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Antimicrobial stewardship for acute-care hospitals: An Asian perspective

  • Anucha Apisarnthanarak (a1), Andrea Lay-Hoon Kwa (a2) (a3) (a4), Cheng-Hsun Chiu (a5), Suresh Kumar (a6), Le Thi Anh Thu (a7), Ban Hock Tan (a8), Zhiyong Zong (a9), Yin Ching Chuang (a10) (a11), Anis Karuniawati (a12) (a13), Maria Fe Tayzon (a14) (a15), Thomas Man-Kit So (a16) and Lance R. Peterson (a17) (a18)...


Inappropriate use of antibiotics is contributing to a serious antimicrobial resistance problem in Asian hospitals. Despite resource constraints in the region, all Asian hospitals should implement antimicrobial stewardship (AMS) programs to optimize antibiotic treatment, improve patient outcomes, and minimize antimicrobial resistance. This document describes a consensus statement from a panel of regional experts to help multidisciplinary AMS teams design programs that suit the needs and resources of their hospitals. In general, AMS teams must decide on appropriate interventions (eg, prospective audit and/or formulary restriction) for their hospital, focusing on the most misused antibiotics and problematic multidrug-resistant organisms. This focus is likely to include carbapenem use with the goal to reduce carbapenem-resistant gram-negative bacteria. Rather than initially trying to introduce a comprehensive, hospital-wide AMS program, it would be practical to begin by pilot testing a simple program based on 1 achievable core intervention for the hospital. AMS team members must work together to determine the most suitable AMS interventions to implement in their hospitals and how best to put them into practice. Continuous monitoring and feedback of outcomes to the AMS teams, hospital administration, and prescribers will enhance sustainability of the AMS programs.


Corresponding author

Author for correspondence: Anucha Apisarnthanarak, Division of Infectious Diseases, Faculty of Medicine, Thammasat University Hospital, Pathumthani, Thailand 12120. E-mail:


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1. O’Neill, J. Tackling drug-resistant infections globally: final report and recommendations. Review on Antimicrobial Resistance website. paper_with cover.pdf. Published May 2016. Accessed November 15, 2017.
2. Antimicrobial resistance in the Western Pacific Region: a review of surveillance and health systems response, 2015. World Health Organization website. Published 2015. Accessed November 15, 2017.
3. Kang, C-I, Song, J-H. Antimicrobial resistance in Asia: current epidemiology and clinical implications. Infect Chemother 2013;45:2231.
4. Lai, C-C, Lee, K, Xiao, Y, et al. High burden of antimicrobial drug resistance in Asia. J Glob Antimicrob Resist. 2014;2:141147.
5. Action agenda for antimicrobial resistance in the Western Pacific Region, 2015. World Health Organization website. Published 2015. Accessed November 15, 2017.
6. Hsu, L-Y, Apisarnthanarak, A, Khan, E, Suwantarat, N, Ghafur, A, Tambyah, PA. Carbapenem-resistant Acinetobacter baumannii and Enterobacteriaceae in South and Southeast Asia. Clin Microbiol Rev 2017;30:122.
7. Suwantarat, N, Carroll, KC. Epidemiology and molecular characterization of multidrug-resistant gram-negative bacteria in Southeast Asia. Antimicrob Resist Infect Control 2016;5:15.
8. Barlam, TF, Cosgrove, SE, Abbo, LM, et al. Implementing an antibiotic stewardship program: guidelines by the Infectious Diseases Society of America and the Society for Healthcare Epidemiology of America. Clin Infect Dis 2016;62:e51e77.
9. Howard, P, Pulcini, C, Levy Hara, G, et al. An international cross-sectional survey of antimicrobial stewardship programmes in hospitals. J Antimicrob Chemother 2015;70:12451255.
10. Sing, DYF, Boo, YL, Mukhlis, R, Chin, PW, Hoo, FK. Antimicrobial stewardship program in a Malaysian district hospital: first year experience. Pakistan J Med Sci 2016;32:9991004.
11. Teng, CB, Lee, W, Yeo, CL, et al. Guidelines for antimicrobial stewardship training and practice. Ann Acad Med Singapore 2012;41:2934.
12. Tiong, JJL, Loo, JSE, Mai, C-W. Global antimicrobial stewardship: a closer look at the formidable implementation challenges. Front Microbiol 2016;7:1860.
