Filling the Gaps: Current Research Directions for a Rational Use of Probiotics in Preterm Infants
Abstract
:1. Introduction
2. Defining the Target: Gut Microbiota vs. Clinical Outcomes
3. Exploring Feeding Contribution: Human Milk vs. Formula
4. Choosing the Probiotic: Is There Strength in (Strain) Numbers?
5. Addressing Safety Concerns: Time for Ghost Probiotics?
6. Choosing the Study Design: The Challenge of Cross-Colonization
7. Conclusions
Author Contributions
Conflicts of Interest
References
- Harrison, M.S.; Goldenberg, R.L. Global burden of prematurity. Semin. Fetal Neonatal Med. 2016, 21, 74–79. [Google Scholar] [CrossRef] [PubMed]
- Platt, M.J. Outcomes in preterm infants. Public Health 2014, 128, 399–403. [Google Scholar] [CrossRef] [PubMed]
- Schüller, S.S.; Kramer, B.W.; Villamor, E.; Spittler, A.; Berger, A.; Levy, O. Immunomodulation to prevent or treat neonatal sepsis: Past, present, and future. Front. Pediatr. 2018, 6, 1–17. [Google Scholar] [CrossRef] [PubMed]
- Dermyshi, E.; Wang, Y.; Yan, C.; Hong, W.; Qiu, G.; Gong, X.; Zhang, T. The “Golden Age” of probiotics: A systematic review and meta-analysis of randomized and observational studies in preterm infants. Neonatology 2017, 112, 9–23. [Google Scholar] [CrossRef] [PubMed]
- AlFaleh, K.; Anabrees, J. Probiotics for prevention of necrotizing enterocolitis in preterm infants. Cochrane Database Syst. Rev. 2014, 4, CD005496. [Google Scholar]
- Aceti, A.; Gori, D.; Barone, G.; Callegari, M.L.M.L.; Di Mauro, A.; Fantini, M.P.M.P.; Indrio, F.; Maggio, L.; Meneghin, F.; Morelli, L.; et al. Probiotics for prevention of necrotizing enterocolitis in preterm infants: Systematic review and meta-analysis. Ital. J. Pediatr. 2015, 41, 89. [Google Scholar] [CrossRef] [PubMed]
- Van den Akker, C.H.P.; van Goudoever, J.B.; Szajewska, H.; Embleton, N.D.; Hojsak, I.; Reid, D.; Shamir, R. Probiotics for preterm infants: A strain-specific systematic review and network meta-analysis. J. Pediatr. Gastroenterol. Nutr. 2018, 67, 103–122. [Google Scholar] [CrossRef] [PubMed]
- Rao, S.C.; Athalye-jape, G.K.; Deshpande, G.C.; Simmer, K.N.; Patole, S.K. Probiotic supplementation and late-onset sepsis in preterm infants: A meta-analysis. Pediatrics 2016, 137, 1–16. [Google Scholar] [CrossRef] [PubMed]
- Aceti, A.; Maggio, L.; Beghetti, I.; Gori, D.; Barone, G.; Callegari, M.L.; Fantini, M.P.; Indrio, F.; Meneghin, F.; Morelli, L.; et al. Probiotics prevent late-onset sepsis in human milk-fed, very low birth weight preterm infants: Systematic review and meta-analysis. Nutrients 2017, 9, 904. [Google Scholar] [CrossRef] [PubMed]
- Athalye-Jape, G.; Deshpande, G.; Rao, S.; Patole, S. Benefits of probiotics on enteral nutrition in preterm neonates: A systematic review. Am. J. Clin. Nutr. 2014, 100, 1508–1519. [Google Scholar] [CrossRef] [PubMed]
- Aceti, A.; Gori, D.; Barone, G.; Callegari, M.L.; Fantini, M.P.; Indrio, F.; Maggio, L.; Meneghin, F.; Morelli, L.; Zuccotti, G.; et al. Probiotics and time to achieve full enteral feeding in human milk-fed and formula-fed preterm infants: Systematic review and meta-analysis. Nutrients 2016, 8, 471. [Google Scholar] [CrossRef] [PubMed]
- Deshpande, G.; Jape, G.; Rao, S.; Patole, S. Benefits of probiotics in preterm neonates in low-income and medium-income countries: A systematic review of randomised controlled trials. BMJ Open 2017, 7, e017638. [Google Scholar] [CrossRef] [PubMed]
