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Nutrient intakes and nutritional biomarkers in pregnant adolescents: a systematic review of studies in developed countries

BMC Pregnancy and ChildbirthBMC series – open, inclusive and trusted201616:268

https://doi.org/10.1186/s12884-016-1059-9

Received: 23 April 2016

Accepted: 6 September 2016

Published: 15 September 2016

Abstract

Background

Babies born to adolescent mothers have been shown to have poorer outcomes compared to those born to adults. Nutritional status may have an important role to play in improving the health of pregnant adolescents; however there is a lack of evidence regarding the adequacy of adolescent diets during pregnancy. This systematic review aims to examine what is known about the nutritional status of adolescent pregnant women.

Methods

A systematic search of the literature identified 21 studies which met the inclusion criteria for the review. Primary research papers using any methods were included where they were published in English between January 1995 and May 2015 and included measurements of nutrient intakes or biological markers of nutritional status in pregnant women aged 11–19 years. Individual study data was first summarised narratively before study means were pooled to give an estimate of nutritional status in the population.

Results

The results show that individual studies reported intakes of energy, fibre and a number of key micronutrients which were below recommended levels. Biological markers of iron and selenium status also showed cause for concern. Pooled analysis of individual means as a percentage of UK Dietary Reference Intakes showed intakes of vitamin D (34.8 % CI 0–83.1) to be significantly below recommendations (p = 0.05). Serum selenium levels were also found to be low (61.8 μg/L, CI 39–84).

Conclusions

This review has identified a number of areas where the nutritional status of pregnant adolescents is sub-optimal, which may have implications for the health of adolescent mothers and their babies. It was not however possible to examine the impact of supplement use or socio-demographic characteristics which limits the interpretation these results. Further work is needed to establish the characteristics of those most at risk within this population, how this differs from adult pregnant women and the role of supplementation in achieving adequate nutrition.

Keywords

Adolescent Pregnancy Nutrition Systematic review

Background

Pregnancy during adolescence is often viewed as a social problem with women who have a child during the teenage years being more likely to suffer social isolation, poverty, lower levels of educational achievement and be unemployed or work in low paid jobs [1]. Rates of teenage conceptions both in the UK and internationally have reduced over recent years; however there are still a significant number of young women having pregnancies and giving birth at a young age. The rate of deliveries to young women aged 15–19 in the UK in 2012 was the highest in the European Union at 19.7 births per 1,000 females in the age group. This does however represent a reduction of more than a quarter (26.8 %) in the UK since 2004. The birth rates to young women in other developed countries have followed a similar pattern of decline, yet rates remain relatively high in the United States (29.4), New Zealand (24.9) and Australia (16.1) [2].

As well as the potential for adverse social outcomes associated with adolescent pregnancies there is evidence to suggest that health outcomes may be less favourable for younger mothers. A systematic review [3] aiming to assess the relationship between early first childbirth and increased risk of poor pregnancy outcomes found that very young maternal age (<15 years or less than 2 years after menarche) had a negative effect on both maternal and foetal growth and infant survival. It is suggested that young women who are still themselves growing may compete with the foetus for nutrients, which may in turn impair foetal growth and result in low birth weight babies or babies who are small for their gestational age. The review also found a moderate relationship between young maternal age and anaemia, premature birth and neonatal mortality.

It has long been established that good pregnancy nutrition has an important influence on birth outcomes, foetal growth and infant survival [4]. While specific nutritional issues may have changed since this early work, it is still maintained that mothers need to consume an adequate, yet not excessive diet in order to optimise pregnancy and birth outcomes [5]. Quantification of dietary adequacy in populations is difficult because individuals will have differing nutrient needs. This is especially true during phases of growth and physical change such as adolescence. However, the use of dietary reference intakes to estimate the adequacy of nutritional intakes has been established as acceptable [6] where the appropriate values for the age, sex and, in the case of pregnant women, stage of pregnancy are used. Evidence also suggests that nutritional needs change during the course of pregnancy with requirements for energy and several micronutrients increasing as pregnancy progresses [7].

Dietary habits of adolescent girls are often poorer than that of older women. The latest results of the UK National Diet and Nutrition Survey [8] showed that girls aged 11–18 years consumed 2.7 portions of fruit and vegetables per day compared to 4.1 portions in women aged 19–64, and adolescent girls also had some of the highest intakes of sugar-sweetened beverages within this dataset. A higher proportion of adolescent girls also had intakes of key vitamins and minerals below the lower reference nutrient intake level than adult women, including vitamin A, riboflavin, vitamin B12, folate, iron, calcium, magnesium, potassium, zinc and iodine. Dietary patterns across highly developed countries have been shown to have substantial similarities [9], while the same cannot be said for less developed regions.

While the evidence presented above suggests that adolescent girls often have a poorer diet than adult women in the general population this may not also necessarily be the case in those who are pregnant. Two systematic reviews have previously been conducted [10, 11] which explored nutritional intake and biochemical markers in pregnant adolescents living in developed countries. It was acknowledged in these reviews that there was a lack of good quality evidence in relation to these topics. However the author concluded that there was some consensus in the available literature that pregnant adolescents had intakes of energy, iron, folate, calcium, vitamin E and magnesium which were below the dietary recommended intakes. The review of biochemical markers reported that indicators of anaemia and iron status were compromised in this population; however no further conclusions could be drawn from the limited available evidence. It is therefore important that the most recent evidence relating to the nutritional intake and status of pregnant adolescents is examined in order to establish what the particular issues may be for this group. The aim of his systematic review was therefore to investigate the nutritional status of pregnant adolescents living in developed countries.

Methods

Search strategy

The search strategy was developed using search terms detailed in Table 1 and applied across nine key electronic databases (AMED, ASSIA, CINAHL, Child Development and Adolescent Studies, Cochrane Library, Health Source: Nursing, Maternity and Infant Care, MEDLINE and MEDLINE in Process, SCOPUS). Reference lists of identified papers were hand searched, and reference and citation functions were used where available.
Table 1

Search terms

Theme

Nutritional Intake

Pregnancy

Age

Nutritional Status

Search Terms

nutrient

pregnan*

adolescen*

biomarker*

nutrition*

gestatio*

teen

iron

diet*

matern*

teenage*

folate

eat*

mother*

youth

calcium

food

gravid*

 

anaemi*

nutrition assessment (MH)

Pregnancy in adolescence (MH)

 

anemi*

Food habits (MH)

  

Biological markers (MH)

Dietary surveys (MH)

   

* indicates truncation of search tearm

Table 1 search terms The main stages of the review including the number of references identified at each stage are illustrated in Fig. 1.
Fig. 1

Protocol for systematic review

Inclusion criteria

Studies were limited to primary research papers using any methods published in English between 1995 and May 2015.

Studies were included where they provided data regarding either the nutritional intake or a biological marker of nutrient status of adolescents aged 11–19 years at any stage of pregnancy, from countries considered as having very high levels of human development by the United Nations Human Development Index [12]. This index has been selected as it provides a multidimensional model incorporating not only wealth but also health and education, and so provides a more reliable basis for assuming some commonality between countries of origin of the included studies. The definition of adolescence has been chosen to correspond with the World Health Organisation Growth Index [13].

Quality appraisal

The identified papers were assessed for risk of bias using the Critical Appraisal and Skills Program (CASP) checklist for systematic reviews [14] which was adapted to accommodate cross-sectional studies. Aspects of the studies giving an indication of methodological and interpretive rigor (e.g. research design, clear statement of research aims, recruitment of participants, consideration of confounding factors and reporting of results) were graded as either ‘good’ (+), ‘adequate or unclear’ (−/+) or poor (−), studies were then given an overall grade for quality.

Data extraction

Included studies were grouped depending on whether the study examined nutrient intake, biological markers of nutritional status or both. Information from the included studies was entered in to data extraction sheets using Microsoft Excel, one each for nutrient intakes and biological markers, and checked by a second reviewer.

