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Perspective

How can we tackle the overuse of antibiotics in low- and middle-income countries?

ORCID Icon, ORCID Icon & ORCID Icon
Pages 1189-1201 | Received 11 Jul 2023, Accepted 22 Sep 2023, Published online: 05 Oct 2023

References

  • Klein EY, Van Boeckel TP, Martinez EM, et al. Global increase and geographic convergence in antibiotic consumption between 2000 and 2015. Proc Natl Acad Sci U S A. 2018;115(15):E3463–e3470. doi: 10.1073/pnas.1717295115
  • Klein EY, Milkowska-Shibata M, Tseng KK, et al. Assessment of WHO antibiotic consumption and access targets in 76 countries, 2000-15: an analysis of pharmaceutical sales data. Lancet Infect Dis. 2021;21(1):107–115. doi: 10.1016/S1473-3099(20)30332-7
  • Hsia Y, Lee BR, Versporten A, et al. Use of the WHO access, Watch, and Reserve classification to define patterns of hospital antibiotic use (AWaRe): an analysis of paediatric survey data from 56 countries. Lancet Glob Health. 2019;7(7):e861–e871. doi: 10.1016/S2214-109X(19)30071-3
  • Sulis G, Daniels B, Kwan A, et al. Antibiotic overuse in the primary health care setting: a secondary data analysis of standardised patient studies from India, China and Kenya. BMJ Glob Health. 2020;5(9):e003393. doi: 10.1136/bmjgh-2020-003393
  • Sulis G, Sayood S, Gandra S. Antimicrobial resistance in low- and middle-income countries: current status and future directions. Expert Rev Anti Infect Ther. 2022;20(2):147–160. doi:10.1080/14787210.2021.1951705
  • Sulis G, Sayood S, Katukoori S, et al. Exposure to World Health Organization’s AWaRe antibiotics and isolation of multidrug resistant bacteria: a systematic review and meta-analysis. Clin Microbiol Infect. 2022;28(9):1193–1202. doi: 10.1016/j.cmi.2022.03.014
  • Baraz A, Chowers M, Nevo D, et al. The time-varying association between previous antibiotic use and antibiotic resistance. Clin Microbiol Infect. 2023;29(3):.e390.391–.e390.394. doi:10.1016/j.cmi.2022.10.021
  • Bell BG, Schellevis F, Stobberingh E, et al. A systematic review and meta-analysis of the effects of antibiotic consumption on antibiotic resistance. BMC Infect Dis. 2014;14(1):13. doi: 10.1186/1471-2334-14-13
  • Poudel AN, Zhu S, Cooper N, et al. The economic burden of antibiotic resistance: a systematic review and meta-analysis. Plos One. 2023;18(5):e0285170. doi: 10.1371/journal.pone.0285170
  • Allwell-Brown G, Hussain-Alkhateeb L, Kitutu FE, et al. Trends in reported antibiotic use among children under 5 years of age with fever, diarrhoea, or cough with fast or difficult breathing across low-income and middle-income countries in 2005-17: a systematic analysis of 132 national surveys from 73 countries. Lancet Glob Health. 2020;8(6):e799–e807. doi: 10.1016/S2214-109X(20)30079-6
  • Sulis G, Adam P, Nafade V, et al. Antibiotic prescription practices in primary care in low- and middle-income countries: a systematic review and meta-analysis. PLOS Med. 2020;17(6):e1003139. doi: 10.1371/journal.pmed.1003139
  • Sulis G, Pradhan R, Kotwani A, et al. India’s ban on antimicrobial fixed-dose combinations: winning the battle, losing the war? J Of Pharm Policy And Pract. 2022;15(1):33. doi:10.1186/s40545-022-00428-w
  • Vliegenthart-Jongbloed K, Jacobs J. Not recommended fixed-dose antibiotic combinations in low- and middle-income countries - the example of Tanzania. Antimicrob Resist Infect Control. 2023;12(1):37. doi:10.1186/s13756-023-01238-8
  • Bortone B, Jackson C, Hsia Y, et al. High global consumption of potentially inappropriate fixed dose combination antibiotics: analysis of data from 75 countries. Plos One. 2021;16(1):e0241899. doi:10.1371/journal.pone.0241899
