Annals of Occupational Hygiene Advance Access originally published online on July 1, 2008
Annals of Occupational Hygiene 2008 52(7):645-651; doi:10.1093/annhyg/men037
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Assessment of Occupational Genotoxic Risk among Brazilian Hairdressers
1 Department of Legal Medicine, Ethics and Occupational Health, São Paulo University Medical School, São Paulo, SP, CEP 05405-000, Brazil
2 Occupational Health Service, Hospital das Clínicas, São Paulo University Medical School, São Paulo, SP, CEP 05405-000, Brazil
* Author to whom correspondence should be addressed. Instituto Oscar Freire, Rua Teodoro Sampaio, 115, São Paulo, SP CEP: 05405-000, Brazil. Tel/fax: +55-11-3085-9677; e-mail: gfgattas{at}usp.br
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ABSTRACT |
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Objectives: To evaluate the genotoxic risk to hairdressers exposed daily to chemical substances such as hair dyes, waving and straightening preparations and manicurists' products by the Comet assay test (single-cell gel electrophoresis).
Methods: The Comet assay was performed on blood samples from 69 female hairdressers (36.4 ± 10.7 years old) currently employed in 21 different beauty institutes in São Paulo, Brazil, and on 55 female control blood donors (32.6 ± 10.0 years old) from the São Paulo University Clinical Hospital blood bank. All the control subjects had occupations other than hairdresser. Comet assays were performed by evaluating 100 blood lymphocytes per individual and graded by visual score according to comet tail length.
Results: The hairdressers showed a higher frequency of DNA damage revealed by Comet Score (159.8 ± 71) when compared to the control group (125.4 ± 64.1), and the difference was statistically significant by the Student's t-test (P = 0.005). Multiple regression analysis showed that in addition to the hairdressers' profession, tobacco use contributed to the higher frequency of cells with comets (P < 0.05).
Conclusions: The observed DNA damage could be associated with the hairdressers' occupational environment, where different chemicals are chronically manipulated and inhaled. Considering that this profession in many countries, including Brazil, is not officially regulated, more attention should focus on these professionals not only by legislative bodies but also by multidisciplinary teams able to develop and implement risk prevention and control strategies for chemical, physical and biological agents to which hairdressers are exposed.
Keywords: Comet assay • DNA damage • hairdressers • occupational health
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INTRODUCTION |
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Human beings are continuously exposed to a variety of both harmful and beneficial chemicals. Lifestyle may contribute to individual susceptibility to cancer because of hazardous exposures or insufficient intake of cancer preventive compounds, such as fruits and vegetables. Environmentally low exposures also are of concern and, although the risk for the individual is low, health effects on populations can be larger because of the number of exposed individuals.
Beauty salon professionals and their clients are chronically exposed to chemical and mechanical hair treatments that contain a high number of potentially harmful chemicals, including aromatic amines and resorcinol (Lind et al., 2005), volatile solvents (van Muiswinkel et al., 1997), diaminotoluene (Sosted et al., 2004), formaldehyde, ammonia, ethanol (Kersemaekers et al., 1995; Hollund and Moen, 1998) and thioglycolic acid (Gan et al., 2003). Some of these chemicals are either known or suspected allergens, carcinogens or mutagens. In the literature, studies of the adverse systemic effects of hairdressing have focused on the association of hair dyes with human malignancies; however, the number of studies is limited. Evidence of cancer among hairdressers was first reviewed by the International Agency for Research on Cancer (IARC, 1993), which showed an excess risk of urinary bladder cancer, lung cancer and non-Hodgkin's lymphoma in these professionals. The profession was considered at that time as ‘probably carcinogenic’ (IARC, 1993).
Subsequent update of these data confirmed an increased risk of upper aerodigestive tract (Ji and Hemminki, 2005), lung (Czene et al., 2003), breast (Pollan, 2001), non-Hodgkin's lymphoma and bladder (Gaertner et al., 2004) cancers. A cohort study of 3637 female and 168 male hairdressers followed for cancer from 1970 to 1987 showed high risk for certain types of cancer, including non-melanoma skin, lung, ovarian, cervical and pancreatic cancers. Some studies showed an increased risk that was most prominent in groups with the longest duration since first employment as a hairdresser (Pukkala et al., 1992). Another study conducted in 24 US states confirmed a significant excess risk among hairdressers for all malignant neoplasms, but primarily lung, stomach, pharyngeal and all lymphatic and hematopoietic cancers (Lamba et al., 2001). Association between different hematolymphopoietic malignancies and exposure to solvents in hairdressers also was investigated (Costantini et al., 2001). More recently, in a large cohort study of the incidence of neoplasic diseases among hairdressers conducted over 39 years, an excess risk for cancer of the upper aerodigestive tract, lung and colon was identified in male hairdressers (Czene et al., 2003). Interestingly, in the same cohort, female hairdressers showed an increased risk of pancreatic, lung and cervical cancers (Czene et al., 2003).
