Originally published as JCO Early Release 10.1200/JCO.2003.04.018 on November 3 2003

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Radiotherapy Patterns of Care Study in Lung Carcinoma

B. Movsas, J. Moughan, R. Komaki, H. Choy, R. Byhardt, C. Langer, M. Goldberg, M. Graham, D. Ettinger, D. Johnstone, R. Abrams, R. Munden, G. Starkschall, J. Owen

From the Fox Chase Cancer Center; American College of Radiology, Philadelphia, PA; M.D. Anderson Cancer Center, Houston, TX; Vanderbilt University Medical Center, Nashville, TN; Medical College of Wisconsin, Milwaukee, WI; Phelps County Regional Medical Center, Rolla, MO; Johns Hopkins Hospital, Baltimore, MD; and University of Rochester, Rochester, NY.

Address reprint requests to Benjamin Movsas, MD, Fox Chase Cancer Center, 7701 Burholme Ave, Philadelphia, PA 19111; e-mail: b_movsas{at}fccc.edu.

	ABSTRACT

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Purpose: For the first time, a lung Patterns of Care Study was conducted to determine the national patterns of radiation (RT) practice in patients treated for nonmetastatic lung cancer in 1998 to 1999.

Materials and Methods: A national survey of randomly selected RT institutions in the United States was conducted using two-stage cluster sampling, stratified by practice type. Patients with nonmetastatic lung cancer (Karnofsky performance score [KPS] 60), who received RT as definitive or adjuvant therapy, were randomly selected. To determine national estimates, sample size was weighted by the relative number of institutions per strata and the number of patient records reviewed per the number of patients eligible. Accordingly, 42,335 patient records from 58 institutions were reviewed by trained research associates. The unweighted sample size (or number of patients) was 541.

Results: The histologies were small-cell lung cancer (SCLC) in 14.5% of patients versus non–small-cell lung cancer (NSCLC) in 85.5% of patients. The median age was 67 years (range, 29 to 92 years); 61% of patients were male, and 38% were current smokers. Bone scans and brain imaging were not obtained in 34% and 52% of clinical stage (CS) III NSCLC patients, respectively. Regarding treatment strategies, for SCLC and CS III NSCLC, chemotherapy plus RT was used significantly more than RT alone (P < .05); in CS I NSCLC, RT alone was the primary treatment (P < .05). Overall, 58% of patients received systemic therapy. On multivariate analysis, factors correlating with increased use of chemotherapy included younger age, histology (SCLC > NSCLC), increasing CS, increasing KPS, and lack of comorbidities. Only 3% of all patients were treated on prospective clinical trials.

Conclusion: This study establishes the general patterns of care for lung carcinoma in RT facilities within the United States. As supported by clinical trials, patients with limited-stage SCLC and CS III NSCLC received chemotherapy plus RT more than they received RT alone. Further improvements in staging, smoking cessation, and increased accrual to clinical trials must be encouraged.

	INTRODUCTION

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OVER THE LAST several decades, the Patterns of Care Study (PCS) mechanism has been used in the United States to determine national practice patterns involving radiation therapy (RT) for primary malignancies in many sites, including prostate cancer,¹ breast cancer,² and colorectal cancer.³ Although lung cancer is the number one cause of cancer death in the United States,⁴ until now the PCS mechanism had not been used for non–small-cell lung cancer (NSCLC) or small-cell lung cancer (SCLC). In this report, we summarize the first PCS study for lung cancer, which was conducted to determine the national patterns of RT practice in patients treated for nonmetastatic lung cancer during 1998 to 1999. Both then and now, lung cancer has been the leading cause of cancer deaths in the United States for both men and women. In 2003, it is estimated that 171,900 cases of lung cancer will be diagnosed with approximately 157,200 deaths,⁴ which exceeds the combined number of cancer deaths from breast cancer, prostate cancer, and colorectal cancer.

A primary goal of the PCS studies is to measure whether results and methodologies from positive clinical trials are being incorporated into national practice. During the 1990s, randomized trials⁵ and meta-analyses⁶ were published showing a benefit to RT plus chemotherapy versus RT alone for selected patients with locally advanced NSCLC. The advantage of combined-modality therapy has also been demonstrated in limited-stage SCLC.⁷ The questions we wished to examine included the following: 1) How well has chemoradiotherapy as a treatment strategy penetrated into the general national practice? 2) If combined-modality therapy is being used, how are these therapies being sequenced, and which chemotherapy agents are most commonly used? 3) What RT doses and techniques are used in various settings? 4) Has computed tomography (CT)-based RT treatment planning penetrated into daily practice?

