ORIGINAL

 

Breakfast, plasma glucose and b-hydroxybutyrate, body mass index and academic performance in children from Extremadura, Spain

Desayuno, glucosa y b-hidroxibutirato plasmaticos, índice de masa corporal y rendimiento académico en niños de Extremadura, España

 

 

M.ª D. Torres, I. Carmona, C. Campillo, G. Pérez y J. E. Campillo

Departamento de Fisiología. Facultad de Medicina. Universidad de Extremadura. Spain.

Correspondence

 

 

---

ABSTRACT

Objectives: Nutritional aspects of breakfast, plasma levels of glucose and b-hydroxybutyrate, body mass index and academic performance have been studied in urban and rural children (Extremadura, Spain).
Methods: Representative samples of schoolchildren (3 to 12 years old, random cluster-sampling in schools).
Results: Children's mean caloric intake with breakfast was 331 kcal. Rural population ingested more carbohydrates (46,9 ± 12,3% versus 43,3 ± 13,2% of the total caloric intake) and fewer lipids (40,5 ± 11,8% versus 43,9 ± 12,8% of the total caloric intake) than the urban population. Academic performance was significantly better in the children inhabiting the rural zone than in those of the urban zone. The glycaemia was higher in the urban than in the rural children, and that the contrary was the case for the b-hydroxybutyrate values. Neither glucose nor b-hydroxybutyrate levels were correlated with academic performance values. BMI was significantly increased in the urban versus rural children.
Conclusion: The present results emphasize the importance of breakfast and life style in the weight and the academic performance of children.

Key words: Breakfast. Glucose. Ketones. Body mass index. Academic performance. Children.

---

RESUMEN

Objetivos: En poblaciones rurales y urbanas de niños de Extremadura, España, se han estudiado aspectos nutricionales del desayuno, los niveles plasmáticos de glucosa y de b-hydroxibutirato, el índice de masa corporal y el rendimiento académico.
Métodos: Se tomaron muestras representativas de los niños (3 a 12 años de edad) aleatoriamente en las diferentes clases de los colegios seleccionados.
Resultados: La ingesta media de calorías en el desayuno fue de 331 kcal. La población rural ingería más carbohidratos (46.9 ± 12.3% versus 43.3 ± 13.2% del total de energía ingerida) y menos lípidos (40.5 ± 11.8% versus 43.9 ± 12.8% del total de energía ingerida) que la población urbana. El rendimiento académico fue significativamente mejor en los niños rurales que en los urbanos. La glucemia era mayor en los niños urbanos que en los rurales, y lo contrario sucedía con los valores de cetonemia. El IMC estaba aumentado significativamente en niños urbanos con respecto a los valores en niños rurales. En conclusión los resultados presentados enfatizan la importancia del desayuno y del estilo de vida en el peso y en el rendimiento académico de los niños.

Palabras clave: Desayuno. Glucosa. Cuerpos cetónicos. Índice de masa corporal. Rendimiento académico. Niños.

---

 

Introduction

Patterns of breakfast intake among children are a public health concern¹. Breakfast is one of the principal meals for children since it ends their long nocturnal fast and provides them with the necessary nutrients to face a morning of play and/or studies². Numerous studies have suggested that a deficient breakfast or its omission, even in populations with a good general nutritional status, can interfere with intellectual functions (cognition) and with the normal development of learning in school^3,4. Nevertheless, it has yet to be well established which are the metabolic, hormonal, or neurotransmitter factors involved in the relationship between breakfast and cognitive functions⁵. Also, the quality of breakfast depends partly on the life-style of children in a given area and on family traditions⁶.

The present study was designed to further explore the relationship between breakfast, overweight and school learning. It was analyzed the nutritional aspects of breakfast, the plasma levels of glucose and b-hydroxybutyrate, and the academic performance in two populations of children, one from an urban area (the city of Badajoz, 150,000 inhabitants, whose principal economic activity is in the services sector) and the other from a rural area (the town of Olivenza, 10,000 inhabitants, whose principal economical activity is agriculture), separated by 25 km, and both belonging to the Autonomous Community of Extremadura, Spain.

