draft...draft page 1 (i) ranking of iron, vitamin d and calcium intakes in relation to maternal...

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Ranking of iron, vitamin D and calcium intakes in relation to

maternal characteristics of pregnant Canadian women

Journal: Applied Physiology, Nutrition, and Metabolism

Manuscript ID apnm-2015-0588.R1

Manuscript Type: Article

Date Submitted by the Author: 19-Feb-2016

Complete List of Authors: Morisset, Anne-Sophie; Centre de recherche du Centre hospitalier universitaire de Sherbrooke; Sainte Justine University Hospital Research Center Weiler, Hope; McGill University, Dubois, Lise; University of Ottawa, School of epidemiology Ashley-Martin, Jillian ; Dalhousie University, Perinatal Epidemiology

Research Unit Shapiro, Gabriel; Sainte Justine University Hospital Research Center Dodds, Linda; Dalhousie University, Perinatal Epidemiology Research Unit Massarelli, Isabelle; Health Canada, Food Directorate Vigneault, Michel ; Health Canada, Food Directorate Arbuckle, Tye; Health Canada, Environmental Health Science and Research Bureau Fraser, William; Centre de recherche du Centre hospitalier universitaire de Sherbrooke; Sainte Justine University Hospital Research Center

Keyword: pregnancy, nutrition, iron, vitamin D, calcium

https://mc06.manuscriptcentral.com/apnm-pubs

Applied Physiology, Nutrition, and Metabolism

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(i) Ranking of iron, vitamin D and calcium intakes in relation to

maternal characteristics of pregnant Canadian women

(ii) Anne-Sophie Morisset, Hope A. Weiler, Lise Dubois, Jillian Ashley-Martin, Gabriel D.

Shapiro, Linda Dodds, Isabelle Massarelli, Michel Vigneault, Tye E. Arbuckle, William D. Fraser

(iii) Address for correspondence: William D. Fraser, MD

Centre de recherche du CHUS (CRCHUS)

3001, 12e Avenue Nord, Sherbrooke, Qc, J1H 5N4

Tel : 1-819-346-1110 poste 12875, Fax : 1-819-564-5445

[email protected]

(iv) Anne-Sophie Morisset* et William D. Fraser : Centre de recherche du Centre hospitalier

universitaire de Sherbrooke, Sherbrooke, Canada et Sainte Justine University Hospital Research

Center, University of Montreal, Montreal, Canada. [email protected] et

[email protected] Hope A. Weiler : School of Dietetics and Human Nutrition,

McGill University, Montreal, Canada, [email protected] Lise Dubois: School of

Epidemiology, Public Health and Preventive Medicine, University of Ottawa, Ottawa, Canada,

[email protected] Jillian Ashley-Marin and Linda Dodds: Perinatal Epidemiology

Research Unit, Dalhousie University, Halifax, Nova Scotia, Canada, Jillian.Ashley-

[email protected] and [email protected] Gabriel D. Shapiro : Sainte Justine University Hospital

Research Center, University of Montreal, Montreal, Canada, [email protected]

Isabelle Massarelli and Michel Vigneault : Food Directorate, Health Canada, Ottawa, Canada,

[email protected] and [email protected] Tye E. Arbuckle:

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Environmental Health Science and Research Bureau, Health Canada, Ottawa, Canada,

[email protected]

* The first author is now assistant professor at Laval University, School of Nutrition. The study

was conducted when she was the recipient of a postdoctoral fellowship from the FRSQ under the

supervision of William D. Fraser and the co-supervision of Hope A. Weiler and Lise Dubois.

William D. Fraser is supported by a CIHR Canada Research Chair

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ABSTRACT

Introduction: Iron, vitamin D and calcium intakes in the prenatal period are important

determinants of maternal and foetal health. Objective: To examine iron, vitamin D and calcium

intake from diet and supplements in relation to maternal characteristics. Methods: Data were

collected in a subsample of 1186 pregnant women from the Maternal-Infant Research on

Environmental Chemicals (MIREC) Study, a cohort study including pregnant women recruited

from 10 Canadian sites between 2008 and 2011. A FFQ was administered to obtain a ranking of

iron, calcium and vitamin D intake (16-21 weeks of pregnancy). Intakes from supplements were

obtained from a separate questionnaire (6-13 weeks of pregnancy). Women were divided into 2

groups according to the median total intake of each nutrient. Results: Supplement intake was an

important contributor to total iron intake (median 74%: IQR 0-81%) and total vitamin D intake

(median 60%: IQR 0-73%), while the opposite was observed for calcium (median 18%: IQR 0-

27%). Being born outside of Canada was significantly associated with lower total intakes of iron,

vitamin D and calcium (p≤0.01 for all). Consistent positive indicators of supplement use (iron,

vitamin D and calcium) were maternal age over 30 years and holding a university degree.

Conclusions: Among Canadian women, the probability of having lower iron, vitamin D and

calcium intake is higher among those born outside Canada. Supplement intake is a major

contributor to iron and vitamin D total intakes. Higher education level and age over 30 years were

associated with supplement intake.

Key words: Pregnancy, nutrition, iron, vitamin D, calcium, food frequency questionnaire,

supplements

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RÉSUMÉ

Introduction : Les apports nutritionnels en fer, calcium et vitamine D durant la grossesse sont

importants pour la santé de la mère et de l’enfant. Objectif : Examiner les apports nutritionnels

en fer, vitamine D et calcium provenant de l’alimentation et des suppléments en association avec

les caractéristiques maternelles. Méthodes : Un sous-échantillon de l’étude MIREC incluant 1186

femmes enceintes canadiennes recrutées sur 10 sites canadiens entre 2008 et 2011 a été examiné.

Les apports nutritionnels provenant des aliments ont été estimés au deuxième trimestre avec un

questionnaire de fréquence alimentaire (FFQ). Les apports nutritionnels provenant des

suppléments ont été évalués par questionnaire à la fin du premier trimestre. Les femmes ont été

divisées selon la médiane des apports totaux pour chacun des nutriments examinés. Résultats :

Le supplément était un important contributeur de l’apport total en fer (médiane 74%: IIQ 0-81%)

et en vitamine D (médiane 60%: IIQ 0-73%), contrairement au calcium (médiane 18%: IIQ 0-

27%). Le fait d’être né à l’extérieur du Canada était associé significativement avec des apports

plus faibles en fer, vitamine D et calcium (p≤0.01 pour tous). Le fait d’être âgé de plus de 30 ans

et d’avoir complété des études universitaires ont été identifiés comme des déterminants d’une

plus grande utilisation de suppléments (fer, vitamine D et calcium). Conclusions : Les femmes

enceintes canadiennes qui sont nées à l’extérieur du pays sont plus à risque d’avoir des apports

totaux plus faibles en fer, vitamine D et calcium.

