Carbonated Soft Drink Consumption and Bone Mineral Density in Adolescence: The Northern Ireland Young Hearts Project

Abstract

In an observational study of 1335 boys and girls aged 12 and 15 years, higher intakes of carbonated soft drinks (CSDs) were significantly associated with lower bone mineral density at the heel, but only in girls. Owing to the upward trend in CSD intake in adolescence, this finding may be of concern.

Introduction: High consumption of carbonated soft drinks (CSD) during adolescence may reduce bone mineral accrual and increase fracture risk. The aim of this study was to examine the relationship between CSD consumption and bone mineral density (BMD) in a representative sample of adolescents.

Materials and Methods: This was a cross-sectional observational study in 36 postprimary schools in Northern Ireland. Participants included 591 boys and 744 girls either 12 or 15 years old. BMD was measured by DXA, and usual beverage consumption was assessed by the diet history method. Adjusted regression modeling was used to investigate the influence of CSD on BMD.

Results: A significant inverse relationship between total CSD intake and BMD was observed in girls at the dominant heel (β, −0.099; 95% CI, −0.173 to −0.025). Non-cola consumption was inversely associated with dominant heel BMD in girls (β, −0.121; 95% CI, −0.194 to −0.048), and diet drinks were also inversely associated with heel BMD in girls (β, −0.087; 95% CI, −0.158 to −0.016). However, no consistent relationships were observed between CSD intake and BMD in boys. Cola consumption and nondiet drinks were not significantly related to BMD in either sex.

Conclusion: CSD consumption seems to be inversely related to BMD at the dominant heel in girls. It is possible that the apparent association results from the displacement of more nutritious beverages from the diet. Although the inverse association observed between CSD consumption and BMD is modest and confined to girls, this finding may have important public health implications given the widespread use and current upward trend in CSD consumption in Western populations.

INTRODUCTION

The adolescent growth period is a critical time for bone development,⁽¹⁾ and it is acknowledged that diet and lifestyle behaviors operating during this period may have important consequences for peak bone mass attainment and future fracture risk. Small scale studies indicate that high consumption of carbonated soft drinks (CSDs), particularly colas, during this period may reduce bone mineral accrual and increase fracture risk.^(1,2) Mechanisms that have been postulated to explain this apparent relationship include the displacement of milk from the diet,⁽³⁾ a high dietary acid load causing increased calcium excretion,⁽⁴⁾ or a direct effect of the phosphorus,⁽¹⁾ fructose,⁽⁵⁾ or caffeine⁽⁶⁾ content of these products.

Consumption of CSDs is extremely popular in affluent western populations, particularly during adolescence.⁽³⁾ Sales of CSDs within the United Kingdom exceed those of most other European countries, with higher sales seen only in Ireland and the United States.^(7,8) Furthermore, with aggressive marketing techniques aimed at children and adolescents,⁽⁸⁾ sales of these products are likely to increase in coming years.⁽⁷⁾ If the consumption of these drinks reduce bone mineral density (BMD), the threat to future public health may be substantial. We investigated the relationship between CSD intake and adolescent BMD in a large cross-sectional study in Northern Ireland.

MATERIALS AND METHODS

Study population

The Young Hearts 2000 (YH2000) survey is the second in a series of large, cross-sectional epidemiological studies performed in a representative sample of Northern Irish adolescents. The target of the study was to recruit approximately 500 children in each of four age-sex groups (12- and 15-year-old boys and girls). Children were recruited through postprimary schools. Schools were stratified by education area board and by school selection policy (grammar and non-grammar). From each stratum, a two-stage cluster sample of children was obtained. The primary sampling units were the 36 schools randomly selected with probabilities proportional to school size; the secondary units were the children randomly selected from the appropriate age-sex groups within the school. Study numbers represented 3.9% of 12 year olds and 3.6% of 15 year olds in Northern Ireland. Ethical approval was obtained from the Research Ethics Committee of The Queen's University of Belfast, and written consent for participation in the study was obtained from the subject and from each subject's parent or guardian. Subjects were screened at schools during normal school hours.

