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Original Studies

Neonatal Bacterial Meningitis

444 Cases in 7 Years

Gaschignard, Jean MD*; Levy, Corinne MD†‡; Romain, Olivier MD*†‡; Cohen, Robert MD†‡; Bingen, Edouard MD†§; Aujard, Yannick MD†‡¶; Boileau, Pascal MD*

Author Information
The Pediatric Infectious Disease Journal: March 2011 - Volume 30 - Issue 3 - p 212-217
doi: 10.1097/INF.0b013e3181fab1e7
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Abstract

Neonates are at high risk of meningitis and of resulting neurologic complications. Neonatal meningitis arising in the first 28 days has a mortality rate of about 10% to 15% and a long-term neurologic morbidity rate of 20% to 50%.1–4

In 2001, the Pediatric Infectious Diseases Group of the French Pediatric Society (GPIP/ACTIV of SFP) established an active bacterial pediatric meningitis surveillance network based in representative hospital sites to collect the clinical and biologic features of bacterial meningitis and their treatment.5,6

The objectives of this study were to determine the etiology and mortality rate of neonatal bacterial meningitis in France between 2001 and 2007, and to analyze the mortality rate according to etiology, age of onset of disease, gestational age (GA), and presence of fetal growth restriction. Meanwhile, in September 2001, recommendations for the prevention of neonatal infections with Group B streptococci (GBS) were released online by the French National Authority for Health. A screening based-approach (vaginal swabs cultures) was used, with subsequent intrapartum antibiotic prophylaxis when needed.7 These recommendations were implemented progressively during 2002. Worries were raised about the risk of increasing the proportion of neonatal infections with other bacteria such as Gram-negative bacilli (and increased resistance to amoxicillin in Gram-negative bacilli) or the number of late-onset GBS meningitis.

In this study, meningitis data concerning specifically the neonatal period collected during the first 7 years of the survey are analyzed.

PATIENTS AND METHODS

A total of 252 pediatric wards and 168 microbiology laboratories participated in the French national survey. Pediatric wards included 45% of neonatal units, and their number and proportion were almost constant between 2001 and 2007.5 All patients less than 18 years of age with confirmed bacterial meningitis were included in the study. Coagulase-negative staphylococci were excluded.

After patient discharge, a standardized form was completed on site by a designated clinical investigator and was sent by electronic or postal mail to the investigating center (ACTIV). All data were validated by a scientific committee. The standardized form covered the following data: clinical signs, severity criteria (coma, mechanical ventilation, shock, seizures, and extensive purpura), date of birth, gender, vaccine status, predisposing factors (eg, meningeal breach, spina bifida, recurrent meningitis, cochlear implant, asplenia, immunodeficiency, or cardiopathy), antibiotic treatment less than 24 hours before lumbar puncture, cerebrospinal fluid (CSF) analysis, blood culture, treatment of the current episode (antibiotics and steroids), and short-term outcome. The diagnosis of meningitis was based on either one of the following criteria: positive culture of CSF and/or positive direct examination of CSF (with a negative culture) and/or presence of positive soluble antigens in the CSF and/or positive PCR in the CSF and/or positive blood culture associated with a pleocytosis (≥10 × 106 cells/L) in the CSF. Bacterial isolates were identified using the rapid 32E system (BioMérieux), K1 capsule antigen determination was made with Antigen Pasteurex (Biorad), and in-house PCR testing were used.

Three times a year, each clinical investigator from each participating ward was contacted to declare their bacterial meningitis cases or to confirm their absence. Since 2003, the number of nonresponder pediatric wards remained very low.5

Neonatal cases were defined as infants ≤28 days of age, who where registered in the French national survey between January 1, 2001 and December 31, 2007. The distinction between early- and late-onset disease is often used and the cut-off varies from 2 to 6 days.8 In the present study, day 4 was used as the threshold to separate early-onset meningitis (occurring between day 0 and day 4) and late-onset meningitis (occurring between day 5 and day 28).

For statistical analysis, the infants were divided into the following 3 groups:

  • Term: born at GA ≥37 weeks.
  • Late-preterm: born at GA between 33 and 36 weeks +6 days.
  • Very preterm: born at GA <33 weeks.

