Influence of iron status on risk of maternal or neonatal infection and on neonatal mortality with an emphasis on developing countries

Nutrition Reviews

Volumn 71, Issue 8, 2013, Pages 528-540

  Brabin, Loretta ^a   Brabin, Bernard J ^b,c   Gies, Sabine ^d  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

^c EMMA CHILDREN S HOSPITAL   (Netherlands)

^d INSTITUTE OF TROPICAL MEDICINE   (Belgium)

Author keywords

Birth outcomes; Infection; Iron; Maternal; Neonatal; Pregnancy; Supplementation

Indexed keywords

FERROPORTIN; FOLIC ACID; HEPCIDIN; IRON; LACTOFERRIN; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN;

ANTIBIOTIC PROPHYLAXIS; ARTICLE; ASYMPTOMATIC INFECTION; CHLAMYDIASIS; CHORIOAMNIONITIS; CLINICAL FEATURE; DEVELOPING COUNTRY; DIET SUPPLEMENTATION; FIRST TRIMESTER PREGNANCY; GENITAL TRACT INFECTION; HEMOGLOBIN DETERMINATION; HUMAN; IMMUNE RESPONSE; IN VITRO STUDY; INDUSTRIALIZATION; INFECTION RISK; IRON DEFICIENCY; IRON DEFICIENCY ANEMIA; IRON OVERLOAD; IRON STORAGE; IRON TRANSPORT; LOW BIRTH WEIGHT; MALARIA; META ANALYSIS (TOPIC); NEWBORN INFECTION; NEWBORN MORTALITY; NEWBORN SEPSIS; PERSISTENT INFECTION; PRACTICE GUIDELINE; PREGNANCY OUTCOME; PREGNANT WOMAN; PREMATURE LABOR; PRENATAL CARE; RANDOMIZED CONTROLLED TRIAL (TOPIC); SECOND TRIMESTER ABORTION; SECOND TRIMESTER PREGNANCY; STILLBIRTH; THIRD TRIMESTER PREGNANCY; TOXOPLASMOSIS; VERTICAL TRANSMISSION;

BIRTH OUTCOMES; INFECTION; IRON; MATERNAL; NEONATAL; PREGNANCY; SUPPLEMENTATION;

ANEMIA, IRON-DEFICIENCY; DEVELOPING COUNTRIES; FEMALE; HEALTH STATUS; HUMANS; INFANT MORTALITY; INFANT, NEWBORN; INFECTION; IRON; PREGNANCY; PREGNANCY COMPLICATIONS, INFECTIOUS; PREGNANCY OUTCOME; PREMATURE BIRTH; RISK FACTORS;

BACTERIA (MICROORGANISMS);

EID: 84880585697     PISSN: 00296643     EISSN: 17534887     Source Type: Journal    
DOI: 10.1111/nure.12049     Document Type: Article

References (187)

