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. 2023 Jul 26;7(7):CD005496.
doi: 10.1002/14651858.CD005496.pub6.

Probiotics to prevent necrotising enterocolitis in very preterm or very low birth weight infants

Sahar Sharif  1 , Nicholas Meader  1 , Sam J Oddie  1   2 , Maria X Rojas-Reyes  3   4 , William McGuire  1
Affiliations

Probiotics to prevent necrotising enterocolitis in very preterm or very low birth weight infants

Sahar Sharif et al. Cochrane Database Syst Rev. .

Abstract

Background: Intestinal dysbiosis may contribute to the pathogenesis of necrotising enterocolitis (NEC) in very preterm or very low birth weight (VLBW) infants. Dietary supplementation with probiotics to modulate the intestinal microbiome has been proposed as a strategy to reduce the risk of NEC and associated mortality and morbidity in very preterm or VLBW infants.

Objectives: To determine the effect of supplemental probiotics on the risk of NEC and associated mortality and morbidity in very preterm or very low birth weight infants.

Search methods: We searched CENTRAL, MEDLINE, Embase, the Maternity and Infant Care database, and CINAHL from inception to July 2022. We searched clinical trials databases and conference proceedings, and examined the reference lists of retrieved articles.

Selection criteria: We included randomised controlled trials (RCTs) and quasi-RCTs comparing probiotics with placebo or no probiotics in very preterm infants (born before 32 weeks' gestation) and VLBW infants (weighing less than 1500 g at birth).

Data collection and analysis: Two review authors independently evaluated risk of bias of the trials, extracted data, and synthesised effect estimates using risk ratios (RRs), risk differences (RDs), and mean differences (MDs), with associated 95% confidence intervals (CIs). The primary outcomes were NEC and all-cause mortality; secondary outcome measures were late-onset invasive infection (more than 48 hours after birth), duration of hospitalisation from birth, and neurodevelopmental impairment. We used the GRADE approach to assess the certainty of the evidence.

Main results: We included 60 trials with 11,156 infants. Most trials were small (median sample size 145 infants). The main potential sources of bias were unclear reporting of methods for concealing allocation and masking caregivers or investigators in about half of the trials. The formulation of the probiotics varied across trials. The most common preparations contained Bifidobacterium spp., Lactobacillus spp., Saccharomyces spp., andStreptococcus spp., alone or in combination. Very preterm or very low birth weight infants Probiotics may reduce the risk of NEC (RR 0.54, 95% CI 0.46 to 0.65; I² = 17%; 57 trials, 10,918 infants; low certainty). The number needed to treat for an additional beneficial outcome (NNTB) was 33 (95% CI 25 to 50). Probiotics probably reduce mortality slightly (RR 0.77, 95% CI 0.66 to 0.90; I² = 0%; 54 trials, 10,484 infants; moderate certainty); the NNTB was 50 (95% CI 50 to 100). Probiotics probably have little or no effect on the risk of late-onset invasive infection (RR 0.89, 95% CI 0.82 to 0.97; I² = 22%; 49 trials, 9876 infants; moderate certainty). Probiotics may have little or no effect on neurodevelopmental impairment (RR 1.03, 95% CI 0.84 to 1.26; I² = 0%; 5 trials, 1518 infants; low certainty). Extremely preterm or extremely low birth weight infants Few data were available for extremely preterm or extremely low birth weight (ELBW) infants. In this population, probiotics may have little or no effect on NEC (RR 0.92, 95% CI 0.69 to 1.22, I² = 0%; 10 trials, 1836 infants; low certainty), all-cause mortality (RR 0.92, 95% CI 0.72 to 1.18; I² = 0%; 7 trials, 1723 infants; low certainty), or late-onset invasive infection (RR 0.93, 95% CI 0.78 to 1.09; I² = 0%; 7 trials, 1533 infants; low certainty). No trials provided data for measures of neurodevelopmental impairment in extremely preterm or ELBW infants.