  • Langford BJ, So M, Simeonova M, et al. Antimicrobial resistance in patients with COVID-19: a systematic review and meta-analysis. Lancet Microbe. 2023;4(3):e179–e191. doi: 10.1016/S2666-5247(22)00355-X
  • Sulis G, Batomen B, Kotwani A, et al. Sales of antibiotics and hydroxychloroquine in India during the COVID-19 epidemic: an interrupted time series analysis. PLOS Med. 2021;18(7):e1003682. doi:10.1371/journal.pmed.1003682
  • Al-Azzam S, Mhaidat NM, Banat HA, et al. An Assessment of the impact of coronavirus disease (COVID-19) pandemic on national antimicrobial consumption in Jordan. Antibiotics. 2021;10(6):690. doi: 10.3390/antibiotics10060690
  • Del Fiol FS, Bergamaschi CC, De Andrade IP Jr., et al. Consumption trends of antibiotics in Brazil during the COVID-19 pandemic. Front Pharmacol. 2022;13:844818. doi:10.3389/fphar.2022.844818
  • Silva ARO, Salgado DR, Lopes LPN, et al. Increased use of antibiotics in the intensive care unit during coronavirus disease (COVID-19) pandemic in a Brazilian hospital. Front Pharmacol. 2021;12:778386. doi:10.3389/fphar.2021.778386
  • Mah EMS, Hassan MZ, Biswas M, et al. Use of antimicrobials among suspected COVID-19 patients at selected hospitals, Bangladesh: findings from the first wave of COVID-19 pandemic. Antibiotics. 2021;10(6):738. doi: 10.3390/antibiotics10060738
  • Nandi A, Pecetta S, Bloom DE. Global antibiotic use during the COVID-19 pandemic: analysis of pharmaceutical sales data from 71 countries, 2020-2022. EClinicalMedicine. 2023;57:101848.
  • Oleribe OO, Momoh J, Uzochukwu BS, et al. Identifying key challenges facing healthcare systems in Africa and potential solutions. Int J Gen Med. 2019;12:395–403. DOI:10.2147/IJGM.S223882
  • Li J, Zhou P, Wang J, et al. Worldwide dispensing of non-prescription antibiotics in community pharmacies and associated factors: a mixed-methods systematic review. Lancet Infect Dis. 2023;23(9):e361–e370. doi: 10.1016/S1473-3099(23)00130-5
  • Belachew SA, Hall L, Erku DA, et al. No prescription? No problem: drivers of non-prescribed sale of antibiotics among community drug retail outlets in low and middle income countries: a systematic review of qualitative studies. BMC Public Health. 2021;21(1):1056. doi:10.1186/s12889-021-11163-3
  • Gong Y, Jiang N, Chen Z, et al. Over-the-counter antibiotic sales in community and online pharmacies, China. Bull World Health Organ. 2020;98(7):449–457. doi: 10.2471/BLT.19.242370
  • Sun N, Gong Y, Liu J, et al. Prevalence of antibiotic purchase online and associated factors among Chinese residents: a nationwide community survey of 2019. Front Pharmacol. 2021;12:761086. DOI:10.3389/fphar.2021.761086
  • Patel SV, Pulcini C, Demirjian A, et al. Rapid diagnostic tests for common infection syndromes: less haste, more speed. J Antimicrob Chemother. 2020;75(8):2028–2030. doi:10.1093/jac/dkaa164
  • Cox S, Vleeming M, Giorgi W, et al. Patients’ experiences, expectations, motivations, and perspectives around urinary tract infection care in general practice: a qualitative interview study. Antibiotics. 2023;12(2):241. doi: 10.3390/antibiotics12020241
  • Lim JM, Huy S, Chhay T, et al. Understanding networks in rural Cambodian farming communities and how they influence antibiotic use: a mixed methods study. PLOS Glob Public Health. 2023;3(3):e0001569. doi:10.1371/journal.pgph.0001569
  • Amábile-Cuevas CF. Myths and Misconceptions around antibiotic resistance: time to get rid of them. Infect Chemother. 2022;54(3):393–408. doi:10.3947/ic.2022.0060
  • Gunasekera YD, Kinnison T, Kottawatta SA, et al. Misconceptions of antibiotics as a potential explanation for their misuse. A survey of the general public in a rural and urban community in Sri Lanka. Antibiotics. 2022;11(4):454. doi: 10.3390/antibiotics11040454
  • Ortega-Paredes D, Larrea-Álvarez CM, Torres-Elizalde L, et al. Antibiotic resistance awareness among undergraduate students in Quito, Ecuador. Antibiotics. 2022;11(2):197. doi: 10.3390/antibiotics11020197
