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Ann Thorac Surg 1996;62:1005-1009
© 1996 The Society of Thoracic Surgeons

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Original Articles: General Thoracic

Photodynamic Therapy for Esophageal Malignancy: A Prospective Twelve-Year Study

Grant Medical Center, Columbus, Ohio

	Abstract

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Background. We wanted to determine factors affecting survival rates of benefits to, and complications in patients with esophageal cancer treated with photodynamic therapy.

Methods. From 1982 to January 1994, we used photodynamic therapy to treat 77 patients with esophageal carcinoma and evaluated survival to July 1994. All patients had failed, refused, or were ineligible for surgical intervention, ionizing radiation therapy, or chemotherapy.

Results. The only significant variable affecting survival was clinical stage. Median survival after photodynamic therapy was as follows: all patients, 6.3 months (mean survival, 9.2 months); stage I, not reached; stage II, 12 months; stage III, 6.2 months; and stage IV, 3.5 months. For stages III and IV, a Karnofsky performance status of 70 or higher had a significant effect. For stage III, the median survival was 6.3 months when the Karnofsky performance status was equal to or greater than 70 and 3.5 months when it was less than 70. For stage IV, the median survival was 5.5 months when the Karnofsky performance status was equal to or greater than 70 and 2.5 months when it was lower than 70. Seven stage I patients with no treatment prior to photodynamic therapy had an estimated 5-year survival rate of 62%. Three patients with stage I invasive adenocarcinoma and Barrett's mucosa diagnosed when they underwent endoscopy for dysphagia were alive with no evidence of disease 17, 44, and 59 months after photodynamic therapy.

Conclusions. Photodynamic therapy for esophageal carcinoma caused minimal complications and no procedure-related deaths. Photodynamic therapy can be considered an alternative treatment for patients with Barrett's esophagus with severe dysplasia or patients with stage I carcinoma who are under consideration for operation but are high surgical risks. The length of palliation for patients having "noncurative" treatment was equal to or better than that reported historically for most other treatment regimens.

	Introduction

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
See also page 1009.

The use of selective photodynamic therapy (PDT) to treat malignant tumors is based on three observations: (1) after being injected intravenously, the photosensitizer disseminates to all cells; (2) because of differences in vascular and lymphatic clearance from tumors and because of retention of the photosensitizer by the tumor cells, the photosensitizer is selectively retained in the tumor cells and interstitial tissue of the tumor, so that after 2 or 3 days, there is a greater concentration of the photosensitizer in the tumor than in the adjacent normal tissue; and (3) the photosensitizer will absorb light energy and produce singlet oxygen, which then destroys the tumor. Because there is less photosensitizer in the adjacent tissue, it will react less. We report here our experience using PDT to treat patients with esophageal cancer.

	Material and Methods

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
In a prospective study from 1982 to January 1994, we used PDT to treat 77 patients with esophageal carcinoma and evaluated their survival to July 1994. Entry criteria were a histologic diagnosis of adenocarcinoma or squamous cell carcinoma of the esophagus and failure of conventional treatment or ineligibility for such treatment because of medical status. Follow-up was 100%. There were 53 white men, 16 white women, 6 black men, and 2 black women. Forty-five had adenocarcinoma and 32, squamous cell carcinoma. Age ranged from 35 to 91 years with a mean and median age of 68 years. Conventional therapies (chemotherapy, surgical intervention, or both; external or brachy irradiation therapy; yttrium-aluminum garnet laser; or any combination of these) had failed in 40 patients.

All patients were clinically staged at the time of PDT using the TNM system: history, physical examination, bronchoscopy, esophagoscopy, barium esophagograms and computed tomographic scans of the chest and abdomen. Eight patients were in stage I (7 adenocarcinoma, 1 squamous cell carcinoma), 11 were in stage II (9 adenocarcinoma, 2 squamous cell), 26 were in stage III (13 adenocarcinoma, 13 squamous cell), and 32 were in stage IV (16 adenocarcinoma, 16 squamous cell).

Treatment
Photodynamic therapy was performed using a 630-nm light generated by an argon dye laser system (Spectra Physics, Mt. View, CA) as the activator and delivered through cylindrical diffusing-tip quartz fibers passed through the biopsy channel of a flexible endoscope. When possible, the diffusing tip was inserted into the tumor; otherwise, it was placed alongside the tumor.

Initial treatments were performed using hematoporphyrin derivative as the photosensitizer. However, for the last 10 years, we have used the more purified form dihematoporphyrin ether (Quadra Logic Technologies, Vancouver, BC, Canada) injected intravenously 1 day to 3 days before treatment.

