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Empyema necessitatis revisited

European Journal of Dermatology. Volume 20, Numéro 1, 115-9, January-February 2010, Clinical report

DOI : 10.1684/ejd.2010.0809

Summary

Auteur(s) : Mar Llamas-Velasco, Inmaculada Domínguez, Enrique Ovejero, Silvia Pérez-Gala, Amaro García-Diez , Department of Dermatology, Hospital Universitario de la Princesa, C/ Diego de León 62, CP 28006, Madrid, Spain, Department of Thoracic Surgery, Hospital Universitario de la Princesa, C/ Diego de León 62, CP 28006, Madrid, Spain.

Illustrations

ARTICLE

Auteur(s) : Mar Llamas-Velasco¹, Inmaculada Domínguez¹, Enrique Ovejero², Silvia Pérez-Gala¹, Amaro García-Diez¹

¹Department of Dermatology, Hospital Universitario de la Princesa, C/ Diego de León 62, CP 28006, Madrid, Spain
²Department of Thoracic Surgery, Hospital Universitario de la Princesa, C/ Diego de León 62, CP 28006, Madrid, Spain

accepté le 26 Août 2009

Empyema necessitatis (EN) is defined as the extension of purulent pleural liquid through adjacent tissues to form an abscess on the thoracic wall. It was first described in 1640 by Baillon [1] and subsequently by Laennec [2] in 1890. Cutaneous manifestations of EN are unspecific. The most important one is the presence of a subacute mass on the costal wall. Thus, dermatologists should be aware of this disease because sometimes they are the first physician to attend these patients.

Case report

A 32-year-old woman went to her primary care physician with a one-month history of non-productive coughing and an enlarging, painful mass on the anterior right thoracic wall. There were no symptoms of fever, dyspnea, thoracic pain or any other. She was diagnosed with nervous anorexia eight years ago and also had a laxative abuse history. The patient was sent to hospital with an altered chest X-ray showing a shadow on the right lung, along with ipsilateral pleural effusion. Physical examination showed moderate-illness with generalised wasting of muscle and subcutaneous fat. She was found to have a pink erythematous, warm, tender mass of 7 centimetres in diameter, between the 5^th and 10^th ribs, with moderate oedema and a fluctuant centre (figure 1). Poor oral hygiene with several caries was observed. Laboratory values revealed a white blood-cell count of 10,240/mm³ with 91.5% neutrophils. Hemoglobin was 11.1 g/dL and platelets were 368,000/mm³. Kidney, liver and thyroid tests were all within normal limits. Several serologies, (Chlamydia, Q-fever, Adenovirus, Mycoplasma, Legionella, Respiratory Syncytial Virus and HIV), were negative. She had a compensated metabolic alkalosis that was thought to be a secondary effect of the laxative abuse. Purified protein derivative (PPD) for a tuberculous skin test was non-reactive. Intravenous cotrimoxazole (400 mg/12 h) and intravenous imipenem (500 mg/8 h) were prescribed at this moment as empiric therapy for fifteen days. A computed tomography scan of the chest revealed a small-sized right pleural effusion and pulmonary infiltration without demonstration of a strange endobronchial body (figure 2). It also revealed the presence of a continuity solution between the pleural empyema and the adjacent subcutaneous tissue. Because of these findings, a fine-needle aspiration biopsy (FNAB) of the mass was performed for microbiological and cytological study. Afterwards, the patient was sent to Thoracic Surgery for drainage of purulent pleural collections. Cytological studies were not useful. The microbiological studies revealed Gram-positive ramified bacillus. Culture results were positive for Actinomyces gerencseriae, Klebsiella corrodens and negative-coagulase Streptococci. Fungal and mycobacterial smears and cultures were negative. Thus, Actinomyces gerencseriae was thought to be the etiological agent of her disease, and she was diagnosed with empyema necessitatis secondary to thoracic actinomycosis (TA). Specific antibiotic treatment with intravenous amoxicillin plus clavulanic acid (2 g/8 h doses, for fifteen days), and oral amoxicillin plus clavulanic acid (875 mg/8 h, for two and a half months) were used, resulting in lung improvement and important clinical progress.

