The hidden burden of influenza: A review of the extra-pulmonary complications of influenza infection

Subhashini A Sellers, Robert S Hagan, Frederick G Hayden, William A Fischer 2nd, Subhashini A Sellers, Robert S Hagan, Frederick G Hayden, William A Fischer 2nd

Abstract

Severe influenza infection represents a leading cause of global morbidity and mortality. Although influenza is primarily considered a viral infection that results in pathology limited to the respiratory system, clinical reports suggest that influenza infection is frequently associated with a number of clinical syndromes that involve organ systems outside the respiratory tract. A comprehensive MEDLINE literature review of articles pertaining to extra-pulmonary complications of influenza infection, using organ-specific search terms, yielded 218 articles including case reports, epidemiologic investigations, and autopsy studies that were reviewed to determine the clinical involvement of other organs. The most frequently described clinical entities were viral myocarditis and viral encephalitis. Recognition of these extra-pulmonary complications is critical to determining the true burden of influenza infection and initiating organ-specific supportive care.

Keywords: extra-pulmonary complications; influenza; respiratory virus; viral encephalitis; viral myocarditis.

© 2017 The Authors. Influenza and Other Respiratory Viruses Published by John Wiley & Sons Ltd.

Figures

Figure 1
Figure 1
Results of search strategy

References

    1. Fischer WA 2nd, Chason KD, Brighton M, Jaspers I. Live attenuated influenza vaccine strains elicit a greater innate immune response than antigenically‐matched seasonal influenza viruses during infection of human nasal epithelial cell cultures. Vaccine. 2014;32:1761‐1767.
    1. Molinari NA, Ortega‐Sanchez IR, Messonnier ML, et al. The annual impact of seasonal influenza in the US: measuring disease burden and costs. Vaccine. 2007;25:5086‐5096.
    1. Monto AS, Whitley RJ. Seasonal and pandemic influenza: a 2007 update on challenges and solutions. Clin Infect Dis. 2008;46:1024‐1031.
    1. Fearnley RA, Lines SW, Lewington AJ, Bodenham AR. Influenza A‐induced rhabdomyolysis and acute kidney injury complicated by posterior reversible encephalopathy syndrome. Anaesthesia. 2011;66:738‐742.
    1. Warren‐Gash C, Bhaskaran K, Hayward A, et al. Circulating influenza virus, climatic factors, and acute myocardial infarction: a time series study in England and Wales and Hong Kong. J Infect Dis. 2011;203:1710‐1718.
    1. Warren‐Gash C, Hayward AC, Hemingway H, et al. Influenza infection and risk of acute myocardial infarction in England and Wales: a CALIBER self‐controlled case series study. J Infect Dis. 2012;206:1652‐1659.
    1. Warren‐Gash C, Smeeth L, Hayward AC. Influenza as a trigger for acute myocardial infarction or death from cardiovascular disease: a systematic review. Lancet Infect Dis. 2009;9:601‐610.
    1. Gurfinkel EP. Influenza vaccine pilot study in acute coronary syndromes and planned percutaneous coronary interventions: the FLU Vaccination Acute Coronary Syndromes (FLUVACS) Study. Circulation. 2002;105:2143‐2147.
    1. Naghavi M, Barlas Z, Siadaty S, Naguib S, Madjid M, Casscells W. Association of influenza vaccination and reduced risk of recurrent myocardial infarction. Circulation. 2000;102:3039‐3045.
    1. Casscells SW, Granger E, Kress AM, Linton A, Madjid M, Cottrell L. Use of oseltamivir after influenza infection is associated with reduced incidence of recurrent adverse cardiovascular outcomes among military health system beneficiaries with prior cardiovascular diseases. Circ Cardiovasc Qual Outcomes. 2009;2:108‐115.
    1. Kodama M. Influenza Myocarditis. Circ J. 2010;74:2060‐2061.
    1. Karjalainen J, Nieminen MS, Heikkilä J. Influenza Al myocarditis in conscripts. Acta Medica Scandinavica. 1980;207:27‐30.
    1. Paddock CD, Liu L, Denison AM, et al. Myocardial injury and bacterial pneumonia contribute to the pathogenesis of fatal influenza B virus infection. J Infect Dis. 2012;205:895‐905.
    1. Oseasohn R, Adelson L, Kaji M. Clinicopathologic study of thirty‐three fatal cases of Asian influenza. N Engl J Med. 1959;260:509‐518.
    1. Ukimura A, Izumi T, Matsumori A, Clinical Research Committee on M . A National Survey on Myocarditis Associated With the 2009 Influenza A (H1N1) Pandemic in Japan. Circ J. 2010;74:2193‐2199.
    1. Ukimura A, Ooi Y, Kanzaki Y, Inomata T, Izumi T. A national survey on myocarditis associated with influenza H1N1pdm2009 in the pandemic and postpandemic season in Japan. J Infect Chemother. 2013;19:426‐431.
    1. Iwanaga N, Nakamura S, Fukuda Y, et al. A fatal case of acute myocardial infarction following the improvement of influenza A(H1N1)pdm2009‐related acute myocarditis. Intern Med. 2014;53:2153‐2157.
    1. Larsen TR, Kinni V, Zaks J, David S, McCullough PA. A lethal case of influenza and type 5 cardiorenal syndrome. Blood Purif. 2013;36:112‐115.
    1. Taremi M, Amoroso A, Nace HL, Gilliam BL. Influenza B‐induced refractory cardiogenic shock: a case report. BMC Infect Dis. 2013;13:452.
    1. Dahdouh Z, Roule V, Lognoné T, Sabatier R, Massetti M, Grollier G. Atrial septostomy in cardiogenic shock related to H1N1 infection. Acute Cardiac Care. 2012;15:7‐9.
    1. Barbandi M, Cordero‐Reyes A, Orrego CM, Torre‐Amione G, Seethamraju H, Estep J. A case series of reversible acute cardiomyopathy associated with H1N1 influenza infection. Methodist DeBakey Cardiovascu J. 2012;8:42.
