The Prevalence of β-haemolytic Streptococcal infection...

9
881 Current Trends in Biotechnology and Pharmacy Vol. 7 (4) 881-889 October 2013, ISSN 0973-8916 (Print), 2230-7303 (Online) Abstract The genus Streptococcus is comprised of a wide variety of both commensal and pathogenic gram-positive bacteria which are found to exhibit a wide range of hosts, including humans, horses, pigs and cows. Streptococcal infections can cause a wide range of diseases from mild infections to sever. Repeated infection results in the non-suppurative sequelae, acute rheumatic fever, and acute glomerulonephritis. Streptococcus remains sensitive to the antibiotic penicillin which can be administered as a means to treat infection or as prophylaxis. Rheumatic fever and rheumatic heart disease continue to ravage millions of people around the world. Children and adolescents of the developing countries are especially susceptible to this disease. The aim of this study is to assess the effect of invasive Streptococcal infection with an objective to determine the prevalence of streptococcal infection in school children of 5-15 years of age in Tripura, North Eastern part of India. From September 2012 - February 2013, a study was conducted on prospective population- based laboratory surveillance of Tripura school children with isolation of Streptococci from throat swab examination of both pharyngitis and non – pharyngitis cases. Throat swabs were collected from 1165 school children, randomly selected from 3 districts of Tripura. These swabs were cultured on blood agar and Mac Conkey plates. Out of 1165 swabs, 43 were alpha haemolytic, 4 were Grp. G (Streptococcus dysgalactiae subsp. equisimilis) and 1063 were of different types than streptococcus. The study present the results of the first prospective surveillance study of Streptococcal infections in north eastern part of India. Keywords: Acute rheumatic fever, Rheumatic heart disease, Impetigo; Pharyngitis, Post- streptococcal Glomerulonephritis Introduction A large genus of spherical or ovoid bacteria that are characteristically arranged in pairs or in chains resembling strings of beads. Many of the streptococci that constitute part of the normal flora of the mouth, throat, intestine, and skin are harmless commensal forms; other streptococci are highly pathogenic. The cells are gram-positive and can grow either anaerobically or aerobically, as they do not require oxygen for metabolic reactions. The group of β-hemolytic streptococci cause a wide spectrum of clinical diseases. Pharyngitis and associated complications are the most common clinical presentations for group A streptococci (GAS). Invasive GAS infections have increased world-wide during the past decade despite the organism remaining sensitive to penicillin and other commonly used Beta lactam antibiotics (1,2) Group B streptococci (GBS) are a leading cause of infection in neonates and pregnant women and have also been recognised as a cause of invasive diseases The Prevalence of β-haemolytic Streptococcal infection among School children in Tripura, North East India Nilratan Majumdar, Nupur Moitra*, Tapan Majumdar, Subrata Baidya, Anamika Nath Agartala Govt. Medical College, Agartala, Tripura - 799006, India *For Correspondence - [email protected] Prevalence of β-haemolytic Streptocoocal infection

Transcript of The Prevalence of β-haemolytic Streptococcal infection...

Page 1: The Prevalence of β-haemolytic Streptococcal infection ...abap.co.in/sites/default/files/Paper-7_14.pdf · gram-positive bacteria which are found to exhibit ... have become rare

881Current Trends in Biotechnology and PharmacyVol. 7 (4) 881-889 October 2013, ISSN 0973-8916 (Print), 2230-7303 (Online)

AbstractThe genus Streptococcus is comprised of

a wide variety of both commensal and pathogenicgram-positive bacteria which are found to exhibita wide range of hosts, including humans, horses,pigs and cows. Streptococcal infections cancause a wide range of diseases from mildinfections to sever. Repeated infection results inthe non-suppurative sequelae, acute rheumaticfever, and acute glomerulonephritis.Streptococcus remains sensitive to the antibioticpenicillin which can be administered as a meansto treat infection or as prophylaxis. Rheumaticfever and rheumatic heart disease continue toravage millions of people around the world.Children and adolescents of the developingcountries are especially susceptible to thisdisease. The aim of this study is to assess theeffect of invasive Streptococcal infection with anobjective to determine the prevalence of streptococcal infection in school children of 5-15years of age in Tripura, North Eastern part ofIndia. From September 2012 - February 2013, astudy was conducted on prospective population-based laboratory surveillance of Tripura schoolchildren with isolation of Streptococci from throatswab examination of both pharyngitis and non –pharyngitis cases. Throat swabs were collectedfrom 1165 school children, randomly selectedfrom 3 districts of Tripura. These swabs werecultured on blood agar and Mac Conkey plates.Out of 1165 swabs, 43 were alpha haemolytic, 4were Grp. G (Streptococcus dysgalactiae subsp.

