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Journal of the American College of Nutrition, Vol. 18, No. 4, 324-329 (1999)
Published by the American College of Nutrition

Original Paper

Riboflavin Levels in Maternal Milk: The Influence of Vitamin B2 Status during the Third Trimester of Pregnancy

Rosa M. Ortega, PhD, FACN, M. Elena Quintas, PhD, Rosa M. Martínez, PhD, Pedro Andrés, PhD, Ana M. López-Sobaler, PhD and Ana M. Requejo, PhD

Departamento de Nutrición, Facultad de Farmacia, Universidad Complutense, Madrid (R.M.O., M.E.Q., A.M.L.-S., A.M.R.), SPAIN
Servicio de Análisis Clínicos, Servicio de Obstetricia y Ginecología, Hospital INSALUD, Cuenca, (R.M.M.), SPAIN
Laboratorio de Técnicas Instrumentales, Facultad de Farmacia, Universidad Complutense, Madrid (P.A.), SPAIN

Address reprint requests to: Profa. Dra. Rosa Ma Ortega, Departamento de Nutrición, Facultad de Farmacia, Universidad Complutense, 28040-Madrid, SPAIN


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 ACKNOWLEDGMENTS
 REFERENCES
 
Objective: The aim of the present investigation was to study the relationship between riboflavin status during the third trimester of pregnancy and levels of this vitamin in transition milk (days 13 to 14 of lactation) and mature milk (day 40 of lactation).

Methods: The pregnancies and lactation periods of 57 healthy women between 18 and 35 years of age (27 ±3.7 years) were monitored, vitamin intake during the third trimester was determined by recording the consumption of foods over five days and by registering the quantities provided by dietary supplements. Riboflavin status during this stage of pregnancy was determined via the measurement of the activation of erythrocyte glutathione reductase (EGR) by flavine adenine dinucleotide (FAD). Milk riboflavin levels were determined by fluorometry.

Results: Those subjects with riboflavin intakes below recommended (1.6 mg/day) (Group L) showed lower consumption of milk products (305.2 ±88.5 g/day) than did those with greater intakes (Group H) (507.9 ±137.2 g/day). The consumption of riboflavin containing supplements was very low and was seen only in two H subjects. Transition and mature milk riboflavin levels were significantly higher in H subjects (948.1 ±700.1 nmol/L for transition milk and 993.8 ±436.6 nmol/L for mature milk) than L subjects (574.9 ±258.7 nmol/L for transition milk and 725.4 ±254.3 nmol/L for mature milk). Subjects with {alpha}-EGR coefficients over 1.2 in the third trimester showed significantly lower mature milk riboflavin levels (704.1 ±241.8 nmol/L) than did subjects with more satisfactory {alpha}-EGR coefficients (996.4 ±302.9 nmol/L).

Conclusion: The influence of maternal vitamin B2 status during pregnancy on breast milk riboflavin levels was confirmed.

Key words: riboflavin intake, pregnancy, lactation, {alpha}-EGR, riboflavin in milk


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 ACKNOWLEDGMENTS
 REFERENCES
 
Fetal growth and the secretion of breast milk are processes that require adequate supplies of nutrients [1]. It is possible that in well-nourished women the requirements of these processes are met by metabolic and physiological adjustments [1]. However, nutritional imbalances suffered during these periods could be harmful to the mother and the outcome of her pregnancy [1–3], and also impair the composition of her breast milk [4–6].

Given that riboflavin is an essential constituent of muscle tissue [7] it is needed in considerably increased amounts during pregnancy for the growth of fetal tissues [5]. Haste et al. [8] report that riboflavin intake during pregnancy is related to the birthweight of the newborn. Riboflavin intake is of greater importance during the pre- and post-natal periods owing to its role as a co-enzyme in energy utilisation [9]. Further, when a child is born, a rapid change occurs from a relatively hypoxic to a relatively hyperoxic environment, with the concurrent risk of reactive oxygen species formation. Vitamin B2 acts mainly as a cofactor of glutathione reductase, which maintains glutathione in the reduced state. It can therefore be considered an indirect antioxidative vitamin [10].

The aim of the present investigation was to study the relationship between vitamin B2 status during the third trimester of pregnancy and levels of this vitamin in maternal milk.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 ACKNOWLEDGMENTS
 REFERENCES
 
The pregnancies and lactation periods of 57 women were followed. The characteristics of the subjects and criteria of inclusion/exclusion have been reported in previous papers [11,12]. The study subjects had normal pregnancies and were free of diabetes, renal diseases or cardiac or liver dysfunction.

