Five-year histological and serological follow-up of operationally tolerant pediatric liver transplant recipients enrolled in WISP-R

Hepatology

Volumn 65, Issue 2, 2017, Pages 647-660

  Feng, Sandy ^a   Demetris, Anthony J ^b   Spain, Katharine M ^c   Kanaparthi, Sai ^d   Burrell, Bryna E ^d   Ekong, Udeme D ^e   Alonso, Estella M ^f   Rosenthal, Philip ^a   Turka, Laurence A ^d   Ikle, David ^c   Tchao, Nadia K ^d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c Rho   (United States)

^d Immune Tolerance Network   (United States)

^e YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE AMINOTRANSFERASE; ALLOANTIBODY; AUTOANTIBODY; CD34 ANTIGEN; COMPLEMENT COMPONENT C1Q; COMPLEMENT COMPONENT C4D; GAMMA GLUTAMYLTRANSFERASE; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2; IMMUNOGLOBULIN G3; IMMUNOGLOBULIN G4; IMMUNOSUPPRESSIVE AGENT; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; SMOOTH MUSCLE ACTIN; IMMUNOGLOBULIN G;

ALLOGRAFT; ARTICLE; BILE DUCT ATRESIA; BINDING AFFINITY; BIOPSY NEEDLE; CHILD; CHOLANGITIS; CHOLESTASIS; CLINICAL ARTICLE; DENDRITIC CELL; DIAPHRAGM HERNIA; DRUG WITHDRAWAL; ENDOTHELIUM CELL; FEMALE; FLUORESCENCE; FOLLOW UP; GRAFT FAILURE; GRAFT RECIPIENT; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; LIVER BIOPSY; LIVER GRAFT; LIVER GRAFT REJECTION; LIVER HISTOLOGY; LIVER HYPERPLASIA; LIVING DONOR; MALE; NODULAR REGENERATIVE HYPERPLASIA; PORTAL VEIN OBSTRUCTION; PORTAL VENOPATHY; POSTOPERATIVE COMPLICATION; PRIORITY JOURNAL; PROSPECTIVE STUDY; PROTEIN EXPRESSION; SEROLOGY; STELLATE CELL; VEIN DISEASE; ADVERSE EFFECTS; CLINICAL TRIAL; CONTROLLED STUDY; GRAFT REJECTION; GRAFT SURVIVAL; HISTOCOMPATIBILITY; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; LIVER DISEASES; LIVER TRANSPLANTATION; MULTICENTER STUDY; NEEDLE BIOPSY; PATHOLOGY; PRESCHOOL CHILD; PROCEDURES; RANDOMIZED CONTROLLED TRIAL; RISK ASSESSMENT; TIME FACTOR; TREATMENT OUTCOME;

ALLOGRAFTS; BIOPSY, NEEDLE; CHILD; CHILD, PRESCHOOL; FEMALE; FOLLOW-UP STUDIES; GRAFT REJECTION; GRAFT SURVIVAL; HUMANS; IMMUNOGLOBULIN G; IMMUNOHISTOCHEMISTRY; IMMUNOSUPPRESSIVE AGENTS; ISOANTIBODIES; LIVER DISEASES; LIVER TRANSPLANTATION; LIVING DONORS; MALE; PROSPECTIVE STUDIES; RISK ASSESSMENT; TIME FACTORS; TRANSPLANTATION IMMUNOLOGY; TREATMENT OUTCOME;

EID: 84979544690     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.28681     Document Type: Article

References (50)

