The interdependencies of viral load, the innate immune response, and clinical outcome in children presenting to the emergency department with respiratory syncytial virus-Associated bronchiolitis

PLoS ONE

Volumn 12, Issue 3, 2017, Pages

  Piedra, Felipe Andrés ^a   Mei, Minghua ^d   Avadhanula, Vasanthi ^a   Mehta, Reena ^b   Aideyan, Letisha ^a   Garofalo, Roberto P ^c   Piedra, Pedro A ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b Allergy Asthma Specialists   (United States)

^c University of Texas Medical Branch School of Medicine   (United States)

^d ELI LILLY AND COMPANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EOTAXIN; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GUANINE NUCLEOTIDE BINDING PROTEIN; INTERLEUKIN 15; INTERLEUKIN 17; INTERLEUKIN 4; NONSTRUCTURAL PROTEIN 1; NONSTRUCTURAL PROTEIN 2; RIBONUCLEASE P; AUTACOID; CYTOKINE;

ARTICLE; CHILD; CONTROLLED STUDY; EMERGENCY WARD; F GENE; FEMALE; G GENE; GENE DOSAGE; HUMAN; HUMAN RESPIRATORY SYNCYTIAL VIRUS; INFANT; INNATE IMMUNITY; MAJOR CLINICAL STUDY; MALE; N GENE; NEWBORN; NONHUMAN; NS1 GENE; NS2 GENE; OUTCOME ASSESSMENT; OXYGEN SATURATION; PULSE OXIMETRY; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RNASE P GENE; VIRAL BRONCHIOLITIS; VIRUS CELL INTERACTION; VIRUS GENE; VIRUS LOAD; BRONCHIOLITIS; HOSPITAL EMERGENCY SERVICE; HOSPITALIZATION; IMMUNOLOGY; METABOLISM; PRESCHOOL CHILD; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RISK FACTOR; VIROLOGY;

BRONCHIOLITIS; CHILD, PRESCHOOL; CYTOKINES; EMERGENCY SERVICE, HOSPITAL; FEMALE; HOSPITALIZATION; HUMANS; IMMUNITY, INNATE; INFANT; INFANT, NEWBORN; INFLAMMATION MEDIATORS; MALE; PATIENT OUTCOME ASSESSMENT; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUS, HUMAN; RISK FACTORS; VIRAL LOAD;

EID: 85014768057     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0172953     Document Type: Article

References (46)

