The burden of antimicrobial resistance (AMR) is considerable in many low- and middle-income countries (LMICs), and it is important to describe the antimicrobial stewardship program (ASP) activities found in these countries and report their impact. Importantly, as these programs target prescribing behavior, the factors influencing prescription of antimicrobials must also be taken into account. This scoping review aimed to (1) describe hospital-based ASP activities, (2) report methods used to measure the impact of ASPs, and (3) explore factors influencing antimicrobial prescribing behavior in LMICs. PubMed was searched from database inception until April 2021. Factors influencing antimicrobial prescribing behavior were canvassed using the Capability-Opportunity-Motivation and Behavior framework. Most of ASP studies in LMICs were predominantly conducted in tertiary care and university-based hospitals. Audit of antimicrobial prescriptions with feedback and restrictive-based strategies was the main reported activity. Total antimicrobial consumption was the main method used to measure the impact of ASPs. Positive outcomes were observed for both clinical and microbiological outcomes; however, these were measured from nonrandomized controlled trials. Dominant factors identified through the behavioral framework were a limited awareness of AMR as a local problem, a perception that overprescription of antimicrobials had limited consequences and was mainly driven by a motivation to help improve patient outcomes. In addition, antimicrobial prescribing practices were largely influenced by existing hierarchy among prescribers. Our scoping review suggests that LMICs need to evaluate antimicrobial appropriateness as an added measure to assess impact. Furthermore, improvements in the access of microbiology and diagnostic facilities and ensuring ASP champions are recruited from senior prescribers will positively influence antimicrobial prescribing behavior, helping improve stewardship of antimicrobials in these countries.
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References
1.
World Health Organization. Global antimicrobial resistance surveillance system (GLASS) report: early implementation 2020. Geneva: World Health Organization; 2020.
2.
AslamB., WangW., ArshadM.I, et al.2018. Antibiotic resistance: a rundown of a global crisis. Infect. Drug Resist. 11:1645–1658.
3.
KhanM.S., Durrance-BagaleA., Legido-QuigleyH., et al.2019. ‘LMICs as reservoirs of AMR’: a comparative analysis of policy discourse on antimicrobial resistance with reference to Pakistan. Health Policy Plan, 34:178–187.
4.
LimC., TakahashiE., HongsuwanM., et al.2016. Epidemiology and burden of multidrug-resistant bacterial infection in a developing country. Elife, 5:e18082.
5.
TillotsonG.S., and ZinnerS.H.. 2017. Burden of antimicrobial resistance in an era of decreasing susceptibility. Expert Rev. Anti. Infect. Ther. 15:663–676.
6.
RobertsR.R., HotaB., AhmadI., et al.2009. Hospital and societal costs of antimicrobial-resistant infections in a Chicago Teaching Hospital: implications for antimicrobial stewardship. Clin. Infect. Dis. 49:1175–1184.
7.
MichaelidisC.I., FineM.J, LinC.J, et al.2016. The hidden societal cost of antibiotic resistance per antibiotic prescribed in the United States: an exploratory analysis. BMC Infect. Dis. 16:655.
8.
LeporeC., SilverL., TheuretzbacherU., ThomasJ., and VisiD.. 2019. The small-molecule antibiotics pipeline: 2014-2018. Nat. Rev. Drug Discov. 18:739.
9.
FrostI., CraigJ., JoshiJ., FaureK., and LaxminarayanR.. 2019. Access barriers to Antibiotics. Center for Disease Dynamics, Economics & Policy, Washington, DC.
10.
HeckerM.T., AronD.C, PatelN.P, LehmannM.K, and DonskeyC.J.. 2003. Unnecessary use of antimicrobials in hospitalized patients: current patterns of misuse with an emphasis on the antianaerobic spectrum of activity. Arch. Intern. Med. 163:972–978.
11.
National Centre for Antimicrobial Stewardship and Australian Commission on Safety and Quality in Health Care. 2018. Antimicrobial prescribing practice in Australian hospitals: results of the 2017 Hospital National Antimicrobial Prescribing Survey. ACSQHC, Sydney.
12.
McGowanJ.E.Jr, and GerdingD.N.. 1996. Does antibiotic restriction prevent resistance?. New Horiz. 4:370–376.
13.
Rennert-MayE., ChewD.S, ConlyJ., et al.2019. Clinical practice guidelines for creating an acute care hospital-based antimicrobial stewardship program: a systematic review. Am. J. Infect. Control. 47:979–993.
14.
DaveyP., MarwickC.A, ScottC.L, et al.2017. Interventions to improve antibiotic prescribing practices for hospital inpatients. Cochrane Database Syst Rev. 2:CD003543.
