- Email: [email protected]
Association between early introduction of fruit juice during infancy and childhood consumption of sweet-tasting foods and beverages among children exposed and unexposed to gestational diabetes mellitus in utero
Accepted Manuscript Association between early introduction of fruit juice during infancy and childhood consumption of sweet-tasting foods and beverages among children exposed and unexposed to gestational diabetes mellitus in utero Camille Dugas, Julie Perron, Isabelle Marc, S. John Weisnagel, Julie Robitaille PII:
S0195-6663(17)31432-0
DOI:
10.1016/j.appet.2018.08.033
Reference:
APPET 4014
To appear in:
Appetite
Received Date: 27 September 2017 Revised Date:
7 August 2018
Accepted Date: 28 August 2018
Please cite this article as: Dugas C., Perron J., Marc I., Weisnagel S.J. & Robitaille J., Association between early introduction of fruit juice during infancy and childhood consumption of sweet-tasting foods and beverages among children exposed and unexposed to gestational diabetes mellitus in utero, Appetite (2018), doi: 10.1016/j.appet.2018.08.033. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
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Association between early introduction of fruit juice during infancy and childhood consumption of sweet-tasting foods and beverages among children exposed and unexposed to gestational diabetes mellitus in utero
Camille Dugas, M.Sc.a,b,c, Julie Perron, M.Sc.b, Isabelle Marc, MD, PhDc, S. John Weisnagel, MD c,d, Julie Robitaille, PhDa,b,c
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School of Nutrition, Laval University. 2425 rue de l‘Agriculture, Quebec City, Canada, G1V 0A6.b Institute of Nutrition and Functional Foods (INAF), Laval University. 2440 Boulevard Hochelaga, Quebec City, Canada, G1V 0A6.c Endocrinology and Nephrology Axis, CHU de Québec Research Center. 2705 boulevard Laurier, Quebec City, Canada, G1V 4G2.d Diabetes Research Unit, Laval University Medical Research Center. 2705 boulevard Laurier, Quebec City, Canada, G1V 4G2.
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Address for correspondence and reprint request:
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Julie Robitaille, RD, PhD, Professor, School of Nutrition. Institute of Nutrition and Functional Foods (INAF), Laval University. Pavillon des services, Room 2729N, Quebec City, Qc, G1V0A6, Canada. Email: [email protected] T: 418.656.2131 ext: 4458
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Abstract
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Background Children exposed to gestational diabetes mellitus (GDM) in utero are at
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high-risk of obesity. Given that nutritional habits can track from infancy to childhood, the
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aim of this study was to evaluate the association between the timing of fruit juice
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introduction in infancy and later consumption of sweet-tasting foods and beverages
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among children exposed (GDM+) and unexposed (GDM-) to GDM. Methods A total of
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107 GDM+ and 59 GDM- participated in the project. Data on the timing of fruit juice
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introduction during infancy were retrospectively collected for 62 GDM+ and 32 GDM-
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children. Current dietary intakes were collected with two 24-hour dietary recall
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questionnaires. Children were divided into groups according to the median timing of
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juice introduction (9 months). Results Mean age of children was 6.3±2.6 and 7.6±3.7
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years for GDM+ and GDM- children, respectively (p=0.08). Mean age of fruit juice
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introduction was similar between groups (p>0.05). Consuming >1 serving of fruit juice
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per day was 2.72 times more prevalent among GDM+ children introduced to fruit juice
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<9 months, compared to GDM+ children introduced ≥9 months (CI: 1.19-6.20). This
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association was not observed in the GDM- group. The timing of fruit juice introduction
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was not associated with later consumption of sweets, desserts and sweet-tasting
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beverages when adjustment for children’s age was made among GDM+ and GDM-
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children. Conclusion Early introduction of fruit juice in infant diet is associated with
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higher prevalence of consumption of >1 serving of fruit juice per day in GDM+ children.
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Key words: early life nutrition, juice consumption, sweet, dietary habits
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Introduction
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Children born to mothers with gestational diabetes mellitus (GDM) are at high risk of
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developing obesity and type 2 diabetes later in life (1, 2). There is a lack of effective
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postnatal strategies to prevent these complications among these high-risk children (3)
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although it is well established that healthy lifestyle behaviours are associated with a
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reduced risk of obesity among children in the general population (4). On the other hand,
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despite efforts made to promote a healthy diet among children, consumption of high
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amounts of ultra-processed foods and beverages rich in free sugar, like fruit juice, sugar-
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sweetened beverages (SSB), pastries and candies is highly prevalent among Canadian
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children (5).
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Preference for sweetness is innate among newborns and this preference generally remains
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during childhood (6). However, pre- and postnatal experiences, like exposure to different
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flavors during in utero and early postnatal periods, can modulate taste preferences (7).
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The introduction of complementary foods in the infant diet represents also a critical
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period for flavor experiences in early life, particularly among non-breastfed children that
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have been exposed since birth to only the flavour of formula (8). Moreover, increasing
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evidence suggests that food preferences in children would depend on foods offered and
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the context of feeding during early life (8). In fact, both healthy and unhealthy dietary
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patterns established during infancy can track into childhood (9). Accordingly, some
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authors evaluated the association between SSB and fruit juice consumption in infancy
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and their later consumption in childhood and found that consumption of these types of
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beverages in early life was positively associated with their consumption during childhood
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3 Abbreviations GDM: gestational diabetes mellitus SSB: sugar sweetened beverage STB: sugar-tasting beverage
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(10, 11). However, to our knowledge, no such study has been conducted among children
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exposed to GDM in utero. Given their in utero exposure to an environment rich in
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glucose, it is possible that taste development in these children could differ from children
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unexposed to GDM, particularly developmental preferences for sweet tasting foods,
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which could impact food habits. In fact, previous research has shown that fetal
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environment could be involved in food preferences programming (12).
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While it is well recognized that SSB have a negative impact on children’s health (13),
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fruit juice is generally considered a healthier food option by parents. In fact, 100% fruit
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juice is considered as a serving of fruits in the 2007 Canada’s Food Guide, which could
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encourage parents to introduce fruit juice early in their infant’s diet (14), without
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consideration for the sweet taste of this type of beverage. Thus, given that food habits
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could track from infancy to childhood (15, 16), and in order to identify new targets for
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prevention of obesity development among children exposed (GDM+) to GDM in utero,
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the primary objective of this study was to evaluate the association between early
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introduction of fruit juice during infancy and childhood consumption of sweet-tasting
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foods and beverages among GDM+ children. Secondly, we evaluated the association
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between early introduction of fruit juice and childhood consumption of sweet-tasting
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foods and beverages among a group of children unexposed (GDM-) to GDM in utero, in
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order to compare results between groups.
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Material and methods
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Population
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All subjects were participants in a cohort study that aims to evaluate the impact of GDM
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on mother’s and children’s health and to examine whether a healthy postnatal
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environment could attenuate the adverse consequences of in utero exposure to GDM.
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This study takes place at the Institute of Nutrition and Functional Foods (INAF), at Laval
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University (Quebec City, Canada), and recruits women with and without a history of
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GDM and their children. Participants were recruited from a previous project conducted
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by our research team that has been previously described (17). Additionally, recruitment is
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conducted through access to medical records from the two major hospitals with a
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neonatal care unit in the metropolitan area of Quebec City (Hôpital Saint-François
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d’Assise and Centre Hospitalier de l’Université Laval-CHUL). Recruitment is also
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conducted by emails sent to Laval University community as well as posts on healthcare
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websites and on social media (Facebook). Children with a history of in utero exposure to
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GDM between 2003 and 2013 are included in the study and children exposed to type 1 or
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type 2 diabetes are excluded. Children from the control group had to be born to a mother
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that never have had diabetes (Type1, 2 or GDM) before or after the index pregnancy. To
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date, a total of 107 children exposed (GDM+) and 59 children unexposed (GDM-) to
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GDM in utero have participated in the project. Written consents were obtained from all
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participating mothers and children and ethical approval was obtained from the Laval
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University Ethics Committee (2011-196-A-4 R-3) and from the Centre Hospitalier
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Universitaire de Québec Ethics Committee (2015-2031). This study is registered in the
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Clinical Trials.gov registry (NCT01340924).
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Exposure
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Children came with their mother to the INAF research center for a single 1-hour visit.
