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Can fish oil in pregnancy and lactation alter maternal and infant immunological responses and prevent allergy in the offspring?
Linköping University, Department of Clinical and Experimental Medicine, Pediatrics . Linköping University, Faculty of Health Sciences. Östergötlands Läns Landsting, Centre of Paediatrics and Gynecology and Obstetrics, Department of Paediatrics in Linköping.
2010 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Background: A connection has been proposed between the increase of allergic disease and the altered composition of fatty acids in the diet in the westernised world. Less oily fish and more vegetable oil are consumed today compared to 50-100 years ago. Programming of the immune responses takes place very early in life and environmental factors, such as fish in the diet, have been suggested to protect from infant allergy.

Aim: The general aim of this thesis was to assess the effects of maternal dietary supplementation with ω-3 long chain polyunsaturated fatty acids (LCPUFA), i.e. fish oil, in pregnancy and lactation on the development of allergic symptoms and sensitisation in the infants as well as some immunological markers in mothers and infants.

Subjects and methods: This thesis is based on the results from a prospective double-blind placebo-controlled multi-centre trial comprising 145 families. Pregnant women, at risk of having an allergic infant, were recruited at the antenatal clinics and randomised to daily supplementation with 1.6 g eicosapentaenoic acid (EPA, C20:5ω-3) and 1.1 g docosahexaenoic acid (DHA, C22:6ω-3) or placebo, starting in the 25th gestational week and continuing through 3.5 months of breastfeeding. Phospholipid fatty acids in maternal and infant plasma were analysed to assess compliance. Maternal prostaglandin E2 (PGE2), leukotriene B4 (LTB4) and cytokines along with infant vaccine induced responses and chemokines were analysed with ELISA and Luminex techniques. Clinical outcomes were allergic disease and positive skin prick test/detectable circulating IgE antibodies to common allergens.

Results: Phospholipid proportions of ω-3 LCPUFA increased significantly in the ω-3 supplemented women and their infants. Lipopolysaccharide-induced PGE2 secretion from whole blood culture supernatants decreased in a majority of the ω-3-supplemented mothers (p<0.01). The decrease in PGE2 production was more pronounced among non-atopic than atopic mothers. No difference in the prevalence of allergic symptoms was found between the intervention groups. The cumulative incidence of IgE associated eczema and IgE mediated food allergy was though reduced in the ω-3 group during the first two years (OR=0.2 and 0.3 compared to placebo, p<0.05 for both). The cumulative incidence of any IgE associated disease during the first two years of life was 13% in the ω-3 supplemented group compared to 30% in the placebo group (p=0.01, OR 0.3, p<0.05). This effect was most evident in infants of non-allergic mothers. Higher maternal and infant proportions of DHA and EPA were associated with lower prevalence of IgE associated disease (p=0.01-0.05), in a dose dependent manner. In addition, no allergic symptoms as compared to multiple allergic symptoms in the infants, regardless of sensitisation, were related to higher maternal and infant ω-3 LCPUFA status (p<0.05). In infants without, but not with, maternal history of allergy, the ω-3 supplementation was related to lower CC-chemokine ligand 17 (CCL17)/ CXC-chemokine ligand 11 (CXCL11) (Th2/Th1) ratios (p<0.05). Furthermore in non-allergic, but not in allergic infants, ω-3 supplementation was linked with higher Th1-associated CXCL11 levels (p<0.05), as well as increased IgG titres to diphtheria (p=0.01) and tetanus (p=0.05) toxins.

Conclusions: A decreased cumulative incidence of IgE associated disease in the infants was found after maternal ω-3 LCPUFA supplementation as well as a reverse dose response relationship between maternal ω-3 LCPUFA status and infant IgE associated disease. Higher plasma proportions of DHA and EPA in were also associated to less severe allergic disease. A tendency towards strengthened Th1 associated response after maternal ω-3 LCPUFA supplementation was indicated in the analysis of maternal and infant immunological markers. These effects, as well as the clinical outcomes, were more pronounced in non-allergic individuals, suggesting gene-by-environment interactions.

Place, publisher, year, edition, pages
Linköping: Linköping University Electronic Press , 2010. , 118 p.
Series
Linköping University Medical Dissertations, ISSN 0345-0082 ; 1206
National Category
Medical and Health Sciences
Identifiers
URN: urn:nbn:se:liu:diva-61947ISBN: 978-91-7393-314-8 (print)OAI: oai:DiVA.org:liu-61947DiVA: diva2:370855
Public defence
2010-12-07, Berzeliussalen, Hälsouniversitetet, Campus US, Linköpings universitet, Linköping, 13:00
Opponent
Supervisors
Available from: 2010-11-18 Created: 2010-11-18 Last updated: 2010-11-18Bibliographically approved
List of papers
1. The Effects of Omega-3 Fatty Acid Supplementation in Pregnancy on Maternal Eicosanoid, Cytokine, and Chemokine Secretion
Open this publication in new window or tab >>The Effects of Omega-3 Fatty Acid Supplementation in Pregnancy on Maternal Eicosanoid, Cytokine, and Chemokine Secretion
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2009 (English)In: Pediatric Research, ISSN 0031-3998, E-ISSN 1530-0447, Vol. 66, no 2, 212-217 p.Article in journal (Refereed) Published
Abstract [en]

