Restricted accessResearch articleFirst published online 2022-07
Carriage Duration and Household Transmission of Enterobacterales Producing Extended-Spectrum Beta-Lactamase in the Community: A Systematic Review and Meta-Analysis
An attributing factor to Enterobacterales producing extended-spectrum beta-lactamase (ESBL-E) community spread is human-to-human transmission. This systematic review and meta-analysis aimed to estimate the duration of ESBL-E carriage in the community and the rate of household transmission. Literature search was performed on PubMed, EMBASE, and Scopus. Dose-response meta-analysis was planned to model the proportion of ESBL-E carriers and household transmission over time. Twenty-six studies (n = 2,505 participants) were included. The median carriage duration was 2 months. Approximately 22% (95% confidence interval: 16–28) had persistent carriage after 12 months. Travelers had significantly shorter carriage (median 1–2 months) than discharged hospital patients (median 6 months) at all measured time points. There were insufficient data to robustly meta-analyze household transmission. Nonetheless, five longitudinal studies reported 18.4% to 35.2% of contacts acquired ESBL-E within 4 to 36 months from hospital discharge of index case. Transmission events from travelers to their contacts appeared lower. Travelers with travel-acquired ESBL-E had significantly faster decolonization rate than discharged patients, suggesting that travel-associated import of multidrug-resistant pathogen may have limited contribution to community transmission of ESBL-E. The substantial prevalence of persistent carriers warrant consideration for additional measures to mitigate exposure risk of ESBL-E from discharged patients in the community and from readmitting patients in the hospital.
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References
1.
WoertherP.L., BurdetC., ChachatyE., and AndremontA.. 2013. Trends in human fecal carriage of extended-spectrum β-lactamases in the community: toward the globalization of CTX-M. Clin. Microbiol. Rev. 26:744–758.
2.
BevanE.R., JonesA.M, and HawkeyP.M.. 2017. Global epidemiology of CTX-M β-lactamases: temporal and geographical shifts in genotype. J. Antimicrob. Chemother. 72:2145–2155.
3.
BezabihY.M., SabiitiW., AlamnehE., et al.2021. The global prevalence and trend of human intestinal carriage of ESBL-producing Escherichia coli in the community. J. Antimicrob. Chemother. 76:22–29.
4.
RogersB.A., SidjabatH.E, and PatersonD.L.. 2011. Escherichia coli O25b-ST131: a pandemic, multiresistant, community-associated strain. J. Antimicrob. Chemother. 66:1–14.
5.
MangesA.R., GeumH.M, GuoA., EdensT.J, FibkeC.D, and PitoutJ.D.D. 2019. Global extraintestinal pathogenic Escherichia coli (ExPEC) lineages. Clin. Microbiol. Rev. 32:e00135-18.
6.
Mughini-GrasL., Dorado-GarcíaA., van DuijkerenE., et al.2019. Attributable sources of community-acquired carriage of Escherichia coli containing β-lactam antibiotic resistance genes: a population-based modelling study. Lancet Planet. Health, 3:e357–e369.
7.
BlakistonM.R., and FreemanJ.T.. 2020. Population-level exposures associated with MRSA and ESBL-E. coli infection across district health boards in Aotearoa New Zealand: an ecological study. N. Z. Med. J. 133:62–69.
8.
Kardaś-SłomaL., YazdanpanahY., PerozzielloA., et al.2020. Hand hygiene improvement or antibiotic restriction to control the household transmission of extended-spectrum β-lactamase-producing Escherichia coli: a mathematical modelling study. Antimicrob. Resist. Infect. Control, 9:139.
9.
WoertherP.-L., AndremontA., and KanteleA.. 2017. Travel-acquired ESBL-producing Enterobacteriaceae: impact of colonization at individual and community level. J. Travel Med. 24:S29–S34.
10.
KaranikaS., KarantanosT., ArvanitisM., GrigorasC., and MylonakisE.. 2016. Fecal colonization with extended-spectrum beta-lactamase-producing Enterobacteriaceae and risk factors among healthy individuals: A systematic review and metaanalysis. Clin. Infect. Dis. 63:310–318.