- Sun, J.; Marwah, G.; Westgarth, M.; Buys, N.; Ellwood, D.; Gray, P.H. Effects of probiotics on necrotizing enterocolitis, sepsis, intraventricular hemorrhage, mortality, length of hospital stay, and weight gain in very preterm infants: A meta-analysis. Adv. Nutr. Int. Rev. J. 2017, 8, 749–763. [Google Scholar] [CrossRef] [PubMed]
- Chang, H.Y.; Chen, J.H.; Chang, J.H.; Lin, H.C.; Lin, C.Y.; Peng, C.C. Multiple strains probiotics appear to be the most effective probiotics in the prevention of necrotizing enterocolitis and mortality: An updated meta-analysis. PLoS ONE 2017, 12, e0171579. [Google Scholar] [CrossRef] [PubMed]
- Cohen, P.A. Probiotic safety-No guarantees. JAMA Intern. Med. 2018. [Google Scholar] [CrossRef] [PubMed]
- Viswanathan, S.; Lau, C.; Akbari, H.; Hoyen, C.; Walsh, M.C. Survey and evidence based review of probiotics used in very low birth weight preterm infants within the United States. J. Perinatol. 2016, 36, 1106–1111. [Google Scholar] [CrossRef] [PubMed]
- Patel, R.M.; Underwood, M.A. Probiotics and necrotizing enterocolitis. Semin. Pediatr. Surg. 2018, 27, 39–46. [Google Scholar] [CrossRef] [PubMed]
- Iozzo, P.; Sanguinetti, E. Early dietary patterns and microbiota development: Still a way to go from descriptive interactions to health-relevant solutions. Front. Nutr. 2018, 5, 5. [Google Scholar] [CrossRef] [PubMed]
- Sanders, M.E.; Guarner, F.; Guerrant, R.; Holt, P.R.; Quigley, E.M.M.; Sartor, R.B.; Sherman, P.M.; Mayer, E. An update on the use and investigation of probiotics in health and disease. Gut 2013, 62, 787–796. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Koletzko, B.; Brands, B.; Grote, V.; Kirchberg, F.F.; Prell, C.; Rzehak, P.; Uhl, O.; Weber, M. Long-term health impact of early nutrition: The power of programming. Ann. Nutr. Metab. 2017, 70, 161–169. [Google Scholar] [CrossRef] [PubMed]
- Schneider, N.; Garcia-Rodenas, C.L. Early nutritional interventions for brain and cognitive development in preterm infants: A review of the literature. Nutrients 2017, 9, 187. [Google Scholar] [CrossRef] [PubMed]
- American Academy of Pediatrics. Breastfeeding and the use of human milk. Pediatrics 2012, 129, e827–e841. [Google Scholar] [CrossRef] [PubMed]
- Chong, C.; Bloomfield, F.; O’Sullivan, J. Factors affecting gastrointestinal microbiome development in neonates. Nutrients 2018, 10, 274. [Google Scholar] [CrossRef] [PubMed]
- De la Cruz, D.; Bazacliu, C. Enteral feeding composition and necrotizing enterocolitis. Semin. Fetal Neonatal Med. 2018. [Google Scholar] [CrossRef]
- Maffei, D.; Schanler, R.J. Human milk is the feeding strategy to prevent necrotizing enterocolitis! Semin. Perinatol. 2017, 41, 36–40. [Google Scholar] [CrossRef] [PubMed]
- Biagi, E.; Quercia, S.; Aceti, A.; Beghetti, I.; Rampelli, S.; Turroni, S.; Faldella, G.; Candela, M.; Brigidi, P.; Corvaglia, L. The bacterial ecosystem of mother’s milk and infant’s mouth and gut. Front. Microbiol. 2017, 8, 1214. [Google Scholar] [CrossRef] [PubMed]
- Zimmermann, P.; Curtis, N. Factors Influencing the intestinal microbiome during the first year of life. Pediatr. Infect. Dis. J. 2018. [Google Scholar] [CrossRef] [PubMed]
