Human Rhinovirus: Molecular and Clinical Overview
Main Article Content
Keywords
respiratory viruses, rhinovirus, genome, picornaviridae
Abstract
Human rhinoviruses (HRVs) are associated with a wide spectrum of clinical manifestations, ranging from mild cold symptoms to more severe respiratory illnesses, significantly burdening global healthcare systems. At the molecular level, HRVs belong to the Picornaviridae family and are classified into three species: HRV-A, HRV-B, and HRV-C. Advances in genomic sequencing and phylogenetic analysis have revealed a remarkable genetic diversity within HRV species, with over 160 serotypes identified. This genetic variability contributes to the ability of HRVs to evade host immune responses and facilitates their continuous circulation in the population. This review provides an overview of the molecular and clinical aspects of HRV infections.
References
1. Bochkov YA, Watters K, Ashraf S, et al. Cadherin-related family member 3, a childhood asthma susceptibility gene product, mediates rhinovirus C binding and replication. Proceedings of the National Academy of Sciences of the United States of America. 2015;112(17):5485-90. https://doi.org/10.1073/pnas.1421178112
2. Hamparian V, Colonno R, Cooney M, et al. A collaborative report: rhinoviruses--extension of the numbering system from 89 to 100. Virology. 1987;159(1):191-192. https://doi.org/10.1016/0042-6822(87)90367-9
3. Al-Dulaimi A, Alsayed AR, Al Maqbali M, et al. Investigating the human rhinovirus co-infection in patients with asthma exacerbations and COVID-19. Pharmacy Practice. 2022;20(2):1-10. https://doi.org/10.18549/pharmpract.2022.2.2665
4. Alsayed AR, Abed A, Abu-Samak M, et al. Etiologies of Acute Bronchiolitis in Children at Risk for Asthma, with Emphasis on the Human Rhinovirus Genotyping Protocol. Journal of Clinical Medicine. 2023;12(12):3909. https://doi.org/10.3390/ jcm12123909
5. Alsayed A, Al-Doori A, Al-Dulaimi A, et al. Influences of bovine colostrum on nasal swab microbiome and viral upper respiratory tract infections–A case report. Respiratory medicine case reports. 2020;31:101189. https://doi.org/10.1016/j. rmcr.2020.101189
6. Alsayed AR, Abed A, Khader HA, et al. Molecular Accounting and Profiling of Human Respiratory Microbial Communities: Toward Precision Medicine by Targeting the Respiratory Microbiome for Disease Diagnosis and Treatment. International Journal of Molecular Sciences. 2023;24(4):4086. https://doi.org/10.3390/ijms24044086
7. Oberste MS, Maher K, Kilpatrick DR, et al. Molecular evolution of the human enteroviruses: correlation of serotype with VP1 sequence and application to picornavirus classification. Journal of virology. 1999;73(3):1941-1948. https://doi.org/10.1128/ jvi.73.3.1941-1948.1999
8. Lee W-M, Kiesner C, Pappas T, et al. A diverse group of previously unrecognized human rhinoviruses are common causes of respiratory illnesses in infants. PLoS one. 2007;2(10):e966. https://doi.org/10.1371/journal.pone.0000966
9. Kiang D, Kalra I, Yagi S, et al. Assay for 5′ noncoding region analysis of all human rhinovirus prototype strains. Journal of clinical microbiology. 2008;46(11):3736-3745. https://doi.org/10.1128/jcm.00674-08
10. Lu X, Holloway B, Dare RK, et al. Real-time reverse transcription-PCR assay for comprehensive detection of human rhinoviruses. Journal of clinical microbiology. 2008;46(2):533-539. https://doi.org/10.1128/jcm.01739-07
11. Tapparel C, Cordey S, Van Belle S, et al. New molecular detection tools adapted to emerging rhinoviruses and enteroviruses. Journal of clinical microbiology. 2009;47(6):1742-1749. https://doi.org/10.1128/jcm.02339-08
12. Gama RE, Horsnell PR, Hughes PJ, et al. Amplification of rhinovirus specific nucleic acids from clinical samples using the polymerase chain reaction. J Med Virol. 1989;28(2):73-7. https://doi.org/10.1002/jmv.1890280204
13. Ireland DC, Kent J, Nicholson KG. Improved detection of rhinoviruses in nasal and throat swabs by seminested RT-PCR. J Med Virol. 1993;40(2):96-101. https://doi.org/10.1002/jmv.1890400204
14. Andeweg AC, Bestebroer TM, Huybreghs M, et al. Improved detection of rhinoviruses in clinical samples by using a newly developed nested reverse transcription-PCR assay. J Clin Microbiol. 1999;37(3):524-30. https://doi.org/10.1128/jcm.37.3.524- 530.1999
15. Alsayed AR, Abed A, Abu-Samak M, et al. Etiologies of Acute Bronchiolitis in Children at Risk for Asthma, with Emphasis on the Human Rhinovirus Genotyping Protocol. J Clin Med. 2023;12(12):3909. https://doi.org/10.3390/jcm12123909
16. Faux CE, Arden KE, Lambert SB, et al. Usefulness of published PCR primers in detecting human rhinovirus infection. Emerging infectious diseases. 2011;17(2):296-298. https://doi.org/10.3201/eid1702.101123
17. Bochkov YA, Gern JE. Clinical and molecular features of human rhinovirus C. Microbes and infection. 2012;14(6):485-494. https://doi.org/10.1016/j.micinf.2011.12.011
18. Huang T, Wang W, Bessaud M, et al. Evidence of recombination and genetic diversity in human rhinoviruses in children with acute respiratory infection. PLoS One. 2009;4(7):e6355. https://doi.org/10.1371/journal.pone.0006355
19. McIntyre CL, Leitch ECM, Savolainen-Kopra C, et al. Analysis of genetic diversity and sites of recombination in human rhinovirus species C. Journal of virology. 2010;84(19):10297-10310. https://doi.org/10.1128/jvi.00962-10
20. Savolainen C, Mulders MN, Hovi T. Phylogenetic analysis of rhinovirus isolates collected during successive epidemic seasons. Virus research. 2002;85(1):41-46. https://doi.org/10.1016/s0168-1702(02)00016-3
21. Ledford RM, Patel NR, Demenczuk TM, et al. VP1 sequencing of all human rhinovirus serotypes: insights into genus phylogeny and susceptibility to antiviral capsid-binding compounds. Journal of virology. 2004;78(7):3663-3674. https://doi.org/10.1128/ jvi.78.7.3663-3674.2004
22. Laine P, Savolainen C, Blomqvist S, et al. Phylogenetic analysis of human rhinovirus capsid protein VP1 and 2A protease coding sequences confirms shared genus-like relationships with human enteroviruses. Journal of general virology. 2005;86(3):697- 706. https://doi.org/10.1099/vir.0.80445-0
23. Wisdom A, Leitch EM, Gaunt E, et al . Screening respiratory samples for detection of human rhinoviruses (HRVs) and enteroviruses: comprehensive VP4-VP2 typing reveals high incidence and genetic diversity of HRV species C. Journal of clinical microbiology. 2009;47(12):3958-3967. https://doi.org/10.1128/jcm.00993-09
24. Oberste MS, Maher K, Pallansch MA. Molecular phylogeny and proposed classification of the simian picornaviruses. Journal of virology. 2002;76(3):1244-1251. https://doi.org/10.1128/jvi.76.3.1244-1251.2002
25. Oberste MS, Maher K, Nix WA, et al. Molecular identification of 13 new enterovirus types, EV79–88, EV97, and EV100– 101, members of the species Human Enterovirus B. Virus research. 2007;128(1):34-42. https://doi.org/10.1016/j. virusres.2007.04.001
26. Oberste MS, Michele SM, Maher K, et al. Molecular identification and characterization of two proposed new enterovirus serotypes, EV74 and EV75. Journal of general virology. 2004;85(11):3205-3212. https://doi.org/10.1099/vir.0.80148-0
27. Brown BA, Maher K, Flemister MR, et al. Resolving ambiguities in genetic typing of human enterovirus species C clinical isolates and identification of enterovirus 96, 99 and 102. Journal of General Virology. 2009;90(7):1713-1723. https://doi.org/10.1099/ vir.0.008540-0
28. Smura TP, Junttila N, Blomqvist S, et al. Enterovirus 94, a proposed new serotype in human enterovirus species D. Journal of general virology. 2007;88(3):849-858. https://doi.org/10.1099/vir.0.82510-0
29. Bouslama L, Nasri D, Chollet L, et al. Natural recombination event within the capsid genomic region leading to a chimeric strain of human enterovirus B. Journal of virology. 2007;81(17):8944-8952. https://doi.org/10.1128/jvi.00180-07
30. Zhang Y, Zhu S, Yan D, et al. Natural type 3/type 2 intertypic vaccine-related poliovirus recombinants with the first crossover sites within the VP1 capsid coding region. PLoS One. 2010;5(12):e15300. https://doi.org/10.1371/journal.pone.0015300
31. Arola A, Santti J, Ruuskanen O, et al. Identification of enteroviruses in clinical specimens by competitive PCR followed by genetic typing using sequence analysis. Journal of clinical microbiology. 1996;34(2):313-318. https://doi.org/10.1128/jcm.34.2.313- 318.1996
32. Oberste MS, Maher K, Pallansch MA. Molecular phylogeny of all human enterovirus serotypes based on comparison of sequences at the 5′ end of the region encoding VP2. Virus research. 1998;58(1):35-43. https://doi.org/10.1016/s0168- 1702(98)00101-4
33. Oberste MS, Maher K, Flemister MR, et al. Comparison of classic and molecular approaches for the identification of untypeable enteroviruses. Journal of clinical microbiology. 2000;38(3):1170-1174. https://doi.org/10.1128/jcm.38.3.1170-1174.2000
34. Lauber C, Gorbalenya AE. Partitioning the genetic diversity of a virus family: approach and evaluation through a case study of picornaviruses. Journal of virology. 2012;86(7):3890-3904. https://doi.org/10.1128/jvi.07173-11
35. Zell R. Picornaviridae—the ever-growing virus family. Archives of virology. 2018;163(2):299-317. 36. Ambros V, Baltimore D. Protein is linked to the 5’end of poliovirus RNA by a phosphodiester linkage to tyrosine. Journal of Biological Chemistry. 1978;253(15):5263-5266.
