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European Journal of Clinical (2013) 67, 424–429 & 2013 Macmillan Publishers Limited All rights reserved 0954-3007/13 www..com/ejcn

REVIEW Nutritional : New perspectives for understanding the - relationship?

H Boeing

Nutritional epidemiology is a subdiscipline of epidemiology and provides specific knowledge to nutritional . It provides data about the diet-disease relationships that is transformed by Public Nutrition into the practise of prevention. The specific contributions of include dietary assessment, description of nutritional exposure and statistical modelling of the diet-disease relationship. In all these areas, substantial progress has been made over the last years and is described in this article. Dietary assessment is moving away from the frequency questionnaire (FFQ) as main dietary assessment instrument in large-scale epidemiological studies towards the use of short-term quantitative instruments due to the potential of gross measurement errors. Web-based instruments for self-administration are therefore evaluated of being able to replace the costly interviewer conducted 24-h-recalls. Much interest is also directed towards the technique of taking and analysing photographs of all ingested, which might improve the dietary assessment in terms of precision. The description of nutritional exposure could greatly benefit from standardisation of the coding of across studies in order to improve comparability. For the investigations of bioactive substances as reflecting nutritional intake and status, the investigation of concentration measurements in body fluids as potential biomarkers will benefit from the new high-throughput of mass spectrometry. Statistical modelling of the dietary data and the diet-disease relationships can refer to complex programmes that convert quantitative short-term measurements into habitual intakes of individuals and correct for the errors in the estimates of the diet-disease relationships by taking data from validation studies with biomarkers into account. For dietary data, substitution modelling should be preferred over simple adding modelling. More attention should also be put on the investigation of non-linear relationships. The increasing complexity of the conduct and analysis of nutritional epidemiological studies is calling for a distinct and advanced training programme for the young scientists moving into this area. This will also guarantee that in the future an increasing number of high- level manuscripts will show up in this and other journals in respect of nutritional epidemiological topics.

European Journal of (2013) 67, 424–429; doi:10.1038/ejcn.2013.47; published online 27 February 2013 Keywords: epidemiology; dietary assessment; statistical modelling; measurement error; nutrition

INTRODUCTION specific knowledge to this scientific field. The field of nutritional Nutritional epidemiology could be regarded as a subdiscipline of epidemiology has evolved since the 1980s from a small speciality epidemiology, which provides a specific expertise that is also an towards a major contributor to science. Nowadays, study results integral part of nutritional . As a subdiscipline of from the many epidemiological studies with dietary data including epidemiology, the overall definition of epidemiology will also cross-sectional nutritional surveys form a large body of publica- hold for nutritional epidemiology. The scientific discipline of tions of this journal. Likewise, in other nutritional journals original epidemiology is defined according to one of the grandfathers of publications in the area of nutritional epidemiology also form a this discipline in the 1970s, Abraham Lilienfeld, in his book large part of the articles. Together with molecular nutrition, ‘Foundations of Epidemiology’ as follows:1 ‘The study of the , and nutritional medicine, nutritional distribution of a disease or a physiological condition in epidemiology can be considered as a major subdiscipline of and of the factors which influence this distribution’. nutritional sciences. Nutrition further represents the Regarding to this definition, nutritional epidemiology is dealing discipline that converts this knowledge into practise. with nutritional exposures and their roles for the occurrence of For the regular readers of scientific journals with interest in diet and impaired health conditions. The assessment of these and nutrition, it is not easy to follow all the articles dealing with exposures and the proper investigation of the link between the relation between nutritional exposures and health risks. Many exposure and end points form therefore the core activities of nutritional epidemiological articles address questions that are nutritional epidemiology. specific for end points ordered according to medical subjects such The establishment of the relations between dietary exposures as endocrinology, cardiology and oncology. However, all of this and fully established diseases, non-clinical intermediate end more subject-related original research uses the research concepts points and impaired health conditions are important information that form the basis of nutritional epidemiology. This includes the that also constitute the scientific knowledge of nutritional areas of dietary assessment, description of nutritional exposure sciences. Many disciplines contribute with their approaches and and statistical modelling of the diet-disease relationship. Some of

