Unilateral pleural effusions associated with stenoses of left brachiocephalic veins in haemodialysis patients

Enrique Morales Ruiz, Eduardo Gutierrez, Alfonso Martínez, Eduardo Hernández, Jose María Alcazar, Juan Carlos Herrero and Manuel Praga

Department of Nephrology, Hospital Universitario 12 de Octubre, Madrid, Spain

Correspondence and offprint requests to: Enrique Morales Ruiz, Carretera de Andalucía Km 5.400, Servicio de Nefrología, Hospital 12 de Octubre, Madrid 28041, Spain. Email: emoralesr{at}senefro.org

Keywords: arteriovenous fistula; brachiocephalic vein; haemodialysis patients; pleural effusion; stenosis



   Introduction
 Top
 Introduction
 Cases
 Discussion
 References
 
Pleural effusion is a frequent complication in patients undergoing haemodialysis. Its more common causes are congestive heart failure, infection, neoplasm and so-called uraemic pleurisy [1,2]. When the work-up of a pleural effusion in a haemodialysis patient does not identify a specific cause, it is usually attributed to uraemic pleurisy [3]. Uraemic pleural effusions have been estimated to develop in 3–10% of patients with advanced renal failure [4]; however, the diagnosis of uraemic pleurisy remains elusive, as no pathognomonic test is available.

We report here on two haemodialysis patients with a novel cause of pleural effusion. In each case, the sum of a severe stenosis in the left brachiocephalic vein and the increased venous flow of an ipsilateral arteriovenous (AV) fistula coincided with the appearance of a massive left sided pleural effusion. Percutaneous venous angioplasty in one patient and ligation of the AV fistula in the other led to dramatic resolutions of the pleural effusions.



   Cases
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 Introduction
 Cases
 Discussion
 References
 
Patient 1
A 53-year-old woman with end-stage kidney disease (due to autosomal dominant polycystic kidney disease) was hospitalized after 2 weeks of dyspnoea, left-sided chest pain and low grade fever. She had begun haemodialysis 13 years earlier. One year later she had received a successful cadaver kidney graft; however, due to chronic graft rejection, 7 years later she had to resume haemodialysis, which was performed through an AV fistula between the left brachial artery and an upper arm vein. Several central venous catheters had been placed in both her right and left jugular and subclavian veins for haemodialysis following past thromboses of her fistula. Two years before admission, poor flow had been detected in the left AV fistula. A venogram had shown a critical stenosis of the brachiocephalic vein. Because percutaneous angioplasty and stent placement at the site of stenosis did not improve blood flow appreciably, a new AV fistula had been created, and during the following 2 years haemodialysis had been performed without problems, via this right arm AV fistula.

The most important physical signs of our patient on admission were decreased breath sounds and dullness in the left hemithorax, along with significant oedema of the left arm. Her left and right arm AV fistulae both had adequate thrills and murmurs on auscultation. Her blood pressure was 136/84 mmHg and temperature 37.3°C. Signs of congestive heart failure were absent. She weighed 60.3 kg (dry weight 60 kg). Her blood count and routine serum biochemistry did not show significant changes. A chest radiograph revealed a massive left sided pleural effusion. Thoracentesis removed 800 ml of straw-coloured fluid—with a pH of 7.4, 1.150 red blood cells/µl and 1.250 leukocytes/µl (45% neutrophils, 35% monocytes, 20% eosinophils). The fluid contained a total protein of 3.8 g/dl (38 g/l), and the ratio of pleural fluid protein to serum protein was 0.5 (serum protein, 7.6 g/dl). In the pleural fluid, lactate dehydrogenase (LDH) was 130 UI/l and the ratio of the pleural fluid LDH to serum LDH was 0.57. The pleural fluid glucose was 88 mg/dl (4.8 mmol/l) and amylase 25 UI/l. Cytological studies of the fluid, antinuclear antibodies, smear for acid-fast bacilli and routine cultures were negative. Echocardiography did not show signs of heart failure or pericardical effusion.

