Experimental studies on carcinogenicity of radiofrequency radiation in animals

Critical Reviews in Environmental Science and Technology

Volumn 41, Issue 18, 2011, Pages 1664-1695

  Juutilainen, Jukka ^a   Heikkinen, Päivi ^a   Lagroye, Isabelle ^b   Miyakoshi, Junji ^c   Van Rongen, Eric ^d   Saunders, Richard ^e   De Seze, Rene ^f   Tenforde, Thomas ^g   Verschaeve, Luc ^h   Veyret, Bernard ^b   Xu, Zhengping ⁱ  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

^b UNIVERSITÉ DE BORDEAUX   (France)

^c KYOTO UNIVERSITY   (Japan)

^d Health Council of the Netherlands   (Netherlands)

^e PUBLIC HEALTH ENGLAND   (United Kingdom)

^f INSTITUT NATIONAL DE L ENVIRONNEMENT INDUSTRIEL ET DES RISQUES INERIS   (France)

^g NATIONAL COUNCIL ON RADIATION PROTECTION AND MEASUREMENTS   (United States)

^h SCIENTIFIC INSTITUTE OF PUBLIC HEALTH   (Belgium)

ⁱ ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

cancer; electromagnetic fields; mobile phones

Indexed keywords

ANIMAL STUDIES; CANCER; CARCINOGENIC EFFECTS; EPIDEMIOLOGICAL STUDIES; EXPERIMENTAL MODELS; EXPERIMENTAL STUDIES; EXPOSURE LEVEL; HUMAN EXPOSURES; MOBILE TELEPHONY; MOBILE-PHONE USERS; RADIO FREQUENCIES; RADIO FREQUENCY RADIATION; RF FIELDS; TUMOR CELLS;

DISEASES; ELECTROMAGNETIC FIELDS; MOBILE DEVICES; MOBILE PHONES; MOBILE TELECOMMUNICATION SYSTEMS; TELEPHONE; TELEPHONE SETS; TUMORS;

ANIMALS;

ANTINEOPLASTIC AGENT;

ANIMAL; BIOASSAY; CANCER; CARCINOGEN; ELECTROMAGNETIC FIELD; EPIDEMIOLOGY; EXPERIMENTAL STUDY; HEALTH IMPACT; HEALTH RISK; IRRADIATION; LITERATURE REVIEW; MOBILE COMMUNICATION; TUMOR;

ARTICLE; BRAIN TUMOR; BREAST TUMOR; CANCER TRANSPLANTATION; CARCINOGENESIS; CARCINOGENICITY; COLON TUMOR; ELECTROMAGNETIC FIELD; EXPERIMENTAL MODEL; EXPERIMENTAL STUDY; GENETIC PREDISPOSITION; GENOTOXICITY; LIVER CARCINOGENESIS; LYMPHOMA; MOBILE PHONE; NONHUMAN; RADIATION EXPOSURE; RADIOFREQUENCY RADIATION; TUMOR CELL;

ANIMALIA; RODENTIA;

EID: 79956290817     PISSN: 10643389     EISSN: 15476537     Source Type: Journal    
DOI: 10.1080/10643389.2010.481584     Document Type: Article

References (66)

