Descriptive study on risk of increased morbidity of schistosomiasis and graft loss after liver transplantation

Graeff-Teixeira, Carlos; Marcolongo-Pereira, Clairton; Kersanach, Betina Bolina; Geiger, Stefan Michael; Negrão-Correa, Deborah

doi:10.1590/0037-8682-0097-2024

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Revista da Sociedade Brasileira de Medicina Tropical

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Review Article • Rev. Soc. Bras. Med. Trop. 57 • 2024 • https://doi.org/10.1590/0037-8682-0097-2024 copy

Descriptive study on risk of increased morbidity of schistosomiasis and graft loss after liver transplantation

Authorship SCIMAGO INSTITUTIONS RANKINGS

ABSTRACT

Solid-organ transplantation procedures have witnessed a surge in frequency. Consequently, increased attention to associated infections and their impact on graft success is warranted. The liver is the principal target for infection by the flatworm Schistosoma mansoni. Hence, rigorous screening protocols for this parasite should be implemented for liver transplantation donors and recipients. This study investigated the risks posed by schistosomiasis-infected liver tissues for successful liver transplantation (LT), considering donors and recipients, by analyzing reported cases. Among the 43 patients undergoing LT (donors = 19; recipients = 24), 32 were infected with S. mansoni, five were infected with other Schistosoma species, and no identification was made in four patients. Reported follow-up periods ranged from 1 to 132 months, and all patients achieved successful recovery. As these helminths do not replicate in their vertebrate hosts, immunosuppressive treatment is not expected to promote increased morbidity or reactivation. Moreover, suspected or confirmed schistosomiasis infections often have a benign course, and generally, should not prevent LT. The available literature was reviewed and a provisional screening protocol has been proposed.

Keywords:
Liver; Transplantation; Schistosoma mansoni; Schistosoma spp; Schistosomiasis

