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Japanese Journal of Clinical Oncology Advance Access originally published online on February 3, 2009
Japanese Journal of Clinical Oncology 2009 39(3):151-157; doi:10.1093/jjco/hyn158
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© The Author (2009). Published by Oxford University Press. All rights reserved

Prediction of Radiation Pneumonitis Following High-dose Thoracic Radiation Therapy by 3 Gy/fraction for Non-small Cell Lung Cancer: Analysis of Clinical and Dosimetric Factors

Dongryul Oh, Yong Chan Ahn, Hee Chul Park, Do Hoon Lim and Youngyih Han

Department of Radiation Oncology, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Republic of Korea

For reprints and all correspondence: Yong Chan Ahn, Department of Radiation Oncology, Samsung Medical Center, Sungkyunkwan University School of Medicine, 50 Ilwon-dong, Gangnam-gu, Seoul 135-710, Republic of Korea. E-mail: ahnyc{at}skku.edu, ycahn.ahn{at}samsung.com; Hee Chul Park, Department of Radiation Oncology, Samsung Medical Center, Sungkyunkwan University School of Medicine, 50 Ilwon-dong, Gangnam-gu, Seoul 135-710, Republic of Korea. E-mail: rophc{at}skku.edu, hee.ro.park{at}samsung.com

Received October 5, 2008; accepted December 18, 2008


   Abstract
TOP
 Abstract
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 Conflict of interest statement
 Acknowledgement
 References
 
Objective: This study was undertaken to identify the factors predictive of radiation pneumonitis (RP) in 69 non-small cell lung cancer patients treated with thoracic radiation therapy only by 3 Gy fractions.

Methods: A total of 69 patients who received only RT in daily 3 Gy were included in this study. Grade ≥3 RP was defined as an RP event. The cumulative incidence of RP was estimated and the correlations of the development of RP with the potential predictors were determined.

Results: The cumulative incidence of events was 17.1% at 12 months. By univariate analysis, all clinical factors [age, performance status, weight loss, pre-RT forced expiratory volume in 1 s, tumour location, stage, RT dose and clinical target volume] were not associated with the risk of Grade ≥3 RP; however, all dosimetric factors [V5–50 and mean lung dose (MLD)] closely correlated with the development of RP. The receiver-operative characteristics (ROC) analysis revealed that MLD was the best predictors of Grade ≥3 RP (area under curve ROC = 0.937). By multivariate analysis, MLD was the only significant factor to be predictive of RP risk: the probability of Grade ≥3 RP was 3.7% when MLD ≤ 16.1 Gy and 78.4% when MLD > 16.1 Gy.

Conclusions: Dosimetric parameters were valuable in predicting the development of RP.

Key Words: radiation pneumonitis • radiation therapy • hypofractionated treatment • lung cancer


   INTRODUCTION
TOP
 Abstract
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 Conflict of interest statement
 Acknowledgement
 References
 
Thoracic radiation therapy (TRT), either alone or combined with chemotherapy, has played an important role in treating non-small cell lung cancer (NSCLC). Especially in patients with medically inoperable or surgically unresectable lesions, high-dose TRT has definitively contributed to the survival prolongation. Minimal tumour dose of 60 Gy or higher has been considered as standard by conventional fractionation schedule at 1.8–2.0 Gy/fraction.

At the authors’ institute, the treatment policy has been surgical resection for Stage I/II. For Stage III NSCLC, surgical resection after neoadjuvant chemo-radiotherapy for Stage IIIA and concurrent chemo-radiotherapy for Stage IIIB has been performed. Not all patients, however, are fit for surgical resection or concurrent chemo-radiotherapy because of various reasons including medical co-morbidities. For these patients, high-dose TRT alone at 3.0 Gy/fraction has been the alternative regimen in our institution. This fraction schedule has the advantages of shortened overall treatment duration and reduced treatment cost, and is similar to the widely used regimens in the UK for many years delivering 50–55 Gy in 20 fractions (1,2). The treatment outcomes by the authors' regimen were reported as comparable with those by more protracted fractionation schedules (3).

