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Systematic review| Volume 123, ISSUE 3, P346-354, June 2017

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Comparison of particle beam therapy and stereotactic body radiotherapy for early stage non-small cell lung cancer: A systematic review and hypothesis-generating meta-analysis

  • Alexander Chi
    Correspondence
    Corresponding authors at: Department of Radiation Oncology, Shanghai Proton and Heavy Ion Center, Shanghai, China (A. Chi). Department of Biostatistics, School of Public Health, West Virginia University, Morgantown, WV, USA (S. Wen).
    Affiliations
    Department of Radiation Oncology, Shanghai Proton and Heavy Ion Center, China
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  • Haiquan Chen
    Affiliations
    Department of Thoracic Surgery, Fudan University Shanghai Cancer Center, China
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  • Sijin Wen
    Correspondence
    Corresponding authors at: Department of Radiation Oncology, Shanghai Proton and Heavy Ion Center, Shanghai, China (A. Chi). Department of Biostatistics, School of Public Health, West Virginia University, Morgantown, WV, USA (S. Wen).
    Affiliations
    Department of Biostatistics, School of Public Health, West Virginia University, Morgantown, USA
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  • Haijuan Yan
    Affiliations
    Department of Biostatistics, School of Public Health, West Virginia University, Morgantown, USA
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  • Zhongxing Liao
    Affiliations
    Department of Radiation Oncology, MD Anderson Cancer Center, Houston, USA
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Published:May 22, 2017DOI:https://doi.org/10.1016/j.radonc.2017.05.007
Comparison of particle beam therapy and stereotactic body radiotherapy for early stage non-small cell lung cancer: A systematic review and hypothesis-generating meta-analysis
Previous ArticleFirst clinical investigation of a 4D maximum likelihood reconstruction for 4D PET-based treatment verification in ion beam therapy
Next ArticleVerifying tumor position during stereotactic body radiation therapy delivery using (limited-arc) cone beam computed tomography imaging

      Abstract

      Purpose

      To assess hypo-fractionated particle beam therapy (PBT)’s efficacy relative to that of photon stereotactic body radiotherapy (SBRT) for early stage (ES) non-small cell lung cancer (NSCLC).

      Methods

      Eligible studies were identified through extensive searches of the PubMed, Medline, Google-scholar, and Cochrane library databases from 2000 to 2016. Original English publications of ES NSCLC were included. A meta-analysis was performed to compare the survival outcome, toxicity profile, and patterns of failure following each treatment.

      Results

      72 SBRT studies and 9 hypo-fractionated PBT studies (mostly single-arm) were included. PBT was associated with improved overall survival (OS; p = 0.005) and progression-free survival (PFS; p = 0.01) in the univariate meta-analysis. The OS benefit did not reach its statistical significance after inclusion of operability into the final multivariate meta-analysis (p = 0.11); while the 3-year local control (LC) still favored PBT (p = 0.03).

      Conclusion

      Although hypo-fractionated PBT may lead to additional clinical benefit when compared with photon SBRT, no statistically significant survival benefit from PBT over SBRT was observed in the treatment of ES NSCLC in this hypothesis-generating meta-analysis after adjusting for potential confounding variables.

      Keywords

      Lung cancer is the most common cancer and the leading cause of cancer-related deaths worldwide [

      Worldwide cancer statistics. Cancer Research UK, www.cancerresearchuk.org/health-professional/cancer-statistics/worldwide-cancer, accessed in July, 2016.

