Association Between the Consumption of Vegetables and Fermented Foods and COVID-19 Mortality at A Country Level in Europe. An Ecological Study


  • Jean Bousquet CHU Montpellier Professor 273 avenue d’Occitanie, 34090 Montpellier, France Author
  • Susana Fonseca Author
  • Xavier Basagana Author
  • Dora Romaguera Author
  • Marcos Quijal Author
  • Wienczyslawa CZARLEWSKI Author
  • Alain Vidal Author
  • Joao Fonseca Author
  • Josep Anto Author
  • Luis Cunha Author



COVID-19, cabbage, country, fermented vegetables, death rates



Many foods have an antioxidant activity, and nutrition may mitigate COVID-19. Some countries with a low COVID-19 mortality have a relatively high consumption of cabbage or fermented foods. To test the potential role of fermented foods and cabbage in COVID-19 mortality in Europe, we performed an ecological study.


The EFSA Comprehensive European Food Consumption Database performed an analysis on country food consumption. Fermented foods were analysed in sub-study 1, and cruciferous and other vegetables in sub-study 2. We obtained the COVID-19 mortality per number of inhabitants from the Johns Hopkins Coronavirus Resource Center. EuroStat data were used for data on potential confounders at the country level including Gross Domestic Product, population density, percentage of people older than 64 years, unemployment rate and obesity. Mortality counts were analysed using quasi-Poisson regression models - with log of population as an offset - to model the death rate while accounting for over-dispersion. A hierarchical model was used to account for multiple data.


Amoung the variables considered, only fermented vegetables reached statistical significance concerning COVID-19 death rate in sub-study 1.  In sub-study 2, cabbage and cucumber showed significance, although, for cucumber, this was no longer the case after hierarchical assessment. Adjustment did not change the point estimate, and results were still significant.


The negative ecological association between COVID-19 mortality and consumption of fermented vegetables or cabbage supports the a priory hypothesis previously reported. This hypothesis needs to be tested in individual studies performed in countries where the consumption of fermented vegetables is common. 


Download data is not yet available.


Bousquet J, Anto J, Iaccarino G, et al. Is diet partly responsible for differences in

Covid-19 death rates between and within countries? Clin Transl Allergy 2020

Bousquet J, Anto J, Czarlewski W, et al. Sulforaphane: from death rate

heterogeneity in countries to candidate for prevention of severe COVID-19

Allergy 2020;in press

Brauner JM, Mindermann S, Sharma M, et al. Inferring the effectiveness of

government interventions against COVID-19. Science 2021;371(6531) doi:

1126/science.abd9338 [published Online First: 2020/12/17]

Jain S, Buttar HS, Chintameneni M, et al. Prevention of Cardiovascular Diseases

with Anti-Inflammatory and Anti- Oxidant Nutraceuticals and Herbal Products:

An Overview of Pre-Clinical and Clinical Studies. Recent Pat Inflamm Allergy

Drug Discov 2018;12(2):145-57. doi: 10.2174/1872213X12666180815144803

[published Online First: 2018/08/16]

Razmpoosh E, Javadi M, Ejtahed HS, et al. Probiotics as beneficial agents in the

management of diabetes mellitus: a systematic review. Diabetes Metab Res Rev

;32(2):143-68. doi: 10.1002/dmrr.2665 [published Online First: 2015/05/13]

Serino A, Salazar G. Protective Role of Polyphenols against Vascular

Inflammation, Aging and Cardiovascular Disease. Nutrients 2018;11(1) doi:

3390/nu11010053 [published Online First: 2019/01/02]

Zabetakis I, Lordan R, Norton C, et al. COVID-19: The Inflammation Link and

the Role of Nutrition in Potential Mitigation. Nutrients 2020;12(5) doi:

3390/nu12051466 [published Online First: 2020/05/23]

Melini F, Melini V, Luziatelli F, et al. Health-Promoting Components in

Fermented Foods: An Up-to-Date Systematic Review. Nutrients 2019;11(5) doi:

3390/nu11051189 [published Online First: 2019/05/30]

Merten C, Ferrari P, Bakker M, et al. Methodological characteristics of the

national dietary surveys carried out in the European Union as included in the

European Food Safety Authority (EFSA) Comprehensive European Food

Consumption Database. Food Addit Contam Part A Chem Anal Control Expo

Risk Assess 2011;28(8):975-95. doi: 10.1080/19440049.2011.576440 [published

Online First: 2011/07/08]

Piorunek E, Satora S, Satora P. [Brines from sauerkraut fermentation as a thrdat

for the environement. Infrastructure and ecology of rural areas]. Polska Akademia

Nauk, Oddzia? w Krakowie, Komisja Technicznej Infrastruktury Wsi


Ver Hoef JM, Boveng PL. Quasi-Poisson vs. negative binomial regression: how

should we model overdispersed count data? Ecology 2007;88(11):2766-72. doi:

