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Differences in micronucleus frequency and acrylamide adduct levels with hemoglobin between vegetarians and non-vegetarians

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Abstract

Purpose

Nutrients and food constituents can prevent or contribute to genotoxicity. In this study, the possible influence of a vegetarian/non-vegetarian diet on genotoxic effects was investigated in 58 non-smoking healthy vegetarians (V) and non-vegetarians (NV), age 21–37 years from the Stockholm area in Sweden.

Methods

Physical activity and dietary habits were similar in both groups, with the exception of the intake of meat and fish. Using flow cytometry, we determined the formation of micronuclei (MN) in transferrin-positive immature peripheral blood reticulocytes (Trf-Ret) (Total: n = 53; V: n = 27; NV: n = 26). Dietary exposure to acrylamide was measured through hemoglobin (Hb) adducts in peripheral erythrocytes (Total: n = 53; V: n = 29; NV: n = 24). Hb adducts of both acrylamide and its genotoxic metabolite glycidamide were monitored as a measure of the corresponding in vivo doses.

Results

Our data demonstrated that compared with the non-vegetarians, the vegetarians exhibited lower frequencies of MN (fMN) in the Trf-Ret (p < 0.01, Student’s t test). A multivariate analysis demonstrated that there was no association between the fMN and factors such as age, sex, intake of vitamins/minerals, serum folic acid and vitamin B12 levels, physical activity, and body mass index. The mean Hb adduct levels of acrylamide and glycidamide showed no significant differences between vegetarians and non-vegetarians. Furthermore, there were no significant relationships between the adduct levels and fMN in the individuals. The ratio of the Hb adduct levels from glycidamide and acrylamide, however, showed a significant difference (p < 0.04) between the two groups.

Conclusions

These data suggest that the vegetarian diet might be beneficial in lowering genomic instability in healthy individuals. The measured Hb adduct levels indicate that the total intake of acrylamide does not differ between the two studied groups and does not contribute to the observed difference in fMN, although an influence of the diet on the metabolic rates of acrylamide was indicated. In addition, the observed significant difference in the background fMN in the two groups demonstrated that the MN analysis method has a sensitivity applicable to the biomonitoring of human lifestyle factors.

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Abbreviations

MN:

Micronuclei

Trf-Ret:

Transferrin-positive reticulocytes

fMN-Trf-Ret:

Frequency of micronucleated transferrin-positive reticulocytes

Hb:

Hemoglobin

MN:

Micronuclei

NV:

Non-vegetarians

Trf-Ret:

Transferrin-positive reticulocytes

V:

Vegetarians

References

  1. Mateuca R, Lombaert N, Aka PV, Decordier I, Kirsch-Volders M (2006) Chromosomal changes: induction, detection methods and applicability in human biomonitoring. Biochimie 88:1515–1531

    Article  CAS  Google Scholar 

  2. Bonassi S, El-Zein R, Bolognesi C, Fenech M (2010) Micronuclei frequency in peripheral blood lymphocytes and cancer risk: evidence from human studies. Mutagenesis 26:93–100

    Article  Google Scholar 

  3. Dertinger SD, Torous DK, Hayashi M, MacGregor JT (2011) Flow cytometric scoring of micronucleated erythrocytes: an efficient platform for assessing in vivo cytogenetic damage. Mutagenesis 26:139–145

    Article  CAS  Google Scholar 

  4. Fenech M (2003) Nutritional treatment of genome instability: a paradigm shift in disease prevention and in the setting of recommended dietary allowances. Nutr Res Rev 16:109–122

    Article  CAS  Google Scholar 

  5. Verhagen H, Rauma AL, Torronen R, de Vogel N, Bruijntjes-Rozier GC, Drevo MA, Bogaards JJ, Mykkanen H (1996) Effect of a vegan diet on biomarkers of chemoprevention in females. Hum Exp Toxicol 15:821–825

    Article  CAS  Google Scholar 

  6. Fenech M, Rinaldi J (1995) A comparison of lymphocyte micronuclei and plasma micronutrients in vegetarians and non-vegetarians. Carcinogenesis 16:223–230

    Article  CAS  Google Scholar 

  7. Tucker JD, Vanderlaan M, Kwan TC, Moore DH II, Felton JS (1993) Effects of diet and folate on levels of micronucleated polychromatic erythrocytes. Mutat Res 301:19–26

