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Ann Thorac Surg 2003;76:1687-1693
© 2003 The Society of Thoracic Surgeons

Original article: general thoracic

Photodynamic therapy as palliation for esophageal cancer: experience in 215 patients

Virginia R. Litle, MDa, James D. Luketich, MDa*, Neil A. Christie, MDa, Percival O. Buenaventura, MDa, Miguel Alvelo-Rivera, MDs, James S. McCaughan, MDa, Ninh T. Nguyen, MDa, Hiran C. Fernando, MDa

a Division of Thoracic and Foregut Surgery, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania, USA

* Address reprint requests to Dr Luketich, C-800, PUH, 200 Lothrop St, Pittsburgh, PA15213, USA.
e-mail: luketichjd{at}msx.upmc.edu

Presented at the Thirty-ninth Annual Meeting of The Society of Thoracic Surgeons, San Diego, CA, Jan 31–Feb 2, 2003.


   Abstract
Top
 Abstract
Introduction
 Patients and methods
 Results
 Comment
 Acknowledgments
 Discussion
 References
 
BACKGROUND: Photodynamic therapy (PDT) utilizes a photosensitizing agent, light, and oxygen to endoscopically ablate cancer cells. This review summarizes our experience with PDT for the palliation of bleeding or obstructing esophageal cancer (EC).

METHODS: All patients with bleeding or obstructing EC treated with PDT from November 1996 through June 2002, were reviewed. After Photofrin II injection, nonthermal light treatment was delivered endoscopically. Dysphagia scores, duration of palliation, reinterventions, complications, and survival after treatment were reviewed.

RESULTS: A total of 215 patients underwent 318 courses of PDT for bleeding (n = 15), obstruction (n = 277), bleeding and obstruction (n = 18), or other indications (n = 8). Tumor histology included 179 adenocarcinomas, 33 squamous cell carcinomas, and 3 undifferentiated. Seventy-five percent of EC were in the distal esophagus. In 85% of courses for obstruction, mean dysphagia scores improved pre- and post-PDT. The mean dysphagia-free interval was 66 days. Supplemental nutrition was discontinued after PDT in 8 of 27 patients (30%). Thirty-five patients required stent placement after PDT with a mean interval to reintervention of 58.5 days. PDT complications included perforation (2% of treatment courses), stricture (2%), Candida esophagitis (2%), pleural effusions (4%), and sunburn (6%). The procedure-related mortality rate was 1.8%, and median survival was 4.8 months.

CONCLUSIONS: PDT offers effective palliation for patients with obstructing EC in 85% of treatment courses. The ideal EC patient for PDT palliation has an obstructing endoluminal cancer. Patients living more than 2 months may require reintervention to maintain palliation of malignant dysphagia, and a multimodality treatment approach is common.


   Introduction
Top
 Abstract
 Introduction
Patients and methods
 Results
 Comment
 Acknowledgments
 Discussion
 References
 

Dr Luketich discloses that he has a financial relationship with Axcan Scandipharm, Inc.

 
The incidence of esophageal adenocarcinoma has been increasing during the past two decades, and approximately 13,100 new cases were diagnosed in the United States in 2002 [1]. The overall survival from esophageal cancer is 5% to 10%, and fewer than 50% of patients will be eligible for potentially curative resection at time of presentation. Most often patients present with dysphagia and weight loss; thus, the majority of patients may be candidates for palliative interventions to improve their swallowing, allow adequate oral intake, and reduce the risk of aspiration pneumonia.

Current modalities of palliating malignant dysphagia and improving esophageal obstruction include external beam radiation therapy, surgical resection, and endoscopic interventions including self-expandable metal stents (SEMS), pneumatic dilation, Neodymium:yttrium-aluminum garnet (Nd:YAG) laser, brachytherapy, and photodynamic therapy (PDT). External beam radiation therapy may take several weeks to relieve dysphagia when compared with stent placement [2]. Esophagectomy or bypass is associated with a longer recovery time than endoscopic interventions, which is an important factor when life expectancy is limited. SEMS palliate patients with obstructing tumors well but are associated with migration, tumor ingrowth and severe gastroesophageal reflux [3, 4]. Nd:YAG laser, when compared with PDT in a randomized trial of obstructing esophagus cancer, had a higher perforation rate [5]. Brachytherapy requires multiple endoscopies and is associated with strictures and fistula formation [6]. PDT is a nonthermal process using selective endoscopic delivery of light with a specific wavelength to activate a photosensitizing agent that results in tumor ablation and can restore endoluminal patency.

