Scedosporiosis in a Combined Kidney and Liver Transplant Recipient: A Case Report of Possible Transmission from a Near-Drowning Donor.
Scedosporium is a saprobic fungus that naturally occurs in soil, manure, sewage, and water bodies polluted by environmental contaminants. Cases of infections with Scedosporium spp. are reported worldwide and can range in severity from colonization or local infection to disseminated disease [1-5]. S. apiospermum most commonly infects the lungs as inhalation is often the suspected mode of organism acquisition .
The genus Scedosporium includes, but is not limited to, three species that cause life-threatening infections in humans: Scedosporium apiospermum, Scedosporium prolificans (recently renamed Lomentospora prolificans), and Scedosporium aurantiacum . Scedosporium spp. appear as branching septate hyphae when isolated on standard culture media.
Scedosporium spp. have been implicated in neardrowning accidents [8-10]. Indeed Scedosporium spp. are the most common cause of fungal pneumonia, infection of the central nervous system, and disseminated disease following near-drowning events. There are few cases of donor to recipient transmission of infection of Scedosporium spp. and even fewer reports of near-drowning donor transmission of diseases [11, 12]. We report the clinical course and management of disseminated S. apiospermum infection in a combined kidney and liver transplantation case receiving organs from a brain-dead donor who suffered a neardrowning accident; we further review the literature on scedosporiosis in solid organ transplant recipients.
2. Case Presentation: Donor
A 41-year-old male fell into a freshwater lake. Emergency responders pulled him from the lake and return of spontaneous circulation was achieved after twenty minutes of resuscitation. Subsequent chest radiographs showed development and worsening of bilateral opacities suspicious for pneumonia. Brain death was declared three days after hospital admission.
3. Case Presentation: Recipient
A 66-year-old male actively listed for a kidney and liver transplant presented to the surgical intensive care unit with sepsis and an oxacillin-sensitive Staphylococcus aureus bacteremia. He was treated with appropriate antibiotic therapy. He then developed acute tubular necrosis requiring continuous venovenous hemofiltration (CVVH). The patient had a chest X-ray showing mild pulmonary congestion and bronchoscopy was not performed as the patient did not show signs of pneumonia. After two weeks within his admission, the patient was treated for Escherichia coli bacteremia with piperacillintazobactam. Repeat blood cultures were negative after two days of therapy.
While the patient was hospitalized, a donor became available. The donor kidney and liver were grossly normal. The patient underwent a combined kidney and liver transplant for chronic kidney failure with associated liver cirrhosis caused by the hepatitis C virus and alcoholism. The explanted liver was cirrhotic without any malignancy. At the time of transplantation, the patient's Model for End Stage Liver Disease (MELD) score was 40, having been decompensated in the surgical intensive care unit for the previous month. A summary of the patient's immunosuppression and antifungal management after transplant is provided in Figure 1.
The patient was given methylprednisolone 500 mg and mycophenolate mofetil 1,000 mg intraoperatively as induction immunosuppression. Maintenance immunosuppression protocols were followed after transplant. CVVH was performed intraoperatively and was discontinued on postoperative day (POD) 1 when renal graft function improved. The patient's hospital stay was complicated by a contained urine leak from the ureteroureterostomy which was managed nonoperatively with drains and ureteral stents. On POD 8, the patient was transferred out of the intensive care unit and on POD 14, to the inpatient rehab care unit as graft function continued to improve. The hepatic transaminases fluctuated and, on POD 25, he was transferred back to the surgical intensive care unit with peritonitis. As infection was suspected, immunosuppression was restricted to the use of corticosteroids tapered down to prednisone 5 mg daily. The patient was taken backto the operating room on POD 28 for a peritoneal washout. Cultures obtained during the procedure are presented in Tables 1 and 2. Of most concern was the S. apiospermum isolated from the perihepatic, perinephric, and biloma fluid. Endoscopic Retrograde Cholangiopancreatography (ERCP) was performed the following day, which did not reveal any extravasation. Discovery of S. apiospermum prompted contact with the Centers for Disease Control and Prevention (CDC), the Disease Transmission Advisory Committee (DTAC) of the United Network for Organ Sharing (UNOS), and the transplant centers treating recipients of allografts from the same donor. Other recipients had no evidence of infection.
