Supplementation of mice with specific nondigestible oligosaccharides during pregnancy or lactation leads to diminished sensitization and allergy in the female offspring

Journal of Nutrition

Volumn 145, Issue 5, 2015, Pages 996-1002

  Hogenkamp, Astrid ^a   Knippels, Leon M J ^a,b   Garssen, Johan ^a,b   Van Esch, Betty C A M ^a,b  

^a UTRECHT UNIVERSITY   (Netherlands)

^b Nutricia Nederland   (Netherlands)

Author keywords

Food allergy; Hen's egg; Maternal dietary intervention; Oligosaccharides; Programming

Indexed keywords

CARBOHYDRATE DERIVATIVE; CHOLERA TOXIN; FRUCTOSE OLIGOSACCHARIDE; GALACTOSE OLIGOSACCHARIDE; IMMUNOGLOBULIN; LONG CHAIN FRUCTO OLIGOSACCHARIDE; OLIGOSACCHARIDE; OVALBUMIN; PECTIN DERIVED ACIDIC OLIGOSACCHARIDE; SHORT CHAIN GALACTO OLIGOSACCHARIDE; UNCLASSIFIED DRUG; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G;

ACUTE ALLERGIC SKIN RESPONSE; ANAPHYLAXIS; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BLOOD SAMPLING; BODY TEMPERATURE; CONTROLLED STUDY; DIET SUPPLEMENTATION; DIETARY INTAKE; FEMALE; FLOW CYTOMETRY; FOOD; FOOD ALLERGY; IMMUNOGLOBULIN BLOOD LEVEL; LACTATION; MALE; MATING; MESENTERY LYMPH NODE; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PREGNANCY; PROGENY; QUANTITATIVE ANALYSIS; REGULATORY T LYMPHOCYTE; SENSITIZATION; SKIN ALLERGY; SPLEEN; SYMPTOM; TH1 CELL; WEANING; ANIMAL; ANTIBODY SPECIFICITY; BIOSYNTHESIS; BLOOD; C3H MOUSE; COMPARATIVE STUDY; DIETARY FIBER; DISEASE MODEL; EGG HYPERSENSITIVITY; FETUS DEVELOPMENT; GERMFREE ANIMAL; HELPER CELL; IMMUNOLOGY; MATERNAL NUTRITION; METABOLISM; RANDOMIZATION; SKIN; THERAPEUTIC USE;

MUS;

ANIMALS; ANTIBODY SPECIFICITY; DIETARY FIBER; DIETARY SUPPLEMENTS; DISEASE MODELS, ANIMAL; EGG HYPERSENSITIVITY; FEMALE; FETAL DEVELOPMENT; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G; LACTATION; MATERNAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; MICE, INBRED C3H; OLIGOSACCHARIDES; OVALBUMIN; PREGNANCY; RANDOM ALLOCATION; SKIN; SPECIFIC PATHOGEN-FREE ORGANISMS; SPLEEN; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 84929472826     PISSN: 00223166     EISSN: 15416100     Source Type: Journal    
DOI: 10.3945/jn.115.210401     Document Type: Article

References (37)