    Article  CAS  Google Scholar 

  8. Kazimirova A, Barancokova M, Krajcovicova-Kudlackova M, Volkovova K, Staruchova M, Valachovicova M, Paukova V, Blazicek P, Wsolova L, Dusinska M (2006) The relationship between micronuclei in human lymphocytes and selected micronutrients in vegetarians and non-vegetarians. Mutat Res 611:64–70

    Article  CAS  Google Scholar 

  9. Abramsson-Zetterberg L, Vikstrom AC, Tornqvist M, Hellenas KE (2008) Differences in the frequency of micronucleated erythrocytes in humans in relation to consumption of fried carbohydrate-rich food. Mutat Res Genet Toxicol Environ Mutagen 653:50–56

    Article  CAS  Google Scholar 

  10. Tareke E, Rydberg P, Karlsson P, Eriksson S, Tornqvist M (2002) Analysis of acrylamide, a carcinogen formed in heated foodstuffs. J Agric Food Chem 50:4998–5006

    Article  CAS  Google Scholar 

  11. European Food Safety Authority (EFSA) (2014) Draft scientific opinion on acrylamide in food, EFSA panel on contaminants in the food chain (CONTAM), pp. 303. http://www.efsa.europa.eu/en/topics/topic/acrylamide.htm. Accessed 12 Feb 2014

  12. Carere A (2006) Genotoxicity and carcinogenicity of acrylamide: a critical review. Ann Ist Super Sanita 42:144–155

    CAS  Google Scholar 

  13. Mottram DS, Low MY, Elmore JS (2006) The Maillard reaction and its role in the formation of acrylamide and other potentially hazardous compounds in foods. In: Skog K, Alexander J (eds) Acrylamide and other hazardous compounds in heat-treated foods. Woodhead Publ Ltd, Cambridge, pp 3–22

    Chapter  Google Scholar 

  14. Chaudhry Q, Cotterill J, Watkins R, Price N (2006) A molecular modelling approach to predict the toxicity of compounds generated during heat treatment of foods. In: Skog K, Alexander J (eds) Acrylamide and other hazardous compounds in heat-treated foods. Woodhead Publ Ltd, Cambridge, pp 132–160

    Chapter  Google Scholar 

  15. Abramsson-Zetterberg L, Zetterberg G, Bergqvist M, Grawe J (2000) Human cytogenetic biomonitoring using flow-cytometric analysis of micronuclei in transferrin-positive immature peripheral blood reticulocytes. Environ Mol Mutagen 36:22–31

    Article  CAS  Google Scholar 

  16. Grawe J, Biko J, Lorenz R, Reiners C, Stopper H, Vershenya S, Vukicevic V, Hempel K (2005) Evaluation of the reticulocyte micronucleus assay in patients treated with radioiodine for thyroid cancer. Mutat Res 583:12–25

    Article  CAS  Google Scholar 

  17. Stopper H, Hempel K, Reiners C, Vershenya S, Lorenz R, Vukicevic V, Heidland A, Grawe J (2005) Pilot study for comparison of reticulocyte-micronulei with lymphocyte-micronuclei in human biomonitoring. Toxicol Lett 156:351–360

    Article  CAS  Google Scholar 

  18. Abramsson-Zetterberg L, Durling LJ, Yang-Wallentin F, Rytter E, Vessby B (2006) The impact of folate status and folic acid supplementation on the micronucleus frequency in human erythrocytes. Mutat Res 603:33–40

    Article  CAS  Google Scholar 

  19. Rytter E, Vessby B, Asgard R, Johansson C, Sjodin A, Abramsson-Zetterberg L, Moller L, Basu S (2009) Glycaemic status in relation to oxidative stress and inflammation in well-controlled type 2 diabetes subjects. Br J Nutr 101:1423–1426

    Article  CAS  Google Scholar 

  20. Bergmark E (1997) Hemoglobin adducts of acrylamide and acrylonitrile in laboratory workers, smokers and nonsmokers. Chem Res Toxicol 10:78–84

    Article  CAS  Google Scholar 

  21. Paulsson B, Athanassiadis I, Rydberg P, Tornqvist M (2003) Hemoglobin adducts from glycidamide: acetonization of hydrophilic groups for reproducible gas chromatography/tandem mass spectrometric analysis. Rapid Commun Mass Spectrom 17:1859–1865

