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Community-Acquired Listeria monocytogenes Meningitis in Adults

  1. Matthijs C. Brouwer1,
  2. Diederik van de Beek1,
  3. Sebastiaan G. B. Heckenberg1,
  4. Lodewijk Spanjaard2, and
  5. Jan de Gans1
  1. 1Departments of Neurology, Amsterdam, The Netherlands
  2. 2Departments of Medical Microbiology, Center of Infection and Immunity Amsterdam, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
  1. Reprints or correspondence: Dr. Matthijs C. Brouwer, Academic Medical Center, University of Amsterdam, Dept. of Neurology H2, P.O. Box 22660, 1100 DD Amsterdam, The Netherlands (m.c.brouwer{at}amc.uva.nl).
 
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Abstract

Background. Listeria monocytogenes is the third most common cause of bacterial meningitis.

Methods. We prospectively evaluated 30 episodes of community-acquired L. monocytogenes meningitis, confirmed by culture of cerebrospinal fluid specimens, in a nationwide study in The Netherlands. Outcome was graded using the Glasgow outcome score; an unfavorable outcome was defined as a score of 1–4.

Results. We found 30 episodes of L. monocytogenes meningitis. All patients were immunocompromised or >50 years old. In 19 (63%) of 30 patients, symptoms were present for >24 h; in 8 patients (27%), symptoms were present for ⩾4 days. The classic triad of fever, neck stiffness, and change in mental status was present in 13 (43%) of 30 patients. An individual cerebrospinal fluid indicator of bacterial meningitis was present in 23 (77%) of 30 cases. Gram staining of cerebrospinal fluid samples revealed the causative organism in 7 (28%) of 25 cases. The initial antimicrobial therapy was amoxicillin based for 21 (70%) of 30 patients. The coverage of initial antimicrobial therapy was microbiologically inadequate for 9 (30%) of the patients. The mortality rate was 17% (5 of 30), and 8 (27%) of 30 patients experienced an unfavorable outcome. Inadequate initial antimicrobial therapy was not related to outcome.

Conclusions. In contrast with previous reports, we found that patients with meningitis due to L. monocytogenes do not present with atypical clinical features; however, typical cerebrospinal fluid findings predictive for bacterial meningitis might be absent. A high proportion of patients received initial antimicrobial therapy that did not cover L. monocytogenes.

Bacterial meningitis is a serious and life-threatening disease. The estimated incidence is 4–6 cases per 100,000 adults per year in developed countries and is up to 10 times higher in less developed countries [1, 2]. Streptococcus pneumoniae and Neisseria meningitidis are the leading causes of bacterial meningitis in adults and cause 85% of all cases [2, 3]. Listeria monocytogenes is the third most frequent cause of bacterial meningitis [2–5]. This gram-positive bacillus is principally spread by contaminated food, which was discovered after outbreaks of listeriosis in the 1980s [1, 6–9]. In the literature, meningitis due to L. monocytogenes is described as a disease in immunocompromised patients and elderly individuals, with high case-fatality rates (24%–62%) [1, 5, 10–17]; however, all previous data on Listeria meningitis in adults were retrospective. We performed the first prospective nationwide cohort study in adults with community-acquired bacterial meningitis [2]. In this report, we describe the clinical features, complications, treatment, and outcome in adults with bacterial meningitis due to L. monocytogenes in this prospective case series.

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Methods

In the Dutch Meningitis Cohort Study, a nationwide observational cohort study in The Netherlands, 696 episodes of community-acquired acute bacterial meningitis were assessed prospectively. All causative organisms were identified by CSF culture, which yielded S. pneumoniae in 352 episodes (51%), N. meningitidis in 257 (37%), L. monocytogenes in 30 (4%), and other bacteria in 57 (8%). Inclusion and exclusion criteria have been described elsewhere [2]. In summary, eligible patients were >16 years old, had bacterial meningitis confirmed by culture of CSF, and were listed in the database of The Netherlands Reference Laboratory for Bacterial Meningitis from October 1998 to April 2002. This laboratory provided daily updates of the names of hospitals where patients with bacterial meningitis had been admitted 2–6 days previously. The start of the cohort study was announced in the journal of the Dutch Neurological Society, with periodic reminders. Before the study started, all neurologists received information by mail about the study, including a case record form. For each patient, the treating physician was contacted, and informed consent was obtained from all participating patients or their legally authorized representatives. The Dutch Meningitis Cohort Study was approved by the ethics committee of the Academic Medical Center, University of Amsterdam (Amsterdam, The Netherlands).

