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References 1. European Centre for Disease Prevention and Control. Clusters

of autochthonous chikungunya cases in Italy, 14 September 2017. Stockholm: The Centre; 2017 [cited 2017 Oct 6]. https://ecdc.europa.eu/sites/portal/files/documents/ 14-Sep-2017-RRA-Chikungunya-Italy-revised.pdf

2. Rezza G, Nicoletti L, Angelini R, Romi R, Finarelli AC, Panning M, et al.; CHIKV Study Group. Infection with chikungunya virus in Italy: an outbreak in a temperate region. Lancet. 2007;370:1840–6. http://dx.doi.org/10.1016/S0140-6736(07)61779-6

3. World Health Organization. Disease outbreak news. Chikungunya—Italy. 2017 [cited 2017 Oct 10]. http:/www.who.int/csr/don/29-september-2017-chikungunya-italy/en

4. Schuffenecker I, Iteman I, Michault A, Murri S, Frangeul L, Vaney MC, et al. Genome microevolution of chikungunya viruses causing the Indian Ocean outbreak. PLoS Med. 2006;3:e263. http://dx.doi.org/10.1371/journal.pmed.0030263

5. Tsetsarkin KA, Vanlandingham DL, McGee CE, Higgs S. A single mutation in chikungunya virus affects vector specificity and epidemic potential. PLoS Pathog. 2007;3:e201. http://dx.doi.org/10.1371/journal.ppat.0030201

6. Vazeille M, Moutailler S, Coudrier D, Rousseaux C, Khun H, Huerre M, et al. Two chikungunya isolates from the outbreak of La Reunion (Indian Ocean) exhibit different patterns of infection in the mosquito, Aedes albopictus. PLoS One. 2007;2:e1168. http://dx.doi.org/10.1371/journal.pone.0001168

7. Bordi L, Carletti F, Castilletti C, Chiappini R, Sambri V, Cavrini F, et al. Presence of the A226V mutation in autochthonous and imported Italian chikungunya virus strains. Clin Infect Dis. 2008;47:428–9. http://dx.doi.org/10.1086/589925

Address for correspondence: Maria R. Capobianchi, Laboratory of Virology, Padiglione Baglivi, National Institute of Infectious Diseases “L. Spallanzani,” Via Portuense 292, 00149 Rome, Italy; email: maria.capobianchi@inmi.it

Inonotosis in Patient with Hematologic Malignancy

Ana Fernández-Cruz,1 Mi Kwon,1 Jesús Guinea, Pilar Escribano, María del Carmen Martínez Jiménez, Ana Pulido, Verónica Parra, David Serrano, Jorge Gayoso, José Luis Díez Martín, Emilio BouzaAuthor affiliations: Hospital General Universitario Gregorio Marañón, Madrid, Spain (A. Fernández-Cruz, M. Kwon, J. Guinea, P. Escribano, M.C. Martínez Jiménez, A. Pulido, V. Parra, D. Serrano, J. Gayoso, J.L. Díez Martin, E. Bouza); Instituto de Investigación Sanitaria Gregorio Marañón, Madrid

(A. Fernández-Cruz, M. Kwon, J. Guinea, P. Escribano, M.D.C.M. Jiménez, A. Pulido, V. Parra, D. Serrano, J. Gayoso, J.L.D. Martin, E. Bouza); CIBER de Enfermedades Respiratorias (CIBERES CB06/06/0058), Madrid (J. Guinea, E. Bouza)

DOI: https://doi.org/10.3201/eid2401.171265

We report a lung-invasive fungal disease with possible cu-taneous needle tract seeding in a patient with a febrile neu-tropenia caused by the Basidiomycetes mold Inonotus spp. Although rare, Inonotus spp. should be added to the list of microorganisms causing invasive fungal disease in neutro-penic patients with hematologic malignancies.

A 33-year-old man in Madrid, Spain, with chronic myeloid leukemia in lymphoid blastic phase under-

went allogeneic stem cell transplantation (SCT) from a matched unrelated donor in 2011. Four years later, he had an extramedullary pulmonary relapse, after which he began intensive reinduction chemotherapy. After the second cycle, prolonged severe aplasia developed in the patient. Invasive fungal disease (IFD) was suspected because of the presence of persistent fever despite broad-spectrum antimicrobial drugs and the appearance of a new pulmonary nodule (Fig-ure, panel A; online Technical Appendix, https://wwwnc.cdc.gov/EID/article/24/1/17-1265-Techapp1.pdf) while the patient was receiving prophylactic micafungin (50 mg/d). Serologic fungal biomarkers were negative. A percutaneous pulmonary biopsy sample was taken, and empirical lipo-somal amphotericin B (3 mg/kg/d) was started (December 2015). Histology showed unspecific inflammatory tissue, and microbiology cultures were negative.