TRT is almost always accompanied with the risk of lung toxicity, which has been reported in 4–30% of patients following conventional fractionation (4–12). Many investigators have described the clinical factors to be predictive of the risk of radiation pneumonitis (RP), which include tumour location, performance status, smoking status during RT and chronic obstructive pulmonary disease (6,8,13,14). Several dosimetric factors derived from the dose–volume histogram (DVH) of the lung such as mean lung dose (MLD) and volume percentage of the lung irradiated more than the indicated dose (Vdose) were shown to be strongly associated with the risk of RP (5–8,11,12,15–18). Most of these factors were studied on the patient group treated with conventional fractionated TRT with or without chemotherapy of diverse regimens. The use of larger fraction size is believed to increase the risk of RP (19,20); however, there have been few studies that have evaluated the effects of fractionation size for the development of RP when using three-dimensional (3D) conformal technique (4).

In this retrospective study, NSCLC patients treated with TRT alone at 3 Gy/fraction were included to identify the clinical and dosimetric factors that would predict the risk of RP and to evaluate the implications of these factors in the current fractionation schedule.


   PATIENTS AND METHODS
TOP
 Abstract
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 Conflict of interest statement
 Acknowledgement
 References
 
Patients
We retrospectively reviewed the medical records of patients with NSCLC who received TRT alone at daily 3 Gy between January 2001 and June 2006 in our institution. The DVH data were restorable in 69 patients who received TRT of ≥45 Gy. Among them, 54 patients were medically unfit for surgery or concurrent chemotherapy and 15 patients refused other aggressive treatment options.

Radiation Therapy
In all patients, contrast enhancement computed tomography (CT) scan was performed on supine position for 3D TRT plan derivation. CT images at 3–5 mm thickness through the regions harbouring the gross lesions, and at 5–10 mm thickness through the remaining regions, were obtained during quiet breathing. After defining the gross tumour volume (GTV) and the normal structures, the clinical target volume (CTV) was delineated around the GTV considering the microscopic tumour extension. Two planning systems (Prowess, Alliant Medical Technologies, Norwood, MA, USA, prior to March 2003 and Pinnacle3, Philips Medical Systems, Madison, WI, USA, after April 2003) were used for 3D planning. Radiation dose was prescribed at the isocentre with heterogeneity correction. Three or four beam arrangements were typically usually used to adequately cover the target volumes and to minimize the dose to the normal tissues (e.g. lung, spinal cord and oesophagus). Typical beam arrangement and dose distribution are illustrated in Fig. 1. Usually, a second CT scan was performed for new plan to deliver as high dose to the CTV as possible, while keeping the dose to the normal structures at the tolerance limits. A median dose of 54 Gy (range, 45–60 Gy) was delivered at daily 3 Gy/fraction over 4 weeks using a linear accelerator with 6–15 MV photons.


Figure 1
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  		Figure 1. Typical beam arrangement and dose distribution. (a) CTV (sky blue colour, indicated by arrowhead) of primary tumour is delineated and is covered with 95% isodose line (blue colour, indicated by arrow). (b) Anterior beam is blocked with 1.5–2 cm margin at the CTV using MLC. (c) Arrangements of ANT/RAO/RPO beams were showed. CTV, clinical target volume; MLC, multi-leaf collimator; ANT, anterior; RAO, right anterior oblique; RPO, right posterior oblique. A colour version of this figure is available as supplementary data at http://www.jjco.oxfordjournals.org.

 
DVH Parameters
The total lung volume (TLV) was defined as the total lung minus the GTV volume. The following DVH parameters for the total lung were obtained: MLD and Vdose (percentage of the TLV irradiated more than the indicated dose, V5–50 in the increment of 5 Gy). Adjustment of the dose to the biologically equivalent dose by conventional fractionation at 2 Gy/fraction was not done.

Evaluation of RP
All patients were evaluated weekly during RT. The follow-up chest CT was performed in 1 month of completion of TRT, which was repeated at 3–4 months for the first 2 years and every 4–6 months thereafter. RP was diagnosed by the clinical symptoms that could be correlated with the radiographic findings in the absence of other causes of symptoms. RP was graded according to the Radiation Therapy Oncology Group (RTOG) Acute and Late Lung Morbidity Scoring Criteria.