Data registration was started at the time of inclusion. The study was undertaken in accordance with Dutch privacy legislation, and information was obtained via a case-record form. Patients receiving immunosuppressive drugs and patients with diabetes mellitus, alcoholism, asplenia, liver cirrhosis, end-stage renal disease, or HIV infection were judged to be immunocompromised. Persisting fever was defined as a body temperature of ⩾38°C for >10 days after the start of appropriate antimicrobial treatment. Recurrent fever was defined as fever reoccurring after at least 1 afebrile day. Hyponatremia was defined as a plasma sodium concentration <135 mmol/L. Patients underwent a neurological examination at discharge, and outcome was graded with the Glasgow outcome scale. This measurement scale is well validated, with scores varying from 1 (death) to 5 (good recovery). A favorable outcome was defined as a score of 5, and an unfavorable outcome was defined as a score of 1–4. Focal neurological abnormalities were divided into focal cerebral deficits (aphasia, monoparesis, or hemiparesis) and cranial nerve palsies. Causes of death were independently classified by 2 investigators (M.C.B. and D.v.d.B.) in 2 categories on the basis of criteria described in previous studies [18, 19]. These 2 categories were: (1) systemic causes, including septic shock, respiratory failure, multiorgan dysfunction, and cardiac ischemia; and (2) neurological causes, including brain herniation, cerebrovascular complications, intractable seizures, and withdrawal of care because of poor neurological prognosis. There were no differences in classification between clinicians.

The Mann-Whitney U test was used to identify differences between groups with respect to continuous variables, and dichotomous variables were compared with use of the χ2 test. All statistical tests were 2-tailed, and a P value of <.05 was regarded as significant. Analyses were undertaken with SPSS software, version 12.0.1 (SPSS).

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Results

In a 3.5-year period, 30 episodes of community-acquired L. monocytogenes meningitis were identified in 30 patients (table 1). The calculated annual incidence was 0.07 cases per 100,000 adults. There was no seasonal pattern of occurrence of L. monocytogenes meningitis, although 5 (50%) of 10 episodes in immunocompetent patients occurred during the summer. Predisposing conditions were present in 21 (70%) of 30 patients; 20 (67%) of 30 patients were considered to be immunocompromised, and 1 patient had sinusitis (3%). All patients who were characterized as immunocompetent were >50 years old (table 2). A previous episode of meningitis had occurred in 1 patient (3%). In 19 (63%) of 30 patients, symptoms were present for >24 h; in 8 (27%), symptoms were present for ⩾4 days.

Table 1
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Table 1

Clinical and laboratory characteristics at admission to the hospital for 30 adults with community-acquired Listeria monocytogenes meningitis.

Table 2
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Table 2

Demographic and clinical characteristics of immunocompetent patients with Listeria monocytogenes meningitis.

Classic symptoms and signs were present in most of the patients. The classic triad of neck stiffness, fever, and altered mental status was found in 13 (43%) of 30 patients. At least 2 of 4 symptoms and signs (classic triad plus headache) were present in 29 (97%) of the patients. One patient had a rash that was characterized as ecchymosis.

CT of the brain was performed at admission for 23 (77%) of 30 patients; the results were normal for 18 patients. Abnormalities were recorded for 5 patients (27%). Cerebral edema was present in 2 patients (9%), evidence of recent infarction was present in 1 patient (5%), lesions possibly indicating an infarction at an earlier date were present in 1 patient (5%), and atrophy was present in 2 patients (9%). Cranial CT was performed before lumbar puncture for 16 (70%) of the 23 patients; therapy was started before CT for only 5 (31%) of the patients. MRI of the brain was performed for 1 patient and revealed no abnormalities.

Lumbar puncture was performed for all patients. Opening pressure was recorded with a water-manometer for 8 (27%) of 30 patients; median pressure was 275 mm of water (range, 150–400 mm of water), and 5 patients had very high pressure (>250 mm of water). At least 1 individual CSF finding indicative of bacterial meningitis (glucose concentration, <1.9 mmol/L; ratio of CSF glucose to blood glucose, <0.23; protein concentration, >2.20 g/L; WBC count, >2000 cells/mL; or CSF neutrophil count, 1180 cells/mL [20]) was found for 23 (77%) of 30 patients. There was no relation between low CSF leukocyte count and age or immunocompetence. Gram staining of CSF samples was performed for 25 (83%) of 30 patients and revealed no microorganisms in 16 (64%), gram-positive rods in 7 (28%), and gram-negative bacteria in 2 (8%).

