The immune consequences of preterm birth

Jacqueline M Melville, Timothy J M Moss, Jacqueline M Melville, Timothy J M Moss

Abstract

Preterm birth occurs in 11% of live births globally and accounts for 35% of all newborn deaths. Preterm newborns have immature immune systems, with reduced innate and adaptive immunity; their immune systems may be further compromised by various factors associated with preterm birth. The immune systems of preterm infants have a smaller pool of monocytes and neutrophils, impaired ability of these cells to kill pathogens, and lower production of cytokines which limits T cell activation and reduces the ability to fight bacteria and detect viruses in cells, compared to term infants. Intrauterine inflammation is a major contributor to preterm birth, and causes premature immune activation and cytokine production. This can induce immune tolerance leading to reduced newborn immune function. Intrauterine inflammation is associated with an increased risk of early-onset sepsis and likely has long-term adverse immune consequences. Requisite medical interventions further impact on immune development and function. Antenatal corticosteroid treatment to prevent newborn respiratory disease is routine but may be immunosuppressive, and has been associated with febrile responses, reductions in lymphocyte proliferation and cytokine production, and increased risk of infection. Invasive medical procedures result in an increased risk of late-onset sepsis. Respiratory support can cause chronic inflammatory lung disease associated with increased risk of long-term morbidity. Colonization of the infant by microorganisms at birth is a significant contributor to the establishment of the microbiome. Caesarean section affects infant colonization, potentially contributing to lifelong immune function and well-being. Several factors associated with preterm birth alter immune function. A better understanding of perinatal modification of the preterm immune system will allow for the refinement of care to minimize lifelong adverse immune consequences.

Keywords: antenatal glucocorticoids; immature immune system; inflammation; preterm; ventilation.

Figures

Figure 1
Figure 1
Leukocyte development begins in the yolk sac before moving to the liver and finally the bone marrow. The development and maturation of primary lymphoid organs (blue) and peripheral blood leukocytes (red) occur throughout gestation but is not complete until after birth. The light gray shading shows the gestational ages of preterm births from the threshold of viability (24 weeks; at which 50% of infants in developed countries survive) to 37 weeks of gestation. Based on a figure from Durandy (2003).

References

    1. Abbas A. K., Lichtman A. H. (2006). Basic Immunology: Functions and Disorders of the Immune System. Philadelphia, PA: Saunders Elsevier
    1. Adams-Chapman I. (2012). Long-term impact of infection on the preterm neonate. Semin. Perinatol. 36, 462–470 10.1053/j.semperi.2012.06.009
    1. Attar M. A., Donn S. M. (2002). Mechanisms of ventilator-induced lung injury in premature infants. Semin. Neonatol. 7, 353–360 10.1053/siny.2002.0129
    1. Ballabh P., Simm M., Kumari J., Krauss A. N., Jain A., Auld P. A., et al. (2003). Lymphocyte subpopulations in bronchopulmonary dysplasia. Am. J. Perinatol. 20, 465–475 10.1055/s-2003-45387
    1. Barak M., Cohen A., Herschkowitz S. (1992). Total leukocyte and neutrophil count changes associated with antenatal betamethasone administration in premature infants. Acta Paediatr. 81, 760–763
    1. Barnes P. J. (2005). Molecular mechanisms and cellular effects of glucocorticoids. Immunol. Allergy Clin. North Am. 25, 451–468 10.1016/j.iac.2005.05.003
