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Objectives: To determine antimicrobial stewardship (AMS) programme practices in Asian secondary- and ter
tiary-care hospitals.
Methods: AMS programme team members within 349 hospitals from 10 countries (Cambodia, India, Indonesia,
Japan, Malaysia, Pakistan, the Philippines, Taiwan, Thailand and Vietnam) completed a questionnaire via a web-
based survey link. The survey contained questions as to whether 12 core components deemed essential for AMS
programmes were implemented.
Results: Overall, 47 (13.5%) hospitals fulfilled all core AMS programme components. There was a mean positive
response rate (PRR) of 85.6% for the responding countries in relation to a formal hospital leadership statement of
support for AMS activities, but this was not matched by budgeted financial support for AMS activities (mean PRR
57.1%). Mean PRRs were ≥80.0% for the core AMS team comprising a physician or other leader responsible for
AMS activities, a pharmacist and infection control and microbiology personnel. Most hospitals had access to a
timely and reliable microbiology service (mean PRR 90.4%). Facility-specific antibiotic treatment guidelines for
common infections (mean PRR 78.7%) were in place more often than pre-authorization and/or prospective audit
and feedback systems (mean PRR 66.5%). In terms of AMS monitoring and reporting, PRRs of monitoring specific
antibiotic use, regularly publishing AMS outcome measures, and the existence of a hospital antibiogram were
75.1%, 64.4% and 77.9%, respectively.
Conclusions: Most hospitals participating in this survey did not have AMS programmes fulfilling the requirements
for gold standard AMS programmes in hospital settings. Urgent action is required to address AMS funding and
resourcing deficits.
© The Author(s) 2022. Published by Oxford University Press on behalf of British Society for Antimicrobial Chemotherapy.
This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (https://
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A survey of AMS programmes in Asia
157 (45.0)b
135 (38.7)
327 (93.7)
317 (90.8)
141 (41.0)
206 (59.0)
57 (16.3)
164 (47.0)
200 (57.3)
94 (26.9)
(n = 349)
9 (2.6)
cluding ≥69.0% of hospitals from Cambodia, Indonesia, Japan,
the Philippines, Taiwan, Thailand and Vietnam. ID specialists
were available in 35.8% to 41.9% of hospitals in India, Malaysia
4 (100.0) and Pakistan. Most hospitals had microbiology laboratories
4 (100.0)
4 (100.0)
4 (100.0)
Vietnam
1 (25.0)
2 (50.0)
2 (50.0)
3 (75.0)
3 (75.0)
(90.8%) and infection control processes (93.7%) in place.
(n = 4)
0
0
Gaps in AMS programme core components
Overall, 47 of 349 hospitals (13.5%) fulfilled all 12 core AMS pro
31 (96.9)
28 (87.5)
10 (31.3)
22 (68.8)
11 (34.4)
19 (59.4)
25 (78.1)
13 (40.6)
Thailand
(n = 32)
1 (3.1)
45 (78.9)
24 (42.1)
33 (57.9)
12 (21.1)
29 (50.9)
50 (87.7)
24 (42.1)
54 (94.7)
(n = 57)
Taiwan
4 (100.0)
4 (100.0)
4 (100.0)
4 (100.0)
for AMS activities was 57.1% (Figure 1). Except for Vietnam, dis
2 (50.0)
2 (50.0)
3 (75.0)
2 (50.0)
(n = 4)
13 (41.9)
16 (51.6)
8 (25.8)
23 (74.2)
4 (12.9)
16 (51.6)
13 (41.9)
7 (22.6)
29 (93.5)
(n = 31)
63 (95.5)
42 (63.6)
24 (36.4)
25 (37.9)
25 (37.9)
65 (98.5)
Malaysia
(n = 66)
3 (4.5)
4 (6.1)
15 (93.8)
3 (18.8)
13 (81.3)
11 (68.8)
5 (31.3)
14 (87.5)
14 (87.5)
(n = 16)
Japan
1 (6.3)
May not total 100% due to inclusion of some hospitals in >1 category.
41 (97.6)
32 (76.2)
29 (69.0)
13 (31.0)
9 (21.4)
29 (69.0)
9 (21.4)
37 (88.1)
(n = 42)
93 (97.9)
24 (25.3)
71 (74.7)
13 (13.7)
53 (55.8)
34 (35.8)
30 (31.6)
87 (91.6)
(n = 95)
2 (2.1)
India
2 (100.0)
2 (100.0)
2 (100.0)
2 (100.0)
1 (50.0)
1 (50.0)
1 (50.0)
1 (50.0)
1 (50.0)
(n = 2)
University-affiliated
ID specialist
93, 52.7%).