Mots clés: Grossesse, nutrition, fer, vitamine D, calcium, questionnaire de fréquence alimentaire,

suppléments

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INTRODUCTION

Micronutrient status in pregnancy may affect maternal health, fetal wellbeing and birth outcomes,

as well as the risk of chronic disease in the offspring (Barker et al. 1993; Blumfield et al. 2013).

Consequently, insufficient micronutrient intake may have negative impacts on maternal and fetal

health.

Three micronutrients of particular importance for a healthy pregnancy are iron, vitamin D and

calcium. Achieving Recommended Dietary Allowances (RDA) for these micronutrients in

pregnancy can be challenging, especially for iron and vitamin D (Blumfield et al. 2013).

Pregnancy is associated with an increased demand for iron to support the expansion of maternal

blood volume and for fetal growth (Simpson et al. 2011). For this reason, dietary requirements are

significantly increased during pregnancy compared to a non-pregnant state (18 mg to 27 mg/day)

(Otten et al. 2006). Insufficient iron intakes have been associated with an increased risk of

anemia, which in turn is associated with low birth weight and preterm birth (Scholl et al. 2000).

Similarly, vitamin D has received particular attention in the last decade, as it is also important for

maternal and fetal health, mostly for skeletal growth and development of the fetus (Simpson et al.

2011). Low vitamin D status, defined as serum 25(OH)D concentrations below 50 nmol/l, has

also been associated with an increased risk of gestational diabetes mellitus (GDM), pre-eclampsia

and low birth weight (Wei et al. 2013). Calcium intake during pregnancy is important for

promoting bone health and possibly in reducing the risk of pre-eclampsia (Hofmeyr et al. 2010).

As calcium absorption is augmented during pregnancy to support the increased demand

(Olausson et al. 2012), there is less need to increase dietary intakes and it is easier to achieve the

RDA (Blumfield et al. 2013). Dietary recommendations for vitamin D and calcium are similar to

those for non-pregnant women (600 IU/day and 1000 mg/day, respectively) (Otten et al. 2006).

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Regarding supplement use, recommendations from the Institute of Medicine (IOM) suggest that

all pregnant women at risk of nutritional deficiency should take a multivitamin/mineral

supplement (Institute of Medicine 1992). Health Canada recommends 16-20 mg/day of iron from

supplemental sources (Cockell et al. 2009). No specific recommendations concerning vitamin D

and calcium intakes from supplements in pregnant women are suggested, as these dietary

requirements should be met by food.

To date, data focusing on nutrient intakes in large, national-scale samples of pregnant women are

scarce. Furthermore, iron, calcium and vitamin D total intakes in Canadian women during

pregnancy, including food and supplements intakes, have not been thoroughly investigated in

relation to maternal characteristics. Therefore, our main objective was to examine total dietary

intakes of iron, vitamin D and calcium during pregnancy in a population of Canadian women in

relation to maternal age, pre-pregnancy body mass index (BMI), education level, household

income and country of birth. An underlying objective was to validate the use of a food frequency

questionnaire (FFQ) in a subsample of our study population.

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MATERIAL AND METHODS

Subjects

Details of the MIREC Study have been previously reported (Arbuckle et al. 2013). Briefly, 2001

women were recruited from 10 Canadian sites from 2008-2011 during their first trimester of

pregnancy. Women were eligible for inclusion if they were < 14 weeks gestation at time of

recruitment, ≥ 18 years of age, able to communicate in French or English, and planning to deliver

in a participating hospital. Women with known foetal or chromosomal anomalies in the current

pregnancy and women with serious medical complications were excluded from the study

(Arbuckle et al. 2013). The population in the present analysis included 1186 mothers who had

singleton live births and completed dietary surveys (FFQ and nutrient supplement questionnaire).

Total iron, vitamin D and calcium dietary intakes

Food frequency questionnaire

At the second trimester visit, between 16 and 21 weeks of pregnancy, a one-month semi-

quantitative FFQ was administered to obtain a ranking of iron, calcium and vitamin D intake. The

FFQ consisted of 46 food items listed in 6 subgroups (vegetables/ fruits/ meat, poultry, fish and

alternatives/ milk products/ grain products/ other foods). For each food item, a frequency

(days/weeks/months), a serving size (less than average (small)/ average / more than average

(large)) and an example of an average serving size (ex: 250 ml or 1 cup) were presented. For each

of the 46 questions in the FFQ, responses were converted to servings per day, with a 33%

reduction factor for small servings and a 33% inflation factor for large servings. In order to assign

a gram weight and amounts of nutrients to each item on the FFQ, foods were matched to

corresponding foods in the 2010 Canadian Nutrient File. The serving size, gram weight and the

amount of nutrient were calculated for each serving of the food item. In the case of questions

consisting of food composites, the relative popularity of each food was estimated from the

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Canadian Community Health Survey Cycle 2.2 Nutrition (CCHS 2.2), a nationally representative

Canadian survey on nutrition including pregnant and non-pregnant women) and the weighted

average amount of nutrients per serving was calculated (Health Canada 2004). Based on the

inherent assumptions of this FFQ, data was grouped according to above and below the median

intakes.

To evaluate the validity of the FFQ, a second FFQ was collected approximately two weeks after

the first in a subsample of 115 MIREC subjects. On both occasions a 24-hour dietary recall was

also administered in order to evaluate the validity and repeatability of the FFQ in pregnant

women. The first FFQ and 24-hour recall were administered by trained research nurses at the

second trimester visit. Repeat interviews were done over the phone. The 24-hour recalls were

processed using the Nutrition Survey System (NSS) developed by the Food Directorate at Health

Canada.