Preterm refers to all infants born at GA <37 weeks.

Data were also analyzed according to birth weight and GA at birth: infants were classified into 2 groups, appropriate for gestational age (AGA) or small for gestational age (SGA), depending on whether they were above or below the 10th percentile of the AUDIPOG9 standards, respectively.

Data handling and statistical analysis were performed using the software “Biostatgv” (Université Pierre et Marie Curie, Paris, and Université Paul Sabatier, Toulouse, INSERM, available at: http://www.u707.jussieu.fr/biostatgv/). Nonparametric tests were used to compare means. Proportions were compared using the χ2 test, with a significant threshold of P < 0.05. Multivariate logistic analysis on mortality rate taking into account GA and being SGA was performed using SAS software, Version 9.1 (SAS Institute Inc, Cary, NC).

RESULTS

Epidemiology

Between 2001 and 2007, 2951 cases of bacterial meningitis in children were recorded in 252 pediatric wards, among which 444 (15%) were reported in infants 28 days or less of age by 114 wards. Late-onset prevailed over early-onset meningitis (68% [301] vs. 32% [143]). Among early-onset cases, 76% (109/143) were diagnosed before day 2 of life.

Eighty-nine percent of patients were diagnosed with meningitis on the basis of a positive culture of the CSF (Fig. 1), and this proportion was stable between 2001 and 2007. Four percent had a positive antigen for a bacteria in the CSF and another 4% had a pleocytosis in the CSF associated with a positive blood culture. Finally, the following 5 cases were diagnosed on pleocytosis and a positive bacteriological culture: 1 urine culture (Escherichia coli), 1 vaginal swab for GBS, 1 blood antigen positive for GBS, and 2 gastric aspirate cultures for GBS. These 5 cases were considered as possible meningitis, and were excluded from analysis. Among the 439 cases retained for analysis, 400 lumbar punctures were performed within the first 48 hours of admission. Thirty-eight CSF were obtained after 48 hours, 6 were positive for GBS, 24 for E. coli, and 8 for other bacteria (3 Streptococcus bovis, 2 enterobacteriaceae, 1 Listeria, 1 Pseudomonas aeruginosa, and 1 Serratia marcescens) and they involved 34 preterm infants. Thirty-five cases were late-onset meningitis, and the other 3 occurred at day 4 (early-onset). The date of lumbar puncture was not available for 1 patient.

FIGURE 1.
FIGURE 1.:
Flowchart of bacterial meningitis diagnosed.

Bacteria identified as causal agent for meningitis in these 439 neonates are presented in Table 1. GBS and E. coli were found in 59% and 28% of cases, respectively. Among other bacteria, Gram-negative bacilli other than E. coli were found in 4% of cases, whereas Neisseria meningitidis and Streptococcus pneumoniae were found in 3% and 2% of cases, respectively. Finally, Listeria monocytogenes was isolated in 7 cases (1.5%) during this 7-year period. For GBS and E. coli meningitis, the serotype was available in 106 and 97 cases, respectively. Main serotypes were serotype III (90%) for GBS and serotype K1 (88%) for E. coli. Two patients had a ventriculoperitoneal shunt before the infection (1 GBS and 1 Enterococcus faecalis), 1 patient had a meningeal breach (E. coli), and no patient was born with spina bifida.

TABLE 1
TABLE 1:
Distribution of Bacteria Isolated in Early-onset (d0–d4) and Late-onset (d5–d28) Neonatal Meningitis From January 1, 2001 to December 31, 2007

GBS was statistically more frequent in early-onset cases of neonatal meningitis compared with late-onset cases (77% vs. 50%, P < 0.01) (Table 1). In contrast, early-onset of E. coli neonatal meningitis was statistically less frequent than late-onset of E. coli meningitis (18% and 33%, respectively, P < 0.01). In a similar way as E. coli, all other bacteria were isolated more frequently in late-onset compared with early-onset meningitis (17% vs. 5%, P < 0.01). Only 2 bacteria were isolated from the 9 meningitis diagnosed on day 0: GBS (8) and E. coli (1).