We summarize our results using PDT for palliation of a large series of patients with locally advanced obstructing or bleeding esophageal cancer.


   Patients and methods
Top
 Abstract
 Introduction
 Patients and methods
Results
 Comment
 Acknowledgments
 Discussion
 References
 
All patients with obstructing or bleeding esophageal cancer treated with PDT at the University of Pittsburgh Medical Center (UPMC) from November 1996 through June 2002, were reviewed retrospectively from a Division of Thoracic Surgery database approved by the Institutional Review Board (August 2001). Before PDT all patients underwent upper endoscopy confirming the presence of esophageal carcinoma. Patients eligible for PDT had advanced locoregional or distant metastatic disease. One PDT course was defined as an injection of the photosensitizing agent followed by two treatments. Patients were eligible for multiple courses of PDT if symptoms of dysphagia or bleeding recurred. The photosensitizing agent Photofrin II (Axcan Scandipharm, Inc., Birmingham, AL), a mixture of dihematoporphyrin ethers and esters (DHE), was administered at a dose of 2 mg/kg intravenously. Patients were then advised to avoid sunlight for the following 4 to 6 weeks. After a 24- to 48-hour wait, patients underwent endoscopic tumor ablation using a 2.5- to 5.0-cm diffusing tip fiber to deliver 630-nm light with a tunable dye laser (Laserscope, San Jose, CA). The fiber was placed at the distal aspect of the tumor and then withdrawn proximally to treat the entire tumor length. The total light dose typically ranged from 300 to 400 J/cm of tumor. For bulky endoluminal disease, the fiber tip was embedded in the mass for light delivery to minimize light exposure to surrounding normal esophageal mucosa. Repeat endoscopy was performed 48-hours later to assess tumor response, dilate the esophageal lumen, debride necrotic tumor, and administer additional laser therapy if necessary. Pneumatic dilation with an 18-mm balloon (Microvasive; Boston Scientific Corporation, Natick, MA) was used liberally to minimize post-PDT stricture formation. Patients typically consumed a clear liquid diet 1-day after initial PDT and were advanced to a soft diet 2 to 3 days after final light treatment.

Dysphagia data were obtained from a prospective database collected by a registered dietician, who clinically evaluated patients for dysphagia before PDT and at 2 to 4 weeks post-PDT. The following dysphagia scoring system was used: grade 1 = asymptomatic; 2 = difficulty swallowing hard solid foods; 3 = difficulty swallowing soft solids; 4 = difficulty swallowing liquids; 5 = unable to swallow anything including saliva [5]. The dietician also recorded whether the patient was receiving supplemental enteral or parenteral nutrition. The pre- and post-PDT dysphagia scores were analyzed using a Wilcoxon signed-rank test. A p value less than 0.05 was considered significant. The dysphagia-free interval was calculated for patients from date of first PDT treatment to date of any additional intervention at UPMC, which included additional Photofrin injections and PDT treatments, stent placement, Nd:YAG laser treatment, or esophageal dilation separate fom a course of PDT.

Patients who underwent PDT for palliation of bleeding tumors were also included in the database. For all patients with obstructed or bleeding cancers, complications of the PDT procedure were determined retrospectively from medical records.

An esophageal stricture can result from light treatment to normal esophageal mucosa because normal cells absorb the photosensitizer. The treatment-related esophageal stricture rate (TRES) was determined by recurrent or persistent dysphagia followed by an upper endoscopy and barium swallow study confirming the stricture and eliminating endoluminal disease or extrinsic compression.

Survival after PDT was recorded in months and date of death determined from patient medical records and phone calls to patients' physicians. A Kaplan-Meier estimate of the survival curve was generated from this data.


