Tissue tropism, pathology and pathogenesis of enterovirus infection†

Journal of Pathology

Volumn 235, Issue 2, 2015, Pages 217-228

  Muehlenbachs, Atis ^a   Bhatnagar, Julu ^a   Zaki, Sherif R ^a  

^a NATIONAL CENTER FOR EMERGING AND ZOONOTIC INFECTIOUS DISEASES   (United States)

Author keywords

Autopsy; Enterovirus; Immunohistochemistry; Meningoencephalitis; Neonatal and congenital infections; PCR

Indexed keywords

VIRUS ANTIGEN;

ANTIGEN DETECTION; ARTICLE; ASYMPTOMATIC INFECTION; CENTRAL NERVOUS SYSTEM INFECTION; CONGENITAL INFECTION; DIAGNOSTIC PROCEDURE; ENTEROVIRUS INFECTION; HAND FOOT AND MOUTH DISEASE; HISTOPATHOLOGY; HUMAN; IMMUNOCOMPETENCE; IMMUNOHISTOCHEMISTRY; NONHUMAN; PATHOLOGIST; RESPIRATORY TRACT INFECTION; TISSUE FIXATION; TISSUE GROWTH; VIRUS MYOCARDITIS; VIRUS PATHOGENESIS; ANIMAL; BIOPSY; ENTEROVIRUS; ENTEROVIRUS INFECTIONS; GENETICS; GENOTYPE; HOST PATHOGEN INTERACTION; IMMUNOLOGY; MOLECULAR PATHOLOGY; PATHOGENICITY; PATHOLOGY; PREDICTIVE VALUE; PROCEDURES; RISK FACTOR; VIRAL TROPISM; VIROLOGY; VIRULENCE;

ANIMALS; BIOPSY; ENTEROVIRUS; ENTEROVIRUS INFECTIONS; GENOTYPE; HOST-PATHOGEN INTERACTIONS; HUMANS; PATHOLOGY, MOLECULAR; PREDICTIVE VALUE OF TESTS; RISK FACTORS; VIRAL TROPISM; VIROLOGY; VIRULENCE;

EID: 84917706134     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4438     Document Type: Article

References (99)

