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(Radiology. 1999;213:860-865.)
© RSNA, 1999

Experimental Studies

Survival of Mammalian Cells Exposed to Ultrahigh Dose Rates from a Laser-produced Plasma X-ray Source1

Carl Tillman, PhD, Gustav Grafström, MSc, Ann-Charlotte Jonsson, MSc, Bo-Anders Jönsson, PhD, Ian Mercer, PhD 2, Sören Mattsson, PhD, Sven-Erik Strand, PhD and Sune Svanberg, PhD

1 From the Division of Atomic Physics, Lund Institute of Technology, Sweden (C.T., I.M., S.S.); the Department of Radiation Physics, Jubileum Institute, Lund University Hospital, SE-221 85 Lund, Sweden (G.G., A.C.J., B.A.J., S.E.S.); and the Department of Radiation Physics, University Hospital Malmo, Sweden (S.M.). Received June 18, 1998; revision requested July 21; revision received March 10, 1999; accepted July 1. Supported in part by the Swedish Medical Research Council, the Swedish Natural Sciences Research Council, Mrs Berta Kamprad's Cancer Foundation, and Gunnar, Arvid, and Elisabeth Nilsson's Foundation. Address reprint requests to B.A.J.


   Abstract
TOP
 Abstract
Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
PURPOSE: To determine whether intense laser-produced x rays have an increased radiation hazard.

MATERIALS AND METHODS: Mammalian cells were exposed to x rays from a laser-produced plasma that produced ultrahigh peak absorbed dose rates, up to a factor of 1010 higher than those produced by conventional x rays used in imaging. The cell survival was studied as a function of the absorbed dose. The survival of mammalian cells exposed to high peak absorbed dose rates with laser-produced x rays was compared with the survival of cells exposed to standard absorbed dose rates with conventional x-ray sources. Comparative survival studies were performed by using a conventional x-ray tube and a cobalt 60 source. The absorbed doses in the irradiation field were measured with thermoluminescent dosimeters.

RESULTS: Cell survival following irradiation by filtered, laser-produced x rays with a high dose rate was not markedly different from the survival following irradiation by conventional sources. There was, however, a notable difference between the survival after exposure to filtered, laser-produced x rays and the survival after exposure to unfiltered laser-produced x rays.

CONCLUSION: Exposure to filtered, laser-produced x rays with a high dose rate does not lead to increased harm to mammalian cells exposed in vitro compared with the harm from exposure to x rays from conventional sources, which indicates that the use of high-power laser facilities for medical imaging is justified.

Index terms: Dosimetry, **.113 • Lasers • Radiations, injurious effects, **.47 • Radiations, measurement, **.11 • Radiobiology, cell and tissue studies, **.47 • Radiography, **.11


   Introduction
TOP
 Abstract
 Introduction
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
The use of x rays in diagnostic radiology is generally considered to give acceptably low absorbed doses to the patient. However, there is always a risk of cell damage, even in the regime of low absorbed doses (1). Novel, extremely intense x-ray sources, based on laser-produced plasmas, are presently being investigated in laboratory studies (2). X rays of sufficiently high photon energies for medical imaging can be produced by focusing ultrashort pulses of radiation from high-power lasers onto a high-atomic-number material. This is a multiphoton process, which is strongly dependent on the intensity of the laser irradiation. The laser pulse duration is typically a fraction of a picosecond, and the x-ray emission, shown to have components up to 1 MeV (3), occurs on the order of a few picoseconds (measured at photon energies below 10 keV) (4).

We have recently demonstrated that such radiation can be used for magnification radiography and for single-pulse imaging of small biologic objects (2). Differential elemental imaging can be performed with laser-produced x rays by changing the target material (5) in a way similar to that demonstrated with monochromatic synchrotron radiation (6).

The use of ultrashort x-ray bursts from a laser-based source in combination with time-gated viewing can reduce the contribution of scattered x rays in the image in a way similar to what is well investigated in the optical domain (7,8). Before this technique can be introduced for medical imaging of humans, it must be shown that the absorbed dose with ultrahigh dose rates does not produce greater biologic effects than the same absorbed dose from a conventional x-ray source.

