Impact of diet on the immunological microenvironment of the pregnant uterus and its relationship to allergic disease in the offspring

a review of the recent literature

Authors

  • Daniella Campelo Batalha Cox Moore Instituto Fernandes Figueira, Fundação Oswaldo Cruz
  • Pedro Xavier Elsas Instituto Fernandes Figueira, Fundação Oswaldo Cruz
  • Elisabeth Santos Maximiano Instituto Fernandes Figueira, Fundação Oswaldo Cruz
  • Maria Ignez Capella Gaspar Elsas Instituto Fernandes Figueira, Fundação Oswaldo Cruz

Keywords:

Allergy, Pregnancy, Diet, Immunology, Child

Abstract

Medical progress has reduced the mortality from infectious diseases in most countries, but allergic diseases have become more prevalent worldwide over the same period, especially in industrialized countries. This has prompted speculation that modern lifestyles have altered the relationship between heredity and environ- ment so as to promote development of an atopic phenotype when exposure to infection decreases. A healthy uterine microenvironment is known to favor Th2 lymphocyte development. However, some evidence suggests that persistence of the Th2 pattern of immunity directs the developing organism’s immune response towards a long-last- ing atopic phenotype. Even though the outcome also depends on other factors (such as infection, functional state of the intestinal microflora, and exposure to environmental allergens at times critical to development), it seems that the immune system during the perinatal period is responsive to interventions that are no longer effective in adulthood. We have reviewed the literature accessible through Medline to identify recent advances in the prevention of allergic disease through interventions in the fetal-maternal relationship. Diet seems to have a significant impact on the immunological profile of the pregnant uterus, as well as on the postnatal development of allergic disease in the offspring, as suggested by the effects of probiotic bacteria and by manipulations of the dietary content of polyunsaturated fatty acids and antioxidants. This highlights the need for further studies, in order to define the best intervention methods, the most appropriate time interval and the individu- als who will most likely benefit from them.

Downloads

Download data is not yet available.

Author Biographies

Daniella Campelo Batalha Cox Moore, Instituto Fernandes Figueira, Fundação Oswaldo Cruz

MD, MSc. Doctoral student in Children’s and Women’s Health, Department of Pediatrics, Instituto Fernandes Figueira, Fundação Oswaldo Cruz (Fiocruz), Rio de Janeiro, Brazil.

Pedro Xavier Elsas, Instituto Fernandes Figueira, Fundação Oswaldo Cruz

MD, PhD. Associate professor, Department of Immunology, Instituto de Microbiologia Professor Paulo de Góes, Universidade Federal do Rio de Janeiro (UFRJ), Rio de Janeiro, Brazil; Visiting Professor, Department of Medicine, Harvard Medical School, Boston, Massachusetts, United States.

Elisabeth Santos Maximiano, Instituto Fernandes Figueira, Fundação Oswaldo Cruz

PhD. Research fellow, Department of Pediatrics, Instituto Fernandes Figueira, Fundação Oswaldo Cruz (Fiocruz), Rio de Janeiro, Brazil.

Maria Ignez Capella Gaspar Elsas, Instituto Fernandes Figueira, Fundação Oswaldo Cruz

MD, PhD. Senior investigator, Department of Pediatrics, Instituto Fernandes Figueira, Fundação Oswaldo Cruz (Fiocruz), Rio de Janeiro, Brazil.

References

Warner JO, Pohunet P, Marguet C, Roche WR, Clough JB. Issues in understanding childhood asthma. J Allergy Clin Im- munol. 2000;105(2 Pt 2):S473-6.

Beasley R, Crane J, Lai CK Pearce N. Prevalence and etiology of asthma. J Allergy Clin Immunol. 2000;105(2 Pt 2):S466-72.

Strachan DP. Hay fever, hygiene, and household size. BMJ. 1989;299(6710):1259-60.

Warner JA, Jones CA, Williams TJ, Warner JO. Maternal programming in asthma and allergy. Clin Exp Allergy. 1998;28(Suppl 5):35-8; discussion 50-1.

Mossman TR, Cherwinski H, Bond MW, Giedlin MA, Coffman RL. Two types of murine helper T cell clone. I. Definition ac- cording to profiles of lymphokine activities and secreted proteins. J Immunol. 1986;136(7):2348-57.

Romagnani S. Th1 and Th2 in human diseases. Clin Immunol Immunopathol. 1996;80(3 Pt 1):225-35.

Rapoport MJ, Bistritzer T, Aharoni D, et al. TH1/TH2 cytokine secretion of first degree relatives of T1DM patients. Cytokine. 2005;30(5):219-27.