1. Lawn JE, Cousens S, Zupan J. 4 million neonatal deaths: when? where? why? Lancet. 2005;365:891-900.
2. Thaver D, Zaidi AK. Burden of neonatal infections in developing countries: a review of evidence from community-based studies. Pediatr Infect Dis J. 2009;28(Suppl):S3-S9.
3. McGreal EP, Hearne K, Spiller OB. Off to a slow start: under-development of the complement system in term newborns is more substantial following premature birth. Immunobiology. 2012;217:176-186.
4. Raqib R, Alam DS, Sarker P, etal. Low birth weight is associated with altered immune function in rural Bangladeshi children: a birth cohort study. Am J Clin Nutr. 2007;85:845-852.
5. Palmer AC. Nutritionally mediated programming of the developing immune system. Adv Nutr. 2011;2:377-395.
6. Basu S, Dewangan S, Shukla RC, etal. Thymic involution as a predictor of early-onset neonatal sepsis. Paed Int Child Health. 2012;32:147-151.
7. Lawn JE, Cousens SN, Darmstadt GL, etal. 1 year after the Lancet Neonatal Survival Series - was the call for action heard? Lancet. 2006;367:1541-1547.
8. Fernández-Gaxiola AC, De-Regil LM. Intermittent iron supplementation for reducing anaemia and its associated impairments in menstruating women. Cochrane Database Syst Rev. 2011;(12):CD009218.
9. World Health Organization. Weekly iron-folic acid supplementations (WIFS) in women of reproductive age: its role in promoting optimal maternal and child health. 2009; Available at: http://www.who.int/nutrition/publications/micronutrients/weekly_iron_folicacid/en/. Accessed 10 May 2013.
10. Peña-Rosas JP, Viteri FE. Effects and safety of preventive oral iron or iron and folic acid supplementation for women during pregnancy. Cochrane Database Syst Rev. 2009;(4):CD004736.
11. Viteri FE. Iron endowment at birth: maternal iron status and other influences. Nutr Rev. 2011;69(Suppl 1):S3-S16.
12. Beard JL. Iron biology in immune function, muscle metabolism and neural functioning. J Nutr. 2001;131:568S-580S.
13. Cousens S, Blencowe H, Stanton C, etal. National, regional, and worldwide estimates of stillbirth rates in 2009 with trends since 1995: a systematic analysis. Lancet. 2011;377:1319-1330.
14. Black RE, Cousens S, Johnson HL, etal. Global, regional, and national causes of child mortality in 2008: a systematic analysis. Lancet. 2010;375:1969-1987.
15. Goldenberg RL, McClure EM, Saleem S, etal. Infection-related stillbirths. Lancet. 2010;375:1482-1490.
16. Muglia LJ, Katz M. The enigma of spontaneous preterm birth. N Engl J Med. 2010;362:529-535.
17. Loyevsky M, LaVaute T, Allerson CR, etal. An IRP-like protein from Plasmodium falciparum binds to a mammalian iron-responsive element. Blood. 2001;98:2555-2562.
18. Coulanges V, Andre P, Ziegler O, etal. Utilization of iron-catecholamine complexes involving ferric reductase activity in Listeria monocytogenes. Infect Immun. 1997;65:2778-2785.
19. Eisenstein BI, Jones GW. The spectrum of infections and pathogenic mechanisms of Escherichia coli. Adv Intern Med. 1988;33:231-252.
20. Mason WJ, Skaar EP. Assessing the contribution of heme-iron acquisition to Staphylococcus aureus pneumonia using computed topography. PLoS ONE. 2009;4:e6668.
21. Chhibber S, Bajaj J. Polysaccharide-iron-regulated cell surface protein conjugate vaccine: its role in protection against Klebsiella pneumoniae-induced lobar pneumonia. Vaccine. 1995;13:179-184.
22. Tsou CC, Chiang-Ni C, Lin YS, etal. An iron-binding protein, Dpr, decreases hydrogen peroxide stress and protects Streptococcus pyogenes against multiple stresses. Infect Immun. 2008;76:4038-4045.
23. Dill BD, Dessus-Babus S, Raulston JE. Identification of iron-responsive proteins expressed by Chlamydia trachomatis reticulate bodies during intracellular growth. Microbiology. 2009;155:210-219.
24. Sokol PA. Surface expression of ferripyochelin-binding protein is required for virulence of Pseudomonas aeruginosa. Infect Immun. 1987;55:2021-2025.
25. Mevissen-Verhage EA, Marcelis JH, Vos MN, etal. Bifidobacterium, Bacteroides, and Clostridium spp. in fecal samples from breast-fed and bottle-fed infants with and without iron supplements. J Clin Microbiol. 1987;25:285-289.
26. Bliss JM, Basavegowda KP, Watson WJ, etal. Vertical and horizontal transmission of Candida albicans in very low birth weight infants using DNA fingerprinting techniques. Pediatr Infect Dis J. 2008;27:231-235.
27. Jarosik GP, Land CB. Identification of a human lactoferrin-binding protein in Gardnerella vaginalis. Infect Immun. 2000;68:3443-3447.
