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(Radiology. 2000;215:858-862.)
© RSNA, 2000

Experimental Studies

Human Fetal Lung Fibroblasts: In Vitro Study of Repetitive Magnetic Field Exposure at 0.2, 1.0, and 1.5 T1

Jakub Wiskirchen, MD, Eckart F. Grönewäller, MD, Frank Heinzelmann, Rainer Kehlbach, PhD, Enno Rodegerdts, MD, Matthias Wittau, H. Peter Rodemann, PhD, Claus D. Claussen, MD and Stephan H. Duda, MD

1 From the Departments of Diagnostic Radiology (J.W., E.F.G., F.H., R.K., E.R., M.W., C.D.C., S.H.D.) and Radiotherapy, Section of Radiobiology and Environmental Research (H.P.R.), Eberhard-Karls-Universität, Hoppe-Seyler-St 3, 72076 Tüebingen, Germany. Received February 26, 1999; revision requested April 28; final revision received September 14; accepted October 4. Supported in part by grant no. 257 from the forüne research program, University of Tüebingen, Germany. Address correspondence to J.W. (e-mail: jakub.wiskirchen@uni-tuebingen.de).


   Abstract
TOP
 Abstract
Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
PURPOSE: To evaluate whether repetitive exposure to magnetic fields of 0.2, 1.0, and 1.5 T affect the growth of human fetal lung fibroblasts (HFLFs).

MATERIALS AND METHODS: Cultured HFLFs were exposed to static magnetic fields of 0.2, 1.0, and 1.5 T for 1 h/d for 5 consecutive days. Control groups were kept under identical environmental conditions, apart from the magnetic field, during the experiments. Cell cycle analysis for synchronously and nonsynchronously growing cells was performed. Population doublings (PDs) were calculated. To rule out midterm effects, proliferation kinetics of the cells were analyzed for 21 days.

RESULTS: Cell cycle analysis of synchronized and nonsynchronized cells did not reveal statistically significant differences between the exposed and control cells. The PDs did not indicate any growth modulation during exposure. Proliferation kinetics did not provide any hint of midterm growth modulation effects of repetitive magnetic field exposure.

CONCLUSION: Repetitive magnetic field exposure does not exert any growth-modulating effect on overall cell growth and cell cycle distribution of cultured HFLFs. Midterm effects due to magnetic field exposure were not found.

Index terms: Magnetic resonance (MR), biological effects • Magnetic resonance (MR), experimental studies • Magnetic resonance (MR), safety • Radiobiology, cell and tissue studies


   Introduction
TOP
 Abstract
 Introduction
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
The use of higher field and gradient strengths and longer exposure times and the increasing probability of repetitive magnetic field exposure to the patient and medical staff during magnetic resonance (MR) imaging have raised concerns about a potential health hazard. Studies of side effects performed in the 1980s did not show any relevant change in the growth of different cell lines in culture or in the development of animals after MR imaging (1–6). However, in the past few years, findings of several published studies (7–17) indicate that there may well be effects on cell growth and fetal development. To our knowledge, no basic data exist about the possible growth-modulating effects of repetitive magnetic field exposure on human fetal cells.

Therefore, the aim of this study was to assess the possible effects of repetitive exposure to the static magnetic fields of three MR imaging units (0.2, 1.0, and 1.5 T) on the growth characteristics of human fetal lung fibroblasts (HFLFs).


   MATERIALS AND METHODS
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
HFLFs were obtained from the American Type Culture Collection, Rockville, Md. The reasons for using this cell type were the following: (a) HFLFs are commercially available. (b) HFLFs are well characterized by the ATCC. (c) Results of initial experiments have shown that HFLF growth can be modified by external stress (eg, radiation, antiproliferative agents such as paclitaxel) and that changes may be detected with the techniques used in the experiments. (d) HFLFs are human cells and, therefore, are probably more sensitive to external stress than are nonhuman cells.

Cultures were routinely grown in Dulbecco modified Eagle medium that was supplemented with 10% fetal calf serum, 2 mmol/L L-glutamine, and standard amounts of antibiotics. The culture medium was changed twice weekly, and the cells were subcultivated weekly to avoid confluence.

