Residential and Occupational Exposures to 50-Hz Magnetic Fields and Breast Cancer in Women: A Population-based Study
Jolanta Kliukiene1 ,
Tore Tynes1,2 and
Aage Andersen1
1 The Cancer Registry of Norway, Institute of Population-based Cancer Research, Oslo, Norway.
2 Norwegian Radiation Protection Authority, Østerås, Norway.
Received for publication September 17, 2003; accepted for publication December 3, 2003.
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ABSTRACT
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A case-control study was conducted to investigate whether residential and occupational exposures to magnetic fields increased the risk for breast cancer among women. Cases of breast cancer diagnosed during 19801996 were identified in a cohort of women living near a high-voltage power line in Norway in 1980 or between 1986 and 1996. Each case was matched by year of birth, municipality, and first year of entry into the cohort with two randomly selected controls without cancer. Residential exposure to magnetic fields was calculated as that generated by the lines before diagnosis, and occupational exposure was based on exposure matrix data. Women with residential exposure had an odds ratio of 1.58 (95% confidence interval (CI): 1.30, 1.92) when compared with unexposed women. The odds ratios for exposed women versus unexposed women with estrogen receptor (ER)-positive and ER-negative breast cancer were 1.33 (95% CI: 0.93, 1.90) and 1.40 (95% CI: 0.78, 2.50), respectively (ER status was available for 44% of the cases). Women with the highest occupational exposure had an odds ratio of 1.13 (95% CI: 0.91, 1.40) when compared with those unexposed at work. The findings suggest an association between exposure to magnetic fields and breast cancer in women.
breast neoplasms; electromagnetic fields; receptors, estrogen
Abbreviations:
Abbreviations: CI, confidence interval; ER, estrogen receptor.
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INTRODUCTION
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The possible link between exposure to magnetic fields and cancer has been studied for two decades. The International Agency for Research on Cancer concluded that extremely low-frequency magnetic fields are possibly carcinogenic to humans, on the basis of an association between high-level residential exposure to magnetic fields and an increased risk for childhood leukemia (1). The evidence for an association with breast cancer in women was, however, considered to be inadequate. That relation was the subject of the study reported here.
A link between exposure to electromagnetic fields and breast cancer was reported in men exposed at work (25). The first report of an association between occupational exposure to electromagnetic fields and breast cancer in women was published in 1994 (6), and this was later corroborated in two other studies (7, 8). Other studies showed a stronger association in premenopausal than in postmenopausal women (9, 10). Nevertheless, no elevated risk for breast cancer was found among women with occupational exposure to electrical devices in other studies (1114).
Relatively few studies on residential exposure to magnetic fields and breast cancer have been reported, and those that have been published had contradictory results. An early study showed an association between death from breast cancer and exposure to magnetic fields (15), another study indicated an elevated risk for exposed women under the age of 50 years (16), but other studies showed no association (1722). Only one study (9) evaluated simultaneous residential and occupational exposures to magnetic fields, but the results were based on small numbers.
In four studies of women with occupational or residential exposure to magnetic fields, the results were also analyzed by estrogen receptor (ER) status (9, 10, 16, 23); three of the studies showed elevated risk estimates for ER-positive breast cancer (9, 10, 16).
In a review of 15 epidemiologic studies of exposure to electric and magnetic fields and breast cancer, the pooled relative risk for women was 1.12, and the result was considered unlikely to be due to chance (24). The authors concluded that, given a latency of 2030 years for breast cancer and the ubiquitous sources of magnetic fields, it might be important to assess total exposure (both at home and at work) over decades. Our study is a response to this recommendation, to test the hypothesis that residential and occupational exposures to magnetic fields increase the risk of breast cancer for women. We also evaluated the results by age group and ER status.
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MATERIALS AND METHODS
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Study population
This study was based on the same population used in a previously reported study of cutaneous malignant melanoma in adults, the report of which described the study population in more detail (25). The cohort used in the present study comprised all women aged 16 or more years who on November 1, 1980, or on January 1 of at least one of the years between 1986 and 1996 were living in a residence in a defined corridor near a high-voltage power line in Norway (table 1). The corridor around each power line was established through geographic information systems and was chosen to be wide enough to include both exposed and unexposed residences. The Norwegian Mapping Authority provided the coordinates of every Norwegian residence linked to its address, and the Norwegian Water Resources and Energy Directorate provided the coordinates of the power lines from 33 to 420 kV. With reference to the address code, Statistics Norway identified all women aged 16 or more years who had lived in such residences at the designated times mentioned above. In total, about 5 percent of all women in Norway during the period 19801996 were included in the cohort. A woman entered the cohort the first year she was registered in a residence within a corridor.
