HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS		QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via ISI Web of Science (55) Citing Articles via Google Scholar Google Scholar Articles by Ellwood, P. Articles by Robertson, C.F Search for Related Content PubMed PubMed Citation Articles by Ellwood, P. Articles by Robertson, C.F

Diet and asthma, allergic rhinoconjunctivitis and atopic eczema symptom prevalence: an ecological analysis of the International Study of Asthma and Allergies in Childhood (ISAAC) data

¹ Dept of Paediatrics, Faculty of Medical and Health Sciences, University of Auckland, Auckland, New Zealand, ² Centre for Allergy Research, Karolinska Institute, Nobels väg 5, Stockholm, Sweden, ³ University of Wales College of Medicine, Temple of Peace and Health, Cathays Park, Cardiff, UK, ⁴ Centre for Public Health Research, Massey University, Wellington Campus, Wellington, New Zealand and ⁵ Dept of Respiratory Medicine, Royal Children's Hospital, Flemington Rd, Parkville, Victoria, Australia

CORRESPONDENCE: Philippa Ellwood, ISAAC International Data Centre, Dept of Paediatrics, Faculty of Medical and Health Science, University of Auckland, Private Bag 92019, Auckland, New Zealand. Fax: 64 9 3737602

Keywords: allergic rhinoconjunctivitis, asthma, atopic eczema, children, diet, ISAAC

Received: September 28, 1999
Accepted November 13, 2000

This work was supported by the Health Research Council of New Zealand, the Asthma and Respiratory Foundation of New Zealand, the National Child Health Research Foundation, the Hawke's Bay Medical Research Foundation, the Waikato Medical Research Foundation, GlaxoWellcome New Zealand and Astra New Zealand, as well as GlaxoWellcome International Medical Affairs for funding the regional coordination centres. The Wellington Asthma Research Group is supported by a Programme Grant from the Health Research Council of New Zealand.

	Abstract

TOP Abstract Methods Results Discussion Acknowledgements References

 
Several studies have suggested that the increasing prevalence of symptoms of asthma, rhinitis and eczema, could be associated with dietary factors. In the present paper, a global analysis of prevalence rates of wheeze, allergic rhinoconjunctivitis and atopic eczema was performed in relation to diet, as defined by national food intake data.

Analyses were based on the International Study of Asthma and Allergies in Childhood (ISAAC) data for 6–7 and 13–14 yr old children. Symptoms of wheeze, allergic rhinoconjunctivitis and atopic eczema symptom prevalence were regressed against per capita food intake, and adjusted for gross national product to account for economic development. Dietary data were based on 1995 Food and Agriculture Organisation of the United Nations data for 53 of the 56 countries that took part in ISAAC phase I (1994/1995).

The 13–14 year age group showed a consistent pattern of decreases in symptoms of wheeze (current and severe), allergic rhinoconjunctivitis and atopic eczema, associated with increased per capita consumption of calories from cereal and rice, protein from cereals and nuts, starch, as well as vegetables and vegetable nutrients. The video questionnaire data for 13–14 yr olds and the ISAAC data for 6–7 yr olds showed similar patterns for these foods.

A consistent inverse relationship was seen between prevalence rates of the three conditions and the intake of starch, cereals, and vegetables. If these findings could be generalised, and if the average daily consumption of these foods increased, it is speculated that an important decrease in symptom prevalence may be achieved.

The incidence of many noncommunicable diseases (NCDs) throughout the world, has been linked to diet 1, and there is a need for standardised multi-country studies of nutrition and disease 2. Many nutritional factors may influence disease, including changes to the production and availability of food, changing food preferences, increased supply of processed foods for consumption as well as supplies for food aid, use of fertilisers and pesticides, land availability, increased prices of staple foods, urbanisation, migration, economic factors and market fluctuations 3–6. Traditional nutritional patterns and patterns of health are changing as are other aspects of lifestyles of populations. Over the past few decades, "Westernization" has seen many countries moving away from the traditional diet of locally grown foods to a more western diet 4. In some countries, these patterns have been shown to be linked to the increase of NCDs 5–7 including obesity, cardiovascular diseases and some cancers 1, 6, 8. Others have reported a lower incidence of chronic disease to be associated with the consumption of a more traditional form of diet 9–12.