Salvage human leukocyte antigen–haploidentical SCT was performed in January 2016. Fever persisted during conditioning therapy, and a solitary cutaneous millimet-ric erythematous lesion appeared at the biopsy puncture site (Figure, panel B). Histopathology of the skin lesion showed dermal infiltration by periodic acid Schiff–posi-tive elements compatible with fungal hyaline hyphae with parallel walls, regular septa, and branched hyphae with oc-casional bulb-like expansions; angioinvasion; and necrosis. Fungal culture of the specimen was negative, but panfungal PCR and further sequencing (1) revealed the presence of Inonotus spp. Voriconazole was added, and the lesion re-solved in days. Neutrophil engraftment was achieved on day 12 post-SCT, with complete donor chimerism.

On day 34, the pulmonary lesion progressed, but we could not prove IFD as the cause of concomitant pleural effusion. Despite intensified antifungal therapy, surgical debridement was required to resolve the empyema. The pa-tient was discharged on oral posaconazole (300 mg/d) that was eventually replaced by micafungin.

A computed tomography scan performed 6 months af-ter the SCT showed persistence of a single mass on the left 1These authors contributed equally to this article.

Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 24, No. 1, January 2018 181

RESEARCH LETTERS

lung inferior lobe together with a new hepatic nodule. We performed pulmonary segmentectomy, and lung histology showed mycetoma with fungal elements similar to those ob-served in the previous skin biopsy. The fungal culture yielded a fluffy, white, slow-growing mold. The lack of sporulation did not permit morphologic identification, although panfun-gal PCR and further sequencing again revealed the presence of Inonotus spp. in the lung tissue sample.

Filamentous Basidiomycetes molds are ubiquitous and able to colonize in patients with chronic pulmonary disease. They cause syndromes comparable to allergic bronchopulmonary or rhinosinusal aspergillosis. How-ever, IFD caused by Basidiomycetes molds are extremely rare (2). It has been hypothesized that IFD could occur in patients with mycetoma if they become immunocompro-mised. Clinical presentation resembles that of other IFDs, with predominantly pulmonary involvement (online Technical Appendix Table 1). Most filamentous Basid-iomycetes are susceptible to antifungal drugs except for fluconazole and echinocandins. However, because many isolates do not sporulate, morphologic identification in the clinical microbiology laboratory is difficult without molecular techniques, and antifungal susceptibility test-ing is impossible to perform (3).

Invasive disease caused by Inonotus spp. (Phellinus tropicalis and P. undulatus) in humans has been described in 1 patient with diabetic nephropathy (3) and 6 patients with chronic granulomatous disease (4–10). Of note, 4 were breakthrough infections in patients receiving prophy-lactic itraconazole or posaconazole. Local infections had a favorable outcome; however, 1 patient with more extensive involvement had multiple relapses.

The infection in the patient we report mimicked other invasive mold infections in neutropenic patients with he-matologic malignancies. However, we observed fungal in-vasion in the skin after the percutaneous puncture for the pulmonary biopsy, which suggests fungal seeding from the lung source during sample collection.

The presence of fungal elements invading the tissues supported the diagnosis of IFD; nevertheless, we did not initially consider Inonotus spp. to be the causative agent of the IFD in this patient because it rarely causes disease in humans. The clinical significance of the isolation of sap-rophytic molds in nonsterile clinical samples is difficult to ascertain. However, detection of Inonotus spp. in the lung tissue sample taken months after the skin lesion biopsy led us to reassess its potential role as an etiologic agent. In ad-dition, the patient could have acquired the lung infection af-ter inhalation of spores, and selective pressure of previous antimicrobial drugs could have triggered the breakthrough invasive Inonotus spp. infection. Antifungal therapy was selected without specific recommendations and without an-tifungal susceptibility testing (because of the poor sporula-tion of the isolate). Immunosuppression was more profound and prolonged than in other cases of IFD caused by Inonotus spp. Both surgery and antifungal therapy were required, and immunologic recovery, along with a subacute course, were probably essential for the favorable outcome of this patient.

