Abstract
Background: Nutri-score is now widely available in food packages in Europe. Aim: To study the overall nutritional quality of the diet in relation to risks of Crohn's disease (CD) and ulcerative colitis (UC), in the European Prospective Investigation into Cancer and Nutrition (EPIC) cohort. Methods: We collected dietary data at baseline from validated food frequency questionnaires. We used a dietary index based on the UK Food Standards Agency modified nutrient profiling system (FSAm-NPS-DI) underlying the Nutri-Score label, to measure the nutritional quality of the diet. We estimated the association between FSAm-NPS-DI score, and CD and UC risks using Cox models stratified by centre, sex and age; and adjusted for smoking status, BMI, physical activity, energy intake, educational level and alcohol intake. Results: We included 394,255 participants (68.1% women; mean age at recruitment 52.1 years). After a mean follow-up of 13.6 years, there were 184 incident cases of CD and 459 incident cases of UC. Risk of CD was higher in those with a lower nutritional quality, that is higher FSAm-NPS-DI Score (fourth vs. first quartile: aHR: 2.04, 95% CI: 1.24–3.36; p-trend: <0.01). Among items of the FSAm-NPS-DI Score, low intakes of dietary fibre and fruits/vegetables/legumes/nuts were associated with higher risk of CD. Nutritional quality was not associated with risk of UC (fourth vs. first quartile of the FSAm-NPS-DI Score: aHR: 0.91, 95% CI: 0.69–1.21; p-trend: 0.76). Conclusions: A diet with low nutritional quality as measured by the FSAm-NPS-DI Score is associated with a higher risk of CD but not UC.
| Original language | English |
|---|---|
| Pages (from-to) | 558-568 |
| Number of pages | 11 |
| Journal | Alimentary Pharmacology and Therapeutics |
| Volume | 59 |
| Issue number | 4 |
| Early online date | 15 Dec 2023 |
| DOIs | |
| Publication status | Published - Feb 2024 |
Keywords
- dietary
- EPIC
- FSAm-NPS DI score
- inflammatory bowel disease
- nutri-score
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- 10.1111/apt.17835Licence: CC BY-NC
- Aliment Pharmacol Ther - 2023 - Meyer - Dietary index based on the Food Standards Agency nutrient profiling system and riskFinal published version, 744 KBLicence: CC BY-NC
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Dietary index based on the Food Standards Agency nutrient profiling system and risk of Crohn's disease and ulcerative colitis. / Meyer, Antoine; Dong, Catherine; Chan, Simon S. M.; Touvier, Mathilde; Julia, Chantal; Huybrechts, Inge; Nicolas, Geneviève; Oldenburg, Bas; Heath, Alicia K.; Tong, Tammy Y. N.; Key, Timothy J.; Tjønneland, Anne; Kyrø, Cecilie; Kaaks, Rudolf; Katzke, Verena A.; Bergman, Manuela M.; Palli, Domenico; Masala, Giovanna; Tumino, Rosario; Sacerdote, Carlotta; Colorado-Yohar, Sandra M.; Sánchez, Maria-Jose; Guevara, Marcela; Grip, Olof; Holmgren, Johanna; Cross, Amanda; Karling, Pontus; Hultdin, Johan; Murphy, Neil; Deschasaux-Tanguy, Mélanie; Hercberg, Serge; Galan, Pilar; Mahamat-Saleh, Yahya; Amiot, Aurélien; Gunter, Marc J.; Boutron-Ruault, Marie Christine; Carbonnel, Franck.
In: Alimentary Pharmacology and Therapeutics, Vol. 59, No. 4, 02.2024, p. 558-568.Research output: Contribution to journal › Article › peer-review
TY - JOUR
T1 - Dietary index based on the Food Standards Agency nutrient profiling system and risk of Crohn's disease and ulcerative colitis
AU - Meyer, Antoine
AU - Dong, Catherine
AU - Chan, Simon S. M.
AU - Touvier, Mathilde
AU - Julia, Chantal
AU - Huybrechts, Inge
AU - Nicolas, Geneviève
AU - Oldenburg, Bas
AU - Heath, Alicia K.
AU - Tong, Tammy Y. N.
AU - Key, Timothy J.
AU - Tjønneland, Anne
AU - Kyrø, Cecilie
AU - Kaaks, Rudolf
AU - Katzke, Verena A.
AU - Bergman, Manuela M.
AU - Palli, Domenico
AU - Masala, Giovanna
AU - Tumino, Rosario
AU - Sacerdote, Carlotta
AU - Colorado-Yohar, Sandra M.
