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The International Journal on Orbital Disorders, Oculoplastic and Lacrimal Surgery
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Review Articles

Immunopathology of COVID-19 and its implications in the development of rhino-orbital-cerebral mucormycosis: a major review

ORCID Icon, ORCID Icon, ORCID Icon &
Pages 670-679 | Received 27 Dec 2021, Accepted 01 Jul 2022, Published online: 20 Jul 2022

References

  • Gamaletsou MN, Sipsas NV, Roilides E. Rhino-orbital-cerebral mucormycosis. Curr Infect Dis Rep. 2012;14(4):423–434. doi:10.1007/s11908-012-0272-6.
  • Chakrabarti A, Das A, Sharma A, Panda N, Das S, Gupta KL, et al. Ten Years’ experience in zygomycosis at a tertiary care centre in India. J Infect. 2001;42(4):261–266. doi:10.1053/jinf.2001.0831.
  • Spellberg B, Edwards J, Ibrahim A. Novel perspectives on mucormycosis. Pathophysiology, presentation and management. Clin Microbiol Rev. 2005;18(3):556–569. doi:10.1128/CMR.18.3.556-569.2005.
  • Ribes JA, Vanover-Sams CL, Baker DJ. Zygomycete in human disease. Clin Microbiol Rev. 2000;13(2):236–301. doi:10.1128/CMR.13.2.236.
  • International Diabetes Federation. 2020. https://idf.org/our-network/regionsmembers/south-eastasia/members/94-india.html. Accessed February 28, 2021
  • Sugar AM. Agents of mucormycosis and related species. In: Mandell G, Bennett J, Dolin R, eds. Principles and Practice of Infectious Diseases. 6th ed. Philadelphia, PA: Elsevier; 2005:2979.
  • Ibrahim AS, Je E, Sg F. Zygomycosis. In: Dismukes W, Pappas P, Sobel J, eds. Clinical Mycology. New York, NY: Oxford University Press; 2003:241–251.
  • Zhou P, Liu Z, Chen Y, Xiao Y, Huang X, Fan XG. Bacterial and fungal infections in COVID-19 patients: a matter of concern. Infect Control Hosp Epidemiol. 2020;41(9):1124–1125. doi:10.1017/ice.2020.156.
  • Chen X, Liao B, Cheng L, Peng X, Xu X, Li Y, et al. The microbial coinfection in COVID-19. Appl Microbiol Biotechnol. 2020;104(18):7777–7785. doi:10.1007/s00253-020-10814-6.
  • White PL, Dhillon R, Hughes H, Wise MP, Backx M. COVID-19 and fungal infection: the need for a strategic approach. Lancet Microbe. 2020;1(5):e196. doi:10.1016/S2666-5247(20)30127-0.
  • Mehta S, Pandey A. Rhino-orbital mucormycosis associated with COVID-19. Cureus. 2020;12:e10726.
  • Waizel-Haiat S, Guerrero-Paz JA, Sanchez-Hurtado L, Calleja-Alarcon S, Romero-Gutierrez L. A case of fatal rhino-orbital Mucormycosis associated with new onset diabetic ketoacidosis and COVID-19. Cureus. 2021;13(2):e13163. doi:10.7759/cureus.13163.
  • Sen M, Lahane S, Lahane TP, Parekh R, Honavar SG. Mucor in a viral land: a tale of two pathogens. Indian J Ophthalmol. 2021;69(2):244–252. doi:10.4103/ijo.IJO_3774_20.
  • Natesan SK, Chandrasekar PH. Isavuconazole for the treatment of invasive aspergillosis and mucormycosis: current evidence, safety, efficacy, and clinical recommendations. Infect Drug Resist. 2016;9:291–300. doi:10.2147/IDR.S102207.
  • Brosnahan SB, Jonkman AH, Kugler MC, Munger JS, Kaufman DA. COVID-19 and respiratory system disorders: current knowledge, future clinical and translational research questions. Arterioscler Thromb Vasc Biol. 2020;40(11):2586–2597. doi:10.1161/ATVBAHA.120.314515.
  • Wang Q, Zhang Y, Wu L, Niu S, Song C, Zhang Z, et al. Structural and functional basis of SARS-CoV-2 entry by using human ACE2. Cell. 2020;181(4):894–904. doi:10.1016/j.cell.2020.03.045.
