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Ann. N.Y. Acad. Sci.

ISSN 0077-8923

A N N A L S O F T H E N E W Y O R K A C A D E M Y O F SC I E N C E S
Issue: Adolescent Women’s Nutritional Status
ORIGINAL ARTICLE

Adolescent pregnancy and nutrition: a subgroup analysis


from the Mamachiponde study in Malawi
Alyssa Friebert,1 Meghan Callaghan-Gillespie,2 Peggy C. Papathakis,1 and Mark J. Manary2,3
1
Department of Nutrition and Food Science, California Polytechnic State University, San Luis Obispo, California. 2 Department
of Pediatrics, Washington University, St. Louis, Missouri. 3 School of Public Health and Family Medicine, College of Medicine,
Blantyre, Malawi

Address for correspondence: Mark J. Manary, Department of Pediatrics, Washington University, St. Louis, MO 63110-1010.
manarymj@wustl.edu

Young age at childbearing (19 years) is common and associated with poor birth outcomes. A trial among Malawian
pregnant women with moderate malnutrition was used to determine outcomes of young adolescents (18 years),
older adolescents (18–20 years), and adults (>20 years). Women received one of three supplementary foods that
provided 900 kcal/day and 33–36 g protein/day and returned every 2 weeks. Newborn/maternal measurements
were taken at delivery and after 6 and 12 weeks. Upon enrollment, adolescents had greater body mass index than
adults (19.9 ± 1.3 versus 19.5 ± 1.4 kg/m2 , P < 0.001). Young adolescents received more rations of food and enrolled
and delivered with a lower fundal height than adults (21.7 ± 5.2 versus 23.0 ± 5.6, P = 0.00 enrollment; 30.2 ± 3.1
versus 31.0 ± 2.8, P < 0.001 delivery). Among newborns, length for age was lowest in young adolescents, greater in
older adolescents, and greatest in adults (Z-scores –1.7 ± 1.2, –1.4 ± 1.2, and –1.1 ± 1.1, respectively; P < 0.001).
These differences persisted in length for age at 6 and 12 weeks of age for infants. Adolescents enrolled earlier in
pregnancy and appeared more nutritionally adequate than adults; adolescent outcomes were inferior to those of
adults, suggesting that they were subject to more physiologic stressors and/or different nutritional needs.

Keywords: adolescent pregnancy; maternal malnutrition; pregnancy; Malawi; dietary supplementation; RUSF

Challenges of pregnancy during the rapid growth and development of the fetus.2
adolescence in the developing world The compounded nutrient demands from preg-
nancy during adolescence put pregnant adolescents
About 11% of all births are to adolescent girls
at greater risk for nutritional depletion as mother
aged 15–19 years, and 95% of these births occur
and fetus compete for nutrients.4
in low- and middle-income countries.1 Significant
In order to meet the nutrient demands of preg-
progress has been made in addressing preventable
nancy, it is ideal that women have optimal nutrition
pregnancy-related morbidity and mortality across
and health before becoming pregnant.5,6 Unfortu-
the globe; however, adverse pregnancy outcomes
nately, many pregnant adolescents in developing
are still occurring at unacceptable rates, particu-
countries have inadequate nutrient reserves, plac-
larly among adolescent women.2 There are increased
ing them at increased risk of fetal growth restric-
risks for both mother and newborn associated with
tion, preterm birth, and other adverse neonatal and
early child bearing; in 2017, pregnancy and child-
maternal outcomes.3 Early child bearing in the con-
birth complications are the second leading cause of
text of undernutrition and/or micronutrient defi-
death among 15- to 19-year-old girls.3 Adolescence
ciencies is most commonly seen in sub-Saharan
is a critical time for growth and development when
Africa and South Asia,3,7 reflected in the high infant
one’s nutritional requirements increase significantly
and maternal mortality rates that occur in countries
to support rapid growth.4 Similarly, pregnancy is a
in these regions.8–10 The cause of maternal mal-
physiologic state that triggers an increase in nutri-
nutrition is multifaceted. Optimal nutrition is best
tional requirements that are essential to support

doi: 10.1111/nyas.13465
Ann. N.Y. Acad. Sci. xxxx (2017) 1–7 
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Adolescent pregnancy and nutrition Friebert et al.