Department of Epidemiology, German Institute of Potsdam-Rehbruecke, Nuthetal, Germany. Correspondence: Professor Dr H Boeing, Department of Epidemiology, German Institute of Human Nutrition Potsdam-Rehbruecke, Arthur Scheunert Allee 114-116, Nuthetal 14558, Germany. E-mail: [email protected] Received 3 January 2013; accepted 8 January 2013; published online 27 February 2013 Nutritional epidemiology H Boeing 425 them can be considered as unique contributions to nutritional The statistical framework to identify and quantify measurement sciences and . error of the FFQ had been further extended to the inclusion of In nutritional epidemiology substantial progress has been biomarkers.13,14 The use of biomarker information has the achieved over the last years. Compared with the practise in advantage that the random errors between self-reports of diet nutritional epidemiology during the 1990s and the first 10 years of and objective measurements can be assumed to be zero. the new century, new approaches are gaining grounds. It seems as Otherwise, the random error between self-reporting instruments if a change of paradigm in how to conduct nutritional epidemio- such as FFQ and 24-h-recalls is usually correlated and needs to be logical studies, will take place in the near future. estimated. This might lead to unidentifiable measurement error Therefore, these new developments are described regarding models. The optimal design to identify the extent of measurement the basis of nutritional epidemiology with the aim to improve the error in connection with FFQs is a subgroup study within the study manuscripts in this area for the future. These new developments , including repeated measurements of all dietary can often only be understood in the context of the historical assessment instruments and biological material as well. background. In light of the FFQ or similar instruments such as dietary histories as prime assessment instrument in nearly all long-term studies established between 1980 and 2010, the question of DIETARY ASSESSMENT measurement error when using such instruments is highly Dietary assessment in the early prospective epidemiological significant. Measurement error is distorting the estimate of studies in the 1950s and 1960s focused mostly on cardiovascular and thus would lead to improper conclusion regarding risk factors and often included several thousands of study the diet-disease relationship per unit of intake or across the whole participants. It used either the method of food recording or the range of intake if non-linear models are taken. Particularly so-called Burke method that added to the recording method important is the loss of power to detect existing true relationships, interviewer-guided based questions of habitual intake.2 With which would result in an increased chance of false negative results the advancement of the computer capabilities in the1980s, the in studies with small power.15 But not only the estimate of relative application of retrospective self-administered dietary assessment risk is distorted by measurement error but also descriptive data instruments, the so-called semi-quantitative food frequency about dietary intake and their relation to -style and questionnaire (FFQ) method, became popular. This instrument environmental data contain a . In this regard there is a lot of asked for a limited number of habitual food intakes and was interest on the quantitative amount of measurement error with considered as superior to actual recording due to the the use of this type of instrument. Usually, the correlation between retrospective nature covering a longer time period.3 the FFQ information and the reference data are in the order of The semi-quantitative FFQ became the prime dietary assess- moderate to good.16 The correlation coefficients are usually better ment instrument in large-scale epidemiological studies due to its if the variance of the assessment has been removed by easy application and reduced time burden for the study staff as energy adjustment (4; see below). However, the most recent well as for the participant. With the introduction of this dietary validation studies of the FFQ with a reference instrument and assessment instrument, also the concept of validation of the objective biomarker information revealed a less optimistic picture dietary instruments has been implemented as the new instrument taking energy and as example. Particularly, the NCI funded was not aiming at the total diet but only for certain important OPEN study attracted a lot of interest for their advanced statistical aspects of dietary intake. The initial idea beyond the concept of and less promising results.17,18 validation was to show that the FFQ has sufficient accuracy and is In light of the results of the validation studies with FFQs, a able to estimate the dietary variable of interest to a certain extent debate started whether measurement error and insufficient compared with a reference method capturing total diet.4 In the performance of the FFQ would have masked important diet- early validation studies of FFQs data from food, records were used disease relationships in the large-scale cohort studies conducted as the reference following the tradition since the 1950s.5 However, so far.19 The new generation of large-scale epidemiological studies the coding of a food record turned out to be time consuming. would therefore need to improve the quality of the dietary data Therefore, some groups proposed the 24-h recall method as substantially. There