Do extremely low frequency magnetic fields enhance the effects of environmental carcinogens? A meta-analysis of experimental studies

References

• Adair R K. Effects of very weak magnetic fields on radical pair reformation. Bioelectromagnetics 1999; 20: 255–263
   PubMed Web of Science ®Google Scholar
• Ager D D, Radul J A. Effect of 60-Hz magnetic fields on ultraviolet light-induced mutation and mitotic recombination in Saccharomyces cerevisiae. Mutation Research 1992; 283: 279–286
   PubMed Web of Science ®Google Scholar
• Anderson L E, Boorman G A, Morris J E, Sasser L B, Mann P C, Grumbein S L, Hailey J R, McNally A, Sills R C, Haseman J K. Effect of 13 week magnetic field exposures on DMBA-initiated mammary gland carcinomas in female Sprague-Dawley rats. Carcinogenesis 1999; 20: 1615–1620
   PubMed Web of Science ®Google Scholar
• Anderson L E, Morris J E, Sasser L B, Löscher W. Effects of 50- or 60-hertz, 100 microT magnetic field exposure in the DMBA mammary cancer model in Sprague-Dawley rats: Possible explanations for different results from two laboratories. Environmental Health Perspectives 2000; 108: 797–802
   PubMed Web of Science ®Google Scholar
• Ansari R M, Hei T K. Effects of 60 Hz extremely low frequency magnetic fields (EMF) on radiation- and chemical-induced mutagenesis in mammalian cells. Carcinogenesis 2000; 21: 1221–1226
   PubMedGoogle Scholar
• Balcer-Kubiczek E K, Zhang X F, Harrison G H, McCready W A, Shi Z M, Han L H, Abraham J M, Ampey L L, Meltzer S J, Jacobs M C, Davis C C. Rodent cell transformation and immediate early gene expression following 60-Hz magnetic field exposure. Environmental Health Perspectives 1996; 104: 1188–1198
   PubMedGoogle Scholar
• Boorman G A, Anderson L E, Morris J E, Sasser L B, Mann P C, Grumbein S L, Hailey J R, McNally A, Sills R C, Haseman J K. Effect of 26 week magnetic field exposures in a DMBA initiation-promotion mammary gland model in Sprague-Dawley rats. Carcinogenesis 1999; 20: 899–904
   PubMed Web of Science ®Google Scholar
• Brocklehurst B. Magnetic fields and radical reactions: Recent developments and their role in nature. Chemical Society Reviews 2002; 31: 301–311
   PubMed Web of Science ®Google Scholar
• Brocklehurst B, McLauchlan K A. Free radical mechanism for the effects of environmental electromagnetic fields on biological systems. International Journal of Radiation Biology 1996; 69: 3–24
   PubMed Web of Science ®Google Scholar
• Cain C D, Thomas D L, Adey W R. 60 Hz magnetic field acts as co-promoter in focus formation of C3H/10T1/2 cells. Carcinogenesis 1993; 14: 955–960
   PubMed Web of Science ®Google Scholar
• Del Carratore R, Morichetti E, Della Croce C, Bronzetti G. Effect of magnetic fields on rodent monooxygenase enzymes. Bioelectromagnetics 1995; 16: 324–329
   PubMed Web of Science ®Google Scholar
• DiCarlo A L, Farrell J M, Litovitz T A. Myocardial protection conferred by electromagnetic fields. Circulation 1999b; 99: 813–816
   PubMed Web of Science ®Google Scholar
• DiCarlo A L, Hargis M T, Penafiel L M, Litovitz T A. Short-term magnetic field exposures (60 Hz) induce protection against ultraviolet radiation damage. International Journal of Radiation Biology 1999a; 75: 1541–1549
   PubMed Web of Science ®Google Scholar
• DiCarlo A, White N, Guo F, Garrett P, Litovitz T. Chronic electromagnetic field exposure decreases HSP70 levels and lowers cytoprotection. Journal of Cellular Biochemistry 2002; 84: 447–454
   PubMed Web of Science ®Google Scholar