37. King AM, Lefkowitz E, Adams MJ, et al. Virus taxonomy: ninth report of the International Committee on Taxonomy of Viruses. Elsevier; 2011.
38. Le Gall O, Christian P, Fauquet CM, et al. Picornavirales, a proposed order of positive-sense single-stranded RNA viruses with a pseudo-T= 3 virion architecture. Archives of virology. 2008;153(4):715. https://doi.org/10.1007/s00705-008-0041-x
39. Pelon W, Mogabgab W, Phillips I, et al. A cytopathogenic agent isolated from naval recruits with mild respiratory illnesses. Experimental Biology and Medicine. 1957;94(2):262-267. https://doi.org/10.3181/00379727-94-22915
40. Price WH. The isolation of a new virus associated with respiratory clinical disease in humans. Proceedings of the National Academy of Sciences. 1956;42(12):892-896. https://doi.org/10.1073/pnas.42.12.892
41. Kapikian A, Conant R, Hamparian V, et al. A collaborative report: rhinoviruses—extension of the numbering system. Virology. 1971;43(2):524-526.
42. Cooney M, Fox J, Kenny G. Antigenic groupings of 90 rhinovirus serotypes. Infection and immunity. 1982;37(2):642-647. https://doi.org/10.1128/iai.37.2.642-647.1982
43. Halfpap LM, Cooney MK. Isolation of rhinovirus intertypes related to either rhinoviruses 12 and 78 or 36 and 58. Infection and immunity. 1983;40(1):213-218. https://doi.org/10.1128/iai.40.1.213-218.1983
44. McIntosh K, Dees JH, Becker WB, et al. Recovery in tracheal organ cultures of novel viruses from patients with respiratory disease. Proceedings of the national academy of sciences. 1967;57(4):933-940. https://doi.org/10.1073/pnas.57.4.933
45. McIntyre CL, McWilliam Leitch EC, Savolainen-Kopra C, et al. Analysis of genetic diversity and sites of recombination in human rhinovirus species C. Journal of virology. 2010;84(19):10297-10310. https://doi.org/10.1128/jvi.00962-10
46. Van Loon A, Cleator G, Ras A. External quality assessment of enterovirus detection and typing. European Union Concerted Action on Virus Meningitis and Encephalitis. Bulletin of the World Health Organization. 1999;77(3):217. http://www.ncbi.nlm.nih.gov/pmc/articles/pmc2557629/
47. Horsnell C, Gama RE, Hughes PJ, et al. Molecular relationships between 21 human rhinovirus serotypes. Journal of general virology. 1995;76(10):2549-2555. https://doi.org/10.1099/0022-1317-76-10-2549
48. Savolainen C, Laine P, Mulders MN, et al. Sequence analysis of human rhinoviruses in the RNA-dependent RNA polymerase coding region reveals large within-species variation. Journal of general virology. 2004;85(8):2271-2277. https://doi. org/10.1099/vir.0.79897-0
49. Palmenberg AC, Spiro D, Kuzmickas R, et al. Sequencing and analyses of all known human rhinovirus genomes reveal structure and evolution. Science. 2009;324(5923):55-59. https://doi.org/10.1126/science.1165557
50. Stanway G, Kalkkinen N, Roivainen M, et al. Molecular and biological characteristics of echovirus 22, a representative of a new picornavirus group. Journal of virology. 1994;68(12):8232-8238. https://doi.org/10.1128/jvi.68.12.8232-8238.1994
51. Li Q, Yafal AG, Lee Y, et al. Poliovirus neutralization by antibodies to internal epitopes of VP4 and VP1 results from reversible exposure of these sequences at physiological temperature. Journal of virology. 1994;68(6):3965-3970. https://doi.org/10.1128/ jvi.68.6.3965-3970.1994
52. Lewis JK, Bothner B, Smith TJ, et al. Antiviral agent blocks breathing of the common cold virus. Proceedings of the National Academy of Sciences. 1998;95(12):6774-6778. https://doi.org/10.1073/pnas.95.12.6774
53. Katpally U, Fu T-M, Freed DC, et al. Antibodies to the buried N terminus of rhinovirus VP4 exhibit cross-serotypic neutralization. Journal of virology. 2009;83(14):7040-7048. https://doi.org/10.1128/jvi.00557-09
54. Hewat EA, Neumann E, Conway JF, et al. The cellular receptor to human rhinovirus 2 binds around the 5‐fold axis and not in the canyon: a structural view. The EMBO journal. 2000;19(23):6317-6325. https://doi.org/10.1093/emboj/19.23.6317
55. Colonno RJ, Condra JH, Mizutani S, et al. Evidence for the direct involvement of the rhinovirus canyon in receptor binding. Proceedings of the National Academy of Sciences. 1988;85(15):5449-5453. https://doi.org/10.1073/pnas.85.15.5449
56. Acharya R, Fry E, Stuart D, et al. The three-dimensional structure of foot-and-mouth disease virus at 2.9 Å resolution. 1989;337(6209):709-16. https://doi.org/10.1038/337709a0
57. Oliveira MA, Zhao R, Lee W-M, et al. The structure of human rhinovirus 16. Structure. 1993;1(1):51-68. https://doi. org/10.1016/0969-2126(93)90008-5
58. Verdaguer N, Blaas D, Fita I. Structure of human rhinovirus serotype 2 (HRV2). Journal of molecular biology. 2000;300(5):1179- 1194. https://doi.org/10.1006/jmbi.2000.3943
59. Smith TJ, Kremer MJ, Luo M, et al. The site of attachment in human rhinovirus 14 for antiviral agents that inhibit uncoating. Science. 1986;233:1286-1294. https://doi.org/10.1126/science.3018924
60. Spector DH, Baltimore D. Requirement of 3′-terminal poly (adenylic acid) for the infectivity of poliovirus RNA. Proceedings of the National Academy of Sciences. 1974;71(8):2983-2987. https://doi.org/10.1073/pnas.71.8.2983
61. Racaniello VR. Picornaviridae: the viruses and their replication. Fields virology. 2001;
62. Rueckert RR, Wimmer E. Systematic nomenclature of picornavirus proteins. Journal of virology. 1984;50(3):957. https://doi. org/10.1128/jvi.50.3.957-959.1984
63. Oberste MS, Maher K, Kilpatrick DR, et al. Typing of human enteroviruses by partial sequencing of VP1. Journal of clinical microbiology. 1999;37(5):1288-1293. https://doi.org/10.1128/jcm.37.5.1288-1293.1999
64. Ortega H, Nickle D, Carter L. Rhinovirus and asthma: Challenges and opportunities. Reviews in Medical Virology. 2021;31(4):e2193. https://doi.org/10.1002/rmv.2193
65. Broberg E, Niemelä J, Lahti E, et al. Human rhinovirus C—associated severe pneumonia in a neonate. Journal of Clinical Virology. 2011;51(1):79-82. https://doi.org/10.1016/j.jcv.2011.01.018
66. Hicks LA, Shepard CW, Britz PH, et al. Two outbreaks of severe respiratory disease in nursing homes associated with rhinovirus. Journal of the American Geriatrics Society. 2006;54(2):284-289. https://doi.org/10.1111/j.1532-5415.2005.00529.x
67. Jartti T, Korppi M. Rhinovirus‐induced bronchiolitis and asthma development. Pediatric Allergy and Immunology. 2011;22(4):350-355. https://doi.org/10.1111/j.1399-3038.2011.01170.x
68. Jackson DJ, Gangnon RE, Evans MD, et al. Wheezing rhinovirus illnesses in early life predict asthma development in highrisk children. American journal of respiratory and critical care medicine. 2008;178(7):667-672. https://doi.org/10.1164/ rccm.200802-309oc
69. Fendrick AM, Monto AS, Nightengale B, et al. The economic burden of non–influenza-related viral respiratory tract infection in the United States. Archives of internal medicine. 2003;163(4):487-494. https://doi.org/10.1001/archinte.163.4.487
70. Alsayed AR, El Hajji FD, Al-Najjar MA, et al. Patterns of antibiotic use, knowledge, and perceptions among different population categories: A comprehensive study based in Arabic countries. Saudi Pharmaceutical Journal. 2022;30(3):317-328. https://doi. org/10.1016/j.jsps.2022.01.013
71. Brownlee JW, Turner RB. New developments in the epidemiology and clinical spectrum of rhinovirus infections. Current opinion in pediatrics. 2008;20(1):67-71. https://doi.org/10.1097/mop.0b013e3282f41cb6
72. Gern JE. The ABCs of rhinoviruses, wheezing, and asthma. Journal of virology. 2010;84(15):7418-7426. https://doi.org/10.1128/ jvi.02290-09
73. Miller EK, Lu X, Erdman DD, et al. Rhinovirus-associated hospitalizations in young children. Journal of Infectious Diseases. 2007;195(6):773-781. https://doi.org/10.1086/511821
74. Peltola V, Waris M, Österback R, et al. Rhinovirus transmission within families with children: incidence of symptomatic and asymptomatic infections. Journal of Infectious Diseases. 2008;197(3):382-389. https://doi.org/10.1086/525542
