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Environmental Science and Pollution Research

, Volume 26, Issue 2, pp 1304–1314 | Cite as

Increase of global DNA methylation patterns in beauty salon workers exposed to low levels of formaldehyde

  • Eduardo Barbosa
  • Ana Laura Anibaletto dos Santos
  • Giovana Piva Peteffi
  • Anelise Schneider
  • Diana Müller
  • Diego Rovaris
  • Claiton Henrique Dotto Bau
  • Rafael Linden
  • Marina Venzon Antunes
  • Mariele Feiffer CharãoEmail author
Research Article
  • 95 Downloads

Abstract

Formaldehyde (FA) is a carcinogenic aldehyde illegally added to creams as a hair straightening agent for the Brazilian blowout (BB). This study aimed to investigate the possible effects of occupational exposure to FA on global DNA methylation in salon workers with different exposure levels. FA exposure was monitored using environmental and biological measurements. The study included 49 salon workers divided by FA levels in the workplace into group A (FA < 0.01 ppm; n = 8), group B (0.03 ppm < FA < 0.06 ppm; n = 15), and group C (0.08 ppm < FA < 0.24 ppm; n = 26). The global DNA methylation levels were 3.12%, 4.55%, and 4.29% for groups A, B, and C, respectively, with statistically higher values for groups B and C compared to group A (p = 0.002). A correlation was found between FA in passive samplers and global DNA methylation (rs = 0.307, p = 0.032). Additionally, when only taking into account the hairdressers that performed the BB on clients instead of the whole group, a stronger correlation was observed between FA in personal passive samplers and global DNA methylation (rs = 0.764, p = 0.006). For the first time, an increase in DNA methylation was observed in subjects occupationally exposed to FA. In conclusion, our results indicated that even low levels of FA exposure could cause a disturbance in DNA methylation, leading to epigenetic changes, which is associated with cancer development. These data suggest a possible contribution of FA to cancer development through occupational exposure.

Keywords

Formaldehyde Epigenetic Global DNA methylation Occupational exposure Hair straightening Brazilian blowout Formic acid 

Notes

Acknowledgments

The authors would like to thank CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Brazil) for the research fellowship provided to master degree student Eduardo Barbosa and Feevale University for the financial support.

Compliance with ethical standards

The study was carried out after approval by the Research Ethics Committee of Feevale University (CAAE 59967716.2.0000.5348).

Conflict of interest

The authors declare that there is no conflict of interest.