AU - Sánchez, Maria-Jose
AU - Guevara, Marcela
AU - Grip, Olof
AU - Holmgren, Johanna
AU - Cross, Amanda
AU - Karling, Pontus
AU - Hultdin, Johan
AU - Murphy, Neil
AU - Deschasaux-Tanguy, Mélanie
AU - Hercberg, Serge
AU - Galan, Pilar
AU - Mahamat-Saleh, Yahya
AU - Amiot, Aurélien
AU - Gunter, Marc J.
AU - Boutron-Ruault, Marie Christine
AU - Carbonnel, Franck
N1 - Funding Information: This work was supported by the Sir Halley Stewart Trust, Crohn's and Colitis UK and The UK National Health Service Executive Eastern Region. The coordination of EPIC is financially supported by the International Agency for Research on Cancer (IARC) and also by the Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London which has additional infrastructure support provided by the NIHR Imperial Biomedical Research Centre (BRC).The national cohorts are supported by: Danish Cancer Society (Denmark); Ligue Contre le Cancer, Institut Gustave Roussy, Mutuelle Générale de l'Education Nationale, Institut National de la Santé et de la Recherche Médicale (INSERM) (France); German Cancer Aid, German Cancer Research Center (DKFZ), German Institute of Human Nutrition Potsdam-Rehbruecke (DIfE), Federal Ministry of Education and Research (BMBF) (Germany); Associazione Italiana per la Ricerca sul Cancro-AIRC-Italy, Compagnia di SanPaolo and National Research Council (Italy); Dutch Ministry of Public Health, Welfare and Sports (VWS), Netherlands Cancer Registry (NKR), LK Research Funds, Dutch Prevention Funds, Dutch ZON (Zorg Onderzoek Nederland), World Cancer Research Fund (WCRF), Statistics Netherlands (The Netherlands); Health Research Fund (FIS) – Instituto de Salud Carlos III (ISCIII), Regional Governments of Andalucía, Asturias, Basque Country, Murcia and Navarra, and the Catalan Institute of Oncology – ICO (Spain); Swedish Cancer Society, Swedish Research Council and County Councils of Skåne and Västerbotten (Sweden); Cancer Research UK (14136 to EPIC-Norfolk; C8221/A29017 to EPIC-Oxford), Medical Research Council (1000143 to EPIC-Norfolk; MR/M012190/1 to EPIC-Oxford) (United Kingdom). The funders had no role in the study design or in the collection, analysis, interpretation of data, writing of the report or decision to submit the article for publication. Associations between the FSAm-NPS DI Score and risks of CD/UC were estimated using Cox proportional hazards models to obtain Hazard Ratios (HR) and 95% confidence intervals (95% CI). Sex-specific quartiles of the FSAm-NPS DI Score were used, the lowest quartile (i.e. higher nutritional quality of the diet) serving as the reference category. Age was used as time scale, with exit time as age at diagnosis of CD/UC, at death, or at censoring date (last follow-up questionnaire retrieved or diagnosis of indeterminate colitis or microscopic colitis), whichever occurred first. For the analysis concerning CD, patients were censored when they were diagnosed with UC and vice versa. Models were stratified by centre and sex, and adjusted for smoking status (never, former or current smoker), BMI (<18.5, 18.5–24.9, 25.0–30.0, >30.0 kg/m2), physical activity (active, moderately active, moderately inactive, inactive), educational level (primary school, secondary school, university degree), energy intake except alcohol (quartiles) and alcohol intake at recruitment (quartiles). Linear trends were tested by using the median value for each category of the studied variables. The assumption of proportional hazards was assessed and confirmed using graphs based on the Schœnfeld residuals and Kolmogorov-type supremum tests. Under the missing at random hypothesis, multiple imputation by chained equations with five imputations was used to address the three covariates with missing data: smoking status (1.7% of missing data), educational level (3.7%) and physical activity (1.8%). We also modelled FSAm-NPS DI Score as sex-specific deciles, as a continuous variable, and using cubic natural splines with four knots. In addition, we performed subgroup analyses according to sex. We conducted analyses of specific items included in the computation of the FSAm-NPS DI Score: total energy intake, sugars, saturated fatty acids, total protein intake, dietary fibre and fruits/vegetables/legumes/nuts. Sensitivity analyses were performed: to assess potential reverse causality due to delayed IBD diagnosis by excluding the first 2 years of follow-up, and to assess misreporting of energy intake by excluding participants with implausible energy intake based on their basal metabolic rate and physical activity level (Goldberg method).15,16 We also conducted an additional analysis based on macronutrient categories (fat, protein, carbohydrates) to compare it to the analysis based on the FSAm-NPS DI Score on the risk of CD and UC. All tests were two-tailed with a limit of significance of p < 0.05. Analyses were performed with SAS® software version 9.4 (SAS Institute, North Carolina, USA). The EPIC study was approved by the ethical committees of the International Agency for Research on Cancer (IARC), and of all individual EPIC centres. The study data cannot be deposited publicly as these