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Community and International Nutrition

Malnourished Children Treated in Day-Hospital or Outpatient Clinics Exhibit Linear Catch-Up and Normal Body Composition¹

Janaina das Neves^*, Paula A. Martins^*,2, Ricardo Sesso and Ana L. Sawaya^*

^* Department of Physiology, Discipline of Physiology of Nutrition, and Department of Medicine, Discipline of Nephrology, Federal University of São Paulo, São Paulo, Brazil

² To whom correspondence should be addressed. E-mail: paulamartins{at}ecb.epm.br.

	ABSTRACT

TOP ABSTRACT SUBJECTS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
The nutritional programming hypothesis proposes that early life malnutrition is related to an increase in body fat later in life. Brazilian boys and girls (n = 94; 4–14 y old) were studied. Malnourished children treated in a Nutrition Recovery Center, were followed up and divided into 2 groups: the Outpatient group (recovered after outpatient care, n = 28), and the Day-hospital group (recovered after day-hospital care, n = 38). They were compared with a Control group (healthy individuals without intervention, n = 28). Nutritional recovery was confirmed by anthropometry. Body composition was evaluated by dual-energy X-ray absorptiometry. Both recovered groups had a greater increase in height-for-age Z-scores than in weight-for-age Z-scores after treatment (P < 0.03). Body fat mass (kg) and the percentage of body fat were significantly lower in recovered groups of girls and boys compared with controls. Among boys, lean mass/height (kg/cm), fat-free mass (kg) and the fat-free mass index (kg/m²) were significantly lower in the Outpatient and Day-hospital groups than in Controls, but girls did not differ. Bone mineral content (BMC)/height (g/cm) did not differ between the recovered girls and the girls in the Control group (P < 0.15) or between the boys in the Day-hospital group and those in the Control group (P = 0.06). The Outpatient boys group had lower BMC/height than boys in the Control group (P = 0.02). This study demonstrates that when malnourished children receive adequate treatment, linear catch-up growth occurs and is followed by appropriate gain in lean body mass and BMC.

KEY WORDS: • nutritional recovery • body composition • DXA • food intake • Brazil

Until recently, treating malnutrition focused mainly on the rapid decrease of the high mortality rate associated with this disease. For this reason, nutritional recovery was based mainly on the consumption of energy-dense diets or formulas, with extra oil and sugar (1). Because the prevalence of severe malnutrition, especially wasting, is decreasing in the world, a greater concern is now focused on malnourished individuals living in poor urban areas (slums). The number of individuals living in these conditions is, in fact, increasing in many countries, including Brazil (2). This new condition is associated with impaired growth, a high prevalence of stunting, low physical activity, and consumption of foods with a poor nutritional profile, associated with an inadequate consumption of fruits and vegetables (3). In addition, these individuals have a markedly increased rate of noncommunicable diseases (4,5).

Several studies showed that early malnutrition may permanently "program" the individual toward an increase in or preservation of fat storage later in life (6–13). Recent studies in developing countries showed that stunting is paradoxically followed by a weight-for-height increase (14–16). Studies in Brazil, for example, found that short stature is strongly associated with overweight or obesity among adolescents and adults living in slums. In 1995, we showed a co-existence of obesity and malnutrition within the same family (17). The prevalence of stunting/obesity among adolescents was almost 2 times higher for girls (13%) compared with boys (8.8%) (17). Similar findings were reported for children from rural areas (18) and urban slums (19), even when food intake was low. Among adults living in urban slums, 30% were stunted in association with overweight/obesity (19), even when the food intake was 63% of the daily requirement (20).

Body composition studies in untreated stunted children reported an accumulation of fat tissue in preference to lean body mass (12,21). Childhood nutritional stunting is associated with impaired fat oxidation, a factor that predicted obesity in other at-risk populations (21). A prospective study of the body composition of stunted adolescents found that they accumulated more body fat than lean body mass over time (12). In addition, a similar prospective study showed that stunted girls had a lower resting metabolic rate associated with a higher rate of weight gain compared with nonstunted girls (22).