Given the negative results of cytological and microbiological studies, uraemic pleurisy was considered the most likely diagnosis. Her haemodialysis regimen was intensified by increasing the hours of haemodialysis per week; however, the pleural effusion did not decrease. Other studies, such as thoracic computed tomography, perfusion lung photoscans and echocardiography, did not contribute significant data. A pleural biopsy showed no granulomas, and cultures for acid-fast bacilli and fungi were negative. In the following month, another thoracentesis performed because of dyspnoea yielded pleural fluid similar to that initially studied. Left arm oedema increased during this period, leading to the performance of left upper extremity venography which revealed a critical stenosis of the stent placed in the left brachiocephalic vein. The percutaneous angioplasty of the stenotic stent was successful. In the following days, the patient's dyspnoea progressively improved together with the subsidence of the arm oedema and a complete disappearance of pleural effusion. After >2 years of follow-up, no recurrence of pleural effusion has been observed.

Patient 2
A 76-year-old man with end-stage renal disease (due to hypertensive nephrosclerosis) was hospitalized because of oedema of his left arm and left hemithoracic pleural effusion. He had a history of uncontrolled hypertension and atrial fibrillation, and had started chronic haemodialysis 2 years before admission. A brachiocephalic AV fistula had been created in the left arm 3 months before the onset of haemodialysis. Due to the poor development of the fistula, however, during the first month of chronic haemodialysis, vascular access was obtained through a catheter placed in his left jugular vein. By the second month on haemodialysis, the fistula had developed adequately and was available for puncture. The patient then had no complications until 3 months before his admission, when poor flow was detected in the AV fistula. A percutaneous catheter was placed in the left subclavian vein, pending the creation of another AV fistula, this in the right arm. In the following weeks, progressive oedema of the left arm developed. An echo-Doppler examination showed the complete thrombosis of the left internal jugular vein, extending to the left subclavian and brachiocephalic veins. Left upper extremity venography demonstrated severe stenosis of his subclavian and brachiocephalic veins. A chest radiogram showed a massive left pleural effusion, and the patient was admitted for work-up.

His blood pressure was 135/64 mmHg, temperature 36.7°C, and weight 69 kg (dry weight 68.5 kg). Dullness in the left hemithorax together with oedema of the left arm were the most important physical findings. Signs of congestive heart failure were absent. Laboratory tests did not show significant abnormalities. A thoracentesis removed 500 ml of straw-coloured fluid with a pH of 7.41, 1.400 red blood cells/µl, 1.190 leukocytes/µl (40% neutrophils, 60% monocytes), a total protein of 3.7 g/dl (37 g/l) and a ratio of pleural fluid protein to serum protein of 0.44 (serum total proteins 8.4 g/dl). The fluid's LDH was 222 UI/l and the ratio of pleural fluid LDH to serum LDH was 0.6; its glucose was 120 mg/dl (6.66 mmol/l) and amylase 155 UI/l. Cytological studies, smear for acid-fast bacilli and routine cultures were negative. Echocardiography ruled out pericardial diseases or congestive heart failure.

Five days after admission, the left AV fistula was ligated surgically and the left subclavian catheter removed. A catheter was placed in the right femoral vein to continue haemodialysis. In the following days, the left pleural effusion and arm oedema improved rapidly. A tunnelled cuffed catheter was placed in the right subclavian vein, and the patient was discharged. During the following months, the complete resolution of his left pleural effusion was observed in follow-up chest radiograms.



   Discussion
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 Introduction
 Cases
 Discussion
 References
 
The most common causes of pleural effusion in dialysis patients are congestive heart failure, infections and tumours [1,2]. There are, however, a number of haemodialysis patients in whom identifyfing the aetiology of pleural effusion remains elusive in spite of systematic and repeated testing. In these cases, usually a tentative diagnosis of uraemic pleurisy is made [4]. Some autopsy studies suggest that uraemic pleurisy is a common complication in patients on chronic haemodialysis [5]. However, information about its clinical characteristics, long-term outcome and treatment is scarce [3,4,6,7]. Thoracentesis often reveals variably bloody fluid, although the fluid can be just serous in some patients. In the majority of reported cases, pleural fluid was consistent with an exudate. The pathogenesis of uraemic pleurisy remains unknown, but its similarities and frequent temporal coincidence with uraemic pericarditis would suggest a condition of uraemic polyserositis. In some patients, the pleural effusion resolves after a few weeks of intensive dialysis; other patients, however, show massive and persistent pleural effusions without any response to increases in the dialysis dose.

