Probiotics Prevent Candida Colonization and Invasive Fungal Sepsis in Preterm Neonates: A Systematic Review and Meta-Analysis of Randomized Controlled Trials

Manzoni, 2007, Use of Lactobacillus casei subspecies rhamnosus GG and gastrointestinal colonization by Candida species in preterm neonates, J Pediatr Gastroenterol Nutr, 45, S190, 10.1097/01.mpg.0000302971.06115.15 Dong, 2015, Late-onset neonatal sepsis: recent developments, Arch Dis Child Fetal Neonatal Ed, 100, F257, 10.1136/archdischild-2014-306213 Tsai, 2014, Incidence, clinical characteristics and risk factors for adverse outcome in neonates with late-onset sepsis, Pediatr Infect Dis J, 33, e7, 10.1097/INF.0b013e3182a72ee0 Shane, 2013, Recent developments and current issues in the epidemiology, diagnosis, and management of bacterial and fungal neonatal sepsis, Am J Perinatol, 30, 131, 10.1055/s-0032-1333413 Filioti, 2007, Invasive candidiasis in pediatric intensive care patients: epidemiology, risk factors, management, and outcome, Intensive Care Med, 33, 1272, 10.1007/s00134-007-0672-5 Stoll, 2002, Late-onset sepsis in very low birth weight neonates: the experience of the NICHD Neonatal Research Network, Pediatrics, 110, 285, 10.1542/peds.110.2.285 Tezer, 2012, Invasive fungal infections during the neonatal period: diagnosis, treatment and prophylaxis, Expert Opin Pharmacother, 13, 193, 10.1517/14656566.2012.647685 Spiliopoulou, 2012, Neonatal intensive care unit candidemia: epidemiology, risk factors, outcome, and critical review of published case series, Mycopathologia, 173, 219, 10.1007/s11046-011-9498-3 Ali, 2012, Prevalence of Candida colonization in preterm newborns and VLBW in neonatal intensive care unit: role of maternal colonization as a risk factor in transmission of disease, J Matern Fetal Neonatal Med, 25, 789, 10.3109/14767058.2011.622005 Adams-Chapman, 2013, Neurodevelopmental outcome of extremely low birth weight infants with Candida infection, J Pediatr, 163, 961, 10.1016/j.jpeds.2013.04.034 Cerikçioğlu, 2004, The relationships between candidemia and candidal colonization and virulence factors of the colonizing strains in preterm infants, Turk J Pediatr, 46, 245 Manzoni, 2006, An association between anatomic site of Candida colonization and risk of invasive candidiasis exists also in preterm neonates in neonatal intensive care unit, Diagn Microbiol Infect Dis, 56, 459, 10.1016/j.diagmicrobio.2006.07.008 Vendettuoli, 2008, The role of Candida surveillance cultures for identification of a preterm subpopulation at highest risk for invasive fungal infection, Pediatr Infect Dis J, 27, 1114, 10.1097/INF.0b013e31817fce78 Singhi, 2008, Candida colonization and candidemia in a pediatric intensive care unit, Pediatr Crit Care Med, 9, 91, 10.1097/01.PCC.0000298643.48547.83 Saiman, 2001, Risk factors for Candida species colonization of neonatal intensive care unit patients, Pediatr Infect Dis J, 20, 1119, 10.1097/00006454-200112000-00005 Manzoni, 2007, A multicenter, randomized trial of prophylactic fluconazole in preterm neonates, N Engl J Med, 356, 2483, 10.1056/NEJMoa065733 Manzoni, 2012, Clinical characteristics and response to prophylactic fluconazole of preterm VLBW neonates with baseline and acquired fungal colonisation in NICU: data from a multicentre RCT, Early Hum Dev, 88, S60, 10.1016/S0378-3782(12)70017-8 Kaufman, 2005, Twice weekly fluconazole prophylaxis for prevention of invasive Candida infection in high-risk infants of <1000 grams birth weight, J Pediatr, 