	MATERIALS AND METHODS

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A national survey was conducted at 59 institutions in a stratified random sample selected from a master list of RT facilities located throughout the United States in 1998. Stratified two-step cluster sampling was used to select institutions and patients for data collection. RT facilities in the master list were divided into the following three strata: academic facility (main teaching hospital of a medical school or National Cancer Institute–designated Comprehensive Cancer Center), large nonacademic facility with 500 or more new RT patients per year, and small nonacademic facility with less than 500 new RT patients per year. Eighty facilities were selected from the three strata and invited to participate in the survey, although two of those facilities had closed before the survey began. Site visits to collect data took place at 22 academic centers, 19 large nonacademic centers, and 18 small nonacademic centers, for a participation rate of 76%. In the second stage of sampling, cases for each disease site were randomly selected for review and data abstraction, based on lists generated by the facility according to eligibility criteria.

Data were collected from 2000 to 2002 by PCS research associates who performed on-site chart review at each participating facility using a survey instrument developed for this purpose by the PCS Lung Committee. Data collected included demographic, diagnostic, staging, and therapeutic information.

To be eligible for analysis in this study, patients had to meet several criteria including treatment between 1998 and 1999, an American Joint Committee on Cancer 1997 nonmetastatic lung cancer stage, the use of RT as definitive or adjuvant therapy, and a Karnofsky performance score (KPS) 60. A weighted sample size of 42,335 patient records from 58 institutions (see Statistical Analysis) was reviewed by trained research associates. This involved a thorough chart review regarding patient demographics, staging, and treatment, with special attention to the RT prescription, technique, and dosimetry. The actual number of patients (or unweighted sample size) was 541 (one institution had no eligible patients).

Statistical Analysis
The Patterns of Care Executive Committee recently changed the method of analysis used in the evaluation of the collected data. This decision has led to the use of SUDAAN statistical software (RTI International, Research Triangle Park, NC), which incorporates the design elements (the two stages of stratification) and weights that reflect the relative contribution of each institution and each patient, in the analysis of this complex survey. The weights were the product of the following two factors:

All figures calculated using SUDAAN are national estimates for the patient population defined by the eligibility criteria listed previously in the article. For these analyses, the weights were calculated using the following strata: academic institutions, large nonacademic institutions ( 500 patients per year), and small nonacademic institutions (< 500 patients per year). Three SUDAAN procedures were used to do this analysis, one for percentages and tests on categoric variables (PROC CROSSTAB), one for descriptive statistics and tests on continuous variables (PROC DESCRIPT), and one for multivariate analysis that calculated odds ratios (PROC RLOGIST). For specific analyses in which the interest was to assess strata (type and size of RT facility) as a covariate, the design was necessarily simplified; these analyses did not include stratification as a design factor. Tests for associations were performed using the Pearson ² statistic in SUDAAN. Differences were deemed significant if their P values were less than .05.

	RESULTS

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The patient and tumor characteristics are listed in Table 1. The median age at the time of RT was 67 years (range, 29 to 92 years). Sixty-one percent of patients were male, 38% were current smokers, 83% had KPS 80, and 61% had comorbidity (mostly cardiopulmonary) as defined in the past medical history. The histologies were SCLC in 14.5% of patients versus NSCLC in 85.5%. The breakdown of NSCLC histologies is shown in the Table 1.

Overall, 58% of all patients received systemic therapy. Of all patients with NSCLC, 52% received chemotherapy in addition to RT, including 30% of patients with CS I NSCLC disease, 48% with CS II NSCLC, and 60% with CS III NSCLC. Of those NSCLC patients who received chemotherapy, 19% received induction chemotherapy followed by RT alone, and 74% received concurrent chemotherapy and RT. Of the NSCLC patients who received concurrent chemoradiotherapy, 21% received induction chemotherapy first, and 30% received consolidation chemotherapy. Regarding chemotherapy agents for NSCLC, 75% of patients received taxanes, of whom 92% received paclitaxel; 67% received carboplatin; 13% received etoposide; 12% received cisplatin-based therapy; and 3% received gemcitabine. Of patients with limited-stage SCLC, 95% received chemotherapy in addition to RT. Sixty-six percent of these patients received concurrent chemotherapy and thoracic RT, of whom 52% also received chemotherapy before RT and 45% also received chemotherapy after RT. Fifty-two percent of patients received cisplatin, 38% received carboplatin, 73% received etoposide, and 10% received paclitaxel. Further details regarding the precise breakdown of specific chemotherapy agents with RT and the timing related to RT will be addressed in a secondary analysis.

