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Published in: BMC Complementary Medicine and Therapies 1/2021

01-12-2021 | Breast Cancer | Research

Oral administration of tartrazine (E102) accelerates the incidence and the development of 7,12-dimethylbenz(a) anthracene (DMBA)-induced breast cancer in rats

Authors: Stéphane Zingue, Elisabeth Louise Ndjengue Mindang, Florence Charline Awounfack, Abel Yanfou Kalgonbe, Moustapha Mohamet Kada, Dieudonné Njamen, Derek Tantoh Ndinteh

Published in: BMC Complementary Medicine and Therapies | Issue 1/2021

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Abstract

Background

Despite the considerable advances made in the treatment of cancer, it remains a global threat. Tartrazine (E102) is a synthetic dye widely used in food industries; it has recently been shown to induce oxidative stress (a well known risk factor of cancer) in rat tissues. The present work therefore aimed to assess the impact of a regular consumption of tartrazine on the incidence of breast cancer in rats.

Methods

Forty (40) Wistar rats aged 55 to 60 days were randomly assigned into 5 groups (n = 8) including two groups serving as normal controls and receiving distilled water (NOR) or tartrazine (NOR + TARZ). The three remaining groups were exposed to the carcinogen DMBA (50 mg/kg) and treated for 20 weeks with either distilled water (DMBA), tartrazine 50 mg/kg (DMBA + TARZ) or a natural dye (DMBA + COL). The parameters evaluated were the incidence, morphology and some biomarkers (CA 15–3, estradiol and α-fetoprotein) of breast cancer. The oxidative status and histomorphology of the tumors were also assessed.

Results

A regular intake of tartrazine led to an early incidence of tumors (100% in rats that received TARZ only vs 80% in rats that received DMBA only), with significantly larger tumors (p < 0.001) (mass = 3500 mg/kg and volume = 4 cm3). The invasive breast carcinoma observed on the histological sections of the animals of the DMBA + TARZ group was more developed than those of the DMBA group. The increase in serum α-fetoprotein (p < 0.05) and CA 15–3 (p < 0.01) levels corroborate the changes observed in tumors. The presence of oxidative activity in animals of the DMBA + TARZ group was confirmed by a significant decrease (p < 0.001) in the activity of antioxidant enzymes (SOD and catalase) as well as the level of GSH and increase in the level of MDA compared to the rats of the DMBA and NOR groups.

