Biological effects and safety in magnetic resonance imaging: a review

Valentina Hartwig, Giulio Giovannetti, Nicola Vanello, Massimo Lombardi, Luigi Landini, Silvana Simi, Valentina Hartwig, Giulio Giovannetti, Nicola Vanello, Massimo Lombardi, Luigi Landini, Silvana Simi

Abstract

Since the introduction of Magnetic Resonance Imaging (MRI) as a diagnostic technique, the number of people exposed to electromagnetic fields (EMF) has increased dramatically. In this review, based on the results of a pioneer study showing in vitro and in vivo genotoxic effects of MRI scans, we report an updated survey about the effects of non-ionizing EMF employed in MRI, relevant for patients' and workers' safety. While the whole data does not confirm a risk hypothesis, it suggests a need for further studies and prudent use in order to avoid unnecessary examinations, according to the precautionary principle.

Keywords: MRI safety; Magnetic Resonance Imaging; electromagnetic fields; genotoxic effects.

Figures

Figure 1.
Figure 1.
Electromagnetic spectrum and some sources of radiation.
Figure 2.
Figure 2.
MN induction at different times after cardiac MRI scans. * Statistically different from control (p

References

    1. Picano E. Sustainability of medical imaging. BMJ. 2004;328:578–580.
    1. Simi S, Ballardin M, Casella M, De Marchi D, Hartwig V, Giovannetti G, Vanello N, Gabbriellini S, Landini L, Lombardi M. Is the genotoxic effect of magnetic resonance negligible? Low persistence of micronucleus frequency in lymphocytes of individuals after cardiac scan. Mutat. Res. Fundam. Mol. Mech. Mutagen. 2008;645:39–43.
    1. Bonassi S, Znaor A, Ceppi M, Lando C, Chang WP, Holland N, Kirsch-Volders M, Zeiger E, Ban S, Barale R, Bigatti MP, Bolognesi C, Cebulska-Wasilewska A, Fabianova E, Fucic A, Hagmar L, Joksic G, Martelli A, Migliore L, Mirkova E, Scarfi MR, Zijno A, Norppa H, Fenech M. An increased micronucleus frequency in peripheral blood lymphocytes predicts the risk of cancer in humans. Carcinogenesis. 2007;28:625–631.
    1. McRobbie DW, Moore EA, Graves MJ, Prince MR. MRI - From Picture to Proton. Cambridge University Press; Cambridge, New York, USA: 2006.
    1. SCENIHR (Scientific Committee on Emerging and Newly Identified Health Risks) Possible effects of Electromagnetic Fields (EMF) on Human Health. European Commission; Brussels, Belgium: Mar 21, 2007.
    1. International Commission on Non-ionizing Radiation Protection (ICNIRP): Guidelines for limiting exposure to time-varying electric, magnetic, and electromagnetic fields (up to 300GHz) Health Phys. 1998;74:494–522.
    1. McNeil DG. M.R.I.’s Strong Magnets Cited in Accidents. New York Times. 2005 Aug 19;
    1. U.S. Food and Drug Administration (FDA) Medical Device Reporting (MDR) Available online: (accessed May 4, 2009)
    1. ECRI Health Device Alerts (HDA) Available online: (accessed May 4, 2009).
    1. Shellock FG. MR safety update 2002: implants and devices. J. Magn. Reson. Imaging. 2002;16:485–496.
    1. Formica D, Silvestri S. Biological effects of exposure to magnetic resonance imaging: an overview. BioMed. Eng. OnLine. 2004;3:11.
    1. Drinker CK, Thomson RM. Does the magnetic field constitute an industrial hazard? J. Ind. Hyg. 1921;3:117–129.
    1. Davis LD, Pappajohn K, Plavnieks IM. Bibliography of the biological effects of magnetic fields. Fed. Proc. 1962;21:1–38.
    1. Schenck JF. Safety of strong, static magnetic fields. J. Magn. Reson. Imaging. 2000;12:2–19.
    1. World Health Organization . Environmental Health Criteria 232. Static fields. World Health Organization; Geneva, Switzerland: 2006.
    1. Franco G, Perduri R, Murolo A. Effetti biologici da esposizione occupazionale a campi magnetostatici utilizzati in imaging a risonanza magnetica nucleare: una rassegna. Med. Lav. 2008;99:16–28.