  • Shamim MA, Padhi BK, Satapathy P, et al. Parents’ expectation of antibiotic prescriptions for respiratory infections in children: a systematic review and meta-analysis. Ther Adv Infect Dis. 2023;10:20499361231169429. DOI:10.1177/20499361231169429
  • Al-Taie A, Hussein AN, Albasry Z. A cross-sectional study of patients’ practices, knowledge and attitudes of antibiotics among Iraqi population. J Infect Dev Ctries. 2021;15(12):1845–1853. doi:10.3855/jidc.13066
  • Elong Ekambi GA, Okalla Ebongue C, Penda IC, et al. Knowledge, practices and attitudes on antibiotics use in Cameroon: self-medication and prescription survey among children, adolescents and adults in private pharmacies. Plos One. 2019;14(2):e0212875. doi:10.1371/journal.pone.0212875
  • Shamsudeen SM, Priya RS, Sujatha G, et al. Self-medication with antibiotics: a knowledge, attitude, and practice appraisal of 610 dental patients in Chennai, India, from 2016 to 2017. J Educ Health Promot. 2018;7:66. doi:10.4103/jehp.jehp_143_17
  • Ahmed I, King R, Akter S, et al. Determinants of antibiotic self-medication: a systematic review and meta-analysis. Res Social Adm Pharm. 2023;19(7):1007–1017. doi:10.1016/j.sapharm.2023.03.009
  • World Health Organization. Antibiotic resistance: multi-country public awareness survey. Geneva (Switzerland): World Health Organization (WHO); 2015
  • Chukwu EE, Oladele DA, Awoderu OB, et al. A national survey of public awareness of antimicrobial resistance in Nigeria. Antimicrob Resist Infect Control. 2020;9(1):72. doi: 10.1186/s13756-020-00739-0
  • Muleme J, Ssempebwa JC, Musoke D, et al. Antimicrobial resistance among farming communities in Wakiso District, Central Uganda: a knowledge, awareness and practice study. Plos One. 2023;18(6):e0284822. doi: 10.1371/journal.pone.0284822
  • Whitehorn A, Fu L, Porritt K, et al. Mapping clinical barriers and evidence-based implementation strategies in low-to-middle income countries (LMICs). Worldviews Evid Based Nurs. 2021;18(3):190–200. doi: 10.1111/wvn.12503
  • Greer SL, Méndez CA. Universal Health coverage: a political struggle and governance challenge. Am J Public Health. 2015;105(Suppl 5):S637–639. doi:10.2105/AJPH.2015.302733
  • Sulis G, Gandra S. Access to antibiotics: not a problem in some LMICs. Lancet Glob Health. 2021;9(5):e561–e562. doi:10.1016/S2214-109X(21)00085-1
  • Porter G, Kotwani A, Bhullar L, et al. Over-the-counter sales of antibiotics for human use in India: the challenges and opportunities for regulation. Med Law Int. 2021;21(2):147–173. doi:10.1177/09685332211020786
  • Wirtz VJ, Herrera-Patino JJ, Santa-Ana-Tellez Y, et al. Analysing policy interventions to prohibit over-the-counter antibiotic sales in four Latin American countries. Trop Med Int Health. 2013;18(6):665–673. doi:10.1111/tmi.12096
  • Jacobs TG, Robertson J, van den Ham HA, et al. Assessing the impact of law enforcement to reduce over-the-counter (OTC) sales of antibiotics in low- and middle-income countries; a systematic literature review. BMC Health Serv Res. 2019;19(1):536. doi:10.1186/s12913-019-4359-8
  • Kumah E. The informal healthcare providers and universal health coverage in low and middle-income countries. Global Health. 2022;18(1):45. doi:10.1186/s12992-022-00839-z
  • Rao UP, Rao NSS. The rural medical practitioner of India. J Evol Med Dental ScI. 2017;6:5321+. doi:10.14260/Jemds/2017/1154
  • Das J, Chowdhury A, Hussam R, et al. The impact of training informal health care providers in India: a randomized controlled trial. Science. 2016;354(6308). doi: 10.1126/science.aaf7384
  • Sudhinaraset M, Ingram M, Lofthouse HK, et al. What is the role of informal healthcare providers in developing countries? A systematic review. Plos One. 2013;8(2):e54978. doi:10.1371/journal.pone.0054978
