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(Chest. 2005;128:684-689.)
© 2005 American College of Chest Physicians

Prospective Randomized Trial of Silver Nitrate vs Talc Slurry in Pleurodesis for Symptomatic Malignant Pleural Effusions*

Marcello da Silveira Paschoalini, MD; Francisco S. Vargas, MD, FCCP; Evaldo Marchi, MD, FCCP; José Rodrigues Pereira, MD; Fabio B. Jatene, MD; Leila Antonangelo, MD and Richard W. Light, MD, FCCP

* From Pérola Byington Hospital (Dr. Paschoalini), São Paulo, Brazil; the Laboratory of Pleura (Drs. Vargas, Jatene, Marchi, and Antonangelo), Division of Pulmonary Diseases, Heart Institute (InCor), University of São Paulo Medical School, São Paulo, Brazil; AVC Cancer Institute (Dr. Pereira), São Paulo, Brazil; and the Department of Medicine (Dr. Light), Saint Thomas Hospital and the Center for Lung Research, Vanderbilt University, Nashville, TN.

Correspondence to: Richard W. Light, MD, FCCP, Director of Pulmonary Disease Program, Saint Thomas Hospital, 4220 Harding Rd, Nashville, TN 37205; e-mail: RLIGHT98{at}yahoo.com


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Study objectives: To compare the efficacy and the safety of talc slurry and silver nitrate (SN) in the treatment of symptomatic malignant pleural effusions.

Patients and methods: Sixty patients were enrolled into the study, and all received a chest tube (26F or 28F) that was placed using local anesthesia. The patients were randomized to receive either 5 g talc diluted to a total volume of 50 mL with saline solution or 20 mL 0.5% SN through the chest tube. Patients were clinically evaluated before and after treatment regarding pain, and were evaluated at monthly intervals with respect to the effectiveness of pleurodesis. Eleven patients did not return for their 30-day follow-up visit and were excluded from further analysis. Pleurodesis therapy was considered to be successful if there was no recurrence of the effusion. The patients who did not have a pleurodesis at one visit were excluded from subsequent visits.

Results: Forty-nine patients returned at 30 days for follow-up, including 24 patients who received SN and 25 who received talc. The groups were similar in age (p = 0.23), sex (p = 0.70), Karnofsky index (p = 0.94), and pathology (p = 0.68). After the induction of pleurodesis, neither the total mean (± SE) fluid drainage (SN, 901 ± 125 mL; talc, 766 ± 74 mL; p = 0.36) nor the level of pain (SN, 2.58 ± 0.26; talc, 2.62 ± 0.30; p = 0.91) differed significantly between the groups, and no patient in either group developed ARDS. The mean number of days spent in the hospital was nearly identical (SN group, 3.7 ± 0.15 days; talc group, 3.6 ± 0.13 days; p = 0.47). Both SN and talc were effective agents. Thirty days after the procedure, 23 of 24 patients (96%) who had received SN and 21 of 25 patients (84%) who had received talc showed an effective pleurodesis (p = 0.35). Similar results were observed after 60 days (SN group, 18 of 18 patients [100%]; talc group, 13 of 13 patients [100%]; p = > 0.99), 90 days (SN group, 16 of 16 patients [100%]; talc, 8 of 9 patients [89%]; p = 0.36), and 120 days (SN group, 4 of 4 patients [100%]; talc group, 4 of 4 patients [100%]; p > 0.99).

Conclusions: The present study suggests that SN is an effective agent for producing a pleurodesis. In the present study, SN showed a tendency to be more effective than talc, but the power of the test to detect a significance difference was low in this small group of patients. The side effects of 0.5% SN appear to be minimal, but since only a small number of patients received SN and nearly 20% of the patients were lost to follow-up, significant long-term side effects cannot be excluded. Since SN appears to be as effective as talc, and since there is no evidence that it induces ARDS as has been reported with talc, it should be considered as an alternative to talc for the production of a pleurodesis.