13. Wertheim, HFL, Chandna, A, Vu, PD, et al. Providing impetus, tools, and guidance to strengthen national capacity for antimicrobial stewardship in Viet Nam. PLoS Med 2013;10:e1001429.
14. Antimicrobial stewardship: systems and processes for effective antimicrobial medicine use, August 2015. National Institute for Health and Care Excellence (NICE) website. Published 2015. Accessed November 15, 2017.
15. Pollack, LA, Srinivasan, A. Core elements of hospital antibiotic stewardship programs from the Centers for Disease Control and Prevention. Clin Infect Dis 2014;59 Suppl 3:S97S100.
16. Baur, D, Gladstone, BP, Burkert, F, et al. Effect of antibiotic stewardship on the incidence of infection and colonisation with antibiotic-resistant bacteria and Clostridium difficile infection: a systematic review and meta-analysis. Lancet Infect Dis 2017;17:9901001.
17. Honda, H, Ohmagari, N, Tokuda, Y, Mattar, C, Warren, DK. Antimicrobial stewardship in inpatient settings in the Asia Pacific Region: a systematic review and meta-analysis. Clin Infect Dis 2017;64:S119S126.
18. Schuts, EC, Hulscher, MEJL, Mouton, JW, et al. Current evidence on hospital antimicrobial stewardship objectives: a systematic review and meta-analysis. Lancet Infect Dis 2016;16:847856.
19. Levy Hara, G. Antimicrobial stewardship in hospitals: Does it work and can we do it? J Glob Antimicrob Resist 2014;2:16.
20. Nguyen, K Van, Thi Do, NT, Chandna, A, et al. Antibiotic use and resistance in emerging economies: a situation analysis for Viet Nam. BMC Public Health 2013;13:1158.
21. Wang, L, Zhang, X, Liang, X, Bloom, G. Addressing antimicrobial resistance in China: policy implementation in a complex context. Global Health 2016;12:30.
22. Hadi, U, Keuter, M, van Asten, H, van den Broek, P, Study Group “Antimicrobial resistance in Indonesia: Prevalence and Prevention” (AMRIN). Optimizing antibiotic usage in adults admitted with fever by a multifaceted intervention in an Indonesian governmental hospital. Trop Med Int Health 2008;13:888899.
23. Om, C, Daily, F, Vlieghe, E, McLaughlin, JC, McLaws, M-L. “If it’s a broad spectrum, it can shoot better”: inappropriate antibiotic prescribing in Cambodia. Antimicrob Resist Infect Control 2016;5:58.
24. Dellit, TH, Owens, RC, McGowan, JE, et al. Infectious Diseases Society of America and the Society for Healthcare Epidemiology of America guidelines for developing an institutional program to enhance antimicrobial stewardship. Clin Infect Dis 2007;44:159177.
25. Doron, S, Davidson, LE. Antimicrobial stewardship. Mayo Clin Proc 2011;86:11131123.
26. Akpan, MR, Ahmad, R, Shebl, NA, Ashiru-Oredope, D. A review of quality measures for assessing the impact of antimicrobial stewardship programs in hospitals. Antibiotics 2016;5.
27. Davey, P, Marwick, CA, Scott, CL, et al. Interventions to improve antibiotic prescribing practices for hospital inpatients. Cochrane Database Syst Rev 2017;2:CD003543.
28. Karanika, S, Paudel, S, Grigoras, C, Kalbasi, A, Mylonakis, E. Systematic review and meta-analysis of clinical and economic outcomes from the implementation of hospital-based antimicrobial stewardship programs. Antimicrob Agents Chemother 2016;60:48404852.
29. Kim, J, Craft, DW, Katzman, M. Building an Antimicrobial stewardship program: cooperative roles for pharmacists, infectious diseases specialists, and clinical microbiologists. Lab Med 2015;46:e65e71.
30. Waters, CD. Pharmacist-driven antimicrobial stewardship program in an institution without infectious diseases physician support. Am J Health Syst Pharm 2015;72:466468.
31. Duguid, M, Cruickshank, M, eds. Antimicrobial stewardship in Australian hospitals 2011. Australian Commission on Safety and Quality in Health Care website. Published 2011. Accessed November 15, 2017.
32. Wu, C-T, Chen, C-L, Lee, H-Y, et al. Decreased antimicrobial resistance and defined daily doses after implementation of a clinical culture-guided antimicrobial stewardship program in a local hospital. J Microbiol Immunol Infect 2017;50:846856.
