Rare post-operative intracranial abscess due to Serratia marcescens: what we can learn from it?

Bacterial infections of the central nervous system (CNS) remain to be an important cause of morbidity and mortality after craniotomies. The incidence rate is 1–3%, with Staphylococcus aureus (S. aureus) being the most common pathogen. Serratia marcescens is a gram-negative enteric bacillus that rarely colonizes human hosts. It is widely distributed in hospital environments and is regarded as an opportunistic pathogen that occasionally causes various infections, such as wound infections and pneumonia [1‐4]. Most brain abscesses caused by Serratia marcescens occurred in settings such as intensive care units (ICUs), especially neonatal units (NICUs) [5‐9]. Serratia marcescens, a member of the Enterobacteriaceae, is a well-known pathogen of the respiratory tract, urinary tract, and a common etiology of wound infections, which has raised concerns as a causative pathogen of nosocomial infections [10, 11]. However, Serratia marcescens is a rare pathogen of adult CNS infections [12]. Here, we present a case of brain abscess caused by S. marcescens, with accompanying review of literatures.

A 63-year-old man presented with complaints of right limb weakness over the past 4 months and was brought to the emergency department after a seizure episode. The patient had a 10-year history of unstable angina and underwent skin grafting 5 years prior. There had no recent history of fever, excessive sleepiness, or nuchal rigidity. Neurological and systemic examinations revealed grade 4 + on the right limb on manual muscle testing. Computed tomography (CT) of the brain showed a lesion occupying the left parietal lobe with a mild mass effect and a midline shift. Convex meningioma was presumptively diagnosed based on magnetic resonance imaging (MRI) results (Fig. 1).

On June 1, 2022, the patient underwent left parietal craniotomy with total resection of the tumor. Consistent with Fig. 1B, the lesion exhibited bony erosion of the entire skull during craniotomy (Fig. 2). A histopathological examination of an intra-operative fast frozen section biopsy (Identification number D22-27096; Qingdao, China) demonstrated a meningeal epithelial tumor with mild-moderate cellular atypia and rich vessel supply, predisposed to atypical meningiomas (WHO II-III). It was recommended to wait for a large number of paraffin samples and immunohistochemistry (IHC) results to exclude the possibility of higher-grade lesions. The tumor had invaded the dura mater and skull. We performed an excision of the involved dura mater and skull, reaching a Simon Grade 5 level of resection. Consequently, in the process of cranial closure, we used an artificial dura mater for precise suturing of the dura mater and a titanium mesh to reconstruct the affected areas of the skull. This approach also potentially contributed to the risk of persistent and spreading infection in the patient. We sterilized the titanium mesh rigorously before it was implanted.

However, 8 days after the craniotomy, when all sutures were removed, the wound healed poorly. We changed dressings more frequently and, at the same time, applied vancomycin based on weight and creatinine clearance. Notably, the patient showed no signs of local and systemic infection. Thirteen days after craniotomy, the final histopathological diagnosis (Identification number D22-26985; Qingdao, China) confirmed the diagnosis of angiomatous meningioma, which was defined by hypervascularity, with tumoral blood vessels exceeding 50% of the total volume (WHO I) [13]. The IHC provided the definitive information –Vimentin ( +), SSTR2 ( +), PR ( +), CD34 ( +), STAT6 ( +), GFAP (-), S-100 (-), Olig-2 (-), Ki-67 (+ ,2%) (Fig. 3).

However, when we planned to remove the secondary sutures around the poorly healing wound on June 27, 2022, a copious amount of a thin yellow liquid was squeezed out of the wound. It was then contemplated that titanium implants should be removed immediately after performing another MRI examination. The imaging findings showed an evident light-yellow empyema around the titanium plate (Fig. 4).

We reviewed the postoperative cranial MR on June 28, 2022. Cranial MR suggests postoperative changes in the left frontoparietal tumor, a high likelihood of a left frontal lobe hematoma, and a high likelihood of bilateral parietal subcutaneous hematomas or effusions (Fig. 5).

Surgical repair and debridement were performed by removing the titanium plate and cleaning up the suppurative secretions. Before discharge, five laboratory tests were conducted to identify possible pathogenic microorganisms. The first bacterial culture was obtained from wound discharge and the other three organisms were isolated from soft tissues obtained during the surgical procedure. Only Serratia marcescens was isolated from all four cultures (Fig. 4G), which was identified to be not antibiotic-resistant. On the 10th day after brain debridement, the sutures were removed and the wound healed well (Fig. 6). After the patient was treated with sensitive antibiotics based on the drug susceptibility test results, the condition gradually improved, and he was transferred to a rehabilitation facility.

Herein, we present a unique case of an uncommon occurrence in which a 63-year-old male patient with a mass in the left parietal region developed an intracranial abscess caused by Serratia marcescens following surgery. Through this case, we would like to discuss several problems as follows. When and how to make hair preparation before surgery? How to quickly identify postoperative intracranial infection? We should be wary of Serratia marcescens in neurosurgery clinical work. How to deal with the challenges posed by infection after titanium mesh implantation.

In this case, the patient's preoperative preparation was to shave his head the day before the operation instead of cutting hair. Whether the presence of hair at surgical sites increases the risk of neurosurgical infections remains controversial. Preoperative head shaving improves the visibility of the incision line and reduces postoperative surgical site infections. However, many recent studies have reported that shaving the head can change the normal flora around the surgical area and usually results in minor trauma to the scalp, and both of which increase the risk of neurosurgical infection [14‐25].

