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Prevalence of HHV-6 in cerebrospinal fluid of children younger than 2 years with febrile convulsion
 Setareh Mamishi1 MD, Laura Kamrani1 MD, Nazanin Zahra Shafiei Jandaghi 2PhD, Masoud Mohammadpour1 MD, Jila Yavarian*2 MD, PhD
Department of Pediatric, Pediatric Medical Center, Tehran University of Medical Sciences, Tehran, Iran
Virology department, School of Public Health, Tehran University of Medical Sciences
*Corresponding address: Jila Yavarian, MD, PhD.     yavarian@tums.ac.ir 
Virology department, School of Public Health, Tehran University of Medical Sciences, Porsina Ave, Keshavarz Blv., Tehran, Iran. Tel: 88962343; fax: 88962343.



	




Prevalence of HHV-6 in cerebrospinal fluid of children younger than 2 years with febrile convulsion
Abstract
Background: Febrile convulsion is a common disorder in children. Viral infections such as human herpes virus 6 (HHV-6) which results in roseola infantum may contribute in developing seizure. The objective of this study was determining the prevalence of HHV-6 by detecting DNA in cerebrospinal fluid (CSF) of children with febrile convulsion and without any rash of roseola infantum.
Methods: In this descriptive cross sectional study, CSF of 100 children younger than 2 years with febrile convulsion was evaluated for detecting HHV-6 DNA by PCR method. All of them were referred to emergency ward in Pediatric Medical Center since March 2010 to March 2011. General information, clinical manifestations, laboratory tests and outcomes were collected in the questionnaires.
Results: We evaluated 100 children including 59 males and 41 females. HHV-6 was detected from CSF in six patients (6%) by PCR method. Mean age was 8 months. All of them were younger than 12 months. The most common primary manifestation was fever alone. None of them had rash. Majority of cases has occurred in winter. We had no case of encephalitis and all of the patients recovered.
Conclusion: Based on the prevalence of roseola infantum in the children younger than 1 year with febrile convulsion, evaluation of CSF (detecting HHV-6 DNA by PCR) is recommended and regarding to the low frequency of bacterial meningitis in febrile convulsion cases, it is recommended to avoid irrational prescribed antibiotics.
Keywords: Human Herpes Virus 6; Febrile Convulsion; children; CSF

