Case report
Eikenella corrodens and Porphyromonas asaccharolytica pleural empyema in a diabetic patient with obstructive sleep apnea syndrome on noninvasive ventilation
Empiema pleural por Eikenella corrodens e Porphyromonas saccharolytica numa doente diabética sob ventilação não invasiva por síndrome de apneia obstrutiva do sono
J. Caiano Gil
, R. Calisto, J. Amado, V. Barreto
Corresponding author
Serviço de Medicina Interna e Serviço de Pneumologia, Departamento de Medicina, Hospital Pedro Hispano, Unidade Local de Saúde de Matosinhos - E.P.E., Senhora da Hora, Portugal
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Values are expressed as mean<span class="elsevierStyleHsp" style=""></span>±<span class="elsevierStyleHsp" style=""></span>SEM. <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span><<span class="elsevierStyleHsp" style=""></span>0.001 significantly different between controls and whole COPD group. <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span><<span class="elsevierStyleHsp" style=""></span>0.01 significantly different between controls and non-smoker patients. <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span><<span class="elsevierStyleHsp" style=""></span>0.001 significantly different between controls and ex-smoker patients. There was no significant differences between non-smokers and ex-smokers COPD patients.</p>" ] ] ] "autores" => array:1 [ 0 => array:2 [ "autoresLista" => "C. Cristóvão, L. Cristóvão, F. Nogueira, M. Bicho" "autores" => array:4 [ 0 => array:2 [ "nombre" => "C." "apellidos" => "Cristóvão" ] 1 => array:2 [ "nombre" => "L." "apellidos" => "Cristóvão" ] 2 => array:2 [ "nombre" => "F." "apellidos" => "Nogueira" ] 3 => array:2 [ "nombre" => "M." 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"apellidos" => "Caiano Gil" "email" => array:1 [ 0 => "joao.gil@ulsm.min-saude.pt" ] "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">¿</span>" "identificador" => "cor0005" ] ] ] 1 => array:2 [ "nombre" => "R." "apellidos" => "Calisto" ] 2 => array:2 [ "nombre" => "J." "apellidos" => "Amado" ] 3 => array:2 [ "nombre" => "V." "apellidos" => "Barreto" ] ] "afiliaciones" => array:1 [ 0 => array:1 [ "entidad" => "Serviço de Medicina Interna e Serviço de Pneumologia, Departamento de Medicina, Hospital Pedro Hispano, Unidade Local de Saúde de Matosinhos - E.P.E., Senhora da Hora, Portugal" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "titulosAlternativos" => array:1 [ "pt" => array:1 [ "titulo" => "Empiema pleural por <span class="elsevierStyleItalic">Eikenella corrodens</span> e <span class="elsevierStyleItalic">Porphyromonas saccharolytica</span> numa doente diabética sob ventilação não invasiva por síndrome de apneia obstrutiva do sono" ] ] "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle">Case report</span><p id="par0005" class="elsevierStylePara elsevierViewall">A 69-year-old female, with a history of obesity, diabetes mellitus, arterial hypertension, dyslipidemia, New York Heart Association class II heart failure, atrial fibrillation and obstructive sleep apnea syndrome (OSAS) on noninvasive ventilation – nocturnal continuous positive airway pressure (CPAP) delivered through an oronasal mask – was evaluated for shortness of breath and dry cough which had developed over seven days. On admission, she was afebrile, with mean arterial pressure of 114<span class="elsevierStyleHsp" style=""></span>mmHg, pulse of 93<span class="elsevierStyleHsp" style=""></span>bpm and respiratory rate of 24/min, with hypoxemic respiratory insufficiency. Auscultation revealed diminished breath sounds and tactile fremitus over the left chest. Her teeth were in reasonable condition, with no suspicious lesions in the oropharynx. Physical examination was otherwise unremarkable. Laboratory markers of inflammation were elevated and chest roentgenogram demonstrated a large left pleural effusion. The patient underwent thoracentesis that revealed a purulent fluid collection. A chest tube was inserted, attached to water-seal drainage, and ceftriaxone plus metronidazole were empirically prescribed. A non-beta-lactamase-producing strain of <span class="elsevierStyleItalic">Eikenella corrodens</span> was isolated from the pleural fluid on the sixth day; antibiotics were then changed to penicillin-G benzathine. A strain of <span class="elsevierStyleItalic">Porphyromonas asaccharolytica</span> was subsequently isolated from the same sample. All blood and sputum cultures, as well as acid-fast bacillus and fungal cultures of pleural fluid, were negative.