- Research
- Open Access
Risk of secondary cancers from scattered radiation during intensity-modulated radiotherapies for hepatocellular carcinoma
https://doi.org/10.1186/1748-717X-9-109
© Kim et al.; licensee BioMed Central Ltd. 2014
- Received: 10 September 2013
- Accepted: 17 March 2014
- Published: 8 May 2014
Abstract
Purpose
To evaluate and compare the risks of secondary cancers from therapeutic doses received by patients with hepatocellular carcinoma (HCC) during intensity-modulated radiotherapy (IMRT), volumetric arc therapy (VMAT), and tomotherapy (TOMO).
Methods
Treatments for five patients with hepatocellular carcinoma (HCC) were planned using IMRT, VMAT, and TOMO. Based on the Biological Effects of Ionizing Radiation VII method, the excess relative risk (ERR), excess absolute risk (EAR), and lifetime attributable risk (LAR) were evaluated from therapeutic doses, which were measured using radiophotoluminescence glass dosimeters (RPLGDs) for each organ inside a humanoid phantom.
Results
The average organ equivalent doses (OEDs) of 5 patients were measured as 0.23, 1.18, 0.91, 0.95, 0.97, 0.24, and 0.20 Gy for the thyroid, lung, stomach, liver, small intestine, prostate (or ovary), and rectum, respectively. From the OED measurements, LAR incidence were calculated as 83, 46, 22, 30, 2 and 6 per 104 person for the lung, stomach, normal liver, small intestine, prostate (or ovary), and rectum.
Conclusions
We estimated the secondary cancer risks at various organs for patients with HCC who received different treatment modalities. We found that HCC treatment is associated with a high secondary cancer risk in the lung and stomach.
Keywords
- HCC
- IMRT
- VMAT
- Tomotherapy
- Radiophotoluminescence
- OED
- EAR
- ERR
- LAR
Introduction
Hepatocellular carcinoma (HCC), the most common primary cancer of the liver, is a malignant disease that causes death within a few months, unless it is treated appropriately [1, 2]. Surgical resection is the standard treatment for HCC, but approximately 80% of cases are unresectable, generally because of preexisting hepatic dysfunction associated with cirrhosis or the multifocality of its presentation [3]. Transcatheter arterial chemoembolization (TACE), percutaneous ablation [4, 5], and radiation therapy (RT) [6, 7] have been used for patients with unresectable HCC, but the standard treatment modality for primary HCC has not yet been established. Only TACE has been proven to provide a survival benefit in a phase III study of advanced-stage disease [8]. In the past, the role of RT for HCC has been limited because of the low tolerance of the liver to RT and the risks of radiation-induced liver disease [9]. However, RT treatments have tended to shift from palliative to cure-oriented therapies with each new development in RT techniques, such as intensity-modulated radiotherapy (IMRT) [10–16] (including volumetric-modulated arc therapy [17, 18]), helical tomotherapy (TOMO) [19–24] and particle therapy [25–27].
When tumors are exposed to the high doses that are prescribed for a definitive or palliative goal, the surrounding normal tissues are generally exposed to intermediate doses because of the primary radiation in the beam path. Therefore, the treatment planning is optimized to identify the option that best satisfies two conflicting priorities: reducing the dose that the surrounding normal organ is exposed to, and focusing the prescription dose into a target volume. However, out-of-field exposure is another issue of concern; during radiation treatment, the rest of the body is also exposed to low doses because therapeutic radiation in out-of-field region where is all tissues without the trans-axial planed of PTV. Therefore, it is also important to measure the exposed dose for normal organs in out-of-field regions, as well as the corresponding cancer risk.