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During this visit, data about the timing of fruit juice introduction were retrospectively
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collected by a self-administrated questionnaire completed by the mother of each child.
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Mothers were asked when their child drank fruit juice, defined as 100% pure juice, for
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the first time (infant age given in months and/or weeks). A randomly selected subsample
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of participants (n=20) completed this questionnaire for a second time at home, within a 2
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weeks interval between each completion, in order to evaluate the reliability of answers
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given for this questionnaire. Results of the reliability test showed a strong correlation
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between answers given for the completion of both infant feeding questionnaires (r=0.81,
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p < 0.001).
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Outcomes
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In order to estimate current dietary intakes of children, a 24-hour dietary recall (24HDR)
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was conducted with a trained dietitian using the 5 steps of the Automated Multiple-Pass
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Method (AMPM): 1) quick list of the food items consumed 2) reminder of the food items
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frequently forgotten 3) time and type of meals 4) details about serving size consumed,
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brand name of commercial products, ingredients and methods of homemade foods 5)
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review of the dietary recall (18). All food and drink items consumed in the previous day,
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from midnight to midnight, were recorded. Three-dimensional food models were used to
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enhance accuracy of portion size estimates. Mothers of children younger than 10 years
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were asked to complete the 24HDR whereas children were present during the interview
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and were asked to add information if needed (i.e. for food consumed outside home). For
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children ≥10 years, the 24HDR was completed directly by the child, with the help of the
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mother if needed (i.e. for food preparation details). A second 24HDR was completed over
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the phone with the mother following the same validated method, the AMPM (18), 7-10
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days after their visit. Mean intakes for the two questionnaires were used in analyses.
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Dietary intake data were analyzed using Nutrition Data System for Research (NDSR)
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(19, 20). From this software, reports can be extracted by nutrients or by food group
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categories for each participant. In order to extract data regarding sweet-tasting foods and
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beverages, the Nutrition Coordinating Center (NCC) Food Group Count System from
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NDSR was used (19, 20). The NCC Food Group Count System is composed of 9 groups
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and 168 subgroups of foods, based on recommendations made by the Dietary Guidelines
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for Americans and the USDA Food Guide Pyramid. For the purpose of this study, groups
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and subgroups of foods containing high amount of sugar (21) or known for their sweet
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taste were extracted and compiled together to form 4 foods and beverages groups. These
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groups were used in analyses, with a description of a portion size provided bellow:
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(125 ml).
2- Sweet-tasting beverages (STB), which include sweetened and artificially
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1- Fruit juice, defined as 100% pure juice, which include citrus and non-citrus juice
sweetened soft drinks, fruit drinks, tea and water (125 ml). 3- Desserts, which include cakes (55g to 125g), cookies (30g), pies, cobblers and
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pastries (125g), danish and doughnuts (55g).
4- Sweets, which include sugar (4g), syrup (30-60 ml), honey, jam and molasses (15 ml), fudge, caramel and chocolate syrup (30 ml), candy, chocolate candy and gum
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drops (40g), frosting or glaze (35g) and sweetened flavored milk beverage powder
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(1 cup prepared).
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Children were categorised as non-consumers (0 serving/d), consumers (>0 serving /day)
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or high consumers (>1 serving/day) of the 4 different sweet-tasting food and beverage
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groups described above.
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Statistical analyses
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Descriptive statistics were calculated as mean ± standard deviation (SD) or as percentage
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(%). Participant’s characteristics and dietary intakes during childhood of GDM+ and
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GDM- children were compared using Student t-test, Chi-squared test (χ2) or Fisher’s
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exact test (when cell number was <5). GDM+ and GDM- children were divided into
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groups according to the median timing of fruit juice introduction during infancy, which
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was 9 months. Fisher’s exact test and χ2 test were performed to evaluate the distribution
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of children across different groups of consumers and high consumers of sweet tasting
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food and beverages among GDM+ and GDM- children. Finally, prevalence ratios (PR)
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using log binominal model were calculated to evaluate the prevalence of consumers and
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high consumers of food items from the different food groups in children introduced to
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fruit juice before 9 months compared to those introduced at 9 months or later among
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GDM+ and GDM- children. Given the low prevalence of children who consumed >1
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serving of STB per day in both groups, the PR of high consumption of STB was not
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computed. Finally, stepwise regression analyses were performed to determine which
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cofactors should be included in the adjusted models among the following: breastfeeding
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duration, timing of solid food introduction, children’s sex and age, maternal education
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level and family incomes. Accordingly, analyses were only adjusted for children’s age.
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The p value ≤0.05 and confidence interval (CI) of 95% were used to identify statistically
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significant results. SAS software, version 9.4, was used for analyses.
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Results
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A total of 107 GDM+ and 59 GDM- children were recruited, but only 62 GDM+ and 32
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GDM- children had complete information regarding the timing of fruit juice introduction.
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Within the subsample with missing information, 9 mothers did not answer the specific
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question regarding the timing of fruit juice introduction and 63 gave the answer “I don’t’
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know” to this question. Thus, analyses included the 94 children with complete
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information. Among GDM+ children without data on fruit juice introduction (n=45), a
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lower proportion had been breastfed compared to children included in analyses (80%
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compared to 95%, p=0.03). However, there was no difference regarding children’s age
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and sex, maternal education level, family incomes and the timing of solid food
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introduction (results not shown). There was also no statistically significant difference in
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characteristics of GDM- children included and excluded from analyses. Characteristics of
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the 94 participating children are presented in Table 1. Overall, 77 % and 78% of GDM+
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and GDM- children received fruit juice during the first year of life, respectively.
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Table 1. Participants’ characteristics
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Characteristics
Mean ± SD or n (%) GDM+
GDM-
P value
N=62
N=32
6.3±2.6
7.6±3.7
0.08
2-5 (years)
29 (47.8)
12 (37.5)
0.10
6-9 (years)
25 (40.3)
10 (31.3)
10-14 (years)
8 (12.9)
10 (31.3)
Boys
32 (51.6)
11 (34.4)
Demographic Age (years)
Sex 0.12 9
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Girls
30 (48.4)
21 (65.6)
0.04±0.98
-0.01±0.70
0.76
4 (7.7)
3 (11.5)
0.48
40 000 – 79 000
20 (38.5)
9 (34.6)
80 000- 99 999
13 (25.0)
3 (11.5)
>100 000
15 (28.9)
11 (42.3)
High school
12 (21.8)
4 (15.4)
College
7 (12.7)
2 (7.7)
University
36 (65.5)
BMI z-score (kg/m2)
0 – 39 000
0.65
20 (76.9)
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Maternal age
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Maternal education level
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Family income (CAD$/year)
38.0±4.2
37.1±4.5
0.33
27.7±7.7
26.2±5.0
0.24
2±0.7
2±0.6
0.62
58 (95)
27 (93)
0.66
8.9±7.8
10.1±4.6
0.39
Age of solid food introduction (months)c
4.9±1.0
4.9±1.3
0.81
Age of fruit juice introduction (months)
8.7±3.0
7.6±3.7
0.13
Maternal BMI Parity Infant feeding practices Breastfed infantsa
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Breastfeeding duration (months)b
Results are presented as mean ± SD or n (%) and were compared using Student t-test, chi-square test or Fisher’s exact test. BMI: body mass index. an=61 for GDM+ and n=29 for GDM-, bn=57 for GDM+ and n=27 for GDM-, cn=59 for GDM+ and n=29 for GDM-.
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During childhood, the average consumption of fruit juice was 0.92 serving of 125 ml per
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day for GDM+ and 1.13 servings for GDM- children, including children that did not
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consume any amount of fruit juice (Table 2). Among the consumers only, mean intake
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was 1.96 and 1.65 servings of 125 ml per day for GDM+ and GDM- children,
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respectively (results not shown). Similarly, mean intake for STB was 0.69 and 0.79
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serving per day for all GDM+ and GDM- children, respectively (Table 2). However, the
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average consumption of STB among consumers only was 1.02 and 0.94 serving of 125
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ml per day for GDM+ and GDM- children, respectively (results not shown). Frequency
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of consumption of any amount of fruit juice per day tended to be higher among GDM-
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than GDM+ children (p=0.05, Table 2).
