Validation of biomarkers of food intake—critical assessment of candidate biomarkers

Biomarkers of food intake (BFIs) are a promising tool for limiting misclassification in nutrition research where more subjective dietary assessment instruments are used. They may also be used to assess compliance to dietary guidelines or to a dietary intervention. Biomarkers therefore hold promise for direct and objective measurement of food intake. However, the number of comprehensively validated biomarkers of food intake is limited to just a few. Many new candidate biomarkers emerge from metabolic profiling studies and from advances in food chemistry. Furthermore, candidate food intake biomarkers may also be identified based on extensive literature reviews such as described in the guidelines for Biomarker of Food Intake Reviews (BFIRev). To systematically and critically assess the validity of candidate biomarkers of food intake, it is necessary to outline and streamline an optimal and reproducible validation process. A consensus-based procedure was used to provide and evaluate a set of the most important criteria for systematic validation of BFIs. As a result, a validation procedure was developed including eight criteria, plausibility, dose-response, time-response, robustness, reliability, stability, analytical performance, and inter-laboratory reproducibility. The validation has a dual purpose: (1) to estimate the current level of validation of candidate biomarkers of food intake based on an objective and systematic approach and (2) to pinpoint which additional studies are needed to provide full validation of each candidate biomarker of food intake. This position paper on biomarker of food intake validation outlines the second step of the BFIRev procedure but may also be used as such for validation of new candidate biomarkers identified, e.g., in food metabolomic studies.     

Biomarkers of the metabolic syndrome: influence of selected foodstuffs,containing bioactive components

The influence of various non-nutritive bioactive foodstuffs and food components on the biomarkers of the metabolic syndrome in humans is critically reviewed. Tea, coffee, cocoa, soy, olive oil, fruit and nuts are most of the time found to be effective in improving lipid profiles, CRP and adiponectin. Spices (garlic, curcumin and cinnamon), carotenoids and the phytosterol/-stanols are frequently related to lower risk of metabolic syndrome and improved biomarkers. Since food is a complex matrix and the heterogeneity of studied population and served diets are not always well-defined, this could explain some contradictory results found in literature. Other factors jeopardizing definite conclusions are mentioned.     

Validation of overweight children's fruit and vegetable intake using plasma carotenoids

Assessing dietary intake in children is difficult and limited validated tools exist. Plasma carotenoids are nutritional biomarkers of fruit and vegetable intake and therefore suitable to validate reported dietary intakes. The aim of this study was to examine the comparative validity of a food frequency questionnaire (FFQ), completed by parents reporting child fruit and vegetable intake compared to plasma carotenoid concentrations. A sample of children aged 5-12 years (n = 93) from a range of weight categories were assessed. Dietary intake was measured using a 137-item semi-quantitative FFQ. Plasma carotenoids were measured using reverse phase high-performance liquid chromatography. Pearson correlation coefficients between reported dietary intake of carotenoids and plasma carotenoid concentrations were strongest after adjustment for BMI (beta-carotene (r = 0.56, P < 0.05), alpha-carotene (r = 0.51, P < 0.001), cryptoxanthin (r = 0.32, P < 0.001)). Significantly lower levels (P < 0.05) of all plasma carotenoids, except lutein, were found among overweight and obese children when compared to healthy weight children. Parental report of children's carotenoid intakes, using a FFQ can be used to provide a relative validation of fruit and vegetable intake. The lower plasma carotenoid concentrations found in overweight and obese children requires further investigation.     

Associations of Children’s Appetitive Traits with Weight and Dietary Behaviours in the Context of General Parenting

Background

Individual variations in child weight can be explained by genetic and behavioural susceptibility to obesity. Behavioural susceptibility can be expressed in appetite-related traits, e.g. food responsiveness. Research into such behavioural factors is important, as it can provide starting points for (preventive) interventions.

Objectives

To examine associations of children’s appetitive traits with weight and with fruit, snack and sugar-sweetened beverage intake, and to examine whether parenting style interacts with appetite in determining child weight/intake.

