• Cystic fibrosis;
  • liver transplantation;
  • lung transplantation


  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and Methods
  5. Discussion
  6. Acknowledgments
  7. References

Sequential bilateral single lung-liver transplantation (SBSL-LTx) is a therapeutic option for patients with end stage lung and liver disease (ESLLD) due to cystic fibrosis (CF). A few cases have been reported, all of them were performed with the use of cardio-pulmonary by-pass (CPB). We performed SBSL-LTx in three young men affected by CF. All the recipients had respiratory failure and portal hypertension with hypersplenism. Along with lung transplants, two patients received a whole liver graft and one an extended right graft from an in situ split liver. During transplantation neither CPB nor veno-venous by-pass (VVB) were employed. Immunosuppression was based on basiliximab, tacrolimus, steroids and azathioprine. The three recipients are alive with a median follow-up of 670 days (range 244–1533). Combined SBSL-LTx is a complex but effective procedure for the treatment of ESLLD due to CF, not necessarily requiring the use of CPB or VVB.


  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and Methods
  5. Discussion
  6. Acknowledgments
  7. References

Cystic fibrosis (CF) is a multi-systemic genetic disease of secretory epithelia caused by mutations in a single gene on the long arm of chromosome 7, encoding for a cyclic-adenosyl mono-phosphate dependent chloride channel, the CFTR (CF trans-membrane conductance regulator). Lack of CFTR or its functional deficiency affects the respiratory, hepato-biliary, gastrointestinal, male reproductive systems and the pancreas. Exocrine pancreatic insufficiency and chronic pulmonary infections with acute exacerbations, leading eventually to respiratory insufficiency, are the most frequent complications. Respiratory failure accounts for over 90% of the fatalities (1,2) and replacement of both lungs is a treatment option for patients with CF and end-stage lung disease. According to the International Society of Heart and Lung Transplantation (ISHLT), CF account for 30% of adult lung transplantation and about 60% of pediatric lung transplantation performed worldwide (3,4). In the past, ‘en bloc’ heart and lung transplantation and double lung transplantation were the techniques utilized for replacement of both the lungs. More recently, the sequential bilateral single lung transplantation (SBSLTx) has become the technique of choice (5).

Liver disease represents the third cause of death among the patients affected by CF. Liver transplantation (LTx) has rarely been performed in patients with CF-related liver disease and the best results were achieved when LTx was performed before severe worsening of the respiratory function (1). The combined transplantation of the lungs and liver is a very complex and rarely performed operation indicated in patients who would not be expected to survive transplantation of either organ alone. A very few cases have been reported and cardio-pulmonary by-pass (CPB) was employed in all of them (6–9). In this paper we report our experience with three cases of combined SBSLTx and LTx for CF.

Patients and Methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and Methods
  5. Discussion
  6. Acknowledgments
  7. References

Between November 2002 and May 2006 we performed a SBSL-LTx in three young men affected by CF. The three operations were performed by the same surgical team, through separated bilateral anterolateral sternothoracotomy and abdominal incision. The lungs were transplanted first as a sequential bilateral procedure, followed by the liver. Recipients' and donors' characteristics are reported in Tables 1, 2 and 3.

Table 1.  Demographic data for the recipients of SBSL-LTx
PatientsAge (years)SexWeight (kg)Height (cm)UNOS statusDiagnosisFEV1% predictedPT INRBilirubin (mg/dL)PLT ×103/mmcWaiting time (days)
  1. CF = cystic fibrosis; FEV1 = forced expiratory volume in 1 s; PT = prothrombin time; INR = international normalized ratio.

222.7M541702BCF32%1.31.850 50
Table 2.  Recipients' preoperative hemodynamic parameters
 RA (mmHg)RV (mmHg)PAP (mmHg)PCWP (mmHg)CO (L/min)CI (L/min/m2)PVR (wood)
  1. RA = right atrium pressure; RV = right ventricle pressure; PAP = pulmonary artery pressure sistolic/diastolic/mean; PCWP = pulmonary capillary wedge pressure; CO = cardiac output; CI = cardiac index; PVR = pulmonary vascular resistance.

