• 1.

    Nathan C , Cars O , 2014. Antibiotic resistance: problems, progress, and prospects. N Engl J Med 371: 17611763.

  • 2.

    Rossolini GM , Arena F , Pecile P , Pollini S , 2014. Update on the antibiotic resistance crisis. Curr Opin Pharmacol 18: 5660.

  • 3.

    World Health Organization , 2014. Antimicrobial Resistance: Global Report on Surveillance. Geneva, Switzerland: WHO.

  • 4.

    Boerlin P , Reid-Smith RJ , 2008. Antimicrobial resistance: its emergence and transmission. Anim Health Res Rev 9: 115.

  • 5.

    Goldmann DA et al., 1996. Strategies to prevent and control the emergence and spread of antimicrobial-resistant microorganisms in hospitals: a challenge to hospital leadership. JAMA 275: 234240.

    • Search Google Scholar
    • Export Citation
  • 6.

    Baker S , Thomson N , Weill FX , Holt KE , 2018. Genomic insights into the emergence and spread of antimicrobial-resistant bacterial pathogens. Science 360: 733738.

    • Search Google Scholar
    • Export Citation
  • 7.

    Pärnänen K , Karkman A , Tamminen M , Lyra C , Hultman J , Paulin L , Virta M , 2016. Evaluating the mobility potential of antibiotic resistance genes in environmental resistomes without metagenomics. Sci Rep 6: 19.

    • Search Google Scholar
    • Export Citation
  • 8.

    Jasovský D , Littmann J , Zorzet A , Cars O , 2016. Antimicrobial resistance: a threat to the world’s sustainable development. Ups J Med Sci 121: 159164.

    • Search Google Scholar
    • Export Citation
  • 9.

    O’Neill J , 2014. Antimicrobial Resistance: Tackling a Crisis for the Health and Wealth of Nations: December 2014. London, UK: Review on Antimicrobial Resistance.

  • 10.

    Ampaire L et al., 2016. A review of antimicrobial resistance in East Africa. Afr J Lab Med 5: 16.

  • 11.

    Clinical Laboratory and Standard Institute , 2019. Performance Standards for Antimicrobial Susceptibility Testing, 29th edition. CLSI supplement M100. Wayne, PA: Clinical Laboratory Standards Institute.

    • Search Google Scholar
    • Export Citation
  • 12.

    WC W, 2006. Koneman’s Color Atlas and Textbook of Diagnostic Microbiology, 6th edition. Philadelphia, PA: Lippincott Williams & Wilkins, 845853.

    • Search Google Scholar
    • Export Citation
  • 13.

    Cheesbrough M , 2006. District Laboratory Practice in Tropical Countries Part 2. New York, NY: Cambridge University Press, 300301.

  • 14.

    Patel SS et al., 2017. Isolation and identification of Klebsiella pneumoniae from sheep: case report. Int J Curr Microbiol Appl Sci 6: 331334.

    • Search Google Scholar
    • Export Citation
  • 15.

    Aruhomukama D , 2020. Review of phenotypic assays for detection of extended-spectrum β-lactamases and carbapenemases: a microbiology laboratory bench guide. Afr Health Sci 20: 10901108.

    • Search Google Scholar
    • Export Citation
  • 16.

    Drieux L , Brossier F , Sougakoff W , Jarlier V , 2008. Phenotypic detection of extended‐spectrum β‐lactamase production in Enterobacteriaceae: review and bench guide. Clin Microbiol Infect 14: 90103.

    • Search Google Scholar
    • Export Citation
  • 17.

    Kateete DP , Nakanjako R , Namugenyi J , Erume J , Joloba ML , Najjuka CF , 2016. Carbapenem resistant Pseudomonas aeruginosa and Acinetobacter baumannii at Mulago Hospital in Kampala, Uganda (2007–2009). Springerplus 5: 111.

    • Search Google Scholar
    • Export Citation
  • 18.

    Parikh R , Mathai A , Parikh S , Sekhar GC , Thomas R , 2008. Understanding and using sensitivity, specificity and predictive values. Indian J Ophthalmol 56: 45.

    • Search Google Scholar
    • Export Citation
  • 19.

    Panta K , Ghimire P , Rai SK , Mukhiya RK , Singh RN , Rai G , 2013. Antibiogram typing of Gram negative isolates in different clinical samples of a tertiary hospital. Asian J Pharm Clin Res 6: 153156.

    • Search Google Scholar
    • Export Citation
  • 20.

    Flournoy DJ , 1982. Quantitative antibiogram as a potential tool for epidemiological typing. Infect Control Hosp Epidemiol 3: 384387.

