Whole genome analysis of Pantoea species identified from sepsis patients in selected Ethiopian referral hospitals: emerging pathogens.
Pantoea
/ genetics
Ethiopia
/ epidemiology
Humans
Sepsis
/ microbiology
Whole Genome Sequencing
Phylogeny
Enterobacteriaceae Infections
/ microbiology
Genome, Bacterial
Drug Resistance, Multiple, Bacterial
/ genetics
Female
Anti-Bacterial Agents
/ pharmacology
Middle Aged
Male
Adult
Aged
Plasmids
/ genetics
Microbial Sensitivity Tests
Young Adult
Hospitals
Antimicrobial Resistance genes
Ethiopia
Novel Pantoea species
Plasmids
Sepsis-causing emerging pathogens
Whole genome sequencing
Journal
BMC microbiology
ISSN: 1471-2180
Titre abrégé: BMC Microbiol
Pays: England
ID NLM: 100966981
Informations de publication
Date de publication:
12 Oct 2024
12 Oct 2024
Historique:
received:
06
11
2023
accepted:
30
09
2024
medline:
13
10
2024
pubmed:
13
10
2024
entrez:
12
10
2024
Statut:
epublish
Résumé
The burden of sepsis worsens due to the continuation of emerging pathogens such as multidrug-resistant Pantoea species. A multicenter study was conducted between October 2019 and September 2020 at four hospitals located in central, southern, and northern parts of Ethiopia. A total of 1416 sepsis patients were recruited and blood cultures were performed. At each study site, positive cultures were characterized by their colony characteristics, gram stain, and conventional biochemical tests. All Pantoea species were identified using Matrix-Assisted Laser Desorption/Ionization Time-of-Flight Mass Spectrometry (MALDI TOF) and subjected to whole genome sequencing (WGS) using Illumina HiSeq 2500. The phylogeny structure of Pantoea isolates was calculated using IQ-TREE v1.6.12 from single-nucleotide polymorphisms detected by Snippy v.4.6.0 and filtered by Gubbins v.2.3.4. Average nucleotide identity was estimated by using OrthoANI v.0.93.1 on Shovill v.1.1.0 assemblies. Antimicrobial resistance genes and plasmid replicons were detected using ARIBA v.2.14.6. Phylogenetic trees were visualized using iTOLv.6.5.2. Multiple Pantoea species include: P. dispersa (n = 19), P. septica (n = 1), and a novel Pantoea spp. (n = 1), were identified among sepsis patients. All P. dispersa isolates and the novel Pantoea species were isolated at Dessie Referral Hospital and displayed phylogenetic clonality, including the ubiquity of an IncM1 plasmid and identical antimicrobial resistance (AMR) gene profiles, encoding bla The emerging Pantoea spp. carrying multiple AMR genes were identified from sepsis patients. Implementation of strong infection prevention strategies and building surveillance capacity with advanced bacteriology laboratories capable of identifying multidrug-resistant emerging pathogens is strongly recommended.
Sections du résumé
BACKGROUND
BACKGROUND
The burden of sepsis worsens due to the continuation of emerging pathogens such as multidrug-resistant Pantoea species.
METHODS
METHODS
A multicenter study was conducted between October 2019 and September 2020 at four hospitals located in central, southern, and northern parts of Ethiopia. A total of 1416 sepsis patients were recruited and blood cultures were performed. At each study site, positive cultures were characterized by their colony characteristics, gram stain, and conventional biochemical tests. All Pantoea species were identified using Matrix-Assisted Laser Desorption/Ionization Time-of-Flight Mass Spectrometry (MALDI TOF) and subjected to whole genome sequencing (WGS) using Illumina HiSeq 2500. The phylogeny structure of Pantoea isolates was calculated using IQ-TREE v1.6.12 from single-nucleotide polymorphisms detected by Snippy v.4.6.0 and filtered by Gubbins v.2.3.4. Average nucleotide identity was estimated by using OrthoANI v.0.93.1 on Shovill v.1.1.0 assemblies. Antimicrobial resistance genes and plasmid replicons were detected using ARIBA v.2.14.6. Phylogenetic trees were visualized using iTOLv.6.5.2.
