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Research Paper

Reversible aberrancies in gut microbiome of moderate and late preterm infants: results from a randomized, controlled trial

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Article: 2283913 | Received 15 Jun 2023, Accepted 12 Nov 2023, Published online: 27 Nov 2023

References

  • Lawn JE, Ohuma EO, Bradley E, Idueta LS, Hazel E, Okwaraji YB, Erchick DJ, Yargawa J, Katz J, Lee AC, et al. Small babies, big risks: global estimates of prevalence and mortality for vulnerable newborns to accelerate change and improve counting. Lancet. 2023;401(10389):1707–14. doi:10.1016/S0140-6736(23)00522-6.
  • Underwood MA, Sohn K. The microbiota of the extremely preterm infant. Clin Perinatol. 2017;44(2):407–427. doi:10.1016/j.clp.2017.01.005.
  • Hiltunen H, Hanani H, Luoto R, Turjeman S, Ziv O, Isolauri E, Salminen S, Koren O, Rautava S. Preterm infant meconium microbiota transplant induces growth failure, inflammatory activation, and metabolic disturbances in germ-free mice. Cell Rep Med. 2021;2(11):100447. doi:10.1016/j.xcrm.2021.100447.
  • Sim K, Powell E, Cornwell E, Kroll JS, Shaw AG. Development of the gut microbiota during early life in premature and term infants. Gut Pathog. 2023;15(1):3. doi:10.1186/s13099-022-00529-6.
  • Forsgren M, Isolauri E, Salminen S, Rautava S. Late preterm birth has direct and indirect effects on infant gut microbiota development during the first six months of life. Acta Paediatr. 2017;106(7):1103–1109. doi:10.1111/apa.13837.
  • Zou ZH, Liu D, Li HD, Zhu DP, He Y, Hou T, Yu JL. Prenatal and postnatal antibiotic exposure influences the gut microbiota of preterm infants in neonatal intensive care units. Ann Clin Microbiol Antimicrob. 2018;17(1):9. doi:10.1186/s12941-018-0264-y.
  • Stewart CJ, Ajami NJ, O´brien J, Hutchinson DS, Smith DP, Wong MC, Ross MC, Lloyd RE, Doddapaneni H, Metcalf GA, et al. Temporal development of the gut microbiome in early childhood from the TEDDY study. Nature. 2018;562(7728):583–588. doi:10.1038/s41586-018-0617-x.
  • Tirone C, Pezza A, Paladini A, Tana M, Aurilia C, Lio A, D’Ippolito S, Tersigni C, Posteraro B, Sanguinetti M, et al. Gut and lung microbiota in preterm infants: immunological modulation and implication in neonatal outcomes. Front Immunol. 2019;10:2910. doi:10.3389/fimmu.2019.02910.
  • Aguilar-Lopez M, Dinsmoor AM, Ho TTB, Donovan SM. A systematic review of the factors influencing microbial colonization of the preterm infant gut. Gut Microbes. 2021;13(1):1–33. doi:10.1080/19490976.2021.1884514.
  • Milani C, Duranti S, Bottacini F, Casey E, Turroni F, Mahony J, Belzer C, Delgado Palacio S, Arboleya Montes S, Mancabelli L, et al. The first microbial colonizers of the human gut: composition, activities, and health implications of the infant gut microbiota. Microbiol Mol Biol Rev. 2017;81(4):e00036–17. doi:10.1128/MMBR.00036-17.
  • Xiang Q, Yan X, Shi W, Li H, Zhou K. Early gut microbiota intervention in premature infants: application perspectives. J Adv Res. 2023;51:59–72. doi:10.1016/j.jare.2022.11.004.
  • Butel MJ, Suau A, Campeotto F, Magne F, Aires J, Ferraris L, Kalach N, Leroux B, Dupont C. Conditions of bifidobacterial colonization in preterm infants: a prospective analysis. J Pediatr Gastroenterol Nutr. 2007;44(5):577–582. doi:10.1097/MPG.0b013e3180406b20.
  • Korpela K, Blakstad EW, Moltu SJ, Strømmen K, Nakstad B, Rønnestad AE, Brække K, Iversen PO, Drevon CA, de Vos W. Intestinal microbiota development and gestational age in preterm neonates. Sci Rep. 2018;8(1):2453. doi:10.1038/s41598-018-20827-x.
  • Jia J, Xun P, Wang X, He K, Tang Q, Zhang T, Wang Y, Tang W, Lu L, Yan W, et al. Impact of postnatal antibiotics and parenteral nutrition on the gut microbiota in preterm infants during early life. J Parenter Enter Nutr. 2020;44(4):639–654. doi:10.1002/jpen.1695.
