Abstract
Purpose of Review
Yellow fever is an emerging infectious disease, with epidemics occurring in Africa and South America, and poses great concern due to high lethality rates of up to 60% in severe cases, despite the availability of an efficacious vaccine. In this paper, we sought to review the epidemiology, clinical manifestations, diagnosis, prevention strategies, and treatment in overall and in the transplant population.
Recent Findings
Yellow fever control relies mainly on adequate vaccine coverage, and as the yellow fever vaccine is composed of live, attenuated virus, it is contraindicated in the immunosuppressed individuals, including solid organ transplant and hematopoietic stem cell transplant recipients. Therefore, these patients should be preferably vaccinated in the pre-transplant period. There are few case series where vaccine is given to immunocompromised patients that showed a low incidence of adverse effects, although the number of patients in these reports is small. Donors who live in or with recent travel to yellow fever endemic or epidemic areas should be evaluated as to their suitability for donation. There is no specific therapy for infection and supportive treatment in intensive care units is required in severe cases. Recently, liver transplantation has been performed in several severe yellow fever cases, and although it was lifesaving in some, overall, there were high post-transplant mortality rates.
Summary
Yellow fever is still responsible for devastating epidemics, and some particularities pertaining to the transplant population are discussed. Prevention strategies including vaccination in the pre-transplant period and recommendations for donors living or with recent travel to yellow fever high-risk areas are discussed, as well as recent attempts of treatment with liver transplantation in severe cases.
Similar content being viewed by others
References
Monath TP. Yellow fever: an update. Lancet Infect Dis. 2001;1(1):11–20.
Carter HR. Yellow fever: an epidemiological and historical study of its place of origin. Baltimore, Mp., USA, The Williams & Wilkins Company: United States Public Health Service; 1931. p. 332.
Monath TP, Vasconcelos PFC. Yellow fever. Journal of clinical virology: the official publication of the Pan American Society for Clinical Virology. 2015;64:160–73.
PAHO. Yellow fever 2021 [https://www.paho.org/en/topics/yellow-fever]. Available from: https://www.paho.org/en/topics/yellow-fever.
Chippaux J-P, Chippaux A. Yellow fever in Africa and the Americas: a historical and epidemiological perspective. J Venom Anim Toxins Incl Trop Dis. 2018;24:20.
Barnett ED. Yellow Fever: Epidemiology and Prevention. Clin Infect Dis. 2007;44(6):850–6.
WHO. Yellow Fever 2021
Wang L, Zhou P, Fu X, Zheng Y, Huang S, Fang B, et al. Yellow fever virus: Increasing imported cases in China. J Infect. 2016;73(4):377–80.
Wkly Epidemiol Rec 2017. Yellow fever in Africa and the Americas, 2016 28799735]. Available from: https://www.ncbi.nlm.nih.gov/pubmed/28799735.
Ministry of Health. Monitoramento da Situação Epidemiológica da Febre Amarela no Brasil. 2018. [Available from http://portalarquivos2.saude.gov.br/images/pdf/2018/maio/18/Informe-FA-26.pdf.
Litvoc MN, Novaes CTG, Lopes MIBF. Yellow fever. Rev Assoc Med Bras. 2018;64:106–13.
Johansson MA, Vasconcelos PFC, Staples JE. The whole iceberg: estimating the incidence of yellow fever virus infection from the number of severe cases. Trans R Soc Trop Med Hyg. 2014;108(8):482–7.
Ministry of Health BRAZIL. Manual de manejo clínico da febre amarela www.saude.gov.br/bvs: Ministério da Saúde; 2020 [Available from: http://bvsms.saude.gov.br/bvs/publicacoes/manual_manejo_clinico_febre_amarela.pdf.
Song ATW, Albuquerque LAC. Yellow Fever: Prevention in Transplant Candidates and Emerging Treatment Data for Liver Transplant. Morris MI KC, Wolfe C, editor. Emerging Transplant Infections: Clinical Challenges and Implications; 2020. p.1–16.
Kallas EG, Zanella LGFABD, Moreira CHV, Buccheri R, Diniz GBFD, Castiñeiras ACP, et al. Predictors of mortality in patients with yellow fever: an observational cohort study. Lancet Infect Dis. 2019;19(7):750–8.
Tuboi SH, Costa ZG, da Costa Vasconcelos PF, Hatch D. Clinical and epidemiological characteristics of yellow fever in Brazil: analysis of reported cases 1998–2002. Trans R Soc Trop Med Hyg. 2007;101(2):169–75.
Osório FMF, Cançado GGL, Nardelli MJ, Vidigal PVT, Xavier MAP, Clemente WT. Hepatitis relapse after yellow fever infection: is there another wave? Rev Soc Bras Med Trop. 2020;53:e20200152.
Blandine D, Chirio D, Ponscarme D, Brichler S, Verdière NC, Simon F, et al. Hepatitis rebound after infection with yellow fever virus. Emerg Infect Dis. 2019;25(6):1248–9.