Nutrient supplement questionnaire

The nutrient supplement questionnaire was completed by participants around 16 weeks of

pregnancy and consisted of a detailed list of supplements taken in the last 30 days (name and

description of product/ drug identification number on bottle (Drug Identification Number (DIN) /

Natural Product Number (NPN) / Homeopathic Medicine Number (DIN-HM)) /amount taken

each time (# of pills, tabs, caps, teaspoon, etc.)/ frequency). Daily iron, calcium and vitamin D

content were derived using Health Canada’s Drug Product database and/or the detailed

ingredients list from the product monograph. Daily iron intake from supplements was compared

to Health Canada recommendation (16 to 20 mg per day (Cockell et al. 2009)), and the proportion

of women not taking any supplement was also calculated. In the absence of specific

recommendations for supplemental intakes of vitamin D and calcium, only the proportion of

women taking a daily supplement was calculated.

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Maternal and infant characteristics

Data collected on maternal age, parity, education level, family income and country of birth were

obtained from the baseline questionnaire administered at the first visit (between 6 and 13 weeks

of pregnancy). Body weight was measured during study clinic visits throughout pregnancy and/or

at delivery. Total gestational weight gain was calculated as the difference between maternal

weight measured at delivery or at the last prenatal visit (≥37th week), and self-reported pre-

pregnancy weight. Total gestational weight gain was compared to the 2009 IOM

recommendations (Institute of Medicine 2009). Impaired glucose tolerance (IGT) and GDM were

assessed by chart review based on the results of a 50 g glucose challenge test (GCT) and 75 or

100 g oral glucose tolerance test (OGTT), in accordance with guidelines from the Canadian

Diabetes Association and the Society of Obstetricians and Gynaecologists of Canada (Berger et

al. 2002; CDA 2008). Subjects were assigned a diagnosis of IGT if one of the OGTT cut-off

values was met or exceeded. If the result of the 1-hour 50-g GCT was ≥10.3 mmol/L, or if at least

2 of the cut-off values were met or exceeded on a 75-g or 100-g OGTT, a diagnosis of GDM was

assigned. Infant birth weight was assessed from the hospital birth chart. Foetal growth was

assessed using the sex-specific Canadian reference charts for birth weight for gestational age

(Kramer et al. 2001). Infants were categorized as small-for-gestational-age (SGA) (where the

birth weight was <10th percentile for gestational age); normal-for-gestational-age (GA); or large-

for-gestational-age (LGA) (where the birth weight was >90th percentile for gestational age)

(Kramer et al. 2001).

Statistical analysis

Validation of the FFQ questionnaire

Validity of the FFQ was assessed in a subset of the cohort as described above. The FFQ was

administered to obtain a ranking of iron, calcium and vitamin D intakes. Correlations between

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recall and FFQ measurements (recall-FFQ pairs) were computed, first comparing the absolute

amount of food in grams and absolute intakes of nutrients, then comparing the ranks of the

amounts of food and the ranks of intakes of nutrients. For the gram amount and for each of the

three nutrients studied, 4 correlation analyses were performed: the first recall intake against the

first FFQ intake; the second recall intake against the second FFQ intake; the recall average intake

(as a surrogate for usual intake) against the first FFQ intake; and; the recall average intake against

the second FFQ intake. For each paired recall-FFQ measurement, Pearson product-moment

correlation coefficients were estimated, which measures the degree of linear association between

the FFQ and recall intakes. Spearman rank-order correlations were also computed to measure the

degree to which the nutrient intakes from the 24-hour recall and from the FFQ were associated,

but not necessarily linearly associated. A rank-order correlation of 100% means perfect positive

correlation (i.e. when the FFQ intake ranks matched perfectly against those from the recalls). A

correlation of 0% means the rank-orders were statistically independent. For each correlation

estimate, a P-value was estimated to test the hypothesis of a non-zero correlation. These analyses

were performed using SAS statistical software (version 9.2).

Descriptive and multivariate logistic regression analyses

Descriptive analyses for main characteristics of the subjects were performed. It was impossible to

use continuous variables for nutrient intakes or a subdivision based on whether the RDA was

achieved because the FFQ did not capture all nutrient sources and consequently total dietary

nutrient intakes. Instead, women were divided into two groups of total nutrient intake (lower vs.

higher) according to the median value of iron, vitamin D and calcium intake. Only 2 categories

were used since the total diet varied mostly as a function of supplemental intakes; by categorizing

women into two groups it best captured those taking lower supplemental amounts of iron,

calcium or vitamin D compared to those taking higher supplemental amounts. For each nutrient,

Student’s t tests were computed to ensure that both nutrient and supplement intakes were

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significantly lower in women with lower vs. higher total intakes. Typically supplemental intakes

were low or high and thus tertiles were not necessary (e.g. 10 vs. 40 mg iron/supplement).

Proportions of main food components contributing to each nutrient, women taking an iron

supplement at least 16 mg/day (Health Canada guideline), and women not taking iron, vitamin D

or calcium supplements were all determined. A Chi-square comparison was used to test

differences in maternal characteristics between women with lower vs. higher total intake (for

vitamin D, calcium and iron intake). Multivariate logistic regression analyses were performed to

evaluate the odds of having lower nutrient intake in models including all clinically relevant

maternal characteristics (maternal age, pre-pregnancy BMI, family income, education level and

country of birth). Similar analyses were performed to determine indicators of iron, vitamin D and

calcium supplement intakes. Interaction terms were not included in the models since this was not

the purpose of these analyses. These analyses were performed using JMP statistical software

version 10.0 (SAS Institute, Cary, NC, USA).

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RESULTS

The main characteristics of the cohort are shown in Table 1. More than half of the women were

over 30 years of age (73.0%). Most of them were in their first (44.9%) or second pregnancy

(41.3%) at the time of the study. The majority of women had a university degree (63.5%) and

were born in Canada (79.6%). One third of women entered pregnancy overweight (21.4%) or

obese (14.0%) based on pre-pregnancy BMI, and 55.9% gained in excess of the current IOM

gestational weight gain recommendations. Mean gestational age at delivery was 39.3±1.7 weeks

and 82 mothers (3.2%) delivered prematurely. 4.6% of women gave birth to an SGA infant and

12.5% to an LGA infant. The prevalence of GDM was 4.2%, while IGT was observed in 4.4% of

participants. Similar characteristics were found in the subsample of women included in the FFQ

validation (data not shown).