The study protocol was approved by the Comité de Investigación de la Facultad de Farmacia, Universidad Complutense de Madrid and by the Comité Ético del Hospital del INSALUD de Cuenca.

During their third trimester of gestation (between weeks 32 and 36), dietary, anthropometric and biochemical studies were made. After subjects gave birth, the study was continued. The composition of the now lactating subjects’ maternal milk was analyzed at days 13 to 14 (transitional milk) and 40 (mature milk) [13].

Dietary Survey
Food intake was recorded by keeping a food record booklet for five days, including a Sunday. Kitchen scales were provided to all subjects in order to facilitate the weighing of food. After the questionnaire was completed, the booklets were returned in person. A qualified nutritionist inspected the records to ensure that they were complete and that sufficient detail had been recorded. In the same interview, a "food frequency intake" questionnaire was completed in order to contrast subjects’ answers with the results of their five day dietary record and an explanation was requested if answers were inconsistent. The details of the dietetic method used have been published previously [11,12].

The vitamin B2 contents of consumed foods were calculated using "Tables of Food Composition" published by the Instituto de Nutrición [14]. The recommended intake of riboflavin accepted in this study was that for women in the second half of pregnancy as established in the "Tables of Recommended Energy and Nutrient Intakes for the Spanish Population" [15] (0.6 mg/1000 kcal + 0.2 mg, with a minimum provision of 1.6 mg/day). Given that no subject showed high energy intakes, recommended intake (RI) was established as 1.6 mg/day.

The intake of supplements was recorded by asking subjects what and how much they had taken during their pregnancy. This was then added to the quantity of riboflavin provided by their diet. The adequacy of the diet with respect to riboflavin was determined by comparing this figure to that recommended.

Biochemical Study
10 mL of venous blood was taken first thing in the morning from night-fasted subjects. Samples were collected in heparinized tubes and maintained at 4° to 6°C until riboflavin analysis was performed, (always before the elapse of 48 hours). For the determination of hematocrit, five mL of heparin-free blood was transferred to another test tube and analyzed at room temperature within an hour of collection. Vitamin B2 status was determined by measuring the activation of erythrocyte glutathione reductase (EGR) (EC 1.6.4.2.) by flavine adenine dinucleotide (FAD) (Boehringer-Mannheim GMbH, Mannheim, Germany). The activity of the enzyme was measured in basal conditions and after the addition of excess FAD from hemolyzed blood samples, by spectrophotometric determinations at 340 nm of NADP formed in a spectrophotometer Shimadzu UV-1203 (Shimadzu Corporation, Kyoto, Japan). The relationship between enzyme activity before and after saturation is expressed by the saturation coefficient ‘{alpha}’. High {alpha} coefficients imply an unfavorable biochemical riboflavin status [16] (C.V = 4.4%). The hematocrit index, necessary for the calculation of the {alpha}-EGR coefficient, was determined using a Coulter S. Plus analyser (Coulter Diagnostics, Hialeah FL 33014, USA) [17].

Milk samples were taken between 10 and 11 o’clock in the morning by manual expression of a five mL sample from each breast at the beginning and end of feeds. The protocol for both the collection and subsequent handling of milk has been previously described [11,12].

Milk samples were subjected to complete acid hydrolysis by autoclaving the sample in 0.1 N HCl (Merck, Darmstadt D-6100 Franfurter Strasse 250, Germany). The proteins were removed by adjusting the pH to 4.5 with NaOH (Merck) and centrifuging. Extract was acidified with glacial acetic acid (Merck) and oxidized with potassium permanganate (Merck); the excess of the oxidizing agent was destroyed with hydrogen peroxide (Merck). Riboflavin levels then determined by fluorometry (Perkin Elmer MPF-2A, Beconsfield, UK). Fluorescent measurements were made at the excitation and emission wave lengths of 440 and 565 nm, respectively, on sample solutions containing an internal standard (Riboflavine Merck) and on samples treated with 20 mg of sodium hydrosulphite (Merck) as a blank to correct for postoxidation remnant fluorescence [18]. The coefficient of variation was found to be 3.8%.

In order to establish normality limits for the {alpha}-EGR coefficients, the criteria of the following authors were taken into account: Vuillemier et al. [16] and Dostálová [19], who regard coefficients of <1.20 as an indicator of low risk, those between 1.20 and 1.29 as indicators of moderate risk and those above 1.29 as a high risk of deficiency; Bates et al. [4], who consider levels to be deficient when {alpha}-EGR is >1.30; Vir et al. [20], who consider the same when this coefficient is >1.20; Açkurt et al. [9] and Keller and Salkeld [21], who consider {alpha}-EGR coefficients of >1.52 as indicators of high risk, those between 1.44 and 1.52 as indicators of moderate risk and <1.44 to represent low risk.

