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Research Paper

Effects of breastfeeding on children’s gut colonization with multidrug-resistant Enterobacterales in peri-urban Lima, Peru

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Article: 2309681 | Received 24 Jul 2023, Accepted 19 Jan 2024, Published online: 01 Feb 2024

References

  • Murray CJL, Ikuta KS, Sharara F, Swetschinski L, Robles Aguilar G, Gray A, Han C, Bisignano C, Rao P, Wool E. et al. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. The Lancet. 2022 Feb 12;399(10325):629–16. doi:10.1016/S0140-6736(21)02724-0.
  • Ruppé E, Lixandru B, Cojocaru R, Büke C, Paramythiotou E, Angebault C, Visseaux C, Djuikoue I, Erdem E, Burduniuc O. et al. Relative fecal abundance of extended-spectrum-β-lactamase-producing Escherichia coli strains and their occurrence in urinary tract infections in women. Antimicrob Agents Chemother. 2013 Sep;57(9):4512–4517. doi:10.1128/AAC.00238-13. PMCID: PMC3754361.
  • Denis B, Lafaurie M, Donay JL, Fontaine JP, Oksenhendler E, Raffoux E, Hennequin C, Allez M, Socie G, Maziers N. et al. Prevalence, risk factors, and impact on clinical outcome of extended-spectrum beta-lactamase-producing Escherichia coli bacteraemia: a five-year study. Int J Infect Dis. 2015 Oct;39:1–6. doi:10.1016/j.ijid.2015.07.010. PMID: 26189774.
  • Islam MA, Amin MB, Roy S, Asaduzzaman M, Islam MR, Navab-Daneshmand T, Mattioli MC, Kile ML, Levy K, Julian TR. Fecal colonization with multidrug-resistant E. coli among healthy infants in rural Bangladesh. Front Microbiol. 2019;10:640. doi:10.3389/fmicb.2019.00640.
  • Kothari C, Gaind R, Singh LC, Sinha A, Kumari V, Arya S, Chellani H, Saxena S, Deb M. Community acquisition of β-lactamase producing Enterobacteriaceae in neonatal gut. BMC Microbiol. 2013 Jun 17;13(1):136. doi:10.1186/1471-2180-13-136. PMCID: PMC3689095.
  • Herindrainy P, Rabenandrasana MAN, Andrianirina ZZ, Rakotoarimanana FMJ, Padget M, de Lauzanne A, Ndir A, Kermorvant-Duchemin E, Garin B, Piola P. et al. Group for the B study. Acquisition of extended spectrum beta-lactamase-producing Enterobacteriaceae in neonates: a community based cohort in Madagascar. PloS ONE. 2018;13(3):1–17. doi:10.1371/journal.pone.0193325.
  • Hofmann P, Alabi A, Manouana GP, Onwugamba FC, Hasenauer A, Agbanrin MD, Gouleu CSM, Bingoulou G, Borrmann S, McCall MBB. et al. High ESBL-E colonization rate among children in Gabon: a follow-up study. J Med Microbiol [Internet]. 2021 Aug 17;70:(8):001405. [accessed 2022 Mar 25]. doi:10.1099/jmm.0.001405.
  • Matheu J, Aidara-Kane A, Andremont A. The ESBL tricycle AMR surveillance project: a simple, one health approach to global surveillance. AMR Control: Overcoming Global Antimicrobial Resistance [Internet]. Paris; 2017. http://resistancecontrol.info/2017/the-esbl-tricycle-amr-surveillance-project-a-simple-one-health-approach-to-global-surveillance/.
  • Montealegre MC, Greenwood EE, Teichmann L, Nadimpalli ML, Caduff L, Swarthout JM, Nydegger T, Sultana S, Islam MA, Lanza VF. et al. Drinking water chlorination impact on fecal carriage of extended-spectrum beta-lactamase-producing Enterobacteriaceae in Bangladeshi children in a double-blind, cluster-randomized controlled trial. Environ Health Perspect. 2022 Nov;130(11):117702. doi:10.1289/EHP11359. PMCID: PMC9683094.
