A 24-hour dietary recall for assessing the intake pattern of choline among Bangladeshi pregnant women at their third trimester of pregnancy

Shatabdi Goon1, Sima Rani Dey2

1Dept. of Nutrition and Food Engineering, Daffodil International University, Dhaka, Bangladesh; 2Dept. of Applied Statistics, East West University, Dhaka, Bangladesh

Abstract

Maternal choline intake during the third trimester of human pregnancy can modify systemic and local epigenetic marks in fetal-derived tissues, promoting better pregnancy outcomes, increased immunity, as well as improved mental and physical work capacity with proper memory and cognitive development. 103 pregnant women presenting to the antenatal care of Azimpur Maternity Hospital of Dhaka, Bangladesh in their third trimester of pregnancy were randomly selected for this cross sectional study exploring dietary intake patterns of choline. A dietary recall form was administered to estimate frequency and amount of food consumption of foods for the previous 24 hours. Most women reported diets that delivered less than the recommended choline intake (mean ± SD; 189.5 ± 98.2) providing only 42.72% of total RDA value. The results of this study may indicate that dietary choline among pregnant, Bangladeshi women may not be adequate to meet the needs of both, the mother and fetus. Further studies are warranted to determine clinical implications.

Keywords: choline, pregnancy, fetal development, cognition, pregnancy outcome



Introduction


Choline, an essential1-6 nutrient found in eggs, liver, milk, meat, nuts, legumes, and cruciferous vegetables,7 plays a significant role during the third trimester of human pregnancy to reduce the negative effect of a mother's stress8 on child health8, promoting fetal growth,6,9,10 proper brain11-16 and memory function,17-22 and learning capabilities,23-27 while protecting the future health of the child. Previous findings suggest that higher maternal choline intake may counter some adverse effects28,28,29 of prenatal stress on behavioral,29-32 neuroendocrine, and metabolic development33,34 in offspring. Higher choline intake contributed to a more stable Hypothalamic-Pituitary-Adrenal (HPA) axis,8 which translated to lower cortisol levels in the fetus. Changes in fetal genetic expression likely continue into adulthood, where they play a role in stress-related disease prevention.35 Dietary choline intake by the pregnant mother and by the infant directly affects brain development and results in permanent changes in brain function.36 Variations in maternal choline intake influence memory performance in their offspring.37

Several animal model studies have reported on the effect of choline intake and fetal development. Offspring born to pregnant rats given choline supplements were found to be faster learners with better memories.12 More choline during days 11 to 18 of gestation resulted in increased cell proliferation and decreased apoptosis in rodent fetal hippocampal progenitor cells, promoting better memory and cognitive function.12 Choline deprivation (CD)-induced dysfunction in brain mitochondria may be responsible for impairment in cognition and underlines that the brain needs an adequate choline supply for its normal functioning. Memory can be permanently enhanced by exposure to choline during the latter part of gestation.16 Also, Zeisel et al. showed that when rat pups received choline supplements, their brain function changed, resulting in lifelong memory enhancement.27 Mellot et al. showed that increased dietary intake of choline early in life improves performance of adult rats on memory tasks and prevents their age-related memory decline.22 Choline supplementation during gestation in rats leads to augmentation of spatial memory in adulthood.38 Maternal choline appears to decrease the risk of neural tube defect (NTD).39,40 A retrospective case-control study of periconceptional dietary choline intake in California, USA women found that women in the lowest quartile for daily choline intake had a 4-fold greater risk of having a baby with an NTD than women in the highest quartile for intake.40

Another study showed that a deficiency of choline substantially impaired the body's ability to regulate homocysteine levels.41 Excessive homocysteine is apparently linked with increased risks for birth defects, cardiovascular disease,42 cancer, type-2 diabetes, hypertension, depression, and more. Higher intakes of dietary choline are related to lower homocysteine concentrations.43,44

Foods rich in choline may help reduce the risk of inflammation associated with chronic diseases such as cardiovascular disease, bone loss, dementia, and Alzheimer's disease.43 A study funded by the National Institutes of Health concluded that dietary choline during pregnancy is associated with a 24% reduced risk of breast cancer in female offspring.45,46 Tumor growth rate was inversely related to choline content in the prenatal diet, resulting in 50% longer survival. Choline deficiency during pregnancy may lead to increased risk of complications during delivery, including prolonged labour, preterm delivery, preeclampsia, prematurity, very low birth weight,47 and maternal and neonatal death. It is recommended that pregnant women take 450mg of choline per day from common food sources or supplements.