11.
RoerL., HansenF., HasmanH., HammerumA.M, and CavacoL.M.. 2020. Characterisation of extended-spectrum β-lactamase/plasmid AmpC-β-lactamase-producing Escherichia coli isolates from long-term recurrent bloodstream infections. Int. J. Antimicrob. Agents, 56:106041.
12.
LeeC.-H., SuL.-H, ChenF.-J, TangY.-F, ChienC.-C, and LiuJ.-W.. 2015. Clinical and microbiologic characteristics of adult patients with recurrent bacteraemia caused by extended-spectrum β-lactamase-producing Escherichia coli or Klebsiella pneumoniae. Clin. Microbiol. Infect. 21:1105.e1–e1105.e8.
13.
LingW., Furuya-KanamoriL., EzureY., HarrisP.N.A, and PatersonD.L.. 2021. Adverse clinical outcomes associated with infections by Enterobacterales producing ESBL (ESBL-E): a systematic review and meta-analysis. JAC Antimicrobial Resist. 3:dlab068.
14.
StroupD.F., BerlinJ.A, MortonS.C, et al.2000. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis of Observational Studies in Epidemiology (MOOSE) group. JAMA, 283:2008–2012.
15.
OuzzaniM., HammadyH., FedorowiczZ., and ElmagarmidA.. 2016. Rayyan-a web and mobile app for systematic reviews. Syst. Rev. 5:210.
16.
TufanaruC., Z. Munn, E. Aromataris, J. Campbell, and L. Hopp. Chapter 3: systematic reviews of effectiveness. In: E. Aromataris and Z. Munn (eds). Joanna Briggs Institute Reviewer's Manual. The Joanna Briggs Institute, 2017.
17.
WellsG.A., B. Shea, D. O'Connell, J. Peterson, V. Welch, M. Losos, and P. Tugwell. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. Available at http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp
18.
XuC., and DoiS.A.R. 2018. The robust error meta-regression method for dose–response meta-analysis. Int. J. Evid. Based. Healthc. 16:138–144.
19.
LukacP.J., BonomoR.A, and LoganL.K.. 2015. Extended-spectrum β-lactamase-producing Enterobacteriaceae in children: old foe, emerging threat. Clin. Infect. Dis. 60:1389–1397.
20.
Furuya-KanamoriL., XuC., and DoiS.A.. 2021. REMR: stata module to implement robust error meta-regression method for dose–response meta-analysis. Statistical Software Components, S458793, Boston College Department of Economics.
21.
ÖstholmBalkhed, Å., TärnbergM., NilssonM., NilssonL.E, HanbergerH., and HällgrenA.. 2018. Duration of travel-associated faecal colonisation with ESBL-producing Enterobacteriaceae—a one year follow-up study. PLoS One, 13:e0205504.
22.
ArcillaM.S., van HattemJ.M, HaverkateM.R, et al.2017. Import and spread of extended-spectrum β-lactamase-producing Enterobacteriaceae by international travellers (COMBAT study): a prospective, multicentre cohort study. Lancet Infect. Dis. 17:78–85.
23.
LübbertC., StraubeL., SteinC., et al.2015. Colonization with extended-spectrum beta-lactamase-producing and carbapenemase-producing Enterobacteriaceae in international travelers returning to Germany. Int. J. Med. Microbiol. 305:148–156.
24.
PaltansingS., VlotJ.A, KraakmanM.E.M, et al.2013. Extended-spectrum β-lactamase-producing Enterobacteriaceae among travelers from the Netherlands. Emerg. Infect. Dis. 19:1206–1213.
25.
PiresJ., KraemerJ.G, KuenzliE., et al.2019. Gut microbiota dynamics in travelers returning from India colonized with extended-spectrum cephalosporin-resistant Enterobacteriaceae: a longitudinal study. Travel Med. Infect. Dis. 27:72–80.
26.