  • Berendes D, Knee J, Sumner T, Capone D, Lai A, Wood A, Patel S, Nalá R, Cumming O, Brown J. et al. Gut carriage of antimicrobial resistance genes among young children in urban Maputo, Mozambique: associations with enteric pathogen carriage and environmental risk factors. PloS ONE. 2019;14(11):e0225464. doi:10.1371/journal.pone.0225464. PMCID: PMC6874316.
  • Caruso BA, Paniagua U, Hoffman I, Manji K, Saidi F, Sudfeld CR, Vernekar SS, Bakari M, Duggan CP, Kibogoyo GC. et al. Safe infant feeding in healthcare facilities: assessment of infection prevention and control conditions and behaviors in India, Malawi, and Tanzania. PLOS Glob Public Health. 2023;3(6):e0001843. doi:10.1371/journal.pgph.0001843. PMCID: PMC10249877.
  • Rothstein JD, Mendoza AL, Cabrera LZ, Pachas J, Calderón M, Pajuelo MJ, Caulfield LE, Winch PJ, Gilman RH. Household contamination of baby bottles and opportunities to improve bottle hygiene in Peri-Urban Lima, Peru. Am J Trop Med Hyg. 2019 Apr 3;100(4):988–997. doi:10.4269/ajtmh.18-0301.
  • Taft DH, Liu J, Maldonado-Gomez MX, Akre S, Huda MN, Ahmad SM, Stephensen CB, Mills DA, Suen G. Bifidobacterial dominance of the gut in early life and acquisition of antimicrobial resistance. mSphere. 2018 26;3(5):e00441–18. doi:10.1128/mSphere.00441-18. PMCID: PMC6158511.
  • McCormick BJJ, Richard SA, Murray-Kolb LE, Kang G, Lima AAM, Mduma E, Kosek MN, Rogawski McQuade ET, Houpt ER, Bessong P. et al. MAL-ED network investigators. Full breastfeeding protection against common enteric bacteria and viruses: results from the MAL-ED cohort study. Am J Clin Nutr. 2022 Mar 4;115(3):759–769. doi:10.1093/ajcn/nqab391. PMCID: PMC8895209.
  • Ochoa TJ, Cleary TG. Effect of lactoferrin on enteric pathogens. Biochimie. 2009 Jan;91(1):30–34. doi:10.1016/j.biochi.2008.04.006. PMCID: PMC2626156.
  • Peterson R, Cheah WY, Grinyer J, Packer N. Glycoconjugates in human milk: protecting infants from disease. Glycobiology. 2013 Dec;23(12):1425–1438. doi:10.1093/glycob/cwt072. PMID: 24000281.
  • Alamiri F, Riesbeck K, Hakansson AP. HAMLET, a protein complex from human milk, has bactericidal activity and enhances the activity of antibiotics against pathogenic streptococci. Antimicrob Agents Chemother. 2019 Dec 1;63(12):e01193–19. doi:10.1128/AAC.01193-19.
  • Davisse-Paturet C, Adel-Patient K, Divaret-Chauveau A, Pierson J, Lioret S, Cheminat M, Dufourg MN, Charles MA, de Lauzon-Guillain B. Breastfeeding status and duration and infections, hospitalizations for infections, and antibiotic use in the first two years of life in the ELFE Cohort. Nutrients. 2019 Jul 15;11(7):1607. doi:10.3390/nu11071607. PMCID: PMC6682893.
  • Korpela K, Salonen A, Virta LJ, Kekkonen RA, de Vos WM. Association of early-life antibiotic use and protective effects of breastfeeding: role of the intestinal microbiota. JAMA Pediatr. 2016 Aug 1;170(8):750. doi:10.1001/jamapediatrics.2016.0585.
  • Lipsitch M, Samore MH. Antimicrobial use and antimicrobial resistance: a population perspective. Emerg Infect Dis. 2002 Apr;8(4):347–354. doi:10.3201/eid0804.010312. PMCID: PMC2730242.