References

  1. Abraham LS, Moreira AM, de Moura LH et al (2009) Tratamentos estéticos e cuidados dos cabelos: uma visão médica (parte 2). Surg Cosmet Dermatology 1:178–185Google Scholar
  2. Agency for Toxic Substances and Disease Registry (ATSDR) (1999) Toxicological profile for formaldehyde. Atlanta, GAGoogle Scholar
  3. Alemayehu A, Sebova K, Fridrichova I (2008) Redundant DNA methylation in colorectal cancers of lynch-syndrome patients. Genes Chromosom Cancer 47:906–914.  https://doi.org/10.1002/gcc.20586 CrossRefGoogle Scholar
  4. American Conference of Governmental Industrial Hygienists (ACGIH) (2010). TLVs and BEIs based on the documentation of the threshold limit values for chemical substances and physical agents & biological exposure indices. Cincinnati (OH): SignatureGoogle Scholar
  5. Anvisa (2013) RESOLUÇÃO - RDC no15 de março de 2013Google Scholar
  6. Benedetti D, Lopes Alderete B, de Souza CT, Ferraz Dias J, Niekraszewicz L, Cappetta M, Martínez-López W, da Silva J (2017) DNA damage and epigenetic alteration in soybean farmers exposed to complex mixture of pesticides. Mutagenesis 33:1–9.  https://doi.org/10.1093/mutage/gex035 Google Scholar
  7. Bird A (2007) Perceptions of epigenetics. Nature 447:396–398.  https://doi.org/10.1038/nature05913 CrossRefGoogle Scholar
  8. Bollati V, Baccarelli A, Hou L, Bonzini M, Fustinoni S, Cavallo D, Byun HM, Jiang J, Marinelli B, Pesatori AC, Bertazzi PA, Yang AS (2007) Changes in DNA methylation patterns in subjects exposed to low-dose benzene. Cancer Res 67:876–880.  https://doi.org/10.1158/0008-5472.CAN-06-2995 CrossRefGoogle Scholar
  9. Bureau of Labor Statistics (BLS) (2018) Occupational outlook handbook, barbers, hairstylists, and cosmetologists. In: U.S. Dep. Labor. https://www.bls.gov/ooh/personal-care-and-service/barbers-hairstylists-and-cosmetologists.htm. Accessed 13 Oct 2018
  10. Carmo AT, Prado RT (1999) Qualidade do Ar Interno. Relat do Ambient interno 20Google Scholar
  11. Casanova M, d’A. Heck H, Everitt JI, et al (1988) Formaldehyde concentrations in the blood of rhesus monkeys after inhalation exposure. Food Chem Toxicol 26:715–716. doi:  https://doi.org/10.1016/0278-6915(88)90071-3
  12. Cheetham S, Tang MJ, Mesak F, Kennecke H, Owen D, Tai IT (2008) SPARC promoter hypermethylation in colorectal cancers can be reversed by 5-Aza-2′deoxycytidine to increase SPARC expression and improve therapy response. Br J Cancer 98:1810–1819.  https://doi.org/10.1038/sj.bjc.6604377 CrossRefGoogle Scholar
  13. Coelho MCSDM (2009) O formaldeído em ambiente laboral: determinação do ácido fórmico em urina de trabalhadores de uma fábrica produtora de formaldeído. Universidade do Porto, PortoGoogle Scholar
  14. De Prins S, Koppen G, Jacobs G et al (2013) Influence of ambient air pollution on global DNA methylation in healthy adults: a seasonal follow-up. Environ Int 59:418–424.  https://doi.org/10.1016/j.envint.2013.07.007 CrossRefGoogle Scholar
  15. Devóz PP, Gomes WR, De Araújo ML et al (2017) Lead (Pb) exposure induces disturbances in epigenetic status in workers exposed to this metal. J Toxicol Environ Heal - Part A Curr Issues 80:1098–1105.  https://doi.org/10.1080/15287394.2017.1357364 CrossRefGoogle Scholar
  16. Dhareshwar SS, Stella VJ (2008) Your prodrug releases formaldehyde: should you be concerned?. No! J Pharm Sci 97:4184–4193.  https://doi.org/10.1002/jps.21319 CrossRefGoogle Scholar
