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Original Article

Association between adverse perinatal outcomes and amino acid levels measured with nutrient questionnaire in adolescent pregnancies

Guzel, Ali Irfana,*; Cinar, Mehmeta; Erkilinc, Selcuka; Aksoy, Rıfat Tanera; Yumusak, Omer Hamida; Celik, Fatmab; Celik, Yusufc

Author Information
Journal of the Chinese Medical Association: June 2016 - Volume 79 - Issue 6 - p 335-339
doi: 10.1016/j.jcma.2015.12.008


    1. Introduction

    Adolescent pregnancies are pregnancies that occur in women aged between 10 years and 19 year.1 In 2011, a total of 333,771 live births were reported in the US.2 In Turkey, the incidence of adolescent pregnancies was reported to be 4–7%, with such pregnancies generally in socioeconomically disadvantaged mothers with impaired iron–mineral metabolism related to nutritional deficiencies.3–5 These pregnancies are under risk of adverse maternal and perinatal outcomes when compared with reproductive-age pregnancies. Leppälahti et al6 reported that adolescent pregnancies were more socioeconomically disadvantaged versus reproductive-age pregnancies. In a previous study, adolescent pregnancies were reported to have lower gestational weeks at delivery, lower birth weights, and lower APGAR scores when compared with reproductive-age pregnancies.7 Eclampsia, proteinuria, urinary tract infections, pyelonephritis, and anemia were also higher in adolescent pregnancies.6 Baker et al8 designed a study to evaluate the micronutrient status in adolescent pregnancies and found an association between impaired maternal micronutrient status and adverse perinatal outcomes in adolescent pregnancies.

    In this report, we designed a prospective dietary questionnaire study in adolescent pregnancies to evaluate the maternal amino acid levels.

    2. Methods

    We designed this prospective study in Ergani State Hospital, between January 2010 and August 2010. This is a hospital in rural Turkey. Most of the patients have a lower socio-economical and educational status. Health services are provided free of charge by the government. The study was performed according to the standards of the Helsinki Declaration. Informed consent was obtained from all participants.

    Adolescent age was defined as age between 10 years and 19 years, according to the World Health Organization criteria.1 A total of 160 pregnant women were included in the study; of these women, 121 were normal-age pregnancies (Group 1: age range, 20–37 years) and 39 were adolescent pregnancies (Group 2: age range, 16–19 years).

    On the routine antenatal follow up, in the first trimester, the patients were asked to complete the new 92-item nutrient questionnaire developed by Satia et al9 An appointed nurse, the same person in each case, helped the participants to complete the questionnaire. The results obtained from the questionnaire were uploaded to the nutrient database program (BeBiS software program; Bebispro for Windows, Stuttgart, Germany; Turkish Version (Bebis 4), Istanbul Program uses data from Bundeslebensmittelschlüssel (BLS) 11.3 and USDA 15, 2004) designed to evaluate the Turkish traditional foods and commercial processed foods and the validated mean amino acid levels were measured. Gestational age of the pregnant women was assessed according to the last menstrual period or ultrasonographic measurement (SDU-2200 Pro; Shimadzu, Kyoto, Japan), or both.

    Data recorded were: age of the patients, gravidity, body mass index (BMI; calculated as kg/m2), gestational weeks, socio-economic and educational status, maternal amino acid levels and gestational week at birth, and birth weight of the new born.

    2.1. Statistical analysis

    Means and standard deviations (SD) were calculated for continuous variables. Participant characteristics and demographics were analyzed descriptively. The normal distribution of the variables was analyzed by the Kolmogorov–Smirnov test. Student t test and Chi-square (χ2) test were used to evaluate associations between the categorical and continuous variables respectively. The binary logistic regression method was used to find the risk variables for adolescent pregnancies by including all variables in the model and calculating the odds ratios. Receiver operating characteristic (ROC) curve analysis was used to assess the discriminative role of amino acids. All variables were included in the backward stepwise procedure. Two-sided p-values were considered statistically significant at p<0.05. Statistical analyses were carried out using the statistical package SPSS version 15.0 for Windows (SPSS Inc., Chicago, IL, USA).

    3. Results

    Table 1 presents the clinical characteristics of the groups. The mean ages of the patients in Groups 1 and 2 were 26.01±4.90 years and 19.61±4.25 years, respectively (p<0.05). The mean gravidity (min–max) was 3.16 (2–6) in Group 1 and 1.02 (0–1) in Group 2 (p=0.007). There was no statistically significant difference between groups in terms of BMI and gestational weeks.

    Table 1
    Table 1:
    The comparison of the clinical characteristics of the groups.

    Table 2 shows the mean amino acid levels between the groups. There was a statistically significant difference between the groups in terms of isoleucine, leucine, lysine, methionine, phenylalanine, tyrosine, threonine, valine, arginine, and proline levels (p<0.05). The mean cysteine, tryptophan, histidine, aspartate, glutamate, glycine, and serine levels were similar between the groups (p>0.05).

