Toxicological Research

Korean Society of Toxicology & Korea Environmental Mutagen Society (한국독성학회)
권호 표지
DOI QR코드

DOI QR Code

Effect of tartrazine on digestive enzymatic activities: in vivo and in vitro studies

  • Ameur, Fatma Zohra (Laboratory of Physiology of Nutrition and Food Security, University Oran1 Ahmed BenBella) ;
  • Mehedi, Nabila (Laboratory of Physiology of Nutrition and Food Security, University Oran1 Ahmed BenBella) ;
  • Rivas, Cristina Soler (Department of Production and Characterization of Novel Foods, CIAL-Research Institute in Food Science (UAM-CSIC)) ;
  • Gonzalez, Antonio (Institute of Molecular Pathology Biomarkers, University of Extremadura) ;
  • Kheroua, Omar (Laboratory of Physiology of Nutrition and Food Security, University Oran1 Ahmed BenBella) ;
  • Saidi, Djamel (Laboratory of Physiology of Nutrition and Food Security, University Oran1 Ahmed BenBella)
  • Received : 2019.06.17
  • Accepted : 2019.08.22
  • Published : 2020.04.15
⟨ Previous Next ⟩

Abstract

Tartrazine (E102) is a synthetic food coloring, which belongs to the class of mono azo dyes and is known to cause numerous health problems. The current research aimed to evaluate the effect of this food dye on the enzymatic activity of amylase, lipase and proteases after a subchronic ingestion in Swiss mice. Additionally, an in vitro digestion model was used to highlight the relationship between the probable toxicity of tartrazine and the nature of the food ingested. The results show that there were no adverse effects of tartrazine on the body weight gain, and on amylase or lipase activities. However, in the high dose of tartrazine (0.05%) group, a significant decrease in trypsin and chymotrypsin enzymatic activities were observed. Regarding the in vitro digestion model, our findings show that there were no changes in the trypsin and chymotrypsin enzymatic activities either using 7.5 or 75 mg of tartrazine mixed with rice, butter or milk. We conclude that excessive consumption of tartrazine appears to alter the enzymatic activity of proteases in vivo which may have deleterious consequences on digestion. Even thought the dose close to the acceptable daily intake does not affect those activities, a strict control of tartrazine dose in high-consumption foods especially among children is an indispensable task.

Keywords

Acknowledgement

This research was supported by the Directorate General for Scientific Research and Technological Development (DGRSDT, MESRS, Algeria). We appreciate the assistance and advices of Prof Cristina Trenzado (Faculty of Sciences, University of Granada) about the enzymatic activities' measurement.