In the exposure-free periods, all cells were kept in the same air incubator (Haereus, Hanau, Germany) to provide identical environmental conditions (95% sterile filtered normal air and 5% carbon dioxide, 37.0°C ± 0.5°C, saturated atmosphere). To guarantee constant environmental growth conditions during magnetic field exposure, special Plexiglass exposure chambers were built. Those boxes were connected to a warm-water cycle so that the temperature within the boxes was constant in the range of 36.5°C–37.5°C. Furthermore, 300 mL of CO2 was insufflated into the boxes to prevent the culture medium and cells from becoming too alkalotic.

During the experiments, the exposure groups were placed into such a chamber that was positioned in the center of the magnetic field of the MR imaging unit. The control groups were put into a second chamber that was positioned outside the magnetic field in the control room. Temperature control was provided by the use of nonferromagnetic alcohol thermometers.

The effect of the magnetic field of three MR imaging units was examined. For the analysis of possible effects of a weak static magnetic field, the cells were placed into the static magnetic field of an 0.2-T MR imaging unit (Magnetom Open; Siemens, Erlangen, Germany). For the evaluation of high-field-strength effects, the cells were positioned in the magnetic bore of a 1.0- or 1.5-T MR imaging unit (Magnetom Expert or Vision; Siemens).

In experiment one, the effects of repetitive magnetic field exposure on the cell cycle distribution of nonsynchronized growing cells were examined. To analyze the cell cycle distribution of nonsynchronized growing cells, HFLFs were plated with a density of 2,000 cells per square centimeter in ventilated 25-cm2 tissue flasks (Falcon; Becton Dickinson, Franklin Lakes, NJ) in 5 mL of culture medium. Afterward, they were exposed for 1 h/d on days 2–6 after plating. Exposure and control groups were analyzed at 0, 12, 24, 36, and 48 hours after magnetic field exposure for possible cell cycle changes due to the repetitive magnetic field exposure.

In experiment two, the effects of repetitive magnetic field exposure on the cell cycle distribution of synchronized growing cells and their total proliferation were examined. To examine the cell cycle and proliferation kinetics of synchronized cells, 700,000 cells were plated in a 75-cm2 flask in 10 mL of culture medium. One day after plating, the culture medium was changed to remove possible stress particles. On days 2–6 after plating, the cells were exposed to the magnetic field for 1 h/d. On day 7 after plating, cells were harvested by trypsinization. The population doublings (PDs), parameters used to describe cell growth, were calculated. PDs describe the number of times a culture doubles within a certain period. PDs were calculated as follows: PD = [ln(no. of harvested cells) - ln(no. of subcultivated cells)]/ln 2.

Furthermore, cells were plated with a density of 8,000 cells per square centimeter in 25-cm2 flasks for cell cycle analysis at 24, 36, 48, 72, and 96 hours after plating. For cell cycle analysis, HFLFs were incubated with 10 µmol of bromodeoxyuridine (BrDu), a thymidine-analog, for 1 hour. Then, they were harvested by means of treatment with trypsin, washed with phosphate-buffered saline, and resuspended in 70% ethanol. Subsequently, they were stored at -20°C until further analysis.

In detail, the nuclei were isolated by means of membrane digestion with pepsin. For denaturation of the DNA, the nuclei were incubated in 2N hydrochloric acid then stained with a monoclonal mouse-antiBrDu antibody (Becton Dickinson) and a secondary fluorescein isothiocyanate–labeled rabbit-antimouse antibody (DAKO, Hamburg, Germany). In addition, total DNA was stained with the intercalating fluorochrome propidium iodide. Finally, possible double-stranded RNA was removed with a ribonuclease. The cells were analyzed with the use of a flow cytometer (FACSort; Becton Dickinson). Calculation of the different cell phases (G1, S, and G2–M) was performed with the program Cell Quest (Becton Dickinson).

Cells were plated for analysis of proliferation kinetics in the 21 days after subcultivation. Cells were subcultivated with a density of 30,000 cells in 5 mL of culture medium in 25-cm2 flasks. Absolute cell numbers were calculated on days 2, 4, 8, 12, 14, 16, 18, and 21 after plating with the use of an electronic cell counter (Casy; Schärfe Systems, Reutlingen, Germany).

