Patterns of antibiotic use, pathogens, and prediction of mortality in hospitalized neonates and young infants with sepsis: A global neonatal sepsis observational cohort study (NeoOBS).
<h4>Background</h4>There is limited data on antibiotic treatment in hospitalized neonates in low- and middle-income countries (LMICs). We aimed to describe patterns of antibiotic use, pathogens, and clinical outcomes, and to develop a severity score predicting mortality in neonatal sepsi...
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2023-06-01
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| author | Neal J Russell Wolfgang Stöhr Nishad Plakkal Aislinn Cook James A Berkley Bethou Adhisivam Ramesh Agarwal Nawshad Uddin Ahmed Manica Balasegaram Daynia Ballot Adrie Bekker Eitan Naaman Berezin Davide Bilardi Suppawat Boonkasidecha Cristina G Carvalheiro Neema Chami Suman Chaurasia Sara Chiurchiu Viviane Rinaldi Favarin Colas Simon Cousens Tim R Cressey Ana Carolina Dantas de Assis Tran Minh Dien Yijun Ding Nguyen Trong Dung Han Dong Angela Dramowski Madhusudhan Ds Ajay Dudeja Jinxing Feng Youri Glupczynski Srishti Goel Herman Goossens Doan Thi Huong Hao Mahmudul Islam Khan Tatiana Munera Huertas Mohammad Shahidul Islam Daniel Jarovsky Nathalie Khavessian Meera Khorana Angeliki Kontou Tomislav Kostyanev Premsak Laoyookhon Sorasak Lochindarat Mattias Larsson Maia De Luca Surbhi Malhotra-Kumar Nivedita Mondal Nitu Mundhra Philippa Musoke Marisa M Mussi-Pinhata Ruchi Nanavati Firdose Nakwa Sushma Nangia Jolly Nankunda Alessandra Nardone Borna Nyaoke Christina W Obiero Maxensia Owor Wang Ping Kanchana Preedisripipat Shamim Qazi Lifeng Qi Tanusha Ramdin Amy Riddell Lorenza Romani Praewpan Roysuwan Robin Saggers Emmanuel Roilides Samir K Saha Kosmas Sarafidis Valerie Tusubira Reenu Thomas Sithembiso Velaphi Tuba Vilken Xiaojiao Wang Yajuan Wang Yonghong Yang Liu Zunjie Sally Ellis Julia A Bielicki A Sarah Walker Paul T Heath Mike Sharland |
| author_facet | Neal J Russell Wolfgang Stöhr Nishad Plakkal Aislinn Cook James A Berkley Bethou Adhisivam Ramesh Agarwal Nawshad Uddin Ahmed Manica Balasegaram Daynia Ballot Adrie Bekker Eitan Naaman Berezin Davide Bilardi Suppawat Boonkasidecha Cristina G Carvalheiro Neema Chami Suman Chaurasia Sara Chiurchiu Viviane Rinaldi Favarin Colas Simon Cousens Tim R Cressey Ana Carolina Dantas de Assis Tran Minh Dien Yijun Ding Nguyen Trong Dung Han Dong Angela Dramowski Madhusudhan Ds Ajay Dudeja Jinxing Feng Youri Glupczynski Srishti Goel Herman Goossens Doan Thi Huong Hao Mahmudul Islam Khan Tatiana Munera Huertas Mohammad Shahidul Islam Daniel Jarovsky Nathalie Khavessian Meera Khorana Angeliki Kontou Tomislav Kostyanev Premsak Laoyookhon Sorasak Lochindarat Mattias Larsson Maia De Luca Surbhi Malhotra-Kumar Nivedita Mondal Nitu Mundhra Philippa Musoke Marisa M Mussi-Pinhata Ruchi Nanavati Firdose Nakwa Sushma Nangia Jolly Nankunda Alessandra Nardone Borna Nyaoke Christina W Obiero Maxensia Owor Wang Ping Kanchana Preedisripipat Shamim Qazi Lifeng Qi Tanusha Ramdin Amy Riddell Lorenza Romani Praewpan Roysuwan Robin Saggers Emmanuel Roilides Samir K Saha Kosmas Sarafidis Valerie Tusubira Reenu Thomas Sithembiso Velaphi Tuba Vilken Xiaojiao Wang Yajuan Wang Yonghong Yang Liu Zunjie Sally Ellis Julia A Bielicki A Sarah Walker Paul T Heath Mike Sharland |
| author_sort | Neal J Russell |
| collection | DOAJ |