</p><p id="par0010" class="elsevierStylePara elsevierViewall">The patient remained afebrile over the following days, with no signs of respiratory distress by day 5, when the chest tube was removed. Evaluation with flexible bronchoscopy on the seventh day showed no endobronchial lesions and analysis of the bronchoalveolar lavage fluid was negative for microorganisms and cancer cells. Transthoracic echocardiography revealed pulmonary hypertension in correlation with OSAS.</p><p id="par0015" class="elsevierStylePara elsevierViewall">The patient was discharged from hospital on day 23, on respiratory kinesitherapy and amoxicillin-clavulanate for two additional weeks. Pre-discharge chest roentgenogram showed residual pleural effusion. The patient remained well during follow-up two years after hospitalization.</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle">Discussion</span><p id="par0020" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">E. corrodens</span> is a normal inhabitant of the oral cavity, gastrointestinal and genitourinary tracts, and it has been isolated from head and neck infections, as well as those associated with human bites.<a class="elsevierStyleCrossRefs" href="#bib0005"><span class="elsevierStyleSup">1,2</span></a> Other reported infections include endocarditis, osteomyelitis, parotitis, sinusitis, meningitis, cerebral abscess and chorioamnionitis.<a class="elsevierStyleCrossRefs" href="#bib0005"><span class="elsevierStyleSup">1–4</span></a></p><p id="par0025" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">E. corrodens</span> is a slowly growing, microaerophilic gram-negative bacillus. Its identification is based on the characteristics of colonies, which have typically pitting morphology; these are usually small with brighter center, irregular contours and hypochlorite odor. Other features include failure to produce catalase from glucose and capacity to reduce nitrates to nitrites.<a class="elsevierStyleCrossRefs" href="#bib0010"><span class="elsevierStyleSup">2,3</span></a> Since it requires several-day incubation on routine aerobic cultures, clinical suspicion is crucial.</p><p id="par0030" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">E. corrodens</span> is also recognizable for its intrinsic resistance to antibiotics with anaerobic activity such as clindamycin and metronidazole.<a class="elsevierStyleCrossRef" href="#bib0025"><span class="elsevierStyleSup">5</span></a> It is generally considered susceptible to penicillin-G and ampicillin, since most strains are non-beta-lactamase producers. Sensitivity to cephalosporins is variable.<a class="elsevierStyleCrossRefs" href="#bib0005"><span class="elsevierStyleSup">1–3</span></a></p><p id="par0035" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">P. asaccharolytica</span> is a strict anaerobic gram-negative bacillus commonly found in gastrointestinal and genitourinary tracts.<a class="elsevierStyleCrossRef" href="#bib0030"><span class="elsevierStyleSup">6</span></a> This bacterium develops into convex colonies, which are distinguishable due to their centripetal darkening appearance attributable to protoheme production. Although very few cases have been described, reported clinical presentations include soft-tissue infections, pleural empyema and appendicular abscess.</p><p id="par0040" class="elsevierStylePara elsevierViewall">Most of the patients with pleuropulmonary infection by <span class="elsevierStyleItalic">E. corrodens</span> present as parapneumonic effusion, pleural empyema, pneumonia and pulmonary abscess.<a class="elsevierStyleCrossRefs" href="#bib0010"><span class="elsevierStyleSup">2,5,6</span></a> Many cases are associated with mixed infections by microaerophilic streptococci, <span class="elsevierStyleItalic">Streptococcus viridans</span>, <span class="elsevierStyleItalic">Bacteroides fragilis</span>, <span class="elsevierStyleItalic">Prevotella melaninogenica</span> and <span class="elsevierStyleItalic">P. asaccharolytica</span>, most of which are normal inhabitants of the oral cavity.