equisimilis) and 1063 were of different types thanstreptococcus. The study present the results ofthe first prospective surveillance study ofStreptococcal infections in north eastern part ofIndia.

Keywords: Acute rheumatic fever, Rheumaticheart disease, Impetigo; Pharyngitis, Post-streptococcal Glomerulonephritis

IntroductionA large genus of spherical or ovoid bacteria

that are characteristically arranged in pairs or inchains resembling strings of beads. Many of thestreptococci that constitute part of the normalflora of the mouth, throat, intestine, and skin areharmless commensal forms; other streptococciare highly pathogenic. The cells are gram-positiveand can grow either anaerobically or aerobically,as they do not require oxygen for metabolicreactions.

The group of β-hemolytic streptococcicause a wide spectrum of clinical diseases.Pharyngitis and associated complications are themost common clinical presentations for group Astreptococci (GAS). Invasive GAS infectionshave increased world-wide during the pastdecade despite the organism remaining sensitiveto penicillin and other commonly used Betalactam antibiotics (1,2) Group B streptococci(GBS) are a leading cause of infection inneonates and pregnant women and have alsobeen recognised as a cause of invasive diseases

The Prevalence of βββββ-haemolytic Streptococcal infectionamong School children in Tripura, North East India

Nilratan Majumdar, Nupur Moitra*, Tapan Majumdar, Subrata Baidya,Anamika Nath

Agartala Govt. Medical College, Agartala, Tripura - 799006, India*For Correspondence - [email protected]

Prevalence of β-haemolytic Streptocoocal infection

Page 2: The Prevalence of β-haemolytic Streptococcal infection ...abap.co.in/sites/default/files/Paper-7_14.pdf · gram-positive bacteria which are found to exhibit ... have become rare

882Current Trends in Biotechnology and PharmacyVol. 7 (4) 881-889 October 2013, ISSN 0973-8916 (Print), 2230-7303 (Online)

in children and non-pregnant females (2, 3).Group C (GCS) and group G (GGS) streptococciare commensals of the pharynx, skin,gastrointestinal tract and female genital tract; the‘large colony’-forming strains resemble GAS interms of their virulence (2).

Streptococcal (strep) infections arecommunicable diseases that develop whenbacteria normally found on the skin or in theintestines, mouth, nose, reproductive tract, orurinary tract invade other parts of the body andcontaminate blood or tissue. In the last decade,there has been an increase in reports of seriousstreptococcal infections worldwide (4).Strepinfections are an occupational disease of schoolchildren between the ages of 5 and 15.

Streptococcal infections with an estimateddeath rate of over 500,000 individuals/year placeGAS among major human pathogens, exceededby HIV, Mycobacterium tuberculosis,Plasmodium falciparum and S. Pneumoniae andprobably comparable to rotavirus, measles,Haemophilus influenzae type b (Hib), andHepatitis B (5, 6).

Autoimmune response to infection withgroup A streptococcus is actually resulted intoRheumatic fever. Although the acute illnesscauses considerable morbidity, and somemortality, the major clinical and public healtheffects derive from long-term damage to the heartvalves, i.e., rheumatic heart disease (RHD). Overthe past century, as living conditions havebecome more hygienic and less crowded, andnutrition and access to medical care haveimproved, acute rheumatic fever (ARF) and RHDhave become rare in developed countries. But,rheumatic fever/ rheumatic heart disease is thecommonest cardiac disease in children andyoung adults and remains a major public healthproblem in developing countries (7).

GAS infection causes a substantial numberof illnesses and deaths, especially in thedeveloping world, withH” 500,000 deathsworldwide annually, attributable mostly to ARFand its sequelae, rheumatic heart disease, and

invasive infection (8). The epidemiology ofrheumatic fever (RF) is linked with that of GroupA beta-haemolytic streptococcal pharyngitis; bothhave a maximum incidence in the age group of5 – 15 years (9).

