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American Journal of Epidemiology Advance Access originally published online on May 7, 2007
American Journal of Epidemiology 2007 166(3):263-269; doi:10.1093/aje/kwm080
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American Journal of Epidemiology © The Author 2007. Published by the Johns Hopkins Bloomberg School of Public Health. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org.

ORIGINAL CONTRIBUTIONS

Nighttime Exposure to Electromagnetic Fields and Childhood Leukemia: An Extended Pooled Analysis

Joachim Schüz1, Anne Louise Svendsen1, Martha S. Linet2, Mary L. McBride3, Eve Roman4, Maria Feychting5, Leeka Kheifets6, Tracy Lightfoot4, Gabor Mezei7, Jill Simpson4 and Anders Ahlbom5

1 Institute of Cancer Epidemiology, Danish Cancer Society, Copenhagen, Denmark
2 Division of Cancer Epidemiology and Genetics, National Cancer Institute, Rockville, MD
3 British Columbia Cancer Agency, Vancouver, British Columbia, Canada
4 Epidemiology and Genetics Unit, Department of Health Sciences, University of York, York, United Kingdom
5 Institute of Environmental Medicine, Karolinska Institute, Stockholm, Sweden
6 Department of Epidemiology, School of Public Health, University of California, Los Angeles, Los Angeles, CA
7 Electric Power Research Institute, Palo Alto, CA

Correspondence to Dr. Joachim Schüz, Institute of Cancer Epidemiology, Danish Cancer Society, Strandboulevarden 49, DK-2100 Copenhagen, Denmark (e-mail: joachim{at}cancer.dk).

Received for publication November 10, 2006. Accepted for publication February 7, 2007.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
It has been hypothesized that nighttime bedroom measurements of extremely low frequency electromagnetic fields (ELF EMF) may represent a more accurate reflection of exposure and have greater biologic relevance than previously used 24-/48-hour measurements. Accordingly, the authors extended a pooled analysis of case-control studies on ELF EMF exposure and risk of childhood leukemia to examine nighttime residential exposures. Data from four countries (Canada, Germany, the United Kingdom, and the United States) were included in the analysis, comprising 1,842 children diagnosed with leukemia and 3,099 controls (diagnosis dates ranged from 1988 to 1996). The odds ratios for nighttime ELF EMF exposure for categories of 0.1–<0.2 µT, 0.2–<0.4 µT, and ≥0.4 µT as compared with <0.1 µT were 1.11 (95% confidence interval (CI): 0.91, 1.36), 1.37 (95% CI: 0.99, 1.90), and 1.93 (95% CI: 1.11, 3.35), respectively. The fact that these estimates were similar to those derived using 24-/48-hour geometric mean values (odds ratios of 1.09, 1.20, and 1.98, respectively) indicates that the nighttime component cannot, on its own, account for the pattern observed. These results do not support the hypotheses that nighttime measures are more appropriate; hence, the observed association between ELF EMF and childhood leukemia still lacks a plausible explanation.

child; electromagnetic fields; epidemiologic methods; leukemia, lymphocytic, acute, L1; melatonin; meta-analysis; neoplasms

Abbreviations: CI, confidence interval; ELF EMF, extremely low frequency electromagnetic fields


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
In 2000, a pooled analysis of epidemiologic data on the relation between exposure to extremely low frequency electromagnetic fields (ELF EMF) and childhood leukemia showed a twofold increased risk associated with exposures of 0.4 µT or more but no relation with exposure below this level (1). The nine case-control studies included in the pooled analysis met specified quality criteria, including a defined population base and exposure assessment based on 24-hour or longer residential ELF EMF measurements (24-/48-hour ELF EMF) or calculations of ELF EMF from power lines based on historical power-load information. This pooled analysis was the primary impetus for the International Agency for Research on Cancer's classifying ELF EMF as a possible human carcinogen (2). The likelihood that the statistical association might be etiologically relevant is reduced by a lack of supportive data from experimental research and the absence of a plausible biologic explanation (2–5), and some investigations have suggested that selection bias and confounding may have led to overestimation of the risk (5–9).

