Characterisation of group A streptococcal (GAS) isolates from children with tic disorders
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1 Indian J Med Res 119 (Suppl) May 2004, pp Characterisation of group A streptococcal (GAS) isolates from children with tic disorders R. Creti, F. Cardona*, M. Pataracchia, C. von Hunolstein, G. Cundari*, A. Romano* & G. Orefici Istituto di Sanità, & Department of Child Neuropsychiatry, University La Sapienza, Rome, Italy Received August 6, 2003 Background & objectives: An association between the onset or recrudescence of some neuropsychiatric disorders in children such as tic disorders and group A streptococcal (GAS) infections has been suggested. No information is available on the characterization of GAS strains associated with such disorders. The present study was undertaken to characterize the GAS strains isolated from children with tic disorders and to determine and correlate the antistreptolysin O (ASO) titre with the presence of GAS. Methods: During , 368 children with tic disorders were investigated for possible exposition to streptococcal antigens. All children, at the time of the first visit and during the follow up visits were apparently healthy and showed no clinical evidence of streptococcal infections or post streptococcal sequelae. Blood and throat swab samples were collected and serological and bacteriological tests done. The isolates obtained were investigated for T pattern, M protein and emm type, as well as for the production of protease. Results: Of the 800 throat swabs studied 100, corresponding to 67 patients, were positive for GAS; 49 children were found positive for GAS only once during the study, 18 had more than one sample positive for different serotypes, 8 were positive twice or more for the same type. ASO titres of these children were, in general, elevated. Five types, namely type M12, 3, 13, 11, 1, accounted for 39 per cent of the isolates, M12 being the most common, but a large number of different types were also found. A large number of isolates (62%) showed an elevated prodution of protease in the casein plate assay. Interpretation & conclusion: Despite the high level of ASO titres found, the results were not in favour of a particular virulence or invasivity of the isolates. Only a few colonies per sample were found indicating that factors different from the microbial virulence play a role in this type of disease. Key words Antistreptolysin O titre - emm typing - fic disorder - group A streptococcal infection In recent years, existence of an association between the onset or the recrudescence of some neuropsychiatric disorders in children (tics and/or obsessive compulsive disorders) and group A Streptococcal (GAS) infections has been suggested 1. As supporting evidence, a temporal relationship between these neuropsychiatric symptoms and signs of GAS infections (i.e., rise of antistreptolysin O (ASO) antibody and/or anti DNAse B titres or positive throat swabs) in a subset of patients has been reported 1. By analogy with Sydenham s chorea, a pathogenic mechanism consisting of an autoimmune process against structures of human central nervous system was hypothesized and the acronym of PANDAS (pediatric autoimmune neuropsychiatric disorders associated with streptococcal infection) was coined 1. However, the concept of PANDAS was not generally accepted and received many criticisms, mainly due to the absence of prospective studies 2,3. 174
2 CRETI et al : GAS STRAINS FROM CHILDREN WITH TIC DISORDERS Up to now, only two relevant studies on PANDAS patients have been published 4,5. In both these studies, little attention has been paid to the microbiological aspects providing some information on ASO titres and characterization of the GAS strains associated with the diagnosis of PANDAS was not done. 175 and nalidixic acid 7.5 µg/ml). The second swab was immersed in 2 ml of Todd-Hewitt broth (Oxoid, Milan, Italy) and transported to the WHO Collaborating Center laboratory, (Rome) where pour plates were performed. Growth of GAS was screened by using bacitracin test and confirmed by latex agglutination 6. The present study was undertaken with the objective to characterize the GAS strains isolated during a 5 yr period ( ) in a population of children with tics that was also examined for clinical and laboratory signs of streptococcal infections and to verify if the presence of GAS in the throat swab was correlated with higher ASO titres, and if specific serotypes could be isolated in this children population. Material & Methods Between March 1996 and December 2001, a population of 368 consecutive children (age 9.04 ± 2.7 yr, range yr, 318 male 50 females) with tics was studied at the outpatient division of the Developmental Neuropsychiatric Department of the University of Rome La Sapienza. Besides the complete physical and neurological examination of the children, blood samples and throat swab specimens were collected. Laboratory tests were performed, including complete blood count and erythrocyte sedimentation rate (ESR). Specific