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Factors Influencing Gastrointestinal Tract and Microbiota Immune Interaction in Preterm Infants

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Factors Influencing Gastrointestinal Tract and Microbiota Immune Interaction in Preterm Infants Review nature publishing group Factors influencing gastrointestinal tract and microbiota immune interaction in preterm infants María Carmen Collado1, María Cernada2,3, Josef Neu4, Gaspar Pérez-Martínez1, María Gormaz3 and Máximo Vento2,3 The role of microbial colonization is indispensable for keeping balanced immune response but also have a significant impact a balanced immune response in life. However, the events that on the intestinal mucosal barrier function and intestinal matu- regulate the establishment of the microbiota, their timing, and ration. Furthermore, these disturbances may predispose to the way in which they interact with the host are not yet fully specific diseases later in life. Early host-microbe interactions understood. Factors such as gestational age, mode of delivery, may provide a signal for immune system development and environment, hygienic measures, and diet influence the estab- maturation (2). lishment of microbiota in the perinatal period. Environmental The “Early programming” theory is based upon the fact microbes constitute the most important group of exogenous that environmental exposures including nutritional during stimuli in this critical time frame. However, the settlement of a the perinatal period can induce permanent changes in many stable gut microbiota in preterm infants is delayed compared physiological processes. Postnatal diet mainly breastfeeding to term infants. Preterm infants have an immature gastrointes- practices are therefore critical for the ongoing developmental tinal tract and immune system which predisposes to infectious maturation of many organ systems and optimal physiological morbidity. Neonatal microbial dynamics and alterations in early functions The effects of early programming extend into adult- gut microbiota may precede and/or predispose to diseases hood and are linked to the risk of acquiring specific diseases in such as necrotizing enterocolitis (NEC), late-onset sepsis or adult life (3–5). others. During this critical period, nutrition is the principal con- tributor for immunological and metabolic development, and PREMATURITY AND MICROBIOTA microbiological programming. Breast milk is a known source of In the last decades, mortality of very preterm infants has molecules that act synergistically to protect the gut barrier and been substantially reduced. Improvement in the survival rates enhance the maturation of the gut-related immune response. has been attributed to a series of factors such as regionaliza- Host-microbe interactions in preterm infants and the protec- tion, generalization of antenatal steroids, new modalities of tive role of diet focused on breast milk impact are beginning mechanical ventilation, and the use of surfactant replace- to be unveiled. ment therapy (6). However, this has not always been paral- leled by a simultaneous decrease in morbidity. The prevalence of serious complications such as retinopathy of prematurity, urrent evidence supports the role of microbiota in promot- bronchopulmonary dysplasia, or periventricular leukomala- Cing and maintaining a balanced immune response and the cia has remained practically unchanged especially in the very establishment of the gut barrier in the immediate postnatal preterm infants (<32 wk gestation) (7). Of note, mortality as life. The human body harbors a dynamic and complex micro- a consequence of neonatal septicemia has been reported to bial population, which includes around 500–1,000 different be around 18% of all neonatal deaths. Interestingly, ~50% of species. In the perinatal period, neonates are exposed not only these deaths occur in the first week of life, and the remain- to a vast microbial diversity but also to a variety of organisms ing 50% are nosocomial infections acquired during prolonged such as viruses, fungi and parasites. After weaning, the infant’s hospitalization (8). gut is colonized by a rapidly diversifying microbiota that leads The role of microbiota in preterm birth and the conse- to an adult-like pattern of intestinal flora. The composition of quences of prematurity upon postnatal microbiome develop- the neonatal microbiota is influenced by numerous perinatal ment are emerging fields of discussion. The exact mechanisms factors such as mode of delivery, environment, hygienic mea- responsible for preterm birth are multifactorial and yet not sures, antibiotic treatment, and breastfeeding practices (1). completely unveiled (Table 1). However, the link between Adverse circumstances affecting the establishment of a nor- infection and prematurity has been well established. In addi- mal microbiota may result in failure in the development of a tion to