    1. Tseng G‐S, Hsieh C‐Y, Hsu C‐T, Lin J‐C, Chan J‐S. Myopericarditis and exertional rhabdomyolysis following an influenza A (H3N2) infection. BMC Infect Dis. 2013;13:283.
    1. Babamahmoodi F, Davoodi AR, Ghasemian R, Delavarian L. Report of two rare complications of pandemic influenza A (H1N1). J Infect Dev Ctries. 2011;6:204‐207.
    1. Davoudi AR, Maleki AR, Beykmohammadi AR, Tayebi A. Fulminant myopericarditis in an immunocompetent adult due to pandemic 2009 (H1N1) influenza A virus infection. Scand J Infect Dis. 2012;44:470‐472.
    1. Adedayo O, Iheonunekwu N, Jefferson D. Acute fulminant myocarditis and the 2009 pandemic influenza A virus (H1N1). West Indian Med J. 2011;60:217‐219.
    1. Himmel F, Hunold P, Schunkert H, Bode F. Influenza A positive but H1N1 negative myocarditis in a patient coming from a high outbreak region of new influenza. Cardiol J. 2011;18:441‐445.
    1. Haessler S, Paez A, Rothberg M, Higgins T. 2009 pandemic H1N1‐associated myocarditis in a previously healthy adult. Clin Microbiol Infect. 2011;17:572‐574.
    1. Cobas M, Abbo L, Santos M, Baccini‐Jauregui C, Pham S. Successful management of fulminant influenza A subtype H1N1 myocarditis. BMJ Case Rep 2010; [Epub ahead of print].
    1. Takehana H, Inomata T, Kuwao S, et al. Recurrent fulminant viral myocarditis with a short clinical course. Circ J. 2003;67:646‐648.
    1. Mamas MA, Fraser D, Neyses L. Cardiovascular manifestations associated with influenza virus infection. Int J Cardiol. 2008;130:304‐309.
    1. McGovern PC, Chambers S, Blumberg EA, et al. Successful explantation of a ventricular assist device following fulminant influenza type A‐associated myocarditis. J Heart Lung Transplant. 2002;21:290‐293.
    1. Ray CG, Icenogle TB, Minnich LL, Copeland JG, Grogan TM. The use of intravenous ribavirin to treat influenza virus‐associated acute myocarditis. J Infect Dis. 1989;159:829‐836.
    1. Yoshimizu N, Tominaga T, Ito T, et al. Repetitive fulminant influenza myocarditis requiring the use of circulatory assist devices. Intern Med. 2014;53:109‐114.
    1. Chiu CW, Yen HH, Chiu CC, Chen YC, Siao FY. Prolonged cardiac arrest: successful resuscitation with extracorporeal membrane oxygenation. Am J Emerg Med 2013;31:1627. e1625‐1626.
    1. Erden I, Erden EÇ, Özhan H, Basar C. Acute myocarditis mimicking acute myocardial infarction associated with pandemic 2009 (H1N1) influenza A virus. Cardiol J. 2011;18:552‐555.
    1. Horai Y, Miyamura T, Takahama S, et al. Influenza virus B‐associated hemophagocytic syndrome and recurrent pericarditis in a patient with systemic lupus erythematosus. Mod Rheumatol. 2010;20:178‐182.
    1. Miura M, Asaumi Y, Wada Y, et al. A case of influenza subtype A virus‐induced fulminant myocarditis: an experience of percutaneous cardio‐pulmonary support (PCPS) treatment and immunohistochemical analysis. Tohoku J Exp Med. 2001;195:11‐19.
    1. Liao YC, Hsieh YC, Chang WC, Huang JL, Ting CT, Wu TJ. Fulminant myocarditis in an adult with 2009 pandemic influenza A (H1N1 influenza) infection. J Chin Med Assoc. 2011;74:130‐133.
    1. Khouzam RN, Parizianu C, Hafiz AM, Chawla S, Schwartz R. Fulminant myocarditis associated with novel H1N1 influenza A. Heart Lung. 2011;40:566‐568.
    1. Şahin DY, Demir M, Kurtaran B, Usal A. A case of myocarditis mimicking acute coronary syndrome associated with H1N1 influenza A virus infection. Türk Kardiyol Dern Arş. 2010;38:572‐575.
    1. Asai N, Ohkuni Y, Komatsu A, et al. A case of asthma‐complicated influenza myocarditis. J Infect Chemother. 2011;17:429‐432.
    1. Chang H‐L, Hsu J‐F, Tsai Y‐M, Lin S‐Y, Kuo H‐F, Yang C‐J. Acute respiratory distress syndrome and acute myocarditis developed in a previously healthy adult with influenza B. BMC Pulm Med. 2016;16:1.
    1. Onitsuka H, Imamura T, Miyamoto N, et al. Clinical manifestations of influenza a myocarditis during the influenza epidemic of winter 1998‐1999. J Cardiol. 2001;37:315‐324.
    1. Kaji M, Kuno H, Turu T, Sato Y, Oizumi K. Elevated serum myosin light chain I in influenza patients. Internal Med. 2001;40:594‐597.
    1. Greaves K, Oxford JS, Price CP, Clarke GH, Crake T. The prevalence of myocarditis and skeletal muscle injury during acute viral infection in adults: measurement of cardiac troponins I and T in 152 patients with acute influenza infection. Arch Intern Med. 2003;163:165‐168.
    1. Ison MG, Campbell V, Rembold C, Dent J, Hayden FG. Cardiac findings during uncomplicated acute influenza in ambulatory adults. Clin Infect Dis. 2005;40:415‐422.
    1. Calabrese F, Carturan E, Chimenti C, et al. Overexpression of tumor necrosis factor (TNF)alpha and TNFalpha receptor I in human viral myocarditis: clinicopathologic correlations. Mod Pathol. 2004;17:1108‐1118.
    1. Davey RT Jr, Lynfield R, Dwyer DE, et al. The association between serum biomarkers and disease outcome in influenza A(H1N1)pdm09 virus infection: results of two international observational cohort studies. PLoS ONE. 2013;8:e57121.
    1. Lee N, Wong CK, Chan PK, et al. Cytokine response patterns in severe pandemic 2009 H1N1 and seasonal influenza among hospitalized adults. PLoS ONE. 2011;6:e26050.