15.
BarlamT.F., CosgroveS.E, AbboL.M, et al.2016. Implementing an antibiotic stewardship program: guidelines by the Infectious Diseases Society of America and the Society for Healthcare Epidemiology of America. Clin. Infect. Dis. 62:e51–e77.
16.
KaranikaS., PaudelS., GrigorasC., KalbasiA., and MylonakisE.. 2016. Systematic review and meta-analysis of clinical and economic outcomes from the implementation of hospital-based antimicrobial stewardship programs. Antimicrob. Agents Chemother. 60:4840–4852.
17.
LeeC.F., CowlingB.J, FengS., et al.2018. Impact of antibiotic stewardship programmes in Asia: a systematic review and meta-analysis. J. Antimicrob. Chemother. 73:844–851.
18.
HondaH., OhmagariN., TokudaY., MattarC., and WarrenD.K.. 2017. Antimicrobial Stewardship in inpatient settings in the Asia Pacific Region: a systematic review and meta-analysis. Clin. Infect. Dis. 64,(suppl_2)::S119–S126.
19.
GoffD.A., KullarR., GoldsteinEJC, et al.2017. A global call from five countries to collaborate in antibiotic stewardship: united we succeed, divided we might fail. Lancet. Infect. Dis. 17:e56–e63.
20.
World Health Organization. 2015. Global Action Plan on Antimicrobial Resistance. WHO Press, Geneva.
21.
LorencattoF., CharaniE., SevdalisN., TarrantC., and DaveyP.. 2018. Driving sustainable change in antimicrobial prescribing practice: how can social and behavioural sciences help? J. Antimicrob. Chemother. 73:2613–2624.
22.
MichieS., van StralenM.M, and WestR.. 2011. The behaviour change wheel: a new method for characterising and designing behaviour change interventions. Implement. Sci. 6:42.
Morris, A.M. 2014. Antimicrobial Stewardship Programs: appropriate measures and metrics to study their impact. Curr. Treat Options Infect. Dis. 6:101–112.
28.
CaneJ., O'ConnorD., and MichieS.. 2012. Validation of the theoretical domains framework for use in behaviour change and implementation research. Implement. Sci. 7:37.
29.
GebretekleG.B., Haile MariamD., Abebe TayeW., et al.2020. Half of prescribed antibiotics are not needed: a pharmacist-led antimicrobial stewardship intervention and clinical outcomes in a referral hospital in Ethiopia. Front Public Health. 8:109.
30.
LesterR., HaighK., WoodA., et al.2020. Sustained reduction in third-generation cephalosporin usage in adult inpatients following introduction of an antimicrobial stewardship program in a large, urban hospital in Malawi. Clin. Infect. Dis. 71:e478–e486.
31.
TiwariS.A., GhonganeB.B, DaswaniB.R, and DabhadeS.S.. 2017. Restricted parenteral antibiotics usage policy in a tertiary care teaching hospital in India. J. Clin. Diagn. Res. 11:FC06-FC09.
32.
SinghS., MenonV.P, MohamedZ.U, et al.2018. Implementation and impact of an antimicrobial stewardship program at a tertiary care center in South India. Open Forum Infect. Dis. 6:ofy290.
33.
WattalC., KhannaS., GoelN., OberoiJ.K, and RaoB.K.. 2017. Antimicrobial prescribing patterns of surgical speciality in a tertiary care hospital in India: role of persuasive intervention for changing antibiotic prescription behaviour. Indian J. Med. Microbiol. 35:369–375.
34.
VermaM., ShafiqN., TripathyJ.P, et al.2019. Antimicrobial stewardship programme in a trauma centre of a tertiary care hospital in North India: effects and implementation challenges. J. Glob. Antimicrob. Resist. 17:283–290.
35.
NauriyalV., RaiS.M, JoshiR.D, et al.2020. Evaluation of an antimicrobial stewardship program for wound and burn care in three hospitals in Nepal. Antibiotics (Basel). 9:914.
36.
JoshiR.D., ZervosM., KaljeeL.M, et al.2019. Evaluation of a hospital-based post-prescription review and feedback pilot in Kathmandu, Nepal. Am. J. Trop. Med Hyg. 101:923–928.
37.
HussainK., KhanM.F, AmbreenG., et al.2020. An antibiotic stewardship program in a surgical ICU of a resource-limited country: financial impact with improved clinical outcomes. J. Pharm. Policy Pract. 13:69.
38.
HoşoğluS., EsenS., OzturkR., et al.2005. The effect of a restriction policy on the antimicrobial consumption in Turkey: a country-wide study. Eur. J. Clin. Pharmacol. 61:727–731.