described as the consumption of essential nutrients process begins in adolescence.3–5 This study aims
necessary for optimal growth, function, and health; to provide a better understanding and to improve
however, a consensus as to the type and quan- nutritional interventions for adolescent pregnant
tity of nutrients that constitute optimal nutrition women. The aim of the following analyses is twofold:
in undernourished pregnant adolescents remains to determine whether the effects of treatment on
uncertain.4,11,12 There is a spectrum of nutritional adolescent mothers in the Mamachiponde study dif-
states that are considered suboptimal. Similarly, fer between the three treatment groups and to deter-
there is a range of associated risk factors and causes mine whether there are differing effects of treatment
that promote these compromised states. While epi- after pooling all adolescents and stratifying by age.
demiologic data suggest that pregnancy during ado-
The Mamachiponde study: study design,
lescence is likely to result in worse outcomes for
interventions, and subgroup analysis
mother and newborn, there is a dearth of informa-
tion as to what can be done to ameliorate these poor Study design
outcomes. The study was an assessor-blinded, randomized,
Repletion of nutritional status during pregnancy controlled clinical trial that compared mater-
could have many beneficial effects for the mother, nal and offspring anthropometry among mod-
infant, family, and community.5 Although current erately malnourished pregnant women receiving
recommendations for undernourished pregnant either ready-to-use supplementary food (RUSF),
women include micronutrient supplementation a fortified corn soy blend (CSB+) with a
with iron and folic acid (IFA), evidence showing daily multiple micronutrient antenatal supplement
that treatment of malnourished children with (the UNICEF/WHO/UNU international multiple-
a lipid-based supplement leads to remarkable micronutrient preparation (UNIMMAP)), or
recovery cannot be ignored.13 Researchers have standard of care (CSB+ with IFA). Moderate malnu-
hypothesized about the benefits of supplemental trition was defined as MUAC 20.6 and 23.0 cm.18
feeding during pregnancy to increase macro- Eligibility criteria included fundal height (FH) of
and micronutrient intake, which will reduce the <35 cm and willingness to return to antenatal clinic
risk of adverse pregnancy outcomes.14 Several every 2 weeks for follow-up throughout their preg-
studies have suggested that multiple micronutrient nancy and at 6 and 12 weeks postpartum. Pregnant
deficiencies, along with IFA deficiencies, occur in women with complications were excluded from the
this vulnerable population of pregnant women, and study.
supplementation may confer benefits.15,16 These
Enrollment
observations inspired an initiative to assess the
From March 2014 through December 2015, preg-
outcomes of treating moderately malnourished
nant women identified as moderately malnourished
pregnant women in rural Malawi, a randomized
aged 16 years were recruited, screened for eligi-
clinical trial known as the Mamachiponde study.17
bility, and enrolled at antenatal clinics in southern
The Mamachiponde study found that maternal
Malawi. At enrollment, demographic and health
and infant outcomes were not affected by the type
information were recorded, FH was measured,
of food provided to the women during pregnancy,17
household food insecurity was determined using
and the overall improvements were modest. Across
the Household Food Insecurity Access Scale19 sur-
all treatment groups, rates of maternal weight gain
vey, and maternal anthropometry was performed,
were low, mid-upper arm circumference (MUAC)
which included weight, height, and MUAC. The
was unchanged, and 20% of infants were born
subjects’ HIV status was determined by antibody
underweight (weight-for-age Z-score (WAZ) <−2).
testing or data from the medical record.
However, every additional week of supplementary
feeding was associated with an additional 0.21 kg of Follow-up
maternal weight gain and a reduction in the odds of Participants returned for follow-up every 2 weeks
stunting at birth by 3.9%.17 for anthropometric measurements, health checks,
There is emerging agreement that nutrition sup- and provision of food. Participants “graduated”
port is necessary to improve the health of vulnerable from the study when MUAC was 23.1 cm for two
women, as well as an escalating consensus that this consecutive visits, at which time the treatment food

