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Department of Nutritional Science and Dietetics, University of Nebraska, Lincoln, NE 68583
3To whom correspondence should be addressed.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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1.25 were observed in
30%, and plasma PLP concentrations 
30 nmol/L were observed in
25%; these values are considered indicative of vitamin B-6 inadequacy.
Similar percentages of male and female subjects had inadequate vitamin
B-6 status. Significantly more (P < 0.05) rural
children than urban had inadequate vitamin B-6 status as assessed by
the three indices. Vitamin B-6 inadequacy was found to be prevalent
among these Indonesian children, especially those living in rural
areas.
KEY WORDS: • vitamin B-6 status • alanine aminotransferase • plasma PLP • Indonesian children
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). Food and nutrition
intervention programs often are designed to help eliminate predominant
nutrition problems. A food supplementation program was implemented in
1996 in Indonesia (Syarief et al. 1996
) for this reason.
Information regarding the vitamin B-6 status of Indonesian children
does not exist, nor are data available on their intakes of the vitamin.
Currently, no single index of vitamin B-6 status is recommended. Most
investigators utilize two or more assessment indices in their studies
(Driskell 1994
, Leklem 1990
). Reynolds (1990)
indicates that the most fundamental, but not necessarily the
best, index of vitamin B-6 status of an individual may be the amount of
the vitamin in the typically consumed diet (Reynolds 1990
). Erythrocyte alanine aminotransferase (EALAT)4
activity coefficient is frequently utilized in the assessment of vitamin B-6 status and is considered to be a long-term status indicator
because of the life span of erythrocytes (Driskell 1994
,
Leklem 1990
). Plasma pyridoxal phosphate (PLP) level has
been the most acceptable and most widely used vitamin B-6 status index
in the last decade (Driskell 1994
). Leklem (1990)
suggested PLP as an appropriate additional index of vitamin B-6 status,
because it is the primary form of vitamin B-6 and it crosses all
membranes under postprandial conditions. In humans, plasma PLP
concentration has been correlated with dietary vitamin B-6 intake
(Leklem 1991
).
The objectives of the present study were to evaluate the vitamin B-6 status of third-grade elementary school children (ages = 8–9 y) in Bogor, West Java, Indonesia, by three commonly used status criteria: vitamin B-6 dietary intake, EALAT activity coefficient and plasma PLP concentration. Comparisons were made among data obtained by the three methodologies as well as between genders and rural vs. urban residential areas.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The study was conducted in elementary schools located in rural and urban residential areas in Bogor, West Java, Indonesia, during Fall 1997. The study was approved by the Institute of Research of Institut Pertanian Bogor (Bogor Agricultural University) in Indonesia and the Institutional Review Board of the University of Nebraska (Lincoln, NE).
Subjects.
Thirty-eight third-grade elementary school children in rural and 39
in urban areas voluntarily participated in this study. The subjects
included male and female students. These subjects came from three rural
and two urban randomly selected schools in Bogor, Indonesia; all
students eligible volunteered as subjects. Informed consent was
obtained from both the students and their parents. Subjects were
measured for height and weight while wearing light clothing but no
shoes (Gibson 1990
). Their parents were asked if they
perceived that their children were in good health; also, the parents
were asked whether their children took medications or supplements;
students taking these were not included in the study. Demographic
information (number of children, household size, father’s occupation,
educational level of each parent and family income) was also obtained
from the parents.
Dietary intake assessments.
A trained dietary interviewer obtained food intake information from the
subjects via two 24-h food recalls. One recall was for a weekday and
the other, a weekend day. Food models were used in estimating portion
sizes (Gibson 1990
). A pilot study was conducted by
observing 12 students characteristic of the study population while they
ate a meal, and the next day a trained dietary interviewer had these
students recall what and how much they ate at this meal. Basically,
these students accurately described what they had eaten. The decision
was made to interview the children to obtain dietary intake
information. The dietary energy and protein intakes were calculated
using the Indonesian Food Composition Table (Departemen Kesehatan Republik Indonesia 1995
). The dietary vitamin B-6 intakes were
calculated using analyzed vitamin B-6 values (Setiawan et al. 1999
). The estimated daily energy and protein intakes were
compared with the Indonesian Recommended Dietary Allowances (RDA) for
the appropriate age group (Muhilal et al. 1994
) and the
daily vitamin B-6 intakes with the 1998 RDA and Estimated Average
Requirements (EAR) intended for use in the United States and Canada
(Institute of Medicine 1998
).
Blood collection.