| description | <h4>Background</h4>There is limited data on antibiotic treatment in hospitalized neonates in low- and middle-income countries (LMICs). We aimed to describe patterns of antibiotic use, pathogens, and clinical outcomes, and to develop a severity score predicting mortality in neonatal sepsis to inform future clinical trial design.<h4>Methods and findings</h4>Hospitalized infants <60 days with clinical sepsis were enrolled during 2018 to 2020 by 19 sites in 11 countries (mainly Asia and Africa). Prospective daily observational data was collected on clinical signs, supportive care, antibiotic treatment, microbiology, and 28-day mortality. Two prediction models were developed for (1) 28-day mortality from baseline variables (baseline NeoSep Severity Score); and (2) daily risk of death on IV antibiotics from daily updated assessments (NeoSep Recovery Score). Multivariable Cox regression models included a randomly selected 85% of infants, with 15% for validation. A total of 3,204 infants were enrolled, with median birth weight of 2,500 g (IQR 1,400 to 3,000) and postnatal age of 5 days (IQR 1 to 15). 206 different empiric antibiotic combinations were started in 3,141 infants, which were structured into 5 groups based on the World Health Organization (WHO) AWaRe classification. Approximately 25.9% (n = 814) of infants started WHO first line regimens (Group 1-Access) and 13.8% (n = 432) started WHO second-line cephalosporins (cefotaxime/ceftriaxone) (Group 2-"Low" Watch). The largest group (34.0%, n = 1,068) started a regimen providing partial extended-spectrum beta-lactamase (ESBL)/pseudomonal coverage (piperacillin-tazobactam, ceftazidime, or fluoroquinolone-based) (Group 3-"Medium" Watch), 18.0% (n = 566) started a carbapenem (Group 4-"High" Watch), and 1.8% (n = 57) a Reserve antibiotic (Group 5, largely colistin-based), and 728/2,880 (25.3%) of initial regimens in Groups 1 to 4 were escalated, mainly to carbapenems, usually for clinical deterioration (n = 480; 65.9%). A total of 564/3,195 infants (17.7%) were blood culture pathogen positive, of whom 62.9% (n = 355) had a gram-negative organism, predominantly Klebsiella pneumoniae (n = 132) or Acinetobacter spp. (n = 72). Both were commonly resistant to WHO-recommended regimens and to carbapenems in 43 (32.6%) and 50 (71.4%) of cases, respectively. MRSA accounted for 33 (61.1%) of 54 Staphylococcus aureus isolates. Overall, 350/3,204 infants died (11.3%; 95% CI 10.2% to 12.5%), 17.7% if blood cultures were positive for pathogens (95% CI 14.7% to 21.1%, n = 99/564). A baseline NeoSep Severity Score had a C-index of 0.76 (0.69 to 0.82) in the validation sample, with mortality of 1.6% (3/189; 95% CI: 0.5% to 4.6%), 11.0% (27/245; 7.7% to 15.6%), and 27.3% (12/44; 16.3% to 41.8%) in low (score 0 to 4), medium (5 to 8), and high (9 to 16) risk groups, respectively, with similar performance across subgroups. A related NeoSep Recovery Score had an area under the receiver operating curve for predicting death the next day between 0.8 and 0.9 over the first week. There was significant variation in outcomes between sites and external validation would strengthen score applicability.<h4>Conclusion</h4>Antibiotic regimens used in neonatal sepsis commonly diverge from WHO guidelines, and trials of novel empiric regimens are urgently needed in the context of increasing antimicrobial resistance (AMR). The baseline NeoSep Severity Score identifies high mortality risk criteria for trial entry, while the NeoSep Recovery Score can help guide decisions on regimen change. NeoOBS data informed the NeoSep1 antibiotic trial (ISRCTN48721236), which aims to identify novel first- and second-line empiric antibiotic regimens for neonatal sepsis.<h4>Trial registration</h4>ClinicalTrials.gov, (NCT03721302). |
| format | Article |
| id | doaj-art-72ca0b6efbd84ba3bf3e40c592391f16 |
| institution | OA Journals |
| issn | 1549-1277 1549-1676 |
