COVID-19 aspects as risk factors for coccidioidomycosis infection or reactivation: a systematic review

Authors

DOI:

https://doi.org/10.33448/rsd-v11i12.35062

Keywords:

Coccidioidomycosis; Coccidioides spp.; COVID-19; Post-COVID-19; Secondary Infection; Neglected diseases.

Abstract

Coccidioidomycosis is a deep mycosis caused by dimorphic fungi of the genus Coccidioides. Clinical manifestations of Coccidioides spp. infection can be considerably diverse. The main clinical form of coccidioidomycosis is respiratory infection which most frequent signs and symptoms are cough, dyspnea, chest pain, fever, arthralgia, myalgia, fatigue, and weight loss. Pulmonary coccidioidomycosis, especially acute pneumonia, can be easily confused with other pneumopathies, including COVID-19. The aim of this manuscript is to perform a systematic review coccidioidomycosis cases in patients with SARS-CoV-2 infection or individuals who developed this mycosis in the period after COVID-19. The context of COVID-19 and its treatment with corticosteroids cn ease the infection with Coccidioides spp. or reactivation of latent infections of this fungus. The main life risk for those affected by coccidioidomycosis concurrent or subsequent to COVID-19 is late diagnosis. The use of corticosteroids in the treatment of COVID-19 and diabetes are the most relevant risk factors for the development of infection with Coccidioides spp. or the reactivation of latent fungal infection. Laboratory biopsy and culture tests of patient’s airways and skin lesions, as well as serology to diagnose coccidioidomycosis, should be incorporated into the routine evaluation of secondary infections in COVID-19 and pneumopathies subsequent to SARS-CoV-2 infection, mainly among more susceptible individuals in regions of high endemicity.

References

Adetiloye, A. O., Ghosh, K., Villavicencio, C., Velasquez, M. R., Oliva, M., Delgado Lazo, V., Trenard, N., & Poor, A. (2022). Chronic Pulmonary Aspergillosis Occurring Post Treatment of COVID-19 Pneumonia with Tocilizumab. C61. Breaking the Mold, A4518–A4518. https://doi.org/10.1164/ajrccm-conference.2022.205.1_MeetingAbstracts.A4518

Aduroja, O., Okudo, J., & Padilla, A. (2021). Disseminated Coccidioidomycosis Presenting as Septic Shock with Multiorgan Failure. Case Reports in Infectious Diseases, 2021, 1–6. https://doi.org/10.1155/2021/8837493

Benedict, K., Williams, S., Beekmann, S. E., Polgreen, P. M., Jackson, B. R., & Toda, M. (2021). Testing Practices for Fungal Respiratory Infections and SARS-CoV-2 among Infectious Disease Specialists, United States. Journal of Fungi, 7(8), 605. https://doi.org/10.3390/jof7080605

Berbudi, A., Rahmadika, N., Tjahjadi, A. I., & Ruslami, R. (2020). Type 2 Diabetes and its Impact on the Immune System. Current Diabetes Reviews, 16(5), 442–449. https://doi.org/10.2174/1573399815666191024085838

Blue, S. A., Devine, J. A., Ruiz, M. P., McDaniel, K., Hartsell, A. R., Pierce, C. J., Johnson, M., Tinglov, A. K., Yang, M., Wu, X., Moya, S., Cross, E., & Starnes, C. A. (2021). Im/Mobility at the US–Mexico Border during the COVID-19 Pandemic. Social Sciences, 10(2), 47. https://doi.org/10.3390/socsci10020047

Boro, R., Iyer, P. C., & Walczak, M. A. (2022). Current Landscape of Coccidioidomycosis. Journal of Fungi, 8(4), 413. https://doi.org/10.3390/jof8040413

Brandt, M. E., Gomez, B. L., & Warnock, D. W. (2011). Histoplasma, Blastomyces, Coccidioides , and Other Dimorphic Fungi Causing Systemic Mycoses. Em J. Versalovic, K. C. Carroll, G. Funke, J. H. Jorgensen, M. L. Landry, & D. W. Warnock (Orgs.), Manual of Clinical Microbiology (1o ed, p. 1902–1918). Wiley. https://doi.org/10.1128/9781555816728.ch120