Reference (year)	Number of Cases	Source of infection	Diagnosis of schistosomiasis	PZQ* treatment before/after liver transplantation	PZQ dosages	Evidence for increased morbidity with schistosomiasis in recipients	Time of follow up (months)
⁵5. Kayler LK, Rudich SM, Merion RM. Orthotopic liver transplantation from a donor with a history of schistosomiasis. Transplant Proc. 2003;35(8):2974-76. Available from: https://doi.org/10.1016/j.transproceed.2003.10.065 https://doi.org/10.1016/j.transproceed.2... (2003)	1	Donor	ND**	Before, 5 and 24 months	ND	No	7
²⁷27. Pannegeon V, Masini JP, Paye F, Chazouillères O, Girard PM. Schistosoma mansoni infection and liver graft. Transplantation. 2005;80(2):287. Available from: https://doi.org/10.1097/01.TP.0000158429.94014.B5 https://doi.org/10.1097/01.TP.0000158429... (2005)	1	Donor	Liver biopsy S.mansoni	After 2 days repeated 15 days	ND	No	6
²⁸28. Abdullah K, Abdeldayem H, Hali WO, Sakran A, Yassen K, Abdulkareem A. Twenty cases of adult-to-adult living-related liver transplantation: single-center experience in Saudi Arabia. Transplant Proc. 2005;37(7):3144-46. Available from: https://doi.org/10.1016/j.transproceed.2005.07.056 https://doi.org/10.1016/j.transproceed.2... (2005)	1	Recipient	ND	ND	ND	No	ND
²⁹29. Hoare M, Gelson WT, Davies SE, Curran M, Alexander GJ. Hepatic and intestinal schistosomiasis after orthotopic liver transplant. Liver transplantation. 2005;11(12):1603-07. Available from: https://doi.org/10.1002/lt.20622 https://doi.org/10.1002/lt.20622... (2005)	2	Recipient 1	Gastric biopsy & serology (ND)	After 6 weeks	40 mg/Kg (1 dosis)	No	18
		Recipient 2	Liver biopsy S.mansoni	Before ND time and After 1 year		No	12
³⁰30. Pungpapong S, Krishna M, Abraham SC, Keaveny AP, Dickson RC, Nakhleh RE. Clinicopathologic findings and outcomes of liver transplantation using grafts from donors with unrecognized and unusual diseases. Liver Transplant. 2006;12(2):310-5. Available from: https://doi.org/10.1002/lt.20641 https://doi.org/10.1002/lt.20641... (2006)	3	Donor 1	Liver biopsy & serology	After 1 month	40 mg/Kg (div 2)	No	4 ***
		Donor 2	(MAMA-ELISA) S.mansoni	After 1 month		No	7 ***
		Donor 3		After 1 month		No	22 ***
²⁴24. McManus DP, Dunne DW, Sacko M, Utzinger J, Vennervald BJ, Zhou XN. Schistosomiasis. Nat Rev Dis Primers. 2018;4(1):13. Available from: https://doi.org/10.1038/s41572-018-0013-8 https://doi.org/10.1038/s41572-018-0013-... (2006)	1	Recipient	Liver biopsy & serology, probably S.mansoni	After 6 months	60 mg/Kg (1 dosis)	Yes, raised liver enzymes	ND
³¹31. Ahmed K, Safdar K, Kemmer N, Atiq M, Wang J, Neff GW. Intestinal Schistosomiasis Following Orthotopic Liver Transplantation: A Case Report. Transplant Proc. 2007;39(10):3502-4. Available from: https://doi.org/10.1016/j.transproceed.2007.07.093 https://doi.org/10.1016/j.transproceed.2... (2007)	1	Recipient	Pré-LT: ND	Before LT, ND	ND	Suspected #	132 ****
			Post-LT: intestinal biopsy	time
			Probably S.mekongi
³²32. Kotton CN, Lattes R. Parasitic Infections in Solid Organ Transplant Recipients. Am J Transplant. 2009;9:S234-51. Available from: https://doi.org/10.1111/j.1600-6143.2009.02915.x https://doi.org/10.1111/j.1600-6143.2009... (2009)	1	Donor	Intestinal biopsy, brain-dead donor	After 1, 2, 3, 18, 42 days	40 mg/Kg	No	Not informed
					(div 2)
					(recipient)
			Suspected S. haematobium
³³33. Vincenzi R, Neto JS, Fonseca EA, Pugliese V, Leite KRM, Benavides MR, et al. Schistosoma mansoni infection in the liver graft: The impact on donor and recipient outcomes after transplantation. Liver Transplantation. 2011;17(11):1299-303. Available from: https://doi.org/10.1002/lt.22316 https://doi.org/10.1002/lt.22316... (2011)	6	Donor 1	Liver biopsy	Living donors were treated	Total 80 mg/Kg	No	56
			S.mansoni
		Donor 2	Liver biopsy	Untreated recipients	20mg/Kg bid for 2 days	No	14
			S.mansoni
		Donor 3	Liver biopsy			No	35
			S.mansoni
		Donor 4	Liver biopsy			No	31
			S.mansoni
		Donor 5	Liver biopsy			No	29
			S.mansoni
		Donor 6	Liver biopsy			Suspected ##	ND
			S.mansoni
³⁴34. Ariza-Heredia E, Razonable RR. Incidental hepatic schistosomiasis in a liver transplant recipient. Transpl Infect Dis. 2012;14(1):75-8. (2012)	1	Recipient	Liver biopsy	ND	ND	ND	ND