      ]. Non-small cell lung cancer (NSCLC), which represents the majority of lung cancer diagnosed, often presents in late stages. Low-dose (LD) CT screening of patients who are at a high risk to develop lung cancer has been associated with a decrease in lung cancer related mortality and a high specificity in selected studies [
      • The National Lung Screening Trial Research Team
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      Occurrence and lung cancer probability of new solid nodules at incidence screening with low-dose CT: analysis of data from the randomised, controlled NELSON trial.
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      ]. Its clinical adaptation in the high-risk population has caused an increase in the number of patients diagnosed with stage I NSCLC in recent years [
      • The National Lung Screening Trial Research Team
      Reduced lung-cancer mortality with low-dose computed tomographic screening.
      N Engl J Med. 2011; 365: 395-409
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      ]. Early-stage (ES) NSCLC has traditionally been treated with surgery in operable patients. As an alternative, excellent clinical outcome following high dose irradiation delivered with stereotactic body radiotherapy (SBRT) has been observed in inoperable patients with ES, lymph node negative, NSCLC [
      • Chi A.
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      ]. This treatment technique is also known as stereotactic ablative radiotherapy (SABR). An ablative dose is delivered to the tumor with SBRT over one to two weeks. This is administered under daily image guidance to ensure accurate tumor localization and maximal sparing of the surrounding normal tissue. SBRT has been quickly adopted into clinical practice worldwide. Its efficacy was found to be potentially comparable to surgery in selected patients [
      • Onishi H.
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      • Gomi K.
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      Stereotactic body radiotherapy (SBRT) for operable stage I non-small-cell lung cancer: can SBRT be comparable to surgery?.
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      • Chang J.
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      ]. As more patients are diagnosed with ES NSCLC through LD-CT screening, high dose irradiation with precision, such as SBRT, may become increasingly considered for this disease. However, SBRT is not without limitations. For example, its application is still limited by tumor location with severe toxicity more frequently encountered in patients with centrally located lesions [
      • Chi A.
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      ]. This problem may be mitigated by increasing dose fractionation because of photons’ physical characteristics. However, tumor proximity to critical thoracic structures still prohibits the utility of SBRT in many patients due to the risk of severe toxicity associated high doses to these structures if a therapeutic dose were to be delivered. Also, photon SBRT poses great challenges in the delivery of subsequent high dose re-irradiation for loco-regional recurrence in many patients as a result of the high dose already delivered to critical thoracic organs during the first course of treatment. As an emerging technology, particle beam (proton and heavy ions, such as carbon ions) therapy (PBT) possesses unique physical properties that allow the irradiation of tumors at any depth within the body with a very sharp dose gradient at the distal edge of the tumor target [

      Linz U. Physical and biological rationale for using ions in therapy, Ion Beam Therapy: Fundamentals, Technology, Clinical Applications. Linz U, Ed., Springer, Heidelberg, Dordrecht, London, New York, 2012; 45–59.

      ]. This may greatly decrease the dose to the healthy tissues surrounding the tumor in the setting of high dose irradiation in comparison with photon SBRT. Heavy ions, such as carbon ions, also have a biological advantage over photons due to the higher probability of tumor DNA damage associated with their high linear energy transfer (LET). In recent years, more facilities have been delivering PBT for the treatment of ES NSCLC. In this comprehensive critical review and hypothesis-generating meta-analysis, we aim to analyze and compare the efficacy of hypo-fractionated PBT, which is delivered with highly-advanced technology, with that of photon SBRT, a relatively more mature technique that has been in clinical use for over a decade, in the treatment of ES NSCLC.