75. Turner RB, Lee W. Rhinovirus. Clinical virology. 2009;(Ed. 3):1063-1082.
76. Alsayed AR. Illustrating How to Use the Validated Alsayed_v1 Tools to Improve Medical Care: A Particular Reference to the Global Initiative for Asthma 2022 Recommendations. Patient preference and adherence. 2023:1161-1179. https://doi. org/10.2147/ppa.s403239
77. Ko FWS, Ip M, Chan PKS, et al. A 1-year prospective study of the infectious etiology in patients hospitalized with acute exacerbations of COPD. CHEST Journal. 2007;131(1):44-52. https://doi.org/10.1378/chest.06-1355
78. Papi A, Bellettato CM, Braccioni F, et al. Infections and airway inflammation in chronic obstructive pulmonary disease severe exacerbations. American journal of respiratory and critical care medicine. 2006;173(10):1114-1121. https://doi.org/10.1164/ rccm.200506-859oc
79. Perotin JM, Dury S, Renois F, et al. Detection of multiple viral and bacterial infections in acute exacerbation of chronic obstructive pulmonary disease: a pilot prospective study. Journal of medical virology. 2013;85(5):866-873. https://doi. org/10.1002/jmv.23495
80. McManus TE, Marley A-M, Baxter N, et al. Respiratory viral infection in exacerbations of COPD. Respiratory medicine. 2008;102(11):1575-1580. https://doi.org/10.1016/j.rmed.2008.06.006
81. Kherad O, Kaiser L, Bridevaux P-O, et al. Upper-respiratory viral infection, biomarkers, and COPD exacerbations. CHEST Journal. 2010;138(4):896-904. https://doi.org/10.1378/chest.09-2225
82. Hutchinson AF, Ghimire AK, Thompson MA, et al. A community-based, time-matched, case-control study of respiratory viruses and exacerbations of COPD. Respiratory medicine. 2007;101(12):2472-2481. https://doi.org/10.1016/j.rmed.2007.07.015
83. Hewitt R, Farne H, Ritchie A, et al. The role of viral infections in exacerbations of chronic obstructive pulmonary disease and asthma. Therapeutic advances in respiratory disease. 2015;10(2):158-74. https://doi.org/10.1177/1753465815618113
84. Jackson DJ, Gangnon RE, Evans MD, et al. Wheezing rhinovirus illnesses in early life predict asthma development in highrisk children. American journal of respiratory and critical care medicine. 2008;178(7):667-72. https://doi.org/10.1164/ rccm.200802-309OC
85. Holt PG, Sly PD. Viral infections and atopy in asthma pathogenesis: new rationales for asthma prevention and treatment. Nature medicine. 2012;18(5):726-35. https://doi.org/10.1038/nm.2768
86. Lemanske RF, Jr., Jackson DJ, Gangnon RE, et al. Rhinovirus illnesses during infancy predict subsequent childhood wheezing. The Journal of allergy and clinical immunology. 2005;116(3):571-7. https://doi.org/10.1016/j.jaci.2005.06.024
87. Gern JE. Viral respiratory infection and the link to asthma. The Pediatric infectious disease journal. 2008;27(10 Suppl):S97-103. https://doi.org/10.1097/INF.0b013e318168b718
88. Alsayed AR, Hasoun L, Khader HA, et al. Co-infection of COVID-19 patients with atypical bacteria: A study based in Jordan. Pharmacy Practice. 2023;21(1):1-5. https://doi.org/10.18549/pharmpract.2023.1.2753
89. Alsayed AR, Talib W, Al-Dulaimi A, et al. The first detection of Pneumocystis jirovecii in asthmatic patients post-COVID-19 in Jordan. Bosnian Journal of Basic Medical Sciences. 2022;22(5):784. https://doi.org/10.17305/bjbms.2022.7335
90. Corne JM, Marshall C, Smith S, et al. Frequency, severity, and duration of rhinovirus infections in asthmatic and non-asthmatic individuals: a longitudinal cohort study. Lancet (London, England). 2002;359(9309):831-4. https://doi.org/10.1016/s0140- 6736(02)07953-9
91. Allakhverdi Z, Comeau MR, Jessup HK, et al. Thymic stromal lymphopoietin is released by human epithelial cells in response to microbes, trauma, or inflammation and potently activates mast cells. The Journal of experimental medicine. 2007;204(2):253- 8. https://doi.org/10.1084/jem.20062211
92. Kato A, Favoreto S, Jr., Avila PC, Schleimer RP. TLR3- and Th2 cytokine-dependent production of thymic stromal lymphopoietin in human airway epithelial cells. Journal of immunology (Baltimore, Md : 1950). 2007;179(2):1080-7. https://doi.org/10.4049/ jimmunol.179.2.1080
93. Jackson DJ, Makrinioti H, Rana BM, et al. IL-33-dependent type 2 inflammation during rhinovirus-induced asthma exacerbations in vivo. American journal of respiratory and critical care medicine. 2014;190(12):1373-82. https://doi.org/10.1164/ rccm.201406-1039OC
94. Sigurs N, Bjarnason R, Sigurbergsson F, et al. Respiratory syncytial virus bronchiolitis in infancy is an important risk factor for asthma and allergy at age 7. American journal of respiratory and critical care medicine. 2000;161(5):1501-7. https://doi. org/10.1164/ajrccm.161.5.9906076
95. Sigurs N, Gustafsson PM, Bjarnason R, et al. Severe respiratory syncytial virus bronchiolitis in infancy and asthma and allergy at age 13. American journal of respiratory and critical care medicine. 2005;171(2):137-41. https://doi.org/10.1164/rccm.200406- 730OC
96. Kusel MM, de Klerk NH, Kebadze T, et al. Early-life respiratory viral infections, atopic sensitization, and risk of subsequent development of persistent asthma. The Journal of allergy and clinical immunology. 2007;119(5):1105-10. https://doi. org/10.1016/j.jaci.2006.12.669
97. Olenec JP, Kim WK, Lee WM, et al. Weekly monitoring of children with asthma for infections and illness during common cold seasons. The Journal of allergy and clinical immunology. 2010;125(5):1001-1006.e1. https://doi.org/10.1016/j.jaci.2010.01.059
98. Edwards MR, Strong K, Cameron A, et al. Viral infections in allergy and immunology: How allergic inflammation influences viral infections and illness. The Journal of allergy and clinical immunology. 2017;140(4):909-920. https://doi.org/10.1016/j. jaci.2017.07.025
99. Bisgaard H, Hermansen MN, Bønnelykke K, et al. Association of bacteria and viruses with wheezy episodes in young children: prospective birth cohort study. BMJ (Clinical research ed). 2010;341:c4978. https://doi.org/10.1136/bmj.c4978
100. Lynch SV, Wood RA, Boushey H, et al. Effects of early-life exposure to allergens and bacteria on recurrent wheeze and atopy in urban children. The Journal of allergy and clinical immunology. 2014;134(3):593-601.e12. https://doi.org/10.1016/j. jaci.2014.04.018
101. Kloepfer KM, Lee WM, Pappas TE, et al. Detection of pathogenic bacteria during rhinovirus infection is associated with increased respiratory symptoms and asthma exacerbations. The Journal of allergy and clinical immunology. 2014;133(5):1301- 7, 1307.e1-3. https://doi.org/10.1016/j.jaci.2014.02.030
