Flavonoids are a subclass of polyphenolic compounds found ubiquitously in plant foods. Their secondary metabolites have roles in processes such as pigmentation, defence immune responses and protection from ultraviolet-B radiationReference Bruce, Folkerts, Garnaat, Crasta, Roth and Bowen1, Reference Scalbert, Morand, Manach and Remesy2. More than 5000 identified flavonoids occur in plantsReference Ross and Kasum3 and are divided into six major classes: anthocyanidins, flavan-3-ols, flavanones, flavones, flavonols and isoflavonesReference Ross and Kasum3, Reference Hu and Willett4.
In vitro and in vivo studies indicate that dietary flavonoids affect the risk of various diseases including cancer and coronary heart disease (CHD). Population studies have shown associations between flavonoid consumption and CHD riskReference Cook and Samman5–Reference Maron7. At the molecular level, flavonoids may contribute to CHD risk reduction by affecting low-density lipoprotein (LDL) oxidationReference De Whalley, Rankin, Hoult, Jessup and Leake8, Reference Negre-Salvayre and Salvayre9, fatty plaquesReference Steinberg, Parthasarathy, Carew, Khoo and Witztum10, Reference Laughton, Evans, Moroney, Hoult and Halliwell11 and hypercholesterolaemiaReference Hu and Willett4, Reference Maron7. Moreover, they can inhibit the formation of reactive oxygen species and protect genes that decrease cancer riskReference Rolfes, Whitney and DeBruyne12, Reference Sizer and Whitney13. In addition to antioxidant properties, some flavonoids exhibit antimicrobial, antiviralReference Hanasaki, Ogawa and Fukui14, erythrocyte protectionReference Youdim, Shukitt Hale, MacKinnon, Kalt and Joseph15, anti-inflammatory and antiallergenic propertiesReference Hope, Welton, Fiedler-Nagy, Batula-Bernardo and Coffey16.
Given the potential role of flavonoids in disease prevention, it is useful to understand variations in consumption patterns. To date, few consumption studies have been published. One early study estimated the mean intake of total flavonoids in the USA to be about 1 g dailyReference Kuhnau17. More recent studies have estimated individual flavonoid or flavonoid profile intakes in the USAReference Sampson, Rimm, Hollman, de Vries and Katan18, DenmarkReference Justesen, Knuthsen and Leth19, HollandReference Hertog, Hollman, Katan and Kromhout20, FinlandReference Kumpulainen, Voutilainen and Salonen21, FranceReference Commenges, Scotet, Renaud, Jacqmin-Gadda, Barberger-Gateau and Dartigues22, GreeceReference Lagiou, Samoli, Lagiou, Peterson, Tzonou and Dwyer23, JapanReference Arai, Watanabe, Kimira, Shimoi, Mochizuki and Kinae24 and SpainReference Garcia-Closas, Gonzalez, Agudo and Riboli25, although the dietary intake methodologies vary substantially. The present study was initiated to add an Australian perspective to international comparisons. Further, major contributors to dietary flavonoid intake such as wine and tea vary in consumption across age groups26. The study sought to provide insight into how sources and intakes of various flavonoids vary according to age.
Methods
Data from two sources were used to formulate estimates of flavonoid intake. First, intake of flavonoids was derived from the most recent survey of dietary intake in Australia (the National Nutrition Survey 1995; NNS95)26. This survey used a nationally representative sub-sample (n = 17 326) of the National Health Survey. People over the age of 2 years were included in the survey and the overall response rate was 80%. It was based on a 24-hour recall of food and beverage intake on the day prior to the interview, midnight to midnight. This survey collected detailed descriptions on types and quantities of all foods and beverages consumed by respondents. Standardised measuring guides were used to assist respondents in estimating the amount of food actually consumed.
In the published NNS95 analysis, vegetables and fruits were grouped together. Therefore, the original dataset was reassessed by the Australian Bureau of Statistics (ABS) to provide intake data of consumption of individual flavonoid-containing foods (including mixed dishes), according to age grouping, based on the 24 hour-recall data. The following categories were ungrouped into individual foods: pome, berry, citrus, stone, tropical fruit, other fruits, cabbage, cauliflower and similar brassica vegetables, carrot and similar root vegetables, peas and beans, leaf and stalk vegetables, other fruiting vegetables, other vegetables and legumes.
To provide another perspective on flavonoid consumption, apparent consumption (per capita, all ages) of major dietary flavonoid sources was derived from agricultural production data27. In certain instances, single foods are grouped into categories within this agricultural dataset. For example, lettuce and celery are grouped into the category of leaf and green vegetables but have very different flavonoid profiles28. Therefore, industry production data sources were used in such cases to estimate the proportion of individual foods within the various ABS agricultural categories.
