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(Journal of Nutrition. 2001;131:325-330.)
© 2001 The American Society for Nutritional Sciences


Articles

Variability in Nutrient Intakes among Pregnant Women in Indonesia: Implications for the Design of Epidemiological Studies Using the 24-h Recall Method1

Viveka Persson*,{dagger}2, Anna Winkvist{dagger}, T. Ninuk, S. Hartini{dagger},**, Ted Greiner*, Mohammad Hakimi{ddagger} and Hans Stenlund{dagger}

* Section for International Maternal and Child Health, Department of Women’s and Children’s Health, Uppsala University, Uppsala, Sweden; {dagger} Epidemiology, Department of Public Health and Clinical Medicine, Umeå University, Umeå, Sweden; ** Nutrition Academy, Ministry of Health, Yogyakarta, Indonesia and {ddagger} Community Health and Nutrition Research Laboratory, Faculty of Medicine, University of Gadjah Mada, Yogyakarta, Indonesia

2To whom correspondence should be addressed at Section for International Maternal and Child Health, Entrance 11, Uppsala University, 751 85 Uppsala, Sweden. E-mail: viveka.persson{at}kbh.uu.se


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Few studies have assessed the reliability of dietary intake methods during pregnancy. Between 1996 and 1998, a longitudinal study of dietary intake during pregnancy was carried out among 451 women in Central Java, Indonesia. Six 24-h recalls were performed each trimester. We report here on intraindividual and interindividual variability in energy and nutrient intakes, as well as the reliability of the 24-h diet recall method. Implications of the use of different numbers of replicate days for estimating dietary intake and the relationships between dietary intake and health outcomes are also discussed. Intravariance-to-intervariance ratios were <1 for energy and carbohydrates and >1 for all other nutrients throughout pregnancy. Reliability analyses found good agreement (reliability coefficient >0.7) with three replicates for the macronutrients, but at least six replicates were needed for an agreement of >=0.6 for the micronutrients. To estimate true individual average intake with a precision of ±20%, six replicate recalls were sufficient for energy, carbohydrates, vitamin A, iron and vitamin C. In conclusion, mean intake of several nutrients can be reliably measured with the 24-h recall method, using a limited number of days. The nutrient of interest, the primary objectives and method of analyses should all be taken into account when planning sample size and number of replicates.


KEY WORDS: • diet recall • pregnancy • reliability • variance • Indonesia • humans


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Muchresearch and intervention in low-income countries aim at ensuring optimal nutritional status and health of the pregnant woman for her sake as well as that of the newborn. One factor of great importance in achieving this is an adequate dietary intake during pregnancy. To assess dietary intake during pregnancy, as well as to establish links between diet and maternal and child health, reliable estimates of energy and nutrient intakes are often needed. However, estimating dietary intake during pregnancy is challenging, because pregnancy is a period when women’s dietary intakes may vary significantly over time. Factors that can affect dietary habits during pregnancy include nutritional requirements (FAO 1988Citation , FAO/WHO/UNU 1985Citation ), activity (Banerjee et al. 1971Citation ), appetite (Coons 1933Citation ) and self-selected diet (Dickens and Trethowan 1971Citation ). Any dietary intake measurement is specific to the stage of pregnancy.

Information on variation in nutrient intake (intraindividual and interindividual) is required to guide decisions on the number of replicate measurements needed and on sample sizes. If too few replicate measures are taken or the sample size is too small, the statistical precision of intakes can be jeopardized and measures of diet-health outcome associations, such as correlations and relative risk, may be attenuated (Freudenheim et al. 1989Citation , Liu et al. 1978Citation , Sempos et al. 1985Citation , Walker and Blettner 1985Citation ). In contrast, taking too many replications or too large a sample wastes resources and disturbs respondents without serving any purpose.

Unfortunately, data assessing the precision of dietary intake methods during pregnancy are scarce and most come from the Western World (Nelson et al. 1989Citation , Osofsky 1975Citation , Rush and Kristal 1982Citation ). To our knowledge, only one study has reported patterns of dietary variability in women from a developing country (Launer et al. 1991Citation ). Food intake in that study was directly weighed for three consecutive d/mo from mo 6–9 in pregnancy among 743 Indonesian women.

