Assessing Antimicrobial Resistance, Utilization, and Stewardship in Yemen: An Exploratory Mixed-Methods Study

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;

Search for other papers by Ebiowei S. F. Orubu in
Current site
Google Scholar
PubMed
Close
,
Najwa Al-Dheeb Public Health Network, Aden, Yemen;

Search for other papers by Najwa Al-Dheeb in
Current site
Google Scholar
PubMed
Close
,
Carly Ching Department of Biomedical Engineering, College of Engineering, Boston University, Boston, Massachusetts;

Search for other papers by Carly Ching in
Current site
Google Scholar
PubMed
Close
,
Sima Bu Jawdeh Department of Biomedical Engineering, College of Engineering, Boston University, Boston, Massachusetts;

Search for other papers by Sima Bu Jawdeh in
Current site
Google Scholar
PubMed
Close
,
Jessica Anderson Department of Biomedical Engineering, College of Engineering, Boston University, Boston, Massachusetts;

Search for other papers by Jessica Anderson in
Current site
Google Scholar
PubMed
Close
,
Rashad Sheikh Public Health Network, Aden, Yemen;

Search for other papers by Rashad Sheikh in
Current site
Google Scholar
PubMed
Close
,
Fadhel Hariri Yemeni Pharmacovigilance Center, Aden, Yemen;

Search for other papers by Fadhel Hariri in
Current site
Google Scholar
PubMed
Close
,
Huda Basaleem Faculty of Medicine and Health Sciences, University of Aden, Yemen

Search for other papers by Huda Basaleem in
Current site
Google Scholar
PubMed
Close
, and
Muhammad H. Zaman Department of Biomedical Engineering, College of Engineering, Boston University, Boston, Massachusetts;

Search for other papers by Muhammad H. Zaman in
Current site
Google Scholar
PubMed
Close
Restricted access

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

Address correspondence to Ebiowei S. F. Orubu, Institute for Health System Innovation & Policy, Boston University, 44 Cummington Mall, Boston, MA 02215. E-mail: sforubu@bu.edu

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.

  • 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: 6373.

  • 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: 2633.

  • 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: E3463E3470.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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: 424429.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    Nwokike J , Clark A , Nguyen PP , 2018. Medicines quality assurance to fight antimicrobial resistance. Bull World Health Organ 96: 135137.

  • 10.

    Weinstein ZB , Zaman MH , 2019. Evolution of rifampin resistance in Escherichia coli and Mycobacterium smegmatis due to substandard drugs. Antimicrob Agents Chemother 63: e01243e18.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    WHO , 2020. Antimicrobial Resistance. Available at: https://www.who.int/news-room/fact-sheets/detail/antimicrobial-resistance. Accessed October 21, 2020.

    • PubMed
    • Export Citation
  • 13.

    WHO , 2019. AWaRe Policy Brief. Available at: https://adoptaware.org/assets/pdf/aware_policy_brief.pdf. Accessed October 23, 2020.

    • PubMed
    • Export Citation
  • 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: 356361.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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: 166168.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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: 803811.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Maltezou HC , Theodoridou M , Daikos GL , 2017. Antimicrobial resistance and the current refugee crisis. J Glob Antimicrob Resist 10: 7579.

  • 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.

    • PubMed
    • Export Citation
  • 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.

    • PubMed
    • Export Citation
  • 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.

    • PubMed
    • Export Citation
  • 23.

    Ibrahim MK , Zambruni M , Melby CL , Melby PC , 2017. Impact of childhood malnutrition on host defense and infection. Clin Microbiol Rev 30: 919971.

  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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: .

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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: 217223.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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: 11571160.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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: 231239.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    Banajeh SM , 2001. Bacterial aetiology and anti-microbial resistance of childhood diarrhoea in Yemen. J Trop Pediatr 47: 301302.

  • 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.

    • PubMed
    • Export Citation
  • 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.

    • PubMed
    • Export Citation
  • 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: 6169.

  • 35.

    Hertzog MA , 2008. Considerations in determining sample size for pilot studies. Res Nurs Health 31: 180191.

  • 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: 13751379.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39.

    XE , 2020. 3500 YER to USD, Convert Yemeni Rials to US Dollars. Available at: https://www.xe.com/currencyconverter/convert/?Amount=3%2C500&From=YER&To=USD. Accessed October 22, 2020.