28. Rodrigues MM, Fernandes PA, Haddad JP, etal. Frequency of Chlamydia trachomatis, Neisseria gonorrhoeae, Mycoplasma genitalium, Mycoplasma hominis and Ureaplasma species in cervical samples. J Obstet Gynaecol. 2011;31:237-241.
29. Lehker MW, Alderete JF. Iron regulates growth of Trichomonas vaginalis and the expression of immunogenic trichomonad proteins. Mol Microbiol. 1992;6:123-132.
30. Dimier IH, Bout DT. Interferon-gamma-activated primary enterocytes inhibit Toxoplasma gondii replication: a role for intracellular iron. Immunology. 1998;94:488-495.
31. Ratledge C. Iron, mycobacteria and tuberculosis. Tuberculosis (Edinb). 2004;84:110-130.
32. Pfisterer C, Faber R, Horn LC. Chorioamnionitis-induced changes of fetal extramedullar hematopoeisis in the second trimester of gestation. Is diagnosis from fetal autopsy possible? Virchows Arch. 2005;446:150-156.
33. McClure E, Dudley DJ, Reddy UM, etal. Infectious causes of stillbirth: a clinical perspective. Clin Obstet Gynecol. 2010;53:635-645.
34. Folgosa E, Gonzalez C, Osman NB, etal. A case control study of chorioamniotic infection and histological choriamnionitis in stillbirth. APMIS. 1997;105:329-336.
35. Zaidi AK, Thaver D, Ali SA, etal. Pathogens associated with sepsis in newborns and young infants in developing countries. Pediatr Infect Dis J. 2009;28(Suppl 1):S10-S18.
36. Van Geertruyden JP, Thomas F, Erhart A, etal. The contribution of malaria in pregnancy to perinatal mortality. Am J Trop Med Hyg. 2004;71:35-40.
37. Goldenberg RL, Andrews WW, Hauth JC. Choriodecidual infection and preterm birth. Nutr Rev. 2002;60(Suppl 5):S19-S25.
38. Leitich J, Bodner-Adler B, Brunbauer M, etal. Bacterial vaginosis as a risk factor for preterm delivery: a meta-analysis. Am J Obstet Gynecol. 2003;189:139-147.
39. Koumans E, Markowitz LE, Hogan V for the CDC BV Working Group. Indications for therapy and treatment recommendations for bacterial vaginosis in nonpregnant and pregnant women: a synthesis of data. Clin Infect Dis. 2002;35(Suppl 2):S152-S172.
40. Hay PE, Morgan DJ, Ison CA, etal. A longitudinal study of bacterial vaginosis during pregnancy. Br J Obstet Gynaecol. 1994;101:1048-1053.
41. Donders GG, Van Calsteren K, Bellen G, etal. Predictive value for preterm birth of abnormal vaginal flora, bacterial vaginosis and aerobic vaginitis during the first trimester of pregnancy. Br J Obstet Gynaecol. 2009;116:1315-1324.
42. Romero R, Oyarzun E, Mazor M, etal. Meta-analysis of the relationship between asymptomatic bacteriuria and preterm delivery/low birth weight. Obstet Gynecol. 1989;73:576-582.
43. Villar J, Gülmezoglu AM, de Onis M. Nutritional and antimicrobial interventions to prevent preterm birth: an overview of randomized controlled trials. Obstet Gynecol Surv. 1998;53:575-585.
44. Munn MB, Groome LJ, Atterbury JL, etal. Pneumonia as a complication of pregnancy. J Matern Fetal Med. 1999;8:151-154.
45. Ormerod P. Tuberculosis in pregnancy and the puerperium. Thorax. 2001;54:494-499.
46. Brabin BJ, Romagosa C, Abdelgalil S, etal. The sick placenta - the role of malaria. Placenta. 2004;25:359-378.
47. Hammerschlag MR. Chlamydial infections. J Pediatr. 1989;114:727-734.
48. Valkenburg-van den Berg AW, Houtman-Roelofsen RL, Oostvogel PM, etal. Timing of Group B streptococcus screening in pregnancy: a systematic review. Gynecol Obstet Invest. 2010;69:174-183.
49. Sterkers Y, Pratlong F, Albaba S, etal. Novel interpretation of molecular diagnosis of congenital toxoplasmosis according to gestational age at the time of maternal infection. J Clin Microbiol. 2012;50:3944-3951.
50. Senior K. Antenatal screening for group B streptococcus. Lancet Infect Dis. 2012;12:589-590.
51. Blatt AJ, Lieberman JM, Hoover DR, etal. Chamydial and gonococcal testing during pregnancy in the United States. Am J Obstet Gynecol. 2012;207:e1-e8.
52. Rasmussen KM. Is there a causal relationship between iron deficiency or iron-deficiency anemia and weight at birth, length of gestation and perinatal mortality? J Nutr. 2001;131:S590-S601.
53. McCaw-Binns A, Greenwood R, Ashley D, etal. Antenatal and perinatal care in Jamaica: do they reduce perinatal death rates? Paediatr Perinat Epidemiol. 1994;8(Suppl 1):86-97.
54. Christian P, West KP, Khatry SK, etal. Effects of maternal micronutrient supplementation on fetal loss and infant mortality: a cluster-randomized trial in Nepal. Am J Clin Nutr. 2003;78:1194-1202.
55. Hemminki E, Rimpelä U. A randomized comparison of routine versus selective iron supplementation during pregnancy. J Am Coll Nurs. 1991;10:3-10.