Case 175050/16/28225.153.51.7
Case 262828/10/1685.75 3.59 2.22
Case 3220/220/5/115105.80.6
Table 3.  Donors' characteristics for SBSL-LTx
 Age (years)SexWeight (kg)Height (cm)Liver GraftLung 1 Ischemia (min)Lung 2 Ischemia (min)Liver Ischemia (min)
236.8M90180Split I, IV–VIII120240420

Case 1

A 22.1-year-old man affected by end-stage lung and liver disease secondary to CF (Forced Expiratory Volume in 1 s FEV1 25%, ascites, esophageal varices and hypersplenism) with chronic infection of the respiratory tract (Staphylococcus aureus, Pseudomonas aeruginosa) after a waiting time of 607 days underwent SBSL-LTx with grafts procured from a 35.9-year-old deceased donor (weight 60 kg, height 165 cm). During the preoperative workup the patient had undergone assessment of the cardiac function with echocardiogram and right heart catheterization. Lungs and whole liver grafts were harvested in standard fashion. The patient was intubated with a left-sided double lumen endobronchial tube. A full hemodynamic monitoring was instituted by placing a Swan-Ganz catheter, a radial artery catheter and a Foley catheter (Table 4). Furthermore, intra-operatively cardiac function was monitored with trans-esophageal echocardiogram. The lungs were transplanted with a standard SBSLTx. LTx was performed through a ‘renal flap’ incision using a standard technique with bi-caval anastomosis. Biliary anastomosis was performed by a duct-to-duct reconstruction. The total ischemia time was 120 min for the first lung, 180 min for the second and 540 min for the liver. Neither CPB nor veno-venous by-pass (VVB) was used during the whole procedure that lasted 12 h in total. No heparin was given during the SBSLTx. Immunosuppression induction was achieved with basiliximab, tacrolimus and steroids. Perioperative antibiotic prophylaxis was based on piperacillin + tazobactam, ciprofloxacin and liposomal amphotericin B. Due to a positive culture from a bronchoalveolar lavage for Methicillin-resistant staphylococcus aureaus and Haemophilus influenzae, linezolid was introduced from day 6 until day 15.

Table 4.  Hemodynamics and respiratory monitoring during combined bilateral sequential lung and liver transplantation
PatientStart of operation1st Lung implantation2nd Lung implantationEnd of lung TxEnd of OLTx
  1. PAP = pulmonary artery pressure sistolic/diastolic; CVP = Central venous pressure; MAP = Mean arterial pressure; NA = noradrenaline.

Case 1pH7.33pH7.11pH7.33pH7.43pH7.11
PaO291 mmHgPaO2133 mmHgPaO247 mmHgPaO282 mmHgPaO2200 mmHg
PaCO290 mmHgPaCO2137 mmHgPaCO274 mmHgPaCO239.8 mmHgPaCO240 mmHg
PAP57/28 mmHgPAP38/21 mmHgPAP46/11 mmHgPAP20/10 mmHgPAP20/8 mmHg
CVP7 mmHgCVP7 mmHgCVP16 mmHgCVP11 mmHgCVP10 mmHg
MAP73 mmHgMAP63 mmHgMAP77 mmHgMAP77 mmHgMAP80 mmHg
Dopamine3 γ/kg/minDopamine10 γ/kg/minDopamine10 γ/kg/minDopamine5 γ/kg/minDopamine5 γ/kg/min
NANA0.05γ/kg/minNA0.05 γ/kg/minNA0.05 γ/kg/minNA0.02 γ/kg/min
Case 2pH7.34pH7.28pH7.32pH7.38pH7.39
PaO280 mmHgPaO275 mmHgPaO2105 mmHgPaO298 mmHgPaO2102 mmHg
PaCO250 mmHgPaCO255 mmHgPaCO240 mmHgPaCO237 mmHgPaCO238 mmHg
PAP35/18 mmHgPAP38/20 mmHgPAP35/15 mmHgPAP29/11 mmHgPAP31/14 mmHg
CVP8 mmHgCVP7 mmHgCVP6 mmHgCVP8 mmHgCVP8 mmHg
MAP70 mmHgMAP55 mmHgMAP58 mmHgMAP70 mmHgMAP65 mmHg
DopamineDopamine5 γ/kg/minDopamine7 γ/kg/minDopamine7γ/kg/minDopamine7γ/kg/min
Case 3pH7.42pH7.32pH7.33pH7.39pH7,41
PaO278 mmHgPaO250 mmHgPaO280 mmHgPaO2105 mmHgPaO2228 mmHg
PaCO240 mmHgPaCO270 mmHgPaCO245 mmHgPaCO241 mmHgPaCO242 mmHg
PAP35/15 mmHgPAP37/20 mmHgPAP35/22 mmHgPAP30/18 mmHgPAP31/15 mmHg
CVP12 mmHgCVP13 mmHgCVP14 mmHgCVP10 mmHgCVP4 mmHg
MAP75 mmHgMAP65 mmHgMAP65 mmHgMAP55 mmHgMAP70 mmHg
Dopamine3 γ/kg/minDopamine5 γ/kg/minDopamine5 γ/kg/minDopamine3 γ/kg/minDopamine10 γ/kg/min
NANANANA0.01 γ/kg/minNA0.01 γ/kg/min