Conclusion

Tartrazine therefore appears to be a promoter of DMBA-induced breast tumorigenesis in rats through its oxidative potential. This work encourages further studies on the mechanisms of action of tartrazine (E102) and its limits of use.
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Literature
1.
go back to reference Sarkar B, Ullah A, Islam S, Hossain S. Anticancer potential of medicinal plants from Bangladesh and their effective compounds against cancer. J PharmacognPhytochem. 2019;8:827–33. Sarkar B, Ullah A, Islam S, Hossain S. Anticancer potential of medicinal plants from Bangladesh and their effective compounds against cancer. J PharmacognPhytochem. 2019;8:827–33.
2.
go back to reference Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer JClin. 2018;68:394–424. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer JClin. 2018;68:394–424.
3.
go back to reference Siegel RL, Miller KD, Jemal A. Cancer statistics, (2018). CA Cancer J Clin. 2018;68:7–30.PubMed Siegel RL, Miller KD, Jemal A. Cancer statistics, (2018). CA Cancer J Clin. 2018;68:7–30.PubMed
5.
go back to reference Lalloo E, Evans DG. Familiar breast cancer. Clin Genet. 2012;82:105–14.PubMed Lalloo E, Evans DG. Familiar breast cancer. Clin Genet. 2012;82:105–14.PubMed
6.
go back to reference Gelboin HV. Benzo[alpha]pyrene metabolism, activation and carcinogenesis: Role and regulation of mixed-function oxidases and related enzymes. Physiol Rev. 1980;60:1107–66.PubMed Gelboin HV. Benzo[alpha]pyrene metabolism, activation and carcinogenesis: Role and regulation of mixed-function oxidases and related enzymes. Physiol Rev. 1980;60:1107–66.PubMed
7.
go back to reference Leung HY, Yung LH, Poon CH, Shi G, Lu AL, Leung LK. Genistein protects against polycyclic aromatic hydrocarbon-induced oxidative DNA damage in non-cancerous breast cells MCF-10A. Br J Nutr. 2009;101:257–62.PubMed Leung HY, Yung LH, Poon CH, Shi G, Lu AL, Leung LK. Genistein protects against polycyclic aromatic hydrocarbon-induced oxidative DNA damage in non-cancerous breast cells MCF-10A. Br J Nutr. 2009;101:257–62.PubMed
8.
go back to reference Brinton LA, Awuah B, Nat C-LJ, Wiafe-Addai B, Ansong D, Nyarko KM, et al. Design considerations for identifying breast cancer risk factors in a population-based study in Africa. Int J Cancer. 2017;140:2667–77.PubMedPubMedCentral Brinton LA, Awuah B, Nat C-LJ, Wiafe-Addai B, Ansong D, Nyarko KM, et al. Design considerations for identifying breast cancer risk factors in a population-based study in Africa. Int J Cancer. 2017;140:2667–77.PubMedPubMedCentral
9.
go back to reference Vidotti EC, Cancino JC, Oliviera CC, Rollemberg ME. Simultaneous determination of food dyes by first derivative spectrophotometry with sorption onto polyurethane foam. Anal Sci. 2005;21:149–53.PubMed Vidotti EC, Cancino JC, Oliviera CC, Rollemberg ME. Simultaneous determination of food dyes by first derivative spectrophotometry with sorption onto polyurethane foam. Anal Sci. 2005;21:149–53.PubMed
10.
go back to reference Mansour HB, Corroler D, Barillier D, Kamel G, Chekir L, Mosrati R. Evaluation of genotoxicity and pro-oxidant effect of the azo dyes: acids yellow 17, violet 7 and orange 52, and of their degradation products by Pseudomonas putida mt-2. Food ChemToxicol. 2007;45:1670–7. Mansour HB, Corroler D, Barillier D, Kamel G, Chekir L, Mosrati R. Evaluation of genotoxicity and pro-oxidant effect of the azo dyes: acids yellow 17, violet 7 and orange 52, and of their degradation products by Pseudomonas putida mt-2. Food ChemToxicol. 2007;45:1670–7.
11.
go back to reference Husain A, Sawaya W, Al-Omair A, Al-Zenki S, Al-Amiri H, Ahmed N, et al. Estimates of dietary exposure of children to artificial food colours in Kuwait. Food Addit Contam. 2006;23:245–51.PubMed Husain A, Sawaya W, Al-Omair A, Al-Zenki S, Al-Amiri H, Ahmed N, et al. Estimates of dietary exposure of children to artificial food colours in Kuwait. Food Addit Contam. 2006;23:245–51.PubMed