33. Apisarnthanarak, A, Lapcharoen, P, Vanichkul, P, Srisaeng-Ngoen, T, Mundy, LM. Design and analysis of a pharmacist-enhanced antimicrobial stewardship program in Thailand. Am J Infect Control 2015;43:956959.
34. Pulcini, C, Botelho-Nevers, E, Dyar, OJ, Harbarth, S. The impact of infectious disease specialists on antibiotic prescribing in hospitals. Clin Microbiol Infect 2014;20:963972.
35. Schmitt, S, McQuillen, DP, Nahass, R, et al. Infectious diseases specialty intervention is associated with decreased mortality and lower healthcare costs. Clin Infect Dis 2014;58:2228.
36. Kanter, G, Connelly, NR, Fitzgerald, J. A system and process redesign to improve perioperative antibiotic administration. Anesth Analg 2006;103:15171521.
37. Xiao, Y, Zhang, J, Zheng, B, Zhao, L, Li, S, Li, L. Changes in Chinese policies to promote the rational use of antibiotics. PLoS Med 2013;10:e1001556.
38. Loo, LW, Liew, YX, Lee, W, Chlebicki, P, Kwa, AL-H. Impact of antimicrobial stewardship program (ASP) on outcomes in patients with acute bacterial skin and skin structure infections (ABSSSIs) in an acute tertiary care hospital. Infect Dis Ther 2015;4:1525.
39. Liew, YX, Lee, W, Cai, YY, et al. Utility and safety of procalcitonin in an antimicrobial stewardship program (ASP) in patients with malignancies. Eur J Clin Microbiol Infect Dis. 2012;31:30413046.
40. Gupta, K, Hooton, TM, Naber, KG, et al. International clinical practice guidelines for the treatment of acute uncomplicated cystitis and pyelonephritis in women: a 2010 update by the Infectious Diseases Society of America and the European Society for Microbiology and Infectious Diseases. Clin Infect Dis 2011;52:e103e120.
41. Kalil, AC, Metersky, ML, Klompas, M, et al. Management of adults with hospital-acquired and ventilator-associated pneumonia: 2016 clinical practice guidelines by the Infectious Diseases Society of America and the American Thoracic Society. Clin Infect Dis 2016;63:e61e111.
42. Lipsky, BA, Berendt, AR, Cornia, PB, et al. 2012 Infectious Diseases Society of America clinical practice guideline for the diagnosis and treatment of diabetic foot infections. Clin Infect Dis 2012;54:e132e173.
43. Stevens, DL, Bisno, AL, Chambers, HF, et al. Practice guidelines for the diagnosis and management of skin and soft tissue infections: 2014 update by the Infectious Diseases Society of America. Clin Infect Dis 2014;59:e10e52.
44. Falagas, ME, Matthaiou, DK, Bliziotis, IA. The role of aminoglycosides in combination with a beta-lactam for the treatment of bacterial endocarditis: a meta-analysis of comparative trials. J Antimicrob Chemother 2006;57:639647.
45. Bliziotis, IA, Samonis, G, Vardakas, KZ, Chrysanthopoulou, S, Falagas, ME. Effect of aminoglycoside and beta-lactam combination therapy versus beta-lactam monotherapy on the emergence of antimicrobial resistance: a meta-analysis of randomized, controlled trials. Clin Infect Dis 2005;41:149158.
46. Paul, M, Dickstein, Y, Schlesinger, A, Grozinsky-Glasberg, S, Soares-Weiser, K, Leibovici, L. Beta-lactam versus beta-lactam-aminoglycoside combination therapy in cancer patients with neutropenia. Cochrane Database Syst Rev 2013:CD003038 .
47. Paul, M, Lador, A, Grozinsky-Glasberg, S, Leibovici, L. Beta lactam antibiotic monotherapy versus beta lactam-aminoglycoside antibiotic combination therapy for sepsis. Cochrane Database Syst Rev 2014;28:CD003344.
48. Tamma, PD, Cosgrove, SE, Maragakis, LL. Combination therapy for treatment of infections with gram-negative bacteria. Clin Microbiol Rev 2012;25:450470.
49. Falagas, ME, Matthaiou, DK, Karveli, EA, Peppas, G. Meta-analysis: randomized controlled trials of clindamycin/aminoglycoside vs. beta-lactam monotherapy for the treatment of intra-abdominal infections. Aliment Pharmacol Ther 2007;25:537556.
