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Prevalence and concentration of fumonisins in cereal-based foods: a global systematic review and meta-analysis study

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Abstract

Cereal-based foods are utilized as an essential food segment worldwide. Nevertheless, their contamination by mycotoxins, also fumonisins, could pose a critical health risk. The present research provides the first systematic review regarding the prevalence and concentration of fumonisins in cereal-based food with the aid of a meta-analysis. In this regard, some international databases PubMed, Web of Science, Google Scholar, and Scopus were explored during the last 30 years. Among 9729 screened articles, 73 articles (which meet the proposed inclusion criteria), including 11,132 data, were incorporated in the performed meta-analysis. The overall rank order regarding the concentration of fumonisins in cereal-based foods was corn-based foods > wheat-based foods > other cereal foods > barley-based foods > rice-based foods > oat-based foods. Based on the prevalence of fumonisins, the overall rank order was other cereal foods > corn-based foods > rice-based foods > wheat-based foods > oat-based foods > barley-based food. The present meta-analysis results can be a beneficial database for risk assessment model progress, which can help industries and organizations decrease the presence of fumonisins in cereal-based food.

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References

  • Alshannaq A, Yu JH (2017) Occurrence, toxicity, and analysis of major mycotoxins in food. Int J Environ Res Public Health 14. https://doi.org/10.3390/ijerph14060632

  • Bordin K, Rosim RE, Neeff DV, Rottinghaus GE, Oliveira CAF (2014) Assessment of dietary intake of fumonisin B1 in São Paulo, Brazil. Food Chem 155:174–178. https://doi.org/10.1016/j.foodchem.2014.01.0572014.01.057

  • Bordini JG, Ono MA, Garcia GT, Fazani VHM, Vizoni É, Rodrigues KCB, Hirooka EY, Ono EYS (2017) Impact of industrial dry-milling on fumonisin redistribution in non-transgenic corn in Brazil. Food Chem 220:438–443

  • Borenstein M, Hedges LV, Higgins JP, Rothstein HR (2011) Introduction to meta-analysis. John Wiley & Sons

  • Bryla M, Roszko M, Szymczyk K, Jedrzejczak R, Obiedzinski MW (2016) Fumonisins and their masked forms in maize products. Food Control 59:619–627. https://doi.org/10.1016/j.foodcont.2015.06.032

    Article  CAS  Google Scholar 

  • Bullerman LB, Ryu D, Jackson LS (2002) Stability of fumonisins in food processing. In: DeVries JW, Trucksess MW, Jackson LS (eds) Mycotoxins and food safety. Springer US, Boston, pp 195–204. https://doi.org/10.1007/978-1-4615-0629-4_20

    Chapter  Google Scholar 

  • Caldas ED, Silva AC (2007) Mycotoxins in corn-based food products consumed in Brazil: an exposure assessment for fumonisins. J Agric Food Chem 55:7974–7980. https://doi.org/10.1021/jf0712898

    Article  CAS  Google Scholar 

  • Cendoya E, MdP M, Chiacchiera SM, Farnochi MC, Ramirez ML (2018) Influence of water activity and temperature on growth and fumonisin production by Fusarium proliferatum strains on irradiated wheat grains. Int J Food Microbiol 266:158–166. https://doi.org/10.1016/j.ijfoodmicro.2017.12.001

    Article  CAS  Google Scholar 

  • Cherkani-Hassani A, Mojemmi B, Mouane N (2016) Occurrence and levels of mycotoxins and their metabolites in human breast milk associated to dietary habits and other factors: a systematic literature review, 1984–2015. Trends Food Sci Technol 50:56–69

    Article  CAS  Google Scholar 

  • Chilaka CA, De Boevre M, Atanda OO, De Saeger S (2019) Fate of Fusarium mycotoxins during processing of Nigerian traditional infant foods (ogi and soybean powder). Food Res Int 116:408–418

    Article  CAS  Google Scholar 

  • Cook DA, Levinson AJ, Garside S, Dupras DM, Erwin PJ, Montori VM (2008) Internet-based learning in the health professions: a meta-analysis. JAMA 300:1181–1196

    Article  CAS  Google Scholar 

  • D’Arco G, Fernandez-Franzon M, Font G, Damiani P, Manes J (2009) Survey of fumonisins B1, B2 and B3 in conventional and organic retail corn products in Spain and Italy and estimated dietary exposure Food additives & contaminants Part B. Surveillance 2:146–153. https://doi.org/10.1080/02652030903148314