Few researchers have evaluated potential errors in risk estimation resulting from possible exposure misclassification. German studies have shown a higher risk of childhood leukemia associated with nighttime ELF EMF measurements than with 24-hour measurements (10–12) and a statistically significant dose-response relation between nighttime ELF EMF and childhood leukemia (12). Nighttime measurements might represent a more appropriate measure of exposure than 24-/48-hour ELF EMF measurements, because children are likely to spend higher proportions of time in their bedrooms during the night than during the day (13), leading to less misclassification of actual exposure. Such misclassification would be likely to produce underestimation of the strength of the association (5). Additionally, nighttime exposure may be more biologically relevant. It has been hypothesized that exposure to ELF EMF at night may suppress nocturnal production and release of melatonin from the pineal gland, with melatonin being assumed to have oncostatic capabilities (14, 15). This hypothesis was put forward by Stevens (14) in relation to breast cancer risk in 1987, but epidemiologic and experimental studies have not shown clear evidence of associations between magnetic field exposure, melatonin, and risk of breast cancer (2). Nevertheless, there has been speculation that disruption of melatonin metabolism might account for the association between residential magnetic field exposures and childhood leukemia (15), and there has been heightened interest in evaluating the hypothesis further in light of recent findings that bone marrow cells produce melatonin (16, 17). Using data from the four studies in the previous pooled analysis (1) that included 24-/48-hour measurements, we evaluated the risk of childhood leukemia associated with nighttime ELF EMF exposure versus 24-/48-hour ELF EMF exposure.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
Subjects
We used data from our previous pooled analysis (1, 10, 11, 18–25), focusing on studies that included residential measurements of at least 24 hours' duration from which nighttime ELF EMF data could be extracted. Studies carried out in Canada (18), Germany (10–12), the United Kingdom (24), and the United States (25) met the eligibility criteria.

The United Kingdom study (24) had two measurement phases, with only phase 2 including measurements taken during the night; therefore, the United Kingdom data set was restricted to subjects with phase 2 measurements only. The first German study started in Lower Saxony and was extended to Berlin; results were first published for Lower Saxony alone (10) and later for Lower Saxony and Berlin combined (11). That study was included in the previous pooled analysis by Ahlbom et al. (1). A second German study was set up to confirm or refute the findings of the first study. Between completion of the first pooled analysis and the start of this one in November 2005, those results were published (12) and are included here.

Exposure assessment
Details on exposure assessment are shown in table 1. The following metrics were used for the present analysis. From the 48-hour personal dosimetry and 24-hour stationary area measurements taken in the child's bedroom in the Canadian study, we used the geometric mean of the nighttime period from the stationary measurement (18). The median magnetic field level for the nighttime period was used as the primary metric from the German studies (10–12). The geometric mean of the two nighttime periods from the 48-hour measurements taken in the United Kingdom study (24) comprised the metric for this study. From the US study (25), we employed the geometric mean of the nighttime period from the 24-hour child's bedroom measurement. For all studies, the nighttime period was defined as the time between 10:00 p.m. and 6:00 a.m., which corresponds to an 8-hour period. In accordance with the categories of our previous analysis (1), exposure was categorized into <0.1 µT, 0.1–<0.2 µT, 0.2–<0.4 µT, and ≥0.4 µT. The cutoff point of 0.4 µT was empirically established from epidemiologic studies on ELF EMF and childhood leukemia (1) and was not based on experimental studies or biologically based investigations.


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  		TABLE 1. Exposure assessment methods used in a pooled analysis of case-control study data on extremely low frequency electromagnetic fields and childhood leukemia risk, Canada, Germany, United Kingdom, and United States, 1988–1996

 
Statistical methods
We applied logistic regression models to estimate odds ratios and their respective 95 percent confidence intervals (26). All analyses were adjusted for sex, age group (0, 1, 2, 3, 4, 5–9, and 10–14 years), socioeconomic status, and region in Germany (East vs. West). The country-specific definitions of socioeconomic status used in our previous pooled analysis (1) were employed in the present investigation, including three levels of maternal education for Canada (18), two levels of combined parental education and household income in Germany (10–12), seven levels of a deprivation index from the United Kingdom (24), and six levels of household income in the United States (25). Therefore, the pooled risk estimates were also adjusted for country.

Risk estimates were calculated for comparisons of the three exposure categories described above with the baseline category of <0.1 µT. Dose-response was first investigated using ELF EMF as a continuous variable; we calculated risk for each 0.2-µT increase in exposure. Next, we fitted a dose-response curve by truncating the exposure scale to the left, defining measures below 0.1 µT as 0.05 µT, which was considered to be the detection limit for an accurate measurement. In an attempt to fit a spline for exposures above 0.1 µT, no knot point became statistically significant (data not shown); hence, the exposure was modeled linearly.

Risk estimates are shown for single countries and for the pooled study population with and without the inclusion of Germany, where the hypothesis-generating studies were conducted (10–12). Risk estimates were also calculated for specific subgroups defined a priori, including cases of acute lymphoblastic leukemia only and cases of acute lymphoblastic leukemia by age group (<5 years vs. 5–14 years). All analyses were performed with SAS 8.02 (SAS Institute Inc., Cary, North Carolina).

