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1. Colonisation of hospital surfaces from low- and middle-income countries by extended spectrum β-lactamase- and carbapenemase-producing bacteria

Author

Maria Nieto-Rosado, Kirsty Sands, Edward A. R. Portal, Kathryn M. Thomson, Maria J. Carvalho, Jordan Mathias, Rebecca Milton, Calie Dyer, Chinenye Akpulu, Ian Boostrom, Patrick Hogan, Habiba Saif, Ana D. Sanches Ferreira, Thomas Hender, Barbra Portal, Robert Andrews, W. John Watkins, Rabaab Zahra, Haider Shirazi, Adil Muhammad, Syed Najeeb Ullah, Muhammad Hilal Jan, Shermeen Akif, Kenneth C. Iregbu, Fatima Modibbo, Stella Uwaezuoke, Lamidi Audu, Chinago P. Edwin, Ashiru H. Yusuf, Adeola Adeleye, Aisha S. Mukkadas, Jean Baptiste Mazarati, Aniceth Rucogoza, Lucie Gaju, Shaheen Mehtar, Andrew N. H. Bulabula, Andrew Whitelaw, Lauren Roberts, Grace Chan, Delayehu Bekele, Semaria Solomon, Mahlet Abayneh, Gesit Metaferia, Group BARNARDS, and Timothy R. Walsh

Subjects
Science
Abstract

Abstract Hospital surfaces can harbour bacterial pathogens, which may disseminate and cause nosocomial infections, contributing towards mortality in low- and middle-income countries (LMICs). During the BARNARDS study, hospital surfaces from neonatal wards were sampled to assess the degree of environmental surface and patient care equipment colonisation by Gram-negative bacteria (GNB) carrying antibiotic resistance genes (ARGs). Here, we perform PCR screening for extended-spectrum β-lactamases (bla CTX-M-15) and carbapenemases (bla NDM, bla OXA-48-like and bla KPC), MALDI-TOF MS identification of GNB carrying ARGs, and further analysis by whole genome sequencing of bacterial isolates. We determine presence of consistently dominant clones and their relatedness to strains causing neonatal sepsis. Higher prevalence of carbapenemases is observed in Pakistan, Bangladesh, and Ethiopia, compared to other countries, and are mostly found in surfaces near the sink drain. Klebsiella pneumoniae, Enterobacter hormaechei, Acinetobacter baumannii, Serratia marcescens and Leclercia adecarboxylata are dominant; ST15 K. pneumoniae is identified from the same ward on multiple occasions suggesting clonal persistence within the same environment, and is found to be identical to isolates causing neonatal sepsis in Pakistan over similar time periods. Our data suggests persistence of dominant clones across multiple time points, highlighting the need for assessment of Infection Prevention and Control guidelines.

Published
2024
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2. Characterisation of Staphylococci species from neonatal blood cultures in low- and middle-income countries

Author

Kirsty Sands, Maria J. Carvalho, Owen B. Spiller, Edward A. R. Portal, Kathryn Thomson, William John Watkins, Jordan Mathias, Calie Dyer, Chinenye Akpulu, Robert Andrews, Ana Ferreira, Thomas Hender, Rebecca Milton, Maria Nieto, Rabaab Zahra, Haider Shirazi, Adil Muhammad, Shermeen Akif, Muhammad Hilal Jan, Kenneth Iregbu, Fatima Modibbo, Stella Uwaezuoke, Grace J. Chan, Delayehu Bekele, Semaria Solomon, Sulagna Basu, Ranjan Kumar Nandy, Sharmi Naha, Jean-Baptiste Mazarati, Aniceth Rucogoza, Lucie Gaju, Shaheen Mehtar, Andre N. H. Bulabula, Andrew Whitelaw, BARNARDS Group, and Timothy R. Walsh

Subjects
LMIC, Staphylococci, Neonatal sepsis, Genomics, Mammaliicocci, Mortality, Infectious and parasitic diseases, RC109-216
Abstract