Four variables were evaluated: photosensitizer dose, day of treatment after injection, light power density, and light dose [1]. Analyses of the results led us to now use 60 mg of dihematoporphyrin ether per square meter of body surface area; power densities of 500 mW per centimeter of diffusing fiber; light doses of 300 J per centimeter of diffusing fiber; interstitial treatment of the tumor if possible; and treatment 1 day to 3 days after injection of the photosensitizer.

Two to 3 days after PDT, esophagoscopy was repeated, and necrotic tissue was mechanically removed. One month after PDT, repeat endoscopy was done, and residual tumor was treated after another injection of photosensitizer. Patients then underwent endoscopy periodically and repeat treatment of symptomatic residual tumor. One hundred twenty-five injections of photosensitizer were made (mean number, 1.6 per patient), and 147 PDT esophagoscopies were performed (mean number, 1.9 per patient).

Stage of disease, Karnofsky performance status (KPS), weight, diet, and complications were recorded at each endoscopy. Biopsy samples and brushings were taken at each endoscopy. At the beginning and end of every endoscopy, the minimal diameter opening of the esophagus and the length, thickness, and color of the tumor were recorded. Edema, exudate, bleeding, and mucitis were evaluated and recorded on an ordinal scale.

Follow-up
Follow-up is 100%, and surviving patients continue to be followed up.

Statistical Analysis
Statistical analyses were performed using SuperANOVA, StatView, and Survival Tools (Abacus Concepts, Inc, Berkeley, CA). Because the average age of the patients was 68 years, many had severe medical problems unrelated to cancer, and the effect of treatment of specific disease on survival is better analyzed by time to death caused by the disease; disease-specific survival times in months were calculated from the time of the first PDT to the end point of July 1994 using Kaplan-Meier tables and curves. The Breslow-Gehan-Wilcoxon test was used to compare the significance of differences in survival distributions because it is more likely to detect early differences than log rank tests, and most deaths occur early in all series of esophageal cancer. Cox proportional hazards tests were used to estimate the effects of different variables on the length of survival. All statistics used 95% confidence limits.

	Results

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Survival
The effect of different variables on the survival after PDT of the 77 patients with adenocarcinoma or squamous cell carcinoma was estimated using multivariate analysis. A model of the effects of age (p = 0.739), sex (p = 0.763), race (p = 0.826), KPS (p = 0.139), day of treatment (p = 0.264), histology (p = 0.969), location of tumor (p = 0.506), length of tumor (p = 0.616), minimum diameter of esophageal opening (p = 0.171), and clinical stage (p = 0.0008) showed the last to be the most significant variable. The global likelihood ratio for the model was significant (p < 0.0001).

The median survival after PDT for all patients was 6.3 months (mean survival 9.2 months) (Fig 1). Kaplan-Meier curves for survival after PDT were significantly different when patients were stratified by clinical stage at the time of PDT (p < 0.0001). Median survival was as follows: stage I, not reached; stage II, 12 months; stage III, 6.2 months; and stage IV, 3.5 months (Fig 2).

View larger version (15K): [in this window] [in a new window]   Fig 1. . Kaplan-Meier cumulative (Cum.) survival curve for all patients (unstratified) with carcinoma of the esophagus treated with photodynamic therapy (PDT).

View larger version (19K): [in this window] [in a new window]   Fig 2. . Kaplan-Meier cumulative (Cum.) survival curves for patients with carcinoma of the esophagus treated with photodynamic therapy (PDT) stratified by clinical stage at the time of PDT. Numbers in parentheses indicate the number of patients in each stage at the time of PDT.

View larger version (19K): [in this window] [in a new window]   Fig 3. . Kaplan-Meier cumulative (Cum.) survival curves for patients with stage III carcinoma of the esophagus treated with photodynamic therapy (PDT) and stratified by a Karnofsky performance status of equal to or greater than 70 or less than 70. Numbers in parentheses indicate the number of patients.

View larger version (20K): [in this window] [in a new window]   Fig 4. . Kaplan-Meier cumulative (Cum.) survival curves for patients with stage IV carcinoma of the esophagus treated with photodynamic therapy (PDT) and stratified by a Karnofsky performance status equal to or greater than 70 or less than 70. Numbers in parentheses indicate the number of patients.