Recently worldwide population based datahas been reviewed to estimate the burden of GASdiseases and highlighted deficiencies in theavailable data (10). According to WHO, at least15.6 million people have RHD. Out of the 5,00,000 individuals who acquire ARF every year,3,00,000 go on to develop RHD; and 2,33,000deaths annually are attributable to ARF or RHD(11). The greatest burden in streptococcaldiseases is due to RHD, with a prevalence of atleast 15.6 million cases, with 2, 82,000 new casesand 2, 33,000 deaths each year (8). It isestimated that approximately 600,000 childrenless than 15 years of age are currently sufferingfrom chronic rheumatic heart disease, and thatapproximately 121,000 children are newlydiagnosed with acute rheumatic fever every year.

During the past two decades, ARF/RHDhas become uncommon health problems indeveloped countries. However, in third worldcountries such as India, the middle-east, sub-Saharan Africa, RF remains the leading causeof heart disease in children and young adults (12).In India, the disease burden of streptococcalinfections is considerable (13). Prevalence ofrheumatic heart disease and pharyngitis in India,varies from 1 to 5.4/1,000 (14) and 4.2% to13.7%, (15, 16) school-age children respectively,which is comparable to the rates reported fromdeveloped countries (17). Streptococcuspyogenes pharyngitis has a high prevalence inNorth India (18), whereas pyoderma is morefrequent in South India (19). In light of invasiveinfection, this is a completely neglected field inIndia and the only data available in the literatureis one retrospective study of invasive β-hemolyticstreptococcal infections (20). There areconsiderable socio-economic losses due to highcardiovascular mortality and morbidity of Indianpopulation (21). Incidence of streptococcalpharyngitis has been reported to be 8-18

Nilratan Majumdar et al

Page 3: The Prevalence of β-haemolytic Streptococcal infection ...abap.co.in/sites/default/files/Paper-7_14.pdf · gram-positive bacteria which are found to exhibit ... have become rare

883Current Trends in Biotechnology and PharmacyVol. 7 (4) 881-889 October 2013, ISSN 0973-8916 (Print), 2230-7303 (Online)

episodes per week per 1000 children in the agegroup of 5-15 years in India. Clinical scoring cardfor diagnosis of Group A Streptococcal sore throatwas developed (22). For the last 20 years, in Indiavarious research programmes have been carriedout at different centres mostly by ICMR and afew by WHO (23). Padmavati, in 1995 examinedthe status of RF & RHD in India with reference toboth prevalence and incidence based on the last10 years data and showed RHD in 1 to 5.4/1000and RF in 0.3-0.5/1000 children. Recently theburden of group A streptococcal disease in Indiawas addressed and treatment optionsstandardized by the World Health Organizationwas also discussed (13).

Streptococcal infections are extremelycommon due to the overall susceptibility of theseorganisms to antibiotics, especially penicillin.While infections caused by the Lancefield groupA streptococcus (GAS or Streptococcuspyogenes) have dominated the streptococcalmedical literature, Lancefield groups C and Gshare many microbiologic and clinicalcharacteristics with GAS (24). Work in the early20th century described S. pyogenes as anexclusively human pathogen and detailed thefrequency of carriers and the most characteristicinfections (25). The pioneering work of RebeccaLancefield led to the identification of a numberof groups of streptococci including A, C and G,producing haemolysis on sheep blood agar,exhibiting different biochemical properties andisolated from a variety of animal species (26).Classification methods based upon theLancefield methodology were established soonthereafter (27).

Among this diverse group, the group C andgroup G streptococci have assumed moreimportant clinical roles. For a number of reasons,they can be considered together, separate fromother members of the genus Streptococcus.Although less extensively studied, groups C andG streptococci are now appreciated to produceinfections quite similar to GAS although theymore commonly cause opportunistic andnosocomial infections than GAS. No. of recent

reports have described their association withstreptococcal syndromes generally caused byGAS such as streptococcal toxic shocksyndrome (STSS) (28) and acute rheumatic fever(ARF) (29). This assumes significance incountries like India where ARF continues to be amajor health problem.