On admission in Intensive Care Unit (ICU), he was on pressure-regulated volume control (PRVC) with a tidal volume (TD) of 400 mL (10 mL/kg), a positive end expiratory pressure (PEEP) of 4 cm H2O with a FiO2 of 50% with a PaO2 of 206 mmHg (PaO2/FiO2 of 412). After 6 h from his arrival in ICU he was placed on pressure support ventilation (PSV) + sigh and was extubated 18 h later (Table 5). A paralysis of the left hemi-diaphragm was diagnosed on the 3rd postoperative day. On the 5th and 12th postoperative days, he experienced a fall in spirometric value, a worsening of the arterial blood gas test and interstitial infiltrate on chest x-ray that were interpreted as acute lung rejection episodes and treated with intravenous methylprednisolone 500 mg daily × 3 days in the first case and subsequently with methylprednisolone 500 mg followed by recycle with oral prednisone 100 mg, 80 mg, 60 mg, 40 mg and 20 mg. During these episodes, the patient periodically required noninvasive ventilation (NINV) with a facial mask. On the 18th postoperative day the patient was transferred to the ward.

Table 5.  Respiratory parameters during ICU staying
Patient noExtubation time from arrival in ICU (hours)ICU stay (days)PaO2/FiO2 ratio admission ICUPaO2/FiO2 ratio discharge from ICU
2 4 4260419
324 4380428
Mean ± SD17.3 ± 11.58.7 ± 8351 ± 80428 ± 9.5

An early program of intensive respiratory and motor physiotherapy was instituted as an early resumption of the oral feeding.

The patient was discharged 34 days after transplantation. Unfortunately 3.8 years after transplant, due to a nonadherence with immunosuppressive therapy, he developed a ductopenic chronic rejection of the liver and a severe bronchiolitis obliterans syndrome (BOS). Four-and-a-half years after transplantation the patient is alive with a good liver function and under evaluation for lung retransplantation. The current immunosuppressive therapy is tacrolimus, everolimus, mofetil mycophenolate and steroids.

Case 2

A 22.7-year-old man affected by CF with end-stage lung and liver disease (ESLLD) (FEV1 32%, Hypersplenism, secondary biliary cirrhosis, esophageal varices and a previous episode of gastro-esophageal bleeding) with chronic infection of the lungs (Achromobacter Xylosoxidans) underwent combined SBSL-split liver (segments I, IV–VIII) transplantation after a waiting time of 50 days. The grafts were procured from a 36.8-year-old donor (weight 90 kg, height 180 cm). Organ procurement was performed in a standard manner with in situ splitting of the liver (10). The liver was split electively and not to overcome a size mismatch between the donor and the recipient. The reason for splitting was simply the presence of a suitable pediatric recipient on the waiting list for the left lateral segment. A full hemodynamic monitoring, as described for the first case, was undertaken. First, a SBSLTx was performed without giving any heparin. LTx was performed using a standard technique with bi-caval anastomosis. Biliary reconstruction was performed by a duct-to-duct anastomosis. Total ischemia time was 120 min for the first lung, 240 for the second and 420 for the liver. Neither CPB nor VVB was used. The total operative time was 10 h and 30 min. Immunosuppression was based on basiliximab, tacrolimus and steroids. On arrival in ICU, he was on PRVC with a TD of 550 mL (10 mL/kg), with a PEEP of 4 cm H2O, with a FiO2 of 40% and with a PaO2 of 104 mmHg (PaO2/FiO2 of 260). After 2 h from his arrival in ICU he was placed on PSV + sigh and was extubated 2 h later (Table 5). Course in the ICU was uneventful and the patient was discharged and transferred to the ward on 4th postoperative day.

