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Journal of Global Antimicrobial Resistance 4 (2016) 2127

Contents lists available at ScienceDirect

Journal of Global Antimicrobial Resistance


journal homepage: www.elsevier.com/locate/jgar

Administration of a survey to evaluate the attitudes of house staff


physicians towards antimicrobial resistance and the antimicrobial
stewardship programme at a community teaching hospital
Veena Venugopalan a,b,1, Nathan Trustman c,2, Nyla Manning b,d, Nehal Hashem b,e,
Leonard Berkowitz b,3, Levita Hidayat f,g,*
a
Scripps La Jolla, 9888 Genesee Avenue, La Jolla, CA 92037, USA
b
The Brooklyn Hospital Center, 121 DeKalb Avenue, Brooklyn, NY 11201, USA
c
Long Island University, 1 University Plaza, Brooklyn, NY 11201, USA
d
SUNY Downstate Medical Center, 450 Clarkson Avenue, Brooklyn, NY 11203, USA
e
Lancaster General Hospital, 555 North Duke Street, Lancaster, PA 17602, USA
f
Touro College of Pharmacy, 230 West 125th Street, New York, NY 10027, USA
g
The Medicines Company, 8 Sylvan Way, Parsippany, NJ 07054, USA

A R T I C L E I N F O A B S T R A C T

Article history: Antimicrobial stewardship programmes (ASPs) are used in numerous institutions in an effort to promote
Received 15 October 2015 safe and effective antimicrobial use. The objectives of this study were to (i) assess physicians
Received in revised form 14 January 2016 perceptions, attitudes and knowledge about antimicrobial use, resistance and the ASP at The Brooklyn
Accepted 18 January 2016
Hospital Center (TBHC) and (ii) measure physicians beliefs and attitudes to the current system of prior
Available online 8 February 2016
authorisation of antimicrobials. A 75-item, anonymous, voluntary, traditional paper and pencil survey
was distributed to resident physicians at TBHC. Multiple-choice, 5-point Likert scale and knowledge-
Keywords:
based questions were utilised. Of the 261 residents, 129 (49%) completed the survey. The respondents
Survey
signicantly believed that antibiotics are overused more frequently nationally vs. locally [117/129 (91%)
Antimicrobial stewardship
Prior authorisation vs. 91/129 (71%); P = 0.0001]. Although 49% (63/129) felt that other providers overprescribe antibiotics,
Attitudes only 26% (34/129) agreed that they themselves were contributing to the current problem (P = 0.0003).
Perceptions Fifty-seven percent of respondents agreed that individual patient care is improved by having an
antibiotic approval programme; however, 45% of respondents reported that the antibiotic approval
programme limits their autonomy in choosing antibiotics. Compared with surgical residents, medical
residents were more likely (33% vs. 13%; P = 0.02) to feel that the antibiotic approval programme forced
them to choose an inappropriate antibiotic. On the antibiotic knowledge assessment segment of the
survey, there was no difference in score when stratied by specialty or years of postgraduate training.
Based on the survey results, house staff are supportive of antimicrobial stewardship and feel that the ASP
is valuable for patient care.
2016 International Society for Chemotherapy of Infection and Cancer. Published by Elsevier Ltd. All
rights reserved.

1. Introduction

According to the US Centers for Disease Control and Prevention


(CDC), antimicrobial resistance has become increasingly problem-
* Corresponding author. Present address: The Medicines Company, 8 Sylvan Way,
Parsippany, NJ 07054, USA. Tel.: +1 626 841 9242.
atic and is on the rise [1]. Studies have noted that ca. 30% of days of
E-mail address: Lkhidayat@gmail.com (L. Hidayat). antimicrobial therapy may be deemed unnecessary [24]. Antimi-
1
Present address: Department of Pharmacy, Scripps Green Hospital, 10666 N. crobial stewardship programmes (ASPs) have been shown to
Torrey Road, La Jolla, CA 92037, USA. improve antimicrobial use and to reduce antimicrobial resistance,
2
Present address: Department of Pharmacy, Coney Island Hospital, 2601 Ocean
mortality, hospital length of stay and healthcare costs [5]. The
Pkwy, Brooklyn, NY 11235, USA.
3
Present address: Division of Infectious Diseases, Medical Director, PATH Center, Infectious Diseases Society of America (IDSA) and the Society for
Department of Internal Medicine, 121 DeKalb Avenue, Brooklyn, NY 11201, USA. Healthcare Epidemiology of America (SHEA) advocate the

http://dx.doi.org/10.1016/j.jgar.2016.01.004
2213-7165/ 2016 International Society for Chemotherapy of Infection and Cancer. Published by Elsevier Ltd. All rights reserved.
22 V. Venugopalan et al. / Journal of Global Antimicrobial Resistance 4 (2016) 2127

