**3.1 Daily energy expenditure structure**

Unlike basal metabolism, which is the minimum level of body energy expenditure, average daily metabolism includes the sum of all expenditures associated with the realization of various body functions. Food processing and digestion, thermoregulation and muscle activity are the most power-consuming functions. Unfortunately, there is almost no data in literature on the energy value of mental activity (not taking into consideration the indirect calculations by Holliday, 1971).

Fig. 3. Age changes in contribution of various organs and tissues into the structure of human basal metabolism (After: Holliday, 1971; Kornienko, 1979; modified)

Energy Metabolism in Children and Adolescents 127

The rate of heat production is considerably increased after food consumption, despite of lack of muscle activity, and it remains elevated for 2-3 hours (depending on the structure of food and other factors). Though the thermogenic effect of food is a known phenomenon and has been studied since the end of the 19th century, there is still no single opinion about its reasons and occurrence mechanisms. The simplest explanation, which states that extra energy production is required to activate a motor function of the gastrointestinal tract, has not been borne out by experiments: the thermogenic effect of glucose cannot be recovered in patients with diabetes and lab animals, even though carbohydrate is absorbed to the

Today the most probable reason considered for the thermogenic effect of food is the effect of enterohormones produced by the duodenum epithelium. For example, it has been proven that the lack of these hormones in blood results in a lower body temperature, meaning heat production (Ugolev et al, 1976). But even in this case it is unclear which particular tissue accounts for extra heat production. Recently brown adipose tissue has been considered as the reason (Himms-Hagen, 1989; Nedergaard & Cannon, 2010), which, according to recent data, is preserved in adults (Nedergaard et al., 2007) and maintains substrate homeostasis

A unique systematic research of age changes in the thermogenic effect of food substance (glucose) in school children was made in the laboratory of I.A.Kornienko (Kornienko et al, 1984). A standard test was used to evaluate glucose tolerance during this study: glucose was taken orally on an empty stomach in quantity proportional to mass (1g/kg). Content of glucose in blood in such a probe is usually increased during 30 minutes after intake and gradually normalizes within 2-3 hours. As glucose increases, with some delay (about 0.5 hours) oxidation processes start in the body, and in 3 hours the oxygen consumption levels return to the primary level. Total intensification of energy production with age for children

The given data proves that reactivity of oxygen metabolism decreases with age, meaning efficiency of mechanisms providing homeostasis increases. The difference in age dynamics of thermogenic glucose effect for boys and girls is the most interesting phenomenon. It is known that adult women, on average, have a better tolerance to glucose than men (Korkushko &

Age, years Boys Girls

Table 1. Total thermogenic effect of glucose (per oral 1 g/kg) for school children for 3 hours

In the same research (Son'kin et al., 1975) it was proved that glucose put into the body depends considerably on their body constitution: children of 11-12 years with a low fat content in the body of no less 1/3 introduced glucose is oxidized in process of a thermogenic response to its putting into the body, while children with a high fat content a thermogenic response to input of glucose is considerably less. Similar results for adult

7 – 8 2.125 + 0.16 (n=18) 1.825 + 0.14 (n=23) 11 – 12 1.255 + 0.10 (n=22) 1.365 + 0.11 (n=21) 15 – 17 0.585 + 0.06 (n=16) 1.060 + 0.08 (n=14)

of 7-8 up to 15-17 years is considerably reduced, especially for boys (Table 1).

Orlov, 1974). Possibly, the given data reflects the formation of such sex differences.

persons are described in press of the last years (Nedergaard & Cannon, 2010).

of observation (kcal/kg, M±m) (After: Kornienko et al., 1984)

**3.3 Specific – Dynamic (thermogenic) effect of food** 

bloodstream and is extracted with urine (Lusk, 1919).

(Son'kin et al., 2010).

