Feeding from Toddlers to Adolescence: edited by Angel Ballabriga, Nestle Nutrition Workshop Series, Vol. 37. Nestec Ltd., Vevey/ Lippincott-Raven Publishers, Philadelphia, © 1996.

The Nutritional Role of Soft Drinks during Childhood and Adolescence

Pierre R. Guesry

Nestle Research Centre, Vers-chez-les-Blanc, Lausanne, Switzerland

Years ago, children were drinking milk in Scandinavian and Anglo-Saxon countries whereas in Latin countries, they were drinking either plain or water mixed with a small amount of wine, cider, or syrup. Adolescents were gradually switching to beer, wine, or cider at an age that depended on their type of work and socioeco- nomic class. Nowadays, from north to south, west to east, and independent of their work or socioeconomic class, the great majority of children and adolescents drink soft drinks (1) during meals and between meals. This has caused changes in various nutrient intakes which have important consequences.

DEFINITION

Soft drinks are ready-to-use drinks, carbonated or uncarbonated, containing or intense sweeteners and neither alcohol nor milk. This definition excludes water, either plain or , even when flavored (but without the addition of sugar or sweeteners), and it excludes beer, cider, wine, and milk. The definition includes "sports drinks," which are increasingly consumed outside sports, and fruit juices, which are often sweetened and mixed with still or sparkling water.

CONSUMPTION

Most data come from the USA where very extensive surveys were conducted on teenagers in 1977 (2) and again in 1987 (3). Since we can assume that the trends shown in the American studies will hold true for the rest of the world after a lapse of a few years, the 1987 survey may give a good representation of what is happening elsewhere today. For the whole population, the consumption of all soft drinks in the USA was about 200 I/year in 1993,1401 in Mexico, 1101 in Canada, 701 in Argentina, and 601 in Saudi Arabia, with an increase varying from 5% to 30% since 1989 depend- ing on the country (4). The worldwide average consumption of carbonated soft drinks in most African, eastern European, and far eastern countries including India is 10 769 170 NUTRITIONAL ROLE OF SOFT DRINKS

TABLE 1. Soft drink consumption by adolescents 12 to 19 years old in the United States in 1987

Carbonated soft drinks (ml/d) Total Coffee and tea Fruit-based drinks (ml/d) (ml/d) (ml/d) Regular Diet

Boys 587 114 83 361 29 Girls 490 98 109 215 68

From U.S. Dept. of Agriculture (3).

I/year (5) below the international average, and in North American countries, it is far above the international average. Most western European countries, Australia, South Africa, Argentina, Brazil, and Japan are above the international average, and Mexico has the number one per capita consumption in the world, just in front of the USA, at about 120 I/year. For boys from 12 to 19 years of age, the average total consumption (Table 1) of soft drinks in 1987 in the USA was 587 ml/day, carbonated soft drinks representing 390 ml/day, coffee and tea 114 ml/day, and fruit drinks 83 ml/day. For girls in the same survey, the average total daily consumption was only 490 ml/day, carbonated soft drinks representing 283 ml/day, broken down into 215 ml/day of regular and 68 ml/day of low-calorie drinks. The consumption of cold tea increased dramatically in Europe from 259,000 1 in 1989 to 1,296,0001 in 1994. For 1994, the annual per capita consumption varied from 1.2 1 in France to 45 1 in Switzerland. There was more detailed longitudinal information in the 1977 survey, which showed an increase in the consumption of soft drinks during a 3-day period from 40% of the 0- to 4-year-old population to 70% for males in the age range 17-18 years (Fig. 1) (6). There was a small difference of about 5% between males and females in this last age group for naturally sweetened products, and a larger difference of about 10% in favor of females for diet varieties. The average total daily consumption was 128 ml at 0-4 years, 159 ml at 5-6 years, 170 ml at 7-8 years, 222 ml at 11-12 years, 256 ml at 13-14 years, 300 ml at 15-16 years, and 332 ml at 17-18 years (Fig. 2). In the 1987 survey, the values are similar at the younger ages but increased dramatically to 587 ml/day in the 12-19 years age group. In a survey done in 1990-1991 in a college in Michigan (7), 82% of boys were consuming soft drinks, among which 8% were diet varieties, whereas 72% of the girls were consuming soft drinks, 28% of which were diet varieties. In a survey done in Germany in 1992 (Euromonitor, February 1993), 82.6% of 14- to 19-year-olds were consuming soft drinks in western Germany and 78.2% in eastern Germany, suggesting an increasing uniformity of soft drink consumption in the coun- try as a whole. Consumption increased with household income, the opposite of what was observed in USA (2). Soft drink consumption is increasing steadily. In the USA (Fig. 3), the average consumption of all soft drinks in young adults increased between 1977 and 1985 from NUTRITIONAL ROLE OF SOFT DRINKS 171

Males & Females • ••••• Females 70 Males

60

50 •\ regular o ho Q.

