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Eur J Cardiothorac Surg 2004;26:776-781
© 2004 Elsevier Science NL

Reverse cardiac remodelling in patients with primary pulmonary hypertension after isolated lung transplantation

Marie-Theres Kasimirb, Gernot Seebachera, Peter Jakscha, Günther Winklera, Katharina Schmidc, Gabriel M. Martaa, Paul Simona, Walter Klepetkoa*

a Department of Cardiothoracic Surgery, General Hospital Vienna, Medical University of Vienna, Waehringer Guertel 18-20, 1090 Vienna, Austria
b Department of Cardiothoracic and Vascular Anaesthesia and Intensive Care, Medical University of Vienna, Vienna, Austria
c Department of Pathology, Medical University of Vienna, Vienna, Austria

Received 23 December 2003; received in revised form 19 May 2004; accepted 26 May 2004.

* Corresponding author
e-mail: walter.klepetko{at}meduniwien.ac.at


   Abstract
Top
 Abstract
1. Introduction
 2. Material and methods
 3. Results
 4. Discussion
 References
 
Objective: Pulmonary hypertension eventually leads to severe distortion of the cardiac geometry with consequent impact on cardiac function. The purpose of this study was to prove reverse cardiac remodelling after isolated bilateral lung transplantation (LuTX) in patients with advanced primary pulmonary hypertension (PPH) and severe alterations of cardiac morphology and function. Methods: In the period of 2000–2002 17 (10 female, seven male) patients with advanced PPH underwent isolated bilateral LuTX. Median age was 30 years (range 16–53). All patients were in NYHA III or IV, most of them with intractable ascites, established renal impairment, malnutrition and immobility, continuously deteriorating despite various forms of pharmacological treatment including i.v. and inhalative prostacyclin, diuretics, Ca-antagonists, bosentan and catecholamines. Echocardiography and Doppler echocardiography measurements were performed before and 3 months after transplantation. Left and right ventricular diameters and function were assessed and tricuspid valve regurgitation was determined. Results: Mortality after 3 months was 17.5% (cerebral bleeding, multi-organ failure and diffuse myocardial infarction in one patient each). Three months after LuTX the 14 surviving patients were in NYHA I or II. Echocardiography showed normal left ventricular function and markedly improved right ventricular function with normal size of the RV. The leftward shifted flattened interventricular septum had returned in its physiological position and the high-grade tricuspid insufficiency had disappeared in all patients. Conclusions: Advanced alterations of cardiac morphology and function normalize completely and pre-existing tricuspid insufficiency disappears in PPH patients after isolated bilateral LuTX. Quality of life is excellent. Therefore, LuTX is preferred and safe in patients with advanced PPH even with severe cardiac dysfunction.

Key Words: Primary pulmonary hypertension • Lung transplantation • Cardiac remodelling


   1. Introduction
Top
 Abstract
 1. Introduction
2. Material and methods
 3. Results
 4. Discussion
 References
 
Primary pulmonary hypertension (PPH) is a rare and rapidly progressive disorder with an estimated annual incidence of 1–2 per million of the population. The etiology of PPH is still unknown. It appears that PPH is a result of abnormal interaction of environmental and genetic factors, leading to sustained elevations of the pulmonary artery pressure (PAP). Female gender, appetite suppressants and HIV infection were identified to be definitely associated with PPH and connective tissue disease, portal hypertension, congenital cardiac shunts, pregnancy and amphetamines are very likely risk factors for developing PH [1–3]. The pathological lesions of the pulmonary arteries range from early medial hypertrophy to end-stage plexiform fibrosis. PPH is often diagnosed in its later stages due to the non-specific symptoms of this disorder.

