Global Study of Viral Meningitis: A Systematic Review and Meta-analysis

Authors

1 Department of Microbiology, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran

2 Department of Microbiology, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran.

3 Virology Department, School of Medicine, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran

4 Department of Biochemistry and Biophysics, Metabolic Disorders Research Center, School of Medicine, Golestan University of Medical Science, Gorgan, Iran

5 Health Research Institute, Infectious and Tropical Diseases Research Center, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran

6 Department of Biochemistry, Royan institute, Tehran, Iran.

7 Department of Emergency Medicine, School of Medicine, Ahvaz Jundishapur University of Medical Sciences, Ahvaz

8 School of Medicine, Ahvaz Jundishapur University of Medical Sciences, Ahvaz

9 Department of Biology, Islamic Azad University, Sari Branch, Sari, Iran

10 1. Gorgan Congenital Malformations Research Center, Golestan University of Medical Sciences, Gorgan, Iran. 2. Ischemic Disorders Research Center, Golestan University of Medical Sciences, Gorgan, Iran. 3. Department of Medical Genetics, School of Advanced Technologies in Medicine, Golestan University of Medical Sciences, Gorgan, Iran.

Abstract

Meningitis can quickly become a life-threatening sickness and therefore is considered a medical emergency. Viruses, after bacteria, are known as main pathogens involved in meningitis; therefore, we investigated the prevalence of viral meningitis worldwide and evaluated the clinical and preclinical features for rapid detection of viral meningitis. The results showed that the most prevalent viruses in viral meningitis are Enterovirus, Coxaci, Tick-borne encephalitis virus, Herpesviridae family; and the most prevalent viruses in aseptic meningitis are Echovirus, Enterovirus, Coxaci and HSV. The findings revealed differences in the prevalence of various viruses in these two types of meningitis, even though there was no significant difference in clinical manifestations between viral and bacterial meningitis. This indicates the importance of laboratory diagnostic methods for discriminating between these two types of meningitis.

Keywords

Full Text

1- INTRODUCTION

Meningitis is known as an inflammation in the meninges (the defensive membranes of brain and spinal cord) (1). A report by the Global Burden of Disease in 2015, showed that almost 8.7 million persons were living with meningitis worldwide which could lead to 379,000 deaths (2). Meningitis can quickly become a life-threatening illness due to inflammation in the central nervous system (CNS); hence, it is considered a health emergency (3). Meningitis can be caused by pathogens such as bacteria, viruses, fungi, protozoa and various non-infectious elements (i.e. drug allergies, chemical reactions, some cancers and inflammatory diseases like sarcoidosis) (4, 5). Several viruses could lead to meningitis, including enteroviruses, Herpes simplex virus type 1 (HSV-1) or 2 (HSV-2), varicella zoster (VZV), mumps virus, cytomegalovirus (CMV), Epstein–Barr virus (EBV), West Nile virus (WNV), Human herpesvirus 6 (HHV-6) and Tick-borne encephalitis virus (TBEV) (6). The term aseptic meningitis refers to patients who have the clinical and laboratory evidence for meningeal inflammation without the growth of pyogenic bacteria in cultures of Cerebrospinal fluid (CSF) (7). The viral meningitis is the most common form of the aseptic meningitis, although it can be caused by other etiologies including fungal infections, syphilis, Lyme disease, tuberculosis, drug allergies, and malignancies (8). Coxsackieviruses and echoviruses, two members of the enterovirus group accounted for almost 50% of aseptic meningitis mainly occur at summer and early fall (9). Although the EBV and HHV-6 cause various illnesses (10-13), diagnosis of acute meningitis is according to the mixture of distinctive clinical symptoms and the CSF outcome which are important in screening meningitis (14). Clinical symptoms and signs (i.e. severe headache, fever, neck stiffness, nausea, vomiting, altered consciousness, seizures, sleepiness, skin rash, and photophobia) are important factors in the screening of meningitis (15). The results of lumbar puncture (a needle is injected into the spinal canal to obtain a specimen of cerebrospinal fluid) can diagnose or rule out meningitis (16). Viral meningitis can be suspected, because of clinical features and CSF findings, but bacterial meningitis and viral meningitis cannot be clinically distinguished. Similarly, CSF results for bacterial and viral meningitis significantly overlap (17, 18). When the clinical symptoms and CSF tests of bacterial and viral meningitis overlap, the etiology is unknown. Therefore, a definitive detection of viral meningitis is based on negative CSF culture for routine bacterial pathogens and positive detection of a viral pathogen in CSF or the other patient specimens (19). In this study, we have tried to evaluate the clinical and preclinical features for detection and screening of viral meningitis. According to the recent studies, reports of the prevalence of viral meningitis are limited to specific geographic areas and till now there is not any comprehensive study regarding the prevalence of viral and aseptic meningitis. Based on our knowledge, there is no collected data regarding the epidemiology of viral meningitis all over the world. The exact data of the prevalence of viral meningitis could be helpful for preventing and controlling this emergent disease. As there is no precise assessment of the prevalence of viral meningitis worldwide, the present systematic review and meta-analysis provides useful insights on the prevalence and epidemiology of viral meningitis worldwide.

