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Rhino-Orbital Mucormycosis Due to Apophysomyces Ossiformis in A Martínez-Herrera et al. BMC Infectious Diseases (2020) 20:614 https://doi.org/10.1186/s12879-020-05337-4 CASE REPORT Open Access Rhino-orbital mucormycosis due to Apophysomyces ossiformis in a patient with diabetes mellitus: a case report Erick Martínez-Herrera1, María Guadalupe Frías-De-León1, Angélica Julián-Castrejón1, Luis Cruz-Benítez1, Juan Xicohtencatl-Cortes2 and Rigoberto Hernández-Castro3* Abstract Background: The most common aetiological agents of mucormycosis are Rhizopus, Mucor, Apophysomyces and Lichtheimia. Apophysomyces is comparatively rare, as it has been reported in less than 3% of mucormycosis cases. The genus Apophysomyces includes six species, and only A. elegans, A. mexicanus, A. variabilis and A. ossiformis have been reported to cause infections in both immunocompetent and immunocompromised patients. Case presentation: We present a case of a 46-year-old male patient with bilateral blepharoedema, corneal opacity in the left eye and poorly controlled diabetes mellitus. The patient was subjected to total maxillectomy, exenteration of the left orbit and treatment with liposomal amphotericin B. Direct mycological analysis with KOH 10% revealed hyaline, coenocytic, long and wide hyphae. Apophysomyces ossiformis was identified from maxillary biopsy using 18S-ITS1–5.8S-ITS2-28S rRNA gene amplification and sequencing. The patient requested to be transferred to another hospital to continue treatment, where he died on the ninth day after admittance. Conclusion: To the best of our knowledge, this is the first case of rhino-orbital mucormycosis due to A. ossiformis with a fatal outcome. This case reveals the need to identify the fungus causing mucormycosis with molecular methods to identify adequate treatment therapies for patients with this infection. Keywords: Apophysomyces ossiformis, Diabetes mellitus, Invasive fungal disease, Mucormycosis Background Apophysomyces and Lichtheimia. Apophysomyces is Mucormycosis is an invasive infection caused by Mucor- comparatively rare, as it has been reported in less than ales [1]. The main risk factors for this mycosis are 3% of mucormycosis cases [4]. The genus Apophyso- diabetes mellitus type 2, immunosuppression, neutro- myces includes six species (A. elegans, A. mexicanus, A. penia, metabolic acidosis, leukaemia, lymphoma, and ossiformis, A. thailandensis, A. trapeziformis, and A. organ transplants [2]. The clinical presentation can be variabilis), and only A. elegans, A. mexicanus, A. ossifor- pulmonary, gastrointestinal, cutaneous, and dissemi- mis and A. variabilis have been reported to cause nated; however, the most frequent presentation is rhino- infections in both immunocompetent and immunocom- cerebral, with a high mortality rate [1, 3]. The most promised patients [5–7]. We present the first case of common aetiological agents are Rhizopus, Mucor, rhino-orbital mucormycosis due to A. ossiformis in a patient with poorly controlled diabetes from the central * Correspondence: [email protected] region of Mexico. 3Departamento de Ecología de Agentes Patógenos, Hospital General “Dr. Manuel Gea González”, Sección XVI, Tlalpan 14080, Ciudad de México, Mexico Full list of author information is available at the end of the article © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Martínez-Herrera et al. BMC Infectious Diseases (2020) 20:614 Page 2 of 4 Case presentation surgical debridement was performed with total maxil- A 46-year-old male patient presented with a conjunctival lectomy and exenteration of the left orbit; a microvascu- infection and probable Reis-Bücklers dystrophy (clinic- larized femur graft was obtained to reconstruct the left ally characterized by superficial corneal opacities, recur- orbit (Fig. 1d). During surgery, necrosis of the whole rent erosions and significant visual impairment), and maxilla as well as the orbit floor, including the nasal multiple antimicrobial treatments showed no improve- septum, was observed. Samples of the maxillary tissue, ments. At admittance to our institution, the patient ocular globe, and nasal septum were sent for histopatho- reported a headache and moderate pain in the bilateral logical analysis. orbitofrontal region radiating to the occipital region. He Haematoxylin-eosin