Asthma, a chronic respiratory disease, is classified as an NCD but there has been little study of its relationship to dietary factors. Recent hypotheses have focused on potential relationships between food content and the airway inflammatory response 13, 14. Decreased consumption of fruit and vegetables in the United Kingdom has been postulated to be associated with an increase in prevalence of asthma and rhinitis through their antioxidant properties, which may protect against inflammation 13, 15. Similarly, increased consumption of linoleic acid, found in polyunsaturated fatty acids (PUFAs), is thought to be linked to asthma, eczema and allergic rhinitis 12, 16. It is postulated that an increase in consumption of linoleic acid leads to an increase in the synthesis of prostaglandin-E₂ (PGE₂), resulting in allergic sensitisation 14. More recently, a European investigation indicated an association between trans-fatty acids and the prevalence of childhood asthma, rhinitis and eczema 17. Oily fish consumption has been associated with reduced risk of children having asthma and previous studies postulated that increased consumption of oily fish, rich in omega-3 fatty acids, reduces the synthesis of proinflammatory cytokines 18. Migration and food aid (including processed food) have been associated with the rapid increase in asthma prevalence, suggesting a potent environmental factor 6, 19, 20. Thus, in seeking explanations for the large world-wide variations in the prevalence of asthma, rhinitis and eczema, and the increases within populations over the last few decades, dietary factors are a potentially important field for study. The findings of an ecological analysis of the relationship between per capita food intake and the prevalence of symptoms of asthma, allergic rhinoconjunctivitis and atopic eczema are reported here.

	Methods

TOP Abstract Methods Results Discussion Acknowledgements References

 
Sources of data
Symptom prevalence data
The International Study of Asthma and Allergies in Childhood (ISAAC) programme 21, has reported major world-wide variation in the prevalence of symptoms of asthma, allergic rhinoconjunctivitis and atopic eczema 22–25. The methods have been described in detail elsewhere 21 and they are mentioned only briefly here. ISAAC Phase One studied a total of 721,601 children of two age groups (6–7 and 13–14 yr olds) from 156 collaborating centres in 56 countries. Each centre was responsible for obtaining its own funding and obtained the necessary approval from an ethics committee before the start of the study. Three one-page core questionnaires on asthma, rhinitis and eczema symptoms for both age groups were used and an asthma symptoms video questionnaire used for the older age group. The basic question used for assessing asthma symptom prevalence was "Have you had wheezing or whistling in the chest in the last 12 months?" (current wheeze). The prevalence of asthma severity was assessed by using the question "In the last 12 months, how often, on average has your sleep been disturbed due to wheezing?" and identifying respondents who reported such sleep disturbance "one or more nights per week". The allergic rhinoconjunctivitis prevalence analyses were based on positive answers to two questions; "In the past 12 months have you had a problem with sneezing or a runny or blocked nose when you DID NOT have a cold or the flu?" If yes: "In the past 12 months has this nose problem been accompanied by itchy watery eyes?" The atopic eczema prevalence analyses used positive answers to three questions relating to an itchy rash: "Have you ever had an itchy rash which was coming and going for at least six months?" If yes: "Have you had this itchy rash at any time in the last 12 months?" If yes: "Has this itchy rash at any time affected any of the following places: the folds of the elbows, behind the knees, in front of the ankles, under the buttocks, or around the neck, ears, or eyes?" The older age group self completed the questions and also answered a video questionnaire, for which the first scene, wheezing at rest, was used for analysis. Questions for the younger age group were reworded accordingly and answered by the parent/guardian of the child.

Food Balance Sheets
We used the 1995 food balance sheet and food supply data, from the Food and Agriculture Organisation (FAOSTAT) website 26 to obtain comparative figures of food and nutrient intake among the large number of countries who took part in ISAAC Phase One. FAOSTAT data was obtained for 53 out of the 56 ISAAC countries (all except Oman, Singapore and Taiwan). FAOSTAT data describe amounts of food produced per country, and amounts exported and imported, but wastage is not accounted for. Food consumption per capita is calculated as the sum of food production and food imports, minus food exports, divided by the population, and the resulting food balance sheets subjected to rigorous internal and external consistency checks 26. This information was analysed using an international Food and Nutrient database (www.healthnz.co.nz) which estimated per capita consumption of macro nutrients and micro nutrients in appropriate units or as a percentage of total energy consumption (%TEC) corrected for edibility obtained from food composition tables 27, 28.