2- METHOD

2-1. Search strategies

From January 1, 2000 to January 1, 2017 all related studies were searched and collected by two independent reviewers from major databases including Embase, Medline (via PubMed), and Cochrane library. The gray literature and unpublished data were searched on the Web of Science, Cumulative Index to Nursing and Allied Health Literature (CINAHL), and WHO databases. The following search terms containing Medical Subject Headings (MeSH) keywords and their synonyms in title, abstract, or text were utilized: “Viral meningitides or viral meningitis’’, “Meningitis”,  “Meningitis, Aseptic”, “Central nervous system viral infections’’, “Central Nervous System Viral Diseases’’, “Cerebrospinal fluid or CSF”. Furthermore, we explored the references (forward citation) and citation lists (backward citation) of the regain reviews and original articles afterwards, we picked any extra scientific study (recommended with the Cochrane guideline) (20). Studies extracted through the search strategy were evaluated for eligibility using the titles and abstracts and by two independent researchers. The complete manuscripts of the articles collected by the title and abstract were checked by the same researchers (Table 1). The discrepancies were resolved by disquisition. This systematic review was updated in May 2017. This study was performed based on PRISMA guidelines (21).

2-2. Study selection

2-2.1. Inclusion criteria

Every published original article in English and other languages regarding the viral meningitides in patients with suspected meningitis with confirmatory standard lab tests were considered. We also found research studies in other languages rather than English and translated them by Google Translate (http://translate.google.com). Standard laboratory examinations for viral meningitides included: culturing, different molecular tests such as polymerase chain reaction (PCR), reverse transcriptase PCR, real-time PCR, nested PCR, nested real-time PCR (NRT PCR), multiplex PCR, restriction fragment length polymorphism (RFLP), serological assays such as enzyme-linked immunosorbent assay (ELISA), neutralization, and sequencing. The following laboratory feature analyses of viral meningitis were found in fifty eight studies: thirteen studies on CSF glucose (22-34), eight studies on CSF leukocyte (24, 27, 30-35), fifteen studies on CSF protein (22-25, 28-33, 35-39), five studies on CSF WBC (22, 28, 31, 36), twelve studies on the  duration of hospitalization (30, 36, 37, 40-48) and five studies accounted for PMN (neutrophil) (22, 24, 32, 39, 49) (Table 1).

2-3. Exclusion criteria

Patients with normal CSF were considered sub-acute or chronic meningitis. Articles which were not retrievable in full text and did not comprise adequate data in their abstracts like including only individual groups of patients, surveying other infectious meningitis rather than viral meningitis such as bacterial or fungal, and those that had not used standard methods were excluded. Twenty-five studies were excluded from epidemiological studies because their reports of meningitis were not separated from the other virus infections (29, 39, 45, 50-71). Also, Thirty-two studies were ruled out because of inappropriate data (26, 31, 42, 54, 72-99). This study focused on viruses and aseptic meningitis; therefore, studies on Mollaret's meningitis (a form of meningitis known as recurrent benign lymphocytic meningitis) were excluded.

2-4. Data extraction and Data collection

The papers were assessed for eligibility and were double-checked by two researchers to remove any eligibility error; finally, the appropriate articles were included in our meta-analysis. The data was extracted by 2 pundit independent researchers and were rechecked by a third professional researcher. Remarkably, contradictions between the investigators were discussed to obtain a distinct agreement. The following data were extracted from the chosen articles: first author’s name, publication date, min, max, and mean age, number of participants and sample size, viral meningitis diagnostic methods, time period and where the experiment took place, the season of sample collection, methodological quality, and study design. Evidently, if any of the mentioned data were not found in the publications, they were marked as “UNKnown, UN”. Data extraction and the finally chosen articles were assessed independently by two reviewers, and the differences were resolved by agreement.

2-5. Quality assessment

The quality of the articles was assessed by two independent researchers according to the adapted Critical Appraisal Checklist suggested via the Joanna Briggs Institute, and the discrepancies were decided upon, through agreement. The researchers answered a checklist containing seven enquiries for each paper. Each Yes-answered item acquired one score. Therefore, the total score for each paper varied from zero to seven.

2-6. Analysis

The outcomes were analyzed by the Comprehensive Meta-Analysis (V2.0, Biostat) software. The assessment points of the effect size, the prevalence of viral and aseptic meningitis, and its 95% confidence interval (95% CI) in all studies were evaluated. In addition, we analyzed the proportion of laboratory and clinical features. The controversial data was analyzed by Cochran's Q-statistic I2 squared. Some of the analyses demonstrated significant heterogeneity. Therefore, we used subgroups (meta-regression), and sensitivity tests to identify causes of heterogeneity. The modeling of random effects was conducted to assess pooled effects because of high heterogeneity. With the purpose of assessment of possible publication bias, Egger weighted regression was performed. The P-values less than 0.05 were considered significant for publication bias.

3- RESULT

3-1. Selection of the studies

A total of 50349 publications were reviewed in a systematic search and 49771 papers were excluded after the first screening.  Finally, 464 studies were included in the meta-analysis (Table 1).

3-2. Various virus proportions in viral and aseptic meningitis

Overall, the virus proportions in viral meningitis were 68.3 % (48-83.3) Enterovirus, 11 % (95% CI, 0.4-80) Coxaci, 10.6 % (95% CI, 0.7-65.3) Tick-borne encephalitis, 9 % (95% CI, 5-15.7) HSV, 5.3 % (95% CI, 1.3-19) Mumps, 4.6 % (95% CI, 1.9-1.-0.5) HHV6, 4.5 % (95% CI, 2.3-8.8), 4.2 % (95% CI, 2.4-7.3) VZV, and 3.4 % (95% CI, 0.9-12.4) EBV (Fig. S1, S2, S3, S4, S5, S6, S7, S8, S9, S10 in the supplementary materials).

