Abstract
Purpose
While the consumption of ultra-processed foods is steadily increasing, there is a growing interest in more sustainable diets that would include more plant protein. We aimed to study associations between the degree of food processing, patterns of protein intake, diet quality and cardiometabolic risk.
Methods
Using the NOVA classification, we assessed the proportion of energy from unprocessed/minimally processed foods (MPFp), processed foods (PFp) and ultra-processed foods (UPFp) in the diets of 1774 adults (18–79 years) from the latest cross-sectional French national survey (INCA3, 2014–2015). We studied the associations between MPFp, PFp and UPFp with protein intakes, diet quality (using the PANDiet scoring system, the global (PDI), healthful (hPDI) and unhealthful (uPDI) plant-based diet indices) and risk of cardiometabolic death (using the EpiDiet model).
Results
MPFp was positively associated with animal protein intake and plant protein diversity, whereas PFp was positively associated with plant protein intake and negatively with plant protein diversity. The PANDiet was positively associated with MPFp (β = 0.14, P < 0.0001) but negatively with UPFp (β = − 0.05, P < 0.0001). These associations were modified by adjustment for protein intakes and plant protein diversity. As estimated with comparative risk assessment modeling between extreme tertiles of intake, mortality from cardiometabolic diseases would be decreased with higher MPFp (e.g. by 31% for ischemic heart diseases) and increased with higher UPFp (by 42%) and PFp (by 11%).
Conclusions
In the French population, in contrast with UPFp, higher MPFp was associated with higher animal protein intake, better plant protein diversity, higher diet quality and markedly lower cardiometabolic risk.
Similar content being viewed by others
Availability of data and materials
The datasets of the INCA3 survey are available at data.gouv.fr. Data sets generated during the current study are available from the corresponding author on reasonable request.
Code availability
Custom code are available from the corresponding author on reasonable request.
Abbreviations
- ANSES:
-
French Agency for Food, Environmental and Occupational Health and Safety
- AS:
-
Adequacy Subscore
- BI:
-
Berry-Index
- BI-ABF:
-
Berry-Index-animal-based families
- BI-PBF:
-
Berry-Index-plant-based families
- CIQUAL:
-
French Centre for Information on Food Quality
- EpiDiet:
-
Evaluate the Potential Impact of a Diet
- hPDI:
-
Healthful Plant-based Diet Index
- INCA3:
-
Third Individual and National Study on Food Consumption Survey
- MPF:
-
Unprocessed/minimally processed foods
- MPFp:
-
Proportion of total energy intake from MPF
- MS:
-
Moderation subscore
- PANDiet:
-
Probability of adequate nutrient intake
- PDI:
-
Plant-based diet Index
- PF:
-
Processed foods
- PFp:
-
Proportion of total energy intake from PF
- uPDI:
-
Unhealthful plant-based DIET Index
- UI:
-
Uncertainty interval
- UPF:
-
Ultra-processed foods
- UPFp:
-
Proportion of total energy intake from UPF
References
Monteiro CA, Cannon G, Levy R et al (2016) NOVA. The star shines bright. [Food classification Puclib health]. World Nutr 7:28–38
Monteiro CA, Cannon G, Levy RB et al (2019) Ultra-processed foods: what they are and how to identify them. Public Health Nutr 22:936–941. https://doi.org/10.1017/S1368980018003762
Martínez Steele E, Baraldi LG, da Louzada MLC et al (2016) Ultra-processed foods and added sugars in the US diet: evidence from a nationally representative cross-sectional study. BMJ Open 6:e009892. https://doi.org/10.1136/bmjopen-2015-009892
Rauber F, da Costa Louzada ML, Steele E et al (2018) Ultra-processed food consumption and chronic non-communicable diseases-related dietary nutrient profile in the UK (2008–2014). Nutrients 10:587. https://doi.org/10.3390/nu10050587
Monteiro CA, Moubarac J-C, Cannon G et al (2013) Ultra-processed products are becoming dominant in the global food system: ultra-processed products: global dominance. Obes Rev 14:21–28. https://doi.org/10.1111/obr.12107