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Table 2. Dietary intakes during childhood
GDM+
GDM-
Consumers (yes)
29 (46.8)
22 (68.8)*
High consumers (>125 ml)
18 (29.0)
11 (34.4)
0.92±1.57
1.13±1.36
Fruit juice
Mean intake (servings of 125 ml/d)
Consumers (yes)
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STB
21 (33.9)
14 (43.8)
9 (14.5)
3 (9.4)
Mean intake (servings of 125 ml/d)
0.69±1.41
0.79±1.38
Consumers (yes)
50 (80.6)
25 (78.1)
High consumers (>1 serving)
10 (16.1)
6 (18.8)
Mean intake (serving/d)
0.44±0.50
0.63±1.16
Consumers (yes)
38 (61.3)
19 (59.4)
High consumers (>1 serving)
15 (24.2)
7 (21.9)
Mean intake (serving/d)
0.69±1.02
0.49±0.57
1686±439
1790±585
High consumers (>125 ml)
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Energy intake (kcal)
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Sweets
Desserts
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Food groups
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Mean ± SD or n (%)
211 212 213 214 215
Fruit juice includes citrus and non-citrus 100% pure juice; sweet-tasting beverages (STB) include sweetened and artificially sweetened soft drinks, fruit drinks, tea and water; sweets include sugar, syrup, honey, jam, molasses, fudge, caramel, chocolate syrup, candy, chocolate candy, gum drops, frosting or glaze and sweetened flavored milk beverage powder; desserts include cakes, cookies, pies, pastries, danish, doughnuts and cobblers. *p=0.05.
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Among GDM+ children, consuming >125 ml of fruit juice per day was more frequent
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among children introduced to fruit juice earlier, i.e. before 9 months, compared to those
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introduced at 9 months or later (Table 3). Still among GDM+ children, the same pattern
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was seen for STB that were more frequently consumed, for any amount of STB as well as
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for >125 ml/d, among GDM+ children exposed to fruit juice earlier. However, no
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statistically significant difference was seen for the distribution of children who reported
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consuming any amount of desserts, sweets or fruit juice (>0 serving/d) or for high
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consumers of sweets and desserts (>1 serving/d), between GDM+ children exposed to
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fruit juice before and ≥ 9 months (Table 3). Among GDM- children, any amount of
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desserts tended to be more frequently consumed among children introduced to fruit juice
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<9 months (73.7% of consumers) compared to those introduced to fruit juice ≥9 months
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(26.3% of consumers, p=0.05, Table 3). No other difference was seen in the distribution
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of consumption of any food and beverage groups among GDM- children (Table 3).
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Table 3. Association between the timing of fruit juice introduction and consumption of
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sweet-tasting foods and beverages during childhood among GDM+ and GDM- children
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Introduced to juice < 9
Introduced to juice ≥ 9
months
months
N (%)
N (%)
p
15 (51.7)
14 (48.3)
0.22
>125 ml
12 (66.7)
6 (33.3)
0.02
Yes
13 (61.9)
8 (38.1)
0.04
>125 ml
8 (88.9)
1 (11.1)
0.008
Yes
20 (52.6)
18 (47.4)
0.07
>1 serving
8 (53.3)
7 (46.7)
0.38
Yes
24 (48.0)
26 (52.0)
0.10
>1 serving
6 (60.0)
4 (40.0)
0.25
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Childhood consumption GDM+ children
STB
Desserts
Sweets
Yes
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Fruit juice
GDM- children 12
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STB
Desserts
Sweets
Yes
12 (54.5)
10 (45.5)
0.22
>125 ml
8 (72.7)
3 (27.3)
0.17
Yes
10 (71.4)
4 (28.6)
0.14
>125 ml
2 (66.7)
1 (33.3)
0.45
Yes
14 (73.7)
5 (26.3)
0.05
>1 serving
5 (71.4)
2 (28.6)
0.27
Yes
15 (60.0)
10 (40.0)
0.33
>1 serving
3 (50.0)
3 (50.0)
0.31
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Fruit juice
The group “yes” refers to children who reported having consumed any amount of items from the specific food group. Fruit juice includes citrus and non-citrus 100% pure juice; sweet-tasting beverages (STB) include sweetened and artificially sweetened soft drinks, fruit drinks, tea and water; sweets include sugar, syrup, honey, jam, molasses, fudge, caramel, chocolate syrup, candy, chocolate candy, gum drops, frosting or glaze and sweetened flavored milk beverage powder; desserts include cakes, cookies, pies, pastries, danish, doughnuts and cobblers. P value was calculated with χ2 analyses and with Fisher’s exact test when cell number was <5.
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As seen in Table 4, GDM+ children introduced to fruit juice before 9 months did not
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have different PR for the consumption of any amount of fruit juice, sweets and desserts
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compared to GDM+ children introduced to fruit juice ≥ 9 months. However, consuming
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more than 125 ml of fruit juice per day was 2.72 times more prevalent among GDM+
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children introduced to fruit juice before 9 months, compared to those introduced at 9
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months or later (CI: 1.19-6.20). Although prevalence of consumption of any amount of
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STB in the crude model was 2.11 higher for GDM+ children exposed to fruit juice earlier
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(CI: 1.02-4.34, result not shown), this latter was no longer statistically significant after
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adjustment for children’s age (PR: 1.43, CI: 0.85-2.42, Table 4). Among GDM- children,
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the prevalence for the consumption of any amount or for >1 serving of any food and
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beverage groups was similar according to the timing of fruit juice introduction (Table 4).
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Table 4. Prevalence of consumption of sweet-tasting foods and beverages in GDM+ and
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GDM- children introduced to fruit juice <9 months compared to those introduced at or
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after 9 months of age
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Prevalence ratio
95% CI
Yes
1.56
(0.93; 2.60)
>125 ml
2.72
(1.19; 6.20)
STB
Yes
1.43
(0.85; 2.42)
Desserts
Yes
1.44
>1 serving
1.42
Yes
1.19
Sweets
>1 serving
-
GDM- children Yes
-
>125 ml STB
Yes
Desserts
Yes >1 serving Yes
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Sweets
>1 serving
(0.58; 3.49)
(0.94; 1.51) -
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Fruit juice
(0.97; 2.13)
SC
Fruit juice
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GDM+ children
-
1.67
(0.51; 5.45)
1.47
(0.55; 3.97)
1.63
(0.72; 3.71)
-
-
0.96
(0.64; 1.43)
0.35
(0.07; 1.61)
Table 4. Log-binominal regression analyses showing prevalence ratios with 95% CI for consumption of
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fruit juice, sweet-tasting beverages (STB), sweets, desserts, >125 ml of fruit juice and >1 serving of sweets
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and dessert in GDM+ and GDM- children introduced to fruit juice before 9 months compared to those
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introduced at 9 months or later (reference group). Increase prevalence of children consuming these food
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groups are above the 95% confidence limit of an agreement ratio of 1.00. Results presented are adjusted for
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children’s age.
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Given the small number in some cells, adjusted prevalence ratio could not be computed in some models.
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Discussion
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This study showed that early introduction of fruit juice during infancy, defined as before
261
9 months of age, is associated with a higher odds of consuming sweetened and artificially
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sweetened beverages and high amounts of fruit juice during childhood among GDM+
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children. The association between the timing of fruit juice introduction and odds of
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consuming >125 ml of fruit juice per day remained statistically significant after
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adjustment for children’s age, but the association between fruit juice introduction and
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later consumption of STB was no longer statistically significant after adjustment for
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children’s age. Among GDM- children, no statistically significant association between
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the timing of fruit juice introduction and consumption of sweet-tasting food and
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beverages during childhood was observed.
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Results of this study suggest that the prevalence of consumption of more than 1 serving
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of fruit juice per day was higher among GDM+ children exposed to fruit juice before 9
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months compared to those exposed to juice at or after 9 months. To our knowledge, this
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is the first study that evaluated the association between early life nutrition and food and
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beverage intakes during childhood among GDM+ children, which limits comparison of
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these results with the current literature. However, few studies conducted in the general
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population that investigated the association between SSB or juice intakes in infancy and
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beverage consumption in childhood showed similar results that these found in the GDM+
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group (10, 11). Analyses from the Infant Feeding Practices Study II (IFPS II), a national
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longitudinal study conducted in the United-States, showed that consuming SSB during
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the first year of life was associated with an increased risk of consuming SSB more than
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one time per day at the age of 6 years (10). In addition, Sonneville et al. showed that
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higher intakes of fruit juice at the age of 12 months was associated with a higher
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consumption of fruit juice and SSB in both early and mid-childhood when compared to
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infant that did not consume any amount of fruit juice at 12 months (11). More
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specifically, children consuming ≥16 oz of juice per day at 1 year consumed twice as
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much juice per day during childhood compared to those that did not consume any amount
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of juice at 1 year (2.4 vs 1.2 servings per day) (11).
