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Zygomycosis Caused by Cunninghamella Bertholletiae in a Kidney Transplant Recipient

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Zygomycosis Caused by Cunninghamella Bertholletiae in a Kidney Transplant Recipient Medical Mycology April 2004, 42, 177Á/180 Case report Zygomycosis caused by Cunninghamella bertholletiae in a kidney transplant recipient D. QUINIO*, A. KARAM$, J.-P. LEROY%, M.-C. MOAL§, B. BOURBIGOT§, O. MASURE*, B. SASSOLAS$ & A.-M. LE FLOHIC* Departments of *Microbiology, $Dermatology, %Pathology and §Kidney Transplantation, Brest University Hospital Brest France Downloaded from https://academic.oup.com/mmy/article/42/2/177/964345 by guest on 23 September 2021 Infections caused by Cunninghamella bertholletiae are rare but severe. Only 32 cases have been reported as yet, but in 26 of these this species was a contributing cause of the death of the patient. This opportunistic mould in the order Mucorales infects immunocompromized patients suffering from haematological malignancies or diabetes mellitus, as well as solid organ transplant patients. The lung is the organ most often involved. Two cases of primary cutaneous infection have been previously reported subsequent to soft-tissue injuries. We report a case of primary cutaneous C. bertholletiae zygomycosis in a 54-year-old, insulin-dependent diabetic man who was treated with tacrolimus and steroids after kidney transplantation. No extracutaneous involvement was found. In this patient, the infection may have been related to insulin injections. The patient recovered after an early surgical excision of the lesion and daily administration of itraconazole for 2 months. This case emphasizes the importance of an early diagnosis of cutaneous zygomycosis, which often presents as necrotic-looking lesions. Prompt institution of antifungal therapy and rapid surgical intervention are necessary to improve the prospects of patients who have contracted these potentially severe infections. Keywords Cunninghamella bertholletiae, cutaneous zygomycosis, diabetes mellitus, kidney transplantation Introduction sub-tropical areas. Mucormycosis mainly develops in patients with haematological malignancies and neutro- Zygomycosis is caused by the filamentous fungi in the penia, in transplant recipients, or in patients with class Zygomycetes. Two different types of infection can diabetes mellitus and ketoacidosis [1,2]. Although the be distinguished: (i) mucormycosis, caused by fungi in diagnosis of zygomycosis is not easy, the effectiveness the order Mucorales and characterized by clinical of therapy is dependent on early diagnosis and treat- polymorphism and high resistance to medical treat- ment. We report a case of primary cutaneous zygomy- ment, and (ii) entomophthoromycosis, caused by fungi cosis due to Cunninghamella bertholletiae in a kidney in the order Entomophthorales and most commonly transplant recipient. seen as a chronic disease indigenous to tropical and Case report Received 14 October 2002; Accepted 29 April 2003 A 54-year-old male patient with insulin-dependent Correspondence: Dorothe´e Quinio, Department of Microbiology, Brest University Hospital, 5 avenue Foch, 29609 Brest Cedex, France. diabetes mellitus underwent a kidney transplantation Tel.: /33 2 9822 3308; Fax: /33 2 9822 3987; E-mail: in February 2001 and was treated with tacrolimus and [email protected] steroids. Five months later, a firm ulcerated nodule, – 2004 ISHAM DOI: 10.1080/13693780310001644644 178 Quinio et al. bertholletiae by Dr Nicole Nolard at The Scientific Public Health InstituteÁ/Louis Pasteur, Brussels (cul- ture number ISP/14/HB/KM/01/0935). No extracuta- neous lesions were observed. Amphotericin B was not administered because of its known side-effects on the kidney. The patient was treated with itraconazole capsules at 400 mg/day for 1 month, then at 200 mg/ day for a further 1 month. The MIC for itraconazole tested by Etest† (AB Biodisk, Solna, Sweden) was 0.75 mg/ml. Itraconazole levels were measured to monitor the absorption of the drug. Neither recurrence nor any extracutaneous lesions were observed 3 months after Downloaded from https://academic.oup.com/mmy/article/42/2/177/964345 by guest on 23 September 2021 the excision. Discussion The order Mucorales is subdivided into six families of significance in causing human or animal disease: Mucoraceae, Cunninghamellaceae, Saksenaeaceae, Thamnidiaceae, Syncephalastraceae and Mortierella- ceae. Under this classification system, most human zygomycosis cases are caused by the members of the Mucoraceae. In the Cunningamellaceae, only one species, C. bertholletiae, has so far been proven to infect humans [1]. C. bertholletiae is a rare cause of invasive mould infection. Only 32 cases have been reported in the literature, although in 26 of these C. bertholletiae was a contributing cause of death [3,4]. Most infections have been described