Venous blood (~20 mL) was collected from fasting subjects in two
EDTA-containing vacutainer tubes by a qualified phlebotomist
between 0800 and 1000 h. The samples were kept in crushed ice and
protected from light. Blood samples were centrifuged at 3000 x g and 5°C for 10 min. Plasma was frozen at -20°C
for plasma PLP analyses. Erythrocytes were treated as described by
Heddle et al. (1963)
utilizing saline and phosphate buffer, and frozen
at -20°C for EALAT analyses (Driskell and Moak 1986
).
EALAT and plasma PLP analyses.
EALAT activities were determined by the method of Tonhazy et al. (1950)
as modified by Heddle et al. (1963)
and Driskell and Moak (1986)
. The
procedure of Raica and Sauberlich (1964)
was used in measuring EALAT
activity coefficients. EALAT EC 2.6.1.2, converts alanine plus
-ketoglutarate to pyruvate plus glutamic acid. When erythrocyte
hemolysates were spiked with pyruvate and with alanine prior to
analyses, the percentage recoveries were 88 and 92%, respectively
(Driskell et al. 1985
). Pilot studies indicated that no
loss in enzymatic activity occurred when samples were frozen for 1 y as hemolysates prepared in phosphate buffer.
Plasma PLP concentrations were measured using radioenzymatic assay by
the method described by Chabner and Livingston (1970)
as modified by
Fries et al. (1981)
. This method is based on the measurement of
14CO2 evolved during the decarboxylation of
L-tyrosine-1-14C by PLP-dependent tyrosine
apodecarboxylase, EC 4.1.1.25, using a Scintillation Analyzer (Tri-Carb Liquid Scintillation Analyzer, Model 1900 TR;Packard Instrument Company,Meriden,CT). A recovery of 94% was obtained when plasma
samples were spiked with PLP before analyses. Pilot studies indicated
that no loss in plasma PLP concentration occurred when samples were
frozen for 1 y.
Statistical analyses.
Height and weight values were converted to height-for-age,
weight-for-age and weight-for-height Z-scores (WHO 1983
). Data were analyzed using the general linear model,
Duncan’s multiple range test, Chi-square and Pearson correlation
procedures of SAS (version 6.12; SAS Institute, Cary, NC). Differences
were considered significant at P < 0.05. The
percentages of subjects having low (Z-scores of -2) height-for-age
(stunted), weight-for-age (underweight) and weight-for height
(wasted) values (WHO 1995
) were calculated.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The urban groups had significantly lower (P < 0.05)
numbers of children in the family, more fathers having professional
rather than laborer positions, greater family incomes and higher levels
of fathers’ and mothers’ education than the rural groups. However,
household sizes of rural and urban groups were not different
(P 0.05). In the urban groups, most of the
households had two children (62%), fathers worked as professionals
(74%) and the level of fathers’ education (51%) and mothers’
education (49%) were senior high school graduate. In contrast, in
rural groups the highest percentage (32%) had five children, fathers
worked as laborers (50%) and the levels of fathers’ education (68%)
and mothers’ education (82%) were elementary school graduates. The
males were 103.6 ± 3.4 mo old and the females, 102.4 ± 3.8
mo (means ± SD).
Anthropometric measurements.
The height-for-age,weight-for-age and weight-for-height
Z-scores of the four groups of subjects were significantly
different (P < 0.0005)(Table 1
);however, these scores did not differ (P 0.05) due to residential area (rural vs. urban) or gender. Between 0
and 17% of the subjects in each group had Z-score values
indicative of their being stunted, underweight or wasted.
Height-for-age and weight-for-age Z-scores (r = 0.76, P < 0.0001), and weight-for-age and
weight-for-height Z-scores (r = 0.78, P
< 0.0001) were correlated.
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Dietary information obtained from the weekday 24-h recall was not
significantly different (P 0.05) from that of the
weekend, so the data were combined. The majority of the subjects also
reported that these were typical of their usual intakes. There were
significant differences (P < 0.05) between residential
areas (rural vs. urban) in food energy, protein and vitamin B-6 intakes
(Table 2
). However, intakes by gender did not differ (P 0.05).
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) indicated that subjects
in urban areas received significantly more (P < 0.05)
of the vitamin from meat, milk and fruit groups and not starch, fish,
egg, legume and vegetable groups (Table 3
).
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EALAT activity coefficients did not differ (P 0.05)
between residential areas or genders (Table 4
). However, the mean EALAT activity coefficient of rural females was
significantly higher (P < 0.05) than that of urban
females.