Authors' conclusions: Given the low to moderate certainty of evidence for the effects of probiotic supplements on the risk of NEC and associated morbidity and mortality for very preterm or VLBW infants, and particularly for extremely preterm or ELBW infants, there is a need for further large, high-quality trials to provide evidence of sufficient validity and applicability to inform policy and practice.

Trial registration: ClinicalTrials.gov NCT01315821 NCT00977912 NCT01181791 NCT01375309 NCT02552706.

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Conflict of interest statement

SS has no conflicts of interest to declare. NM is Deputy Co‐ordinating Editor for Cochrane Common Mental Disorders but was not involved in the editorial process or decision‐making for this review. SJO has no conflicts of interest to declare. MXRR is an Associate Editor of Cochrane Neonatal but was not involved in the editorial process or decision‐making for this review. WM is a Co‐ordinating Editor of Cochrane Neonatal but was not involved in the editorial process or decision‐making for this review.

Figures

1
1
Study flow diagram: review update 2022.
2
2
Risk of bias summary: review authors' judgements about each risk of bias item for each included study.
3
3
Forest plot of comparison: 1 Probiotics versus placebo or no probiotics, outcome: 1.1 Necrotising enterocolitis.
4
4
Funnel plot of comparison: 1 Probiotics versus placebo or no probiotics, outcome: 1.1 Necrotising enterocolitis.
5
5
Forest plot of comparison: 1 Probiotics versus placebo or no probiotics, outcome: 1.2 Mortality.
6
6
Funnel plot of comparison: 1 Probiotics versus placebo or no probiotics, outcome: 1.2 Mortality.
1.1
1.1. Analysis
Comparison 1: Probiotics versus placebo or no probiotics (very preterm or very low birth weight infants), Outcome 1: Necrotising enterocolitis
1.2
1.2. Analysis
Comparison 1: Probiotics versus placebo or no probiotics (very preterm or very low birth weight infants), Outcome 2: All‐cause mortality
1.3
1.3. Analysis
Comparison 1: Probiotics versus placebo or no probiotics (very preterm or very low birth weight infants), Outcome 3: Late‐onset invasive infection
1.4
1.4. Analysis
Comparison 1: Probiotics versus placebo or no probiotics (very preterm or very low birth weight infants), Outcome 4: Duration of hospitalisation from birth (days)
1.5
1.5. Analysis
Comparison 1: Probiotics versus placebo or no probiotics (very preterm or very low birth weight infants), Outcome 5: Neurodevelopmental impairment
1.6
1.6. Analysis
Comparison 1: Probiotics versus placebo or no probiotics (very preterm or very low birth weight infants), Outcome 6: Cerebral palsy
