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REVIEW

C URRENT
OPINION Advances in the management of malignant
pleural effusion
Labib G. Debiane and David E. Ost

Purpose of review
The current review describes the latest evidence in the management of malignant pleural effusions (MPE).
Recent findings
Daily drainage of indwelling pleural catheters achieved auto-pleurodesis at a higher rate compared with
every-other-day drainage [0.47 vs. 0.24; difference in proportion of 0.23; 95% confidence interval (CI)
0.08 0.38; P 0.003]. In patients with MPE undergoing talc pleurodesis, a large multicenter randomized
clinical trial found that pain control with opiates vs. nonsteroidal anti inflammatory drugs (NSAID) group
were not significantly different (mean visual analog scale of 23.8 vs. 22.1 mm, respectively, adjusted
difference 1.5 mm; 95% CI 1.33.4; P 0.40). NSAID use was found to be noninferior to opiates with
respect to the rate of pleurodesis failure at 3-month follow-up (prespecified noninferiority margin 15%,
failure rates 20% opiates vs. 23% NSAIDS, respectively, difference 3%, 95% CI 10% to 1; P 0.004
for noninferiority). Talc remains the most effective sclerosing agent based on multiple systematic reviews
and meta-analyses.
Summary
More prospective studies are needed to determine the optimal frequency of indwelling pleural catheters
drainage. NSAIDS can be used for pain control and do not adversely impact the chance of successful
pleurodesis.
Keywords
indwelling pleural catheter, malignant pleural effusion, pleurodesis, sclerosing agent, thoracoscopy

INTRODUCTION
Malignant pleural effusions (MPE) are commonly encountered among cancer patients. They significantly
impair quality of life and constitute a major source of distress for both patients and their families. Although the
exact annual incidence of MPE in the United States is unknown, it is estimated to be greater than 150 000 cases
per year [1]. In addition to being a great burden on society, MPEs are associated with increased healthcare
expenditures. Based on the Nationwide Inpatient Sample database for year 2012, the hospital charges for the
MPE-related admissions are estimated to exceed 5 billion US dollars per year [2,3]. The focus of this review is
to shed light on the latest clinical trials and research studies conducted in the past 1 2 years exploring various
aspects of the management of MPEs.

CAUSE
A pleural effusion is called malignant when the pleural fluid demonstrates the presence of exfoliated

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malignant cells on cytopathologic examination or when pleural tissue biopsy reveals presence of malignant cells
[4]. A large number of cancers can result in metastatic disease to the pleura. The most common is lung cancer
followed by breast cancer. Together these two cancers account for more than 50% of all MPEs [5]. Other causes
of MPE include lymphoma, genitourinary cancers, gastrointestinal cancers, and cancers of unknown primary
[5 7]. Malignant pleural mesothelioma is another cause of MPE but is a rare disease with an age adjusted
incidence of 0.9117 cases per 100 000 population in the United
States in 2013 [8].

Department of Pulmonary Medicine, MD Anderson Cancer Center, Houston, Texas, USA


Correspondence to David E. Ost, MD, MPH, Department of Pulmonary Medicine, MD Anderson Cancer Center, 1515 Holcombe Blvd, Unit 1462,
Houston, TX 77030, USA.
Tel: +1 713 792 3962; e-mail: DOst@mdanderson.org
Curr Opin Pulm Med 2017, 23:000000 DOI:10.1097/MCP.0000000000000392

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Neoplasms of the lung with imaging

KEY POINTS
Patients with MPE have a limited survival and
identifying prognostic indicators can assist physicians
in personalizing treatment strategies.
In patients with recurring MPE, indwelling pleural
catheters provide significant symptom relief, are well
tolerated, have a low complication rate, and can be
done on an entirely outpatient-basis.
Talc is the most effective sclerosing agent.

For patients with MPE undergoing talc pleurodesis,


NSAIDS can be used for pain control and do not
adversely impact the chance of successful pleurodesis.