SchaumburgF., SerticS.M, Correa-MartinezC., MellmannA., KöckR., and BeckerK.. 2019. Acquisition and colonization dynamics of antimicrobial-resistant bacteria during international travel: a prospective cohort study. Clin. Microbiol. Infect. 25:1287.e1–e1287.e7.
27.
TängdénT., CarsO., MelhusA., and LöwdinE.. 2010. Foreign travel is a major risk factor for colonization with Escherichia coli producing CTX-M-type extended-spectrum β-lactamases: a prospective study with Swedish volunteers. Antimicrob. Agents Chemother. 54:3564–3568.
28.
ThamJ., WalderM., MelanderE., and OdenholtI.. 2012. Duration of colonization with extended-spectrum beta-lactamase-producing Escherichia coli in patients with travellers' diarrhoea. Scand. J. Infect. Dis. 44:573–577.
29.
WorbyC.J., EarlA.M, TurbettS.E, et al.2020. Acquisition and long-term carriage of multidrug-resistant organisms in US international travelers. Open Forum Infect. Dis. 7:ofaa543.
30.
BevanE.R., McNallyA., ThomasC.M, PiddockL.J.V, and HawkeyP.M. 2018. Acquisition and loss of CTX-M-producing and non-producing Escherichia coli. in the fecal microbiome of travelers to South Asia. MBio 9: e02408–e0, 2418.
31.
BirgandG., Armand-LefevreL., LolomI., RuppeE., AndremontA., and LucetJ.-C.. 2013. Duration of colonization by extended-spectrum β-lactamase-producing Enterobacteriaceae after hospital discharge. Am. J. Infect. Control, 41:443–447.
32.
HagelS., MakarewiczO., HartungA., et al.2019. ESBL colonization and acquisition in a hospital population: the molecular epidemiology and transmission of resistance genes. PLoS One, 14:e0208505.
33.
HaverkateM.R., T.N. Platteel, A.C. Fluit, et al. 2017. Quantifying within-household transmission of extended-spectrum β-lactamase-producing bacteria. Clin. Microbiol. Infect. 23:46.e1–e46.e7.
34.
JørgensenS.B., SøraasA., SundsfjordA., LiestølK., LeegaardT.M, and JenumP.A.. 2017. Fecal carriage of extended spectrum β-lactamase producing Escherichia coli and Klebsiella pneumoniae after urinary tract infection—a three year prospective cohort study. PLoS One, 12:e0173510.
35.
LohrI.H., RettedalS., NatasO.B, NaseerU., OymarK., and SundsfjordA.. 2013. Long-term faecal carriage in infants and intra-household transmission of CTX-M-15-producing Klebsiella pneumoniae following a nosocomial outbreak. J. Antimicrob. Chemother. 68:1043–1048.
36.
NordbergV., JonssonK., GiskeC.G, et al.2018. Neonatal intestinal colonization with extended-spectrum β-lactamase–producing Enterobacteriaceae—a 5-year follow-up study. Clin. Microbiol. Infect. 24:1004–1009.
37.
StrengerV., FeierlG., ReschB., et al.2013. Fecal carriage and intrafamilial spread of extended-spectrum β-lactamase-producing Enterobacteriaceae following colonization at the neonatal ICU. Pediatr. Crit. Care Med. 14:157–163.
38.
TitelmanE., HasanC.M, IversenA., et al.2014. Faecal carriage of extended-spectrum β-lactamase-producing Enterobacteriaceae is common 12 months after infection and is related to strain factors. Clin. Microbiol. Infect. 20:O508–O515.
39.
WendtR., NickelO., BotschA., et al.2020. Low colonization rates with Multidrug-resistant Gram-negative bacteria in a German hospital-affiliated hemodialysis center. PLoS One, 15:e0240314.
40.
FreemanJ.T., GormackS., De AlmeidaM.N, and RobertsS.A.. 2013. Natural history of rectal colonisation with extended- spectrum beta-lactamase producing Enterobacteriaceae: a retrospective review with up to 6 years of follow-up. Healthc. Infect. 18:152–155.