      Methods

      Search strategy and selection criteria

      A systematic search was conducted in PubMed, Medline, Google-scholar, and the Cochrane library for studies published between January 2000, and June 2016. The subject heading “non-small cell lung cancer/ carcinoma” was combined with the following terms: “early stage”, “stage I”, “T1”, “T2”, “stereotactic body radiation therapy”, “stereotactic body radiotherapy”, “stereotactic ablative radiotherapy”, “SBRT”, “SABR”, “hypo-fractionated radiotherapy”, “particle beam therapy”, “proton therapy”, “carbon ion therapy”, “carbon ion radiotherapy”, and “carbon ion radiation therapy”. Relevant articles, abstracts, and review articles were selected and reviewed. The references from these sources were searched for additional studies. Proceedings of the annual meetings of the American Society of Radiation Oncology, American Society of Clinical Oncology, and the European Society of Radiotherapy & Oncology from 2000 onward were manually searched for relevant abstracts, then a search for a fully published manuscript was done. The Physician Data Query (PDQ) clinical trials database was searched for relevant ongoing trials. The last search was conducted on July 1, 2016.
      Only studies published in English in peer-reviewed journals were included. Eligible studies include prospective or retrospective studies of SBRT or SABR, and hypo-fractionated PBT, such as proton therapy and carbon ion therapy, as definitive treatment for ES NSCLC (T1, T2, or T3, N0, M0 per the 7th edition of cancer staging by the American Joint Committee on Cancer (AJCC)). Only the latest study with the most comprehensive report of clinical outcome and treatment toxicity was selected when multiple studies on the same patient population from the same institution were found. Multiple reports from the same institution were included if the patient populations were from different time periods, treated differently, or the reports on the same patient population complement each other in data reporting. The search was conducted based on the Preferred Reporting Items for Systematic Reviews and Meta-analysis (PRISMA) guidelines [
      • Liberati A.
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      • Mulrow C.
      • Gøtzsche P.C.
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      ], and a structured literature search schema was followed (Suppl. Fig. 1).

      Data extraction

      Studies were extracted independently by two investigators. All relevant characteristics, such as first author, publication year, country, study design, age, sample size, tumor stage, follow up period, clinical outcome (including patterns of failure and survival data), and treatment related toxicity, were collected. For each study, the radiation dose fractionation regimen used was recorded. For survival endpoints, 1, 2, 3, 4, and 5 year data were collected when available. Local control was defined as freedom from any local progression. Survival data were extracted from Kaplan–Meier survival curves when survival rates were not explicitly stated. The biologically effective dose (BED10) for tumor was calculated based on the linear-quadratic equation: BED10 = D [1 + d/(α/β)], where D and d represents the total and fractional radiation dose. α/β for tumor equals to 10 Gy−1.

      Statistical analysis

      The clinical outcomes of interest include local control, overall survival, progression-free survival at 1, 2, 3, 4 and 5 years and treatment related toxicity. Descriptive statistics and exploratory data analysis were used to summarize the data, including summary tables, box-plots, proportions, mean, median, and range. Summary estimates of event proportion, and relative risk (RR) were estimated from the available data at each time point, using the weighted regression model, and the random-effects model/mixed-effects model (Supplementary material) [
      • Seber G.A.F.
      Linear regression analysis.
      Wiley, New York1977
      ,
      • Arends L.R.
      • Hunink M.G.M.
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      Meta-analysis of summary survival data.
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      ]. Continuous data such as tumor size and median follow-up were evaluated using weighted mean with 95% confidence intervals (CI). Dichotomous data such as adverse effects were summarized using proportion and relative risk with 95% CI. Forest plots were used to evaluate relative risk on local control and 3-year survival between two conditions such as T1 vs. T2 groups, where 95% confidence intervals for RR in each study were represented by horizontal lines and the point estimate by a square. The height of each square is inversely proportional to the standard error of the estimate. The summary RR is represented by a diamond with horizontal limits at the 95% confidence interval and width inversely proportional to its standard error. A multivariate meta-regression model was used to assess treatment effect, including covariates, such as patient/tumor characteristics, and treatment modality, to account for population heterogeneity. Data analysis was performed using the meta-analysis package “meta” [
      • Schwarzer G.
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      ] and statistical software R (version 3.31, R Foundation, Vienna, Austria).

      Results

      Study selection and characteristics

      The study selection process is shown in Suppl. Fig. 1. Among 501 relevant publications on SBRT and 113 relevant publications on PBT, 205 full text articles for SBRT and 19 full text articles for hypo-fractionated PBT (proton and carbon ion therapy) were assessed for eligibility. Of these, 72 studies on photon SBRT and 9 studies on PBT for ES NSCLC were selected [
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