S 30 _ V\ i 20

10 '.diet

0-4 5-6 7-8 9-10 11-12 13-14 15-16 17-18 19-24 25-34 35-44 45-54 55-64 65+

Years of Age

FIG. 1. Percentage of population, classification by age/sex, consuming soft drinks (regular and artificially sweetened) at least once during 3 surveyed days. (Reproduced from J Am Diet Assoc 1985:85:352-4, with permission.)

763 ml to 1051 ml, and carbonated sodas from 294 ml to 491 ml. In France, it increased from 29 I/year in 1988 to 35 I/year in 1992 for the whole population, and in Japan from 57.6 I/year in 1981 to 93.5 I/year in 1991. More generally, in the European Community, consumption has increased from 183 1 per capita per year in 1989 to 200 1 in 1993. Among the carbonated soft drinks, the most popular all across Europe are the colas, with preferences ranging from 52% in Germany to 84% in Italy; colas are followed by orangeade, varying from 10% in the UK to 49% in Italy, and then by 172 NUTRITIONAL ROLE OF SOFT DRINKS

600 - ml/day '587

500 -•

400

300 t USA 1987

20(1 USA 1977

!• 1976 100 4-

I I I I I I I I I I I I 2 4 6 8 10 12 14 16 18 20 years of age

FIG. 2. Average daily consumption of soft drinks.

491 500 -j- ml/day 474

400 4-

Coll'cc and lea 300 4- 294 l-'ruil based Juices

200 4- Carbonated Soft Drinks

100 87

1977 1985

FIG. 3. Evolution of soft drinks consumption in the USA between 1977 and 1985 in young adults (19-34 years of age). NUTRITIONAL ROLE OF SOFT DRINKS 173

lemonade, from 10% in Italy to 23% in France. Among the fruit-based drinks, orange is by far the most popular everywhere in Europe, followed by apple, tropical fruits, and pineapple.

COMPOSITION

The average composition of the most commonly consumed soft drinks is summa- rized in Table 2. Among these, colas of various brands usually have a similar composi- tion. The total in regular varieties is around 110 g/1, with 40 g , 35 g , and 35 g fructose per liter (8). The sodium content ranges from 15 to 50 mg/1, potassium 10 mg/liter, phosphorus 300 mg/liter, and calcium 60 mg/1. Caffeine content is 125 mg/1. pH is low at 2.4 and titrable acidity quite high (10 ml NaOH N/l). There are now varieties in which the are replaced by intense sweeteners, usually aspartame at a concentration of about 400 mg/1. Benzoates and sorbates are allowed and used as preservative agents for carbonated soft drinks. Lemonades are usually less sweet and contain only about 60 g/1 of carbohydrate, half as sucrose and the rest split equally between glucose and fructose. In contrast, is sweeter and contains 160 g/1 of CHO, but no sucrose. Unsweetened orange juice contains 81 g/1 of CHO, half as sucrose and the rest as glucose and fructose. It also contains 1.8 g/1 of potassium (9). Unsweetened apple juice contains 100 g/1 of CHO made up of 63% fructose, 26% glucose, and 11% sucrose. Apple juice also contains 1.1 g/1 of potassium. Industrial ready-to-drink teas and coffees contain about 90 g/1 of CHO and 100 to 200 mg/1 of caffeine, respectively, for iced tea and coffee.

TABLE 2. Approximate composition of the most commonly consumed soft drinks

Sweeteners Sucrose Glucose Fructose Intense Sodium Potassium Phosphorus Caffeine (g/D (g/i) (g/i) (g/i) (mg/l) (mg/l) (mg/l) pH (mg/l)

Colas classic 40 35 35 0 15-50 10 300 2.4 125 light 0 0 0 0.4 15-50 10 300 2.4 Lemonades regular 30 15 15 0 15-50 10 light 0 0 0 0.4 15-50 10 Orange juice 40 20 20 0 20 1800 160 4 0 Apple juice 10 30 60 0 20 1100 60 5 0 Iced teas regular 40 25 25 0 0 200 20 120 light 0 0 0 0.4 0 200 20 120 Coffees regular 40 25 25 0 0 300 30 100-200 light 0 0 0 0.4 0 300 30 100-200 / 74 NUTRITIONAL ROLE OF SOFT DRINKS