50. Austin, DJ, Kristinsson, KG, Anderson, RM. The relationship between the volume of antimicrobial consumption in human communities and the frequency of resistance. Proc Natl Acad Sci U S A 1999;96:11521156.
51. Peterson, LR, Samia, NI, Skinner, AM, Chopra, A, Smith, B. Antimicrobial stewardship lessons from mupirocin use and resistance in methicillin-resitant Staphylococcus aureus . Open Forum Infect Dis 2017;4:ofx093.
52. Sandiumenge, A, Lisboa, T, Gomez, F, Hernandez, P, Canadell, L, Rello, J. Effect of antibiotic diversity on ventilator-associated pneumonia caused by ESKAPE organisms. Chest 2011;140:643651.
53. Sandiumenge, A, Diaz, E, Rodriguez, A, et al. Impact of diversity of antibiotic use on the development of antimicrobial resistance. J Antimicrob Chemother 2006;57:11971204.
54. Teo, J, Kwa, ALH, Loh, J, Chlebicki, MP, Lee, W. The effect of a whole-system approach in an antimicrobial stewardship programme at the Singapore General Hospital. Eur J Clin Microbiol Infect Dis 2012;31:947955.
55. Apisarnthanarak, A, Danchaivijitr, S, Khawcharoenporn, T, et al. Effectiveness of education and an antibiotic-control program in a tertiary care hospital in Thailand. Clin Infect Dis 2006;42:768775.
56. Song, YJ, Kim, M, Huh, S, et al. Impact of an antimicrobial stewardship program on unnecessary double anaerobic coverage prescription. Infect Chemother 2015;47:111116.
57. Teng, CB, Ng, TM, Tan, MW, et al. Safety and effectiveness of improving carbapenem use via prospective review and feedback in a multidisciplinary antimicrobial stewardship programme. Ann Acad Med Singapore 2015;44:1925.
58. Lew, KY, Ng, TM, Tan, M, et al. Safety and clinical outcomes of carbapenem de-escalation as part of an antimicrobial stewardship programme in an ESBL-endemic setting. J Antimicrob Chemother 2015;70:12191225.
59. Levy Hara, G, Kanj, SS, Pagani, L, et al. Ten key points for the appropriate use of antibiotics in hospitalised patients: a consensus from the Antimicrobial Stewardship and Resistance Working Groups of the International Society of Chemotherapy. Int J Antimicrob Agents 2016;48:239246.
60. Cotta, MO, Roberts, JA, Lipman, J. Antibiotic dose optimization in critically ill patients. Med Intensiva 2015;39:563572.
61. Morency-Potvin, P, Schwartz, DN, Weinstein, RA. Antimicrobial Stewardship: How the microbiology laboratory can right the ship. Clin Microbiol Rev 2017;30:381407.
62. Liew, YX, Lee, W, Tay, D, et al. Prospective audit and feedback in antimicrobial stewardship: is there value in early reviewing within 48 h of antibiotic prescription? Int J Antimicrob Agents 2015;45:168173.
63. Baysari, MT, Lehnbom, EC, Li, L, Hargreaves, A, Day, RO, Westbrook, JI. The effectiveness of information technology to improve antimicrobial prescribing in hospitals: a systematic review and meta-analysis. Int J Med Inform 2016;92:1534.
64. Cheon, S, Kim, M-J, Yun, S-J, Moon, JY, Kim, Y-S. Controlling endemic multidrug-resistant Acinetobacter baumannii in intensive care units using antimicrobial stewardship and infection control. Korean J Intern Med 2016;31:367374.
65. Guo, W, He, Q, Wang, Z, et al. Influence of antimicrobial consumption on gram-negative bacteria in inpatients receiving antimicrobial resistance therapy from 2008–2013 at a tertiary hospital in Shanghai, China. Am J Infect Control 2015;43:358364.
66. Chen, I-L, Lee, C-H, Su, L-H, Wang, Y-CL, Liu, J-W. Effects of implementation of an online comprehensive antimicrobial-stewardship program in ICUs: a longitudinal study. J Microbiol Immunol Infect 2018;51:5563.
67. Chow, AL, Ang, A, Chow, CZ, et al. Implementation hurdles of an interactive, integrated, point-of-care computerised decision support system for hospital antibiotic prescription. Int J Antimicrob Agents 2016;47:132139.
68. Chow, A, Lye, DCB, Arah, OA. Psychosocial determinants of physicians’ acceptance of recommendations by antibiotic computerised decision support systems: a mixed methods study. Int J Antimicrob Agents 2015;45:295304.