Cancer registration in Norway is based on compulsory reporting of all new cancer cases from clinicians, pathology laboratories, and death certificates to ensure complete registration. The cohort members were linked to the Cancer Registry by their unique personal identification number, and all women in whom invasive breast cancer was diagnosed after they entered the cohort, between January 1, 1980, and December 31, 1996, were identified; 99 percent of the cases were confirmed by pathology laboratories (26). For each case (n = 1,830), two controls were selected randomly from the cohort according to the following criteria: they were free of breast cancer and alive at the time of diagnosis of the case, they had entered the cohort in the same year as the case, they had been born within 5 years of the case, and they had lived in the same municipality at the time of entering the cohort (table 2). Statistics Norway provided residential histories for cases and controls as far back as to 1967. For the years 19671985, information on migration between municipalities was available and, for the years 19861996, information on migration within a municipality was also available. The latter made it possible to capture the move in and out of the corridor when moving within the same municipality. A womans length of residence near a power line was calculated by combining this information with the year the power line was built.
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TABLE 2. Distribution of characteristics of breast cancer cases and controls among women living in corridors around high-voltage power lines, Norway, 19801996
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Exposure to magnetic fields
Residential exposure was defined as exposure to magnetic fields generated by power lines close to dwellings within the corridor. Cases and matched controls were followed up for exposure from January 1, 1967, until the year of diagnosis. Calculations were performed with a computer program (Teslaw) developed at SINTEF Energy, Norway, which presents the results as the root mean square of magnetic field strength, expressed as µT, the sum of the vectors for the individual conductor in a given situation integrated over a given period. Underground cables were not taken into account, because they are considered not to be a significant source of magnetic fields. The calculations took account of the height of the towers, the distance between phases, the ordering of phases, the distance between a power line and a house, and the average (mean) load on the power line during each year a study subject lived in the house. Changes in the configuration of the power lines were taken into account. Because data from the geographic information systems for distances to power lines were somewhat crude, we collected corrected distances from economic maps (scale, 1:5,000). For practical reasons, this was done only for the residences situated in the half of the corridor closest to the line. On the other hand, we expected that correction would be of greater value for these residences (27). The time-weighted average residential exposure to magnetic fields was divided a priori into three categories, with cutoff points at 0.05 and 0.2 µT. The first cutoff point was based on the fact that Norwegian homes generally have low exposure (28); the latter point was based on the cutoff used in earlier reports in the literature. The time-weighted average exposures evaluated were from January 1, 1967, until diagnosis and for the last 5 years before diagnosis. The latter was the alternative exposure estimation due to the fact that migration within a municipality was not registered in the period 19671985, which might have caused misclassification of exposure for the total follow-up period.
For the analysis of the continuous data of residential exposure, we fitted a model with the risk described as a function of the logarithmic transformation of residential exposure to magnetic fields. The model may be written ln(OR) = ß x ln(twa + 1), where "ln" denotes the natural logarithm (loge); "OR" denotes the odds ratio; "twa" denotes the time-weighted average; and ß denotes the coefficient to be estimated (the corresponding p value is presented in tables 3 and 4 in the column ptrend). Attenuation of exposure-response curves at high exposure levels has been described recently (29), and the exposure-response relation has been found to be represented best by nonlinear relative risk models, such as the "power" model (30).