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Our study showed no statistically significant association between the timing of fruit juice
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introduction during infancy and later consumption of foods containing high amount of
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sugar among GDM+ children. To our knowledge, no study has evaluated the association
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between juice introduction in infancy and later consumption of sweet foods in children
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exposed or unexposed to GDM in utero. However, Rose et al. evaluated the association
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between dietary patterns in early life and dietary patterns in childhood using data from
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the IFPS II (9). This study showed that infants having a high density energy diet at 9
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months, which included high amounts of juice, sweet foods and French fries, were greater
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consumers of SSB, sweet desserts and fried potatoes at 6 years, compared to other dietary
297
patterns in infancy (9). Liquid and solid foods have different properties. Indeed, sugars
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from liquid sources are associated with less satiety compared to sugar from solid foods,
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mainly due to the different fiber content (22). However, we are unaware of any published
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study evaluating the influence of the food matrix on taste development, thus it is unclear
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whether sugar intake from juice could affect taste preference for sugar from solid foods
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the same way that for sugar from liquids.
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Furthermore, this study showed no statistically significant association between the timing
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of fruit juice introduction and later consumption of sweet tasting food and beverages
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among GDM- children. The lack of association in the control group, which is not in
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agreement with studies conducted in the general population (9-11), could possibly be
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explained by the small number of participants in the GDM- group, which limits the
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statistical power to detect statistically significant results.
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The association between the timing of fruit juice introduction in infant diet and beverages
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consumption in childhood among GDM+ children could be explained in part by the
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development of taste preferences in early life. As mentioned earlier, it has been
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demonstrated that taste preferences track from infancy to childhood and that the early life
313
period could be a critical moment to program children’s dietary habits (8). In fact,
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nutritional experiences in early life have neurological programing effect that influence
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eating behaviour later in life (23). A study conducted in mice that evaluate the
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neuroanatomical development of the olfactory system showed that exposure through
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mother’s milk to odours that activate GFP-tagged olfactory receptors was associated with
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larger glomeruli in the olfactory bulb and with significant preferences for the activating
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odour (24). These results suggest that exposure to specific flavours during early life result
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in enhanced detection of these learned odours, which could facilitate their acceptance by
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children. Among studies conducted in humans, Pepino et al. demonstrated that infants
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who were routinely fed with sweet water in early life preferred high levels of sucrose in
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childhood, compared to those who were not routinely fed with sweet water in infancy,
324
highlighting the impact of early exposure to sweet on modulation of taste preference for
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sweetness (25). However, even if the early life period is recognized as critical for the
326
development of taste preferences, the exact timing to shift taste preferences is still
327
unknown (26). In order to answer this gap, a randomized clinical trial has been conducted
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among formula-fed infants to test whether the timing of introduction of protein
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hydrolysate formulas (PHF), known for their particularly unpleasant flavour, in infant
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diet would influence its acceptance later in infancy (27). This study showed that infant
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exposed to PHF earlier (i.e. at 1.5 and 2.5 months) consumed significantly more amount
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of PHF at 7.5 months compared to infants exposed later (i.e at 3.5 months) (27). Infants
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exposed to PHF at 3.5 months consumed the same amount of PHF at 7.5 months as
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infants from the control group who were fed with cow-milk base formulas (27). Thus,
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authors suggested that the window of opportunity to modulate taste preferences could
336
start to close as early as 3.5 months.
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Although we first hypothesized that early introduction of fruit juice in the infant diet
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would lead to an increased consumption of sweet-tasting foods and beverages, we only
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found associations with beverage intakes. As mentioned above, it is possible that the food
340
matrix of juice, a liquid with no fiber, would influence differently the consumption of
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beverages and solid foods because of their different properties (22). Furthermore, in
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addition to the taste preference theory, it has been suggested that fruit juice intake in
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infancy could be a gateway to later consumption of caloric beverages by establishing the
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habit of consuming these types of drinks (11). Similarly, the association between the
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timing of fruit juice introduction and its later consumption could also be explained by
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dietary habits established by parents during infancy that could remain during childhood.
347
In fact, it is possible to think that parents continue to feed their children the same types of
348
food from infancy to childhood, explaining associations seen for beverages but not for
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foods.
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Our study presents some limitations. First, given the cross-sectional study design, the
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timing of fruit juice introduction was retrospectively collected. This did not allow us to
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quantify the amount of juice intakes in infant diet neither the frequency of consumption
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during this period, which can have an impact on taste development and dietary habits.
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This study design is also at risk of recall bias, although our reliability test showed a
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strong correlation between answers given for the two completed questionnaires.
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Furthermore, mothers had the possibility to answer “I don’t know” to the question
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regarding the timing of juice introduction, which reduces risk of recall bias in our
358
analyses. In fact, it is possible to think that mothers that answered this question were
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confident of their answer. However, this study should be repeated using a prospective
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study design in order to limit this bias. Another limitation of the study is its small sample
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size, in both the GDM+ and GDM- groups, which increases the likelihood of type 2 error.
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Indeed, given the small sample size of participants in the control group (n=32), it is
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possible that the lack of association observed in this group is due to low statistical power.
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Furthermore, the homogeneity of participant’s characteristics (high income families with
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high education level) restricts our results to this study population only. Finally, this study
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did not evaluate specifically taste preferences of children, which limits interpretation of
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these results. In fact, Divert et al. showed that consumption of sweet tasting foods and
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beverages was not clearly associated with sweet liking, evaluated using a liking score, in
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a cohort study of school-aged children (28). Despite these limitations, this study presents
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several strengths. This is, to our knowledge, the first study that evaluated the impact of
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early life nutrition on dietary habits during childhood among children exposed to GDM in
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utero, a population at high-risk of many health problems such as obesity (1). Another
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strength is the use of two 24HDR to evaluate current dietary intakes of children. This
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allowed us to have quantitative data regarding food group intakes, while others studies
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generally use semi-quantitative questionnaires (10, 11). The use of two recalls, as it has
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been done by others in large population studies (29-31), helps to reduce the day-to-day
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variability of dietary intakes measured with 24HDR while minimizing the burden on
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participants (32). Finally, the fact that dietary questionnaires were conducted by a trained
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dietitian minimized risk of food misclassification, especially for fruit juice and fruit
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drinks.
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Conclusion
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This study suggests that early introduction of fruit juice in the infant diet is associated
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with higher prevalence of consumption of high amounts of fruit juice in GDM+ children.
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Further studies using a prospective study design in a larger cohort will be necessary to
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investigated whether delaying or avoiding the introduction of fruit juice in infancy could
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be a promising strategy to improve dietary habits, with possible lower consumption of
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high caloric foods, and therefore, prevent obesity among this high-risk population of
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children.
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Conflicts of interest: none.
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Acknowledgements: All co-authors revised the final version of the paper. We would like
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to sincerely thank all participants for their dedicated time.
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Funding: This work was supported by the Canadian Diabetes Association [Grant
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number: OG-3-14-4543-JR, 2014-2017] and the Danone Institute of Canada. Funding
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sources had no involvement in the study.
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References
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1. Nehring I, Chmitorz A, Reulen H, von Kries R, Ensenauer R. Gestational diabetes predicts the risk of childhood overweight and abdominal circumference independent of maternal obesity. Diabet Med. 2013;30(12):1449-56. 2. Burguet A. Long-term outcome in children of mothers with gestational diabetes. Diabetes Metab. 2010;36(6 Pt 2):682-94. 3. Dugas C, Perron J, Kearney M, Mercier R, Tchernof A, Marc I, et al. Postnatal Prevention of Childhood Obesity in Offspring Prenatally Exposed to Gestational Diabetes mellitus: Where Are We Now? Obes Facts. 2017;10(4):396-406.