Data synthesis

Reported data were first tabulated to explore patterns across the included studies and described narratively. Where 95 % confidence intervals were not reported they were calculated for the mean and used to assess the extent to which the study mean differed from the relevant reference value. Where the lower confidence limit was above the reference value the study mean was considered to be significantly higher, where the upper confidence limit was below the reference value the study mean was considered significantly lower, otherwise no significant difference was reported.

Analysis of micronutrient intakes was undertaken by comparing the reported data from included studies with the UK reference nutrient intake (RNI) [15] and US recommended daily allowance (RDA) [16] where available. Analysis has been undertaken using both UK and US thresholds as, while the majority of studies were undertaken in the USA, this review is also concerned with applying the results to the UK context. Energy intake was calculated by taking the mean of the single year of age estimated average requirements (EAR) for young women aged 11–19 with an increment applied in the third trimester; a population level EAR is only available in the UK [17]. For macronutrients an estimate of the percentage contribution to energy, if not provided, was calculated from the mean macronutrient intake and the mean energy intake.

In the case of biological markers, minimum thresholds for nutrient deficiency provided by WHO, UK and US authorities (where available) have been compared with reported study data. Nationally or internationally recognised cut offs for deficiency are not currently available for zinc, selenium, copper, magnesium and phosphorous, therefore these elements have been compared with suggested thresholds in academic literature [1822].

Where data were available from two or more studies for a single nutrient or biological marker a pooled mean was calculated and weighted by the number of participants in each study. Mean measures of micronutrient and energy intake were expressed as a percentage of dietary reference values to allow for comparisons across different nutrients.

Sub-group analyses were performed by country of origin (USA only and UK only), stage of pregnancy (first, second and third trimester and reported average over the pregnancy) and age of adolescents (15 years and under and 16–19 years).

Results

A total of 4,084 unique papers were identified from the search of the literature with 78 studies remaining after title and abstract screening. Following examination of the full text of these papers a total of 21 papers were identified that met the review inclusion criteria. Details of the excluded studies are given in Additional file 1: Table S1. In brief, the main reasons for exclusion were not reporting appropriate data and the study population not meeting the inclusion criteria for age or pregnancy.

No studies were excluded for reasons of poor quality; after quality assessment 16 of the included studies were considered to be of good quality while the remaining five studies were of a satisfactory standard (Table 2).
Table 2

Characteristics of included studies

Study Information

Participants

Supplements

Measurement

Quality

Study

Country

Study design

Study groups

Number

Age

Inclusion criteria

Exclusion criteria

Supplement type and dose

Number with available data

Estimated compliance: N (%)

Data collection method (s)

Time period(s)

Quality rating

Baker et.al (2009) [23]

UK

Cross-sectional study

NA

500

14–18

Singleton pregnancy, age 14–18, gestational age < =20 weeks

Inability to provide informed consent, preeclampsia, clotting disorders, HIV/AIDS, haemoglobinopathies, diabetes, renal disease, hypertension, multiple gestations, history of 3= > previous miscarriages

Preconception folic acid

498

34 (6.9)

24 h recall (multiple)

Third trimester

+

Folic acid in early pregnancy

498

220 (44.2)

Iron in early pregnancy

498

39 (7.8)

Multivitamins in early pregnancy

498

19 (3.8)

Folic acid only in 3rd trimester

290

5 (1.7)

Iron and folic acid in 3rd trimester

290

13 (4.5)

Iron only in 3rd trimester

290

42 (14.5)

Multivitamins in 3rd trimester

290

7 (2.4)

Castillo-Duran et.al (2001) [43]

Chile

RCT

Zinc supplemented

249

16.4 (mean)

Beginning prenatal visits before 20 weeks gestation, aged <19 at estimated due date

Adolescents whose background included chronic diseases, drug abuse, mental retardation, illiteracy or pregnancy due to incest or rape

20 mg Zinc sulphate daily

Intervention group - 249

At least 50 % compliance

24 h recall (multiple)

Second and third trimester

+

Placebo

258

40 mg iron sulphate

All participants - 507

 

Chan et.al (2006) [24]

USA

RCT

Control group, 2 intervention groups excluded from review*

23

15–17

Enrolled before 20 weeks gestation

Hypertension, diabetes, renal or liver disease, alcohol or tobacco use, using medicines effecting Ca metabolism

No additional supplements reported

  

Food diary (weighing not mentioned)

Second and third trimester

−/+

Chang et.al (2003) [37]

USA

Retrospective chart review

NA

918

12–17

Self-reported racial group as African-American; singleton pregnancy

Birth results not available due to abortion, miscarriage or transfer of care

90 mg carbonyl iron daily plus additional up to 120 mg for those classified as anaemic

918

Not reported

Not reported

Second and third trimester

+

Dawson et.al (2000) [35]

USA

RCT

One-A-Day without Iron

20

16–20

Aged 16–20, less than 16 weeks gestation, no iron supplementation for previous 30 days

Hypertension; diabetes; other medical problems; haemoglobin <11 g/dL; haematocrit <30 %

Vitamin A 5000 IU, vitamin D 400 IU, vitamin E 10 mg, vitamin C 60 mg, folic acid 0.4 mg, thiamine 1.5 mg, riboflavin 1.7 mg, niacin 20 mg, pyridoxine 2 mg, vitamin B- 6 mg, pantothenic acid 10 mg

20

Not reported

Venous blood sample

Second and third trimester and delivery

−/+

One-A-Day with Iron

20

18 mg Iron, Vitamin A 5000 IU, vitamin D 400 IU, vitamin E 10 mg, vitamin C 60 mg, folic acid 0.4 mg, thiamine 1.5 mg, riboflavin 1.7 mg, niacin 20 mg, pyridoxine 2 mg, vitamin B- 6 mg, pantothenic acid 10 mg

20

Derbyshire (2009) [39]

UK

Cross-sectional study

NA

20

15–19

Attending antenatal classes or community clinics

Incomplete diary

None reported

  

Food diary unweighed

Third trimester

+

Gadowsky et.al (1995) [42]

Canada

Cross-sectional study

NA

58

14–19

Not reported

Not reported

Folic Acid Mean 479 μg/day

58

82 %

Venous blood sample

Third trimester

+

Elemental Iron Mean 31.5 mg/day

Cyanocobalamin (B12) Mean 2.24 μg/d

Giddens et.al (2000) [27]

USA

RCT (subset from a larger study)

NA

59

13–18

Singleton pregnancies, between 13 and 19 weeks gestation

Not reported

Reported that any contribution from supplements was not included in analysis

  

Food diary weighed

Mean over pregnancy

−/+

Ginde et.al (2010) [32]

USA

Secondary analysis of cross sectional survey

NA

84

13–19

Not reported

Not reported

Some participants taking vitamin D supplements

Not reported

Not reported

Venous blood sample

Mean over pregnancy

+

Gutierrez et.al (1999) [28]

USA

Cross-sectional study

NA

46

13–18

Self-identified ethnicity as Mexican American, primigravida, 13–18 years of age

History of miscarriage or health problems, involved in competitive athletic performances or heavy exercise, planned to move away during study period

None reported

  

24 h recall (single)

Second and third trimester

+

Iannotti et.al (2005) [36]

USA

Cross-sectional study

NA

80

13–18

Self-reported racial group as African-American; singleton pregnancy

Not reported

None reported

  

10 ml Venous blood sample

Second and third trimesters

+

Job et.al (1995) [41]

Australia

Cross-sectional study

NA

35

13–19

Not reported

Not reported

None reported

  

24 h recall

Mean over pregnancy

+

Lee et.al (2013) [25]

USA

Cross-sectional study

NA

156

13–18

Age 18 or under, carrying a single fetus, 12–30 weeks gestation at recruitment

Not reported

Reported that any contribution from supplements was not included in analysis

  

