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Aseptic sampling of pleural fluids was performed by thoracentesis or endothoracic drainage&#59; the samples underwent microbiological processing including culture&#44; identification using biochemical galleries and mass spectrometry&#44; direct observation by electron microscopy in the case of filamentous fungi&#44; followed by antifungal sensitivity testing using commercial Sensititre<span class="elsevierStyleSup">&#174;</span> Yeast One panels &#40;Thermo Fisher Scientific&#44; UK&#41;&#46;</p><p id="par0015" class="elsevierStylePara elsevierViewall">Fungal isolates were obtained from 9 patients &#40;8 males with a median age of 65<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>10 years&#41; characterized by nonspecific symptoms &#40;respiratory failure and dyspnea&#41;&#44; a 5-week mortality rate of 50&#37;&#44; and long hospital stays &#40;47<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>24 days&#41;&#46; Seven yeasts &#40;2 non-<span class="elsevierStyleItalic">Candida albicans</span> species&#41; and 3 <span class="elsevierStyleItalic">Aspergillus fumigatus</span> &#40;<span class="elsevierStyleItalic">A&#46; fumigatus</span>&#41; were isolated&#44; and no resistance was documented&#46; The total rate of antifungal therapy was 55&#37;&#44; the most common being azole derivatives&#44; and the least common&#44; caspofungin or inhaled liposomal amphotericin B&#46; None of the patients had received antifungal prophylaxis prior to the study episode&#46; <a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a> lists the risk factors for fungal infection identified in each patient and the species isolated in each case&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0020" class="elsevierStylePara elsevierViewall">As in other series with larger numbers of cases&#44;<a class="elsevierStyleCrossRefs" href="#bib0030"><span class="elsevierStyleSup">1&#44;2</span></a> the causative agents associated with fungal empyema that presented a slightly lower mortality rate in our series were <span class="elsevierStyleItalic">Candida</span> spp&#46; followed by <span class="elsevierStyleItalic">A&#46; fumigatus</span>&#46; All patients except one had 1 or more previous immunodeficiency diseases according to the accepted classifications<a class="elsevierStyleCrossRef" href="#bib0030"><span class="elsevierStyleSup">1</span></a>&#58; cancer&#44; diabetes mellitus&#44; long-term steroid treatment&#44; hepatic cirrhosis&#44; solid organ transplant&#44; alcoholism&#44; human immunodeficiency virus infection&#44; or surgery in the 4 weeks prior to isolation of the fungus&#46;</p><p id="par0025" class="elsevierStylePara elsevierViewall">Clinical suspicion&#44; chest drainage&#44; early introduction of antifungal agents&#44; and long-term treatment are associated with a reduced mortality rate&#46;<a class="elsevierStyleCrossRef" href="#bib0030"><span class="elsevierStyleSup">1</span></a> However&#44; the treatment of fungal empyema is not protocolized&#44; and combinations that include several drugs can be used &#40;amphotericin B and voriconazole&#44; echinocandins&#41; due the variable penetration of systemically administered antifungals into the pleural cavity&#46;<a class="elsevierStyleCrossRefs" href="#bib0040"><span class="elsevierStyleSup">3&#44;4</span></a> The percentage of patients treated with broad-spectrum antibiotic therapy was higher than that of patients treated with antifungal drugs&#44; despite determination of the etiology&#44; and no subsequent antibiotic de-escalation was performed&#46;</p><p id="par0030" class="elsevierStylePara elsevierViewall">The lack of specific antifungal treatment may be due to clinicians&#8217; failure to consider fungi as true pathogens&#46; Each case must be studied on an individual basis and the role of each causative agent must be evaluated in order to optimize treatment&#46; This includes the need for pharmacological prophylaxis in patients at high risk of developing fungal empyema &#40;hemodialysis&#44; post-surgical re-exploration&#44; environmental colonization by <span class="elsevierStyleItalic">Aspergillus</span>&#44; or documented cytomegalovirus infection&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">5</span></a></p><p id="par0035" class="elsevierStylePara elsevierViewall">The seriousness of this entity and its devastating consequences in patients should not be underestimated&#46;</p></span>"
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                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Candida krusei</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Solid tumor &#40;pleural mesothelioma&#41;<span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span>chemotherapy&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Candida parapsilosis</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">3&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">No documented risk factors&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Candida albicans</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">4&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Previous surgery &#40;esophagectomy&#41;<span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span>alcoholism<span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span>solid tumor &#40;esophageal epidermoid carcinoma&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Candida albicans</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">5&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Previous surgery &#40;total gastrectomy&#41;<span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span>solid tumor &#40;gastric&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Candida albicans</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">6&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Previous surgery &#40;bariatric&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Candida albicans</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">7&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Heart transplant<span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span>diabetes mellitus 2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Aspergillus fumigatus</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">8&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Hematological cancer &#40;myelodysplastic syndrome&#41;<span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span>diabetes mellitus 2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Aspergillus fumigatus</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">9&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Previous surgery &#40;lateral thoracotomy&#41;<span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span>alcoholism<span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span>chronic obstructive pulmonary disease&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Aspergillus fumigatus</span>&nbsp;\t\t\t\t\t\t\n
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Journal Information
Vol. 53. Issue 11.
Pages 641-642 (November 2017)
Vol. 53. Issue 11.
Pages 641-642 (November 2017)
Scientific Letter
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Fungal Empyema: An Uncommon Entity With High Mortality
Empiema fúngico: una entidad infrecuente con elevada mortalidad
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11044
Blanca de Vega Sáncheza,
Corresponding author
blancadevegasanchez@gmail.com