1. Lim RH, Kobzik L, Dahl M. Risk for asthma in offspring of asthmatic mothers versus fathers: a meta-analysis. PLoS ONE 2010;5:e10134.
2. Lim RH, Kobzik L. Maternal transmission of asthma risk. Am J Reprod Immunol 2009;61:1-10.
3. Leme AS, Hubeau C, Xiang Y, Goldman A, Hamada K, Suzaki Y, Kobzik L. Role of breast milk in a mouse model of maternal transmission of asthma susceptibility. J Immunol 2006;176:762-9.
4. Guilbert TW, Stern DA, Morgan WJ, Martinez FD, Wright AL. Effect of breastfeeding on lung function in childhood and modulation by maternal asthma and atopy. Am J Respir Crit Care Med 2007;176:843-8.
5. Wright AL, Holberg CJ, Taussig LM, Martinez FD. Factors influencing the relation of infant feeding to asthma and recurrent wheeze in childhood. Thorax 2001;56:192-7.
6. DesRoches A, Infante-Rivard C, Paradis L, Paradis J, Haddad E. Peanut allergy: is maternal transmission of antigens during pregnancy and breastfeeding a risk factor? J Investig Allergol Clin Immunol 2010;20:289-94.
7. Kirsten TB, de Oliveira BP, de Oliveira AP, Kieling K, de Lima WT, Palermo-Neto J, Bernardi MM. Single early prenatal lipopolysaccharide exposure prevents subsequent airway inflammation response in an experimental model of asthma. Life Sci 2011;89:15-9.
8. Hansen JS, Nygaard UC, Lyle R, Lovik M. Early life interventions to prevent allergy in the offspring: the role of maternal immunization and postnatal mucosal allergen exposure. Int Arch Allergy Immunol 2012;158:261-75.
9. Hourihane JO, Aiken R, Briggs R, Gudgeon LA, Grimshaw KE, DunnGalvin A, Roberts SR. The impact of government advice to pregnant mothers regarding peanut avoidance on the prevalence of peanut allergy in United Kingdom children at school entry. J Allergy Clin Immunol 2007;119:1197-202.
10. Wennergren G. What if it is the other way around? Early introduction of peanut and fish seems to be better than avoidance. Acta Paediatr 2009;98:1085-7.
11. van Vlies N, Hogenkamp A, Fear AL, van Esch BCAM, Oosting A, van de Heijning B, van der Beek PC, Calder PC, Garssen J. Perinatal programming of murine immune responses by polyunsaturated fatty acids. JDOHaD 2011;2:112-23.
12. Schabussova I, Hufnagl K, Tang ML, Hoflehner E,Wagner A, Loupal G, Nutten S, Zuercher A, Mercenier A, Wiedermann U. Perinatal maternal administration of Lactobacillus paracasei NCC 2461 prevents allergic inflammation in a mouse model of birch pollen allergy. PLoS ONE 2012;7:e40271.
13. Furuhjelm C, Warstedt K, Larsson J, Fredriksson M, Bottcher MF, Falth-Magnusson K, Duchen K. Fish oil supplementation in pregnancy and lactation may decrease the risk of infant allergy. Acta Paediatr 2009;98:1461-7.
14. Rautava S, Kainonen E, Salminen S, Isolauri E. Maternal probiotic supplementation during pregnancy and breast-feeding reduces the risk of eczema in the infant. J Allergy Clin Immunol 2012;130:1355-60.
15. Palmer DJ, Sullivan T, Gold MS, Prescott SL, Heddle R, Gibson RA, Makrides M. Randomized controlled trial of fish oil supplementation in pregnancy on childhood allergies. Allergy 2013;68:1370-6.
16. Boehm G, Stahl B, Jelinek J, Knol J, Miniello V, Moro GE. Prebiotic carbohydrates in human milk and formulas. Acta Paediatr Suppl 2005;94:18-21.
17. Shen Q, Tuohy KM, Gibson GR, Ward RE. In vitro measurement of the impact of human milk oligosaccharides on the faecal microbiota of weaned formula-fed infants compared to a mixture of prebiotic fructooligosaccharides and galactooligosaccharides. Lett Appl Microbiol 2011;52:337-43.
18. Haarman M, Knol J. Quantitative real-time PCR analysis of fecal Lactobacillus species in infants receiving a prebiotic infant formula. Appl Environ Microbiol 2006;72:2359-65.
19. Fanaro S, Boehm G, Garssen J, Knol J, Mosca F, Stahl B, Vigi V. Galacto-oligosaccharides and long-chain fructo-oligosaccharides as prebiotics in infant formulas: a review. Acta Paediatr Suppl 2005;94: 22-6.
20. Fanaro S, Jelinek J, Stahl B, Boehm G, Kock R, Vigi V. Acidic oligosaccharides from pectin hydrolysate as new component for infant formulae: effect on intestinal flora, stool characteristics, and pH. J Pediatr Gastroenterol Nutr 2005;41:186-90.
