Hepatopulmonary Syndrome After Living Donor Liver Transplantation and Deceased Donor Liver Transplantation: A Single-Center Experience

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1 Hepatopulmonary Syndrome After Living Donor Liver Transplantation and Deceased Donor Liver Transplantation: A Single-Center Experience Elizabeth J. Carey, 1 David D. Douglas, 1 Vijayan Balan, 1 Hugo E. Vargas, 1 Thomas J. Byrne, 1 Adyr A. Moss, 2 and David C. Mulligan 2 Hepatopulmonary syndrome (HPS) is a progressive, debilitating complication of end-stage liver disease. In contrast to the well-established reversal of HPS after deceased donor liver transplantation (DDLT), little has been written about the natural course of HPS after the newer procedure of living donor liver transplantation (LDLT). We describe HPS in a small series of 4 liver transplant recipients (2 DDLT; 2 LDLT) at a single center. Before transplantation, these 4 patients had a mean shunt fraction of % and a mean PaO 2 of mm Hg. All 4 patients used supplemental oxygen before transplantation. Sixteen weeks after transplantation, all 4 patients had normalized or improved shunt fraction and PaO 2. These patients regained normal pulmonary function within a few months, despite the period of hepatic regeneration after LDLT. In conclusion, both DDLT and LDLT are associated with rapid and dramatic reversal of HPS. (Liver Transpl 2004;10: ) Hepatopulmonary syndrome (HPS) is a progressive, debilitating complication of end-stage liver disease that occurs in 4 to 22% of liver transplant candidates. 1 3 The diagnosis of HPS rests on the triad of cirrhosis, hypoxemia, and intrapulmonary vascular dilation. 4,5 HPS can greatly impair quality of life. Patients suffer from progressive dyspnea and often require supplemental oxygen. Several medications have been used to treat HPS, but the results have been disappointing. 5 Liver transplantation is the only known cure for HPS. 5 The onset of HPS may be an indicator of poor prognosis. In the absence of transplantation, patients with HPS have a mortality rate as high as 41% within 2.5 years after the onset of symptoms. 6 Although the reversal of HPS after deceased donor liver transplantation (DDLT) is well established, 1,5,7 the course of HPS after living donor liver transplantation (LDLT) is not well described. Japanese reports have documented the reversal of HPS in children after LDLT, 8 but there is little information on the course of HPS after LDLT in the United States. We describe our experience with HPS after DDLT and LDLT in a single-center setting. Methods Patients All patients evaluated for liver transplantation at our center are routinely screened for HPS. All patients who were diagnosed with HPS and who underwent liver transplantation at our center between June 1999 and August 2003 are included in this series. Diagnosis of HPS The diagnosis of HPS was based on the following criteria: 1. End-stage liver disease diagnosed by advanced fibrosis on liver biopsy specimens, imaging findings consistent with cirrhosis, or a Child-Turcotte-Pugh score of 7 or more. 2. Hypoxemia with a room air PaO 2 of less than 70 mm Hg on arterial blood gas. 3. Delayed positive contrast enhanced echocardiography, a positive nuclear medicine cardiac shunt study, or both. Screening for HPS All candidates for liver transplantation at our center undergo the following routine tests as part of the pretransplantation work-up: arterial blood gas analysis, pulmonary function testing (e.g., spirometry, lung volumes, and reduced oxygen-diffusing capacity), and transthoracic 2-dimensional echocardiography to estimate pulmonary arterial and right atrial pressures. When the PaO 2 is less than 70 mm Hg, a contrast-enhanced bubble echocardiogram is added. If the contrast-enhanced echocardiogram is positive, a nuclear medicine cardiac shunt detection study is obtained to quantify the size of the shunt. Abbreviations: HPS, hepatopulmonary syndrome; DDLT, deceased donor liver transplantation; LDLT, living donor