868028 case-report20192019 TAI0010.1177/2049936119868028Therapeutic Advances in Infectious DiseaseL Roc, C de Mendoza Therapeutic Advances in Infectious Disease Case Report Rapid subacute myelopathy following Ther Adv Infectious Dis 2019, Vol. 6: 1–8 kidney transplantation from HTLV-1 donors: DOI: 10.1177/ https://doi.org/10.1177/2049936119868028 https://doi.org/10.1177/2049936119868028 2049936119868028 role of immunosuppresors and failure of © The Author(s), 2019. Article reuse guidelines: sagepub.com/journals- antiretrovirals permissions Lourdes Roc, Carmen de Mendoza, Miriam Fernández-Alonso, Gabriel Reina, Vicente Soriano and on behalf of the Spanish HTLV Network Abstract: Two kidney transplant recipients from a single donor became infected with HTLV-1 (human T-lymphotropic virus type 1) in Spain. One developed myelopathy 8 months following surgery despite early prescription of antiretroviral therapy. The allograft was removed from the second recipient at month 8 due to rejection and immunosuppressors discontinued. To date, 3 years later, this patient remains infected but asymptomatic. HTLV-1 infection was recognized retrospectively in the donor, a native Spaniard who had sex partners from endemic regions. Our findings call for a reappraisal of screening policies on donor–recipient organ transplantation. Based on the high risk of disease development and the large flux of persons from HTLV-1 endemic regions, pre-transplant HTLV-1 testing should be mandatory in Spain. Keywords: antiretroviral drugs, HTLV-1, myelopathy, screening, transplantation Received: 26 April 2019; revised manuscript accepted: 16 July 2019. Introduction Spain is one of the world leading countries per- Correspondence to: Vicente Soriano Human T-lymphotropic virus type 1 (HTLV-1) forming solid organ transplants. The annual fig- UNIR Health Sciences infection is a neglected disease despite there being ure is steadily rising, and is currently nearly 5300 School, Calle Almansa 101, Madrid, 28040, Spain 10–15 million people infected worldwide.1,2 As in transplants per year. To date, more than 110,000 vicente.soriano@unir.net HIV infection, chronicity uniformly occurs fol- individuals have benefited from organ donations. Lourdes Roc lowing acute HTLV-1 acquisition and there are More than 60% are kidney transplants, with liver Microbiology Department, Hospital Miguel Servet, no self-limited infections. However, less than 10% being the second most frequent allograft. Heart, Zaragoza of HTLV-1 carriers may develop lifelong clinical lung and pancreas are transplanted less fre- Carmen de Mendoza manifestations, including two life-threatening ill- quently. On the other hand, of the nearly 47 mil- Puerta de Hierro Research Institute and University nesses, namely a subacute invalidating myelopa- lion people currently living in Spain, around Hospital, Majadahonda, thy known as tropical spastic paraparesis (TSP)3 4.5 million are foreigners. In addition, the coun- Madrid, Spain and an acute T-cell leukemia/lymphoma (ATLL).4 try is a frequent destination for tourists, with Miriam Fernández-Alonso Gabriel Reina 75 million visitors during 2016, more than 10% Microbiology Department, HTLV-1 is efficiently transmitted perinatally from HTLV-1 endemic regions.8 Clinica Universitaria, Pamplona (breastfeeding), sexually (more from male to female) and parenterally (transfusions, injection Rapid-onset subacute myelopathy and T lym- drug use and transplants).2 The diagnosis is based phomas associated with HTLV-1 infection have on the demonstration of specific serum HTLV-1 both been reported following solid organ trans- antibodies. A high HTLV-1 proviral load predicts plantation. At least three different scenarios have the risk of disease development5 and sexual trans- been described for HTLV-1 acquisition and dis- mission.6 To date there is neither ­prophylactic ease in the transplantation setting, including vaccine nor effective antiviral therapy.7 