2 Ann. N.Y. Acad. Sci. xxxx (2017) 1–7 


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Friebert et al. Adolescent pregnancy and nutrition

was no longer distributed. IFA supplements were trients as the RUSF treatment. The UNIMMAP
continued for the rest of the pregnancy. After grad- contains 15 micronutrients and has been used
uation, women were asked to visit the clinic every in many settings worldwide in pregnant women.
4 weeks for reassessment. If relapse (MUAC 23.0 A meta-analysis and other studies have suggested
cm) was found, mothers resume assigned treatment that multiple-micronutrient supplementation dur-
food/supplements. ing pregnancy improves birth weight, length, rate
Since birth measurements were primary out- of small-for-gestational-age infants, and preterm
comes, a birth anthropometry team was identified birth.16 The CSB+ with IFA treatment provided
and trained to obtain accurate birth measurements the same quantity of CSB+ as the CSB+ with
within 24–48 h of delivery. Recumbent length was UNIMMAP ration, but with a daily iron (60 mg)
measured (Seca 417 length board, Hamburg, Ger- and folic acid (400 ␮g) tablet instead of a daily
many) in triplicate to the nearest millimeter and UNIMMAP tablet.21
averaged for analysis. Birth weight was measured in
duplicate (Adam Equipment digital scale, MTB20, Data analyses
Oxford, CT) to the nearest 10 g and averaged for Data were transformed by recoding the maternal
analysis. If the two measurements differed by more age at enrollment variable as a continuous vari-
than 10 g, a third was taken, and the outlier was elim- able into new categorical variables; young adolescent
inated. Head circumference was measured (Seca (<18 years), older adolescent (18–20 years), and
head circumference measuring band 212) to the adults (20 years). Data were analyzed using JMP
nearest millimeter in duplicate and averaged. Efforts Pro software (Version 12.1.0, SAS Institute, Cary,
were made to minimize interobserver bias by peri- NC) and IBM’s SPSS software (Version 23 SPSS, Inc.,
odic interobserver comparison and use of standard- Chicago, IL). Women for whom newborn outcomes
ized training and technique. Infant weight, height, were not collected were considered to have defaulted
head circumference, and MUAC were also measured and were not included in maternal outcome anal-
at 6- and 12-week postpartum visits. ysis. Only singleton pregnancies were included in
the newborn and maternal outcome comparisons.
Study interventions An intention-to-treat analysis was used to com-
Two dietary interventions were compared to the pare all baseline variables using analysis of variance
standard of care (CSB+ with IFA). One intervention (ANOVA) for continuous parameters and a ␹ 2 test
was a specialized food product (RUSF), which pro- to compare categorical outcomes. Wilcoxon rank
vided 920 kcal/day, 36 g of protein/day, and approxi- sum tests were performed if the normality require-
mately 200% of the recommended dietary allowance ment was not met.
(RDA) for most micronutrients during pregnancy. Two comparisons of outcomes were made: (1)
The energy content of the RUSF was designed to pro- between adolescents receiving one of the food inter-
vide 450 kcal/day to support the increased energy ventions to the standard of care and (2) pooling all
needs during the second and third trimesters of dietary treatment groups, comparing young adoles-
pregnancy plus an additional 470 kcal/day to sup- cents (<18 years), older adolescents (18–20 years),
port recovery from moderate malnutrition. The and adults (20 years).
Institute of Medicine’s RDA recommends an addi-
Adolescent findings from the
tional 25 g of protein during pregnancy; the 36 g of
Mamachiponde study
protein/day meets this increase in protein require-
ment and allows for an additional 11 g of protein/day Comparing adolescents receiving one of the
to support nutritional recovery.20 Since the RDA is food interventions to the standard of care
based on healthy and nutritionally replete persons, A total of 2284 pregnant women with MUAC
the micronutrient content of the RUSF was selected 23.0 cm were screened and evaluated for enroll-
to target this vulnerable, nutritionally deplete popu- ment. Of these, 876 adolescents (<20 years) and
lation with ample amounts of micronutrients with- 949 adults (20 years) were enrolled. Character-
out exceeding the upper limit. istics of adolescents were similar across dietary
The CSB+ with UNIMMAP treatment ration had intervention groups, with the average age at
similar amounts of energy, protein, and micronu- enrollment being 17.8 years. More than 80% of the

