Nonthermal GSM RF and ELF EMF effects upon rat BBB permeability

Abstract

Since the late 1980s, our group has examined the effects of radiofrequency electromagnetic fields (RF-EMF), including pulse-modulated waves of the type emitted by mobile phones, upon the blood–brain barrier. In more than 2,000 rats, we have repeatedly demonstrated a passage of the rats’ own albumin from the blood through the brain capillaries into the surrounding brain parenchyma at SAR values down to 0.1mW/kg. In most of these experiments, the animals were exposed in TEM-cells, ventilated by an external electrical fan at 50 Hz. In the present study, we examined whether the extremely low frequency (ELF) magnetic fields from the fan (50 Hz, 0.3–1.5 μT) might add to the RF effect. Sixty-four rats were divided into 4 groups: RF only, ELF only and RF + ELF exposure plus a sham group. The GSM-900 MHz RF exposure was at the very low, nonthermal, average whole-body SAR level 0.4 mW/kg. Demonstration of the normally occurring albumin extravasation in the basal hypothalamus is our inbuilt control proving that the staining is reliable. Two full series of staining of the whole material gave negative results for hypothalamus. Not until we changed to avidin, biotin, and antibodies from a third supplier, we received an acceptable staining. Twenty-five percent of the RF animals had a pathological albumin leakage, while the ELF and RF + ELF groups with three and two pathological findings, respectively, were not significantly different from the control group. We conclude that the use of external fans has had no major influence upon the result.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Belyaev IY, Bauréus Koch C, Terenius O, Roxstrom-Lindquist K, Malmgren LOG, Sommer WH, Salford LG, Persson BRR (2006) Exposure of rat brain to 915 MHz GSM microwaves induces changes in gene expression but not double stranded DNA breaks or effects on chromatin conformation. Bioelectromagnetics 27:295–306

    Article  CAS  Google Scholar 

  2. Crawford ML (1974) Generation of standard EM using TEM transmission cells. IEEE Trans Electromagn Compat 16:189–195

    Article  Google Scholar 

  3. Eberhardt JL, Persson B, Brun A, Salford LG, Malmgren L (2008) Blood-brain barrier permeability and nerve cell damage in the rat brain 14 and 28 days after exposure to microwaves from GM mobile phones. Electromagn Biol Med 27:215–229

    Article  CAS  Google Scholar 

  4. Finnie JW, Blumbergs PC, Manavis JC (2001) Effect of global system for mobile communication (GSM)-like radiofrequency fields on vascular permeability in mouse brain. Pathology 33:338–340

    CAS  Google Scholar 

  5. Frank RN, Dutta S, Mancini MA (1987) Pericyte coverage is greater in the retinal than in the cerebral capillaries of the rat. Invest Ophthalmol Vis Sci 28:1086–1091

    CAS  Google Scholar 

  6. Fritze K, Sommer C (1997) Effect of global system for mobile communication (GSM) microwave exposure on BBB permeability in rat. Acta Neuropathol 94:465–470

    Article  CAS  Google Scholar 

  7. Ghersi-Egea JF, Minn A, Siest G (1988) A new aspect of the protective functions of the BBB: activities of four drug-metabolizing enzymes in isolated rat brain microvessels. Life Sci 42:2515–2523

    Article  CAS  Google Scholar 

  8. Grafström G, Nittby H, Brun A, Malmgren L, Persson BR, Salford L, Eberhardt J (2008) Histopathological examinations of rat brains after long-term exposure to GSM-900 mobile phone radiation. Brain Res Bull 77:257–263

    Article  Google Scholar 

  9. Gulturk S, Demirkazik A, Kosar I, Cetin A, Dokmets HS, Demir T (2010) Effect of exposure to 50 Hz magnetic field with or without insulin on blood-brain barrier permeability in streptozotocin-induced diabetic rats. Bioelectromagnetics 31:262–269

    Google Scholar 

  10. Kuribayashi M, Wang J, Fujiwara O, Doi Y, Nabae K, Tamano S, Ogiso T, Asamoto M, Shirai T (2005) Lack of effects of 1439 MHz electromagnetic near field exposure on the BBB in immature and young rats. Bioelectromagnetics 26:578–588

    Article  Google Scholar 

  11. Lai H (2004) Interaction of microwaves and a temporally incoherent magnetic field on spatial learning in the rat. Physiol Behav 82:785–789