  • Xu X, Chen P, Wang J, Feng J, Zhou H, Li X, et al. Evolution of the novel coronavirus from the ongoing Wuhan outbreak and modeling of its spike protein for risk of human transmission. Life Sci. 2020;63(3):457–460. doi:10.1007/s11427-020-1637-5.
  • Koparal M, Kurt E, Altuntas EE, Dogan F. Assessment of mucociliary clearance as an indicator of nasal function in patients with COVID-19: a cross-sectional study. Eur Arch Otorhinolaryngol. 2020;13:1–6.
  • Chilvers MA, McKean M, Rutman A, Myint BS, Silverman M, O’-Callaghan C. The effects of coronavirus on human nasal ciliated respiratory epithelium. Eur Respir J. 2001;18(6):965–970. doi:10.1183/09031936.01.00093001.
  • Bouchara JP, Oumeziane NA, Lissitzky JC, Larcher G, Tronchin G, Chabasse D. Attachment of spores of the human pathogenic fungus Rhizopus oryzae to extracellular matrix components. Eur J Cell Biol. 1996;70:76–83.
  • Huang Y, Yang C, Xu XF, Xu W, Liu SW. Structural and functional properties of SARS-CoV-2 spike protein: potential antivirus drug development for COVID-19. Acta Pharmacol Sin. 2020;3:1–9.
  • Ou X, Liu Y, Lei X, Li P, Mi D, Ren L, et al. Characterization of spike glycoprotein of SARS-CoV-2 on virus entry and its immune cross-reactivity with SARS-CoV. Nat Commun. 2020;11(1):1620. doi:10.1038/s41467-020-15562-9.
  • Shang J, Ye G, Shi K. Structural basis of receptor recognition by SARS-CoV-2. Nature. 2020;581(7807):221–224. doi:10.1038/s41586-020-2179-y.
  • Versteeg GA, Ps VDN, Bredenbeek PJ, Spaan WJM. The coronavirus spike protein induces endoplasmic reticulum stress and upregulation of intracellular chemokine mRNA concentrations. J Virol. 2007;81(20):10981–10990. doi:10.1128/JVI.01033-07.
  • Chu H, Chan CM, Zhang X, Wang Y, Yuan S, Zhou J, et al. Middle East respiratory syndrome coronavirus and bat coronavirus HKU9 both can utilize GRP78 for attachment onto host cells. J Biol Chem. 2018;293(30):11709–11726. doi:10.1074/jbc.RA118.001897.
  • Sabirli R, Koseler A, Goren T, Turkcuer I, Kurt O. High GRP78 levels in Covid-19 infection: a case-control study. Life Sci. 2021;265:118781. doi:10.1016/j.lfs.2020.118781.
  • Köseler A, Sabirli R, Gören T, Türkçüer İ, Kurt Ö. Endoplasmic reticulum stress markers in SARS-COV-2 infection and pneumonia: case-control study. In Vivo. 2020;34(3 suppl):1645–1650. doi:10.21873/invivo.11956.
  • Liu M, Spellberg B, Phan QT, Fu Y, Fu Y, Lee AS, et al. The endothelial cell receptor GRP78 is required for mucormycosis pathogenesis in diabetic mice. J Clin Invest. 2010;120(6):1914–1924. doi:10.1172/JCI42164.
  • Alqarihi A, Gebremariam T, Gu Y, Swidergall M, Alkhazraji S, Soliman SSM, et al. GRP78 and integrins play different roles in host cell invasion during mucormycosis. MBio. 2020;2(11):01087–20.
  • Feng Z, Diao B, Wang R, Wang G, Wang C, Tan Y, et al. The novel severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) directly decimates human spleens and lymph nodes. medRxiv; 2020.
  • Gordon DE, Jang GM, Bouhaddou M, Xu J, Obernier K, White KM, et al. A SARS-CoV-2 protein interaction map reveals targets for drug repurposing. Nature. 2020;583(7816):1–13. doi:10.1038/s41586-020-2286-9.
  • Dirk BS, Pawlak EN, Johnson AL, Van Nynatten LR, Jacob RA, Heit B, et al. HIV-1 Nef sequesters MHC-I intracellularly by targeting early stages of endocytosis and recycling. Sci Rep. 2016;6(1):37021. doi:10.1038/srep37021.
  • Dirk BS, Heit B, Dikeakos JD. Visualizing interactions between HIV-1 nef and host cellular proteins using ground-state depletion microscopy. AIDS Res Hum Retroviruses. 2015;31(7):671–672. doi:10.1089/aid.2014.0333.