On POD 28, due to worsening hemodynamics and peritonitis, another laparotomy and another washout were performed to evacuate an infected hematoma. The entire peritoneal surface was lined with mold. On POD 32, a mold suggestive of Scedosporium spp. grew from surgical cultures. Expert opinion for the management of our patient's suspected S. apiospermum infection was to use voriconazole targeting a trough of 2-4 mcg/mL, which we started on POD 32. Additionally, terbinafine was started for suspected synergy with voriconazole. A sample of the S. apiospermum was sent out for synergy studies which were expected to take a week or more to be conclusive. On POD 41 S. apiospermum was identified. Laboratory results suggested terbinafine was not synergistic with voriconazole. Additionally, terbinafine is distributed rapidly to skin and bone and as such is not distributed well into visceral tissue and accumulation of terbinafine may cause hepatotoxicity. In response, terbinafine was discontinued and granulocyte macrophage colony-stimulating factor (GMCSF) initiated on POD 42. The patient developed neurologic deficits with decreased vision to the right side and blurred vision bilaterally on POD 46. Magnetic resonance imaging (MRI) of the brain, shown in Figure 2, revealed multiple ring-enhancing lesions in the supratentorial compartment consistent with hematogenous central nervous system (CNS) scedosporiosis. We continued treatment with antifungal therapy. He developed septic shock and expired on POD 55.
Differential diagnoses for opportunistic pathogens causing pneumonia related to near-drowning events include several key pathogenic bacteria and fungi. Gram negative bacteria are most often the causative agents in near-drowning cases . Aeromonas spp. have been described most often in near-drowning pneumonia cases. Aeromonas spp. naturally thrive in fresh and brackish waters and have been isolated in humans in wound and gastrointestinal infections after exposure to contaminated water. Other potential bacterial pathogens include Pseudomonas aeruginosa, Legionella spp., Klebsiella spp., and other Enterobacteriaceae . Scedosporium spp. are the most common cause of invasive fungal infection, including pneumonia, CNS disease, and dissemination following near-drowning.
We identified 60 published cases of scedosporiosis after solid organ transplantation between the year 2000 and the present. Few were cases of scedosporiosis after solitary liver transplantation (5/60); most were reported following solitary lung (18/60) or kidney (18/60) transplantation. Table 3 [2, 12, 14-42] provides a summary of the comprehensive literature review performed. S. apiospermum was isolated in the majority of cases, though S. prolificans and S. aurantiacum were also isolated. In four cases, both S. apiospermum and S. prolificans were identified in the same patient. In patients who had infections with a single isolate of Scedosporium spp., the observed mortality rates of S. apiospermum, S. prolificans, and S. aurantiacum were 54.5% (24/44), 70% (7/10), and 100% (3/3), respectively (excluding four cases with combined infections). Observed mortality of all Scedosporium spp. infections was 59% (36/61) including our patient case.
Kim et al. reported three fatal and two nonfatal cases of scedosporiosis following solid organ transplantation from the same donor who was victim to a near-drowning accident . Additionally, they reviewed national Korean data on transplants and found that, among 2600 deceased-donor transplants over thirteen years, 27 (1%) of donors were victims of drowning. We accessed data from the United States Organ Procurement and Transplantation Network and found a similar rate: in 2015,102/7586 (approximately 1.3%) of solid organ donors died of near-drowning events . While this is a low percentage of all donors, the significance of our case is enhanced by the 58.3% mortality rate of infections involving Scedosporium spp. after solid organ transplantation.
At our center, liver transplant recipients are given antifungal prophylaxis based on their risk level. We stratify higher risk patients as those with MELD scores greater than 35, renal failure, requiring hemodialysis or CVVH prior to transplantation, recurrent spontaneous bacterial peritonitis, or preoperative prealbumin less than 10. High risk liver transplant recipients receive micafungin intravenously unless resistant Candida glabrata, Aspergillus spp., or Cryptococcus spp. are suspected; in such cases, amphotericin B lipid complex or voriconazole would be used. Our patient was classified as high risk and given micafungin prophylaxis.
All cases of suspected donor-derived infections should be reported to the DTAC. Communications with the CDC, DTAC, and the centers treating the recipients of the other organs provided by this donor revealed the recipient of the heart was receiving voriconazole prophylaxis, while the recipients of the other kidney and the pancreas were not. To the best of our knowledge, no other recipient of this donor's organs is infected with Scedosporium spp. The other centers were advised by the CDC to commence voriconazole prophylaxis for an undetermined duration. Expert opinion for the management of our patient's scedosporiosis was voriconazole targeting a trough of 2-4mcg/mL. Additionally, immunosuppression was to be limited or discontinued to improve infection clearance.
S. apiospermum is inherently resistant to amphotericin B, including the lipid formulations. Of the newer triazole antifungals, data on the in vitro activity of voriconazole is most robust, showing activity against S. apiospermum with MICs of 0.12 to 0.5 mcg/mL in clinical isolates . Because of poor activity with single agents, various antifungal combinations have been examined for efficacy against S. apiospermum. Strong synergy was found in vitro between voriconazole and terbinafine against clinical isolates of Scedosporium spp. . Combination of micafungin and voriconazole has demonstrated a synergistic effect against several fungi in vitro including Scedosporium spp. The synergistic mechanism may include reorganization of the cell wall allowing increased exposure of beta-glucan to the immune system .