Key Words: pleura • pleural effusion • pleurodesis • silver nitrate • talc


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Approximately 50% of patients with malignant pleural disease have an associated malignant pleural effusion (MPE). These MPEs occur most commonly secondary to lung, breast, and ovarian cancer, and lymphoma. Breast and lung malignancies are responsible for approximately 75% of these MPEs.1

The most common symptoms secondary to an MPE are progressive dyspnea, cough, and chest pain. The presence of the fluid itself can be responsible for the dyspnea and cough. If these symptoms are relieved with therapeutic thoracentesis, then it is reasonable to take measures that prevent the reaccumulation of pleural fluid. This is most commonly done with the injection of a sclerosing agent through a chest tube in an attempt to produce a pleurodesis.

The first pleurodesis was probably done by Spengler in the beginning of the 20th century. He injected silver nitrate (SN) into the pleural space to control recurrent pneumothorax.2 There are no additional clear references for this procedure until 1935 when Bethune3 introduced talc into the pleural space after lobectomy in patients with lung cancer. Since then, multiple other agents have been injected in attempts to create a pleurodesis.

However, the ideal sclerosing agent has yet to be identified. It should be inexpensive, readily available, easy to handle, easy to introduce into the pleural space, and should not cause significant side effects.

Beginning in 1935 talc was used as a sclerosant. It became popular because it was cheap, easy to handle, and available worldwide. It was well-tolerated, with few side effects, and was effective in > 90% of the patients.4 However, since it was administered by insufflation during the early years of its usage, thoracoscopy or thoracotomy was necessary for its administration, and this restricted its use. In 1958, it was reported5 that talc was effective when administered as a slurry (ie, talc in a saline solution) through a chest tube. This obviated the requirement for thoracoscopy or thoracotomy.5 The side effects and the effectiveness (around 90%) for insufflated talc and talc slurry are similar.4

In the 1980s, several cases of the ARDS were attributed to talc.6 In our personal experience during the last 15 years, the administration of 2 g talc into the pleural space of 614 patients resulted in seven (1.2%) cases of ARDS, of which three were fatal.4 These observations motivated us to study agents that had been previously used and shown to be effective.

SN is an effective sclerosant, inducing a caustic injury to the mesothelium that results in an effective pleurodesis.78 SN was used throughout the 1970s and 1980s for pleurodesis.910 During that period, the concentrations of SN used (1 to 10%) caused severe pain and pleural injury that sometimes resulted in large exudative effusions. These side effects probably led to the diminution in its use. In 1995, we demonstrated7 in rabbits that the intrapleural injection of a lower concentration of SN (0.5%) produced a pleurodesis at least as effectively as did talc.

This prospective randomized trial was designed to compare the efficacy and the safety of talc and SN given via thoracostomy tube, in the treatment of symptomatic MPE. Based on our animal studies, we hypothesized that the two agents would be equally effective.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Sixty patients with unilateral MPEs were enrolled into this study. The patients were recruited between January 2000 and July 2002 from the following two hospitals: AVC Cancer Institute and Pérola Byington Hospital. The medical staff is the same in both hospitals. Inclusion in the study required documentation of an MPE (ie, positive result of testing of pleural biopsy specimen or cytology), a Karnofsky index score of > 60, and a life expectancy > 1 month. Patients with loculated or trapped lungs after drainage were excluded from the study. The study was approved by the Ethics Committee of our institution, and an informed consent was obtained from eligible patients. Eleven of the patients did not return for their follow-up visit and were excluded from the analysis.