Antibiotic perioperative prophylaxis was with piperacillin. On the 9th postoperative day the patient developed an acute renal failure (tacrolimus trough level 18.4 ng/mL) and a pulmonary interstitial infiltrate on chest x-ray probably related to a fluid overload. Lung biopsies were negative for rejection and a broncho-alveolar lavage was positive for Enterobacter cloacae. An antibiotic therapy (piperacillin-tazobactam, ciprofloxacin and fluconazole) was started. Azathioprine was added to immunosuppression and the tacrolimus dosage was reduced. The clinical picture was resolved with administration of diuretics and restriction of fluids. The patient was discharged on the 27th postoperative day. On the 7th postoperative month the patient was switched from azathioprine to everolimus to prevent a worsening of mild renal failure. In a follow-up of 1.9 years patient is in good condition, with excellent function of the transplanted organs and living a fully autonomous normal life.

Case 3

A 26.4-year-old man affected by CF with end-stage lung and liver disease (FEV1 30%, cirrhosis, hypersplenism, portal hypertension), diabetes mellitus and with chronic infection of the lungs (multi resistant Pseudomonas Aeruginosa) after a waiting time of 676 days underwent SBSL-LTx. Both lungs and the liver were harvested in a standard fashion from a 19.4-year-old donor (weight 80 kg, height 180 cm). A full hemodynamic monitoring was instituted during the entire recipient's procedure (Table 4). LTx was performed, using a standard technique with a bi-caval anastomosis, through a bilateral subcostal incision. Biliary reconstruction was performed by a duct-to-duct anastomosis. Total ischemia time was 225 min for the first lung, 345 for the second and 580 for the liver. Neither CPB nor VVB were used. No heparin was administered during SBSLTx. Total operative time was 10 h and 55 min. Immunosuppression was based on basiliximab, tacrolimus, azathioprine and steroids. Perioperative antibiotics prophylaxis was with ceftazidime, amikacin and fluconazole. On admission in the ICU, he was on PRVC with a TD of 450 mL (10 mL/kg), with a PEEP of 4 cm H2O with a FiO2 of 60% with a PaO2 of 228 mmHg (PaO2/FiO2 of 380). He was placed on PSV + sigh 6 h later and extubated after 18 h. The following course in ICU was uneventful and he was transferred to the ward on the 4th postoperative day.

During his stay in the ward the clinical course was complicated by a transient renal impairment that resolved within a few days with administration of diuretics and the maintenance of the tacrolimus trough level between 6 and 8 ng/mL. The patient was discharged in good condition on 28th postoperative day. Eight months after the transplantation, he as well as the grafts are currently functioning within normal levels.


  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and Methods
  5. Discussion
  6. Acknowledgments
  7. References

Cystic fibrosis is the most common indication for combined thoracic organ-liver transplantation.

Patients affected by CF may require a transplant in three different situations. The most common, is a patient with end-stage lung disease and an almost normal liver who will need a replacement of the lungs. The second possible situation is a patient with a mild to moderate lung disease (FEV1 40–69%) combined with an end-stage liver disease, requiring an LTx. In fact about 20–30% of CF patients will develop a liver cirrhosis and progress to portal hypertension, hypersplenism, variceal bleeding and eventually, end-stage liver failure (11). Some authors have proposed a scoring system that might be used to decide about timing of LTx (12,13). LTx has become the treatment of choice for end-stage liver disease in CF patients, but its utility is limited by the severity of the lung disease. LTx should probably be performed before severe worsening of lung function (FEV1 < 50%). It has been shown that pulmonary function remains stable or can significantly improve after isolated liver transplantation for CF in patients with mild to moderate lung disease (1,12,13).

