lack of resources to
purchase proprietary CLSI documents, lack of support from cli-
nicians and/or multidisciplinary teams, and small numbers of iso-
lates that impair the interpretability of cumulative data. Several
hospitals in our cohort do not have infectious disease specialists
on staff. Specific efforts to address problems with production of
high-quality antibiograms and to promote antibiogram use for
facility decision making are needed in order to provide reliable,
local susceptibility estimates and to track the emergence of drug
resistance in community hospitals. Educational outreach on the
elements of CLSI guidance and provision of CLSI documents by
state health departments may have some benefit, as demonstrated
by investigators in Michigan (9). Also, regular review and feed-
back from clinical providers are essential for both the accuracy
and the usability of the antibiogram document, as well as for dis-
tribution of the information for clinical use. To specifically ad-
dress the problems of small isolate numbers, pooled data from
multiple facilities or longer cumulative data collection periods
(e.g., including more than 1 year of data) may provide more reli-
able estimates of drug resistance for small facilities. In our study,
there was variation in what patient populations were included in
different institutions antibiograms (e.g., inpatient versus outpa-
tient), which made pooling of antibiogram data in order to com-
pare regional trends impossible to accomplish.
We believe that CLSI should expand and highlight specific
guidance for small facilities in their recommendations for cumu-
lative antibiogram preparation. Specifically, guidelines should ad-
dress the commonly encountered problem of small isolate num-
bers and encourage standardization in order to assist public health
authorities in obtaining comparable data between institutions. In
addition, there is substantial opportunity to improve reporting
through electronic medical record vendors, which could stream-
line the process of data collection and analysis, use methods that
are both CLSI compliant and reliable, and produce standardized
data that can be pooled between facilities. We recently established
the Duke Antimicrobial Stewardship Outreach Network to sup-
port the development of antimicrobial stewardship programs in
community hospitals in our region (http://dason.medicine.duke
.edu/home). We have initiated review and feedback of annual an-
tibiograms as part of our consultation services as a result of this
study.
This study has limitations. While it is limited to community
hospitals within DICON, review of the literature suggests that
problems identified in our study are also present in other geo-
graphic areas. The survey portion of our study is subject to recall
and response bias due to its voluntary design and lack of indepen-
dent verification of responses. Preparation of the antibiogram re-
port and the survey response date were separated by approxi-
mately 1 year, which could have further contributed to recall bias.
Data for cumulative antibiograms may have been directly ob-
tained from automated testing instruments instead of laboratory
September 2015 Volume 53 Number 9 Journal of Clinical Microbiology
Challenges in Preparing Antibiograms
information systems. Therefore, some of the data used in antibi-
ograms may have included unverified results. We could not inves-
tigate this specifically, but it may contribute significantly to some
of the errors in reporting of pathogen-drug combinations and
problems with compliance with CLSI guidance. We also did not
determine the brand of electronic laboratory information system
used at each hospital, which may impact the ability to adhere to
CLSI guidance. We considered lack of documentation regarding
removal of duplicates to indicate nonadherence. If this recom-
mendation was followed without documentation on the report,
adherence to this criterion may have been misclassified. Despite
these limitations, we believe that this study highlights problems
that need attention from both clinicians and public health advo-
cates, especially as bacterial resistance to existing antibiotics con-
tinues to worsen (12, 13).
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In conclusion, full compliance with CLSI guidance for hospital
antibiograms was uncommon in our cohort of community hos-
pitals. A survey of antibiogram preparers revealed uncertainty
about CLSI guidance and little perceived effect from use of facility
antibiogram reports. Alternate strategies, such as using pooled
regional data and educational outreach, are greatly needed in or-
der to improve the quality of antibiograms, emphasize the ur-
gency of emerging antibiotic resistance in local settings, and pro-
vide reliable and appropriate susceptibility data for clinicians
practicing in community hospitals.
ACKNOWLEDGMENTS
We thank all participating DICON hospitals for their continued contri-
butions to research efforts.
This study was funded by a grant from The Duke Endowment to D.J.S.
and R.W.M. D.J.A. was supported by NIH K23 AI095357. R.W.M. was
supported by AHRQ K08 HS023866-01.
