2,494
Views
1
CrossRef citations to date
0
Altmetric
Research Paper

Cholestasis impairs gut microbiota development and bile salt hydrolase activity in preterm neonates

, , , , , , & ORCID Icon show all
Article: 2183690 | Received 28 Sep 2022, Accepted 16 Feb 2023, Published online: 26 Feb 2023

References

  • Walani SR. Global burden of preterm birth. Int J Gynecol Obstet. 2020;150(1):31–18. doi:10.1002/ijgo.13195.
  • Purisch SE, Gyamfi-Bannerman C. Epidemiology of preterm birth. Semin Perinatol. 2017;41(7):387–391. doi:10.1053/j.semperi.2017.07.009.
  • Neu J. Gastrointestinal development and meeting the nutritional needs of premature infants. Am J Clin Nutr. 2007;85(2):629S–634S. doi:10.1093/ajcn/85.2.629S.
  • 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.
  • Nastasio S, Maggiore G. Cholestasis in preterm infants: when is a yellow alert?. Ital J Pediatr. 2014;40(S2). A12, 1824-7288-40-S2–A12. doi:10.1186/1824-7288-40-S2-A12.
  • Gotze T, Blessing H, Grillhosl C, Gerner P, Hoerning A. 2015. Neonatal cholestasis – differential diagnoses, current diagnostic procedures, and treatment. Front Pediatr [Internet]. [accessed 2022 Apr 25]. doi:10.3389/fped.2015.00043
  • Satrom K, Gourley G. Cholestasis in preterm infants. Clin Perinatol. 2016;43(2):355–373. doi:10.1016/j.clp.2016.01.012.
  • Christensen RD, Henry E, Wiedmeier SE, Burnett J, Lambert DK. Identifying patients, on the first day of life, at high-risk of developing parenteral nutrition-associated liver disease. J Perinatol. 2007;27(5):284–290. doi:10.1038/sj.jp.7211686.
  • Feldman AG, Sokol RJ. Recent developments in diagnostics and treatment of neonatal cholestasis. Semin Pediatr Surg. 2020;29(4):150945. doi:10.1016/j.sempedsurg.2020.150945.
  • de Aguiar Vallim Tq, Tarling EJ, Edwards PA. Pleiotropic roles of bile acids in metabolism. Cell Metab. 2013;17(5):657–669. doi:10.1016/j.cmet.2013.03.013.
  • Hofmann AF. The continuing importance of bile acids in liver and intestinal disease. Arch Intern Med. 1999;159(22):2647. doi:10.1001/archinte.159.22.2647.
  • Guo C, Li Y, Wang P, Li Y, Qiu C, Li M, Wang D, Zhao R, Li D, Wang Y, et al. Alterations of gut microbiota in cholestatic infants and their correlation with hepatic function. Front Microbiol. 2018;9:2682. doi:10.3389/fmicb.2018.02682.
  • Ridlon JM, Harris SC, Bhowmik S, Kang D-J, Hylemon PB. Consequences of bile salt biotransformations by intestinal bacteria. Gut Microbes. 2016;7(1):22–39. doi:10.1080/19490976.2015.1127483.
  • Chand D, Avinash VS, Yadav Y, Pundle AV, Suresh CG, Ramasamy S. Molecular features of bile salt hydrolases and relevance in human health. Biochim Biophys Acta (BBA) - Gen Sub. 2017;1861(1):2981–2991. doi:10.1016/j.bbagen.2016.09.024.
  • Younge NE, Newgard CB, Cotten CM, Goldberg RN, Muehlbauer MJ, Bain JR, Stevens RD, O’connell TM, Rawls JF, Seed PC, et al. Disrupted maturation of the microbiota and metabolome among extremely preterm infants with postnatal growth failure. Sci Rep. 2019;9(1):8167. doi:10.1038/s41598-019-44547-y.
  • Grier A, Qiu X, Bandyopadhyay S, Holden-Wiltse J, Kessler HA, Gill AL, Hamilton B, Huyck H, Misra S, Mariani TJ, et al. Impact of prematurity and nutrition on the developing gut microbiome and preterm infant growth. Microbiome. 2017;5(1):158. doi:10.1186/s40168-017-0377-0.
