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Assessing Antimicrobial Resistance, Utilization, and Stewardship in Yemen: An Exploratory Mixed-Methods Study
Ebiowei S. F. Orubu
Ebiowei S. F. Orubu
Institute for Health System Innovation & Policy, Boston University, Boston, Massachusetts;
Department of Biomedical Engineering, College of Engineering, Boston University, Boston, Massachusetts;
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Department of Biomedical Engineering, College of Engineering, Boston University, Boston, Massachusetts;
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Najwa Al-Dheeb
Najwa Al-Dheeb
Public Health Network, Aden, Yemen;
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Carly Ching
Carly Ching
Department of Biomedical Engineering, College of Engineering, Boston University, Boston, Massachusetts;
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Sima Bu Jawdeh
Sima Bu Jawdeh
Department of Biomedical Engineering, College of Engineering, Boston University, Boston, Massachusetts;
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Jessica Anderson
Jessica Anderson
Department of Biomedical Engineering, College of Engineering, Boston University, Boston, Massachusetts;
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Rashad Sheikh
Rashad Sheikh
Public Health Network, Aden, Yemen;
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Fadhel Hariri
Fadhel Hariri
Yemeni Pharmacovigilance Center, Aden, Yemen;
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Huda Basaleem
Huda Basaleem
Faculty of Medicine and Health Sciences, University of Aden, Yemen
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Muhammad H. Zaman
Muhammad H. Zaman
Department of Biomedical Engineering, College of Engineering, Boston University, Boston, Massachusetts;
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ABSTRACT.
Antimicrobial resistance (AMR), largely driven by irrational use of antimicrobials, is a global, multifaceted problem calling for a complete understanding of all contributory factors for effective containment. In conflict settings, war-wounds and malnutrition can combine with existing social determinants to increase demand for antibiotics, compounding irrational use. In this study, we focus on Yemen, a low-income country with active conflict for the last 5 years, and analyze the current status of awareness and stewardship efforts regarding AMR. We performed a survey of prescribers/physicians and pharmacists to describe perceptions of AMR prevalence, antibiotic use practices, and stewardship in Yemen, supported by a nonsystematic scoping literature review and a key informant interview. Participants (96%, N = 54) reported a perceived high AMR prevalence rate. Prescribers (74%, 20/27) reported pressure to prescribe broad-spectrum antibiotics. In the majority of cases (81%, 22/27), antimicrobial sensitivity tests (AST) were not performed to inform antibiotic choice. The main barrier to AST was cost. Most pharmacists (67%, 18/27) sold antibiotics without prescriptions. Amoxicillin (including amoxicillin-clavulanate) was the most-commonly prescribed (63%, 17/27) or dispensed (81%, 22/27) antibiotic. AST was rated the least important solution to AMR in Yemen. While there was awareness of a high AMR rate, stewardship is poor in Yemen. We note that barriers to the use of AST could be addressed through the deployment of reliable, affordable, quality rapid diagnostics, and AST kits. Compulsory continuing education emphasizing the use of AST to guide prescribing and patients’ awareness programs could help avoid irrational use.
- Supplemental Materials (DOCX 54 KB)
Author Notes
Financial support: We confirm no financial support was received for this project.
Disclosure: Ethical clearance (REC-81-2020) was obtained from the Research Ethics Committee of the University of Aden – in line with similar studies – before questionnaires were distributed.24
Authors’ addresses: Ebiowei S. F. Orubu, Institute for Health System Innovation & Policy, Boston University, Boston, MA, E-mail: sforubu@bu.edu. Najwa Al-Dheeb and Rashad Sheikh Public Health Network, Aden, Yemen, E-mails: nyaldheeb@gmail.com and rashadinwork@gmail.com. Carly Ching, Department of Biomedical Engineering, College of Engineering, Boston University, Boston, MA, E-mail: chingc@bu.edu. Sima Bu Jawdeh, Jessica Anderson, and Muhammad H. Zaman, Department of Biomedical Engineering, College of Engineering, Boston University, Boston, MA, E-mails: simabujawdeh@gmail.com, andersoj@bu.edu, and zaman@bu.edu. Fadhel Hariri, Yemeni Pharmacovigilance Center, Aden, Yemen, E-mail: ypvcsbd59@gmail.com. Huda Basaleem, Faculty of Medicine and Health Sciences, University of Aden, Yemen, E-mail: hudabasaleem92@yahoo.com.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
World Bank , 2017. Drug-Resistant Infections: A Threat to Our Economic Future. Washington, DC: The World Bank.
