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ORIGINAL ARTICLE
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Adaptive radiation therapy (art) for patients with limited-stage small cell lung cancer (LS-SCLC): A dosimetric evaluation


 Department of Radiation Oncology, University of Health Sciences, Gulhane Medical Faculty, Ankara, Turkey

Date of Submission30-Jan-2020
Date of Decision30-Apr-2020
Date of Acceptance08-Jun-2020
Date of Web Publication14-Oct-2022

Correspondence Address:
Omer Sager,
Department of Radiation Oncology, University of Health Sciences, Gulhane Medical Faculty, Ankara
Turkey
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/ijc.IJC_73_20

  Abstract 


Background: Adaptive radiation therapy (ART) refers to redesigning of radiation therapy (RT) treatment plans with respect to dynamic changes in tumor size and location throughout the treatment course. In this study, we performed a comparative volumetric and dosimetric analysis to investigate the impact of ART for patients with limited-stage small cell lung cancer (LS-SCLC).
Methods: Twenty-four patients with LS-SCLC receiving ART and concomitant chemotherapy were included in the study. ART was performed by replanning of patients based on a mid-treatment computed tomography (CT)-simulation which was routinely scheduled for all patients 20–25 days after the initial CT-simulation. While the first 15 RT fractions were planned using the initial CT-simulation images, the latter 15 RT fractions were planned using the mid-treatment CT-simulation images acquired 20–25 days after the initial CT-simulation. In order to document the impact of ART, target and critical organ dose-volume parameters acquired from this adaptive radiation treatment planning (RTP) were compared with the RTP based solely on the initial CT-simulation to deliver the whole RT dose of 60 Gy.
Results: Statistically significant reduction was detected in gross tumor volume (GTV) and planning target volume (PTV) during the conventionally fractionated RT course along with statistically significant reduction in critical organ doses with incorporation of ART.
Conclusion: One-third of the patients in our study who were otherwise ineligible for curative intent RT due to violation of critical organ dose constraints could be treated with full dose irradiation by use of ART. Our results suggest significant benefit of ART for patients with LS-SCLC.


Keywords: Adaptive radiation therapy, computed tomography-simulation, limited-stage small cell lung cancer
Key Message: Adaptive radiation therapy offers significant reduction in critical organ doses and may improve treatment outcomes for patients with limited-stage small cell lung cancer.



How to cite this URL:
Sager O, Dincoglan F, Demiral S, Uysal B, Gamsiz H, Ozcan F, Colak O, Elcim Y, Gundem E, Dirican B, Beyzadeoglu M. Adaptive radiation therapy (art) for patients with limited-stage small cell lung cancer (LS-SCLC): A dosimetric evaluation. Indian J Cancer [Epub ahead of print] [cited 2022 Dec 2]. Available from: https://www.indianjcancer.com/preprintarticle.asp?id=358503





  Introduction Top


Lung cancer is a global health concern as the leading cause of cancer-related mortality.[1],[2] Although accounting for approximately 14% of all lung cancers, small cell lung cancer (SCLC) constitutes the deadliest form with the worst prognosis.[3],[4],[5],[6] With its short doubling time and high-growth fraction, SCLC presents with widespread metastases in the majority of patients following an aggressive clinical course.[3],[4],[5],[6] Nevertheless, approximately one-third of the patients suffer from limited disease confined to the chest at diagnosis with a more favorable prognosis compared to patients with extensive disease.[5],[6] Although most patients succumb to their disease with a limited lifespan, SCLC responds well to both chemotherapy and radiotherapy (RT).[6] The role of RT has been well-established in SCLC management.[6] Addition of thoracic RT to chemotherapy has been found to achieve improved local control and overall survival on two meta-analyses, and multimodality management including chemotherapy with concurrent RT has been the current standard of care for patients with limited-stage SCLC (LS-SCLC).[7],[8] A systematic review focusing on timing of RT for LS-SCLC revealed that early thoracic RT within 9 weeks of chemotherapy commencement improved survival.[9]

