Lung imaging characteristics in a patient infected with Elizabethkingia miricola following cerebral hemorrhage surgery: A case report

Abstract

BACKGROUND

Elizabethkingia miricola is a non-fermenting gram-negative bacterium, which was first isolated from the condensate of the Russian peace space station in 2003. Most studies on this bacterium have been carried out in the laboratory, and clinical case studies are rare. To date, a total of 6 clinical cases have been reported worldwide.

CASE SUMMARY

We present the first case of postoperative pulmonary infection in a patient with intracerebral hemorrhage due to Elizabethkingia miricola. The imaging characteristics of pulmonary infection were identified and the formulation and selection of the clinical treatment plan for this patient are discussed.

CONCLUSION

Elizabethkingia miricola infection is rare. When pulmonary infection occurs, computed tomography imaging may show diffuse distribution of a ground glass density shadow in both lungs, the air containing bronchial sign in local areas, thickening of bronchial vascular bundle, and pleural effusion.

Key Words: Elizabethkingia miricola; Cerebral hemorrhage surgery; Postoperative pulmonary infection; Imaging features; Case report

Core Tip:Elizabethkingia miricola infection is rarely reported. We report a 54-year-old male with Elizabethkingia miricola infection in the lungs after surgery for cerebral hemorrhage. The clinical symptoms after infection were nonspecific and could not be timely and accurately diagnosed. Therefore, this report focuses on the imaging characteristics of pulmonary Elizabethkingia miricola infection.

INTRODUCTION

Elizabethkingia miricola is a rare non-fermenting gram-negative bacterium, which was first isolated from the condensate water in the Mir space station[1] in 2003. The original name of the bacterium was Chryseobacterium miricola. The model strain was KCTC 12492 (T) = GTC 862 (T). In 2005, the bacterium was classified into the genus Elizabethkingia together with Elizabethkingia meningoseptica. The bacterium rarely causes clinical infection[2], which was reported in laboratory research. To date, there have only been 6 clinical cases of this bacterial infection worldwide. These clinical reports mainly show that the bacterium can cause bacteremia and sepsis. In addition, infection by this bacterium has also been found in patients with cystic fibrosis and alcoholic pancreatitis. We report the first case of Elizabethkingia miricola infection in a patient who underwent surgery for cerebral hemorrhage. We discuss the imaging characteristics after infection and the disease development and treatment process, in order to provide a reference for the early detection and identification of the bacterium in clinical practice.

CASE PRESENTATION

Chief complaints

A 54-year-old male was admitted to the hospital due to sudden headache and left limb weakness for 3 h.

History of present illness

The patient presented with severe swelling and pain, accompanied by weakness in the left limb, unstable walking, and nausea and vomiting once before admission without any obvious cause.

History of past illness

The patient had a history of hypertension for 1 year, but did not take antihypertensive drugs or monitor his blood pressure regularly.

Personal and family history

The patient had a history of occasional smoking and drinking, and his family members had no history of cerebral hemorrhage.

Physical examination

On admission, the patient was lethargic and had difficulty opening his eyes. The Glasgow Coma Scale score was 13 points, the National Institute of Health Stroke Scale score was 17 points, and the left limb muscle strength was grade 0.

Laboratory examinations

Routine blood tests, liver and kidney function, and coagulation tests showed no significant abnormalities.

Imaging examinations

After admission, he underwent head computed tomography (CT) in the emergency department (Figure 1A). Right basal ganglia hemorrhage was observed, and the amount of bleeding was approximately 60 mL.

Figure 1 Computed tomography results. A: Preoperative computed tomography (CT) findings. The hemorrhage was in the right basal ganglia, with a volume of approximately 60 mL. The brain tissue was pushed to the left, and the midline was obviously deviated to the left; B: Postoperative CT findings. The intracranial hematoma was basically cleared after surgery, and there was no obvious deviation in the midline, resulting in intracranial decompression; C and D: Before pulmonary infection with Elizabethkingia miricola, the lungs were in good condition at the time of admission to the emergency department and on the first day after surgery, without obvious inflammatory signs; E and F: Following pulmonary infection with Elizabethkingia miricola, lung CT showed diffuse distribution of a ground glass density shadow in both lungs, the air containing bronchial sign in local areas, thickening of bronchial vascular bundles in both lungs, and pulmonary edema.

FINAL DIAGNOSIS

Right basal ganglia hemorrhage and hypertension.