1. American Academy of Pediatrics Subcommittee on D, Management of B. Diagnosis and management of bronchiolitis. Pediatrics. 2006; 118(4):1774-93. doi:10.1542/peds.2006-2223 PMID: 17015575.
2. Hasegawa K, Tsugawa Y, Brown DF, Mansbach JM, Camargo CA Jr. Temporal trends in emergency department visits for bronchiolitis in the United States, 2006 to 2010. Pediatr Infect Dis J. 2014; 33 (1):11-8. doi:10.1097/INF.0b013e3182a5f324 PMID: 23934206.
3. Mansbach JM, Piedra PA, Teach SJ, Sullivan AF, Forgey T, Clark S, et al. Prospective multicenter study of viral etiology and hospital length of stay in children with severe bronchiolitis. Arch Pediatr Adolesc Med. 2012; 166(8):700-6. doi:10.1001/archpediatrics.2011.1669PMID: 22473882.
4. Nair H, Nokes DJ, Gessner BD, Dherani M, Madhi SA, Singleton RJ, et al. Global burden of acute lower respiratory infections due to respiratory syncytial virus in young children: A systematic review and metaanalysis. Lancet. 2010; 375(9725):1545-55. doi:10.1016/S0140-6736(10)60206-1 PMID: 20399493.
5. Zorc JJ, Hall CB. Bronchiolitis: Recent evidence on diagnosis and management. Pediatrics. 2010; 125 (2):342-9. doi:10.1542/peds.2009-2092 PMID: 20100768.
6. Fulginiti VA, Eller JJ, Sieber OF, Joyner JW, Minamitani M, Meiklejohn G. Respiratory virus immunization. I. A field trial of two inactivated respiratory virus vaccines; an aqueous trivalent parainfluenza virus vaccine and an alum-precipitated respiratory syncytial virus vaccine. Am J Epidemiol. 1969; 89(4):435- 48. PMID: 4305199.
7. Graham BS, Johnson TR, Peebles RS. Immune-mediated disease pathogenesis in respiratory syncytial virus infection. Immunopharmacology. 2000; 48(3):237-47. PMID: 10960663.
8. Johnson KM, Chanock RM, Rifkind D, Kravetz HM, Knight V. Respiratory syncytial virus. IV. Correlation of virus shedding, serologic response, and illness in adult volunteers. JAMA. 1961; 176:663-7. PMID: 13790307.
9. Kapikian AZ, Mitchell RH, Chanock RM, Shvedoff RA, Stewart CE. An epidemiologic study of altered clinical reactivity to respiratory syncytial (RS) virus infection in children previously vaccinated with an inactivated RS virus vaccine. Am J Epidemiol. 1969; 89(4):405-21. PMID: 4305197.
10. Openshaw PJ, Tregoning JS. Immune responses and disease enhancement during respiratory syncytial virus infection. Clin Microbiol Rev. 2005; 18(3):541-55. doi:10.1128/CMR.18.3.541-555.2005 PMID: 16020689.
11. Polack FP, Teng MN, Collins PL, Prince GA, Exner M, Regele H, et al. A role for immune complexes in enhanced respiratory syncytial virus disease. J Exp Med. 2002; 196(6):859-65. doi:10.1084/jem.20020781 PMID: 12235218.
12. Tripp RA. Pathogenesis of respiratory syncytial virus infection. Viral Immunol. 2004; 17(2):165-81. doi:10.1089/0882824041310513 PMID: 15279697.
13. Bennett BL, Garofalo RP, Cron SG, Hosakote YM, Atmar RL, Macias CG, et al. Immunopathogenesis of respiratory syncytial virus bronchiolitis. J Infect Dis. 2007; 195(10):1532-40. doi:10.1086/515575PMID: 17436234.
14. Laham FR, Israele V, Casellas JM, Garcia AM, Lac Prugent CM, Hoffman SJ, et al. Differential production of inflammatory cytokines in primary infection with human metapneumovirus and with other common respiratory viruses of infancy. J Infect Dis. 2004; 189(11):2047-56. doi:10.1086/383350 PMID: 15143472.
15. Mehta R, Scheffler M, Tapia L, Aideyan L, Patel KD, Jewell AM, et al. Lactate dehydrogenase and caspase activity in nasopharyngeal secretions are predictors of bronchiolitis severity. Influenza Other Respir Viruses. 2014; 8(6):617-25. doi:10.1111/irv.12276 PMID: 25132512.
16. Nicholson EG, Schlegel C, Garofalo RP, Mehta R, Scheffler M, Mei M, et al. A Robust Cytokine and Chemokine Response in Nasopharyngeal Secretions is Associated with Decreased Severity in Children with Physician Diagnosed Bronchiolitis. J Infect Dis. 2016.