In the 1980s, Sahn [4,9] introduced the term paramalignant effusions for patients who did not have
direct involvement of their pleura with tumor and when no other causes were established for the pleural
effusion. Paramalignant pleural effusions can result from local tumor effects (such as lymphatic obstruction,
super vena cava syndrome, and trapped lung), systemic effects of tumor (such as pulmonary embolism and
hypoalbuminemia), and complications of chemotherapy and radiation therapy [10]. As paramalignant
effusions behave clinically in a similar manner to MPE, they are often managed the same way. In this
review, the indications for treatment and the management options that we discuss apply to both malignant
and paramalignant effusions.

PROGNOSIS
Patients with MPE have a poor prognosis with a reported overall median survival ranging from 2.8 to 6.8
months [11 13]. However, although median survival is low, there is significant variability between
patients, depending on the type of under- lying malignancy and their performance status at time of MPE
diagnosis [12,13]. As the optimal management strategy of MPE is affected by overall survival, identifying
prognostic indicators and developing predictive models can assist physicians in personalizing treatment
strategies.
Using three large international prospectively collected databases of patients with MPE, Clive et al. [12]
developed and validated a clinical prognostic scoring system (0 7) using pleural fluid Lactate
Dehydrogenase, the Eastern Cooperative Oncology Group (ECOG) performance score, the neutrophil-to-
lymphocyte ratio, and the tumor type (LENT score). Median survival in the low-risk group (LENT score 0 1)
was 319 days, in the moderate-risk

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group (LENT score 2 4) was 130 days, and in the high-risk group (LENT score 5 7) was 44 days. Com- pared with
ECOG alone, the LENT score resulted in better prediction of survival at 1, 3, and 6 months from diagnosis [12]. The
LENT score still needs to undergo prospective validation [14].
Two other recent studies in 2016 looked at prognostic factors for MPE. The first study evaluated a cohort of
patients with non small cell lung carcinoma and MPE. They found on multivariate analysis that a high serum C-
reactive protein level (>5.0 mg/ dl), a low serum albumin level (<3.4 g/dl), a low pleural protein level (4.7 g/dl),
and the presence of distant metastasis were associated with a shorter survival [15]. The second study looked
strictly at MPE in patients with good performance status (ECOG score 02) and showed that a low pleural fluid
albumin (<2.5 mg/dl), a high neutrophil-to- lymphocyte ratio (>5), and the presence of gastro- intestinal
malignancy were significantly associated with increased mortality [16].

MANAGEMENT OF MALIGNANT PLEURAL EFFUSIONS

Indications for treatment


The main indication to treat MPE is to relieve dyspnea [1]. Along with chest pain, dyspnea is the most common
symptom associated with MPE and significantly affects quality of life [17]. As the goal of treatment is palliation of
dyspnea, selection of a management strategy needs to take into consider- ation patient-centered outcomes, such as
improving health-related quality of life, remaining free of dyspnea, minimizing invasive procedures, and avoiding
inpatient hospital stays when possible [18]. Diagnosis of MPE is usually established by thoracentesis. If MPEs
subsequently recur, the three main management options for achieving palliation of dyspnea are repeat
thoracentesis, indwelling pleural catheters (IPCs), and pleurodesis.

Thoracentesis
One key factor to consider when selecting a management strategy for MPE is to assess whether the pleural fluid is
recurring at a slow or fast pace after the initial thoracentesis. For patients with slow fluid reaccumulation, a short
life expectancy (typically less than 1 month) and a poor performance status, it is reasonable to perform a repeat
thoracentesis on an as needed basis [1,5]. Repeat thoracentesis in this context can be done in the outpatient setting
at fairly low risk. In select cases of patients with very limited life expectancy, this may be the best option.

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Advances in the management of malignant pleural effusion Debiane and Ost

For patients with rapid recurrence of symptomatic MPE that have longer life expectancies, a repeat
thoracentesis strategy becomes less desirable as it can cause pleural inflammation and fibrin formation
resulting in loculation of the pleural space [19]. More suitable options include placing an IPC or performing a
pleurodesis (chemical or mechanical). Less common interventions include pleurectomy, usually used in
patients with MPE due to mesothelioma.