    1. Beato M., Herrlich P., Schultz G. (1995). Steriod hormone receptors: many actors in search of a plot. Cell 83, 851–857 10.1016/0092-8674(95)90201-5
    1. Beck S., Wojdyla D., Say L., Betran A. P., Merialdi M., Requejo J. H., et al. (2010). The worldwide incidence of preterm birth: a systematic review of maternal mortality and morbidity. Bull. World Health Organ. 88, 31–38 10.2471/BLT.08.062554
    1. Been J. V., Rours I. G. I. J. G., Kornelisse R. F., Lima Passos V., Kramer B. W., Schneider T. A. J., et al. (2009). Histologic chorioamnionitis, fetal involvement, and antenatal steroids: effects on neonatal outcome in preterm infants. Am. J. Obstet. Gynecol. 201, 587e1–587e8 10.1016/j.ajog.2009.06.025
    1. Berrington J. E., Barge D., Fenton A. C., Cant A. J., Spickett G. P. (2005). Lymphocyte subsets in term and significantly preterm UK infants in the first year of life analysed by single platform flow cytometry. Clin. Exp. Immunol. 140, 289–292 10.1111/j.1365-2249.2005.02767.x
    1. Berry S. M., Romero R., Gomez R., Puder K. S., Ghezzi F., Cotton D. B., et al. (1995). Premature parturition is characterized by in utero activation of the fetal immune system. Am. J. Obstet. Gynecol. 173, 1315–1320
    1. Biasucci G., Rubini M., Riboni S., Morelli L., Bessi E., Retetangos C. (2010). Mode of delivery affects the bacterial community in the newborn gut. Early Hum. Dev. 86Suppl. 1, 13–15 10.1016/j.earlhumdev.2010.01.004
    1. Bohrer B., Silveira R. C., Neto E. C., Procianoy R. S. (2010). Mechanical ventilation of newborns infant changes in plasma pro- and anti-inflammatory cytokines. J. Pediatr. 156, 16–19 10.1016/j.jpeds.2009.07.027
    1. Bose C. L., Laughon M. M., Allred E. N., O'Shea T. M., Van Marter L. J., Ehrenkranz R. A., et al. (2013). Systemic inflammation associated with mechanical ventilation among extremely preterm infants. Cytokine 61, 315–322 10.1016/j.cyto.2012.10.014
    1. Brinkmann V., Zychlinsky A. (2012). Neutrophil extracellular traps: Is immunity the second function of chromatin? J. Cell Biol. 198, 773–783 10.1083/jcb.201203170
    1. Brown M. K., DiBlasi R. M. (2011). Mechanical ventilation of the premature neonate. Respir. Care 56, 1298–1311 discussion: 1311–1313. 10.4187/respcare.01429
    1. Bujdoso R., Young P., Harkiss G. D., McConnell I. (1989). Antigen presentation in the sheep: generation of antigen-specific T-cell lines. Immunology 66, 559–564
    1. Carr R. (2000). Neutrophil production and function in newborn infants. Br. J. Haematol. 110, 18–28 10.1046/j.1365-2141.2000.01992.x
    1. Carr R., Brocklehurst P., Dore C. J., Modi N. (2009). Granulocyte-macrophage colony stimulating factor administered as prophylaxis for reduction of sepsis in extremely preterm, small for gestational age neonates (the PROGRAMS trial): a single-blind, multicentre, randomised controlled trial. Lancet 373, 226–233 10.1016/S0140-6736(09)60071-4
    1. Carr R., Modi N. (1997). Haemopoietic colony stimulating factors for preterm neonates. Arch. Dis. Child. Fetal Neonatal Ed. 76, F128–F133 10.1136/fn.76.2.F128
    1. Cepika A. M., Bendelja K., Vergles J. M., Malenica B., Kapitanovic S., Gagro A. (2010). Monocyte response to LPS after exposure to corticosteroids and chloroquine with implications for systemic lupus erythematosus. Scand. J. Immunol. 72, 434–443 10.1111/j.1365-3083.2010.02450.x
    1. Chabra S., Cottrill C., Rayens M. K., Cross R., Lipke D., Bruce M. (1998). Lymphocyte subsets in cord blood of preterm infants: effect of antenatal steroids. Biol. Neonate 74, 200–207