Introduction:
Febrile convulsion is the most common type of seizure  in  the children between 3 -60 months old [1,2].Its  frequency is 2-5%[3]. In recent years multiple investigations have been conducted for evaluating the role of viral infections in developing febrile convulsion[4]. Among viral infections, HHV-6 as a probable cause of febrile convulsion has been considered and its prevalence has been evaluated in various areas in the world [4-6].
Roseola infantum or exanthem subitum is a common infection due to HHV-6 in the infants. Classic form of roseola infantum is high grade fever that lasts for 3-5 days and maculopapular rash that appears subsequently after subsiding fever. This classic manifestation only appears in 15% of patients and mostly nonspecific manifestations such as fever , rhinorrhea , cough ,seizure ,irritability , lymphadenopathy  and nausea are developed [5,7].  Previous studies showed  that febrile convulsion is common during exanthem subitum  ADDIN EN.CITE <EndNote><Cite><Author>Krugman S</Author><RecNum>15</RecNum><record><rec-number>15</rec-number><foreign-keys><key app="EN" db-id="5ze5pr5rxszt9me2se9pftv2zetd0r59xtz2">15</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Krugman S, Katz SL, Gershon AA, Wilfert CM.Exanthem Surbitum (roseola infantum). In: Krugman S, Katz SL, Gershon AA, Eilfert CM, eds. Infectious diseases of children, 9th ed. St. Louis: CV Mosbey, 1992:377-80</author></authors></contributors><titles><title> </title></titles><dates></dates><urls></urls></record></Cite></EndNote>[8] . For years , investigators believed that fever is the cause of seizure in this infection , but recent studies have shown that HHV-6  is able to involve central nervous system during roseola disease ADDIN EN.CITE <EndNote><Cite><Author>Yamanishi K</Author><Year>1988 </Year><RecNum>12</RecNum><record><rec-number>12</rec-number><foreign-keys><key app="EN" db-id="5ze5pr5rxszt9me2se9pftv2zetd0r59xtz2">12</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Yamanishi K, Okuno T, Shiraki K, Takahashi M, Kondo T, Asano Y, Kurata T.</author></authors></contributors><titles><title>Identification of human herpesvirus-6 as a causal agent for exanthem subitum</title><secondary-title>Lancet</secondary-title></titles><periodical><full-title>Lancet</full-title></periodical><pages>1065-7.</pages><volume>14</volume><number>1</number><dates><year>1988 </year></dates><urls></urls></record></Cite><Cite><Author>Ishiguro N</Author><Year>1990 </Year><RecNum>16</RecNum><record><rec-number>16</rec-number><foreign-keys><key app="EN" db-id="5ze5pr5rxszt9me2se9pftv2zetd0r59xtz2">16</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Ishiguro N, Yamada S, Takahashi T, Takahashi Y, Togashi T, Okuno T, Yamanishi K.</author></authors></contributors><titles><title>Meningo-encephalitis associated with HHV-6 related exanthem subitum</title><secondary-title>Acta Paediatr Scand</secondary-title></titles><periodical><full-title>Acta Paediatr Scand</full-title></periodical><pages>987-9</pages><volume>79</volume><number>10</number><dates><year>1990 </year></dates><urls></urls></record></Cite></EndNote>[9-10].
For evaluating the prevalence of HHV-6 in the children with febrile convulsion we designed this cross sectional study and used PCR method for detecting HHV-6 DNA in cerebrospinal fluid. The results of our investigation would help us to deciding about applying molecular tests as a diagnostic method in pediatric febrile convulsion .Also, the results of this investigation help us to use antibiotics rationally in the febrile convulsion.
Materials and Methods:
Specimen collection
In this descriptive cross sectional study, 100 children younger than 2 years with febrile convulsion were enrolled. They were referred to emergency ward in Pediatric Medical Center. After obtaining informed consent from parents, cerebrospinal fluid was obtained from all of them and evaluated for analysis and detecting HHV-6 by PCR (polymerase chain reaction) method in virology department of Tehran University of Medical Sciences.
DNA extraction
DNA was extracted from 150 �L of samples using the Roche extraction kit according to the manufactures� instruction.
Primers
Primers designed based on conserved part of U22 gene of HHV-6 genome. Forward primer: 5�-TCGAAATAAGCATTAATAGGCACACT-3�and Reverse primer: 
5�- CGGAGTTAAGGCATTGGTTGA-3�.
Polymerase Chain Reaction
Each 50 �l PCR mixture contained 5 �l of 10X PCR buffer, 2 �l Mgcl2 50 mM, 1 �l dNTPs 10mM, 2.5 �l of each of the primers with 10pmol/ �l concentration, 0.4 �l of Taq DNA polymerase, 31.5 �l ddH2O and 5 �l of extracted DNA. The amplification process was conducted under following conditions: 94�C for 6 min; then 40 cycles of 94�C for 30s, 55�C for 30s, and 72�C for 45s; and finally 72�C for 7 min. Positive control was bought from Vircell company.
Statistical methods
General information and laboratory findings were collected in questionnaires and finally data were analyzed by SPSS-13.
Results:
We evaluated 100 children younger than 2 years in this study. They had referred to Pediatric Medical Center with fever and convulsion. All of them were undergone lumbar puncture for ruling out meningitis and encephalitis. HHV-6 was detected from CSF in six patients (6%) by PCR method. General information and laboratory findings on blood and CSF in all studied patients as well as HHV-6 positive patients have been shown in table1. 
Fifteen percent of patients mentioned history of previous seizure. Six patients (6%) had seizure about 48 hours before fever. Seven patients (7%) had vaccination about 48 hours before febrile convulsion including six cases with MMR vaccination and one child with influenza vaccination. Two cases (2%) had rash at the time of febrile convulsion. Gram positive diplococi was found in CSF gram staining in only one case. 
Among patients with HHV-6 positive, one case (16.6%) had pleocytosis (900 leucocytes including 60% lymphocytes and 40% polymorphoneuclears) and 20 red blood cells in �l; whereas , there was no RBC and WBC in CSF in the other patients (83.3%).
In Five patients (83.4%) with roseola, seizure was generalized tonic clonic whereas 1 case (16.6%) had atonic seizure. 
In the patients with HHV-6 positive, the youngest patient was 4 months and all of the patients were younger than 12 months. Exanthem subitus( classic rash for roseola infantum) was manifested in none of the patients. 
Discussion:
HHV-6 infection mostly occurs in early years of life. It�s most common manifestations are fever, rash and seizure[5].