β-hemolytic streptococcus belonging toGroup G (Streptococcus dysgalactiae subsp.Equisimilis) has attracted attention as possibleetiological agents of pharyngitis and post-streptococcal sequelae. Normally present on theskin, in the mouth and throat, and in the intestinesand genital tract, Group G Streptococcus (GGS)is most likely to lead to infection in alcoholics andin people who have cancer, diabetes mellitus,rheumatoid arthritis and other conditions thatsuppress immune-system activity.

Till date, no report is available in Tripuraabout the streptococcal infection in schoolchildren; hence the present study was designedto study the prevalence of β-hemolyticStreptococcal infection among School childrenin Tripura, North Eastern part of India. This studyalso provides an opportunity to establish thedirection of further investigations and to focusinterventions in Tripura.

Materials and MethodsPresent study was conducted after the

clearance of institutional ethical committee (IET)of Agartala Govt. Medical College and G. B. PHospital, Agartala. Cross sectional prospectivestudy was conducted to find out the GAS isolatesin Tripura, north eastern part of India at AgartalaGovt. Medical College and G. B. P Hospital,Agartala. The school children of 5-15 years agegroup in different schools from 3 districts ofTripura were considered for the study. Besides,patients were not included those who have takenantibiotics prior to this programme. In asepticcondition, throat swabs were collected induplicate using torch light under direct vision andwith the aid of a tongue depressor. Swabs wererubbed quickly but thoroughly over both tonsilsand tonsillar fossae. Since the sites of collection

Prevalence of β-haemolytic Streptocoocal infection

Page 4: The Prevalence of β-haemolytic Streptococcal infection ...abap.co.in/sites/default/files/Paper-7_14.pdf · gram-positive bacteria which are found to exhibit ... have become rare

884Current Trends in Biotechnology and PharmacyVol. 7 (4) 881-889 October 2013, ISSN 0973-8916 (Print), 2230-7303 (Online)

were not very far from the microbiology laboratoryso within two hours collected samples weretransported to the lab at room temperature.

Sample processing - Two types of plates wereused for culturing the sample; Blood agar andMac Conkey. Blood agar plates were kept incandle jar to have microaerophilic conditionwhereas the Mac Conkey plates were allowedto incubate for 24-48 hours at 37°C.

After 24-48 hours incubation, bacterialcolonies grown on blood agar plates showingbeta haemolytic colonies were further processedfrom the mixed colony and incubate at the sameatmosphere for 24 hours. Following day Gramstaining was prepared from the suspected betahaemolytic colonies and catalase test was also

performed for further confirmation. Based on thegram staining reaction and catalase test result,grouping was performed with the help of Streptexkit.

Streptococcal Grouping : Streptex agglutina-tion was carried out on colonies from purityplates. The extraction enzyme provided in theStreptex kit was reconstituted by the addition of11 ml sterile distilled water and was stored at4°C. With cultures from solid media, colonieswere suspended in 4 ml extraction enzyme andincubated at 37°C for 1 hr. The enzyme extractwas used for agglutination reactions without anycentrifugation. One drop of extract was added toone drop of each of the latex particles coatedwith group-specific immunoglobulin to groups A,B, C, D, F and G on the clean glass groupingtiles provided. After thorough mixing, the tile wasrocked gently for a maximum of one minute andthen the agglutination pattern was read. Whereagglutination was weak or occurred with morethan one latex suspension the test was repeatedusing the extraction enzyme alone in parallel withthe extract (30).

The number of positive throat swabs werethen analyzed and represented in tabular form.As a part of external quality control, the methodsand materials were supervised by expert of PGI,Chandigarh within our study period.