1. Pallansch MA, Oberste MS, Whitton JL. Enteroviruses: polioviruses, coxsackieviruses, echoviruses, and newer enteroviruses. In Fields Virol og y, 6th edn, Fields BN, Knipe DM, Howley PM (eds). Wolters Kluwer/Lippincott Williams & Wilkins Health: Philadelphia, PA, 2013; 490-530.
2. Oberste MS, Maher K, Pallansch MA. Evidence for frequent recombination within species human enterovirus B based on complete genomic sequences of all thirty-seven serotypes. J Virol 2004; 78: 855-867.
3. Oberste MS, Penaranda S, Maher K, et al. Complete genome sequences of all members of the species Human enterovirus A. J Gen Virol 2004; 85: 1597-607.
4. Bodian D. Emerging concept of poliomyelitis infection. Science 1955; 122: 105-108.
5. He Y, Ong KC, Gao Z, et al. Tonsillar crypt epithelium is an important extra-central nervous system site for viral replication in EV71 encephalomyelitis. Am J Pathol 2014; 184: 714-720.
6. Xatzipsalti M, Kyrana S, Tsolia M, et al. Rhinovirus viremia in children with respiratory infections. Am J Resp Crit Care Med 2005; 172: 1037-1040.
7. Cheng HY, Huang YC, Yen TY, et al. The correlation between the presence of viremia and clinical severity in patients with enterovirus 71 infection: a multi-center cohort study. BMC Infect Dis 2014; 14: 417.
8. Horstmann DM, Mc CR, Mascola AD. Viremia in human poliomyelitis. J Exp Med 1954; 99: 355-369.
9. McKinney RE Jr, Katz SL, Wilfert CM. Chronic enteroviral menin-goencephalitis in agammaglobulinemic patients. Rev Infect Dis 1987; 9: 334-356.
10. Servais S, Caers J, Warling O, et al. Enteroviral meningoencephalitis as complication of Rituximab therapy in a patient treated for diffuse large B cell lymphoma. Br J Haematol 2010; 150: 379-381.
11. Tan PL, Verneris MR, Charnas LR, et al. Outcome of CNS and pulmonary enteroviral infections after hematopoietic cell transplantation. Pediatr Blood Cancer 2005; 45: 74-75.
12. Lefterova MI, Rivetta C, George TI, et al. Severe hepatitis associated with an echovirus 18 infection in an immune-compromised adult. J Clin Microbiol 2013; 51: 684-687.
13. MacLennan C, Dunn G, Huissoon AP, et al. Failure to clear persistent vaccine-derived neurovirulent poliovirus infection in an immunode-fcient man. Lancet 2004; 363: 1509-1513.
14. Halsey NA, Pinto J, Espinosa-Rosales F, et al. Search for poliovirus carriers among people with primary immune defciency diseases in the United States, Mexico, Brazil, and the United Kingdom. Bull World Health Org 2004; 82: 3-8.
15. Julien J, Leparc-Goffart I, Lina B, et al. Postpolio syndrome: poliovirus persistence is involved in the pathogenesis. J Neurol 1999; 246: 472-476.
16. Archard LC, Khan MA, Soteriou BA, et al. Characterization of Coxsackie B virus RNA in myocardium from patients with dilated cardiomyopathy by nucleotide sequencing of reverse transcription-nested polymerase chain reaction products. Hum Pathol 1998; 29: 578-584.
17. Baboonian C, Treasure T. Meta-analysis of the association of enteroviruses with human heart disease. Heart 1997; 78: 539-543.
18. Melchers W, de Visser M, Jongen P, et al. The postpolio syndrome: no evidence for poliovirus persistence. Ann Neurol 1992; 32: 728-732.
19. de Leeuw N, Melchers WJ, Balk AH, et al. No evidence for persistent enterovirus infection in patients with end-stage idiopathic dilated cardiomyopathy. J Infect Dis 1998; 178: 256-259.
20. Arnesjo B, Eden T, Ihse I, et al. Enterovirus infections in acute pancreatitis-a possible etiological connection. Scand J Gastroenterol 1976; 11: 645-649.
21. D'Alessio DJ. A case-control study of group B Coxsackievirus immunoglobulin M antibody prevalence and HLA-DR antigens in newly diagnosed cases of insulin-dependent diabetes mellitus. Am J Epidemiol 1992; 135: 1331-1338.
