Multicountry Distribution and Characterization of Extended-spectrum β-Lactamase-associated Gram-negative Bacteria from Bloodstream Infections in Sub-Saharan Africa

Trevor Toy, Gi Deok Pak, Trung Pham Duc, James I. Campbell, Muna Ahmed El Tayeb, Vera Von Kalckreuth, Justin Im, Ursula Panzner, Ligia Maria Cruz Espinoza, Daniel Eibach, Denise Myriam Dekker, Se Eun Park, Hyon Jin Jeon, Frank Konings, Ondari D. Mogeni, Leonard Cosmas, Morten Bjerregaard-Andersen, Nagla Gasmelseed, Julian T. Hertz, Anna Jaeger & 30 others Ralf Krumkamp, Benedikt Ley, Kamala Thriemer, Leon Parfait Kabore, Aissatou Niang, Tiana Mirana Raminosoa, Emmanuel Sampo, Nimako Sarpong, Abdramane Soura, Ellis Owusu-Dabo, Mekonnen Teferi, Biruk Yeshitela, Sven Poppert, Jürgen May, Jerome H. Kim, Yun Chon, Jin Kyung Park, Abroaham Aseffa, Robert F. Breiman, Heidi Schütt-Gerowitt, Peter Aaby, Yaw Adu-Sarkodie, John A. Crump, Raphaël Rakotozandrindrainy, Christian G. Meyer, Amy Gassama Sow, John D. Clemens, Thomas F. Wierzba, Stephen Baker, Florian Marks

    Research output: Contribution to journalArticleResearchpeer-review

    Abstract

    Background: Antimicrobial resistance (AMR) is a major global health concern, yet, there are noticeable gaps in AMR surveillance data in regions such as sub-Saharan Africa. We aimed to measure the prevalence of extended-spectrum β-lactamase (ESBL) producing Gram-negative bacteria in bloodstream infections from 12 sentinel sites in sub-Saharan Africa. 

    Methods: Data were generated during the Typhoid Fever Surveillance in Africa Program (TSAP), in which standardized blood cultures were performed on febrile patients attending 12 health facilities in 9 sub-Saharan African countries between 2010 and 2014. Pathogenic bloodstream isolates were identified at the sites and then subsequently confirmed at a central reference laboratory. Antimicrobial susceptibility testing, detection of ESBL production, and conventional multiplex polymerase chain reaction (PCR) testing for genes encoding for β-lactamase were performed on all pathogens. 

    Results: Five hundred and five pathogenic Gram-negative bloodstream isolates were isolated during the study period and available for further characterization. This included 423 Enterobacteriaceae. Phenotypically, 61 (12.1%) isolates exhibited ESBL activity, and genotypically, 47 (9.3%) yielded a PCR amplicon for at least one of the screened ESBL genes. Among specific Gram-negative isolates, 40 (45.5%) of 88 Klebsiella spp., 7 (5.7%) of 122 Escherichia coli, 6 (16.2%) of 37 Acinetobacter spp., and 2 (1.3%) of 159 of nontyphoidal Salmonella (NTS) showed phenotypic ESBL activity. 

    Conclusions: Our findings confirm the presence of ESBL production among pathogens causing bloodstream infections in sub-Saharan Africa. With few alternatives for managing ESBL-producing pathogens in the African setting, measures to control the development and proliferation of AMR organisms are urgently needed.

