Systematic review of statistical approaches to quantify, or correct for, measurement error in a continuous exposure in nutritional epidemiology

BackgroundSeveral statistical approaches have been proposed to assess and correct for exposure measurement error. We aimed to provide a critical overview of the most common approaches used in nutritional epidemiology.MethodsMEDLINE, EMBASE, BIOSIS and CINAHL were searched for reports published in English up to May 2016 in order to ascertain studies that described methods aimed to quantify and/or correct for measurement error for a continuous exposure in nutritional epidemiology using a calibration study.ResultsWe identified 126 studies, 43 of which described statistical methods and 83 that applied any of these methods to a real dataset. The statistical approaches in the eligible studies were grouped into: a) approaches to quantify the relationship between different dietary assessment instruments and “true intake”, which were mostly based on correlation analysis and the method of triads; b) approaches to adjust point and interval estimates of diet-disease associations for measurement error, mostly based on regression calibration analysis and its extensions. Two approaches (multiple imputation and moment reconstruction) were identified that can deal with differential measurement error.ConclusionsFor regression calibration, the most common approach to correct for measurement error used in nutritional epidemiology, it is crucial to ensure that its assumptions and requirements are fully met. Analyses that investigate the impact of departures from the classical measurement error model on regression calibration estimates can be helpful to researchers in interpreting their findings. With regard to the possible use of alternative methods when regression calibration is not appropriate, the choice of method should depend on the measurement error model assumed, the availability of suitable calibration study data and the potential for bias due to violation of the classical measurement error model assumptions. On the basis of this review, we provide some practical advice for the use of methods to assess and adjust for measurement error in nutritional epidemiology.

[1]  H. Boshuizen,et al.  Evaluation of a two‐part regression calibration to adjust for dietary exposure measurement error in the Cox proportional hazards model: A simulation study , 2016, Biometrical journal. Biometrische Zeitschrift.

[2]  B. Zemel,et al.  Reproducibility and intermethod reliability of a calcium food frequency questionnaire for use in Hispanic, non-Hispanic Black, and non-Hispanic White youth. , 2015, Journal of the Academy of Nutrition and Dietetics.

[3]  H Boeing,et al.  Validation of a self-administered food-frequency questionnaire administered in the European Prospective Investigation into Cancer and Nutrition (EPIC) Study: comparison of energy, protein, and macronutrient intakes estimated with the doubly labeled water, urinary nitrogen, and repeated 24-h dietary , 1999, The American journal of clinical nutrition.

[4]  D. Stram,et al.  Regression calibration when foods (measured with error) are the variables of interest: markedly non-Gaussian data with many zeroes. , 2012, American journal of epidemiology.

[5]  R. Prentice,et al.  Biomarker-calibrated Energy and Protein Consumption and Cardiovascular Disease Risk Among Postmenopausal Women , 2011, Epidemiology.

[6]  Victor Kipnis,et al.  Dealing with dietary measurement error in nutritional cohort studies. , 2011, Journal of the National Cancer Institute.

[7]  Bernard Rosner,et al.  Optimal allocation of resources in a biomarker setting , 2015, Statistics in medicine.

[8]  D. Stram,et al.  Dietary assessment in the California Teachers Study: reproducibility and validity , 2008, Cancer Causes & Control.

[9]  S. Bingham,et al.  Biomarkers in nutritional epidemiology: applications, needs and new horizons , 2009, Human Genetics.

[10]  A. Phillips,et al.  The design of prospective epidemiological studies: more subjects or better measurements? , 1993, Journal of clinical epidemiology.

[11]  M. Nelson 8. The validation of dietary assessment , 1997 .

[12]  Miguel A. Padilla,et al.  Correlation Attenuation Due to Measurement Error , 2012 .

[13]  Raymond J Carroll,et al.  A comparison of a food frequency questionnaire with a 24-hour recall for use in an epidemiological cohort study: results from the biomarker-based Observing Protein and Energy Nutrition (OPEN) study. , 2003, International journal of epidemiology.

[14]  Donna Spiegelman,et al.  Approaches to uncertainty in exposure assessment in environmental epidemiology. , 2010, Annual review of public health.

[15]  D Spiegelman,et al.  Measurement error correction for logistic regression models with an "alloyed gold standard". , 1997, American journal of epidemiology.

[16]  Raymond J Carroll,et al.  Intake_epis_food(): An R Function for Fitting a Bivariate Nonlinear Measurement Error Model to Estimate Usual and Energy Intake for Episodically Consumed Foods. , 2012, Journal of statistical software.