    • Search Google Scholar
    • Export Citation
  • 21.

    Najjuka CF , Kateete DP , Kajumbula HM , Joloba ML , Essack SY , 2016. Antimicrobial susceptibility profiles of Escherichia coli and Klebsiella pneumoniae isolated from outpatients in urban and rural districts of Uganda. BMC Res Notes 9: 114.

    • Search Google Scholar
    • Export Citation
  • 22.

    Birgy A et al., 2012. Community faecal carriage of extended-spectrum beta-lactamase-producing Enterobacteriaceae in French children. BMC Infect Dis 12: 15.

    • Search Google Scholar
    • Export Citation
  • 23.

    Calva JJ , Sifuentes-Osornio J , Céron C , 1996. Antimicrobial resistance in fecal flora: longitudinal community-based surveillance of children from urban Mexico. Antimicrob Agents Chemother 40: 16991702.

    • Search Google Scholar
    • Export Citation
  • 24.

    Kouyos RD , Zur Wiesch PA , Bonhoeffer S , 2011. On being the right size: the impact of population size and stochastic effects on the evolution of drug resistance in hospitals and the community. PLoS Pathog 7: e1001334.

    • Search Google Scholar
    • Export Citation
  • 25.

    Kateregga JN , Kantume R , Atuhaire C , Lubowa MN , Ndukui JG , 2015. Phenotypic expression and prevalence of ESBL-producing Enterobacteriaceae in samples collected from patients in various wards of Mulago Hospital, Uganda. BMC Pharmacol Toxicol 16: 16.

    • Search Google Scholar
    • Export Citation
  • 26.

    Andrew B , Kagirita A , Bazira J , 2017. Prevalence of extended-spectrum beta-lactamases-producing microorganisms in patients admitted at KRRH, southwestern Uganda. Int J Microbiol 2017.

    • Search Google Scholar
    • Export Citation
  • 27.

    Naseer U , Haldorsen B , Simonsen GS , Sundsfjord A , 2010. Sporadic occurrence of CMY-2-producing multidrug-resistant Escherichia coli of ST-complexes 38 and 448, and ST131 in Norway. Clin Microbiol Infect 16: 171178.

    • Search Google Scholar
    • Export Citation
  • 28.

    Young BE , Lye DC , Krishnan P , Chan SP , Leo YS , 2014. A prospective observational study of the prevalence and risk factors for colonization by antibiotic resistant bacteria in patients at admission to hospital in Singapore. BMC Infect Dis 14: 17.

    • Search Google Scholar
    • Export Citation
  • 29.

    Woerther PL et al., 2013. Characterization of fecal extended-spectrum-β-lactamase-producing Escherichia coli in a remote community during a long time period. Antimicrob Agents Chemother 57: 50605066.

    • Search Google Scholar
    • Export Citation
  • 30.

    Bailey JK , Pinyon JL , Anantham S , Hall RM , 2010. Commensal Escherichia coli of healthy humans: a reservoir for antibiotic-resistance determinants. J Med Microbiol 59: 13311339.

    • Search Google Scholar
    • Export Citation
  • 31.

    Overdevest I et al., 2011. Extended-spectrum β-lactamase genes of Escherichia coli in chicken meat and humans, the Netherlands. Emerg Infect Dis 17: 1216.

    • Search Google Scholar
    • Export Citation
  • 32.

    Sharma S , Zapatero-Rodríguez J , Estrela P , O’Kennedy R , 2015. Point-of-care diagnostics in low resource settings: present status and future role of microfluidics. Biosensors (Basel) 5: 577601.

    • Search Google Scholar
    • Export Citation
  • 33.

    Diaz Granados CA , Cardo DM , McGowan JE Jr ., 2008. Antimicrobial resistance: international control strategies, with a focus on limited-resource settings. Int J Antimicrob Agents 32: 19.

    • Search Google Scholar
    • Export Citation
  • 34.

    Wee BA , Muloi DM , van Bunnik BA , 2020. Quantifying the transmission of antimicrobial resistance at the human and livestock interface with genomics. Clin Microbiol Infect.

    • Search Google Scholar
    • Export Citation
  • 35.

    European Food Safety Authority, European Centre for Disease Prevention and Control , 2015. EU summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2013. EFSA J 13: 4036.

    • Search Google Scholar
    • Export Citation
  • 36.

    Sserwadda I , Lukenge M , Mwambi B , Mboowa G , Walusimbi A , Segujja F , 2018. Microbial contaminants isolated from items and work surfaces in the post-operative ward at Kawolo General Hospital, Uganda. BMC Infect Dis 18: 16.

