Abstract
An eighty-three-year-old man suffered from cough, right chest pain, and progressive dyspnea for sixteen days. He had hypoxemia, high white blood cells and C-reactive protein, and moderate right-sided pleural effusion on radiographic imaging. A pleural fluid examination revealed exudate. He was diagnosed with pleural infection and treated with intravenous ampicillin/sulbactam. On the second day of hospitalization, the treatment was changed to levofloxacin and clindamycin due to drug eruption. He improved gradually and was prescribed only oral levofloxacin on the eighteenth day of hospitalization. However, improvements in inflammation and imaging findings were poor. Actinomyces meyeri resistant to fluoroquinolones was cultured from a pleural effusion sample on the twenty-sixth day of hospitalization. The treatment was changed to oral clindamycin, and his medical condition subsequently improved. We reviewed twenty-eight patients with Actinomyces pleural infection and thirty-eight patients with other pleural infection phenotypes from our hospital and published case reports. Actinomyces pleural infection is a long-term process and results in a large amount of pleural effusion compared to other pleural infection phenotypes. These results might be related to the fact that Actinomyces is a slow-growing organism.
Keywords: Actinomyces meyeri, Pleural fluid, Penicillin allergy, Pleural infection, Actinomycosis
Abbreviations: COPD, chronic obstructive pulmonary disease; HOT, home oxygen therapy; DM, diabetes mellitus; CRP, C-reactive protein; CT, computed tomography; LDH, lactate dehydrogenase
1. Introduction
Actinomyces is an anaerobic gram-positive bacterium, commonly associated with cervicofacial, abdominopelvic, and thoracic granulomatous infection [1, 2], which can be chronic, and disseminated cases have been reported [2, 3]. Actinomyces meyeri usually involves the lungs and is a rare pathogen of pleural infection, including empyema and parapneumonic effusion. Actinomyces pleural infection is treated with long-term antibiotic therapy, such as penicillin, and chest drainage [4], [5], [6] This is a case report of Actinomyces meyeri pleural infection that was difficult to treat due to the delayed culture of A. meyeri and a penicillin allergy. Furthermore, we reviewed the characteristics of twenty-eight patients with Actinomyces pleural infection through comparisons to those of patients with pleural infections due to other pathogens.
2. Case presentation
An 83-year-old man suffered from cough, right chest pain, and progressive dyspnea for sixteen days. The patient had a medical history of chronic obstructive pulmonary disease (COPD) with home oxygen therapy (HOT), chronic renal disorder, diabetes mellitus (DM), and cerebral infarction. He had a smoking history (30 pack-years), alcohol abuse history, and poor dental hygiene.
His vital signs on admission showed afebrile status, tachycardia at 105 beats per minute, and hypoxemia with an oxygen saturation of 88% with a 5 L nonrebreather mask. Physical examination revealed no abnormalities, except for inspiratory coarse crackles in the right lower lung. An arterial blood sample showed a PaCO2 of 27.4 mmHg and a PaO2 of 59.3 mmHg with a 5 L nonrebreather mask. The laboratory findings showed leukocytosis (13980/μL with 90.0% polymorphic nuclear leukocytes), increased C-reactive protein (CRP) (28.24 mg/dL), renal dysfunction, and hemoglobin A1c at 7.7% (Table 1). A moderate amount of right-sided pleural effusion was present on the radiograph (Fig. 1), and chest computed tomography (CT) showed right loculated pleural effusion and emphysematous changes in both lungs (Fig. 2). A chest drainage tube was inserted, and pleural fluid analysis was performed. The pleural fluid examination revealed a high white blood cell count, at 2794/μL, with 55.0% neutrophils and 43.5% lymphocytes. High protein and lactate dehydrogenase (LDH) in the pleural fluid indicated exudative effusions. Gram staining of pleural fluid was negative.
Table 1.
