Seasonal H3N2 influenza A virus fails to enhance Staphylococcus aureus co-infection in a non-human primate respiratory tract infection model

Virulence

Volumn 4, Issue 8, 2013, Pages 707-715

  Kobayashi, Scott D ^a   Olsen, Randall J ^b,c   LaCasse, Rachel A ^a   Safronetz, David ^a   Ashraf, Madiha ^b,c   Porter, Adeline R ^a   Braughton, Kevin R ^a   Feldmann, Friederike ^a   Clifton, Dawn R ^a   Kash, John C ^d   Bailey, John R ^a   Gardner, Donald J ^a   Otto, Michael ^a   Brining, Douglas L ^a   Kreiswirth, Barry N ^e   Taubenberger, Jeffrey K ^d   Parnell, Michael J ^a   Feldmann, Heinz ^a   Musser, James M ^b,c   DeLeo, Frank R ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

^c HOUSTON METHODIST HOSPITAL   (United States)

^d NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^e PUBLIC HEALTH RESEARCH INSTITUTE   (United States)

Author keywords

Coinfection; Influenza a virus; MRSA; Pneumonia; Staphylococcus aureus; USA300

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CLINICAL ASSESSMENT; COMORBIDITY; CONTROLLED STUDY; DISEASE COURSE; DISEASE PREDISPOSITION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HISTOPATHOLOGY; INCIDENCE; INFLUENZA A (H3N2); INFLUENZA VIRUS A H3N2; MACAQUE MODEL; MALE; MIXED INFECTION; MORBIDITY; MORTALITY; NONHUMAN; PLAQUE FORMING CELL; RADIOGRAPHY; REAL TIME POLYMERASE CHAIN REACTION; RESPIRATORY TRACT INFECTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STAPHYLOCOCCAL PNEUMONIA; STAPHYLOCOCCUS INFECTION; VIRUS DETECTION; ANIMAL; DISEASE MODEL; GROWTH, DEVELOPMENT AND AGING; HUMAN; INFLUENZA VIRUS A; LUNG; MACACA FASCICULARIS; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIOLOGY; ORGANISMAL INTERACTION; ORTHOMYXOVIRUS INFECTION; PATHOLOGY; PNEUMONIA; STAPHYLOCOCCUS AUREUS; USA300; VIROLOGY;

ANIMALIA; BACTERIA (MICROORGANISMS); INFLUENZA A VIRUS; MACACA; MACACA FASCICULARIS; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; PRIMATES; STAPHYLOCOCCUS AUREUS;

COINFECTION; INFLUENZA A VIRUS; MRSA; PNEUMONIA; STAPHYLOCOCCUS AUREUS; USA300;

ANIMALS; COINFECTION; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; INFLUENZA A VIRUS, H3N2 SUBTYPE; LUNG; MACACA FASCICULARIS; MALE; MICROBIAL INTERACTIONS; ORTHOMYXOVIRIDAE INFECTIONS; PNEUMONIA, STAPHYLOCOCCAL; STAPHYLOCOCCUS AUREUS;

EID: 84888352324     PISSN: 21505594     EISSN: 21505608     Source Type: Journal    
DOI: 10.4161/viru.26572     Document Type: Article

References (51)