While there is consensus on the utility of early thoracic RT concomitant with a platinum-based chemotherapy regimen for LS-SCLC management, optimal RT dose and fractionation has yet to be defined. Various dose-fractionation schemes have been considered to achieve improved local control and survival outcomes. A standard RT dose-fractionation scheme for LS-SCLC is based on the intergroup trial by Turrisi et al. which demonstrated the superiority of twice-daily over once-daily fractionation with 45 Gy RT dose in both treatment arms.[10] However, nearly one-third of patients in the twice-daily RT group suffered from grade 3–4 esophagitis, and the study has been criticized based on the insufficient and radiobiologically inequivalent dose in the once-daily RT arm.[10] In this context, dose escalation to ≥60 Gy with conventional fractionation offers a viable alternative to hyperfractionated Turrisi regimen with encouraging treatment results and remains to be widely practiced worldwide.[11],[12],[13],[14],[15],[16],[17],[18]

The delivery of high-RT doses may potentially improve treatment outcomes for patients with LS-SCLC due to a dose–response relationship.[17],[18] However, the delivery of higher RT doses to the target volume should be accomplished without violation of critical organ dose constraints. Several strategies have been utilized to achieve this goal including image-guided radiation therapy (IGRT), intensity modulated radiation therapy (IMRT), respiratory motion management, and adaptive radiation therapy (ART). Given the encouraging results with ART in the management of various cancers, it may serve as a viable therapeutic approach for patients receiving concomitant chemoradiotherapy for LS-SCLC in view of the radiosensitivity and chemosensitivity of SCLC. The concept of ART has been introduced by Yan et al.[19] as a viable strategy for redesignation of RT treatment plans with respect to specific and dynamic changes in tumor size and location throughout the treatment course. Studies on ART for lung cancer management mostly include patients with NSCLC.[20],[21],[22],[23],[24],[25],[26],[27] There is paucity of data regarding the utility of ART for patients with LS-SCLC exclusively, which may partly be due to the rarity of LS-SCLC comprising approximately 5% of all lung cancers.[3],[4],[5],[6] Nevertheless, few studies, case reports, and also studies including patients with both NSCLC and SCLC include data on ART for patients with LS-SCLC.[23],[24],[25],[26],[27],[28],[29],[30] Data from these few studies suggest improved management of patients with ART by virtue of reduced normal tissue exposure which may allow for dose escalation to optimize tumor control.[23],[24],[25],[26],[27],[28],[29],[30]

In this study, we investigate the benefits of incorporating ART in management of LS-SCLC using the primary outcome measures of tumor shrinkage and normal tissue sparing. A homogeneous group of LS-SCLC patients treated with ART using a uniform dose-fractionation schedule and concomitant chemotherapy are evaluated for target volume changes during the course of irradiation, and dosimetric consequences of the adaptive treatment strategy in terms of doses to the critical organs including the heart, lungs, esophagus, and the spinal cord are assessed with statistical analysis. Clinical implications of this contemporary treatment approach are addressed in light of the volumetric and dosimetric results with focus on the potential of ART in enabling administration of curative intent RT for patients with unfavorable critical organ dosimetry at the outset.


  Methods Top


Twenty-four patients with LS-SCLC receiving ART and concomitant chemotherapy were included in the study. Written informed consents of all patients were taken before treatment with institutional tumor board approval at our tertiary cancer center, and the study was performed in compliance with the Declaration of Helsinki principles and its later amendments. All patients had a histopathological diagnosis of SCLC and were referred for concomitant chemoradiotherapy after thorough evaluation based on performance status, blood chemistry, and imaging data including computed tomography (CT) and positron emission tomography (PET) scans. No patients had prior chest RT or surgical resection of their tumor. RT dose was 60 Gy in 30 fractions for all patients starting with the first or second cycle of platinum-based chemotherapy. Results were stratified based on if RT was received with first or second cycle of chemotherapy. CT-simulations for radiation treatment planning (RTP) were performed at CT-simulator (GE Lightspeed RT, GE Healthcare, Chalfont St. Giles, UK) with optimal immobilization of the patients using a Wing-Board (CIVCO, Kalona, IA, USA). Acquired images with 3.75–5 mm slice thickness at CT-simulation were transferred to the contouring workstation via the network. Advantage Sim MD simulation and localization software (Advantage SimMD, GE, UK) was used for delineation of target volumes and critical organs including the lungs, spinal cord, heart, and esophagus. Delineation of target volumes and critical organs was performed by the same physician at the same window level settings to improve consistency and concordance. After contouring was completed, structure sets were sent to the planning workstation via the network.