Abstract Background In low- and middle-income countries (LMIC) Staphylococcus aureus is regarded as one of the leading bacterial causes of neonatal sepsis, however there is limited knowledge on the species diversity and antimicrobial resistance caused by Gram-positive bacteria (GPB). Methods We characterised GPB isolates from neonatal blood cultures from LMICs in Africa (Ethiopia, Nigeria, Rwanda, and South Africa) and South-Asia (Bangladesh and Pakistan) between 2015–2017. We determined minimum inhibitory concentrations and performed whole genome sequencing (WGS) on Staphylococci isolates recovered and clinical data collected related to the onset of sepsis and the outcome of the neonate up to 60 days of age. Results From the isolates recovered from blood cultures, Staphylococci species were most frequently identified. Out of 100 S. aureus isolates sequenced, 18 different sequence types (ST) were found which unveiled two small epidemiological clusters caused by methicillin resistant S. aureus (MRSA) in Pakistan (ST8) and South Africa (ST5), both with high mortality (n = 6/17). One-third of S. aureus was MRSA, with methicillin resistance also detected in Staphylococcus epidermidis, Staphylococcus haemolyticus and Mammaliicoccus sciuri. Through additional WGS analysis we report a cluster of M. sciuri in Pakistan identified between July-November 2017. Conclusions In total we identified 14 different GPB bacterial species, however Staphylococci was dominant. These findings highlight the need of a prospective genomic epidemiology study to comprehensively assess the true burden of GPB neonatal sepsis focusing specifically on mechanisms of resistance and virulence across species and in relation to neonatal outcome.

Published
2022
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3. Neonatal sepsis and mortality in low-income and middle-income countries from a facility-based birth cohort: an international multisite prospective observational study

Author

Rebecca Milton, David Gillespie, Calie Dyer, Khadijeh Taiyari, Maria J Carvalho, Kathryn Thomson, Kirsty Sands, Edward A R Portal, Kerenza Hood, Ana Ferreira, Thomas Hender, Nigel Kirby, Jordan Mathias, Maria Nieto, William J Watkins, Delayehu Bekele, Mahlet Abayneh, Semaria Solomon, Sulagna Basu, Ranjan K Nandy, Bijan Saha, Kenneth Iregbu, Fatima Z Modibbo, Stella Uwaezuoke, Rabaab Zahra, Haider Shirazi, Syed U Najeeb, Jean-Baptiste Mazarati, Aniceth Rucogoza, Lucie Gaju, Shaheen Mehtar, Andre N H Bulabula, Andrew C Whitelaw, Timothy R Walsh, Grace J Chan, Oludare Odumade, Rozina Ambachew, Zenebe Gebre Yohannes, Gesit Metaferia, Redeat Workneh, Tefera Biteye, Yahya Zekaria Mohammed, Alula M Teklu, Balkachew Nigatu, Wendimagegn Gezahegn, Partha Sarathi Chakravorty, Sharmi Naha, Anuradha Mukherjee, Khairiyya Muhammad Umar, Asunugwo Vivian Akunna, Queen Nsude, Ifeoma Uke, Mary-Joe Okenu, Chinenye Akpulu, Chukwuemeka Mmadueke, Samuel Yakubu, Lamidi Audu, Nura Idris, Safiya Gambo, Jamila Ibrahim, Edwin Chinago, Ashiru Yusuf, Shamsudden Gwadabe, Adeola Adeleye, Muhammad Aliyu, Amina Muhammad, Aishatu Kassim, Aisha Sani Mukaddas, Rashida Yakubu Khalid, Fatima Ibrahim Alkali, Maryam Yahaya Muhammad, Fatima Muhammad Tukur, Surayya Mustapha Muhammad, Adeola Shittu, Murjanatu Bello, Fatima Habib Sa ad, Shaheed Zulfiqar, Adil Muhammad, Muhammad Hilal Jan, and Lauren Paterson

Subjects
Pregnancy, Sepsis, Infant Mortality, Infant, Newborn, Humans, Premature Birth, Female, General Medicine, Prospective Studies, Neonatal Sepsis, Developing Countries
Abstract