Assessment of BMD

BMD of the nondominant forearm (distal radius) and dominant heel (os calcis) were measured by DXA using the Norland Lunar PIXI bone densitometer (Lunar Corp., Madison, WI, USA). Before each scan, the densitometer was calibrated using quasi-anthropomorphic phantoms according to the manufacturer's recommendations. The results of the scan were expressed as BMD in grams of calcium hydroxyapatite per square centimeter.

Dietary intake assessment

Dietary data were collected using a nutritionist-administered diet history method, using an open-ended interview,⁽⁹⁾ to ascertain the habitual food and beverage intake of each subject. In the age groups under study, the diet history method has been shown to produce more valid estimates of energy intake at group level than weighed records.⁽¹⁰⁾ Energy and nutrient intakes were calculated using a computerized food composition database (WISP; Tinuviel Software, Warrington, UK). A food file was also created using WISP software. For each subject, the food file recorded every type of food eaten, the quantity of every food eaten, and the energy and nutrient values corresponding to the specific weight of each food recorded. For the purposes of this study, CSDs were defined as all nonalcoholic carbonated drinks. In addition, colas were defined as drinks using phosphoric acid as the acidulant and non-colas were defined as any drink using citric acid as the acidulant. Carbonated soft diet drinks were defined as beverages that contained artificial sweeteners (e.g., aspartame) instead of added sugar. Liquid milk intake was defined as any liquid milk consumed, including that taken with breakfast cereals. All drinks were recorded and analyzed in grams per day. Calcium from other sources was defined as calcium derived from sources other than liquid milk.

Other measurements

Standing height was measured to the nearest millimeter using a Holtain stadiometer (Holtain Ltd., Crymych, Dyfed, UK), and body weight was measured to the nearest 0.1 kg using a Seca 770 electronic weighing scale (Seca Ltd., Hamburg, Germany). For both measurements, subjects wore light indoor clothes and no shoes. The pubertal status of each subject was assessed by a pediatrician, using visual signs such as nongenital secondary hair growth, vocal timber, body habitus, general muscular development, and overall breast development in girls.

For the girls, the length of time postmenarche was used as proxy for estrogen exposure. Lifestyle data were obtained by a self-report questionnaire, which included questions on smoking and drinking habits. Socioeconomic status was assessed by each subject's father's socioeconomic status obtained from the parental questionnaire and was coded according to the Office of Population Censuses and Surveys Standard Occupational Classification (1990).⁽¹¹⁾ Physical activity data were obtained using a modification of the Baecke questionnaire of habitual physical activity,⁽¹²⁾ which was designed to quantify work activity, sports activity, and nonsports leisure activity. Body fat was measured to the nearest 0.1 mm using Harpenden skin-fold calipers at four sites on the dominant side of the body: mid-biceps, mid-triceps, super-iliac, and subscapular. These four measurements enabled estimation of the subjects body fat composition according to Durnin.⁽¹³⁾

Statistical analyses

Statistical analyses were performed using SPSS (SPSS for Windows 10.0; SPSS Inc., Chicago, IL, USA). Independent sample t-tests were used to determine differences in BMD measurements, height, weight, and reported dietary intakes between boys and girls aged 12 years, and also between boys and girls aged 15 years. Independent t-tests were also used to ascertain if there were any differences between subjects with BMD data and those without. ANOVA was performed to assess differences in percentage body fat between subjects who reported low, moderate, or high levels of physical activity, and also low, moderate, and high consumers of CSDs, correcting for multiple testing using the Duncan range test.

Sex-specific regression analyses were then undertaken to assess the extent of the relationship between CSD intake and BMD. Univariate models were constructed with forearm BMD or heel BMD as the dependent variable and CSD intake as the explanatory variable. Multivariate models were then constructed with adjustment for potential cofounders including age, height, weight, pubertal status, social status, alcohol intake, smoking habits, physical activity, liquid milk consumption, and calcium obtained from sources other than liquid milk. These models were repeated within tertiles of physical activity.