17. Hasegawa K, Jartti T, Mansbach JM, Laham FR, Jewell AM, Espinola JA, et al. Respiratory syncytial virus genomic load and disease severity among children hospitalized with bronchiolitis: multicenter cohort studies in the United States and Finland. J Infect Dis. 2015; 211(10):1550-9. doi:10.1093/infdis/jiu658PMID: 25425699.
18. De Vincenzo JP, Wilkinson T, Vaishnaw A, Cehelsky J, Meyers R, Nochur S, et al. Viral load drives disease in humans experimentally infected with respiratory syncytial virus. Am J Respir Crit Care Med. 2010; 182(10):1305-14. doi:10.1164/rccm.201002-0221OCPMID: 20622030.
19. Houben ML, Coenjaerts FE, Rossen JW, Belderbos ME, Hofland RW, Kimpen JL, et al. Disease severity and viral load are correlated in infants with primary respiratory syncytial virus infection in the community. J Med Virol. 2010; 82(7):1266-71. doi:10.1002/jmv.21771PMID: 20513094.
20. Buckingham SC, Bush AJ, Devincenzo JP. Nasal quantity of respiratory syncytical virus correlates with disease severity in hospitalized infants. Pediatr Infect Dis J. 2000; 19(2):113-7. PMID: 10693996.
21. De Vincenzo JP, El Saleeby CM, Bush AJ. Respiratory syncytial virus load predicts disease severity in previously healthy infants. J Infect Dis. 2005; 191(11):1861-8. doi:10.1086/430008 PMID: 15871119.
22. Fodha I, Vabret A, Ghedira L, Seboui H, Chouchane S, Dewar J, et al. Respiratory syncytial virus infections in hospitalized infants: Association between viral load, virus subgroup, and disease severity. J Med Virol. 2007; 79(12):1951-8. doi:10.1002/jmv.21026PMID: 17935185.
23. Scagnolari C, Midulla F, Selvaggi C, Monteleone K, Bonci E, Papoff P, et al. Evaluation of viral load in infants hospitalized with bronchiolitis caused by respiratory syncytial virus. Med Microbiol Immunol. 2012; 201(3):311-7. doi:10.1007/s00430-012-0233-6 PMID: 22406873.
24. Legg JP, Hussain IR, Warner JA, Johnston SL, Warner JO. Type 1 and type 2 cytokine imbalance in acute respiratory syncytial virus bronchiolitis. Am J Respir Crit Care Med. 2003; 168(6):633-9. doi:10.1164/rccm.200210-1148OC PMID: 12773328.
25. Wright PF, Gruber WC, Peters M, Reed G, Zhu Y, Robinson F, et al. Illness severity, viral shedding, and antibody responses in infants hospitalized with bronchiolitis caused by respiratory syncytial virus. J Infect Dis. 2002; 185(8):1011-8. doi:10.1086/339822PMID: 11930309.
26. Fuller JA, Njenga MK, Bigogo G, Aura B, Ope MO, Nderitu L, et al. Association of the CT values of realtime PCR of viral upper respiratory tract infection with clinical severity, Kenya. J Med Virol. 2013; 85 (5):924-32. doi:10.1002/jmv.23455 PMID: 23508918.
27. Spann KM, Tran KC, Chi B, Rabin RL, Collins PL. Suppression of the induction of alpha, beta, and lambda interferons by the NS1 and NS2 proteins of human respiratory syncytial virus in human epithelial cells and macrophages [corrected]. J Virol. 2004; 78(8):4363-9. doi:10.1128/JVI.78.8.4363-4369.2004 PMID: 15047850.
28. Swedan S, Musiyenko A, Barik S. Respiratory syncytial virus nonstructural proteins decrease levels of multiple members of the cellular interferon pathways. J Virol. 2009; 83(19):9682-93. doi:10.1128/JVI.00715-09 PMID: 19625398.
29. Yang P, Zheng J, Wang S, Liu P, Xie M, Zhao D. Respiratory syncytial virus nonstructural proteins 1 and 2 are crucial pathogenic factors that modulate interferon signaling and Treg cell distribution in mice. Virology. 2015; 485:223-32. doi:10.1016/j.virol.2015.07.016 PMID: 26298859.
30. Zheng J, Yang P, Tang Y, Pan Z, Zhao D. Respiratory Syncytial Virus Nonstructural Proteins Upregulate SOCS1 and SOCS3 in the Different Manner from Endogenous IFN Signaling. J Immunol Res. 2015; 2015:738547. doi:10.1155/2015/738547 PMID: 26557722.
