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Table of Contents
CASE REPORT
Year : 2021  |  Volume : 15  |  Issue : 2  |  Page : 169-175

Invasive fungal diseases in renal transplantation - Case series


Department of Nephrology and Renal Transplantation, VPS Lakeshore Hospital and Research Center, Kochi, Kerala, India

Date of Submission04-Apr-2020
Date of Decision07-May-2020
Date of Acceptance10-Feb-2021
Date of Web Publication30-Jun-2021

Correspondence Address:
Dr. Kartik Ganesh
Department of Nephrology and Renal Transplantation, VPS Lakeshore Hospital and Research Center, Kochi, Kerala
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ijot.ijot_28_20

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  Abstract 

We describe 6 cases of invasive fungal diseases in the post kidney transplant setting. These include 2 cases each of mucormycosis and Aspergillosis and 1 case each of pheohyphomycosis and histoplasmosis. Our case series includes the first described case of aspergillus sacroilitis post kidney transplant and also reviews the literature on various modalities of treatment of fungal infections, follow up, diagnostic modalities and appropriate drug choices.

Keywords: Infections, invasive fungal disease, renal transplantation


How to cite this article:
Ganesh K, Abraham M A, Kumar JS, Simon S. Invasive fungal diseases in renal transplantation - Case series. Indian J Transplant 2021;15:169-75

How to cite this URL:
Ganesh K, Abraham M A, Kumar JS, Simon S. Invasive fungal diseases in renal transplantation - Case series. Indian J Transplant [serial online] 2021 [cited 2021 Jul 24];15:169-75. Available from: https://www.ijtonline.in/text.asp?2021/15/2/169/319883


  Introduction Top


Invasive fungal infections represent some of the most lethal infections in an immunocompromised patient.[1],[2] Often underdiagnosed, they need a high index of suspicion to detect and treatment is often multi-disciplinary. We present our experience with invasive fungal infections at varying times post kidney transplant.


  Case Reports Top


Case 1

A 51-year-old male, with diabetic nephropathy, on maintenance hemodialysis for 2 years through a left forearm AV fistula underwent renal transplantation. On the post-operative day 11, he developed severe right hypochondriac pain along with fever and a toxic appearance. Relevant investigations were as follows: Hb 8.8 g/dl, TC 33,000 cells/mcL, aspartate aminotransferase (AST) 250 U/L, AST 766 U/L, and alkaline phosphatase 166U/L. An ultrasound (USG) abdomen showed a 17-mm hypoechoic area in the right lobe of the liver. A computed tomography (CT) of the abdomen showed an enlarged liver with multiple hypodense lesions around 3.5 cm in size involving both lobes [Figure 1]a. An USG-guided fine-needle aspiration cytology of one of the liver abscesses was done to show broad branching septate hyphae, suggestive of mucor [Figure 2]a. The patient was started on broad-spectrum antifungals (liposomal amphotericin B) and antibiotics. However, he developed worsening sepsis and liver failure and succumbed on the postoperative day 22.
Figure 1: Radiological features: (a) Case 1, computed tomography Abdomen: Enlarged liver with multiple hypodense lesions in both lobes of liver- abscess/metastasis. (b) case 2: computed tomography Chest: Ill defined area with soft tissue margins involving apical segment of right upper lobe, probable fungal mass. (c) Case 3, computed tomography Chest: 8 and 10 mm subpleural nodules- base of left lower lobe. (d) Case 4: computed tomography Paranasal sinus: Complete soft tissue opacification of the right maxillary sinus with defect in its medial wall and extension into the nasal cavity

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Figure 2: Histopathology: (a) Case 1, Liver lesion aspirate Silver stain, Broad branching septate Hyphae, Mucor species. (b) Case 2, Lung biopsy, H and E stain, fungal hyphae among necrotic tissue, Mucor species. (c) Case 3, Lung biopsy, silver stain, Sheets of histiocytes distended with intracellular ovoid yeasts with narrow based budding basophilic nucleus and perinuclear halo. (d) Case 5, bone biopsy, H and E stain, thin hyphae with acute angle branching, Aspergillus species. (e) Case 5, bone biopsy, silver stain, Aspergillus species