Legg JP, Hussain IR, Warner JA, Johnston SL, Warner JO. Type 1 and type 2 cytokine imbalance in acute respiratory syncytial virus bronchiolitis. Am J Respir Crit Care Med. 2003;168(6):633-9.

Wegmann TG, Lin H, Guilbert L, Mosmann TR. Bidirec- tional cytokine interactions in the maternal-fetal relationship: is successful pregnancy a TH2 phenomenon? Immunol Today. 1993;14(7):353-6.

Arck PC, Ferrick DA, Steele-Norwood D, et al. Murine T cell determination of pregnancy outcome. Cell Immunol. 1999;196(2):71-9.

Clark DA, Croitoru K. TH1/TH2,3 imbalance due to cytokine- producing NK, gammadelta T and NK-gammadelta T cells in murine pregnancy decidua in success or failure of pregnancy. Am J Reprod Immunol. 2001;45(5):257-65.

Warner JA, Warner JO. Early life events in allergic sensitisation. Br Med Bull. 2000;56(4):883-93.

Warner JA, Little SA, Pollock I, Longbottom JL, Warner JO. The influence of exposure to house dust mite, cat, pollen and fungal allergens in the home on primary sensitization in asthma. Pediatr Allergy Immunol. 1991;1:79-86.

Brown MA, Rad PY, Halonen MJ. Method of birth alters inter- feron-gamma and interleukin-12 production by cord blood mono- nuclear cells. Pediatr Allergy Immunol. 2003;14(2):106-11.

Liu CA, Wang CL, Chuang H, Ou CY, Hsu TY, Yang KD. Pre- natal prediction of infant atopy by maternal but not paternal total IgE levels. J Allergy Clin Immunol. 2003;112(5):899-904.

Jones CA, Warner JA, Warner JO. Fetal swallowing of IgE. Lancet. 1998;351(9119):1859.

Bieber T. Fc epsilon RI-expressing antigen-presenting cells: new players in the atopic game. Immunol Today. 1997;18(7):311-3.

van Gool CJ, Thijs C, Dagnelie PC, et al. Determinants of neo- natal IgE level: parity, maternal age, birth season and perinatal essential fatty acid status in infants of atopic mothers. Allergy. 2004;59(9):961-8.

Ruiz RG, Richards D, Kemeny DM, Price JF. Neonatal IgE: a poor screen for atopic disease. Clin Exp Allergy. 1991;21(4):467-72.

Jones AC, Miles EA, Warner JO, Colwell BM, Bryant TN, Warner JA. Fetal peripheral blood mononuclear cell proliferative responses to mitogenic and allergenic stimuli during gestation. Pediatr Allergy Immunol. 1996;7(3):109-16.

Daffos F, Forestier F, Grangeot-Keros L, et al. Prenatal diagnosis of congenital rubella. Lancet. 1984:2(8393):1-3.

Gill TJ 3rd, Repetti CF, Metlay LA, et al. Transplacental im- munization of the human fetus to tetanus by immunization of the mother. J Clin Invest. 1983;72(3):987-96.

Vance GH, Holloway JA. Early life exposure to dietary and inhalant allergens. Pediatr Allergy Immunol. 2002;13(Suppl 15):14-8.

Viscarello RR, Cullen MT, DeGennaro NJ, Hobbins JC. Fetal blood sampling in human immunodeficiency virus--seropositive women before elective midtrimester termination of pregnancy. Am J Obstetr Gynecol. 1992;167(4 Pt 1):1075-9.

Kilshaw PJ, Cant AJ. The passage of maternal dietary proteins into human breast milk. Int Arch Allergy Appl Immunol. 1984;75(1):8-15.

Szepfalusi Z, Pichler J, Elsasser S, et al. Transplacental prim- ing of the human immune system with environmental al- lergens can occur early in gestation. J Allergy Clin Immunol. 2000;106(3):530-6.

Spencer J, MacDonald TT, Finn T, Isaacson PG. The development of gut associated lymphoid tissue in the terminal ileum of fetal human intestine. Clin Exp Immunol. 1986;64(3):536-43.

Butland BK, Strachan DP, Anderson HR. Fresh fruit intake and asthma symptoms in young British adults: confounding of effect modification by smoking? Eur Respir J. 1999;13(4):744-50.

Langley-Evans S. Fetal programming of immune function and respiratory disease. Clin Exp Allergy. 1997;27(12):1377-9.

Kalliomaki M, Salminen S, Arvilommi H, Kero P, Koski- nen P, Isolauri E. Probiotics in primary prevention of atopic disease: a randomised placebo-controlled trial. Lancet. 2001;357(9262):1076-9.

Vaarala O. Immunological effects of probiotics with special refer- ence to lactobacilli. Clin Exp Allergy. 2003;33(12):1634-40.