The primary goal of the present study was to describe the intraindividual (within) and interindividual (between) variability in energy and nutrient intake in each trimester of pregnancy among women in a developing country. Second, because the weighing method presents difficulties in large studies, we wanted to elucidate how reliably the more practical 24-h recall method could be used in a developing country. Finally, we used our estimates of variance to show the implications of using different number of days for estimating true average intake as well as relationships between dietary intake and health outcomes.


    SUBJECTS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Study site and sampling design.

The study was conducted in Purworejo District, Central Java, Indonesia, which consists of 16 subdistricts and 494 villages. The total population is 750,000. Since 1994, the Faculty of Medicine at Gadjah Mada University has been operating a Community Health and Nutrition Research Laboratory in this area to support the Ministry of Health of Indonesia in developing and implementing a community health and nutrition surveillance program.

A two-stage cluster sampling method was used to select a 10% sample of households representative of the district. The sampling frame for the first stage consisted of a 20% sample of the enumeration areas or "wilcah," developed by the Central Bureau of Statistics for the 1990 census. In the second stage, the same number (101) of households was systematically sampled from each wilcah (Wilopo and team Community Health and Nutrition Laboratory 1997Citation ). From 1994 to 1998, each household was visited every 3rd mo for data collection. In addition, to identify new pregnancies, households with women likely to become pregnant (i.e., married women of reproductive age) were visited monthly. The nutritional status of women of reproductive age in the area is described in detail elsewhere (Nurdiati et al. 1998Citation , Winkvist et al. 2000Citation ).

Between April 1996 and October 1998, a cohort of 846 women in early pregnancy was recruited for a study on nutritional status during reproduction. Within this framework, dietary data were collected among a subsample of 493 women. The remaining 353 women were not included for the following reasons: refusal (n = 42); abortions, stillbirths or death (n = 32); being deaf, too shy or mentally ill (n = 23); migration (n = 21); or because of difficulties with the fieldwork during the economic crisis or because they were recruited before dietary assessments were started (n = 235). We also excluded women who did not have six complete 24-h recalls per trimester (n = 28, 43 and 67 in trimesters 1, 2 and 3, respectively). However, these women were only excluded from analyses for those trimesters where fewer than six recalls were completed. This caused the total study sample to drop from 493 to 451. Of these 451 women, 122, 406 and 356 women in trimesters 1, 2 and 3, respectively, were included in the dietary analysis, referred to as the study sample. Hence, 451 women with data on at least one trimester were included.

Dietary intake.

In each trimester, six 24-h recalls were used to estimate the dietary intake of the individual women. This number was based on the results of Launer et al. (1991Citation ) on random variation and was expected to be adequate to estimate intake of vitamin A and energy within an error of ±20%. These replications were randomly distributed among the five different days of the Javanese calendar on nonconsecutive days. The time lapses (mean ± SD) between the first and the sixth interview in the first, second and third trimesters were 30 ± 5, 37 ± 12 and 35 ± 8 d, respectively. Detailed descriptions of all foods, beverages and vitamin and mineral supplements consumed between 00:00 and midnight the previous day, as well as cooking methods, were recorded. Exact recipes were collected for each woman’s intake on each day. In total, information on >11,000 recipes was collected. Quantities were estimated using seven household utensils and ~20 types of food models (e.g., fish, tomato, banana and meat). The average weight of each type of food equivalent to the portion sizes and fitting into the household utensils was estimated to the nearest gram. To calculate nutrient intakes, the Indonesian nutrient composition database was used in most cases (Department of Health, Indonesia, 1995Citation , Hardiansyah and Briawan 1990Citation , Mahmud et al. 1990Citation ); for example, 92% of all energy and fat values came from these sources. Vitamin A values were predominantly taken from the food composition table of de Pee and Bloem (1999Citation ). The standard conversion factor of 1 µg retinol = 6 µg of ß-carotene was used (FAO 1988Citation ).

