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Agent of Disseminated Infection Received: 16 August 2016 | Revised: 17 September 2016 | Accepted: 11 October 2016 DOI: 10.1111/myc.12583 ORIGINAL ARTICLE A novel dimorphic pathogen, Emergomyces orientalis (Onygenales), agent of disseminated infection Peng Wang1 | Chris Kenyon2 | Sybren de Hoog3 | Lina Guo1 | Hongwei Fan4 | Hongrui Liu5 | Zhongwei Li6 | Ruiyuan Sheng4 | Ying Yang7 | Yanping Jiang3,8 | Li Zhang1 | Yingchun Xu1 1Division of Clinical Microbiology, P.U.M.C.H., Beijing, China Summary 2Sexually Transmitted Infection A novel dimorphic fungus, Emergomyces orientalis sp. nov. a close relative of systemic Unit, Institute of Tropical Medicine, pathogens in the family Ajellomycetaceae (Blastomyces, Histoplasma). The fungus is re- Antwerp, Belgium ported in a 64- year- old male from Shanxi, China. The patient developed disseminated 3CBS-KNAW Fungal Biodiversity Centre, Utrecht, The Netherlands skin lesions, productive cough with fever and showed nodular opacities in his left lung 4Division of Internal Medicine, P.U.M.C.H., on chest radiography. The patient had no identified cause of immunodeficiency apart Beijing, China from type- 2 diabetes mellitus. Clinical, histopathological and mycological characteris- 5Division of Pathology, P.U.M.C.H., Beijing, China tics of the agent are given, and its phylogenetic position is determined with multilocus 6Division of Bioinformatics, Academy of sequence data. Military Medical Science, Beijing Institute of Radiation Medicine, Beijing, China KEYWORDS 7 Division of Fungi, Academy of Military AIDS-related mycosis, diabetes, dimorphic fungi, Emergomyces, Emmonsia, endemic mycosis Medical Science, Beijing Institute of Radiation Medicine, Beijing, China 8Department of Dermatology, The Affiliated Hospital, Guizhou Medical University, Guiyang, China Correspondence Yingchun Xu, Division of Clinical Microbiology, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences, Beijing, China. Email: [email protected] 1 | INTRODUCTION found globally in humans rather than in rodents, and may occur in the form of outbreaks with dozens of cases, such as in South Africa.1 This A new clinical entity is emerging among the thermally dimorphic fungi1,2 has led to new visions on the pathology of the dimorphic pathogens, and by species that have provisionally been identified as “Emmonsia”. obviously the taxonomy of the Ajellomycetaceae has to be revised con- Previously, “emmonsiosis” was thought to only affect humans via inha- siderably. In this paper, we present a fungus from a disseminated human lation of fungal elements which swell in the lungs to form large adia- infection presented in 2005 that could not be identified with any known spores, leading to respiratory symptoms that can be mild to severe.1 species; it was provisionally reported3 in 2009. Phylogenetically, it clus- The classical species Emmonsia parva and E. crescens mainly colonise tered among members of the recently described (Dukik K, Muñoz J, the respiratory tract of small subterranean mammals, human infections Jiang Y et al; Unpublished data) genus Emergomyces in Ajellomycetaceae only being exceptional. In contrast, the novel emmonsia- like species are and is reported below as a novel species, Emergomyces orientalis. This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made. Mycoses 2017; 1–10 wileyonlinelibrary.com/journal/myc © 2017 The Authors. Mycoses Published by | 1 Blackwell Verlag GmbH 2 | WANG ET AL. silver (GMS) stains, but Mayer’s mucicarmine stain was negative. 1.1 | Case report Despite these conflicting data, a provisional diagnosis of dis- In 2005, a 64- year- old male from Shanxi, China, with no previ- seminated cryptococcosis was made and the patient was treated ous medical history, presented with a productive cough, fever and with intravenous fluconazole 200 mg twice a day for 3 weeks. pustular lesions on his neck. Within a week, similar lesions had He showed no improvement on this therapy and was therefore appeared on his face, trunk and scalp. He also developed subcu- transferred to the Peking Union Medical College Hospital. On taneous nodules throughout his body (Figure 1A,B). A computer- admission, he was febrile (38.5°C) and physical examination re- ised tomographic (CT) scan of his chest revealed multiple nodular vealed cervical and axillary lymphadenopathy and multiple new densities in the left lower lung (Figure 2 Left). He showed no papules (~1 cm in diameter) all over his body (Figure 1). He was therapeutic response to 5 days of intravenous ceftriaxone and diagnosed with type- 2 diabetes mellitus and appropriate therapy penicillin G, and was therefore transferred to a tertiary hospital in was