Research ArticleClinical Studies
Open Access

Influence of Respiratory Motion on Dose Distribution in Gastric Mucosa-associated Lymphoid Tissue Lymphoma Radiotherapy

TADASHI MATSUMOTO, RYO TOYA, YOSHINOBU SHIMOHIGASHI, KOHSEI YAMAGUCHI, TAKAHIRO WATAKABE, TOMOHIKO MATSUYAMA, YOSHIYUKI FUKUGAWA, YUDAI KAI and NATSUO OYA
Anticancer Research February 2024, 44 (2) 687-694; DOI: https://doi.org/10.21873/anticanres.16859

Abstract

Background/Aim: The present study investigated the effect of respiratory motion on planned radiotherapy (RT) dose for gastric mucosa-associated lymphoid tissue (MALT) lymphoma using four-dimensional dose (4D-dose) accumulation. Patients and Methods: 4D-computed tomography (4D-CT) images of 10 patients with gastric MALT lymphomas were divided into 10 respiratory phases. Further, the 3D-dose was calculated using 3D conformal RT (3D-CRT) and volumetric modulated arc therapy (VMAT) plans based on the average intensity projection (AIP) images. Then, both plans were recalculated according to each phase image. Moreover, the dose distributions in each phase were transferred to the AIP images using deformable image registration. The 4D-dose distribution was calculated by summing the doses of each phase, and it was compared with the dosimetric parameters of the 3D-dose distribution. Results: For 3D-CRT, the D95 and D99 of the 4D-dose in the planning target volume (PTV) were significantly lower than those of the 3D-dose, with mean differences of 0.2 (p=0.009) and 0.1 Gy (p=0.021), respectively. There were no significant differences in the other PTV and organ-at-risk dosimetric parameters of 3D-CRT or in any dosimetric parameters of VMAT between the 3D- and 4D-dose distributions. Conclusion: The effect of respiratory motion on the planned 3D-CRT and VMAT dose distributions for gastric MALT lymphoma is minimal and clinically negligible.

Key Words:

Mucosa-associated lymphoid tissue (MALT) lymphoma can arise from any part of the human body, with the stomach being the most common site. Gastric MALT lymphomas are commonly found within the stomach, with stage IE accounting for 70%-80% of cases (1). Radiotherapy (RT) is the primary treatment option among Helicobacter pylori (HP)-positive patients who do not respond to eradication therapy, HP-positive patients with certain genetic mutations, and HP-negative patients (2). RT for gastric MALT lymphoma can achieve a local control rate of >90%, and a prescribed dose of 30 Gy in 20 fractions is recommended. Gastric MALT lymphoma patients can have a good prognosis after RT (3). Therefore, the organ-at-risk (OAR) doses should be maintained at the lowest possible value.

The stomach is a large organ surrounded by various radiosensitive organs, including the kidneys, liver, spinal cord, small bowel, and duodenum. RT for gastric MALT lymphoma is challenging because it requires a huge target volume to be irradiated while avoiding these radiosensitive organs. Traditionally, three-dimensional conformal RT (3D-CRT) is widely used for the treatment (4). In the last decade, volumetric modulated arc therapy (VMAT) has been increasingly used for abdominal tumors (5, 6). VMAT can deliver beams while modifying the dose rate, field shape, and gantry rotation speed (7). A previous study on gastric MALT lymphoma showed that the VMAT plan is superior to the 3D-CRT plan in terms of homogeneity and conformity of the planning target volume (PTV) while reducing the OAR doses (8). Meanwhile, the abdominal organs change position with respiration (9), possibly affecting the planned dose distribution of the target volumes and OARs (10, 11). Thus, the remaining concern is the influence of respiratory motion on the dose distribution of treatment plans for gastric MALT lymphoma.

Four-dimensional computed tomography (4D-CT) imaging, which provides morphologic information about the structures in each respiratory phase, is a useful technique for assessing the respiratory changes of the target volume and OARs (12). Additionally, deformable image registration (DIR) techniques, which yield tissue deformation by resolving the voxel-to-voxel changes between two images, have recently improved (13). These technical advancements facilitate the use of four-dimensional dose (4D-dose) accumulation, which involves the integration of the 3D-dose distribution per respiratory phase produced by 4D-CT imaging onto the target image using DIR. Currently, 4D-dose accumulation is the standard method used for assessing the effect of respiratory changes on the treatment plan’s dose distribution (14). However, studies examining the effect of respiratory changes on dose distribution in RT planning for gastric MALT lymphoma using 4D-dose accumulation are lacking. Thus, the current study aimed to investigate the effect of respiratory motion on the planned RT dose for gastric MALT lymphomas using 4D-dose accumulation.