1. Adey, W.R., Byus, C.V., Cain, C.D., Higgins, R.J., Jones, R.A., Kean, C.J., Kuster, N., MacMurray, A., Stagg, R.B., and Zimmerman, G. (1999). Spontaneous and nitrosourea-induced primary tumors of the central nervous system in Fischer 344 rats chronically exposed to 836 MHz modulated microwaves. Radiation Research, 152, 293-302. (Pubitemid 29413665)
2. Adey, W.R., Byus, C.V., Cain, C.D., Higgins, R.J., Jones, R.A., Kean, C.J., Kuster, N., MacMurray, A., Stagg, R.B., and Zimmerman, G. (2000). Spontaneous and nitrosourea-induced primary tumors of the central nervous system in Fischer 344 rats exposed to frequency-modulated microwave fields. Cancer Research, 60, 1857-63. (Pubitemid 30207644)
3. Ahlbom, A., Bridges, J., de Seze, R., Hillert, L., Juutilainen, J., Mattsson, M.O., Neubauer, G., Schuz, J., Simko, M., and Bromen, K. (2008). Possible effects of electromagnetic fields (EMF) on human health-opinion of the scientific committee on emerging and newly identified health risks (SCENIHR). Toxicology, 246, 248-50.
4. Ahlbom, A., Feychting, M., Green, A., Kheifets, L., Savitz, D.A., and Swerdlow, A.J. (2009). Epidemiologic evidence on mobile phones and tumor risk: A review. Epidemiology, 20, 639-52.
5. Ahlbom, A., Green, A., Kheifets, L., Savitz, D., and Swerdlow, A. (2004). Epidemiology of health effects of radiofrequency exposure. Environmental Health Perspectives, 112, 1741-54. (Pubitemid 40017297)
6. Ames, B.N., and Gold, L.S. (1990). Too many rodent carcinogens: Mitogenesis increases mutagenesis. Science, 249, 970-1.
7. Anane, R., Dulou, P.E., Taxile, M., Geffard, M., Crespeau, F.L., and Veyret, B. (2003). Effects of GSM-900 microwaves on DMBA-induced mammary gland tumors in female Sprague-Dawley rats. Radiation Research, 160, 492-7. (Pubitemid 37174518)
8. Anderson, L.E., Sheen, D.M., Wilson, B.W., Grumbein, S.L., Creim, J.A., and Sasser, L.B. (2004). Two-year chronic bioassay study of rats exposed to a 1.6 GHz radiofrequency signal. Radiation Research, 162, 201-10. (Pubitemid 39100020)
9. Bartsch, H., Bartsch, C., Seebald, E., Deerberg, F., Dietz, K., Vollrath, L., and Mecke, D. (2002). Chronic exposure to a GSM-like signal (mobile phone) does not stimulate the development of DMBA-induced mammary tumors in rats: Results of three consecutive studies. Radiation Research, 157, 183-90. (Pubitemid 34101370)
10. Chagnaud, J.L., Moreau, J.M., and Veyret, B. (1999). No effect of short-term exposure to GSM-modulated low-power microwaves on benzo(a)pyrene-induced tumours in rats. International Journal of Radiation Biology, 75, 1251-6. (Pubitemid 29500007)
11. Chou, C.K., Guy, A.W., Kunz, L.L., Johnson, R.B., Crowley, J.J., and Krupp, J.H. (1992). Long-term, low-level microwave irradiation of rats. Bioelectromagnetics, 13, 469-96.
12. Dewhirst, M.W., Lora-Michiels, M., Viglianti, B.L., Dewey, W.C., and Repacholi, M. (2003). Carcinogenic effects of hyperthermia. International Journal of Hyperthermia, 19, 236-51. (Pubitemid 36740797)
13. Ebert, S., Eom, S.J., Schruderer, J., Apostel, U., Tillmann, T., Dasenbrock, C., and Kuster, N. (2005). Response, thermal regulatory threshold and thermal breakdown threshold of restrained RF-exposed mice at 905 MHz. Physics in Medicine and Biology, 50, 5203-5215. (Pubitemid 41503998)