TREATMENT

On the day of admission, evacuation of intracerebral hematoma by craniotomy was performed in the emergency department, and the outcome of this procedure was considered satisfactory. The following day, a head CT scan showed that the hematoma was basically cleared (Figure 1B), which resulted in reduced intracranial pressure. The day after surgery, the patient was found to be unconscious, but the sting stimulus induced eye opening. An emergency chest CT (Figure 1C) and a subsequent chest CT re-examination (Figure 1D) showed that the lungs were in good condition. Mannitol and sedation were administered routinely. A small amount of gram-negative bacteria was found in the sputum smear, and ceftizoxime sodium 2 g q8h intravenous drip was given to prevent infection. On the third day after surgery, chest CT re-examination showed a small amount of bilateral pleural effusion with poor air content in adjacent lung tissues. White blood cell count was 16.6 × 10⁹/L and neutrophil percentage was 87.9%, and a small amount of Klebsiella oxytoca were found in the sputum culture. Bacterial infection was considered, the previous antibiotic treatment was continued, and a tracheotomy was performed on the fifth day after surgery. During this period, acid fast staining of the Mycobacterium tuberculosis smear was performed; however, no acid fast bacteria were found. Thus, tuberculous infection was excluded. No fungi were observed in the fungal smear after staining, and fungal infection was excluded. On the ninth day after surgery, procalcitonin and interleukin-6 levels were higher than the normal level due to decreased blood oxygen saturation. Aggravation of pulmonary infection was considered, and the treatment plan was adjusted to piperacillin sulbactam anti-infection treatment, and purulent airway secretions were removed by fiberoptic bronchoscopy on the 10^th d after surgery. Two days later, chest CT showed that a ground glass density shadow was diffusely distributed in both lungs, the air containing bronchial sign was seen in local areas, and the trachea and vascular bundle of both pulmonary bronchi were thickened. Considering that the inflammatory changes were obvious, accompanied by pulmonary edema (Figure 1E), and sputum culture on the 13th day after surgery showed infection with Staphylococcus haemolyticus, the treatment scheme was adjusted to oral linezolid 600 mg q12h + cefoperazone sodium sulbactam sodium injection 3 g q8h intravenous drip combined with anti-infection treatment. The results of 19ncov RNA detected by real-time polymerase chain reaction were negative, and coronavirus disease 2019 was eliminated. Chest CT re-examination on the 16^th d after surgery showed that the ground glass density shadow was diffusely distributed, the air containing bronchial sign was seen in the local area, and the bronchial vascular bundles of both lungs were thickened. Considering these inflammatory changes, pulmonary edema was not excluded, and there was no significant improvement compared with the previous CT scan findings (Figure 1F). The sputum culture showed that there were more Klebsiella spp., and the blood culture (aerobic + anaerobic) results showed no bacterial growth and elimination of bacteremia. The treatment regimen was adjusted to oral linezolid 600 mg q12h + meropenem 1 g q8h intravenous drip combined with anti-infection treatment. High throughput sequencing technology was used to analyze the nucleic acid sequence of microorganisms in the lung lavage fluid 20 d after surgery. Elizabethkingia miricola was detected. The DNA detection results showed that the total length of the genome was 46062 (BP), the coverage was 1.0839%, the average depth was 1.03 × (Figure 2A), the type was g-, the number of genus sequences was 1183, the relative abundance was 38.28%, and the number of species sequences was 708. The RNA detection results showed that the total length of the genome was 7301 (BP), the coverage was 0.1718%, the average depth was 1.36 ×, the type was g-, the number of genus sequences was 166, the relative abundance was 28.77%, and the sequence number of species was 47 (Figure 2B). Drug sensitivity testing showed that the patient was sensitive to quinolone antibiotics and moxifloxacin was administered. As the patient's condition was severe, he developed respiratory failure 22 d after surgery, and his family members did not permit further treatment.

Figure 2 Sequence analysis of microbial nucleic acid in alveolar lavage fluid using high-throughput sequencing technology.Elizabethkingia miricola was detected. A: The results of RNA detection showed that the total length of the bacterial genome was 7301 (BP), the coverage was 0.1718%, and the average depth was 1.36 ×; B: The results of DNA detection showed that the total length of the bacterial genome was 46062 (BP), the coverage was 1.0839%, and the average depth was 1.03 ×.

OUTCOME AND FOLLOW-UP

The patient died on the second day after discharge during telephone follow-up.