39.
ApisarnthanarakA., DanchaivijitrS., KhawcharoenpornT., et al.2006. Effectiveness of education and an antibiotic-control program in a tertiary care hospital in Thailand. Clin. Infect. Dis. 42:768–775.
40.
ApisarnthanarakA., LapcharoenP., VanichkulP., Srisaeng-NgoenT., and MundyL.M.. 2015. Design and analysis of a pharmacist-enhanced antimicrobial stewardship program in Thailand. Am. J. Infect. Control. 43:956–959.
41.
BoylesT.H., WhitelawA., BamfordC., et al.2013. Antibiotic stewardship ward rounds and a dedicated prescription chart reduce antibiotic consumption and pharmacy costs without affecting inpatient mortality or re-admission rates. PLoS One, 8:e79747.
42.
DjordjevicZ.M., FolicM.M, and JankovicS.M.. 2017. Influence of regular reporting on local Pseudomonas aeruginosa and Acinetobacter spp. sensitivity to antibiotics on consumption of antibiotics and resistance patterns. J. Clin. Pharm. Ther. 42:585–590.
43.
BantarC., SartoriB., VescoE., et al.2003. A hospitalwide intervention program to optimize the quality of antibiotic use: impact on prescribing practice, antibiotic consumption, cost savings, and bacterial resistance. Clin. Infect. Dis. 37:180–186.
44.
HouD., WangQ., JiangC., TianC., LiH., and JiB.. 2014. Evaluation of the short-term effects of antimicrobial stewardship in the intensive care unit at a tertiary hospital in China. PLoS One, 9:e101447.
45.
MagedanzL., SilliprandiE.M, and dos SantosR.P.. 2012. Impact of the pharmacist on a multidisciplinary team in an antimicrobial stewardship program: a quasi-experimental study. Int. J. Clin. Pharm. 34:290–294.
46.
YusefD., HayajnehW.A, Bani IssaA., et al.2021. Impact of an antimicrobial stewardship programme on reducing broad-spectrum antibiotic use and its effect on carbapenem-resistant Acinetobacter baumannii (CRAb) in hospitals in Jordan. J. Antimicrob. Chemother. 76:516–523.
47.
ZhangD., CuiK., WangT., et al.2018. Trends in and correlations between antibiotic consumption and resistance of Staphylococcus aureus at a tertiary hospital in China before and after introduction of an antimicrobial stewardship programme. Epidemiol. Infect. 147:1–6.
48.
AltunsoyA., AypakC., AzapA., Ö. Ergönül, and BalıkI.. 2011. The impact of a nationwide antibiotic restriction program on antibiotic usage and resistance against nosocomial pathogens in Turkey. Int. J. Med. Sci. 8:339–344.
49.
Díaz-MadrizJ.P., Cordero-GarcíaE., Chaverri-FernándezJ.M, et al.2020. Impact of a pharmacist-driven antimicrobial stewardship program in a private hospital in Costa Rica. Rev. Panam Salud Publica. 44:e57.
50.
MoghniehR., AwadL., AbdallahD., et al.2020. Effect of a “handshake” stewardship program versus a formulary restriction policy on high-end antibiotic use, expenditure, antibiotic resistance, and patient outcome. J. Chemother. 32:368–384.
51.
ZhangZ.G., ChenF., and OuY.. 2017. Impact of an antimicrobial stewardship programme on antibiotic usage and resistance in a tertiary hospital in China. J. Clin. Pharm. Ther. 42:579–584.
52.
SulimanS.M., YousefB.A, and HamadelnilA.A.. 2020. Impact of guidelines implementation for the rational use of prophylactic antibiotics in elective cesarean sections at Elqutainah Teaching Hospital. J. Family Med. Prim. Care. 9:162–167.
53.
SwamyA., SoodR., KapilA., et al.2019. Antibiotic stewardship initiative in a Medicine unit of a tertiary care teaching hospital in India: a pilot study. Indian J. Med. Res. 150:175–185.
54.
AbubakarU., Syed SulaimanS.A, and AdesiyunA.G.. 2019. Impact of pharmacist-led antibiotic stewardship interventions on compliance with surgical antibiotic prophylaxis in obstetric and gynecologic surgeries in Nigeria. PLoS One, 14:e0213395.
55.
AhmedS.A., KumarA., SethiP., KapilA., PandeyR.M, and WigN.. 2018. Effectiveness of education and antibiotic control programme at All India Institute of Medical Sciences, New Delhi. Natl. Med. J. India, 31:262–267.
56.