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0.05) due to residential area or
gender. However, the plasma PLP concentration of rural females was
significantly lower (P < 0.05) than those of other
groups. Plasma PLP concentrations and EALAT activity coefficients were negatively correlated (r = -0.54, P < 0.0001). A negative correlation (r = -0.47, P < 0.0001) was observed between daily vitamin B-6 intakes and EALAT activity coefficients. Daily vitamin B-6 intakes and plasma PLP concentrations were positively correlated (r = 0.54, P < 0.0001).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). Anthropometric
indices, expressed in terms of Z-scores, should be used in
evaluating anthropometric data from less industrialized countries
(WHO 1995
). This method measures the deviation of
anthropometric measurements from reference medians in terms of
Z-scores. Mean Z-score values for height-for-age,
weight-for age and weight-for-height of the children in the current
study were indicative of normalcy; however, some of the subjects did
have Z-score values (WHO 1995
) indicative of their
being stunted, underweight or wasted. The vast majority of Indonesian
children that served as subjects in the current study were not
malnourished as most of these Z-score values were within two
standard deviations of the median for well-nourished populations.
However, the prevalence of stunting, underweight and wasting may have
increased due to the recent monetary crisis in Indonesia. The
anthropometric measurements presented in the current study may be
useful in the establishment of normal ranges for Indonesian children.
The Indonesian RDA for energy and protein for children 7–9-y-old are
7.95 MJ/d and 37 g/d, respectively (Lembaga Ilmu Pengetahuan Indonesia 1999
). Nutrient intakes below recommended levels do not necessarily
indicate that the intakes are inadequate to meet the individual’s
requirements. However, it is appropriate to consider levels well below
the RDA to indicate risks to dietary adequacy; the existence of
deficiencies must be confirmed or rejected on the basis of biochemical
and/or anthropometric data. As an approach for determining adequacy of
diet, the method utilized involved using 2/3 RDA as the cutoff
point. The percentages of subjects having energy and protein intakes <
2/3 RDA were as follows, respectively: rural females (22.2%,
11.1%); rural males (5.0%, 5.0%); urban females (5.0%, 5.0%);
urban males (5.3%, 0.0%); all rural subjects (13.1%, 7.9%); all
urban subjects (5.1%, 2.6%); all females (13.1%, 7.9%); all males
(5.1%, 2.6%); and all subjects (9.1%, 5.2%). Rice provided about
half of the total food energy intakes of the subjects in the current
study.
The current researchers believe, as a result of the pilot study, that the subjects were able to accurately recall the foods that they had eaten. A limited number of foods are consumed by the typical Indonesian. Only 65 different foods were consumed by the subjects during these 2 d. This limited number of foods being consumed may have made it easier for the children in the current study to recall what they had eaten.
The estimated daily vitamin B-6 intakes in the current study (0.57
± 0.26 mg/d, mean ± SD) were lower than
published values for American children in different ranges of age.
Kirksey et al. (1978)
reported that the vitamin B-6 intake of 127
females (12–14-y-old) was 1.24 ± 0.70 mg/d (mean ± SD). The mean vitamin B-6 intake of 22 males and females
(2–9-y-old) was 1.10 mg/d (Lewis and Nunn 1977
); the
mean vitamin B-6 intake of 35 males and females (3–4-y-old) was 1.20
mg/d (Fries et al. 1981
). The estimated dietary vitamin
B-6 intake from the study of Driskell et al. (1985)
with 583 white and
black girls living in five Southern states in the U.S., 12–16-y-old,
was 1.20 ± 0.06 mg/d, mean ± SEM
The Indonesian RDA for vitamin B-6 has not been established. The 1998
EAR for vitamin B-6 for children utilizes the protein requirement for
growth in estimating a growth factor; the EAR has been used in setting
the RDA (Institute of Medicine 1998
). If the data from
the current study were to be used in establishing the equivalent of an
EAR for 8–9-y-old Indonesian children, one might utilize the data from
the rural female group. The rural female group (n = 18) had a median vitamin B-6 intake of 0.415 mg/d, and 44.4 and 50.0%
of this group had EALAT coenzyme coefficients and plasma PLP
concentrations (using 30 nmol/L rather than 20 nmol/L),
respectively, which are considered to be indicative of adequate status.
(The percentage of subjects having 30 nmol/L was similar to
that percentage considered adequate in the vitamin using EALAT activity
coefficients.) Therefore, about half of the children in this group had
adequate vitamin B-6 status as judged by these two biochemical indices.
