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Interact CardioVasc Thorac Surg 2009;9:391-394. doi:10.1510/icvts.2009.203356 © 2009 European Association of Cardio-Thoracic Surgery
Pleural electrophysiology variations according to location in pleural cavity
a Department of Physiology, Medical School, University of Thessaly, New buildings, Mezourlo 41 110, PO Box 1400, Larissa, Greece Received 23 January 2009; received in revised form 29 April 2009; accepted 4 May 2009
*Corresponding author. Tel.: +30 2410 55 65 56; fax: +30 2410 67 02 40.
The aim of the study was to compare the electrophysiology profile of sheep pleura originated from different locations of the pleural cavity with the respective profile in humans. Sheep specimens obtained from upper and lower lung lobes, 1st–4th and 8th–12th rib, ventral-dorsal diaphragm and mediastinum were mounted between Ussing chambers. Human visceral tissues were obtained from patients subjected to lobectomy. Trans-mesothelial resistance (RTM) was determined as an indicator of the tissue permeability, while amiloride and ouabain were used as inhibitors of cellular transportation via ion transporters. Control values RTM were low in lower lobe visceral, caudal costal parietal and diaphragmatic pleura. Amiloride increased RTM at all locations except upper visceral and mediastinum. Higher RTM increases were found in caudal parietal and dorsal diaphragmatic samples. Ouabain increased RTM of lower visceral, caudal parietal and diaphragmatic pleura but not of mediastinal specimens. Observations made in sheep tissue were comparable with human visceral, parietal and mediastinal regions. In conclusion, results suggest heterogeneity of trans-mesothelial permeability among different pleural locations in sheep as was the case for humans. Thoracic surgeons should consider physiology function of each part of pleural cavity before pleural tissue manipulation. Observations made in sheep may be used to understand human physiology.
Key Words: Human; Pleura; Sheep; Electrophysiology; Permeability; Ussing
Pleural membrane is often wasted during thoracic surgery; the parietal pleura of the upper thoracic cage is stripped off during total pleurectomy for pneumothorax surgery [1] while an important surface of upper lung lobes visceral pleura is discarded during wedge resection for bullae removal [2]. Thickened parietal pleura is stripped off to optimize thoracic cage movement after decortication for thoracic empyema [3]. Mediastinal pleura is transected during oncology thoracic surgery for mediastinal lymph node picking. From a physiology aspect, pleural mesothelium is important for pleural fluid recycling [4–6]. Parietal pleura located over the caudal parts of the human pleural cavity showed higher permeability and greater cellular transportation ability when compared with the cranial or the mediastinal pleura [7]. However, the exact permeability profile of all pleural parts has not yet been totally clarified since visceral pleura is extremely difficult to be stripped off without air leakage, whereas stripping off the diaphragmatic pleura may result in significant bleeding. In order to circumvent this problem, sheep pleural tissue may be used as it is considered relative to human [4]. The aim of the study is to identify the electrophysiology profile of sheep pleura originated from visceral, costal parietal, diaphragmatic and mediastinal regions and to compare it with the respective human pleural regions electrophysiology profile.
Intact sheets of sheep pleura were obtained from ten adult sheep, immediately after death, from a local slaughterhouse. Specimens from different anatomical locations were obtained; visceral pleura from upper and lower lobes, parietal pleura over 8th–12th rib (caudal) and over 1st–4th rib (cranial), diaphragmatic pleura from ventral (sternum-costal part) and dorsal regions (vertebral-costal part) and mediastinal pleura near the hilum. Human visceral tissues were obtained from patients who underwent lobectomy for lung cancer. All other comparisons with human tissue were made with results from our previous studies [7]. Permission for conducting the study was obtained from the Local Animals Committee (University of Thessaly, Greece) for experimenting on animals and from the Local Veterinary Committee. The tissues were thoroughly examined for holes, adherent lung or fat tissue and residual blood clots. Each piece was sent for histopathology examination after the end of the experiments and only the healthy tissues were included in the study. Tissues were transported to the laboratory in Krebs–Ringer Bicarbonate (KRB) solution chilled to 4 °C [7].
The tissues were mounted as planar sheets between Ussing-type chambers [6, 7]. Trans-mesothelial resistance (RTM, Na+-channel amiloride (Sigma Chemical Co, USA, 10–5 M, n=12 experiments for each sheep region, 8 for human visceral) and Na+-K+ pump inhibitor ouabain (Sigma Chemical Co, USA, 10–3 M, n=12 experiments for each sheep region, 8 for human visceral) solutions were added towards the mesothelial surface (that faces the pleural space in vivo) in order to clarify cellular transportation alterations [7]. Statistical analysis was performed using the SPSS, version 10.0 for Windows. Data are expressed as mean RTM±S.E. of mean or as the net increase of RTM above control level at the 1st min. Statistical significance between pairs was determined by paired t-test and among groups by ANOVA (Bonferroni Post-hocs). P-values <0.05 were accepted as significant.