In 1994, a report was published on a patient on haemodialysis who had massive left pleural effusion and ipsilateral breast and arm oedema [8]. The surgical closure after a successful kidney transplantation of her proximally placed left sided AV fistula led to the complete resolution of the pleural effusion. Later, a duplex scan of her left upper extremity was consistent with a partial obstruction of the left brachiocephalic vein. The authors suggested that the stenosis of the left brachiocephalic vein and ipsilateral pleural effusion were directly connected. The combination of a brachiocephalic stenosis and the high venous flow rates provided by an ipsilaterally situated AV fistula would locally elevate the venous pressure, which would impede the drainage of the left superior intercostal vein into the left subclavian and brachiocephalic veins. In 2001, another similar case was reported [6]: a woman on haemodialysis developed a massive left pleural effusion. She had a iatrogenic AV fistula in her left forearm. A venogram of the arm demonstrated the critical stenosis of the brachiocephalic vein, and the successful elimination of the stenosis by percutaneous angioplasty was followed by the complete disappearance of her pleural effusion.

Our two cases provide further support for the existence of a relationship between an abnormally high venous pressure in the left brachiocephalic vein and ipsilateral pleural effusion. The pleural fluids were consistent with a transudate in both cases; however, no signs of overhydration, congestive heart failure or obstruction of the superior vena cava were found during their work-ups. Infections or tumours were also ruled out. As in the patients previously reported [8,9], severe stenoses of the left brachiocephalic veins were documented. In our first patient, the cause of the obstruction was the restenosis of a venous stent—previously placed in the left subclavian vein to improve the venous flow of a poorly functioning ipsilateral AV fistula. This and the second patient both had had catheterizations of their jugular and subclavian veins. In both of our patients, again as in the two patients previously reported, an ipsilateral AV fistula was present. In our first patient, percutaneous venous angioplasty led to the complete and rapid resolution of pleural effusion. In the second patient, a similar resolution was observed after the ligation of the AV fistula and removal of the subclavian catheter.

Our patients, and the two others previously described, had massive left pleural effusions. This left-sided preponderance might be based on the anatomical peculiarities of the thoracic venous drainage. The left superior intercostal vein drains a considerable number of the bronchial and intercostal veins in the left hemithorax [8]. It, in turn, drains into the left subclavian and brachiocephalic veins. In contrast, bronchial and intercostal veins in the right hemithorax drain into the right brachiocephalic vein (right superior intercostal vein) and superior vena cava (azygos vein). To our knowledge, there have been no reports of similar effusions in the right hemithorax. However, anatomical variations of thoracic venous drainage are frequent; and, therefore, theoretically, it is quite possible to come across similar cases involving the right side.

In recent years, catheterization for temporary or permanent access for haemodialysis has increased dramatically [10]. A well known, and increasingly diagnosed, complication of such catheterizations is subclavian vein stenosis [11]. For these reasons, an increase in the incidence of pleural effusions associated with high brachiocephalic venous pressure might be anticipated in haemodialysis patients.

It should be further kept in mind that, although the stenosis of the subclavian vein is a complication of the catheterization of either the jugular or subclavian vein, it occurs significantly more frequently after subclavian catheterization. In our patients, central catheters were placed in both the left jugular and subclavian veins.

In summary, as far as we know, only four cases, including our two, of pleural effusion associated with high brachiocephalic venous pressure have been published so far. It is possible that other routes of venous drainage were also occluded in our patients or in the two others previously reported. Haemodialysis patients that develop otherwise unexplained pleural effusions ipsilateral to a functioning AV fistula should be investigated for stenosis in the brachiocephalic vein, particularly those patients who have had previous catheterizations of the jugular or subclavian veins on the same side as the effusion. The presence of ipsilateral arm oedema should reinforce the clinical suspicion. Relieving the stenosis by venous angioplasty or the ligation of the ipsilateral fistula, or both, can dramatically resolve the pleural effusion.

Conflict of interest statement. None declared.



   References
 Top
 Introduction
 Cases
 Discussion
 References
 

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Received for publication: 22.10.04
Accepted in revised form: 3. 2.05





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