Expert consensus on prevention of mucormycosis secondary to viral respiratory infection_West China Medical Journal

Authors：

QU Junyan ¹ , LIU Xinyao ² , QUAN Min ¹ , QIAO Fu ³ , CHEN Yijian ⁴ , LIU Jing ⁵ , PENG Hong ⁶ , PAN Jue ⁷ , GU Li ⁸ , ZHOU Zhihui ⁹ , YANG Wenjie ¹⁰ , GE Ying ¹¹ , ZHANG Jingping ¹² , LI Jiabin ¹³ , WU Anhua ¹⁴ ,  ZONG Zhiyong ^1,2

1. Center of Infectious Diseases, West China Hospital, Sichuan University, Chengdu, Sichuan 610041, P. R. China;
2. Laboratory of Pathogen Research, West China Hospital, Sichuan University, Chengdu, Sichuan 610041, P. R. China;
3. Department of Infection Control, West China Hospital, Sichuan University, Chengdu, Sichuan 610041, P. R. China;
4. Institute of Antibiotics, Huashan Hospital, Fudan University, Shanghai 200040, P. R. China;
5. Department of Infectious Diseases, the Third Affiliated Hospital of Sun Yat-sen University, Guangzhou, Guangdong 510630, P. R. China;
6. Department of Infectious Diseases, Guizhou Provincial People’s Hospital, Guiyang, Guizhou 550002, P. R. China;
7. Department of Infectious Diseases, Zhongshan Hospital, Fudan University, Shanghai 200032, P. R. China;
8. Department of Infectious Diseases, Beijing Chaoyang Hospital, Capital Medical University, Beijing 100020, P. R. China;
9. Department of Infectious Disease, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang 310016, P. R. China;
10. Department of Infectious Diseases, Tianjin First Central Hospital, Tianjin 300192, P. R. China;
11. Department of Infectious Diseases, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences, Beijing 100000, P. R. China;
12. Department of Infection Diseases, the First Affiliated Hospital of China Medical University, Shenyang, Liaoning 11000l, P. R. China;
13. Department of Infectious Diseases, the First Affiliated Hospital of Anhui Medical University, Hefei, Anhui 230000, P. R. China;
14. Center for Infection Control, Xiangya Hospital, Central South University, Changsha, Hunan 410008, P. R. China;

Corresponding author：

ZONG Zhiyong, Email: zongzhiy@scu.edu.cn

Keywords：

Respiratory virus; mucor; mucormycosis; prevention; consensus

DOI：

10.7507/1002-0179.202502125

Video：

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Abstract Full text Figures/Tables Video References Cited by

The epidemiology of respiratory viruses in China are complex and diverse, and viral infections are prone to secondary mucormycosis, posing serious challenges to clinical and public health. The consensu is formulated by domestic experts organized by the Center of Infectious Diseases of West China Hospital of Sichuan University, aiming to identify high-risk groups of respiratory virus infection secondary to mucormycosis, and put forward systematic prevention suggestions. The content covers four aspects: education and training, personal protection, early diagnosis and treatment, and infection control, forming 11 specific recommended measures. It also points out the prevention measures that are still controversial or lack evidence and future research directions, in order to improve the understanding of clinical medical staff, optimize prevention and control strategies, and reduce the risk of secondary mucormycosis.

Citation： QU Junyan, LIU Xinyao, QUAN Min, QIAO Fu, CHEN Yijian, LIU Jing, PENG Hong, PAN Jue, GU Li, ZHOU Zhihui, YANG Wenjie, GE Ying, ZHANG Jingping, LI Jiabin, WU Anhua, ZONG Zhiyong. Expert consensus on prevention of mucormycosis secondary to viral respiratory infection. West China Medical Journal, 2025, 40(3): 354-362. doi: 10.7507/1002-0179.202502125 Copy