infection from the organ donor, contaminated journals.sagepub.com/home/tai 1 Creative Commons Non Commercial CC BY-NC: This article is distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 License (http://www.creativecommons.org/licenses/by-nc/4.0/) which permits non-commercial use, reproduction and distribution of the work without further permission provided the original work is attributed as specified on the SAGE and Open Access pages (https://us.sagepub.com/en-us/nam/open-access-at-sage). Therapeutic Advances in Infectious Disease 6 blood transfusions during surgery, and baseline Patient 2 carriage of HTLV-1 by the recipient.9,10 It seems A 65-year-old male was the second kidney trans- that the immunosuppression used to avoid organ plant recipient from the same infected donor. Like rejection (e.g. corticoids, tacrolimus, cyclo- the other recipient, he was a white native Spaniard sporine, mycophenolate, etc.) plays a major role who denied any risk factor for HTLV-1 infection. in frequent and rapid-onset disease development He also became infected with HTLV-1 after trans- in this population, particularly for HTLV-1 plantation but to date, 3 years later, has not devel- associated myelopathy (HAM).9,10 oped any disease. He received antiretroviral drugs, including zidovudine, lamivudine plus raltegravir during the first 2 months following transplanta- Case reports tion. It should be highlighted that immunosup- pressive therapy (mycophenolate and tacrolimus) Patient 1 dosing had to be reduced from the second month During 2015 a 54-year-old woman underwent due to hematological toxicity. Finally, rejection of kidney transplantation in Spain. She was a white the allograft forced its removal 8 months following native Spaniard and denied any risk factors for transplantation. The patient is no longer undergo- HTLV-1 infection. To date, HTLV testing of ing immunosuppressant treatment and is ­currently blood and tissues in Spain is only recommended undergoing hemodialysis. His proviral load has for ‘donors that came from or live in highly always been low, in the range of 25 HTLV-1 DNA endemic regions, or have either sex partners or copies per 10,000 peripheral blood ­mononuclear parents from those regions’.11 However, many cells/ml. transplantation centers do HTLV screening in all donor-recipients when possible. In this case, results of the donor HTLV testing are received Discussion after surgery, informing of reactivity for HTLV Similar cases of HAM/TSP shortly after trans- antibodies using a commercial enzyme immuno- plantation have been reported in the literature assay. No organs other than the two kidneys were (Table 1).13–25 Myelopathy was originally reported transplanted from the same donor. in a heart transplant recipient in France following HTLV-1 acquisition from contaminated blood Positivity for HTLV-1 in the first kidney recipi- transfusions during the surgery.13 In Spain, two ent was confirmed thereafter using immunoblot. kidney recipients and one liver transplant recipi- Soon after this became known she was informed ent who received organs from a single deceased and antiretroviral therapy with zidovudine, lami- HTLV-1 donor developed HAM/TSP within vudine plus raltegravir was introduced within 2 years.16 More recently, in the USA two kidney the first week following transplantation. transplant recipients from separate infected Antiretrovirals were used for at least 18 months. donors developed HAM/TSP.19,20 In a retrospective interview of the deceased donor’s relatives, it became apparent that he In Japan, where HTLV-1 is endemic, cases of HAM/ most likely had acquired HTLV-1 from a TSP have been reported following either kidney or Brazilian heterosexual partner. liver transplants.14,15,17,22–24 More interesting, how- ever, is the diagnosis of ATLL shortly following solid Eight months later the recipient developed diffi- organ transplants, mostly among native Japanese culty walking, along with unsteady