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Antenatal dietary advice and supplementation to increase energy and protein intake

  1. Erika Ota1,*,
  2. Ruoyan Tobe-Gai2,
  3. Rintaro Mori3,
  4. Diane Farrar4

Editorial Group: Cochrane Pregnancy and Childbirth Group

Published Online: 12 SEP 2012

Assessed as up-to-date: 22 DEC 2011

DOI: 10.1002/14651858.CD000032.pub2


How to Cite

Ota E, Tobe-Gai R, Mori R, Farrar D. Antenatal dietary advice and supplementation to increase energy and protein intake. Cochrane Database of Systematic Reviews 2012, Issue 9. Art. No.: CD000032. DOI: 10.1002/14651858.CD000032.pub2.

Author Information

  1. 1

    Graduate School of Medicine, The University of Tokyo, Department of Global Health Policy, Tokyo, Japan

  2. 2

    School of Public Health, Shandong University, Jinan, China

  3. 3

    National Center for Child Health and Development, Department of Health Policy, Tokyo, Tokyo, Japan

  4. 4

    Bradford Institute for Health Research, Maternal and Child Health, Bradford, UK

*Erika Ota, Department of Global Health Policy, Graduate School of Medicine, The University of Tokyo, 7-3-1 Hongo Bunkyo-ku, Tokyo, 113-0011, Japan. e-i@umin.ac.jp.

Publication History

  1. Publication Status: New search for studies and content updated (conclusions changed)
  2. Published Online: 12 SEP 2012

SEARCH

 

Summary of findings    [Explanations]

  1. Top of page
  2. Summary of findings    [Explanations]
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Appendices
  12. What's new
  13. History
  14. Contributions of authors
  15. Declarations of interest
  16. Sources of support
  17. Differences between protocol and review
  18. Index terms

 
Summary of findings for the main comparison. Nutritional advice compared to no counselling or advice during pregnancy for perinatal outcomes

Nutritional advice compared to no counselling or advice during pregnancy for perinatal outcomes

Patient or population: Pregnant women
Settings:
Intervention: Nutritional advice during pregnancy

OutcomesIllustrative comparative risks* (95% CI)Relative effect
(95% CI)
No of Participants
(studies)
Quality of the evidence
(GRADE)
Comments

Assumed riskCorresponding risk

ControlNutritional advice during pregnancy

StillbirthStudy populationRR 0.37
(0.07 to 1.9)
431
(1 study)
⊕⊕⊝⊝
low1,2

24 per 10009 per 1000
(2 to 46)

Moderate

24 per 10009 per 1000
(2 to 46)

Neonatal deathStudy populationRR 1.28
(0.35 to 4.72)
448
(1 study)
⊕⊕⊝⊝
low1,2

18 per 100023 per 1000
(6 to 83)

Moderate

18 per 100023 per 1000
(6 to 85)

Birthweight (g)The mean birthweight (g) in the intervention groups was
205.75 higher
(242.54 lower to 654.03 higher)
426
(2 studies)
⊕⊝⊝⊝
very low1,2,3

Birth head circumference (cm)The mean birth head circumference (cm) in the intervention groups was
0.99 higher
(0.43 to 1.55 higher)
389
(1 study)
⊕⊕⊕⊝
moderate2

Small-for-gestational ageStudy populationRR 0.97
(0.45 to 2.11)
404
(1 study)
⊕⊕⊝⊝
low1,2

60 per 100058 per 1000
(27 to 127)

Moderate

60 per 100058 per 1000
(27 to 127)

Preterm birthStudy populationRR 0.46
(0.21 to 0.98)
449
(2 studies)
⊕⊕⊝⊝
low2,3

85 per 100039 per 1000
(18 to 84)

Moderate

92 per 100042 per 1000
(19 to 90)

Protein intake (g/day)The mean protein intake (g/day) in the intervention groups was
6.99 higher
(3.02 to 10.97 higher)
632
(3 studies)
⊕⊕⊝⊝
low2,4

*The basis for the assumed risk (e.g. the median control group risk across studies) is provided in footnotes. The corresponding risk (and its 95% confidence interval) is based on the assumed risk in the comparison group and the relative effect of the intervention (and its 95% CI).
CI: Confidence interval; RR: Risk ratio;

GRADE Working Group grades of evidence
High quality: Further research is very unlikely to change our confidence in the estimate of effect.
Moderate quality: Further research is likely to have an important impact on our confidence in the estimate of effect and may change the estimate.
Low quality: Further research is very likely to have an important impact on our confidence in the estimate of effect and is likely to change the estimate.
Very low quality: We are very uncertain about the estimate.

 1 Wide 95% CI.
2 Sample size is smaller than optimal information size.
3 Allocation concealment, blinding, incomplete outcome reporting is high risk of bias in one study.
4 Random sequence, allocation concealment is unclear in some studies.

 Summary of findings 2 Balanced protein and energy supplementation compared to control or no intervention in pregnancy for perinatal and maternal outcomes

 Summary of findings 3 High protein supplementation in pregnancy and perinatal outcomes

 Summary of findings 4 Isocaloric balanced protein supplementation in pregnancy and outcomes

 

Background

  1. Top of page
  2. Summary of findings    [Explanations]
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Appendices
  12. What's new
  13. History
  14. Contributions of authors
  15. Declarations of interest
  16. Sources of support
  17. Differences between protocol and review
  18. Index terms
 

Description of the condition

Pregnancy requires an increased intake of macronutrient and micronutrients for maternal and fetal needs, and malnourishment or inadequate dietary intake during pregnancy can lead to adverse perinatal outcomes. Observational studies (IOM 1990; Kramer 1987; Rush 2001) have indicated that both gestational weight gain and energy intake are strongly and positively associated with fetal growth, and possibly associated with a reduced risk of preterm birth. Moreover, these associations are stronger in undernourished women, i.e. those with low pre-pregnancy body mass index (BMI) (Ota 2011). Fetal development complications, such as low birthweight (LBW) and infants born small-for-gestational age, are associated with increases in perinatal mortality and morbidities (Ashworth 1998; Kramer 1987). Globally, it is estimated that more than approximately 20 million low birthweight infants are born each year, and more than 95% of these babies are born in developing countries (Unicef-WHO 2004). The effects of poor maternal nutrition on both immediate birth outcomes and longer term health has been well described in many epidemiological studies, including the effects from the Dutch winter famine of 1944 to 1945 (Stein 1975). Recognised longer-term health risks associated with poor infant growth include type 2 diabetes, hypertension, cardiovascular disease and obesity (Barker 1998; Barker 2002; Eriksson 2001).

 

Description of the interventions and how the interventions might work

Undernourished maternal nutritional status at conception and inadequate maternal nutritional status during pregnancy can result adverse perinatal outcomes (Viswanathan 2008). Dietary advice to pregnant women and balanced protein energy supplementation aim to achieve appropriate energy intakes lead to increase in maternal weight gain during pregnancy and fetal growth (de Onis 1998; Kulier 1998; Viller 1998). Protein generally comprises about 10% to 15% of dietary energy (Garlick 2000). Balanced protein energy supplementation (i.e. supplements in which protein provides less than 25% of the total energy content) has been shown to have significant positive impacts on maternal and perinatal birth outcomes, such as reductions in the incidences of preterm birth (Viller 1998), stillbirth (Imdad 2011) and intrauterine growth restriction (de Onis 1998). Furthermore, non-randomised trials have reported beneficial effects on fetal growth (Lechtig 1975; Prentice 1983), although the evidence from properly randomised trials suggests more modest benefits (Rush 1989; Rush 2001). On the other hand, data from severe dietary carbohydrate restriction with very high animal protein intake was counselled as part of routine antenatal care in a moderately affluent area suggest that high-protein dietary supplementation may have depressed birthweight by 400 g or more (Grieve 1979: Rush 1989). Isocaloric protein supplementation denotes a supplement, in which the protein content is 'balanced', i.e. provides less than 25% of its total energy content, but the protein replaced an equal quantity of non-protein energy in the control group. The observational findings reported for a non-randomised trial in Guatemala (Lechtig 1975) also suggest that protein supplementation is unlikely to benefit pregnant women or their infants.

 

Why it is important to do this review

Reliable high-quality information is required about the benefits and harms of energy/protein supplementation during pregnancy both for the woman and her infant. This review updates the review by one additional trial (Huybregts 2009), in order to aid clinical decisions and health policy-making.

 

Objectives

  1. Top of page
  2. Summary of findings    [Explanations]
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Appendices
  12. What's new
  13. History
  14. Contributions of authors
  15. Declarations of interest
  16. Sources of support
  17. Differences between protocol and review
  18. Index terms

To assess the benefits and harms of dietary advice, supplementation or restriction on health outcomes for women and their infants. More specifically, the purpose of this review was to evaluate the five items listed below.

  1. Effects of advising pregnant women to increase their energy and protein intakes on gestational weight gain and outcomes of pregnancy, including fetal growth, gestational duration, and maternal and fetal/infant morbidity and mortality.
  2. Effects of balanced energy and protein supplements during pregnancy on gestational weight gain and outcomes of pregnancy.
  3. Effects of high-protein nutritional supplements during pregnancy on gestational weight gain and outcomes of pregnancy.
  4. Effects of isocaloric protein supplements (i.e. where the protein replaces an equal quantity of non-protein energy) during pregnancy on gestational weight gain and outcomes of pregnancy.

 

Methods

  1. Top of page
  2. Summary of findings    [Explanations]
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Appendices
  12. What's new
  13. History
  14. Contributions of authors
  15. Declarations of interest
  16. Sources of support
  17. Differences between protocol and review
  18. Index terms
 

Criteria for considering studies for this review

 

Types of studies

We included all randomised controlled trials with randomisation at either individual or cluster level. We did not include quasi-randomised trials or cross-over trials.

For assessing dietary advice to increase energy and protein intakes: randomised controlled trials of such advice, whether administered on a one-to-one basis or to groups of women.

For assessing dietary supplementation: randomised controlled trials of energy and protein supplementation, with or without placebo.

 

Types of participants

All pregnant women with no systematic illness.

 

Types of interventions

Specific advice to increase dietary energy and protein intakes, energy and protein supplementation. The types of supplements included those that were 'balanced' energy and protein supplements (i.e. an energy supplement in which less than 25% of the energy is from protein), high-protein supplements (i.e. an energy supplement in which more than 25% of the energy is from protein), and isocaloric protein supplements (i.e. a supplement in which the protein content is 'balanced', i.e. provides less than 25% of total energy content, but the protein replaced an equal quantity of non-protein energy in the control group).

 

Types of outcome measures

 

Primary outcomes

  • Perinatal mortality (defined by trialists)
  • Stillbirth (death after 20 weeks' gestation and before birth)
  • Neonatal death (death of a live infant within the first 28 days of life)

 

Secondary outcomes

 
Maternal outcomes

  • Pre-eclampsia (defined by trialists)
  • Energy intake (kcal/day)
  • Protein intake (g/day)
  • Gestational weight gain (kg)
  • Duration of labour (hours)
  • Mode of birth
  • Number of antenatal hospital admissions
  • Exclusive breast feeding at six months (defined by trialists)

 
Fetal/infant outcomes

  • Birthweight (g)
  • Small-for-gestational weight (defined by trialists)
  • Low birthweight (less than 2500 g)
  • Macrosomia (birthweight > 4 kg and birth injury
  • Birth length (cm)
  • Birth head circumference (cm)
  • Neurological development
  • Preterm birth (prior to 37 weeks' gestation) 
  • Respiratory distress syndrome
  • Admission to neonatal intensive care unit
  • Chronic lung disease 
  • Periventricular leukomalacia
  • Intraventricular haemorrhage
  • Necrotising enterocolitis
  • Retinopathy of prematurity
  • Child growth (weight, height, head circumference, BMI)

 
Child outcomes

  • Child growth (weight, height, head circumference, BMI)
  • Neurological development

 

Search methods for identification of studies

 

Electronic searches

We searched the Cochrane Pregnancy and Childbirth Group's Trials Register by contacting the Trials Search Co-ordinator (22 July 2011). We updated this search on 12 July 2012 and added the results to Studies awaiting classification.