31. Bukreyev A, Yang L, Collins PL. The secreted G protein of human respiratory syncytial virus antagonizes antibody-mediated restriction of replication involving macrophages and complement. J Virol. 2012; 86(19):10880-4. doi:10.1128/JVI.01162-12 PMID: 22837211.
32. Bukreyev A, Yang L, Fricke J, Cheng L, Ward JM, Murphy BR, et al. The secreted form of respiratory syncytial virus G glycoprotein helps the virus evade antibody-mediated restriction of replication by acting as an antigen decoy and through effects on Fc receptor-bearing leukocytes. J Virol. 2008; 82 (24):12191-204. doi:10.1128/JVI.01604-08 PMID: 18842713.
33. McLellan JS, Ray WC, Peeples ME. Structure and function of respiratory syncytial virus surface glycoproteins. Curr Top Microbiol Immunol. 2013; 372:83-104. doi:10.1007/978-3-642-38919-1-4PMID: 24362685.
34. Chirkova T, Boyoglu-Barnum S, Gaston KA, Malik FM, Trau SP, Oomens AG, et al. Respiratory syncytial virus G protein CX3C motif impairs human airway epithelial and immune cell responses. J Virol. 2013; 87(24):13466-79. doi:10.1128/JVI.01741-13 PMID: 24089561.
35. Harcourt JL, Karron RA, Tripp RA. Anti-G protein antibody responses to respiratory syncytial virus infection or vaccination are associated with inhibition of G protein CX3C-CX3CR1 binding and leukocyte chemotaxis. J Infect Dis. 2004; 190(11):1936-40. doi:10.1086/425516PMID: 15529257.
36. Collins PL, Melero JA. Progress in understanding and controlling respiratory syncytial virus: still crazy after all these years. Virus Res. 2011; 162(1-2):80-99. doi:10.1016/j.virusres.2011.09.020PMID: 21963675.
37. Yokota S, Okabayashi T, Fujii N. The battle between virus and host: modulation of Toll-like receptor signaling pathways by virus infection. Mediators Inflamm. 2010; 2010:184328. doi:10.1155/2010/184328 PMID: 20672047.
38. Krathwohl MD, Anderson JL. Chemokine CXCL10 (IP-10) is sufficient to trigger an immune response to injected antigens in a mouse model. Vaccine. 2006; 24(15):2987-93. doi:10.1016/j.vaccine.2005.11.032 PMID: 16500735.
39. Sun Y, Jain D, Koziol-White CJ, Genoyer E, Gilbert M, Tapia K, et al. Immunostimulatory Defective Viral Genomes from Respiratory Syncytial Virus Promote a Strong Innate Antiviral Response during Infection in Mice and Humans. PLoS Pathog. 2015; 11(9):e1005122. doi:10.1371/journal.ppat.1005122 PMID: 26336095.
40. Lopez CB. Defective viral genomes: critical danger signals of viral infections. J Virol. 2014; 88 (16):8720-3. doi:10.1128/JVI.00707-14 PMID: 24872580.
41. Pathak KB, Nagy PD. Defective Interfering RNAs: Foes of Viruses and Friends of Virologists. Viruses. 2009; 1(3):895-919. doi:10.3390/v1030895 PMID: 21994575.
42. Laham FR, Trott AA, Bennett BL, Kozinetz CA, Jewell AM, Garofalo RP, et al. LDH concentration in nasal-wash fluid as a biochemical predictor of bronchiolitis severity. Pediatrics. 2010; 125(2): 225-33. doi:10.1542/peds.2009-0411 PMID: 20100751.
43. Avadhanula V, Chemaly RF, Shah DP, Ghantoji SS, Azzi JM, Aideyan LO, et al. Infection with novel respiratory syncytial virus genotype Ontario (ON1) in adult hematopoietic cell transplant recipients, Texas, 2011-2013. J Infect Dis. 2015; 211(4):582-9. doi:10.1093/infdis/jiu473 PMID: 25156562.
44. Peret TC, Hall CB, Schnabel KC, Golub JA, Anderson LJ. Circulation patterns of genetically distinct group A and B strains of human respiratory syncytial virus in a community. J Gen Virol. 1998; 79 (Pt 9):2221-9.
45. Tapia LI, Shaw CA, Aideyan LO, Jewell AM, Dawson BC, Haq TR, et al. Gene sequence variability of the three surface proteins of human respiratory syncytial virus (HRSV) in Texas. PLoS One. 2014; 9(3): E90786. doi:10.1371/journal.pone.0090786 PMID: 24625544.
46. Data Analysis on the ABI PRISM® 7700 Sequence Detection System: Setting Baselines and Thresholds. 2002.