Methods

Data were used from 1275 children participating in the INPACT study in 2009–2010, with a mean age of 9 years in 2009. Their height and weight were measured to calculate body mass index (BMI). Parents completed a questionnaire to measure children’s appetitive traits, children’s dietary intake and parenting style. Child BMI z-scores, fruit, snack and sugar-sweetened beverage intake were regressed on appetitive traits. Moderation by parenting style was tested by adding interaction terms to the regression analyses.

Results

Food-approaching appetitive traits were positively, and food-avoidant appetitive traits were negatively related to child BMI z-scores and to child fruit intake. There were no or less consistent associations for snack and sugar-sweetened beverage intake. Authoritative parenting voided the negative association between food fussiness and fruit intake, while neglecting parenting strengthened the positive association between food-approaching appetitive traits and weight.

Conclusions

Early assessment of appetitive traits could be used to identify children at risk for overweight. As parenting style can moderate the associations between appetitive traits and weight/intake in a favourable way, parents are a promising target group for preventive interventions aimed at influencing the effect of appetitive traits on children.     

Feeding ecology of the northern Ryukyu fruit bat, Pteropus dasymallus dasymallus, in a warm-temperate region

The warm-temperate fruit bat, Pteropus dasymallus dasymallus consumed at least 17 species of fruits, five of flowers, nine of leaves, one of bark and eight of insects. Soft fruits formed the bulk of its diet. Ficus eaten by the bat fruited asynchronously among individuals of the same species. In these species, the ratios of trees bearing ripe fruit to all trees cxamined each month were very low except for F. erecta. On the other hand, some plant species showed synchronous fruit production over a short period. Both types of plants supply fruits in every season. Seasonal dietary shifts and food choice were evident, and flowers, leaves or insects formed a small but nutritionally important component of the diet of the bat. The frequency of mastication was 124–155 per one pellet produced within a few minutes. The bat extracted and swallowed 61 82% ofthe fruits' wet weight and 58–73% of the insects' weight. The swallowed juice passed through the digestive systems in only 34 min on average. The bat ingested 0.5 times its body weight in figs per day. It is probablc that such a low food intake is adapted for the seasonal changes of food availability in the warm temperate region.     

Dietary generalists and nutritional specialists: Feeding strategies of adult female blue monkeys (Cercopithecus mitis) in the Kakamega Forest,Kenya

Generalist primates eat many food types and shift their diet with changes in food availability. Variation in foods eaten may not, however, match variation in nutrient intake. We examined dietary variation in a generalist‐feeder, the blue monkey (Cercopithecus mitis), to see how dietary food intake related to variation in available food and nutrient intake. We used 371 all‐day focal follows from 24 adult females (three groups) in a wild rainforest population to quantify daily diet over 9 months. We measured food availability using vegetation surveys and phenology monitoring. We analyzed >700 food and fecal samples for macronutrient content. Subjects included 445 food items (species‐specific plant parts and insect morphotypes) in their diet. Variation in fruit consumption (percentage of diet and total kcal) tracked variation in availability, suggesting fruit was a preferred food type. Fruits also constituted the majority of the diet (by calories) and some fruit species were eaten more than expected based on relative availability. In contrast, few species of young leaves were eaten more than expected. Also, subjects ate fewer young leaves (based on calories consumed) when fruit or young leaves were more available, suggesting that young leaves served as fallback foods. Despite the broad range of foods in the diet, group differences in fiber digestibility, and variation that reflected food availability, subjects and groups converged on similar nutrient intakes (grand mean ± SD: 637.1 ± 104.7 kcal overall energy intake, 293.3 ± 46.9 kcal nonstructural carbohydrate, 147.8 ± 72.4 kcal lipid, 107.8 ± 12.9 kcal available protein, and 88.1 ± 17.5 kcal structural carbohydrate; N = 24 subjects). Thus, blue monkeys appear to be food composition generalists and nutrient intake specialists, using flexible feeding strategies to regulate nutrient intake. Findings highlight the importance of simultaneously examining dietary composition at both levels of foods and nutrients to understand primate feeding ecology.     