Ann. N.Y. Acad. Sci. xxxx (2017) 1–7 


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Adolescent pregnancy and nutrition Friebert et al.

Table 1. Anthropometric and demographic characteristics of moderately malnourished Malawian pregnant women
enrolled in supplementary feeding trial, stratified by agea
Mother <18 years Mother 18–20 years Mother >20 years
Characteristic n = 287 n = 560 n = 905 Pb

Age (years) 16.6 ± 0.5* 18.4 ± 0.8** 25.0 ± 5.3*** <0.00


First pregnancy 281 (95)* 455 (79)** 117 (12)*** <0.00
Clean water source 209 (70) 426 (74) 657 (69) 0.15
Education
None 17 (6)* 28 (5)* 151(16)**
1–6 years 162 (55) 298 (52) 495 (52) <0.00
7+ years 118 (40) 253 (44) 302 (32)
Body mass index (kg/m2 ) 19.9 ± 1.3* 19.8 ± 1.3* 19.5 ± 1.4** <0.00
Mid-upper arm circumference (cm) 22.2 ± 0.6* 22.3 ± 0.6*,** 22.3 ± 0.6** 0.16
Height (cm) 153.7 ± 5.2 154.3 ± 5.8 154.3 ± 5.7 0.27
Fundal height (cm) 21.7 ± 5.2* 22.3 ± 5.4*,** 23.0 ± 5.6** <0.00
HIV infected 5* (2) 11* (2) 178** (19) <0.00
a Values expressed as mean ± SD or n (%).
bP values calculated using one-way ANOVA (continuous measures) and ␹ 2 (categorical measures). Numerals with different super-
scripts (*, **) in the same row are different (P < 0.05).

adolescents were primigravid in each treatment Maternal outcomes for these three groups of
group, and most in each group were severely food women were similar (Table 2); while young ado-
insecure. FH at enrollment was 1 cm less in the lescents received more food rations and showed a
RUSF group (P = 0.04). All maternal outcomes were greater increase in MUAC, they did not gain more
similar across food treatment groups. Adolescents weight. In contrast, newborns delivered by young
received on average five rations of their assigned adolescents were shorter by 0.6 cm than infants born
food intervention. There was no evidence that to older adolescents and 1.2 cm shorter than infants
the adolescent mothers adhered differently to the born to adults (P < 0.001, Table 3). Young ado-
interventions than the more mature mothers when lescents had higher rates of newborn stunting and
asked at each follow-up visit about consumption underweight compared with those from older ado-
and acceptability of the foods. All treatment groups lescents or adults (P < 0.001). Birth weight, head
gained similar total weight before delivery, had a circumference, and MUAC were the least in infants
mean change in MUAC of 0.2 cm, and final FH born to young adolescents. At 6 and 12 weeks post-
within 14 days before delivery of about 30 cm partum, infants born to young adolescents remained
(P > 0.05). Similarly, there were no differences shorter than those from adults (Table 3).
in infant outcomes at birth or at 6- and 12-week
postpartum follow-up across treatment groups Summary of the Mamachiponde study
(P > 0.05). In the Mamachiponde study, while pregnant young
adolescents did not have characteristics of more
Comparing young adolescents, older severe clinical malnutrition, such as lower BMI,
adolescents, and adults more HIV infection, or lower maternal height, they
In the pooled treatment group analysis comparing gave birth to newborns whose weight and length
young adolescents (<18 years), older adolescents were less than those born to older adolescents and
(18–20 years), and adults (20 years), young adults. FH at enrollment was less among young
adolescents had greater body mass index (BMI) adolescents, which may well be due to presentation
and smaller FH by 1.3 cm compared with adults earlier in pregnancy. Differences in weight-for-age
(Table 1). The percentage of mothers infected with Z-score (WAZ) and length-for-age Z-score (LAZ)
HIV increased with age, with 19% of adults infected between adolescents and adults were greater than
with HIV compared with less than 5% of adolescents weight for length, which is also consistent with this
(P < 0.001). notion.