Monteiro CA, Cannon G, Moubarac J-C et al (2018) The UN Decade of Nutrition, the NOVA food classification and the trouble with ultra-processing. Public Health Nutr 21:5–17. https://doi.org/10.1017/S1368980017000234
Martínez Steele E, Raubenheimer D, Simpson SJ et al (2018) Ultra-processed foods, protein leverage and energy intake in the USA. Public Health Nutr 21:114–124. https://doi.org/10.1017/S1368980017001574
Gerber PJ, Food and Agriculture Organization of the United Nations (2013) Tackling climate change through livestock: a global assessment of emissions and mitigation opportunities. Food and Agriculture Organization of the United Nations, Rome
Wu G, Fanzo J, Miller DD et al (2014) Production and supply of high-quality food protein for human consumption: sustainability, challenges, and innovations: sustainability, challenge and innovations. Ann NY Acad Sci 1321:1–19. https://doi.org/10.1111/nyas.12500
Springmann M, Clark M, Mason-D’Croz D et al (2018) Options for keeping the food system within environmental limits. Nature 562:519–525. https://doi.org/10.1038/s41586-018-0594-0
Willett W, Rockström J, Loken B et al (2019) Food in the anthropocene: the EAT–Lancet Commission on healthy diets from sustainable food systems. The Lancet 393:447–492. https://doi.org/10.1016/S0140-6736(18)31788-4
World Cancer Research Fund, American Institute for Cancer Research. (2018) Diet, nutrition, physical activity and cancer: a global perspective. The third Expert Report
Mariotti F (2019) Animal and plant protein sources and cardiometabolic health. Adv Nutr 10:S351–S366. https://doi.org/10.1093/advances/nmy110
Song M, Fung TT, Hu FB et al (2016) Association of animal and plant protein intake with all-cause and cause-specific mortality. JAMA Intern Med 176:1453. https://doi.org/10.1001/jamainternmed.2016.4182
Satija A, Bhupathiraju SN, Spiegelman D et al (2017) Healthful and unhealthful plant-based diets and the risk of coronary heart disease in U.S. Adults J Am Coll Cardiol 70:411–422. https://doi.org/10.1016/j.jacc.2017.05.047
Satija A, Bhupathiraju SN, Rimm EB et al (2016) Plant-based dietary patterns and incidence of type 2 diabetes in US men and women: results from three prospective cohort studies. PLoS Med 13:e1002039. https://doi.org/10.1371/journal.pmed.1002039
Gehring J, Touvier M, Baudry J et al (2020) Consumption of ultra-processed foods by pesco-vegetarians, vegetarians, and vegans: associations with duration and age at diet initiation. J Nutr 151:120–131. https://doi.org/10.1093/jn/nxaa196
Moodie R, Stuckler D, Monteiro C et al (2013) Profits and pandemics: prevention of harmful effects of tobacco, alcohol, and ultra-processed food and drink industries. The Lancet 381:670–679. https://doi.org/10.1016/S0140-6736(12)62089-3
Vandevijvere S, Jaacks LM, Monteiro CA et al (2019) Global trends in ultraprocessed food and drink product sales and their association with adult body mass index trajectories. Obes Rev 20:10–19. https://doi.org/10.1111/obr.12860
Monteiro CA, Cannon G, Lawrence M et al (2019) Ultra-processed foods, diet quality, and health using the NOVA classification system. FAO, Rome
Fiolet T, Srour B, Sellem L et al (2018) Consumption of ultra-processed foods and cancer risk: results from NutriNet-Santé prospective cohort. BMJ. https://doi.org/10.1136/bmj.k322
Mendonça R de D, Lopes ACS, Pimenta AM et al (2017) Ultra-processed food consumption and the incidence of hypertension in a mediterranean cohort: the Seguimiento Universidad de Navarra Project. Am J Hypertens 30:358–366. https://doi.org/10.1093/ajh/hpw137
Nardocci M, Leclerc B-S, Louzada M-L et al (2019) Consumption of ultra-processed foods and obesity in Canada. Can J Public Health 110:4–14. https://doi.org/10.17269/s41997-018-0130-x
Blanco-Rojo R, Sandoval-Insausti H, López-Garcia E et al (2019) Consumption of ultra-processed foods and mortality: a National Prospective Cohort in Spain. Mayo Clin Proc 94:2178–2188. https://doi.org/10.1016/j.mayocp.2019.03.035
