First case of bloodstream infection due to Caulobacter spp. associated with a postoperative meningitis

Abstract

Caulobacter species are aerobic Gram-negative bacilli initially isolated from aquatic environments and are an uncommon cause of human infection. We report a case of bloodstream infection and postoperative meningitis caused by Caulobacter spp. that occurred in a 53-year old woman two weeks after surgery for a breast carcinoma cerebral metastasis. Polymerase chain reaction (PCR) amplification and sequencing of the 16 S ribosomal DNA identified Caulobacter spp. in three blood cultures and two cerebrospinal fluid (CSF) cultures. Based on our susceptibility results, the patient was successfully treated by a 2-week course of iv imipenem followed by a 4-week course of oral trimethoprim-sulfamethoxazole.

Introduction

Caulobacter species are Gram-negative telluric bacilli initially isolated from aquatic environments [1], shower hoses [2] and were first described in 1935 by Henrici and Johnson [3]. So far, there have been few reports involving Caulobacter spp. in human infections, including two post neurosurgical infections [4], [5] and a peritoneal fluid infection in a patient undergoing peritoneal dialysis [6]. We presently report a case of Caulobacter spp. bloodstream infection and meningitis occurring post neurosurgery.

Case report

A 53-year old woman with a medical history of breast carcinoma and cerebral metastasis was admitted to the neurosurgical department on October 2022. Her breast carcinoma had been initially treated in 2016 by chemotherapy with trastuzumab and mastectomy. Subsequent complications included recurrent cerebral metastasis requiring neurosurgery and radiotherapy in 2019 and 2020, which resulted in a cerebral radionecrosis. Two weeks before admission, she underwent a surgical procedure for excision of the radionecrosis lesion and perform a bone cement cranioplasty. On admission, the patient reported a few days of asthenia, anorexia, headache, neck pain and fever. Physical examination showed fever, a normal blood pressure, neck stiffness and a CSF leak from the recent scar. A cerebral computed tomography scan revealed no infectious lesions. A patient’s peripheral blood cell count demonstrated a neutrophilic leukocytosis (12.8 ×10⁹/L) and a C-reactive protein level of 24 mg/L. Analysis of a CSF sample obtained by lumbar puncture showed a meningitis with 330 nucleated cells/mm3 (80% neutrophils), a protein level of 0.48 g/L and a normal level of glycorrhachia. Bacteria were not visualized on Gram stain. Two blood culture bottles were collected before starting an empirical antibiotic therapy with daptomycin and cefepime according to the local protocol for postoperative meningitis.

The initial set of blood cultures remained negative after 5 days. The CSF culture was positive after 96hrs at 35 °C for a strictly aerobic, curved Gram-negative rod (Fig. 1). Proteomic methods by matrix-assisted laser desorption–ionization time-of-flight (MALDI-TOF) mass spectrometry failed to identify the isolate. A PCR amplification and sequencing of a fragment of the 16 S ribosomal DNA gene identified the isolate as Caulobacter spp. (99% sequence identity with Caulobacter spp. 16 S rDNA gene). Susceptibility testing by the E-test method indicated resistance to cefepime and susceptibility to carbapenems and trimethoprim-sulfamethoxazole (Table 1). However, this organism was initially discarded as a likely contaminant and the treatment with cefepime and daptomycin was continued.

Fig. 1.

Gram staining of the Caulobacter spp. isolate.

Table 1.

Antibiotic susceptibility of the Caulobacter spp isolate.