 

Methods

Representative samples of schoolchildren (3 to 12 years old) were selected in two cities (Badajoz, 150,000 inhabitants, and Olivenza, 10,000 inhabitants, at a distance of 25 km from each other) of the Autonomous Community of Extremadura, Spain, during the 2005-2006 school year. The children were selected by means of random cluster-sampling in schools. At a first stage, one school was selected in each city; at the second stage, the classes and the pupils were selected. Children reported by their parents to be suffering from any chronic disease were excluded from the study.

The study protocol was in accordance with the Helsinki Declaration guidelines and the European and Spanish statutary provisions governing research on human subjects⁷. The research protocol was formally approved by the Research Ethics Committee of the University of Extremadura. The study design was presented to the Board of Governors (Consejo Escolar) of each school, and then a letter containing complete information about the study and securing their written authorization was circulated to the parents of the children invited to participate in the study. The children were given the opportunity to refuse prior to the day of the survey, and their participation in the study was rewarded with a gift.

At the school, anthropometry and nutritional data were collected by a field team trained in anthromopetry and in the use of an adapted food-frequency questionnaire (FFQ) previously validated in Spain⁸. This team conducted the survey and obtained the relevant information from the children's parents. The nutrient database software used for the study was that corresponding to the Spanish database⁹. The diagnostic of obesity was applied when the BMI of a child exceeded the 95^th percentile for children of the same age and sex, the term overweight was applied when the BMI was at or exceeded the 90^th percentile for the same age and sex^10,11. Academic performance was evaluated by the each school's teachers in accordance with their usual procedures, quantifying it as: 1.0, very poor; 2.0, poor; 3.0, regular; 4.0, good; and 5.0, very good (arbitrary units).

Blood glucose and blood b-hydroxybutyrate levels were determined immediately before the morning break, and before the children ate their mid-morning food (at around 11 a.m.), by taking samples of fresh capillary whole blood from the fingers. The assays were performed using a MediSense Optium Blood Glucose and Ketone Sensor (Abbott Laboratories).

Results are expressed as mean ± SD. Data analysis and statistical evaluation was performed using SPSS for Windows. P-values < 0.05 were considered to indicate an acceptable level of significance.

 

Results

A total of 224 children were studied, aged from 3 to 12 years, and distributed by gender and population as given in table I. With respect to the BMI (kg/m²), the only significant difference (P < 0.05) observed was in the lower value corresponding to the children from the rural area (16.9 ± 3.4) relative to the value corresponding to the children from the urban area (18.4 ± 5.5). The prevalence of obesity and overweight was increased in urban (12.1% and 17.7% respectively) versus rural (8.2% and 12.9% respectively) children. The energy intake with breakfast ranged between 300 and 400 kcal for most children. The only significant difference (P < 0.05) was found between the energy intake of rural (353 ± 149 kcal) versus urban (312 ± 126) children. No significant differences were observed in the percentage of obesity or overweight related to the total energy intake during breakfast. Energy intake with breakfast increased with age until 8-9 years old, and then declined. It was noteworthy that a smaller percentage of the rural area children skipped breakfast (1%) than the urban children (4.04%).

Proteins comprised 12.7 ± 4.1% of caloric intake overall, and the values were similar for boys and girls, and for the urban and the rural groups. Carbohydrates comprised 44.9 ± 12.9% of the total energy intake overall, but now, while the values were similar for boys and girls, the percentage was significantly greater (P < 0.05) in the rural (46.9 ± 12.3%) than in the urban (43.3 ± 13.2%) children. This significant difference between the rural and the urban children was maintained when the absolute value of carbohydrate consumption was considered (table II). Total fat intake was 42.3 ± 12.2% of the energy intake overall, and was significantly lower (P < 0.05) in the rural (40.5 ± 11.8%) than in the urban (43.9 ± 12.8%) children. With respect to the distribution of the different types of fat, the greater consumption of total fats by the boys was maintained in a greater consumption of all the types of fat, including cholesterol (table II).

The intake of vitamins and minerals during breakfast was similar in boys and girls. The significant differences found in the intake of vitamins and minerals between the rural and the urban groups are given in table III. The breakfast of the rural children contained greater quantities of the vitamins thiamine, riboflavin, niacin, cyanocobalamin, folates, and vitamin D, and of the minerals iron, magnesium, and phosphorus.