To date, there have been many measurements of secondary scattered dose and many assessments of secondary cancer risk [28–34]. These studies reflect concerns that the secondary cancer risk may be increased by IMRT compared with that by 3D-CRT because IMRT uses more fields and monitor units, which cause a higher whole-body exposure to leakage radiation. It has been reported that IMRT induces almost twice the incidence of second malignancies that is associated with 3D-CRT [28–34]. Yoon et al. have investigated the secondary scattered radiation doses of IMRT and proton therapy for patients with lung and liver cancer [31]. They presented secondary scattered dose measurements for IMRT at 20–50 cm from the isocenter, which ranged from 5.8 to 1.0 mGy per 1 Gy of the target volume dose (Gray [Gy] is the SI unit of therapeutic absorbed dose). In a previous study, we reported organ equivalent dose (OED) measurements for patients with stage III non-small cell lung cancer [30]. The mean values of the relative OEDs of secondary doses from VMAT and TOMO, which were normalized by IMRT, ranged from 88.63% to 41.59%.
In this study, we compared the risks of secondary cancer from out-of-field and in-field radiation for three treatment modalities, using the concept of OED for radiation-induced cancer in patients with primary HCC.
Methods and materials
Patient data and treatment planning
Patient information
ID | Sex | Age | Disease | Stage | PTV volume (cc) | Prescription dose (Gy) |
---|---|---|---|---|---|---|
1 | Male | 62 | HCC | III | 483 | 55.0 |
2 | Male | 54 | HCC | I | 60 | 66.0 |
3 | Male | 59 | HCC | III | 421 | 52.5 |
4 | Female | 49 | HCC | IV | 2112 | 60.0 |
5 | Female | 42 | HCC | IV | 214 | 72.0 |
Patient 4’s dose distribution for different modalities: IMRT, VMAT, and TOMO. The prescription dose was 62.5 Gy in 25 fractions.
Calibration of the radiophotoluminescence glass dosimeter
In this study, we used a commercially available radiophotoluminescence glass dosimeter (RPLGD; GD-302 M, Asahi Techno Glass Co., Japan) for dose measurements [35–37]. For these RPLGDs, the absorbed dose was proportional to the light signal (500–700 nm) from the irradiated dosimeter when it was exposed to 365-nm mono-energetic laser light. At energies >200 keV, RPLGDs have a reliable reproducibility of approximately 1% and relatively low energy dependency compared with themoluminescence dosimeters (TLDs) [35–37]. In addition, RPLGDs have a relatively small incident-beam angular dependency and a low toxicity inside the human body compared with TLDs or optically stimulated luminescence dosimeters (OSLDs) [38–40]. Our RPLGDs had a rod-like shape with a diameter of 1.5 mm and a length of 8.5 mm.
RPLGDs were calibrated by measuring the response of each detector after being exposed to a 10 × 10 cm2 open field photon beam at the depth of the maximum dose in water-equivalent solid phantom, with a 100-cm source-to-surface distance (SSD) and the absorbed dose at the calibration point was sat as 1 cGy per one monitor units (MU). The reproducibility of the RPLGDs was estimated by calculating the standard deviation of dose measurements that were taken when the same detector was exposed to the photon beam three times. Additionally, the deviations of each RPLGD detector were measured to characterize the RPLGDs.
Measurement of therapeutic dose during IMRT, VMAT, and Tomotherapy treatment
The setup for the therapeutic dose measurement with a humanoid phantom. To measure the organ doses in the out-of-field region, two or three RPLGDs were inserted at the positions of interesting organs inside the humanoid phantom: the thyroid, small intestine, prostate/ovary, and rectum.
Cancer incidence risk estimation attributable to secondary doses
where M(D, e, a) is the excess absolute risk at attained age a from exposed age e, S(a)/S(e) is the ratio of the probability of surviving at age a and e, and L is the latent period (5 y for solid cancers) (National Research Council 2006).