56. Ziaei S, Norrozi M, Faghihzadeh S, etal. A randomised placebo-controlled trial to determine the effect of iron supplementation on pregnancy outcome in pregnant women with haemoglobin ≥13.2g/dL. Br J Obstet Gynaecol. 2007;1145:684-688.
57. Zeng L, Dibley MJ, Cheng Y, etal. Impact of micronutrient supplementation during pregnancy on birth weight, duration of gestation, and perinatal mortality in rural western China: double blind cluster randomised controlled trial. BMJ. 2008;337:a2001.
58. Titaley CR, Dibley MJ, Roberts CL, etal. Iron and folic acid supplements and reduced early neonatal deaths in Indonesia. Bull World Health Organ. 2010;88:500-508.
59. Titaley CR, Dibley MJ, Roberts CL, etal. Combined iron/folic acid supplements and malaria prophylaxis reduce neonatal mortality in 19 sub-Saharan countries. Am J Clin Nutr. 2010;92:235-243.
60. Preziosi P, Prual A, Galan P, etal. Effect of iron supplementation on the iron status of pregnant women: consequences for newborns. Am J Clin Nutr. 1997;66:1178-1182.
61. Christian P, Shrestha J, LeClerq SC, etal. Supplementation with micronutrients does not further improve the hematologic status of pregnant women in rural Nepal. J Nutr. 2003;133:3492-3498.
62. Dibley MJ, Titaley CR, d'Este C, etal. Iron and folic acid supplements in pregnancy improve child survival in Indonesia. Am J Clin Nutr. 2012;95:220-230.
63. Ronsmans C, Fisher DJ, Osmond C, etal. for the Maternal Micronutrient Supplementation Group. Multiple micronutrient supplementation during pregnancy in low-income countries: a meta-analysis of effects on stillbirths and on early and late neonatal mortality. Food Nutr Bull. 2009;30(Suppl 4):S547-S555.
64. Shankar AH, Jahari AB, Sebayang SK, etal. Effect of maternal multiple micronutrient supplementation on fetal loss and infant death in Indonesia: a double-blind cluster-randomised trial. Lancet. 2008;371:215-227.
65. Peña Rosas JP, De-Regil LM, Dowswell T, etal. Intermittent oral iron supplementation during pregnancy. Cochrane Database Syst Rev. 2012;(7):CD009997.
66. Fleming AF, Ghatoura GB, Harrison KA, etal. The prevention of anaemia in pregnancy in primigravidae in the guinea savanna of Nigeria. Ann Trop Med Parasitol. 1986;80:211-233.
67. Menendez C, Todd J, Alonso PL, etal. The effects of iron supplementation during pregnancy, given by traditional birth attendants, on the prevalence of anaemia and malaria. Trans R Soc Trop Med Hyg. 1994;88:590-593.
68. Nacher M, McGready R, Stepniewska K, etal. Haematinic treatment of anaemia increases the risk of Plasmodium vivax malaria in pregnancy. Trans R Soc Trop Med Hyg. 2003;97:273-276.
69. Byles AB, D'sa A. Reduction of reaction due to iron dextran infusion using chloroquine. BMJ. 1970;3:625-627.
70. Oppenheimer SJ, MacFarlane SB, Moody JB, etal. Total dose of iron infusion, malaria and pregnancy in Papua New Guinea. Trans R Soc Trop Med Hyg. 1986;80:818-822.
71. Garn SM, Ridella SA, Petzold AS, etal. Maternal hematological levels and pregnancy outcomes. Semin Perinatol. 1981;5:155-162.
72. Murphy JF, O'Riordan J, Newcombe RG, etal. Relation of haemoglobin levels in first and second trimesters to outcome of pregnancy. Lancet. 1986;327:992-995.
73. Zhou L-M, Yang W-W, Hua J-Z, etal. Relation of hemoglobin measured at different times in pregnancy to preterm birth and low birth weight in Shanghai, China. Am J Epidemiol. 1998;148:998-1006.
74. Scanlon KS, Yip R, Schieve LA, etal. High and low hemoglobin levels during pregnancy: differential risks for preterm birth and small for gestational age. Obstet Gynecol. 2000;96:741-748.
75. Stephansson O, Dickman PW, Johansson A, etal. Maternal hemoglobin concentration during pregnancy and risk of stillbirth. JAMA. 2000;284:2611-2617.
76. Brabin BJ, Hakimi M, Pelletier D. An analysis of anemia and pregnancy-related maternal mortality. J Nutr. 2001;131:S604-S614.
77. Casanueva E, Viteri FE, Mares-Galindo M, etal. Weekly iron as a safe alternative to daily supplementation for nonanemic pregnant women. Arch Med Res. 2006;37:674-682.
78. Steer P, Alam MA, Wadsworth J, etal. Relation between maternal haemoglobin concentration and birth weight in different ethnic groups. BMJ. 1995;310:489-491.
79. Ribot B, Aranda N, Viteri F, etal. Depleted iron stores without anaemia early in pregnancy carries increased risk of lower birthweight even when supplemented daily with moderate iron. Hum Reprod. 2012;27:1260-1266.
80. Yip R. Significance of an abnormally low or high hemoglobin concentration during pregnancy: special consideration of iron nutrition. Am J Clin Nutr. 2000;72(Suppl):S272-S279.