The virus proportions in aseptic meningitis were 49.3 % (95% CI, 40.3-58.3) Enterovirus, 51.1 % (95% CI, 29.5-72.3) Echovirus, 26.4 % (95% CI, 9.6-55) Coxaci, 9.3 % (95% CI, 6.3-11.5) Mumps,7.3 % (95% CI, 5.8-9.2) VZV, 6.1 % (95% CI, 3-12) HHV1, 6 % (95% CI, 2.9-12) HHV2, 2.9 % (95% CI, 0.5-15.5) CMV, and 2.1 % (95% CI, 0.7-6.5) HHV6 (Table 2).

3-3. Proportion of Clinical features in viral meningitis

The clinical presentation of viral meningitis was characterized by, headache 84.7 % (95% CI, 79-89), nausea 56% (95% CI, 48.4-63), seizures 8.3% (95% CI, 4.5-14.7), photophobia 45.8% (95% CI, 38.3-53.4), rash 17% (95% CI, 12-23), neck stiffness 52.6% (95% CI, 46.4-58.7), vomiting 65.3% (95% CI, 60-70), and fever 72% (95% CI, 67.3-76). In addition, the duration of hospitalization was 4.23 % (95% CI, 3.1-5.27) days (Table 3).

3-4. Mean of laboratory findings in viral meningitis

Laboratory findings in CSF-culture positive samples were characterized by the increased CSF leukocytes counts [173.7 (cells/mm3), 95% CI 134-213], increased CSF protein [52.9 (mg/dl), 95% CI 40-65.8], decreased CSF glucose [57.15 (mg/dl), and 95% CI 25. 55-59.3], increased CSF WBC [246.17 (mm3), 95% CI 108.7-383.5], and increased PMN (neutrophil) [45.9 (106/l), 95% CI 30.8-61] (Table 4).

4- DISCUSSION

Among the elements mentioned, the virus is considered to be the leading cause of meningitis. Therefore, this study examined the prevalence of viral meningitis worldwide, and evaluated clinical symptoms quickly detecting viral meningitis. According to the previous studies, enteroviruses accounted for 85 to 95% of cases of viral meningitis (100), while group B coxsackieviruses and parechoviruses mainly associated with aseptic meningitis in infants under three months of age (99, 101, 102). Our results showed that the highest proportion of viruses in viral meningitis belongs to Enterovirus, Coxaci, Tick-borne encephalitis, HSV, Mumps, HHV6, CMV, VZV and EBV, respectively and the highest proportion of viruses in aseptic meningitis belongs to Echovirus, Enterovirus, Coxaci, HSV, Mumps, VZV, CMV, and HHV6. These results showed a difference in virus incidents in these two types of meningitis. Despite a lack of report for some herpes viruses, this virus family significantly causes viral and aseptic meningitis. Thus, since effective commercial medications are available for the treatment of herpes viruses such as acyclovir for HSV1, HSV2 and VZV and ganciclovir for CMV, a rapid and correct diagnosis could lead to the prevention of further disorders and the treatment of this infections (103).

Before the introduction of mumps vaccine in 1967, this virus was a common cause of viral meningitis, accounted for 10 and 20 percent of all cases but the results of this meta-analysis show that the virus accounts for 5.3% of viral meningitides.

Although bacterial meningitis and viral meningitis overlap in clinical symptoms, but one retrospective cohort study reported that nausea, vomiting, headache and neck stiffness were more common in viral meningitis in comparison to bacterial meningitis (viral versus bacterial: nausea: 79% versus 48%, P = 0.005; vomiting: 81% versus 52%, P = 0.009; headache: 78% versus 10%, P < 0.0001; neck stiffness: 88% versus 62%, P = 0.006) (104). This analysis showed that headache, fever, vomiting, nausea and neck stiffness were the most common clinical symptoms of viral meningitis. Therefore, the presence of them can somewhat contribute to the screening of viral meningitis.

In regard to the high heterogeneity, these clinical symptoms of viral meningitis cannot be used as an important factor in diagnosing this type of meningitis.  Fever, nausea, vomiting and imbalance are the most common clinical symptoms of bacterial meningitis. There is no significant difference in the clinical manifestations of viral and bacterial meningitis (105), which indicates the importance of laboratory diagnostic methods for discriminating these two types of meningitis.

According to Table 4, the level of glucose in the cerebrospinal fluid of patients with viral meningitis is normal, while protein level is slightly higher than the normal range. The amount of white blood cells in the cerebrospinal fluid in people with viral meningitis is significantly higher than the normal range with leukocytes as a significant percentage of it. Our results similar to other studies indicate an increase of leukocytes in the CSF of viral meningitis (106). According to the previous reports, children with a CSF WBC count of <500/microL with >50 percent mononuclear cells, normal or high CSF protein, normal CSF glucose, and negative gram stain are likely suspected viral meningitis (107, 108); hence, this laboratory finding can provide a support for a provisional diagnosis of viral meningitis.

Due to limitations in the number of publications of prevalence-based studies, we couldn’t report the global prevalence of aseptic and viral meningitis. The results of this study indicate that herpes viruses are one of the major causes of viral meningitis; and the presence of antiviral drugs against some of them indicates the importance of their rapid and accurate diagnosis. In addition, clinical signs are helpful in the screening of viral meningitis, but the final diagnosis is based on laboratory methods.

5- ACKNOWLEDGEMENT

We would like to thank the “Department of Microbiology, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran” for their kind cooperation. The authors received no specific funding for this work.

6- CONFLICTS OF INTEREST

None.