  • Ghuman H, Voelz K. Innate and adaptive immunity to mucorales. J Fungi (Basel). 2017;3(3):48. doi:10.3390/jof3030048.
  • López-Muñoz A, Nicolás FE, García-Moreno D, Pérez-Oliva AB, Navarro-Mendoza MI, Hernández-Oñate MA, et al. An adult zebrafish model reveals that Mucormycosis induces apoptosis of infected macrophages. Sci Rep. 2018;8(1):12802. doi:10.1038/s41598-018-30754-6.
  • Waldorf AR, Levitz SM, Diamond RD. In vivo broncho alveolar macrophage defense against Rhizopus oryzae and Aspergillus fumigatus. J Infect Dis. 1984;150:752–760.
  • Lamichhane PP, Samarasinghe AE. The role of innate leukocytes during influenza virus infection. J Immunol Res. 2019;12:8028725.
  • Rosales C. Neutrophils at the crossroads of innate and adaptive immunity. J Leukoc Biol. 2020;108(1):377–396. doi:10.1002/JLB.4MIR0220-574RR.
  • Barr FD, Ochsenbauer C, Wira CR, Rodriguez-Garcia M. Neutrophil extracellular traps prevent HIV infection in the female genital tract. Mucosal Immunol. 2018;11(5):1420–1428. doi:10.1038/s41385-018-0045-0.
  • Ruan Q, Yang K, Wang W, Jiang L, Song J. Correction to: clinical predictors of mortality due to COVID-19 based on an analysis of data of 150 patients from Wuhan, China. Intensive Care Med. 2020;46(6):1294–1297. doi:10.1007/s00134-020-06028-z.
  • Min CK, Cheon S, Ha NY, Sohn KM, Kim Y, Aigerim A, et al. Comparative and kinetic analysis of viral shedding and immunological responses in MERS patients representing a broad spectrum of disease severity. Sci Rep. 2016;6(1):25359. doi:10.1038/srep25359.
  • Jorch SK, Kubes P. An emerging role for neutrophil extracellular traps in noninfectious disease. Nat Med. 2017;23(3):279–287. doi:10.1038/nm.4294.
  • Coutinho HD, Lôbo KM, Bezerra DA, Lôbo I. Peptides and proteins with antimicrobial activity. Indian J Pharmacol. 2008;40(1):3–9. doi:10.4103/0253-7613.40481.
  • Chamilos G, Lewis RE, Lamaris G, Walsh TJ, Kontoyiannis DP. Zygomycetes hyphae trigger an early, robust proinflammatory response in human polymorphonuclear neutrophils through toll-like receptor 2 induction but display relative resistance to oxidative damage. Antimicrob Agents Chemother. 2008;52(2):722–724. doi:10.1128/AAC.01136-07.
  • Chinn RY, Diamond RD. Generation of chemotactic factors by Rhizopus oryzae in the presence and absence of serum: relationship to hyphal damage mediated by human neutrophils and effects of hyperglycemia and ketoacidosis. Infect Immun. 1982;38(3):1123–1129. doi:10.1128/iai.38.3.1123-1129.1982.
  • Patel A, Agarwal R, Rudramurthy SM, Shevkani M, Xess I, Sharma R, et al. Multicenter epidemiologic study of coronavirus disease–associated Mucormycosis, India. Emerg Infect Dis. 2021 Jun 4;27(9):2349–2359. doi:10.3201/eid2709.210934. Epub ahead of print. PMID: 34087089.
  • Watson CN, Kerrigan SW, Cox D, Henderson IR, Watson SP, Arman M. Human platelet activation by Escherichia coli: roles for FcγRIIA and integrin αIIbβ3. Platelets. 2016;27(6):535–540. doi:10.3109/09537104.2016.1148129.
  • van Eeden C, Khan L, Osman MS, Cohen Tervaert JW. Natural killer cell dysfunction and its role in COVID-19. Int J Mol Sci. 2020;21(17):6351. doi:10.3390/ijms21176351.
  • Terpos E, Ntanasis-Stathopoulos I, Elalamy I, Kastritis E, Sergentanis TN, Politou M, et al. Hematological findings and complications of COVID-19. Am J Hematol. 2020;95(7):834–847. doi:10.1002/ajh.25829.
  • Rao VUS, Arakeri G, Subash A, Rao J, Jadhav S, Suhail Sayeed M, et al. COVID-19: loss of bridging between innate and adaptive immunity? Med Hypotheses. 2020;144:109861. doi:10.1016/j.mehy.2020.109861.
