Key Issues Surrounding Appropriate Antibiotic Use for Prevention of Surgical Site Infections in Low- and Middle-Income Countries: A Narrative Review and the Implications

References

• 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. 2020;21:107–115. doi:10.1016/S1473-3099(20)30332-7
   PubMed Web of Science ®Google Scholar
• 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–e70. doi:10.1073/pnas.1717295115
   PubMed Web of Science ®Google Scholar
• Schellack N, Benjamin D, Brink A, et al. A situational analysis of current antimicrobial governance, regulation, and utilization in South Africa. Int J Infect Dis. 2017;64:100–106. doi:10.1016/j.ijid.2017.09.002
   PubMed Web of Science ®Google Scholar
• Bell BG, Schellevis F, Stobberingh E, Goossens H, Pringle M. A systematic review and meta-analysis of the effects of antibiotic consumption on antibiotic resistance. BMC Infect Dis. 2014;14:13. doi:10.1186/1471-2334-14-13
   PubMed Web of Science ®Google Scholar
• Cassini A, Hogberg LD, Plachouras D, et al. Attributable deaths and disability-adjusted life-years caused by infections with antibiotic-resistant bacteria in the EU and the European Economic Area in 2015: a population-level modelling analysis. Lancet Infect Dis. 2019;19(1):56–66. doi:10.1016/S1473-3099(18)30605-4
   PubMed Web of Science ®Google Scholar
• Godman B, Fadare J, Kibuule D, et al. Initiatives across countries to reduce antibiotic utilisation and resistance patterns: impact and implications. In: Arora G, Sajid A, Kalia VC, editors. Drug Resistance in Bacteria, Fungi, Malaria, and Cancer. Cham: Springer International Publishing; 2017:539–576.
   Google Scholar
• Hofer U. The cost of antimicrobial resistance. Nat Rev Microbiol. 2019;17(1):3. doi:10.1038/s41579-018-0125-x
   PubMedGoogle Scholar
• Vicentini C, Politano G, Corcione S, et al. Surgical antimicrobial prophylaxis prescribing practices and impact on infection risk: results from a multicenter surveillance study in Italy (2012–2017). Am J Infect Control. 2019;47(12):1426–1430. doi:10.1016/j.ajic.2019.07.013
   PubMed Web of Science ®Google Scholar
• Weber WP, Marti WR, Zwahlen M, et al. The timing of surgical antimicrobial prophylaxis. Ann Surg. 2008;247(6):918–926. doi:10.1097/SLA.0b013e31816c3fec
   PubMed Web of Science ®Google Scholar
• Young PY, Khadaroo RG. Surgical site infections. Surg Clin North Am. 2014;94(6):1245–1264. doi:10.1016/j.suc.2014.08.008
   PubMed Web of Science ®Google Scholar
• Mwita JC, Souda S, Magafu M, Massele A, Godman B, Mwandri M. Prophylactic antibiotics to prevent surgical site infections in Botswana: findings and implications. Hosp Pract. 2018;46(3):97–102. doi:10.1080/21548331.2018.1450605
   PubMedGoogle Scholar
• Ngaroua JE, Benet T, Djibrilla Y, Djibrilla Y. [Incidence of surgical site infections in sub-Saharan Africa: systematic review and meta-analysis]. Pan Afr Med J. 2016;24:171. French. doi:10.11604/pamj.2016.24.171.9754
   Google Scholar
• Saito H, Inoue K, Ditai J, Weeks AD. Pattern of peri-operative antibiotic use among surgical patients in a regional referral and teaching hospital in Uganda. Surg Infect (Larchmt). 2020;21(6):540–546. doi:10.1089/sur.2019.176
   PubMed Web of Science ®Google Scholar
• Anderson DJ, Podgorny K, Berrios-Torres SI, et al. Strategies to prevent surgical site infections in acute care hospitals: 2014 update. Infect Control Hosp Epidemiol. 2014;35(6):605–627. doi:10.1086/676022
   PubMed Web of Science ®Google Scholar
• Zimlichman E, Henderson D, Tamir O, et al. Health care-associated infections: a meta-analysis of costs and financial impact on the US health care system. JAMA Intern Med. 2013;173(22):2039–2046. doi:10.1001/jamainternmed.2013.9763
   PubMed Web of Science ®Google Scholar
• Korol E, Johnston K, Waser N, et al. A systematic review of risk factors associated with surgical site infections among surgical patients. PLoS One. 2013;8(12):e83743. doi:10.1371/journal.pone.0083743
   PubMed Web of Science ®Google Scholar
• Goyal R, Pal H, Sandhu S, Kumar A, Kosey S, Mehra N. Surveillance method for surgical site infection. Indian J Pharm Pract. 2015;8:54–60. doi:10.5530/ijopp.8.2.2
   Google Scholar
• Najjar PA, Smink DS. Prophylactic antibiotics and prevention of surgical site infections. Surg Clin North Am. 2015;95(2):269–283. doi:10.1016/j.suc.2014.11.006
   PubMed Web of Science ®Google Scholar
• Saleem Z, Hassali MA, Godman B, Hashmi FK, Saleem F. A multicenter point prevalence survey of healthcare-associated infections in Pakistan: findings and implications. Am J Infect Control. 2019;47(4):421–424. doi:10.1016/j.ajic.2018.09.025
   PubMed Web of Science ®Google Scholar
• Labi AK, Obeng-Nkrumah N, Owusu E, et al. Multi-centre point-prevalence survey of hospital-acquired infections in Ghana. J Hosp Infect. 2019;101(1):60–68. doi:10.1016/j.jhin.2018.04.019
   PubMed Web of Science ®Google Scholar
• Abubakar U. Antibiotic use among hospitalized patients in northern Nigeria: a multicenter point-prevalence survey. BMC Infect Dis. 2020;20(1):86. doi:10.1186/s12879-020-4815-4
   PubMed Web of Science ®Google Scholar
• Abubakar U. Point-prevalence survey of hospital acquired infections in three acute care hospitals in Northern Nigeria. Antimicrob Resist Infect Control. 2020;9(1):63. doi:10.1186/s13756-020-00722-9
   PubMed Web of Science ®Google Scholar