Stage I
When seen for PDT, 8 patients were in clinical stage I. Seven had a complete response to PDT. The estimated 5-year survival rate for all stage I patients was 51% (see Fig 2). At the time of PDT, 17 months after a subtotal gastrectomy and chemotherapy, 1 patient had recurrence. After PDT, he had a complete response that lasted for 16 months. He died of the disease 42 months after the diagnosis and 25 months after PDT.

The other 7 stage I patients had had no previous treatment but were medically ineligible for surgical intervention. Three were alive with no evidence of tumor 17, 44, and 59 months after PDT. One died 32 months after PDT of cardiac disease with no evidence of tumor, and 1 died at 13.5 months of cardiac disease with residual tumor. One died of disease 19 months after PDT. The 1 patient with squamous cell carcinoma had a complete response that lasted 8 months with recurrence at an untreated site. He died of the disease 18 months after PDT. The 5-year survival rate after PDT for the 7 stage I patients with no previous treatment is estimated to be 62%.

Mortality Within 30 Days After PDT
One patient in stage IV with a KPS of 30 died 4 days after PDT of a saddle pulmonary embolus. One other patient in stage IV with a KPS of 30 died 21 days after PDT of an unrelated cause, a previously placed, leaking jejunostomy feeding tube.

Complications
Transient elevations of both white blood cell count and temperature frequently developed immediately after PDT. Unilateral or bilateral pleural effusions did occur over several days but resolved spontaneously.

Four patients had pulmonary complications after PDT (infiltrates, 2 patients; aspiration pneumonia, 1 patient; pulmonary edema, 1), all of which resolved. Four patients had development of fistulas related to PDT (trachea, 2; left main bronchus, 2). All had squamous cell cancer, and 1 patient had visible tumor in the left main bronchus before PDT. Two of the patients were in stage III and 2, stage IV. One died of gastrointestinal bleeding after insertion of an esophageal stent. The other 3 died of their disease. Treatment before PDT consisted of external irradiation in 1 patient; brachytherapy and yttrium-aluminum garnet laser in 1; brachytherapy, chemotherapy, and immunotherapy in 1; and external irradiation, chemotherapy, and yttrium-aluminum garnet laser in 1.

Strictures in 4 patients developed after PDT. All strictures were manageable with dilation. The incidences of stricture and fistula formation were no greater than those reported for other treatment regimens [2, 3].

Solar photosensitivity of the skin may last for up to 8 weeks after the injection of dihematoporphyrin ether. Three patients experienced erythema and itching on the hands, face, or both from sun exposure. All had spontaneous resolution. Three patients had edema of the hands and 1 of the face. The edema resolved completely over a few days with oral steroids. One patient fell asleep next to a window and had development of a 1-cm area of necrosis on the hand; this healed spontaneously. A few patients had a long-lasting brownish tanning of exposed areas. By carefully increasing sun exposure and following repeated instructions, no patient experienced any serious photosensitivity reactions to the sun.

	Comment

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
The most significant variable affecting length of survival in our series was stage of the disease. When staged, there was no significant difference because of age, sex, race, day of treatment, length of tumor, minimal diameter opening of the esophagus, or location of tumor. There was no significant difference in the survival distributions within each stage between adenocarcinoma and squamous cell carcinoma. However, for stages III and IV, a KPS of 70 or higher was a significant favorable prognosticator, and it should be considered in comparing survival rates from different treatment regimens for these stages.

Complete responses of early esophageal cancers to PDT have been reported by several investigators [2–9]. Seven of our 8 patients with stage I disease had a complete response to PDT. The median and projected 5-year survival for patients with stage I esophageal cancer treated with PDT is comparable to other reported treatment regimens and better than some. The 7 stage I patients without no previous treatment had a projected 5-year survival rate of 62% with no procedure-related deaths. Reported 5-year survival rates after operation for stage I esophageal carcinoma are 46%, 47%, 55%, 60%, 63%, and 70% [10–15].

Three of our patients with stage I invasive adenocarcinoma who also had Barrett's mucosa were alive 17, 44, and 59 months after PDT. After PDT, Barrett's mucosa becomes necrotic and is replaced with squamous epithelium or scar tissue. Fifteen months after PDT, 1 of these patients had recurrence of Barrett's mucosa but no recurrence of tumor. Another patient with stage II esophageal carcinoma associated with Barrett's mucosa died 6.5 months after PDT of aspiration pneumonia with residual cancer. Streitz and associates [16] reported a 5-year postoperative survival rate of 58% for patients with pathologic stage I adenocarcinoma in Barrett's esophagus.