1. Londono MC, Rimola A, O'Grady J, Sanchez-Fueyo A. Immunosuppression minimization vs. complete drug withdrawal in liver transplantation. J Hepatol 2013;59:872–879.
2. Orlando G, Manzia T, Baiocchi L, Sanchez-Fueyo A, Angelico M, Tisone G. The Tor Vergata weaning off immunosuppression protocol in stable HCV liver transplant patients: the updated follow up at 78 months. Transpl Immunol 2008;20:43–47.
3. Ekong UD, Melin-Aldana H, Seshadri R, Lokar J, Harris D, Whitington PF, Alonso EM. Graft histology characteristics in long-term survivors of pediatric liver transplantation. Liver Transpl 2008;14:1582–1587.
4. Evans HM, Kelly DA, McKiernan PJ, Hubscher S. Progressive histological damage in liver allografts following pediatric liver transplantation. Hepatology 2006;43:1109–1117.
5. Miyagawa-Hayashino A, Yoshizawa A, Uchida Y, Egawa H, Yurugi K, Masuda S, Minamiguchi S, et al. Progressive graft fibrosis and donor-specific human leukocyte antigen antibodies in pediatric late liver allografts. Liver Transpl 2012;18:1333–1342.
6. Sanada Y, Matsumoto K, Urahashi T, Ihara Y, Wakiya T, Okada N, et al. Protocol liver biopsy is the only examination that can detect mid-term graft fibrosis after pediatric liver transplantation. World J Gastroenterol 2014;20:6638–6650.
7. Scheenstra R, Peeters PM, Verkade HJ, Gouw AS. Graft fibrosis after pediatric liver transplantation: ten years of follow-up. Hepatology 2009;49:880–886.
8. Venturi C, Sempoux C, Quinones JA, Bourdeaux C, Hoyos SP, Sokal E, Reding R. Dynamics of allograft fibrosis in pediatric liver transplantation. Am J Transplant 2014;14:1648–1656.
9. Yoshitomi M, Koshiba T, Haga H, Li Y, Zhao X, Cheng D, et al. Requirement of protocol biopsy before and after complete cessation of immunosuppression after liver transplantation. Transplantation 2009;87:606–614.
10. Grabhorn E, Binder TM, Obrecht D, Brinkert F, Lehnhardt A, Herden U, et al. Long-term clinical relevance of de novo donor-specific antibodies after pediatric liver transplantation. Transplantation 2015;99:1876–1881.
11. Wozniak LJ, Hickey MJ, Venick RS, Vargas JH, Farmer DG, Busuttil RW, et al. Donor-specific HLA antibodies are associated with late allograft dysfunction after pediatric liver transplantation. Transplantation 2015;99:1416–1422.
12. Yamada H, Kondou H, Kimura T, Ikeda K, Tachibana M, Hasegawa Y, et al. Humoral immunity is involved in the development of pericentral fibrosis after pediatric live donor liver transplantation. Pediatr Transplant 2012;16:858–865.
13. Egawa H, Miyagawa-Hayashino A, Haga H, Teramukai S, Yoshizawa A, Ogawa K, et al. Non-inflammatory centrilobular sinusoidal fibrosis in pediatric liver transplant recipients under tacrolimus withdrawal. Hepatol Res 2012;42:895–903.
14. Feng S, Ekong UD, Lobritto SJ, Demetris AJ, Roberts JP, Rosenthal P, et al. Complete immunosuppression withdrawal and subsequent allograft function among pediatric recipients of parental living donor liver transplants. JAMA 2012;307:283–293.
15. DeLeve LD. Liver sinusoidal endothelial cells in hepatic fibrosis. Hepatology 2015;61:1740–1746.
16. Puche JE, Saiman Y, Friedman SL. Hepatic stellate cells and liver fibrosis. Compr Physiol 2013;3:1473–1492.
17. Chen G, Tyan DB. C1q assay for the detection of complement fixing antibody to HLA antigens. Methods Mol Biol 2013;1034:305–311.
