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Clearing Vaccine-Derived Poliovirus Infection Following Hematopoietic Stem Cell Transplantation: a Case Report and Review of Literature

  • Mohammadreza Shaghaghi
  • Mona Irannejad
  • Hassan Abolhassani
  • Shohreh Shahmahmoodi
  • Amir Ali Hamidieh
  • Saeed Soleyman-Jahi
  • Reza Yazdani
  • Gholamreza Azizi
  • Asghar Aghamohammadi
Original Article
  • 5 Downloads

Abstract

The use of oral poliovirus vaccine in a worldwide scale has led to a 99.9% decrease in annual incidence of wild-type poliomyelitis and the eradication of serotype 2 poliovirus. However, the emergence of vaccine-derived polioviruses (VDPVs) is endangering the eradication program. Patients with combined immunodeficiencies are at increased risk of both vaccine-associated poliomyelitis and prolonged asymptomatic infection with immunodeficiency-associated VDPVs (iVDPVs). Herein, we present a severe combined immunodeficiency patient with prolonged and asymptomatic iVDPV infection. He continued to shed poliovirus during immunoglobulin replacement therapy and cleared the infection following successful hematopoietic stem cell transplantation (HSCT). To explain the efficiency of HSCT in clearing the infection, we reviewed the literature for all reports of HSCT in iVDPV-excreting patients and discussed novel ideas about the role of different immune mechanisms, including cell-mediated interactions, in mounting immune responses against poliovirus infections. This study could provide further insights into the immune mechanisms contributing to the clearance of enteroviral infections.

Keywords

Hematopoietic stem cell transplantation poliomyelitis poliovirus vaccine primary immunodeficiency 

Notes

Acknowledgments

We thank Ahmad Nejati, Maryam Yousefi, Yaghoob Mollaie, and all the staff members of the Iran National Polio Laboratory and also CDC-Atlanta for performing thorough virologic studies.