The incidence of allergic diseases has increased, and,I relation between allergy and dietary fatty acids has been proposed. Modulation of the maternal immune function during pregnancy may have an impact on future clinical outcomes in the child. The aim of this Study was to determine the effects of omega (omega)-3 long-chain polyunsaturated fatty acids (LCPUFA) Supplementation during pregnancy on the plasma fatty acid composition in relation to the maternal immune function. Pregnant women with allergic disease in their immediate family were supplemented daily with 2.7 g omega-3 LCPUFA (n = 70) or 2.8 g soybean oil as placebo (n = 75) from the 25th gestational week. The proportions of eicosapentaenoic acid and docosahexaenoic acid in plasma/serum phospholipids increased in the omega-3-supplemented group, whereas arachidonic acid decreased during intervention. Lipopolysaccharide-induced prostaglandin E, secretion from whole blood culture supernatants (it = 59) decreased in a majority of the omega-3-supplemented mothers (18 of 28, p = 0.002). The decreased prostaglandin E-2, production was more pronounced among nonatopic than atopic mothers. The lipopolysaccharide-induced cytokine and chemokine secretion was not affected. Out results indicate that omega-3 LCPUFA supplementation during the last trimester may dampen certain immune responses involved in allergic inflammation.

National Category
Medical and Health Sciences
Identifiers
urn:nbn:se:liu:diva-20127 (URN)10.1203/PDR.0b013e3181aabd1c (DOI)
Available from: 2009-08-31 Created: 2009-08-31 Last updated: 2017-12-13
2. Fish oil supplementation in pregnancy and lactation may decrease the risk of infant allergy
Open this publication in new window or tab >>Fish oil supplementation in pregnancy and lactation may decrease the risk of infant allergy
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2009 (English)In: Acta Paediatrica, ISSN 0803-5253, E-ISSN 1651-2227, Vol. 98, no 9, 1461-1467 p.Article in journal (Refereed) Published
Abstract [en]

Maternal intake of omega-3 (-3) polyunsaturated fatty acids (PUFAs) during pregnancy has decreased, possibly contributing to a current increased risk of childhood allergy. Aim: To describe the effects of maternal -3 long-chain PUFA supplementation during pregnancy and lactation on the incidence of allergic disease in infancy. Methods: One hundred and forty-five pregnant women, affected by allergy themselves or having a husband or previous child with allergies, were included in a randomized placebo-controlled trial. Daily maternal supplementation with either 1.6 g eicosapentaenoic acid and 1.1 g docosahexaenoic acid or placebo was given from the 25(th) gestational week to average 3-4 months of breastfeeding. Skin prick tests, detection of circulating specific immunoglobulin E (IgE) antibodies and clinical examinations of the infants were performed. Results: The period prevalence of food allergy was lower in the -3 group (1/52, 2%) compared to the placebo group (10/65, 15%, p andlt; 0.05) as well as the incidence of IgE-associated eczema (-3 group: 4/52, 8%; placebo group: 15/63, 24%, p andlt; 0.05). Conclusion: Maternal -3 fatty acid supplementation may decrease the risk of food allergy and IgE-associated eczema during the first year of life in infants with a family history of allergic disease.

Keyword
Allergy, Eczema, Lactation, Polyunsaturated fatty acids, Pregnancy
National Category
Medical and Health Sciences
Identifiers
urn:nbn:se:liu:diva-19806 (URN)10.1111/j.1651-2227.2009.01355.x (DOI)
Available from: 2009-08-11 Created: 2009-08-10 Last updated: 2017-12-13
3. Allergic disease in infants up to 2 yr of age in relation to plasma omega-3 fatty acids and maternal fish oil supplementation inpregnancy and lactation
Open this publication in new window or tab >>Allergic disease in infants up to 2 yr of age in relation to plasma omega-3 fatty acids and maternal fish oil supplementation inpregnancy and lactation
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2011 (English)In: Pediatric Allergy and Immunology, ISSN 0905-6157, E-ISSN 1399-3038, Vol. 22, no 5, 505-514 p.Article in journal (Refereed) Published
Abstract [en]

