Case Report: Pericardial Actinomycosis in a 79-Year-Old Man with Poor Dental Hygiene

ABSTRACT.

Actinomycosis is an uncommon infection caused by Actinomyces species, and the diagnosis is often challenging owing to low prevalence and diverse clinical manifestations. Pericardial involvement of actinomycosis is particularly rare. Here, we present a case of a 79-year-old man who initially complained of exertional dyspnea, orthopnea, and decreased urine amount. There was no fever, chest pain, or productive cough. Physical examination was remarkable for decreased breath sounds at the left lower lung field. Poor dental hygiene and a firm, well-defined mass without discharge over the hard palate were noted. Echocardiography revealed reduced ejection fraction of the left ventricle, global hypokinesia, and thickened pericardium (> 5 mm) with a small amount of pericardial effusion. On admission, the patient underwent diagnostic thoracentesis, and the results suggested an exudate. However, bacterial and fungal cultures were all negative. There was no malignant cell by cytology. Computed tomography revealed contrast-enhanced pericardial nodular masses. Video-assisted thoracoscopic pericardial biopsy was performed. Histopathology confirmed actinomycosis with chronic abscess formation, and a tissue culture yielded Aggregatibacter actinomycetemcomitans. The symptoms resolved with administration of clindamycin for 6 months. This case highlights the challenge in the diagnosis of cardiac actinomycosis, the potential role of concomitant microorganisms as diagnostic clues, and the favorable clinical response achieved with appropriate antibiotic treatment.

INTRODUCTION

Actinomycosis is an indolent, slowly progressive infection caused by Actinomyces species that normally colonize the oropharynx, gastrointestinal tract, and urogenital tract. Disruption of mucosa can lead to symptomatic infection, which is often characterized by abscess formation, tissue fibrosis, and draining sinuses. To date, diverse clinical manifestations of actinomycosis have been reported, including involvement of the cervicofacial area, thorax, abdominopelvic region, and central nervous system.¹ Despite a decrease in prevalence in the antibiotic era, the diagnosis of actinomycosis remains challenging.² Cases of actinomycosis with involvement of the pericardium are rarely reported. Here, we present the clinical course of pericardial actinomycosis in a 79-year-old man who had poor dental hygiene.

CASE REPORT

This 79-year-old Taiwanese man had been in his usual state of health until 3 weeks prior to this admission, when exertional dyspnea developed. Orthopnea, pitting edema over bilateral feet, decreased urine amount, and weight gain of 2 kg in a month were reported. There was no fever, night sweats, chest pain, productive cough, hemoptysis, abdominal discomfort, or dysuria.

He had a history of hypertension, dyslipidemia, paroxysmal atrial fibrillation (CHA₂DS₂-VASc score = 5), and coronary artery disease, two-vessel disease, for which he had undergone balloon angioplasty with stenting to the right coronary artery 3 years prior to this evaluation. He had been taking valsartan, furosemide, spironolactone, bisoprolol, digoxin, rivaroxaban, and rosuvastatin for years. He was married and lived with his wife in Taipei City. He had smoked one pack of cigarettes per day for 20 years and had quit for 40 years. He had had alcohol consumption on social occasions since adulthood and had quit for 3 years. He did not chew betel nuts. His mother had type 2 diabetes mellitus and hypertension. He reported no history of trauma within 6 months before this admission.

On examination, the patient was alert and fully oriented. The temperature was 36.4°C, the pulse 91 beats per minute, the respiratory rate 18 breaths per minute, the blood pressure 133/99 mm Hg, and the oxygen saturation 96% while he was breathing ambient air. Physical examination was remarkable for decreased breath sounds at the left lower lung field and bilateral lower limb pitting edema. A firm, well-defined mass without discharge over his hard palate was found (Figure 1A). He reported a history of poor oral hygiene since elementary school and had a total of five dental implants, with the most recent implant placed approximately 6 months prior to this evaluation. He also reported allergy to penicillin with fulminant skin rashes; thus he did not receive antibiotic prophylaxis during previous dental procedures. No rash or lymphadenopathy was found.

Figure 1.

Physical, microscopic, and imaging examinations. (A) A firm, well-defined mass without discharge was found on the hard palate. (B) Histopathology of a biopsy sample showed Splendore–Hoeppli phenomenon, H&E stain, 400×. (C) Branching filamentous gram-positive bacteria, GMS stain. (D) Low-dose CT of the chest, 6 months prior to this admission. (E) A CT scan performed upon admission showed pericardial soft-tissue lesions and pericardium thickening. (F) A CT scan performed 4 months after clindamycin treatment showed normalized thickness of the pericardium. CT = computed tomography; GMS = Grocott methenamine silver; H&E = hematoxylin and eosin.

