Maternal and Infant Health Outcomes Associated with Medical Nutrition Therapy by Registered Dietitian Nutritionists in Pregnant Women with Malnutrition: An Evidence Analysis Center Systematic Review

FROM THE ACADEMY Evidence Analysis Center

Maternal and Infant Health Outcomes Associated with Medical Nutrition Therapy by Registered Dietitian Nutritionists in Pregnant Women with Malnutrition: An Evidence Analysis Center Systematic Review Maria Pari-Keener, MS, RDN, CDN; Sina Gallo, PhD, MSc, RDN; Barbara Stahnke, MEd, RDN, LD; Joann M. McDermid, MSc, PhD, RDN, FAND; Rima Itani Al-Nimr, MS, RDN, LD; Julie M. Moreschi, MS, RDN, LDN; Rubina Hakeem, PhD, RDN, FAND, FAfN; Deepa Handu, PhD, RDN, LDN; Feon W. Cheng, PhD, MPH, RDN, CHTS-CP ABSTRACT Malnutrition during the critical period of pregnancy has significant health outcomes for both the mother and her offspring. Medical nutrition therapy (MNT) by a registered dietitian nutritionist (RDN) may help mitigate negative health effects, although studies that support the role of the RDN have not been comprehensively evaluated. The objective was to explore the health effects of MNT by an RDN on maternal and infant outcomes in pregnant women with malnutrition. A systematic review of studies published between 2000 and 2014 that incorporated MNT by an RDN during pregnancy were retrieved from a PubMed search, using criteria established by the Academy of Nutrition and Dietetics Evidence Analysis Process. Among 94 identified studies, five controlled trials met the inclusion criteria. The initial search was extended to include one study published between 2014 and 2019. Outcomes included maternal gestational weight gain, maternal markers of glycemic control, maternal complications such as hypertension, incidence of caesarean section, infant birth weight both in grams and in clinical categories, infant gestational age, and infant complications. There was good/strong evidence that MNT by an RDN decreased gestational weight gain, although there was no effect on maternal complications, caesarean section deliveries, and gestational age among women with mixed body mass index status or those who were overweight/obese. The evidence was deemed fair in support of an effect on glycemic control, infant birth weight, and infant complications. The heterogeneity in the results are due to the variation among populations studied, types of interventions, and inconsistency among outcomes. In addition, the training and educational requirements of the RDN or the international equivalent may vary widely across the four countries in which studies were conducted. There was good evidence for MNT by an RDN during pregnancy on improving gestational weight gain among overweight/obese women. To better support the role of MNT by an RDN in the health care of pregnant women, research that clearly identifies the role of the RDN in the intervention, includes a control group, and studies more heterogeneous populations is needed. J Acad Nutr Diet. 2020;-(-):---.

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HE FIRST 1,000 DAYS OF LIFE IS the critical period from conception to age 2 and, as recognized by the United Nations Children’s Fund, is when the foundations of optimum health, growth, and neurodevelopment across the life span are established.1 Fetal programming, which occurs during the early period of embryonic and fetal development, may determine susceptibility to adult disease. Programming is the result of adaptations initiated when the materno-placental nutrient 2212-2672/Copyright ª 2020 by the Academy of Nutrition and Dietetics. https://doi.org/10.1016/j.jand.2019.10.024

ª 2020 by the Academy of Nutrition and Dietetics.

supply fails to match the fetal nutrient demand.2 Hence, environmental insults as a result of maternal malnutrition during this time may affect the first 1,000 days of life. As both undernutrition and overnutrition during fetal development can produce similar abnormalities in offspring,3 malnutrition has been broadly defined using both these terms for the purpose of this review. Rates of undernutrition in pregnancy are considerable, especially in lowincome and middle-income countries, where more than one third of child deaths can be attributed to maternal and child undernutrition.4 Stunting, severe wasting, intrauterine growth restriction, or prenatal nutrient

deficiencies were responsible for 2.2 million deaths and 21% of disabilityadjusted life-years for children younger than 5 years.4 Short maternal stature, a well-known indicator of malnutrition, is responsible for approximately 6.5 million small-forgestational-age neonates and/or preterm births in low- and middle-income countries.5 Becoming increasingly more common is overnutrition, defined as the intake of excess calories of poor quality causing overweight and obesity, which is also a risk factor for adverse maternal and infant outcomes.6-8 Excessive gestational weight gain (GWG) is associated with a risk of twoto threefold excess weight retention for pregnant women after birth.9 Excessive

