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        Primary Care Respiratory Journal (2011); 20(1): 75-78



        ORIGINAL RESEARCH

        Per capita sugar consumption is associated with severe
        childhood asthma: an ecological study of 53 countries
        *Simon Thornleya, Alistair Stewarta, Roger Marshalla, Rod Jacksona
        a
            Section of Epidemiology and Biostatistics, School of Population Health, Tamaki Campus, University of Auckland, Auckland,
            New Zealand

        Received 10th March 2010; revised 14th July 2010; accepted 18th September 2010; online 28th December 2010

            Abstract
            Aims: To examine the ecological association between population asthma symptom prevalence in six to seven year-old children and per




                                                                                                            K
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            capita sugar consumption seven years earlier (during the perinatal period).




                                                                                                       y
            Methods: The asthma data (from the International Study of Asthma and Allergies in Childhood [ISAAC] study) were collected between




                                                                                                    et
            1999 and 2004 from 53 countries, and per capita sugar consumption data (seven years before the asthma prevalence) were extracted from




                                                                                i
                                                                             oc
            United Nations Food and Agriculture (UNFAO) food balance sheets. Linear regression and Spearman’s rank coefficient were used to




                                                                       ite S
            evaluate the relationship between exposure and disease outcome.

                                                                     ib ory
            Results: Per capita sugar consumption varied more than six fold-between countries. A log-linear relationship was found between severe


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                                                                   oh at
            asthma symptoms (%) and per capita added sugar consumption in kg/capita/year (exponentiated beta coefficient 1.020; 95% CI 1.005 to
                                                                 pr ir

            1.034; P = 0.012). Spearman’s rank correlation coefficient was 0.34 (P= 0.015), which indicates moderate correlation.
                                                                n sp


            Conclusions: We have demonstrated an ecological association between sugar consumption during the perinatal period and subsequent
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            risk of severe asthma symptoms in six and seven year-olds.
            © 2011 Primary Care Respiratory Society UK. All rights reserved.
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            S Thornley et al. Prim Care Respir J 2011; 20(1): 75-78
                                                        ro C




            doi:10.4104/pcrj.2010.00087
                                                   ep ry
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        Keywords asthma, aetiology, ISAAC data, sugar consumption, observational study, nutrition
                                                      i
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        Introduction                                                             Childhood (ISAAC) has generated individual level information on
                                                ht




                                                                                 asthma symptoms and putative exposures from 463,801
                                              ig




        The global prevalence of both obesity and asthma has increased
                                           yr




        substantially in the last forty years.1 The co-occurrence of these       children aged between 13 and 14 years and 257,800 children
                                       op




        two epidemics has led some investigators to propose that                 aged 6 and 7 in 58 countries.6 The authors reported considerable
                                     C




        nutritional factors responsible for obesity may also cause               variation in the prevalence of asthma between countries
        asthma.2,3 The association between obesity and asthma at an              (measured with a standardised definition), suggesting that
        individual level has been reported, and remains controversial.3          potentially avoidable causes may be present.
        Links between obesity and asthma have been drawn in both                     The importance of exposures during the perinatal period has
        children and adults and a number of hypotheses put forward to            been highlighted for both obesity and asthma7,8 and several
        explain these links.                                                     reports have shown that rapid growth after birth is associated
            Recently, we proposed that increased refined carbohydrate            with increased risk of asthma.7 We therefore linked UNFAO and
        intake may be responsible for increasing prevalence of obesity.4         ISAAC data from 53 countries to explore the possibility of an
        Ecological analyses of country-level per capita food                     association between added sugar consumption and asthma
        disappearance data on added sugar, from the routinely                    symptom prevalence, linking country-level data on severe
        published United Nations Food and Agriculture (UNFAO) Food               asthma symptoms in children aged 6-7 years with per capita
        Balance Sheets, supports our hypothesis.5                                added sugar consumption data in the same countries during the
            The International Study of Asthma and Allergies in                   children’s perinatal period, seven years earlier.


        * Corresponding author: Dr Simon Thornley, Section of Epidemiology and Biostatistics, Level 4, School of Population Health,Tamaki Campus, The
          University of Auckland, Private Bag 92019, Auckland 1151, New Zealand. Tel: +6493737599 ext 81971 E-mail: s.thornley@auckland.ac.nz

        PRIMARY CARE RESPIRATORY JOURNAL                                         75
        www.thepcrj.org
        doi:10.4104/pcrj.2010.00087


                                                        http://www.thepcrj.org
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        S Thornley et al.



