Abstract
Background
Radiotherapy (RT) for localized gastric lymphoma requires large margins due to respiratory motion. Breath-hold RT is performed to reduce respiratory motion. However, intrafractional variation (IV) during breath-hold RT has not been fully evaluated. We quantitatively evaluated IV during breath-hold RT for gastric lymphoma.
Methods
Twenty-one patients with localized gastric lymphoma underwent breath-hold RT between 2013 and 2023. They underwent 3–4 computed tomography (CT) simulation scans with breath-holding during the end-expiratory phase of the respiratory cycle. Two radiation oncologists jointly defined a clinical target volume (CTV), and the sum of all CTVs (CTVsum) was defined as the volume covering the CTVs of all CT images. We evaluated CTV changes, displacement of the CTV center, and displacement of each CTV border from the CTVsum. The maximum displacement of the initial breath-hold CT scan (CT1) from the CTVsum was compared with the mean of subsequent breath-hold CT scans (CT2–4) in each direction (anterior–posterior [AP], left–right [LR], superior–inferior [SI]) and across all directions (overall). Factors influencing the maximum overall displacement were assessed using the Mann–Whitney U test (p < 0.05).
Results
Mean CTV was 209 ± 86 cm³, with all patients showing maximum volumetric changes within 4% of the mean CTV. Mean CTV center displacement from the mean center position was 1.6 ± 1.0 mm (AP), 1.1 ± 0.9 mm (LR), and 2.1 ± 1.6 mm (SI). Mean displacement of each CTV border from the CTVsum was 7.5 ± 2.5, 7.2 ± 2.6, 7.2 ± 2.5, and 8.0 ± 2.6 mm for AP, LR, SI, and overall directions, respectively. The displacement of CT1 was significantly larger than that of CT2–4 in all directions (p < 0.001). The overall displacement in patients aged ≥ 70 years was significantly larger than in patients aged < 70 years (10.1 ± 2.5 mm vs. 6.9 ± 2.0 mm; p = 0.01).
Conclusions
Breath-hold RT for gastric lymphoma achieves a small IV, but significantly larger IVs were observed in CT1 than CT2–4 and in elderly patients. Multiple breath-hold CT scans at simulation are recommended to assess the IV, and application of breath-hold RT in elderly patients should be individualized.
Keywords: Gastric lymphoma, Radiotherapy, Breath-hold radiotherapy, Intrafractional variation, Respiratory motion, Target volume
Background
Radiotherapy (RT) plays an important role in the treatment of localized gastric lymphomas, particularly subtypes such as mucosa-associated lymphoid tissue (MALT) lymphoma and diffuse large B-cell lymphoma (DLBCL) [1, 2]. The challenging aspect of RT for gastric lymphoma is the large target volume. The clinical target volume (CTV) is typically defined as the gross tumor volume (GTV) plus the entire gastric volume between the gastroesophageal junction and the distal duodenal bulb. An extra margin is required for the planning target volume (PTV) to account for stomach motion due to deformation and respiratory motion of the stomach [3]. Specifically, respiratory motion is a major source of intrafractional stomach motion [4, 5]. The typical RT field in free breathing RT for gastric MALT lymphoma has been defined by adding a 20-mm margin to the soft-tissue outline of the gastric wall [6].
Intensity-modulated radiation therapy (IMRT) has recently been introduced for RT of gastric lymphoma to enhance the dose concentration to the target volume and minimize radiation exposure to organs at risk [7–9]. Breath-hold techniques have also been used to reduce respiratory motion in high-precision RT [10, 11]. Exhalation breath-hold is widely used, especially for RT of the upper abdomen [12]. Since IMRT has a steep dose gradient, precise localization is essential when using breath-hold techniques. However, intrafractional variation (IV) of breath-hold RT for gastric lymphoma has not been fully investigated. This study quantitatively evaluated the IV of breath-hold RT in patients with gastric lymphoma using images of computed tomography (CT) simulation.
Methods
Patients
This retrospective study was approved by the Institutional Research Ethics Board of our hospital (No. 24091903). Twenty-one consecutive patients with localized gastric lymphoma who underwent RT at our institution between February 2013 and December 2023 were included in this study. All consecutive patients treated during the study period were included in the analysis with no arbitrary exclusions.