[17]  S. Thompson,et al.  Correcting for regression dilution bias: comparison of methods for a single predictor variable , 2000 .

[18]  J. DiNicolantonio,et al.  The questionable benefits of exchanging saturated fat with polyunsaturated fat. , 2014, Mayo Clinic proceedings.

[19]  Petter Laake,et al.  Sensitivity of regression calibration to non‐perfect validation data with application to the Norwegian Women and Cancer Study , 2015, Statistics in medicine.

[20]  A Trichopoulou,et al.  Reproducibility and relative validity of an extensive semi-quantitative food frequency questionnaire using dietary records and biochemical markers among Greek schoolteachers. , 1997, International journal of epidemiology.

[21]  Jay S Kaufman,et al.  Measurement error adjustment in essential fatty acid intake from a food frequency questionnaire: alternative approaches and methods , 2007, BMC medical research methodology.

[22]  M C Ocké,et al.  Biochemical markers as additional measurements in dietary validity studies: application of the method of triads with examples from the European Prospective Investigation into Cancer and Nutrition. , 1997, The American journal of clinical nutrition.

[23]  W. Willett,et al.  An overview of issues related to the correction of non-differential exposure measurement error in epidemiologic studies. , 1989, Statistics in medicine.

[24]  C. Astre,et al.  Validation of a food-frequency questionnaire using multiple-day records and biochemical markers: application of the triads method. , 2000, Journal of epidemiology and biostatistics.

[25]  Gary E Fraser,et al.  Correlations between estimated and true dietary intakes: using two instrumental variables. , 2005, Annals of epidemiology.

[26]  D. Altman,et al.  STATISTICAL METHODS FOR ASSESSING AGREEMENT BETWEEN TWO METHODS OF CLINICAL MEASUREMENT , 1986, The Lancet.

[27]  Raymond J Carroll,et al.  A comparison of regression calibration, moment reconstruction and imputation for adjusting for covariate measurement error in regression , 2008, Statistics in medicine.

[28]  D. Moher,et al.  Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. , 2010, International journal of surgery.

[29]  S. Stewart,et al.  Reliability and Validity of an Assessment of Usual Phytoestrogen Consumption (United States) , 2006, Cancer Causes & Control.

[30]  R J Carroll,et al.  Measurement error and dietary intake. , 1998, Advances in experimental medicine and biology.

[31]  Donna Spiegelman,et al.  American Journal of Epidemiology Practice of Epidemiology Application of a Repeat-measure Biomarker Measurement Error Model to 2 Validation Studies: Examination of the Effect of Within-person Variation in Biomarker Measurements , 2022 .

[32]  Nina Teicholz,et al.  The scientific report guiding the US dietary guidelines: is it scientific? , 2015, BMJ : British Medical Journal.

[33]  D O Stram,et al.  Cost-efficient design of a diet validation study. , 1995, American journal of epidemiology.

[34]  Ruth H. Keogh,et al.  Allowing for never and episodic consumers when correcting for error in food record measurements of dietary intake , 2011, Biostatistics.

[35]  H. Vorster,et al.  A culture-sensitive quantitative food frequency questionnaire used in an African population: 1. Development and reproducibility , 2001, Public Health Nutrition.

[36]  G. Davey Smith,et al.  Reproducibility measures and their effect on diet–cancer associations in the Boyd Orr cohort , 2007, Journal of Epidemiology and Community Health.

[37]  R J Carroll,et al.  Implications of a new dietary measurement error model for estimation of relative risk: application to four calibration studies. , 1999, American journal of epidemiology.

[38]  M. C. Busstra,et al.  Comparison of approaches to correct intake–health associations for FFQ measurement error using a duplicate recovery biomarker and a duplicate 24 h dietary recall as reference method , 2014, Public Health Nutrition.

[39]  G. Fraser,et al.  A multivariate method for measurement error correction using pairs of concentration biomarkers. , 2007, Annals of epidemiology.

[40]  D Spiegelman,et al.  Application of the method of triads to evaluate the performance of food frequency questionnaires and biomarkers as indicators of long-term dietary intake. , 2001, American journal of epidemiology.

[41]  C. Wild,et al.  The exposome: from concept to utility. , 2012, International journal of epidemiology.

[42]  L. Ovesen,et al.  Selection of methodology to assess food intake , 2002, European Journal of Clinical Nutrition.

[43]  Renata Tiene de Carvalho Yokota,et al.  Applying the triads method in the validation of dietary intake using biomarkers. , 2010, Cadernos de saude publica.