    CAS  Google Scholar 

  12. Malmgren L (1998) Radio frequency systems for NMR imaging: coil development and studies of non-thermal biological effects. Dissertation, Lund University

  13. Martens L, van Hese J, De Zutter D, De Wagter C, Malmgren L, Persson BRR, Salford LG (1993) Electromagnetic field calculations used for exposure experiments on small animals in TEM-cells. Bioelectrochem Bioenerg 30:73–81

    Article  Google Scholar 

  14. McQuade JMS, Merritt JH, Miller SA, Scholin T, Cook MC, Salazar A, Rahimi OB, Murphy MR, Mason PA (2009) Radiofrequency-radiation exposure does not induce detectable leakage of albumin across the blood-brain barrier. Radiat Res 171:15–621

    Article  Google Scholar 

  15. Nittby H, Grafström G, Tian DP, Malmgren L, Brun A, Persson BRR, Salford LG, Eberhardt J (2008a) Cognitive impairment in rats after long-term exposure to GSM-900 mobile phone radiation. Bioelectromagnetics 29:219–232

    Article  Google Scholar 

  16. Nittby H, Widegren B, Krogh M, Grafström G, Berlin H, Rehn G, Eberhardt JL, Malmgren L, Persson BRR, Salford LG (2008b) Exposure to radiation from global system for mobile communications at 1, 800 MHz significantly changes gene expression in rat hippocampus and cortex. Environmentalist 28:458–465

    Article  Google Scholar 

  17. Nittby H, Grafström G, Eberhardt JL, Malmgren L, Brun A, Persson BRR, Salford LG (2008c) Radiofrequency and extremely low-frequency electromagnetic field effects on the blood-brain barrier. Electromagn Biol Med 27:103–126

    Article  Google Scholar 

  18. Nittby H, Brun A, Eberhardt J, Malmgren L, Persson BRR, Salford LG (2009) Increased blood-brain barrier permeability in the mammalian brain seven days after exposure to the radiation from a GSM-900 mobile phone. Pathophysiology 16:103–112

    Article  CAS  Google Scholar 

  19. Oberheim NA, Wang X, Goldman S, Nedergaard M (2006) Astrocytic complexity distinguishes the human brain. Trends Neurosci 29:547–553

    Article  CAS  Google Scholar 

  20. Oberheim NA, Takano T, Han X (2009) Uniquely hominid features of adult human astrocytes. J Neurosci 29:3276–3287

    Article  CAS  Google Scholar 

  21. Oztas B, Kalkan T, Tuncel H (2004) Influence of 50 Hz frequency sinusoidal magnetic field on the blood-brain barrier permeability of diabetic rats. Bioelectromagnetics 25:400–402

    Article  Google Scholar 

  22. Persson BRR, Salford LG, Brun A (1997) Blood-brain barrier permeability in rats exposed to electromagnetic fields used in wireless communication. Wireless Netw 3:455–461

    Article  Google Scholar 

  23. Salford LG, Brun A, Eberhardt J, Malmgren L, Persson BRR (1992) Electromagnetic field-induced permeability of the blood-brain barrier shown by immunohistochemical methods. In: Nordén B, Ramel C (eds) Interaction mechanism of low-level electromagnetic fields, living systems Oxford. Oxford University Press, UK, pp 251–258

    Google Scholar 

  24. Salford LG, Brun A, Eberhardt JL, Persson BRR (1993) Permeability of the blood-brain-barrier induced by 915 MHz electromagnetic-radiation, continuous wave and modulated at 8, 16, 50 and 200 Hz. Bioelectrochem Bioenerg 30:293–301

    Article  Google Scholar 

  25. Salford LG, Brun A, Sturesson K, Eberhardt J, Persson BRR (1994) Permeability of the blood-brain barrier induced by 915 MHz electromagnetic-radiation, continuous wave and modulated at 8, 16, 50 and 200 Hz. Microsc Res Tech 27:535–542

    Article  CAS  Google Scholar 

  26. Salford LG, Persson B, Malmgren L, Brun A (2001) Téléphonie Mobile et Barrière Sang-Cerveau. In : Téléphonie mobile—effects potentiels sur la santè des ondes électromagnétiques de haute fréquence Pietteur Marco Ed., Belgium, Emburg, pp. 141–152