• Karaali C, Emiroglu M, Atalay S, et al. A new antibiotic stewardship program approach is effective on inappropriate surgical prophylaxis and discharge prescription. J Infect Dev Ctries. 2019;13(11):961–967. doi:10.3855/jidc.11734
   PubMed Web of Science ®Google Scholar
• Saleem Z, Hassali MA, Godman B, et al. Point prevalence surveys of antimicrobial use: a systematic review and the implications. Expert Rev Anti Infect Ther. 2020;18:897–910. doi:10.1080/14787210.2020.1767593
   PubMed Web of Science ®Google Scholar
• Versporten A, Zarb P, Caniaux I, et al. Antimicrobial consumption and resistance in adult hospital inpatients in 53 countries: results of an internet-based global point prevalence survey. Lancet Global Health. 2018;6(6):e619–e29. doi:10.1016/S2214-109X(18)30186-4
   PubMed Web of Science ®Google Scholar
• Al Matar M, Enani M, Binsaleh G, et al. Point prevalence survey of antibiotic use in 26 Saudi hospitals in 2016. J Infect Public Health. 2019;12(1):77–82. doi:10.1016/j.jiph.2018.09.003
   PubMed Web of Science ®Google Scholar
• Mahmoudi L, Ghouchani M, Mahi-Birjand M, Bananzadeh A, Akbari A. Optimizing compliance with surgical antimicrobial prophylaxis guidelines in patients undergoing gastrointestinal surgery at a referral teaching hospital in southern Iran: clinical and economic impact. Infect Drug Resist. 2019;12:2437–2444. doi:10.2147/IDR.S212728
   PubMed Web of Science ®Google Scholar
• de Lissovoy G, Fraeman K, Hutchins V, Murphy D, Song D, Vaughn BB. Surgical site infection: incidence and impact on hospital utilization and treatment costs. Am J Infect Control. 2009;37(5):387–397. doi:10.1016/j.ajic.2008.12.010
   PubMed Web of Science ®Google Scholar
• De Simone B, Sartelli M, Coccolini F, et al. Intraoperative surgical site infection control and prevention: a position paper and future addendum to WSES intra-abdominal infections guidelines. World J Emerg Surg. 2020;15(1):10. doi:10.1186/s13017-020-0288-4
   PubMed Web of Science ®Google Scholar
• Olowo-Okere A, Ibrahim YKE, Olayinka BO, Ehinmidu JO. Epidemiology of surgical site infections in Nigeria: a systematic review and meta-analysis. Niger Postgrad Med J. 2019;26(3):143–151. doi:10.4103/npmj.npmj_72_19
   PubMedGoogle Scholar
• Allegranzi B, Bagheri Nejad S, Combescure C, et al. Burden of endemic health-care-associated infection in developing countries: systematic review and meta-analysis. Lancet. 2011;377(9761):228–241. doi:10.1016/S0140-6736(10)61458-4
   PubMed Web of Science ®Google Scholar
• Mawalla B, Mshana SE, Chalya PL, Imirzalioglu C, Mahalu W. Predictors of surgical site infections among patients undergoing major surgery at Bugando Medical Centre in Northwestern Tanzania. BMC Surg. 2011;11. doi:10.1186/1471-2482-11-21
   PubMed Web of Science ®Google Scholar
• Rickard J, Beilman G, Forrester J, et al. Surgical infections in low- and middle-income countries: a global assessment of the burden and management needs. Surg Infect (Larchmt). 2020;21(6):478–494. doi:10.1089/sur.2019.142
   PubMed Web of Science ®Google Scholar
• Olowo-Okere A, Ibrahim YKE, Sani AS, Olayinka BO. Occurrence of surgical site infections at a tertiary healthcare facility in Abuja, Nigeria: a prospective observational study. Med Sci. 2018;6(3):60. doi:10.3390/medsci6030060
   Google Scholar
• Maleknejad A, Dastyar N, Badakhsh M, et al. Surgical site infections in Eastern Mediterranean region: a systematic review and meta-analysis. Infect Dis. 2019;51(10):719–729. doi:10.1080/23744235.2019.1642513
   PubMed Web of Science ®Google Scholar
• Ling ML, Apisarnthanarak A, Abbas A, et al. APSIC guidelines for the prevention of surgical site infections. Antimicrob Resist Infect Control. 2019;8(1):174. doi:10.1186/s13756-019-0638-8
   PubMed Web of Science ®Google Scholar
• Rojas-Gutierrez E, Vilar-Compte D. An overview of surgical site infection in low- and middle-income countries: the role of recent guidelines, limitations, and possible solutions. Curr Treat Options Infect Dis. 2019;11(3):300–316. doi:10.1007/s40506-019-00198-1
   Google Scholar
• Loftus MJ, Guitart C, Tartari E, et al. Hand hygiene in low- and middle-income countries. Int J Infect Dis. 2019;86:25–30. doi:10.1016/j.ijid.2019.06.002
   PubMed Web of Science ®Google Scholar
• Ng-Kamstra JS, Arya S, Greenberg SLM, et al. Perioperative mortality rates in low-income and middle-income countries: a systematic review and meta-analysis. BMJ Global Health. 2018;3(3):e000810. doi:10.1136/bmjgh-2018-000810
   PubMed Web of Science ®Google Scholar
• Roa L, Citron I, Ramos JA, et al. Cross-sectional study of surgical quality with a novel evidence-based tool for low-resource settings. BMJ Open Qual. 2020;9(1):e000880. doi:10.1136/bmjoq-2019-000880
   PubMedGoogle Scholar
• Saluja S, Mukhopadhyay S, Amundson JR, et al. Quality of essential surgical care in low- and middle-income countries: a systematic review of the literature. Int J Qual Health Care. 2019;31(3):166–172. doi:10.1093/intqhc/mzy141
   PubMed Web of Science ®Google Scholar
• Bull AL, Worth LJ, Spelman T, Richards MJ. Antibiotic prescribing practices for prevention of surgical site infections in Australia: increased uptake of national guidelines after surveillance and reporting and impact on infection rates. Surg Infect (Larchmt). 2017;18(7):834–840. doi:10.1089/sur.2017.119
   PubMed Web of Science ®Google Scholar