The laboratory findings of the patient.
| Hematology | Biochemistry | Arterial blood gas (5 L/min mask) | |||
|---|---|---|---|---|---|
| Hb | 12.0 g/dL | Na | 139 mmol/L | pH | 7.301 |
| Ht | 34.4 % | K | 4.3 mmol/L | PaCO2 | 27.4 Torr |
| RBC | 354 × 104/μL | Cl | 108 mmol/L | PaO2 | 59.3 Torr |
| WBC | 13980/μL | BUN | 55.0 mg/dL | HCO3 | 27.4 mmol/L |
| Seg | 90.0 % | Cr | 3.23 mg/dL | BE | −11.6 mmol/L |
| Eo | 0.0 % | TP | 6.84 g/dL | ||
| Baso | 0.1 % | Alb | 2.09 g/dL | Pleural fluid | |
| Mono | 2.8 % | T-bil | 0.3 mg/dL | Total cell count | 2794/μL |
| Lymph | 7.1 % | AST | 25 IU/L | Neutrophils | 55.0 % |
| Plt | 33.7 × 104/μL | ALT | 21 IU/L | Lymphocytes | 43.5 % |
| PT-INR | 1.15 | LDH | 163 IU/L | Eosinophils | 1.0 % |
| APTT | 29.0 sec | CK | 162 IU/L | Macrophages | 0.5 % |
| Fib | 732 mg/mL | Glu | 377 mg/dL | TP | 4.82 g/dL |
| FDP | 28.0 μg/mL | CRP | 28.24 mg/dL | LDH | 944 IU/L |
| D-dimer | 2.12 μg/mL | PCT | 1.19 ng/mL | Glu | 285 mg/dL |
| (1 → 3)-β-D-glucan | <6.0 ng/mL | ADA | 34.9 U/L | ||
| HbA1c | 7.7 % | ||||
Fig. 1.
A chest radiograph showing right pleural effusion.
Fig. 2.
A chest computed tomography scan showing right pleural effusion, without pulmonary lesions or gas bubbles throughout.
He was diagnosed with pleural infection and treated empirically with ampicillin/sulbactam 3.0 g IV every 8 hours. However, drug eruption appeared two days after starting the antibiotic. He was diagnosed with a penicillin allergy, and the treatment was changed to clindamycin and levofloxacin. He improved gradually, and the pleural fluid was reduced. Therefore, the chest drain tube was removed, clindamycin was stopped, and 250 mg of oral levofloxacin daily was prescribed on the eighteenth day of hospitalization. However, the improvement of empyema stopped (Fig. 3). On the twenty-sixth day of hospitalization, A. meyeri was cultured from pleural effusion fluid on Gifu anaerobic medium semisolid agar; other bacteria were not cultured. He was diagnosed with complex complicated parapneumonic effusion based on Light's classification [7]. Drug-susceptibility testing revealed that the cultured A. meyeri was resistant to tosufloxacin and sensitive to clindamycin. The treatment was changed to 900 mg of oral clindamycin daily, and his CRP level decreased to within normal limits; a chest radiograph showed complete resolution of the pleural effusion. He had received clindamycin therapy for 3 months, and there has been no evidence of recurrence thus far. We obtained informed consent from the patient's family for the publication of this report.
Fig. 3.
The clinical course of the patient. SBT/ABPC ampicillin/sulbactam; LVFX levofloxacin; CLDM clindamycin; WBC white blood cell; CRP C-reactive protein.
3. Discussion
This is a case report of a rare pleural infection caused by A. meyeri in a patient with a penicillin allergy. The treatment was difficult due to the delayed culture of A. meyeri. Actinomyces is a gram-positive anaerobic bacteria [4], [5], [6], 8] and a slow-growing organism that can be cultured for up to three weeks [8]. Therefore, patients with Actinomyces pleural infection need to be treated without information regarding the causative pathogen for a long time until Actinomyces is cultured, and they might receive ineffective antibiotics, similar to our case. Previous studies have reported the following other features of Actinomyces infections [1]: there is typically slow progression of disease [[2], [9]]; drug-susceptibility testing can indicate Actinomyces susceptibility to β lactams, clindamycin, and other agents, whereas fluoroquinolones perform poorly [8, 10]; and there are risk factors of pulmonary actinomycosis, such as being a middle-aged or elderly male, having a history of alcoholism, having poor dental hygiene, and having structural lung diseases [6, 11, 12]. Our patient showed similar risk factors. However, Actinomyces pleural infection is rare and does not have specific reported clinical findings [1, [4], [5], [6], 13]. If the characteristics of Actinomyces pleural infection are known, patients might be able to avoid treatment with ineffective antibiotics. Therefore, we reviewed the data of patients with Actinomyces pleural infection and compared the data to those for other pathogens.