    Article  CAS  Google Scholar 

  • De Boevre M et al (2012) Natural occurrence of mycotoxins and their masked forms in food and feed products. World Mycotoxin J 5:207–219

    Article  Google Scholar 

  • De Girolamo A, Lattanzio VMT, Schena R, Visconti A, Pascale M (2016) Effect of alkaline cooking of maize on the content of fumonisins B1 and B2 and their hydrolysed forms. Food Chem 192:1083–1089. https://doi.org/10.1016/j.foodchem.2015.07.059

    Article  CAS  Google Scholar 

  • Egger M, Davey-Smith G, Altman D (2008) Systematic reviews in health care: meta-analysis in context. John Wiley & Sons

  • Esposito F, Fasano E, Scognamiglio G, Nardone A, Triassi M, Cirillo T (2016) Exposure assessment to fumonisins B1, B2 and B3 through consumption of gluten-free foodstuffs intended for people affected by celiac disease. Food Chem Toxicol 97:395–401

    Article  CAS  Google Scholar 

  • Fandohan P, Zoumenou D, Hounhouigan DJ, Marasas WFO, Wingfield MJ, Hell K (2005) Fate of aflatoxins and fumonisins during the processing of maize into food products in Benin. Int J Food Microbiol 98:249–259. https://doi.org/10.1016/j.ijfoodmicro.2004.07.007

    Article  CAS  Google Scholar 

  • Feijó Corrêa JA, Orso PB, Bordin K, Hara RV, Luciano FB (2018) Toxicological effects of fumonisin B1 in combination with other Fusarium toxins. Food Chem Toxicol 121:483–494. https://doi.org/10.1016/j.fct.2018.09.043

    Article  CAS  Google Scholar 

  • Franco LT, Petta T, Rottinghaus GE, Bordin K, Gomes GA, Alvito P, Assunção R, Oliveira CA (2019) Assessment of mycotoxin exposure and risk characterization using occurrence data in foods and urinary biomarkers in Brazil. Food Chem Toxicol 128:21–34. https://doi.org/10.1016/j.fct.2019.03.046

    Article  CAS  Google Scholar 

  • Hedges LV, Vevea JL (1998) Fixed-and random-effects models in meta-analysis. Psychol Methods 3:486

    Article  Google Scholar 

  • Hedges LV, Gurevitch J, Curtis PS (1999) The meta-analysis of response ratios in experimental ecology. Ecology 80:1150–1156

    Article  Google Scholar 

  • Higgins J, Green S (2011) Cochrane handbook for systematic reviews of interventions: Cochrane book series Chichester England. Wiley-Blackwell, USA, Hoboken

    Google Scholar 

  • Higgins, Thompson S (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21:1539–1558

    Article  Google Scholar 

  • Higgins J, White IR, Anzures-Cabrera J (2008) Meta-analysis of skewed data: combining results reported on log-transformed or raw scales. Stat Med 27:6072–6092

    Article  Google Scholar 

  • Hussain N, Sun D-W, Pu H (2019) Classical and emerging non-destructive technologies for safety and quality evaluation of cereals: a review of recent applications. Trends Food Sci Technol 91:598–608. https://doi.org/10.1016/j.tifs.2019.07.018

    Article  CAS  Google Scholar 

  • IARC (2002) International Agency for Research on Cancer, IARC. (2002). Monographs, 82, 301e366. In: International Agency for Research on Cancer, IARC. (2002), vol 82

  • Jaenke R, Barzi F, McMahon E, Webster J, Brimblecombe J (2017) Consumer acceptance of reformulated food products: a systematic review and meta-analysis of salt-reduced foods. Crit Rev Food Sci Nutr 57:3357–3372

    Article  CAS  Google Scholar 

  • Kamle M, Mahato DK, Devi S, Lee KE, Kang SG, Kumar P (2019) Fumonisins: impact on agriculture, food, and human health and their management strategies. Toxins 11. https://doi.org/10.3390/toxins11060328

  • Khademi F, Sahebkar A (2019) A systematic review and meta-analysis on the prevalence of antibiotic-resistant Listeria species in food, animal and human specimens in Iran. J Food Sci Technol 56:5167–5183. https://doi.org/10.1007/s13197-019-04040-w

    Article  Google Scholar 

  • Khaneghah AM, Fakhri Y, Raeisi S, Armoon B, Sant’Ana AS (2018) Prevalence and concentration of ochratoxin A, zearalenone, deoxynivalenol and total aflatoxin in cereal-based products: a systematic review and meta-analysis. Food Chem Toxicol 118:830–848

