Article information
Abstract
Although influenza is usually a self-limited disease, patients who develop complications are at increased risk of hospitalization, intensive care unit admission and death. Since preventive and early therapeutic measures should be prioritized in higher risk patients, identification of the risk factors for severe infection is important from a public health perspective. Risk factors for complications in pandemics may show some differences with regard to seasonal influenza. During the influenza A(H1N1)pmd09 pandemic, although many cases occurred in younger adults, the risk factors identified for severe infections and complications were similar to those for seasonal influenza, including chronic respiratory, renal, liver, and heart diseases. Aged patients, although less frequently affected, were also at higher risk. Obesity, and particularly morbid obesity (>40 body mass index) has been noted as a significant risk factor for severe disease in the 2009 influenza pandemic. Some interesting recent studies provide insights into the biological reasons behind the poor outcomes in morbidly obese patients. In terms of pregnancy, the studies have shown contradictory results due to variations in methodology and medical care. However, it seems that pregnancy, particularly during the third trimester, increases the risk of complications, and that early antiviral treatment is associated with improved outcomes.
Keywords:
Influenza infection
A(H1N1)
Pandemic influenza
Seasonal influenza
Influenza complications
Risk factors
Outcomes
Resumen
Aunque la gripe es habitualmente una enfermedad autolimitada, el desarrollo de complicaciones se asocia con mayor riesgo de ingreso, de necesidad de cuidados intensivos y de muerte. Dado que las medidas preventivas y terapéuticas deben priorizarse en los pacientes de mayor riesgo, el conocimiento de los factores de riesgo tiene gran importancia desde la perspectiva de la salud pública. Los factores de riesgo de enfermedad grave pueden ser distintos en las pandemias; los factores identificados durante la pandemia 2009 A(H1N1), a pesar de que muchos de los casos ocurrieron en personas jóvenes, son similares a los de la infección estacional, incluyendo las enfermedades respiratorias, renales, hepáticas y cardíacas crónicas. Los pacientes ancianos, aunque menos frecuentemente afectados, también mostraron mayor riesgo. La obesidad, sobre todo la mórbida (índice de masa corporal > 40) ha sido también un factor de riesgo significativo durante esta pandemia. Recientemente se han publicado datos interesantes sobre las posibles explicaciones biológicas de este hecho. Con respecto al embarazo, los datos de los estudios son contradictorios debido a diferencias metodológicas y de atención sanitaria. Sin embargo, parece que el embarazo, particularmente durante el tercer trimestre, aumenta el riesgo de complicaciones, y que el tratamiento antiviral precoz mejora el pronóstico.
Palabras clave:
Infección de gripe
A(H1N1)
Gripe pandémica
Gripe estacional
Complicaciones de la gripe
Factores de riesgo
Resultados
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References
[2.]
A.E. Fiore, D. Shay, K. Broder, J.K. Iskander, T. Uyeki, G. Mootrey, et al.
Centers for Disease Control and Prevention. Prevention and control of seasonal influenza with vaccines: recommendations of the Advisory Committee on Immunization Practices (ACIP), 2009.
MMWR Recomm Rep, 58 (2009), pp. 1-52
[3.]
J.M. Navarro-Marí, J.M. Mayoral-Cortés, M. Pérez-Ruiz, J. Rodríguez-Baño, J. Carratalá, V. Gallardo-García.
Influenza a (H1N1) virus infection in humans: review to 30th October 2009.
Enferm Infecc Microbiol Clin, 28 (2010), pp. 446-452
[4.]
D. Viasus, J.R. Paño-Pardo, J. Pachón, M. Riera, F. López-Medrano, A. Payeras, et al.
Pneumonia complicating pandemic (H1N1) 2009. Risk factors, clinical features, and outcomes.
Medicine, 90 (2011), pp. 328-336
[5.]
D.J. Jamieson, M.A. Honein, S.A. Rasmussen, J.L. Williams, D.L. Swerdlow, M.S. Biggerstaff, et al.
H1N1 2009 influenza virus infection during pregnancy in the USA.
Lancet, 374 (2009), pp. 451-458
[6.]
S. Hewagama, S.P. Walker, R.L. Stuart, C. Gordon, P.D.R. Johnson, N.D. Friedman, et al.
2009 H1N1 Influenza A and pregnancy outcomes in Victoria, Australia.
Clin Infect Dis, 50 (2010), pp. 686-690
[7.]
L.J. Donaldson, P.D. Rutter, B.M. Ellis, F.E.C. Greaves, O.T. Mytton, R.G. Pebody, et al.