gait, followed recipients already infected with H ­TLV–1.28,29 by progressive lower extremity weakness, all sug- Similar cases have been reported in other places.26,27 gestive of HAM/TSP.12 Her HTLV-1 proviral This is somewhat unique since most post-transplant load had been high in sequential longitudinal lymphoproliferative disorders are of B lymphocytes samples collected soon after transplantation, in and linked to Epstein–Barr virus infection. the range of 320–350 HTLV-1 DNA copies per Anecdotally, in Germany, transplanted kidneys and 10,000 peripheral blood mononuclear cells/ml. At a liver resulted in primary cutaneous T-cell lym- the time of presentation of the initial neurological phoma in at least two patients infected from a single symptoms, the proviral load in the cerebrospinal HTLV-1 donor.30 Table 1 summarizes the major fluid was also very high (2340 HTLV-1 DNA features of ATLL cases reported so far following copies per 10,000 mononuclear cells/ml). solid organ transplantation. 2 journals.sagepub.com/home/tai L Roc, C de Mendoza et al. Table 1. Reports of HTLV-1 associated diseases in solid organ transplant recipients.HAM/TSP developed in recipients negative for HTLV-1 who received organs from infected donors or, more occasionally, contaminated blood transfusions during surgery. In contrast, most recipients who developed ATLL were HTLV-1 before transplantation and immunosuppression. Country Year Age (years) Gender Organ Interval Reference HTLV-1 associated myelopathy/tropical spastic paraparesis (HAM/TSP) 1 France 1990 41 Male Heart 5 months Gout et al.13 2 Japan 1992 32 Male Kidney 11 months Kuroda et al.14 3 Japan 2000 50 Male Kidney 4 years Nakatsuji et al.15 4 Spain 2003 44 Female Liver 18 months Toro et al.16 5 Spain 2003 54 Female Kidney <3 months Toro et al.16 6 Spain 2003 57 Male Kidney 20 months Toro et al.16 7 Japan 2008 58 Male Liver 20 months Soyama et al.17 8 Japan 2010 51 Male Kidney 10 months Inose et al.18 9 USA 2014 56 Male Kidney 5 months Ramanan et al.19 10 USA 2015 59 Female Kidney 8 years Younger20 11 Germany 2016 46 Female Kidney 4 years Gövert et al.21 12 Japan 2015 38 Female Kidney 2 months Nagamine et al.22 13 Japan 2016 42 Female Kidney 3 years Tajima et al.23 14 Japan 2016 65 Male Kidney 8 months Tajima et al.23 15 Japan 2016 ? ? Liver 15 months Yoshizumi et al.24 16 Japan 2016 ? ? Liver 46 months Yoshizumi et al.24 17 Ecuador 2016 40 Male Kidney 2 years Montesdeoca et al.25 18 Spain 2016 54 Female Kidney 8 months Current case Adult T-cell leukemia/lymphoma (ATLL) 1 Canada 1989 58 Female Kidney 11 years Zanke et al.26 2 UK 1995 ? Male Kidney ? Jenks et al.27 3 Japan 2001 32 Male Kidney 5 months Hoshida et al.28 4 Japan 2001 32 Male Kidney 11 months Hoshida et al.28 5 Japan 2001 43 Male Kidney 4 years Hoshida et al.28 6 Japan 2001 56 Male Kidney 18 months Hoshida et al.28 7 Japan 2001 47 Female Kidney <3 months Hoshida et al.28 8 Japan 2006 39 Female Liver 6 months Kawano et al.29 9 Japan 2006 67 Male Liver 9 months Kawano et al.29 10 Japan 2006 45 Male Liver 25 months Kawano et al.29 (Continued) journals.sagepub.com/home/tai 3 Therapeutic Advances in Infectious Disease 6 Table 1. (Continued) Country Year Age (years) Gender Organ Interval Reference 11 Germany 2008 59 Male Liver 2 years Glowacka et al.30 12 Germany 2009 28 Male Kidney 3 years Glowacka et al.30 13 Japan 2016 39 Female Liver 181 days Yoshizumi et al.24 14 Japan 2016 45 Male Liver 291 days Yoshizumi et al.24 15 Japan 2016 67 Male Liver 257 days Yoshizumi et al.24 16 Japan 2016 48 Male Liver 823 days Yoshizumi et al.24 17 Japan 2016 59 Female Liver 1315 days Yoshizumi et al.24 These findings call into question the current view that persons infected with HTLV be counseled that anti-HTLV screening of donated organs is not ‘not to donate blood, semen, body organs or other needed or is only recommended when there is sus- tissues’.35 Nevertheless, in 2009 the recommenda- picion. This opinion is based