Fig. 1. Mac Conkey Plate

Fig. 3. Streptococcal colonies shown on BloodAgar Plate

Fig. 2. Plates kept in Candle Jar

Nilratan Majumdar et al

Page 5: The Prevalence of β-haemolytic Streptococcal infection ...abap.co.in/sites/default/files/Paper-7_14.pdf · gram-positive bacteria which are found to exhibit ... have become rare

885Current Trends in Biotechnology and PharmacyVol. 7 (4) 881-889 October 2013, ISSN 0973-8916 (Print), 2230-7303 (Online)

Fig. 4. Grouping of β-haemolytic colonies through Streptex Kit

Fig. 5. Distribution of Cases from September, 2012 to February 2013

Prevalence of β-haemolytic Streptocoocal infection

Page 6: The Prevalence of β-haemolytic Streptococcal infection ...abap.co.in/sites/default/files/Paper-7_14.pdf · gram-positive bacteria which are found to exhibit ... have become rare

886Current Trends in Biotechnology and PharmacyVol. 7 (4) 881-889 October 2013, ISSN 0973-8916 (Print), 2230-7303 (Online)

Results and DiscussionIn the present study, 1165 throat swabs

were randomly collected from school children of3 districts of Tripura within a 6 months’ timeperiod. Socio demographic profile of the studysubjects evaluated on the basis of sex, age andreligion which is shown in the figure 5. Out of1165 throat swabs, female children were more(608) in comparison to male (508). Whereas, 10-15 yrs children were much higher in number(1033) as compared to 5-10 yrs. children (146).So far religion is concerned, number of Hinduchildren were maximum as compared to Muslimand Christian. In the following figure 5, schoolchildren were more from urban area (34) thanrural (2). Within same time period, 30 Govt.Schools were visited.

Laboratory investigation reportsOut of 1165 throat swabs cultured, 52 cases

were with no growth observed in blood agar.Mixed bacterial colonies were present in MacConkey. Out of total cultured samples (1165) 91.24% cases exhibited different types of bacteriaother than Streptococcus. Whereas, 3.94%cases exhibited Alpha haemolytic and 0.34 %exhibited with Beta haemolytic (GGS). Theresults of throat swab cultures were shown intable 1.

Streptex kit analysis of 4 haemolyticcolonies showed only the presence of group G.

Table 1. Result of Throat Swab Examination in blood agar

Month Beta Alpha Bacteria NoHemolyticHemolytic other than Growth

Streptococcus

Sept,2012 0 4 148 10Oct,2012 0 6 766 34Nov,2012 0 5 213 8Dec,2012 0 11 294 0Jan,2013 0 19 228 0Feb,2013 4 (Group G) 1 104 0

Total 4 46 1063 52

Out of these 4 cases, 3 were males and one wasfemale.

In our study, carriage rate of Group GStreptococcus (GGS) was higher in males thanfemales. In case of age group, GGS infectionwas high in the age group of 11 years. Similarstudies were conducted in various part of theworld with similar findings. In the present study,though GAS was not found but the carriage ratein GGS (Group G Streptococcus) was higher inboys (75 %) than girls (25 %) which were similarto other reports (31,32). Age has been found tobe an important factor in the microbiologicaletiology of pharyngitis, the peak incidence of GASpharyngitis occurring in children aged 5–10 years(33). In the present study, the Group GStreptococcal infection was higher in 10 – 15 yrs.age group. All the 4 cases of Group G found inthis study were of 11 yrs. and of more than 11yrs. which was similar to other reports (33, 34).In Varanasi (India), the prevalence of beta-haemolytic streptococcal sore throat was 13.6%in a rural area (35). In our study, though GAScould not be isolated but the carriage rate in GGSwas predominant in urban area (80 %).

The variations in the carriage rates amongdifferent schools in the same village may beexplained on the basis of the location which wasstudied (36). Location wise present studyrevealed higher rate in govt. school (92 %) thanprivate school (8 %).

Throat cultures have always beenconsidered as the “gold standard” for diagnosingthe presence of GAS (37). The healthy carriersof GAS are the sources of a bacterialdissemination and they are able to communicatethe disease and even lead to severe epidemics(31). Different studies reported that, GAS is seenmore in the pharynges of children as comparedto that in adults (31). In the present study, thereis a complete absence of Group A Streptococciamong the school going children (5-15 yrs.) withinthe period of 6 months. Early use of antibioticsmay be one of the factors for completedisappearance of group A Streptococcus in this

Nilratan Majumdar et al

Page 7: The Prevalence of β-haemolytic Streptococcal infection ...abap.co.in/sites/default/files/Paper-7_14.pdf · gram-positive bacteria which are found to exhibit ... have become rare

887Current Trends in Biotechnology and PharmacyVol. 7 (4) 881-889 October 2013, ISSN 0973-8916 (Print), 2230-7303 (Online)

area. The prevalence of beta-haemolyticStreptococcus in healthy individuals in differentparts of India has been reported ranging between11.2-34% (33). Various studies were conductedin different parts of South India like Vellore, SouthIndia – 2.3% (1977) (15), Chennai, South India -5.2 % (2005) and 8.4 % (2006) (38,39),Coimbatore, S.India – 5.09 % (2012) (40) and4. B.G. Nagara, Karnataka – 1.9% (2013) (41).In Northern India, the incidences of sore throatand GAS sore throat were-7.05 and 0.95episodes per child/year (2001) respectively (17).

