Trends in antimicrobial resistance in bloodstream infection isolates at a large urban hospital in Malawi (1998–2016): a surveillance study

Patrick Musicha, Jennifer E. Cornick, Naor Bar-Zeev, Neil French, Clemens Masesa, Brigitte Denis, Neil Kennedy, Jane Mallewa, Melita A. Gordon, Chisomo L. Msefula, Robert S. Heyderman, Dean B. Everett, Nicholas A. Feasey

Research output: Contribution to journalArticle

Abstract

Background Bacterial bloodstream infection is a common cause of morbidity and mortality in sub-Saharan Africa, yet few facilities are able to maintain long-term surveillance. The Malawi-Liverpool-Wellcome Trust Clinical Research Programme has done sentinel surveillance of bacteraemia since 1998. We report long-term trends in bloodstream infection and antimicrobial resistance from this surveillance. Methods In this surveillance study, we analysed blood cultures that were routinely taken from adult and paediatric patients with fever or suspicion of sepsis admitted to Queen Elizabeth Central Hospital, Blantyre, Malawi from 1998 to 2016. The hospital served an urban population of 920 000 in 2016, with 1000 beds, although occupancy often exceeds capacity. The hospital admits about 10 000 adults and 30 000 children each year. Antimicrobial susceptibility tests were done by the disc diffusion method according to British Society of Antimicrobial Chemotherapy guidelines. We used the Cochran-Armitage test for trend to examine trends in rates of antimicrobial resistance, and negative binomial regression to examine trends in icidence of bloodstream infection over time. Findings Between Jan 1, 1998, and Dec 31, 2016, we isolated 29 183 pathogens from 194 539 blood cultures. Pathogen detection decreased significantly from 327·1/100 000 in 1998 to 120·2/100 000 in 2016 (p<0·0001). 13 366 (51·1%) of 26 174 bacterial isolates were resistant to the Malawian first-line antibiotics amoxicillin or penicillin, chloramphenicol, and co-trimoxazole; 68·3% of Gram-negative and 6·6% of Gram-positive pathogens. The proportions of non-Salmonella Enterobacteriaceae with extended spectrum beta-lactamase (ESBL) or fluoroquinolone resistance rose significantly after 2003 to 61·9% in 2016 (p<0·0001). Between 2003 and 2016, ESBL resistance rose from 0·7% to 30·3% in Escherichia coli, from 11·8% to 90·5% in Klebsiella spp and from 30·4% to 71·9% in other Enterobacteriaceae. Similarly, resistance to ciprofloxacin rose from 2·5% to 31·1% in E coli, from 1·7% to 70·2% in Klebsiella spp and from 5·9% to 68·8% in other Enterobacteriaceae. By contrast, more than 92·0% of common Gram-positive pathogens remain susceptible to either penicillin or chloramphenicol. Meticillin-resistant Staphylococcus aureus (MRSA) was first reported in 1998 at 7·7% and represented 18·4% of S aureus isolates in 2016. Interpretation The rapid expansion of ESBL and fluoroquinolone resistance among common Gram-negative pathogens, and the emergence of MRSA, highlight the growing challenge of bloodstream infections that are effectively impossible to treat in this resource-limited setting. Funding Wellcome Trust, H3ABionet, Southern Africa Consortium for Research Excellence (SACORE).

Original languageEnglish (US)
Pages (from-to)1042-1052
Number of pages11
JournalThe Lancet Infectious Diseases
Volume17
Issue number10
DOIs
StatePublished - Oct 1 2017
Externally publishedYes

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Malawi
Urban Hospitals
Enterobacteriaceae
beta-Lactamases
Methicillin
Klebsiella
Fluoroquinolones
Chloramphenicol
Penicillins
Staphylococcus aureus
Bed Occupancy
Infection
Sentinel Surveillance
Escherichia coli
Southern Africa
Urban Population
Africa South of the Sahara
Amoxicillin
Sulfamethoxazole Drug Combination Trimethoprim
Ciprofloxacin

ASJC Scopus subject areas

  • Infectious Diseases

Cite this

Trends in antimicrobial resistance in bloodstream infection isolates at a large urban hospital in Malawi (1998–2016) : a surveillance study. / Musicha, Patrick; Cornick, Jennifer E.; Bar-Zeev, Naor; French, Neil; Masesa, Clemens; Denis, Brigitte; Kennedy, Neil; Mallewa, Jane; Gordon, Melita A.; Msefula, Chisomo L.; Heyderman, Robert S.; Everett, Dean B.; Feasey, Nicholas A.

In: The Lancet Infectious Diseases, Vol. 17, No. 10, 01.10.2017, p. 1042-1052.