This study was done at the Research Center for Immunodeficiencies, Tehran University of Medical Sciences, Tehran, Iran. The Iran National Polio Laboratory is supported by the Ministry of Health and Medical Education, the World Health Organization, and Tehran University of Medical Sciences.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Kew OM, Sutter RW, de Gourville EM, Dowdle WR, Pallansch MA. Vaccine-derived polioviruses and the endgame strategy for global polio eradication. Annu Rev Microbiol. 2005;59:587–635.  https://doi.org/10.1146/annurev.micro.58.030603.123625.CrossRefPubMedGoogle Scholar
  2. 2.
    Morales M, Tangermann RH, Wassilak SG. Progress toward polio eradication—worldwide, 2015-2016. MMWR Morb Mortal Wkly Rep. 2016;65(18):470–3.  https://doi.org/10.15585/mmwr.mm6518a4.CrossRefPubMedGoogle Scholar
  3. 3.
    Minor PD. The polio-eradication programme and issues of the end game. J Gen Virol. 2012;93(3):457–74.  https://doi.org/10.1099/vir.0.036988-0.CrossRefPubMedGoogle Scholar
  4. 4.
    Khetsuriani N, Prevots DR, Quick L, Elder ME, Pallansch M, Kew O, et al. Persistence of vaccine-derived polioviruses among immunodeficient persons with vaccine-associated paralytic poliomyelitis. J Infect Dis. 2003;188(12):1845–52.  https://doi.org/10.1086/379791.CrossRefPubMedGoogle Scholar
  5. 5.
    Minor P. Characteristics of poliovirus strains from long-term excretors with primary immunodeficiencies. Dev Biol (Basel). 2001;105:75–80.Google Scholar
  6. 6.
    Alexander JP Jr, Gary HE Jr, Pallansch MA. Duration of poliovirus excretion and its implications for acute flaccid paralysis surveillance: a review of the literature. J Infect Dis. 1997;175(Suppl 1):S176–82.CrossRefPubMedGoogle Scholar
  7. 7.
    Henderson DA, Witte JJ, Morris L, Langmuir AD. Paralytic disease associated with oral polio vaccines. JAMA. 1964;190:41–8.CrossRefPubMedGoogle Scholar
  8. 8.
    CDC. Update on vaccine-derived polioviruses—worldwide, April 2011-June 2012. MMWR Morb Mortal Wkly Rep. 2012;61:741–6.Google Scholar
  9. 9.
    Sutter RW, Prevots DR. Vaccine-associated paralytic poliomyelitis among immunodeficient persons. Infect Med. 1994;11(6):426–38.Google Scholar
  10. 10.
    MacLennan C, Dunn G, Huissoon AP, Kumararatne DS, Martin J, O’Leary P, et al. Failure to clear persistent vaccine-derived neurovirulent poliovirus infection in an immunodeficient man. Lancet. 2004;363(9420):1509–13.  https://doi.org/10.1016/s0140-6736(04)16150-3.CrossRefPubMedGoogle Scholar
  11. 11.
    Dunn G, Klapsa D, Wilton T, Stone L, Minor PD, Martin J. Twenty-eight years of poliovirus replication in an immunodeficient individual: impact on the Global Polio Eradication Initiative. PLoS Pathog. 2015;11(8):e1005114.  https://doi.org/10.1371/journal.ppat.1005114.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Tebbens RJD, Pallansch MA, Kew OM, Caceres VM, Jafari H, Cochi SL, et al. Risks of paralytic disease due to wild or vaccine-derived poliovirus after eradication. Risk Anal. 2006;26(6):1471–505.  https://doi.org/10.1111/j.1539-6924.2006.00827.x.CrossRefPubMedGoogle Scholar
  13. 13.
    Alexander JP, Ehresmann K, Seward J, Wax G, Harriman K, Fuller S, et al. Transmission of imported vaccine-derived poliovirus in an undervaccinated community in Minnesota. J Infect Dis. 2009;199(3):391–7.  https://doi.org/10.1086/596052.CrossRefPubMedGoogle Scholar
  14. 14.
    Robbins FC. Polio. Rochester: BOYE6; 1999.Google Scholar
  15. 15.
    Shaghaghi M, Shahmahmoodi S, Abolhassani H, Soleyman-Jahi S, Parvaneh L, Mahmoudi S, et al. Vaccine-derived polioviruses and children with primary immunodeficiency, Iran, 1995-2014. Emerg Infect Dis. 2016;22(10):1712–9.  https://doi.org/10.3201/eid2210.151071.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Shaghaghi M, Soleyman-Jahi S, Abolhassani H, Yazdani R, Azizi G, Rezaei N, et al. New insights into physiopathology of immunodeficiency-associated vaccine-derived poliovirus infection; systematic review of over 5 decades of data. Vaccine. 2018;36(13):1711–9.  https://doi.org/10.1016/j.vaccine.2018.02.059.CrossRefPubMedGoogle Scholar
  17. 17.
    New clinical diagnosis criteria for the ESID Registry. https://esid.org/Working-Parties/Registry/Diagnosis-criteria#. Accessed 12/28/2017.
  18. 18.