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FROM THE ACADEMY pregnancy weight gain can lead to increased likelihood of preeclampsia, cesarean section, and gestational diabetes mellitus (GDM).10-12 Beyond the health risks to the mother, it has been shown that women who gained weight in excess of recommendations have offspring with more adipose tissue and higher risk of cardiovascular disease.13 Those women are also at risk for preterm birth, large-for-gestational-age (LGA) neonates, and structural birth defects.14,15 Educational interventions during pregnancy can help mitigate malnutrition and associated health risks. A Cochrane review of antenatal dietary education to help increase protein and energy intake found pregnant women who received nutritional education had a lower risk of preterm birth and infant low birth weight.16 A Romanian study found nutritional education was associated with an appropriate GWG in 44.3% of women, compared with 40.7% among women who did not receive advice.17 A meta-analysis of 39 studies found that antenatal dietary interventions in obese pregnant women can reduce maternal GWG without affecting infant birth weight.18 Registered dietitian nutritionists (RDNs) are uniquely qualified to provide medical nutrition therapy (MNT) services due to their specialized education and training.19 However, studies that support the role of RDNs to affect change in pregnant women have not been comprehensively evaluated. Well-designed and executed randomized controlled trials generally provide the strongest evidence, and therefore the purpose of this systematic review of eligible controlled trials is to evaluate maternal and infant outcomes affected by MNT with an RDN among pregnant women with malnutrition.

METHODS Evidence Analysis Team and Process The workgroup consisted of experts across research, public health, and clinical practice. A complete description of the Academy of Nutrition and Dietetics’ Evidence Analysis Library (EAL) process has been published.20 Briefly, the search results were first

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screened by the lead analyst for relevancy. The relevant articles were then assigned to two workgroup members who independently evaluated them for inclusion. The EAL analysts extracted data from the included articles using the EAL Data Extraction Tool. Both the analysts and lead analyst independently evaluated the quality of the included studies using the Quality Criteria Checklist.20 The checklist includes 10 domains on scientific soundness and rates studies as positive, negative, or neutral. Any discrepancies were further evaluated by a third reviewer. Once data extraction was completed, the lead analysts, along with the workgroup members, developed the evidence summary table and narrative.

Literature Search and Application of Inclusion and Exclusion Criteria Studies meeting the eligibility criteria included human studies that were published in English from 2000 to 2014 and reported the effects of MNT by an RDN on maternal and infant health outcomes. A comprehensive search of PubMed was conducted, and the following search term combinations were used: “Pregnancy”[MeSH] AND ((“obesity”[MeSH Terms] OR “obesity”[All Fields]) OR (“malnutrition”[MeSH Terms] OR “malnutrition”[All Fields])) AND “diet therapy”[Subheading] NOT (“review”[Publication Type] OR “review literature as topic”[MeSH Terms] OR “review”[All Fields]). Additional a priori inclusion criteria were mean maternal age between 15 and 55 years of age (nonadolescent or older women), randomized controlled trials or clinical controlled studies, a minimum of 10 participants per group or arm in the study, and a dropout rate of less than 30% (previous reviews used 20%, but a higher rate was adopted due to longer follow-up required during pregnancy and neonatal period). Outcomes were identified based on the studies with available outcome data, in combination with considerations for the outcomes’ relative importance in the field. The outcomes of interest were GWG, markers of glycemic control (ie, glucose, oral glucose tolerance test [OGTT], insulin use), maternal

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complications (ie, GDM, hypertensive disorders of pregnancy [preeclampsia or eclampsia, hypertension], cesarean section, birth weight in grams, birth weight in clinical categories, preterm delivery and gestational age) and infant illnesses or complications (ie, perinatal mortality, neonatal intensive care unit [NICU] admissions, congenital malformations rate). Articles were excluded from consideration if it was not clear that an RDN or international equivalent21 was involved in the intervention, if the participants were outside the specified age range, if the studies were noncontrolled studies or observational designs or did not include outcomes of interest, or if the article appeared in non-peer-reviewed journals. Because no consistent definition of malnutrition in pregnancy exists, malnutrition was defined as a state of nutritional imbalance in calories, macronutrients, vitamins, or minerals and only studies that included a malnutrition condition (as identified by anthropometric, biochemical, clinical, dietary, or other) in the target population were reported.

Development of Conclusion Statements The workgroup employed the standard EAL methodology to create its conclusion statements20 and considered five main elements (ie, quality, consistency, quantity, clinical impact, and generalizability) when grading the evidence. The five possible grades were as follows: grade I (good or strong), grade II (fair), grade III (limited or weak), grade IV (expert opinion only), or grade V (grade not assignable).22

RESULTS Research Reviewed Of the 94 records, five studies met the inclusion criteria (Figure). There were three positive-quality23-25 and one neutral-quality26 randomized controlled trials and one positive-quality nonrandomized quasi-controlled trial.27 A detailed description of each trial is shown in Table 1. All studies compared a control group with routine prenatal care to intervention groups with various methods of counseling by an RDN. Two studies25,26 were conducted in the United States, one study24 was conducted in Europe, one study23 was

