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Ann Thorac Surg 2004;77:1484-1491
© 2004 The Society of Thoracic Surgeons

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Review

Photodynamic therapy in nonsmall cell lung cancer: a systematic review

^a University of Ottawa, Ottawa Hospital–General Campus, Ottawa, Canada
^b Practice Guidelines Initiative, Cancer Care Ontario Program in Evidence-Based Care, McMaster University–Courthouse T27, Hamilton, Canada
^c Cancer Care Ontario, Toronto, Ontario, Canada

^* Address reprint requests to Dr Maziak, University of Ottawa, Ottawa Hospital–General Campus, 501 Smyth Rd 6NW-6356, Ottawa, Ontario K1H 8L6, Canada.
e-mail: dmaziak{at}ohri.ca

	Abstract

Top Footnotes Abstract Introduction Material and methods Results Outcomes Mixed stages of lung... Late stage lung cancer Response Survival Palliation Toxicity External review Comment Conclusions Acknowledgments References

 
A systematic review and evaluation of evidence for photodynamic therapy in nonsmall cell lung cancer was undertaken. Two authors selected relevant articles according to predefined criteria. External feedback was obtained from Ontario clinicians and the provincial Lung Cancer Disease Site Group approved the review. The Group concluded that photodynamic therapy may have a role in treating superficial early stage disease or in palliating symptoms in late stage disease. The safety and effectiveness of photodynamic therapy compared with other treatment modalities remains undefined. Serious adverse effects can occur; therefore, the suitability of patients for this treatment should be carefully assessed.

	Introduction

Top Footnotes Abstract Introduction Material and methods Results Outcomes Mixed stages of lung... Late stage lung cancer Response Survival Palliation Toxicity External review Comment Conclusions Acknowledgments References

 
Photodynamic therapy (PDT) is a local treatment that involves a two-stage process: intravenous administration of a photosensitizer that is selectively retained in higher concentrations in the tumor than in surrounding tissue for a short period, and activation of the photosensitizer through irradiation of the tumor using nonthermal laser light at a specified wavelength (630 nm ± 3 nm for porfimer sodium) 2 to 4 days later. The cytotoxic effect produced by PDT is achieved through generation of free radicals, production of singlet oxygen through energy transfer from light to triplet oxygen, or by ischemic necrosis through neovascular shutdown partly mediated by thromboxane A₂ release (antiangiogenic effect) [1].

Photodynamic therapy is typically performed endobronchially with debridement of necrotic tumor undertaken within a few days of each treatment to prevent airway obstruction. Laser light can be reapplied within 4 to 5 days of the photosensitizer administration and the PDT process can be repeated once or twice, with a minimum of 30 days between injections of the photosensitizer [1].

Photodynamic therapy using porfimer sodium as a photosensitizer has been used in Europe since the 1980s for treatment of various cancers, and although its use for lung cancer in Canada is still very limited, there is increasing use of PDT worldwide. The Lung Cancer Disease Site Group (Lung DSG) conducted a systematic review and evaluation of the best available evidence for PDT to address the following questions:

1. What is the role for PDT in the management of early stage lung cancer?
   
2. What is the role for PDT in the palliation of patients with symptomatic, locally advanced lung cancer?
   

	Material and methods

Top Footnotes Abstract Introduction Material and methods Results Outcomes Mixed stages of lung... Late stage lung cancer Response Survival Palliation Toxicity External review Comment Conclusions Acknowledgments References

 
Development of systematic review and evidence evaluation
This systematic review and evidence evaluation report was developed by the Practice Guidelines Initiative (PGI) of Cancer Care Ontario's Program in Evidence-based Care, using the methodology of the practice guidelines development cycle [2]. The PGI is sponsored by, but is editorially independent of, Cancer Care Ontario and the Ontario Ministry of Health and Long-Term Care. Evidence for this report was independently searched for, selected, and reviewed by one member of the PGI's Lung DSG and methodologists. Selection of relevant articles was determined according to the predefined inclusion and exclusion criteria, and disagreements were resolved through discussion. The members of the Lung DSG reviewed, provided feedback on, and approved the final report. External review of the report was obtained through a mailed survey of Ontario practitioners and final approval was obtained from the Practice Guidelines Coordinating Committee. The report is intended as information for individuals and groups to use in making decisions and policies where the evidence is uncertain. Members of the Lung DSG disclosed potential conflict of interest information.

