Pyopneumothorax caused by Parvimonas micra and Prevotella oralis: a case report

Parvimonas is a group of Gram-positive bacteria that are common anaerobic cocci in the oral cavity and the gastrointestinal tract and one of the pathogens of periodontitis,[1] and Prevotella is a group of Gram-negative anaerobic bacteria that are found mainly in the oral cavity and intestinal tract and are mainly involved in periodontal infections.[2] In immunocompromised patients, the abovementioned pathogens can cause infections in sites other than the oral cavity, such as bloodstream infections,[3] infective endocarditis,[4] liver abscesses,[5] meningitis,[6] and iliopsoas abscesses.[7] Because of the atypical presentation and the difficulty of culture, it is often difficult to identify these pathogenic bacteria in a timely manner in clinical practice.[8] Here, we report a case of severe pneumothorax caused by a co-infection with Parvimonas micra and Prevotella oralis.

CASE

On June 19, 2022, a 59-year-old male patient presented to the Emergency Center of Beijing Chao-Yang Hospital, Capital Medical University, complaining of right chest pain and dyspnea, with a temperature of 36.9 °C, heart rate of 145 beats per minute, breathing of 38 breaths per minute, and blood pressure of 130/73 mmHg (1 mmHg=0.133 kPa). The patient was a long-term alcoholic (equivalent to alcohol 250 g/d for more than 40 years) but was not drunk when he had chest pain. Nine days before admission, he had intermittent right chest sharp pain, accompanied by coughing and producing yellow mucous sputum; four days ago, the right chest pain worsened, accompanied by dyspnea, and the volume of the coughed-up sputum increased significantly; and one day ago, the patient’s chest pain continued to be unrelieved, dyspnea progressively worsened, and he was referred to our emergency department. Chest computed tomography (CT) revealed right pleural enveloping effusion with infection and double lung inflammation (Figure 1A). The results of laboratory tests were as follows: white blood cell (WBC) count 11.8×10⁹/L, C-reactive protein (CRP) 209.8 mg/L, procalcitonin (PCT) 4.71 ng/mL, and partial pressure of blood oxygen (PO₂) 71 mmHg (oxygen concentration: 60%). Meropenem combined with vancomycin was given for anti-infection and closed drainage of the right side of the chest cavity was performed; the drainage pus was yellow-green purulent pleural fluid with a foul odor. A repeat chest CT demonstrated that the right lung had reopened, and the left lung infection was more progressive than before (Figure 1B). The pus culture and the sputum culture were negative repeatedly. The results of next-generation sequencing (NGS) of purulent pleural fluid on the 5^th day after admission suggested Peptostreptococcus (6.25%), Clostridiales Family XIII. Incertae Sedis (4.80%), Slackia (4.34%), Prevotella (21.49%), Parvimonas (36.33%), of which Parvimonas micra (36.33%) and Prevotella oralis (17.23%) dominated, with 12 probable normal flora (14.86%), with no Mycobacteria, no Mycoplasma/Chlamydia/Rickettsia, no Fungi, no DNA viruses, and no Parasites, so metronidazole was added for anti-infection. The dentistry consultation confirmed the presence of chronic periodontitis, poor oral hygiene, tartar (++), and a large amount of plaque and soft tartar. On the 7^th day after admission, he developed fever with a temperature of 37.8 °C; the blood cultures was negative, and the sputum culture suggested Candida albicans, and fluconazole antifungal treatment was added. On the 8^th day post admission, the body temperature returned to normal, sputum culture suggested pan-resistant Acinetobacter baumannii and Candida albicans, and tigecycline and sulfonamide anti-infection treatment was added. On the 11^th day post admission, sputum culture suggested pan-resistant Acinetobacter baumannii, pan-resistant Klebsiella pneumoniae, and Candida albicans; chest X-ray showed that the left lung infection did not improve, and the WBC count further increased to 29.1×10⁹/L. Therefore, the anti-infective regimen was modified to inclue cefoperazone sulbactam, linezolid, amikacin, and fluconazole, after which the patient’s infection index gradually decreased, and the follow-up chest CT showed improvement (Figure 1C). The patient received effective respiratory support and nutritional support during hospitalization and discharged after the improvement of his general condition.

Figure 1.

Comparison of chest computed tomography before and after treatment: A: before treatment, right pleural enveloping effusion with infection and double lungs inflammation; B: after chest drainage, right effusion decreased, right lung reopened, left lung progressed compared to before; C: after treatment, right effusion and pneumonia improved significantly, left lung infection improved compared to before.

DISCUSSION

Here, we report a case of pyopneumothorax caused by anaerobic bacteria associated with periodontitis. As the lung is an oxygen-rich organ, anaerobic bacteria-related infections rarely occur, and the pulmonary environment is unsuitable for the growth and reproduction of anaerobic bacteria such as Parvimonas micra and Prevotella oralis. Thus far, there have been very few reports of pneumonia caused by Parvimonas micra,[9] and this patient had a co-infection of Parvimonas micra and Prevotella oralis causing pyopneumothorax combined with severe pneumonia, which is rare.