Milk was part of the breakfast of 91.0% of the rural and 82.9% of the urban children (fig. 1). A typical breakfast of the children in the study consisted of milk with powdered cocoa and sugar, and a choice of biscuits, breakfast cereals, or bread. Some children (between 7 and 13%) consumed margarine or butter. Almost no child included fruit in their breakfast, whether whole or in juices.

The levels of glycaemia measured three hours after breakfast were within the normal fasting limits of glycaemia. It was noteworthy that the levels in the urban children were significantly greater (P < 0.001) than in the rural children (table I). There were also significant differences (P < 0.05) in the values of ketone bodies, but this time the values were higher in the rural than in the urban children. Academic performance (arbitrary units) also presented a higher value (P < 0.01) in the rural (3.8 ± 0.4) than in the urban (3.5 ± 0.9) children.

 

Discussion

Numerous studies have suggested that children's intake of nutrients with breakfast contributes to creating a favourable nutritional environment for the learning process and for physical exercise^2,6,8. It is not clear, however, which are the mechanisms that link the nutritional quality of breakfast with cognitive activities in school⁴. The learning process is complex, and depends on a multitude of non-nutritional as well as nutritional factors, including social, emotional, psychological, and life-style factors. In order to obtain more data on this interesting problem, it has been studied two populations of children in the Autonomous Community of Extremadura, Spain, with good nutritional and health status. One group of children were pupils of a school in Badajoz (a city of 150,000 inhabitants, service economy, a more modern life-style, and a high proportion of women sharing their work day between housework and a job away from home). The other children were pupils of a school in Olivenza (town of 10,000 inhabitants, agricultural economy, more traditional life-style, and where most women are solely occupied with household tasks).

The BMI distribution of the sample corresponded to that expected for this population group^10,11. Rural children, carrying a most active life style, presented the lower index of overweigh and obesity¹². In the present study was not found any significant correlation between total energy intake with breakfast and overweight. In those children with the lowest energetic breakfast (N = 39; 164.2 ± 31.9 Kcal) was detected a 10.2% of obesity and in that one with the highest energetic breakfast (N = 591.0 ± 101.2) an 8% of obesity.

The children's mean caloric intake with breakfast was 331 kcal (table II). This value is identical to that reported in the "enKid" study of a sample of more than 3,000 Spanish children⁸. The rural children of the present study, however, had a greater caloric intake with breakfast than the urban children, a finding that is contrary to that of the "enKid" study⁸ in which the equivalent values were less in rural than in urban areas.

The protein intake was similar in all the groups studied. The carbohydrate intake was greater in the rural than in the urban children. The boys ingested more fats than the girls in absolute terms, although this was simply a consequence of their greater total food intake, since in percentage terms there were no significant differences in fat intake. For the study population overall, the results differed from those of "enKid"⁸. In particular, the children of the present study consumed a greater percentage of fats relative to total energy intake at breakfast (42.3 ± 12.4%) than did those of the"enKid" study (34.7%).

The vitamin and mineral content of breakfast conformed in general to that recommended by most studies. Significant between-group differences were found only in the content of thiamine, riboflavin, niacin, vitamin B₁₂, folic acid, iron, magnesium, and phosphorus between rural and urban children. In general, given the nutritional data and the type of food consumed (fig. 1), the breakfast consumed by the rural population could be regarded as of higher quality⁸ than that of the urban population.

The endocrine and metabolic factors that affect the relationship between breakfast and cognitive functions in children are poorly understood. There have been numerous studies measuring the change in glycaemia, insulinaemia, and certain neurotransmitters^3,4, but very few measuring the levels of ketone bodies which may play a major role in this process¹³. Until recently the determination of ketone bodies required the extraction of a certain quantity of blood, so that the few studies that have been made were carried out in hospitals, and not in the child's natural environment¹⁴. Here, we used a system that allows the glycaemia and b-hydroxybutyrate levels to be determined simultaneously in a reliable and simple way from a single drop of blood obtained by pricking the finger. It was noteworthy that the glycaemia was higher in the urban than in the rural children, and that the contrary was the case for the b-hydroxybutyrate values. It is difficult to interpret these data in terms of the nutritional quality of the breakfast, since the rural population ingested more carbohydrates (46.9± 12.3% versus 43.3 ± 13.2% of the total caloric intake) and fewer lipids (40.5 ± 11.8% versus 43.9 ± 12.8% of the total caloric intake) than the urban population (table II). The findings could perhaps be attributed not to the acute effect of a single breakfast but to the chronic effect of a generally greater habitual physical activity and more traditional meals and life-style in the rural children¹². An incorrect diet and a sedentary life-style could lead to a situation of metabolic alteration in which homeostatic mechanisms would tend to maintain the circulating levels of glucose in the blood¹³.

