American Journal of Epidemiology Advance Access originally published online on May 26, 2006
American Journal of Epidemiology 2006 164(1):47-55; doi:10.1093/aje/kwj187
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Original Contribution |
Association between Personal Use of Hair Dyes and Lymphoid Neoplasms in Europe
1 Catalan Institute of Oncology, Barcelona, Spain
2 German Cancer Research Center, Heidelberg, Germany
3 Masaryk Memorial Cancer Institute, Brno, Czech Republic
4 Registre des Hémopathies Malignes de Côte d'Or, Dijon, France
5 Institute of Occupational Medicine, University of Cagliari, Cagliari, Italy
6 School of Public Health and Population Science, University College Dublin, Dublin, Ireland
7 Department of Pathology, Tampere University Hospital, Tampere, Finland
8 International Agency for Research on Cancer, Lyon, France
9 Department of Pathology, Hospital Verge de la Cinta, Tortosa, Spain
Correspondence to Dr. Silvia de Sanjosé, Servei d'Epidemiologia i Registre del Cancer, Institut d'Investigació Biomèdica de Bellvitge, Institut Catala d'Oncologia, Gran Via Km 2.7, 08907 L'Hospitalet, Barcelona, Spain (e-mail: s.sanjose{at}iconcologia.net).
Received for publication October 24, 2005. Accepted for publication January 20, 2006.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Hair dyes have been evaluated as possibly being mutagenic and carcinogenic in animals. Studies of the association between human cancer risk and use of hair dyes have yielded inconsistent results. The authors evaluated the risk of lymphoid malignancies associated with personal use of hair dyes. The analysis included 2,302 incident cases of lymphoid neoplasms and 2,417 hospital- or population-based controls from the Czech Republic, France, Germany, Ireland, Italy, and Spain (1998–2003). Use of hair dyes was reported by 74% of women and 7% of men. Lymphoma risk among dye users was significantly increased by 19% in comparison with never use (odds ratio (OR) = 1.19, 95% confidence interval (CI): 1.00, 1.41) and by 26% among persons who used hair dyes 12 or more times per year (OR = 1.26, 95% CI: 1.00, 1.60; p for linear trend = 0.414). Lymphoma risk was significantly higher among persons who had started coloring their hair before 1980 (OR = 1.37, 95% CI: 1.09, 1.72) and persons who had used hair dyes only before 1980 (OR = 1.62, 95% CI: 1.10, 2.40). Personal use of hair dyes is associated with a moderate increase in lymphoma risk, particularly among women and persons who used dyes before 1980. Specific compounds associated with this risk remain to be elucidated.
carcinogens; case-control studies; hair dyes; lymphatic system; neoplasms; odds ratio
Abbreviations: CI, confidence interval; OR, odds ratio
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Hair coloring products include a wide range of over 5,000 chemical substances, some of which have been reported to be mutagenic and carcinogenic in animals. In 1993, the International Agency for Research on Cancer classified hairdressing and barbering as occupations entailing exposures that were probably carcinogenic on the basis of suspicion of an increased risk of bladder cancer. In line with these observations, excess risks of hematologic cancer among cosmetologists and hairdressers were described in early studies (1
, 2). At the time, cancer risk among personal users of hair dyes could not be evaluated because of a lack of adequate data on humans (3).
Use of hair dyes has been inconsistently associated with the etiology of lymphomas. In 1988, Cantor et al. (4) suggested an approximately twofold increased risk of leukemia and non-Hodgkin's lymphoma with long-term use of hair dyes (odds ratio (OR) = 1.8 and OR = 2.0, respectively) among men. Zahm et al. (5) reported increased risks of non-Hodgkin's lymphoma, Hodgkin's lymphoma, and multiple myeloma but not of chronic lymphocytic leukemia among women using hair-coloring products. Other investigators have not reported positive associations between ever use of permanent hair dye and hematopoietic cancers (6–10).
In a case-control study carried out among women in Connecticut, Zhang et al. (11) reported a 30 percent increased risk of non-Hodgkin's lymphoma for lifetime ever use of hair coloring. That study was restricted to women who had started using hair dyes before 1980. The risk was increased twofold for persons using darker dye colors. Within all non-Hodgkin's lymphoma histologies, follicular lymphoma was the category with the highest risk (OR = 1.9).