Literature search strategy
The MEDLINE (1966 through October 2002), CANCERLIT (1975 through September 2002), and the Cochrane Library (2002, Issue 4) databases were searched using the medical subject headings (MeSH) for "Lung neoplasms" combined with "bronchial neoplasms," "dihematoporphyrin ether," "hematoporphyrins," "hematoporphyrin photoradiation," "phototherapy," and each of the following phrases used as text words: "lung," "bronchogenic," or "bronchial" combined with "cancer," "carcinoma," "malignancy," "photofrin," "porphrin," "porphyrin," "hematoporphyrin," "dihematoporphyrin ether," or "porfimer sodium." In addition, the proceedings of the annual meetings of the American Society of Clinical Oncology (1997 through 2002) and the American Society for Therapeutic Radiology and Oncology (1999 through 2002), and the reference lists from relevant articles, abstracts, and reviews were also searched for additional trials.

Study inclusion criteria
Fully published reports or abstracts that met the following criteria were selected for inclusion:

1. Randomized controlled trials (RCTs) or noncontrolled prospective studies of PDT, alone or in combination with other therapies, for the treatment of nonsmall cell lung cancer.
   
2. Outcomes of survival, response rate, toxicity, or symptom palliation were reported.
   

Study exclusion criteria
The following were not considered

1. Studies involving detection of lung cancer.
   
2. Individual case reports, pilot studies, and retrospective studies were not considered because higher levels of evidence were available (RCTs, phase II trials, and other prospective studies).
   
3. Letters and editorials.
   
4. Publications in languages other than English.
   
5. Papers that may include data published by the same author in a later publication.
   

Evidence synthesis
The three randomized trials identified in the literature search did not have similar treatment comparisons; therefore, a meta-analysis of this data were not considered appropriate. In addition, the other prospective trials identified in the literature search were noncomparative and were not suitable for meta-analysis.

	Results

Top Footnotes Abstract Introduction Material and methods Results Outcomes Mixed stages of lung... Late stage lung cancer Response Survival Palliation Toxicity External review Comment Conclusions Acknowledgments References

 
Literature search results
No current practice guidelines on this topic were identified. The following were eligible for inclusion in the systematic review of the evidence: 3 RCTs in patients with late stage lung cancer (two reported in a single abstract) [3, 4]; 10 noncontrolled studies in early stage lung cancer (three reported in a single abstract) [5–12]; 1 summary paper reporting the cumulative results of PDT studies in early stage disease conducted in Japan more than 19 years [13]; 1 noncontrolled study that included a mix of stages [14]; and 5 noncontrolled studies of PDT in late stage disease [15–19].

In abstracts where the results of several trials were reported, the method of pooling data were not provided [3, 5]. Where the same data are reported in more than one publication, the most recently available data are used. Two early studies were excluded because of limited data on lung cancer and the use of inadequate power density in laser treatment [20] and limited data on relevant outcomes [21].

The research to date has mostly consisted of small studies that describe clinical experience with PDT at a single center [6, 7, 9–12, 15–18]. For many of these studies, trial methodology is not described in detail and it is unclear if all eligible patients received treatment. Overall, the quality of the published research is limited.

	Outcomes

Top Footnotes Abstract Introduction Material and methods Results Outcomes Mixed stages of lung... Late stage lung cancer Response Survival Palliation Toxicity External review Comment Conclusions Acknowledgments References

 
Early stage lung cancer
Tables 1 and 2 summarize the 10 noncontrolled prospective studies and the 1 summary paper of PDT in the treatment of early stage lung cancer. Most treated patients were considered medically inoperable or had refused surgery [5–7, 9, 12]; however, one study included only patients who were considered candidates for surgery [10].

Four studies conducted subgroup analyses of response to PDT according to tumor size and found response rates were higher with tumors of length less than 2 cm [13] or equal to 1 cm [8], or surface area equal to 3 cm² [6, 9]. Higher response rates were also obtained with carcinomas in situ compared to T1N0M0 tumors [8, 9], although the differences were not significant and it is not clear that the two studies reporting this comparison are entirely independent.

Survival
The 5-year survival rates were reported for five noncontrolled studies of early stage disease [7, 9–11, 13] and varied from 43% among 36 patients with poor pulmonary or cardiac function [7] to 72% among 21 patients who were surgical candidates [10]. These rates are difficult to interpret because the studies all include the use of other treatment modalities at some point, eg, surgery, radiation, or brachytherapy.