[44]  H Boeing,et al.  Nutritional epidemiology: New perspectives for understanding the diet-disease relationship? , 2013, European Journal of Clinical Nutrition.

[45]  E Riboli,et al.  Estimating the accuracy of dietary questionnaire assessments: validation in terms of structural equation models. , 1994, Statistics in medicine.

[46]  D O Stram,et al.  Regression calibration in studies with correlated variables measured with error. , 2001, American journal of epidemiology.

[47]  Raymond J Carroll,et al.  Structure of dietary measurement error: results of the OPEN biomarker study. , 2003, American journal of epidemiology.

[48]  Raymond J Carroll,et al.  A New Method for Dealing with Measurement Error in Explanatory Variables of Regression Models , 2004, Biometrics.

[49]  D. Hall Measurement Error in Nonlinear Models: A Modern Perspective , 2008 .

[50]  R. Carroll,et al.  Statistical design of calibration studies. , 1997, American Journal of Clinical Nutrition.

[51]  D. Ruppert,et al.  Measurement Error in Nonlinear Models , 1995 .

[52]  E. Riboli,et al.  Invited commentary: the challenge of multi-center cohort studies in the search for diet and cancer links. , 2000, American journal of epidemiology.

[53]  T R Holford,et al.  Study design for epidemiologic studies with measurement error , 1995, Statistical methods in medical research.

[54]  E Riboli,et al.  Biochemical markers of dietary intake. , 1997, IARC scientific publications.

[55]  D. Bennett,et al.  Study protocol: the empirical investigation of methods to correct for measurement error in biobanks with dietary assessment , 2011, BMC medical research methodology.

[56]  S. McNaughton,et al.  Validation of a FFQ to estimate the intake of PUFA using plasma phospholipid fatty acids and weighed foods records , 2007, British Journal of Nutrition.

[57]  Gary E Fraser,et al.  Correlations between estimated and true dietary intakes. , 2004, Annals of epidemiology.

[58]  I. White,et al.  A toolkit for measurement error correction, with a focus on nutritional epidemiology , 2014, Statistics in medicine.

[59]  M Y Wong,et al.  Measurement error in epidemiology: the design of validation studies II: bivariate situation. , 1999, Statistics in medicine.

[60]  R. Kaaks,et al.  Biochemical markers as additional measurements in studies of the accuracy of dietary questionnaire measurements: conceptual issues. , 1997, The American journal of clinical nutrition.

[61]  W Willett,et al.  Total energy intake: implications for epidemiologic analyses. , 1986, American journal of epidemiology.

[62]  A Hofman,et al.  Dietary assessment in the elderly: validation of a semiquantitative food frequency questionnaire , 1998, European Journal of Clinical Nutrition.

[63]  R J Carroll,et al.  Empirical evidence of correlated biases in dietary assessment instruments and its implications. , 2001, American journal of epidemiology.

[64]  B Rosner,et al.  Correction of logistic regression relative risk estimates and confidence intervals for measurement error: the case of multiple covariates measured with error. , 1990, American journal of epidemiology.

[65]  W. Willett,et al.  Interval estimates for correlation coefficients corrected for within-person variation: implications for study design and hypothesis testing. , 1988, American journal of epidemiology.

[66]  James R Hebert,et al.  Urinary excretion of dithiocarbamates and self-reported Cruciferous vegetable intake: application of the ‘method of triads’ to a food-specific biomarker , 2002, Public Health Nutrition.

[67]  Amy F Subar,et al.  Carotenoid and tocopherol estimates from the NCI diet history questionnaire are valid compared with multiple recalls and serum biomarkers. , 2006, The Journal of nutrition.

[68]  Raymond J Carroll,et al.  Modeling Data with Excess Zeros and Measurement Error: Application to Evaluating Relationships between Episodically Consumed Foods and Health Outcomes , 2009, Biometrics.

[69]  R. Prentice,et al.  Calibration of Self-Reported Dietary Measures Using Biomarkers: An Approach to Enhancing Nutritional Epidemiology Reliability , 2013, Current Atherosclerosis Reports.

[70]  D Spiegelman,et al.  Correlated errors in biased surrogates: study designs and methods for measurement error correction , 2005, Statistics in medicine.

[71]  A. Green,et al.  Validation of a food-frequency questionnaire assessment of carotenoid and vitamin E intake using weighed food records and plasma biomarkers: The method of triads model , 2005, European Journal of Clinical Nutrition.

[72]  M. Singer,et al.  Nutritional Epidemiology , 2020, Definitions.