102. Kloepfer KM, Sarsani VK, Poroyko V, et al. Community-acquired rhinovirus infection is associated with changes in the airway microbiome. The Journal of allergy and clinical immunology. 2017;140(1):312-315.e8. https://doi.org/10.1016/j. jaci.2017.01.038
103. Stein RT, Sherrill D, Morgan WJ, et al. Respiratory syncytial virus in early life and risk of wheeze and allergy by age 13 years. Lancet (London, England). 1999;354(9178):541-5. https://doi.org/10.1016/s0140-6736(98)10321-5
104. Jackson DJ. The role of rhinovirus infections in the development of early childhood asthma. Current opinion in allergy and clinical immunology. 2010;10(2):133-8. https://doi.org/10.1097/ACI.0b013e3283352f7c
105. Kotaniemi-Syrjänen A, Vainionpää R, Reijonen TM, et al. Rhinovirus-induced wheezing in infancy--the first sign of childhood asthma? The Journal of allergy and clinical immunology. 2003;111(1):66-71. https://doi.org/10.1067/mai.2003.33
106. ly PD, Kusel M, Holt PG. Do early-life viral infections cause asthma? The Journal of allergy and clinical immunology. 2010;125(6):1202-5. https://doi.org/10.1016/j.jaci.2010.01.024
107. Rantala AK, Jaakkola MS, Mäkikyrö EM, et al. Early Respiratory Infections and the Development of Asthma in the First 27 Years of Life. American journal of epidemiology. 2015;182(7):615-23. https://doi.org/10.1093/aje/kwv093
108. Rosenthal LA, Avila PC, Heymann PW, et al. Viral respiratory tract infections and asthma: the course ahead. The Journal of allergy and clinical immunology. 2010;125(6):1212-7. https://doi.org/10.1016/j.jaci.2010.04.002
109. Wu P, Dupont WD, Griffin MR, et al. Evidence of a causal role of winter virus infection during infancy in early childhood asthma. American journal of respiratory and critical care medicine. 2008;178(11):1123-9. https://doi.org/10.1164/rccm.200804-579OC
110. Bartlett NW, McLean GR, Chang YS, et al. Genetics and epidemiology: asthma and infection. Current opinion in allergy and clinical immunology. 2009;9(5):395-400. https://doi.org/10.1097/ACI.0b013e32833066fa
111. Gern JE. Rhinovirus and the initiation of asthma. Current opinion in allergy and clinical immunology. 2009;9(1):73-8. https:// doi.org/10.1097/ACI.0b013e32831f8f1b
112. Sigurs N, Aljassim F, Kjellman B, et al. Asthma and allergy patterns over 18 years after severe RSV bronchiolitis in the first year of life. Thorax. 2010;65(12):1045-52. https://doi.org/10.1136/thx.2009.121582
113. Simões EA, Carbonell-Estrany X, Rieger CH, et al. The effect of respiratory syncytial virus on subsequent recurrent wheezing in atopic and nonatopic children. The Journal of allergy and clinical immunology. 2010;126(2):256-62. https://doi.org/10.1016/j. jaci.2010.05.026
114. Martinez FD, Morgan WJ, Wright AL, et al. Diminished lung function as a predisposing factor for wheezing respiratory illness in infants. The New England journal of medicine. 1988;319(17):1112-7. https://doi.org/10.1056/nejm198810273191702
115. Martinez FD, Wright AL, Taussig LM, et al. Asthma and wheezing in the first six years of life. The Group Health Medical Associates. The New England journal of medicine. 1995;332(3):133-8. https://doi.org/10.1056/nejm199501193320301
116. Pattemore PK, Johnston SL, Bardin PG. Viruses as precipitants of asthma symptoms. I. Epidemiology. Clinical and experimental allergy : journal of the British Society for Allergy and Clinical Immunology. 1992;22(3):325-36. https://doi. org/10.1111/j.1365-2222.1992.tb03094.x
117. Shaheen SO. Changing patterns of childhood infection and the rise in allergic disease. Clinical and experimental allergy : journal of the British Society for Allergy and Clinical Immunology. 1995;25(11):1034-7. https://doi.org/10.1111/j.1365-2222.1995. tb03248.x
118. Sigurs N, Bjarnason R, Sigurbergsson F, et al. Asthma and immunoglobulin E antibodies after respiratory syncytial virus bronchiolitis: a prospective cohort study with matched controls. Pediatrics. 1995;95(4):500-5.
119. Cogswell JJ, Halliday DF, Alexander JR. Respiratory infections in the first year of life in children at risk of developing atopy. British medical journal (Clinical research ed). 1982;284(6321):1011-3. https://doi.org/10.1136/bmj.284.6321.1011
120. Welliver RC. RSV and chronic asthma. Lancet (London, England). 1995;346(8978):789-90. https://doi.org/10.1016/s0140- 6736(95)91615-6
121. Bacharier LB, Cohen R, Schweiger T, et al. Determinants of asthma after severe respiratory syncytial virus bronchiolitis. The Journal of allergy and clinical immunology. 2012;130(1):91-100.e3. https://doi.org/10.1016/j.jaci.2012.02.010
122. Jartti T, Kuusipalo H, Vuorinen T, et al. Allergic sensitization is associated with rhinovirus-, but not other virus-, induced wheezing in children. Pediatric allergy and immunology : official publication of the European Society of Pediatric Allergy and Immunology. 2010;21(7):1008-14. https://doi.org/10.1111/j.1399-3038.2010.01059.x
123. Gern JE, Vrtis R, Grindle KA, et al. Relationship of upper and lower airway cytokines to outcome of experimental rhinovirus infection. American journal of respiratory and critical care medicine. 2000;162(6):2226-31. https://doi.org/10.1164/ ajrccm.162.6.2003019
124. GINA. Global Initiative for Asthma, Global Strategy for Asthma Management and Prevention. 2023. http: //www.gi-nasthma. org
125. Vincenzo SD, Ferrante G, Ferraro M, et al. Oxidative Stress, Environmental Pollution, and Lifestyle as Determinants of Asthma in Children. Biology. 2023;12(1):133. https://doi.org/10.3390/biology12010133
126. Nakagome K, Nagata M. Innate immune responses by respiratory viruses, including rhinovirus, during asthma exacerbation. Frontiers in immunology. 2022;13:865973. https://doi.org/10.3389/fimmu.2022.865973
127. Dinwiddie DL, Kaukis N, Pham S, et al. Viral infection and allergy status impact severity of asthma symptoms in children with asthma exacerbations. Annals of Allergy, Asthma & Immunology. 2022;129(3):319-326. e3. https://doi.org/10.1016/j. anai.2022.06.017
128. Kim SR. Viral infection and airway epithelial immunity in asthma. International Journal of Molecular Sciences. 2022;23(17):9914. https://doi.org/10.3390/ijms23179914
129. Ramphul M. Increased inhaled corticosteroids for treating acute asthma exacerbations. Wiley Online Library; 2023. p. 388- 391. https://doi.org/10.1111/cea.14306
130. McDowell PJ, Busby J, Heaney LG. Asthma Exacerbations in Severe Asthma: Why Systemic Corticosteroids May not Always Be the Best Treatment Option. Current Treatment Options in Allergy. 2023;10(1):53-63.