  • Chi C, Fan Y, Li C, Li Y, Guo S, Li T, Buys N, Clifton VL, Colditz PB, Yin C, et al. Early gut microbiota colonisation of premature infants fed with breastmilk or formula with or without probiotics: a cohort study. Nutrients. 2021;13(11):4068. doi:10.3390/nu13114068.
  • Drysdale SB, Lo J, Prendergast M, Alcazar M, Wilson T, Zuckerman M, Smith M, Broughton S, Rafferty GF, Peacock JL, et al. Lung function of preterm infants before and after viral infections. Eur J Pediatr. 2014;173(11):1497–1504. doi:10.1007/s00431-014-2343-1.
  • Haataja P, Korhonen P, Ojala R, Hirvonen M, Paassilta M, Gissler M, Luukkaala T, Tammela O. Asthma and atopic dermatitis in children born moderately and late preterm. Eur J Pediatr. 2016;175(6):799–808. doi:10.1007/s00431-016-2708-8.
  • Crump C, Sundquist J, Sundquist K. Preterm or early term birth and long-term risk of asthma into midadulthood: a national cohort and cosibling study. Thorax. 2023;78(7):653–660. doi:10.1136/thorax-2022-218931.
  • Chawanpaiboon S, Vogel JP, Moller AB, Lumbiganon P, Petzold M, Hogan D, Landoulsi S, Jampathong N, Kongwattanakul K, Laopaiboon M, et al. Global, regional, and national estimates of levels of preterm birth in 2014: a systematic review and modelling analysis. Lancet Glob Health. 2019;7(1):e37–e46. doi:10.1016/S2214-109X(18)30451-0.
  • Jamaluddine Z, Sharara E, Helou V, El Rashidi N, Safadi G, El-Helou N, Ghattas H, Sato M, Blencowe H, Campbell OMR. Effects of size at birth on health, growth and developmental outcomes in children up to age 18: an umbrella review. Arch Dis Child. 2023 Jun 20. archdischild-2022–324884. Online ahead of print. doi:10.1136/archdischild-2022-324884.
  • Harijan P, Boyle EM. Health outcomes in infancy and childhood of moderate and late preterm infants. Semin Fetal Neonatal Med. 2012;17(3):159–162. doi:10.1016/j.siny.2012.02.002.
  • Boyle JD, Boyle EM. Born just a few weeks early: does it matter? Arch Dis Child Fetal Neonatal Ed. 2013;98(1):F85–88. doi:10.1136/archdischild-2011-300535.
  • Natarajan G, Shankaran S. Short- and long-term outcomes of moderate and late preterm infants. Am J Perinatol. 2016;33(3):305–317. doi:10.1055/s-0035-1571150.
  • Sbihi H, Boutin RCT, Cutler C, Suen M, Finlay BB, Turvey SE. Thinking bigger: how early-life environmental exposures shape the gut microbiome and influence the development of asthma and allergic disease. Allergy. 2019;74(11):2103–2115. doi:10.1111/all.13812.
  • Heiss CN, Olofsson LE. The role of the gut microbiota in development, function and disorders of the central nervous system and the enteric nervous system. J Neuroendocrinol. 2019;31(5):12684. doi:10.1111/jne.12684.
  • Cryan JF, O´riordan OJ, Cowan CSM, Sandhu KV, Bastiaanssen TFS, Boehme M, Codagnone MG, Cussotto S, Fulling C, Golubeva AV, et al. The microbiota-gut-brain axis. Physiol Rev. 2019;99(4):1877–2013. doi:10.1152/physrev.00018.2018.
  • Henderickx JGE, Zwittink RD, van Lingen RA, Knol J, Belzer C. The preterm gut microbiota: an inconspicuous challenge in nutritional neonatal care. Front Cell Infect Microbiol. 2019;9:85. doi:10.3389/fcimb.2019.00085.
  • Cuna A, Morowitz MJ, Ahmed I, Umar S, Sampath V. Dynamics of the preterm gut microbiome in health and disease. Am J Physiol Gastrointest Liver Physiol. 2020;320(4):G411–G419. doi:10.1152/ajpgi.00399.2020.
  • Arboleya S, Martinez-Camblor P, Solís G, Suárez M, Fernández N, de Los Reyes-Gavilán CG, Gueimonde M. Intestinal microbiota and weight-gain in preterm neonates. Front Microbiol. 2017;8:183. doi:10.3389/fmicb.2017.00183.