FFQ validation results

Table 2 shows comparisons between recall-FFQ pairs of responses in 115 subjects. The FFQ

consistently underestimated total intakes of nutrients: by more than 50% for iron, by about 10%

for vitamin D, and by about 30% for calcium. However, for all paired recall-FFQ intake totals,

Pearson product-moment correlations were strictly positive: they ranged from 31% to 42% for

iron, from 16% to 45% for vitamin D and, from 31% to 47% for calcium. All P-values for these

correlations were below 0.01, with the exception of vitamin D (first recall vs. first FFQ). Finally,

Spearman rank-order correlation estimates were consistently between 30% and 50%: they ranged

from 42% to 50% for iron, from 30% to 47% for vitamin D and, 36% to 46% for calcium. All P-

values for rank-order correlations were below 0.01. Regarding the repeatability of the FFQ, 50%

of food-level responses were concordant (data not shown). For the remainder, the average

discordance was small: two-tenths of a portion when one response was zero, and three-tenths

when both responses were non-zero

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Micronutrients intakes

Iron

Figure 1A shows average iron intakes in women with higher vs. lower relative iron intakes

(groups divided by median total iron intake). Iron intakes from diet as well as iron from

supplements were both significantly higher in women with higher vs. lower total daily iron

intakes (9.1±0.1 vs. 7.4±2.8 mg/d from diet, 50.1±1.3 vs. 17.5±0.5 mg/d from supplement,

p<0.0001 for both comparisons). Overall, iron from supplement intake accounted for a median of

74% of total iron intake, with an interquartile range of 0% to 81% (data not shown). A proportion

of 67.7% of the women took a supplement/multivitamin containing at least 16 mg iron (data not

shown). Overall, 73% took a supplement/multivitamin containing iron and 65% of women met or

exceed RDA for iron, considering only intake from supplement. The three major food

components contributing to dietary iron intake were cold cereals (22.7%), red meat (7.6%) and

pasta (6.5%) (data not shown). Figure 1B shows the proportion of women with intakes below the

median according to maternal characteristics. A higher proportion of women with lower iron

intakes were born outside of Canada (χ2=0.0034, p=0.0435), had less than a university degree

(χ2=0.0071, p=0.0009), had family income of less than $60,000 (χ2=0.0060, p=0.0062), BMI

over 25 kg/m2 (χ2=0.0103, p=0.0001) and were below 30 years of age (χ2=0.0101, p=0.0002). No

significant difference was found for any of the pregnancy outcomes available between women

with lower vs. higher relative iron intakes (data not shown).

Vitamin D

Figure 2A shows average vitamin D intakes in women with higher vs. lower relative vitamin D

intakes (groups divided by median total vitamin D intake). Vitamin D intakes from diet as well as

vitamin D from supplements were significantly higher in women with higher vs. lower total daily

vitamin D intakes (285.4±5.5 vs. 194.9±4.5 IU/d from diet, 631.7±25.9 vs. 169.7±7.8 IU/d from

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supplement, p<0.0001 for both comparison). Overall, vitamin D from supplement intake

accounted for a median of 60% of total vitamin D intake with an interquartile range of 0% to 73%

(data not shown). 73% of the women were taking a supplement/multivitamin containing vitamin

D. This proportion decreased to 66% for a supplement containing at least 400 IU (data not

shown). The three major food components contributing to dietary vitamin D intake were milk

(52.3%), fish (all species) (9.1%), and yogurt (8.6%) (data not shown). Figure 2B shows the

proportion of women with low vitamin D intake according to maternal characteristics. A higher

proportion of women with lower vitamin D intakes were born outside of Canada (χ2=0.0052,

p=0.0074), had less than a university degree (χ2=0.0110, p<0.0.001), family income less than

$60,000 (χ2=0.0111, p=0.0002) and were below 30 years of age (χ2=0.0069, p=0.0040). No

significant difference was found for any of the pregnancy outcomes available between women

with lower vs. higher relative vitamin D intakes (data not shown).

Calcium

Figure 3A shows average calcium intakes in women with higher vs. lower relative calcium

intakes (groups divided by median total calcium intake). Calcium intakes from diet as well as

calcium from supplements were significantly higher in women with higher vs. lower total daily

calcium intakes (1131.3±17.8 vs. 825.3±15.3 mg/d from diet, 443.2±32.3 vs. 136.9±12.7 mg/d

from supplement, p<0.0001 for both comparisons) Overall, calcium from supplement intake

accounted for a median of 18% of total calcium intake with an interquartile range of 0% to 27%.

73% of the women took a supplement/multivitamin containing calcium. The three major food

components contributing to dietary calcium intake were milk (39.3%), cheese (12.0%), and

yogurt (11.6%). Figure 3B shows the proportion of women with low intakes according to

maternal characteristics. A higher proportion of women having lower calcium intakes were born

outside of Canada (χ2=0.0063, p=0.0062). No significant difference was found for any of the

pregnancy outcomes studied between women with lower vs. higher relative calcium intakes

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except for a smaller proportion of women with lower relative calcium intake in women exceeding

the IOM recommendations for gestational weight gain (χ2=0.0041, p=0.0487)

Independent predictors of lower total nutrient intake and daily supplement intake

Table 3 presents multivariate regression models including maternal characteristics as indicators of

lower iron, vitamin D and calcium intakes. Model A presents the risk of having lower iron intake.

Age less than 30 years, pre-pregnancy BMI over 25 kg/m2 and being born outside of Canada were

each significantly associated with lower total iron intake (model A). Having less than a university

degree and being born outside Canada were significantly associated with lower vitamin D intake

(model B). Being born outside of Canada was the only significant indicator of lower calcium

intake (model C)

Significant indicators of taking an iron supplement ≥16 mg daily included age over 30 years

(OR:1.39, CI:1.03-1.87, p=0.0337) and a university degree (OR:1.34, CI:1.10-1.80, p=0.048).

Those taking a vitamin D supplement were more likely to be over 30 years of age (OR:1.54,

CI:1.13-2.12, p=0.0068), hold a university degree (OR:1.56, CI:1.16-2.11, p=0.0039) and be born

in Canada (OR:1.52, CI:1.09-2.11, p=0.0144). These three variables were also significantly

associated with taking a calcium supplement (p<0.03 for all).