implementation of ASPs and appropriate infection prevention and antimicrobial agents prescribed in the past 6 months, years since
control strategies in order to provide patients with safe and graduating from medical school, year of residency/fellowship if
effective therapy and limit the emergence of resistant pathogens applicable, area of specialty and years since graduating from that
[6]. Institutions have implemented ASPs in an effort to promote the specialty. Questions regarding antimicrobial education sources
judicious use of antimicrobial agents. The IDSA/SHEA guidelines and antimicrobial perceptions and attitudes consisted of a
for developing an institutional programme to enhance antimicro- combination of standard multiple-choice questions and those
bial stewardship outlined two core strategies for ASP practice, utilising a 5-point Likert scale with responses that ranged from
namely (i) prospective review with intervention and feedback and strongly agree to strongly disagree, always to never, or always
(ii) formulary restriction with prior authorisation (PA) [6]. Supple- useful to never useful. The survey concluded with ten knowl-
ments to these core ASP strategies include education, guidelines edge-based questions that were obtained from a previously
and clinical pathways implementation, antimicrobial cycling, conducted survey with permission from the author [9].
antimicrobial order forms, combination therapy, streamlining Following Institutional Review Board approval, the survey was
and de-escalation of therapy, dose optimisation, and parenteral-to- distributed at various physician conferences. Completion of the
oral conversion. Implementing multiple strategies has been shown survey served to indicate a participants consent to participate in
to be effective in the hospital setting in reducing antimicrobial the study. An incentive in the form of a $5 gift card was provided
overuse and improving physicians antimicrobial knowledge upon completion of the survey.
[7,8]. Peto et al. evaluated patients with bloodstream infections
and found that mean antimicrobial consumption was signicantly 2.2. Setting and antimicrobial stewardship programme
reduced following a stewardship intervention [8]. The intervention
included formulary restriction and authorisation allowing only TBHC is a 416-bed community teaching facility in Brooklyn, NY.
intensive care unit consultants to prescribe antimicrobials. An ASP was established at TBHC in 2005 using a PA strategy that
Physicians perceptions of antimicrobial use and resistance required prescribers to obtain approval from a member of the
and ASPs have been shown to vary from institution to institution stewardship team before restricted antibiotics are dispensed. A
[915]. Studies noted that while physicians agree that antimicro- previously conducted audit of the programme revealed that the
bials are overused on a national scale, they do not agree that most common antibiotic approvals were for vancomycin (72%),
antimicrobials are overused at their own institution [9,14]. Simi- piperacillin/tazobactam (27%) and cefepime (24%). The indications
larly, surveys taken by house staff physicians with regard to for which antibiotics were most frequently requested for were skin
antimicrobial resistance suggest that more physicians agree that and soft-tissue infections (60%) and pneumonia (23%). In 49% of
antimicrobial resistance is a national issue rather than a local one patients, restricted antibiotics were initiated empirically without
[1012]. Overall, formal education of physicians on antimicrobials an established source of infection. Forty-ve percent of interven-
in an effort to prevent antimicrobial resistance and overuse has tions performed by the ASP involved therapeutic dose monitoring
been well received [1114]. However, the varying degree of combined with renal dose adjustment. Also, recommendations for
antimicrobial knowledge among specialties presents a challenge in ordering laboratory tests and cultures to assess response to
identifying strategies to focus educational efforts [14]. treatment were made in 23% of cases.
Whilst a literature search revealed few studies that evaluated The ASP team is comprised of two infectious diseases-trained
physicians opinions of PA-based ASPs, these have all been clinical pharmacists, ve PGY-1 and one infectious diseases PGY-2
conducted in large academic institutions, therefore house staff pharmacy residents, one infectious diseases physician and one
attitudes of stewardship practice and antimicrobial resistance in clinical microbiologist. The pharmacy residents at TBHC partici-
smaller community-based facilities is unknown [15,16]. The pate in stewardship activities through a 24-h in-house on-call
objectives of this study were (i) to assess the perceptions, attitudes programme.
and knowledge of physicians about antimicrobial use, resistance Prescriber education and training performed by the ASP at TBHC
and the ASP at The Brooklyn Hospital Center (TBHC) (Brooklyn, NY) was developed based on the educational strategies described by
and (ii) to measure the beliefs and attitudes of physicians regarding Pulcini et al. and include activities such as antimicrobial
the current system of PA of antimicrobials. Obtaining this stewardship-focused lectures, development of clinical pathways,
information will be critical in enhancing the effectiveness of the restrictive formulary with PA, and prospective audits with active
ASP in training physicians on the appropriate use of antimicrobials. intervention on restricted antimicrobials [12].