liver transplantation; PaO 2, partial pressure of oxygen, arterial; OLT, orthotopic liver transplantation; GMT, geometric mean of technetium; NM, nuclear medicine. From the 1 Division of Transplantation Medicine and the 2 Division of Transplant Surgery, Mayo Clinic, Scottsdale, Arizona. This work is published in abstract form in Am J Transplant 2003; 3(Suppl 5):241. Address reprint requests to David D. Douglas, MD, Division of Transplantation Medicine, Mayo Clinic Hospital, 5777 East Mayo Boulevard, Phoenix, AZ Telephone: ; FAX: ; Douglas.david@mayo.edu Copyright 2004 by the American Association for the Study of Liver Diseases Published online in Wiley InterScience ( DOI /lt Liver Transplantation, Vol 10, No 4 (April), 2004: pp

2 530 Carey et al. Table 1. Characteristics of 4 Patients With Hepatopulmonary Syndrome Before Liver Transplantation Patient No. Age Gender Diagnosis Procedure Graft: Recipient Weight Ratio SaO 2 (%) Room Air PaO 2 100% oxygen Shunt Index* (%) O 2 Use 1 28 F NASH DDLT Yes 2 48 M HCV, ALD DDLT Yes 3 50 M HBV LDLT 0.8% Yes 4 48 M HCV LDLT 1.2% Yes Abbreviations: ALD, alcoholic liver disease; DDLT, deceased donor liver transplantation; HBV, hepatitis B virus; HCV, hepatitis C virus; LDLT, living donor liver transplantation; MELD, Model for End-Stage Liver Disease; NASH, nonalcoholic steatohepatitis; SaO 2, percent oxygen saturation. *A shunt index of 5% is normal. Twelve months after DDLT, shunt index was 5.2%. Arterial Blood Gas To determine the arterial blood gas of patients, a standard radial artery puncture was used to obtain a blood sample. Arterial blood gas analyses were performed with patients sitting at rest and breathing room air. A PaO 2 of less than 70 mm Hg was the cutoff for hypoxemia; these patients were further evaluated for HPS. If the PaO 2 was less than 70 mm Hg, arterial blood gas measurement was repeated on 100% inspired oxygen. Failure for the PaO 2 to reach a value of at least 300 mm Hg with 100% inspired oxygen suggests the presence of large anatomic arteriovenous shunts that will not respond to liver transplantation. Contrast-Enhanced Echocardiogram All patients whose arterial blood gas showed hypoxemia underwent contrast-enhanced echocardiography. To screen for intracardiac or intrapulmonary shunting, hand-agitated saline was administered intravenously during the procedure. The echocardiogram was considered positive for intrapulmonary shunting when it showed delayed (more than 3 cardiac cycles) microbubble opacification of the left heart chambers. Doppler assessment of pulmonary arterial pressure was conducted during the same examination. Nuclear Medicine Lung Perfusion Scan If the contrast-enhanced echocardiogram was positive, a nuclear medicine lung perfusion scan was obtained to quantify the size of the intrapulmonary shunt. Total body imaging was performed 5 minutes after the intravenous administration of technetium-labeled macroaggregated albumin. Assuming that 13% of the cardiac output is delivered to the brain, 9 the extrapulmonary shunt fraction was calculated with the geometric mean of technetium (GMT) counts around the brain and the lung using the following formula: (GMT brain) / (GMT brain GMT lung) A shunt fraction of greater than 5% was considered abnormal and consistent with HPS. 10 Results Preoperative Characteristics Between June 1999 and August 2003, 156 patients underwent liver transplantation at our institution (133 DDLT; 23 LDLT). Four patients with HPS received transplants Table 2. Post-Operative Course of 4 Patients with Hepatopulmonary Syndrome 4 Months After Liver Transplantation Post-Transplant Patient No. PaO 2 on Room Air Shunt Index (%)* O 2 use (days) Abbreviations: ALD, alcoholic liver disease; DDLT, deceased donor liver transplantation; HBV, hepatitis B virus; HCV, hepatitis C virus; LDLT, living donor liver transplantation; MELD, Model for End-Stage Liver Disease; NASH, nonalcoholic steatohepatitis. *A shunt index of 5% is normal. Twelve months after DDLT, shunt index was 5.2%.

