Bioelectromagnetics 21:480^482 (2000)

Brief Communication

Heart RateVariabilityand Physiological Arousalin Men Exposed to 60 Hz Magnetic Fields

Charles Graham,1* Antonio Sastre,1 Mary R. Cook,1 and Robert Kavet2

1Midwest Research Institute, Kansas City, MO2EPRI, PaloAlto, CA

In previous research, intermittent exposure to sinusoidal 60 Hz magnetic ®elds at a resultant ¯uxdensity of 28.3 mT was found to alter heart rate variability (HRV) in men during night sleep. Whenthe 24 men in the present study were exposed under similar conditions, HRV was not altered. Theprevious studies included the hourly collection of blood samples via an indwelling venous catheter,while the present study did not. This may account for the observed differences in results. Furtherresearch is needed to determine if ®eld exposure interacts with physiological arousal mechanisms toalter autonomic nervous system control over cardiac rhythms. Bioelectromagnetics 21:480±482, 2000. ß 2000 Wiley-Liss, Inc.

Key words: EMF; human; ECG; autonomic nervous system; cardiovascular disease

Epidemiologic and clinical research conductedover the past two decades has shown that reduced heartrate variability (HRV), especially in the low frequency(LF) band, is predictive of speci®c types of cardiovas-cular morbidity and mortality in otherwise healthypersons [Tsuji et al., 1994, 1996; Malik and Camm,1995; Liao et al., 1997]. Sastre et al. [1998] recentlyreported that overnight exposure of healthy men duringsleep to an intermittent 60 Hz circularly polarizedmagnetic ®eld at a resultant ¯ux density of 28.3mTaltered HRV. Speci®cally, exposure resulted in areduction of LF power and an increase in power inthe high frequency (HF) band of the HRV spectrum.Power alterations in the LF band re¯ect the actions ofthermoregulatory and blood pressure control mechan-isms on the heart, primarily mediated through thesympathetic branch of the autonomic nervous system(ANS). Alterations in HF power re¯ect respiratorycontrol mechanisms and consequent sinus arrhythmia,mediated through the parasympathetic branch of theANS.

The study reported here was based on the reportby Sastre et al. [1998] and the potentially importanthealth implications of altered HRV due to an environ-mental exposure. The relevance of this research isfurther highlighted by the recent epidemiological studyof electric utility workers by Savitz et al. [1999]. Theseauthors reported signi®cant associations of measuresof occupational magnetic ®eld exposure with mortalityfrom acute myocardial infarction and arrhythmia-

related diseases, but not with mortality from chroniccoronary heart disease and atherosclerosis. The formertwo disease categories are related to altered HRV,while the latter two categories are not.

The present study utilized a randomized, doubleblind, cross-over design in which each subject servedas his own control. Research participants were 24healthy, nonsmoking male volunteers (mean age 21.5years, range 18±33 years), who had regular sleep anddietary habits and were not taking medications. Thestudy protocol was approved by Midwest ResearchInstitute's Institutional Review Board, and writteninformed consent was obtained. Characteristics of theexposure facility in which the study was performedhave been documented by the U.S. Department ofEnergy as part of the National EMF-RAPID researchprogram [Olden, 1999], and the facility is described inDoynov et al. [1999]. Subjects slept in the facility onthree nights from 23:00±07:00 hours. On the shamcontrol night, they were only exposed to the ambient60 Hz background ®eld in the laboratory (� 0.2mT);

ß2000Wiley-Liss, Inc.

ÐÐÐÐÐÐContract grant sponsor: EPRI; Contract grant number: WO8021-12.

*Correspondence to: Charles Graham, Ph.D., Midwest ResearchInstitute, 425 Volker Boulevard, Kansas City, MO 64110. E-mail:cgraham@mriresearch.org

Received for review 28 October 1999; Final revision received 1March 2000

on another night, they were continuously exposed to acircularly polarized 60 Hz sinusoidal magnetic ®eldgenerated at a resultant ¯ux density of 28.3mT; and onanother night they were intermittently exposed to thesame ®eld.