Initial antimicrobial treatment consisted of penicillin or amoxicillin for 9 (30%) of 30 patients, a third-generation cephalosporin for 5 (17%), and a combination of amoxicillin and a third-generation cephalosporin for 8 (27%); other regimens were used for 8 patients (27%). In 21 episodes (70%), the initial therapy included penicillin or amoxicillin; a combination with aminoglycosids was given in 7 (23%) of the episodes. Nine (30%) of 30 patients received inappropriate initial antimicrobial therapy. Among these patients, the median time from admission to the hospital to receipt of adequate therapy was 3 days (range, 1–5 days). Adjunctive steroids were given in 5 episodes (17%); however, 3 patients had already used prednisone before admission to the hospital, and 1 patient received dexamethasone as treatment for an exacerbation of chronic obstructive pulmonary disease. In 1 additional patient, dexamethasone therapy was started after the patient experienced clinical deterioration.

Complications developed in a high proportion of patients (table 3). Persisting fever was present in 11 (37%) of 30 patients. Subsequent lumbar punctures were performed for 3 patients, which all showed a decrease in CSF pleocytosis; CSF cultures had negative results for all patients. The cause of persisting fever was unknown in most patients (63%); other causes were pneumonia in 2 (18%), drug-related fever in 1 (9%), and sepsis in 1 (9%). Mean time to defervescence was 4.9 days (range, 1–18 days). Recurrent fever occurred in 11 episodes (37%); causes were unknown in 6 (54%), pneumonia in 3 (27%), and drug-related fever in 2 (18%). During hospitalization, cranial CT scanning was repeated for 5 patients; 1 of these CT scans had abnormal findings, showing a subarachnoid hemorrhage.

Table 3
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Table 3

Complications during hospitalization and outcome for patients with Listeria monocytogenes meningitis.

Hyponatremia was found at admission to the hospital for 22 (73%) of 30 patients; 8 patients had severe hyponatremia (plasma sodium level, <130 mmol/L), and 14 patients had mild hyponatremia (plasma sodium level, <135 mmol/L). An additional 3 patients developed hyponatremia during hospitalization. Five (20%) of 25 patients were treated for hyponatremia; in 1 patient, this treatment consisted of fluid restriction.

Five (17%) of 30 patients in this cohort died. All of these patients died within 3 days after admission to the hospital, and all patients who died were >55 years old. Two of these 5 patients died of systemic complications, and 3 patients died of neurological complications. One patient died following a subarachnoid hemorrhage 1 day after admission to the hospital. Neurological examination was performed at discharge from the hospital for all 25 surviving patients and revealed cranial nerve palsies in 2 (8%) and focal cerebral deficits in 2 (8%). No patients had hearing impairment. In a univariate analysis, predictors for an unfavorable outcome were a low score on the Glasgow coma scale at admission to the hospital (P = .015) and a low platelet count (P = .024). Of the 9 patients who received microbiologically inadequate initial antimicrobial therapy, 2 (22%) of died; the other 7 patients had favorable outcomes.

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Discussion

Our findings show that meningitis due to L. monocytogenes is a disease that occurs among immunocompromised patients and elderly individuals. This corresponds with previous reports, which describe L. monocytogenes infection in patients with impaired cellular immunity (e.g., attributable to immunosuppressive therapy, immunosenescence, diabetes, or malignancies) [23, 24]. L. monocytogenes meningitis in young, previously healthy adults has been reported only in anecdotal observations [11, 14]. In a large literature review including all case series and case reports, this group constitutes only 6% of patients with L. monocytogenes CNS infection [14]. In our series, all patients were either immunocompromised or >50 years old.

Symptoms and signs of patients presenting with L. monocytogenes meningitis were not different from those found in the general population of patients with community-acquired bacterial meningitis. The prevalence of the classic triad of fever, neck stiffness, and altered mental status was 43%, and almost all patients presented with at least 2 of the 4 classic symptoms of headache, fever, neck stiffness, and altered mental status. Similar prevalences have been reported in the general population of patients with bacterial meningitis [2, 21]. This is in contrast with previous reports, which stressed the importance of the atypical presentation of patients with L. monocytogenes meningitis [14, 22]. This difference may well be explained by the retrospective design of these previous studies. This is the first prospective study of L. monocytogenes meningitis to date. Concordant with previous reports was the subacute development of disease in most cases [14, 22]. In a large proportion of patients, symptoms were present for ⩾4 days (27%).

A high proportion of adults with L. monocytogenes meningitis had atypical CSF findings; 23% of the patients had no individual CSF findings indicative of bacterial meningitis. In addition, Gram staining had a low yield. The causative microorganism was revealed by Gram staining in only 24% of patients. The atypical CSF findings and the low yield of Gram staining have been described previously in L. monocytogenes meningitis [3, 14].