81. Viteri FE, Casanueva E, Tolentino MC, etal. Antenatal iron supplements consumed daily produce oxidative stress in contrast to weekly supplementation in Mexican non-anemic women. Reprod Toxicol. 2012;34:125-132.
82. Scholl TO. High third-trimester ferritin concentration: associations with very preterm delivery, infection, and maternal nutritional status. Obstet Gynecol. 1998;92:161-166.
83. Verstraelen H, Delanghe J, Roelens K, etal. Subclinical iron deficiency is a strong predictor of bacterial vaginosis in early pregnancy. BMC Infect Dis. 2005;5:55.
84. Kortman GA, Boleij A, Swinkels DW, etal. Iron availability increases the pathogenic potential of Salmonella typhimurium and other enteric pathogens at the intestinal epithelial interface. PLoS ONE. 2012;7:e29968.
85. Paradkar PN, De Domenico I, Durchfort N, etal. Iron depletion limits intracellular bacterial growth in macrophages. Blood. 2008;112:866-874.
86. Ganz T, Nemeth E. Hepcidin and iron homeostasis. Biochim Biophys Acta. 2012;1823:1434-1443.
87. Evastatiev R, Gasche C. Iron sensing and signaling. Gut. 2012;61:933-952.
88. Young MF, Griffin J, Pressman E, etal. Maternal hepcidin is associated with placental transfer of iron derived from dietary heme and nonheme sources. J Nutr. 2012;142:33-39.
89. Rehu M, Punnonen K, Ostland V, etal. Maternal serum hepcidin is low at term and independent of cord blood iron status. Eur J Haematol. 2010;85:345-352.
90. Finberg KE. Unraveling mechanisms regulating systemic iron homeostasis. Hematology Am Soc Hematol Educ Program. 2011;2011:532-537.
91. Nairz M, Theurl I, Schroll A, etal. Absence of functional Hfe protects mice from invasive Salmonella enteritica serovar Typhimurium infection via induction of lipocalin-2. Blood. 2009;114:3642-3651.
92. Liu XB, Hill P, Haile DJ. Role of the ferroportin iron-responsive element in iron and nitric oxide dependent gene regulation. Blood Cells Mol Dis. 2002;29:315-326.
93. Gyarmati B, Szabó E, Szalay B, etal. Serum maternal hepcidin levels 3 days after delivery are higher compared to those measured at parturition. J Obstet Gynaecol Res. 2011;37:1620-1624.
94. Byrd TF, Horwitz MA. Interferon gamma-activated human monocytes downregulate transferrin receptors and inhibit the intracellular multiplication of Legionella pneumophila by limiting the availability of iron. J Clin Invest. 1989;83:1457-1465.
95. Boelart JR, Vandecasteele SJ, Appelberg R, etal. The effect of the host's iron status on tuberculosis. J Infect Dis. 2007;195:1745-1753.
96. Baker EN, Baker HM, Kidd RD. Lactoferrin and transferrin: functional variations on a common structural framework. Biochem Cell Biol. 2002;80:27-34.
97. Rebelo I, Carvalho-Guerra F, Pereira-Leite L, etal. Lactoferrin as a sensitive blood marker of neutrophil activation in normal pregnancies. Eur J Obstet Gynecol. 1995;62:189-194.
98. Freestone PP, Lyte M, Neal CP, etal. The mammalian neuroendocrine hormone norepinephrine supplies iron for bacteria growth in the presence of transferrin or lactoferrin. J Bacteriol. 2000;182:6091-6098.
99. Sandrini SM, Shergill R, Woodward J, etal. Elucidation of the mechanism by which catecholamine stress hormones liberate iron from the innate immune defence proteins transferrin and lactoferrin. J Bacteriol. 2010;192:587-594.
100. Lyte M, Vulchanova L, Brown DR. Stress at the intestinal surface: catecholamines and mucosa-bacteria interactions. Cell Tissue Res. 2011;343:23-32.
101. Teng CT, Beard C, Gladwell W. Differential expression and estrogen response of lactoferrin gene in the female reproductive tract of mouse, rat, and hamster. Biol Reprod. 2002;67:1439-1449.
102. Teng CT. Factors regulating lactoferrin gene expression. Biochem Cell Biol. 2006;84:263-267.
103. Cohen MS, Britigan BE, French M, etal. Preliminary observations on lactoferrin secretion in human vaginal mucus: variation during the menstrual cycle, evidence of hormonal regulation, and implications for infection with Neisseria gonorrhoeae. Am J Obstet Gynecol. 1987;157:1122-1125.
104. Goldenberg RL, Andrews WW, Guerrant RL, etal. for the National Institute of Child Health and Human Development Maternal-Fetal Medicine Units Network. The Preterm Prediction Study: cervical lactoferrin concentration, other markers of lower genital tract infection, and preterm birth. Am J Obstet Gynecol. 2000;182:631-635.
105. Tang LJ, De Seta F, Odreman F, etal. Proteomic analysis of human cervical-vaginal fluids. J Proteome Res. 2007;6:2874-2883.