1. Kochanek KD, Kirmeyer SE, Martin JA, Strobino DM, Guyer B. Annual summary of vital statistics: 2009. Pediatrics 2012; 129:338-48. PMID:22291121; http://dx.doi.org/10.1542/peds.2011-3435
2. Morens DM, Taubenberger JK, Fauci AS. Predominant role of bacterial pneumonia as a cause of death in pandemic influenza: implications for pandemic influenza preparedness. J Infect Dis 2008; 198:962-70. PMID:18710327; http://dx.doi.org/10.1086/591708
3. Schwarzmann SW, Adler JL, Sullivan RJ Jr., Marine WM. Bacterial pneumonia during the Hong Kong influenza epidemic of 1968-1969. Arch Intern Med 1971; 127:1037-41. PMID:5578560; http://dx.doi.org/10.1001/archinte.127.6.1037
4. Robertson L, Caley JP, Moore J. Importance of Staphylococcus aureus in pneumonia in the 1957 epidemic of influenza A. Lancet 1958; 2:233-6. PMID:13564806; http://dx.doi.org/10.1016/S0140-6736(58)90060-6
5. Finland M, Peterson OL, Strauss E. Staphylococcic pneumonia occurring during an epidemic of influenza. Arch Intern Med 1942; 70:183-205. http://dx.doi.org/10.1001/archinte.1942.00200200003001
6. Chickering HT, Park JH. Staphylococcus aureus pneumonia. J Am Med Assoc 1919; 72:617-26. http://dx.doi.org/10.1001/jama.1919.02610090001001
7. Centers for Disease Control and Prevention (CDC). Bacterial coinfections in lung tissue specimens from fatal cases of 2009 pandemic influenza A (H1N1)-United States, May-August 2009. MMWR Morb Mortal Wkly Rep 2009; 58:1071-4. PMID:19798021
8. Hageman JC, Uyeki TM, Francis JS, Jernigan DB, Wheeler JG, Bridges CB, Barenkamp SJ, Sievert DM, Srinivasan A, Doherty MC, et al. Severe community-acquired pneumonia due to Staphylococcus aureus, 2003-04 influenza season. Emerg Infect Dis 2006; 12:894-9. PMID:16707043; http://dx.doi.org/10.3201/eid1206.051141
9. Kallen AJ, Brunkard J, Moore Z, Budge P, Arnold KE, Fosheim G, Finelli L, Beekmann SE, Polgreen PM, Gorwitz R, et al. Staphylococcus aureus community-acquired pneumonia during the 2006 to 2007 influenza season. Ann Emerg Med 2009; 53:358-65. PMID:18534715; http://dx.doi.org/10.1016/j. annemergmed.2008.04.027
10. Finelli L, Fiore A, Dhara R, Brammer L, Shay DK, Kamimoto L, Fry A, Hageman J, Gorwitz R, Bresee J, et al. Influenza-associated pediatric mortality in the United States: increase of Staphylococcus aureus coinfection. Pediatrics 2008; 122:805-11. PMID:18829805; http://dx.doi.org/10.1542/peds.2008-1336
11. Diep BA, Gill SR, Chang RF, Phan TH, Chen JH, Davidson MG, Lin F, Lin J, Carleton HA, Mongodin EF, et al. Complete genome sequence of USA300, an epidemic clone of community-acquired meticillinresistant Staphylococcus aureus. Lancet 2006; 367:731-9. PMID:16517273; http://dx.doi.org/10.1016/S0140-6736(06)68231-7
12. Moran GJ, Krishnadasan A, Gorwitz RJ, Fosheim GE, McDougal LK, Carey RB, Talan DA; EMERGEncy ID Net Study Group. Methicillinresistant S. aureus infections among patients in the emergency department. N Engl J Med 2006; 355:666-74. PMID:16914702; http://dx.doi. org/10.1056/NEJMoa055356
13. Kennedy AD, Otto M, Braughton KR, Whitney AR, Chen L, Mathema B, Mediavilla JR, Byrne KA, Parkins LD, Tenover FC, et al. Epidemic communityassociated methicillin-resistant Staphylococcus aureus: recent clonal expansion and diversification. Proc Natl Acad Sci U S A 2008; 105:1327-32. PMID:18216255; http://dx.doi.org/10.1073/pnas.0710217105