RESULTS

Of the 3147 children randomly selected for the study, 64% (2017) agreed to participate. Owing to limited availability of the bone densitometer, not all subjects had BMD measurements taken. BMD measurements were available at the forearm for 591 boys and 744 girls and at the heel for 587 boys and 740 girls. There were no differences in physical, dietary, or lifestyle characteristics between subjects with BMD data and those without (data not shown).

Table 1 presents subject characteristics, BMD measurements, and selected nutritional information for the study population. Boys aged 12 years had higher forearm BMD, heel BMD, were more physically active, and reported consuming more CSDs, liquid milk, and calcium from other sources than their female counterparts. Girls aged 12 years were taller and heavier than boys aged 12 years. Boys aged 15 years were taller, heavier, had higher heel BMD, were more physically active, and reported consuming more CSDs and liquid milk than their female counterparts. Girls aged 15 years had higher forearm BMD than boys aged 15 years.

Table Table 1. Descriptive Characteristics of the Study Population

In univariate analysis, total CSD intake was not related to forearm BMD, but at the heel, a significant inverse relationship was observed in girls (β = standardized regression coefficient, −0.122; 95% CI, −0.195 to −0.049). Cola consumption was not related to forearm or heel BMD in either girls or boys. No association was apparent between non-cola consumption and forearm BMD in either sex, but at the heel, a significant inverse relationship was apparent in girls (β,−0.121; 95% CI, −0.194 to −0.048). No consistent relationship between heel BMD and non-cola consumption was observed in boys. In univariate analysis, nondiet drinks were inversely related to forearm and heel BMD in girls (β,−0.076; 95% CI, −0.149 to −0.003 and β, −0.139; 95% CI, −0.210 to −0.069, respectively); no association was observed in boys. No consistent relationship was observed between diet drinks and BMD in boys or girls.

Table 2 illustrates the adjusted relationships between CSD consumption and BMD at the forearm and heel. After adjustment for height, weight, and pubertal status, a significant inverse relationship of CSD intake was apparent in girls at the forearm and at the heel. Further adjustment for lifestyle factors including physical activity, social class, smoking, alcohol intake, liquid milk intake, and calcium from other sources slightly attenuated this relationship. No consistent relationship was observed between BMD and CSD consumption in boys. Inclusion of length of time postmenarche did not affect any of the relationships observed (data not shown). Habitual activity was positively related to higher BMD at the forearm in girls and boys (β, 0.062; 95% CI, −0.001 to 0.123 and β, 0.133; 95% CI, 0.055 to 0.211, respectively) and at the heel in girls and boys (β, 0.111; 95% CI, 0.040 to 0.182 and β, 0.098; 95% CI, 0.027 to 0.169, respectively). The association between CSD and BMD of the forearm in girls was stronger in highly active girls (β,−0.120; 95% CI. −0.230 to −0.010) in comparison with the moderately (β,−0.059; 95% CI, −0.161 to 0.043) and low active girls (β,−0.010; 95% CI, −0.130 to 0.110). A similar effect was observed at the heel but to a lesser extent; in boys no such effect was apparent.

Table Table 2. Unadjusted and Adjusted Regression Analysis of the Relationship Between Total Carbonated Soft Drink (CSD) Intake and Forearm and Heel BMD

Table 3 presents the adjusted relationships between cola intake, non-cola intake, diet drinks, and nondiet drinks and BMD. The adjusted relationships between cola consumption and BMD at the forearm and heel revealed no association with either site. The adjusted relationship between non-cola consumption and BMD demonstrated a significant inverse relationship at the heel in girls, but no relationship was seen in boys. The adjusted relationship between diet drinks and BMD demonstrated a significant inverse association at the heel in girls. Nondiet drinks had an association similar in magnitude at the heel in girls, but this failed to reach statistical significance. No associations were observed in boys. No independent association was observed between reported dietary phosphorus intakes and BMD at either site (results not shown).