Brennan-Krohn, T., Yoon, E., Nishino, M., Kirby, J. E., & Riedel, S. (2018). Arthroconidia in lung tissue: An unusual histopathological finding in pulmonary coccidioidomycosis. Human Pathology, 71, 55–59. https://doi.org/10.1016/j.humpath.2017.07.013

Bui, A., Shrivastava, S., & Seda, G. (2022). Disseminated Coccidioidomycosis Following COVID-19. C61. BREAKING THE MOLD, A4511–A4511. https://doi.org/10.1164/ajrccm-conference.2022.205.1_MeetingAbstracts.A4511

Chang, C. C., Senining, R., Kim, J., & Goyal, R. (2020). An Acute Pulmonary Coccidioidomycosis Coinfection in a Patient Presenting With Multifocal Pneumonia With COVID-19. Journal of Investigative Medicine High Impact Case Reports, 8, 232470962097224. https://doi.org/10.1177/2324709620972244

Chen, J. C., Wong, D., Rabi, S., Worswick, S., DeClerck, B., & Gibb, J. (2021). All That Coughs Is Not COVID-19: A Delayed Diagnosis of Disseminated Coccidioidomycosis Following Severe Acute Respiratory Syndrome Coronavirus 2 Infection. Open Forum Infectious Diseases, 8(7), ofab246. https://doi.org/10.1093/ofid/ofab246

Cheon, I. S., Li, C., Son, Y. M., Goplen, N. P., Wu, Y., Cassmann, T., Wang, Z., Wei, X., Tang, J., Li, Y., Marlow, H., Hughes, S., Hammel, L., Cox, T. M., Goddery, E., Ayasoufi, K., Weiskopf, D., Boonyaratanakornkit, J., Dong, H., … Sun, J. (2021). Immune signatures underlying post-acute COVID-19 lung sequelae. Science Immunology, 6(65), eabk1741. https://doi.org/10.1126/sciimmunol.abk1741

Cordeiro, R., Moura, S., Castelo-Branco, D., Rocha, M. F., Lima-Neto, R., & Sidrim, J. J. (2021). Coccidioidomycosis in Brazil: Historical Challenges of a Neglected Disease. Journal of Fungi, 7(2), 85. https://doi.org/10.3390/jof7020085

Crum, N. F. (2022). Coccidioidomycosis: A Contemporary Review. Infectious Diseases and Therapy, 11(2), 713–742. https://doi.org/10.1007/s40121-022-00606-y

Deus Filho, A. de, Deus, A. C. B. de, Meneses, A. de O., Soares, A. S., & Lira, A. L. de A. (2010). Manifestações cutâneo-mucosas da coccidioidomicose: Estudo de trinta casos procedentes dos estados do Piauí e Maranhão. Anais Brasileiros de Dermatologia, 85(1), 45–51. https://doi.org/10.1590/S0365-05962010000100006

Diaz, J. H. (2018). Travel-related risk factors for coccidioidomycosis. Journal of Travel Medicine, 25(1). https://doi.org/10.1093/jtm/tay027

Febbo, J. A., & Ketai, L. (2021). Emerging Pulmonary Infections in Clinical Practice. Advances in Clinical Radiology, 3, 103–124. https://doi.org/10.1016/j.yacr.2021.04.010

Fisher, M. C., Koenig, G. L., White, T. J., San-Blas, G., Negroni, R., Alvarez, I. G., Wanke, B., & Taylor, J. W. (2001). Biogeographic range expansion into South America by Coccidioides immitis mirrors New World patterns of human migration. Proceedings of the National Academy of Sciences, 98(8), 4558–4562. https://doi.org/10.1073/pnas.071406098