The statistical calculations were performed by using SPSS (SPSS, Chicago, Ill). To detect differences between the exposure and control groups, the Wilcoxon rank sum (Mann-Whitney) test was performed. Differences with a P value of less than .05 were considered significant.


   RESULTS
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
Experiment One: Nonsynchronized Cells
The percentage of cells in the different cell cycle phases (G1, S, G2–M) varied with the time of measurement and between the exposure groups (Fig 1). Although differences were seen between the exposed and corresponding control groups, the differences were never significant. Depending on the phases the cells were in, within 48 hours, the percentage of cells in the G1 phase increased, and the percentages of cells in the S and G2–M phases decreased.



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  		Figure 1a. Graphs depict the cell cycle distribution of nonsynchronized cells after repetitive exposure to magnetic fields of (a) 0.2, (b) 1.0, and (c) 1.5 T at 0-48 hours after the last exposure. No statistically significant differences between the exposed and corresponding control groups were detected. Data are the mean ± SD. Phases of the exposed and control groups, respectively, are as follows: G1, and {bigcirc}; S, {block} and {square}; and G2, {blacktriangleup} and {triangleup}.

 


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  		Figure 1b. Graphs depict the cell cycle distribution of nonsynchronized cells after repetitive exposure to magnetic fields of (a) 0.2, (b) 1.0, and (c) 1.5 T at 0-48 hours after the last exposure. No statistically significant differences between the exposed and corresponding control groups were detected. Data are the mean ± SD. Phases of the exposed and control groups, respectively, are as follows: G1, and {bigcirc}; S, {block} and {square}; and G2, {blacktriangleup} and {triangleup}.

 


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  		Figure 1c. Graphs depict the cell cycle distribution of nonsynchronized cells after repetitive exposure to magnetic fields of (a) 0.2, (b) 1.0, and (c) 1.5 T at 0-48 hours after the last exposure. No statistically significant differences between the exposed and corresponding control groups were detected. Data are the mean ± SD. Phases of the exposed and control groups, respectively, are as follows: G1, and {bigcirc}; S, {block} and {square}; and G2, {blacktriangleup} and {triangleup}.

 
The differences between the 0.2- and 1.5-T groups and the 1.0-T groups may have had different causes: (a) The cells used in the 1.0-T experiments were more stressed during the subcultivating process and, therefore, reached their peak of cells in the S phase during the observation time; and/or, (b) the culture medium used in those experiments activated the cells less quickly than it did in other experiments, which is possible since the growth-stimulating effects of fetal calf serum and its growth factors vary from time to time.

Experiment Two: Synchronized Cells
PDs.—The values of the PDs ranged between 2.5 (0.2-T exposure group) and 3.2 (1.0-T control group) (Fig 2). Slight but nonsignificant differences (P < .05) between the PDs of the exposure and corresponding control groups were found. The 0.2-T exposure group had a PD of 2.5 ± 0.4 (mean ± SD), whereas the corresponding control group had a PD of 2.4 ± 0.2. The 1.0-T exposure group had a PD of 3.1 ± 0.4 after five 1-hour magnetic field exposures; the control group had a PD of 3.3 ± 0.4. Finally, the 1.5-T exposure group had a PD of 3.1 ± 0.1; the control group had a PD of 3.1 ± 0.2.



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  		Figure 2. Graph depicts the PDs after repetitive magnetic field exposure at 0.2, 1.0, and 1.5 T. No differences in the PDs of the exposed (MR) and control (Co) groups were found. Data are the mean ± SD.

 
Most probably, the differences between the mean PDs of the 0.2-T groups and the 1.0- and 1.5-T groups were due to (a) interresearcher variability and (b) a longer transfer time for the HFLFs from the air incubator to the exposure chambers, as the 0.2-T system was not located in the same area as the 1.0- and 1.5-T systems.

Cell cycle analysis.—The percentages of cells in the different phases varied with the time of measurement and between the different exposure groups (Fig 3). However, no significant difference in the phases of cells in the exposure and control groups for any one MR imaging unit was found at any time. In all groups, the percentage of cells in the S phase was maximal at 48 hours after subcultivation; results were as follows (exposure group vs control group): 0.2 T, 34.0% versus 33.0%; 1.0 T, 32.5% versus 32.8%; and 1.5 T, 29.5% versus 29.6%.