Mortality from pandemic A/H1N1 2009 influenza in England: public health surveillance study.
BMJ, 339 (2009), pp. b5213
[8.]
A.M. Siston, S.A. Rasmussen, M.A. Honein, A.M. Fry, K. Seib, W.M. Callaghan, et al.
Pandemic 2009 influenza A(H1N1) virus illness among pregnant women in the United States.
JAMA, 303 (2010), pp. 1517-1525
[9.]
ANZIC Influenza Investigators and Australasian Maternity Outcomes Surveillance System.
Critical illness due to 2009 A/H1N1 influenza in pregnant and postpartum women: population based cohort study.
BMJ, 340 (2010), pp. c1279
[10.]
E. Maraví-Poma, I. Martin-Loeches, E. Regidor, C. Laplaza, K. Cambra, S. Aldunate, et al.
Severe 2009 A/H1N1v influenza in pregnant women in Spain.
Crit Care Med, 39 (2011), pp. 945-951
[11.]
M.L. Lim, C.Y. Chong, W.S.N. Tee, W.Y. Lim, J.J. Chee.
Influenza A/H1N1 (2009) infection in pregnancy—an Asian perspective.
BJOG, 117 (2010), pp. 551-556
[12.]
P. Gérardin, R. Amrani el, B. Cyrille, M. Gabrièle, P. Guillermin, M. Boukerrou, et al.
Low clinical burden of 2009 pandemic influenza A (H1N1) infection during pregnancy on the island of La Réunion.
PLoS One, 5 (2010), pp. e10896
[13.]
J.R. Paño-Pardo, J. Rodríguez-Baño, N. Martínez-Sánchez, D. Viasus, M.C. Fariñas, M. Leyes, et al.
Prognosis of 2009 A(H1N1) influenza in hospitalized pregnant women in a context of early diagnosis and antiviral therapy.
Antivir Ther, 17 (2012), pp. 719-728
[14.]
A. Nakai, H. Minakami, N. Unno, S. Saito, M. Morikawa, Y. Yoshimura, et al.
Characteristics of pregnant Japanese women who required hospitalization for treatment of pandemic (H1N1) 2009—low mortality rate may be due to early antiviral use.
J Infect, 62 (2011), pp. 232-233
[15.]
L.G. Mosby, S.A. Rasmussen, D.J. Jamieson.
2009 pandemic influenza A (H1N1) in pregnancy: a systematic review of the literature.
Am J Obstet Gynecol, 205 (2011), pp. 10-18
[16.]
Centers for Disease Control and Prevention CDC.
Influenza vaccination coverage among pregnant women - 29 States and New York City, 2009–10 season.
MMWR Morb Mortal Wkly Rep, 61 (2012), pp. 113-118
[17.]
R. Freund, C. Le Ray, C. Charlier, C. Avenell, V. Truster, J.M. Tréluyer, et al.
Determinants of non-vaccination against pandemic 2009 H1N1 influenza in pregnant women: a prospective cohort study.
PLoS One, 6 (2011), pp. e20900
[18.]
B. Pasternak, H. Svanström, D. Mølgaard-Nielsen, T.G. Krause, H.D. Emborg, M. Melbye, et al.
Vaccination against pandemic A/H1N1 2009 influenza in pregnancy and risk of fetal death: cohort study in Denmark.
BMJ, 344 (2012), pp. e2794
[19.]
D.B. Fell, A.E. Sprague, N. Liu, A.S. Yasseen, S.W. Wen, G. Smith, et al.
H1N1 Influenza vaccination during pregnancy and fetal and neonatal outcomes.
Am J Public Health, 102 (2012), pp. e33-e40
[20.]
A. Berghofer, T. Pischon, T. Reinhold, C.M. Apovian, A.M. Sharma, S.N. Willich.
Obesity prevalence from a European perspective: a systematic review.
BMC Public Health, 8 (2008), pp. 200
[21.]
A. Rodríguez-Martín, J.P. Novalbos Ruiz, J.M. Martínez Nieto, L. Escobar Jiménez.
Life-style factors associated with overweight and obesity among Spanish adults.
Nutr Hosp, 24 (2009), pp. 144-151
[22.]
F.X. Pi-Sunyer.
The obesity epidemic: pathophysiology and consequences of obesity.
Obes Res, 10 (2002), pp. 97S-104S
[23.]
M.E. Falagas, A.P. Athanasoulia, G. Peppas, D.E. Karageorgopoulos.
Effect of body mass index on the outcome of infections:a systematic review.
Obes Rev, 10 (2009), pp. 280-289
[24.]