14. Foster, K.R., and Repacholi, M.H. (2004). Biological effects of radiofrequency fields: Does modulation matter? Radiation Research, 162, 219-25. (Pubitemid 39100022)
15. Frei, M.R., Berger, R.E., Dusch, S.J., Guel, V., Jauchem, J.R., Merritt, J.H., and Stedham, M.A. (1998a). Chronic exposure of cancer-prone mice to low-level 2450 MHz radiofrequency radiation. Bioelectromagnetics, 19, 20-31. (Pubitemid 128474913)
16. Frei, M.R., Jauchem, J.R., Dusch, S.J., Merritt, J.H., Berger, R.E., and Stedham, M.A. (1998b). Chronic, low-level (1.0 W/kg) exposure of mice prone to mammary cancer to 2450 MHz microwaves. Radiation Research, 150, 568-76. (Pubitemid 28499057)
17. Goldstein, L.S., Kheifets, L., van Deventer, E., and Repacholi, M. (2003a). Comments on ?Long-term exposure of Emicro-Pim1 transgenic mice to 898.4 MHz microwaves does not increase lymphoma incidence? by Utteridge et al., Radiat. Res. 158, 357-364 (2002). Radiation Research, 159, 275-6; author reply 276-8.
18. Goldstein, L.S., Kheifets, L., Van Deventer, E., and Repacholi, M. (2003b). Further comments on ?Long-term exposure of Emu-Pim1 transgenic mice to 898.4 MHz microwaves does not increase lymphoma incidence? by Utteridge et al. Radiation Research, 159, 835-6. (Pubitemid 36676876)
19. Heikkinen, P., Ernst, H., Huuskonen, H., Komulainen, H., Kumlin, T., Maki-Paakkanen, J., Puranen, L., and Juutilainen, J. (2006). No effects of radiofrequency radiation on 3-chloro-4-(dichloromethyl)-5-hydroxy-2(5H)- furanoneinduced tumorigenesis in female Wistar rats. Radiation Research, 166, 397-408. (Pubitemid 44157377)
20. Heikkinen, P., Kosma, V.M., Alhonen, L., Huuskonen, H., Komulainen, H., Kumlin, T., Laitinen, J.T., Lang, S., Puranen, L., and Juutilainen, J. (2003). Effects of mobile phone radiation on UV-induced skin tumourigenesis in ornithine decarboxylase transgenic and non-transgenic mice. International Journal of Radiation Biology, 79, 221-33. (Pubitemid 36774199)
21. Heikkinen, P., Kosma, V.M., Hongisto, T., Huuskonen, H., Hyysalo, P., Komulainen, H., Kumlin, T., Lahtinen, T., Lang, S., and Puranen, L. (2001). Effects of mobile phone radiation on X-ray-induced tumorigenesis in mice. Radiation Research, 156, 775-85. (Pubitemid 34024273)
22. Higashikubo, R., Culbreth, V.O., Spitz, D.R., LaRegina, M.C., Pickard, W.F., Straube, W.L., Moros, E.G., and Roti, J.L. (1999). Radiofrequency electromagnetic fields have no effect on the in vivo proliferation of the 9L brain tumor. Radiation Research, 152, 665-71.
23. Hruby, R., Neubauer, G., Kuster, N., and Frauscher, M. (2008). Study on potential effects of "902-MHz GSM-type Wireless Communication Signals" on DMBAinduced mammary tumours in Sprague-Dawley rats. Mutation Research, 649, 34-44. (Pubitemid 350235303)
24. Huang, T.Q., Lee, J.S., Kim, T.H., Pack, J.K., Jang, J.J., and Seo, J.S. (2005). Effect of radiofrequency radiation exposure on mouse skin tumorigenesis initiated by 7,12-dimethybenz[alpha]anthracene. International Journal of Radiation Biology, 81, 861-7.
25. Imaida, K., Kuzutani, K., Wang, J., Fujiwara, O., Ogiso, T., Kato, K., and Shirai, T. (2001). Lack of promotion of 7,12-dimethylbenz[a]anthracene- initiated mouse skin carcinogenesis by 1.5 GHz electromagnetic near fields. Carcinogenesis, 22, 1837-41. (Pubitemid 33064850)