Data analysis
The data for the three conditions and dietary variables were entered onto a computer and analysed using PC SAS (SAS Institute, Cary, NC, USA). Analyses of dietary variables were performed both by units of kg and by %TEC. The results given are for %TEC unless otherwise stated, to enable a focus on dietary patterns rather than total food intake (which may be more prone to inaccuracies due to wastage or miss reporting). Mixed model regression analyses were carried out to incorporate the different structure of each of the data sets, with FAOSTAT data representing whole countries and ISAAC data using centres within countries. All analyses were repeated with gross national product (GNP) in the model to account for the level of economic development of countries, a factor related to symptom prevalence 29. The analysis did not examine combinations and interactions of the diet variables.

	Results

TOP Abstract Methods Results Discussion Acknowledgements References

 
There were 53 countries with both FAOSTAT and ISAAC data with a wide range of per capita food supply. TEC (expressed as kilocalorie (kCal) for consistency with the data obtained from FAOSTAT) ranged from 1602–4013 kCal·day^–1; protein 48–119 g·day^–1 (5–14%TEC); carbohydrate from 311–587 g·day^–1 (42–74%TEC) and fat 24–181 g·day^–1 (13–43%TEC). Table 1 shows these and the range of other dietary variables.

View larger version (15K): [in this window] [in a new window]   Fig. 1.— Ranked consumption of calories from cereal and rice in percentage of total energy consumption (%TEC) by country.

View larger version (22K): [in this window] [in a new window]   Fig. 2.— Current wheeze (%) against consumption of calories from cereal and rice (%TEC), 13–14 yr data. Each point represents a country, averaged from centre data.

There was no association between total monounsaturated fatty acid (MUFA) and polyunsaturated fatty acid (PUFA) intake %TEC, as well as MUFA and PUFA from vegetable oils and animals, for current wheeze, severe wheeze, allergic rhinoconjunctivitis and atopic eczema. However, significant negative associations were seen between MUFA from vegetables and current wheeze, atopic eczema and PUFA from vegetables and current wheeze, allergic rhinoconjunctivitis and atopic eczema (GNP adjusted).

For oils, olive oil (g) showed a negative association with current wheeze, severe wheeze and allergic rhinoconjunctivitis, becoming significantly negative with atopic eczema. Soya oil (g) was positively associated with all three conditions and significantly positive with severe wheeze.

The video questionnaire showed generally the same pattern of associations as for current wheeze. Although most were insignificant, significant negative associations were seen with starch and protein from cereals and nuts. For example, a 50 g increase in starch was associated with a 1.4% (1.6% unadjusted for GNP) decrease in symptoms from the video questionnaire.

The 6–7 yr age group (data not shown), showed the same pattern as for the 13–14 yr age group data. Significant negative associations were seen between starch (g) and current wheeze and atopic eczema; calories from cereal and rice (%TEC) and current wheeze and severe wheeze; as well as significant negative associations between fat (g), vitamin E from vegetables (mg), PUFA (%TEC); olive oil (g); oleic fat (%TEC); total fibre (g) and atopic eczema. For example a 10%TEC increase of calories from cereals and rice was associated with a 2.8% decrease in current wheeze and a 50 g increase of starch with a 2.7% decrease. A significant positive association was seen between soya oil and current wheeze and severe wheeze (GNP adjusted).

	Discussion

TOP Abstract Methods Results Discussion Acknowledgements References

 
This world wide analysis of food intake and symptoms of asthma, allergic rhinoconjunctivitis and atopic eczema has shown, for the 13–14 yr age group, a consistent negative association between all three atopic conditions and kCals, protein, vegetables and specific vegetable nutrients (vitamin A, Vitamin E, protein, MUFA, PUFA and saturated fats), starch, calories from cereal and rice, total fibre, protein from cereals and nuts, total seafood, all fish (fresh and frozen) and olive oil. There were no consistent associations for other foods. The video questionnaire results showed similar, but weaker, associations with the diet variables. For the 6–7 yr age group the negative and positive associations generally remained as for the older age group, but were also weaker. This may indicate that the diet of 13–14 year old children is more accurately reflected in the average per capita per day intake of food and may account for the stronger associations seen for the older age group.

