Secondary Logo

Journal Logo

Systematic Review and/or Meta-analysis

Pericardial and pulmonary actinomycosis, simulating inflammatory myofibroblastic tumor: the role of surgery

Chaudhry, Ikram ul H. FRCS(CTh); M. AlFraih, Othman MD; A. AlAbdulhai, Meenal MD; A.L. Qahtani, Yousif MD; Al Maimon, Hisham MD; Tariq Khan, Mohammad MD; Ihsan, Esha MD; Alghamdi, Abdullah M. MD

Author Information
doi: 10.1097/SR9.0000000000000051
  • Open

Abstract

Patients and methods

We identified 8 cases of actinomycosis on a retrospective review of patient charts from 2008 to 2021, which presented different clinical manifestations1. In 8 cases, 6 men and 2 women with a mean age of 56 years were diagnosed on radiographic findings [computed tomography (CT) of the chest]. Patients were smokers. One patient had a history of bronchiectasis. Five patients had poor oral hygiene (dental issues). One patient presented with right side chest mass, pyrexia, and weight loss.

Follow-up and analysis

We reviewed patient charts and collected the data. All patients were followed up for 2 years in outpatient. Chest x-ray and CT scan of the thorax were analyzed, and there was no relapse of the disease.

Imaging treatment and outcome

Patients’ clinical manifestations varied. Hemoptysis, weight loss, and dental issues. Fatigue weakness; 1 patient presented with a chest wall mass and fever. Blood investigations were within normal limits, and sputum examination showed normal flora and no abnormal pathogens. CT scan of the chest showed three patients had right lower lobe opacity and infiltrate. Two patients had left upper lobe mass. Two patients had left pericardial mass, and 1 had right upper chest wall mass. Bronchial lavage was not conclusive, and CT-guided biopsy for all patients showed a myofibroblastic tumor with no actinomyces colonies. Therefore, surgery was indicated for resection of the neoplastic mass. Surgical resection included right upper lobectomy (3 patients) (Figs. 1, 2), left upper lobectomy (1 patient), segmentectomy 1 patient, pericardial resection along with lung wedge, pericardial defect was repaired with gortex patch to avoid cardiac herniation (2 patients) (Figs. 3, 4). The chest wall resection enblock with right upper lobe 1 (patient) operating time was 60–200 minutes mean operating time (90 min). Blood loss varied from 100 to 600 ml. No operative complication or death was recorded. Postoperative antibiotics treatment was continued for 2–6 months. All patients were followed up with a serial chest x-ray, and there has been no recurrence.

F1
Figure 1:
Computed tomographic (CT) (A, B) scan of thorax soft tissue window showing left chest mass adherent to the pericardium. C and D, A follow-up CT scan of the chest after 6 months showed no residual disease.
F2
Figure 2:
A, Macroscopic picture of the resected lung. B, Microscopic appearance of lung tissue showing actinomycosis colonies.
F3
Figure 3:
A and B, Resected specimen. C, Pericardial repair.
F4
Figure 4:
A, Preoperative computed tomographic (CT) scan of the chest, soft tissue window showing right upper zone chest mass adherent to superior vena cava. B, The lung window shows a mass in the right chest upper zone. C, CT scan thorax, the postoperation mediastinal window shows no residual disease. D, Lung window after upper and lower lobectomy. E and F, Postoperative CT scan chest.

Introduction

Actinomycosis is a rare, slowly growing suppurative granulomatous bacterial infection caused by microaerophilic bacteria Actinomyces israeli named after a German surgeon, James Adolf Israel (1848–1926). Wolf and Israel studied the organism for the first time in 1878–1891 from autopsy samples and described their cultural characteristic and anaerobic growth2,3. Further studies identified a family of these organisms (Actinomyces pyrogens, Actinomyces naeslundii, Actinomyces voscosus, Actinomyces denticolens, Actinomyces howellii, Actinomyces meyeri, Actinomyces hordevulneris). Ponfic, in 1882, reported the first case of thoracic actinomycosis4. In 1936 Owen wrote a series of cases of actinomycosis caused by actinomycosis Bovis. Thoracic actinomycosis is an uncommon entity, and it poses a real diagnostic challenge. Sometimes, surgery is the only definite answer for diagnosing and treating complex cases. A diagnosis is often based on histologic evidence of sulphur granules colonies of actinomyces. Thoracic actinomycosis can present as lung abscess, empyema, chest wall sinuses, mediastinitis, and rarely life-threatening hemoptysis5,6.