If the EAR is estimated to be 0.415 mg/d, and an RDA is calculated
according to the Institute of Medicine (1998)
, the RDA would be
estimated to be 0.415 multiplied by 1.2 or about 0.5 mg/d. Likewise,
the median vitamin B-6 intake of rural subjects (n
= 39) was 0.425 mg/d, and 57.9 and 60.5% of these subjects had
EALAT activity coefficients and plasma PLP values indicative of
adequate vitamin B-6 status. Utilizing these values in the calculation,
the estimated EAR for vitamin B-6 would be 0.425 mg/d, and the
estimated RDA, 0.51 mg/d. This estimation is comparable with the 1998
Dietary Reference Intakes for 4–8-y-old children from the USA and
Canada; these values are an EAR of 0.5 mg of vitamin B-6/d and a RDA of
0.6 mg/d (Institute of Medicine 1998
). This method of
estimation has limitations including there being a limited number of
subjects in the rural female groups as well as in the whole study.
However, this estimation might be utilized until such time that
additional data are available, and this estimation does agree well with
the 1998 RDA. Hence, it is appropriate to compare the dietary intakes
of these Indonesian children to the 1998 EAR and RDA for vitamin B-6.
The EAR (Institute of Medicine 1998
) may be used to
estimate the prevalence of inadequate nutrient intake. The 1998 EAR for
vitamin B-6 is 0.5 mg for children 4–8-y-old and 0.8 mg for those
9–13-y-old. In that 66 of the 77 subjects were 8-y-old, the EAR for
4–8-y-old (0.5 mg/d) was utilized for comparisons. Utilizing the
method of Guenther et al. (1997)
in calculating usual intakes, the
percentages of subjects in the current study consuming less than the
EAR were as follows: rural females (72.2%), rural males (65.0%),
urban females (45.0%), urban males (36.8%), all rural subjects
(68.4%), all urban subjects (38.5%), all females (57.9%), all males
(51.3%) and all subjects (54.5%). Significantly more
(P < 0.05) rural subjects than urban had
inadequate vitamin B-6 intakes as assessed using this variable.
However, similar percentages of male and female subjects had inadequate
vitamin B-6 intakes.
Requirements of children for vitamin B-6 are based on relatively few
studies. There are no well-designed feeding studies that have
evaluated vitamin B-6 requirements, and no experimental studies have
been conducted to directly determine requirements as related to protein
intake. Published data are available for dietary vitamin B-6 intakes
and status (Driskell 1994
, Leklem 1991
).
Hence, the requirement for vitamin B-6 for children may be estimated
assuming that a direct relationship between protein intake and vitamin
B-6 requirement exists (Leklem 1991
, Driskell 1994
), or that a proportional relationship exists between
vitamin B-6 requirements and the protein requirement for growth
(Institute of Medicine 1998
).
The dietary vitamin B-6/protein intake ratio has been expressed as
0.020 mg/g (Leklem 1991
). Ninety-nine percentage of
the subjects in the present study reported consuming <0.020 mg of
vitamin B-6/g protein. A study with black and white girls (ages = 12–16 y) living in Virginia found that 58% of the 186 subjects
reported consuming <0.020 mg vitamin B-6/g protein (Driskell and Moak 1986
). Another study with younger children (ages
= 2–9 y) reported that 59% of 22 subjects consumed <0.020 mg of
vitamin B-6/g protein (Lewis and Nunn 1977
). Using
2/3 of the vitamin B-6/protein ratio value (or <0.013 mg
vitamin B-6/g protein), the percentage of the subjects in the current
study having ratios less than the cutoff was 74%.
Protein requirements of Southeast Asian countries, including Indonesia,
have been adjusted by the net protein utilization of 60–70 for the
protein quality of the diet (Tee 1998
). Studies by the
Nutrition Research and Development Center, Bogor, Indonesia, reported
that the protein digestibility of the typical Indonesian diet was about
85%. Moreover, based on the consumption survey, the amino acid score
for proteins consumed by Indonesian school children was 76
(Muhilal et al. 1994
). Adjustment for the Indonesian
dietary pattern may be made by deriving a weighted digestibility factor
based on the digestibilities of the protein sources consumed and the
amino acid score. The vitamin B-6/protein ratio of the subjects in the
current study may also be adjusted, taking into account the protein
digestibility (85%) and the amino acid score (76) of typical
Indonesian diet. The mean ratio of 0.011 mg of vitamin B-6/g protein
becomes 0.018 mg of vitamin B-6/g protein following adjustment. Hence,
after adjustment, 74% of the subjects in the current study reported
consuming < 0.020 mg of vitamin B-6/g protein, the recommended
ratio (Leklem 1991
).