The analysis used reliable data from standardised sources (ISAAC and FAOSTAT). FAOSTAT data must be interpreted with care, however, as its accuracy depends on the reliability of the underlying statistics of population, supply and utilisation of foods and of their nutritive value. Food balance data provide direct information about the availability of foods, but only indirect information about dietary intake. Furthermore, FAOSTAT is at times, updated retrospectively when more reliable information becomes available. An example would be 1995 census data for a country becoming available in 1999, allowing legitimate changes to the data (already submitted) to be made, or perhaps food groups being separated as more accurate country data becomes available. The associations seen therefore may change slightly once the FAOSTAT data is updated.

The limitations of ecological analyses are well known 30. In particular, an association at the country level may be due to complex biases and may not apply at the individual level, since dietary variations between countries are likely to reflect broader cultural and environmental differences and may not be directly causal. Nevertheless, an ecological approach has certain advantages in examining possible relationships between diet and disease. In so far as diet varies more widely between countries than within them, associations may be detectable when comparisons are made between different countries that would not be evident within any one country 31. Ecological studies also avoid the regression dilution bias that arises in studies of individuals whose diet varies over time.

There was a large between country variability within some food groups, as shown in table 1, illustrating the minimum and maximum range of country food supply per capita per day. There was over a 1500 fold difference between the two countries at the extreme for olive oil consumption, a 25 fold difference for the two countries at the extremes for vegetable consumption and nearly a 3 fold difference for the two countries at the extremes for calories from cereal and rice. The between country variability of calories from cereal and rice, as illustrated in figure 1, shows the country with the lowest consumption (Germany, 21%TEC) to the country with the highest consumption (Ethiopia 72%TEC). Although the country range is relatively small, the analysis showed a significant negative association with current and severe wheeze, allergic rhinoconjunctivitis and atopic eczema.

It is striking that when adjusted for GNP, the negative association of total calories, protein, vegetables, vegetable fats and vegetable micronutrients, starch, total fibre, calories from cereal and rice, protein from cereals and nuts, total seafood, all fish and olive oil was consistent for symptoms of all three conditions, asthma, allergic rhinoconjunctivitis and atopic eczema. There was no consistent pattern for any other food category, so it seems unlikely that these findings simply reflect systematic bias or confounding by other unknown dietary factors. Do these foods have a protective effect in the expression of symptoms of these conditions? A possibility for the association seen between vegetables and vegetable micronutrients is that this could be due to their antioxidant effects. In particular, Vitamins A and E are known antioxidants that are essential in the lung defence mechanisms against reactive oxidant propagation, inhibitor of oxidant propagation and scavenging of hydroxyl radicals and singlet oxygen 13. These antioxidant defences may be important in reducing airway inflammation and lung permeability in response to cigarette smoke, air pollutants and ozone 13, and may also prove to be important in allergic rhinoconjunctivitis and atopic eczema. Although vitamin C may have similar properties 32, no consistent association was found in this analysis. However, it would be premature to focus on specific micronutrients at this stage. By analogy, there is clear evidence that vegetable consumption is a negatively associated cancer risk, but interventions based on specific micronutrient supplementation have been ineffective 33. Thus, other potential mechanisms for a possible protective effect of vegetables also deserve attention. One such possibility is indicated by differences in the intestinal microflora between countries with a high and low prevalence of allergies 34 and between allergic and nonallergic children 35.

Of interest is the strong negative association between calories from cereal and rice and protein from cereal and nuts and the three atopic conditions. Throughout human development dietary patterns have evolved and now vary greatly in different parts of the world. The diet of economically developed countries and urban areas of the developing world are now relatively low in cereals, tubers and other starchy foods and relatively high in sugar, fat, protein of animal origin, salt, meat, dairy produce and alcohol. Plant based carbohydrate-rich diets have been associated with lower rates of other NLDs 9, 10, 11, 33, 36 and it is of interest that this association has been found for asthma, allergic rhinoconjunctivitis and atopic eczema. Although it is speculated that antioxidants contained in cereal, rice and vegetables may be a reason for this protective effect, other mechanisms need to be explored.