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Friebert et al. Adolescent pregnancy and nutrition

Table 2. Maternal outcomes of malnourished Malawian pregnant women, stratified by agea

Mother <18 years Mother 18–20 years Mother >20 years


Outcome n = 287 n = 560 n = 905 Pb

Weight gain from enrollment to final measurementc (kg) 3.0 ± 2.2 2.9 ± 2.4 3.2 ± 2.5 0.17
Time from enrollment to delivery (weeks) 11.9 ± 6.2* 11.5 ± 6.3*,** 11.2 ± 6.5** 0.02
Treatment rations received 5.3 ± 2.9* 5.1 ± 2.9*,** 4.8 ± 2.8** 0.02
Weight gainc <454 g/week 221* (88) 410* (86) 630** (81) 0.01
Change in MUAC 0.2 ± 0.8* 0.2 ± 0.8* 0.0 ± 0.8** <0.00
Final MUAC (cm) 22.0 ± 0.9* 22.1 ± 0.9* 22.3 ± 0.9** <0.00
Attained MUAC >23 cm 83* (30) 163* (30) 313** (36) 0.05
Final fundal height (cm) 30.2 ± 3.1* 30.5 ± 3.08 31.0 ± 2.8*,** <0.00
Final fundal height <28 cm 26* (9) 34*,** (6) 32** (4) <0.00
Lost pregnancy type
Miscarriage 1 (0.3) 7 (1.3) 9 (1.0) 0.45
Stillbirth 3 (1.0) 5 (0.9) 11 (1.2) 0.84
Perinatal death 4 (1.4) 6 (1.1) 10 (1.1) 0.91

MUAC, mid-upper arm circumference.


a Values expressed as mean ± SD or n (%).
b P values calculated using one-way ANOVA (continuous measures) and ␹ 2 (categorical measures). Numerals with different super-

scripts (*, **, ***) in the same row are different (P < 0.05).
c Weight gain analysis includes only women on treatment for at least 14 days who had singleton births and were not lost to follow-up.

Differences in infant anthropometry per- for young adolescents to either prevent or treat
sisted for 3 months after birth, suggesting that malnutrition.
anthropometric measures, such as WAZ, LAZ, and The Mamachiponde study is quite limited in that
WLZ, may continue to be lower with little to no only women with moderate malnutrition were con-
catch-up in infants of young adolescents compared sidered for supplementary feeding, so we have no
with infants of older adolescents and adults. The information about young adolescents with a normal
birth outcomes were inferior in all adolescents, but MUAC in this context or about women <16 years of
more so among the young adolescents, suggesting age. The reliance on FH as a measure of gestational
additional vulnerability in this demographic. age introduced further uncertainty as to what role
These findings are consistent with those of recent premature delivery played in these findings.
observational studies, which have highlighted that
adolescent pregnancy in low- and middle-income Future directions
countries is strongly associated with low birth Pregnancy is a time when nutrition requirements
weight, preterm birth, and stunting.22–27 Interven- increase substantially, and a woman’s body, regard-
tions to reduce low birth weight and premature less of age, undergoes significant physiological
delivery should be considered in this population. changes to accommodate the fetus. Adolescent girls
Testing and treatment for urinary tract infections are an especially vulnerable group owing to their
and bacterial vaginosis are promising with regard rapid growth and development, and pregnancy in
to reducing premature delivery. this population, more specifically, in those younger
Our observations support the notion that the than 18 years of age, is more likely to result in
compounded demands in nutrient requirements increased health risk for the mother and additional
necessary in pregnancy and adolescence may lead growth faltering for the offspring. Evidence has
to a competition for nutrients between the young also shown that teenage pregnancy can have social
mother and fetus, and that young mothers may and economic consequences that result in limited
have greater nutrient requirements than adults. This socioeconomic opportunities. The risk of stunting
competition may result in reduced fetal growth and is higher in adolescent pregnancies and leads to
subsequent stunting. Understanding these require- numerous short- and long-term effects, such as poor
ments is necessary for designing interventions cognition and educational performance, reduced