CT simulation procedures
All patients were instructed to fast for at least 6 h prior to the CT simulation to reduce stomach volume. CT simulation was performed using a dedicated RT CT scanner (Aquilion Exceed LB, Canon Medical Systems, Tochigi, Japan) with the patient in a supine position with arms raised. To achieve breath-hold conditions, Abches III (Apex Medical, Tokyo, Japan), a nonelectronic, contact-based respiratory monitoring device, was used to ensure that patients reached the same end-expiratory level for each breath-hold during both simulation and treatment [13–15]. Patients were instructed to hold their breath during the end-expiratory phase of the respiratory cycle, which has been reported to result in less intra-breath-hold organ motion than inspiration breath-hold [16]. CT simulation was performed with parameters of 120 kV, automatic exposure control, a gantry rotation time of 1 s, and a slice interval of 3 mm. Each patient underwent 3–4 consecutive CT scans within a single CT simulation to obtain images for treatment planning, with the number of scans (3 or 4) determined by the attending radiation oncologist according to patient factors such as age and performance status.
Treatment
Four-field three-dimensional conformal radiotherapy (3D-CRT) with 10-MV photon beams was used for delivering RT. Each beam was delivered within a single breath-hold (i.e., 4 breath-holds per treatment session). During treatment, breath-holding was monitored using the same Abches III system that was used during simulation. The radiation therapist visually monitored the Abches III pointer and initiated beam delivery once the patient reached and maintained the end-expiratory breath-hold level.
Image analysis
All CT images were exported to the RT planning system (Eclipse version 16.0, Varian Medical Systems, Palo Alto, CA, USA), and all CT images were fused with the initial CT image using a hardware arrangement. Two radiation oncologists with five and nine years of experience jointly delineated the CTV of each breath-hold CT scan by consensus, using the same approach as in the previous studies [17, 18], with fused CT images for reference. CTV was defined as the GTV plus the total gastric volume from the gastroesophageal junction to the distal duodenal bulb, based on the Radiation Therapy Oncology Group consensus guidelines [19]. All GTVs were appropriately included in the CTV. The clinical target volume sum (CTVsum) was defined as the volume necessary to cover the CTVs of all CT images. The IV in this study reflects the combined effect of respiratory motion and peristaltic stomach deformation between breath-holds.
We evaluated the change in CTV, displacement of the CTV center, and displacement of each CTV border from the CTVsum. The CTV was measured on each breath-hold CT scan, and the difference from the per-patient mean CTV was calculated. The CTV center was determined for each image set, and the maximum absolute displacement distances from the mean CTV center position were measured in the anterior–posterior (AP), left–right (LR), and superior–inferior (SI) directions. To evaluate displacement of each CTV border from the CTVsum, regions of interest were generated by isotropically contracting the CTVsum in 1-mm increments in all directions (Fig. 1) [20, 21]. The maximum displacement of each CTV border from the CTVsum was calculated for each of the six directions (anterior, posterior, left, right, superior, and inferior). We also determined the maximum value along each axis (AP, LR, SI) and across all directions (overall). Furthermore, the maximum displacement of the initial breath-hold CT scan (CT1) from the CTVsum was compared with the mean of subsequent breath-hold CT scans (CT2–4) in each direction (AP, LR, SI, and overall).
Fig. 1.
CT simulation images showing the CTV of each breath-hold CT scan (yellow), the CTVsum (magenta), and isotropic contractions of the CTVsum by 3 mm (blue), 5 mm (light green), 10 mm (orange), and 15 mm (beige). Axial (a), sagittal (b), and coronal (c) CT simulation images
Statistical analysis
The Mann–Whitney U test was used to analyze factors influencing the overall displacement of each CTV border from the CTVsum. These factors included age, Eastern Cooperative Oncology Group performance status, histology, stomach volume, and number of breath-hold CT scans. We also used the Friedman test to compare CTV border displacement values between the six directions, and the Wilcoxon signed-rank test to compare the CTV border displacement of CT1 with the mean displacement of CT2–4. Statistical significance was set at p < 0.05. All statistical analyses were performed using JMP Pro 17.2 (SAS Institute, Cary, NC, USA).
Results
Patient and treatment characteristics
Table 1 summarizes patient characteristics. The prescription doses for MALT lymphoma were 30 Gy in 20 fractions for 12 patients and 30.6 Gy in 17 fractions for 2 patients. For DLBCL, the prescription doses were 40.5 Gy in 27 fractions for 3 patients, and 30, 36, 41.4, and 45 Gy in 15, 20, 23, and 30 fractions, respectively, for 1 patient each.
Table 1.
