Skip to main content
Top
Published in: Allergy, Asthma & Clinical Immunology 1/2017

Open Access 01-12-2017 | Research

Dietary intake is associated with respiratory health outcomes and DNA methylation in children with asthma

Authors: L. Montrose, T. J. Ward, E. O. Semmens, Y. H. Cho, B. Brown, C. W. Noonan

Published in: Allergy, Asthma & Clinical Immunology | Issue 1/2017

Login to get access

Abstract

Background

Asthma is an increasingly common chronic disease among children, and data point toward a complex mechanism involving genetic, environmental and epigenetic factors. Epigenetic modifications such as DNA hypo- or hyper-methylation have been shown to occur in response to environmental exposures including dietary nutrients.

Methods

Within the context of the asthma randomized trial of indoor wood smoke (ARTIS) study, we investigated relationships between diet, asthma health measures, and DNA methylation. Asthma health measures included a quality of life instrument, diurnal peak flow variability (dPFV) and forced expiratory volume in the first second (FEV1). Dietary intake was assessed with a food frequency questionnaire. Methylation levels of LINE-1 repetitive element and two promoter CpG sites for interferon gamma (IFNγ, -186 and -54) from buccal cell DNA were measured using pyrosequencing assays.

Results

Data were collected on 32 children with asthma living in western Montana who were recruited to the ARTIS study. Selenium and several methyl donor dietary nutrients were positively associated with the asthma quality of life measure. Intake of methyl donating nutrients including folate was positively associated LINE-1 methylation and negatively associated with IFNγ CpG-186. Higher levels of LINE-1 methylation were associated with greater dPFV.