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TABLE 3. Risk of breast cancer for Norwegian women by residential and occupational exposures to magnetic fields, 19801996
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TABLE 4. Risk of breast cancer for Norwegian women by estrogen receptor status and residential and occupational exposures to magnetic fields, 19801996
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Exposure to magnetic fields at work was assessed a priori by a method that was a practical modification of the expert judgment used by Flynn et al. (31). They compared expert judgment with personal monitoring of exposure to magnetic fields and concluded that an expert panel was able to differentiate job titles with regard to exposure to 50-Hz magnetic fields. The assessment was performed individually by an expert panel and has been described in more detail elsewhere (32). The experts were advised to assign a rank of "1" if they considered that the job involved exposure above background level (0.1 µT) for less than 4 hours a week, a rank of "2" for 4 or more hours and less than 24 hours per week, and a rank of "3" for 24 or more hours per week. Jobs were classified on the basis of a three- to five-digit industry code and a three-digit occupation code used in the Norwegian censuses of 1960, 1970, 1980, and 1990 (33, 34). In the questionnaire of the 1990 census, the question on occupation was included for only a 10 percent sample of the total population. For the many women for whom the occupation in 1990 was missing, we assigned the information for 1980 to that year. Exposure was followed up from January 1, 1955, until the date of diagnosis, and the potentially occupationally active period was defined as the age interval of 1867 years. We cumulated exposure categories multiplied by the number of years. For women who changed occupation between two censuses, we cumulated the first occupation until the midpoint between the two relevant censuses. We used the first and third quartiles for controls as cutoff points, with values of 18 and 31 category-years, respectively.
For the estimates of concurrent residential and occupational exposures, we used three exposure categories: only residential exposure, only occupational exposure, and both residential and occupational exposures. Only women with information available on exposure both at home and at work were included in this analysis (table 2). Women were considered to be unexposed if their residential exposure was less than 0.05 µT and their contemporary occupational exposure was less than or equal to 30 category-years. Women were considered to have been exposed if their residential exposure was greater than or equal to 0.05 µT and their occupational exposure was greater than 30 category-years.
Other factors
Information on ER status was obtained from all pathology laboratories and clinical chemistry departments in the country; receptor status was available for 44 percent of the cases (table 2). A case was considered ER positive if the ER content of the primary tumor was greater than or equal to 10 fmol/mg of protein.
Data on fertility, such as the age at birth of the first child, were available from Statistics Norway. Educational level was used as an indicator of socioeconomic status, with the following categories: 1, primary school; 2, secondary school; 3, university or research degree. The information was collected from the census closest in time to the year of diagnosis for which such information was available. The type of residence was coded as one-family house or apartment.
Statistical methods
The odds ratio was used as the measure of association between exposure and disease. It was computed by conditional logistic regression models for matched sets with the computer package EGRET (35). In the model evaluating residential exposure, as well as in the model evaluating occupational exposure, the following potential confounders were considered: age at birth of the first child, educational level, and type of residence. The distribution of these factors was, however, similar among cases and controls (table 2), and adjustments for these potential confounders did not affect the results. Therefore, we present the results of the crude analysis only.
Confidence intervals at the 95 percent level were calculated. A trend test for ordinal levels of exposure was performed by assigning the scores, 1, 2, and 3, to the three levels of exposure. The risk for breast cancer was evaluated for two age groups, below 50 years and 50 years or older. In addition, the data were analyzed by estrogen receptor status.
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RESULTS
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Twelve percent of the cases and 8 percent of the controls were exposed to residential exposure above background level, and 5 percent of the cases and 4 percent of the controls were in the highest residential exposure group (table 3). In the highest occupational exposure category were 14 percent of the cases and 13 percent of the controls.
The odds ratio for women living in residences with a time-weighted average exposure to magnetic fields above the background level during the total follow-up period, compared with those living in unexposed residences, was 1.58 (95 percent confidence interval (CI): 1.30, 1.92), and a statistically significant trend (p < 0.001) by exposure category was observed, although it did not increase monotonically (table 3). The odds ratios for exposed versus unexposed women were similar in both age groups, but a statistically significant trend was found only in the older group; the odds ratio for women less than 50 years of age who had been exposed to magnetic fields at greater than 0.2 µT was close to unity. When exposure only during the last 5 years before diagnosis was analyzed, the odds ratio for women aged less than 50 years was 1.82 (95 percent CI: 1.32, 2.50), while that for women aged 50 or more years was 1.46 (95 percent CI: 1.19, 1.78). The trends were statistically significant in both age groups.