In our study HHV-6 DNA was detected from 6% of CSF specimens obtained from 100 children younger than 2 years who were referred to Pediatric Medical Center. Results of our study were similar to several investigations in various areas worldwide. For instance, Ward and coworkers studied 200 children younger than 2 years with primary HHV-6 infection. They detected HHV-6 DNA  from CSF in 7% of cases[5].  Of course, in some studies the prevalence of HHV-6 has been lower or higher than our study. For example , in Tavakoli study in 2007, prevalence of HHV-6 DNA positivity in 1482 CSF specimens obtained from cases with meningitis or encephalitis was reported as 1.75%[6].  Also, in some investigations such as Bertolani study ,35% of patients with febrile convulsion were positive for HHV-6  ADDIN EN.CITE <EndNote><Cite><Author>Bertolani MF</Author><Year>1996 </Year><RecNum>6</RecNum><record><rec-number>6</rec-number><foreign-keys><key app="EN" db-id="5ze5pr5rxszt9me2se9pftv2zetd0r59xtz2">6</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author> Bertolani MF, Portolani M, Marotti F, Sabbattini AM, Chiossi C, Bandieri MR, Cavazzuti GB</author></authors></contributors><titles><title>A study of childhood febrile convulsions with particular reference to HHV-6 infection: pathogenic considerations</title><secondary-title>Childs Nerv Syst</secondary-title></titles><periodical><full-title>Childs Nerv Syst</full-title></periodical><pages>534-9</pages><volume>12</volume><number>9</number><dates><year>1996 </year></dates><urls></urls></record></Cite></EndNote>[11]. 
HHV-6 primary infection is associated with 10-20% of febrile convulsion in infants. Most of them do not experience rash .HHV-6 DNA was detected in  CSF of 6% children and adults with focal encephalitis with unknown origin[5]. 
Our results were comparable with the other studies which showed the peak acquisition of primary HHV6 infection, from 6 to 15 months of age. Before 6 months of age, there is a low rate (<10%) of primary HHV6 infection [5].
Similar to other investigations, none of patients with febrile convulsion and HHV-6 had exanthema subitus. In present study, mean of white blood cell was 12000 cell/mL with a relative Lymphocytosis. One of our cases has significant poleocytosis with predominacy of Lymphocyte in CSF. The CSF of other patients was normal (without RBC and WBC).
In Roseola, WBC counts of 8000 � 9000 cell/ml may be found during the 1st few days of fever in children. The CSF in children with HHV6 associated febrile seizures typically is normal. The CSF from rare cases of HHV6 associated meningoencephalitis and encephalitis is characterized by a mild pleocytosis with predominance of mononuclear cells, normal glucose and normal to slightly elevated protein [5].
In Yoshikawa study in 2009, 86 cases with exanthema subitum and encephalitis/encephalopathy were evaluated and HHV-6 DNA was detected in 21 patients ADDIN EN.CITE <EndNote><Cite><Author>Yoshikawa T</Author><Year>2009</Year><RecNum>3</RecNum><record><rec-number>3</rec-number><foreign-keys><key app="EN" db-id="5ze5pr5rxszt9me2se9pftv2zetd0r59xtz2">3</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author> Yoshikawa T, Ohashi M, Miyake F, et al</author></authors></contributors><titles><title>Exanthemsubitum - associated encephalitis: nation wide survey in japan</title><secondary-title>Pediatr.Neurol</secondary-title></titles><periodical><full-title>Pediatr.Neurol</full-title></periodical><pages>353 - 8</pages><volume>41</volume><dates><year>2009</year></dates><urls></urls></record></Cite></EndNote>[12].
In present study all of our patients survived and we had no death whereas in Yoshikawa study 2 cases of death occurred among 86 cases ADDIN EN.CITE <EndNote><Cite><Author>Yoshikawa T</Author><Year>2009</Year><RecNum>3</RecNum><record><rec-number>3</rec-number><foreign-keys><key app="EN" db-id="5ze5pr5rxszt9me2se9pftv2zetd0r59xtz2">3</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author> Yoshikawa T, Ohashi M, Miyake F, et al</author></authors></contributors><titles><title>Exanthemsubitum - associated encephalitis: nation wide survey in japan</title><secondary-title>Pediatr.Neurol</secondary-title></titles><periodical><full-title>Pediatr.Neurol</full-title></periodical><pages>353 - 8</pages><volume>41</volume><dates><year>2009</year></dates><urls></urls></record></Cite></EndNote>[13]. In another study on 138 patients with encephalitis, 9 cases was HHV-6 positive which four of them had complete recovery, 3 cases had neurological complications , one case had status epilepticus and one case died ADDIN EN.CITE <EndNote><Cite><Author>McCullers</Author><Year>1995</Year><RecNum>4</RecNum><record><rec-number>4</rec-number><foreign-keys><key app="EN" db-id="5ze5pr5rxszt9me2se9pftv2zetd0r59xtz2">4</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>McCullers, J. A., et al. </author></authors></contributors><titles><title>Human herpesvirus 6 is associated with focal encephalitis. </title><secondary-title>Clin. Infect. Dis.</secondary-title></titles><periodical><full-title>Clin. Infect. Dis.</full-title></periodical><pages>571-76</pages><volume> 21</volume><dates><year>1995</year></dates><urls></urls></record></Cite></EndNote>[14].
Suga and colleagues evaluated 21 children with HHV-6 infection and neurological complications (seizure and encephalitis). In their study HHV-6 DNA was detected in CSF by PCR method in 3 cases. One of them died immediately after admission and seizure was remained in one case as a complication ADDIN EN.CITE <EndNote><Cite><Author>Suga S</Author><Year>1993 Jun;().</Year><RecNum>5</RecNum><record><rec-number>5</rec-number><foreign-keys><key app="EN" db-id="5ze5pr5rxszt9me2se9pftv2zetd0r59xtz2">5</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Suga S, Yoshikawa T, Asano Y, Kozawa T, Nakashima T, Kobayashi I, Yazaki T, Yamamoto H, Kajita Y, Ozaki T. </author></authors></contributors><titles><title>Clinical and virological analyses of 21 infants with exanthem subitum (roseola infantum) and central nervous system complications. </title><secondary-title>Ann Neurol. </secondary-title></titles><periodical><full-title>Ann Neurol.</full-title></periodical><pages>597-603</pages><volume>33</volume><number>6</number><dates><year>1993 Jun;().</year></dates><urls></urls></record></Cite></EndNote>[15].
Conclusion
This study was a cross sectional descriptive study on immunocompetent children.  According to this study and the prevalence of roseola infantum in the children with febrile convulsion evaluation of CSF (detecting HHV-6 DNA by PCR) is recommended in children younger than 12 months old who admitted with febrile convulsion. Further studies on immunocompromised children are recommended for comparing results in immunocompetent and immunocompromised children. Because our sample size was small, more studies with larger number of participants are recommended for achieving more accurate results. Also, regarding to low frequency of bacterial meningitis in febrile convulsion cases, it is recommended to avoid irrational prescribed antibiotics.
Acknowledgments
The authors thank the entire staff of the National Influenza Center, School of Public Health, Tehran University of Medical Sciences.