    1. de Jong MD, Simmons CP, Thanh TT, et al. Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat Med. 2006;12:1203‐1207.
    1. Hall MW, Geyer SM, Guo C‐Y, et al. Innate immune function and mortality in critically ill children with influenza: a multicenter study. Crit Care Med. 2013;41:224.
    1. Bradley‐Stewart A, Jolly L, Adamson W, et al. Cytokine responses in patients with mild or severe influenza A (H1N1) pdm09. J Clin Virol. 2013;58:100‐107.
    1. Kumar K, Guirgis M, Zieroth S, et al. Influenza myocarditis and myositis: case presentation and review of the literature. Can J Cardiol. 2011;27:514‐522.
    1. Martin SS, Hollingsworth CL, Norfolk SG, Wolfe CR, Hollingsworth JW. Reversible cardiac dysfunction associated with pandemic 2009 influenza A(H1N1). Chest. 2010;137:1195‐1197.
    1. Brown SM, Pittman J, Miller Iii RR, et al. Right and left heart failure in severe H1N1 influenza A infection. Eur Respir J. 2011;37:112‐118.
    1. Lichenstein R, Magder LS, King RE, King JC Jr. The relationship between influenza outbreaks and acute ischemic heart disease in Maryland residents over a 7‐year period. J Infect Dis. 2012;206:821‐827.
    1. Madjid M, Miller CC, Zarubaev VV, et al. Influenza epidemics and acute respiratory disease activity are associated with a surge in autopsy‐confirmed coronary heart disease death: results from 8 years of autopsies in 34,892 subjects. Eur Heart J. 2007;28:1205‐1210.
    1. Smeeth L, Thomas SL, Hall AJ, Hubbard R, Farrington P, Vallance P. Risk of myocardial infarction and stroke after acute infection or vaccination. N Engl J Med. 2004;351:2611‐2618.
    1. Ludwig A, Lucero‐Obusan C, Schirmer P, Winston C, Holodniy M. Acute cardiac injury events </=30 days after laboratory‐confirmed influenza virus infection among U.S. veterans, 2010–2012. BMC Cardiovasc Disord. 2015;15:109.
    1. Corrales‐Medina VF, Musher DM, Wells GA, Chirinos JA, Chen L, Fine MJ. Cardiac complications in patients with community‐acquired pneumonia incidence, timing, risk factors, and association with short‐term mortality. Circulation. 2012;125:773‐781.
    1. Gwini SM, Coupland CA, Siriwardena AN. The effect of influenza vaccination on risk of acute myocardial infarction: self‐controlled case‐series study. Vaccine. 2011;29:1145‐1149.
    1. Ciszewski A, Bilinska ZT, Brydak LB, et al. Influenza vaccination in secondary prevention from coronary ischaemic events in coronary artery disease: FLUCAD study. Eur Heart J. 2008;29:1350‐1358.
    1. Siriwardena AN, Gwini SM, Coupland CA. Influenza vaccination, pneumococcal vaccination and risk of acute myocardial infarction: matched case‐control study. CMAJ. 2010;182:1617‐1623.
    1. Jackson LA. Influenza vaccination is not associated with a reduction in the risk of recurrent coronary events. Am J Epidemiol. 2002;156:634‐640.
    1. Corrales‐Medina VF, Madjid M, Musher DM. Role of acute infection in triggering acute coronary syndromes. Lancet Infect Dis. 2010;10:83‐92.
    1. Naghavi M. Influenza infection exerts prominent inflammatory and thrombotic effects on the atherosclerotic plaques of apolipoprotein E‐deficient mice. Circulation. 2003;107:762‐768.
    1. Madjid M, Aboshady I, Awan I, Litovsky S, Casscells SW. Influenza and cardiovascular disease: is there a causal relationship? Tex Heart Inst J. 2004;31:4.
    1. Tse H, To KK, Wen X, et al. Clinical and virological factors associated with viremia in pandemic influenza A/H1N1/2009 virus infection. PLoS ONE. 2011;6:e22534.
    1. Likos AM, Kelvin DJ, Cameron CM, Rowe T, Kuehnert MJ, Norris PJ. Influenza viremia and the potential for blood‐borne transmission. Transfusion. 2007;47:1080‐1088.
    1. Haidari M, Wyde PR, Litovsky S, et al. Influenza virus directly infects, inflames, and resides in the arteries of atherosclerotic and normal mice. Atherosclerosis. 2010;208:90‐96.
    1. Auer J, Leitinger M, Berent R, et al. Influenza A and B IgG seropositivity and coronary atherosclerosis assessed by angiography. Heart Dis (Hagerstown, Md). 2001;4:349‐354.
    1. Krummel‐McCracken K. Stroke as a complication of H1N1 influenza infection: a case study. Crit Care Nurse. 2011;31:e1‐e8.
    1. Burad J, Bhakta P, George J, Kiruchennan S. Development of acute ischemic stroke in a patient with acute respiratory distress syndrome (ARDS) resulting from H1N1 pneumonia. Acta Anaesthesiol Taiwan. 2012;50:41‐45.
    1. Nichol KL, Nordin J, Mullooly J, Lask R, Fillbrandt K, Iwane M. Influenza vaccination and reduction in hospitalizations for cardiac disease and stroke among the elderly. N Engl J Med. 2003;348:1322‐1332.
    1. Hung IF, Leung AY, Chu DW, et al. Prevention of acute myocardial infarction and stroke among elderly persons by dual pneumococcal and influenza vaccination: a prospective cohort study. Clin Infect Dis. 2010;51:1007‐1016.
    1. Lavallée P, Perchaud V, Gautier‐Bertrand M, Grabli D, Amarenco P. Association between influenza vaccination and reduced risk of brain infarction. Stroke. 2002;33:513‐518.
    1. Grau AJ, Fischer B, Barth C, Ling P, Lichy C, Buggle F. Influenza vaccination is associated with a reduced risk of stroke. Stroke. 2005;36:1501‐1506.
    1. Lavallée PC, Labreuche J, Fox KM, et al. Influenza vaccination and cardiovascular risk in patients with recent TIA and stroke. Neurology. 2014;82:1905‐1913.