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Case 2

A 40-year-old male, underwent renal transplantation. 1 year after transplant, he presented with 2 weeks history of exertional dyspnea and recurrent hemoptysis. Chest X-ray showed haziness in the right upper zone. A CT chest showed an ill-defined area with soft-tissue margins involving the apical segment of the right upper lobe [Figure 1]b. He was immediately started on broad-spectrum antibiotics and antifungals (Liposomal Amphotericin, Posaconazole) and given intermittent hemodialysis due to worsening graft function. After 2 weeks of therapy, a repeat HRCT chest showed progression of the right lung lesion with new infiltrates in the left lung base. He then underwent a right lung lobectomy. Histopathology showed broad nonseptate fungal hyphae within necrotic tissue along with demonstrable angio-invasion, later identified as Mucor [Figure 2]b. In addition, he received prolonged anti-fungal therapy with Amphotericin B and Posaconazole. A repeat HRCT chest done 2 weeks after the lobectomy showed resolution of residual lesions. The patient survived; his graft failed and is currently on maintenance hemodialysis planning for a second transplant.

Case 3

A 41-year-old female, underwent renal transplantation. She presented with a 2 month history of weight loss and intermittent fever 14 years after transplant. As part of fever workup, a CT chest showed multiple small lymph nodes in the bilateral lower paratracheal region and left hilum [Figure 1]c and subpleural nodules of 8 and 10 mm in size in the base of left lower lobe. A video-assisted thoracoscopic biopsy of the nodule was done. Histopathology revealed sheets of histiocytes distended with intracellular ovoid yeasts with basophilic nucleus, perinuclear halo and narrow base budding, which were subsequently identified as Histoplasma Capsulatum [Figure 2]c. She was treated with Parenteral Amphotericin B for 4 weeks, and then switched to Itraconazole for 1 year. Tacrolimus dose adjusted to achieve a Tac level of 4–6 ng/ml. Gradually, she became afebrile and asymptomatic.

Case 4

A 52-year-old male, underwent renal transplantation. 7 months posttransplant, he presented with swelling over the right side of the face. A CT scan of the face and paranasal sinuses showed complete soft-tissue opacification of the right maxillary sinus with extension into the nasal cavity [Figure 1]d and destruction of the posterior wall with the lesion extending into the infratemporal fossa. A functional endoscopic sinus surgical biopsy was done to reveal Fungal hyphae with septation and acute angle branching and no angioinvasion, later identified as Aspergillus fumigatus. The lesion was cleared surgically and he was continued on Voriconazole for a year with close monitoring of tacrolimus dose. There was complete clearance of the lesion on follow-up CT scans. He currently has normal graft function 4 years after the surgery.

Case 5

A 52-year-old male with diabetic kidney disease underwent renal transplantation. 6 months posttransplant, he presented with severe pain in the right gluteal region along with inability to walk without severe pain. A magnetic resonance imaging (MRI) of the affected area showed articular erosions in the right sacroiliac joint. An open bone biopsy was done. The histopathology showed multiple foci fungal hyphae infiltrating the bone, with septation and acute angle branching, which was further identified as Aspergillus species [Figure 2]d and [Figure 2]e. He was started on liposomal amphotericin B and given a cumulative dose of 5 g. He showed marked clinical improvement and was mobile without support at the end of antifungal therapy. Graft functions remained reasonably stable throughout the course of treatment.

Case 6

A 44-year-old male with presumed chronic glomerulonephritis underwent renal transplantation. 13 months posttransplant, the patient presented with a slowly growing swelling on the dorsum of the right hand in the web space between thumb and index finger of about 2 months. A wedge biopsy was done and the smear showed branching hyphae, later identified as phaeohyphomycosis. Along with surgical resection, he was treated with liposomal Amphotericin B for a week followed by oral Voriconazole for 1 year. With treatment, the swelling subsided and the patient became asymptomatic.