24 h recall (multiple)

<23 weeks gestation, 23–30 weeks gestation and Mean over pregnancy

+

McGuire et.al. (2010) [31]

USA

Cross-sectional study

NA

80

Under 18 (mean 16.5)

Self-reported ethnic group as African American, singleton pregnancy

Not reported

Routinely prescribed prenatal supplements containing 400 IU vitamin D

 

Data not available

Venous blood sample

Second and third trimester

+

Meier et.al (2002) [34]

USA

RCT

Iron supplemented

20

15–18

Not reported

Iron deficiency anaemia at recruitment

60 mg elemental iron & 1 mg folic acid

20

 

Venous blood sample

Second and third trimesters

+

Placebo

17

1 mg folic acid

17

Mistry et.al (2014) [40]

UK

Cross-sectional study

Appropriate for gestational age babies

107

14–18

Not reported

Inability to provide informed consent, pre-eclampsia, clotting disorders, HIV/AIDS, Haemoglobinpathies, diabetes, renal disease, hypertension, multiple pregnancy and previous miscarriage

None reported

  

30 ml venous blood sample

Third trimester

+

Small for gestational age babies

9

O’Brien et.al (2003) [33]

USA

Cross-sectional study

NA

23

Mean 16.5

First, singleton pregnancies; no medical problems; no medications known to influence calcium metabolism; non-smokers; no history of drug or alcohol abuse

Not reported

Prenatal supplement including 5 mmol Ca

23

39 %

Not reported

Third trimester

+

Pobocik et.al (2003) [38]

Guam (USA Teritory)

Cross-sectional study

NA

434

14–20

Not reported

Not reported

Reported that any contribution from supplements was not included in analysis

  

24 h recall (single)

Mean over pregnancy

−/+

Rycel et.al (2009) [44]

Poland

Retro-spective cohort

NA

102

15–18

Not reported

Not reported

none reported

  

Venous blood sample

Before and after delivery

−/+

Young et.al (2010) [29]

USA

Cross-sectional study

NA

92

14–18

Healthy, singleton pregnancy

HIV, diabetes, pre-eclampsia, eating disorders, malabsorption diseases, self-reported drug use

Prenatal supplement including 27 mg iron

92

Not reported

Venous blood sample

Second trimester and delivery

+

Young et.al (2012) [30]

USA

Cross-sectional study

NA

171

Under 18 (mean 17.1)

Healthy, singleton pregnancy

HIV, diabetes, pre-eclampsia, eating disorders, malabsorption diseases

400 IU Vitamin D supplement given to participants found to be deficient

46 (estimated from reported percentages)

26.4 % - daily, 35.8 % at least twice per week

10 ml venous blood sample

Delivery

+

Of the included studies, six provided information on dietary intakes only, 12 on biological markers only and three reported both types of information. Nutrient intakes from food sources were reported (therefore excluding any contribution from supplements) in all but one paper [23]. However, the majority (10 out of 15) of papers reporting biological markers also reported that participants were taking nutritional supplements, details of which along with other characteristics of the included studies are shown in Table 2. Due to inconsistencies in the type, dose, duration and compliance with supplement use it was not possible to quantify the impact of supplements on the results.

Of the 21 included studies 14 were carried out in the USA [2437], one in the US territory of Guam [38], three in the UK [23, 39, 40] and one in each of Australia [41], Canada [42], Chile [43] and Poland [44]. Nutritional status was a primary outcome measure in all but one of the included studies where the primary outcomes were birth weight and prematurity [43].

The study designs of the included studies are listed within Table 2. The majority of the studies were cross-sectional surveys. Five studies were randomised controlled trials, where baseline dietary assessments before randomisation, or data from the control group only, permitted the inclusion of nutritional intake or biomarker data cross-sectionally. One study was a retrospective cohort analysis and one was a retrospective chart review.

Participants were all aged between 12 and 20 years with the majority being aged 16 and over. The majority of studies selected participants using convenience samples; other sampling methods used were purposive [26], representative probability sample [32], stratified random sample [44] and a retrospective medical chart review including all eligible records [37].

The majority of studies reported a range of ethnicities in the sample with the exception of three studies where all participants were African American [31, 36, 37], one including only Mexican American participants [28] and one where all participants were White [26]. Where reported the majority of participants had a BMI in the healthy range. Six studies reported participant’s weight gain from recruitment to delivery which ranged from 14 to 17 kg.

All but two of the studies reporting biological markers collected venous blood samples which were analysed in laboratories using standard testing procedures. One study which was a medical records review [37] did not provide details of how samples were collected. One study also assessed biological markers of calcium absorption using a 24 h urine collection followed by daily spot urine collections [33]. Data relating to participants nutrient intakes used a variety of data collection methods. Three studies used food diaries [24, 27, 39], one of which was weighed [27]. The remaining studies used single [28, 38, 41] or multiple [25, 43, 23] 24 h recalls. Four out of the nine studies reporting nutrient intakes stated that dietary assessments were carried out by a trained nutritionist or similar professional [25, 26, 43, 27].

Nutrient intakes

Energy intake was reported by nine studies with seven of these reporting intakes below the recommendations at one or more time point (Table 3). Four studies also reported gestational weight gain which ranged from 14 to 17 kg. Pooled analysis of the percentage of the EAR for energy in these 10 studies revealed wide confidence limits around the estimated mean, with an average intake 9 % lower than the UK EAR (mean % EAR, 91.2 %, CI 29.6–152.8 %). Analysis of energy intake by trimester and study country of origin did not show any significant differences (UK studies 89.1 % CI 39.2–139.1 %, US studies 100.4 %, CI 24.2–176.6 %). Analysis of those studies reporting gestational weight gain only showed young women to be achieving a higher percentage of the EAR for energy (99.1 %, CI 41.0–157.2 %) than those studies which did not report weight gain (90.2 %, CI 27.9–152.5 %) but this difference was not statistically significant.
Table 3

Mean energy intake in individual studies compared to UK estimated average requirement

 

Study

Second Trimester

Third Trimester

Mean over pregnancy

N=

Mean

Confidence Interval

N=

Mean

Confidence Interval

N=

Mean

Confidence Interval

Energy kcal/day a

Baker (2009)

   

290

↓2147

2075, 2219

   

Castillo-Duran (2001) a

249

↓1887

1825, 1949

249

↓2030

1968, 2092

   

Castillo-Duran (2001) b

258

↓1863

1790, 1936

258

↓1982

1927, 2038

   

Chan (2006)

23

↔2223

2057, 2389

23

↓2276

2059, 2493

   

Derbyshire (2009)

   

20

↓2273

2052, 2494

   

Giddens (2000)

      

59

↓2342

2187, 2497

Gutierrez (1999)

46

↔2390

2150, 2630

46

↔2620

2389, 2851

   

Job (1995)

      

70

↓2134

1949, 2320

Lee (2013)

   

133

↓2303

2161, 2446

156

↔2273

2167, 2379

Pobocik (2003)

      

434

↑2487

2388, 2586

aComparison to UK EARs, First and Second Trimester requirement (Average UK EAR for Females aged 11–19) 2355 kcal/day, Third Trimester requirement 2546 kcal/day, Mean over pregnancy requirement (average of three trimester values) 2419 kcal/d, ↑ Study mean higher than reference value (p < 0.05), ↔ Study mean not different to reference value (p < 0.05), ↓ Study mean lower than reference value (p < 0.05)

Mean intakes of macronutrients are show in Table 4. Intakes of protein and total carbohydrate were roughly in line with recommendations. There were too few studies reporting intakes of total fat, fat types or sugars to permit conclusions to be drawn. Three studies reported any measurements of dietary fibre, all of which were below recommended levels.
Table 4

Mean intakes of macronutrients (g/day or percent of energy) and dietary fibre (g/day) in individual studies compared to UK and US dietary reference values

  