Exposure order was counterbalanced such thatequal numbers of subjects would participate in eachcondition on each night. Eight subjects were randomlyassigned to be tested in the order sham/intermittent/continuous (SIC), eight in the order ICS, and eight inthe order CSI. Due to a computer error in subjectassignment, however, seven subjects were tested in the®rst order, eight in the second order and nine in thethird order. Intermittent exposure followed the proto-col described in Sastre et al. [1998]. This consisted ofalternating 1 h ®eld-on and ®eld-off periods. During®eld-off hours, the coils were not energized. During®eld-on hours, the ®eld cycled on and off at 15 sintervals. A zero current crossing technique enabledthe ®elds to be switched on and off without at the sametime generating high frequency magnetic ®eld tran-sients. An automated double blind control systemprevented subjects and investigators from knowingwhen control or exposure conditions were in effect.

Acquisition of cardiac data and statistical analy-sis of HRV also followed Sastre et al. [1998]. Theelectrocardiogram (lead II ECG) was sampled at256 Hz throughout each session and stored. A hard-ware detector (Beckman coupler Type 9857) identi®edthe R waves (ventricular contractions) in the ECG with0.1 ms accuracy. The R-R interval data were ®rstconverted to instantaneous heart rate to provide aregularly spaced time series with a 1 s resolution overthe period from midnight to 06:00 hours. In the Sastreet al. [1998] studies, blood was drawn from anindwelling venous catheter on the hour through thenight for determination of plasma melatonin levels. Toreduce possible artifacts associated with this proce-dure, the earlier investigators deleted 10 min segments(5 min before and after each hour) from the ECG dataset and analyzed HRV over six 50 min hours. Forcomparability, we performed the same data deletionprocedure here, even though blood samples were notcollected in the present study. Each 50 min hour wasfurther divided into three equal periods containing1024 points. After detrending and the application of aHamming window, a Digital Fourier Transform wasperformed on each period with the results expressed asthe power spectrum in the 0.0±0.5 Hz range.

Analysis of variance (ANOVA) for mixeddesigns was the primary statistical technique used toevaluate the HRV spectral analyses results. ExposureType (sham control, intermittent, continuous), Hour(midnight to 06:00 hours), and Period (1±3 in each h)

were the within-subject variables, and Exposure Order(1, 2, or 3) was the between subjects variable. Resultswere considered statistically signi®cant if P� 0.05.Probability values were corrected for lack of sphericityusing the Huynh±Feldt epsilon technique. Signi®cantmain effects or interactions were followed up withsimple effects analyses. Analyses were performed todetermine if the test conditions differed on total powerin all frequency bands of the HRV spectrum; absoluteand percent power in the low frequency (LF: 0.04±0.15 Hz) and high frequency (HF: 0.15±0.40 Hz)bands; and the power ratio between bands (LF/HF).Band de®nitions followed consensus guidelines[Anonymous, 1996].

No signi®cant effects were found for absolute orpercent power HRV values when analyzed by ANOVAfor possible ®eld-related changes in total power, powerin the LF and HF spectral bands, or the LF/HF ratio.Additional analyses were performed on the previouslydeleted 10 min ECG data segments to determine ifHRV parameters in the 5 min preceding each hourdiffered from HRV parameters in the 5 min followingeach hour. These analyses also failed to reveal any pre-post differences in total power, LF and HF power, orthe LF/HF ratio in any test condition. For purposes ofillustration, Figure 1 plots hourly mean values acrossthe night for percent power in the LF (Panel A) and HF(Panel B) spectral band under control and ®eldexposure conditions. Data for absolute power valuesare not presented due to space considerations, but areavailable from the ®rst author on request.

