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Radiation Dose to Organs and Tissues from Mammography: Monte Carlo and Phantom Study¹

¹ From the Department of Radiology and Winship Cancer Institute, Emory University School of Medicine, Atlanta, Ga (I.S., S.S., S.V., C.J.D., A.K.); and Wallace H. Coulter Department of Biomedical Engineering, Georgia Institute of Technology, Atlanta, Ga (I.S., A.K.). Received February 6, 2007; revision requested April 11; revision received April 26; accepted May 29; final version accepted July 9. Supported in part by National Institutes of Health grant RO1-EB004015 from the National Institute of Biomedical Imaging and Bioengineering. Supported by a grant from the Georgia Cancer Coalition. Address correspondence to A.K., Department of Radiology, University of Massachusetts Medical School, 55 Lake Avenue North S2-836, Worcester, MA 01655 (e-mail: Andrew.Karellas{at}umassmed.edu).

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION ADVANCES IN KNOWLEDGE IMPLICATIONS FOR PATIENT CARE... References

 
Purpose: To prospectively determine the radiation dose to the organs of the body during standard bilateral two-view mammography by using Monte Carlo simulations and a phantom.

Materials and Methods: A modified version of the Cristy mathematic anthropomorphic phantom was implemented in the Geant4 Monte Carlo tool kit to simulate the conditions present in screen-film and digital mammography. The breast was simulated with compression in both the craniocaudal and the mediolateral oblique views. X-rays were tracked from the source until their absorption in the body or in the detector or their exit from the simulation limits, with recording of all the intermediate interactions in the body. The simulation was performed with x-rays of energy ranging from 6 to 35 keV to obtain results for clinically relevant spectra. The ratio of dose to an organ in the body per unit glandular dose to the breast, denoted the relative organ dose (ROD), was computed. The effect of using a body protective shield was also investigated.

Results: The organs that received an ROD of 0.10% or higher in at least one view and one spectrum were the contralateral breast, ipsilateral eye and eye lens, heart, ipsilateral lung, and thymus. Among the organs, the maximum ROD was 0.62%. The maximum ROD for the bone surfaces was 2.36% and that for the red bone marrow was 0.56%. The highest ROD measured for the uterus or fetus at the first trimester was less than 10^–5.

Conclusion: The radiation dose to all tissues other than the breast is extremely low. The dose to the first-trimester fetus is minimal.

© RSNA, 2007

	INTRODUCTION

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Although the radiation dose to the imaged breast during a standard mammographic acquisition is well known (1–8), the dose received by the other organs and tissues of the body from a mammographic procedure are not as well known. Data about organ dose during mammographic acquisition will help the study of issues relating to the safety of mammography performed during pregnancy (9) and the epidemiologic study of radiation-related onset of specific diseases (10). In more practical terms, radiologists have adequate data to communicate the radiation dose delivered to the breast during mammography, but no detailed data are available about radiation dose to other tissues as a result of this procedure. This information is important for patients who are not aware that they are pregnant at the time of the procedure and for pregnant women who are suspected of having breast abnormalities that may warrant mammography. To our knowledge, only one study (11) has been published about the radiation dose to the other organs of the human body from a mammographic procedure. In that study, performed by using a phantom and thermoluminescence dosimetry, investigators reported the measured dose in a limited number of organs and tissues. Thus, the purpose of our study was to prospectively determine the radiation dose to the organs of the body during standard bilateral two-view mammography by using Monte Carlo simulations and a phantom.

	MATERIALS AND METHODS

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With the use of the Geant4 tool kit (12,13) for Monte Carlo simulations, a C++ computer program was implemented by one of the authors (I.S.) to simulate the acquisition of a standard two-view bilateral mammogram. The simulation included a representation of the human body that was based on the current version of the Cristy phantom (14), developed by Cristy (15) at the Oak Ridge National Laboratory, Oak Ridge, Tenn. In addition to the anthropomorphic phantom, the simulation included an x-ray point source as an approximation of the focal spot of the mammographic x-ray tube, the breast compression plate, the breast support plate, and the x-ray detector with cover plate.