The white blood cell count was 10,610 cells/μL, with 74.6% neutrophils and 12.4% lymphocytes; the hemoglobin level was 12.6 g/dL, and the platelet count was 334,000 cells/μL. The serum creatinine value was 1.3 mg/dL, and the alanine aminotransferase value was 13 U/L (reference range, 0–41 U/L). The C-reactive protein level was 4.4 mg/dL. The NT-proB–type natriuretic peptide level was 11,091 pg/mL. There was no elevation of other cardiac enzymes. A chest radiograph showed a massive pleural effusion and cephalization of the pulmonary veins at the left lower lung. Electrocardiography showed sinus tachycardia without any ST-T change. Echocardiography revealed a small amount of pericardial effusion, diffuse global hypokinesia, and a thickened pericardium (> 5 mm).

Upon admission, the patient received diuretics, nitroglycerin, and bilevel noninvasive positive pressure ventilation for acute decompensated heart failure. The patient underwent diagnostic thoracentesis, and the results suggested an exudate. However, bacterial and fungal cultures and a polymerase chain reaction test for Mycobacteria tuberculosis of pleural effusion were all negative. Cytology revealed no malignant cells. Moreover, tumor markers and screening tests for autoimmune diseases were all negative. Computed tomography (CT) of the chest showed pericardial masses with contrast enhancement. Video-assisted thoracoscopic pericardial biopsy was performed to reveal a well-defined, round pericardial tumor of 3 cm in the greatest diameter. Histopathology reported the presence of sulfur granules with Splendore-Hoeppli phenomenon, along with branching filamentous gram-positive bacteria shown in the biopsy specimen, which confirmed a diagnosis of pericardial actinomycosis with chronic abscess formation (Figure 1B and C). Further tissue culture yielded Aggregatibacter actinomycetemcomitans. Owing to a history of allergy to penicillin, clindamycin 900-mg infusion every 8 hours was prescribed, and the patient was discharged on the 14th day of treatment. The patient declined biopsy of his oral lesion.

A 6-month treatment with clindamycin was planned. During the follow-up period, the patient remained afebrile. After 4-week clindamycin infusion therapy, he was switched to oral clindamycin 450 mg every 6 hours. The CT performed 4 months after initiation of clindamycin treatment showed a reduction in the size of pericardial lesions and normalization of pericardium thickness, with full resolution of his symptoms (Figure 1D–F). The oral lesion also decreased in size after 6-month clindamycin therapy.

DISCUSSION

Actinomycosis is a rare heterogeneous infection and remains a great diagnostic challenge because of its low prevalence and insidious course. The diagnosis of actinomycosis is rarely considered, particularly when it mimics other diseases.³ Confirmation of actinomycosis relies mainly on histopathology and microbiologic identification from a sterile site.⁴ However, isolation and identification of actinomyces occur in only a minority of instances, probably related to prior antibiotic exposure, the inhibitory influence of concurrent or contaminating microorganisms on Actinomyces growth, suboptimal culture environments, or insufficient short-term incubation periods.¹ To improve the yield rate, strict anaerobic processing and anaerobic growth conditions should be used because of its microaerophilic or strict anaerobic character. In addition, tissue from surgical biopsy or pus is the most appropriate specimen, whereas swab specimens should be avoided.⁵ Furthermore, suspicion of actinomycosis should be relayed to the microbiologist and pathologist to ensure appropriate culture environments and extended incubation periods.⁴ Gram staining is usually more sensitive than culture, especially for those with previous antibiotic exposure. Sulfur granules and Splendore-Hoeppli phenomenon are highly suggestive of the diagnosis, but they are not specific and can also be observed in other chronic infections, such as nocardiosis, fungal infection, and even parasitic infection.⁶ Therefore, special staining such as silver staining can provide benefit to differentiate gram-positive filamentous branching bacteria from fungi, cocci, or bacilli.

In our case, the recurrence of symptoms and poor dental hygiene prompted consideration of alternative differential diagnoses, notably actinomycosis. Moreover, the presence of co-isolated A. actinomycetemcomitans, previously known as Actinobacillus actinomycetemcomitans, may provide additional diagnostic clues. Aggregatibacter actinomycetemcomitans was first found in 1912 as a co-isolate with Actinomyces israelii in patients with cervicofacial actinomycosis and has been reported as a co-isolate in a variety of anatomical localizations of actinomycosis.^7–9 The presence of A. actinomycetemcomitans with sulfur granules and coexisting gram-positive rods elicits suspicion for actinomycosis.¹⁰

Cardiac actinomycosis is a rare form of thoracic actinomycosis, with a reported incidence of 1–2%,¹¹ and results from aspiration of organisms from the oropharynx. Pericardial effusion or pericarditis is present in 70% of cases of cardiac actinomycosis.¹² Initially, the disease may be asymptomatic, but it can progress to life-threatening pericarditis or cardiac tamponade.¹³ The diagnosis of cardiac actinomycosis relies primarily on histopathology, as the yield rate of pericardial fluid cultures is relatively low. Fife et al.¹⁴ also demonstrated that dental or periodontal disease could be a potential risk factor for actinomycosis, manifesting in 26% of cases.¹⁴ However, since the most recent review in 1991,¹⁴ only case reports—and few with a literature review¹⁵ of cardiac actinomycosis—have been published, typically characterized by pronounced hemodynamic instability. A literature search was carried out in PubMed (https://pubmed.ncbi.nlm.nih.gov/) and Google Scholar (https://scholar.google.com.tw/) to identify cases of pericardial actinomycosis published from 1991 to 2023. The electronic literature search was updated until October 2023. Only articles in English were included. The following search terms were used: (actinomycosis) OR (actinomyces) AND (pericarditis) OR (pericardial) OR (cardiac). Articles were reviewed in two stages. In the first stage, articles were screened for eligibility by title and abstract. In the second stage, the full text of the eligible articles was reviewed and analyzed. We excluded pediatric cases and those lacking clear documentation of cardiac involvement. In addition, when articles included literature reviews, only information from the primary case series was collected (Table 1).^16–43

Table 1.