To evaluate agreement between nighttime ELF EMF exposure and 24-/48-hour ELF EMF exposure, we calculated weighted kappa coefficients. The kappa statistic ({kappa}) quantifies the extent of agreement beyond the level that would be expected by chance alone (27). Kappa values range from 1 (perfect agreement) to 0 (no agreement) to –1 (perfect disagreement), with values between 0.6 and 0.8 representing good agreement.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
The study population comprised 1,842 children with leukemia and 3,099 controls. Dates of diagnosis in the various studies ranged from 1988 to 1996. Of all cases, 272 came from Canada, 689 from Germany, 286 from the United Kingdom, and 595 from the United States. The corresponding figures for controls were 301, 1,710, 558, and 530, respectively. Among cases, 54.6 percent were boys, and the age distribution was 3.8 percent, 51.8 percent, 28.5 percent, and 15.9 percent for the age groups <1, 1–4, 5–9, and 10–14 years, respectively. Of the leukemia cases in this pooled data set, 1,668 children (90.6 percent) had acute lymphoblastic leukemia.

There was a good agreement between 24-/48-hour ELF EMF measurements and nighttime ELF EMF measurements (table 2). Of cases with 24-/48-hour ELF EMF exposure greater than or equal to 0.4 µT, 62.2 percent were in the same high exposure category during the night. Of cases with nighttime ELF EMF exposure greater than or equal to 0.4 µT, 69.7 percent were in the same high exposure category throughout the full day. The figures for controls were 69.2 percent and 75.0 percent, respectively. Overall agreement was similar for cases and controls. The highest agreement was seen in the United States (weighted {kappa} = 0.88 (95 percent confidence interval (CI): 0.85, 0.91) among cases and 0.81 (95 percent CI: 0.77, 0.86) among controls), followed by the United Kingdom ({kappa} = 0.79 (95 percent CI: 0.70, 0.89) among cases and 0.75 (95 percent CI: 0.67, 0.83) among controls), Germany ({kappa} = 0.78 (95 percent CI: 0.71, 0.86) among cases and 0.71 (95 percent CI: 0.64, 0.77) among controls), and Canada ({kappa} = 0.63 (95 percent CI: 0.55, 0.71) among cases and 0.71 (95 percent CI: 0.64, 0.78) among controls). Only in Canada was the agreement better among controls than among cases.


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  		TABLE 2. Agreement (distribution of participants) between exposure to extremely low frequency electromagnetic fields during the night and average exposure over a 24-/48-hour period in a pooled analysis of case-control study data from Canada, Germany, the United Kingdom, and the United States, 1988–1996

 
Table 3 shows the results of the main risk analyses. Overall, the risk estimates derived from 24-/48-hour ELF EMF and nighttime ELF EMF exposures were similar, and they were almost identical when exposures were modeled as continuous variables. Omitting the hypothesis-generating studies from the analysis (10–12) yielded slightly stronger associations with 24-/48-hour ELF EMF as compared with nighttime ELF EMF. Country-level differences (table 4) were stronger, with nighttime risks being higher than the 24-hour average in Germany, while the difference was not as pronounced in the United States, although there was a slight tendency towards a stronger association for nighttime exposure in the intermediate category of 0.2–<0.4 µT. No difference by exposure measure was seen in United Kingdom data. Canada showed an effect opposite that of Germany, with a weaker association for nighttime ELF EMF exposure than for 24-hour ELF EMF exposure.


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  		TABLE 3. Estimated risk of childhood leukemia for exposure to extremely low frequency electromagnetic fields during the night as compared with average exposure over a 24-/48-hour period in a pooled analysis of case-control study data from Canada, Germany, the United Kingdom, and the United States, 1988–1996

 

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  		TABLE 4. Estimated risk of childhood leukemia according to exposure to extremely low frequency electromagnetic fields during the night as compared with average exposures over a 24-/48-hour period, by country, in a pooled analysis of case-control study data from Canada, Germany, the United Kingdom, and the United States, 1988–1996

 
For acute lymphoblastic leukemia alone, risk estimates for 24-/48-hour and nighttime ELF EMF exposures were similar (data not shown). Further, no consistent age patterns were evident for nighttime ELF EMF; the odds ratios for the highest exposure category (≥0.4 µT) were 2.52 (95 percent CI: 1.15, 5.50) among children aged 5–14 years and 1.62 (95 percent CI: 0.71, 3.71) among children aged less than 5 years. On the other hand, in the intermediate exposure category (0.2–<0.4 µT), the odds ratios were 1.29 (95 percent CI: 0.79, 2.12) among children aged 5–14 years as compared with 1.56 (95 percent CI: 0.99, 2.47) among children aged less than 5 years. However, again, the two exposure measures led to similar risk estimates.

In a regression model including the two exposure measures, neither of the measures prevailed. The odds ratio was 1.12 (95 percent CI: 0.85, 1.48) for 24-/48-hour ELF EMF exposure and 1.10 (95 percent CI: 0.84, 1.45) for nighttime ELF EMF exposure.

