A cohort study of severe H1N1 influenza patients with invasive pulmonary aspergillosis_Chinese Journal of Respiratory and Critical Care Medicine

Authors：

DUAN Yishan , CHEN Yusha , LIANG Binmiao ,  OU Xuemei

Department of Respiratory and Critical Care Medicine, West China Hospital of Sichuan University, Chengdu, Sichuan 610041, P. R. China;

Corresponding author：

OU Xuemei, Email: ouxuemei@163.com

Keywords：

Invasive pulmonary aspergillosis; Severe H1N1 influenza; Prognosis; Clinical features

DOI：

10.7507/1671-6205.202007050

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To analyze risk factors, clinical features and outcome factors of invasive pulmonary aspergillosis (IPA) in severe H1N1 patients so as to achieve early diagnosis and improve prognosis.Methods Fifty severe H1N1 influenza patients with IPA admitted to West China Hospital and 64 severe H1N1 influenza patients in the same period matched by age and gender were collected. Patient characteristics, laboratory examinations, radiological imaging, microbiology data and prognostic indicators were involved into analysis.Results The mortality of severe H1N1 influenza patients with IPA was significantly higher than those without IPA (51.6% vs. 32.0%, P=0.036). However, the incidence of IPA in severe H1N1 influenza patients was not related with the patient's age, gender, underlying disease, glucocorticoid use and CD4⁺ T cell count. Serum C-reactive protein level [(125.0±88.8) vs. (86.1±80.1) mg/L, P=0.038] and interleukin-6 level [(148.7±154.2) vs. (81.7±110.2) μg/L, P=0.039] of severe H1N1 influenza patients with IPA were significantly higher than those without IPA. Besides, more patients presented with fever (81.3% vs. 64.0%, P=0.038) and dyspnea (51.6% vs. 24.0%, P=0.003) in severe H1N1 patients with IPA. The radiological imaging of severe H1N1 patients with IPA were mostly characterized by combining with nodular changes on the basis of ground-glass opacity.Conclusion The occurrence of IPA in severe H1N1 influenza patients may be related with pulmonary excessive inflammatory response secondary to viral invasion rather than basic condition of the patient.

Citation： DUAN Yishan, CHEN Yusha, LIANG Binmiao, OU Xuemei. A cohort study of severe H1N1 influenza patients with invasive pulmonary aspergillosis. Chinese Journal of Respiratory and Critical Care Medicine, 2021, 20(5): 310-314. doi: 10.7507/1671-6205.202007050 Copy