I. Baik, G.C. Curhan, E.B. Rimm, A. Bendich.
A prospective study of age and lifestyle factors in relation to community-acquired pneumonia in US men and women.
Arch Intern Med, 160 (2000), pp. 3082-3088
[25.]
K.M. Flegal, B.I. Graubard, D.F. Williamson, M.H. Gail.
Excess deaths associated with underweight, overweight, and obesity.
JAMA, 293 (2005), pp. 1861-1867
[27.]
A. Sood.
Obesity, adipokines, and lung disease.
J Appl Physiol, 108 (2010), pp. 744-753
[28.]
Centers for Disease Control and Prevention (CDC).
Intensive-care patients with severe novel influenza A (H1N1) virus infection - Michigan, June 2009.
MMWR Morb Mortal Wkly Rep, 58 (2009), pp. 749-752
[29.]
A. Kumar, R. Zarychanski, R. Pinto, D.J. Cook, J. Marshall, J. Lacroix, et al.
Critically ill patients with 2009 influenza A(H1N1) infection in Canada.
JAMA, 302 (2009), pp. 1872-1879
[30.]
G. Vaillant La Ruche, A. Tarantola, P. Barboza.
Epidemic Intelligence Team at InVS. Epidemiology of fatal cases associated with pandemic H1N1 influenza 2009, July 2009-update, 7 July 2009.
Weekly Epidemiologic Record, 84 (2009), pp. 301-308
[31.]
S.A. Webb, V. Pettilä, I. Seppelt, R. Bellomo, M. Bailey, D.J. Cooper, ANZIC Influenza Investigators, et al.
Critical care services and 2009 H1N1 influenza in Australia and New Zealand.
N Engl J Med, 361 (2009), pp. 1925-1934
[32.]
J.K. Louie, M. Acosta, M.C. Samuel, R. Schechter, D.J. Vugia, K. Harriman, et al.
A novel risk factor for a novel virus: obesity and 2009 pandemic influenza A (H1N1).
Clin Infect Dis, 52 (2011), pp. 301-312
[33.]
H. Yu, Z. Feng, T.M. Uyeki, Q. Liao, L. Zhou, L. Feng, et al.
Risk factors for severe illness with 2009 pandemic influenza A (H1N1) virus infection in China.
Clin Infect Dis, 52 (2011), pp. 457-465
[34.]
S. Lucas.
Predictive clinicopathological features derived from systematic autopsy examination of patients who died with A/H1N1 influenza infection in the UK 2009–10 pandemic.
Health Technol Assess, 14 (2010), pp. 83-114
[35.]
C. Fuhrman, I. Bonmarin, D. Bitar, T. Cardoso, N. Duport, M. Herida, et al.
Adult intensive-care patients with 2009 pandemic influenza A(H1N1) infection.
Epidemiol Infect, 139 (2011), pp. 1202-1209
[36.]
P. Santa-Olalla Peralta, M. Cortes-García, M. Vicente-Herrero, C. Castrillo-Villamandos, P. Arias-Bohigas, I. Pachon-del Amo, et al.
Risk factors for disease severity among hospitalised patients with 2009 pandemic influenza A (H1N1) in Spain, April - December 2009.
Euro Surveill, 15 (2010), pp. 19667
[37.]
M.E. Falagas, P.K. Koletsi, E. Baskouta, P.I. Rafailidis, G. Dimopoulos, D.E. Karageorgopoulos.
Pandemic A(H1N1) 2009 influenza: review of the Southern Hemisphere experience.
Epidemiol Infect, 139 (2011), pp. 27-40
[38.]
D. Viasus, J.R. Paño-Pardo, J. Pachón, A. Campins, F. López-Medrano, A. Villoslada, et al.
Factors associated with severe disease in hospitalized adults with pandemic (H1N1) 2009 in Spain.
Clin Microbiol Infect, 17 (2011), pp. 738-746
[39.]
J.S. Nguyen-Van-Tam, P.J. Openshaw, A. Hashim, E.M. Gadd, W.S. Lim, M.G. Semple, et al.
Risk factors for hospitalisation and poor outcome with pandemic A/H1N1 influenza: United Kingdom first wave (May-September 2009).
Thorax, 65 (2010), pp. 645-651
[40.]
L. Satterwhite, A. Mehta, G.S. Martin.
Novel findings from the second wave of adult pH1N1 in the United States.
Crit Care Med, 38 (2010), pp. 2059-2061
[41.]
S. Jain, L. Kamimoto, A.M. Bramley, A.M. Schmitz, S.R. Benoit, J. Louie, et al.
Hospitalized patients with 2009 H1N1 influenza in the United States, April-June 2009.