Statistical Analysis
Grade ≥3 pneumonitis was defined as an RP event. Patients who had a local recurrence within the RT field during follow-up were censored at the time of recurrence. The cumulative incidence of RP was calculated in an actuarial manner by the Kaplan–Meier method. The correlations of the development of RP with the potential predictors, both independently and simultaneously, were determined using the Cox regression analysis. The potential predictors were as follows: clinical parameters [age, performance status, weight loss, pre-RT forced expiratory volume in 1 s (FEV1), tumour location, stage, RT dose and CTV]; and dosimetric parameters (MLD and V5–50). The receiver-operative characteristics (ROC) curve was used to assess the predictability of dosimetric parameters. The ROC curve is a plot of the true-positive rate against the false-positive rate. For each dosimetric parameter, the ROC area under curve (AUC) value was determined to assess the predictability of a certain parameter regarding RP event. The closer the AUC value is to 1.0, the more predictive the DVH parameter regarding RP event is. A possible association between dosimetric factors was tested with Pearson’s correlation coefficient. Factors with a P value of ≤0.05 were considered to be statistically significant. Statistical analyses were performed using SAS software (SAS for Windows, version 9.0, SAS Institute, Cary, NC, USA).


   RESULTS
TOP
 Abstract
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 Conflict of interest statement
 Acknowledgement
 References
 
Patient Characteristics
The median age of all patients was 71 years (range, 32–88 years), and the majority was male (57/69, 82.6%). About half of the patients were in rather poor performance status of Eastern Cooperative Oncology Group (ECOG) 2 or higher (35/39, 50.7%), and a quarter of the patients were with FEV1 under 1.2 l (18/69, 26.1%). Tumours were located in the upper lobes in 38 patients (55.1%) and in the middle or lower lobes in 31 patients (44.9%), and more than half were with Stage III (36/69, 52.2%). The total dose was 45–54 Gy in 43 patients (62.3%) and was 57–60 Gy in 26 (37.7%). The median CTV was 144.9 cm3 (range, 7.2–625.4 cm3). The clinical and treatment-related factors are shown in Table 1. The median follow-up period was 11 months (range, 3–40 months).


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  		Table 1. The clinical and treatment-related factors of patients

 
Development of RP
Grade ≥3 RP developed in 11 patients after 1–6 months (median 3 months) following the completion of RT. The cumulative incidence of RP was 17.1% at 12 months (Fig. 2). By univariate analysis, all clinical and treatment-related factors including age (>70 vs.≤70 years), sex, performance status (ECOG 0–1 vs. ECOG ≥2), weight loss, pre-RT FEV1 (≥1.2 vs. <1.2 l), tumour location (upper lobe vs. middle or lower lobe), Stage (I/II vs. III), RT dose (≤54 vs. >54 Gy) and CTV (>145 vs. ≤145 cm3) were not associated with the risk of Grade ≥3 RP (Table 2). However, all dosimetric factors (V5–50 and MLD) closely correlated with the development of RP (Table 3).


Figure 2
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  		Figure 2. The cumulative incidence of Grade ≥3 RP in all patients. RP, radiation pneumonitis.

 

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  		Table 2. Univariate analysis of the clinical and treatment-related factors predicting radiation pneumonitis

 

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  		Table 3. Univariate analysis of the dosimetric factors predicting radiation pneumonitis

 
The ROC analysis revealed that V20 and MLD were the best predictors of Grade ≥3 toxicity (AUC ROC = 0.910 and 0.937, Table 4). The ROC curves of V20 and MLD are shown in Fig. 3. The actuarial incidences of RP were 0.0% when V20 ≤ 27.5 (n = 41) and 41.8% when V20 > 27.5 (n = 28), and those were 3.7% when MLD ≤ 1610 cGy (n = 56) and 78.4% when MLD > 1610 cGy (n = 13) (Fig. 4).


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  		Table 4. The predictability of DVH parameters using ROC analysis

 

Figure 3
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  		Figure 3. The ROC curve of V20 and MLD. ROC, receiver-operative characteristics; V20, the percentage of lung volume receiving more than a dose of 20 Gy; MLD, mean lung dose.