<a class="elsevierStyleCrossRefs" href="#bib0010"><span class="elsevierStyleSup">2,3,7</span></a> The possibility of synergistic mechanisms between <span class="elsevierStyleItalic">E. corrodens</span> and streptococcal strains has been brought up by some studies.<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a></p><p id="par0045" class="elsevierStylePara elsevierViewall">Pleuropulmonary infections by <span class="elsevierStyleItalic">E. corrodens</span> are rare, particularly in immunocompetent adults; fewer than fifteen cases have been described. Host factors such as immunosuppressive conditions, underlying lung disease and oropharyngeal and gastrointestinal aspiration predisposing factors play an important role in the pathogeny of this infection.<a class="elsevierStyleCrossRef" href="#bib0015"><span class="elsevierStyleSup">3</span></a> In fact, there is a close relationship between <span class="elsevierStyleItalic">E. corrodens</span> infection and neoplastic disease, alcoholism, diabetes mellitus, and chronic pulmonary and cerebrovascular disease, as well as poor dental hygiene and chronic glucocorticoid use.<a class="elsevierStyleCrossRefs" href="#bib0005"><span class="elsevierStyleSup">1–3,7</span></a></p><p id="par0050" class="elsevierStylePara elsevierViewall">Some of the studies suggest that OSAS can contribute to aspiration. Beal et al.<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">8</span></a> reported that these patients are at an increased risk for pharyngeal aspiration when compared to normal patients. Gleeson et al.<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a> performed quantitative measurements of aspirated material in a standard population of patients, and showed that aspiration was negligible in normal volunteers without symptoms of sleep apnea. The exact reason for this is not totally clear, although it may be due to factors generally found in patients with OSAS such as increased respiratory effort, higher body mass index and oropharyngeal anatomic abnormalities. In another study, Teramoto et al.<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">10</span></a> demonstrated that the swallowing reflex is significantly impaired in patient with OSAS; the authors suggest that sleep apnea can cause impaired function of receptors and afferent nerves to the respiratory and swallowing brain centers, which can further predispose to aspiration.</p><p id="par0055" class="elsevierStylePara elsevierViewall">Many patients with OSAS have symptoms suggestive of gastroesophageal reflux (GER), but there has not been a clear agreement on the precise association between these clinical entities. Due to the study design, Beal et al.<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">8</span></a> could not determine whether aspiration was consequence of true pharyngeal aspiration, or the result of aspiration of refluxed gastric content, although none of the patients had symptoms of GER. Likewise, Kerr et al.<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">11</span></a> failed to determine a temporal association between sleep apnea and reflux. In fact, most of the studies reporting an increased frequency of GER disease in patients with OSAS have not been controlled<a class="elsevierStyleCrossRefs" href="#bib0060"><span class="elsevierStyleSup">12–14</span></a> and it is not known whether the relationship is causative or due to conditions usually shared by OSAS and GER patients such as obesity and alcohol ingestion.</p><p id="par0060" class="elsevierStylePara elsevierViewall">Accordingly, there has been some uncertainty as to the role of CPAP in the predisposition for oropharyngeal aspiration. Even though Diaz et al.<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">15</span></a> showed that CPAP reduced GER in patients with both OSAS and GER disease (which was interpreted as evidence that OSAS caused GER), this result may be unrelated to the effect of noninvasive ventilation on OSAS, but instead a direct consequence of CPAP on intraesophageal and resting lower esophageal pressures; Kerr et al.<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">16</span></a> demonstrated that CPAP could decrease GER in patients without OSAS. On the contrary, Nishino et al.