It is normally assumed that there is no dose-rate effect beyond an absorbed dose rate of 1 Gy/min, since the mechanism of the dose-rate effect is the repair of sublethal damage, with a half-life of about 1 hour. If the radiation exposure time is short compared with the repair half-life, there is no opportunity for sublethal damage to occur (9).

At ultrahigh dose rates of about 1010 Gy/min, the level of oxygen may be depleted, which leads to increased survival. When oxygen is present, it reacts with radiation-induced free radicals to cause irreparable biologic damage (9). A report (10) on ultrahigh dose-rate effects from the late 1960s indicated abnormally high cell survival at high absorbed doses and ultrahigh absorbed dose rates, that is, over 4 x 1010 Gy/min. A correlation between ultrahigh dose rate and oxygen depletion was demonstrated in a study (11) in which various oxygen concentrations were employed. It was shown that the slope, or D0 value, of all the survival curves was initially the same but changed to a slope typical for anaerobic conditions after a certain threshold dose. This study was performed with a radiosensitive bacterium, with threshold doses in the range of 10–40 Gy and a dose rate of 2 x 1010 Gy/min. In mammalian cells, the sensitive sites may be protected from free diffusion of oxygen, which allows even relatively small absorbed doses delivered at exceedingly high dose rates to exhaust local oxygen supplies (10).

In studies of chromosome aberrations in human lymphocytes, no increase in damage was found when the absorbed dose was delivered in a single microsecond pulse with a dose rate of 3 x 108 Gy/min compared to an absorbed dose rate of 1 Gy/min of 15-MeV electrons (12). However, when the absorbed dose rate reached 2.7 x 1010 Gy/min, a decrease in chromosomal aberration in human lymphocytes was observed (13).

The absorbed dose rate in the present study is similar to that reported by Berry et al (10), although the average photon energy employed in the present study was much lower. This difference in photon energy and the possibility of obtaining higher absorbed dose rates with laser-based x-ray sources in the near future are the main reasons for studying the survival of mammalian cells exposed to such irradiation.

Methodological difficulties in measuring the absorbed dose may be expected and were encountered in this investigation, as the response of dosimeters to short-pulse, intense radiation is not well known. However, it has been reported that the response of thermoluminescent dosimeters (TLDs) is linear with the x-ray absorbed dose from laser-produced plasmas (14).

The purpose of this study was to provide data on cell damage following irradiation with high dose rates, as assessed with the survival of mammalian cells. The reason for raising the question of whether the biologic effects are greater for the absorbed dose from laser-produced x rays than they are for the same absorbed dose from conventional x-ray tubes is that the peak absorbed dose rate is typically 1010 times higher with laser-produced x rays. It is known that the biologic effect of x rays is due mainly to the indirect action of free radicals close to DNA molecules, which cause the breaking of bonds. The question is whether the damage to cells will be greater due to the extremely high absorbed dose rate, that is, 1011 Gy/min in the picosecond pulses of x rays, than it is with conventional diagnostic x rays.


   MATERIALS AND METHODS
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
Laser-based X-ray Source
Laser pulses, with a peak power of about 1012 W, are provided at a repetition rate of 10 Hz by a terawatt laser system (15). A high-density plasma is created when these pulses are focused on a metal target at an air pressure of about 20 mbar (2 kPa) (Fig 1). The laser pulses, with a duration of 135 fsec, a pulse energy of 150 mJ, and a diameter of 50 mm, were focused down to an ultrasmall spot of a few micrometers diameter. The spot diameter was measured at a low laser intensity and was found to be 3 µm. The laser intensity reached 1017 W · cm-2.



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  		Figure 1. Diagram shows the high-power laser equipment. A pulsed laser beam is focused by a parabolic mirror onto a rotating target. The extremely high-power intensity of the focal spot creates a plasma from which x rays are emitted.

 
A tantalum target foil, positioned in the focal spot, was rapidly heated and ionized by the focused laser radiation. Radiation was emitted within a spectrum from visible light to high-energy x rays. Characteristic features of this x-ray source are both the ultrashort pulse duration, which is on the order of a few picoseconds at photon energies below 10 keV (4), and a spatial extent of less than 60 µm, which allows the recording of images with a high degree of magnification (2).