N Engl J Med, 361 (2009), pp. 1935-1944
[42.]
O.W. Morgan, A. Bramley, A. Fowlkes, D.S. Freedman, T.H. Taylor, P. Gargiullo, et al.
Morbid obesity as a risk factor for hospitalization and death due to 2009 pandemic influenza A(H1N1) disease.
PLoS One, 5 (2010), pp. e9694
[43.]
E. Díaz, A. Rodríguez, I. Martín-Loeches, L. Lorente, M. Del Mar Martín, J.C. Pozo, H1N1 SEMICYUC Working Group, et al.
Impact of obesity in patients infected with 2009 influenza A(H1N1).
Chest, 139 (2010), pp. 382-386
[44.]
E.L. Chippirraz, L. Sorlí, M. Montero, V. Mas, E.L. Granados, C. Vilaplana, et al.
Predictive factors for pneumonia in adults infected with the new pandemic A (H1H1) influenza virus.
Rev Esp Quimioter, 24 (2011), pp. 204-208
[45.]
R. Riquelme, P. Jiménez, A.J. Videla, H. Lopez, J. Chalmers, A. Singanayagam, et al.
Predicting mortality in hospitalized patients with 2009 H1N1 influenza pneumonia.
Int J Tuberc Lung Dis, 15 (2011), pp. 542-566
[46.]
L. Fezeu, C. Julia, A. Henegar, F.B. Hu, D.E. Grobbee, A.P. Kengne, et al.
Obesity is associated with higher risk of intensive care unit admission and death in influenza A (H1N1) patients: a systematic review and meta-analysis.
Obes Rev, 12 (2011), pp. 653-659
[47.]
M.D. Van Kerkhove, K.A. Vandemaele, V. Shinde, V. Shinde, G. Jaramillo-Gutierrez, A. Koukounari, et al.
Risk factors for severe outcomes following 2009 influenza A (H1N1) infection: a global pooled analysis.
PLoS Med, 8 (2011), pp. e1001053
[48.]
V. Zacharioudaki, A. Androulidaki, A. Arranz, G. Vrentzos, A.N. Margioris, C. Tsatsanis.
Adiponectin promotes endotoxin tolerance in macrophages by inducing IRAK-M expression.
J Immunol, 182 (2009), pp. 6444-6451
[49.]
H. Nave, G. Beutel, J.T. Kielstein.
Obesity-related immunodeficiency in patients with pandemic influenza H1N1.
Lancet Infect Dis, 11 (2011), pp. 14-15
[50.]
N. Hagau, A. Slavcovici, D.N. Gonganau, S. Oltean, D.S. Dirzu, E.S. Brezoszki, et al.
Clinical aspects and cytokine response in severe H1N1 influenza A virus infection.
Crit Care, 14 (2010), pp. R203
[51.]
P.A. Sheridan, H.A. Paich, J. Handy, E.A. Karlsson, M.G. Hudgens, A.B. Sammon, et al.
Obesity is associated with impaired immune response to influenza vaccination in humans.
Int J Obes (Lond), 36 (2012), pp. 1072-1077
[52.]
A.G. Smith, P.A. Sheridan, R.J. Tseng, J.F. Sheridan, M.A. Beck.
Selective impairment in dendritic cell function and altered antigen-specific CD8þ T-cell responses in diet-induced obese mice infected with influenza virus.
Immunology, 126 (2009), pp. 268-279
[53.]
E.A. Karlsson, P.A. Sheridan, M.A. Beck.
Diet-induced obesity impairs the T cell memory response to influenza virus infection.
J Immunol, 184 (2010), pp. 3127-3133
[54.]
M.P. Pai, T.P. Lodise Jr..
Oseltamivir and oseltamivir carboxylate pharmacokinetics in obese adults: dose modification for weight is not necessary.
Antimicrob Agents Chemother, 55 (2011), pp. 5640-5645
[55.]
Centers for Disease Control and Prevention (CDC). Updated interim recommendations for the use of antiviral medications in the treatment and prevention of influenza for the 2009–2010 season [accessed 2012 Jun 10]. Available at: http://www.cdc.gov/h1n1flu/recommendations.htm.
[56.]
R.E. Ariano, D.S. Sitar, S.A. Zelenitsky, R. Zarychanski, A. Pisipati, S. Ahern, et al.
Enteric absorption and pharmacokinetics of oseltamivir in critically ill patients with pandemic (H1N1) influenza.
CMAJ, 182 (2010), pp. 357-363
[57.]