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DISCUSSION

Assessment of dietary nutrient intakes in pregnancy is lacking in Canada and valid tools are

necessary to facilitate such investigations. According to our validation analysis, the FFQ in the

current study can be used to rank relative dietary intakes of iron, vitamin D and calcium among

this sample of pregnant women across Canada. For the majority of pregnant women in this study,

iron and vitamin D intakes from supplemental sources accounted for a substantial proportion of

total daily intakes during pregnancy, as other investigators have found (Gomez et al. 2013). In

contrast, most of the calcium intake was from diet, which is also reflected in other studies

(Haugen et al. 2008; Gomez et al. 2013). Pregnant women who were younger, those with a higher

pre-pregnancy BMI and those born outside in Canada were more likely to have lower total dietary

iron intakes. Women with a lower level of education and those born outside Canada were more

likely to have lower vitamin D total intakes. The only significant risk factor associated with lower

total calcium intake was being born outside Canada. In summary, the probability of having lower

iron, vitamin D and calcium intake is higher in women born outside of Canada. Conversely,

significant indicators of taking a supplement (iron, vitamin D and calcium) were age over 30

years and holding a university degree.

An important finding of the current study is that being born outside Canada is an independent risk

factor for having low relative intakes of all nutrients studied. Consistently, these women are

found at higher risk of not taking iron, vitamin D or calcium supplements. This is an significant

finding since 20% of the sample is composed of immigrant women, which is reflective of the

Canadian population (Gagnon et al. 2013). This may represent a considerable challenge from a

nutritional and public health point of view, particularly during pregnancy. It has been shown that

newly-arrived pregnant women are at increased risk for maternal morbidity (Pottie et al. 2011).

Social isolation, poor access to work opportunities, unprotected or unregulated work

environments, lower family income as well as language barriers may explain the increased risk of

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maternal morbidity (Pottie et al. 2011) and possibly the relationship we observed with

micronutrient intakes. It will be of interest for future research to investigate nutritional variables

in relation to the time of acculturation and different immigration classes (ex: refugees, migrant

workers, etc.). Furthermore, new Canadians should receive particular clinical attention regarding

nutrition during pregnancy.

Interestingly, iron and vitamin D supplement intake accounted for an important part of total

intakes of those nutrients, while the contrary was observed for calcium intakes. This finding is

consistent with those from several other recent studies. Haugen et al. found in a large sample of

41,108 pregnant Norwegian women that supplements provided more that 50% of the total intake

of vitamin D and iron, but less than 20% of the total amount for calcium (Haugen et al. 2008). A

Canadian study conducted in 599 pregnant women from Alberta demonstrated that on average,

women met or exceed the RDA for vitamin D and iron, considering only intakes from

supplements, with median daily intakes of 400 IU and 27 mg respectively (Gomez et al. 2013).

Thus, we can assume that supplements accounted for an important part of total intakes of vitamin

D and iron in those women. In the latter study, calcium intake from supplements provided 31% of

the RDA on average (Gomez et al. 2013).

Overall, the proportion of women taking vitamin D and iron supplements (or multivitamins) was

high (73% for both). In a population of 797 Finnish pregnant women, 78% were taking iron

supplements while 40% were taking vitamin D supplements (Arkkola et al. 2006). At the time of

the latter study (2006), there was a recommendation that women take 400 IU of vitamin D from a

supplement during the darker months, from October to March (Arkkola et al. 2006). This may in

part explain the finding, from these authors, of a lower proportion of women taking vitamin D. In

our population, the proportion of women taking vitamin D supplements is relatively high, even

though there is currently no specific recommendation regarding vitamin D supplementation

during pregnancy in Canada. The high proportion of vitamin D coming from supplements that we

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observed in our study is largely explained by vitamin D specifically from multivitamin

supplements. Health organisations and research projects are currently studying strategies to

fortify additional food items (ex: cheese, eggs, etc.) with vitamin D (Browning et al. 2014). It is

of interest to study the feasibility of achieving vitamin D requirements in pregnant women from

diet only, with increased availability of food items containing vitamin D.

The most significant predictors of higher total and supplemental intakes of vitamin D and iron

were older age and higher education. Other studies have demonstrated similar results. Popa et al.

studied 400 pregnant women in Romania and found those with more than 12 years of formal

education were more likely to use an iron supplement during pregnancy (OR, 2.3; 95% CI, 1.1-

4.9) (Popa et al. 2013). Interestingly, nutritional knowledge was a strong predictor of taking iron

supplements in that study (Popa et al. 2013). Nutritional knowledge was not evaluated in our

study but could partly explain the associations we observed between education level and intake of

iron and vitamin D. In another study carried out in a larger sample of 21,889 women from

Tanzania, one factor associated with iron supplementation was advanced age (Ogundipe et al.

2012). A study by Habib et al. found that women with higher education levels were more

compliant in taking iron supplements during pregnancy, which was evaluated at each trimesters

(Habib et al. 2009). Unfortunately, data on supplement use at multiple time points was not

available in the current study, which limits comparison with this study. Similar to our findings,

Arkkola et al. demonstrated that supplement intake during pregnancy was favoured by older and

better-educated Finnish pregnant women (n=797) (Arkkola et al. 2006). We suggest that older

and more educated women are aware of the advantages of taking iron and vitamin D supplement

to achieve the RDA, as was observed in other studies (Popa et al. 2013; Shastri et al. 2014).

The results of our study demonstrate that the one-month semi-quantitative FFQ can be used to

obtain a ranking of iron, calcium and vitamin D intakes. The FFQ consistently underestimated the

total intakes of nutrient, but there are legitimate reasons that could explain the underestimation.

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The limited numbers of questions in the FFQ are meant to capture only the main sources of

nutrients. Foods that are broadly consumed, with a significant concentration of the targeted

nutrients, are ideal candidates for the FFQ. Beyond those targeted foods, there are a multitude of

foods consumed infrequently, by a small proportion of the population, or in small nutrient

concentrations. In order to capture completely the absolute intakes, the FFQ would need to ask an

inordinate amount of questions, and may impose a burden exceeding that of a food diary. If

measurement of absolute intakes was needed, this study would have opted for multiple recalls or

a food diary instead. However, Pearson correlations were strictly positive and Spearman rank-

order correlation estimates were consistently between 30% and 50%. All p-values for rank-order

correlations were significant, providing evidence that the intake measurements were not

statistically independent. Even though the low correlation levels suggest a weak to moderate

statistical association, we can conclude from their consistency, their statistical significance and

the adequate sample size, that the rank order of FFQ intakes provides a valid and reliable method

of ranking the nutrient intake total. Other FFQ questionnaires have been previously validated in

the pregnant Canadian population (Shatenstein et al. 2011; Morisset et al. 2014), but the one used

in the current study is, to our knowledge, the first focusing on these three nutrients, all of which

are important during pregnancy.