    • Search Google Scholar
    • Export Citation
  • 37.

    Weber DJ , Anderson D , Rutala WA , 2013. The role of the surface environment in healthcare-associated infections. Curr Opin Infect Dis 26: 338344.

    • Search Google Scholar
    • Export Citation
  • 38.

    Allegranzi B , Pittet D , 2009. Role of hand hygiene in healthcare-associated infection prevention. J Hosp Infect 73: 305315.

  • 39.

    van den Dool C , Haenen A , Leenstra T , Wallinga J , 2016. The role of nursing homes in the spread of antimicrobial resistance over the healthcare network. Infect Control Hosp Epidemiol 37: 761767.

    • Search Google Scholar
    • Export Citation
  • 40.

    Kigera JWM , 2010. Patterns of spine surgeries at Mulago Hospital. East Afr Orthop J 4.

  • 41.

    Akinyemi KO , Atapu AD , Adetona OO , Coker AO , 2009. The potential role of mobile phones in the spread of bacterial infections. J Infect Dev Countries 3: 628632.

    • Search Google Scholar
    • Export Citation
  • 42.

    Shobo CO et al., 2020. Bacterial diversity and functional profile of microbial populations on surfaces in public hospital environments in South Africa: a high throughput metagenomic analysis. Sci Total Environ 719: 137360.

    • Search Google Scholar
    • Export Citation
  • 43.

    Seni J et al., 2013. Antimicrobial resistance in hospitalized surgical patients: a silently emerging public health concern in Uganda. BMC Res Notes 6: 17.

    • Search Google Scholar
    • Export Citation
  • 44.

    Pena C et al., 2006. Risk-factors for acquisition of extended-spectrum β-lactamase-producing Escherichia coli among hospitalised patients. Clin Microbiol Infect 12: 279284.

    • Search Google Scholar
    • Export Citation
  • 45.

    George EA , Sankar S , Jesudasan MV , Sudandiradoss C , Nandagopal B , 2014. Incidence of extended spectrum beta lactamase producing Escherichia coli among patients, healthy individuals and in the environment. Indian J Med Microbiol 32.

    • Search Google Scholar
    • Export Citation
  • 46.

    Babu R , Kumar A , Karim S , Warrier S , Nair SG , Singh SK , Biswas R , 2016. Faecal carriage rate of extended-spectrum β-lactamase-producing Enterobacteriaceae in hospitalised patients and healthy asymptomatic individuals coming for health check-up. J Glob Antimicrob Resist 6: 150153.

    • Search Google Scholar
    • Export Citation
  • 47.

    Aruhomukama D , Sserwadda I , Mboowa G , 2019. Investigating colistin drug resistance: the role of high-throughput sequencing and bioinformatics. F1000 Res 8.

    • Search Google Scholar
    • Export Citation
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Transmission Dynamics of Antimicrobial Resistance at a National Referral Hospital in Uganda

Gerald MboowaDepartment of Immunology and Molecular Biology, College of Health Sciences, School of Biomedical Sciences, Makerere University, Kampala, Uganda;
African Center of Excellence in Bioinformatics and Data Intensive Sciences, The Infectious Disease Institute, Makerere University, Kampala, Uganda;

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Ivan SserwaddaDepartment of Immunology and Molecular Biology, College of Health Sciences, School of Biomedical Sciences, Makerere University, Kampala, Uganda;

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Douglas BulafuDepartment of Disease Control and Environmental Health, School of Public Health, College of Health Sciences, Makerere University, Kampala, Uganda;

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Duku ChaplainClinical Microbiology Laboratory, Mulago National Referral Hospital, Kampala, Uganda;
Clinical Microbiology Laboratory, Mbarara University Teaching Hospital Mbarara, Uganda;

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Izale WewedruClinical Microbiology Laboratory, Mulago National Referral Hospital, Kampala, Uganda;

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Jeremiah SeniDepartment of Microbiology and Immunology, Catholic University of Health and Allied Sciences, Bugando, Mwanza, Tanzania;

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Benson KidenyaDepartment of Microbiology and Immunology, Catholic University of Health and Allied Sciences, Bugando, Mwanza, Tanzania;

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Stephen MshanaDepartment of Microbiology and Immunology, Catholic University of Health and Allied Sciences, Bugando, Mwanza, Tanzania;

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Moses JolobaDepartment of Immunology and Molecular Biology, College of Health Sciences, School of Biomedical Sciences, Makerere University, Kampala, Uganda;
Department of Medical Microbiology, College of Health Sciences, School of Biomedical Sciences, Makerere University, Kampala, Uganda

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Dickson AruhomukamaDepartment of Immunology and Molecular Biology, College of Health Sciences, School of Biomedical Sciences, Makerere University, Kampala, Uganda;
Department of Medical Microbiology, College of Health Sciences, School of Biomedical Sciences, Makerere University, Kampala, Uganda

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ABSTRACT.