We retrospectively collected the data of forty-one patients with pleural infection for whom pathogens were cultivated from pleural effusion samples at the Respiratory Disease Center of Fukujuji Hospital from January 2012 to December 2018. Actinomyces were cultured in three out of 41 patients (7.3%), and other pathogens, such as the Streptococcus anginosus group (n = 11, 26.8%), Streptococcus pneumoniae (n = 3, 7.3%), Streptococcus mitis (n = 3, 7.3%), Staphylococcus aureus (n = 2, 4.9%), anaerobic bacteria (n = 13, 31.7%), and others (n = 5, 13.2%) were cultured from the rest of the patients. Seven patients (18.4%) presented coinfections. Actinomyces pleural infection was not as rare as 7.3% and was similar to the rate of S. pneumoniae pleural infection. In addition, the data of nineteen adult patients with Actinomyces pleural infection were collected from PubMed and the Japan Medical Abstracts Society, using the keywords “actinomyces empyema”, “actinomyces pleural effusion”, and “actinomyces pleuritis” in English and Japanese only [4], [5], [6], [11], [12], [13], [14], [15], [16], [17], [18], [19], [20], [21], [22], [23], [24], [25], [26], [27], [28], [29], [30], [31], [32]. Cases with no Actinomyces identified in the pleural effusion and no English abstracts were excluded. The data of those patients and our three patients were combined for analysis, and finally, the characteristics were compared between the twenty-eight patients with Actinomyces pleural infection (the Actinomyces group) and our thirty-eight patients with other-pathogen pleural infection (the other pathogens group) (Table 2). All data were analyzed and processed using EZR, version 1.35. Student's t tests, Mann–Whitney U tests, and Fisher's exact tests were used to compare groups. The level of statistical significance was set at p = 0.05 (2-tailed).
Table 2.
The characteristics of the 23 cases of Actinomyces empyema from the literature review compared to the other-pathogen cases.
| Actinomyces (n = 28) | Other pathogensa (n = 38) | p-value | |
|---|---|---|---|
| Age, median (IQR), years | 57.0 (43.5–68.3) | 68.0 (59.3–73.0) | 0.008 |
| Sex (Male/Female) | 21/7 | 33/5 | 0.333 |
| Comorbidity, n (%)a | 19 (73.1) | 30 (83.3) | 0.360 |
| Respiratory disease as an underlying disease, n (%)a | 5 (19.2) | 16 (44.4) | 0.057 |
| Immune suppression, n (%)a | 7 (27.0) | 12 (33.3) | 0.781 |
| Smoking history, n (%)b | 16 (100) | 30 (83.3) | 0.408 |
| Alcohol abuse, n (%)c | 11 (78.6) | 12 (38.7) | 0.023 |
| Duration from symptom onset to hospital admission, median (IQR), dayd | 25.5 (13.3–45.0) | 9.5 (4.0–14.3) | <0.001 |
| Radiological findings | |||
| Pleural effusion in half or more of thorax on chest radiograph, n (%)e,b | 15 (75.0) | 16 (43.2) | 0.023 |
| Pleural effusion | |||
| LDH, median (IQR), IU/Lf | 1045 (879–20265) | 3817 (1586–11844) | 0.646 |
| TP, median (IQR), g/dLf | 3.70 (2.90–4.76) | 3.86 (3.07–4.56) | 1.000 |
| Multiple pathogens cultured, n (%) | 8 (25.0) | 7 (18.4) | 0.382 |
| Treatment | |||
| A chest drainage tube inserted, n (%) | 21 (75.0) | 31 (81.6) | 0.555 |
| Duration of antibiotic therapy, median (IQR), weeks | 16 (6–24) | 4 (3–7) | <0.001 |
| Thoracotomy, n (%) | 6 (15.8) | 3 (7.9) | 0.153 |
| Intrapleural urokinase, n (%) | 1 (3.6) | 7 (18.4) | 0.125 |
LDH lactate dehydrogenase, TP total protein.
a; Actinomyces n = 26, other pathogens n = 36, b; Actinomyces n = 17, other pathogens n = 36, c; Actinomyces n = 14, other pathogens n = 31, d; Actinomyces n = 20, other pathogens n = 36, e; Actinomyces n = 20, other pathogens n = 37, f; Actinomyces n = 11, other pathogens n = 27.