Patients and Methods

Patients. The 4D-CT images of 10 consecutive patients with stage IE gastric MALT lymphoma [7 men and 3 women with a median age of 63 (range=52-72) years] who received RT at our hospital between February 2019 and October 2021 were used in the present study.

CT simulation. The detailed information on CT simulation has been described previously (8). In our study, the patients fasted for at least 8 h before the CT simulation. 4D-CT imaging was performed for RT planning, and the images were divided into 10 respiratory phases. The average intensity projection (AIP) of the CT images was created based on all respiratory phase projection data. All CT images were exported to the treatment planning system (RayStation Clinical version 10A SP1, RaySearch Laboratories, Stockholm, Sweden) and registered by the hardware arrangement.

Definition of contours. To define the target volumes and OARs, the Radiation Therapy Oncology Group contouring atlases were used (15). Contouring was performed via a consensus decision between two radiation oncologists with 6 and 18 years of experience. According to the endoscopic examination results, we determined the gross tumor volume. The clinical target volume (CTV) was defined as the volume of the whole stomach (stomach CTV), from the gastro–esophageal junction to the duodenal bulb. The CTV was delineated on the AIP and 10 respiratory phase CT images. The CTV-4D, defined as the volume covering the stomach’s 10 respiratory phases, was delineated on the AIP CT image data sets using fused 4D-CT images (9). Based on the guideline recommendation, the PTV was generated by adding a 10-mm margin for CTV-4D, which included intra- and inter-fractional changes in stomach volume, respiratory movement, and set-up errors (16). The OARs, including the kidneys, liver, spinal cord, small bowel, and duodenum, were delineated on the AIP and each respiratory phase CT image.

Treatment planning. The 3D-CRT and VMAT plans were based on the AIP CT images. For irradiation in both plans, a linear accelerator (TrueBeam Edge; Varian Medical Systems, Palo Alto, CA, USA) was used. The dose of 30 Gy in 20 fractions was prescribed. The 3D-CRT plan comprised a four-box field with a 10-MV X-ray (8). The multileaf collimator was adjusted with a 5-mm leaf margin in all directions from the PTV. The VMAT plan comprised a single full arc with a 6-MV X-ray (8). The goals of each VMAT plan were as follows: minimum coverage dose for 95% of the PTV (D95) should be >95% of the prescribed dose; mean dose (Dmean) in the liver, <12.5 Gy; Dmean of each kidney, <10 Gy; maximum dose (Dmax) of the spinal cord, <30 Gy; and Dmax of the small bowel and duodenum, <31.5 Gy (17). The collapsed cone convolution algorithm with a 2.0-mm grid size was used for dose calculation.

4D-dose accumulation. The 4D-dose accumulation workflow is shown in Figure 1. The AIP-based treatment plans were copied onto the 4D-CT images of each phase without changing the planning parameters. The dose was then recalculated based on each 4D-CT phase image. Subsequently, DIR was performed to produce a 4D-dose distribution. In the present study, an anatomically constrained deformation algorithm was used for DIR (13). Using the AIP as a reference image, each phase image was deformed to produce a deformation map (Figure 2). To confirm whether the target volumes and OARs were deformed appropriately, a visual inspection was performed (18). Each dose distribution was accumulated with equal weighting equivalent to 1/10th of the prescribed dose on a reference image using the corresponding deformation map. Moreover, the dose difference percentage was estimated by subtracting the 3D-dose distribution from the 4D-dose distribution.

Figure 1.
Figure 1.

Flow chart of the 4D-dose accumulation. PTV (pink) and CTV-4D (purple) are displayed on the beam’s eye view of the average intensity projection (AIP)-based treatment plans. DIR: Deformable image registration.

Figure 2.
Figure 2.