Research output: Contribution to journalArticle

Musicha, P, Cornick, JE, Bar-Zeev, N, French, N, Masesa, C, Denis, B, Kennedy, N, Mallewa, J, Gordon, MA, Msefula, CL, Heyderman, RS, Everett, DB & Feasey, NA 2017, 'Trends in antimicrobial resistance in bloodstream infection isolates at a large urban hospital in Malawi (1998–2016): a surveillance study', The Lancet Infectious Diseases, vol. 17, no. 10, pp. 1042-1052. https://doi.org/10.1016/S1473-3099(17)30394-8
Musicha, Patrick ; Cornick, Jennifer E. ; Bar-Zeev, Naor ; French, Neil ; Masesa, Clemens ; Denis, Brigitte ; Kennedy, Neil ; Mallewa, Jane ; Gordon, Melita A. ; Msefula, Chisomo L. ; Heyderman, Robert S. ; Everett, Dean B. ; Feasey, Nicholas A. / Trends in antimicrobial resistance in bloodstream infection isolates at a large urban hospital in Malawi (1998–2016) : a surveillance study. In: The Lancet Infectious Diseases. 2017 ; Vol. 17, No. 10. pp. 1042-1052.
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abstract = "Background Bacterial bloodstream infection is a common cause of morbidity and mortality in sub-Saharan Africa, yet few facilities are able to maintain long-term surveillance. The Malawi-Liverpool-Wellcome Trust Clinical Research Programme has done sentinel surveillance of bacteraemia since 1998. We report long-term trends in bloodstream infection and antimicrobial resistance from this surveillance. Methods In this surveillance study, we analysed blood cultures that were routinely taken from adult and paediatric patients with fever or suspicion of sepsis admitted to Queen Elizabeth Central Hospital, Blantyre, Malawi from 1998 to 2016. The hospital served an urban population of 920 000 in 2016, with 1000 beds, although occupancy often exceeds capacity. The hospital admits about 10 000 adults and 30 000 children each year. Antimicrobial susceptibility tests were done by the disc diffusion method according to British Society of Antimicrobial Chemotherapy guidelines. We used the Cochran-Armitage test for trend to examine trends in rates of antimicrobial resistance, and negative binomial regression to examine trends in icidence of bloodstream infection over time. Findings Between Jan 1, 1998, and Dec 31, 2016, we isolated 29 183 pathogens from 194 539 blood cultures. Pathogen detection decreased significantly from 327·1/100 000 in 1998 to 120·2/100 000 in 2016 (p<0·0001). 13 366 (51·1{\%}) of 26 174 bacterial isolates were resistant to the Malawian first-line antibiotics amoxicillin or penicillin, chloramphenicol, and co-trimoxazole; 68·3{\%} of Gram-negative and 6·6{\%} of Gram-positive pathogens. The proportions of non-Salmonella Enterobacteriaceae with extended spectrum beta-lactamase (ESBL) or fluoroquinolone resistance rose significantly after 2003 to 61·9{\%} in 2016 (p<0·0001). Between 2003 and 2016, ESBL resistance rose from 0·7{\%} to 30·3{\%} in Escherichia coli, from 11·8{\%} to 90·5{\%} in Klebsiella spp and from 30·4{\%} to 71·9{\%} in other Enterobacteriaceae. Similarly, resistance to ciprofloxacin rose from 2·5{\%} to 31·1{\%} in E coli, from 1·7{\%} to 70·2{\%} in Klebsiella spp and from 5·9{\%} to 68·8{\%} in other Enterobacteriaceae. By contrast, more than 92·0{\%} of common Gram-positive pathogens remain susceptible to either penicillin or chloramphenicol. Meticillin-resistant Staphylococcus aureus (MRSA) was first reported in 1998 at 7·7{\%} and represented 18·4{\%} of S aureus isolates in 2016. Interpretation The rapid expansion of ESBL and fluoroquinolone resistance among common Gram-negative pathogens, and the emergence of MRSA, highlight the growing challenge of bloodstream infections that are effectively impossible to treat in this resource-limited setting. Funding Wellcome Trust, H3ABionet, Southern Africa Consortium for Research Excellence (SACORE).",
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TY - JOUR

T1 - Trends in antimicrobial resistance in bloodstream infection isolates at a large urban hospital in Malawi (1998–2016)

T2 - a surveillance study

AU - Musicha, Patrick

AU - Cornick, Jennifer E.

AU - Bar-Zeev, Naor

AU - French, Neil

AU - Masesa, Clemens

AU - Denis, Brigitte

AU - Kennedy, Neil

AU - Mallewa, Jane

AU - Gordon, Melita A.

AU - Msefula, Chisomo L.

AU - Heyderman, Robert S.

AU - Everett, Dean B.

AU - Feasey, Nicholas A.