Parameters for preferred risk incidence models in BEIR VII a
Cancer | ERR model | EAR model | ||||||
---|---|---|---|---|---|---|---|---|
βM | βF | γ | η | βM | βF | γ | η | |
Thyroid | 0.53 | 1.05 | −0.83 | 0.00 | Not used | |||
Lung | 0.32 | 1.40 | −0.30 | −1.40 | 2.30 | 3.40 | −0.41 | 5.20 |
Stomach | 0.21 | 0.48 | −0.30 | −1.40 | 4.90 | 4.90 | −0.41 | 2.80 |
Liver | 0.32 | 0.32 | −0.30 | −1.40 | 2.20 | 1.00 | −0.41 | 4.10 |
Colon | 0.63 | 0.43 | −0.30 | −1.40 | 3.20 | 1.60 | −0.41 | 2.80 |
Bladder | 0.50 | 1.65 | −0.30 | −1.40 | 1.20 | 0.75 | −0.41 | 6.00 |
Prostate | 0.12 | - | −0.30 | −1.40 | 1.20 | - | −0.41 | 2.80 |
Ovary | - | 0.38 | −0.30 | −1.40 | - | 0.70 | −0.41 | 2.80 |
Organ equivalent dose (Gy) per prescription dose at each organ
Organ | δ | Modality\ID | 1 | 2 | 3 | 4 | 5 |
---|---|---|---|---|---|---|---|
Thyroid | 0.69 | IMRT | 0.21 | 0.09 | 0.28 | 0.55 | 0.17 |
VMAT | 0.15 | 0.08 | 0.23 | 0.47 | 0.17 | ||
TOMO | 0.18 | 0.14 | 0.19 | 0.40 | 0.11 | ||
Lung | 0.15 | IMRT | 0.13 | 0.07 | 0.18 | 2.59 | 0.25 |
VMAT | 0.13 | 0.08 | 0.20 | 2.87 | 0.31 | ||
TOMO | 1.72 | 1.65 | 2.37 | 3.27 | 1.89 | ||
Stomach | 1.20 | IMRT | 0.83 | 0.82 | 0.83 | 0.83 | 1.08 |
VMAT | 0.83 | 0.83 | 0.83 | 0.83 | 1.73 | ||
TOMO | 0.83 | 0.83 | 0.83 | 0.83 | 0.83 | ||
Normal liver | 1.14 | IMRT | 0.83 | 0.72 | 0.83 | 0.80 | 1.69 |
VMAT | 0.83 | 0.72 | 0.83 | 0.83 | 1.74 | ||
TOMO | 0.88 | 0.86 | 0.88 | 0.88 | 0.88 | ||
Small intestine | 0.26 | IMRT | 0.67 | 0.26 | 0.88 | 2.04 | 0.48 |
VMAT | 0.63 | 0.29 | 0.90 | 2.03 | 0.69 | ||
TOMO | 0.70 | 0.21 | 0.88 | 3.51 | 0.41 | ||
Prostate/Ovary | 0.73 | IMRT | 0.25 | 0.13 | 0.25 | 0.59 | 0.18 |
VMAT | 0.19 | 0.07 | 0.24 | 0.48 | 0.17 | ||
TOMO | 0.21 | 0.08 | 0.22 | 0.44 | 0.14 | ||
Rectum | 0.26 | IMRT | 0.18 | 0.08 | 0.22 | 0.51 | 0.14 |
VMAT | 0.15 | 0.06 | 0.18 | 0.41 | 0.15 | ||
TOMO | 0.17 | 0.06 | 0.16 | 0.40 | 0.12 |
In this study, we have investigated the OED based cancer incidence risk. The doses and cancer risks were evaluated for thyroid, lung, stomach, normal liver, small intestine, prostate/Ovary and rectum which were provided the parameter values for calculation by preferred risk models in BEIR VII.