TABLE 3. Sports drinks composition (from label declaration)

CHO Na K Ca Mg VitC Brand Company (g/D (mg/l) (mg/l) (mg/l) (mg/l) (mg/l)

Aquarius" Coca Cola 37 230 588 200 480 188 Quaker 60 410 117 ? 70 ? Isostar Wander 72 540 120 100 44 22 Lucozade Sport Beecham 64 550 100 20 10 100 Nesfit Nestle 52 332 260 28 38 Red Bull" Red Bull 113 ? ? ? ? ?

CHO, carbohydrate. " contains 54 ml/I of saccharine. 6 Red Bull contains 320 ml/l of caffeine.

Sports drinks are more diverse. The average compositions of the most commonly sold sports drinks are summarized in Table 3. In addition, and depending more on the container than on the product itself, some of these soft drinks may contain lead or aluminum (10,11), particularly if their pH is low, which is the case with most colas and fruit juices, though the values of these trace elements remain within authorized limits.

NUTRITIONAL CONSEQUENCES

Role of Carbohydrates

Excessive sugar consumption has been blamed for a long list of sins, ranging from acne to deficiencies, by way of bubonic plague, alopecia, and schizophrenia (12). Most of these accusations are ridiculous and do not merit discussion, but I shall examine the role of sugar consumption on obesity, dental caries, hyperlipidemia, hyperactivity in children, and soft drink-induced diarrhea.

Obesity

One of four children in the United States is obese (13) and the prevalence has doubled over the last 20 years (14). During this period, soft drink consumption in- creased but total sugar consumption did not. The level of consumption of sugared sodas by Navajo adolescents is more than twice the U.S. average, whereas the preva- lence of obesity is 34% higher than the average for the rest of the USA (15), leading the Indian Health Services to set a program to reduce sugared soda consumption. In an experiment in which 1.15 I/day of soda sweetened with high-fructose corn syrup was given over 3 weeks, the subjects gained more than 1 kg body weight compared to volunteers receiving the same amount of diet soda sweetened with aspartame (16). Paradoxically, during this study there were no changes in intakes of NUTRITIONAL ROLE OF SOFT DRINKS 175 , protein, or complex carbohydrates, contrary to the fears expressed by the Council of Foods and Nutrition (17) which had led to a ban on the distribution of soft drinks in school lunch rooms. With a more usual consumption of 500 ml/day, the CHO intake would be 50 g/day, representing less than 10% of the daily energy intake and within the recommended limits. Depending on when it is taken before the next meal, sucrose, even when consumed in a drink (18), tends to cause a compensatory decrease in food intake to maintain energy balance, thus also decreasing fat intake, which is believed to be more important in the genesis of obesity. There are many reasons other than increased soft drink consumption that could be responsible for the increased prevalence of obesity in adolescents of industrialized countries, such as the increase proportion of dietary fat and decreased energy expenditure due to air conditioning, motor transport, and excessive television watching. To conclude, there is no proof that a reasonable consumption of soft drinks by children and adolescents induces obesity, but if the consumption exceeds half a liter a day, it would be sensible to switch to a diet version rather than a sugared one, since excessive consumption of energy from soft drinks might reduce the intake of other foods containing useful nutrients.

Dental Caries

It is well recognized that Streptococcus mutans, the usual host of the dental plaque, metabolizes sucrose, fructose, maltose, and glucose (19) (Fig. 4). Lactic acid is pro- duced as a byproduct, which results in a rapid and pronounced decrease of pH (20) which may reach values as low as pH 4 within 10 minutes. Below a pH of 5.5, the tooth enamel starts to dissolve, producing caries. Sucrose is also the only sugar used by S. mutans to synthesize the sticky dextran which enables the dental microflora to adhere to the dental surface. The low pH of the cola drinks (pH 2.4) and of fruit- based drinks further increase the potential dangers of soft drinks for dental health. For decades, investigators have pointed out the particular importance of the fre- quency of sugar intake in determining caries activity, not only because of its ability to adhere to the enamel (21,22). Soft drinks are usually consumed more frequently than snacks as they are easy to sip, and it is common practice in the USA to have a can of soft drink in the hand while walking or participating in a meeting. In 1984, Ismail implicated soft drinks as one of the factors promoting the highest caries activity (23) in spite of the fact that their cariogenic potential is not the greatest (24). Along the same lines, other investigators (25) have reported correlations between sucrose consumption and an increase in decayed, missed, and/illed feeth (DMFT). In Spain, the rate of DMFT doubled between 1968 and 1985 when average sugar consumption increased from 40 g/day per capita to 80 g/day. A parallel situation was observed in Greece during the same period (26). However, in Belgium, Finland, and the UK between the 1970s and the 1980s, the rate of DMFT decreased dramatically, although sugar consumption remained high. This was thought to be the result of the generalized 176 NUTRITIONAL ROLE OF SOFT DRINKS