  17. Dong W, Chen X, Xie J, Sun P, Wu Y (2010) Epigenetic inactivation and tumor suppressor activity of HAI-2/SPINT2 in gastric cancer. Int J Cancer 127:1526–1534.  https://doi.org/10.1002/ijc.25161 CrossRefGoogle Scholar
  18. Galão OF, Silva GL, Prete MC (2013) Determinação de formol em amostras de produtos de alisamento capilar. Semin Ciências Exatas e Tecnológicas 34:167.  https://doi.org/10.5433/1679-0375.2013v34n2p167 CrossRefGoogle Scholar
  19. Guyton KZ, Kyle AD, Aubrecht J, Cogliano VJ, Eastmond DA, Jackson M, Keshava N, Sandy MS, Sonawane B, Zhang L, Waters MD, Smith MT (2009) Improving prediction of chemical carcinogenicity by considering multiple mechanisms and applying toxicogenomic approaches. Mutat Res - Rev Mutat Res 681:230–240.  https://doi.org/10.1016/j.mrrev.2008.10.001 CrossRefGoogle Scholar
  20. Heck H d’A, Casanova-Schmitz M, Dodd PB et al (1985) Formaldehyde (CH 2 O) Concentrations in the blood of humans and Fischer-344 rats exposed to CH 2 O under controlled conditions. Am Ind Hyg Assoc J 46:1–3.  https://doi.org/10.1080/15298668591394275 CrossRefGoogle Scholar
  21. Huang L, Mo J, Sundell J, Fan Z, Zhang Y (2013) Health risk assessment of inhalation exposure to formaldehyde and benzene in newly remodeled buildings, Beijing. PLoS One 8:e79553.  https://doi.org/10.1371/journal.pone.0079553 CrossRefGoogle Scholar
  22. IARC Group Working On The Evaluation of Carcinogenic Risks to Humans (2006) Formaldehyde, 2-butoxyethanol and 1-tert-butoxypropan-2-ol. IARC Monogr Eval Carcinog Risks Hum 88:1–478Google Scholar
  23. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans (2012) Chemical agents and related occupations. IARC Monogr Eval Carcinog Risks Hum 100:9–562Google Scholar
  24. Jia X, Jia Q, Zhang Z, Gao W, Zhang X, Niu Y, Meng T, Feng B, Duan H, Ye M, Dai Y, Jia Z, Zheng Y (2014) Effects of formaldehyde on lymphocyte subsets and cytokines in the peripheral blood of exposed workers. PLoS One 9:e104069.  https://doi.org/10.1371/journal.pone.0104069 CrossRefGoogle Scholar
  25. Jiménez-Garza O, Guo L, Byun H-M, Carrieri M, Bartolucci GB, Barrón-Vivanco BS, Baccarelli AA (2018) Aberrant promoter methylation in genes related to hematopoietic malignancy in workers exposed to a VOC mixture. Toxicol Appl Pharmacol 339:65–72.  https://doi.org/10.1016/j.taap.2017.12.002 CrossRefGoogle Scholar
  26. Kawanishi M, Matsuda T, Yagi T (2014) Genotoxicity of formaldehyde : molecular basis of DNA damage and mutation. 2:1–8.  https://doi.org/10.3389/fenvs.2014.00036
  27. Kim JC, Choi JS, Roh SA, Cho DH, Kim TW, Kim YS (2010) Promoter methylation of specific genes is associated with the phenotype and progression of colorectal adenocarcinomas. Ann Surg Oncol 17:1767–1776.  https://doi.org/10.1245/s10434-009-0901-y CrossRefGoogle Scholar
  28. Kurdyukov S, Bullock M (2016) DNA methylation analysis: choosing the right method. Biology (Basel) 5:3.  https://doi.org/10.3390/biology5010003 Google Scholar
  29. Lahiri DK, Numberger JI (1991) A rapid non-enzymatic method for the preparation of HMW DNA from blood for RFLP studies. Nucleic Acids Res 19:5444.  https://doi.org/10.1093/nar/19.19.5444 CrossRefGoogle Scholar