Because hair dyes contain aromatic amines, analysis of their carcinogenicity in humans has focused on urothelial cancer. Epidemiological studies have investigated the risk of bladder cancer both among hairdressers and among consumers of hair dyes (Golka et al., 2004). A Canadian case–control study conducted between 1994 and 1997 showed a significant increased risk for bladder cancer (odds ratio = 3.42; 1.09–10.8) among men employed as hairdressers (Gaertner et al., 2004). In contrast, a study in Sweden only showed an increased bladder cancer risk only in female hairdressers exposed in former decades (Czene et al., 2003).
The single-cell gel electrophoresis (SCGE) or Comet assay, described by Östling and Johanson (1984), is a simple and sensitive method for studying DNA damage and repair. A cell suspension is embedded in agarose on a microscope slide, lysed to liberate the DNA and subjected to electrophoresis under alkaline condition. In cells with increased DNA damage, chromosomal DNA migrates from the nucleus in a shape that resembles a comet. Data are expressed based on tail shape and length (% DNA in the tail). Protocols, applications and limitations have been summarized (Collins, 2004). Similarly to other genotoxicity tests, the Comet assay is not predictive of individual cancer risk but represents a useful tool to evaluate early and still repairable genotoxic effects due to occupational or environmental exposure (Moller et al., 2000). Considering that, to our knowledge, there is no published cytogenetic data concerning hairdressers in Brazil, the objective of this study was to use the Comet assay to evaluate the genotoxic risk to hairdressers compared to a control group not exposed to similar work conditions.
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METHODS |
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Study population
A total of 69 females employed in 21 beauty institutes in the city of São Paulo, Brazil, were included in this study. A reference group composed of 55 women not occupationally exposed as hairdressers was selected from blood donors in the blood bank service of São Paulo University Medical School Hospital. All subjects were aware of the objectives of the study and gave informed consent to participate. This study received approval from the Institutional Research Bioethics Committee and the Brazilian National Commission on Bioethics in Research.
Beauty institutes
Although not officially designated, Brazilian beauty institutes are ‘classified’ as categories A, B and C, according to the number of employees, size of the establishment, location, type of beauty products in use and offered services. In this investigation, the participating salons were nearby the São Paulo University Medical School, and all categories of institutes were included.
Questionnaire and sample collection
Detailed information including age, occupational status, years of employment, alcohol and tobacco consumption, personal use of hair dyes, diet, reproductive history, contraceptive use, X-ray exposure and health problems were collected using a standard questionnaire. Control women completed the same questionnaire, except specific questions about hairdressers' occupation were omitted. Hairdressers completed the questionnaire after work hours, and the blood samples were collected in the workplace.
The alkaline Comet assay
Alkaline electrophoresis was performed according to Singh et al. (1988) with minor modifications. An aliquot of blood (7 µl) was mixed with 100 µl of 0.75% low-melting point agarose (Sigma–Aldrich, St Louis, MO, USA) and spread on four slides previously coated with 1% normal melting point agarose (Sigma, St Louis, MO, USA). After solidification, the slides were immersed for 24 h in fresh lysing solution [2.5 M NaCl, 100 mM ethylenediaminetetraacetic acid (EDTA)-2Na and 10 mM Tris–HCl, pH 10] with the addition of 1% Triton X-100 and 10% dimethyl sulfoxide, prepared at the time of use. The slides were incubated for 60 min in alkaline buffer solution (300 mM NaOH and 1 mM EDTA, pH 13.2), prepared at time of use.
Electrophoresis and staining
Cells on the slides were submitted to electrophoresis for 30 min at 300 mA and 25 V. After, the slides were neutralized by washing three times with neutralization buffer (400 mM Tris–HCl, pH 7.5) for 5 min each and were stained with 50 µl of 10 µg ml–1 ethidium bromide. Positive controls were incubated for 2 h at 37°C with 10 µl of hydrogen peroxide to evaluate test efficiency and electrophoresis conditions.