Casadio L, Nastri AC, Malta FM, Araujo J, Silva JB, Salomao J, et al. Late-onset relapsing hepatitis associated with yellow fever. N Engl J Med. 2020;382(21):2059–61.
Rezende IM, Pereira LS, Fradico JRB, Xavier MAP, Alves PA, Campi-Azevedo AC, et al. Late-relapsing hepatitis after yellow fever Viruses. 2020;12:222.
CDC. Yellow Fever: clinical & laboratory evaluation 2015 [Available from: https://www.cdc.gov/yellowfever/healthcareproviders/healthcareproviders-clinlabeval.html.
Domingo C, Patel P, Yillah J, Weidmann M, Méndez JA, Nakouné ER, et al. Advanced yellow fever virus genome detection in point-of-care facilities and reference laboratories. J Clin Microbiol. 2012;50(12):4054–60.
PAHO. Laboratory diagnosis of yellow fever virus infection 2018 [Available from: https://www.paho.org/hq/index.php?option=com_docman&view=download&category_slug=guidelines-5053&alias=46877-laboratory-diagnosis-of-yellow-fever-virus-infection&Itemid=270〈=en.
Shope RE, Woodall JP, Rosa AT. The epidemiology of diseases caused by viruses in groups C and Guama (Bunyaviridae); 2019. p. 37–52.
Nassar ES, Chamelet ELB, Coimbra TLM, Souza LTM, Suzuki A, Ferreira IB, et al. Jungle yellow fever: clinical and laboratorial sudies emphasizing viremia on a human case. Rev. Inst. Med. trop. S. Paulo vol.37 no.4 São Paulo; 1995. p. 337–41.
Reusken CBEM, Knoester M, GeurtsvanKessel C, Koopmans M, Knapen DG, Bierman WFW, et al. Urine as sample type for molecular diagnosis of natural yellow fever virus infections. J Clin Microbiol. 2017;55(11):3294–6.
Barbosa CM, Paola ND, Cunha MP, Rodrigues-Jesus MJ, Araujo DB, Silveira VB, et al. Yellow fever virus RNA in urine and semen of convalescent patient. Brazil Emerg Infect Dis. 2018;17(ed2018):176–8.
Domingo C, Charrel RN, Schmidt-Chanasit J, Zeller H, Reusken C. Yellow fever in the diagnostics laboratory. Emerg Microbes Infect. 2018;7:129.
Morris MI, Grossi P, Nogueira ML, Azevedo LS. Arboviruses recommendations for solid-organ transplant recipients and donors. Transplantation. 2018;102(2S Suppl 2):S42-S51.
Morris MI, Kotton CN, Wolfe C. Emerging transplant infections - clinical challenges and implications 2020.
Grobusch MP, van Aalst M, Goorhuis A. Yellow fever vaccination - once in a lifetime? Travel Med Infect Dis. 2017;15:1–2.
Reinhardt B, Jaspert R, Niedrig M, Kostner C, L'age-Stehr J. Development of viremia and humoral and cellular parameters of immune activation after vaccination with yellow fever virus strain 17D: a model of human flavivirus infection. J Med Virol. 1998;56(2):159–67.
Wyplosz B, Burdet C, François H, Durrbach A, Duclos-Vallée JC, Mamzer-Bruneel MF, et al. Persistence of yellow fever vaccine-induced antibodies after solid organ transplantation. Am J Transplant. 2013;13(9):2458–61.
Monath TP, Cetron MS, Teuwen DE. Yellow fever vaccine. 5ª ed2008. 959–1055 p.
WHO. Detection and investigation of serious adverse events following yellow fever vaccination: WHO; 2008 [Available from: https://www.who.int/publications/i/item/detection-and-investigation-of-serious-adverse-events-following-yellow-fever-vaccination.
Porudominsky R, Gotuzzo EH. Yellow fever vaccine and risk of developing serious adverse events: a systematic review. Rev Panam Salud Publica. 2018;42:e75.
Wieten RW, Goorhuis A, Jonker EFF, Bree GJ, Visser AW, van Genderen PJJ, et al. 17D yellow fever vaccine elicits comparable long-term immune responses in healthy individuals and immune-compromised patients. The Journal of Infection. 2018;72(6).
Croce E, Hatz C, Jonker EF, Visser LG, Jaeger VK, Bühler S. Safety of live vaccinations on immunosuppressive therapy in patients with immune-mediated inflammatory diseases, solid organ transplantation or after bone-marrow transplantation - A systematic review of randomized trials, observational studies and case reports. Vaccine. 2017;35(9):1216–26.
Azevedo LS, Lasmar EP, Contieri FLC, Boin I, Percegona L, Saber LTS, et al. Yellow fever vaccination in organ transplanted patients: is it safe? A multicenter study Transpl Infect Dis. 2012;14(3):237–41.
Miranda LJC, Agena F, Sartori AMC, David-Neto E, Azevedo LS, Pierrotti LC. Awareness of inadvertent use of yellow fever vaccine among recipients of renal transplant. Transplant Proc. 2020;52(5):1291–3.