1890/07-0043.1 [published Online First: 2007/12/07]

Sunyer J, Jarvis D, Pekkanen J, et al. Geographic variations in the effect of atopy

on asthma in the European Community Respiratory Health Study. J Allergy Clin

Immunol 2004;114(5):1033-9. doi: 10.1016/j.jaci.2004.05.072 [published Online

First: 2004/11/13]

Kissler SM, Tedijanto C, Goldstein E, et al. Projecting the transmission dynamics

of SARS-CoV-2 through the postpandemic period. Science 2020 doi:

1126/science.abb5793 [published Online First: 2020/04/16]

Fardet A, Rock E. In vitro and in vivo antioxidant potential of milks, yoghurts,

fermented milks and cheeses: a narrative review of evidence. Nutrition Res Rev


Shiby VK, Mishra HN. Fermented milks and milk products as functional foods-

-a review. Crit Rev Food Sci Nutr 2013;53(5):482-96. doi:

1080/10408398.2010.547398 [published Online First: 2013/02/09]

Koutnikova H, Genser B, Monteiro-Sepulveda M, et al. Impact of bacterial

probiotics on obesity, diabetes and non-alcoholic fatty liver disease related

variables: a systematic review and meta-analysis of randomised controlled trials.

BMJ Open 2019;9(3):e017995. doi: 10.1136/bmjopen-2017-017995 [published

Online First: 2019/04/01]

Tang GY, Meng X, Li Y, et al. Effects of Vegetables on Cardiovascular Diseases

and Related Mechanisms. Nutrients 2017;9(8) doi: 10.3390/nu9080857

[published Online First: 2017/08/11]

Alkhatib A, Tsang C, Tiss A, et al. Functional Foods and Lifestyle Approaches

for Diabetes Prevention and Management. Nutrients 2017;9(12) doi:

3390/nu9121310 [published Online First: 2017/12/02]

Patel H, Chandra S, Alexander S, et al. Plant-Based Nutrition: An Essential

Component of Cardiovascular Disease Prevention and Management. Curr

Cardiol Rep 2017;19(10):104. doi: 10.1007/s11886-017-0909-z [published

Online First: 2017/09/10]

Dang Y, Zhou T, Hao L, et al. In Vitro and in Vivo Studies on the AngiotensinConverting Enzyme Inhibitory Activity Peptides Isolated from Broccoli Protein

Hydrolysate. J Agric Food Chem 2019;67(24):6757-64. doi:

1021/acs.jafc.9b01137 [published Online First: 2019/06/12]

Fahey JW, Wade KL, Stephenson KK, et al. Bioavailability of Sulforaphane

Following Ingestion of Glucoraphanin-Rich Broccoli Sprout and Seed Extracts

with Active Myrosinase: A Pilot Study of the Effects of Proton Pump Inhibitor

Administration. Nutrients 2019;11(7) doi: 10.3390/nu11071489 [published

Online First: 2019/07/03]

Vanduchova A, Anzenbacher P, Anzenbacherova E. Isothiocyanate from

Broccoli, Sulforaphane, and Its Properties. J Med Food 2019;22(2):121-26. doi:

1089/jmf.2018.0024 [published Online First: 2018/10/30]

Larocca M, Perna AM, Simonetti A, et al. Antioxidant and anti-inflammatory

effects of cauliflower leaf powder-enriched diet against LPS induced toxicity in

rabbits. Food Funct 2017;8(9):3288-96. doi: 10.1039/c7fo00253j [published

Online First: 2017/08/24]

Baenas N, Marhuenda J, Garcia-Viguera C, et al. Influence of Cooking Methods

on Glucosinolates and Isothiocyanates Content in Novel Cruciferous Foods.

Foods 2019;8(7) doi: 10.3390/foods8070257 [published Online First:


Iddir M, Brito A, Dingeo G, et al. Strengthening the Immune System and

Reducing Inflammation and Oxidative Stress through Diet and Nutrition:

Considerations during the COVID-19 Crisis. Nutrients 2020;12(6) doi:

3390/nu12061562 [published Online First: 2020/05/31]

Senger DR, Li D, Jaminet SC, et al. Activation of the Nrf2 Cell Defense Pathway

by Ancient Foods: Disease Prevention by Important Molecules and Microbes

Lost from the Modern Western Diet. PLoS One 2016;11(2):e0148042. doi:

1371/journal.pone.0148042 [published Online First: 2016/02/18]

Kalantar-Zadeh K, Ward S, Kalantar-Zadeh K, et al. Considering the effects of

microbiome and diet on SARS-CoV-2 infection: nantechnology roles. ACSNano

:in press.

