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Unilateral Empyema Caused by Cutibacterium acnes in a Patient With Hepatic Abscess and History of Mastectomy

Introduction. A 74-year-old woman with a past medical history of stage IV invasive ductal carcinoma presented to the emergency department with fatigue and gradually worsening dyspnea during the past 2 months.

History. The patient had undergone partial mastectomy of the right breast with sentinel lymph node biopsy approximately 2 months prior to presentation. Additionally, she complained of severe activity intolerance and endorsed bilateral lower extremity swelling.

On physical examination, the patient appeared dyspneic at rest and was noted to have decreased breath sounds throughout the right lung. Further, she exhibited 3+ bilateral, lower extremity, non-pitting edema. On review of vital signs, the patient was noted to be afebrile, normotensive with a heart rate of 117 beats per minute (normal range: 60 to 100 bpm), and oxygen saturation of 95% on three liters of nasal cannula.

Diagnostic testing. An initial radiography of the chest showed a large right-sided pleural effusion with a mass effect. Bedside ultrasonography of the right lung showed decreased volume with elevation of the right hemidiaphragm. A loculated fluid collection was also seen in the liver. To investigate further, computed tomography (CT) of the abdomen was performed and showed a large cavitary lesion involving the right lobe of the liver with a complex air/fluid collection.

Initial laboratory workup, including complete blood count, showed a decreased leukocyte count of 2.95 x 109/uL and a low erythrocyte count of 3.25 x 109/uL. The patient was indicated for macrocytic anemia with a hemoglobin of 10.6 g/dL on presentation. On further laboratory testing, she was found to be hypoalbuminemic with an albumin level of 2.4 g/dL. She also had an increased lactate dehydrogenase level of 276 unit/L, total serum protein of 5.9 g/dL, and an elevated lactic acid level of 2.7 mmol/L. As a result of her increased oxygen requirement, the patient was transferred to the intensive care unit for close monitoring of her airway. There, she underwent bedside thoracentesis with pleural fluid analysis and cytology followed by chest tube placement.

A pleural fluid analysis yielded a turbid fluid with a lactate dehydrogenase of greater than 2500 unit/L, PH of 7.2, total protein of 3 g/dL, white blood cell count of 7640 u/L, and a glucose of 6 mg/dL. Cytology displayed inflammatory debris, and no malignant cells were seen. However, anaerobic cultures from the pleural fluid grew Cutibacterium acnes (formerly Proprionibacterium acnes).


Figure 1. Initial X-ray of the chest showing a large right-sided pleural effusion with mass effect.

Differential diagnosis. Regarding differential diagnosis, malignant pleural effusion was considered and placed at the top of the differentials list, especially considering that the patient had a personal history of invasive ductal carcinoma of the breast. Additionally, the patient had a history of cardiac disease. Therefore, heart failure-associated transudative pleural effusion was also considered, but ultimately ruled out after assessing the pleural fluid analysis results, which showed an elevated pleural fluid LDH to serum LDH ratio of 9, meeting Light’s criteria for an exudative pleural effusion.

Treatment and management. The patient was started on empiric parenteral antibiotics with vancomycin (1800 mg intravenously [IV] every 12 hours), cefepime (2 g IV every 8 hours), and metronidazole (500 mg IV every 8 hrs) while awaiting cultures.

Her antibiotic regimen was eventually de-escalated by our infectious disease specialist due to confirmed C acnes infection via the anaerobic cultures. The patient was de-escalated to 2 g IV ceftriaxone every 12 hours for 7 days and eventually transitioned to IV ampicillin-sulbactam (1.5 g for 5 days) up until discharge. Regarding the hepatic abscess, the patient received CT-guided aspiration, which grew few gram-positive and gram-negative bacilli. In our view, this postulate was a direct extension of the C acnes from the primary source of infection in the lung pleura.

