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The Epidemiology of Meningitis in Infants Under 90 Days of Age in a Large Pediatric Hospital

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The Epidemiology of Meningitis in Infants Under 90 Days of Age in a Large Pediatric Hospital microorganisms Article The Epidemiology of Meningitis in Infants under 90 Days of Age in a Large Pediatric Hospital Timothy A. Erickson 1,2, Flor M. Munoz 3, Catherine L. Troisi 2 , Melissa S. Nolan 4 , Rodrigo Hasbun 5, Eric L. Brown 2 and Kristy O. Murray 1,* 1 Department of Pediatrics, Section of Pediatric Tropical Medicine, William T. Shearer Center for Human Immunobiology, Baylor College of Medicine and Texas Children’s Hospital, Houston, TX 77030, USA; [email protected] 2 School of Public Health, University of Texas Health Science Center, Houston, TX 77030, USA; [email protected] (C.L.T.); [email protected] (E.L.B.) 3 Department of Pediatrics, Section of Infectious Diseases, Baylor College of Medicine and Texas Children’s Hospital, Houston, TX 77030, USA; fl[email protected] 4 Department of Epidemiology and Biostatistics, Arnold School of Public Health, University of South Carolina, Columbia, SC 29208, USA; [email protected] 5 McGovern Medical School, University of Texas, Houston, TX 77030, USA; [email protected] * Correspondence: [email protected] Abstract: Background: Meningitis is associated with substantial morbidity and mortality, particularly in the first three months of life. Methods: We conducted a retrospective review of patients <90 days of age with meningitis at Texas Children’s Hospital from 2010–2017. Cases were confirmed using the National Healthcare Safety Network (NHSN) definition of meningitis. Results: Among 694 infants with meningitis, the most common etiology was viral (n = 351; 51%), primarily caused by Citation: Erickson, T.A.; Munoz, enterovirus (n = 332; 95%). A quarter of cases were caused by bacterial infections (n = 190; 27%). The F.M.; Troisi, C.L.; Nolan, M.S.; most common cause of bacterial meningitis was group B Streptococcus (GBS, n = 60; 32%), followed Hasbun, R.; Brown, E.L.; Murray, by Gram-negative rods other than E. coli (n = 40; 21%), and E. coli (n = 37; 19%). The majority K.O. The Epidemiology of Meningitis in Infants under 90 Days of Age in a of Gram-negative organisms (63%) were resistant to ampicillin, and nearly one-fourth of Gram- Large Pediatric Hospital. negative rods (23%) other than E. coli and 2 (6%) E. coli isolates were resistant to third-generation Microorganisms 2021, 9, 526. https:// cephalosporins. Significant risk factors for bacterial meningitis were early preterm birth and the doi.org/10.3390/microorganisms Black race. Conclusions: Enteroviruses most commonly caused viral meningitis in infants; GBS was 9030526 the most common bacterial cause despite universal screening and intrapartum prophylaxis. The emergence of MRSA and resistance to third-generation cephalosporins in Gram-negative bacterial Academic Editor: James Stuart meningitis challenges the options for empirical antimicrobial therapy. Received: 15 January 2021 Keywords: neonatal infections; meningitis; epidemiology; antibiotic resistance; etiologic diagnosis; Accepted: 9 February 2021 enterovirus; group B Streptococcus Published: 4 March 2021 Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in 1. Introduction published maps and institutional affil- iations. Meningitis is associated with substantial morbidity and mortality, particularly in infants. Numerous causes of meningitis exist, with viral and bacterial infectious agents the most common. About one-quarter of the cases of meningitis lacks an identified cause [1]. Infants, particularly those under 90 days of age, historically have the highest attack rates for bacterial meningitis, with Haemophilus influenzae type b (Hib) being most common in the Copyright: © 2021 by the authors. Streptococcus E. coli Licensee MDPI, Basel, Switzerland. era prior to routine vaccination and group B (GBS) and most commonly This article is an open access article reported since. Other leading causes include viral infection with enterovirus and herpes distributed under the terms and simplex virus (HSV) [2–9]. Only a few studies have investigated the epidemiology of infant conditions of the Creative Commons meningitis since the introduction of antenatal screening and antepartum treatment for GBS Attribution (CC BY) license (https:// in pregnant women and the advent of molecular diagnosis [7,8,10,11]. creativecommons.org/licenses/by/ Contemporary studies examining the etiology and epidemiology of infant meningi- 4.0/). tis are needed, given advances in diagnostic methods available to clinicians in the last Microorganisms 2021, 9, 526. https://doi.org/10.3390/microorganisms9030526 https://www.mdpi.com/journal/microorganisms Microorganisms 2021, 9, 526 2 of 11 decade. Similarly, studies describing antimicrobial resistance patterns are needed [9]. This information is particularly important as antibiotic resistance has increased in the past two decades among the most common bacterial pathogens known to cause infant meningitis, most particularly among Gram-negatives [12,13]. To address these gaps, we conducted an investigation into the epidemiology of meningitis in infants 0 to 90 days of life at a large pediatric hospital in Houston, Texas. 