Comparison to UK Dietary Reference Value

Comparison to US Dietary Reference Value

Nutrient

Study

Second Trimester

Third Trimester

Mean over pregnancy

Second Trimester

Third Trimester

Mean over pregnancy

N=

Mean

Confidence Interval

N=

Mean

Confidence Interval

N=

Mean

Confidence Interval

N=

Mean

Confidence Interval

N=

Mean

Confidence Interval

N=

Mean

Confidence Interval

Protein grams/day a

Castillo-Duran (2001) a

249

↑60

58, 62

249

↑62

59, 64

   

249

↓60

58, 62

249

↓62

59, 64

   

Castillo-Duran (2001) b

258

↑59

57, 61

258

↑60

58, 61

   

258

↓59

57, 61

258

↓60

58, 61

   

Chan (2006)

23

↑76

65, 87

23

↑76

65, 87

   

23

↔76

65, 87

23

↔76

65, 87

   

Derbyshire (2009)

   

20

↑72

65, 79

      

20

↔72

65, 79

   

Giddens (2000)

      

59

↑82

77, 87

      

59

↑82

77, 87

Gutierrez (1999)

46

↑111

98, 124

46

↑118

105, 130

   

46

↑111

98, 124

46

↑118

105, 130

   

Job (1995)

      

70

↑73

73, 73

      

70

↑73

73, 73

Lee (2013)

   

133

↑81

76, 87

156

↑70

65, 75

   

133

↑81

76, 87

156

↔70

65, 75

Pobocik (2003)

      

434

↑99

95, 103

      

434

↑99

95, 103

Englyst Fibre grams/day b

Derbyshire (2009)

    

↓12

11, 13

            

AOAC Fibre grams/day c

Giddens (2000)

               

59

↓14

13, 15

Lee (2013)

            

133

↓13

12, 14

156

↓14

13,14

  

N=

% of Energy

 

N=

% of Energy

 

N=

% of Energy

          

Total Carbohydrate

Derbyshire (2009)

   

20

54 %

             

Giddens (2000)

      

59

50 %

          

Lee (2013)

   

133

51 %

 

156

52 %

          

Gutierrez (1999)

46

56 %

 

46

56 %

             

Total Fat

Chan (2006)

23

29 %

 

23

29 %

             

Gutierrez (1999)

46

29 %

 

46

27 %

             

Saturated Fat

Chan (2006)

23

9 %

 

23

10 %

             

Total Sugars

Derbyshire (2009)

   

20

25 %

             

Added Sugars

Lee (2013)

   

133

17 %

 

156

17 %

          

a Comparison to UK RNI 51 g/day and US RDA 71 g/day, b Comparison to UK RNI 18 g/day, c Comparison to US RDA 28 g/day, ↑ Study mean higher than reference value (p < 0.05), ↔ Study mean not different to reference value (p < 0.05), ↓ Study mean lower than reference value (p < 0.05)

Tables 5 and 6 show the pattern of micronutrient intakes across the included studies compared to UK and US Dietary Reference Values (DRVs).
Table 5

Intake of micronutrients in individual studies compared to UK and US dietary reference values - minerals

  

Comparison to UK Dietary Reference Value

Comparison to US Dietary Reference Value

Nutrient

Study

Second Trimester

Third Trimester

Mean over pregnancy

Second Trimester

Third Trimester

Mean over pregnancy

N=

Mean

Confidence Interval

N=

Mean

Confidence Interval

N=

Mean

Confidence Interval

N=

Mean

Confidence Interval

N=

Mean

Confidence Interval

N=

Mean

Confidence Interval

Calcium mg/day a

Baker (2009)

   

290

↔840

800, 880

      

290

↓840

800, 880

   

Chan (2006)

23

↔835

711, 959

23

↔862

714, 1010

   

23

↓835

711, 959

24

↓862

714, 1010

   

Derbyshire (2009)

   

20

↑1007

867, 1147

      

20

↓1007

867, 1147

   

Giddens (2000)

      

59

↑989

904, 1074

      

59

↓989

904, 1074

Gutierrez (1999)

46

↑1561

1334, 1789

46

↑1655

1424, 1886

   

46

↑1561

1334, 1789

46

↑1655

1424, 1886

   

Job (1995)

      

70

↔923

756, 1090

      

70

↓923

756, 1090

Lee (2013)

   

133

↑916

838, 995

156

↑886

824, 948

   

133

↓916

838, 995

156

↓886

824, 948

Pobocik (2003)

      

434

↓743

689, 797

      

434

↓743

689, 797

Phosphorous mg/day b

Chan (2006)

23

↑934

811, 1057

23

↑961

812, 1110

   

23

↓934

811, 1057

24

↓961

812, 1110

   

Giddens (2000)

      

59

↑1340

1248, 1432

      

59

↔1340

1248, 1432

Lee (2013)

   

133

↑1264

1182, 1347

156

↑1196

1131, 1261

   

133

↔1264

1182, 1347

156

↔1196

1131, 1261

Pobocik (2003)

      

434

↑1338

1279, 1397

      

434

↑1338

1279, 1397

Iron mg/day c

Baker (2009)

   

290

↑17

15, 19

      

290

↓17

15, 19

   

Castillo-Duran (2001) a

249

↑15.5

15, 16

249

↑16.8

16, 17

   

249

↓15.5

15, 16

249

↓16.8

16, 17

   

Castillo-Duran (2001) b

258

↑16.6

16, 17

258

↑16.8

16, 17

   

258

↓16.6

16, 17

258

↓16.8

16, 17

   

Chan (2006)

23

↑22

18, 26

23

↑25

20, 30

   

23

↓22

18, 26

23

↔25

20, 30

   

Derbyshire (2009)

   

20

↓12.6

11, 14

      

20

↔12.6

11, 14

   

Giddens (2000)

      

59

↔16

15, 17

      

59

↓16

15, 17

Gutierrez (1999)

46

↑17.7

15, 20

46

↑22.7

17, 28

   

46

↓17.7

15, 20

46

↔22.7

17, 28

   

Job (1995)

      

70

↓11.2

10, 12

      

70

↓11.2

10, 12

Lee (2013)

   

133

↑18.8

17, 20

156

↑18.6

17, 20

   

133

↓18.8

17, 20

156

↓18.6

17, 20

Pobocik (2003)

      

434

↑20

19, 21

      

434

↓20

19, 21

Magnesium mg/day d

Baker (2009)

   

290

↓236

227, 245

       

↓236

227, 245

   

Chan (2006)

23

↓263

230, 296

23

↓264

231, 297

    

↓263

230, 296

 

↓264

231, 297

   

Derbyshire (2009)

   

20

↓244

218, 270

       

↓244

218, 270

   

Giddens (2000)

      

59

↓252

234, 270

       

↓252

234, 270

Lee (2013)

   

133

↓237

222, 253

156

↓231

218, 244

    

↓237

222, 253

 

↓231

218, 244

Pobocik (2003)

      

434

↓270

258, 282

       

↓270

258, 282

Potassium mg/day e

Chan (2006)

23

↓2802

2512, 3092

23

↓2954

2635, 3273

   

23

↓2802

2512, 3092

23

↓2954

2635, 3273

   

Derbyshire (2009)

   

20

↓2948

2659, 3237

      

20

↓2948

2659, 3237

   

Zinc mg/day f

Baker (2009)

   

290

↑8.1

7.8, 8.4

      

290

↓8.1

7.8, 8.4

   

Castillo-Duran (2001) a

249

↑7.4

7.1, 7.7

249

↑7.7

7.4, 8

   

249

↓7.4

7.1, 7.7

249

↓7.7

7.4, 8

   

Castillo-Duran (2001) b

258

↑7.4

7.1, 7.7

258

↑7.4

7.2, 7.6

   

258

↓7.4

7.1, 7.7

258

↓7.4

7.2, 7.6

   

Chan (2006)