  • Khare S, Purohit M, Sharma M, et al. Antibiotic prescribing by informal healthcare providers for common illnesses: a repeated cross-sectional study in rural India. Antibiotics. 2019;8(3):139. doi: 10.3390/antibiotics8030139
  • Ingelbeen B, Phanzu DM, Phoba MF, et al. Antibiotic use from formal and informal healthcare providers in the democratic Republic of Congo: a population-based study in two health zones. Clin Microbiol Infect. 2022;28(9):1272–1277. doi: 10.1016/j.cmi.2022.04.002
  • Kotwani A, Joshi PC, Jhamb U, et al. Prescriber and dispenser perceptions about antibiotic use in acute uncomplicated childhood diarrhea and upper respiratory tract infection in New Delhi: qualitative study. Indian J Pharmacol. 2017;49(6):419–431. doi:10.4103/ijp.IJP_508_17
  • Poluektova O, Robertson DA, Rafferty A, et al. A scoping review and behavioural analysis of factors underlying overuse of antimicrobials. JAC Antimicrob Resist. 2023;5(3):dlad043. doi:10.1093/jacamr/dlad043
  • Van Hecke O, Raymond M, Lee JJ, et al. In-vitro diagnostic point-of-care tests in paediatric ambulatory care: a systematic review and meta-analysis. Plos One. 2020;15(7):e0235605. doi: 10.1371/journal.pone.0235605
  • Huth PFB, Addo M, Daniel T, et al. Extensive antibiotic and antimalarial prescription rate among children with acute febrile diseases in the Lake Victoria region, Tanzania. J Trop Pediatr. 2021;67(1). doi: 10.1093/tropej/fmaa135
  • World Health Organization. Guidelines for the management of symptomatic sexually transmitted infections. Geneva (Switzerland): World Health Organization (WHO); 2021
  • Wangdi K, Kasturiaratchi K, Nery SV, et al. Diversity of infectious aetiologies of acute undifferentiated febrile illnesses in south and Southeast Asia: a systematic review. BMC Infect Dis. 2019;19(1):577. doi:10.1186/s12879-019-4185-y
  • Escadafal C, Incardona S, Fernandez-Carballo BL, et al. The good and the bad: using C reactive protein to distinguish bacterial from non-bacterial infection among febrile patients in low-resource settings. BMJ Glob Health. 2020;5(5). doi: 10.1136/bmjgh-2020-002396
  • Apisarnthanarak A, Bin Kim H, Moore LSP, et al. Utility and applicability of rapid diagnostic testing in antimicrobial stewardship in the Asia-Pacific region: a Delphi consensus. Clin Infect Dis. 2022;74(11):2067–2076. doi: 10.1093/cid/ciab910
  • Luan J, Seth A, Gupta R, et al. Ultrabright fluorescent nanoscale labels for the femtomolar detection of analytes with standard bioassays. Nat Biomed Eng. 2020;4(5):518–530. doi: 10.1038/s41551-020-0547-4
  • Gupta R, Gupta P, Wang S, et al. Ultrasensitive lateral-flow assays via plasmonically active antibody-conjugated fluorescent nanoparticles. Nat Biomed Eng. 2023. doi: 10.1038/s41551-022-01001-1
  • Zay Ya K, Win PTN, Bielicki J, et al. Association between antimicrobial stewardship programs and antibiotic use globally: a systematic review and meta-analysis. JAMA Netw Open. 2023;6(2):e2253806. doi:10.1001/jamanetworkopen.2022.53806
  • O’Leary EN, van Santen KL, Webb AK, et al. Uptake of antibiotic stewardship programs in US acute care hospitals: findings from the 2015 national healthcare safety network annual hospital survey. Clin Infect Dis. 2017;65(10):1748–1750. doi:10.1093/cid/cix651
  • Nathwani D, Varghese D, Stephens J, et al. Value of hospital antimicrobial stewardship programs [ASPs]: a systematic review. Antimicrob Resist Infect Control. 2019;8(1):35. doi: 10.1186/s13756-019-0471-0
  • Simmons B, Ariyoshi K, Ohmagari N, et al. Progress towards antibiotic use targets in eight high-income countries. Bull World Health Organ. 2021;99(8):550–561. doi: 10.2471/BLT.20.270934