The Cochrane Pregnancy and Childbirth Group’s Trials Register is maintained by the Trials Search Co-ordinator and contains trials identified from: 

  1. quarterly searches of the Cochrane Central Register of Controlled Trials (CENTRAL);
  2. weekly searches of MEDLINE;
  3. weekly searches of EMBASE;
  4. handsearches of 30 journals and the proceedings of major conferences;
  5. weekly current awareness alerts for a further 44 journals plus monthly BioMed Central email alerts.

Details of the search strategies for CENTRAL, MEDLINE and EMBASE, the list of handsearched journals and conference proceedings, and the list of journals reviewed via the current awareness service can be found in the ‘Specialized Register’ section within the editorial information about the Cochrane Pregnancy and Childbirth Group

Trials identified through the searching activities described above are each assigned to a review topic (or topics). The Trials Search Co-ordinator searches the register for each review using the topic list rather than keywords.  

 

Searching other resources

We contacted authors for additional data.

We did not apply any language restrictions.

 

Data collection and analysis

For the methods used when assessing the trials identified in the previous version of this review, see Appendix 1.

For this update, we used the following methods when assessing the trials identified by the updated search.

 

Selection of studies

Review authors Erika Ota (EO) and Ruoyan Tobe-Gai (RT) independently assessed all the potential studies we identified as a result of the updated search strategy for inclusion and resolved any disagreements through discussion or, if required, through consultation with Rintaro Mori (RM).

 

Data extraction and management

For eligible studies, EO and RT extracted the data independently and entered them into Review Manager software (RevMan 2011). We resolved any discrepancies through discussion or, if required, through consultation with RM. Data were checked for accuracy.

When information regarding any of the above was unclear, we attempted to contact the authors of the original reports to provide further details.

 

Assessment of risk of bias in included studies

Two review authors (EO and RT) independently assessed risk of bias for the one new study included in this update ( Huybregts 2009) using the criteria outlined in the Cochrane Handbook for Systematic Reviews of Interventions (Higgins 2011). We resolved discrepancies through discussion.

EO, RM and RT independently re-assessed the risk of bias for additional columns newly required for all the studies already included in the previous version with respect to changes in the methods (Higgins 2011).

 

(1) Sequence generation (checking for possible selection bias

For each included study, we described the method used to generate the allocation sequence in sufficient detail to allow an assessment of whether it should produce comparable groups.

We assessed the methods as indicated below:

  • low risk of bias: any truly random process (e.g. random number table; computer random number generator);
  • high risk of bias: any non-random process (e.g. odd or even date of birth; hospital or clinic record number);
  • unclear risk of bias.   

 

 (2) Allocation concealment (checking for possible selection bias)

For each included study, we described the method used to conceal the allocation sequence in sufficient detail and determined whether the intervention allocation could have been foreseen in advance of or during recruitment, or changed after assignment.

We assessed the methods as indicated below:

  • low risk of bias (e.g. telephone or central randomisation; consecutively numbered sealed opaque envelopes);
  • high risk of bias (e.g. open random allocation; unsealed or non-opaque envelopes, alternation; date of birth);
  • unclear risk of bias. 

 

(3) Blinding of participants, personnel and outcome assessment (checking for possible performance bias and detection bias)

For each included study, we described the methods used to blind study participants and personnel from knowledge of which intervention a participant received. Studies were judged at low risk of bias if they were blinded, or if we judged that the lack of blinding could not have affected the results. Blinding was assessed separately for different outcomes or classes of outcomes.

We assessed the methods as indicated below:

  • low, high or unclear risk of bias for participants;
  • low, high or unclear risk of bias for personnel;
  • low, high or unclear risk of bias for outcome assessment.

 

(4) Incomplete outcome data (checking for possible attrition bias through withdrawals, dropouts, protocol deviations)

For each included study, and each outcome or class of outcomes, we described the completeness of the data including attrition and exclusions from the analysis. We stated whether attrition and exclusions were reported, the numbers included in the analysis at each stage (compared with the total randomised participants), reasons for attrition or exclusion where reported, and whether missing data were balanced across groups or were related to outcomes. Where sufficient information was reported or supplied by the trial authors, we re-included missing data in the analyses that we undertook.

We assessed methods as indicated below:

  • low risk of bias (e.g. no missing outcome data; missing outcome data balanced across groups);
  • high risk of bias (e.g. numbers or reasons for missing data imbalanced across groups; 'as treated' analysis done with substantial departure of intervention received from that assigned at randomisation);
  • unclear risk of bias.

 

(5) Selective reporting bias

For each included study, we described how we investigated the possibility of selective outcome reporting bias and what we found.

We assessed the methods as indicated below:

  • low risk of bias (where it was clear that all of the study's pre-specified outcomes and all expected outcomes of interest to the review had been reported);
  • high risk of bias (where not all of the study's pre-specified outcomes have been reported; one or more reported primary outcomes were not pre-specified; outcomes of interest were reported incompletely and could not be used; study failed to include results of a key outcome that would have been expected to have been reported);
  • unclear risk of bias.

 

(6) Other bias (checking for bias caused by problems not covered by section (1) to (5) above)

For each included study, we described any important concerns we have about other possible sources of bias.

We assessed whether each study was free of other problems that could put it at risk of bias as indicated below:

  • low risk of other bias;
  • high risk of other bias;
  • unclear risk of other bias.

 

(7) Overall risk of bias

We made explicit judgements about whether studies were at high risk of bias, according to the criteria given in the Cochrane Handbook for Systematic Reviews of Interventions (Higgins 2011). With reference to points (1) to (6) above, we assessed the likely magnitude and direction of the bias and whether we considered it was likely to impact on the findings. 

 

Measures of treatment effect

 

Dichotomous data

For dichotomous data, we presented the results as the summary risk ratio with the 95% confidence intervals. 

 

Continuous data

For continuous data, we used the mean difference if the outcomes were measured in the same way between trials. If necessary, we planned to use the standardised mean difference to combine trials that measured the same outcome, but used different methods.  

 

Unit of analysis issues

 

Cluster-randomised trials

We included cluster-randomised trials in the analyses along with individually-randomised trials. We adjusted their sample sizes using the methods described in the Cochrane Handbook for Systematic Reviews of Interventions (Higgins 2011) using an estimate of the intra-cluster correlation co-efficient (ICC) derived from the trial (if possible), from a similar trial or from a study of a similar population. If we used ICCs from other sources, we reported this and conducted sensitivity analyses to investigate the effect of variation in the ICC. When we wanted to identify both cluster-randomised trials and individually-randomised trials, we planned to synthesise the relevant information. We would have considered it reasonable to combine the results from both if there was little heterogeneity between the study designs and the interaction between the effect of intervention and the choice of randomisation unit was considered to be unlikely. Two of the trials (Ceesay 1997; Kafatos 1989) gave no published or unpublished data on the outcome-specific ICC. Therefore, we assumed a value of 0.01 and adjusted the corresponding sample sizes according to the design effect, i.e. by dividing the crude (individual) sample sizes by 1+ (m -1)r, where m is the average cluster size and r is the ICC (assumed to be 0.01). We conducted sensitivity analyses to investigate the effect of variation in the ICC (Figure 1; Figure 2).

 FigureFigure 1. Sensitivity analysis of the effect of clustering : Nutritional advice during pregnancy (1.7 preterm birth) Kafatos 1989
 FigureFigure 2. Sensitivity analysis of the effect of clustering : Balanced protein/energy supplementation in pregnancy (2.1 Stillbirth) Ceesay 1997

 

Cross-over trials

Cross-over trials were not considered in this review.

 

Dealing with missing data

For included studies, the levels of attrition were noted. The impact of including studies with high levels of missing data in the overall assessment of the treatment effect was explored using a sensitivity analysis.

All outcomes analyses were carried out, as far as possible, on an intention-to-treat basis, i.e. we attempted to include all participants randomised to each group in the analyses. The denominator for each outcome in each trial was the randomised number minus any participants whose outcomes were known to be missing.

 

Assessment of heterogeneity

We assessed the statistical heterogeneity in each meta-analysis using T², I² and Chi² statistics. We regarded heterogeneity as substantial if the I² was greater than 30% and either T² was greater than zero, or there was a low P value (less than 0.10) in the Chi² test for heterogeneity. 

 

Assessment of reporting biases

If there were 10 or more studies in the meta-analysis, we investigated the reporting biases (such as publication bias) using funnel plots. We assessed the funnel plot asymmetry visually, and used formal tests for funnel plot asymmetry. For continuous outcomes, we used the test proposed by Egger 1997, and for dichotomous outcomes, we used the test proposed by Harbord 2006. If asymmetry was detected in any of these tests or was suggested by a visual assessment, we performed exploratory analyses to investigate this.

 

Data synthesis

We carried out statistical analysis using Review Manager software (RevMan 2011). We used a fixed-effect inverse variance meta-analysis for combining data where trials were examining the same intervention, and the trials' populations and methods were judged to be sufficiently similar. If there was clinical heterogeneity sufficient to expect that the underlying treatment effects differed between trials, or if substantial statistical heterogeneity was detected, we used a random-effects meta-analysis to produce an overall summary when an average treatment effect across trials was considered clinically meaningful. The random-effects summary was treated as the average range of possible treatment effects and we discussed the clinical implications of treatment effects differing between trials. Where the average treatment effect was not clinically meaningful, we did not combine trials.

When we performed random-effects analyses, the results were presented as the average treatment effects with 95% confidence intervals, and the estimates of T² and I².

 

Subgroup analysis and investigation of heterogeneity

When we identified substantial heterogeneity, we investigated it using subgroup analyses and sensitivity analyses. We considered whether an overall summary was meaningful, and if it was, we used a random-effects analysis to produce such a summary.

Since observational studies (IOM 1990; Kramer 1987) suggest a stronger association between gestational weight gain and fetal growth in women who were under-nourished before pregnancy, we stratified the analysis of the effects on mean birthweight into those trials in which the majority of women had low pre-pregnancy (or early pregnancy) weight (Ceesay 1997; Girija 1984; Kardjati 1988; Mora 1978; Rush 1980), and those in which the participants appeared adequately nourished (Elwood 1981; Ross 1985; Viegas 1982a). For the Taiwan trial (Blackwell 1973) and (Huybregts 2009; Viegas 1982b), within-trial stratification was possible, based on data contained in the published reports.

For fixed-effect inverse variance meta-analyses, we assessed differences between subgroups by interaction tests. For random-effects and fixed-effect meta-analyses using methods other than inverse variance, we assessed differences between subgroups by inspection of the subgroups' confidence intervals, in which non-overlapping confidence intervals indicated a statistically significant difference in the treatment effects between the subgroups.

Because growth varies with differences in sex (Onis 2007), it is desirable to compare growth between groups after adjusting for variations by sex. We conducted subgroup analysis on the children, separated by sexes for follow-up results of balanced protein and energy supplementation at the age of 11 to 17 years (height, weight, systolic blood pressure, diastolic blood pressure, BMI z-score, and body fat).

 

Sensitivity analysis

We carried out sensitivity analyses to explore the effects of fixed- or random-effects analyses for outcomes with statistical heterogeneity.

 

Results

  1. Top of page
  2. Summary of findings    [Explanations]
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Appendices
  12. What's new
  13. History
  14. Contributions of authors
  15. Declarations of interest
  16. Sources of support
  17. Differences between protocol and review
  18. Index terms
 

Description of studies

See: Characteristics of included studies; Characteristics of excluded studies; Characteristics of ongoing studies.