on the assumption tion for universal HTLV screening in deceased that HTLV-1 associated diseases will develop only organ donors was dropped in the USA because of in a small proportion of carriers and that progres- the perception of low HTLV-1 prevalence and low sion to disease is slow compared with the average positive predictive value of serologic screening lifespan of humans and therefore poses no major tests.36 Alongside this recommendation, most threats to public health.31 We postulate that in the international transplant society guidelines cur- transplant setting the very high risk of transmission rently do not provide any advice on HTLV-1 and the high rate along with the rapidity of devel- screening and use of donated organs. oping HTLV-1 disease is the result of immuno- suppressive therapy. Interestingly, it seems to be a High rates of HTLV-1 have been found in spe- divergent predominant clinical manifestation cific groups in nonendemic regions of North depending on whether the allograft derives from an America37,38 and Europe,39 and decades of migra- HTLV-1 infected donor or it is the recipient who tion/immigration and tourism/traveling have actually carries the virus (Figure 1). When the altered the demographics of many Western coun- recipient is already infected, transplantation might tries. For example, the ongoing refugee migration lead more frequently to ATLL, whereas when from the Middle East and Africa would rapidly HTLV-1 is acquired from the donor, the recipi- change the prevalence of HTLV-1 in many ent’s greater risk is for HAM/TSP. European countries. For a while this has been the case with Latin Americans in Spain, given the In a recent large retrospective study conducted in large influx of immigration facilitated by strong Japan including over 180 kidney transplants that cultural and ancestral links.8 Since 1988 there has involved HTLV-1 either in donors or recipients, been a national register of HTLV-1 cases in 4 out of 10 HTLV-negative recipients that Spain. As of December 2018, a total of 369 cases became infected following transplantation of a have been reported. Most cases are concentrated positive donor developed HAM/TSP within around the largest urban areas (Madrid and 4 years. In contrast, only 1 of 59 HTLV-1 positive Barcelona), where the greatest immigrant popula- recipients developed complications, with the only tions are living. However, HTLV-1 infected per- exception being a patient who developed both sons have been identified across the whole TSP/HAM and ATLL at 8 and 10 years, respec- Spanish geography. tively, after transplantation.32 In response to the worldwide evolving foci of More than 35 years after the discovery of HTLV-1 infections and the very poor prognosis HTLV-1,33 donor/recipient screening for the virus of post-transplant TSP and ATLL, there are remains sporadic or nonexistent in most coun- urgent calls for broader HTLV-1 screening of live tries.34 In 1993, the American CDC recommended and –more difficult – deceased organ donors. 4 journals.sagepub.com/home/tai L Roc, C de Mendoza et al. Figure 1. Model for HTLV-1 disease development in transplant recipients. Organ procurement organizations and transplant organ transplant HTLV-1 screening. In the mean- programs should determine local prevalence to time, some transplant centers around the world, guide HTLV-1 screening efforts.37 Targeted including a few in Spain, have already imple- screening of potential high-risk living (and mented ‘rapid’ (or ‘urgent’) HTLV-1 testing of all deceased) donors for HTLV-1 has been recom- deceased organ donors. In parallel, diagnostic mended by some experts.19 Suggestions have also companies should improve the specificity of been put forward for national or international HTLV-1 screening tests and design rapid tools registries of all HTLV-1 affected transplants.10 (i.e. point-of-care, or PIC, tests) to minimize Alerted to the dangers of rapid-onset TSP follow- unwanted