STARCH

XYLITOL SORBITOL MANNITOL DISACCHARIDE ALCOHOLS

ACID (LACTIC ACID)

FIG. 4. Dietary carbohydrates are a source of energy for the bacteria of dental plaque. use of fluoride as a dentifrice or supplement, which may exempt sucrose and soft drink consumption from blame in the formation of dental caries.

Hyperlipidemia

Fructose (and as a result sucrose) follows a distinct metabolic pathway from glu- cose. Fructose is metabolized in the liver almost entirely to glycerol and fatty acids, whereas since all cells metabolize glucose, only 30-40% is processed by the liver. In addition, the enzymes of the lipogenic pathway are induced by fructose (27). In rodents, a high-fructose diet induces hypertriglyceridemia and hypercholesterol- emia and causes atheroma in monkeys and rabbits (28,29). A consumption of 500 ml a day of cola or apple juice will increase the fructose intake (directly or indirectly through sucrose) by about 30 g/day. This chronic increase over many years may have a deleterious effect and a limitation of intake seems reasonable, particularly for children and adolescents at risk of developing early hypercholesterolemia.

Hyperactivity in Childhood

Attention deficit hyperactivity disorder (ADHD) affects about 3% of preadolescent children, almost exclusively boys. It is characterized by inappropriate inattention, excessive levels of gross motor activity, and impulsive behavior. NUTRITIONAL ROLE OF SOFT DRINKS 177

In 1980, Prinz et al. (30) showed that although hyperactive and normal children by and large ate the same amount of sugar, there was a positive correlation in children with ADHD between sugar consumption and destructive aggressive behavior. The authors were prudent in their interpretation of the facts, but the mass media took up the story and as a result many practitioners now advise parents to reduce the sugar intake of their hyperactive children. Even university hospitals have proposed special diets which, in addition to reducing sugar by 50%, eliminate artificial colors and flavors, chocolate, monosodium glutamate, preservatives, caffeine, and so on. In a crossover design study (31), 42% of the children investigated (only 10 children) were reported by their parents to show improvement in behavior and 42% showed no effect of the diet. More recently, Wolraich et al. (32) evaluated the behavior of school age and pre- school children receiving diets high in sucrose or in which sucrose had been replaced by aspartame or saccharine. Monosodium glutamate, artificial flavors, and caffeine were kept low in the three different diets, which were fed to all of the children for 3 weeks using a crossover design. Neither sucrose nor aspartame had significant behavioral or cognitive effect in normal preschool children or in school age children thought to be sensitive to sugar.

Soft drink—induced diarrhea

This is a benign situation not to be confused with the severe diarrhea induced by impaired dissacharide digestion such as sucrase-isomaltase deficiency, lactase deficiency, or impaired congenital monosaccharide absorption. Soft drink-induced diarrhea occurs only when large quantities of fruit juice or soda containing high- fructose corn syrup are ingested (33,34) because fructose alone is not as well absorbed as fructose associated with glucose, sucrose, or starch (35) and thus excess of fructose without other could induce diarrhea. Sorbitol, which is present in certain fruits (apples, pears, and prunes), is not ab- sorbed and ferments in the colon, producing diarrhea if ingested in significant amounts. A small series of seven cases has been reported in American Academy of Pediatrics News (36). Some investigators also believe that soft drink-induced diarrhea could be caused by excessive fluid intake (37) but this is doubtful since excessive water consumption alone in children with antidiuretic hormone deficiency does not induce diarrhea.