• DiGiovanni J, Johnston D A, Rupp T, Sasser L B, Anderson L E, Morris J E, Miller D L, Kavet R, Walborg E F, Jr. Lack of effect of a 60 Hz magnetic field on biomarkers of tumor promotion in the skin of SENCAR mice. Carcinogenesis 1999; 20: 685–689
   PubMedGoogle Scholar
• Ding G R, Nakahara T, Miyakoshi J. Exposure to power frequency magnetic fields and X-rays induces GAP-43 gene expression in human glioma MO54 cells. Bioelectromagnetics 2002; 23: 586–591
   PubMedGoogle Scholar
• Ding G R, Nakahara T, Tian F R, Guo Y, Miyakoshi J. Transient suppression of X-ray-induced apoptosis by exposure to power frequency magnetic fields in MCF-7 cells. Biochemical and Biophysical Research Communications 2001; 286: 953–957
   PubMed Web of Science ®Google Scholar
• Ding G R, Yaguchi H, Yoshida M, Miyakoshi J. Increase in X-ray-induced mutations by exposure to magnetic field (60 Hz, 5 mT) in NF-kappaB-inhibited cells. Biochemical and Biophysical Research Communications 2000; 276: 238–243
   PubMedGoogle Scholar
• Egger M, Davey Smith G, Schneider M, Minder C E. Bias in meta-analysis detected by a simple, graphical test. British Medical Journal 1997; 315: 629–634
   PubMed Web of Science ®Google Scholar
• Eveson R W, Timmel C R, Brocklehurst B, Hore P J, McLauchlan K A. The effects of weak magnetic fields on radical recombination reactions in micelles. International Journal of Radiation Biology 2000; 76: 1509–1522
   PubMed Web of Science ®Google Scholar
• Fairbairn D W, O'Neill K L. The effect of electromagnetic field exposure on the formation of DNA single strand breaks in human cells. Cellular and Molecular Biology (Noisy-le-grand) 1994; 40: 561–567
   PubMed Web of Science ®Google Scholar
• Finkel T. Oxidant signals and oxidative stress. Current Opinions in Cell Biology 2003; 15: 247–254
   PubMed Web of Science ®Google Scholar
• Fiorani M, Biagiarelli B, Vetrano F, Guidi G, Dacha M, Stocchi V. In vitro effects of 50 Hz magnetic fields on oxidatively damaged rabbit red blood cells. Bioelectromagnetics 1997; 18: 125–131
   PubMed Web of Science ®Google Scholar
• Frazier M E, Reese J A, Morris J E, Jostes R F, Miller D L. Exposure of mammalian cells to 60-Hz magnetic or electric fields: Analysis of DNA repair of induced, single-strand breaks. Bioelectromagnetics 1990; 11: 229–234
   PubMed Web of Science ®Google Scholar
• Gamble S C, Wolff H, Arrand J E. Syrian hamster dermal cell immortalization is not enhanced by power line frequency electromagnetic field exposure. British Journal of Cancer 1999; 81: 377–380
   PubMedGoogle Scholar
• Griffin G D, Khalaf W, Hayden K E, Miller E J, Dowray V R, Creekmore A L, Carruthers C W, Jr, Williams M W, Gailey P C. Power frequency magnetic field exposure and gap junctional communication in Clone 9 cells. Bioelectrochemistry 2000; 51: 117–123
   PubMed Web of Science ®Google Scholar
• Heredia-Rojas J A, Rodriguez-De La Fuente A O, del Roble Velazco-Campos M, Leal-Garza C H, Rodriguez-Flores L E, de La Fuente-Cortez B. Cytological effects of 60 Hz magnetic fields on human lymphocytes in vitro: Sister-chromatid exchanges, cell kinetics and mitotic rate. Bioelectromagnetics 2001; 22: 145–149
   PubMed Web of Science ®Google Scholar
• Hintenlang D E. Synergistic effects of ionizing radiation and 60 Hz magnetic fields. Bioelectromagnetics 1993; 14: 545–551
   PubMed Web of Science ®Google Scholar
• Hu G L, Chiang H, Zeng Q L, Fu Y D. ELF magnetic field inhibits gap junctional intercellular communication and induces hyperphosphorylation of connexin43 in NIH3T3 cells. Bioelectromagnetics 2001; 22: 568–573
   PubMed Web of Science ®Google Scholar