Analysis of continuous loge-transformed data of residential exposure showed an odds ratio of 1.87 (95 percent CI: 1.07, 3.28) and a p value of 0.0304 for all women for the total exposure period, and it showed an odds ratio of 1.76 (95 percent CI: 1.27, 2.44) and a p value of <0.001 when only exposure during the last 5 years before diagnosis was analyzed (table 3).
Analysis of the risk by occupational exposure showed a somewhat elevated risk for all women in the highest exposure category, with an odds ratio of 1.13 (95 percent CI: 0.91, 1.40); the odds ratio was 1.16 (95 percent CI: 0.91, 1.48) for women aged 50 or more years and close to unity for the younger group.
The odds ratios for women with ER-positive and ER-negative breast cancer living in exposed residences, compared with those living in unexposed homes, were 1.33 (95 percent CI: 0.93, 1.90) and 1.40 (95 percent CI: 0.78, 2.50), respectively, and no statistically significant trends were observed in any of the age groups (table 4). When exposure only during the last 5 years before diagnosis was analyzed, a statistically significant result was observed for women with ER-positive breast cancer where the odds ratio was 1.42 (95 percent CI: 1.04, 1.93), with a significant trend by categories of exposure (p = 0.0162), while no statistically significant results were observed for women with ER-negative breast cancer. For occupational exposure, no statistically significant results were shown by ER status, and overall and in the age groups there was no evidence of a trend. The odds ratios for women in the highest occupational exposure category were 1.17 (95 percent CI: 0.82, 1.69) for ER-positive breast cancer and 1.33 (95 percent CI: 0.74, 2.39) for ER-negative breast cancer, and the results were similar in both age groups.
Table 5 shows the results of the analyses of concurrent residential and occupational exposures to magnetic fields. For women of all ages combined, elevated odds ratios were found in all categories of exposure, although statistically significant only in those with residential-only exposure. For women aged less than 50 years, the increased risk was associated with residential exposure but not with occupational exposure, and the association was strongest for women who were exposed both at home and at work, with an odds ratio of 2.32 that was not statistically significant (95 percent CI: 0.84, 6.41). For women aged 50 or more years, a borderline increase in risk was observed for the categories of residential exposure only and occupational exposure only, while the odds ratio was close to unity for those exposed both at home and at work. For both women with ER-positive breast cancer and women with ER-negative breast cancer, the odds ratios were elevated for residential-only and occupational-only exposure categories, although not statistically significantly. No increase in risk for ER-positive breast cancer was found in relation to concomitant residential and occupational exposures, while the odds ratio for ER-negative breast cancer was 3.16 (95 percent CI: 0.87, 11.53).
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TABLE 5. Risk of breast cancer for Norwegian women in 19801996 with residential and occupational exposures to magnetic fields
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DISCUSSION
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The present study showed a 60 percent increase in risk for breast cancer among women living in residences with exposure to magnetic fields generated by power lines compared with those living in unexposed residences. A significant but nonmonotonic trend by exposure category was observed, and no clear dose-response relation was shown. The magnitude of the excess risk was similar for women aged less than 50 years and those aged 50 or more years. A borderline increase in risk was also observed for older women exposed to magnetic fields at work, while the younger women had a nonsignificant increase in risk of 130 percent if exposed both at home and at work (based on small numbers). Exposure to magnetic fields was associated with increased risks for both ER-positive and ER-negative breast cancer, although the result was significant only for ER-positive women who had been exposed during the last 5 years before diagnosis.
The strength of this study is that it is population based, with complete data from Statistics Norway and the national cancer registry, thus minimizing selection bias. As the study population consisted of adults who had lived in geographic areas crossed by high-voltage power lines, we could assume that these lines were the main source of exposure; 12 percent of the cases and 8 percent of the controls had residential exposure above the background level. The matched design made it possible to control for factors associated with the area of residence. The distribution of other potential confounding factors, such as fertility and socioeconomic status, also appeared to be similar among cases and controls. Consequently, adjustment for age at first birth, socioeconomic status, and type of dwelling did not give additional information to the study, and therefore we presented only crude results.