Sweeteners

We have seen many reasons for decreasing the consumption of sucrose or high- fructose corn syrup in soft drinks, but the industry waited for decades for an intense sweetener which did not also give bitterness and which was approved for mass con- sumption by health authorities. The first low-calorie (cyclamate-based) cola drink was launched in 1963, but in 1969 the U.S. Food and Drug Administration (FDA) 178 NUTRITIONAL ROLE OF SOFT DRINKS banned the use of cyclamates in soft drinks. Only in 1983 did FDA approval of aspartame allow Diet Coke to be launched and this immediately started controversy about the possible deleterious effects of aspartame on blood phenylalanine levels, appetite, hyperactivity in children, and allergenicity. Most diet soft drinks contain about 400 mg/1 of aspartame to give a sweetness comparable to 100 g/1 of sucrose, since the sweetness of aspartame is about 200 times that of sucrose. Aspartame is metabolized to phenylalanine and aspartic acid, but a loading dose of 34 mg aspartame per kg body weight (BW) only increases plasma phenylalanine concentration from a fasting level of 6 /imol/100 ml to 11 /xmol/100 ml. As much as 200 mg/kg BW of aspartame—corresponding to half a liter of soft drink per kg BW—would be required to increase blood phenylalanine to 50 /xmol/ 100 ml, which could induce a risk (38). It is recommended that aspartame-sweetened soft drinks should be avoided by phenylketonuric patients who need to control their phenylalanine intake. For normal children, the contribution of aspartame to the phe- nylalanine intake would be trivial compared to the normal protein intake. Some investigators (39,40) consider that aspartame-sweetened soft drinks may stimulate the appetite, whereas others state that they have no effect. Black et al. (41) conducted a study on 18 normal young males and concluded that encapsulated aspartame had no effect on appetite and that appetite reduction following consump- tion of an aspartame-sweetened drink is due to drink volume rather than aspartame, confirming the results of Canty and Chan (42). The effect of aspartame on hyperactive children has been studied in parallel with the role of sucrose (32), and neither sucrose nor aspartame affected behavior. Between 1982 and 1984, 199 patients were reported to the Centers for Disease Control in Atlanta, Georgia (USA) for allergic reactions to aspartame, and of these 65 had symptoms considered to be classic for food allergy (43). However, in a study initiated in the National Institutes of Health in Bethesda, Maryland (USA) in 1986 and reported in 1991 (44), no subject with a clearly reproducible adverse reaction to aspartame was identified from 61 patients referred for possible problems.

Phosphorus and Acid Load

Most cola drinks are acidified to around pH 2.4 by the addition of phosphoric acid, bringing the level of phosphorus to 300 mg/1 and the net acid load to 20 mmol/1. Chronic ingestion of such an acid load is thought to cause slow dissolution of bone minerals (45), which could impair the achievement of optimal peak bone mass that is so necessary for the long-term prevention of osteoporosis. This is particularly important in girls during childhood and adolescence, and the problem is compounded by the increased phosphate load. The recommended dietary allowance of phosphorus for children and adolescents is 800-1200 mg/day (46). The food presently consumed in industrialized societies is very rich in phosphorus, providing an intake of 1000-1600 mg/day, mainly in the form of phosphate food additives used by industry (47). The addition of about 200 mg/day from soft drinks represents an additional 15-20%. Serum NUTRITIONAL ROLE OF SOFT DRINKS 179 phosphorus depends on the phosphate intake, and hyperphosphatemia induces hyper- parathyroidism and bone demineralization (48,49). This effect is aggravated by the usual low calcium intake in adolescent diets. Limiting the ingestion of colas and encouraging the consumption of more milk- based products rich in calcium is important for children and adolescents, especially girls.

Caffeine

Cola drinks contain around 125 mg/1 of caffeine, whereas iced teas contain about 120 mg/1, as do ready-to-drink coffees. A cup of regular coffee contains about 80 mg of caffeine. The amount of caffeine in soft drinks can easily be handled by an adolescent drinking reasonable quantities. For a younger child, however, it may induce sleep problems, and the use of caffeine-free soft drinks would be preferable. Strain et al. (50) suggest that a small percentage of coffee or soft drink users show symptoms of caffeine dependence. Fortunately, risks associated with caffeine consumption are generally low (51), and the only recognized problem is that high daily caffeine intakes (>450 mg/day) in postmenopausal women with low calcium intakes decrease bone mineral density of the spine (52). To my knowledge, no study has been yet conducted in adolescents, but such studies are certainly needed before recommendations can be made.

Allergy

Many food additives and coloring agents may be allergenic, in addition to fruits and particularly citrus fruits; thus allergy related to soft drink ingestion is a possibility (53). According to Moneret-Vautrin and Kanny (54), 50% of children with atopic dermatitis are sensitive to vanilla and vanillin, which are flavorings used in soft drinks. However, these flavorings are ubiquitous and there are many opportunities for coming into contact with them other than through soft drink consumption. Sor- bates and benzoates used as preservatives in carbonated soft drinks can also be allergenic.