The objective of the present study was to evaluate the body composition of previously malnourished children and adolescents who adequately recovered their height and weight after being treated at the Nutrition Education and Recovery Center (CREN).³

	SUBJECTS AND METHODS

TOP ABSTRACT SUBJECTS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
    Experimental design. Children and adolescents (n = 94), aged 4–14 y, of both genders, living in the same neighborhood, were divided into 3 groups. The Control group consisted of 28 children and adolescents who had, at the time of the study, weight-for-age Z-scores ranging from 0 to +1.645 and height-for-age Z-scores from 0 to +2. The Outpatient group consisted of 28 recovered children and adolescents, with weight-for-age and height-for-age Z-scores ranging from –2 to –1.645 when admitted to treatment at CREN. The Day-hospital group consisted of 38 recovered children, who had weight-for-age Z-scores and height-for-age Z-scores lower than –2 when admitted to treatment in Day-hospital care at CREN. Both groups of recovered children had weight-for-age Z-scores and height-for-age Z-scores, during the protocol that were higher than –1.645 (5th percentile), which is the CREN criterion for discharging the patient. Outpatient and Day-hospital children were admitted between 1994 and 2002.

The children and adolescents who participated in the follow-up study were recruited and screened during the months of May and June 2001. The screening process included collecting blood samples to determine iron levels, and urine and stool samples to determine whether infections and parasites were present. When laboratory tests indicated the presence of anemia, infections, and/or parasites, these were treated before the protocol began. All the of children selected for screening were included in the research protocol. The protocol began in October 2001 and lasted until April 2004. The children were studied for a median time of 3 y after they were discharged from CREN (range: 6 mo to 7 y).

Controls were selected through home visits and anthropometric measurements in schools. The Control children belonged to the same communities as the recovered groups. The majority of the recovered children still had some contact with the center through outpatient care during the study.

CREN

CREN offers outpatient assistance to children with mild malnutrition and day-hospital care to those who show moderate/severe malnutrition.

    Day-hospital care. The daily follow-up of a child at the Center aims to provide overall improvement of the nutritional, cognitive, motor, psychological, and social status. The routine was adapted to the process of nutritional recovery, with 5 balanced meals/d, 1 h of sleep in the morning and 1 h in the afternoon. Moderate physical activities were performed to spare the child from excessive energy expenditure (because the children already expended energy to cover the distance from their home to the Center and back to their home every day).

The Center provided the customary diet that the children received in their homes. Meal times were planned with the teachers, so that the children learned to establish a routine, in addition to learning about good eating habits and hygienic practices. The diet was nutritionally adequate and made with typical Brazilian food staples, such as rice, beans, meats, fruits, and vegetables. The children also received iron and vitamin (A, B, C, and D) supplements in prophylactic doses (23). During the day, they engaged in educational activities and were divided into groups of 15 children, according to their age. The children stayed at the Center from Monday to Friday, from 0730 until 1730.

Pediatricians, nutritionists, social workers, psychologists, and teachers participated in the treatment. A nurse assistant carried out a daily follow-up of each child's health. A pediatrician monitored the clinical-laboratory and anthropometric progress of each child. A nutritionist monitored the children's diet during their stay at the Center, and carried out an individual nutrition intervention to correct problems identified during the treatment. A pediatrician, together with a nutritionist, provided outpatient consultation and follow-up after discharge. Laboratory tests (blood and stools) were done each semester. The parents were also involved in frequent activities such as periodical visits to their homes and social and psychological support. Parents also had the opportunity to engage in technical training classes and a series of other activities to reinforce and strengthen their social network. The methodology adopted by CREN for treating malnourished children was described in detail elsewhere (23–25). The discharge criteria for the Day-hospital group was a height-for-age or weight-for-age Z-score greater than or equal to –1.645. However, some children (n = 3) were discharged from the Day-hospital and continued the treatment at the Out-patient Clinic.

    Outpatient care. Children with mild malnutrition were seen by a pediatrician and a nutritionist to prevent and treat diseases and for dietary guidance. Follow-up appointments were set according to individual needs, but initially they were on a monthly basis. Laboratory tests were also performed every 6 mo. Families were seen by a social worker and when a severe lack of access to food was detected, they were given a basket containing the foods routinely consumed in the region such as rice, beans, pasta, or wheat flour. Educational activities with the parents included preparing meals and exchanging recipes in an experimental kitchen. The median number of visits of the Outpatient group was 4 (range: 2–17).