On univariate analysis, factors correlating with increased use of chemotherapy included younger age (68% 70 years v 41% > 70 years, P < .0001), small-cell histology (95% SCLC v 52% NSCLC, P < .0001), increasing CS (P = .0002), increasing KPS (P = .04), lack of comorbidities (P = .002), and strata (63% academic v 62% nonacademic < 500 patients v 48% nonacademic 500 patients, P = .0143). On multivariate analysis (Table 4), the following covariates significantly predicted for the use of chemotherapy: histology (P = .0003), absence of comorbidities (P = .0006), lower age (P = .0017), increasing CS (P = .0448), and higher KPS (P = .0467). The effect of strata became marginally significant (P = .0504). The distribution of patients varied considerably by practice type. For example, significantly more patients older than 70 years were treated at large nonacademic facilities (44%) compared with smaller nonacademic (34%) or academic institutions (29%; P = .03). Similarly, although not significant factors on their own, more patients with comorbidities and lower KPS were treated at large nonacademic facilities (data not shown). Of all chemotherapy patients, 72% received chemotherapy concurrently with RT. Carboplatin and paclitaxel were used in NSCLC more than SCLC (P = .01). Cisplatin and etoposide were used more in SCLC than in NSCLC (P = .0002). Systemic therapy was administered before RT in 44% of patients and after RT in 29% of patients.

	DISCUSSION

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This study establishes the general patterns of care for lung cancer in RT facilities within the United States. The breakdown in histologies (14.5% SCLC v 85.5% NSCLC) is similar to the expected national averages.⁸ Almost 40% of patients were current smokers at the time of treatment. Because continued smoking has been associated with not only an increased risk of developing a secondary neoplasm⁹ but also poorer outcome with treatment,¹⁰ efforts aimed at promoting smoking cessation after a diagnosis of lung cancer should be an important priority. Although the vast majority of patients (98%) had a chest CT scan as part of staging, staging appeared incomplete in CS III NSCLC patients, in whom bone and brain scans were not obtained in approximately one third and one half of patients, respectively. Positron emission tomography scanning was used in only 3% of patients. Although the average maximum spinal cord dose was acceptable at 41 Gy, this value was unknown (or not documented) in 21% of all patients. This PCS study suggests that further improvement in staging (particularly for CS III NSCLC) and documentation of spinal cord doses should be encouraged. Because only 3% of all patients were treated on protocols, increased accrual to clinical trials is critical.

As expected, treatment strategies varied significantly by histology and stage (Table 3, P < .0001). By definition, all patients in this study received RT either as part or the entirety of their treatment. A key purpose of this survey was to determine what other therapies, if any, were included as part of the overall treatment regimen in different clinical situations. As supported by clinical trials, patients with limited-stage SCLC and CS III NSCLC received chemotherapy plus RT significantly more than RT alone. In the landmark trial from the Cancer and Leukemia Group B Trial 84–33,⁵ induction chemotherapy followed by RT was associated with a significant improvement in 5-year survival compared with RT alone (P = .01) in patients with CS III NSCLC. Several meta-analyses subsequently confirmed a modest survival advantage to combined-modality therapy versus RT alone in locally advanced NSCLC.^6,11 Similarly, a meta-analysis in patients with limited-stage SCLC demonstrated a significant benefit in survival by adding thoracic RT to chemotherapy.⁷

Which patients were more likely to receive chemotherapy in addition to RT? Overall, approximately 60% of all patients in this study received systemic therapy. On both univariate and multivariate analysis, factors correlating with increased use of chemotherapy included younger age, histology (SCLC > NSCLC), increasing CS, increasing KPS, and lack of comorbidities. Most of these factors seem to follow good clinical judgment. In a prior Radiation Therapy Oncology Group analysis of approximately 1,000 patients with locally advanced NSCLC, Movsas et al¹² found that there was no clear benefit in quality-adjusted survival by adding chemotherapy to RT in patients older than 70 years of age. More recently, however, a secondary analysis of the Radiation Therapy Oncology Group Trial 9410 suggested that patients older than 70 years seemed to benefit from combined-modality therapy.¹³ These discordant findings may be a result of the better selection and management over time of elderly patients treated with intensive chemoradiotherapy regimens. Certainly, age alone should not be used to make treatment recommendations, but rather other underlying criteria should be used such as the presence of comorbidities, which seemed to be an important selection factor in this survey. Of all chemotherapy patients, the majority (72%) received chemotherapy concurrently with RT. Around the time of the PCS Lung Survey, the results of a key randomized trial became available that favored the use of concurrent chemoradiotherapy over sequential therapies in patients with inoperable CS III NSCLC.¹⁴