Preparation and Analysis of Cell Samples
V79 Chinese hamster lung fibroblast cells (cell line V79-CH) were cultured in a controlled humidified environment (95% air and 5% CO2 at 37°C) and in complete growth medium (Dulbecco's Modified Eagle's Medium; Gibco, Life Technologies, Paisley, Scotland) supplemented with 10% fetal bovine serum (Gibco), 2% L-glutamine (Gibco), and 1% penicillin–streptomycin–amphotericin B (Gibco). The cells grew in a monolayer, with a doubling time of 9 hours.

Cells in exponential growth were loosened by means of exposure to trypsin, and cell concentration was determined with a hemocytometer; 2 x 105 cells were transferred to 600-µL tubes, and complete growth medium was added to produce a final volume of 400 µL. The cells were centrifuged to form a pellet and were transported to the irradiation laboratory. After irradiation, the cells were resuspended by mixing with a vortex mixer, they were diluted, and they were seeded in petri dishes containing 5 mL of complete growth medium for colony growth. At least five dishes were seeded for each irradiated cell sample (16).

The cell survival as a function of the absorbed dose was evaluated. The data from the five dishes from each cell sample were averaged to give one data point, with the SD within the group as a measure of the uncertainty in cell survival. An exponential regression curve was fitted to each series of inverted variance-weighted data points. The assumed equation for the curve was ln(S) = {alpha}D + ßD2, where S is the relative cell survival, D is the absorbed dose, and {alpha} and ß are constants.

Preparation and Readout of TLDs
TLDs of lithium fluoride doped with magnesium and titanium (Harshaw TLD 100; Bicron, Solon, Ohio) were used to determine the absorbed dose to the cells. Microrods 1 mm in diameter and 6 mm long were used. The signals from the TLDs were read in a Pitman 654 Toledo TLD reader (Pitman, Weybridge, England). The TLDs were preheated for 35 seconds at 135°C; this was followed by readouts during 30 seconds at a temperature elevation rate of 25°C · sec-1 to a temperature of 270°C in a nitrogen atmosphere. The TLDs were annealed for 15 minutes at 400°C after readout, which allowed them to be reused.

The TLDs were recalibrated prior to each irradiation experiment. Calibration was performed by using a cobalt 60 source to repeatedly irradiate with 1.6 Gy at 0.5 Gy/min at a distance of 80 cm. The uncertainty in the absorbed dose with these dosimeters was less than 2%. The dosimeter signal has been shown to be independent of the absorbed dose rate up to 6 x 1010 Gy/min (17). The supralinear characteristics of the TLDs were determined by means of irradiation with absorbed doses of up to 35 Gy. The relative energy response {epsilon}rel(E) to photons with energies different from that of 60Co (mean, 1.25 MeV) was calculated by using the relation

where µen is the mass energy-absorption coefficient and {rho} is the mass density. The mass energy-absorption coefficient for cells was assumed to be equal to the mass energy-absorption coefficient of water. The relative energy response has a maximum of 1.3–1.4 for photon energies of 20–30 keV.

Exposure with the Laser-produced Plasma
Cell samples and TLDs were prepared and treated at the Department of Radiation Physics, Lund University Hospital, Sweden, and were then transported to the High-Power Laser Facility, Department of Physics, Lund University, Sweden, for irradiation (15). All samples were irradiated in small, sealed, plastic test tubes with a wall thickness of 0.7 mm. These tubes were mounted in a Lucite holder (Fig 2, A). TLDs were also mounted in similar plastic tubes in another Lucite holder (Fig 2, A). The two Lucite holders, which contained samples and detectors, were then mounted in the experimental chamber as illustrated in Figure 2, part B. The distance from the laser-based x-ray source to the samples and detectors was varied from 110 to 130 mm.



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  		Figure 2. A, Diagram shows test tubes containing a cylindric TLD and a cell pellet. Medium = cell growth medium. B, Diagram shows irradiation geometry. Cell samples and TLDs in test tubes are arranged in two rows in Lucite holders. Every cell sample is assigned to a corresponding TLD, with a distance of 5 mm in between the cell sample and TLD.