 

References

  1. Okokhere PO, Bankole IA, Iruolagbe CO, Muoebonam BE, Okonofua MO, Dawodu SO, Akpede GO. Aseptic Meningitis Caused by Lassa Virus: Case Series Report. Case reports in neurological medicine. 2016; 2016.
  2. Brian OO. Leveraging on Prompt Proactive and Preventive Integrated Strategies (PPPIS) for Meningitis Control in Nigeria: Getting it Right.
  3. Sharifi-Mood B, Khajeh A, Metanat M, Rasouli A. Epidemiology of Meningitis Studied at a University Hospital in Zahedan, South-Eastern Iran. International Journal of Infection. 2015; 2(2).
  4. Attia J, Hatala R, Cook DJ, Wong JG. Does this adult patient have acute meningitis? Jama. 1999; 282(2):175-81.
  5. Ginsberg L. Difficult and recurrent meningitis. Journal of Neurology, Neurosurgery & Psychiatry. 2004; 75(suppl 1):i16-i21.
  6. Ludlow M, Kortekaas J, Herden C, Hoffmann B, Tappe D, Trebst C, Griffin DE, Brindle HE, Solomon T, Brown AS, Riel D, Wolthers KC, Pajkrt D, Wohlsein P, Martina BE, Baumgärtner W, Verjans GM, Osterhaus A. Neurotropic virus infections as the cause of immediate and delayed neuropathology. Acta neuropathologica. 2016; 131(2):159-84.
  7. Parasuraman T, Frenia K, Romero J. Enteroviral Meningitis. Pharmacoeconomics. 2001; 19(1):3-12.
  8. Connolly KJ, Hammer SM. The acute aseptic meningitis syndrome. Infect Dis Clin North Am. 1990; 4(4):599-622.
  9. Kupila L, Vuorinen T, Vainionpää R, Hukkanen V, Marttila R, Kotilainen P. Etiology of aseptic meningitis and encephalitis in an adult population. Neurology. 2006; 66(1):75-80.
  10. Pormohammad A, Azimi T, Falah F, Faghihloo E. Relationship of Human Herpes Virus 6 and Multiple Sclerosis: A Systematic Review and Meta‐analysis. Journal of cellular physiology. 2017.
  11. Faghihloo E, Saremi MR, Mahabadi M, Akbari H, Saberfar E. Prevalence and characteristics of Epstein-Barr virus-associated gastric cancer in Iran. Archives of Iranian medicine. 2014; 17(11):767-70.
  12. Mahabadi M, Faghihiloo E, Alishiri GH, Ataee MH, Ataee RA. Detection of Epstein-Barr virus in synovial fluid of rheumatoid arthritis patients. Electronic physician. 2016; 8(3):2181.
  13. Mirzaei H, Goudarzi H, Eslami G, Faghihloo E. Role of Viruses in Gastrointestinal cancer. Journal of cellular physiology. 2017.
  14. Nagarathna S, Veenakumari H, Chandramuki A. Laboratory diagnosis of meningitis. Meningitis: InTech; 2012.
  15. Kumar R. Aseptic meningitis: diagnosis and management. The Indian Journal of Pediatrics. 2005; 72(1):57-63.
  16. Doherty CM, Forbes RB. Diagnostic lumbar puncture. The Ulster medical journal. 2014; 83(2):93.
  17. Logan SA, MacMahon E. Viral meningitis. Bmj. 2008; 336(7634):36-40.
  18. Negrini B, Kelleher KJ, Wald ER. Cerebrospinal fluid findings in aseptic versus bacterial meningitis. Pediatrics. 2000; 105(2):316-9.
  19. Cecilia Di Pentima M, Nordli Jr DR. Viral meningitis: Management, prognosis, and prevention in children.
  20. Van Tulder M, Furlan A, Bombardier C, Bouter L, Group EBotCCBR. Updated method guidelines for systematic reviews in the cochrane collaboration back review group. Spine. 2003; 28(12):1290-9.
  21. Liberati1 A, Altman DG, Tetzlaff J, Mulrow C, Gøtzsche PC, Ioannidis JP, Clarke M, Devereaux PJ, KleijnenJ, Moher D. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. PLoS medicine. 2009; 6(7):e1000100.
  22. ÇETİN K, EROL S, AKSOY H, TAŞYARAN MA. The relation of cerebrospinal fluid nitric oxide levels to prognosis and differential diagnosis of meningitis. Turkish Journal of Medical Sciences. 2002; 32(5):385-90.
  23. Caballero PJ, Escudero FM, Carretero SM, Pérez AV. Descriptive analysis of viral meningitis in a general hospital: differences in the characteristics between children and adults. Neurología (English Edition). 2011; 26(8):468-73.
  24. Jaeger F, Leroy J, Duchene F, Baty V, Baillet S, Estavoyer J, Hoen B. Validation of a diagnosis model for differentiating bacterial from viral meningitis in infants and children under 3.5 years of age. European Journal of Clinical Microbiology and Infectious Diseases. 2000; 19(6):418-21.
  25. M H Asadi SMM, A Esmaielzadeh. The relationship between serum CRP and spinal cord fluid with type of bacterial and viral meningitis in patients referred to Loghman Hakim hospitals, Mofid Hospital in Tehran and Valiasr in Zanjan. Journal of Zanjan University of Medical Sciences. 2001; 35:14-20.
  26. Miller S, Mateen FJ, Aksamit AJ. Herpes simplex virus 2 meningitis: a retrospective cohort study. Journal of neurovirology. 2013; 19(2):166-71.
  27. Raso SM, Echániz JS, Fernández JB, Ronco MV, Zache SC, Martín IG, editors. Tratamiento extrahospitalario de los niños con meningitis viral. Anales de Pediatría; 2000: Elsevier.