- Xu, W.; Judge, M.; Maas, K.; Hussain, N.; McGrath, J.M.; Henderson, W.A.; Cong, X. Systematic review of the effect of enteral feeding on gut microbiota in preterm infants. J. Obstet. Gynecol. Neonatal Nurs. 2017, 47, 451–463. [Google Scholar] [CrossRef] [PubMed]
- Repa, A.; Thanhaeuser, M.; Endress, D.; Weber, M.; Kreissl, A.; Binder, C.; Berger, A.; Haiden, N. Probiotics (Lactobacillus acidophilus and Bifidobacterium bifidum) prevent NEC in VLBW infants fed breast milk but not formula. Pediatr. Res. 2015, 77, 381–388. [Google Scholar] [CrossRef] [PubMed]
- Thomas, J.P.; Raine, T.; Reddy, S.; Belteki, G. Probiotics for the prevention of necrotising enterocolitis in very low-birth-weight infants: A meta-analysis and systematic review. Acta Paediatr. 2017, 106, 1729–1741. [Google Scholar] [CrossRef] [PubMed]
- Embleton, N.D.; Zalewski, S.; Berrington, J.E. Probiotics for prevention of necrotizing enterocolitis and sepsis in preterm infants. Curr. Opin. Infect. Dis. 2016, 29, 256–261. [Google Scholar] [CrossRef] [PubMed]
- Autran, C.A.; Kellman, B.P.; Kim, J.H.; Asztalos, E.; Blood, A.B.; Spence, E.C.H.; Patel, A.L.; Hou, J.; Lewis, N.E.; Bode, L. Human milk oligosaccharide composition predicts risk of necrotising enterocolitis in preterm infants. Gut 2018, 67, 1064–1070. [Google Scholar] [CrossRef] [PubMed]
- Kantorowska, A.; Wei, J.C.; Cohen, R.S.; Lawrence, R.A.; Gould, J.B.; Lee, H.C. Impact of Donor Milk Availability on Breast Milk Use and Necrotizing Enterocolitis Rates. Pediatrics 2016, 137, e20153123. [Google Scholar] [CrossRef] [PubMed]
- Sharpe, J.; Way, M.; Koorts, P.J.; Davies, M.W. The availability of probiotics and donor human milk is associated with improved survival in very preterm infants. World J. Pediatr. 2018. [Google Scholar] [CrossRef] [PubMed]
- O’Connor, D.L.; Gibbins, S.; Kiss, A.; Bando, N.; Brennan-Donnan, J.; Ng, E.; Campbell, D.M.; Vaz, S.; Fusch, C.; Asztalos, E.; et al. Effect of supplemental donor human milk compared with preterm formula on neurodevelopment of very low-birth-weight infants at 18 months: A randomized clinical trial. JAMA 2016, 316, 1897–1905. [Google Scholar] [CrossRef] [PubMed]
- Peila, C.; Moro, G.E.; Bertino, E.; Cavallarin, L.; Giribaldi, M.; Giuliani, F.; Cresi, F.; Coscia, A. The effect of holder pasteurization on nutrients and biologically-active components in donor human milk: A review. Nutrients 2016, 8, 477. [Google Scholar] [CrossRef] [PubMed]
- Parra-Llorca, A.; Gormaz, M.; Alcántara, C.; Cernada, M.; Nuñez-Ramiro, A.; Vento, M.; Collado, M.C. Preterm gut microbiome depending on feeding type: Significance of donor human milk. Front. Microbiol. 2018, 9, 1376. [Google Scholar] [CrossRef] [PubMed]
- Guarner, F.; Malagelada, J.R. Gut flora in health and disease. Lancet 2003, 361, 512–519. [Google Scholar] [CrossRef]
- Zhang, G.-Q.; Hu, H.-J.; Liu, C.-Y.; Shakya, S.; Li, Z.-Y. Probiotics for preventing late-onset sepsis in preterm neonates: A PRISMA-compliant systematic review and meta-analysis of randomized controlled trials. Medicine 2016, 95, e2581. [Google Scholar] [CrossRef] [PubMed]
- Athalye-Jape, G.; Rao, S.; Simmer, K.; Patole, S. Bifidobacterium breve M-16V as a probiotic for preterm infants: A strain-specific systematic review. J. Parenter. Enter. Nutr. 2018, 42, 677–688. [Google Scholar] [CrossRef] [PubMed]
- Athalye-Jape, G.; Rao, S.; Patole, S. Lactobacillus reuteri DSM 17938 as a probiotic for preterm neonates: A strain-specific systematic review. J. Parenter. Enter. Nutr. 2016, 40, 783–794. [Google Scholar] [CrossRef] [PubMed]
