Arshad, Syed Hasan

Dean, Tara

Glasbey, Gill

Glueck, Deborah

Grundy, Jane

Maslin, Kate

Mitchell, Frances

Palumbo, Michaela

Potter, Stephen

Venter, Carina

English

Background: The association between maternal and infant dietary exposures and risk of allergic disease development is an area of considerable scientific uncertainty.Objective: This study aims to compare dietary habits during pregnancy and lactation in two pre-birth cohorts from the same location approximately 10 years apart, a timeframe characterised by changes in government dietary advice.Methods: The FAIR cohort is an unselected birth cohort born between 2001-2002. The 3rd generation cohort was born between 2010-2018. Both cohorts were established on the Isle of Wight (UK) to investigate prevalence of allergic diseases. Nutrition and allergy data was collected prospectively from recruitment and throughout the infant’s early life. Here we present dietary data collected in the third trimester of pregnancy and at three months of age. Differences between cohorts were tested using t-tests, Wilcoxon rank sum tests, chi-squared and Fisher’s exact tests.Results: Data was available for 1331 participants (969 FAIR and 362 3rd generation). The proportion of mothers that reported excluding peanuts during pregnancy was significantly lower for the 3rd generation compared to the FAIR cohort (16.0% vs. 55.6%, p &lt; 0.01). Cohort membership, primiparity, and maternal education were significantly associated with excluding peanuts during pregnancy (p &lt; 0.01). The proportion of mothers who reported excluding any foods during breastfeeding was significantly lower for the 3rd generation compared to the FAIR cohort (22.8% vs. 43.4%, p &lt; 0.01).Conclusion: Maternal exclusion of peanut during pregnancy was lower for mothers giving birth between 2012-2018, compared to mothers giving birth between 2001-2002