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  		Figure 3a. Graphs depict the cell cycle distribution of synchronized cells after repetitive exposure to magnetic fields of (a) 0.2, (b) 1.0, and (c) 1.5 T at 24-96 hours after subcultivation. No statistically significant differences between the exposed and corresponding control groups were found. Data are the mean ± SD. Phases of the exposed and control groups, respectively, are as follows: G1, and {bigcirc}; S, {block} and {square}; and G2, {blacktriangleup} and {triangleup}.

 


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  		Figure 3b. Graphs depict the cell cycle distribution of synchronized cells after repetitive exposure to magnetic fields of (a) 0.2, (b) 1.0, and (c) 1.5 T at 24-96 hours after subcultivation. No statistically significant differences between the exposed and corresponding control groups were found. Data are the mean ± SD. Phases of the exposed and control groups, respectively, are as follows: G1, and {bigcirc}; S, {block} and {square}; and G2, {blacktriangleup} and {triangleup}.

 


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  		Figure 3c. Graphs depict the cell cycle distribution of synchronized cells after repetitive exposure to magnetic fields of (a) 0.2, (b) 1.0, and (c) 1.5 T at 24-96 hours after subcultivation. No statistically significant differences between the exposed and corresponding control groups were found. Data are the mean ± SD. Phases of the exposed and control groups, respectively, are as follows: G1, and {bigcirc}; S, {block} and {square}; and G2, {blacktriangleup} and {triangleup}.

 
At the same time, the percentage of cells in the G1 phase was minimal, except in the 0.2-T control group. In that group, the minimal percentage of cells in the G1 phase was found at 36 hours after subcultivation (36 hours, 53.9%; 48 hours, 55.0%). The percentage of cells in the G2 phase peaked at 48 hours after subcultivation in the 0.2- and 1.0-T exposure groups and 1.0-T control group; the percentage was maximal at 36 hours after subcultivation in the 0.2-T control and 1.5-T exposure and control groups.

Proliferation kinetics.—In all groups, cell growth formed S-shaped curves on the line charts (Fig 4). In all groups (0.2-, 1.0-, and 1.5-T exposure and control groups), the period of maximal proliferation (log phase) was between days 4 and 12 after subcultivation. All groups reached their plateau level (peak value with no increase in cell numbers for the following two measurements) at day 16 after subcultivation. The peak values ranged between 1,517,000 cells ± 416,000 (27.4%) in a 25-cm2 flask for the 0.2-T control group and 1,754,000 cells ± 291,000 (16.6%) in the 1.0-T exposure group. However, neither the steepness of the growth curve during the log phase nor the absolute cell numbers at their peak levels differed significantly in the corresponding groups.



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  		Figure 4a. Graphs depict the proliferation kinetics of subcultured cells after repetitive exposure to magnetic fields of (a) 0.2, (b) 1.0, and (c) 1.5 T. During 21 days, no statistically significant differences between the exposed () and control ({bigcirc}) groups were found. Data are the mean ± SD.

 


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  		Figure 4b. Graphs depict the proliferation kinetics of subcultured cells after repetitive exposure to magnetic fields of (a) 0.2, (b) 1.0, and (c) 1.5 T. During 21 days, no statistically significant differences between the exposed () and control ({bigcirc}) groups were found. Data are the mean ± SD.

 


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  		Figure 4c. Graphs depict the proliferation kinetics of subcultured cells after repetitive exposure to magnetic fields of (a) 0.2, (b) 1.0, and (c) 1.5 T. During 21 days, no statistically significant differences between the exposed () and control ({bigcirc}) groups were found. Data are the mean ± SD.

 

   DISCUSSION
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
Since its introduction into diagnostic radiology about 15 years ago, the use of MR imaging has increased tremendously. However, with increasing MR imaging exposure to patients and staff and with the wish to perform MR imaging examinations in pregnant women, concerns arose about possible biologic effects of magnetic field exposure. Obviously, there is a lack of information about the effect of repetitive magnetic field exposure on biologic systems and on fetal growth. The results of studies of side effects are contradictory.

