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Eur J Cardiothorac Surg 2004;26:432-436
© 2004 Elsevier Science NL

Impact of pleural effusion pH on the efficacy of thoracoscopic mechanical pleurodesis in patients with breast carcinoma

A. Crnjaca*, M. Sokb, M. Kamenikc

a Department of Thoracic Surgery, Teaching Hospital Maribor, Ljubljanska 5, 2000 Maribor, Slovenia
b Department of Thoracic Surgery, University Medical Centre Ljubljana, Ljubljana, Slovenia
c Department of Anaesthesiology, Teaching Hospital Maribor, Maribor, Slovenia

Received 5 January 2004; received in revised form 9 March 2004; accepted 15 March 2004.

* Corresponding author. Tel.: +386-2-3211420; fax: +386-2-3324830
e-mail: crnjac{at}sb-mb.si


   Abstract
Top
 Abstract
1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
 5. Conclusion
 References
 
Objective: A prospective randomised study was conducted to compare the efficacy of treating malignant pleural effusions (MPE) in patients with breast carcinoma by thoracoscopic mechanical pleurodesis (TMP) as a new palliative treatment and talc pleurodesis (TP) at various pleural fluid pH levels and to determine whether at low pH values, when the success of TP is reduced, TMP is more successful. Methods: 87 female patients with breast carcinoma and a resulting MPE resistant to systemic therapy were divided into two groups: TMP and TP groups. In the TMP group 24 patients with pH levels above 7.3 and 21 patients with pH levels below 7.3 underwent thoracoscopic parietal and visceral pleural abrasion utilising general anaesthesia. In the TP group, 22 patients with pH levels above 7.3 and 20 patients with pH levels below 7.3 were administered 5 g of sterile talc, dissolved in 100 ml of physiological solution, via a chest tube, utilising local anaesthesia. Postoperative follow-up was performed to determine a possible recurrence of MPE with periodic radiographs, the duration of chest tube drainage and hospitalisation, occurrence of complications, and perioperative mortality. The following was used for statistical analysis: t-test for odd samples, {chi}2 test, logistic regression, and multiple linear regression. Results: TMP and TP were equally successful (92 and 91%) in patients with pH levels above 7.3. Differences occurred in patients with pH below 7.3 (81 and 55%) (P=0.07). The lowest pH value at which TMP proved successful was 7.06, while for TP this value was 7.25. In TMP group the average duration of chest tube drainage amounted to 3.8 days and hospitalisation to 5.5 days, while in TP group it was 5.6 and 7.5 days, respectively. Differences were statistically significant (P<0.05). 16% of easily treatable complications and no case of perioperative mortality were identified in TMP group, while 26% of complications and four cases of perioperative mortality were noted in TP group. Conclusions: TMP is a safe palliative treatment for MPE in breast carcinoma, with a minimal number of complications and a short hospital stay; it is more successful than TP in patients with pH of MPE below 7.3.

Key Words: Breast carcinoma • Malignant pleural effusion • pH • Video-assisted thoracic surgery • Mechanical pleurodesis


   1. Introduction
Top
 Abstract
 1. Introduction
2. Patients and methods
 3. Results
 4. Discussion
 5. Conclusion
 References
 
Carcinoma is the second most frequent cause of pleural effusions in patients aged over 50 years. 40% of all pleural effusions are due to a malignant neoplasm [1]. Breast carcinoma is the underlying cause in approximately 25% of all malignant pleural effusions (MPE) [2]. Approximately 50% of patients with breast carcinoma develop an MPE during their illness [3]. Although MPE signifies an advanced stage of the underlying disease, patients with breast carcinoma are not considered to be in the terminal stage of disease, as survival can be several months or years [2] after a successfully treated effusion. Patients suffer from the original disease, while MPE causes respiratory distress, chronic cough and pain resulting in a significantly lower quality of their remaining life.