Galgiani, J. N., Ampel, N. M., Blair, J. E., Catanzaro, A., Johnson, R. H., Stevens, D. A., & Williams, P. L. (2005). Coccidioidomycosis. Clinical Infectious Diseases, 41(9), 1217–1223. https://doi.org/10.1086/496991

Gorris, M. E., Treseder, K. K., Zender, C. S., & Randerson, J. T. (2019). Expansion of Coccidioidomycosis Endemic Regions in the United States in Response to Climate Change. GeoHealth, 3(10), 308–327. https://doi.org/10.1029/2019GH000209

Han, M., Ma, K., Wang, X., Yan, W., Wang, H., You, J., Wang, Q., Chen, H., Guo, W., Chen, T., Ning, Q., & Luo, X. (2021). Immunological Characteristics in Type 2 Diabetes Mellitus Among COVID-19 Patients. Frontiers in Endocrinology, 12, 596518. https://doi.org/10.3389/fendo.2021.596518

Heaney, A. K., Head, J. R., Broen, K., Click, K., Taylor, J., Balmes, J. R., Zelner, J., & Remais, J. V. (2021). Coccidioidomycosis and COVID-19 Co-Infection, United States, 2020. Emerging Infectious Diseases, 27(5), 1266–1273. https://doi.org/10.3201/eid2705.204661

Hoenigl, M., Seidel, D., Sprute, R., Cunha, C., Oliverio, M., Goldman, G. H., Ibrahim, A. S., & Carvalho, A. (2022). COVID-19-associated fungal infections. Nature Microbiology, 7(8), 1127–1140. https://doi.org/10.1038/s41564-022-01172-2

Huff, D., Ampel, N. M., & Blair, J. E. (2022). Coccidioidomycosis and COVID-19 Infection. An Analysis from a Single Medical Center Within the Coccidioidal Endemic Area. Mycopathologia, 187(2–3), 199–204. https://doi.org/10.1007/s11046-022-00629-6

Kabadi, A. A., Dewolf, S., & Crotty Alexander, L. E. (2022). A Tangled Web of COVID-19, Organizing Pneumonia, Pulmonary Emboli, and Reactivation of Pulmonary Coccidioidomycosis: A Case Report. D107. Show Us What You’ve Got: Interesting Case Reports A5455–A5455. https://doi.org/10.1164/ajrccm-conference.2022.205.1_MeetingAbstracts.A5455

Kirkland, T. N., & Fierer, J. (2018). Coccidioides immitis and posadasii ; A review of their biology, genomics, pathogenesis, and host immunity. Virulence, 9(1), 1426–1435. https://doi.org/10.1080/21505594.2018.1509667

Kirkland, T. N., Stevens, D. A., Hung, C.-Y., Beyhan, S., Taylor, J. W., Shubitz, L. F., Duttke, S. H., Heidari, A., Johnson, R. H., Deresinski, S. C., Lauer, A., & Fierer, J. (2022). Coccidioides Species: A Review of Basic Research: 2022. Journal of Fungi, 8(8), 859. https://doi.org/10.3390/jof8080859

Ko, J., & Lee, M. M. (2021). A Case of Disseminated Coccidioidomycosis in a Patient with a Prolonged Course of COVID-19 Pneumonia. TP98. TP098 fungus among-us - rare fungal case reports, A3997–A3997. https://doi.org/10.1164/ajrccm-conference.2021.203.1_MeetingAbstracts.A3997

Kole, A. (2022). What is the cause of this patient’s persistent fever? JAAPA, 35(8), 62–63. https://doi.org/10.1097/01.JAA.0000832652.64634.66

Kollath, D. R., Miller, K. J., & Barker, B. M. (2019). The mysterious desert dwellers: Coccidioides immitis and Coccidioides posadasii , causative fungal agents of coccidioidomycosis. Virulence, 10(1), 222–233. https://doi.org/10.1080/21505594.2019.1589363

Krauth, D. S., Jamros, C. M., Rivard, S. C., Olson, N. H., & Maves, R. C. (2021). Accelerated Progression of Disseminated Coccidioidomycosis Following SARS-CoV-2 Infection: A Case Report. Military Medicine, 186(11–12), 1254–1256. https://doi.org/10.1093/milmed/usab132