        Methods                                                                       sugar consumption is calculated by taking the difference of
        Outcome data – asthma symptom prevalence                                      quantity of the sum of added sugar imported and produced
        The ISAAC study, Phase Three, generated asthma symptom                        from total added sugar exported or used for industry. The
        prevalence information at country level, drawn from surveys of                quantity that remains has therefore ‘disappeared’ and is
        6-7 and 13-14 year-old children, using a standardised                         assumed to have been consumed. Food balance sheet data,
        questionnaire, from 58 countries. A number of indicators of                   therefore, does not account for food either not consumed or
        asthma prevalence have been reported including current                        wasted.
        wheeze, parental- (6 to 7 year-olds) or self- (13 to 14 year-old) Data analysis
        reported asthma, and symptoms of severe asthma. We used the We linked the exposure and outcome data using linear
        6-7 year-old age group with “symptoms of severe asthma” as regression and Spearman’s rank correlation coefficient.
        our measure of asthma prevalence because we believed that this Asthma symptom prevalence was log transformed to stabilise
        category would be most consistently reported between its variance. The R-project was used for all analyses.
                                                                                                                                                      10



        countries and may be less subject to measurement error than the
        other reported measures of “current wheeze” and the question Results
        “has your child ever had asthma?”.                                   We found estimates of severe asthma symptom prevalence for




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            Symptoms of severe asthma included respondents with 58 countries from ISAAC publications, but five of these countries




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        one or more of the following symptoms:                               did not appear in UNFAO food balance records, leaving 53




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        (1) > 4 attacks of wheeze in the last year, or,                      countries with paired data for analysis. Symptom prevalence




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        (2) > one or more nights per week sleep disturbance from ranged from 1.1% in Indonesia to 20.3% in Costa Rica. Sample




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                                                                             sizes of surveys ranged from 1,181 (Bulgaria – one survey) to


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            wheeze in the last year, or,

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        (3) wheeze affecting speech in the last year.                        46,761 (India – pooled estimate). Severe asthma symptom
                                                                             prevalence was generally higher in English speaking and Latin

                                                                                                         d
            Published prevalence estimates for
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        these countries were derived from surveys
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        carried out between 1999 and 2004.6 Figure 1. Severe asthma symptom prevalence in 6 and 7 year-old children
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        Although we have reported country                plotted against average per capita added sugar consumption, 7 years
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        estimates, these surveys were taken from         prior, by country. Solid line shows log-linear regression line with dashed
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        specific localities within countries – and in    lines illustrating 95% confidence intervals.
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        some cases, several regional study results
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        have been pooled to provide a total                                                                                                           Costa Rica
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        country estimate.                                                                                                                              Cuba
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        Exposure data – added sugar
                                               Severe asthma symptom prevalence (%)




        consumption
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                                                                             ig




        We used the United Nations Food and
                                            yr




        Agricultural Organisation (UNFAO) food
                                                                         15
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        balance sheets9 to estimate per capita
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                                                                                             Sri Lanka
        consumption of a variety of simple
                                                                                                                      Venezuela                Brazil
        carbohydrates. We used the UNFAO
                                                                                                         South Africa   UK
        category “sugar and sweeteners” which                                                                              Jordan      New Zealand
                                                            10




                                                                                                       Nicaragua
        includes a variety of monosaccharides and                                                           Panama
                                                                                                    Uruguay                         Australia
        disaccharides which mainly consist of                                                                       Honduras

        sucrose (from sugar beet or cane), glucose,                Nigeria
                                                                                                                                 Argentina
                                                                                                                                             Barbados
                                                                                                                                            Canada
        honey or high fructose corn syrup referred
                                            5
                                                                                                             El Salvador Poland Chile
        to here as “added sugar”. Such foods are                                                      Bulgaria                       Germany
                                                                                                                 Ecuador
                                               5




                                                                  Vietnam                                                                 Colombia
                                                                           Kyrgyzstan Thailand Pakistan                    Sweden
        high in fructose concentration, either free                                              Iran Portugal                         Malta
                                                                                                       Japan Russia Ukraine
        or as part of a disaccharide (i.e. sucrose).                                Georgia       Estonia                       Belgium Mexico
                                                                                            India                                             Croatia
                                                                                                       Italy Greece Syria
        This nutrient exposure information was                               Serbia and Montanegro                             Austria
                                                                                                                Korea                       Hungary
                                                                           Indonesia               Albania                   Malaysia
        extracted from the period when the                                                                Lithuania

        mothers of the children surveyed for
                                                                       10            20                30               40               50               60
        asthma symptoms were most likely to be
                                                                                  Added sugar consumption (kg/capita/year)
        pregnant (seven years before the asthma
        survey was undertaken). Per capita added

        PRIMARY CARE RESPIRATORY JOURNAL                                              76
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        Sugar consumption and childhood asthma



        American countries, with lower estimates in Asia, Eastern              previously identified many causal associations. We have linked
        European and Mediterranean countries. Per capita added sugar           an estimate of total per capita added sugar disappearance at a
        consumption recorded seven years before the asthma surveys             country level to an estimate of asthma symptom prevalence
        varied more than six-fold, with lowest average consumption in          from either one or an aggregation of regional population
        Vietnam (8.15 kg/capita/year in 1994) and highest in Costa Rica        samples for a defined age group in these countries. We do not
        (58.95 kg/capita/year in 1995) and Cuba (58.23 kg/capita/year in       know if the relative or total consumption of added sugar in
        1995), two sugar exporting nations. The bivariate distribution of      pregnant women is likely to be similar to the population
        the data is displayed in Figure 1. A log-linear relationship was       average. The accuracy of food disappearance data to measure
        found between severe asthma symptoms (%) and per capita                actual food intake is also unknown. Previous studies have
        sugar consumption in kg/capita/year (exponentiated beta                focused on the use of this data to estimate average and relative
        coefficient 1.020; 95% CI 1.005 to 1.034; P=0.012 [estimate            fat intakes.11 Another limitation of our analysis was the
        and 95% CI displayed in Figure 1]). The model indicates that           exclusion of the United States (USA), which did not report
        centres with a further 35 kg/capita/year greater added sugar           asthma symptom prevalence in this phase of the ISAAC study.
        disappearance have double the symptom prevalence compared              If included, the USA had the highest per capita sugar
        to a country with lesser consumption. Although most countries          consumption of any country in our cohort, with 66.4