RupaliP., PalanikumarP., ShanthamurthyD., et al.2019. Impact of an antimicrobial stewardship intervention in India: evaluation of post-prescription review and feedback as a method of promoting optimal antimicrobial use in the intensive care units of a tertiary-care hospital. Infect. Control Hosp. Epidemiol. 40:512–519.
57.
MurniI.K., DukeT., KinneyS., DaleyA.J, and SoenartoY.. 2015. Reducing hospital-acquired infections and improving the rational use of antibiotics in a developing country: an effectiveness study. Arch. Dis. Child, 100:454–459.
58.
MitchellK.F., SafdarN., and AbadC.L.. 2019. Evaluating carbapenem restriction practices at a private hospital in Manila, Philippines as a strategy for antimicrobial stewardship. Arch. Public Health, 77:31.
59.
El-SokkaryR.H., NegmE.M, OthmanH.A, TawfeekM.M, and MetwallyW.S.. 2020. Stewardship actions for device associated infections: an intervention study in the emergency intensive care unit. J. Infect. Public Health, 13:1927–1931.
60.
SaiedT., HafezS.F, KandeelA., et al.2015. Antimicrobial stewardship to optimize the use of antimicrobials for surgical prophylaxis in Egypt: a multicenter pilot intervention study. Am. J. Infect. Control. 43:e67–e71.
61.
OpondoC., AyiekoP., NtoburiS., et al.2011. Effect of a multi-faceted quality improvement intervention on inappropriate antibiotic use in children with non-bloody diarrhoea admitted to district hospitals in Kenya. BMC Pediatr. 11:109.
62.
WangH., WangH., YuX., et al.2019. Impact of antimicrobial stewardship managed by clinical pharmacists on antibiotic use and drug resistance in a Chinese hospital, 2010-2016: a retrospective observational study. BMJ Open, 9:e026072.
63.
Dos SantosR.P., DalmoraC.H, LukasewiczS.A, et al.2019. Antimicrobial stewardship through telemedicine and its impact on multi-drug resistance. J. Telemed. Telecare, 25:294–300.
64.
ZhangZ.G., ChenF., and ChenJ.Z.. 2018. Introducing an antibiotic stewardship program in a pediatric center in China. World J. Pediatr. 14:274–279.
65.
MoghniehR., AbdallahD., AwadL., et al.2020. The effect of an antibiotic stewardship program on tigecycline use in a Tertiary Care Hospital, an intervention study. Ann. Clin. Microbiol. Antimicrob. 19:35.
66.
BrinkA.J., MessinaA.P, FeldmanC., et al.2016. Antimicrobial stewardship across 47 South African hospitals: an implementation study. Lancet. Infect. Dis. 16:1017–1025.
67.
Ertürk ŞengelB., BilginH., B. Ören Bilgin, et al. 2019. The need for an antibiotic stewardship program in a hospital using a computerized pre-authorization system. Int. J. Infect. Dis. 82:40–43.
68.
BhallaN., HusseinN., AtariM., et al.2016. Introducing an antibiotic stewardship program in a humanitarian surgical hospital. Am. J. Infect. Control. 44:1381–1384.
69.
ChautrakarnS., AnugulruengkittS., PuthanakitT., RattananupongT., and HiransuthikulN.. 2019. Impact of a prospective audit and feedback Antimicrobial Stewardship Program in pediatric units in tertiary care teaching hospital in Thailand. Hosp. Pediatr. 9:851–858.
70.
LibertinC.R., WatsonS.H, TillettW.L, and PetersonJ.H.. 2017. Dramatic effects of a new antimicrobial stewardship program in a rural community hospital. Am. J. Infect. Control. 45:979–982.
71.
LiZ., ChengB., ZhangK., et al.2017. Pharmacist-driven antimicrobial stewardship in intensive care units in East China: a multicenter prospective cohort study. Am. J. Infect. Control. 45:983–989.
72.
ZhouY., MaL.Y, ZhaoX., TianS.H, SunL.Y, and CuiY.M.. 2015. Impact of pharmacist intervention on antibiotic use and prophylactic antibiotic use in urology clean operations. J. Clin. Pharm. Ther. 40:404–408.
73.
MaX., XieJ., YangY., et al.2016. Antimicrobial stewardship of Chinese ministry of health reduces multidrug-resistant organism isolates in critically ill patients: a pre-post study from a single center. BMC Infect. Dis. 16:704.
74.
MessinaA.P., van den BerghD., and GoffD.A.. 2015. Antimicrobial Stewardship with pharmacist intervention improves timeliness of antimicrobials across thirty-three hospitals in South Africa. Infect. Dis. Ther. 4,(Suppl 1)::5–14.