2. Method 2.3. Data analysis

2.1. Survey instrument and administration Following distribution and collection of the survey from all
participants, data were organised and compiled. Demographic and
The study was conducted at TBHC from November 2012 through practice pattern data were recorded. Interns and upper-year
July 2013. House staff employed by the institution (n = 261) were residents were compared based on the factors that inuenced their
allowed to participate. A 75-item, voluntary, anonymous, tradi- antibiotic selection, their perceptions about antimicrobial use and
tional paper and pencil survey was utilised. A survey instrument resistance, and their attitudes towards the ASP and the antimicro-
based on two previously published studies on physicians bial PA process at TBHC. Interspecialty perceptions were compared
attitudes, beliefs and knowledge on antimicrobial use and based on their perceptions about antimicrobial use and resistance
resistance was developed [9,16]. The rst survey was originally and their attitudes towards the ASP and the antimicrobial PA
developed by Abbo et al. and the Get Smart for Healthcare program process at TBHC. Performance on the knowledge-based section
of the CDCs Division of Healthcare Quality Promotion [9] and the was compared between interns and upper-year residents and
second was created by Seemugal and Bruno [16]. Permission to use between specialties (i.e. emergency medicine, internal medicine,
these surveys was granted by the corresponding authors. paediatrics, surgery, etc.).
The survey consisted of four major sections: (i) demographics; The study objectives were analysed through univariate and
(ii) educational sources relating to antimicrobials; (iii) antimicro- bivariate analyses. A x2 or Fishers exact test was performed for all
bial perceptions and attitudes; and (iv) attitudes towards the ASP. categorical variables and a Students t-test was performed for all
Demographic information included an estimation of the number of continuous variables. A P-value of 0.05 was considered to
V. Venugopalan et al. / Journal of Global Antimicrobial Resistance 4 (2016) 2127 23

indicate signicance. Statistical analyses were performed using therapy and tailor antibiotic regimens based upon culture results
GraphPad Prism v.6.0 (GraphPad Software Inc., San Diego, CA). (81/129; 63%). However, only 25 (19%) based their decision on the
hospital antibiogram and almost one-third (37/129; 29%) based
their decision on antibiotic resources such as The Sanford Guide to
3. Results Antimicrobial Therapy and UpToDate (Table 1).
The utility of various sources of antimicrobial continuing
3.1. Demographics education and information is summarised in Table 2. Overall,
infectious diseases colleagues and UpToDate were rated as the
Of the 261 residents, 129 (49%) completed the survey. The most useful [105/129 (81%) and 104/129 (81%), respectively], and
response was highest among rst-year interns with 45 (35%), pharmaceutical-sponsored off-campus lectures as the least useful
compared with 33 (26%) second-year, 27 (21%) in their third-year (30/129; 23%). Other resources used and found to be always or
and 24 (19%) in their fourth year or higher (Table 1). The two most often useful include the Sanford guide (68/129; 53%), grand rounds
common specialties among the respondents were internal medi- (71/129; 55%), case conference (73/129; 57%) and ward rotations
cine (54/129; 42%) and surgery (40/129; 31%). (84/129; 65%).
Almost all respondents agreed that strong knowledge of
3.2. Antimicrobial use and education antibiotics is critical for their medical career (121/129; 94%)
(Table 3). In addition, the majority of respondents were in
The majority of respondents (123/129; 95%) noted that they had agreement that they would like more education on antibiotics
been involved in antibiotic prescribing in the past 6 months and would like feedback on their antibiotic selections [107/129
and most of their clinical time was spent in the inpatient setting (83%) and 104/129 (81%), respectively] (Table 3).
(96/129; 74%). When asked about empirical antibiotic selection, the
majority of respondents preferred to start with broad-spectrum 3.3. Attitudes about resistance and antimicrobial use

