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Anthroposophic lifestyle is associated with a lower incidence of food allergen sensitization in early childhood

2015; Elsevier BV; Volume: 137; Issue: 4 Linguagem: Inglês

10.1016/j.jaci.2015.11.009

1097-6825

Sara Fagerstedt, Helena Marell Hesla, Emelie Ekhager, Helen Rosenlund, Axel Mie, Lina Benson, Annika Scheynius, Johan Alm,

Asthma and respiratory diseases

Sensitization to food allergens is increasing more rapidly than sensitization to pollen or animal allergens.1Prescott S. Allen K.J. Food allergy: riding the second wave of the allergy epidemic.Pediatr Allergy Immunol. 2011; 22: 155-160Crossref PubMed Scopus (369) Google Scholar, 2Nwaru B.I. Hickstein L. Panesar S.S. Roberts G. Muraro A. Sheikh A. et al.Prevalence of common food allergies in Europe: a systematic review and meta-analysis.Allergy. 2014; 69: 992-1007Crossref PubMed Scopus (615) Google Scholar On a population level, development of allergic sensitization commonly begins with food allergen sensitization in early infancy, followed or sometimes replaced by sensitization to animals and later, at 4 to 5 years of age, including sensitization to pollen. The cause for the onset or development of sensitization to allergens and allergy-related diseases is still not known. Environmental and lifestyle factors are considered to contribute to disease development.3Brooks C. Pearce N. Douwes J. The hygiene hypothesis in allergy and asthma: an update.Curr Opin Allergy Clin Immunol. 2013; 13: 70-77Crossref PubMed Scopus (118) Google Scholar Anthroposophy is a holistic philosophy that was founded by the Austrian philosopher Rudolf Steiner (1861-1925) and covers most aspects of life, including education, health care, agriculture, and diet.4Glöckler M. Goebel W. A guide to child health—a holistic approach to raising healthy children.4th ed. Floris Books, Edinburgh (United Kingdom)2013Google Scholar Previous cross-sectional studies have shown that Steiner school children, who often come from families with an anthroposophic lifestyle, have a lower prevalence of sensitization and allergic disease compared with reference children.5Alm J.S. Swartz J. Lilja G. Scheynius A. Pershagen G. Atopy in children of families with an anthroposophic lifestyle.Lancet. 1999; 353: 1485-1488Abstract Full Text Full Text PDF PubMed Scopus (434) Google Scholar, 6Floistrup H. Swartz J. Bergstrom A. Alm J.S. Scheynius A. van Hage M. et al.Allergic disease and sensitization in Steiner school children.J Allergy Clin Immunol. 2006; 117: 59-66Abstract Full Text Full Text PDF PubMed Scopus (153) Google Scholar These observations have been confirmed in the prospective birth cohort Assessment of Lifestyle and Allergic Disease During Infancy (ALADDIN).7Stenius F. Swartz J. Lilja G. Borres M. Bottai M. Pershagen G. et al.Lifestyle factors and sensitization in children—the ALADDIN birth cohort.Allergy. 2011; 66: 1330-1338Crossref PubMed Scopus (37) Google Scholar In Hesla et al,8Hesla H.M. Stenius F. Pettersson H.P. Alm J. Allergy-related disease in relation to early life exposures: The ALADDIN birth cohort.J Allergy Clin Immunol. 2016; ([In press])PubMed Google Scholar we report the clinical manifestations up to 2 years of age in the ALADDIN cohort and provide a description of demographics and early lifestyle exposures. We observed that anthroposophic lifestyle was associated with a reduced risk of reported food hypersensitivity and reported recurrent wheeze but not eczema. Moreover, delayed washing of the newborn's whole body (after 7 days of age) was associated with a reduced risk of allergen sensitization, whereas an increased risk was seen for children who had a mother who worked during pregnancy. However, much of the effect of anthroposophic lifestyle on allergen sensitization was unexplained. In this letter we report how the association between lifestyle and sensitization to food, animal, and pollen allergens differs with the child's age. For complete materials and methodology, see the Methods section in this article's Online Repository at www.jacionline.org. Briefly, this study is based on the Swedish prospective cohort ALADDIN,7Stenius F. Swartz J. Lilja G. Borres M. Bottai M. Pershagen G. et al.Lifestyle factors and sensitization in children—the ALADDIN birth cohort.Allergy. 