Ann. N.Y. Acad. Sci. xxxx (2017) 1–7 


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Adolescent pregnancy and nutrition Friebert et al.

Table 3. Infant and clinical anthropometric outcomes stratified by mother’s agea

Mother <18 years Mother 18–20 years Mother >20 years


Outcome n = 287 n = 560 n = 905 Pb

Weight for age (WFA) at birth, Z-score –1.6 ± 1.0* –1.5 ± 1.0* –1.1 ± 0.9** <0.00
Length for age (LFA) at birth, Z-score –1.7 ± 1.2* –1.4 ± 1.2** –1.1 ± 1.1*** <0.00
Weight for length at birth, Z-scorec –0.5 ± 1.0*,** –0.5 ± 1.0** –0.4 ± 1.1* <0.00
Head circumference for age at birth, Z-score –0.1 ± 1.5* –0.0 ± 1.2*,** 0.1 ± 1.2** 0.03
Birth MUAC (cm) 9.3 ± 0.8* 9.4 ± 0.83* 9.7 ± 0.85** <0.00
Underweight at birth, WFA < –2 70 (30)* 108 (24)* 99 (14)** <0.00
Stunted at birth, LFA < –2 80 (35)* 118 (27)** 126 (17)*** <0.00
Weight for age at 6 weeks, Z-score –1.1 ± 1.2* –0.9 ± 1.1*,** –0.8 ± 1.0** <0.00
Length for age at 6 weeks, Z-score –1.5 ± 1.3* –1.3 ± 1.2** –1.0 ± 1.1*** <0.00
Weight for length at 6 weeks, Z-scorec 0.3 ± 1.1 0.4 ± 1.0 0.3 ± 1.1 0.33
MUAC at 6 weeks (cm) 11.7 ± 1.2* 11.9 ± 1.1*,** 11.9 ± 1.0** 0.01
Head circumference at 6 weeks (cm) 37.8 ± 1.6* 38.0 ± 1.5*,** 38.1 ± 1.5** 0.03
Weight for age at 12 weeks, Z-score –0.8 ± 1.1* –0.8 ± 1.0* –1.0 ± 1.1** <0.00
Length for age at 12 weeks, Z-score –1.4 ± 1.3* –1.1 ± 1.2** –1.0 ± 1.1** <0.00
Weight for length at 12 weeks, Z-score 0.3 ± 1.0* 0.3 ± 1.0* 0.1 ± 1.1** 0.01
MUAC at 12 weeks (cm) 13.0 ± 1.05 13.1 ± 1.12 13.1 ± 1.20 0.28
Head circumference at 12 weeks (cm) 40.1 ± 1.70* 40.4 ± 1.47** 40.4 ± 1.45** 0.13
Infant deathsc 9 (3) 19 (3) 36 (4) 0.74

MUAC, mid-upper arm circumference.


a Values expressed as mean ± SD or n (%).
b P values calculated using one-way ANOVA (continuous measures) and ␹ 2 (categorical measures). Numerals with different super-

scripts (*, **, ***) in the same row are different (P < 0.05).
c Infant death is defined as death reported by mother or local health workers before 12 weeks.