Since there is no comprehensive composition dataset for flavonoid contents of Australian foods, US Department of Agriculture (USDA) data were applied28, an approach that has been used in similar studies in other countriesReference Sampson, Rimm, Hollman, de Vries and Katan18, Reference Lagiou, Samoli, Lagiou, Peterson, Tzonou and Dwyer23. This currently is the most complete database available, with 225 reference foods. It should be noted that the USDA database has collated data from a range of sources, with variations in data quality28.
Previous studies from Denmark, The Netherlands and the USA published dietary data in conjunction with estimates of flavonoid intake. The dietary data from such studies were reanalysed for all flavonoids listed in Table 1, applying USDA food composition data, to derive the reanalysed totals in Table 2. The Statistical Package for the Social Sciences (SPSS version 12.0.1; SPSS Inc., Chicago, IL, USA) was used to derive mean intake values.
Flavonoid intake (mg day−1) according to age, based on 24-hour recall data from the Australian National Nutrition Survey 1995
Flavonoid intake (mg day−1) reported in various studies, including reanalysis (using all flavonoids in Table 1) according to reported consumption of foods
FFQ – food-frequency questionnaire.
Results
Dietary flavonoid intake from NNS95 data was estimated at 225 mg person− 1 day− 1 (only 145 of the 225 USDA reference foods were reported to be consumed). Consumption of individual flavonoids in each age group is shown in Table 1. People aged 19 years and over consumed 454 mg day− 1, of which 92% were flavan-3-ols (Fig. 1). This difference between all ages and adult people was due predominantly to tea consumption, which increased with age starting at 19–24 years (see Fig. 6 below). The average Australian apparent flavonoid consumption was 351 mg day–1 of which 75% were flavan-3-ols (Fig. 1). Apart from tea which contributed 76% of flavonoid intake, the highest flavonoid source was oranges – supplying four times more flavonoids than any other fruit, beverage or vegetable group. Other important flavonoid sources were, in descending order, other citrus fruit, grapes, wine, apples and leaf and stalk vegetables.
Intakes (proportions) of flavonoid classes reported in the USAReference Sampson, Rimm, Hollman, de Vries and Katan18 and DenmarkReference Justesen, Knuthsen and Leth19 compared with Australian estimates (24-hour recall data from the National Nutrition Survey 1995 (NNS95) and apparent consumption data) from the present study
In the NNS95 analysis, black tea was the major flavonoid source (predominantly flavan-3-ols). Figure 2 shows proportions of non-flavan-3-ol flavonoid classes determined by the two intake assessment methods. Because of the dominance of flavan-3-ols in total flavonoid intake, the data from NNS95 were analysed in the absence of contributions from black and green tea (Fig. 3). This enabled a clearer visualisation of the intake dynamics of flavonoids other than those supplied exclusively by black and green tea.
Intakes (proportions) of flavonoid classes (other than flavan-3-ol) reported in the USAReference Sampson, Rimm, Hollman, de Vries and Katan18 and DenmarkReference Justesen, Knuthsen and Leth19 compared with Australian estimates (24-hour recall data from the National Nutrition Survey 1995 (NNS95) and apparent consumption data) from the present study
Intakes (proportions) of flavonoid classes reported in the USAReference Justesen, Knuthsen and Leth19 and DenmarkReference Sampson, Rimm, Hollman, de Vries and Katan18 compared with Australian estimates (24-hour recall data from the National Nutrition Survey 1995 (NNS95) and apparent consumption data) from the present study (excluding tea consumption)
The range of individual flavonoids included in previous consumption studies is relatively varied and comparisons are therefore limited in their scope. Figure 4 compares the consumption estimates for five major flavonoids from previous studies with those of the present study. Quercetin dominated flavonoid intake profiles for all four countries (Fig. 4) even when tea consumption was not considered (Fig. 5).