 

Figure 4
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  		Figure 4. The cumulative incidence curves of Grade ≥3 RP stratified by V20 and MLD.

 
The best predictor, MLD, was included only for multivariate analysis because all dosimetric factors were highly correlated with each other by Pearson’s correlation coefficient (range, 0.26–0.98). Among clinical and treatment-related factors, none except MLD was a significant predictor of RP on multivariate analysis (Table 5).


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  		Table 5. Multivariate analysis of the predicting factors of radiation pneumonitis

 

   DISCUSSION
TOP
 Abstract
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
Conflict of interest statement
 Acknowledgement
 References
 
In our institution, TRT at daily 3 Gy/fraction has been applied for NSCLC patients who were medically unfit for aggressive treatment employing surgery and/or concurrent chemoradiation. Shortening of the overall treatment time, in this setting, can provide more convenience for medically unfit patients and reduce the healthcare costs (3). However, some studies have suggested that a larger fraction size increases pulmonary toxicity when compared with conventional fractionation. Roach et al. (20) investigated the factors associated with RP following combined modality therapy and found that the use of fraction size >2.67 Gy was the most significant factor associated with the increased risk of RP. They concluded that hypofractionated RT should be avoided in combined modality therapy setting. Pirtoli et al. (19) also reported that 55% of patients with severe lung toxicity received TRT with a larger faction size. However, studies of Roach et al. (20) and Pirtoli et al. (19) have a limitation in interpretation, as they included TRT by 2D techniques, which could have resulted in higher RP risk.

Using 3D conformal RT (3D-CRT), it is possible to spare a significant proportion of normal tissue and to reduce normal tissue toxicities as a consequence. Thirion et al. (10) employed, on a Phase I/II study, the regimen that delivered 72 Gy in 24 daily fractions, while keeping V25 of the total lung <30%, and only one among 22 patients experienced Grade 3 pneumonitis (4.5%, 1/22). In this patient, V25 and MLD were 28% and 21 Gy, whereas for all patients, the median values of V25 and MLD were 20% (range, 12–29%) and 16.2 Gy (range, 7.4–21.0 Gy). Lester et al. (1) also reported on the safety of hypofractionated regimens that delivered 50–55 Gy in 15–20 fractions over 3–4 weeks, and there was no Grade ≥3 lung toxicity when restricting V20 of the total lung <40% by 3D-CRT.

In our institution, the cumulative incidence of Grade 3 RP at 12 months was 17.1%, which was higher than the results of the above-mentioned studies. As restriction of DVH parameters was not done in our regimen, the dosimetric data showed a wide range: median V25 and MLD of all patients were equivalent to 24.6% (range, 6.6–48.3%) and 16.3 Gy (range, 5.6–28.1 Gy), if adjusted for the equivalent fraction size (i.e. biologically equivalent dose at 2 Gy/fraction assuming the {alpha}/β ratio to be 3 in the linear quadratic model). The ranges of dosimetric parameters in our study were wider than those of Thirion et al. (10). In our study, V25 was <30% in 55 patients (79.7%), in whom the cumulative incidence of RP at 12 months was only 5.7%, which was comparable to the results of Thirion et al. (10). Even though conventional fraction size was not employed in our study, the results of ours and of Thirion et al. (10) suggest that the risk of RP was low if DVH parameters had been strictly restricted when using larger fraction size.