  28. Rasti M, Makvandi M, Neisi N, Azaran A, Rastegarvand N, Khalafkhany D, Jahangirnezhad E, Teimoori A, Hadian M, Shabani A, Shamsizadeh A, Nikfar R, Varnaseri M. Three cases of mumps virus and enterovirus coinfection in children with enteroviral meningitis. Medicine. 2016; 95 (49).
  29. S Abdoli Oskouie MB, A Malekian. Relation meningitis cases with MMR vaccine. Medical journal of tabriz university of medical sciences. 2006; 4:81-4.
  30. Shaker OG, Abdelhamid N. Detection of enteroviruses in pediatric patients with aseptic meningitis. Clinical neurology and neurosurgery. 2015; 129:67-71.
  31. Wang SM, Lei HY, Su LY, Wu JM, Yu CK, Wang JR, Liu CC. Cerebrospinal fluid cytokines in enterovirus 71 brain stem encephalitis and echovirus meningitis infections of varying severity. Clinical Microbiology and Infection. 2007; 13(7):677-82.
  32. Viallon A, Desseigne N, Marjollet O, Birynczyk A, Belin M, Guyomarch S, Borg J, Pozetto B, Claude Bertrand J, Zeni F. Meningitis in adult patients with a negative direct cerebrospinal fluid examination: value of cytochemical markers for differential diagnosis. Critical care. 2011; 15(3):R136.
  33. Rezaei M, Mamishi S, Mahmoudi S, Pourakbari B, Khotaei G, Daneshjou K, Hashemi N. Cerebrospinal fluid ferritin in children with viral and bacterial meningitis. British journal of biomedical science. 2013; 70(3):101-3.
  34. Kieslich M, Acconci D, Berger A, Jarisch A, Böhles H, Bollinger M, Jacobi G, Hernaiz Driever P. Diagnosis and outcome of neurotropic enterovirus infections in childhood. Klinische Pädiatrie. 2002; 214(6):327-31.
  35. Sulik A, Kroten A, Wojtkowska M, Oldak E. Increased levels of cytokines in cerebrospinal fluid of children with aseptic meningitis caused by mumps virus and echovirus 30. Scandinavian journal of immunology. 2014; 79(1): 68-72.
  36. Mohseni MM, Wilde JA. Viral meningitis: which patients can be discharged from the emergency department? The Journal of emergency medicine. 2012; 43(6): 1181-7.
  37. Nowak D, Boehmer R, Fuchs HH. A retrospective clinical, laboratory and outcome analysis in 43 cases of acute aseptic meningitis. European Journal of Neurology. 2003; 10(3):271-80.
  38. Soares CN, Castro MJC, Peralta JM, de Freitas MR, Puccioni-Sohler M. Is West Nile virus a potential cause of central nervous system infection in Brazil? Arquivos de neuro-psiquiatria. 2010; 68(5): 761-3.
  39. Tyler K, Pape J, Goody R, Corkill M, Kleinschmidt-DeMasters B. CSF findings in 250 patients with serologically confirmed West Nile virus meningitis and encephalitis. Neurology. 2006; 66(3): 361-5.
  40. Giulieri SG, Chapuis-Taillard C, Manuel O, Hugli O, Pinget C, Wasserfallen J-B, Sahli R, Jaton K, Marchetti O, Meylan P. Rapid detection of enterovirus in cerebrospinal fluid by a fully-automated PCR assay is associated with improved management of aseptic meningitis in adult patients. Journal of Clinical Virology. 2015; 62: 58-62.
  41. Han T-H, Chung J-Y, You SJ, Youn J-L, Shim G-H. Human parechovirus-3 infection in children, South Korea. Journal of Clinical Virology. 2013; 58(1): 194-9.
  42. Ihekwaba UK, Kudesia G, McKendrick MW. Clinical features of viral meningitis in adults: significant differences in cerebrospinal fluid findings among herpes simplex virus, varicella zoster virus, and enterovirus infections. Clinical infectious diseases. 2008; 47(6): 783-9.
  43. Juillet SM, Lion M, Pilmis B, Tomini E, Dommergues M-A, Laporte S, Foucaud P. Intérêt de l’amplification génique dans le sérum pour le diagnostic des méningites à entérovirus. Archives de pédiatrie. 2013; 20(6): 589-93.
  44. Meqdam MM, Khalousi MM, Al‐Shurman A. Enteroviral meningitis in northern Jordan: prevalence and association with clinical findings. Journal of medical virology. 2002; 66(2): 224-8.
  45. Murray KO, Baraniuk S, Resnick M, Arafat R, Kilborn C, Shallenberger R, York T L, Martinez D, Malkoff M, Elgawley N, McNeely W, Khuwaja SA. Clinical investigation of hospitalized human cases of West Nile virus infection in Houston, Texas, 2002–2004. Vector-Borne and Zoonotic Diseases. 2008; 8(2): 167-74.
  46. Österback R, Kalliokoski T, Lähdesmäki T, Peltola V, Ruuskanen O, Waris M. Echovirus 30 meningitis epidemic followed by an outbreak-specific RT-qPCR. Journal of Clinical Virology. 2015; 69: 7-11.
  47. Robinson CC, Willis M, Meagher A, Gieseker KE, Rotbart H, Glode MP. Impact of rapid polymerase chain reaction results on management of pediatric patients with enteroviral meningitis. The Pediatric infectious disease journal. 2002; 21(4): 283-6.