18. Muczynski KA, Ekle DM, Coder DM, Anderson SK. Normal human kidney HLA-DR-expressing renal microvascular endothelial cells: characterization, isolation, and regulation of MHC class II expression. J Am Soc Nephrol 2003;14:1336–1348.
19. Page C, Rose M, Yacoub M, Pigott R. Antigenic heterogeneity of vascular endothelium. Am J Pathol 1992;141:673–683.
20. Valenzuela NM, Mulder A, Reed EF. HLA class I antibodies trigger increased adherence of monocytes to endothelial cells by eliciting an increase in endothelial P-selectin and, depending on subclass, by engaging FcgammaRs. J Immunol 2013;190:6635–6650.
21. Tryphonopoulos P, Ruiz P, Weppler D, Nishida S, Levi DM, Moon J, et al. Long-term follow-up of 23 operational tolerant liver transplant recipients. Transplantation 2010;90:1556–1561.
22. Perito ER, Mohammad S, Rosenthal P, Alonso EM, Ekong UD, Lobritto SJ, Feng S. Posttransplant metabolic syndrome in the withdrawal of immunosuppression in Pediatric Liver Transplant Recipients (WISP-R) pilot trial. Am J Transplant 2015;15:779–785.
23. Girnita A, Mazariegos GV, Castellaneta A, Reyes J, Bentlejewski C, Thomson AW, Zeevi A. Liver transplant recipients weaned off immunosuppression lack circulating donor-specific antibodies. Hum Immunol 2010;71:274–276.
24. Ohe H, Waki K, Yoshitomi M, Morimoto T, Nafady-Hego H, Satoda N, et al. Factors affecting operational tolerance after pediatric living-donor liver transplantation: impact of early post-transplant events and HLA match. Transpl Int 2012;25:97–106.
25. Todo S, Yamashita K, Goto R, Zaitsu M, Nagatsu A, Oura T, et al. A pilot study of operational tolerance with a regulatory t cell-based cell therapy in living donor liver transplantation. Hepatology 2016 Jan 16. doi: 10.1002/hep.28459. [Epub ahead of print]
26. Demetris AJ, Zeevi A, O'Leary JG. ABO-compatible liver allograft antibody-mediated rejection: an update. Curr Opin Organ Transplant 2015;20:314–324.
27. Dar W, Agarwal A, Watkins C, Gebel HM, Bray RA, Kokko KE, et al. Donor-directed MHC class I antibody is preferentially cleared from sensitized recipients of combined liver/kidney transplants. Am J Transplant 2011;11:841–847.
28. Olausson M, Mjornstedt L, Norden G, Rydberg L, Molne J, Backman L, Friman S. Successful combined partial auxiliary liver and kidney transplantation in highly sensitized cross-match positive recipients. Am J Transplant 2007;7:130–136.
29. Taner T, Gandhi MJ, Sanderson SO, Poterucha CR, De Goey SR, Stegall MD, Heimbach JK. Prevalence, course and impact of HLA donor-specific antibodies in liver transplantation in the first year. Am J Transplant 2012;12:1504–1510.
30. Rouger P, Gugenheim J, Gane P, Capron-Landereau M, Michel F, Reynes M, Bismuth J. Distribution of the MHC antigens after liver transplantation: relationship with biochemical and histological parameters. Clin Exp Immunol 1990;80:404–408.
31. Knolle P, Schlaak J, Uhrig A, Kempf P, Meyer zum Buschenfelde KH, Gerken G. Human Kupffer cells secrete IL-10 in response to lipopolysaccharide (LPS) challenge. J Hepatol 1995;22:226–229.
32. Thomson AW, Knolle PA. Antigen-presenting cell function in the tolerogenic liver environment. Nat Rev Immunol 2010;10:753–766.
33. Kamada N, Shinomiya T. Serology of liver transplantation in the rat. I. Alloantibody responses and evidence for tolerance in a nonrejector combination. Transplantation 1986;42:7–13.