  • La Rosa PS, Warner BB, Zhou Y, Weinstock GM, Sodergren E, Hall-Moore CM, Stevens HJ, Bennett WE, Shaikh N, Linneman LA, et al. Patterned progression of bacterial populations in the premature infant gut. Proc Natl Acad Sci U S A. 2014;111(34):12522–12527. doi:10.1073/pnas.1409497111.
  • 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.
  • Ttb H, Groer MW, Kane B, Yee AL, Torres BA, Gilbert JA, Maheshwari A. Dichotomous development of the gut microbiome in preterm infants. Microbiome. 2018;6(1):157. doi:10.1186/s40168-018-0547-8.
  • Gopal-Srivastava R, Hyelemon PB. Purification and characterization of bile salt hydrolase from Clostridium perfringens. J Lipid Res. 1988;29(8):1079–1085. doi:10.1016/S0022-2275(20)38464-9.
  • Coleman JP, Hudson LL. Cloning and characterization of a conjugated bile acid hydrolase gene from Clostridium perfringens. Appl Environ Microbiol. 1995;61(7):2514–2520. doi:10.1128/aem.61.7.2514-2520.1995.
  • Setchell KD, Lawson AM, Tanida N, Sjövall J. General methods for the analysis of metabolic profiles of bile acids and related compounds in feces. J Lipid Res. 1983;24(8):1085–1100. doi:10.1016/S0022-2275(20)37923-2.
  • Nakagawa M, Setchell KD. Bile acid metabolism in early life: studies of amniotic fluid. J Lipid Res. 1990;31(6):1089–1098. doi:10.1016/S0022-2275(20)42749-X.
  • Colombo C, Zuliani G, Ronchi M, Breidenstein J, Setchel KDR. Biliary bile acid composition of the human fetus in early gestation. Pediatr Res. 1987;21(2):197–200. doi:10.1203/00006450-198702000-00017.
  • Lester R, St Pyrek J, Little JM, Adcock EW. Diversity of bile acids in the fetus and newborn infant. J Pediatr Gastroenterol Nutr. 1983;2(2):355–364. doi:10.1097/00005176-198305000-00026.
  • Niijima S-I. Studies on the conjugating activity of bile acids in children. Pediatr Res. 1985;19(3):302–307. doi:10.1203/00006450-198503000-00010.
  • Jönsson G, Midtvedt A-C, Norman A, Midtvedt T. Intestinal microbial bile acid transformation in healthy infants. J Pediatr Gastroenterol Nutr. 1995;20(4):394–402. doi:10.1097/00005176-199505000-00004.
  • Crosignani A, Setchell KD, Invernizzi P, Larghi A, Rodrigues CM, Podda M. Clinical pharmacokinetics of therapeutic bile acids. Clin Pharmacokinet. 1996;30(5):333–358. doi:10.2165/00003088-199630050-00002.
  • Setchell KDR, Heubi JE, Shah S, Lavine JE, Suskind D, Al-Edreesi M, Potter C, Russell DW, O’connell NC, Wolfe B, et al. Genetic defects in bile acid conjugation cause fat-soluble vitamin deficiency. Gastroenterology. 2013;144(5):945-955.e6; quiz e14–15. doi:10.1053/j.gastro.2013.02.004.
  • Setchel KDR, Kritchevsky D, Nair P. The bile acids, methods, and applications. New York: Plenum Press; 1988.
  • Chernikova DA, Madan JC, Housman ML, Zain-Ul-Abideen M, Lundgren SN, Morrison HG, Sogin ML, Williams SM, Moore JH, Karagas MR, et al. The premature infant gut microbiome during the first 6 weeks of life differs based on gestational maturity at birth. Pediatr Res. 2018;84(1):71–79. doi:10.1038/s41390-018-0022-z.
  • Saturio S, Nogacka AM, Suárez M, Fernández N, Mantecón L, Mancabelli L, Milani C, Ventura M, de Los Reyes-Gavilán CG, Solís G, et al. Early-life development of the bifidobacterial community in the infant gut. IJMS. 2021;22(7):3382. doi:10.3390/ijms22073382.