131. Bagnasco D, Testino E, Nicola S, et al. Specific Therapy for T2 Asthma. Journal of Personalized Medicine. 2022;12(4):593. https://doi.org/10.3390/jpm12040593
132. Blanken MO, Rovers MM, Molenaar JM, et al. Respiratory syncytial virus and recurrent wheeze in healthy preterm infants. The New England journal of medicine. 2013;368(19):1791-9. https://doi.org/10.1056/NEJMoa1211917
133. Scheltema NM, Nibbelke EE, Pouw J, et al. Respiratory syncytial virus prevention and asthma in healthy preterm infants: a randomised controlled trial. The Lancet Respiratory medicine. 2018;6(4):257-264. https://doi.org/10.1016/s2213- 2600(18)30055-9
134. Holt PG, Strickland DH, Hales BJ, et al. Defective respiratory tract immune surveillance in asthma: a primary causal factor in disease onset and progression. Chest. 2014;145(2):370-378. https://doi.org/10.1378/chest.13-1341
135. Durrani SR, Montville DJ, Pratt AS, et al. Innate immune responses to rhinovirus are reduced by the high-affinity IgE receptor in allergic asthmatic children. The Journal of allergy and clinical immunology. 2012;130(2):489-95. https://doi.org/10.1016/j. jaci.2012.05.023
136. Gill MA, Bajwa G, George TA, et al. Counterregulation between the FcepsilonRI pathway and antiviral responses in human plasmacytoid dendritic cells. Journal of immunology (Baltimore, Md : 1950). 2010;184(11):5999-6006. https://doi.org/10.4049/ jimmunol.0901194
137. Teach SJ, Gill MA, Togias A, et al. Preseasonal treatment with either omalizumab or an inhaled corticosteroid boost to prevent fall asthma exacerbations. The Journal of allergy and clinical immunology. 2015;136(6):1476-1485. https://doi.org/10.1016/j. jaci.2015.09.008
138. Esquivel A, Busse WW, Calatroni A, et al. Effects of omalizumab on rhinovirus infections, illnesses, and exacerbations of asthma. American journal of respiratory and critical care medicine. 2017;196(8):985-992. https://doi.org/10.1164/rccm.201701- 0120oc
139. Teach SJ, Gill MA, Togias A, et al. Preseasonal treatment with either omalizumab or an inhaled corticosteroid boost to prevent fall asthma exacerbations. Journal of Allergy and Clinical Immunology. 2015;136(6):1476-1485. https://doi.org/10.1016/j. jaci.2015.09.008
140. Fu Z, Xu Y, Cai C. Efficacy and safety of omalizumab in children with moderate-to-severe asthma: a meta-analysis. Journal of Asthma. 2021;58(10):1350-1358. https://doi.org/10.1080/02770903.2020.1789875
2. Hamparian V, Colonno R, Cooney M, et al. A collaborative report: rhinoviruses--extension of the numbering system from 89 to 100. Virology. 1987;159(1):191-192. https://doi.org/10.1016/0042-6822(87)90367-9
3. Al-Dulaimi A, Alsayed AR, Al Maqbali M, et al. Investigating the human rhinovirus co-infection in patients with asthma exacerbations and COVID-19. Pharmacy Practice. 2022;20(2):1-10. https://doi.org/10.18549/pharmpract.2022.2.2665
4. Alsayed AR, Abed A, Abu-Samak M, et al. Etiologies of Acute Bronchiolitis in Children at Risk for Asthma, with Emphasis on the Human Rhinovirus Genotyping Protocol. Journal of Clinical Medicine. 2023;12(12):3909. https://doi.org/10.3390/ jcm12123909
5. Alsayed A, Al-Doori A, Al-Dulaimi A, et al. Influences of bovine colostrum on nasal swab microbiome and viral upper respiratory tract infections–A case report. Respiratory medicine case reports. 2020;31:101189. https://doi.org/10.1016/j. rmcr.2020.101189
6. Alsayed AR, Abed A, Khader HA, et al. Molecular Accounting and Profiling of Human Respiratory Microbial Communities: Toward Precision Medicine by Targeting the Respiratory Microbiome for Disease Diagnosis and Treatment. International Journal of Molecular Sciences. 2023;24(4):4086. https://doi.org/10.3390/ijms24044086
7. Oberste MS, Maher K, Kilpatrick DR, et al. Molecular evolution of the human enteroviruses: correlation of serotype with VP1 sequence and application to picornavirus classification. Journal of virology. 1999;73(3):1941-1948. https://doi.org/10.1128/ jvi.73.3.1941-1948.1999
8. Lee W-M, Kiesner C, Pappas T, et al. A diverse group of previously unrecognized human rhinoviruses are common causes of respiratory illnesses in infants. PLoS one. 2007;2(10):e966. https://doi.org/10.1371/journal.pone.0000966
9. Kiang D, Kalra I, Yagi S, et al. Assay for 5′ noncoding region analysis of all human rhinovirus prototype strains. Journal of clinical microbiology. 2008;46(11):3736-3745. https://doi.org/10.1128/jcm.00674-08
10. Lu X, Holloway B, Dare RK, et al. Real-time reverse transcription-PCR assay for comprehensive detection of human rhinoviruses. Journal of clinical microbiology. 2008;46(2):533-539. https://doi.org/10.1128/jcm.01739-07
11. Tapparel C, Cordey S, Van Belle S, et al. New molecular detection tools adapted to emerging rhinoviruses and enteroviruses. Journal of clinical microbiology. 2009;47(6):1742-1749. https://doi.org/10.1128/jcm.02339-08
12. Gama RE, Horsnell PR, Hughes PJ, et al. Amplification of rhinovirus specific nucleic acids from clinical samples using the polymerase chain reaction. J Med Virol. 1989;28(2):73-7. https://doi.org/10.1002/jmv.1890280204
13. Ireland DC, Kent J, Nicholson KG. Improved detection of rhinoviruses in nasal and throat swabs by seminested RT-PCR. J Med Virol. 1993;40(2):96-101. https://doi.org/10.1002/jmv.1890400204
14. Andeweg AC, Bestebroer TM, Huybreghs M, et al. Improved detection of rhinoviruses in clinical samples by using a newly developed nested reverse transcription-PCR assay. J Clin Microbiol. 1999;37(3):524-30. https://doi.org/10.1128/jcm.37.3.524- 530.1999
15. Alsayed AR, Abed A, Abu-Samak M, et al. Etiologies of Acute Bronchiolitis in Children at Risk for Asthma, with Emphasis on the Human Rhinovirus Genotyping Protocol. J Clin Med. 2023;12(12):3909. https://doi.org/10.3390/jcm12123909
16. Faux CE, Arden KE, Lambert SB, et al. Usefulness of published PCR primers in detecting human rhinovirus infection. Emerging infectious diseases. 2011;17(2):296-298. https://doi.org/10.3201/eid1702.101123
17. Bochkov YA, Gern JE. Clinical and molecular features of human rhinovirus C. Microbes and infection. 2012;14(6):485-494. https://doi.org/10.1016/j.micinf.2011.12.011
18. Huang T, Wang W, Bessaud M, et al. Evidence of recombination and genetic diversity in human rhinoviruses in children with acute respiratory infection. PLoS One. 2009;4(7):e6355. https://doi.org/10.1371/journal.pone.0006355
19. McIntyre CL, Leitch ECM, Savolainen-Kopra C, et al. Analysis of genetic diversity and sites of recombination in human rhinovirus species C. Journal of virology. 2010;84(19):10297-10310. https://doi.org/10.1128/jvi.00962-10
20. Savolainen C, Mulders MN, Hovi T. Phylogenetic analysis of rhinovirus isolates collected during successive epidemic seasons. Virus research. 2002;85(1):41-46. https://doi.org/10.1016/s0168-1702(02)00016-3
21. Ledford RM, Patel NR, Demenczuk TM, et al. VP1 sequencing of all human rhinovirus serotypes: insights into genus phylogeny and susceptibility to antiviral capsid-binding compounds. Journal of virology. 2004;78(7):3663-3674. https://doi.org/10.1128/ jvi.78.7.3663-3674.2004
22. Laine P, Savolainen C, Blomqvist S, et al. Phylogenetic analysis of human rhinovirus capsid protein VP1 and 2A protease coding sequences confirms shared genus-like relationships with human enteroviruses. Journal of general virology. 2005;86(3):697- 706. https://doi.org/10.1099/vir.0.80445-0
23. Wisdom A, Leitch EM, Gaunt E, et al . Screening respiratory samples for detection of human rhinoviruses (HRVs) and enteroviruses: comprehensive VP4-VP2 typing reveals high incidence and genetic diversity of HRV species C. Journal of clinical microbiology. 2009;47(12):3958-3967. https://doi.org/10.1128/jcm.00993-09
24. Oberste MS, Maher K, Pallansch MA. Molecular phylogeny and proposed classification of the simian picornaviruses. Journal of virology. 2002;76(3):1244-1251. https://doi.org/10.1128/jvi.76.3.1244-1251.2002
25. Oberste MS, Maher K, Nix WA, et al. Molecular identification of 13 new enterovirus types, EV79–88, EV97, and EV100– 101, members of the species Human Enterovirus B. Virus research. 2007;128(1):34-42. https://doi.org/10.1016/j. virusres.2007.04.001
26. Oberste MS, Michele SM, Maher K, et al. Molecular identification and characterization of two proposed new enterovirus serotypes, EV74 and EV75. Journal of general virology. 2004;85(11):3205-3212. https://doi.org/10.1099/vir.0.80148-0
27. Brown BA, Maher K, Flemister MR, et al. Resolving ambiguities in genetic typing of human enterovirus species C clinical isolates and identification of enterovirus 96, 99 and 102. Journal of General Virology. 2009;90(7):1713-1723. https://doi.org/10.1099/ vir.0.008540-0
28. Smura TP, Junttila N, Blomqvist S, et al. Enterovirus 94, a proposed new serotype in human enterovirus species D. Journal of general virology. 2007;88(3):849-858. https://doi.org/10.1099/vir.0.82510-0
29. Bouslama L, Nasri D, Chollet L, et al. Natural recombination event within the capsid genomic region leading to a chimeric strain of human enterovirus B. Journal of virology. 2007;81(17):8944-8952. https://doi.org/10.1128/jvi.00180-07
30. Zhang Y, Zhu S, Yan D, et al. Natural type 3/type 2 intertypic vaccine-related poliovirus recombinants with the first crossover sites within the VP1 capsid coding region. PLoS One. 2010;5(12):e15300. https://doi.org/10.1371/journal.pone.0015300
31. Arola A, Santti J, Ruuskanen O, et al. Identification of enteroviruses in clinical specimens by competitive PCR followed by genetic typing using sequence analysis. Journal of clinical microbiology. 1996;34(2):313-318. https://doi.org/10.1128/jcm.34.2.313- 318.1996
32. Oberste MS, Maher K, Pallansch MA. Molecular phylogeny of all human enterovirus serotypes based on comparison of sequences at the 5′ end of the region encoding VP2. Virus research. 1998;58(1):35-43. https://doi.org/10.1016/s0168- 1702(98)00101-4
33. Oberste MS, Maher K, Flemister MR, et al. Comparison of classic and molecular approaches for the identification of untypeable enteroviruses. Journal of clinical microbiology. 2000;38(3):1170-1174. https://doi.org/10.1128/jcm.38.3.1170-1174.2000
34. Lauber C, Gorbalenya AE. Partitioning the genetic diversity of a virus family: approach and evaluation through a case study of picornaviruses. Journal of virology. 2012;86(7):3890-3904. https://doi.org/10.1128/jvi.07173-11
35. Zell R. Picornaviridae—the ever-growing virus family. Archives of virology. 2018;163(2):299-317. 36. Ambros V, Baltimore D. Protein is linked to the 5’end of poliovirus RNA by a phosphodiester linkage to tyrosine. Journal of Biological Chemistry. 1978;253(15):5263-5266.