  30. Lai J, Wang H, Luo Q, Huang S, Lin S, Zheng Y, Chen Q (2017) The relationship between DNA methylation and Reprimo gene expression in gastric cancer cells. Oncotarget 8:108610–108623.  https://doi.org/10.18632/oncotarget.21296 Google Scholar
  31. Lind L, Penell J, Luttropp K, Nordfors L, Syvänen AC, Axelsson T, Salihovic S, van Bavel B, Fall T, Ingelsson E, Lind PM (2013) Global DNA hypermethylation is associated with high serum levels of persistent organic pollutants in an elderly population. Environ Int 59:456–461.  https://doi.org/10.1016/j.envint.2013.07.008 CrossRefGoogle Scholar
  32. Liou S-H, Wu W-T, Liao H-Y, Chen CY, Tsai CY, Jung WT, Lee HL (2017) Global DNA methylation and oxidative stress biomarkers in workers exposed to metal oxide nanoparticles. J Hazard Mater 331:329–335.  https://doi.org/10.1016/j.jhazmat.2017.02.042 CrossRefGoogle Scholar
  33. Liu Q, Yang L, Gong C, Tao G, Huang H, Liu J, Zhang H, Wu D, Xia B, Hu G, Wang K, Zhuang Z (2011) Effects of long-term low-dose formaldehyde exposure on global genomic hypomethylation in 16HBE cells. Toxicol Lett 205:235–240.  https://doi.org/10.1016/j.toxlet.2011.05.1039 CrossRefGoogle Scholar
  34. Lu K, Boysen G, Gao L, Collins LB, Swenberg JA (2008) Formaldehyde-induced histone modifications in vitro. Chem Res Toxicol 21:1586–1593.  https://doi.org/10.1021/tx8000576 CrossRefGoogle Scholar
  35. Manno M, Viau C, Cocker J, Colosio C, Lowry L, Mutti A, Nordberg M, Wang S (2010) Biomonitoring for occupational health risk assessment (BOHRA). Toxicol Lett 192:3–16.  https://doi.org/10.1016/j.toxlet.2009.05.001 CrossRefGoogle Scholar
  36. Mazzei JL, Figueiredo ÉV, Da Veiga LJ et al (2009) Mutagenic risks induced by homemade hair straightening creams with high formaldehyde content. J Appl Toxicol 30:8–14.  https://doi.org/10.1002/jat.1464 CrossRefGoogle Scholar
  37. Minardi D, Lucarini G, Filosa A, Milanese G, Zizzi A, Primio RD, Montironi R, Muzzonigro G (2009) Prognostic role of global DNA-methylation and histone acetylation in pT1a clear cell renal carcinoma in partial nephrectomy specimens. J Cell Mol Med 13:2115–2121.  https://doi.org/10.1111/j.1582-4934.2008.00482.x CrossRefGoogle Scholar
  38. Muggerud AA, Rønneberg JA, Wärnberg F et al (2010) Frequent aberrant DNA methylation of ABCB1, FOXC1, PPP2R2B and PTEN in ductal carcinoma in situ and early invasive breast cancer. Breast Cancer Res 12:R3.  https://doi.org/10.1186/bcr2466 CrossRefGoogle Scholar
  39. National Institute for Occupational Safety and Health (NIOSH) (2003) Method 2016: Formaldehyde. NIOSH Man. Anal. methods, Third Suppl. 1–7Google Scholar
  40. National Toxicology Program (NTP) (2010) Final report on carcinogens background document for formaldehyde. Rep Carcinog Backgr doc formaldehyde i-512Google Scholar
  41. National Toxicology Program (NTP) (2011) NTP 12th report on carcinogens. Rep Carcinog Carcinog profiles 12:iii-499Google Scholar
  42. National Toxicology Program (NTP) (2016) Report on Carcinogens, Fourteenth edition. Rep Carcinog 14:7Google Scholar
  43. Norma Regulamentadora 15 (NR 15) (1978) Atividades e operações insalubres. D.O.U. Portaria MTb n° 3:214Google Scholar
  44. Norma Regulamentadora 7 (NR7) (1978) Programa de controle médico de saúde ocupacional. D.O.U. Portaria MTb n.o 3.214 1–16Google Scholar
  45. Occupational Safety and Health Administration (OSHA) (2005) Formaldehyde - OSHA 1007. Osha 1–32Google Scholar