As a specific recommendation for the FFQ, consideration should be given to modifying the

question concerning fish consumption, specifying one question for salmon, trout and any other

popular fish with higher vitamin D content, and possibly a second question for other fish species.

This would better identify vitamin D intakes from diet and clarify which fish species contribute to

vitamin D intake, since fish is the second most important food contributor in the current sample.

Finally, to improve dietary assessment of nutrient intakes in pregnancy, it would be interesting to

replicate this study and precisely measure food intake through direct observation at various time

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points during pregnancy, or more achievable, to assess repeated 24-hour dietary recalls in each

trimester for the entire sample.

Strengths and limitations of our study should be acknowledged. First, a targeted FFQ does not

provide usual nutrient intakes; for this reason, comparison with the RDA was not possible.

Second, the FFQ may have underestimated some nutrient intakes. However, using ranking, we

could demonstrate in a large sample of women from across Canada that total nutrient intakes are

associated with some of the maternal characteristics. The requirement that participants be able to

communicate in French or English may have limited the inclusion of women from some ethnic

minorities; however, this restriction only accounted for about 3% of all potentially eligible

women. Moreover, we studied a large and ethnically diverse sample of women from different

provinces across Canada. Of note, participants in the current study were similarly to those in the

full MIREC cohort (n=2001). As observed in the full MIREC cohort, pregnant women tended to

be older and more educated compared to the overall population of Canadian women who gave

birth in 2009 (Arbuckle et al. 2013). However, based on categorical analyses, we were able to

demonstrate that older pregnant women and those with higher education levels were more likely

to have better total nutrient intakes. One can suppose that nutrient intake from diet and the

proportion of women reporting taking a supplement could be lower in a more representative

sample (in terms of maternal age and education level). We assessed total iron, calcium and

vitamin D intakes, including detailed supplement intake, which have been demonstrated to be

important contributors to total intakes of vitamin D and iron. To our knowledge, our study is the

first to examine intakes of iron, vitamin D and calcium in relationship to maternal characteristics

in a large sample in Canada. Supplement intakes were studied only at one time point during

pregnancy; thus, compliance was not assessed. This point merits consideration in future research.

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CONCLUSION

In conclusion, the probability of having lower vitamin D, calcium and iron intake is increased in

women born outside Canada. We also demonstrated that supplement intake is a major contributor

to total iron and vitamin D intakes. Indicators of taking supplements were a higher level of

education, being older, and being born in Canada. From a clinical viewpoint, professional health-

care providers may pay particular attention to pregnant women who are not taking iron and

vitamin D supplements since these are important contributors to total intakes of those nutrients.

ACKNOWLEDGEMENTS: We would like to acknowledge the MIREC Study Group as well as

the MIREC study participants and staff for their dedication.

SOURCE OF FUNDING: The MIREC Study was funded by the Chemicals Management Plan

of Health Canada, the Canadian Institutes for Health Research (MOP – 81285), and the Ontario

Ministry of the Environment. ASM was the recipient of a postdoctoral fellowship from the FRSQ.

CONFLICT OF INTEREST: The authors declare they have no actual or potential competing

financial interests.

AUTHORSHIP: Authors were participating in formulating the research question (ASM, HAW,

WDF) designing the study (WDF, TA, LD), carrying it out (IM, MV), analysing the data (ASM,

MV, LD, HAW, JAM, GDS, TA), writing the article (ASM, GDS, HAW) and reviewing it (all).

ETHICAL STANDARDS DISCLOSURE: This study was conducted according to the

guidelines laid down in the Declaration of Helsinki and all procedures involving human

subjects/patients were approved by the Research Ethics Board at Health Canada and the research

ethics committee at the coordinating centre at Ste-Justine’s Hospital in Montreal, as well as the

academic and hospital ethics committees at each study site.

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REFERENCES

Arbuckle, T.E., Fraser, W.D., Fisher, M., Davis, K., Liang, C.L., Lupien, N., et al.,2013, Cohort profile: the maternal-infant research on environmental chemicals research platform. Paediatr Perinat Epidemiol 27: 415-25. Arkkola, T., Uusitalo, U., Pietikainen, M., Metsala, J., Kronberg-Kippila, C., Erkkola, M., et al.,2006, Dietary intake and use of dietary supplements in relation to demographic variables among pregnant Finnish women. Br J Nutr 96: 913-20. Barker, D.J., Gluckman, P.D., Godfrey, K.M., Harding, J.E., Owens, J.A., andRobinson, J.S.,1993, Fetal nutrition and cardiovascular disease in adult life. Lancet 341: 938-41. Berger, H., Crane, J., Farine, D., Armson, A., De La, R.S., Keenan-Lindsay, L., et al.,2002, Screening for gestational diabetes mellitus. J Obstet.Gynaecol.Can 24: 894-912. Blumfield, M.L., Hure, A.J., Macdonald-Wicks, L., Smith, R., and Collins, C.E.,2013, A systematic review and meta-analysis of micronutrient intakes during pregnancy in developed countries. Nutr Rev 71: 118-32. Browning, L.C. and Cowieson, A.J.,2014, Vitamin D fortification of eggs for human health. J Sci Food Agric 94: 1389-96. CDA,2008, Canadian Diabetes Association 2008 Clinical Practice Guidelines for the Prevention and Management of Diabetes in Canada. Canadian Journal of Diabetes 32: S1-S201. Cockell, K.A., Miller, D.C., andLowell, H.,2009, Application of the Dietary Reference Intakes in developing a recommendation for pregnancy iron supplements in Canada. Am J Clin Nutr 90: 1023-8. Gagnon, A.J., Dougherty, G., Wahoush, O., Saucier, J.F., Dennis, C.L., Stanger, E., et al.,2013, International migration to Canada: the post-birth health of mothers and infants by immigration class. Soc Sci Med 76: 197-207. Gomez, M.F., Field, C.J., Olstad, D.L., Loehr, S., Ramage, S., and McCargar, L.J.,2013, Use of micronutrient supplements among pregnant women in Alberta: results from the Alberta Pregnancy Outcomes and Nutrition (APrON) cohort. Matern Child Nutr. Habib, F., Alabdin, E.H., Alenazy, M., and Nooh, R.,2009, Compliance to iron supplementation during pregnancy. J Obstet Gynaecol 29: 487-92. Haugen, M., Brantsaeter, A.L., Alexander, J., andMeltzer, H.M.,2008, Dietary supplements contribute substantially to the total nutrient intake in pregnant Norwegian women. Ann Nutr Metab 52: 272-80. Health Canada,2004, Canadian community Health Survey, Cycle 2.2, Nutrition: Statistics Canada.