Laniado-Laborín, R., Arathoon, E. G., Canteros, C., Muñiz-Salazar, R., & Rendon, A. (2019). Coccidioidomycosis in Latin America. Medical Mycology, 57(Supplement_1), S46–S55. https://doi.org/10.1093/mmy/myy037

Liang, G., Shen, Y., Lv, G., Zheng, H., Mei, H., Zheng, X., Kong, X., Blechert, O., Li, D., & Liu, W. (2018). Coccidioidomycosis: Imported and possible domestic cases in China: A case report and review, 1958-2017. Mycoses, 61(7), 506–513. https://doi.org/10.1111/myc.12750

Luoma, K., & Crouch, D. R. (2021). Opportunistic Coccidioides Pulmonary Infection Following COVID-19 Pneumonia. TP100. TP100 UNEXPECTED COVID-19 CASE REPORTS, A4082–A4082. https://doi.org/10.1164/ajrccm-conference.2021.203.1_MeetingAbstracts.A4082

Mathew, J., Cherukuri, S. V., & Dihowm, F. (2021). SARS-CoV-2 with concurrent coccidioidomycosis complicated by refractory pneumothorax in a Hispanic male: A case report and literature review. World Journal of Respirology, 11(1), 1–11. https://doi.org/10.5320/wjr.v11.i1.1

Millington, M. A., Nishioka, S. de A., Martins, S. T., Santos, Z. M. G. dos, Lima, F. E. F. de, & Alves, R. V. (2018). Paracoccidioidomicose: Abordagem histórica e perspectivas de implantação da vigilância e controle. Epidemiologia e Serviços de Saúde, 27(esp). https://doi.org/10.5123/S1679-49742018000500002

Mina, S., Yaakoub, H., Annweiler, C., Dubée, V., & Papon, N. (2022). COVID-19 and Fungal Infections: A Double Debacle. Microbes and Infection, 105039. https://doi.org/10.1016/j.micinf.2022.105039

Moher, D., Liberati, A., Tetzlaff, J., & Altman, D. G., The PRISMA Group. (2009). Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement. PLoS Medicine, 6(7), e1000097. https://doi.org/10.1371/journal.pmed.1000097

Moradi, N., & Rivero-Moragrega, P. (2021). Reactivation of pulmonar Coccidioides in the setting of COVID-19 infection. Chest, 160(4), A342. https://doi.org/10.1016/j.chest.2021.07.344

Narang, V. K., Dao, K., Jaratanian, S., D’Assumpcao, C., Kuran, R., Munoz, A., & Heidari, A. (2022). Pulmonary Giant Cavitary Coccidioides With Fungal Ball and Hemoptysis. Journal of Investigative Medicine High Impact Case Reports, 10, 232470962210848. https://doi.org/10.1177/23247096221084852

Nassif, E. F., Maloney, N., Conley, A. P., & Keung, E. Z. (2021). Disseminated Coccidioidomycosis Following COVID-19 Mimicking Metastatic Thoracic Relapse of Well-Differentiated Liposarcoma: A Case Report. Frontiers in Medicine, 8, 715939. https://doi.org/10.3389/fmed.2021.715939

Nielsen, M. C., Reynoso, D., & Ren, P. (2021). Closing the Brief Case: A Fatal Case of SARS-CoV-2 Coinfection with Coccidioides in Texas—Another Challenge We Face. Journal of Clinical Microbiology, 59(8), e00164-21. https://doi.org/10.1128/JCM.00164-21

Norberg C. M. B. M., Norberg, P. R. B. M., Norberg, A. N., Matos, A. A. L., Guerra-Sanches, F. B., Manhães, F. C., & Mangiavacchi, B. M. (2021a). Candida infections associated with COVID-19: an underestimated risk. World Journal of Pharmacy and Pharmaceutical Sciences, 10(9), 48–64. https://doi.org/.20959/wjpps20219-19930