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5.	Himaal Dev GJ, Venkategowda PM, Sutar AR, et al. Intestinal mucormycosis in an adult with H1N1 pneumonia on extracorporeal membrane oxygenation. Ann Card Anaesth, 2021, 24(1): 92-94.
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25.	Schmidt S, Tramsen L, Schneider A, et al. Immunotherapeutic strategies against mucormycosis in haematopoietic stem cell transplantation. Mycoses, 2014, 57(Suppl 3): 8-12.
26.	Davari HR, Malekhossini SA, Salahi HA, et al. Outcome of mucormycosis in liver transplantation: four cases and a review of literature. Exp Clin Transplant, 2003, 1(2): 147-152.
27.	Patel C, Parmar K, Patel D, et al. Effect of corticosteroid therapy on mortality in COVID-19 patients-a systematic review and meta-analysis. Rev Med Virol, 2022, 32(5): e2386.
28.	Roden MM, Zaoutis TE, Buchanan WL, et al. Epidemiology and outcome of zygomycosis: a review of 929 reported cases. Clin Infect Dis, 2005, 41(5): 634-653.
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32.	Lee TH, Chen JJ, Wu CY, et al. Immunosenescence, gut dysbiosis, and chronic kidney disease: interplay and implications for clinical management. Biomed J, 2024, 47(2): 100638.
33.	Rizik S, Bentur L, Bar-Yoseph R, et al. Clinical significance of mucor in airway culture of immunocompetent patients with chronic lung disease. Pediatr Infect Dis J, 2024, 43(10): 987-990.
34.	Duffy J, Harris J, Gade L, et al. Mucormycosis outbreak associated with hospital linens. Pediatr Infect Dis J, 2014, 33(5): 472-476.
35.	梁官钊, 刘维达. 2019 年欧洲毛霉病诊疗指南解读. 中国真菌学杂志, 2021, 16(2): 116-120.
36.	Basílio FM, Hammerschmidt M, Mukai MM, et al. Mucormycosis and chromoblastomycosis occurring in a patient with leprosy type 2 reaction under prolonged corticosteroid and thalidomide therapy. An Bras Dermatol, 2012, 87(5): 767-771.
37.	Skiada A, Pavleas I, Drogari-Apiranthitou M. Epidemiology and diagnosis of mucormycosis: an update. J Fungi (Basel), 2020, 6(4): 265.
38.	Nasiri MJ, Danaei B, Deravi N, et al. Impact of educational interventions on the prevention of influenza: a systematic review. Front Public Health, 2022, 10: 978456.
39.	Zhou X, Zhao X, Liu J, et al. Effectiveness of educational intervention on influenza vaccine uptake: a meta-analysis of randomized controlled trials. Iran J Public Health, 2020, 49(12): 2256-2263.
40.	Du P, Jin S, Lu S, et al. Strategies to increase the coverage of influenza and pneumonia vaccination in older adults: a systematic review and network meta-analysis. Age Ageing, 2024, 53(3): afae035.
41.	Ceccarelli A, Munafò G, Sintoni F, et al. Effectiveness of general practitioners’ involvement in adult vaccination practices: a systematic review and meta-analysis of international evidence. Vaccines (Basel), 2024, 12(12): 1438.
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1. Sigera LSM, Denning DW. A systematic review of the therapeutic outcome of mucormycosis. Open Forum Infect Dis, 2023, 11(1): ofad704.
2. Narayanan S, Chua JV, Baddley JW. Coronavirus disease 2019-associated mucormycosis: risk factors and mechanisms of disease. Clin Infect Dis, 2022, 74(7): 1279-1283.
3. Hoenigl M, Seidel D, Carvalho A, et al. The emergence of COVID-19 associated mucormycosis: a review of cases from 18 countries. Lancet Microbe, 2022, 3(7): e543-e552.
4. Ahmadikia K, Hashemi SJ, Khodavaisy S, et al. The double-edged sword of systemic corticosteroid therapy in viral pneumonia: a case report and comparative review of influenza-associated mucormycosis versus COVID-19 associated mucormycosis. Mycoses, 2021, 64(8): 798-808.
5. Himaal Dev GJ, Venkategowda PM, Sutar AR, et al. Intestinal mucormycosis in an adult with H1N1 pneumonia on extracorporeal membrane oxygenation. Ann Card Anaesth, 2021, 24(1): 92-94.