    1. Madjid M, Curkendall S, Blumentals WA. The influence of oseltamivir treatment on the risk of stroke after influenza infection. Cardiology. 2009;113:98‐107.
    1. Goenka A, Michael BD, Ledger E, et al. Neurological manifestations of influenza infection in children and adults: results of a National British Surveillance Study. Clinical Infect Dis. 2014;58(6):775‐84.
    1. Glaser CA, Winter K, DuBray K, et al. A population‐based study of neurologic manifestations of severe influenza A (H1N1) pdm09 in California. Clin Infect Dis. 2012;55:514‐520.
    1. Mizuguchi M. Influenza encephalopathy and related neuropsychiatric syndromes. Influenza Other Respir Viruses. 2013;7:67‐71.
    1. Steininger C, Popow‐Kraupp T, Laferl H, et al. Acute encephalopathy associated with influenza A virus infection. Clin Infect Dis. 2003;36:567‐574.
    1. Gonzalez BE, Brust DG. Novel influenza A (H1N1) presenting as an acute febrile encephalopathy in a mother and daughter. Clin Infect Dis. 2009;49:1966‐1967.
    1. Fugate JE, Lam EM, Rabinstein AA, Wijdicks EF. Acute hemorrhagic leukoencephalitis and hypoxic brain injury associated with H1N1 influenza. Arch Neurol. 2010;67:756‐758.
    1. Chen Y‐C, Lo C‐P, Chang T‐P. Novel influenza A (H1N1)‐associated encephalopathy/encephalitis with severe neurological sequelae and unique image features—A case report. J Neurol Sci. 2010;298:110‐113.
    1. Akins PT, Belko J, Uyeki TM, Axelrod Y, Lee KK, Silverthorn J. H1N1 encephalitis with malignant edema and review of neurologic complications from influenza. Neurocrit Care. 2010;13:396‐406.
    1. Pula JH, Issawi A, DeSanto JR, Kattah JC. Cortical vision loss as a prominent feature of H1N1 encephalopathy. J Neuroophthalmol. 2012;32:48‐50.
    1. Ishigami A, S‐i Kubo, Ikematsu K, et al. An adult autopsy case of acute encephalopathy associated with influenza A virus. Leg Med. 2004;6:252‐255.
    1. Simon M, Hernu R, Cour M, Casalegno J‐S, Lina B, Argaud L. Fatal influenza A (H1N1) pdm09 encephalopathy in immunocompetent man. Emerg Infect Dis. 2013;19:1005.
    1. Bartynski WS, Upadhyaya AR, Boardman JF. Posterior reversible encephalopathy syndrome and cerebral vasculopathy associated with influenza A infection: report of a case and review of the literature. J Comput Assist Tomogr. 2009;33:917‐922.
    1. Hayase Y, Tobita K. Probable post‐influenza cerebellitis. Intern Med. 1997;36:747‐749.
    1. Ak Ö, Biteker F, Cag Y, et al. Influenza B‐associated encephalopathy in two adults. J Infect Chemother. 2012;18:961‐964.
    1. Santini M, Kutleša M, Zarkovic K, Drazenovic V, Barsic B. Influenza A 2009 H1N1 encephalitis in adults with viral RNA in cerebrospinal fluid. Scand J Infect Dis. 2012;44:992‐996.
    1. Cheng A, Kuo K‐H, Yang C‐J. Pandemic (H1N1) 2009 encephalitis in woman, Taiwan. Emerg Infect Dis. 2011;17:1925.
    1. Cunha BA, Corbett M, Mickail N. Influenza A presenting as viral encephalitis in an adult. Heart Lung. 2012;41:308‐309.
    1. Tsai C‐K, Lai Y‐H, Yang F‐C, Chen C‐Y, Peng G‐S. Clinical and radiologic manifestations of H1N1 virus infection associated with neurological complications: a case report. Neurologist. 2011;17:228‐231.
    1. Ito S, Shima S, Ueda A, Kawamura N, Asakura K, Mutoh T. Transient splenial lesion of the corpus callosum in H1N1 influenza virus‐associated encephalitis/encephalopathy. Intern Med. 2011;50:915‐918.
    1. Alakare J, Jurkko R, Kaukonen K‐M, et al. Viral encephalitis associated with pandemic 2009 (H1N1) influenza A. BMJ Case Rep 2010; [Epub ahead of print].
    1. Lee N, Wong CK, Chan PK, et al. Acute encephalopathy associated with influenza A infection in adults. Emerg Infect Dis. 2010;16:139.
    1. Locuratolo N, Mannarelli D, Colonnese C, et al. Unusual posterior reversible encephalopathy syndrome in a case of influenza A/H1N1 infection. J Neurol Sci. 2012;321:114‐116.
    1. Iijima H, Wakasugi K, Ayabe M, Shoji H, Abe T. A case of adult influenza A virus–associated encephalitis: magnetic resonance imaging findings. J Neuroimaging. 2002;12:273‐275.
    1. Jeganathan N, Fox M, Schneider J, Gurka D, Bleck T. Acute hemorrhagic leukoencephalopathy associated with influenza A (H1N1) virus. Neurocrit Care. 2013;19:218‐221.
    1. Wang J, Stewart E, Dapaah‐Afriyie K, Finn A. Mild encephalopathy with reversible splenial lesion in a patient with influenza A infection—first report in an adult patient in the USA. BMJ Case Rep 2015; [Epub ahead of print].
    1. Tomás J, Macário MC, Gaspar E, Santana I. Severe post‐influenza (H1N1) encephalitis involving pulvinar nuclei in an adult patient. BMJ Case Rep 2015; [Epub ahead of print].
    1. Morishima T, Togashi T, Yokota S, et al. Encephalitis and encephalopathy associated with an influenza epidemic in Japan. Clin Infect Dis. 2002;35:512‐517.
    1. Fujimoto S, Kobayashi M, Uemura O, et al. PCR on cerebrospinal fluid to show influenza‐associated acute encephalopathy or encephalitis. Lancet. 1998;352:873‐875.
    1. Pabbaraju K, Tellier R, Wong S, et al. Full‐genome analysis of avian influenza A (H5N1) virus from a human, North America, 2013. Emerg Infect Dis. 2014;20:887‐891.