collaborative data originate from multiple research institutions across 8 European countries with different legal frameworks. Information on submitting applications to access the EPIC data can be made to https://epic.iarc.fr/access. The EPIC cohort was established in 1991 to investigate the role of dietary and lifestyle factors in various cancers and chronic diseases in middle-aged participants. EPIC includes about 520,000 men and women from 23 centres in 10 European countries (Denmark, France, Germany, Greece, Italy, the Netherlands, Norway, Spain, Sweden and the United Kingdom).12 Participants were prospectively included in the study between 1991 and 1999. Participants were recruited from the general population, except in France (women enrolled in a health insurance scheme for school and university employees), and Utrecht in the Netherlands (mammographic-screening program). In addition, half of the Oxford cohort in the United Kingdom consisted of non-meat eaters due to targeted oversampling of this group. The EPIC-IBD cohort is a subgroup of the EPIC cohort which includes EPIC centres which agreed to collect and certify new diagnoses of IBD which occurred after inclusion. The EPIC-IBD cohort includes 437,972 participants without IBD from eight European countries within the EPIC cohort (namely Denmark, France, Germany, Italy, the Netherlands, Spain, Sweden and the United Kingdom). Dietary data were collected at baseline using country- or centre-specific validated questionnaires (individual interviews or self-administered questionnaires). Food frequency questionnaires (FFQ) recorded average intakes of 98–2059 food items (depending on the centre) over the past 12 months, and enabled computation of individual mean intakes of foods or food groups in grams per day. Total energy and nutrient intakes were estimated by using the FFQs and the standardised EPIC Nutrient Database.13 Participants who did not complete dietary questionnaire or with implausible dietary intakes, namely within the lowest and highest 1% of the cohort distribution of the ratio of reported total energy intake over energy requirement, were excluded. The FSAm-NPS score (food level score) was computed based on the nutrient content for 100 g of foods or beverages (with the exception of alcoholic beverages that are beyond the scope of the nutrient profile). Up to 10 points were allocated for each nutrient that should be eaten in limited quantities, that is sugars (g), saturated fatty acids (g), sodium (mg), and energy (kJ) and up to 5 points were allocated for each nutrient that is recommended, that is dietary fibre (g) and protein (g) and for the proportion of vegetables, legumes, fruit and nuts (%) in the food. To obtain the FSAm-NPS score, the sum of points for nutrients that are recommended is then subtracted from the sum of points for nutrients that should be eaten in limited quantities. Therefore, the FSAm-NPS score for each food or beverage is based on a continuous scale ranging from −15 points (highest nutritional quality) to 40 points (lowest nutritional quality). Cut-offs are then applied to the FSAm-NPS score to derive the Nutri-Score. It should be noted that sodium intake has an incomplete reliability as it has not been initially recorded. The FSAm-NPS is a modified version of the original FSA-NPS initially developed by the British Food Standards Agency, with slight adaptations to the allocation of points for specific foods (beverages, cheese and added fats) recommended by the French High Council for Public Health to ensure a proper discrimination of the nutritional quality of products within these groups and a high consistency of the FSAm-NPS score with dietary guidelines (see Appendix S1). In a second step, the FSAm-NPS DI score was computed to characterise the nutritional quality of an individual's diet (individual level score). The FSAm-NPS DI score was obtained as the sum of FSAm-NPS scores for each consumed food or beverage multiplied by the amount of energy provided by this product, and divided by the total energy intake with the exception of alcoholic beverages.14 A higher FSAm-NPS DI score reflects an overall lower nutritional quality of the diet. Details on the FSAm-NPS DI score have been described elsewhere and are available in Appendix S1. Participants who developed incident IBD during follow-up were identified either by self-administered follow-up questionnaires or by national registries of cancers and chronic diseases, depending on centres. For each suspected case, local physicians ascertained the diagnosis of UC or CD by reviewing the medical, endoscopic, radiological and histological reports. Participants without follow-up after inclusion were excluded. Participants who developed indeterminate colitis or microscopic colitis were censored. At baseline, standardised self-administered questionnaires were applied across centres to record information on smoking, physical activity and educational level. Body mass indices (BMI) were calculated in kg/m2 from the participants' weights and heights measured at baseline except in France and Oxford (UK), where anthropometric data were self-reported