Guidelines for suspected bacterial meningitis recommend amoxicillin-based empirical antimicrobial therapy for patients aged >50 years old or with risk factors to cover L. monocytogenes, because this bacterium is resistant to cephalosporins [25, 26]. Most patients in our case series received empirical therapy, including amoxicillin (70%). However, a considerable proportion of patients received third-generation cephalosporin monotherapy (27%). The median delay before these patients received adequate antimicrobial therapy was 3 days. This delay, however, was not associated with an unfavorable outcome. Although speculative, the absence of a relation between delay of adequate therapy and outcome might be explained by the limited number of patients included in the study. Another explanation could be the subacute development of disease in patients with L. monocytogenes meningitis. If meningitis due to L. monocytogenes is proven, either by Gram stain or CSF culture, we advise that patients be treated with amoxicillin, administered at a dosage of 2 g every 4 h for at least 21 days [22, 25, 27–29].

A clinical trial showed a beneficial effect of early dexamethasone treatment in adults with bacterial meningitis [30]. A recent meta-analysis confirmed these results [31]. Although 5 patients in our case series were eventually treated with steroids, none received adjunctive dexamethasone according to current guidelines [25]. Immunocompromised patients were excluded from the studies of adjunctive dexamethasone [30, 31]; therefore, these patients should not receive dexamethasone. Dexamethasone treatment is indicated for most patients with suspected bacterial meningitis; however, it remains unclear whether dexamethasone has beneficial effects in L. monocytogenes meningitis.

Our study has several important limitations. First, only patients who had a positive CSF culture result were included. Negative CSF culture results occur in 11%–30% of patients with bacterial meningitis, and this rate may be even higher among patients with L. monocytogenes meningitis, although exact figures are unknown [2, 3, 13, 22]. However, the clinical presentation of patients with positive and negative CSF culture results was closely similar in several studies [3, 5, 24]. Furthermore, patients with space-occupying lesions visible on CT may not undergo lumbar puncture [26]. Brain abscesses are found in 5% of L. monocytogenes infections of the CNS [14]. In patients with coagulation disorders or severe septic shock, lumbar puncture might be postponed, which can result in CSF cultures with negative results, as well [25]. Therefore, these patient groups were probably only partly represented in our study.

We describe, to our knowledge, the first patient with a subarachnoid hemorrhage as a complication in L. monocytogenes meningitis. Subarachnoid hemorrhage is known to be a rare complication of tuberculous meningitis, actinomycotic meningitis, and bacterial meningitis due to S. pneumoniae, but it has never been described in L. monocytogenes meningitis [32–34].

Another interesting observation in our study was the high rate of patients with hyponatremia (83%). Although high rates of hyponatremia are known from case series of tuberculous and group A streptococci meningitis, this has not been described in L. monocytogenes meningitis [35, 36]. Probable causes of hyponatremia are the syndrome of inappropriate antidiuretic hormone secretion and the cerebral salt wasting syndrome [37, 38]. The appropriate treatment for syndrome of inappropriate antidiuretic hormone secretion—fluid restriction—is opposite from the usual treatment of hyponatremia caused by cerebral salt wasting syndrome. Differentiation between the syndromes, however, is difficult. In children with bacterial meningitis and hyponatremia, fluid restriction does not improve either brain edema or outcome [39]. Current guidelines recommend that treatment of adults with bacterial meningitis should aim for a normovolemic state [25].

In conclusion, our study showed that L. monocytogenes meningitis is found in immunosuppressed patients and elderly individuals. Patients presented with signs and symptoms that were similar to those of the general population with bacterial meningitis, albeit with a longer prodromal phase. Despite frequent complications during hospitalization, the associated mortality rate was relatively low.

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Acknowledgments

We are indebted to many physicians in The Netherlands for their cooperation.

Financial support. Baxter BV (research grant to J.d.G.), the Meningitis Research Foundation (research grant to D.v.d.B.), and The Netherlands Organization for Health Research and Development (ZonMw) (NWO-Veni grant 2006 [916.76.023] and NWO-Rubicon grant 2006 [019.2006.1.310.0001] to D.v.d.B.). The Dutch Meningitis Cohort Study was supported in part by a research grant from Roche Pharmaceuticals.

Potential conflicts of interest. All authors: no conflicts.

  • Received May 8, 2006.
  • Accepted June 14, 2006.
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  1. Clin Infect Dis. (2006) 43 (10): 1233-1238. doi: 10.1086/508462
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