Approximately one-third of MPE have pH below 7.3, which is a consequence of impaired transport of the end products of glucose metabolism in pleural fluid through the pleura, changed due to tumour infiltration and fibrosis, and an accumulation of hydrogen ions in pleural fluid [2,4].

In practice, talc pleurodesis (TP) is most often used as palliative treatment for recurrent MPE, its success rate being approximately 90% without relapse [5–7]. While most authors report that the success of TP drops considerably in malignant effusions with pleural pH below 7.3 [8–10], others found no such relationship [7].

Since 1993, a new palliative technique, thoracoscopic mechanical pleurodesis (TMP), for treating recurrent MPE has been developed by the Department of Thoracic Surgery of Maribor Teaching Hospital. Our experience revealed a high success rate (93.2%) of TMP in managing recurrent MPE. In the present study we have attempted to determine whether changed pH values have an impact on the efficacy of TMP.


   2. Patients and methods
Top
 Abstract
 1. Introduction
 2. Patients and methods
3. Results
 4. Discussion
 5. Conclusion
 References
 
2.1. Patient grouping
The prospective randomised study included 87 female patients with breast carcinoma and a resulting morphologically confirmed MPE, hospitalised at the Department of Thoracic Surgery of Maribor Teaching Hospital between June 1996 and June 2003. Patients not fit to undergo surgery under general anaesthesia because of the primary or accompanying diseases were excluded from the study. Randomisation was performed using the sealed envelope method. The research was approved by the National Medical Ethics Commission.

On hospital admission, the time span between the onset of breast carcinoma treatment and the occurrence of MPE was calculated for all patients. A therapeutic thoracentesis was performed, the volume of fluid measured, and the fluid sample sent to a laboratory for pH measurement, cytological and bacteriological analyses. To exclude errors in pH values caused during transport to the laboratory, samples were taken under sterile conditions and transported in heparinised syringes on ice. pH values were determined within 1 h after sampling in a manner analogous to that for arterial pH values by using a blood gas analyser (AVL 990).

Samples for histological verification were collected preoperatively using blind needle biopsy or by targeted biopsy during the video-assisted thoracic surgery (VATS) procedure.

Patients were assigned to two groups depending on the MPE treatment method (TMP group: thoracoscopic mechanical pleurodesis; TP group: talc pleurodesis). Within each group, patients were classified according to pH values of MPE.

2.2. Surgical methods
TMP was performed utilising general anaesthesia with double lumen orotracheal intubation allowing for ipsilateral lung collapse. Patients were placed in a lateral decubitus position as for posterolateral thoracotomy. The trocar for thoracoscope was inserted through the fifth or sixth intercostal space in the mid axillary line. Two working portals were also used. A thorough inspection of the pleural cavity, lysis of possible adhesions (to ensure lung expansion) and biopsy of suspected areas were performed prior to pleurodesis. This was followed by the scarification of parietal and visceral pleura to induce petechial bleeding, resulting in a diffuse inflammatory response and fibroplasia. After scarification, the anaesthesiologist administered artificial ventilation to ensure lung expansion. The chest tube, inserted in one of the working portals, was removed when its drainage was below 100 ml over 24 h.

Patients treated by TP had a chest tube inserted through the fifth or sixth intercostal space in the mid axillary line under local anaesthesia. Five grams of sterile talc dissolved in 100 ml of physiological solution were insufflated. Patients were given 100 mg of pethidine an hour before the procedure. The drain was removed when drainage was below 100 ml over 24 h also in the case of these patients.

2.3. Data collection and statistical methods
The following data were collected from the patients:

  1. recurrence of pleural effusion after 1 day, 1 week, 1 month, 3 months, and 6 months (signs of pleural effusion on conventional and/or lateral decubitus radiographs);
  2. the lowest value of MPE pH at which the methods were still effective;
  3. time of chest tube drainage and hospitalisation (economic factor);
  4. complications after individual treatments;
  5. perioperative mortality (30-day mortality) and mortality after 6 months.