3 Hepatopulmonary Syndrome Posttransplantation 531 Figure 1. Improvement in oxygenation (PaO 2 ) on room air of 2 patients after DDLT and of 2 patients after LDLT. Abbreviations: DDLT, deceased donor liver transplantation; LDLT, living donor liver transplantation; OLT, orthotopic liver transplantation; PaO 2, partial pressure of oxygen. (2.6%) (Table 1). Before transplantation, the mean shunt fraction in the patients with HPS was %, and the mean PaO 2 was mm Hg. All 4 patients required supplemental oxygen at rest. Pulmonary arterial pressure was normal in all 4 patients. Postoperative Course Patient 1 (DDLT) had a remote history of a ventriculoperitoneal shunt for hydrocephalus. Hypoxia requiring the use of supplemental oxygen developed 3 months before the transplant evaluation. The work-up for HPS, including arterial blood gas measurement and nuclear medicine (NM) shunt detection, was performed during the transplant evaluation. After the transplant evaluation, the shunt was revised to a ventriculopleural shunt to prevent infection of the brain ventricles during liver transplantation. Six months later, a cadaveric organ became available, and liver transplantation was performed. The postoperative recovery was unremarkable, and the patient was released from the hospital in 7 days. After transplantation, a unilateral pleural effusion developed on the side of the shunt, mandating 2 further hospitalizations for therapeutic thoracentesis and symptom control. Patient 1 required supplemental oxygen for 90 days after transplantation; dyspnea resolved entirely by 4 months after transplantation. The shunt was revised back to a ventriculoperitoneal shunt 5 months after transplantation without recurrence of hypoxia, dyspnea, or pleural effusion. It is difficult to determine the relative contributions of HPS and the pleural effusion to this patient s symptoms in the months after transplantation. After therapeutic thoracentesis, she reported less dyspnea and had decreased need for supplemental oxygen, supporting a role for the pleural effusion in her symptoms. However, dyspnea and use of supplemental oxygen resolved spontaneously by the fourth month after orthotopic liver transplantation, before the ventriculopleural shunt was revised and before the resolution of a moderate-sized pleural effusion, suggesting HPS as the cause of her symptoms. Patient 2 (DDLT) had an intraoperative cardiac arrest that necessitated cardiopulmonary resuscitation and cardioversion. HPS was not believed to have contributed to the arrest. Postoperatively, renal failure developed, and the patient required temporary dialysis. He was discharged 3 weeks after transplantation, and his renal function recovered soon thereafter. Supplemental oxygen was discontinued 30 days after transplantation, and no further cardiopulmonary events have occurred. Patient 3 (LDLT) had a prolonged hospitalization because of a posttransplantation bile leak. The patient improved after percutaneous biliary stenting and was released from the hospital. Symptoms of HPS resolved within 10 days after transplantation. Patient 4 (LDLT) had an uneventful postoperative course and was released 5 days after transplantation. Supplemental oxygen was discontinued 30 days after transplantation. All 4 patients are still alive at a mean of 16 months after transplantation. Before transplantation, 2 patients had a shunt fraction of more than 20%, and 1 patient had both a PaO 2 of less than 50 mm Hg and a shunt fraction of more than 20%. Patient 2 had a major perioperative complication that probably was not related to HPS. He suffered an intraoperative cardiac arrest, despite having a good-quality preoperative dobutamine stress echocardiogram negative for myocardial ischemia or structural heart disease. A postoperative echocardiogram in this patient showed only Figure 2. Improvement in the nuclear medicine shunt index of 2 patients after DDLT and of 2 patients after LDLT. Abbreviations: DDLT, deceased donor liver transplantation; LDLT, living donor liver transplantation; OLT, orthotopic liver transplantation. Note: A shunt index of < 5% is normal.

4 532 Carey et al. hyperdynamic left ventricular function and trivial mitral valve regurgitation. Acute tubular necrosis developed postoperatively, and he required hemodialysis for approximately 6 weeks. He has had no further cardiopulmonary complications, and the HPS has resolved. Postoperative Pulmonary Function HPS was reassessed 4 months after transplantation with a repeat nuclear medicine lung perfusion scan. Patients 2, 3, and 4 had complete normalization of the intrapulmonary shunt ( 5%) (see Table 2), and patient 1 had significant improvement. Mean PaO 2 improved in all patients after transplantation. All patients were able to discontinue the use of supplemental oxygen within 90 days of transplantation. Living donor recipients seemed to resolve their HPS comparably to their deceased donor recipient counterparts, as characterized by an improvement in nuclear medicine shunt fraction and oxygenation 4 months after transplantation (Figure 1 and 2). Discussion HPS is a complication of end-stage liver disease associated with significant morbidity. Patients with HPS often have debilitating hypoxemia and require the use of supplemental oxygen. Pharmacologic treatment of HPS has been suboptimal, and liver transplantation is the only known cure. Reversal of HPS after DDLT has been well described, but this is the first known report in the United States of HPS resolving after LDLT. The pathophysiology of HPS is not understood completely. Abnormal dilation of the pulmonary vasculature results in the shunting of deoxygenated blood into the systemic circulation. Autopsy studies have shown dilation of the precapillary and capillary vessels. 