Advanced PPH leads to significant alterations of the cardiac morphology including right ventricular dilatation and hypertrophy, tricuspid regurgitation and septum deviation, with consequent impact on cardiac function. The current therapies include medical treatment with calcium channel blockers, prostacyclin, (nitric oxide) and bosentan [1,4]. Both, isolated lung transplantation (LuTX) and combined heart–lung transplantation (HLuTX) have been performed for PPH reported with similar survival rates of these two procedures [5,6]. However, the severe RV dilatation, dysfunction and reduction of pump function together with the typical tricuspid valve regurgitation and the limited volume capacity of the left ventricle, continue to be a matter of concern when isolated LuTX is performed in these patients. Both, the perioperative capacity of the heart to immediately compensate the significantly altered hemodynamic situation after LuTX as well as the long-term effects of LuTX on RV-hypertrophy originating from the combined chronic pressure load and hypoxia are so far insufficiently described in literature.

The purpose of this study was therefore to describe the potential for reverse cardiac remodelling after isolated bilateral LuTX in patients with advanced PPH and severe alterations of the cardiac morphology.


   2. Material and methods
Top
 Abstract
 1. Introduction
 2. Material and methods
3. Results
 4. Discussion
 References
 
2.1. Patients
In the 3 year period, 2000–2002, 17 patients with end-stage PPH underwent isolated bilateral LuTX. Median age of the 10 female and seven male patients was 30 years with a range from 16 to 53 years. All patients were in NYHA class function III or IV. Demographics of patients are shown in Table 1. In most patient's intractable ascites, renal impairment and severe malnutrition and immobility were present. All patients deteriorated continuously despite various forms of pharmacological treatment including i.v. and inhalative prostacyclin, calcium channel blockers, the endothelin receptor antagonist bosentan, diuretics and catecholamines. Details of preoperative therapy are shown in Table 2.


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  		Table 1. Demographics

 

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  		Table 2. Preoperative pharmacological therapy

 
2.2. Assessment of cardiac dimensions and function
Transthoracic two-dimensional echocardiography (TTE), spectral Doppler and colour Doppler echocardiography measurements (HP Sonos 2500, 2.5 MHz) were performed before and 3 months after transplantation. Left and right ventricular dimension and function were assessed in the standard para-sternal long-axis and apical four-chamber view. RV diameters were assessed at the level of the tricuspid annulus, the base and the mid portion. RV free wall thickness was measured in the mid portion. In addition the length was measured and the RV area determined by planimetry. Severity of tricuspid regurgitation was graded semi-quantitatively by means of width and length of the regurgitation jet in the right atrium (grade 0–4) with colour flow Doppler. Peak systolic PAP was calculated from the tricuspid regurgitation velocity profile which was obtained with continuous wave Doppler in the four-chamber view [7].

Right ventricular ejection fraction was determined from right heart catheterization pre- and postoperatively.

2.3. Surgical procedure
Donor lungs were harvested en bloc as part of a multi-organ procurement. Organ preservation was accomplished by infusion and storage in a high molecular dextran solution (Perfadex®; Vitrolife, Gothenburg) and topical cooling. Double LuTX was performed in all cases by a standard technique through transverse thoracosternotomy (Clamshell incision) in 11 patients and by two separate anterolateral thoracotomies in the fourth or fifth intercostal space in six patients. All transplantations were done on extracorporeal membrane oxygenation (ECMO) support, in 13 patients with femoral cannulation and in four patients with central cannulation of the aorta [8]. Donor lungs were implanted using single running suture technique for the bronchial (4/0 polydiaxolon PDS; Ethicon Inc., Sommerville, NJ), pulmonary artery and left atrial anastomoses (5/0 PDS). No HLuTX was performed during the same period.

2.4. Postoperative management
ECMO was explanted in 16 patients within the first 24 h after LuTX, only one patient required ECMO for 3 days. Right heart failure was not the indication for ECMO. Our strategy is to leave the patient on ECMO support for the first 12 h after transplantation to decrease pulmonary flow and allow gradual adaptation of the heart to the new pathophysiological situation [8]. All patients received a triple drug immunosuppressive therapy including tacrolimus or cyclosporine, mycophenolat mofetil and methylprednisolone. Prophylaxis against pneumocystis carinii, cytomegalovirus and fungal infections was given.