2011; 66: 1330-1338Crossref PubMed Scopus (37) Google Scholar in which 552 children and their families were followed using questionnaires, examinations, and blood samples. The families were classified into 3 lifestyle groups (anthroposophic, partly anthroposophic, and nonanthroposophic). Blood samples were collected from the children at 6, 12, 24, and 60 months of age. Sensitization to food (hen's egg, cow's milk, and/or peanut), animal (dog and/or cat), and pollen (birch and/or timothy) allergens was determined. IgE values of 0.35 kUA/L or greater were regarded as being sensitized. Incidence and prevalence of sensitization were determined. The inclusion process and distribution of children and available blood samples are presented in Fig E1 in this article's Online Repository at www.jacionline.org, and prevalences of IgE sensitization for the individual allergens are presented in Table E1 in this article's Online Repository at www.jacionline.org. As described in Hesla et al,8Hesla H.M. Stenius F. Pettersson H.P. Alm J. Allergy-related disease in relation to early life exposures: The ALADDIN birth cohort.J Allergy Clin Immunol. 2016; ([In press])PubMed Google Scholar several demographic and early lifestyle exposures differed between the lifestyle groups; however, neither parental sensitization nor parental report of allergy-related disease were associated with anthroposophic lifestyle. In addition, parental sensitization was not associated with child sensitization. Incidence proportions of sensitization for the different allergen categories are presented in Fig 1, A to D. In the nonanthroposophic group the incidence proportions of food allergen sensitization were high up to 12 months of age: 15% and 16% were first time sensitized for the age periods of 0 to 6 and 6 to 12 months, respectively, and then decreased to 5% from 12 to 24 months to increase again to 16% from 24 to 60 months. In contrast, in the anthroposophic group the incidence proportions of food sensitization were low at up to 12 months of age and similar for the 4 age periods as follows: 1% (0 to 6 months), 1% (6-12 months), 8% (12-24 months), and 9% (24-60 months). In the partly anthroposophic group the incidence proportions of food allergen sensitization were stable, around 7% for all age periods. In all lifestyle groups sensitization to animal and pollen allergens occurred later than to food allergens. We used general estimating equation models to study the interaction between age and lifestyle and found that age significantly modified the association between lifestyle and food allergen sensitization (P = .02, Fig 2). The inverse association between anthroposophic lifestyle and food allergen sensitization was stronger at 6, 12, and 24 months (odds ratio [OR], 0.16, 0.18, and 0.25, respectively) than at 60 months (OR, 0.58). The association between partly anthroposophic lifestyle and food allergen sensitization was similar at all 4 ages (OR, 0.42, 0.41, 0.40, and 0.35, respectively). No such interaction between age and lifestyle was observed for animal (P = .89) or pollen (P = .91) allergen sensitization (Fig 2). The pattern of allergic sensitization, starting with sensitization against food allergens and followed by animal and pollen allergen sensitization, has been described earlier.9Lack G. Update on risk factors for food allergy.J Allergy Clin Immunol. 2012; 129: 1187-1197Abstract Full Text Full Text PDF PubMed Scopus (310) Google Scholar However, few studies have reported the prevalence of allergen sensitization in early infancy.2Nwaru B.I. Hickstein L. Panesar S.S. Roberts G. Muraro A. Sheikh A. et al.Prevalence of common food allergies in Europe: a systematic review and meta-analysis.Allergy. 2014; 69: 992-1007Crossref PubMed Scopus (615) Google Scholar Tolerance to cow's milk and hen's egg usually develops at 4 to 6 years of age.9Lack G. Update on risk factors for food allergy.J Allergy Clin Immunol. 2012; 129: 1187-1197Abstract Full Text Full Text PDF PubMed Scopus (310) Google Scholar, 10Kulig M. Bergmann R. Klettke U. Wahn V. Tacke U. Wahn U. Natural course of sensitization to food and inhalant allergens during the first 6 years of life.J Allergy Clin Immunol. 1999; 103: 1173-1179Abstract Full Text Full Text PDF PubMed Scopus (376) Google Scholar Because the prevalence of animal and pollen sensitization was low in the present study, which is expected at these ages,9Lack G. Update on risk factors for food allergy.J Allergy Clin Immunol. 