Streptococcus milleri group (n = 11, 26.8%), Streptococcus pneumoniae (n = 3, 7.3%), Streptococcus mitis (n = 3, 7.3%), Staphylococcus aureus (n = 2, 4.9%), anaerobic bacteria (n = 13, 31.7%), and others (n = 5, 13.2%).
The measurement of pleural effusion was calculated as the length from lung base to the top of the pleural effusion divided by the length from lung base to the top of the apex on the midclavicular line on chest radiographs.
Among the Actinomyces group, the Actinomyces species were A. meyeri (n = 10, 35.7%), Actinomyces israelii (n = 10, 35.7%), Actinomyces naeslundii (n = 2, 7.1%), Actinomyces odontolites (n = 1, 3.6%), and Actinomyces spp. (n = 6, 21.4%). One patient showed both A. meyeri and A. israelii. Eight patients (28.6%) presented coinfections with other anaerobic bacteria. The median age in the Actinomyces group was 57.0 years (interquartile range (IQR): 43.5–68.3 years), which was lower than that in the other pathogens group (median (IQR): 63 years (59.3–73.0), p = 0.008). The number of patients with alcohol abuse in the Actinomyces group was higher than that in the other pathogens group (n = 11 (78.6%) vs n = 12 (38.7%), p = 0.023). However, there were no significant differences in the ratios of males (males n = 21 (75.0%) vs n = 33 (86.8%), p = 0.333) or the rates of underlying pulmonary disease (n = 5 (19.2%) vs n = 16 (44.4%), p = 0.057), which were both reported as risk factors for pulmonary actinomycosis. We evaluated pleural effusion by calculating the length from the lung base to the top of the pleural effusion divided by the length from lung base to the top of the apex on the midclavicular line on the chest radiograph. The rate of pleural effusion involving half or more of the thorax on chest radiographs was higher in the Actinomyces group than in the other pathogens group (n = 15 (75.0%) vs n = 16 (43.2%), p = 0.023). Furthermore, the duration from symptom onset to hospital admission was longer in the Actinomyces group than in the other pathogens group (median (IQR) 25.5 days (13.3–45.0 days) vs 9.5 days (4.0–14.3 days), p < 0.001). These results might be related to the fact that Actinomyces is a slow-growing organism [8] and that actinomycosis has a slow disease progression [9]. We suspected that Actinomyces would induce weak symptoms in the early stage and gradually induce stronger symptoms with growth. The characteristics in the Actinomyces group were similar to those of pneumonia and lung abscess caused by actinomycetes [8].
This investigation had several limitations. This review was conducted retrospectively in a single-center hospital, and some medical data were not recorded. There was publication bias because the data of many of the patients with Actinomyces pleural infection were from published reports. Moreover, the detailed measurement of pleural effusion is difficult. Some medical data, such as the duration from symptom onset to hospital visit, were not described in detail. Some patients in the other pathogens group might have been infected with Actinomyces but were not diagnosed because Actinomyces is a difficult species to culture, while all cases of other phenotypes in our study had negative Actinomyces results on anaerobic culture. The review was approved by the Institutional Review Board of the Fukujuji Hospital.
4. Conclusion
A. meyeri pleural infection in a patient with a penicillin allergy was difficult to treat due to the delayed culture of A. meyeri. Furthermore, we demonstrated that Actinomyces pleural infection is a long-term process, resulting in a large amount of pleural effusion compared to other pleural infection phenotypes. When a patient with a severe pleural infection shows slow progression, Actinomyces infection should be considered.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
None.