The third situation, an uncommon scenario, is when an end-stage liver disease is associated with a severe lung disease. In this situation replacement of both liver and lungs may be the option of choice because these patients would not be expected to survive transplantation of either organ alone. In the past, ‘en bloc’ transplantation of heart and lungs have been widely used in these patients. After the introduction of SBSLTx, the techniques of the ‘en bloc’ double lung or heart/lung transplantation have become obsolete. Aside from case reports, only three series of combined thoracic organ-liver transplantation for CF (1 from United Kingdom, 1 from France and 1 from United States) are reported in the literature (6–8,14,15). A total of 12 heart-lung-liver transplantations and 16 SBSL-LTx have been reported (Table 6), all of them performed with the use of CPB.

Table 6.  Largest series reported for Heart-Lung-Liver (H-L-L) and Double Lung-Liver (L-L) transplantation for cystic fibrosis.
AuthorYearOrgans transplantedNoFEV1% predicted (Mean)Cardio-pulmonary by-passFollow-up monthsOverall survival (%)
  1. 1 1 en bloc double lung-liver transplantation; 3 sequential double lung liver transplantation; 1 bilateral lobar lung transplantation from a split left lung and reduced liver (left lobe) transplantation.

  2. 2 2 sequential double lung-whole liver transplantation; 1 sequential double lung—extended right split liver graft (segment I, IV–VIII) transplantation.

Couetil (14)1995H-L-L5 Yes 
 - (29%) 6/10 (60%)
L-L15 Yes  
Praseedom (8)2001H-L-L720–38 (29%)Yes0.5–91 2/7 (29%)
Barshes (6)2005L-L11 22–38 (30%)Yes0.7–908/11 (73%)
Present series2007L-L2325–32 (29%)No 8.1–51.1  3/3 (100%)

In our series with a median follow-up of 670 days (range 244–1533), all the recipients are alive for an overall survival of 100%. The development of chronic rejection of the liver and a severe BOS in the first transplanted patients, due to a noncompliance with the immunosuppressive therapy, raises the problem of an adequate psychological support in this type of patient (16).

Our series of patients has several peculiarities. The combined lung-liver transplants have been performed by the same surgical team, which at our Institution is leading both the liver and the lung transplantation programs. In all the three cases no CPB was used. Except for lung transplants performed for pulmonary vascular disease, CPB is used in a selective fashion. CPB is warranted when the patients develop refractory pulmonary hypertension, poor right ventricular function, hemodynamic instability, hypoxemia or worsening hypercarbia during single lung ventilation or temporary occlusion of one branch of the pulmonary artery. During SBSLTx, CPB may also be required to facilitate implantation of the second lung, due to dysfunction of the first allograft implanted. The requirement for CPB, in these cases, is usually dependent on unpredictable intra-operative factors (17). In fact, according to our protocol, use of CPB is indicated when patients develop, intra-operatively, a severe pulmonary hypertension (mean PAP > 40 mmHg) or a PaO2 < 45 mmHg or cardiac arrhythmia, or a right heart insufficiency (pressure in the right atrium > 15 mmHg) or pulmonary vascular resistance (PVR) > 6 U wood. None of our recipients had any of these indications for using CPB. Since the need for CPB during lung transplantation depends often on unpredictable intra-operative factors, we start the procedure with the CPB circuit set ready for use and with the perfusionist present in the operating room. Usually, a trial cross-clamping of the first pulmonary artery is performed; if this is tolerated we proceed straight with the removal of the native lung and implantation of the graft, otherwise the CBP is first established. The same assessment is performed before proceeding with the second lung.

Increase in PaCO2 (case 1 and case 3) may be tolerated as long as adequate oxygenation and hemodynamic stability are maintained. To our patients, vasopressors (dopamine and noradrenalin) were administered to support function of the right ventricle. Furthermore, inhaled nitric oxide was used in all the three cases to improve oxygenation and to lower increased PVR. In the management of these three cases of SBSL-LTx, our attitude was to exactly reproduce the standard techniques that we use for isolated SBSLTx and LTx. Regarding LTx in adulthood we have always adopted the technique of bi-caval anastomosis without using VVB.

