Norovirus infection in primary immune deficiency

Reviews in Medical Virology

Volumn 27, Issue 3, 2017, Pages

  Brown, Li An K ^a   Clark, Ian ^a   Brown, Julianne R ^b   Breuer, Judith ^c   Lowe, David M ^c  

^a ROYAL FREE LONDON NHS FOUNDATION TRUST   (United Kingdom)

^b GREAT ORMOND STREET HOSPITAL   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

immunodeficiency; norovirus; primary immune deficiency

Indexed keywords

IMMUNOGLOBULIN; IMMUNOSUPPRESSIVE AGENT; NITAZOXANIDE; RIBAVIRIN;

ANTIVIRAL THERAPY; BREAST MILK; CHRONIC DISEASE; COMMON VARIABLE IMMUNODEFICIENCY; ENTEROPATHY; HUMAN; IMMUNE DEFICIENCY; IMMUNE RESPONSE; IMMUNOCOMPROMISED PATIENT; NONHUMAN; NOROVIRUS; NOROVIRUS INFECTION; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; VIRAL CLEARANCE;

EID: 85014618413     PISSN: 10529276     EISSN: 10991654     Source Type: Journal    
DOI: 10.1002/rmv.1926     Document Type: Review

References (107)

1. Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA. Virus Taxonomy: VIIIth Report of the International Committee on Taxonomy of Viruses. San Diego: Elsevier / Academic Press; 2005.
2. Robilotti E, Deresinski S, Pinsky BA. Norovirus. Clin Microbiol Rev. 2015;28(1):134-164.
3. Hall AJ, Lopman BA, Payne DC, et al. Norovirus disease in the United States. Emerg Infect Dis. 2013;19(8):1198-1205.
4. Zheng DP, Ando T, Fankhauser RL, Beard RS, Glass RI, Monroe SS. Norovirus classification and proposed strain nomenclature. Virology. 2006;346(2):312-323.
5. Lindesmith LC, Donaldson EF, Lobue AD, et al. Mechanisms of GII.4 norovirus persistence in human populations. PLoS Med. 2008;5(2):e31
6. Arias A, Emmott E, Vashist S, Goodfellow I. Progress towards the prevention and treatment of norovirus infections. Future Microbiol. 2013;8(11):1475-1487.
7. Tseng CY, Chen CH, Su SC, et al. Characteristics of norovirus gastroenteritis outbreaks in a psychiatric centre. Epidemiol Infect. 2011;139(02):275-285.
8. Bok K, Green KY. Norovirus gastroenteritis in immunocompromised patients. N Engl J Med. 2012;367(22):2126-2132.
9. Green KY. Norovirus infection in immunocompromised hosts. Clin Microbiol Infect. 2014;20(8):717-723.
10. Wobus CE, Thackray LB, Virgin HW. Murine norovirus: a model system to study norovirus biology and pathogenesis. J Virol. 2006;80(11):5104-5112.
11. Bok K, Parra GI, Mitra T, et al. Chimpanzees as an animal model for human norovirus infection and vaccine development. Proc Natl Acad Sci. 2011;108(1):325-330.
12. Cheetham S, Souza M, Meulia T, Grimes S, Han MG, Saif LJ. Pathogenesis of a genogroup II human norovirus in gnotobiotic pigs. J Virol. 2006;80(21):10372-10381.
13. Souza M, Azevedo MS, Jung K, Cheetham S, Saif LJ. Pathogenesis and immune responses in gnotobiotic calves after infection with the genogroup II. 4-HS66 strain of human norovirus. J Virol. 2008;82(4):1777-1786.
14. Taube S, Kolawole AO, Hohne M, et al. A mouse model for human norovirus. MBio. 2013;4(4):e00450-13.
15. Jones MK, Watanabe M, Zhu S, et al. Enteric bacteria promote human and mouse norovirus infection of B cells. Science. 2014;346(6210):755-759.
16. Jones MK, Grau KR, Costantini V, et al. Human norovirus culture in B cells. Nat Protoc. 2015;10(12):1939-1947.
17. Thorne L, Arias A, Goodfellow I. Advances toward a norovirus antiviral: from classical inhibitors to lethal mutagenesis. J Infect Dis. 2016;213(suppl 1):S27-S31.