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        occupy the area within the bounds of uncertainty of the                kg/capita/year consumed in 1994. In earlier phases of the




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        regression estimate, some outliers exist such as Nigeria and Sri       ISAAC study, the USA prevalence of asthma in 13 to 14 year




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                                                                                                et
        Lanka, with unexpectedly high prevalence given their average           old children was about 20% or 8th out of 56 surveyed




                                                                              i
        sugar consumption. Conversely, Hungary, Austria and Malaysia           countries, immediately below Brazil.12 If the USA had a similar




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        have low rates of asthma at relatively high levels of sugar            between-country rank for 6 to 7 year-old severe asthma


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                                                                   ib ory
        consumption. Plots of residual versus predicted values indicated       symptoms, the inclusion of this data point would further
        acceptable model fit. When data from two high outliers (Costa          strengthen the relationship we found between other countries.

                                                                        d
                                                                 oh at
        Rica and Cuba) were excluded, the magnitude of the                          A strength of this study lies in the use of the ISAAC study
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        exponentiated beta coefficient reduced to 1.013 (95% CI 0.998          information, which has provided the most comprehensive,
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        to 1.028; P=0.104).                                                    standardised, between-country attempt to estimate global
                                                          ct e R




            Our regression analysis implies directionality, so that average    asthma prevalence in children to date. Also, the ubiquitous
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        between-country asthma symptom prevalence is estimated from            nature of sweeteners in modern diets suggests that our study
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        observed values of added sugar consumption, which reflects our         is less likely to suffer from confounding related directly or
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        a priori belief that increased sugar consumption influences            indirectly to food choices. Our sensitivity analysis, which
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        asthma symptom prevalence. Spearman’s rho rank correlation             excluded two outliers, showed that a positive relationship was
                                                    i




        coefficient, in contrast, is an unconditional measure of               still observed between the variables, although the strength of
                                                 Pr




        association, estimated at 0.34 (P= 0.015) – which indicates            the association was diminished.
                                              ht




        moderate correlation between the two variables.                             Despite multiple possible sources of error, we have
                                            ig
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                                                                               demonstrated a correlation between these two variables,
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        Discussion                                                             which is unlikely to be due to chance alone. These findings
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        Per capita added sugar consumption (an indirect indicator of           were not part of a ‘data trawling’ exercise but represent the
        perinatal sugar exposure) estimated from FAO food balance              first joint analyses of these datasets by the first author (ST),
        sheets, positively correlated with between-country level               who is developing a research program on the relationship
        estimates of severe asthma symptom prevalence in 6 and 7               between refined carbohydrates and disease. Also,
        year-olds, measured seven years later. Of note, the two                epidemiological evidence of rising sugar consumption,5 the
        countries with the highest recorded prevalence of severe               rising prevalence of obesity,1 and the reported association
        asthma symptoms also had the highest average rate of sugar             between asthma and obesity2 at an individual level make a
        consumption. This association explains the pattern of high             plausible argument to link these disorders.
        rates of childhood asthma in English speaking and Latin                     Although these trends coincide, we can only speculate on a
        American countries. Also, the countries with the top five              biological mechanism that may link sugar consumption and
        highest prevalence of severe asthma in this age group (Costa           childhood asthma.5 The generally accepted co-occurrence of
        Rica, Cuba, Sri Lanka, Venzuela and Brazil) all have local sugar       obesity and asthma is still poorly understood at a physiological
        manufacturing industries.                                              level. Adipose tissue secretes hormones such as leptin, which
            Our analysis, like all ecological studies, is limited by the use   induces satiety in the hypothalamus but also modulates the
        of aggregate data. These types of studies are prone to                 function of T-helper immune cells.13 Other disorders that are
        measurement error and confounding, but nevertheless have               linked with the immunocompromised state – such as a range of

        PRIMARY CARE RESPIRATORY JOURNAL                                       77
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        S Thornley et al.