Rebekah W. Moehring has no direct conflicts. She has received royal-
ties from UpToDate, Inc. Kevin C. Hazen has no direct conflicts. He has
received research support from bioMrieux, Inc. Myra R. Hawkins has no
conflicts. Richard H. Drew has no direct conflicts. He has received royal-
ties from UpToDate, Inc.; development royalties from CustomID; and
speaker honoraria from both Vemco Medical Education and the Ameri-
can Society for Microbiology. Daniel J. Sexton has no direct conflicts. He
has received research support from CDC and royalties from UpToDate,
Inc. Deverick J. Anderson has no direct conflicts. He has received royalties
from UpToDate, Inc.
REFERENCES
1. Hindler JF, Stelling J. 2007. Analysis and presentation of cumulative
antibiograms: a new consensus guideline from the Clinical and Laboratory
Standards Institute. Clin Infect Dis 44:867 873. http://dx.doi.org/10.1086
/511864.
2. Standiford HC, Chan S, Tripoli M, Weekes E, Forrest GN. 2012.
Antimicrobial stewardship at a large tertiary care academic medical
center: cost analysis before, during, and after a 7-year program. Infect
Control Hosp Epidemiol 33:338 345. http://dx.doi.org/10.1086
/664909.
3. Clinical and Laboratory Standards Institute. 2009. Analysis and presen-
tation of cumulative antimicrobial susceptibility test data; approved
guideline. CLSI document M39-A3. Clinical and Laboratory Standards
Institute, Wayne, PA.
4. National Committee for Clinical Laboratory Standards. 2002. Analysis
and presentation of cumulative antimicrobial susceptibility test data; ap-
proved guideline. NCCLS document M39-A. National Committee for
Clinical Laboratory Standards, Wayne, PA.
5. Anderson DJ, Miller BA, Chen LF, Adcock LH, Cook E, Cromer AL,
Louis S, Thacker PA, Sexton DJ. 2011. The network approach for
prevention of healthcare-associated infections: long-term effect of par-
ticipation in the Duke Infection Control Outreach Network. Infect
jcm.asm.org 2981
Moehring et al.
Control Hosp Epidemiol 32:315322. http://dx.doi.org/10.1086
/658940.
6. Clinical and Laboratory Standards Institute. 2013. Performance stan-
dards for antimicrobial susceptibility testing; 23rd informational supple-
ment. CLSI document M100-S23. Clinical and Laboratory Standards In-
stitute, Wayne, PA.
7. Lautenbach E, Nachamkin I. 2006. Analysis and presentation of cumu-
lative antimicrobial susceptibility data (antibiograms): substantial vari-
ability across medical centers in the United States. Infect Control Hosp
Epidemiol 27:409 412. http://dx.doi.org/10.1086/503342.
8. Ernst EJ, Diekema DJ, BootsMiller BJ, Vaughn T, Yankey JW, Flach SD,
Ward MM, Franciscus CL, Acosta E, Pfaller MA, Doebbeling BN. 2004.
Are United States hospitals following national guidelines for the analysis
and presentation of cumulative antimicrobial susceptibility data? Di-
agn Microbiol Infect Dis 49:141145. http://dx.doi.org/10.1016/j
.diagmicrobio.2004.03.007.
9. Boehme MS, Somsel PA, Downes FP. 2010. Systematic review of antibi-
ograms: a National Laboratory System approach for improving antimi-
2982 jcm.asm.org Journal of Clinical Microbiology
crobial susceptibility testing practices in Michigan. Public Health Rep
125(Suppl 2):6372.
10. Xu R, Polk RE, Stencel L, Lowe DK, Guharoy R, Duggal RW, Wiest M,
Putney KS, Flint NB. 2012. Antibiogram compliance in University
Health System Consortium participating hospitals with Clinical and Lab-
oratory Standards Institute guidelines. Am J Health Syst Pharm 69:598
606. http://dx.doi.org/10.2146/ajhp110332.
11. Zapantis A, Lacy MK, Horvat RT, Grauer D, Barnes BJ, ONeal B,
Couldry R. 2005. Nationwide antibiogram analysis using NCCLS M39-A
guidelines. J Clin Microbiol 43:2629 2634. http://dx.doi.org/10.1128
/JCM.43.6.2629-2634.2005.
12. Centers for Disease Control and Prevention. 2013. Centers for Disease
Control and Prevention: antimicrobial resistance threat report. http:
//www.cdc.gov/drugresistance/threat-report-2013/. Accessed 15 October
2013.
13. Spellberg B, Bartlett JG, Gilbert DN. 2013. The future of antibiotics
and resistance. N Engl J Med 368:299 302. http://dx.doi.org/10.1056
/NEJMp1215093.
Downloaded from http://jcm.asm.org/ on October 6, 2017 by guest
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