22. Clements GB, Galbraith DN, Taylor KW. Coxsackie B virus infection and onset of childhood diabetes. Lancet 1995; 346: 221-223.
23. Bastis D, Simonet S, Patterson MA, et al. Identifcation of enteroviruses by indirect immunofuorescence using monoclonal antibodies. Clin Diagn Virol 1995; 3: 83-93.
24. Tsao KC, Huang CG, Huang YL, et al. Epidemiologic features and virus isolation of enteroviruses in Northern Taiwan during 2000-2008. J Virol Methods 2010; 165: 330-332.
25. Nielsen AC, Bottiger B, Midgley SE, et al. A novel enterovirus and parechovirus multiplex one-step real-time PCR-validation and clinical experience. J Virol Methods 2013; 193: 359-363.
26. Papadakis G, Chibo D, Druce J, et al. Detection and genotyping of enteroviruses in cerebrospinal fuid in patients in Victoria, Australia, 2007-2013. J Med Virol 2014; 86: 1609-1613.
27. Robinson CC, Willis M, Meagher A, et al. Impact of rapid poly-merase chain reaction results on management of pediatric patients with enteroviral meningitis. Pediatr Infect Dis J 2002; 21: 283-286.
28. Tsao LY, Lin CY, Yu YY, et al. Microchip, reverse transcription-polymerase chain reaction and culture methods to detect enterovirus infection in pediatric patients. Pediatr Int (Japan) 2006; 48: 5-10.
29. Zhang S, Wang J, Yan Q, et al. A one-step, triplex, real-time RT-PCR assay for the simultaneous detection of enterovirus 71, cox-sackie a16 and pan-enterovirus in a single tube. PloS One 2014; 9: e102724.
30. Nolte FS, Rogers BB, Tang YW, et al. Evaluation of a rapid and completely automated real-time reverse transcriptase PCR assay for diagnosis of enteroviral meningitis. J Clin Microbiol 2011; 49: 528-533.
31. Renaud C, Kuypers J, Ficken E, et al. Introduction of a novel pare-chovirus RT-PCR clinical test in a regional medical center. J Clin Vi ro l 2011; 51: 50-53.
32. Poritz MA, Blaschke AJ, Byington CL, et al. FilmArray, an automated nested multiplex PCR system for multi-pathogen detection: development and application to respiratory tract infection. PloS One 2011; 6: e26047.
33. Renaud C, Crowley J, Jerome KR, et al. Comparison of FilmAr-ray Respiratory Panel and laboratory-developed real-time reverse transcription-polymerase chain reaction assays for respiratory virus detection. Diagn Microbiol Infect Dis 2012; 74: 379-383.
34. Bhatnagar J, Blau DM, Shieh WJ, et al. Molecular detection and typing of dengue viruses from archived tissues of fatal cases by RT-PCR and sequencing: diagnostic and epidemiologic implications. Am J Trop Med Hyg 2012; 86: 335-340.
35. Bhatnagar J, Guarner J, Paddock CD, et al. Detection of West Nile virus in formalin-fxed, paraffn-embedded human tissues by RT-PCR: a useful adjunct to conventional tissue-based diagnostic methods. J Clin Virol 2007; 38: 106-111.
36. Guarner J, Bhatnagar J, Shieh WJ, et al. Histopathologic, immuno-histochemical, and polymerase chain reaction assays in the study of cases with fatal sporadic myocarditis. Hum Pathol 2007; 38: 1412-1419.
37. Mills AM, Guo FP, Copland AP, et al. A comparison of CMV detection in gastrointestinal mucosal biopsies using immunohistochem-istry and PCR performed on formalin-fxed, paraffn-embedded tissue. Am J Surg Pathol 2013; 37: 995-1000.
38. Sharma M, Mishra B, Vandana, et al. Ribonucleic acid extraction from archival formalin fxed paraffn embedded myocardial tissues for gene expression and pathogen detection. J Clin Lab Anal 2012; 26: 279-285.
39. Casas I, Palacios GF, Trallero G, et al. Molecular characterization of human enteroviruses in clinical samples: comparison between VP2, VP1, and RNA polymerase regions using RT nested PCR assays and direct sequencing of products. J Med Virol 2001; 65: 138-148.