         Summary
                                                                                Although by no means confirmatory, this study raises the
                                                                            possibility of a link between increasing global sugar
          This study shows a moderate association between per capita        consumption and asthma prevalence. Longitudinal studies –
          sugar consumption during the perinatal period and                 both observational and experimental – using individual level
          subsequent prevalence of severe childhood asthma                  information are needed to investigate further the strength of
          symptoms. This association explains the pattern of high rates     this association.
          of childhood asthma in English speaking and Latin American
                                                                            Conflict of interest declarations
          countries. Cohort studies that collect detailed nutrient
                                                                            None.
          information, may further investigate the strength of this
          association. If sugar consumption is causally associated with     Funding
                                                                            This work was funded by a salaried position at the University of Auckland
          the onset of childhood asthma, restricting intake of this
          substance is likely to improve symptoms and reduce
                                                                            References
          frequency of exacerbations in people with established             1.   OECD, OECD Health Data 2009: Statistics and Indicators for 30 Countries.
          disease.                                                               2009, OECD publishing: Paris.
                                                                            2.   Deane S, Thomson A. Obesity and the pulmonologist. Arch Dis Child 2006




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                                                                                 91(2):188-91. http://dx.doi.org/10.1136/adc.2005.072223




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        cancers – are also linked to obesity.14 However, the mechanism by   3.   Ford ES. The epidemiology of obesity and asthma. Journal of Allergy and




                                                                                                         y
                                                                                 Clinical   Immunology     2005;115(5):897-909.       http://dx.doi.org/10.1016/
        which obesity and asthma are linked is yet to be determined.13,15




                                                                                                      et
                                                                                 j.jaci.2004.11.050




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            To our knowledge, this is the only study so far to link sugar




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                                                                            4.   Thornley S, McRobbie H, Eyles H, Walker N, Simmons G. The obesity epidemic:
        or fructose with asthma symptom prevalence. Although



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                                                                                 is glycemic index the key to unlocking a hidden addiction? Medical Hypotheses
        previous studies have attempted to uncover a dietary link
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                                                                                 2008;71(5):709-14. http://dx.doi.org/10.1016/j.mehy.2008.07.006
        between childhood asthma and dietary factors, most studies          5.   Popkin BM, SJ Nielsen. The sweetening of the world's diet. Obesity Research



                                                                       d
                                                                oh at
                                                                                 2003;11(11):1325-32. http://dx.doi.org/10.1038/oby.2003.179
        have focused on the role of different sub-types of fats, vitamins
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                                                                            6.   Lai CK, Beasley R, Crane J, Foliaki S, Shah J, Weiland S. Global variation in the
                                                             n sp


        or trace elements,13 none of which show persuasive evidence of
                                                                                 prevalence and severity of asthma symptoms: phase three of the International
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        an association, let alone causation. Other studies have                  Study of Asthma and Allergies in Childhood (ISAAC). Thorax 2009;64(6):476-
                                                         ct e R




        implicated the importance of perinatal exposures; again,                 83. http://dx.doi.org/10.1136/ thx.2008.106609
        however, no consistent evidence for a causative mechanism has
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                                                                            7.   Litonjua AA, Gold DR. Asthma and obesity: common early-life influences in the
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        been forthcoming. Our analyses were based on an a priori                 inception of disease. J Allergy Clin Immunol 2008;121(5):1075-84; quiz 1085-
                                                                                 6. http://dx.doi.org/10.1016/j.jaci.2008.03.005
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        hypothesis, but we did check the association between asthma
                                                                            8.   Gilliland FD, Berhane K, Islam T, et al. Obesity and the Risk of Newly Diagnosed
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        symptom prevalence and sugar consumption measured over                   Asthma in School-age Children. Am J Epidemiol 2003;158(5):406-15.
        the same period. A lesser association was observed
                                                   i
                                                Pr




                                                                                 doi:10.1093/aje/kwg175
        (exponentiated beta coefficient 1.015; 95% CI 1.029 to 1.001;       9.   United Nations Food and Agriculture Organisation. FAOSTAT. 2009 [cited 2009
                                             ht




        P=0.038; Spearman’s correlation coefficient 0.24). This finding          4 November]; Available from: http://faostat.fao.org/site/291/default.aspx.
                                           ig




                                                                            10. R Development Core Team, R: A language and environment for statistical
        strengthens the argument that a latency period (birth to 6-7
                                       yr




                                                                                 computing. 2007, R Foundation for Statistical Computing: Vienna.
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        years-old chosen in this study) is necessary for sugar
                                                                            11. Laugesen M, Swinburn B. The New Zealand food supply and diet--trends 1961-
        consumption to influence asthma prevalence.
                                 C