The method that it has been used to establish academic performance possibly does not measure all the potentially confounding factors, but it has the advantage of reflecting the real situation as judged by the children's own teachers. Academic performance was significantly better in the children inhabiting the rural zone than in those of the urban zone. Neither the glucose nor the b-hydroxybutyrate levels were correlated with the values of academic performance. It is possible that this parameter is also influenced by chronic nutritional factors and by the children's life-style¹².

 

Acknowledgements

The study was made possible through a grant from Junta de Extremadura. The generous collaboration of the participating teachers, students and parents of the school "Francisco Ortiz Lopez" of Olivenza and the school "Nuestra Señora de la Soledad" of Badajoz are gratefully acknowledged.

 

References

1. Siega-Riz AM, Popkin BM, Carson T. Trends in breakfast consumption for children in the United States from 1965 to 1991. Am J Clin Nutr 1998; 67(Supl.):748-56.        [ Links ]

2. Nicklas TA, Bao W, Webber L, Berenson GS. Breakfast consumption affects adequacy of total daily intake in children. J Am Dietetic Assoc 1993; 93:886-91.        [ Links ]

3. Kleinman RE, Hall S, Green H, Korzec-Ramirez D, Patton K, Pagano ME, Murphy JM. Diet, breakfast, and academic performance in children. Ann Nutr Metab 2002; 46:24-30.        [ Links ]

4. Pollit E, Mathews R. Breakfast and cognition: an integrative summary. Am J Clin Nutr 1998; 67:804-13.        [ Links ]

5. Benton D, Parker PY. Breakfast, blood glucose and cognition. Am J Clin Nutr 1998; 67:772-78.        [ Links ]

6. Alaimo K, Olson CM, Frongillo EA, & Briefel RR. Food insufficiency, family income, and health in US preschool and school aged children. Am J Public Health 2001; 91:781-786.        [ Links ]

7. BOE; Boletín Oficial del Estado. 1993; Real Decreto 561: 14346-14364.        [ Links ]

8. Aranceta J, Serra-Majem L, Ribas L, Pérez-Rodrigo C. Breakfast consumption in Spanish children and young people. Public Health Nutr 2001; 4:1439-44.        [ Links ]

9. Mataix J, Mañas M, LLopis J, Martínez de Vitoria E. Tabla de Composición de Alimentos. Universidad de Granada, 1998 Granada, Spain.        [ Links ]

10. Dietz WH. Overweight in childhood and adolescence. New Engl J Med 2004; 350:855-57.        [ Links ]

11. Barrio R, López-Capape M, Colino E, Mustieles C, Alonso M. Obesidad y síndrome metabólico en la infancia. Endocrinol Nutr 2005; 52:65-74.        [ Links ]

12. Weiss R, Dziura J, Burget T, Tamborlane WV, Taksali SE, Yeckel CM, Allen K, Lopes M, Savoye M, Morrison J, Shervin RS, Caprio S. Obesity and the Metabolic Syndrome in Children and Adolescent. N Engl J Med 2004; 350:2362-74.        [ Links ]

13. VanItallie MD, Thomas H. Nufert BA. Ketones: Metabolism's Ugly Duckling. Nutr Rev 2003; 61:327-41.        [ Links ]

14. Pollit E, Cueto S, Jacoby ER. Fasting and cognition in well-and undernourished schoolchildren: a review of three experimental studies. Am J Clin Nutr 1998; 67:779-84.        [ Links ]

 

 

Correspondence:
J. E. Campillo.
Departamento de Fisiología. Facultad de Medicina.
Avda. de Elvas, s/n.
06071 Badajoz. España.
E-mail: campillo@unex.es

Recibido: 23-III-2007.
Aceptado: 01-IV-2007.