Patient characteristics
| N (%) | ||
|---|---|---|
| Age (years) | Median 63 (range: 36–82) | |
| Sex | Male | 15 (71) |
| Female | 6 (29) | |
| ECOG PS | 0 | 15 (71) |
| 1 | 6 (29) | |
| Histology | MALT lymphoma | 14 (67) |
| DLBCL | 7 (33) | |
| No. of breath-hold CT scans | 3 | 14 (67) |
| 4 | 7 (33) |
ECOG PS: Eastern Cooperative Oncology Group performance status. MALT: Mucosa-Associated Lymphoid Tissue. DLBCL: Diffuse Large B-cell Lymphoma. No.: Number. CT: Computed Tomography
CTV volume changes
The mean CTV across all patients and CT images was 209 ± 86 cm³. Results of CTV changes from the mean CTV are shown in Fig. 2. All patients showed maximum volumetric changes within 4% of the mean CTV.
Fig. 2.
Relative CTV volume (%) of each CT scan compared with the mean CTV for each patient
Displacement of the CTV center and the CTV border
Results of the displacements of the CTV center and the CTV border are shown in Table 2. The mean CTV center displacement from the mean center position in each axial direction was 1.6 ± 1.0 mm for AP, 1.1 ± 0.9 mm for LR, and 2.1 ± 1.6 mm for SI. The mean displacement of each CTV border from the CTVsum was 7.5 ± 2.5 mm, 7.2 ± 2.6 mm, and 7.2 ± 2.5 mm for AP, LR, and SI, respectively. The overall displacement of each CTV border from the CTVsum was 8.0 ± 2.6 mm. The six directions of CTV border displacement showed no significant differences (p = 0.73).
Table 2.
The displacements of the CTV center and the CTV border from the CTVsum
| Mean (mm) | Range (mm) | SD (mm) | ||
|---|---|---|---|---|
| Displacement of CTV center | ||||
| AP | 1.6 | 0.5–3.7 | 1.0 | |
| LR | 1.1 | 0.1–3.3 | 0.9 | |
| SI | 2.1 | 0.4–8.0 | 1.6 | |
| The displacement of each CTV border from the CTVsum | ||||
| A | 5.3 | 1–12 | 2.8 | |
| P | 6.5 | 1–12 | 3.0 | |
| L | 5.6 | 1–12 | 2.5 | |
| R | 6.4 | 2–13 | 2.9 | |
| S | 6.8 | 3–12 | 2.8 | |
| I | 5.4 | 2–12 | 2.3 | |
| AP | 7.5 | 5–12 | 2.5 | |
| LR | 7.2 | 4–13 | 2.6 | |
| SI | 7.2 | 5–12 | 2.5 | |
| Overall | 8.0 | 5–13 | 2.6 |
A: Anterior. P: Posterior. AP: Anterior–Posterior. CTV: Clinical Target Volume. L: Left. R: Right. LR: Left–Right. S: Superior. I: Inferior. SI: Superior–Inferior
Comparison of CT1 with CT2–4
The maximum displacement of each CTV border from the CTVsum was significantly larger for CT1 than for the mean of CT2–4 across all directions (Fig. 3). CT1 showed greater mean displacement than CT2–4 in the AP (7.4 ± 2.6 mm vs. 2.8 ± 2.1 mm, p < 0.001), LR (7.2 ± 2.6 mm vs. 3.0 ± 1.6 mm, p < 0.001), SI (7.2 ± 2.5 mm vs. 3.7 ± 2.6 mm, p < 0.001), and overall directions (8.0 ± 2.6 mm vs. 5.2 ± 2.4 mm, p < 0.001).
Fig. 3.
Comparison of the maximum displacement of each CTV border from the CTVsum between CT1 and CT2–4 in the AP, LR, SI, and overall directions. Blue dots represent individual CT1 values (n = 21), whereas orange dots represent individual CT2–4 values (n = 49). Box plots show the median and interquartile range, with whiskers indicating the minimum and maximum values
Factors influencing the maximum overall displacement of the CTV border from the CTVsum
Results of analyzing factors influencing the maximum overall displacement of the CTV border from the CTVsum are shown in Table 3. Patient age was the only significant factor influencing the displacement. The overall displacement in patients ≥ 70 years of age was significantly larger than that in patients < 70 years (10.1 ± 2.5 mm vs. 6.9 ± 2.0 mm, p = 0.01).
Table 3.