                                                                                 95 and comparison with other OECD countries. Organisation for Economic Co-
            If our observed association is causal, and sugar consumption         operation and Development. N Z Med J 2000;113(1114):311-15.
        plays a role in the aetiology of asthma, we also expect that        12. Beasley R. The burden of asthma with specific reference to the United States. J
        limiting sugar consumption in people with established asthma             Allergy Clin Immunol 2002;109(5):S482-S489. http://dx.doi.org/10.1067/
                                                                                 mai.2002.122716
        may result in clinical benefit. To our knowledge, no randomised
                                                                            13. Tantisira KG, Weiss ST. Complex interactions in complex traits: obesity and
        controlled trials have been conducted to test such a hypothesis.         asthma. Thorax 2001;56(90002):ii64-74.
        One Singaporean observational study of mothers of children          14. Bianchini F, Kaaks R, Vainio H. Overweight, obesity, and cancer risk. The Lancet
        with asthma showed that five of the most commonly reported               Oncology 2002;3(9):565-74. http://dx.doi.org/10.1016/S1470-2045(02)00849-5
        food items thought to exacerbate the condition had high levels      15. Weiss ST, Shore S. Obesity and Asthma: Directions for Research. Am J Respir
                                                                                 Crit Care Med 2004;169(8):963-8. http://dx.doi.org/10.1164/rccm.200303-
        of added sugar, and the second most commonly reported food
                                                                                 403WS
        was “fizzy drinks”.16 Given that sugar (sucrose) has little
                                                                            16. Ang K, Foo S. Childhood asthma and dietary management among Singapore
        nutritional value, few adverse effects are likely to result from         parents. Nutrition & Food Science 2001;31(6):310-35.
        dietary advice to restrict sugar consumption in people with
        established asthma.

                                                    Available online at http://www.thepcrj.org


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Study of sugar consumption and asthma prevalence, by country