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0 additional records identified through other sources

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94 records identified through database searching

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94 records screened

94 full-text articles assessed for eligibility

Included

5 studies included in qualitative synthesis

0 records excluded

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89 full-text articles excluded Not study design of interest (eg, review, case study, comment) (n=26) Ineligible population (n=8) Dropout rate over 30% (n=1) Did not include exposures or comparator of interest (n=50) Did not include outcomes of interest (n=4)

Figure. Search strategy flow diagram for literature examining the health outcomes associated with medical nutrition therapy by a registered dietitian nutritionist or international equivalent in pregnant women with malnutrition.

conducted in Australia, and one study25 was conducted in Mexico. Four studies23-26 included overweight or obese women, and one study27 focused on women with GDM or diabetes mellitus (DM). Interventions all included dietary advice provided by an RDN but the nature of the interventions varied widely including providing

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standardized dietary and physical activity recommendations,26 two sessions with an RDN plus telephone calls by trained people,23 intensive MNT,27 individualized plans plus group therapy,25and physical activity plus low-fat Mediterranean diet instructions.24 Control groups ranged from standard prenatal care,23,24,26 one visit with an

RDN,27 or medical records of women who completed groups sessions.25 Duration of MNT ranged from 11 weeks27 to 29 weeks.24

Maternal Outcomes Gestational Weight Gain. There was consistent evidence in three studies24-26

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Author(s), year; PMIDc; study design; quality

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Asbee and colleagues, 200926 PMID 19155899 Randomized controlled trial Rating: neutral

USA

n¼100; age: control group: 26.45 y, MNT group: 26.76 y; BMId: control group: 25.65.1, MNT group: 25.56; pregnant women (6-16 wk gestation) without major comorbidity (eg, preexisting diabetes; BMI>40); singleton pregnancy

Control group (n¼43): Routine prenatal care MNT intervention group (n¼ 57): RDN provided standardized prenatal dietary counseling based on 40, 30, 30 macronutrients along with exercise recommendations and guidance on weight gain at the initial visit only. F/ue visits were with MDf or NPg (at regular prenatal visits) who provided standardized encouragement based on weight gain per IOMh guidelines. Duration: initial to delivery (6-16 wk gestation at baseline)

Maternal gestational weight gain: Compared with control group, MNT intervention group had significantly less weight gain (13.055.68 kg vs 16.187.05 kg; P¼0.01). Maternal complications: No significant differences in preeclampsia and gestational diabetes were observed between groups (values not provided; P>0.05). Maternal cesarean section: The rates of cesarean section were not significantly different between MNT intervention and control groups (14.0% vs 27.9%; P¼0.09).

Dodd and colleagues, 201423 PMID 24513442 Randomized controlled trial Rating: positive

Australia

n¼2,122; age: control group: 29.65.6 y, MNT group: 29.35.4 y old; BMI (median [IQRi]): control group: 31.1 (27.7-35.6), MNT group: 31 (28.1-35.9) entered study at 14.1 wk (range¼11.917.0 wk); overweight or obese at entry (BMI25.0), predominantly white (90.5%), and half (54.3%) were in the bottom two quintiles of socioeconomic disadvantage per Australian Census data); singleton pregnancy

Control group (n¼1,104): Standard prenatal care without dietary, exercise, or prenatal weight gain guidance. MNT intervention group (n¼1,018): Two sessions of intervention with research dietitian at initiation and at 28 wk, with f/u via telephone call by trained assistants at 22, 24, and 32 wk and trained assistant face-to- face visit at 36 wk. Counseling followed Australian diet recommendations as well as walking and increased activity recommendations and behavioral change counseling utilizing Stages of Change. In the intervention group,

Maternal gestational weight gain No significant difference in gestational weight gain between the intervention and control groups (adjusted mean difference¼ 0.04 kg (0.55-0.48; P¼0.89). Maternal complications: No difference in maternal outcomes of hypertension, preeclampsia, gestational diabetes between MNT intervention and control groups (P>0.05). Maternal cesarean section: No difference in cesarean section is noted between control and MNT groups (P¼0.34). (continued on next page)

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Table 1. The evidence for the effects of MNTa by RDNb or international equivalent on maternal and infant health outcomes

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Mexico

n¼194; age (median [range]): control group: 32.3 (19-43) y, MNT group: 32.3 (22-42) y; BMI: N/Al; women with pregestational or gestational diabetes.