In Japan, a case of neonatal toxic shocksyndrome due to S. dysgalactiae subsp.Equisimilis was reported (28). Invasive infectionscaused by this species are also increasingly seenin Japan (42) while one case of necrotizingfascitis and another case of toxic shocksyndrome were reported from Norway (43) Dueto these reasons, it is believed that GGS strainsmay be involved in the pathogenesis of post-streptococcal sequelae. Meanwhile, our studywas based on a relatively small sample sizewithin only 6 months time period. Hence it isimperative to carry forward to further study in abroader spectrum in different seasons to look forthe presence of seasonal variability. We shouldexplore the application of newer technologies toisolate GAS from the study subject. The resultsof the present study highlighted the importanceof regular surveillance programmes to keep theStreptococcus infections and their carriage incheck. The children who were found to be carrierscould be adequately treated with antibiotics. Thiswould further facilitate the control and thedevelopment of non-suppurative sequelae suchas acute rheumatic fever and post streptococcalglomerulonephritis, which are debilitating anddifficult to treat.

AcknowledgmentsThe authors are thankful to Indian Council

of Medical Research (ICMR) for funding theresearch project for North East research priority.We also thank the Principal of Agartala Govt.Medical College Agartala for permitting us toconduct this study.

References1. Schwartz, B., Facklam, R.R. and Breiman,

R.F. (1990). Changing epidemiologyof groupA streptococcal infection in the USA. Lancet,336: 1167–1171.

2. Ruoff, K. L. (1998). Streptococcal diseases.In: Collier L, Balows A, Sussman M (eds)Topley & Wilson’s microbiology andmicrobial infections, 9th edn, vol 3: Bacterialinfections. London, Arnold., 257–275.

3. Tyrrell, G.J., Senzilet, L.D., Spika, J.S., Kertesz, D. A., Alagaratnam, M., Lovgren,M. and Talbot, J. A. (2000). Invasive diseasedue to group B streptococcal infection inadults: results from a Canadian population-based, active laboratory surveillance study-1996. J Infect Dis., 182: 168–173.

4. Efstratiou, A. (1990). GroupA Streptococciin the 1990s. J. Antimicrob. Chemother.2000, 45:3-12.

5. Carapetis, J. R., Steer, A. C., Mulholland,E. K. and Weber, M. (2005). The global1.burden of group A streptococcaldiseases. Lancet Infect Dis. ;5:685–94.

6. World Health Organization. The WorldHealth Report 2004. WHO, Geneva. (http://www.who.int/whr/previous/en/index.html)

7. Mishra, T. K. (2007). Acute Rheumatic Feverand Rheumatic Heart Disease: CurrentScenario. JIACM, 8(4): 324-30.

8. World Health Organization. (2005). Thecurrent evidence for the burden of group Astreptococcal diseases. Geneva: TheOrganization. page 60.

9. Sainani, G. S. and Sainani, A. R. (2006).Rheumatic fever - how relevant in Indiatoday? JAPI, 54: 42-47.

10. Carapetis, J.R,. Steer, A.C., Mulholand,E.K. and Weber, M. (2005). The globalburden of group A streptococcal diseases.Lancet Infect. Dis. 5:685.

Prevalence of β-haemolytic Streptocoocal infection

Page 8: The Prevalence of β-haemolytic Streptococcal infection ...abap.co.in/sites/default/files/Paper-7_14.pdf · gram-positive bacteria which are found to exhibit ... have become rare

888Current Trends in Biotechnology and PharmacyVol. 7 (4) 881-889 October 2013, ISSN 0973-8916 (Print), 2230-7303 (Online)

11. Carapetis, J. R. (2004). The currentevidence of the burden of Group Astreptococcal diseases. World HealthOrganisation, 1-57.