    Article  CAS  Google Scholar 

  22. Tornqvist M (1994) Epoxide adducts to N-terminal valine of hemoglobin. Hemoglob Pt B Method Enzymol 231:650–657

    Article  CAS  Google Scholar 

  23. Fenech M, Bonassi S (2011) The effect of age, gender, diet and lifestyle on DNA damage measured using micronucleus frequency in human peripheral blood lymphocytes. Mutagenesis 26:43–49

    Article  CAS  Google Scholar 

  24. Battershill JM, Burnett K, Bull S (2008) Factors affecting the incidence of genotoxicity biomarkers in peripheral blood lymphocytes: impact on design of biomonitoring studies. Mutagenesis 23:423–437

    Article  CAS  Google Scholar 

  25. Offer T, Ho E, Traber MG, Bruno RS, Kuypers FA, Ames BN (2005) A simple assay for frequency of chromosome breaks and loss (micronuclei) by flow cytometry of human reticulocytes. FASEB J 19:485–487

    CAS  Google Scholar 

  26. Fenech M (2001) The role of folic acid and Vitamin B12 in genomic stability of human cells. Mutat Res 475:57–67

    Article  CAS  Google Scholar 

  27. MacGregor JT, Wehr CM, Hiatt RA, Peters B, Tucker JD, Langlois RG, Jacob RA, Jensen RH, Yager JW, Shigenaga MK, Frei B, Eynon BP, Ames BN (1997) ‘Spontaneous’ genetic damage in man: evaluation of interindividual variability, relationship among markers of damage, and influence of nutritional status. Mutat Res 377:125–135

    Article  CAS  Google Scholar 

  28. Mowrer J, Tornqvist M, Jensen S, Ehrenberg L (1986) Modified Edman degradation applied to hemoglobin for monitoring occupational exposure to alkylating agents. Toxicol Environ Chem 11:215–231

    Article  CAS  Google Scholar 

  29. Tornqvist M, Mowrer J, Jensen S, Ehrenberg L (1986) Monitoring of environmental cancer initiators through hemoglobin adducts by a modified Edman degradation method. Anal Biochem 154:255–266

    Article  CAS  Google Scholar 

  30. Vikstrom AC, Abramsson-Zetterberg L, Naruszewicz M, Athanassiadis I, Granath FN, Tornqvist MA (2011) In vivo doses of acrylamide and glycidamide in humans after intake of acrylamide-rich food. Toxicol Sci 119:41–49

    Article  Google Scholar 

  31. Fenech M, Bonassi S (2010) The effect of age, gender, diet and lifestyle on DNA damage measured using micronucleus frequency in human peripheral blood lymphocytes. Mutagenesis 26:43–49

    Article  Google Scholar 

  32. Thomas P, Wu J, Dhillon V, Fenech M (2011) Effect of dietary intervention on human micronucleus frequency in lymphocytes and buccal cells. Mutagenesis 26:69–76

    Article  CAS  Google Scholar 

  33. Gooderham NJ, Murray S, Lynch AM, Yadollahi-Farsani M, Zhao K, Boobis AR, Davies DS (2001) Food-derived heterocyclic amine mutagens: variable metabolism and significance to humans. Drug Metab Dispos 29:529–534

    CAS  Google Scholar 

  34. Anderson KE, Sinha R, Kulldorff M, Gross M, Lang NP, Barber C, Harnack L, DiMagno E, Bliss R, Kadlubar FF (2002) Meat intake and cooking techniques: associations with pancreatic cancer. Mutat Res 506–507:225–231

    Article  Google Scholar 

  35. Lewin MH, Bailey N, Bandaletova T, Bowman R, Cross AJ, Pollock J, Shuker DE, Bingham SA (2006) Red meat enhances the colonic formation of the DNA adduct O6-carboxymethyl guanine: implications for colorectal cancer risk. Cancer Res 66:1859–1865

    Article  CAS  Google Scholar 

  36. IARC (2010) Ingested nitrate and nitrite and cyanobacterial peptide toxins. IARC Monogr Eval Carcinog Risks Hum 94:43–325

    Google Scholar 

  37. Magagnotti C, Orsi F, Bagnati R, Celli N, Rotilio D, Fanelli R, Airoldi L (2000) Effect of diet on serum albumin and hemoglobin adducts of 2-amino-1-methyl-6-phenylimidazo 4,5-b pyridine (PhIP) in humans. Int J Cancer 88:1–6