Results and discussion
Treatment planning information
ID | Modality | # of fields (or arcs) | MU/Gy |
---|---|---|---|
1 | IMRT | 8 | 543 |
VMAT | 2 | 291 | |
TOMO | n/a | 907 | |
2 | IMRT | 8 | 312 |
VMAT | 2 | 346 | |
TOMO | n/a | 534 | |
3 | IMRT | 8 | 597 |
VMAT | 2 | 345 | |
TOMO | n/a | 717 | |
4 | IMRT | 8 | 722 |
VMAT | 2 | 317 | |
TOMO | n/a | 1865 | |
5 | IMRT | 8 | 384 |
VMAT | 2 | 304 | |
TOMO | n/a | 776 |
The absorbed dose per 1 Gy of therapeutic dose at each organ
Organ | Modality\ID | Organ dose per 1 Gy (cGy/Gy) | ||||
---|---|---|---|---|---|---|
1 | 2 | 3 | 4 | 5 | ||
Thyroid | IMRT | 0.4 | 0.1 | 0.6 | 1.1 | 0.3 |
VMAT | 0.3 | 0.1 | 0.5 | 0.9 | 0.3 | |
TOMO | 0.4 | 0.2 | 0.4 | 0.8 | 0.2 | |
Lung | IMRT | 2.6 | 1.1 | 5.2 | 8.8 | 1.8 |
VMAT | 2.8 | 0.1 | 5.5 | 10.1 | 2.4 | |
TOMO | 6.9 | 3.0 | 11.6 | 16.5 | 6.1 | |
Stomach | IMRT | 10.5 | 30.7 | 49.3 | 26.0 | 1.7 |
VMAT | 23.4 | 30.5 | 49.5 | 30.3 | 7.3 | |
TOMO | 28.3 | 46.7 | 53.3 | 43.0 | 13.5 | |
Normal liver | IMRT | 41.0 | 20.1 | 45.2 | 45.7 | 29.3 |
VMAT | 42.7 | 18.5 | 38.7 | 54.1 | 30.6 | |
TOMO | 47.0 | 25.3 | 44.9 | 49.8 | 35.0 | |
Small intestine | IMRT | 1.3 | 0.4 | 1.9 | 4.8 | 0.7 |
VMAT | 1.3 | 0.5 | 1.9 | 4.8 | 1.1 | |
TOMO | 1.4 | 0.3 | 1.9 | 15.7 | 0.6 | |
Prostate/Ovary | IMRT | 0.5 | 0.2 | 0.5 | 1.2 | 0.3 |
VMAT | 0.4 | 0.1 | 0.5 | 1.0 | 0.3 | |
TOMO | 0.4 | 0.1 | 0.5 | 0.9 | 0.2 | |
Rectum | IMRT | 0.3 | 0.1 | 0.4 | 0.9 | 0.2 |
VMAT | 0.3 | 0.1 | 0.4 | 0.7 | 0.2 | |
TOMO | 0.3 | 0.1 | 0.3 | 0.7 | 0.2 |
Dose-volume histogram (DVH) for IMRT (dashed), VMAT (dotted), and TOMO (solid line) plans. These histograms include dose-volume information of patient 1 for the lung (blue), normal liver (green), and stomach (black).
For the absorbed doses of organs in in-field region, the uncertainties were assumed to less than 3% because the absorbed dose values from primary radiation for IMRT, VMAT and TOMO were based on the dose calculation from the radiation treatment planning system (RTPS). The dose measurement uncertainties of organs at out-of-fields region where is mainly contributed by stray radiation was less than 3% for each RPLGD measurement.