14. Verlinde JD, Makstenieks O. Experimental respiratory infection in monkeys produced by influenza A virus and Staphylococcus aureus. Arch Gesamte Virusforsch 1954; 5:345-60. PMID:13171853; http://dx.doi.org/10.1007/BF01243004
15. Kobasa D, Jones SM, Shinya K, Kash JC, Copps J, Ebihara H, Hatta Y, Kim JH, Halfmann P, Hatta M, et al. Aberrant innate immune response in lethal infection of macaques with the 1918 influenza virus. Nature 2007; 445:319-23. PMID:17230189; http://dx.doi.org/10.1038/nature05495
16. Olsen RJ, Kobayashi SD, Ayeras AA, Ashraf M, Graves SF, Ragasa W, Humbird T, Greaver JL, Cantu C, Swain JL, et al. Lack of a major role of Staphylococcus aureus Panton-Valentine leukocidin in lower respiratory tract infection in nonhuman primates. Am J Pathol 2010; 176:1346-54. PMID:20093487; http://dx.doi.org/10.2353/ajpath.2010.090960
17. Ohara-Nemoto Y, Haraga H, Kimura S, Nemoto TK. Occurrence of staphylococci in the oral cavities of healthy adults and nasal oral trafficking of the bacteria. J Med Microbiol 2008; 57:95-9. PMID:18065673; http://dx.doi.org/10.1099/jmm.0.47561-0
18. Rimmelzwaan GF, Baars M, van Beek R, van Amerongen G, Lövgren-Bengtsson K, Claas EC, Osterhaus AD. Induction of protective immunity against influenza virus in a macaque model: comparison of conventional and iscom vaccines. J Gen Virol 1997; 78:757-65. PMID:9129647
19. Brining DL, Mattoon JS, Kercher L, LaCasse RA, Safronetz D, Feldmann H, Parnell MJ. Thoracic radiography as a refinement methodology for the study of H1N1 influenza in cynomologus macaques (Macaca fascicularis). Comp Med 2010; 60:389-95. PMID:21262125
20. Chertow DS, Memoli MJ. Bacterial coinfection in influenza: a grand rounds review. JAMA 2013; 309:275-82. PMID:23321766; http://dx.doi.org/10.1001/jama.2012.194139
21. Gorwitz RJ, Kruszon-Moran D, McAllister SK, McQuillan G, McDougal LK, Fosheim GE, Jensen BJ, Killgore G, Tenover FC, Kuehnert MJ. Changes in the prevalence of nasal colonization with Staphylococcus aureus in the United States, 2001-2004. J Infect Dis 2008; 197:1226-34. PMID:18422434; http://dx.doi.org/10.1086/533494
22. Goslings WR, Mulder J, Djajadiningrat J, Masurel N. Staphylococcal pneumonia in influenza in relation to antecedent staphylococcal skin infection. Lancet 1959; 2:428-30. PMID:13851372; http://dx.doi.org/10.1016/S0140-6736(59)90417-9
23. Moran GJ, Krishnadasan A, Gorwitz RJ, Fosheim GE, Albrecht V, Limbago B, Talan DA; EMERGEncy ID NET Study Group. Prevalence of methicillinresistant staphylococcus aureus as an etiology of community-acquired pneumonia. Clin Infect Dis 2012; 54:1126-33. PMID:22438343; http://dx.doi.org/10.1093/cid/cis022
24. Murray RJ, Robinson JO, White JN, Hughes F, Coombs GW, Pearson JC, Tan HL, Chidlow G, Williams S, Christiansen KJ, et al. Communityacquired pneumonia due to pandemic A(H1N1)2009 influenzavirus and methicillin resistant Staphylococcus aureus co-infection. PLoS One 2010; 5:e8705. PMID:20090931; http://dx.doi.org/10.1371/journal.pone.0008705
25. Fridkin SK, Hageman JC, Morrison M, Sanza LT, Como-Sabetti K, Jernigan JA, Harriman K, Harrison LH, Lynfield R, Farley MM; Active Bacterial Core Surveillance Program of the Emerging Infections Program Network. Methicillin-resistant Staphylococcus aureus disease in three communities. N Engl J Med 2005; 352:1436-44. PMID:15814879; http://dx.doi.org/10.1056/NEJMoa043252