In addition to antifungal agents, GM-CSF has been studied with some success [44,45]. While antifungal therapy remains crucial to recovery, the treatment of scedosporiosis infections depends on the function of the host's innate immune system, in particular, polymorphonuclear cells (PMNs). The mechanism of GM-CSF increases the antifungal action of PMNs in vitro .
Despite good allograft function, our patient did not survive disseminated infection with S. apiospermum after combined kidney and liver transplantation. The exact mode of transmission and acquisition of S. apiospermum in this patient remains uncertain. We suspect donor to recipient transmission as the donor was the victim of a near-drowning event and had chest radiographs suspicious for pneumonia; however, we cannot rule out recipient colonization or nosocomial infection after the transplant.
Infections caused by Scedosporium spp. following solid organ transplant, while not common, are often fatal for recipients. There are no standards of practice for prophylaxis for patients at risk for developing scedosporiosis, such as recipients of organs from nearly drowned donors. Considering our case and the scedosporiosis mortality rate over 50% and the low rate of nearly drowned donors, we recommend screening for Scedosporium spp. when donated organs originate from a near-drowning victim.
The authors declare that there is no significant conflict of interests regarding the publication of this paper.
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Rachael Leek, (1) Erika Aldag, (1) IramNadeem, (1) Vikraman Gunabushanam, (1) Ajay Sahajpal, (1, 2) David J. Kramer, (2,3) and Thomas J. Walsh (4)
(1) Department of Abdominal Transplant, Aurora St. Luke's Medical Center, Milwaukee, WI, USA
(2) University of Wisconsin School of Medicine and Public Health, Madison, WI 53726, USA
(3) Department of Critical Care, Aurora St. Luke's Medical Center, Milwaukee, WI, USA
(4) Weill Cornell Medicine, Cornell University and New York Presbyterian Hospital, New York, NY, USA
Correspondence should be addressed to Erika Aldag; email@example.com
Received 29 August 2016; Accepted 6 November 2016
Academic Editor: Graeme Forrest
Caption: Figure 1: Antifungal agents and immunosuppression management.
Caption: Figure 2: MRI of the brain. Multiple ring-enhancing lesions with associated diffusion restriction and T2/FLAIR hyperintensity are present throughout the supratentorial white matter.
Table 1: Culture results. Date Culture site Source Result C. tropicalis POD 28 Abdominal fluid Surgical specimen E. faecalis E. coli M. morganii E. faecium POD 28 Biloma fluid Surgical specimen E. faecalis S. apiospermum C. tropicalis S. apiospermum POD 28 Perihepatic fluid Surgical specimen E. faecium C. tropicalis POD 28 Perinephric hematoma Surgical specimen S. apiospermum tissue POD 32 Abdominal clot Surgical specimen S. apiospermum POD 32 Intestinal serosal Surgical specimen S. apiospermum tissue E. faecium POD 50 LUQ abdominal fluid Surgical specimen C. glabrata C. tropicalis POD 50 Cerebrospinal fluid Lumbar puncture Negative Table 2: Susceptibility testing of fungal isolates. Isolate Resistant (MIC) Intermediate (MIC) Scedosporium 5-Fluorocytosine (>64), apiospermum amphotericin B (>16), caspofungin (>8), None micafungin (>8), terbinafine (>2) Candida tropicalis None None Candida glabrata None None Isolate Susceptible (MIC) Scedosporium apiospermum Voriconazole (1) Caspofungin ([less than or equal to] 0.25), Candida tropicalis fluconazole ([less than or equal to] 1), voriconazole ([less than or equal to] 0.12) Caspofungin (2), Candida glabrata fluconazole ([less than or equal to] 1), voriconazole ([less than or equal to] 0.12) Table 3: Review of solid organ transplant-associated Scedosporium infection. Ref # Year Recipient information Recipient Age (years) Gender organ(s)  2000 67 Male Heart 42 Female Heart/lung 22 Female Heart/lung  42 Male Heart/lung 2001 49 Male Lung 39 Male Lung 52 Female Lung 38 Female Heart/lung 58 Female Liver 37 Male Lung 30 Male Lung  2002 37 Female Heart/lung 39 Male Liver 67 Male Heart 36 Male Kidney  2002 49 Male Kidney  2002 62 Female Kidney 58 Male Kidney  2002 64 Female Lung  2002 71 Male Heart  2003 24 Male Lung 59 Male