147, 172, 10.1016/j.jpeds.2005.03.036 Kaufman, 2001, Fluconazole prophylaxis against fungal colonization and infection in preterm infants, N Engl J Med, 345, 1660, 10.1056/NEJMoa010494 Sims, 1988, Prophylactic oral nystatin and fungal infections in very-low-birthweight infants, Am J Perinatol, 5, 33, 10.1055/s-2007-999649 Ganesan, 2009, Prophylactic oral nystatin for preterm babies under 33 weeks' gestation decreases fungal colonisation and invasive fungaemia, Arch Dis Child Fetal Neonatal Ed, 94, F275, 10.1136/adc.2008.145359 Joint FAO-WHO Working Group Report on Drafting Guidelines for the Evaluation of Probiotics in Food. Guidelines for the evaluation of probiotics in food: report of a Joint FAO/WHO working group on drafting guidelines for the evaluation of probiotics in food, London, Ontario, Canada, April 30 and May 1, 2002. Available at ftp://ftp.fao.org/es/esn/food/wgreport2.pdf. [Accessed September 17, 2016]. Villena, 2011, Immunomodulatory and protective effect of probiotic Lactobacillus casei against Candida albicans infection in malnourished mice, Microbiol Immunol, 55, 434, 10.1111/j.1348-0421.2011.00334.x Samonis, 2011, Saccharomyces boulardii and Candida albicans experimental colonization of the murine gut, Med Mycol, 49, 395, 10.3109/13693786.2010.533203 Matsubara, 2012, Treatment with probiotics in experimental oral colonization by Candida albicans in murine model (DBA/2), Oral Dis, 18, 260, 10.1111/j.1601-0825.2011.01868.x Ishijima, 2012, Effect of Streptococcus salivarius K12 on the in vitro growth of Candida albicans and its protective effect in an oral candidiasis model, Appl Environ Microbiol, 78, 2190, 10.1128/AEM.07055-11 Liberati, 2009, The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration, Ann Intern Med, 151, W65, 10.7326/0003-4819-151-4-200908180-00136 Higgins, 2011 Higgins, 2011, The Cochrane Collaboration's tool for assessing risk of bias in randomised trials, BMJ, 343, d5928, 10.1136/bmj.d5928 Higgins, 2003, Measuring inconsistency in meta-analyses, BMJ, 327, 557, 10.1136/bmj.327.7414.557 Begg, 1994, Operating characteristics of a rank correlation test for publication bias, Biometrics, 50, 1088, 10.2307/2533446 Egger, 1997, Bias in meta-analysis detected by a simple, graphical test, BMJ, 315, 629, 10.1136/bmj.315.7109.629 Kumar, 2013, Evaluation of efficacy of probiotics in prevention of Candida colonization in a PICU–a randomized controlled trial, Crit Care Med, 41, 565, 10.1097/CCM.0b013e31826a409c Manzoni, 2012, Bovine lactoferrin prevents invasive fungal infections in very low birth weight infants: a randomized controlled trial, Pediatrics, 129, 116, 10.1542/peds.2011-0279 Manzoni, 2009, Bovine lactoferrin supplementation for prevention of late-onset sepsis in very low-birth-weight neonates: a randomized trial, JAMA, 302, 1421, 10.1001/jama.2009.1403 Al-Hosni, 2012, Probiotics-supplemented feeding in extremely low-birth-weight infants, J Perinatol, 32, 253, 10.1038/jp.2011.51 Manzoni, 2006, Oral supplementation with Lactobacillus casei subspecies rhamnosus prevents enteric colonization by Candida species in preterm neonates: a randomized study, Clin Infect Dis, 42, 1735, 10.1086/504324 Oncel, 2014, Lactobacillus reuteri for the prevention of necrotising enterocolitis in very low birthweight infants: a randomised controlled trial, Arch Dis Child Fetal Neonatal Ed, 99, F110, 10.1136/archdischild-2013-304745 Romeo, 2011, Role of probiotics in the prevention of the enteric colonization by Candida