Further details of the case series are provided in [Table 1].
Table 1: Fungal case series details

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  Discussion Top


Among kidney transplant (KT) recipients, fungal infections represent 5% of all infections.[1] Candidiasis is the most frequent, followed by aspergillosis and cryptococcosis. Infections are the second-highest cause of mortality in KT recipients, with an increased incidence mainly related to the patient's immunosuppressed status. We present six such cases of invasive fungal infections in the KT population among patients treated at our hospital.

Cases 1 and 2 demonstrated two very different forms of presentation and outcomes with mucormycosis. Mucormycosis, though uncommon, is associated with high mortality in transplant recipients. Mucormycosis refers to a spectrum of diseases caused by fungi of the class.

Zygomycetes, order Mucorales. Although Zygomycetes are common in the environment, infection with this fungus is rare in humans due to the effectiveness of the intact human immune system.[2] Augmented immunosuppression to treat rejection, mainly in the form of steroids, may accelerate the course of mucormycosis infection. Renal transplant recipients are also at high-risk for mucormycosis because of chronic immunosuppression, frequent use of broad-spectrum antibiotics, and underlying metabolic disorders such as uremia and posttransplant diabetes mellitus.[3]

Modern day transplant physicians should be aware of mucormycosis as a deadly infection. In a large study among renal transplant recipients,[4] pulmonary mucormycosis accounted for 25% of patients with a mortality rate of 42.2%. Worrying statistics analyzed by this paper indicated a rising trend of mucormycosis in articles published from the 1970s to 2015. The possible causes of the growing incidence are manifold-enhanced use of immunosuppressive therapy, prolonged prophylaxis with antifungals lacking activity against zygomycetes, the rising prevalence of diabetes mellitus, advances in diagnostic techniques, increased awareness of clinicians and of course, publication bias.

In another study by Rammaert et al.,[5] major underlying diseases in cases of health care associated mucormycosis were solid organ transplantation (24%), diabetes mellitus (22%), and severe prematurity (21%). Graft-transmitted mucormycosis accounted for 14% of 169 cases of healthcare-associated mucormycosis. Mucormycosis was associated with the longest duration of hospitalization and the shortest 2-year survival in renal transplant patients, although it comprised only 2%–6% of invasive fungal infection (10-to 50-fold less common than invasive Candida or Aspergillus infections).

Indian data regarding mucormycosis has been published in a study conducted in IKDRC Ahmedabad by Godara et al.,[6] 1.20% of patients had evidence of mucor infection with a survival rate of 62.5%. The predominant forms of presentation of mucormycosis are rhinocerebral, pulmonary, gastrointestinal, cutaneous, and disseminated.

The mode of infection is commonly via inhalation of spores, and also by hematogenous dissemination. Transmission of mucor through deceased donor kidneys has been documented with near drowning victims.[7] Pulmonary mucor is transmitted through inhalation, hematogenous spread or lymphatics. It can present as Lobar consolidation, Isolated masses, Nodular disease, Cavitation or Wedge-shaped infarcts (thrombosis of the pulmonary vessels due to fungal angioinvasion).

The diagnosis of pulmonary mucormycosis is rarely made antemortem due to multiple factors-acute nature, lack of awareness, and the need for tissue to establish the diagnosis. In addition, sputum cultures are usually negative. Definite diagnosis requires histological demonstration of tissue invasion with characteristic broad aseptate hyphae showing angioinvasion. In case 1, due to the rapidity and severity of the development of liver abscesses, an aspiration of the liver lesion yielded mucor. In case 2, it was only diagnosed on histopathological examination of the pneumonectomy specimen. Cultures in both cases were not rewarding.