Anthropomorphic Phantom
The Cristy phantom consists of a representation of the human body and its organs with the use of geometric shapes that are based on mathematic formulas. With the use of different parameters for the formulas, the phantom is adjusted to represent a human body at six different ages. The phantom used in this study represents an adult female (denoted in the Oak Ridge National Laboratory report as 15-AF).

In our implementation of the Cristy phantom (Figure), some modifications were made to enhance the simulation, to adapt the geometric shapes to the capabilities of Geant4, and to recreate the conditions during mammography. The major modifications, which were based on data from publication 89 of the International Commission on Radiological Protection (16), report 46 of the International Commission on Radiation Units and Measurements (17), and anatomy literature (18), were the use of different elemental compositions and densities for each tissue and the addition of the eyes, eye lenses, and sternum to the phantom. Two geometric adaptations were introduced in the phantom to allow a simpler implementation in Geant4. These were the (a) reorientation of the legs so that their long axis was vertical, as opposed to at an angle as in the original description, and (b) the cross section of the tori, which represent the sigmoid colon, was circular as opposed to elliptic. These two geometric modifications were estimated to have a negligible effect on the results, given the expected low radiation levels reaching the lower portion of the phantom. The adaptations necessary to recreate the conditions during a mammographic study were simulating the imaged breast as compressed either horizontally for the CC view or at an angle for the MLO view and rotating the head of the phantom toward the opposite side of the imaged breast in the CC view. The anthropomorphic phantom in this simulation had a total of 66 volumes (49 base volumes, with doubling of some because the body has two, such as eyes) of organs, bones, skin sections, and other soft tissues (Table 1).

View larger version (47K): [in this window] [in a new window] [Download PPT slide]   Simulation geometry used in this study for (a) craniocaudal (CC) and (b) mediolateral oblique (MLO) views. In the CC view, only outline of small intestine is included to show pelvis. In the MLO view, rib cage and sternum are omitted to show other organs. Sk. = skeleton.

To characterize the variation in organ dose with compressed breast thickness, the Monte Carlo simulations were repeated for thin breasts (2 cm thick in the CC view and 2.2 cm thick in the MLO view) and thick breasts (8 cm thick in the CC view and 8.5 cm thick in the MLO view).

Monte Carlo Simulation
To simulate the acquisition of a standard mammogram, the x-ray source, compression and support plates, and detector were placed in the appropriate location according to the simulated mammographic view and the imaged breast. For both views, the source-to-imager distance was set at 66 cm, and the air gap was set at 1.5 cm. At each energy level, 60 million monochromatic x-rays were emitted from the point source toward a random location on the detector surface so that the x-ray field at the detector surface was uniform and congruent with the detector edges. The path traveled by the x-rays was followed until the x-rays either exited the simulation limits or were completely absorbed. The energy lost by the x-rays at each interaction, along with the organ in which the deposition took place, was recorded. The total energy deposited in the imaged breast was used to compute the glandular dose, D_g(E), as described by Boone (7) with the suggestion of Wilkinson and Heggie (25), whereas the total energy deposited in the other organs was divided by each organ's mass to obtain the dose to each organ. The simulation was repeated with monochromatic x-rays of energies ranging from 6 to 35 keV in 1-keV steps. Because of the asymmetry of the distribution of the organs, the simulations were repeated for both breasts. The monochromatic results were interpolated to 0.5-keV resolution and combined by weighting them with the relative number of photons in each spectrum studied. The dose to each organ was normalized to that of the glandular dose to the breast, resulting in the relative organ dose (ROD), which represented the dose to an organ in the body per unit glandular dose to the breast. The simulations were performed in the Emory High Performance Computer Cluster (Emory University, Atlanta, Ga), which consists of 128 2.2-GHz processors (Opteron; Advanced Micro Devices, Sunnyvale, Calif).

To measure the resulting uncertainty in the results caused by the random nature of Monte Carlo simulations, the simulations of the two views of the left breast were repeated five times, and the coefficient of variation, or 100/µ, of the ROD for all the organs was computed for the x-ray spectra with the lowest total number of x-rays (molybdenum [Mo]/Mo target-filter combination with 25 kVp) and with the highest total number of x-rays (rhodium [Rh]/Rh target-filter combination with 35 kVp).