¹⁰10. Cooper DKC. The White House Organ Summit. Am J Transplant. 2017;17(2):576. Available from: https://doi.org/10.1111/ajt.14056 https://doi.org/10.1111/ajt.14056... (2012)	2	Donor 1	Liver biopsy	Untreated	Untreated	No, died (sepsis)	0.5 *****
			S.mansoni			14 days AFT
		Donor 2	Eggs in stools	Before LT, time was not informed	ND	No	24 ****
			S.mansoni
³⁵35. Osório FMF, Lauar GM, Lima AS, Vidigal PVT, Ferrari TCA, CA Couto. Epidemiological aspects of hepatocellular carcinoma ina referral center of Minas Gerais, Brazil. Arq Gastroenterol. 2013;50(2):97-100. (2013)	2	Recipient 1	Liver biopsy	ND	ND	No	ND
			S.mansoni
		Recipient 2	Liver biopsy	ND	ND	No	ND
			S.mansoni
³⁶36. Brasil IRC, Nepomuceno LR, Schüller RT, Esmeraldo TM, Esmeraldo RM, Esmeraldo RM. Hepatic schistosomiasis as an occasional finding in a transplanted liver. Medicina (Ribeirão Preto) 2013;46(2):178-82. (2013)	1	Donor	Liver biopsy	After 19 days	ND	No	ND
			S.mansoni
³⁷37. Patel R, Patel P, Nagaraju S, Mangus R, Lin J. Incidental Schistosomiasis in Transplant Liver: A Case Report and Review of the Literature. Am J Clin Pathol. 2015;144(S2):A321-A321. (2015)	1	Donor	Liver biopsy	Untreated	untreated	No	ND
			S.japonicum
¹²12. Moghazy W El, Kashkoush S, O’Hali W, Abdallah K. Long-term outcome after liver transplantation for hepatic schistosomiasis: A single-center experience over 15 years. Liver Transplant. 2015;21(1):47-56. Available from: https://doi.org/10.1002/lt.24010 https://doi.org/10.1002/lt.24010... (2015)	14	Recipient	Liver histology & serology (COPT)	Before LT	15mg/Kg	No	12-180 ****
			S.mansoni	Repeated with positive serology	40 mg/Kg div 2
³⁸38. Carrai P, Zammarchi L, Pollina LE, Giordani L, Mangano V, Iapoce R, et al. Post-transplant liver graft schistosomiasis in a migrant from Sub-Saharan Africa. Transpl Infect Dis. 2018;20(5):e12950. Available from: https://doi.org/10.1111/tid.12950 https://doi.org/10.1111/tid.12950... (2018)	1	Recipient	Liver biopsy & serology (AWE-WB), antigen detection (POC-CCA) suspected S.haematobium	After 8 months	Repeated after 21 days	Suspected ###	ND
³⁹39. Kron M, Gordon C, Bauers T, Lu Z, Mahatme S, Shah J, et al. Persistence of schistosoma japonicum DNA in a kidney-liver transplant recipient. Am J Trop Med Hyg. 2019;100(3):584-7. Available from: https://doi.org/10.4269/ajtmh.18-0752 https://doi.org/10.4269/ajtmh.18-0752... (2019)	1	Recipient	Liver and intestines histology	Before, 6 yearly treatment and After 1 year	ND	No	24 ****
			Serology: MAMA
			ELISA
			DNA sequencing: S.japonicum
⁴⁰40. Fonseca-Neto OCL, Parente RI, Rabelo P, Melo PSV, Amorim AG, Jucá N, et al. Use of liver graft with Schistosoma mansoni: report of an unexpected finding. J Bras Transpl. 2019;22(1):1-77. (2019)	1	Donor	Liver biopsy	Untreated	ND	No	ND
			S.mansoni
²⁶26. Falcão LTDM, Batista AD, Maranhão EC, Santos SSF, Madeiro VRV, Moura FM, et al. Schistosomiasis of liver graft as a differential diagnosis of abnormal liver tests after transplantation: report of two cases. Rev Inst Med trop S Paulo. 2023;65:e2. Available from: https://doi.org/10.1590/S1678-9946202365002 https://doi.org/10.1590/S1678-9946202365... (2022)	2	Donor	Liver biopsy	After 18 months	50 mg/Kg	Yes, raised liver enzymes and active granulomas and live eggs	ND
			S.mansoni		(1 dosis)
		Donor	Liver biopsy	After 2 months	50 mg/Kg (1 dosis)		ND
			S.mansoni

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[1] ✉ Dr. Carlos Graeff-Teixeira. e-mail:graeff.teixeira@gmail.com

Recurrence	A more general concept of “coming back”, returning
Recrudescence (Relapse)	A more specific concept of a recurrent deleterious process, disease; exacerbation of lesions or symptoms; example: returning clinical manifestations of malaria from “reactivation” of liver hypnozoites.
Reactivation	Infectious agents that increase metabolism and reproduction activities, after being in a latent or dormant stage; examples: Toxoplasma gondii, Trypanosoma cruzi.
Hyperinfection	De novo infection superimposed on an existing infection; example: Strongyloides stercoralis and the acceleration of infective L3 maturation while still in transit in intestinal lumen leading to successive “waves” of larvae migrating through tissues after penetration in the intestinal mucosa.