18. Newman KL, Leon JS. Norovirus immunology: of mice and mechanisms. Eur J Immunol. 2015;45(10):2742-2757.
19. Green KY. Editorial commentary: noroviruses and B cells. Clin Infect Dis. 2016;62(9):1139-1140.
20. Newman KL, Moe CL, Kirby AE, Flanders WD, Parkos CA, Leon JS. Norovirus in symptomatic and asymptomatic individuals: cytokines and viral shedding. Clin Exp Immunol. 2016. doi:10.1111/cei.12772
21. Ko G, Jiang ZD, Okhuysen PC, DuPont HL. Fecal cytokines and markers of intestinal inflammation in international travelers with diarrhea due to noroviruses. J Med Virol. 2006;78(6):825-828.
22. Souza M, Cheetham SM, Azevedo MS, Costantini V, Saif LJ. Cytokine and antibody responses in gnotobiotic pigs after infection with human norovirus genogroup II.4 (HS66 strain). J Virol. 2007;81(17):9183-9192.
23. Chachu KA, Strong DW, LoBue AD, Wobus CE, Baric RS, Virgin HW 4th. Antibody is critical for the clearance of murine norovirus infection. J Virol. 2008;82(13):6610-6617.
24. Brown JR, Gilmour K, Breuer J. Norovirus infections occur in B-cell–deficient patients. Clin Infect Dis. 2016;62(9):1136-1138.
25. Tomov VT, Osborne LC, Dolfi DV, et al. Persistent enteric murine norovirus infection is associated with functionally suboptimal virus-specific CD8 T cell responses. J Virol. 2013;87(12):7015-7031.
26. Chachu KA, LoBue AD, Strong DW, Baric RS, Virgin HW. Immune mechanisms responsible for vaccination against and clearance of mucosal and lymphatic norovirus infection. PLoS Pathog. 2008;4(12):e1000236.
27. Zhu S, Regev D, Watanabe M, et al. Identification of immune and viral correlates of norovirus protective immunity through comparative study of intra-cluster norovirus strains. PLoS Pathog. 2013;9(9): e1003592.
28. Changotra H, Jia Y, Moore TN, et al. Type I and type II interferons inhibit the translation of murine norovirus proteins. J Virol. 2009;83(11):5683-5692.
29. Jung K, Wang Q, Kim Y, et al. The effects of simvastatin or interferon-alpha on infectivity of human norovirus using a gnotobiotic pig model for the study of antivirals. PLoS One. 2012;7(7): e41619.
30. Thackray LB, Duan E, Lazear HM, et al. Critical role for interferon regulatory factor 3 (IRF-3) and IRF-7 in type I interferon-mediated control of murine norovirus replication. J Virol. 2012;86(24):13515-13523.
31. Baldridge MT, Nice TJ, McCune BT, et al. Commensal microbes and interferon-lambda determine persistence of enteric murine norovirus infection. Science. 2015;347(6219):266-269.
32. Nice TJ, Baldridge MT, McCune BT, et al. Interferon-lambda cures persistent murine norovirus infection in the absence of adaptive immunity. Science. 2015;347(6219):269-273.
33. Di Sabatino A, Lenti MV, Giuffrida P, Vanoli A, Corazza GR. New insights into immune mechanisms underlying autoimmune diseases of the gastrointestinal tract. Autoimmun Rev. 2015;14(12):1161-1169.
34. Troeger H, Loddenkemper C, Schneider T, et al. Structural and functional changes of the duodenum in human norovirus infection. Gut. 2009;58(8):1070-1077.
35. Woodward JM, Gkrania-Klotsas E, Cordero-Ng AY, et al. The role of chronic norovirus infection in the enteropathy associated with common variable immunodeficiency. Am J Gastroenterol. 2015;110(2):320-327.
36. McAllister CS, Lakhdari O, Pineton de Chambrun G, et al. TLR3, TRIF, and caspase 8 determine double-stranded RNA-induced epithelial cell death and survival in vivo. J Immunol. 2013;190(1):418-427.