In conclusion, Inonotus spp. should be added to the list of potential causal agents of IFD in neutropenic hema-tological patients. Systematic use of panfungal PCR tar-geting the internal transcribed tracer regions coupled with sequencing in patients at a high risk for IFD may be helpful for diagnosing rare invasive fungal infections.

AcknowledgmentsWe thank Thomas O’Boyle for his help in the preparation of the manuscript and the members of the COMIC (Collaboration in Mycology) study group for their contribution to the work: Almudena Burillo, Amaya Bustinza, Ana Cabrero, Ana Fernández Cruz, Ana Pulido, Antonio Vena, Belén Padilla, Carlos Sánchez, Carmen Rodríguez, Diego Rincón, Eduardo Zarataín, Elena Zamora, Emilio Bouza, Fernando Anaya, Gabriela Rodríguez-Macías, Isabel Frías Soriano, Javier Alarcón, Javier García, Javier Hortal, Jesús Guinea, Jesús Torre, Jorge Gayoso, José Eugenio Guerrero, José María Tellado,

Figure. Pulmonary nodule and skin lesion in patient with invasive fungal disease caused by Inonotus spp., Madrid, Spain. A) Computed tomography of the lungs shows pulmonary nodule with halo sign in the left superior lobe, with peripheral distribution. B) Skin lesion at biopsy site 4 weeks after biopsy.

182 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 24, No. 1, January 2018

RESEARCH LETTERS

José Peral, Lola Vigil, Lorenzo Fernández Quero, Magdalena Salcedo, Mamen Martínez, Manuel Martínez Selles, Manuel Sánchez Luna, María Olmedo, María Sanjurjo, Maricela Valerio, Marina Machado, Marisa Alegre, Marisa Navarro, Marisa Rodríguez, Marta Grande, Mi Kwon, Miguel Martín, Nerea Álava, Paloma Gijón, Patricia Muñoz, Pilar Escribano, Rafael Bañares, Roberto Alonso, Teresa Hernández Sampelayo, and Verónica Parra.

This work was partially supported by grants PI14/00740, PI08/1463, PI11/00708, PI14/01731, MS15/00115, and RD12/0036/0061 and co-financed by Fondo de Investigación Sanitaria (FIS), Instituto de Salud Carlos III; Plan Nacional de I+D+I 2013–2016 and Fondo Europeo de Desarrollo Regional FEDER “Una manera de hacer Europa” support, along with grants from the Fundación LAIR, Asociación Madrileña de Hematología y Hemoterapia (AMHH), Asociación Española Contra el Cáncer (AECC), and Fundación Mutua Madrileña (FMM). FIS supported P.E. (CPI15/00115) and J.G. (CPII15/00006).

The subject of the case report signed an informed consent document for publication.

About the Author Dr. Fernández-Cruz is an internist and a consultant for hemato-oncological patients in the Clinical Microbiology and Infectious Diseases Department in Hospital Gregorio Marañón in Madrid. Dr. Kwon is a hematology specialist at the Stem Cell Transplant Unit in Hospital Gregorio Marañón in Madrid.

References 1. White TJ, Bruns T, Lee S, Taylor J. Amplification and direct

sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White, TJ, editors. PCR protocols: a guide to methods and applications. New York: Academic Press, 1990. p. 315–22.

2. Chowdhary A, Kathuria S, Agarwal K, Meis JF. Recognizing filamentous basidiomycetes as agents of human disease:

a review. Med Mycol. 2014;52:782–97. http://dx.doi.org/10.1093/mmy/myu047

3. Williamson D, Pandey S, Taylor S, Rogers K, Storey L, Marshall MR, et al. A case of infection caused by the basidiomycete Phellinus undulatus. J Med Microbiol. 2011;60:256–8. http://dx.doi.org/10.1099/jmm.0.025569-0

4. Davis CM, Noroski LM, Dishop MK, Sutton DA, Braverman RM, Paul ME, et al. Basidiomycetous fungal Inonotus tropicalis sacral osteomyelitis in X-linked chronic granulomatous disease. Pediatr Infect Dis J. 2007;26:655–6. http://dx.doi.org/10.1097/INF.0b013e3180616cd0

5. Ramesh M, Resnick E, Hui Y, Maglione PJ, Mehta H, Kattan J, et al. Phellinus tropicalis abscesses in a patient with chronic granulomatous disease. J Clin Immunol. 2014;34:130–3. http://dx.doi.org/10.1007/s10875-013-9967-1