乙醇浓度对圈养长舌果蝠摄食糖水量的影响

正在自然生境中,果蝠主要以果实或者花蜜为食,成熟果实或花蜜由于微生物发酵而含一定量的乙醇。乙醇在生态系统中是一种常见物质,它是生物厌氧代谢的终端产物之一(Van Waarde,1991)。一旦果实成熟,它们中的糖分就会被微生物或者自身发酵代谢成乙醇(Battcock and Azam-Ali,1998;Dudley,2000,2004)。果实中的乙醇浓度主要是由这些以糖分为能源的发酵微生物的扩增状态来决定     

The effects of resource availability on alternative mating tactics in guppies (Poecilia reticulata)

Food availability can influence the optimal allocation of timeand energy among alternative behaviors such as foraging, courting,and competing for mates. If populations differ consistentlyin food availability, selection may cause geographic divergencein allocation strategies. At the opposite extreme, a norm ofreaction may evolve such that food intake influences the allocationstrategy of individuals in the same way in all populations.Between these two extremes, food intake reaction norms may divergegenetically among populations. For example, at sites where foodis scarce, selection may strengthen the effect of food intakeon behavior, whereas at sites with abundant food, selectionmay be weak or even oppose plasticity. We tested these ideasby raising male guppies from streams differing in food availabilityin a common laboratory environment on either low or high foodlevels, and then observing them in the presence of male competitors(from the same population and diet group) and receptive females.Males from low-food-availability streams spent more time foragingthan males from high-food-availability streams, independentof food intake. Compared with males raised on the high foodlevel, males raised on the low food level spent more time foragingand were less aggressive towards other males. Courtship displayrate increased with food intake but only in males from low-foodstreams. In contrast, males from high-food streams showed greaterplasticity with respect to male-male aggression. These resultsgenerally support the resource availability/behavioral tradeoffhypothesis while also revealing a surprising degree of ontogeneticcomplexity in a relatively simple system.     

Do Fruit Nutrients Affect Subgrouping Patterns in Wild Spider Monkeys (<Emphasis Type="Italic">Ateles geoffroyi</Emphasis>)?

One of the main costs of group living is feeding competition. Fission–fusion dynamics are thought to be a strategy to avoid overt competition for food resources. We tested whether food abundance and quality affected such dynamics in a species characterized by a high degree of fission–fusion dynamics. We collected data on 22 adult and subadult spider monkeys (Ateles geoffroyi) living in a large community in the protected area of Otoch Ma’ax Yetel Kooh, Yucatan, Mexico. We recorded subgroup size and fission events as well as fruit abundance during 12 mo and conducted nutritional analyses on the fruit species that the study subjects consumed most. We found no effect of fruit abundance or nutritional quality of recently visited food patches on individual fission decisions, but the amount of protein in the food patches visited over the course of the day was a good predictor of subgroup size. While the absence of support for a relationship between fruit characteristics and fission decisions may be due to the short temporal scale of the analysis, our findings relating subgroup size to the amount of protein in the visited food patches over the course of the day may be explained by individual spider monkeys attempting to obtain sufficient protein intake from their fruit-based diet.     

Biomarker of food intake for assessing the consumption of dairy and egg products

Dairy and egg products constitute an important part of Western diets as they represent an excellent source of high-quality proteins, vitamins, minerals and fats. Dairy and egg products are highly diverse and their associations with a range of nutritional and health outcomes are therefore heterogeneous. Such associations are also often weak or debated due to the difficulty in establishing correct assessments of dietary intake. Therefore, in order to better characterize associations between the consumption of these foods and health outcomes, it is important to identify reliable biomarkers of their intake. Biomarkers of food intake (BFIs) provide an accurate measure of intake, which is independent of the memory and sincerity of the subjects as well as of their knowledge about the consumed foods. We have, therefore, conducted a systematic search of the scientific literature to evaluate the current status of potential BFIs for dairy products and BFIs for egg products commonly consumed in Europe. Strikingly, only a limited number of compounds have been reported as markers for the intake of these products and none of them have been sufficiently validated. A series of challenges hinders the identification and validation of BFI for dairy and egg products, in particular, the heterogeneous composition of these foods and the lack of specificity of the markers identified so far. Further studies are, therefore, necessary to validate these compounds and to discover new candidate BFIs. Untargeted metabolomic strategies may allow the identification of novel biomarkers, which, when taken separately or in combination, could be used to assess the intake of dairy and egg products.     