  • Kalliomäki M, Collado MC, Salminen S, Isolauri E. Early differences in fecal microbiota composition in children may predict overweight. Am J Clin Nutr. 2008;87(3):534–538. doi:10.1093/ajcn/87.3.534.
  • Pärtty A, Luoto R, Kalliomäki M, Salminen S, Isolauri E. Effects of early prebiotic and probiotic supplementation on development of gut microbiota and fussing and crying in preterm infants: a randomized, double-blind, placebo-controlled trial. J Pediatr. 2013;163(5):1272–1277.e1–2. doi:10.1016/j.jpeds.2013.05.035.
  • Tojo R, Suarez A, Clemente MG, de Los Reyes-Gavilán CG, Margolles A, Gueimonde M, Ruas-Madiedo P. Intestinal microbiota in health and disease: role of bifidobacteria in gut homeostasis. World J Gastroenterol. 2014;20(14):15163–15176. doi:10.3748/wjg.v20.i41.15163.
  • Stewart CJ, Nelson A, Treumann A, Skeath T, Cummings SP, Embleton ND, Berrington JE. Metabolomic and proteomic analysis of serum from preterm infants with necrotising entercolitis and late-onset sepsis. Pediatr Res. 2016;79(3):425–431. doi:10.1038/pr.2015.235.
  • Ames SR, Lotoski LC, Azad MB. Comparing early life nutritional sources and human milk feeding practices: personalized and dynamic nutrition supports infant gut microbiome development and immune system maturation. Gut Microbes. 2023;15(1):2190305. doi:10.1080/19490976.2023.2190305.
  • Hiltunen H, Collado MC, Ollila H, Kolari T, Tölkkö S, Isolauri E, Salminen S, Rautava S. Spontaneous preterm delivery is reflected in both early neonatal and maternal gut microbiota. Pediatr Res. 2022;91(7):1804–1811. doi:10.1038/s41390-021-01663-8.
  • Koren O, Goodrich JK, Cullender TC, Spor A, Laitinen K, Bäckhed HK, Gonzalez A, Werner JJ, Angenent LT, Knight R, et al. Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell. 2012;150(3):470–480. doi:10.1016/j.cell.2012.07.008.
  • Neu J, Walker WA. Necrotizing enterocolitis. N Engl J Med. 2011;364(3):255–264. doi:10.1056/NEJMra1005408.
  • Ruiz L, Moles L, Gueimonde M, Rodriguez JM. Perinatal microbiomes’ influence on preterm birth and preterms’ health: influencing factors and modulation strategies. J Pediatr Gastroenterol Nutr. 2016;63(6):e193–e203. doi:10.1097/MPG.0000000000001196.
  • Uzan-Yulzari A, Turta O, Belogolovski A, Ziv O, Kunz C, Perschbacher S, Neuman H, Pasolli E, Oz A, Ben-Amram H, et al. Neonatal antibiotic exposure impairs child growth during the first six years of life by perturbing intestinal microbial colonization. Nat Commun. 2021;12(1):443. doi:10.1038/s41467-020-20495-4.
  • Cox LM, Yamanishi S, Sohn J, Alekseyenko AV, Leung JM, Cho I, Kim SG, Li H, Gao Z, Mahana D, et al. Altering the intestinal microbiota during a critical developmental window has lasting metabolic consequences. Cell. 2014;158(4):705–721. doi:10.1016/j.cell.2014.05.052.
  • Hu T, Dong Y, Yang C, Zhao M, He Q. Pathogenesis of children´s allergic diseases: refocusing the role of the gut microbiota. Front Physiol. 2021;12:749544. doi:10.3389/fphys.2021.749544.
  • Yao Y, Cai X, Ye Y, Wang F, Chen F, Zheng C. The role or microbiota in infant health: from early life to adulthood. Front Immunol. 2021;12:708472. doi:10.3389/fimmu.2021.708472.
  • Dotinga BM, Eshuis MS, Bocca-Tjeertes IF, Kerstjens JM, Van Braeckel KN, Reijneveld SA, Bos AF. Longitudinal growth and neuropsychological functioning at age 7 in moderate and late preterms. Pediatrics. 2016;138(4):e20153638. doi:10.1542/peds.2015-3638.
  • De Nardo MC, Mario CD, Laccetta G, Boscarino G, Terrin G. Enteral and parenteral energy intake and neurodevelopment in preterm infants: a systematic review. Nutrition. 2021;97:111572. doi:10.1016/j.nut.2021.111572.
  • De Lucia Rolfe E, de Franga GVA, Vianna CA, Gigante DP, Miranda JJ, Yudkin JS, Horta BL, Ong KK. Associations of stunting in early childhood with cardiometabolic risk factors in adulthood. PLoS ONE. 2018;13(4):e0192196. doi:10.1371/journal.pone.0192196.
