Abstract
A 47-year-old Malay man who presented with fever, poor oral intake and loss of weight for 1 month duration. Further work-up revealed evidence of disseminated Salmonella infection that was further complicated with pericardial and pleural empyema. Cultures from pericardial and pleural fluids grew Salmonella species with negative serial blood cultures. Contrast enhanced CT thorax showed pleural effusion with large pericardial effusion. The patient was treated with antibiotics and drainage of pericardial and pleural empyema was done and he was discharged well.
Keywords: pericardial disease, tropical medicine (infectious disease)
Background
Salmonellosis is an important healthcare problem which occurs worldwide especially in places with poor sanitation and monitoring of food processing. This has brought endemics of salmonellosis in many developing countries.1 Southeast Asia region is an area with high prevalence of mainly the Salmonella enterica species and this disease has been difficult to eradicate.2–4 In Malaysia, there have been numerous reports in the prevalence of Salmonella infection due to poor handling and contamination during food processing.2 5 Salmonellosis is often presented with gastroenteritis, enteric fever, bacteraemia, vascular infection and chronic carrier state.6 Clinical presentation of salmonellosis may occur in different ways in humans. Less than 30% of cases presented with extra intestinal Salmonella infections.7Localised infection is frequently seen in Salmonella bacteraemia and usually occurs with enteric fever or gastroenteritis. Both pulmonary and pericardial involvements of Salmonella infection are extremely rare. Empyema commonly occurs in older patients with comorbidities such as diabetes mellitus, malignancy or pulmonary disease.8
In this modern antibiotic era, the prevalence of purulent pericarditis and pleuritis are rare. Based on the literature review pertaining to salmonellosis with purulent pericarditis, only four reported cases have been published so far.9–12 To the best of the researchers’ knowledge, this is the first reported case of salmonellosis involving pericardial and pleural empyema in Malaysia. We herein report the case of disseminated salmonellosis with purulent pericarditis associated with uncontrolled diabetes mellitus.
Case presentation
A 47-year-old man was admitted to the hospital with continuous fever for 1 month, as well as abdominal pain associated with poor oral intake and loss of weight. The patient had a history of type 2 diabetes mellitus and was diagnosed for 10 years and is currently on premixed insulin 28 U twice a day(BD). Acute cholecystitis was diagnosed based on clinical symptoms and ultrasound of hepato-biliary during admission. The patient was diagnosed as septicaemia secondary to acute cholecystitis complicated with left pleural and pericardial effusion. Pleural tapping was done, and pleural fluid culture was found to isolate the Salmonella species. During hospitalisation, the patient had completed 2 weeks of intravenous ceftazidime and subsequently 4 weeks of oral ampicillin sulbactam after being discharged from the hospital. There was no surgical intervention done for his acute cholecystitis and it was treated conservatively via antibiotic. In regards of his pericardial effusion, transthoracic echocardiography was done, and the result revealed global pericardial effusion with no sign and symptoms of cardiac tamponade; hence, no pericardial tapping was done at that time.
A month later, the same patient was admitted to the hospital again due to dyspnoea. He claimed to have on and off fever after his last admission however, he did not seek any medical treatment. Echocardiography, chest X-ray and CT scan of thorax revealed a large amount of pericardial effusion with pericardial thickening and moderate left pleural effusion without pulmonary parenchymal involvement. A chest tube insertion was subsequently performed, and 1-L of pleural fluid mixed with pus was drained. Analysis of pleural fluid revealed cloudy appearance, a protein concentration of 32 g/L and a lactate dehydrogenase level of 406 U/L, consistent with an exudative effusion. The pleural fluid culture and sensitivity were found to isolate the Salmonella species which was susceptible to ampicillin, ceftriaxone, chloramphenicol, ciprofloxacin and trimethoprim–sulfamethoxazole.
Emergency pericardiocentesis was performed, however, the procedure got complicated with an unintentional puncture of the RV. Sternotomy with open pericardial drainage together with removal of catheter were done by a cardiothoracic surgeon in the hospital. Intraoperative finding showed thick pericardium with dense adhesion. Pericardial collection appeared to be cloudy and haemorrhagic was found to be mixed with slough. The catheter was found to be buried inside the RV and then removed; suture done at the puncture site. Tissue and pericardial culture and sensitivity results also showed the presence of Salmonella species isolated with sensitivity pattern like those isolated from the pleural fluids.
Based on the pericardial thickening together with the fibrinous and exudative effusion, the patient was diagnosed with constrictive pericarditis secondary salmonellosis. Post-procedure, the patient recovered well and was discharged from the hospital. Written informed consent was obtained from the patient for the publication of this case report.
Physical examination and investigations
On examination, the patient was tachypneic, toxic looking and in sepsis. His vital signs showed the following; respiratory rate of 24 breaths/min, tachycardia (112 beats/min), blood pressure of 127/68 mm Hg and temperature of 38.2°C. Cardiovascular examination revealed elevated jugular venous pressure with muffle heart sound. There was reduced air entry, dullness to percussion at the left middle to the lower zones, with reduced breath sounds noted in the same area. The abdomen was tense and tender. There was presence of hepatomegaly with liver span of 20 cm. Bilateral pitting oedema was noted up to the level of the knees.