• Varley AJ, Sule J, Absalom AR. Principles of antibiotic therapy. Critical Care Pain. 2009;9(6):184–188. doi:10.1093/bjaceaccp/mkp035
   Google Scholar
• Culver DH, Horan TC, Gaynes RP, et al. Surgical wound infection rates by wound class, operative procedure, and patient risk index. National nosocomial infections surveillance system. Am J Med. 1991;91(3):152s–7s. doi:10.1016/0002-9343(91)90361-Z
   PubMed Web of Science ®Google Scholar
• Butt SZ, Ahmad M, Saeed H, Saleem Z, Javaid Z. Post-surgical antibiotic prophylaxis: impact of pharmacist’s educational intervention on appropriate use of antibiotics. J Infect Public Health. 2019;12(6):854–860. doi:10.1016/j.jiph.2019.05.015
   PubMed Web of Science ®Google Scholar
• Umeokonkwo CD, Madubueze UC, Onah CK, et al. Point prevalence survey of antimicrobial prescription in a tertiary hospital in South East Nigeria: a call for improved antibiotic stewardship. J Global Antimicrob Resist. 2019;17:291–295. doi:10.1016/j.jgar.2019.01.013
   PubMed Web of Science ®Google Scholar
• Halawi E, Assefa T, Hussen S. Pattern of antibiotics use, incidence and predictors of surgical site infections in a Tertiary Care Teaching Hospital. BMC Res Notes. 2018;11(1):538. doi:10.1186/s13104-018-3643-8
   PubMedGoogle Scholar
• Bratzler DW, Dellinger EP, Olsen KM, et al. Clinical practice guidelines for antimicrobial prophylaxis in surgery. Surg Infect (Larchmt). 2013;14(1):73–156. doi:10.1089/sur.2013.9999
   PubMed Web of Science ®Google Scholar
• Malhotra NR, Piazza M, Demoor R, et al. Impact of reduced preincision antibiotic infusion time on surgical site infection rates: a retrospective cohort study. Ann Surg. 2020;271(4):774–780. doi:10.1097/SLA.0000000000003030
   PubMed Web of Science ®Google Scholar
• Cooper L, Sneddon J, Afriyie DK, et al. Supporting global antimicrobial stewardship: antibiotic prophylaxis for the prevention of surgical site infection in low- and middle-income countries (LMICs): a scoping review and meta-analysis. JAC-AMR. 2020;2(3). doi:10.1093/jacamr/dlaa070.
   Google Scholar
• Yang Z, Zhao P, Wang J, et al. DRUGS system enhancing adherence of Chinese surgeons to antibiotic use guidelines during perioperative period. PLoS One. 2014;9(8):e102226. doi:10.1371/journal.pone.0102226
   PubMed Web of Science ®Google Scholar
• de Jonge SW, Gans SL, Atema JJ, Solomkin JS, Dellinger PE, Boermeester MA. Timing of preoperative antibiotic prophylaxis in 54,552 patients and the risk of surgical site infection: a systematic review and meta-analysis. Medicine. 2017;96(29):e6903. doi:10.1097/MD.0000000000006903
   PubMed Web of Science ®Google Scholar
• Branch-Elliman W, O’Brien W, Strymish J, Itani K, Wyatt C, Gupta K. Association of duration and type of surgical prophylaxis with antimicrobial-associated adverse events. JAMA Surg. 2019;154(7):590–598. doi:10.1001/jamasurg.2019.0569
   PubMed Web of Science ®Google Scholar
• Harbarth S, Samore MH, Lichtenberg D, Carmeli Y. Prolonged antibiotic prophylaxis after cardiovascular surgery and its effect on surgical site infections and antimicrobial resistance. Circulation. 2000;101(25):2916–2921. doi:10.1161/01.cir.101.25.2916
   PubMed Web of Science ®Google Scholar
• Hawn MT, Knowlton LM. Balancing the risks and benefits of surgical prophylaxis: timing and duration do matter. JAMA Surg. 2019;154(7):598–599. doi:10.1001/jamasurg.2019.0570
   PubMed Web of Science ®Google Scholar
• Langerman A, Thisted R, Hohmann S, Howell M. Antibiotic and duration of perioperative prophylaxis predicts surgical site infection in head and neck surgery. Otolaryngol Head Neck Surg. 2016;154(6):1054–1063. doi:10.1177/0194599816634303
   PubMed Web of Science ®Google Scholar
• Musmar SM, Ba’ba H, Owais A. Adherence to guidelines of antibiotic prophylactic use in surgery: a prospective cohort study in North West Bank, Palestine. BMC Surg. 2014;14:69. doi:10.1186/1471-2482-14-69
   PubMed Web of Science ®Google Scholar
• Alemkere G, Hawryluk GWJ. Antibiotic usage in surgical prophylaxis: a prospective observational study in the surgical ward of Nekemte referral hospital. PLoS One. 2018;13(9):e0203523. doi:10.1371/journal.pone.0203523
   PubMed Web of Science ®Google Scholar
• Madubueze CC, Umaru H, Alada A. Attitudes of Nigerian orthopaedic surgeons to the use of prophylactic antibiotics. Int Orthop. 2015;39(11):2161–2165. doi:10.1007/s00264-015-2822-7
   PubMed Web of Science ®Google Scholar
• Nkurunziza T, Kateera F, Sonderman K, et al. Prevalence and predictors of surgical-site infection after caesarean section at a rural district hospital in Rwanda. Br J Surg. 2019;106(2):e121–e8. doi:10.1002/bjs.11060
   PubMed Web of Science ®Google Scholar
• Shankar R. Implementation of the WHO Surgical Safety Checklist at a teaching hospital in India and evaluation of the effects on perioperative complications. Int J Health Plann Manage. 2018;33(4):836–846. doi:10.1002/hpm.2533
   PubMed Web of Science ®Google Scholar
• Alahmadi YM, Alharbi RH, Aljabri AK, Alofi FS, Alshaalani OA, Alssdi BH. Adherence to the guidelines for surgical antimicrobial prophylaxis in a Saudi tertiary care hospital. J Taibah Univ Med Sci. 2020;15(2):136–141. doi:10.1016/j.jtumed.2020.01.005
   PubMed Web of Science ®Google Scholar
• Afriyie DK, Sefah IA, Sneddon J, et al. Antimicrobial Point Prevalence Surveys in two Ghanaian hospitals: opportunities for antimicrobial stewardship. JAC AMR. 2020;1–9.