Several investigators reported the prediction of RP risk by dosimetric parameters such as V13, V20, V25, V30 and MLD. Armstrong and McGibney (15) found that V25 was a good predictor for RP risk, when delivering median 70.2 Gy in daily 1.8 Gy fractions to 31 NSCLC patients using 3D-CRT technique. Four patients (12.9%) developed RTOG Grade ≥3 RP: 1 among 23 (4.3%) with V25 ≤ 30%; and 3 among 8 (37.5%) with V25 > 30% (P = 0.04). Kim et al. (7) found that MLD was a useful indicator of RP risk: RTOG Grade ≥3 RP was observed in none among 28 patients with MLD < 10 Gy; in 3 among 28 (10.7%) with MLD of 10–14.9 Gy; and in 9 among 20 (45.0%) with MLD ≥ 15 Gy. Kim et al. (7) included more or less heterogeneous patients with respect to treatment modality: two-thirds were treated by TRT with concurrent chemotherapy; and the remaining were treated by TRT alone with daily 1.8–2.0 Gy fractions. Recently, Wang et al. (12) showed that V5 was the most significant factor associated with RP risk among 223 patients receiving conventional fractionated high-dose TRT with concurrent chemotherapy. The 1-year actuarial incidences of pneumonitis ≥Grade 3 by Common Toxicity Criteria 3.0 were 3% and 38% in the groups with V5 ≤ 42% and V5 > 42% (P = 0.001). The above three studies are different with respect to use of chemotherapy, even though they have similarity of using conventional fractionation schedule, and no reliable implication on using higher fraction size can be drawn. Clenton et al. (4), on the patients treated by rather heterogeneous fractionation regimens (36% with 1.5 Gy bid, 34% with 2.75 Gy qd and 12% with 2.5 Gy qd), found that there was no correlation between pneumonitis score and V20 or other possible predictive factors.

Our study included homogenous patients treated by TRT only in daily 3 Gy. Dosimetric parameters were significant in the prediction of the risk of RP in our study. The 1-year actuarial incidence of RP was 0.0% when V20 ≤ 27.5 and 41.8% when V20 > 27.5, and 3.7% when MLD ≤ 16.1 Gy and 78.4% when MLD > 16.1 Gy. It could be speculated that the current results be more reliable when using daily 3 Gy fraction.

There were many clinical factors associated with RP risk such as performance status, age, tumour location, current smoking status, the presence of pulmonary disease and poor pulmonary function (6,8,13,14). Our study did not show any correlation of RP risk with these clinical factors, which might be partly explained by rather small sample size.

In conclusion, the current study showed that dosimetric parameters (V20 and MLD) were predictive of the development of RP in patients treated with TRT only with 3 Gy fractions.


   Conflict of interest statement
TOP
 Abstract
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 Conflict of interest statement
Acknowledgement
 References
 
None declared.


   Acknowledgement
TOP
 Abstract
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 Conflict of interest statement
 Acknowledgement
References
 
This work has been partly supported by IN-SUNG Foundation for Medical Research.


   References
TOP
 Abstract
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 Conflict of interest statement
 Acknowledgement
 References
 
1 Lester JF, Macbeth FR, Brewster AE, Court JB, Iqbal N. CT-planned accelerated hypofractionated radiotherapy in the radical treatment of non-small cell lung cancer. Lung Cancer (2004) 45:237–42.[CrossRef][Web of Science][Medline]

2 Price A. Results of a survey of UK Clinical Oncologists. (2001).

3 Kim B, Ahn YC, Lim do H, Nam HR. High-dose thoracic radiation therapy at 3.0 Gy/fraction in inoperable stage I/II non-small cell lung cancer. Jpn J Clin Oncol (2008) 38:92–8.[Abstract/Free Full Text]

4 Clenton SJ, Fisher PM, Conway J, Kirkbride P, Hatton MQ. The use of lung dose-volume histograms in predicting post-radiation pneumonitis after non-conventionally fractionated radiotherapy for thoracic carcinoma. Clin Oncol (R Coll Radiol) (2005) 17:599–603.[Medline]

5 Fay M, Tan A, Fisher R, Mac Manus M, Wirth A, Ball D. Dose-volume histogram analysis as predictor of radiation pneumonitis in primary lung cancer patients treated with radiotherapy. Int J Radiat Oncol Biol Phys (2005) 61:1355–63.[Web of Science][Medline]

6 Hernando ML, Marks LB, Bentel GC, Zhou SM, Hollis D, Das SK, et al. Radiation-induced pulmonary toxicity: a dose-volume histogram analysis in 201 patients with lung cancer. Int J Radiat Oncol Biol Phys (2001) 51:650–9.[CrossRef][Web of Science][Medline]