in patients with Fig. 1 Ulcerated nodule caused by Cunninghamella bertholletiae. haematological malignancies and neutropenia. The Nodule is ringed by an inflammatory halo. other cases occurred in transplant recipients, diabetic patients, persons with AIDS or b-thalassemia, or surrounded with inflammatory halo, appeared on his patients receiving deferoxamine treatment because of right hip (Fig. 1). Histological examination showed, iron overload. One case was seen in an alcohol abuser within the hypoderma, an inflammatory granuloma without any other cause of immunological dysfunction containing plasma cells, lymphocytes and neutrophils, [1]. In most cases, infection involved the lung. Other together with numerous macrophages and occasional infected organs included the sinus, the kidney, the multinucleated giant cells engulfing hyphae. There was gastrointestinal tract and the skin. Skin involvement an ischaemic necrosis containing rounded, swollen may be primary or may follow dissemination of the formations positive in periodic acid-Schiff (PAS) and mould. Only two cases of a primary cutaneous infec- Grocott-methenamine silver stains. Typical long, tion with C. bertholletiae have been reported to date, branched, aseptate hyphae were visible in less inflamed one in an AIDS patient, who died, and one in a areas of the lesion (Fig. 2). diabetic, who survived after amputation of his leg [5,6]. The lesion was excised. Culture of the specimen on In these two cases, a soft-tissue injury had occurred at Sabouraud dextrose agar at 258C yielded a greyÁ/white the site where the infection originated. cottony growth within 48 h. Lactophenol cotton blue Although various other cutaneous zygomycotic in- preparations showed acutely branched, broad, aseptate fections have been reported, the primary cutaneous hyphae. Sporangiophores diverged from the hyphae infection described here seems to be the first featuring and ended in vesicles that were covered with mono- C. bertholletiae in a kidney transplant recipient. The sporous sporangioles produced on short stalks (Fig. 3). applicable risk factors for this patient were post- Verticillately branching sporangiophores were also transplant immunosuppressive treatment and diabetes. observed. The isolate was finally identified as C. As the infection was at the site of daily injections of – 2004 ISHAM, Medical Mycology, 42, 177Á/180 Cutaneous Cunninghamella zygomycosis 179 Downloaded from https://academic.oup.com/mmy/article/42/2/177/964345 by guest on 23 September 2021 Fig. 2 Histological skin section showing hypha of Cunninghamella bertholletiae. GomoriÁ/Grocott sil- ver stain, original magnification/ 600. insulin, the infectious agent may have been introduced Among 72 cases of previously reported cases of via these subcutaneous injections. primary cutaneous zygomycosis, C. bertholletiae was Fig. 3 Microscopic features of Cunninghamella bertholletiae in culture on Sabouraud dextrose agar. Sporangiophores terminating in vesicles entirely covered with monosporous sporangioles. Lacto- phenol cotton blue preparation, original magnification/600. – 2004 ISHAM, Medical Mycology, 42, 177Á/180 180 Quinio et al. involved in only 1% of the cases, far fewer than Mucorales. Concomitant use of topical antifungal Rhizopus spp. (39%) Mucor spp. (21%) and Absidia agents is of high interest in association with intravenous spp. (11%). These are the organisms that in general are amphotericin B, because little or no diffusion is most often involved in zygomycosis [7]. Clinically, in observed into necrotic tissues when amphotericin B is primary cutaneous cases, the lesions often looked like administered intravenously [1,5,7]. There are very few necrotic lesions, nodules or ulcerations. The patients case reports concerning the treatment of zygomycosis often suffered from diabetes or haematological malig- by itraconazole and the sensitivity to this drug varies nancies. In some cases, infection occurred as a compli- among the different species of Mucorales tested [2]. In cation of burns or after administration of subcutaneous addition, one documented cluster of four pulmonary injections. infections caused by C. bertholletiae involved three Cunninghamella bertholletiae infection is most often patients who were on itraconazole prophylaxis [4]. acquired by inhalation of airborne spores, particularly Despite the inconsistent results obtained with itraco- Downloaded from https://academic.oup.com/mmy/article/42/2/177/964345 by guest on 23 September 2021 in pulmonary and rhinocerebral infections. Transmis- nazole in previous C. bertholletiae cases, our patient sion via the gastrointestinal tract is also suggested by responded well to surgical excision and itraconazole, the prominent involvement of these organs in some and the isolate was susceptible to itraconazole in vitro. cases. C. bertholletiae has been found in a wide
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