Sodium

Soft drinks usually contain low concentrations of sodium. Sports drinks, which youngsters now drink more and more without having any involvement in competitive sports, are the exception. Their sodium content varies from 200 to 550 mg/1. Those with the highest sodium content provide more salt than is lost during exercise, and when they are consumed without accompanying sporting activity, the sodium intake is not balanced by losses. However, the sodium intake provided by these drinks comprises only about 10% of the usual sodium intake of a child or adolescent. The 180 NUTRITIONAL ROLE OF SOFT DRINKS main risk is that of getting used to the salty taste, which could induce further salt abuse.

CONCLUSIONS

Except in very specific cases, a reasonable intake of most soft drinks does not represent a nutritional health hazard for normal children or adolescents. Their toler- ance of high energy intakes is greater than that of adults because of their greater physical activity and their energy needs for growth. The deleterious effect of sugar- sweetened soft drinks on dental health should be discussed with the parents and the child, who could decide to switch to artificially sweetened products. The possible role of acidic carbonated sodas on bone mineralization during the critical period of bone growth should be further investigated.

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49. Mazariegos-Ramos E, Guerrero-Romero F, Rodriguez-Moran M, Lazcano-Borciaga G, Paniaga R, Amato D. Consumption of soft drinks with phosphoric acid as a risk factor for the development of hypocalcemia in children. / Pediatr 1995; 126: 940-2. 50. Strain EC, Mumford GK, Silverman K, Griffiths RR. Caffeine dependence syndrome: evidence for case histories and experimental evaluations. JAMA 1994; 272: 1043-8. 51. Garattini S, ed. Caffeine, coffee and health. New York: Raven Press, 1993. 52. Harris SS, Dawson-Hughes B. Caffeine and bone loss in healthy post menopausal women. Am J Clin Nutr 1994; 60: 573-8. 53. Lockey SD. Reactions to hidden agents in foods, beverages and drugs. Ann Allergy 1971; 29: 461-6. 54. Moneret-Vautrin DA, Kanny G. Intolerance et immunotoxicite' des additifs alimentaires. Med Hyg 1993; 51: 881-8.

DISCUSSION

Dr. Ballabriga: I was surprised to read an article about the "squash drinking syndrome" (1) in which a study shows that over 70% of preschool children studied in a United Kingdom hospital never drank plain water. I do not think this is the case in our country, but I don't know what the situation is in the rest of Europe. Squash drinks are a fruit flavor drink concentrate diluted with water before consumption, and one of the most common is black currant squash. Can you tell us anything about this matter? Dr. Guesry: In the USA, 40% of drinks are commercial soft drinks versus only 10% tap water and a few percent mineral water. Thus soft drinks are three to four times more used than water in United States. For the European Community, the available statistics do not give information about tap water, but only about soft drinks vs. mineral water, where the proportions are 70% soft drinks and 30% mineral water. Dr. Gracey: We have a very similar phenomenon to the squash syndrome in Australia (2), where children are given what we call cordials, which is essentially what happens in the UK. A similar phenomenon has been reported from Europe (3). Most children in Australia drink cordials and because we have very hot summers, children tend to drink large volumes of cordial which can be a common cause of diarrhea. It is also one of the commonest reasons for referral of children to pediatric gastroenterologists in our city. Stopping the squash stops the syndrome; it is as simple as that. Dr. Lentze: In relation to this diarrhea problem, today fructose in soft drinks is probably more important than sorbitol because fructose is transported through the membrane by the GLUT 5 transporter, but the density of this transporter is different from child to child. But not only fructose is important; the presence of other sugars in these drinks is also important, such as glucose and sucrose, and the more glucose or sucrose is present along with the fructose, the less diarrhea you have. So the predominance of fructose alone will produce the diarrhea, but no diarrhea will occur if you have glucose or sucrose at the same time in the fruit juice. So the problem depends on the predominance of fructose rather than on sorbitol or other sugars. Dr. Guesry: As you know, fructose is rarely present on its own in these types of soft drink, especially the carbonated soft drinks. The ratio is set by the ratio you find in inverted sugars and is basically one third sucrose, one third glucose, and one third fructose. In fruit juice it is different, although in most of the fruits there is a mixture of sucrose, glucose, and fructose. However, some contain more fructose than others, and this is probably the case with apple. So that may explain why you see more often this diarrhea induced by apple juice than by other types of juice. Dr. Dupont: Could the presence of, for example, fructo-oligosaccharides be responsible for diarrhea? We know that excessive consumption leads to diarrhea and they can be generated by some industrial processes. NUTRITIONAL ROLE OF SOFT DRINKS 183