6. 成人急性呼吸道病毒感染急诊诊疗专家共识组. 成人急性呼吸道病毒感染急诊诊疗专家共识. 中华急诊医学杂志, 2021, 30(12): 1417-1428.
7. World Health Organization. Clinical management of severe acute respiratory infection when novel coronavirus (nCoV) infection is suspected. Geneva: World Health Organization, 2020.
8. Dadwal SS, Hohl TM, Fisher CE, et al. American Society of Transplantation and Cellular Therapy series, 2: management and prevention of aspergillosis in hematopoietic cell transplantation recipients. Transplant Cell Ther, 2021, 27(3): 201-211.
9. 中国医师协会血液科医师分会, 中国侵袭性真菌感染工作组. 血液病/恶性肿瘤患者侵袭性真菌病的诊断标准与治疗原则(第六次修订版). 中华内科杂志, 2020, 59(10): 754-763.
10. Denning DW. Global incidence and mortality of severe fungal disease. Lancet Infect Dis, 2024, 24(7): e428-e438.
11. GBD 2016 Lower Respiratory Infections Collaborators. Estimates of the global, regional, and national morbidity, mortality, and aetiologies of lower respiratory infections in 195 countries, 1990-2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet Infect Dis, 2018, 18(11): 1191-1210.
12. Chow EJ, Uyeki TM, Chu HY. The effects of the COVID-19 pandemic on community respiratory virus activity. Nat Rev Microbiol, 2023, 21(3): 195-210.
13. Yang J, Lin S, Shu Y. Challenges and strategies for influenza response after COVID-19 pandemic. Infect Dis Immun, 2024, 4(2): 51-55.
14. Abdoli A, Falahi S, Kenarkoohi A. COVID-19-associated opportunistic infections: a snapshot on the current reports. Clin Exp Med, 2022, 22(3): 327-346.
15. Zhou F, Yu T, Du R, et al. Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study. Lancet, 2020, 395(10229): 1054-1062.
16. Salazar F, Bignell E, Brown GD, et al. Pathogenesis of respiratory viral and fungal coinfections. Clin Microbiol Rev, 2022, 35(1): e0009421.
17. Schauwvlieghe AFAD, 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.
18. Song G, Liang G, Liu W. Fungal co-infections associated with global COVID-19 pandemic: a clinical and diagnostic perspective from China. Mycopathologia, 2020, 185(4): 599-606.
19. Banerjee M, Pal R, Bhadada SK. Intercepting the deadly trinity of mucormycosis, diabetes and COVID-19 in India. Postgrad Med J, 2022, 98(e2): e108-e109.
20. Chen H, Yu L, Wang L, et al. Demographic characteristics and risk factors for invasive fungal sinusitis in the context of COVID-19: a systematic review and meta-analysis. Int J Infect Dis, 2024, 144: 107054.
21. Klekotka RB, Mizgała E, Król W. The etiology of lower respiratory tract infections in people with diabetes. Pneumonol Alergol Pol, 2015, 83(5): 401-408.
22. Shah NN, Khan Z, Ahad H, et al. Mucormycosis an added burden to COVID-19 patients: an in-depth systematic review. J Infect Public Health, 2022, 15(11): 1299-1314.
23. Tissot F, Agrawal S, Pagano L, et al. ECIL-6 guidelines for the treatment of invasive candidiasis, aspergillosis and mucormycosis in leukemia and hematopoietic stem cell transplant patients. Haematologica, 2017, 102(3): 433-444.
24. Bao J, Liu C, Dong Y, et al. Clinical manifestations of pulmonary mucormycosis in recipients of allogeneic hematopoietic stem cell transplantation: a 21-case series report and literature review. Can Respir J, 2022, 2022: 1237125.
25. Schmidt S, Tramsen L, Schneider A, et al. Immunotherapeutic strategies against mucormycosis in haematopoietic stem cell transplantation. Mycoses, 2014, 57(Suppl 3): 8-12.
26. Davari HR, Malekhossini SA, Salahi HA, et al. Outcome of mucormycosis in liver transplantation: four cases and a review of literature. Exp Clin Transplant, 2003, 1(2): 147-152.
27. Patel C, Parmar K, Patel D, et al. Effect of corticosteroid therapy on mortality in COVID-19 patients-a systematic review and meta-analysis. Rev Med Virol, 2022, 32(5): e2386.