1.7
1.7. Analysis
Comparison 1: Probiotics versus placebo or no probiotics (very preterm or very low birth weight infants), Outcome 7: Visual impairment
1.8
1.8. Analysis
Comparison 1: Probiotics versus placebo or no probiotics (very preterm or very low birth weight infants), Outcome 8: Hearing impairment
1.9
1.9. Analysis
Comparison 1: Probiotics versus placebo or no probiotics (very preterm or very low birth weight infants), Outcome 9: Cognitive performance
2.1
2.1. Analysis
Comparison 2: Probiotics versus placebo or no probiotics (extremely preterm or extremely low birth weight infants), Outcome 1: Necrotising enterocolitis
2.2
2.2. Analysis
Comparison 2: Probiotics versus placebo or no probiotics (extremely preterm or extremely low birth weight infants), Outcome 2: All‐cause mortality
2.3
2.3. Analysis
Comparison 2: Probiotics versus placebo or no probiotics (extremely preterm or extremely low birth weight infants), Outcome 3: Late‐onset invasive infection
2.4
2.4. Analysis
Comparison 2: Probiotics versus placebo or no probiotics (extremely preterm or extremely low birth weight infants), Outcome 4: Duration of hospitalisation from birth (days)
3.1
3.1. Analysis
Comparison 3: Subgroup analysis by type of feeding, Outcome 1: Necrotising enterocolitis
3.2
3.2. Analysis
Comparison 3: Subgroup analysis by type of feeding, Outcome 2: All‐cause mortality
3.3
3.3. Analysis
Comparison 3: Subgroup analysis by type of feeding, Outcome 3: Late‐onset invasive infection
3.4
3.4. Analysis
Comparison 3: Subgroup analysis by type of feeding, Outcome 4: Duration of hospitalisation from birth (days)
4.1
4.1. Analysis
Comparison 4: Sensitivity analyses: trials at low risk of bias, Outcome 1: Necrotising enterocolitis
4.2
4.2. Analysis
Comparison 4: Sensitivity analyses: trials at low risk of bias, Outcome 2: All‐cause mortality
4.3
4.3. Analysis
Comparison 4: Sensitivity analyses: trials at low risk of bias, Outcome 3: Late‐onset invasive infection
4.4
4.4. Analysis
Comparison 4: Sensitivity analyses: trials at low risk of bias, Outcome 4: Duration of hospitalisation from birth (days)
4.5
4.5. Analysis
Comparison 4: Sensitivity analyses: trials at low risk of bias, Outcome 5: Neurodevelopmental impairment
4.6
4.6. Analysis
Comparison 4: Sensitivity analyses: trials at low risk of bias, Outcome 6: Cerebral palsy
4.7
4.7. Analysis
Comparison 4: Sensitivity analyses: trials at low risk of bias, Outcome 7: Visual impairment
4.8
4.8. Analysis
Comparison 4: Sensitivity analyses: trials at low risk of bias, Outcome 8: Hearing impairment
See this image and copyright information in PMC