  • 1. 03-0024 Thornley 1/3/11 11:43 Page 1 Copyright PCRS-UK - reproduction prohibited Primary Care Respiratory Journal (2011); 20(1): 75-78 ORIGINAL RESEARCH Per capita sugar consumption is associated with severe childhood asthma: an ecological study of 53 countries *Simon Thornleya, Alistair Stewarta, Roger Marshalla, Rod Jacksona a Section of Epidemiology and Biostatistics, School of Population Health, Tamaki Campus, University of Auckland, Auckland, New Zealand Received 10th March 2010; revised 14th July 2010; accepted 18th September 2010; online 28th December 2010 Abstract Aims: To examine the ecological association between population asthma symptom prevalence in six to seven year-old children and per K U capita sugar consumption seven years earlier (during the perinatal period). y Methods: The asthma data (from the International Study of Asthma and Allergies in Childhood [ISAAC] study) were collected between et 1999 and 2004 from 53 countries, and per capita sugar consumption data (seven years before the asthma prevalence) were extracted from i oc United Nations Food and Agriculture (UNFAO) food balance sheets. Linear regression and Spearman’s rank coefficient were used to ite S evaluate the relationship between exposure and disease outcome. ib ory Results: Per capita sugar consumption varied more than six fold-between countries. A log-linear relationship was found between severe d oh at asthma symptoms (%) and per capita added sugar consumption in kg/capita/year (exponentiated beta coefficient 1.020; 95% CI 1.005 to pr ir 1.034; P = 0.012). Spearman’s rank correlation coefficient was 0.34 (P= 0.015), which indicates moderate correlation. n sp Conclusions: We have demonstrated an ecological association between sugar consumption during the perinatal period and subsequent io e ct e R risk of severe asthma symptoms in six and seven year-olds. © 2011 Primary Care Respiratory Society UK. All rights reserved. du ar S Thornley et al. Prim Care Respir J 2011; 20(1): 75-78 ro C doi:10.4104/pcrj.2010.00087 ep ry R ma Keywords asthma, aetiology, ISAAC data, sugar consumption, observational study, nutrition i Pr Introduction Childhood (ISAAC) has generated individual level information on ht asthma symptoms and putative exposures from 463,801 ig The global prevalence of both obesity and asthma has increased yr substantially in the last forty years.1 The co-occurrence of these children aged between 13 and 14 years and 257,800 children op two epidemics has led some investigators to propose that aged 6 and 7 in 58 countries.6 The authors reported considerable C nutritional factors responsible for obesity may also cause variation in the prevalence of asthma between countries asthma.2,3 The association between obesity and asthma at an (measured with a standardised definition), suggesting that individual level has been reported, and remains controversial.3 potentially avoidable causes may be present. Links between obesity and asthma have been drawn in both The importance of exposures during the perinatal period has children and adults and a number of hypotheses put forward to been highlighted for both obesity and asthma7,8 and several explain these links. reports have shown that rapid growth after birth is associated Recently, we proposed that increased refined carbohydrate with increased risk of asthma.7 We therefore linked UNFAO and intake may be responsible for increasing prevalence of obesity.4 ISAAC data from 53 countries to explore the possibility of an Ecological analyses of country-level per capita food association between added sugar consumption and asthma disappearance data on added sugar, from the routinely symptom prevalence, linking country-level data on severe published United Nations Food and Agriculture (UNFAO) Food asthma symptoms in children aged 6-7 years with per capita Balance Sheets, supports our hypothesis.5 added sugar consumption data in the same countries during the The International Study of Asthma and Allergies in children’s perinatal period, seven years earlier. * Corresponding author: Dr Simon Thornley, Section of Epidemiology and Biostatistics, Level 4, School of Population Health,Tamaki Campus, The University of Auckland, Private Bag 92019, Auckland 1151, New Zealand. Tel: +6493737599 ext 81971 E-mail: s.thornley@auckland.ac.nz PRIMARY CARE RESPIRATORY JOURNAL 75 www.thepcrj.org doi:10.4104/pcrj.2010.00087 http://www.thepcrj.org
  • 2. 03-0024 Thornley 1/3/11 11:43 Page 2 Copyright PCRS-UK - reproduction prohibited S Thornley et al. Methods sugar consumption is calculated by taking the difference of Outcome data – asthma symptom prevalence quantity of the sum of added sugar imported and produced The ISAAC study, Phase Three, generated asthma symptom from total added sugar exported or used for industry. The prevalence information at country level, drawn from surveys of quantity that remains has therefore ‘disappeared’ and is 6-7 and 13-14 year-old children, using a standardised assumed to have been consumed. Food balance sheet data, questionnaire, from 58 countries. A number of indicators of therefore, does not account for food either not consumed or asthma prevalence have been reported including current wasted. wheeze, parental- (6 to 7 year-olds) or self- (13 to 14 year-old) Data analysis reported asthma, and symptoms of severe asthma. We used the We linked the exposure and outcome data using linear 6-7 year-old age group with “symptoms of severe asthma” as regression and Spearman’s rank correlation coefficient. our measure of asthma prevalence because we believed that this Asthma symptom prevalence was log transformed to stabilise category would be most consistently reported between its variance. The R-project was used for all analyses. 10 countries and may be less subject to measurement error than the other reported measures of “current wheeze” and the question Results “has your child ever had asthma?”