Fontbrune FS, Arnaud C, Cheminant M, Boulay A, Konopacki J, Lapusan S, et al. Immunogenicity and safety of yellow fever vaccine in allogeneic hematopoietic stem cell transplant recipients after withdrawal of immunosuppressive therapy. J Infect Dis. 2018;217(3):494–7.
Avelino-Silva VI, Freire MS, Rocha V, Rodrigues CA, Novis YS, Sabino EC, et al. Persistence of Yellow Fever vaccine-induced antibodies after cord blood stem cell transplant. Hum Vaccin Immunother. 2016;12(4):937–8.
Pierrotti LC, Duarte-Neto AN, Song ATW, Ventura CG, David-Neto E, Azevedo LS. Fatal Yellow Fever in a Kidney Transplant Patient. Clin Infect Dis. 2020;70(1):144–8.
Buchan CA, Kotton CN. Travel medicine, transplant tourism, and the solid organ transplant recipient-Guidelines from the American Society of Transplantation Infectious Diseases Community of Practice. Clin Transplant. 2019;33(9):e13529.
Grossi PA. Urban Spread of Flaviviruses: A New Challenge in Solid-organ Transplant Recipients. Clin Infect Dis. 2020;70(1):149–51.
Julander JG, Bantia S, Taubenheim BR, Minning DM, Kotian P, Morrey JD, et al. BCX4430, a novel nucleoside analog, effectively treats yellow fever in a Hamster model. Antimicrob Agents Chemother. 2014;58(11):6607–14.
Sbrana E, Xiao S-Y, Guzman H, Ye M, Rosa APAT, Tesh RB. Efficacy of post-exposure treatment of yellow fever with ribavirin in a hamster model of the disease. The American Journal of Tropical Medicine and Hygiene. 2004;71(3).
Freitas CS, Higa LM, Sacramento CQ, Ferreira AC, Reis PA, Delvecchio R, et al. Yellow fever virus is susceptible to sofosbuvir both in vitro and in vivo. PLoS Negl Trop Dis. 2019;13(1:e0007072).
Figueiredo-Mello C, Casadio LVB, Avelino-Silva VI, Yeh-Li H, Sztajnbok J, Joelsons D, et al. Efficacy of sofosbuvir as treatment for yellow fever: protocol for a randomised controlled trial in Brazil (SOFFA study). BMJ Open. 2019;9((11)e027207).
USNLo M. A Study to Evaluate the Safety, Pharmacokinetics and Antiviral Effects of Galidesivir in Yellow Fever or COVID-19. ClinicalTrialsgov. 2020.
Lu X, Xiao H, Li S, Pang X, Song J, Liu S, et al. Double Lock of a Human Neutralizing and Protective Monoclonal Antibody Targeting the Yellow Fever Virus Envelope. Cell Rep. 2019;26:438–46.
Larsen FS, Schmidt LE, Bernsmeier C, Rasmussen A, Isoniemi H, Patel VC, et al. High-volume plasma exchange in patients with acute liver failure: An open randomised controlled trial. J Hepatol. 2016;64(1):69–78.
Ho Y-L, Joelsons D, Leite GFC, Malbouisson LMS, Song ATW, Perondi B, et al. Severe yellow fever in Brazil: clinical characteristics and management. J Travel Med. 2019;26((5):taz040).
Duarte-Neto AN, Cunha MDP, Marcilio I, Song ATW, Martino RB, Ho Y-L, et al. Yellow fever and orthotopic liver transplantation: new insights from the autopsy room for an old but re-emerging disease. Histopathology. 2019;75(5):638–48.
Ministry of Health BRAZIL. PORTARIA N° 1.173 DOU de 01108118.1: Diário Oficial Imprensa Nacional; 2018 [61].
Sousa MV, Zollner RL, Stucchi RSB, Boin IFSF, Ataide EC, Mazzali M. Yellow fever disease in a renal transplant recipient: Case report and literature review. Transpl Infect Dis. 2019;21(5):e13151.
CDC. Transfusion-related transmission of yellow fever vaccine virus. 2010 Jan. MMWR Morb Mortal Wkly Rep. 2010;59(2):34–7.
Slifka MK, Hammarlund E, Lewis MW, Poore EA, Hanifin JM, Marr KA, et al. Antiviral immune response after live yellow fever vaccination of a kidney transplant recipient treated with IVIG. Transplantation. 2013;95(9):e59-61.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
Alice T. W. Song and Wanessa Trindade Clemente declare that they have no conflict of interest.
Human and Animal Rights and Informed Consent
This article does not contain any studies with human or animal subjects performed by any of the authors.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
This article is part of the Topical Collection on Transplant and Oncology
Rights and permissions
About this article
Cite this article
Song, A.T.W., Clemente, W.T. Yellow Fever in Transplantation. Curr Infect Dis Rep 23, 18 (2021). https://doi.org/10.1007/s11908-021-00761-2
Accepted:
Published:
DOI: https://doi.org/10.1007/s11908-021-00761-2