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1  "Temporal change in maternal dietary intake during pregnancy and lactation between and 1 within two pregnancy cohorts assembled in the United Kingdom" 2 Kate Maslin1,2 PhD, Carina Venter2,3,4 PhD, Michaela Palumbo5 MSc, Deborah Glueck4,5 PhD, 3 Frances Mitchell2 MSc, Stephen Potter2, Jane Grundy2 RN, Gill Glasbey2, Tara Dean2,6 PhD & 4 Syed Hasan Arshad2,7 PhD. 5 1. School of Nursing and Midwifery, University of Plymouth, United Kingdom. 6 2. David Hide Asthma and Allergy Centre, Isle of Wight, United Kingdom. 7 3. Children’s Hospital Colorado, United States. 8 4. Department of Pediatrics, University of Colorado School of Medicine, United States  9 5. Lifecourse Epidemiology of Adiposity and Diabetes (LEAD) Center, University of 10 Colorado Denver, United States. 11 6. University of Brighton, United Kingdom. 12 7. Clinical and Experimental Sciences, University of Southampton, United Kingdom. 13 Corresponding author: Dr. Kate Maslin, School of Nursing and Midwifery, Drake Circus, 14 University of Plymouth, Plymouth, Devon, PL4 8AA, UK.  15 Email address: maslinkate@gmail.com 16 Phone: (+44) 01752 586 500 17 Clinical implications: 18 Advice regarding peanut intake during pregnancy has changed over the last 20 years. Future 19 guidance on peanut intake during pregnancy, lactation and complementary feeding should be 20 clearly communicated by the government and professional bodies, to prevent unnecessary 21 dietary exclusion. 22 Key words: pregnancy, lactation, allergy prevention, maternal diet, maternal nutrition, 23 peanut, birth cohort.   24 2  Abstract 25 Background: The association between maternal and infant dietary exposures and risk of 26 allergic disease development is an area of considerable scientific uncertainty. 27 Objective: This study aims to compare dietary habits during pregnancy and lactation in two 28 pre-birth cohorts from the same location approximately 10 years apart, a timeframe 29 characterised by changes in government dietary advice. 30 Methods: The FAIR cohort is an unselected birth cohort born between 2001-2002. The 3rd 31 generation cohort was born between 2010-2018. Both cohorts were established on the Isle of 32 Wight (UK) to investigate prevalence of allergic diseases. Nutrition and allergy data was 33 collected prospectively from recruitment and throughout the infant’s early life. Here we 34 present dietary data collected in the third trimester of pregnancy and at three months of age. 35 Differences between cohorts were tested using t-tests, Wilcoxon rank sum tests, chi-squared 36 and Fisher’s exact tests. 37 Results: Data was available for 1331 participants (969 FAIR and 362 3rd generation). The 38 proportion of mothers that reported excluding peanuts during pregnancy was significantly 39 lower for the 3rd generation compared to the FAIR cohort (16.0% vs. 55.6%, p < 0.01). Cohort 40 membership, primiparity, and maternal education were significantly associated with 41 excluding peanuts during pregnancy (p < 0.01). The proportion of mothers who reported 42 excluding any foods during breastfeeding was significantly lower for the 3rd generation 43 compared to the FAIR cohort (22.8% vs. 43.4%, p < 0.01).  44 Conclusion: Maternal exclusion of peanut during pregnancy was lower for mothers giving birth 45 between 2012-2018, compared to mothers giving birth between 2001-2002.  46   47 3  To The Editor 48 The association between maternal and infant dietary exposures and risk of allergic disease 49 development has been an area of considerable scientific uncertainty and debate in recent 50 years (1). Overall research has been largely inconclusive, with no evidence supporting 51 maternal exclusion diets for the prevention of food allergy or atopic disease in the offspring 52 (2). The inconsistency in scientific evidence is reflected in contradictory dietary guidelines 53 about peanut intake over the past 20 years. In the United Kingdom, the Department of Health 54 issued a report in 1998, advising that pregnant mothers with a family history of atopy should 55 avoid peanuts during pregnancy/lactation (3). Ten years later, this advice was no longer 56 deemed appropriate and was rescinded based on data from our group (4, 5) (see Figure 1). 57 Similar advice was recommended internationally. Since then, the concept that exposure to 58 potential food allergens could be protective of allergic disease has now been widely adopted. 59 The aim of this study was to compare dietary habits during pregnancy and lactation in two 60 allergy birth cohorts born in the same geographical location approximately 10 years apart.  61 The FAIR cohort is a whole population birth cohort born on the Isle of Wight, United 62 Kingdom, between 2001-2002 (n = 969) (Figure 1).   Demographic, socioeconomic and family 63 history of allergy information was collected from pregnant women at 12 weeks gestation. 64 A validated food frequency questionnaire was completed at 36 weeks gestation (6) (see file 1 65 in online repository). Information about infant feeding was collected prospectively via a 66 standardized questionnaire at 3 and 6 months postpartum. The 3rd generation cohort is the 67 offspring of the Isle of Wight Whole Population Birth Cohort (n = 1456), born in 1989. 68 Participants of this cohort were followed up to 27 years of age. Since 2010 their offspring have 69 been enrolled in the 3rd generation study (7).  The majority of 3rd generation participants were 70 recruited antenatally at 12 weeks gestation. Dietary data was collected by questionnaire at 28 71 weeks gestation using a modified version of the FAIR questionnaire and again at 3 and 6 72 4  months postpartum (6). Details of statistical methods are included in supplementary file 2. 73 Ethical approval for both studies was obtained from the Isle of Wight, Portsmouth and South 74 East Hampshire Research Ethics Committee. 