. We found estimates of severe asthma symptom prevalence for K Symptoms of severe asthma included respondents with 58 countries from ISAAC publications, but five of these countries U one or more of the following symptoms: did not appear in UNFAO food balance records, leaving 53 y et (1) > 4 attacks of wheeze in the last year, or, countries with paired data for analysis. Symptom prevalence i (2) > one or more nights per week sleep disturbance from ranged from 1.1% in Indonesia to 20.3% in Costa Rica. Sample oc sizes of surveys ranged from 1,181 (Bulgaria – one survey) to ite S wheeze in the last year, or, ib ory (3) wheeze affecting speech in the last year. 46,761 (India – pooled estimate). Severe asthma symptom prevalence was generally higher in English speaking and Latin d Published prevalence estimates for oh at pr ir these countries were derived from surveys n sp carried out between 1999 and 2004.6 Figure 1. Severe asthma symptom prevalence in 6 and 7 year-old children io e Although we have reported country plotted against average per capita added sugar consumption, 7 years ct e R estimates, these surveys were taken from prior, by country. Solid line shows log-linear regression line with dashed du ar specific localities within countries – and in lines illustrating 95% confidence intervals. ro C some cases, several regional study results ep 20 ry have been pooled to provide a total Costa Rica R ma country estimate. Cuba i Pr Exposure data – added sugar Severe asthma symptom prevalence (%) consumption ht ig We used the United Nations Food and yr Agricultural Organisation (UNFAO) food 15 op balance sheets9 to estimate per capita C Sri Lanka consumption of a variety of simple Venezuela Brazil carbohydrates. We used the UNFAO South Africa UK category “sugar and sweeteners” which Jordan New Zealand 10 Nicaragua includes a variety of monosaccharides and Panama Uruguay Australia disaccharides which mainly consist of Honduras sucrose (from sugar beet or cane), glucose, Nigeria Argentina Barbados Canada honey or high fructose corn syrup referred 5 El Salvador Poland Chile to here as “added sugar”. Such foods are Bulgaria Germany Ecuador 5 Vietnam Colombia Kyrgyzstan Thailand Pakistan Sweden high in fructose concentration, either free Iran Portugal Malta Japan Russia Ukraine or as part of a disaccharide (i.e. sucrose). Georgia Estonia Belgium Mexico India Croatia Italy Greece Syria This nutrient exposure information was Serbia and Montanegro Austria Korea Hungary Indonesia Albania Malaysia extracted from the period when the Lithuania mothers of the children surveyed for 10 20 30 40 50 60 asthma symptoms were most likely to be Added sugar consumption (kg/capita/year) pregnant (seven years before the asthma survey was undertaken). Per capita added PRIMARY CARE RESPIRATORY JOURNAL 76 www.thepcrj.org http://www.thepcrj.org
  • 3. 03-0024 Thornley 1/3/11 11:43 Page 3 Copyright PCRS-UK - reproduction prohibited Sugar consumption and childhood asthma American countries, with lower estimates in Asia, Eastern previously identified many causal associations. We have linked European and Mediterranean countries. Per capita added sugar an estimate of total per capita added sugar disappearance at a consumption recorded seven years before the asthma surveys country level to an estimate of asthma symptom prevalence varied more than six-fold, with lowest average consumption in from either one or an aggregation of regional population Vietnam (8.15 kg/capita/year in 1994) and highest in Costa Rica samples for a defined age group in these countries. We do not (58.95 kg/capita/year in 1995) and Cuba (58.23 kg/capita/year in know if the relative or total consumption of added sugar in 1995), two sugar exporting nations. The bivariate distribution of pregnant women is likely to be similar to the population the data is displayed in Figure 1. A log-linear relationship was average. The accuracy of food disappearance data to measure found between severe asthma symptoms (%) and per capita actual food intake is also unknown. Previous studies have sugar consumption in kg/capita/year (exponentiated beta focused on the use of this data to estimate average and relative coefficient 1.020; 95% CI 1.005 to 1.034; P=0.012 [estimate fat intakes.11 Another limitation of our analysis was the and 95% CI displayed in Figure 1]). The model indicates that exclusion of the United States (USA), which did not report centres with a further 35 kg/capita/year greater added sugar asthma symptom prevalence in this phase of the ISAAC study. disappearance have double the symptom prevalence compared If included, the USA had the highest per capita sugar to a country with lesser consumption. Although most countries consumption of any country in our cohort, with 66.4 K occupy the area within the bounds of uncertainty of the kg/capita/year consumed in 1994. In earlier phases of the U regression estimate, some outliers exist such as Nigeria and Sri ISAAC study, the USA prevalence of asthma in 13 to 14 year y et Lanka, with unexpectedly high prevalence given their average old children was about 20% or 8th out of 56 surveyed i sugar consumption. Conversely, Hungary, Austria and Malaysia countries, immediately below Brazil.12 If the USA had a similar oc have low rates of asthma at relatively high levels of sugar between-country rank for 6 to 7 year-old severe asthma ite S ib ory consumption. Plots of residual versus predicted values indicated symptoms, the inclusion of this data point would further acceptable model fit. When data from two high outliers (Costa strengthen the relationship we found between other countries. d oh at Rica and Cuba) were excluded, the magnitude of the A strength of this study lies in the use of the ISAAC study pr ir n sp exponentiated beta coefficient reduced to 1.013 (95% CI 0.998 information, which has provided the most comprehensive, io e to 1.028; P=0.104). standardised, between-country attempt to estimate global ct e R Our regression analysis implies directionality, so that average asthma prevalence in children to date. Also, the ubiquitous du ar between-country asthma symptom prevalence is estimated from nature of sweeteners in modern diets suggests that our study ro C observed values of added sugar consumption, which reflects our is less likely to suffer from confounding related directly or ep ry a priori belief that increased sugar consumption influences indirectly to food choices. Our sensitivity analysis, which R ma asthma symptom prevalence. Spearman’s rho rank correlation excluded two outliers, showed that a positive relationship was i coefficient, in contrast, is an unconditional measure of still observed between the variables, although the strength of Pr association, estimated at 0.34 (P= 0.015) – which indicates the association was diminished. ht moderate correlation between the two variables. Despite multiple possible sources of error, we have ig yr demonstrated a correlation between these two variables, op Discussion which is unlikely to be due to chance alone. These findings C Per capita added sugar consumption (an indirect indicator of were not part of a ‘data trawling’ exercise but represent the perinatal sugar exposure) estimated from FAO food balance first joint analyses of these datasets by the first author (ST), sheets, positively correlated with between-country level who is developing a research program on the relationship estimates of severe asthma symptom prevalence in 6 and 7 between refined carbohydrates and disease. Also, year-olds, measured seven years later. Of note, the two epidemiological evidence of rising sugar consumption,5 the countries with the highest recorded prevalence of severe rising prevalence of obesity,1 and the reported association asthma symptoms also had the highest average rate of sugar between asthma and obesity2 at an individual level make a consumption. This association explains the pattern of high plausible argument to link these disorders. rates of childhood asthma in English speaking and Latin Although these trends coincide, we can only speculate on a American countries. Also, the countries with the top five biological mechanism that may link sugar consumption and highest prevalence of severe asthma in this age group (Costa childhood asthma.5 The generally accepted co-occurrence of Rica, Cuba, Sri Lanka, Venzuela and Brazil) all have local sugar obesity and asthma is still poorly understood at a physiological manufacturing industries. level. Adipose tissue secretes hormones such as leptin, which Our analysis, like all ecological studies, is limited by the use induces satiety in the hypothalamus but also modulates the of aggregate data. These types of studies are prone to function of T-helper immune cells.13 Other disorders that are measurement error and confounding, but nevertheless have linked with the immunocompromised state – such as a range of PRIMARY CARE RESPIRATORY JOURNAL 77 www.thepcrj.org http://www.thepcrj.org