Corresponding author.
, Irene López Ramosb, Raúl Ortiz de Lejarazub, Carlos Disdier Vicentea,c
a Servicio de Neumología, Hospital Clínico Universitario de Valladolid, Valladolid, Spain
b Servicio de Microbiología, Hospital Clínico Universitario de Valladolid, Valladolid, Spain
c CIBERES (Centro de Investigación en Red Enfermedades Respiratorias), Valladolid, Spain
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Tables (1)
Table 1. Risk factors in patients with fungal pleural effusion and species isolated.
Full Text
To the Editor,

Fungal infections have increased in the last few decades as a result of the widespread use of broad-spectrum antibiotics and the growing number of immunocompromised patients in our clinics, which have led to changes in the saprophytic microorganisms usually isolated. Even so, fungal empyemas are still rare entities, with a mortality rate of over 70%. The most common ways for fungi to reach the pleural cavity are via lung infections, complications of pre-existing chronic empyemas, esophageal-bronchial fistulas, or repeated thoracentesis,1 so in patients with risk factors, the possibility of a fungal etiology must be taken into account.

We report a retrospective analysis of exclusively fungal pleural effusions diagnosed in our hospital between 2005 and 2016. Aseptic sampling of pleural fluids was performed by thoracentesis or endothoracic drainage; the samples underwent microbiological processing including culture, identification using biochemical galleries and mass spectrometry, direct observation by electron microscopy in the case of filamentous fungi, followed by antifungal sensitivity testing using commercial Sensititre® Yeast One panels (Thermo Fisher Scientific, UK).

Fungal isolates were obtained from 9 patients (8 males with a median age of 65±10 years) characterized by nonspecific symptoms (respiratory failure and dyspnea), a 5-week mortality rate of 50%, and long hospital stays (47±24 days). Seven yeasts (2 non-Candida albicans species) and 3 Aspergillus fumigatus (A. fumigatus) were isolated, and no resistance was documented. The total rate of antifungal therapy was 55%, the most common being azole derivatives, and the least common, caspofungin or inhaled liposomal amphotericin B. None of the patients had received antifungal prophylaxis prior to the study episode. Table 1 lists the risk factors for fungal infection identified in each patient and the species isolated in each case.

Table 1.

Risk factors in patients with fungal pleural effusion and species isolated.