Major findings

86.7% and 77.2% attended their initiation and secondary visit (respectively) with the dietitian. Duration: approximately 19.0-24.1 wk (11.9-17.0 wk gestation at baseline)

Infant birth weight: There was no significant difference in large for gestational age between intervention and control groups (ORj 0.90; 95% CI: 0.77-1.07; P¼0.24). However, infants were less likely to weigh >4,000 g with the intervention group at 15% when compared with those in the control group at 19%. The treatment effect for this was OR 0.82, 95% CI: 0.68-0.99, P¼0.04. Infant preterm delivery and gestational age: No differences in preterm delivery were observed between intervention (6%) and control (8%) groups (P¼0.07). Infant illnesses: NICU admission: No difference in admission to NICUk were observed between intervention (37%) and control (36%) groups (P¼0.99). Congenital malformation rate: Similarly, no difference in major congenital anomaly were noted between intervention (2%) and control (1%) groups (P¼0.08).

Control group (n¼86): Medical records of women who saw an endocrinologist and attended only one group nutrition education session. MNT intervention group (n¼ 108): Women received intensive nutritional counseling with a registered dietitian

Maternal markers of glycemic control (glucose, OGTTm, insulin use): Glucose: There were no significant differences in fasting or 2 h postprandial serum glucose during the last outpatient visit between the two groups (P>0.05 for all). Insulin use: No (continued on next page)

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Perichart-Perera and colleagues, 200927 PMID 19696205 Nonrandomized controlled trial (quasi) Rating: positive

Intervention (n[randomized n)

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that included capillary glucose selfmonitoring. Duration: w11 wk (<29 wk gestation at baseline until delivery)

differences in the frequency or amount of insulin usage and were noted between both groups throughout the intervention (P>0.05). Maternal complications: More women in the control group developed preeclampsia than in the MNT group (16.3% vs 2.3%, P¼0.001). Infant birth weight: There were no significant differences in birth weight between control (median: 3,114.94 g; range¼1,740-4,800 g) and MNT intervention (median: 3,010.51 g; range¼1,370-4,350 g) groups (P¼0.24). Although not statistically significant, babies with macrosomia (>4,000 g) were born more frequently in the control group compared with the MNT group (8.5% vs 4.8%, P¼0.36) as were LBWn (<2,500 g) babies, who were also born more frequently in the control group compared with the MNT group (14.6% vs 9.6%, P¼0.45). Infant preterm delivery and gestational age: Age at delivery were similar between control (37.951.93 wk gestation) and MNT intervention (38.201.8 wk gestation) groups (P¼0.34). Similarly, no significant differences were observed in the incidence of prematurity (<37 wk) in control vs MNT groups (15.9% vs 12%, P¼0.63). (continued on next page)

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Table 1. The evidence for the effects of MNTa by RDNb or international equivalent on maternal and infant health outcomes (continued)

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Table 1. The evidence for the effects of MNTa by RDNb or international equivalent on maternal and infant health outcomes (continued)

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Intervention (n[randomized n)

Major findings

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Infant illnesses: NICU admission: More infants born to women in the control group were admitted to NICU compared with the MNT group (51.2% vs 25.9%; P¼0.001). Perinatal death: Intrauterine death was similar for both the control and MNT groups (3.5% vs 3.4%; P¼0.64).

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Renault and colleagues, 201424 PMID 24060449 Randomized controlled trial Rating: positive

Denmark

n¼425; age: control group: 31.34.2 y, MNT-PAo group: 34.14.4; MNT-PAþDp group: 34.44.2 y; BMI: control group: 33.73.5, MNT-PA group: 34.14.4, MNT-PAþD group: 34.44.2; healthy pregnant women in gestational wk 1114 with a prepregnancy BMI of 30

Maternal gestational weight gain: The intervention group PAþD had the least gestational weight gain with a median of 8.6 kg (9.6-34.1) compared with group PA, which had a median of 9.4 kg (3.4-28.2) and control group which had a median of 10.9 kg (4.428.7) (PAþD vs control: P¼0.01), although the difference between PAþD and PA was not significant (P¼0.57). Maternal markers of glycemic control (glucose, OGTT, insulin use): There was no significant difference in OGTT (2-h values mmol/L) at 17-20 wk (7.11.4 in PAþD group vs 6.81.1 in PA group vs 7.11.4 in control group) or OGTT at 27-30 wk (6.71.4 in PAþD group vs 6.8 1.2 in PA group vs 6.91.2 in control group) (P>0.05 for all). Maternal complications: Although more women developed GDM in the control group (7 of 134 or 5.2%) compared with group PA (2 of 125 or (continued on next page)

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Control group (n¼141): Received standard care MNT intervention group-PA (n¼142): Received pedometer with goal of 11,000 steps per day MNT intervention group-PAþD (n¼142): Received pedometer and dietary instruction to follow low-fat Mediterranean diet Duration: 26-29 wk (11-14 wk gestation at baseline to delivery)