    1. Cheong J. L., Doyle L. W. (2012). Increasing rates of prematurity and epidemiology of late preterm birth. J. Paediatr. Child Health 48, 784–788 10.1111/j.1440-1754.2012.02536.x
    1. Correa-Rocha R., Perez A., Lorente R., Ferrando-Martinez S., Leal M., Gurbindo D., et al. (2012). Preterm neonates show marked leukopenia and lymphopenia that are associated with increased regulatory T-cell values and diminished IL-7. Pediatr. Res. 71, 590–597 10.1038/pr.2012.6
    1. Currie A. J., Curtis S., Strunk T., Riley K., Liyanage K., Prescott S., et al. (2011). Preterm infants have deficient monocyte and lymphocyte cytokine responses to group B streptococcus. Infect. Immun. 79, 1588–1596 10.1128/IAI.00535-10
    1. de Groot J., Kranendonk G., Fillerup M., Hopster H., Boersma W., Hodgson D., et al. (2007). Response to LPS in female offspring from sows treated with cortisol during pregnancy. Physiol. Behav. 90, 612–618 10.1016/j.physbeh.2006.11.013
    1. Dembinski J., Behrendt D., Martini R., Heep A., Bartmann P. (2003). Modulation of pro- and anti-inflammatory cytokine production in very preterm infants. Cytokine 21, 200–206 10.1016/S1043-4666(02)00498-2
    1. Doyle L. W. (2001). Outcome at 5 years of age of children 23 to 27 weeks' gestation: refining the prognosis. Pediatrics 108, 134–141 10.1542/peds.108.1.134
    1. Driscoll M. S., Thomas V. L., Ramamurthy R. S., Casto D. T. (1990). Longitudinal evaluation of polymorphonuclear leukocyte chemiluminescence in premature infants. J. Pediatr. 116, 429–434
    1. Duggan P., Maalouf E., Watts T., Sullivan M., Counsell S., Allsop J., et al. (2001). Intrauterine T-cell activation and increased proinflammatory cytokine concentration in preterm infants with cerebral lesions. Lancet 358, 1699–1700 10.1016/S0140-6736(01)06723-X
    1. Duncan J. R., Cock M. L., Suzuki K., Scheerlinck J. P. Y., Harding R., Rees S. M. (2006). Chronic endotoxin exposure causes brain injury in the ovine fetus in the absence of hypoxemia. J. Soc. Gynecol. Investig. 13, 87–96 10.1016/j.jsgi.2005.12.003
    1. Durandy A. (2003). Ontogeny of the immune system. Transfus. Med. Hemother. 30, 222–227 10.1016/j.dci.2005.08.001
    1. Edelstone D. I., Mueller-Heubach M. D., Caritis S. N. (1978). Effects of dexamethasone on leukocyte counts in pregnant sheep and fetal lambs. Am. J. Obstet. Gynecol. 131, 677–681
    1. Fahey J. O. (2008). Clinical management of intra-amniotic infection and chorioamnionitis: a review of the literature. J. Midwifery Womens Health 53, 227–235 10.1016/j.jmwh.2008.01.001
    1. Fietta A., Sacchi F., Bersani C., Gialdroni Grassi G., Stronati M., Gancia P., et al. (1987). Complement-dependent bactericidal activity for E. coli K12 in serum of preterm newborn infants. Acta Paediatr. Scand. 76, 37–41
    1. Fuenfer M. M., Herson V. C., Raye J. R., Woronick C. L., Eisenfeld L., Ingardia C. J., et al. (1987). The effect of betamethasone on neonatal neutrophil chemotaxis. Pediatr. Res. 22, 150–153 10.1203/00006450-198708000-00009
    1. Goldenberg R. L., Culhane J. F. (2003). Infection as a cause of preterm birth. Clin. Perinatol. 30, 677–700
    1. Goldenberg R. L., Hauth J. C., Andrews W. W. (2000). Intrauterine infection and preterm delivery. New Engl. J. Med. 342, 1500–1507 10.1056/NEJM200005183422007
    1. Gotsch F., Romero R., Kusanovic J. P., Mazaki-Tovi S., Pineles B. L., Erez O., et al. (2007). The fetal inflammatory response syndrome. Clin. Obstet. Gynecol. 50, 652–683 10.1097/GRF.0b013e31811ebef6
    1. Gronlund M. M., Lehtonen O. P., Eerola E., Kero P. (1999). Fecal microflora in healthy infants born by different methods of delivery: permanent changes in intestinal flora after cesarean delivery. J. Pediatr. Gastroenterol. Nutr. 28, 19–25
