EDITORIAL COMMENTARY

Comparing Complications of Pandemic and Seasonal Influenza Is Complicated Charlotte Warren-Gash University College London Research Department of Infection and Population Health, Royal Free Hospital, London, United Kingdom

(See the Major Article by Reed et al on pages 166–74.)

influenza A; (H1N1)pdm09; hospitalization; complications.

Influenza has a major global impact on illness and deaths, with an estimated 3– 5 million cases of severe illness occurring each year as well as 250 000–500 000 deaths from influenza complications [1]. The types of complications that arise vary depending both on host-related factors, such as a patient’s age and underlying comorbidities, and on virus-related factors such as the virulence of circulating strains [2]. For seasonal influenza, the elderly and those with underlying chronic diseases are well recognized to have the highest risk of complications, which are typically respiratory and cardiovascular. These groups are therefore targeted for annual seasonal influenza vaccination [1]. In an influenza pandemic, the types of people who are susceptible to a novel virus may change markedly compared with seasonal influenza, resulting in differing patterns of disease. Accurately quantifying such patterns has important implications for pandemic planning,

Received 8 April 2014; accepted 13 April 2014; electronically published 29 April 2014. Correspondence: Charlotte Warren-Gash, PhD, MRCP, UCL Research Department of Infection and Population Health, 1st Floor, Royal Free Hospital, Rowland Hill St, London NW3 2PF, UK ([email protected]). Clinical Infectious Diseases 2014;59(2):175–6 © The Author 2014. Published by Oxford University Press on behalf of the Infectious Diseases Society of America. All rights reserved. For Permissions, please e-mail: journals. [email protected]. DOI: 10.1093/cid/ciu289

including guiding vaccine recommendations and clinical management [3]. In a study published in this issue of Clinical Infectious Diseases, Reed and colleagues analyzed data from >9000 patients hospitalized with laboratoryconfirmed influenza between 2005 and 2010 captured through the Emerging Infections Program Influenza Surveillance Network [4]. They compared clinical complication profiles using ICD-9 discharge diagnosis codes for adults hospitalized during periods of seasonal influenza circulation with those hospitalized during circulation of the influenza A(H1N1) pandemic strain (H1N1 pdm09). Whereas the younger age of those affected by H1N1pdm09 has been well documented previously [5]—47 years in this study compared with a median of 68 years for seasonal influenza—the frequency of complications in patients hospitalized with H1N1pdm09 has been less consistently reported. After controlling for age and underlying medical conditions, Reed and colleagues demonstrated that the risks of lower respiratory tract complications, septic shock and organ failure, intensive care unit (ICU) admission, and death were greater for patients hospitalized with H1N1pdm09 than for those hospitalized with seasonal influenza. This is in accordance with other studies demonstrating comparatively higher rates of pneumonia [6] and development

of critical illness [7] in people hospitalized with H1N1pdm09. Comparing the burden of seasonal and pandemic influenza is not straightforward. Greater awareness of influenza during a pandemic can profoundly affect patient consultation behavior and shape investigation and management by clinicians. This may in turn notably alter the information available from surveillance [8]. Many of the outcomes in this study are “hard outcomes,” such as requirements for ICU admission, mechanical ventilation, and mortality, which are less likely to be altered by clinician perceptions of pandemic severity. Nonetheless, authors note that one limitation to their study is the potential for thresholds for influenza testing to differ in pandemic vs nonpandemic periods. There was also increased use of a more sensitive polymerase chain reaction (PCR) to diagnose influenza during the pandemic. Is it therefore possible that young patients with severe lower respiratory complications were more likely to be diagnosed with influenza during the 2009–2010 influenza pandemic, leading to underrepresentation of these complications in nonpandemic years? To gain further insight into such questions, it is also helpful to look beyond the tip of the iceberg (or most severe) cases characterized in this study toward illness burden in the community. Hayward and

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profiles seen in this study—such as the greater emphasis on asthma and pregnancy in patients hospitalized with H1N1pdm09 compared with chronic obstructive pulmonary disease and chronic cardiovascular or metabolic disease in patients hospitalized with seasonal influenza— highlight the importance of tailoring resources for influenza prevention and control to shifting patterns of clinical need. Timely research using large routinely collected datasets (such as this work by Reed and colleagues) has the potential to be of great use during an emerging influenza pandemic: Rapid assessment of likely comorbidities and complications has implications for clinical management and hospital resourcing; it can also help target interventions such as antivirals and vaccination to those at greatest risk of severe disease. Examining host genetic factors underlying influenza disease pathogenesis during emerging pandemics, and in particular factors associated with severe influenza, may improve targeting of therapeutic options and inform development of new therapies. A mechanism to share large datasets across countries early in the course of a pandemic to facilitate such research has been called for by Wong and colleagues [10]. Key questions relate to the likely length of stay in hospital, optimum management and treatment options, and estimated mortality from a novel influenza strain [12]. Establishing robust case definitions and definitions for mortality will be of prime importance to allow valid international comparisons to be made. Despite the relatively mild nature of H1N1pdm09 when measured on a population scale, we should underestimate neither its devastating impact on victims’ families nor the potential for a future influenza pandemic to have a completely different clinical and epidemiological profile. Note Potential conflicts of interest. Author certifies no potential conflicts of interest.