    Original languageEnglish
    Pages (from-to)S449-S458
    Number of pages10
    JournalClinical Infectious Diseases
    Volume69
    Issue numberSupplement_6
    DOIs
    Publication statusPublished - 30 Oct 2019

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    Africa South of the Sahara
    Gram-Negative Bacteria
    Infection
    Acinetobacter
    Klebsiella
    Typhoid Fever
    Multiplex Polymerase Chain Reaction
    Health Facilities
    Enterobacteriaceae
    Salmonella
    Genes
    Fever
    Escherichia coli
    Polymerase Chain Reaction

    Cite this

    Toy, Trevor ; Pak, Gi Deok ; Duc, Trung Pham ; Campbell, James I. ; El Tayeb, Muna Ahmed ; Von Kalckreuth, Vera ; Im, Justin ; Panzner, Ursula ; Cruz Espinoza, Ligia Maria ; Eibach, Daniel ; Dekker, Denise Myriam ; Park, Se Eun ; Jeon, Hyon Jin ; Konings, Frank ; Mogeni, Ondari D. ; Cosmas, Leonard ; Bjerregaard-Andersen, Morten ; Gasmelseed, Nagla ; Hertz, Julian T. ; Jaeger, Anna ; Krumkamp, Ralf ; Ley, Benedikt ; Thriemer, Kamala ; Kabore, Leon Parfait ; Niang, Aissatou ; Raminosoa, Tiana Mirana ; Sampo, Emmanuel ; Sarpong, Nimako ; Soura, Abdramane ; Owusu-Dabo, Ellis ; Teferi, Mekonnen ; Yeshitela, Biruk ; Poppert, Sven ; May, Jürgen ; Kim, Jerome H. ; Chon, Yun ; Park, Jin Kyung ; Aseffa, Abroaham ; Breiman, Robert F. ; Schütt-Gerowitt, Heidi ; Aaby, Peter ; Adu-Sarkodie, Yaw ; Crump, John A. ; Rakotozandrindrainy, Raphaël ; Meyer, Christian G. ; Sow, Amy Gassama ; Clemens, John D. ; Wierzba, Thomas F. ; Baker, Stephen ; Marks, Florian. / Multicountry Distribution and Characterization of Extended-spectrum β-Lactamase-associated Gram-negative Bacteria from Bloodstream Infections in Sub-Saharan Africa. In: Clinical Infectious Diseases. 2019 ; Vol. 69, No. Supplement_6. pp. S449-S458.
    @article{bc8aaaa898c84939a4a976cc31e5b4a7,
    title = "Multicountry Distribution and Characterization of Extended-spectrum β-Lactamase-associated Gram-negative Bacteria from Bloodstream Infections in Sub-Saharan Africa",
    abstract = "Background: Antimicrobial resistance (AMR) is a major global health concern, yet, there are noticeable gaps in AMR surveillance data in regions such as sub-Saharan Africa. We aimed to measure the prevalence of extended-spectrum β-lactamase (ESBL) producing Gram-negative bacteria in bloodstream infections from 12 sentinel sites in sub-Saharan Africa. Methods: Data were generated during the Typhoid Fever Surveillance in Africa Program (TSAP), in which standardized blood cultures were performed on febrile patients attending 12 health facilities in 9 sub-Saharan African countries between 2010 and 2014. Pathogenic bloodstream isolates were identified at the sites and then subsequently confirmed at a central reference laboratory. Antimicrobial susceptibility testing, detection of ESBL production, and conventional multiplex polymerase chain reaction (PCR) testing for genes encoding for β-lactamase were performed on all pathogens. Results: Five hundred and five pathogenic Gram-negative bloodstream isolates were isolated during the study period and available for further characterization. This included 423 Enterobacteriaceae. Phenotypically, 61 (12.1{\%}) isolates exhibited ESBL activity, and genotypically, 47 (9.3{\%}) yielded a PCR amplicon for at least one of the screened ESBL genes. Among specific Gram-negative isolates, 40 (45.5{\%}) of 88 Klebsiella spp., 7 (5.7{\%}) of 122 Escherichia coli, 6 (16.2{\%}) of 37 Acinetobacter spp., and 2 (1.3{\%}) of 159 of nontyphoidal Salmonella (NTS) showed phenotypic ESBL activity. Conclusions: Our findings confirm the presence of ESBL production among pathogens causing bloodstream infections in sub-Saharan Africa. With few alternatives for managing ESBL-producing pathogens in the African setting, measures to control the development and proliferation of AMR organisms are urgently needed.",
    keywords = "Africa, antibiotic resistance, antimicrobial resistance, ESBL, extended-spectrum β-lactamase, surveillance",
    author = "Trevor Toy and Pak, {Gi Deok} and Duc, {Trung Pham} and Campbell, {James I.} and {El Tayeb}, {Muna Ahmed} and {Von Kalckreuth}, Vera and Justin Im and Ursula Panzner and {Cruz Espinoza}, {Ligia Maria} and Daniel Eibach and Dekker, {Denise Myriam} and Park, {Se Eun} and Jeon, {Hyon Jin} and Frank Konings and Mogeni, {Ondari D.} and Leonard Cosmas and Morten Bjerregaard-Andersen and Nagla Gasmelseed and Hertz, {Julian T.} and Anna Jaeger and Ralf Krumkamp and Benedikt Ley and Kamala Thriemer and Kabore, {Leon Parfait} and Aissatou Niang and Raminosoa, {Tiana Mirana} and Emmanuel Sampo and Nimako Sarpong and Abdramane Soura and Ellis Owusu-Dabo and Mekonnen Teferi and Biruk Yeshitela and Sven Poppert and J{\"u}rgen May and Kim, {Jerome H.} and Yun Chon and Park, {Jin Kyung} and Abroaham Aseffa and Breiman, {Robert F.} and Heidi Sch{\"u}tt-Gerowitt and Peter Aaby and Yaw Adu-Sarkodie and Crump, {John A.} and Rapha{\"e}l Rakotozandrindrainy and Meyer, {Christian G.} and Sow, {Amy Gassama} and Clemens, {John D.} and Wierzba, {Thomas F.} and Stephen Baker and Florian Marks",
    year = "2019",
    month = "10",
    day = "30",
    doi = "10.1093/cid/ciz450",
    language = "English",
    volume = "69",
    pages = "S449--S458",
    journal = "Clinical Infectious Diseases",
    issn = "1058-4838",
    publisher = "Oxford University Press",
    number = "Supplement_6",