    Bousfiha A, Jeddane L, Al-Herz W, Ailal F, Casanova JL, Chatila T, et al. The 2015 IUIS phenotypic classification for primary immunodeficiencies. J Clin Immunol. 2015;35(8):727–38.  https://doi.org/10.1007/s10875-015-0198-5.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Aghamohammadi A, Mohammadinejad P, Abolhassani H, Mirminachi B, Movahedi M, Gharagozlou M, et al. Primary immunodeficiency disorders in Iran: update and new insights from the third report of the national registry. J Clin Immunol. 2014;34(4):478–90.  https://doi.org/10.1007/s10875-014-0001-z.CrossRefPubMedGoogle Scholar
  20. 20.
    Abolhassani H, Chou J, Bainter W, Platt CD, Tavassoli M, Momen T, et al. Clinical, immunologic, and genetic spectrum of 696 patients with combined immunodeficiency. J Allergy Clin Immunol. 2018;141(4):1450–8.  https://doi.org/10.1016/j.jaci.2017.06.049.CrossRefPubMedGoogle Scholar
  21. 21.
    World Health Organization. Polio laboratory manual. 4th ed. WHO/IVB/04.10, 2004. http://www.who.int/iris/handle/10665/68762. Accessed 12/28/2017.
  22. 22.
    Aghamohammadi A, Abolhassani H, Kutukculer N, Wassilak SG, Pallansch MA, Kluglein S, et al. Patients with primary immunodeficiencies are a reservoir of poliovirus and a risk to polio eradication. Front Immunol. 2017;8:685.  https://doi.org/10.3389/fimmu.2017.00685.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Macklin G, Liao Y, Takane M, Dooling K, Gilmour S, Mach O, et al. Prolonged excretion of poliovirus among individuals with primary immunodeficiency disorder: an analysis of the World Health Organization Registry. Front Immunol. 2017;8:1103.  https://doi.org/10.3389/fimmu.2017.01103.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Jorba J, Diop OM, Iber J, Sutter RW, Wassilak SG, Burns CC. Update on vaccine-derived polioviruses—worldwide, January 2015-May 2016. MMWR Morb Mortal Wkly Rep. 2016;65(30):763–9.  https://doi.org/10.15585/mmwr.mm6530a3. CrossRefPubMedGoogle Scholar
  25. 25.
    Driss N, Mellouli F, Yahia AB, Touzi H, Barbouche MR, Triki H, et al. Sequential asymptomatic enterovirus infections in a patient with major histocompatibility complex class II primary immunodeficiency. J Clin Microbiol. 2014;52(9):3486–9.  https://doi.org/10.1128/JCM.01122-14. CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Schubert A, Böttcher S, Eis-Hübinger AM. Two cases of vaccine-derived poliovirus infection in an oncology ward. N Engl J Med. 2016;374(13):1296–8.  https://doi.org/10.1056/NEJMc1508104.CrossRefPubMedGoogle Scholar
  27. 27.
    de Koning C, Plantinga M, Besseling P, Boelens JJ, Nierkens S. Immune reconstitution after allogeneic hematopoietic cell transplantation in children. Biol Blood Marrow Transplant. 2016;22(2):195–206.  https://doi.org/10.1016/j.bbmt.2015.08.028.CrossRefPubMedGoogle Scholar
  28. 28.
    Oshrine BR, Li Y, Teachey DT, Heimall J, Barrett DM, Bunin N. Immunologic recovery in children after alternative donor allogeneic transplantation for hematologic malignancies: comparison of recipients of partially T cell-depleted peripheral blood stem cells and umbilical cord blood. Biol Blood Marrow Transplant. 2013;19(11):1581–9.  https://doi.org/10.1016/j.bbmt.2013.08.003.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Booth C, Lawson S, Veys P. The current role of T cell depletion in paediatric stem cell transplantation. Br J Haematol. 2013;162(2):177–90.  https://doi.org/10.1111/bjh.12400.CrossRefPubMedGoogle Scholar
  30. 30.
    Chen X, Hale GA, Barfield R, Benaim E, Leung WH, Knowles J, et al. Rapid immune reconstitution after a reduced-intensity conditioning regimen and a CD3-depleted haploidentical stem cell graft for paediatric refractory haematological malignancies. Br J Haematol. 2006;135(4):524–32.  https://doi.org/10.1111/j.1365-2141.2006.06330.x.CrossRefPubMedGoogle Scholar
  31. 31.
    Yazdani R, Sharifi M, Shirvan AS, Azizi G, Ganjalikhani-Hakemi M. Characteristics of innate lymphoid cells (ILCs) and their role in immunological disorders (an update). Cell Immunol. 2015;298(1–2):66–76.  https://doi.org/10.1016/j.cellimm.2015.09.006.CrossRefPubMedGoogle Scholar
  32. 32.
    Cherrier M. Innate lymphoid cells: new players of the mucosal immune response. Med Sci. 2014;30(3):280–8.  https://doi.org/10.1051/medsci/20143003016.
  33. 33.
    Colonna M, Jonjic S, Watzl C. Natural killer cells: fighting viruses and much more. Nat Immunol. 2011;12(2):107–10.  https://doi.org/10.1038/ni0211-107.CrossRefPubMedGoogle Scholar