75 Data was available for 1331 participants (969 FAIR and 362 3rd generation). Maternal 76 characteristics are shown in Table E1 (supplementary file 2). The proportion of mothers that 77 reported excluding peanuts during pregnancy was significantly lower for the 3rd generation 78 compared to the FAIR cohort (16.0% vs. 55.6%, p < 0.01).  Results of the multivariable logistic 79 regression model showed that cohort membership, primiparity, and maternal education were 80 significantly associated with excluding peanuts during pregnancy (supplementary file 1, Table 81 E2). Specifically, 3rd generation mothers had 0.18 times the odds of excluding peanuts during 82 pregnancy compared to FAIR mothers (OR: 0.18, 95% CI: 0.12-0.27, p < 0.01). First time 83 mothers had 65% greater odds of excluding peanuts during pregnancy (OR: 1.65, 95% CI: 1.25-84 2.17, p < 0.01). Vegetarian diet, maternal food allergy, and maternal age were not significantly 85 associated with exclusion of peanuts during pregnancy.    86 Figure 2 illustrates differences between the FAIR and 3rd generation cohorts in terms 87 of maternal frequency of consumption of key food allergens during pregnancy. A significantly 88 greater proportion of 3rd generation mothers reported regular consumption (once per week 89 or more) of peanuts, tree nuts, and seeds during pregnancy compared to FAIR mothers  (all p 90 < 0.01).  Information regarding infant feeding and maternal dietary intake during lactation is 91 shown in Table E1 (supplementary file 2). The proportion of mothers who reported excluding 92 any foods during breastfeeding was significantly lower for the 3rd generation compared to the 93 FAIR cohort (22.8% vs. 43.4%, p < 0.01).  94 Figure 3 shows that among participants from the 3rd generation cohort only, exclusion 95 of peanuts during pregnancy showed a decreasing trend over time from 2013 to 2018. The 96 results of the multivariable logistic regression model found an overall significant difference in 97 5  the proportion of mothers excluding peanuts during pregnancy between any of the offspring 98 years of birth (Wald X2 = 10.27, df = 4, p = 0.036). Results of the pairwise tests (Table E3 99 supplementary file 2) found that women who gave birth in 2017 had 0.1 times the odds of 100 excluding peanuts during pregnancy compared to women who gave birth in 2013 (OR: 0.10, 101 95% CI: 0.02-0.57, p = 0.01). Primiparity, maternal education, maternal food allergy, nor 102 maternal age were significantly associated with exclusion of peanuts during pregnancy among 103 the 3rd generation participants. 104 Dietary data on peanut consumption may not be consistently reported as peanuts are 105 not usually differentiated from tree nuts and may be included under broad categories (e.g. 106 “nuts and seeds”) (8). Qualitative research with mothers of young children suggests that 107 peanuts are considered primarily in the form of whole peanuts, or in the form of peanut 108 butter, rather than being ingredients in food, meaning that study participants may in fact 109 consume more than they realise (8). In both the FAIR and 3rd generation studies, the same 110 validated questionnaire was used (6), which separated peanut, tree nuts and seeds into 111 different categories and gave several examples for each item (supplementary file 1).  Research 112 from the Europrevall birth cohort study, a multicentre study in nine European countries 113 indicated wide practices in peanut intake; with only 2.7% of Dutch women avoiding eating 114 peanut in pregnancy, compared to 44.4 % of British women (8). In addition, pregnant women 115 in the UK were the highest avoiders of peanut and tree nuts (16.8%) compared to the other 116 eight countries. The UK was the only country at the time to have any national guidance on 117 peanut consumption during pregnancy, advocating peanut avoidance in high-risk families. 118 Against a backdrop of changing scientific evidence surrounding food allergy 119 prevention, the importance of providing clear dietary advice to the public, is paramount. In 120 the case of peanut exclusion variations in information provision, a lack of clarity in relation to 121 risks and the importance of atopy have been highlighted as potential issues (9). Due to this 122 confusion, there has been a concern that the 1998 advice (3) could possibly have increased 123 6  the prevalence of peanut allergy in the UK, as the advice may have been acted upon by non–124 high-risk families, to whom the advice was not targeted (4, 10). Ongoing data collection by 125 our group of the 3rd generation participants will allow us to assess whether any changes in 126 peanut sensitisation and clinical allergy have occurred as a result of changes in their dietary 127 behaviour. 128 A strength of this study is that it was conducted in one area of the UK, although this 129 limits external generalization. There were some differences between the two cohorts, 130 meaning there is a risk of residual confounding. Maternal food allergy was self-reported and 131 data was collected at one pregnancy time point. In conclusion, maternal exclusion of peanut 132 during pregnancy was lower for mothers giving birth between 2012-2018 when compared to 133 mothers giving birth between 2001-2002. These results align with the change in government 134 dietary advice in 2008 and a paradigm shift towards exposure to dietary allergens via infant 135 feeding, as a preventative approach to food allergy in infancy. 136 Funding: The FAIR study was funded by the Food Standards Agency UK and the 3rd generation 137 cohort study is supported by two National Institute of Health R01 project grants (R01- 138 HL132321-01A1 and R01-AI091905). The sponsor and funders played no role in the study 139 design; in the collection, analysis, and interpretation of data; in the writing of the report; and 140 in the decision to submit the article for publication. The researchers acted independent of the 141 funders.  142 Conflicts of interest: None declared. 