Kim H, Hu EA, Rebholz CM (2019) Ultra-processed food intake and mortality in the USA: results from the Third National Health and Nutrition Examination Survey (NHANES III, 1988–1994). Public Health Nutr 22:1777–1785. https://doi.org/10.1017/S1368980018003890
Hall KD, Ayuketah A, Brychta R et al (2019) Ultra-processed diets cause excess calorie intake and weight gain: an inpatient randomized controlled trial of Ad libitum food intake. Cell Metab 30:67-77.e3. https://doi.org/10.1016/j.cmet.2019.05.008
French Agency for Food, Environmental and Occupational Health & Safety (ANSES) (2017) Opinion of the French Agency for Food, Environmental and Occupational Health & Safety on “the Third Individual and National Survey on Food Consumption (INCA3 survey)”. ANSES. Available at: https://www.anses.fr/en/system/files/NUT2014SA0234EN.pdf
Dubuisson C, Dufour A, Carrillo S et al (2019) The Third French Individual and National Food Consumption (INCA3) Survey 2014–2015: method, design and participation rate in the framework of a European harmonization process. Public Health Nutr 22:584–600. https://doi.org/10.1017/S1368980018002896
Henry C (2005) Basal metabolic rate studies in humans: measurement and development of new equations. Public Health Nutr 8:1133–1152. https://doi.org/10.1079/PHN2005801
Black A (2000) Critical evaluation of energy intake using the Goldberg cut-off for energy intake:basal metabolic rate. A practical guide to its calculation, use and limitations. Int J Obes 24:1119–1130. https://doi.org/10.1038/sj.ijo.0801376
Slimani N, Freisling H, Huybrechts I, et al (2013) Food Consumption Data Collection Methodology for the EU Menu Survey (EMP‐PANEU) Final Report. EFSA supporting publication
French Agency for Food, Environmental and Occupational Health & Safety (ANSES) (2016) ANSES-CIQUAL French food composition table version 2016
Salomé M, de Gavelle E, Dufour A et al (2020) Plant-protein diversity is critical to ensuring the nutritional adequacy of diets when replacing animal with plant protein: observed and modeled diets of French adults (INCA3). J Nutr 150:536–545. https://doi.org/10.1093/jn/nxz252
Drescher LS, Thiele S, Mensink GBM (2007) A new index to measure healthy food diversity better reflects a healthy diet than traditional measures. J Nutr 137:647–651. https://doi.org/10.1093/jn/137.3.647
de Oliveira Otto MC, Padhye NS, Bertoni AG et al (2015) Everything in moderation—dietary diversity and quality, central obesity and risk of diabetes. PLoS ONE 10:e0141341. https://doi.org/10.1371/journal.pone.0141341
Verger EO, Mariotti F, Holmes BA et al (2012) Evaluation of a Diet Quality Index based on the probability of adequate nutrient intake (PANDiet) using National French and US Dietary Surveys. PLoS ONE 7:e42155. https://doi.org/10.1371/journal.pone.0042155
de Gavelle E, Huneau J-F, Fouillet H, Mariotti F (2019) The initial dietary pattern should be considered when changing protein food portion sizes to increase nutrient adequacy in french adults. J Nutr 149:488–496. https://doi.org/10.1093/jn/nxy275
French Agency for Food, Environmental and Occupational Health & Safety (ANSES) (2016) Actualisation des repères du PNNS : élaboration des références nutritionnelles. Anses. Available at: https://www.anses.fr/fr/system/files/NUT2012SA0103Ra-2.pdf
French Agency for Food, Environmental and Occupational Health & Safety (Anses) (2019) Opinion of the French Agency for Food, Environmental and Occupation Health & Safety on the updating of the PNNS dietary guidelines for women from menopause and men over 65 years of age. Anses. Available at: https://www.anses.fr/en/system/files/NUT2017SA0143EN.pdf
Murray CJL, Lopez AD (2013) Measuring the global burden of disease. N Engl J Med 369:448–457. https://doi.org/10.1056/NEJMra1201534
Kesse-Guyot E, Chaltiel D, Wang J et al (2020) Sustainability analysis of French dietary guidelines using multiple criteria. Nat Sustain 3:377–385. https://doi.org/10.1038/s41893-020-0495-8
Aune D, Giovannucci E, Boffetta P et al (2017) Fruit and vegetable intake and the risk of cardiovascular disease, total cancer and all-cause mortality—a systematic review and dose-response meta-analysis of prospective studies. Int J Epidemiol 46:1029–1056. https://doi.org/10.1093/ije/dyw319