  48. Stellrecht K, Harding I, Hussain F, Mishrik N, Czap R, Lepow M, Veneziaa R.A. A one-step RT-PCR assay using an enzyme-linked detection system for the diagnosis of enterovirus meningitis. Journal of clinical virology. 2000; 17(3):143-9.
  49. Shahroodi MJG, Ghazvini K, Sadeghi R, Sasan MS. Enteroviral Meningitis in neonates and children of Mashhad, Iran. Jundishapur journal of microbiology. 2016; 9(5).
  50. Becerra JCL, Sieber R, Martinetti G, Costa ST, Meylan P, Bernasconi E. Infection of the central nervous system caused by varicella zoster virus reactivation: a retrospective case series study. International Journal of Infectious Diseases. 2013; 17(7):e529-e34.
  51. Bhangoo S, Chua R, Hammond C, Kimmel Z, Semenov I, Videnovic A, Kessler J, Borsody M. Focal neurological injury caused by West Nile virus infection may occur independent of patient age and premorbid health. Journal of the neurological sciences. 2005; 234(1):93-8.
  52. Gandelman-Marton R, Kimiagar I, Itzhaki A, Klein C, Theitler J, Rabey J. Electroencephalography findings in adult patients with West Nile virus—associated meningitis and meningoencephalitis. Clinical infectious diseases. 2003; 37(11):1573-8.
  53. Landry ML, Greenwold J, Vikram HR. Herpes simplex type-2 meningitis: presentation and lack of standardized therapy. The American journal of medicine. 2009; 122(7):688-91.
  54. Lee KY, Lee MS, Kim DB. Neurologic manifestations of enterovirus 71 infection in Korea. Journal of Korean medical science. 2016; 31(4):561-7.
  55. Simko JP, Caliendo AM, Hogle K, Versalovic J. Differences in laboratory findings for cerebrospinal fluid specimens obtained from patients with meningitis or encephalitis due to herpes simplex virus (HSV) documented by detection of HSV DNA. Clinical infectious diseases. 2002; 35(4):414-9.
  56. Varani S, Gelsomino F, Bartoletti M, Viale P, Mastroianni A, Briganti E, Ortolani P, Albertini F, Calzetti C, Prati F, Cenni P, Castellani G, Morini S, Rossini G, Landini MP, Sambri V. Meningitis caused by toscana virus is associated with strong antiviral response in the cns and altered frequency of blood antigen-presenting cells. Viruses. 2015; 7(11):5831-43.
  57. Vollbach S, Müller A, Drexler JF, Simon A, Drosten C, Eis-Hübinger AM, Panning M. Prevalence, type and concentration of human enterovirus and parechovirus in cerebrospinal fluid samples of pediatric patients over a 10-year period: a retrospective study. Virology journal. 2015; 12(1):199.
  58. Wang J-R, Tsai H-P, Huang S-W, Kuo P-H, Kiang D, Liu C-C. Laboratory diagnosis and genetic analysis of an echovirus 30-associated outbreak of aseptic meningitis in Taiwan in 2001. Journal of clinical microbiology. 2002; 40(12):4439-44.
  59. Haukali Omland L, Faber Vestergaard B, Heugh Wandall J. Herpes simplex virus type 2 infections of the central nervous system: a retrospective study of 49 patients. Scandinavian journal of infectious diseases. 2008; 40(1):59-62.
  60. Aberle SW, Aberle JH, Steininger C, Puchhammer-Stöckl E. Quantitative real time PCR detection of Varicella-zoster virus DNA in cerebrospinal fluid in patients with neurological disease. Medical microbiology and immunology. 2005; 194(1-2):7-12.
  61. Ansari A, Li S, Abzug MJ, Weinberg A. Human Herpesviruses 6 and 7 and Central Nervous System Infection in Children1. Emerging infectious diseases. 2004; 10(8):1450.
  62. Kaewpoowat Q, Salazar L, Aguilera E, Wootton SH, Hasbun R. Herpes simplex and varicella zoster CNS infections: clinical presentations, treatments and outcomes. Infection. 2016; 44(3):337-45.
  63. M S Sasan MHS. Aseptic meningitis after vaccine MMR in infants mashhad. Medical journal of mashhad university of medical sciences. 2010; 3:163-8.
  64. Meylan S, Robert D, Estrade C, Grimbuehler V, Péter O, Meylan PR, Sahli R. Real-time PCR for type-specific identification of herpes simplex in clinical samples: evaluation of type-specific results in the context of CNS diseases. Journal of Clinical Virology. 2008; 41(2):87-91.
  65. Murphy RF, Caliendo AM. Relative quantity of cerebrospinal fluid herpes simplex virus DNA in adult cases of encephalitis and meningitis. American journal of clinical pathology. 2009; 132(5):687-90.
  66. Nagai T, Okafuji T, Miyazaki C, Ito Y, Kamada M, Kumagai T, Yuri K, Sakiyama H, Miyata A, Ihara T, Ochiai H, Shimomura K, Suzuki E, Torigoe S, Igarashi M, Kase T, Okuno Y, Nakayama T. A comparative study of the incidence of aseptic meningitis in symptomatic natural mumps patients and monovalent mumps vaccine recipients in Japan. Vaccine. 2007; 25(14):2742-7.