In Bangladesh, knowledge of the impact of maternal food and micronutrient supplementation on infant micronutrient status is limited. Most pregnant Bangladeshi women do not meet recommended levels of micronutrients, including choline. The main objective of this study was to determine the present status of the choline intake pattern by Bangladeshi pregnant women in their third trimester of pregnancy.


Methods



This cross sectional study was carried out from the 4-May to 6-June, 2013 at Azimpur maternity hospital, Dhaka, Bangladesh. A total of two hundred pregnant women were randomly selected from all pregnant women present the first day of the survey. Of the initial 200, 103 women were in their third trimester of pregnancy and were included in this investigation. Exclusion critieria included: women not in their third trimester of pregnancy, history of hypertension, gestational diabetes, or history of spontaneous abortions. All participants signed an informed consent form.

A semi-structured pre-tested questionnaire (see Appendix 1) was developed to gather participant characteristics including: age, occupation, stage of pregnancy, weight, height, and educational level. A dietary recall form was administrated to gather information regarding dietary intake for the previous 24 hours. Choline content of foods was calculated using published data from the USDA-Nutrient Database for Standard Reference then multiplying the frequency of consumption of each food item by its choline content and summing the nutrient contributions of all foods. All of the collected data were analyzed using SPSS v-15.0. Descriptive statistics including mean, standard deviation, and frequency were obtained. All variables were normally distributed.

Results


Subject Profile

In the maternity hospital in Dhaka, Bangladesh, 69.9% of participants aged 21-25 years. 27.2% and 2.9% of were aged 26-30 years and >31 years, respectively. Approximately 6.8% of participants were illiterate; 10.7%, 56.3%, 11.7%, and 14.5% completed primary, secondary, undergraduate, and graduate levels of study, respectively. 87.4% of participants were housewives and 12.6% were service holders. In this study, 30.1% of participants were in the seventh month of pregnancy, 28.16% in the eighth month of pregnancy, and 41.74%, the ninth. Based on calculated body mass index (BMI), 3.8% were underweight, 42.72% normal weight, 33.98% overweight, 13.59% moderately obese, 3.88% severely obese, and 1.95% were very severely obese. Table 1 shows the overall subject profile attending the study.


Table 1: Characteristics of pregnant women

Variable n(%)
Age (years)
21-25 72 (69.9%)
26-30 28(27.2%)
> 31 3(2.9%)
Years of Education
Illiterate 7(6.8%)
Primary (Level 1-5) 11(10.7%)
Secondary (Level 6-10) 58(56.3%)
Undergraduate (Level 11-12) 12(11.7%)
Graduate (more than 12 years of education) 15(14.5%)
Status of Pregnant Women
Housewife 90(87.4%)
Service holder 13(12.6%)
Stage of Pregnancy
7th month of pregnancy 31(30.1%)
8th month of pregnancy 29(28.16%)
9th month of pregnancy 43(41.74%)
BMI Status
15-16 0
16-18.5 4(3.9%)
18.5-25 44(42.72%)
25-30 35(33.98%)
25-30 35(33.98%)
30-35 14(14%
35-40 4(3.9%)
Over 40 2

Dietary choline consumption

Most participants reported low consumption of choline-rich foods selected from the Bangladeshi diet. Only one participant showed adequate or near adequate intake of choline (> 400mg). The mean dietary choline consumed was 189.5mg ± 98.2 (mean ± SD). 25.2%, 31.2%, 23.3%, and 19.4% of pregnant women took choline ranges from 0-100, 101-200, 201-300, and 301-400 mg/day, respectively, through regular diet.