Discussion

Human actinomycosis is a chronic suppurative disease caused by 5 species of the genus of Actinomyces, but Actinomyces israelli most commonly produces infection in humans. Actinomyces is a component of the normal flora of the mouth and gastrointestinal tract, female genitalia. Cardiac involvement is rare, and the pericardium is the most frequently involved from the adjacent pulmonary foci. Actinomycosis is endemic, occurring worldwide. It has no predilection for sex, age, race, and occupation5–8.

Thoracic actinomycosis commonly occurs by aspiration of oropharyngeal secretions containing actinomycetes, contamination from esophageal perforation, and rarely by direct or hematogenous spread from distant source neck or neck abdomen lesions. If diagnosis and treatment are delayed, thoracic actinomyces, which initially present as lung mass or pulmonary infiltrates, can spread to the pleura, pericardium, and chest wall, leading to chronic Sulphur discharging sinuses9–11.

It has been reported in patients with HIV and leukemia and in patients with other causes of immunodeficiency, although it is not an opportunistic organism. However, no underlying disease or immunosuppression is found in most patients. Actinomycosis is a chronic granulomatous infection that can involve any system in human being12–14.

Chest pain, dyspnea, fever, weight loss, and cough are prevalent manifestations of thoracic and pericardial involvement. Examination of pleural and pericardial fluid may reveal a polymorphonuclear leukocyte predominance, but detection of sulfur granules and culture of the Actinomyces organism are negative15. The exact cause of this disease is unknown possible risk factors include aspiration pneumonia, alcohol abuse, and periodontal disease. Actinomyces can cause serious health issues like purulent pericarditis leading to cardiac tamponade or constrictive pericarditis. Most cases originate from a thoracopulmonary site of actinomycosis and spread directly to the pericardium.

The reported incidence of actinomycosis is cervical, 55% abdominal, 20% thoracic, 15% and 10% involve multiple organs. Pulmonary actinomycosis accounts for 15%–45% of all cases reported, and cardiac involvement is only 2%. Eighty percent of patients have an infection of the pericardium16–18. In 1944 Cornell and Shookhoff reported 68 cases of cardiac actinomycosis. Since this publication, it has been suggested that the heart has been involved in only about 2% of all cases of this infection, with the pericardium as the most common site. The usual presentation of pericardial actinomycosis is pericardial effusion that may evolve into cardiac tamponade or constrictive pericarditis19.

Pulmonary actinomycosis also has been reported in patients with fracture mandible and dental procedures; most likely, this is due to hematogenous spread. Intrathoracic actinomycosis is more prone in patients who had oropharyngeal aspiration, dental and periodontal disease, and immunocompromised patients.20–22

Cardiac actinomycosis is a rare disease and usually manifests as pericardial disease, accounting for almost 70%–80% of cardiac cases. Endocarditis and myocarditis are exceedingly rare23. Thoracic actinomycosis is a significant risk factor for the involvement of pericardium. The patient with cardiac actinomycosis usually presents with nonspecific clinical manifestations such as dyspnea (53%), cough (63%), chest pain (53%), pleural effusion (68%), tachycardia (63%), hepatomegaly and peripheral edema, and cutaneous sinuses (30%–50% cardiac tamponade and constrictive pericarditis in 48% and 36%, respectively15,24. There are very few cases of pericardial actinomycosis reported in the medical literature. Purulent pericarditis is exceedingly rare. Usually, patients with pericardial actinomycosis develop symptoms about 6 months before diagnosis. Diagnosis of pericardial and pulmonary actinomycosis is a real dilemma due to difficulty in isolation and culture of the organism. It must be cultured in strictly anaerobic conditions. Fife and colleagues; in 1991 reported a primary thoracic focus of infection in 15 subjects, and in 4, there was no identifiable contiguous site of infection. They obtained 2 purulent pericardial fluids from 10 (53%) of 19 patients. However, A. israeli was successfully cultured from the fluid in only 2 cases25. In the majority of cases in the literature, actinomycosis has been diagnosed by histopathology because it is challenging by radiologic examination, bronchoscopic lavage and sputum culture to differentiate from pulmonary neoplasm inflammatory myofibroblast tumors, tuberculosis, and fungal infection. Actinomycosis can induce an inflammatory myofibroblast reaction. Therefore, histopathologic examination of surgical biopsy is still the best diagnostic tool8. Patients with pulmonary actinomycosis usually present with a chronic chest infection, fever, cough, chest pain, and rarely life-threatening hemoptysis. If the treatment is delayed, apart from chronic pneumonitis, the disease can spread to the chest wall, pleura, pericardium, and mediastinum and also can progress to other organs by hematogenous spread. Unless the bronchial lavage, sputum analysis, or true cut biopsy do not show the actinomycosis colonies, the diagnosis cannot be confirmed because the Sulphur granules are not disease-specific as the absence of sulphur granules has been reported in cerebral actinimycosis26. Histopathologic confirmation of sulphur granules and actinomyces colony is essential to establish the diagnosis. Surgery is indicated if there is no established diagnosis, failure of response to medical treatment, uncontrolled infection, and hemoptysis.