1.	Kwon OK, Lee MG, Kim HS, et al. Invasive pulmonary aspergillosis after influenza A infection in an immunocompetent patient. Tuberc Respir Dis (Seoul), 2013, 75(6): 260-263.
2.	Shah MM, Hsiao EI, Kirsch CM, et al. Invasive pulmonary aspergillosis and influenza co-infection in immunocompetent hosts: case reports and review of the literature. Diagn Microbiol Infect Dis, 2018, 91(2): 147-152.
3.	Schauwvlieghe A, Rijnders BJA, Philips N, et al. Invasive aspergillosis in patients admitted to the intensive care unit with severe influenza: a retrospective cohort study. Lancet Respir Med, 2018, 6(10): 782-792.
4.	Huang L, Zhang N, Huang X, et al. Invasive pulmonary aspergillosis in patients with influenza infection: a retrospective study and review of the literature. Clin Respir J, 2019, 13(4): 202-211.
5.	Vanderbeke L, Spriet I, Breynaert C, et al. Invasive pulmonary aspergillosis complicating severe influenza: epidemiology, diagnosis and treatment. Curr Opin Infect Dis, 2018, 31(6): 471-480.
6.	Ku YH, Chan KS, Yang CC, et al. Higher mortality of severe influenza patients with probable aspergillosis than those with and without other coinfections. J Formos Med Assoc, 2017, 116(9): 660-670.
7.	Duan YS, Ou XM, Chen YS, et al. Severe influenza with invasive pulmonary aspergillosis in immunocompetent hosts: a retrospective cohort study. Front Med (Lausanne), 2020, 7: 602732.
8.	Meersseman W, Lagrou K, Maertens J, et al. Invasive aspergillosis in the intensive care unit. Clin Infect Dis, 2007, 45(2): 205-216.
9.	Roosen J, Frans E, Wilmer A, et al. Comparison of premortem clinical diagnoses in critically ill patients and subsequent autopsy findings. Mayo Clin Proc, 2000, 75(6): 562-567.
10.	De Pauw B, Walsh TJ, Donnelly JP, et al. Revised definitions of invasive fungal disease from the European Organization for Research and Treatment of Cancer/Invasive Fungal Infections Cooperative Group and the National Institute of Allergy and Infectious Diseases Mycoses Study Group (EORTC/MSG) Consensus Group. Clin Infect Dis, 2008, 46(12): 1813-1821.
11.	Crum-Cianflone NF. Invasive aspergillosis associated with severe influenza infections. Open Forum Infect Dis, 2016, 3(3): ofw171.
12.	Venkatesh B, Finfer S, Cohen J, et al. Adjunctive glucocorticoid therapy in patients with septic shock. N Engl J Med, 2018, 378(9): 797-808.
13.	Van De Veerdonk FL, Kolwijck E, Lestrade PP, et al. Influenza-associated aspergillosis in critically ill patients. Am J Respir Crit Care Med, 2017, 196(4): 524-527.
14.	Shieh WJ, Blau DM, Denison AM, et al. 2009 pandemic influenza A (H1N1): pathology and pathogenesis of 100 fatal cases in the United States. Am J Pathol, 2010, 177(1): 166-175.
15.	Kang H, Lee KS, Jeong YJ, et al. Computed tomography findings of influenza A (H1N1) pneumonia in adults: pattern analysis and prognostic comparisons. J Comput Assist Tomogr, 2012, 36(3): 285-290.
16.	Guo XJ, Thomas PG. New fronts emerge in the influenza cytokine storm. Semin Immunopathol, 2017, 39(5): 541-550.
17.	Lewis M, Kallenbach J, Ruff P, et al. Invasive pulmonary aspergillosis complicating influenza A pneumonia in a previously healthy patient. Chest, 1985, 87(5): 691-693.
18.	Hartemink KJ, Paul MA, Spijkstra JJ, et al. Immunoparalysis as a cause for invasive aspergillosis?. Intensive Care Med, 2003, 29(11): 2068-2071.
19.	Gershov D, Kim S, Brot N, et al. C-Reactive protein binds to apoptotic cells, protects the cells from assembly of the terminal complement components, and sustains an antiinflammatory innate immune response: implications for systemic autoimmunity. J Exp Med, 2000, 192(9): 1353-1364.
20.	Chiaretti A, Pulitano S, Conti G, et al. Interleukin and neurotrophin up-regulation correlates with severity of H1N1 infection in children: a case-control study. Int J Infect Dis, 2013, 17(12): e1186-e1193.
21.	Volk HD, Reinke P, Docke WD. Clinical aspects: from systemic inflammation to 'immunoparalysis'. Chem Immunol, 2000, 74: 162-177.
22.	Zuniga J, Torres M, Romo J, et al. Inflammatory profiles in severe pneumonia associated with the pandemic influenza A/H1N1 virus isolated in Mexico City. Autoimmunity, 2011, 44(7): 562-570.
23.	Park SY, Lim C, Lee SO, et al. Computed tomography findings in invasive pulmonary aspergillosis in non-neutropenic transplant recipients and neutropenic patients, and their prognostic value. J Infect, 2011, 63(6): 447-456.
24.	Mccullers JA. The co-pathogenesis of influenza viruses with bacteria in the lung. Nat Rev Microbiol, 2014, 12(4): 252-262.
25.	Boch T, Reinwald M, Spiess B, et al. Detection of invasive pulmonary aspergillosis in critically ill patients by combined use of conventional culture, galactomannan, 1-3-beta-D-glucan and Aspergillus specific nested polymerase chain reaction in a prospective pilot study. J Crit Care, 2018, 47: 198-203.