    1. International Commission on Non-ionizing Radiation Protection (ICNIRP): Guidelines on limits of exposure to static magnetic field. Health Phys. 2009;96:504–514.
    1. Nakahara T, Yaguchi H, Yoshida M, Miyakoshi J. Effects of Exposure of CHO-K1 Cells to a 10-T Static Magnetic Field. Radiology. 2002;224:817–822.
    1. Valiron O, Peris L, Rikken G, Schweitzer A, Saoudi Y, Remy C, Job D. Cellular disorders induced by high magnetic fields. J. Magn. Reson. Imaging. 2005;22:334–340.
    1. Yamamoto T, Nagayama Y, Tamura M. A blood oxygenation dependent increase in blood viscosity due to a static magnetic field. Phys. Med. Biol. 2004;49:3267–3277.
    1. Myakoshi J.Effects of a static magnetic field at the cellular level Prog Biophys Mol Biol 2004. doi:10.1016/j.pbiomolbio.2004.08.008
    1. Tenforde TS, Gaffey CT, Moyer BR, Budinger TF. Cardiovascular alterations in Macaca monkeys exposed to stationary magnetic fields: experimental observations and theoretical analysis. Bioelectromagnetics. 1983;4:1–9.
    1. Saunders R. Static magnetic fields: animal studies. Prog. Biophys. Mol. Biol. 2005;87:225–239.
    1. Wikswo JP, Barach JP. An estimate of the steady magnetic field strength required to influence nerve conduction. IEEE Trans. Biomed. Eng. 1980;27:722–723.
    1. Rosen AD, Lubowsky J. Magnetic field influence on central nervous system function. Exp. Neurol. 1987;95:679–687.
    1. Rosen AD, Lubowsky J. Modification of spontaneous unit discharge in the lateral geniculate body by a magnetic field. Exp. Neurol. 1990;108:261–265.
    1. Rosen AD. Mechanism of action of moderate-intensity static magnetic fields on biological systems. Cell Biochem. Biophys. 2003;39:163–173.
    1. Kangarlu A, Burgess RE, Zhu H, Nakayama T, Hamlin RL, Abduljalil AM, Robataille PML. Cognitive, cardiac, and physiological safety studies in ultra high field magnetic resonance imaging. Magn. Reson. Imaging. 1999;17:1407–1416.
    1. High WB, Sikora J, Ugurbil K, Garwood M. Subchronic in vivo effects of a high static magnetic field (9.4 T) in rats. J. Magn. Reson. Imaging. 2000;12:122–139.
    1. Matthes R, McKinlay AF, Bernhardt JH, Vecchia P, Veyret B, editors. Biological Effects and Health Consequences (0–100 kHz) ICNIRP; Munich, Germany: 2003. International Commission on Non-ionizing Radiation (ICNIRP). Exposure to static and low frequency electromagnetic fields.
    1. McKinlay AF, Allen SG, Cox R, Dimbylow PJ, Mann SM, Muirhead CR, Saunders RD, Sienkiewicz ZJ, Stather JW, Wainwright PR. Review of the Scientific Evidence for Limiting Exposure to Electromagnetic Fields (0–300 GHz) 3 Vol. 15. NRPB; Chilton, UK: 2003.
    1. Suzuki Y, Ikehata M, Nakamura K, Nishioka M, Asanuma K, Koana T, Shimizu H. Induction of micronuclei in mice exposed to static magnetic fields. Mutagenesis. 2001;16:499–501.
    1. International Agency for Research on Cancer (IARC) IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. Non-Ionising Radiation. Part 1: Static and Extremely Low Frequency (ELF) Electric and Magnetic Fields, vol. 80. IARC; Lyon, France: 2002.
    1. Chakeres DW, De Vocht F. Static magnetic field effects on human subjects related to magnetic resonance imaging systems. Prog. Biophys. Mol. Biol. 2005;87:255–265.
    1. De Vocht F, van Drooge H, Engels H, Kromhout H. Exposure, health complaints and cognitive performance among employees of an MRI scanners manufacturing department. J. Magn. Reson. Imaging. 2006;23:197–204.