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Hofmeyr, G.J., Lawrie, T.A., Atallah, A.N., and Duley, L.,2010, Calcium supplementation during pregnancy for preventing hypertensive disorders and related problems. Cochrane Database Syst Rev: CD001059. Institute of Medicine,1992, Nutrition During Pregnancy and Lactation: An Implementation Guide: Insitute of Medicine, National Academies Press: Washington, DC. Institute of Medicine,2009, Weight gain recommendations: reexamining the guidelines. Committee to Reexamine IOM Pregnancy Weight Guidelines, Institute of Medicine, National Research Council, Washington, DC: National Academy Press. Kramer, M.S., Platt, R.W., Wen, S.W., Joseph, K.S., Allen, A., Abrahamowicz, M., et al.,2001, A new and improved population-based Canadian reference for birth weight for gestational age. Pediatrics 108: E35. Morisset, A.S., Cote, J.A., Michaud, A., Robitaille, J., Tchernof, A., Dube, M.C., et al.,2014, Dietary intakes in the nutritional management of gestational diabetes mellitus. Can J Diet Pract Res 75: 64-71. Ogundipe, O., Hoyo, C., Ostbye, T., Oneko, O., Manongi, R., Lie, R.T., et al.,2012, Factors associated with prenatal folic acid and iron supplementation among 21,889 pregnant women in Northern Tanzania: a cross-sectional hospital-based study. BMC Public Health 12: 481. Olausson, H., Goldberg, G.R., Laskey, M.A., Schoenmakers, I., Jarjou, L.M., andPrentice, A.,2012, Calcium economy in human pregnancy and lactation. Nutr Res Rev 25: 40-67. Otten, J., Hellwig, J., andMeyers, L.,2006, Dietary Reference Intakes: The Essential Guide to Nutrient Requirements Washington DC. Popa, A.D., Nita, O., Graur Arhire, L.I., Popescu, R.M., Botnariu, G.E., Mihalache, L., et al.,2013, Nutritional knowledge as a determinant of vitamin and mineral supplementation during pregnancy. BMC Public Health 13: 1105. Pottie, K., Greenaway, C., Feightner, J., Welch, V., Swinkels, H., Rashid, M., et al.,2011, Evidence-based clinical guidelines for immigrants and refugees. CMAJ 183: E824-925. Scholl, T.O. and Reilly, T.,2000, Anemia, iron and pregnancy outcome. J Nutr 130: 443S-447S. Shastri, L., Mishra, P.E., Dwarkanath, P., Thomas, T., Duggan, C., Bosch, R., et al.,2014, Association of oral iron supplementation with birth outcomes in non-anaemic South Indian pregnant women. Eur J Clin Nutr. Shatenstein, B., Xu, H., Luo, Z.C., and Fraser, W.,2011, Relative validity of a food frequency questionnaire for pregnant women. Can J Diet Pract Res 72: 60-9. Simpson, J.L., Bailey, L.B., Pietrzik, K., Shane, B., and Holzgreve, W.,2011, Micronutrients and women of reproductive potential: required dietary intake and consequences of dietary deficiency or excess. Part II--vitamin D, vitamin A, iron, zinc, iodine, essential fatty acids. J Matern Fetal Neonatal Med 24: 1-24.

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Wei, S.Q., Qi, H.P., Luo, Z.C., and Fraser, W.D.,2013, Maternal vitamin D status and adverse pregnancy outcomes: a systematic review and meta-analysis. J Matern Fetal Neonatal Med 26: 889-99.

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TABLES AND FIGURES

Table 1. Characteristics of the study population

All (n=1186)

Variables Mean ± SD / n (%) Maternal age (years) 32.7 ± 5.0

<20 1 (0.1) 20-24 58 (4.9) 25-29 262 (22.1) 30-34 417 (35.2) 35+ 448 (37.8)

Parity (number of previous viable pregnancy) 0 532 (44.9) 1 490 (41.3) 2 125 (10.5) 3+ 39 (3.3)

Education level High school or less 100 (8.4) Some college 69 (5.8) College diploma 262 (22.1) University degree 753 (63.5)

Family income from all sources ($) <20 000 53 (4.5) 20 001 - 40 000 89 (7.5) 40 001 - 60 000 119 (10.0) 60 001 - 80 000 181 (15.3) 80 001 - 100 000 238 (20.0) 100 001+ 459 (38.7) No response 47 (4.0)

Mother born in Canada Yes 944 (79.6)

Pre-pregnancy BMI (kg/m2)a 24.8 ± 5.4 Underweight (<18.5) 35 (3.2) Normal weight (18.5-24.99) 675 (61.4) Overweight (25.00-29.99) 235 (21.4) Obese (≥30.00) 153 (14.0)

Gestational age at delivery (wks)b 39.32 ± 1.68 Preterm birth (<37 wks) 82 (3.2)

Birth weight (g) 3457.5 ± 522.7 SGA (≤10th percentile for gestational age) 55 (4.6) LGA (≥90th percentile for gestational age) 148 (12.5)

Infant sex Male 633 (53.4) Female 552 (46.5)

Gestational weight gain (kg)b 15.5 ± 6.0 Below IOM recommendations 115 (15.2) Within IOM recommendations 218 (28.9) Above IOM recommendations 422 (55.9)

Glucose intolerance (GDM or IGT)c 67 (8.6)

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BMI: body mass index, IOM: Institute of Medicine, GDM: gestational diabetes mellitus, IGT:

impaired glucose tolerance, an=1100, bn=755, cn=833

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Table 2. Validation correlation analysis, for comparison between 24-hour-recall and FFQ in a subsample of 115 women 1