23

↑16

11.9, 20.1

23

↑18

13.5, 22.5

   

23

↔16

11.9, 20.1

23

↑18

13.5, 22.5

   

Derbyshire (2009)

   

20

↑8.1

7.4, 8.9

      

20

 

7.4, 8.9

   

Giddens (2000)

      

59

↑11.6

10.5, 12.7

      

59

↑11.6

10.5, 12.7

Gutierrez (1999)

46

↑14.5

12.6, 16.4

46

↑15.3

13.4, 17.2

   

46

↑14.5

12.6, 16.4

46

↑15.3

13.4, 17.2

   

Job (1995)

      

70

↑9.5

8.5, 10.5

      

70

↑9.5

8.5, 10.5

Lee (2013)

   

133

↑12.8

 

156

↑12.6

11.4, 13.8

   

133

↑12.8

 

156

↑12.6

11.4, 13.8

Pobocik (2003)

      

434

↑13

12.2, 13.8

      

434

↑13

12.2, 13.8

Sodium mg/day g

Chan (2006)

23

↑3316

2809, 3823

23

↑3323

2812, 3834

    

↑3316

2809, 3823

 

↑3323

2812, 3834

   

Derbyshire (2009)

   

20

↑3089

2722, 3456

       

↑3089

2722, 3456

   

Copper μg/day h

Giddens (2000)

      

59

↑1200

1098, 1302

      

59

↑1200

1098, 1302

Lee (2013)

   

133

↑1100

1015, 1185

156

↑1085

1021, 1151

   

133

↑1100

1015, 1185

156

↑1085

1021, 1151

Selenium μg/day i

Giddens (2000)

      

59

↑116

109, 123

      

59

↑116

109, 123

aComparison to UK RNI 800 mg/day and US RDA 1300 mg/day, bComparison to UK RNI 625 mg/day and US RDA 1250 mg/day, cComparison to UK RNI 14.8 mg/day and US RDA 27 mg/day, dComparison to UK RNI 300 mg/day and US RDA 400 mg/day, eComparison to UK RNI 3500 mg/day and US RDA 4700 mg/day, fComparison to UK RNI 7 mg/day and US RDA 12 mg/day, gComparison to UK RNI 1500 mg/day and US RDA 1600 mg/day, hComparison to UK RNI 1000 μg/day and US RDA 1000 μg/day, iComparison to UK RNI 60 μg/day and US RDA 60 μg/day, ↑ Study mean higher than reference value (p < 0.05), ↔ Study mean not different to reference value (p < 0.05), ↓ Study mean lower than reference value (p < 0.05)

Table 6

Intake of micronutrients in individual studies compared to UK and US dietary reference values - vitamins

  

Comparison to UK Dietary Reference Value

Comparison to US Dietary Reference Value

Nutrient

Study

Second Trimester

Third Trimester

Mean over pregnancy

Second Trimester

Third Trimester

Mean over pregnancy

N=

Mean

Confidence Interval

N=

Mean

Confidence Interval

N=

Mean

Confidence Interval

N=

Mean

Confidence Interval

N=

Mean

Confidence Interval

N=

Mean

Confidence Interval

Vitamin D μg/day a

Baker (2009)

   

290

↓2.1

2, 2.3

      

290

↓2.1

2, 2.3

   

Chan (2006)

23

↓2.8

1.9, 3.7

23

↓3.1

2.2, 4

   

23

↓2.8

1.9, 3.7

23

↓3.1

2.2, 4

   

Derbyshire (2009)

   

20

↓2.0

1.5, 2.6

      

20

↓2.0

1.5, 2.6

   

Giddens (2000)

      

59

↓6.4

5.7, 7.1

      

59

↓6.4

5.7, 7.1

Lee (2013)

   

133

↓5.4

4.7, 6.1

156

↓5.1

4.6, 5.6

   

133

↓5.4

4.7, 6.1

156

↓5.1

4.6, 5.6

Vitamin E b

Baker (2009)

            

290

↓8.9

8.3, 9.5

   

Derbyshire (2009)

            

20

↓7.7

6.5, 8.9

   

Gutierrez (1999)

         

46

↓10.7

10.7

46

↓11.2

8.2, 14.1

   

Lee (2013)

            

133

↓6.9

6.2, 7.6

156

↓6.9

6.4, 7.4

Pobocik (2003)

               

434

↓8

7.2, 8.8

Vitamin C c

Baker (2009)

   

290

↑160

146, 174

      

290

↑160

146, 174

   

Derbyshire (2009)

   

20

↑138

111, 165

      

20

↑138

111, 165

   

Giddens (2000)

      

59

↑128

112, 144

      

59

↑128

112, 144

Gutierrez (1999)

46

↑252

208, 296

46

↑231

190, 271

   

46

↑252

208, 296

46

↑231

190, 271

   

Job (1995)

      

70

↑135

92, 178

      

70

↑135

92, 178

Lee (2013)

   

133

↑97

81, 113

156

↑106

94, 118

   

133

↑97

81, 113

156

↑106

94, 118

Pobocik (2003)

      

434

↑167

150, 184

      

434

↑167

150, 184

Folate d

Baker (2009)

   

290

↔285

269, 301

      

290

↓285

269, 301

   

Derbyshire (2009)

   

20

↓227

205, 249

      

20

↓227

205, 249

   

Giddens (2000)

      

59

↔312

277, 347

      

59

↓312

277, 347

Gutierrez (1999)

46

↑447

355, 540

46

↑393

340, 445

   

46

↓447

355, 540

46

↓393

340, 445

   

Lee (2013)

   

133

↑829

723, 935

156

↑849

645, 1053

   

133

↑829

723, 935

156

↑849

645, 1053

Pobocik (2003)

      

434

↔292

269, 315

      

434

↓292

269, 315

Riboflavin e

Chan (2006)

23

↑2.3

1.8, 2.8

23

↑2.4

2, 2.8

   

23

↑2.3

1.8, 2.8

23

↑2.4

2, 2.8

   

Giddens (2000)

      

59

↑2.3

       

59

↑2.3

2.1, 2.5

Lee (2013)

   

133

↑2.5

2.3, 2.7

156

↑2.4

    

133

↑2.5

2.3, 2.7

156

↑2.4

2.2, 2.6

Pobocik (2003)

      

434

↑2.1

       

434

↑2.1

2, 2.2

B12 f

Baker (2009)

   

290

↑5.3

4.7, 5.9

      

290

↑5.3

4.7, 5.9

   

Chan (2006)

23

↑5

3.8, 6.2

23

↑5.2

3.7, 6.7

   

23

↑5

3.8, 6.2

23

↑5.2

3.7, 6.7

   

Giddens (2000)

      

59

↑5.3

4.6, 6

      

59

↑5.3

4.6, 6

Lee (2013)

   

133

↑5.6

5, 6.2

156

↑5.5

5, 6

   

133

↑5.6

5, 6.2

156

↑5.5

5, 6

Pobocik (2003)

      

434

↑5.5

4.8, 6.2

      

434

↑5.5

4.8, 6.2

Thiamin g

Baker (2009)

   

290

↑1.6

1.5, 1.7

      

290

↑1.6

1.5, 1.7

   

Giddens (2000)

      

59

↑2.1

1.9, 2.3

      

59

↑2.1

1.9, 2.3

Lee (2013)

   

133

↑2.1

1.9, 2.3

156

↑2.1

1.9, 2.3

   

133

↑2.1

1.9, 2.3

156

↑2.1

1.9, 2.3

Pobocik (2003)

      

434

2.4

2.3, 2.5

      

434

2.4

2.3, 2.5

Niacin h

Baker (2009)

   

290

↑33

32, 35

      

290

↑34

32, 35

   

Giddens (2000)

      

59

↑24

22, 26

      

59

↑24

22, 26

Lee (2013)

   

133

↑28

26, 30

156

↑26

24, 27

   