 

Results of the search

Initially we examined 110 reports corresponding to 46 trials. Of these trials, 15 were included and 30 were excluded. One trial is ongoing (Moore 2011) with the results expected in 2013 (see Characteristics of ongoing studies). (Three reports from an updated search in July 2012 have been added to Studies awaiting classification.)

 

Included studies

We included 15 trials published between 1973 to 2009 that met the inclusion criteria. Most of the trials focused on assessing the effects of dietary advice, supplementation, or restriction on gestational weight gain, pre-eclampsia and/or pregnancy outcomes, or the development of the children. Four trials (Briley 2002; Hunt 1976; Kafatos 1989; Sweeney 1985) evaluated nutritional advice to increase energy and protein intake. Eleven trials (Blackwell 1973; Ceesay 1997; Elwood 1981; Girija 1984; Huybregts 2009; Kardjati 1988; Mora 1978; Ross 1985; Rush 1980; Viegas 1982a; Viegas 1982b) assessed the impact of balanced energy/protein supplementation. Only one trial assessed the effects of high-protein nutritional supplements (Rush 1980). Two trials (Viegas 1982a; Viegas 1982b) investigated the effects of isocaloric protein supplements. Seven trials were from high-income countries such as the USA and UK, and eight trials from low- and middle-income countries such as Ganbia, Taiwan, India, Burkina Faso, Greece, Indonesia, Colombia, South Africa. Four trials were conducted in an economically disadvantaged area including under-nourished populations; the other 11 trials included well-nourished populations. Interventions for nutritional advice included counselling or classes versus no interventions (three trials; Hunt 1976; Kafatos 1989; Sweeney 1985) and counselling versus home visits without counselling (one trial; Briley 2002). Interventions for balanced energy and protein supplementation included supplementation versus control supplements (eight trials; Blackwell 1973; Huybregts 2009; Kardjati 1988; Mora 1978; Ross 1985; Rush 1980; Viegas 1982a; Viegas 1982b) and supplementation versus no intervention (three trials; Ceesay 1997; Elwood 1981; Girija 1984). Intervention for high-protein nutritional supplements included supplementation versus supplement containing vitamins/minerals (Rush 1980). Intervention for isocaloric-protein nutritional supplements included supplementation versus supplement of flavoured carbonated water containing iron and vitamin C (Viegas 1982a; Viegas 1982b).

For details of the included studies, see the Characteristics of included studies table.

 

Excluded studies

We excluded 30 trials. Of these trials, eight trials did not match the interventions in this review, nine involved participants who were outside the scope of the review, one did not have a control group, one trial's analysis was based on individual women despite randomising by village, and 11 trials did not involve randomisation, or the designs were outside the scope of the review.

For details of the excluded studies, see the Characteristics of excluded studies table.

 

Risk of bias in included studies

See Figure 3 and Figure 4.

 FigureFigure 3. 'Risk of bias' graph: review authors' judgements about each risk of bias item presented as percentages across all included studies.
 FigureFigure 4. 'Risk of bias' summary: review authors' judgements about each risk of bias item for each included study.

 

Allocation (selection bias)

 

Sequence generation

Six trials had a low risk of bias because of adequate randomisation of participants to the intervention groups (Elwood 1981; Huybregts 2009; Kafatos 1989; Kardjati 1988; Rush 1980; Sweeney 1985). For nine trials, risk of bias could not be adequately judged because no detailed information was provided about allocation sequence generation (Blackwell 1973; Briley 2002; Ceesay 1997; Girija 1984; Hunt 1976; Mora 1978; Ross 1985; Viegas 1982a; Viegas 1982b).

 

Allocation concealment

Five trials had a low risk of bias through the use of sequentially numbered, opaque, sealed envelopes or drug containers of identical appearance (Elwood 1981; Huybregts 2009; Kardjati 1988; Rush 1980; Sweeney 1985). Ten trials provided no information about allocation concealment (Blackwell 1973; Briley 2002; Ceesay 1997; Girija 1984; Hunt 1976; Kafatos 1989; Mora 1978; Ross 1985; Viegas 1982a; Viegas 1982b).

 

Blinding (performance bias and detection bias)

Six trials had a low risk of bias using single or double blinding, or used no blinding but reported outcomes and outcome measurements that were not likely to be influenced by the lack of blinding. Seven trials had a high risk of bias owing to a lack of blinding. Two trials could not be judged for the risk because no information was provided (Viegas 1982a; Viegas 1982b).

 

Incomplete outcome data (attrition bias)

Losses to follow-up ranged from 1.5% in Viegas 1982b to 25.9% in Briley 2002. Eleven trials had a low risk of bias, two trials had a high risk of bias and two trials were judged as unclear bias owing to insufficient information.

 

Selective reporting (reporting bias)

Fourteen trials were judged as unclear risk because the protocol was not available for judgment of this bias. Only one trial (Huybregts 2009) had a protocol and was judged as low risk for selective reporting.

 

Other potential sources of bias

Eight trials had a high risk of bias because no data were presented on compliance or substitution, and for other reasons. Three trials had a low risk of bias and four trials had insufficient information and were judged as unclear risk.

The funnel plots (Figure 5; Figure 6) did not show any publication bias.

 FigureFigure 5. Funnel plot of comparison: 2 Balanced protein/energy supplementation in pregnancy, outcome: 2.3 Birthweight (g).
 FigureFigure 6. Funnel plot of comparison: 2 Balanced protein/energy supplementation in pregnancy, outcome: 2.9 Weekly gestational weight gain (g/week).

 

Effects of interventions

See:  Summary of findings for the main comparison Nutritional advice compared to no counselling or advice during pregnancy for perinatal outcomes;  Summary of findings 2 Balanced protein and energy supplementation compared to control or no intervention in pregnancy for perinatal and maternal outcomes;  Summary of findings 3 High protein supplementation in pregnancy and perinatal outcomes;  Summary of findings 4 Isocaloric balanced protein supplementation in pregnancy and outcomes

 

Nutritional advice to increase energy and protein intakes

Four trials of nutritional advice, involving 790 women, were included. For the primary outcomes, there was no significant effect on stillbirth (risk ratio (RR) 0.37, 95% confidence interval (CI) 0.07 to 1.90; one trial, 431 women-  Analysis 1.1) or neonatal death (RR 1.28, 95% CI 0.35 to 4.72; one trial, 448 women-  Analysis 1.2 ). There was no significant effects on the outcomes of birthweight ( Analysis 1.3), birth length ( Analysis 1.4), and small-for-gestational age ( Analysis 1.6). Because the results of total gestational weight gain (Briley 2002; Kafatos 1989) were inconsistent and showed high heterogeneity we have not combined the studies in the analysis (no total shown in  Analysis 1.11). Birth head circumference (cm) was significantly increased in the intervention group (mean difference (MD) 0.99 cm, 95% CI 0.43 to 1.55; one trial, 389 women -  Analysis 1.5). The 'significant' reduction in preterm birth associated with advice (RR 0.46, 95% CI 0.21 to 0.98, P < 0.05; two trials, 449 women -  Analysis 1.7) was not consistent with the total absence of effect on mean gestational age (MD -0.10 weeks, 95% CI -0.48 to 0.28; one trial, 399 women -  Analysis 1.8). Sensitivity analyses (Figure 1) was conducted in using values of 0.01 for the ICC did not qualitatively change the relative risks for preterm in Kafatos 1989. Within the methodological limitations discussed above, advice to increase protein intake seems to be successful in achieving its goal (protein intake: MD +6.99 g/day, 95% CI 3.02 to 10.97, P < 0.05; three trials, 632 women-  Analysis 1.9), but there was no significant increase in energy intake (energy intake: MD +105.61 kcal/day, 95% CI -18.94 to 230.15, P = 0.10; three trials, 342 women -  Analysis 1.10).

 

Balanced energy/protein supplementation

Eleven trials, involving 5385 women, were included. Providing balanced energy and protein supplementation significantly reduced the risk of stillbirth (RR 0.62, 95% CI 0.40 to 0.98; five trials, 3408 women -  Analysis 2.1). Neonatal death was unaffected (RR 0.68, 95% 0.43 to 1.07; five trials, 3381 women -  Analysis 2.2). Sensitivity analyses (Figure 2) for ICCs of 0.02 to 0 made little difference, using values of 0.01 for the ICC did not qualitatively change the relative risks for stillbirth in Ceesay 1997.

Supplementation was also associated with significant increases in mean birthweight (random-effects MD +40.96 g, 95% CI 4.66 to 77.26, Tau2 = 1744, I2 = 44%, P = 0.03; 11 trials, 5385 infants -  Analysis 2.3 ). Although clinically small, birth length (cm) was statistically significantly increased (fixed-effect MD +0.16 cm, 95% CI 0.01 to 0.31; five trials, 3370 women -  Analysis 2.4), while no significant difference was found for birth head circumference ( Analysis 2.5). The incidence of small-for-gestational age birth was significantly reduced (RR 0.79, 95% CI 0.69 to 0.90, I2 = 16%; seven trials, 4408 women -  Analysis 2.6). There were no significant effects observed on preterm birth ( Analysis 2.7), gestational age (week) ( Analysis 2.8), or weekly gestational weight gain (g/week) ( Analysis 2.9). The rather meagre data on pre-eclampsia did not suggest a reduction in risk with supplementation (RR 1.48, 95% CI 0.82 to 2.66; two trials, 463 women -  Analysis 2.10).

Although postnatal follow-up was limited to a small number of trials, the enhancement of fetal growth observed in those trials was not reflected in larger size or improved neurocognitive development at one year. Bayley mental score at one year had no significant effect in one trial (Rush 1980;  Analysis 2.11). The Taiwan trial (Blackwell 1973) detected no effect on Stanford-Binet IQ score at five years ( Analysis 2.12), and weight at one year ( Analysis 2.13). The data of the standard deviation of length at one year for Blackwell 1973 were not credible compared with the Rush 1980 study, we have omitted this trial from the analysis and only showed the data from Rush 1980 ( Analysis 2.14). There was no significant effect on head circumference at one year from either the Taiwan (Blackwell 1973) or Harlem trials (Rush 1980) ( Analysis 2.15).

Maternal outcomes other than weight gain were reported infrequently. Only one trial each reported results on other outcomes. The Bogota trial (Mora 1978) detected no significant reduction in duration of labour with supplementation ( Analysis 2.16). The East Java trial (Kardjati 1988) found neither an increase in maternal weight at four weeks postpartum ( Analysis 2.17).

Follow-up at 6.5 to 9.5 years of age for approximately 25% of the children randomised in Ceesay 1997 found no difference in immune function (delayed-hypersensitivity skin tests, antibody responses to pneumococcal and rabies vaccines, and salivary IgA concentration) between the intervention and control groups (data not shown in data and analysis table). Follow-up at 11 to 17 years of age for approximately two-thirds of the children who were still alive found no significant differences in height ( Analysis 2.18), weight ( Analysis 2.19), or systolic or diastolic blood pressure ( Analysis 2.20;  Analysis 2.21), but did find a small increase in the mean BMI z-score (MD +0.16, 95% CI +0.01 to +0.31; one trial, 855 children -  Analysis 2.22) in the control group. However, the difference in BMI was in contrast with the absence of the effect on per cent body fat ( Analysis 2.23).