  • Law HK, Cheung CY, Ng HY, Sia SF, Chan YO, Luk W, et al. Chemokine up-regulation in SARS-coronavirus–infected, monocyte-derived human dendritic cells. Blood. 2005;106(7):2366–2374. doi:10.1182/blood-2004-10-4166.
  • Perkhofer S, Kainzner B, Kehrel BE, Dierich MP, Nussbaumer W, Lass-Flörl C. Potential antifungal effects of human platelets against zygomycetes in vitro. J Infect Dis. 2009;200(7):1176–1179. doi:10.1086/605607.
  • Ibrahim AS, Spellberg B, Edwards J Jr. Iron acquisition: a novel perspective on mucormycosis pathogenesis and treatment. Curr Opin Infect Dis. 2008;21(6):620–625. doi:10.1097/QCO.0b013e3283165fd1.
  • Voelz K, Gratacap RL, Wheeler RT. A zebrafish larval model reveals early tissue-specific innate immune responses to Mucor circinelloides. Dis Model Mech. 2015;8(11):1375–1388. doi:10.1242/dmm.019992.
  • Huang C, Wang Y, Li X, Ren L, Zhao J, Hu Y, et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet. 2020;395(10223):497–506. doi:10.1016/S0140-6736(20)30183-5.
  • Kell DB, Pretorius E. Serum ferritin is an important inflammatory disease marker, as it is mainly a leakage product from damaged cells. Metallomics. 2014;6(4):748–773. doi:10.1039/C3MT00347G.
  • Kernan KF, Carcillo JA. Hyperferritinemia and inflammation. Int Immunol. 2017;29(9):401–409. doi:10.1093/intimm/dxx031.
  • Rouault TA. Mitochondrial iron overload: causes and consequences. Curr Opin Genet Dev. 2016;38:31–37. doi:10.1016/j.gde.2016.02.004.
  • Starkov AA. The role of mitochondria in reactive oxygen species metabolism and signaling. Ann NY Acad Sci. 2008;1147(1):37–52. doi:10.1196/annals.1427.015.
  • Herst PM, Rowe MR, Carson GM, Berridge MV. Functional mitochondria in health and disease. Front Endocrinol (Lausanne). 2017;8:296. doi:10.3389/fendo.2017.00296.
  • Jo EK, Kim JK, Shin DM, Sasakawa C. Molecular mechanisms regulating NLRP3 inflammasome activation. Cell Mol Immunol. 2016;13(2):148–159. doi:10.1038/cmi.2015.95.
  • Naik E, Dixit VM. Mitochondrial reactive oxygen species drive proinflammatory cytokine production. J Exp Med. 2011;208(3):417–420. doi:10.1084/jem.20110367.
  • Jouihan HA, Cobine PA, Cooksey RC, Hoagland EA, Boudina S, Abel ED. Iron-Mediated inhibition of mitochondrial manganese uptake mediates mitochondrial dysfunction in a mouse model of hemochromatosis. Mol Med. 2008;14(3–4):98–108. doi:10.2119/2007-00114.Jouihan.
  • Aguirre JD, Culotta VC. Battles with iron: manganese in oxidative stress protection. J Biol Chem. 2012;287(17):13541–13548. doi:10.1074/jbc.R111.312181.
  • Park D, Han CZ, Elliott MR, Kinchen JM, Trampont PC, Das S, et al. Continued clearance of apoptotic cells critically depends on the phagocyte UCP2 protein. Nature. 2011;477(7363):220–224. doi:10.1038/nature10340.
  • Janssen E, Tabeta K, Barnes MJ, Rutschmann S, McBride S, Bahjat KS, et al. Efficient T cell activation via a Toll-Interleukin 1 Receptor-independent pathway. Immunity. 2006;24(6):787–799. doi:10.1016/j.immuni.2006.03.024.
  • Navarro A, Boveris A. The mitochondrial energy transduction system and the aging process. Am J Physiol Cell Physiol. 2007;292(2):C670–686. doi:10.1152/ajpcell.00213.2006.
  • Chougnet CA, Thacker RI, Shehata HM, Hennies CM, Lehn MA, Lages CS, et al. Loss of phagocytic and antigen cross-presenting capacity in aging dendritic cells is associated with mitochondrial dysfunction. J Immunol. 2015;195(6):2624–2632. doi:10.4049/jimmunol.1501006.