The fusion views and deformable vector fields from the 0% phase to the average intensity projection (AIP) images. (A) Before deformable image registration (DIR). (B) After DIR. The blue and orange colors represent the AIP and 0% phase images, respectively. (C) Displacement field color table. The blue and red meshes indicate the lower and higher magnitudes, respectively.

Dosimetric parameters for plan evaluation. Plan evaluation was performed using a dose–volume histogram. D95 was used to evaluate the PTV coverage. The homogeneity index (HI) and conformity index (CI) of the PTV were calculated using equations [1] and [2], which are as follows (8):

Embedded Image [1],

Embedded Image [2],

where D1 and D99 are the minimum doses covering 1% and 99% of the PTV, respectively, and Dp is the prescription dose. D1 and D99 were used to evaluate the maximum and minimum doses of the PTV, respectively. BV95 is the body volume receiving 95% of the prescribed dose.

The Dmean and Dmax were used for evaluating the parallel organs (kidneys and liver) and serial organs (spinal cord, small bowel, and duodenum), respectively.

Stomach CTV center of mass displacement. The coordinates of the center of mass (COM) of the stomach CTV in the 0% phase image were set as zero. In each patient, the displacement from the 0% phase images to the other respiratory phase images for the anterior–posterior (AP), left–right (LR), and superior–inferior (SI) directions was calculated.

Statistical analysis. To compare the 3D- and 4D-dose distributions, we performed the Wilcoxon signed-rank test. The Statistical Package for the Social Sciences (version 26.0; IBM, Armonk, NY, USA) was used for the statistical analyses. A p-value of <0.05 was considered statistically significant.

Ethics approval and consent to participate. The present study was approved by Institutional Ethical Review Board (Kumamoto University Hospital Review Board No. 1878). All patients were enrolled with prior written informed consent for this study and consent regarding the use of image data. All research procedures were performed in accordance with the Declaration of Helsinki, related guidelines, and regulations.

Results

Stomach displacements. Figure 3 and Table I show the stomach CTV COM respiratory displacement. The average (±standard deviation) respiratory displacement in 10 patients in the AP, LR, and SI directions were 0.41 (±0.10), 0.35 (±0.19), and 0.67 (±0.16) cm, respectively.

Figure 3.
Figure 3.

Respiratory displacement in each respiratory phase for the center of mass of the clinical target volume.

View this table:
Table I.

Respiratory displacement of the center of mass of the clinical target volume in 10 patients.

Dosimetric parameters. Table II shows the dosimetric parameters of the 3D- and 4-D doses. Figure 4 depicts an example of the dose distribution in the 3D-CRT and VMAT plans. For the 3D-CRT plan, the D95 and D99 of the 4D-dose in PTV were significantly lower than those of the 3D-dose, with mean difference of 0.2 (p=0.009) and 0.1 Gy (p=0.021), respectively. There were no significant differences in the other PTV and OAR dosimetric parameters of the 3D-CRT plan or any dosimetric parameters of the VMAT plan between the 3D- and 4D-dose distributions.

View this table:
Table II.

Dosimetric parameters of the 3D- and 4D-dose distributions.

Figure 4.
Figure 4.

Examples of the dose distributions for (A) three-dimensional (3D) conformal radiotherapy and (B) volumetric modulated arc therapy plans. Left: 3D-dose; center: 4D-dose; right: dose difference (%) between the 3D- and 4D-dose distributions (4D-dose minus 3D-dose).

Discussion

We evaluated the 4D-dose distribution of 3D-CRT and VMAT plans delivered to patients with gastric MALT lymphoma using 4D-dose accumulation with 4D-CT and DIR. The results revealed that the effect of respiratory motion on the planned dose distributions for gastric MALT lymphoma is minimal and clinically negligible in both plans.

In the current study, 4D-dose accumulation was used for evaluating the 4D-dose distribution of OARs and PTV (19). Uchinami et al. have assessed stomach motion based on the dosimetric parameters in 10 gastric lymphoma patients receiving intensity-modulated RT. The isocenter shift method was used, wherein the isocenter and beams were shifted three-dimensionally in the opposite direction of the actual organ motion to reproduce the stomach motion in the treatment planning system (20). They reported that the dose reduction in CTV is clinically low with <1% of the planned dose. However, the OAR doses were not evaluated because the OAR’s 4D-dose could not be calculated using the isocenter shift method. We were able to assess the 4D-dose distribution of PTV and OARs using DIR.