at baseline and validated for a selected number of participants. Participants who did not complete lifestyle questionnaires were excluded. Associations between the FSAm-NPS DI Score and risks of CD/UC were estimated using Cox proportional hazards models to obtain Hazard Ratios (HR) and 95% confidence intervals (95% CI). Sex-specific quartiles of the FSAm-NPS DI Score were used, the lowest quartile (i.e. higher nutritional quality of the diet) serving as the reference category. Age was used as time scale, with exit time as age at diagnosis of CD/UC, at death, or at censoring date (last follow-up questionnaire retrieved or diagnosis of indeterminate colitis or microscopic colitis), whichever occurred first. For the analysis concerning CD, patients were censored when they were diagnosed with UC and vice versa. Models were stratified by centre and sex, and adjusted for smoking status (never, former or current smoker), BMI (<18.5, 18.5–24.9, 25.0–30.0, >30.0 kg/m2), physical activity (active, moderately active, moderately inactive, inactive), educational level (primary school, secondary school, university degree), energy intake except alcohol (quartiles) and alcohol intake at recruitment (quartiles). Linear trends were tested by using the median value for each category of the studied variables. The assumption of proportional hazards was assessed and confirmed using graphs based on the Schœnfeld residuals and Kolmogorov-type supremum tests. Under the missing at random hypothesis, multiple imputation by chained equations with five imputations was used to address the three covariates with missing data: smoking status (1.7% of missing data), educational level (3.7%) and physical activity (1.8%). We also modelled FSAm-NPS DI Score as sex-specific deciles, as a continuous variable, and using cubic natural splines with four knots. In addition, we performed subgroup analyses according to sex. We conducted analyses of specific items included in the computation of the FSAm-NPS DI Score: total energy intake, sugars, saturated fatty acids, total protein intake, dietary fibre and fruits/vegetables/legumes/nuts. Sensitivity analyses were performed: to assess potential reverse causality due to delayed IBD diagnosis by excluding the first 2 years of follow-up, and to assess misreporting of energy intake by excluding participants with implausible energy intake based on their basal metabolic rate and physical activity level (Goldberg method).15,16 We also conducted an additional analysis based on macronutrient categories (fat, protein, carbohydrates) to compare it to the analysis based on the FSAm-NPS DI Score on the risk of CD and UC. All tests were two-tailed with a limit of significance of p < 0.05. Analyses were performed with SAS® software version 9.4 (SAS Institute, North Carolina, USA). The EPIC study was approved by the ethical committees of the International Agency for Research on Cancer (IARC), and of all individual EPIC centres. The study data cannot be deposited publicly as these collaborative data originate from multiple research institutions across 8 European countries with different legal frameworks. Information on submitting applications to access the EPIC data can be made to https://epic.iarc.fr/access. Funding Information: This work was supported by the Sir Halley Stewart Trust, Crohn's and Colitis UK and The UK National Health Service Executive Eastern Region. The coordination of EPIC is financially supported by the International Agency for Research on Cancer (IARC) and also by the Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London which has additional infrastructure support provided by the NIHR Imperial Biomedical Research Centre (BRC).The national cohorts are supported by: Danish Cancer Society (Denmark); Ligue Contre le Cancer, Institut Gustave Roussy, Mutuelle Générale de l'Education Nationale, Institut National de la Santé et de la Recherche Médicale (INSERM) (France); German Cancer Aid, German Cancer Research Center (DKFZ), German Institute of Human Nutrition Potsdam‐Rehbruecke (DIfE), Federal Ministry of Education and Research (BMBF) (Germany); Associazione Italiana per la Ricerca sul Cancro‐AIRC‐Italy, Compagnia di SanPaolo and National Research Council (Italy); Dutch Ministry of Public Health, Welfare and Sports (VWS), Netherlands Cancer Registry (NKR), LK Research Funds, Dutch Prevention Funds, Dutch ZON (Zorg Onderzoek Nederland), World Cancer Research Fund (WCRF), Statistics Netherlands (The Netherlands); Health Research Fund (FIS) – Instituto de Salud Carlos III (ISCIII), Regional Governments of Andalucía, Asturias, Basque Country, Murcia and Navarra, and the Catalan Institute of Oncology – ICO (Spain); Swedish Cancer Society, Swedish Research Council and County Councils of Skåne and Västerbotten (Sweden); Cancer Research UK (14136 to EPIC‐Norfolk; C8221/A29017 to EPIC‐Oxford), Medical Research Council (1000143 to EPIC‐Norfolk; MR/M012190/1 to EPIC‐Oxford) (United Kingdom). The funders had no role in the study design or in the collection, analysis, interpretation of data, writing of the report or decision to submit the article for publication.