Intakes of individual flavonols and flavones (percentage of total flavonoid intake) reported in the USAReference Sampson, Rimm, Hollman, de Vries and Katan18, DenmarkReference Justesen, Knuthsen and Leth19 and The NetherlandsReference Hertog, Hollman, Katan and Kromhout20, Reference Arts, Hollman, Feskens, Bueno de Mesquita and Kromhout32 compared with Australian estimates (24-hour recall data from the National Nutrition Survey 1995 (NNS95) and apparent consumption data) from the present study (including tea consumption)
Intakes of individual flavonoids (percentage of total flavonoid intake) reported in the USAReference Sampson, Rimm, Hollman, de Vries and Katan18 and DenmarkReference Justesen, Knuthsen and Leth19 compared with Australian estimates (24-hour recall data from the National Nutrition Survey 1995 (NNS95) and apparent consumption data) from the present study (excluding tea consumption)
Apart from tea flavonoids, hesperetin and naringenin consumption was high, in view of citrus fruit intake (especially oranges). Tea was not the sole source of catechin, epicatechin and quercetin, which were still important contributors to total flavonoid consumption (via wine) for adults and apples for all ages. Although these five flavonoids were the major dietary flavonoids across all ages in the present study, variations in consumption of individual flavonoids occurred according to age (Figs 678910). Analysis of 24 hour-recall data from the NNS95 revealed apple as the most important source of quercetin until age 16–18 years, after which onions became an increasingly important prominent source. Variations in hesperetin consumption reflected orange intake. Apple was also the major source of epicatechin and catechin for children. For catechin, grapes and peach also contributed. However, these sources became less prominent as wine consumption increased in adulthood. Wine was the predominant source of malvidin, as well as delphinidin, peonidin and petunidin which all followed wine consumption patterns. Variations in hesperetin consumption reflected orange intake. Naringenin intake was consistent as a percentage of total flavonoid intake until 19–24 years, corresponding to orange intake. Naringenin intake then increased with age corresponding to grapefruit intake.
Comparison of total flavonoid intake (mg day− 1), with or without tea, according to age group; 24-hour recall data from the Australian National Nutrition Survey 1995
Contribution to total flavonoid intake (mg day− 1) of tea (left axis) and wine (right axis), according to age group; 24-hour recall data from the Australian National Nutrition Survey 1995
Percentage of total flavonoid intake contributed by flavonoid classes, according to age (excluding tea consumption); 24-hour recall data from the Australian National Nutrition Survey 1995
Intake of major flavonoids, as a percentage of total flavonoid intake, according to age (excluding tea consumption); 24-hour recall data from the Australian National Nutrition Survey 1995
Intake of minor flavonoids (mg day− 1), according to age group (excluding tea consumption); 24-hour recall data from the Australian National Nutrition Survey 1995
Discussion
The use of US flavonoid content data in the analysis of Australian dietary data is not ideal, and was done in the absence of adequate local data. The USDA acknowledges that factors such as cultivar, geography, climate, farming practices, processing and storage can introduce substantial variation in flavonoid content of foods28. The extent to which flavonoid intake estimates in this study would vary if local composition data were available is not known.
The consumption of flavan-3-ol dominated the flavonoid intake profile determined by both methods in this study, similar to consumption data for national flavonoid intakes for Denmark and the USA (Fig. 1). This is due to the importance of black tea in the diet of these countries. The reported average total flavonoid consumption for Denmark is markedly lower than the Australian and US estimates (175 vs. 454 and 211 mg day− 1, respectively), due to variations in single flavonoid intakes between countries (Table 2). In the USA, flavan-3-ols represented only 68% of total flavonoid consumption due to lower tea consumption.
The second most abundant class of flavonoids in the US diet are flavanones (15% of total flavonoids). In Denmark and the present 24-hour recall analysis, flavanones represent a smaller proportion because of the dominance of flavan-3-ols from black tea (Fig. 1). When tea consumption was excluded, variations in flavanone proportions were still apparent (Fig. 3). Anthocyanidin consumption was higher in the USA than in other countries, probably due to higher consumption of blueberries which are a very rich source28. However, the Danish analysis only included blackcurrant and not other major anthocyanidin sources such as cherries and berries, and may therefore be an underestimate of true consumption. The consumption of flavones in Australia was higher than that reported for Denmark and USA, due to celery and parsley consumption not being analysed in the Danish and US studies. Comparisons of flavonoid intake from various countries are shown in Table 2. These combined data indicate that such dietary studies vary in their methodological approaches. In view of the number of dietary flavonoid sources and the extensive range of flavonoids found in foods, diet diary methods offer more reliable flavonoid intake data than food-frequency questionnaires, since the latter often have not been validated for flavonoid intake and individual flavonoid sources can easily be overlooked.
Figure 3 revealed a higher flavan-3-ol consumption in Australia than the comparison countries due to the inclusion of both wine and apple (vs. apple only) in the present study. Figure 4 highlights the lack of methodological consistency between studies outlined in Table 2. Apiengenin consumption appears higher in Australia, but is due to parsley and celery consumption not being included in other studies. The apparent greater diversities of flavonoid consumption in Australia compared with Denmark and the USA is likely due to the broader range of flavonoid-rich foods included the present study. In Table 2, estimates were reanalysed using food intakes reported in the original studies. Reanalysis of the Dutch study was not done because consumption of individual foods was not reported.