 

High-protein supplementation

Only one trial (Rush 1980), involving 1051 women, was included. For primary outcomes, the Harlem trial (Rush 1980) reported non-significant effects in stillbirth (RR 0.81, 95% CI 0.31 to 2.15; one trial, 529 women -  Analysis 3.1) and neonatal death (RR 2.78, 95% CI 0.75 to 10.36; one trial, 529 women -  Analysis 3.2) with high-protein supplementation. The only available trial (Rush 1980) provided the evidence of significant increases in infants born small-for-gestational age (RR 1.58, 95% CI 1.03 to 2.41, P = 0.04; one trial, 505 women -  Analysis 3.3), although no significant effect for birthweight ( Analysis 3.4) or preterm birth ( Analysis 3.5).

High-protein supplementation had no effect on weekly gestational weight gain (MD +4.50 g/week, 95% CI -33.55 to +42.55; one trial, 486 women -  Analysis 3.6). At one-year follow-up in the Harlem trial (Rush 1980), high-protein supplementation was not associated with detectable differences in weight ( Analysis 3.7), length ( Analysis 3.8), head circumference ( Analysis 3.9) or Bayley mental score ( Analysis 3.10).

 

Isocaloric protein supplementation

Two trials, involving 184 women, were included. Owing to the significant heterogeneity in the results for birthweight and gestational weight gain, the data were pooled using a random-effects model. There was no significant effect on birthweight or gestational weight gain of isocaloric protein supplementation. For mean birthweight the MD was +108.25 g (95% CI -220.89 to 437.40, Tau2 = 47211, I2 = 84%; two trials, 184 infants -  Analysis 4.1), while for gestational weight gain, the MD was +110.45 g/week (95% CI 82.87 to 303.76, Tau2 = 16542, I2 = 85%; two trials, 184 women -  Analysis 4.2).

 

Subgroup analysis in balanced energy/protein supplementation

Since observational studies (IOM 1990; Kramer 1987) suggested a stronger association between gestational weight gain and fetal growth in women who were under-nourished before pregnancy, we stratified the analysis of the effects on mean birthweight into those trials in which the majority of women had low pre-pregnancy (or early pregnancy) weight (Ceesay 1997; Girija 1984; Kardjati 1988; Mora 1978; Rush 1980) and those in which the participants appeared adequately nourished (Elwood 1981; Ross 1985; Viegas 1982a). For the Taiwan trial (Blackwell 1973), (Huybregts 2009) and (Viegas 1982b), within-trial stratification was possible, based on the data contained in the published reports. Only the mean birthweight in balanced energy/protein supplementation were analysed for the subgroups of undernourished and nourished women. However, there was no evidence of a subgroup differences between the malnourished and adequately nourished groups (test for subgroup differences: Chi2 = 2.35. df = 1(P = 0.12), I2 = 57.5%).

 

Discussion

  1. Top of page
  2. Summary of findings    [Explanations]
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Appendices
  12. What's new
  13. History
  14. Contributions of authors
  15. Declarations of interest
  16. Sources of support
  17. Differences between protocol and review
  18. Index terms
 

Summary of main results

Nutritional advice was successful in reducing the risk of preterm birth, increasing head circumference at birth and increasing protein intake, however, there was no evidence of benefit or adverse effect for any other outcome reported.

Balanced energy/protein supplementation was associated with significantly reduced risk of stillbirth, increased mean birthweight, and a significant reduction in the risk of small-for-gestational-age birth. No significant effect was detected for preterm birth, or neonatal death.

High-protein supplementation was associated with a significantly increased risk of infants born small-for-gestational age, but this is based on only one trial including 1051 women. Isocaloric protein supplementation had no significant effect on birthweight or weekly gestational weight gain, based on two trials including only 184 women.

 

Overall completeness and applicability of evidence

Nutritional advice appears effective in increasing pregnant women's protein intake, reducing preterm birth and significant increases in birth head circumference. No data have been reported on other important maternal pregnancy outcomes, such as duration of labour, caesarean section, or postpartum weight retention.

The modest increase in birthweight associated with balanced energy/protein supplementation may well be explained by the rather small net increases in energy intake achieved in most of the trials. Noncompliance and dietary substitution are likely explanations for these small net increases, and the much higher energy supplement provided in the Gambia trial (Ceesay 1997) appeared to have a much larger effect on mean birthweight. Of the seven sizeable trials with the highest methodological quality (Blackwell 1973; Ceesay 1997; Elwood 1981; Huybregts 2009; Kardjati 1988; Mora 1978; Rush 1980), only the East Java trial (Kardjati 1988) failed to show any benefit for mean birthweight ( Analysis 2.3), despite convincing evidence that the trial participants were under-nourished prior to the intervention. Owing to the large sample size, chance is an unlikely explanation for the absence of benefit in the East Java trial( Kardjati 1988), and an undetected substitution of the normal home diet by the supplement seems more likely. Due to the significant effect on mean birthweight ( Analysis 2.3), the reduction in the risk of infant born in small-for-gestational age ( Analysis 2.6) was substantial. Nonetheless, that reduction did not appear to be associated with long-term benefits for child growth or development, but long-term follow-up was only reported in two trials (Ceesay 1997; Rush 1980). Of greatest importance is the evidence indicating reduced risk of stillbirth ( Analysis 2.1). However, this evidence is based on five trials and the evidence is classified as low quality, and the biological mechanism for such risk reduction remains unclear, given the modest effects observed on the indices of fetal growth.

Most of the supplements/dietary manipulations also involved changes to the micronutrient (vitamins and minerals) content of the diet in the both intervention and control. As micronutrient supplementation may also alter some pregnancy outcomes independent of protein and energy, it is difficult to separate the contribution to the effects, particularly in the "balanced protein and energy" studies.

The available evidence from one trial provides no justification for prescribing high-protein nutritional supplements to pregnant women. Not only do such supplements appear to lack beneficial effects, but the evidence suggests that they may even be harmful. Furthermore, the data derived from these trials suggest that isocaloric protein supplementation alone (i.e. without energy supplementation) is unlikely to be of benefit to pregnant women or their infants. The included two trials had high heterogeneity, probably because amounts of energy supplementation were different (273 kcal in Viegas 1982a; 425 kcal in Viegas 1982b). The finding of the excluded trial of Mardones 1988, which reported increases in the risk of infant born small-for-gestational age, remains uncertain, given the methodological limitations of the trial. Moreover, the normal-protein "control" supplement in Mardones 1988 contained much higher quantities of iron and other micronutrients than the high protein supplement.

The results of this review should be interpreted with caution considering that the majority of trials were published in 1970/1980s. The incidence of inadequate nutrition and overweight and obesity is likely to be different today and most trials included a mixed population of those considered to have poor nutritional status and potentially those with adequate nutrition or over-nutrition. Indeed seven trials were from high-income countries where recent reports suggest two-thirds of the general population and half of pregnant women are overweight or obese (Haslehurst 2006; Wang 2011).

 

Quality of the evidence

We included 15 trials involving 7410 women. The quality of the evidence in this review is assessed using the GRADE approach (Guyatt 2008) and the results are presented in  Summary of findings for the main comparison;  Summary of findings 2;  Summary of findings 3; and  Summary of findings 4. The GRADE uses four levels of quality (very low, low, moderate and high) over several domains covering limitations in the design and implementation of the studies, indirectness of evidence, unexplained heterogeneity or inconsistency in the results, imprecision of the results and high probability of publication bias. In the nutritional advice during pregnancy studies ( Summary of findings for the main comparison), the evidence was judged to be of moderate quality (birth head circumference), and low quality (Stillbirth, neonatal death, preterm birth, infants born small-for-gestational age and protein intake) which includes two of the primary outcomes, to very low quality (birthweight) suggesting that the estimates were very uncertain. In the balanced protein and energy supplementation in pregnancy studies ( Summary of findings 2), with significant reductions in stillbirth and infants born small-for-gestational age, and significant increase in birthweight were considered to be of moderate quality. Preterm birth was moderate quality. Neonatal death were of low quality and pre-eclampsia was of very low quality. In the high-protein supplementation in pregnancy studies ( Summary of findings 3), the significant increase in infants born small-for-gestational age was of moderate quality in only one study (Rush 1980). In the isocaloric balanced protein supplementation in pregnancy studies ( Summary of findings 4), the evidence was judged to be of very low quality (birthweight, weekly gestational weight gain) meaning that the estimates were very uncertain.

 

Potential biases in the review process

There were several potential biases in the review process. We made efforts to limit the bias in several ways: two review authors assessed the eligibility for inclusion and assessed the risks of bias independently. Although the authors' views varied, we decided to accept the final conclusions after extensive discussion and reaching a consensus. Carrying out reviews, however, may require a number of subjective judgements, and it is possible that a different review team may have reached different decisions regarding the assessments of eligibility and risks of bias. Feedback from readers will serve to improve the next review update.

 

Agreements and disagreements with other studies or reviews

We have included only randomised controlled trials (RCTs) and excluded the quasi-RCTs previously included in the review (Kramer 2003). The new findings of this review are that balanced energy and protein supplementation was associated with significant increases in mean birthweight, while the other major findings are consistent with those of the previous Cochrane Review (Kramer 2003). Prenatal supplementation with multi-micronutrients was associated with a significantly reduced risk of low-birthweight infants and with improved birthweight when compared with iron-folic acid supplementation, although there was no effect on the risk of preterm birth or small-for gestational-age infants (Shah 2009). Researchers should aim to include only those women in trials to increase energy and protein intake who have the potential to benefit. Observational data suggest women who are overweight or obese or who exceed their daily energy and protein requirements during pregnancy are at increased risk of adverse pregnancy outcomes including: stillbirth and large-for-gestational age and macrosomia (birthweight > 4 kg) (Chen 2009; Heslehurst 2008; Thangaratinam 2012), therefore, the effect of increasing protein and energy intakes could have opposite effects on different populations within the same trial if those included are not adequately defined and selected.

 

Authors' conclusions

  1. Top of page
  2. Summary of findings    [Explanations]
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Appendices
  12. What's new
  13. History
  14. Contributions of authors
  15. Declarations of interest
  16. Sources of support
  17. Differences between protocol and review
  18. Index terms

 

Implications for practice

This review provides encouraging evidence that nutritional advice to increase protein and energy intake and balanced energy and protein supplementation may reduce some perinatal adverse outcomes. The long-term effects are unclear and it seems likely that targeting undernourished women rather than the whole obstetric population would convey the most benefit. For most of the included trials in this review, the risk of bias was either unclear or high for at least one category examined, and the results of this review should therefore be interpreted with caution.

Nutritional advice appears to be effective in increasing pregnant women's protein intake, and increases fetal growth such as birth head circumference. The 54% relative reduction in preterm birth for nutritional advice in energy and protein compared with no nutritional counselling may be beneficial to pregnant women.

Balanced energy and protein supplementation appears to reduce the risks of stillbirth, although the biological mechanisms underlying these reductions remain unclear. Furthermore, balanced protein and energy intervention, as provided in most trials, results in significant increases in maternal weight gain and infant birthweight, and decreases the risk of infants born in small-for-gestational age. These effects do not seem to confer long-term benefits to the child in terms of growth, neurocognitive development, and adiposity or blood pressure. The available evidence is inadequate to evaluate the potential effects on preterm birth, neonatal death or maternal health.

Based on the available evidence, there is no justification for prescribing high-protein and isocaloric nutritional supplements to pregnant women, although the number of trials and women included are few.

 
Implications for research

High-quality randomised trials are needed that target those women who are nutritionally deprived or underweight with reduced energy intake; long-term follow-up is required.

Given the modest benefits in preterm delivery documented for balanced energy and protein advice during pregnancy, future randomised trials need to assess the effects on perinatal outcomes such as stillbirth, neonatal death and birthweight. Effective interventions, such as the content and frequency of nutritional advice, need to be clarified.

Future energy and protein supplementation trials should focus their attention on outcomes other than fetal growth, especially in undernourished women and particularly on confirming the evidence of intervention on reduced risks of stillbirth and infants born small-for-gestational age. Such trials will require large sample sizes. Any future trials should also assess the effects on women, including duration of labour, caesarean section, macrosomia and postpartum weight retention.