    1. de Jong MD, Cam BV, Qui PT, et al. Fatal avian influenza A (H5N1) in a child presenting with diarrhea followed by coma. N Engl J Med. 2005;352:686‐691.
    1. Ichiyama T, Morishima T, Isumi H, Matsufuji H, Matsubara T, Furukawa S. Analysis of cytokine levels and NF‐κB activation in peripheral blood mononuclear cells in influenza virus‐associated encephalopathy. Cytokine. 2004;27:31‐37.
    1. J‐i Kawada, Kimura H, Ito Y, et al. Systemic cytokine responses in patients with influenza‐associated encephalopathy. J Infect Dis. 2003;188:690‐698.
    1. Hasegawa S, Matsushige T, Inoue H, Shirabe K, Fukano R, Ichiyama T. Serum and cerebrospinal fluid cytokine profile of patients with 2009 pandemic H1N1 influenza virus‐associated encephalopathy. Cytokine. 2011;54:167‐172.
    1. Hasegawa S, Matsushige T, Inoue H, et al. Serum soluble CD163 levels in patients with influenza‐associated encephalopathy. Brain Dev. 2013;35:626‐629.
    1. Shinohara M, Saitoh M, Takanashi J, et al. Carnitine palmitoyl transferase II polymorphism is associated with multiple syndromes of acute encephalopathy with various infectious diseases. Brain Dev. 2011;33:512‐517.
    1. Shinohara M, Saitoh M, Nishizawa D, et al. ADORA2A polymorphism predisposes children to encephalopathy with febrile status epilepticus. Neurology. 2013;80:1571‐1576.
    1. Neilson DE, Adams MD, Orr CM, et al. Infection‐triggered familial or recurrent cases of acute necrotizing encephalopathy caused by mutations in a component of the nuclear pore, RANBP2. Am J Human Genet. 2009;84:44‐51.
    1. Zhang L‐K, Chai F, Li H‐Y, Xiao G, Guo L. Identification of host proteins involved in Japanese encephalitis virus infection by quantitative proteomics analysis. J Proteome Res. 2013;12:2666‐2678.
    1. Ocwieja KE, Brady TL, Ronen K, et al. HIV integration targeting: a pathway involving Transportin‐3 and the nuclear pore protein RanBP2. PLoS Pathog. 2011;7:e1001313.
    1. Zhang R, Mehla R, Chauhan A. Perturbation of host nuclear membrane component RanBP2 impairs the nuclear import of human immunodeficiency virus‐1 preintegration complex (DNA). PLoS ONE. 2010;5:e15620.
    1. Sivadon‐Tardy V, Orlikowski D, Porcher R, et al. Guillain‐Barré syndrome and influenza virus infection. Clin Infect Dis. 2009;48:48‐56.
    1. Kutleša M, Santini M, Krajinović V, Raffanelli D, Baršić B. Acute motor axonal neuropathy associated with pandemic H1N1 influenza A infection. Neurocrit Care. 2010;13:98‐100.
    1. Hara M, Morita A, Ichihara K, et al. Miller Fisher syndrome associated with influenza A infection. Intern Med. 2012;51:2621‐2623.
    1. Cortese A, Baldanti F, Tavazzi E, et al. Guillain–Barré syndrome associated with the D222E variant of the 2009 pandemic influenza A (H1N1) virus: case report and review of the literature. J Neurol Sci. 2012;312:173‐176.
    1. Wells C, James W, Evans A. Guillain‐Barré syndrome and virus of influenza A (Asian strain): report of two fatal cases during the 1957 epidemic in Wales. AMA Arch Neurol Psychiatry. 1959;81:699‐705.
    1. Tam CC, O'brien SJ, Petersen I, Islam A, Hayward A, Rodrigues LC. Guillain‐Barré syndrome and preceding infection with campylobacter, influenza and Epstein‐Barr virus in the general practice research database. PLoS ONE. 2007;2:e344.
    1. Tam CC, O'Brien SJ, Rodrigues LC. Influenza, Campylobacter and Mycoplasma infections, and hospital admissions for Guillain‐Barré syndrome, England. Emerg Infect Dis. 2006;12:1880.
    1. Sivadon‐Tardy V, Orlikowski D, Rozenberg F, et al. Guillain‐Barré syndrome, greater Paris area. Emerg Infect Dis. 2006;12:990.
    1. Stowe J, Andrews N, Wise L, Miller E. Investigation of the temporal association of Guillain‐Barre syndrome with influenza vaccine and influenzalike illness using the United Kingdom General Practice Research Database. Am J Epidemiol. 2009;169:382‐388.
    1. Lehmann HC, Hartung H‐P, Kieseier BC, Hughes RA. Guillain‐Barré syndrome after exposure to influenza virus. Lancet Infect Dis. 2010;10:643‐651.
    1. Kwong JC, Vasa PP, Campitelli MA, et al. Risk of Guillain‐Barré syndrome after seasonal influenza vaccination and influenza health‐care encounters: a self‐controlled study. Lancet Infect Dis. 2013;13:769‐776.
    1. Lei T, Siu K‐L, Kok K‐H, et al. Anti‐ganglioside antibodies were not detected in human subjects infected with or vaccinated against 2009 pandemic influenza A (H1N1) virus. Vaccine. 2012;30:2605‐2610.
    1. Ravaglia S, Ceroni M, Moglia A, Todeschini A, Marchioni E. Post‐infectious and postvaccinal acute disseminated encephalomyelitis occurring in the same patients. J Neurol. 2004;251:1147‐1150.
    1. Jun Y, Yu‐Guang W, Yun‐Liang X, Xian‐Ling R, Yu M, Xing‐Wang L. A (H1N1) influenza pneumonia with acute disseminated encephalomyelitis: a case report. Biomed Environ Sci. 2010;23:323‐326.
    1. Wang J, Duan S, Zhao J, Zhang L. Acute disseminated encephalomyelitis associated with influenza A H1N1 infection. Neurol Sci. 2011;32:907‐909.