Diet of Grauer's Gorillas in the Montane Forest of Kahuzi,Democratic Republic of Congo

We describe the diet of a semihabituated group of Grauer's gorillas (Gorilla beringei graueri) inhabiting the montane forest of Kahuzi-Biega National Park, Democratic Republic of Congo, based on direct observations, feeding remains in their fresh trails, and fecal samples collected over 9 yr. We examined fruit availability in their habitat; consumption of fruit, vegetative, and animal food; and daily intake of vegetative plant food using a transect, fruit monitoring trails, fecal analysis, and tracing of the animal's daily trails between consecutive nest sites. The fruit food repertoire of Kahuzi gorillas resembles that of western and eastern lowland gorillas inhabiting lowland tropical forests, while their vegetative food repertoire resembles that of mountain gorillas inhabiting montane forests. Among 236 plant foods (116 species), leaves, pith, and barks constitute the major parts (70.2%), with fruit making up the minor part (19.7%). About half (53.2%) of the total fecal samples included fruit remains. The gorillas used leaves, stems and other vegetative plant parts as staples. Their fruit intake was similar to that reported for mountain gorillas in Bwindi. They ate animal foods, including earthworms, on rare occasions. Variation in fruit consumption was positively associated with variation in fruit production. The gorillas ate fig fruits frequently; fig intake is positively correlated with that of other fruits, and figs were not fallback foods. They relied heavily on bamboo shoots on a seasonal basis; however, no bamboo shoots were available for several years after a major flowering event. Our results support the argument that variation in gorilla diets mostly reflects variation in vegetational composition of their habitats.     

Fruit availability, chimpanzee diet, and grouping patterns on Rubondo Island, Tanzania

We examined seasonal patterns of fruit availability, dietary quality, and group size in the descendants of an introduced chimpanzee population on Rubondo Island, Tanzania. The site has supported a free-ranging population without provisioning for 40 years. Our goals were to determine whether Rubondo chimpanzees experience periods of fruit shortage, and whether they respond to changes in fruit availability similarly to chimpanzees at endemic sites. We indexed the fruit availability of tree and liana species on transects stratified across three chimpanzee ranging areas. We used fecal analyses to evaluate seasonal changes in diet, and used data on party size and nesting group size to examine seasonal patterns of grouping. Tree fruit availability was positively correlated with rainfall, with a period of relative tree fruit scarcity corresponding with the long dry season. Liana fruit availability was not related to rainfall, and lianas exhibited less variable fruiting patterns across seasons. Fruits made up the majority of the chimpanzee diet, with lianas accounting for 35% of dietary fruit species. Fruits of the liana Saba comorensis were available during all months of phenological monitoring, but they were consumed more when tree fruit was scarce, suggesting that Saba comorensis fruits may be a fallback food for Rubondo chimpanzees. There were no increases in consumption of lower-quality plant parts between seasons, and there were no changes in group size between seasons. These results contrast with evidence from several endemic chimpanzee study sites, and indicate that Rubondo chimpanzees may have access to abundant and high-quality foods year round.     

Reducing obesity will require involvement of all sectors of society

We need all sectors of society involved in reducing obesity. The food industry's effort to reduce energy intake as part of the Healthy Weight Commitment Foundation is a significant step in the right direction and should be recognized as such by the public health community. We also need to get organizations that promote physical inactivity, such as computer, automobile, and entertainment industries, to become engaged in efforts to reduce obesity.     

Diet quality and the attractiveness of male body odor

Human axillary sweat may provide information pertaining to genetic relatedness and health status. A significant contributor to good health, both in the short and longer term, is a diet rich in fruit and vegetables. In this study we tested whether dietary fruit and vegetable intake, assessed indirectly by skin spectrophotometry (assessing dietary carotenoid intakes) and subjectively by food frequency questionnaire, was associated with more pleasant smelling sweat. Male participants provided axillary sweat samples and dietary information. Female participants then evaluated these samples on several affective, qualitative and psychophysical dimensions. The skin spectrophotometry measure (CIELab b*), indicative of greater fruit and vegetable intake, was significantly associated with more pleasant smelling sweat (with more floral, fruity, sweet and medicinal qualities), independent of sweat intensity. Self-report dietary data revealed that fat, meat, egg and tofu intake was associated with more pleasant smelling sweat, and greater carbohydrate intake with stronger smelling less pleasant sweat. These data parallel facial judgments, in which yellower more carotenoid rich skin, is found to be more attractive.     