Therefore, the rising incidence and high mortality associated with mucormycosis, especially in an immunosuppressed scenario make it imperative to make a quick diagnosis and execute effective treatment. A major obstacle in choosing antifungal is the lack of clinical trials and a poor rate of success of monotherapy, making it difficult to perform comparative trials given the life threatening nature of the illness. Amphotericin B is the mainstay of therapy in mucormycosis, since various species that cause mucormycosis have a broad range of susceptibilities to amphotericin. Preference for liposomal amphotericin over conventional preparations was demonstrated by a retrospective review of 120 cases of mucormycosis in patients with hematological malignancies.[8] Treatment with liposomal amphotericin was associated with a 67% survival rate, compared to 39% survival when patients were treated with amphotericin B deoxycholate. There are also animal studies showing the superiority of liposomal amphotericin,[9] where the survival rate was nearly double with high dose liposomal amphotericin B. These studies are limited by their retrospective nature and obvious limitations in animal models; nevertheless, based on the combination of these retrospective clinical data, animal models and historical experiences high doses of lipid formulation amphotericin are increasingly the preferred initial antifungal therapy for patients with mucormycosis. Itraconazole is the only azole that has in vitro activity against Mucorales.[10] However, Itraconazole should not be considered a first-line agent and should be used as adjunctive therapy. Posaconazole and ravuconazole are investigational triazoles that have promising in vitro activity against the agents of mucormycosis. In experimental animal models of disseminated mucormycosis, posaconazole is more efficacious than itraconazole but less efficacious than conventional amphotericin B (10.). Successful outcomes have been seen in patients with rhinocerebral mucormycosis in conjunction with amphotericin,[11] and in a heart/KT patient who failed on amphotericin therapy.[12] Both our patients received the combination of liposomal amphotericin B and posaconazole.

Clinical experience with echinocandins is limited. There are case reports of micafungin being used as an add on salvage therapy to a patient failing antifungal therapy for craniofacial mucormycosis.[13] The patient began responding to therapy shortly after the addition of micafungin and was ultimately cured. These data suggest that echinocandins may have a role as a second agent.

Source control being of paramount importance, whenever possible, surgical resection should be carried out. In Case 2, since the lesions increased with antifungal therapy alone, and since the lung lesion was reasonably well demarcated, an early pneumonectomy was done. This in addition to continued antifungal therapy was contributory in saving his life. The role of early pneumonectomy has been described.[14] Although the procedure is not without its complications (empyema, infectious seeding), it may be life saving in certain cases.

The importance of source control in mucormycosis was also demonstrated in a study by Tedder et al.[15] In this study, overall mortality in mucormycosis was 65% for patients with isolated lung involvement, 96% for those with disseminated disease, and 80% overall. However, mortality in patients treated surgically was 11%.

Histoplasmosis is an endemic mycosis that can cause serious manifestations in the immunosuppressed setting. The spectrum of pulmonary histoplasmosis can be widespread, with presentations such as pneumonia, mediastinal or hilar masses, pulmonary nodules, cavitary lung disease, pericarditis with mediastinal lymphadenopathy, pulmonary manifestations with arthritis or arthralgia plus erythema nodosum, and superior vena cava syndrome.

In the largest published series (152 cases) of histoplasmosis after solid organ transplant,[16] Histoplasma-related mortality was 10%, with most deaths occurring soon after diagnosis. One-third of the cases occurred within 1 year of transplant, and almost half occurred in the first 2 years after transplant. The median time from transplant to diagnosis with histoplasmosis was 27 months, but 34% presented in the 1st year, with 2% presenting within 1 month of transplant. The longest interval from transplant to diagnosis was 20 years. Our case is probably an outlier, presenting 14 years post KT. Very early development of disease and presence of granulomas in the transplanted organ are clues to donor derived etiology.

The incidence of clinical histoplasmosis varies, but is <0.5% in most studies. Infection can be difficult to predict with variable clinical presentation, response to therapy, and risk for complications. Symptomatic infection could occur via primary infection, secondary infection in patients with prior exposure who come in contact with a large inoculum in an immunosuppressed state, and reactivation of previous latent infection.

Sources of infection in the posttransplant scenario may be de novo, reactivation and rarely donor derived. While assessing live donors for possible prior history of histoplasmosis, the following factors should be asked for: Prior history of undiagnosed pneumonia in the past 2 years, CF titers of ≥1:32, antigenuria or antigenemia, Pneumonia, fever antibody, sweats, weight loss. In case of active disease in the donor, the donor should be treated with-itraconazole for 3–6 months prior to organ donation.

In cases of deceased donor transplant, where extensive history taking may be difficult, issues such as hospitalization for nonhemorrhagic neurological disease, fever of unknown origin, or pneumonia of unknown etiology, use of antifungal prophylaxis or therapy, or presence of hepatosplenomegaly should point toward a possible fungal etiology.