DNA migration (comet) assessment
Images of 100 randomly selected cells from each individual were analyzed by use of an epifluorescence microscope equipped with a 455-nm excitation filter. Comet tail lengths (comprising nuclear region and tail) for each cell were manually scored into five Comet Classes: Class 0 (undamaged, no tail), Class 1 (tail up to 1.5 times the diameter of the comet nucleus), Class 2 (tail 1.5–2.0 times the diameter of the comet nucleus), Class 3 (tail 2.0–2.5 times the diameter of the comet nucleus) and Class 4 (maximally damaged, tail >2.5 times the diameter of the comet nucleus). A final overall DNA damage rating for all 100 cells (Comet Score) was obtained by summation of the number of cells in each class times the class number, yielding a rating between 0 (completely undamaged) and 400 (maximum damaged) (Collins, 2004). Technicians assessing tail length were blinded to occupational status of the participants.
Statistical analysis
All statistical analyses were conducted using SPSS and SAS 8.0 statistical software packages for Windows. The mean and dispersion of the data were calculated (Bussab and Morettin, 1987), and the results were compared to linear generalized models assuming a Gaussian distribution (McCullagh and Nelder, 1989). To assess the independent statistical relationships of all relevant variables simultaneously, a multiple regression analysis was used. The relationships between the comet frequency and variables were determinated by Spearman correlation test (Conover, 1980). The tests were interpreted using a 5% degree of significance.
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RESULTS |
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General characteristics of the study population, including age, marital status, occupation, reproductive history and alcohol and tobacco consumption are shown in Table 1. Drinkers were defined as those who consumed alcoholic beverages at least once a week and former drinkers as those who had not consumed alcoholic beverages for >1 year. For tobacco use, former smokers were defined as those who had not smoked for >1 year. Occupations of the control group included professionals, students, housewives and unemployed individuals. The mean age of hairdressers (36.4 ± 10.7 years) was similar to that of the controls (32.6 ± 10.0 years), and the difference was not statistically significant (P = 0.22). Marital status was more frequent in the control group (P = 0.04). Hairdressers had an increased number of spontaneous abortions compared to controls (23.1 versus 14.5%), although the difference was not considered significant (P = 0.25). Twenty-five percent of the hairdressers who had miscarried had done so more than once, in contrast to 12.5% of controls, although these differences were not statistically significant (P = 0.63). The intensity and frequency of alcoholic beverage consumption by hairdressers were similar to those reported by the controls. The same was not observed for tobacco consumption. Not only the number of smokers was higher among hairdressers when compared to controls (31.9 versus 12.7%, P = 0.01) but also 63.6% of the hairdressers consumed >11 cigarettes per day compared to 14.3% of controls (P = 0.03).
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DNA damage observed in the hairdresser group was significantly higher than that observed in the control group (Comet Score 159.8 ± 71.0 versus 125.4 ± 64.1, P = 0.005) (Table 2). In addition, Comet Class 3 (15.1 ± 9.9 cells) and Class 4 (12.2 ± 14.6 cells) were observed more frequently in hairdressers than in the control group (9.9 ± 9.1 and 7.0 ± 9.7 cells, respectively). The opposite finding was observed with undamaged cells; Comet Class 0 was observed more frequently in the control group compared to the hairdressers (34.6 ± 22.5 versus 24.8 ± 17.2 cells) (Table 2). Duration of occupational exposure did not affect the Comet Score. Although women who worked as hairdressers for 11–20 years had the highest mean Comet Score (164.5 ± 75.3), duration of occupational exposure was not correlated with Comet Score (r = –0.79; P = 0.52) (Table 3).
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When hairdressers were evaluated separately according to their job function in the salon, the mean Comet Score observed in hairstylists (165.9 ± 72.2) and colourists (164.2 ± 88.6) was higher than that observed in nail care specialists (143.0 ± 62.8), but the difference was not statistically significant (P > 0.05) (Table 4). Also, the Comet Score of hairdressers who reported use of personal protective equipment (PPE) was similar to that found in hairdressers who reported no PPE use (161.3 ± 72.4 versus 156.8 ± 69.7, P > 0.05) (Table 4).
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Factors that could confound these results, such as alcohol and tobacco use, were adjusted for in the multiple regression analysis (Table 5). In addition to the occupation of hairdresser, only tobacco use was associated with Comet Score. Other variables, including alcohol consumption, X-ray exposure, contraceptive use and personal use of hair dyes were not included in the final statistical model because they were not statistically significant (data not shown).
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DISCUSSION |
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The present report aims to evaluate DNA damage associated with workplace exposure to xenobiotic substances among hairdressers using the Comet assay. Our results showed that these professionals have a significant increase in genetic damage as measured by the Comet Score compared to controls without occupational exposure. This increase in genetic damage could be associated in part with the occupational conditions to which hairdressers are chronically exposed.