• Hu G L, Fu Y D, Zeng Q L, Xu Z P, Chiang H. Study on gap junctional intercellular communication inhibition by ELF magnetic fields using FRAP method. Electromagnetic Biology and Medicine 2002; 21: 155–160
   Web of Science ®Google Scholar
• IARC. Non-ionizing radiation, Part 1: static and extremely low-frequency (ELF) electric and magnetic fields. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans 2002; 80: 1–395
   PubMedGoogle Scholar
• ICNIRP. International Commission on Non-Ionizing Radiation Protection. ICNIRP guidelines: Guidelines for limiting exposure to time-varying electric, magnetic, and electromagnetic fields. Health Physics 1998; 74: 494–522
   PubMed Web of Science ®Google Scholar
• Ismael S J, Callera F, Garcia A B, Baffa O, Falcao R P. Increased dexamethasone-induced apoptosis of thymocytes from mice exposed to long-term extremely low frequency magnetic fields. Bioelectromagnetics 1998; 19: 131–135
   PubMed Web of Science ®Google Scholar
• Jajte J, Zmyslony M, Palus J, Dziubaltowska E, Rajkowska E. Protective effect of melatonin against in vitro iron ions and 7 mT 50 Hz magnetic field-induced DNA damage in rat lymphocytes. Mutation Research 2001; 483: 57–64
   PubMed Web of Science ®Google Scholar
• Juutilainen J, Lang S, Rytömaa T. Possible cocarcinogenic effects of ELF electromagnetic fields may require repeated long-term interaction with known carcinogenic factors. Bioelectromagnetics 2000; 21: 122–128
   PubMed Web of Science ®Google Scholar
• Juutilainen J, Liimatainen A. Mutation frequency in Salmonella exposed to weak 100-Hz magnetic fields. Hereditas 1986; 104: 145–147
   PubMed Web of Science ®Google Scholar
• Kawczyk-Krupka A, Sieron A, Shani J, Czuba Z B, Krol W. Biological effects of extremely low-frequency magnetic fields on stimulated macrophages J774.2 in cell culture. Electromagnetic Biology and Medicine 2002; 21: 141–153
   Web of Science ®Google Scholar
• Korneva H A, Grigoriev V A, Isaeva E N, Kaloshina S M, Barnes F S. Effects of low-level 50 Hz magnetic fields on the level of host defense and on spleen colony formation. Bioelectromagnetics 1999; 20: 57–63
   PubMed Web of Science ®Google Scholar
• Kumlin T, Heikkinen P, Kosma V M, Alhonen L, Jänne J, Juutilainen J. p53-independent apoptosis in UV-irradiated mouse skin: possible inhibition by 50 Hz magnetic fields. Radiation and Environmental Biophysics 2002; 41: 155–158
   PubMed Web of Science ®Google Scholar
• Kumlin T, Kosma V M, Alhonen L, Jänne J, Komulainen H, Lang S, Rytömaa T, Servomaa K, Juutilainen J. Effects of 50 Hz magnetic fields on UV-induced skin tumourigenesis in ODC-transgenic and non-transgenic mice. International Journal of Radiation Biology 1998; 73: 113–121
   PubMed Web of Science ®Google Scholar
• Lagroye I, Poncy J L. The effect of 50 Hz electromagnetic fields on the formation of micronuclei in rodent cell lines exposed to gamma radiation. International Journal of Radiation Biology 1997; 72: 249–254
   PubMed Web of Science ®Google Scholar
• Lagroye I, Poncy J L. Influences of 50-Hz magnetic fields and ionizing radiation on c-jun and c-fos oncoproteins. Bioelectromagnetics 1998; 19: 112–116
   PubMed Web of Science ®Google Scholar
• Li C M, Chiang H, Fu Y D, Shao B J, Shi J R, Yao G D. Effects of 50 Hz magnetic fields on gap junctional intercellular communication. Bioelectromagnetics 1999; 20: 290–294
   PubMed Web of Science ®Google Scholar
• Loberg L I, Engdahl W R, Gauger J R, McCormick D L. Cell viability and growth in a battery of human breast cancer cell lines exposed to 60 Hz magnetic fields. Radiation Research 2000b; 153: 725–728