37. Abadie V, Jabri B. IL-15: a central regulator of celiac disease immunopathology. Immunol Rev. 2014;260(1):221-234.
38. Al-Herz W, Bousfiha A, Casanova JL, et al. Primary immunodeficiency diseases: an update on the classification from the International Union of Immunological Societies Expert Committee for primary immunodeficiency. Front Immunol. 2014;5:162.
39. Tam JS, Routes JM. Common variable immunodeficiency. Am J Rhinol Allergy. 2013;27(4):260-265.
40. Agarwal S, Cunningham-Rundles C. Autoimmunity in common variable immunodeficiency. Curr Allergy Asthma Rep. 2009;9(5):347-352.
41. Angarone M, Ison MG. Diarrhea in solid organ transplant recipients. Curr Opin Infect Dis. 2015;28(4):308-316.
42. Roos-Weil D, Ambert-Balay K, Lanternier F, et al. Impact of norovirus/sapovirus-related diarrhea in renal transplant recipients hospitalized for diarrhea. Transplantation. 2011;92(1):61-69.
43. Kaufman SS, Chatterjee NK, Fuschino ME, et al. Calicivirus enteritis in an intestinal transplant recipient. Am J Transplant. 2003;3(6):764-768.
44. Kaufman SS, Chatterjee NK, Fuschino ME, et al. Characteristics of human calicivirus enteritis in intestinal transplant recipients. J Pediatr Gastroenterol Nutr. 2005;40(3):328-333.
45. Schorn R, Hohne M, Meerbach A, et al. Chronic norovirus infection after kidney transplantation: molecular evidence for immune-driven viral evolution. Clin Infect Dis. 2010;51(3):307-314.
46. Ye X, Van JN, Munoz FM, et al. Noroviruses as a cause of diarrhea in immunocompromised pediatric hematopoietic stem cell and solid organ transplant recipients. Am J Transplant. 2015;15(7):1874-1881.
47. Westhoff TH, Vergoulidou M, Loddenkemper C, et al. Chronic norovirus infection in renal transplant recipients. Nephrol Dial Transplant. 2009;24(3):1051-1053.
48. Florescu DF, Hill LA, McCartan MA, Grant W. Two cases of Norwalk virus enteritis following small bowel transplantation treated with oral human serum immunoglobulin. Pediatr Transplant. 2008;12(3):372-375.
49. Lee BE, Pang XL, Robinson JL, Bigam D, Monroe SS, Preiksaitis JK. Chronic norovirus and adenovirus infection in a solid organ transplant recipient. Pediatr Infect Dis J. 2008;27(4):360-362.
50. Echenique IA, Stosor V, Gallon L, Kaufman D, Qi C, Zembower TR. Prolonged norovirus infection after pancreas transplantation: a case report and review of chronic norovirus. Transpl Infect Dis. 2016;18:98-104. doi:10.1111/tid.12472
51. Chagla Z, Quirt J, Woodward K, Neary J, Rutherford C. Chronic norovirus infection in a transplant patient successfully treated with enterally administered immune globulin. J Clin Virol. 2013;58(1):306-308.
52. Ebdrup L, Bottiger B, Molgaard H, Laursen AL. Devastating diarrhoea in a heart-transplanted patient. J Clin Virol. 2011;50(4):263-265.
53. Boillat Blanco N, Kuonen R, Bellini C, et al. Chronic norovirus gastroenteritis in a double hematopoietic stem cell and lung transplant recipient. Transpl Infect Dis. 2011;13(2):213-215.
54. Gairard-Dory AC, Degot T, Hirschi S, et al. Clinical usefulness of oral immunoglobulins in lung transplant recipients with norovirus gastroenteritis: a case series. Transplant Proc. 2014;46(10):3603-3605.