Computation of Dose to the Red Bone Marrow and the Bone Surfaces
Bone dosimetry is affected by the complex microscopic histologic features of the bones, which are impossible to account for in macroscopic Monte Carlo simulations. Therefore, the development of methodologies to compute dose to the bone surfaces (BSs) and to the red bone marrow (RBM) from macroscopic data has been an issue of intense research (26–33). In our study, the dose to the RBM was estimated by one of the authors (I.S.) with the three-parameter mass-energy absorption coefficient ratio method (26–28,33). This method has been shown to yield results comparable to those with all other methods applicable to a macroscopic Monte Carlo simulation (33). To compute the dose to the BS, the homogeneous bone approximation (33), which assigns the dose to the BS as the dose to the whole homogeneous bone volume, was used. These two methods have been shown to lead to overestimation of the dose to the RBM and BS at the low-energy range, so the results in this study represent a conservative upper limit (33).

Computation of Tissue Dose and Effective Dose
By using the computed ROD, an example of the calculation of the total dose to the organs, bones, and skin sections resulting from a standard one-breast two-view mammogram was computed. To perform this calculation, it was assumed that the CC view results in a glandular dose to the breast of 2 mGy, whereas the MLO view results in a glandular dose of 2.5 mGy.

By using the dose to each organ found from the Monte Carlo simulations, the effective dose was calculated by one of the authors (I.S.) with use of both the current recommended tissue-weighting factors that were based on publication 60 of the International Commission on Radiological Protection (34) and the new proposed recommendations of the commission posted at the commission's Web site on January 12, 2007 (35). The effective dose was computed in both cases for a complete mammographic examination (two views, both breasts) per unit glandular dose to both breasts.

Study of Possible Dose Reduction with a Lead Shield
To study the possibility of reducing the radiation dose to the organs of the body, a virtual 0.25-mm-thick lead shield placed between the simulated patient and the x-ray field was included in the simulations. In the simulations, the shield was implemented as transparent to the x-rays, but the fact that the x-rays had entered the shield was recorded. With this record, a second computation of the dose to the organs was performed automatically by the Monte Carlo program, in which the dose deposited in the organs by x-rays that were flagged as having entered the shield was ignored. This allowed the simultaneous computation of the dose to the organs with and without the shield. The only assumption necessary for this algorithm to work was that the lead shield was thick enough to absorb all x-rays that entered it. The necessity of making the lead shield thick enough to absorb all x-rays was accomplished by simulating a 0.25-mm-thick shield, which results in an absorption of 99.7% of x-rays at 35 keV.

The shield was simulated as large enough to cover the whole body, with an opening for the imaged breast. The opening had a length along the chest wall of 20 cm and a variable height 6 cm larger than the breast thickness.

Validation
The breast in the CC view was modified to match the geometry reported by Boone (8), and the simulations were repeated with 1 million monochromatic x-rays from 6 to 35 keV in 1-keV steps. The resulting glandular dose to the breast was compared with the results reported in the study by Boone. The mean deviation between our data and the fit equation reported by Boone was 7.2%.

Previous validations of simulations of the conditions present in mammography with the Geant4 tool kit point to the capability of the Monte Carlo simulation for prediction of the dose levels to the organs and tissues outside the primary x-ray field. The total linear attenuation coefficients, as well as the individual linear attenuation coefficients of the three relevant physical interactions between x-rays and soft tissue, used by Geant4 were reported to be previously validated in comparison with data from the National Institute of Standards and Technology (20). In addition, the x-ray scatter functions in mammography used with Geant4 also have been previously validated (21,36,37), pointing to the applicability of this package in the study of dosimetry related to x-rays scattered in the breast.

	RESULTS

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Tables 2 (CC view) and 3 (MLO view) show the ROD value for the organs (including the uterus or fetus), bones (discriminated into BS and RBM), and skin sections that received an ROD of 0.10% or higher in at least one view and one spectrum. Dose values that resulted in an ROD lower than this level were deemed negligible and are not shown for space considerations. For most volumes, the ROD remained constant after varying which breast was imaged. For these volumes, the mean ROD is reported. For the volumes for which a different ROD was found, depending on which breast was imaged, values for both left and right breasts are shown. The simulated spectra (38) used and their first half-value layers are also listed in Tables 2 and 3. The negligible dose levels received by the phantom's legs and sigmoid colon confirm the minimal effect of the two geometric modifications introduced in the design of the anthropomorphic phantom. Table 4 shows the results of the example of the calculation of total dose to the organs from a standard one-breast two-view mammogram.