the traditionally accepted ascending infection from the 1Instituto de Agroquímica y Tecnología de Alimentos, Consejo Superior de Investigaciones Científicas (IATA-CSIC), Valencia, Spain; 2Health Research Institute (Instituto de ­Investigación Sanitaria) La Fe, Valencia, Spain; 3Division of Neonatology, University and Polytechnic Hospital, Valencia, Spain; 4Division of Neonatology, Department of ­Pediatrics, University of Florida, Gainesville, Florida. Correspondence: Máximo Vento ([email protected]) Received 2 July 2014; accepted 3 December 2014; advance online publication 1 April 2015. doi:10.1038/pr.2015.54 726 Pediatric ReSearch Volume 77 | Number 6 | June 2015 Copyright © 2015 International Pediatric Research Foundation, Inc. Preterm microbiota Review lower genital tract recent research suggests that other forms of lipopolysaccharides, flagellin, or other Gram-negative sub- bacterial spreading could be responsible for preterm delivery stances may interact with the intestinal Toll-like receptors (9). Interestingly, studies by Madianos et al. (10) and Aargard (TLR) and confer “tolerance” to further inflammatory stimuli et al. (11) have shown resemblances between fetal and neonatal (18). In a recent study, it was shown that early Proteobacteria bacterial colonization and maternal oral cavity and placental colonization might cause an exacerbated immune response, flora strongly suggesting a hematogenous dissemination in the which may impact on the intestinal barrier enhancing ­bacterial perinatal period. translocation and the risk to develop sepsis, necrotizing entero- The interaction of preterm infants’ altered gut microbiota colitis (NEC) and other inflammatory problems (19–21). The with an immature immunologic intestinal response trig- concept of bacterial translocation and gut-originated sepsis gers proinflammatory and counter-inflammatory cytokine and NEC as a cause of systemic infectious complications has response (12). These factors are extremely important for pre- emerged over the last years, although the exact clinical rele- term infants because they influence the pattern of bacterial gut vance of these phenomena continues to be debated (21). colonization, which is different to that in the healthy full-term infant (Figure 1). Briefly, preterm infants showed retarded GASTROINTESTINAL TRACT IMMUNE SYSTEM AND Bifidobacterium- microbiota colonization, a high prevalence of MICROBIOME INTERACTION IN PRETERM INFANTS Staphylococcus, Enterobacteriaceae, Enterococcaceae and other At birth, the adaptive immune system is quite rudimentary lactic acid bacteria as the genus Lactobacillus and Weissella in and untrained. Hence, normal term newborns highly rely on a low-diversity bacterial ecosystem (13–15). In preterm birth a trans-placental passage of mother’s IgG during the last 3 mo of negative correlation with gestational age and a tendency toward gestation for control of pathogens showing a remarkable acti- a higher inflammatory response has been associated with vation of T cells (22,23). Furthermore, the immune response higher presence of Enterobacter, Enterococcus, Lactobacillus, to gut pathogens in term newborn infants still requires protein Photorhabdus, and Tannerella spp. (17). Microbial coloniza- components from mother’s milk to efficiently fulfill TLR bind- tion of meconium and feces of preterm infants analyzed dur- ing and signal transduction (24). Innate immune functions in ing the first months of life using traditional culture-based the fetus are ontologically regulated through gestation; hence, methods and molecular techniques to analyze bacterial diver- developmental events may give rise to differences in the innate sity revealed that Firmicutes was the predominant phylum immune response of the neonate, and particularly in prema- in meconium while Proteobacteria was present in neonatal ture newborns, putting them at high risk of developing severe fecal samples. Interestingly, the Proteobacteria phylum may infections. A high proportion of Th1-polarizing cytokines dur- increase the inflammatory response in the preterm intestine, ing pregnancy has been related to a high probability of abor- and it has been speculated that exposure to low quantities of tion (25). Therefore, in the fetus, expression of Th2 cytokines abIntervention term/preterm Microbiome impact Breastmilk vs. formula Bifidobacterium spp Enterobacteriaceae Vaginal vs. C-section Lactobacillus, Prevotella and Sneathia (maternal vaginal and intestinal microbiota) Staphylococcus, Propionibacterium and Corynebacterium (skin and oral microbiota, environmental bacteria) TERM Delayed bacteroides colonization Proteobacteria and Firmicutes Antibiotic treatment reduced utilization of human milk Enterobacteriaceae (E. coli and Klebsiella spp.) prolonged hospitalization Staphylococcus, Propionibacterium and Corynebacterium PRETERM Bacterial translocation Inflammation Oxidative
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