Analysis According to GA at Birth

Among the neonatal cases of bacterial meningitis, 330 (78%) infants were born at term (GA ≥37 weeks) and 93 were born preterm (GA <37 weeks). Among the latter, 67 infants (16%) were born between 33 weeks and 36 weeks +6 days (late-preterm), and 26 infants (6%) were born before 33 weeks (very preterm). GA was not available for 16 infants.

GBS was the most common pathogen identified (66%, 219/330) in term infants, whereas E. coli was the most common cause among the late-preterm and the very preterm infants with respectively 42% (28/67) and 54% (14/26) of the cases (Fig. 2). E. coli was the most common bacteria isolated in late-onset cases among late-preterm (47%, 20/43) and very preterm infants (52%, 12/23). In early-onset meningitis, E. coli was also the most common pathogen identified among the preterm infants with 44% (12/27) versus 41% (11/27) for GBS.

FIGURE 2.
FIGURE 2.:
Distribution of early- and late-onset neonatal meningitis according to GA at birth. The number of cases of meningitis observed according to the GA at birth for each type of isolated bacteria is shown in the corresponding histogram.

Finally, non-GBS early-onset neonatal meningitis was significantly more frequent in preterm compared with term infants (59% [16/27] vs. 14% [15/110]). Similarly, non-GBS late-onset neonatal meningitis was significantly more frequent among the preterm compared with the term infants (71% [47/66] vs. 44% [96/220] P < 0.05).

Analysis According to Birth Weight

The distribution of bacteria according to the classification of meningitis (early- or late-onset) and to the SGA or AGA infant status at birth is shown in Table 2. No significant difference was found between the AGA and SGA groups for the occurrence of early- or late-onset meningitis (analysis carried out on 416 infants: 372 AGA and 44 SGA).

TABLE 2
TABLE 2:
Distribution of Early and Late-onset Neonatal Meningitis According to Birthweight

Clinical and Biologic Features of Neonatal Bacterial Meningitis

Of the neonates with bacterial meningitis, 24% (100/416) showed signs of shock at the time of diagnosis, regardless of the etiology (GBS: 25% [61/242], E. coli: 23% [27/118], and other bacteria: 21% [12/56]). Seizures were reported in 34% (143/420) of the neonatal cases. They were significantly more common in GBS (41%, 101/246) compared with E. coli meningitis (25%, 30/118, P < 0.01) and meningitis because of other bacteria (21%, 12/56, P < 0.01).

The CSF protein value (data available for 307 infants out of 439; 3.3 ± 2.4, 3.3 ± 2.3, and 3.6 ± 3.0 g/L), blood glucose ratio (data available for 231/439; 0.30 ± 0.33, 0.28 ± 0.33, and 0.39 ± 0.44), pleocytosis (data available for 387/439 and are given as median values and ranges; 4993 [2;80000 cells/mm3], 7766 [4;65000 cells/mm3], and 4544 [20;35000 cells/mm3]), and neutrophil percentage (data available for 272/439; 82%, 79%, and 85%) for GBS, E. coli, and other bacteria, respectively, were not statistically different between the 3 groups of bacteria.

Mortality

Neonatal mortality rate of bacterial meningitis was 13% (Table 3). There was no significant difference between the rate in those with meningitis caused by E. coli (12%, 15/123), GBS (13%, 34/258), and other bacteria (17%, 10/58).

TABLE 3
TABLE 3:
Mortality of Neonatal Bacterial Meningitis

In contrast, the mortality rate was significantly higher in the preterm infants compared with term infants (26% vs. 10%, P < 0.01). Mortality rate was also significantly higher in SGA compared with AGA infants (25% vs. 12%, P < 0.04). However, we performed a multivariate logistic analysis including GA and being SGA as covariates. Being preterm was identified as an independent risk factor of death (adjusted odds ratio, 2.97 [95% confidence interval, 1.62–5.45]) whereas being SGA was not (adjusted odds ratio, 1.79 [95% confidence interval, 0.82–3.91]). Infant death occurred on average 8 days after the first lumbar puncture (range, 0–21 days).