7 Kim TH, Cho KH, Pyo HR, Lee JS, Zo JI, Lee DH, et al. Dose-volumetric parameters for predicting severe radiation pneumonitis after three-dimensional conformal radiation therapy for lung cancer. Radiology (2005) 235:208–15.[Abstract/Free Full Text]

8 Rancati T, Ceresoli GL, Gagliardi G, Schipani S, Cattaneo GM. Factors predicting radiation pneumonitis in lung cancer patients: a retrospective study. Radiother Oncol (2003) 67:275–83.[CrossRef][Web of Science][Medline]

9 Schallenkamp JM, Miller RC, Brinkmann DH, Foote T, Garces YI. Incidence of radiation pneumonitis after thoracic irradiation: Dose-volume correlates. Int J Radiat Oncol Biol Phys (2007) 67:410–6.[Web of Science][Medline]

10 Thirion P, Holmberg O, Collins CD, O’shea C, Moriarty M, Pomeroy M, et al. Escalated dose for non-small-cell lung cancer with accelerated hypofractionated three-dimensional conformal radiation therapy. Radiother Oncol (2004) 71:163–6.[CrossRef][Web of Science][Medline]

11 Tsujino K, Hirota S, Kotani Y, Kado T, Yoden E, Fujii O, et al. Radiation pneumonitis following concurrent accelerated hyperfractionated radiotherapy and chemotherapy for limited-stage small-cell lung cancer: Dose-volume histogram analysis and comparison with conventional chemoradiation. Int J Radiat Oncol Biol Phys (2006) 64:1100–5.[CrossRef][Web of Science][Medline]

12 Wang S, Liao Z, Wei X, Liu HH, Tucker SL, Hu CS, et al. Analysis of clinical and dosimetric factors associated with treatment-related pneumonitis (TRP) in patients with non-small-cell lung cancer (NSCLC) treated with concurrent chemotherapy and three-dimensional conformal radiotherapy (3D-CRT). Int J Radiat Oncol Biol Phys (2006) 66:1399–407.[Web of Science][Medline]

13 Robnett TJ, Machtay M, Vines EF, McKenna MG, Algazy KM, McKenna WG. Factors predicting severe radiation pneumonitis in patients receiving definitive chemoradiation for lung cancer. Int J Radiat Oncol Biol Phys (2000) 48:89–94.[Web of Science][Medline]

14 Yamada M, Kudoh S, Hirata K, Nakajima T, Yoshikawa J. Risk factors of pneumonitis following chemoradiotherapy for lung cancer. Eur J Cancer (1998) 34:71–5.[CrossRef][Web of Science][Medline]

15 Armstrong J, McGibney C. The impact of three-dimensional radiation on the treatment of non-small cell lung cancer. Radiother Oncol (2000) 56:157–67.[CrossRef][Web of Science][Medline]

16 Graham MV, Purdy JA, Emami B, Harms W, Bosch W, Lockett MA, et al. Clinical dose-volume histogram analysis for pneumonitis after 3D treatment for non-small cell lung cancer (NSCLC). Int J Radiat Oncol Biol Phys (1999) 45:323–9.[Web of Science][Medline]

17 Rodrigues GB. A prospective study on radiation pneumonitis following conformal radiation therapy in non-small-cell lung cancer: clinical and dosimetric factors analysis. Radiother Oncol (2005) 75:120–1.[CrossRef][Web of Science][Medline]

18 Yorke ED, Jackson A, Rosenzweig KE, Braban L, Leibel SA, Ling CC. Correlation of dosimetric factors and radiation pneumonitis for non-small-cell lung cancer patients in a recently completed dose escalation study. Int J Radiat Oncol Biol Phys (2005) 63:672–82.[CrossRef][Web of Science][Medline]

19 Pirtoli L, Bindi M, Bellezza A, Pepi F, Tucci E. Unfavorable experience with hypofractionated radiotherapy in unresectable lung cancer. Tumori (1992) 78:305–10.[Web of Science][Medline]

20 Roach M 3rd, Gandara DR, Yuo HS, Swift PS, Kroll S, Shrieve DC, et al. Radiation pneumonitis following combined modality therapy for lung cancer: analysis of prognostic factors. J Clin Oncol (1995) 13:2606–12.[Abstract]


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