#### **3.2 Functional range**

Various body tissues can change their metabolic activity to a different degree, ranging from rest to maximum functional activity. It depends on the organization of metabolic paths in cells that form the corresponding tissue. Based on content and activity data of vital energy ferments in body tissues, Demin (1983) calculated the hypothetic values of minimum and maximum metabolic activity for the liver, brain and muscles of a young man (Fig. 4). Characteristics of the functional range in skeletal muscles obtained using this method are close to the actual measured maximum energy expenditure (Son'kin, 1990; Kornienko, et al, 2000). As seen in fig. 3, muscles have both the highest potential for metabolic activity and the widest functional range. It should be noted that the maximum level of functional activity is carried out through the anaerobic metabolic processes, not limited by the possibilities of mitochondrial oxidation. The functional range value of various tissues can be affected differently depending on age. According to Demin (1983), this value for the brain is at its peak in childhood; for the liver it stays more or less the same at all periods of postnatal ontogenesis; for skeletal muscles it considerably increases from birth to the end of puberty.

Fig. 4. Comparative characteristic of functional range in various tissues of human body (calculation for a young man) (After: Demin, 1985; modified)

The intensity of body functions in a child is much higher than of an adult. The rate of children's basal metabolism is 1.5-2 times higher, but the maximum activity level is considerably lower than that of an adult. This results in a smaller functional range, and that makes the child body's existence more stressful.

The high intensity of energy metabolism in children becomes particularly obvious when you look at the fact that the child's body reacts with higher intensity to an impact equal in power, demonstrating a higher lability of autonomic systems and metabolic processes. These differences are well known, when talking about muscle activity (Åstrand, 1952; Kornienko et al, 2000). The fact that similar differences are evident in metabolic reactions to other functional loads, in particular food load, is less known.

Various body tissues can change their metabolic activity to a different degree, ranging from rest to maximum functional activity. It depends on the organization of metabolic paths in cells that form the corresponding tissue. Based on content and activity data of vital energy ferments in body tissues, Demin (1983) calculated the hypothetic values of minimum and maximum metabolic activity for the liver, brain and muscles of a young man (Fig. 4). Characteristics of the functional range in skeletal muscles obtained using this method are close to the actual measured maximum energy expenditure (Son'kin, 1990; Kornienko, et al, 2000). As seen in fig. 3, muscles have both the highest potential for metabolic activity and the widest functional range. It should be noted that the maximum level of functional activity is carried out through the anaerobic metabolic processes, not limited by the possibilities of mitochondrial oxidation. The functional range value of various tissues can be affected differently depending on age. According to Demin (1983), this value for the brain is at its peak in childhood; for the liver it stays more or less the same at all periods of postnatal ontogenesis; for skeletal muscles it considerably increases

Fig. 4. Comparative characteristic of functional range in various tissues of human body

The intensity of body functions in a child is much higher than of an adult. The rate of children's basal metabolism is 1.5-2 times higher, but the maximum activity level is considerably lower than that of an adult. This results in a smaller functional range, and that

The high intensity of energy metabolism in children becomes particularly obvious when you look at the fact that the child's body reacts with higher intensity to an impact equal in power, demonstrating a higher lability of autonomic systems and metabolic processes. These differences are well known, when talking about muscle activity (Åstrand, 1952; Kornienko et al, 2000). The fact that similar differences are evident in metabolic reactions to

(calculation for a young man) (After: Demin, 1985; modified)

other functional loads, in particular food load, is less known.

makes the child body's existence more stressful.

**3.2 Functional range** 

from birth to the end of puberty.

#### **3.3 Specific – Dynamic (thermogenic) effect of food**

The rate of heat production is considerably increased after food consumption, despite of lack of muscle activity, and it remains elevated for 2-3 hours (depending on the structure of food and other factors). Though the thermogenic effect of food is a known phenomenon and has been studied since the end of the 19th century, there is still no single opinion about its reasons and occurrence mechanisms. The simplest explanation, which states that extra energy production is required to activate a motor function of the gastrointestinal tract, has not been borne out by experiments: the thermogenic effect of glucose cannot be recovered in patients with diabetes and lab animals, even though carbohydrate is absorbed to the bloodstream and is extracted with urine (Lusk, 1919).

Today the most probable reason considered for the thermogenic effect of food is the effect of enterohormones produced by the duodenum epithelium. For example, it has been proven that the lack of these hormones in blood results in a lower body temperature, meaning heat production (Ugolev et al, 1976). But even in this case it is unclear which particular tissue accounts for extra heat production. Recently brown adipose tissue has been considered as the reason (Himms-Hagen, 1989; Nedergaard & Cannon, 2010), which, according to recent data, is preserved in adults (Nedergaard et al., 2007) and maintains substrate homeostasis (Son'kin et al., 2010).