Norberg, A. N., Norberg P. R. B. M., Norberg, C. M. B. M., Guerra-Sanches, F. G. Manhães, F. C., Matos, A. L., & Mangiavacchi B. M. (2021b). Impact of the Aspergillus spp. infection in severe COVID-19 patients. World Journal of Pharmacy and Pharmaceutical Sciences, 10(10), 120–133. https://doi.org/10.20959/wjpps202110-20271

Norberg, P. R. B. M., Manhães, F. C., Matos, A. A. L., Ferreira-Filho, R. M., Norberg, C. M. B. M., Cruz, M. C., Mangiavacchi, B. M., & Norberg, A. N. Migrants, asylum seekers and refugees ar the context of COVID-19: a highly vulnerable key population in pandemic times. World Journal of Pharmacy and Pharmaceutical Sciences, 11(2), 188–199. https://doi.org/10.20959/wjpps20222-21267

Pal, R., & Banerjee, M. (2021). Are people with uncontrolled diabetes mellitus at high risk of reinfections with COVID-19? Primary Care Diabetes, 15(1), 18–20. https://doi.org/10.1016/j.pcd.2020.08.002

Panackal, A. A., Hajjeh, R. A., Cetron, M. S., & Warnock, D. W. (2002). Fungal Infections among Returning Travelers. Clinical Infectious Diseases, 35(9), 1088–1095. https://doi.org/10.1086/344061

Parish, J. M., & Blair, J. E. (2008). Coccidioidomycosis. Mayo Clinic Proceedings, 83(3), 343–349. https://doi.org/10.4065/83.3.343

Passeri, M. F., Villafuerte, D. B., Qazi, R., & Deliz, R. J. (2022). Fulminant Superimposed Covid-19 Pneumonia on Coccidioidomycosis Disseminated Infection. Journal of Infectious Diseases & Case Reports, 1–6. https://doi.org/10.47363/JIDSCR/2022(3)165

Peláez-Jaramillo, C. A., Jiménez-Alzate, M. D. P., Araque-Marin, P., Hung, C.-Y., Castro-Lopez, N., & Cole, G. T. (2021). Lipid Secretion by Parasitic Cells of Coccidioides Contributes to Disseminated Disease. Frontiers in Cellular and Infection Microbiology, 11, 592826. https://doi.org/10.3389/fcimb.2021.592826

Saha, S., Al-Rifai, R. H., & Saha, S. (2021). Diabetes prevalence and mortality in COVID-19 patients: A systematic review, meta-analysis, and meta-regression. Journal of Diabetes and Metabolic Disorders, 20(1), 939–950. https://doi.org/10.1007/s40200-021-00779-2

Sánchez, K. A., & Ambriz, D. P. (2022). Coccidioidomicosis en paciente con COVID-19. Reporte de caso en la Unidad de Terapia Intensiva. Medicina Crítica, 36(4), 249–253. https://doi.org/10.35366/105797

Santelli, A. C., Blair, J. E., & Roust, L. R. (2006). Coccidioidomycosis in patients with diabetes mellitus. The American Journal of Medicine, 119(11), 964–969. https://doi.org/10.1016/j.amjmed.2006.03.033

Segrelles-Calvo, G., de S Araújo, G. R., & Frases, S. (2020). Systemic mycoses: A potential alert for complications in COVID-19 patients. Future Microbiology, 15(14), 1405–1413. https://doi.org/10.2217/fmb-2020-0156

Shah, A. S., Heidari, A., Civelli, V. F., Sharma, R., Clark, C. S., Munoz, A. D., Ragland, A. S., & Johnson, R. H. (2020). The Coincidence of 2 Epidemics, Coccidioidomycosis and SARS-CoV-2: A Case Report. Journal of Investigative Medicine High Impact Case Reports, 8, 232470962093054. https://doi.org/10.1177/2324709620930540

Shah, D. A., James, S., Uche, I. U., Sharer, R., & Radhakrishnan, P. (2021). Cutaneous and Pulmonary Manifestations: COVID-19 Virus or Coccidioidomycosis? Cureus. https://doi.org/10.7759/cureus.15060