Table 2: Distribution of pregnant women by daily intake of choline (mg)

Choline intake level (mg/day) n (%)
0-100 26 (25.2%)
101-200 32 (31.2%)
201-300 24 (23.3%)
301-400 20 (19.4%)
≥ 400 1 (0.9%)
Total 103


Parallel improvements were observed in average choline intake with educational achievement. Average intake level of choline was 147.7 ± 83.3, 157.8 ± 110.5, 185.9 ± 97.4, 208.2 ± 94.2, and 231.4 ± 94.9 mg/day for illiterate participants, those who completed primary, secondary, undergraduate, and graduate levels of study, respectively. Table 3 illustrates dietary choline consumption.

Table 3: Gradual improvement of average choline intake per day with educational status

Educational level Average choline intake/day (mg)
Illiterate 147.7 ± 83.3
Primary 157.8 ± 110.5
Secondary 185.9 ± 97.4
Undergraduate 208.2 ± 94.2
≥ Graduate 231.4 ± 94.9


Among the factors affecting choline level intake, education level and age of participant have substantial effect. Both factors are positively correlated with choline level intake, though the correlation is weak.

Table 4: Correlation Analysis

Correlations
Choline Level Education Level Age
Choline Level 1 0.186 0.166
Education Level 0.186 1 -0.008
Age 0.166 -0.008 1


Discussion


Improving choline intake through regular diet benefits all individuals through increasing immunity and lower morbidity from infectious diseases, improving physical work capacity, memory and cognitive development. Pregnant women are less likely to have poor pregnancy outcomes (including perinatal mortality) and may deliver infants with larger birth weights and greater choline stores.

In this study, an assessment of dietary choline intake was made using a dietary recall system to record food intake by pregnant women over the previous 24 hours. Analysis revealed that the choline status of Bangladeshi pregnant women is far below clinical suggestions, as defined by the Institute of Medicine of the National Academy of Sciences (450 mg/day).

Data suggest that pregnant Bangladeshi women are consuming less than adequate amounts of choline, with mean consumption of 189.5 ± 98.2 mg/day. For comparision, in a New Zealand study,49 daily intake of choline was 316 (± 66) mg/day; in another, mean intake was 304 mg/day in women;50 in a third study, mean intake of choline by common food sources among a Taiwanese female population51 was estimated as 265 ± 9 mg/day. A study conducted in Jamaica also showed poor choline status among pregnant women with 278.5 mg/day, which was higher than the Bangladeshi scenario.52

Bangladeshi pregnant women took only 42.72% of the RDA value of 450mg/day. Poverty and lack of knowledge regarding the importance of choline among both pregnant women and health care professionals leads to less choline supplementation during pregnancy. Therefore, the dietary intake pattern of choline during third trimester of pregnancy is important to estimate.

Maternal age is an important determinant of nutritional status for pregnant women. The ideal age of pregnancy is 19-30 years. In this population, the majority were 20-25 years of age. Maternal education level has a significant effect on choline status during pregnancy. The present study showed a direct relationship between increase in consumption of choline in pregnancy and increase in maternal education level. This may due to generally better understanding of the mother regarding public health knowledge and nutritional status. Weight status also reflects the nutritional status of women. About 43% of pregnant women were categorized as “healthy weight”. 13.59%, 3.88%, and 1.95% of participants were moderately, severely, and very severely obese, indicating an increase level of obesity during pregnancy. The overall survey result also shows that most women don’t consume the recommended level of choline.

This is the first documented study evaluating dietary choline intake among the Bangladeshi population and suggests a need to further assess whether the diets of this population ensure an adequate plasma choline levels during pregnancy. An extension of this study should also examine the implications of low plasma choline concentration including the significance it may have in ensuring healthy fetal brain development in humans.

Our study has a number of limitations. The data was self-reported and the study is cross-sectional which does not infer causal relationships. Furthermore, we examined only one maternity hospital located in Dhaka, Bangladesh. Caution should be taken to generalize the data for other maternity hospitals outside Dhaka city. A 24-hour dietary recall was taken to calculate the daily choline intake. Twenty-four hour recall is a retrospective method of diet assessment, where an individual is interviewed about their food and beverage consumption during the previous day or the preceding 24 hours. However, a single 24-hour recall is not considered to be representative of habitual diet at an individual level. While there may have been a small amount of recall bias, this methodology is adequate for surveying intake in a large group and estimating group mean intakes of diet.