2012; 129: 1187-1197Abstract Full Text Full Text PDF PubMed Scopus (310) Google Scholar the association with lifestyle should be interpreted with caution. However, our results are in accordance with earlier studies of school-aged children in which the association with anthroposophic lifestyle was significant only for food but not inhalant allergen sensitization.5Alm J.S. Swartz J. Lilja G. Scheynius A. Pershagen G. Atopy in children of families with an anthroposophic lifestyle.Lancet. 1999; 353: 1485-1488Abstract Full Text Full Text PDF PubMed Scopus (434) Google Scholar, 6Floistrup H. Swartz J. Bergstrom A. Alm J.S. Scheynius A. van Hage M. et al.Allergic disease and sensitization in Steiner school children.J Allergy Clin Immunol. 2006; 117: 59-66Abstract Full Text Full Text PDF PubMed Scopus (153) Google Scholar A higher proportion of families in the anthroposophic group did not consent to blood sampling. However, introduction of selection bias is unlikely because this reluctance to participate in blood sampling was likely to be related to lifestyle and not to sensitization of the child or parent. Consent to blood sampling was made before the parents received any results regarding their own or the child's blood sample analyses. In conclusion, our findings suggest that the reduced prevalence of allergen sensitization seen among children of families with an anthroposophic lifestyle was largely explained by a low incidence of food sensitization before 1 year of age. This indicates that anthroposophic lifestyle has a greater effect on allergen sensitization during the first year of life. We acknowledge the families participating in the ALADDIN study for their trust and contribution and the ALADDIN team for their involvement in this work, especially nurse and coordinator Margareta Eriksson, medical doctor Fredrik Stenius, laboratory manager Catharina Johansson, and biomedical analysts Monica Nordlund and Carina Wallén. This study is based on the prospective birth cohort ALADDIN.E1Stenius F. Swartz J. Lilja G. Borres M. Bottai M. Pershagen G. et al.Lifestyle factors and sensitization in children—the ALADDIN birth cohort.Allergy. 2011; 66: 1330-1338Crossref PubMed Scopus (45) Google Scholar The families were recruited between September 2004 and November 2011 from anthroposophic and conventional maternal-child health care centers (MCHCs) in Stockholm and Järna, a village situated south of Stockholm with a community of anthroposophic followers. Parents were informed about the study at their MCHC, and families interested in participation were enrolled. A total of 552 families were recruited, of whom 444 were recruited during pregnancy and 108 shortly after birth. Preterm infants (born before gestational week 36) and miscarriages were excluded. The parents answered detailed questionnaires about their daily life, health, and food, and the children were examined repeatedly.E2Stenius F. Swartz J. Lindblad F. Pershagen G. Scheynius A. Alm J. et al.Low salivary cortisol levels in infants of families with an anthroposophic lifestyle.Psychoneuroendocrinology. 2010; 35: 1431-1437Crossref PubMed Scopus (22) Google Scholar Inclusion criteria for children in the present study were having a lifestyle classification (see below) and at least 1 (of 4) blood samples taken (Fig E1). The study was approved by the local ethics committee in Stockholm, and written informed consent was obtained from all parents. The families were classified into 3 lifestyle groups (anthroposophic, partly anthroposophic, and nonanthroposophic) based on their choice of MCHC and based on answers to 3 questionnaire questions: (1) “What kind of preschool/school will your newborn child probably go to?”; (2) “Has either of the parents, no matter which type of school you have planned for your child, an anthroposophic view of life?”; and (3) “Is the family's everyday life influenced by an anthroposophic view of life?” Families answering “anthroposophic school” to question 1 and yes to questions 2 and 3 and also attending anthroposophic MCHCs were defined as being anthroposophic. Families answering “conventional” or any other nonanthroposophic type of school to question 1, no to questions 2 and 3, and attending conventional MCHCs were defined as being nonanthroposophic. Families with any other combination of answers were defined as being partly anthroposophic. Blood samples were collected in sodium heparin tubes from parents at the time of inclusion and from the children at 6, 12, 24, and 60 months of age. Plasma was stored at −20°C. Parental sensitization was determined by using