Azo Dye Toxicity: Sunset Yellow Toxicity in Foods

Abstract

One of the most important synthetic azo dyes is Sunset Yellow FCF (E110), which is widely used in the food industry. Sunset Yellow continues to be investigated in terms of its adverse properties affecting human health, especially its effect on the development of attention deficit hyperactivity disorder (ADHD) and cancer and other systemic adverse effects due to excessive consumption. The main purpose of this review is to critically discuss the acceptable daily intake (ADI) of Sunset Yellow and the developmental, geno-cytotoxic and immunotoxic effects associated with exceeding the ADI.

Keywords

• Sunset Yellow
• Geno-cytotoxicity
• Developmental Toxicity
• Immunotoxicity

References

1. [1] Rovina K, Prabakaran PP, Siddiquee S, Shaarani SM. Methods for the analysis of Sunset Yellow FCF (E110) in food and beverage products- a review. In: TrAC - Trends in Analytical Chemistry (2016).
2. [2] Xing Y, Meng M, Xue H, Zhang T, Yin Y, Xi R. Development of a polyclonal antibody-based enzyme-linked immunosorbent assay (ELISA) for detection of Sunset Yellow FCF in food samples. Talanta (2012) 99. doi:10.1016/j.talanta.2012.05.029.
3. [3] Robens JF, Dill GS, Ward JM, Joiner JR, Griesemer RA, Douglas JF. Thirteen-week subchronic toxicity studies of Direct Blue 6, Direct Black 38, and Direct Brown 95 dyes. Topics in Catalysis (1980) 54(3). doi:10.1016/0041-008X(80)90170-2.
4. [4] Fazeli S, Sohrabi B, Tehrani-Bagha AR. The study of Sunset Yellow anionic dye interaction with gemini and conventional cationic surfactants in aqueous solution. Dyes and Pigments (2012) 95(ue 3)). doi:10.1016/j.dyepig.2012.03.022.
5. [5] Amchova P, Kotolova H, Ruda-Kucerova J. Health safety issues of synthetic food colorants. Regulatory Toxicology and Pharmacology (2015) 73(3):914–922. doi:10.1016/j.yrtph.2015.09.026.
6. [6] Ghoneim MM, El-Desoky HS, Zidan NM. Electro-Fenton oxidation of Sunset Yellow FCF azo-dye in aqueous solutions. Desalination (2011) 274(1–3). doi:10.1016/j.desal.2011.01.062.
7. [7] Lok K, Chung YW, Benzie I, Woo J. Synthetic colourings of some snack foods consumed by primary school children aged 8-9 years in Hong Kong. Food Additives and Contaminants: Part B Surveillance (2011) 4(3). doi:10.1080/19393210.2011.585246.
8. [8] Tripathi M, Khanna SK, Das M. Surveillance on use of synthetic colours in eatables vis a vis Prevention of Food Adulteration Act of India. Food Control (2007) 18(3). doi:10.1016/j.foodcont.2005.09.016.