40. Iturriza-Gomara M, Megson B, Gray J. Molecular detection and characterization of human enteroviruses directly from clinical samples using RT-PCR and DNA sequencing. J Med Virol 2006; 78: 243-253.
41. Minnaar RP, Koen G, de Haan K, et al. Evaluation of two (semi-) nested VP1-based PCRs for typing enteroviruses directly from cerebral spinal fuid samples. J Virol Methods 2012; 185: 228-233.
42. Thoelen I, Lemey P, Van Der Donck I, et al. Molecular typing and epidemiology of enteroviruses identifed from an outbreak of aseptic meningitis in Belgium during the summer of 2000. J Med Virol 2003; 70: 420-429.
43. Chan YF, AbuBaker S. Recombinant human enterovirus 71 in hand, foot and mouth disease patients. Emerg Infect Dis 2004; 10: 1468-1470.
44. Yoke-Fun C, AbuBakar S. Phylogenetic evidence for intertypic recombination in the emergence of human enterovirus 71 subgeno-types. BMC Microbiol 2006; 6: 74.
45. Chiang PS, Huang ML, Luo ST, et al. Comparing molecular methods for early detection and serotyping of enteroviruses in throat swabs of pediatric patients. PloS One 2012; 7: e48269.
46. Nix WA, Oberste MS, Pallansch MA. Sensitive, semi-nested PCR amplifcation of VP1 sequences for direct identifcation of all enterovirus serotypes from original clinical specimens. J Clin Microbiol 2006; 44: 2698-2704.
47. Rotbart HA. Enteroviral infections of the central nervous system. Clin Infect Dis 1995; 20: 971-981.
48. Finkelstein SD. Polioviruses. In Pathology of Infectious Diseases, Connor DH (ed.). Appleton & Lange: Stamford, CT, 1997.
49. Hsueh C, Jung SM, Shih SR, et al. Acute encephalomyelitis during an outbreak of enterovirus type 71 infection in Taiwan: report of an autopsy case with pathologic, immunofuorescence, and molecular studies. Mod Pathol 2000; 13: 1200-1205.
50. Jiang M, Wei D, Ou WL, et al. Autopsy fndings in children with hand, foot, and mouth disease. N Engl J Med 2012; 367: 91-92.
51. Chan LG, Parashar UD, Lye MS, et al. Deaths of children during an outbreakof hand, foot, and mouth disease in Sarawak, Malaysia: clinical and pathological characteristics of the disease. For the Outbreak Study Group. Clin Infect Dis 2000; 31: 678-683.
52. Shieh WJ, Jung SM, Hsueh C, et al. Pathologic studies of fatal cases in outbreak of hand, foot, and mouth disease, Taiwan. Emerg Infect Dis 2001; 7: 146-148.
53. Mendelsohn CL, Wimmer E, Racaniello VR. Cellular receptor for poliovirus: molecular cloning, nucleotide sequence, and expression of a new member of the immunoglobulin superfamily. Cell 1989; 56: 855-865.
54. Gromeier M, Solecki D, Patel DD, et al. Expression of the human poliovirus receptor/CD155 gene during development of the central nervous system: implications for the pathogenesis of poliomyelitis. Virology 2000; 273: 248-257.
55. Yamayoshi S, Yamashita Y, Li J, et al. Scavenger receptor B2 is a cellular receptor for enterovirus 71. Nat Med 2009; 15: 798-801.
56. Nishimura Y, Shimojima M, Tano Y, et al. Human P-selectin glyco-protein ligand-1 is a functional receptor for enterovirus 71. Nat Med 2009; 15: 794-797.
57. Berkovic SF, Dibbens LM, Oshlack A, et al. Array-based gene discovery with three unrelated subjects shows SCARB2/LIMP-2 defciency causes myoclonus epilepsy and glomerulosclerosis. Am J Hum Genet 2008; 82: 673-684.
58. Herron MJ, Nelson CM, Larson J, et al. Intracellular parasitism by the human granulocytic ehrlichiosis bacterium through the P-selectin ligand, PSGL-1. Science 2000; 288: 1653-1656.