Reliable data on antimicrobial resistance (AMR) transmission dynamics in Uganda remains scarce; hence, we studied this area. Eighty-six index patients and “others” were recruited. Index patients were those who had been admitted to the orthopedic ward of Mulago National Referral Hospital during the study period; “others” included medical and non-medical caretakers of the index patients, and index patients’ immediate admitted hospital neighbors. Others were recruited only when index patients became positive for carrying antimicrobial-resistant bacteria (ARB) during their hospital stay. A total of 149 samples, including those from the inanimate environment, were analyzed microbiologically for ARB, and ARB were analyzed for their antimicrobial susceptibility profiles and mechanisms underlying observed resistances. We describe the diagnostic accuracy of the extended-spectrum β-lactamase (ESBL) production screening method, and AMR acquisition and transmission dynamics. Index patients were mostly carriers of ESBL-producing Enterobacteriaceae (PE) on admission, whereas non-ESBL-PE carriers on admission (61%) became carriers after 48 hours of admission (9%). The majority of ESBL-PE carriers on admission (56%) were referrals or transfers from other health-care facilities. Only 1 of 46 samples from the environment isolated an ESBL-PE. Marked resistance (> 90%) to β-lactams and folate-pathway inhibitors were observed. The ESBL screening method’s sensitivity, specificity, positive predictive value, and negative predictive value were 100%, 50%, 90%, and 100%, respectively. AMR acquisition and transmission occurs via human–human interfaces within and outside of health-care facilities compared with human–inanimate environment interfaces. However, this remains subject to further research.

Author Notes

Address correspondence to Dickson Aruhomukama, Department of Immunology and Molecular Biology, College of Health Sciences, School of Biomedical Sciences, Makerere University, P.O. Box 7072, Kampala, Uganda. E-mail: dickson.aruhomukama@chs.mak.ac.ug

Financial support: This work was supported through the Grand Challenges Africa program (grant no. GCA/AMR/rnd2/058). Grand Challenges Africa is a program of the African Academy of Sciences (AAS) implemented through the Alliance for Accelerating Excellence in Science in Africa platform, an initiative of the AAS and the African Union Development Agency. Grand Challenges Africa is supported by the Bill & Melinda Gates Foundation, and AAS and its partners.

Disclaimer: The views expressed herein are those of the authors and not necessarily those of the AAS and its partners.

Authors’ addresses: Gerald Mboowa, Department of Immunology and Molecular Biology, College of Health Sciences, School of Biomedical Sciences, Makerere University, Kampala, Uganda, and African Center of Excellence in Bioinformatics and Data Intensive Sciences, The Infectious Disease Institute, Makerere University, Kampala, Uganda, E-mail: gerald.mboowa@chs.mak.ac.ug. Ivan Sserwadda, Department of Immunology and Molecular Biology, College of Health Sciences, School of Biomedical Sciences, Makerere University, Kampala, Uganda, E-mail: ivangunz23@gmail.com. Douglas Bulafu, Department of Disease Control and Environmental Health, School of Public Health, College of Health Sciences, Makerere University, Kampala, Uganda, E-mail: bulafudouglas@gmail.com. Duku Chaplain, Clinical Microbiology Laboratory, Mulago National Referral Hospital, Kampala, Uganda, and Clinical Microbiology Laboratory, Mbarara University Teaching Hospital Mbarara, Uganda, E-mail: chaplain.duku@yahoo.com. Izale Wewedru, Clinical Microbiology Laboratory, Mulago National Referral Hospital, Kampala, Uganda, E-mail: wewedruiza@hotmail.com. Jeremiah Seni, Benson Kidenya, and Stephen Mshana, Department of Microbiology and Immunology, Catholic University of Health and Allied Sciences, Bugando, Mwanza, Tanzania, E-mails: senijj80@gmail.com, benkidenya@gmail.com, and stephen72mshana@gmail.com. Moses Joloba and Dickson Aruhomukama, Department of Immunology and Molecular Biology, College of Health Sciences, School of Biomedical Sciences, Makerere University, Kampala, Uganda, and Department of Medical Microbiology, College of Health Sciences, School of Biomedical Sciences, Makerere University, Kampala, Uganda, E-mails: mlj10@case.edu and dickson.aruhomukama@chs.mak.ac.ug.

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