Control RTM was low for all regions (Fig. 1). Lower RTM values were determined for caudal parietal (18.81± 0.6  ·cm2) and dorsal diaphragmatic regions (18.75±0.7 ·cm2) which were statistically different (P<0.05) from the regions where higher RTM values were observed; visceral upper (20.27±0.5 ·cm2), cranial parietal (20.20±0.5 ·cm2) and mediastinal regions (20.00±0.9 ·cm2). Control RTM for human upper visceral was 20.71±0.8 ·cm2 whereas for lower visceral was 19.49±0.7 ·cm2 values which were similar to the respective sheep visceral parts.
Within the 1st min from amiloride addition (Fig. 2), the net increase of RTM of lower lobe visceral (1.35±0.3 ·cm2), caudal parietal (1.99±0.4 ·cm2), ventral diaphragmatic (1.15±0.3 ·cm2) and dorsal diaphragmatic pleura (2.09±0.3 ·cm2) was higher from baseline (P<0.05). For visceral pleura, the net increase of RTM was statistically different (P=0.024) when the lower when compared with the upper regions (0.60±0.3 ·cm2). For parietal pleura, caudal regions responded greater (P=0.028) than the cranial regions (0.70±0.4 ·cm2). The net RTM increase was significantly different (P=0.048) between parietal and visceral pleural lower regions. The net RTM increase of dorsal diaphragmatic pleura was statistically significant (P=0.048) when compared to the net RTM increase of ventral diaphragmatic pleura, to upper visceral (P<0.02) and cranial parietal pleura (P=0.028), lower visceral pleura (P<0.02) and mediastinal pleura (P<0.02). Response of caudally located parietal pleura was similar to ventral diaphragmatic pleura (P>0.05). Non-significant changes were observed for the mediastinal pleura (0.3±0.2 ·cm2) when compared to baseline. Addition of amiloride in human visceral pleura increased RTM by 0.64±0.8 ·cm2 for upper visceral and by 1.12±0.8 ·cm2 for lower visceral parts (P=0.041 but P>0.05 vs. parietal parts and vs. sheep respective parts, Fig. 3a).
Within the 1st min from ouabain addition (Fig. 4), RTM of lower lobe visceral (1.35±0.3 ·cm2), caudal parietal (1.15±0.4 ·cm2) ventral diaphragmatic (1.34±0.2 ·cm2) and dorsal diaphragmatic pleura (1.58±0.6 ·cm2) was statistically higher from baseline (P<0.05). For visceral pleura, the net increase of RTM of lower regions responded greater (P=0.022) than the upper regions (0.59±0.4 ·cm2). For parietal pleura this increase had the tendency to reach statistical significant level (P=0.06) when compared to that of cranial regions (0.78±0.3 ·cm2). The net RTM increase between parietal caudal and visceral lower regions was not different (P>0.05). No difference (P>0.05) was also observed between ventral and dorsal diaphragmatic pleura. The net RTM increase of dorsal diaphragmatic pleura was statistically different when compared to the net RTM increase of upper visceral (P<0.02), cranial parietal pleura (P=0.035) and mediastinal pleura (P<0.02). Response of lower visceral and caudal parietal pleura was similar to the response of the ventral and dorsal diaphragmatic pleura (P>0.05). Non-significant changes were observed for the mediastinal pleura (0.2±0.3 ·cm2) when compared to baseline. Addition of ouabain in human visceral pleura increased RTM by 0.68±0.6 ·cm2 for upper visceral and by 1.02±0.8 ·cm2 for lower visceral parts (P=0.06 but P>0.05 vs. parietal parts and vs. sheep respective parts, Fig. 3b).
The main finding of this study was that the caudal and diaphragmatic pleural regions demonstrated more intense electrical changes after each drug addition, indicating that the interference of the pleural membrane to pleural fluid recycling is more intense over these regions. Sheep visceral, parietal and mediastinal pleural electrophysiology was similar to human suggesting that observations for different regions made in sheep may be used to understand the respective human. The lower visceral and diaphragmatic pleural parts of the pleural cavity are also important for water and electrolyte transportation apart from the caudal parietal and should therefore be manipulated with cushion by surgeons. Control RTM measurements showed that caudal parietal, lower visceral and dorsal diaphragmatic sheep pleura had lower RTM after equilibration and stimulation only by current, in the absence of ion transporter blockers, and thus these regions were more ‘leaky’ than the other parts of the pleural cavity and thus more permeable to electrolytes and water [6–10]. Control RTM values for visceral, parietal and mediastinal pleura were similar with the human values [7].