Secondary
Level of care
Military
Private
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Table 2. Positive responses to AMS programme core component questions from responding hospitals in each surveyed country
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Core AMS programme Cambodia India Indonesia Japan Malaysia Pakistan Philippines Taiwan Thailand Vietnam Overall
component, n (%)a (n = 2) (n = 95) (n = 42) (n = 16) (n = 66) (n = 31) (n = 4) (n = 57) (n = 32) (n = 4) (n = 349)
Chang et al.
Fulfilled all components 0 6/95 (6.3) 6/42 (14.3) N/Ab 9/66 (13.6) 3/31 (9.7) 2/4 (50.0) 17/57 (29.8) 4/32 (12.5) 0 47/349 (13.5)
Hospital leadership
support
Formal statement of 2/2 (100) 65/93 (69.9) 38/42 (90.5) 14/16 (87.5) 62/66 (93.9) 27/31 (87.1) 4/4 (100.0) 52/56 (92.9) 19/32 (59.4) 3/4 (75.0) 286/346 (82.7)
support
Budgeted financial 1/2 (50.0) 48/92 (52.2) 26/42 (61.9) 6/16 (37.5) 30/66 (45.5) 15/31 (48.4) 3/4 (75.0) 38/55 (69.1) 10/32 (31.3) 4/4 (100.0) 181/344 (52.6)
support
AMS team
Physician (or other) 2/2 (100.0) 53/95 (55.8) 36/42 (85.7) 16/16 (100.0) 64/66 (97.0) 19/31 (61.3) 4/4 (100.0) 49/57 (86.0) 26/32 (81.3) 3/4 (75.0) 272/349 (77.9)
leader
Pharmacist 2/2 (100.0) 40/95 (42.1) 38/42 (90.5) 16/16 (100.0) 66/66 (100.0) 19/31 (61.3) 4/4 (100.0) 49/56 (87.5) 22/32 (68.8) 2/4 (50.0) 258/348 (74.1)
IC staff 1/2 (50.0) 72/92 (78.3) 33/40 (82.5) 13/16 (81.3) 63/66 (95.5) 23/29 (79.3) 3/3 (100.0) 47/57 (82.5) 29/32 (90.6) 3/4 (75.0) 287/341 (84.2)
Microbiology staff 2/2 (100.0) 86/93 (92.5) 29/39 (74.4) 13/16 (81.3) 64/66 (97.0) 24/31 (77.4) 3/3 (100.0) 42/57 (73.7) 25/32 (78.1) 4/4 (100.0) 292/343 (85.1)
AMS Interventions
Pre-authorization and/or 0 49/93 (52.7) 18/39 (46.2) 14/16 (87.5) 63/66 (95.5) 22/31 (71.0) 3/3 (100.0) 49/54 (90.7) 23/32 (71.9) 2/4 (50.0) 243/340 (71.5)
PAF
Facility-specific 2/2 (100.0) 69/93 (74.2) 25/39 (64.1) 12/16 (75.0) 38/66 (57.6) 24/31 (77.4) 3/3 (100.0) 46/54 (85.2) 17/32 (53.1) 4/4 (100.0) 240/340 (70.6)
treatment guidelines
AMS monitoring and
reporting
Monitor specific 2/2 (100.0) 37/88 (42.0) 33/38 (86.8) 13/16 (81.3) 65/66 (98.5) 19/31 (61.3) 2/3 (66.7) 52/53 (98.1) 20/30 (66.7) 2/4 (50.0) 245/331 (74.0)
antibiotic use by DOT or
DDD
Regularly publish AMR 1/2 (50.0) 42/88 (47.7) 22/38 (57.9) 15/16 (93.8) 41/66 (62.1) 11/31 (35.3) 3/3 (100.0) 46/53 (86.8) 18/30 (60.0) 2/4 (50.0) 201/331 (60.7)
data and AMS outcome
measures
Hospital antibiogram 2/2 (100.0) 69/88 (78.4) 24/38 (63.2) 14/16 (87.5) 49/66 (74.2) 15/31 (48.4) 3/3 (100.0) 51/54 (94.4) 25/30 (83.3) 2/4 (50.0) 254/332 (76.5)
Hospital infrastructure
Timely/reliable 2/2 (100.0) 83/87 (95.4) 27/38 (71.1) NAb 57/66 (86.4) 28/31 (90.3) 3/3 (100.0) 49/54 (90.7) 24/30 (80.0) 4/4 (100.0) 277/315 (87.9)
microbiology service
DDD, defined daily dose; DOT, days of therapy; IC, infection control; NA, not applicable; PAF, prospective audit and feedback.