Background\udNeonatal sepsis is a primary cause of neonatal mortality and is an urgent global health concern, especially within low-income and middle-income countries (LMICs), where 99% of global neonatal mortality occurs. The aims of this study were to determine the incidence and associations with neonatal sepsis and all-cause mortality in facility-born neonates in LMICs.\udMethods\udThe Burden of Antibiotic Resistance in Neonates from Developing Societies (BARNARDS) study recruited mothers and their neonates into a prospective observational cohort study across 12 clinical sites from Bangladesh, Ethiopia, India, Pakistan, Nigeria, Rwanda, and South Africa. Data for sepsis-associated factors in the four domains of health care, maternal, birth and neonatal, and living environment were collected for all mothers and neonates enrolled. Primary outcomes were clinically suspected sepsis, laboratory-confirmed sepsis, and all-cause mortality in neonates during the first 60 days of life. Incidence proportion of livebirths for clinically suspected sepsis and laboratory-confirmed sepsis and incidence rate per 1000 neonate-days for all-cause mortality were calculated. Modified Poisson regression was used to investigate factors associated with neonatal sepsis and parametric survival models for factors associated with all-cause mortality.\udFindings\udBetween Nov 12, 2015 and Feb 1, 2018, 29 483 mothers and 30 557 neonates were enrolled. The incidence of clinically suspected sepsis was 166·0 (95% CI 97·69–234·24) per 1000 livebirths, laboratory-confirmed sepsis was 46·9 (19·04–74·79) per 1000 livebirths, and all-cause mortality was 0·83 (0·37–2·00) per 1000 neonate-days. Maternal hypertension, previous maternal hospitalisation within 12 months, average or higher monthly household income, ward size (>11 beds), ward type (neonatal), living in a rural environment, preterm birth, perinatal asphyxia, and multiple births were associated with an increased risk of clinically suspected sepsis, laboratory-confirmed sepsis, and all-cause mortality. The majority (881 [72·5%] of 1215) of laboratory-confirmed sepsis cases occurred within the first 3 days of life.\udInterpretation\udFindings from this study highlight the substantial proportion of neonates who develop neonatal sepsis, and the high mortality rates among neonates with sepsis in LMICs. More efficient and effective identification of neonatal sepsis is needed to target interventions to reduce its incidence and subsequent mortality in LMICs.\udFunding\udBill & Melinda Gates Foundation.

Published
2022

4. Characterization of antimicrobial resistant Gram-negative bacteria that cause neonatal sepsis in seven low and middle-income countries

Author

Rabaab Zahra, Khadijeh Taiyari, Ana Ferreira, Stella N. Uwaezuoke, Maria Nieto, Kathryn Thomson, Fatima Modibbo, David Gillespie, Maria J. Carvalho, Thomas Hender, Shaheen Mehtar, Rebecca Milton, Delayehu Bekele, Suchandra Mukherjee, Calie Dyer, Haider Shirazi, Grace J Chan, Kirsty Sands, Jean-Baptiste Mazarati, Kenneth Iregbu, Adil Muhammad, Robert Andrews, Timothy R. Walsh, Chinenye Akpulu, Jordan Mathias, André N.H. Bulabula, Sulagna Basu, Aniceth Rucogoza, P. Chattopadhyay, Edward Portal, Semaria Solomon, Lucie Gaju, Kerenza Hood, and Andrew Whitelaw

Subjects
Microbiology (medical), Asia, medicine.drug_class, Klebsiella pneumoniae, Immunology, Cephalosporin, Antibiotics, Antimicrobial resistance, Applied Microbiology and Biotechnology, Microbiology, Article, beta-Lactamases, Sepsis, 03 medical and health sciences, Antibiotic resistance, Bacterial Proteins, Drug Resistance, Multiple, Bacterial, Gram-Negative Bacteria, Genetics, Medicine, Humans, Developing Countries, Phylogeny, 030304 developmental biology, 0303 health sciences, biology, Neonatal sepsis, 030306 microbiology, business.industry, Infant, Newborn, Genetic Variation, Bacteriology, Cell Biology, Genomics, medicine.disease, Antimicrobial, biology.organism_classification, Anti-Bacterial Agents, Serratia marcescens, Africa, Neonatal Sepsis, business, Gram-Negative Bacterial Infections, Genome, Bacterial, Plasmids
Abstract