  67. Ortner B, Huang CW, Schmid D, Mutz I, Wewalka G, Allerberger F, Yang JY, Huemer HP. Epidemiology of enterovirus types causing neurological disease in Austria 1999–2007: detection of clusters of echovirus 30 and enterovirus 71 and analysis of prevalent genotypes. Journal of medical virology. 2009; 81(2):317-24.
  68. Persson A, Bergström T, Lindh M, Namvar L, Studahl M. Varicella-zoster virus CNS disease—viral load, clinical manifestations and sequels. Journal of clinical virology. 2009; 46(3):249-53.
  69. Shah SS, Hodinka RL, Turnquist JL, Elliott MR, Coffin SE. Cerebrospinal fluid mononuclear cell predominance is not related to symptom duration in children with enteroviral meningitis. The Journal of pediatrics. 2006; 148(1):118-21.
  70. Trallero G, Casas I, Avellon A, Pérez C, Tenorio A, De La Loma A. First epidemic of aseptic meningitis due to echovirus type 13 among Spanish children. Epidemiology & Infection. 2003; 130(2):251-6.
  71. Tsai H-P, Huang S-W, Wu F-L, Kuo P-H, Wang S-M, Liu C-C, Su JJ, Wang JR. An echovirus 18-associated outbreak of aseptic meningitis in Taiwan: epidemiology and diagnostic and genetic aspects. Journal of medical microbiology. 2011; 60(9):1360-5.
  72. Boriskin YS, Rice PS, Stabler RA, Hinds J, Al-Ghusein H, Vass K, Butcher PD. DNA microarrays for virus detection in cases of central nervous system infection. Journal of clinical microbiology. 2004; 42(12):5811-8.
  73. Chomel J-J, Antona D, Thouvenot D, Lina B. Three ECHOvirus serotypes responsible for outbreak of aseptic meningitis in Rhone-Alpes region, France. European Journal of Clinical Microbiology and Infectious Diseases. 2003; 22(3):191-3.
  74. Faustini A, Fano V, Muscillo M, Zaniratti S, La Rosa G, Tribuzi L, Perucci CA. An outbreak of aseptic meningitis due to echovirus 30 associated with attending school and swimming in pools. International journal of infectious diseases. 2006; 10(4):291-7.
  75. Forsgren M, Sköldenberg B, Aurelius E, Gille E. Neurologic morbidity after herpes simplex virus type 2 meningitis: a retrospective study of 40 patients. Scandinavian journal of infectious diseases. 2002; 34(4):278-83.
  76. Liu N, Jia L, Yin J, Wu Z, Wang Z, Li P, Hao R, Wang L, Wang Y, Qiu S, Song H. An outbreak of aseptic meningitis caused by a distinct lineage of coxsackievirus B5 in China. International Journal of Infectious Diseases. 2014; 23:101-4.
  77. Mao N, Zhao L, Zhu Z, Chen X, Zhou S, Zhang Y, Cui A, Ji Y, Xu S, Xu W. An aseptic meningitis outbreak caused by echovirus 6 in Anhui province, China. Journal of medical virology. 2010; 82(3):441-5.
  78. Markey PG, Davis JS, Harnett GB, Williams SH, Speers DJ. Meningitis and a febrile vomiting illness caused by echovirus type 4, Northern Territory, Australia. Emerging infectious diseases. 2010; 16(1):63.
  79. Nishikawa M, Matsubara T, Yoshitomi T, Ichiyama T, Hayashi T, Furukawa S. Abnormalities of brain perfusion in echovirus type 30 meningitis. Journal of the neurological sciences. 2000; 179(1):122-6.
  80. Park SK, Park B, Ki M, Kim H, Lee K, Jung C, Sohn YM, Choi SM, Kim DK, Lee DS, Tae Ko J, Kim MK, Cheong HK. Transmission of seasonal outbreak of childhood enteroviral aseptic meningitis and hand-foot-mouth disease. Journal of Korean medical science. 2010; 25(5):677-83.
  81. Rajasingham R, Rhein J, Klammer K, Musubire A, Nabeta H, Akampurira A, Mossel EC, Williams DA, Boxrud DJ, Crabtree MB, Miller BR, Rolfes MA, Tengsupakul S, Andama AO, Meya DB, Boulware DR. Epidemiology of meningitis in an HIV-infected Ugandan cohort. The American journal of tropical medicine and hygiene. 2015; 92(2):274-9.
  82. Rasti M, Samarbaf-Zadeh A, Makvandi M, Neisi N, Shamsizadeh A. Relative Frequency of Echovirus 30 in Patients Suffering From Enterovirus Meningitis in Ahvaz. Jundishapur Journal of Microbiology. 2013; 6(2):157-61.
  83. Sojka M, Wsolova L, Petrovičová A. Coxsackieviral infections involved in aseptic meningitis: a study in Slovakia from 2005 to 2009. Euro Surveill. 2011; 16.
  84. Adler-Shohet FC, Cheung MM, Hill M, Lieberman JM. Aseptic meningitis in infants younger than six months of age hospitalized with urinary tract infections. The Pediatric infectious disease journal. 2003; 22(12):1039-42.
  85. Ćosić G, Đurić P, Milošević V, Đekić J, Čanak G, Turkulov V. Ongoing outbreak of aseptic meningitis associated with echovirus type 30 in the City of Novi Sad, Autonomous Province of Vojvodina, Serbia, June–July 2010. Eurosurveillance. 2010; 15(32):19638.
  86. Czupryna P, Niczyporuk J, Samorek-Salamonowicz E, Moniuszko A, Dunaj J, Zajkowska J, Pancewicz SA. Detection of West Nile Virus RNA in patients with meningitis in Podlaskie Province. Przeglad epidemiologiczny. 2014; 68(1):17-20, 109-11.