Lower pleural regions (dorsal diaphragmatic, costal parietal) responded greater than the upper (cranial costal parietal, upper visceral) after amiloride addition. Lower and dorsal pleural regions might possibly have more amiloride-sensitive transporters promoting water/Na+ transportation out from the pleural cavity [6]. Similarly, lower pleural regions (dorsal, ventral diaphragmatic, costal parietal, lower visceral) responded greater than the upper after ouabain addition. Lower pleural regions possibly have more transporters blocked by ouabain (Na+-K+ pumps) which are homogenously dispersed in the lower parts of the pleural cavity, regulating K+ recycling or rebalancing water/Na+ movement via the amiloride-Na+ channels [6]. Therefore, it can be hypothesized that cellular transportation mainly occurs over the lower pleural (visceral and parietal) and diaphragmatic regions of the pleural cavity. Mediastinal pleura again [7] showed insignificant electrical changes. Lower visceral human pleura responded greater than the upper parts after amiloride addition but had the tendency to reach statistically significant level after ouabain addition. No differences were found when visceral and parietal pleura were compared. The net RTM increase of human visceral, parietal [7] and mediastinal pleura [7] when compared with the respective sheep net RTM increase was found to be similar for both ion inhibitors used except for the caudal costal parietal pleura after amiloride addition where the sheep RTM increase (1.99±0.4 The findings of the present study agree with other physiology observations constituting the lower pleural cavity as the area of greater lymphatic absorption of pleural fluid, [11, 12] radio-labeled accumulation of particles [13], pleural pressure, pleural liquid thickness and lymphatic stomata abundance [4]. Anatomically, sheep pleura is considered to be homologous to human as they both are mammals with thick visceral pleura [4]. Furthermore, sheep cranial and caudal parietal pleura as well as mediastinal pleura control electrophysiology profile and response after drug addition in this study were similar with that of the human pleura [7]. Therefore, from an electrophysiology aspect, sheep parietal pleura present similar characteristics with the human parietal pleura in vitro. Similar observations were also shown for upper and lower visceral sheep and human pleura. In this way, information about human pleura which are difficult to be stripped off during surgery may be obtained by observations made in sheep pleura. Sheep pleural tissue may consist of an adequate experimental model for in vitro electrophysiology, at least in studies. However, there exist differences that need to be addressed; sheep walk on four legs whereas humans on two and events in the pleural cavity in vivo include many factors which affect the pleural fluid recycling as the diaphragm movement, lymphatic drainage, respiration and others. Pleura is manipulated during thoracic surgery. Results from our studies support the resection of the parietal pleura of the apex during total apical pleurectomy during pneumothorax surgery [1, 7]. Similarly, visceral pleura of the upper lobes may also be resected in pneumothorax surgery since it showed in the present study limited permeability and cellular transporting ability [2]. In empyema thoracis, however, visceral pleura remains thin under the fibrous peel which covers the pleural cavity and should be left intact in order to avoid air leaks since, from a physiology aspect, it does not present important permeability function [3, 14]. Surgery involving the lower lung lobes should spare as much visceral pleura as possible, since it plays an important role in fluid recycling, as shown from the present study. Mediastinal pleura can be safely opened and resected during e.g. cancer surgery in order to perform lymph node picking or resect mediastinal tumors [7]. Pleural flaps for any use during surgery if needed should be obtained from upper parts of the pleural cavity [7]. Stripping off the parietal pleura over the lower pleural regions may affect fluid recycling postoperatively i.e. during empyema surgery where no apparent benefit was shown after decortication [3, 15]. Finally, this study enhances the idea of avoiding unnecessary manipulations of the diaphragmatic pleura, i.e. during empyema surgery or other surgery involving the diaphragm, as from this study is concluded that it presents the greatest permeability and cellular transportation ability. In conclusion, our results provide evidence of more intense electrochemical changes over the lower visceral and parietal pleural regions in sheep which were similar to the respective regions in humans, while the role of the diaphragmatic pleura, although important in sheep, needs further investigation in humans.
The authors thank Mr C. Foroulis for his thoracic surgery editing of the manuscript and all cardiothoracic surgeons of the Cardiothoracic Surgery Department, Larissa University Hospital, Greece for kindly providing the human visceral pleural specimens.
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Abstract
1. Introduction