In comparing the slope of the fitted dose-response analysis of 24-/48-hour ELF EMF with the respective slope of nighttime ELF EMF, both showed a statistically significant monotonic increase (p = 0.02 for 24-/48-hour ELF EMF and p = 0.04 for nighttime ELF EMF) (figure 1). The slope was slightly steeper for 24-/48-hour ELF EMF. The point estimates at higher ELF EMF levels illustrate that estimates at field levels above 0.4 µT became very imprecise due to small numbers. Therefore, the prediction of a significant monotonic increase was derived mainly from field levels between 0.1 µT and 0.4 µT.


Figure 1
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  		FIGURE 1. Comparison of dose-response trends for childhood leukemia risk according to nighttime and 24-/48-hour exposure to extremely low frequency electromagnetic fields in a pooled analysis of case-control studies from Canada, Germany, the United Kingdom, and the United States, 1988–1996. Each graph shows both the odds ratio point estimates rounded off in increments of 0.05 µT (solid line with filled circles) and the fitted linear curve (dashed line with open circles).

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
The results of this nighttime exposure analysis differed only marginally from those of our previous pooled analysis (1). Hence, our original conclusions remain the same. Overall, our data provide no support for the hypothesis that nighttime measurement is a more appropriate measure of ELF EMF exposure than 24-hour measurement. An apparently strong effect of nighttime exposure was confined to Germany (10–12). Because similar dose-response relations were present for both 24-/48-hour and nighttime exposure measures, the somewhat clearer dose-response relation for the current analysis as compared with our previous pooled analysis is almost certainly not due to the alternative exposure measure but to the exclusion of the Nordic studies (19, 20, 22, 23) and the inclusion of a second German study (12). The dose-response analysis, using either exposure measure, was primarily limited by the small number of children exposed to ELF EMF at levels of 0.4 µT or higher. The pattern of the data at these higher levels is compatible with trends ranging from a further increase in risk to a constant risk or even a downward gradient.

While there was little difference between nighttime measures and 24-/48-hour measures in the pooled analysis, nighttime exposure was more strongly linked with childhood leukemia risk in the German data, and a similar trend was seen in the US data. The choice of exposure measure made no difference in the United Kingdom, while results from Canada and Germany pointed in opposite directions. Although there were many similarities between the four countries, they had different designs: The sampling frames and methods used for selecting controls varied (Canada: government health insurance rolls, Germany: population registers, United Kingdom: family health services lists, United States: random digit dialing); measurement protocols differed (as described above); the time lag between diagnosis and measurement varied (shortest in the United Kingdom, followed by Canada, the United States, and Germany); and effect modifiers differed among studies (e.g., mobility in Canada). These differences in design features among the four studies are unlikely to have led to systematic differences across studies. This and the fact that the confidence intervals of the risk estimates were overlapping suggest that the country-specific differences in results according to exposure measure (nighttime vs. 24-/48-hour) may reflect random variation and support the view that restricting exposure to the nighttime period is not associated with a stronger childhood leukemia risk.

We had a smaller sample in the present pooled analysis than in the previous pooled analysis (1), because only studies with a minimum measurement interval of at least 24 hours were eligible. Because of restrictions on the availability of such data, slightly different exposure metrics were used to estimate nighttime ELF EMF—namely the median for the nighttime period in Germany (10–12) and the geometric mean in the remaining three studies (18, 24, 25). Other limitations of the current analysis were low participation rates (50–65 percent for cases and controls), raising concerns about selection bias (1, 2, 5, 8). Data suggested that families with a lower social status were particularly underrepresented among controls (6, 12, 28). In the US study, a direct link between socioeconomic characteristics and ELF EMF exposure was shown, with higher ELF EMF exposures being observed among persons of lower social class, suggesting a possible overestimation in risk due to selection bias (6). Similarly, in Germany, the likelihood of measuring higher fields increased with the number of apartments per building, and buildings with a higher number of apartments tended to be occupied by families of lower social status (29). Thus, the risk may also have been overestimated in the European setting. However, it is likely that this would have affected both 24-/48-hour ELF EMF and nighttime ELF EMF, since agreement between the two measures was good.

In conclusion, the results of this extended pooled analysis do not support the hypothesis that leukemia risk in children is more strongly associated with residential ELF EMF exposure measurements taken at night. Therefore, they do not indicate that using average field intensities from longer time periods (24 or 48 hours) introduces extra exposure misclassification leading to underestimation of risk. Furthermore, our data provide no support for the suggestion that exposure incurred during the night is biologically more relevant. While our results are in line with those of previous studies showing an association between ELF EMF exposure and childhood leukemia, the explanation for this association is still unknown.


   ACKNOWLEDGMENTS
 
The authors acknowledge funding from the Electric Power Research Institute, Palo Alto, California (grant EP-P19728/C9699).

Conflict of interest: none declared.


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

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