    Article  Google Scholar 

  • Kirinčič S, Škrjanc B, Kos N, Kozolc B, Pirnat N, Tavčar-Kalcher G (2015) Mycotoxins in cereals and cereal products in Slovenia – official control of foods in the years 2008–2012. Food Control 50:157–165. https://doi.org/10.1016/j.foodcont.2014.08.034

    Article  CAS  Google Scholar 

  • Kuroki T, Watanabe Y, Teranishi H, Izumiyama S, Amemura-Maekawa J, Kura F (2017) Legionella prevalence and risk of legionellosis in Japanese households. Epidemiol Infect 145:1398–1408

    Article  CAS  Google Scholar 

  • Liberati A et al (2009) The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. PLoS Med 6:e1000100

    Article  Google Scholar 

  • Malachova A, Dzuman Z, Veprikova Z, Vaclavikova M, Zachariasova M, Hajslova J (2011) Deoxynivalenol, deoxynivalenol-3-glucoside, and enniatins: the major mycotoxins found in cereal-based products on the Czech market. J Agric Food Chem 59:12990–12997

    Article  CAS  Google Scholar 

  • Manova R, Mladenova R (2009) Incidence of zearalenone and fumonisins in Bulgarian cereal production. Food Control 20:362–365. https://doi.org/10.1016/j.foodcont.2008.06.001

    Article  CAS  Google Scholar 

  • Marvier M (2011) Using meta-analysis to inform risk assessment and risk management. J Verbr Lebensm 6:113–118

    Article  Google Scholar 

  • McInnes MDF, Moher D, Thombs BD, McGrath TA, Bossuyt PM, the P-DTAG (2018) Preferred reporting items for a systematic review and meta-analysis of diagnostic test accuracy studies: the PRISMA-DTA statement. JAMA 319:388–396. https://doi.org/10.1001/jama.2017.19163

    Article  Google Scholar 

  • Moher D, Liberati A, Tetzlaff J, Altman DG (2010) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int J Surg 8:336–341

    Article  Google Scholar 

  • Mousavi Khaneghah A, Eş I, Raeisi S, Fakhri Y (2018) Aflatoxins in cereals: state of the art. J Food Saf 38. https://doi.org/10.1111/jfs.12532

  • Mousavi Khaneghah A, Fakhri Y, Gahruie HH, Niakousari M, Sant’Ana AS (2019a) Mycotoxins in cereal-based products during 24 years (1983–2017): s global systematic review. Trends Food Sci Technol 91:95–105. https://doi.org/10.1016/j.tifs.2019.06.007

    Article  CAS  Google Scholar 

  • Mousavi Khaneghah A, Kamani MH, Fakhri Y, Coppa CFSC, de Oliveira CAF, Sant’Ana AS (2019b) Changes in masked forms of deoxynivalenol and their co-occurrence with culmorin in cereal-based products: a systematic review and meta-analysis. Food Chem 294:587–596. https://doi.org/10.1016/j.foodchem.2019.05.034

    Article  CAS  Google Scholar 

  • Mousavi Khaneghah A, Farhadi A, Nematollahi A, Vasseghian Y, Fakhri Y (2020) A systematic review and meta-analysis to investigate the concentration and prevalence of trichothecenes in the cereal-based food. Trends Food Sci Technol 102:193–202. https://doi.org/10.1016/j.tifs.2020.05.026

    Article  CAS  Google Scholar 

  • Nyaga VN, Arbyn M, Aerts M (2014) Metaprop: a Stata command to perform meta-analysis of binomial data. Arch Public Health 72:39–43

    Article  Google Scholar 

  • Ojuri OT et al (2019) Mycotoxin co-exposures in infants and young children consuming household- and industrially-processed complementary foods in Nigeria and risk management advice. Food Control 98:312–322. https://doi.org/10.1016/j.foodcont.2018.11.049

    Article  CAS  Google Scholar 

  • Ortuzar J, Martinez B, Bianchini A, Stratton J, Rupnow J, Wang B (2018) Quantifying changes in spore-forming bacteria contamination along the milk production chain from farm to packaged pasteurized milk using systematic review and meta-analysis. Food Control 86:319–331

    Article  Google Scholar 

  • Pereira VL, Fernandes JO, Cunha SC (2014) Mycotoxins in cereals and related foodstuffs: a review on occurrence and recent methods of analysis. Trends Food Sci Technol 36:96–136. https://doi.org/10.1016/j.tifs.2014.01.005