Indwelling pleural catheters


IPCs are silicone drainage tubes with a one-way valve that are inserted in the pleural cavity, tunneled under
the skin, and secured subcutaneously by a Teflon cuff [20]. They allow intermittent out- patient drainage by
the patient, or the patients caregiver, and as such eliminate the need for returning clinic visits for repeat
thoracentesis. The pleural cavity can be drained daily or every other day.
IPCs are indicated for the relief of symptoms in situations in which pleurodesis is expected to have a high
failure rate from the inability of the lung to fully re expand [21]; such conditions include untreatable
endobronchial obstruction and any cause of irreversible lung entrapment. Complications are rare with the
most commonly encountered being wound site infection (4%), clogging of IPC (3%), trapped lung with
hydropneumothorax (2%), IPC dislodgement (1%), and empyema (1%)
[11].

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The use of IPC has gained popularity in the last decade because it is less invasive and is an entirely
outpatient-based approach for the management of recurring MPE [22,23]. It relieves dyspnea significantly, with
the greatest improvements in utility being associated with more severe dyspnea at base- line and the use of
subsequent chemotherapy and/or radiotherapy after IPC placement [11].
The ultimate goal of MPE management is to prevent symptomatic recurrence. A large body of the IPC
literature uses the terms spontaneous pleurodesis to imply the absence of symptomatic ipsilateral recurre nce.
The reported rate of spontaneous pleurodesis from IPCs is variable and was found in a recent systematic
review of the literature to be around 45% [24] with a mean time top leurodesis ranging from 26 days to 90 days
[24 26]. Pleural fluid recurrence requiring repeat interven- tions usually occur in 7.9 9% [11,23,25]. In our
institution, we used the algorithm listed in Fig. 1, and fluid recurrence requiring repeat procedures was seen in
9% of patients whose IPCs were electively removed (due to decreased fluid drainage) [11].
The optimal frequency of IPC drainage to
achieve spontaneous pleurodesis remains undetermined. Recently, a multicenter randomized con- trolled trial
(ASAP Trial) was conducted by Wahidi et al. [27 ] and compared a daily drainage strategy (aggressive) to an
&&

every other day pleural fluid drainage approach (standard). The primary end- point of the study was the
incidence proportion of auto pleurodesis at 12 weeks post-IPC insertion.

FIGURE 1. Standardized indwelling pleural catheters Drainage Algorithm (University of Texas MD Anderson Cancer Center).
CXR, chest radiograph; IPC, indwelling pleural catheter. Reproduced with permission from [11].

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Neoplasms of the lung with imaging

The authors definition of auto pleurodesis was low fluid drainage ( 50 ml) on three consecutive drain- age
procedures with concurrent resolution of effusion-related symptoms. Although the amount of pleural
effusion on chest radiograph was evaluated, it did not play a major role in defining the primary outcome.
Patients in the aggressive drainage arm achieved auto pleurodesis at a higher rate compared with the
standard drainage arm [0.47 vs. 0.24; difference in proportion of 0.23 with 95% confidence interval (CI) (0.08;
0.38) and P 0.003] [27 ]. It is worth noting that there was a disparity in the percentage of patients who
&&

were unable to complete the study in the aggressive and standard arms (12 vs. 29%, respectively) and in the
percentage of patients who died prior to the end of the study (25 vs. 34%, respectively) [27 ]. The incidence
&&

proportion com- parison at 12 weeks has inherent technical limitations as it cannot deal with competing
risks and loss to follow-up easily. Irrespective of how early or late death occurred, the authors chose to
count death as failure to achieve
auto pleurodesis at 12 weeks. As death can be a type of informative
censoring, a competing risk model would have been more suit- able. So although this study is an important
and informative study for use of IPC in the treatment of MPE, it is not defi nitive because of these
methodologic limitations. More studies addressing the optimal frequency of fluid drainage are needed
before widespread definitive recommendations can be made.