133

↑28

26, 30

156

↑26

24, 27

Pobocik (2003)

      

434

↑30

29, 31

      

434

↑30

29, 31

B6 i

Baker (2009)

   

290

↑2.3

2.1, 2.4

      

290

↑2.3

2.1, 2.4

   

Giddens (2000)

      

59

↑1.9

1.7, 2.1

      

59

↑1.9

1.7, 2.1

Lee (2013)

   

133

↑2.2

2, 2.4

156

↑2.1

1.9, 2.3

   

133

↑2.2

2, 2.4

156

↑2.1

1.9, 2.3

Pobocik (2003)

      

434

↑2

1.9, 2.1

      

434

↑2

1.9, 2.1

Vitamin A j

Baker (2009)

   

290

↑759

651, 867

      

290

↑759

651, 867

   

Derbyshire (2009)

   

20

↑555

439, 671

      

20

↓555

439, 671

   

Giddens (2000)

    

↑105

 

59

↑1053

907, 1199

    

↑1053

 

59

↑1053

907, 1199

Gutierrez (1999)

46

↑2492

1466, 3518

46

↑197

1432, 2523

   

46

↑2492

1466, 3518

46

↑1978

1432, 2523

   

Job (1995)

      

70

↑973

802, 1144

      

70

↑973

802, 1144

Lee (2013)

   

133

↑698

614, 783

156

↑666

615, 717

   

133

↑698

614, 783

156

↓666

615, 717

Pobocik (2003)

      

434

↑109

944, 1242

      

434

↑1093

944, 1242

Vitamin K k

Lee (2013)

            

133

↔70

57, 83

156

↔70

59, 81

a Comparison to UK RNI 10 μg/day and US RDA 15 μg/day, b Comparison to US RDA 15 mg/day, c Comparison to UK RNI 40 mg/day and US RDA 80 mg/day, d Comparison to UK RNI 200 μg/day and US RDA 600 μg/day, e Comparison to UK RNI 1.1 mg/day and US RDA 1.4 mg/day, f Comparison to UK RNI 1.5 μg/day and US RDA 2.6 μg/day, g Comparison to UK RNI 0.8 mg/day and US RDA 1.4 mg/day, h Comparison to UK RNI 14 mg/day and US RDA 18 mg/day, i Comparison to UK RNI 1.2 mg/day and US RDA 1.9 mg/day, j Comparison to UK RNI 600 μg/day and US RDA 750 μg/day, k Comparison to US AI 75 μg/day, ↑ Study mean higher than reference value (p < 0.05), ↔ Study mean not different to reference value (p < 0.05), ↓ Study mean lower than reference value (p < 0.05)

The individual study results show that the majority of reported nutrient intakes were significantly below both the UK RNI and US RDA for vitamin D, potassium and magnesium and below the US RDA for calcium, vitamin E, folate, phosphorous and iron. Zinc intakes reported as the mean intake over pregnancy were low whereas this was not the case in the studies reporting intakes in the second or third trimesters specifically.

Results of the pooled analyses however showed that only intake of vitamin D remained significantly below both the UK RNI and US RDA, and intakes of potassium below the US RDA. Sub-group analysis showed that micronutrient intake was lower in UK based studies than those based in the USA for all micronutrients with the exception of vitamin C, however vitamin D was the only micronutrient where the percentage of the DRV in UK based studies was below the UK RNI (21.4 %, CI 0–63.5 %) and US RDA (14.3 %, CI 0–42.3 %). Results of the pooled analysis of micronutrients are shown in Fig. 2. Detailed results of the sub-group analysis of nutrient intakes are available in Additional file 1: Table S2 and Additional file 1: Table S3.
Fig. 2

Pooled weighted mean micronutrient intake compared to UK and US dietary reference values

Micronutrient analysis by stage of pregnancy showed that intake of vitamin D in the second (28 % of the UK RNI, CI 26–30 %) and third (31.2 % of the UK RNI, CI 0–47 %) trimesters was below recommendations; this was not the case for measures reported as a mean over pregnancy (54 % of the UK RNI, CI 0–114.3 %). In the third trimester the percentage of the US RDA represented by intakes of magnesium (19.9 %, CI 20.4–98.6 %) and potassium (62.8 %, CI 32.5–93.1 %) were also below recommendations.

Biological markers

Table 7 shows the pattern of biological markers reported across the included studies compared to WHO, UK and US minimum thresholds for deficiency where available. As the recommended cut off points given by all three authorities are consistent, the results are presented in one combined table for clarity. Other nutrients were considered compared to deficiency thresholds suggested in the academic literature as previously discussed.
Table 7

Biological markers of nutritional status in individual studies compared to reference values

 

Study ID

First Trimester

Second Trimester

Third Trimester

Delivery

  

N=

Mean

Confidence Interval

N=

Mean

Confidence Interval

N=

Mean

Confidence Interval

N=

Mean

Confidence Interval

Haemoglobin (g/L) a

Baker (2009)

404

↑122

121, 123

   

362

↓108

107, 109

   

Chang (2003)

445

↑121

121, 122

319

↑112

112, 114

836

↓107

107, 109

   

Dawson (2000) a

   

21

↑124

123, 125

21

↑115

114, 116

20

↑114

111, 112

Dawson (2000) b

   

20

↑125

124, 126

20

↑119

118, 120

21

↑116

112, 114

Dawson (2000) a

      

21

↑114

113, 115

   

Dawson (2000) b

      

20

↑120

119, 121

   

Gadowsky (1995)

      

50

↑119

115, 123

   

Iannotti (2005)

   

35

↔111

107, 115

70

↔107

104, 110

   

McGuire Davies (2010)

   

78

↑118

118, 118

76

↓107

107, 108

   

Meier (2002) a

   

20

↑125

122, 129

15

↑123

119, 128

   

Meier (2002) b

   

17

↑128

124, 132

16

↑117

112, 123

   

Meier (2002) a

   

19

↑116

112, 120

      

Meier (2002) b

   

16

↑113

110, 116

      

Rycel (2009)

         

102

↑120

120, 229

Rycel (2009)

         

102

↓103

103, 103

Young (2010)

   

48

↑113

    

62

↑117

113, 121

Ferritin (μg/L or ng/ml) b

Gadowsky (1995)

   

50

↓7.4

5.7, 9.1

      

Iannotti (2005)

   

44

↑33

26.8, 40.6

59

↔15

12.6, 17.8

   

Meier (2002) a

   

19

↑42

31.3, 52.8

15

↔25

14.6, 35.4

   

Meier (2002) b

   

17

↑57

36.5, 77.5

15

↓6.8

5.2, 8.5

   

Meier (2002) a

   

19

↑46

24, 68.8

      

Meier (2002) b

   

16

↓10

7.9, 13

      

Young (2010)

   

81

↔16

12.9, 20.1

   

88

↔17

14.9, 20.3

Haematocrit (g/L) c

Chang (2003)

445

↑36

35.7, 36.3

319

↔33

32.7, 33.3

836

↓32

31.8, 32.2

   

Gadowsky (1995)

      

50

↑36

34.8, 37.2

   

Iannotti (2005)

   

35

↔33

32, 34

70

↓32

31.3, 32.7

   

Rycel (2009)

         

102

34

34.6, 34.8

Rycel (2009)

         

102

↓31

31.4, 31.6

Zinc μmol/L-1 d

Castillo-Duran (2001) a

249

↑11.9

11.7, 12.1

   

249

↑10.9

10.7, 11.1

   

Castillo-Duran (2001) b

258

↑11.7

11.5, 11.9

   

258

↑10.9

10.7, 11.1

   

Castillo-Duran (2001) a

      

249

↑10.5

10.3, 10.7

   

Castillo-Duran (2001) b

      

258

↑10.2

10, 10.4

   

Chan (2006)

         

23

↑26.3

23.2, 29.4

Mistry (2014) a

      