  87. Di Nicuolo G, Pagliano P, Battisti S, Starace M, Mininni V, Attanasio V, Faella FS. Toscana virus central nervous system infections in southern Italy. Journal of clinical microbiology. 2005; 43(12):6186-8.
  88. Dos Santos GP, Skraba I, Oliveira D, Lima AA, de Melo MMM, Kmetzsch CI, Costa E, Silva E. Enterovirus meningitis in Brazil, 1998–2003. Journal of medical virology. 2006; 78(1):98-104.
  89. Holmes CW, Koo SS, Osman H, Wilson S, Xerry J, Gallimore CI, Allen DJ, Tang JW. Predominance of enterovirus B and echovirus 30 as cause of viral meningitis in a UK population. Journal of clinical virology. 2016; 81:90-3.
  90. Kirschke DL, Jones TF, Buckingham SC, Craig AS, Schaffner W. Outbreak of aseptic meningitis associated with echovirus 13. The Pediatric infectious disease journal. 2002; 21(11):1034-8.
  91. Liu S-C, Lee P-I, Lee C-Y, Wang J-D, Chiang B-L, Chou M-C. Different cytokine levels in enterovirus meningitis and encephalitis. Infectious Diseases in Clinical Practice. 2005; 13(5):241-6.
  92. Mladenova Z, Buttinelli G, Dikova A, Stoyanova A, Troyancheva M, Komitova R, Stoycheva M, Pekova L, Parmakova K, Fiore L. Aseptic meningitis outbreak caused by echovirus 30 in two regions in Bulgaria, May–August 2012. Epidemiology & Infection. 2014; 142(10):2159-65.
  93. Papa A, Dumaidi K, Franzidou F, Antoniadis A. Genetic variation of coxsackievirus B5 strains associated with aseptic meningitis in Greece. Clinical microbiology and infection. 2006; 12(7):688-91.
  94. Rottenstreich A, Oz ZK, Oren I. Association between viral load of varicella zoster virus in cerebrospinal fluid and the clinical course of central nervous system infection. Diagnostic microbiology and infectious disease. 2014; 79(2):174-7.
  95. Science M, MacGregor D, Richardson SE, Mahant S, Tran D, Bitnun A. Central nervous system complications of varicella-zoster virus. The Journal of pediatrics. 2014; 165(4):779-85.
  96. Taghavi n. Study in changes of CSF in 50 patients with bacterial and viral and TB meningitis in booali hospital. 2002.
  97. Volle R, Bailly J-L, Mirand A, Pereira B, Marque-Juillet S, Chambon M, Regagnon C, Brebion A, Henquell C, Peigue-Lafeuille H, Archimbaud C. Variations in cerebrospinal fluid viral loads among enterovirus genotypes in patients hospitalized with laboratory-confirmed meningitis due to enterovirus. The Journal of infectious diseases. 2014; 210(4):576-84.
  98. Wolfaardt M, Büchner A, Myburgh M, Avenant T, Du Plessis NM, Taylor MB. Molecular characterisation of enteroviruses and clinical findings from a cluster of paediatric viral meningitis cases in Tshwane, South Africa 2010–2011. Journal of Clinical Virology. 2014; 61(3):400-5.
  99. Wolthers KC, Benschop KS, Schinkel J, Molenkamp R, Bergevoet RM, Spijkerman IJ, Kraakman HC, Pajkrt D. Human parechoviruses as an important viral cause of sepsis like illness and meningitis in young children. Clinical Infectious Diseases. 2008; 47(3):358-63.
  100. Rotbart HA. Viral meningitis. Seminars in neurology. 2000; 20(3):277-92.
  101. Kaplan MH, Klein SW, McPhee J, Harper RG. Group B coxsackievirus infections in infants younger than three months of age: a serious childhood illness. Reviews of infectious diseases. 1983; 5(6):1019-32.
  102. Khetsuriani N, LaMonte A, Oberste MS, Pallansch M. Neonatal enterovirus infections reported to the national enterovirus surveillance system in the United States, 1983–2003. The Pediatric infectious disease journal. 2006; 25(10):889-93.
  103. Britton P, Jones C. Central nervous system herpesvirus infections. Paediatrics and Child Health. 2014; 24(6):248-54.
  104. De Cauwer HG, Eykens L, Hellinckx J, Mortelmans LJ. Differential diagnosis between viral and bacterial meningitis in children. European journal of emergency medicine: official journal of the European Society for Emergency Medicine. 2007; 14(6):343-7.
  105. Houri H, Pormohammad A, Riahi SM, Nasiri MJ, Fallah F, Dabiri H, Pouriran R. Acute bacterial meningitis in Iran: Systematic review and meta-analysis. PloS one. 2017; 12(2):e0169617.
  106. Almeida SMd, Nogueira MB, Raboni SM, Vidal LR. Laboratorial diagnosis of lymphocytic meningitis. Brazilian Journal of Infectious Diseases. 2007; 11(5):489-95.
  107. Jaffe M, Srugo I, Tirosh E, Colin A, Tal Y. The ameliorating effect of lumbar puncture in viral meningitis. American Journal of Diseases of Children. 1989; 143(6):682-5.
  108. Seiden JA, Zorc JJ, Hodinka RL, Shah SS. Lack of cerebrospinal fluid pleocytosis in young infants with enterovirus infections of the central nervous system. Pediatric emergency care. 2010; 26(2):77-81.
International Journal of Pediatrics
Volume 10, Issue 4
April 2022
Pages 15865-15880

Files

Share

How to cite

Statistics