41.
van der ZwetW.C., van RiessenN., BergervoetP.W.M, van der LaanJ.R, SavelkoulP.H.M, and SebensF.W.. 2005. [Outbreak of multi-resistant Escherichia coli on a surgical ward: course, measures and consequences for future admissions of contaminated patients]. Ned. Tijdschr. Geneeskd. 149:2281–2286.
42.
ApisarnthanarakA., BaileyT.C, and FraserV.J.. 2008. Duration of stool colonization in patients infected with extended-spectrum β-lactamase–producing Escherichia coli and Klebsiella pneumoniae. Clin. Infect. Dis. 46:1322–1323.
43.
LjungquistO., SchönbeckM., RiesbeckK., and ThamJ.. 2019. Risk factors associated with prolonged intestinal colonization of ESBL-producing Enterobacteriaceae—a prospective cohort study. Infect. Drug Resist. 12:2637–2648.
44.
Salazar-OspinaL., VanegasJ.M, and JiménezJ.N.. 2021. High intermittent colonization by diverse clones of β-lactam-resistant Gram-negative bacilli suggests an excessive antibiotic use and different sources of transmission in haemodialysis patients. J. Hosp. Infect. 107:76–86.
45.
RoydenA., OrmandyE., PinchbeckG., et al.2019. Prevalence of faecal carriage of extended-spectrum β-lactamase (ESBL)-producing Escherichia coli in veterinary hospital staff and students. Vet. Rec. Open, 6:e000307.
46.
van den BuntG., FluitA.C, BootsmaM.C.J, et al.2020. Dynamics of intestinal carriage of extended-spectrum beta-lactamase-producing Enterobacteriaceae in the Dutch General Population, 2014–2016. Clin. Infect. Dis. 71:1847–1855.
47.
HiltyM., BetschB.Y, Bögli-StuberK., et al.2012. Transmission dynamics of extended-spectrum β-lactamase-producing Enterobacteriaceae in the tertiary care hospital and the household setting. Clin. Infect. Dis. 55:967–975.
48.
RiccioM.E., VerschuurenT., ConzelmannN., et al.2021. Household acquisition and transmission of extended-spectrum β-lactamase (ESBL)-producing Enterobacteriaceae after hospital discharge of ESBL-positive index patients. Clin. Microbiol. Infect. 27:1322–1329.
49.
LiakopoulosA., van den BuntG., GeurtsY., et al.2018. High prevalence of intra-familial co-colonization by extended-spectrum cephalosporin resistant Enterobacteriaceae in preschool children and their parents in Dutch households. Front. Microbiol. 9:293.
50.
LoW.-U., HoP.-L, ChowK.-H, LaiE.L, YeungF., and ChiuS.S.. 2010. Fecal carriage of CTXM type extended-spectrum beta-lactamase-producing organisms by children and their household contacts. J. Infect. 60:286–292.
51.
Rodriguez-BanoJ., Lopez-CereroL., NavarroM.D, de AlbaP.D, and PascualA.. 2008. Faecal carriage of extended-spectrum -lactamase-producing Escherichia coli: prevalence, risk factors and molecular epidemiology. J. Antimicrob. Chemother. 62:1142–1149.
52.
Toombs-RuaneL.J., BenschopJ., FrenchN.P, et al.2020. Carriage of extended-spectrum-beta-lactamase- and AmpC beta-lactamase-producing Escherichia coli strains from humans and pets in the same households. Appl. Environ. Microbiol. 86:e01613–e01620.
53.
Furuya-KanamoriL., StoneJ., YakobL., et al.2020. Risk factors for acquisition of multidrug-resistant Enterobacterales among international travellers: a synthesis of cumulative evidence. J. Travel Med. 27:taz083.
54.
Bar-YosephH., HusseinK., BraunE., and PaulM.. 2016. Natural history and decolonization strategies for ESBL/carbapenem-resistant Enterobacteriaceae carriage: systematic review and meta-analysis. J. Antimicrob. Chemother. 71:2729–2739.
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