12.
go back to reference Engel F, Pinto L, Ciampo L, Lorenzi L, Heyder C, Hader D, et al. Comparative toxicity of physiological and biochemical parameters in Euglena gracilisto short-term exposure to potassium sorbate. Ecotoxicology. 2015;24:153–62.PubMed Engel F, Pinto L, Ciampo L, Lorenzi L, Heyder C, Hader D, et al. Comparative toxicity of physiological and biochemical parameters in Euglena gracilisto short-term exposure to potassium sorbate. Ecotoxicology. 2015;24:153–62.PubMed
13.
go back to reference Khayyat L, Essawy A, Sorour J, Soffar A. Tartrazine induces structural and functional aberrations and genotoxic effects in vivo. Peer J. 2017;5:e3041.PubMedPubMedCentral Khayyat L, Essawy A, Sorour J, Soffar A. Tartrazine induces structural and functional aberrations and genotoxic effects in vivo. Peer J. 2017;5:e3041.PubMedPubMedCentral
14.
go back to reference Roomi MW, Niedzwiecki A, Rath M. Scientific evaluation of dietary factors in cancer. J Nutri Med Diet Care. 2018;4:029. Roomi MW, Niedzwiecki A, Rath M. Scientific evaluation of dietary factors in cancer. J Nutri Med Diet Care. 2018;4:029.
15.
go back to reference Erdemli Z, Altinoz E, Erdemli ME, Gul M, Bag HG, Gul S. Ameliorative effects of crocin on tartrazine dye-induced pancreatic adverse effects: a biochemical and histological study. Environ Sci Pollut Res Int. 2021;28:2209–18.PubMed Erdemli Z, Altinoz E, Erdemli ME, Gul M, Bag HG, Gul S. Ameliorative effects of crocin on tartrazine dye-induced pancreatic adverse effects: a biochemical and histological study. Environ Sci Pollut Res Int. 2021;28:2209–18.PubMed
16.
go back to reference Erdemli ME, Gul M, Altinoz E, Zayman E, Aksungur Z, Bag HG. The protective role of crocin in tartrazine induced nephrotoxicity in Wistar rats. Biomed Pharmacother. 2017;96:930–5.PubMed Erdemli ME, Gul M, Altinoz E, Zayman E, Aksungur Z, Bag HG. The protective role of crocin in tartrazine induced nephrotoxicity in Wistar rats. Biomed Pharmacother. 2017;96:930–5.PubMed
17.
go back to reference Mpountoukas P, Pantazaki A, Kostareli E, Christodoulou DK, Poliliou S, Mourelatos C, et al. Cytogenetic evaluation and DNA interaction studies of the food colorants amaranth, eythrosine and tartrazine. Food ChemToxicol. 2010;48:2934–44. Mpountoukas P, Pantazaki A, Kostareli E, Christodoulou DK, Poliliou S, Mourelatos C, et al. Cytogenetic evaluation and DNA interaction studies of the food colorants amaranth, eythrosine and tartrazine. Food ChemToxicol. 2010;48:2934–44.
18.
go back to reference El-desoky GE, Abdel-ghaffar A, Al-othman ZA, Habila MA, Al-sheikh YA, Ghneim HK, et al. Curcumin protects against tartrazine-mediated oxidative stress and hepatotoxicity in male rats. Eu Rev Med Pharmacol Sci. 2017;21:635–45. El-desoky GE, Abdel-ghaffar A, Al-othman ZA, Habila MA, Al-sheikh YA, Ghneim HK, et al. Curcumin protects against tartrazine-mediated oxidative stress and hepatotoxicity in male rats. Eu Rev Med Pharmacol Sci. 2017;21:635–45.
19.
go back to reference Al-Seeni MN, El Rabey HA, Al-Hamed AM, Zamazami MA. Nigella sativa oil protects against tartrazine toxicity in male rats. Toxicol Rep. 2018;5:146–55.PubMed Al-Seeni MN, El Rabey HA, Al-Hamed AM, Zamazami MA. Nigella sativa oil protects against tartrazine toxicity in male rats. Toxicol Rep. 2018;5:146–55.PubMed
20.
go back to reference Mefegue AF, Michel T, Kamto ELD, Kenmogne LV, Awounfack CF, Noundou XS, et al. Anti-breast cancer potential of Anonidium mannii (Oliv.) Engl. & Diels barks ethanolic extract: UPLC-ESI-QTOF-MS detection of anticancer alkaloids. J Ethnopharmacol. 2021;276:114–31. Mefegue AF, Michel T, Kamto ELD, Kenmogne LV, Awounfack CF, Noundou XS, et al. Anti-breast cancer potential of Anonidium mannii (Oliv.) Engl. & Diels barks ethanolic extract: UPLC-ESI-QTOF-MS detection of anticancer alkaloids. J Ethnopharmacol. 2021;276:114–31.
21.