    1. Athauda D, Andrews TC, Holmes PA, Howard RS. Multiphasic acute disseminated encephalomyelitis (ADEM) following influenza type A (swine specific H1N1). J Neurol. 2012;259:775‐778.
    1. Chan A, Ng S. Tumefactive acute disseminated encephalomyelitis complicating human swine influenza (H1N1). Hong Kong Med J. 2014;20:447‐450.
    1. Amano H, Miyamoto N, Shimura H, et al. Influenza‐associated MOG antibody‐positive longitudinally extensive transverse myelitis: a case report. BMC Neurol. 2014;14:224.
    1. Partinen M, Kornum BR, Plazzi G, Jennum P, Julkunen I, Vaarala O. Narcolepsy as an autoimmune disease: the role of H1N1 infection and vaccination. Lancet Neurol. 2014;13:600‐613.
    1. Han F, Lin L, Warby SC, et al. Narcolepsy onset is seasonal and increased following the 2009 H1N1 pandemic in China. Ann Neurol. 2011;70:410‐417.
    1. Tesoriero C, Codita A, Zhang M‐D, et al. H1N1 influenza virus induces narcolepsy‐like sleep disruption and targets sleep–wake regulatory neurons in mice. Proc Natl Acad Sci USA. 2016;113:E368‐E377.
    1. Varma RR, Riedel DR, Komorowski RA, Harrington GJ, Nowak TV. Reye's syndrome in nonpediatric age groups. JAMA. 1979;242:1373‐1375.
    1. Davis LE, Kornfeld M. Influenza A virus and Reye's syndrome in adults. J Neurol Neurosurg Psychiatry. 1980;43:516‐521.
    1. Studahl M. Influenza virus and CNS manifestations. J Clin Virol. 2003;28:225‐232.
    1. McCall S, Henry JM, Reid AH, Taubenberger JK. Influenza RNA not detected in archival brain tissues from acute encephalitis lethargica cases or in postencephalitic Parkinson cases. J Neuropathol Exp Neurol. 2001;60:696‐704.
    1. Lo K, Geddes J, Daniels R, Oxford J. Lack of detection of influenza genes in archived formalin‐fixed, paraffin wax‐embedded brain samples of encephalitis lethargica patients from 1916 to 1920. Virchows Arch. 2003;442:591‐596.
    1. Dale RC, Church AJ, Surtees RA, et al. Encephalitis lethargica syndrome: 20 new cases and evidence of basal ganglia autoimmunity. Brain. 2004;127:21‐33.
    1. González‐Duarte A, Zamora LM, Brito CC, García‐Ramos G. Hypothalamic abnormalities and Parkinsonism associated with H1N1 influenza infection. J Neuroinflammation. 2010;7:47.
    1. Gamboa ET, Wolf A, Yahr MD, et al. Influenza virus antigen in postencephalitic parkinsonism brain: detection by immunofluorescence. Arch Neurol. 1974;31:228‐232.
    1. Rohn TT, Catlin LW. Immunolocalization of influenza A virus and markers of inflammation in the human Parkinson's disease brain. PLoS ONE. 2011;6:e20495.
    1. Toovey S, Jick SS, Meier CR. Parkinson's disease or Parkinson symptoms following seasonal influenza. Influenza Other Respir Viruses. 2011;5:328‐333.
    1. Tanaka T, Takada T, Takagi D, Takeyama N, Kitazawa Y. Acute renal failure due rhabdomyolysis associated with echovirus 9 infection. A case report and review of literature. Jpn J Med. 1989;28:237‐242.
    1. Singh U, Scheld WM. Infectious etiologies of rhabdomyolysis: three case reports and review. Clin Infect Dis. 1996;22:642‐649.
    1. Annerstedt M, Herlitz H, Mölne J. Rhabdomyolysis and acute renal failure associated with influenza virus type A. Scandinavian J Urol Nephrol. 1999;33:260‐264.
    1. Unverdi S, Akay H, Ceri M, et al. Acute kidney injury due to Rhabdomyolysis in H1N1 influenza infection. Ren Fail. 2011;33:450‐451.
    1. Naderi ASA, Palmer BF. Rhabdomyolysis and acute renal failure associated with influenza virus type B infection. Am J Med Sci. 2006;332:88‐89.
    1. Cunningham E, Kohli R, Venuto RC. Influenza‐associated myoglobinuric renal failure. JAMA. 1979;242:2428‐2429.
    1. Wakabayashi Y, Nakano T, Kikuno T, Ohwada T, Kikawada R. Massive rhabdomyolysis associated with influenza A infection. Intern Med. 1994;33:450‐453.
    1. Berry L, Braude S. Influenza A infection with rhabdomyolysis and acute renal failure–a potentially fatal complication. Postgrad Med J. 1991;67:389‐390.
    1. Foulkes W, Rees J, Sewry C. Influenza A and rhabdomyolysis. J Infect. 1990;21:303‐304.
    1. Yoshino M, Suzuki S, Adachi K, Fukayama M, Inamatsu T. High incidence of acute myositis with type A influenza virus infection in the elderly. Intern Med. 2000;39:431‐432.
    1. Ayala E, Kagawa FT, Wehner JH, Tam J, Upadhyay D. Rhabdomyolysis associated with 2009 influenza A (H1N1). JAMA. 2009;302:1863‐1864.
    1. Oba K, Nishihara A, Okamura K, et al. Two cases of acute myositis associated with influenza A virus infection in the elderly. J Nippon Med Sch. 2000;67:126‐129.
    1. Parikh M, Dolson G, Ramanathan V, Sangsiraprapha W. Novel H1N1‐associated rhabdomyolysis leading to acute renal failure. Clin Microbiol Infect. 2010;16:330‐332.
    1. Kessler HA, Trenholme GM, Harris AA, Levin S. Acute myopathy associated with influenza A/Texas/1/77 infection: isolation of virus from a muscle biopsy specimen. JAMA. 1980;243:461‐462.
    1. Kaida K, Kamakura K, Masaki T, Okano M, Nagata N, Inoue K. Painful small‐fibre multifocal mononeuropathy and local myositis following influenza B infection. J Neurol Sci. 1997;151:103‐106.