The influence of ambient temperature and the energy and protein content of food on nitrogenous excretion in the Egyptian fruit bat (Rousettus aegyptiacus)

The diets of frugivorous and nectarivorous vertebrates contain much water and generally have high energy but low protein contents. Therefore, we tested the prediction that to save energy under conditions of high energy demands and high water intake, frugivorous Egyptian fruit bats (Rousettus aegyptiacus) will increase both the absolute quantity and the proportion of ammonia in their urine. We also examined whether such changes occur when protein intake is low and water intake is high. We did three feeding trials. In trials 1 and 2, bats were fed one of four liquid diets containing constant soy protein concentrations but varying in sucrose concentration and were kept at ambient temperatures (T(a)) of 30 degrees Celsius and 12 degrees Celsius, respectively. In trial 3, bats were kept at Ta=12 degrees Celsius and fed one of four liquid diets with equal sucrose concentrations but varying protein concentrations. In trial 1, food intake at a sucrose concentration of 256 mmol/kg H(2)O was initially high but decreased to a constant rate with further increases in sucrose concentration, while in trial 2, food intake decreased exponentially with increasing sucrose concentration. As predicted, at 12 degrees Celsius with varying sucrose concentration, both the absolute quantity and the fraction of ammonia in the bats' urine increased significantly with food intake (P<0.02), while the absolute quantity of urea and the fraction of urea nitrogen excreted decreased significantly with food intake (P<0.03). Varying sucrose concentration had no significant effect on nitrogen excretion at Ta=30 degrees Celsius. Varying protein concentration had no significant effect on nitrogen excretion at Ta=12 degrees Celsius. We suggest that Egyptian fruit bats can increase ammonia excretion in response to increased energetic demands, and we calculate that they can save energy equal to approximately 2% of their daily metabolic rate by doing so.     

Food Items Consumed by White-headed Langurs in Fusui, China

We studied the socioecology of white-headed langurs (Trachypithecus leucocephalus) from September 1997 to September 1998 in Fusui Precious Animal Reserve, SW Guangxi, China. We collected data on climate, phenology of food plant species, and foods consumed by langurs living in habitats with different levels of human disturbance. Feeding records showed that the most food is from less common plant species. Young leaves were the staple food item in all langur groups, and consumption correlates with availability. Consumption of mature leaves is not significantly correlated with their availability, but the langurs fed on them, and other food items such as fruits and seeds, when the availability of young leaves was low. Langurs in different areas had broadly similar diets, but they varied most in the proportion of supplementary items such as fruit. Groups in more disturbed habitat did not increase the overall proportion of mature leaves in their diet, but instead maintained their intake of young leaves from a greater diversity of species, and incorporated more immature fruit. Conservationists should direct efforts toward protection of rare plant species providing preferred food items, particularly supplementary foods at times when, and in areas where, preferred food items are less available.     

Involvement of cortisol and sirtuin1 during the response to stress of hypothalamic circadian system and food intake-related peptides in rainbow trout,Oncorhynchus mykiss