26. Imaida, K., Taki, M., Watanabe, S., Kamimura, Y., Ito, T., Yamaguchi, T., Ito, N., and Shirai, T. (1998a). The 1.5 GHz electromagnetic near-field used for cellular phones does not promote rat liver carcinogenesis in a medium-term liver bioassay. Japanese Journal of Cancer Research, 89, 995-1002. (Pubitemid 28544773)
27. Imaida, K., Taki, M., Yamaguchi, T., Ito, T., Watanabe, S., Wake, K., Aimoto, A., Kamimura, Y., Ito, N., and Shirai, T. (1998b). Lack of promoting effects of the electromagnetic near-field used for cellular phones (929.2 MHz) on rat liver carcinogenesis in a medium-term liver bioassay. Carcinogenesis, 19, 311-4. (Pubitemid 28375426)
28. International Commission on Non-Ionizing Radiation Protection. (1998). Guidelines for limiting exposure to time-varying electric, magnetic, and electromagnetic fields (up to 300 GHz). Health Physics, 74, 494-522.
29. Jauchem, J.R., Ryan, K.L., Frei, M.R., Dusch, S.J., Lehnert, H.M., and Kovatch, R.M. (2001). Repeated exposure of C3H/HeJ mice to ultra-wideband electromagnetic pulses: lack of effects on mammary tumors. Radiation Research, 155, 369-77. (Pubitemid 32125989)
30. Juutilainen, J., and de Seze, R. (1998). Biological effects of amplitude-modulated radiofrequency radiation. Scandinavian Journal of Work, Environment & Health, 24, 245-54. (Pubitemid 28425321)
31. Juutilainen, J., Lang, S., and Rytomaa, T. (2000). Possible cocarcinogenic effects of ELF electromagnetic fields may require repeated long-term interaction with known carcinogenic factors. Bioelectromagnetics, 21, 122-8.
32. Keenan, K.P., Laroque, P., Ballam, G.C., Soper, K.A., Dixit, R., Mattson, B.A., Adams, S.P., and Coleman, J.B. (1996). The effects of diet, ad libitum overfeeding, and moderate dietary restriction on the rodent bioassay: the uncontrolled variable in safety assessment. Toxicologic Pathology, 24, 757-68. (Pubitemid 27029927)
33. Klurfeld, D.M., Lloyd, L.M., Welch, C.B., Davis, M.J., Tulp, O.L., and Kritchevsky, D. (1991). Reduction of enhanced mammary carcinogenesis in LA/N-cp (corpulent) rats by energy restriction. Proceedings of the Society for Experimental Biology and Medicine, 196, 381-4.
34. Kundi, M. (2003a). Comments on ?Long-term exposure of Emicro-Pim1 transgenic mice to 898.4 MHz microwaves does not increase lymphoma incidence? by Utteridge et al. Radiation Research, 159, 274-8. (Pubitemid 36182407)
35. Kundi, M. (2003b). Comments on the responses of Utteridge et al. (Radiat. Res. 159, 277-278, 2003) to letters about their paper (Radiat. Res. 158, 357-364, 2002). Radiation Research, 160, 613-4.
36. La Regina, M., Moros, E.G., Pickard, W.F., Straube, W.L., Baty, J., and Roti Roti, J.L. (2003). The effect of chronic exposure to 835.62 MHz FDMA or 847.74 MHz CDMA radiofrequency radiation on the incidence of spontaneous tumors in rats. Radiation Research, 160, 143-51. (Pubitemid 36897493)
37. Lerchl, A. (2003). Comments on the recent publication on microwave effects on Emicro-Pim1 transgenic mice (Utteridge et al., Radiat. Res. 158, 357-364, 2002). Radiation Research, 159, 276-8.
38. Logani, M.K., Bhanushali, A., Anga, A., Majmundar, A., Szabo, I., and Ziskin, M.C. (2004). Combined millimeter wave and cyclophosphamide therapy of an experimental murine melanoma. Bioelectromagnetics, 25, 516-23. (Pubitemid 39421851)
39. Logani, M.K., Szabo, I., Makar, V., Bhanushali, A., Alekseev, S., and Ziskin, M.C. (2006). Effect of millimeter wave irradiation on tumor metastasis. Bioelectromagnetics, 27, 258-64.