a
Not all hospitals responded to all questions; PRRs were based on completed responses to the relevant question (i.e. excluded any hospitals that did not respond to the question).
b
Question C12 was not included in the Japanese survey.
AMS monitoring and reporting Taiwan. Pakistan and Vietnam were the only countries in which
antibiograms were available in ≤50.0% of responding hospitals.
Monitoring use of specific antibiotics by days of therapy or defined
daily dose occurred in ≥81.3% of responding hospitals from
Cambodia, Indonesia, Japan, Malaysia and Taiwan (Table 2), Microbiology services
but the lower PRR from other countries led to a mean PRR of The mean PRR for the 10 responding countries was 90.4% for ac
75.1% (Figure 1). Indian hospitals had the lowest PRR in relation cess to a timely and reliable microbiology service (Figure 1).
to such antibiotic monitoring (37/88, 42.0%). Except for Indonesia (71.1% PRR), ≥ 80.0% of hospitals from all
The mean PRR for the 10 countries was 64.4% for regular pub countries had an in-house microbiology laboratory or access to
lishing of AMR data and AMS outcome measures (Figure 1). As a timely and reliable microbiology service (Table 2).
shown in Table 2, this occurred in 93.8% (15/16) of Japanese hos
pitals and 86.8% (46/53) of Taiwanese hospitals, as well as all re
sponding hospitals in the Philippines. AMS data and outcome Gaps in AMS programme supplementary components
measures were published regularly in ≤50% of responding hospi Responses to supplementary component questions (Table S3)
tals from Cambodia, India, Pakistan and Vietnam. showed that 68.0% of AMS leaders and 54.3% of pharmacists
Hospital antibiograms were available in ≥83.3% of responding working on AMS activities had specialized ID training.
hospitals from several countries, including Japan, Thailand and Guidelines for de-escalation of broad-spectrum antibiotics and
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intravenous-to-oral conversion of antibiotics were available in sometimes or very much challenging by >60% of responding
49.4% and 54.7% of hospitals, respectively. Among hospitals hospitals in each of the surveyed countries (Figure S2).
with antibiograms, 92.1% had them regularly updated. Rapid Overall, almost 60% of hospitals indicated that there was a
diagnostic testing and selective susceptibility reporting were lack of administrative AMS awareness, and that lack of adminis
used in 72.2% and 85.7% of hospitals with access to reliable trative support for AMS posed a challenge for the implementation
microbiology services, respectively. Many hospitals did not have of hospital AMS programmes (Figure 2).
IT systems to support the AMS programme: 48.8% had the IT cap
ability to gather and analyse AMS data, 64.7% used electronic
health records and 56.0% used computerized physician order en
Discussion
try. Educational activities on improving antibiotic prescribing The results of our survey have shown that only 13.5% of 349
were provided for clinicians and other relevant staff in 77.0% of secondary- and tertiary-care hospitals surveyed across 10 Asian
hospitals overall. Such educational activities were provided in countries with wide-ranging economic development levels ful
≥86.4% of hospitals from Japan, Malaysia and Taiwan. Overall, filled all 12 AMS programme core components.