Table 1 Factors inuencing respondents antibiotic prescribing are


Demographics and characteristics of respondents (N = 129). summarised in Table 4. Factors that most providers felt always
or often inuenced their antibiotic selection were the risk of
Characteristic Respondents
[n (%)]
missing an infection and if the patient is critically ill or
immunocompromised [93/129 (72%) and 107/129 (83%), respec-
Year of postgraduate training
tively] (Table 4). These two factors were also signicantly more
First 45 (35)
Second 33 (26) important in inuencing antibiotic selection for upper-year
Third 27 (21) residents compared with rst-year interns (P = 0.05). Cost savings
Fourth or higher 24 (19) for the hospital and for patients as well as the risk of developing
Area of specialtya Clostridium difcile colitis were not signicant inuencing factors
Anaesthesiology 2 (2) for antibiotic selection.
Critical care 3 (2) The perceptions of respondents about antibiotic use and
Emergency medicine 19 (15)
resistance are summarised in Table 3. Most respondents agreed
Hospitalist 2 (2)
Infectious diseases 2 (2) that antibiotics are overused, however the respondents signi-
Internal medicine 54 (42) cantly believed that antibiotics are more frequently overused
Paediatrics 9 (7) nationally vs. locally [117/129 (91%) vs. 91/129 (71%); P = 0.0001,
Surgery 40 (31) data not shown]. Upper-year residents were more signicantly in
Years of post-specialty trainingb agreement that antibiotics are overused both nationally and at
One 3 (2) TBHC compared with interns (P = 0.02 and P = 0.05, respectively).
Two There was no difference between upper-year residents and interns
Three 1 (1)
Four or higher 16 (12)
Not applicable/resident/fellow 103 (80)
Table 2
No. of involvements in antibiotic prescribing in the past 6 monthsb Utility of various antimicrobial continuing education sources (N = 129).a
0
16 4 (3) Educational source Not familiar Sometimes Often or
712 8 (6) or never [n (%)] always
1324 13 (10) useful or useful
>24 98 (76) rarely [n (%)]
[n (%)]
Clinical time is spent caring for:b
Inpatients 96 (74) Ward rotations 12 (9) 28 (22) 84 (65)
Outpatients 6 (5) Grand rounds 17 (13) 33 (26) 71 (55)
Approximately equal time between both 23 (18) Case/noon conference 16 (12) 29 (22) 73 (57)
Infectious diseases 5 (4) 16 (12) 105 (81)
Empirical antibiotic selection colleagues
I start with broad-spectrum and tailor upon culture results 81 (63) Pharmaceutical 27 (21) 33 (26) 63 (49)
I base my decision on the hospital antibiogram 25 (19) representatives
I base my decision on the antibiotic 37 (29) Off-campus lectures 48 (37) 32 (25) 30 (23)
resources (i.e. Sanford Guide, UpToDate) sponsored by
I ask my resident 12 (9) pharmaceutical
I ask my attending 16 (12) companies
I use the same one or two antibiotics 5 (4) CME online or live lectures 28 (22) 39 (30) 47 (36)
Otherc 5 (4) Medical journals 9 (7) 34 (26) 78 (60)
a Sanford guide 13 (10) 30 (23) 68 (53)
Multiple specialties for one respondent.
b UpToDate 4 (3) 15 (12) 104 (81)
Some respondents left this section blank.
c a
Others include based on history and physical (H&P), pharmacokinetic (PK) Percentage may not total 100 because of rounding and/or some respondents did
consult and infectious diseases consult. not complete the questionnaires.
24 V. Venugopalan et al. / Journal of Global Antimicrobial Resistance 4 (2016) 2127

Table 3
Agreement of respondents with statements regarding perceptions about antimicrobial use and resistance.

Perception All respondents Interns Upper-year P-value


(N = 129) [n (%)] (N = 45) [n (%)] residents
(N = 84) [n (%)]

Antibiotics are overused nationally 117 (91) 37 (82) 80 (95) 0.02


Antibiotics are overused at TBHC 91 (71) 27 (60) 64 (76) 0.05
Antibiotic resistance is not a signicant problem nationally 19 (15) 11 (24) 8 (10) 0.02
Antibiotic resistance is not a signicant problem at TBHC 12 (9) 6 (13) 6 (7) 0.2
Better use of antibiotics will reduce problems with antibiotic-resistant 114 (88) 37 (82) 77 (92) 0.14
organisms
Strong knowledge of antibiotics is important in my medical career 121 (94) 40 (89) 81 (96) 0.09
I am condent that I use antibiotics optimally outside the ICU 66 (51) 20 (44) 46 (55) 0.26
I am condent that I use antibiotics optimally in the ICU 67 (52) 18 (40) 49 (58) 0.04
I overprescribe antibiotics 34 (26) 15 (33) 19 (23) 0.19
Other doctors overprescribe antibiotics 63 (49) 20 (44) 43 (51) 0.46
I would like more feedback on my antibiotic selections 104 (81) 33 (73) 71 (85) 0.12
I would like more education on antibiotics 107 (83) 37 (82) 70 (83) 0.87
Interactions with pharmaceutical representatives do not inuence 66 (51) 19 (42) 47 (56) 0.14
my antibiotic selections
Locally developed guidelines for antibiotic treatment would be more 87 (67) 22 (49) 65 (77) 0.001
useful to me than national guidelines
I am concerned about antibiotic resistance in the community when 106 (82) 31 (69) 75 (89) 0.004
I prescribe antibiotics
I am concerned about antibiotic resistance in my hospital when 107 (83) 34 (76) 73 (87) 0.1
I prescribe antibiotics
New antibiotics will be developed in the future that will keep up 50 (39) 23 (51) 27 (32) 0.04
with the problem of resistance
Prescribing broad-spectrum antibiotics when there are equally 92 (71) 31 (69) 61 (73) 0.65
effective narrower-spectrum antibiotics increases antibiotic
resistance
Poor infection control practices by healthcare professionals causes 79 (61) 25 (56) 54 (64) 0.94
antibiotic resistance
Inappropriate use of antibiotics can harm patients 115 (89) 39 (87) 76 (90) 0.51
Inappropriate use of antibiotics is professionally unethical 90 (70) 31 (69) 59 (70) 0.9