We have previously reported a protective effect of maternal omega-3 long-chain polyunsaturated fatty acids (x-3 LCPUFA) supplementation in pregnancy and lactation on IgE-associated eczema and food allergy in the infant during the first year of life. Here we investigate whether the effects of the LCPUFA supplementation on IgE-associated diseases last up to 2 yr of age and assess the relationship between plasma proportions of x-3 PUFAs and the frequency and severity of infant allergic disease. 145 pregnant women, at risk of having an allergic infant, were randomized to daily supplementation with 1.6 g eicosapentaenoic acid (EPA) and 1.1 g docosahexaenoic acid (DHA) or placebo starting in the 25th gestational week and continuing through 3.5 months of breastfeeding. Clinical examinations, skin prick tests and analysis of maternal and infant plasma phospholipid fatty acids and infant specific IgE were performed. No difference in the prevalence of allergic symptoms was found between the intervention groups. Thecumulative incidence of IgE-associated disease was lower in the x-3-supplemented group (6/54, 13%) compared with the placebo group (19/62, 30%, p = 0.01). Higher maternal and infant proportions of DHA and EPA were associated with lower prevalence of IgE associated disease (p = 0.01–0.05) in a dose-dependent manner. Higher maternal and infant proportions of DHA and EPA were found if the infants presented none, when compared with multiple allergic symptoms, (p < 0.05) regardless of sensitization. In summary, the x-3 supplementation offered no obvious preventive effect on the prevalence of clinical symptoms of allergic disease, but the decrease in cumulative incidence of IgE-associated disease seen during the first year still remained until 2 yr of age. Furthermore, high proportions of DHA and EPA in maternal and infant plasma phospholipids were associated with less IgE-associated disease and a reduced severity of the allergic phenotype.

Place, publisher, year, edition, pages
John Wiley & Sons A/S, 2011
Keyword
allergy; eczema; fatty acids; pregnancy; lactation; dietary supplements; infant
National Category
Medical and Health Sciences
Identifiers
urn:nbn:se:liu:diva-61945 (URN)10.1111/j.1399-3038.2010.01096.x (DOI)000292931300009 ()
Note
Original Publication: Catrin Furuhjelm, Kristina Warstedt, Malin Fagerås Böttcher, Karin Fälth-Magnusson, Johanna Larsson, Mats Fredriksson and Karel Duchén, Allergic disease in infants up to 2 yr of age in relation to plasma omega-3 fatty acids and maternal fish oil supplementation inpregnancy and lactation, 2011, Pediatric Allergy and Immunology, (22), 5, 505-514. http://dx.doi.org/10.1111/j.1399-3038.2010.01096.x Copyright: John Wiley and Sons http://www.wiley.com/ Available from: 2010-11-18 Created: 2010-11-18 Last updated: 2017-12-12
4. Th1 and Th2 chemokines, vaccine induced 1 immunity and allergic disease in infants  after maternal ω-3 fatty acid supplementation during pregnancy and lactation
Open this publication in new window or tab >>Th1 and Th2 chemokines, vaccine induced 1 immunity and allergic disease in infants  after maternal ω-3 fatty acid supplementation during pregnancy and lactation
2011 (English)In: Pediatric Research, ISSN 0031-3998, E-ISSN 1530-0447, Vol. 69, no 3, 259-264 p.Article in journal (Refereed) Published
Abstract [en]

We investigated whether the previously reported preventive effect of maternal ω-3 fatty acid supplementation on IgE-associated allergic disease in infancy may be mediated by facilitating a balanced circulating Th2/Th1 chemokine profile in the infant. Vaccine-induced immune responses at 2 y of age were also evaluated. Pregnant women, at risk of having an allergic infant, were randomized to daily supplementation with 1.6 g eicosapentaenoic acid and 1.1 g docosahexaenoic acid or placebo from the 25th gestational week through 3.5 mo of breastfeeding. Infant plasma was analyzed for chemokines (cord blood, 3, 12, 24 mo) and anti-tetanus and anti-diphtheria IgG (24 mo). High Th2-associated CC-chemokine ligand 17 (CCL17) levels were associated with infant allergic disease (p < 0.05). In infants without, but not with, maternal history of allergy, the ω-3 supplementation was related to lower CCL17/CXC-chemokine ligand 11 (CXCL11) (Th2/Th1) ratios (p < 0.05). Furthermore, in nonallergic, but not in allergic infants, ω-3 supplementation was linked with higher Th1-associated CXCL11 levels (p < 0.05), as well as increased IgG titers to diphtheria (p = 0.01) and tetanus (p = 0.05) toxins. Thus, the prospect of balancing the infant immune system toward a less Th2-dominated response, by maternal ω-3 fatty acid supplementation, seems to be influenced by allergic status.

Place, publisher, year, edition, pages
Nature Publishing Group, 2011
National Category
Medical and Health Sciences
Identifiers
urn:nbn:se:liu:diva-61946 (URN)10.1203/PDR.0b013e3182072229 (DOI)000287621700014 ()21099447 (PubMedID)
Available from: 2010-11-18 Created: 2010-11-18 Last updated: 2017-12-12Bibliographically approved

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