<a class="elsevierStyleCrossRef" href="#bib0085"><span class="elsevierStyleSup">17</span></a> demonstrated that CPAP exerts an inhibitory influence on swallowing reflex, which could facilitate oropharyngeal aspiration.</p><p id="par0065" class="elsevierStylePara elsevierViewall">Our report refers to a pleural empyema caused by co-infection with <span class="elsevierStyleItalic">E. corrodens</span> and <span class="elsevierStyleItalic">P. asaccharolytica</span>, in an immunocompetent diabetic patient with OSAS on CPAP, without symptoms of GER or other known predisposing factors for this infection. Extrapolating from this, it is our belief that noninvasive ventilation may have had an important role in the development of the disorder, either directly by facilitating oropharyngeal aspiration, or indirectly by inhibiting swallowing reflex, thus altering the normal breathing-swallowing pattern.</p><p id="par0070" class="elsevierStylePara elsevierViewall">Further randomized studies are required to better assess the role of noninvasive ventilation in the development of pleuropulmonary infections.</p></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle">Conclusion</span><p id="par0075" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">E. corrodens</span> should be considered as a possible causative agent when patients with presumed anaerobic infections fail to improve with standard treatment with clindamycin or metronidazole. Laboratory personnel and physicians should be aware of this in order to promote early diagnosis and prompt treatment.</p><p id="par0080" class="elsevierStylePara elsevierViewall">The susceptibility pattern of <span class="elsevierStyleItalic">E. corrodens</span> and other likely microorganisms must be considered when a therapeutic regimen is chosen. Simultaneous use of more than one antibiotic may be required.</p><p id="par0085" class="elsevierStylePara elsevierViewall">Despite not having been reported as an epidemiological context for the development of pleural empyema, it is our conviction that oropharyngeal aspiration of microorganisms facilitated by noninvasive ventilation may have been responsible for this infection.</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle">Ethical disclosures</span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle">Protection of human and animal subjects</span><p id="par0090" class="elsevierStylePara elsevierViewall">The authors declare that no experiments were performed on humans or animals for this study.</p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle">Confidentiality of data</span><p id="par0095" class="elsevierStylePara elsevierViewall">The authors declare that they have followed the protocols of their work center on the publication of patient data and that all the patients included in the study received sufficient information and gave their written informed consent to participate in the study.</p></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle">Right to privacy and informed consent</span><p id="par0100" class="elsevierStylePara elsevierViewall">The authors have obtained the written informed consent of the patients or subjects mentioned in the article. The corresponding author is in possession of this document.</p></span></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle">Conflicts of interest</span><p id="par0105" class="elsevierStylePara elsevierViewall">The authors have no conflicts of interest to declare.</p></span></span>" "textoCompletoSecciones" => array:1 [ "secciones" => array:10 [ 0 => array:2 [ "identificador" => "xres175794" "titulo" => "Abstract" ] 1 => array:2 [ "identificador" => "xpalclavsec164129" "titulo" => "Keywords" ] 2 => array:2 [ "identificador" => "xres175795" "titulo" => "Resumo" ] 3 => array:2 [ "identificador" => "xpalclavsec164128" "titulo" => "Palavras-chave" ] 4 => array:2 [ "identificador" => "sec0005" "titulo" => "Case report" ] 5 => array:2 [ "identificador" => "sec0010" "titulo" => "Discussion" ] 6 => array:2 [ "identificador" => "sec0015" "titulo" => "Conclusion" ] 7 => array:3 [ "identificador" => "sec0020" "titulo" => "Ethical disclosures" "secciones" => array:3 [ 0 => array:2 [ "identificador" => "sec0025" "titulo" => "Protection of