and Grocott-Gomori staining had a history of uncontrolled diabetes mellitus type 2 for allowed the observation of wide hyphae with irregular 3 years and poor treatment compliance. A physical contours (Fig. 2), and a direct mycological study with examination revealed fever, chills, and general malaise, KOH 10% revealed hyaline, coenocytic, long and wide with moderate bilateral ocular pain, nasal congestion, filaments, compatible with members of the order dehydrated nasal mucosa, odynophagia, cough, dys- Mucorales. No mycological culture was performed. pnoea, hemoptysis, bilateral blepharoedema, and corneal Molecular identification was performed by the amplifi- opacity in the left eye (Fig. 1a, b). A black eschar was cation and sequencing of DNA fragments containing the seen on the palate (Fig. 1c). 18S rRNA gene, the internal transcribed spacer regions The patient was evaluated in the Ophthalmology De- (ITS1, 5.8S gene, and ITS2), and the 5′ end of the 28S partment, where a lacrimal gland biopsy was performed, rRNA gene. Genomic DNA was isolated from the maxil- and acute inflammation of the orbit of unknown origin lary tissue using a DNeasy blood and tissue kit (Qiagen, was observed. A facial CT scan was performed and re- Ventura, CA, USA) according to the manufacturer’s in- vealed pansinusitis with deformation of the left ocular structions. For polymerase chain reaction (PCR), a set of globe, luxation of the crystalline, maxillary affectation, primers previously reported for fungal species (ITS1–5′- and deformation of the floor of the bilateral orbital bone TCCGTAGGTGAACCTGCGG-3′ and ITS4–5′-TCCT occupied by both maxillary sinuses. The recommended CCCGCTTATTGATATGC-3′) was used [8, 9]. The starting treatment was liposomal amphotericin B (5 mg/ amplicon was purified, and the nucleotide sequence was kg/day) and the initiation of glycaemic control due to determined in both directions with Taq FS dye- probable mucormycosis. A biopsy was taken, and terminator cycle-sequencing fluorescence-based sequen- cing and analysed on an Applied Biosystems 3730 xl DNA sequencing system. A PCR product of approxi- mately 730 bp was amplified from the maxillary sample. The PCR product was purified and sequenced in both Fig. 1 Acute inflammation of the orbit of the left eye a; corneal opacity of the left eye b; oral cavity with necrotic ulcers c; and total Fig. 2 Histopathological findings: wide and long non-septate maxillectomy and exenteration of the left orbit d hyphae with irregular contours (Grocott-Gomori staining, × 40) Martínez-Herrera et al. BMC Infectious Diseases (2020) 20:614 Page 3 of 4 directions using the same primers. A consensus se- agar, a culture medium that is not appropriate for the quence homology search was performed in the GenBank growth of Apophysomyces spp., as well as for the harsh database (nucleotide BLAST); the obtained sequence processing of tissue. However, the visualization of showed 100% homology with the Apophysomyces ossifor- hyphae characteristic of Mucorales allowed rapid action, mis UTHSC 04–838 strain, 99% homology with the A. such as surgical intervention in the affected area, the ossiformis UTHSC 07–204 strain, and 94% homology beginning of treatment and molecular identification. with the A. thailandensis SDBR-CMUS219 and A. trape- From a clinical point of view, Apophysomyces can ziformis DUM101.13 strains. cause necrotizing fasciitis and renal and rhino-orbital- Afterward, the patient was kept in the intensive care cerebral infections, and the treatment of choice is unit for 7 days and then transferred for continued amphotericin B. However, research in a murine model hospitalization with an antibiotic regimen of piperacillin- showed the efficacy of posaconazole for the treatment of tazobactam IV 4.5 g/6 h and liposomal amphotericin B disseminated infections by A. variabilis. Further clinical (10 mg/kg/day). On day 15, the patient requested to re- studies are needed to determine the potential use of this turn to the General Hospital of Tlaxcala to continue antifungal agent in human infections [11, 13]. Ampho- treatment. The patient died 9 days after admittance due tericin B is the first-line antifungal monotherapy recom- to complications associated with his poorly controlled mended by the global mucormycosis guide.
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