  • 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.
  • Ferraris L, Butel MJ, Campeotto F, Vodovar M, Rozé JC, Aires J. Clostridia in premature neonates’ gut: incidence, antibiotic susceptibility, and perinatal determinants influencing colonization. Forestier C, editor. Plos One. 2012;7(1):e30594. doi:10.1371/journal.pone.0030594.
  • van Best N, Rolle-Kampczyk U, Schaap FG, Basic M, Olde Damink SWM, Bleich A, Savelkoul PHM, von Bergen M, Penders J, Hornef MW. Bile acids drive the newborn’s gut microbiota maturation. Nat Commun. 2020;11(1):3692. doi:10.1038/s41467-020-17183-8.
  • Tanaka M, Sanefuji M, Morokuma S, Yoden M, Momoda R, Sonomoto K, Ogawa M, Kato K, Nakayama J. The association between gut microbiota development and maturation of intestinal bile acid metabolism in the first 3 y of healthy Japanese infants. Gut Microbes. 2020;11(2):205–216. doi:10.1080/19490976.2019.1650997.
  • Kiu R, Hall LJ. An update on the human and animal enteric pathogen Clostridium perfringens. Emerg Microbes Infect. 2018;7(1):1–15. doi:10.1038/s41426-018-0144-8.
  • Kiu R, Sim K, Shaw A, Cornwell E, Pickard D, Kroll JS, Hall LJ. Genomic analysis of clostridium perfringens BEC/CPILE-positive, toxinotype D and E strains isolated from healthy children. Toxins. 2019;11(9):543. doi:10.3390/toxins11090543.
  • Nagpal R, Ogata K, Tsuji H, Matsuda K, Takahashi T, Nomoto K, Suzuki Y, Kawashima K, Nagata S, Yamashiro Y. Sensitive quantification of Clostridium perfringens in human feces by quantitative real-time PCR targeting alpha-toxin and enterotoxin genes. BMC Microbiol. 2015;15(1):219. doi:10.1186/s12866-015-0561-y.
  • Kiu R, Shaw A, Sim K, Bedwell H, Cornwell E, Pickard D, Belteki G, Malsom J, Philips S, Young GR, et al. 2021. Dissemination and pathogenesis of toxigenic Clostridium perfringens strains linked to neonatal intensive care units and Necrotising Enterocolitis [Internet]. [place unknown]. Microbiology. [accessed 2022 Jun 22]. doi:10.1101/2021.08.03.454877
  • Zöhrer E, Resch B, Scharnagl H, Schlagenhauf A, Fauler G, Stojakovic T, Hofer N, Lang U, Jahnel J. Serum bile acids in term and preterm neonates: a case–control study determining reference values and the influence of early-onset sepsis. Medicine. 2016;95(44):e5219. doi:10.1097/MD.0000000000005219.
  • Setchell KD, Dumaswala R, Colombo C, Ronchi M. Hepatic bile acid metabolism during early development revealed from the analysis of human fetal gallbladder bile. J Biol Chem. 1988;263(32):16637–16644. doi:10.1016/S0021-9258(18)37438-6.
  • Russell DW, Setchell KDR. Bile acid biosynthesis. Biochemistry. 1992;31(20):4737–4749. doi:10.1021/bi00135a001.
  • Bremmelgaard A, Sjövall J. Bile acid profiles in urine of patients with liver diseases. Eur J Clin Invest. 1979;9(5):341–348. doi:10.1111/j.1365-2362.1979.tb00894.x.
  • Degirolamo C, Rainaldi S, Bovenga F, Murzilli S, Moschetta A. Microbiota modification with probiotics induces hepatic bile acid synthesis via downregulation of the Fxr-Fgf15 axis in mice. Cell Rep. 2014;7(1):12–18. doi:10.1016/j.celrep.2014.02.032.
  • Hou G, Peng W, Wei L, Li R, Yuan Y, Huang X, Yin Y. Lactobacillus delbrueckii interfere with bile acid enterohepatic circulation to regulate cholesterol metabolism of growing–finishing pigs via its bile salt hydrolase activity. Front Nutr. 2020; 7:617676. doi:10.3389/fnut.2020.617676.