    1. De Vocht F, Stevens T, van Wendel De Joode B, Engels H, Kromhout H. Acute neurobehavioral effects of exposure to static magnetic fields: analyses of exposure-response relations. J. Magn. Reson. Imaging. 2006;23:291–297.
    1. Evans JA, Savitz DA, Kanal E, Gillen J. Infertility and pregnancy outcome among magnetic resonance imaging workers. J. Occup. Med. 1993;35:1191–1195.
    1. De Wilde JP, Rivers AW, Proce DL. A review of the current use of magnetic resonance imaging in pregnancy and safety implications for the fetus. Prog. Biophys. Mol. Biol. 2005;87:335–353.
    1. Feychting M. Health effects of static magnetic fields—a review of the epidemiological evidence. Prog. Biophy. Mol. Biol. 2005;87:241–246.
    1. Greenland S, Sheppard AR, Kaune WT, Poole C, Kelsh MA. A pooled analysis of magnetic fields, wire codes, and childhood leukemia. Childhood Leukemia-EMF Study Group. Epidemiology. 2000;11:624–634.
    1. Foliart DE, Pollock BH, Mezei G, Iriye R, Silva JM, Ebi KL, Kheifets L, Link MP, Kavet R. Magnetic field exposure and long-term survival among children with leukaemia. Br. J. Cancer. 2006;94:161–164.
    1. Forssen UM, Rutqvist LE, Ahlbom A, Feychting M. Occupational magnetic fields and female breast cancer: a case-control study using Swedish population registers and new exposure data. Am. J. Epidemiol. 2005;161:250–259.
    1. Vogt FM, Ladd ME, Hunold P, Mateiescu S, Hebrank FX, Zhang A, Debatin JF, Göhde SC. Increased time rate of change of gradient fields: effect on peripheral nerve stimulation at clinical MR imaging. Radiology. 2004;233:548–554.
    1. Crozier S, Wang H, Trakic A, Liu F. Exposure of workers to pulsed gradients in MRI. J. Mag. Res. Imaging. 2007;26:1236–1254.
    1. Lai H, Singh NP. Magnetic-field-induced DNA strand breaks in brain cells of the rat. Environ. Health Perspect. 2004b;112:687–694.
    1. Fedrowitz M, Westermann J, Löscher W. Magnetic field exposure increases cell proliferation but does not affect melatonin levels in the mammary gland of female Sprague Dawley rats. Cancer Res. 2002;62:1356–1363.
    1. Scarfí MR, Sannino A, Perrotta A, Sarti M, Mesirca P, Bersani F. Evaluation of genotoxic effects in human fibroblasts after intermittent exposure to 50 Hz electromagnetic fields: a confirmatory study. Radiat. Res. 2005;164:270–276.
    1. Geard CR, Osmak RS, Hall EJ, Simon HE, Maudsley AA, Hilal SK. Magnetic resonance and ionizing radiation: A comparative evaluation in vivo of oncogenic and genotoxic potential. Radiology. 1984;152:199–202.
    1. Cohen MM, Kunska A, Astemborski JA, McCulloch D, Paskewitz DA. Effect of low-level, 60-Hz electromagnetic fields on human lymphoid cells: I. Mitotic rate and chromosome breakage in human peripheral lymphocytes. Bioelectromagnetics. 1986;7:415–423.
    1. Cohen MM, Kunska A, Astemborski JA, McCulloch D. Effect of low-level, 60-Hz electromagnetic fields on human lymphoid cells: II. Sister-chromatid exchanges in peripheral lymphocytes and lymphoblastoid cell lines. Mutat. Res. 1986;172:177–184.
    1. Liboff AR, Williams T, Jr, Strong DM, Wistar R., Jr Time-varying magnetic fields: effect on DNA synthesis. Science. 1984;223:818–820.
    1. Rodegerdts EA, Gronewaller EF, Kehlbach R, Roth P, Wiskirchen J, Gebert R, Claussen CD, Duda S. In vitro evaluation of teratogenic effects by time-varying MR gradient fields on fetal human fibroblast. J. Magn. Reson. Imaging. 2000;12:150–156.
    1. Juutilainen J, Kumlin T, Naarala J. Do extremely low frequency magnetic fields enhance the effects of environmental carcinogens? A meta-analysis of experimental studies. Int. J. Radiat. Biol. 2006;82:1–12.