  • Rogawski ET, Platts-Mills JA, Seidman JC, John S, Mahfuz M, Ulak M, Shrestha SK, Soofi SB, Yori PP, Mduma E. et al. Use of antibiotics in children younger than two years in eight countries: a prospective cohort study. Bull World Health Organ. 2017 Jan 1;95(1):49–61. doi:10.2471/BLT.16.176123. PMCID: PMC5180352.
  • Pajuelo MJ, Noazin S, Cabrera L, Toledo A, Velagic M, Arias L, Ochoa M, Moulton LH, Saito M, Gilman RH. et al. Epidemiology of enterotoxigenic Escherichia coli and impact on the growth of children in the first two years of life in Lima, Peru. In Revision at Frontiers in Public Health. 2023.
  • Saito M, Goel-Apaza S, Espetia S, Velasquez D, Cabrera L, Loli S, Crabtree JE, Black RE, Kosek M, Checkley W. et al. Multiple norovirus infections in a birth cohort in a Peruvian Periurban community. Clin Infect Dis. 2014 Feb;58(4):483–491. doi:10.1093/cid/cit763. PMCID: PMC3905757.
  • Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Royal Stat Soc Series B (Methodol) [Royal Stat Soc, Wiley]. 1995;57(1):289–300. doi:10.1111/j.2517-6161.1995.tb02031.x.
  • Nadimpalli ML, Marks SJ, Montealegre MC, Gilman RH, Pajuelo MJ, Saito M, Tsukayama P, Njenga SM, Kiiru J, Swarthout J. et al. Urban informal settlements as hotspots of antimicrobial resistance and the need to curb environmental transmission. Nat Microbiol. 2020 Jun 1;5(6):787–795. doi:10.1038/s41564-020-0722-0.
  • Nicolas-Chanoine MH, Bertrand X, Madec JY. Escherichia coli ST131, an intriguing clonal group. Clin Microbiol Rev. 2014 Jul;27(3):543–574. doi:10.1128/CMR.00125-13. PMCID: PMC4135899.
  • Tchesnokova VL, Rechkina E, Larson L, Ferrier K, Weaver JL, Schroeder DW, She R, Butler-Wu SM, Aguero-Rosenfeld ME, Zerr D. et al. Rapid and extensive expansion in the United States of a new multidrug-resistant Escherichia coli clonal group, sequence type 1193. Clin Infect Dis. 2019 Jan 7;68(2):334–337. doi: 10.1093/cid/ciy525.
  • Abreu-Salinas F, Díaz-Jiménez D, García-Meniño I, Lumbreras P, López-Beceiro AM, Fidalgo LE, Rodicio MR, Mora A, Fernández J. High prevalence and diversity of cephalosporin-resistant Enterobacteriaceae including extraintestinal pathogenic E. coli CC648 Lineage in Rural and urban dogs in Northwest Spain. Antibiot (Basel). 2020 Aug 1;9(8):E468. doi:10.3390/antibiotics9080468. PMCID: PMC7460362.
  • Infant and young child feeding: Fact Sheet [Internet]. Geneva: World Health Organization; 2021. https://www.who.int/news-room/fact-sheets/detail/infant-and-young-child-feeding
  • U.S. Department of Health and Human Services. Centers for Disease Control and Prevention (CDC). Antibiotic resistance threats in the United States, 2019 [internet]. Atlanta, GA; 2019 p. 148. https://www.cdc.gov/drugresistance/pdf/threats-report/2019-ar-threats-report-508.pdf
  • Bevan ER, McNally A, Thomas CM, Piddock LJV, Hawkey PM, Jacoby GA. Acquisition and loss of CTX-M-Producing and non-producing Escherichia coli in the fecal microbiome of Travelers to South Asia. Jacoby GA, editor. mBio. 2018 Dec 21;9(6):e02408–18. doi:10.1128/mBio.02408-18.