  • LeBlanc DM, Barousse MM, Pl F Jr. Role for dendritic cells in immunoregulation during experimental vaginal candidiasis. Infect Immun. 2006;74(6):3213–3221. doi:10.1128/IAI.01824-05.
  • Eapen MS, Sharma P, Sohal SS. Mitochondrial dysfunction in macrophages: a key to defective bacterial phagocytosis in COPD. Eur Respir J. 2019;54(4):1901641. doi:10.1183/13993003.01641-2019.
  • Nicolás FE, Murcia L, Navarro E, Navarro-Mendoza MI, Pérez-Arques C, Garre V. Mucorales species and macrophages. J Fungi (Basel). 2020;6(2):94. doi:10.3390/jof6020094.
  • Roilides E, Antachopoulos C, Simitsopoulou M. Pathogenesis and host defence against Mucorales: the role of cytokines and interaction with antifungal drugs. Mycoses. 2014;57:40–47. doi:10.1111/myc.12236.
  • Morikawa K, Oseko F, Morikawa S. A role for ferritin in hematopoiesis and the immune system. Leuk Lymphoma. 1995;18(5–6):429–433. doi:10.3109/10428199509059641.
  • Govender N, Khaliq OP, Moodley J, and Naicker T. Insulin resistance in COVID-19 and diabetes. Prim Care Diabetes. 2021 Aug;15(4):629–634. doi:10.1016/j.pcd.2021.04.004.
  • Vallianou NG, Evangelopoulos A, Kounatidis D, Stratigou T, Christodoulatos GS, Karampela I, et al. Diabetes mellitus and SARS-CoV-2 infection: pathophysiologic mechanisms and implications in management. Curr Diabetes Rev. 2020;31.
  • Rubino F, Amiel SA, Zimmet P, Alberti G, Bornstein S, Eckel RH, et al. New-onset diabetes in Covid-19. N Engl J Med. 2020;383(8):789–790. doi:10.1056/NEJMc2018688.
  • Zhu L, She ZG, Cheng X, Qin JJ, Zhang XJ, Cai J, et al. Association of blood glucose control and outcomes in patients with COVID-19 and pre-existing type 2 diabetes. Cell Metab. 2020;31(6):1068–1077.e3. doi:10.1016/j.cmet.2020.04.021.
  • Holman N, Knighton P, Kar P, O’-Keefe J, Curley M, Weaver A, et al. Risk factors for COVID-19-related mortality in people with type 1 and type 2 diabetes in England: a population-based cohort study. Lancet Diabetes Endocrinol. 2020;8(10):823–833. doi:10.1016/S2213-8587(20)30271-0.
  • Hollstein T, Schulte DM, Schulz J, Glück A, Ziegler AG, Bonifacio E, et al. Autoantibody-Negative insulin-dependent diabetes mellitus after SARS-CoV-2 infection: a case report. Nat Metab. 2020;2(10):1021–1024. doi:10.1038/s42255-020-00281-8.
  • Chee YJ, Ng SJH, Yeoh E. Diabetic ketoacidosis precipitated by COVID-19 in a patient with newly diagnosed diabetes mellitus. Diabetes Res Clin Pract. 2020;164:108166. doi:10.1016/j.diabres.2020.108166.
  • Li J, Wang X, Chen J, Zuo X, Zhang H, Deng A. COVID-19 infection may cause ketosis and ketoacidosis. Diabetes Obes Metab. 2020;22(10):1935–1941. doi:10.1111/dom.14057.
  • Ren H, Yang Y, Wang F, Yan Y, Shi X, Dong K, et al. Association of the insulin resistance marker TyG index with the severity and mortality of COVID-19. Cardiovasc Diabetol. 2020;19(1):58. doi:10.1186/s12933-020-01035-2.
  • Groop LC, Bonadonna RC, DelPrato S, Ratheiser K, Zyck K, Ferrannini E, et al. Glucose and free fatty acid metabolism in non-insulin-dependent diabetes mellitus. Evidence for multiple sites of insulin resistance. J Clin Invest. 1989;84(1):205–213. doi:10.1172/JCI114142.
  • Eketunde AO, Mellacheruvu SP, Oreoluwa P. A review of postmortem findings in patients with COVID-19. Cureus. 2020;12:e9438.