6,11 Pulmonary angiography demonstrates diffuse abnormality without discrete arteriovenous communication. The pathogenesis of the pulmonary vascular abnormalities has not been determined precisely but may be the result of retention of a vascular mediator normally cleared by the liver or the production of one by the diseased liver. The presence of portal hypertension results in an increased return to the systemic circulation of blood from the inferior vena cava that has bypassed the liver completely. Nitric oxide, a potent vasodilator, has been implicated as a mediator of HPS. Increased concentrations of exhaled nitric oxide have been found in cirrhotic patients, with a return to normal levels after transplantation. 12 The oxygenation abnormalities of HPS do not reverse immediately after transplantation, and in fact take months to resolve. This slow resolution suggests that vascular remodeling must occur before oxygenation normalizes and that increased levels of nitric oxide may be a secondary phenomenon. Animal models of HPS suggest that the production of nitric oxide in pulmonary vasculature increases because of enhanced endothelin-b receptor expression and because of the production of endothelin-1 mediated nitric oxide synthase. 13 Many authors describe near-universal improvement in HPS after liver transplantation, although complete resolution may take as long as 1 year. 1,7,14,15 Once thought to be a contraindication to liver transplantation, HPS is now considered an indication for liver transplantation in many patients. Careful patient selection is important, however, because HPS is associated with increased mortality after transplantation. A prospective study of 24 liver transplant recipients found 29% mortality in the first 10 weeks after transplantation, with 5 of the 7 deaths resulting from cardiopulmonary complications. 16 The strongest predictors of postoperative mortality were a preoperative PaO 2 of less than 50 mm Hg alone or in combination with a shunt fraction of more than 20%. LDLT is a new procedure being performed with increasing frequency in the United States. It is an attractive option for transplant candidates who face a prolonged wait time for a cadaveric organ. The living donor undergoes a right hepatic lobectomy, and the excised lobe is then transplanted into the recipient. Within 30 days, both the recipient graft and the donor remnant regenerate to almost full size, with the majority of regeneration occurring within the first 2 weeks. 17,18 Although both DDLT and LDLT result in a fully functional graft for the recipient, there are differences in the course of recovery between the 2 procedures. Compared with DDLT, LDLT is associated with increased concentrations of serum bilirubin and with increased prothrombin times during the first 3 to 4 days after transplantation. At 1 week, LDLT and DDLT recipients show no difference in aminotransferase levels or in synthetic function 17 ; however, drug metabolism differs. At the same medication dose, LDLT recipients have higher blood concentrations of cyclosporine than do DDLT recipients. 19 This finding extends to 6 months after transplantation longer than expected given the rapid regeneration of hepatic tissue. Recurrence of hepatitis C virus also is reported to be more severe after LDLT, 20,21 although more recent reports have found no difference in outcome between DDLT and LDLT for hepatitis C. 22,23 A graft-to-recipient weight ratio of 0.8% is recommended in LDLT to ensure adequate hepatic function for the recipient. 17 Whether a ratio of 0.8% is sufficient for the resolution of HPS after LDLT is a question that can-

5 Hepatopulmonary Syndrome Posttransplantation 533 not be answered by this small series. One LDLT patient in this series had a ratio of 0.8%, and the other had a ratio of 1.2%. Both LDLT patients had mild HPS that rapidly reversed after transplantation, with cessation of supplemental oxygen within 1 month and normalization of intrapulmonary shunting by 4 months after LDLT. On the basis of these limited data, it appears that a graft-torecipient weight ratio of 0.8% is sufficient for resolution of mild HPS, but increased experience with LDLT will help to gain further insight into this process. Egawa and colleagues 14 described 21 patients with HPS who had LDLT in Japan (19 children and 2 adults), all with biliary atresia as the underlying cause of liver disease. Patients with HPS had higher rates of wound infection and bile leak, but their HPS improved after transplantation. Graft volume was not addressed in this study. We have found no previous reports of adult