    Study procedures. The families were visited in their homes to assess the children's daily food consumption and to evaluate the socioeconomic status of the family. At the end of the same week, the children were taken to CREN for an anthropometric evaluation and pubertal staging, both done in the morning. In the afternoon of the same day, they were taken to UNIFESP to undergo bone densitometry and were then returned to their homes.

    Pubertal stages. A pediatrician determined the pubertal stages of the children following Tanner's criteria for boys (26) and girls (27). Children were classified as pubertal or prepubertal according to the cut-off points recommended by the WHO: breast stage = 2 for girls and genitalia stage = 3 for boys (28).

    Anthropometry. Body weight and height were evaluated according to the procedures recommended by Lohman (29). The children were weighed and measured in bare feet wearing underwear. Body weight was measured using an electronic scale (model SD-150; Country Technologies) with a 150-kg capacity and 10-g accuracy. Stature was measured using a standard stadiometer, with a precision to the nearest 0.1 cm. Children stood with their heels together touching the vertical pole, heads on the Frankfort plane.

The Epi-Info program, version 3.2, which makes use of the reference standards of the National Center for Health Statistics (30), was used to assess nutritional status. Weight-for-age and height-for-age Z-scores were determined with the 1977 growth charts and BMI-for-age (percentiles and Z-scores) with the 2000 growth charts.

Growth charts from 1977 were used to calculate weight-for-age and height-for-age because the study groups were defined according to the modality of intervention each child received, and this had been established initially according to the indices calculated with the 1977–1978 curves at the time the children were admitted. Because most children were admitted to the study and received interventions before the year 2000, we feel that reclassifying the groups according to the 2000 curves would introduce a bias in our classification.

    Body composition and bone mineral density. Body composition and bone mineral density (BMD) were assessed by dual-energy X-ray absorptiometry (DXA), using the Hologic densitometer (model QDR-4500 A; Hologic). Total body fat and lean mass were measured with the Enhanced Whole Body software (version 8.26; Hologic Inc.). A body composition phantom provided by the manufacturer was used before each set of measurements for quality control.

DXA provides a 3-component model for measuring body composition: body fat mass, lean mass, and total bone mineral content (BMC). From these, relative body fat, fat-free mass, and total BMD can be calculated.

Recent advances in DXA technology have allowed this procedure to be used more frequently in body composition analysis because it measures whole-body as well as regional bone mass, lean mass, and fat mass with low precision error (31,32). Other advantages of the DXA are the relatively quick scan time (5 min) and the minimal radiation exposure (33,34). The total radiation dose to the subject is <1.0 mRem (35).

    Dietary recall inquiry. An interviewer visited the families in their homes on 3 separate days (including a weekend day) to fill out the dietary questionnaire and determine the child's food intake during a 24-h period. These visits occurred in the same week in which the anthropometric and bone densitometry evaluation were performed. The energy content and composition of the diet were calculated using a computer program specially designed for Brazilian Food (36) and a Brazilian Food Composition Table (37). The program also determined the amount of high biological value protein in the child's diet, corresponding to the relative intake of animal-source protein. The data were analyzed according to the percentage of adequacy based on the Dietary Reference Intakes (DRI) (38). The macronutrient intake and respective percentage contribution in relation to total energy value were calculated, based on the following reference percentages: 10–15% protein, 50–60% carbohydrate, and 15–30% lipids. The micronutrient requirements adopted were based on age and gender, and any value ranging from 90 to 110% was considered adequate (39–41).

    Socioeconomic, family, and living conditions. A standardized questionnaire was used to obtain information on the socioeconomic, family and living conditions (17). The families were interviewed in their homes. The number of families who answered the entire questionnaire was 78.

Parents signed a Free Consent Form. The Research Ethics Committee of UNIFESP approved the study.