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S0195-6663(17)31432-0
DOI:
10.1016/j.appet.2018.08.033
Reference:
APPET 4014
To appear in:
Appetite
Received Date: 27 September 2017 Revised Date:
7 August 2018
Accepted Date: 28 August 2018
Please cite this article as: Dugas C., Perron J., Marc I., Weisnagel S.J. & Robitaille J., Association between early introduction of fruit juice during infancy and childhood consumption of sweet-tasting foods and beverages among children exposed and unexposed to gestational diabetes mellitus in utero, Appetite (2018), doi: 10.1016/j.appet.2018.08.033. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
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Association between early introduction of fruit juice during infancy and childhood consumption of sweet-tasting foods and beverages among children exposed and unexposed to gestational diabetes mellitus in utero
Camille Dugas, M.Sc.a,b,c, Julie Perron, M.Sc.b, Isabelle Marc, MD, PhDc, S. John Weisnagel, MD c,d, Julie Robitaille, PhDa,b,c
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School of Nutrition, Laval University. 2425 rue de l‘Agriculture, Quebec City, Canada, G1V 0A6.b Institute of Nutrition and Functional Foods (INAF), Laval University. 2440 Boulevard Hochelaga, Quebec City, Canada, G1V 0A6.c Endocrinology and Nephrology Axis, CHU de Québec Research Center. 2705 boulevard Laurier, Quebec City, Canada, G1V 4G2.d Diabetes Research Unit, Laval University Medical Research Center. 2705 boulevard Laurier, Quebec City, Canada, G1V 4G2.
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Address for correspondence and reprint request:
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Julie Robitaille, RD, PhD, Professor, School of Nutrition. Institute of Nutrition and Functional Foods (INAF), Laval University. Pavillon des services, Room 2729N, Quebec City, Qc, G1V0A6, Canada. Email: [email protected] T: 418.656.2131 ext: 4458
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Abstract
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Background Children exposed to gestational diabetes mellitus (GDM) in utero are at
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high-risk of obesity. Given that nutritional habits can track from infancy to childhood, the
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aim of this study was to evaluate the association between the timing of fruit juice
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introduction in infancy and later consumption of sweet-tasting foods and beverages
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among children exposed (GDM+) and unexposed (GDM-) to GDM. Methods A total of
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107 GDM+ and 59 GDM- participated in the project. Data on the timing of fruit juice
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introduction during infancy were retrospectively collected for 62 GDM+ and 32 GDM-
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children. Current dietary intakes were collected with two 24-hour dietary recall
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questionnaires. Children were divided into groups according to the median timing of
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juice introduction (9 months). Results Mean age of children was 6.3±2.6 and 7.6±3.7
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years for GDM+ and GDM- children, respectively (p=0.08). Mean age of fruit juice
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introduction was similar between groups (p>0.05). Consuming >1 serving of fruit juice
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per day was 2.72 times more prevalent among GDM+ children introduced to fruit juice
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<9 months, compared to GDM+ children introduced ≥9 months (CI: 1.19-6.20). This
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association was not observed in the GDM- group. The timing of fruit juice introduction
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was not associated with later consumption of sweets, desserts and sweet-tasting
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beverages when adjustment for children’s age was made among GDM+ and GDM-
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children. Conclusion Early introduction of fruit juice in infant diet is associated with
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higher prevalence of consumption of >1 serving of fruit juice per day in GDM+ children.
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Key words: early life nutrition, juice consumption, sweet, dietary habits
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Introduction
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Children born to mothers with gestational diabetes mellitus (GDM) are at high risk of
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developing obesity and type 2 diabetes later in life (1, 2). There is a lack of effective
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postnatal strategies to prevent these complications among these high-risk children (3)
53
although it is well established that healthy lifestyle behaviours are associated with a
54
reduced risk of obesity among children in the general population (4). On the other hand,
55
despite efforts made to promote a healthy diet among children, consumption of high
56
amounts of ultra-processed foods and beverages rich in free sugar, like fruit juice, sugar-
57
sweetened beverages (SSB), pastries and candies is highly prevalent among Canadian
58
children (5).
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Preference for sweetness is innate among newborns and this preference generally remains
60
during childhood (6). However, pre- and postnatal experiences, like exposure to different
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flavors during in utero and early postnatal periods, can modulate taste preferences (7).
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The introduction of complementary foods in the infant diet represents also a critical
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period for flavor experiences in early life, particularly among non-breastfed children that
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have been exposed since birth to only the flavour of formula (8). Moreover, increasing
65
evidence suggests that food preferences in children would depend on foods offered and
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the context of feeding during early life (8). In fact, both healthy and unhealthy dietary
67
patterns established during infancy can track into childhood (9). Accordingly, some
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authors evaluated the association between SSB and fruit juice consumption in infancy
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and their later consumption in childhood and found that consumption of these types of
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beverages in early life was positively associated with their consumption during childhood
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3 Abbreviations GDM: gestational diabetes mellitus SSB: sugar sweetened beverage STB: sugar-tasting beverage
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(10, 11). However, to our knowledge, no such study has been conducted among children
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exposed to GDM in utero. Given their in utero exposure to an environment rich in
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glucose, it is possible that taste development in these children could differ from children
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unexposed to GDM, particularly developmental preferences for sweet tasting foods,
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which could impact food habits. In fact, previous research has shown that fetal
76
environment could be involved in food preferences programming (12).
77
While it is well recognized that SSB have a negative impact on children’s health (13),
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fruit juice is generally considered a healthier food option by parents. In fact, 100% fruit
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juice is considered as a serving of fruits in the 2007 Canada’s Food Guide, which could
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encourage parents to introduce fruit juice early in their infant’s diet (14), without
81
consideration for the sweet taste of this type of beverage. Thus, given that food habits
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could track from infancy to childhood (15, 16), and in order to identify new targets for
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prevention of obesity development among children exposed (GDM+) to GDM in utero,
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the primary objective of this study was to evaluate the association between early
85
introduction of fruit juice during infancy and childhood consumption of sweet-tasting
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foods and beverages among GDM+ children. Secondly, we evaluated the association
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between early introduction of fruit juice and childhood consumption of sweet-tasting
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foods and beverages among a group of children unexposed (GDM-) to GDM in utero, in
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order to compare results between groups.
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Material and methods
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Population
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All subjects were participants in a cohort study that aims to evaluate the impact of GDM
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on mother’s and children’s health and to examine whether a healthy postnatal
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environment could attenuate the adverse consequences of in utero exposure to GDM.
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This study takes place at the Institute of Nutrition and Functional Foods (INAF), at Laval
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University (Quebec City, Canada), and recruits women with and without a history of
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GDM and their children. Participants were recruited from a previous project conducted
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by our research team that has been previously described (17). Additionally, recruitment is
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conducted through access to medical records from the two major hospitals with a
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neonatal care unit in the metropolitan area of Quebec City (Hôpital Saint-François
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d’Assise and Centre Hospitalier de l’Université Laval-CHUL). Recruitment is also
102
conducted by emails sent to Laval University community as well as posts on healthcare
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websites and on social media (Facebook). Children with a history of in utero exposure to
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GDM between 2003 and 2013 are included in the study and children exposed to type 1 or
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type 2 diabetes are excluded. Children from the control group had to be born to a mother
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that never have had diabetes (Type1, 2 or GDM) before or after the index pregnancy. To
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date, a total of 107 children exposed (GDM+) and 59 children unexposed (GDM-) to
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GDM in utero have participated in the project. Written consents were obtained from all
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participating mothers and children and ethical approval was obtained from the Laval
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University Ethics Committee (2011-196-A-4 R-3) and from the Centre Hospitalier
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Universitaire de Québec Ethics Committee (2015-2031). This study is registered in the
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Clinical Trials.gov registry (NCT01340924).
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Exposure
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Children came with their mother to the INAF research center for a single 1-hour visit.
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During this visit, data about the timing of fruit juice introduction were retrospectively
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collected by a self-administrated questionnaire completed by the mother of each child.
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Mothers were asked when their child drank fruit juice, defined as 100% pure juice, for
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the first time (infant age given in months and/or weeks). A randomly selected subsample
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of participants (n=20) completed this questionnaire for a second time at home, within a 2
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weeks interval between each completion, in order to evaluate the reliability of answers
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given for this questionnaire. Results of the reliability test showed a strong correlation
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between answers given for the completion of both infant feeding questionnaires (r=0.81,
123
p < 0.001).