Table Table 3. Adjusted Regression Analysis Between Cola and Non-Cola Consumption and Diet and Non-Diet Drinks and Forearm and Heel BMD

Table 4 illustrates the overall relationship between intakes of CSDs and percentage body fat and intakes of liquid milk, calcium (mg/day and mg/MJ/day), and phosphorus. Subjects consuming high and moderate quantities of CSDs had significantly lower intakes of liquid milk than low CSD consumers, as well as lower intakes of calcium expressed in terms of nutrient density. However they also had higher intakes of dietary phosphorus and total calcium. No differences in percentage body fat were observed between low, moderate, and high consumers of CSDs. There were also no differences in percentage body fat in girls or boys between low, moderate, and high levels of activity. In regression modeling, liquid milk consumption had a significant independent effect on forearm BMD (β, 0.110; 95% CI, 0.032 to 0.188) and heel BMD (β, 0.084; 95% CI, 0.013 to 0.155) in boys. In girls, liquid milk consumption was independently related to heel (β, 0.076; 95% CI, 0.007 to 0.145) but not forearm BMD.

Table Table 4. Percentage Body Fat and Intakes of Liquid Milk, Calcium (mg/d and mg/MJ/d) and Phosphorus by Tertile of Carbonated Soft Drink Intake (CSD)

DISCUSSION

This study differs from previous reports^(2,14) that have investigated the relationships between CSDs and bone health, in that it examines BMD in a large, representative population of healthy adolescents. Another strength of the study lies in its use of a relatively robust, validated method^(9,10) for the collection of data concerning habitual food and beverage intake in an adolescent population. In addition, the current study collected extensive information on factors known to affect bone health such as body weight, physical activity, smoking, and drinking habits, enabling the relationship between BMD and CSD consumption to be adjusted for the potential confounding effect of these variables. One potential limitation of this study may be the assessment of pubertal status. It was not possible to use Tanner Staging, owing to the personal nature of the method and unwillingness of subjects to be examined fully in the required manner. Instead, pubertal status was assessed by a pediatrician, using visual signs of secondary sexual characteristics, which may have weakened our ability to discriminate between the various pubertal stages in this adolescent population.

Nevertheless, in common with the only other study to have examined CSD intake and its relationship to bone health, we demonstrated an inverse relationship between heel BMD and CSD consumption in girls. A weaker relationship in the same direction was also seen at the forearm in girls, although statistical significance was not achieved. No such effect was evident for boys, although boys consumed more CSDs than girls. Boys, however, also consumed more liquid milk and participated in more physical activity; behaviors that are known to enhance bone mass.^(15,16) It is also possible that there is a threshold effect for calcium⁽¹⁷⁾ and physical activity,⁽¹⁸⁾ which boys are surpassing and girls are not, enabling boys to consume more CSDs without impinging negatively on their bone health. In the past, the investigation of CSDs in relation to bone health has focused on the consumption of cola beverages.^(14,19) The current study was unable to confirm previous reports of a strong inverse association between cola beverage consumption and bone health. We were, however, able to show an association with non-cola carbonated beverages and BMD at the heel in girls, indicating that it may not be the specific compounds in colas that affect BMD. Total volume of all CSDs may be more important, providing support for the contention that CSDs may be displacing more nutritious beverages from the diet. Furthermore, it has been postulated that the added sugar content of CSD may be responsible for the inverse relationship with BMD. However, given the statistically significant negative effect of diet carbonated soft drinks on BMD in the girls, we suggest that the inverse relationship between CSD and BMD in girls is not likely to be the result of an increase in sugar intakes derived from CSD. In agreement with two previous studies,^(2,20) we found that liquid milk consumption decreased with increased CSD intake. This and other studies have demonstrated positive relationships between milk consumption and bone density.⁽²¹⁾ Milk has been well recognized as a source of calcium and phosphorus in an optimal ratio for building bone tissue.⁽²²⁾ Thus, the bone specific nutritional benefits derived from milk products may be reduced in individuals consuming higher quantities of CSD. While there was no consistent relationship between absolute intakes of calcium across the tertiles of CSD intake, we observed that the calcium density of the diets decreased significantly as CSD consumption increased. The latter observation reflects that the quality of the diet with respect to calcium becomes poorer as CSD intake increases. However, owing to the cross-sectional nature of the study, it is impossible to ascertain whether the negative effect of CSD consumption on BMD is owing to the CSD, or whether lower BMDs are as a result of poorer calcium profiles. Furthermore, it is possible that the overall combined effect of a healthy diet and exercise results in individuals having higher BMD, although we attempted to account for the potential effect of this healthier lifestyle by correcting for social class and physical activity. However, it is also possible that moderate and high consumers of CSD may be partaking in something detrimental to their bone health that as yet we are unaware of.