ART was performed by replanning of patients based on a mid-treatment CT-simulation which was routinely scheduled for all patients 20–25 days after the initial CT-simulation. While the first 15 RT fractions were planned using the initial CT-simulation images, the latter 15 RT fractions were planned using the mid-treatmet CT-simulation images acquired 20–25 days after the initial CT-simulation. In order to document the dosimetric impact of ART, target and critical organ dose-volume parameters acquired from this adaptive RT planning (RTP) were compared with the RTP based solely on the initial CT-simulation to deliver the whole RT dose of 60 Gy. RTP was performed by the same physicist using PrecisePLAN (Elekta, UK) Treatment Planning System with identical beam organization in both RT plans.

Gross tumor volume (GTV) consisted of the macroscopically visible disease and involved lymph nodes (with a short axis diameter of larger than 1 cm) on CT-simulation images. Bronchoscopy and/or mediastinoscopy findings along with recent imaging data of the patients including CT and PET scans were used in tailoring of target volume delineation. Clinical target volume (CTV) was generated by isotropical expansion of the GTV by 10 mm to account for microscopic tumor extentions, and CTV contouring was edited to respect anatomical boundaries. Margins added to the CTV to generate the planning target volume (PTV) were 8 mm in the craniocaudal direction, and 5 mm in the mediolateral and anteroposterior directions. Target volumes along with critical organ dose-volume parameters including mean lung dose (MLD), lung volume receiving ≥20 Gy (V20), mean esophageal dose (MED), mean heart dose (MHD), and spinal cord maximum doses in both RTPs of each patient were assessed to document volumetric changes during the conventionally fractionated RT course and to investigate the dosimetric impact of ART. Analysis of data was performed by using Statistical Package for the Social Sciences, version 15.0 (SPSS, Inc., Chicago, IL) software with the level of significance set at P < 0.05.


  Results Top


A total of 24 patients (17 men, 7 women) receiving ART and concomitant chemotherapy for LS-SCLC were assessed. Patient, tumor, and treatment characteristics are shown in [Table 1]. Median age was 63 (range: 44–74) years. RT dose was 60 Gy for all patients. Out of the total 30 RT fractions, RTP was based on the initial CT-simulation for the first 15 RT fractions and mid-treatment CT-simulation for the latter 15 RT fractions. Median time interval between the 2 CT-simulations was 24 (range: 20-25) days.
Table 1: Patient, tumor, and treatment characteristics

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RT was started with the first cycle of platinum-based chemotherapy for 9 (37.5%) patients and with the second chemotherapy cycle for 15 (62.5%) patients. Volumetric and dosimetric comparison of dose-volume parameters acquired from 2 RTPs of the patients based on the initial CT-simulation and mid-treatment CT-simulation for ART are shown in [Table 2] with the results stratified based on if RT was received with first or second cycle of chemotherapy. Median volume of GTV and PTV was 187.25 (range: 72.4–432.7) cc and 607.45 (range: 299.3-1139.5) cc, respectively at initial CT-simulation. Median volume of GTV and PTV was 55.3 (range: 45.7-102.9) cc and 324.1 (range: 238-468.2) cc, respectively at the mid-treatment CT-simulation. Median decrease in GTV and PTV volumes was 66.99% (range: 27–82%) and 44.37% (range: 17–65%), respectively both with statistical significance (P < 0.05).
Table 2: Volumetric and dosimetric comparison of dose-volume parameters acquired from 2 RTPs of the patients based on the initial CT-simulation and mid-treatment CT-simulation for ART

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Median MLD and V20 was 1809 (range: 985-2279) cGy and 31.25% (range: 16–38%), respectively at initial CT-simulation. Median MLD and V20 was 1499 (range: 738-1950) cGy and 28.35% (range: 14.3–34%), respectively at the mid-treatment CT-simulation. Median decrease in MLD and V20 was 14.88% (range: 7–48%) and 10.5% (range: 7–17%), respectively both with statistical significance (P < 0.05).

Median MHD was 970.5 (range: 70-2490) cGy and 696.5 (range: 59-2116) cGy at initial CT-simulation and at the mid-treatment CT-simulation, respectively. Median decrease in MHD was 23.4% (range: 8–44%), with statistical significance (P < 0.05).