75.
SzeW.T., and KongM.C.. 2018. Impact of printed antimicrobial stewardship recommendations on early intravenous to oral antibiotics switch practice in district hospitals. Pharm. Pract. (Granada). 16:855.
76.
GongS., QiuX., SongY., et al.2016. Effect of financially punished audit and feedback in a pediatric setting in China, within an Antimicrobial Stewardship Program, and as part of an international accreditation process. Front Public Health, 4:99.
77.
MustafaF., KoekemoerL.A, GreenR.J, TurnerA.C, BeckerP., and van BiljonG.. 2020. Successful antibiotic stewardship in hospitalised children in a developing nation. J. Glob. Antimicrob. Resist. 23:217–220.
78.
JunaidE., JenkinsL., SwanepoelH., NorthZ., and GouldT.. 2018. Antimicrobial stewardship in a rural regional hospital - growing a positive culture. S. Afr. Med. J. 108:546–550.
79.
AntonelloV.S., CunegattoM.C, RosinE.T, et al.2019. The use of mobile educational tools to improve antimicrobial prescription for the treatment of acute pyelonephritis in pregnancy: a retrospective cross-sectional study. Rev. Bras. Ginecol. Obstet. 41:97–101.
80.
SirijatuphatR., NookeuP., and ThamlikitkulV.. 2020. Effectiveness of implementing a locally developed antibiotic use guideline for community-acquired cellulitis at a large tertiary care university hospital in Thailand. Open Forum. Infect. Dis. 7:ofaa411.
81.
DuY., LiJ., WangX., et al.2020. Impact of a multifaceted pharmacist-led intervention on antimicrobial stewardship in a gastroenterology ward: a segmented regression analysis. Front Pharmacol. 11:442.
82.
van den BerghD., MessinaA.P., GoffD.A., et al. 2020. A pharmacist-led prospective antibiotic stewardship intervention improves compliance to community-acquired pneumonia guidelines in 39 public and private hospitals across South Africa. Int. J. Antimicrob. Agents. 56:106189.
83.
LiX., ChenH., ZhuS., et al.2018. Efficacy and feasibility of a collaborative multidisciplinary program for antibiotic prophylaxis in clean wound surgery. Int. J. Clin. Pharm. 40:150–159.
84.
ZhouL., MaJ., GaoJ., ChenS., and BaoJ.. 2016. Optimizing prophylactic antibiotic practice for cardiothoracic surgery by pharmacists' effects. Medicine (Baltimore), 95:e2753.
85.
AzapA., P. TopçuoğluA, Yeşilkaya, et al. 2005. The effect of a nationwide antibiotic restriction policy on antibiotic usage in a stem cell transplantation unit. Turk. J. Haematol. 22:87–90.
86.
YangP., JiangS.P, and LuX.Y.. 2017. Effectiveness of continuous improvement by a clinical pharmacist-led guidance team on the prophylactic antibiotics usage rationality in intervention procedure at a Chinese tertiary teaching hospital. Ther. Clin. Risk Manag. 13:469–476.
87.
ZhangD., CuiK., LuW., et al.2019. Evaluation of carbapenem use in a tertiary hospital: antimicrobial stewardship urgently needed. Antimicrob. Resist. Infect. Control, 8:5.
88.
RodriguesR.M., FontesA.M, ManteseO.C, MartinsR.S, and JorgeM.T.. 2013. Impact of an intervention in the use of sequential antibiotic therapy in a Brazilian university hospital. Rev. Soc. Bras. Med. Trop. 46:50–54.
89.
BaoL., PengR., WangY., et al. 2015. Significant reduction of antibiotic consumption and patients' costs after an action plan in China, 2010-2014. PLoS One 10: e011, 8868.
90.
ZouX.X., FangZ., MinR., et al.2014. 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. 34:456–463.
91.
XiaoY., ShenP., ZhengB., ZhouK., LuoQ., and LiL.. 2020. Change in antibiotic use in secondary and tertiary hospitals nationwide after a national antimicrobial stewardship campaign was launched in China, 2011–2016: an observational study. J. Infect. Dis. 221,(Suppl 2)::S148–S155.
92.
WeiX., YinJ., WalleyJ.D, et al.2017. Impact of China's essential medicines scheme and zero-mark-up policy on antibiotic prescriptions in county hospitals: a mixed methods study. Trop. Med. Int. Health, 22:1166–1174.
93.
MurniI.K., DukeT., KinneyS., et al. 2020. Multifaceted interventions for healthcare-associated infections and rational use of antibiotics in a low-to-middle-income country: can they be sustained?. PLoS One, 15:e0234233.