References

  1. Mpountoukas P, Pantazaki A, Kostareli E, Christodoulou P, Kareli D, Poliliou S, Mourelatos C, Lambropoulou V, Lialiaris T (2010) Cytogenetic evaluation and DNA interaction studies of the food colorants amaranth, erythrosine and tartrazine. Food Chem Toxicol 48:2934-2944 https://doi.org/10.1016/j.fct.2010.07.030
  2. Greluk M, Hubicki Z (2011) Efficient removal of Acid Orange 7 dye from water using the strongly basic anion exchange resin Amberlite IRA-958. Desalination 278:219-226 https://doi.org/10.1016/j.desal.2011.05.024
  3. Amin KA, Abdel Hameid II H, Abd Elsttar AH (2010) Effect of food azo dyes tartrazine and carmoisine on biochemical parameters related to renal, hepatic function and oxidative stress biomarkers in young male rats. Food Chem Toxicol 48:2994-2999 https://doi.org/10.1016/j.fct.2010.07.039
  4. Mehedi N, Ainad-Tabet S, Mokrane N, Addou S, Zaoui C, Kheroua O, Saidi D (2009) Reproductive toxicology of tartrazine (FD and C Yellow No. 5) in Swiss albino mice. Am J Pharmacol Toxicol 4:130-135 https://doi.org/10.3844/ajptsp.2009.130.135
  5. JECFA (1964) Specifications for the identity and purity of food additives and their toxicological evaluation: food colours and some antimicrobials and antioxidants, eighth report of the Joint FAO/WHO Expert Committee on Food Additives 8-17 December. World Health Organization, Geneva
  6. JECFA (2016) Compendium of food additive specifications: eighty-second report of the Joint FAO/WHO Expert Committee on Food Additives. FAO JECFA Monographs, Rome
  7. Sawaya W, Husain A, Al-Otaibi J, Al-Foudari M, Hajji A (2008) Colour additive levels in foodstuffs commonly consumed by children in Kuwait. Food Control 19:98-105 https://doi.org/10.1016/j.foodcont.2007.06.001
  8. Hashem MM, Atta AH, Arbid MS, Nada SA, Asaad GF (2010) Immunological studies on Amaranth, Sunset Yellow and Curcumin as food colouring agents in albino rats. Food Chem Toxicol 48:1581-1586 https://doi.org/10.1016/j.fct.2010.03.028
  9. Sasaki YF, Kawaguchi S, Kamaya A, Ohshita M, Kabasawa K, Iwama K, Taniguchi K, Tsuda S (2002) The comet assay with 8 mouse organs: results with 39 currently used food additives. Mutat Res 519:103-119 https://doi.org/10.1016/S1383-5718(02)00128-6
  10. Hassan G (2010) Effects of some synthetic coloring additives on DNA damage and chromosomal aberrations of rats. Arab J Biotechnol 13:13-24
  11. Khayyat L, Essawy A, Sorour J, Soffar A (2017) Tartrazine induces structural and functional aberrations and genotoxic effects in vivo. PeerJ 5:30-41
  12. Himri I, Bellahcen S, Souna F, Belmekki F, Aziz M, Bnouham M, Zoheir J, Berkia Z, Mekhfi H, Saalaoui E (2011) A 90-day oral toxicity study of tartrazine, a synthetic food dye, in wistar rats. Int J Pharm Pharm Sci 3:159-169
  13. Visweswaran B, Krishnamoorthy G (2012) Oxidative stress by tartrazine in the testis of Wistar rats. J Pharm Biol Sci 2:44-49
  14. Hashem MM, Abd-Elhakim YM, Abo-EL-Sooud K, Eleiwa MM (2019) Embryotoxic and teratogenic effects of tartrazine in rats. Toxicol Res 35:75 https://doi.org/10.5487/TR.2019.35.1.075
  15. Demirkol O, Zhang X, Ercal N (2012) Oxidative effects of Tartrazine (CAS No. 1934-21-0) and New Coccin (CAS No. 2611-82-7) azo dyes on CHO cells. J Verbrauch Lebensm 7:229-236 https://doi.org/10.1007/s00003-012-0782-z
  16. Jones R, Ryan A, Wright S (1964) The metabolism and excretion of tartrazine in the rat, rabbit and man. Food Cosmet Toxicol 2:447-452 https://doi.org/10.1016/S0015-6264(64)80287-X
  17. EFSA (2009) Scientific opinion on the reevaluation Tartrazine (E 102) on request from the European Commission, Panel on Food Additives and Nutrient Sources added to Food (ANS), Italy, p 8
  18. Ghonimi WA, Elbaz A (2015) Histological changes of selected westar rat tissues following the ingestion of tartrazine with special emphasis on the protective effect of royal jelly and cod liveroil. J Cytol Histol 6:1