are several options to be discussed. One alternative to a food record for validation by taking up some ideas option is the use of the reference methods in addition to the FFQ. proposed by Burke.2 This interviewer conducted instrument The reference methods such as 24-h-recalls or food records reflect requests for the consumption of foods of the previous day in total dietary intake and are short-term instruments. For a proper detail. The conduct of the interview through a trained interviewer estimate of the diet of an individual several days need to be can be further standardised through computer programmes that covered. The key statistical feature is the intra-individual variation also include probing questions regarding potentially missed of the dietary exposure between days. Statistical calculations occasions and foods and a detailed food list.6 Compared suggest between 2–4 days for frequently eaten foods and up to 6 with a food record, an unannounced conducted 24-recall is non- days for less often eaten foods.20 reactive regarding study specific food choices. Further, it turned Another option is the use of innovative application of traditional out that a 24-h-recall did not need to be done face to face, but instruments via the internet. These instruments have to be tailored could also be done by telephone with the same quality.7,8 Thus, for self-administration, which might result in less precision and compared with food records, the effort is reduced to apply less compared with the interviewer conducted methods. measurements of the complete diet in larger populations. Web-based tools for self-administering 24-h-recalls are already The statistical approach of validation of the FFQ was further available and under further investigation.21 Other groups already refined with the aim to calibrate the dietary data and to correct organised the complete with dietary assessment by the estimate of the relative risk for the measurement error.9 The web-based techniques.22 The critical issue is the validity of the proposed design was the conduct of a validation study in a web-based approach for self-administration compared with subgroup of the cohort population with multiple days of the interviewer approach forming currently the reference recording respective interviews.10,11 In the multi-centric EPIC- method. The overall philosophy of the application of the study, only one 24-h-recall was conducted in a subgroup of the instruments developed so far is based on the insight, that each study sample (about 8% of the total sample).12 Later, it was type of dietary assessment instrument provides specific revealed that the calibration formula in a situation of one FFQ and information. This information can further be used by complex one 24-h-recall has limitations, compared with the situation of two statistical algorithms to calculate the best estimate of habitual and more 24-h-recalls per person.10 dietary exposures for each study subject from FFQ and reference

& 2013 Macmillan Publishers Limited European Journal of Clinical Nutrition (2013) 424 – 429 Nutritional epidemiology H Boeing 426 data.20 As a consequence, the best estimates for each study Efforts had also been undertaken during the last years to extend subject will also form the intake distribution of that study. existing databases towards bioactive compounds in Precisely estimated dietary intake values favour the calculation of addition to and to apply this knowledge in studies the relative risk on the continuous scale instead of using ranking assessing the intakes. Thus, intake of i.a. carotenoids, flavonoids, procedures such as quantiles (see below). phenols and phytoestrogens can nowadays be calculated by A further and not yet fully developed option to improve dietary combining food code systems and specific nutrient databases.28 assessment is the application of a new technique that is based on However, it needs to be discussed whether the calculation of the use of mobile phones.23 Mobile phone pictures of all foods dietary intakes of nutrients and other bioactive compounds by the consumed can be taken and transmitted to a server, which assessment of food intake will provide the information that is contains recognition programmes allowing a computerised required to judge the impact of a bioactive compound on disease analysis regarding type of food and amount. This technique is risk. One disadvantage of the approach is the variation of still under development but might be the tool of the future due to concentrations of food compounds within the foods. Usually, a the low cost of conduct compared with interviews. In addition, nutrient table makes use of the mean concentration in a food and with this technique the amounts of foods being eaten can be not of the variation. Another disadvantage of the approach is the estimated with a still unreached precision. fact that intake does not directly reflect the internal dose as it does not consider of the nutrients. The internal dose of a bioactive substance seems to be the most biologically important information, and the most relevant for disease risk. ESTIMATE OF NUTRITIONAL EXPOSURE Inter-individual variation of resorption and transportation of the The dietary assessment instruments provide data on food intake compounds due to genetic predisposition and the influence of and, if wanted, data on supplement use. The type of information other dietary compounds is considered by this approach which is about a food could be obtained in