Toxicity
Of the eight studies that provided data on adverse effects [5–10], all reported reactions relating to photosensitivity, typically described as mild to moderate. Edell and Cortese [6] reported fatal hemoptysis within 1 month of treatment in 8% of 38 patients and suggested that this was likely related to tumor necrosis and bleeding as a result of PDT. Mild to moderate adverse pulmonary events were common [5, 8] and productive expectoration or cough was reported as a mainly short-term side effect of treatment in two studies [6, 10]. Temporary airway stenosis or obstruction was reported in two studies [6, 9], and 3 patients experienced hypercapnic respiratory failure requiring mechanical ventilation. One of these patients subsequently died due to tension pneumothorax. Other reported toxicities are described in Table 2.

	Mixed stages of lung cancer

Top Footnotes Abstract Introduction Material and methods Results Outcomes Mixed stages of lung... Late stage lung cancer Response Survival Palliation Toxicity External review Comment Conclusions Acknowledgments References

 
In the series of 175 patients treated with PDT (Table 3), the longest median survival was obtained for patients with the earliest stage disease [14] and, in a mulitvariate analysis, only disease stage (p = 0.0001) and performance status (0 = 0.013) influenced survival. The length of palliation for patients with incurable disease was reported as equal to, or better than, historical controls.

	Late stage lung cancer

Top Footnotes Abstract Introduction Material and methods Results Outcomes Mixed stages of lung... Late stage lung cancer Response Survival Palliation Toxicity External review Comment Conclusions Acknowledgments References

 
Table 4 summarizes the three RCTs (two reported in a single abstract) and five noncontrolled prospective studies (one in abstract form) of PDT for the treatment of late stage lung cancer. Although PDT is typically delivered endobronchially, one study performed pleural PDT intraoperatively [19]. Median follow-up data were not available for the late stage disease studies.

	Response

Top Footnotes Abstract Introduction Material and methods Results Outcomes Mixed stages of lung... Late stage lung cancer Response Survival Palliation Toxicity External review Comment Conclusions Acknowledgments References

Response was reported in two small noncontrolled studies. In one study, which included an independent assessment of response, the diseased airway was enlarged to at least 50% of normal in all 9 assessable patients [16]; in the other study, tumor volume was reduced by more than 50% in 7 of 17 patients [15].

	Survival

Top Footnotes Abstract Introduction Material and methods Results Outcomes Mixed stages of lung... Late stage lung cancer Response Survival Palliation Toxicity External review Comment Conclusions Acknowledgments References

 
Wieman and colleagues [3] reported similar overall survival for both the PDT and Nd:YAG laser treatment groups; however, detailed survival data were not provided. Median survival was similar for patients randomly allocated to radiotherapy alone or PDT with radiotherapy, although the combined treatment group remained recurrence free for significantly longer [4]. It was unclear if patients whose initial treatment was unsuccessful in the randomized trials subsequently received additional treatments, a situation that could influence the results.

Four of five noncontrolled studies reported median survival with a range of 40 days [15] to 21.7 months [19]. The shortest median survival, reported by Vincent and coworkers [15], may have been due in part to the high light doses used for PDT in this study (from 200 to 3000 J) and the fact that routine toilet bronchoscopies with debridement were not conducted, resulting in a high rate of significant complications. The longest median survival was obtained in a combined modality study that included surgery, intraoperative pleural (not endobronchial) PDT, chemotherapy, and radiotherapy [19].

	Palliation

Top Footnotes Abstract Introduction Material and methods Results Outcomes Mixed stages of lung... Late stage lung cancer Response Survival Palliation Toxicity External review Comment Conclusions Acknowledgments References

 
Photodynamic therapy with radiotherapy produced a significant improvement in hemoptysis and shortness of breath at 3 months posttreatment compared with radiotherapy alone (p < 0.05), although both groups improved from baseline [4]. In the PDT group coughing was also significantly reduced at 1 month and 3 months posttreatment compared with baseline (p < 0.05) [4]. More patients demonstrated an improvement in dyspnea grade 1 month after PDT compared with Nd:YAG laser therapy (30% vs 17% of patients, p value not reported), although the PDT group had a greater number of adverse events [3]. None of the RCTs specified the symptom severity scale used or reported if assessment of symptoms was blinded.