TBHC, The Brooklyn Hospital Center; ICU, intensive care unit.

Table 4 when asked whether better use of antibiotics will reduce problems
Frequency distribution of respondents and factors inuencing their antibiotic
with antibiotic-resistant organisms [77/84 (92%) vs. 37/45 (82%);
selection (N = 129).
P = 0.14). When further stratied by specialty, surgical residents
Factor Never or Sometimes Often or P-value felt more strongly than internal medicine residents that resistance
rarely [n (%)] always
could be reduced with more appropriate antibiotic usage [38/40
[n (%)] [n (%)]
(95%) vs. 44/54 (81%); P = 0.05, data not shown].
Cost savings for patients 0.45 Overall, 49% (63/129) agreed that other providers overprescribe
Intern 12 (9) 20 (16) 13 (10)
antibiotics, however only 26% (34/129) felt that they themselves
Upper-year residents 17 (13) 37 (29) 29 (22)
overprescribe antibiotics (P = 0.0003). When further stratied by
Cost savings for the hospital 0.54 specialty, there was a trend for surgical residents to indicate that
Intern 16 (12) 17 (13) 12 (9)
Upper-year residents 41 (32) 25 (19) 18 (14)
other doctors overprescribe antibiotics compared with internal
medicine residents [21/40 (53%) vs. 19/54 (35%); P = 0.09, data not
Risk of missing an infection 0.05 shown]. Upper-year residents were signicantly more concerned
Intern 1 (1) 9 (7) 34 (26)
Upper-year residents 6 (5) 16 (12) 59 (46)
with antibiotic resistance in the community when they prescribed
antibiotics compared with interns [75/84 (89%) vs. 31/45 (69%);
Patient demands and expectations for antibiotics 0.13
P = 0.004]. A majority of the respondents agreed that locally
Intern 28 (22) 11 (9) 6 (5)
Upper-year residents 59 (46) 11 (9) 14 (11)
developed guidelines for antibiotic treatment would be more
useful to them than national guidelines (87/129; 67%). Upper-year
Patient is critically ill and/or immunocompromised 0.05
residents were more in favour of locally developed guidelines
Intern 2 (2) 6 (5) 37 (29)
Upper-year residents 3 (2) 9 (7) 70 (54) compared with interns [65/84 (77%) vs. 22/45 (49%); P = 0.001].
Whilst the majority of respondents agreed that inappropriate
Reassurance when using an antibiotic even if it might be the wrong 0.17
use of antibiotics could harm patients (115/129; 89%), when
one
Intern 26 (20) 7 (5) 10 (8) stratied based on specialty, surgical residents were overwhelm-
Upper-year residents 65 (50) 16 (12) 3 (2) ingly more in agreement with this statement compared with
internal medicine residents [39/40 (98%) vs. 40/54 (74%); P = 0.002,
Unexplained fever or leukocytosis even if culture results 0.46
Intern 12 (9) 18 (14) 14 (11) data not shown].
Upper-year residents 19 (15) 42 (33) 23 (18)

Treat colonisation to prevent infections 0.29 3.4. Attitudes towards the antimicrobial stewardship programme
Intern 21 (16) 10 (8) 14 (11)
Upper-year residents 48 (37) 19 (15) 16 (12) Perceptions of respondents towards the ASP and the antimi-
Risk of developing Clostridium difcile colitis 0.62 crobial PA (dened earlier) process at TBHC are summarised in
Intern 12 (9) 12 (9) 21 (16) Table 5. Fifty-eight percent (75/129) of respondents felt that a
Upper-year residents 19 (15) 34 (26) 31 (24) reduction in antimicrobial resistance was the ASPs major
V. Venugopalan et al. / Journal of Global Antimicrobial Resistance 4 (2016) 2127 25

Table 5
Perceptions of respondents towards the antimicrobial stewardship programme (ASP) and the antimicrobial prior authorisation process.