Discussion

EN is most commonly reported in adults. We could not find prevalence and incidence data about EN, although global incidence is thought to be decreasing. There are non-infectious causes of EN such as carcinoma, mesothelioma and lymphoma [3, 4], but infectious ones are the most important. Tuberculosis, actinomycosis, and pyogenic bacteria are the most commonly reported, but fungi are also found [5-7]. This rare complication of pleural space infection occurs mostly due to inadequate or late treatment of such infections. Actinomyces is a gram-positive, non-spore forming, predominantly anaerobic prokaryotic bacteria. Most of EN caused by actinomycetes are produced by A. israelii but A. odontolyticus has also been described as a causal agent [8]. A. gerencseriae, the etiological bacteria in our case, is considered the serovariety 2 of A. Israelii [9]. Recently, Freeman et al. reviewed 26 cases of EN in the English medical literature from 1966 to 2004 [5]. They found that 50% were the result of M. tuberculosis and 24% were due to Actinomyces infection. A computerized search for reports in the English and Spanish literature up to 2004 was carried out using Pubmed and Medline and a summary of those cases of EN, excluding non-infectious causes, can be seen in table 1. We found 18 articles, including ours, describing 20 cases (table 1 [10-17]). Only one article included several cases [7]. Most of the patients included (n = 15, 75%) were men. Patients were aged from 3 months-old to 88-year-old. Mycobacterium tuberculosis was less frequent than in previous reports (n = 7, 35%) but it is still necessary to rule out this etiology. Instead, thoracic actinomycosis seems to be slightly more relevant nowadays (n = 5, 25%). The remaining cases (n = 8, 40%) were the result of infections by S. aureus, E. coli and Aspergillus spp. Therefore, there has been a change in the causal agents. It is remarkable that the etiological agent is methicillin resistant Staphylococcus aureus (MRSA) in two cases, both of them in USA reports [18, 19]. This fact can be a sign of the increasing importance of this pathogen in several countries, especially in the USA.

In empyema development, pleural fluid passes through three pathogenic stages of increasing host defence activity and bacterial invasion [20, 21]. In the first one, which is also called the exudative stage, bacterial infection and inflammation release cytokines (IL-8, TNF-α) that increase tissue and capillary permeability. In the second one, called the fibrinopurulent stage, pleural fluid is invaded by bacterium. In the last stage there is a fibroblastic proliferation in the inner surface of the pleura. This whole process is known to be driven by mediators such as transforming growth factor (TGF-β) and platelet derived growth-factor (PDGF) [22].

Clinically, patients mostly had an enlarging, painful, slightly erythematous, moderate demarcated mass, in the chest wall (n = 8, 40%), cough (n = 6, 30%), pleuritic-type chest pain (n = 4, 20%) and dyspnea (n = 2, 10%). Although a few cases with mastitis-like debut have been described [6], none of these reported patients presented it. Extension tends to occur along the pathway of least resistance and in this manner, EN usually affects between the second and sixth intercostal spaces [23] as in our case. Three cases (cases 5, 6 and ours) had poor teeth care [24, 25] but no one, apart from our patient, had anorexia. Symptoms for TA are unspecific. Constitutional symptoms usually begin between two months and six years prior to disease characterization, which has a medium delay of six months [26, 27]. Thus, delayed diagnosis or misdiagnosis such as tuberculosis, lung abscess or lung tumour is common and inadequate surgical approaches can be taken [28]. Sometimes cutaneous signs such as chest wall swelling, appearance of an abscess or thoracic skin fistulation are present from the beginning [29] and we can obtain an earlier diagnosis. We find risk factors such as chronic alcoholism, caquexia, EPOC, TBC, poor teeth health, bronchiectasias, etc., in 50% of patients with TA. There are also several cases associated with intrabronchial bodies [30], tumours or even concomitant tuberculous disease, but there is no higher incidence in HIV patients [29]. The finding of a lithic lesion on the ribs in X-rays is highly suspicious but infrequent [31].

EN diagnosis requires demonstration of continuity between the purulent pleural fluid and the thoracic wall abscess, so we usually need TC to diagnose. FNAB (fine-needle aspiration biopsy) is a very useful diagnosis method in EN [7, 32]. This technique allows us to make a cytological diagnosis as well as to obtain material for culture. EN has rarely been reported to extend to abdominal spaces or to the head and neck [33-35] or in the reverse pathway [24]. On the other hand, actinomycosis diagnosis requires the demonstration, by culture, of the etiological agent but sputum culture is not useful because Actinomyces genre is a common oropharynx inhabitant [31]. Blood culture is usually negative, but there are several cases with septic dissemination [36]. Various bacteria have all been isolated, with Actinomyces spp in some combinations [37]. In our case, we found Klebsiella corrodens and negative-coagulase Streptococci, both previously described. They are thought to enhance the pathogenicity of Actinomyces by creating an anaerobic environment.