The data were collected by 22 trained female interviewers, and each respondent was interviewed at home by the same interviewer for all measurements. The interview lasted 1–2 h. Data form editing was conducted in the field within a few days, and supervisors checked all interviewers periodically. Ethical approval was received from the research ethics committees of the medical faculties of Gadjah Mada University, Yogyakarta, Indonesia, and Umeå University, Umeå, Sweden.

Statistical methods.

Data were analyzed with SPSS/PC statistical software (Version 8.0). The distribution of each nutrient (the mean for each trimester) was tested for normality before analysis. Results for slightly skewed variables were transformed to logarithmic scale.

To address the first study goal, variance components are reported as absolute values, ratios and coefficients of intraindividual (within) variation (CVw) .3 The Variance Components procedure in SPSS was used to calculate the absolute values, and eq. 1 shows how CVw was calculated:

(1)

where sw is the square root of the estimated intraindividual variance. To evaluate another source of variation, i.e., the trend in energy intake between each measurement occasion of each trimester (expressed as change per day), we applied a multilevel modeling technique (MlwiN 1.02). The first level was measurement occasion, and the second level was each woman. The model itself is a random regression model (Goldstein 1995Citation ):

where ß0 and ß1 are assumed to vary over the study population, and where Xij represents time between last menstrual period and measurement occasion.

To address our second goal, the reliability of 24-h recall, we used the intraclass correlation coefficient ({alpha} coefficient, rxx) as a function of number of recalls. This is a measure derived by Cronbach et al. (1972Citation ) that indicates the degree of agreement among repeated measures of some variable, in the present case, dietary intake. The Reliability Analysis procedure in SPSS was used for this purpose.

For the third goal, values of CVw were used to illustrate the required number of recalls per individual for the various nutrients (Willett 1990Citation ):

(2)

where n is the number of replicate days required, and Z{alpha} is the normal deviate for the percentage of times a confidence interval should cover the "true" average mean intake of an individual (e.g., Z{alpha} = 1.96 for 95% confidence). Finally, D is half the length of the interval, as a percentage of the mean.

In addition, the values of variance (sb2 and sw2) were used to illustrate the error in a regression analysis designed to look at the relation between dietary intake and some hypothetical outcome, with observed dietary intake as an independent variable. The error is measured by the ratio of the observed-to-true slope coefficients (Beaton et al. 1979Citation ), using eq. 3 :

(3)

where b0 is observed regression coefficient, bt is true regression coefficient, r is number of replications per individual, sb2 is estimated interindividual variance component and sw2 is estimated intraindividual variance component. Independent sample t tests were used to determine whether those excluded from dietary analyses (n = 395) were different from the study sample (n = 451) with respect to socioeconomic status and nutritional status.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Sample characteristics.

The age of the study sample was 28.8 ± 5.4 y, and the mean parity was 1.6 ± 1.4. The mean height and mid-upper arm circumference (MUAC) at 2 mo of pregnancy were 150.0 ± 4.9 and 25.1 ± 2.9 cm, respectively. Most (90%) lived in the rural areas, and 46% had >=7 y of schooling.

Representativeness of the study sample.

The sample of 451 women from the pregnancy cohort included in the dietary intake analyses did not differ significantly from those excluded (n = 395) with respect to age, parity, height, MUAC at 2 mo of pregnancy, altitude of residence, education, type of toilet or water source (P > 0.05). However, a greater proportion of those included in the analyses lived in the urban areas (10% versus 4.5%, P < 0.01), and fewer worked with agriculture (38% versus 47%, P < 0.05).

The mean height and age of the total sample of women of reproductive age (n = 13,094) in Purworejo were 149.1 ± 5.1 cm and 30.4 ± 9.7 y, respectively, of which both were different from the study sample (P < 0.05). Forty-six percent of these women had >=7 y of schooling, and 14% worked with agriculture, of which both were not different from the study sample. However, a greater proportion, 14% compared with 10%, lived in the urban areas (P < 0.01) (Nurdiati et al. 1998Citation ).

Variance component analyses.