Sous, R., Levkiavska, Y., Sharma, R., Jariwal, R., Amodio, D., Johnson, R. H., Heidari, A., & Kuran, R. (2022). Two Cases of Miliary and Disseminated Coccidioidomycosis Following Glucocorticoid Therapy and Literature Review. Journal of Investigative Medicine High Impact Case Reports, 10, 232470962110519. https://doi.org/10.1177/23247096211051928

Stockamp, N. W., & Thompson, G. R. (2016). Coccidioidomycosis. Infectious Disease Clinics of North America, 30(1), 229–246. https://doi.org/10.1016/j.idc.2015.10.008

Sun, H., Saeedi, P., Karuranga, S., Pinkepank, M., Ogurtsova, K., Duncan, B. B., Stein, C., Basit, A., Chan, J. C. N., Mbanya, J. C., Pavkov, M. E., Ramachandaran, A., Wild, S. H., James, S., Herman, W. H., Zhang, P., Bommer, C., Kuo, S., Boyko, E. J., & Magliano, D. J. (2022). IDF Diabetes Atlas: Global, regional and country-level diabetes prevalence estimates for 2021 and projections for 2045. Diabetes Research and Clinical Practice, 183, 109119. https://doi.org/10.1016/j.diabres.2021.109119

Swain, S., Sharma, K., Ray, A., Vyas, S., Singh, G., Joshi, M., Jain, D., Xess, I., Sinha, S., & Wig, N. (2022). Post-COVID-19-Invasive Pulmonary Mycosis. Libyan International Medical University Journal, 07(01), 007–011. https://doi.org/10.1055/s-0042-1750711

Toda, M., Gonzalez, F. J., Fonseca-Ford, M., Franklin, P., Huntington-Frazier, M., Gutelius, B., Kawakami, V., Lunquest, K., McCracken, S., Moser, K., Oltean, H., Ratner, A. J., Raybern, C., Signs, K., Zaldivar, A., Chiller, T. M., Jackson, B. R., & McCotter, O. (2019). Notes from the Field: Multistate Coccidioidomycosis Outbreak in U.S. Residents Returning from Community Service Trips to Baja California, Mexico — July–August 2018. MMWR. Morbidity and Mortality Weekly Report, 68(14), 332–333. https://doi.org/10.15585/mmwr.mm6814a5

Ward, R. A., Thompson, G. R., Villani, A.-C., Li, B., Mansour, M. K., Wuethrich, M., Tam, J. M., Klein, B. S., & Vyas, J. M. (2021). The Known Unknowns of the Immune Response to Coccidioides. Journal of Fungi, 7(5), 377. https://doi.org/10.3390/jof7050377

Williams, S. L., & Chiller, T. (2022). Update on the Epidemiology, Diagnosis, and Treatment of Coccidioidomycosis. Journal of Fungi, 8(7), 666. https://doi.org/10.3390/jof8070666

Zavala, A., & Stark, C. M. (2021). Chest Pain and Fever in a Healthcare Provider During the Global Coronavirus Pandemic. Military Medicine, usab435. https://doi.org/10.1093/milmed/usab435

Published

23/09/2022

How to Cite

NORBERG, A. N. .; NORBERG, P. R. B. M. .; MANHÃES, F. C. .; MANGIAVACCHI, B. M. .; LOPES, S. de O. .; FERREIRA FILHO, R. M. .; FAIAL, L. C. M.; BORGES, T. R. B. .; NUNES, C. dos R. .; COLETE, C. C. F. A. COVID-19 aspects as risk factors for coccidioidomycosis infection or reactivation: a systematic review. Research, Society and Development, [S. l.], v. 11, n. 12, p. e526111235062, 2022. DOI: 10.33448/rsd-v11i12.35062. Disponível em: https://rsdjournal.org/index.php/rsd/article/view/35062. Acesso em: 5 nov. 2024.

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Health Sciences