2.5. Statistical analysis
Means and standard deviation were calculated when appropriate. Student's t-test was used for analysis of changes between preoperative and postoperative measurements. Statistical significance was assumed at P<0.05.


   3. Results
Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
4. Discussion
 References
 
Mortality was 17.5% after 3 months. Causes of death were cerebral bleeding, multi-organ failure and diffuse myocardial infarction in three patients, respectively. Three months after LuTX all 14 surviving patients had improved to NYHA functional class I or II. Preoperatively markedly elevated mean PAP of 61.5±16.5 mmHg (range, 42–87) normalized after LuTX (17.4±3.7 mmHg; range, 9–23; P<0.005) (Fig. 1) . Preoperative cardiac index was severely reduced with a mean value of 2.2±0.8 l/min per m2 (range, 1.1–3.7). During the postoperative period no patient developed right heart failure.



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  		Fig. 1. Mean pulmonary artery pressure (PAP) before and 3 months after lung transplantation (P<0.005).

 
Three months after LuTX the cardiac index increased significantly when compared to preoperative observation, resulting in a mean value of 4.1±1.28 l/min per m2 (3.1–7.5) (P<0.005) (Fig. 1).

Echocardiography showed normal left ventricular function before and after LuTX (preoperative, EF 69.9±8.5%; postoperative, 73.8±4.1%; P=0.023). Preoperatively all patients showed high grade right ventricular dilatation and hypertrophy and moderate to highly impaired right ventricular function (RVEF 32.7±16.7%). After LuTX right ventricular dimensions (Table 3) and function returned to normal (RVEF 67.3±4.7%, P<0.005) (Fig. 2) . Only a moderate degree of right ventricular hypertrophy was detectable. Colour Doppler echocardiography revealed severe tricuspid regurgitation before transplantation, which decreased significantly after LuTX (preoperative, 2.9±1.0; postoperative, 0.46±0.41; P<0.005). The septum had returned in its physiological position in all patients (Figs. 3 and 4) .


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  		Table 3. Right ventricular dimensions

 


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  		Fig. 2. Right ventricular ejection fraction (%) before and 3 months after lung transplantation (P<0.005).

 


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  		Fig. 3. Parasternal long-axis echocardiography. (a) Preoperative, dilatation and hypertrophy of the RV; (b) Postoperative (3 months follow-up), normalized RV-dimensions. LA, left atrium; LV, left ventricle; RV, right ventricle; PF, pericardium fluid.

 


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  		Fig. 4. Apical four-chamber echocardiography. (a) Preoperative, dilatation of the RV and RA, septum deviation to the left; (b) Postoperative (3 months follow-up), normalized RV and LV. LA, left atrium; LV, left ventricle; RA, right atrium; RV, right ventricle; PF, pericardium fluid.

 

   4. Discussion
Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
 4. Discussion
References
 
Conventional pharmacological treatment with vasodilators and anticoagulants improves hemodynamic and life expectancy in only few patients with PPH in NYHA class III or IV [1,9]. Treatment with epoprostenol, beraprost and bosentan has been shown to be more effective than conventional therapy and leads in most of the patients with PPH to improved exercise capacity, hemodynamics and survival depending on the severity of the disease at baseline [4,10,11]. However, some patients do not respond to therapy or start to deteriorate again after initial period of improvement. For those patients lung or combined HLuTX has been established as an effective therapy [6,12–15].

PPH and pulmonary hypertension associated with congenital heart disease are the main indications for HLuTX in the adult population. The availability of organs for combined heart and LuTX is limited and doubles the waiting time for transplantation when compared to isolated LuTX. Isolated LuTX certainly is the more organ sparing method of transplantation, but arises the question if the same functional outcome is reachable when compared to HLuTX. Advanced PPH affects cardiac morphology severely, leading to right ventricular dilatation and hypertrophy, tricuspid insufficiency and septum deviation with subsequent deterioration of right and left ventricular function. Therefore, it remains an ongoing point of discussion, whether these marked alterations can be reversed with isolated LuTX.