Estimates of flavonoid consumption in various countries have used non-representative sub-samples of national populations. An Australian study of 24 women reported total flavonoid intake of 128 mg day− 1, with intake dominated by 59% attributed to flavon-3-ols. However, their study was based on only 15 flavonoids (vs. 26 in the present study). An analysis of our data using the same flavonoids as Lyons-Wall et al. Reference Lyons-Wall, Autenzio, Lee, Moss, Gie and Samman30 (except for fisetin which is not included in the USDA database) yielded an average intake of 216 mg day− 1 for people aged 19 years and over and 173 mg day− 1 for 25–44-year-olds. Proportions of flavanones (3%) and flavonols (10%) in the present study were lower than those reported by Lyons-Wall et al. Reference Lyons-Wall, Autenzio, Lee, Moss, Gie and Samman30 (18 and 20%, respectively). Details of such studies from other countries are noted in Table 2.
Total flavonoid intake derived from apparent consumption data exceeded estimates from 24-hour recall data of a representative sample of the national population. This difference was despite the common occurrence of overreporting of flavonoid-rich foods (i.e. fruits and vegetables) reported previously in such surveys (NNS). Both apparent consumption and 24-recall data indicated that apigenin intake was markedly higher in Australia than reported in either the USA or Denmark, due presumably to differences in consumption of leaf and stalk vegetables (e.g. lettuce and celery) and parsley. Compared with the NNS95 analysis, apparent flavanone consumption was higher and apparent flavonol consumption lower due to differences in the ratio of orange to apple consumption in the two methods. The inherent weaknesses of apparent consumption estimates are well documented, and these data were included specifically as a comparison to previous studies which have used this same methodology.
If tea consumption is excluded for all ages, five flavonoids emerge as major dietary contributors: catechin, epicatechin, hesperetin, naringenin and quercetin. Even if their proportions of total flavonoid intake decrease with age, absolute intakes either remain constant or increase (except for young adults because of lower vegetable and fruit consumption). This study identifies apple consumption as an important flavonoid source for young people, as is citrus fruit for hesperetin and naringenin consumption. Hesperitin and naringenin have possible antiviral and antibacterial propertiesReference Hanasaki, Ogawa and Fukui14 and anthocyanidins have been shown to exert effects on red blood cellsReference Youdim, Shukitt Hale, MacKinnon, Kalt and Joseph15. It is therefore conceivable that variations in intake according to age may have some potential for impact on disease patterns.
Black tea and green tea differ in their flavonoid profiles. Green tea is richer in epicatechin, epicatechin-3-gallate, epigallocatechin and epigallocatechin-3-gallate (EGCG) but has lower levels of thearubigins and theaflavins28. Upwards of 78% of all tea consumption in Western countries is black tea, the contrary being true for Asian countriesReference Siddiqui, Afaq, Adhami, Ahmad and Mukhtar33. Such variations may have health implications in view of the specific roles of the various flavonoids. For example, both thearubigins and EGCG are implicated in cancer preventionReference Siddiqui, Afaq, Adhami, Ahmad and Mukhtar33, Reference Lambert and Yang34 but EGCG is further implicated in heart disease aetiologyReference Arts, Hollman, Feskens, Bueno de Mesquita and Kromhout32.
Conclusion
Estimates of total flavonoid consumption such as in the present study represent a preliminary step in the understanding of flavonoid–health relationships. At present, it is unclear whether absolute intakes of individual flavonoids or ratios between them are more relevant to human health. For this reason, intake studies should report data in both formats. Similarly, because of uncertainty regarding the chemical classificationReference Haslam35 and biological natureReference Scalbert, Morand, Manach and Remesy2 of flavonoids, data on individual flavonoids should be presented where possible. Food preparation methods are also an issue to be addressed in further studies, since there is clear evidence that these can affect bioavailability substantially28, Reference Andlauer, Stumpf, Hubert, Rings and Furst36, Reference Manach, Scalbert, Morand, Remesy and Jimenez37.
The present study reports age-related variations in the intake and sources of dietary flavonoids. Cohort studies are needed to determine if these variations are a longitudinal phenomenon. The profile of flavonoid intake seen in Australia from this present study revealed some differences to estimates from other countries. More consistent methods between studies are required to confirm the nature and extent of these differences.