Leklem (1990)
suggested that an EALAT activity coefficient <1.25 was
indicative of adequate vitamin B-6 status. The EALAT activity
coefficients of all subjects in the current study was 1.20 ± 0.16, mean ± SD The percentages of subjects in the
current study who had EALAT activity coefficients 1.25 were as
follows: rural females (55.6%), rural males (30.0%), urban females
(10.0%), urban males (26.3%), all rural subjects (42.1%), all urban
subjects (17.9%), all females (31.6%), all males (28.2%) and all
subjects (29.9%). Significantly more (P < 0.05)
rural subjects than urban had inadequate vitamin B-6 status as assessed
by the EALAT activity coefficient index. However, similar percentages
of male and female subjects had inadequate vitamin B-6 status as
indicated by this parameter.
The EALAT activity coefficients in the current study were higher than
published values for children in the U.S. Driskell et al. (1985)
reported that the EALAT activity coefficients of the adolescent girls
were 1.14 ± 0.01, mean ± SEM, and 13% of the
subjects had EALAT activity coefficients 1.25.
Leklem (1990)
also suggested that a plasma PLP >30 nmol/L be
considered as being indicative of adequate vitamin B-6 status. Plasma
PLP concentrations of the subjects in the current study were 54 ± 30 nmol/L (means ± SD). The percentages of subjects
having plasma PLP concentrations 30 nmol/L were as follows:
rural females (50.0%), rural males (30.0%), urban females (5.0%),
urban males (15.8%), all rural subjects (39.5%), all urban subjects
(10.3%), all females (26.3%), all males (23.1%) and all subjects
(24.7%). Significantly more (P < 0.05) rural
subjects than urban had inadequate vitamin B-6 status as assessed by
plasma PLP concentrations. However, similar percentages of male and
female subjects had inadequate vitamin B-6 status as assessed by this
index. Other investigators have proposed that a plasma PLP
concentration < 20 nmol/L is indicative of inadequacy
(Institute of Medicine 1998
, Liu et al. 1985
). In the present study, only two rural males (10.0% of
group) had plasma PLP <20 nmol/L.
These two biochemical indices of vitamin B-6 deficiency were reflective of the vitamin B-6 intakes of children in the present study. The dietary vitamin B-6 intakes of subjects having adequate status as judged by EALAT activity coefficients (<1.25) and plasma PLP concentrations (>30 nmol/L) were as follows: (means ± SD) 9-y-old subjects, 0.66 ± 0.28 mg/d; 8-y-old subjects, 0.67 ± 0.22 mg/d; and 8–9-y-old subjects, 0.66 ± 0.23 mg/d.
A metabolic study on the effect of a high protein diet (1.55 g protein/kg body weight) from either animal or plant sources on the vitamin B-6 requirement of young women was done by Kretsch and co-workers (1982). Most biochemical indices were normalized at an intake of 0.015 mg of vitamin B-6/g protein, with the rest being normalized at 0.020 mg of vitamin B-6/g protein with the exception of total urinary vitamin B-6 which was not normalized. Similar findings were observed for both plant protein and animal protein diets at this high protein intake. However, this may not be true if a diet lower in protein had been fed. The subjects in the current study reported consuming a diet high in protein.
Both rural and urban subjects consumed noodles providing vitamin B-6 (0.051 and 0.058 mg/d, respectively), and noodles are manufactured by large-scale producers; if the decision were made to fortify a food(s) in order to help students and others meet their vitamin B-6 requirements, noodles may be the ideal food to fortify.
All the three commonly used status criteria indicated that the
percentages of subjects with vitamin B-6 inadequacy was significantly
higher (P < 0.05) in rural than urban areas
(Fig. 1
). About 40% of rural and around 10% of urban children included in
this study were found to have inadequate vitamin B-6 status, and almost
70 and 40% of rural and urban children, respectively, had inadequate
intakes (<EAR) of the vitamin. Based on these data, elementary
children in Indonesia need to be encouraged to consume vitamin B-6
dense foods that are inexpensive and locally available. These foods
include plantain, banana, mango, water spinach and fish
(Setiawan et al. 1999
). Vitamin B-6 inadequacy appears
to be a prevalent nutritional problem in Indonesian school children,
particularly those in rural areas.
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FOOTNOTES |
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2 Current address: Jurusan Gizi Masyarakat dan Sumberdaya Keluarga, Fakultas Pertanian, Institut Pertanian Bogor, Kampus Darmaga, Bogor, Indonesia.
4 Abbreviations used: EALAT, erythrocyte alanine aminotransferase; EAR, 1998 Estimated Average Requirement; PLP, pyridoxal phosphate; RDA, recommended dietary allowance
Manuscript received June 9, 1999. Initial review completed August 2, 1999. Revision accepted November 12, 1999.
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