Pleurodesis
Pleurodesis obliterates the pleural space by promoting a symphysis between the visceral and parietal
pleurae, preventing the reaccumulation of either air or liquid in the pleural space [28]. A complete apposition
between the pleural linings is desirable as it improves the chances of a successful pleurodesis

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[28]. While mechanical pleurodesis is achieved by the physical irritation of the pleura (such as pleural abrasion
with a rough-surfaced pad [29] or repetitive pleural irritation by an IPC), chemical pleurodesis involves the
intrapleural instillation of a sclerosing agent. This can be achieved thoracoscopically or via a chest tube.
At the present time, there are no clear guidelines describing when to proceed with IPC vs. pleurodesis as a first
line management. Two randomized con- trolled trials compared IPCs with chemical pleurodesis using chest tubes
with talc slurry: the CALGB and TIME2 trials. The CALGB trial concluded that IPC was associated with greater
relief of dyspnea. The authors acknowledged however that their study was limited and closed early due t o slow
accrual and difficulty in randomization that resulted in increased type I error and a reduced statistical power to
detect infrequent events [30]. The multi- center TIME2 trial found no significant difference between IPC and talc
slurry pleurodesis via a chest tube in relieving dyspnea at 42 days in patients with MPE, although dyspnea
improvement was greater in the IPC group at 6 months [31]. In general, pleurodesis can be offered to patients with
MPE with an expected survival of more than 3 months and with good pleural apposition, particularly if the patient
prefers a single definitive procedure [32].

Sclerosing agents
Multiple agents have been used including talc, doxycycline, tetracycline, and iodopovidone, among others. As
indicated by multiple meta-analyses and systematic reviews of the literature [33,34,35 ], talc appears to be the
&

most effective sclerosing agent (Fig. 2). In the last 2 years, new investigative studies compared different sclerosing
agents.
Talc powder pleurodesis was compared with povidone iodine pleurodesis by Ibrahim et al. [36] in a
prospective randomized trial. Successful

FIGURE 2. Talc poudrage during right-sided pleuroscopy. Pleuroscopy with talc poudrage was performed in the right
hemithorax to achieve pleurodesis in a patient with metastatic adenocarcinoma of the lung (right upper lobe) and recurrent
symptomatic right malignant pleural effusion: (a) before talc poudrage and (b) during talc poudrage.

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Advances in the management of malignant pleural effusion Debiane and Ost

pleurodesis was achieved in 80.9% in the talc group compared with 72.2% in the povidone iodine group (P
0.519) in which success was defined as a normal chest radiograph or radiological reaccumulation of fluid
without recurrence
of dyspnea. In another prospective randomized trial conducted, the efficacy and safety of
autologous blood pleurodesis (ABP) compared to pleurodesis with tetracycline was assessed in patients with
symptomatic MPE [37]. Successful pleurodesis at 1 month in the ABP and tetracycline groups was achieved in
83.4 and 87.5%, respectively (P 0.36), in which success was defined as either complete (no pleural effusion
detected) or partial response (minimal pleural fluid without the need for repeat drainage). In both studies,
samples sizes were small and power calculations were not provided.
A group of investigators from Japan conducted a
propensity score-matched comparison of the efficacies of OK-432 and talc slurry pleurodesis in patients with
adenocarcinoma of the lungs and MPE [38]. The 30-day success rate was 80.7% for OK-432 and 76.9% for talc
slurry (Odds Ratio 1.26, 95% CI 0.334.77, P 0.73). Neither the 90-day success rates nor the overall incidence
of adverse events differed significantly. A limitation of the study is that the OK-432 dose varied between
patients. Knowing that OK-432 was shown in prior studies to produce dose-dependent effects during
pleurodesis procedures
[39], its success rate might have been underestimated.