Micha R, Peñalvo JL, Cudhea F et al (2017) Association between dietary factors and mortality from heart disease, stroke, and type 2 diabetes in the United States. JAMA 317:912. https://doi.org/10.1001/jama.2017.0947
Scarborough P, Harrington RA, Mizdrak A et al (2014) The preventable risk integrated ModEl and its use to estimate the health impact of public health policy scenarios. Scientifica 2014:1–21. https://doi.org/10.1155/2014/748750
Inserm CépiDC Classification internationale des maladies (CIM). In: CépiDC Internet. https://www.cepidc.inserm.fr/causes-medicales-de-deces/classification-internationale-des-maladies-cim. Accessed 26 Feb 2019
Insee Évolution et structure de la population en 2014. In: Insee Internet. https://www.insee.fr/fr/statistiques/2862200. Accessed 26 Feb 2019
CépiDc (2019) Causes Médicales des Décès en 2014. https://www.cepidc.inserm.fr/causes-medicales-de-deces/interroger-les-donnees-de-mortalite . Accessed 26 Feb 2019
Thiébaut A, Kesse E, Com-Nougué C et al (2004) Ajustement sur l’apport énergétique dans l’évaluation des facteurs de risque alimentaires. Rev Épidémiol Santé Publ 52:539–557. https://doi.org/10.1016/S0398-7620(04)99093-1
Willett WC, Howe GR, Kushi LH (1997) Adjustment for total energy intake in epidemiologic studies. Am J Clin Nutr 65:1220S-1228S. https://doi.org/10.1093/ajcn/65.4.1220S
Saltelli A, Ratto M, Andres T et al (2008) Global sensitivity analysis: the primer. Wiley, Chichester
Adams J, White M (2015) Characterisation of UK diets according to degree of food processing and associations with socio-demographics and obesity: cross-sectional analysis of UK National Diet and Nutrition Survey (2008–12). Int J Behav Nutr Phys Act 12:160. https://doi.org/10.1186/s12966-015-0317-y
Julia C, Martinez L, Allès B et al (2018) Contribution of ultra-processed foods in the diet of adults from the French NutriNet-Santé study. Public Health Nutr 21:27–37. https://doi.org/10.1017/S1368980017001367
Baraldi LG, Martinez Steele E, Canella DS, Monteiro CA (2018) Consumption of ultra-processed foods and associated sociodemographic factors in the USA between 2007 and 2012: evidence from a nationally representative cross-sectional study. BMJ Open 8:e020574. https://doi.org/10.1136/bmjopen-2017-020574
Machado PP, Steele EM, da Louzada MLC et al (2019) Ultra-processed food consumption drives excessive free sugar intake among all age groups in Australia. Eur J Nutr. https://doi.org/10.1007/s00394-019-02125-y
Baker P, Machado P, Santos T, et al (2020) Ultra‐processed foods and the nutrition transition: Global, regional and national trends, food systems transformations and political economy drivers. Obesity Reviews 21. https://doi.org/10.1111/obr.13126
de Gavelle E, Huneau J-F, Mariotti F (2018) Patterns of protein food intake are associated with nutrient adequacy in the general French adult population. Nutrients 10:226. https://doi.org/10.3390/nu10020226
Gazan R, Béchaux C, Crépet A et al (2016) Dietary patterns in the French adult population: a study from the second French national cross-sectional dietary survey (INCA2) (2006–2007). Br J Nutr 116:300–315. https://doi.org/10.1017/S0007114516001549
da Louzada MLC, Ricardo CZ, Steele EM et al (2018) The share of ultra-processed foods determines the overall nutritional quality of diets in Brazil. Public Health Nutr 21:94–102. https://doi.org/10.1017/S1368980017001434
Martínez Steele E, Popkin BM, Swinburn B, Monteiro CA (2017) The share of ultra-processed foods and the overall nutritional quality of diets in the US: evidence from a nationally representative cross-sectional study. Popul Health Metrics 15:6. https://doi.org/10.1186/s12963-017-0119-3
Rauber F, da Louzada MLC, Martinez Steele E et al (2019) Ultra-processed foods and excessive free sugar intake in the UK: a nationally representative cross-sectional study. BMJ Open 9:e027546. https://doi.org/10.1136/bmjopen-2018-027546
Rauber F, Chang K, Vamos EP et al (2020) Ultra-processed food consumption and risk of obesity: a prospective cohort study of UK Biobank. Eur J Nutr. https://doi.org/10.1007/s00394-020-02367-1