    }

    Toy, T, Pak, GD, Duc, TP, Campbell, JI, El Tayeb, MA, Von Kalckreuth, V, Im, J, Panzner, U, Cruz Espinoza, LM, Eibach, D, Dekker, DM, Park, SE, Jeon, HJ, Konings, F, Mogeni, OD, Cosmas, L, Bjerregaard-Andersen, M, Gasmelseed, N, Hertz, JT, Jaeger, A, Krumkamp, R, Ley, B, Thriemer, K, Kabore, LP, Niang, A, Raminosoa, TM, Sampo, E, Sarpong, N, Soura, A, Owusu-Dabo, E, Teferi, M, Yeshitela, B, Poppert, S, May, J, Kim, JH, Chon, Y, Park, JK, Aseffa, A, Breiman, RF, Schütt-Gerowitt, H, Aaby, P, Adu-Sarkodie, Y, Crump, JA, Rakotozandrindrainy, R, Meyer, CG, Sow, AG, Clemens, JD, Wierzba, TF, Baker, S & Marks, F 2019, 'Multicountry Distribution and Characterization of Extended-spectrum β-Lactamase-associated Gram-negative Bacteria from Bloodstream Infections in Sub-Saharan Africa', Clinical Infectious Diseases, vol. 69, no. Supplement_6, pp. S449-S458. https://doi.org/10.1093/cid/ciz450