  • Durkin MJ, Keller M, Butler AM, et al. An Assessment of inappropriate antibiotic use and guideline adherence for uncomplicated urinary tract infections. Open Forum Infect Dis. 2018;5(9):ofy198. doi: 10.1093/ofid/ofy198
  • Havers FP, Hicks LA, Chung JR, et al. Outpatient antibiotic prescribing for acute respiratory infections during influenza seasons. JAMA Netw Open. 2018;1(2):e180243. doi: 10.1001/jamanetworkopen.2018.0243
  • Fleming-Dutra KE, Hersh AL, Shapiro DJ, et al. Prevalence of inappropriate antibiotic prescriptions among US ambulatory care visits, 2010-2011. JAMA. 2016;315(17):1864–1873. doi: 10.1001/jama.2016.4151
  • Wellcome Trust. The Global Response to AMR: Momentum, Success, and Critical Gaps. London (UK): Wellcome Trust; 2020
  • Badur İ, Bilgin Badur N, Berk B. Investigation of hidden crisis of prescription drug abuse in Turkey: pregabalin monitoring. Acta Pharm Sci. 2022;60(4):313. doi: 10.23893/1307-2080.APS6021
  • Aydın M, Koyuncuoğlu CZ, Kırmızı İ, et al. Pattern of antibiotic prescriptions in dentistry in Turkey: population based data from the prescription information system. Infect Dis Clin Microbiol. 2019;1(2):62–69. doi: 10.36519/idcm.2019.19010
  • Aksoy M, Isli F, Kadi E, et al. Evaluation of more than one billion outpatient prescriptions and eight-year trend showing a remarkable reduction in antibiotic prescription in Turkey: a success model of governmental interventions at national level. Pharmacoepidemiol Drug Saf. 2021;30(9):1242–1249. doi: 10.1002/pds.5311
  • Blanchette L, Gauthier T, Heil E, et al. The essential role of pharmacists in antibiotic stewardship in outpatient care: an official position statement of the society of infectious diseases pharmacists. J Am Pharm Assoc. 2018;58(5):481–484. doi: 10.1016/j.japh.2018.05.013
  • Kerr F, Sefah IA, Essah DO, et al. Practical pharmacist-led interventions to improve antimicrobial stewardship in Ghana, Tanzania, Uganda and Zambia. Pharmacy. 2021;9(3):124. doi: 10.3390/pharmacy9030124
  • Gebretekle GB, Haile Mariam D, Abebe Taye W, et al. 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. 2020;8:109. DOI:10.3389/fpubh.2020.00109
  • van den Bergh D, Messina AP, Goff DA, et al. 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. 2020;56(6):106189. doi: 10.1016/j.ijantimicag.2020.106189
  • Baubie K, Shaughnessy C, Kostiuk L, et al. Evaluating antibiotic stewardship in a tertiary care hospital in Kerala, India: a qualitative interview study. BMJ Open. 2019;9(5):e026193. doi: 10.1136/bmjopen-2018-026193
  • Rehman IU, Asad MM, Bukhsh A, et al. Knowledge and practice of pharmacists toward antimicrobial stewardship in Pakistan. Pharmacy. 2018;6(4):116. doi: 10.3390/pharmacy6040116
  • Koju P, Rousseau SP, Van der Putten M, et al. Advertisement of antibiotics for upper respiratory infections and equity in access to treatment: a cross-sectional study in Nepal. J Pharm Policy Pract. 2020;13(4). doi: 10.1186/s40545-020-0202-1
  • Matin MA, Khan WA, Karim MM, et al. What influences antibiotic sales in rural Bangladesh? A drug dispensers’ perspective. J Of Pharm Policy And Pract. 2020;13(1):20. doi: 10.1186/s40545-020-00212-8
  • Cuevas C, Batura N, Wulandari LPL, et al. Improving antibiotic use through behaviour change: a systematic review of interventions evaluated in low- and middle-income countries. Health Policy Plan. 2021;36(5):594–605. doi: 10.1093/heapol/czab021
  • Zheng K, Xie Y, Dan L, et al. Effectiveness of educational interventions for Health workers on antibiotic prescribing in outpatient settings in China: a systematic review and meta-analysis. Antibiotics. 2022;11(6):791. doi: 10.3390/antibiotics11060791
  • World Health Organization. The WHO AWaRe (access, Watch, Reserve) antibiotic book. Geneva (Switzerland): World Health Organization (WHO); 2022.