The lack of evidence of benefit, coupled with the possibility of harm, suggests that future trials of high-protein supplementation, and isocaloric protein supplementation should not be considered.

 

Acknowledgements

  1. Top of page
  2. Summary of findings    [Explanations]
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Appendices
  12. What's new
  13. History
  14. Contributions of authors
  15. Declarations of interest
  16. Sources of support
  17. Differences between protocol and review
  18. Index terms

We are grateful to Michael S. Kramer and Ritsuko Kakuma who developed the original review (Kramer 2003) and subsequent updates upon which this updated review is based.

The review authors would like to acknowledge the Pregnancy and Childbirth team for assistance with the preparation of the original review and its update, including the Trials Search Co-ordinator for assistance in developing the search strategy, the editors, co-editors and other staff within the team. We also acknowledge Tommy Tang and Stuart Gilmour, who supported the 2012 update.

As part of the pre-publication editorial process, this review has been commented on by three peers (an editor and two referees who are external to the editorial team) and the Group's Statistical Adviser.

 

Data and analyses

  1. Top of page
  2. Summary of findings    [Explanations]
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Appendices
  12. What's new
  13. History
  14. Contributions of authors
  15. Declarations of interest
  16. Sources of support
  17. Differences between protocol and review
  18. Index terms
Download statistical data

 
Comparison 1. Nutritional advice during pregnancy

Outcome or subgroup titleNo. of studiesNo. of participantsStatistical methodEffect size

 1 Stillbirth1431Risk Ratio (M-H, Fixed, 95% CI)0.37 [0.07, 1.90]

 2 Neonatal death1448Risk Ratio (M-H, Fixed, 95% CI)1.28 [0.35, 4.72]

 3 Birthweight (g)2426Mean Difference (IV, Random, 95% CI)205.75 [-242.54, 654.03]

 4 Birth length (cm)1399Mean Difference (IV, Fixed, 95% CI)0.17 [-0.72, 1.06]

 5 Birth head circumference (cm)1389Mean Difference (IV, Fixed, 95% CI)0.99 [0.43, 1.55]

 6 Small-for-gestational age1404Risk Ratio (M-H, Fixed, 95% CI)0.97 [0.45, 2.11]

 7 Preterm birth2449Risk Ratio (M-H, Fixed, 95% CI)0.46 [0.21, 0.98]

 8 Gestational age (week)1399Mean Difference (IV, Fixed, 95% CI)-0.10 [-0.48, 0.28]

 9 Protein intake (g/day)3632Mean Difference (IV, Fixed, 95% CI)6.99 [3.02, 10.97]

 10 Energy intake (kcal/day)3342Mean Difference (IV, Fixed, 95% CI)105.61 [-18.94, 230.15]

 11 Total gestational weight gain (kg)2Mean Difference (IV, Random, 95% CI)Totals not selected

 
Comparison 2. Balanced protein/energy supplementation in pregnancy

Outcome or subgroup titleNo. of studiesNo. of participantsStatistical methodEffect size

 1 Stillbirth53408Risk Ratio (M-H, Fixed, 95% CI)0.62 [0.40, 0.98]

 2 Neonatal death53381Risk Ratio (M-H, Fixed, 95% CI)0.68 [0.43, 1.07]

 3 Birthweight (g)115385Mean Difference (IV, Random, 95% CI)40.96 [4.66, 77.26]

    3.1 Undernourished women
82903Mean Difference (IV, Random, 95% CI)66.96 [13.13, 120.78]

    3.2 Adequately nourished women
62482Mean Difference (IV, Random, 95% CI)15.93 [-20.83, 52.69]

 4 Birth length (cm)53370Mean Difference (IV, Fixed, 95% CI)0.16 [0.01, 0.31]

 5 Birth head circumference (cm)53352Mean Difference (IV, Random, 95% CI)0.04 [-0.08, 0.17]

 6 Small-for-gestational age74408Risk Ratio (M-H, Fixed, 95% CI)0.79 [0.69, 0.90]

 7 Preterm birth53384Risk Ratio (M-H, Fixed, 95% CI)0.96 [0.80, 1.16]

 8 Gestational age (week)63471Mean Difference (IV, Fixed, 95% CI)-0.10 [-0.22, 0.01]

 9 Weekly gestational weight gain (g/week)92391Mean Difference (IV, Random, 95% CI)18.63 [-1.81, 39.07]

 10 Pre-eclampsia2463Risk Ratio (M-H, Fixed, 95% CI)1.48 [0.82, 2.66]

 11 Bayley mental score at 1 year1411Mean Difference (IV, Fixed, 95% CI)-0.74 [-1.95, 0.47]

 12 IQ at 5 years1153Mean Difference (IV, Fixed, 95% CI)0.0 [-4.98, 4.98]

 13 Weight at 1 year (g)2623Mean Difference (IV, Fixed, 95% CI)30.43 [-139.67, 200.53]

 14 Length at 1 year (cm)1428Mean Difference (IV, Fixed, 95% CI)0.0 [-5.69, 5.69]

 15 Head circumference at 1 year (cm)2627Mean Difference (IV, Fixed, 95% CI)-0.13 [-0.35, 0.10]

 16 Duration of labour (hours)1345Mean Difference (IV, Fixed, 95% CI)-0.09 [-1.18, 1.00]

 17 Maternal weight 4 weeks' postpartum (kg)1354Mean Difference (IV, Fixed, 95% CI)-0.90 [-1.92, 0.12]

 18 Height at age 11-17 years (cm)1855Mean Difference (IV, Fixed, 95% CI)-0.39 [-1.73, 0.94]

    18.1 Boys
1445Mean Difference (IV, Fixed, 95% CI)0.60 [-1.40, 2.60]

    18.2 Girls
1410Mean Difference (IV, Fixed, 95% CI)-1.20 [-3.00, 0.60]

 19 Weight at 11-17 years (kg)1855Mean Difference (IV, Fixed, 95% CI)0.46 [-0.77, 1.69]

    19.1 Boys
1445Mean Difference (IV, Fixed, 95% CI)0.70 [-0.89, 2.29]

    19.2 Girls
1410Mean Difference (IV, Fixed, 95% CI)0.10 [-1.86, 2.06]

 20 Systolic blood pressure at age 11-17 years (mmHg)1855Mean Difference (IV, Fixed, 95% CI)0.60 [-0.61, 1.81]

    20.1 Boys
1445Mean Difference (IV, Fixed, 95% CI)1.10 [-0.61, 2.81]

    20.2 Girls
1410Mean Difference (IV, Fixed, 95% CI)0.10 [-1.60, 1.80]

 21 Diastolic blood pressure at age 11-17 years (mmHg)1855Mean Difference (IV, Fixed, 95% CI)-0.08 [-1.10, 0.93]

    21.1 Boys
1445Mean Difference (IV, Fixed, 95% CI)0.5 [-0.98, 1.98]

    21.2 Girls
1410Mean Difference (IV, Fixed, 95% CI)-0.60 [-1.99, 0.79]

 22 BMI z-score at age 11-17 years1855Mean Difference (IV, Fixed, 95% CI)0.16 [0.01, 0.31]

    22.1 Boys
1445Mean Difference (IV, Fixed, 95% CI)0.20 [0.00, 0.40]

    22.2 Girls
1410Mean Difference (IV, Fixed, 95% CI)0.10 [-0.13, 0.33]

 23 % body fat at 11-17 years1847Mean Difference (IV, Fixed, 95% CI)0.06 [-0.41, 0.52]

    23.1 Boys
1440Mean Difference (IV, Fixed, 95% CI)0.0 [-0.54, 0.54]

    23.2 Girls
1407Mean Difference (IV, Fixed, 95% CI)0.20 [-0.68, 1.08]

 
Comparison 3. High protein supplementation in pregnancy

Outcome or subgroup titleNo. of studiesNo. of participantsStatistical methodEffect size

 1 Stillbirth1529Risk Ratio (M-H, Fixed, 95% CI)0.81 [0.31, 2.15]

 2 Neonatal death1529Risk Ratio (M-H, Fixed, 95% CI)2.78 [0.75, 10.36]

 3 Small-for-gestational age1505Risk Ratio (M-H, Fixed, 95% CI)1.58 [1.03, 2.41]

 4 Birthweight (g)1504Mean Difference (IV, Fixed, 95% CI)-73.0 [-171.26, 25.26]

 5 Preterm birth1505Risk Ratio (M-H, Fixed, 95% CI)1.14 [0.83, 1.56]

 6 Weekly gestational weight gain (g/week)1486Mean Difference (IV, Fixed, 95% CI)4.5 [-33.55, 42.55]

 7 Weight at 1 year (g)1409Mean Difference (IV, Fixed, 95% CI)61.0 [-184.60, 306.60]

 8 Length at 1 year (cm)1412Mean Difference (IV, Fixed, 95% CI)0.20 [-5.59, 5.99]

 9 Head circumference at 1 year1412Mean Difference (IV, Fixed, 95% CI)0.11 [-0.19, 0.41]

 10 Bayley mental score at 1 year1396Mean Difference (IV, Fixed, 95% CI)0.32 [-0.91, 1.55]

 
Comparison 4. Isocaloric balanced protein supplementation in pregnancy

Outcome or subgroup titleNo. of studiesNo. of participantsStatistical methodEffect size

 1 Birthweight (g)2184Mean Difference (IV, Random, 95% CI)108.25 [-220.89, 437.40]

 2 Weekly gestational weight gain (g/week)2184Mean Difference (IV, Random, 95% CI)110.45 [-82.87, 303.76]

 

Appendices

  1. Top of page
  2. Summary of findings    [Explanations]
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Appendices
  12. What's new
  13. History
  14. Contributions of authors
  15. Declarations of interest
  16. Sources of support
  17. Differences between protocol and review
  18. Index terms
 

Appendix 1. Methods used to assess trials included in previous versions of this review

The following methods were used to assess Atton 1990a; Badrawi 1993; Blackwell 1973; Briley 2002; Campbell 1975; Campbell 1983; Campbell Brown 1983a; Ceesay 1997; Elwood 1981; Girija 1984; Hankin 1962a; Hunt 1976; Kafatos 1989; Kardjati 1988; Mardones 1988a; Mora 1978; Ross 1938a; Ross 1985; Rush 1980; Sweeney 1985; Viegas 1982a; Viegas 1982b; Wolff 2008.

 

Selection of studies  

We assessed all potential studies we identified as a result of the search strategy for inclusion in the review, without consideration of the results. We resolved any disagreement through discussion.

 

Data extraction and management  

Both review authors extracted the data using the agreed form. We used the Review Manager software (RevMan 2003) to double-enter all data.

When information regarding any of the above was unclear, we attempted to contact the authors of the original reports to obtain further details.

 

Measures of treatment effects  

We carried out statistical analysis using the Review Manager software (RevMan 2003). We used a fixed-effect meta-analysis for combining data in the absence of significant heterogeneity if trials were sufficiently similar. If heterogeneity was found, we used random-effects meta-analysis.

 

Dichotomous data

For dichotomous data, we presented the results as the summary relative risk with the 95% confidence intervals.

 

Continuous data

For continuous data, we the weighted mean difference when the outcomes were measured in the same way between trials.

 

Unit of analysis issues  

 

Cluster-randomised trials

We included cluster-randomised trials in the analyses along with individually-randomised trials. Their sample sizes were adjusted by using the methods described in Gates 2005 using an estimate of the intra-cluster correlation co-efficient (ICC) derived from the trial (if possible) or from another source. Two of the trials (Ceesay 1997; Kafatos 1989) gave no published or unpublished data on the outcome-specific ICC. Therefore, we assumed a value of 0.01 and adjusted the corresponding sample sizes according to the design effect, i.e. by dividing the crude (individual) sample sizes by 1+ (m -1)r, where m is the average cluster size and r is the ICC (assumed to be 0.01).