For the remaining 49 patients, a diagnosis of malignancy was obtained via cytology in 35 patients, by histologic examination of pleural biopsy specimens in 14 patients, and by both in 3 patients. In all patients, a chest tube (26F or 28F) was inserted using local anesthesia and parenteral meperidine. The drainage of the fluid was slowed when the patient experienced coughing or chest tightness to avoid reexpansion edema. The patients were randomized to receive either talc or SN through the chest tube. The randomization was accomplished by blindly selecting a piece of paper from a box that originally contained 60 small pieces of paper printed with either "silver nitrate" or "talc." As soon as the initial drainage had stopped, the patient was requested to cough to be sure that the pleural cavity was empty. The pleural sclerosant was then injected. The pleural injectate consisted of 5 g sterilized talc diluted to a total volume of 50 mL with saline solution or 20 mL 0.5% SN (Merck; Darmstadt, Germany). The talc preparation used was asbestos-free with a mean length of 25.4 µm (range, 6.4 to 50.5 µm) [USP Pharmacy; Sao Paulo, Brazil]. After the sclerosant was injected, the chest tube was clamped for 1 h, and the patient was placed in the prone, supine, and right and left decubitus positions for periods of 10 to 15 min. The chest tube was then unclamped and placed on suction of –20 cm H2O. Serial radiographs were used to document appropriate lung reexpansion. The first was performed 24 h after the intrapleural injection. The patients were followed up every day, and the chest tube was removed when the amount of fluid collected in the previous 24 h was < 100 mL. They were clinically evaluated before and after treatment regarding pain using a linear scale of 0 to 10 (0, no pain; 10, the worst pain ever felt).11 The patient was asked to provide a number describing their pain. Chest radiographs were obtained immediately following tube removal and at their monthly follow-up visits. Patients were requested to return at monthly intervals for 4 months. At these visits, patients were considered to have a successful pleurodesis if there was no recurrence of the pleural effusion. Patients who did not have a pleurodesis at one of their visits were excluded from subsequent visits.

Statistical Analysis
The data are expressed as the mean ± SE and the median. Information was processed using a statistical software package (Sigma Stat; San Rafael, CA). The Student unpaired t test was used for comparisons between the two groups for continuous variables. The {chi}2 test was used for comparisons between the two groups for proportions.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Sixty patients received an intrapleural injection with talc or SN. Eleven patients were excluded from the study because they were unavailable for follow-up at 30 days. It is unknown whether any of these patients died or had a recurrent effusion during the 30-day follow-up period. The remaining 49 patients were considered to be appropriate for analysis because they were seen for a follow-up visit and had undergone a chest radiograph at least 30 days post-pleural injection. The groups were similar in age (p = 0.22), sex (p = 0.70), Karnofsky index score (p = 0.94), and pathology (p = 0.68) [Table 1 ].


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  		Table 1.. Description of Group Data*

 
Following the treatment (Tables 2 , 3 ), subjective pain was low and similar with both sclerosants. The pain was greatest on the first day and thereafter it diminished. The mean pain did not differ between groups on any of the 5 days (Table 2). The total fluid drainage after the induction of pleurodesis was not statistically different (p = 0.36) between SN (901 ± 125 mL) and talc (766 ± 74 mL). After the intrapleural injection, five patients in the SN group and three patients in the talc group developed a transient elevation of temperature (ie, to > 37.8°C). The mean number of days spent in the hospital was nearly the same in the group that received intrapleural SN (3.7 ± 0.15 days) and in the group that received talc (3.6 ± 0.13 days). None of the patients who returned for follow-up had significant long-term adverse affects from the pleurodesing agents. However, significant long-term adverse effects cannot be ruled out, since nearly 20% of the patients were lost to follow-up and the follow-up period in the remaining patients was relatively short.


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  		Table 2.. Pain Score After the Intrapleural Injection of the Sclerosing Agent*

 

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  		Table 3.. Comparison of Pain Scores, Drainage, Temperature, and Hospitalization in the SN and Talc Groups*

 
Both SN and talc were found to be effective pleurodesis agents in the present study (Table 4 ). Thirty days after undergoing the procedure, 23 of 24 patients (96%) who had received intrapleural SN and 21 of 25 patients (84%) who had received talc had not experienced a recurrence of their pleural effusion. There was no statistically significant difference between the groups (p = 0,349). Similar results were observed after 60 days (SN group, 18 of 18 patients [100%]; talc group, 13 of 13 patients [100%]; p > 0.99), 90 days (SN group, 16 of 16 patients [100%]; talc group, 8 of 9 patients [89%]; p = 0.360), and 120 days (SN group, 4 of 4 patients [100%]; talc group, 4 of 4 patients [100%]; p > 0.99).