 
Exposure was carried out on several occasions. A series of five to seven cell samples with corresponding TLDs were exposed on each occasion. An additional cell sample, kept under similar conditions but not irradiated, was used as a reference. Fluctuations in the emission of x rays led to variation in the absorbed dose rate on the different exposure occasions. The effect of angular inhomogeneities in the emission were minimized by placing the cells and TLDs close together and by interpolating the signals between the separate TLDs. The aim was to expose the cells in each series to absorbed doses between 1 and 15 Gy. Each cell sample was assigned a TLD. Different exposure times were used to achieve the desired absorbed doses. To ensure that other environmental conditions (eg, temperature and pressure) were the same, all samples were kept in a lead container inside the experimental chamber when they were not exposed.

Exposure was performed with two laser plasma x-ray qualities: unfiltered radiation and radiation filtered with 0.15-mm copper (Fig 3). The weighted relative TLD response rel for a photon energy distribution at the TLD {phi}(E) and the energy-dependent TLD response {epsilon}rel(E) (see Eq [1]) were calculated as rel = [{int}{epsilon}rel(E){phi}(E)EdE]/[{int}{phi}(E)EdE]. Compared with the 60Co photon energy response, the weighted relative energy responses of the TLDs were calculated to be 1.20 for unfiltered radiation and 1.12 for radiation filtered with 0.15-mm copper. Half-value layers (HVLs), mean photon energies, TLD responses, and absorbed dose rates are summarized in Table 1.



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  		Figure 3. Graph demonstrates the energy distributions of x rays from the laser-based source. The distribution of the unfiltered radiation was calculated from a pulse-height distribution recorded with a Compton spectrometer (18). The distribution of the radiation filtered with 0.15-mm copper was estimated from the unfiltered energy distribution by taking the attenuation in the filter into account.

 

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  		TABLE 1. HVLs, Mean Photon Energies, TLD Responses, and Absorbed Dose Rates for Five X-ray Sources
 
Exposures with Conventional Radiation Sources
Irradiation of cell samples and TLDs was also performed with a mammographic x-ray tube operated at 25 kVp, a therapeutic x-ray tube operated at 250 kVp and a 60Co source at 1.17 and 1.33 MeV. The 250-kVp and 60Co exposures were performed in a water tank at a depth of 3.6 cm, while the 25-kVp exposure was performed in air. The irradiation procedure and the geometry, apart from the distance to the source, were the same as those for the laser-based experiments. Two series with four to six cell samples in each were exposed by each source. The same correction factors as those used in patient monitoring were used for the energy-response correction of the TLD measurements for cell sample irradiation with conventional x-ray tubes. Characteristic data for the x-ray sources are summarized in Table 1.


   RESULTS
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
Dose Measurements with TLDs
There was no indication that the response of the TLDs to intense, short, x-ray pulses differed from the response to x-ray sources with low absorbed dose rates. Absorbed doses were measured at distances of 10–300 cm from the laser-based x-ray source, at dose rates up to 1.1 x 1011 Gy/min (mean dose rate, 13.2 x 103 pulses). It was found that the absorbed doses followed an inverse squared-distance relation, which demonstrated that the influence of the absorbed dose rate was negligible.

The peak absorbed dose rate from the exposure with the laser-based source and the high absorbed dose rate were averaged for each series, with the assumption of an x-ray pulse duration of 2 psec. The averaged peak absorbed dose rate was 1.1 x 1011 Gy/min for unfiltered radiation (range, 0.2 x 1011 to 2.0 x 1011 Gy/min on different experimental occasions), and the averaged peak absorbed dose rate for filtered radiation was 3.4 x 1010 Gy/min (range, 1.2 x 1010 to 4.0 x 1010 Gy/min). These absorbed dose rates represent a mean of all the x-ray pulses detected by the TLDs, whereas the intensity of the individual x-ray pulses varies with up to one order of magnitude, as indicated by the asymmetric error bars. The pulse duration was not measured directly at these relatively high photon energies but was estimated from measurements at lower photon energies under similar conditions (4). The absorbed dose rate for the conventional sources varied from 0.6 to 6.3 Gy/min.