 

Dealing with missing data  

We analysed data for all participants with available data in the group to which they were allocated, regardless of whether or not they received the allocated intervention. If the participants were not analysed in the group to which they were randomised in the original report, and there was sufficient information in the trial report, we attempted to restore them to the correct group.

 

Assessment of heterogeneity  

We applied tests of heterogeneity between trials, if appropriate, using the I² statistic. If we identified high levels of heterogeneity among the trials (exceeding 50%), we explored it by performing sensitivity analysis. A random-effects meta-analysis was used as an overall summary when considered appropriate.

Since observational studies (Kramer 1987; IOM 1990) suggest a stronger association between gestational weight gain and fetal growth in women who were under-nourished before pregnancy, we stratified the analysis of the effects on mean birthweight into those trials in which the majority of women had low pre-pregnancy (or early pregnancy) weight (Atton 1990a; Campbell Brown 1983a; Ceesay 1997; Girija 1984; Kardjati 1988; Mora 1978; Rush 1980), and those in which the participants appeared adequately nourished (Elwood 1981; Ross 1985; Viegas 1982a). For the Taiwan trial (Blackwell 1973) and Viegas 1982b, within-trial stratification was possible, based on data contained in the published reports.

 

What's new

  1. Top of page
  2. Summary of findings    [Explanations]
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Appendices
  12. What's new
  13. History
  14. Contributions of authors
  15. Declarations of interest
  16. Sources of support
  17. Differences between protocol and review
  18. Index terms

Last assessed as up-to-date: 22 December 2011.


DateEventDescription

22 July 2011New citation required and conclusions have changedNutritional advice to increase energy and protein intakes is associated with significant increases in protein intake. Balanced energy and protein supplementation is associated with significant increases in mean birthweight, although this difference disappeared after excluding one trial of weekly gestational weight gain. The other findings have not changed.

22 July 2011New search has been performedA new team of review authors prepared this updated review.

Search updated. Ten new trials identified: one has been included (Huybregts 2009) and eight excluded (Aaltonen 2011; Behrman 2009; Eneroth 2010; Fung 2010; Guelinckx 2010; Laitinen 2009; Luoto 2010; Rasmussen 2010). One trial is ongoing (Moore 2011).

The methods section has changed to include only RCTs and exclude quasi-RCTs or cross-over trials.

Six trials (Atton 1990; Campbell Brown 1983; Hankin 1962; Iyengar 1967; Mardones 1988; Ross 1938), previously included in the analysis, have now been excluded because of their quasi-RCT design.

The current inclusion of information about caloric restriction for women who are overweight or obese only serves to increase confusion as it requires discussion of the clinical implications for two different populations, thus we excluded the outcome of "energy and protein restriction in women who were overweight or showed high weight gain".

Five trials (Badrawi 1993; Campbell 1975; Campbell 1983; Guelinckx 2010; Wolff 2008), previously included in the analysis, have now been excluded because the target population was out of focus.

Three reports from an updated search in July 2012 have been added to Studies awaiting classification for consideration at the next update.



 

History

  1. Top of page
  2. Summary of findings    [Explanations]
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Appendices
  12. What's new
  13. History
  14. Contributions of authors
  15. Declarations of interest
  16. Sources of support
  17. Differences between protocol and review
  18. Index terms

Protocol first published: Issue 2, 1997
Review first published: Issue 2, 1997


DateEventDescription

22 December 2009New search has been performedSearch updated. One new trial included (Wolff 2008) and two excluded (Aaltonen 2005; Kinra 2008).

2 September 2008AmendedConverted to new review format.

30 November 2006New search has been performedNew search conducted in November 2006 identified eight new reports to evaluate (Anderson 1995; an additional report of Clapp 1997; Fard 2004; Kaseb 2002; Moses 2006; additional reports of Lechtig 1975; Woods 1995), none of which were eligible for inclusion in the update. We have substantially updated the Methods of the review section.

1 August 2003New search has been performedThis updated review combines and replaces five previous Cochrane reviews entitled ''Balanced protein/energy supplementation in pregnancy', 'Energy/protein restriction for high weight-for-height or weight gain during pregnancy' (CDSR 1996a), 'High protein supplementation in pregnancy' (CDSR 1996b), 'Isocaloric balanced protein supplementation in pregnancy' (CDSR 1996c) and 'Nutritional advice in pregnancy' (CDSR 1996d).

This combination was suggested by colleagues in the field, the PCG editors, and by the Cochrane Pregnancy and Childbirth Group's Consumer Panel.



 

Contributions of authors

  1. Top of page
  2. Summary of findings    [Explanations]
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Appendices
  12. What's new
  13. History
  14. Contributions of authors
  15. Declarations of interest
  16. Sources of support
  17. Differences between protocol and review
  18. Index terms

Erika Ota (EO) and Rintaro Mori (RM) independently rated all the included studies for the risk of bias tables from the previous review. EO and Rupuam Tobe-Gai (RT) jointly applied the study selection criteria and extracted data from the included studies for updated trials. EO edited the updated results. RT, RM and Diane Farrar (DF) revised the manuscript. All the authors read and approved the final version to be published.

 

Declarations of interest

  1. Top of page
  2. Summary of findings    [Explanations]
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Appendices
  12. What's new
  13. History
  14. Contributions of authors
  15. Declarations of interest
  16. Sources of support
  17. Differences between protocol and review
  18. Index terms

None known.

 

Sources of support

  1. Top of page
  2. Summary of findings    [Explanations]
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Appendices
  12. What's new
  13. History
  14. Contributions of authors
  15. Declarations of interest
  16. Sources of support
  17. Differences between protocol and review
  18. Index terms
 

Internal sources

  • The University of Tokyo, Department of Global Health Policy, Graduate School of Medicine, Japan.

 

External sources

  • Department of Reproductive Health and Research and Department of Technical Cooperation among Countries, World Health Organization, Geneva, Switzerland.

 

Differences between protocol and review

  1. Top of page
  2. Summary of findings    [Explanations]
  3. Background
  4. Objectives
  5. Methods
  6. Results
  7. Discussion
  8. Authors' conclusions
  9. Acknowledgements
  10. Data and analyses
  11. Appendices
  12. What's new
  13. History
  14. Contributions of authors
  15. Declarations of interest
  16. Sources of support
  17. Differences between protocol and review
  18. Index terms

The methods section has changed to include only randomised controlled trials (RCTs) and to exclude quasi-RCTs or cross-over trials. Six trials (Atton 1990; Campbell Brown 1983; Hankin 1962; Iyengar 1967; Mardones 1988; Ross 1938), previously included in the analysis, have now been excluded because of their quasi-RCT design. The current inclusion of information about caloric restriction for women who are overweight or obese only serves to increase confusion as it requires discussion of the clinical implications for two different populations, thus we excluded the outcome of "energy and protein restriction in women who were overweight or showed high weight gain". Five trials (Badrawi 1993; Campbell 1975; Campbell 1983; Guelinckx 2010; Wolff 2008), previously included in the analysis, have now been excluded because the target population was out of focus. Six trials (Atton 1990; Campbell Brown 1983; Hankin 1962; Iyengar 1967; Mardones 1988; Ross 1938), previously included in the review, have now been excluded because of quasi-RCT design.

We have added subgroup analysis from original protocol since observational studies (IOM 1990; Kramer 1987) suggest a stronger association between gestational weight gain and fetal growth in women who were under-nourished before pregnancy, we stratified the analysis of the effects on mean birthweight into those trials in which the majority of women had low pre-pregnancy (or early pregnancy) weight (Ceesay 1997; Girija 1984; Kardjati 1988; Mora 1978; Rush 1980), and those in which the participants appeared adequately nourished (Elwood 1981; Ross 1985; Viegas 1982a). For the Taiwan trial (Blackwell 1973) and (Huybregts 2009; Viegas 1982b), within-trial stratification was possible, based on data contained in the published reports. Because growth varies with differences in sex (Onis 2007), it is desirable to compare growth between groups after adjusting for variations by sex. We conducted subgroup analysis separated by sexes for follow-up results of balanced protein and energy supplementation at the age of 11 to 17 years (height, weight, systolic blood pressure, diastolic blood pressure, BMI z-score, and body fat).