    1. Hagberg H., Wennerholm U. B., Sävman K. (2002). Sequelae of chorioamnionitis. Curr. Opin. Infect. Dis. 15, 301–306
    1. Hannet I., Erkeller-Yuksel F., Lydyard P., Deneys V., DeBruyere M. (1992). Developmental and maturational changes in human blood lymphocyte subpopulations. Immunol. Today 13, 215, 218. 10.1016/0167-5699(92)90157-3
    1. Hartel C., Adam N., Strunk T., Temming P., Muller-Steinhardt M., Schultz C. (2005). Cytokine responses correlate differentially with age in infancy and early childhood. Clin. Exp. Immunol. 142, 446–453 10.1111/j.1365-2249.2005.02928.x
    1. Heininger U., Riffelmann M., Leineweber B., Wirsing von Koenig C. H. (2009). Maternally derived antibodies against Bordetella pertussis antigens pertussis toxin and filamentous hemagglutinin in preterm and full term newborns. Pediatr. Infect. Dis. J. 28, 443–445 10.1097/INF.0b013e318193ead7
    1. Hillman N. H., Moss T. J., Kallapur S. G., Bachurski C., Pillow J. J., Polglase G. R., et al. (2007). Brief, large tidal volume ventilation initiates lung injury and a systemic response in fetal sheep. Am. J. Respir. Crit. Care Med. 176, 575–581 10.1164/rccm.200701-051OC
    1. Hillman N. H., Pillow J. J., Ball M. K., Polglase G. R., Kallapur S. G., Jobe A. H. (2009). Antenatal and postnatal corticosteroid and resuscitation induced lung injury in preterm sheep. Respir. Res. 10, 124 10.1186/1465-9921-10-124
    1. Hillman N. H., Polglase G. R., Pillow J. J., Saito M., Kallapur S. G., Jobe A. H. (2011). Inflammation and lung maturation from stretch injury in preterm fetal sheep. Am. J. Physiol. Lung Cell. Mol. Physiol. 300, L232–L241 10.1152/ajplung.00294.2010
    1. Holt P. G., Jones C. A. (2000). The development of the immune system during pregnancy and early life. Allergy 55, 688–697 10.1034/j.1398-9995.2000.00118.x
    1. Howson C. P., Kinney M. V., Lawn J. E. (2012). Born Too Soon: The Global Action Report on Preterm Birth. Geneva: March of Dimes, PMNCH, Save the Children and WHO
    1. Jobe A. H., Hillman N., Polglase G., Kramer B. W., Kallapur S., Pillow J. (2008). Injury and inflammation from resuscitation of the preterm infant. Neonatology 94, 190–196 10.1159/000143721
    1. Kallapur S. G., Jobe A. H., Ball M. K., Nitsos I., Moss T. J. M., Hillman N. H., et al. (2007). Pulmonary and systemic endotoxin tolerance in preterm fetal sheep exposed to chorioamnionitis. J. Immunol. 179, 8491–8499
    1. Kramer B. W., Joshi S. N., Moss T. J. M., Newnham J. P., Sindelar R., Jobe A. H., et al. (2007). Endotoxin-induced maturation of monocytes in preterm fetal sheep lung. Am. J. Physiol. Lung Cell. Mol. Physiol. 293, L345–L353 10.1152/ajplung.00003.2007
    1. Källman J., Schollin J., Schalèn C., Erlandsson A., Kihlström E. (1998). Impaired phagocytosis and opsonisation towards group B streptococci in preterm neonates. Arch. Dis. Child. Fetal Neonatal Ed. 78, F46–F50 10.1136/fn.78.1.F46
    1. Kaur K., Chowdhury S., Greenspan N. S., Schreiber J. R. (2007). Decreased expression of tumor necrosis factor family receptors involved in humoral immune responses in preterm neonates. Blood 110, 2948–2954 10.1182/blood-2007-01-069245
    1. Kavelaars A., Van Der Pompe G., Bakker J. M., Van Hasselt P. M., Cats B., Visser G. H. A., et al. (1999). Altered immune function in human newborns after prenatal administration of betamethasone: enhanced natural killer cell activity and decreased T cell proliferation in cord blood. Pediatr. Res. 45, 306–312 10.1203/00006450-199903000-00003
    1. Kay G., Tarcic N., Poltyrev T., Weinstock M. (1998). Prenatal stress depresses immune function in rats. Physiol. Behav. 63, 397–402 10.1016/S0031-9384(97)00456-3