Cell Survival as a Function of Absorbed Dose
The survival of the irradiated cells is presented in Figure 4. The absorbed doses required to reduce the mean survival to 37% are presented in Table 2. Although difficulties were encountered in obtaining similar experimental conditions from one occasion to the next, the survival curves, based on results of several independent experiments, show a substantial difference in the absorbed doses required to reduce the mean survival to 37% between filtered and unfiltered laser-produced x rays (Fig 4, A). This may be explained by the presence of ultraviolet radiation in the unfiltered beam.



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  		Figure 4. Graphs show the relative cell survival as a function of the absorbed dose. A, X rays generated from laser-produced plasma without a filter ({square}) and with a 0.15-mm copper filter ({block}). B, X rays generated from laser-produced plasma with a filter ({block}) and with the x-ray tube operated at 25 kVp ({square}). C, X rays generated from laser-produced plasma with a filter ({block}) and with the x-ray tube operated at 250 kVp ({square}). D, X rays generated from laser-produced plasma with a filter ({block}) and with the 60Co source ({square}). The relative cell survival was normalized to 100% for unexposed cells. An exponential regression curve was fitted to each series of inverted variance-weighted data points. The solid line is the fit to the filled squares, and the dashed line is the fit to the open squares.

 

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  		TABLE 2. Absorbed Doses at which the Relative Cell Survival Was 37%
 
The laser-based x-ray source is sensitive to a number of laser parameters that cannot be fully controlled. The energy dependence of the TLDs was calculated by using Equation (1). For low-energy photons, this is a simplification, as the attenuation within the TLDs is not negligible. The biologic effect scaled according to the absorbed dose is based on the assumption that there are no differences in secondary electron spectra produced by x rays or {gamma} rays. When comparing the filtered, laser-produced x rays with the conventionally produced x rays, no differences in survival were observed (Fig 4, B–D). On the basis of the results obtained here, it would be interesting to carry out more thorough investigations that would include some of the parameters mentioned above.

Findings of an earlier study (11) in which so-called Blumlein generators, capable of delivering 7-nsec pulses of 2-MV x rays, were used have shown a cell survival that differs from the normal case. It was observed in that study that above a critical absorbed dose rate of ~4 x 1010 Gy/min, the slope of the cell survival as a function of the absorbed dose became less steep. The phenomenon could not be duplicated with 50-nsec x-ray pulses in the same study, where the peak absorbed dose rate was below the critical value. The samples were exposed for constant times but at different distances from the x-ray source.

The investigation of cell survival presented here was carried out with peak absorbed dose rates above the reported critical absorbed dose rate. The number of data points above the critical limit was not sufficient to unequivocally demonstrate differences in survival. However, when the results presented in Figure 4, part A were divided into different subseries according to the date of the exposures, one of these subseries showed the same effect as that reported by Berry et al (10). The slope of cell survival changed at a dose of 5.4 Gy.


   DISCUSSION
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
In the present investigation, mammalian cell samples were irradiated with x-ray bursts from a laser-produced plasma at an ultrahigh dose rate (~1011 Gy/min) and with a mean photon energy above 10 keV. The results show no differences in survival after irradiation with filtered (0.15-mm Cu) laser-produced x rays versus conventional sources at moderate absorbed dose rates (<6 Gy/min). There is a substantial difference in cell survival between filtered and unfiltered laser-produced radiation. An explanation of this may be the presence of ultraviolet radiation in the unfiltered beam, but this should be further investigated. The purpose of the experiment, however, was to study possible harmful effects associated with the use of high-power laser facilities in radiology. According to the results obtained in this study, there is no increased hazard associated with the use of intense, laser-produced x rays in medical imaging compared with the use of conventional x-ray tubes.Practical applications: Laser-produced x rays have a potential for lowering the dose with suppression of scattered radiation and can provide magnification and differential radiography, that is, time-gated imaging (8). The present study findings show that these potential advantages will not be eliminated by an increased radiation hazard associated with ultrahigh dose rates. Thus, a basis for continued efforts in the development of compact, laser-produced x-ray sources for medical applications has been established.