Dr. Guesry: The answer is no. We have tested different quantities of fructo-oligosaccha- rides to induce diarrhea. In toddlers, maybe the quantity would be smaller but for an adult or adolescent, you would need to give about 10 g per day of fructo-oligosaccharides to induce soft, frequent stools. I cannot see how the process could produce such a quantity in soft drinks. Dr. Giovannini: In Italy, we have mineral water with calcium, but no mineral water manu- facturer produces mineral water specifically for adolescents and young people. Mineral water has a domestic image, whereas soft drinks have a more cosmopolitan image that appeals to the young. I think we should have an educational programme in the European Community to explain that it is better to drink a good mineral water, maybe with added calcium. I would also like to comment on the problem of plaque and teaching proper teeth cleaning. We made a study with Dr. Vogel's group and we saw many children who don't know how to clean their teeth properly and many who don't clean their teeth every day, or three times a day as recommended by the Italian Dental Academy. It is an unhappy state of affairs that Coke is the official partner of the Olympic games. I think Coke is perhaps better than beer or wine for adolescents, but the big companies should educate young people about drinking mineral water. Dr. Guesry: We are working on this. We have just concluded a study in our research center about the absorption of calcium from mineral water because there was some question as to whether or not it would be as well absorbed as from cow's milk. The good news is that the absorption appears to be similar to that of the calcium from cow's milk and we are going certainly to use this argument for the people who believe that calcium intake should be increased in adolescents, at least in girls, and we will certainly use this argument to promote water. Dr. Gracey: With the increasing affluence of many tropical, so-called developing countries, some of which now have a middle class with quite a large disposable income, there is increas- ing soft drink consumption, and much more fluid is consumed in general than in colder countries. I think this is very important from a nutritional point of view. Would you like to comment on that? Dr. Guesry: Drinking this kind of product gives you a certain social status. I have been visiting a lot of eastern European countries and two of the predominant consumer products in those countries, which are advertised all over the main cities, are Coca Cola and Philip Morris cigarettes. You see people everywhere smoking cigarette after cigarette and drinking Coca Cola. This is also the case in certain parts of the far east or even Africa. You are right. When the family income is limited and they have to choose between good food and these types of soft drink, the risk is that they will drink too much of the soft drinks and get too much energy from them and not enough from the rest of their food. I have always fought against the concept of empty calories, but in this case it could probably be applied. Dr. Cavadini: Do you think that soft drink consumption might impair micronutrient intake in children and adolescents? And do you recommend the consumption of diet soft drinks instead of regular soft drinks? Dr. Guesry: When you have a high consumption of this type of soft drink, you decrease the consumption of other nutrients. We know that the consumption of soft drinks can vary from a few hundred ml per day up to 3 1 in some studies, which represents something like 1300 kcal. For an adolescent, this may account for 40-45% of the energy intake. In that situation, it would certainly reduce the intake of important macro- and micronutrients. I would certainly not recommend drinking more diet soft drinks; I would recommend drinking less sugar-sweetened soft drinks. Dr. Garza: Are you aware of any cross-country comparisons of the top and bottom quar- tiles of soft drink consumption in children in terms of the consumption of other nutrients? 184 NUTRITIONAL ROLE OF SOFT DRINKS