Conclusion

We identified several nutrients that were associated with improved quality of life measures among children with asthma. The IFNγ promoter CpG site -186 but not -54 was associated with the intake of selected dietary nutrients. However, in this small population of children with asthma, the IFNγ promoter CpG sites were not associated with respiratory health measures so it remains unclear through which epigenetic mechanism these nutrients are impacting the quality of life measure. These findings add to the evidence that dietary nutrients, particularly foods containing methyl donors, may be important for epigenetic regulation as it pertains to the control of asthma.
Trial registration ClincialTrials.gov NCT00807183. Registered 10 December 2008
Appendix
Available only for authorised users
Literature
1.
go back to reference Akinbami LJ, et al. Trends in asthma prevalence, health care use, and mortality in the United States, 2001–2010. NCHS Data Brief. 2012;94:1–8. Akinbami LJ, et al. Trends in asthma prevalence, health care use, and mortality in the United States, 2001–2010. NCHS Data Brief. 2012;94:1–8.
3.
go back to reference Thuesen BH, et al. Atopy, asthma, and lung function in relation to folate and vitamin B(12) in adults. Allergy. 2010;65(11):1446–54.CrossRefPubMed Thuesen BH, et al. Atopy, asthma, and lung function in relation to folate and vitamin B(12) in adults. Allergy. 2010;65(11):1446–54.CrossRefPubMed
4.
go back to reference Mehta AK, et al. Choline attenuates immune inflammation and suppresses oxidative stress in patients with asthma. Immunobiology. 2010;215(7):527–34.CrossRefPubMed Mehta AK, et al. Choline attenuates immune inflammation and suppresses oxidative stress in patients with asthma. Immunobiology. 2010;215(7):527–34.CrossRefPubMed
5.
go back to reference Barros R, et al. Adherence to the Mediterranean diet and fresh fruit intake are associated with improved asthma control. Allergy. 2008;63(7):917–23.CrossRefPubMed Barros R, et al. Adherence to the Mediterranean diet and fresh fruit intake are associated with improved asthma control. Allergy. 2008;63(7):917–23.CrossRefPubMed
6.
go back to reference Barros R, et al. Dietary intake of alpha-linolenic acid and low ratio of n-6:n-3 PUFA are associated with decreased exhaled NO and improved asthma control. Br J Nutr. 2011;106(3):441–50.CrossRefPubMed Barros R, et al. Dietary intake of alpha-linolenic acid and low ratio of n-6:n-3 PUFA are associated with decreased exhaled NO and improved asthma control. Br J Nutr. 2011;106(3):441–50.CrossRefPubMed
7.
go back to reference Castro-Rodriguez JA, et al. Mediterranean diet as a protective factor for wheezing in preschool children. J Pediatr. 2008;152(6):823–8.CrossRefPubMed Castro-Rodriguez JA, et al. Mediterranean diet as a protective factor for wheezing in preschool children. J Pediatr. 2008;152(6):823–8.CrossRefPubMed
8.
go back to reference Chatzi L, et al. Diet, wheeze, and atopy in school children in Menorca, Spain. Pediatr Allergy Immunol. 2007;18(6):480–5.CrossRefPubMed Chatzi L, et al. Diet, wheeze, and atopy in school children in Menorca, Spain. Pediatr Allergy Immunol. 2007;18(6):480–5.CrossRefPubMed
9.
go back to reference Chatzi L, et al. Mediterranean diet in pregnancy is protective for wheeze and atopy in childhood. Thorax. 2008;63(6):507–13.CrossRefPubMed Chatzi L, et al. Mediterranean diet in pregnancy is protective for wheeze and atopy in childhood. Thorax. 2008;63(6):507–13.CrossRefPubMed
10.
go back to reference de Batlle J, et al. Mediterranean diet is associated with reduced asthma and rhinitis in Mexican children. Allergy. 2008;63(10):1310–6.CrossRefPubMed de Batlle J, et al. Mediterranean diet is associated with reduced asthma and rhinitis in Mexican children. Allergy. 2008;63(10):1310–6.CrossRefPubMed
11.
go back to reference Garcia-Marcos L, et al. Relationship of asthma and rhinoconjunctivitis with obesity, exercise and Mediterranean diet in Spanish schoolchildren. Thorax. 2007;62(6):503–8.CrossRefPubMedPubMedCentral Garcia-Marcos L, et al. Relationship of asthma and rhinoconjunctivitis with obesity, exercise and Mediterranean diet in Spanish schoolchildren. Thorax. 2007;62(6):503–8.CrossRefPubMedPubMedCentral
12.
go back to reference Romieu I, et al. Dietary intake, lung function and airway inflammation in Mexico City school children exposed to air pollutants. Respir Res. 2009;10:122.CrossRefPubMedPubMedCentral Romieu I, et al. Dietary intake, lung function and airway inflammation in Mexico City school children exposed to air pollutants. Respir Res. 2009;10:122.CrossRefPubMedPubMedCentral
14.
go back to reference Berthon BS, et al. Investigation of the association between dietary intake, disease severity and airway inflammation in asthma. Respirology. 2013;18(3):447–54.CrossRefPubMed Berthon BS, et al. Investigation of the association between dietary intake, disease severity and airway inflammation in asthma. Respirology. 2013;18(3):447–54.CrossRefPubMed