    1. Perez‐Padilla R, De La Rosa‐zamboni D, Ponce de Leon S, et al. Pneumonia and respiratory failure from swine‐origin influenza A (H1N1) in Mexico. N Engl J Med. 2009;361:680‐689.
    1. Borgatta B, Perez M, Rello J, et al. Elevation of creatine kinase is associated with worse outcomes in 2009 pH1N1 influenza A infection. Intensive Care Med. 2012;38:1152‐1161.
    1. Armstrong C, Miranda A, Hsu K, Gamboa E. Susceptibility of human skeletal muscle culture to influenza virus infection: I. Cytopathology and immunofluorescence. J Neurol Sci. 1978;35:43‐57.
    1. Desdouits M, Munier S, Prevost MC, et al. Productive infection of human skeletal muscle cells by pandemic and seasonal influenza A(H1N1) viruses. PLoS ONE. 2013;8:e79628.
    1. Gamboa E, Eastwood A, Hays A, Maxwell J, Penn A. Isolation of influenza virus from muscle in myoglobinuric polymyositis. Neurology. 1979;29:1323‐1335.
    1. Agyeman P, Duppenthaler A, Heininger U, Aebi C. Influenza‐associated myositis in children. Infection. 2004;32:199‐203.
    1. Bove KE, Hilton PK, Partin J, Farrell MK. Morphology of acute myopathy associated with influenza B infection. Fetal Pediatric Pathol. 1983;1:51‐66.
    1. Mansour DE, El‐Shazly AA, Elawamry AI, Ismail AT. Comparison of ocular findings in patients with H1N1 influenza infection versus patients receiving influenza vaccine during a pandemic. Ophthalmic Res. 2012;48:134‐138.
    1. Chan MC, Chan RW, Yu WC, et al. Tropism and innate host responses of the 2009 pandemic H1N1 influenza virus in ex vivo and in vitro cultures of human conjunctiva and respiratory tract. Am J Pathol. 2010;176:1828‐1840.
    1. Koopmans M, Wilbrink B, Conyn M, et al. Transmission of H7N7 avian influenza A virus to human beings during a large outbreak in commercial poultry farms in the Netherlands. The Lancet. 2004;363:587‐593.
    1. Fouchier RA, Schneeberger PM, Rozendaal FW, et al. Avian influenza A virus (H7N7) associated with human conjunctivitis and a fatal case of acute respiratory distress syndrome. Proc Natl Acad Sci USA. 2004;101:1356‐1361.
    1. Tweed SA, Skowronski DM, David ST, et al. Human illness from avian influenza H7N3, British Columbia. Emerg Infect Dis. 2004;10:2196.
    1. CfD Control Prevention . Notes from the field: highly pathogenic avian influenza A (H7N3) virus infection in two poultry workers–Jalisco, Mexico, July 2012. MMWR: Morb Mortal Wkly Rep. 2012;61:726.
    1. te Beest DE, van Boven M, Bos ME, Stegeman A, Koopmans MP. Effectiveness of personal protective equipment and oseltamivir prophylaxis during avian influenza A (H7N7) epidemic, the Netherlands, 2003. Emerg Infect Dis. 2010;16:1562‐1568.
    1. Belser JA, Sleeman K, Pearce MB, Katz JM, Gubareva LV, Tumpey TM. Oseltamivir inhibits H7 influenza virus replication in mice inoculated by the ocular route. Antimicrob Agents Chemother. 2012;56:1616‐1618.
    1. Lopez‐Prats MJ, Sanz Marco E, Hidalgo‐Mora JJ, Garcia‐Delpech S, Diaz‐Llopis M. Bleeding follicular conjunctivitis due to influenza H1N1 virus. J Ophthalmol. 2010;2010:423672.
    1. Rifkin L, Schaal S. H1N1‐associated acute retinitis. Ocul Immunol Inflamm. 2012;20:230‐232.
    1. Fukami S, Wakakura M, Inouye J. Influenza retinitis: association with influenza encephalitis. Ophthalmologica. 2005;219:119‐121.
    1. Pettilä V, Webb SA, Bailey M, Howe B, Seppelt IM, Bellomo R. Acute kidney injury in patients with influenza A (H1N1) 2009. Intensive Care Med. 2011;37:763‐767.
    1. Nin N, Lorente J, Soto L, et al. Acute kidney injury in critically ill patients with 2009 influenza A (H1N1) viral pneumonia: an observational study. Intensive Care Med. 2011;37:768‐774.
    1. Martin‐Loeches I, Papiol E, Rodriguez A, et al. Acute kidney injury in critical ill patients affected by influenza A (H1N1) virus infection. Crit Care. 2011;15:R66.
    1. Demirjian SG, Raina R, Bhimraj A, et al. 2009 influenza A infection and acute kidney injury: incidence, risk factors, and complications. Am J Nephrol. 2011;34:1‐8.
    1. Bagshaw SM, Sood MM, Long J, Fowler RA, Adhikari NK. Acute kidney injury among critically ill patients with pandemic H1N1 influenza A in Canada: cohort study. BMC Nephrol. 2013;14:123.
    1. Jung JY, Park BH, Hong SB, et al. Acute kidney injury in critically ill patients with pandemic influenza A pneumonia 2009 in Korea: a multicenter study. J Crit Care. 2011;26:577‐585.
    1. Carmona F, Carlotti AP, Ramalho LN, Costa RS, Ramalho FS. Evidence of renal infection in fatal cases of 2009 pandemic influenza A (H1N1). Am J Clin Pathol. 2011;136:416‐423.
    1. Mauad T, Hajjar LA, Callegari GD, et al. Lung pathology in fatal novel human influenza A (H1N1) infection. Am J Respir Crit Care Med. 2010;181:72‐79.
    1. Abdulkader RC, Ho YL, de Sousa Santos S, Caires R, Arantes MF, Andrade L. Characteristics of acute kidney injury in patients infected with the 2009 influenza A (H1N1) virus. Clin J Am Soc Nephrol. 2010;5:1916‐1921.
    1. Papic N, Pangercic A, Vargovic M, Barsic B, Vince A, Kuzman I. Liver involvement during influenza infection: perspective on the 2009 influenza pandemic. Influenza Other Respir Viruses. 2012;6:e2‐e5.