PY - 2024/2
Y1 - 2024/2
N2 - Background: Nutri-score is now widely available in food packages in Europe. Aim: To study the overall nutritional quality of the diet in relation to risks of Crohn's disease (CD) and ulcerative colitis (UC), in the European Prospective Investigation into Cancer and Nutrition (EPIC) cohort. Methods: We collected dietary data at baseline from validated food frequency questionnaires. We used a dietary index based on the UK Food Standards Agency modified nutrient profiling system (FSAm-NPS-DI) underlying the Nutri-Score label, to measure the nutritional quality of the diet. We estimated the association between FSAm-NPS-DI score, and CD and UC risks using Cox models stratified by centre, sex and age; and adjusted for smoking status, BMI, physical activity, energy intake, educational level and alcohol intake. Results: We included 394,255 participants (68.1% women; mean age at recruitment 52.1 years). After a mean follow-up of 13.6 years, there were 184 incident cases of CD and 459 incident cases of UC. Risk of CD was higher in those with a lower nutritional quality, that is higher FSAm-NPS-DI Score (fourth vs. first quartile: aHR: 2.04, 95% CI: 1.24–3.36; p-trend: <0.01). Among items of the FSAm-NPS-DI Score, low intakes of dietary fibre and fruits/vegetables/legumes/nuts were associated with higher risk of CD. Nutritional quality was not associated with risk of UC (fourth vs. first quartile of the FSAm-NPS-DI Score: aHR: 0.91, 95% CI: 0.69–1.21; p-trend: 0.76). Conclusions: A diet with low nutritional quality as measured by the FSAm-NPS-DI Score is associated with a higher risk of CD but not UC.
AB - Background: Nutri-score is now widely available in food packages in Europe. Aim: To study the overall nutritional quality of the diet in relation to risks of Crohn's disease (CD) and ulcerative colitis (UC), in the European Prospective Investigation into Cancer and Nutrition (EPIC) cohort. Methods: We collected dietary data at baseline from validated food frequency questionnaires. We used a dietary index based on the UK Food Standards Agency modified nutrient profiling system (FSAm-NPS-DI) underlying the Nutri-Score label, to measure the nutritional quality of the diet. We estimated the association between FSAm-NPS-DI score, and CD and UC risks using Cox models stratified by centre, sex and age; and adjusted for smoking status, BMI, physical activity, energy intake, educational level and alcohol intake. Results: We included 394,255 participants (68.1% women; mean age at recruitment 52.1 years). After a mean follow-up of 13.6 years, there were 184 incident cases of CD and 459 incident cases of UC. Risk of CD was higher in those with a lower nutritional quality, that is higher FSAm-NPS-DI Score (fourth vs. first quartile: aHR: 2.04, 95% CI: 1.24–3.36; p-trend: <0.01). Among items of the FSAm-NPS-DI Score, low intakes of dietary fibre and fruits/vegetables/legumes/nuts were associated with higher risk of CD. Nutritional quality was not associated with risk of UC (fourth vs. first quartile of the FSAm-NPS-DI Score: aHR: 0.91, 95% CI: 0.69–1.21; p-trend: 0.76). Conclusions: A diet with low nutritional quality as measured by the FSAm-NPS-DI Score is associated with a higher risk of CD but not UC.
KW - dietary
KW - EPIC
KW - FSAm-NPS DI score
KW - inflammatory bowel disease
KW - nutri-score
UR - http://www.scopus.com/inward/record.url?scp=85179951683&partnerID=8YFLogxK
U2 - 10.1111/apt.17835
DO - 10.1111/apt.17835
M3 - Article
C2 - 38100159
AN - SCOPUS:85179951683
VL - 59
SP - 558
EP - 568
JO - Alimentary Pharmacology and Therapeutics
JF - Alimentary Pharmacology and Therapeutics
SN - 0269-2813
IS - 4
ER -