J. Mereckiene, S. Cotter, A. Nicoll, D. Levy-Bruhl, A. Ferro, G. Tridente, et al.
National seasonal influenza vaccination survey in Europe, 2008.
Euro Surveill, 13 (2008), pp. 19017
[58.]
K.A. Ward, P.J. Spokes, J.M. McAnulty.
Case-control study of risk factors for hospitalization caused by pandemic (H1N1) 2009.
Emerg Infect Dis, 17 (2011), pp. 1409-1416
[59.]
R.R. Miller 3rd, B.A. Markewitz, R.T. Rolfs, S.M. Brown, K.K. Dascomb, C.K. Grissom, et al.
Clinical findings and demographic factors associated with ICU admission in Utah due to novel 2009 influenza A(H1N1) infection.
Chest, 137 (2010), pp. 752-758
[60.]
I. Martin-Loeches, E. Díaz, L. Vidaur, A. Torres, C. Laborda, R. Granada, et al.
Pandemic and post-pandemic influenza A (H1N1) infection in critically ill patients.
Crit Care, 15 (2011), pp. R286
[61.]
R.T. Yokota, L.M. Skalinski, C.N. Igansi, L.R. De Souza, B.P. Iser, P.O. Reis, et al.
Risk factors for death from pandemic (H1N1) 2009, southern Brazil.
Emerg Infect Dis, 17 (2011), pp. 1467-1471
[62.]
D.L. Thompson, J. Jungk, E. Hancock, C. Smelser, M. Landen, M. Nichols, et al.
Risk factors for 2009 pandemic influenza A (H1N1)-related hospitalization and death among racial/ethnic groups in New Mexico.
Am J Public Health, 101 (2011), pp. 1776-1784
[63.]
L. Fang, J. Lin, C. Chai, Z. Yu.
Risk factors for severe cases of 2009 influenza A (H1N1): a case control study in Zhejiang Province.
China. PLoS One, 7 (2012), pp. e34365
[64.]
C. Launes, J.J. García-García, A. Martínez-Planas, F. Moraga, I. Astigarraga, J. Arístegui, the CIBERESP Cases and Controls in Pandemic Influenza Working Group, et al.
Spain. 2009 H1N1: risk factors for hospitalization in a matched case-control study.
Eur J Pediatr, 171 (2012), pp. 1127-1131
[65.]
J.R. Paño-Pardo, D. Viasus, J. Pachón, A. Campins, F. López-Medrano, A. Villoslada, et al.
Pandemic 2009 A(H1N1) infection requiring hospitalization of elderly Spanish adults.
J Am Geriatr Soc, 60 (2012), pp. 740-744
[66.]
A. Campbell, R. Rodin, R. Kropp, Y. Mao, Z. Hong, J. Vachon, et al.
Risk of severe outcomes among patients admitted to hospital with pandemic (H1N1) influenza.
CMAJ, 182 (2010), pp. 349-355
[67.]
D. Viasus, E. Cordero, J. Rodríguez-Baño, J.A. Oteo, A. Fernández-Navarro, L. Ortega, et al.
Novel Influenza A (H1N1) Study Group of the Spanish Network for Research in Infectious Diseases (REIPI). Changes in epidemiology, clinical features and severity of influenza A (H1N1) 2009 pneumonia in the first post-pandemic influenza season.
Clin Microbiol Infect, 18 (2012), pp. E55-E62
[68.]
H. Yu, Z. Feng, T.M. Uyeki, Q. Liao, L. Zhou, L. Feng, et al.
Risk factors for severe illness with factors for severe illness with 2009 pandemic influenza A (H1N1) virus infection in China.
Clin Infect Dis, 52 (2011), pp. 457-465
[69.]
J.K. Louie, C. Jean, M. Acosta, M.C. Samuel, B.T. Matyas, R. Schechter.
A review of adult mortality due to 2009 pandemic (H1N1) influenza A in California.
PLoS One, 6 (2011), pp. e18221
[70.]
R. Zarychanski, T.L. Stuart, A. Kumar, S. Doucette, L. Elliott, J. Kettner, et al.
Correlates of severe disease in patients with 2009 pandemic influenza (H1N1) virus infection.
CMAJ, 182 (2010), pp. 257-264
[71.]
E. Cordero, T. Aydillo, C. Fariñas, J.R. Paño-Pardo, J. Pachón, D. Viasus, et al.
Immunosupressed patients with pandemic A 2009 (H1N1) virus infection.
Eur J Clin Microbiol Infect Dis, 31 (2012), pp. 547-556
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