15.
go back to reference Cortessis VK, et al. Environmental epigenetics: prospects for studying epigenetic mediation of exposure–response relationships. Hum Genet. 2012;131(10):1565–89.CrossRefPubMedPubMedCentral Cortessis VK, et al. Environmental epigenetics: prospects for studying epigenetic mediation of exposure–response relationships. Hum Genet. 2012;131(10):1565–89.CrossRefPubMedPubMedCentral
16.
go back to reference Lovinsky-Desir S, Miller RL. Epigenetics, asthma, and allergic diseases: a review of the latest advancements. Curr Allergy Asthma Rep. 2012;12(3):211–20.CrossRefPubMedPubMedCentral Lovinsky-Desir S, Miller RL. Epigenetics, asthma, and allergic diseases: a review of the latest advancements. Curr Allergy Asthma Rep. 2012;12(3):211–20.CrossRefPubMedPubMedCentral
18.
go back to reference Bansal P, et al. Intranasal administration of a combination of choline chloride, vitamin C, and selenium attenuates the allergic effect in a mouse model of airway disease. Free Radic Biol Med. 2014;73:358–65.CrossRefPubMed Bansal P, et al. Intranasal administration of a combination of choline chloride, vitamin C, and selenium attenuates the allergic effect in a mouse model of airway disease. Free Radic Biol Med. 2014;73:358–65.CrossRefPubMed
19.
go back to reference North ML, Ellis AK. The role of epigenetics in the developmental origins of allergic disease. Ann Allergy Asthma Immunol. 2011;106(5):355–61.CrossRefPubMed North ML, Ellis AK. The role of epigenetics in the developmental origins of allergic disease. Ann Allergy Asthma Immunol. 2011;106(5):355–61.CrossRefPubMed
20.
go back to reference Dolinoy DC. The agouti mouse model: an epigenetic biosensor for nutritional and environmental alterations on the fetal epigenome. Nutr Rev. 2008;66(Suppl 1):S7–11.CrossRefPubMedPubMedCentral Dolinoy DC. The agouti mouse model: an epigenetic biosensor for nutritional and environmental alterations on the fetal epigenome. Nutr Rev. 2008;66(Suppl 1):S7–11.CrossRefPubMedPubMedCentral
21.
go back to reference Hollingsworth JW, et al. In utero supplementation with methyl donors enhances allergic airway disease in mice. J Clin Invest. 2008;118(10):3462–9.PubMedPubMedCentral Hollingsworth JW, et al. In utero supplementation with methyl donors enhances allergic airway disease in mice. J Clin Invest. 2008;118(10):3462–9.PubMedPubMedCentral
23.
go back to reference Nadeau K, et al. Ambient air pollution impairs regulatory T-cell function in asthma. J Allergy Clin Immunol. 2010;126(4):845–52.CrossRefPubMed Nadeau K, et al. Ambient air pollution impairs regulatory T-cell function in asthma. J Allergy Clin Immunol. 2010;126(4):845–52.CrossRefPubMed
24.
go back to reference Friso S, et al. One-carbon metabolism and epigenetics. Mol Aspects Med. 2016. Friso S, et al. One-carbon metabolism and epigenetics. Mol Aspects Med. 2016.
25.
go back to reference Calderon C, et al. T-cell cytokine profiles are altered in childhood asthma exacerbation. Respirology. 2009;14(2):264–9.CrossRefPubMed Calderon C, et al. T-cell cytokine profiles are altered in childhood asthma exacerbation. Respirology. 2009;14(2):264–9.CrossRefPubMed
26.
go back to reference Crinnion WJ. Do environmental toxicants contribute to allergy and asthma? Altern Med Rev. 2012;17(1):6–18.PubMed Crinnion WJ. Do environmental toxicants contribute to allergy and asthma? Altern Med Rev. 2012;17(1):6–18.PubMed
27.
go back to reference Smart JM, et al. Polyclonal and allergen-induced cytokine responses in adults with asthma: resolution of asthma is associated with normalization of IFN-gamma responses. J Allergy Clin Immunol. 2002;110(3):450–6.CrossRefPubMed Smart JM, et al. Polyclonal and allergen-induced cytokine responses in adults with asthma: resolution of asthma is associated with normalization of IFN-gamma responses. J Allergy Clin Immunol. 2002;110(3):450–6.CrossRefPubMed
28.
go back to reference Meng H, et al. In vitro production of IL-6 and IFN-gamma is influenced by dietary variables and predicts upper respiratory tract infection incidence and severity respectively in young adults. Front Immunol. 2015;6:94.CrossRefPubMedPubMedCentral Meng H, et al. In vitro production of IL-6 and IFN-gamma is influenced by dietary variables and predicts upper respiratory tract infection incidence and severity respectively in young adults. Front Immunol. 2015;6:94.CrossRefPubMedPubMedCentral
29.
go back to reference Mohammadi-Shahrokhi V, et al. Immunomodulatory effects of adjuvants CPG, MPLA, and BCG on the Derp2-induced acute asthma at early life in an animal model of BALB/c Mice. Inflammation. 2016. Mohammadi-Shahrokhi V, et al. Immunomodulatory effects of adjuvants CPG, MPLA, and BCG on the Derp2-induced acute asthma at early life in an animal model of BALB/c Mice. Inflammation. 2016.