Initial blood investigations revealed an elevated white blood cell count of 12.7×109/L with 46% (1.25×109/L) neutrophils and 30% (0.82×109)/L lymphocytes. C reactive protein was elevated at >200 mg/L. The chest radiograph revealed opacification of the lower two-thirds of the left hemithorax, with the loss of the right costophrenic angle. Underlying lung collapse was also noted (figure 1). Contrast enhanced CT thorax showed pericardial effusion with marked pericardial enhancement, focal area discontinuity of the pericardial space at the inferior part represented fibrinous pericarditis. There was also bilateral pleural effusion with loculated left pleural effusion (figure 2). Focal outpouching area at the aortic arch suggestive of atherosclerotic ulcer likely secondary to infective cause was also noted. Serial transthoracic echocardiogram revealed global pericardial effusion which was progressively worsening along the course of admission with the evidence of RV collapse and clinical sign of cardiac tamponade. Blood, sputum, urine and stool culture did not reveal any growth of any identified pathogen. Serology for melioidosis was also negative.
Figure 1.

Posterio-anterior chest X-ray showed opacification of the lower two-thirds of the left hemithorax, with loss of the right costophrenic angle.
Figure 2.

Contrast-enhanced CT thorax showed bilateral pleural effusion and pericardial effusion with focal area of discontinuity of pericardial space at the inferior part which likely represents fibrinous pericarditis.
Differential diagnosis
Tuberculosis.
Melioidosis.
Lymphoma with secondary bacterial infections.
Severe community acquired pneumonia.
Treatment
Following the sensitivity report, a combination of intravenous and oral antibiotic was given. The patient was discharged with oral ciprofloxacin for a total duration of 4 weeks.
Outcome and follow-up
Repeated echocardiography was planned after the completion of antibiotic. No hospitalisation for similar problem was documented following discharge.
Discussion
Biliary tract especially the liver or gall bladder is the most common extra intestinal sites of salmonella infection. Such patients are usually immuno-compromised or have underlying connective tissue diseases.13 14 In the patient of this study, he was initially admitted with sepsis secondary to acute cholecystitis with pleural and pericardial effusion. Approximately up to 10% of mortality rate in patients with purulent pericarditis and the prognosis will depend on underlying medical comorbidities and severity of pericarditis itself.15
This patient was admitted with pleural and pericardial empyema. Pleural or pericardial effusion or empyema due to Salmonella species is rare.3 Pneumonia, bronchopleural fistula and empyema caused by Salmonella infection occurs in 1%–6% of cases only.16 Saphra et al (1957) (had reported 85 cases of pleural empyema due to Salmonella infection which accounted only 1% of all cases of salmonellosis. Purulent pericarditis per se is a rare complication of Salmonella infection as stated by Doig et al.17.17 In a published literature by Cohen et al (1998), there were 10 cases of non-typhoidal Salmonella pericarditis with 7 of them having positive culture from pericardial fluid during life. Furthermore, Fusun et al 18 reported isolated Salmonella typhimurium from both blood and pericardial fluid culture. In the case of this study, none of the blood culture sent was positive Salmonella culture. Only the pericardial fluid and pleural fluid were positive with the Salmonella species.
The case report of this study was observed and found to be consistent with the previous reported cases, which showed no preceding history of Salmonella infection, whereby the blood and stool cultures were negative.1 Prior reports have shown that only 33% of patients had history of gastrointestinal illness. In majority of cases, only 39% had positive stool culture and 30% had positive blood culture. It can be explained that the Salmonella infection may be dormant in reticulo-endothelial system which will later be reactivated and lead to haematogenous spread. Another explanation is that, due to low bacterial load, blood culture is regularly negative in Salmonella bacteraemia. With the longer duration of illness, the sensitivity detection via blood culture was reported to be significantly reduced.
As the mortality of Salmonella empyema is high, it is important to have early recognition and diagnostic investigation. Aggressive intervention which includes urgent pericardiotomy and early initiation of appropriate antibiotics are associated with higher rate of successful recovery.15 With the background of long standing and poorly controlled type 2 diabetes mellitus, the patient of this study is also known to be associated with decreased immune response that leads to increased rates of infection.10
In conclusion, we herein described an unusual case of disseminated salmonellosis in poorly controlled type 2 diabetes mellitus. As we know, both purulent pleuritis and pericarditis are rarely presented with Salmonella infection.8 It also reflects how diagnosis can be delayed if there is no initial suspicions and lack of important history of gastrointestinal symptoms that could aid the diagnosis. Comorbid conditions play an important role especially in this patient who had a poor diabetic control background. This case report adds further information to the current body of knowledge in disseminated Salmonella infection management.
Learning points.
Disseminated Salmonella infection involving pericardial and pleural empyema is a rare manifestation of the disease.
High degree of suspicion is crucial especially in immunosuppression state patients, although the presentation is not typical.
Early eradiation of the primary source of infection is important in determining the clinical outcome of disseminated Salmonella infection.
The key principles of the management are early diagnosis, control the infection with appropriate antibiotics and adequate drainage.
Footnotes
Contributors: MIJ prepared the manuscript. AMB and WSWG edited and approved the final draft of the manuscript. ZY, AMB and MIJ managed the patient.
Funding: The authors have not declared a specific grant for this research from any funding agency in the public, commercial or not-for-profit sectors.
Competing interests: None declared.
Provenance and peer review: Not commissioned; externally peer reviewed.
Patient consent for publication: Obtained.
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