Kidney  2004 50 Male Kidney  2004 58 Male Kidney  2004 56 Female Lung 55 Male Small bowel 40 Male Kidney/pancreas 67 Male Kidney 51 Female Small bowel 67 Male Heart 17 Male Liver  2005 64 Male Liver 45 Male Heart 56 Male Liver 44 Female Heart 68 Male Kidney 52 Male Small bowel 62 Male Kidney/pancreas  2005 26 Female Lung  2006 58 Male Kidney 57 Male Lung  2006 63 Male Lung  2007 59 Female Kidney  2007 43 Male Lung  2008 70 Male Kidney  2009 65 Female Kidney  2010 37 Female Lung  2011 16 Female Lung  2012 35 Male Lung/liver  2012 37 Female Lung  2013 17 Female Lung  2013 70 Female Lung  2014 50 Female Kidney  2014 35 Male Kidney  2015 70 Male Heart 19 Male Heart  2015 56 Male Kidney 57 Female Kidney  2015 40 Male Kidney  2015 18 Female Lung Ref # Year Species of Scedosporium  2000 apiospermum apiospermum prolificans + apiospermum  prolificans + apiospermum 2001 prolificans + apiospermum prolificans + apiospermum apiospermum apiospermum apiospermum apiospermum apiospermum  2002 apiospermum apiospermum apiospermum apiospermum  2002 apiospermum  2002 apiospermum apiospermum  2002 apiospermum  2002 apiospermum  2003 apiospermum apiospermum  2004 apiospermum  2004 apiospermum  2004 prolificans prolificans prolificans apiospermum prolificans apiospermum prolificans  2005 apiospermum apiospermum apiospermum prolificans prolificans apiospermum apiospermum  2005 apiospermum  2006 apiospermum apiospermum  2006 apiospermum  2007 apiospermum  2007 apiospermum  2008 prolificans  2009 apiospermum  2010 apiospermum  2011 apiospermum  2012 apiospermum  2012 apiospermum  2013 apiospermum  2013 prolificans  2014 apiospermum  2014 prolificans  2015 apiospermum aurantiacum  2015 aurantiacum aurantiacum  2015 apiospermum  2015 apiospermum Ref # Year Treatment approach Outcome  2000 Voriconazole Deceased Fluconazole, itraconazole Deceased Fluconazole, itraconazole Deceased  Fluconazole, itraconazole Alive 2001 Fluconazole, itraconazole Deceased Fluconazole, itraconazole Alive Fluconazole, itraconazole Alive Fluconazole, itraconazole Deceased Itraconazole, miconazole Alive Itraconazole Deceased Amphotericin B, miconazole Deceased  2002 Miconazole Deceased 5-Flucytosine, amphotericin B Deceased Itraconazole, voriconazole Deceased Itraconazole, miconazole Deceased  2002 Voriconazole Deceased  2002 None Deceased Itraconazole, voriconazole Alive  2002 Amphotericin B, itraconazole Deceased  2002 Itraconazole Alive  2003 Voriconazole Alive Voriconazole Alive  2004 Voriconazole Alive  2004 Amphotericin B, fluconazole, Alive itraconazole, miconazole  2004 Voriconazole Deceased Amphotericin B Deceased Voriconazole Alive Amphotericin B Alive Amphotericin B, Voriconazole, Deceased caspofungin Voriconazole Deceased Voriconazole Deceased  2005 None Deceased Itraconazole Deceased Voriconazole Deceased Amphotericin B Deceased Voriconazole Alive Amphotericin B, Voriconazole, Alive caspofungin Voriconazole Alive  2005 Miconazole, voriconazole Deceased  2006 Miconazole, voriconazole Alive Terbinafine, voriconazole Alive  2006 Liposomal amphotericin B, Alive terbinafine, voriconazole  2007 Voriconazole Alive  2007 Caspofungin, itraconazole, Deceased liposomal amphotericin B  2008 Terbinafine, voriconazole Alive  2009 Voriconazole Alive  2010 Caspofungin, terbinafine, Deceased voriconazole  2011 Voriconazole Alive  2012 Caspofungin, voriconazole Deceased Aerosolized amphotericin B,  2012 caspofungin, itraconazole, Deceased voriconazole  2013 Caspofungin, posaconazole, Alive voriconazole  2013 Caspofungin, terbinafine, Deceased voriconazole  2014 Voriconazole Alive Itraconazole, liposomal  2014 amphotericin B, micafungin, Deceased voriconazole  2015 Posaconazole, terbinafine Deceased Amphotericin B prophylaxis Deceased  2015 Itraconazole, liposomal Deceased amphotericin B Caspofungin, voriconazole Deceased  2015 Voriconazole Deceased  2015 Terbinafine, voriconazole Alive
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|Title Annotation:||Case Report|
|Author:||Leek, Rachael; Aldag, Erika; Nadeem, Iram; Gunabushanam, Vikraman; Sahajpal, Ajay; Kramer, David J.;|
|Publication:||Case Reports in Transplantation|
|Article Type:||Case study|
|Date:||Jan 1, 2016|
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