While the current study does not support the hypothesis that CSD provides a sufficient amount of phosphorus to inversely affect bone health,⁽¹⁴⁾ it does support the theory that increasing CSD intake, concomitant with decreasing milk consumption, may disrupt the calcium: phosphorus ratio. However, displacement of milk does not fully explain our findings, as the negative relationship between CSD consumption and BMD remained (although weakened), following adjustment for liquid milk consumption and calcium derived from other sources.

To our knowledge, this is the first study to report decreased BMD at the heel in adolescent girls consuming moderate to high amounts of CSD. We describe a stronger negative association of CSD on bone density at the heel than at the wrist. This may be because the heel is composed mainly of trabecular bone, in contrast to the forearm, which is comprised mainly of cortical bone. Trabecular bone is more metabolically active than cortical bone⁽²³⁾ and may be more susceptible to nutritional influences. The current study found that the inverse association of CSD intake and BMD was stronger in moderately and highly active girls than in sedentary girls. It is important to note, however, that our finding does not imply that physical activity per se is detrimental to bone health in girls. Indeed we have shown that physical activity is positively independently associated with BMD in girls and that moderately and highly active girls have significantly higher BMD than those in the low activity group. However, the detrimental influence of CSD intake seems to be more pronounced in moderate and highly active girls than sedentary girls. This finding is somewhat surprising and is not readily explained as the more physically active girls consumed greater quantities of liquid milk and lower quantities of CSD than the less active girls. It is possible that our measurement of physical activity may not adequately capture all activities undertaken and therefore the finding may be spurious. However, it concurs with Wyshak, who found that consumption of cola drinks was particularly associated with bone fractures in physically active girls.⁽¹⁾ In view of the fact that a similar relationship has been reported, further study would be warranted to establish the connection between physical activity and CSD consumption.

In placing the observed association between CSDs and BMD in context of other modifiable factors known to influence BMD, we show the inverse relationship between CSDs and BMD to be similar in magnitude to the positive association between physical activity and BMD. This highlights the importance of our finding as physical activity has been reported to be essential in the development of peak bone mass.⁽²⁴⁾

Although the current study cannot attribute a causative relationship between CSD consumption and BMD, it indicates that CSD consumption may displace more nutritious beverages in the diets of UK adolescents, with potential deleterious consequences for future fracture risk. Although any effect of CSD intake on BMD may be modest, the widespread intake of these products and the projected increase in their consumption⁽⁷⁾ could have substantial public health implications. If the results of this study are substantiated, the consumption of nutritious beverages should be actively promoted as an alternative to CSD and the aggressive marketing policy of soft drink companies tempered.

Acknowledgements

The authors thank Sinead McElhone, Rose O'Neill, and Oriel Ward for collecting the data. We also extend our thanks to the Department of Health, Social Services and Public Safety for Northern Ireland (DHSSPS NI) for funding the Young Hearts Project, and finally, we thank all the young participants for their time and enthusiasm.