Massive hemoptysis is a lethal condition, and mortality of 30%–50% due to asphyxia has been reported in such cases. The gold standard of treatment for pulmonary actinomycosis complicated by massive hemoptysis is surgery27,28. However, bronchial artery embolization was reported in the literature by Remy et al29 in 1973 with good results. Other maneuvers to control the hemoptysis are bronchoscopic cold saline lavage, endotracheal instillation of fibrinogen thrombin, and radiotherapy and laser photocoagulation30,31. In vitro trials have shown that actinomycosis is susceptible to many antibiotics. Therefore, the mainstay of the treatment of actinomycosis is antimicrobial therapy. Penicillin G and amoxicillin are the drugs of choice for at least 6–10 months duration32.

Clinical data support the use of penicillin G as the drug of choice, and in order to avoid relapse, prolonged treatment is advisable. Table 1, should tailor therapy according to individual need, but high doses (18–24 million units/d) of penicillin over a long period of time (2–6 wk) followed by oral therapy with penicillin or amoxicillin to complete 6–12 months is recommended15. However, there are some reports of successful short-term treatment with beta-lactam antibiotics in exceptional circumstances. For penicillin-allergic patients, doxycycline, minocycline, tetracycline, clindamycin, erythromycin, and cephalosporins have been proven to be effective in case reports,33–35. A recent in vitro study assessing the susceptibility of human clinical isolates of Actinomyces species to different antimicrobial agents showed that bacterial identification might be critical because of the resistance to some antibiotics.

Table 1 - Demographic data, treatment and outcome.
N Sex Clinical Manifestations Initial Diagnosis Final Histopathology Treatment Outcome
5 Male Poor oral hygiene, hemoptysis, shortness of breath True cut biopsy, myofibroblastic tumor Actinomycosis 4 patients had lobectomy + Ampicillin for 6 mo Complete
2 Male1 Female1 Sinusitis, cough, True cut biopsy, Myofibroblastic tumor Actinomycosis 2 patients had lung resection+pericardium Ampicillin Complete
1 Male Chest pain, fever, chest wall mass No true cut biopsy Actinomycosis Right upper lobectomy chest wall resection+Ampicillin Complete
Total number of patients 8, N=number of patients=male, female.

Response to therapy can be slow. It may take months. Hyperbaric oxygen therapy may be used as an adjunct to conventional therapy when the disease process is refractory to antibiotics. Surgical treatment is controversial and may include incision and drainage of abscesses, resection of necrotic tissue, and curettage of bone.

Postoperatively patients should continue the antimicrobial therapy for 6 months to eradicate the disease completely. Beik et al36 reported 25 cases of actinomycosis, and 14 cases were operated. Sometimes surgery is the only way to establish the diagnosis and control the massive hemoptysis. Early recognition of actinomycosis is essential to avoid late complications such as lung abscess, empyema thoraces, chest wall sinuses, mediastinitis, pericarditis, and massive hemoptysis37–39.