- Hu, H.J.; Zhang, G.Q.; Zhang, Q.; Shakya, S.; Li, Z.Y. Probiotics prevent candida colonization and invasive fungal sepsis in preterm neonates: A systematic review and meta-analysis of randomized controlled trials. Pediatr. Neonatol. 2017, 58, 103–110. [Google Scholar] [CrossRef] [PubMed]
- Ganguli, K.; Walker, W.A. Probiotics in the prevention of necrotizing enterocolitis. J. Clin. Gastroenterol. 2011, 45, 133–138. [Google Scholar] [CrossRef] [PubMed]
- Hill, C.; Sanders, M.E. Rethinking “probiotics”. Gut Microbes 2013, 4, 269–270. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hill, C.; Guarner, F.; Reid, G.; Gibson, G.R.; Merenstein, D.J.; Pot, B.; Morelli, L.; Canani, R.B.; Flint, H.J.; Salminen, S.; et al. Expert consensus document: The international scientific association for probiotics and prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat. Rev. Gastroenterol. Hepatol. 2014, 11, 506–514. [Google Scholar] [CrossRef] [PubMed]
- Patole, S. Probiotics for preterm infants-The story searching for an end. Indian Pediatr. 2017, 54, 361–362. [Google Scholar] [CrossRef] [PubMed]
- Underwood, M.A. Impact of probiotics on necrotizing enterocolitis. Semin. Perinatol. 2017, 41, 41–51. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sanders, M.E.; Benson, A.; Lebeer, S.; Merenstein, D.J.; Klaenhammer, T.R. Shared mechanisms among probiotic taxa: Implications for general probiotic claims. Curr. Opin. Biotechnol. 2018, 49, 207–216. [Google Scholar] [CrossRef] [PubMed]
- Timmerman, H.M.; Koning, C.J.M.; Mulder, L.; Rombouts, F.M.; Beynen, A.C. Monostrain, multistrain and multispecies probiotics-A comparison of functionality and efficacy. Int. J. Food Microbiol. 2004, 96, 219–233. [Google Scholar] [CrossRef] [PubMed]
- Ouwehand, A.C.; Invernici, M.M.; Furlaneto, F.A.C.; Messora, M.R. Effectiveness of multistrain versus single-strain probiotics current status and recommendations for the future. J. Clin. Gastroenterol. 2018. [Google Scholar] [CrossRef] [PubMed]
- Deshpande, G.C.; Rao, S.C.; Keil, A.D.; Patole, S.K. Evidence-based guidelines for use of probiotics in preterm neonates. BMC Med. 2011, 9, 92. [Google Scholar] [CrossRef] [PubMed]
- Wong, A.; Saint Ngu, D.Y.; Dan, L.A.; Ooi, A.; Lim, R.L.H. Detection of antibiotic resistance in probiotics of dietary supplements. Nutr. J. 2015, 14, 95. [Google Scholar] [CrossRef] [PubMed]
- Zheng, M.; Zhang, R.; Tian, X.; Zhou, X.; Pan, X.; Wong, A. Assessing the risk of probiotic dietary supplements in the context of antibiotic resistance. Front. Microbiol. 2017, 8, 1–8. [Google Scholar] [CrossRef] [PubMed]
- Taverniti, V.; Guglielmetti, S. The immunomodulatory properties of probiotic microorganisms beyond their viability (ghost probiotics: Proposal of paraprobiotic concept). Genes Nutr. 2011, 6, 261–274. [Google Scholar] [CrossRef] [PubMed]
- Adams, C.A. The probiotic paradox: Live and dead cells are biological response modifiers. Nutr. Res. Rev. 2010, 23, 37–46. [Google Scholar] [CrossRef] [PubMed]
- Lahtinen, S.J. Probiotic viability-does it matter? Microb. Ecol. Heal. Dis. 2012, 23, 10–14. [Google Scholar] [CrossRef] [PubMed]
- Lahtinen, S.J.; Gueimonde, M.; Ouwehand, A.C.; Reinikainen, J.P.; Salminen, S.J. Probiotic bacteria may become dormant during storage. Appl. Environ. Microbiol. 2005, 71, 1662–1663. [Google Scholar] [CrossRef] [PubMed]