55. Roddie C, Paul JP, Benjamin R, et al. Allogeneic hematopoietic stem cell transplantation and norovirus gastroenteritis: a previously unrecognized cause of morbidity. Clin Infect Dis. 2009;49(7):1061-1068.
56. Saif MA, Bonney DK, Bigger B, et al. Chronic norovirus infection in pediatric hematopoietic stem cell transplant recipients: a cause of prolonged intestinal failure requiring intensive nutritional support. Pediatr Transplant. 2011;15(5):505-509.
57. Doshi M, Woodwell S, Kelleher K, Mangan K, Axelrod P. An outbreak of norovirus infection in a bone marrow transplant unit. Am J Infect Control. 2013;41(9):820-823.
58. Schwartz S, Vergoulidou M, Schreier E, et al. Norovirus gastroenteritis causes severe and lethal complications after chemotherapy and hematopoietic stem cell transplantation. Blood. 2011;117(22):5850-5856.
59. Morris J, Morris C. Nitazoxanide is effective therapy for norovirus gastroenteritis after chemotherapy and hematopoietic stem cell transplantation (HSCT). Biol Blood Marrow Transplant. 2015;21(2):S255-S256.
60. Simon A, Schildgen O, Maria Eis-Hubinger A, et al. Norovirus outbreak in a pediatric oncology unit. Scand J Gastroenterol. 2006;41(6):693-699.
61. Ludwig A, Adams O, Laws HJ, Schroten H, Tenenbaum T. Quantitative detection of norovirus excretion in pediatric patients with cancer and prolonged gastroenteritis and shedding of norovirus. J Med Virol. 2008;80(8):1461-1467.
62. Brown W, Morris CL. Nitazoxanide is effective therapy for norovirus gastroenteritis after chemotherapy and hematopoietic stem cell transplantation (HSCT). Blood. 2013;122(21):4581-4581.
63. Capizzi T, Makari-Judson G, Steingart R, Mertens WC. Chronic diarrhea associated with persistent norovirus excretion in patients with chronic lymphocytic leukemia: report of two cases. BMC Infect Dis. 2011;11(1):131.
64. Armbrust S, Kramer A, Olbertz D, Zimmermann K, Fusch C. Norovirus infections in preterm infants: wide variety of clinical courses. BMC Res Notes. 2009;2(1):96.
65. Wingfield T, Gallimore CI, Xerry J, et al. Chronic norovirus infection in an HIV-positive patient with persistent diarrhoea: a novel cause. J Clin Virol. 2010;49(3):219-222.
66. Frange P, Touzot F, Debre M, et al. Prevalence and clinical impact of norovirus fecal shedding in children with inherited immune deficiencies. J Infect Dis. 2012;206(8):1269-1274.
67. Duraisingham SS, Manson A, Grigoriadou S, Buckland M, Tong CY, Longhurst HJ. Immune deficiency: changing spectrum of pathogens. Clin Exp Immunol. 2015;181(2):267-274.
68. van de Ven A, Douma JW, Rademaker C, et al. Case report-Pleconaril-resistant chronic parechovirus-associated enteropathy in agammaglobulinaemia. Antivir Ther. 2011;16(4):611.
69. Gallimore CI, Lewis D, Taylor C, Cant A, Gennery A, Gray JJ. Chronic excretion of a norovirus in a child with cartilage hair hypoplasia (CHH). J Clin Virol. 2004;30(2):196-204.
70. Xerry J, Gallimore CI, Cubitt D, Gray JJ. Tracking environmental norovirus contamination in a pediatric primary immunodeficiency unit. J Clin Microbiol. 2010;48(7):2552-2556.
71. Teahon K, Webster AD, Price AB, Weston J, Bjarnason I. Studies on the enteropathy associated with primary hypogammaglobulinaemia. Gut. 1994;35(9):1244-1249.
72. Malamut G, Verkarre V, Suarez F, et al. The enteropathy associated with common variable immunodeficiency: the delineated frontiers with celiac disease. Am J Gastroenterol. 2010;105(10):2262-2275.