RESULTS
RESULTS
Multiple Pantoea species include: P. dispersa (n = 19), P. septica (n = 1), and a novel Pantoea spp. (n = 1), were identified among sepsis patients. All P. dispersa isolates and the novel Pantoea species were isolated at Dessie Referral Hospital and displayed phylogenetic clonality, including the ubiquity of an IncM1 plasmid and identical antimicrobial resistance (AMR) gene profiles, encoding bla
CONCLUSION
CONCLUSIONS
The emerging Pantoea spp. carrying multiple AMR genes were identified from sepsis patients. Implementation of strong infection prevention strategies and building surveillance capacity with advanced bacteriology laboratories capable of identifying multidrug-resistant emerging pathogens is strongly recommended.
Identifiants
pubmed: 39395976
doi: 10.1186/s12866-024-03561-5
pii: 10.1186/s12866-024-03561-5
doi:
Substances chimiques
Anti-Bacterial Agents
0
Types de publication
Journal Article
Multicenter Study
Langues
eng
Sous-ensembles de citation
IM
Pagination
407Subventions
Organisme : Styrelsen för Internationellt Utvecklingssamarbete
ID : ISP 2017/43:9
Informations de copyright
© 2024. The Author(s).
Références
Amanati A, Sajedianfard S, Khajeh S, Ghasempour S, Mehrangiz S, Nematolahi S, et al. Bloodstream infections in adult patients with malignancy, epidemiology, microbiology, and risk factors associated with mortality and multi-drug resistance. BMC Infect Dis. 2021;21(1):1–14.
doi: 10.1186/s12879-021-06243-z
WHO. Global report on the epidemiology and burden of sepsis: current evidence, identifying gaps and future directions. Geneva: World Health Organization; 2020. Licence: CC BY-NC-SA 3.0 IGO. https://www.who.int/publications/i/item/9789240010789
Yang Y, Hu H, Zhou C, Zhang W, Yu Y, Liu Q, et al. Characteristics and accurate identification of Pantoea dispersa with a case of spontaneous rupture of hepatocellular carcinoma in China: a case report. Medicine. 2022;101(2):e28541.
pubmed: 35029210
pmcid: 8758028
doi: 10.1097/MD.0000000000028541
Mehar V, Yadav D, Sanghvi J, Gupta N, Singh K. Pantoea dispersa: an unusual cause of neonatal sepsis. Brazilian J Infect Dis. 2013;17(6):726–8.
doi: 10.1016/j.bjid.2013.05.013
Brady C, Cleenwerck I, Venter S, Vancanneyt M, Swings J, Coutinho T. Phylogeny and identification of Pantoea species associated with plants, humans and the natural environment based on multilocus sequence analysis (MLSA). Syst Appl Microbiol. 2008;31(6–8):447–60.
pubmed: 19008066
doi: 10.1016/j.syapm.2008.09.004
Lo CI, Padhmanabhan R, Mediannikov O, Nguyen TT, Raoult D, Fournier PE, et al. Genome sequence and description of Pantoea septica strain FF5. Stand Genomic Sci. 2015;10:103.
pubmed: 26568786
pmcid: 4644298
doi: 10.1186/s40793-015-0083-0
Van Rostenberghe H, Noraida R, Wan Pauzi W, Habsah H, Zeehaida M, Rosliza A, et al. The clinical picture of neonatal infection with Pantoea species. Jpn J Infect Dis. 2006;59(2):120.
pubmed: 16632913
doi: 10.7883/yoken.JJID.2006.120
Zuberbuhler B, Carifi G, Leatherbarrow B. Acute Dacryocystitis in a 2-Year Old Child caused by Pantoea. Orbit. 2012;31(1):13–4.
pubmed: 22296230
doi: 10.3109/01676830.2011.628435
Im JH, Yeo JY, Park SW, Yang DH, Kim MS, Kim JJ, et al. A case of Pantoea species Cholangitis with Bacteremia. Soonchunhyang Med Sci. 2012;18(2):148–50.