107

↑9.71

8.8, 10.5

   

Mistry (2014) b

      

19

↑10.8

7.8, 13.9

   

Magnesium mmol/l e

Chan (2006)

         

23

↑0.99

0.9, 1.1

Phosphorous mg/dl f

Chan (2006)

         

23

↑5

4, 6

Copper μg/dl g

Mistry (2014) a

      

107

↑206

1991, 2128

   

Mistry (2014) b

      

19

↑196

1712, 2207

   

Selenium μg/L h

Dawson (2000) a

   

21

↓49

46, 52

21

↓55

52.9, 57.1

21

↑114

108.9, 119.1

Dawson (2000) b

   

20

↓44

39.6, 48.4

20

↓53

50.8, 55.2

20

↓55

50.2, 59.8

Dawson (2000) a

   

21

↓50

46.2, 53.8

21

↔85

76.9, 93.1

   

Dawson (2000) b

   

20

↓44

39.6, 48.4

20

↓62

57.2, 66.8

   

Mistry (2014) a

      

107

↓65

62.7, 67.5

   

Mistry (2014) b

      

19

↓49

45.9, 52.9

   

Red blood cell folate (nmol/l) i

Baker (2009)

      

266

↑647

616, 680

   

Serum folate (nmol/l) j

Baker (2009)

      

291

↑12

12, 14

   

Chan (2006)

         

23

↔13

10, 17

Vitamin A (μg/dL)

Chan (2006)

         

23

↑38

31, 45

B12 (pmol/l) k

Baker (2009)

      

293

↑177

169, 185

   

Chan (2006)

         

23

↑265

216, 315

Gadowsky (1995)

      

50

↑170

146, 194

   

Homocysteine (μmol/L) l

Baker (2009)

      

293

7.9

7.6, 8.2

   

Gadowsky (1995)

      

50

6.1

3, 9

   

25OHD (nmol/L) m

Baker (2009)

      

263

↑33

30.4, 35.8

   

Chan (2006)

         

23

↑57

48, 67

Ginde (2010)

            

McGuire Davies (2010)

   

44

↑52

46, 58

36

↑56

50, 63

   

O’Brien (2003)

      

23

↑50

41, 60

   

Young (2012)

         

171

↑54

51, 59

a Target value 110 g/L, b Target value 15 μg/L, c Target value33 g/L, d Target value 6.12 μmol/L-1, e Target value 0.9 mmol/L, f Target value 2.5 mg/dl, g Target value 63.7 μg/dl, h Target value 90 μg/L, i Target value 340 nmol/L, j Target value 20 μg/dl, k Target value 150pmol/L, l Target value less than 13 μmol/L, m Target value 25 nmol/L, ↑ Study mean higher than reference value (p < 0.05), ↔ Study mean not different to reference value (p < 0.05), ↓ Study mean lower than reference value (p < 0.05)

The results show that the mean reported biomarker values in the majority of studies suggested that young women’s nutritional status was sufficient, with the exception of markers of iron and selenium status. Results for haematocrit and plasma ferritin were mixed, with results being more likely to be below the cut off in the third trimester and at delivery. Measures of serum selenium were reported to be less than the cut off in the majority of studies.

Examination of pooled, weighted means showed that only mean selenium concentration was below the reference value. The weighted means for all biological markers where there were two or more valid results are shown in Table 8.
Table 8

Pooled weighted means of biological markers

Biological Marker

Pooled Mean

Confidence Interval

Target Value

Number of studies

Haemoglobin (g/dL)

112.4

95.4–133.8

110

9

25_OH_D (nmol/L)

55.9

6.2–105.7

25

6

Ferritin (μg/L)

18.2

0–48.3

15

4

Haematocrit (g/L)

32.5

28.0–39.4

33

4

Zinc (μmol/L-1)

11.5

5.9–17.1

6.12

3

B12 (pmol/L)

181.6

0–271.1

150

3

Serum Folate (nmol/L)

12.8

0–26.8

10

2

Selenium (μg/L)

61.8*

39.2–84.4

90

2

Homocystine (μmol/L)

7.6

0–17.0

Less than 13

2

* Significant at the p<0.005 level

The sub-group analysis by country of origin was only possible by US vs. non-US studies as there was only one UK based study reporting biological markers. The analysis failed to detect any differences by study country of origin. Analysis by stage of pregnancy suggests a decline in iron status markers haemoglobin, haematocrit and ferritin as pregnancy progresses; the levels observed however do not necessarily reflect iron deficiency. Detailed results of the sub-group analysis of biological markers are available in Additional file 1: Table S4 and Additional file 1: Table S5.

Discussion

Compared with reviews of the nutritional status of pregnant adolescents published in 2007, this review identified a further 13 studies that reported data on nutritional intakes and biomarkers of status. The summary results show that there may be areas of concern in adolescent’s nutritional intake during pregnancy, particularly compared to US recommendations, with regard to calcium, vitamin D, vitamin E, folate, potassium and magnesium. The evidence also suggests that overall energy intake may be lower than recommended.

In terms of comparison with dietary reference values, combined analysis of the individual study means showed very few statistically significant results, with the exception of vitamin D. One possible explanation for this is that there was a high level of variance between participants in the majority of studies resulting in very wide confidence intervals. This suggests that there may be sub-groups of young women within the total population who are at higher risk of poor nutritional status which this review has failed to detect. Differences in micronutrient intake were observed between UK and USA based studies which may in part be explained by routine fortification of food products in the USA compared to the UK. Only one study reported that supplements were included in the reported intake values, and the compliance rates for supplements in this study were low, meaning that the impact of supplement use on intakes data is marginal.

Macronutrient contributions to energy were found to be roughly in line with recommendations, however there was a significant lack of data for carbohydrates (including sugars and fibre) and fats (including saturated fat) meaning these results should be interpreted with caution. Further research into macronutrient intakes in this population, particularly with regard to types of carbohydrates and fats, is needed.

The methods used to assess dietary intake varied across the included studies. The two methods reported by the included studies were 24 h dietary recalls (single and multiple) and food diaries. While these are validated and accepted methods of nutritional surveillance [45], it is acknowledged that underreporting biases may exist [46] and so results should be considered with this in mind.

Four of the studies reporting energy intake also reported mean gestational weight gain which ranged from 14 kg to 17 kg, consistently higher than the required pregnancy weight gain [47]. Mean percentage intake of the EAR for energy was higher in the studies reporting weight gain than those which did not report this measure, but not significantly so. This is potentially contradictory of the finding that energy intake was low in individual studies and suggests further work is needed regarding the potential level of under reporting in this population and the relationship between dietary patterns, overall energy consumption and gestational weight gain.

Inadequacies in nutrient intakes did not necessarily translate to systemic deficiencies as measured by mean values of biological markers, with the possible exceptions of markers of iron and selenium status. One possible explanation for this is that food intake may have been under reported therefore suggesting that intake was insufficient when this was not the case. A further possible explanation is that measures of biological markers were elevated by dietary supplements. Details regarding the type, dose, duration and number of participants taking supplements were inconsistent in the included papers meaning that detailed analysis of the impact of supplement use on nutritional status was not possible, however 10 out of the 15 included studies reporting biomarkers did report some level of supplementation. This finding does suggest that supplements may play an important role in ensuring young women do not experience nutrient insufficiency, however attention to clear reporting of supplement use in research papers is essential to allow a better understanding of the impact of supplementation on nutritional status.

The participants in all of the included studies where supplements were provided may also have been more compliant with taking supplements due to the very fact that they were taking part in a research study than might be expected outside of a study environment. A systematic review [48] of the effect of dietary interventions in adolescent pregnancies found some evidence to suggest that nutritional supplements may reduce the likelihood of low birth weight; however the review also reported a serious lack of good quality research papers in this area. Further work to establish the extent to which pregnant young women in the general population suffer more from nutrient deficiencies and the impact of supplement use would be advantageous.