A unique systematic research of age changes in the thermogenic effect of food substance (glucose) in school children was made in the laboratory of I.A.Kornienko (Kornienko et al, 1984). A standard test was used to evaluate glucose tolerance during this study: glucose was taken orally on an empty stomach in quantity proportional to mass (1g/kg). Content of glucose in blood in such a probe is usually increased during 30 minutes after intake and gradually normalizes within 2-3 hours. As glucose increases, with some delay (about 0.5 hours) oxidation processes start in the body, and in 3 hours the oxygen consumption levels return to the primary level. Total intensification of energy production with age for children of 7-8 up to 15-17 years is considerably reduced, especially for boys (Table 1).

The given data proves that reactivity of oxygen metabolism decreases with age, meaning efficiency of mechanisms providing homeostasis increases. The difference in age dynamics of thermogenic glucose effect for boys and girls is the most interesting phenomenon. It is known that adult women, on average, have a better tolerance to glucose than men (Korkushko & Orlov, 1974). Possibly, the given data reflects the formation of such sex differences.


Table 1. Total thermogenic effect of glucose (per oral 1 g/kg) for school children for 3 hours of observation (kcal/kg, M±m) (After: Kornienko et al., 1984)

In the same research (Son'kin et al., 1975) it was proved that glucose put into the body depends considerably on their body constitution: children of 11-12 years with a low fat content in the body of no less 1/3 introduced glucose is oxidized in process of a thermogenic response to its putting into the body, while children with a high fat content a thermogenic response to input of glucose is considerably less. Similar results for adult persons are described in press of the last years (Nedergaard & Cannon, 2010).

Energy Metabolism in Children and Adolescents 129

the child's body constitution, therefore it is activated in the last turn, if temperature of the

High activity of special mechanisms of thermogenesis in infants is connected not only with small size and large relative surface increasing heat insulation, not only with low heat insulation of cutaneous coverings, but with a relatively low level of basal metabolism, which has been noted before in this paper. Within the first year of life all these parameters are changing and the chemical thermoregulation activity is reduced. For a child of 5—6 months the importance of physical thermoregulation is considerably increased; it makes the temperature threshold and latent period of an interscapular brown adipose tissue activation almost double compared with the same parameters for infants 1-2 months old (Gohblit et al,

Under usual conditions the child older than 3 years old has a high value of heat flow in relation to the body surface unit, and heat insulation of cutaneous coverings is low, therefore children's skin is practically always warm. Even at the age of 4.5—5 years for girls and 5.5—6 years for boys the body heat insulation is very low: 0.226 + 0.003 °C • m2 • hour/kcal, not changed a lot compared to infants. Their mechanisms of physical thermoregulation are poorly developed. Therefore, if such a child is in conditions of room temperature (+ 20°С) in underwear and T-shirt, in 80 cases of 100 his thermoregulatory heat

Intensification of growth processes at the age of 5-7 years results in accelerating the length and surface area of extremities, providing a regulated heat exchange of the body with the environment. It is, in turn, results in the fact that from the age of 5.5— 6 years (it is especially visible for girls) the thermoregulation function is considerably changed. The body heat insulation is increased, and the chemical thermoregulation activity is substantially reduced. This method of body temperature regulation is more efficient and it becomes predominant in further development with age. In girls this transformation of

At the age of 10 years for girls and 11 years for boys quicker growth processes and considerably lower rate of basal metabolism which are typical for them are observed again. According to thermoregulation conditions, this age can be marked out as a crucial period: physical thermoregulation is activated again, with chemical thermoregulation becoming less

The next stage of thermoregulation development is during pubescence, becoming apparent in the frustration of the forming functional system. For 11—12-year old girls and 13-year old boys, despite the continuous decrease in the resting metabolism rate, there is no corresponding adjustment of vascular regulation. Worse heat insulation facilities of covering tissues result in the fact that, notwithstanding the age tendency, the critical temperature shifts to higher values with the temporarily growing role of chemical thermoregulation most teenagers (up to 80%) enlarge their heat production even under slight cooling

Distinct sex differences in dynamics of thermoregulation development are seen during pubescence (Kornienko & Gohblit, 1988). Parallel to decrease in basal metabolism, for girls after the second stage of pubescence (according to Tanner), heat insulation properties are rapidly increased, and the function of physical regulation is restored in full. By the age of 16 this process is usually over, and all thermoregulation parameters reach the values typical for adults. The same tendencies exist in boys, but by the age of 16 years, processes forming

important. For boys these changes are distinctly expressed at the age of 12 years.

body core falls down despite the processes (Kornienko, 1979).