Factors influencing the maximum overall displacement of each CTV border from CTVsum
| N | Mean ± SD (mm) | p-value | |
|---|---|---|---|
| Age (years) | |||
| <70 | 14 | 6.9 ± 2.0 | 0.01 |
| ≥70 | 7 | 10.1 ± 2.5 | |
| ECOG PS | |||
| 0 | 15 | 7.7 ± 2.7 | 0.58 |
| 1 | 6 | 8.5 ± 2.7 | |
| Histology | |||
| MALT | 14 | 8.1 ± 2.9 | 0.73 |
| DLBCL | 7 | 7.6 ± 2.3 | |
| Stomach volume (cm3) | |||
| <200 | 14 | 8.6 ± 2.8 | 0.14 |
| ≥200 | 7 | 6.6 ± 1.6 | |
| No. of breath-hold CT scans | |||
| 3 | 14 | 7.8 ± 2.4 | 0.99 |
| 4 | 7 | 8.3 ± 3.3 |
ECOG PS: Eastern Cooperative Oncology Group performance status. MALT: Mucosa-Associated Lymphoid Tissue. DLBCL: Diffuse Large B-cell Lymphoma. No.: Number. CT: Computed Tomography
Discussion
Our study suggests that the reproducibility of CTV is high under breath-hold conditions. Hirose et al. [22] investigated online adaptive radiation therapy (oART) for gastric MALT lymphoma. Their study included four patients undergoing oART with a breath-hold technique who received 30 Gy in 15 fractions. A total of 120 cone-beam computed tomography (CBCT) scans were analyzed to evaluate intrafractional and interfractional variations in CTV (entire stomach). They evaluated CTV on pretreatment CBCT (CTVpre) and posttreatment CBCT (CTVpost). The mean CTVpre and CTVpost across all fractions were 193.5 ± 25.0 cm³ and 171.9 ± 19.3 cm³, respectively. The CTV under breath-hold conditions in our study was similar to those reported in their study.
Previous studies have reported intrafractional gastric motion based on the center of the CTV under free breathing conditions. Uchinami et al. [5] investigated gastric motion in patients with gastric lymphoma using four-dimensional CT (4D-CT). They evaluated displacement of the CTV center across 10 respiratory phases in 10 patients. They reported mean respiratory-induced displacements of 4.1 ± 1.4 mm in the AP, 2.9 ± 1.3 mm in the LR, and 10.1 ± 4.5 mm in the SI directions. Matsumoto et al. [18] similarly analyzed 10 patients with gastric MALT lymphoma with 4D-CT and reported that mean displacements of the CTV center during respiration were 4.1 ± 1.0 mm in the AP, 3.5 ± 1.9 mm in the LR, 6.7 ± 1.6 mm in the SI direction. In comparison with these previous reports of free breathing conditions, our study confirmed that breath-hold RT yields substantially reduced gastric motion during treatment. Previous studies have reported intrafractional displacements of the gastric border under free breathing conditions. Watanabe et al. [23] investigated intrafractional gastric motion based on the CTV border under free breathing conditions using fluoroscopic imaging of 11 patients. Mean border displacements were 7.1 ± 8.2 mm anteriorly, 6.6 ± 5.8 mm posteriorly, 6.5 ± 6.5 mm to the right, 3.4 ± 2.3 mm to the left, 11.7 ± 8.3 mm superiorly and 11.0 ± 7.1 mm inferiorly. In contrast, our study demonstrated that border displacements of the CTV from the CTVsum under the breath-hold technique were smaller than those under the free breathing technique, especially in the SI direction. Our findings of displacement of the CTV center and border suggest that the use of breath-hold techniques promises smaller IV, results in smaller target volume, and more precise irradiation than conventional free breathing techniques. Additionally, our results showed that displacements of each CTV border from the CTVsum were consistent, 7–8 mm, across all three directions (AP, LR, and SI). This observation indicates that breath-hold RT for gastric lymphoma may allow for uniform margins to cover IV.
Although the overall maximum displacement of each CTV border from the CTVsum was modest, at 7–8 mm, the displacement from the CTVsum was significantly larger for CT1 than for CT2–4 in all directions. Thus, the initial breath-hold CT scan may not adequately represent the typical stomach position, possibly because patients may not yet be fully accustomed to the breath-hold procedure during the initial scan. Therefore, multiple breath-hold CT scans should be acquired at simulation to capture the representative range of IV during breath-hold RT.