References:
1.T�t�nc�olu S KN, Kepe L, Coker C, Berdeli A, Tekg�l H, et al (2001)Proinflammatory 
   cytokines, prostaglandins and zinc in febrile convulsions. Pediatr Int 43:235-239.
2. Gururaj VJ. (1980) Febrile seizure-Current concept. Clin Pediatr (Philadelphia)
   19:731- 738.
3. Joshi C WT, Patrick J, Prasad A (2005) Do clinical variables predict an abnormal 
   EEG in patients with complex febrile seizures? Seizure 14:429-434.
4. Millichap DJ MJ (2006) Viral infections in the etiology of febrile seizure. Pediatr 
   Neurol 35:165-172.
5. Kliegman, Robert M (2007) Nelson Text Book of pediatrics, 18ed. 1381-1382.
6.Tavakoli NP NS, Hull R (2007) Detection and typing of human herpes virus 6 by 
   molecular methods in specimens from patients diagnosed with encephalitis or
   meningitis. J Clin microbiology 45:3972 - 3978.
7. Yamanishi K OT, Shiraki K, Takahashi M, Kondo T, Asano Y,,et al (1988) 
   Identification of human herpesvirus-6 as a causal agent for exanthem subitum. Lancet 
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8. Asano Y, Yoshikawa T, Suga S, Yazaki T, Hata T, et al (1989) Viremia and
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9. Antonyrajah B, Mukundan D (2008) Fever without apparent source on clinical 
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10. Krugman S KS, Gershon AA, Wilfert CM (1992) Exanthem Surbitum (roseola 
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   of children, 9th ed. St. Louis: CV Mosbey:377-80. 
11. Ishiguro N YS, Takahashi T, Takahashi Y (1990) Meningo-encephalitis associated 
    with HHV-6 related exanthem subitum. Acta Paediatr Scand 79:987-989.
12. Bertolani MF PM, Marotti F, Sabbattini AM, Chiossi C, Bandieri MR,,et al (1996)A
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    central nervous system complications. Ann Neurol 33:597-603.