patients with HPS undergoing LDLT in the United States. We report excellent outcomes in a small series of patients with HPS who had LDLT or DDLT. Although a series of 4 patients is too small to detect significant differences, the resolution of HPS in the LDLT patients appeared to mirror that in the DDLT patients. Despite the period of hepatic regeneration required after LDLT, oxygenation returned to normal in both patients within 4 months after transplantation. One DDLT patient had a large shunt preoperatively that was much improved but not fully resolved at the 4-month follow-up. One year after DDLT, the shunt had almost completely normalized. All 4 patients no longer require supplemental oxygen and have no residual cardiopulmonary abnormalities at a mean follow-up of 16 months. Resolution of HPS after LDLT is comparable to that observed in patients with DDLT. References 1. Battaglia SE, Pretto JJ, Irving LB, Jones RM, Angus PW. Resolution of gas exchange abnormalities and intrapulmonary shunting following liver transplantation. Hepatology 1997;25: Martinez GP, Barbera JA, Visa J, Rimola A, Pare JC, Roca J, et al. Hepatopulmonary syndrome in candidates for liver transplantation. J Hepatol 2001;34: Stoller JK, Lange PA, Westveer MK, Carey WD, Vogt D, Henderson JM. Prevalence and reversibility of the hepatopulmonary syndrome after liver transplantation: The Cleveland Clinic experience. West J Med 1995;163: Fallon MB, Abrams GA. Pulmonary dysfunction in chronic liver disease. Hepatology 2000;32: Krowka MJ. Hepatopulmonary syndrome: Recent literature (1997 to 1999) and implications for liver transplantation. Liver Transpl 2000;6(Suppl 1):S31 S Scott VL, Dodson SF, Kang Y. The hepatopulmonary syndrome. Surg Clin North Am 1999;79: Collisson EA, Nourmand H, Fraiman MH, Cooper CB, Bellamy PE, Farmer DG, et al. Retrospective analysis of the results of liver transplantation for adults with severe hepatopulmonary syndrome. Liver Transpl 2002;8: Kikuchi H, Ohkohchi N, Orii T, Satomi S. Living-related liver transplantation in patients with pulmonary vascular disease. Transplant Proc 2000;32: Wade OL, Bishop JM. Cardiac Output and regional blood flow. Oxford: Blackwell Scientific; Ueki J, Hughes JMB, Peters AM, Bellingan GJ, Mohammed MA, Dutton J, et al. Oxygen and 99mTc-MAA shunt estimations in patients with pulmonary arteriovenous malformations: Effects of changes in posture and lung volume. Thorax 1994;49: Herve P, Lebrec D, Brenot F, Simonneau G, Humbert M, Sitbon O, et al. Pulmonary vascular disorders in portal hypertension. Eur Respir J 1998;11: Rolla G, Brussino L, Colagrande P, Scappaticci E, Morello M, Bergerone S, et al. Exhaled nitric oxide and impaired oxygenation in cirrhotic patients before and after liver transplantation. Ann Intern Med 1998;129: Luo B, Liu L, Tang L, Zhang J, Stockard CR, Grizzle WE, et al. Increased pulmonary vascular endothelin B receptor expression and responsiveness to endothelin-1 in cirrhotic and portal hypertensive rats: A potential mechanism in experimental hepatopulmonary syndrome. J Hepatol 2003;38: Egawa H, Kasahara M, Inomata Y, Uemoto S, Asonuma K, Fujita S, et al. Long-term outcome of living related liver transplantation for patients with intrapulmonary shunting and strategy for complications. Transplantation 1999;67: Krowka MJ, Porayko MK, Plevak DJ, Pappas SC, Steers JL, Krom RA, et al. Hepatopulmonary syndrome with progressive hypoxemia as an indication for liver transplantation: Case reports and literature review. Mayo Clin Proc 1997;72: Arguedas MR, Abrams GA, Krowka MJ, Fallon MB. Prospective evaluation of outcomes and predictors of mortality in patients with hepatopulmonary syndrome undergoing liver transplantation. Hepatology 2003;37: Marcos A, Fisher RA, Ham JM, Shiffman ML, Sanyal AJ, Luketic VA, et al. Liver regeneration and function in donor and recipient after right lobe adult to adult living donor liver transplantation. Transplantation 2000;69: Shiffman ML, Brown RS Jr, Olthoff KM, Everson G, Miller C, Siegler M, et al. Living donor liver transplantation: Summary of a conference at The National Institutes of Health. Liver Transpl 2002;8: Trotter JF, Stolpman N, Wachs M, Bak T, Kugelmas M, Kam I, et al. Living donor liver transplant recipients achieve relatively higher immunosuppressant blood levels than cadaveric recipients. Liver Transpl 2002;8: Gaglio PJ Sr, Malireddy S, Russo M, Lapointe-Rudow D, Emond JC, Brown RS Jr. Hepatitis C recurrence in recipients of grafts from living vs cadaveric liver donors [abstract]. Hepatology 2002;36:265A. 21. Taniguchi M, Wachs M, Bak T, Trotter J, Kugelmans M, Everson G, et al. Hepatitis C recurrence in living donor liver transplantation [abstract]. Am J Transplant 2002;2(Suppl 3): Rodriguez-Luna H, Vargas HE, Sharma P, De Petris G, Ortiz J, Balan V, et al. Hepatitis C virus recurrence in living donor liver transplant recipients. Dig Dis Sci 2004;49: Shiffman ML, Fisher RA, Stravitz T, Luketic VA, Sanyal AJ, Mills AS, et al. Histologic analysis of recurrent hepatitis C virus infection following living donor and cadaveric liver transplantation [abstract]. Am J Transplant 2003;3(S5):203.

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