Our analysis suggested that elderly patients (≥ 70 years) showed significantly larger IV than younger patients (< 70 years) and elderly patients have less reproducibility of the CTV under breath-hold than younger patients. This observation is consistent with findings reported in other tumor sites. In a prospective observational study, Ahmad et al. [24] analyzed 253 patients with left-sided breast cancer and identified increasing age as a significant predictor of ineligibility for deep-inspiration breath-hold RT. Their results supports the reduced breath-hold reproducibility in elderly patients observed in our study. In our study, the mean overall displacement of each CTV border from the CTVsum was approximately 10 mm in elderly patients, which was similar to the intrafractional gastric motion under free breathing technique reported by Watanabe et al. [23]. This finding suggests that although the breath-hold technique substantially reduces respiratory-induced gastric motion in the general population, its benefit may be attenuated in elderly patients due to reduced breath-hold ability. Moreover, breath-hold RT typically requires a longer treatment time than free breathing RT, which may yield additional physical burden. Therefore, based on findings from multiple breath-hold CT scans at simulation, the application of breath-hold RT for gastric lymphoma in elderly patients should be individualized.
Our study has some limitations. First, this retrospective study was conducted at a single institution with a relatively small sample size. Second, IV was inferred from discrete breath-hold CT scans obtained during simulation rather than during treatment delivery; thus, the measured variation may not fully represent the actual intrafractional variation during treatment. Third, intra–breath-hold organ motion was not assessed. Lens et al. reported that the pancreas moves continuously during end-expiratory breath-holds (mean displacement: 4.2–4.4 mm in the superior–inferior direction), predominantly as a slow drift in the superior direction resulting from a gradual decrease in lung volume during breath-holding [16]. These findings should be considered when determining planning margins. Fourth, the observed displacements reflect the combined effect of inter–breath-hold positional variation and peristaltic stomach deformation, which could not be separately quantified. Fifth, although our study examined IV during breath-hold RT for gastric lymphoma, we did not investigate interfractional variations. Therefore, we cannot recommend an adequate PTV margin for RT planning. Similarly, we cannot comment on the dosimetric or survival benefits of the breath-hold technique.
The present cohort was treated with 3D-CRT. Nonetheless, our findings on IV remain relevant, given the increasing use of IMRT for gastric lymphoma, where steep dose gradients demand precise target localization.
Conclusions
Our study demonstrated that breath-hold RT for gastric lymphoma achieved a small IV with consistent CTV and minimal displacement of the CTV center. However, the displacement of the CTV border from the CTVsum was significantly larger for CT1 than for CT2–4; thus, the initial scan may not adequately represent the typical stomach position. Additionally, larger IVs were observed in elderly compared with younger patients. Therefore, multiple breath-hold CT scans at simulation are recommended to assess the IV, and application of breath-hold RT in elderly patients should be individualized.
Acknowledgements
None.
Abbreviations
- 3D-CRT
Three-dimensional conformal radiotherapy
- 4D-CT
4D computed tomography
- AP
Anterior–posterior
- CBCT
Cone-beam computed tomography
- CT
Computed tomography
- CT1
The initial breath-hold CT scan
- CT2–4
Subsequent breath-hold CT scans
- CTV
Clinical target volume
- CTVpre
Clinical target volume on pretreatment
- CTVpost
Clinical target volume on posttreatment
- CTVsum
Volume necessary to cover the CTVs of all CT images
- DLBCL
Diffuse large B-cell lymphoma
- GTV
Gross tumor volume
- IMRT
Intensity-modulated radiation therapy
- IV
Intrafractional variation
- LR
Left–right
- MALT
Mucosa-associated lymphoid tissue
- oART
online adaptive radiation therapy
- PTV
Planning target volume
- RT
Radiotherapy
- SI
Superior–inferior
Author contributions
SM and RT were responsible for the study design, collection, analysis, and interpretation of data, statistical analysis, and drafting of the manuscript. YT was responsible for the analysis and interpretation of data and statistical analysis. MN, AE, DN, JN, and TN were responsible for the collection and interpretation of data. TY was responsible for the study design and interpretation of data. All authors have read and approved the final manuscript.
Funding
None.
Data availability
The data supporting the findings of this study are not publicly available as they were used in this study under license. However, the data are available from the authors upon reasonable request and with permission from the Clinical Research Ethics Committee of Nagasaki University Hospital.
Declarations
Ethics approval and consent to participate
This study received full approval from the Clinical Research Ethics Committee of Nagasaki University Hospital (No. 24091903) and it conformed to the principles of the Helsinki Declaration. The consent requirement was waived due to the retrospective nature of the study.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Footnotes
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The data supporting the findings of this study are not publicly available as they were used in this study under license. However, the data are available from the authors upon reasonable request and with permission from the Clinical Research Ethics Committee of Nagasaki University Hospital.