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

International Journal of Radiation Biology

Volumn 82, Issue 1, 2006, Pages 1-12

  Juutilainen, Jukka ^a   Kumlin, Timo ^a   Naarala, Jonne ^a  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

Author keywords

Carcinogenesis; Combined effects; Extremely low frequency; Interaction; Magnetic field; Mechanisms; Meta analysis

Indexed keywords

CARCINOGEN; CHEMICAL AGENT; RADICAL; TOXIC SUBSTANCE;

CANCER; CANCER RISK; CARCINOGENESIS; CARCINOGENIC ACTIVITY; CARCINOGENICITY; CHILDHOOD CANCER; COMPARATIVE STUDY; DATA ANALYSIS; DOSE RESPONSE; ENVIRONMENTAL EXPOSURE; EPIDEMIOLOGICAL DATA; EXPERIMENTAL ANIMAL; EXPERIMENTAL MODEL; GENOTOXICITY; HUMAN; IN VITRO STUDY; LEUKEMIA; MAGNETIC FIELD; MOLECULAR INTERACTION; NONHUMAN; NONLINEAR SYSTEM; PRIORITY JOURNAL; PUBLICATION; RADIATION RESPONSE; REVIEW; RISK ASSESSMENT; RISK FACTOR; TOXICITY;

ANIMALS; APOPTOSIS; CARCINOGENS, ENVIRONMENTAL; ELECTROMAGNETIC FIELDS; HUMANS; NEOPLASMS; RISK ASSESSMENT;

ANIMALIA;

EID: 33645161799     PISSN: 09553002     EISSN: 13623095     Source Type: Journal    
DOI: 10.1080/09553000600577839     Document Type: Review

References (89)

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