  46. Occupational Safety and Health Administration (OSHA) (2011) Formaldehyde. Osha factsheetGoogle Scholar
  47. Orsière T, Sari-Minodier I, Iarmarcovai G, Botta A (2006) Genotoxic risk assessment of pathology and anatomy laboratory workers exposed to formaldehyde by use of personal air sampling and analysis of DNA damage in peripheral lymphocytes. Mutat Res - Genet Toxicol Environ Mutagen 605:30–41.  https://doi.org/10.1016/j.mrgentox.2006.01.006 CrossRefGoogle Scholar
  48. Peteffi GP, da Silva LB, Hahn RZ et al (2015) Simple and fast headspace-gas chromatographic determination of formic acid in urine : application to the assessment of occupational exposure to formaldehyde. Appl Res Toxicol 1:40–45Google Scholar
  49. Peteffi GP, Antunes MV, Carrer C, Valandro ET, Santos S, Glaeser J, Mattos L, da Silva LB, Linden R (2016a) Environmental and biological monitoring of occupational formaldehyde exposure resulting from the use of products for hair straightening. Environ Sci Pollut Res 23:908–917.  https://doi.org/10.1007/s11356-015-5343-4 CrossRefGoogle Scholar
  50. Peteffi GP, Da Silva LB, Antunes MV et al (2016b) Evaluation of genotoxicity in workers exposed to low levels of formaldehyde in a furniture manufacturing facility. Toxicol Ind Health 32:1763–1773.  https://doi.org/10.1177/0748233715584250 CrossRefGoogle Scholar
  51. Pierce JS, Abelmann A, Spicer LJ, Adams RE, Glynn ME, Neier K, Finley BL, Gaffney SH (2011) Characterization of formaldehyde exposure resulting from the use of four professional hair straightening products. J Occup Environ Hyg 8:686–699.  https://doi.org/10.1080/15459624.2011.626259 CrossRefGoogle Scholar
  52. Portal do Empreendedor (2018) Estatística. In: Ministério da Indústria, Comércio Exter. e Serviços. http://www.portaldoempreendedor.gov.br/estatisticas. Accessed 13 Oct 2018
  53. Rager JE, Smeester L, Jaspers I, Sexton KG, Fry RC (2011) Epigenetic changes induced by air toxics: formaldehyde exposure alters miRNA expression profiles in human lung cells. Environ Health Perspect 119:494–500.  https://doi.org/10.1289/ehp.1002614 CrossRefGoogle Scholar
  54. Ramsahoye BH (2002) Measurement of genome wide DNA methylation by reversed-phase high-performance liquid chromatography. Methods 27:156–161.  https://doi.org/10.1016/S1046-2023(02)00069-5 CrossRefGoogle Scholar
  55. Rozhon W, Baubec T, Mayerhofer J, Scheid OM, Jonak C (2008) Rapid quantification of global DNA methylation by isocratic cation exchange high-performance liquid chromatography. Anal Biochem 375:354–360.  https://doi.org/10.1016/j.ab.2008.01.001 CrossRefGoogle Scholar
  56. Steinritz D, Schmidt A, Balszuweit F, Thiermann H, Simons T, Striepling E, Bölck B, Bloch W (2016) Epigenetic modulations in early endothelial cells and DNA hypermethylation in human skin after sulfur mustard exposure. Toxicol Lett 244:95–102.  https://doi.org/10.1016/j.toxlet.2015.09.016 CrossRefGoogle Scholar
  57. Swenberg JA, Moeller BC, Lu K, Rager JE, Fry RC, Starr TB (2013) Formaldehyde carcinogenicity research: 30 years and counting for mode of action, epidemiology, and cancer risk assessment. Toxicol Pathol 41:181–189.  https://doi.org/10.1177/0192623312466459 CrossRefGoogle Scholar
  58. Szyf M (2007) The dynamic epigenome and its implications in toxicology. Toxicol Sci 100:7–23.  https://doi.org/10.1093/toxsci/kfm177 CrossRefGoogle Scholar