6. Nguyen DK, Davis CM, Chinen J, Vallejo JG, Noroski LM. Basidiomycetous Inonotus (Phellinus) tropicalis osteomyelitis in pediatric and adult X-linked chronic granulomatous disease. J Allergy Clin Immunol. 2009;123:S13. http://dx.doi.org/10.1016/ j.jaci.2008.12.060

7. Sutton DA, Thompson EH, Rinaldi MG, Iwen PC, Nakasone KK, Jung HS, et al. Identification and first report of Inonotus (Phellinus) tropicalis as an etiologic agent in a patient with chronic granulomatous disease. J Clin Microbiol. 2005;43:982–7. http://dx.doi.org/10.1128/JCM.43.2.982-987.2005

8. Haidar G, Zerbe CS, Cheng M, Zelazny AM, Holland SM, Sheridan KR. Phellinus species: an emerging cause of refractory fungal infections in patients with X-linked chronic granulomatous disease. Mycoses. 2017;60:155–60. http://dx.doi.org/10.1111/myc.12573

9. Shigemura T, Nakazawa Y, Amano Y, Sudo A, Watanabe M, Kobayashi M, et al. Subcutaneous abscess due to the basidiomycete Phellinus mori in a patient with chronic granulomatous disease. Infec-tion. 2015;43:371–5. http://dx.doi.org/ 10.1007/s15010-015-0724-7

10. De Ravin SS, Parta M, Sutton DA, Wickes BL, Thompson EH, Wiederhold NP, et al. Paravertebral mushroom: identification of a novel species of Phellinus as a human pathogen in chronic granulomatous disease. J Clin Microbiol. 2014;52:2726–9. http://dx.doi.org/10.1128/JCM.00667-14

Address for correspondence: Ana Fernández-Cruz, Servicio de Microbiología Clínica y Enfermedades Infecciosas, Hospital General Universitario Gregorio Marañón, C/ Dr. Esquerdo, 46, 28007 Madrid, Spain; email: anafcruz999@gmail.com

Corrections

Vol. 21, No. 8An incorrect word in a sentence in Escherichia coli O157 Outbreaks in the United States, 2003–2012 (K.E. Heiman et al.) inadvertently changed the meaning. The sentence should have read, “The median annual number of outbreaks reported during 2008–2012 was higher than during 2003–2007 (45 vs. 33, p = 0.12) (Figure 1).” The article has been corrected online (https://wwwnc.cdc.gov/eid/article/21/8/14-1364_article).

Vol. 23, SupplementThe name of author Melanie E. King was incorrectly listed and several items in the text were unclear in Surveillance Training for Ebola Preparedness in Côte d’Ivoire, Guinea-Bissau, Senegal, and Mali (V.M. Cáceres et al.). The article has been corrected online (https://wwwnc.cdc.gov/eid/article/23/13/17-0299_article).

Page 1 of 5

Article DOI: http://dx.doi.org/10.3201/eid2401.171265

Inonotosis in Patient with Hematologic Malignancy

Technical Appendix

Technical Appendix Table. Invasive fungal infections caused by Basidiomycetes in neutropenic hematological patients*

Author Year Place Age, Sex Species

Diagnostic technique

Underlying disease Infection site Therapy Outcome Comments

Nenoff P (1) 1997 Germany 40F Coprinus spp (Hormographiella aspergillata)

Histology, culture

Relapsed ALL 5 y after HSCT

Lung AmB Fatal Coinfection with A. flavus Breakthrough while on fluconazole

Verweij PE (2) 1997 Netherlands 24M Hormographiella aspergillata

Histology, culture, PCR

ALL; HSCT; Relapse

Lung-multiple AmB Itraconazole

Fatal Postmortem diagnosis

Surmont I (3) 2002 Belgium 34F Hormographiella aspergillata

Culture, PCR NHL (lymphoblastic)

Lung abscess AmB Favorable

Buzina W (4) 2005 Austria 9F Irpex lacteus Histology, culture, PCR

ALL Lung abscesses

Voriconazole+AmB Favorable

Lagrou K (5) 2005 Belgium 34M Hormographiella aspergillata

Histology, culture, PCR

AML; HSCT Lung Caspofungin Fatal Postmortem diagnosis.