28. Roden MM, Zaoutis TE, Buchanan WL, et al. Epidemiology and outcome of zygomycosis: a review of 929 reported cases. Clin Infect Dis, 2005, 41(5): 634-653.
29. Spellberg B, Edwards J Jr, Ibrahim A. Novel perspectives on mucormycosis: pathophysiology, presentation, and management. Clin Microbiol Rev, 2005, 18(3): 556-569.
30. Cornely OA, Alastruey-Izquierdo A, Arenz D, et al. Global guideline for the diagnosis and management of mucormycosis: an initiative of the European Confederation of Medical Mycology in cooperation with the Mycoses Study Group Education and Research Consortium. Lancet Infect Dis, 2019, 19(12): e405-e421.
31. Corzo-León DE, Chora-Hernández LD, Rodríguez-Zulueta AP, et al. Diabetes mellitus as the major risk factor for mucormycosis in Mexico: epidemiology, diagnosis, and outcomes of reported cases. Med Mycol, 2018, 56(1): 29-43.
32. Lee TH, Chen JJ, Wu CY, et al. Immunosenescence, gut dysbiosis, and chronic kidney disease: interplay and implications for clinical management. Biomed J, 2024, 47(2): 100638.
33. Rizik S, Bentur L, Bar-Yoseph R, et al. Clinical significance of mucor in airway culture of immunocompetent patients with chronic lung disease. Pediatr Infect Dis J, 2024, 43(10): 987-990.
34. Duffy J, Harris J, Gade L, et al. Mucormycosis outbreak associated with hospital linens. Pediatr Infect Dis J, 2014, 33(5): 472-476.
35. 梁官钊, 刘维达. 2019 年欧洲毛霉病诊疗指南解读. 中国真菌学杂志, 2021, 16(2): 116-120.
36. Basílio FM, Hammerschmidt M, Mukai MM, et al. Mucormycosis and chromoblastomycosis occurring in a patient with leprosy type 2 reaction under prolonged corticosteroid and thalidomide therapy. An Bras Dermatol, 2012, 87(5): 767-771.
37. Skiada A, Pavleas I, Drogari-Apiranthitou M. Epidemiology and diagnosis of mucormycosis: an update. J Fungi (Basel), 2020, 6(4): 265.
38. Nasiri MJ, Danaei B, Deravi N, et al. Impact of educational interventions on the prevention of influenza: a systematic review. Front Public Health, 2022, 10: 978456.
39. Zhou X, Zhao X, Liu J, et al. Effectiveness of educational intervention on influenza vaccine uptake: a meta-analysis of randomized controlled trials. Iran J Public Health, 2020, 49(12): 2256-2263.
40. Du P, Jin S, Lu S, et al. Strategies to increase the coverage of influenza and pneumonia vaccination in older adults: a systematic review and network meta-analysis. Age Ageing, 2024, 53(3): afae035.
41. Ceccarelli A, Munafò G, Sintoni F, et al. Effectiveness of general practitioners’ involvement in adult vaccination practices: a systematic review and meta-analysis of international evidence. Vaccines (Basel), 2024, 12(12): 1438.
42. Okoli GN, Reddy VK, Lam OLT, et al. Interventions on health care providers to improve seasonal influenza vaccination rates among patients: a systematic review and meta-analysis of the evidence since 2000. Fam Pract, 2021, 38(4): 524-536.
43. Minozzi S, Lytras T, Gianola S, et al. Comparative efficacy and safety of vaccines to prevent seasonal influenza: a systematic review and network meta-analysis. EClinicalMedicine, 2022, 46: 101331.
44. Ferdinands JM, Blanton LH, Alyanak E, et al. Protection against influenza hospitalizations from enhanced influenza vaccines among older adults: a systematic review and network meta-analysis. J Am Geriatr Soc, 2024, 72(12): 3875-3889.
45. Presa J, Arranz-Herrero J, Alvarez-Losa L, et al. Influenza vaccine outcomes: a meta-analysis revealing morbidity benefits amid low infection prevention. Eur Respir Rev, 2025, 34(175): 240144.
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West China Medical Journal

Expert consensus on prevention of mucormycosis secondary to viral respiratory infection

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