Recent exploration of PUFA and the potential for promoting allergic sensitisation and asthma 14, 16, 37, found a positive relationship. The present analysis saw a significant association between vegetable derived PUFA and decreased symptom prevalence of the three conditions, as well as vegetable derived MUFA and decreased symptom prevalence of current wheeze and atopic eczema. Similarly, a relationship between the consumption of oily fish and asthma symptoms in children 18, and fish intake and lung function 38 have been observed, although clinical studies (of fish oil supplements) have not shown the expected benefits on airway functioning [39, 40]. The present analysis showed a consistent negative association between total seafood and all fish (fresh and frozen) and the three conditions, although insignificant except for severe wheeze.

In summary, the consistent findings of a negative association between starch, calories from cereals and rice, protein from cereals and nuts and vegetables and symptoms of asthma, allergic rhinoconjunctivitis and atopic eczema, especially in the older age group, warrants further exploration. Antioxidant effects may be important, although other explanations, such as effects on the intestinal microflora, should also be explored. There has been little exploration of the association between starchy foods and these conditions and although it is generally acknowledged that a diet containing large amounts of fruit and vegetables is associated with improved health, the association with cereal should be explored further. From this analysis, it is speculated that, if the daily per capita amount of calories from cereal and rice consumed were to be increased by 10% of total energy consumption, it may be possible to achieve a 3.2% decrease in the prevalence of current wheeze, a 0.4% decrease in severe wheeze, a 2.4% decrease in allergic rhinoconjunctivitis and a 0.6% decrease in atopic eczema. The relationship seen between the intake of cereals, starch and vegetables and symptom prevalence of asthma, allergic rhinoconjunctivitis and atopic eczema is strong enough to be explored further in strategies for prevention of these conditions. However it is likely that other nondietary factors are also of importance.

	Acknowledgements

TOP Abstract Methods Results Discussion Acknowledgements References

 
The writing committee consisted of P.E. Ellwood, M.I. Asher, B. Björkstén, M.L. Burr, N. Pearce and C.F. Robertson. The ISAAC Steering Committee consisted of, N. Aït-Khaled, G. Anabwani, H.R. Anderson, M.I. Asher (Chair), R. Beasley (Coordinator Phase One and Phase Three), B. Björkstén, M.L. Burr, J. Crane, U. Keil, C.K.W. Lai, J. Mallol, F.C. Martinez, E.A. Mitchell, S. Montefort, N. Pearce, C.F. Robertson, J.R. Shah, A.W. Stewart, D.P. Strachan, E. von Mutius, S.K. Weiland (Coordinator Phase Two), and H.C. Williams. The ISAAC International Data Centre consists of M.I. Asher (Director), T.O. Clayton, P. Ellwood, E.A. Mitchell and A.W. Stewart.

The collaborators in the participating centres, all parents, children, teachers and other staff as well as the many field workers, who participated in the surveys and data collection have contributed enormously to the success of ISAAC. The authors would particularly like to thank them. The authors also wish to thank the many funding agencies that have supported ISAAC, especially the funding bodies who supported the ISAAC International Data Centre. Our grateful thanks to R. Akroyd, Paediatric Dietitian, Starship Children's Hospital, Auckland, New Zealand, for her dietary assistance, to Dr Murray Laugesen, Waiheke Island, New Zealand, who supplied the database for the analysis and to T. Clayton from the ISAAC International Data Centre for his statistical assistance.