Wolff et al (1) described the effects of static magnetic fields (0.35 T), pulsed gradient fields, and radio-frequency emissions on Chinese hamster ovarian cells. They focused their work on possible chromosomal aberrations and sister chromatid exchange that they could not detect. One year later, Cooke and Morris (2) exposed human lymphocytes to static magnetic fields of different strengths (0.5 and 1.0 T). They did not find chromatid lesions or chromatid exchanges after magnetic field exposure. Geard et al (3) exposed mouse C3H 10T1/2 cells for up to 17 hours to static magnetic fields (of up to 2.7 T) with pulsed gradient fields and radio-frequency emissions. They could detect neither chromosomal aberrations nor sister chromatid exchange.

In 1985, Wolff et al (4) presented findings from another study that showed no cytogenetic damage due to magnetic field exposure (2.35 T) and radio-frequency emissions (100 MHz) in unstimulated and stimulated lymphocytes and in Chinese hamster ovarian cells. Prasad et al (5) examined the influence of 2.35-T magnetic field exposure on the cytotoxic effects of natural killer cells with and without interleukin 2 stimulation. They concluded that high-field-strength imaging conditions had no adverse influence on the cytotoxic effects of natural killer cells. Mahdi et al (6) exposed different strains of Escherichia coli to a static magnetic field of 0.5 or 3.0 T and to time-varying magnetic fields. They did not detect any increase in DNA damage during static or time-varying magnetic field exposure.

On the contrary, findings from several studies indicate the effects of magnetic field exposure on cell growth in culture and even on the fetal development of mice. Malinin et al (7) described a growth inhibiting effect of a 0.5-T magnetic field (4–8 hours at 4.2 K) on human WI-38 fibroblasts and murine L-929 cells. Norimura et al (8) described growth inhibition of phytohemagglutinin-stimulated T lymphocytes due to strong magnetic field exposure, depending on the field strength (up to 6.3 T) and exposure time (up to 60 hours). Furthermore, they detected an increase in the radiosensitivity of T cells exposed to a static magnetic field (6.3 T for 24 hours) before x-ray exposure.

McDonald (9) found an increase in the turnover and synthesis rate of fibroblasts derived from neonatal rat calvaria due to long-term (up to 10 days) magnetic field exposure (0.6 T). On the contrary, however, stimulation of osteoblasts did not occur. Raylman et al (10) described a substantial reduction in the total number of viable cells in cultures of melanoma, ovarian carcinoma, and lymphoma cells after exposure to a 7.0-T static magnetic field for 64 hours. Hiraoka et al (11) reported an increase in the expression of the c-fos oncogene in cultured HeLAS3 cells after exposure to a static magnetic field of 0.2 T for 2–24 hours compared with control cells. However, changes in c-myc and c-N-ras gene expression could not be detected.

Tyndall and Sulik (12) reported an increase in eye malformations in fetal C57BL/6J mice due to MR imaging exposure (spin-echo T2-weighted sequence; 1.5 T; radio frequency, 64 MHz) of the dams on gestational day 7 for 36 minutes. In another study, Tyndall (13) reported a reduced crown-rump length in fetal C57BL/6J mice after 1.5-T MR exposure. Carnes and Magin (14) observed a reduction in fetal weight and daily sperm production in adult mice after fetal exposure to 4.7-T MR imaging for 8 hours. Espinar et al (15) found that the development of the cerebellum of chick embryos may be irreversibly altered with continuous exposure to a static magnetic field of 20 mT. Findings in further studies (16,17) indicate cell cycle–modulating effects of magnetic field exposure in cultured cells.

In our study, we tried to determine whether repetitive exposure to a static magnetic field exerts cell cycle and, therefore, growth-modulating effects on HFLFs, depending on the magnetic field strength (0.2, 1.0, and 1.5 T). However, at no time did we find any statistically significant difference in the cell cycle distribution of the exposed cells compared with the control groups. Small yet nonsignificant differences are likely to be related to intra- and interresearcher differences in cell analysis. The strength of the magnetic field applied to the cells did not seem to play a role between 0.2 and 1.5 T.