a written manner by food not been considered by the dietary approach. records or requested by interviewers in 24-h-recalls. Depending on Direct measurements of these bioactive compounds in body the instrument, the requested details regarding a food could be fluids consist therefore of the alternative approach compared with variable, such as content, type of packaging, the calculations of intake from food use and nutrient tables. The procedures, and often the brand name. Thus, the coding of such biomarker approach is also independent from the information on foods will pose a challenge. It is estimated that at a particular foods and their role in providing nutrients. Some foods or food point of time about 200 000 commercial foods are available in the groups are important sources not only for one bioactive supermarkets in western societies. Bar code readings of the labels compound, but often for many of them. Thus, it seems nearly of the commercial foods might help in some situations to handle impossible in many instances to distinguish statistically between the detailed information. In some areas such as the European the impact of a food and its major compounds on disease risk. Union, each commercial food has a specific label and some details The use of human biomaterials to characterise and differentiate of the food are available in a database. In general, all foods a study population regarding a specific nutritional exposure has estimated in a study must be assigned a food code and have to be therefore attracted a lot of attention. Research on nutritional integrated into a food code system. Food code systems do not biomarkers has been conducted for a long time, but a break only provide a hierarchical ordering of the foods but also the through was not obtained so far. Still, the traditional nutritional connection to nutrient databases. The number of main food biomarkers are dominating the discussion and only a few groups is usually in the order of 15–20 in such food code systems. biomarkers could be added over the last years.29 Nonetheless, About 40–50 food subgroups usually form the next level within the measurement of concentrations of particularly bioactive the hierarchical food code. Main food and 1st order subgroup compounds in body fluids had been conducted repeatedly in foods are often used for investigating risk relations.24 The use of a epidemiological studies and has added to our understanding of more detailed food code beyond the 1st order subgroups in risk the role of diet on disease risk.30,31 analyses is usually restricted to specific hypotheses, for example, Research on biomarkers for nutritional intake, however, is investigations of a food having a high concentration of a specific ongoing and will hopefully generate substantial progress in the plant component. near future. In particular, there is a great demand for recovery Unfortunately, there is no world-wide common food coding biomarkers that directly help to validate dietary assessment system available for scientific use. Thus, study results on food instruments. A novel approach of detecting and using biomarkers group level and particular food subgroup level might not be for estimating specific dietary intakes and/or the relation to end directly comparable across studies partly because of a non- points has been proposed in connection with the recently standardised food grouping system. Particular questions that is, developed high-throughput of metabolomics.32 This regard the assignment of potatoes to the or staple technology based on mass spectrometry or nuclear magnetic group or nuts to the or as an own group. The detailed resonance spectroscopy provides quantitative information on the composition of a regarding specific foods across presence of hundreds to thousands of metabolites in fluids in one studies can thus widely differ and would hamper systematic run. It is speculated that each food, particular plant foods, will have reviews and meta-analyses in the interpretation. its own finger print of metabolites. First studies are underway that The need for standardisation of food tables25 with the prime link those fingerprints with the metabolites assessed in body fluids, aim to link this food table with a highly standardised and either or blood components.33 Metabolomics offers the very comparable nutrient database is well acknowledged in Europe. interesting perspective that by analysing body fluid information on The European Union has invested into this issue over the last years dietary intake can be derived. Further, these data can be used to by launching specific calls and by supporting collaborations. investigate the risk relation to end points. However, it is still not Particularly, the European Food Information Network definable in as much the biomarker approach, in general, will pushed for the standardisation of the national food tables to improve the estimate of the diet-disease relationship. create an uniform Pan-European food coding system, such as nutrient databases that are already available or being made available in the future.26 This development is important in view of STATISTICAL MODELLING OF THE DIET-DISEASE the development of a standardised 24-h-recall dietary assessment RELATIONSHIP instrument for all European countries for surveys and The FFQ as a semi-quantitative and usually biased instrument epidemiological studies.27 favoured the expression of nutritional exposure as quantile after