   PubMed Web of Science ®Google Scholar
• Loberg L I, Luther M J, Gauger J R, McCormick D L. 60 Hz magnetic fields do not enhance cell killing by genotoxic chemicals in Ataxia telangiectasia and normal lymphoblastoid cells. Radiation Research 2000a; 153: 685–689
   PubMed Web of Science ®Google Scholar
• Löscher W. Do cocarcinogenic effects of ELF electromagnetic fields require repeated long-term interaction with carcinogens? Characteristics of positive studies using the DMBA breast cancer model in rats. Bioelectromagnetics 2001; 22: 603–614
   PubMed Web of Science ®Google Scholar
• Löscher W, Mevissen M, Lehmacher W, Stamm A. Tumor promotion in a breast cancer model by exposure to a weak alternating magnetic field. Cancer Letters 1993; 71: 75–81
   PubMed Web of Science ®Google Scholar
• Maes A, Collier M, Vandoninck S, Scarpa P, Verschaeve L. Cytogenetic effects of 50 Hz magnetic fields of different magnetic flux densities. Bioelectromagnetics 2000; 21: 589–596
   PubMed Web of Science ®Google Scholar
• Markkanen A, Juutilainen J, Lang S, Pelkonen J, Rytömaa T, Naarala J. Effects of 50 Hz magnetic field on cell cycle kinetics and the colony forming ability of budding yeast exposed to ultraviolet radiation. Bioelectromagnetics 2001; 22: 345–350
   PubMed Web of Science ®Google Scholar
• Mevissen M, Kietzmann M, Löscher W. In vivo exposure of rats to a weak alternating magnetic field increases ornithine decarboxylase activity in the mammary gland by a similar extent as the carcinogen DMBA. Cancer Letters 1995; 90: 207–214
   PubMed Web of Science ®Google Scholar
• Mevissen M, Lerchl A, Szamel M, Löscher W. Exposure of DMBA-treated female rats in a 50-Hz, 50 microTesla magnetic field: effects on mammary tumor growth, melatonin levels, and T lymphocyte activation. Carcinogenesis 1996; 17: 903–910
   PubMed Web of Science ®Google Scholar
• Miyakoshi J, Koji Y, Wakasa T, Takebe H. Long-term exposure to a magnetic field (5 mT at 60 Hz) increases X-ray-induced mutations. Journal of Radiation Research (Tokyo) 1999; 40: 13–21
   PubMed Web of Science ®Google Scholar
• Miyakoshi J, Mori Y, Yaguchi H, Ding G, Fujimori A. Suppression of heat-induced HSP-70 by simultaneous exposure to 50 mT magnetic field. Life Sciences 2000a; 66: 1187–1196
   PubMed Web of Science ®Google Scholar
• Miyakoshi J, Ohtsu S, Shibata T, Takebe H. Exposure to magnetic field (5 mT at 60 Hz) does not affect cell growth and c-myc gene expression. Journal of Radiation Research (Tokyo) 1996; 37: 185–191
   PubMed Web of Science ®Google Scholar
• Miyakoshi J, Tsukada T, Tachiiri S, Bandoh S, Yamaguchi K, Takebe H. Enhanced NOR-1 gene expression by exposure of Chinese hamster cells to high-density 50 Hz magnetic fields. Molecular and Cellular Biochemistry 1998; 181: 191–195
   PubMed Web of Science ®Google Scholar
• Miyakoshi J, Yoshida M, Shibuya K, Hiraoka M. Exposure to strong magnetic fields at power frequency potentiates X-ray-induced DNA strand breaks. Journal of Radiation Research (Tokyo) 2000c; 41: 293–302
   PubMed Web of Science ®Google Scholar
• Miyakoshi J, Yoshida M, Yaguchi H, Ding G R. Exposure to extremely low frequency magnetic fields suppresses X-ray-induced transformation in mouse C3H10T1/2 cells. Biochemical and Biophysical Research Communications 2000b; 271: 323–327
   PubMedGoogle Scholar
• Morandi M A, Pak C M, Caren R P, Caren L D. Lack of an EMF-induced genotoxic effect in the Ames assay. Life Sciences 1996; 59: 263–271
   PubMedGoogle Scholar
• Nakasono S, Ikehata M, Koana T, Saiki H. A 50 Hz, 14 mT magnetic field is not mutagenic or co-mutagenic in bacterial mutation assays. Mutation Research 2000; 471: 127–134