	References

TOP Abstract Methods Results Discussion Acknowledgements References

 

1. The WHO MONICA Project. Geographical variation in the major risk factors of coronary heart disease in men and women aged 35–64 years. In: Non-communicable diseases: a global problem. Wld hlth statist quart 1988; 41: 115–40.
2. WHO study group. Diet, nutrition, and the prevention of chronic diseases. WHO Technical Report Series. 1990; 797.
3. Pearce NMatos EVainio HBoffetta PKogevinas M(eds). Occupational cancer in developing countries 1994; IARC Scientific Publications No. 129. Lyon; pp 78.
4. Posner BM, Franz M, Quatromoni P, the INTERHEALTH Steering Committee. Special Article. Nutrition and the Global Risk for Chronic Diseases: The INTERHEALTH Nutrition Initiative. Nutr Rev 1994;52:No 6201–207.[ISI][Medline] [Order article via Infotrieve]
5. Bloom A. Health and Nutrition in the Pacific: Problems and policy issues. In: Human Resources Development in the Pacific. CD Throsby editor . Pacific Policy Paper No.3; pp. 53–85.
6. Schoeffel P. Food, Health and development in the Pacific Islands: Policy Implication for Micronesia. ISLA: J Micronesian Studies. 1:2 Dry Season, 1992; 223–50.
7. Finau S, Prior I, Maddill J. Food consumption patterns among urban and rural Tongans. J Food and Nutr. 1986; 43 2:78–84.
8. Berkowitz RI. Obesity in Childhood and Adolescence. In: Walker WA and Watkins JB editors. Nutrition in Paediatrics. Basic Science and Clinical Applications. 2nd Edn. London BC Decker. 1997; pp. 716–723.
9. Helsing E. Traditional diets and disease patterns of the Mediterranean, circa 1960. Am J Clin Nutr 1995;61:Suppl. 13, 29S–37S.
10. Kimura N. Changing patterns of coronary heart disease, stroke and nutrient intake in Japan. Prev Med 1983;12:222–227.[CrossRef][ISI][Medline] [Order article via Infotrieve]
11. Marchand L, Hankin J, Bach F, et al. An ecological study of diet and lung cancer in the south pactfic. Int J Cancer 1995;62:1–6.[ISI][Medline] [Order article via Infotrieve]
12. Chang CC, Phinney SD, Halpern GM, Gershwin ME. Asthma Mortality: Another Opinion-Is It a Matter of Life and ...Bread? JAsthma 1993;30:93–103.
13. Seaton A, Godden DJ, Brown K. Increase in asthma: a more toxic environment or a more susceptible population? Thorax 1994;49:171–174.[ISI][Medline] [Order article via Infotrieve]
14. Black PN, Sharpe S. Dietary fat and asthma: is there a connection? Eur Respir J 1997;10:6–12.[Abstract]
15. Bodner C, Godden D, Brown K, Little J, Ross S, Seaton A, on behalf of Aberdeen WHEASE Study Group. Antioxidant intake and Adult onset wheeze - a case control study. Eur Respir J 1999;13:22–30.[Abstract]
16. von Mutius E, Weiland SK, Fritzsch C, Duhme H, Keil U. Increasing prevalence of hay fever and atopy among children in Leipzig, East Germany. Lancet 1998;351:862–866.[CrossRef][ISI][Medline] [Order article via Infotrieve]
17. Weiland S, von Mutius E, Hüsing A, Asher MI, onbehalf of the ISAAC Steering Committee. Intake oftrans fatty acids and prevalence of childhood asthma and allergies in Europe. Lancet 1999;353:2040–2041.[CrossRef][ISI][Medline] [Order article via Infotrieve]
18. Hodge L, Salome CM, Peat JK, Haby MM, Xuan W, Woolcock AJ. Consumption of oily fish and childhood asthma risk. Med J Aust 1996;164:137–140.[ISI][Medline] [Order article via Infotrieve]
19. Prior IAM, Stanhope JM, Grimley Evans J, Salmond CE. The Tokelau Island Migrant Study. Int J Epidemiol 1974;3:225–232.[Abstract/Free Full Text]
20. Leung RC, Carlin JB, Burdon JGW, Czarny D. Asthma, allergy and atopy in Asian immigrants in Melbourne. Med J Aust 1994;161:418–425.[ISI][Medline] [Order article via Infotrieve]
21. Asher MI, Keil U, Anderson HR, et al. International Study of Asthma and Allergies in Childhood (ISAAC): rationale and methods. Eur Respir J 1995;8:483–491.[Abstract]