Pohjavuori E, Viljanen M, Korpela R, et al. Lactobacillus GG effect in increasing IFN-gamma production in infants with cow’s milk allergy. J Allergy Clin Immunol. 2004;114(1):131-6.

Helin T, Haahtela S, Haahtela T. No effect of oral treatment with an intestinal bacterial strain, Lactobacillus rhamnosus (ATCC 53103), on birch-pollen allergy: a placebo-controlled double-blind study. Allergy. 2002;57(3):243-6.

Black PN, Sharpe S. Dietary fat and asthma: is there a connec- tion? Eur Respir J. 1997;10(1):6-12.

Devereux G, Seaton A. Diet as a risk factor for atopy and asthma. J Allergy Clin Immunol. 2005;115(6):1109-17; quiz 1118.

Woods RK, Thien FC, Abramson MJ. Dietary marine fatty acids (fish oil) for asthma. Cochrane Database Syst Rev. 2000;(2): CD001283.

Dunstan JA, Mori TA, Barden A, et al. Fish oil supplementa- tion in pregnancy modifies neonatal allergen-specific immune responses and clinical outcomes in infants at high risk of atopy: a randomized, controlled trial. J Allergy Clin Immunol. 2003;112(6):1178-84.

Kankaanpaa P, Nurmela K, Erkkila A, et al. Polyunsaturated fatty acids in maternal diet, breast milk, and serum lipid fatty acids of infants in relation to atopy. Allergy. 2001;56(7):633-8.

Soutar A, Seaton A, Brown K. Bronchial reactivity and dietary antioxidants. Thorax. 1997;52(2):166-70.

Bodner C, Godden D, Brown K, Little J, Ross S, Seaton A. Antioxi- dant intake and adult-onset wheeze: a case-control study. Aberdeen WHEASE Study Group. Eur Respir J. 1999;13(1):22-30.

Romieu I, Sienra-Monge JJ, Ramírez-Aguilar M, et al. Antioxi- dant supplementation and lung functions among children with asthma exposed to high levels of air pollutants. Am J Respir Crit Care Med. 2002;166(5):703-9.

Brown KM, Pickard K, Nicol F, Arthur JR. Selenium status and selenoprotein function in a Scottish population. Proc Nutr Soc. 1997;56:304A.

Fogarty A, Lewis S, Weiss S, Britton J. Dietary vitamin E, IgE concentrations, and atopy. Lancet. 2000;356(9241):1573-4.

Devereux G, Barker RN, Seaton A. Antenatal determinants of neonatal immune responses to allergens. Clin Exp Allergy. 2002;32(1):43-50.

Rubin RN, Navon L, Cassano PA. Relationship of serum antioxidants to asthma prevalence in youth. Am J Respir Crit Care Med. 2004;169(3):393-8.

Harik-Khan RI, Muller DC, Wise RA. Serum vitamin levels and the risk of asthma in children. Am J Epidemiol. 2004;159(4):351-7.

Seaton A, Devereux G. Diet, infection and wheezy illness: lessons from adults. Pediatr Allergy Immunol. 2000;11(Sup- pl 13):37-40.

Harik-Khan RI, Muller DC, Wise RA. Serum vitamin levels and the risk of asthma in children. Am J Epidemiol. 2004;159(4):351-7.

Arora P, Kumar V, Batra S. Vitamin A status in children with asthma. Pediatr Allergy Immunol. 2002;13(3):223-6.

Rubin RN, Navon L, Cassano PA. Relationship of serum antioxidants to asthma prevalence in youth. Am J Respir Crit Care Med. 2004;169(3):393-8.

Hanson M, Gluckman P, Bier D, et al. Report on the 2nd World Congress on Fetal Origins of Adult Disease, Brighton, U.K., June 7-10, 2003. Pediatr Res. 2004;55(5):894-7.

Barker DJ. Developmental origins of adult health and disease. J Epidemiol Community Health. 2004;58(2):114-5.

Holt PG, Jones CA. The development of the immune system during pregnancy and early life. Allergy. 2000;55(8):688-97.

Botto LD, Lisi A, Robert-Gnansia E, et al. International retro- spective cohort study of neural tube defects in relation to folic acid recommendations: are the recommendations working? BMJ. 2005;330(7491):571.

Downloads

Published

2006-09-09

How to Cite

1.
Moore DCBC, Elsas PX, Maximiano ES, Elsas MICG. Impact of diet on the immunological microenvironment of the pregnant uterus and its relationship to allergic disease in the offspring : a review of the recent literature. Sao Paulo Med J [Internet]. 2006 Sep. 9 [cited 2025 Oct. 16];124(5):298-303. Available from: https://periodicosapm.emnuvens.com.br/spmj/article/view/2256

Issue

Section

Updating Article