Among the noncontrolled studies of PDT, one study reported improvement from baseline in breathing for all 9 evaluable patients and a cessation of hemoptysis in 6 patients on a self-report measure [16]; another study obtained reductions from baseline in coughing and dyspnea in most patients (scale unspecified) [17]. Following PDT, two studies reported a reduction in bronchial obstruction, assessed bronchoscopically, from 86% (± 2%) to 57% (± 3%) [17] and from 85.8% (± 19.6%) to 18.5% (± 17.3%) [18]. Pulmonary function, measured by forced vital capacity and forced expiratory volume in 1 second, improved following PDT in one study [18] but not in another [17].

	Toxicity

Top Footnotes Abstract Introduction Material and methods Results Outcomes Mixed stages of lung... Late stage lung cancer Response Survival Palliation Toxicity External review Comment Conclusions Acknowledgments References

 
Three of 20 patients experienced massive and fatal hemoptysis at 67, 187, and 567 days after treatment with PDT and radiotherapy [4]. Hemoptysis, dyspnea, and bronchitis occurred more frequently following PDT compared with Nd:YAG laser therapy, although many of these events occurred more than 30 days after treatment [3]. Photosensitivity associated with PDT occurred in 20% of patients in the randomized trials [3, 4].

Four of the five noncontrolled studies also reported adverse effects associated with photosensitivity for patients receiving PDT, mainly in the form of mild sunburn. Other reported adverse effects are illustrated in Table 4. In 1 patient, worsening breathlessness following PDT led to mechanical ventilation followed by death 1 month after treatment [16]. Friedberg and coworkers [19] reported one death due to sepsis and one postoperative death due to acute respiratory distress syndrome. Vincent and colleagues [15] reported a high rate of significant complications (82%), with 8 of 17 patients admitted to intensive care following PDT, and 1 patient suffering asphyxiation.

	External review

Top Footnotes Abstract Introduction Material and methods Results Outcomes Mixed stages of lung... Late stage lung cancer Response Survival Palliation Toxicity External review Comment Conclusions Acknowledgments References

 
Feedback on a draft version of this systematic review and evidence evaluation report was obtained through a mailed survey of practitioners in Ontario. Forty-seven of 114 practitioners indicated that the report was relevant to their clinical practice and completed the survey. Of the 47 practitioners, 66% agreed that there was a need for a summary of the evidence on this topic, 89% agreed that the literature search was relevant and complete, 87% agreed with the overall interpretation of the evidence, and 72% felt that this type of evidence summary would be useful for clinical decision making. The Practice Guidelines Coordinating Committee also reviewed and approved the report.

Key issues raised by external feedback related to the limited and preliminary nature of the available evidence and the occurrence of very severe toxicities in a small number of patients. The Lung DSG acknowledged both issues and suggested that although PDT would not routinely be used in early stage disease, it could be considered the treatment of choice for patients with early stage disease and poor respiratory function where loss of lung tissue associated with surgery or external beam radiotherapy would preclude definitive interventions. PDT may also be the most useful treatment option for symptom palliation in some circumstances, eg, for tumors resistant to external beam radiotherapy or where the bronchus is completely blocked and the tumor cannot be accessed for brachytherapy or Nd:YAG laser therapy.

	Comment

Top Footnotes Abstract Introduction Material and methods Results Outcomes Mixed stages of lung... Late stage lung cancer Response Survival Palliation Toxicity External review Comment Conclusions Acknowledgments References

 
Photodynamic therapy is relatively easy to administer, can be performed on an outpatient basis, and can be repeated. For early stage, mainly medically inoperable disease, response rates varied from 30.8% to 84.8%. Subgroup analyses in three studies found a tendency toward improved response rates for smaller tumors. The 5-year survival rate varied from 43.4% to 72%, although for most studies this outcome reflected the effects of a combination of treatments rather than PDT alone. Overall, the data suggest that PDT can produce moderate response rates in early stage lung cancer, particularly where the tumor is small. The effect of PDT on survival for patients with early stage lung cancer is less clear.

In the RCTs of late stage disease, no survival advantage was detected for PDT compared with Nd:YAG laser therapy or PDT combined with radiotherapy compared with radiotherapy alone, but there was an advantage for PDT with radiotherapy with respect to symptom control. In comparison to Nd:YAG laser therapy, PDT did improve dyspnea grade but also resulted in a higher number of adverse events. Four of five noncontrolled studies reported post-PDT reductions in dyspnea, hemoptysis, cough, or bronchial obstruction. The palliative effect of PDT in late stage lung cancer is promising, although its effectiveness in comparison to traditional therapies requires further study.