In Brazil, the hairdressing profession is not governmentally regulated. There are no work conditions or standards that must be followed, nor are there inspections of the workplace. Consequently, all over the world these professionals are frequently exposed to many risk factors for occupational diseases such as asthma and other respiratory problems (Moscato and Galdi, 2006), contact dermatitis (Ferrari et al., 2005), poor work posture, repetitive work tasks (English et al., 1995) and cancer (Lamba et al., 2001; Czene et al., 2003; Ji and Hemminki, 2005; Dryson et al., 2007).
In beauty salons, in addition to the traditional washing and cutting of hair, hairdressers are exposed to a range of chemical products that contain ingredients considered to be proven, probable or possible human carcinogens (IARC, 1993). Specifically, hair dying formulations belong to three categories used for temporary, semipermanent and permanent hair coloring. Permanent (oxidative) hair dyes that contain aromatic amines, such as p-phenylenediamines and p-aminophenols, are preferentially used in beauty salons. This type of hair dye is resistant to fading by shampooing and contains adjusting agents including ammonia and a stabilizing solution of hydrogen peroxide. In order to improve the hair penetration, ammonia releasers, such as ammonium chloride or ammonium phosphate, are added. Ammonia and hydrogen peroxide also are ingredients used for permanent waves and hair bleaching. Since 1970, a number of aromatic amines used in oxidative hair dyes were identified as mutagenic or carcinogenic in rodents after lifetime oral administration. In addition, under typical conditions, between 0.1 and 0.5% of applied p-phenylenediamine has been shown to be absorbed through the skin in humans (Bolt and Golka, 2007). In response to the carcinogenicity data, regulatory action was taken, and some hair dye ingredients were banned in the European Union such as lead acetate and 2,3-naphthalenediol (Rollison et al., 2006; Bolt and Golka, 2007). Other substances had the use prohibited or restricted by US Food and Drugs Administration regulations (FDA, 2000), like vinyl chloride, chloroform, hexachlorophene and mercury compounds.
Another substance frequently used in hair straightening solutions is formaldehyde. Along with metacrylate and acetone, it is also handled in beauty salons by the manicurists (Pukkala et al., 1992). A high frequency of micronuclei and comets was observed in wood factory workers exposed to formaldehyde compared to non-exposed controls (Yu et al., 2005), and a review conducted by the IARC concluded that formaldehyde is carcinogenic in humans (Cogliano et al., 2005).
Genotoxicity studies in humans regarding cumulative hair dye application or use have been published in the scientific literature (Hofer et al., 1983; Turanitz et al., 1983). Despite the epidemiologic findings of an association between the profession of hairdresser and human malignancies, no increase in DNA strand breaks (SCGE) or sister chromatid exchange assay in peripheral lymphocytes or in Salmonella-positive mutagenic activity in the urine was found in a population of 15 heavily exposed hairdressers who had an extensive history of work without protective measures (Sardas et al., 1997).
In the present evaluation, 20% of the hairdressers who were engaged in this profession for >21 years did not show a difference in Comet Score compared to those who worked in the profession <21 years. A genotoxic dose–response effect may not be observed due to the small sample size in this investigation. Alternatively, it also could be related to the fact that the beauty salon environment encourages hairdressers to undergo frequent personal hair treatments. This behavior would greatly increase hair dye exposure regardless of duration of employment. In fact, recent studies have suggested an association between personal use of hair dye with bladder and hematopoietic cancers (Andrew et al., 2004; Pelucchi et al., 2006; Bluhm et al., 2007), mainly in women with prolonged use of dark-colored permanent dyes (Bluhm et al., 2007).
In Brazil, in contrast to other countries, nail care professionals and colourists work alongside hairdressers. The number of hairdressers was frequently higher than the number of manicurists and colourists in the participating beauty salons, even after considering the different categories of salons that were included in the study. Comet Score did not change when the different occupations in the beauty salon were considered separately. This result could be in part affected by the lower number of manicurits (26%) and colourists (9%) compared to hairstylists (65%) analyzed in this study. Also, sometimes it was difficult to establish one occupation per participant because the same professional can have more than one function in the same beauty institute. In fact, the Comet Score observed in the colourists (164.1 ± 88.6) was almost the same as that observed in the hairstylists (165.9 ± 72.2).