   PubMedGoogle Scholar
• Nindl G, Hughes E F, Johnson M T, Spandau D F, Vesper D N, Balcavage W X. Effect of ultraviolet B radiation and 100 Hz electromagnetic fields on proliferation and DNA synthesis of Jurkat cells. Bioelectromagnetics 2002; 23: 455–463
   PubMed Web of Science ®Google Scholar
• Normand S L. Meta-analysis: Formulating, evaluating, combining, and reporting. Statistics in Medicine 1999; 18: 321–359
   PubMed Web of Science ®Google Scholar
• Olkin I. Statistical and theoretical considerations in meta-analysis. Journal of Clinical Epidemiology 1995; 48: 133–146
   PubMed Web of Science ®Google Scholar
• Pafkova H, Jerabek J. Interaction of MF 50 Hz, 10 mT with high dose of X-rays: Evaluation of embryotoxicity in chick embryos. Reviews on Environmental Health 1994; 10: 235–241
   PubMedGoogle Scholar
• Pafkova H, Jerabek J, Tejnorova I, Bednar V. Developmental effects of magnetic field (50 Hz) in combination with ionizing radiation and chemical teratogens. Toxicological Letters 1996; 88: 313–316
   PubMed Web of Science ®Google Scholar
• Richard D, Lange S, Viergutz T, Kriehuber R, Weiss D G, Simko M. Influence of 50 Hz electromagnetic fields in combination with a tumour promoting phorbol ester on protein kinase C and cell cycle in human cells. Molecular and Cellular Biochemistry 2002; 232: 133–141
   PubMed Web of Science ®Google Scholar
• Robison J G, Pendleton A R, Monson K O, Murray B K, O'Neill K L. Decreased DNA repair rates and protection from heat induced apoptosis mediated by electromagnetic field exposure. Bioelectromagnetics 2002; 23: 106–112
   PubMed Web of Science ®Google Scholar
• Roy S, Noda Y, Eckert V, Traber M G, Mori A, Liburdy R, Packer L. The phorbol 12-myristate 13-acetate (PMA)-induced oxidative burst in rat peritoneal neutrophils is increased by a 0.1 mT (60 Hz) magnetic field. FEBS Letters 1995; 376: 164–166
   PubMed Web of Science ®Google Scholar
• Saffer J D, Chen G, Colburn N H, Thurston S J. Power frequency magnetic fields do not contribute to transformation of JB6 cells. Carcinogenesis 1997; 18: 1365–1370
   PubMedGoogle Scholar
• Scarfi M R, Bersani F, Cossarizza A, Monti D, Castellani G, Cadossi R, Franceschetti G, Franceschi C. Spontaneous and mitomycin C-induced micronuclei in human lymphocytes exposed to extremely low frequency pulsed magnetic fields. Biochemical and Biophysical Research Communications 1991; 176: 194–200
   PubMed Web of Science ®Google Scholar
• Simko M, Droste S, Kriehuber R, Weiss D G. Stimulation of phagocytosis and free radical production in murine macrophages by 50 Hz electromagnetic fields. European Journal of Cell Biology 2001b; 80: 562–566
   PubMed Web of Science ®Google Scholar
• Simko M, Richard D, Kriehuber R, Weiss D G. Micronucleus induction in Syrian hamster embryo cells following exposure to 50 Hz magnetic fields, benzo(a)pyrene, and TPA in vitro. Mutation Research 2001a; 495: 43–50
   PubMed Web of Science ®Google Scholar
• Snawder J E. Effect of magnetic field exposure on anchorage-independent growth of a promoter-sensitive mouse epidermal cell line (JB6). Environmental Health Perspectives 1999; 107: 195–198
   PubMedGoogle Scholar
• Steiner U E, Ulrich T. Magnetic field effects in chemical kinetics and related phenomena. Chemical Reviews 1989; 89: 51–147
   Web of Science ®Google Scholar
• Sterne J A, Gavaghan D, Egger M. Publication and related bias in meta-analysis: Power of statistical tests and prevalence in the literature. Journal of Clinical Epidemiology 2000; 53: 1119–1129