    Table 2
    Table 2:
    Comparison of amino acid levels between the groups.a

    Receiver operating curve (ROC) curve analysis (Fig. 1) demonstrated the area under curve (AUC) for isoleucine, leucine, lysine, methionine, phenylalanine, tyrosine, threonine, valine, arginine, and proline levels, and Table 3 depicts the AUC, cut-off value and sensitivity and specificity of these variables.

    Table 3
    Table 3:
    The results of AUC, with cut off values of the lower amino acids in adolescent pregnancies.
    Fig. 1
    Fig. 1:
    ROC analyses of amino acids. ROC = receiver operating characteristic.

    Table 4 demonstrates the levels of lower amino acid levels that were established according to the reference values of a previous study,10 and the association of these amino acids with adverse perinatal outcomes including preterm delivery and lower fetal birth weight levels. In adolescent pregnancies, lower tryptophan, histidine, serine, and alanine levels were associated with adverse perinatal outcomes.

    Table 4
    Table 4:
    The levels of lower amino acids and their association between adverse perinatal outcomes.

    4. Discussion

    In this prospective study, we asked 169 pregnant women to complete a newly developed antioxidant dietary questionnaire by Satia et al.9 This is a 92-item self-administered questionnaire modeled after a semiquantitative food frequency questionnaire. The results of the questionnaire were uploaded to the nutrient database program (BeBiS software program, Bebispro for Windows, Bundeslebensmittelschlüssel (BLS) 11.3 and USDA 15, 2004. Stuttgart, Germany) designed to evaluate the Turkish foods and commercial foods and the validated mean amino acid levels were measured. The mean amino acid levels (isoleucine, leucine, lysine, methionine, phenylalanine, tyrosine, threonine, valine, arginine, and proline) were lower in adolescent pregnancies.

    Adolescent pregnancies are risky pregnancies for both mother and newborn. A large percentage of these pregnancies occur in low- and middle-income countries. In these countries, 14% of all unsafe abortions occur in adolescent age women. In Latin America, the risk of maternal death is four times higher in adolescent mothers than mothers in reproductive-age pregnancies. In such young mothers, many medical complications can arise such as anemia, sexually transmitted diseases, postpartum hemorrhage, depression, and can also cause the mothers to leave school. In newborns from adolescent pregnancies, the rates of stillbirth, preterm birth, low birth weight, asphyxia, and future health problems are higher than in reproductive-age pregnancies.11

    The etiology of adverse outcomes in adolescent pregnancies has been debated. Adolescent mothers are a disadvantaged risk group due to their lower socioeconomic status, lower educational status, malnutrition, and micronutrient deficiencies.8,12 American College of Obstetrics and Gynecology (ACOG; Washington, DC, USA) also indicated that family income is related with earlier sexual activity and that in higher-income adolescents, condom use was more common and resulted in lower pregnancy rates.13 In Turkey, adolescents are also under risk of impaired nutritional status and related symptoms.14 This study was performed in rural Turkey, an area in which the nutritional status of adolescents was found to be worse when compared with other regions of the country.15

    Association between maternal nutritional status and fetal growth has been well established in reproductive-age pregnancies.16 Maternal malnutrition adversely affects the perinatal outcomes and leads to intrauterine growth restriction, low birth weight and infant morbidity and mortality.17,18

    Adolescents tend to consume micronutrient-poor, energy-dense diets due to lower socio-economic status.19 Baker et al8 found that serum folate, vitamin B12, total homocysteine, and serum 25-hydroxyvitamin D concentrations were lower in adolescent pregnancies, and that this poor micronutrient intake and status caused adverse perinatal outcomes in such pregnancies. Frisancho et al20 reported that even if adolescent pregnancies consumed nutrition similar with that of reproductive-age women, the adverse outcomes of pregnancies were higher in adolescent pregnancies. They concluded that this could be because in rapidly growing teenagers, the nutritional requirements of pregnancy may be greater than those in reproductive-age pregnancies.

    Amino acids are one of the main nutrient sources for fetal growth, meeting 20–40% of fetal energy requirements.21 Previous reports clarified the association between amino acid levels and perinatal outcomes. Evans et al22 studied maternal fetal amino acid concentrations and fetal outcomes during preeclampsia and observed significantly higher maternal and cord-blood amino acid concentrations in preeclampsia. Cetin et al23 also reported lower amino acid concentrations in fetuses with intrauterine growth restriction. In a previous study evaluating amniotic fluid amino acid levels in nonimmune hydrops fetalis, the authors reported lower mean phosphoserine and serine levels and higher taurine, α-aminoadipic acid, glycine, cysteine, NH(4), and arginine levels.24 We also found significantly lower levels of isoleucine, leucine, lysine, methionine, phenylalanine, tyrosine, threonine, valine, arginine, and proline in adolescent pregnancies. Among these amino acids, tryptophan, histidine, serine, and alanine levels were associated with adverse perinatal outcomes, which is an interesting result of this study.

    To the best of our knowledge, this is the first study evaluating maternal amino acid levels in adolescent pregnancies by using a dietary antioxidant questionnaire. In conclusion, we think that lower maternal amino acid levels may be the cause of adverse perinatal outcomes in adolescent pregnancies. Further studies with greater numbers of participants may give more accurate results on this topic.


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    adolescent; amino acid; dietary questionnaire; pregnancy

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