  • Begley M, Hill C, Gahan CGM. Bile salt hydrolase activity in probiotics. Appl Environ Microbiol. 2006;72(3):1729–1738. doi:10.1128/AEM.72.3.1729-1738.2006.
  • Liu Y, Chen K, Li F, Gu Z, Liu Q, He L, Shao T, Song Q, Zhu F, Zhang L, et al. Probiotic Lactobacillus rhamnosus GG prevents liver fibrosis through inhibiting hepatic bile acid synthesis and enhancing bile acid excretion in mice. Hepatology. 2020;71(6):2050–2066. doi:10.1002/hep.30975.
  • Chen Q, Li Q, Cao M, Yan J, Zhang X. Hierarchy-assembled dual probiotics system ameliorates cholestatic drug-induced liver injury via gut-liver axis modulation. Adv Sci. 2022;9(17):2200986. doi:10.1002/advs.202200986.
  • Tanner SM, Berryhill TF, Ellenburg JL, Jilling T, Cleveland DS, Lorenz RG, Martin CA. Pathogenesis of necrotizing enterocolitis. Am J Pathol. 2015;185(1):4–16. doi:10.1016/j.ajpath.2014.08.028.
  • Wang Y, Hoenig JD, Malin KJ, Qamar S, Petrof EO, Sun J, Antonopoulos DA, Chang EB, Claud EC. 16S rRNA gene-based analysis of fecal microbiota from preterm infants with and without necrotizing enterocolitis. Isme J. 2009;3(8):944–954. doi:10.1038/ismej.2009.37.
  • Dahlgren AF, Pan A, Lam V, Gouthro KC, Simpson PM, Salzman NH, Nghiem-Rao TH. Longitudinal changes in the gut microbiome of infants on total parenteral nutrition. Pediatr Res. 2019;86(1):107–114. doi:10.1038/s41390-019-0391-y.
  • Dilger K, Hohenester S, Winkler-Budenhofer U, Bastiaansen BAJ, Schaap FG, Rust C, Beuers U. Effect of ursodeoxycholic acid on bile acid profiles and intestinal detoxification machinery in primary biliary cirrhosis and health. J Hepatol. 2012;57(1):133–140. doi:10.1016/j.jhep.2012.02.014.
  • Lepercq P, Gã©rard P, Bã©guet F, Raibaud P, Grill J-P, Relano P, Cayuela C, Juste C. Epimerization of chenodeoxycholic acid to ursodeoxycholic acid by Clostridium baratii isolated from human feces. FEMS Microbiol Lett. 2004;235(1):65–72. doi:10.1111/j.1574-6968.2004.tb09568.x.
  • Ovadia C, Perdones-Montero A, Fan HM, Mullish BH, McDonald JAK, Papacleovoulou G, Wahlström A, Ståhlman M, Tsakmaki A, Clarke LCD, et al. Ursodeoxycholic acid enriches intestinal bile salt hydrolase-expressing Bacteroidetes in cholestatic pregnancy. Sci Rep. 2020;10(1):3895. doi:10.1038/s41598-020-60821-w.
  • Hofmann AF. Bile acids: the good, the bad, and the ugly. Physiology. 1999;14(1):24–29. doi:10.1152/physiologyonline.1999.14.1.24.
  • Schanler RJ. Outcomes of human milk-fed premature infants. Semin Perinatol. 2011;35(1):29–33. doi:10.1053/j.semperi.2010.10.005.
  • Sisk PM, Lovelady CA, Gruber KJ, Dillard RG, O’shea TM. Human milk consumption and full enteral feeding among infants who weigh ≤1250 grams. Pediatrics. 2008;121(6):e1528–1533. doi:10.1542/peds.2007-2110.
  • Hair AB, Hawthorne KM, Chetta KE, Abrams SA. Human milk feeding supports adequate growth in infants ≤ 1250 grams birth weight. BMC Res Notes. 2013;6(1):459. doi:10.1186/1756-0500-6-459.