1975; Kornienko, 1979).

conditions effects.

production is activated (Kornienko, 1979).

thermoregulation happens, on average, one year earlier than boys.

Results obtained in such studies as well as other data about thermogenic effect of food cast doubt on the validity of widely used calculations of caloric food value. All such calculations do not take into account energy expenditure on digestion of food substances which are known to take from 1/5 up to 1/3 caloric value of the taken food substance. The problem is complicated by the fact that fats and proteins have a greater thermogenic effect than carbohydrates (Kassirsky, 1934), while mixed products have a smaller thermogenic effect than the total thermogenic effects of food substances they contain (Forbes & Swift, 1944). It is proven that liquid food, with similar calorie value has a less specifically dynamic effect than solids (Habas & Macdonald, 1998). We think that mechanical calculations of food caloricity based on the caloric equivalent of proteins, fats and carbohydrates in it which is widely used in clinic and health-improving systems, including paediatric practice (Morgan, 1980; Young et al. 1991; Schmelzle et al., 2004) need to be corrected.

#### **3.4 Thermoregulation development in ontogenesis**

Thermoregulation, support of constant temperature in the body core is determined by two basic processes: heat production and heat dissipation. Heat production (thermogenesis) depends primarily on the rate of metabolic processes, while heat dissipation is defined by heat insulation provided by cutaneous coverings, vascular reactions, active outer respiration and perspiration. Because of this, thermogenesis is considered a mechanism of chemical thermoregulation, and heat dissipation regulation – a mechanism of physical thermoregulation. Both these processes change with age, as well as their role in providing a constant body temperature.

As a result of laws of physics, increase in mass and body absolute dimensions reduces the contribution of chemical thermoregulation. Thus, the value of thermoregulation heat production for newborn children makes about 0.5 kcal/kg • hour • °C, and for adults – 0.15 kcal/kg• hour•°C.

A newborn child, if temperature of the environment lowers, can enlarge heat production to adult levels - to 4 kcal/kg•hour. But because of lower heat insulation (0.15 °C•m2•hour/kcal) the chemical thermoregulation range of a newborn is small—no more than 5°.

At that it should be accounted that the critical temperature level (Th), switching thermogenesis for a healthy newborn is 33°C, by the adult period it falls down to 27—23°C. But in clothes with heat insulation usually making 2.5 CLO, or 0.45 °C •m2•hour/kcal, Th value falls down to 20°C, therefore a child in his usual clothes at room temperature is in a thermoneutral environment, meaning that in these conditions a child requires no extra expenditure to support body temperature.

If the temperature falls down below threshold values (for instance, during the change of a child's clothes), mechanisms of extra heat production switch on. For a child they are mainly, "nonshivering thermogenesis", localized in metabolically active tissues – liver and brown adipose tissue (Brück, 1970; Kornienko, 1979). Researches of the latest years have revealed that an acute short-term cooling of adults also results in activation of nonshivering thermogenesis in brown adipose tissue (Nedergaard et al., 2007; Son'kin et al., 2010), which is proved to be preserved for most adults residing in a moderate climatic zone (Nedergaard & Cannon, 2010). Another mechanism of thermogenesis is a cold-induced muscle tremor which is usually observed in adults when the cooling effect is strengthened or prolonged. For children this physiological mechanism turns out inefficient due to particular features of

Results obtained in such studies as well as other data about thermogenic effect of food cast doubt on the validity of widely used calculations of caloric food value. All such calculations do not take into account energy expenditure on digestion of food substances which are known to take from 1/5 up to 1/3 caloric value of the taken food substance. The problem is complicated by the fact that fats and proteins have a greater thermogenic effect than carbohydrates (Kassirsky, 1934), while mixed products have a smaller thermogenic effect than the total thermogenic effects of food substances they contain (Forbes & Swift, 1944). It is proven that liquid food, with similar calorie value has a less specifically dynamic effect than solids (Habas & Macdonald, 1998). We think that mechanical calculations of food caloricity based on the caloric equivalent of proteins, fats and carbohydrates in it which is widely used in clinic and health-improving systems, including paediatric practice (Morgan,