    Article  CAS  Google Scholar 

  38. Bessette EE, Yasa I, Dunbar D, Wilkens LR, Le Marchand L, Turesky RJ (2009) Biomonitoring of carcinogenic heterocyclic aromatic amines in hair: a validation study. Chem Res Toxicol 22:1454–1463

    Article  CAS  Google Scholar 

  39. Taubert D, Glockner R, Muller D, Schomig E (2006) The garlic ingredient diallyl sulfide inhibits cytochrome P450 2E1 dependent bioactivation of acrylamide to glycidamide. Toxicol Lett 164:1–5

    Article  CAS  Google Scholar 

  40. Vesper HW, Caudill SP, Osterloh JD, Meyers T, Scott D, Myers GL (2010) Exposure of the US population to acrylamide in the National Health and Nutrition Examination Survey 2003–2004. Environ Health Perspect 118:278–283

    Article  CAS  Google Scholar 

  41. Kassie F, Lhoste EF, Bruneau A, Zsivkovits M, Ferk F, Uhl M, Zidek T, Knasmuller S (2004) Effect of intestinal microfloras from vegetarians and meat eaters on the genotoxicity of 2-amino-3-methylimidazo 4,5-f quinoline, a carcinogenic heterocyclic amine. J Chromatogr B: Anal Technol Biomed Life Sci 802:211–215

    Article  CAS  Google Scholar 

  42. World Cancer Research Fund/American Institute for Cancer Research (2007) Food, nutrition, physical activity, and the prevention of cancer: a global perspective. AICR, Washington DC, pp 517

  43. Ross SA (2003) Diet and DNA methylation interactions in cancer prevention. Ann NY Acad Sci 983:197–207

    Article  CAS  Google Scholar 

  44. Friso S, Choi SW (2002) Gene-nutrient interactions and DNA methylation. J Nutr 132:2382S–2387S

    CAS  Google Scholar 

  45. Mathers JC, Coxhead JM, Tyson J (2007) Nutrition and DNA repair: potential molecular mechanisms of action. Curr Cancer Drug Targets 7:425–431

    Article  CAS  Google Scholar 

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Acknowledgments

The “Harald och Greta Jeanssons Stiftelser” in Sweden, the EU Commission Project ASRISK (QLK4-CT-1999-01142) and FUNCFOOD (1024262), and the Swedish Research Council Formas funded this study. We thank Erika Hartoft for help with the study design and setup. We thank Elvy Netzel and Ioannis Athanassiadis for excellent technical help and all the volunteers for their participation in the study.

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Author information

Author notes

  1. Eden Tareke

    Present address: Division of Applied Nutrition and Food Chemistry, Department of Food Technology, Engineering and Nutrition, Lund University, Lund, Sweden

Authors and Affiliations

  1. Department of Molecular Biosciences, The Wenner-Gren Institute, Stockholm University, 106 91, Stockholm, Sweden

    Natalia Kotova, Siamak Haghdoost & Dag Jenssen

  2. Department of Science, The Swedish National Food Agency, Box 622, 751 26, Uppsala, Sweden

    Natalia Kotova & Lilianne Abramsson-Zetterberg

  3. Environmental Chemistry Unit, Department of Materials and Environmental Chemistry, Stockholm University, 106 91, Stockholm, Sweden

    Cecilia Frostne, Eden Tareke, Birgit Paulsson & Margareta Törnqvist

  4. Knivsbrunna, 755 98, Uppsala, Sweden

    Rolf Bergman

  5. Department of Biosciences and Nutrition, Karolinska Institute, 141 83, Huddinge, Sweden

    Dan Segerbäck

  6. The Rudbeck Laboratory, Cell Analysis Core Facility, Uppsala University, 751 85, Uppsala, Sweden

    Jan Grawé

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  1. Natalia Kotova
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Correspondence to Natalia Kotova.

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Kotova, N., Frostne, C., Abramsson-Zetterberg, L. et al. Differences in micronucleus frequency and acrylamide adduct levels with hemoglobin between vegetarians and non-vegetarians. Eur J Nutr 54, 1181–1190 (2015). https://doi.org/10.1007/s00394-014-0796-7

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  • DOI: https://doi.org/10.1007/s00394-014-0796-7

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