only 45.7% of hospitals that provided such educational activities In a similar survey of tertiary-care hospitals in central Thailand
made them mandatory and certified, most commonly in Japan that assessed the same AMS programme core components in
(76.9%) and Taiwan (84.6%). cluded in the current study, 60.0% of 45 surveyed hospitals ful
filled all 12 core components.25 In our survey, a much lower
proportion of Thai hospitals (12.5%) had implemented all core
AMS programme components. It is possible that, on average,
AMS programme challenges the tertiary-care hospitals in the central Thailand survey had
Some of the most commonly faced challenges when implement more experience with AMS programmes than the hospitals re
ing AMS programmes were related to knowledge gaps and lack of cruited from throughout Thailand in our survey, 31.3% of which
understanding, and inadequate practice, which were considered were secondary-care hospitals as opposed to the more advanced
sometimes or very much challenging by 87.2% and 84.6% of re tertiary level of care. Only 59.4% of the 32 Thai hospitals partici
sponding hospitals, respectively (Figure 2). Further to this, staff pating in our survey had a formal statement of AMS support from
concerns that AMS strategies, such as antibiotic restriction, may hospital leadership; such a statement was available for all hospi
lead to poor patient outcomes were considered sometimes or tals in the central Thailand survey.25
very much challenging by 82.6% of responding hospitals. Staff re Ultimately, resource constraints pose a barrier to the imple
sistance to AMS programmes was a challenge for >60% of re mentation of comprehensive AMS programmes in many Asian
sponding hospitals from all countries except Japan and the hospitals. Although a high proportion of hospitals participating
Philippines (Figure S1). in our survey had formal hospital leadership statements to sup
As shown in Figure 2, lack of funding and resources, including port AMS, this was not reflected in the level of financial support
manpower and IT capabilities, were also common barriers to im for AMS activities. This was the case even in Japan (a high-income
plementing AMS programmes in Asian hospitals. Challenges re country), where there was no budgeted financial AMS support in
lated to lack of resources and manpower were considered 62.5% of 16 responding hospitals. Unsurprisingly, therefore, lack
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of funding and resources, including adequate manpower, IT and and India. Results from the survey by Lee et al. also indicate
funding, were commonly identified as posing challenges for AMS that such interventions were not always implemented in Asia–
programmes. To help overcome funding gaps, hospital adminis Pacific hospitals.3 Formulary restriction and pre-authorization is
trators need to be provided with a credible business case to per likely to be less labour-intensive than prospective audit and feed
suade them that funding an AMS programme is beneficial to the back, and can be implemented on a small scale by evaluating
hospital.19,25 It is recommended that programmes start small antibiotic usage patterns and resistance trends.19 Interventions
and build capacity over time, gradually introducing AMS interven targeted at a single antibiotic agent or class thought to be mis
tions by hospital unit or ward.19 used may be more practical rather than wide-ranging formulary
Once formal approval and support have been obtained from restriction in many resource-limited Asian hospitals.19,39–41
hospital administration, an AMS team, ideally including an ID spe However, prospective audit and feedback is inherently better sui
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As well as being potentially susceptible to nonresponse bias, A summary of our findings has been presented at IDWeek 2021 and
particularly in countries with response rates <60% (India, published in Open Forum Infect Dis 2021; 8: S57–8 as part of the
Indonesia, Philippines, Taiwan), our results may have been influ IDWeek abstracts.
enced by reliance on data reported by staff involved in the hos
pital AMS programmes. No pilot testing was performed to
validate the survey questions. Funding
In addition to differences in AMS programmes between coun This study was supported by an unrestricted educational grant from
tries, there are also large differences between facilities within Pfizer, Inc. to the Infection Control Society of Taiwan (grant no.
countries.45 Another potential limitation of our study pertains 57186265). The sponsor had no role in the preparation, review or approval
to potential over-representation of relatively well-resourced ter of the manuscript or in the decision to submit for publication.
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America and the Society for Healthcare Epidemiology of America guide 2021.e07377
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stewardship. Clin Infect Dis 2007; 44: 159–77. https://doi.org/10.1086/ microbial stewardship programs conducted by the Japanese Society of
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12 Baur D, Gladstone BP, Burkert F et al. Effect of antibiotic stewardship 1016/j.jiac.2018.11.001
on the incidence of infection and colonisation with antibiotic-resistant 28 Moriyama Y, Ishikane M, Kusama Y et al. Nationwide cross-sectional
bacteria and Clostridium difficile infection: a systematic review and me study of antimicrobial stewardship and antifungal stewardship programs
taanalysis. Lancet Infect Dis 2017; 17: 990–1001. https://doi.org/10. in inpatient settings in Japan. BMC infect Dis 2021; 21: 355. https://doi.org/
1016/S1473-3099(17)30325-0 10.1186/s12879-021-06035-5
13 Davey P, Brown E, Charani E. Interventions to improve antibiotic pre 29 Mubarak N, Khan AS, Zahid T et al. Assessment of adherence to the
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