Patient number  Identified risk factors  Isolated species 
Alcoholism+cirrhosis  Candida krusei 
Solid tumor (pleural mesothelioma)+chemotherapy  Candida parapsilosis 
No documented risk factors  Candida albicans 
Previous surgery (esophagectomy)+alcoholism+solid tumor (esophageal epidermoid carcinoma)  Candida albicans 
Previous surgery (total gastrectomy)+solid tumor (gastric)  Candida albicans 
Previous surgery (bariatric)  Candida albicans 
Heart transplant+diabetes mellitus 2  Aspergillus fumigatus 
Hematological cancer (myelodysplastic syndrome)+diabetes mellitus 2  Aspergillus fumigatus 
Previous surgery (lateral thoracotomy)+alcoholism+chronic obstructive pulmonary disease  Aspergillus fumigatus 

As in other series with larger numbers of cases,1,2 the causative agents associated with fungal empyema that presented a slightly lower mortality rate in our series were Candida spp. followed by A. fumigatus. All patients except one had 1 or more previous immunodeficiency diseases according to the accepted classifications1: cancer, diabetes mellitus, long-term steroid treatment, hepatic cirrhosis, solid organ transplant, alcoholism, human immunodeficiency virus infection, or surgery in the 4 weeks prior to isolation of the fungus.

Clinical suspicion, chest drainage, early introduction of antifungal agents, and long-term treatment are associated with a reduced mortality rate.1 However, the treatment of fungal empyema is not protocolized, and combinations that include several drugs can be used (amphotericin B and voriconazole, echinocandins) due the variable penetration of systemically administered antifungals into the pleural cavity.3,4 The percentage of patients treated with broad-spectrum antibiotic therapy was higher than that of patients treated with antifungal drugs, despite determination of the etiology, and no subsequent antibiotic de-escalation was performed.

The lack of specific antifungal treatment may be due to clinicians’ failure to consider fungi as true pathogens. Each case must be studied on an individual basis and the role of each causative agent must be evaluated in order to optimize treatment. This includes the need for pharmacological prophylaxis in patients at high risk of developing fungal empyema (hemodialysis, post-surgical re-exploration, environmental colonization by Aspergillus, or documented cytomegalovirus infection).5

The seriousness of this entity and its devastating consequences in patients should not be underestimated.

References
[1]
S.C. Ko, K.Y. Chen, P.R. Hsueh, K.T. Luh, P.C. Yang.
Fungal empyema thoracis: an emerging clinical entity.
Chest, 117 (2000), pp. 1672-1678
[2]
K.H. Lin, Y.M. Liu, P.C. Lin, C.M. Ho, C.H. Chou, J.H. Wang, et al.
Report of a 63-case series of Candida empyema thoracis: 9-year experience of two medical centers in central Taiwan.
J Microbiol Immunol Infect, 47 (2014), pp. 36-41
[3]
T. Matsuda, Y. Koreeda, H. Mataki, T. Taira, S. Noma, I. Higashimoto.
A case of Aspergillus empyema successfully treated with combination therapy of voriconazole and micafungin: excellent penetration of voriconazole and micafungin into pleural fluid.
Inter Med, 49 (2010), pp. 1163-1169
[4]
T.J. Walsh, E.J. Anaissie, D.W. Denning, R. Herbrecht, D.P. Kontoyannis, K.A. Marr, et al.
Treatment of aspergillosis: clinical practice guidelines of the Infectious Diseases Society of America.
Clin Infect Dis, 46 (2008), pp. 327-360
[5]
R. Zaragoza, J.M. Aguado, R. Ferrer, A.H. Rodríguez, E. Maseda, P. Llinares, et al.
EPICO 3.0. Antifungal prophylaxis in solid organ transplant recipients.
Rev Iberoam Micol, 33 (2016), pp. 187-195

Please cite this article as: de Vega Sánchez B, López Ramos I, Ortiz de Lejarazu R, Disdier Vicente C. Empiema fúngico: una entidad infrecuente con elevada mortalidad. Arch Bronconeumol. 2017;53:641–642.

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