The coefficients of variation of the ROD of the organs listed in Tables 2 and 3, found by repeating the Monte Carlo simulations of the mammograms of the left breast, are listed in Table 5. From these values, it can be seen that the uncertainty of the ROD for most organs is less than 5%. Although the number of x-rays that deposit energy in the eye lens is very low and results in a high coefficient of variation, the small mass of the lens results in an ROD high enough to include this volume in Tables 2 and 3. Because of the high coefficient of variation found for the uterus volume, the ROD reported in Tables 2 and 3 specifies only the order of magnitude of the computed ROD, and not a specific value, since the uncertainty is relatively high.

With the lead shield present, the ROD of the organs that received the highest dose was not decreased substantially (Table 6). The effect of the presence of the lead shield on ROD was found to be a weak function of the x-ray spectrum used and the breast imaged, so Table 6 shows the mean ratio of the ROD with the lead shield to the ROD without the lead shield. The contralateral breast in the CC view and the heart, the ipsilateral lung, and the thymus in both views were minimally protected by the shield. The dose to the contralateral breast in the MLO view was reduced to a third of the dose without the shield, whereas the dose to the ipsilateral eye and eye lens in both views was almost completely eliminated. The dose to the uterus was reduced by a factor of approximately seven in the CC view and a factor of two in the MLO view by the presence of the shield. Of the bones, only the ipsilateral clavicle in the CC view was well protected.

	DISCUSSION

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As expected, compared with the glandular dose, the skin of the imaged breast receives a much higher dose, which decreases with increasing x-ray spectrum energy. If only the portion of the breast skin facing the x-ray tube is considered, its local dose can be approximated to be double that specified for the whole-breast skin. The dose to the skin of the contralateral breast (1.62%–2.25% [Tables 2, 3]) can normally be ignored because that same skin will receive the full dose when the contralateral breast is being imaged.

In our study, we found that the dose to the uterus caused by an average two-view bilateral mammogram is less than 0.03 µGy (0.003 mrad) per imaged breast. This result can be representative of the dose to the fetus during the first trimester, when the volume of the uterus as simulated in our study is still representative of that of a pregnant woman and the conceptus is very small. This amount of dose to the fetus is approximately 100 to 700 times lower than that received by the fetus from a helical chest CT scan in a pregnant patient (42). Even though the dose to the fetus from a mammogram can be considered minimal, the use of a lead shield reduces this dose further by about a factor of between two and seven. Therefore, if a patient underwent standard mammography not knowing that she was in the early stages of pregnancy, our findings suggest that the dose to the fetus is minimal. If, however, a patient is known to be pregnant and mammography is deemed necessary, a lead apron can reduce this low amount of dose to the fetus by at least one-half.

Results with the shield show that most of the dose to the organs is a consequence of x-rays that scatter in the breast tissue and enter the trunk through the breast, thereby minimizing the benefit of using a lead shield or apron with normal circumstances.

The results from the simulations performed with breasts of different thicknesses show no substantial variation in the dose to the organs with varying breast thicknesses, except for the dose to the sternum in the MLO view. This finding can be explained by the fact that most of the x-rays entering the imaged breast are absorbed or scattered in the layers of breast tissue closest to the x-ray tube; therefore, the introduction or removal of additional breast tissue does not contribute substantially to the number of x-rays scattering out of the breast toward the rest of the body. With varying compressed breast thickness in the MLO view, the proximity of the top layer of the breast to the sternum varies and results in the substantial variation found in the dose to the sternum in this view.