Prognosis is excellent provided the diagnosis is made early and appropriate antibiotics therapy is initiated. The most frequent complication of actinomycosis is hematogenous dissemination, especially as a result of thoracic disease. It produces manifestations that can be misdiagnosed as metastatic disease, with multiple nodules in virtually any organ or tissue. However, irrespective of the extent of the disease, it has a good prognosis when discovered in time. Mortality. varies from 0 to 28%, depending mainly on the site of infection and the time to diagnosis.

Conclusion

Thoracic actinomycosis (pulmonary and pericardial) is a diagnostic challenge for the surgeon. All cases were diagnosed primarily as myofibroblastic tumors with a true cut needle biopsy. But later on, the detailed histopathologic examination of the resected specimen revealed actinomycosis as the final diagnosis. Postoperatively, all patients were treated with antimicrobial therapy for 6 months with an excellent outcome. Actinomycosis is a disease that poses a significant diagnostic challenge because of its nonspecific clinical manifestations and its tendency to mimic different conditions. Early diagnosis and appropriate antimicrobial therapy are essential as delayed treatment can lead to increased morbidity and even mortality.

Ethical approval

None.

Patient consent

Written informed consent was obtained from the patients for publication of this and accompanying images. A copy of the written consent is available for review by the Editor in chief of this journal on request.

Sources of funding

None.

Author contribution

None.

Conflicts of interest disclosure

The authors declare that they have no financial conflict of interest with regard to the content of this report.

Research registration unique identifying number (UIN)

Research Registry number 7843.

Guarantor

Ikram ul H. Chaudhry.