Besides conventional invasive evaluation of patients with severe pulmonary hypertension, echocardiography is the best method for monitoring cardiac morphology, function and PAP. All methods to assess the right ventricle are limited by the lack of an appropriate geometrical model. Therefore, quantitative data is difficult to obtain and semi-quantitative estimations were collected.

In this study, all patients showed the typical cardiac alterations resulting from advanced pulmonary hypertension on echocardiography. Pulmonary artery systolic pressure was greater than 60 mmHg associated with substantial leftward ventricular septum shift, enlarged right atrium and ventricle and reduced right ventricular function. In addition tricuspid regurgitation grade 3–4 was present in all patients. Both, right atrial size and severity of tricuspid regurgitation have been described as risk factors for perioperative death after LuTX [16].

Three months after transplantation PAP had normalized in all patients, which resulted in an almost complete reverse remodelling of the distorted cardiac geometry regardless of the preexisting right atrial enlargement and tricuspid insufficiency. The functional performance of the heart had completely normalized and preexisting tricuspid insufficiency had disappeared. Of note, right heart failure did not complicate the postoperative period in any of the patients. These findings are well in line with previously published work where improvements in hemodynamics after single or bilateral LuTX for pulmonary hypertension with a rapid and sustained drop in PAPs and substantial improvement of right ventricular function were reported [17–23]. However, in contrast to the previous works our paper describes a current series of patients receiving the full pharmacological treatment possibilities which became available only in recent years [4,10,11]. It therefore can be anticipated that these patients were in a much more debilitated status than patients referred for LuTX several years ago. Despite full therapy our patients deteriorated to severe impaired functional status including intractable ascites and renal impairment with preoperative creatinine of 1.24±0.59 shown in Table 1.

The advanced status of disease at the time of LuTX in our patients as well as the significantly established co-morbidity resulted in a complex perioperative treatment period. This can be demonstrated with the clearly prolonged ICU-stay of 35.18±46.33 days. However, despite these complex problems the 3-months survival rate of the patients together with the functional outcome was excellent and in the range that is seen in patients undergoing LuTX for other indications. Our results suggest that combined HLuTX would not be an advantage over isolated LuTX in patients with advanced PPH. Also, single LuTX is no alternative to isolated bilateral LuTX. In the acute phase it may result in a perfusion mismatch and may lead to acute overflow of the transplanted lung with severe reperfusion edema because of the preferred blood flow to the allograft [24]. In the chronic phase if bronchiolitis obliterans syndrome (BOS) develops, severe ventilation–perfusion mismatch may ensue.

4.1. Limitations of the study
Intra- and perioperative assessment by transesophageal echo (TEE) is not comparable to transthoracic echo (TTE) used for follow-up. The TTE performed 1 week after transplantation and at discharge is unreliable due to poor image quality in the early postoperative phase and therefore data is supported by a single measurement in time and development of reverse cardiac remodelling cannot be described over time.

In conclusion we are able to demonstrate that even in these patients with most advanced pulmonary hypertension and severe cardiac alterations LuTX results in complete reverse remodelling of the cardiac morphology and function and that isolated LuTX can be performed with excellent early outcome. Patients show rapid improvement not only in respiratory and cardiac function, but recover quickly with significantly improved functional status and satisfactory quality of life. These results suggest that isolated LuTX should be the preferred method of transplantation for patients with end-stage PPH refractory to medical treatment without any limit in terms of cardiac dysfunction.


   Footnotes
 
Presented at the joint 17th Annual Meeting of the European Association for Cardio-thoracic Surgery and the 11th Annual Meeting of the European Society of Thoracic Surgeons, Vienna, Austria, October 12–15, 2003.


   References
Top
 Abstract
 1. Introduction
 2. Material and methods
 3. Results
 4. Discussion
 References
 

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