DISCUSSION

Elizabethkingia miricola rarely causes human disease. In previous studies, only 6 cases have been reported. The first clinical case of human disease caused by this bacterium was a mantle cell lymphoma patient who received allogeneic stem cell transplantation and chemotherapy and required ventilator support[3]. In 2008, the bacterium was isolated from the sputum and blood of the patient by the clinical center of the National Institutes of Health. Since then, five clinical cases of infection caused by this bacterium have been reported. In 2015, a young woman hospitalized due to alcoholic pancreatitis was reported to be infected with Elizabethkingia miricola[4] following blood sampling. In 2016, a clinical case of pulmonary abscess caused by this bacterium was reported[5]. In 2017, a patient with urinary tract infection was reported and Elizabethkingia miricola[6] was isolated from the urine sample. In 2018, it was reported that the bacterium was isolated from the blood of one patient with diffuse large B-cell lymphoma and the sputum sample of one patient with cystic fibrosis[7,8]. The clinical characteristics, possible etiology and prognosis of these cases are summarized in Table 1.

Table 1 Clinical characteristics, etiology and prognosis of this case and previous cases.

Case number	Clinical features	Etiology	Prognosis	Ref.
Previous case 1	Hemoptysis, dyspnea, persistent fever, pulmonary CT showed diffuse infiltration	Respiratory tract infection and bacteremia caused by severe immune dysfunction after stem cell transplantation and chemotherapy	Death	Green et al[3]
Previous case 2	Abdominal pain, fever, respiratory distress, pulmonary CT showed atelectasis, abdominal CT showed hemorrhage	Chronic liver disease and alcohol abuse, bacteremia	Survived	Rossati et al[4]
Previous case 3	Dry cough, fever, dyspnea, chest CT findings: pulmonary abscess and pleural effusion	Pulmonary infection caused by bacteria	Survived	Gonzalez et al[5]
Previous case 4	Dysuria, oliguria, fever, abdominal pain	Urinary tract infection caused by bacteria	Survived	Gupta et al[6]
Previous case 5	Fever, neutropenia	Decreased immunity and bacteremia after chemotherapy	Survived	Lin et al[7]
Previous case 6	Cough, expectoration, shortness of breath, wheezing, decreased lung function	Long-term oral administration of glucocorticoids reduced immunity	Survived	Frost et al[8]
This case	Decreased consciousness, fever, decreased blood oxygen saturation, systemic multiple organ function injury and stressed state. CT showed diffuse distribution of a ground glass density shadow with pulmonary edema in both lungs	Complications after cerebral hemorrhage	Died

CT: Computed tomography.

The case in the current report is the first case of postoperative infection with Elizabethkingia miricola in the world. It is also the seventh report of human disease caused by Elizabethkingia miricola to date. This report mainly discusses the imaging characteristics and changes in this patient with pulmonary infection due to Elizabethkingia miricola, and discusses the selection of strategies and schemes during his treatment.

The CT scans of this patient showed that during pulmonary infection, the imaging features included diffuse distribution of a ground glass density shadow in both lungs, the air containing bronchial sign in local areas, thickening of bronchial vascular bundle in both lungs, and pleural effusion. Here we needed to distinguish Elizabethkingia miricola infection from the following diseases: (1) New type coronavirus infectious pneumonia: The CT imaging features of new coronavirus infectious pneumonia are in the early stage, multiple small patchy shadows or ground glass shadows, and infiltrating shadows in both lungs can be seen in the peripheral distribution of the lung. For severe and critical patients, lung consolidation shadows can be seen, which are generally not accompanied by pleural effusion. The differential diagnosis is based on the results of nucleic acid detection; (2) mycoplasma pneumonia: This disease is characterized by ground glass, lobular core nodules, and airway wall thickening is often seen. Generally, it can be identified in combination with a positive immunoglobulin M laboratory examination; and (3) Pneumocystis pneumoniae pneumonia: The CT imaging manifestations in these patients are ground glass with interlobular septal thickening, and most of them are "empty" under the pleura. A detailed history should be obtained for these patients, and timely use of high-throughput sequencing technology to analyze the nucleic acid sequence of microorganisms in the alveolar lavage fluid should be performed to help identification and treatment.