  • 4. 03-0024 Thornley 1/3/11 11:43 Page 4 Copyright PCRS-UK - reproduction prohibited S Thornley et al. Summary Although by no means confirmatory, this study raises the possibility of a link between increasing global sugar This study shows a moderate association between per capita consumption and asthma prevalence. Longitudinal studies – sugar consumption during the perinatal period and both observational and experimental – using individual level subsequent prevalence of severe childhood asthma information are needed to investigate further the strength of symptoms. This association explains the pattern of high rates this association. of childhood asthma in English speaking and Latin American Conflict of interest declarations countries. Cohort studies that collect detailed nutrient None. information, may further investigate the strength of this association. If sugar consumption is causally associated with Funding This work was funded by a salaried position at the University of Auckland the onset of childhood asthma, restricting intake of this substance is likely to improve symptoms and reduce References frequency of exacerbations in people with established 1. OECD, OECD Health Data 2009: Statistics and Indicators for 30 Countries. disease. 2009, OECD publishing: Paris. 2. Deane S, Thomson A. Obesity and the pulmonologist. Arch Dis Child 2006 K 91(2):188-91. http://dx.doi.org/10.1136/adc.2005.072223 U cancers – are also linked to obesity.14 However, the mechanism by 3. Ford ES. The epidemiology of obesity and asthma. Journal of Allergy and y Clinical Immunology 2005;115(5):897-909. http://dx.doi.org/10.1016/ which obesity and asthma are linked is yet to be determined.13,15 et j.jaci.2004.11.050 i To our knowledge, this is the only study so far to link sugar oc 4. Thornley S, McRobbie H, Eyles H, Walker N, Simmons G. The obesity epidemic: or fructose with asthma symptom prevalence. Although ite S is glycemic index the key to unlocking a hidden addiction? Medical Hypotheses previous studies have attempted to uncover a dietary link ib ory 2008;71(5):709-14. http://dx.doi.org/10.1016/j.mehy.2008.07.006 between childhood asthma and dietary factors, most studies 5. Popkin BM, SJ Nielsen. The sweetening of the world's diet. Obesity Research d oh at 2003;11(11):1325-32. http://dx.doi.org/10.1038/oby.2003.179 have focused on the role of different sub-types of fats, vitamins pr ir 6. Lai CK, Beasley R, Crane J, Foliaki S, Shah J, Weiland S. Global variation in the n sp or trace elements,13 none of which show persuasive evidence of prevalence and severity of asthma symptoms: phase three of the International io e an association, let alone causation. Other studies have Study of Asthma and Allergies in Childhood (ISAAC). Thorax 2009;64(6):476- ct e R implicated the importance of perinatal exposures; again, 83. http://dx.doi.org/10.1136/ thx.2008.106609 however, no consistent evidence for a causative mechanism has du ar 7. Litonjua AA, Gold DR. Asthma and obesity: common early-life influences in the ro C been forthcoming. Our analyses were based on an a priori inception of disease. J Allergy Clin Immunol 2008;121(5):1075-84; quiz 1085- 6. http://dx.doi.org/10.1016/j.jaci.2008.03.005 ep ry hypothesis, but we did check the association between asthma 8. Gilliland FD, Berhane K, Islam T, et al. Obesity and the Risk of Newly Diagnosed R ma symptom prevalence and sugar consumption measured over Asthma in School-age Children. Am J Epidemiol 2003;158(5):406-15. the same period. A lesser association was observed i Pr doi:10.1093/aje/kwg175 (exponentiated beta coefficient 1.015; 95% CI 1.029 to 1.001; 9. United Nations Food and Agriculture Organisation. FAOSTAT. 2009 [cited 2009 ht P=0.038; Spearman’s correlation coefficient 0.24). This finding 4 November]; Available from: http://faostat.fao.org/site/291/default.aspx. ig 10. R Development Core Team, R: A language and environment for statistical strengthens the argument that a latency period (birth to 6-7 yr computing. 2007, R Foundation for Statistical Computing: Vienna. op years-old chosen in this study) is necessary for sugar 11. Laugesen M, Swinburn B. The New Zealand food supply and diet--trends 1961- consumption to influence asthma prevalence. C 95 and comparison with other OECD countries. Organisation for Economic Co- If our observed association is causal, and sugar consumption operation and Development. N Z Med J 2000;113(1114):311-15. plays a role in the aetiology of asthma, we also expect that 12. Beasley R. The burden of asthma with specific reference to the United States. J limiting sugar consumption in people with established asthma Allergy Clin Immunol 2002;109(5):S482-S489. http://dx.doi.org/10.1067/ mai.2002.122716 may result in clinical benefit. To our knowledge, no randomised 13. Tantisira KG, Weiss ST. Complex interactions in complex traits: obesity and controlled trials have been conducted to test such a hypothesis. asthma. Thorax 2001;56(90002):ii64-74. One Singaporean observational study of mothers of children 14. Bianchini F, Kaaks R, Vainio H. Overweight, obesity, and cancer risk. The Lancet with asthma showed that five of the most commonly reported Oncology 2002;3(9):565-74. http://dx.doi.org/10.1016/S1470-2045(02)00849-5 food items thought to exacerbate the condition had high levels 15. Weiss ST, Shore S. Obesity and Asthma: Directions for Research. Am J Respir Crit Care Med 2004;169(8):963-8. http://dx.doi.org/10.1164/rccm.200303- of added sugar, and the second most commonly reported food 403WS was “fizzy drinks”.16 Given that sugar (sucrose) has little 16. Ang K, Foo S. Childhood asthma and dietary management among Singapore nutritional value, few adverse effects are likely to result from parents. Nutrition & Food Science 2001;31(6):310-35. dietary advice to restrict sugar consumption in people with established asthma. Available online at http://www.thepcrj.org PRIMARY CARE RESPIRATORY JOURNAL 78 www.thepcrj.org http://www.thepcrj.org