Median MED was 1758 (range: 103-3356) cGy and 968.5 (range: 88-2665) cGy at initial CT-simulation and at the mid-treatment CT-simulation, respectively. Median decrease in MED was 37.79% (range: 12–47%), with statistical significance (P < 0.05).

Median spinal cord maximum dose was 4869 (range: 305-4970) cGy and 3229.5 (range: 246-4675) cGy at initial CT-simulation and at the mid-treatment CT-simulation, respectively. Median decrease in spinal cord maximum dose was 29.1% (range: 4–49%), with statistical significance (P < 0.05).

[Figure 1] and [Figure 2] shows axial planning CT images of a patient acquired at initial CT-simulation and mid-treatment CT-simulation after 3 weeks for ART, respectively indicating GTV shrinkage during RT for LS-SCLC.
Figure 1: Axial planning computed tomography (CT) images of a patient acquired at initial CT-simulation

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Figure 2: Axial planning computed tomography (CT) images of the same patient acquired at mid-treatment CT-simulation after 3 weeks for adaptive radiation therapy, indicating gross tumor volume shrinkage during radiation therapy for limited-stage small cell lung cancer

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  Discussion Top


Dosimetric results in this study reveal that ART by use of a mid-treatment CT-simulation scheduled 20–25 days after the initial CT-simulation for patients with LS-SCLC improves critical organ sparing through exploiting the advantage of target volume shrinkage during the conventionally fractionated RT course [Table 2]. Several studies have reported the association between dose-volume parameters and RT-induced toxicity.[31],[32],[33] As a rule of thumb, normal tissue exposure should be minimized for an improved toxicity profile and potential for dose escalation. ART may be well-suited for LS-SCLC given the early response to RT and chemotherapy. ART for NSCLC has been extensively addressed in the literature.[20],[21],[22],[23],[24],[25],[26],[27] However, a few studies, case reports, and also studies including patients with both NSCLC and SCLC include data on ART for patients with LS-SCLC.[23],[24],[25],[26],[27],[28],[29],[30] Relative paucity of data on ART for LS-SCLC may possibly be due to the rarity of LS-SCLC comprising approximately 5% of all lung cancers.[3],[4],[5],[6] In this context, our study adds to the literature by demonstrating improved dosimetric results with ART. Potential clinical implications may be inferred to achieve a very pertinent goal of contemporary lung cancer RT which is reduced normal tissue exposure through more precisely focused irradiation for an improved therapeutic ratio.

Repeat CT-simulation for ART has been scheduled 20–25 days after the initial CT-simulation in our study since most of tumor shrinkage occurs during the first weeks of RT.[26],[30] The magnitude of GTV shrinkage may show individual diversities, and these differential changes in GTV during the course of RT may be explained with differences among patient, tumor, and treatment characteristics including timeframe of measurements, intrinsic radiosensitivity, target volume definition, fractionation patterns, and delivered total RT doses with sequential or concurrent chemotherapy regimens.[26],[30],[34] Magnitude of shrinkage in tumor volume has been suggested as a prognostic factor of treatment outcome for patients receiving chemoradiotherapy for LS-SCLC.[34]

In the study by Elsayad et al.[26] assessing cone beam CT guided RT for lung cancer, 6 patients (8.5%) out of the total 71 patients had LS-SCLC while other patients had extensive stage small cell lung cancer (ES-SCLC) or NSCLC. Median total RT dose was 54 Gy (range: 30–72 Gy) delivered using a median fraction dose of 1.8 Gy (range: 1.8–3 Gy) over a median treatment time of 45 days (range: 7–75 days).[26] Mean and median GTV reduction was 46% and 36%, respectively for patients with SCLC.[26] Visual volume reduction was found to be correlated with the number of acquired cone beam CT scans and also with timing of chemotherapy administration.[26] Compared to patients not receiving chemoradiotherapy, volumetric, and/or intrathoracic changes were more commonly detected in patients receiving chemoradiotherapy.[26] Also, patients with more advanced disease stages had increased number of volumetric changes compared to patients with earlier stage lung cancer.[26]