Salas-Salvadó J, Becerra-Tomás N, García-Gavilán JF et al (2018) Mediterranean diet and cardiovascular disease prevention: what do we know? Prog Cardiovasc Dis 61:62–67. https://doi.org/10.1016/j.pcad.2018.04.006
Anand SS (2015) Food consumption and its impact on cardiovascular disease: importance of solutions focused on the globalized food system: a report from the workshop convened by the World Heart Federation. Cardiovasc Dis 66:25
Petersen KS, Flock MR, Richter CK et al (2017) Healthy dietary patterns for preventing cardiometabolic disease: the role of plant-based foods and animal products. Curr Dev Nutr 1:cdn.117.001289. https://doi.org/10.3945/cdn.117.001289
Kim H, Caulfield LE, Garcia-Larsen V et al (2019) Plant-based diets are associated with a lower risk of incident cardiovascular disease, cardiovascular disease mortality, and all-cause mortality in a general population of middle-aged adults. JAHA 8:e012865. https://doi.org/10.1161/JAHA.119.012865
Springmann M, Wiebe K, Mason-D’Croz D et al (2018) Health and nutritional aspects of sustainable diet strategies and their association with environmental impacts: a global modelling analysis with country-level detail. The Lancet Planetary Health 2:e451–e461. https://doi.org/10.1016/S2542-5196(18)30206-7
Tian S, Xu Q, Jiang R et al (2017) Dietary protein consumption and the risk of type 2 diabetes: a systematic review and meta-analysis of cohort studies. Nutrients 9:982. https://doi.org/10.3390/nu9090982
Sanchez-Sabate R, Badilla-Briones Y, Sabaté J (2019) Understanding attitudes towards reducing meat consumption for environmental reasons. A qualitative synthesis review. Sustainability 11:6295. https://doi.org/10.3390/su11226295
Malek L, Umberger WJ, Goddard E (2019) Committed vs. uncommitted meat eaters: understanding willingness to change protein consumption. Appetite 138:115–126. https://doi.org/10.1016/j.appet.2019.03.024
Acknowledgements
The authors would like to thank Benjamin Allès (Nutritional Epidemiology Research Team (EREN) at Université Paris 13, France) for his scientific support in constructing the NOVA database and Emmanuelle Kesse-Guyot (Nutritional Epidemiology Research Team (EREN) at Université Paris 13, France) for her scientific contribution to the constitution of the disease mortality database for the EpiDiet model.
Funding
M. Salomé’s PhD fellowship is currently being funded by a research contract with Terres Univia, the French Interbranch organization for plant oils and proteins. F Mariotti is the scientific leader of this contract.
Author information
Authors and Affiliations
Contributions
MS, LA and FM designed research; MS, LA and JW conducted research; AD, CD and J-LV provided the databases essential for the research; J-FH provided methodological support. MS and LA analyzed data and performed statistical analysis; MS, LA, JW and FM interpreted the results; MS, LA, JW and FM wrote paper; MS and FM had primary responsibility for the final content and all authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no competing interests.
Ethical approval
The INCA3 study was carried out in accordance with the Declaration of Helsinki guidelines and was approved by the ‘Comité Consultatif sur le Traitement de l’Information en matière de Recherche dans le domaine de la Santé’ (Advisory Committee on Information Processing in Health Research).
Consent to participate
For the data collection of the INCA3 survey, oral consent was obtained, witnessed and formally recorded from participants.
Consent for publication
Not applicable.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Salomé, M., Arrazat, L., Wang, J. et al. Contrary to ultra-processed foods, the consumption of unprocessed or minimally processed foods is associated with favorable patterns of protein intake, diet quality and lower cardiometabolic risk in French adults (INCA3). Eur J Nutr 60, 4055–4067 (2021). https://doi.org/10.1007/s00394-021-02576-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00394-021-02576-2