  • Sharland M, Zanichelli V, Ombajo LA, et al. The WHO essential medicines list AWaRe book: from a list to a quality improvement system. Clin Microbiol Infect. 2022;28(12):1533–1535. doi: 10.1016/j.cmi.2022.08.009
  • Sharland M, Cappello B, Ombajo LA, et al. The WHO AWaRe antibiotic book: providing guidance on optimal use and informing policy. Lancet Infect Dis. 2022;22(11):1528–1530. doi: 10.1016/S1473-3099(22)00683-1
  • Zanichelli V, Sharland M, Cappello B, et al. The WHO AWaRe (access, Watch, Reserve) antibiotic book and prevention of antimicrobial resistance. Bull World Health Organ. 2023;101(4):290–296. doi: 10.2471/BLT.22.288614
  • Murray CJL, Ikuta KS, Sharara F, et al. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Lancet. 2022;399(10325):629–655. doi: 10.1016/S0140-6736(21)02724-0
  • Hay SI, Rao PC, Dolecek C, et al. Measuring and mapping the global burden of antimicrobial resistance. BMC Med. 2018;16(1):78. doi: 10.1186/s12916-018-1073-z
  • Dadgostar P. Antimicrobial resistance: implications and costs. Infect Drug Resist. 2019;12:3903–3910. doi:10.2147/IDR.S234610
  • Founou RC, Founou LL, Essack SY, et al. Clinical and economic impact of antibiotic resistance in developing countries: a systematic review and meta-analysis. Plos One. 2017;12(12):e0189621. doi:10.1371/journal.pone.0189621
  • Gandra S, Barter DM, Laxminarayan R. Economic burden of antibiotic resistance: how much do we really know? Clin Microbiol Infect. 2014;20(10):973–980. doi:10.1111/1469-0691.12798
  • Largeron N, Lévy P, Wasem J, et al. Role of vaccination in the sustainability of healthcare systems. J Mark Access Health Policy. 2015;3(1):27043. doi: 10.3402/jmahp.v3.27043
  • Marangu D, Zar HJ. Childhood pneumonia in low-and-middle-income countries: an update. Paediatr Respir Rev. 2019;32:3–9. doi:10.1016/j.prrv.2019.06.001
  • Ladhani SN, Collins S, Djennad A, et al. Rapid increase in non-vaccine serotypes causing invasive pneumococcal disease in England and Wales, 2000-17: a prospective national observational cohort study. Lancet Infect Dis. 2018;18(4):441–451. doi: 10.1016/S1473-3099(18)30052-5
  • Lewnard JA, Lo NC, Arinaminpathy N, et al. Childhood vaccines and antibiotic use in low- and middle-income countries. Nature. 2020;581(7806):94–99. doi:10.1038/s41586-020-2238-4
  • Awuor AO, Ogwel B, Powell H, et al. Antibiotic-prescribing practices for management of childhood diarrhea in 3 Sub-Saharan African countries: findings from the vaccine impact on diarrhea in Africa (VIDA) study, 2015-2018. Clin Infect Dis. 2023;76(Suppl1):S32–s40. doi: 10.1093/cid/ciac980
  • Buckley BS, Henschke N, Bergman H, et al. Impact of vaccination on antibiotic usage: a systematic review and meta-analysis. Clin Microbiol Infect. 2019;25(10):1213–1225. doi: 10.1016/j.cmi.2019.06.030
  • Lewnard JA, Fries LF, Cho I, et al. Prevention of antimicrobial prescribing among infants following maternal vaccination against respiratory syncytial virus. Proc Natl Acad Sci U S A. 2022;119(12):e2112410119. doi: 10.1073/pnas.2112410119
  • Heymann DL, Kieny MP, Laxminarayan R. Adding to the mantra: vaccines prevent illness and death, and preserve existing antibiotics. Lancet Infect Dis. 2022;22(8):1108–1109. doi:10.1016/S1473-3099(22)00374-7