1. Kwon OK, Lee MG, Kim HS, et al. Invasive pulmonary aspergillosis after influenza A infection in an immunocompetent patient. Tuberc Respir Dis (Seoul), 2013, 75(6): 260-263.
2. Shah MM, Hsiao EI, Kirsch CM, et al. Invasive pulmonary aspergillosis and influenza co-infection in immunocompetent hosts: case reports and review of the literature. Diagn Microbiol Infect Dis, 2018, 91(2): 147-152.
3. Schauwvlieghe A, Rijnders BJA, Philips N, et al. Invasive aspergillosis in patients admitted to the intensive care unit with severe influenza: a retrospective cohort study. Lancet Respir Med, 2018, 6(10): 782-792.
4. Huang L, Zhang N, Huang X, et al. Invasive pulmonary aspergillosis in patients with influenza infection: a retrospective study and review of the literature. Clin Respir J, 2019, 13(4): 202-211.
5. Vanderbeke L, Spriet I, Breynaert C, et al. Invasive pulmonary aspergillosis complicating severe influenza: epidemiology, diagnosis and treatment. Curr Opin Infect Dis, 2018, 31(6): 471-480.
6. Ku YH, Chan KS, Yang CC, et al. Higher mortality of severe influenza patients with probable aspergillosis than those with and without other coinfections. J Formos Med Assoc, 2017, 116(9): 660-670.
7. Duan YS, Ou XM, Chen YS, et al. Severe influenza with invasive pulmonary aspergillosis in immunocompetent hosts: a retrospective cohort study. Front Med (Lausanne), 2020, 7: 602732.
8. Meersseman W, Lagrou K, Maertens J, et al. Invasive aspergillosis in the intensive care unit. Clin Infect Dis, 2007, 45(2): 205-216.
9. Roosen J, Frans E, Wilmer A, et al. Comparison of premortem clinical diagnoses in critically ill patients and subsequent autopsy findings. Mayo Clin Proc, 2000, 75(6): 562-567.
10. De Pauw B, Walsh TJ, Donnelly JP, et al. Revised definitions of invasive fungal disease from the European Organization for Research and Treatment of Cancer/Invasive Fungal Infections Cooperative Group and the National Institute of Allergy and Infectious Diseases Mycoses Study Group (EORTC/MSG) Consensus Group. Clin Infect Dis, 2008, 46(12): 1813-1821.
11. Crum-Cianflone NF. Invasive aspergillosis associated with severe influenza infections. Open Forum Infect Dis, 2016, 3(3): ofw171.
12. Venkatesh B, Finfer S, Cohen J, et al. Adjunctive glucocorticoid therapy in patients with septic shock. N Engl J Med, 2018, 378(9): 797-808.
13. Van De Veerdonk FL, Kolwijck E, Lestrade PP, et al. Influenza-associated aspergillosis in critically ill patients. Am J Respir Crit Care Med, 2017, 196(4): 524-527.
14. Shieh WJ, Blau DM, Denison AM, et al. 2009 pandemic influenza A (H1N1): pathology and pathogenesis of 100 fatal cases in the United States. Am J Pathol, 2010, 177(1): 166-175.
15. Kang H, Lee KS, Jeong YJ, et al. Computed tomography findings of influenza A (H1N1) pneumonia in adults: pattern analysis and prognostic comparisons. J Comput Assist Tomogr, 2012, 36(3): 285-290.
16. Guo XJ, Thomas PG. New fronts emerge in the influenza cytokine storm. Semin Immunopathol, 2017, 39(5): 541-550.
17. Lewis M, Kallenbach J, Ruff P, et al. Invasive pulmonary aspergillosis complicating influenza A pneumonia in a previously healthy patient. Chest, 1985, 87(5): 691-693.
18. Hartemink KJ, Paul MA, Spijkstra JJ, et al. Immunoparalysis as a cause for invasive aspergillosis?. Intensive Care Med, 2003, 29(11): 2068-2071.
19. Gershov D, Kim S, Brot N, et al. C-Reactive protein binds to apoptotic cells, protects the cells from assembly of the terminal complement components, and sustains an antiinflammatory innate immune response: implications for systemic autoimmunity. J Exp Med, 2000, 192(9): 1353-1364.
20. Chiaretti A, Pulitano S, Conti G, et al. Interleukin and neurotrophin up-regulation correlates with severity of H1N1 infection in children: a case-control study. Int J Infect Dis, 2013, 17(12): e1186-e1193.
21. Volk HD, Reinke P, Docke WD. Clinical aspects: from systemic inflammation to 'immunoparalysis'. Chem Immunol, 2000, 74: 162-177.
22. Zuniga J, Torres M, Romo J, et al. Inflammatory profiles in severe pneumonia associated with the pandemic influenza A/H1N1 virus isolated in Mexico City. Autoimmunity, 2011, 44(7): 562-570.
23. Park SY, Lim C, Lee SO, et al. Computed tomography findings in invasive pulmonary aspergillosis in non-neutropenic transplant recipients and neutropenic patients, and their prognostic value. J Infect, 2011, 63(6): 447-456.
24. Mccullers JA. The co-pathogenesis of influenza viruses with bacteria in the lung. Nat Rev Microbiol, 2014, 12(4): 252-262.
25. Boch T, Reinwald M, Spiess B, et al. Detection of invasive pulmonary aspergillosis in critically ill patients by combined use of conventional culture, galactomannan, 1-3-beta-D-glucan and Aspergillus specific nested polymerase chain reaction in a prospective pilot study. J Crit Care, 2018, 47: 198-203.

Chinese Journal of Respiratory and Critical Care Medicine

A cohort study of severe H1N1 influenza patients with invasive pulmonary aspergillosis

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