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  		Table 4.. Follow-up*

 

   Discussion
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 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Chemical pleurodesis is the procedure of choice in the management of recurrent pleural effusions. Once a patient is considered to be appropriate for pleurodesis, a sclerosing agent must be chosen. The ideal sclerosant should produce, in the shortest possible time, an effective and safe obliteration of the pleural space. At the present time, talc, doxycycline, and bleomycin are the sclerosing agents most commonly used.

In the 1960s, antineoplastic agents, particularly nitrogen mustard, were most commonly used for pleurodesis.12 When it was realized that it was the fibrosing effects rather than the antineoplastic effects of the agents that was responsible for producing the pleurodesis, nonspecific irritants such as tetracycline and talc were also used for pleurodesis. However, some clinicians continue to use antineoplastic agents. At the present time, bleomycin is the antineoplastic agent that is most commonly used for pleurodesis.13 This is probably because it is the only antineoplastic approved for this purpose by the Federal Drug Administration. However, there is no evidence that bleomycin is superior to other antineoplastic agents (approximately 70%) for use in pleurodesis.1 In addition, it should be noted that bleomycin does not produce pleurodesis in rabbits,14 as do other antineoplastic agents such as mitoxantrone or nitrogen mustard.1516

In the 1980s, tetracycline was the most commonly used sclerosing agent, primarily because a study17 in rabbits demonstrated that it was the most effective agent. However, since the late 1980s tetracycline has not been commercially available in most countries. Subsequently, it was shown that doxycycline was comparable in efficacy to tetracycline. When tetracycline became unavailable, the use of talc as a pleurodesis agent increased rapidly, and it is the agent most commonly used for pleurodesis at the present time.13 It is the choice of many physicians due to its low cost, wide availability, and effectiveness.

The primary problem with talc is that it has been incriminated in causing ARDS, which is fatal in approximately 1% of patients who receive it intrapleurally.18 ARDS can occur after talc is administered either by insufflation or as a slurry.18 The mechanism for ARDS in this setting is not definitely known, but it has been hypothesized that it is due to the systemic absorption of small talc particles.19 Since the life expectancy of patients with malignancy is limited, this would not necessarily mean that talc should be avoided if it were significantly more effective than the other agents. Although it has been stated that talc is 95% effective and that it is much more effective than other agents, some have questioned this statement. In one analysis20 of 433 patients who had been subjected to pleurodesis with talc, tetracycline derivatives, or bleomycin, talc was no more effective than the other agents (all agents were approximately 80% effective). In a study21 from Australia, the insufflation of talc at thoracoscopy in 66 patients with MPEs resulted in complete control in only 52%. Therefore, other agents should be considered.

The intrapleural injection of SN, with the objective of producing effective pleurodesis, was proposed in the 1940s. It was first used in 1942 by Brock22 to produce aseptic pleural adhesions. In 1948, the same author proposed the intrapleural instillation of 10% SN for the treatment of spontaneous pneumothorax.23 Since then, SN has been used sporadically.

High concentrations are effective in humans with pneumothorax. Andersen and Poulsen24 sprayed the lung surface with 10% SN during thoracoscopy in 23 patients with spontaneous pneumothorax. There were no significant side effects from the procedure. The authors reported only one recurrence during a follow-up period of up to 8 years. Wied and coworkers10 reported that there was no recurrence in 16 patients with spontaneous pneumothorax who had been treated with 10% SN over a follow-up period of 5 to 19 months. The efficacy of SN was further confirmed in the report of Hopkirk and coworkers.25 They treated 152 members of the British Air Force who had experienced an episode of spontaneous pneumothorax with a 10% SN solution. The recurrence rate after the procedure was 7% with a follow-up period of 5 years.25

Lower concentrations may also be effective. Stowe and coworkers26 instilled a 1% SN solution in 10 patients and reported only one recurrence. In contrast, Schuster and coworkers27 injected a 1% SN solution into the pleural space of eight patients and reported that three patients had a recurrence. Although some authors suggested that it was the agent of choice for pleurodesis, its use was abandoned, probably due to severe pain and the occurrence of large pleural effusions.10

The mechanism by which sclerosing agents produce pleurodesis is unknown. The creation of a pleurodesis is usually initiated by producing an injury to the pleura. The degree of injury is important in determining whether a pleurodesis will result, and it is important to produce the correct degree of injury. We think that the intrapleural injection of a 10% SN solution injures the pleura too severely, resulting in severe pain and large pleural effusions.