Distribution of Early- and Late-onset Neonatal Meningitis From 2001 to 2007

The annual distribution of neonatal bacterial meningitis between 2001 and 2007 is shown in Figure 3. The mean annual number of neonatal meningitis was compared between the years prior (2001–2002) and post (2003–2007) implementation of the French recommendations for the prevention of neonatal GBS infection. The annual mean number of early-onset meningitis was lower in years 2003–2007 compared with 2001–2002 (16.4 ± 1.7 vs. 29.5 ± 6.4, P = 0.08), whereas the number of pediatric wards was almost constant. This decrease was mainly because of a reduction of early-onset GBS meningitis (12.0 ± 2.0 vs. 24.5 ± 5.0, P = 0.08). Meanwhile, the annual number of non-GBS early-onset meningitis remained unchanged (5.0 ± 1.4 vs. 4.4 ± 0.9). Additionally, the mean annual number of late-onset meningitis did not change before and after 2002 (43.5 ± 12.0 vs. 42.2 ± 5.0).

FIGURE 3.
FIGURE 3.:
Distribution of early- and late-onset neonatal meningitis from 2001 to 2007. The total number of meningitis for each year is shown in the figure. The number of cases with GBS, E. coli, or other bacteria is shown in the Table beneath. During the year 2002, the recommendations by the French National Authority for Health for the antenatal prevention of the bacterial neonatal risk were introduced in the practices.

DISCUSSION

Between 2001 and 2007, 444 cases of neonatal bacterial meningitis were collected in the French national survey for bacterial meningitis in children, and analysis was carried on 439 of proven meningitis cases, the 5 remaining cases were considered as “possible meningitis.” This is currently the largest described series of neonatal bacterial meningitis. Despite this high number of reported cases, it is likely that the incidence of bacterial neonatal meningitis remains underestimated. Several studies have highlighted this underestimation, both for early- and late-onset meningitis. Nearly 30% of bacterial meningitis cases in infants are not diagnosed when only one blood culture is performed to confirm neonatal infection.10,11 Additionally, lumbar puncture is not systematically performed when infection is suspected clinically in neonatal intensive care units, and shock at diagnosis or very low birth weight may limit its performance. In 38 cases, the lumbar puncture was performed more than 48 hours after admission and therefore they were nosocomial. Nevertheless, E. coli which accounts for two-third of these cases is not usually associated with a horizontal contamination.

Our study underlines the predominance of GBS (59%) and E. coli (28%) in neonatal bacterial meningitis. This result is similar to that of other developed countries,2 but it is very different from the situation in developing countries. In the latter, Streptococcus pneumoniae and enterobacteriaceae are the most common infecting bacteria.12 A higher prevalence of E. coli meningitis in the late-onset cases and among the preterm infants has already been reported in developed countries.13 Although prematurity modified the bacterial epidemiology of neonatal meningitis (Fig. 2), bacterial distribution did not change between SGA and AGA infants (Table 2).

The mortality rates found by Holt et al2 among neonates with GBS or E. coli meningitis were 12% and 15%, respectively. They were not different from the mortality rates of 13% and 12% found in the present study for GBS and E. coli neonatal meningitis, respectively. The mortality rate was twice as high in preterm (26%) than in term infants (10%). The difference in mortality rate was also twice between SGA and AGA infants with 25% and 12%, respectively, but not independently of being preterm. Data concerning the mode of delivery (vaginal delivery vs. cesarean section) or the premature rupture of membranes were not available. Furthermore, our study has 2 main limitations: some cases may have escaped this pediatric surveillance network, despite our effort, and outcome was determined only at hospital discharge, which deprives us of clinical information concerning patients, such as long-term neurologic morbidity.

The reduction in the incidence of early-onset neonatal GBS disease after prophylactic intrapartum administration of antibiotics to mothers at risk for transmitting GBS to their newborns is well-established.14 In this study, the number of early-onset meningitis decreased between 2001 and 2007, and more specifically between 2001 and 2004. This reduction could partially be because of the antenatal detection of GBS with vaginal swabbing, which enables the clinician to administrate an intrapartum antibiotic prophylaxis in case of positive GBS carriage. This management was put in practice during the year 2002. The present data suggest that these recommendations have not affected the number of late-onset neonatal meningitis. This is consistent with studies suggesting a community mode of acquisition in late-onset meningitis,8 in contrast with vertical transmission assumed for the pathogenesis of early-onset meningitis. However, the significance of our observation is limited and can be biased, because the prevalence of intrapartum maternal antibiotic prophylaxis, before and after the recommendations from the French National Authority for Health were implemented, are not known. In addition, the French national meningitis survey is a descriptive observational study and caution must be applied for the interpretation of results concerning the total number of neonatal meningitis cases reported during these periods.