9. [9] Alves SP, Brum DM, Andrade É, Pereira Netto AD. Determination of synthetic dyes in selected foodstuffs by high performance liquid chromatography with UV-DAD detection. Food Chemistry (2008) 107(1). doi:10.1016/j.foodchem.2007.07.054.
10. [10] Hashem MM, Atta AH, Arbid MS, Nada SA, Asaad GF. Immunological studies on Amaranth, Sunset Yellow and Curcumin as food colouring agents in albino rats. Food and Chemical Toxicology (2010) 48(6):1581–1586. doi:10.1016/J.FCT.2010.03.028.
11. [11] Llamas NE, Garrido M, Nezio M, Band B. Second order advantage in the determination of amaranth, sunset yellow FCF and tartrazine by UV–vis and multivariate curve resolution-alternating least squares. Analytica Chimica Acta (2009) 655(1–2):38–42. doi:10.1016/J.ACA.2009.10.001.
12. [12] Mikkelsen H, Larsen JC, Tarding F. Hypersensitivity reactions to food colours with special reference to the natural colour annatto extract (butter colour. Archives of Toxicology (1978) I Suppl. 1. doi:10.1007/978-3-642-66896-8_16.
13. [13] Nettis E, Colanardi MC, Ferrannini A, Tursi A. Suspected tartrazine-induced acute urticaria/angioedema is only rarely reproducible by oral rechallenge. Clinical and Experimental Allergy (2003) 33(12). doi:10.1111/j.1365-2222.2003.01825.x.
14. [14] Mental Health in the United States: Prevalence of Diagnosis and Medication Treatment for Attention-Deficit/Hyperactivity Disorder—United States, 2003. JAMA (2005) 294(18):2293–2296. doi:10.1001/jama.294.18.2293-b.
15. [15] Bateman B, Warner JO, Hutchinson E, Dean T, Rowlandson P, Gant C, et al. The effects of a double blind, placebo controlled, artificial food colourings and benzoate preservative challenge on hyperactivity in a general population sample of preschool children. Archives of Disease in Childhood (2004) 89(6). doi:10.1136/adc.2003.031435.
16. [16] Chen H. Recent Advances in Azo Dye Degrading Enzyme Research. Current Protein & Peptide Science (2006) 7(2). doi:10.2174/138920306776359786.
17. [17] Brás R, Gomes A, Ferra M, Pinheiro HM, Gonçalves IC. Monoazo and diazo dye decolourisation studies in a methanogenic UASB reactor. Journal of Biotechnology (2005) 115(1). doi:10.1016/j.jbiotec.2004.08.001.
18. [18] Kiziltan T, Baran A, Kankaynar M, Şenol O, Sulukan E, Yildirim S, et al. Effects of the food colorant carmoisine on zebrafish embryos at a wide range of concentrations. Archives of Toxicology (2022) 96(4):1089–1099. doi:10.1007/s00204-022-03240-2.
19. [19] Atlı Şekeroğlu Z, Güneş B, Kontaş Yedier S, Şekeroğlu V, Aydın B. Effects of tartrazine on proliferation and genetic damage in human lymphocytes. Toxicology Mechanisms and Methods (2017) 27(5):370–375. doi:10.1080/15376516.2017.1296051.
20. [20] Elbanna K, Sarhan OM, Khider M, Elmogy M, Abulreesh HH, Shaaban MR. Microbiological, histological, and biochemical evidence for the adverse effects of food azo dyes on rats. Journal of Food and Drug Analysis (2017) 25(3):667–680. doi:10.1016/J.JFDA.2017.01.005.
21. [21] Chung KT, Stevens SE, Cerniglia CE. The reduction of azo dyes by the intestinal microflora. Critical Reviews in Microbiology (1992) 18(3). doi:10.3109/10408419209114557.
22. [22] Tsuboy MS, Angeli J, Mantovani MS, Knasmüller S, Umbuzeiro GA, Ribeiro LR. Genotoxic, mutagenic and cytotoxic effects of the commercial dye CI Disperse Blue 291 in the human hepatic cell line HepG2. Toxicology in Vitro (2007) 21(8):1650–1655. doi:10.1016/J.TIV.2007.06.020.
23. [23] Macioszek VK, Kononowicz AK. The evaluation of the genotoxicity of two commonly used food colors: Quinoline Yellow (E 104) and Brilliant Black BN (E 151. Cellular and Molecular Biology Letters (2004) 9(1).
24. [24] Feng J, Cerniglia CE, Chen H. Toxicological significance of azo dye metabolism by human intestinal microbiota. Frontiers in Bioscience - Elite (2012) 4 E(2. doi:10.2741/e400.
25. [25] DeVito SC. Predicting Azo Dye Toxicity. Critical Reviews in Environmental Science and Technology (1993) 23(3). doi:10.1080/10643389309388453.
26. [26] Kuswandi B, Futra D, Heng LY. Nanosensors for the Detection of Food Contaminants. In: Nanotechnology Applications in Food: Flavor, Stability, Nutrition and Safety (2017).
27. [27] Bezerra MS, Malaquias GS, Sodusa CE, de JM, Perodn AP. Cytotoxic and genotoxic potential of powdered juices. Food Science and Technology (Brazil (2016) 36(1):49–55. doi:10.1590/1678-457X.0006.
28. [28] J.E.C.F.A. Residue Monograph prepared by the meeting of the Joint FAO/WHO Expert Committee on Food Additives (JECFA. In: 82nd meeting 2016 Carob Bean Gum. In Joint FAO/WHO Expert Committee on Food Additives (2017).
29. [29] Sayed HM, Fouad D, Ataya FS, Hassan N, Fahmy MA. The modifying effect of selenium and vitamins A, C, and E on the genotoxicity induced by sunset yellow in male mice. Mutation Research/Genetic Toxicology and Environmental Mutagenesis (2012) 744(2):145–153. doi:10.1016/J.MRGENTOX.2012.02.003.