In a recent meta-analysis, Takkouche et al. (12) estimated a 15 percent increased risk of hematopoietic cancer associated with personal ever use of hair dyes and a particularly increased risk among men. A slightly elevated risk for Hodgkin's lymphoma was also observed (OR = 1.23, 95 percent confidence interval (CI): 1.16, 2.89).
We evaluated the association between personal use of hair-coloring products and risk of lymphoid neoplasms using data from EpiLymph, a European multicenter case-control study coordinated by the International Agency for Research on Cancer. A preliminary analysis based on the Spanish component of the study identified an increased risk of all lymphomas, particularly among subjects who had used hair dyes before 1980 (13).
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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EpiLymph was carried out in six European countries (Germany, Italy, Spain, Ireland, France, and the Czech Republic) from 1998 to 2003. A common core protocol and interview were used in all countries. The study included 2,302 incident lymphoma cases and 2,417 controls.
Cases were defined as all consecutive patients who were given an initial diagnosis of lymphoid malignancy during the study period. The diagnosis of lymphoma was verified by histologic testing, and 99 percent of these tests were supplemented by immunohistochemistry tests and flow cytometry. Cases were categorized according to the World Health Organization Classification of Neoplastic Diseases of the Hematopoietic and Lymphoid Tissues (14) and included all B-cell, T-cell, and natural killer-cell neoplasms, as well as Hodgkin's lymphoma. Subjects with a diagnosis of uncertain malignant potential, such as posttransplant lymphoproliferative disorder or monoclonal gammopathies of undetermined significance, were excluded. The distribution of the 2,302 cases by major histologic type was as follows: B-cell lymphoma, n = 1,568; T-cell lymphoma, n = 134; Hodgkin's lymphoma, n = 325; and multiple myeloma, n = 273 (two subjects had a clinical diagnosis only). Among the B-cell lymphomas, there were 407 cases of chronic lymphocytic leukemia, 246 cases of follicular lymphoma, and 513 cases of diffuse large B-cell lymphoma.
In Italy and Germany, controls (n = 2,417) were synchronically identified with the cases and were sampled from the general population on the basis of census lists. In the other study countries, controls were recruited from the same hospitals as the cases. In all instances, controls were matched to the cases by age (±5 years), gender, and study center. Potential hospital controls were excluded if the main reason for the hospitalization at the time of recruitment was cancer, organ transplant, and/or systemic infection.
Informed consent was obtained from all subjects prior to enrollment, and the institutional review boards of participating centers approved the study. Cases and controls provided a blood sample for DNA extraction and serologic testing and underwent a personal interview. Among cases, the participation rate was 87 percent (by study center, refusal rates ranged from 7 percent to 18 percent). Among population controls, the participation was 75 percent (refusal rates by center, 4–56 percent).
The structured face-to-face interview solicited information on sociodemographic factors; reproductive, familial, and medical history, including allergies and asthma; use of tobacco, alcohol, and drugs (legal and illegal); use of hair dyes; sun exposure; and occupational history. Subjects were asked about their natural hair color and whether they had ever used hair-coloring products. For ever users, information requested included the color of dye used (brown, black, red, blond, or other), the usual dyeing method (permanent dye, wash-out dye (i.e., rinse), bleaching, or other), age at first and last use, and frequency of hair coloring.
Subjects with missing data on hair dye use were excluded from the analysis (48 controls and 60 cases). Ever users of hair coloring products were compared with never users. Further analysis included data on the color and method used. In the category of dark-colored dye, we included black and brown colors, and the light color category included blond dyes. Users of red dyes were excluded from the color-specific analysis (70 controls and 86 cases). Permanent types of coloring included permanent dyeing and hair bleaching; semipermanent types included wash-out dyes (rinses). Year of starting use of hair dyes, lifetime dose, time of exposure, and mean annual dose were estimated. Categorization of these variables was based on the quartile distribution among controls. For subjects who had used different type of colors or methods in a single period, exposure time was distributed equally according to the number of individual colors or methods used during that period.