  19. Moutinho I, Bertges L, Assis R (2007) Prolonged use of the food dye tartrazine (FD&C yellow n° 5) and its effects on the gastric mucosa of Wistar rats. Braz J Biol 67:141-145 https://doi.org/10.1590/S1519-69842007000100019
  20. Wang J, Liu R, Qin P (2012) Toxic interaction between acid yellow 23 and trypsin: spectroscopic methods coupled with molecular docking. J Biochem Mol Toxicol 26:360-367 https://doi.org/10.1002/jbt.21430
  21. Silva C, Terra W, de Sa MG, Samuels R, Isejima E, Bifano T, Almeida J (2001) Induction of digestive α-amylases in larvae of Zabrotes subfasciatus (Coleoptera: Bruchidae) in response to ingestion of common bean α-amylase inhibitor 1. J Insect Physiol 47:1283-1290 https://doi.org/10.1016/S0022-1910(01)00115-9
  22. Furukawa I, Kurooka S, Arisue K, Kohda K, Hayashi C (1982) Assays of serum lipase by the" BALB-DTNB method" mechanized for use with discrete and continuous-flow analyzers. Clin Chem 28:110-113 https://doi.org/10.1093/clinchem/28.1.110
  23. Faulk C, Benninghoff AD, Holt G (2007) Ontogeny of the gastrointestinal tract and selected digestive enzymes in cobia Rachycentron canadum (L.). J Fish Biol 70:567-583 https://doi.org/10.1111/j.1095-8649.2007.01330.x
  24. Rick W (1976) Chymotrypsin. In: Hu B (ed) Methods of enzymatic analysis, 2nd English edn. Verlag Chemie, New York, pp 1006-1012
  25. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265-275 https://doi.org/10.1016/S0021-9258(19)52451-6
  26. Martin D, Nieto-Fuentes JA, Senorans FJ, Reglero G, Soler-Rivas C (2010) Intestinal digestion of fish oils and ω-3 concentrates under in vitro conditions. Eur J Lipid Sci Technol 112:1315-1322 https://doi.org/10.1002/ejlt.201000329
  27. Arhakis A, Karagiannis V, Kalfas S (2013) Salivary alpha-amylase activity and salivary flow rate in young adults. Open Dent J.= 7:7 https://doi.org/10.2174/1874210601307010007
  28. Jiang Z, Zhou Y, Lu F, Han Z, Wang T (2008) Effects of different levels of supplementary alpha-amylase on digestive enzyme activities and pancreatic amylase mRNA expression of young broilers. Asian-Australas J Anim Sci 21:97-102 https://doi.org/10.5713/ajas.2008.70110
  29. Xu Z, Hu C, Xia M, Zhan X, Wang M (2003) Effects of dietary fructooligosaccharide on digestive enzyme activities, intestinal microflora and morphology of male broilers. Poult Sci 82:1030-1036 https://doi.org/10.1093/ps/82.6.1030
  30. Tanaka T (2006) Reproductive and neurobehavioural toxicity study of tartrazine administered to mice in the diet. Food Chem Toxicol 44:179-187 https://doi.org/10.1016/j.fct.2005.06.011
  31. Guendouz M, Mehedi N, Zaoui C, Saidi D, Kheroua O (2013) Immune response after tartrazine subchronic ingestion in Swiss albino mice. J Pharm Pharm Sci 5:584-592
  32. Ezeuko Vitalis C, Nwokocha Chukwuemeka R, Mounmbegna Philippe E, Nriagu Chinonso C (2007) Effects of Zingiber officinale on liver function of mercuric chloride-induced hepatotoxicity in adult Wistar rats. Electron J Biomed 3:40-45
  33. Keller J, Layer P (2014) The pathophysiology of malabsorption. Visc Med 30:150-154 https://doi.org/10.1159/000364794
  34. Buddington RK, Diamond JM (1989) Ontogenetic development of intestinal nutrient transporters. Annu Rev Physiol 51:601-617 https://doi.org/10.1146/annurev.ph.51.030189.003125
  35. Vaysse N (2005) Physiologie du pancreas exocrine. Ann Gastroenterol Hepatol 2:59-74
  36. Otsuki M, Williams JA (1982) Effect of diabetes mellitus on the regulation of enzyme secretion by isolated rat pancreatic acini. J Clin Invest 70:148-156 https://doi.org/10.1172/JCI110588
  37. Al-Shabib NA, Khan JM, Alsenaidy MA, Alsenaidy AM, Khan MS, Husain FM, Khan MR, Naseem M, Sen P, Alam P (2018) Unveiling the stimulatory effects of tartrazine on human and bovine serum albumin fibrillogenesis: spectroscopic and microscopic study. Spectrochim Acta A Mol Biomol Spectrosc 191:116-124 https://doi.org/10.1016/j.saa.2017.09.062