For each of the five patients, Table 3 presents OED measurements (or calculation from DVH) for IMRT, VMAT, and TOMO. The mean OEDs per prescription dose at the thyroid, lung, stomach, normal liver, small intestine, prostate (or ovary), and rectum were 0.26, 0.65, 0.88, 0.98, 0.87, 0.28, and 0.22 Gy for IMRT; 0.22, 0.72, 1.01, 0.99, 0.91, 0.23, and 0.18 Gy for VMAT; and 0.21, 2.18, 0.83, 0.87, 1.14, 0.22, and 0.18 Gy for TOMO, respectively. (Means were taken over the five patients). The OED decreased as the distance from the in-field region increased. For the OED measurement at out-of-field region, the OED differences for three different modalities at each organ were less than 10% except patient 2. This result conflicts with the findings of a previous study on lung cancer [30]. In this previous study, we reported that TOMO resulted in lower OEDs than IMRT or VMAT, based on estimations of OED for the thyroid, pancreas, bowel, rectum, and prostate. The main difference between these two studies is the measurement setup and treatment site. In the previous study, RPLGDs were positioned on the treatment table without build-up material. In this study, RPLGDs were inserted into the humanoid phantom at each organ position. Because the previous study could not include the maximum out-of-field dose without the build-up material, 6 MV TOMO provided lower OEDs than IMRT or VMAT (which usually use 6 MV photon beam). For in-field region, the OED of lung was greater with TOMO than other modalities as shown as Table 3 because the absorbed dose of lung with TOMO was relatively higher than other modalities. Because the OED calculation was based on a plateau-response model which is converged to 1/δ with high absorbed dose, the OED values of stomach and normal liver were close to 0.83.
Excess relative risk (ERR) and excess absolute risk (EAR) for five patients
Organ | Modality\ID | ERR (EAR*) | ||||
---|---|---|---|---|---|---|
1 | 2 | 3 | 4 | 5 | ||
Thyroid | IMRT | 0.11 | 0.05 | 0.15 | 0.58 | 0.18 |
VMAT | 0.08 | 0.05 | 0.12 | 0.49 | 0.18 | |
TOMO | 0.10 | 0.08 | 0.10 | 0.42 | 0.12 | |
Lung | IMRT | 0.03 (1.47) | 0.02 (0.50) | 0.04 (1.76) | 2.98 (18.22) | 0.34 (1.01) |
VMAT | 0.07 (1.51) | 0.02 (0.53) | 0.04 (1.95) | 3.31 (22.20) | 0.42 (1.26) | |
TOMO | 0.91 (20.08) | 0.39 (11.28) | 0.52 (22.77) | 3.76 (22.97) | 2.53 (7.62) | |
Stomach | IMRT | 0.11 (9.76) | 0.13 (7.22) | 0.12 (8.82) | 0.33 (6.04) | 0.49 (5.79) |
VMAT | 0.44 (9.79) | 0.13 (7.28) | 0.12 (8.82) | 0.33 (6.04) | 0.79 (9.29) | |
TOMO | 0.44 (9.79) | 0.13 (7.35) | 0.12 (8.82) | 0.33 (6.04) | 0.38 (4.48) | |
Normal liver | IMRT | 0.17(6.59) | 0.17 (3.76) | 0.18 (5.62) | 0.21 (1.42) | 0.52 (1.94) |
VMAT | 0.44 (6.60) | 0.17 (3.75) | 0.18 (5.64) | 0.22 (1.48) | 0.53 (2.00) | |
TOMO | 0.46 (6.95) | 0.20 (4.46) | 0.19 (5.95) | 0.23 (1.56) | 0.27 (1.00) | |
Small intestine | IMRT | 0.27 (5.16) | 0.12 (1.47) | 0.38 (6.08) | 0.72 (4.82) | 0.20 (0.85) |
VMAT | 0.33 (4.85) | 0.13 (1.65) | 0.38 (6.20) | 0.72 (4.80) | 0.28 (1.22) | |
TOMO | 0.37 (5.35) | 0.10 (1.20) | 0.38 (6.05) | 1.24 (8.31) | 0.27 (0.71) | |