| language | English |
| publishDate | 2023-06-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Medicine |
| spelling | doaj-art-72ca0b6efbd84ba3bf3e40c592391f162025-08-20T02:22:06ZengPublic Library of Science (PLoS)PLoS Medicine1549-12771549-16762023-06-01206e100417910.1371/journal.pmed.1004179Patterns of antibiotic use, pathogens, and prediction of mortality in hospitalized neonates and young infants with sepsis: A global neonatal sepsis observational cohort study (NeoOBS).Neal J RussellWolfgang StöhrNishad PlakkalAislinn CookJames A BerkleyBethou AdhisivamRamesh AgarwalNawshad Uddin AhmedManica BalasegaramDaynia BallotAdrie BekkerEitan Naaman BerezinDavide BilardiSuppawat BoonkasidechaCristina G CarvalheiroNeema ChamiSuman ChaurasiaSara ChiurchiuViviane Rinaldi Favarin ColasSimon CousensTim R CresseyAna Carolina Dantas de AssisTran Minh DienYijun DingNguyen Trong DungHan DongAngela DramowskiMadhusudhan DsAjay DudejaJinxing FengYouri GlupczynskiSrishti GoelHerman GoossensDoan Thi Huong HaoMahmudul Islam KhanTatiana Munera HuertasMohammad Shahidul IslamDaniel JarovskyNathalie KhavessianMeera KhoranaAngeliki KontouTomislav KostyanevPremsak LaoyookhonSorasak LochindaratMattias LarssonMaia De LucaSurbhi Malhotra-KumarNivedita MondalNitu MundhraPhilippa MusokeMarisa M Mussi-PinhataRuchi NanavatiFirdose NakwaSushma NangiaJolly NankundaAlessandra NardoneBorna NyaokeChristina W ObieroMaxensia OworWang PingKanchana PreedisripipatShamim QaziLifeng QiTanusha RamdinAmy RiddellLorenza RomaniPraewpan RoysuwanRobin SaggersEmmanuel RoilidesSamir K SahaKosmas SarafidisValerie TusubiraReenu ThomasSithembiso VelaphiTuba VilkenXiaojiao WangYajuan WangYonghong YangLiu ZunjieSally EllisJulia A BielickiA Sarah WalkerPaul T HeathMike Sharland<h4>Background</h4>There is limited data on antibiotic treatment in hospitalized neonates in low- and middle-income countries (LMICs). We aimed to describe patterns of antibiotic use, pathogens, and clinical outcomes, and to develop a severity score predicting mortality in neonatal sepsis to inform future clinical trial design.<h4>Methods and findings</h4>Hospitalized infants <60 days with clinical sepsis were enrolled during 2018 to 2020 by 19 sites in 11 countries (mainly Asia and Africa). Prospective daily observational data was collected on clinical signs, supportive care, antibiotic treatment, microbiology, and 28-day mortality. Two prediction models were developed for (1) 28-day mortality from baseline variables (baseline NeoSep Severity Score); and (2) daily risk of death on IV antibiotics from daily updated assessments (NeoSep Recovery Score). Multivariable Cox regression models included a randomly selected 85% of infants, with 15% for validation. A total of 3,204 infants were enrolled, with median birth weight of 2,500 g (IQR 1,400 to 3,000) and postnatal age of 5 days (IQR 1 to 15). 206 different empiric antibiotic combinations were started in 3,141 infants, which were structured into 5 groups based on the World Health Organization (WHO) AWaRe classification. Approximately 25.9% (n = 814) of infants started WHO first line regimens (Group 1-Access) and 13.8% (n = 432) started WHO second-line cephalosporins (cefotaxime/ceftriaxone) (Group 2-"Low" Watch). The largest group (34.0%, n = 1,068) started a regimen providing partial extended-spectrum beta-lactamase (ESBL)/pseudomonal coverage (piperacillin-tazobactam, ceftazidime, or fluoroquinolone-based) (Group 3-"Medium" Watch), 18.0% (n = 566) started a carbapenem (Group 4-"High" Watch), and 1.8% (n = 57) a Reserve antibiotic (Group 5, largely colistin-based), and 728/2,880 (25.3%) of initial regimens in Groups 