   Google Scholar
• Abubakar U, Syed Sulaiman SA, Adesiyun AG. Utilization of surgical antibiotic prophylaxis for obstetrics and gynaecology surgeries in Northern Nigeria. Int J Clin Pharm. 2018;40(5):1037–1043. doi:10.1007/s11096-018-0702-0
   PubMed Web of Science ®Google Scholar
• Aiken AM, Wanyoro AK, Mwangi J, Juma F, Mugoya IK, Scott JA. Changing use of surgical antibiotic prophylaxis in Thika Hospital, Kenya: a quality improvement intervention with an interrupted time series design. PLoS One. 2013;8(11):e78942. doi:10.1371/journal.pone.0078942
   PubMed Web of Science ®Google Scholar
• Friedman ND, Styles K, Gray AM, Low J, Athan E. Compliance with surgical antibiotic prophylaxis at an Australian teaching hospital. Am J Infect Control. 2013;41(1):71–74. doi:10.1016/j.ajic.2012.02.012
   PubMed Web of Science ®Google Scholar
• Opanga SA, Mwang’ombe NJ, Okalebo FA, Godman B, Oluka M, Kuria KAM. Determinants of the effectiveness of antimicrobial prophylaxis among neurotrauma patients at a referral hospital in Kenya: findings and implications. Infect Dis Preve Med. 2017;5:169.
   Google Scholar
• Godman B, Haque M, McKimm J, et al. Ongoing strategies to improve the management of upper respiratory tract infections and reduce inappropriate antibiotic use particularly among lower and middle-income countries: findings and implications for the future. Curr Med Res Opin. 2020;36(2):301–327. doi:10.1080/03007995.2019.1700947
   PubMed Web of Science ®Google Scholar
• Saleem Z, Hassali MA, Hashmi FK. Pakistan’s national action plan for antimicrobial resistance: translating ideas into reality. Lancet Infect Dis. 2018;18(10):1066–1067. doi:10.1016/S1473-3099(18)30516-4
   PubMed Web of Science ®Google Scholar
• Ghana Ministry of Health, Ministry of Food and Agriculture, Ministry of Environment, Science, Technology and Innovation, Ministry of Fisheries and Aquaculture Development. Ghana national action plan for antimicrobial use and resistance; 2017–2021. Available from: http://www.moh.gov.gh/wp-content/uploads/2018/04/NAP_FINAL_PDF_A4_19.03.2018-SIGNED-1.pdf. Accessed January 8, 2021.
   Google Scholar
• Ayukekbong JA, Ntemgwa M, Atabe AN. The threat of antimicrobial resistance in developing countries: causes and control strategies. Antimicrob Resist Infect Control. 2017;6(1):47. doi:10.1186/s13756-017-0208-x
   PubMed Web of Science ®Google Scholar
• Kalungia A, Godman B. Implications of non-prescription antibiotic sales in China. Lancet Infect Dis. 2019;19(12):1272–1273. doi:10.1016/S1473-3099(19)30408-6
   PubMed Web of Science ®Google Scholar
• Akpan MR, Isemin NU, Udoh AE, Ashiru-Oredope D. Implementation of antimicrobial stewardship programmes in African countries: a systematic literature review. J Global Antimicrob Resist. 2020;22:317–324. doi:10.1016/j.jgar.2020.03.009
   PubMed Web of Science ®Google Scholar
• Cox JA, Vlieghe E, Mendelson M, et al. Antibiotic stewardship in low- and middle-income countries: the same but different? Clin Microbiol Infect. 2017;23(11):812–818. doi:10.1016/j.cmi.2017.07.010
   PubMed Web of Science ®Google Scholar
• Charani E, Smith I, Skodvin B, et al. Investigating the cultural and contextual determinants of antimicrobial stewardship programmes across low-, middle- and high-income countries-A qualitative study. PLoS One. 2019;14(1):e0209847. doi:10.1371/journal.pone.0209847
   PubMed Web of Science ®Google Scholar
• Nathwani D, Varghese D, Stephens J, Ansari W, Martin S, Charbonneau C. Value of hospital antimicrobial stewardship programs [ASPs]: a systematic review. Antimicrob Resist Infect Control. 2019;8:35. doi:10.1186/s13756-019-0471-0
   PubMed Web of Science ®Google Scholar
• Fadare JO, Ogunleye O, Iliyasu G, et al. Status of antimicrobial stewardship programmes in Nigerian tertiary healthcare facilities: findings and implications. J Global Antimicrob Resist. 2019;17:132–136. doi:10.1016/j.jgar.2018.11.025
   PubMed Web of Science ®Google Scholar
• Engler D, Meyer JC, Schellack N, Kurdi A, Godman B. Compliance with South Africa’s antimicrobial resistance national strategy framework: are we there yet? J Chemother. 2021;33(1):21–31. doi:10.1080/1120009X.2020.1789389
   PubMed Web of Science ®Google Scholar
• Kalungia AC, Mwambula H, Munkombwe D, et al. Antimicrobial stewardship knowledge and perception among physicians and pharmacists at leading tertiary teaching hospitals in Zambia: implications for future policy and practice. J Chemother. 2019;31(7–8):378–387. doi:10.1080/1120009X.2019.1622293
   PubMed Web of Science ®Google Scholar
• Babatola AO, Fadare JO, Olatunya OS, et al. Addressing antimicrobial resistance in Nigerian hospitals: exploring physicians prescribing behavior, knowledge and perception of antimicrobial resistance and stewardship programs. Expert Rev Anti Infect Ther. 2020;1–10. Doi:10.1080/14787210.2021.1829474
   Web of Science ®Google Scholar
• Firouzabadi D, Mahmoudi L. Knowledge, attitude, and practice of health care workers towards antibiotic resistance and antimicrobial stewardship programmes: a cross-sectional study. J Eval Clin Pract. 2020;26(1):190–196. doi:10.1111/jep.13177
   PubMed Web of Science ®Google Scholar
• Saleem Z, Hassali MA, Hashmi FK, Godman B, Ahmed Z. Snapshot of antimicrobial stewardship programs in the hospitals of Pakistan: findings and implications. Heliyon. 2019;5(7):e02159. doi:10.1016/j.heliyon.2019.e02159
   PubMed Web of Science ®Google Scholar
• Labi AK, Obeng-Nkrumah N, Bjerrum S, et al. Physicians’ knowledge, attitudes, and perceptions concerning antibiotic resistance: a survey in a Ghanaian tertiary care hospital. BMC Health Serv Res. 2018;18(1):126. doi:10.1186/s12913-018-2899-y
   PubMed Web of Science ®Google Scholar
• Singh S, Charani E, Wattal C, Arora A, Jenkins A, Nathwani D. The state of education and training for antimicrobial stewardship programs in indian hospitals-a qualitative and quantitative assessment. Antibiotics. 2019;8(1):11. doi:10.3390/antibiotics8010011
   Web of Science ®Google Scholar
• Hayat K, Rosenthal M, Gillani AH, et al. Perspective of key healthcare professionals on antimicrobial resistance and stewardship programs: a multicenter cross-sectional study from Pakistan. Front Pharmacol. 2020;10:1520. doi:10.3389/fphar.2019.01520
   PubMed Web of Science ®Google Scholar
• Ariyo P, Zayed B, Riese V, et al. Implementation strategies to reduce surgical site infections: a systematic review. Infect Control Hosp Epidemiol. 2019;40(3):287–300. doi:10.1017/ice.2018.355
   PubMed Web of Science ®Google Scholar
• World Bank. GDP per capita; 2020. Available from: https://data.worldbank.org/indicator/NY.GDP.PCAP.CD. Accessed January 8, 2021.