Update of

References

References to studies included in this review

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    1. Reuman PD, Duckworth DH, Smith KL, Kagan R, Bucciarelli RL, Ayoub EM. Lack of effect of Lactobacillus on gastrointestinal bacterial colonization in premature infants. Pediatric Infectious Disease 1986;5(6):663-8. [DOI: 10.1097/00006454-198611000-00013] [PMID: ] - DOI - PubMed
Rougé 2009 {published data only}
    1. Rougé C, Piloquet H, Butel MJ, Berger B, Rochat F, Ferraris L, et al. Oral supplementation with probiotics in very low-birth-weight preterm infants: a randomized, double-blind, placebo-controlled trial. American Journal of Clinical Nutrition 2009;89(6):1828-35. [DOI: 10.3945/ajcn.2008.26919] [PMID: ] - DOI - PubMed
Roy 2014 {published data only}
    1. Roy A, Chaudhuri J, Sarkar D, Ghosh P, Chakraborty S. Role of enteric supplementation of probiotics on late-onset sepsis by Candida species in preterm low birth weight neonates: a randomized, double blind, placebo-controlled trial. North American Journal of Medical Sciences 2014;6(1):50-7. [DOI: 10.4103/1947-2714.125870] [PMID: ] - DOI - PMC - PubMed
Sadowska‐Krawczenko 2012 {published data only}
    1. Sadowska-Krawczenko IK, Polak P, Wietlicka-Piszcz A, Szajewska H. Lactobacilllus rhamnosus ATC A07FA for preventing necrotizing enterocolitis in very-low-birth-weight preterm infants: a randomized controlled trial (preliminary results) [Ocena skutecznoci Lactobacillus rhamnosus ATC A07FAw zapobieganiu martwiczego zapalenia jelit wczeniaków z bardzoma urodzeniow mas ciaa: badanie z randomizacj (wstpnewyniki)]. Polish Journal of Pediatrics 2012;87(2):139-45.
Saengtawesin 2014 {published data only}
    1. Saengtawesin V, Tangpolkaiwalsak R, Kanjanapattankul W. Effect of oral probiotics supplementation in the prevention of necrotizing enterocolitis among very low birth weight preterm infants. Journal of the Medical Association of Thailand 2014;97(Suppl 6):S20-5. [PMID: ] - PubMed
Samanta 2009 {published data only}
    1. Samanta M, Sarkar M, Ghosh P, Ghosh JK, Sinha MK, Chatterjee S. Prophylactic probiotics for prevention of necrotizing enterocolitis in very low birth weight newborns. Journal of Tropical Pediatrics 2009;55(2):128-31. [DOI: 10.1093/tropej/fmn091] [PMID: ] - DOI - PubMed
Sari 2011 {published data only}
    1. Sari FN, Dizdar EA, Oguz S, Erdeve O, Uras N, Dilmen U. Oral probiotics: Lactobacillus sporogenes for prevention of necrotizing enterocolitis in very low-birth weight infants: a randomized, controlled trial. European Journal of Clinical Nutrition 2011;65(4):434-9. [DOI: 10.1038/ejcn.2010.278] [PMID: ] - DOI - PubMed
    1. Sari FN, Eras Z, Dizdar EA, Erdeve O, Oguz SS, Uras N, et al. Do oral probiotics affect growth and neurodevelopmental outcomes in very low-birth-weight preterm infants? American Journal of Perinatology 2012;29(8):579-86. [DOI: 10.1055/s-0032-1311981] [PMID: ] - DOI - PubMed
Serce 2013 {published data only}
    1. Serce O, Benzer D, Gursoy T, Karatekin G, Ovali F. Efficacy of saccharomyces boulardii on necrotizing enterocolitis or sepsis in very low birth weight infants: a randomised controlled trial. Early Human Development 2013;89(12):1033-6. [DOI: 10.1016/j.earlhumdev.2013.08.013] [PMID: ] - DOI - PubMed
    1. Serce O, Gursoy T, Ovali F, Karatekin G. Effects of Saccharomyces boulardii on neonatal hyperbilirubinemia: a randomized controlled trial. American Journal of Perinatology 2015;30(2):137-42. [DOI: 10.1055/s-0034-1376390] [PMID: ] - DOI - PubMed
Shadkam 2015 {published data only}
    1. Shadkam MN, Jalalizadeh F, Nasiriani K. Effects of probiotic lactobacillus reuteri (DSM 17938) on the incidence of necrotizing enterocolitis in very low birth weight premature infants. Iranian Journal of Neonatology 2015;6(4):15-20. [DOI: 10.22038/IJN.2015.6143] - DOI