73. Khodadad A, Aghamohammadi A, Parvaneh N, et al. Gastrointestinal manifestations in patients with common variable immunodeficiency. Dig Dis Sci. 2007;52(11):2977-2983.
74. Daniels JA, Lederman HM, Maitra A, Montgomery EA. Gastrointestinal tract pathology in patients with common variable immunodeficiency (CVID): a clinicopathologic study and review. Am J Surg Pathol. 2007;31(12):1800-1812.
75. Chua I, Standish R, Lear S, et al. Anti-tumour necrosis factor-α therapy for severe enteropathy in patients with common variable immunodeficiency (CVID). Clin Exp Immunol. 2007;150(2):306-311.
76. Boshuizen JA, Reimerink JH, Korteland-van Male AM, et al. Changes in small intestinal homeostasis, morphology, and gene expression during rotavirus infection of infant mice. J Virol. 2003;77(24):13005-13016.
77. Jiang X, Huang P, Zhong W, et al. Human milk contains elements that block binding of noroviruses to human histo—Blood group antigens in saliva. J Infect Dis. 2004;190(10):1850-1859.
78. Nilsson M, Hedlund KO, Thorhagen M, et al. Evolution of human calicivirus RNA in vivo: accumulation of mutations in the protruding P2 domain of the capsid leads to structural changes and possibly a new phenotype. J Virol. 2003;77(24):13117-13124.
79. Florescu DF, Hermsen ED, Kwon JY, et al. Is there a role for oral human immunoglobulin in the treatment for norovirus enteritis in immunocompromised patients? Pediatr Transplant. 2011;15(7):718-721.
80. Rossignol JF. Nitazoxanide: a first-in-class broad-spectrum antiviral agent. Antiviral Res. 2014;110:94-103.
81. Rossignol JF, El-Gohary YM. Nitazoxanide in the treatment of viral gastroenteritis: A randomized double-blind placebo-controlled clinical trial. Aliment Pharmacol Ther. 2006;24(10):1423-1430.
82. Siddiq DM, Koo HL, Adachi JA, Viola GM. Norovirus gastroenteritis successfully treated with nitazoxanide. J Infect. 2011;63(5):394-397.
83. Chang K-O, George DW. Interferons and ribavirin effectively inhibit Norwalk virus replication in replicon-bearing cells. J Virol. 2007;81(22):12111-12118.
84. Andrassy J, Hoffmann VS, Rentsch M, et al. Is cytomegalovirus prophylaxis dispensable in patients receiving an mTOR inhibitor–based immunosuppression? A systematic review and meta-analysis. Transplantation. 2012;94(12):1208-1217.
85. Webster AC, Lee VW, Chapman JR, Craig JC. Target of rapamycin inhibitors (sirolimus and everolimus) for primary immunosuppression of kidney transplant recipients: a systematic review and meta-analysis of randomized trials. Transplantation. 2006;81(9):1234-1248.
86. Engelen MA, Gunia S, Stypmann J. Elimination of norovirus in a chronic carrier under immunosuppression after heart transplantation–effect of everolimus. Transpl Int. 2011;24(11):e102-e103.
87. Losonsky GA, Johnson JP, Winkelstein JA, Yolken R. Oral administration of human serum immunoglobulin in immunodeficient patients with viral gastroenteritis. A pharmacokinetic and functional analysis. J Clin Investig. 1985;76(6):2362
88. Kaufman SS, Green KY, Korba BE. Treatment of norovirus infections: moving antivirals from the bench to the bedside. Antiviral Res. 2014;105:80-91.
89. Jin Z, Tucker K, Lin X, et al. Biochemical evaluation of the inhibition properties of favipiravir and 2′-C-methyl-cytidine triphosphates against human and mouse norovirus RNA polymerases. Antimicrob Agents Chemother. 2015;59(12):7504-7516.