Pooled logistic regression was used to estimate the association between hair dye use and risk of hematologic disease. The potentially confounding variables included in the final model were sex, age (in quintiles), educational level, home ownership, and country. Adjustment for other variables, such as natural hair color, family history of hematologic disease, smoking status, and alcohol consumption, did not modify the observed associations, so these variables were not included in the final model. Odds ratios and 95 percent confidence intervals were calculated using the statistical package SPSS 9.0 (SPSS, Inc., Chicago, Illinois).
We evaluated heterogeneity among countries using a likelihood ratio test that compares models with and without a term for interaction between country and exposure to hair dyes. The interaction term did not reach statistical significance and therefore was not included in the final models.
Some results are presented graphically. Summary odds ratios are plotted as black squares whose size is inversely proportional to the variance of the estimate. Diamonds are used to plot the summary odds ratio for all studies together and subentities. A log scale was used for the odds ratio to preserve the symmetry of the confidence intervals.
Restricted cubic splines were used to measure the effect of year of starting use of hair dye products on lymphoma risk. Under these models, the fit is represented as a piecewise (usually cubic) polynomial with breakpoints (knots) at prechosen values of the covariate year at the start of using hair dyes (i.e., tertiles of year of starting use). The best model is considered the one with the lowest Akaike Information Criterion (15); these models provide a flexible estimate of the odds ratio function but must be interpreted as a complement of the categorical analyses.
Analysis was performed evaluating use of hair dyes before 1980 and during and after 1980, as this year was detected in the spline models as the best point characterizing changes in risk.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Table 1 shows the characteristics of the study population in relation to age, sex, educational level, and home ownership by participant country for cases and controls. There were slightly more men than women (54.7 percent vs. 45.3 percent; p = 0.14). The average age of the study population was 56 years, with no difference between cases and controls. No difference in the age distribution was observed for cases and controls based on the quintile distribution, with the exception of Czech cases, who were slightly younger. Cases in Spain and France were significantly more likely to own their homes in comparison with their respective controls. The educational levels of cases and controls were similar in all countries, except for Germany, where controls were slightly more educated than cases. Of the 4,719 subjects, ever use of hair coloring was reported by 895 (37.0 percent) of the controls and 866 (37.6 percent) of the cases. The proportion of controls reporting ever use of hair dyes ranged from 31.5 percent in the Czech Republic to 41.1 percent in Ireland.
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Table 2 summarizes the adjusted associations between hair dye characteristics and the risk of lymphoma for men and women and overall. Among women, the use of hair dyes was more commonly reported by cases than by controls (77 percent vs. 72 percent; p = 0.023), while no differences in use were observed among men (7 percent for both cases and controls; p = 0.883). Ever users of hair dyes as compared with never users were at 19 percent increased risk of lymphoma. The risk estimate was slightly higher for women (OR = 1.24, 95 percent CI: 1.01, 1.53). The increased risk observed among women was similarly observed for any color or type of dye used, increasing slightly for users of longer periods. However, the risk of lymphoma increased with increasing number of years of using dark hair dyes (p for linear trend = 0.076). A similar result was observed among persons who started using hair dye before 1980 and those who started using it during or after 1980.
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The lymphoma risk associated with ever use of hair dyes was consistent among the six countries (figure 1). Odds ratios for individual countries ranged from 1.15 in Spain to 1.23 in the Czech Republic.
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The risk estimates for hair dye characteristics (ever use vs. never use, light color vs. dark color, permanent vs. wash-out, and age at starting use) were homogeneous among countries, except for duration of use of dark color (p = 0.03). Sensitivity analysis showed consistency with an increasing risk with increasing number of years of using hair dyes.
Table 3 summarizes the risk of lymphoma associated with the calendar period of first use of hair dyes. Lymphoma risk was 37 percent higher for persons who had started using hair dye before 1980 as compared with never users, while a nonsignificant increase in risk was observed for persons who had started in 1980 or later. Subjects who had started coloring their hair earlier had a higher lymphoma risk if they had used dark hair color or used a wash-out method. Subjects who had stopped coloring their hair before 1980 had an odds ratio for lymphoma of 1.6 (95 percent CI: 1.1, 2.4) compared with never users, while subjects who stopped coloring their hair in 1980 or later had an odds ratio of 1.3 (95 percent CI: 1.0, 1.7) (p for heterogeneity between groups = 0.21). Age at starting use did not modify the period effect.