94.
GarciaC., LlamoccaL.P, GarciaK., et al.2011. Knowledge, attitudes and practice survey about antimicrobial resistance and prescribing among physicians in a hospital setting in Lima, Peru. BMC Clin. Pharmacol. 11:18.
95.
AberaB., KibretM., and MuluW.. 2014. Knowledge and beliefs on antimicrobial resistance among physicians and nurses in hospitals in Amhara Region, Ethiopia. BMC Pharmacol. Toxicol. 15:26.
96.
GebretekleG.B., Haile MariamD., AbebeW., et al.2018. Opportunities and barriers to implementing antibiotic stewardship in low and middle-income countries: lessons from a mixed-methods study in a tertiary care hospital in Ethiopia. PLoS One, 13:e0208447.
97.
QuetF., VliegheE., LeyerC., et al.2015. Antibiotic prescription behaviours in Lao People's Democratic Republic: a knowledge, attitude and practice survey. Bull World Health Organ. 93:219–227.
98.
HoqueR., MostafaA., and HaqueM.. 2015. Intern doctors' views on the current and future antibiotic resistance situation of Chattagram Maa O Shishu Hospital Medical College, Bangladesh. Ther. Clin. Risk Manag. 11:1177–1185.
99.
FathiI., SamehO., Abu-OlloM., et al.2017. Knowledge, attitudes, and beliefs regarding antimicrobial therapy and resistance among physicians in Alexandria University teaching hospitals and the associated prescription habits. Microb. Drug Resist. 23:71–78.
100.
SaleemZ., HassaliM.A, GodmanB., HashmiF.K, and SaleemF.. 2019. Antimicrobial prescribing and determinants of antimicrobial resistance: a qualitative study among physicians in Pakistan. Int. J. Clin. Pharm. 41:1348–1358.
101.
OmC., VliegheE., McLaughlinJ.C, DailyF., McLawsM.L. 2016. Antibiotic prescribing practices: a national survey of Cambodian physicians. Am. J. Infect. Control. 44:1144–1148.
102.
ShahidA., IftikharF., ArshadM.K, et al.2017. Knowledge and attitude of physicians about antimicrobial resistance and their prescribing practices in Services hospital, Lahore, Pakistan. J. Pak. Med. Assoc. 67:968.
103.
BabatolaA.O., FadareJ.O, OlatunyaO.S, et al.2021. Addressing antimicrobial resistance in Nigerian hospitals: exploring physicians prescribing behavior, knowledge, and perception of antimicrobial resistance and stewardship programs. Expert Rev. Anti. Infect. Ther. 19:537–546.
104.
AtifM., IhsanB., MalikI., et al.2021. Antibiotic stewardship program in Pakistan: a multicenter qualitative study exploring medical doctors' knowledge, perception and practices. BMC Infect. Dis. 21:374.
105.
MathewP., RanjalkarJ., and ChandyS.J.. 2020. Challenges in implementing antimicrobial stewardship programmes at secondary level hospitals in India: an exploratory study. Front Public Health, 8:493904.
106.
KagoyaE.K., RoyenK.V, WaakoP., et al.2021. Experiences and views of healthcare professionals on the prescription of antibiotics in Eastern Uganda: a qualitative study. J. Glob. Antimicrob. Resist. 25:66–71.
107.
TarrantC., KrockowE.M, W.NakkawitaM.I.D, et al.2020. Moral and contextual dimensions of “inappropriate” antibiotic prescribing in secondary care: a three-country interview study. Front Sociol. 5:7.
108.
TarrantC., ColmanA.M, JenkinsD.R, et al.2021. Drivers of broad-spectrum antibiotic overuse across diverse hospital contexts-a qualitative study of prescribers in the UK, Sri Lanka and South Africa. Antibiotics (Basel). 10:94.
109.
ReynoldsL., and McKeeM.. 2009. Factors influencing antibiotic prescribing in China: an exploratory analysis. Health Policy. 90:32–36.
110.
SinghS., MendelsonM., SurendranS., et al. 2021. Investigating infection management and antimicrobial stewardship in surgery: a qualitative study from India and South Africa. Clin. Microbiol. Infect. S1198-743X(20)30773-4. [Epub ahead of print]; DOI: 10.1016/j.cmi.2020.12.013.
111.
AhmedH., BhimaniS., KhanumI., et al.2020. Knowledge, attitude and perception survey of doctors regarding antibiotic use and resistance in Karachi, Pakistan. J. Pak. Med. Assoc. 70:1023–1028.
112.