In the 3D-CRT plan, our results showed that the dose coverage of PTV and the minimum dose to PTV in the 4D-dose distribution were slightly lower than those in the 3D-dose distribution, which may be due to the dose gradient at the PTV’s peripheral part. Mankinen et al. compared the planned dose between VMAT and 3D-CRT for 10 whole-breast irradiation plans at free-breathing (21). Using 4D-dose accumulation, they found that the PTV coverage mainly decreased in areas with steep dose fall-off gradients. The 3D-CRT plan had a steeper dose gradient than the VMAT plan in the area corresponding to the edge of the field around the PTV, which might lead to a significant dose reduction caused by respiratory motions in the 4D-dose distribution of the 3D-CRT plan. However, the difference was ≤0.2 Gy with <1% of the prescribed dose, and the other dosimetric parameters of 3D-CRT were not significantly different between the 3D- and 4D-doses. We confirmed that, in the 3D-CRT plan, the clinical impact of the differences in dose distribution caused by the respiratory changes is clinically negligible. Furthermore, for the VMAT plan, we confirmed that the dosimetric changes in PTV and OARs caused by the respiratory motion are totally negligible. Considering that the dose distribution of VMAT is significantly better than that of 3D-CRT, VMAT should be aggressively introduced into RT for gastric MALT lymphoma (8).

Only a few studies have quantified the gastric respiratory motion of COM. Uchinami et al. assessed the intrafraction gastric motion of COM in 10 patients with stomach lymphomas via 4D-CT imaging at free-breathing (18). Their results showed that the average respiratory motions of the stomach COM in the AP, LR, and SI directions were 0.41 (±0.14), 0.29 (±0.13), and 1.01 (±0.45) cm, respectively. Similar to Uchinami et al.’s results, our findings showed that the stomach CTV COM showed the largest displacement in the SI direction (20).

The current study has some limitations. First, although the expiration phase is practically longer than the inspiration phase, we calculated the 4D-dose distribution via equal weighting for each respiratory phase (22). Second, as we performed planning based on the single 4D-CT imaging, the effects of inter- and intrafractional changes of the structures on dose distribution were not considered. Third, although we evaluated the stomach CTV COM respiratory displacement, we were unable to evaluate the shift position of the CTV contours. Fourth, the interplay effects of VMAT were not considered. However, a previous study has suggested the minimal impact of interplay effect in cases with large irradiated fields or a large number of irradiations, such as gastric MALT lymphoma (23).

Conclusion

In both 3D-CRT and VMAT plans, the difference in the dose distributions produced by the respiratory motion is clinically negligible. Considering that VMAT’s dose distribution is significantly better than that of 3D-CRT, VMAT should be aggressively introduced into RT for patients with gastric MALT lymphoma.

Footnotes

  • Authors’ Contributions

    TM developed the study design; collected, analyzed, and interpreted the data; performed the statistical analysis; and drafted the manuscript. RT developed the study design; collected, analyzed, and interpreted the data; and revised the manuscript. YS developed the study design; performed radiotherapy planning; and collected, analyzed, and interpreted the data. KY, TW, and YK developed the study design and collected and interpreted the data. TM, YF, and NO developed the study design and interpreted the data. All Authors have read and approved the final manuscript.

  • Conflicts of Interest

    The Authors declare that they have no competing interests in relation to this study.

  • Funding

    No funds, grants, or other support was received.

  • Received December 12, 2023.
  • Revision received December 29, 2023.
  • Accepted January 2, 2024.

This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY-NC-ND) 4.0 international license (https://creativecommons.org/licenses/by-nc-nd/4.0).

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Influence of Respiratory Motion on Dose Distribution in Gastric Mucosa-associated Lymphoid Tissue Lymphoma Radiotherapy
TADASHI MATSUMOTO, RYO TOYA, YOSHINOBU SHIMOHIGASHI, KOHSEI YAMAGUCHI, TAKAHIRO WATAKABE, TOMOHIKO MATSUYAMA, YOSHIYUKI FUKUGAWA, YUDAI KAI, NATSUO OYA
Anticancer Research Feb 2024, 44 (2) 687-694; DOI: 10.21873/anticanres.16859
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