[73]  Ian R White,et al.  Using surrogate biomarkers to improve measurement error models in nutritional epidemiology , 2013, Statistics in medicine.

[74]  D. Midthune,et al.  Re: "Application of a repeat-measure biomarker measurement error model to 2 validation studies: examination of the effect of within-person variation in biomarker measurements". , 2012, American journal of epidemiology.

[75]  C. Guest Design Concepts in Nutritional Epidemiology , 1992 .

[76]  E. Riboli,et al.  Sample size requirements for calibration studies of dietary intake measurements in prospective cohort investigations. , 1995, American journal of epidemiology.

[77]  M. Kenward,et al.  Multiple imputation for missing data in epidemiological and clinical research: potential and pitfalls , 2009, BMJ : British Medical Journal.

[78]  B Rosner,et al.  Correction of logistic regression relative risk estimates and confidence intervals for random within-person measurement error. , 1992, American journal of epidemiology.

[79]  R J Carroll,et al.  Estimating the relation between dietary intake obtained from a food frequency questionnaire and true average intake. , 1991, American journal of epidemiology.

[80]  J. A. Harris ON THE CALCULATION OF INTRA-CLASS AND INTER-CLASS COEFFICIENTS OF CORRELATION FROM CLASS MOMENTS WHEN THE NUMBER OF POSSIBLE COMBINATIONS IS LARGE , 1913 .

[81]  B Rosner,et al.  Regression calibration method for correcting measurement-error bias in nutritional epidemiology. , 1997, The American journal of clinical nutrition.

[82]  Walter C Willett,et al.  Understanding nutritional epidemiology and its role in policy. , 2015, Advances in nutrition.

[83]  R. Carroll,et al.  A new statistical method for estimating the usual intake of episodically consumed foods with application to their distribution. , 2006, Journal of the American Dietetic Association.

[84]  D. Midthune,et al.  Statistical methods for estimating usual intake of nutrients and foods: a review of the theory. , 2006, Journal of the American Dietetic Association.

[85]  L. Leemis Applied Linear Regression Models , 1991 .

[86]  N. Day,et al.  Measurement error in epidemiology: the design of validation studies I: univariate situation. , 1999, Statistics in medicine.

[87]  A. Schatzkin,et al.  Abandon neither the Food Frequency Questionnaire nor the Dietary Fat-Breast Cancer Hypothesis , 2007, Cancer Epidemiology, Biomarkers and Prevention.

[88]  A F Subar,et al.  Design and serendipity in establishing a large cohort with wide dietary intake distributions : the National Institutes of Health-American Association of Retired Persons Diet and Health Study. , 2001, American journal of epidemiology.

[89]  W. Sauerbrei,et al.  STRengthening Analytical Thinking for Observational Studies: the STRATOS initiative , 2014, Statistics in medicine.

[90]  Annamaria Guolo,et al.  Robust techniques for measurement error correction: a review , 2008, Statistical methods in medical research.

[91]  R. Carroll,et al.  Performance of a food-frequency questionnaire in the US NIH–AARP (National Institutes of Health–American Association of Retired Persons) Diet and Health Study , 2008, Public Health Nutrition.

[92]  J M Bland,et al.  Statistical methods for assessing agreement between two methods of clinical measurement , 1986 .

[93]  L. Freedman,et al.  Design aspects of calibration studies in nutrition, with analysis of missing data in linear measurement error models. , 1997, Biometrics.

[94]  Bernard Rosner,et al.  Measurement error correction for nutritional exposures with correlated measurement error: Use of the method of triads in a longitudinal setting , 2008, Statistics in medicine.

[95]  C. Wild Complementing the Genome with an “Exposome”: The Outstanding Challenge of Environmental Exposure Measurement in Molecular Epidemiology , 2005, Cancer Epidemiology Biomarkers & Prevention.

[96]  M Blettner,et al.  Measurement error correction using validation data: a review of methods and their applicability in case-control studies , 2000, Statistical methods in medical research.

[97]  Sandra C Fuchs,et al.  Handling random errors and biases in methods used for short-term dietary assessment , 2014, Revista de saude publica.

[98]  Cristián Zegers Ariztía,et al.  Manual , 2002 .

[99]  Yi Li,et al.  Survival Analysis with Error‐Prone Time‐Varying Covariates: A Risk Set Calibration Approach , 2011, Biometrics.

[100]  B Rosner,et al.  Correction of logistic regression relative risk estimates and confidence intervals for systematic within-person measurement error. , 2006, Statistics in medicine.