European Journal of Clinical Nutrition (2013) 424 – 429 & 2013 Macmillan Publishers Limited Nutritional epidemiology H Boeing 427 ranking the study participants according to the estimated dietary Modelling strategies of the diet-disease relationship should exposure. The study participants were allocated to classes of further investigate non-linear relationships such as thresholds and intake, such as tertile, quartile of quintile and thereafter related to levelling off of effects. Regression models with one linear term per disease risk. It would be a mistake to label these quantiles with the exposure variable assume a linear relationship across the range of dietary estimates derived from the semi-quantitative instrument the invested variables if the continuous variable is modelled. In due to the measurement error. The better estimate of the principle, the non-linear risk modelling of dietary variables on a nutritional exposure within the FFQ-quantiles would be the continuous scale is preferred against the modelling of cate- average intake observed in the validation study for these subjects gories.41 Modelling the diet-disease relationship on a continuous estimated in the reference instrument.34 scale assumes that the range and distribution of dietary exposure This remark should direct the general interest to a common within the study population is properly assessed (see above). quality assurance system for published dietary intake values across There are several suggestions of modelling non-linear all the disciplines of . This means that given relationships. Most of them propose to add power terms to the quantities such as a gram of fat should reflect the same true modelling equation in addition to the linear term. For modelling amount whether being used in , human non-linear relationships on a continuous scale the most oftenly intervention studies or estimated in observational studies. used method is restricted cubic spline regression.42,43 In this Observational studies have—given the challenge of quality approach, knots are defined and the regression lines between the assurance—the problem that self-reports of diet might under- knots are modelled with simple, quadratic and cubic terms. The estimate true intake.7,35,36 Therefore, even well-conducted use of this technique requires the definition of a reference which epidemiological studies with several 24-HDRs might not provide could be different across studies. Other approaches include the the correct true intake values and their variation within the search for the best fit by using the fractional polynomial population. However, this type of measurement error in well- technique.44 This technique has been developed to provide the conducted studies seems to be small, compared with the most proper adjustment formula for a variable. By using this systematic bias usually observed for FFQs and other types of technique non-linear relations between dietary variables can be instruments aiming at measuring habitual diet directly. It should analysed and presented. be therefore the aim of nutritional epidemiology to present proper and comparable dietary data that can be immediately linked to nutritional knowledge generated in other fields. An important aspect of dietary intake assessment is to estimate true DISCUSSION intake distributions within the study population and to reduce Progress over the last years in the different fields of activities bias of the population estimates. Due to its feasibility in large forming the core of nutritional epidemiology will change the population studies, FFQs will continue to be selected as the main practise regarding dietary assessment, formation of dietary dietary assessment instrument, coupled with validation sub- variables and statistical modelling of the diet-disease relationship studies integrated into the data collection of the whole popu- in the future. Subsequently, also the current standard of study lation. Therefore, it will still be demand to integrate the infor- presentations will change. mation from the validation studies into the overall assessment of The most likely scenario of a well-conducted study in the future diet in a study population.37 will include the use of multiple short-term instruments for food An important question is the adjustment for energy when the intake preferentially applied via the web in a kind of method mix diet-disease relationship is modelled. Adjustment for energy coupled with complex statistical methods that calculate the best means to model an iso-caloric situation. Energy intake itself will estimate of habitual food intake of an individual. The food data will not be considered as important variable as energy intake is only be further corrected for measurement error using validation studies one of the components comprising the energy balance. At with biomarkers in subgroups integrated into the study. The thus constant body weight, energy intake of a subject reflects resting estimated food intake will be linked to extended food tables energy expenditure, physical activity and the individual metabolic allowing calculating the intake of nutrients and many bioactive capacity to utilise energy and macronutrients, but is not a variable compounds. The diet-disease relationship will be investigated with predicting energy balance respective weight change. When non-linear modelling using the quantitative values and substitution energy adjusted models are used to describe the diet-disease models with defined exchange relationships. relationship, the energy intake