1 to 4 were escalated, mainly to carbapenems, usually for clinical deterioration (n = 480; 65.9%). A total of 564/3,195 infants (17.7%) were blood culture pathogen positive, of whom 62.9% (n = 355) had a gram-negative organism, predominantly Klebsiella pneumoniae (n = 132) or Acinetobacter spp. (n = 72). Both were commonly resistant to WHO-recommended regimens and to carbapenems in 43 (32.6%) and 50 (71.4%) of cases, respectively. MRSA accounted for 33 (61.1%) of 54 Staphylococcus aureus isolates. Overall, 350/3,204 infants died (11.3%; 95% CI 10.2% to 12.5%), 17.7% if blood cultures were positive for pathogens (95% CI 14.7% to 21.1%, n = 99/564). A baseline NeoSep Severity Score had a C-index of 0.76 (0.69 to 0.82) in the validation sample, with mortality of 1.6% (3/189; 95% CI: 0.5% to 4.6%), 11.0% (27/245; 7.7% to 15.6%), and 27.3% (12/44; 16.3% to 41.8%) in low (score 0 to 4), medium (5 to 8), and high (9 to 16) risk groups, respectively, with similar performance across subgroups. A related NeoSep Recovery Score had an area under the receiver operating curve for predicting death the next day between 0.8 and 0.9 over the first week. There was significant variation in outcomes between sites and external validation would strengthen score applicability.<h4>Conclusion</h4>Antibiotic regimens used in neonatal sepsis commonly diverge from WHO guidelines, and trials of novel empiric regimens are urgently needed in the context of increasing antimicrobial resistance (AMR). The baseline NeoSep Severity Score identifies high mortality risk criteria for trial entry, while the NeoSep Recovery Score can help guide decisions on regimen change. NeoOBS data informed the NeoSep1 antibiotic trial (ISRCTN48721236), which aims to identify novel first- and second-line empiric antibiotic regimens for neonatal sepsis.<h4>Trial registration</h4>ClinicalTrials.gov, (NCT03721302).https://journals.plos.org/plosmedicine/article/file?id=10.1371/journal.pmed.1004179&type=printable |
| spellingShingle | Neal J Russell Wolfgang Stöhr Nishad Plakkal Aislinn Cook James A Berkley Bethou Adhisivam Ramesh Agarwal Nawshad Uddin Ahmed Manica Balasegaram Daynia Ballot Adrie Bekker Eitan Naaman Berezin Davide Bilardi Suppawat Boonkasidecha Cristina G Carvalheiro Neema Chami Suman Chaurasia Sara Chiurchiu Viviane Rinaldi Favarin Colas Simon Cousens Tim R Cressey Ana Carolina Dantas de Assis Tran Minh Dien Yijun Ding Nguyen Trong Dung Han Dong Angela Dramowski Madhusudhan Ds Ajay Dudeja Jinxing Feng Youri Glupczynski Srishti Goel Herman Goossens Doan Thi Huong Hao Mahmudul Islam Khan Tatiana Munera Huertas Mohammad Shahidul Islam Daniel Jarovsky Nathalie Khavessian Meera Khorana Angeliki Kontou Tomislav Kostyanev Premsak Laoyookhon Sorasak Lochindarat Mattias Larsson Maia De Luca Surbhi Malhotra-Kumar Nivedita Mondal Nitu Mundhra Philippa Musoke Marisa M Mussi-Pinhata Ruchi Nanavati Firdose Nakwa Sushma Nangia Jolly Nankunda Alessandra Nardone Borna Nyaoke Christina W Obiero Maxensia Owor Wang Ping Kanchana Preedisripipat Shamim Qazi Lifeng Qi Tanusha Ramdin Amy Riddell Lorenza Romani Praewpan Roysuwan Robin Saggers Emmanuel Roilides Samir K Saha Kosmas Sarafidis Valerie Tusubira Reenu Thomas Sithembiso Velaphi Tuba Vilken Xiaojiao Wang Yajuan Wang Yonghong Yang Liu Zunjie Sally Ellis Julia A Bielicki A Sarah Walker Paul T Heath Mike Sharland Patterns of antibiotic use, pathogens, and prediction of mortality in hospitalized neonates and young infants with sepsis: A global neonatal sepsis observational cohort study (NeoOBS). PLoS Medicine |