Parvimonas micra is a normal flora of the digestive system, genitourinary system, and skin, but is not a dominant bacterium in an aerobic environment, and it is prone to causing periodontitis in poor oral conditions.[1] There have been several cases of abdominal infection,[10] intervertebral discitis,[11] lumbar muscle infection,[7] intracranial infection,[10] and bloodstream infection[3] associated with Parvimonas micra, but there are few reported cases of severe pneumonia caused by it. There has been only one case of a 35-year-old female with cerebral hemorrhage, in which the sputum culture was negative several times, and an NGS examination of the bronchoalveolar lavage fluid revealed that the pathogen causing pneumonia was Parvimonas micra.[9] The lack of specific symptoms of infection of Parvimonas micra and the relative difficulty of the microbial culture lead to a delay in the identification of the pathogenic bacteria and the adjustment of the anti-infective treatment. The application of NGS technology can be used clinically as a supplementary means of pathogenic bacteria culture,[12] particularly in the case of anaerobic bacterial infections with a low culture positivity rate. In addition, some of the lung abscesses formed by Parvimonas micra are difficult to distinguish from lung cancer in radiology, and the use of NGS technology can clarify the disease diagnosis rapidly.[13] Parvimonas micra is sensitive to carbapenem, metronidazole, penicillin, vancomycin, and linezolid.[14] The previous case reports were mostly of elderly patients or patients undergoing surgery and cancer treatment, suggesting that immune insufficiency and postoperative stress may be the risk factors for a Parvimonas micra infection. However, our patient had no history of immune insufficiency or cancer, long-term alcohol abuse and poor oral hygiene as risk factors for this infection are considered.

Prevotella oralis is mainly found in the oral cavity and the intestinal tract, particularly in the gingival crevices.[2] In addition to oral and periodontal infections, bloodstream infections,[5,15] neck abscesses,[16] liver abscesses,[5] meningitis,[6] and breast abscesses[17] have been reported in patients with diabetes, post-surgical procedures, and immunosuppression. Prevotella oralis is an anaerobic bacterium with a low positive microbiological culture rate, and NGS can significantly increase the positive rate of this bacterium.[18] The bacterium may be resistant to penicillin and clindamycin, with a documented resistance rate of 77% to penicillin and 31%–43.5% to clindamycin, and has high sensitivity to carbapenem antibiotics.[5]

Patients with anaerobic infections are highly susceptible to secondary infections with other bacteria, with most studies reporting that less than 50% of anaerobic infections alone and more than half of anaerobic infections are mixed[19] The British Thoracic Society, in its 2010 Guidelines for the Management of Pleural Disease,[20] stated that 65% of the community-acquired pleural infections had Gram-positive aerobic microorganisms as the causative agent, and 12%–34% of patients had anaerobic infections. However, with the development of anaerobic detection methods and isolation techniques, researchers have found that anaerobes are present in up to 76% of cases, and in approximately 14% of patients, anaerobes may be the only pathogen found.

In our case, the NGS was positive for anaerobic bacteria on the 5^th day after admission, and then we added anti-anaerobic bacteria treatment according to the results and the patient’s condition showed remission. However, fever developed on the 7^th day, which, combined with the patient’s long-term alcohol abuse and treatment with carbapenems advanced antibiotics in the pre-course of the disease, suggested the occurrence of nosocomial infection, and the pathogen, in this case, was pan-drug resistant Acinetobacter. Acinetobacter is capable of accumulating multiple antibiotic resistance genes, resulting in multi-drug resistant or pan-drug resistant strains,[21] and the mechanisms of resistance often expressed by hospital-based strains of Acinetobacter include the acquisition of β-lactamases,[22] altered cell wall channels, and efflux pumps,[23] which may be the mechanism for the development of Acinetobacter infections in such patients.

There are some limitations of our case report. First, we did not find Parvimonas micra and Prevotella oralis in the blood, sputum, or pus cultures. Second, because of the high cost, we did not perform NGS testing on the oral cavity to further clarify the homology of the pyopneumothorax pathogens, nor did we send the sputum or the bronchoalveolar lavage fluid for NGS after treatment to clarify whether Parvimonas micra and Prevotella oralis were eradicated after treatment.

CONCLUSION

The clinical manuifestations of anaerobic pneumonia are difficult to distinguish from gernal bacterial pneumonia, prone to abscess formation, sputum or pus foul odor, but the bacterial culture is mostly negative, so identifying the pathogenic organism is the key to treating infections, and NGS allows for a rapid and accurate diagnosis when the bacterial culture results do not match the clinical presentation, and play a guiding role in the rapid response to emergency.