adult productivity and income, and increased risk Diseases, and Nutrition, Bureau for Global Health,
for morbidity and mortality. The data presented United States Agency for International Develop-
in this study substantiate this notion, highlighting ment (USAID) under terms of Cooperative Agree-
the importance of expanding and enhancing pub- ment No. AID-OAA-A-12-00005; the Food and
lic health efforts to delay the age of first pregnancy, Nutrition Technical Assistance III Project (FANTA),
as these could confer benefits to affected individu- managed by FHI 360; Feed the Future (Peanut and
als and their societies. Additionally, further research Mycotoxin Innovation Lab); California Polytech-
is needed to gain an understanding of the nutrient nic State University, San Luis Obispo; the Califor-
requirements needed throughout adolescent preg- nia Agricultural Research Initiative; the U.S. Dairy
nancy to assist in providing these women with a Export Council, the Dairy Research Initiative; and
sufficient diet that supports optimal maternal and the Hickey Family Foundation. The contents of
fetal health and development. Targeting adolescent this article are the responsibility of the authors
women early in their pregnancy will help to mitigate and do not necessarily reflect the views of any
the adverse pregnancy outcomes associated with sponsors.
adolescent pregnancy. Cumulatively, these efforts
will increase awareness, supplemental support, and Competing interests
targeted nutrition programs to help improve preg-
The authors declare no competing interests.
nancy outcomes and to increase national policies.
Acknowledgments
References
This work was supported by the Sackler Institute 1. WHO. 2016. Adolescents: health risks and solutions:
for Nutrition Science, the New York Academy of fact sheet. Accessed May 1, 2017. http://www.who.int/
Sciences; the Office of Global Health, Infectious mediacentre/factsheets/fs345/en/.

6 Ann. N.Y. Acad. Sci. xxxx (2017) 1–7 


C 2017 New York Academy of Sciences.
Friebert et al. Adolescent pregnancy and nutrition