PY - 2017/10/1

Y1 - 2017/10/1

N2 - Background Bacterial bloodstream infection is a common cause of morbidity and mortality in sub-Saharan Africa, yet few facilities are able to maintain long-term surveillance. The Malawi-Liverpool-Wellcome Trust Clinical Research Programme has done sentinel surveillance of bacteraemia since 1998. We report long-term trends in bloodstream infection and antimicrobial resistance from this surveillance. Methods In this surveillance study, we analysed blood cultures that were routinely taken from adult and paediatric patients with fever or suspicion of sepsis admitted to Queen Elizabeth Central Hospital, Blantyre, Malawi from 1998 to 2016. The hospital served an urban population of 920 000 in 2016, with 1000 beds, although occupancy often exceeds capacity. The hospital admits about 10 000 adults and 30 000 children each year. Antimicrobial susceptibility tests were done by the disc diffusion method according to British Society of Antimicrobial Chemotherapy guidelines. We used the Cochran-Armitage test for trend to examine trends in rates of antimicrobial resistance, and negative binomial regression to examine trends in icidence of bloodstream infection over time. Findings Between Jan 1, 1998, and Dec 31, 2016, we isolated 29 183 pathogens from 194 539 blood cultures. Pathogen detection decreased significantly from 327·1/100 000 in 1998 to 120·2/100 000 in 2016 (p<0·0001). 13 366 (51·1%) of 26 174 bacterial isolates were resistant to the Malawian first-line antibiotics amoxicillin or penicillin, chloramphenicol, and co-trimoxazole; 68·3% of Gram-negative and 6·6% of Gram-positive pathogens. The proportions of non-Salmonella Enterobacteriaceae with extended spectrum beta-lactamase (ESBL) or fluoroquinolone resistance rose significantly after 2003 to 61·9% in 2016 (p<0·0001). Between 2003 and 2016, ESBL resistance rose from 0·7% to 30·3% in Escherichia coli, from 11·8% to 90·5% in Klebsiella spp and from 30·4% to 71·9% in other Enterobacteriaceae. Similarly, resistance to ciprofloxacin rose from 2·5% to 31·1% in E coli, from 1·7% to 70·2% in Klebsiella spp and from 5·9% to 68·8% in other Enterobacteriaceae. By contrast, more than 92·0% of common Gram-positive pathogens remain susceptible to either penicillin or chloramphenicol. Meticillin-resistant Staphylococcus aureus (MRSA) was first reported in 1998 at 7·7% and represented 18·4% of S aureus isolates in 2016. Interpretation The rapid expansion of ESBL and fluoroquinolone resistance among common Gram-negative pathogens, and the emergence of MRSA, highlight the growing challenge of bloodstream infections that are effectively impossible to treat in this resource-limited setting. Funding Wellcome Trust, H3ABionet, Southern Africa Consortium for Research Excellence (SACORE).

AB - Background Bacterial bloodstream infection is a common cause of morbidity and mortality in sub-Saharan Africa, yet few facilities are able to maintain long-term surveillance. The Malawi-Liverpool-Wellcome Trust Clinical Research Programme has done sentinel surveillance of bacteraemia since 1998. We report long-term trends in bloodstream infection and antimicrobial resistance from this surveillance. Methods In this surveillance study, we analysed blood cultures that were routinely taken from adult and paediatric patients with fever or suspicion of sepsis admitted to Queen Elizabeth Central Hospital, Blantyre, Malawi from 1998 to 2016. The hospital served an urban population of 920 000 in 2016, with 1000 beds, although occupancy often exceeds capacity. The hospital admits about 10 000 adults and 30 000 children each year. Antimicrobial susceptibility tests were done by the disc diffusion method according to British Society of Antimicrobial Chemotherapy guidelines. We used the Cochran-Armitage test for trend to examine trends in rates of antimicrobial resistance, and negative binomial regression to examine trends in icidence of bloodstream infection over time. Findings Between Jan 1, 1998, and Dec 31, 2016, we isolated 29 183 pathogens from 194 539 blood cultures. Pathogen detection decreased significantly from 327·1/100 000 in 1998 to 120·2/100 000 in 2016 (p<0·0001). 13 366 (51·1%) of 26 174 bacterial isolates were resistant to the Malawian first-line antibiotics amoxicillin or penicillin, chloramphenicol, and co-trimoxazole; 68·3% of Gram-negative and 6·6% of Gram-positive pathogens. The proportions of non-Salmonella Enterobacteriaceae with extended spectrum beta-lactamase (ESBL) or fluoroquinolone resistance rose significantly after 2003 to 61·9% in 2016 (p<0·0001). Between 2003 and 2016, ESBL resistance rose from 0·7% to 30·3% in Escherichia coli, from 11·8% to 90·5% in Klebsiella spp and from 30·4% to 71·9% in other Enterobacteriaceae. Similarly, resistance to ciprofloxacin rose from 2·5% to 31·1% in E coli, from 1·7% to 70·2% in Klebsiella spp and from 5·9% to 68·8% in other Enterobacteriaceae. By contrast, more than 92·0% of common Gram-positive pathogens remain susceptible to either penicillin or chloramphenicol. Meticillin-resistant Staphylococcus aureus (MRSA) was first reported in 1998 at 7·7% and represented 18·4% of S aureus isolates in 2016. Interpretation The rapid expansion of ESBL and fluoroquinolone resistance among common Gram-negative pathogens, and the emergence of MRSA, highlight the growing challenge of bloodstream infections that are effectively impossible to treat in this resource-limited setting. Funding Wellcome Trust, H3ABionet, Southern Africa Consortium for Research Excellence (SACORE).

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