Intravariance and intervariance components for the nutrient intake of the Indonesian women are shown by trimester in Table 1Citation . In all three trimesters, the ratio of intraindividual to interindividual variation was <1.0 for energy and carbohydrates. Also in all trimesters, the ratios were greatest for the micronutrients (iron, vitamins A and C, thiamin and calcium). For most nutrients, the ratios were lowest in the first trimester.


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Table 1. Intraindividual and interindividual variance components in trimester 1 (n = 122), 2 (n = 406) and 3 (n = 356) in dietary intake data for pregnant women in Indonesia

 
Values of CVw are shown in Table 2Citation . For most nutrients, the CVw was highest in the first trimester and lowest in the third. However, the differences in CVw between the trimesters were not large. We also evaluated those women with 18 complete 24-h recalls (n = 84) to determine whether fluctuations in CVw among these women were the same as the fluctuations in CVw for the entire study sample. The differences between the two samples were always <10% in all three trimesters (data not shown).


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Table 2. Number of 24-h recalls needed to estimate true average intake of pregnant women in Indonesia

 
Using random regression models, the slope (ß1) (SE), estimated during the first trimester, was 45.23 (7.82) (P < 0.001), indicating an average increase in intake of 45.23 kJ/d. For the second and third trimesters, the slope estimates were 12.62 (2.93) (P < 0.001) and 6.14 (3.13) (P = 0.05), respectively.

Reliability of 24-h recalls.

Table 3Citation indicates the {alpha} coefficient as a function of the number of 24-h recalls in trimester 2. The reliabilities for two recalls are low for the micronutrients but respectable for the macronutrients. When six recalls are used, the {alpha} coefficients for all nutrients fall above 0.55.


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Table 3. Alpha (reliability) coefficients (rxx) as a function of the number of 24-h recalls for pregnant women in Indonesia

 
Estimating true average intake.

The number of 24-h recalls needed to estimate true average intakes of individuals is presented in Table 2Citation . The number of replicates needed to estimate true average intake within an error of ±10% would be beyond the scope of most surveys for all nutrients. However, if an error range of ±20% is accepted, six replicates would be sufficient to estimate energy, carbohydrates, iron and vitamins A and C.

Dietary intake in regression analyses.

Relationships between dietary intake and health outcomes are often evaluated with regression analyses. The ratio of the observed to true regression slope as a function of the number of replicates, with the different nutrients as the independent variable, is shown in Table 4Citation . The results are based on the second trimester, but similar results were found for the other two trimesters. In contrast to CVw, the ratio of the observed to true regression coefficient is a direct function of the ratio of intravariation to intervariation. The attenuation of the true regression coefficient with decreased replicates was greatest for the micronutrients. The regression coefficient for energy and carbohydrates did not change substantially by reducing the number of days from 6 to 4.


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Table 4. Ratio of the observed to true regression slope with the various nutrients as independent variables, given different numbers of replicates for pregnant women in Indonesia

 

    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
This is the first population-based study to report nutrient variance ratios for women in a developing country throughout pregnancy. It is also the first study to investigate the reliability of the 24-h recall method in pregnancy in a developing country.

A major finding was that the intravariance-to-intervariance ratios were <1.0 for energy and carbohydrates in all three trimesters but were >1.0 for all other nutrients, except for protein in the first trimester. The largest variance ratios were found for the micronutrients. Hence, micronutrients are measured with greater error, meaning it will be more difficult to discover associations between micronutrient intake and certain outcomes than is the case for macronutrients. However, this study also showed that to estimate the mean intake of individuals with a precision of ±20% of the true intake, the current number of replicates (six) per individual would be sufficient for energy, carbohydrates, iron and vitamins A and C.

For most nutrients, a tendency toward larger CVw values in the first trimester was seen, perhaps because for the majority of nutrients, the intraindividual variation was largest during the first trimester. This may in turn have been because many women experienced nausea at that time. In addition, the nutrient intake was smallest that trimester, as shown in Table 1Citation .