Antimicrobial resistance in neonatal sepsis is rising, yet mechanisms of resistance that often spread between species via mobile genetic elements, ultimately limiting treatments in low- and middle-income countries (LMICs), are poorly characterized. The Burden of Antibiotic Resistance in Neonates from Developing Societies (BARNARDS) network was initiated to characterize the cause and burden of antimicrobial resistance in neonatal sepsis for seven LMICs in Africa and South Asia. A total of 36,285 neonates were enrolled in the BARNARDS study between November 2015 and December 2017, of whom 2,483 were diagnosed with culture-confirmed sepsis. Klebsiella pneumoniae (n = 258) was the main cause of neonatal sepsis, with Serratia marcescens (n = 151), Klebsiella michiganensis (n = 117), Escherichia coli (n = 75) and Enterobacter cloacae complex (n = 57) also detected. We present whole-genome sequencing, antimicrobial susceptibility and clinical data for 916 out of 1,038 neonatal sepsis isolates (97 isolates were not recovered from initial isolation at local sites). Enterobacterales (K. pneumoniae, E. coli and E. cloacae) harboured multiple cephalosporin and carbapenem resistance genes. All isolated pathogens were resistant to multiple antibiotic classes, including those used to treat neonatal sepsis. Intraspecies diversity of K. pneumoniae and E. coli indicated that multiple antibiotic-resistant lineages cause neonatal sepsis. Our results will underpin research towards better treatments for neonatal sepsis in LMICs., Genomic and clinical analysis of 916 bacterial isolates from neonates with sepsis in seven low- and middle-income countries (the BARNARDS study) reveals that the main species present were antimicrobial-resistant Klebsiella, Escherichia coli and Enterobacter.

Published
2021

5. Effects of antibiotic resistance, drug target attainment, bacterial pathogenicity and virulence, and antibiotic access and affordability on outcomes in neonatal sepsis: an international microbiology and drug evaluation prospective substudy (BARNARDS)