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Outcomes
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In order to estimate current dietary intakes of children, a 24-hour dietary recall (24HDR)
126
was conducted with a trained dietitian using the 5 steps of the Automated Multiple-Pass
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Method (AMPM): 1) quick list of the food items consumed 2) reminder of the food items
128
frequently forgotten 3) time and type of meals 4) details about serving size consumed,
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brand name of commercial products, ingredients and methods of homemade foods 5)
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review of the dietary recall (18). All food and drink items consumed in the previous day,
131
from midnight to midnight, were recorded. Three-dimensional food models were used to
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enhance accuracy of portion size estimates. Mothers of children younger than 10 years
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were asked to complete the 24HDR whereas children were present during the interview
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and were asked to add information if needed (i.e. for food consumed outside home). For
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children ≥10 years, the 24HDR was completed directly by the child, with the help of the
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mother if needed (i.e. for food preparation details). A second 24HDR was completed over
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the phone with the mother following the same validated method, the AMPM (18), 7-10
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days after their visit. Mean intakes for the two questionnaires were used in analyses.
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Dietary intake data were analyzed using Nutrition Data System for Research (NDSR)
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(19, 20). From this software, reports can be extracted by nutrients or by food group
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categories for each participant. In order to extract data regarding sweet-tasting foods and
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beverages, the Nutrition Coordinating Center (NCC) Food Group Count System from
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NDSR was used (19, 20). The NCC Food Group Count System is composed of 9 groups
144
and 168 subgroups of foods, based on recommendations made by the Dietary Guidelines
145
for Americans and the USDA Food Guide Pyramid. For the purpose of this study, groups
146
and subgroups of foods containing high amount of sugar (21) or known for their sweet
147
taste were extracted and compiled together to form 4 foods and beverages groups. These
148
groups were used in analyses, with a description of a portion size provided bellow:
152 153 154 155 156
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(125 ml).
2- Sweet-tasting beverages (STB), which include sweetened and artificially
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1- Fruit juice, defined as 100% pure juice, which include citrus and non-citrus juice
sweetened soft drinks, fruit drinks, tea and water (125 ml). 3- Desserts, which include cakes (55g to 125g), cookies (30g), pies, cobblers and
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137
pastries (125g), danish and doughnuts (55g).
4- Sweets, which include sugar (4g), syrup (30-60 ml), honey, jam and molasses (15 ml), fudge, caramel and chocolate syrup (30 ml), candy, chocolate candy and gum
157
drops (40g), frosting or glaze (35g) and sweetened flavored milk beverage powder
158
(1 cup prepared).
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Children were categorised as non-consumers (0 serving/d), consumers (>0 serving /day)
160
or high consumers (>1 serving/day) of the 4 different sweet-tasting food and beverage
161
groups described above.
162
Statistical analyses
163
Descriptive statistics were calculated as mean ± standard deviation (SD) or as percentage
164
(%). Participant’s characteristics and dietary intakes during childhood of GDM+ and
165
GDM- children were compared using Student t-test, Chi-squared test (χ2) or Fisher’s
166
exact test (when cell number was <5). GDM+ and GDM- children were divided into
167
groups according to the median timing of fruit juice introduction during infancy, which
168
was 9 months. Fisher’s exact test and χ2 test were performed to evaluate the distribution
169
of children across different groups of consumers and high consumers of sweet tasting
170
food and beverages among GDM+ and GDM- children. Finally, prevalence ratios (PR)
171
using log binominal model were calculated to evaluate the prevalence of consumers and
172
high consumers of food items from the different food groups in children introduced to
173
fruit juice before 9 months compared to those introduced at 9 months or later among
174
GDM+ and GDM- children. Given the low prevalence of children who consumed >1
175
serving of STB per day in both groups, the PR of high consumption of STB was not
176
computed. Finally, stepwise regression analyses were performed to determine which
177
cofactors should be included in the adjusted models among the following: breastfeeding
178
duration, timing of solid food introduction, children’s sex and age, maternal education
179
level and family incomes. Accordingly, analyses were only adjusted for children’s age.
180
The p value ≤0.05 and confidence interval (CI) of 95% were used to identify statistically
181
significant results. SAS software, version 9.4, was used for analyses.
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Results
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A total of 107 GDM+ and 59 GDM- children were recruited, but only 62 GDM+ and 32
184
GDM- children had complete information regarding the timing of fruit juice introduction.
185
Within the subsample with missing information, 9 mothers did not answer the specific
186
question regarding the timing of fruit juice introduction and 63 gave the answer “I don’t’
187
know” to this question. Thus, analyses included the 94 children with complete
188
information. Among GDM+ children without data on fruit juice introduction (n=45), a
189
lower proportion had been breastfed compared to children included in analyses (80%
190
compared to 95%, p=0.03). However, there was no difference regarding children’s age
191
and sex, maternal education level, family incomes and the timing of solid food
192
introduction (results not shown). There was also no statistically significant difference in
193
characteristics of GDM- children included and excluded from analyses. Characteristics of
194
the 94 participating children are presented in Table 1. Overall, 77 % and 78% of GDM+
195
and GDM- children received fruit juice during the first year of life, respectively.
196
Table 1. Participants’ characteristics
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Characteristics
Mean ± SD or n (%) GDM+
GDM-
P value
N=62
N=32
6.3±2.6
7.6±3.7
0.08
2-5 (years)
29 (47.8)
12 (37.5)
0.10
6-9 (years)
25 (40.3)
10 (31.3)
10-14 (years)
8 (12.9)
10 (31.3)
Boys
32 (51.6)
11 (34.4)
Demographic Age (years)
Sex 0.12 9
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Girls
30 (48.4)
21 (65.6)
0.04±0.98
-0.01±0.70
0.76
4 (7.7)
3 (11.5)
0.48
40 000 – 79 000
20 (38.5)
9 (34.6)
80 000- 99 999
13 (25.0)
3 (11.5)
>100 000
15 (28.9)
11 (42.3)
High school
12 (21.8)
4 (15.4)
College
7 (12.7)
2 (7.7)
University
36 (65.5)
BMI z-score (kg/m2)
0 – 39 000
0.65
20 (76.9)
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Maternal age
SC
Maternal education level
RI PT
Family income (CAD$/year)
38.0±4.2
37.1±4.5
0.33
27.7±7.7
26.2±5.0
0.24
2±0.7
2±0.6
0.62
58 (95)
27 (93)
0.66
8.9±7.8
10.1±4.6
0.39
Age of solid food introduction (months)c
4.9±1.0
4.9±1.3
0.81
Age of fruit juice introduction (months)
8.7±3.0
7.6±3.7
0.13
Maternal BMI Parity Infant feeding practices Breastfed infantsa
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Breastfeeding duration (months)b
Results are presented as mean ± SD or n (%) and were compared using Student t-test, chi-square test or Fisher’s exact test. BMI: body mass index. an=61 for GDM+ and n=29 for GDM-, bn=57 for GDM+ and n=27 for GDM-, cn=59 for GDM+ and n=29 for GDM-.
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During childhood, the average consumption of fruit juice was 0.92 serving of 125 ml per
201
day for GDM+ and 1.13 servings for GDM- children, including children that did not
202
consume any amount of fruit juice (Table 2). Among the consumers only, mean intake
203
was 1.96 and 1.65 servings of 125 ml per day for GDM+ and GDM- children,
204
respectively (results not shown). Similarly, mean intake for STB was 0.69 and 0.79
205
serving per day for all GDM+ and GDM- children, respectively (Table 2). However, the
206
average consumption of STB among consumers only was 1.02 and 0.94 serving of 125
207
ml per day for GDM+ and GDM- children, respectively (results not shown). Frequency
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of consumption of any amount of fruit juice per day tended to be higher among GDM-
209
than GDM+ children (p=0.05, Table 2).