    Statistical analysis. The studied variables were age (y), group (Control, Outpatient, and Day-hospital), gender (boys and girls), pubertal stage (pubertal and prepubertal), weight (kg), height (cm), weight-for-age (Z-score), height-for-age (Z-score), weight-for age increment (Z-score), BMI-for-age (Z-score and percentiles), body fat (kg), body fat (%), lean mass/height (g/cm), fat-free mass (kg), fat-free mass index (kg/m²), bone mineral content (g), bone mineral content/height (g/cm), bone mineral density (g/cm²), nutrient intake variables (energy, protein, fat, carbohydrate, calcium, iron, zinc, vitamin C, and vitamin A) and socioeconomic variables (number of people per family, family income, per capita income, number of rooms, type of construction, flooring of the houses, safe water supply, sewage, level of formal education, and employment status). The differences among the 3 groups were tested with ANOVA, followed by Tukey's test for pair-wise comparisons. The differences between Outpatient and Day-hospital groups were determined by Student's t test (for nutritional status variables at baseline and increment). The analyses of body composition data were stratified by gender and because of the reduced number of children per group, the differences among the 3 groups were determined with the Kruskal-Wallis test and the differences between every 2 groups with the Mann-Whitney test. Differences in the distribution of category variables among the 3 groups and between every 2 groups were determined using the ² test. Weight-for-age and height-for-age increments (Z-score) were adjusted for baseline Z-scores, and food intake data were adjusted according to gender, age, and pubertal stages using analysis of covariance. Differences between weight-for-age and height-for-age increments (Z-score) in Outpatient and in Day-hospital groups were determined with the paired-samples t test. Analyses were carried out with the statistical software SPSS 10.0 for Windows (SPSS ), with = 0.05 for all analyses

	RESULTS

TOP ABSTRACT SUBJECTS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
    Time of treatment. A total of 52 boys and 42 girls were investigated. The median time between the beginning of the treatment and the follow-up evaluation in the Outpatient group was 3 y (range 1–7 y); in the Day-hospital group, the interval was 2 y (7 mo to 7 y). The median duration of treatment in the Outpatient group was 1.3 y (range 6 mo to 5 y) and in the Day-hospital group, it was 1.5 y (range 6 mo to 3 y).

To investigate how the duration of treatment affected the results, analyses were made by stratifying the sample into 2 groups: one above and one below the median value between the beginning of treatment and the follow-up date. The 2 groups did not differ significantly in any of the studied variables.

    Nutritional status. The ages of the groups did not differ at baseline or follow-up (Table 1). Upon admission to CREN, the Day-hospital group had significantly lower weight-for-age Z-scores but not height-for-age Z-scores than the Outpatient group. At follow-up, both treated groups had similar weight-for-age Z-scores and height-for-age Z-scores, but these were lower than those of the Controls. Nevertheless, the Outpatient and Day-hospital groups were above the cut-off value for normal height (74 and 79% of the Outpatient and Day-hospital group had Z-scores above –1.00, respectively) and weight (56 and 58% of the Outpatient and Day-hospital group had Z-scores above –1.00, respectively), with no significant differences between these groups. The increment in weight-for-age Z-scores and height-for-age Z-scores in the Day-hospital group did not differ from those in the Outpatient group. Weight-for-age Z-scores and height-for-age Z-scores increments did not differ for the boys or girls (data not shown). Both recovered groups had a higher increment in height-for-age Z-scores compared with weight-for-age Z-scores (P < 0.30, calculated from Table 1).

When analyzing the girls (including pubertal and prepubertal subjects), the difference in stature became significant between Control and recovered groups (P = 0.03). Therefore, lean mass/height and fat-free mass index for the recovered girls were significantly lower than those for the Control group.

    Bone mineral content (BMC) and bone mineral density (BMD). BMC analysis for the prepubertal children showed that the Outpatient group had lower BMC than the Control group (P < 0.05 for girls and boys) but BMC did not differ between girls in the Day-hospital group and girls in the Control group (P = 0.17); among the boys, however, the Day-hospital group had lower BMC than the Control group (P = 0.04) (Fig. 1A). BMC/height did not differ between the recovered girls and the girls in the Control group (P < 0.15); boys in the Outpatient group had significantly lower BMC/height than those of the Control group (P = 0.02) but this difference was not significant for the Day-hospital group (P = 0.06, Fig. 1B). BMD for the Outpatient, Day-hospital and Control groups was very similar for both girls and boys (girls P = 0.15 and P = 0.49, boys P = 0.11 and 0.95, Outpatient and Day-hospital respectively, Fig. 1C).