   Google Scholar
• Haque M, McKimm J, Godman B, Abu Bakar M, Sartelli M. Initiatives to reduce postoperative surgical site infections of the head and neck cancer surgery with a special emphasis on developing countries. Expert Rev Anticancer Ther. 2019;19(1):81–92. doi:10.1080/14737140.2019.1544497
   PubMed Web of Science ®Google Scholar
• Franco LM, Cota GF, Pinto TS, Ercole FF. Preoperative bathing of the surgical site with chlorhexidine for infection prevention: systematic review with meta-analysis. Am J Infect Control. 2017;45(4):343–349. doi:10.1016/j.ajic.2016.12.003
   PubMed Web of Science ®Google Scholar
• Shi D, Yao Y, Yu W. Comparison of preoperative hair removal methods for the reduction of surgical site infections: a meta-analysis. J Clin Nurs. 2017;26(19–20):2907–2914. doi:10.1111/jocn.13661
   PubMed Web of Science ®Google Scholar
• Yao R, Tan T, Tee JW, Street J. Prophylaxis of surgical site infection in adult spine surgery: a systematic review. J Clin Neurosci. 2018;52:5–25. doi:10.1016/j.jocn.2018.03.023
   PubMed Web of Science ®Google Scholar
• Schreiber PW, Sax H, Wolfensberger A, Clack L, Kuster SP. The preventable proportion of healthcare-associated infections 2005–2016: systematic review and meta-analysis. Infect Control Hosp Epidemiol. 2018;39(11):1277–1295. doi:10.1017/ice.2018.183
   PubMed Web of Science ®Google Scholar
• Boonchan T, Wilasrusmee C, McEvoy M, Attia J, Thakkinstian A. Network meta-analysis of antibiotic prophylaxis for prevention of surgical-site infection after groin hernia surgery. Br J Surg. 2017;104(2):e106–e17. doi:10.1002/bjs.10441
   PubMed Web of Science ®Google Scholar
• Godman B, Basu D, Pillay Y, et al. Review of ongoing activities and challenges to improve the care of patients with type 2 diabetes across Africa and the implications for the future. Front Pharmacol. 2020;11:108. doi:10.3389/fphar.2020.00108
   PubMed Web of Science ®Google Scholar
• Godman B, Grobler C, Van-De-Lisle M, et al. Pharmacotherapeutic interventions for bipolar disorder type II: addressing multiple symptoms and approaches with a particular emphasis on strategies in lower and middle-income countries. Expert Opin Pharmacother. 2019;20(18):2237–2255. doi:10.1080/14656566.2019.1684473
   PubMed Web of Science ®Google Scholar
• Godman B, McCabe H, Leong T et al. Fixed dose drug combinations - are they pharmacoeconomically sound? Findings and implications especially for lower- and middle-income countries. Expert Rev Pharmacoecon Outcomes Res. 2020;20(1):1–26. doi:10.1080/14737167.2020.1734456
   PubMed Web of Science ®Google Scholar
• Ogunleye OO, Basu D, Mueller D, et al. Response to the Novel Corona virus (COVID-19) pandemic across Africa: successes, challenges, and implications for the future. Front Pharmacol. 2020;11:1205.
   PubMed Web of Science ®Google Scholar
• Wettermark B, Godman B, Jacobsson B, Haaijer-Ruskamp FM. Soft regulations in pharmaceutical policy making: an overview of current approaches and their consequences. Appl Health Econ Health Policy. 2009;7(3):137–147. doi:10.1007/BF03256147
   PubMedGoogle Scholar
• Godman B. Health authority activities to enhance the quality and efficiency of medicine use and their impact. Adv Human Biol. 2021;11:11–16.