doi: 10.15746/sms.12.032
Okwundu N, Mercer J. Pantoea agglomerans cutaneous infection. J Dermatology Dermatol Surg. 2019;23(1):41–3.
doi: 10.4103/jdds.jdds_43_18
Aibinu I, Pfeifer Y, Peters F, Ogunsola F, Adenipekun E, Odugbemi T, et al. Emergence of bla CTX-M-15, qnrB1 and aac(6′)-Ib-cr resistance genes in Pantoea agglomerans and Enterobacter cloacae from Nigeria (sub-saharan Africa). J Med Microbiol. 2012;61(1):165–7.
pubmed: 21921107
doi: 10.1099/jmm.0.035238-0
Shrestha B, K C N, Bastola C, Jahir T, Risal R, Thapa S, et al. Pantoea agglomerans: an elusive contributor to Chronic Obstructive Pulmonary Disease Exacerbation. Cureus. 2021;13(10):e18562.
pubmed: 34760410
pmcid: 8571802
Pandya S, Aslam S, Shenoy R, Denham JD, Nanjappa S, Greene JN. Pantoea infections in Cancer patients: a Retrospective Chart Review and Review of Literature. Infect Dis Clin Pract. 2018;26(5):275–8.
doi: 10.1097/IPC.0000000000000635
Gan HM, Parthasarathy A, Henry KR, Savka MA, Thomas BN, Hudson AO. Whole-genome sequencing of < i > Pantoea sp. Strain RIT388, a potential oral opportunistic Pathogen isolated from a chewing Stick (< i > Distemonanthus benthamianus). Microbiol Resource Announcements. 2020;9(9):e01468–19.
doi: 10.1128/MRA.01468-19
Asai N, Koizumi Y, Yamada A, Sakanashi D, Watanabe H, Kato H, et al. Pantoea dispersa bacteremia in an immunocompetent patient: a case report and review of the literature. J Med Case Rep. 2019;13(33):1–5.
Sengupta M, Banerjee S, Das NK, Guchhait P, Misra S. Early Onset neonatal septicaemia caused by Pantoea agglomerans. J Clin Diagn Res. 2016;10(5):Dd01–2.
pubmed: 27437219
pmcid: 4948395
Siwakoti S, Sah R, Rajbhandari RS, Khanal B. Pantoea agglomerans Ininfectionsn ChchildrenRereportf Twtwoases. Case Rep Pediatr. 2018;2018:1–3.
doi: 10.1155/2018/4158734
Tiwari S, Beriha SS. Pantoea species causing early onset neonatal sepsis: a case report. J Med Case Rep. 2015;9(188):1–3.
Yablon BR, Dantes R, Tsai V, Lim R, Moulton-Meissner H, Arduino M, et al. Outbreak of < i > Pantoea agglomerans bloodstream infections at an Oncology Clinic—Illinois, 2012–2013. Infect Control Hosp Epidemiol. 2017;38(3):314–9.
pubmed: 27919308
doi: 10.1017/ice.2016.265
Oliveira MI, Batalha S, Gouveia C, Maia R, Kjöllerstrom P. Pantoea species Bacteremia in a child with Sickle Cell Disease: looking for a culprit. J Pediatr Hematol Oncol. 2017;39(6):e307–8.
pubmed: 28267078
doi: 10.1097/MPH.0000000000000819
Schmid H, Weber SSC, Bogner JR. Isolation of a Pantoea dispersa -like strain from a 71-Year-old woman with Acute myeloid leukemia and multiple myeloma. Infection. 2003;31(1):66–7.
pubmed: 12608369
doi: 10.1007/s15010-002-3024-y
Mani S, Nair J. Pantoea infections in the neonatal Intensive Care Unit. Cureus. 2021;13(2):e13103.
pubmed: 33643749
pmcid: 7886163
Mardaneh J, Dallal MM. Isolation, identification and antimicrobial susceptibility of Pantoea (Enterobacter) agglomerans isolated from consumed powdered infant formula milk (PIF) in NICU ward: first report from Iran. Iran J Microbiol. 2013;5(3):263–7.