40. Mason, P.A., Walters, T.J., DiGiovanni, J., Beason, C.W., Jauchem, J.R., Dick, E.J., Jr., Mahajan, K., Dusch, S.J., Shields, B.A., and Merritt, J.H. (2001). Lack of effect of 94 GHz radio frequency radiation exposure in an animal model of skin carcinogenesis. Carcinogenesis, 22, 1701-8. (Pubitemid 32952150)
41. Moulder, J.E., Foster, K.R., Erdreich, L.S., and McNamee, J.P. (2005). Mobile phones, mobile phone base stations and cancer: A review. International Journal of Radiation Biology, 81, 189-203. (Pubitemid 40911069)
42. Oberto, G., Rolfo, K., Yu, P., Carbonatto, M., Peano, S., Kuster, N., Ebert, S., and Tofani, S. (2007). Carcinogenicity study of 217 Hz pulsed 900 MHz electromagnetic fields in Pim1 transgenic mice. Radiation Research, 168, 316-26. (Pubitemid 351295134)
43. Radzievsky, A.A., Gordiienko, O.V., Szabo, I., Alekseev, S.I., and Ziskin, M.C. (2004). Millimeter wave-induced suppression of B16 F10 melanoma growth in mice: Involvement of endogenous opioids. Bioelectromagnetics, 25, 466-73. (Pubitemid 39166581)
44. Repacholi, M.H., Basten, A., Gebski, V., Noonan, D., Finnie, J., and Harris, A.W. (1997). Lymphomas in E mu-Pim1 transgenic mice exposed to pulsed 900 MHZ electromagnetic fields. Radiation Research, 147, 631-40. (Pubitemid 27204100)
45. Salford, L.G., Brun, A., and Persson, B. (1997). Brain tumour development in rats exposed to electromagnetic fields used in wireless communication. Wireless Networks, 3, 463-469. (Pubitemid 127718358)
46. Salford, L.G., Brun, A., Persson, B.R.R., and Eberhardt, J. (1993). Experimental studies of brain-tumor development during exposure to continuous and pulsed 915 Mhz radiofrequency radiation. Bioelectrochemistry and Bioenergetics, 30, 313-318.
47. Saran, A., Pazzaglia, S., Mancuso, M., Rebessi, S., Di Majo, V., Tanori, M., Lovisolo, G.A., Pinto, R., and Marino, C. (2007). Effects of exposure of newborn patched1 heterozygous mice to GSM, 900 MHz. Radiation Research, 168, 733-40. (Pubitemid 351295110)
48. Shirai, T., Ichihara, T., Wake, K., Watanabe, S., Yamanaka, Y., Kawabe, M., Taki, M., Fujiwara, O., Wang, J., and Takahashi, S. (2007). Lack of promoting effects of chronic exposure to 1.95-GHz W-CDMA signals for IMT-2000 cellular system on development of N-ethylnitrosourea-induced central nervous system tumors in F344 rats. Bioelectromagnetics, 28, 562-72. (Pubitemid 47556777)
49. Shirai, T., Kawabe, M., Ichihara, T., Fujiwara, O., Taki, M., Watanabe, S., Wake, K., Yamanaka, Y., Imaida, K., and Asamoto, M. (2005). Chronic exposure to a 1.439 GHz electromagnetic field used for cellular phones does not promote N-ethylnitrosourea induced central nervous system tumors in F344 rats. Bioelectromagnetics, 26, 59-68. (Pubitemid 40053364)
50. Sinha, D.K., Gebhard, R.L., and Pazik, J.E. (1988). Inhibition of mammary carcinogenesis in rats by dietary restriction. Cancer Letters, 40, 133-41.
51. Smith, P., Kuster, N., Ebert, S., and Chevalier, H.J. (2007). GSM and DCS wireless communication signals: Combined chronic toxicity/carcinogenicity study in the Wistar rat. Radiation Research, 168, 480-92. (Pubitemid 351303176)