The organ should be inspected for granulomas at the time of harvesting. If donor granulomas are noted, histopathological analysis as well as antigen and antibody testing should be performed. The recipient should be tested for antigenemia and antigenuria at 3-month intervals during the 1st year after transplantation Positive tests for antigen would be an indication for treatment for histoplasmosis.[17]

In the study by Assi et al.,[16] antigen detection provided the highest sensitivity for diagnosis, 93% for antigenuria and 86% for antigenemia. The detection of antibody was the least sensitive diagnostic method, positive in 36% of cases. Antigen detection was more sensitive in patients with disseminated disease compared to those with pulmonary disease alone. Antigenuria was the most sensitive diagnostic test. Antigenuria or antigenemia are good parameters useful in noninvasive diagnosis of the disease and can be used in follow-up to monitor disease activity. The sensitivity of these parameters reduces in pulmonary histoplasmosis.

The duration of treatment is ill defined. Guidelines cited by Singh et al. recommend using Liposomal amphotericin B in moderately severe infections until the infection is controlled and then switching over to Itraconazole which should be given for at least a year, perhaps indefinitely in case of further need of immunosuppression in the form of anti-rejection therapies. In our case, we continued liposomal amphotericin for 4 weeks and then switched to Itraconazole, which was maintained for a year and gradually withdrawn. Tacrolimus doses were regularly monitored to keep the levels between 4 and 6 ng/ml. There were no intervening rejections and graft function stabilized. Guidelines published by the American Society of KT recommend Liposomal amphotericin B for 1–2 weeks in patients with more severe illness, followed by itraconazole. Treatment should be continued for at least 1 year and further, until the prescribed markers of serum Histoplasma antigen level and urine antigen levels have become negative and < 2 ng/ml, respectively. Longer courses may be necessary depending upon the response.

However due to limited availability of these tests, often the clinician has to make a clinical decision in the treatment duration.

Itraconazole is appropriate in patients with milder illness not requiring hospitalization. Prolonged therapy with itraconazole may be required in some patients such as individuals in whom antigenemia and antigenuria fail to meet the criteria for discontinuation of therapy or who relapse upon discontinuation of therapy. Some physicians continue itraconazole indefinitely in patients who require augmented immunosuppression for rejection. Voriconazole, posaconazole, and fluconazole may be considered as alternatives to itraconazole Fluconazole is the least active of the azoles for histoplasmosis.

Invasive aspergillosis is a rapidly fatal condition in the immunocompromised host if not diagnosed early and treated promptly. Aspergillosis covers a wide spectrum of disease from allergic and hypersensitivity pneumonitis to invasive pulmonary disease. Invasive aspergillosis causes tremendous morbidity and mortality.

Data from the Transplant Associated Infections Surveillance Network from 2001 to 2006[18] revealed a 25.4% and 59% 1-year survival from among hematopoietic stem cell transplant recipients and solid organ transplant recipients, respectively.

While invasive rhino-orbital aspergillosis is well documented, Aspergillus sacroilitis is rare. In an article by Golmia et al.,.[19] a case of Aspergillus sacroilitis was described in a patient post an autologous stem cell transplant who presented with intense low back pain. The MRI of the pelvis showed marrow edema at the sacroiliac joint. Fluid aspiration from the joint yielded Aspergillus. Our patient also presented with low back pain and had marrow edema on the MRI. Both these cases underscore the high index of suspicion of infective etiologies in cases of otherwise seemingly nonspecific “aches and pains” in immunosuppressed individuals.

Aspergillus is widespread in nature and is acquired via the inhalational route. In the study by Golmia et al., hematological malignancies, stem cell transplantation, and postarticular corticosteroid infiltration were the three major medical conditions associated with joint infection by Aspergillus. It is the first report of a sacroiliac joint affected by Aspergillus. To our knowledge, ours is the first case of Aspergillus sacroilitis described in the post renal transplant setting and the second case reported overall.