- Zorzela, L.; Ardestani, S.K.; McFarland, L.V.; Vohra, S. Is there a role for modified probiotics as beneficial microbes: A systematic review of the literature. Benef. Microbes 2017, 8, 739–754. [Google Scholar] [CrossRef] [PubMed]
- Deshpande, G.; Athalye-Jape, G.; Patole, S. Para-probiotics for preterm neonates-The next frontier. Nutrients 2018, 10, 871. [Google Scholar] [CrossRef] [PubMed]
- Millar, M.R.; Bacon, C.; Smith, S.L.; Walker, V.; Hall, M.A. Enteral feeding of premature infants with Lactobacillus GG. Arch. Dis. Child. 1993, 69, 483–487. [Google Scholar] [CrossRef] [PubMed]
- Kitajima, H.; Sumida, Y.; Tanaka, R.; Yuki, N.; Takayama, H.; Fujimura, M. Early administration of Bifidobacterium breve to preterm infants: Randomised controlled trial. Arch. Dis. Child. Fetal Neonatal Ed. 1997, 76, F101–F107. [Google Scholar] [CrossRef] [PubMed]
- Hickey, L.; Garland, S.M.; Jacobs, S.E.; O’Donnell, C.P.F.; Tabrizi, S.N. Cross-colonization of infants with probiotic organisms in a neonatal unit. J. Hosp. Infect. 2014, 88, 226–229. [Google Scholar] [CrossRef] [PubMed]
- Jacobs, S.E.; Tobin, J.M.; Opie, G.F.; Donath, S.; Tabrizi, S.N.; Pirotta, M.; Morley, C.J.; Garland, S.M. Probiotic Effects on Late-onset Sepsis in Very Preterm Infants: A Randomized Controlled Trial. Pediatrics 2013, 132, 1055–1062. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Costeloe, K.; Hardy, P.; Juszczak, E.; Wilks, M.; Millar, M.R. Bifidobacterium breve BBG-001 in very preterm infants: A randomised controlled phase 3 trial. Lancet 2016, 387, 649–660. [Google Scholar] [CrossRef]
- Deshpande, G.; Rao, S.; Athalye-Jape, G.; Conway, P.; Patole, S. Probiotics in very preterm infants: The PiPS trial. Lancet 2016, 388, 655. [Google Scholar] [CrossRef]
- Karthikeyan, G.; Bhat, B.V. The PiPS (Probiotics in Preterm Infants Study) trial-controlling the confounding factor of crosscontamination unveils significant benefits. Indian Pediatr. 2017, 54, 162. [Google Scholar] [PubMed]
- Meadow, J.F.; Altrichter, A.E.; Bateman, A.C.; Stenson, J.; Brown, G.; Green, J.L.; Bohannan, B.J.M. Humans differ in their personal microbial cloud. PeerJ 2015, 3, e1258. [Google Scholar] [CrossRef] [PubMed]
- Totsu, S.; Yamasaki, C.; Terahara, M.; Uchiyama, A.; Kusuda, S. Bifidobacterium and enteral feeding in preterm infants: Cluster-randomized trial. Pediatr. Int. 2014, 56, 714–719. [Google Scholar] [CrossRef] [PubMed] [Green Version]
© 2018 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Aceti, A.; Beghetti, I.; Maggio, L.; Martini, S.; Faldella, G.; Corvaglia, L. Filling the Gaps: Current Research Directions for a Rational Use of Probiotics in Preterm Infants. Nutrients 2018, 10, 1472. https://doi.org/10.3390/nu10101472
Aceti A, Beghetti I, Maggio L, Martini S, Faldella G, Corvaglia L. Filling the Gaps: Current Research Directions for a Rational Use of Probiotics in Preterm Infants. Nutrients. 2018; 10(10):1472. https://doi.org/10.3390/nu10101472
Chicago/Turabian StyleAceti, Arianna, Isadora Beghetti, Luca Maggio, Silvia Martini, Giacomo Faldella, and Luigi Corvaglia. 2018. "Filling the Gaps: Current Research Directions for a Rational Use of Probiotics in Preterm Infants" Nutrients 10, no. 10: 1472. https://doi.org/10.3390/nu10101472