However, since similar results were obtained in humans for pleurodesis with SN concentrations from 1 to 10%, we hypothesized that lower concentrations of SN might produce a degree of pleural injury sufficient to induce pleurodesis without the severe pain and large effusions.8 This hypothesis was confirmed in rabbits. A low concentration of SN (0.5%) was as effective as tetracycline (35 mg/kg)7 and was more effective than talc (400 mg/kg).8 It produced a greater degree of macroscopic and microscopic fibrosis, and was associated with the presence of more collagen.8 The lung damage, represented by alveolar collapse, was moderate during the first 30 days after treatment, and subsequently had a clear tendency to normalize over time.28

In the present study, we compared the efficacy of talc slurry and administration of low concentrations of SN in controlling MPEs in humans. Both sclerosing agents were effective, with no statistically significant difference between them. One month after the local treatment, the pleural effusion was controlled in 84% of patients (21 of 25 patients) who received the talc slurry and in 96% of those (23 of 24 patients) who received SN. It should be noted that the study was underpowered to detect a significant difference. If the administration of talc slurry is effective in 84% of patients and SN is effective in 96% of patients, 190 patients would have to be enrolled to have a test power of 0.80. It should also be noted that the SN group contained more patients with breast cancer, and one might expect these patients to have a better result with pleurodesis than those with other malignancies, particularly, lung cancer.

No significant problems with pain were observed in any of the patients. The medium peak pain score obtained during the hospitalization period (talc group, 3.6; SN group, 3.7) indicated only mild-to-moderate pain that was similar in both groups. Although no other significant side affects either in the short term or the long term were observed in this study, we cannot draw unequivocal conclusions regarding the safety of SN, since the number of patients receiving SN was small, nearly 20% of the patients were lost to follow-up, and overall the follow-up period was relatively short.

One shortcoming of the present study is that 11 of the 60 patients were lost to follow-up. Although it would be nice to obtain follow-up information on these patients, this is virtually impossible in Brazil. In Brazil, many patients do not have telephone numbers, good addresses for next of kin, or national identifying numbers like a social security number. It is possible that the higher rate of loss to follow-up in the SN group is due to a higher death rate, a higher recurrence rate, or more significant side effects. Only a study with a larger number of patients and more complete follow-up would be able to evaluate this possibility. In the worst-case scenario, assuming that all patients lost to follow-up had a recurrent pleural effusion, the rate of recurrence at 30 days in the SN group (10 of 33 patients; 30%) did not differ significantly from that in the talc group (6 of 27 patients; 22%) [{chi}2 = 0.17; p = 0.68]. However, the power of the test was only 0.065. Another shortcoming of the present study is that the investigators were not blinded to the treatment. This could have resulted in some bias in the interpretation of pain or the results of the pleurodesis.

In conclusion, the present study demonstrates that SN was an effective agent for producing a pleurodesis in this small group of patients. It appears to be at least as effective as talc. Moreover, the side effects of intrapleural SN at a concentration of 0.5% appear to be minimal and were comparable to those with talc, although the small number of patients and the large percentage lost to follow-up make it impossible to draw an unequivocal conclusion regarding the safety of SN. Other advantages of SN are that it is available throughout the world and is inexpensive. In Brazil, the cost for 5 g talc is $2.00, while the cost for 20 mL 0.5% SN is $3.00. Since SN appears to be as effective as talc, and since there is no evidence that the intrapleural injection of SN produces ARDS, it should be considered to be a viable alternative to talc and other sclerosing agents for the production of a pleurodesis.


   Footnotes
 
Abbreviations: MPE = malignant pleural effusion; SN = silver nitrate

This study was supported by the Foundation to Support Research from the State of São Paulo (FAPESP) and by the National Board of Scientific and Technologic Development (CNPq) of Brazil.

Received for publication September 11, 2003. Accepted for publication January 21, 2005.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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