59. Yu P, Gao Z, Zong Y, et al. Histopathological features and distribution of EV71 antigens and SCARB2 in human fatal cases and a mouse model of enterovirus 71 infection. Vi r us Res 2014; 189C: 121-132.
60. Jiao XY, Guo L, Huang DY, et al. Distribution of EV71 receptors SCARB2 and PSGL-1 in human tissues. Viru s Re s 2014; 190C: 40-52.
61. Gaaloul I, Riabi S, Harrath R, et al. Coxsackie B3 myocarditis in a case of sudden unexpected death in young athlete: histopathologi-cal, immunohistochemical and molecularpathological for diagnosis. Forens Sci Int 2011; 208: e10-14.
62. Baboonian C, Davies MJ, Booth JC, et al. Coxsackie B viruses and human heart disease. Curr Topics Microbiol Immunol 1997; 223: 31-52.
63. Verma NA, Zheng XT, Harris MU, et al. Outbreak of life-threatening coxsackievirus B1 myocarditis in neonates. Clin Infect Dis 2009; 49: 759-763.
64. Shafren DR, Bates RC, Agrez MV, et al. Coxsackieviruses B1, B3, and B5 use decay accelerating factor as a receptor for cell attachment. J Virol 1995; 69: 3873-3877.
65. Bergelson JM, Cunningham JA, Droguett G, et al. Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science 1997; 275: 1320-1323.
66. Cohen CJ, Shieh JT, Pickles RJ, et al. The coxsackievirus and aden-ovirus receptor is a transmembrane component of the tight junction. Proc Natl Acad Sci USA 2001; 98: 15191-15196.
67. Lisewski U, Shi Y, Wrackmeyer U, et al. The tight junction protein CAR regulates cardiac conduction and cell-cell communication. J Exp Med 2008; 205: 2369-2379.
68. Noutsias M, Fechner H, de Jonge H, et al. Human coxsackie-adenovirus receptor is colocalized with integrins αvβ3 and αvβ5 on the cardiomyocyte sarcolemma and upregulated in dilated cardiomy-opathy: implications for cardiotropic viral infections. Circulation 2001; 104: 275-280.
69. Jenista JA, Powell KR, Menegus MA. Epidemiology of neonatal enterovirus infection. J Pediatr 1984; 104: 685-690.
70. Ventura KC, Hawkins H, Smith MB, et al. Fatal neonatal echovirus 6 infection: autopsy case report and review of the literature. Mod Pathol 2001; 14: 85-90.
71. Modlin JF. Perinatal echovirus infection: insights from a literature review of 61 cases of serious infection and 16 outbreaks in nurseries. Rev Infect Dis 1986; 8: 918-926.
72. Abzug MJ, Keyserling HL, Lee ML, et al. Neonatal enterovirus infection: virology, serology, and effects of intravenous immune globulin. Clin Infect Dis 1995; 20: 1201-1206.
73. Bailly JL, Beguet A, Chambon M, et al. Nosocomial transmission of echovirus 30: molecular evidence by phylogenetic analysis of the VP1 encoding sequence. J Clin Microbiol 2000; 38: 2889-2892.
74. Konstantinidou A, Anninos H, Spanakis N, et al. Transplacental infection of Coxsackievirus B3 pathological fndings in the fetus. J Med Virol 2007; 79: 754-757.
75. Euscher E, Davis J, Holzman I, et al. Coxsackie virus infection of the placenta associated with neurodevelopmental delays in the newborn. Obstet Gynecol 2001; 98: 1019-1026.
76. Tassin M, Martinovic J, Mirand A, et al. A case of congenital Echovirus11 infection acquired early inpregnancy.J Clin Virol 2014; 59: 71-73.
77. Chow KC, Lee CC, Lin TY, et al. Congenital enterovirus 71 infection: a case study with virology and immunohistochemistry. Clin Infect Dis 2000; 31: 509-512.
78. Garcia AG, Basso NG, Fonseca ME, et al. Congenital echo virus infection-morphological and virological study of fetal and placen-tal tissue. J Pathol 1990; 160: 123-127.
79. Garcia AG, Basso NG, Fonseca ME, et al. Enterovirus associated placental morphology: a light, virological, electron microscopic and immunohistologic study. Placenta 1991; 12: 533-547.
80. Feuer R, Mena I, Pagarigan RR, et al. Coxsackievirus B3 and the neonatal CNS: the roles of stem cells, developing neurons, and apoptosis in infection, viral dissemination, and disease. Am J Pathol 2003; 163: 1379-1393.