| title | Patterns of antibiotic use, pathogens, and prediction of mortality in hospitalized neonates and young infants with sepsis: A global neonatal sepsis observational cohort study (NeoOBS). |
| title_full | Patterns of antibiotic use, pathogens, and prediction of mortality in hospitalized neonates and young infants with sepsis: A global neonatal sepsis observational cohort study (NeoOBS). |
| title_fullStr | Patterns of antibiotic use, pathogens, and prediction of mortality in hospitalized neonates and young infants with sepsis: A global neonatal sepsis observational cohort study (NeoOBS). |
| title_full_unstemmed | Patterns of antibiotic use, pathogens, and prediction of mortality in hospitalized neonates and young infants with sepsis: A global neonatal sepsis observational cohort study (NeoOBS). |
| title_short | Patterns of antibiotic use, pathogens, and prediction of mortality in hospitalized neonates and young infants with sepsis: A global neonatal sepsis observational cohort study (NeoOBS). |
| title_sort | patterns of antibiotic use pathogens and prediction of mortality in hospitalized neonates and young infants with sepsis a global neonatal sepsis observational cohort study neoobs |
| url | https://journals.plos.org/plosmedicine/article/file?id=10.1371/journal.pmed.1004179&type=printable |
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patternsofantibioticusepathogensandpredictionofmortalityinhospitalizedneonatesandyounginfantswithsepsisaglobalneonatalsepsisobservationalcohortstudyneoobs AT valerietusubira patternsofantibioticusepathogensandpredictionofmortalityinhospitalizedneonatesandyounginfantswithsepsisaglobalneonatalsepsisobservationalcohortstudyneoobs AT reenuthomas patternsofantibioticusepathogensandpredictionofmortalityinhospitalizedneonatesandyounginfantswithsepsisaglobalneonatalsepsisobservationalcohortstudyneoobs AT sithembisovelaphi patternsofantibioticusepathogensandpredictionofmortalityinhospitalizedneonatesandyounginfantswithsepsisaglobalneonatalsepsisobservationalcohortstudyneoobs AT tubavilken patternsofantibioticusepathogensandpredictionofmortalityinhospitalizedneonatesandyounginfantswithsepsisaglobalneonatalsepsisobservationalcohortstudyneoobs AT xiaojiaowang patternsofantibioticusepathogensandpredictionofmortalityinhospitalizedneonatesandyounginfantswithsepsisaglobalneonatalsepsisobservationalcohortstudyneoobs AT yajuanwang patternsofantibioticusepathogensandpredictionofmortalityinhospitalizedneonatesandyounginfantswithsepsisaglobalneonatalsepsisobservationalcohortstudyneoobs AT yonghongyang patternsofantibioticusepathogensandpredictionofmortalityinhospitalizedneonatesandyounginfantswithsepsisaglobalneonatalsepsisobservationalcohortstudyneoobs AT liuzunjie patternsofantibioticusepathogensandpredictionofmortalityinhospitalizedneonatesandyounginfantswithsepsisaglobalneonatalsepsisobservationalcohortstudyneoobs AT sallyellis patternsofantibioticusepathogensandpredictionofmortalityinhospitalizedneonatesandyounginfantswithsepsisaglobalneonatalsepsisobservationalcohortstudyneoobs AT juliaabielicki patternsofantibioticusepathogensandpredictionofmortalityinhospitalizedneonatesandyounginfantswithsepsisaglobalneonatalsepsisobservationalcohortstudyneoobs AT asarahwalker patternsofantibioticusepathogensandpredictionofmortalityinhospitalizedneonatesandyounginfantswithsepsisaglobalneonatalsepsisobservationalcohortstudyneoobs AT paultheath patternsofantibioticusepathogensandpredictionofmortalityinhospitalizedneonatesandyounginfantswithsepsisaglobalneonatalsepsisobservationalcohortstudyneoobs AT mikesharland patternsofantibioticusepathogensandpredictionofmortalityinhospitalizedneonatesandyounginfantswithsepsisaglobalneonatalsepsisobservationalcohortstudyneoobs |