Aspergillus species have been rarely cultured from the preservation fluid[20] and contaminated preservation fluid has been suspected to be the mode of transmission of aspergillosis associated with fungal arteritis, mycotic aneurysms, anastomotic infections, and graft site abscesses/fungus ball in kidney and liver transplant recipients.

Voriconazole forms the mainstay of treatment. In the study by the Global Aspergillus study group,[21] two management strategies for invasive aspergillosis were compared-conventional amphotericin B versus voriconazole. Voriconazole was found to be more effective in terms of response, survival and drug reactions. Therefore, initial therapy of invasive aspergillosis can be started with Voriconazole monotherapy. In severe disease, an echinocandin may be added for the first 2 weeks. When there is concern for drug interactions between azoles (as a class) and other agents, as occurs in transplant patients on calcineurin inhibitors, a lipid formulation of amphotericin B can be used. Fluconazole has no activity against Aspergillus. We initially treated our patient with liposomal amphotericin B and then switched to voriconazole with close monitoring of tacrolimus levels and adjusting the dose accordingly. Certain species like Aspergillus calidoustus and Aspergillus terreus tend to be azole resistant-in these cases, a combination of drugs (e.g., voriconazole and an echinocandin) may be considered. Thus species identification is paramount to guide choice of antifungal agents. Antifungal therapy is generally continued until all signs and symptoms of the infection have resolved and often longer in patients with persistent immune defects.

If an invasive mold infection is suspected but the diagnosis of invasive aspergillosis has not been established-treating empirically with a lipid formulation of amphotericin B in order to provide antifungal activity against both Aspergillus species and the Mucorales is rational, since the Mucorales are intrinsically resistant to voriconazole. The optimum duration of therapy is unknown. The guidelines by the American Society of transplantation[17] recommend full treatment dose of Voriconazole (6 mg/kg BID × 2 doses, then 4 mg/kg BID, or 200–300 mg BID) until complete resolution, and then to consider the lower dose as secondary lifelong prophylaxis.

The term “phaeohyphomycosis” describes infections caused by pigmented filamentous fungi (dematiaceous) with cell wall melanin. The word “Dematiaceous” is a broad term denoting darkly pigmented fungi. There are more than 100 species and 60 genera of fungi in a variety of clinical syndromes caused by pheohyphomycosis. Revankar et al.[22] found immunosuppression to be the major risk factor in developing the disease, however solid organ transplant ranked below neutropenia, AIDS, bone marrow transplant, and malignancies in the risk assessment profile. Optimal therapy for these infections remains uncertain.

The pathogenesis of infections due to dematiaceous fungi is not well understood. Superficial infections are generally considered secondary to local trauma and manifest little tissue invasion; disseminated infection is uncommon except in immunocompromised individuals. Melanin, which is present in the cell wall of all dematiaceous fungi, is a likely virulence factor. The diagnosis of phaeohyphomycosis, as noted in our study, primarily relies on careful examination of growth that appears in culture and histopathological examination of tissue specimens. The Fontana-Masson stain, which is specific to melanin, should be used.[23]

The European Confederation of Medical Mycology, together with the European Society of Clinical Microbiology and Infectious Diseases, recently published recommendations for therapy of phaeohyphomycosis (ESCMID and ECMM joint clinical guidelines for the diagnosis and management of systemic phaeohyphomycosis: diseases caused by black fungi.[24] According to these guidelines, There are no standardized therapies but voriconazole, posaconazole, and itraconazole demonstrated consistent in vitro activity against these fungi. Oral itraconazole has been considered the drug of choice, given the extensive clinical experience with this drug. Posaconazole is a possible alternative drug choice, backed by less clinical experience but with excellent salvage treatment results after failure of other antifungals. Amphotericin B has been useful as alternative therapy in some cases. Combination antifungal therapy is recommended for cerebral abscesses when surgery is not possible and for disseminated infections in immunocompromised patients. Length of therapy is primarily based on the clinical presentation, the underlying condition of the host and the initial response. For subcutaneous nodules in particular, surgery alone has been effective. Multiple subcutaneous nodules have to be treated with systemic antifungal agents. Itraconazole or voriconazole at 400 mg are recommended. The guidelines suggest using combination antifungal therapy for the central nervous system and disseminated infection, and combination therapy is often used for more refractory infections.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form, the legal guardian has given his consent for images and other clinical information to be reported in the journal. The guardian understands that names and initials will not be published and due efforts will be made to conceal identity, but anonymity cannot be guaranteed.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
  References Top