Shashidhar 2017 {published data only}
    1. Shashidhar A, Suman Rao PN, Nesargi S, Bhat S, Chandrakala BS. Probiotics for promoting feed tolerance in very low birth weight neonates – a randomized controlled trial. Indian Pediatrics 2017;54(5):363-7. [DOI: 10.1007/s13312-017-1106-2] [PMID: ] - DOI - PubMed
Sowden 2022 {published data only}
    1. Sowden M, Weissenbruch MM, Bulabula AN, Wyk L, Twisk J, Niekerk E. Effect of a multi-strain probiotic on the incidence and severity of necrotizing enterocolitis and feeding intolerances in preterm neonates. Nutrients 2022;14(16):3305. [DOI: 10.3390/nu14163305] [PMID: ] - DOI - PMC - PubMed
Stratiki 2007 {published data only}
    1. Stratiki Z, Costalos C, Sevastiadou S, Kastanidou O, Skouroliakou M, Giakoumatou A, et al. The effect of a bifidobacteria supplemented bovine milk on intestinal permeability of preterm infants. Early Human Development 2007;83(9):575-9. [DOI: 10.1016/j.earlhumdev.2006.12.002] [PMID: ] - DOI - PubMed
Strus 2018 {published data only}
    1. Strus M, Helwich E, Lauterbach R, Rzepecka-Węglarz B, Nowicka K, Wilińska M, et al. Effects of oral probiotic supplementation on gut Lactobacillus and Bifidobacterium populations and the clinical status of low-birth-weight preterm neonates: a multicenter randomized, double-blind, placebo-controlled trial. Infection and Drug Resistance 2018;11:1557-71. [DOI: 10.2147/IDR.S166348] [PMID: ] - DOI - PMC - PubMed
Tewari 2015 {published data only}
    1. Tewari VV, Dubey SK, Gupta G. Bacillus clausii for prevention of late-onset sepsis in preterm infants: a randomized controlled trial. Journal of Tropical Pediatrics 2015;61(5):377-85. [DOI: 10.1093/tropej/fmv050] [PMID: ] - DOI - PubMed
Totsu 2014 {published data only}
    1. Totsu S, Terahara M, Kusuda S. Probiotics and the development of very low birthweight infants: follow-up study of a randomised trial. BMJ Paediatrics Open 2018;2(1):e000256. [DOI: 10.1136/bmjpo-2018-000256] [PMID: ] - DOI - PMC - PubMed
    1. Totsu S, Yamasaki C, Terahara M, Uchiyama A, Kusuda S, Probiotics Study Group in Japan. Bifidobacterium and enteral feeding in preterm infants: cluster-randomized trial. Pediatrics International 2014;56(5):714-9. [DOI: 10.1111/ped.12330] [PMID: ] - DOI - PMC - PubMed
Van Niekerk 2014 {published data only}
    1. Van Niekerk E, Kirsten GF, Nel DG, Blaauw R. Probiotics, feeding tolerance, and growth: a comparison between HIV-exposed and unexposed very low birth weight infants. Nutrition 2014;30(6):645-53. [DOI: 10.1016/j.nut.2013.10.024] [PMID: ] - DOI - PubMed
Wang 2007 {published data only}
    1. Wang C, Shoji H, Sato H, Nagata S, Ohtsuka Y, Shimizu T, et al. Effects of oral administration of bifidobacterium breve on fecal lactic acid and short-chain fatty acids in low birth weight infants. Journal of Pediatric Gastroenterology and Nutrition 2007;44(2):252-7. [DOI: 10.1097/01.mpg.0000252184.89922.5f] [PMID: ] - DOI - PubMed
Wejryd 2019 {published data only}
    1. Wejryd E, Marchini G, Frimmel V, Jonsson B, Abrahamsson T. Probiotics promoted head growth in extremely low birthweight infants in a double-blind placebo-controlled trial. Acta Paediatrica 2019;108(1):62-9. [DOI: 10.1111/apa.14497] [PMID: ] - DOI - PubMed
Zeber‐Lubecka 2016 {published data only}
    1. Zeber-Lubecka N, Kulecka M, Ambrozkiewicz F, Paziewska A, Lechowicz M, Konopka E, et al. Effect of Saccharomyces boulardii and mode of delivery on the early development of the gut microbial community in preterm infants. PLOS One 2016;11(2):e0150306. [DOI: 10.1371/journal.pone.0150306] [PMID: ] - DOI - PMC - PubMed