	MIC (µg/ml)	Interpretation
Amoxicillin	12	R
Amoxicillin-clavulanate	1.5	S
Piperacillin- tazobactam	> 256	R
Ceftazidime	> 256	R
Cefepime	> 256	R
Imipenem	0.5	S
Meropenem	0.5	S
Levofloxacin	4	R
Ciprofloxacin	6	R
Trimethoprim-sulfamethoxazole	0.064	S

With this antibiotic treatment, the patient’s symptoms markedly improved. A second CSF sample obtained 9 days after admission showed 170 nucleated cells/mm with 55% neutrophils and grew Caulobacter spp. Meanwhile, the same organism with a similar susceptibility profile was isolated from 3 consecutive peripheral aerobic blood culture bottles taken for persistent fever, respectively 6, 9 and 10 days after admission which grew in 61, 101 and 47 hours. Based on the susceptibility results, the initial antibiotic treatment was switched to iv imipenem (1 g per 8 h).

To exclude alternative sources of bloodstream infection, the implantable venous access port was removed and culture was negative for Caulobacter spp. Control blood cultures obtained after starting imipenem treatment were negative and a transthoracic echocardiography excluded an endocarditis. The patient completed a 14-day course of imipenem followed by a 4-week course of oral trimethoprim-sulfamethoxazole accounting for cranioplasty. A new surgery consisted of foreign body removal and correct the CSF leak was associated and the patient was cured after this treatment.

Discussion

Meningitis caused by Caulobacter spp. has been reported in only two previous cases, including a pediatric patient in 2012 [4] and an adult patient in 2016 [5], both occurring a few days after a neurosurgical procedure. To our knowledge, positive blood cultures with this organism had never been reported so far. We presently describe the first case of Caulobacter spp. bloodstream infection, which was associated with a postoperative meningitis. Two CSF cultures and three blood cultures grew the same organism, and this ruled out the initial hypothesis of a contaminant. These isolates were identified as Caulobacter spp. by 16 S rDNA sequencing after MALDI-TOF mass spectrometry failed to reach a correct identification. This confirms previous reports that 16 S rDNA gene sequencing is necessary to identify this organism. We can notice the initial set of blood cultures remained negative after 5 days then subsequent blood cultures were positive. This is usual in about 75% of bacterial meningitis that have positive blood cultures [7], [8].

Postoperative bacterial and aseptic meningitis cannot be distinguished by clinical manifestations or CSF findings, and this differential diagnosis is therefore mostly based on culture results [9]. In the present case, the Caulobacter spp. isolate from the first CSF sample was initially regarded as a contaminant and therapy with cefepime and daptomycin was empirically continued. It is noteworthy that the patient’s condition markedly improved and the number of CSF polymorphonuclear cells decreased despite the isolate’s resistance to these antibiotics. This discordance between clinical response and in vitro susceptibility of Caulobacter spp. together with the paucisymptomatic presentation of previous meningitis case reports strongly suggests poor virulence of this organism. After blood cultures were detected positive, the antibiotic treatment was adapted to the susceptibility test results and switched to imipenem. All blood cultures taken thereafter were negative.

The mode of contamination and the exact role of Caulobacter spp. in the physiopathology of meningitis is unclear. In the present case, the patient developed signs of meningitis a few days after neurosurgery while a CSF leak had occurred. Meningeal contamination may have been perioperative or, most probably, percutaneous via the surgical scar after postoperative scalp colonization with Caulobacter spp. present in tap water. The patient was allowed to shower and any particular water exposure were identified. It is surprising that the patient developed bloodstream infection with three consecutive positive blood cultures following meningitis. However, alternative sources of bacteremia such as endocarditis and implantable venous access port colonization were ruled out. Our report indicates that, despite its apparent low pathogenicity, Caulobacter spp. can disseminate via the blood from a primary infected site.

Ethical approval

Not applicable

Consent

Written informed consent was obtained from the patient for publication of this casereport and accompanying images. A copy of the written consent is available forreview by the Editor-in-Chief of this journal on request.

Sources of funding

None

CRediT authorship contribution statement

Romain Manchon: Writing – review & editing, Virginie Zarrouk: Writing – review & editing, Véronique Leflon: Reviewing, Gueorgui Iakovlev: Reviewing, Frédéric Bert: Writing – review & editing, Supervision.

Declaration of Competing Interest

None.