30.
go back to reference Santeliz JV, et al. Amb a 1-linked CpG oligodeoxynucleotides reverse established airway hyperresponsiveness in a murine model of asthma. J Allergy Clin Immunol. 2002;109(3):455–62.CrossRefPubMed Santeliz JV, et al. Amb a 1-linked CpG oligodeoxynucleotides reverse established airway hyperresponsiveness in a murine model of asthma. J Allergy Clin Immunol. 2002;109(3):455–62.CrossRefPubMed
32.
go back to reference Ward TJ, et al. Efficacy of interventions targeting household air pollution from residential wood stoves. J Expo Sci Environ Epidemiol. 2017;27(1):64–71.CrossRefPubMed Ward TJ, et al. Efficacy of interventions targeting household air pollution from residential wood stoves. J Expo Sci Environ Epidemiol. 2017;27(1):64–71.CrossRefPubMed
35.
go back to reference Block G, et al. Revision of dietary analysis software for the health habits and history questionnaire. Am J Epidemiol. 1994;139(12):1190–6.CrossRefPubMed Block G, et al. Revision of dietary analysis software for the health habits and history questionnaire. Am J Epidemiol. 1994;139(12):1190–6.CrossRefPubMed
36.
go back to reference Block G, DiSogra C. WIC dietary assessment validation study. Final report. Alexandria: US Department of Agriculture, Food and Nutrition Service; 1995. Block G, DiSogra C. WIC dietary assessment validation study. Final report. Alexandria: US Department of Agriculture, Food and Nutrition Service; 1995.
37.
go back to reference Block G, et al. Comparison of two dietary questionnaires validated against multiple dietary records collected during a 1-year period. J Am Diet Assoc. 1992;92:686–93.PubMed Block G, et al. Comparison of two dietary questionnaires validated against multiple dietary records collected during a 1-year period. J Am Diet Assoc. 1992;92:686–93.PubMed
38.
go back to reference Block G, et al. Validation of a self-administered diet history questionnaire using multiple diet records. J Clin Epidemiol. 1990;43(12):1327–35.CrossRefPubMed Block G, et al. Validation of a self-administered diet history questionnaire using multiple diet records. J Clin Epidemiol. 1990;43(12):1327–35.CrossRefPubMed
39.
go back to reference Juniper EF, et al. Measuring quality of life in children with asthma. Qual Life Res. 1996;5(1):35–46.CrossRefPubMed Juniper EF, et al. Measuring quality of life in children with asthma. Qual Life Res. 1996;5(1):35–46.CrossRefPubMed
40.
go back to reference Benjamini Y, Hochberg Y. Controlling the false discovery rate—a practical and powerful approach to multiple testing. J R Stat Soc Series B-Methodol. 1995;57(1):289–300. Benjamini Y, Hochberg Y. Controlling the false discovery rate—a practical and powerful approach to multiple testing. J R Stat Soc Series B-Methodol. 1995;57(1):289–300.
41.
go back to reference Lung National Heart, Institute Blood. Expert panel report 3: guidelines for the diagnosis and management of asthma. Bethesda: National Heart Lung, and Blood Institute; 2007. Lung National Heart, Institute Blood. Expert panel report 3: guidelines for the diagnosis and management of asthma. Bethesda: National Heart Lung, and Blood Institute; 2007.
42.
go back to reference Sharma S, Litonjua A. Asthma, allergy, and responses to methyl donor supplements and nutrients. J Allergy Clin Immunol. 2014;133(5):1246–54.CrossRefPubMed Sharma S, Litonjua A. Asthma, allergy, and responses to methyl donor supplements and nutrients. J Allergy Clin Immunol. 2014;133(5):1246–54.CrossRefPubMed
44.
go back to reference Crider KS, et al. Prenatal folic acid and risk of asthma in children: a systematic review and meta-analysis. Am J Clin Nutr. 2013;98(5):1272–81.CrossRefPubMed Crider KS, et al. Prenatal folic acid and risk of asthma in children: a systematic review and meta-analysis. Am J Clin Nutr. 2013;98(5):1272–81.CrossRefPubMed
45.
go back to reference Lin JH, et al. Relationships between folate and inflammatory features of asthma. J Allergy Clin Immunol. 2013;131(3):918–20.CrossRefPubMed Lin JH, et al. Relationships between folate and inflammatory features of asthma. J Allergy Clin Immunol. 2013;131(3):918–20.CrossRefPubMed
46.
47.
go back to reference Farres MN, et al. Study of folate status among Egyptian asthmatics. Intern Med. 2011;50(3):205–11.CrossRefPubMed Farres MN, et al. Study of folate status among Egyptian asthmatics. Intern Med. 2011;50(3):205–11.CrossRefPubMed
48.
go back to reference Blatter J, et al. Folate deficiency, atopy, and severe asthma exacerbations in Puerto Rican children. Ann Am Thorac Soc. 2016;13(2):223–30.PubMedPubMedCentral Blatter J, et al. Folate deficiency, atopy, and severe asthma exacerbations in Puerto Rican children. Ann Am Thorac Soc. 2016;13(2):223–30.PubMedPubMedCentral