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1.6%) and group PA-D (6 of 103 or 3.8%), the differences were not significantly different (P>0.05). Similarly, hypertensive diseases, including hypertension and preeclampsia, were not significantly different between the two groups (P>0.05). Maternal cesarean section: Women in PA-D group were less likely to have emergency cesarean section delivery than those in PA group and control group: n¼32 (25%) vs n¼ 51 (41%) vs n¼50 (37%), P¼0.016. Infant birth weight: All three groups had similar birth weights, even after adjusting for gestational age and sex (3,605 g or relative birth weight mean 102.6%14.7% in PAþD group vs 3,695 g or relative birth weight mean 102.3%13.4% in PA group vs 3,641 g or relative birth weight mean 102.5%13.3% in control group) (P>0.05). Infant preterm delivery and gestational age: Gestational age was nearly identical in all three groups, 27811 wk in PAþD group vs 27814 wk in PA group vs 27812 wk in control group (P>0.05).

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Vesco and colleagues, 201425 PMID 25164259

USA

n¼118; age: 31.8  4.8 y; BMI: 36.74.9 (obese); initiating intervention at 14.92.6 wk; 86% white race; 58%

Control group (n¼58): One visit with study dietitian that was in addition to routine prenatal care for

Maternal gestational weight gain: The MNT intervention group weight gain from study initiation to 2 wk (continued on next page)

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Table 1. The evidence for the effects of MNTa by RDNb or international equivalent on maternal and infant health outcomes (continued)

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college graduates; approximately 68% over income for WICq (estimated using WIC income guidelines for family of 4 (<1/2 were nulliparous).

Major findings

this clinic that included feedback about food diaries but, no specific DASHr dietary management or weight management. MNT intervention group (n¼ 56): Two individual counseling sessions with study dietitian providing specific dietary and physical activity guidance based on assessment; this was followed by weekly group sessions (up to 16) which continued up to delivery. Duration: 24.7  3.0 wk (14.9  2.6 wk gestation at baseline).

postpartum was less than that of control group (2.6 vs þ1.2 kg, P<0.001). Maternal complications: No significant differences in outcomes between intervention and control group for gestational hypertension or preeclampsia, or gestational diabetes (OR 0.85, 95% CI: 0.24, 2.96; OR 0.87, 95% CI: 0.28, 2.78, respectively). Maternal cesarean section: No significant differences in cesarean section delivery between intervention and control group (OR 0.74, 95% CI: 0.35, 1.56). Infant birth weight: Significant lessening of prevalence for large for gestational age for the intervention group without a significant difference in the prevalence of small for gestational age or macrosomia. 





26% of the control group and 9% of the intervention group were large for gestational age, P<0.05. 7% of the control group and 5% of the intervention group were small for gestational age, P>0.05. 22% of the control group and 11% of the intervention group were macrosomia, P>0.05. (continued on next page)

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Major findings No significant difference between intervention and control group for birth weight, birth weight adjusted for gestational age, or weight for gestational age z-score (mean difference: 194 g, 95% CI for difference: 411, 22; mean difference: 146 g, 95% CI for difference: 331, 39, mean difference: 0.31, 95% CI for difference: 0.67, 0.01, respectively). Infant preterm delivery and gestational age: No significant difference between intervention and control group for preterm birth (OR 4.38, 95% CI: 0.41-219.64). Infant illnesses: NICU admission: No significant differences between intervention and control group in NICU admission (OR 0.33, 95% CI: 0.03, 2.00) and other complications (P>0.05).

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MNT¼medical nutrition therapy. RDN¼registered dietitian nutritionist. PMID¼PubMed ID. d BMI¼body mass index. e F/u¼follow-up. f MD¼medical doctor. g NP¼nurse practitioner. h IOM¼Institute of Medicine. i IQR¼intraquartile range. j OR¼odds ratio. k NICU¼neonatal intensive care unit. l N/A¼not available. m OGTT¼oral glucose tolerance test. n LBW¼low birth weight. o PA¼physical activity. p D¼diet. q WIC¼Special Supplemental Nutrition Program for Women, Infants, and Children. r DASH¼Dietary Approaches to Stop Hypertension. b c

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Table 1. The evidence for the effects of MNTa by RDNb or international equivalent on maternal and infant health outcomes (continued)

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FROM THE ACADEMY that MNT provided by an RDN can help lower maternal GWG in women of mixed body mass index (BMI) status or overweight or obese, although one study23 found no significant difference in GWG between the intervention and control groups among pregnant women who were overweight or obese. The overall strength of the available evidence was scored as grade I (good or strong).

Markers of Glycemic Control (Glucose, OGTT, Insulin Use). The effects of MNT by an RDN in pregnant women on markers of glycemic control were consistent, although there were only two studies.24,27 Both noted no significant differences between groups in fasting or 2-hour postprandial serum glucose, as well as frequency and amount of insulin usage, among pregnant women with GDM or type 2 DM27 and OGTT among pregnant women who were obese.24 The overall strength of the available evidence was scored as grade II (fair).