    1. Duchini A, Viernes ME, Nyberg LM, Hendry RM, Pockros PJ. Hepatic decompensation in patients with cirrhosis during infection with influenza A. Arch Intern Med. 2000;160:113‐115.
    1. Whitworth JR, Mack CL, O'Connor JA, Narkewicz MR, Mengshol S, Sokol RJ. Acute hepatitis and liver failure associated with influenza A infection in children. J Pediatr Gastroenterol Nutr. 2006;43:536‐538.
    1. Polakos NK, Cornejo JC, Murray DA, et al. Kupffer cell‐dependent hepatitis occurs during influenza infection. Am J Pathol 2006;168:1169‐1178 ; quiz 1404‐1165.
    1. Bal A, Suri V, Mishra B, et al. Pathology and virology findings in cases of fatal influenza A H1N1 virus infection in 2009‐2010. Histopathology. 2012;60:326‐335.
    1. Yuen KY, Chan PKS, Peiris M, et al. Clinical features and rapid viral diagnosis of human disease associated with avian influenza A H5N1 virus. The Lancet. 1998;351:467‐471.
    1. Gao H‐N, Lu H‐Z, Cao B, et al. Clinical findings in 111 cases of influenza A (H7N9) virus infection. N Engl J Med. 2013;368:2277‐2285.
    1. Ru YX, Li YC, Zhao Y, et al. Multiple organ invasion by viruses: pathological characteristics in three fatal cases of the 2009 pandemic influenza A/H1N1. Ultrastruct Pathol. 2011;35:155‐161.
    1. Fraňková V, Jirasek A, Tůmová B. Type A influenza: postmortem virus isolations from different organs in human lethal cases. Adv Virol. 1977;53:265‐268.
    1. Han J, Zhang N, Zhang P, et al. Th2‐type inflammation under conditions of pre‐existing chronic disease is associated with liver damage in patients with avian influenza H7N9 virus. Microbes Infect. 2014;16:672‐677.
    1. Stucchi RS, Boin IF, Angerami RN, et al. Correlations between A/H1N1 influenza and acute cellular rejection in liver transplantation patients. Transplant Proc. 2010;42:4184‐4186.
    1. Harms PW, Schmidt LA, Smith LB, et al. Autopsy findings in eight patients with fatal H1N1 influenza. Am J Clin Pathol. 2010;134:27‐35.
    1. van Wissen M, Keller TT, Ronkes B, et al. Influenza infection and risk of acute pulmonary embolism. Thromb J. 2007;5:16.
    1. Bunce PE, High SM, Nadjafi M, Stanley K, Liles WC, Christian MD. Pandemic H1N1 influenza infection and vascular thrombosis. Clin Infect Dis. 2011;52:e14‐e17.
    1. Zhu T, Carcaillon L, Martinez I, et al. Association of influenza vaccination with reduced risk of venous thromboembolism. Thromb Haemost. 2009;102:1259‐1264.
    1. Rhee H, Song SH, Lee YJ, et al. Pandemic H1N1 influenza A viral infection complicated by atypical hemolytic uremic syndrome and diffuse alveolar hemorrhage. Clin Exp Nephrol. 2011;15:948‐952.
    1. Kosugi N, Tsurutani Y, Isonishi A, Hori Y, Matsumoto M, Fujimura Y. Influenza A infection triggers thrombotic thrombocytopenic purpura by producing the anti‐ADAMTS13 IgG inhibitor. Intern Med. 2010;49:689‐693.
    1. Wasserstein A, Hill G, Goldfarb S, Goldberg M. Recurrent thrombotic thrombocytopenic purpura after viral infection: clinical and histologic simulation of chronic glomerulonephritis. Arch Intern Med. 1981;141:685‐687.
    1. Asaka M, Ishikawa I, Nakazawa T, Tomosugi N, Yuri T, Suzuki K. Hemolytic uremic syndrome associated with influenza A virus infection in an adult renal allograft recipient: case report and review of the literature. Nephron. 2000;84:258‐266.
    1. Klein P, Bulla M, Newman R, et al. Thomsen Friedenreich antigen in hæmolytic‐uræmic syndrome. The Lancet. 1977;310:1024‐1025.
    1. To K‐F, Chan PK, Chan K‐F, et al. Pathology of fatal human infection associated with avian influenza A H5N1 virus. J Med Virol. 2001;63:242‐246.
    1. Ando M, Miyazaki E, Hiroshige S, et al. Virus associated hemophagocytic syndrome accompanied by acute respiratory failure caused by influenza A (H3N2). Intern Med. 2006;45:1183‐1186.
    1. Fukaya S, Yasuda S, Hashimoto T, et al. Clinical features of haemophagocytic syndrome in patients with systemic autoimmune diseases: analysis of 30 cases. Rheumatology. 2008;47:1686‐1691.
    1. Harper SA, Bradley JS, Englund JA, et al. Seasonal influenza in adults and children—diagnosis, treatment, chemoprophylaxis, and institutional outbreak management: clinical practice guidelines of the Infectious Diseases Society of America. Clin Infect Dis. 2009;48:1003‐1032.
    1. Watkins P, Soler N, Fitzgerald M, Malins J. Diabetic ketoacidosis during the influenza epidemic. Br Med J. 1970;4:89‐91.
    1. Krishna S, Sunil K, Prasad RD, Modi K. Precipitation of new onset diabetes by H1N1 infection. Indian J Endocrinol Metab. 2012;16:438.
    1. Sano H, Terasaki J, Tsutsumi C, Imagawa A, Hanafusa T. A case of fulminant type 1 diabetes mellitus after influenza B infection. Diabetes Res Clin Pract. 2008;79:e8‐e9.
    1. Moghadami M, Honarvar B, Sabaeian B, et al. H1N1 influenza infection complicated with diabetic ketoacidosis. Arch Iran Med 2012;15:55.
    1. Bouter KP, Diepersloot RJ, van Romunde LK, et al. Effect of epidemic influenza on ketoacidosis, pneumonia and death in diabetes mellitus: a hospital register survey of 1976–1979 in The Netherlands. Diabetes Res Clin Pract. 1991;12:61‐68.

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