12. Veasy, L. G., Wiedmeier, S. E., Orsmond,G. S., Ruttenberg, H. D., Boucek, M.M., Roth, S. J., Tait, V. F., Thompson, J.A., Daly, J. A., Kaplan, E.L. and Harry R. H.(1987). Resurgence of acute rheumaticfever in the intermountain area of the UnitedStates. N. Eng. J. Med., 316: 421-427.

13. Shet, A., and Kaplan, E. (2004). Addressingthe burden of group A streptococcal diseasein India. Indian J. Ped., 71:41-48.

14. Capoor, M. R., Nair, D., Dev, M., Batra, K.and Aggarwal, P. (2006). Resistance toErythromycin and Rising Penicillin MIC inStreptococcus Pyogenes in India. Jpn. J.Infect. Dis., 59: 334-336.

15. Koshi, G. and Benjamin, V. (1977). Surveill-ance of streptococcal infection in childrenin a South Indian community: a pilot survey.Ind. J. Medical Research, 66: 379-388.

16. Koshi, G., Jadhar, M. and Myers, R. M.(1970). Streptococcal pharyngitis in childrenin SouthernIndia. Ind. J. Medical Research,58: 161–165.

17. Nandi, S. Kumar, R., Ray, P., Vohra, H. andGanguly, N. K. (2001). Group A strep-tococcal sore throat in a periurbanpopulation of northern India: a one-yearprospective study. Bulletin of the WorldHealth Organization, 79: 528–533.

18. Kumar, R., Vohra, H. Chakraborty, A.,Sharma, Y.P., Bandhopadhya, S.,Dhanda,V., Sagar, V., Sharma, M., Shah,B. and Ganguly, N. K. (2009). Epidemiologyof group A streptococcal pharyngitis &impetigo: a cross-sectional & follow up studyin a rural community of northern India. IndianJ Med Res. 130:765-771.

19. Brahmadathan, K. N. and Koshi, G. (1988).Epidemiology of streptococcal pyoderma in

an orphanage community of a tropicalcountry. J. Trop. Med. Hyg., 91:306-314.

20. Mathur, P., Kapil, A., Das, B., Dhawan, B.and Dwivedi, S.N. (2002). Invasive beta-haemolytic streptococcal infections in atertiary care hospital in northern. India. JMed Microbiol., 51:791-792.

21. Zaman, M. M., Rouf, M. A., Haque, S., Khan,L. R., Chowdhury, N. A., Razzauqe, S. A.,Yoshike, N. and Tanaka, H. (1998). Doesrheumatic fever occur usually between theages of 5 and 15 years?. Int J Cardiol., 66:17-21.

22. Nandi, S., Kumar, R., Ray, P., Vohra H.and Ganguly, N. K. (2002). Clinical scorecard for diagnosis of group A streptococcalsore throat. Ind. J. Pediatr., 69: 471-5.

23. Padmavati, S. (1987). Rheumatic feverand Rheumatic heart disease in India.Progress in Cardiology 15th ed, (Paul, N.Yu.), Philadelphia, Lea & Febiger.

24. Laura, N. B., Beneden, C.V., Beall, B.,Facklam, R., Shewmaker, P.L. and Malpiedi,P. (2009). Population-based study ofinvasive disease due to beta-hemolyticstreptococci of groups other than A and B.Clin Infect Dis., 48:706-12.

25. Rammelkamp, C. H. Jr. (1956).Epidemiology of streptococcal infections.Harvey Lect., 51:113.

26. Lancefield, R. C. (1933). A SerologicalDifferentation of Human And Other Groupsof Hemolytic Streptococci. J Exp Med.,57:571.

27. Sherman, J. M. (1937). The Streptococci.Bacteriol. Rev., 1:3.

28. Yamaoka, S., Ogihara, T., Yasui, M.,Hasegawa, M., Hira, S., Oue, S., Ubukata,K., Watanabe, H. and Takahashi, T. (2010).Neonatal streptococcal toxic shocksyndrome caused by Streptococcusdysgalactiae subsp. Equisimilis. Pediatr.Infect. Dis. J., 29:979-981.