   Web of Science ®Google Scholar
• Godman B, Wettermark B, van Woerkom M, et al. Multiple policies to enhance prescribing efficiency for established medicines in Europe with a particular focus on demand-side measures: findings and future implications. Front Pharmacol. 2014;5:106. doi:10.3389/fphar.2014.00106
   PubMed Web of Science ®Google Scholar
• Niaz Q, Godman B, Massele A, et al. Validity of World Health Organisation prescribing indicators in Namibia’s primary healthcare: findings and implications. Int J Qual Health Care. 2019;31(5):338–345. doi:10.1093/intqhc/mzy172
   PubMed Web of Science ®Google Scholar
• Nakwatumbah S, Kibuule D, Godman B, et al. Compliance to guidelines for the prescribing of antibiotics in acute infections at Namibia’s national referral hospital: a pilot study and the implications. Expert Rev Anti Infect Ther. 2017;15(7):713–721. doi:10.1080/14787210.2017.1320220
   PubMed Web of Science ®Google Scholar
• Niaz Q, Godman B, Campbell S, Kibuule D. Compliance to prescribing guidelines among public health care facilities in Namibia; findings and implications. Int J Clin Pharm. 2020;42(4):1227–1236. doi:10.1007/s11096-020-01056-7
   PubMed Web of Science ®Google Scholar
• Hoffmann M. The right drug, but from whose perspective? A framework for analysing the structure and activities of drug and therapeutics committees. Eur J Clin Pharmacol. 2013;69(Suppl 1):79–87. doi:10.1007/s00228-013-1491-y
   PubMed Web of Science ®Google Scholar
• Matlala M, Gous AGS, Meyer JC, Godman B. Formulary management activities and practice implications among public sector hospital pharmaceutical and therapeutics committees in a South African Province. Front Pharmacol. 2020;11:1267. doi:10.3389/fphar.2020.01267
   PubMed Web of Science ®Google Scholar
• Matlala M, Gous AG, Godman B, Meyer JC. Structure and activities of pharmacy and therapeutics committees among public hospitals in South Africa; findings and implications. Expert Rev Clin Pharmacol. 2017;10(11):1273–1280. doi:10.1080/17512433.2017.1364625
   PubMed Web of Science ®Google Scholar
• Mpinda-Joseph P, Anand Paramadhas BD, Reyes G, et al. Healthcare-associated infections including neonatal bloodstream infections in a leading tertiary hospital in Botswana. Hosp Pract. 2019;47(4):203–210. doi:10.1080/21548331.2019.1650608
   PubMedGoogle Scholar
• Lee MH, Lee GA, Lee SH, Park YH. Effectiveness and core components of infection prevention and control programmes in long-term care facilities: a systematic review. J Hosp Infect. 2019;102(4):377–393. doi:10.1016/j.jhin.2019.02.008
   PubMed Web of Science ®Google Scholar
• Sharland M, Gandra S, Huttner B, et al. Encouraging AWaRe-ness and discouraging inappropriate antibiotic use-the new 2019 Essential Medicines List becomes a global antibiotic stewardship tool. Lancet Infect Dis. 2019;19(12):1278–1280. doi:10.1016/S1473-3099(19)30532-8
   PubMed Web of Science ®Google Scholar
• Saleem Z, Hassali MA, Godman B, et al. Sale of WHO AWaRe groups antibiotics without a prescription in Pakistan: a simulated client study. J Pharm Policy Pract. 2020;13(1):26. doi:10.1186/s40545-020-00233-3
   PubMedGoogle Scholar
• Mashaba TP, Matlala M, Godman B, Meyer JC. Implementation and monitoring of decisions by pharmacy and therapeutics committees in South African public sector hospitals. Expert Rev Clin Pharmacol. 2019;12(2):159–168. doi:10.1080/17512433.2018.1545572
   PubMed Web of Science ®Google Scholar
• Brooks J. US Medicare will stop paying for preventable errors. CMAJ. 2007;177(8):841–842. doi:10.1503/cmaj.071347
   PubMed Web of Science ®Google Scholar
• Alrasheedy AA, Alsalloum MA, Almuqbil FA, et al. The impact of law enforcement on dispensing antibiotics without prescription: a multi-methods study from Saudi Arabia. Expert Rev Anti Infect Ther. 2020;18(1):87–97. doi:10.1080/14787210.2020.1705156
   PubMed Web of Science ®Google Scholar
• Jacobs TG, Robertson J, van den Ham HA, Iwamoto K, Bak Pedersen H, Mantel-Teeuwisse AK. 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
   PubMed Web of Science ®Google Scholar
• Anand Paramadhas BD, Tiroyakgosi C, Mpinda-Joseph P, et al. Point prevalence study of antimicrobial use among hospitals across Botswana; findings and implications. Expert Rev Anti Infect Ther. 2019;17(7):535–546. doi:10.1080/14787210.2019.1629288
   PubMed Web of Science ®Google Scholar
• Talaat M, Saied T, Kandeel A, et al. A point prevalence survey of antibiotic use in 18 hospitals in Egypt. Antibiotics. 2014;3(3):450–460. doi:10.3390/antibiotics3030450
   Google Scholar
• Saied T, Hafez SF, Kandeel A, et al. Antimicrobial stewardship to optimize the use of antimicrobials for surgical prophylaxis in Egypt: a multicenter pilot intervention study. Am J Infect Control. 2015;43(11):e67–e71. doi:10.1016/j.ajic.2015.07.004
   PubMed Web of Science ®Google Scholar
• Ntumba P, Mwangi C, Barasa J, Aiken A, Kubilay Z, Allegranzi B. Multimodal approach for surgical site infection prevention – results from a pilot site in Kenya. Antimicrob Resist Infect Control. 2015;4(1):P87. doi:10.1186/2047-2994-4-S1-P87
   Google Scholar
• Okoth C, Opanga S, Okalebo F, Oluka M, Baker Kurdi A, Godman B. Point prevalence survey of antibiotic use and resistance at a referral hospital in Kenya: findings and implications. Hosp Pract. 2018;46(3):128–136. doi:10.1080/21548331.2018.1464872
   PubMedGoogle Scholar
• Oshikoya KA, Ogunyinka IA, Adamaigbo C, Olowo-Okere A. Surgical antimicrobial prophylaxis and its dose appropriateness among paediatric patients in a Nigerian teaching hospital. J Chemother. 2019;31(6):329–342. doi:10.1080/1120009X.2019.1615725
   PubMed Web of Science ®Google Scholar
• Fowotade A, Fasuyi T, Aigbovo O, et al. Point prevalence survey of antimicrobial prescribing in a Nigerian hospital: findings and implications on antimicrobial resistance. West Afr J Med. 2020;37(3):216–220.
   PubMedGoogle Scholar
• Saleem Z, Hassali MA, Versporten A, et al. A multicenter point prevalence survey of antibiotic use in Punjab, Pakistan: findings and implications. Expert Rev Anti Infect Ther. 2019;17(4):285–293. doi:10.1080/14787210.2019.1581063
   PubMed Web of Science ®Google Scholar
• Satti MZ, Hamza M, Sajid Z, et al. 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. 2019;11(5):e4776.