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José Pérez-Sáez M, Mir M, Montero MM, Crespo M, Montero N, Gomez J, et al. Invasive aspergillosis in kidney transplant recipients: A cohort study. Exp Clin Transplant 2014;2:101-5.  Back to cited text no. 1
    
2.
Kauffman CA, Malani AN. Zygomycosis: An emerging fungal infection with new options for management. Curr Infect Dis Rep 2007;9:435-40.  Back to cited text no. 2
    
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Rammaert B, Lanternier F, Zahar JR, Dannaoui E, Bougnoux ME, Lecuit M, et al. Healthcare-associated mucormycosis. Clin Infect Dis 2012;54:S44-54.  Back to cited text no. 5
    
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Jacobs P, Wood L, Du Toit A, Esterhuizen K. Eradication of invasive mucormycosis – Effectiveness of the Echinocandin FK463. Hematology 2003;8:119-23.  Back to cited text no. 13
    
14.
Vercillo MS, Liptay MJ, Seder CW. Early pneumonectomy for pulmonary mucormycosis. Ann Thorac Surg 2015;99:e67-8.  Back to cited text no. 14
    
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Assi M, Martin S, Wheat LJ, Hage C, Freifeld A, Avery R, et al. Histoplasmosis after solid organ transplant. Clin Infect Dis 2013;57:1542-9.  Back to cited text no. 16
    
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Singha N, Huprikar S, Burdette SD, Morris MI, Blair JE, Wheat LJ, et al. Donor-derived fungal infections in organ transplant recipients: Guidelines of the American Society of Transplantation, infectious diseases community of practice. Am J Transplant 2012;12:2414-28.  Back to cited text no. 17
    
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Dimitrios P, Marr KA, Park BJ, Alexander BD, Anaissie EJ, Walsh TJ, et al., Prospective surveillance for invasive fungal infections in hematopoietic stem cell transplant recipients, 2001–2006: Overview of the Transplant-Associated Infection Surveillance Network (TRANSNET) Database. Clin Infect Dis 2010;50:1091-100.  Back to cited text no. 18
    
19.
Golmia R, Bello I, Marra A, Hamerschlak N, Osawa A, Scheinberg M. Aspergillus fumigatus joint infection: A review. Semin Arthritis Rheum 2011;40:580-4.  Back to cited text no. 19
    
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Battaglia M, Ditonno P, Selvaggio O, Garofalo L, Palazzo S, Schena A, et al. Kidney transplants from infected donors: Our experience. Transplant Proc 2004;36:491-2.  Back to cited text no. 20
    
21.
Herbrecht R, Denning DW, Patterson TF, Bennett JE, Greene RE, Oestmann JW, et al. Voriconazole versus amphotericin B for primary therapy of invasive aspergillosis. N Engl J Med 2002;347:408-15.  Back to cited text no. 21
    
22.
Revankar SG, Baddley JW, Chen SC, Kauffman CA, Slavin M, Vazquez JA, et al. A mycoses study group international prospective study of phaeohyphomycosis: An analysis of 99 proven/probable cases. Open Forum Infect Dis 2017;4:ofx200. doi: 10.1093/ofid/ofx200. eCollection Fall 2017.  Back to cited text no. 22
    
23.
Matsumoto T, Ajello L, Matsuda T, Szaniszlo PJ, Walsh TJ. Developments in hyalohyphomycosis and phaeohyphomycosis. J Med Vet Mycol 1994;32 Suppl: 329-49.  Back to cited text no. 23
    
24.
Chowdhary A, Meis JF, Guarro J, de Hoog GS, Kathuria S, Arendrup MC, et al. ESCMID and ECMM joint clinical guidelines for the diagnosis and management of systemic phaeohyphomycosis: Diseases caused by black fungi. Clin Microbiol Infect 2014;20 Suppl 3:47-75.  Back to cited text no. 24
    


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