  • Ehrenkranz RA, Dusick AM, Vohr BR, Wright LL, Wrage LA, Poole WK. For the national institutes of child health and human development neonatal research network. Growth in the neonatal intensive care unit influences neurodevelopmental and growth outcomes of extremely low birth weight infants. Pediatrics. 2006;117(4):1253–1261. doi:10.1542/peds.2005-1368.
  • Best C, Gourley GR. Management of neonatal cholestasis. Therapy. 2009;6(1):75–81. doi:10.2217/14750708.6.1.75.
  • Moreau GB, Ramakrishnan G, Cook HL, Fox TE, Nayak U, Ma JZ, Colgate ER, Kirkpatrick BD, Haque R, Petri WA. Childhood growth and neurocognition are associated with distinct sets of metabolites. EBioMedicine. 2019.44: 597–606. doi:10.1016/j.ebiom.2019.05.043.
  • Zhao X, Setchell KDR, Huang R, Mallawaarachchi I, Ehsan L, Dobrzykowski IE, Zhao J, Syed S, Ma JZ, Iqbal NT, et al. Bile acid profiling reveals distinct signatures in undernourished children with environmental enteric dysfunction. J Nutr. 2021;151(12):3689–3700. doi:10.1093/jn/nxab321.
  • Ridlon JM, Kang D-J, Hylemon PB. Isolation and characterization of a bile acid inducible 7α-dehydroxylating operon in Clostridium hylemonae TN271. Anaerobe. 2010;16(2):137–146. doi:10.1016/j.anaerobe.2009.05.004.
  • Lee J-Y, Arai H, Nakamura Y, Fukiya S, Wada M, Yokota A. Contribution of the 7β-hydroxysteroid dehydrogenase from Ruminococcus gnavus N53 to ursodeoxycholic acid formation in the human colon. J Lipid Res. 2013;54(11):3062–3069. doi:10.1194/jlr.M039834.
  • Ford SL, Lohmann P, Preidis GA, Gordon PS, O’donnell A, Hagan J, Venkatachalam A, Balderas M, Luna RA, Hair AB. Improved feeding tolerance and growth are linked to increased gut microbial community diversity in very-low-birth-weight infants fed mother’s own milk compared with donor breast milk. Am J Clin Nutr. 2019;109(4):1088–1097. doi:10.1093/ajcn/nqz006.
  • Mirzayi C, Renson A, Standards Consortium G, Analysis M, Control Society Q, Zohra F, Elsafoury S, Geistlinger L, Kasselman LJ, Eckenrode K, et al. Reporting guidelines for human microbiome research: the STORMS checklist. Nat Med. 2021;27(11):1885–1892. doi:10.1038/s41591-021-01552-x.
  • Beghini F, McIver LJ, Blanco-Míguez A, Dubois L, Asnicar F, Maharjan S, Mailyan A, Manghi P, Scholz M, Thomas AM, et al. Integrating taxonomic, functional, and strain-level profiling of diverse microbial communities with bioBakery 3. eLife. 2021;10:e65088. doi:10.7554/eLife.65088.
  • Kanehisa M. KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 2000;28(1):27–30. doi:10.1093/nar/28.1.27.
  • Jose S, Mukherjee A, Horrigan O, Setchell KDR, Zhang W, Moreno-Fernandez ME, Andersen H, Sharma D, Haslam DB, Divanovic S, et al. Obeticholic acid ameliorates severity of Clostridioides difficile infection in high fat diet-induced obese mice. Mucosal Immunol. 2021;14(2):500–510. doi:10.1038/s41385-020-00338-7.
  • Tanaka H, Hashiba H, Kok J, Mierau I. Bile salt hydrolase of bifidobacterium longum —biochemical and genetic characterization. Appl Environ Microbiol. 2000;66(6):2502–2512. doi:10.1128/AEM.66.6.2502-2512.2000.
  • McMurdie PJ, Holmes S. Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. Plos One. 2013;8(4):e61217. doi:10.1371/journal.pone.0061217.
  • Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12(6):R60. doi:10.1186/gb-2011-12-6-r60.
  • Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’hara RB, Simpson GL, Solymos P, et al. Vegan: Community Ecology Package. R package version 2.5-7. 2020. https://CRAN.R-project.org/package=vegan