  • Kantele A, Kuenzli E, Dunn SJ, Dance DAB, Newton PN, Davong V, Mero S, Pakkanen SH, Neumayr A, Hatz C. et al. Dynamics of intestinal multidrug-resistant bacteria colonisation contracted by visitors to a high-endemic setting: a prospective, daily, real-time sampling study. Lancet Microbe. 2021 Apr;2(4):e151–e158. doi: 10.1016/S2666-5247(20)30224-X.
  • Salinas L, Cárdenas P, Johnson TJ, Vasco K, Graham J, Trueba G, Castanheira M. Diverse Commensal Escherichia coli Clones and Plasmids Disseminate Antimicrobial Resistance Genes in Domestic Animals and Children in a Semirural Community in Ecuador. mSphere. 2019 Jun 26;4(3):e00316–19. doi:10.1128/mSphere.00316-19. PMID: 31118304.
  • Salinas L, Loayza F, Cárdenas P, Saraiva C, Johnson TJ, Amato H, Graham JP, Trueba G. Environmental spread of extended spectrum beta-lactamase (ESBL) producing Escherichia coli and ESBL genes among children and domestic animals in Ecuador. Environ Health Perspect. 2021 Feb;129(2):027007. doi: 10.1289/EHP7729.
  • Fuentes-Castillo D, Farfán-López M, Esposito F, Moura Q, Fernandes MR, Lopes R, Cardoso B, Muñoz ME, Cerdeira L, Najle I. et al. Wild owls colonized by international clones of extended-spectrum β-lactamase (CTX-M)-producing Escherichia coli and Salmonella Infantis in the Southern Cone of America. Sci Total Environ. 2019 Jul 15;674:554–562. doi:10.1016/j.scitotenv.2019.04.149. PMID: 31022545.
  • Guzman-Otazo J, Gonzales-Siles L, Poma V, Bengtsson-Palme J, Thorell K, Flach CF, Iñiguez V, Sjöling Å, Goodman J. Diarrheal bacterial pathogens and multi-resistant enterobacteria in the Choqueyapu River in La Paz, Bolivia. Goodman J, editor. PloS ONE. 2019 Jan 14;14(1):e0210735. doi:10.1371/journal.pone.0210735.
  • Montero L, Irazabal J, Cardenas P, Graham JP, Trueba G. Extended-Spectrum Beta-Lactamase Producing-Escherichia coli Isolated From Irrigation Waters and Produce in Ecuador. Front Microbiol [Internet]. 2021;12. [accessed 2022 May 12]. doi:10.3389/fmicb.2021.709418.
  • Medina-Pizzali ML, Venkatesh A, Riveros M, Cuicapuza D, Salmon-Mulanovich G, Mäusezahl D, Hartinger SM. Whole-genome characterisation of ESBL-Producing E. coli isolated from drinking water and dog faeces from rural Andean households in Peru. Antibiot (Basel). 2022 May 20;11(5):692. doi:10.3390/antibiotics11050692. PMCID: PMC9137468.
  • Murray M, Salvatierra G, Dávila-Barclay A, Ayzanoa B, Castillo-Vilcahuaman C, Huang M, Pajuelo MJ, Lescano AG, Cabrera L, Calderón M. et al. Market chickens as a source of antibiotic-resistant Escherichia coli in a Peri-Urban Community in Lima, Peru. Front Microbiol. 2021 Mar 2;12:635871. doi:10.3389/fmicb.2021.635871.
  • Benavides JA, Godreuil S, Opazo-Capurro A, Mahamat OO, Falcon N, Oravcova K, Streicker DG, Shiva C. Long-term maintenance of multidrug-resistant Escherichia coli carried by vampire bats and shared with livestock in Peru. Sci Total Environ. 2022 Mar 1;810:152045. doi:10.1016/j.scitotenv.2021.152045. PMID: 34883172.