Outcome and follow-up. Ultimately, the patient responded well to the treatment and no longer required respiratory support. Her oxygen saturation was adequately maintained on room air, and her chest tube output remained minimal towards the end of her hospital course, which prompted removal of her chest tube. The patient was downgraded to a sub-acute rehabilitation facility where she could continue 500 mg of oral amoxicillin-clavulanate for an additional 6 weeks with close follow-up, as per recommendation from our infectious disease specialist

Discussion. Empyema is a condition where there is an accumulation of purulent material in the pleural space. It is most often caused by a direct extension or inoculation of bacteria such as streptococci, staphylococci or pseudomonas aeruginosa into the pleura. Most often, procedures such as thoracotomy, thoracic surgery, or pneumonia are culprits precipitating the formation of this potentially life-threatening infection. However, in this unusual case, we present a patient with breast carcinoma who recently underwent sentinel lymph node biopsy and mastectomy that ultimately developed unilateral right-sided empyema secondary to C acnes. In addition, this patient presented with a concomitant hepatic abscess secondary to this pathogen, which highlights the potential invasiveness and resilience of this bacterium.

Cutibacterium acnes is commonly known as a normal commensal of the oral cavity, genitourinary, gastrointestinal tract and skin. C acne is practically all-pervasive throughout the skin. It is most prevalent in the sebaceous glands and face. Interestingly, the number of organisms in adults with or without manifestation of acne is uncertain1 C acnes is believed to form comedones via hydrolysis of sebum and later secretes enzymes that assist in lysis of comedone walls, forming a nidus for sequelae into acne vulgaris or folliculitis. This commensal organism has proven ability to induce inflammatory response via multiple mechanisms, among which are monocyte activation via nuclear factor kappa B (NFKB),1 Toll-like receptor 2 (TLR-2) mediated monocyte cytokine production,1,2 and through the production of neutrophil chemotactic factor (NCF).2

C acnes has also been reported as the culprit in prosthetic joint infections, cardiovascular devices, breast implants, and cerebrovascular shunts. The mechanism of infection is not quite clear, but the most accepted current mechanism of action is via biofilm formation. It has also been reported that after antiseptic preparation, C acnes can recolonize wound edges within 30 minutes to 2 hours, and it is also thought to persist in the skin's dermis, allowing intraoperative seeding.3 These could be a plausible explanation for the isolation of the normal commensal in the pathogenesis prosthetic joint infections, cerebrovascular shunts, implant devices, and even abscesses.

Although multiple cases of C acnes’ involvement in infection of cerebrovascular shunts and joint prosthesis infections have been previously reported, there are few cases of its involvement in respiratory infections. Indeed, only four cases of C acnes isolated on cultures in the setting of a lung empyema were found upon our PubMed search.4-7 The four cases all involved pulmonary complications with infections caused by C acnes.

The first case described a 50-year-old nonsmoking woman with primary lung adenocarcinoma who developed C acnes infections after multiple thoracentesis procedures.4 The second case involved a 75-year-old man who smoked with chronic pleural effusions and a hydropneumothorax. In this case, C acnes was identified in the exudative fluid status postmedical thoracoscopy and talc pleurodesis due to symptomatic right-sided pleural effusion.5 The third case was a 29-year-old man on immunosuppressive therapy after a cardiac transplant, who developed a lung abscess infected with C acnes.6 The fourth case involved a 57-year-old man with severe chronic obstructive pulmonary disease who also had a lung abscess caused by C acnes.7 While all cases involved lung infections with C acnes and encompassed a prior thoracic intervention, they differed in patient demographics, underlying health conditions, and specific pulmonary complications.

Regarding the treatment of infections caused by C acnes, while there is no established definitive treatment guideline, it appears that a prolonged treatment course with a beta-lactam antibiotic for a duration of 3 to 6 months in addition to a 2 to 6 weeks course of IV therapy is sufficient, especially for surgical site infections8 Other literature presented successful eradication of lung abscess infections caused by C acnes with the use Doxycycline 100 mg twice a day for 21 days and amoxicillin/clavulanic acid 625 mg three times a day for 6 weeks.9 In our case, the patient was treated with parenteral ampicillin/sulbactam while hospitalized up until discharge and then switched to oral amoxicillin/clavulanic acid for an additional 6 weeks. C acnes lung empyema, though still quite uncommon, is something we are beginning to see more of in practice.