52. Sommer, A.M., Bitz, A.K., Streckert, J., Hansen, V.W., and Lerchl, A. (2007). Lymphoma development in mice chronically exposed to UMTS-modulated radiofrequency electromagnetic fields. Radiation Research, 168, 72-80. (Pubitemid 351292927)
53. Sommer, A.M., Streckert, J., Bitz, A.K., Hansen, V.W., and Lerchl, A. (2004). No effects of GSM-modulated 900 MHz electromagnetic fields on survival rate and spontaneous development of lymphoma in female AKR/J mice. BMC Cancer, 4, 77.
54. Szmigielski, S., Szudzinski, A., Pietraszek, A., Bielec, M., Janiak, M., and Wrembel, J.K. (1982). Accelerated development of spontaneous and benzopyrene-induced skin cancer in mice exposed to 2450-MHz microwave radiation. Bioelectromagnetics, 3, 179-91. (Pubitemid 13227690)
55. Tillmann, T., Ernst, H., Ebert, S., Kuster, N., Behnke, W., Rittinghausen, S., and Dasenbrock, C. (2007). Carcinogenicity study of GSM and DCS wireless communication signals in B6C3F1 mice. Bioelectromagnetics, 28, 173-87. (Pubitemid 46555874)
56. Toler, J.C., Shelton, W.W., Frei, M.R., Merritt, J.H., and Stedham, M.A. (1997). Longterm, low-level exposure of mice prone to mammary tumors to 435 MHz radiofrequency radiation. Radiation Research, 148, 227-34. (Pubitemid 27374099)
57. Utteridge, T.D., Gebski, V., Finnie, J.W., Vernon-Roberts, B., and Kuchel, T.R. (2002). Long-term exposure of E-mu-Pim1 transgenic mice to 898.4 MHz microwaves does not increase lymphoma incidence. Radiation Research, 158, 357-64. (Pubitemid 34919924)
58. Valberg, P.A., van Deventer, T.E., and Repacholi, M.H. (2007). Workgroup report: Base stations and wireless networks-radiofrequency (RF) exposures and health consequences. Environmental Health Perspectives, 115, 416-24. (Pubitemid 46554441)
59. Vecchia, P., Matthes, R., Ziegelberger, G., Lin, J., Saunders, R., and Swerdlow, A. (2009). Exposure to high frequency electromagnetic fields, biological effects and health consequences (100 kHz-300 GHz). ICNIRP 16/2009. International Commission on Non-Ionizing Radiation Protection 2009.
60. Vijayalaxmi, Obe, G. (2004). Controversial cytogenetic observations in mammalian somatic cells exposed to radiofrequency radiation. Radiation Research, 162, 481-96.
61. Vijayalaxmi, Prihoda, T.J. (2008). Genetic damage in mammalian somatic cells exposed to radiofrequency radiation: A meta-analysis of data from 63 publications (1990-2005). Radiation Research, 169, 561-74.
62. World Health Organization. (1993). Electromagnetic fields (300 Hz-300 GHz). Environmental Health Criteria 137. Geneva, Switzerland: World Health Organization.
63. Wu, R.Y., Chiang, H., Shao, B.J., Li, N.G., and Fu, Y.D. (1994). Effects of 2.45-GHz microwave radiation and phorbol ester 12-O-tetradecanoylphorbol-13- acetate on dimethylhydrazine-induced colon cancer in mice. Bioelectromagnetics, 15, 531-8.
64. Yu, D., Shen, Y., Kuster, N., Fu, Y., and Chiang, H. (2006). Effects of 900 MHz GSM wireless communication signals on DMBA-induced mammary tumors in rats. Radiation Research, 165, 174-80. (Pubitemid 43153130)
65. Zook, B.C., and Simmens, S.J. (2001). The effects of 860 MHz radiofrequency radiation on the induction or promotion of brain tumors and other neoplasms in rats. Radiation Research, 155, 572-83. (Pubitemid 32260255)
66. Zook, B.C., and Simmens, S.J. (2006). The effects of pulsed 860 MHz radiofrequency radiation on the promotion of neurogenic tumors in rats. Radiation Research, 165, 608-15.