    1. Nyenhuis JA, Bourland JD, Mouchawar GA, Elabbady TZ, Geddes LA, Schaefer DJ, Riehl ME. Comparison of stimulation effects of longitudinal and transverse MRI gradient coils. Proceedings of the Society for Magnetic Resonance in Medicine Annual Meeting; San Francisco, CA, USA. 1990; p. 1275.
    1. Bourland JD, Nyenhuis JA, Mouchawar GA, Geddes LA, Schaefer DJ. Human peripheral nerve stimulation from z-gradients. Proceedings of the Society for Magnetic Resonance in Medicine Annual Meeting; San Francisco, CA, USA. 1990; p. 1157.
    1. Bourland JD, Nyenhuis JA, Schaefer DJ. Physiologic effects of intense MR Imaging gradient fields. Neuroimaging Clin. N. Am. 1999;9:363–377.
    1. Juutilainen J. Developmental effects of electromagnetic fields. Bioelectromagnetics. 2005;7:S107–115.
    1. Schaefer DJ, Bourland JD, Nyenhuis JA. Review of patient safety in time-varying gradient fields. J. Magn. Reson. Imaging. 2000;12:20–29.
    1. International Electrotechnical Commission . IEC 60601-2-33 Particular requirements for basic safety and essential performance of magnetic resonance equipment for medical diagnosis. 2nd ed. International Electrotechnical Commission; Geneva, Switzerland: 2002.
    1. Reilly JP. Applied bioelectricity: From electrical stimulation to electropathology. Springer-Verlag; New York, NY, USA: 1998.
    1. Krasin F, Wagner H. Biological effects of nonionizing electromagnetic radiation. In: Webster JG, editor. Encyclopedia of Medical Devices and Instrumentation. Wiley; Hoboken, NJ, USA: 1988.
    1. Polk C. Biological effects of nonionizing electromagnetic fields. In: Bronzino JD, editor. Handbook of biomedical engineering. J. CRC Press; Boca Raton, FL, USA: 1995.
    1. Shellock FG. Radiofrequency energy-induced heating during MR procedures: a review. J. Magn. Reson. Imaging. 2000;12:30–36.
    1. Shellock FG, Rothman B, Sarti D. Heating of the scrotum by highfield strength MR imaging. Am. J. Roentgenol. 1990;154:1229–1232.
    1. Shellock FG, Crues JV. Corneal temperature changes associated with high-field MR imaging using a head coil. Radiology. 1988;167:809–811.
    1. Vahlensieck M. Tattoo-related cutaneous inflammation (burn grade I) in a mid-field MR scanner (letter) Eur. Radiol. 2000;10:197.
    1. Wagle WA, Smith M. Tattoo-induced skin burn during MR imaging (letter) Am. J. Roentgenol. 2000;174:1795.
    1. Kreidstein ML, Giguere D, Freiberg A. MRI interaction with tattoo pigments: case report, pathophysiology, and management. Plast. Reconstr. Surg. 1997;99:1717–1720.
    1. Bottomley PA, Redington RW, Edelstein WA, Schenck JF. Estimating radiofrequency power deposition in body NMR imaging. Magn. Reson. Med. 1985;2:336–349.
    1. Adair ER, Berglund LG. On the thermoregulatory consequences of NMR imaging. Magn. Reson. Imaging. 1986;4:321–333.
    1. Shellock FG, Schaefer DJ, Crues JV. Alterations in body and skin temperatures caused by MR imaging: is the recommended exposure for radiofrequency radiation too conservatice? Brit. J. Radiol. 1989;62:904–909.
    1. Van den Berg CAT, van den Bergen B, van de Kamer JB, Raaymakers BW, Kroeze H, Bartels LW, Lagendijk JJW. Simultaneous B+1 Homogenization and Specific Absorption Rate Hotspot Suppression Using a Magnetic Resonance Phased Array Transmit Coil. Mag. Res. Med. 2007;57:577–586.
    1. Liu F, Zhao HW, Crozier S. Calculation of electric fields induced by body and head motion in high-field MRI. J. Magn. Reson. 2003;161:99–107.