    Multicountry Distribution and Characterization of Extended-spectrum β-Lactamase-associated Gram-negative Bacteria from Bloodstream Infections in Sub-Saharan Africa. / Toy, Trevor; Pak, Gi Deok; Duc, Trung Pham; Campbell, James I.; El Tayeb, Muna Ahmed; Von Kalckreuth, Vera; Im, Justin; Panzner, Ursula; Cruz Espinoza, Ligia Maria; Eibach, Daniel; Dekker, Denise Myriam; Park, Se Eun; Jeon, Hyon Jin; Konings, Frank; Mogeni, Ondari D.; Cosmas, Leonard; Bjerregaard-Andersen, Morten; Gasmelseed, Nagla; Hertz, Julian T.; Jaeger, Anna; Krumkamp, Ralf; Ley, Benedikt; Thriemer, Kamala; Kabore, Leon Parfait; Niang, Aissatou; Raminosoa, Tiana Mirana; Sampo, Emmanuel; Sarpong, Nimako; Soura, Abdramane; Owusu-Dabo, Ellis; Teferi, Mekonnen; Yeshitela, Biruk; Poppert, Sven; May, Jürgen; Kim, Jerome H.; Chon, Yun; Park, Jin Kyung; Aseffa, Abroaham; Breiman, Robert F.; Schütt-Gerowitt, Heidi; Aaby, Peter; Adu-Sarkodie, Yaw; Crump, John A.; Rakotozandrindrainy, Raphaël; Meyer, Christian G.; Sow, Amy Gassama; Clemens, John D.; Wierzba, Thomas F.; Baker, Stephen; Marks, Florian.

    In: Clinical Infectious Diseases, Vol. 69, No. Supplement_6, 30.10.2019, p. S449-S458.

    Research output: Contribution to journalArticleResearchpeer-review

    TY - JOUR

    T1 - Multicountry Distribution and Characterization of Extended-spectrum β-Lactamase-associated Gram-negative Bacteria from Bloodstream Infections in Sub-Saharan Africa

    AU - Toy, Trevor

    AU - Pak, Gi Deok

    AU - Duc, Trung Pham

    AU - Campbell, James I.

    AU - El Tayeb, Muna Ahmed

    AU - Von Kalckreuth, Vera

    AU - Im, Justin

    AU - Panzner, Ursula

    AU - Cruz Espinoza, Ligia Maria

    AU - Eibach, Daniel

    AU - Dekker, Denise Myriam

    AU - Park, Se Eun

    AU - Jeon, Hyon Jin

    AU - Konings, Frank

    AU - Mogeni, Ondari D.

    AU - Cosmas, Leonard

    AU - Bjerregaard-Andersen, Morten

    AU - Gasmelseed, Nagla

    AU - Hertz, Julian T.

    AU - Jaeger, Anna

    AU - Krumkamp, Ralf

    AU - Ley, Benedikt

    AU - Thriemer, Kamala

    AU - Kabore, Leon Parfait

    AU - Niang, Aissatou

    AU - Raminosoa, Tiana Mirana

    AU - Sampo, Emmanuel

    AU - Sarpong, Nimako

    AU - Soura, Abdramane

    AU - Owusu-Dabo, Ellis

    AU - Teferi, Mekonnen

    AU - Yeshitela, Biruk

    AU - Poppert, Sven

    AU - May, Jürgen

    AU - Kim, Jerome H.

    AU - Chon, Yun

    AU - Park, Jin Kyung

    AU - Aseffa, Abroaham

    AU - Breiman, Robert F.

    AU - Schütt-Gerowitt, Heidi

    AU - Aaby, Peter

    AU - Adu-Sarkodie, Yaw

    AU - Crump, John A.

    AU - Rakotozandrindrainy, Raphaël

    AU - Meyer, Christian G.

    AU - Sow, Amy Gassama

    AU - Clemens, John D.

    AU - Wierzba, Thomas F.