In the pre-antibiotic era, mortality was globally 66% [27]. The mortality rate is nowadays less than 5% in infectious cases because most of them respond promptly to antibiotics. In contrast, neoplastic EN portends a poor prognosis with limited survival [7]. EN mortality mechanisms are all interconnected and can co-exist. They can be grouped as follows: 1) respiratory insufficiency, with diminished lung or chest wall elasticity and ventilation-perfusion matching alterations, because of intra-alveolar filling; 2) cardiac failure, secondary to pericarditis or hypoxemia; 3) mediastinitis, which alters proper cardiac function and can compress airways; 4) haematogenous dissemination, that can produce hemodynamic instability and sepsis, with multiple-organ failure; 5) acute renal insufficiency due to dehydration and low-output cardiac failure; and 6) iatrogenic causes such as incorrect chest-tube placement technique or haemorrhagic problems due to the use of intrapleural fibrinolytics. All these facts can be aggravated because of previous diseases, and they are much more likely to happen in older patients. EN treatment includes a double approach: medical and surgical. Empirical antibiotic treatment (highly recommended because decreasing morbidity and mortality rates) using a second-generation cephalosporin or aminopenicillin with a β-lactamase inhibitor plus anaerobic coverage or, for sensitive patients, a combination of ciprofloxacin plus clindamycin, covers all likely pathogens. There exist no direct data on how long to treat empyema, but most authors advise one week with intravenous treatment followed by 1-3 weeks of oral treatment. For actinomyces there are some articles suggesting that shorter treatments are at least equally effective [38] and recommending using antibiotics whose activity fights concomitant bacteria, instead of penicillin [39]. In our case, using this new treatment approach was very successful. There is an expert consensus that pus within the pleural space requires prompt tube drainage. Optimal timing of drainage is also a controversial theme. In any case, clinical response is the most important factor. There are also several surgical techniques that can be used here, such as drainage with thoracotomy, decortication and wide surgical drainage. New techniques, such as VATS (Video-Assisted Thoracic surgery) [40], will probably be used in the near future for this disease.
Table 1 Clinical, etiologic agents and received treatments summary

Reference	Age/Genre	Predisposing	Clinic	Etiology	Diagnosis	Treatment	Surgery
Porcel JM [7]	88/M	Old pleural TB	Dyspnea+mass	MT	FNBA	None	Chest tube
Chaiyasate K [10]	18/M	None	Costal mass	MT	Culture	Anti TB	Unknown
Soto-Hurtado E [6]	65/M	Alcoholic. Smoker. Previous TB	Dyspnea+pain+constitutional syndrome	Assp	Biopsy	Anfotericine	Thoracotomy+costal resection
Pinarli FG [11]	9/F	None	Pleuritic pain+ anorexia	Asp	Biopsy	Penicillin	Unknown
Huits RM [25]	43/M	Caries, undernourishment	Cough+pleuritic pain	Asp	FNBA	Unknown	Unknown
De Wit M [24]	44/M	Caries, alcohol, colonic adenoma	Costal mass+non productive cough	EC+SA	Culture	Wide spectrum antibiotics	Thoraco-centesis
Moore FO [12]	3m/F	None	Fever + rash	MRSA	Culture	Vancomycin+linezolid	Decortication +chest tube
Fatureto M [13]	26/M	None	Costal mass	Asp	Biopsy	Ciprofloxacin	None
Kono SA [26]	52/M	Alcoholic, marihuana smoking	Cough+dyspnea+fever	Asp	UK	Piperacillin-tazobactam	VATS
Reyes CV [4]	68/M;79/M;29/M 47/M	Unknown	Unknown	MT AI	FNBA	Anti TB Penicillin	Pleurodesis
Tonna I [14]	53/M	None	Myalgia+mass	SA	Culture	Intravenous antibiotics	Surgical debridement
Lee JK [15]	12/F	None	Cough+constitutional syndrome	ASP	Culture	Penicillin+ doxycycline	None
Tezel C [16]	68/F	None	Costal mass. Pleural thickenning	UK	Culture	Anti TB	Chest tube + thoracostomy
Sennent C, et al. [18]	24/M	None	Fever+cough+abdominal wall mass	MT	PCR	Anti TB	Chest tube
García-Gasalla M, et al. [19]	50/M	Old pleural TB	Thoracic ulceration	MT	Culture	Anti TB	None
Mizell KN [17]	59/M	None	Costal mass+pain	MRSA	Culture	Vancomycin+ciprofloxacin+TMT-SMX	Wedge resection of upper left lobe
Llamas M, et al.	32/F	Caries, undernourishment	Costal mass+non productive cough	AG	FNBA	Amoxicyllin+clavulanic	Chest tube

Conclusion

From a dermatological point of view, we must remember that any enlarging and painful subacute thoracic mass with fluctuation should be considered as an EN suspicious lesion. When we suspect it, the diagnostic approach must include a chest X-ray, to rule out lung affectation. In that case, TC is useful to demonstrate the presence of continuity between empyema and the subcutaneous abscess, and, so, to consolidate the diagnosis. In any case, timely pleural fluid analysis, when we find pleural effusion, can prevent this complication [30]. Thus, FNAB should be considered as a first approach to diagnosis because of the possibility of reaching an etiologic diagnostic, which lets us choosing the most appropriate therapy [41]. Early diagnosis and treatment reduces complications, and that’s the reason why dermatologists should be aware of this entity, to promote an earlier recognition and treatment.

Acknowledgements

Financial support: none. Conflict of interest: none.

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