    1. Meltz ML. Radiofrequency exposure and mammalian cell toxicity, genotoxicity, and transformation. Biolectrom. Suppl. 2003;6:S196–S213.
    1. Diem E, Schwarz C, Adlkofer F, Jahn O, Rudiger H. Non-thermal DANN breakage by mobile phone radiation (1800 MHz) in human fibroblasts and in transformed GFSH-R17 rat granulosa cells in vitro. Mutat. Res. 2005;583:178–183.
    1. Nikolova T, Czyz J, Rolletschek A, Blyszczuk P, Fuchs J, Jovtchev G. Electromagnetic fields affect transcript levels of apoptosis-related genes in embryonic stem cell-derived neural progenitor cells. FASEB J. 2005;19:1686–1693.
    1. Speit G, Schutz P, Hoffmann H. Genotoxic effects of exposure to radiofrequency electromagnetic fields (RF-EMF) in cultured mammalian cells are not independently reproducible. Mutat. Res. 2007;626:42–47.
    1. Lantow M, Viergutz T, Weiss DG, Simkó M. Comparative study of cell cycle kinetics and induction of apoptosis or necrosis after exposure to radiofrequency radiation in human Mono Mac 6 cells. Radiat. Res. 2006c;166:539–543.
    1. Caraglia M, Marra M, Mancinelli F, D’Ambrosio G, Massa R, Giordano A, Budillon A, Abbruzzese A, Bismuto E. Electromagnetic fields at mobile phone frequency induce apoptosis and inactivation of the multi-chaperone complex in human epidermoid cancer cells. J. Cell. Physiol. 2005;204:39–48.
    1. Scarfì MR, Fresegna AM, Villani P, Pinto R, Marino C, Sarti M, Altavista P, Sannino A, Lovisolo GA. Exposure to radiofrequency radiation (900 MHz, GSM signal) does not affect micronucleus frequency and cell proliferation in human peripheral blood lymphocytes: an interlaboratory study. Radiat. Res. 2006;165:655–663.
    1. Zeni O, Schiavoni A, Perrotta A, Forigo D, Depilano M, Scarfi MR. Evaluation of genotoxic effects in human leukocytes after in vitro exposure to 1950 MHz UMTS radiofrequency field. Bioelectromagnetics. 2008;29:177–184.
    1. Saunders RD, Kowalczuk CI, Beechley CV, Dunford R. Studies of the induction of dominant lethal and translocations in male mice after chronic exposure to microwave radiation. Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med. 1988;53:983–992.
    1. Lloyd DC, Saunders RD, Moquet JE, Kowalczuk CI. Absence of chromosomal damage in human lymphocytes exposed to microwave radiation with hyperthermia. Bioelectromagnetics. 1986;7:235–237.
    1. Muscat JE, Malkin MG, Thompson S, Shore RE, Stellman SD, McRee D, Neugut AI, Wynder EL. Handheld cellular telephone use and risk of brain cancer. JAMA. 2000;284:3001–3007.
    1. Inskip PD, Hatch EE, Stewart PA, Heineman EF, Ziegler RG, Dosemeci M, Parry D, Rothman N, Boice JD, Wilcosky TC, Watson DJ, Shapiro WR, Selker RG, Fine HA, Black P, Loeffler JS, Linet MS. Study design for a case-control investigation of cellular telephones and other risk factors for brain tumours in adults. Radiat. Prot. Dosim. 1999;86:45–52.
    1. Hardell L, Nasman A, Pahlson A, Hallquist A, Hansson Mild K. Use of cellular telephones and the risk for brain tumours: a case–control study. Int. J. Oncol. 1999;15:113–116.
    1. Lonn S, Ahlbom A, Hall P, Feychting M. Long-term mobile phone use and brain tumour risk. Am. J. Epidemiol. 2005;161:526–535.
    1. Schüz J, Böhler E, Berg G, Schlehofer B, Hettinger I, Schlaefer K, Wahrendorf J, Kunna-Grass K, Blettner M. Cellular phones, cordless phones, and the risk of glioma and meningioma (Interphone study group, Germany) Am. J. Epidemiol. 2006a;163:512–520.