GebrehiwotZ., and TadiwosY.. 2020. Knowledge and beliefs of health care professionals towards antimicrobial resistance in Hiwot Fana Specialized University Hospital, in Harar, Ethiopia. Infect. Drug Resist. 13:2027–2035.
113.
SayeghN., HallitS., HallitR., SalehN., and ZeidanR.K.. 2021. Physicians' attitudes on the implementation of an antimicrobial stewardship program in Lebanese hospitals. Pharm. Pract. (Granada). 19:2192.
114.
OgunleyeO.O., FadareJ.O, Yinka-OgunleyeA.F, Anand ParamadhasB.D, and GodmanB.. 2019. Determinants of antibiotic prescribing among doctors in a Nigerian urban tertiary hospital. Hosp. Pract. (1995). 47:53–58.
115.
HayatK., RosenthalM., GillaniA.H, et al.2019. Perspective of Pakistani physicians towards hospital Antimicrobial Stewardship Programs: a multisite exploratory qualitative study. Int. J. Environ. Res. Public Health, 16:1565.
116.
KalungiaA.C., MwambulaH., MunkombweD., et al.2019. Antimicrobial stewardship knowledge and perception among physicians and pharmacists at leading tertiary teaching hospitals in Zambia: implications for future policy and practice. J. Chemother. 31:378–387.
117.
HayatK., RosenthalM., GillaniA.H, et al. 2020. Perspective of key healthcare professionals on antimicrobial resistance and stewardship programs: a multicenter cross-sectional study from Pakistan. Front. Pharmacol. 10:, 1520.
118.
MulaC.T., MiddletonL., HumanN., and VargaC.. 2018. Assessment of factors that influence timely administration of initial antibiotic dose using collaborative process mapping at a referral hospital in Malawi: a case study of pneumonia patients. BMC Infect. Dis. 18:697.
119.
RaviN., LahaA., HmarL., et al.2017. Exploring the prescribing behaviours and the mind of antibiotic prescribers is critical for a successful antibiotic stewardship programme: results of a survey from Eastern India. Indian J. Med. Microbiol. 35:299–301.
120.
HayatK., RosenthalM., ZhuS., et al.2019. Attitude of clinicians towards hospital-based antimicrobial stewardship programs: a multicenter cross-sectional study from Punjab, Pakistan. Expert Rev. Anti. Infect. Ther. 17:661–669.
121.
BaubieK., ShaughnessyC., KostiukL., et al. 2019. Evaluating antibiotic stewardship in a tertiary care hospital in Kerala, India: a qualitative interview study. BMJ Open 9:e02, 6193.
122.
MulaC.T., HumanN., and MiddletonL.. 2019. An exploration of workarounds and their perceived impact on antibiotic stewardship in the adult medical wards of a referral hospital in Malawi: a qualitative study. BMC Health Serv. Res. 19:64.
123.
SinghS., CharaniE., WattalC., AroraA., JenkinsA., and NathwaniD.. 2019. The state of education and training for Antimicrobial Stewardship Programs in Indian hospitals-a qualitative and quantitative assessment. Antibiotics (Basel). 8:11.
124.
RolfeR.Jr, KwobahC., MuroF., et al.2021. Barriers to implementing antimicrobial stewardship programs in three low- and middle-income country tertiary care settings: findings from a multi-site qualitative study. Antimicrob. Resist. Infect. Control. 10:60.
125.
OmC., DailyF., VliegheE., McLaughlinJ.C, and McLawsM.L.. 2016. “If it's a broad spectrum, it can shoot better”: inappropriate antibiotic prescribing in Cambodia. Antimicrob. Resist. Infect. Control. 5:58.
126.
ThakolkaranN., ShettyA.V, D'SouzaN.D.R, and ShettyA.K.. 2017. Antibiotic prescribing knowledge, attitudes, and practice among physicians in teaching hospitals in South India. J. Family Med. Prim. Care. 6:526–532.
127.
TrikhaS., DalpathS.K, SharmaM., and ShafiqN.. 2020. Antibiotic prescribing patterns and knowledge of antibiotic resistance amongst the doctors working at public health facilities of a state in northern India: a cross sectional study. J. Family Med. Prim. Care, 9:3937–3943.
128.
YamanH., and YayliG.. 2003. Perceptions of physicians on infection control activities in Turkish hospitals: a cross-sectional survey. Am. J. Infect. Control. 31:325–328.
129.
GupteV., GogtayJ., and ManiR.K.. 2018. A questionnaire-based survey of physician perceptions of the prevalence of antimicrobial resistance and their antibiotic prescribing patterns. Indian J. Crit. Care Med. 22:491–497.
130.