22. The International Study of Asthma and Allergies in Childhood (ISAAC) Steering Committee. Worldwide variations in the prevalence of asthma symptoms: theInternational Study of Asthma and Allergies inChildhood (ISAAC). Eur Respir J 1998;12:315–335.[Abstract]
23. The International Study of Asthma Allergies in Childhood (ISAAC) Steering Committee. Worldwide variation in prevalence of symptoms of asthma, allergic rhinoconjunctivitis, and atopic eczema: ISAAC. Lancet 1998;351:1225–1232.[CrossRef][ISI][Medline] [Order article via Infotrieve]
24. Strachan DP, Sibbald B, Weiland SK, et al. Worldwide variations in prevalence of symptoms of allergic rhinoconjunctivitis in children: the International study of Asthma and Allergies in Childhood (ISAAC). Pediatr Allergy Immunol 1997;8:161–176.[ISI][Medline] [Order article via Infotrieve]
25. Williams H, Robertson C, Stewart A, et al. Worldwide variations in the prevalence of symptoms of atopic eczema in the international study of asthma and allergies in childhood. J Allergy Clin Immunol 1999;103:125–38.[CrossRef][ISI][Medline] [Order article via Infotrieve]
26. FAO. Food balance sheets. www.fao.org/: Food and Agricultural Organization, 1998.
27. McCance RA, Widdowson EM, Holland B. McCance and Widdowson's. The composition of Foods. 5th Edn. London: Royal Society of Chemistry and Ministry of Agriculture, Fisheries and Foods. 1991.
28. Paul A, Southgate D. The Composition of Foods. 4th ed. London: Royal Society of Chemistry and Ministry of Agriculture Food and Fisheries HMSO, 1978; P 31.
29. Stewart AW, Mitchell EA, Pearce N, Strachan DP, Weiland SK, on behalf of the ISAAC Steering Committee. The relationship of per capita gross national product to the prevalence of symptoms of asthma and other atopic diseases in children: the International Study of Asthma and Allergies in Childhood (ISAAC). Int J Epidemiol 2001;;30:173–179.
30. Greenland S, Morgenstern H. Ecological bias, confounding and effect modification. Int J Epid 1989;18:269–274.[Abstract/Free Full Text]
31. Rose G. The strategy of preventive medicine. Oxford. Oxford University Press, 1992; p 53–63.
32. Hatch GE. Asthma, inhaled oxidants, and dietary antioxidants. Am J Clin Nutr 1995;61:Suppl. 6, 25S–30S.
33. Willett W, Colditz G. Vitamin A and lung cancer. In Willet W, editor. Nutritional Epidemiology. 2nd ed. New York: Oxford University Press, 1998; pp 357–376.
34. Sepp E, Julge K, Vasar M, Naaber P, Björkstén B, Mikelsaar M. Intestinal microflora of Estonian and Swedish infants. Acta Paediatr 1997;86:956–961.[ISI][Medline] [Order article via Infotrieve]
35. Björkstén B, Naaber P, Sepp E, Mikelsaar M. The intestinal microflora in allergic Estonian and Swedish 2-year old children. Clin Exp Allergy 1999;29:342–346.[CrossRef][ISI][Medline] [Order article via Infotrieve]
36. Slavin J, Jacobs D, Marquart L. Whole-Grain Consumption and Chronic Disease: Protective Mechanisms. Nutr Cancer 1997;27:14–21.[ISI][Medline] [Order article via Infotrieve]
37. Black PN. The prevalence of allergic disease and Linoleic acid in the diet. J Allergy Clin Immunol 1999;103:351–2.[CrossRef][ISI][Medline] [Order article via Infotrieve]
38. Hodge L, Salome CM, Hughes JM, et al. Effect of dietary intake of omega-3 and omega-6 fatty acids on severity of asthma in children. Eur Respir J 1998;11:361–365.[Abstract]
39. Schwartz J, Weiss ST. The relationship of dietary fish intake to level of pulmonary function in the first National Health and Nutrition Survey (NHANES 1). Eur Respir J 1994;7:1821–1824.[Abstract]
40. Monteleone CA, Sherman AR. Nutrition and Asthma. Review article. Arch Intern Med 1997;157:23–34.[Abstract]