    1. Elwood JM. Epidemiological studies of radio frequency exposures and human cancer. Biolectrom Suppl. 2003;6:S63–S73.
    1. IEE Position Statement. The Possible Harmful Biological Effects of Low Level Electromagnetic Fields of Frequencies up to 300 GHz 2002Available online: (accessed June 5, 2009)
    1. Christ A, Kuster N. Differences in RF energy absorption in the heads of adults and children. Bioelectromagnetics. 2005;7:S31–44.
    1. Regel SJ, Negovetic S, Röösli M, Berdinas V, Schuderer J, Huss A, Lott U, Kuster N, Achermann P. UMTS base station-like exposure, well being and cognitive performance. Environ. Health Perspect. 2006;114:1270–1275.
    1. Schaefer DJ, Barber BJ, Gordon CJ, Zielonka J, Hecker J. Book of abstracts, Society for magnetic resonance in medicine Volume 2. Society for Magnetic Resonance in Medicine; Berkeley, CA, USA: 1985. Thermal effects of magnetic resonance imaging; p. 925.
    1. Shellock FG, Schaefer DJ, Crues JV. Evaluation of skin blood flow, body and skin temperatures in man during MR imaging at high levels of RF energy. Magn. Reson. Imaging. 1989;7:335.
    1. Kido DK, Morris TW, Erickson JL, Plewes DB, Simon JH. Physiologic changes during high field strength MR imaging. Am. J. Roentgenol. 1987;148:1215–1218.
    1. Shellock FG, Schaefer DJ, Kanal E. Physiologic responses to MR imaging performed at an SAR level of 6.0 W/Kg. Radiology. 1994;192:865–868.
    1. Shellock FG, Schatz CJ. Increases in corneal temperature caused by MR imaging of the eye with a dedicated local coil. Radiology. 1992;185:697–699.
    1. International Commission on Non-ionizing Radiation Protection (ICNIRP): medical magnetic resonance (MR) procedures: Protection of patients. Health Phys. Soc. 2004;87:197–216.
    1. Shellock FG, Crues JV. MR Procedures: biologic effects, safety, and patient care. Radiology. 2004;232:635–652.
    1. Shellock FG, Slimp G. Severe burn of the finger caused by using a pulse oximeter during MR imaging (letter) Am. J. Roentgenol. 1989;153:1105.
    1. Shellock FG, Spinazzi A. MRI safety update 2008: part 1, MRI contrast agents and nephrogenic systemic fibrosis. Am. J. Roentgenol. 2008;191:1129–1139.
    1. Schiffer IB, Schreiber WG, Graf R, Schreiber EM, Jung D, Rose DM, Hehn M, Gebhard S, Sagemüller J, Spiess HW, Oesch F, Thelen M, Hengstler JG. No influence of magnetic fields on cell cycle progression using conditions relevant for patients during MRI. Bioelectromagnetics. 2003;24:241–250.
    1. Magin RL, Lee JK, Klintsova A, Carnes KI, Dunn F. Biological Effects of Long-Duration, High-Field (4 T) MRI on Growth and Development in the Mouse. J. Mag. Res. Imaging. 2000;12:140–149.
    1. Ali MA. Magnetic resonance imaging and associated alteration in some biophysical properties of blood. Rom. J. Biophys. 2007;17:277–286.
    1. Karpowicz J, Hietanen M, Gryz K. Occupational risk from static magnetic fields of MRI scanners. Environmentalist. 2007;27:533–538.
    1. Directive 2004/40/EC of the European Parliament and of the Council of 29 April 2004 on the minimum health and safety requirements regarding the exposure of workers to the risks arising from physical agents (electromagnetic fields). Official Journal of the European Union L 159 of 30 April 2004 (and corrigenda L 184 of 24 May 2004).Available online: (accessed June 21, 2005).
    1. Zaremba LA. Guidance for Industry and FDA Staff: Criteria for Significant Risk Investigations of Magnetic Resonance Diagnostic Devices US. Department of Health and Human Services Food and Drug Administration; Silver Spring, MD, USA: 2003. Available online: (accessed December 2003)
    1. IAPO . Policy Statement on Patient Involvement. IAPO; London, UK: 2005. Available online: (accessed June 2005)
    1. Welch HG, Schwartz L, Woloshin S. What’s making us sick is an epidemic of diagnoses. New York Times. 2007 Jan 2;

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