69. Apisarnthanarak, A, Pinitchai, U, Thongphubeth, K, et al. A multifaceted intervention to reduce pandrug-resistant Acinetobacter baumannii colonization and infection in 3 intensive care units in a Thai tertiary care center: a 3-year study. Clin Infect Dis 2008;47:760767.
70. Nagel, JL, Kaye, KS, LaPlante, KL, Pogue, JM. Antimicrobial stewardship for the infection control practitioner. Infect Dis Clin N Am 2016;30:771784.
71. Apisarnthanarak, A, Ratz, D, Greene, MT, Khawcharoenporn, T, Weber, DJ, Saint, S. National survey of practices to prevent health care-associated infections in Thailand: the role of prevention bundles. Am J Infect Control 2017;45:805810.
72. Zhou, W-J, Luo, Z-N, Tang, C-M, Zou, X-X, Zhao, L, Fang, P-Q. Is there an improvement of antibiotic use in China? Evidence from the usage analysis of combination antibiotic therapy for type I incisions in 244 hospitals. J Huazhong Univ Sci Technolog Med Sci 2016;36:772779.
73. Zou, X, Fang, Z, Min, R, et al. Is nationwide special campaign on antibiotic stewardship program effective on ameliorating irrational antibiotic use in China? Study on the antibiotic use of specialized hospitals in China in 2011–2012. J Huazhong Univ Sci Technolog Med Sci 2014;34:456463.
74. Trivedi, KK, Kuper, K. Hospital antimicrobial stewardship in the nonuniversity setting. Infect Dis Clin N Am 2014;28:281289.
75. Ng, CK, Wu, TC, Chan, WM, et al. Clinical and economic impact of an antibiotics stewardship programme in a regional hospital in Hong Kong. Qual Saf Health Care 2008;17:387392.
76. Hou, D, Wang, Q, Jiang, C, Tian, C, Li, H, Ji, B. Evaluation of the short-term effects of antimicrobial stewardship in the intensive care unit at a tertiary hospital in China. PLoS One 2014;9:e101447.
77. Takesue, Y, Nakajima, K, Ichiki, K, et al. Impact of a hospital-wide programme of heterogeneous antibiotic use on the development of antibiotic-resistant Gram-negative bacteria. J Hosp Infect 2010;75:2832.
78. Chong, Y, Shimoda, S, Yakushiji, H, et al. Antibiotic rotation for febrile neutropenic patients with hematological malignancies: clinical significance of antibiotic heterogeneity. PLoS One 2013;8:e54190.
79. Shen, J, Sun, Q, Zhou, X, et al. Pharmacist interventions on antibiotic use in inpatients with respiratory tract infections in a Chinese hospital. Int J Clin Pharm 2011;33:929933.
80. Cheng, VC, To, KK, Li, IW, et al. Antimicrobial stewardship program directed at broad-spectrum intravenous antibiotics prescription in a tertiary hospital. Eur J Clin Microbiol Infect Dis 2009;28:14471456.
81. Shi, Q, Ding, F, Sang, R, Liu, Y, Yuan, H, Yu, M. Drug use evaluation of cefepime in the first affiliated hospital of Bengbu medical college: A retrospective and prospective analysis. BMC Infect Dis 2013;13:160.
82. Ikai, H, Morimoto, T, Shimbo, T, Imanaka, Y, Koike, K. Impact of postgraduate education on physician practice for community-acquired pneumonia. J Eval Clin Pract 2012;18:389395.
83. Lin, YS, Lin, IF, Yen, YF, et al. Impact of an antimicrobial stewardship program with multidisciplinary cooperation in a community public teaching hospital in Taiwan. Am J Infect Control 2013;41:10691072.
84. Apisarnthanarak, A, Bhooanusas, N, Yaprasert, A, Mundy, LM. Carbapenem de-escalation therapy in a resource-limited setting. Infect Control Hosp Epidemiol 2013;34:13101313.
85. Park, SM, Kim, HS, Jeong, YM, et al. Impact of intervention by an antimicrobial stewardship team on conversion from intravenous to oral fluoroquinolones. Infect Chemother 2017;49:3137.
86. Davies, J, Gordon, CL, Tong, SY, Baird, RW, Davis, JS. Impact of results of a rapid Staphylococcus aureus diagnostic test on prescribing of antibiotics for patients with clustered gram-positive cocci in blood cultures. J Clin Microbiol 2012;50:20562058.
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