    • PubMed
    • Export Citation
  • 40.

    World Bank , 2020. Yemen Overview. Available at: https://www.worldbank.org/en/country/yemen/overview. Accessed October 1, 2020.

    • PubMed
    • Export Citation
  • 41.

    World Bank , 2020. Yemen Monthly Economic Update April 2020. Available at: https://www.worldbank.org/en/country/yemen/publication/yemen-monthly-economic-update-april-2020. Accessed October 20, 2020.

    • PubMed
    • Export Citation
  • 42.

    Save the Children , 2018. YEMEN: Cost of Food Nearly Doubles, Putting Thousands of Lives at Risk. Available at: https://www.savethechildren.org/us/about-us/media-and-news/2018-press-releases/yeme-cost-of-food-nearly-doubles. Accessed October 20, 2020).

    • PubMed
    • Export Citation
  • 43.

    Davies J , Davies D , 2010. Origins and evolution of antibiotic resistance. Microbiol Mol Biol Rev 74: 417433.

  • 44.

    Olesen SW , Barnett ML , MacFadden DR , Brownstein JS , Hernández-Díaz S , Lipsitch M , Grad YH , 2018. The distribution of antibiotic use and its association with antibiotic resistance. eLife 7: e39435.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 45.

    Van Boeckel TP , Pires J , Silvester R , Zhao C , Song J , Criscuolo NG , Gilbert M , Bonhoeffer S , Laxminarayan R , 2019. Global trends in antimicrobial resistance in animals in low- and middle-income countries. Science 365: eaaw1944.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 46.

    Kimera ZI , Mshana SE , Rweyemamu MM , Mboera LEG , Matee MIN , 2020. Antimicrobial use and resistance in food-producing animals and the environment: an African perspective. Antimicrob Resist Infect Control 9: 37.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 47.

    International Displacement Monitoring Centre , 2020. Yemen. Available at: https://www.internal-displacement.org/countries/yemen. Accessed October 20, 2020.

    • PubMed
    • Export Citation
  • 48.

    Ali Al-Worafi YM , Fathelrahman AI , Ibrahim MIM & Wertheimer AI Pharmacy Practice in Developing Countries. Boston, MA: Academic Press, 267287.

  • 49.

    Halboup A , Alzoubi K , Othman G , 2018. Awareness of bacterial resistance to antibiotics among healthcare providers in Sana’a City, Yemen. YJMS 12: 1221.

  • 50.

    Basu S , Garg S , 2018. Antibiotic prescribing behavior among physicians: ethical challenges in resource-poor settings. J Med Ethics Hist Med 11: 5.

  • 51.

    Teixeira Rodrigues A , Roque F , Falcão A , Figueiras A , Herdeiro MT , 2013. Understanding physician antibiotic prescribing behaviour: a systematic review of qualitative studies. Int J Antimicrob Agents 41: 203212.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 52.

    Centre for Clinical Practice at NICE (United Kingdom) , 2008. Respiratory Tract Infections - Antibiotic Prescribing: Prescribing of Antibiotics for Self-Limiting Respiratory Tract Infections in Adults and Children in Primary Care. London, United Kingdom: National Institute for Health and Clinical Excellence.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 53.

    NICE , 2020. Summary of Antimicrobial Prescribing Guidance – Managing Common Infections. Public Health England. Available at: https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/906668/Common_Infect_PHE_context_references_and_rationale_August_2020.pdf. Accessed October 20, 2020.

    • PubMed
    • Export Citation
  • 54.

    Cross ELA , Tolfree R , Kipping R , 2017. Systematic review of public-targeted communication interventions to improve antibiotic use. J Antimicrob Chemother 72: 975987.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 55.

    Halboup A , Abdi A , Ahmed M , Al-Qadasi F , Othman GQ , 2020. Access to antibiotics without prescription in community pharmacies in Yemen during the political conflict. Public Health 183: 3035.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 56.

    Negarandeh R , Shayan SJ , Nazari R , Kiwanuka F , Rad SA , 2020. Self-Medication with Antibiotics in WHO Eastern Mediterranean Region: A Systematic Review and Meta-Analysis [Review]. doi: .

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 57.

    WHO , 2019. Yemen: Health Resources and Services Availability Mapping System 2018 (HeRAMS). Available at: https://www.who.int/initiatives/herams. Accessed December 12, 2020.