  • Bastidas-Caldes C, Romero-Alvarez D, Valdez-Vélez V, Morales RD, Montalvo-Hernández A, Gomes-Dias C, Calvopiña M. Extended-spectrum beta-lactamases producing Escherichia coli in South America: a systematic review with a one health perspective. Infect Drug Resist. 2022;15:5759–5779. doi:10.2147/IDR.S371845. PMCID: PMC9531622.
  • Kaarme J, Riedel H, Schaal W, Yin H, Nevéus T, Melhus Å. Rapid Increase in carriage rates of Enterobacteriaceae producing extended-spectrum β-lactamases in healthy preschool children, Sweden. Emerg Infect Dis. 2018;24(10):1874–1881. doi:10.3201/eid2410.171842. PMCID: PMC6154144.
  • Fernández-Reyes M, Vicente D, Gomariz M, Esnal O, Landa J, Oñate E, Pérez-Trallero E. High rate of fecal carriage of extended-spectrum-β-lactamase-producing Escherichia coli in healthy children in Gipuzkoa, Northern Spain. Antimicrob Agents Chemother. 2014 Mar;58(3):1822–1824. doi: 10.1128/AAC.01503-13.
  • Nadimpalli M, Vuthy Y, de Lauzanne A, Fabre L, Criscuolo A, Gouali M, Huynh BT, Naas T, Phe T, Borand L. et al. Meat and fish as sources of extended-spectrum β-Lactamase–Producing Escherichia coli, Cambodia. Emerg Infect Dis. 2019;25(1):126. doi:10.3201/eid2501.180534. PMCID: PMC6302604.
  • Ludden C, Raven KE, Jamrozy D, Gouliouris T, Blane B, Coll F, de Goffau M, Naydenova P, Horner C, Hernandez-Garcia J. et al. One health genomic surveillance of Escherichia coli demonstrates distinct lineages and mobile genetic elements in isolates from humans versus livestock. MBio. 2019 22;10(1):10–128. doi:10.1128/mBio.02693-18. PMCID: PMC6343043.
  • Yamaji R, Friedman CR, Rubin J, Suh J, Thys E, McDermott P, Hung-Fan M, Riley LW, Bradford PA. A population-based surveillance study of shared genotypes of Escherichia coli isolates from retail meat and suspected cases of urinary tract infections. mSphere. 2018 Aug 15;3(4):e00179–18. doi:10.1128/mSphere.00179-18. PMCID: PMC6094058.
  • Ortega-Paredes D, de Janon S, Villavicencio F, Ruales KJ, De La Torre K, Villacís JE, Wagenaar JA, Matheu J, Bravo-Vallejo C, Fernández-Moreira E. et al. Broiler Farms and Carcasses Are an Important Reservoir of Multi-Drug Resistant Escherichia coli in Ecuador. Front Vet Sci. 2020;7:547843. doi:10.3389/fvets.2020.547843. PMCID: PMC7724036.
  • Fuentes‐Castillo D, Esposito F, Cardoso B, Dalazen G, Moura Q, Fuga B, Fontana H, Cerdeira L, Dropa M, Rottmann J. et al. Genomic data reveal international lineages of critical priority Escherichia coli harbouring wide resistome in Andean condors (Vultur gryphus Linnaeus, 1758). Mol Ecol. 2020 May;29(10):1919–1935. doi:10.1111/mec.15455.
  • Martínez-Puchol S, Riveros M, Ruidias K, Granda A, Ruiz-Roldán L, Zapata-Cachay C, Ochoa TJ, Pons MJ, Ruiz J. Dissemination of a multidrug resistant CTX-M-65 producer Salmonella enterica serovar infantis clone between marketed chicken meat and children. Int J Food Microbiol. 2021 Apr 16;344:109109. doi:10.1016/j.ijfoodmicro.2021.109109. PMID: 33677191.
  • Lapierre L, Cornejo J, Zavala S, Galarce N, Sánchez F, Benavides MB, Guzmán M, Sáenz L. Phenotypic and genotypic characterization of virulence factors and susceptibility to antibiotics in salmonella infantis strains isolated from chicken meat: first findings in Chile. Anim (Basel). 2020 Jun 18;10(6):1049. doi:10.3390/ani10061049. PMCID: PMC7341295.