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Evaluation of the association between use of hair dyes and lymphoma subtype (table 4) identified an increased risk of chronic lymphocytic leukemia (OR = 1.43, 95 percent CI: 1.01, 2.03), and borderline statistical significance was detected for Hodgkin's lymphoma. Starting use of hair dyes before 1980 increased the odds ratio for chronic lymphocytic leukemia to 2.02 (95 percent CI: 1.31, 3.11) and the odds ratio for Hodgkin's lymphoma to 1.75 (95 percent CI: 0.90, 3.38) (p for heterogeneity between groups = 0.003). The odds ratio for the commonly used category of non-Hodgkin's lymphoma was 1.16 (95 percent CI: 0.96, 1.4).
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Figure 2 shows the country-specific odds ratios for lymphoma subtypes that were of borderline statistical significance in the overall analysis. The risk of chronic lymphocytic leukemia associated with ever use of hair dyes was greater than 1 in Spain, Germany, Italy, and Ireland; however, the sensitivity analysis showed that the statistical significance was mainly explained by the Spanish data.
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The risk estimate for follicular lymphoma among ever users was consistently increased in all countries but the Czech Republic, although in all of them the 95 percent confidence interval included 1.
The risk of Hodgkin's lymphoma associated with hair dye use was increased in Spain, France, Italy, Ireland, and the Czech Republic, although in none of these study centers did the 95 percent confidence interval exclude 1. The estimate in Germany was 1. The odds ratio for Hodgkin's lymphoma for ever use of hair dyes excluding Germany was 1.67 (95 percent CI: 1.05, 2.65).
Among all study subjects, 57 reported having worked as hairdressers or barbers. No increased lymphoma risk was observed in this subgroup (OR = 0.57, 95 percent CI: 0.18, 1.81).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Based on a large series of patients, our data suggest that personal use of hair coloring is associated with a small increase in lymphoma risk, particularly among women who started using hair coloring products before 1980.
The risk estimates observed were of a small-to-moderate magnitude, and dose-response effects with increasing exposure were not detected. We cannot exclude the possibility that the weak effect is explained by inconsistencies in the reporting of frequency of use. However, the elevated risk was generally consistent when the data were stratified by period of use, and estimates were higher when use was restricted to persons who started using hair coloring before 1980; this is consistent with previous work by Zhang et al. (11). The lack of effect among more recent users could be explained by temporal variation in the hazard of cancer following changes in the composition of hair dyes.
Use of hair dyes before 1980 was more common in Germany than in other participating countries. However, sensitivity analysis produced homogeneous odds ratios with the exclusion of each country; there was no evidence of change in the odds ratio estimates. It has been reported that the composition of hair-coloring products has been extensively modified over time (7, 16). During 1978–1982, all oxidative dye products were reformulated to eliminate some ingredients that had been reported to produce tumors in bioassays (16). Whether the resultant compounds could still induce carcinogenesis or affect the overall immune response is not known. The issue requires careful monitoring, since any increase in risk for use of hair dyes could have important public health implications due to the high prevalence of this exposure. In their recent meta-analysis of relevant studies, Takkouche et al. (12) concluded that the overall increase in risk of hematologic neoplasms was on the order of 15 percent, which they considered too small to have a public health impact. However, when the prevalence of exposure is high, as in the case of hair dye use, the impact can be considerable. In our data, we estimated that among women there was a 24 percent increased risk of lymphoma with a prevalence of hair dye use of 74 percent. In this circumstance, the proportion of lymphomas in the female population that could be attributable to hair dyes is on the order of 10 percent, assuming that the association is real and unbiased.