Nilratan Majumdar et al

Page 9: The Prevalence of β-haemolytic Streptococcal infection ...abap.co.in/sites/default/files/Paper-7_14.pdf · gram-positive bacteria which are found to exhibit ... have become rare

889Current Trends in Biotechnology and PharmacyVol. 7 (4) 881-889 October 2013, ISSN 0973-8916 (Print), 2230-7303 (Online)

29. Haidan, A., Talay, S. R., Rohde, M.,Sriprakash, K. S., Currie, B.J. and Chhatwal,G.S. (2000). Pharyngeal carriage of GroupC and Group G streptococci and acuterheumatic fever in an Aboriginal population.Lancet, 356:1167-1169.

30. Castled, D., Kessock-Philip, S. and Easmon,C. S. F. (1982). Evaluation of an improvedStreptex kit for the grouping of beta-haemolytic streptococci by agglutination. JClin Pathol., 35:719-722.

31. Nabipour, F. and Tayar, Z. M. (2005).Prevalence of Beta-haemolyticstreptococcus carriage state and itssensitivity to different antibiotics amongguidance- school children in Kerman-Iran.Am J Infect Dis., 1:128-31.

32. Navneeth, B. V., Nimanda, R., Chawda, S.,Selvarani, P., Bhaskar, M. and Sugan-thi, N.(2001). Prevalence of beta -haemolyticstreptococci carrier rate among schoolchildren in Salem. Indian J Paediatr., 68:985-86.

33. Nandi, S., Kumar, R., Ray, P., Vohra, H. andGanguly, N. K. (2001). Group AStreptococcal sore throat in a periurbanpopulation of northern India: a one-yearprospective study. World Health Organ.,79 : 528-33.

34. Kaplan, E. L., Bisno, A. L., Gerber, M. A.and Gwaltney, J. M. Jr. (1971). Diagnosisof streptococcal pharyngitis: differentiationof active infection from the carrier state insymptomatic child. Journal of InfectiousDiseases, 123: 490–501. 24.

35. Sarkar, S., Biswas, R., Gaur, S. D., Sen, P.C. and Reddy, D. C. (1988). A study on sorethroat and beta-hemolytic streptococcalpharyngitis among rural school children inVaranasi with reference to age and season.Indian Journal of Public Health, 32: 191-198.

36. Dumre, S. P., Sapkota, K., Adhikari, N.,Acharya, D., Karki, M. and Bista, S. (2009).Asymptomatic throat carriage rate andantimicrobial resistance pat-tern ofstreptococcus pyogenes in Nepalese Schoolchildren. Kath-mandu University Med J., 7:392-96.

37. Shet, A. and Kaplan, E. (2004). Addressingthe burden of group A streptococcaldisease in India. Ind. J. Pediatr., 71 (1):41-48.

38. Anbu, M. and Thangam, M. (2005).Biotyping of the group A Streptococci whichwere isolated from normal school childrenin south India. Indian Journal for thePractising Doctor. 17-18.

39. Charmaine, A. C. L., Swarna, E. J. andThangam, M. ( 2006). Pharyngeal carriageof the group A streptococci in school childrenin Chennai. Indian J Med Res. 124: 195-98.

40. Muthusamy, D., Boppe, A. and Suresh., S.P. (2012 September). Prevalence of GroupA Beta Haemolytic Streptococcal CarriersAmong School Children in Coimbatore,South India. Journal of Clinical andDiagnostic Research. 6:1181-1183.

41. Vijaya, D., Sathish, J. V. and Jana Kiram, K.(2013). The Prevalence of Group AStreptococci Carriers AmongAsymptomaticSchool Children Journal of Clinical andDiagnostic Research, 7: 446-448.

42. Takahashi, T., Ubukata, K. and Watanabe,H. (2011). Invasive infection caused byStreptococcus dysgalactiae subsp.equisimilis: characteristics of strains andclinical features. J. Infect. Chemother. 17:1-10.

43. Kittang, B. R., Langeland, N., Skrede, S. andMylvaganam, H. (2010). Two Unusual casesof severe soft tissue infection caused byStreptococcus dysgalactiae subsp.equisimilis. J. Clin. Microbiol., 48:1484-1487.

Prevalence of β-haemolytic Streptocoocal infection