   Results
Top
 Abstract
 Introduction
 Patients and methods
 Results
Comment
 Acknowledgments
 Discussion
 References
 
A total of 215 patients with esophageal carcinoma underwent 318 courses of PDT. There were 165 males and 50 females with overall mean age of 69 years old (range 22 to 93 years old). Tumor histology included 179 adenocarcinomas, 33 squamous cell carcinomas (SCC), and 3 undifferentiated carcinomas. Seventy-five percent of the cancers involved the distal third of the esophagus (161 of 215 patients), 12% the midesophagus (25 of 215 patients), and 6% the proximal esophagus (13 of 215 patients). Sixteen additional patients (16 of 215 patients, 7%) represented local recurrences from transhiatal, Ivor-Lewis, or minimally invasive esophagectomy. Forty percent of patients (86 of 215 patients) had received other surgical or nonoperative treatment before PDT, and some patients had received more than one type of other treatment (Table 1). Fifty-three patients had undergone prior chemotherapy or radiation treatments. Thirty-six patients had had previous self-expanding metal stent (SEMS) placement, Nd:YAG laser ablation, or brachytherapy. A total of 16 patients underwent esophagectomy (11 adenocarcinoma and 5 SCC) before PDT. Indications for PDT were for obstruction in the majority (295 of 318 courses, 93%), but 15% of the (15 of 318 courses) PDT courses were for bleeding alone and 2% (8 of 318 courses) for palliation of tumor causing heartburn, pain, or poor appetite. Twelve of 16 patients (75%) who had undergone an esophagectomy received PDT for anastomotic recurrence, whereas the other 4 patients had symptomatic recurrent tumor in their gastric tube (2 patients) or proximal esophagus [2].


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  		Table 1. Interventions Before Photodynamic Therapy for Palliation of 215 Esophageal Carcinoma Patients

 
Endoscopic views immediately post-PDT routinely demonstrated edema and tumor necrosis as seen in a distal esophageal lesion in Figure 1A. There was minimal effect on adjacent normal esophageal mucosa. After debridement and esophageal pneumatic dilation, patients with residual tumor had additional light delivered during the routine 48-hour follow-up endoscopy (Fig 1B).



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  		Fig 1. (A) Endoscopic view of an obstructing esophageal carcinoma. (B) Tumor necrosis is seen 48 hours after photodynamic therapy.

 
Before PDT 13% of the patients (27 of 215 patients) were receiving supplemental nutrition by either feeding tube (23 patients) or total parenteral nutrition (4 patients). Eight of 27 patients (30%) were able to discontinue supplemental feeds after PDT treatment, including all 4 patients who had been receiving total parenteral nutrition.

Pre- and post-PDT dysphagia scores were obtainable for 251 PDT courses for obstruction. Eighty-five percent of PDT treatment courses resulted in a reduction of at least one unit in the pre-PDT dysphagia score. The median dysphagia score before the PDT course was 3 (range 2–5) and after PDT was 2 (range 1–5); thus, the median change in the dysphagia score was –1 with a bootstrap 90% confidence interval of 0 to –2. The reduction in the dysphagia score was statistically significant (p < 0.0001, Wilcoxon signed rank test). Therefore, patients with dysphagia were palliated in 85% of courses of PDT.

Self-expanding metal stents are susceptible to tumor ingrowth into uncovered stents or overgrowth at the end of covered stents. Forty-three of 295 PDT courses (15%) were done to restore patency to an obstructed metal stent and palliate malignant dysphagia. A total of 29 patients underwent 43 PDT courses for stent obstruction. Sixty-five percent (19/29) of the patients with stents underwent an additional intervention for obstruction including PDT, Nd:YAG laser, pneumatic dilation, or placement of an additional stent (Table 2). Additional PDT was the most common reintervention, and the interval to reintervention for stent ingrowth or overgrowth ranged from 30 to 88 days.


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  		Table 2. PDT Used to Treat Tumor Ingrowth or Overgrowth of a Self-Expanding Metal Stent in 29 Patientsa

 
Thirty-one patients underwent PDT for bleeding (16 for bleeding and obstruction, and 15 for bleeding alone). Bleeding was controlled in 29 of 31 patients (93%) with one PDT course. One patient with adenocarcinoma had two PDT courses for bleeding and obstruction, and subsequently underwent stent placement for persistent obstruction. Another patient with SCC underwent three total PDT courses to control bleeding and obstruction.