Conclusion


Choline is a mostly neglected micronutrient by both pregnant women and health care professionals. These professions have poor knowledge regarding its importance and therefore are missing many potential causes of health complications due to choline deficiency. The results of this study may be an indication that the choline included in the diet of pregnant Bangladeshi women may not be adequate to meet both the needs of the mother and fetus. The results presented here may be useful in understanding the present choline status among Bangladeshi pregnant women aiming to improve using strategic nutritional intervention by both government and public stakeholders.

Acknowledgement


We would like to thank our honorable professors, colleagues, and friends for supporting us in initiating the study subject. We are also grateful to those pregnant women, the doctors, and the staff of the selected maternity hospital.

Conflict of Interest


The authors report no conflict of interest.

References


1. Zeisel SH, da Costa KA. Choline: an essential nutrient for public health. Nutr Rev. Nov 2009;67(11):615-623.

2. Corbin KD, Zeisel SH. The nutrigenetics and nutrigenomics of the dietary requirement for choline. Prog Mol Biol Transl Sci. 2012;108:159-177.

3. Blusztajn JK, Mellott TJ. Choline nutrition programs brain development via DNA and histone methylation. Cent Nerv Syst Agents Med Chem. Jun 2012;12(2):82-94.

4. Sheard NF, Zeisel SH. Choline: an essential dietary nutrient? Nutrition. Jan-Feb 1989;5(1):1-5.

5. Buchman AL. The addition of choline to parenteral nutrition. Gastroenterology. Nov 2009;137(5 Suppl):S119-128.

6. Zeisel SH. Choline: critical role during fetal development and dietary requirements in adults. Annual review of nutrition. 2006;26:229.

7. Zeisel SH, Mar MH, Howe JC, Holden JM. Concentrations of choline-containing compounds and betaine in common foods. J Nutr. May 2003;133(5):1302-1307.

8. Jiang X, Yan J, West AA, et al. Maternal choline intake alters the epigenetic state of fetal cortisol-regulating genes in humans. FASEB J. Aug 2012;26(8):3563-3574.

9. Zeisel SH. Nutrition in pregnancy: the argument for including a source of choline. Int J Womens Health. 2013;5:193-199.

10. Mehedint MG, Craciunescu CN, Zeisel SH. Maternal dietary choline deficiency alters angiogenesis in fetal mouse hippocampus. Proc Natl Acad Sci U S A. Jul 20 2010;107(29):12834-12839.

11. Albright CD, Tsai AY, Friedrich CB, Mar MH, Zeisel SH. Choline availability alters embryonic development of the hippocampus and septum in the rat. Brain Res Dev Brain Res. Mar 12 1999;113(1-2):13-20.

12. Craciunescu CN, Albright CD, Mar M-H, Song J, Zeisel SH. Choline availability during embryonic development alters progenitor cell mitosis in developing mouse hippocampus. The Journal of nutrition. 2003;133(11):3614-3618.

13. Michel V, Bakovic M. Editorial: choline and brain function. Cent Nerv Syst Agents Med Chem. Jun 2012;12(2):69.

14. Zeisel SH. Nutritional importance of choline for brain development. Journal of the American College of Nutrition. 2004;23(suppl 6):621S-626S.

15. Zeisel SH. The supply of choline is important for fetal progenitor cells. Semin Cell Dev Biol. Aug 2011;22(6):624-628.

16. Zeisel SH, Niculescu MD. Perinatal choline influences brain structure and function. Nutrition reviews. 2006;64(4):197-203.

17. Wong-Goodrich SJ, Glenn MJ, Mellott TJ, Blusztajn JK, Meck WH, Williams CL. Spatial memory and hippocampal plasticity are differentially sensitive to the availability of choline in adulthood as a function of choline supply in utero.Brain Res. Oct 27 2008;1237:153-166.

18. Niculescu MD, Craciunescu CN, Zeisel SH. Dietary choline deficiency alters global and gene-specific DNA methylation in the developing hippocampus of mouse fetal brains. FASEB J. Jan 2006;20(1):43-49.