References to studies excluded from this review

Ahmed 2022 {published data only}
    1. Ahmed N, Siddique T, Aftab M, Ashfaq Ahmed K, Mateen A, Bibi R. Effectiveness of oral probiotics in prevention of necrotizing enterocolitis in preterm infants. Journal of Pharmaceutical Research International 2022;34:1-5. [DOI: 10.9734/jpri/2022/v34i41A36268] - DOI
Arora 2017 {published data only}
    1. Arora S, Khurana MS, Saini R. To study the role of probiotics in the prevention of necrotizing enterocolitis in preterm neonates. International Journal of Contemporary Pediatrics 2017;4(5):6. [DOI: 10.18203/2349-3291.ijcp20173787] - DOI
Awad 2010 {published data only}
    1. Awad H, Mokhtar H, Imam SS, Gad GI, Hafez H, Aboushady N. Comparison between killed and living probiotic usage versus placebo for the prevention of necrotizing enterocolitis and sepsis in neonates. Pakistan Journal of Biological Sciences 2010;13(6):253-62. [DOI: 10.3923/pjbs.2010.253.262] [PMID: ] - DOI - PubMed
Chi 2019 {published data only}
    1. Chi C, Xue Y, Liu R, Wang Y, Lv N, Zeng H, et al. Effects of a formula with a probiotic Bifidobacterium lactis supplement on the gut microbiota of low birth weight infants. European Journal of Nutrition 2019;59(4):1493-503. [DOI: 10.1007/s00394-019-02006-4] [PMID: ] - DOI - PubMed
Dasopoulou 2015 {published data only}
    1. Dasopoulou M, Briana DD, Boutsikou T, Karakasidou E, Roma E, Costalos C, et al. Motilin and gastrin secretion and lipid profile in preterm neonates following prebiotics supplementation: a double-blind randomized controlled study. Journal of Parenteral and Enteral Nutrition 2015;39(3):359-68. [DOI: 10.1177/0148607113510182] [PMID: ] - DOI - PubMed
Deng 2010 {published data only}
    1. Deng J, Chen K. Early minimal feeding combined with probiotics to prevent necrotizing enterocolitis in preterm infant. Chinese Journal of Modern Drug Application 2010;4(6):13-4.
Denkel 2016 {published data only}
    1. Denkel LA, Schwab F, Garten L, Geffers C, Gastmeier P, Piening B. Protective effect of dual-strain probiotics in preterm infants: a multi-center time series analysis. PLOS One 2016;11(6):e0158136. [DOI: 10.1371/journal.pone.0158136] [PMID: ] - DOI - PMC - PubMed
Di 2010 {published data only}
    1. Di M, Li X. Effects of Bifidobacterium supplementation for prevention of necrotizing enterocolitis in preterm infants: a randomized, controlled trial. Zhong Guo She Qu Yi Shi 2010;231:69. [CENTRAL: CN-00921248]
Dongol‐Singh 2017 {published data only}
    1. Dongol Singh S, Klobassa DS, Resch B, Urlesberger B, Shrestha RP. Placebo controlled introduction of prophylactic supplementation of probiotics to decrease the incidence of necrotizing enterocolitis at Dhulikhel Hospital in Nepal. Kathmandu University Medical Journal 2017;15(60):319-23. [PMID: ] - PubMed
Hua 2014 {published data only}
    1. Hua X-T, Tang J, Mu D-Z. Effect of oral administration of probiotics on intestinal colonization with drug resistant bacteria in preterm infants [口服益生菌对早产儿肠道耐药菌定植的影响]. Chinese Journal of Contemporary Pediatrics 2014;16(6):606-9. [PMID: ] - PubMed
Hussain 2016 {published data only}
    1. Hussain M, Jabeen S, Subhani RU. Role of probiotics in prevention of necrotizing enterocolitis in preterm low birth weight neonates. Pakistan Journal of Medicine and Health Sciences 2016;10:455-9.
Ke 2008 {published data only}
    1. Ke D, Su Z, Li L. Effects of Bifido supplement for prevention of necrotizing enterocolitis in preterm infants: a randomized controlled trial. Chinese Pediatric Emergency Medicine 2008;12:69-71.
Koksal 2015 {published data only}
    1. Köksal N, Varal İ, Özkan H, Bagcı O, Doğan P. Effect of probiotic support on feeding intolerance and mortality at preterm infants. In: Journal of Perinatal Medicine. Vol. 43. 2015:P-0612.
Moles 2015 {published data only}