EDITORIAL COMMENTARY

The author has submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest. Conflicts that the editors consider relevant to the content of the manuscript have been disclosed.

References 1. World Health Organization. Seasonal influenza factsheet no. 211. 2014. Available at: http://www.who.int/mediacentre/factsheets/ fs211/en/. Accessed 7 April 2014. 2. Hui DS, Hayden FG. Editorial commentary: host and viral factors in emergent influenza virus infections. Clin Infect Dis 2014; 58:1104–6. 3. Mertz D, Kim TH, Johnstone J, et al. Populations at risk for severe or complicated influenza illness: systematic review and meta-analysis. BMJ 2013; 347:f5061. 4. Reed C, Chaves SS, Perez A, et al. Complications among adults hospitalized with influenza: a comparison of seasonal influenza and the 2009 H1N1 pandemic. Clin Infect Dis 2014; 59:166–74. 5. Campbell CN, Mytton OT, McLean EM, et al. Hospitalization in two waves of pandemic influenza A(H1N1) in England. Epidemiol Infect 2011; 139:1560–9. 6. Belongia EA, Irving SA, Waring SC, et al. Clinical characteristics and 30-day outcomes for influenza A 2009 (H1N1), 2008–2009 (H1N1), and 2007–2008 (H3N2) infections. JAMA 2010; 304:1091–8. 7. Lee N, Chan PKS, Lui GCY, et al. Complications and outcomes of pandemic 2009influenza A (H1N1) virus infection in hospitalized adults: how do they differ from those in seasonal influenza? J Infect Dis 2011; 203:1739–47. 8. Brooks-Pollock E, Tilston N, Edmunds WJ, Eames KT. Using an online survey of healthcare-seeking behaviour to estimate the magnitude and severity of the 2009 H1N1v influenza epidemic in England. BMC Infect Dis 2011; 11:68. 9. Hayward AC, Fragaszy EB, Bermingham A, et al. Comparative community burden and severity of seasonal and pandemic influenza: results of the Flu Watch cohort study [Epub ahead of print]. Lancet Respir Med 2014. Available at: http://linkinghub.elsevier.com/ retrieve/pii/S2213260014700347. Accessed 4 April 2014. 10. Wong JY, Kelly H, Ip DK, Wu JT, Leung GM, Cowling BJ. Case fatality risk of influenza A(H1N1pdm09): a systematic review. Epidemiology 2013; 24:830–41. 11. Dawood FS, Iuliano AD, Reed C, et al. Estimated global mortality associated with the first 12 months of 2009 pandemic influenza A H1N1 virus circulation: a modelling study. Lancet Infect Dis 2012; 12:687–95. 12. Infectious Disease Research Network. Planning for a pandemic—addressing research for influenza and other respiratory threats. London: IDRN, 2014. Available at: http://www.idrn.org/ pandemicplanning/. Accessed 4 April 2014.

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colleagues recently published results from a large household cohort study in England that used active weekly surveillance throughout periods of circulation of both seasonal and pandemic influenza strains [9]. This showed that infections with both seasonal influenza and H1N1pdm09 were characterized by high rates of mainly asymptomatic infection. When symptoms did occur, they were usually relatively mild, not requiring medical attention. Infection and disease rates due to H1N1pdm09 were similar to if not slightly lower than prepandemic periods, although in the winter of 2010–2011, rates in young adults were unusually high. Interestingly, in this study symptoms caused by PCR-confirmed H1N1pdm09 in community cases were less severe than symptoms caused by H3N2, although this does not preclude an increased propensity for the H1N1pdm09 virus to cause severe idiosyncratic manifestations in young adults, particularly those with underlying comorbidities. A recent systematic review quantifying case fatality risk for H1N1pdm09 across international studies showed that estimates ranged from 10 000 deaths per 100 000 infections [10]. The disparities were likely to arise from heterogeneity in case definitions, which affected the denominator used for calculations. In general, underestimating the community burden of disease tends to lead to overestimates of disease severity [9]. Nonetheless, it is clear from Reed and colleagues’ work that H1N1pdm09 had a significant impact on young adults with limited preexisting immunity. The younger age of those affected by severe disease led to an increase in years of life lost during the 2009 pandemic compared with some seasonal periods [11]. The fact that younger adults were affected meant greater implications for the workforce and childcare. Despite the relatively mild nature of the H1N1pdm09 pandemic, it still caused significant alarm and disruption as well as a range of health service and other costs. The different comorbidity

Comparing complications of pandemic and seasonal influenza is complicated.

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