The intravenous administration of Photofrin II was not associated with any acute toxicities. Complications of the procedure in 318 PDT courses are summarized in Table 3. Most sunburn cases were limited to erythema (first degree). One patient developed blistering (second degree). Symptomatic pleural effusions occurred after 3.5% of PDT courses and were treated with therapeutic thoracenteses. Candida esophagitis was diagnosed in 5 patients with dysphagia who had endoscopic evidence of fungal infection. Five patients (5 of 215 patients, 2.3%) were diagnosed with TRES, and they were treated with pneumatic dilation and a self-expanding metal stent if the stricture persisted.


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  		Table 3. Perioperative Complications in 318 Courses of Photodynamic Therapy for Esophageal Carcinoma

 
Five patients developed esophageal perforation after PDT and was confirmed with postprocedural barium swallow for a perforation rate of 1.6% of 318 PDT courses. The overall perforation rate for patients was 2.3% (5 of 215 patients). Two of 5 patients expired from complications of their perforations; the other patients were treated with drainage or nonoperatively. Aspiration pneumonia was documented in 4 patients, and 2 of these patients also died from this complication. The 30-day procedure-related mortality rate was 1.8% (4 of 215 patients).

Forty patients (19%) required additional PDT alone for recurrent dysphagia at a mean interval of 71-days after initial PDT. Three patients underwent additional PDT and placement of a self-expanding stent to relieve obstruction, whereas 15% (32 of 215 patients) had a stent placed at a mean interval of 61-days after PDT, and 9% (20 of 215 patients) had pneumatic dilation without stent placement. The mean dysphagia-free interval for the 95 patients (95 of 215 patients, 44%) undergoing reintervention was 66 days.

Follow-up data were available for 197 of 215 patients (92%). Of these patients 94% (186 of 197 patients) died primarily of advanced disease. The median overall survival from time of first PDT treatment to death was 4.8 months. Eleven patients were alive at a median follow-up of 6.4 months. Figure 2 illustrates the Kaplan-Meier estimated survival curve for the patients.



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  		Fig 2. Estimated survival curve for patients undergoing photodynamic therapy (PDT) for bleeding or obstructing esophageal carcinoma (197 patients). Median survival was 4.8 months.

 

   Comment
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
Acknowledgments
 Discussion
 References
 
Locally advanced esophageal cancer is associated with complications of malignant dysphagia and bleeding in more than 70% of patients [7]. Palliation of dysphagia becomes an important factor for patients with advanced disease and short life expectancy. Goals of palliation should include return of oral intake, ease of treatment, and short hospital stay. Palliative options primarily include surgical resection or bypass, chemotherapy, external beam radiation (EBRT), and endoscopic interventions. Patients may need supplemental tube feedings or total parenteral nutrition to maintain adequate caloric intake but this of course does not improve dysphagia or quality of life, local pain, and risk of aspiration pneumonia. Palliative esophagectomy or bypass is rarely performed in patients with esophageal cancer because it is associated with morbidity and mortality rates of up to 60% and 45%, respectively [8–10], and may result in a prolonged hospital stay worsening quality of life. Although chemotherapy with EBRT improves dysphagia better than EBRT alone, complications are greater than with radiation alone and interval to improvement may exceed patients' already short life expectancy [11].

Endoscopic approaches for relieving malignant dysphagia and bleeding include placement of SEMS, balloon dilation, injection of vasoactive substances, and tumor ablation with Nd:YAG laser or PDT. SEMS may produce improved oral intake compared with surgical bypass [12], but can be associated with severe gastroesophageal reflux, chest pain, stent migration, and tumor ingrowth into the stent [2, 3, 13]. SEMS are ideal for esophageal obstruction secondary to extrinsic compression, and in our experience PDT is likely to fail in such patients [14]. Advantages of SEMS include ease of insertion, no photosensitivity, and immediate relief of dysphagia.

Thermal ablation with Nd:YAG laser is good for endoluminal disease but depth of penetration is unpredictable and has been associated with esophageal perforation. One study compared prospectively Nd:YAG and PDT for palliation of esophageal cancer in a multicenter randomized trial. The authors concluded tumor response and palliation were similar, but PDT was easier and associated with significantly fewer perforations [5]. Rates of dysphagia relief are similar for PDT and Nd:YAG [5, 15]; however, duration of response was found to be longer with PDT in one study [15].