37. King AM, Lefkowitz E, Adams MJ, et al. Virus taxonomy: ninth report of the International Committee on Taxonomy of Viruses. Elsevier; 2011.
38. Le Gall O, Christian P, Fauquet CM, et al. Picornavirales, a proposed order of positive-sense single-stranded RNA viruses with a pseudo-T= 3 virion architecture. Archives of virology. 2008;153(4):715. https://doi.org/10.1007/s00705-008-0041-x
39. Pelon W, Mogabgab W, Phillips I, et al. A cytopathogenic agent isolated from naval recruits with mild respiratory illnesses. Experimental Biology and Medicine. 1957;94(2):262-267. https://doi.org/10.3181/00379727-94-22915
40. Price WH. The isolation of a new virus associated with respiratory clinical disease in humans. Proceedings of the National Academy of Sciences. 1956;42(12):892-896. https://doi.org/10.1073/pnas.42.12.892
41. Kapikian A, Conant R, Hamparian V, et al. A collaborative report: rhinoviruses—extension of the numbering system. Virology. 1971;43(2):524-526.
42. Cooney M, Fox J, Kenny G. Antigenic groupings of 90 rhinovirus serotypes. Infection and immunity. 1982;37(2):642-647. https://doi.org/10.1128/iai.37.2.642-647.1982
43. Halfpap LM, Cooney MK. Isolation of rhinovirus intertypes related to either rhinoviruses 12 and 78 or 36 and 58. Infection and immunity. 1983;40(1):213-218. https://doi.org/10.1128/iai.40.1.213-218.1983
44. McIntosh K, Dees JH, Becker WB, et al. Recovery in tracheal organ cultures of novel viruses from patients with respiratory disease. Proceedings of the national academy of sciences. 1967;57(4):933-940. https://doi.org/10.1073/pnas.57.4.933
45. McIntyre CL, McWilliam Leitch EC, Savolainen-Kopra C, et al. Analysis of genetic diversity and sites of recombination in human rhinovirus species C. Journal of virology. 2010;84(19):10297-10310. https://doi.org/10.1128/jvi.00962-10
46. Van Loon A, Cleator G, Ras A. External quality assessment of enterovirus detection and typing. European Union Concerted Action on Virus Meningitis and Encephalitis. Bulletin of the World Health Organization. 1999;77(3):217. http://www.ncbi.nlm.nih.gov/pmc/articles/pmc2557629/
47. Horsnell C, Gama RE, Hughes PJ, et al. Molecular relationships between 21 human rhinovirus serotypes. Journal of general virology. 1995;76(10):2549-2555. https://doi.org/10.1099/0022-1317-76-10-2549
48. Savolainen C, Laine P, Mulders MN, et al. Sequence analysis of human rhinoviruses in the RNA-dependent RNA polymerase coding region reveals large within-species variation. Journal of general virology. 2004;85(8):2271-2277. https://doi. org/10.1099/vir.0.79897-0
49. Palmenberg AC, Spiro D, Kuzmickas R, et al. Sequencing and analyses of all known human rhinovirus genomes reveal structure and evolution. Science. 2009;324(5923):55-59. https://doi.org/10.1126/science.1165557
50. Stanway G, Kalkkinen N, Roivainen M, et al. Molecular and biological characteristics of echovirus 22, a representative of a new picornavirus group. Journal of virology. 1994;68(12):8232-8238. https://doi.org/10.1128/jvi.68.12.8232-8238.1994
51. Li Q, Yafal AG, Lee Y, et al. Poliovirus neutralization by antibodies to internal epitopes of VP4 and VP1 results from reversible exposure of these sequences at physiological temperature. Journal of virology. 1994;68(6):3965-3970. https://doi.org/10.1128/ jvi.68.6.3965-3970.1994
52. Lewis JK, Bothner B, Smith TJ, et al. Antiviral agent blocks breathing of the common cold virus. Proceedings of the National Academy of Sciences. 1998;95(12):6774-6778. https://doi.org/10.1073/pnas.95.12.6774
53. Katpally U, Fu T-M, Freed DC, et al. Antibodies to the buried N terminus of rhinovirus VP4 exhibit cross-serotypic neutralization. Journal of virology. 2009;83(14):7040-7048. https://doi.org/10.1128/jvi.00557-09
54. Hewat EA, Neumann E, Conway JF, et al. The cellular receptor to human rhinovirus 2 binds around the 5‐fold axis and not in the canyon: a structural view. The EMBO journal. 2000;19(23):6317-6325. https://doi.org/10.1093/emboj/19.23.6317
55. Colonno RJ, Condra JH, Mizutani S, et al. Evidence for the direct involvement of the rhinovirus canyon in receptor binding. Proceedings of the National Academy of Sciences. 1988;85(15):5449-5453. https://doi.org/10.1073/pnas.85.15.5449
56. Acharya R, Fry E, Stuart D, et al. The three-dimensional structure of foot-and-mouth disease virus at 2.9 Å resolution. 1989;337(6209):709-16. https://doi.org/10.1038/337709a0
57. Oliveira MA, Zhao R, Lee W-M, et al. The structure of human rhinovirus 16. Structure. 1993;1(1):51-68. https://doi. org/10.1016/0969-2126(93)90008-5
58. Verdaguer N, Blaas D, Fita I. Structure of human rhinovirus serotype 2 (HRV2). Journal of molecular biology. 2000;300(5):1179- 1194. https://doi.org/10.1006/jmbi.2000.3943
59. Smith TJ, Kremer MJ, Luo M, et al. The site of attachment in human rhinovirus 14 for antiviral agents that inhibit uncoating. Science. 1986;233:1286-1294. https://doi.org/10.1126/science.3018924
60. Spector DH, Baltimore D. Requirement of 3′-terminal poly (adenylic acid) for the infectivity of poliovirus RNA. Proceedings of the National Academy of Sciences. 1974;71(8):2983-2987. https://doi.org/10.1073/pnas.71.8.2983
61. Racaniello VR. Picornaviridae: the viruses and their replication. Fields virology. 2001;
62. Rueckert RR, Wimmer E. Systematic nomenclature of picornavirus proteins. Journal of virology. 1984;50(3):957. https://doi. org/10.1128/jvi.50.3.957-959.1984
63. Oberste MS, Maher K, Kilpatrick DR, et al. Typing of human enteroviruses by partial sequencing of VP1. Journal of clinical microbiology. 1999;37(5):1288-1293. https://doi.org/10.1128/jcm.37.5.1288-1293.1999
64. Ortega H, Nickle D, Carter L. Rhinovirus and asthma: Challenges and opportunities. Reviews in Medical Virology. 2021;31(4):e2193. https://doi.org/10.1002/rmv.2193
65. Broberg E, Niemelä J, Lahti E, et al. Human rhinovirus C—associated severe pneumonia in a neonate. Journal of Clinical Virology. 2011;51(1):79-82. https://doi.org/10.1016/j.jcv.2011.01.018
66. Hicks LA, Shepard CW, Britz PH, et al. Two outbreaks of severe respiratory disease in nursing homes associated with rhinovirus. Journal of the American Geriatrics Society. 2006;54(2):284-289. https://doi.org/10.1111/j.1532-5415.2005.00529.x
67. Jartti T, Korppi M. Rhinovirus‐induced bronchiolitis and asthma development. Pediatric Allergy and Immunology. 2011;22(4):350-355. https://doi.org/10.1111/j.1399-3038.2011.01170.x
68. Jackson DJ, Gangnon RE, Evans MD, et al. Wheezing rhinovirus illnesses in early life predict asthma development in highrisk children. American journal of respiratory and critical care medicine. 2008;178(7):667-672. https://doi.org/10.1164/ rccm.200802-309oc
69. Fendrick AM, Monto AS, Nightengale B, et al. The economic burden of non–influenza-related viral respiratory tract infection in the United States. Archives of internal medicine. 2003;163(4):487-494. https://doi.org/10.1001/archinte.163.4.487
70. Alsayed AR, El Hajji FD, Al-Najjar MA, et al. Patterns of antibiotic use, knowledge, and perceptions among different population categories: A comprehensive study based in Arabic countries. Saudi Pharmaceutical Journal. 2022;30(3):317-328. https://doi. org/10.1016/j.jsps.2022.01.013
71. Brownlee JW, Turner RB. New developments in the epidemiology and clinical spectrum of rhinovirus infections. Current opinion in pediatrics. 2008;20(1):67-71. https://doi.org/10.1097/mop.0b013e3282f41cb6
72. Gern JE. The ABCs of rhinoviruses, wheezing, and asthma. Journal of virology. 2010;84(15):7418-7426. https://doi.org/10.1128/ jvi.02290-09
73. Miller EK, Lu X, Erdman DD, et al. Rhinovirus-associated hospitalizations in young children. Journal of Infectious Diseases. 2007;195(6):773-781. https://doi.org/10.1086/511821
74. Peltola V, Waris M, Österback R, et al. Rhinovirus transmission within families with children: incidence of symptomatic and asymptomatic infections. Journal of Infectious Diseases. 2008;197(3):382-389. https://doi.org/10.1086/525542