in preterm newborns: incidence of late-onset sepsis and neurological outcome, J Perinatol, 31, 63, 10.1038/jp.2010.57 Roy, 2014, 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, N Am J Med Sci, 6, 50, 10.4103/1947-2714.125870 Sari, 2011, Oral probiotics: Lactobacillus sporogenes for prevention of necrotizing enterocolitis in very low-birth weight infants: a randomized, controlled trial, Eur J Clin Nutr, 65, 434, 10.1038/ejcn.2010.278 Hikaru, 2010, Bifidobacteria prevents preterm infants from developing infection and sepsis, Int J Probiotics Prebiotics, 5, 33 Wagner, 1997, Biotherapeutic effects of probiotic bacteria on candidiasis in immunodeficient mice, Infect Immun, 65, 4165, 10.1128/IAI.65.10.4165-4172.1997 Wagner, 2000, Probiotic effects of feeding heat-killed Lactobacillus acidophilus and Lactobacillus casei to Candida albicans-colonized immunodeficient mice, J Food Prot, 63, 638, 10.4315/0362-028X-63.5.638 Oncel, 2015, Comparison of Lactobacillus reuteri and nystatin prophylaxis on Candida colonization and infection in very low birth weight infants, J Matern Fetal Neonatal Med, 28, 1790, 10.3109/14767058.2014.968842 Demirel, 2013, Prophylactic Saccharomyces boulardii versus nystatin for the prevention of fungal colonization and invasive fungal infection in premature infants, Eur J Pediatr, 172, 1321, 10.1007/s00431-013-2041-4 Murina, 2014, Can Lactobacillus fermentum LF10 and Lactobacillus acidophilus LA02 in a slow-release vaginal product be useful for prevention of recurrent vulvovaginal candidiasis?: a clinical study, J Clin Gastroenterol, 48, S102, 10.1097/MCG.0000000000000225 Martinez, 2009, Improved treatment of vulvovaginal candidiasis with fluconazole plus probiotic Lactobacillus rhamnosus GR-1 and Lactobacillus reuteri RC-14, Lett Appl Microbiol, 48, 269, 10.1111/j.1472-765X.2008.02477.x Ehrström, 2010, Lactic acid bacteria colonization and clinical outcome after probiotic supplementation in conventionally treated bacterial vaginosis and vulvovaginal candidiasis, Microbes Infect, 12, 691, 10.1016/j.micinf.2010.04.010 Campeotto, 2011, A fermented formula in preterm infants: clinical tolerance, gut microbiota, down-regulation of faecal calprotectin and up-regulation of faecal secretory IgA, Br J Nutr, 105, 1843, 10.1017/S0007114510005702 Grönlund, 2000, Importance of intestinal colonisation in the maturation of humoral immunity in early infancy: a prospective follow up study of healthy infants aged 0–6 months, Arch Dis Child Fetal Neonatal Ed, 83, F186, 10.1136/fn.83.3.F186 Ahrne, 2011, Effect of lactobacilli on paracellular permeability in the gut, Nutrients, 3, 104, 10.3390/nu3010104 Hardy, 2013, Probiotics, prebiotics and immunomodulation of gut mucosal defences: homeostasis and immunopathology, Nutrients, 5, 1869, 10.3390/nu5061869 Frei, 2015, Prebiotics, probiotics, synbiotics, and the immune system: experimental data and clinical evidence, Curr Opin Gastroenterol, 31, 153, 10.1097/MOG.0000000000000151 Zhang, 2016, Probiotics for preventing late-onset sepsis in preterm neonates: a PRISMA-compliant systematic review and meta-analysis of randomized controlled trials, Medicine (Baltimore), 95, e2581, 10.1097/MD.0000000000002581 AlFaleh, 2014, Probiotics for prevention of necrotizing enterocolitis in preterm infants, Cochrane Database Syst Rev, CD005496 Wheeler, 2016, Use of probiotics to prevent ventilator-associated pneumonia: a survey of pharmacists' attitudes, J Crit Care, 31, 221, 10.1016/j.jcrc.2015.10.016