    1. Koksal N., Kayik B., Cetinkaya M., Ozkan H., Budak F., Kilic S., et al. (2012). Value of serum and bronchoalveolar fluid lavage pro- and anti-inflammatory cytokine levels for predicting bronchopulmonary dysplasia in premature infants. Eur. Cytokine Netw. 23, 29–35 10.1684/ecn.2012.0304
    1. Kolokotroni O., Middleton N., Gavatha M., Lamnisos D., Priftis K. N., Yiallouros P. K. (2012). Asthma and atopy in children born by caesarean section: effect modification by family history of allergies – a population based cross-sectional study. BMC Pediatr. 12:179 10.1186/1471-2431-12-179
    1. Kramer B. W., Ikegami M., Moss T. J. M., Nitsos I., Newnham J. P., Jobe A. H. (2004). Antenatal betamethasone changes cord blood monocyte responses to endotoxin in preterm lambs. Pediatr. Res. 55, 764–768 10.1203/01.PDR.0000120678.72485.19
    1. Kramer B. W., Ikegami M., Moss T. J., Nitsos I., Newnham J. P., Jobe A. H. (2005). Endotoxin-induced chorioamnionitis modulates innate immunity of monocytes in preterm sheep. Am. J. Respir. Crit. Care Med. 171, 73–77 10.1164/rccm.200406-745OC
    1. Kumar D., Schatz F., Moore R. M., Mercer B. M., Rangaswamy N., Mansour J. M., et al. (2011). The effects of thrombin and cytokines upon the biomechanics and remodeling of isolated amnion membrane, in vitro. Placenta 32, 206–213 10.1016/j.placenta.2011.01.006
    1. Lahra M. M., Jeffery H. E. (2004). A fetal response to chorioamnionitis is associated with early survival after preterm birth. Am. J. Obstet. Gynecol. 190, 147–151 10.1016/j.ajog.2003.07.012
    1. Laws P., Abeywardana S., Walker J., Sullivan E. (2007). Australia's mothers and babies 2005, in Perinatal Statistics Series; AIHW National Perinatal Statistics Unit, 20(Cat. no. PER 40), (Sydney: ).
    1. Levy E., Xanthou G., Petrakou E., Zacharioubaki V., Tsatsanis C., Fotopoulos S., et al. (2009). Distinct roles of TLR4 and CD14 in LPS-induced inflammatory responses of neonates. Pediatr. Res. 66, 179–184 10.1203/PDR.0b013e3181a9f41b
    1. Levy O. (2004). Antimicrobial proteins and peptides: anti-infective molecules of mammalian leukocytes. J. Leukoc. Biol. 76, 909–925 10.1189/jlb.0604320
    1. Li Z., McNally L., Hilder L., Sullivan E. (2011). Australia's mothers and babies 2009, in Perinatal Statistics Series; AIHW National Perinatal Epidemiology and Statistics Unit, 20(Cat. no. PER 52), (Sydney: ).
    1. Liggins G. C. (1969). Premature delivery of foetal lambs infused with glucocorticoids. J. Endocrinol. 45, 515–523 10.1677/joe.0.0450515
    1. Liu Y. J., Banchereau J. (1997). Regulation of B-cell commitment to plasma cells or to memory B cells. Semin. Immunol. 9, 235–240 10.1006/smim.1997.0080
    1. Maitra A., Sherriff A., Strachan D., Henderson J. (2004). Mode of delivery is not associated with asthma or atopy in childhood. Clin. Exp. Allergy 34, 1349–1355 10.1111/j.1365-2222.2004.02048.x
    1. Marodi L. (2006). Innate cellular immune responses in newborns. Clin. Immunol. 118, 137–144 10.1016/j.clim.2005.10.012
    1. Martin J. A., Hamilton B. E., Ventura S. J., Osterman M. J., Kirmeyer S., Mathews T. J., et al. (2011). Births: final data for 2009. Natl. Vital Stat. Rep. 60, 1–70
    1. McGreal E. P., Hearne K., Spiller O. B. (2012). Off to a slow start: under-development of the complement system in term newborns is more substantial following premature birth. Immunobiology 217, 176–186 10.1016/j.imbio.2011.07.027
    1. Medzhitov R., Janeway C. A., Jr. (1997). Innate immunity: impact on the adaptive immune response. Curr. Opin. Immunol. 9, 4–9 10.1016/S0952-7915(97)80152-5