With respect to riboflavin levels in maternal milk, 800 nmol/L was established as the lower normal limit [22].

Anthropometric Study
All data were collected in the morning. Weight and height were measured with subjects in bare feet and underwear, using a digital electronic weighing scale (Seca alpha; Rue Lavoisier 91430, Igmy, France; range: 0.1–150 Kg) and a digital stadiometer (Harpenden Pfifter 450; Badem, Padum Aveny, Carlstadt, NJ, USA; range 70–205 cm), respectively. Body mass index (BMI) (kg/m2) was calculated from these data. All data were collected by trained personnel following norms set out by the World Health Organisation (WHO) [23].

To measure changes in anthropometric values during pregnancy, the values of these variables at the beginning of pregnancy (4 to 8 weeks of gestation) were obtained from subjects’ clinical records. Weight and length of the newborn were measured immediately after birth.

Other Data
The maternal gestation age at delivery was calculated from the agreed delivery data recorded from the last menstrual period and early ultrasound examination data. Data such as age, parity and use of tobacco were recorded in a questionnaire during the first interview.

Statistical Analysis
Mean values and SD are shown. Where the distribution of results was normally distributed, the degree of significance of differences between means was calculated using Student’s t test. Where the distribution of results was not normally distributed, the Mann-Whitney test was applied. Analysis of covariance was used to eliminate the influence of variables, such as age, that could modify the results. Differences were considered significant if p < 0.05 [24].


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
ACKNOWLEDGMENTS
 REFERENCES
 
Subjects’ data are presented with respect to whether their intakes were below that recommended (Group L) or above (Group H) (Tables 1–3). Table 1 shows both the mothers’ and newborns’ demographic and anthropometric data and reveals that H subjects were older than L subjects. No other significant differences were found with respect to these parameters.


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  		TABLE 1. Demographic and Anthropometric Data of Subjects and their Newborn

 

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  		TABLE 3. Riboflavin Status (Determined by Measuring the Activation Coefficient of Erythrocyte Glutathione Reductase, {alpha}-EGR) during the Third Trimester and Levels of Riboflavin in Transition (Days 13–14) and Mature Milk (Day 40)

 
Table 2 shows the riboflavin intake during the third trimester of pregnancy. L subjects showed significantly lower intakes of milk products (305.2 ±88.5 g/day) than did H subjects (507.9 ±137.2 g/day). These differences are probably the reason for the greater intake of riboflavin seen in H subjects (Table 2).


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  		TABLE 2. Riboflavin Intake during the Third Trimester of Pregnancy

 
Only two H subjects took a riboflavin-containing supplement during the third trimester and even then in very small amounts (2 mg/day). The dietetic results are, therefore, hardly modified when supplements are taken into account (Table 2).

Table 3 lists riboflavin status during the third trimester and levels of riboflavin in transition and mature milk. Though H subjects showed more satisfactory serum {alpha}-EGR coefficients than did L subjects, this difference was not significant. However, subjects with riboflavin intakes of <1.4 mg/day (25th percentile) showed less adequate {alpha}-EGR coefficients (1.32 ±0.40) than did those with greater riboflavin intakes (1.07 ±0.16) (p < 0.05).

Transition and mature milk riboflavin levels were significantly higher in H subjects, while the percentage of subjects with riboflavin levels below the normal limit was greater among L subjects (Table 3).

Analysis of covariance shows that the differences in transition and mature milk vitamin B2 concentrations between L and H subjects are independent of the age difference between these groups (Table 1).

Subjects with {alpha}-EGR coefficients >1.2 in the third trimester showed significantly lower mature milk riboflavin levels (704.1 ±241.8 nmol/L) than did subjects with more satisfactory {alpha}-EGR levels (996.4 ±302.9 nmol/L).


   DISCUSSION
 
The duration of pregnancy and the anthropometric data of the mothers and their newborn (Table 1) are similar to those reported in other studies [9,25–27]. The mean intake of vitamin B2 (Table 2) observed during the third trimester was similar to that reported by other authors [2,8,26,28–30].

Though mean riboflavin intake is generally satisfactory [6,26,29] given the increased intake of milk products usually seen during pregnancy [26,29], in the present study 43.9% of subjects showed riboflavin intakes lower than those recommended. This was higher than that recorded by Ortega et al. [26] in Guadalajara (Spain), where only 23% showed intakes below recommended. When supplements were taken into account this figure fell to only 3%.

Heller et al. [31] indicate that riboflavin supplementation is recommended to prevent subclinical metabolic disturbances of vitamin-dependent enzyme systems. However, in the present population, the use of riboflavin supplements was scarce (Table 2).