210
Table 2. Dietary intakes during childhood
GDM+
GDM-
Consumers (yes)
29 (46.8)
22 (68.8)*
High consumers (>125 ml)
18 (29.0)
11 (34.4)
0.92±1.57
1.13±1.36
Fruit juice
Mean intake (servings of 125 ml/d)
Consumers (yes)
M AN U
STB
21 (33.9)
14 (43.8)
9 (14.5)
3 (9.4)
Mean intake (servings of 125 ml/d)
0.69±1.41
0.79±1.38
Consumers (yes)
50 (80.6)
25 (78.1)
High consumers (>1 serving)
10 (16.1)
6 (18.8)
Mean intake (serving/d)
0.44±0.50
0.63±1.16
Consumers (yes)
38 (61.3)
19 (59.4)
High consumers (>1 serving)
15 (24.2)
7 (21.9)
Mean intake (serving/d)
0.69±1.02
0.49±0.57
1686±439
1790±585
High consumers (>125 ml)
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Energy intake (kcal)
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Sweets
Desserts
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Food groups
RI PT
Mean ± SD or n (%)
211 212 213 214 215
Fruit juice includes citrus and non-citrus 100% pure juice; sweet-tasting beverages (STB) include sweetened and artificially sweetened soft drinks, fruit drinks, tea and water; sweets include sugar, syrup, honey, jam, molasses, fudge, caramel, chocolate syrup, candy, chocolate candy, gum drops, frosting or glaze and sweetened flavored milk beverage powder; desserts include cakes, cookies, pies, pastries, danish, doughnuts and cobblers. *p=0.05.
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Among GDM+ children, consuming >125 ml of fruit juice per day was more frequent
217
among children introduced to fruit juice earlier, i.e. before 9 months, compared to those
218
introduced at 9 months or later (Table 3). Still among GDM+ children, the same pattern
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was seen for STB that were more frequently consumed, for any amount of STB as well as
220
for >125 ml/d, among GDM+ children exposed to fruit juice earlier. However, no
221
statistically significant difference was seen for the distribution of children who reported
222
consuming any amount of desserts, sweets or fruit juice (>0 serving/d) or for high
223
consumers of sweets and desserts (>1 serving/d), between GDM+ children exposed to
224
fruit juice before and ≥ 9 months (Table 3). Among GDM- children, any amount of
225
desserts tended to be more frequently consumed among children introduced to fruit juice
226
<9 months (73.7% of consumers) compared to those introduced to fruit juice ≥9 months
227
(26.3% of consumers, p=0.05, Table 3). No other difference was seen in the distribution
228
of consumption of any food and beverage groups among GDM- children (Table 3).
229
Table 3. Association between the timing of fruit juice introduction and consumption of
230
sweet-tasting foods and beverages during childhood among GDM+ and GDM- children
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Introduced to juice < 9
Introduced to juice ≥ 9
months
months
N (%)
N (%)
p
15 (51.7)
14 (48.3)
0.22
>125 ml
12 (66.7)
6 (33.3)
0.02
Yes
13 (61.9)
8 (38.1)
0.04
>125 ml
8 (88.9)
1 (11.1)
0.008
Yes
20 (52.6)
18 (47.4)
0.07
>1 serving
8 (53.3)
7 (46.7)
0.38
Yes
24 (48.0)
26 (52.0)
0.10
>1 serving
6 (60.0)
4 (40.0)
0.25
EP
Childhood consumption GDM+ children
STB
Desserts
Sweets
Yes
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STB
Desserts
Sweets
Yes
12 (54.5)
10 (45.5)
0.22
>125 ml
8 (72.7)
3 (27.3)
0.17
Yes
10 (71.4)
4 (28.6)
0.14
>125 ml
2 (66.7)
1 (33.3)
0.45
Yes
14 (73.7)
5 (26.3)
0.05
>1 serving
5 (71.4)
2 (28.6)
0.27
Yes
15 (60.0)
10 (40.0)
0.33
>1 serving
3 (50.0)
3 (50.0)
0.31
RI PT
Fruit juice
The group “yes” refers to children who reported having consumed any amount of items from the specific food group. Fruit juice includes citrus and non-citrus 100% pure juice; sweet-tasting beverages (STB) include sweetened and artificially sweetened soft drinks, fruit drinks, tea and water; sweets include sugar, syrup, honey, jam, molasses, fudge, caramel, chocolate syrup, candy, chocolate candy, gum drops, frosting or glaze and sweetened flavored milk beverage powder; desserts include cakes, cookies, pies, pastries, danish, doughnuts and cobblers. P value was calculated with χ2 analyses and with Fisher’s exact test when cell number was <5.
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As seen in Table 4, GDM+ children introduced to fruit juice before 9 months did not
239
have different PR for the consumption of any amount of fruit juice, sweets and desserts
240
compared to GDM+ children introduced to fruit juice ≥ 9 months. However, consuming
241
more than 125 ml of fruit juice per day was 2.72 times more prevalent among GDM+
242
children introduced to fruit juice before 9 months, compared to those introduced at 9
243
months or later (CI: 1.19-6.20). Although prevalence of consumption of any amount of
244
STB in the crude model was 2.11 higher for GDM+ children exposed to fruit juice earlier
245
(CI: 1.02-4.34, result not shown), this latter was no longer statistically significant after
246
adjustment for children’s age (PR: 1.43, CI: 0.85-2.42, Table 4). Among GDM- children,
247
the prevalence for the consumption of any amount or for >1 serving of any food and
248
beverage groups was similar according to the timing of fruit juice introduction (Table 4).
249
Table 4. Prevalence of consumption of sweet-tasting foods and beverages in GDM+ and
250
GDM- children introduced to fruit juice <9 months compared to those introduced at or
251
after 9 months of age
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Prevalence ratio
95% CI
Yes
1.56
(0.93; 2.60)
>125 ml
2.72
(1.19; 6.20)
STB
Yes
1.43
(0.85; 2.42)
Desserts
Yes
1.44
>1 serving
1.42
Yes
1.19
Sweets
>1 serving
-
GDM- children Yes
-
>125 ml STB
Yes
Desserts
Yes >1 serving Yes
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Sweets
>1 serving
(0.58; 3.49)
(0.94; 1.51) -
M AN U
Fruit juice
(0.97; 2.13)
SC
Fruit juice
RI PT
GDM+ children
-
1.67
(0.51; 5.45)
1.47
(0.55; 3.97)
1.63
(0.72; 3.71)
-
-
0.96
(0.64; 1.43)
0.35
(0.07; 1.61)
Table 4. Log-binominal regression analyses showing prevalence ratios with 95% CI for consumption of
253
fruit juice, sweet-tasting beverages (STB), sweets, desserts, >125 ml of fruit juice and >1 serving of sweets
254
and dessert in GDM+ and GDM- children introduced to fruit juice before 9 months compared to those
255
introduced at 9 months or later (reference group). Increase prevalence of children consuming these food
256
groups are above the 95% confidence limit of an agreement ratio of 1.00. Results presented are adjusted for
257
children’s age.
258
Given the small number in some cells, adjusted prevalence ratio could not be computed in some models.
259
Discussion
260
This study showed that early introduction of fruit juice during infancy, defined as before
261
9 months of age, is associated with a higher odds of consuming sweetened and artificially
262
sweetened beverages and high amounts of fruit juice during childhood among GDM+
263
children. The association between the timing of fruit juice introduction and odds of
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consuming >125 ml of fruit juice per day remained statistically significant after
265
adjustment for children’s age, but the association between fruit juice introduction and
266
later consumption of STB was no longer statistically significant after adjustment for
267
children’s age. Among GDM- children, no statistically significant association between
268
the timing of fruit juice introduction and consumption of sweet-tasting food and
269
beverages during childhood was observed.
270
Results of this study suggest that the prevalence of consumption of more than 1 serving
271
of fruit juice per day was higher among GDM+ children exposed to fruit juice before 9
272
months compared to those exposed to juice at or after 9 months. To our knowledge, this
273
is the first study that evaluated the association between early life nutrition and food and
274
beverage intakes during childhood among GDM+ children, which limits comparison of
275
these results with the current literature. However, few studies conducted in the general
276
population that investigated the association between SSB or juice intakes in infancy and
277
beverage consumption in childhood showed similar results that these found in the GDM+
278
group (10, 11). Analyses from the Infant Feeding Practices Study II (IFPS II), a national
279
longitudinal study conducted in the United-States, showed that consuming SSB during
280
the first year of life was associated with an increased risk of consuming SSB more than
281
one time per day at the age of 6 years (10). In addition, Sonneville et al. showed that
282
higher intakes of fruit juice at the age of 12 months was associated with a higher
283
consumption of fruit juice and SSB in both early and mid-childhood when compared to
284
infant that did not consume any amount of fruit juice at 12 months (11). More
285
specifically, children consuming ≥16 oz of juice per day at 1 year consumed twice as
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much juice per day during childhood compared to those that did not consume any amount
287
of juice at 1 year (2.4 vs 1.2 servings per day) (11).