We were interested in possible relationships between the interval from the onset of the disease till the occurrence of pleural effusion, the volume of pleural fluid, patients' age, pH value, and treatment efficacy in each group.

The following was used in statistical analysis: t-test for odd samples, {chi}2 test, logistic regression, and multiple linear regression. The statistical significance threshold was set at P<0.05.


   3. Results
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
4. Discussion
 5. Conclusion
 References
 
Preoperative characteristics of the study population by groups are given in Table 1.


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  		Table 1. Patients' demographic data for both groups

 
Between the groups, there were no statistically significant differences in age, the time of diagnosing breast carcinoma and the occurrence of MPE, pleural fluid volume, pleural fluid pH value, and the share of patients with positive results on cytology. However, the share of patients with positive histology specimens was significantly higher in TMP group (P=0.000).

Recurrence of MPE, time of chest tube drainage and hospitalisation, number of complications, perioperative mortality and mortality within 6 months after the treatment in each group are given in Table 2.


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  		Table 2. Duration of chest tube drainage, duration of hospitalisation, frequency of pleural effusion recurrence, perioperative mortality and mortality after 6 months in both groups of patients

 
The success of TMP in the whole study population was 87%, and of TP 74%. The difference is not statistically significant. The average time of chest tube drainage was significantly shorter in TMP group (3.8 days) than in TP group (5.6 days) (P=0.000). The average time of hospitalisation was also statistically significantly shorter in TMP group (5.5 days) than in TP group (7.5 days) (P=0.001). All complications in TMP group were easily treated (3 cases of prolonged lung deflation, 1 case of significant bleeding, 1 case of subcutaneous emphysema, 2 cases of wound inflammation). In TP group, the most frequent complication was empyema and the inflammation of the wound around the chest tube (8 cases), two patients had subcutaneous emphysema, and one developed a bronchopleural fistula. There was no case of perioperative death (within 30 days after the intervention) in TMP group, while in TP group two patients died due to pulmonary embolism, one due to myocardial infarction, and one due to sepsis. There were 8 deaths within 6 months in TP group, and 6 in TMP group. The difference was not significant. From the additional four patients in the TP group who died within 6 months one died from pulmonary embolism and one from the progression of the malignant disease, for two patients we have no data. From the six patients who died within 6 months in the TMP group three patients died from the progression of the malignant disease and for three patients we have no data. From the nine patients who died in the hospital the cause of death was not MPE and for the five patients who died at home we do not know the precise cause of death.

We investigated the differences in the above-mentioned variables occurring in groups after the classification of patients according to pH values of MPE (Table 3). In TMP group, 24 patients had pH values above 7.3 and 21 patients below 7.3. In TP group, 22 patients had pH values above 7.3 and 20 patients below 7.3.


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  		Table 3. Duration of chest tube drainage, duration of hospitalisation, frequency of pleural effusion recurrence, perioperative mortality and mortality after 6 months in both groups of patients, divided by subgroups in relation to pleural effusion pH values (pH>7.3 and <7.3)

 
While TMP and TP were equally successful (92 and 91%) in patients with pH levels above 7.3, differences occurred in patients with pH below 7.3 (81 and 55%) (P=0.07). The lowest pH value of pleural fluid at which the methods were still successful was 7.06 in TMP group and 7.25 in TP group.

The average time of TMP was 35 min (25–70), and the average blood loss remained below 200 ml.

Multivariate analysis was used to analyse the impact of patients' age, the time between diagnosing breast carcinoma and the occurrence of pleural effusion, pleural fluid volume, effusion treatment option, and pleural fluid pH value upon treatment results (Table 4).