81. Foulis AK, Farquharson MA, Cameron SO, et al. A search for the presence of the enteroviral capsid protein VP1 in pancreases of patients with type 1 (insulin-dependent) diabetes and pancreases and hearts of infants who died of coxsackieviral myocarditis. Diabetolo-gia 1990; 33: 290-298.
82. Iwasaki T, Monma N, Satodate R, et al. An immunofuorescent study of generalized Coxsackie virus B3 infection in a newborn infant. Acta Pathol Japon 1985; 35: 741-748.
83. Ylipaasto P, Klingel K, Lindberg AM, et al. Enterovirus infection in human pancreatic islet cells, islet tropism in vivo and receptor involvement in cultured islet β cells. Diabetologia 2004; 47: 225-239.
84. Shieh JT, Bergelson JM. Interaction with decay-accelerating factor facilitates coxsackievirus B infection of polarized epithelial cells. J Vi ro l 2002; 76: 9474-9480.
85. Holmes CH, Simpson KL, Wainwright SD, et al. Preferential expression of the complement regulatory protein decay accelerating factor at the fetomaternal interface during human pregnancy. J Immunol 1990; 144: 3099-3105.
86. Delorme-Axford E, Sadovsky Y, Coyne CB. Lipid raft-and SRC family kinase-dependent entry of coxsackievirus B into human pla-cental trophoblasts. J Virol 2013; 87: 8569-8581.
87. Feder HM, Jr., Bennett N, Modlin JF. Atypical hand, foot, and mouth disease: a vesiculobullous eruption caused by Coxsackie virus A6. Lancet Infect Dis 2014; 14: 83-86.
88. Chung WH, Shih SR, Chang CF, et al. Clinicopathologic analysis of coxsackievirus A6 new variant induced widespread mucocutaneous bullous reactions mimicking severe cutaneous adverse reactions. J Infect Dis 2013; 208: 1968-1978.
89. Jacobson LM, Redd JT, Schneider E, et al. Outbreak of lower respiratory tract illness associated with human enterovirus 68 among American Indian children. Pediatr Infect Dis J 2012; 31: 309-312.
90. Imamura T, Fuji N, Suzuki A, et al. Enterovirus 68 among children with severe acute respiratory infection, the Philippines. Emerg Infect Dis 2011; 17: 1430-1435.
91. Cox DW, Bizzintino J, Ferrari G, et al. Human rhinovirus species C infection in young children with acute wheeze is associated with increased acute respiratory hospital admissions. Am J Resp Crit Care Med 2013; 188: 1358-1364.
92. Hasegawa K, Mansbach JM, Teach SJ, et al. Multicenter study of viral etiology and relapse in hospitalized children with bronchiolitis. Pediatr Infect Dis J 2014; 33: 809-813.
93. Wright PF, Deatly AM, Karron RA, et al. Comparison of results of detection of rhinovirus by PCR and viral culture in human nasal wash specimens from subjects with and without clinical symptoms of respiratory illness. J Clin Microbiol 2007; 45: 2126-2129.
94. Papadopoulos NG, Bates PJ, Bardin PG, et al. Rhinoviruses infect the lower airways. J Infect Dis 2000; 181: 1875-1884.
95. Greve JM, Davis G, Meyer AM, et al. The major human rhinovirus receptor is ICAM-1. Cell 1989; 56: 839-847.
96. Staunton DE, Merluzzi VJ, Rothlein R, et al. A cell adhesion molecule, ICAM-1, is the major surface receptor for rhinoviruses. Cell 1989; 56: 849-853.
97. Milne DS, Gascoigne AD, Wilkes J, et al. MHC class II and ICAM-1 expression and lymphocyte subsets in transbronchial biopsies from lung transplant recipients. Transplantation 1994; 57: 1762-1766.
98. Cunningham AC, Kirby JA. Regulation and function of adhesion molecule expression by human alveolar epithelial cells. Immunology 1995; 86: 279-286.
99. Burns AR, Takei F, Doerschuk CM. Quantitation of ICAM-1 expression in mouse lung during pneumonia. J Immunol 1994; 153: 3189-3198.