19. Mehedint MG, Niculescu MD, Craciunescu CN, Zeisel SH. Choline deficiency alters global histone methylation and epigenetic marking at the Re1 site of the calbindin 1 gene. The FASEB Journal. 2010;24(1):184-195.

20. Zeisel SH. Importance of methyl donors during reproduction. The American journal of clinical nutrition. 2009;89(2):673S-677S.

21. Kovacheva VP, Mellott TJ, Davison JM, et al. Gestational choline deficiency causes global and Igf2 gene DNA hypermethylation by up-regulation of Dnmt1 expression. J Biol Chem. Oct 26 2007;282(43):31777-31788.

22. Mellott TJ, Follettie MT, Diesl V, Hill AA, Lopez-Coviella I, Blusztajn JK. Prenatal choline availability modulates hippocampal and cerebral cortical gene expression. FASEB J. May 2007;21(7):1311-1323.

23. Boeke CE, Gillman MW, Hughes MD, Rifas-Shiman SL, Villamor E, Oken E. Choline intake during pregnancy and child cognition at age 7 years. Am J Epidemiol. Jun 15 2013;177(12):1338-1347.

24. Wu BT, Dyer RA, King DJ, Richardson KJ, Innis SM. Early second trimester maternal plasma choline and betaine are related to measures of early cognitive development in term infants. PloS one. 2012;7(8):e43448.

25. Beydoun H, Saftlas AF. Physical and mental health outcomes of prenatal maternal stress in human and animal studies: a review of recent evidence. Paediatr Perinat Epidemiol. Sep 2008;22(5):438-466.

26. Blusztajn JK, Mellott TJ. Neuroprotective actions of perinatal choline nutrition. Clin Chem Lab Med. Mar 1 2013;51(3):591-599.

27. Zeisel SH. Choline: needed for normal development of memory. J Am Coll Nutr. Oct 2000;19(5 Suppl):528S-531S.

28. Marasco V, Robinson J, Herzyk P, Spencer KA. Pre- and post-natal stress in context: effects on the stress physiology in a precocial bird. J Exp Biol. Nov 15 2012;215(Pt 22):3955-3964.

29. Catalani A, Alema GS, Cinque C, Zuena AR, Casolini P. Maternal corticosterone effects on hypothalamus-pituitary-adrenal axis regulation and behavior of the offspring in rodents. Neurosci Biobehav Rev. Jun 2011;35(7):1502-1517.

30. Macri S, Zoratto F, Laviola G. Early-stress regulates resilience, vulnerability and experimental validity in laboratory rodents through mother-offspring hormonal transfer. Neurosci Biobehav Rev. Jun 2011;35(7):1534-1543.

31. Mairesse J, Lesage J, Breton C, et al. Maternal stress alters endocrine function of the feto-placental unit in rats. Am J Physiol Endocrinol Metab. Jun 2007;292(6):E1526-1533.

32. Rangon CM, Fortes S, Lelievre V, et al. Chronic mild stress during gestation worsens neonatal brain lesions in mice. J Neurosci. Jul 11 2007;27(28):7532-7540.

33. Hirst JJ, Walker DW, Yawno T, Palliser HK. Stress in pregnancy: a role for neuroactive steroids in protecting the fetal and neonatal brain. Dev Neurosci. 2009;31(5):363-377.

34. Son GH, Geum D, Chung S, et al. Maternal stress produces learning deficits associated with impairment of NMDA receptor-mediated synaptic plasticity. J Neurosci. Mar 22 2006;26(12):3309-3318.

35. Wilkinson J. High maternal choline intake may prevent the development of stress-related disorders through epigenetic mechanisms. Epigenomics. Oct 2012;4(5):479-480.

36. Zeisel SH. The fetal origins of memory: the role of dietary choline in optimal brain development. The Journal of pediatrics. 2006;149(5):S131-S136.

37. Zeisel SH. Choline: essential for brain development and function. Advances in pediatrics. 1997;44:263.

38. Pyapali GK, Turner DA, Williams CL, Meck WH, Swartzwelder HS. Prenatal dietary choline supplementation decreases the threshold for induction of long-term potentiation in young adult rats. J Neurophysiol. Apr 1998;79(4):1790-1796.