    Article  CAS  Google Scholar 

  • Piacentini KC, Savi GD, Pereira ME, Scussel VM (2015) Fungi and the natural occurrence of deoxynivalenol and fumonisins in malting barley (Hordeum vulgare L.). Food Chem 187:204–209. https://doi.org/10.1016/j.foodchem.2015.04.101

    Article  CAS  Google Scholar 

  • Quan H, Zhang J (2003) Estimate of standard deviation for a log-transformed variable using arithmetic means and standard deviations. Stat Med 22:2723–2736

    Article  Google Scholar 

  • Rahmani J et al (2018) The prevalence of aflatoxin M1 in milk of Middle East region: a systematic review, meta-analysis and probabilistic health risk assessment. Food Chem Toxicol 118:653–666

    Article  CAS  Google Scholar 

  • Rheeder JP, Marasas WF, Vismer HF (2002) Production of fumonisin analogs by Fusarium species. Appl Environ Microbiol 68:2101–2105

    Article  CAS  Google Scholar 

  • Savi GD, Piacentini KC, Marchi D, Scussel VM (2016) Fumonisins B1 and B2 in the corn-milling process and corn-based products, and evaluation of estimated daily intake. Food additives & contaminants. Part A, Chemistry, analysis, control, exposure & risk assessment 33:339–45

  • Soriano JM, Dragacci S (2004) Occurrence of fumonisins in foods. Food Res Int 37:985–1000. https://doi.org/10.1016/j.foodres.2004.06.009

    Article  CAS  Google Scholar 

  • Suman M, Bergamini E, Catellani D, Manzitti A (2013) Development and validation of a liquid chromatography/linear ion trap mass spectrometry method for the quantitative determination of deoxynivalenol-3-glucoside in processed cereal-derived products. Food Chem 136:1568–1576

    Article  CAS  Google Scholar 

  • Torovic L (2018) Fusarium toxins in corn food products: a survey of the Serbian retail market. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 35:1596–1609. https://doi.org/10.1080/19440049.2017.1419581

    Article  CAS  Google Scholar 

  • Vanara F, Reyneri A, Blandino M (2009) Fate of fumonisin B1 in the processing of whole maize kernels during dry-milling. Food Control 20:235–238. https://doi.org/10.1016/j.foodcont.2008.05.014

    Article  CAS  Google Scholar 

  • World Health O, Food, Agriculture Organization of the United N, Joint FAOWHOECoFAM (2011) Evaluation of certain food additives and contaminants: seventy-fourth [74th] report of the Joint FAO/WHO Expert Committee on Food Additives. World Health Organization, Geneva

    Google Scholar 

  • Zhang K, Flannery BM, Oles CJ, Adeuya A (2018) Mycotoxins in infant/toddler foods and breakfast cereals in the US retail market. Food Addit Contam Part B 11:183–190

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Clinical Sciences, Faculty of Veterinary Medicine, University of Tabriz, Tabriz, Iran

    Ahmad Farhadi

  2. Food Health Research Center, Department of Environmental Health Engineering, Hormozgan University of Medical Sciences, Bandar Abbas, Iran

    Yadolah Fakhri

  3. Molecular Biology Research Center, Systems Biology and Poisonings Institute, Baqiyatallah University of Medical Sciences, Tehran, Iran

    Reza Kachuei

  4. Institute of Research and Development, Duy Tan University, Da Nang, 550000, Vietnam

    Yasser Vasseghian

  5. Research Laboratory of Intelligent Control and Decision Making Systems in Industry and Economics, Azerbaijan State Oil and Industry University, 20 Azadlig Ave., AZ1010, Baku, Azerbaijan

    Elcin Huseyn

  6. Department of Food Science and Nutrition, Faculty of Food Engineering, University of Campinas (UNICAMP), Rua Monteiro Lobato, 80. Caixa Postal: 6121, Campinas, São Paulo, CEP: 13083-862, Brazil

    Amin Mousavi Khaneghah

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  1. Ahmad Farhadi
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AMK and RK had the idea for the article. AF, AMK, and YV reviewed the literature. AF, YF, and AMK checked and managed the data. YF and MDK performed data analysis. AF, MDK, and RK drafted the manuscript. YF, YV, and AMK provided expert review of the manuscript and reviewed and approved the manuscript. All authors contributed to the research article and approved the final version.

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Correspondence to Reza Kachuei or Amin Mousavi Khaneghah.

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Farhadi, A., Fakhri, Y., Kachuei, R. et al. Prevalence and concentration of fumonisins in cereal-based foods: a global systematic review and meta-analysis study. Environ Sci Pollut Res 28, 20998–21008 (2021). https://doi.org/10.1007/s11356-021-12671-w

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