106. Koczura R, Kaznowski A. The Yersinia high-pathogenicity island and iron uptake systems in clinical isolates of Escherichia coli. J Med Microbiol. 2003;52:637-642.
107. Pereira L, Reddy AP, Jacob T, etal. Identification of novel protein biomarkers of preterm birth in human cervical-vaginal fluid. J Proteome Res. 2007;6:1269-1276.
108. Legrand D, Mazurier J. A critical review of the roles of host lactoferrin in immunity. Biometals. 2010;23:365-376.
109. Aroutcheva A, Ling Z, Faro S. Prevotella bivia as a source of lipopolysaccharide in the vagina. Anaerobe. 2008;14:256-260.
110. Otsuki K, Yoda A, Toma Y, etal. Lactoferrin and interleukin-6 interactions in amniotic infection. Adv Exp Med Biol. 1998;443:267-271.
111. Otsuki K, Yakuwa K, Sawada M, etal. Recombinant lactoferrin has preventive effects on lipopolysaccharide-induced preterm delivery and production of inflammatory cytokines in mice. J Perinat Med. 2005;33:320-323.
112. Flo TH, Smith KD, Sato S, etal. Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron. Nature. 2004;432:917-921.
113. Miethke M, Skerra A. Neutrophil gelatinase-associated lipocalin expresses antimicrobial activity by interfering with L-norepinephrine-mediated bacterial iron acquisition. Antimicrob Agents Chemother. 2010;54:1580-1589.
114. Tadesse S, Luo G, Park JS, etal. Intra-amniotic infection upregulates neutrophil gelatinase-associated lipocalin (NGAL) expression at the maternal-fetal interface at term: implications for infection-related preterm birth. Reprod Sci. 2011;18:713-722.
115. Goetz DH, Holmes MA, Borregaard N, etal. The neutrophil lipocalin NGAL is a bacteriostatic agent that interferes with siderophore-mediated iron acquisition. Mol Cell. 2002;10:1033-1043.
116. Brown JS, Holden DW. Iron acquisition by gram-positive bacterial pathogens. Microbes Infect. 2002;4:1149-1156.
117. Garcia EC, Brumbaugh AR, Mobley HL. Redundancy and specificity of Escherichia coli iron acquisition systems during urinary tract infection. Infect Immun. 2011;79:1225-1235.
118. Posey JE, Gherardini FC. Lack of a role for iron in the Lyme disease pathogen. Science. 2000;288:1651-1653.
119. McLaughlin HP, Hill C, Gahan CG. The impact of iron on Listeria monocytogenes; inside and outside the host. Curr Opin Biotechnol. 2011;22:194-199.
120. Brown MR, Allison DG, Gilbert P. Resistance of bacterial biofilms to antibiotics: a growth-related effect? J Antimicrob Chemother. 1988;22:777-780.
121. Singh PK, Parsek MR, Greenberg EP, etal. A component of innate immunity prevents bacterial biofilm development. Nature. 2002;417:552-555.
122. Swidsinski A, Mendling W, Loening-Baucke V, etal. Adherent biofilms in bacterial vaginosis. Obstet Gynecol. 2005;106:1013-1023.
123. Verstraelen H, Swidsinski A. The biofilm in bacterial vaginosis: implications for epidemiology, diagnosis and treatment. Current Opin Infect Dis. 2013;26:86-89.
124. Macklaim JM, Gloor GB, Anukam KC, etal. At the crossroads of vaginal health and disease, the genome sequence of Lactobacillus iners AB-1. Proc Natl Acad Sci U S A. 2011;108:4688-4695.
125. Jarosik GP. Identification of a Gardnerella vaginalis hemoglobin-binding protein. Curr Microbiol. 2001;42:49-52.
126. Yeoman CJ, Yildirim S, Thomas SM, etal. Comparative genomics of Gardnerella vaginalis strains reveals substantial differences in metabolic and virulence potential. PLoS One. 2010;5:e12411.
127. Rohde KH, Dyer DW. Mechanisms of iron acquisition by the human pathogens Neisseria meningitidis and Neisseria gonorrhoeae. Front Biosci. 2003;8:1186-1218.
128. Noinaj N, Easley NC, Oke M, etal. Structural basis for iron piracy by pathogenic Neisseria. Nature. 2012;483:53-58.
129. Igietseme JU, Ananaba GA, Candal DH, etal. Immune control of chlamydial growth in the human epithelial cell line RT4 involves multiple mechanisms that include nitric oxide induction, tryptophan catabolism and iron deprivation. Microbiol Immunol. 1998;42:617-625.
130. Al-Younes HM, Rudel T, Brinkmann V, etal. Low iron availability modulates the course of Chlamydiae pneumoniae infection. Cell Microbiol. 2001;3:427-437.
131. Vancini RG, Benchimol M. Entry and intracellular location of Mycoplasma hominis in Trichomonas vaginalis. Arch Microbiol. 2008;189:7-18.
132. Clancy A, Loar JW, Speziali CD, etal. Evidence for siderophore-dependent iron acquisition in group B streptococcus. Mol Microbiol. 2006;59:707-721.
133. Borges SF, Silva JG, Teixeira PC. Survival and biofilm formation of Listeria monocytogenes in simulated vaginal fluid: influence of pH and strain origin. FEMS Immunol Med Microbiol. 2011;62:315-320.