Thermoregulation, support of constant temperature in the body core is determined by two basic processes: heat production and heat dissipation. Heat production (thermogenesis) depends primarily on the rate of metabolic processes, while heat dissipation is defined by heat insulation provided by cutaneous coverings, vascular reactions, active outer respiration and perspiration. Because of this, thermogenesis is considered a mechanism of chemical thermoregulation, and heat dissipation regulation – a mechanism of physical thermoregulation. Both these processes change with age, as well as their role in providing a

As a result of laws of physics, increase in mass and body absolute dimensions reduces the contribution of chemical thermoregulation. Thus, the value of thermoregulation heat production for newborn children makes about 0.5 kcal/kg • hour • °C, and for adults – 0.15

A newborn child, if temperature of the environment lowers, can enlarge heat production to adult levels - to 4 kcal/kg•hour. But because of lower heat insulation (0.15 °C•m2•hour/kcal) the chemical thermoregulation range of a newborn is small—no more

At that it should be accounted that the critical temperature level (Th), switching thermogenesis for a healthy newborn is 33°C, by the adult period it falls down to 27—23°C. But in clothes with heat insulation usually making 2.5 CLO, or 0.45 °C •m2•hour/kcal, Th value falls down to 20°C, therefore a child in his usual clothes at room temperature is in a thermoneutral environment, meaning that in these conditions a child requires no extra

If the temperature falls down below threshold values (for instance, during the change of a child's clothes), mechanisms of extra heat production switch on. For a child they are mainly, "nonshivering thermogenesis", localized in metabolically active tissues – liver and brown adipose tissue (Brück, 1970; Kornienko, 1979). Researches of the latest years have revealed that an acute short-term cooling of adults also results in activation of nonshivering thermogenesis in brown adipose tissue (Nedergaard et al., 2007; Son'kin et al., 2010), which is proved to be preserved for most adults residing in a moderate climatic zone (Nedergaard & Cannon, 2010). Another mechanism of thermogenesis is a cold-induced muscle tremor which is usually observed in adults when the cooling effect is strengthened or prolonged. For children this physiological mechanism turns out inefficient due to particular features of

1980; Young et al. 1991; Schmelzle et al., 2004) need to be corrected.

**3.4 Thermoregulation development in ontogenesis** 

constant body temperature.

expenditure to support body temperature.

kcal/kg• hour•°C.

than 5°.

the child's body constitution, therefore it is activated in the last turn, if temperature of the body core falls down despite the processes (Kornienko, 1979).

High activity of special mechanisms of thermogenesis in infants is connected not only with small size and large relative surface increasing heat insulation, not only with low heat insulation of cutaneous coverings, but with a relatively low level of basal metabolism, which has been noted before in this paper. Within the first year of life all these parameters are changing and the chemical thermoregulation activity is reduced. For a child of 5—6 months the importance of physical thermoregulation is considerably increased; it makes the temperature threshold and latent period of an interscapular brown adipose tissue activation almost double compared with the same parameters for infants 1-2 months old (Gohblit et al, 1975; Kornienko, 1979).

Under usual conditions the child older than 3 years old has a high value of heat flow in relation to the body surface unit, and heat insulation of cutaneous coverings is low, therefore children's skin is practically always warm. Even at the age of 4.5—5 years for girls and 5.5—6 years for boys the body heat insulation is very low: 0.226 + 0.003 °C • m2 • hour/kcal, not changed a lot compared to infants. Their mechanisms of physical thermoregulation are poorly developed. Therefore, if such a child is in conditions of room temperature (+ 20°С) in underwear and T-shirt, in 80 cases of 100 his thermoregulatory heat production is activated (Kornienko, 1979).

Intensification of growth processes at the age of 5-7 years results in accelerating the length and surface area of extremities, providing a regulated heat exchange of the body with the environment. It is, in turn, results in the fact that from the age of 5.5— 6 years (it is especially visible for girls) the thermoregulation function is considerably changed. The body heat insulation is increased, and the chemical thermoregulation activity is substantially reduced. This method of body temperature regulation is more efficient and it becomes predominant in further development with age. In girls this transformation of thermoregulation happens, on average, one year earlier than boys.