Pain management
One of the main challenges physicians face when performing chemical pleurodesis is pain control.
Traditionally, opiates have been favored by most physicians over the use of nonsteroidal anti inflammatory
drugs (NSAIDs) for pain management fol- lowing talc pleurodesis. This stems from a concern that NSAIDs
may suppress the acute inflammatory reaction and decrease the efficacy of pleurodesis [40 ]. In a 2 2
&&

factorial randomized controlled design (TIME1 trial), Rahman et al. assessed the effect of NSAIDs compared
with opiates for the outcomes of pleurodesis pain control (superiority trial) and pleurodesis failure rates (non
inferiority trial). Although all patients were allowed to have acetaminophen, th e NSAIDs arm received oral
ibuprofen 800 mg three times daily, and the opiate arm received oral morphine 10 20 mg four times daily.
Breakthrough intravenous morphine was allowed in both groups after a maximum dose of either medications
had been reached. Pain score was measured using a 100-mm visual analog scale (VAS) in which 0 mm
indicated no pain. Pleurodesis failure was defined as the need for pleural intervention to

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relieve dyspnea during the 3 months post randomization.
The study failed to demonstrate a difference between NSAIDs and opiates for overall pain control in patients
with MPE who underwent pleurodesis and chest tube placement (VAS of 23.8 15.8 mm and 22.1 16.9 mm for
opiates and NSAIDs, respectively, adjusted mean VAS difference 1.5 mm, 95% CI 5.0 to 2.0 mm, P 0.40).
However, patients on NSAIDS received more rescue pain medications (P 0.003).
For the outcome of pleurodesis failure, the inves- tigators chose
T a noninferiority margin of 15%. So if the
lower bound of the 1-sided CI for the difference between opiates and NSAIDs was more positive than 15%, then
NSAIDs would be considered noninferior to opiates for the outcome of pleurodesis failure. NSAIDs were found
to be noninferior to opiates with respect to the rate of pleurodesis failure at 3 months using these criteria

(pleurodesis failure rates were 20 and 23% for opiates and NSAIDs, respectively, differ- ence 3%, 1-sided 95% CI
10% to ,P 0.004 for
noninferiority).

Chest tube size


To address the question of optimal chest tube size for pleurodesis, the TIME1 trial investigators also studied
tubes compared
within the same 2 2 factorial design the effect of small (12 Fr) chest with larger
1 (24 Fr) chest
tubes on pain (superiority trial) and success of talc pleurodesis (non inferiority trial) [40 ]. All patients
&&

undergoing thoracoscopy guided talc poudrage pleurodesis had a 24-Fr chest tubes placed per local practice
guidelines whereas the talc slurry group were randomized to 24 Fr (n 56) vs. 12 Fr (n 54) chest tubes. So the
results for chest tube size are only relevant to talc slurry.
Compared with large chest tubes, small chest tubes resulted in lower pain scores (mean VAS scores
22.0 16.6 mm vs. 26.8 16.9 mm, respectively, P 0.04). However, T given that the
T clinically signifi- cant
threshold for the VAS pain score was set at 13 mm, the magnitude
of the difference would not be considered
clinically large [40 ].
&&

Using the same noninferiority margin of 15%, pleurodesis failure rates were lower with large chesttubes
than small chest tubes (30 vs. 24%), but this failed to meet the noninferiority criteria (risk differ- ence 6%, 1-
sided 95% CI 20% to, P 0.14 for noninferiority). So whether or not smaller tubes are noninferior to larger tubes
remain unknown [40 ].
&&

1
CONCLUSION
MPEs significantly impact quality of life and constitute an economic burden. The advent of IPCs has

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Neoplasms of the lung with imaging

the potential to transform the management of MPEs to an entirely outpatient treatment approach,
consistent with patient centered outcomes. More prospective studies, however, are needed to guide
physicians as to what constitutes the optimal frequency of IPC drainage. When pleurodesis is per- formed,
the available evidence suggests that talc has the best efficacy among the various sclerosing agents. NSAIDS
can be used for pain control and do not adversely impact the chance of successful pleurodesis.

Acknowledgements
None.

Financial support and sponsorship


None.

Conflicts of interest
There are no conflicts of interest.

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Papers of particular interest, published within the annual period of review, have
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& of special interest

&& of outstanding interest

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The importance of this 2 2 factorial phase 3 randomized clinical trial is that it showed that nonsteroidal anti-inflammatory drugs
can be used for pain control and do not adversely
impact the chance of successful pleurodesis.

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