SattiM.Z., HamzaM., SajidZ., et al.2019. Compliance rate of surgical antimicrobial prophylaxis and its association with knowledge of guidelines among surgical residents in a tertiary care public hospital of a developing country. Cureus, 11:e4776.
131.
KhawcharoenpornT., ApisarnthanarakA., and MundyL.M.. 2013. National survey of antimicrobial stewardship programs in Thailand. Am. J. Infect. Control. 41:86–88.
NaickerS., Plange-RhuleJ., TuttR.C, and EastwoodJ.B.. 2009. Shortage of healthcare workers in developing countries-Africa. Ethn. Dis. 19,(1 Suppl 1)::S1-60-4.
134.
LiuJ.X., GoryakinY., MaedaA., BrucknerT., and SchefflerR.. 2017. global health workforce labor market projections for 2030. Hum. Resour Health, 15:11.
135.
Ministry of Health Republic Indonesia. 2020. Profil Kesehatan Indonesia Tahun 2019. Ministry of Health Republic of Indonesia, Jakarta.
136.
ChungG.W., WuJ.E, YeoC.L, ChanD., and HsuL.Y.. 2013. Antimicrobial stewardship: a review of prospective audit and feedback systems and an objective evaluation of outcomes. Virulence, 4:151–157.
KullarR., NagelJ., BleasdaleS.C, et al.2019. Going for the gold: a description of the centers of excellence designation by the Infectious Diseases Society of America. Clin. Infect. Dis. 68:1777–1782.
139.
CharaniE., SmithI., SkodvinB., et al.2019. Investigating the cultural and contextual determinants of antimicrobial stewardship programmes across low-, middle- and high-income countries-A qualitative study. PLoS One, 14:e0209847.
140.
KimB., HwangH., KimJ., LeeM.J, and PaiH.. 2018. A few antibiotics can represent the total hospital antibiotic consumption. BMC Infect. Dis. 18:247.
de WithK., BestehornH., Steib-BauertM., and KernW.V.. 2009. Comparison of defined versus recommended versus prescribed daily doses for measuring hospital antibiotic consumption. Infection, 37:349–352.
143.
TamV.H., ChangK.T, ZhouJ., et al.2017. Determining β-lactam exposure threshold to suppress resistance development in Gram-negative bacteria. J. Antimicrob. Chemother. 72:1421–1428.
144.
HolmesA.H., MooreL.S, SundsfjordA., et al.2016. Understanding the mechanisms and drivers of antimicrobial resistance. Lancet. 387:176–187.
145.
TsaiD., JamalJ.A, DavisJ.S, LipmanJ., and RobertsJ.A.. 2015. Interethnic differences in pharmacokinetics of antibacterials. Clin. Pharmacokinet. 54:243–260.
146.
RobertsJ.A., Abdul-Aziz, LipmanJ., et al.2014. Individualised antibiotic dosing for patients who are critically ill: challenges and potential solutions. Lancet. Infect. Dis. 14:498–509.
147.
DikJ.W., HendrixR., PoelmanR., et al.2016. Measuring the impact of antimicrobial stewardship programs. Expert Rev. Anti. Infect. Ther. 14:569–575.
148.
de KrakerM.E.A., AbbasM., HuttnerB., and HarbarthS.. 2017. Good epidemiological practice: a narrative review of appropriate scientific methods to evaluate the impact of antimicrobial stewardship interventions. Clin. Microbiol. Infect. 23:819e25.
149.
HebertC., RidgwayJ., VekhterB., BrownE.C, WeberS.G, and RobicsekA.. 2012. Demonstration of the weighted-incidence syndromic combination antibiogram: an empiric prescribing decision aid. Infect. Control Hosp. Epidemiol. 33:381–388.
150.
BarkerF., AtkinsL., and de LusignanS.. 2016. Applying the COM-B behaviour model and behaviour change wheel to develop an intervention to improve hearing-aid use in adult auditory rehabilitation. Int. J. Audiol. 55 Suppl, 3:S90–S98.
151.
DoN.T.T., VuH.T.L, NguyenC.T.K, et al.2021. Community-based antibiotic access and use in six low-income and middle-income countries: a mixed-method approach. Lancet. Glob. Health. 9:e610–e619.
152.
TorresN.F., ChibiB., KuupielD., et al.2021. The use of non-prescribed antibiotics; prevalence estimates in low-and-middle-income countries. A systematic review and meta-analysis. Arch. Public Health. 79:2.
153.
WidayantiA.W., GreenJ.A, HeydonS., and NorrisP.. 2020. Health-Seeking behavior of people in Indonesia: a narrative review. J. Epidemiol. Glob. Health. 10:6–15.
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