There were some problems during the treatment of this case which are worth noting: (1) Early identification: In the early stage of pulmonary infection, the CT imaging features of this patient were not fully displayed, and the sputum smear and sputum culture failed to detect Elizabethkingia miricola, which led to the failure of early diagnosis; thus, the administration of ceftizoxime sodium anti-infection treatment was ineffective. At present, there are few reported clinical cases of Elizabethkingia miricola infection, and there is still no unified reference standard for its imaging characteristics and clinical manifestations. Therefore, our findings may provide a new reference for the early identification of possible infection by this bacterium, combined with the imaging characteristics of the patient, and establish an early understanding of the disease and related microbial verification sequence detection, early detection and early treatment; (2) drug selection: Previous studies showed that the strain was sensitive to levofloxacin, ciprofloxacin and other quinolones, but the report of a patient with urinary tract infection caused by Elizabethkingia miricola showed that the strain was resistant to levofloxacin and ciprofloxacin, but sensitive to gentamicin, ceftriaxone and piperacillin tazobactam. Therefore, the choice of empirical quinolones for treatment in the early stage is still controversial. During treatment, our patient was given antibiotics including ceftizoxime sodium, linezolid, cefoperazone sodium, sulbactam sodium, meropenem and so on, but was not treated with quinolones. Therefore, the patient's infection could not be controlled in time, and he eventually died of lung infection; (3) susceptible populations and conditions of the bacterium: In previous studies, patients who used glucocorticoids for long periods were more likely to become infected with Elizabethkingia miricola. In addition, it was also reported that cancer patients and patients with low immunity were more likely to be infected with the bacterium. In this case report, the patient underwent surgery for cerebral hemorrhage, and then developed coma, limb dysfunction, and multiple organ function damage and a stressed state. These factors may have led to infection with Elizabethkingia miricola more easily and eventually caused disease. However, it is worth mentioning that cerebral hemorrhage in young patients may be related to blood system diseases[9]. Although the patient in this case study was young, no blood diseases related to cerebral hemorrhage were found, and cerebral hemorrhage caused by hypertension was considered; (4) previous studies showed that bacteria were mostly isolated from the patient's blood and sputum. In this case report, Elizabethkingia miricola was not found in the early sputum smear, sputum culture and blood culture. The bacterium was found by high-throughput sequencing analysis of the microbial nucleic acid in alveolar lavage fluid. Therefore, according to the imaging characteristics of pulmonary infection treatment with cephalosporin antibiotics was ineffective. With regard to sputum culture in the case of failure to find pathogenic bacteria in blood culture, it is suggested that microbial nucleic acid sequence detection can be carried out on sputum and blood samples at an early stage to aid early diagnosis and treatment; and (5) limitations: This case report has some limitations; for example, although the imaging manifestations of patients with pulmonary infection are obvious, they still lack characteristics or a gold standard for identification, and are not representative enough. These manifestations cannot be identified completely by imaging features, and need to be combined with genetic detection technology to make a clear diagnosis. The reason for this is that there are fewer relevant cases that can be referred to at present, and there is still a lack of summable imaging manifestations, which needs to be further explored in a follow-up study. In addition, this patient developed systemic multiple organ failure following cerebral hemorrhage surgery. These factors affect each other, and the causal relationship between cerebral hemorrhage and pulmonary infection cannot be completely elucidated. Although close attention has been paid to pulmonary CT and oxygen saturation in this case, this may be subjective and lacks continuous and complete monitoring data of pulmonary function indicators. The above deficiencies need to be improved in future research.

CONCLUSION

Elizabethkingia miricola infection is relatively rare. When it leads to pulmonary infection, it has the CT imaging characteristics of diffuse distribution of a ground glass density shadow in both lungs, the air containing bronchial sign in local areas, thickening of bronchial vascular bundle in both lungs, pleural effusion and so on, but needs to be differentiated from new coronavirus pneumonia. When possible Elizabethkingia miricola infection is indicated, early empirical use of quinolones may be effective in patients. In addition, it is suggested that microbial nucleic acid sequence analysis and other techniques should be used for early diagnosis and identification.

In the future, with continuous research on infection by Elizabethkingia spp., early detection and drug treatment of this new pathogen will be improved. Further research should include a comparison of the therapeutic effect of combined antibiotic therapy and single antibiotic therapy, early detection and identification of the pathogen using high-throughput sequencing technology, and various new technologies that are currently being developed. For example, the use of gene sequence targeted therapy for the bacterium, artificial intelligence detection methods and other directions may become the research focus and direction in the future.