The {alpha}-EGR coefficients obtained (Table 2) were similar to those seen in similar subjects during the third trimester of pregnancy by Bates et al. [4] (1.19 ±0.08 in pregnant women of Cambridge), Açkurt et al. [9] (1.4 ±0.28) and Dostálová [19] (0.99 ±0.12).

In the present study, although H subjects showed more adequate serum {alpha}-EGR coefficients than did L subjects, the difference was not significant. Neither was the correlation between riboflavin intake and {alpha}-EGR statistically significant. However, the influence of riboflavin intake on {alpha}-EGR coefficients is confirmed since those of subjects with intakes of <1.4 mg/day (25th percentile) showed less adequate serum {alpha}-EGR coefficients (1.32 ±0.40 compared to 1.07 ±0.16 in subjects with greater riboflavin intakes) (p < 0.05).

The mean concentration of riboflavin in breast milk (Table 3) was similar to that reported in other studies. Bamji et al. [32] found a concentration of 1095 nmol/L in the transition milk (6 to 30 days) of Indian mothers and 611 nmol/L in their mature milk. Further, the Committee on Nutrition [33] and the National Research Council [34] indicate that the milk of well-nourished mothers contains riboflavin concentrations of approximately 930 nmol/L. Similarly, Fomon [35] and Schwarz [36] report mature milk riboflavin concentrations of 957 nmol/L and 983 mol/L respectively.

In agreement with Ford et al. [37], the present results show riboflavin values to change little in the weeks following parturition (Table 3). Nail et al. [6] also report that riboflavin values did not change significantly as milk matured from one to six weeks postpartum.

Though Nail et al. [6] and Bamji et al. [32] report that levels of riboflavin in milk were generally satisfactory; in the present population, 14% of subjects showed values of <800 nmol/L in transition milk and 15.8% showed the same in mature milk. This should be improved, especially for L women.

Some authors dispute the influence of intake on breast milk levels. Bamji et al. [32] report a lack of clear-cut correlations between the enzymatic indices of vitamin status and milk levels of the corresponding vitamins. Neither does the Institute of Medicine [38] find any relationship between maternal intake of riboflavin and the concentration of vitamin B2 in milk. However, Nail et al. [6] report that milk riboflavin values were significantly lower in a non-supplemented group of mothers, both at one and six weeks postpartum. Bates et al. [4] indicate that lower concentrations found in riboflavin-deficient populations can be increased by supplementation. In agreement with the latter authors, the results of the present study show a higher riboflavin concentration in the milk of H subjects (Table 3).

Though no data is available for riboflavin intake during lactation, it is probable that the mother’s diet does not change drastically during after giving birth. This is confirmed by information that was possible to collect from some of the lactating subjects. Further, it is very likely that the composition of transition milk (day 13 to 14 postpartum) is greatly influenced by riboflavin intake at the end of pregnancy. In the present study, H subjects showed higher transition and mature milk riboflavin levels than did L subjects.

Breast milk riboflavin levels may have a significant influence on the nutritional status and health of suckling infants. Riboflavin is included among the antioxidative vitamins since it acts mainly as the essential cofactor of glutathione reductase, representing the most important cellular SH-bearing molecule [10]. At the moment of birth there is a rapid change from a relatively hypoxic to a relatively hyperoxic environment, with the risk of peroxidation reactions occurring which could damage the health of the newborn [10].

An adequate supply of riboflavin via the milk may be of extreme importance in certain clinical conditions. Light therapy for hyperbilirubinemia of the newborn is a common and readily employed means of therapy. This phototherapy has been recognized as a cause of riboflavin deficiency [39]; within 24 hours of phototherapy plasma riboflavin concentration decreases by about 50%. Low riboflavin concentrations indicate insufficient antioxidative protection through insufficient glutathione regeneration [10].

In agreement with Borrud et al. [29], it is probable that efforts to improve the nutritional status of pregnant and lactating women would be well served if all women of child bearing age were encouraged to maximize the nutritional quality of their diets. It is especially important to recommend an increase in the consumption of milk products during pregnancy, not only to raise riboflavin intake, but also that of calcium, the deficiency of which is associated with serious health problems in both mother and newborn [40–42].


   ACKNOWLEDGMENTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 ACKNOWLEDGMENTS
REFERENCES
 
This work was supported by grants of the Fondo de Investigaciones Sanitarias de la Seguridad Social (FISss) (Spain) (Ref. 92/1181).

Received . Accepted .


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 ACKNOWLEDGMENTS
 REFERENCES
 

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