In this study, we only accounted for intravariation and intervariation in nutrient intake. We could not examine the extent to which the estimate of usual intake contained other errors, such as nutrient content of foods, bioavailability of nutrients, nutrient interactions or errors in recording. We do believe that the food composition data we used were more accurate and complete than those used in most studies from Indonesia, because our project included extensive efforts to obtain details on recipes and to conduct additional examinations on the composition of foods that have not been analyzed previously.

Intraindividual variance has in earlier studies been shown to consist of several different components; these include method of data collection (Tarasuk and Beaton 1991Citation ), sequence of observation (Beaton et al. 1979Citation , Hartman et al. 1990Citation ), day-of-the-week effect (Beaton et al. 1979Citation , Hankin et al. 1967Citation , Hartman et al. 1990Citation , McGee et al. 1982Citation ) and seasonal differences (Hartman et al. 1990Citation ).

Intraindividual variance may also vary with changes in appetite, physical activity and intake that occur during pregnancy. We found an average increase of 45.23, 12.62 and 6.14 kJ/d during each trimester, although individual variation around this mean increase was large. Thus, there was no indication of fatigue in repeated recalls. Also, for the other nutrients, no trend of declining intake was seen according to sequence of the recall (data not shown).

To minimize the days of the week effect, we included all 5 d in the Javanese calendar, accounting for market days when dietary habits may change. The variation due to interview occasion was partitioned from the total intravariance but was found to be <5% of the total intravariance. The effect of season was not investigated in this study, although the effect on macronutrient intake in this area is likely to be small. The economic crisis in Indonesia, which started approximately in October 1997, could also have contributed to variation in intake. However, we compared the variance ratios of women who completed their pregnancy before the crisis (~50%) with those after the crisis and found them to be quite similar.

To our knowledge, the only other study that has evaluated variance components of pregnant women from the developing world is that of Launer and colleagues (1991Citation ) from East Java, Indonesia. Their results are derived from mo 6–9 in pregnancy among 743 women, whereas we present one estimate per trimester among 451 women. Launer and colleagues used a 3-consecutive-d food weighing method every month, whereas we used six nonconsecutive 24-h recalls within ~1 mo in each trimester. Although error may be greater (likely toward underreporting) in measuring individual intake with the 24-h recall method than with the direct weighing method (Block 1982Citation ), recall is cheaper and simpler, making it more suitable for larger studies. A recent study (Harrison et al. 2000Citation ) suggests that underreporting was less of a problem in one developing country, Egypt. It may also be easier with the 24-h recall method to assess nonconsecutive days, which gives a better estimate of the variance ratio (Block 1982Citation , Tarasuk and Beaton 1991Citation ). The 24-h recall method is considered suitable for measuring change over time (Tarasuk and Beaton 1992Citation ) and does not require literate respondents.

Launer and coworkers (1991Citation ) suggest that "whether or not the ratio of intra- to inter-individual variation derived from recall data would differ from those reported here depends on the type of error." For example, if errors in the recall data cause only a systematic shift away from the true mean, this may not affect the variance components or their ratio. However, other types of error could inflate or deflate the ratios.

Because the two studies not only used different methods but were conducted in different areas of Central Java 14 y apart, a comparison of results should be made with caution. Most likely, the socioeconomic situation has improved, resulting in the higher energy and fat intakes seen among our women. For protein and vitamin A, the variance ratios are comparable (ranging from 0.82 to 1.50 and 3.12 to 3.44, respectively, for the three trimesters in our study, compared with 1.28 and 3.8, in their study), as were the CVw’s for energy (0.20–0.26, compared with 0.24 in their study). However, for energy and fat, our ratios were lower (0.57–0.78 and 1.30–1.50, respectively, compared with 1.35 and 3.24 in theirs). In contrast, the CVw for protein and vitamin A in our study was slightly higher (0.31–0.35 and 0.21–0.24, respectively, compared with 0.25 and 0.19 in their study).