    1. Moles L, Escribano E, De Andres J, Montes MT, Rodriguez JM, Jimenez E, et al. Administration of Bifidobacterium breve PS12929 and Lactobacillus salivarius PS12934, two strains isolated from human milk, to very low and extremely low birth weight preterm infants: A pilot study. Journal of Immunology Research 2015;2015:538171. [DOI: 10.1155/2015/538171] [PMID: ] - DOI - PMC - PubMed
Partty 2013 {published data only}
    1. Partty A, Luoto R, Kalliomaki 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. Journal of Pediatrics 2013;163(5):1272-7. [DOI: 10.1016/j.jpeds.2013.05.035] [PMID: ] - DOI - PubMed
Qiao 2017 {published data only}
    1. Qiao LX, Zhu WY, Zhang HY, Wang H. Effect of early administration of probiotics on gut microflora and feeding in pre-term infants: a randomised controlled trial. Journal of Maternal-Fetal & Neonatal Medicine 2017;30(1):13-6. [DOI: 10.3109/14767058.2016.1163674] [PMID: ] - DOI - PubMed
Rojas 2012 {published data only}
    1. Rojas MA, Lozano JM, Rojas MX, Rodriguez VA, Rondon MA, Bastidas JA, et al. Prophylactic probiotics to prevent death and nosocomial infection in preterm infants. Pediatrics 2012;130(5):e1113-20. [DOI: 10.1542/peds.2011-3584] [PMID: ] - DOI - PubMed
Romeo 2011 {published data only}
    1. Romeo MG, Romeo DM, Trovato L, Oliveri S, Palermo F, Cota F, et al. Role of probiotics in the prevention of the enteric colonization by Candida in preterm newborns: incidence of late-onset sepsis and neurological outcome. Journal of Perinatology 2011;31(1):63-9. [DOI: 10.1038/jp.2010.57] [PMID: ] - DOI - PMC - PubMed
Shujie 2011 {published data only}
    1. Shujie Y, Haiying Y, Bin G, Shu X, Xianglan D, Jiang W. The clinical application value of endangered preterm infants given earlier amounts of micro feedings and adding probiotics. Journal of Pediatric Pharmacy 2011;17:21-4.
Sinha 2015 {published data only}
    1. Sinha A, Gupta SS, Chellani H, Maliye C, Kumari V, Arya S, et al. Role of probiotics VSL#3 in prevention of suspected sepsis in low birthweight infants in India: a randomised controlled trial. BMJ Open 2015;5(7):e006564. [DOI: 10.1136/bmjopen-2014-006564] [PMID: ] - DOI - PMC - PubMed
Thanhaeuser 2014 {published data only}
    1. Thanhaeuser M, Repa A, Weber M, Endress D, Kreissl A, Binder C, et al. Probiotics (infloran) for NEC prevention: influence of enteral nutrition. In: Archives of Disease in Childhood. 5th Congress of the European Academy of Paediatric Societies, EAPS 2014, Barcelona, Spain. Vol. 99. 2014:A176-7.
Uhlemann 1999 {published data only}
    1. Uhlemann M, Heine W, Mohr C, Plath C, Pap S. Effects of oral administration of bifidobacteria on intestinal microflora in premature and newborn infants. Zeitschrift fur Geburtshilfe und Neonatologie 1999;203(5):213-7. [PMID: ] - PubMed
Underwood 2014 {published data only}
    1. Underwood MA, Kalanetra KM, Bokulich NA, Mirmiran M, Barile D, Tancredi DJ, et al. Prebiotic oligosaccharides in premature infants. Journal of Pediatric Gastroenterology and Nutrition 2014;58(3):352-60. [DOI: 10.1097/MPG.0000000000000211] [PMID: ] - DOI - PubMed
Xu 2016 {published data only}
    1. Xu L, Wang Y, Wang Y, Fu J, Sun M, Mao Z, et al. A double-blinded randomized trial on growth and feeding tolerance with Saccharomyces boulardii CNCMI-745 in formula-fed preterm infants. Jornal de Pediatria 2016;92(3):296-301. [DOI: 10.1016/j.jped.2015.08.013] [PMID: ] - DOI - PubMed
Zhou 2012 {published data only}
    1. Zhou N. The observation of effect of probiotics in the prevention of neonatal necrotizing enterocolitis. Chinese Journal of Ethnomedicine and Ethnopharmacy 2012;21:81.
Zhuang 2007 {published data only}
    1. Zhuang X-Y, Li X-Y, Gao X-X, Su L-D. Relative factors of neonatal necrotizing enterocolitis and preventive effect of microeco-preparation. Journal of Applied Clinical Pediatrics 2006;22:1392-3.