    AU - Baker, Stephen

    AU - Marks, Florian

    PY - 2019/10/30

    Y1 - 2019/10/30

    N2 - Background: Antimicrobial resistance (AMR) is a major global health concern, yet, there are noticeable gaps in AMR surveillance data in regions such as sub-Saharan Africa. We aimed to measure the prevalence of extended-spectrum β-lactamase (ESBL) producing Gram-negative bacteria in bloodstream infections from 12 sentinel sites in sub-Saharan Africa. Methods: Data were generated during the Typhoid Fever Surveillance in Africa Program (TSAP), in which standardized blood cultures were performed on febrile patients attending 12 health facilities in 9 sub-Saharan African countries between 2010 and 2014. Pathogenic bloodstream isolates were identified at the sites and then subsequently confirmed at a central reference laboratory. Antimicrobial susceptibility testing, detection of ESBL production, and conventional multiplex polymerase chain reaction (PCR) testing for genes encoding for β-lactamase were performed on all pathogens. Results: Five hundred and five pathogenic Gram-negative bloodstream isolates were isolated during the study period and available for further characterization. This included 423 Enterobacteriaceae. Phenotypically, 61 (12.1%) isolates exhibited ESBL activity, and genotypically, 47 (9.3%) yielded a PCR amplicon for at least one of the screened ESBL genes. Among specific Gram-negative isolates, 40 (45.5%) of 88 Klebsiella spp., 7 (5.7%) of 122 Escherichia coli, 6 (16.2%) of 37 Acinetobacter spp., and 2 (1.3%) of 159 of nontyphoidal Salmonella (NTS) showed phenotypic ESBL activity. Conclusions: Our findings confirm the presence of ESBL production among pathogens causing bloodstream infections in sub-Saharan Africa. With few alternatives for managing ESBL-producing pathogens in the African setting, measures to control the development and proliferation of AMR organisms are urgently needed.

    AB - Background: Antimicrobial resistance (AMR) is a major global health concern, yet, there are noticeable gaps in AMR surveillance data in regions such as sub-Saharan Africa. We aimed to measure the prevalence of extended-spectrum β-lactamase (ESBL) producing Gram-negative bacteria in bloodstream infections from 12 sentinel sites in sub-Saharan Africa. Methods: Data were generated during the Typhoid Fever Surveillance in Africa Program (TSAP), in which standardized blood cultures were performed on febrile patients attending 12 health facilities in 9 sub-Saharan African countries between 2010 and 2014. Pathogenic bloodstream isolates were identified at the sites and then subsequently confirmed at a central reference laboratory. Antimicrobial susceptibility testing, detection of ESBL production, and conventional multiplex polymerase chain reaction (PCR) testing for genes encoding for β-lactamase were performed on all pathogens. Results: Five hundred and five pathogenic Gram-negative bloodstream isolates were isolated during the study period and available for further characterization. This included 423 Enterobacteriaceae. Phenotypically, 61 (12.1%) isolates exhibited ESBL activity, and genotypically, 47 (9.3%) yielded a PCR amplicon for at least one of the screened ESBL genes. Among specific Gram-negative isolates, 40 (45.5%) of 88 Klebsiella spp., 7 (5.7%) of 122 Escherichia coli, 6 (16.2%) of 37 Acinetobacter spp., and 2 (1.3%) of 159 of nontyphoidal Salmonella (NTS) showed phenotypic ESBL activity. Conclusions: Our findings confirm the presence of ESBL production among pathogens causing bloodstream infections in sub-Saharan Africa. With few alternatives for managing ESBL-producing pathogens in the African setting, measures to control the development and proliferation of AMR organisms are urgently needed.

    KW - Africa

    KW - antibiotic resistance

    KW - antimicrobial resistance

    KW - ESBL

    KW - extended-spectrum β-lactamase

    KW - surveillance

    UR - http://www.scopus.com/inward/record.url?scp=85074337131&partnerID=8YFLogxK

    U2 - 10.1093/cid/ciz450

    DO - 10.1093/cid/ciz450

    M3 - Article

    VL - 69

    SP - S449-S458

    JO - Clinical Infectious Diseases

    JF - Clinical Infectious Diseases

    SN - 1058-4838

    IS - Supplement_6

    ER -