At the age of 10 years for girls and 11 years for boys quicker growth processes and considerably lower rate of basal metabolism which are typical for them are observed again. According to thermoregulation conditions, this age can be marked out as a crucial period: physical thermoregulation is activated again, with chemical thermoregulation becoming less important. For boys these changes are distinctly expressed at the age of 12 years.

The next stage of thermoregulation development is during pubescence, becoming apparent in the frustration of the forming functional system. For 11—12-year old girls and 13-year old boys, despite the continuous decrease in the resting metabolism rate, there is no corresponding adjustment of vascular regulation. Worse heat insulation facilities of covering tissues result in the fact that, notwithstanding the age tendency, the critical temperature shifts to higher values with the temporarily growing role of chemical thermoregulation most teenagers (up to 80%) enlarge their heat production even under slight cooling conditions effects.

Distinct sex differences in dynamics of thermoregulation development are seen during pubescence (Kornienko & Gohblit, 1988). Parallel to decrease in basal metabolism, for girls after the second stage of pubescence (according to Tanner), heat insulation properties are rapidly increased, and the function of physical regulation is restored in full. By the age of 16 this process is usually over, and all thermoregulation parameters reach the values typical for adults. The same tendencies exist in boys, but by the age of 16 years, processes forming

Energy Metabolism in Children and Adolescents 131

(MOC) rises proportionally to the muscle mass growth (Kornienko et al., 2000), but it lacks information about qualitative changes in muscle energy supply of children and teenagers

Newborn 0,9 0,6 - - 5 – 7 4,6 6,7 1,01 151 9 5,2 10,5 1,8 171 11 6,6 11,6 2,1 181 14 4,8 21,2 3,5 165 20 4,5 25,0 4,1 164 36-40 3,7 28,3 3,9 138 Table 2. Age changes in cytochrome **a** content in thigh muscle and human aerobic capacity

Age dynamics of cytochrome **a** content – a terminal site of the oxidative chain – in human skeletal muscles (Kornienko, 1979; Demin et al., 1987) is given in Table 2. Calculations of the estimated value for specific MOC (per 1 kg of somatic muscle mass) are shown. As obvious from the given data, the highest cytochrome **a** concentration is registered in skeletal muscles for boys 9-11 years old. It is also proved by data of electron microscopic researches (Kornienko, 1979; Kornienko et al, 1987): the number of mitochondria in relation to the area of myofibrils for 11-year old boy is considerably more than in an adult man (Table 3). It is remarkable, that, according to data of morphologists, a capillary network in the muscles of extremities turns out to be more developed in children of 9-11 years (Topol'sky, 1951), which is the age when there is the highest content of oxidizing ferments in the muscle tissue. Thus, an age development of the energy production aerobic source in skeletal muscles does not happen monotonously, but gets the expressed maximum during prepubescence (Fig.5). These conditions have a

Muscle mass, kg (after: Holliday, 1971)

MOC, l/min (after: Åstrand, 1952)

MOC, ml/kg muscle mass

(Son'kin & Tambovtseva, 2011).

(After: Kornienko, 1979)

Age, years Cytochrome **а**

concentration, nM/g raw mass of muscle tissue

Fig. 5. Dynamics of aerobic capacity indices in schoolboys

considerable effect on the functioning of the muscle energy supply system.

mechanisms of physical thermoregulation are incomplete. Only in youths after pubescence do thermoregulation facilities reach their final level. Increase in tissue heat insulation to the level of 1.1 CLO allows to function without activating the chemical thermoregulation (meaning extra heat production) even when the environment temperature falls down by 10-15 degrees below thermoneutral. Such body reaction is naturally more economical and efficient.

The given data prove that in the process of postnatal ontogenesis the primary line of the system development providing temperature homeostasis is indirect (Falk, 1998). At each stage of individual organism development there is a complex dependence of thermoregulation active mechanisms on growth and development, the rate of metabolic processes and conditions of some autonomic functions. It is this dependence that determines a primary activity of physical or chemical thermoregulation mechanisms, providing temperature homeostasis at the corresponding stage of development.