Although currently used safely, the use of CPB may have some potential disadvantages: (i) the necessity to administer a large volume of crystalloid that can have a negative impact on the pulmonary grafts, (ii) the requested systemic heparinization increase the risk of bleeding that may lead to severe coagulopathy and fibrinolysis, (iii) neurological and renal complications are common after CPB. Thus, lung transplantation is performed without CPB whenever possible. Overall in our experience with lung transplantation, CPB has been used in 22% (5 out of 23) of adult recipients and 85% (6 out of 7) of pediatric recipients.

In our series, coagulopathy was of mild grade (INR range 1.3–2.17) and was managed by administration of fresh frozen plasma (FFP) and tranexamic acid during the entire procedure in all of the cases. Portal hypertension did not seem to interfere at all with the thoracic procedures. During the operation, 4 units of packed red blood cells (PRBC) and 8 units of FFP were administered to patient 1, 3 units of PRBC and 2 units of FFP were transfused to patient 2 and 9 units of PRBC and 7 units of FFP were administered to patient 3. During the ICU stay, no further blood products were given to patient 2; two units of PRBC were administered to patient one on the 2nd postoperative day; on the 1st postoperative day, patient 3 was transfused with 1 unit of PRBC and 2 units of FFP.

The elective use in one case of a right split graft, not forced by any size mismatch between the donor and the recipient, reflects our policy of extensive use of the splitting technique. We have previously reported that with such policy the outcome of right split grafts at our Institution is not worse, rather better although not significantly, than that of whole size livers (18).

In our experience liver transplantation did not show any detrimental effect on the transplanted lungs. Once the lungs were replaced, they immediately demonstrated adequate function and the subsequent course of the transplantation of the liver was similar to that of an isolated LTx.

All the recipients of a combined SBSL-LTx had a minimal ventilator support in the ICU and were extubated within 24 h from admission. The first patient needed a prolong ICU stay due to a lung rejection episode and an infection with a concomitant paralysis of the left hemidiaphragm that required a NINV with a facial mask. Otherwise the course in the ICU of the remaining two recipients was quite short (4 days).

The last peculiar characteristic of this series has been the immunosuppressive regimen adopted. All the combined thoracic organ-liver transplantations reported in the literature have been immunosuppressed with antilymphocyte globulin, tacrolimus or cyclosporine, steroids and azathioprine. In our patients, we used basiliximab as induction and the maintenance therapy was based on tacrolimus and steroids. Azathioprine or everolimus were added to reduced tacrolimus trough level to preserve an already impaired renal function due to a long lasting history of massive antibiotic therapy for recurrent lungs infections. It has been suggested that transplantation of the liver along with other organs may offer an immunologic advantage (19,20). Barshes et al. (6) have observed 26 episodes of lung rejection and 8 episodes of liver rejection among 11 recipients of a combined bilateral lung-liver transplantation and concluded that the liver did not have a demonstrable immunosuppressive protective effect regarding the associated transplanted thoracic organs. Differently from these findings, in our series we observed only two episodes of lung rejection in the first patient (manifested by a deterioration of the blood gas test and interstitial infiltrate at chest x-ray, not biopsy proven) on the 5th and 12th postoperative day that was resolved with steroids boluses. The other two patients with a follow-up of 670 and 244 days did not show any sign of liver rejection, lung acute rejection or BOS. Thus we concluded that at least in term of acute rejection the associated liver transplant might play a role.

In conclusion, combined SBSL-LTx is a very rare and challenging operation that can be performed safely without using CPB and VVB. In patients with CF end-stage liver disease and severe lung disease this therapeutic option should be aggressively pursued since the expected patient survival appears comparable to that of isolated transplantation of the lungs or the liver.


  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and Methods
  5. Discussion
  6. Acknowledgments
  7. References

The authors thank Rose Luciano for her contribution in reviewing the manuscript.


  1. Top of page
  2. Abstract
  3. Introduction
  4. Patients and Methods
  5. Discussion
  6. Acknowledgments
  7. References
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