Summary of cardiac actinomycosis in the current and previous cases

Source	Origin	Cardiac involvement	Pathogen	Possible risk factors	Reference
Hepatic	Hepatic actinomycosis	Cardiac tamponade	Actinomyces israelii	–	16
	Multiple liver abscess	Purulent pericarditis, cardiac tamponade	Actinomyces spp.	–	17
	Liver abscess	Cardiac tamponade	Actinomyces spp.	–	18
	Liver abscess	Pericardial effusion, cardiac tamponade	A. israelii.	–	19
	Liver abscess with fistula	Pericardial effusion	Actinomyces spp.	Abdominal surgery	20
Thoracic	Pulmonary actinomycosis	Constrictive pericarditis	Actinomyces meyeri	–	21
	Pulmonary actinomycosis	Constrictive pericarditis	Actinomyces spp. with Actinobacillus actinomycetemcomitans	–	22
	Pulmonary actinomycosis	Cardiac tamponade	A. israelii	Pulmonary surgery	23
	Cervicothoracic actinomycosis	Pericarditis	Actinomyces spp.	–	24
	Cutaneous thoracic abscess and pneumonia	Constrictive pericarditis	A. israelii	Very poor oral hygiene	25
	Cardiac actinomycosis	Cardiac tamponade, pericardial tumor	Actinomyces spp.	–	13
	Cardiac actinomycosis	Cardiac tamponade	Actinomyces odontolyticus	Abdominal surgery	26
	Cardiac actinomycosis	Cardiac tamponade, intracardiac mass	Actinomyces spp.	–	27
	Endocarditis	Endocarditis	Actinomyces georgiae	–	28
	Pulmonary actinomycosis	Cardiac tamponade	Actinomyces spp.	–	29
	Pericardial mass	Pericardial thickening	Actinomyces spp.	–	30
	Pulmonary actinomycosis	Cardiac tamponade	A. meyeri	–	31
	Thoracic actinomycosis	Cardiac tamponade	Actinomyces spp.	Poor dental hygiene	32
	Endocarditis	Severe mitral and aortic regurgitation	A. israelii	–	33
	Pericardial effusion	Cardiac tamponade and constrictive pericarditis	A. meyeri	Previous dental restoration	34
	Pericardial infiltration	Constrictive pericarditis	Actinomyces spp.	–	35
	Percutaneous coronary intervention	Epicardial abscess	Actinomyces oris	Percutaneous coronary intervention	36
	Pericardial effusion	Purulent pericarditis, cardiac tamponade	A. odontolyticus	–	37
	Myocardial abscess	Cardiac tamponade	A. israelii, Aggregatibacter actinomycetemcomitans, Fusobacterium nucleatum	Poor dental hygiene	38
Dental	Dentigerous cyst	Cardiac tamponade	A. odontolyticus	Poor endodontic treatments	39
Disseminated	Disseminated	Myocarditis and pericarditis	Actinomyces spp.	–	40
	Cutaneous tract	Right ventricular and pericardial infiltration	Actinomyces spp.	Farmer	41
	Aortic root abscess	Infective endocarditis	Actinomyces neuii	Previous bacterial endocarditis	42
	Bacteremia	Purulent pericarditis, cardiac tamponade	A. odontolyticus	–	43

To date, there is limited research to guide the management of pericardial actinomycosis, especially in terms of treatment duration. However, most physicians prefer a high-dose therapy with an extended treatment duration, with intravenous antibiotic therapy for 2–6 weeks followed by oral antibiotic therapy for 6–12 months.⁵ However, debate regarding the optimal duration of intravenous antibiotics has not reached a definitive conclusion, and an extended course of treatment may not be universally required for all patients.^44,45 Individualized therapeutic modalities should be applied, considering the disease burden, the feasibility of surgery, and the clinical and radiological responses to treatment. In our case, the assessment of treatment response was conducted through follow-up CT and showed a favorable outcome.

CONCLUSION

We present a rare case of cardiac actinomycosis with the co-isolate of A. actinomycetemcomitans. Our case highlights the significance of histopathological analysis and comprehensive physical examination in achieving a timely diagnosis of cardiac actinomycosis. Early detection and prompt treatment are crucial for a favorable prognosis. The coexistence of A. actinomycetemcomitans may serve as an additional clue suggestive of the presence of actinomycosis.