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  		Table 4. Results of multivariate analysis of the impact of patients' age, time span between diagnosis and the occurrence of pleural effusion (time), treatment options (group), pleural effusion volume (effusion), and pleural fluid pH value upon treatment results

 
Multivariate analysis results showed that the success of the treatment of MPE depended on the treatment option and pleural fluid pH value, while patients' age, time interval and volume of effusion had no impact (Table 4). The number of postoperative complications was influenced by the time from the onset of disease till the occurrence of effusion and the pleural fluid pH value. The time of chest tube drainage and hospitalisation was related to the time interval, treatment option and pH values. Patients' age and the volume of pleural fluid had no influence on treatment results (Table 4).


   4. Discussion
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
5. Conclusion
 References
 
Under normal circumstances, the influx of fluid into pleural space is in equilibrium with the efflux. In breast carcinoma, pleural fluid accumulation is most often caused by the obstruction of pleural lymphatic drainage [2] or direct tumour infiltration of pleural space [11]. According to various authors, 35–50% of recurrent MPE in patients with breast carcinoma can be treated by systemic therapy [11,12], while the rest require local palliative interventions to prevent fluid accumulation and thus improve the patients' quality of remaining life. The choice of palliative treatment depends on the patient's general condition, speed of pleural fluid accumulation, stage of primary disease, and the patient's survival expectancy.

Chemical pleurodesis with talc insufflated via a chest tube or under controlled conditions by thoracoscopy [6,13] is successful in treating recurrent MPE in 85–95% [14,15]. Our study yielded identical results: 91% success was achieved in the group of patients with MPE pH value above 7.3. When pH values are below 7.3, the success of TP decreases because the sclerosant does not induce a strong enough inflammatory reaction and fibroplasia on pleura changed by carcinoma or fibrosis [8]. Success in our patients with pleural pH below 7.3 was 55%.

TMP is normally used to treat recurrent pneumothorax. Some authors also use VATS to manage recurrent MPE, but they perform obliteration of pleural space by pleurectomy [16,17], which is a rather demanding surgical procedure for a carcinoma patient. In our study TMP gave excellent results in treating MPE in the group of patients with pH values above 7.3 (92%). Its success is comparable to chemical pleurodesis. In the group of patients with pleural fluid pH below 7.3, the success was 81%, which is better than in chemical pleurodesis (55%) (P=0.07). Better success of TMP is attributed to the lysis of eventual adhesions in the pleural space, occasional lung decortication and better lung expansion after the surgical procedure with artificial lung ventilation by overpressure. Patients with MPE in whom massive carcinomatosis of visceral pleura and trapped lung are diagnosed during thoracoscopic exploration remain a special problem. Such changes were discovered in three of our patients who were treated by TMP and whose pH values were below 7.3. Some authors perform pleuroperitoneal shunt in such cases [18] while others recommend the use of small-bore catheters [19]. In the past we used to perform repeated therapeutic thoracocentsis after the removal of chest tube drainage in cases of massive effusions. In the last year the patients with persistent massive effusions are also treated with small-bore catheters in our institution. The main advantage of this method is reduced patient discomfort. If trapped lung due to fibrotic changes of visceral pleura was discovered during thoracoscopic exploration, thoracoscopic decortication of affected lung, successful in the majority of cases, was performed.

In the group of patients treated with TMP, the average duration of chest tube drainage was 3.8 days and of hospitalisation 5.5 days, which is well comparable with results achieved by other authors [7,15], who report 3–4.5 days of chest tube drainage and 4–5.7 days of hospitalisation. In our study, chest tube drainage and hospitalisation were statistically significantly shorter in patients treated by TMP than in patients treated by TP. Because the essence of palliation in recurrent MPE is to alleviate patients' problems and achieve the shortest hospitalisation possible, TMP is fully satisfactory from this perspective too. Despite all the benefits of early chest tube removal, early extubation might be one of the reasons for recurrence of MPE. Since most of the recurrences of MPE in both groups of our patients occurred in the first week after the procedure, we believe that the main cause for recurrences was unsuccessful pleurodesis.