    1. Melville J. M., Bischof R. J., Meeusen E. N., Westover A. J., Moss T. J. (2012). Changes in fetal thymic immune cell populations in a sheep model of intrauterine inflammation. Reprod. Sci. 19, 740–747 10.1177/1933719111432873
    1. Moss T. J. M., Davey M. G., Harding R., Newnham J. P. (2002a). Effects of intra-amniotic endotoxin on lung structure and function two months after term birth in sheep. J. Soc. Gynecol. Investig. 9, 220–225
    1. Moss T. J. M., Harding R., Newnham J. P. (2002b). Lung function, arterial pressure and growth in sheep during early postnatal life following single and repeated prenatal corticosteroid treatments. Early Hum. Dev. 66, 11–24
    1. Moss T. J. M., Nitsos I., Kramer B. W., Ikegami M., Newnham J. P., Jobe A. H. (2002c). Intra-amniotic endotoxin induces lung maturation by direct effects on the developing respiratory tract in preterm sheep. Am. J. Obstet. Gynecol. 187, 1059–1065 10.1067/mob.2002.126296
    1. Murthy K. K., Moya F. R. (1994). Effect of betamethasone on maternal, fetal and neonatal rat cellular immunity. Early Hum. Dev. 36, 1–11 10.1016/0378-3782(94)90028-0
    1. Mwaniki M. K., Atieno M., Lawn J. E., Newton C. R. (2012). Long-term neurodevelopmental outcomes after intrauterine and neonatal insults: a systematic review. Lancet 379, 445–452 10.1016/S0140-6736(11)61577-8
    1. Nilsson A., Vesterlund L., Oldenborg P. A. (2012). Macrophage expression of LRP1, a receptor for apoptotic cells and unopsonized erythrocytes, can be regulated by glucocorticoids. Biochem. Biophys. Res. Commun. 417, 1304–1309 10.1016/j.bbrc.2011.12.137
    1. Nitsos I., Rees S. M., Duncan J., Kramer B. W., Harding R., Newnham J. P., et al. (2006). Chronic exposure to intra-amniotic lipopolysaccharide affects the ovine fetal brain. J. Soc. Gynecol. Investig. 13, 239–247 10.1016/j.jsgi.2006.02.011
    1. Nonoyama S., Penix L. A., Edwards C. P., Lewis D. B., Ito S., Aruffo A., et al. (1995). Diminished expression of CD40 ligand by activated neonatal T cells. J. Clin. Invest. 95, 66–75 10.1172/JCI117677
    1. Nussbaum C., Sperandio M. (2011). Innate immune cell recruitment in the fetus and neonate. J. Reprod. Immunol. 90, 74–81 10.1016/j.jri.2011.01.022
    1. O'Connor A. R., Wilson C. M., Fielder A. R. (2007). Ophthalmological problems associated with preterm birth. Eye 21, 1254–1260 10.1038/sj.eye.6702838
    1. Pelkonen A. S., Suomalainen H., Hallman M., Turpeinen M. (1999). Peripheral blood lymphocyte subpopulations in schoolchildren born very preterm. Arch. Dis. Child. Fetal Neonatal Ed. 81, F188–F193 10.1136/fn.81.3.F188
    1. Perez A., Bellon J. M., Gurbindo M. D., Munoz-Fernandez M. A. (2010). Impairment of stimulation ability of very-preterm neonatal monocytes in response to lipopolysaccharide. Hum. Immunol. 71, 151–157 10.1016/j.humimm.2009.11.011
    1. Pistiner M., Gold D. R., Abdulkerim H., Hoffman E., Celedon J. C. (2008). Birth by cesarean section, allergic rhinitis, and allergic sensitization among children with a parental history of atopy. J. Allergy Clin. Immunol. 122, 274–279 10.1016/j.jaci.2008.05.007
    1. Pringle K. C. (1986). Human fetal lung development and related animal models. Clin. Obstet. Gynecol. 29, 502–513
    1. Renz-Polster H., David M. R., Buist A. S., Vollmer W. M., O'Connor E. A., Frazier E. A., et al. (2005). Caesarean section delivery and the risk of allergic disorders in childhood. Clin. Exp. Allergy 35, 1466–1472 10.1111/j.1365-2222.2005.02356.x
    1. Reyes T. M., Coe C. L. (1997). Prenatal manipulations reduce proinflammatory response to a cytokine challenge in juvenile monkeys. Brain Res. 769, 29–35 10.1016/S0006-8993(97)00687-2