Evaluation of the effect of hair dye use by histologic category identified chronic lymphocytic leukemia, follicular lymphoma, and Hodgkin's lymphoma to be more common among ever users. The analysis by country showed that the point estimates were fairly consistent for the three entities, but estimates were not robust enough to provide any unambiguous conclusion. Interestingly, the increased risk of Hodgkin's lymphoma was consistent in all countries but Germany. Hodgkin's lymphoma subjects are younger than other lymphoma cases, and patterns of hair dye use could vary by country and age group. However, patterns of use among younger subjects were not distinctive in Germany as compared with the rest of the study subjects (reported prevalences of ever use among controls younger than age 40 years were 51.4 percent and 45 percent, respectively; p = 0.06). Outside the EpiLymph context, results from studies that have explored the association between hair dyes and chronic lymphocytic leukemia have been mainly negative (17) or based on few numbers (5). The meta-analysis by Takkouche et al. (12) identified an 11 percent increase in risk of chronic lymphocytic leukemia associated with use of hair dyes, on the basis of six studies. Our statistically increased odds ratio of 1.43 for chronic lymphocytic leukemia among ever users was strongly driven by the Spanish data. The question of whether these country-specific variations are due to real changes in hair dye composition or hair dye use or are simply statistical artifacts needs to be further explored in larger series.
The mechanisms through which hair dyes could act in producing lymphomas are unknown. Hair dyes contain aniline metabolites that can induce chromosomal aberrations with complex rearrangements and single-strand DNA breaks. DNA damage in lymphocytes has been reported after hair dyeing (3, 18), but direct DNA damage due to use of hair dye has been questioned in some recent experiments (19). The observation in humans that certain metabolites of hair dyes can be detected in the urine after skin application provides evidence for the absorption of some hair dye application products.
This was a large study with systematic inclusion of lymphoma cases, careful histologic evaluation, and a comparable group of controls. Cases were compared with a group of subjects of similar age and sex who were selected from the same study centers during the same period of time. The findings presented are of particular relevance because they incorporate populations from six different countries that may differ in terms of cultural attitudes toward undyed hair; therefore, results are unlikely to have been driven by use of a particular dye product. In addition, the study employed a detailed questionnaire on use of hair dyes that allowed for thorough assessment of exposure. However, during a lifetime, people tend to be exposed to a wide range of colors and dyeing methods. Part of this variability is unknown to the exposed subject. These changes are motivated by commercial changes, fashion, and individual preferences; consequently, the identification of specific chemical exposures is almost impossible. Evaluation of lifetime exposure to hair dyes in these circumstances is thus based on surrogate measures, such as color category (dark vs. light) as reported by the subject. This potential source of misclassification is likely to be nondifferential between cases and controls and is unlikely to explain the positive association we observed. Another source of mismeasurement error is that we had to rely on self-reports of past use. It is feasible that the precision and validity of this information could differ by case/control status if participants were aware of our working hypothesis across the different study areas. The cross-country consistency of the data presented strongly supports the conclusion that differential misclassification is unlikely to account for the overall association.
We included both men and women in our analysis on the assumption that any risk should operate equally in both sexes for similar exposures. However, to allow for potential sex differences in the use and composition of hair dyes, we also present sex-specific information. The increased risk observed among persons who started using hair dyes before 1980 was consistent for both men and women (OR = 1.52 and OR = 1.38, respectively), although statistical power among men was low.
The overall participation rate was high for the majority of the study sites, with the exception of relatively low participation of population controls in Germany. It could be argued that variations in hair dye use could be related to factors affecting participation. However, the fact that the risk estimates were consistent across the study sites for the different evaluations based on color, length of time exposed, and lymphoma subtype indicates that the results presented were not influenced by participation bias.
Overall, our data contribute additional evidence for a possible association between personal use of hair dyes and risk of lymphoma. We excluded major sources of bias and considered a large number of variables that could be considered potential confounders. Although these data do not provide proof of causality, we identified an increased risk among persons potentially exposed during a period when hair dyes were more likely to include carcinogenic substances. These associations are biologically compatible, and our results were consistent across populations. However, the moderate magnitude of the association and the weak dose-response pattern observed are potential weaknesses in attempts to establish a role of hair dyes in lymphomagenesis.
In conclusion, our data identified an increased risk of lymphoma associated with hair dye use. Our data are compatible with a temporal hazard change associated with the composition of hair dyes. Further assessment of the risk of hematologic neoplasms from hair dye use is required.
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ACKNOWLEDGMENTS |
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This work was supported by the Spanish Ministry of Health (grants 04-0091 and RCESP C03/09) and the European Commission Fifth Framework Programme ("Quality of Life and Management of Living Resources") (grant QLK4-CT-2000-00422).
Conflict of interest: none declared.
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