   PubMed Web of Science ®Google Scholar
• Kaya S, Aktas S, Senbayrak S, et al. An evaluation of surgical prophylaxis procedures in Turkey: a multi-center point prevalence study. Eurasian J Med. 2016;48(1):24–28. doi:10.5152/eurasianjmed.2015.15222
   PubMedGoogle Scholar
• Gomez MI, Acosta-Gnass SI, Mosqueda-Barboza L, Basualdo JA. Reduction in surgical antibiotic prophylaxis expenditure and the rate of surgical site infection by means of a protocol that controls the use of prophylaxis. Infect Control Hosp Epidemiol. 2006;27(12):1358–1365. doi:10.1017/S0195941700075305
   PubMed Web of Science ®Google Scholar
• Bozkurt F, Kaya S, Tekin R, et al. Analysis of antimicrobial consumption and cost in a teaching hospital. J Infect Public Health. 2014;7(2):161–169. doi:10.1016/j.jiph.2013.09.007
   PubMed Web of Science ®Google Scholar
• Kim RY, Kwakye G, Kwok AC, et al. Sustainability and long-term effectiveness of the WHO surgical safety checklist combined with pulse oximetry in a resource-limited setting: two-year update from Moldova. JAMA Surg. 2015;150(5):473–479. doi:10.1001/jamasurg.2014.3848
   PubMed Web of Science ®Google Scholar
• Brink AJ, Messina AP, Feldman C, Richards GA, van den Bergh D. From guidelines to practice: a pharmacist-driven prospective audit and feedback improvement model for peri-operative antibiotic prophylaxis in 34 South African hospitals. J Antimicrob Chemother. 2017;72(4):1227–1234. doi:10.1093/jac/dkw523
   PubMed Web of Science ®Google Scholar
• Allegranzi B, Aiken AM, Zeynep Kubilay N, et al. A multimodal infection control and patient safety intervention to reduce surgical site infections in Africa: a multicentre, before-after, cohort study. Lancet Infect Dis. 2018;18(5):507–515. doi:10.1016/S1473-3099(18)30107-5
   PubMed Web of Science ®Google Scholar
• Abubakar U, Syed Sulaiman SA, Adesiyun AG, Lo TS. Impact of pharmacist-led antibiotic stewardship interventions on compliance with surgical antibiotic prophylaxis in obstetric and gynecologic surgeries in Nigeria. PLoS One. 2019;14(3):e0213395. doi:10.1371/journal.pone.0213395
   PubMed Web of Science ®Google Scholar
• Ozgun H, Ertugrul BM, Soyder A, Ozturk B, Aydemir M. Peri-operative antibiotic prophylaxis: adherence to guidelines and effects of educational intervention. Int J Surg. 2010;8(2):159–163. doi:10.1016/j.ijsu.2009.12.005
   PubMed Web of Science ®Google Scholar
• Godman B, Shrank W, Andersen M, et al. Comparing policies to enhance prescribing efficiency in Europe through increasing generic utilization: changes seen and global implications. Expert Rev Pharmacoecon Outcomes Res. 2010;10(6):707–722. doi:10.1586/erp.10.72
   PubMed Web of Science ®Google Scholar
• Godman B, Wettermark B, Miranda J, Bennie M, Martin A, Malmstrom RE. Influence of multiple initiatives in Sweden to enhance ARB prescribing efficiency following generic losartan; findings and implications for other countries. Int J Clin Pract. 2013;67(9):853–862. doi:10.1111/ijcp.12130
   PubMed Web of Science ®Google Scholar
• Martin A, Godman B, Miranda J, et al. Measures to improve angiotensin receptor blocker prescribing efficiency in the UK: findings and implications. J Comp Eff Res. 2014;3(1):41–51. doi:10.2217/cer.13.83
   PubMed Web of Science ®Google Scholar
• Leporowski A, Godman B, Kurdi A, et al. Ongoing activities to optimize the quality and efficiency of lipid-lowering agents in the Scottish national health service: influence and implications. Expert Rev Pharmacoecon Outcomes Res. 2018;18(6):655–666. doi:10.1080/14737167.2018.1501558
   PubMed Web of Science ®Google Scholar
• Godman B, Kurdi A, McCabe H, et al. Ongoing initiatives within the Scottish National Health Service to affect the prescribing of selective serotonin reuptake inhibitors and their influence. J Comp Eff Res. 2019;8(7):535–547. doi:10.2217/cer-2018-0132
   PubMed Web of Science ®Google Scholar
• Furst J, Cizman M, Mrak J, et al. The influence of a sustained multifaceted approach to improve antibiotic prescribing in Slovenia during the past decade: findings and implications. Expert Rev Anti Infect Ther. 2015;13(2):279–289. doi:10.1586/14787210.2015.990381
   PubMed Web of Science ®Google Scholar
• Molstad S, Lofmark S, Carlin K, et al. Lessons learnt during 20 years of the Swedish strategic programme against antibiotic resistance. Bull World Health Organ. 2017;95(11):764–773. doi:10.2471/BLT.16.184374
   PubMed Web of Science ®Google Scholar
• Bao L, Peng R, Wang Y, et al. Significant reduction of antibiotic consumption and patients’ costs after an action plan in China, 2010–2014. PLoS One. 2015;10(3):e0118868. doi:10.1371/journal.pone.0118868
   PubMed Web of Science ®Google Scholar
• Godman B, Bishop I, Finlayson AE, Campbell S, Kwon HY, Bennie M. Reforms and initiatives in Scotland in recent years to encourage the prescribing of generic drugs, their influence and implications for other countries. Expert Rev Pharmacoecon Outcomes Res. 2013;13(4):469–482. doi:10.1586/14737167.2013.820956
   PubMed Web of Science ®Google Scholar
• Godman B, Petzold M, Bennett K, et al. Can authorities appreciably enhance the prescribing of oral generic risperidone to conserve resources? Findings from across Europe and their implications. BMC Med. 2014;12:98. doi:10.1186/1741-7015-12-98
   PubMed Web of Science ®Google Scholar
• Bennie M, Bishop I, Godman B, et al. Are prescribing initiatives readily transferable across classes: the case of generic losartan in Scotland? Qual Prim Care. 2013;21(1):7–15.