    1. Roberts D., Dalziel S. (2006). Antenatal corticosteroids for accelerating fetal lung maturation for women at risk of preterm birth (review). Cochrane Database Syst. Rev. 3, Art No. CD004454. 10.1002/14651858.CD004454.pub2
    1. Romero R., Gotsch F., Pineles B., Kusanovic J. P. (2007). Inflammation in pregnancy: its roles in reproductive physiology, obstetrical complications, and fetal injury. Nutr. Rev. 65(12 Pt 2), S194–S202 10.1111/j.1753-4887.2007.tb00362.x
    1. Romero R., Savasan Z. A., Chaiworapongsa T., Berry S. M., Kusanovic J. P., Hassan S. S., et al. (2011). Hematologic profile of the fetus with systemic inflammatory response syndrome. J. Perinat. Med. 40, 19–32 10.1515/JPM.2011.100
    1. Salam M. T., Margolis H. G., McConnell R., McGregor J. A., Avol E. L., Gilliland F. D. (2006). Mode of delivery is associated with asthma and allergy occurrences in children. Ann. Epidemiol. 16, 341–346 10.1016/j.annepidem.2005.06.054
    1. Sharma A. A., Jen R., Butler A., Lavoie P. M. (2012). The developing human preterm neonatal immune system: a case for more research in this area. Clin. Immunol. 145, 61–68 10.1016/j.clim.2012.08.006
    1. Shen C. M., Lin S. C., Niu D. M., Kou Y. R. (2009). Labour increases the surface expression of two Toll-like receptors in the cord blood monocytes of healthy term newborns. Acta Paediatr. 98, 959–962 10.1111/j.1651-2227.2009.01280.x
    1. Siggers R. H., Siggers J., Thymann T., Boye M., Sangild P. T. (2011). Nutritional modulation of the gut microbiota and immune system in preterm neonates susceptible to necrotizing enterocolitis. J. Nutr. Biochem. 22, 511–521 10.1016/j.jnutbio.2010.08.002
    1. Soraisham A. S., Singhal N., McMillan D. D., Sauve R. S., Lee S. K. (2009). A multicenter study on the clinical outcome of chorioamnionitis in preterm infants. Am. J. Obstet. Gynecol. 200, 372.e1–372.e6 10.1016/j.ajog.2008.11.034
    1. Strunk T., Currie A., Richmond P., Simmer K., Burgner D. (2011). Innate immunity in human newborn infants: prematurity means more than immaturity. J. Matern Fetal Neonatal Med. 24, 25–31 10.3109/14767058.2010.482605
    1. Strunk T., Doherty D., Jacques A., Simmer K., Richmond P., Kohan R., et al. (2012). Histologic chorioamnionitis is associated with reduced risk of late-onset sepsis in preterm infants. Pediatrics 129, e134–e141 10.1542/peds.2010-3493
    1. Strunk T., Temming P., Gembruch U., Reiss I., Bucsky P., Schultz C. (2004). Differential maturation of the innate immune response in human fetuses. Pediatr. Res. 56, 219–226 10.1203/01.PDR.0000132664.66975.79
    1. Swierzko A. S., Atkinson A. P., Cedzynski M., MacDonald S. L., Szala A., Domzalska-Popadiuk I., et al. (2009). Two factors of the lectin pathway of complement, l-ficolin and mannan-binding lectin, and their associations with prematurity, low birthweight and infections in a large cohort of Polish neonates. Mol. Immunol. 46, 551–558 10.1016/j.molimm.2008.07.025
    1. Sykes L., MacIntyre D. A., Yap X. J., Teoh T. G., Bennett P. R. (2012). The Th1:th2 dichotomy of pregnancy and preterm labour. Mediators Inflamm. 2012, 967629 10.1155/2012/967629
    1. Szekeres-Bartho J. (2002). Immunological relationship between the mother and the fetus. Int. Rev. Immunol. 21, 471–495
    1. Tatad A. M. F., Nesin M., Peoples J., Cheung S., Lin H., Sison C., et al. (2008). Cytokine expression in response to bacterial antigens in preterm and term infant cord blood monocytes. Neonatology 94, 8–15 10.1159/000112541
    1. Thavagnanam S., Fleming J., Bromley A., Shields M. D., Cardwell C. R. (2008). A meta-analysis of the association between Caesarean section and childhood asthma. Clin. Exp. Allergy 38, 629–633 10.1111/j.1365-2222.2007.02780.x