organ discharge. ing HTLV-1 infected organ transplants, Japan begun in 2014 HTLV-1 screening of all kidney Acknowledgements donations. Similarly, the UK issued new trans- We would like to thank all members of the HTLV plantation guidance on HTLV-1 screening of Spanish Study Group. cadaveric solid organs in 2011. Finally, the Global Virus Network has recently called for more sys- C. Rodríguez, M. Vera and J. del Romero (Centro tematic HTLV-1 screening before solid organ Sanitario Sandoval, Madrid); G. Marcaida and transplantation everywhere.31 M.D. Ocete (Hospital General Universitario, Valencia); E. Caballero and I. Molina (Hospital It has been highlighted that ‘whereas not screening Vall d’Hebró, Barcelona); A. Aguilera, J.J. donors . . . for HIV infection would be considered Rodríguez-Calviño, D. Navarro, C. Rivero and unethical, the same is not the case for HTLV-1, M.D. Vilariño (Hospital Conxo-CHUS, another human retrovirus, where risk assessments Santiago); R. Benito, S. Algarate and J. Gil are made based on the predicted prevalence of (Hospital Clínico Universitario Lozano Blesa, cases among donors, the probable risk of transmis- Zaragoza); R. Ortiz de Lejarazu and S. Rojo sion, and the subsequent likelihood of disease’.10 (Hospital Clínico Universitario, Valladolid); J.M. Yet, those risk estimates are based on inadequate Eirós and A. San Miguel (Hospital Rio Hortega, national epidemiology, ignoring changing demo- Valladolid); C. Manzardo and J.M. Miró graphics in many countries,1,2 and a poor under- (Hospital Clínic-IDIBAPS, Barcelona); J. García standing of the transplant-acquired HTLV-1 and I. Paz (Hospital Cristal-Piñor, Orense); E. disease risk.9,10 The screening costs for HTLV-1 Poveda (INIBIC-Complejo Hospitalario are small in comparison with the cost of post- Universitario, A Coruña); E. Calderón (Hospital transplant illness and/or death associated with Virgen del Rocío and CIBERESP, Sevilla); D. TSP or ATLL following HTLV-1 infection.40 For Escudero (Hospital Germans Trias i Pujol, all these reasons, the American and European Barcelona); M. Trigo, J. Diz and M. García- CDCs, along with other health agencies, should Campello (Complejo Hospitalario, Pontevedra); urgently update their policy recommendations on M. Rodríguez-Iglesias (Hospital Universitario, journals.sagepub.com/home/tai 5 Therapeutic Advances in Infectious Disease 6 Puerto Real); A. Hernández-Betancor and A.M. Conflict of interest statement Martín (Hospital Insular Hospital Universitario, The author(s) declare that there is no conflict of Las Palmas de Gran Canaria); J.M. Ramos and interest. A. Gimeno (Hospital Universitario, Alicante); F. Gutiérrez, J.C. Rodríguez and V. Sánchez Funding (Hospital General, Elche); C. Gómez-Hernando The author(s) received no financial support for (Complejo Hospitalario Virgen de la Salud, the research, authorship and/or publication of Toledo); G. Cilla and E. Pérez-Trallero (Hospital this article. Donostia, San Sebastián); J. López-Aldeguer (Hospital La Fe, Valencia); L. Fernández-Pereira Ethical approval (Hospital San Pedro de Alcántara, Cáceres); J. This study was approved by the Puerta de Hierro Niubó (Ciudad Sanitaria de Bellvitge, Barcelona); Research Institute, where the coordinator of the M. Hernández, A.M. López-Lirola and J.L. HTLV Spanish study group is based. Gómez-Sirvent (Hospital Universitario La Laguna, Tenerife); L. Force (Hospital General, Informed consent Mataró); C. Cifuentes (Hospital Son Llátzer, Data recorded were collected anonymously Palma de Mallorca); S. Pérez and L. Morano through the national registry. (Hospital do Meixoeiro, Vigo); C. Raya (Hospital del Bierzo, Ponferrada); A. González-Praetorius ORCID iD (Hospital Universitario, Guadalajara); J.L. Pérez Vicente Soriano https://orcid.org/0000-0002- and M. Peñaranda (Hospital Son Espases, 4624-5199 Mallorca); S. Hernáez-Crespo (Hospital de Basurto, Bilbao); J.M. 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