Complications: GDM, Hypertensive Disorders of Pregnancy, (Preeclampsia or Eclampsia and Hypertension). The evidence reviewed found no significant differences in maternal complications (GDM, preeclampsia, or hypertension) between groups among pregnant women with mixed BMI status and those who were overweight or obese in four studies,23-26 although a significantly (P¼0.001) higher incidence of preeclampsia was observed in the control group among pregnant women with GDM or type 2 DM in one study.27 The overall strength of the available evidence was scored as grade I (good or strong).

“failure to progress” compared with the intensive counseling group. The overall strength of the available evidence was scored as grade I (good or strong).

Infant Outcomes Birth Weight (in Grams). The effects on birth weight (in grams) were consistent among three studies.24,25,27 Among pregnant women with GDM or type 2 DM or those who were obese, no significant differences in infant birth weight were noted between groups. The overall strength of the available evidence was scored as grade II (fair).

Birth Weight (in Categories). Among pregnant women who were either overweight or obese, the MNT group had significantly fewer LGA infants25 and infants were less likely to weigh >4,000 g (macrosomia)23 compared with the control group. No effects on low birth weight or small for gestational age were observed among studies. The overall strength of the available evidence was scored as grade II (fair).

Preterm Delivery/Gestational Age. In four studies, the effects of MNT by an RDN in pregnant women on preterm delivery and gestational age were consistent. Among pregnant women with GDM or type 2 DM and those who were either overweight or obese, no significant differences in preterm delivery or gestational age between groups were observed.23-26 The overall strength of the available evidence was scored as grade I (good or strong).

Cesarean Section. One study found

Illnesses or Complications: Perinatal Mortality, NICU Admissions, Congenital Malformations Rate.

that obese pregnant women in the MNT plus physical activity group were less likely to have an emergency cesarean section,24 but three studies23,25,26 observed no significant differences between groups in pregnant women with mixed BMI status and those who were either overweight or obese. However, one study26 also found the routine care group had significantly more cesarean deliveries (P¼0.02) due to

Only one study27 reported significantly (51.2% vs 25.9%; P¼0.001) more infants born to women in the control group admitted to the NICU compared with the MNT group among pregnant women with GDM and type 2 DM. Yet, no differences were seen in NICU admissions,23,25 congenital malformation rate,23 or perinatal death.27 The overall strength of the available evidence was scored as grade II (fair).

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Research Published after Completion of the Initial Review To determine whether the results of the initial review were consistent with literature published after 2014, an additional systematic review was conducted for literature published between 2014 and 2019 using the same procedures as the initial search. A total of 93 abstracts were reviewed for relevance with one study28 retrieved for detailed evaluation and included in this updated review. Detailed description and results for this trial are shown in Table 2. In brief, this study was conducted in Europe and included high-risk pregnant women with BMI30 or a history of GDM and compared group dietary counseling with an RDN plus three 1-hour sessions with a nurse (intervention) to leaflets on diet and exercise (control). Women in the intervention group had a reduced incidence of GDM compared with controls (13.9% vs 21.6%; adjusted P¼0.044), as well as a lower GWG compared with controls from baseline to the second trimester (2.5 kg vs 3.1 kg, respectively), which was significant (P¼0.039) only after adjustment for age, previous GDM status, the number of weeks of gestation, and baseline weight. There were no differences in infant outcomes including mean birth weight, gestational age, respiratory distress, and congenital malformations.

DISCUSSION This present review is the first to provide a comprehensive assessment of maternal and infant clinical health outcomes associated with MNT by an RDN among pregnant women with malnutrition. The review employed the Academy’s rigorous methodology and included only experimental studies with a control group. Although only six studies23-28 met the inclusion criteria after screening, the majority were deemed positive quality. Overall, there is strong support that MNT by an RDN for pregnant women may help lower maternal GWG in women of mixed BMI status or who are overweight or obese. Among four studies,24-26,28 the MNT intervention group had significantly less weight gain than the control group. Overweight and obese women may have the greatest potential to benefit from MNT. In a study by Vesco

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Author(s), year; PMIDa; study design; quality Location Koivusalo and Finland colleagues, 2016 28 PMID 26223239 Randomized controlled trial Rating: not rated

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PMID¼PubMed ID. MNT¼medical nutrition therapy. c BMI¼body mass index. d GDM¼gestational diabetes mellitus. e OGTT¼oral glucose tolerance test. b

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Intervention (n[randomized n)

Major findings

n¼293; age: control group 32.64.5 y, MNTb group 32.34.9 y; BMIc at baseline: control group 32.35.4, MNT group 32.25.9; pregnant women (<20 wk); high-risk pregnant women with BMI30 or history of GDMd; singleton pregnancy