There is significant evidence in the literature regarding the role of nutrition in supporting healthy pregnancies and allowing the foetus to achieve its full potential. Adolescent girls are at particular risk of iron deficiency anaemia due in part to rapid growth during adolescence [49] combined with the onset of menarche. This coupled with the increased demand for iron in pregnancy for expansion of maternal tissues and foetal growth, makes pregnant adolescents a particularly vulnerable group. There is some evidence to suggest that iron deficiency is implicated in the risk of adverse birth outcomes such as prematurity and low birth weight [50], meaning this is potentially an important factor in improving maternal and infant health. While analysis of mean values for markers of iron deficiency in this review did not indicate a significant issue, consideration of the reported prevalence of iron deficiency anaemia in the included studies suggests that this may be a concern for this population.

Vitamin D and calcium have an essential role in the mineralization of the developing foetal skeleton and insufficient intake of these nutrients may impact on foetal bone growth. The interaction between these two nutrients has been shown to be key to maximising foetal bone growth in pregnant adolescents and that growth is adversely affected when either of the two nutrients were lacking [30]. The pooled mean for vitamin D status as reflected in blood 25 (OH)D in this review was significantly below recommended levels across all trimesters. It was not possible to conduct analysis of vitamin D status by ethnicity or exposure to sunlight, however, which are factors known to have a significant impact on vitamin D status [5153].

The role of folate in the prevention of neural tube defects in early pregnancy has been well documented [54]. There is a lack of data collected in early pregnancy in the papers included in the current review, however the observed failure to meet recommendations for folate intake in later pregnancy reported may suggest that the participants were unlikely to have been meeting recommendations prior to taking part in a research study. A systematic review of the impact of folate intake over the course of pregnancy [55] also found a significant effect in the second and third trimesters on infant birth weight, suggesting that the importance of folate for a healthy pregnancy extends beyond the first trimester.

Selenium status has been identified as a potential area of concern in this review. Selenium is a trace element which has an anti-oxidative effect and protects cell membranes [56]. The target value used to assess selenium status was based on the intake necessary for maximisation of plasma glutathione peroxidase activity, which is the criteria used in the derivation of the US RDA [18]. Selenium status has been shown to be associated with a number of adverse outcomes for both mother and child including neural tube defects [57], lower birth weights [58], cholestasis [59] and gestational diabetes [60].

While demographic characteristics of participants were reported in the included studies data was generally reported for the study population as a whole, meaning that sub-group analysis was not possible. This is significant in that evidence suggests that younger adolescents, those who smoke and those from more deprived backgrounds may be at higher risk of nutritional issues [3, 61, 62].

There is also evidence to suggest that the nutritional status of adult pregnant women may raise similar concerns to those identified within this review. A systematic review of micronutrient intakes in pregnancy found that intakes of folate, vitamin D and iron were sub-optimal [63]. A further review focusing on energy and macronutrient intake in this population found that intakes of energy and fibre were also below recommendations [64]. These results are consistent with the findings of this review suggesting that maternal age alone may not be the most important factor in sub-optimal nutritional status during pregnancy. Further work to identify the characteristics of those most at risk, particularly within the adolescent population, and the nature of that risk is needed.

Limitations

There were some significant limitations which impact on the conclusions of this review. The majority of the included papers used convenience samples meaning that there is likely to be an element of bias in the reported outcomes. The majority of participants in the included studies were aged 16 and over meaning that the results may not be generalisable to younger adolescents, who may also be at greater nutritional risk compared to older adolescents due to competing growth needs [3]. The lack of detail regarding participant’s supplement use meant that it was not possible to evaluate the impact of supplements on biological markers of nutritional status. It is therefore likely that these results may have been biased by supplement use in some participants.

There was significant heterogeneity in the included papers in terms of study design. Measurements of dietary intake differed between papers however the majority of studies used 24 h recall methods to assess nutrient intake. This has been shown to have limitations in terms of both participants reporting their intake accurately and the likelihood that the recorded intake is representative of the usual diet, particularly in adolescents [46]. Three studies used multiple 24 h recalls in order to produce more reliable estimates of intakes; however this approach was not consistent across the included studies using this method.

There were also considerable differences in the number of nutritional indicators represented. Pooled means were calculated wherever two or more data points were available in order to maximise the results available from the review. This however means that some estimates will be more robust than others depending on the number of data points on which they are based. There was a large degree of variation in the amount of data available for different nutrients, for example assessment of serum selenium was based on data from only two papers whereas nine independent studies contributed data on haemoglobin concentration.

The pooling of study means gives a useful indication of potential inadequacies across the population as a whole; however this approach lacks the sensitivity to draw conclusions regarding the prevalence of nutrient deficiencies in the population. Examination of the reported prevalence of deficiency in the included studies shows results which are inconsistent with the analysis based on study means. The prevalence of iron deficiency anaemia measured by haemoglobin concentration reportedly ranged from 1.2 to 63.5 %, with prevalence in the third trimester ranging from 29 to 63.5 %. Other markers of iron status followed a similar pattern with higher prevalence of deficiency occurring in the third trimester. The prevalence of vitamin D deficiency in many of these studies was also higher than suggested by the analysis of study means. This suggests, similarly to the data regarding nutrient intakes, that there are substantial skews within the data and sub-groups of young women who may be more at risk of deficiencies.

Conclusion

This review identifies some concerns in the nutritional status of pregnant adolescents which may impact on maternal and infant outcomes. Intake of vitamin D and serum selenium status were identified as being significantly low in pooled analysis of included studies. Fibre intake was also below recommendations.. This said there are some significant limitations meaning these results should be interpreted with caution. No analysis of the effect of demographic characteristics on either nutritional intake or biological markers was possible, nor was it possible to examine the impact of supplement use on biological markers.

Patterns in this population are also similar to those reported in the adult population during pregnancy. These findings suggest that targeted work to identify those most at risk, and the nature of that risk, is needed. Recommendations for other areas of further research include the macronutrient composition of adolescent’s diet during pregnancy, the relationship between nutrient intakes and birth outcomes and the role of nutritional supplements in this population.

Abbreviations

CASP: 

Critical appraisal and skills program

DRV: 

Dietary reference value

EAR: 

Estimated average requirement

RDA: 

Recommended daily allowance

RNI: 

Reference nutrient intake

WHO: 

World Health Organisation

Declarations

Acknowledgments

The authors would like to thank Dr Karen Kilner for her assistance with the statistical methods used in this review.

We would also like to thank the National Institute for Health Research Collaboration for Leadership in Applied Health Research and Care for Yorkshire and Humber (NIHR CLAHRC YH) for supporting us in conducing this review. Further details about the new NIHR CLAHRC YH can be found at www.clahrc-yh.nihr.ac.uk. The views and opinions expressed are those of the authors, and not necessarily those of the NHS, the NIHR or the Department of Health.

Funding

This review has been carried out as part of a PhD project supported by Sheffield Hallam University and the National Institute for Health Research Collaboration for Leadership in Applied Health Research and Care for Yorkshire and Humber. Therefore no additional funding was required for this work.

Availability of data and materials

All data on which the paper is based has been made available in either the main tables or Additional file 1: Tables S1-S5.

Authors’ contributions

KM-D Primary responsibility for development of research question and study design, extraction and analysis of data and writing the main body of the article. VB Advisory role in development of research question and study design, revisions to and approval of final article. HS Advisory role in development of research question and study design, cross-checking of all extracted data, revisions to and approval of final article. All authors read and approved the final manuscript.

Competing interests

The authors declare that they have no competing interests.

Consent for publication

Not applicable.

Ethics approval and consent to participate

Ethical approval was not required for this systematic review due to only studies previously published in the academic literature being eligible for inclusion.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Centre for Health and Social Care Research, Sheffield Hallam University
(2)
School of Food Sciences and Nutrition, University of Leeds

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