Perception All respondents Interns Upper-year residents P-value


(N = 129) [n (%)] (N = 45) [n (%)] (N = 84) [n (%)]

Individual patient care is improved by having an antibiotic approval 74 (57) 27 (60) 47 (56) 0.95
programme
Having to call for approval makes the team think more carefully about 66 (51) 24 (53) 42 (50) 0.93
choosing an antibiotic
The antibiotic approval programme limits clinicians autonomy in choosing 58 (45) 22 (49) 36 (43) 0.75
antibiotics
I nd the antibiotic approval process educational 56 (43) 20 (44) 36 (43) 0.83
The recommendations I get from the antibiotic approval programme are 65 (50) 27 (60) 38 (45) 0.16
consistent
Because of the antibiotic approval programme I am forced to choose 25 (19) 9 (20) 16 (19) 0.93
antibiotics I feel are inappropriate
If there was no antibiotic approval programme our team would likely 57 (44) 23 (51) 34 (40) 0.38
consult ID more frequently
The primary purpose of the antibiotic approval programme is to decrease 75 (58) 25 (56) 50 (60) 0.24
antibiotic resistance in the hospital
The primary purpose of the antibiotic approval programme is to reduce the 47 (36) 17 (38) 30 (36) 0.92
amount of money the hospital spends on antibiotics
Having an antibiotic approval programme helps me provide better care for 68 (53) 23 (51) 45 (54) 0.4
my patients
I nd the antibiotic approval programme helpful in assisting me in dosing 67 (52) 26 (58) 41 (49) 0.52
antibiotics appropriately
Having an antibiotic approval system helps to prevent the development of 71 (55) 27 (60) 44 (52) 0.65
antibiotic resistance in the hospital
I nd having to call for antibiotic approval frustrating 35 (27) 10 (22) 25 (30) 0.22
The clinician who is seeing the patient is in a more appropriate position to 48 (37) 20 (44) 28 (33) 0.31
pick the correct antibiotic than someone on the phone who has never seen
the patient

ID, infectious diseases.

objective, whilst 36% (47/129) perceived cost savings to the indwelling catheters [97/129 (75%) and 115/129 (89%), respec-
hospital as the primary purpose. tively, data not shown]. There was no difference in antibiotic
Eighty-one percent (104/129) of respondents stated that they knowledge score when stratied by specialty or years of
would like more feedback on their antibiotic selections and 83% postgraduate training.
(107/129) would like more education on antibiotics. Whilst more
than one-half of the respondents (74/129; 57%) agreed that 4. Discussion
individual patient care is improved by having an antibiotic
approval programme, 45% (58/129) reported that the antibiotic To the best of our knowledge, this is the rst study assessing a
approval programme limits their autonomy in choosing anti- PA-based ASP in a community teaching hospital [1317]. Overall,
biotics. There were no difference in perceptions of these two the results demonstrated that house staff are aware of antimicro-
factors between upper-year residents and interns. One-half of the bial resistance and overuse problems both at a national and local
respondents (65/129; 50%) agreed that the recommendations from level, with no signicant interspecialty differences. Based on the
the antibiotic approval programme are consistent; however, 19% survey responses, upper-year residents were signicantly more in
(25/129) felt that the antibiotic approval programme forced them an agreement with the problem of national and local antimicrobial
to choose an antibiotic that they considered inappropriate. There resistance and overuse compared with interns. In addition, similar
were no difference in perceptions of these two factors between to results from previous studies, 91% of the respondents
upper-year residents and interns. However, when stratied by signicantly felt that antibiotics are overused nationally, whilst
specialty, internal medicine residents were more in agreement 71% felt that antibiotics are overused at TBHC [9,14,17].
that recommendations from members of the ASP are consistent The strict PA process for broad-spectrum antibiotics at TBHC
compared with surgical residents [39/54 (72%) vs. 20/40 (50%); may contribute to the perceived differences in overuse of
P = 0.03, data not shown]. In addition, internal medicine residents antibiotics nationally vs. locally among medical staff.
felt more strongly than surgical residents that the ASP forced them Most respondents also signicantly agreed that while other
to choose an antibiotic that they felt was inappropriate [18/54 practitioners overprescribe antibiotics, they did not feel that their
(33%) vs. 5/40 (13%); P = 0.02, data not shown]. own prescribing practice was a problem. This nding is consistent
with those in prior studies performed at large academic institu-
3.5. Antibiotic knowledge score tions and highlights the commonality of such preconceptions
regardless of size of institution or practice site [9,14].
The overall median score for all respondents was 70 [inter- The PA strategy, requiring prescribers to obtain approval from a
quartile range (IQR) 6080]. Overall, 76% (98/129) of respondents member of the ASP team before restricted antibiotics are
were able to identify correct rst-line treatment for patients with dispensed, is frequently employed as an ASP strategy
meticillin-resistant Staphylococcus aureus (MRSA) bacteraemia [6,15,16]. PA ASPs may be perceived negatively as it is time
compared with only 33% (42/129) who were able to identify consuming and infringing on the prescribers autonomy. Lack of
correct treatment of extended-spectrum b-lactamase (ESBL)- prescribers buy-in to the ASP may prevent it from being
positive Escherichia coli. The vast majority were able to identify maximally effective [16]. We are only aware of a few studies that
specic antibiotics that can potentially increase the risk assessed the attitudes of house staff on PA-based ASPs [15,16]. A
of developing C. difcile and the appropriate management of study by Seemungal and Bruno noted that one-half of their
26 V. Venugopalan et al. / Journal of Global Antimicrobial Resistance 4 (2016) 2127