go back to reference Das A, Mukherjee A. Genotoxicity Testing of the Food Colours Amaranth and Tartrazine. Int J Hum Genet. 2017;4:277–80. Das A, Mukherjee A. Genotoxicity Testing of the Food Colours Amaranth and Tartrazine. Int J Hum Genet. 2017;4:277–80.
22.
go back to reference Kubatka P, Uramova S, Kello M, Kajo K, Samec M, Jasek K, et al. Anticancer Activities of Thymus vulgaris L. in Experimental Breast Carcinoma In Vivo and In Vitro. Int J Mol Sci. 2019;20:1749.PubMedCentral Kubatka P, Uramova S, Kello M, Kajo K, Samec M, Jasek K, et al. Anticancer Activities of Thymus vulgaris L. in Experimental Breast Carcinoma In Vivo and In Vitro. Int J Mol Sci. 2019;20:1749.PubMedCentral
23.
go back to reference Gonal AG, Bardwill GS, David MM. Determination of serum proteins by the means of biuret reactions. J Biol Chem. 1949;177:751–66. Gonal AG, Bardwill GS, David MM. Determination of serum proteins by the means of biuret reactions. J Biol Chem. 1949;177:751–66.
24.
go back to reference Misra F. Determination of the level of superoxide dismutase in whole blood. New Haven: Yale University, Press; 1972. p. 101–9. Misra F. Determination of the level of superoxide dismutase in whole blood. New Haven: Yale University, Press; 1972. p. 101–9.
25.
go back to reference Wilbur KM, Bernheim F, Shapiro OW. Determination of lipid peroxidation. Arch Biochem Biophys. 1949;24:305–10. Wilbur KM, Bernheim F, Shapiro OW. Determination of lipid peroxidation. Arch Biochem Biophys. 1949;24:305–10.
26.
go back to reference Sinha AK. Colorimetric assay of catalase. Anal Brochem. 1972;47:389–94. Sinha AK. Colorimetric assay of catalase. Anal Brochem. 1972;47:389–94.
27.
go back to reference Ellman GL. Tissue sulfhydryl group. Arch Biochem Biophys. 1959;82:70–7.PubMed Ellman GL. Tissue sulfhydryl group. Arch Biochem Biophys. 1959;82:70–7.PubMed
28.
go back to reference Russo J, Russo IH. Atlas and histologic classification of Tumors of rat mammary gland. J Mammary Gland Biol Neoplasia. 2000;5:187–200.PubMed Russo J, Russo IH. Atlas and histologic classification of Tumors of rat mammary gland. J Mammary Gland Biol Neoplasia. 2000;5:187–200.PubMed
29.
go back to reference Harbeck N, Cortes J, Gnant M, Houssami N, Poortmans P, Ruddy K, et al. Breast cancer. Nat Rev Dis Primers. 2019;5:66.PubMed Harbeck N, Cortes J, Gnant M, Houssami N, Poortmans P, Ruddy K, et al. Breast cancer. Nat Rev Dis Primers. 2019;5:66.PubMed
30.
go back to reference Sores BM, Araujo TMT, Ramos JAB, Pinto LC, Khayat BM, Bahia MDOB, et al. Effect on repair in human lymphocytes exposed to the food dye tartrazine yellow. Anticancer Res. 2015;35:1465–74. Sores BM, Araujo TMT, Ramos JAB, Pinto LC, Khayat BM, Bahia MDOB, et al. Effect on repair in human lymphocytes exposed to the food dye tartrazine yellow. Anticancer Res. 2015;35:1465–74.
31.
go back to reference Nguedia MY, Tueche AB, Yaya AJG, Yadji V, Ndinteh DT, Njamen D, et al. Daucosterol from Crateva adansonii DC (Capparaceae) reduces 7,12-dimethylbenz(a)anthracene-induced mammary tumors in Wistar rats. Environ Toxicol. 2020;2020:1–12. Nguedia MY, Tueche AB, Yaya AJG, Yadji V, Ndinteh DT, Njamen D, et al. Daucosterol from Crateva adansonii DC (Capparaceae) reduces 7,12-dimethylbenz(a)anthracene-induced mammary tumors in Wistar rats. Environ Toxicol. 2020;2020:1–12.
32.
go back to reference Himri I, Souna F, Aziz M, Hakkou A, Saalaoui E. DNA damage induced by tartrazine in rat whole blood using comet assay (Single cell Gel Electrophoresis). Adv Environ Biol. 2012;6:2875–81. Himri I, Souna F, Aziz M, Hakkou A, Saalaoui E. DNA damage induced by tartrazine in rat whole blood using comet assay (Single cell Gel Electrophoresis). Adv Environ Biol. 2012;6:2875–81.
33.
go back to reference Datta P, Lundin-Schiller S. Estrogenecity of the synthetic food colorants tartrazine, erythrosine B, and sudan I in an estrogen-responsive human breast cancer cell line. Estrogenecity of the synthetic food colorants tartrazine, erythrosine B, and sudan I in an estrogen-responsive human breast cancer cell line. J Tenn Acad Sci. 2008;83:45. Datta P, Lundin-Schiller S. Estrogenecity of the synthetic food colorants tartrazine, erythrosine B, and sudan I in an estrogen-responsive human breast cancer cell line. Estrogenecity of the synthetic food colorants tartrazine, erythrosine B, and sudan I in an estrogen-responsive human breast cancer cell line. J Tenn Acad Sci. 2008;83:45.