26. Lee MH, Arrecubieta C, Martin FJ, Prince A, Borczuk AC, Lowy FD. A postinfluenza model of Staphylococcus aureus pneumonia. J Infect Dis 2010; 201:508-15. PMID:20078212; http://dx.doi.org/10.1086/650204
27. Weeks-Gorospe JN, Hurtig HR, Iverson AR, Schuneman MJ, Webby RJ, McCullers JA, Huber VC. Naturally occurring swine influenza A virus PB1-F2 phenotypes that contribute to superinfection with Gram-positive respiratory pathogens. J Virol 2012; 86:9035-43. PMID:22674997; http://dx.doi.org/10.1128/JVI.00369-12
28. Iverson AR, Boyd KL, McAuley JL, Plano LR, Hart ME, McCullers JA. Influenza virus primes mice for pneumonia from Staphylococcus aureus. J Infect Dis 2011; 203:880-8. PMID:21278211; http://dx.doi.org/10.1093/infdis/jiq113
29. Sellers TF Jr., Schulman J, Bouvier C, McCUNE R, Kilbourne ED. The influence of influenza virus infection on exogenous staphylococcal and endogenous murine bacterial infection of the bronchopulmonary tissues of mice. J Exp Med 1961; 114:237-56. PMID:13749920; http://dx.doi.org/10.1084/jem.114.2.237
30. Jakab GJ, Warr GA, Knight ME. Pulmonary and systemic defenses against challenge with Staphylococcus aureus in mice with pneumonia due to influenza A virus. J Infect Dis 1979; 140:105-8. PMID:458195; http://dx.doi.org/10.1093/infdis/140.1.105
31. Burnet FM. Influenza virus "A" infections of cynomolgus monkeys. Aust J Med Sci Med Biol 1941; 19:281-90; http://dx.doi.org/10.1038/icb.1941.43
32. McCullers JA, Rehg JE. Lethal synergism between influenza virus and Streptococcus pneumoniae: characterization of a mouse model and the role of platelet-activating factor receptor. J Infect Dis 2002; 186:341-50. PMID:12134230; http://dx.doi.org/10.1086/341462
33. Janssen RJ, Chappell WA, Gerone PJ. Synergistic activity between Pr8 Influenza virus and Staphylococcus aureus in the guinea pig. Am J Hyg 1963; 78:275-84. PMID:14071350
34. Eriksen NH, Espersen F, Rosdahl VT, Jensen K. Carriage of Staphylococcus aureus among 104 healthy persons during a 19-month period. Epidemiol Infect 1995; 115:51-60. PMID:7641838; http://dx.doi.org/10.1017/S0950268800058118
35. Williams RE. Healthy carriage of Staphylococcus aureus: its prevalence and importance. Bacteriol Rev 1963; 27:56-71. PMID:14000926
36. Good RC, May BD. Respiratory pathogens in monkeys. Infect Immun 1971; 3:87-93. PMID:16557951
37. Lina G, Piémont Y, Godail-Gamot F, Bes M, Peter MO, Gauduchon V, Vandenesch F, Etienne J. Involvement of Panton-Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clin Infect Dis 1999; 29:1128-32. PMID:10524952; http://dx.doi.org/10.1086/313461
38. Gillet Y, Issartel B, Vanhems P, Fournet JC, Lina G, Bes M, Vandenesch F, Piémont Y, Brousse N, Floret D, et al. Association between Staphylococcus aureus strains carrying gene for Panton-Valentine leukocidin and highly lethal necrotising pneumonia in young immunocompetent patients. Lancet 2002; 359:753-9. PMID:11888586; http://dx.doi.org/10.1016/S0140-6736(02)07877-7
39. Löffler B, Hussain M, Grundmeier M, Brück M, Holzinger D, Varga G, Roth J, Kahl BC, Proctor RA, Peters G. Staphylococcus aureus panton-valentine leukocidin is a very potent cytotoxic factor for human neutrophils. PLoS Pathog 2010; 6:e1000715. PMID:20072612; http://dx.doi.org/10.1371/journal.ppat.1000715