In addition, we analyzed the proliferation kinetics of the exposed cells because possible effects due to magnetic field exposure may become important when the cells become older and more differentiated. However, during a follow-up period of 21 days after magnetic field exposure, we did not find any difference in the exposure groups compared with the control groups. The period of maximal growth and the level of the plateau phase were not affected by magnetic field exposure.

On the basis of our results, we conclude that repetitive magnetic field exposure (five 1-hour exposures at 0.2–1.5 T) does not exert relevant growth-modulating effects on cultured HFLFs.

Practical application: Although in vitro experiments can never be a substitute for conscientious clinical examinations, in vitro systems are successfully used for initial screening in many disciplines (eg, pharmacology, molecular biology). With an increase in the magnetic field strengths of new MR imaging units (up to 8 T) and with a broadening of the spectrum of indications for MR imaging (eg, dynamic, fetal, and interventional MR imaging), safety studies that address the changed parameters (eg, higher field strength, fetal exposure, repetitive exposure) are necessary. The negative results of our in vitro study do not rule out a possible health risk because of (a) the variety of cell types that form the human body; (b) the fact that many cell types interact in vivo, whereas cell interaction cannot be examined in a monolayer model of one cell type; and (c) the fact that an in vitro model can be used to examine only single aspects of the in vivo situation. However, our results can be used as basic data for further safety studies, as well as for the development of screening systems for possible toxic reactions to MR imaging.


   Footnotes
 
Abbreviations: BrDu = bromodeoxyuridine, HFLF = human fetal lung fibroblast, PD = population doubling

Author contributions: Guarantor of integrity of entire study, J.W.; study concepts, S.H.D., C.D.C.; study design, J.W., S.H.D., H.P.R.; definition of intellectual content, J.W.; literature research, E.F.G., E.R.; experimental studies, J.W., E.F.G., F.H., R.K.; data acquisition, E.F.G., F.H.; data analysis, J.W., F.H., M.W.; statistical analysis, F.H., M.W.; manuscript preparation, J.W.; manuscript editing, H.P.R., C.D.C., E.R.; manuscript review, H.P.R., C.D.C., S.H.D.


   References
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

  1. Wolff S, Crooks LE, Brown P, Howard R, Painter RB. Test for DNA and chromosomal damage induced by nuclear magnetic resonance imaging. Radiology 1980; 136:707-710.[Abstract/Free Full Text]
  2. Cooke P, Morris PG. The effects of NMR exposure on living organisms. II. A genetic study of human lymphocytes. Br J Radiol 1981; 54:622-625.[Abstract/Free Full Text]
  3. Geard CR, Osmak RS, Hall EJ, Simon HE, Maudsley AA, Hilal SK. Magnetic resonance and ionizing radiation: a comparative evaluation in vitro of oncogenic and genotoxic potential. Radiology 1984; 152:199-202.[Abstract/Free Full Text]
  4. Wolff S, James TL, Young GB, Margulis AR, Bodycote J, Afzal V. Magnetic resonance imaging: absence of in vitro cytogenic damage. Radiology 1985; 155:163-165.[Abstract/Free Full Text]
  5. Prasad N, Lotzava E, Thornby JI, Taber KH. The effects of 2.35-T MR imaging on natural killer cell cytotoxicity with and without interleukin-2. Radiology 1990; 175:261-263.[Abstract/Free Full Text]
  6. Mahdi A, Gowland PA, Mansfield P, Coupland RE, Lloyd RG. The effects of static 3.0 T and 0.5 T magnetic fields and the echo-planar imaging experiment at 0.5 T on E coli. Br J Radiol 1994; 67:983-987.[Abstract/Free Full Text]
  7. Malinin GI, Gregory WD, Morelli L, Sharma VK, Houck JC. Evidence of morphological and physiological transformation of mammalian cells by strong magnetic fields. Science 1976; 194:844-846.[Abstract/Free Full Text]
  8. Norimura T, Imada H, Kunugita N. Effects of strong magnetic fields on cell growth and radiation response of human T-lymphocytes in culture. Sangyo Ika Daigaku Zasshi 1993; 15:103-112.
  9. McDonald F. Effect of static magnetic fields on osteoblasts and fibroblasts in vitro. Bioelectromagnetics 1993; 14:187-196.[Medline]
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