143 Acknowledgements:  We would like to thank the participants of both studies. The authors are 144 grateful to research nurses C Bernadette Clayton, Deborah Frazer and Maria Larsson at the 145 David Hide Asthma & Allergy Research Centre, Isle of Wight, UK for their help in recruitment 146 and sample collection.  147  148 7  References 149 1. Prescott SL. Early-life environmental determinants of allergic diseases and the wider 150 pandemic of inflammatory noncommunicable diseases. J Allergy Clin Immunol. 151 2013;131(1):23-30. 152 2. Garcia-Larsen V, Ierodiakonou D, Jarrold K, Cunha S, Chivinge J, Robinson Z, et al. Diet 153 during pregnancy and infancy and risk of allergic or autoimmune disease: A systematic review 154 and meta-analysis. PLoS Med. 2018;15(2):e1002507. 155 3. Committee on Toxicity of Chemicals in Food CPa, (COT) tE. Adverse reactions to Food 156 and Food Ingredients. 1998. 157 4. Dean T, Venter C, Pereira B, Grundy J, Clayton CB, Higgins B. Government advice on 158 peanut avoidance during pregnancy--is it followed correctly and what is the impact on 159 sensitization? Journal of human nutrition and dietetics : the official journal of the British 160 Dietetic Association. 2007;20(2):95-9. 161 5. Committee on Toxicity of Chemicals in Food CPatE. Statement on the review of the 162 1998 COT recommendations on peanut avoidance. 2008. 163 6. Venter C, Higgins B, Grundy J, Clayton CB, Gant C, Dean T. Reliability and validity of a 164 maternal food frequency questionnaire designed to estimate consumption of common food 165 allergens. Journal of Human Nutrition and Dietetics : the official journal of the British Dietetic 166 Association. 2006;19(2):129-38. 167 7. Arshad SH, Karmaus W, Zhang H, Holloway JW. Multigenerational cohorts in patients 168 with asthma and allergy. The Journal of allergy and clinical immunology. 2017;139(2):415-21. 169 8. Oliver EM, Grimshaw KE, Schoemaker AA, Keil T, McBride D, Sprikkelman AB, et al. 170 Dietary habits and supplement use in relation to national pregnancy recommendations: data 171 from the EuroPrevall birth cohort. Maternal and child health journal. 2014;18(10):2408-25. 172 8  9. Turke J, Venter C, Dean T. Maternal experiences of peanut avoidance during 173 pregnancy/lactation: an in-depth qualitative study. Pediatric allergy and immunology : official 174 publication of the European Society of Pediatric Allergy and Immunology. 2005;16(6):512-8. 175 10. Hourihane JO, Aiken R, Briggs R, Gudgeon LA, Grimshaw KE, DunnGalvin A, et al. The 176 impact of government advice to pregnant mothers regarding peanut avoidance on the 177 prevalence of peanut allergy in United Kingdom children at school entry. The Journal of Allergy 178 and Clinical Immunology. 2007;119(5):1197-202. 179 180 9  Figure legends Figure 1: Timeline illustrating the two different cohorts and timing of dietary recommendations and new guidance. COT: Committee on Toxicity of Chemicals in Food (5).  FAIR: Food Allergy and Intolerance Research Study.  LEAP: Learning Early About Peanut Allergy (11).  Figure 2. Percent of participants in the FAIR and 3rd generation cohorts that regularly consumed various food allergens during the third trimester of pregnancy. *Significant difference at Bonferroni-corrected alpha level: p < 0.0001 Figure 3. Percent of 3rd generation cohort participants that excluded peanut during pregnancy by child’s year of birth (with exact 95% confidence limits). Due to a small number of observations (n=2) with a birth year of 2012, Figure 3 only presents data from births between 2013 and 2018.      Supplementary file 1 Excerpt from FAIR pregnancy questionnaire  Q1. Please tick all of the following statements that are applicable to you:  a. I am following a normal diet       O Yes  O No  b. I am following a vegetarian diet      O Yes  O No   c. I am following a vegan diet       O Yes  O No   d. I am excluding raw eggs, unpasteurised soft cheese,    O Yes  O No  liver etc. due to my pregnancy  e. I am excluding PEANUTS due to my pregnancy    O Yes  O No   f. I am following a special diet due to medical reasons    O Yes  O No (please state medical condition) ………………………  g. I am excluding certain foods due to personal choice (please list foods) O Yes  O No    ………………………   Q2.On average, how often have you eaten these foods during pregnancy?  Never Rarely (1-2 or less per month)  Occasionally (1-3 per week)  4 or more times per week  Uncertain  Milk and milk products (e.g. custard, yoghurt, ice cream, chocolate, butter, margarines, cheese – pizza, cheese sauce, lasagne, cheesy biscuits)         Egg (e.g. omelettes, flans, meringues, cakes, cookies, batter mixes, egg pasta, quorn, mayonnaise, quiches)         Wheat (e.g. bread, cereals, pasta, pizza, cakes, pies, pastry)            White fish (e.g. tuna, fish cakes, battered fish, fish fingers)            Shellfish (e.g. crab, prawns, shrimp, lobster, crayfish)            Oily fish (e.g. mackerel, salmon, sardines, pilchards, herring, kipper, white bait, trout, crab, FRESH tuna)            Peanuts (e.g. Bombay mix, peanut butter, peanut brittle, peanut cookies, sate, some vegetarian meals)          Tree nuts - almonds, brazil nuts, pecan nuts, hazel nuts, walnuts etc (e.g. in chocolate, crunchy nut cornflakes, stuffing mix, sweet mincemeat, choc chip cookies, almond slice, marzipan, pesto sauce. Vegetarian meals, Greek desserts like baklava)           Seeds – sesame, poppy, sunflower (e.g. on bread rolls, tahini paste)        Citrus Fruits (e.g. orange, tangerine, grapefruit, lemon, lime)           

Temporal change in maternal dietary intake during pregnancy and lactation between and within 2 pregnancy cohorts assembled in the United Kingdom

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Temporal change in maternal dietary intake during pregnancy and lactation between and within 2 pregnancy cohorts assembled in the United Kingdom

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