tests for intercurrent (culture of throat swab specimen) or antecedent (measurement of O antistreptolysin titre) GAS infections were also performed. Each patient was examined at least twice during the study, but more frequently in case of recrudescence of the neurological symptoms. ASO titres higher than 407 IU were considered abnormal. This cut-off was based on the finding of a previous study 6 where this value was found to be 2 SD higher than the mean value obtained in a normal control group of children of same age group seen at the time of the study. Bacteriological evaluation: Samples were taken in duplicate by swabbing tonsils and the posterior pharynx. One swab was streaked onto Columbia agar plates with 5 per cent sheep blood and CNA (colimycin, 5 µg/ml Serological typing: GAS isolates were serologically typed following the WHO recommendations by T-pattern typing sera (Serapharma, Praha, Czech Republic) and, on the basis of the results of serum opacity factor test 7, finally typed by M-protein agglutination. Currently, 29 M types can be identified in our laboratory. emm typing: emm typing was performed on all untypable strains by M-protein agglutination. DNA was prepared by suspending an abundant loop of an overnight culture in 1000 µl water. Sequence and primers were used according to the CDC protocol for emm typing 8. According to the CDC protocol, a sequence was considered to belong to a specific emm gene (or to a sequence type) allele when, over the first 160 bases of sequence, it had 95 per cent or greater identity with that of the reference emm gene. Protease activity: Protease activity was tested using the casein plate assay 9. Isolates were classified as no producers, low producers (<10 mm diameter) and high producers (>10 mm diameter). Statistical analysis: Data were analysed using X 2 test. Results None of the children examined, seen either during a routine check up or because of a recrudescence of the neurological symptoms, showed clinical signs of streptococcal infections. Of the 368 children seen during the study, 67 (53 males, 14 females; 18 %) had one or more throat swab positive for GAS. In total, 800 swabs samples were examined, 100 (12.5%) were positive for GAS. Forty nine children had only one swab positive for GAS. Of the 18 children with two or more GAS positive swabs, 8 were found to carry the same serotype while 10 had a different type. Laboratory tests showed that, in 15 (23%) of GAS positive children, GAS positivity was associated with
3 176 INDIAN J MED RES (SUPPL) MAY 2004 Fig.1. ASO titres in children with tics and GAS positive throat swab. Fig.2. ASO titres in children with tics and negative throat swab.
4 CRETI et al : GAS STRAINS FROM CHILDREN WITH TIC DISORDERS 177 Table I. Characteristics of children with tics Parameters GAS positive GAS negative children (n=67) children (n=301) ASO titre > 407 (IU) 41 (61.2%)** 108 (35.8%) Mean ASO titre (IU) 499 ± 328** 367 ± 270 ESR > (22.4%)* 36 (11.9%) Leukocytosis (> WBC) 4 (5.9) ND ASO, anti streptolysin O; ESR, erythrocyte sedimentation rate; ND, not detected P*<0.005; **< compared to GAS negative children Table II. GAS types isolated in patients with tics (100 isolates) and in patients with pharyngitis during the same time period (114 isolates) Types Percentages Tics Pharyngitis 10 M M M M13 7 NF M M M M M M2 4 NF M M M66 3 NF M M M18 3 NF M9 3 NF M M M25, M61, M62, M81, M102, M50, STC839 1 NF NF, not found. Superscript numeral denotes reference number an ESR higher than 16, in comparison with 36 (11.9%) GAS negative children. Forty one (61%) of GASpositive and 108 (35.8%) of GAS-negative children (P<0.0001) (39% of the whole population examined) had ASO titres higher than 407 IU. The mean value for ASO titres was 499 ± 328 IU in GAS-positive and 367 ± 270 IU in GAS-negative children (Table I). Both these values were significantly higher than the mean ASO titre reported in a previous study in our control population (155 ± 126 IU) 6. No significant variation in ASO titres distribution was found during the study period (Figs 1 and 2). In 18 children with more than one swab sample positive for GAS, no differences were found in ASO titres between children bearing the same serotype of the first sample and children acquiring a new serotype. All isolates were typable by T agglutination pattern, but 41 per cent could not be typed by M protein sera available at the laboratory. All the untypable strains were typed by emm typing. The result of the typing showed that no specific serotypes could be found in this population. The isolates belonged to a wide range of types (Table II): the types more frequently isolated were M12 (15%), M3 (8%), M5 and M13 (7% each), M11 (6%), M4 (5%) but many other serotypes were also found. Type M89, frequently found in invasive infections during the last few years (unpublished observation), and type M4, often isolated in our country from patients with scarlet fever were scarcely represented. Moreover, this distribution was apparently different from that found in patients of pharyngitis 10, where the more frequent types were M12, M89, M4, M1 and M87. It should be noticed that in several cases (12%) strains typed only by emm typing were not typed by the homologous M serum. Among the most frequent serotypes, M3, M5 and M11 were in general associated to ASO titres higher than 407 IU, but statistical comparison with the other serotypes could not be performed due to small number of isolates. Irrespective of the serotype, a large number of isolates (about 60%) were high producers of protease, but no statistical differences in the protease production were found among the most frequent serotypes. Discussion Though none of the children seen during the study period showed, at the time of clinical evaluation, signs or