34.
go back to reference Axon A, May EBF, 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. Toxicol. 2012;298:40–51. Axon A, May EBF, 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. Toxicol. 2012;298:40–51.
35.
go back to reference Jilin H, Jinman Z, Ying C, Baosheng Z. A rat model of placental inflammation explains the unexplained elevated maternal serum alpha-fetoprotein associated with adverse pregnancy outcomes. J Obstet Gynaecol Res. 2019;45:10. Jilin H, Jinman Z, Ying C, Baosheng Z. A rat model of placental inflammation explains the unexplained elevated maternal serum alpha-fetoprotein associated with adverse pregnancy outcomes. J Obstet Gynaecol Res. 2019;45:10.
36.
go back to reference Moldogazieva NT, Terentiev AA. Structural and functional mapping of alpha-fetoproteine. Biochem. 2006;71:120–32. Moldogazieva NT, Terentiev AA. Structural and functional mapping of alpha-fetoproteine. Biochem. 2006;71:120–32.
37.
go back to reference Yager JD, Davidson NE. Estrogen carcinogenesis in breast cancer. N Engl J Med. 2006;354:270–82.PubMed Yager JD, Davidson NE. Estrogen carcinogenesis in breast cancer. N Engl J Med. 2006;354:270–82.PubMed
38.
go back to reference Shruti S, Muddeshwar M, Suchet G, Ganesh N. Antioxidant enzymes and lipid peroxidation in different stages of breast cancer. Free Radic Res. 2009;38:81–7. Shruti S, Muddeshwar M, Suchet G, Ganesh N. Antioxidant enzymes and lipid peroxidation in different stages of breast cancer. Free Radic Res. 2009;38:81–7.
39.
go back to reference Haleng J, Pincemail J, Defraigne J, Charlier C, Chapelle J. Le stress oxydant. Rev Med Liège. 2007;10:628–38. Haleng J, Pincemail J, Defraigne J, Charlier C, Chapelle J. Le stress oxydant. Rev Med Liège. 2007;10:628–38.
40.
go back to reference Michel F, Bonnefont-Rousselot D, Mas E, Drai J, Thérond P. Biomarqueurs de la peroxydation lipidique : aspects analytiques. Ann Biol Clin. 2008;66:605–20. Michel F, Bonnefont-Rousselot D, Mas E, Drai J, Thérond P. Biomarqueurs de la peroxydation lipidique : aspects analytiques. Ann Biol Clin. 2008;66:605–20.
41.
go back to reference Saxena B, Sharma S. Food color induced hepatotoxicity in Swiss albino rats, Rattus norvegicus. Toxicol Int. 2015;22:152–7.PubMedPubMedCentral Saxena B, Sharma S. Food color induced hepatotoxicity in Swiss albino rats, Rattus norvegicus. Toxicol Int. 2015;22:152–7.PubMedPubMedCentral
42.
go back to reference Balasubramanian K, Padma PR. Anticancer Activity of Zea mays Leaf Extracts on Oxidative Stress-induced Hep2 Cells. J Acupunct Meridian Stud. 2013;6:149–58.PubMed Balasubramanian K, Padma PR. Anticancer Activity of Zea mays Leaf Extracts on Oxidative Stress-induced Hep2 Cells. J Acupunct Meridian Stud. 2013;6:149–58.PubMed
43.
go back to reference Ying P, Yunen L, Xiaodong X. Change Trends of Organ Weight Background Data in Sprague Dawley Rats at Different Ages. J Toxicol Pathol. 2013;26:29–34. Ying P, Yunen L, Xiaodong X. Change Trends of Organ Weight Background Data in Sprague Dawley Rats at Different Ages. J Toxicol Pathol. 2013;26:29–34.
Metadata
Title
Oral administration of tartrazine (E102) accelerates the incidence and the development of 7,12-dimethylbenz(a) anthracene (DMBA)-induced breast cancer in rats
Authors
Stéphane Zingue
Elisabeth Louise Ndjengue Mindang
Florence Charline Awounfack
Abel Yanfou Kalgonbe
Moustapha Mohamet Kada
Dieudonné Njamen
Derek Tantoh Ndinteh
Publication date
01-12-2021
Publisher
BioMed Central
Published in
BMC Complementary Medicine and Therapies / Issue 1/2021
Electronic ISSN: 2662-7671
DOI
https://doi.org/10.1186/s12906-021-03490-0

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