Author

Kathryn M Thomson, Calie Dyer, Feiyan Liu, Kirsty Sands, Edward Portal, Maria J Carvalho, Matthew Barrell, Ian Boostrom, Susanna Dunachie, Refath Farzana, Ana Ferreira, Francis Frayne, Brekhna Hassan, Ellis Jones, Lim Jones, Jordan Mathias, Rebecca Milton, Jessica Rees, Grace J Chan, Delayehu Bekele, Abayneh Mahlet, Sulagna Basu, Ranjan K Nandy, Bijan Saha, Kenneth Iregbu, Fatima Modibbo, Stella Uwaezuoke, Rabaab Zahra, Haider Shirazi, Najeeb U Syed, Jean-Baptiste Mazarati, Aniceth Rucogoza, Lucie Gaju, Shaheen Mehtar, Andre N H Bulabula, Andrew Whitelaw, Johan G C van Hasselt, Timothy R Walsh, Samir Saha, Maksuda Islam, Zabed Bin-Ahmed, Wazir Ahmed, Taslima Begum, Mitu Chowdhury, Shaila Sharmin, Chumki Rani Dey, null Uttam, Abdul Matin, Sowmitra Ranjan Chakraborty, Sadia Tasmin, Dipa Rema, Rashida Khatun, Liza Nath, Nigatu Balkachew, Katherine Schaughency, Semaria Solomon, Zenebe Gebreyohanes, Rozina Ambachew, Oludare Odumade, Misgana Haileselassie, Grace Chan, Abigail Russo, Redeat Workneh, Gesit Metaferia, Mahlet Abayneh, Yahya Zekaria Mohammed, Tefera Biteye, Alula Teklu, Wendimagegn Gezahegn, Partha Sarathi Chakravorty, Anuradha Mukherjee, Ranjan Kumar Nandy, Samarpan Roy, Anuradha Sinha, Sharmi Naha, Sukla Saha Malakar, Siddhartha Bose, Monaki Majhi, Subhasree Sahoo, Putul Mukherjee, Sumitra Kumari Routa, Chaitali Nandi, Pinaki Chattopadhyay, Fatima Zara Isa Modibbo, Dilichukwu Meduekwe, Khairiyya Muhammad, Queen Nsude, Ifeoma Ukeh, Mary-Joe Okenu, Akpulu Chinenye, Samuel Yakubu, Vivian Asunugwo, Folake Aina, Isibong Issy, Dolapo Adekeye, Adiele Eunice, Abdulmlik Amina, R Oyewole, I Oloton, BC Nnaji, M Umejiego, PN Anoke, S Adebayo, GO Abegunrin, OB Omotosho, R Ibrahim, B Igwe, M Abroko, K Balami, L Bayem, C Anyanwu, H Haruna, J Okike, K Goroh, M Boi-Sunday, Augusta Ugafor, Maryam Makama, Kaniba Ndukwe, Anastesia Odama, Hadiza Yusuf, Patience Wachukwu, Kachalla Yahaya, Titus Kalade Colsons, Mercy Kura, Damilola Orebiyi, Kenneth C. Iregbu, Chukwuemeka Mmadueke, Lamidi Audu, Nura Idris, Safiya Gambo, Jamila Ibrahim, Edwin Precious, Ashiru Hassan, Shamsudden Gwadabe, Adeola Adeleye Falola, Muhammad Aliyu, Amina Ibrahim, Aisha Sani Mukaddas, Rashida Yakubu Khalid, Fatima Ibrahim Alkali, Maryam Yahaya Muhammad, Fatima Mohammad Tukur, Surayya Mustapha Muhammad, Adeola Shittu, Murjanatu Bello, Muhammad Abubakar Hassan, Fatima Habib Sa ad, Aishatu Kassim, Adil Muhammad, Syed Najeeb Ullah, Muhammad Hilal Jan, Rubina Kamran, null Sajana, Jazba Saeed, Noreen Maqsood, Maria Zafar, Saraeen Sadiq, Sumble Ahsan, Madiha Tariq, Sidra Sajid, Hasma Mustafa, Anees-ur Rehman, Atif Muhammad, Gahssan Mehmood, Mahnoor Nisar, Shermeen Akif, Tahira Yasmeen, Sabir Nawaz, Anam Shanal Atta, Mian Laiq-ur-Rehman, Robina Kousar, Kalsoom Bibi, Kosar Waheed, Zainab Majeed, Ayesha Jalil, Espoir Kajibwami, Innocent Nzabahimana, Mazarati Jean-Baptiste, Kankundiye Riziki, Brigette Uwamahoro, Rachel Uwera, Eugenie Nyiratuza, Kumwami Muzungu, Violette Uwitonze, Marie C Horanimpundu, Francine Nzeyimana, Prince Mitima, Angela Dramowski, Lauren Paterson, Mary Frans, Marvina Johnson, Eveline Swanepoel, Zoleka Bojana, Mieme du Preez, Andre Bulabula, Johan GC van Hasselt, Timothy Walsh, Maria Carvalho, Kathryn Thomson, Robert Andrews, John Watkins, David Gillespie, Kerry Hood, Katie Taiyai, Nigel Kirby, Maria Nieto, Thomas Hender, Patrick Hogan, Habiba Saif, Brad Spiller, Julian Parkhill, Apollo - University of Cambridge Repository, and Group, BARNARDS

Subjects
medicine.medical_specialty, Staphylococcus aureus, medicine.drug_class, Antibiotics, Sepsis, Cohort Studies, Antibiotic resistance, Enterobacteriaceae, Internal medicine, medicine, Humans, Developing Countries, Poverty, Neonatal sepsis, Virulence, business.industry, Enterobacteriaceae Infections, Infant, Newborn, Drug Resistance, Microbial, Articles, Amoxicillin, Staphylococcal Infections, medicine.disease, Anti-Bacterial Agents, Infectious Diseases, Amikacin, Colistin, Gentamicin, Drug Therapy, Combination, Neonatal Sepsis, business, medicine.drug
Abstract