A vast majority of preterm infants escapes antenatal screening for GBS, which is usually performed after 35 weeks in France. At this point, a high incidence of non-GBS early-onset meningitis was observed in preterm (59%) compared with term infants (14%). This high rate of early-onset non-GBS meningitis could be partially explained by empirical antepartum administration of antibiotics (usually containing amoxicillin) because infectious causes of preterm delivery are systematically evoked. Finally, while prematurity has been established as a risk factor for late-onset meningitis with GBS,15 this study also describes a high incidence of late-onset non-GBS meningitis among the preterm infants (71% in preterm vs. 46% in term infants). Nevertheless, at the dawn of the 21st century, GBS remains the dominant cause of neonatal bacterial meningitis in developed countries such as France.

ACKNOWLEDGMENTS

The authors thank the pediatricians and microbiologists from the French national survey of bacterial meningitis of the child, the doctors, and professors Abdelkadous, Abou Tara, Achkar, Adam, Akhdar, Akitani, Akli, Alba-sauviat, Albertini, Aljazayri, Allia, Alonso, Altuzarra, Amira, Amirault, Amsallem, Andlauer, Andriamanjeto, Andriantahina, Arlet, Armengaud, Arnault, Asensi, Aubert, Aucher, Audry, Aufrant, Aujard, Auvray, Bachelier, Bajolle, Banerjee, Barbier, Barbut, Barnaud, Barrans, Barraud, Barre, Barthez, Bartizel, Bassil, Bataille, Bayle, Bebear, Benchekroun, Benezech, Bengrina, Benkhelifa, Benoit, Benseddik, Berardi-grassias, Berche, Berger, Bernard, Berrahma, Bertecottière, Berthelot, Berthier, Bessis, Besson-leaud, Biessy, Bigirimana, Bina, Bineau, Bingen, Biran-mucignat, Bitar, Blanc, Blanchard, Bland, Blezel, Blondel, Blondin, Blot, Boileau, Boize, Bolot, Bompard, Bonardi, Boniface, Bonnin, Boquet, Born, Bosdure, Bost-bru, Bouainane, Bouderlique, Bouige, Bouillie, Bour, Bourrillon, Boutet, Boutte, Bouygues, Bouziges, Bovero, Bowete, Boyer, Branca, Branger, Brault, Briand, Briffod, Brintet, Brizard, Brocard, Brotslhi, Brouard, Broussin, Broussine, Bruand, Brunel, Bruyas, Budniok, Burel, Burnichon, Cabon Boudard, Cahiez, Caillaux, Callamand, Calvez, Camboulives, Camenen, Campet, Canarelli, Canis, Canonne, Cantagrel, Canzi, Capbern, Capdeville, Carbonnelle, Carre, Carre-Cavellier, Carriere, Carroger, Castelnau, Catteau, Cattoen, Cau, Cauby, Caveriviere, Cecille, Chabrol, Chaix, Chalvon Demersay, Chaker, Chalumeau, Chami, Chamouilli, Chamoux, Chantelat, Chantepie, Chaplain, Chappet, Charachon, Charara, Chardon, Charpentier, Charras, Chassevent, Chenaud, Cheron, Cheuret, Chevallier, Chopard, Choulot, Claris, Clergeau, Coache, Colin-gorski, Collignon, Colombani, Combe, Constanty, Copin, Cordier, Cormier, Costa, Cottancin, Cotteau, Cottin, Couchot, Coumenges, Courcol, Cousinard, Crepet, Croix, Croize, Crost, Cuntz, Cuvelier, Cuzzi, Dabernat, Dagorne, D'albignac, Dalmon, Daltroff, Danjean-deguin, Danjoux, Daoud, Daoudi, Darchis, Darras, Dassieu, Dauger, Daumergues, David, David