  • Schueller E, Nandi A, Joshi J, et al. Associations between private vaccine and antimicrobial consumption across Indian states, 2009-2017. Ann N Y Acad Sci. 2021;1494(1):31–43. doi:10.1111/nyas.14571
  • Yousafzai MT, Qamar FN, Shakoor S, et al. Ceftriaxone-resistant Salmonella Typhi outbreak in Hyderabad city of Sindh, Pakistan: high time for the introduction of typhoid conjugate vaccine. Clin Infect Dis. 2019;68(Suppl 1):S16–s21. doi: 10.1093/cid/ciy877
  • Qamar FN, Yousafzai MT, Khalid M, et al. Outbreak investigation of ceftriaxone-resistant Salmonella enterica serotype Typhi and its risk factors among the general population in Hyderabad, Pakistan: a matched case-control study. Lancet Infect Dis. 2018;18(12):1368–1376. doi: 10.1016/S1473-3099(18)30483-3
  • Klemm EJ, Shakoor S, Page AJ, et al. Emergence of an extensively drug-resistant Salmonella enterica serovar Typhi clone harboring a promiscuous plasmid encoding resistance to fluoroquinolones and third-generation cephalosporins. MBio. 2018;9(1). doi: 10.1128/mBio.00105-18
  • Qureshi S, Naveed AB, Yousafzai MT, et al. Response of extensively drug resistant Salmonella Typhi to treatment with meropenem and azithromycin, in Pakistan. PLoS Negl Trop Dis. 2020;14(10):e0008682. doi: 10.1371/journal.pntd.0008682
  • Gomes MZR, de Lima EM, Martins Aires CA, et al. Outbreak report of polymyxin-carbapenem-resistant Klebsiella pneumoniae causing untreatable infections evidenced by synergy tests and bacterial genomes. Sci Rep. 2023;13(1):6238. doi: 10.1038/s41598-023-31901-4
  • Allel K, Day L, Hamilton A, et al. Global antimicrobial-resistance drivers: an ecological country-level study at the human-animal interface. Lancet Planet Health. 2023;7(4):e291–e303. doi: 10.1016/S2542-5196(23)00026-8
  • World Health Organization. Regional office for the Eastern Mediterranean. Pakistan first country to introduce new typhoid vaccine into routine immunization programme. Karachi (Pakistan): World Health Organization (WHO) Regional Office for the Eastern Mediterranean; 2019.
  • Nampota-Nkomba N, Nyirenda OM, Khonde L, et al. Safety and immunogenicity of a typhoid conjugate vaccine among children aged 9 months to 12 years in Malawi: a nested substudy of a double-blind, randomised controlled trial. Lancet Glob Health. 2022;10(9):e1326–e1335. doi: 10.1016/S2214-109X(22)00275-3
  • Yousafzai MT, Karim S, Qureshi S, et al. Effectiveness of typhoid conjugate vaccine against culture-confirmed Salmonella enterica serotype Typhi in an extensively drug-resistant outbreak setting of Hyderabad, Pakistan: a cohort study. Lancet Glob Health. 2021;9(8):e1154–e1162. doi: 10.1016/S2214-109X(21)00255-2
  • Birger R, Antillón M, Bilcke J, et al. Estimating the effect of vaccination on antimicrobial-resistant typhoid fever in 73 countries supported by Gavi: a mathematical modelling study. Lancet Infect Dis. 2022;22(5):679–691. doi: 10.1016/S1473-3099(21)00627-7
  • Frost I, Sati H, Garcia-Vello P, et al. The role of bacterial vaccines in the fight against antimicrobial resistance: an analysis of the preclinical and clinical development pipeline. Lancet Microbe. 2023;4(2):e113–e125. doi: 10.1016/S2666-5247(22)00303-2
  • World Health Organization. WHO priority pathogens list for R&D of new antibiotics. Geneva (Switzerland): World Health Organization (WHO); 2017.