90. Rocha-Pereira J, Jochmans D, Dallmeier K, Leyssen P, Nascimento MS, Neyts J. Favipiravir (T-705) inhibits in vitro norovirus replication. Biochem Biophys Res Commun. 2012;424(4):777-780.
91. Arias A, Thorne L, Goodfellow I. Favipiravir elicits antiviral mutagenesis during virus replication in vivo. Elife. 2014;3:e03679.
92. Furuta Y, Gowen BB, Takahashi K, Shiraki K, Smee DF, Barnard DL. Favipiravir (T-705), a novel viral RNA polymerase inhibitor. Antiviral Res. 2013;100(2):446-454.
93. Rocha-Pereira J, Jochmans D, Dallmeier K, et al. Inhibition of norovirus replication by the nucleoside analogue 2′-C-methylcytidine. Biochem Biophys Res Commun. 2012;427(4):796-800.
94. Costantini VP, Whitaker T, Barclay L, et al. Antiviral activity of nucleoside analogues against norovirus. Antivir Ther. 2012;17(6):981.
95. Rocha-Pereira J, Jochmans D, Debing Y, Verbeken E, Nascimento MS, Neyts J. The viral polymerase inhibitor 2′-C-methylcytidine inhibits Norwalk virus replication and protects against norovirus-induced diarrhea and mortality in a mouse model. J Virol. 2013;87(21):11798-11805.
96. Kolawole AO, Rocha-Pereira J, Elftman MD, Neyts J, Wobus CE. Inhibition of human norovirus by a viral polymerase inhibitor in the B cell culture system and in the mouse model. Antiviral Res. 2016;132:46-49. doi:10.1016/j.antiviral.2016.05.011
97. Rocha-Pereira J, Jochmans D, Neyts J. Prophylactic treatment with the nucleoside analogue 2′-C-methylcytidine completely prevents transmission of norovirus. J Antimicrob Chemother. 2015;70:190-197. doi:10.1093/jac/dku363
98. Pierra C, Amador A, Benzaria S, et al. Synthesis and pharmacokinetics of valopicitabine (NM283), an efficient prodrug of the potent anti-HCV agent 2'-C-methylcytidine. J Med Chem. 2006;49(22):6614-6620.
99. Coats SJ, Garnier-Amblard EC, Amblard F, et al. Chutes and ladders in hepatitis C nucleoside drug development. Antiviral Res. 2014;102:119-147.
100. Manns MP, Foster GR, Rockstroh JK, Zeuzem S, Zoulim F, Houghton M. The way forward in HCV treatment—finding the right path. Nat Rev Drug Discov. 2007;6(12):991-1000.
101. Muir AJ, Arora S, Everson G, et al. A randomized phase 2b study of peginterferon lambda-1a for the treatment of chronic HCV infection. J Hepatol. 2014;61(6):1238-1246.
102. Zhang X-F, Tan M, Chhabra M, Dai Y-C, Meller J, Jiang X. Inhibition of histo-blood group antigen binding as a novel strategy to block norovirus infections. PLoS One. 2013;8(7): e69379.
103. Feng X, Jiang X. Library screen for inhibitors targeting norovirus binding to histo-blood group antigen receptors. Antimicrob Agents Chemother. 2007;51(1):324-331.
104. Lindesmith LC, Beltramello M, Donaldson EF, et al. Immunogenetic mechanisms driving norovirus GII.4 antigenic variation. PLoS Pathog. 2012;8(5):e1002705. doi:10.1371/journal.ppat.1002705
105. Lochridge VP, Jutila KL, Graff JW, Hardy ME. Epitopes in the P2 domain of norovirus VP1 recognized by monoclonal antibodies that block cell interactions. J Gen Virol. 2005;86(10):2799-2806.
106. Chen Z, Sosnovtsev SV, Bok K, et al. Development of Norwalk virus-specific monoclonal antibodies with therapeutic potential for the treatment of Norwalk virus gastroenteritis. J Virol. 2013;87(17):9547-9557.
107. Garaicoechea L, Aguilar A, Parra GI, et al. Llama nanoantibodies with therapeutic potential against human norovirus diarrhea. PLoS One. 2015;10(8):e0133665.