In the study by Yee et al.[30] evaluating temporal lung tumor volume changes in SCLC patients undergoing chemoradiotherapy, 104 CT scans of 10 patients acquired at different time points were analyzed. Median prescribed chest RT dose was 50 (range: 26-62) Gy delivered by either conventional fractionation (2 Gy per fraction) or hypofractionation (2.48 Gy per fraction) over a median RT treatment time of 25 (range: 13-25) days.[30] Median shrinkage in GTV was 52.8% (range: 13.3–83.6%) with the majority of shrinkage occurring by the end of initial week of RT.[30]

Inclusion of patients with different subtypes of lung cancer having different disease stages and diverse disease extents and the use of different dose-fractionation schemes and total RT doses may potentially affect treatment outcome assessments in studies of ART for lung cancer. In this context, a strength of our study may include focusing on a selected group of LS-SCLC patients for whom curative intent RT was delivered using a uniform dose-fractionation scheme and total dose. However, several limitations should also be acknowledged such as the absence of a control group treated without ART and absence of data on clinical outcome measures such as local control, survival, and toxicity assessment.

Nevertheless, our study aimed at investigating the benefits of incorporating ART in management of LS-SCLC using the primary outcome measures of tumor shrinkage and normal tissue sparing. Substantial tumor shrinkage occurred during RT with a median reduction of 66.99% in GTV and 44.37% in PTV. Adaptation of treatment volumes with incorporation of ART resulted in improved normal tissue sparing with statistical significance [Table 2]. Results of our study which reveal significant benefit of ART may have several important and clinically meaningful implications particularly for management of LS-SCLC patients who are considered ineligible for RT with curative intent due to violation of critical organ dose constraints, which has not been the focus of previous studies. As a notable finding of our study, ART by use of the mid-treatment CT-simulation has allowed for treating one-third of the study group with full dose RT to 60 Gy while respecting dose-volume constraints. These 8 patients would be ineligible for curative intent irradiation due to unfavorable critical organ dosimetry at the outset. Despite the absence of clinical outcome data for these patients, delivery of full dose irradiation by ART with curative intent may potentially translate into improved therapeutic results for this patient group. In this context, another merit of ART may be exploited by providing an opportunity for selected patients to be irradiated to curative RT doses. Given the typically high disease burden in patients presenting with SCLC, utilization of ART may be considered as a viable therapeutic strategy for administration of curative intent RT.

Although ART may offer several benefits in terms of exploiting the advantage of tumor shrinkage for improved normal tissue sparing and potential for dose escalation, there have been concerns regarding the risk of undertreatment of microscopic disease.[35] Clinical significance of tumor shrinkage without documentation of histologic tumor clearance has been questioned with suggestions against the use of reduced treatment fields with respect to changes in tumor volume during the course of irradiation.[35] On the contrary, Ramella et al.[22] reported a low rate of marginal failure in the prospective LARTIA trial assessing local control and toxicity of ART for locally advanced NSCLC. The authors concluded that reduced toxicity and low rate of marginal failures rendered the adaptive approach a modern option for future randomized studies.[22] Moreover, another study by Guckenberger et al.[23] revealed that adaptation of RT to the shrinking GTV did not compromise coverage of suspected microscopic disease and ART also had the potential to increase tumor control probability. While the concept of ART should be thoroughly investigated in randomized controlled trials for validation before widespread clinical use, it may be pertinent to consider that the rationale of using post-chemotherapy volumes in LS-SCLC patients may judiciously be extrapolated to irradiate a limited target volume after a few initial RT fractions for the same patient group.[36],[37]

In conclusion, our data suggest significant benefit of ART for patients with LS-SCLC. Substantial shrinkage of GTV during the first weeks of conventionally fractionated RT resulted in improved critical organ sparing with ART. One-third of the patients in our study who were otherwise ineligible for curative intent RT due to violation of critical organ dose constraints could be treated with full dose irradiation by use of ART. Although there is room for improvement, the use of ART may be considered for LS-SCLC patients otherwise deemed ineligible for curative RT due to violation of dose volume constraints. Shrinkage of GTV during the conventionally fractionated RT course may be exploited by use of a mid-treatment CT-simulation for the latter part of treatment in an attempt to achieve reduced normal tissue exposure for an improved therapeutic ratio. ART strategy may have potential clinical implications for dose escalation and reduced adverse RT effects despite the need for further supporting evidence.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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    Figures

  [Figure 1], [Figure 2]
 
 
    Tables

  [Table 1], [Table 2]



 

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