5 178 INDIAN J MED RES (SUPPL) MAY 2004 symptoms of an active streptococcal infection, 39 per cent of them had ASO titres significantly higher than in a normal population of the same age group. No other sign specifically indicating a streptococcal infection was detectable, though patients with elevated ESR (23%) were noticed. The percentage of GAS-positive children in the present study was not significantly higher than that found in a control population in a previous study (10-12%, unpublished data). Lack of symptoms and low rate of positivity for GAS, together with the low number of colonies per plate found (generally, <10), led us to assume that these children were only carriers. This assumption was supported by the wide pattern of serotypes found in GAS positive children, different from those found in patients with pharyngitis or other streptococcal diseases, and by a large number untypable isolates by the typing sera routinely used. Several (12 %) of these isolates were typable only by emm typing. It might be possible that these strains did not express the corresponding M protein, though bearing the gene for it. The definition of carrier (a subject colonized by a pathogen without clinical manifestations or immune response) is in contrast with the high number of children who showed elevated ASO titres at the beginning of the study or during the follow up, even if their throat swabs were never positive for GAS (36%). Moreover, the significant difference in ASO titres found between swab-positive and swab-negative children suggested a role played by the presence of GAS, independently from the number of colonies found in the swab. Could all the above facts indicate that even a very low throat colonisation rate (undetectable even by PCR), or a colonisation in other sites of the body or in parts of the throat not reachable by swabbing (i.e., tonsil criptae), might be responsible for the relevant antibody response to streptococcal O streptolysin? Besides the questions regarding the definition of PANDAS, the intriguing problem about the categorization of these children as carriers or as infected remained unanswered. In conclusion, the present work confirmed that children affected by tic disorders represented a population prone to having a high frequency of exposure to streptococcal infections or at least responding to that exposure with a strong and long lasting antibody production. The present data showed that a large variety of GAS serotypes seemed to be responsible for elevated ASO titres though difference in the ASO titres associated with the more frequent serotypes was found. References 1. Garvey MA, Giedd J, Swedo SE. PANDAS: the search for environmental triggers of pediatric neuropsychiatric disorders. Lesson from rheumatic fever. J Child Neurol 1998; 13 : Kaplan E. PANDAS? Or PAND? Or both? Or neither? Assessing a (possible?) temporal or pathogenetic relationship with the Group A streptococcal disease complex. Contemp Pediatr 2000; 17 : Shulman S. Pediatric autoimmune neuropsychiatric disorders associated with streptococci (PANDAS). Pediatr Infect Dis J 1999; 18 : Swedo SE, Leonard HL, Garvey M, Mittleman B, Allen AJ, Perlmutter S. Pediatric autoimmune neuropsychiatric disorders associated with streptococcal infections: clinical description of the first 50 cases. Am J Psychiatry 1998; 155 : Murphy ML, Pichichero ME. Prospective identification and treatment of children with pediatric autoimmune neuropsychiatric disorders associated with group A streptococcal infections. Arch Pediatr Adolesc Med 2002; 156 : Cardona F, Orefici G. Group A streptococcal infections and tic disorders in an Italian pediatric population. J Pediatr 2001; 138 : Johnson DR, Kaplan EL, Sramek J, Bicova R, Havlicek H, Motlova J, Kriz P. Laboratory diagnosis of streptococcal infections. Geneva: World Health Organization; 1996 p accessed on Hynes WL, Tagg LA. A simple plate assay for detection of group A streptococcal proteinase. J Microbiol Methods 1985; 4 : Dicuonzo G, Gherardi G, Lorino G, Angeletti S, Battistoni F, Bertuccini L. Group A streptococcal genotypes from pediatric throat isolates in Rome, Italy. J Clin Microbiol 2001; 39 : Reprint requests: Dr Graziella Orefici, Istituto Superiore di Sanità, Viale Regina Elena 299, Rome, Italy
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