At the end it should be underlined that approximately 25% of MPEs remain unconfirmed by cytological analysis and blind needle biopsy of pleura, which often makes their correct and efficient management difficult. By using thoracoscopy as a diagnostic technique, the percentage of accurate diagnoses rose to 96% [19]. In our study, patients treated by VATS underwent targeted biopsy of suspected areas prior to pleurodesis itself; the presence of a malignant neoplasm was confirmed in 93%, which is statistically significantly a higher percentage (P=0.000) than in the other group (60%) that underwent blind needle biopsy.


   5. Conclusion
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
 5. Conclusion
References
 
Results of our study show that TMP is a better palliative method for treating MPE in breast carcinoma than TP when pleural fluid pH values are below 7.3. In the group of patients with pH values above 7.3 the TP method is a better choice since it is equally effective than the TMP method but easier to perform. However, even in this group of patients the TMP method may have some advantages whenever we suspect pleural adhesions and in cases of undiagnosed pleural effusions.


   References
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
 5. Conclusion
 References
 

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  3. Goldsmith H.S., Bailey H.D., Callahan E.L. Pumonary lymphangitic metastases from breast carcinoma. Arch Surg 1967;94:483-488.[Abstract/Free Full Text]
  4. Good J.T., Jr., Taryle D.A., Sahn S.A. The pathogenesis of low glucose, low pH malignant effusions. Am Rev Resp Dis 1985;131:7737-7741.
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  8. Sahn S.A., Good J.T., Jr. Pleural fluid pH in malignant effusions: diagnostic, prognostic and therapeutic implications. Ann Intern Med 1988;108:345-349.[Abstract/Free Full Text]
  9. Rodrigues-Pandero F., Lopez Mejias J. Survival time of patients with pleural metastatic carcinoma predicted by glucose and pH studies. Chest 1989;95:320-324.[Abstract/Free Full Text]
  10. Sanches-Armengol A., Rodrigues-Pandero F. Survival and talc pleurodesis in metastatic pleural carcinoma, revisited: report of 125 cases. Chest 1993;104:1482-1485.[Abstract/Free Full Text]
  11. Apffelstaedt J.P., Van Zyl J.A., Muller A.G.S. Breast cancer complicated by pleural effusion: patient characteristic and results of surgical management. J Surg Oncol 1995;58:173-175.[Medline]
  12. Fentiman I.S., Millis R.R., Sexton S., Hayward J.L. Pleural effusion in breast cancer: a review of 105 cases. Cancer 1981;47:2087-2092.[CrossRef][Medline]
  13. Schultze M., Boehle A.S., Kurdow R., Dohrmann P., Henne-Bruns D. Effective treatment of malignant pleural effusion by minimal invasive thoracic surgery: thoracoscopic talc pleurodesis and pleuroperitoneal shunts in 101 patients. Ann Thorac Surg 2001;71:1809-1812.[Abstract/Free Full Text]
  14. Bresticker M.A., Oba J., LoCicero J., Greene R. Optimal pleurodesis. A comparison study. Ann Thorac Surg 1993;55:364-367.[Abstract]
  15. Danby C.A., Adebonojo S.A., Moritz D.M. Video-assisted talc pleurodesis for malignant pleural effusions utilizing local anesthesia and IV sedation. Chest 1998;113:739-742.[Abstract/Free Full Text]
  16. Waller D.A., Morritt G.N., Forty J. Video-assisted thoracoscopic pleurectomy in the management of malignant pleural effusion. Chest 1995;107:1454-1456.[Abstract/Free Full Text]
  17. Harvey J.C., Erdman C.B., Beatie E.J. Early experience with videothoracoscopic hydrodissection pleurectomy in the treatment of malignant pleural effusion. J Surg Oncol 1995;59:243-245.[Medline]
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  19. Belani C.P., Pajeau T.S., Bennet C.L. Treating malignant pleural effusions cost consciously. Chest 1998;113:78-85.[CrossRef]



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