2. World Health Organization. 2016. WHO recommendations middle-income countries: a systematic review and meta-
on antenatal care for a positive pregnancy experience. World analysis. Matern. Child Nutr. 11: 415–432.
Health Organization, Geneva. 15. Gernand, A.D., K.J. Schulze, C.P. Stewart, et al. 2016.
3. Johnson, W. & S. Moore. 2016. Adolescent pregnancy, nutri- Micronutrient deficiencies in pregnancy worldwide: health
tion, and health outcomes in low- and middle-income effects and prevention. Nat. Rev. Endocrinol. 12: 274–289.
countries: what we know and what we don’t know. BJOG 16. Haider, B.A. & Z.A. Bhutta. 2015. Multiple-micronutrient
123: 1589–1592. supplementation for women during pregnancy. Cochrane
4. Hanson, M.A., A. Bardsley, L.M. De-Regil, et al. 2015. Database Syst. Rev. 11: CD004905.
The International Federation of Gynecology and Obstet- 17. Callaghan-Gillespie, M., A.A. Schaffner, P. Garcia, et al. 2017.
rics (FIGO) recommendations on adolescent, preconcep- Trial of ready-to-use supplemental food and corn-soy blend
tion, and maternal nutrition: “Think Nutrition First”. Int. J. in pregnant Malawian women with moderate malnutrition:
Gynaecol. Obstet. 131(Suppl. 4): S213–S253. a randomized controlled clinical trial. Am. J. Clin. Nutr.
5. Lassi, Z.S., A. Moin, J.K. Das, et al. 2017. Systematic review https://doi.org/10.3945/ajcn.117.157198.
on evidence-based adolescent nutrition interventions. Ann. 18. Ververs, M.T., A. Antierens, A. Sackl, et al. 2013. Which
N.Y. Acad. Sci. 1393: 34–50. anthropometric indicators identify a pregnant woman as
6. Frith, A.L., R.T. Naved, L.A. Persson & E.A. Frongillo. 2015. acutely malnourished and predict adverse birth outcomes
Early prenatal food supplementation ameliorates the nega- in the humanitarian context? PLoS Curr. 5. https://doi.org/
tive association of maternal stress with birth size in a ran- 10.1371/currents.dis.54a8b618c1bc031ea140e3f2934599c8.
domised trial. Matern. Child Nutr. 11: 537–549. 19. Coates, J., A. Swindale & P. Bilinsky. 2007. Household Food
7. Vir, S.C. 2016. Improving women’s nutrition imperative for Insecurity Access Scale (HFIAS) for measurement of food
rapid reduction of childhood stunting in South Asia: cou- access: indicator guide. USAID, Washington DC.
pling of nutrition specific interventions with nutrition sen- 20. IOM. 2006. Dietary reference intakes: the essential guide
sitive measures essential. Matern. Child Nutr. 12(Suppl. 1): to nutrient requirements. The National Academies Press,
72–90. Washington DC.
8. Kozuki, N., J. Katz, A.C. Lee, et al. 2015. Short mater- 21. World Food Programme. 2014. Technical specifications for
nal stature increases risk of small-for-gestational-age and the manufacture of super cereal—corn soya blend with
preterm births in low- and middle-income countries: sugar. Version 14.1. Rome: World Food Programme.
individual participant data meta-analysis and population 22. Hoque, M. & C. Hoque. 2010. A comparison of obstet-
attributable fraction. J. Nutr. 145: 2542–2550. rics and perinatal outcomes of teenagers and older women:
9. Garcı́a-Basteiro, A.L., L. Quintó, E. Macete, et al. 2017. Infant experiences from rural South Africa. Afr. J. Prim. Health Care
mortality and morbidity associated with preterm and small- Fam. Med. 2: 171.
for-gestational-age births in Southern Mozambique: a ret- 23. Brits, H., M. Adriaanse, D.M. Rall, et al. 2005. Causes of
rospective cohort study. PLoS One 12: e0172533. prematurity in the Bloemfontein Academic Complex. South
10. Kozuki, N., J. Katz, S.C. LeClerq, et al. 2015. Risk factors and Afr. Fam. Pract. 57: 223–226.
neonatal/infant mortality risk of small-for-gestational-age 24. Fall, C.H.D. et al. 2015. Association between maternal age
and preterm birth in rural Nepal. J. Matern. Fetal Neonatal at childbirth and child and adult outcomes in the offspring:
Med. 28: 1019–1025. a prospective study in five low-income and middle-income
11. Lassi, Z.S., T. Mansoor, R.A. Salam, et al. 2017. Review of countries. Lancet Glob. Health 3: e341–e422.
nutrition guidelines relevant for adolescents in low- and 25. Momno-Ngoma, G. et al. 2016. Young adolescent girls
middle-income countries. Ann. N.Y. Acad. Sci. 1393: 51–60. are at high risk for adverse pregnancy outcomes in sub-
12. Pencharz, P.B. 2005. Special problems of nutrition in the Saharan Africa: an observational multicountry study. BMJ
pregnancy of teenagers. Nestle Nutr. Workshop Ser. Pediatr. 6: e011783.
Program 55: 213–217; discussion 217–220. 26. Althabe, F. et al. 2015. Adverse maternal and perinatal
13. Bhutta, Z.A., T. Ahmed, R.E. Black, et al. 2008. What works? outcomes in adolescent pregnancies; the Global Network’s
Interventions for maternal and child undernutrition and Maternal Newborn Health Registry study. Reprod. Health
survival. Lancet 371: 417–440. 12(Suppl. 2): S8.
14. Stevens, B., P. Buettner, K. Watt, et al. 2015. The effect of bal- 27. Ganchimen, T. et al. 2013. Maternal and perinatal outcomes
anced protein energy supplementation in undernourished among nulliparous adolescents in low- and middle-income
pregnant women and child physical growth in low- and countries: a multi-country study. BJOG 120: 1622–1630.

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