References
- 1.Kononen E., Wade W.G. Actinomyces and related organisms in human infections. Clin. Microbiol. Rev. 2015;28(2):419–442. doi: 10.1128/CMR.00100-14. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Heo S.H., Shin S.S., Kim J.W., Lim H.S., Seon H.J., Jung S.I., Jeong Y.Y., Kang H.K. Imaging of actinomycosis in various organs: a comprehensive review. Radiographics. 2014;34(1):19–33. doi: 10.1148/rg.341135077. [DOI] [PubMed] [Google Scholar]
- 3.Markey C.M., Vestal L.E. Actinomyces meyeri: a rare cause of postsurgical pelvic actinomycosis. Case Rep Obstet Gynecol. 2018:3842048. doi: 10.1155/2018/3842048. 2018. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Clerigo V., Fernandes L., Feliciano A., Carvalho L. A rare case of Actinomyces meyeri empyema: still a challenging entity to manage. Respir Med Case Rep. 2017;22:203–205. doi: 10.1016/j.rmcr.2017.08.010. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Vallet C., Pezzetta E., Nicolet-Chatelin G., El Lamaa Z., Martinet O., Ris H.B. Stage III empyema caused by Actinomyces meyeri: a plea for decortication. J. Thorac. Cardiovasc. Surg. 2004;127(5):1511–1513. doi: 10.1016/j.jtcvs.2003.11.043. [DOI] [PubMed] [Google Scholar]
- 6.Paris E., Piscopo T., Cassar K. Empyema secondary to actinomyces meyeri treated successfully with ceftriaxone followed by Doxycycline. Case Rep Infect Dis. 2016:9627414. doi: 10.1155/2016/9627414. 2016. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Light R.W. A new classification of parapneumonic effusions and empyema. Chest. 1995;108(2):299–301. doi: 10.1378/chest.108.2.299. [DOI] [PubMed] [Google Scholar]
- 8.Wong V.K., Turmezei T.D., Weston V.C. Actinomycosis, BMJ. 2011;343:d6099. doi: 10.1136/bmj.d6099. [DOI] [PubMed] [Google Scholar]
- 9.Kono S.A., Nauser T.D. Contemporary empyema necessitatis. Am. J. Med. 2007;120(4):303–305. doi: 10.1016/j.amjmed.2006.09.019. [DOI] [PubMed] [Google Scholar]
- 10.Smith A.J., Hall V., Thakker B., Gemmell C.G. Antimicrobial susceptibility testing of Actinomyces species with 12 antimicrobial agents. J. Antimicrob. Chemother. 2005;56(2):407–409. doi: 10.1093/jac/dki206. [DOI] [PubMed] [Google Scholar]
- 11.Jung H.W., Cho C.R., Ryoo J.Y., Lee H.K., Ha S.Y., Choi J.H., Kwak Y.G. Actinomyces meyeri empyema: a case report and review of the literature. Case Rep Infect Dis. 2015:291838. doi: 10.1155/2015/291838. 2015. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Attaway A., Flynn T. Actinomyces meyeri: from "lumpy jaw" to empyema. Infection. 2013;41(5):1025–1027. doi: 10.1007/s15010-013-0453-8. [DOI] [PubMed] [Google Scholar]
- 13.Kleontas A., Asteriou C., Efstathiou A., Konstantinou E., Tsapas C., Barbetakis N. Actinomyces israelii: a rare cause of thoracic empyema. Tuberk Toraks. 2011;59(4):399–401. doi: 10.5578/tt.2454. [DOI] [PubMed] [Google Scholar]
- 14.Ferreiro L., Perez Del Molino M.L., Rabade C., Valdes L. Actinomyces meyeri empyema. Arch. Bronconeumol. 2017;53(5):274–276. doi: 10.1016/j.arbres.2016.09.016. [DOI] [PubMed] [Google Scholar]
- 15.Ishiguro T., Takayanagi N., Tanaka K., Yoneda K., Sugita Y., Watanabe K. [A case of empyema due to Capnocytophaga sp. and Actinomyces israelii] Nihon Kokyuki Gakkai Zasshi. 2009;47(10):906–911. (Japanese) [PubMed] [Google Scholar]
- 16.Matsuura Y., Ishikawa S., Takiguchi Y. [Two cases of anaerobic empyema including Actinomyces] Nihon Kokyuki Gakkai Zasshi. 2009;47(3):191–194. (Japanese) [PubMed] [Google Scholar]
- 17.Hooi L.N., Na B.S., Sin K.S. A case of empyema thoracis caused by actinomycosis. Med. J. Malaysia. 1992;47(4):311–315. [PubMed] [Google Scholar]