  • Kalliomäki M, Salminen S, Arvilommi H, Kero P, Koskinen P, Isolauri E. Probiotics in primary prevention of atopic disease: a randomised placebo-controlled trial. Lancet. 2001;357(9262):1076–1079. doi:10.1016/S0140-6736(00)04259-8.
  • Luoto R, Ruuskanen O, Waris M, Kalliomäki M, Salminen S, Isolauri E. Prebiotic and probiotic supplementation prevents rhinovirus infections in preterm infants: a randomized, placebo-controlled trial. J Allergy Clin Immunol. 2014;133(2):405–413. doi:10.1016/j.jaci.2013.08.020.
  • Faith JJ, Guruge JL, Charbonneau M, Subramanian S, Seedorf H, Goodman AL, Clemente JC, Knight R, Heath AC, Leibel RL, et al. The long-term stability of the human gut microbiota. Sci. 2013;341(6141):1237439. doi:10.1126/science.1237439.
  • Gensollen T, Iyer SS, Kasper DL, Blumberg RS. How colonization by microbiota in early life shapes the immune system. Sci. 2016;352(6285):539–544. doi:10.1126/science.aad9378.
  • Hooper LV, Littman DR, Macpherson AJ. Interaction between the microbiota and immune system. Sci. 2012;336(6086):1268–1273. doi:10.1126/science.1223490.
  • Olszak T, An D, Zeissig S, Vera MP, Richter J, Franke A, Glickman JN, Siebert R, Baron RM, Kasper DL, et al. Microbial exposure during early life has persistent effects on natural killer T cell function. Sci. 2012;336(6080):489–493. doi:10.1126/science.1219328.
  • Gluckman PD, Hanson MA, Cooper C, Thornburg KL. Effect of in utero and early-life conditions on adult health and disease. N Engl J Med. 2008;359(1):61–73. doi:10.1056/NEJMra0708473.
  • Rautava S, Luoto R, Salminen S, Isolauri E. Microbial contact during pregnancy, initial colonization and human disease. Nat Rev Gastroenterol Hepat. 2012;9(10):565–576. doi:10.1038/nrgastro.2012.144.
  • Rautava S, Kainonen E, Salminen S, Isolauri E. Maternal probiotic supplementation during pregnancy and breast-feeding reduces the risk of eczema in the infant. J Allergy Clin Immunol. 2012;130(6):1355–1360. doi:10.1016/j.jaci.2012.09.003.
  • Pasolli E, Asnicar F, Manara S, Zolfo M, Karcher N, Armanini F, Beghini F, Manghi P, Tett A, Ghensi P, et al. Extensive unexplored human microbiome diversity revealed by over 150,000 genomes from metagenomes spanning age, geography, and lifestyle. Cell. 2019;176(3):649–662.e20. doi:10.1016/j.cell.2019.01.001.
  • Nielsen HB, Almeida M, Juncker AS, Rasmussen S, Li J, Sunagawa S, Plichta DR, Gautier L, Pedersen AG, Le Chatelier E, et al. Identification and assembly of genomes and genetic elements in complex metagenomic samples without using reference genomes. Nat Biotechnol. 2014;32(8):822–828. doi:10.1038/nbt.2939.
  • Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 2015;25(7):1043–1055. doi:10.1101/gr.186072.114.
  • Langmead B, Salzberg SL. Fast gapped-read alignment with bowtie 2. Nat Methods. 2012;9(4):357–359. doi:10.1038/nmeth.1923.
  • Schubert M, Lindgreen S, Orlando L. AdapterRemoval v2: rapid adapter trimming, identification, and read merging. BMC Res Notes. 2016;9(1):88. doi:10.1186/s13104-016-1900-2.
  • Li H, Durbin R. Fast and accurate short alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25(14):1754–1760. doi:10.1093/bioinformatics/btp324.
  • Huerta-Cepas J, Forslund K, Coelho LP, Szklarczyk D, Jensen LJ, von Mering C, Bork P. Fast genome-wide functional annotation through orthology assignment by eggNOG-Mapper. Mol Biol Evol. 2017;34(8):2115–2122. doi:10.1093/molbev/msx148.
  • Vieira-Silva S, Falony G, Darzi Y, Lima-Mendez G, Garcia Yunta R, Okuda S, Vandeputte D, Valles-Colomer M, Hildebrand F, Chaffron S, et al. Species-function relationships shape ecological properties of the human gut microbiome. Nature Microbiology. 2016;1(8):16088. doi:10.1038/nmicrobiol.2016.88.