21. Arslanoglu S, Moro GE, Schmitt J, Tandoi L, Rizzardi S, Boehm G. Early dietary intervention with a mixture of prebiotic oligosaccharides reduces the incidence of allergic manifestations and infections during the first two years of life. J Nutr 2008;138:1091-5.
22. Moro G, Arslanoglu S, Stahl B, Jelinek J, Wahn U, Boehm G. A mixture of prebiotic oligosaccharides reduces the incidence of atopic dermatitis during the first six months of age. Arch Dis Child 2006;91:814-9.
23. van Hoffen E, Ruiter B, Faber J, M'Rabet L, Knol EF, Stahl B, Arslanoglu S, Moro G, Boehm G, Garssen J. A specific mixture of shortchain galacto-oligosaccharides and long-chain fructo-oligosaccharides induces a beneficial immunoglobulin profile in infants at high risk for allergy. Allergy 2009;64:484-7.
24. Shadid R, Haarman M, Knol J, Theis W, Beermann C, Rjosk-Dendorfer D, Schendel DJ, Koletzko BV, Krauss-Etschmann S. Effects of galactooligosaccharide and long-chain fructooligosaccharide supplementation during pregnancy on maternal and neonatal microbiota and immunity-a randomized, double-blind, placebo-controlled study. Am J Clin Nutr 2007;86:1426-37.
25. Fujiwara R, Watanabe J, Sonoyama K. Assessing changes in composition of intestinal microbiota in neonatal BALB/c mice through cluster analysis of molecular markers. Br J Nutr 2008;99:1174-7.
26. Fujiwara R, Takemura N, Watanabe J, Sonoyama K. Maternal consumption of fructo-oligosaccharide diminishes the severity of skin inflammation in offspring of NC/Nga mice. Br J Nutr 2010;103:530-8.
27. van Vlies N, Hogenkamp A, Thijssen S, Dingjan GM, Knipping K, Garssen J, Knippels LM. Effects of short-chain galacto- and long-chain fructo-oligosaccharides on systemic and local immune status during pregnancy. J Reprod Immunol 2012;94:161-8.
28. Hogenkamp A, van Vlies N, Fear AL, van Esch BC, Hofman GA, Garssen J, Calder PC. Dietary fatty acids affect the immune system in male mice sensitized to ovalbumin or vaccinated with influenza. J Nutr 2011;141:698-702.
29. Li XM, Schofield BH, Huang CK, Kleiner GI, Sampson HA. A murine model of IgE-mediated cow's milk hypersensitivity. J Allergy Clin Immunol 1999;103:206-14.
30. Deurloo DT, van Esch BC, Hofstra CL, Nijkamp FP, van Oosterhout AJ. CTLA4-IgG reverses asthma manifestations in a mild but not in a more "severe" ongoing murine model. Am J Respir Cell Mol Biol 2001;25: 751-60.
31. Faber J, Vos P, Kegler D, van Norren K, Argiles JM, Laviano A, Garssen J, van Helvoort A. Beneficial immune modulatory effects of a specific nutritional combination in a murine model for cancer cachexia. Br J Cancer 2008;99:2029-36.
32. Fusaro AE, Brito CA, Victor JR, Rigato PO, Goldoni AL, Duarte AJ, Sato MN. Maternal-fetal interaction: preconception immunization in mice prevents neonatal sensitization induced by allergen exposure during pregnancy and breastfeeding. Immunology 2007;122:107-15.
33. Smit JJ, Willemsen K, Hassing I, Fiechter D, Storm G, van Bloois L, Leusen JH, Pennings M, Zaiss D, Pieters RH. Contribution of classic and alternative effector pathways in peanut-induced anaphylactic responses. PLoS ONE 2011;6:e28917.
34. Finkelman FD. Anaphylaxis: lessons from mouse models. J Allergy Clin Immunol 2007;120:506-15.
35. Fujiwara R, Sasajima N, Takemura N, Ozawa K, Nagasaka Y, Okubo T, Sahasakul Y, Watanabe J, Sonoyama K. 2,4-Dinitrofluorobenzeneinduced contact hypersensitivity response in NC/Nga mice fed fructooligosaccharide. J Nutr Sci Vitaminol (Tokyo) 2010;56:260-5.
36. Canani RB, Costanzo MD, Leone L, Bedogni G, Brambilla P, Cianfarani S, Nobili V, Pietrobelli A, Agostoni C. Epigenetic mechanisms elicited by nutrition in early life. Nutr Res Rev 2011;24:198-205.
37. Hogenkamp A, Thijssen S, van Vlies N, Garssen J. Supplementing pregnant mice with a specific mixture of nondigestible oligosaccharides reduces symptoms of allergic asthma in male offspring. J Nutr 2015;145: 640-6.