ImmunoCAP Phadiatop (Thermo Fisher Scientific, Uppsala, Sweden) for IgE levels to a set of 11 inhalant allergens. Sensitization at 6, 12, and 24 months of age was determined by using ImmunoCAP (Thermo Fisher Scientific) for IgE levels to hen's egg, cow's milk, peanut, dog, cat, birch, and timothy. Sensitization at 5 years of age was determined by using Phadiatop and a food mix of cow's milk, hen's egg, fish, wheat, soybean, and peanut (fx5, Thermo Fisher Scientific). Subjects with allergen-specific IgE levels of 0.35 kUA/L or greater were regarded as being sensitized. Allergens were divided into 3 categories: food, animal, and pollen allergens. The analysis at 60 months was restricted to the same 7 allergens used at earlier time points to obtain a comparable longitudinal observation of the development of sensitization. Incidence and prevalence were depicted graphically for the 3 allergen categories, as well as for any sensitization, by lifestyle. Prevalence was calculated as the number of sensitized children at each age through the number of nonmissing observations at the respective age. Incidence proportions were calculated as the number of first time–sensitized children (cases) during the time period divided by the number of children at risk. The children with missing previous samples were considered at risk for that time period, as long as they had not previously been sensitized and had a nonmissing value for age at the end of the time period. To evaluate whether the association between lifestyle and prevalence of sensitization of the respective categories of allergens varied with age, we used generalized estimating equation models with an unstructured correlation matrix and included an interaction term between lifestyle and age as a continuous variable. The significance level was set at .05 (2-sided). Statistical analyses were performed with R v3.1.3 (R Foundation for Statistical Computing, Vienna, Austria) and SAS v9.4 (SAS Institute, Cary, NC) software.Table E1Point prevalence of IgE sensitization against different allergens at 6, 12, 24, and 60 months of age in children from families with anthroposophic, partly anthroposophic, and nonanthroposophic lifestylesAnthroposophic, n/N (%)Partly anthroposophicn/N (%)Nonanthroposophic, n/N (%)Sensitization at 6 mo Any allergen∗Differences were significant at P values of less than .05.2/71 (2.8)14/160 (8.8)25/139 (18)Food∗Differences were significant at P values of less than .05.1/75 (1.3)12/172 (7.0)22/143 (15.4)Milk∗Differences were significant at P values of less than .05.0515Egg1911Peanut032Animal1/71 (1.4)3/160 (1.9)7/139 (5.0)Cat124Dog013Pollen0/73 (0)0/162 (0)0/140 (0)Birch000Timothy000Sensitization at 12 mo Any allergen∗Differences were significant at P values of less than .05.3/71 (4.2)23/167 (13.8)37/139 (26.6)Food∗Differences were significant at P values of less than .05.2/75 (2.7)21/170 (12.4)37/145 (25.5)Milk∗Differences were significant at P values of less than .05.01117Egg∗Differences were significant at P values of less than .05.21224Peanut076Animal1/70 (1.4)4/167 (2.4)8/137 (5.8)Cat125Dog025Pollen0/74 (0)0/167 (0)1/137 (0.7)Birch001Timothy001Sensitization at 24 mo Any allergen∗Differences were significant at P values of less than .05.13/86 (15.1)22/166 (13.3)35/147 (23.8)Food8/86 (9.3)19/169 (11.2)27/148 (18.2)Milk81619Egg∗Differences were significant at P values of less than .05.3816Peanut087Animal∗Differences were significant at P values of less than .05.2/86 (2.3)3/167 (1.8)11/147 (7.5)Cat228Dog∗Differences were significant at P values of less than .05.038Pollen4/86 (4.7)6/166 (3.6)9/148 (6.1)Birch456Timothy025Sensitization at 60 mo Any allergen∗Differences were significant at P values of less than .05.14/68 (20.6)22/123 (17.9)37/97 (38.1)Food∗Differences were significant at P values of less than .05.8/68 (11.8)11/123 (8.9)28/97 (28.9)Milk∗Differences were significant at P values of less than .05.5722Egg∗Differences were significant at P values of less than .05.6314Peanut∗Differences were significant at P values of less than .05.239Animal∗Differences were significant at P values of less than .05.3/68 (4.4)7/123 (5.7)15/97 (15.5)Cat∗Differences were significant at P values of less than .05.3512Dog∗Differences were significant at P values of less than .05.2511Pollen9/68 (13.2)12/123 (9.8)16/97 (16.5)Birch899Timothy51013∗ Differences were significant at P values of less than .05. 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