Depending on the occupational setting in Brazil, the use of PPE is mandatory. Inhalation and dermal absorption are considered the most frequent routes of exposure to chemical agents among hairdressers (Wong et al., 2005). Although gloves and masks are considered PPE that prevent skin contact with different beauty products, including oxidative hair dyes, they are often used for esthetic, but not health reasons. Direct hand contact with oxidative hair dyes produces an undesirable, long-lasting discoloration of hands and fingernails (Nixon et al., 2006). Comparisons between hand rinse samples collected from hairdressers before the start of hair dying, after application of the dye and after cutting the newly dyed hair suggested that working with or without gloves during hair dying did not change the hand hair dye residues detected because the glove use was often improper and was insufficient to prevent exposure (Lind et al., 2005). In contrast, professionals who did not use protective equipment had twice the number of skin diseases compared to those who wore gloves and masks (Nienhaus et al., 2004). In this study, the Comet Score was not significantly different between hairdressers who used or did not use PPE. In fact, the subgroup that reported to use PPE had a slightly higher Comet Score (161.3 ± 72.4) compared to those who reported no PPE use (156.8 ± 69.7). Although the majority of hairdressers (66%) self-reported PPE use, mainly glove use during chemical manipulation, this information was not completely reliable because as consumers we know that they rarely use gloves and masks in the workplace. A recent European study reported that 98% of hairdressers wear gloves during hair dying (Sinclair and Green, 2006), but this information is not available in Brazil because there is no monitoring of PPE use in beauty institutes.
A number of potential confounding factors may affect the frequency of the DNA damage in humans. Age, alcohol consumption and smoking status were considered to be the major confounders in this study. In the multiple regression analysis, in addition to a profession as a hairdresser, tobacco use was associated with Comet Score (P = 0.025).
Results from biomonitoring studies of smoking-induced DNA damage are inconclusive. Some studies clearly confirmed the genotoxic effects of tobacco smoke (Hininger et al., 2004; Kopjar et al., 2006) while others reported no significant increase in the markers of DNA damage evaluated (Speit et al., 2003; Hoffmann and Speit, 2005). Several factors may explain these conflicting results. Differences in the brand of cigarettes smoked, absence of data on the number of cigarettes smoked per day or variation in the amount of tar contained in cigarettes may be responsible for the observed differences in DNA damage. Additionally, genetic polymorphisms of enzymes that metabolize genotoxicants contained in tobacco may influence the results. Moreover, the conflicting results may be due to the fact that the influence of passive smoking is usually overlooked, although it may contribute to DNA damage in control populations (Kopjar et al., 2006). The population of hairdressers of this study contained a higher percentage of smokers and higher mean daily cigarette use compared to the control population. In addition, in most of the beauty institutes in Brazil, smoking is not prohibited and can significantly increase tobacco exposure during the day. Similar results, although not statistically significant, were observed by Sardas et al. (1997), evaluating hairdressers and controls by different genotoxic tests. For these reasons, the association of cigarette smoking on DNA damage observed in this investigation warrants further investigation.
The recognition that skin is not an impermeable barrier to percutaneous penetration or absorption of hair dyes suggests the possibility of systemic human exposure and warrants thorough genetic toxicity and carcinogenicity investigation. Results from our study showed an increase in DNA damage among hairdressers that strengthen findings from epidemiological studies showing an increased risk of cancer among these professionals compared to non-occupationally exposed populations.
Differences in study outcomes may arise because it is difficult to quantify the amount of exposure, the type of hair products used and the frequency of specific hair treatments (Kirkland et al., 2005). It is interesting to note that hair treatment, including dying, has become more common and frequent in young girls, increasing both the lifetime exposure to hair chemicals and hairdressers' working time contact with hair dyes. Moreover, considering that hairdressing is a common profession worldwide, particularly among women, and involves constant exposure to potentially hazardous chemical products, more attention should be focused on health outcomes in this category of workers. Other tests including micronuclei and chromosomal aberration assays are under analysis in the same hairdresser and control population in our laboratory.
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CONCLUSION |
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In conclusion, the observed DNA damage in hairdressers could be associated with the professional environment where different chemical substances are chronically inhaled and manipulated. The hairdressing profession is not officially regulated in Brazil, and more attention should be focused on these workers not only by the legislative bodies but also by multidisciplinary teams able to suggest risk prevention and control strategies for chemical, physical and biological agents to which hairdressers are exposed.
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FUNDING |
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Hospital das Clínicas Faculdade de Medicina da Universidade de São Paulo – Laboratório de Investigação Médica 40 (HC FMUSP – LIM40).
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ACKNOWLEDGEMENTS |
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We thank Karen Huyck for suggestions and critical review of the manuscript.
Received March 1, 2008; in final form April 23, 2008
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