Practice type was a significant factor predicting for the use of chemotherapy on univariate, but not multivariate, analysis. This seems to be at least partly because of the distribution of patients seen at the different types of practices. Factors predicting for decreased use of chemotherapy (eg, older age, comorbidities, and lower KPS) were observed in more patients treated at large nonacademic institutions. Interestingly, in a separate, parallel Japanese lung PCS, Uno et al¹⁵ found that chemotherapy (in addition to RT) was used significantly more in academic facilities than nonacademic facilities (P = .003). Another difference noted in the Japanese study based on practice type related to the use of cobalt RT. Cobalt RT was used much more commonly in small nonacademic sites (20%) than in larger academic facilities (~1%). In the United States PCS Lung Study, approximately 1% of patients were treated with cobalt RT, regardless of practice type. Prior studies have suggested that cobalt RT is not optimal for the treatment of lung cancer.¹⁶

Overall, the doses of RT used in this study were within the guidelines of the American College of Radiology Appropriateness Criteria.¹⁷ For example, for NSCLC, the median RT dose was 60 Gy. Although the median dose for SCLC was 50.4 Gy, only 6% of SCLC patients received twice-daily RT, and only 22% received PCI. Two landmark studies supporting twice-daily RT¹⁸ and PCI in SCLC¹⁹ were published in the New England Journal of Medicine in 1999, and it is possible that these trials will impact on the future patterns of care regarding RT for this group of patients. Turrisi et al¹⁸ demonstrated a significant benefit in the 5-year survival rate with the use of twice-daily RT (45 Gy in 1.5 Gy fractions bid) with chemotherapy, compared with once-daily RT (45 Gy in 1.8 Gy fractions every day) with chemotherapy (26% v 15%, respectively). However, it is not clear whether accelerated hyperfractionated RT to 45 Gy is superior to higher RT doses (60 to 70 Gy) delivered via more standard fractionation.²⁰ In a meta-analysis, Auperin et al¹⁹ demonstrated not only a significant benefit in local control but also a modest improvement in survival with the use of PCI. Because the current study included a relatively small number of SCLC patients, the next PCS Lung Study will focus more on this group of patients to further address these important questions.

The ability to use higher doses of RT using more sophisticated treatment planning techniques, such as three-dimensional conformal RT, is a recent development with potentially important therapeutic implications. A phase I study in NSCLC has demonstrated that doses up to 102.9 Gy can be safely delivered via three-dimensional conformal RT with careful planning.²¹ In the United States PCS Lung Study, CT-based treatment planning was used in 49% of patients, and of these patients, approximately half reported using three-dimensional conformal RT. Exactly what this entailed, however, is not precisely known. This issue will be further studied in the next PCS Lung Study. Of note, in CS III NSCLC patients, CT treatment planning was used in more patients receiving chemotherapy and RT (61%) versus RT alone (30%; P = .047). Because the potential for RT toxicity is increased with the use of chemotherapy and the underlying prognosis is improved with this strategy (v RT alone), it seems reasonable that CT treatment planning would be used more in the setting of combined-modality therapy.

In conclusion, this first PCS Lung Study has established the general patterns of care for lung cancer in RT facilities within the United States. As supported by clinical trials, patients with limited-stage SCLC and CS III NSCLC are being treated with chemoradiotherapy (more than RT alone). Further improvements in staging, smoking cessation, and increased accrual to clinical trials must be encouraged. Because key studies supporting twice-daily RT and PCI in SCLC were published in 1999, the penetration of these trials will be assessed in the next survey. Future studies will also focus on the technical aspects of RT, such as the use of three-dimensional conformal RT for lung cancer, as well as analyses of outcomes.

	AUTHORS’ DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST

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The authors indicated no potential conflicts of interest.

	ACKNOWLEDGMENTS

 
We thank radiation oncologists and staff at participating facilities for their support, the PCS principal investigators (G.E. Hanks, MD, and J.F. Wilson, MD), the PCS research associates (T. Iarocci, MD, MS; D. Grant, RN, MSN; A. Mann, MHSA, RT(T); A. Trent, RN, MSN; and K. Roy, RN, BSN), and L. Morabito and D. Malone.

	NOTES

 
Supported by grant no. CA 65435 from the National Cancer Institute, National Institutes of Health, Bethesda, MD.

	REFERENCES

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Submitted April 2, 2003; accepted August 6, 2003.

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