Control group (n¼155): Received pamphlets on diet and exercise MNT group (n¼138): Received one 2-h group counseling session led by a dietitian emphasizing Nordic Nutrition Recommendations (whole grains, fruits and vegetables, low-fat dairy, fish, low-fat meats and low-sugar foods) plus 3 visits with a nurse who provided individualized dietary counseling along with physical activity guidelines with goal of 150 min moderate intensity per week. Duration: <20 wk at baseline until delivery

Maternal: gestational weight gain: Those in the intervention group had a lower gestational weight gain, from baseline to the second trimester, than those in the control group 2.5 kg (95% CI 2.1-3.0) vs 3.1 kg (95% CI 2.7-3.5) and the mean difference was 0.5 kg (95% CI 21.1-0.05; P¼0.072, unadjusted; P¼0.039, after adjustment for age, previous GDM status, the number of weeks of gestation, and baseline weight. From baseline to the third trimester, those in the intervention group also had lower gestational weight gain compared with the control group, 7.6 kg (95% CI 6.7-8.3 kg) vs 7.7 kg (95% CI 7.1-8.4 kg) and the mean difference was 0.2 kg (95% CI: 21.1-0.8); P¼0.74, unadjusted; P¼0.37, after adjustment for age, previous GDM status, the number of weeks of gestation, and baseline weight. Maternal complications: Of the 138 participants in the intervention group, 20 developed GDM (13.9% [95% CI 8.7%-20.6%]) compared with 27 in the control group of 155 participants (21.6% [95% CI 14.7%-29.8%]) (P¼0.097, unadjusted; P¼0.044, after adjustment for age, prepregnancy BMI, previous GDM status, and number of weeks of gestation at the time of the diagnostic OGTTe. Infant outcomes: There were no significant differences in infant mean birth weight (P¼0.43), mean gestational age (P¼0.8), respiratory distress or transient tachypnea of newborn (P¼0.79), or congenital malformations (P¼0.34).

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Table 2. Characteristics and main findings of study published after completion of initial review, 2014-2019

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FROM THE ACADEMY and colleagues25 among women with a prepregnancy weight in the obese category, the intervention group weight gain (2.6 kg) was significantly less than that of control group (þ1.2 kg, P<0.001). This result was consistent with two other systematic reviews on this topic.29,30 Nutrition education and counseling (not limited to MNT by an RDN) significantly improved GWG (mean difference: 0.45 kg, 95% CI: 0.12 to 0.79 kg, 13 studies, N¼2,833),29 and a trend (P¼0.06) toward reduced GWG was shown for women receiving the combined diet and exercise intervention (0.76 kg, 1.55 to 0.03; 8 trials, N¼2707).30 There was strong evidence to support no significant effect on cesarean section deliveries and preterm delivery or gestational age among women with mixed BMI status or those who were either overweight or obese and no effect on other maternal complications (preeclampsia or hypertension). However, the evidence was deemed “fair” on markers of maternal glycemic control, yet this was limited to only two studies conducted among pregnant women with GDM or type 2 DM27 or who were obese.24 The most recent study,28 which was added after the initial review, was the first to find combined group and individualized sessions with an RDN and nursemidwife on both diet and physical activity led to a 39% reduction of GDM in the intervention group. Women participating in this trial were at high risk for GDM as evidenced by their high prevalence of OGTT results early in pregnancy, which may have led to differential results compared with previous studies. In addition, the sessions were individualized to the participant preferences, hence the tailoring and focus of the intervention may have led to the significant outcomes observed. Among infant outcomes, there was no effect observed for birth weight; two studies noted decreases in LGA and macrosomia in the MNT group compared with control group.23,25 A recent randomized controlled trial conducted by Peccei and colleagues similarly found that their intensive prenatal nutrition counseling did not help obese and overweight women achieve GWG within Institute of Medicine guidelines but did decrease LGA births.31 No significant differences in

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infant illnesses were observed, although one study did find nearly double the number of NICU admissions in the control (52.1%) vs the MNT groups (25.9%, P¼0.001).23 This is similar to a finding also seen in the ATLANTIC DIP study where women with GDM treated with insulin therapy had more NICU admissions then those with GDM treated with MNT (odds ratio 4.88, 95% CI 3.54 to 6.73).32

Strengths and Limitations Although there are limitations, this review is the first to analyze the role of the RDN employing MNT and how it affects maternal and infant health outcomes on pregnant women with malnutrition. This review consisted of only six controlled trials on the effects on MNT by an RDN in studies over an almost 2-decade period, 2000-2019. Although the majority of studies were graded as positive quality, this number limits the ability to translate findings to clinical and policy guidelines. Heterogeneity in the populations assessed, types of interventions, and inconsistency in outcomes examined further limited the results of this review. Subjects included those with mixed BMI status, overweight or obese, with DM or GDM. Although we aimed to include all studies which incorporated MNT for malnutrition during pregnancy, no studies of undernourished pregnant women were identified, as these were more likely to be included as part of supplementation trials and not MNT. Interventions were always performed by an RDN but varied in number of individual or group counseling sessions, type of dietary advice, and nature of the physical activity recommendations. Although the studies included in this review were conducted in multiple global regions, the training and educational requirements for the RDN credential may vary widely and hence, may have contributed to variation in study results.