Background Sepsis is a major contributor to neonatal mortality, particularly in low-income and middle-income countries (LMICs). WHO advocates ampicillin–gentamicin as first-line therapy for the management of neonatal sepsis. In the BARNARDS observational cohort study of neonatal sepsis and antimicrobial resistance in LMICs, common sepsis pathogens were characterised via whole genome sequencing (WGS) and antimicrobial resistance profiles. In this substudy of BARNARDS, we aimed to assess the use and efficacy of empirical antibiotic therapies commonly used in LMICs for neonatal sepsis. Methods In BARNARDS, consenting mother–neonates aged 0–60 days dyads were enrolled on delivery or neonatal presentation with suspected sepsis at 12 BARNARDS clinical sites in Bangladesh, Ethiopia, India, Pakistan, Nigeria, Rwanda, and South Africa. Stillborn babies were excluded from the study. Blood samples were collected from neonates presenting with clinical signs of sepsis, and WGS and minimum inhibitory concentrations for antibiotic treatment were determined for bacterial isolates from culture-confirmed sepsis. Neonatal outcome data were collected following enrolment until 60 days of life. Antibiotic usage and neonatal outcome data were assessed. Survival analyses were adjusted to take into account potential clinical confounding variables related to the birth and pathogen. Additionally, resistance profiles, pharmacokinetic–pharmacodynamic probability of target attainment, and frequency of resistance (ie, resistance defined by in-vitro growth of isolates when challenged by antibiotics) were assessed. Questionnaires on health structures and antibiotic costs evaluated accessibility and affordability. Findings Between Nov 12, 2015, and Feb 1, 2018, 36 285 neonates were enrolled into the main BARNARDS study, of whom 9874 had clinically diagnosed sepsis and 5749 had available antibiotic data. The four most commonly prescribed antibiotic combinations given to 4451 neonates (77·42%) of 5749 were ampicillin–gentamicin, ceftazidime–amikacin, piperacillin–tazobactam–amikacin, and amoxicillin clavulanate–amikacin. This dataset assessed 476 prescriptions for 442 neonates treated with one of these antibiotic combinations with WGS data (all BARNARDS countries were represented in this subset except India). Multiple pathogens were isolated, totalling 457 isolates. Reported mortality was lower for neonates treated with ceftazidime–amikacin than for neonates treated with ampicillin–gentamicin (hazard ratio [adjusted for clinical variables considered potential confounders to outcomes] 0·32, 95% CI 0·14–0·72; p=0·0060). Of 390 Gram-negative isolates, 379 (97·2%) were resistant to ampicillin and 274 (70·3%) were resistant to gentamicin. Susceptibility of Gram-negative isolates to at least one antibiotic in a treatment combination was noted in 111 (28·5%) to ampicillin–gentamicin; 286 (73·3%) to amoxicillin clavulanate–amikacin; 301 (77·2%) to ceftazidime–amikacin; and 312 (80·0%) to piperacillin–tazobactam–amikacin. A probability of target attainment of 80% or more was noted in 26 neonates (33·7% [SD 0·59]) of 78 with ampicillin–gentamicin; 15 (68·0% [3·84]) of 27 with amoxicillin clavulanate–amikacin; 93 (92·7% [0·24]) of 109 with ceftazidime–amikacin; and 70 (85·3% [0·47]) of 76 with piperacillin–tazobactam–amikacin. However, antibiotic and country effects could not be distinguished. Frequency of resistance was recorded most frequently with fosfomycin (in 78 isolates [68·4%] of 114), followed by colistin (55 isolates [57·3%] of 96), and gentamicin (62 isolates [53·0%] of 117). Sites in six of the seven countries (excluding South Africa) stated that the cost of antibiotics would influence treatment of neonatal sepsis. Interpretation Our data raise questions about the empirical use of combined ampicillin–gentamicin for neonatal sepsis in LMICs because of its high resistance and high rates of frequency of resistance and low probability of target attainment. Accessibility and affordability need to be considered when advocating antibiotic treatments with variance in economic health structures across LMICs. Funding The Bill & Melinda Gates Foundation.

Published
2020

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