    1. Tsianakas A., Varga G., Barczyk K., Bode G., Nippe N., Kran N., et al. (2012). Induction of an anti-inflammatory human monocyte subtype is a unique property of glucocorticoids, but can be modified by IL-6 and IL-10. Immunobiology 217, 329–335 10.1016/j.imbio.2011.10.002
    1. Tuckermann J. P., Kleiman A., McPherson K. G., Reichardt H. M. (2005). Molecular mechanisms of glucocorticoids in the control of inflammation and lymphocyte apoptosis. Crit. Rev. Clin. Lab. Sci. 42, 71–104
    1. Turunen R., Nupponen I., Siitonen S., Repo H., Andersson S. (2006). Onset of mechanical ventilation is associated with rapid activation of circulating phagocytes in preterm infants. Pediatrics 117, 448–454 10.1542/peds.2005-0123
    1. Turunen R., Vaarala O., Nupponen I., Kajantie E., Siitonen S., Lano A., et al. (2009). Activation of T cells in preterm infants with respiratory distress syndrome. Neonatology 96, 248–258 10.1159/000220764
    1. van den Berg J. P., Westerbeek E. A. M., van der Klis F. R. M., Berbers G. A. M., van Elburg R. M. (2011). Transplacental transport of IgG antibodies to preterm infants: a review of the literature. Early Hum. Dev. 87, 67–72 10.1016/j.earlhumdev.2010.11.003
    1. Vermillion S. T., Soper D. E., Newman R. B. (2000). Neonatal sepsis and death after multiple courses of antenatal betamethasone therapy. Am. J. Obstet. Gynecol. 183, 810–814 10.1067/mob.2000.108838
    1. Walker J. C., Smolders M. A., Gemen E. F., Antonius T. A., Leuvenink J., de Vries E. (2011). Development of lymphocyte subpopulations in preterm infants. Scand. J. Immunol. 73, 53–58 10.1111/j.1365-3083.2010.02473.x
    1. Wallace E. M., Ekkel K., Cotter T., Tippett C., Catalano J. (1998). Haematological effects of betamethasone treatment in late pregnancy. Aust. N.Z. J. Obstet. Gynaecol. 38, 396–398
    1. Wallace M. J., Probyn M. E., Zahra V. A., Crossley K., Cole T. J., Davis P. G., et al. (2009). Early biomarkers and potential mediators of ventilation-induced lung injury in very preterm lambs. Respir. Res. 10, 19 10.1186/1465-9921-10-19
    1. Westover A. J., Hooper S. B., Wallace M. J., Moss T. J. (2012). Prostaglandins mediate the fetal pulmonary response to intrauterine inflammation. Am. J. Physiol. Lung Cell. Mol Physiol 302, L664–L678 10.1152/ajplung.00297.2011
    1. Witko-Sarsat V., Rieu P., Descamps-Latscha B., Lesavre P., Halbwachs-Mecarelli L. (2000). Neutrophils: molecules, functions and pathophysiological aspects. Lab. Invest. 80, 617–653
    1. Wolfs T. G. A. M., Buurman W. A., Zoer B., Moonen R. M. J., Derikx J. P. M., Thuijls G., et al. (2009). Endotoxin induced chorioamnionitis prevents intestinal development during gestation in fetal sheep. PLoS ONE 4:e5837 10.1371/journal.pone.0005837
    1. Wynn J. L., Neu J., Moldawer L. L., Levy O. (2009). Potential of immunomodulatory agents for prevention and treatment of neonatal sepsis. J. Perinatol. 29, 79–88 10.1038/jp.2008.132
    1. Xu B., Pekkanen J., Hartikainen A. L., Jarvelin M. R. (2001). Caesarean section and risk of asthma and allergy in adulthood. J. Allergy Clin. Immunol. 107, 732–733 10.1067/mai.2001.113048
    1. Xu B., Pekkanen J., Jarvelin M. R. (2000). Obstetric complications and asthma in childhood. J. Asthma 37, 589–594
    1. Yost C. C., Cody M. J., Harris E. S., Thornton N. L., McInturff A. M., Martinez M. L., et al. (2009). Impaired neutrophil extracellular trap (NET) formation: a novel innate immune deficiency of human neonates. Blood 113, 6419–6427 10.1182/blood-2008-07-171629

Source: PubMed

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