* Indicates the major publication for the study

References

References to studies included in this review

  1. Top of page
  2. AbstractRésumé scientifiqueアブストラクト
  3. Summary of findings
  4. Background
  5. Objectives
  6. Methods
  7. Results
  8. Discussion
  9. Authors' conclusions
  10. Acknowledgements
  11. Data and analyses
  12. Appendices
  13. What's new
  14. History
  15. Contributions of authors
  16. Declarations of interest
  17. Sources of support
  18. Differences between protocol and review
  19. Characteristics of studies
  20. References to studies included in this review
  21. References to studies excluded from this review
  22. References to studies awaiting assessment
  23. References to ongoing studies
  24. Additional references
  25. References to other published versions of this review
Blackwell 1973 {published data only}
  • Adair LS, Pollitt E. Outcome of maternal nutritional supplementation: a comprehensive review of the Bacon Chow Study. American Journal of Clinical Nutrition 1985;41:948-78.
  • Adair LS, Pollitt E, Mueller WH. The Bacon Chow Study: effect of nutritional supplementation on maternal weight and skinfold thickness during pregnancy and lactation. British Journal of Nutrition 1984;51:357-69.
  • Blackwell RQ, Chow BF, Chinn KSK, Blackwell BN, Hsu SC. Prospective maternal nutrition study in Taiwan: rationale, study design, feasibility and preliminary findings. Nutrition Reports International 1973;7:517-32.
  • Joos SK, Pollitt E, Mueller WH, Albright DL. The Bacon Chow Study: maternal nutritional supplementation and infant behavioral development. Child Development 1983;54:669-76.
  • McDonald EC, Pollitt E, Mueller W, Hsueh AM, Sherwin R. The Bacon Chow study: maternal nutritional supplementation and birth weight of offspring. American Journal of Clinical Nutrition 1981;34:2133-44.
  • Mueller WH, Pollitt E. The Bacon Chow study: effects of maternal nutritional supplementation on birth measurements of children, accounting for the size of a previous (unsupplemented) child. Early Human Development 1984;10:127-36.
  • Mueller WH, Pollitt E. The Bacon Chow Study: effects of nutrition supplementation on sibling-sibling anthropometric correlations. Human Biology 1982;54:455-68.
  • Pollitt E, Mueller W. Maternal nutrition supplementation during pregnancy interferes with physical resemblance of siblings at birth according to infant sex. Early Human Development 1982;7:251-6.
  • Wohlleb JC, Pollitt E, Mueller WH, Bigelow R. The Bacon Chow Study: maternal supplementation and infant growth. Early Human Development 1983;9:79-91.
Briley 2002 {published data only}
  • Briley C, Flanagan NL, Lewis NM. In-home prenatal nutrition intervention increased dietary iron intakes and reduced low birthweight in low-income African-American women. Journal of the American Dietetic Association 2002;102(7):984-7.
Ceesay 1997 {published data only}
  • Ceesay SM, Saidykhan S, Prentice AM, Cole TJ, Day KC, Rowland MGM, et al. Effect on birth weight of a community-based supplementation programme for pregnant Gambian women: first year results. Proceedings of the Nutrition Society 1992;51:77A.
  • Ceesay SN, Prentice AM, Cole TJ, Foord F, Weaver LT, Poskitt EME, et al. Effects on birth weight and perinatal mortality of maternal dietary supplements in rural Gambia: 5 year randomised controlled trial. BMJ 1997;315:786-90.
  • Hawkesworth S, Prentice AM, Fulford AJ, Moore SE. Dietary supplementation of rural Gambian women during pregnancy does not affect body composition in offspring at 11-17 years of age. Journal of Nutrition 2008;138(12):2468-73.
  • Hawkesworth S, Prentice AM, Fulford AJ, Moore SE. Maternal protein-energy supplementation does not affect adolescent blood pressure in The Gambia. International Journal of Epidemiology 2009;38(1):119-27.
  • Moore SE, Collinson AC, Prentice AM. Immune function in rural Gambian children is not related to season of birth, birth size, or maternal supplementation status. American Journal of Clinical Nutrition 2001;74:840-7.
Elwood 1981 {published and unpublished data}
  • Ben-Shlomo Y, Holly J, McCarthy A, Savage P, Davies D, Davey Smith G. Prenatal and postnatal milk supplementation and adult insulin-like growth factor I: long-term follow-up of a randomized controlled trial. Cancer Epidemiology, Biomarkers & Prevention 2005;14(5):1336-9.
  • Ben-Shlomo Y, McCarthy A, Hughes R, Tilling K, Davies D, Smith GD. Immediate postnatal growth is associated with blood pressure in young adulthood: the Barry Caerphilly growth study. Hypertension 2008;52:638-44.
  • Elwood PC, Haley TJL, Hughes SJ, Sweetnam PM, Gray OP, Davies DP. Child growth (0-5 years), and the effect of entitlement to a milk supplement. Archives of Disease in Childhood 1981;56:831-5.
Girija 1984 {published and unpublished data}
Hunt 1976 {published data only}
  • Hunt IF, Jacob M, Ostergard NJ, Masri G, Clark VA, Coulson AH. Effect of nutrition education on the nutritional status of low-income pregnant women of Mexican descent. American Journal of Clinical Nutrition 1976;29:675-84.
Huybregts 2009 {published data only}
  • Huybregts L, Roberfroid D, Lanou H, Menten J, Meda N, Van Camp J, et al. Prenatal food supplementation fortified with multiple micronutrients increases birth length: a randomized controlled trial in rural Burkina Faso. American Journal of Clinical Nutrition 2009;90(6):1593-600.
Kafatos 1989 {published and unpublished data}
  • Kafatos AG, Vlachonikolis IG, Codrington CA. Nutrition during pregnancy: the effects of an educational intervention program in Greece. American Journal of Clinical Nutrition 1989;50:970-9.
Kardjati 1988 {published data only}
  • Kardjati S, Kusin JA, De With C. Energy supplementation in the last trimester of pregnancy in East Java: I. Effect on birthweight. British Journal of Obstetrics and Gynaecology 1988;95:783-94.
  • Kardjati S, Kusin JA, Schofield WM, De With C. Energy supplementation in the last trimester of pregnancy in East Java, Indonesia: effect on maternal anthropometry. American Journal of Clinical Nutrition 1990;52:987-94.
  • Kusin JA, Kardjati S, Houtkooper JM, Renqvist UH. Energy supplementation during pregnancy and postnatal growth. Lancet 1992;340:623-6.
  • Van Steenbergen WM, Kusin JA, Kardjati S, De With C. Energy supplementation in the last trimester of pregnancy in East Java, Indonesia: effect on breast-milk output. American Journal of Clinical Nutrition 1989;50:274-9.
Mora 1978 {published data only}
  • Christiansen N, Mora JO, Navarro L, Herrera MG. Effects of nutritional supplementation during pregnancy upon birth weight: the influence of pre-supplementation on diet. Nutrition Reports International 1980;21:615-24.
  • Herrera MG, Mora JO, De Paredes B, Wagner M. Maternal weight/height and the effect of food supplementation during pregnancy and lactation. Maternal nutrition during pregnancy and lactation. A Nestlé Foundation workshop; 1979 April 26-27; Lausanne, Switzerland. Bern: Hans Huber, 1980:252-63.
  • Mora JO, Clement J, Christiansen N, Suescun J, Wagner M, Herrera MG. Nutritional supplementation and the outcome of pregnancy. III. Perinatal and neonatal mortality. Nutrition Reports International 1978;18:167-75.
  • Mora JO, De Navarro L, Clement J, Wagner M, De Paredes B, Herrera MG. The effect of nutritional supplementation on calorie and protein intake of pregnant women. Nutrition Reports International 1978;17:217-28.
  • Mora JO, De Paredes B, Wagner M, De Navarro L, Suescun J, Christiansen N, et al. Nutritional supplementation and the outcome of pregnancy. I. Birth weight. American Journal of Clinical Nutrition 1979;32:455-62.
  • Mora JO, Herrera MG, Suescun J, De Navarro L, Wagner M. The effects of nutritional supplementation on physical growth of children at risk of malnutrition. American Journal of Clinical Nutrition 1981;34:1885-92.
  • Mora JO, Sanchez R, De Paredes B, Herrera MG. Sex related effects of nutritional supplementation during pregnancy on fetal growth. Early Human Development 1981;5:243-51.
  • Overholt C, Sellers SG, Mora JO, de Paredes B, Herrera MG. The effects of nutritional supplementation on the diets of low-income families at risk of malnutrition. American Journal of Clinical Nutrition 1982;36:1153-61.
  • Vuori L, Christiansen N, Clement J, Mora JO, Wagner M, Herrera MG. Nutritional supplementation and the outcome of pregnancy. II. Visual habituation at 15 days. American Journal of Clinical Nutrition 1979;32:463-9.
  • Vuori L, De Navarro L, Christiansen N, Mora JO, Herrera MG. Food supplementation of pregnant women at risk of malnutrition and their newborns' responsiveness to stimulation. Developmental Medicine and Child Neurology 1980;22:61-71.
  • Waber DP, Vuori-Christiansen L, Ortiz N, Clement JR, Christiansen NE, Mora JO, et al. Nutritional supplementation, maternal education, and cognitive development of infants at risk of malnutrition. American Journal of Clinical Nutrition 1981;34:807-13.
Ross 1985 {published data only}
Rush 1980 {published and unpublished data}
  • Jacobson HN. A randomized controlled trial of prenatal nutritional supplementation. Pediatrics 1980;65:835-6.
  • Pereira M, Rush D, Campbell-Brown M, Rosso P, Winick M, Brasel JA, et al. Effects of prenatal nutritional supplementation on the placenta: report of a randomized controlled trial. American Journal of Clinical Nutrition 1982;36:229-34.
  • Rush D, Kristal A, Blanc W, Navarro C, Chauham P, Campbell-Brown M, et al. The effects of maternal cigarette smoking on placental morphology, histomorphometry, and biochemistry. American Journal of Perinatology 1986;3:263-72.
  • Rush D, Kristal A, Navarro C, Chauhan P, Blanc W, Naeye R, et al. The effects of dietary supplementation during pregnancy on placental morphology, pathology, and histomorphometry. American Journal of Clinical Nutrition 1984;39:863-71.
  • Rush D, Stein Z, Susser, M. The rationale for, and design of, a randomized controlled trial of nutritional supplementation in pregnancy. Nutrition Reports International 1973;7:547-53.
  • Rush D, Stein Z, Susser M. A randomized controlled trial of prenatal nutritional supplementation in New York City. Pediatrics 1980;65:683-97.
  • Rush D, Stein Z, Susser M. Controlled trial of prenatal nutrition supplementation defended. Pediatrics 1980;66:656-8.
  • Rush D, Stein Z, Susser M. Diet in pregnancy: a randomized controlled trial of nutritional supplements. Birth Defects 1980;16:1-187.
  • Stein Z, Susser M, Rush D. Prenatal nutrition and birth weight: experiments and quasi-experiments in the past decade. Journal of Reproductive Medicine 1978;21:287-97.
Sweeney 1985 {published data only}
Viegas 1982a {published data only}
  • Viegas OAC, Scott PH, Cole TJ, Mansfield HN, Wharton P, Wharton BA. Dietary protein energy supplementation of pregnant Asian mothers at Sorrento, Birmingham. I. Unselective during second and third trimesters. BMJ 1982;285:589-92.
Viegas 1982b {published data only}
  • Viegas OAC, Scott PH, Cole TJ, Eaton P, Needham PG, Wharton BA. Dietary protein energy supplementation of pregnant Asian mothers at Sorrento, Birmingham. II. Selective during third trimester only. BMJ 1982;285:592-5.