40. Yoong P, Pier GB. Antibody-mediated enhancement of community-acquired methicillin-resistant Staphylococcus aureus infection. Proc Natl Acad Sci U S A 2010; 107:2241-6. PMID:20133867; http://dx.doi.org/10.1073/pnas.0910344107
41. Graves SF, Kobayashi SD, Braughton KR, Whitney AR, Sturdevant DE, Rasmussen DL, Kirpotina LN, Quinn MT, DeLeo FR. Sublytic concentrations of Staphylococcus aureus Panton-Valentine leukocidin alter human PMN gene expression and enhance bactericidal capacity. J Leukoc Biol 2012; 92:361-74. PMID:22581932; http://dx.doi.org/10.1189/jlb.1111575
42. Yoong P, Pier GB. Immune-activating properties of Panton-Valentine leukocidin improve the outcome in a model of methicillin-resistant Staphylococcus aureus pneumonia. Infect Immun 2012; 80:2894-904. PMID:22665379; http://dx.doi.org/10.1128/IAI.06360-11
43. Malachowa N, Kobayashi SD, Braughton KR, Whitney AR, Parnell MJ, Gardner DJ, Deleo FR. Staphylococcus aureus leukotoxin GH promotes inflammation. J Infect Dis 2012; 206:1185-93. PMID:22872735; http://dx.doi.org/10.1093/infdis/jis495
44. rd, Higgs E, Randolph AG, Smoot BE, Thompson BT; NHLBI ARDS Network. Critical illness from 2009 pandemic influenza A virus and bacterial coinfection in the United States. Crit Care Med 2012; 40:1487-98. PMID:22511131; http://dx.doi.org/10.1097/CCM.0b013e3182416f23
45. Randolph AG, Vaughn F, Sullivan R, Rubinson L, Thompson BT, Yoon G, Smoot E, Rice TW, Loftis LL, Helfaer M, et al.; Pediatric Acute Lung Injury and Sepsis Investigator's Network and the National Heart, Lung, and Blood Institute ARDS Clinical Trials Network. Critically ill children during the 2009-2010 influenza pandemic in the United States. Pediatrics 2011; 128:e1450-8. PMID:22065262; http://dx.doi.org/10.1542/peds.2011-0774
46. Voyich JM, Otto M, Mathema B, Braughton KR, Whitney AR, Welty D, Long RD, Dorward DW, Gardner DJ, Lina G, et al. Is Panton-Valentine leukocidin the major virulence determinant in community-associated methicillin-resistant Staphylococcus aureus disease? J Infect Dis 2006; 194:1761-70. PMID:17109350; http://dx.doi.org/10.1086/509506
47. Shopsin B, Gomez M, Montgomery SO, Smith DH, Waddington M, Dodge DE, Bost DA, Riehman M, Naidich S, Kreiswirth BN. Evaluation of protein A gene polymorphic region DNA sequencing for typing of Staphylococcus aureus strains. J Clin Microbiol 1999; 37:3556-63. PMID:10523551
48. Memoli MJ, Jagger BW, Dugan VG, Qi L, Jackson JP, Taubenberger JK. Recent human influenza A/H3N2 virus evolution driven by novel selection factors in addition to antigenic drift. J Infect Dis 2009; 200:1232-41. PMID:19743921; http://dx.doi.org/10.1086/605893
49. Cottey R, Rowe CA, Bender BS. Influenza virus. Curr Protoc Immunol 2001; Chapter 19:Unit 1911.
50. Safronetz D, Rockx B, Feldmann F, Belisle SE, Palermo RE, Brining D, Gardner D, Proll SC, Marzi A, Tsuda Y, et al. Pandemic swine-origin H1N1 influenza A virus isolates show heterogeneous virulence in macaques. J Virol 2011; 85:1214-23. PMID:21084481; http://dx.doi.org/10.1128/JVI.01848-10
51. Richt JA, Rockx B, Ma W, Feldmann F, Safronetz D, Marzi A, Kobasa D, Strong JE, Kercher L, Long D, et al. Recently emerged swine influenza A virus (H2N3) causes severe pneumonia in Cynomolgus macaques. PLoS One 2012; 7:e39990. PMID:22808082; http://dx.doi.org/10.1371/journal.pone.0039990