Average intake Pearson correlations Spearman rank-

order correlations

Nutrient name Recall visit

FFQ visit

From recall

From FFQ

Estimate (%)

P-value Estimate

(%) P-value

Amount (g/d) First First 3544.9 1337.7 27.0 0.0035 29.6 0.0013

Amount (g/d) Second Second 3791.9 1285.1 16.3 0.0814 17.2 0.0658

Amount (g/d) Avg First 3668.4 1337.7 16.5 0.0783 29.8 0.0012

Amount (g/d) Avg Second 3668.4 1285.1 22.2 0.0172 21.8 0.0195

Iron (mg/d) First First 17.8 8.7 31.0 0.0007 41.6 <0.0001

Iron (mg/d) Second Second 17.3 8.0 38.1 <0.0001 47.3 <0.0001

Iron (mg/d) Avg First 17.6 8.7 37.0 <0.0001 48.1 <0.0001

Iron (mg/d) Avg Second 17.6 8.0 41.5 <0.0001 49.5 <0.0001

Vitamin D (µg/d) First First 7.0 5.9 16.3 0.0827 30.0 0.0011

Vitamin D (µg/d) Second Second 6.1 6.0 26.7 0.004 37.4 <0.0001

Vitamin D (µg/d) Avg First 6.5 5.9 25.6 0.0058 37.2 <0.0001

Vitamin D (µg/d) Avg Second 6.5 6.0 44.9 <0.0001 47.2 <0.0001

Calcium (mg/d) First First 1311.6 958.5 43.2 <0.0001 41.4 <0.0001

Calcium (mg/d) Second Second 1292.5 935.0 30.9 0.0008 35.7 <0.0001

Calcium (mg/d) Avg First 1302.0 958.5 41.0 <0.0001 42.3 <0.0001

Calcium (mg/d) Avg Second 1302.0 935.0 47.0 <0.0001 46.1 <0.0001

2

FFQ : Food frequency questionnaire; Avg : average, 3

4

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Table 3. Multivariate logistic regression analysis for the risk of having lower total nutrient intake, including various maternal characteristics

Odds ratio 95%CI P Value

Model A - Iron intake

Maternal age (<30 vs. ≥30 years old) 1.54 1.15-2.06 0.0037

Pre-pregnancy BMI (≥25 vs. <25 kg/m2) 1.61 1.253-2.09 0.0002

Family income (<60 000 vs. ≥$60 000) 1.10 0.79-1.51 NS

Education level (<university vs. ≥university degree) 1.19 0.91-1.57 NS

Country of birth (other countries vs. Canada) 1.54 1.14-2.09 0.0053

Model B - Vitamin D intake

Maternal age (<30 vs. ≥30 years old) 1.24 0.93-1.66 NS

Pre-pregnancy BMI (≥25 vs. <25 kg/m2) 1.03 0.80-1.33 NS


Education level (<university vs. ≥university) 1.47 1.12-1.93 0.0053


Model C - Calcium intake

Maternal age (<30 vs. ≥30 years old) 1.00 0.75-1.33 NS

Pre-pregnancy BMI (≥25 vs. <25 kg/m2) 1.11 0.87-1.44 NS


Education level (<university vs. ≥university) 1.15 0.88-1.51 NS


BMI: body mass index, NS: non-significant

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FIGURE LEGENDS

Figure 1. Total iron intakes and relationship with maternal characteristics. A. Average total

iron intakes for women with low (<33.7 mg, left column) and high median intakes (> 33.7 mg,

right column) ± SEM (black line). Iron intakes from foods are in black; iron intakes from

supplements are in gray. B. Bars represent the proportion of women with lower iron intakes

according to maternal characteristics (country of birth, education level, family income, pre-

pregnancy BMI and maternal age). *P value ≤ 0.05 indicates a significant difference in the

proportion of women having lower iron intakes vs. higher iron intakes for each maternal

characteristic (chi-square comparison). BMI: body mass index.

Figure 2. Total vitamin D intakes and relationship with maternal characteristics A. Average

total vitamin D intakes for women with low (<581.5 IU, left column) and high median intakes

(>581.5 UI, right column) ± SEM (black line). Vitamin D intakes from foods are in black;

vitamin D intakes from supplements are in gray. B. Bars represent the proportion of women with

lower vitamin D intakes according to maternal characteristics (country of birth, education level,

family income, pre-pregnancy BMI and maternal age). *P value ≤ 0.05 indicates a significant

difference in the proportion of women having lower vitamin D intakes vs. higher vitamin D

intakes for each maternal characteristic (chi-square comparison). BMI: body mass index.

Figure 3. Total calcium intakes and relationship with maternal characteristics. A. Average

total calcium intakes for women with low (<1150.5 mg, left column) and high median intakes

(>1150.5 mg, right column) ± SEM (black line). Calcium intakes from foods are in black;

calcium intakes from supplements are in gray. B. Bars represent the proportion of women with

lower calcium intakes according to maternal characteristics (country of birth, education level,

family income, pre-pregnancy BMI and maternal age).*P value ≤ 0.05 indicates a significant

difference in the proportion of women having lower vitamin D intakes vs. higher vitamin D

intakes for each maternal characteristic (chi-square comparison). BMI: body mass index.

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A.

Figure 1.

B. Lower intakes Higher intakes

10

0

20

30

40

50

60

70

Iron

(mg)

FoodsSupplements

Age < 30Age ≥ 30

BMI < 25BMI ≥ 25

Income < $60 000Income ≥ $60 000

Less than University degreeUniversity degree

Mothers not born in CanadaMothers born in Canada

Proportion of women with lower iron intake (%)

*

*

**

*

0 20 40 60 80

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A.

Figure 2.

B.Lower intakes Higher intakes

FoodsSupplements

Age < 30Age ≥ 30

BMI < 25BMI ≥ 25

Income < $60 000Income ≥ $60 000



Proportion of women with lower iron intake (%)0 20 40 60 80

0

200

400

600

800

1000

1200

Vita

min

D (I

U)

*

*

*

*

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A.

Figure 3.

B. Lower intakes Higher intakes

FoodsSupplements

Age < 30Age ≥ 30

BMI < 25BMI ≥ 25

Income < $60 000Income ≥ $60 000



Proportion of women with lower iron intake (%)0 20 40 60 80

0

500

1000

1500

2000

Cal

cium

(mg)

*

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