In view of all this, it would be reasonable to consider a differential of C acnes infection, especially in a patient who has severe respiratory disease, is immunocompromised, on immunosuppressive regimen, or with a diagnosis of malignancy, and a recent thoracic procedure.

Conclusion. Parapneumonic pleural effusions/empyema caused by C acnes are far less commonly encountered than microorganisms such Staphylococcus aureus, Streptococcus pneumonia, and Haemophilus influenzae. It is of great importance to treat these infections with a prolonged course of IV and oral antibiotics, however it is of more important significance to prevent these infections from occurring in the first place. Common diagnostic and therapeutic procedures such as thoracostomy, thoracotomy, mastectomy, CT-guided lung biopsy, and lymph node biopsy must follow strict sterile technique when performed.
 

References
  1. Propionibacterium acnes. Science Direct. Accessed July 31, 2024. https://www.sciencedirect.com/topics/biochemistry-genetics-and-molecular-biology/propionibacterium-acnes
  2. Grange PA, Raingeaud J, Morelle W, Marcelin AG, Calvez V, Dupin N. Characterization of a Propionibacterium acnes surface protein as a fibrinogen-binding protein. Sci Rep. 2017;7(1):6428. doi: 10.1038/s41598-017-06940-3
  3. Achermann Y, Goldstein EJ, Coenye T, Shirtliff ME. Propionibacterium acnes: from commensal to opportunistic biofilm-associated implant pathogen. Clin Microbiol Rev. 2014;27(3):419-440. doi: 10.1128/CMR.00092-13
  4. de Prost N, Lavolé A, Taillade L, Wislez M, Cadranel J. Gefitinib-associated Propionibacterium acnes pleural empyema. J Thorac Oncol. 2008;3(5):556-557. doi: 10.1097/JTO.0b013e31816e2417
  5. Lawrence H, Moore T, Webb K, Lim WS. Propionibacterium acnes pleural empyema following medical thoracoscopy. Respirol Case Rep. 2017;5(5):e00249. doi: 10.1002/rcr2.249
  6. Veitch D, Abioye A, Morris-Jones S, McGregor A. Propionibacterium acnes as a cause of lung abscess in a cardiac transplant recipient. BMJ Case Rep. 2015;2015:bcr2015212431
  7. Adlakha A, Muppala N. Propionibacterium acnes: an uncommon cause of lung abscess in chronic obstructive pulmonary disease complicated with bullous emphysema. J Osteopath Med. 2022;122(10):493-497. doi: 10.1515/jom-2021-0240
  8. Shiono Y, Ishii K, Nagai S, et al. Delayed Propionibacterium acnes surgical site infections occur only in the presence of an implant. Sci Rep. 2016;6:32758. doi: 10.1038/srep32758
  9. Adlakha A, Muppala N. Propionibacterium acnes: an uncommon cause of lung abscess in chronic obstructive pulmonary disease complicated with bullous emphysema. J Osteopath Med. 2022;122(10):493-497. doi: 10.1515/jom-2021-0240.

AUTHORS:
Preslav Valchev MD1 Jerry Kenmoe MD1 Narjis Batool MD1

AFFILIATION:
1Internal Medicine Residency, McLaren Flint Hospital, Flint, MI

CITATION:
Valchev P, Kenmoe J, Batool N. Unilateral empyema caused by Cutibacterium acnes in a patient with hepatic abscess and history of mastectomy. Consultant. Published online August 7, 2024. doi:10.25270/con.2024.08.000002

Received January 15, 2024. Accepted May 7, 2024.

DISCLOSURES:
The authors report no relevant financial relationships.

ACKNOWLEDGEMENTS:
None.

CORRESPONDENCE:
Preslav Valchev MD, 401 S Ballenger Hwy, Flint, MI 48532 (preslav.valchev@mclaren.org)


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