Dr. Guesry: No, there are very few studies that I could find, and I reviewed what has been published thoroughly. There is, however, one publication that I didn't have time to discuss, from the United Kingdom, showing that in the population of children drinking the largest quantities of soft drinks, there was a risk of macro- and micronutrient deficiency (4). Dr. Garza: Was calcium the primary nutrient displaced? Dr. Guesry: Milk consumption is decreased and milk is a principal source of calcium, so it certainly reduces the calcium intake. Dr. Baerlocher: In our nutrition review, we calculated the intake of sugar from soft drinks and found it was about 45-60% of the daily intake. That is quite a large amount. What we noticed also was that a lot of children consumed iced tea. In which group do you place iced tea? Dr. Guesry: Iced tea and also ready-to-drink coffee, which is becoming more and more popular, usually contain less carbohydrate than other soft drinks, usually around 80 to 90 g/1. They contain some potassium and also caffeine—about 100 mg of caffeine per liter. So it is a soft drink according to the definition I choose. I am surprised at your data showing that about 50% of the daily sugar consumption was from soft drinks. According to recommen- dations, sugar should represent about 50% of the energy intake, which would mean about 300 g per day for an adolescent. This means that in Switzerland you would have a consumption of about 150 g of carbohydrate from soft drinks, which means an average intake of more than 1 1 per day of soft drinks. That is a huge consumption compared to the international average. Dr. Gruskin: In the last 20 years, the use of fluoride drops has been associated with dramatic decreases in dental caries. It is also possible that this effect has been impacted by the increased exposure to soft drinks. I am curious to know whether the various studies that you reviewed have taken into account previous usage of fluoride. Dr. Guesry: Between the end of the 1960s and the beginning of the 1980s there was an increase in dental caries in Greece and Spain parallel to the increase in consumption of sugar by the country. During the same period, with no change in consumption of sugar, a decrease in dental caries occurred in Finland, Belgium, and United Kingdom which was attributed to the use of fluoride. Dr. Gallart Catald: A report from the American Academy of Pediatrics about fluoride and modifications for fluoride supplementation has been recently published (5). The recommenda- tions have been reassessed because of what seems to be an increased incidence of dental fluorosis in children living in the United States. Is it possible that soft drinks contribute to increase fluoride ingestion? What is the concentration of fluoride in these drinks? For instance, in Spain, there is a mineral water containing 2 ppm of fluoride and this is very commonly drink. Dr. Guesry: We know the advantage of adding fluoride to the diet of children to protect against dental caries, but the limit between what is useful and what might be dangerous is narrow. This is why in many countries fluoridation of tap water is not allowed. We know also that in certain countries, the natural water supply is rich in fluoride and in certain countries, milk is also rich in fluoride. We have not analyzed soft drink fluoride content, so I can't answer your question. But it probably depends on the type of water that is used, which will vary from country to country. As you know, the most important soft drink companies ship concentrates overseas which are reconstituted locally with sugar and water, and of course, depending on the water you use, the concentration of fluoride could vary widely. Dr. Agostoni: If I remember correctly, Wurtman and others were worried by the possible effects of aspartame, not in the normal population but in heterozygotes for phenylalanine NUTRITIONAL ROLE OF SOFT DRINKS 185 hydroxylase deficiency (who are often unaware of their condition), and they are still worried that there might be a detrimental effect on the fetus in heterozygous pregnant women. Dr. Guesry: I agree, when you have the genetic trait for phenylketonuria, you should adapt the phenylalanine intake to your tolerance. Dr. Bonjour: Over a wide range of phosphate intake, we did not find an association between this element and bone mass in our study, but following your suggestion, I will go back to our data and look at the phosphate intake from soft drinks and see whether we can find any association. Dr. Guesry: Two liters a day of these carbonated soft drinks would provide 60% of your recommended daily intake of phosphate. Also the foods commonly consumed in Western countries, which are mainly industrialized foods, are preserved with phosphate. Thus we have an accumulation of phosphate in the diet as I mentioned. If you combine this with a net acid load of about 20 mmol per liter, the low pH, and the caffeine, I wonder if all this could not be deleterious for bone calcification. I mention caffeine because there was a recent report on postmenopausal women where there was a relation between caffeine consumption and the level of osteoporosis (6).

REFERENCES

1. Hourihane JO'B, Rolles CJ. Morbidity from excessive intake of high energy fluids: the "squash drinking syndrome." Arch Dis Child 1995; 72: 141-3. 2. Hill R, Kamath KR. "Pink" diarrhoea. MedJAust 1982; 1: 387-9. 3. Hoekstra JH, van Kempen AAMW, Kneepkens CMF. Apple juice malabsorption: fructose or sorbitol? J Pediatr Gastroenterol Nutr 1993; 16: 39-42. 4. Hackett AF, Rugg-Gunn AJ, Appleton DR, Eastoe JE, Jenkins GN. A 2 year longitudinal nutritional survey of 405 Northumberland children initially aged 11.5 years. Br J Nutr 1984; 51: 67-75. 5. AAP/CON. Fluoride supplementation for children: Interim Policy Recommendations. Pediatrics 1995; 95: 777. 6. Harris SS, Dawson-Hughes B. Caffeine and bone loss in healthy postmenopausal women. Am J Clin Nutr 1994; 60: 573-8.