30. [30] Seesuriyachan P, Takenaka S, Kuntiya A, Klayraung S, Murakami S, Aoki K. Metabolism of azo dyes by Lactobacillus casei TISTR 1500 and effects of various factors on decolorization. Water Research (2007) 41(5):985–992. doi:10.1016/J.WATRES.2006.12.001.
31. [31] Pearce CI, Lloyd JR, Guthrie JT. The removal of colour from textile wastewater using whole bacterial cells: a review. Dyes and Pigments (2003) 58(3):179–196. doi:10.1016/S0143-7208(03)00064-0.
32. [32] Axon A, May F, Gaughan LE, Williams FM, Blain PG, Wright MC. Tartrazine and sunset yellow are xenoestrogens in a new screening assay to identify modulators of human oestrogen receptor transcriptional activity. Toxicology (2012) 298(1–3):40–51. doi:10.1016/J.TOX.2012.04.014.
33. [33] Şensoy E, Güneş E. Determination of the effect of sunset yellow on the morphological parameters of male mice during the development period. Food and Chemical Toxicology (2024) 188:114653. doi:10.1016/J.FCT.2024.114653.
34. [34] Christy LD, Vignesh K, Nellore J, Tippabathani J. Impact of food additives on neurodevelopmental processes in zebrafish (Danio rerio): Exploring circadian clock genes and dopamine system. Developmental Neurobiology (2024) 84(3):191–202. doi:10.1002/dneu.22947.
35. [35] Ershoff BH. Effects of diet on growth and survival of rats fed toxic levels of tartrazine. Journal of Nutrition (1977) 107(5). doi:10.1093/jn/107.5.822.
36. [36] Jiang LL, Li K, Yan DL, Yang MF, Ma L, Xie LZ. Toxicity Assessment of 4 Azo Dyes in Zebrafish Embryos. International Journal of Toxicology (2020) 39(2). doi:10.1177/1091581819898396.
37. [37] Joshi V, Pancharatna K. Food colorant Sunset Yellow (E110) intervenes developmental profile of zebrafish (Danio rerio. Journal of Applied Toxicology (2019) 39(4). doi:10.1002/jat.3747.
38. [38] Bhatt D, Vyas K, Singh S, John PJ, Soni IP. Sunset Yellow induced biochemical and histopathological alterations in rat brain sub-regions. Acta Histochemica (2024) 126(3). doi:10.1016/j.acthis.2024.152155.
39. [39] Salim EI, Elbassuny MI, Mahfouz ME, El Nashar EM, Alghamdi MA, El-Nablaway M, et al. Promoting effect of sunset yellow on N-methyl N-nitrosourea-induced rat mammary carcinogenesis: Implications of molecular mechanisms. Toxicology Letters (2024) 401:13–23. doi:10.1016/J.TOXLET.2024.08.008.
40. [40] Zahran SA, Mansour SM, Ali AE, Kamal SM, Römling U, El-Abhar HS, et al. Sunset Yellow dye effects on gut microbiota, intestinal integrity, and the induction of inflammasomopathy with pyroptotic signaling in male Wistar rats. Food and Chemical Toxicology (2024) 187:114585. doi:10.1016/J.FCT.2024.114585.
41. [41] Dara M, Nazari F, Dianatpour M, Karimi F, Alaee S, Shirazi R, et al. Effect of Sunset Yellow on Testis: Molecular Evaluation, and Protective Role of Coenzyme Q10 in Male Sprague-Dawley Rats. Cell Biochemistry and Biophysics (2024). doi:10.1007/s12013-024-01398-3.
42. [42] Karimi F, khodabandeh Z, Nazari F, Dara M, Masjedi F, Momeni-Moghaddam M. Post-Weaning Exposure to Sunset Yellow FCF Induces Changes in Testicular Tight and Gap Junctions in Rats: Protective Effects of Coenzyme Q10. Reproductive Sciences (2023) 30(10):2962–2972. doi:10.1007/s43032-023-01240-w.
43. [43] Pan X, Yu XZ, Qin P. Effects of two food colorants on catalase and trypsin: Binding evidences from experimental and computational analysis. Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy (2023) 297:122702. doi:10.1016/J.SAA.2023.122702.
44. [44] Poul M, Jarry G, Elhkim MO, Poul JM. Lack of genotoxic effect of food dyes amaranth, sunset yellow and tartrazine and their metabolites in the gut micronucleus assay in mice. Food and Chemical Toxicology (2009) 47(2):443–448. doi:10.1016/j.fct.2008.11.034.
45. [45] Souza C, Chapman JM, Silva TA, Silva Filho T, Dias CS, Oliveira NM, et al. Genotoxic and cytotoxic potential of food azodyes: preclinical safety assessment using the in vivo micronucleus assay. Brazilian Journal of Development (2022). doi:10.34117/bjdv8n8-158.
46. [46] Gupta S, Singh S, Yadav S, Cavallo C, Mourya D, Shukla P, et al. Sunset Yellow protects against oxidative damage in human keratinocyte-derived HaCaT cells and exhibits chemopreventive efficacy in DMBA/TPA-induced skin carcinogenesis (2023). doi:10.21203/rs.3.rs-3233668/v1.
47. [47] Yadav A, Kumar A, Tripathi A, Das M. Sunset yellow FCF, a permitted food dye, alters functional responses of splenocytes at non-cytotoxic dose. Toxicology Letters (2013) 217(3). doi:10.1016/j.toxlet.2012.12.016.
48. [48] Berktay E, Çelik İ, Çelik S. In ovo given sunset yellow adversely affects embryonic development of chick thymus and bursa Fabricii as evidenced by histological and enzyme histochemical findings. Beni-Suef University Journal of Basic and Applied Sciences (2023) 12(1). doi:10.1186/s43088-023-00399-0.
49. [49] Sharma G, Sharma S, Dixit A, Gautam D, Goyal RP. Effect of Kesari powder on haematological and serological parameters in female Swiss albino MICE. Pharmacologyonline (2010) 2.