  38. Ang WS, Elimelech M (2007) Protein (BSA) fouling of reverse osmosis membranes: implications for wastewater reclamation. J Membr Sci 296:83-92 https://doi.org/10.1016/j.memsci.2007.03.018
  39. Nilsson MT, Krajewski WW, Yellagunda S, Prabhumurthy S, Chamarahally GN, Siddamadappa C, Srinivasa BR, Yahiaoui S, Larhed M, Karlen A (2009) Structural basis for the inhibition of Mycobacterium tuberculosis glutamine synthetase by novel ATP-competitive inhibitors. J Mol Biol 393:504-513 https://doi.org/10.1016/j.jmb.2009.08.028
  40. Siraki AG, Chan TS, Galati G, Teng S, O'Brien PJ (2002) N-oxidation of aromatic amines by intracellular oxidases. Drug Metab Rev 34:549-564 https://doi.org/10.1081/DMR-120005657
  41. Sweeney EA, Chipman JK, Forsythe SJ (1994) Evidence for direct-acting oxidative genotoxicity by reduction products of azo dyes. Environ Health Perspect 102:119-122
  42. Hur SJ, Lim BO, Decker EA, McClements DJ (2011) In vitro human digestion models for food applications. Food Chem 125:1-12 https://doi.org/10.1016/j.foodchem.2010.08.036
  43. Boisen S, Eggum B (1991) Critical evaluation of in vitro methods for estimating digestibility in simple-stomach animals. Nutr Res Rev 4:141-162 https://doi.org/10.1079/NRR19910012
  44. Menard O, Dupont D (2014) Atouts et limites des modeles de digestion gastro-intestinale: de l'in vitro a l'in vivo. Innov Agron 36:27-41
  45. Goldenring J, Batter D, Shaywitz B (1982) Sulfanilic acid: behavioral change related to azo food dyes in developing rats. Neurobehav Toxicol Teratol 4:43-49
  46. Ameur FZ, Mehedi N, Kheroua O, Saidi D, Salido GM, Gonzalez A (2018) Sulfanilic acid increases intracellular free-calcium concentration, induces reactive oxygen species production and impairs trypsin secretion in pancreatic AR42J cells. Food Chem Toxicol 120:71-80 https://doi.org/10.1016/j.fct.2018.07.001
  47. Boussada M, Lamine J, Bini I, Abidi N, Lasrem M, El-Fazaa S, El-Golli N (2017) Assessment of a sub-chronic consumption of tartrazine (E102) on sperm and oxidative stress features in Wistar rat. Int Food Res J 24:1473-1481
  48. Cemek M, Buyukokuroglu ME, Sertkaya F, Alpdagtas S, Hazini A, Onul A, Gones S (2014) Effects of food color additives on antioxidant functions and bioelement contents of liver, kidney and brain tissues in rats. J Food Nutr Res 2:686-691 https://doi.org/10.12691/jfnr-2-10-6
  49. El Golli N (2016) Toxicity induced after subchronic administration of the synthetic food dye tartrazine in adult rats, role of oxidative stress. Recent Adv Biol Med 2:20-28 https://doi.org/10.18639/RABM.2016.02.284474
  50. Haleng J, Pincemail J, Defraigne J-O, Charlier C, Chapelle J-P (2007) Le stress oxydant. Rev Med Liege 62:628-638
  51. Migdal C, Serres M (2011) Especes reactives de l'oxygene et stress oxydant. M/S Rev 27:405-412
  52. Salimi A, Talatappe BS, Pourahmad J (2017) Xylene induces oxidative stress and mitochondria damage in isolated human lymphocytes. Toxicol Res 33:233 https://doi.org/10.5487/TR.2017.33.3.233
  53. Onyema OO, Farombi EO, Emerole GO, Ukoha AI, Onyeze GO (2006) Effect of vitamin E on monosodium glutamate induced hepatotoxicity and oxidative stress in rats. Indian J Biochem Biophys 43:20-24
  54. Elhkim MO, Heraud F, Bemrah N, Gauchard F, Lorino T, Lambre C, Fremy JM, Poul J-M (2007) New considerations regarding the risk assessment on Tartrazine: an update toxicological assessment, intolerance reactions and maximum theoretical daily intake in France. Regul Toxicol Pharm 47:308-316 https://doi.org/10.1016/j.yrtph.2006.11.004

Cited by

  1. Detection of tartrazine in fake saffron containing products by a sensitive optical nanosensor vol.350, 2020, https://doi.org/10.1016/j.foodchem.2021.129197