  34. 34.
    Driss N, Ben-Mustapha I, Mellouli F, Ben Yahia A, Touzi H, Bejaoui M, et al. High susceptibility for enterovirus infection and virus excretion features in Tunisian patients with primary immunodeficiencies. Clin Vaccine Immunol. 2012;19(10):1684–9.  https://doi.org/10.1128/cvi.00293-12. CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Bae KW, Kim BE, Koh KN, Im HJ, Seo JJ. Factors influencing lymphocyte reconstitution after allogeneic hematopoietic stem cell transplantation in children. Korean J Hematol. 2012;47(1):44–52.  https://doi.org/10.5045/kjh.2012.47.1.44.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Rouzaire P, Mayol K, Viel S, Bienvenu J, Walzer T. Homeostasis of natural killer cells. Med Sci. 2012;28(4):403–8.  https://doi.org/10.1051/medsci/2012284018.
  37. 37.
    Yoon SR, Chung JW, Choi I. Development of natural killer cells from hematopoietic stem cells. Mol Cells. 2007;24(1):1–8.PubMedGoogle Scholar
  38. 38.
    Shaghaghi M, Parvaneh N, Ostad-Rahimi P, Fathi SM, Shahmahmoodi S, Abolhassani H, et al. Combined immunodeficiency presenting with vaccine-associated paralytic poliomyelitis: a case report and narrative review of literature. Immunol Investig. 2014;43(3):292–8.  https://doi.org/10.3109/08820139.2013.859156.CrossRefGoogle Scholar
  39. 39.
    Chiesa R, Gilmour K, Qasim W, Adams S, Worth AJ, Zhan H, et al. Omission of in vivo T-cell depletion promotes rapid expansion of naive CD4+ cord blood lymphocytes and restores adaptive immunity within 2 months after unrelated cord blood transplant. Br J Haematol. 2012;156(5):656–66.  https://doi.org/10.1111/j.1365-2141.2011.08994.x.CrossRefPubMedGoogle Scholar
  40. 40.
    Lopez C, Biggar WD, Park BH, Good RA. Nonparalytic poliovirus infections in patients with severe combined immunodeficiency disease. J Pediatr. 1974;84(4):497–502.CrossRefPubMedGoogle Scholar
  41. 41.
    MacCallum FO. Hypogammaglobulinaemia in the United Kingdom. VII. The role of humoral antibodies in protection against and recovery from bacterial and virus infections in hypogammaglobulinaemia. Spec Rep Ser Med Res Counc (G B). 1971;310:72–85.Google Scholar
  42. 42.
    Sutter RW, Suleiman AJ, Malankar P, Al-Khusaiby S, Mehta F, Clements GB, et al. Trial of a supplemental dose of four poliovirus vaccines. N Engl J Med. 2000;343(11):767–73.  https://doi.org/10.1056/NEJM200009143431103.CrossRefPubMedGoogle Scholar
  43. 43.
    Barbouche MR, Galal N, Ben-Mustapha I, Jeddane L, Mellouli F, Ailal F, et al. Primary immunodeficiencies in highly consanguineous North African populations. Ann N Y Acad Sci. 2011;1238:42–52.  https://doi.org/10.1111/j.1749-6632.2011.06260.x.CrossRefPubMedGoogle Scholar
  44. 44.
    Rezaei N, Pourpak Z, Aghamohammadi A, Farhoudi A, Movahedi M, Gharagozlou M, et al. Consanguinity in primary immunodeficiency disorders; the report from Iranian Primary Immunodeficiency Registry. Am J Reprod Immunol. 2006;56(2):145–51.  https://doi.org/10.1111/j.1600-0897.2006.00409.x.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Mohammadreza Shaghaghi
    • 1
    • 2
  • Mona Irannejad
    • 1
  • Hassan Abolhassani
    • 1
    • 3
  • Shohreh Shahmahmoodi
    • 4
    • 5
  • Amir Ali Hamidieh
    • 6
  • Saeed Soleyman-Jahi
    • 7
  • Reza Yazdani
    • 1
  • Gholamreza Azizi
    • 8
  • Asghar Aghamohammadi
    • 1
  1. 1.Research Center for Immunodeficiencies, Children’s Medical Center HospitalTehran University of Medical SciencesTehranIran
  2. 2.Network of Immunology in Infections, Malignancy and Autoimmunity (NIIMA)Universal Scientific Education and Research Network (USERN)TehranIran
  3. 3.Division of Clinical Immunology, Department of Laboratory MedicineKarolinska Institute at Karolinska University Hospital HuddingeStockholmSweden
  4. 4.Department of Virology, School of Public HealthTehran University of Medical SciencesTehranIran
  5. 5.Food Microbiology Research CenterTehran University of Medical SciencesTehranIran
  6. 6.Children’s Medical CenterTehran University of Medical SciencesTehranIran
  7. 7.Cancer Immunology Project (CIP)Universal Scientific Education and Research Network (USERN)TehranIran
  8. 8.Non-Communicable Diseases Research CenterAlborz University of Medical SciencesKarajIran

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