134. Cotch MF, Pastorek JG, Nugent RP, etal. Trichomonas vaginalis associated with low birth weight and preterm delivery. The Vaginal Infections and Prematurity Study Group. Sex Transm Dis. 1997;24:353-360.
135. Leitsch D, Kolarich D, Duchêne M. The flavin inhibitor diphenyleneiodonium renders Trichomonas vaginalis resistant to metronidazole, inhibits thioredoxin reductase and flavin reductase, and shuts off hydrogenosomal enzymatic pathways. Mol Biochem Parasitol. 2010;171:17-24.
136. Peterson KM, Alderete JF. Iron uptake and increased intracellular enzyme activity follow host lactoferrin binding by Trichomonal vaginalis receptors. J Exp Med. 1984;160:398-410.
137. De Mast Q, Nadjm B, Reyburn H, etal. Assessment of urinary concentrations of hepcidin provides novel insight into disturbances in iron homeostasis during malarial infection. J Infect Dis. 2009;199:253-262.
138. Portugal S, Carret C, Recker M, etal. Host-mediated regulation of superinfection in malaria. Nat Med. 2011;17:732-737.
139. Kabyemela ER, Fried M, Kurtis JD, etal. Decreased susceptibility to Plasmodium falciparum infection in pregnant women with iron deficiency. J Infect Dis. 2008;198:163-166.
140. Senga EL, Harper G, Koshy G, etal. Reduced risk for placental malaria in iron deficient women. Malar J. 2011;10:47.
141. Choi JW, Kim CS, Pai SH. Erythopoietic activity and soluble transferrin receptor levels in neonates and maternal blood. Acta Paediatr. 2000;89:675-679.
142. McArdle HJ, Lang C, Hayes H, etal. Role of the placenta in regulation of fetal iron status. Nutr Rev. 2011;69(Suppl 1):S17-S22.
143. Balesaria S, Hanif R, Salama MF, etal. Fetal iron levels are regulated by maternal and fetal Hfe genotype and dietary iron. Haematologica. 2012;97:661-669.
144. Baker RD, Greer FR, and the Committee on Nutrition American Academy of Pediatrics. Diagnosis and prevention of iron deficiency and iron-deficiency anemia in infants and young children (0-3 years of age). Pediatrics. 2010;126:1040-1050.
145. Chockalingam UM, Murphy E, Ophoven JC, etal. Cord transferrin and ferritin values in newborn infants at risk for prenatal uteroplacental insufficiency and chronic hypoxia. J Pediatr. 1987;111:283-286.
146. Siddappa AM, Rao R, Long JD, etal. The assessment of newborn iron stores at birth: a review of the literature and standards for ferritin concentrations. Neonatology. 2007;92:73-82.
147. Evans PJ, Evans R, Kovar IZ, etal. Bleomycin-detectable iron in the plasma of premature and full-term neonates. FEBS Lett. 1992;303:210-212.
148. Buonocore G, Perrone S, Bracci R. Free radicals and brain damage in the newborn. Biol Neonate. 2001;79:180-186.
149. Rao R, Georgieff MK. Iron therapy for preterm infants. Clin Perinatol. 2009;36:27-42.
150. Mills RJ, Davies MW. Enteral iron supplementation in preterm and low birth weight infants. Cochrane Database Syst Rev. 2012;(3):CD005095.
151. Ojukwu JU, Okebe JU, Yahav D, etal. Oral iron supplementation for preventing and treating anaemia among children in malaria-endemic areas. Cochrane Database Syst Rev. 2011;(10): CD006589.
152. Oppenheimer SJ. Iron and its relation to immunity and infectious disease. J Nutr. 2001;131:S616-S633.
153. Barry DM, Reeve AW. Increased incidence of gram-negative neonatal sepsis with intramuscular iron administration. Pediatrics. 1977;60:908-912.
154. Levine RL, Lemons JA. Letter: Concentrations of serum iron in relation to infection in the neonate. J Pediatr. 1975;87:331-332.
155. Becroft DM, Dix MR, Farmer K. Intramuscular iron dextran and susceptibility of neonates to bacterial infections. In vitro studies. Arch Dis Child. 1977;52:778-781.
156. Juul S, Zerzan JC, Strandjord TP, etal. Zinc protoporphyrin/heme as an indicator of iron status in NICU patients. J Pediatr. 2003;142:273-278.
157. Bardaji A, Sigauque B, Sanz S, etal. Impact of malaria at the end of pregnancy on infant mortality and morbidity. J Infect Dis. 2011;203:691-699.
158. Schwarz NG, Adegnika AA, Breitling LP, etal. Placental malaria increases malaria risk in the first 30 months of life. Clin Infect Dis. 2008;47:1017-1025.
159. Malhotra I, Dent A, Mungai P, etal. Can prenatal malaria exposure produce an immune tolerant phenotype?: A prospective birth cohort study in Kenya. PLoS Med. 2009;6:e1000116.
160. Hartman TK, Rogerson SJ, Fischer PR. The impact of maternal malaria on newborns. Ann Trop Paediatr. 2010;30:271-282.