Prostate/Ovary | IMRT | 0.02 (0.07) | 0.01 (0.03) | 0.02 (0.06) | 0.18 (0.61) | 0.07 (0.14) |
VMAT | 0.10 (0.05) | 0.01 (0.01) | 0.02 (0.06) | 0.15 (0.49) | 0.06 (0.13) | |
TOMO | 0.11 (0.06) | 0.01 (0.01) | 0.02 (0.05) | 0.14 (0.46) | 0.05 (0.11) | |
Rectum | IMRT | 0.07 (1.36) | 0.04 (0.44) | 0.09 (1.49) | 0.18 (1.20) | 0.06 (0.25) |
VMAT | 0.08 (1.12) | 0.03 (0.35) | 0.08 (1.26) | 0.14 (0.96) | 0.06 (0.26) | |
TOMO | 0.09 (1.32) | 0.03 (0.36) | 0.07 (1.13) | 0.14 (0.95) | 0.05 (0.20) |
Lifetime attributable risk (LAR) for five patients
Organ | Modality\ID | LAR* | ||||
---|---|---|---|---|---|---|
1 | 2 | 3 | 4 | 5 | ||
Lung | IMRT | 4.1 | 3.3 | 6.9 | 220.4 | 18.0 |
VMAT | 4.3 | 3.4 | 7.7 | 244.3 | 22.5 | |
TOMO | 56.4 | 72.6 | 89.6 | 277.9 | 135.3 | |
Stomach | IMRT | 27.4 | 46.5 | 34.7 | 73.0 | 102.9 |
VMAT | 27.5 | 46.9 | 34.7 | 73.0 | 165.1 | |
TOMO | 27.5 | 47.3 | 34.7 | 73.0 | 79.5 | |
Normal liver | IMRT | 18.5 | 24.2 | 22.1 | 17.2 | 34.4 |
VMAT | 18.5 | 24.1 | 22.2 | 17.9 | 35.5 | |
TOMO | 19.5 | 28.7 | 23.4 | 18.8 | 17.8 | |
Small intestine | IMRT | 14.5 | 9.5 | 23.9 | 58.4 | 15.1 |
VMAT | 13.6 | 10.6 | 24.4 | 58.1 | 21.6 | |
TOMO | 15.0 | 7.7 | 23.8 | 100.5 | 12.6 | |
Prostate/Ovary | IMRT | 0.2 | 0.2 | 0.2 | 7.4 | 2.5 |
VMAT | 0.1 | 0.1 | 0.2 | 6.0 | 2.4 | |
TOMO | 0.2 | 0.1 | 0.2 | 5.5 | 2.0 | |
Rectum | IMRT | 3.8 | 2.8 | 5.9 | 14.6 | 4.4 |
VMAT | 3.1 | 2.3 | 4.9 | 11.7 | 4.5 | |
TOMO | 3.7 | 2.3 | 4.5 | 11.5 | 3.6 |
Although the risk of radiogenic cancer is generally proportional to exposed dose, there are non-negligible uncertainties in the risk model such as the uncertainty in the dose–response relationship for carcinogenesis, uncertainty in the model parameter and etc. The latest report on radiation risk suggested that one cannot choose decisively among the several dose–response models based on the empirical data [17]. This means that there might be large inherent uncertainties in the risk estimation. In addition, there is the systematic uncertainty of applying a risk model for a general U.S. population to international liver cancer patients in our study. This implies that further study on the correlation between dose and secondary cancer risk is needed.
Conclusion
In this study, we compared secondary cancer risks for patients with HCC. We found that the secondary cancer risk in the out-of-field region depends on the distance from the target volume and the target volume size. Of all the organs that were considered, the lung was subject to the highest risk of radiation-induced cancer after HCC RT.
Consent
Written informed consent was obtained from the patient for the publication of this report and accompanying images.
Declarations
Acknowledgment
This work was supported by the General Researcher Program (NRF-2012R1A1A2003174); the Nuclear Safety Research Program (Grant No. 1305033) through the Korea Radiation Safety Foundation (KORSAFe) and the Nuclear Safety and Security Commission (NSSC); the Radiation Safety Program (2011–31115); and Radiation Technology Development Program (2013M2A2A4027117), Republic of Korea.
Authors’ Affiliations
References
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