   PubMedGoogle Scholar
• Kim Y, Kwon H-Y, Godman B, Moorkens E, Simoens S, Bae S. Uptake of biosimilar infliximab in the UK, France, Japan, and Korea: budget savings or market expansion across countries? Front Pharmacol. 2020;11:970. doi:10.3389/fphar.2020.00970
   PubMed Web of Science ®Google Scholar
• Abilova V, Kurdi A, Godman B. Ongoing initiatives in Azerbaijan to improve the use of antibiotics; findings and implications. Expert Rev Anti Infect Ther. 2018;16(1):77–84. doi:10.1080/14787210.2018.1417835
   PubMed Web of Science ®Google Scholar
• Bojanic L, Markovic-Pekovic V, Skrbic R, et al. Recent initiatives in the Republic of Srpska to enhance appropriate use of antibiotics in ambulatory care; their influence and implications. Front Pharmacol. 2018;9:442. doi:10.3389/fphar.2018.00442
   PubMed Web of Science ®Google Scholar
• Wojkowska-Mach J, Godman B, Glassman A, et al. Antibiotic consumption and antimicrobial resistance in Poland; findings and implications. Antimicrob Resist Infect Control. 2018;7(1):136. doi:10.1186/s13756-018-0428-8
   PubMed Web of Science ®Google Scholar
• Campbell SM, Godman B, Diogene E, et al. Quality indicators as a tool in improving the introduction of new medicines. Basic Clin Pharmacol Toxicol. 2015;116(2):146–157. doi:10.1111/bcpt.12295
   PubMed Web of Science ®Google Scholar
• Robertson J, Iwamoto K, Hoxha I, et al. Antimicrobial medicines consumption in Eastern Europe and Central Asia – an updated cross-national study and assessment of quantitative metrics for policy action. Front Pharmacol. 2019;9:1156. doi:10.3389/fphar.2018.01156
   PubMed Web of Science ®Google Scholar
• Le Maréchal M, Tebano G, Monnier AA, et al. Quality indicators assessing antibiotic use in the outpatient setting: a systematic review followed by an international multidisciplinary consensus procedure. J Antimicrob Chemother. 2018;73(suppl_6):vi40–vi9. doi:10.1093/jac/dky117
   PubMed Web of Science ®Google Scholar
• Ghassemi S, Dehnavieh R. Applying the results of Health Technology Assessment reports in developing countries, the pale face of coin. Technol Health Care. 2016;24(5):781–782. doi:10.3233/THC-161233
   PubMed Web of Science ®Google Scholar
• Oortwijn W, van Oosterhout S, Kapiriri L. Application of evidence-informed deliberative processes in health technology assessment in low- and middle-income countries. Int J Technol Assess Health Care. 2020;1–5.
   PubMedGoogle Scholar
• Dehnavieh R, Noori Hekmat S, Ghasemi S, Mirshekari N. The vulnerable aspects of application of “Health Technology Assessment”. Int J Technol Assess Health Care. 2015;31(3):197–198. doi:10.1017/S0266462315000288
   PubMed Web of Science ®Google Scholar
• Oortwijn W, Determann D, Schiffers K, Tan SS, van der Tuin J. Towards integrated health technology assessment for improving decision making in selected countries. Value Health. 2017;20(8):1121–1130. doi:10.1016/j.jval.2017.03.011
   PubMed Web of Science ®Google Scholar
• WHO. Key elements for establishing a national system of HTA; 2020. Available from: https://www.who.int/health-technology-assessment/about/SYSTEMHTA/en/. Accessed January 8, 2021.
   Google Scholar
• Gustafsson LL, Wettermark B, Godman B, et al. The ‘wise list’- a comprehensive concept to select, communicate and achieve adherence to recommendations of essential drugs in ambulatory care in Stockholm. Basic Clin Pharmacol Toxicol. 2011;108(4):224–233. doi:10.1111/j.1742-7843.2011.00682.x
   PubMed Web of Science ®Google Scholar
• Eriksen J, Gustafsson LL, Ateva K, et al. High adherence to the ‘Wise List’ treatment recommendations in Stockholm: a 15-year retrospective review of a multifaceted approach promoting rational use of medicines. BMJ Open. 2017;7(4):e014345. doi:10.1136/bmjopen-2016-014345
   PubMed Web of Science ®Google Scholar
• Bjorkhem-Bergman L, Andersen-Karlsson E, Laing R, et al. Interface management of pharmacotherapy. Joint hospital and primary care drug recommendations. Eur J Clin Pharmacol. 2013;69(Suppl 1):73–78. doi:10.1007/s00228-013-1497-5
   PubMed Web of Science ®Google Scholar
• Yoon CH, Ritchie SR, Duffy EJ, et al. Impact of a smartphone app on prescriber adherence to antibiotic guidelines in adult patients with community acquired pneumonia or urinary tract infections. PLoS One. 2019;14(1):e0211157. doi:10.1371/journal.pone.0211157
   PubMed Web of Science ®Google Scholar
• Campbell SM, Kontopantelis E, Hannon K, Burke M, Barber A, Lester HE. Framework and indicator testing protocol for developing and piloting quality indicators for the UK quality and outcomes framework. BMC Fam Pract. 2011;12:85. doi:10.1186/1471-2296-12-85
   PubMed Web of Science ®Google Scholar
• Lorencatto F, Charani E, Sevdalis N, Tarrant C, Davey P. Driving sustainable change in antimicrobial prescribing practice: how can social and behavioural sciences help? J Antimicrob Chemother. 2018;73(10):2613–2624. doi:10.1093/jac/dky222
   PubMed Web of Science ®Google Scholar
• McGinn D, Godman B, Lonsdale J, Way R, Wettermark B, Haycox A. Initiatives to enhance the quality and efficiency of statin and PPI prescribing in the UK: impact and implications. Expert Rev Pharmacoecon Outcomes Res. 2010;10(1):73–85. doi:10.1586/erp.09.73
   PubMed Web of Science ®Google Scholar
• Schellack N, Bronkhorst E, Coetzee R, et al. SASOCP position statement on the pharmacist’s role in antibiotic stewardship 2018. South Afr J Infect Dis. 2018;33(1):28–35. doi:10.4102/sajid.v33i1.24
   Google Scholar
• Chigome AK, Matlala M, Godman B, Meyer JC. Availability and use of therapeutic interchange policies in managing antimicrobial shortages among South African public sector hospitals; findings and implications. Antibiotics. 2019;9(1):4. doi:10.3390/antibiotics9010004
   Web of Science ®Google Scholar