The studies available from Western countries on pregnant women are generally smaller (n = 60–225) and less complete samples than these two from Indonesia. Two studies used the 24-h recall method, either up to four repeated recalls taken during the second trimester (Rush and Kristal 1982Citation ) or up to four recalls before delivery without specifying time points (Osofsky 1975Citation ). A third one used weighed diet records (4 d at approximately monthly intervals from week 12–16) (Nelson et al. 1989Citation ). Their intravariance-to-intervariance ratios for energy (1.14–1.4), carbohydrates (1.18–1.2) (Nelson et al. 1989Citation , Osofsky 1975Citation , Rush and Kristal 1982Citation ) and vitamin A (4.9) (Nelson et al. 1989Citation ) were all higher than ours. For protein, they were either similar (1.38) (Rush and Kristal 1982Citation ) or higher (1.7–1.9) (Nelson et al. 1989Citation , Osofsky 1975Citation ). For vitamin C (1.2) (Nelson et al. 1989) and calcium, they were lower (0.98–1.8) (Nelson et al. 1989Citation , Rush and Kristal 1982Citation ). The reasons behind the mostly lower variance component ratios seen in our study could be that in developing countries, diets tend to be more monotonous and what people eat is more closely linked to income. In both cases, this would increase interindividual variation in relation to intraindividual variation.

Implications regarding the design of future studies.

Our population-based study using the 24-h recall method has generated results similar to a population-based study conducted in the same country using the more accurate weighing method. This has several implications for future research.

First, it suggests that the usual mean intake of several nutrients among pregnant women can be reliably measured using the more practical 24-h recall method. The reliability analysis (Table 3)Citation indicates that it is possible to obtain good agreement with two or three repeated recalls for the macronutrients. However, for vitamin A and vitamin C, six replications are not sufficient to obtain an "acceptable" value of ~0.7 for the {alpha} coefficient.

Second, our data on attenuation of the simple regression coefficients of the macronutrients suggest that it should be possible to use dietary intake data from 24-h recalls during pregnancy when evaluating the effect of diet on different outcomes of pregnancy. However, the regression coefficients of the micronutrients showed a much larger attenuation. Thus, for example, an association between the mother’s vitamin A intake and her breast milk vitamin A content would be difficult to find even with six replicate 24-h recalls, because the observed regression coefficient would be attenuated almost 35%.

Third, in our analyses, we evaluated the effect of using different numbers of replications on CVw, regression coefficients and {alpha} coefficients. When the primary objective of a study is to detect differences between groups of individuals, the choices also include increasing sample size. The choice between increasing sample size or increasing number of replicates would depend on factors such as costs of repeated dietary sampling relative to the cost of recruiting additional subjects as well as availability of subjects. However, Freudenheim et al. (1989Citation ) showed that for weaker underlying associations, nondifferential misclassification due to intraindividual variability induced bias in the odds ratio (toward unity) would persist, even with a larger sample size.

Fourth, our variance component ratios for macronutrients were generally lower than those reported for pregnant women in the industrialized world (Nelson et al. 1989Citation , Osofsky 1975Citation , Rush and Kristal 1982Citation ). Thus, it may not be appropriate to generalize findings on intraindividual-to-interindividual variance derived from the Western world to populations in low-income countries.

Finally, when using the 24-h recall method, the nutrient of interest, the primary objectives of the study and the methods of analysis to be used should all be taken into account when planning the sample size and number of replicate measures.


    FOOTNOTES
 
1 Supported by grants from Sida/SAREC (Swedish International Development Cooperation Agency, Department of Research Cooperation) and the World Bank through the Community Health and Nutrition Development Project of the Ministry of Health, Indonesia (IBRD loan no. 3550-IND). Data analysis and preparation of the manuscript were facilitated by support from STINT (The Swedish Foundation for International Cooperation in Research and Higher Education). Back

3 Abbreviations used: b0, observed regression coefficient; bt, true regression coefficient; CVw, coefficients of intraindividual (within) variation; MUAC, mid-upper arm circumference; Za, the normal deviate; r, number of replications per individual; sb2, estimated interindividual variation component; sw,2 estimated intraindividual variation component; sw, square root of the estimated intraindividual variation. Back

Manuscript received June 9, 2000. Initial review completed August 5, 2000. Revision accepted November 2, 2000.


    REFERENCES
 TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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