These results are not consistent with thosereported previously by Sastre et al. [1998]. A majordifference between the studies concerns the collec-tion of blood samples through the night. Althoughthe serial blood collection protocol used in theprevious studies was designed to minimize distur-bances, volunteers were somewhat aroused from sleepby this procedure; and individuals differed in theirdegree of responsiveness.

Physiological arousal level during sleep, asindexed by EEG-de®ned sleep stages, is known to betightly linked to alterations in HRV [e.g., seeOtzenberger et al., 1998]. Thus, these protocoldifferences between studies could potentially resultin changing demands being placed on cardiac controlmechanisms, through altered levels of sympatheticnervous system activity or disruption of the naturalpatterns of sleep, and hence lead to divergent HRVresults across studies. The possibility that the magnetic®eld may interact with arousal mechanisms to alterautonomic nervous system control of cardiac rhythmsrequires further investigation. Given the implicationsof the epidemiological results of Savitz et al. [1999], it

HRVandMagnetic Fields 481

is important to resolve inconsistencies in the labora-tory studies and to better understand the relationshipbetween acute cardiac responses and chronic cardio-vascular disease.

ACKNOWLEDGMENTS

We wish to thank Donald W. Rif¯e (night supervisor),Mary M. Gerkovich (statistics), Jeffrey L. Hackman(ECG signal processing), Richard M. Ulrich (program-ming) and Brian E. Peterson (data management).

REFERENCES

Anonymous. 1996. Heart rate variability: standards of measure-ment, physiological interpretation and clinical use. Specialreport, Task Force of the European Society of Cardiologyand the North American Society of Pacing and Electro-physiology. Circulation 93:1043±1065.

Doynov P, Cohen HD, Cook MR, Graham C. 1999. Test facility forhuman exposure to AC and DC magnetic ®elds. Bioelec-tromagnetics 20:101±111.

Liao D, Cai JC, Rosamond WD, Barnes RW, Hutchinson RG,Whitsel EA, Rautaharju P, Heiss G. 1997. Cardiac auto-nomic function and incident coronary heart disease: apopulation-based case-cohort study. Am J Epidemiol 145:696±706.

Malik M, Camm AJ. 1995. Heart rate variability. Armonk, NewYork: Futura Publ. Co.

Olden, K. 1999. NIEHS report on health effects from exposure topower-line frequency electric and magnetic ®elds. NIHPublication 99-4493.

Otzenberger H, Gron®er C, Simon C, Charloux A, Ehrhart J,Piquard F, Brandenberger G. 1998. Dynamic heart ratevariability: a tool for exploring sympathovagal balancecontinuously during sleep in men. Am J Physiol 275:H946±H950.

Sastre A, Cook MR, Graham C. 1998. Nocturnal exposure tointermittent 60-Hz magnetic ®elds alters human cardiacrhythm. Bioelectromagnetics, 19:98±106.

Savitz DA, Liao D, Sastre A, Kleckner RC, Kavet R. 1999.Magnetic ®eld exposure and cardiovascular disease mortal-ity among electric utility workers. Am J Epidemiol149:135±142.

Tsuji H, Venditti FJ, Manders ES, Evans JC, Larson MG, FeldmanCL, Levy D. 1994. Reduced heart rate variability andmortality risk in an elderly cohort: the Framingham heartstudy. Circulation 90:878±883.

Tsuji H, Martin G, Larson MG, Venditti FJ, Manders ES, Evans JC,Feldman CL, Levy D. 1996. Impact of reduced heart ratevariability on risk for cardiac events: the Framingham heartstudy. Circulation 94:2850±2855.

Fig. 1. Meanpercent power in the low frequency (LF,Panel A) andhigh frequency (HF, Panel B) bands of the HRV spectrum areplotted frommidnight to 06:00 hours.LF power wasnot alteredbyintermittent or continuous exposure to the magnetic field (60 Hz,28.3 mT), compared to the no-exposure control condition(F� 0.99,P� 0.45).HFpowershowedasimilarlackof field-relatedeffects (F�1.09,P� 0.37).

482 Graham et al.