View larger version (15K): [in this window] [in a new window]   FIGURE 1  Whole body BMC (A), BMC/height (B) and BMD (C) of the Control, Outpatient, and Day-Hospital groups, including only prepubertal children. The box represents the interquartile range (50% of the values), the whiskers are the highest and lowest values (excluding outliers), and the line is the median, n = 5–18. Medians without a common letter differ, P < 0.05.

    Food Intake. Food intake in terms of energy, macronutrients, and some micronutrients was evaluated according to the DRI (38–41) (Table 4). The mean energy consumption over the 3 days surveyed did not differ among the 3 groups. The protein intake was adequate in the 3 groups but the Outpatient and Day-hospital groups consumed significantly more protein than the Control group. The lipid intake, although adequate in terms of total energy value, was replaced by carbohydrates in the Control and Outpatient groups, presenting an intake > 60% of the energy content. Fat, carbohydrate, calcium, zinc, vitamin A, and C intake of the 3 groups did not differ. Macro- and micronutrient intake did not differ between Day-hospital and Outpatient children, except for iron because the Outpatient group consumed less iron than the Day-hospital and Control groups. The intake of calcium, iron (except Control group), zinc, and vitamin A was <90% of recommended daily requirements, according to gender and age. Vitamin C consumption was above the recommended values. Compared with the Outpatient group, the Day-hospital group had a more adequate consumption of macro- and micronutrients. The 3 groups did not differ in the relative intake of animal vs. plant protein.

The socioeconomic and environmental information was gathered by means of a home visit questionnaire (Table 5). The 3 groups had very similar living conditions and were very poor. Of those who completed the questionnaire, approximately only half of the children's guardians were employed. The worst sanitation was found in the Day-hospital group (P < 0.05), in which open sewage was observed in 48% of the homes. Almost 15% of the children in the Day-hospital group lived in slum shacks.

	DISCUSSION

TOP ABSTRACT SUBJECTS AND METHODS RESULTS DISCUSSION LITERATURE CITED

    Nutritional recovery and body composition. The recovered girls gained more in height, leading to a gain in lean mass/height and fat-free mass, accompanied by a lower percentage of body fat. This was found for both outpatient assistance and day-hospital treatment. Among boys, the results were less evident. Although they had a lower percentage of body fat than controls, lean mass/height, fat-free mass, and fat-free mass index were also lower. Therefore, the present results showed an improvement in body composition for both severely and mildly malnourished children, but this was more evident among girls than boys.

When other anthropometric indices for the classification of nutritional status were used, such as BMI/Age percentiles, a large number of subjects in Outpatient and Day-hospital groups were still considered malnourished. However, in a study with British reference children of the same age group, the value for the fat-free mass index was similar to that of the present recovered groups (43). This finding indicates that the fat-free mass of the children treated in this study could be appropriate in both boys and girls.

BMC/height did not differ among the recovered groups and Control children, with the exception of Outpatient boys who had a lower BMC/height value. One possible reason for this significant impairment of bone content may be that the absence of a feeding intervention was particularly harmful for boys who received only Outpatient treatment. The results of total BMD reinforce the importance of an adequate treatment for nutritional recovery, not only for height but also for bone growth because both recovered groups had values similar to those of the controls.

The present results differ dramatically from another prospective study done with stunted adolescents. They lived in the same communities as the ones in this study but were never treated (12). These individuals accumulated more fat and had lower lean mass at follow-up (36 mo). One explanation for this difference may be the type of treatment that is offered to the children by CREN, as described previously. There is a direct link between the intake of animal foodstuffs and growth (44,45). Whenever animal protein intake is adequate, the daily requirements of iron, zinc, calcium, vitamin A, vitam-1in B-12, and riboflavin are met, and these are essential to a child's growth (46). A direct link between protein intake and lean mass was also demonstrated (47). According to Weisstaub and Araya (47), nutritional management is highly important because it may allow gain in height without an excessive increase in energy deposition, which may prevent obesity in the future. The intake of zinc and possibly other micronutrients is essential to guarantee that the recovered tissues have adequate composition (48).