human and animal subjects" ] 1 => array:2 [ "identificador" => "sec0030" "titulo" => "Confidentiality of data" ] 2 => array:2 [ "identificador" => "sec0035" "titulo" => "Right to privacy and informed consent" ] ] ] 8 => array:2 [ "identificador" => "sec0040" "titulo" => "Conflicts of interest" ] 9 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2012-02-29" "fechaAceptado" => "2012-10-24" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec164129" "palabras" => array:5 [ 0 => "Pleural empyema" 1 => "Continuous positive airway pressure" 2 => "Obstructive sleep apnea" 3 => "<span class="elsevierStyleItalic">Eikenella corrodens</span>" 4 => "<span class="elsevierStyleItalic">Porphyromonas</span>" ] ] ] "pt" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palavras-chave" "identificador" => "xpalclavsec164128" "palabras" => array:5 [ 0 => "Empiema pleural" 1 => "Ventilação não invasiva" 2 => "Apneia obstrutiva do sono" 3 => "<span class="elsevierStyleItalic">Eikenella corrodens</span>" 4 => "<span class="elsevierStyleItalic">Porphyromonas</span>" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "en" => array:2 [ "titulo" => "Abstract" "resumen" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall"><span class="elsevierStyleItalic">Eikenella corrodens</span> is a normal inhabitant of the human oral cavity and gastrointestinal and genitourinary tracts.</p><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Pleuropulmonary infections by this microorganism are uncommon. Pulmonary aspiration is a chief predisposing condition. Although the outcome is usually favorable, its distinctive antibiotic sensitivity pattern makes bacterial identification an important feature in dealing with this infection.</p><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">The authors report a case of pleural empyema caused by co-infection with <span class="elsevierStyleItalic">E. corrodens</span> and <span class="elsevierStyleItalic">Porphyromonas asaccharolytica</span>, in an immunocompetent diabetic patient with obstructive sleep apnea syndrome, followed by a discussion on the role of noninvasive ventilation in the development of this infection.</p>" ] "pt" => array:2 [ "titulo" => "Resumo" "resumen" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">A <span class="elsevierStyleItalic">Eikenella corrodens</span> é um microrganismo habitualmente encontrado na mucosa oral, trato gastrointestinal e trato geniturinário de humanos.</p><p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">Os casos de infeção pleuropulmonar por este agente são raros em indivíduos imunocompetentes, sendo a aspiração um fator importante na sua patogenia. Apesar de apresentar geralmente um prognóstico favorável, o reconhecimento desta infeção é essencial dado o perfil de sensibilidades característico.</p><p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">Os autores apresentam um caso de empiema pleural por <span class="elsevierStyleItalic">E. corrodens</span>, em coinfeção com <span class="elsevierStyleItalic">Porphyromonas asaccharolytica</span>, numa doente diabética imunocompetente com síndrome de apneia obstrutiva do sono, discutindo o papel da ventilação não invasiva como fator predisponente da referida infeção.</p>" ] ] "NotaPie" => array:1 [ 0 => array:2 [ "etiqueta" => "☆" "nota" => "<p class="elsevierStyleNotepara">Please cite this article as: Caiano Gil JC, et al. Empiema pleural por <span class="elsevierStyleItalic">Eikenella corrodens</span> e <span class="elsevierStyleItalic">Porphyromonas saccharolytica</span> numa doente diabética sob ventilação não invasiva por síndrome de apneia obstrutiva do sono. Rev Port Pneumol. 2013. <span class="elsevierStyleInterRef" href="doi:10.1016/j.rppneu.2012.10.004">http://dx.doi.org/10.1016/j.rppneu.2012.10.004</span>.</p>" ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0005" "bibliografiaReferencia" => array:17 [ 0 => array:3 [ "identificador" => "bib0005" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Pleuropulmonary infection with chest wall infiltration by <span class="elsevierStyleItalic">Eikenella corrodens</span>" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:3 [ 0 => "J.W. Killen" 1 => "G.L. Swift" 2 => "R.J. 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