Stress is conditioning animal welfare by negatively affecting a wide range of physiological and behavioral functions. This may be applied to circadian physiology and food intake. Cortisol, the stress-related hormone, may mediate such effect of stress, but other indirect mediators might be considered, such as sirtuin1. Then, either the independent modulatory effect or the existence of any interaction between mediators may be responsible. The circadian system is the main modulator of several integrative mechanisms at both central and peripheral levels that are rhythmically presented, thus influencing different processes such as food intake. In this way, food intake is controlled by the circadian system, as demonstrated by the persistence of such rhythms of food intake in the absence of environmental external cues. Our study aimed to evaluate the daily profile of hypothalamic mRNA abundance of circadian clock genes (clock1a, bmal1, per1 and rev-erbβ-like), and food intake regulators (crf, pomc-a1, cart, and npy) in rainbow trout (Oncorhynchus mykiss), the impact of stress on such rhythms, and the involvement of cortisol and sirtuin1 as mediators. Four cohorts of trout were subjected to 1) normal stocking density (control group), 2) high stocking density for 72 hours (stress group), 3) normal stocking density and implanted with mifepristone, a glucocorticoid receptors antagonist, and 4) mifepristone administered and stressed for 72 hours. Fish from each group were sampled every 4-h along the 24-h LD cycle, and cortisol, glucose and lactate plasma levels were evaluated. Hypothalamic mRNA abundance of clock genes, food intake regulators, glucocorticoid receptors and sirtuin1 were qPCR assayed. Our results reveal the impact of stress on most of the genes assayed, but different mechanisms appear to be involved. The rhythm of clock genes displayed decreased amplitude and averaged levels in stressed trout, with no changes of the acrophase being observed. This effect was not prevented by mifepristone. On the contrary, the effect of stress on the daily profile of crf, pomc-a1, and npy was totally prevented by mifepristone administration. Accordingly, cortisol appears to mainly mediate the effect of stress on food intake regulators through binding to specific glucocorticoid receptors within trout hypothalamus, whereas sirtuin1 is apparently mediating such effects on the circadian system in the same brain region. Further research must be performed to clarify those mechanisms through which stress influences food intake and the circadian oscillator within the same brain region, hypothalamus, in rainbow trout, and the interaction among them all.     

The diet of chimpanzees in the Budongo Forest Reserve, Uganda

Chimpanzee diets are highly variable, but in all cases dominated by ripe fruit. Previous work has suggested that in the Budongo Forest Reserve, Uganda, ripe fruit remains available throughout the year, but dietary data for chimpanzees at this site remain sparse. This paper details the diet of a recently habituated community of Budongo chimpanzees living in the Sonso region. Chimpanzees of this community spent 64.5% of their feeding time eating fruit, and 19.7% eating arboreal leaves. Terrestrial herbaceous vegetation formed only a minor component of the diet. In these general dietary characteristics, Budongo chimpanzees show greater similarity to those of the Gombe National Park than they do to those in the geographically closer and floristically more similar Kibale Forest National Park. The diet was dominated by the fruit of four species and leaves of two species, although the composition of the diet varied from month to month, remaining diverse. Figs were consumed throughout much of the year, and in consequence, should perhaps be regarded as a staple, rather than fallback, food. A period of food scarcity was not apparent in this study and future comparative nutritional investigation will be required to determine whether these chimpanzees face a time of dietary hardship.     

Intravenous infusion of glucagon-like peptide-1 potently inhibits food intake, sham feeding, and gastric emptying in rats

Glucagon-like peptide-1(7-36)-amide (GLP-1) is postulated to act as a hormonal signal from gut to brain to inhibit food intake and gastric emptying. A mixed-nutrient meal produces a 2 to 3-h increase in plasma GLP-1. We determined the effects of intravenous infusions of GLP-1 on food intake, sham feeding, and gastric emptying in rats to assess whether GLP-1 inhibits food intake, in part, by slowing gastric emptying. A 3-h intravenous infusion of GLP-1 (0.5-170 pmol.kg(-1).min(-1)) at dark onset dose-dependently inhibited food intake in rats that were normally fed with a potency (mean effective dose) and efficacy (maximal % inhibition) of 23 pmol.kg(-1).min(-1) and 82%, respectively. Similar total doses of GLP-1 administered over a 15-min period were less potent and effective. In gastric emptying experiments, GLP-1 (1.7-50 pmol.kg(-1).min(-1)) dose-dependently inhibited gastric emptying of saline and ingested chow with potencies of 18 and 6 pmol.kg(-1).min(-1) and maximal inhibitions of 74 and 83%, respectively. In sham-feeding experiments, GLP-1 (5-50 pmol.kg(-1).min(-1)) dose-dependently reduced 15% aqueous sucrose intake in a similar manner when gastric cannulas were closed (real feeding) and open (sham feeding). These results demonstrate that intravenous infusions of GLP-1 dose-dependently inhibit food intake, sham feeding, and gastric emptying with a similar potency and efficacy. Thus GLP-1 may inhibit food intake in part by reducing gastric emptying, yet can also inhibit food intake independently of its action to reduce gastric emptying. It remains to be determined whether intravenous doses of GLP-1 that reproduce postprandial increases in plasma GLP-1 are sufficient to inhibit food intake and gastric emptying.