Table 1: General information and laboratory findings of all studied patients.
variablesAll children with febrile convulsion(n=100)Children with HHV-6 PCR positive(n=6) 
Gendermale59(59%)6(100%)female41(41%)0(0%) Mean of age11 months8 months 

SeasonSpring15(15%)0(0%)Summer5(5%)1(16.6%)Fall43(43%)2(33.3%)winter37(37%)3(50%)

Primary manifestations


 Fever98(98%)6(100%)Fever and diarrhea13(13%)0(0%)Fever and vomiting8(8%)0(0%)Fever and cough19(19%)1(16.6%)Fever and coryza14(14%)1(16.6%)
Episode of seizureOne episode81(81%)5(83.3%)More than one episode19(19%)1(16.6%)Interval between fever and convulsionLess than 24 hours87(87%)5(83.3%)More than 24 hours13(13%)1(16.6%)

Laboratory findingsWBC16679�11880 (cell/mm3)11986�8842 (cell/mm3)PMN52.1�19.3(%)45�7(%)Lymphocyte41.1�26.7(%)47�7(%)ESR77�16(mm/h)16�6(mm/h)
CSF      analysis  WBC(mean�SD)130�27(cell/mm3)RBC(mean�SD)3450�616(cell/ �l)Sugar(mean�SD)62�17(mg/dl)57�7(mg/dl)protein(mean�SD)22�30 (mg/dl)22�14(mg/dl)Encephalitis0(0%)0(0%)Complete recovery100(100%)6(100%)	

 ADDIN 









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