  27. Salford LG, Brun AE, Eberhardt JL, Malmgren L, Persson BRR (2003) Nerve cell damage in mammalian brain after exposure to microwaves from GSM mobile phones. Environ Health Perspect 111:881–883

    Article  Google Scholar 

  28. Salford LG, Nittby H, Brun A, Grafström G, Eberhardt JL, Malmgren L, Persson BRR (2007) Nonthermal effects of EMF upon the mammalian brain: the Lund experience. Environmentalist 27:493–500

    Article  Google Scholar 

  29. Salford LG, Nittby H, Brun A, Eberhardt J, Malmgren L, Persson BRR (2010) Effects of microwave radiation upon the mammalian blood-brain barrier. Non-thermal effects and mechanism of interaction between electromagnetic fields and living matter. An ICEMS monograph. Eds Giuliani, Bologna 2010. Eur J Oncol 5:333–356

    Google Scholar 

  30. Shivers RR, Kavaliers M, Teskey GC, Prato ES, Pelletier RM (1987) Magnetic resonance imaging temporarily alters blood-brain barrier permeability in the rat. Neurosci Lett 76:25–31

    Article  CAS  Google Scholar 

  31. Sun WJ, Yu YN, Chiang H, Fu YD, Lu DQ (2001a) Effects of 50 Hz magnetic fields exposure on protein tyrosine phosphorylation in cultured cell. Electro- and magnetobiology 20:207–214

    CAS  Google Scholar 

  32. Sun WJ, Chiang H, Fu YD, Yu YN, Xie HY, Lu DQ (2001b) Exposure to 50 Hz electromagnetic fields induces the phosphorylation and activity of stress-activated protein kinase in cultured cells. Electro Magn 20:415–423

    Article  CAS  Google Scholar 

  33. Sun WJ, Chiang H, Fu Y, Lu D, Xu Z (2002) Effects of electromagnetic noise on the enhancement of stress-activated protein kinase (SAPK) phosphorylation induced by 50 Hz magnetic fields. Zhonghua Lao Dong Wei Sheng Zhi Ye Bing Za Zhi 20:246–248 (Article in Chinese.)

    CAS  Google Scholar 

  34. Thomas WE (1999) Brain macrophages: on the role of pericytes and perivascular cells. Brain Res Rev 31:42–57

    Article  CAS  Google Scholar 

  35. Töre F, Dulou PE, Haro E, Veyret B, Aubineau P (2001) Two-hour exposure to 2-W/kg, 900-MHZ GSM microwaves induces plasma protein extravasation in rat brain and dura mater. In: Proceedings of the 5th International congress of the EBEA. Helsinki, Finland, pp. 43–45

  36. Töre F, Dulou PE, Haro E, Veyret B, Aubineau P (2002) Effect of 2 h GSM-900 microwave exposures at 2.0, 0.5 and 0.12 W/kg on plasma protein extravasation in rat brain and dura mater. In: Proceedings of the 24th annual meeting of the BEMS, pp. 61–62

  37. Tsurita G, Nagawa H, Ueno S, Watanabe S, Taki M (2000) Biological and morphological effects on the brain after exposure of rats to a 1439 MHz TDMA field. Bioelectromagnetics 21:364–371

    Article  CAS  Google Scholar 

  38. Van Hese J, Martens L, De Zutter D, De Wagter C, Malmgren L, Persson BRR, Salford LG (1992) Simulation of the effects of inhomogenities in TEM transmission cells using the FDTD-method. IEEE Trans Electromagn Compat 34:292–298

    Article  Google Scholar 

Download references

Acknowledgments

We thank associate professor Gunnar Skagerberg, Department of Neurosurgery, Lund University for sharing his deep knowledge in staining techniques as well as his chemicals with us. We also thank BMA Catarina Blennow at the Rausing Laboratory for excellent technical assistance. This work was supported by grants from the Hans and Märit Rausing Charitable Foundation and from the Lund University Hospital research funds.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Henrietta Nittby.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Nittby, H., Brun, A., Strömblad, S. et al. Nonthermal GSM RF and ELF EMF effects upon rat BBB permeability. Environmentalist 31, 140–148 (2011). https://doi.org/10.1007/s10669-011-9307-z

Download citation

Keywords

  • Albumin
  • Blood–brain barrier
  • Electromagnetic field
  • Histopathology
  • Mobile phone
  • Rat