161. Brabin BJ. An analysis of malaria parasite rates in infants: 40 years after Macdonald. Trop Dis Bull. 1990;87:R1-R21.
162. Riley EM, Wagner GE, Akanmori BD, etal. Do maternally acquired antibodies protect infants from malaria infection? Parasite Immunol. 2001;23:51-59.
163. D'Alessandro U, Ubben D, Hamed K, etal. Malaria in infants aged less than six months - is it an area of unmet medical need? Malar J. 2012;11:400.
164. Le Cessie S, Verhoeff FH, Mengistie G, etal. Changes in haemoglobin levels in infants in Malawi: effect of low birth weight and fetal anaemia. Arch Dis Child Fetal Neonatal Ed. 2002;86:F182-F187.
165. Brabin BJ, Kalanda BF, Verhoeff FH, etal. Risk factors for fetal anaemia in a malarious area of Malawi. Ann Trop Paediatr. 2004;24:311-321.
166. Prus E, Fibach E. The labile iron pool in human erythroid cells. Br J Haematol. 2008;142:301-307.
167. Gwamaka M, Kurtis JD, Sorensen BE, etal. Iron deficiency protects against severe Plasmodium falciparum malaria and death in young children. Clin Infect Dis. 2012;54:1137-1144.
168. Jonker FA, Calis JC, Boele van Hensbroek MB, etal. Iron status predicts malaria risk in Malawian preschool children. PLoS One. 2012;7:e42670.
169. Portugal S, Drakesmith H, Mota MM. Superinfection in malaria: Plasmodium shows its iron will. EMBO Rep. 2011;12:1233-1242.
170. Maltha J, Jacobs J. Iron deficiency and malaria mortality: possible implication of invasive bacterial diseases. Clin Infect Dis. 2012;55:748.
171. Ter Kuile FO, Van Eijk AM, Filler SJ. Effect of sulfadoxine-pyrimethamine resistance on the efficacy of preventive therapy for malaria control during pregnancy. JAMA. 2007;297:2603-2616.
172. Van Eijk AM, Hill J, Alegana VA, etal. Coverage of malaria protection in pregnant women in sub-Saharan Africa: a synthesis and analysis of national survey data. Lancet Infect Dis. 2011;11:190-207.
173. Hancock V, Ferrières L, Klemm P. The ferric yersiniabactin uptake receptor FyuA is required for efficient biofilm formation by urinary tract infectious Escherichia coli in human urine. Microbiology. 2008;154:167-175.
174. Ishida S, Arai M, Niikawa H, etal. Inhibitory effect of cyclic trihydroxamate siderophore, desferrioxamine E, on the biofilm formation of Mycobacterium species. Biol Pharm Bull. 2011;34:917-920.
175. Gordeuk VR, Loyevsky M. Antimalarial effects of iron chelators. Adv Exp Med Biol. 2002;509:251-257.
176. Weinberg ED. Iron availability and infection. Biochim Biophys Acta. 2009;1790:600-605.
177. Alteri CJ, Hagan EC, Sivick KE, etal. Mucosal immunization with iron receptor antigens protects against urinary tract infection. PLoS Pathog. 2009;5:e1000586.
178. Lao TT, Tam K-F, Chan LY. Third trimester iron status and pregnancy outcome in non-anaemic women; pregnancy unfavourably affected by maternal iron excess. Hum Reprod. 2000;15:1843-1848.
179. Senga E, Koshy G, Brabin BJ. Zinc erythrocyte protoporphyrin as a marker of malaria risk in pregnancy - a retrospective cross-sectional and longitudinal study. Malar J. 2012;11:249.
180. Sazawal S, Black RE, Ramsan M, etal. Effects of routine prophylactic supplementation with iron and folic acid on admission to hospital and mortality in preschool children in a high malaria transmission setting: community-based, randomised, placebo-controlled trial. Lancet. 2006;367:133-143. Erratum in: Lancet 2006;367:302.
181. Actor JK, Hwang S-A, Kruzel ML. Lactoferrin as a natural immune modulator. Curr Pharm Des. 2009;15:1956-1973.
182. Nappi C, Tommaselli GA, Morra I, etal. Efficacy and tolerability of oral bovine lactoferrin compared to ferrous sulfate in pregnant women with iron deficiency anemia: a prospective controlled randomized study. Acta Obstet Gynecol Scand. 2009;88:1031-1035.
183. Nibbering PH, Ravensbergen E, Welling MM, etal. Human lactoferrin and peptides are highly effective against infections with antibiotic-resistant bacteria. Infect Immun. 2001;69:1469-1476.
184. Manzoni P, Rinaldi M, Cattani S, etal. Bovine lactoferrin supplementation for prevention of late-onset sepsis in very low-birth-weight neonates: a randomised trial. JAMA. 2009;302:1421-1428.
185. Ward PP, Conneely OM. Lactoferrin: role in iron homeostasis and host defence against microbial infection. Biometals. 2004;17:203-208.
186. Pammi M, Abrams SA. Oral lactoferrin for the prevention of sepsis and necrotizing enterocolitis in preterm infants. Cochrane Database Syst Rev. 2011;(10):CD007137.
187. Tarnow-Mordi W, Isaacs D, Dutta S. Adjunctive immunologic interventions in neonatal sepsis. Clin Perinatol. 2010;37:481-499.