-
2.
Kirchhelle C et al., 2020. Setting the standard: multidisciplinary hallmarks for structural, equitable and tracked antibiotic policy. BMJ Glob Health 5: e003091.
-
3.
Haraoui DL-P , 2019. Armed conflicts and antimicrobial resistance: A deadly convergence. AMR Control 2019: 63–73.
-
4.
Abbara A et al., 2018. A summary and appraisal of existing evidence of antimicrobial resistance in the Syrian conflict. Int J Infect Dis 75: 26–33.
-
5.
Kanapathipillai R et al., 2019. Antibiotic resistance in conflict settings: lessons learned in the Middle East. JAC-Antimicrob Res 1: dlz002.
-
6.
Collignon P , McEwen S , 2019. One health—its importance in helping to better control antimicrobial resistance. TropicalMed 4: 22.
-
7.
Klein EY , Van Boeckel TP , Martinez EM , Pant S , Gandra S , Levin SA , Goossens H , Laxminarayan R , 2018. Global increase and geographic convergence in antibiotic consumption between 2000 and 2015. Proc Natl Acad Sci USA 115: E3463–E3470.
-
8.
Belkina T , Al Warafi A , Hussein Eltom E , Tadjieva N , Kubena A , Vlcek J , 2014. Antibiotic use and knowledge in the community of Yemen, Saudi Arabia, and Uzbekistan. J Infect Dev Ctries 8: 424–429.
-
9.
Nwokike J , Clark A , Nguyen PP , 2018. Medicines quality assurance to fight antimicrobial resistance. Bull World Health Organ 96: 135–137.
-
10.
Weinstein ZB , Zaman MH , 2019. Evolution of rifampin resistance in Escherichia coli and Mycobacterium smegmatis due to substandard drugs. Antimicrob Agents Chemother 63: e01243–e18.
-
11.
Ramay BM et al., 2020. Antibiotic use and hygiene interact to influence the distribution of antimicrobial-resistant bacteria in low-income communities in Guatemala. Sci Rep 10: 13767.
-
12.
WHO , 2020. Antimicrobial Resistance. Available at: https://www.who.int/news-room/fact-sheets/detail/antimicrobial-resistance. Accessed October 21, 2020.
-
13.
WHO , 2019. AWaRe Policy Brief. Available at: https://adoptaware.org/assets/pdf/aware_policy_brief.pdf. Accessed October 23, 2020.
-
14.
Dau AA , Tloba S , Daw MA , 2013. Characterization of wound infections among patients injured during the 2011 Libyan conflict. East Mediterr Health J 19: 356–361.
-
15.
Bazzi W et al., 2020. Heavy metal toxicity in armed conflicts potentiates AMR in A. baumannii by selecting for antibiotic and heavy metal co-resistance mechanisms. Front Microbiol 11: 68.
-
16.
Kassem DF , Hoffmann Y , Shahar N , Ocampo S , Salomon L , Zonis Z , Glikman D , 2017. Multidrug-resistant pathogens in hospitalized Syrian children. Emerg Infect Dis 23: 166–168.
-
17.
Petersen K , Riddle MS , Danko JR , Blazes DL , Hayden R , Tasker SA , Dunne JR , 2007. Trauma-related infections in battlefield casualties from Iraq. Ann Surg 245: 803–811.
-
18.
Älgå A , Wong S , Shoaib M , Lundgren K , Giske CG , von Schreeb J , Malmstedt J , 2018. Infection with high proportion of multidrug-resistant bacteria in conflict-related injuries is associated with poor outcomes and excess resource consumption: a cohort study of Syrian patients treated in Jordan. BMC Infect Dis 18: 233.
-
19.
Maltezou HC , Theodoridou M , Daikos GL , 2017. Antimicrobial resistance and the current refugee crisis. J Glob Antimicrob Resist 10: 75–79.
-
20.
United Nations , 2019. Humanitarian Crisis in Yemen Remains the Worst in the World, Warns UN. Available at: https://news.un.org/en/story/2019/02/1032811. Accessed February 14, 2019.