75. Turner RB, Lee W. Rhinovirus. Clinical virology. 2009;(Ed. 3):1063-1082.
76. Alsayed AR. Illustrating How to Use the Validated Alsayed_v1 Tools to Improve Medical Care: A Particular Reference to the Global Initiative for Asthma 2022 Recommendations. Patient preference and adherence. 2023:1161-1179. https://doi. org/10.2147/ppa.s403239
77. Ko FWS, Ip M, Chan PKS, et al. A 1-year prospective study of the infectious etiology in patients hospitalized with acute exacerbations of COPD. CHEST Journal. 2007;131(1):44-52. https://doi.org/10.1378/chest.06-1355
78. Papi A, Bellettato CM, Braccioni F, et al. Infections and airway inflammation in chronic obstructive pulmonary disease severe exacerbations. American journal of respiratory and critical care medicine. 2006;173(10):1114-1121. https://doi.org/10.1164/ rccm.200506-859oc
79. Perotin JM, Dury S, Renois F, et al. Detection of multiple viral and bacterial infections in acute exacerbation of chronic obstructive pulmonary disease: a pilot prospective study. Journal of medical virology. 2013;85(5):866-873. https://doi. org/10.1002/jmv.23495
80. McManus TE, Marley A-M, Baxter N, et al. Respiratory viral infection in exacerbations of COPD. Respiratory medicine. 2008;102(11):1575-1580. https://doi.org/10.1016/j.rmed.2008.06.006
81. Kherad O, Kaiser L, Bridevaux P-O, et al. Upper-respiratory viral infection, biomarkers, and COPD exacerbations. CHEST Journal. 2010;138(4):896-904. https://doi.org/10.1378/chest.09-2225
82. Hutchinson AF, Ghimire AK, Thompson MA, et al. A community-based, time-matched, case-control study of respiratory viruses and exacerbations of COPD. Respiratory medicine. 2007;101(12):2472-2481. https://doi.org/10.1016/j.rmed.2007.07.015
83. Hewitt R, Farne H, Ritchie A, et al. The role of viral infections in exacerbations of chronic obstructive pulmonary disease and asthma. Therapeutic advances in respiratory disease. 2015;10(2):158-74. https://doi.org/10.1177/1753465815618113
84. Jackson DJ, Gangnon RE, Evans MD, et al. Wheezing rhinovirus illnesses in early life predict asthma development in highrisk children. American journal of respiratory and critical care medicine. 2008;178(7):667-72. https://doi.org/10.1164/ rccm.200802-309OC
85. Holt PG, Sly PD. Viral infections and atopy in asthma pathogenesis: new rationales for asthma prevention and treatment. Nature medicine. 2012;18(5):726-35. https://doi.org/10.1038/nm.2768
86. Lemanske RF, Jr., Jackson DJ, Gangnon RE, et al. Rhinovirus illnesses during infancy predict subsequent childhood wheezing. The Journal of allergy and clinical immunology. 2005;116(3):571-7. https://doi.org/10.1016/j.jaci.2005.06.024
87. Gern JE. Viral respiratory infection and the link to asthma. The Pediatric infectious disease journal. 2008;27(10 Suppl):S97-103. https://doi.org/10.1097/INF.0b013e318168b718
88. Alsayed AR, Hasoun L, Khader HA, et al. Co-infection of COVID-19 patients with atypical bacteria: A study based in Jordan. Pharmacy Practice. 2023;21(1):1-5. https://doi.org/10.18549/pharmpract.2023.1.2753
89. Alsayed AR, Talib W, Al-Dulaimi A, et al. The first detection of Pneumocystis jirovecii in asthmatic patients post-COVID-19 in Jordan. Bosnian Journal of Basic Medical Sciences. 2022;22(5):784. https://doi.org/10.17305/bjbms.2022.7335
90. Corne JM, Marshall C, Smith S, et al. Frequency, severity, and duration of rhinovirus infections in asthmatic and non-asthmatic individuals: a longitudinal cohort study. Lancet (London, England). 2002;359(9309):831-4. https://doi.org/10.1016/s0140- 6736(02)07953-9
91. Allakhverdi Z, Comeau MR, Jessup HK, et al. Thymic stromal lymphopoietin is released by human epithelial cells in response to microbes, trauma, or inflammation and potently activates mast cells. The Journal of experimental medicine. 2007;204(2):253- 8. https://doi.org/10.1084/jem.20062211
92. Kato A, Favoreto S, Jr., Avila PC, Schleimer RP. TLR3- and Th2 cytokine-dependent production of thymic stromal lymphopoietin in human airway epithelial cells. Journal of immunology (Baltimore, Md : 1950). 2007;179(2):1080-7. https://doi.org/10.4049/ jimmunol.179.2.1080
93. Jackson DJ, Makrinioti H, Rana BM, et al. IL-33-dependent type 2 inflammation during rhinovirus-induced asthma exacerbations in vivo. American journal of respiratory and critical care medicine. 2014;190(12):1373-82. https://doi.org/10.1164/ rccm.201406-1039OC
94. Sigurs N, Bjarnason R, Sigurbergsson F, et al. Respiratory syncytial virus bronchiolitis in infancy is an important risk factor for asthma and allergy at age 7. American journal of respiratory and critical care medicine. 2000;161(5):1501-7. https://doi. org/10.1164/ajrccm.161.5.9906076
95. Sigurs N, Gustafsson PM, Bjarnason R, et al. Severe respiratory syncytial virus bronchiolitis in infancy and asthma and allergy at age 13. American journal of respiratory and critical care medicine. 2005;171(2):137-41. https://doi.org/10.1164/rccm.200406- 730OC
96. Kusel MM, de Klerk NH, Kebadze T, et al. Early-life respiratory viral infections, atopic sensitization, and risk of subsequent development of persistent asthma. The Journal of allergy and clinical immunology. 2007;119(5):1105-10. https://doi. org/10.1016/j.jaci.2006.12.669
97. Olenec JP, Kim WK, Lee WM, et al. Weekly monitoring of children with asthma for infections and illness during common cold seasons. The Journal of allergy and clinical immunology. 2010;125(5):1001-1006.e1. https://doi.org/10.1016/j.jaci.2010.01.059
98. Edwards MR, Strong K, Cameron A, et al. Viral infections in allergy and immunology: How allergic inflammation influences viral infections and illness. The Journal of allergy and clinical immunology. 2017;140(4):909-920. https://doi.org/10.1016/j. jaci.2017.07.025
99. Bisgaard H, Hermansen MN, Bønnelykke K, et al. Association of bacteria and viruses with wheezy episodes in young children: prospective birth cohort study. BMJ (Clinical research ed). 2010;341:c4978. https://doi.org/10.1136/bmj.c4978
100. Lynch SV, Wood RA, Boushey H, et al. Effects of early-life exposure to allergens and bacteria on recurrent wheeze and atopy in urban children. The Journal of allergy and clinical immunology. 2014;134(3):593-601.e12. https://doi.org/10.1016/j. jaci.2014.04.018
101. Kloepfer KM, Lee WM, Pappas TE, et al. Detection of pathogenic bacteria during rhinovirus infection is associated with increased respiratory symptoms and asthma exacerbations. The Journal of allergy and clinical immunology. 2014;133(5):1301- 7, 1307.e1-3. https://doi.org/10.1016/j.jaci.2014.02.030
102. Kloepfer KM, Sarsani VK, Poroyko V, et al. Community-acquired rhinovirus infection is associated with changes in the airway microbiome. The Journal of allergy and clinical immunology. 2017;140(1):312-315.e8. https://doi.org/10.1016/j. jaci.2017.01.038
103. Stein RT, Sherrill D, Morgan WJ, et al. Respiratory syncytial virus in early life and risk of wheeze and allergy by age 13 years. Lancet (London, England). 1999;354(9178):541-5. https://doi.org/10.1016/s0140-6736(98)10321-5
104. Jackson DJ. The role of rhinovirus infections in the development of early childhood asthma. Current opinion in allergy and clinical immunology. 2010;10(2):133-8. https://doi.org/10.1097/ACI.0b013e3283352f7c
105. Kotaniemi-Syrjänen A, Vainionpää R, Reijonen TM, et al. Rhinovirus-induced wheezing in infancy--the first sign of childhood asthma? The Journal of allergy and clinical immunology. 2003;111(1):66-71. https://doi.org/10.1067/mai.2003.33
106. ly PD, Kusel M, Holt PG. Do early-life viral infections cause asthma? The Journal of allergy and clinical immunology. 2010;125(6):1202-5. https://doi.org/10.1016/j.jaci.2010.01.024
107. Rantala AK, Jaakkola MS, Mäkikyrö EM, et al. Early Respiratory Infections and the Development of Asthma in the First 27 Years of Life. American journal of epidemiology. 2015;182(7):615-23. https://doi.org/10.1093/aje/kwv093