instituted. Cryptococcal antigen testing of the serum and cer- Beijing. Histopathological evaluation of a CT- guided percutaneous ebrospinal fluid were both negative. His therapy was changed to pulmonary biopsy revealed chronic granulomatous changes and amphotericin B deoxycholate plus fluconazole (200 mg twice a day a negative Ziehl- Neelsen stain. Histopathology of a subcutane- intravenous) to treat an uncharacterised invasive fungal infection. ous nodule showed fungal cells similar to those of Cryptococcus After 3 weeks, sputum fungal culture yielded a dimorphic fungus, by periodic acid- Schiff (PAS) (Figure 3) and Gomori methenamine which was provisionally identified as an emmonsia- like species. (A) (B) (C) FIGURE 1 A- C, Clinical aspect of disseminated cutaneous lesions on torso and legs (A) (B) (C) FIGURE 2 Chest computerised tomography showing evolution of left lung lesions, A, before treatment with dense areas of consolidation visible in the left lower lobe, B, after 5 months of therapy with reduction of the lesions, and C, 10 years after therapy with only residual linear opacification WANG ET AL. | 3 (A) (B) FIGURE 3 A, B, Histopathology (PAS) of bronchial biopsy showing multiple yeast cells FIGURE 4 Declining trend in body temperature during antifungal therapy. Temperature declined 0.8°C after 8 months. The second and third of five temperature peak values were concomitant with Enterobacter sakazakii bacteraemia, while the causes of remaining temperature peaks remained unknown TABLE 1 Clinical presentation and Presentation Follow- up Follow- up Normal laboratory parameters 24/01/2005 25/8/2005 10 years range White cell count×10−9/L 20.26 11.92 9.22 4.00- 10.00 Neutrophil count×10−9/L 17.07 9.57 6.5 2.00- 7.50 Lymphocyte count×10−9/L 1.44 1.19 1.73 0.8- 4.00 Platelet count×10−9/L 285 315 197 100- 360 Alanine aminotransferase 28 15 24 5- 40 U/L Aspartate aminotransferase 19 13 25 5- 37 U/L Alkaline phosphatase U/L 377 238 111 27- 107 Haemoglobin g/L 112 103 170 110- 160 Creatinine μmol/L 1.11 1.06 79 (59- 104)a 0.60- 1.55 Albumin g/dL 7.5 3.7 45 (35- 52)a 3.5- 5.1 Globulin g/dL 4.4 4 2.8 3- 3.4 aCreatinine method was used ELISA. To convert values for creatinine to milligrams per decilitre, divide by 88.4. 4 | WANG ET AL. TABLE 2 Origins and nucleotide sequence accession numbers of isolates used in this study Group Name (No.) Strain No. Source Accession No. Rf. No. Group 1 Emmonsia crescens UAMH 3008, ATCC 13704, CBS 177.60 Rodent lung, Norway AF038334 5 (19) UAMH 7365 Lung of possum, New Zealand, 1992 AF038335 5 UAMH 349 Lung of mole, USA, 1954 AF038336 5 UAMH 7268 Lung of possum, New Zealand, 1992 AF038337 5 UAMH 395 Lung of Apodemus sp., Korea, 1953 AF038338 5 UAMH 393 Lung of Clethrionomys sp., Korea, 1953 AF038339 5 UAMH 394 Lung of Clethrionomys sp., Korea, 1953 AF038340 5 UAMH 136 Skunk, Lake County, Montana, USA AF038341 5 UAMH 137 Muskrat, Lake County, Mont., AF038342 5 UAMH 129 Lung of Peromyscus maniculatus borealis, AF038343 5 Alberta, 1947 UAMH 127, CBS 475.77, ATCC 10785 Mouse lung, Alberta, 1946 AF038344 5 UAMH 128 Mouse lung, Alberta, 1946 AF038345 5 UAMH 1067 Lung of wild field mouse, Edmonton, Alberta, AF038346 5 1961 UAMH 1140 Lung of wild field mouse, Alberta, 1961 AF038347 5 UAMH 4076 Soil, Edmonton, Alberta, 1976 AF038348 5 UAMH 4077 Mouldy straw bales in a mushroom house, AF038349 5 1975 UAMH 140 Lung of Peromyscus maniculatus, Alberta, 1950 AF038350 5 UAMH 132 Lung of Peromyscus maniculatus, Alberta. AF038351 5 UAMH 126, ATCC 10784, CBS 191.55 Mouse lung, Canada, 1946 AF038319 5 Group 2 E. pasteuriana (3) SYSU 2014 Human, China, 2014 KP260922 6 NCPF 4236 Type National Collection of Pathogenic Fungi, UK HF563671 1 UAMH 9510 Unknown EF592152 a E africana (16) NCPF 4164 National Collection of Pathogenic Fungi, UK HF563670 1 MVW 0029 Human, South Africa, 2008—2012 JX398288 1 MVW 0030 Human, South Africa, 2008—2012 JX398289 1 MVW 0021 Human, South Africa, 2008—2012 JX398290 1 MVW 0013 Human, South Africa, 2008—2012 JX398291 1 MVW 0009 Human, South Africa, 2008—2012 JX398292 1 MVW 0126 Human, South Africa, 2008—2012 JX398293 1 MVW 0124 Human, South Africa, 2008—2012 JX398294 1 MVW 0078 Human, South Africa, 2008—2012 JX398295 1 MVW 0059 Human, South Africa, 2008—2012 JX398296 1 MVW 0125 Human, South Africa, 2008—2012 JX398297 1 MVW 0127 Human, South Africa, 2008—2012 JX398298 1 MVW 0123 Human, South Africa, 2008—2012 JX398299 1 SN 264 Human, South Africa, 2014 KM199782 a SN 273 Human, South Africa, 2014 KM199783 a MRL 425 Human, South Africa, 2014 KM492927 21 Emmonsia sp.(3) UAMH 10427 Unknown EF592164 a UAMH 7172 HIV+ patient, Canada, 1992 AF038322 5 NCPF 4091 National Collection of Pathogenic
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