References

1. Agha RA, Sohrabi C, Mathew G, et al. The Process 2020 Guidelines: updating consensus preferred reporting of case series in surgery (PROCESS): guidelines. Int J Surg 2020;2 84:231–5.
2. Israel J, Tedder M, Wolf WG. Neue Beobachtungen auf dem Gebiete der Mykosen des Menschen. Actinomycosis and nocardial infections. Chest Surg Clin North Am 1993;3:653–70.
3. Ponfic E. Die Actinomycosis des Menshen Eine Neue Infeckionsk-rankeit Auf Vergleiccened-Pathologischen und Experimenteller. Berlin, Hirschwald: Grundiage Gescdildert; 1882.
4. Mabeza GF, Macfarlane J. Pulmonary actinomycosis. Eur Respir J 2003;21:545–51.
5. Smego R Jr, Foglia G. Actinomycosis. Clin Infect Dis 1998;26:1255–61.
6. Sarkonen N, Kononen E, Summanen P, et al. Oral colonization with Actinomyces species in infants by two years of age. J Dent Res 2000;79:864–7.
7. Nikolaitchouk N, Hoyles L, Falsen E, et al. Collins characterization of Actinomyces isolates from samples from the human urogenital tract: description of Actinomyces urogenital sp.nov. Int J Syst Evol Microbiol 2000;50:1649–54.
8. Russo T Kasper DL, Fauci AS, Longo DL, Braunwald E, Hauser SL, Jameson JL. Actinomycosis. Harrison’s Principles of Internal Medicine, 16th ed. USA: McGraw-Hill; 2005:937–9.
9. De Montpreville VT, Nashashibi N, Dulmet EM. Actinomycosis and other bronchopulmonary infections with bacterial granules. Ann Diagn Pathol 1999;3:67–74.
10. Lerner PI. The lumpy jaw. Cervicofacial actinomycosis. Infect Dis Clin North Am 1988;2:203.
11. Arora AK, Nord J, Olofinlade O, et al. Esophageal actinomycosis: a case report and review of the literature. Dysphagia 2003;18:27–31.
12. Chaudhry SI, Greenspan JS. Actinomycosis in HIV infection: a review of a rare complication. Int J STD AIDS 2000;11:349–55.
13. Chen CY, Chen YC, Tang JL, et al. Splenic actinomycotic abscess in a patient with acute myeloid leukemia. Ann Hematol 2002;81:532–4.
14. Dominguez DC, Antony SJ. Actinomyces and Nocardia infections in immunocompromised and non-immunocompromised patients. J Natl Med Assoc 1999;91:35–9.
15. Makaryus AN, Latzman J, Yang R, et al. A rare case of Actinomyces israelii presenting as pericarditis in a 75-year-old man. Cardiol Rev 2005;13:125–7.
16. Peters GL, Davies RA, Veinot JP, et al. Cardiac actinomycosis; an unusual cause of the intracardiac mass. J Amar Soc Echocardiogr 2006;19:1530.e7–153011.
17. Hsieh M, Liu HP, Chang JP, et al. Thoracic actinomycosis. Chest 1993;104:366–70.
18. Endo S, Murayama F, Yamaguchi T, et al. Surgical considerations for pulmonary actinomycosis. Ann Thorac Surg 2002;74:185–90.
19. Comell A, Shookhoff HB. Actinomycosis of the heart simulating rheumatic fever: report of three cases with review of the literature. Arch Intern Med 1944;74:11–27.
20. Litwin KA, Jadbabaie F, Villanueva M. Case of pleural-pericardial disease caused by Actinomyces odontolyticus that resulted in cardiac tamponade. Clin Infect Dis 1999;29:219–220.
21. Sandoval V, Orea TA, Garcia ML, et al. Chronic cardiac actinomycosis: case report and literature review. Arch Inst Cardiol Mex 1988;58:243–5.
22. Slutzky AD, Claypool WD. Pericardial actinomycosis with cardiac tamponade from a contiguous thoracic lesion. Thorax 1989;44:442–3.
23. Shinagawa N, Yamaguchi E, Takahashi T, et al. Pulmonary actinomycosis followed by pericarditis and intractable pleuritis. Intern Med 2002;41:319–22.
24. Dutton W, Inclan AP. Cardiac actinomycosis chest. Chest 1968;54:565–6.
25. Fife TD, Finegold SM, Grennan T. Pericardial actinomycosis: case report and review. Rev Infect Dis 1991;13:120–6.
26. Acevedo F, Baudrand R, Letelier LM, et al. Actinomycosis: a great pretender. Case reports of unusual presentations and a review of the literature. Int J Infect Dis 2008;12:358–62.
27. Gourin A, Garzon A. Control of hemorrhage in emergency pulmonary resection for massive hemoptysis. Chest 1975;68:120–21.
28. Sehat S, Oreizie M, Moinuddin K. Massive pulmonary hemorrhage surgical approach as a choice of treatment. Ann Thorac Surg 1987;25:12–15.
29. Remy J, Voisin C, Ribet M, et al. Treatment embolization of severe or repeated hemoptysis associated with systemic hypervascularization. Nouv Presse Med 1973;2:2060–8.
30. Tsukamoto T, Sasaki H, Nakamura H, et al. Treatment of hemoptysis patients by thrombin and fibrinogen-thrombin therapy using a fiberoptic bronchoscope. Chest 1989;96:473–6.
31. Conolon AA, Hurwitz SS, Krije L. Massive hemoptysis review of 123 cases. J Thorac Cardiovasc Surg 1983;85:120–4.
32. Smith AJ, Hall V, Thakker B, et al. Antimicrobial susceptibility testing of Actinomyces species with 12 antimicrobial agents. J Antimicrob Chemother 2005;56:407–9.
33. Wagenlehner FM, Mohren B, Naber KG, et al. Abdominal actinomycosis. Clin Microbiol Infect 2003;9:881–5.
34. Leafstedt SW, Gleeson RM. Cervicofacial actinomycosis. Am J Surg 1975;130:496–8.
35. Louerat C, Depagne C, Nesme P, et al. Disseminated actinomycosis. Rev Mal Respir 2005;22:473–6.
36. Baik JJ, Lee GL, Yoo C-G, et al. Pulmonary actinomycosis in Korea. J Respirol 1999;4:31–35.
37. Chaudhry Iuh, Alhaji Z, Khan IS, et al. Role of surgery in pulmonary actinomycosis. JFJMC 2014;8:89–92.
38. Sharma M, Briski LE, Khatib R. Hepatic actinomycosis: an overview of salient features and outcome of therapy. Scand J Infect Dis 2002;34:386–91.
39. Rizzi A, Rocco G, Della Pona C, et al. Pulmonary actinomycosis: surgical considerations. Monaldi Arch Chest Dis 1996;51:369–72.
Keywords:

Pericardial mass; Myofibroblast tumor; Actinomycosis; Lung; Surgery

Copyright © 2022 The Authors. Published by Wolters Kluwer Health, Inc. on behalf of IJS Publishing Group Ltd.