49.
go back to reference Fabian E, et al. Nutritional supplements and plasma antioxidants in childhood asthma. Wien Klin Wochenschr. 2013;125(11–12):309–15.CrossRefPubMed Fabian E, et al. Nutritional supplements and plasma antioxidants in childhood asthma. Wien Klin Wochenschr. 2013;125(11–12):309–15.CrossRefPubMed
50.
go back to reference Rosenlund H, et al. Antioxidant intake and allergic disease in children. Clin Exp Allergy. 2012;42(10):1491–500.CrossRefPubMed Rosenlund H, et al. Antioxidant intake and allergic disease in children. Clin Exp Allergy. 2012;42(10):1491–500.CrossRefPubMed
52.
go back to reference Pollock AH, et al. Prolonged Intake of dietary lipids alters membrane structure and T cell responses in LDLr−/− Mice. J Immunol. 2016;196(10):3993–4002.CrossRefPubMed Pollock AH, et al. Prolonged Intake of dietary lipids alters membrane structure and T cell responses in LDLr−/− Mice. J Immunol. 2016;196(10):3993–4002.CrossRefPubMed
54.
go back to reference de Pablo MA, Puertollano MA, Alvarez de Cienfuegos G. Biological and clinical significance of lipids as modulators of immune system functions. Clin Diagn Lab Immunol. 2002;9(5):945–50.PubMed de Pablo MA, Puertollano MA, Alvarez de Cienfuegos G. Biological and clinical significance of lipids as modulators of immune system functions. Clin Diagn Lab Immunol. 2002;9(5):945–50.PubMed
55.
58.
go back to reference Liu J, et al. Combined inhaled diesel exhaust particles and allergen exposure alter methylation of T helper genes and IgE production in vivo. Toxicol Sci. 2008;102(1):76–81.CrossRefPubMed Liu J, et al. Combined inhaled diesel exhaust particles and allergen exposure alter methylation of T helper genes and IgE production in vivo. Toxicol Sci. 2008;102(1):76–81.CrossRefPubMed
59.
go back to reference Brand S, et al. DNA methylation of TH1/TH2 cytokine genes affects sensitization and progress of experimental asthma. J Allergy Clin Immunol. 2012;29(6):1602–10.CrossRef Brand S, et al. DNA methylation of TH1/TH2 cytokine genes affects sensitization and progress of experimental asthma. J Allergy Clin Immunol. 2012;29(6):1602–10.CrossRef
61.
go back to reference Kohli A, et al. Secondhand smoke in combination with ambient air pollution exposure is associated with increasedx CpG methylation and decreased expression of IFN-gamma in T effector cells and Foxp3 in T regulatory cells in children. Clin Epigenetics. 2012;4(1):17.CrossRefPubMedPubMedCentral Kohli A, et al. Secondhand smoke in combination with ambient air pollution exposure is associated with increasedx CpG methylation and decreased expression of IFN-gamma in T effector cells and Foxp3 in T regulatory cells in children. Clin Epigenetics. 2012;4(1):17.CrossRefPubMedPubMedCentral
62.
go back to reference White GP, et al. CpG methylation patterns in the IFNgamma promoter in naive T cells: variations during Th1 and Th2 differentiation and between atopics and non-atopics. Pediatr Allergy Immunol. 2006;17(8):557–64.CrossRefPubMed White GP, et al. CpG methylation patterns in the IFNgamma promoter in naive T cells: variations during Th1 and Th2 differentiation and between atopics and non-atopics. Pediatr Allergy Immunol. 2006;17(8):557–64.CrossRefPubMed
63.
64.
go back to reference Lovinsky-Desir S, et al. DNA methylation of the allergy regulatory gene interferon gamma varies by age, sex, and tissue type in asthmatics. Clin Epigenetics. 2014;6(1):9.CrossRefPubMedPubMedCentral Lovinsky-Desir S, et al. DNA methylation of the allergy regulatory gene interferon gamma varies by age, sex, and tissue type in asthmatics. Clin Epigenetics. 2014;6(1):9.CrossRefPubMedPubMedCentral
66.
go back to reference Huang SL, Pan WH. Dietary fats and asthma in teenagers: analyses of the first Nutrition and Health Survey in Taiwan (NAHSIT). Clin Exp Allergy. 2001;31(12):1875–80.CrossRefPubMed Huang SL, Pan WH. Dietary fats and asthma in teenagers: analyses of the first Nutrition and Health Survey in Taiwan (NAHSIT). Clin Exp Allergy. 2001;31(12):1875–80.CrossRefPubMed
67.
go back to reference Heinrich J, et al. Allergic sensitization and diet: ecological analysis in selected European cities. Eur Respir J. 2001;17(3):395–402.CrossRefPubMed Heinrich J, et al. Allergic sensitization and diet: ecological analysis in selected European cities. Eur Respir J. 2001;17(3):395–402.CrossRefPubMed
Metadata
Title
Dietary intake is associated with respiratory health outcomes and DNA methylation in children with asthma
Authors
L. Montrose
T. J. Ward
E. O. Semmens
Y. H. Cho
B. Brown
C. W. Noonan
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Allergy, Asthma & Clinical Immunology / Issue 1/2017
Electronic ISSN: 1710-1492
DOI
https://doi.org/10.1186/s13223-017-0187-8

Other articles of this Issue 1/2017

Allergy, Asthma & Clinical Immunology 1/2017 Go to the issue