108. Rosenthal LA, Avila PC, Heymann PW, et al. Viral respiratory tract infections and asthma: the course ahead. The Journal of allergy and clinical immunology. 2010;125(6):1212-7. https://doi.org/10.1016/j.jaci.2010.04.002
109. Wu P, Dupont WD, Griffin MR, et al. Evidence of a causal role of winter virus infection during infancy in early childhood asthma. American journal of respiratory and critical care medicine. 2008;178(11):1123-9. https://doi.org/10.1164/rccm.200804-579OC
110. Bartlett NW, McLean GR, Chang YS, et al. Genetics and epidemiology: asthma and infection. Current opinion in allergy and clinical immunology. 2009;9(5):395-400. https://doi.org/10.1097/ACI.0b013e32833066fa
111. Gern JE. Rhinovirus and the initiation of asthma. Current opinion in allergy and clinical immunology. 2009;9(1):73-8. https:// doi.org/10.1097/ACI.0b013e32831f8f1b
112. Sigurs N, Aljassim F, Kjellman B, et al. Asthma and allergy patterns over 18 years after severe RSV bronchiolitis in the first year of life. Thorax. 2010;65(12):1045-52. https://doi.org/10.1136/thx.2009.121582
113. Simões EA, Carbonell-Estrany X, Rieger CH, et al. The effect of respiratory syncytial virus on subsequent recurrent wheezing in atopic and nonatopic children. The Journal of allergy and clinical immunology. 2010;126(2):256-62. https://doi.org/10.1016/j. jaci.2010.05.026
114. Martinez FD, Morgan WJ, Wright AL, et al. Diminished lung function as a predisposing factor for wheezing respiratory illness in infants. The New England journal of medicine. 1988;319(17):1112-7. https://doi.org/10.1056/nejm198810273191702
115. Martinez FD, Wright AL, Taussig LM, et al. Asthma and wheezing in the first six years of life. The Group Health Medical Associates. The New England journal of medicine. 1995;332(3):133-8. https://doi.org/10.1056/nejm199501193320301
116. Pattemore PK, Johnston SL, Bardin PG. Viruses as precipitants of asthma symptoms. I. Epidemiology. Clinical and experimental allergy : journal of the British Society for Allergy and Clinical Immunology. 1992;22(3):325-36. https://doi. org/10.1111/j.1365-2222.1992.tb03094.x
117. Shaheen SO. Changing patterns of childhood infection and the rise in allergic disease. Clinical and experimental allergy : journal of the British Society for Allergy and Clinical Immunology. 1995;25(11):1034-7. https://doi.org/10.1111/j.1365-2222.1995. tb03248.x
118. Sigurs N, Bjarnason R, Sigurbergsson F, et al. Asthma and immunoglobulin E antibodies after respiratory syncytial virus bronchiolitis: a prospective cohort study with matched controls. Pediatrics. 1995;95(4):500-5.
119. Cogswell JJ, Halliday DF, Alexander JR. Respiratory infections in the first year of life in children at risk of developing atopy. British medical journal (Clinical research ed). 1982;284(6321):1011-3. https://doi.org/10.1136/bmj.284.6321.1011
120. Welliver RC. RSV and chronic asthma. Lancet (London, England). 1995;346(8978):789-90. https://doi.org/10.1016/s0140- 6736(95)91615-6
121. Bacharier LB, Cohen R, Schweiger T, et al. Determinants of asthma after severe respiratory syncytial virus bronchiolitis. The Journal of allergy and clinical immunology. 2012;130(1):91-100.e3. https://doi.org/10.1016/j.jaci.2012.02.010
122. Jartti T, Kuusipalo H, Vuorinen T, et al. Allergic sensitization is associated with rhinovirus-, but not other virus-, induced wheezing in children. Pediatric allergy and immunology : official publication of the European Society of Pediatric Allergy and Immunology. 2010;21(7):1008-14. https://doi.org/10.1111/j.1399-3038.2010.01059.x
123. Gern JE, Vrtis R, Grindle KA, et al. Relationship of upper and lower airway cytokines to outcome of experimental rhinovirus infection. American journal of respiratory and critical care medicine. 2000;162(6):2226-31. https://doi.org/10.1164/ ajrccm.162.6.2003019
124. GINA. Global Initiative for Asthma, Global Strategy for Asthma Management and Prevention. 2023. http: //www.gi-nasthma. org
125. Vincenzo SD, Ferrante G, Ferraro M, et al. Oxidative Stress, Environmental Pollution, and Lifestyle as Determinants of Asthma in Children. Biology. 2023;12(1):133. https://doi.org/10.3390/biology12010133
126. Nakagome K, Nagata M. Innate immune responses by respiratory viruses, including rhinovirus, during asthma exacerbation. Frontiers in immunology. 2022;13:865973. https://doi.org/10.3389/fimmu.2022.865973
127. Dinwiddie DL, Kaukis N, Pham S, et al. Viral infection and allergy status impact severity of asthma symptoms in children with asthma exacerbations. Annals of Allergy, Asthma & Immunology. 2022;129(3):319-326. e3. https://doi.org/10.1016/j. anai.2022.06.017
128. Kim SR. Viral infection and airway epithelial immunity in asthma. International Journal of Molecular Sciences. 2022;23(17):9914. https://doi.org/10.3390/ijms23179914
129. Ramphul M. Increased inhaled corticosteroids for treating acute asthma exacerbations. Wiley Online Library; 2023. p. 388- 391. https://doi.org/10.1111/cea.14306
130. McDowell PJ, Busby J, Heaney LG. Asthma Exacerbations in Severe Asthma: Why Systemic Corticosteroids May not Always Be the Best Treatment Option. Current Treatment Options in Allergy. 2023;10(1):53-63.
131. Bagnasco D, Testino E, Nicola S, et al. Specific Therapy for T2 Asthma. Journal of Personalized Medicine. 2022;12(4):593. https://doi.org/10.3390/jpm12040593
132. Blanken MO, Rovers MM, Molenaar JM, et al. Respiratory syncytial virus and recurrent wheeze in healthy preterm infants. The New England journal of medicine. 2013;368(19):1791-9. https://doi.org/10.1056/NEJMoa1211917
133. Scheltema NM, Nibbelke EE, Pouw J, et al. Respiratory syncytial virus prevention and asthma in healthy preterm infants: a randomised controlled trial. The Lancet Respiratory medicine. 2018;6(4):257-264. https://doi.org/10.1016/s2213- 2600(18)30055-9
134. Holt PG, Strickland DH, Hales BJ, et al. Defective respiratory tract immune surveillance in asthma: a primary causal factor in disease onset and progression. Chest. 2014;145(2):370-378. https://doi.org/10.1378/chest.13-1341
135. Durrani SR, Montville DJ, Pratt AS, et al. Innate immune responses to rhinovirus are reduced by the high-affinity IgE receptor in allergic asthmatic children. The Journal of allergy and clinical immunology. 2012;130(2):489-95. https://doi.org/10.1016/j. jaci.2012.05.023
136. Gill MA, Bajwa G, George TA, et al. Counterregulation between the FcepsilonRI pathway and antiviral responses in human plasmacytoid dendritic cells. Journal of immunology (Baltimore, Md : 1950). 2010;184(11):5999-6006. https://doi.org/10.4049/ jimmunol.0901194
137. Teach SJ, Gill MA, Togias A, et al. Preseasonal treatment with either omalizumab or an inhaled corticosteroid boost to prevent fall asthma exacerbations. The Journal of allergy and clinical immunology. 2015;136(6):1476-1485. https://doi.org/10.1016/j. jaci.2015.09.008
138. Esquivel A, Busse WW, Calatroni A, et al. Effects of omalizumab on rhinovirus infections, illnesses, and exacerbations of asthma. American journal of respiratory and critical care medicine. 2017;196(8):985-992. https://doi.org/10.1164/rccm.201701- 0120oc
139. Teach SJ, Gill MA, Togias A, et al. Preseasonal treatment with either omalizumab or an inhaled corticosteroid boost to prevent fall asthma exacerbations. Journal of Allergy and Clinical Immunology. 2015;136(6):1476-1485. https://doi.org/10.1016/j. jaci.2015.09.008
140. Fu Z, Xu Y, Cai C. Efficacy and safety of omalizumab in children with moderate-to-severe asthma: a meta-analysis. Journal of Asthma. 2021;58(10):1350-1358. https://doi.org/10.1080/02770903.2020.1789875
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Human Rhinovirus: Molecular and Clinical Overview. Pharm Pract (Granada) [Internet]. 2024 Mar. 6 [cited 2025 Jan. 21];22(1):1-11. Available from: https://pharmacypractice.org/index.php/pp/article/view/2925
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Human Rhinovirus: Molecular and Clinical Overview. Pharm Pract (Granada) [Internet]. 2024 Mar. 6 [cited 2025 Jan. 21];22(1):1-11. Available from: https://pharmacypractice.org/index.php/pp/article/view/2925