References to studies awaiting assessment

Coleta 2013 {published data only}
    1. Coleta E, Gheonea M, Sarbu M. Oral supplementation with probiotics in premature infants – a randomised clinical trial. In: Intensive Care Medicine. 24th Annual Meeting of the European Society of Paediatric and Neonatal Intensive Care edition. Vol. 39. Rotterdam, Netherlands, 2013:S113.
Kaban 2019 {published data only}
    1. Kaban RK, Hegar B, Rohsiswatmo R, Handryastuti S, Amelia N, Muktiarti D, et al. Lactobacillus reuteri DSM 17938 improves feeding intolerance in preterm infants. Pediatric Gastroenterology, Hepatology & Nutrition 2019;22(6):545-53. [DOI: 10.5223/pghn.2019.22.6.545] [PMID: ] - DOI - PMC - PubMed
Niazi 2021 {published data only}
    1. Niazi S, Saeed F, Tariq S, Farooq MA, Khan S, Akhter SF. Efficacy of probiotics to prevent necrotizing enterocolitis in low birth weight preterm neonates. The Professional Medical Journal 2021;28(3):328-32. [DOI: 10.29309/TPMJ/2021.28.03.5786] - DOI
Punnahitananda 2006 {unpublished data only}ISRCTN39142169
    1. Punnahitananda S, Thaithumyanon P, Soongsawang K. Nosocomial infection and necrotizing enterocolitis in preterm neonates treated with Lactobacillus acidophilus and Bifidobacterium infantis in a neonatal intensive care unit: a randomized controlled study. In: 14th Congress of the Federation of Asia Oceania Perinatal Societies. Bangkok, Thailand, 2006.
Reznikov 2022 {published data only (unpublished sought but not used)}
    1. Reznikov E, Pippa M, Pak J, Riley R, Panigrahi P, Rubin L. Probiotic supplementation in very low birthweight infants: effects on systemic immunity and intestinal inflammation. Current Developments in Nutrition 2022;6(Suppl 1):706. [DOI: 10.1093/cdn/nzac061.090] - DOI

References to ongoing studies

Marißen 2019 {published data only}
    1. Marißen J, Haiß A, Meyer C, Van Rossum T, Bünte LM, Frommhold D, et al, PRIMAL consortium. Efficacy of Bifidobacterium longum, B. infantis and Lactobacillus acidophilus probiotics to prevent gut dysbiosis in preterm infants of 28+0-32+6 weeks of gestation: a randomised, placebo-controlled, double-blind, multicentre trial: the PRIMAL Clinical Study protocol. BMJ Open 2019;9(11):e032617. [DOI: 10.1136/bmjopen-2019-032617] [PMID: ] - DOI - PMC - PubMed
NCT00977912 {unpublished data only}
    1. NCT00977912. Necrotizing enterocolitis (Nec) and B. Lactis in premature babies [Prevention of NEC in preterm Infants with B. lactis]. clinicaltrials.gov/ct2/show/NCT00977912 (first received 16 September 2009).
NCT01181791 {unpublished data only}
    1. NCT01181791. Effects of Lactobacillus reuteri in premature infants (reuteri) [Pilot study to evaluate the effects of Lactobacillus reuteri in preterm newborns]. clinicaltrials.gov/ct2/show/NCT01181791 (first received 13 August 2010).
NCT01375309 {unpublished data only}
    1. NCT01375309. Bifidobacterium supplementation for very low birth weight infants (Bifido(RCT)) [Effect of bifidobacterium bifidum supplementation on morbidity of very low birth weight infants]. clinicaltrials.gov/ct2/show/NCT01375309 (first received 17 June 2011).
NCT04541771 {published data only}
    1. NCT04541771. The role of Lactobacillus reuteri in preventing necrotizing enterocolitis (NEC) in pre-term infants (NEC) [The role of Lactobacillus reuteri (L. reuteri) in preventing necrotizing enterocolitis (NEC) in pre-term infants less than 34 weeks of gestation]. clinicaltrials.gov/ct2/show/NCT04541771 (first received 9 September 2020).

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