Rubin, De Champs, De Cousser, De Lumley, De Montclos, De Montgolfier, De Ricaud, Debriel, Decoster, Decoux, Deforches, Dehan, Delacourt, Delahaye, Delamare, Delaporte, Delarbre, Delbeke, Deligne, Delisle, Delubac, Demachy, Demarcq, Demarque, Demarquez, Denis, De Preville, De Prunele, De Ricaud, Despert, Desprez, Desson, Destuynder, Devictor, Deville, Devouge, Dib, Dieckmann, Doeuvre, Dolhem, Douard, Doucet-populaire, Douchain, Douillet, Drugeon, Dublanchet, Dubois, Dubos, Dubourdieu, Duchaine, Duhamel, Dulucq, Dumont, Dumoulard, Dupic, Dupont, Dupre, Durand, Duval Arnould, Eb, Eicher, Eloy, Enchery, Escarguel, Estournet Mathiaud, Estrangin, Etienne, Evrard, Eyssette Guerrau, Faibis, Farges, Faye, Feit, Ferre, Ferroni, Fevre, Fieschi, Fiette, Fischbach, Flipo, Floret, Flurin, Forget, Fortier, Fortin, Fos, Foucaud, Fournet, Fournier, Fremaux, Freydiere, Freysz, Fruchart-flamenbaum, Furioli, Gagliardone, Gaillard, Galanti-cuyeu, Gallou, Ganivala, Garandeau, Garbarg-chenon, Garcera, Garnier, Gaudeau-toussaint, Gaudelus, Gauduchon, Gautry, Gavignet, Gbadamassi, Geffroy, Gendrel, Geraudel, Gevaudan, Ghnassia, Gilbert Bonnemaison, Girier, Giudicelli, Glastre, Gold, Goldstein, Goma, Goudeau, Gougeon, Goumy, Gouraud, Gout, Goux, Graff, Grancher, Grand'Esnon, Granier, Granry, Gras-le Guen, Grasmick, Gremeaux, Gremillet, Gressier, Grimprel, Grise, Guerin, Guibert, Guichard, Guiet, Guilhaume, Guillaume, Guillaume Bodet, Guillermet Fromentin, Guillois, Guillot, Guyon, Guyot, Haas, Hachani, Hage, Hallalel, Halphen, Hamza, Hand, Hasselmann, Hautefort, Hefteh, Heidt, Hermann, Hernandorena, Herve, Hees, Heuclin, Heurte, Heusse, Hevin Martin, Heyman, Hidri, Hoffmann, Holler, Honore, Hubert, Hudebine, Huet, Huin, Hureaux, Husson, Ikunga, Imbs, Ingrand, Jacob, Jalloul, Jan, Janaud, Jarlier, Jeannoel, Jeannot, Jeny, Jeudy, Jokic, Joly-guillou, Jomaa, Joram, Joubert, Joussein, Julien, Jullien, Jullienne, Kaid Omar, Kaiffer, Kalach, Kermad, Khazaal, Kirch, Kitzis, Klein, Kone-paut, Kowalczyk, Kretz, Kuntzel, Kurtz, Labbe, Laborie, Laboreau, Labrune, Lacombe, Lacomme, Lafargue, Lagier, Laidj, Laisney, Lajarrige, Lakhdari, Laluque, Lamarca, Lambert, Landragin, Landrot, Langs, Lanotte, Lansiaux, Larchet, Larroque, Larrouy, Laurent, Layadi, Le Bail, Le Bideau, Le Gagneur, Le Gall, Le Lorier, Le Luyer, Le Turdu, Lebas, Leberre, Leblanc, Leboucher, Lebrun, Lecaillon Thibon, Lecine, Leclerc, Leclercq, Lecomte, Lefrand-crepin, Lehnert, Lehours, Lejeune, Lelioux, Leluan, Lemaitre, Lemble, Lemeland, Lenclen, Lenoir, Leotard, Leraillez, Lesage, Lesbros, Lescanne, Letouzey, Levy, Lhermitte-cahuzac, Lina, Louf, Lubrano, Lucet, Lureau, Lusina, Madhi, Magny, Maillotte, Malbrunot, Mallet, Maman, Mancini, Mangeol, Mangin, Marani, Marchand, Marcolene, Marcou, Marcu-Marin, Marmouset, Marie