A second explanation for the difference in body composition in relation to that of stunted adolescents (12) could be the age of the children of the present study. The children of the present study were younger (mean age, 7 y) than the children in the study done with nontreated stunted children (mean age, 13 y) living in the same community (12). Therefore, we have to consider that the children in the present study might have a greater potential for growth, i.e., gain stature and muscle mass, as well as better bone mineralization associated with lower body fat because this potential decreases with age. This could be the factor that enabled the younger group to undergo better catch-up growth, rather than the quality of rehabilitation. More studies are warranted to clarify these differences. We are not aware of other studies in recovered children that investigated this aspect.

    Nutritional recovery and food intake. The recovery in height and normal body composition found at follow-up indicate that the nutritional education and change in dietary habits that occurred at CREN may have continued after discharge even if the living conditions remained the same for these poor children.

Energy consumption did not differ significantly among the 3 groups. The energy intake for the children in the Control group was below their daily requirement. Energy intake was adequate for the Outpatient group and above the daily requirement for the Day-hospital group. These findings may indicate that the children and families, after receiving treatment at CREN, learned to give better attention to their food consumption, compared with controls.

In terms of macronutrient consumption, the percentage of adequacy was within the recommended levels. Pooled together, the present results show that Day-hospital and Outpatient treatment brought about a change in nutritional habits and types of food consumed by the children and their families that continued over time. The protein intake and growth data suggest that both groups did equally well in terms of food habits.

The present food intake results show more adequate food consumption among these low-income children than many studies in Brazil, thus reinforcing the importance of the nutritional intervention performed at CREN. One study, for example, reported that children presented an inadequate intake of carbohydrates and an excessive intake of lipids and proteins (49).

The same was found for mineral intake. Although calcium intake was below the recommended levels for the 3 groups, this is common among Brazilian children. In one study involving boys and girls (7–15 y) enrolled in Public Schools, the children's calcium intake was similar to that in our study (50). In addition, we found a significantly lower iron intake in the Outpatient group compared with the Control group. However the iron intake of the recovered children in this study was higher than those reported by other studies (51). Zinc adequacy ranged between 46 and 87% for the 3 groups. One study with obese and normal children also found decreased zinc consumption (48). Ascorbic acid consumption in all groups was above the recommended levels. For vitamin C, da Silva (48) showed percentages <90% (7 to 12 y) or <50% (13 and 15 y). In the present study, vitamin A intake was similar to that found by Gonçalves-Carvalho (50), who observed low vitamin A intake (66%) in children (10 and 11 y). Despite the fact that the micronutrient consumption of the children in this study was higher or similar to these other Brazilian studies, we do not consider the amounts to be adequate.

The socioeconomic information confirmed that all of the studied children had similar living and family conditions except for a poorer sanitary condition among the most severely malnourished children, i.e., those in the Day-hospital group. The lack of a proper sewage system was probably the main cause for the severity of malnutrition as indicated by many studies (52,53).

In conclusion, this study revealed that adequate treatment can lead to a linear growth catch-up and a normal body composition for malnourished children at follow-up after 2–3 y. The present study also shows that nutritional education and a change in dietary habits during childhood may persist after discharge even if the living conditions do not change for these poor populations. Additionally, this study shows that Day-hospital treatment improved the quality of recovery to a significant degree, especially in terms of total BMC and BMC/height among girls. The results on improvement of BMC and BMC/height for the Outpatient group were less evident, especially for boys. Finally, suitable treatment such as the one offered by CREN may be essential for a good quality of nutritional recovery and for a long-lasting health benefit. Future longer-term studies are required to evaluate the effects of this treatment on the prevention of chronic diseases, as described by many authors (11).

	ACKNOWLEDGMENTS

 
We thank Dr. Marise Lazareti Castro and Dr. Elizabeth Ribeiro Barro from the Department of Endocrinology of UNIFESP for DXA exams and Luiza Modesto for English review.

	FOOTNOTES

 
¹ Sponsored by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP).

³ Abbreviations used: BMC, bone mineral content; BMD, bone mineral density; CREN, Nutrition Education and Recovery Center; DRI, dietary reference intakes; DXA, dual-energy X-ray absorptiometry.

Manuscript received 24 March 2005. Initial review completed 16 May 2005. Revision accepted 16 December 2005.

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TOP ABSTRACT SUBJECTS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 

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