This article has been cited by other articles:

				N. Pearce, N. Ait-Khaled, R. Beasley, J. Mallol, U. Keil, E. Mitchell, C. Robertson, and and the ISAAC Phase Three Study Group Worldwide trends in the prevalence of asthma symptoms: phase III of the International Study of Asthma and Allergies in Childhood (ISAAC) Thorax, September 1, 2007; 62(9): 758 - 766. [Abstract] [Full Text] [PDF]

				L. Garcia-Marcos, I. M. Canflanca, J. B. Garrido, A. L.-S. Varela, G. Garcia-Hernandez, F. G. Grima, C. Gonzalez-Diaz, I. Carvajal-Uruena, A. Arnedo-Pena, R. M Busquets-Monge, et al. Relationship of asthma and rhinoconjunctivitis with obesity, exercise and Mediterranean diet in Spanish schoolchildren Thorax, June 1, 2007; 62(6): 503 - 508. [Abstract] [Full Text] [PDF]

				C Tabak, A H Wijga, G de Meer, N A H Janssen, B Brunekreef, and H A Smit Diet and asthma in Dutch school children (ISAAC-2) Thorax, December 1, 2006; 61(12): 1048 - 1053. [Abstract] [Full Text] [PDF]

				W. Eder, M. J. Ege, and E. von Mutius The asthma epidemic. N. Engl. J. Med., November 23, 2006; 355(21): 2226 - 2235. [Full Text] [PDF]

				B D Patel, A A Welch, S A Bingham, R N Luben, N E Day, K-T Khaw, D A Lomas, and N J Wareham Dietary antioxidants and asthma in adults Thorax, May 1, 2006; 61(5): 388 - 393. [Abstract] [Full Text] [PDF]

				L. G. Wood, M. L. Garg, R. J. Blake, S. Garcia-Caraballo, and P. G. Gibson Airway and Circulating Levels of Carotenoids in Asthma and Healthy Controls J. Am. Coll. Nutr., December 1, 2005; 24(6): 448 - 455. [Abstract] [Full Text] [PDF]

				S. Foliaki, S. K. Nielsen, B. Bjorksten, E. von Mutius, S. Cheng, N. Pearce, and the ISAAC Phase I Study Group Antibiotic sales and the prevalence of symptoms of asthma, rhinitis, and eczema: The International Study of Asthma and Allergies in Childhood (ISAAC) Int. J. Epidemiol., June 1, 2004; 33(3): 558 - 563. [Abstract] [Full Text] [PDF]

				R. N. Rubin, L. Navon, and P. A. Cassano Relationship of Serum Antioxidants to Asthma Prevalence in Youth Am. J. Respir. Crit. Care Med., February 1, 2004; 169(3): 393 - 398. [Abstract] [Full Text] [PDF]

				S. Farchi, F. Forastiere, N. Agabiti, G. Corbo, R. Pistelli, C. Fortes, V. Dell'Orco, and C.A. Perucci Dietary factors associated with wheezing and allergic rhinitis in children Eur. Respir. J., November 1, 2003; 22(5): 772 - 780. [Abstract] [Full Text] [PDF]

				R. da Costa Lima, C. G. Victora, A. M. B. Menezes, and F. C. Barros Do Risk Factors for Childhood Infections and Malnutrition Protect Against Asthma? A Study of Brazilian Male Adolescents Am J Public Health, November 1, 2003; 93(11): 1858 - 1864. [Abstract] [Full Text] [PDF]

				W. Phipatanakul Diet and Asthma, Allergic Rhinoconjunctivitis and Atopic Eczema Symptom Prevalence: An Ecological Analysis of the International Study of Asthma and Allergies in Childhood (ISAAC) Data Pediatrics, August 1, 2002; 110(2): 431 - 432. [Full Text] [PDF]

				S. O. SHAHEEN, J. A. C. STERNE, R. L. THOMPSON, C. E. SONGHURST, B. M. MARGETTS, and P. G. J. BURNEY Dietary Antioxidants and Asthma in Adults . Population-based Case-Control Study Am. J. Respir. Crit. Care Med., November 15, 2001; 164(10): 1823 - 1828. [Abstract] [Full Text] [PDF]

This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via ISI Web of Science (55) Citing Articles via Google Scholar Google Scholar Articles by Ellwood, P. Articles by Robertson, C.F Search for Related Content PubMed PubMed Citation Articles by Ellwood, P. Articles by Robertson, C.F