NICE guidelines identified that surgeons should opt to use clippers rather than shaving for hair removal [26]. Razors cause microtrauma, facilitating microbial entry and proliferation in incisions. Studies indicate increased SSIs with shaving versus clipping [27, 28]. Interestingly, few studies have evaluated the risk of SSIs between hair clipping and no hair removal. Forensic evidence shows individual-specific bacterial flora in hair, highlighting endogenous flora as a primary SSI source [29‐31]. The necessity and efficacy of hair removal in preventing SSIs are debatable, as are the effectiveness of disinfection methods for unshaved hair and strategies to mitigate clipping-associated risks, such as optimal timing and location of hair removal.

Serratia marcescens is a gram-negative bacterium that has garnered attention due to its association with healthcare-associated infections [10]. Serratia marcescens, commonly found in hospital environments, medical equipment, and on healthcare workers' hands, can infect various clinical samples like sputum, urine, and blood. Although most skin flora are gram-positive bacteria, Serratia marcescens infections have been reported in both healthy and immunocompromised individuals. Serratia marcescens has exhibited increasing resistance to multiple antibiotics, including β-lactams, aminoglycosides, and fluoroquinolones [32‐34]. Its resistance mechanisms mainly include efflux pumps, downregulation or alteration of outer membrane pore proteins, chromosomally encoded antibiotic-modifying enzymes, plasmid-encoded ribosomal methyltransferases, and aminoglycoside-modifying enzymes [32].

Recent studies have focused on understanding the mechanisms of resistance and exploring alternative treatment options [32]. Combination therapies, such as the use of β-lactamase inhibitors in combination with β-lactam antibiotics, have shown efficacy in combating resistant strains [35, 36]. Additionally, research is underway to investigate the potential of novel antimicrobial agents and therapeutic approaches like phage therapy [37, 38]. Genomic analysis of Serratia marcescens provides a comprehensive understanding of its genetic composition, including virulence factors, antibiotic resistance genes, and regulatory networks [39‐41]. It facilitates the identification of potential targets for therapeutic interventions, the development of diagnostic tools, and the implementation of effective strategies for controlling infections caused by this bacterium.

Antibiotics, the behind-the-scenes heroes of modern medicine, are used to treat various infectious diseases. However, several bacteria have become resistant to most currently available antibiotics. Staphylococci and drug-resistant gram-negative bacilli are the most likely causes of post-neurosurgical intracranial infections [42, 43]. The mortality rate of intracranial infections caused by gram-negative bacteria is significantly higher than that caused by other pathogenic bacteria [44]. Drug susceptibility tests indicated that only a few drugs, such as polymyxins and aminoglycosides, were effective against gram-negative bacteria. However, conventional drug delivery routes have low brain penetration rates, making it difficult to achieve effective therapeutic results. Thus, it is suggested to try some new routes of drug delivery such as intrathecal and intracerebroventricular administration [45]. In addition, the optimal antibiotic treatment for S. marcescens CNS infections remains controversial.

Currently, no clinical or preclinical studies demonstrate a direct relationship between the staging of meningiomas and infection. The pathology report after the patient's surgery showed that he had an angiomatous meningioma, which is a type of brain tumor classified as WHO I. Serratia marcescens infection occurred after surgery, possibly due to intraoperative contamination or suboptimal preoperative shaving, and was not significantly associated with the meningioma stage. We don't detect this latent infection very quickly. Therefore, exploring some methods for rapid identification of postoperative intracranial infection is necessary.

Some cytokines can be used as markers to diagnose bacterial infections. Significantly elevated levels of cerebrospinal fluid IL-6, IL-8, and INF-α occur in bacterial intracranial infections. Cerebrospinal fluid (CSF) analysis is currently considered the gold standard for diagnosing intracranial infections, and biomarkers such as CSF lactate, heparin-binding protein, C-reactive protein, and procalcitonin play ancillary roles [46‐49]. With the development of molecular biology, laboratory diagnostic tools have evolved from the cellular to the molecular DNA levels [50, 51]. Pathogenic high-throughput genetic testing enables the rapid detection of disease-causing microorganisms. In addition, diffusion-weighted MR imaging (DWI) and apparent diffusion coefficient (ADC) help distinguish abscesses from other pathologies.

Infection of titanium mesh implants is a common postcranioplasty complication. We analyzed the various causes of titanium implant-associated infections after cranioplasty, such as poor underlying conditions of patients, failure to achieve strict aseptic operation or contamination of the titanium mesh during the procedure, poor local blood supply due to pressure on the scalp caused by a poorly shaped titanium mesh, and local tissue necrosis due to excessive intraoperative hemostasis [52, 53]. Second, cranioplasty requires breakthroughs in materials science, and finding new alternative biomaterials is an urgent clinical requirement. Recent studies revealed that PEEK has the lowest risk of cranioplasty revision and new hydrogel biomaterials show promising antibacterial properties and bone regeneration effects [54‐57]. In this case, the autogenous bone was discarded after the meningioma was found to erode the skull, and a titanium mesh was selected for repair during the craniotomy procedure. However, it is questionable to rashly use allogeneic metal materials for repair when the grade of meningioma is not clear enough.

Serratia marcescens is a rare but significant cause of postoperative brain abscesses, often leading to high mortality despite advanced antibiotics and radiology. This pathogen, not previously reported in adult neurosurgery, poses a significant risk for nosocomial infections. The case and literature review aims to share insights for diagnosing and treating such infections.

Preventive measures include proper hair removal before surgery, monitoring postoperative inflammatory markers, and early diagnostic imaging for delayed wound healing. Effective treatment hinges on selecting appropriate antibiotics based on drug sensitivity and understanding their mechanisms. New therapies, including phage therapy and antibiotic combinations, are promising against this pathogen. Additionally, correct titanium mesh implantation and stringent sterilization are crucial to prevent related infections, with research on infection-resistant materials ongoing. Ultimately, timely removal of artificial materials and abscess resection are key to managing these infections.