In addition, we have observed that hard tumors that cannot be dilated become soft after PDT and are easier to dilate.

Comparison of Survival With Other Treatment Regimens
In a retrospective analysis of survival from diagnosis in 268 patients with carcinoma of the esophagus, Oliver and colleagues [17] found no difference between adenocarcinoma or squamous cell carcinoma. The overall median survival stratified by primary treatment was as follows: surgical intervention, 9.8 months; radical radiation therapy, 6.3 months; intubation, 3.3 months; and palliative radiotherapy, 2.7 months. However, the patients were not staged, and only 34% were eligible for surgical intervention. The operative mortality rate was 9%; intubation had a mortality rate of 15%.

Baba and co-workers [13] reported the survival results after 106 subtotal esophagectomies with three-field lymphadenectomy. The hospital mortality rate was 10.4% and the morbidity, 65%. There was a 60% 5-year survival rate for 8 stage I patients.

Fok and associates [18] compared patients who had radiation treatment after operation with those who had operation only. The median survival by treatment were as follows: curative resection, 21 months; curative resection with irradiation, 15 months; palliative resection, 12 months; and palliative resection with irradiation, 7 months.

Sauter and associates [19] reported an overall median survival of 13 months for 30 stage I and stage II patients entered into a trial of preoperative chemotherapy and irradiation for adenocarcinoma of the esophagus and esophagogastric junction. The median survival of the 18 patients who actually had an esophagectomy was 23 months. The treatment mortality rate was 10%. Urba and co-workers [20] reported a median survival of 11 months for 24 patients with adenocarcinoma of the esophagus treated with preoperative chemotherapy and irradiation. Twenty-two patients were in stage II, 1 was in stage I, and 1 was in stage III. In a Southwest Oncology Group study, [21], 106 patients with squamous cell carcinoma of the esophagus received combined preoperative chemotherapy and external irradiation. The overall median survival was 12 months, and the operative mortality rate was 11%.

LePrise and colleagues [22] found that preoperative chemotherapy and radiation therapy did not change the operative mortality or length of survival for patients with stage I or II squamous cell carcinoma of the esophagus. The operative mortality rate was 8.5% for those receiving the combined treatment and 7% for those who did not. The median survival was 10 months for both groups. Skinner and co-workers [12] reported an actuarial 5-year survival rate of 55% for patients with the "earliest" lesions (W1 [W = wall penetration], N0) treated with en bloc esophagectomy for "cure." The median survival of those chosen for "standard esophagectomy" for palliation because of more extensive disease was 8 months. Finally, Law and associates [23] obtained median survivals after palliative resection of 7 months for 236 patients with squamous cell carcinoma and 8 months for 57 patients with adenocarcinoma.

Nineteen of our patients treated with PDT were in stage I or II (12, adenocarcinoma; 7, squamous cell carcinoma). The survival of these patients after PDT showed no significant difference in terms of histology (p = 0.7681); the median survival after PDT was 15 months for patients with adenocarcinoma and 18 months for those with squamous cell carcinoma.

Conclusions

1. The only significant variable affecting survival after PDT of carcinoma of the esophagus was clinical stage. Analysis of each individual stage showed KPS to be the only significant confounding variable, and the most significant effect occurred when the KPS was 70 or higher for stages III and IV.
   
2. The median disease-related survival after PDT for esophageal carcinoma was as follows: stage I, not reached; stage II, 12 months; stage III, 6.2 months; and stage IV, 3.5 months.
   
3. The 5-year survival rate after PDT for 7 previously untreated patients with stage I carcinoma of the esophagus is estimated to be 62%.
   
4. Three patients with stage I adenocarcinoma in Barrett's esophagus all had complete responses to PDT and were alive with no evidence of disease 17, 44, and 59 months after PDT.
   
5. Photodynamic therapy can be used concomitantly with chemotherapy and x-ray irradiation and can be repeated indefinitely.
   

	Footnotes

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Presented at the Thirty-second Annual Meeting of The Society of Thoracic Surgeons, Orlando, FL, Jan 29–31, 1996.

Address reprint requests to Dr McCaughan, Division of Photodynamic Therapy, Laser Medical Research Foundation, 323 E Town St, Columbus, OH 43215.

	References

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 

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This Article Abstract Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): James S. McCaughan, Jr Thomas E. Williams Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by McCaughan, J. S. Articles by Williams, T. E. Search for Related Content PubMed PubMed Citation Articles by McCaughan, J. S., Jr Articles by Williams, T. E. Related Collections Related Article