pubmed: 24475334
pmcid: 3895565
Kaur IP, Inkollu S, Prakash A, Gandhi H, Mughal MS, Du D. Pantoea agglomerans Bacteremia: is it dangerous? Case Rep Infect Dis. 2020;2020:7890305.
pubmed: 32313708
pmcid: 7160720
Gajdács M. Epidemiology and antibiotic resistance trends of Pantoea species in a tertiary-care teaching hospital: a 12-year retrospective study. Developments Health Sci. 2019;2(3):72–5.
doi: 10.1556/2066.2.2019.009
AbdAlhussen LS, Darweesh MF. Prevelance and antibiotic susceptibility patterns of Pantoea spp. isolated form clinical and environmental sources in Iraq. Int J ChemTech Res. 2016;9(8):430–7.
Bhatti MD, Kalia A, Sahasrabhojane P, Kim J, Greenberg DE, Shelburne SA. Identification and whole genome sequencing of the first case of Kosakonia radicincitans causing a human bloodstream infection. Front Microbiol. 2017;8:62.
pubmed: 28174569
pmcid: 5258702
doi: 10.3389/fmicb.2017.00062
Sng ECY, Goh KCM, Tan SH, Tan AL, Oh HML. Leclercia adecarboxylata bacteraemia: clinical features and antibiotic susceptibilities in 2 hospitals in Singapore. Ann Acad Med Singapore. 2021;50(8):643–5.
pubmed: 34472560
doi: 10.47102/annals-acadmedsg.202195
Singhal N, Kumar M, Kanaujia PK, Virdi JS. MALDI-TOF mass spectrometry: an emerging technology for microbial identification and diagnosis. Front Microbiol. 2015;6:791.
pubmed: 26300860
pmcid: 4525378
doi: 10.3389/fmicb.2015.00791
Soutar CD, Stavrinides J. Molecular validation of clinical Pantoea isolates identified by MALDI-TOF. PLoS ONE. 2019;14(11):e0224731.
pubmed: 31682625
pmcid: 6827907
doi: 10.1371/journal.pone.0224731
Zayet S, Lang S, Garnier P, Pierron A, Plantin J, Toko L, et al. Leclercia adecarboxylata as Emerging Pathogen in Human infections: clinical features and Antimicrobial susceptibility testing. Pathogens. 2021;10(11):1399.
pubmed: 34832555
pmcid: 8619052
doi: 10.3390/pathogens10111399
Legese MH, Asrat D, Swedberg G, Hasan B, Mekasha A, Getahun T, et al. Sepsis: emerging pathogens and antimicrobial resistance in Ethiopian referral hospitals. Antimicrob Resist Infect Control. 2022;11(83):1–6.
Institute CLS. Performance standards for antimicrobial susceptibility testing;30th ed. CLSI. 2020;M100.
Andrews S. FastQC: A Quality Control Tool for High Throughput Sequence Data [Online]. Available online at: http://www.bioinformatics.babraham.ac.uk/projects/fastqc/ . 2010.
Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30(15):2114–20.
pubmed: 24695404
pmcid: 4103590
doi: 10.1093/bioinformatics/btu170
Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics. 2013;29(8):1072–5.
pubmed: 23422339
pmcid: 3624806
doi: 10.1093/bioinformatics/btt086
Hunt M, Mather AE, Sánchez-Busó L, Page AJ, Parkhill J, Keane JA, et al. ARIBA: rapid antimicrobial resistance genotyping directly from sequencing reads. Microb Genom. 2017;3(10):e000131.
pubmed: 29177089
pmcid: 5695208
Gupta SK, Padmanabhan BR, Diene SM, Lopez-Rojas R, Kempf M, Landraud L, et al. ARG-ANNOT, a new bioinformatic tool to discover antibiotic resistance genes in bacterial genomes. Antimicrob Agents Chemother. 2014;58(1):212–20.
pubmed: 24145532
pmcid: 3910750
doi: 10.1128/AAC.01310-13
Carattoli A, Zankari E, García-Fernández A, Larsen MV, Lund O, Villa L, et al. In Silico Detection and Tytypingf Plplasmidssing PlasmidFinder and Plplasmidumultilocusesequenceyping. Antimicrob Agents Chemother. 2014;58(7):3895–903.
pubmed: 24777092
pmcid: 4068535
doi: 10.1128/AAC.02412-14
Seemann T, Shovill. Faster SPAdes assembly of Illumina reads. https://github.com/tseemann/shovill . 2017.
Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014;30(14):2068–9.
pubmed: 24642063
doi: 10.1093/bioinformatics/btu153
Carver T, Harris SR, Berriman M, Parkhill J, McQuillan JA. Artemis: an integrated platform for visualization and analysis of high-throughput sequence-based experimental data. Bioinformatics. 2012;28(4):464–9.
pubmed: 22199388
doi: 10.1093/bioinformatics/btr703
Madeira F, Madhusoodanan N, Lee J, Eusebi A, Niewielska A, Tivey ARN, et al. The EMBL-EBI Job dispatcher sequence analysis tools framework in 2024. Nucleic Acids Res. 2024;52(W1):W521–5.
pubmed: 38597606
pmcid: 11223882
doi: 10.1093/nar/gkae241
Seemann T. Snippy: rapid haploid variant calling and core SNP phylogeny. 2015.
Croucher NJ, Page AJ, Connor TR, Delaney AJ, Keane JA, Bentley SD, et al. Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res. 2014;43(3):e15–e.
pubmed: 25414349
pmcid: 4330336
doi: 10.1093/nar/gku1196
Page AJ, Taylor B, Delaney AJ, Soares J, Seemann T, Keane JA, et al. SNP-sites: rapid efficient extraction of SNPs from multi-FASTA alignments. Microb Genom. 2016;2(4):e000056.
pubmed: 28348851
pmcid: 5320690
Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2014;32(1):268–74.
pubmed: 25371430
pmcid: 4271533
doi: 10.1093/molbev/msu300
Lee I, Ouk Kim Y, Park S-C, Chun J. OrthoANI: an improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol MicroBiol. 2016;66(2):1100–3.
pubmed: 26585518
doi: 10.1099/ijsem.0.000760
Letunic I, Bork P. Interactive tree of life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics. 2007;23(1):127–8.
pubmed: 17050570
doi: 10.1093/bioinformatics/btl529
Chalita M, Kim YO, Park S, Oh HS, Cho JH, Moon J et al. EzBioCloud: a genome-driven database and platform for microbiome identification and discovery. Int J Syst Evol Microbiol. 2024;74(6).
WHO. Improving the prevention, diagnosis and clinical management of sepsis. 2017; https://apps.who.int/gb/ebwha/pdf_files/EB140/B140_12-en.pdf
Sękowska A, Gospodarek-Komkowska E. New species of Bacteria in human infections. Postępy Mikrobiologii - Advancements Microbiol. 2019;58(1):29–34.
doi: 10.21307/PM-2019.58.1.029
Panditrao P M, Panditrao P M. Pantoea dispersa it the next emerging monster in our intensive care units? A case report and review of literature. Anesthesia: Essays Researches. 2018;12(4):963–6.
Mahapatra A, Dhal S, Jena PP, Mohapatra A, Dash D, Padhee A. Neonatal septicaemia due to a rare bacterium: Pantoea agglomerans (case series). Pediatr Infect Disease. 2014;6(3):102–4.
doi: 10.1016/j.pid.2014.02.001
Hagiya H, Otsuka F. Pantoea dispersa bacteremia caused by central line-associated bloodstream infection. Brazilian J Infect Dis. 2014;18(6):696–7.
doi: 10.1016/j.bjid.2014.06.006
Dargère S, Cormier H, Verdon R. Contaminants in blood cultures: importance, implications, interpretation and prevention. Clin Microbiol Infect. 2018;24(9):964–9.
pubmed: 29621616
doi: 10.1016/j.cmi.2018.03.030