Dit Dinard, Marret, Martha Le Gall, Martin, Martinat, Martinot, Mas, Massard, Masutti, Mathieu, Mattei, Maugard, Maurage, Mazataud, M'bamba, Medejel, Megraud, Melon, Menget, Menouar, Menouni-foray, Merlin, Mettey, Metton, Meunier, Meyer, Mikail, Milesi, Milh, Milleret-proyart, Mitanchez, Mokhtari, Mondaud, Monfort-gouraud, Monier, Monin, Morales-gineste, Moreau, Moregne, Morice, Moriette, Morin, Morisot, Morville, Motte, Mougin-Joubert, Moulene, Moulie, Mounzer, Mselati, Muller, Nacer, Naudion, Nelson, Nerl Schiavini, Nerome, Netter, Neuwirth, Nordmann, Noseda, Nouvellon, Orzechowski, Otterbein, Oules, Paget, Pangon, Pannecouck, Paris, Pascal, Pateyron, Pauchard, Paul, Pautard, Pellerin, Pelletier, Pellot, Pelloux, Penaud, Penel, Peralta, Perrin, Peter, Petit Boulanger, Peyraud, Philippe, Philippon, Picaud, Picherot, Piemont, Pierre, Pierrejean, Pigeon, Pignol, Pinard, Pincemaille, Pincet, Pinquier, Pinto Da Costa, Plasse, Ploton, Plouvier, Poilane, Poilly, Poirier, Poirot, Pollet, Popelard, Porcheret, Poulain, Pradeaux, Prere, Priqueler, Puech, Queinnec, Quinet, Raber, Raoult, Ravussin, Raymond, Raynaud, Rebaud, Redouani, Reguet, Renard, Renaud, Rennes, Renolleau, Retali, Retornaz, Reveil, Richardin, Riegel, Rimet, Rio, Rivaux, Riviere, Robin, Rodiere, Rolland, Romanet, Ropert, Rossignol, Roudaut, Rougier, Roullaud, Roussellier, Roybet, Roze, Rudler, Ryckewaert, Sadik, Sadki, Saf, Saillant, Saliba, Sanchez, Santerne, Sanyas, Sardet, Sarlangue, Sartre, Savoy, Sayegh, Scanvic, Scart, Scat, Schaefer, Schnebelen, Schneider, Seaume, Sebag, Secher, Seguin, Semon, Sep-hieng, Sermet-Gaudelus, Sfez, Sibille, Sicard, Siegel, Simonin, Sirot, Sivadon-tardy, Smati, Sommabere, Spicq, Stach, Tahiri, Taillebois, Talon, Tchanga, Terki, Tessier, Texier, Thevenieau, Thibaud, Thibault, Thierry, Thore, Tillier, Tiry, Tisseron, Tixier, Tommasi, Tourrand, Tous, Trioche, Tronc, Turchini, Tytgat, Uzan, Vachee, Valayer, Vallee, Van De Perre, Vandenesch, Vasquez, Vasselon-raina, Vaucel, Vergerond, Vergnaud, Vergne, Vernet-garnier, Vernoux, Vic, Vidailhet, Vignaud, Vigne, Vigneron, Villemain, Villeneuve, Voisine, Voyer, Vray, Vrillon, Vu Thien, Warin, Wasels, Weiber, Weil-olivier, Weisse, Wemeau, Worcel, Yang Ting, Ygout, Ythier, Zaoui, Zelinsky-gurung, Zimmermann, Zumbo, Zupan-Simunek, Zyka.

The authors also thank the staff from ACTIV for the data handling and the technical help, Elvira Martin, Aurélie Lecuyer, France de la Roque, Michel Boucherot, Nathalie Kohn, Sadia Tortorelli, Manuela Pereira, Pascale Latile, and Isabelle Ramay.

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Keywords:

neonatal; bacterial; meningitis; mortality; group B streptococci; Escherichia coli

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