39. Rees WD, Wilson FA, Maloney CA. Sulfur amino acid metabolism in pregnancy: the impact of methionine in the maternal diet. J Nutr. Jun 2006;136(6 Suppl):1701S-1705S.

40. Shaw GM, Carmichael SL, Yang W, Selvin S, Schaffer DM. Periconceptional dietary intake of choline and betaine and neural tube defects in offspring. Am J Epidemiol. Jul 15 2004;160(2):102-109.

41. Molloy AM, Mills JL, Cox C, et al. Choline and homocysteine interrelations in umbilical cord and maternal plasma at delivery. Am J Clin Nutr. Oct 2005;82(4):836-842.

42. Chan J, Deng L, Mikael LG, et al. Low dietary choline and low dietary riboflavin during pregnancy influence reproductive outcomes and heart development in mice. Am J Clin Nutr. Apr 2010;91(4):1035-1043.

43. Cho E, Zeisel SH, Jacques P, et al. Dietary choline and betaine assessed by food-frequency questionnaire in relation to plasma total homocysteine concentration in the Framingham Offspring Study. Am J Clin Nutr. Apr 2006;83(4):905-911.

44. Detopoulou P, Panagiotakos DB, Antonopoulou S, Pitsavos C, Stefanadis C. Dietary choline and betaine intakes in relation to concentrations of inflammatory markers in healthy adults: the ATTICA study. Am J Clin Nutr. Feb 2008;87 (2):424-430.

45. Kovacheva VP, Davison JM, Mellott TJ, et al. Raising gestational choline intake alters gene expression in DMBA-evoked mammary tumors and prolongs survival. FASEB J. Apr 2009;23(4):1054-1063.

46. Xu X, Gammon MD, Zeisel SH, et al. Choline metabolism and risk of breast cancer in a population-based study. FASEB J. Jun 2008;22(6):2045-2052.

47. Vollset SE, Refsum H, Irgens LM, et al. Plasma total homocysteine, pregnancy complications, and adverse pregnancy outcomes: the Hordaland Homocysteine study. Am J Clin Nutr. Apr 2000;71(4):962-968.

48. Allen MC. Neurodevelopmental outcomes of preterm infants. Curr Opin Neurol. Apr 2008;21(2):123-128.

49. Mygind VL, Evans SE, Peddie MC, Miller JC, Houghton LA. Estimation of usual intake and food sources of choline and betaine in New Zealand reproductive age women. Asia Pac J Clin Nutr. 2013;22(2):319-324.

50. Yonemori KM, Lim U, Koga KR, et al. Dietary choline and betaine intakes vary in an adult multiethnic population. J Nutr. Jun 2013;143(6):894-899.

51. Chu DM, Wahlqvist ML, Chang HY, Yeh NH, Lee MS. Choline and betaine food sources and intakes in Taiwanese. Asia Pac J Clin Nutr. 2012;21(4):547-557.

52. Gossell-Williams M, Fletcher H, McFarlane-Anderson N, Jacob A, Patel J, Zeisel S. Dietary intake of choline and plasma choline concentrations in pregnant women in Jamaica. West Indian Med J. Dec 2005;54(6):355-359.

53. Caudill MA. Pre- and postnatal health: evidence of increased choline needs. J Am Diet Assoc. Aug 2010;110(8):1198-1206.

54. Albright CD, Friedrich CB, Brown EC, Mar MH, Zeisel SH. Maternal dietary choline availability alters mitosis, apoptosis and the localization of TOAD-64 protein in the developing fetal rat septum. Brain Res Dev Brain Res. Jun 2 1999;115(2):123-129.

55. Fisher MC, Zeisel SH, Mar MH, Sadler TW. Perturbations in choline metabolism cause neural tube defects in mouse embryos in vitro. FASEB J. Apr 2002;16(6):619-621.

56. Meck WH, Smith RA, Williams CL. Pre- and postnatal choline supplementation produces long-term facilitation of spatial memory. Dev Psychobiol. May 1988;21(4):339-353.

57. Jensen HH, Batres-Marquez SP, Carriquiry A, Schalinske KL. Choline in the diets of the US population: NHANES, 2003–2004. FASEB J. 2007;21:lb219.