The depth of penetration and tumor necrosis after PDT is limited to 5 mm, which provides a safety factor in minimizing risk of esophageal perforation. However, full-thickness perforation can occur if the light dose is too high [16]. In our series reported here the esophageal perforation rate was 1.5% of all PDT courses. In several of these five cases balloon dilation was performed before PDT to allow passage of the endoscope through the obstructing tumor. It is unclear whether the mechanical dilation of the esophagus, the use of PDT, or a combination of the two factors contributed to this complication. In none of the 5 patients was the PDT probe tip embedded directly into the tumor, although it is important to note that such a maneuver into a peripheral endoluminal tumor would likely increase the perforation risk.

TRES after PDT occurred in 2% of patients, although up to 9% of patients required esophageal dilation alone and 16% required stent placement after PDT. The combination of radiation, chemotherapy, and PDT typically increase risk of stricture formation, and 2 of 5 patients in our series with TRES had prior chemoradiation.

A treatment algorithm for palliative management of locally advanced symptomatic esophageal cancer at our institution is outlined in Figure 3. Patients with bleeding tumors can be endoscopically relieved with PDT or Nd:YAG laser with good control in greater then 90% of patients. Nd:YAG laser lacks associated photosensivity but is associated with greater risk of perforation and patient discomfort, often requiring general anesthesia for delivery.



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  		Fig 3. Treatment algorithm for endoscopic palliation of locally advanced esophageal carcinoma. (EC = esophageal cancer; PDT = photodynamic therapy; YAG = neodymium:yttrium-aluminum garnet laser.)

 
For the majority of symptomatic patients presenting with malignant dysphagia, location of tumor mass influences choice of therapy. Obstruction secondary to bulky mediastinal nodes or an external mass should be relieved with the SEMS to achieve the best result. Reflux can result in distal tumors and aspiration precautions are still necessary. If the tumor is causing bulky endoluminal obstruction, PDT is our treatment of choice. Patients who prefer to avoid sunlight precautions for 4 to 6 weeks are not candidates for PDT and then may be considered for endoscopic SEMS, Nd:YAG, or brachytherapy. Brachytherapy with and without laser treatment can improve dysphagia in the short-term, but again is associated with multiple hospital visits and stricture rates approaching 25% [6, 17, 18]. Nonendoscopic options still include EBRT with chemotherapy, although the risks of fistula formation and grades 3 and 4 esophagitis requiring hospitalization remain. The result of chemotherapy alone for malignant dysphagia has not been reported, but in our experience this generally improves.

The overall advantages of PDT for treating locally advanced esophageal cancer include improvement in malignant dysphagia within days of treatment, minimal pain of treatment administration, and ability to deliver it with conscious sedation. The main disadvantages include the skin photosensitivity in patients with a limited life expectancy and the costs of specialized equipment and the photosensitizing agent. There are also the added costs of at least two endoscopies, and in our series 44% of patients living longer than 2 months underwent additional endoscopies with subsequent interventions.

In conclusion, PDT is effective at improving malignant dysphagia from obstructing esophageal carcinoma. PDT also is effective at controlling bleeding tumors and ablating tumor ingrowth or overgrowth of esophageal stents. PDT can be given concurrently with other treatments, including chemotherapy or radiation, and multiple treatments can be given to improve dysphagia. Ideal candidates for PDT for palliation of locally advanced esophageal carcinoma have primarily endoluminal disease with minimal stricturing and extrinsic compression. Several treatments and a multimodality approach may be required to relieve recurrent dysphagia in patients with survival exceeding 2 months.


   Acknowledgments
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 Acknowledgments
Discussion
 References
 
Dr Luketich is a recipient of a research grant from Axcan Scandipharm, Inc. We thank Kathryn Lovas and Sue Churma for their help with data collection for this manuscript.


   Discussion
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 Acknowledgments
 Discussion
References
 
DR ERIC VALLIERES (Seattle, WA): Nice presentation. Did I hear you right that you admit these patients for a day or two prior to each procedure and that they stay in after the procedure for a few more days? What then is the length of stay for these patients every time you treat them? Is this need for in-hospital stay(s) taken into consideration for these patients who have a median survival of 4.8 months? Thank you.