288
Our study showed no statistically significant association between the timing of fruit juice
289
introduction during infancy and later consumption of foods containing high amount of
290
sugar among GDM+ children. To our knowledge, no study has evaluated the association
291
between juice introduction in infancy and later consumption of sweet foods in children
292
exposed or unexposed to GDM in utero. However, Rose et al. evaluated the association
293
between dietary patterns in early life and dietary patterns in childhood using data from
294
the IFPS II (9). This study showed that infants having a high density energy diet at 9
295
months, which included high amounts of juice, sweet foods and French fries, were greater
296
consumers of SSB, sweet desserts and fried potatoes at 6 years, compared to other dietary
297
patterns in infancy (9). Liquid and solid foods have different properties. Indeed, sugars
298
from liquid sources are associated with less satiety compared to sugar from solid foods,
299
mainly due to the different fiber content (22). However, we are unaware of any published
300
study evaluating the influence of the food matrix on taste development, thus it is unclear
301
whether sugar intake from juice could affect taste preference for sugar from solid foods
302
the same way that for sugar from liquids.
303
Furthermore, this study showed no statistically significant association between the timing
304
of fruit juice introduction and later consumption of sweet tasting food and beverages
305
among GDM- children. The lack of association in the control group, which is not in
306
agreement with studies conducted in the general population (9-11), could possibly be
307
explained by the small number of participants in the GDM- group, which limits the
308
statistical power to detect statistically significant results.
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The association between the timing of fruit juice introduction in infant diet and beverages
310
consumption in childhood among GDM+ children could be explained in part by the
311
development of taste preferences in early life. As mentioned earlier, it has been
312
demonstrated that taste preferences track from infancy to childhood and that the early life
313
period could be a critical moment to program children’s dietary habits (8). In fact,
314
nutritional experiences in early life have neurological programing effect that influence
315
eating behaviour later in life (23). A study conducted in mice that evaluate the
316
neuroanatomical development of the olfactory system showed that exposure through
317
mother’s milk to odours that activate GFP-tagged olfactory receptors was associated with
318
larger glomeruli in the olfactory bulb and with significant preferences for the activating
319
odour (24). These results suggest that exposure to specific flavours during early life result
320
in enhanced detection of these learned odours, which could facilitate their acceptance by
321
children. Among studies conducted in humans, Pepino et al. demonstrated that infants
322
who were routinely fed with sweet water in early life preferred high levels of sucrose in
323
childhood, compared to those who were not routinely fed with sweet water in infancy,
324
highlighting the impact of early exposure to sweet on modulation of taste preference for
325
sweetness (25). However, even if the early life period is recognized as critical for the
326
development of taste preferences, the exact timing to shift taste preferences is still
327
unknown (26). In order to answer this gap, a randomized clinical trial has been conducted
328
among formula-fed infants to test whether the timing of introduction of protein
329
hydrolysate formulas (PHF), known for their particularly unpleasant flavour, in infant
330
diet would influence its acceptance later in infancy (27). This study showed that infant
331
exposed to PHF earlier (i.e. at 1.5 and 2.5 months) consumed significantly more amount
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of PHF at 7.5 months compared to infants exposed later (i.e at 3.5 months) (27). Infants
333
exposed to PHF at 3.5 months consumed the same amount of PHF at 7.5 months as
334
infants from the control group who were fed with cow-milk base formulas (27). Thus,
335
authors suggested that the window of opportunity to modulate taste preferences could
336
start to close as early as 3.5 months.
337
Although we first hypothesized that early introduction of fruit juice in the infant diet
338
would lead to an increased consumption of sweet-tasting foods and beverages, we only
339
found associations with beverage intakes. As mentioned above, it is possible that the food
340
matrix of juice, a liquid with no fiber, would influence differently the consumption of
341
beverages and solid foods because of their different properties (22). Furthermore, in
342
addition to the taste preference theory, it has been suggested that fruit juice intake in
343
infancy could be a gateway to later consumption of caloric beverages by establishing the
344
habit of consuming these types of drinks (11). Similarly, the association between the
345
timing of fruit juice introduction and its later consumption could also be explained by
346
dietary habits established by parents during infancy that could remain during childhood.
347
In fact, it is possible to think that parents continue to feed their children the same types of
348
food from infancy to childhood, explaining associations seen for beverages but not for
349
foods.
350
Our study presents some limitations. First, given the cross-sectional study design, the
351
timing of fruit juice introduction was retrospectively collected. This did not allow us to
352
quantify the amount of juice intakes in infant diet neither the frequency of consumption
353
during this period, which can have an impact on taste development and dietary habits.
354
This study design is also at risk of recall bias, although our reliability test showed a
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strong correlation between answers given for the two completed questionnaires.
356
Furthermore, mothers had the possibility to answer “I don’t know” to the question
357
regarding the timing of juice introduction, which reduces risk of recall bias in our
358
analyses. In fact, it is possible to think that mothers that answered this question were
359
confident of their answer. However, this study should be repeated using a prospective
360
study design in order to limit this bias. Another limitation of the study is its small sample
361
size, in both the GDM+ and GDM- groups, which increases the likelihood of type 2 error.
362
Indeed, given the small sample size of participants in the control group (n=32), it is
363
possible that the lack of association observed in this group is due to low statistical power.
364
Furthermore, the homogeneity of participant’s characteristics (high income families with
365
high education level) restricts our results to this study population only. Finally, this study
366
did not evaluate specifically taste preferences of children, which limits interpretation of
367
these results. In fact, Divert et al. showed that consumption of sweet tasting foods and
368
beverages was not clearly associated with sweet liking, evaluated using a liking score, in
369
a cohort study of school-aged children (28). Despite these limitations, this study presents
370
several strengths. This is, to our knowledge, the first study that evaluated the impact of
371
early life nutrition on dietary habits during childhood among children exposed to GDM in
372
utero, a population at high-risk of many health problems such as obesity (1). Another
373
strength is the use of two 24HDR to evaluate current dietary intakes of children. This
374
allowed us to have quantitative data regarding food group intakes, while others studies
375
generally use semi-quantitative questionnaires (10, 11). The use of two recalls, as it has
376
been done by others in large population studies (29-31), helps to reduce the day-to-day
377
variability of dietary intakes measured with 24HDR while minimizing the burden on
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participants (32). Finally, the fact that dietary questionnaires were conducted by a trained
379
dietitian minimized risk of food misclassification, especially for fruit juice and fruit
380
drinks.
381
Conclusion
382
This study suggests that early introduction of fruit juice in the infant diet is associated
383
with higher prevalence of consumption of high amounts of fruit juice in GDM+ children.
384
Further studies using a prospective study design in a larger cohort will be necessary to
385
investigated whether delaying or avoiding the introduction of fruit juice in infancy could
386
be a promising strategy to improve dietary habits, with possible lower consumption of
387
high caloric foods, and therefore, prevent obesity among this high-risk population of
388
children.
389
Conflicts of interest: none.
390
Acknowledgements: All co-authors revised the final version of the paper. We would like
391
to sincerely thank all participants for their dedicated time.
392
Funding: This work was supported by the Canadian Diabetes Association [Grant
393
number: OG-3-14-4543-JR, 2014-2017] and the Danone Institute of Canada. Funding
394
sources had no involvement in the study.
395
References
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1. Nehring I, Chmitorz A, Reulen H, von Kries R, Ensenauer R. Gestational diabetes predicts the risk of childhood overweight and abdominal circumference independent of maternal obesity. Diabet Med. 2013;30(12):1449-56. 2. Burguet A. Long-term outcome in children of mothers with gestational diabetes. Diabetes Metab. 2010;36(6 Pt 2):682-94. 3. Dugas C, Perron J, Kearney M, Mercier R, Tchernof A, Marc I, et al. Postnatal Prevention of Childhood Obesity in Offspring Prenatally Exposed to Gestational Diabetes mellitus: Where Are We Now? Obes Facts. 2017;10(4):396-406.
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