References to studies excluded from this review

  1. Top of page
  2. AbstractRésumé scientifiqueアブストラクト
  3. Summary of findings
  4. Background
  5. Objectives
  6. Methods
  7. Results
  8. Discussion
  9. Authors' conclusions
  10. Acknowledgements
  11. Data and analyses
  12. Appendices
  13. What's new
  14. History
  15. Contributions of authors
  16. Declarations of interest
  17. Sources of support
  18. Differences between protocol and review
  19. Characteristics of studies
  20. References to studies included in this review
  21. References to studies excluded from this review
  22. References to studies awaiting assessment
  23. References to ongoing studies
  24. Additional references
  25. References to other published versions of this review
Aaltonen 2005 {published data only}
  • Aaltonen J, Ojala T, Laitinen K, Isolauri E. Programming of infants systolic blood pressure by accelerated foetal growth during early pregnancy. Journal of Pediatric Gastroenterology and Nutrition 2005;40(5):624.
  • Aaltonen J, Ojala T, Laitinen K, Pirainen TJ, Poussa TA, Isolauri E. Evidence of infant blood pressure programming by maternal nutrition during pregnancy: a prospective randomized controlled intervention study. Journal of Pediatrics 2008;152:79-84.
  • Aaltonen J, Ojala T, Laitinen K, Poussa T, Ozanne S, Isolauri E. Impact of maternal diet during pregnancy and breastfeeding on infant metabolic programming: a prospective randomized controlled study. European Journal of Clinical Nutrition 2011;65(1):10-9.
  • Huurre A, Laitinen K, Rautava S, Korkeamaki M, Isolauri E. Impact of maternal atopy and probiotic supplementation during pregnancy on infant sensitization: a double-blind placebo-controlled study. Clinical and Experimental Allergy 2008;38(8):1342-8.
  • Isolauri E. The effects of maternal nutrition during pregnancy and breast feeding on the risk of allergic disease in child (NAMI). ClinicalTrials.gov (http://clinicaltrials.gov/) (accessed 6 Nov 2007).
  • Laitinen K,  Poussa T,  Isolauri E,  Nutrition, Allergy, Mucosal Immunology and Intestinal Microbiota Group. Probiotics and dietary counselling contribute to glucose regulation during and after pregnancy: a randomised controlled trial. British Journal of Nutrition 2009;101:1679–87.
  • Luoto R, Laitinen K, Nermes M, Isolauri E. Impact of maternal probiotic-supplemented dietary counselling on pregnancy outcome and prenatal and postnatal growth: a double-blind, placebo-controlled study. British Journal of Nutrition 2010;103(12):1792-9.
  • Luoto R, Nermes M, Laitinen K, Isolauri E. Impact of maternal probiotic-supplemented dietary counselling on pregnancy outcome and prenatal and postnatal growth: a double-blind, placebo-controlled study. Pediatric Academic Societies Annual Meeting; 2009 May 2-5; Baltimore, USA. 2009.
  • Piirainen T, Isolauri E, Lagstrom H, Laitinen K. Impact of dietary counselling on nutrient intake during pregnancy: a prospective cohort study. British Journal of Nutrition 2006;96:1095-104.
Adams 1978 {published data only}
Anderson 1995 {published data only}
Atton 1990 {published data only}
Badrawi 1993 {published data only}
  • Badrawi H, Hassanein MK, Badraoui MHH, Wafa YA, Shawky HA, Badrawi N. Pregnancy outcome in obese pregnant mothers. Journal of Perinatal Medicine 1992;20(Suppl 1):203.
  • Badrawi H, Hassanein MK, Badrroui MHH, Wafa YA, Shawky HA, Badrawi N. Pregnancy outcome in obese pregnant mothers. New Egypt Journal of Medicine 1993;8(6):1717-26.
Campbell 1975 {published data only}
Campbell 1983 {published data only}
  • Campbell DM. Dietary restriction in obesity and its effect on neonatal outcome. Nutrition in pregnancy. Proceedings of 10th Study Group of the RCOG; 1983; London, UK. London: RCOG, 1983:243-50.
Campbell Brown 1983 {published data only}
  • Campbell Brown M. Protein energy supplements in primigravid women at risk of low birthweight.. In: Campbell DM, Gillmer MDG editor(s). Nutrition in pregnancy. Proceedings of the 10th Study Group of the RCOG. London: RCOG, 1983:85-98.
Clapp 1997 {published data only}
  • Clapp JF. Diet, exercise, and feto-placental growth. Archives of Gynecology and Obstetrics 1997;260:101-8.
  • Clapp JF. Effects of dietary carbohydrate on the glucose and insulin response to mixed caloric intake and exercise in both nonpregnant and pregnant women. Diabetes Care 1998;21(Suppl 2):B107-B112.
Dirige 1987 {published data only}
  • Dirige OV, McNutt SW, Hamatake CK, McGee RI, Manayan CA. The effect of nutrition education on the nutritional status of pregnant Filipino women in Hawaii. Nutrition Research 1987;7:197-209.
Ebbs 1941 {published data only}
  • Ebbs JH, Scott WA, Tisdall FF, Moyle WJ, Bell M. Nutrition in pregnancy. Canadian Medical Association Journal 1942;46:1-6.
  • Ebbs JH, Tisdall FF, Scott WA. The influence of prenatal diet on the mother and child. Journal of Nutrition 1941;22:515-6.
Eneroth 2010 {published data only}
  • Eneroth H, El Arifeen S, Persson LA, Lonnerdal B, Hossain MB, Stephensen CB, et al. Maternal multiple micronutrient supplementation has limited impact on micronutrient status of Bangladeshi infants compared with standard iron and folic acid supplementation. Journal of Nutrition 2010;140(3):618-24.
Fard 2004 {published data only}
  • Fard NM, Mehrabian F, Sarraf-zadegan N, Sajadi F. Fat-modified diets during pregnancy and lactation and serum lipids after birth. Indian Journal of Pediatrics 2004;71:683-7.
Fung 2010 {published data only}
  • Fung EB, Ritchie LD, Walker BH, Gildengorin G, Crawford PB. Randomized, controlled trial to examine the impact of providing yogurt to women enrolled in WIC. Journal of Nutrition Education and Behavior 2010;42(3 Suppl):S22-29.
Guelinckx 2010 {published data only}
  • Guelinckx I, Devlieger R, Mullie P, Vansant G. Effect of lifestyle intervention on dietary habits, physical activity, and gestational weight gain in obese pregnant women: a randomized controlled trial. American Journal of Clinical Nutrition 2010;91(2):373-80.
Hankin 1962 {published data only}
  • Hankin ME, Symonds EM. Body weight, diet and pre-eclamptic toxaemia of pregnancy. Australian and New Zealand Journal of Obstetrics and Gynaecology 1962;4:156-60.
Iyengar 1967 {published data only}
  • Iyengar L. Effects of dietary supplements late in pregnancy on the expectant mother and her newborn. Indian Journal of Medical Research 1967;55:85-9.
Kaseb 2002 {published data only}
  • Kaseb F, Kimiagar M, Ghafarpoor M, Valaii N. Effect of traditional food supplementation during pregnancy on maternal weight gain and birthweight. International Journal for Vitamin & Nutrition Research 2002;72(6):389-93.
Kinra 2008 {published data only}
  • Kinra S, Rameshwar Sarma KV, Ghafoorunissa, Mendu VV, Ravikumar R, et al. Effect of integration of supplemental nutrition with public health programmes in pregnancy and early childhood on cardiovascular risk in rural Indian adolescents: long term follow-up of hyderabad nutrition trial. BMJ 2008;337:a605.
Lechtig 1975 {published data only}
  • Behrman JR, Calderon MC, Preston SH, Hoddinott J, Martorell R, Stein AD. Nutritional supplementation in girls influences the growth of their children: prospective study in Guatemala. American Journal of Clinical Nutrition 2009;90(5):1372-9.
  • Conlisk AJ, Barnhart HX, Martorell R, Grajeda R, Stein AD. Maternal and child nutritional supplementation are inversely associated with fasting plasma glucose concentration in young Guatemalan adults. Journal of Nutrition 2004;134(4):890-7.
  • Delgado H, Martorell R, Brineman E, Klein RE. Nutrition and length of gestation. Nutrition Research 1982;2:117-26.
  • Delgado HL, Martorell R, Klein RE. Nutrition, lactation, and birth interval components in rural Guatemala. American Journal of Clinical Nutrition 1982;35:1468-76.
  • Hoddinott J, Maluccio JA, Behrman JR, Flores R, Martorell R. Effect of a nutrition intervention during early childhood on economic productivity in Guatemalan adults. Lancet 2008;371(9610):411-6.
  • Lechtig A, Habicht JP, Delgado H, Klein RE, Yarbrough C, Martorell R. Effect of food supplementation during pregnancy on birthweight. Pediatrics 1975;56:508-20.
  • Lechtig A, Klein RE, Daza CH, Read MS, Kahn SG. Effects of maternal nutrition on infant health: implications for action. Archivos Latinoamericanos de Nutricion 1979;29:1-26.
  • Lechtig A, Yarbrough C, Delgado H, Martorell R, Klein RE, Behar M. Effect of moderate maternal malnutrition on the placenta. American Journal of Obstetrics and Gynecology 1975;123:191-201.
  • Merchant K, Martorell R, Haas J. Maternal and fetal responses to the stresses of lactation concurrent with pregnancy and of short recuperative intervals. American Journal of Clinical Nutrition 1990;52:280-8.
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Luke 2001 {published data only}
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Mardones 1988 {published and unpublished data}
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Metcoff 1985 {published and unpublished data}
  • Metcoff J, Costiloe P, Crosby WM, Dutta S, Sandstead H, Milne D, et al. Effects of WIC supplement on maternal nutritional status between 19 and 36 weeks pregnancy. American Journal of Clinical Nutrition 1983;37:703.
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Moses 2006 {published data only}
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Qureshi 1973 {published data only}
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Tompkins 1954 {published data only}
Tontisirin 1986 {published data only}
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Wolff 2008 {published data only}
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Woods 1995 {published data only}
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References to studies awaiting assessment

  1. Top of page
  2. AbstractRésumé scientifiqueアブストラクト
  3. Summary of findings
  4. Background
  5. Objectives
  6. Methods
  7. Results
  8. Discussion
  9. Authors' conclusions
  10. Acknowledgements
  11. Data and analyses
  12. Appendices
  13. What's new
  14. History
  15. Contributions of authors
  16. Declarations of interest
  17. Sources of support
  18. Differences between protocol and review
  19. Characteristics of studies
  20. References to studies included in this review
  21. References to studies excluded from this review
  22. References to studies awaiting assessment
  23. References to ongoing studies
  24. Additional references
  25. References to other published versions of this review
Hawkesworth 2011 {published data only}
  • Hawkesworth S, Walker CG, Sawo Y, Fulford AJ, Jarjou LM, Goldberg GR, et al. Nutritional supplementation during pregnancy and offspring cardiovascular disease risk in The Gambia. American Journal of Clinical Nutrition 2011;94(6 Suppl):1853S-60S.
Kinra 2011 {published data only}
  • Kinra S, Sarma KV, Hards M, Smith GD, Ben-Shlomo Y. Is relative leg length a biomarker of childhood nutrition? Long-term follow-up of the Hyderabad Nutrition Trial. International Journal of Epidemiology 2011;40(4):1022-9.
Walsh 2012 {published data only}
  • Walsh J, Mahony R, Foley M, McAuliffe F. ROLO study: a randomized control trial of low glycemic index diet to prevent macrosomia in euglycemic women. American Journal of Obstetrics and Gynecology 2012;206(Suppl 1):S4.

Additional references

  1. Top of page
  2. AbstractRésumé scientifiqueアブストラクト
  3. Summary of findings
  4. Background
  5. Objectives
  6. Methods
  7. Results
  8. Discussion
  9. Authors' conclusions
  10. Acknowledgements
  11. Data and analyses
  12. Appendices
  13. What's new
  14. History
  15. Contributions of authors
  16. Declarations of interest
  17. Sources of support
  18. Differences between protocol and review
  19. Characteristics of studies
  20. References to studies included in this review
  21. References to studies excluded from this review
  22. References to studies awaiting assessment
  23. References to ongoing studies
  24. Additional references
  25. References to other published versions of this review
Aaltonen 2011
  • Aaltonen J, Ojala T, Laitinen K, Poussa T, Ozanne S, Isolauri E. Impact of maternal diet during pregnancy and breastfeeding on infant metabolic programming: a prospective randomized controlled study. European Journal of Clinical Nutrition 2011;65(1):10-9.
Ashworth 1998
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Barker 1998
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Barker 2002
  • Barker DJP,  Eriksson JG,  Forsén T,  Osmond C . Fetal origins of adult disease: strength of effects and biological basis. International Journal of Epidemiology 2002;31:1235–9.
Behrman 2009
  • Behrman JR, Calderon MC, Preston SH, Hoddinott J, Martorell R, Stein AD. Nutritional supplementation in girls influences the growth of their children: prospective study in Guatemala. American Journal of Clinical Nutrition 2009;90(5):1372-9.
Chen 2009
de Onis 1998
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Egger 1997
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Eriksson 2001
Garlick 2000
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Guyatt 2008
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Harbord 2006
Haslehurst 2006
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Higgins 2011
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Imdad 2011
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IOM 1990
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Kardjati 1983
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Kramer 1987
Kulier 1998
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Laitinen 2009
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Prentice 1983
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Rasmussen 2010
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Thangaratinam 2012
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References to other published versions of this review

  1. Top of page
  2. AbstractRésumé scientifiqueアブストラクト
  3. Summary of findings
  4. Background
  5. Objectives
  6. Methods
  7. Results
  8. Discussion
  9. Authors' conclusions
  10. Acknowledgements
  11. Data and analyses
  12. Appendices
  13. What's new
  14. History
  15. Contributions of authors
  16. Declarations of interest
  17. Sources of support
  18. Differences between protocol and review
  19. Characteristics of studies
  20. References to studies included in this review
  21. References to studies excluded from this review
  22. References to studies awaiting assessment
  23. References to ongoing studies
  24. Additional references
  25. References to other published versions of this review
CDSR 1996a
  • Kramer MS. Energy/protein restriction for high weight-for-height or weight gain during pregnancy. Cochrane Database of Systematic Reviews 1996, Issue 3. [DOI: 10.1002/14651858.CD000080]
CDSR 1996b
  • Kramer MS. High protein supplementation in pregnancy. Cochrane Database of Systematic Reviews 1996, Issue 4. [DOI: 10.1002/14651858.CD000105]
CDSR 1996c
  • Kramer MS. Isocaloric balanced protein supplementation in pregnancy. Cochrane Database of Systematic Reviews 1996, Issue 4. [DOI: 10.1002/14651858.CD000118]
CDSR 1996d
Kramer 2003
  • Kramer MS,  Kakuma R. Energy and protein intake in pregnancy. Cochrane Database of Systematic Reviews 2003, Issue 4. [DOI: 10.1002/14651858.CD000032]