   PubMed Web of Science ®Google Scholar
• Sterne J A, et al. Funnel plots for detecting bias in meta-analysis: Guidelines on choice of axis. Journal of Clinical Epidemiology 2001; 54: 1046–1055
   PubMed Web of Science ®Google Scholar
• Suri A, deBoer J, Kusser W, Glickman B W. A 3 milliTesla 60 Hz magnetic field is neither mutagenic nor co-mutagenic in the presence of menadione and MNU in a transgenic rat cell line. Mutation Research 1996; 372: 23–31
   PubMed Web of Science ®Google Scholar
• Tabrah F L, Mower H F, Batkin S, Greenwood P B. Enhanced mutagenic effect of a 60 Hz time-varying magnetic field on numbers of azide-induced TA100 revertant colonies. Bioelectromagnetics 1994; 15: 85–93
   PubMed Web of Science ®Google Scholar
• Tao Q, Henderson A. EMF induces differentiation in HL-60 cells. Journal of Cellular Biochemistry 1999; 73: 212–217
   PubMed Web of Science ®Google Scholar
• Thun-Battersby S, Mevissen M, Löscher W. Exposure of Sprague-Dawley rats to a 50-Hertz, 100-microTesla magnetic field for 27 weeks facilitates mammary tumorigenesis in the 7,12-dimethylbenz[a]-anthracene model of breast cancer. Cancer Research 1999; 59: 3627–3633
   PubMed Web of Science ®Google Scholar
• Tian F, Nakahara T, Yoshida M, Honda N, Hirose H, Miyakoshi J. Exposure to power frequency magnetic fields suppresses X-ray-induced apoptosis transiently in Ku80-deficient xrs5 cells. Biochemical and Biophysical Research Communications 2002; 292: 355–361
   PubMed Web of Science ®Google Scholar
• Till U, Timmel C R, Brocklehurst B, Hore P J. The influence of very small magnetic fields on radical recombination reactions in the limit of slow recombination. Chemical Physics Letters 1998; 298: 7–14
   Web of Science ®Google Scholar
• Timmel C R, Till U, Brocklehurst B, McLaughlan K A, Hore P J. Effects of weak magnetic fields on free radical recombination reactions. Molecular Physics 1998; 95: 71–89
   Web of Science ®Google Scholar
• Tuinstra R, Goodman E, Greenebaum B. Protein kinase C activity following exposure to magnetic field and phorbol ester. Bioelectromagnetics 1998; 19: 469–476
   PubMed Web of Science ®Google Scholar
• Walleczek J, Shiu E C, Hahn G M. Increase in radiation-induced HPRT gene mutation frequency after nonthermal exposure to nonionizing 60 Hz electromagnetic fields. Radiation Research 1999; 151: 489–497
   PubMed Web of Science ®Google Scholar
• Wei M, Guizzetti M, Yost M, Costa L G. Exposure to 60-Hz magnetic fields and proliferation of human astrocytoma cells in vitro. Toxicology and Applied Pharmacology 2000; 162: 166–176
   PubMed Web of Science ®Google Scholar
• Yaguchi H, Yoshida M, Ding G R, Shingu K, Miyakoshi J. Increased chromatid-type chromosomal aberrations in mouse m5S cells exposed to power-line frequency magnetic fields. International Journal of Radiation Biology 2000; 76: 1677–1684
   PubMedGoogle Scholar
• Yaguchi H, Yoshida M, Ejima Y, Miyakoshi J. Effect of high-density extremely low frequency magnetic field on sister chromatid exchanges in mouse m5S cells. Mutation Research 1999; 440: 189–194
   PubMed Web of Science ®Google Scholar
• Yoshikawa T, Tanigawa M, Tanigawa T, Imai A, Hongo H, Kondo M. Enhancement of nitric oxide generation by low frequency electromagnetic field. Pathophysiology 2000; 7: 131–135
   PubMedGoogle Scholar
• Zmyslony M, Palus J, Jajte J, Dziubaltowska E, Rajkowska E. DNA damage in rat lymphocytes treated in vitro with iron cations and exposed to 7 mT magnetic fields (static or 50 Hz). Mutation Research 2000; 453: 89–96
   PubMed Web of Science ®Google Scholar