-
21.
WHO EMRO , 2020. Outbreak Update – Cholera in Yemen, 12 January 2020, Cholera | Epidemic and Pandemic Diseases. Available at: http://www.emro.who.int/pandemic-epidemic-diseases/cholera/outbreak-update-cholera-in-yemen-12-january-2020.html. Accessed October 21, 2020.
-
22.
United Nations , 2020. Yemeni Children Suffer Record Rates of Acute Malnutrition, Putting ‘Entire Generation’ at Risk. Available at: https://news.un.org/en/story/2020/10/1076272. Accessed October 27, 2020.
-
23.
Ibrahim MK , Zambruni M , Melby CL , Melby PC , 2017. Impact of childhood malnutrition on host defense and infection. Clin Microbiol Rev 30: 919–971.
-
24.
Badulla WFS , Alshakka M , Mohamed Ibrahim MI , 2020. Antimicrobial resistance profiles for different isolates in Aden, Yemen: a cross-sectional study in a resource-poor setting. BioMed Res Int 2020: 1810290.
-
25.
AL-Magrami RTF, Al-Shamahy HA , 2019. Pseudomonas aeruginosa skin-nasopharyngeal colonization in the in-patients: Prevalence, risk factors and antibiotic resistance in tertiary hospitals in Sana’a City - Yemen .Univ J Pharm Res. doi: .
-
26.
Al-Haddad AM , Ghouth A , El-Hosseiny M , 2010. Microbial resistance in patients with urinary tract infections in Al-Mukalla, Yemen. Sudan J Med Sci 5: 145–149.
-
27.
Al-Haroni MH , Skaug N , Al-Hebshi NN , 2006. Prevalence of subgingival bacteria resistant to aminopenicillins and metronidazole in dental patients from Yemen and Norway. Int J Antimicrob Agents 27: 217–223.
-
28.
Al-Moyed KA , Harmal NS , Al-Harasy AH , Al-Shamahy HA , 2006. Increasing single and multi-antibiotic resistance in Shigella species isolated from shigellosis patients in Sana’a, Yemen. Saudi Med J 27: 1157–1160.
-
29.
Al-Hammadi MA , Al-Shamahy HA , Ali AQ , Abdulghani MAM , Pyar H , AL-Suboal I , 2020. Class 1 integrons in clinical multi drug resistance E. coli, Sana’a Hospitals, Yemen. Pak J Biol Sci 23: 231–239.
-
30.
Banajeh SM , 2001. Bacterial aetiology and anti-microbial resistance of childhood diarrhoea in Yemen. J Trop Pediatr 47: 301–302.
-
31.
Anon , 2020. Yemen: Going Behind the Front Lines of a Hidden War. Doctors Without Borders – USA. Available at: https://www.doctorswithoutborders.org/what-we-do/news-stories/story/yemen-going-behind-front-lines-hidden-war. Accessed October 20, 2020.
-
32.
Nasser A , 2020. COVID-19 in Yemen – A Perfect Storm. Human Rights Watch. Available at: https://www.hrw.org/news/2020/04/14/covid-19-yemen-perfect-storm. Accessed April 14, 2020.
-
33.
WHO , 2020. Global Antimicrobial Resistance Surveillance System (GLASS) Report: Early Implementation 2020. Geneva, Switzerland: World Health Organization.
-
34.
Leech NL , Onwuegbuzie AJ , 2010. Guidelines for conducting and reporting mixed research in the field of counseling and beyond. J Couns Dev 88: 61–69.
-
35.
Hertzog MA , 2008. Considerations in determining sample size for pilot studies. Res Nurs Health 31: 180–191.
-
36.
Viechtbauer W , Smits L , Kotz D , Budé L , Spigt M , Serroyen J , Crutzen R , 2015. A simple formula for the calculation of sample size in pilot studies. J Clin Epidemiol 68: 1375–1379.
-
37.
WHO , 2015. Global Action Plan on Antimicrobial Resistance. Geneva, Switzerland: World Health Organization.
-
38.
World Health Organization , 2019. The 2019 WHO AWaRe Classification of Antibiotics for Evaluation and Monitoring of Use. Geneva, Switzerland: World Health Organization.
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