  59. Torng PL, Lin CW, Chan MWY, Yang HW, Huang SC, Lin CT (2009) Promoter methylation of IGFBP-3 and p53 expression in ovarian endometrioid carcinoma. Mol Cancer 8:1–12.  https://doi.org/10.1186/1476-4598-8-120 CrossRefGoogle Scholar
  60. Tunsaringkarn T, Siriwong W, Prueksasit T et al (2012) Potential risk comparison of formaldehyde and acetaldehyde exposures in office and gasoline station. Int J Sci Res Publ 2:2–6Google Scholar
  61. U.S. EPA (2010) IRIS Toxicological Review of Formaldehyde (Inhalation) (External Review Draft 2010). U.S. Environ. Prot. AgencyGoogle Scholar
  62. Wei C, Wen H, Yuan L, McHale CM, Li H, Wang K, Yuan J, Yang X, Zhang L (2016) Formaldehyde induces toxicity in mouse bone marrow and hematopoietic stem/progenitor cells and enhances benzene-induced adverse effects. Arch Toxicol 91:921–933.  https://doi.org/10.1007/s00204-016-1760-5 CrossRefGoogle Scholar
  63. Wieslander G, Norbäck D, Björnsson E, Janson C, Boman G (1997) Asthma and the indoor environment: the significance of emission of formaldehyde and volatile organic compounds from newly painted indoor surfaces. Int Arch Occup Environ Health 69:115–124.  https://doi.org/10.1007/s004200050125 CrossRefGoogle Scholar
  64. World Health Organization (WHO) (2010) WHO guidelines for indoor air quality: selected pollutants. WHO Guidel 9:454Google Scholar
  65. Yang X, Yuan Y, Lu X, Yang J, Wang L, Song J, Nie J, Zhang Q, Niu Q (2015) The relationship between cognitive impairment and global DNA methylation decrease among aluminum Potroom workers. J Occup Environ Med 57:713–717.  https://doi.org/10.1097/JOM.0000000000000474 CrossRefGoogle Scholar
  66. Yu M, Lou J, Xia H, Zhang M, Zhang Y, Chen J, Zhang X, Ying S, Zhu L, Liu L, Jia G (2017) Global DNA hypomethylation has no impact on lung function or serum inflammatory and fibrosis cytokines in asbestos-exposed population. Int Arch Occup Environ Health 90:265–274.  https://doi.org/10.1007/s00420-017-1195-1 CrossRefGoogle Scholar
  67. Zhang B-Y, Shi Y-Q, Chen X, Dai J, Jiang ZF, Li N, Zhang ZB (2013a) Protective effect of curcumin against formaldehyde-induced genotoxicity in A549 cell lines. J Appl Toxicol 33:1468–1473.  https://doi.org/10.1002/jat.2814 CrossRefGoogle Scholar
  68. Zhang Y, Liu X, McHale C, Li R, Zhang L, Wu Y, Ye X, Yang X, Ding S (2013b) Bone marrow injury induced via oxidative stress in mice by inhalation exposure to formaldehyde. PLoS One 8:e74974.  https://doi.org/10.1371/journal.pone.0074974 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Eduardo Barbosa
    • 1
    • 2
  • Ana Laura Anibaletto dos Santos
    • 1
  • Giovana Piva Peteffi
    • 1
  • Anelise Schneider
    • 1
  • Diana Müller
    • 3
    • 4
  • Diego Rovaris
    • 3
    • 4
  • Claiton Henrique Dotto Bau
    • 3
    • 4
  • Rafael Linden
    • 1
    • 2
  • Marina Venzon Antunes
    • 1
    • 2
  • Mariele Feiffer Charão
    • 1
    • 2
    Email author
  1. 1.Analytical Toxicology LaboratoryUniversidade FeevaleNovo HamburgoBrazil
  2. 2.Graduate Program on Toxicology and Analytical ToxicologyUniversidade FeevaleNovo HamburgoBrazil
  3. 3.Department of Genetics, Instituto de BiociênciasUniversidade Federal do Rio Grande do SulPorto AlegreBrazil
  4. 4.ADHD Outpatient Program, Adult DivisionHospital de Clínicas de Porto AlegrePorto AlegreBrazil

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