We were successful in obtaining the necessary information from national authorities to estimate residential exposure, and the study was not biased by differential recall of exposure by cases and controls. The use of calculated magnetic fields from power lines as the only measure for residential exposure, with no personal measurements, may have introduced some exposure misclassification. A previous study with dosimeter measurements among children living close to a power line in Norway showed fairly high correlation between calculated and actual exposure; correlation coefficients varied between 0.81 and 0.98 (28). The proportion of misclassification of exposure varied depending on whether home-only or 24-hour exposure was used in the analysis. The study showed that the magnetic fields from the line were the major source of exposure among children living close to a power line. This should be the case for adults, too, particularly for those not exposed to magnetic fields at work. We used the same cutoff points for residential exposure as those used in the dosimeter study. The level of 0.05 µT is the typical upper limit of the exposure in Norwegian homes far away from electrical installations. The contribution of ground currents to magnetic fields in homes in Norway is less than that in many countries, like Sweden, because of a different grounding system.
Our finding of an increased risk for breast cancer in women of all ages related to residential exposure to magnetic fields was stronger when exposure during the last 5 years before diagnosis was evaluated. Most likely this is due to the fact that our information for recent years was of higher quality compared with earlier years, but it might also be related to the idea that magnetic fields might act as a late stage promoter for breast cancer. The finding of an increased risk for women of all ages shown in our study has little support from other studies, although an association for women aged less than 50 years was shown in two previous studies (15, 16). A small increase in risk related to occupational exposure was also shown earlier in another Norwegian study (8) and is supported by the results of a number of other studies (6, 7, 9, 10, 36). Our finding of a higher risk for women aged less than 50 years with combined exposure at home and at work has some support from a Swedish study, which reported no increase in relative risk for women of all ages but an elevated risk for women less than 50 years of age; however, the basis of only four cases yielded very wide confidence limits (9). In our study, the occupational exposure might have been underestimated owing to the crude exposure classification: The matrix was based on job titles and industry branch only, and no individual measurements were made.
A biologic mechanism to explain how magnetic fields might contribute to breast cancer has been sought for 25 years. In 1978, Cohen et al. (37) suggested that a lowered production of the pineal hormone melatonin might increase the circulating levels of estrogen, which would stimulate the proliferation of breast tissue and subsequently lead to the development of breast cancer. A few experimental studies on animals in the early 1980s indicated that melatonin inhibits the growth of breast cancer in vivo and in vitro (38, 39). Stevens (40) in 1987 also proposed that magnetic fields lower the level of melatonin, leading to an increased estrogen level and stimulation of the turnover of breast epithelial cells at risk. Some years later, the same author suggested that a low melatonin level might also release existing cancer cells from a quiescent state (41). It has been suggested that magnetic fields act as tumor promoters rather than initiators, especially as they are not known to cause chromosomal damage (1).
The pineal gland produces melatonin at night. The residential exposure of economically active adults occurs mainly in the evening and at night. One could speculate that this exposure is of greater importance for risk than daytime exposure at work.
In our study, we also investigated risk by ER status and found residential exposure to be associated with a 3040 percent increase in risk for both ER-positive and ER-negative breast cancer; occupational exposure was associated with a somewhat lower increase in risk. The excess risk for ER-positive breast cancer is in accordance with the results of some other studies (9, 10, 16, 42), but no support for an increased risk for ER-negative breast cancer has been reported. A link among magnetic fields, melatonin, and ER-positive breast cancer was indicated by Liburdy et al. (43) and later confirmed by Blackman et al. (44). Furthermore, low serum melatonin concentrations have been found in women with ER-positive breast cancer (45). Our finding of an elevated risk for ER-negative breast cancer in women of all ages exposed to magnetic fields both at home and at work needs further investigation.
In conclusion, our results show an association between exposure to magnetic fields and the risk of breast cancer and a more important role for residential exposure than for occupational exposure, in particular in the last 5 years before diagnosis.
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ACKNOWLEDGMENTS
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The project was supported by grants from the Norwegian Research Council.
The authors give special thanks to Oddveig Selboe at Statistics Norway for providing information from databases and to Lars Klæboe and Jan Ivar Martinsen at the Cancer Registry of Norway for help in collecting and processing the data.
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NOTES
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Reprint requests to Dr. Jolanta Kliukiene, The Cancer Registry of Norway, Institute of Population-based Cancer Research, Montebello, N-0310 Oslo, Norway (e-mail: jolanta.kliukiene{at}kreftregisteret.no). 
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