respondents nd calling for antibiotic approval frustrating [16]. In aimed at informing prescribers about resistance, antimicrobial
contrast, less than one-third of the respondents in the current usage patterns within the institution, and prescribing patterns
study found having to call for antibiotic approval frustrating and among house staff. Education is an essential element of any
one-half of respondents believed that they received consistent programme designed to inuence prescribing behaviour and can
recommendations. The difference in ndings from the previous provide a foundation of knowledge that will enhance and increase
study may be due to the ASP team providing around-the-clock the acceptance of stewardship strategies [6]. We believe the results
services, whilst the prior study had only an 8 am to 10 pm ASP from the current study will be valuable in guiding educational
approval service [16]. As noted in previous studies, the current efforts in order for ASPs to be successful and well received by
study also found that most physicians agreed that knowledge of clinicians in their respective institutions.
antibiotics is important, that they would like more education and
feedback on their antibiotic selections, that they are less likely to Funding
prescribe restricted agents requiring pre-approval, and that locally
developed guidelines for antimicrobial treatment are more useful This study was funded through the senior authors intramural
than national guidelines [1315,18]. Conversely, in the current funding during her tenure at Touro College of Pharmacy (New York,
study upper-year residents were more likely to be in agreement NY).
with the usefulness of locally developed guidelines compared with
interns. The difference in this result may largely due to better
Competing interests
understanding of antimicrobial use and resistance by upper-year
residents compared with interns.
None declared.
The results of this survey are noteworthy and reveal that house
staff at TBHC nd the ASP services valuable. Less than one-half of
the respondents perceive cost savings to the hospital as the Ethical approval
primary purpose of the ASP, whilst more than one-half of
respondents felt that reduction of antimicrobial resistance was This study was approved by the Institutional Review Board of
the major objective and the ASP helps them provide better care for The Brooklyn Hospital Center (Brooklyn, NY).
their patients. This nding highlights the need to present the ASP at
our institution as a best practice rather than a cost cutting Acknowledgments
initiative. The majority of respondents reported that they would
like more education on antibiotics and feedback on their antibiotic The authors would like to thank Drs Lilian Abbo (University of
selections. This information will be vital in the development of Miami Miller School of Medicine, Miami, FL) and Christopher
guidelines and educational programmes to promote appropriate Bruno (Drexel University College of Medicine, Philadelphia, PA) for
antimicrobial use. permission to use their survey questionnaires.
Similar to other survey results, the respondents agreed that
other physicians overprescribe antibiotics compared with their References
own prescribing patterns. Internal medicine residents in particular
[1] Centers for Disease Control and Prevention (CDC). CDCs campaign to prevent
were more likely than surgical residents to feel that others antimicrobial resistance in health-care settings. MMWR Morb Mortal Wkly
overprescribe. Rep 2002;51:343.
These results are also consistent with the results of prior [2] Werner NL, Hecker MT, Sethi AK, Donskey CJ. Unnecessary use of uoroquino-
lone antibiotics in hospitalized patients. BMC Infect Dis 2011;11:187.
surveys [9,14]. The current ndings are in agreement with those of [3] Hecker MT, Aron DC, Patel NP, Lehmann MK, Donskey CJ. Unnecessary use of
Srinivasan et al. that the interspecialty variations on several items antimicrobials in hospitalized patients: current patterns of misuse with an
suggest that the answers on the survey were a true reection of emphasis on the antianaerobic spectrum of activity. Arch Intern Med
2003;163: 9728.
practice [14]. Internal medicine residents were more likely to feel [4] Antoine TL, Curtis AB, Blumberg HM. Knowledge, attitudes, and behaviors
that the ASP forced them to choose an antibiotic that they felt was regarding piperacillintazobactam prescribing practices: results from a mul-