is assumed to be fixed and the It is the question how we can train the young scientists that increase or decrease of intake of a food or energy containing decide to be trained in the subject of nutritional epidemiology as nutrients can only be accomplished by the exchange of other a PhD student or young post-doc. It is obvious that the dietary variables. The most adequate modelling procedure with transformation of the newly developed approaches into a energy adjustment would be to run well-defined substitution standard practise will require a lot of training. Therefore, new models.38–40 Modelling the substitution of a dietary component students need an updated curriculum for advanced training that with another dietary component means to formulate the allow the new generation of students to go beyond the current modelling part in such a way that one dietary variable is practise. The curriculum needs to have at least a master’s level and replaced by another dietary variable, taking energy as the have to include basics in epidemiology and natural and medical common unit across the dietary factors. Substitution models sciences and advanced courses in the core fields forming that hold energy constant are only useful to be applied if the nutritional epidemiological sciences. Only the establishment of dietary variable contains energy, such as macronutrients or foods. specific training facilities for young sciences will allow to practice The application of substitution models, however, is in principle not the increasing complexity of the subject and to push for further restricted to holding energy constant. For example., in case of innovations. It is obvious that we need to establish new large scale foods, also the total amount of food can be hold constant and 1 g epidemiological studies that adopt the new ideas and provide the of a specific food exchanged with 1 g of another food. Substitution data that are necessary to address the still unsolved question of models will give a much better insight into the health implication the role of diet for disease risk. of changing a diet compared with models that assume a change It is the hope that efforts in training and adoption of the new also in energy intake or are unspecific regarding the replacement methods will also result in manuscripts that adopt the new of the dietary exposure. It could be shown, for example, that the methods and reflect up-to-date techniques. This will also be a increase of poultry consumption will not have an effect on risk of challenge for editors and reviewers for establishing a proper colorectal caner, but the replacement of red meat by poultry.40 procedure to filter the best papers out of the incoming

& 2013 Macmillan Publishers Limited European Journal of Clinical Nutrition (2013) 424 – 429 Nutritional epidemiology H Boeing 428 manuscripts and to present meaningful insights to the readers of generation (with better observation. Epidemiol Biomarkers Prev 2009; 18: this and other journals. 1026–1032. Nutrition is in addition to , tobacco smoking and physical 19 Schatzkin A, Kipnis V. Could exposure assessment problems give us activity still considered as one of the major driving forces wrong answers to nutrition and cancer questions? J Natl Cancer Inst 2004; 96: influencing and the occurrence of chronic diseases 1564–1565. in a population.45 By understanding major aspects of the diet- 20 Carroll RJ, Midthune D, Subar AF, Shumakovich M, Freedman LS, Thompson FE et disease relationship, the potential of prevention of chronic disease al. Taking advantage of the strengths of 2 different dietary assessment instru- can be better assessed and proper prevention measures develo- ments to improve intake estimates for nutritional epidemiology. Am J Epidemiol 2012; 175: 340–347. ped by the discipline of public health nutrition. In addition, 21 Subar AF, Kirkpatrick SI, Mittl B, Zimmerman TP, Thompson FE, Bingley C et al. The nutrition is deeply involved in all types of mechanisms that Automated Self-Administered 24-hour dietary recall (ASA24): a resource for constitute life. By shedding light on the diet-disease relationship researchers, clinicians, and educators from the National Cancer Institute. J Acad nutritional epidemiology helps to understand the enormous Nutr Diet 2012; 112: 1134–1137. complexity of life a little bit better. 22 Hercberg S. Web-based studies: The future in nutritional epidemiology (and overarching epidemiology) for the benefit of public health? Prev Med 2012; 55: 544–545. CONFLICT OF INTEREST 23 Daugherty BL, Schap TE, Ettienne-Gittens R, Zhu FM, Bosch M, Delp EJ et al. Novel technologies for assessing dietary intake: evaluating the usability of a The authors declare no conflict of interest. mobile telephone food record among adults and adolescents. J Med Internet Res 2012; 14: 58. 24 von Ruesten A, Feller S, Bergmann MM, Boeing H. Diet and risk of chronic REFERENCES diseases: Results from the first 8 years of follow-up in the EPIC-Potsdam 1 Lilienfeld AM. Foundations of Epidemiology. 1st edn, Oxford University press: study. Eur J Clin Nutr; e-pub ahead of print 6 February 2013; doi:10.1038/ New York, NY, USA, 1976. ejcn.2013.7. 2 Burke BS. The dietary history as a tool in research. J Am Diet Assoc 1947; 23: 25 Ireland JD, Møller A. Lanngual food description: a learning process. Eur J Clin Nutr 1041–1046. 2010; 64: S44–S48. 3 Rohan TE, Potter ID. Retrospective assessment of dietary intake. 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