2. Materials and Methods We conducted a retrospective medical record review of all patients with an ICD-9 or -10 diagnosis code corresponding to meningitis admitted to Texas Children’s Hospital from 1 January 2010 to 30 December 2017 (Table S1). Only infants <90 days of age at the time of diagnosis were retained for analysis. We employed the National Healthcare Safety Network (NHSN) definition of meningitis, which states that a case of meningitis requires having either (1) an organism identified from the cerebrospinal fluid (CSF) by culture (e.g., bacteria, fungi), PCR (e.g., viruses), or confirmatory level of IgM (e.g., arbovirus), OR (2) CSF pleocytosis and compatible signs and symptoms [14,15]. If a patient with pleocytosis and clinically compatible signs and symptoms had no organism identified in the CSF but had an organism isolated from a different sterile site (i.e., blood or urine) that is a known cause of meningitis, then they were classified as meningitis caused by that organism. Meningitis occurring after intravenous immunoglobulin (IVIG) was classified as meningitis due to IVIG, a well-known phenomenon [16]. Patients were classed into groups and subgroups by cause (viral, bacterial, fungal, and unknown). Medical records were abstracted to acquire demographic information, pre- and post- natal metrics, including gestational age at birth, microbiology and laboratory values at the time of admission, and clinical outcomes. Patient length of stay was calculated from the date of hospital admission to date of discharge except in the case of those patients initially admitted for a non-meningeal cause; these were calculated from the date of the first identification of an abnormal CSF result. Patients were divided by age into the following categories: <7 days of age, 7–14 days, 15–21 days, 21–28 days, and >28 days of age; and by gestational age at birth as term (≥37 weeks gestation) or preterm (<37 weeks gestation). Patients with preterm birth were defined as either early preterm (≤34 weeks gestation) or late preterm (35 or 36 weeks gestation). Maternal age, GBS screen status (conducted, positive/negative), type of delivery (spontaneous vaginal delivery or cesarean section), and maternal antibiotic treatment were also obtained. Categorical variables were compared using a Pearson’s chi-square test with statistical significance set at the 0.05 level. All statistics were calculated using STATA version 14.2 (StataCorp, College Station, TX, USA). This study was reviewed and approved by the Baylor College of Medicine Institutional Review Board (H-35069). 3. Results From 2010–2017, 1501 cases of meningitis and encephalitis were admitted to Texas Children’s Hospital. Almost half (n = 694; 46%) of all patients presented in the first 90 days of life (Figure1). These infant patients accounted for 9518 days of hospital stay, with a median length of stay of 3 days. Fourteen patients (2%) died from their infections (Table1). An etiologic cause could be determined for 547 patients in this population (79%). Overall, viral causes were most common (n = 351; 51%), followed by bacteria (n = 190; 27%), fungi (n = 5; 1%); and one case occurring after IVIG treatment (Table2). One of every five patients had no known cause identified (n = 147; 21%). Twenty-five patients (4%) had healthcare-associated ventriculitis and meningitis (HCAVM). Among the 190 bacterial meningitis cases, the majority were culture-positive in the CSF (n = 150; 79%), followed by blood (n = 29; 15%), urine (n = 9; 5%), wound site on brain (n = 1; <1%), and one unknown. Microorganisms 2021, 9, x FOR PEER REVIEW 3 of 11 Microorganisms 2021, 9, 526 the majority were culture-positive in the CSF (n = 150; 79%), followed by blood (n3 = of 29; 11 15%), urine (n = 9; 5%), wound site on brain (n = 1; <1%), and one unknown. Figure 1. Selection flowchart. Figure 1. Selection flowchart. Table 1. Demographic and clinical3.1. Viral characteristics Infections of meningitis by etiology in infants under 90 days of age, Houston, TX 2010–2017 *. The vast majority of viral meningitis cases were caused by enteroviral infection Enterovirus (332/351, 95% of all viruses identified).Gram- Enterovirus infectionsGram exhibited seasonal trends, Demographics Staphylococcus and West Nile HSV GBS Positive E. coli Negative Fungal Unknown and Clinical with cases occurring Speciesmost commonly in the summer and with peaks in 2014 and 2015 Virus n = 18 n = 60 Others n = 37 Others n= 5 n
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