    • PubMed
    • Export Citation
  • 58.

    WHO , 2020. Global Health Observatory, By Category, Medical Doctors: Yemen. Available at: https://apps.who.int/gho/data/node.main.HWFGRP_0020?lang=en. Accessed 2020.

    • PubMed
    • Export Citation
  • 59.

    Sakeena MHF , Bennett AA , McLachlan AJ , 2018. Enhancing pharmacists’ role in developing countries to overcome the challenge of antimicrobial resistance: a narrative review. Antimicrob Resist Infect Control 7: 63.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 60.

    Gubbins PO , Klepser ME , Adams AJ , Jacobs DM , Percival KM , Tallman GB , 2017. Potential for pharmacy-public health collaborations using pharmacy-based point-of-care testing services for infectious diseases. J Public Health Manag Pract 23: 593600.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 61.

    Alshakka M , Said K , Babakri M , Ansari M , Aldhubhani A , Azmi Hassali M , Mohamed Ibrahim MI , 2016. A study on antibiotics prescribing pattern at outpatient department in four hospitals in Aden-Yemen. JPPCM 2: 8893.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 62.

    Alfadly S , Ballaswad MR , Amra AS , Alghadeer SM , Wajid S , Al-Arifi MN , Babelghaith SD , 2017. Self-medication with antibiotic amongst adults attending community pharmacies in Mukalla district, Yemen. Lat Am J Pharm 36: 224228.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 63.

    Mohanna M , 2010. Self-medication with antibiotic in children in Sana’a City, Yemen. Oman Med J 25: 4143.

  • 64.

    Diack A, Seiter A, Hawkins L, Dweik IS, 2010. Assessment of Governance and Corruption in the Pharmaceutical Sector. Washington, DC: The International Bank for Reconstruction and Development/The World Bank.

    • PubMed
    • Export Citation
  • 65.

    Alshakka M , Mohamed Ibrahim MI , Bahattab A , Badulla WFS , Shankar PR , 2020. An insight into the pharmaceutical sector in Yemen during conflict: challenges and recommendations. Med Confl Surviv 36: 232248.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 66.

    Mohamed Ibrahim MI , Alshami AK , Abdorabbo A , 2011. The quality of prescriptions with antibiotics in Yemen. J Clin Diagn Res 5: 808812.

  • 67.

    MSF , 2020. MSF Mini-Lab Project. Médecins Sans Frontières Access Campaign. Available at: https://msfaccess.org/msf-mini-lab-project. Accessed October 20, 2020.

    • PubMed
    • Export Citation
  • 68.

    Hays JP et al., 2019. The successful uptake and sustainability of rapid infectious disease and antimicrobial resistance point-of-care testing requires a complex “mix-and-match” implementation package. Eur J Clin Microbiol Infect Dis 38: 10151022.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 69.

    Alshakka M , Badulla WF , Alawi S , Al-abd N , Mahmoud MA , Alahmadi Y , Wajid S , Attef O , 2020. Status of antimicrobial stewardship in hospitals in Aden, Yemen. Lat Am J Pharm 39: 936943.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 70.

    Alshakka M , Badulla WF , Bahattab A , Al-Abd N , Mahmoud MA , Alahmadi Y , Wajid S , Attef O , 2019. Perception and practices of antimicrobial stewardship by community pharmacists in Aden-Yemen. Biomed Res 30: 819825.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 71.

    Dickerson LM , Mainous AG , Carek PJ , 2000. The pharmacist’s role in promoting optimal antimicrobial use. Pharmacotherapy 20: 711723.

  • 72.

    Weber NC , Klepser ME , Akers JM , Klepser DG , Adams AJ , 2016. Use of CLIA-waived point-of-care tests for infectious diseases in community pharmacies in the United States. Expert Rev Mol Diagn 16: 253264.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 73.

    WHO , 2019. Antimicrobial Stewardship Programmes in Health-care Facilities in Low- and Middle-income Countries: A WHO Practical Toolkit. Geneva, Switzerland: World Health Organization.

    • PubMed
    • Search Google Scholar
    • Export Citation
Past two years Past Year Past 30 Days
Abstract Views 1649 483 50
Full Text Views 223 56 0
PDF Downloads 179 14 0
 
 
 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save