Abuali M (6) 2009 NY (USA) 14F Hormographiella aspergillata

Culture, PCR AML; HSCT Cutaneous (previous, palatal Mucor), probably disseminated (brain, lung cavitating lesions)

LAmB+caspofungin Fatal Mixed infection: first, palatal Rhizomucor variabilis Breakthrough while on Posaconazole and caspofungin

Conen A (7) 2010 Switzerland 41F Hormographiella aspergillata

Histology, blood culture, PCR

AML; double HSCT

Lung nodules, eye, brain

Voriconazole Posaconazole Caspofungin

Fatal GVHD Postmortem diagnosis.

63F Hormographiella aspergillata

Histology, culture, PCR

AML Lung nodules Voriconazole Posaconazole LAmB+surgery Voriconazole

Favorable, but death from underlying disease

55M Hormographiella aspergillata

Histology, culture, PCR

AML; HSCT (double cord)

Lung nodules LAmB+wedge resection Voriconazole

Fatal Breakthrough while on voriconazole (previous proven aspergillosis).

Salit RB (8) 2010 Bethesda, MD, USA

41F Volvariella volvacea

Histology, culture, PCR

HL; HSCT (cord)

Lung wedge infiltrates and CNS focal lesions

Voriconazole+LAmB

Fatal

Page 2 of 5

Author Year Place Age, Sex Species

Diagnostic technique

Underlying disease Infection site Therapy Outcome Comments

Pang KA (9) 2011 Strasbourg 25F Hormographiella aspergillata

Histology, culture

ALL Lung Voriconazole, LAmB

Favorable Breakthrough while on caspofungin)

Suárez F (10) 2011 Paris 23F Hormographiella aspergillata

Histology, culture, PCR

Acute biphenotypic leukemia

Lung

Voriconazole LAmB

Favorable Breakthrough while on caspofungin

27M Hormographiella aspergillata

Histology, culture, PCR

Adrenoleuko Dystrophy; HSCT (cord)

Lung, spleen Caspofungin LAmB

Fatal Postmortem diagnosis.

Bojic M (11) 2013 Austria 61F Hormographiella aspergillata

Histology, culture, PCR

AML; AlloHSCT Skin, lung nodules

Surgical debridement skin LAmB

Fatal

Toya T (12) 2013 Japan 23F Schizophyllum commune

Culture, PCR ALL, SCT (cord)

Maxillary and etmoidal sinusitis

LAmB Voriconazole LAmB

Favorable Breakthrough while on Itraconazole followed by micafungin

Heiblig M (13) 2015 France 19M Hormographiella aspergillata

Histology, culture, PCR

Mitochondrial cytopathy MDS-AML; HSCT

Sino-orbito-cerebral involvement

Surgical debridement+ LAmB+Voriconazole

Reduction of involvement, death from bacterial septic shock

Breakthrough while on Posaconazole (previous empirical caspofungin)

Corzo-León DE (14)

2015 Mexico 52F Hormographiella aspergillata

Culture, PCR AML; AlloHSCT Lung Voriconazole LAmB

Favorable, but died

Improvement, but died of unspecified cause

Nanno S (15) 2016 Japan 51M Hormographiella aspergillata

Histology, culture, PCR

SMD-EB; Cord HSCT

Small intestine, lung and brain

LAmB+caspo Fatal Postmortem diagnosis, although previously detected in transbronchial biopsy, but not identified Breakthrough while on itraconazole

Lim DS (16) 2017 Singapore 1 M Earliella scabrosa Histology, culture, PCR

Aplastic anemia Cutaneous emboli (multiple purpuric skin lesions), disseminated (pulmonary nodules

Not specified Fatal

Godet C (17) 2017 France 36M Hormographiella aspergillata

Histology, PCR

AML. Cord HSCT

Lung nodule Voriconazole Surgical resection LAmB+ Nebulized LAmB

Favorable

Fernández- Cruz A (this study)

2017 Spain 33M Inonotus spp Histology, culture, PCR

ALL. Lung nodule, skin

LAmB+vori Surgery Micafungin

Favorable Breakthrough while on micafungin

*ALL, acute lymphoblastic leukemia; AlloHSCT, allogenic hematopietic stem cell transplantation; AmB, amphotericin B deoxicolate; AML, acute myeloblastic leukemia; HL, Hodgkin lymphoma; HSTC, hematopoietic stem cell transplant; LAmB, liposomal amphotericin B; MDS, myelodysplastic syndrome.

Page 3 of 5

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