- 18.Karetzky M.S., Garvey J.W. Empyema due to Actinomyces naeslundi. Chest. 1974;65(2):229–230. doi: 10.1378/chest.65.2.229. [DOI] [PubMed] [Google Scholar]
- 19.Mohan D.R., Antony B., Shivakumarappa G.M. Empyema thoracis due to actinomyces odontolyticus. Indian J. Pathol. Microbiol. 2009;52(1):120–121. doi: 10.4103/0377-4929.44995. [DOI] [PubMed] [Google Scholar]
- 20.Reyes C.V., Thompson K.S., Jensen J. Fine needle aspiration biopsy of mastitis secondary to empyema necessitatis. A report of two cases. Acta Cytol. 1999;43(5):873–876. doi: 10.1159/000331307. [DOI] [PubMed] [Google Scholar]
- 21.Lentino J.R., Allen J.E., Stachowski M. Hematogenous dissemination of thoracic actinomycosis due to Actinomyces meyeri. Pediatr. Infect. Dis. 1985;4(6):698–699. doi: 10.1097/00006454-198511000-00026. [DOI] [PubMed] [Google Scholar]
- 22.Ikezawa Y., Harada T., Akiyama Y., Ogasawara H., Kishi F. [A case of thoracic empyema caused by Actinomyces species nova] Nihon Kokyuki Gakkai Zasshi. 2009;47(8):727–730. (Japanese) [PubMed] [Google Scholar]
- 23.Tamaki Sato S.I., Nakano Hiroshi, Sato Kento, Sato Masamichi, Abe Shuichi, Shibata Yoko, Kubota Isao. [A case of pyothorax due to mixed infection including actinomyces] Jpn. J. Chest Dis. 2015;74(11):1255–1259. (Japanese) [Google Scholar]
- 24.Yamamoto Y., Matsuda M., Shibata M. [A case of pyothrax caused by Actinomyces israelii], Japanese. J. Med. Technol. 2000;49(8):1184–1187. (Japanese) [Google Scholar]
- 25.Gupta A., Lodato R.F. Empyema necessitatis due to Actinomyces israelii. Am. J. Respir. Crit. Care Med. 2012;185(12):e16. doi: 10.1164/rccm.201108-1532CR. [DOI] [PubMed] [Google Scholar]
- 26.Yamato T., Otsuka M., Sekine K., Yoshioka Y., Morinari H., Furuie T., Yoshioka I., Tanaka M., Fujino T. [A case of empyema due to Actinomyces israelii (author's transl)] Jpn. J. Thorac. Dis. 1981;19(7):496–501. (Japanese) [PubMed] [Google Scholar]
- 27.Dolai T.K., Kumar R., Chakrabarti P., Das A., Mahapatra M., Mishra P., Saxena R., Chaudhury R. Actinomycetes species infection in a patient of T-cell acute lymphoblastic leukemia (ALL) presenting with loculated pleural effusion. Pediatr. Hematol. Oncol. 2008;25(5):477–480. doi: 10.1080/08880010802106580. [DOI] [PubMed] [Google Scholar]
- 28.Shinagawa N., Yamaguchi E., Takahashi T., Nishimura M. Pulmonary actinomycosis followed by pericarditis and intractable pleuritis. Intern. Med. 2002;41(4):319–322. doi: 10.2169/internalmedicine.41.319. [DOI] [PubMed] [Google Scholar]
- 29.Nagao M., Fukuda A., Matsumura T., Kimura T., Seno H. Pulmonary actinomycosis mimicking a lung metastasis from esophageal cancer; a case report. BMC Pulm. Med. 2018;18(1):39. doi: 10.1186/s12890-018-0602-z. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 30.Maki Y., Fujikura Y., Tagami Y., Hamakawa Y., Sasaki H., Misawa K., Hayashi N., Kawana A. Empyema with multiple bronchopleural fistulae improved by bronchial occlusion using an Endobronchial Watanabe spigot with the push and slide method. Intern. Med. 2019;58(9):1315–1319. doi: 10.2169/internalmedicine.1877-18. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31.Sato T., Inoue S., Nakano H., Sato K., Sato M., Yamauchi K., Igarashi A., Abe S., Shibuya Y., Kubota I. [A case of pyothorax due to mixed infection including actinomyces] Jpn. J. Chest Dis. 2015;74(11):1255–1259. (Japanese) [Google Scholar]
- 32.Nishio C., Konishi H., Oh K., Tomioka H. [Thoracic actinomycosis mimicking lung cancer] AJRS. 2018;7(4):255–258. (Japanese) [Google Scholar]