IMPLICATIONS FOR RESEARCH AND PRACTICE There is clearly a need for a comprehensive and consistent definition of malnutrition during pregnancy, and likely this definition will need to encompass both underand

overnutrition, with the latter becoming increasingly more common. This review found good evidence to support the role of the RDN in improving GWG among women with mixed BMI status or who were overweight or obese. This has important public health recommendations given the majority of women do not gain optimal weight according to recommendations (21% insufficient, 48% excess).33 Excess GWG is associated with a number of complications during pregnancy and delivery and in the long term for both mother and offspring.10,15 More consistent research is needed that clearly identifies the role of the RDN in the intervention, includes a control group, and also is conducted with more diverse populations to establish clinical and policy guidelines. Despite challenges to insurance reimbursement for services by RDNs, the ongoing efforts in health care legislation and professional advocacy have helped to promote a necessary shift toward prevention.33,34 Optimal health care for pregnant women will be best achieved when RDNs can bill for not only DM and renal disease, but also obesity, among other conditions. The Academy of Nutrition and Dietetics has long supported the benefit of preventive services by RDNs.35 RDNs play a valuable role in providing health care to pregnant women, and thus, MNT provided by an RDN should be included in a comprehensive perinatal health care plan.

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FROM THE ACADEMY AUTHOR INFORMATION M. Pari-Keener is a clinical dietitian, Outpatient Clinic, Department of Pediatrics, New York-Presbyterian Brooklyn Methodist Hospital, Brooklyn. S. Gallo is an assistant professor, Nutrition and Food Studies, College of Health and Human Services, George Mason University, Fairfax, VA. B. Stahnke is a WIC advisory team manager, Georgia Department of Health, Division of Health Promotion, Georgia Special Supplemental Nutrition Program for Women, Infants and Children, Program Integrity and Strategy Unit, Atlanta. J. M. McDermid is an assistant professor; Division of Infectious Diseases & International Health, Department of Medicine, University of Virginia, Charlottesville. R. I. Al-Nimr is the director, Nutrition in Medical Education Program, and a clinical instructor in Medicine & Medical Education, The Geisel School of Medicine, Dartmouth College, Hanover, NH, and a clinical dietitian in research, Dartmouth-Hitchcock Medical Center, Lebanon, NH. J. M. Moreschi is a regional educator, University of Illinois Extension, SNAP-Ed, Ottawa. R. Hakeem is a principal, and professor of nutrition, Raana Liaqat Ali Khan Government College of Home Economics, Karachi, Pakistan. D. Handu is a senior scientific director, Evidence Analysis Center, Research, International and Scientific Affairs, and F. W. Cheng is a nutrition researcher, Evidence Analysis Center, Research, International and Scientific Affairs, both at Academy of Nutrition and Dietetics, Chicago, IL. Address correspondence to: Feon W. Cheng, PhD, MPH, RDN, CHTS-CP, Evidence Analysis Center, Research, International and Scientific Affairs, Academy of Nutrition and Dietetics, 120 S Riverside Plaza, Suite 2190, Chicago, IL 60606-6995. E-mail: [email protected]

STATEMENT OF POTENTIAL CONFLICT OF INTEREST No potential conflict of interest was reported by the authors.

FUNDING/SUPPORT Supported by the Academy of Nutrition and Dietetics and the Women’s Health Dietetic Practice Group.

ACKNOWLEDGEMENTS The authors thank Irma Gutierrez (workgroup member between 2014 to 2016), Taylor Wolfram, MS, RDN, LDN (project manager between 2014 and 2015), and Constantina Papoutsakis, PhD, RDN (project manager between 2015 and 2016) for their contributions to this project. The authors also thank the Academy of Nutrition and Dietetics and the Women’s Health Dietetic Practice Group for their financial support. The authors also thank the Academy of Nutrition and Dietetics and the Women’s Health Dietetic Practice Group for their financial support.

AUTHOR CONTRIBUTIONS All authors were involved in the data collection. M. Pari-Keener wrote first draft with contributions from S. Gallo, B. Stahnke, and F. W. Cheng. All authors reviewed and commented on subsequent drafts of the manuscript.

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