  • Micoli F, Bagnoli F, Rappuoli R, et al. The role of vaccines in combatting antimicrobial resistance. Nat Rev Microbiol. 2021;19(5):287–302. doi:10.1038/s41579-020-00506-3
  • Riou J, Althaus CL, Allen H, et al. Projecting the development of antimicrobial resistance in Neisseria gonorrhoeae from antimicrobial surveillance data: a mathematical modelling study. BMC Infect Dis. 2023;23(1):252. doi: 10.1186/s12879-023-08200-4
  • Whittles LK, White PJ, Didelot X. Assessment of the potential of vaccination to combat antibiotic resistance in gonorrhea: a modeling analysis to determine preferred product characteristics. Clin Infect Dis. 2020;71(8):1912–1919. doi:10.1093/cid/ciz1241
  • Causey K, Fullman N, Sorensen RJD, et al. Estimating global and regional disruptions to routine childhood vaccine coverage during the COVID-19 pandemic in 2020: a modelling study. Lancet. 2021;398(10299):522–534. doi: 10.1016/S0140-6736(21)01337-4
  • Basu S, Ashok G, Debroy R, et al. Impact of the COVID-19 pandemic on routine vaccine landscape: a global perspective. Hum Vaccin Immunother. 2023;2199656. doi: 10.1080/21645515.2023.2199656
  • World Health Organization. Global partners announce a new effort – “The Big Catch-up” – to vaccinate millions of children and restore immunization progress lost during the pandemic. Geneva (Switerland): World Health Organization (WHO); 2023
  • NTT D, HTL V, Nguyen CTK, et al. Community-based antibiotic access and use in six low-income and middle-income countries: a mixed-method approach. Lancet Glob Health. 2021;9(5):e610–e619. doi: 10.1016/S2214-109X(21)00024-3
  • Kotwani A, Bhanot A, Singal GL, et al. Marketing and distribution system foster misuse of antibiotics in the community: insights from drugs wholesalers in India. Antibiotics. 2022;11(1):95. doi: 10.3390/antibiotics11010095
  • Statista. Share of urban population worldwide in 2022, by continent. Statista Research Department; 2023. https://www.statista.com/statistics/270860/urbanization-by-continent/
  • Davis Mike. Slum Ecology. In: Planet of slums. London: Verso; 2006. p. 120–150.
  • Ritchie H, Roser M. Urbanization. OurWorldInData.org; 2018. https://ourworldindata.org/urbanization
  • Collignon P, Beggs JJ. Socioeconomic enablers for contagion: factors impelling the antimicrobial resistance epidemic. Antibiotics. 2019;8(3):86. doi: 10.3390/antibiotics8030086
  • Denyer Willis L, Chandler C. Quick fix for care, productivity, hygiene and inequality: reframing the entrenched problem of antibiotic overuse. BMJ Glob Health. 2019;4(4):e001590. doi: 10.1136/bmjgh-2019-001590
  • Dixon J, MacPherson EE, Nayiga S, et al. Antibiotic stories: a mixed-methods, multi-country analysis of household antibiotic use in Malawi, Uganda and Zimbabwe. BMJ Glob Health. 2021;6(11):e006920. doi: 10.1136/bmjgh-2021-006920
  • Ramay BM, Caudell MA, Cordón-Rosales C, et al. Antibiotic use and hygiene interact to influence the distribution of antimicrobial-resistant bacteria in low-income communities in Guatemala. Sci Rep. 2020;10(1):13767. doi: 10.1038/s41598-020-70741-4

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