Bousquet J, Czarlewski W, Blain H, et al. Rapid Response: Why Germany’s case

fatality rate seems so low: Is nutrition another possibility. April 17, 2020. bmj


Xu K, Cai H, Shen Y, et al. [Management of Corona Virus disease-19 (COVID19): The Zhejiang Experience]. Zhejiang Da Xue Xue Bao Yi Xue Ban 2020;49

Houstis N, Rosen ED, Lander ES. Reactive oxygen species have a causal role in

multiple forms of insulin resistance. Nature 2006;440(7086):944-8. doi:

1038/nature04634 [published Online First: 2006/04/14]

Hurrle S, Hsu WH. The etiology of oxidative stress in insulin resistance. Biomed

J 2017;40(5):257-62. doi: 10.1016/ [published Online First:


Wen H, Gwathmey JK, Xie LH. Oxidative stress-mediated effects of angiotensin

II in the cardiovascular system. World J Hypertens 2012;2(4):34-44. doi:

5494/wjh.v2.i4.34 [published Online First: 2012/08/23]

Dalan R, Bornstein SR, El-Armouche A, et al. The ACE-2 in COVID-19: Foe or

Friend? Horm Metab Res 2020;52(5):257-63. doi: 10.1055/a-1155-0501

[published Online First: 2020/04/28]

Uruno A, Yagishita Y, Yamamoto M. The Keap1-Nrf2 system and diabetes

mellitus. Arch Biochem Biophys 2015;566:76-84. doi:

1016/ [published Online First: 2014/12/22]

Vasileva LV, Savova MS, Amirova KM, et al. Obesity and NRF2-mediated

cytoprotection: Where is the missing link? Pharmacol Res 2020;156:104760. doi:

1016/j.phrs.2020.104760 [published Online First: 2020/03/25]

Guo Z, Mo Z. Keap1-Nrf2 signaling pathway in angiogenesis and vascular

diseases. J Tissue Eng Regen Med 2020;14(6):869-83. doi: 10.1002/term.3053

[published Online First: 2020/04/27]

McCord JM, Hybertson BM, Cota-Gomez A, et al. Nrf2 Activator PB125(R) as

a Potential Therapeutic Agent Against COVID-19. bioRxiv 2020 doi:

1101/2020.05.16.099788 [published Online First: 2020/06/09]

Adekunle IA, Onanuga AT, Akinola OO, et al. Modelling spatial variations of

coronavirus disease (COVID-19) in Africa. Sci Total Environ 2020;729:138998.

doi: 10.1016/j.scitotenv.2020.138998 [published Online First: 2020/05/04]

Rosenthal PJ, Breman JG, Djimde AA, et al. COVID-19: Shining the Light on

Africa. Am J Trop Med Hyg 2020 doi: 10.4269/ajtmh.20-0380 [published Online

First: 2020/05/07]

Azam M, Mohsin M, Ijaz H, et al. Review - Lactic acid bacteria in traditional

fermented Asian foods. Pak J Pharm Sci 2017;30(5):1803-14. [published Online

First: 2017/11/01]

Battcock M, Azam-Alie S. Fermented frutis and vegetavbles. A global

perspecrtive. Rome1998.

Patra JK, Das G, Paramithiotis S, et al. Kimchi and Other Widely Consumed

Traditional Fermented Foods of Korea: A Review. Front Microbiol 2016;7:1493.

doi: 10.3389/fmicb.2016.01493 [published Online First: 2016/10/14]

Rhee SJ, Lee JE, Lee CH. Importance of lactic acid bacteria in Asian fermented

foods. Microb Cell Fact 2011;10 Suppl 1:S5. doi: 10.1186/1475-2859-10-S1-S5

[published Online First: 2011/10/26]

Agyei D, Owusu-Kwarteng J, Akabanda F, et al. Indigenous African fermented

dairy products: Processing technology, microbiology and health benefits. Crit

Rev Food Sci Nutr 2020;60(6):991-1006. doi: 10.1080/10408398.2018.1555133

[published Online First: 2019/01/23]

Haahtela T, von Hertzen L, Anto JM, et al. Helsinki by nature: The Nature Step

to Respiratory Health. Clin Transl Allergy 2019;9:57. doi: 10.1186/s13601-019-

-2 [published Online First: 2019/11/07]

Vandana UK, Barlaskar NH, Gulzar ABM, et al. Linking gut microbiota with the

human diseases. Bioinformation 2020;16(2):196-208. doi:

6026/97320630016196 [published Online First: 2020/05/15]

McCall LI, Callewaert C, Zhu Q, et al. Home chemical and microbial transitions

across urbanization. Nat Microbiol 2020;5(1):108-15. doi: 10.1038/s41564-019-

-4 [published Online First: 2019/11/07]

Haahtela T, Anto J, Bousquet J. Slow Health Catastrophe of Homo urbanicus ‒

Loss of Resilience. Porto Med J 2020

O’Callaghan C, Anto J. COVID-19: The Disease of the Anthropocene. Env Res

;187:109683.doi: 10.1016/j.envres.2020.83. Epub 2020 May 15.






ORIGINAL ARTICLES ~ Allied Health Sciences

Similar Articles

1-10 of 63

You may also start an advanced similarity search for this article.