34. DeVos JM, Gaber AO, Knight RJ, Land GA, Suki WN, Gaber LW, Patel SJ. Donor-specific HLA-DQ antibodies may contribute to poor graft outcome after renal transplantation. Kidney Int 2012;82:598–604.
35. Freitas MC, Rebellato LM, Ozawa M, Nguyen A, Sasaki N, Everly M, et al. The role of immunoglobulin-G subclasses and C1q in de novo HLA-DQ donor-specific antibody kidney transplantation outcomes. Transplantation 2013;95:1113–1119.
36. Tagliamacco A, Cioni M, Comoli P, Ramondetta M, Brambilla C, Trivelli A, et al. DQ molecules are the principal stimulators of de novo donor-specific antibodies in nonsensitized pediatric recipients receiving a first kidney transplant. Transpl Int 2014;27:667–673.
37. Willicombe M, Brookes P, Sergeant R, Santos-Nunez E, Steggar C, Galliford J, et al. De novo DQ donor-specific antibodies are associated with a significant risk of antibody-mediated rejection and transplant glomerulopathy. Transplantation 2012;94:172–177.
38. Kaneku H, O'Leary JG, Banuelos N, Jennings LW, Susskind BM, Klintmalm GB, Terasaki PI. De novo donor-specific HLA antibodies decrease patient and graft survival in liver transplant recipients. Am J Transplant 2013;13:1541–1548.
39. Everly MJ, Rebellato LM, Haisch CE, Briley KP, Bolin P, Kendrick WT, et al. Impact of IgM and IgG3 anti-HLA alloantibodies in primary renal allograft recipients. Transplantation 2014;97:494–501.
40. O'Leary JG, Kaneku H, Banuelos N, Jennings LW, Klintmalm GB, Terasaki PI. Impact of IgG3 subclass and C1q-fixing donor-specific HLA alloantibodies on rejection and survival in liver transplantation. Am J Transplant 2015;15:1003–1013.
41. Loupy A, Lefaucheur C, Vernerey D, Prugger C, Duong van Huyen JP, Mooney N, et al. Complement-binding anti-HLA antibodies and kidney-allograft survival. N Engl J Med 2013;369:1215–1226.
42. Chin C, Chen G, Sequeria F, Berry G, Siehr S, Bernstein D, et al. Clinical usefulness of a novel C1q assay to detect immunoglobulin G antibodies capable of fixing complement in sensitized pediatric heart transplant patients. J Heart Lung Transplant 2011;30:158–163.
43. Kubal CA, Mangus RS, Saxena R, Lobashevsky A, Higgins N, Agarwal A, et al. Crossmatch-positive liver transplantation in patients receiving thymoglobulin-rituximab induction. Transplantation 2014;97:56–63.
44. Drachenberg CB, Papadimitriou JC. Endothelial injury in renal antibody-mediated allograft rejection: a schematic view based on pathogenesis. Transplantation 2013;95:1073–1083.
45. Brunt EM, Gouw AS, Hubscher SG, Tiniakos DG, Bedossa P, Burt AD, et al. Pathology of the liver sinusoids. Histopathology 2014;64:907–920.
46. Deleve LD, Wang X, Guo Y. Sinusoidal endothelial cells prevent rat stellate cell activation and promote reversion to quiescence. Hepatology 2008;48:920–930.
47. Lalor PF, Lai WK, Curbishley SM, Shetty S, Adams DH. Human hepatic sinusoidal endothelial cells can be distinguished by expression of phenotypic markers related to their specialised functions in vivo. World J Gastroenterol 2006;12:5429–5439.
48. Xu B, Broome U, Uzunel M, Nava S, Ge X, Kumagai-Braesch M, et al. Capillarization of hepatic sinusoid by liver endothelial cell-reactive autoantibodies in patients with cirrhosis and chronic hepatitis. Am J Pathol 2003;163:1275–1289.
49. Benseler V, Tay SS, Bowen DG, Bertolino P. Role of the hepatic parenchyma in liver transplant tolerance: a paradigm revisited. Dig Dis 2011;29:391–401.
50. Crispe IN. Immune tolerance in liver disease. Hepatology 2014;60:2109–2117.