  • Zhang H, Penninger JM, Li Y, Zhong N, Slutsky AS. Angiotensin-Converting enzyme 2 (ACE2) as a SARS-CoV-2 receptor: molecular mechanisms and potential therapeutic target. Intensive Care Med. 2020;46(4):586–590. doi:10.1007/s00134-020-05985-9.
  • Liu F, Long X, Zhang B, Zhang W, Chen X, Zhang Z. ACE2 expression in Pancreas may cause pancreatic damage after SARS-CoV-2 infection. Clin Gastroenterol Hepatol. 2020;18(9):2128–2130.e2. doi:10.1016/j.cgh.2020.04.040.
  • Reddy PK, Kuchay MS, Mehta Y, Mishra SK. Diabetic ketoacidosis precipitated by COVID-19: a report of two cases and review of literature. Diabetes Metab Syndr. 2020;14(5):1459–1462. doi:10.1016/j.dsx.2020.07.050.
  • Nair AG, Adulkar NG, D’-Cunha L, Rao PR, Bradoo RA, Bapaye MM, et al. Rhino-Orbital mucormycosis following COVID-19 in previously non-diabetic, immunocompetent patients. Orbit. 2021;40(6):499–504. doi:10.1080/01676830.2021.1960382.
  • Dave TV, Nair AG, Hegde R, Vithalani N, Desai S, Adulkar N, et al. Clinical presentations, management and outcomes of rhino-orbital-cerebral Mucormycosis (ROCM) following COVID-19: a multi-centric study. Ophthalmic Plast Reconstr Surg. 2021;37(5):488–495. doi:10.1097/IOP.0000000000002030.
  • Tater D, Tepaut B, Bercovici JP, Youinou P. Polymorphonuclear cell derangements in type I diabetes. Horm Metab Res. 1987;19(12):642–647. doi:10.1055/s-2007-1011899.
  • Delamaire M, Maugendre D, Moreno M, Le Goff MC, Allannic H, et al. Impaired leucocyte functions in diabetic patients. Diabet Med. 1997;14(1):29–34. doi:10.1002/(SICI)1096-9136(199701)14:1<29:AID-DIA300>3.0.CO;2-V.
  • Marhoffer W, Stein M, Maeser E, Federlin K. Impairment of polymorphonuclear leukocyte function and metabolic control of diabetes. Diabetes Care. 1992;15(2):256–260. doi:10.2337/diacare.15.2.256.
  • Abbaspour N, Hurrell R, Kelishadi R. Review on iron and its importance for human health. J Res Med Sci. 2014;19:164–174.
  • Van Asbeck BS, Marx JJ, Struyvenberg A, Verhoef J. Functional defects in phagocytic cells from patients with iron overload. J Infect. 1984;8(3):232–240. doi:10.1016/S0163-4453(84)93955-0.
  • Garner B, Li W, Roberg K, Brunk UT. On the cytoprotective role of ferritin in macrophages and its ability to enhance lysosomal stability. Free Radic Res. 1997;27(5):487–500. doi:10.3109/10715769709065788.
  • Carrasco-Marín E, Alvarez-Domínguez C, López-Mato P, Martínez-Palencia R, Leyva-Cobián F. Iron salts and iron-containing porphyrins block presentation of protein antigens by macrophages to MHC class II-restricted T cells. Cell Immunol. 1996;171(2):173–185. doi:10.1006/cimm.1996.0192.
  • Artis WM, Fountain JA, Delcher HK, Jones HE. A mechanism of susceptibility to mucormycosis in diabetic ketoacidosis: transferrin and iron availability. Diabetes. 1982;31(12):1109–1114. doi:10.2337/diacare.31.12.1109.
  • Husain S, Alexander BD, Munoz P, Avery RK, Houston S, Pruett T, et al. Opportunistic mycelial fungal infections in organ transplant recipients: emerging importance of non-Aspergillus mycelial fungi. Clin Infect Dis. 2003;37(2):221–229. doi:10.1086/375822.
  • Boelaert JR, Fenves AZ, Coburn JW. Registry on mucormycosis in dialysis patients. J Infect Dis. 1989;160(5):914. doi:10.1093/infdis/160.5.914.
  • Boelaert JR, Fenves AZ, Coburn JW. Mucormycosis among patients on dialysis. New Engl J Med. 1989;321:190–191.
  • Aasa R, Malmstroem BG, Saltman P. The specific binding of iron(iii) and copper(ii) to transferrin and conalbumin. Biochim Biophys Acta. 1963, September 24;75:203–222. doi:10.1016/0006-3002(63)90599-7.