Most treatment side effects were considered mild to moderate with photosensitivity being evident in most studies and adverse pulmonary events occurring commonly. In the studies reviewed, there were three patients with hypercapnic respiratory failure requiring mechanical ventilation among 67 patients with early stage lung cancer. One RCT in locally advanced disease reported fatal hemoptysis at 2, 9, and 18 months posttreatment for 3 of 20 patients receiving PDT with radiotherapy. In two noncontrolled studies, 7 of 213 patients (3 patients with early stage and 4 patients with locally advanced disease) died from hemoptysis or pulmonary hemorrhage within 1 month of treatment. One small study that did not include posttreatment toilet bronchoscopies also reported a high rate of significant complications (82%). The data on toxicity emphasize the need to ensure that patients understand the risks of exposure to sunlight in the period following treatment. The risk for serious adverse events should be taken into consideration in light of the patient's history and clinical condition. Toilet bronchoscopies should always be completed following endobronchial PDT to minimize the risk of bronchial obstruction, and the risk of hemoptysis should be considered before therapy and monitored post therapy.

Much current research is of limited quality and there is a need to fully assess the effectiveness of PDT through RCTs comparing PDT to surgery, chemotherapy, radiation therapy, and brachytherapy in early and late stage lung cancers.

	Conclusions

Top Footnotes Abstract Introduction Material and methods Results Outcomes Mixed stages of lung... Late stage lung cancer Response Survival Palliation Toxicity External review Comment Conclusions Acknowledgments References

 
There is currently insufficient high-quality evidence (RCTs, meta-analyses, or other comparative trials) on which to base a practice guideline on the use of PDT in nonsmall cell lung cancer. From the available evidence, the Lung DSG believes that PDT could be considered as a treatment option for patients with medically inoperable early stage disease that is accessible by bronchoscopy. Evidence to date suggests that PDT may be most effective with small, superficial airway lesions 1 cm or less in length. The relative safety and effectiveness of PDT compared with radiotherapy, an alternative treatment for patients with inoperable early stage disease, remains undefined.

In locally advanced and symptomatic lung cancer PDT, with or without radiotherapy, can contribute to the relief of airway obstruction and hemoptysis, but it has not exhibited a survival advantage when compared with current treatments, such as Nd:YAG laser therapy or radiotherapy alone. There is a role for PDT in the palliation of advanced lung cancer; however, this is not well defined in relation to other modalities of palliation.

Serious adverse effects including fatal hemoptysis and respiratory failure can occur; therefore, the suitability of patients for this treatment should be carefully assessed. Because tumor necrosis can result in posttreatment airway obstruction, patients should be closely monitored after undergoing the procedure and toilet bronchoscopies repeated as indicated.

	Acknowledgments

Top Footnotes Abstract Introduction Material and methods Results Outcomes Mixed stages of lung... Late stage lung cancer Response Survival Palliation Toxicity External review Comment Conclusions Acknowledgments References

 
Sponsored by Cancer Care Ontario and the Ontario Ministry of Health and Long-Term Care.

	Footnotes

Top Footnotes Abstract Introduction Material and methods Results Outcomes Mixed stages of lung... Late stage lung cancer Response Survival Palliation Toxicity External review Comment Conclusions Acknowledgments References

 
^* Yasmin Alam, MD; Michael Brundage, MD; A. R. Dar, MD; Gail Darling, MD; Peter Dixon, MD; Peter Ellis, MD; Conrad Falkson, MD; Ronald Feld, MD; Glen Goss, MD; Ian Graham PhD, Richard Gregg, MD; Walter Kocha, MD; Jaro Kotalik, MD; Scott Laurie, MD; Diane Logan, MD; Pedro Lopez, MD; Richard Malthaner, MD; Donna Maziak, MD; Joanne Meng, MD; John Miller, MD; Jonathan Noble, MD; Gordon Okawara, MD; Frances Shepherd, MD; David Stewart, MD; Mark Vincent, MD; Yee C. Ung, MD; Edward Yu, MD; and two community representatives also contributed to the development of this practice guideline. Methodologists working with the Lung Disease Site Group included: Anna Gagliardi, Lubna Baig, Angela Eady, and Toni Newman. Please see the Cancer Care Ontario Practice Guidelines Initiative (CCOPGI) web site (http://www.ccopebc.ca) for a complete list of current Lung Cancer Disease Site Group members.

	References

Top Footnotes Abstract Introduction Material and methods Results Outcomes Mixed stages of lung... Late stage lung cancer Response Survival Palliation Toxicity External review Comment Conclusions Acknowledgments References

 

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