   Acknowledgments
 
The authors thank Matthias Grätz, PhD, and Claes-Göran Wahlström, PhD, for helpful assistance and valuable discussions.


   Footnotes
 
2 Current address: Lawrence Livermore National Laboratory, Livermore, Calif. Back

**. Multiple body systems Back

Abbreviations: HVL = half-value layer TLD = thermoluminescent dosimeter

Author contributions: Guarantor of integrity of entire study, S.S.; study concepts, B.A.J., S.M., S.E.S., S.S.; study design, C.T., G.G., B.A.J., I.M., S.M., S.E.S.; definition of intellectual content, G.G., A.C.J., B.A.J., I.M., S.M., S.E.S., S.S.; literature research, C.T., G.G., A.C.J., B.A.J.; experimental studies, C.T., A.C.J.; data acquisition, C.T., G.G., A.C.J., I.M.; data analysis, C.T., G.G., A.C.J., B.A.J., S.M., S.E.S.; manuscript preparation, C.T., G.G., A.C.J., B.A.J.; manuscript editing, G.G., B.A.J., S.E.S., S.S.; manuscript review, all authors.


   References
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

  1. The International Commission on Radiological Protection. Radiological protection in biomedical research ICRP publication no. 62. Oxford, England: Pergamon Press, 1992.
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  3. Kmetec JD, Gordon IIICL, Macklin JJ, Lemoff LE, Brown GS, Harris SE. MeV x-ray generation with a femtosecond laser. Phys Rev Lett 1992; 68:1527-1530.[Medline]
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  5. Tillman C, Mercer I, Svanberg S, Herrlin K. Elemental biological imaging by differential absorption with a laser-produced plasma x-ray source. J Opt Soc Am [B] 1996; 13:209-215.
  6. Dix WR. Intravenous coronary angiography with synchrotron radiation. Prog Biophys Mol Biol 1995; 63:159-191.[Medline]
  7. Gordon CL, III, Yin GY, Lemoff BE, Bell PM, Barty CPJ. Time-gated imaging with an ultrashort-pulse, laser-produced plasma x-ray source. Optics Letters 1995; 20:1056-1058.
  8. Grätz M, Pifferi A, Wahlström CG, Svanberg S. Time-gated imaging in radiology: theoretical and experimental studies. IEEE J Selected Top Quantum Electronics 1996; 2:1041-1048.
  9. Hall EJ. Radiation damage and the dose-rate effect In: Radiobiology for the radiologist. 3rd ed. Philadelphia, Pa: Lippincott, 1988; 125.
  10. Berry RJ, Hall EJ, Forster DW, Storr TH, Goodman MJ. Survival of mammalian cells exposed to X-rays at ultra-high dose-rates. Br J Radiol 1969; 42:102-107.[Medline]
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  12. Purrot RJ, Reeder EJ. Chromosome aberration yields induced in human lymphocytes by 15 MeV electrons given at a conventional dose-rate and in microsecond pulses. Int J Radiat Biol 1977; 31:251-256.
  13. Prempree T, Michelsen A, Merz T. The repair time of chromosome breaks induced by pulsed x-rays of ultra-high dose rate. Int J Radiat Biol 1969; 15:571-574.
  14. Schnürer M, Kalashnikov MP, Nickles PV, et al. Hard x-ray emission from intense short pulse laser plasmas. Phys Plasmas 1995; 2:3106-3110.
  15. Svanberg S, Larsson J, Persson A, Wahlström CG. Lund high-power laser facility systems and first results. Phys Scripta 1994; 49:187-197.
  16. Jonsson AC, Jönsson BA, Strand SE, Grafström G, Spanne P. Cell survival after Auger electron emission from stable intracellular indium exposed to monochromatic synchrotron radiation. Acta Oncol 1996; 35:947-952.[Medline]
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  18. Tillman C, Johansson SÅ, Erlandsson B, et al. High resolution spectroscopy of laser-produced plasmas in the photon energy range above 10 keV. Nucl Instruments Methods Phys Res [A] 1997; 394:387-396.



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