A limitation of our study is that the results depend on the applicability of the mathematic phantom as representative of the human body. Although this phantom is used extensively for dosimetry in radiology, its simplification of the shapes of the organs of the human body has the potential of introducing severe errors in the results, particularly with patients with a body habitus that greatly deviates from the assumed shape of the phantom. However, in a recent study by Castellano et al (43), in which the dose estimations from CT acquisitions with the Cristy phantom were compared with those with a voxel-based phantom, the researchers found the disagreements between the two phantoms to be less than 38% and to be within 15% if the imaged sections of the phantoms are matched appropriately. Although these deviations are considerable, the importance of the dose to the different organs from mammography found in our study is still applicable because an increase in ROD of 40% would still result in maxima of 0.17% (ipsilateral lung), 0.78% (sternum RBM), and 3.30% (sternum BS). The effective dose computations, even with the additional 40% in the dose to all the organs except the imaged breast, are still valid, because the dose to the breast accounts for over 96% of the effective dose.

Another limitation is that two sources of radiation were not taken into account in our study: x-ray leakage from the shielded portions of the x-ray tube and the fraction of x-rays from the primary field that are transmitted through the imager support arm. According to the U.S. Code of Federal Regulations (44), the x-ray leakage in a mammographic system must be limited to a maximum air kerma of 0.88 mGy (100 mR [2.58 x 10^–5 C/kg] exposure) per hour at 1.0 m from the source. Approximating the time to obtain a bilateral two-view mammogram to entail 6 seconds of x-ray exposure, the air kerma at 1 m from the focal spot from leakage radiation must be less than 1.5 µGy (0.167 mR [4.31 x 10^–8 C/kg] exposure). The same chapter of the U.S. Code of Federal Regulations (44) limits the radiation transmitted through the imager support arm to 0.88 µGy air kerma (0.1 mR [2.58 x 10^–8 C/kg] exposure) 5 cm under the support arm per acquisition. Therefore, the radiation from tube leakage and primary barrier transmission is well within the uncertainty level of our study.

In summary, by using Monte Carlo methods and a modified anthropomorphic geometric phantom, a simulation of the conditions present during a standard mammographic acquisition was implemented and used to compute the radiation dose levels received by 66 different volumes representing the organs of the body during both CC and MLO view acquisitions. The dose to the organs and tissues located outside the primary x-ray field was found to be very low.

Practical application: The results of our study indicate the radiation dose levels received by the organs and tissues of the body from standard mammography. This information may be used by epidemiologists studying the risks involved in screening and diagnostic mammography and by radiologists to assuage patients' concerns about the amount of radiation exposure during mammography. Furthermore, since the dose to the uterus was found to be extremely low, a mammographic procedure, especially with the use of a lead apron, may be considered by the radiologist faced with a pregnant patient with a possible breast cancer diagnosis.

	ADVANCES IN KNOWLEDGE

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• On the basis of the results of our Monte Carlo and phantom study, the radiation dose to the organs and tissues of the body outside the primary x-ray field from standard mammography was very low (<2.5% of the average glandular dose to the imaged breast).
  
• The uterus is exposed to extremely low dose levels (<10^–5 of the average glandular dose to the imaged breast) during standard mammography, resulting in equally low dose levels to the fetus during early pregnancy.
  
• The use of a lead apron or other added shielding does not substantially decrease most of the dose to the organs and tissues of the body but does further reduce the already minimal dose to the fetus.
  

	IMPLICATIONS FOR PATIENT CARE

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• On the basis of the results of our Monte Carlo and phantom study, mammography can be considered as an option by radiologists faced with an early-stage pregnant patient with a possible diagnosis of breast cancer.
  
• If mammography is performed in a pregnant patient, the use of a lead apron to further decrease the dose to the fetus is advised.
  
• If a patient is not aware of her pregnancy status and happens to undergo mammography, the risk to the fetus appears to be mini-mal.
  

	ACKNOWLEDGMENTS

 
The authors thank Steve Pittard for providing technical assistance with the use of the Emory High Performance Computer Cluster.

	FOOTNOTES

 

Abbreviations: BS = bone surface • CC = craniocaudal • MLO = mediolateral oblique • RBM = red bone marrow • ROD = relative organ dose

Guarantor of integrity of entire study, I.S.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, I.S., S.S., S.V., A.K.; experimental studies, all authors; statistical analysis, I.S.; and manuscript editing, all authors

Authors stated no financial relationship to disclose. The contents are solely the responsibility of the authors and do not necessarily represent the official views of the NIH, NIBIB, or the GCC.

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