  • Quino W, Hurtado CV, Escalante-Maldonado O, Flores-León D, Mestanza O, Vences-Rosales F, Zamudio ML, Gavilán RG. Multidrogorresistencia de Salmonella infantis en Perú: un estudio mediante secuenciamiento de nueva generación. Rev Peru Med Exp Salud Publica. 2019 Mar 8;36(1):37. doi:10.17843/rpmesp.2019.361.3934.
  • Vallejos-Sánchez K, Tataje-Lavanda L, Villanueva-Pérez D, Bendezú J, Montalván Á, Zimic-Peralta M, Fernández-Sánchez M, Fernández-Díaz M, Putonti C. Whole-genome sequencing of a Salmonella enterica subsp. enterica serovar infantis strain isolated from Broiler Chicken in Peru. Putonti C, editor. Microbiol Resour Announc. 2019 Oct 24;8(43):e00826–19. doi:10.1128/MRA.00826-19.
  • Palma N, Pons MJ, Gomes C, Mateu J, Riveros M, García W, Jacobs J, García C, Ochoa TJ, Ruiz J. Resistance to quinolones, cephalosporins and macrolides in Escherichia coli causing bacteraemia in Peruvian children. J Glob Antimicrob Resist. 2017 Dec;11:28–33. doi:10.1016/j.jgar.2017.06.011. PMID: 28743651.
  • Garcia C, Hinostroza N, Astocondor L, Ochoa T, Jacobs J. For The Salmoiber Cyted Network null. Characterization of ESBL-Producing Salmonella enterica Serovar Infantis Infection in Humans, Lima, Peru. Am J Trop Med Hyg. 2019 Oct;101(4):746–748. doi:10.4269/ajtmh.19-0213. PMCID: PMC6779204.
  • Yang JT, Zhang LJ, Lu Y, Zhang RM, Jiang HX. Genomic insights into global blaCTX-M-55-Positive Escherichia coli epidemiology and transmission characteristics. Microbiol Spectr. 2023 Jun;11(4):e0108923. doi:10.1128/spectrum.01089-23. PMID: 37358409.
  • Rao L, Lv L, Zeng Z, Chen S, He D, Chen X, Wu C, Wang Y, Yang T, Wu P. et al. Increasing prevalence of extended-spectrum cephalosporin-resistant Escherichia coli in food animals and the diversity of CTX-M genotypes during 2003–2012. Vet Microbiol. 2014 Aug;172(3–4):534–541. doi:10.1016/j.vetmic.2014.06.013.
  • Marcia P, Rosario R, John B, Nicomedes V, Jorge A, Juan S, Reynaldo C. Molecular characterization of extended-spectrum β-lactamases in strains of Escherichia coli causing urinary infection in immunocompromised patients. Rev Med La Paz. 2019 Dec;25(2):10–18.
  • Rodríguez-Revuelta MJ, López-Cerero L, Serrano L, Luna-Lagares S, Pascual A, Rodríguez-Baño J. Incidence and risk factors for acquisition of extended-spectrum β-lactamase-producing Enterobacteriaceae in Newborns in Seville, Spain: a prospective cohort study. Int J Antimicrob Agents. 2018 Dec;52(6):835–841. doi:10.1016/j.ijantimicag.2018.09.007. PMID: 30236957.
  • Shimasaki T, Seekatz A, Bassis C, Rhee Y, Yelin RD, Fogg L, Dangana T, Cisneros EC, Weinstein RA, Okamoto K. et al. Centers for disease control and prevention epicenters program. Increased relative abundance of Klebsiella pneumoniae carbapenemase-producing Klebsiella pneumoniae within the gut microbiota is associated with risk of bloodstream infection in long-term acute care hospital patients. Clin Infect Dis. 2019 May 30;68(12):2053–2059. doi:10.1093/cid/ciy796. PMCID: PMC6541703.