DR LITLE: We did not determine the exact length of stay in our patients, but, yes, we do typically admit them, inject the Photofrin (Axcon Scandipharma, Birmingham, AL), and wait a day before we take them to the operating room for their endoscopies. I would approximate an average length of stay of 3–5 days. Often times these patients are dehydrated from poor oral intake or are suffering from an aspiration pneumonia and need hospitalization for intravenous hydration or antibiotics as well as the the phototherapy treatment. When patients are maintaining adequate intake and have no other current problems, we inject the photosensitizing agent on an outpatient basis and bring the patient back 2 days later for their endoscopic light treatment.

DR THOMAS J. WATSON (Rochester, NY): I enjoyed your talk. I just question in your final algorithm why patients with endoluminal tumor are getting photodynamic therapy (PDT) rather than a stent? Do you have any data regarding the relative costs of PDT, all costs considered, including reinterventions and the subsequent need for stents in a great number of patients, and comparing that to all costs for patients receiving stents as primary therapy? Also, after which therapy do patients symptomatically come out better, especially given the high reintervention rates with PDT, the fact that patients need to stay out of the sun for a month, and their median survival of only 4 to 5 months? Thank you.

DR LITLE: Most of the patients in our series have distal esophageal obstructing tumors, and we have previously reported that some of the downsides of stents include localized pain as well as severe reflux across the distal esophageal obstruction. For patients with extrinsic compression, we usually offer them self-expanding metal stents, although occasionally we use stents to treat endoluminal obstruction also. Overall we prefer to offer such patients phototherapy if they are willing to forego exposure to sunlight for a month. We do not have any specific cost analysis on it, though, but it would be a good idea to evaluate that.

DR NASSER ALTORKI (New York, NY): I may have missed this. Were these heavily pretreated patients that you palliated with PDT or not, and if not, then how does this fit in the algorithm of other palliative agents, as an example, primary chemotherapy? We just heard the other day that about 90% of the patients are palliated from their dysphagia within the first cycle.

DR LITLE: Almost half of these patients had received prior other palliative treatments, including chemoradiation, radiation alone, chemotherapy alone and/or stents. For chemotherapy alone I am not familiar with the recent report you are alluding to. Chemoradiation takes several weeks to improve the malignant dysphagia and is associated with a higher stricture rate, especially if you add PDT to the equation. In addition chemoradiation frequently requires multiple hospitalizations. Endoluminal brachytherapy also involves several weekly brachytherapy treatments and is also associated with a stricture rate and fistula formation of up to 10%.

DR STEPHEN HAZELRIGG (Springfield, IL): I saw in your numbers a 5% incidence of sunburn, or 6%, although I note you calculate the numbers on the number of treatments, not on the number of patients when you did percentages. My question really is, how significant is this sunburn issue? Are these minor issues, big issues? For those who don't use it, can you give us a little insight?

DR LITLE: We think it is a minor issue. Most of the patients who developed sunburn did so early in our experience. We do advise patients before we inject them that they have to avoid the sunlight, including sunlight coming through windows. None of the burns were third degree, and most were first degree with skin erythema. So I would say it is a minor issue except of course for those who experienced it. Thank you.


   References
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 Acknowledgments
 Discussion
 References
 

  1. American Cancer Society. Cancer facts and figures. . Atlanta, GA: American Cancer Society, 2002.
  2. Cwikiel M., Cwikiel W., Albertsson M. Palliation of dysphagia in patients with malignant esophageal strictures. Comparison of results of radiotherapy, chemotherapy and esophageal stent treatment. Acta Oncol 1996;35:75-79.
  3. Fan Z., Dai N., Chen L. Expandable thermal-shaped memory metal esophageal stent: experiences with a new nitinol stent in 129 patients. Gastrointest Endosc 1997;46:352-357.[Medline]
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  14. Luketich J.D., Christie N.A., Buenaventura P.O., Weigel T.L., Keenan R.J., Nguyen N.T. Endoscopic photodynamic therapy for obstructing esophageal cancer: 77 cases over a 2-year period. Surg Endosc 2000;14:653-657.[Medline]
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How to Keep the Treatment of Esophageal Disease in the Surgeon's Hands
Ann. Thorac. Surg., February 1, 2008; 85(2): S760 - S763.
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