inappropriate compared with surgical residents. No differences ticenter study. Infect Control Hosp Epidemiol 2006;27:12747.
[5] Klevens RM. Estimating health care-associated infections and deaths in U.S.
were found when stratied between interns vs. upper-year
hospitals, 2002. Public Health Rep 2007;122:1606.
residents. This study also found that surgical residents were more [6] Dellit TH, Owens RC, McGowan Jr JE, Gerding DN, Weinstein RA, Burke JP, et al.
in agreement than internal medicine residents with the statement Infectious Diseases Society of America and the Society for Healthcare Epide-
that recommendations from members of the ASP are consistent. miology of America guidelines for developing institutional program to en-
hance antimicrobial stewardship. Clin Infect Dis 2007;44:15977.
These survey ndings will assist us in targeted interventions such [7] Apisarnthanarak A, Danchaivijitr S, Khawcharoenporn T. Effectiveness of
as tailoring antimicrobial education to specic specialties. education and an antibiotic-control program in a tertiary care hospital in
The overall median score of the antibiotic knowledge test in this Thailand. Clin Infect Dis 2006;42:76875.
[8] Peto Z, Benko R, Matuz M, Csullog E, Molnar A, Hajdu E. Results of a local
study was higher compared with a previous study [14]. In the antibiotic management program on antibiotic use in a tertiary intensive care
current study, the respondents median score was 70 (IQR 6080) unit in Hungary. Infection 2008;36:5604.
and no difference in antibiotic knowledge score was found when [9] Abbo L, Sinkowitz-Cochran R, Smith L, Ariza-Heredia E, Gomez-Marn O,
Srinivasan A, et al. Faculty and resident physicians attitudes, perceptions,
stratied by specialty or years of postgraduate training. However, and knowledge about antimicrobial use and resistance. Infect Control Hosp
only 33% of respondents were able to identify correct treatment of Epidemiol 2011;32:7148.
ESBL-positive E. coli. These results demonstrate the need for [10] Giblin TB, Sinkowitz-Cochran R, Harris PL, Jacobs S, Liberatore K, Palfreyman
MA, et al. Clinicians perceptions of the problem of antimicrobial resistance in
continued educational efforts with particular focus on topics such
healthcare facilities. Arch Intern Med 2004;164:16628.
as antimicrobial resistance mechanisms. [11] Wester CW, Durairaj L, Evans AT, Schwartz DN, Husain S, Martinez E. Antibiotic
A limitation of this study is that house staff who chose not to resistance: a survey of physician perceptions. Arch Intern Med 2002;162:
22106.
participate may have opinions signicantly different from those of
[12] Pulcini C, Williams F, Molinari N, Davey P, Nathwani D. Junior doctors
responders, potentially introducing unmeasured bias. However, knowledge and perceptions of antibiotic resistance and prescribing: a survey
we believe the results of this survey are encouraging and in France and Scotland. Clin Microbiol Infect 2011;17:807.
demonstrate the widespread support for PA-based ASPs and ASPs [13] Guerra CM, Pereira CA, Neves Neto AR, Cardo DM, Correa L. Physicians
perceptions, beliefs, attitudes, and knowledge concerning antimicrobial resis-
in hospitals. The survey ndings have also revealed areas of tance in a Brazilian teaching hospital. Infect Control Hosp Epidemiol 2007;28:
improvement for our ASP, such as focused educational efforts 14114.
V. Venugopalan et al. / Journal of Global Antimicrobial Resistance 4 (2016) 2127 27

[14] Srinivasan A, Song X, Richards A. A survey of knowledge, attitudes, and beliefs [17] Paterson DL. The role of antimicrobial management programs in optimizing
of house staff physicians from various specialties concerning antimicrobial use antibiotic prescribing within hospitals. Clin Infect Dis 2006;42(Suppl 2):
and resistance. Arch Intern Med 2004;164:14516. S905.
[15] Bannan A, Buono E, McLaws ML, Gottlieb T. A survey of medical staff attitudes [18] Steinberg M, Dresser LD, Daneman N, Smith OM, Matte A, Marinoff N, et al. A
to an antibiotic approval and stewardship programme. Intern Med J 2009;39: national survey of critical care physicians knowledge, attitudes, and percep-
6628. tions of antimicrobial stewardship programs. J Intensive Care Med 2016;31:
[16] Seemugal IA, Bruno CJ. Attitudes of housestaff toward a prior-authorization- 615.
based antibiotic stewardship program. Infect Control Hosp Epidemiol
2012;33:42931.

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