0
We're unable to sign you in at this time. Please try again in a few minutes.
Retry
We were able to sign you in, but your subscription(s) could not be found. Please try again in a few minutes.
Retry
There may be a problem with your account. Please contact the AMA Service Center to resolve this issue.
Contact the AMA Service Center:
Telephone: 1 (800) 262-2350 or 1 (312) 670-7827  *   Email: subscriptions@jamanetwork.com
Error Message ......
Article |

Incidence of Streptococcal Carriers in Private Pediatric Practice FREE

Michael E. Pichichero, MD; Steven M. Marsocci, MD; A. Marie Lynd Murphy, MD; William Hoeger, MD; John L. Green, MD; Ann Sorrento, PNP
[+] Author Affiliations

From the Department of Microbiology and Immunology, University of Rochester Medical Center, Elmwood Pediatric Group, Rochester, NY.


Arch Pediatr Adolesc Med. 1999;153(6):624-628. doi:10.1001/archpedi.153.6.624.
Text Size: A A A
Published online

Objective  To determine the incidence of group A β-hemolytic streptococcus (GABHS) carriers in children who are well, in children seen with presumed and documented viral illnesses with sore throat, and in children after treatment of acute GABHS tonsillopharyngitis with 10 days of oral penicillin V potassium, oral cephalosporins, or macrolides.

Methods  Prospective collection of clinical and microbiologic data from October 1996 to June 1997 in a private pediatric practice were obtained from children who were asymptomatic and well, from children with both presumed (and documented) viral sore throats, and from children who had completed a full antibiotic treatment course for acute GABHS throat infections.

Results  The incidence of GABHS carriers was 2.5% among well children (n=227), 4.4% among children with upper respiratory tract infections including sore throat of presumed viral etiology (n=296), and 6.9% among children with upper respiratory tract infections including sore throat from whom viruses were isolated (n=87). Following 10 days' treatment of acute GABHS tonsillopharyngitis, 81 (11.3%) of 718 children treated with penicillin, 22 (4.3%) of 508 children treated with an oral cephalosporin, and 10 (7.1%) of 140 children treated with a macrolide were GABHS carriers (P<.001).

Conclusions  A small percentage of children seen in private pediatric practices who are well or who have apparent viral upper respiratory tract infections with sore throat are GABHS carriers. Penicillin treatment of acute GABHS tonsillopharyngitis results in a higher GABHS carriage rate than occurs following treatment with cephalosporins and macrolides.

CARRIERS OF group A β-hemolytic streptococcus (GABHS) harbor the organism in their nose or throat but display no symptoms of acute infection. The incidence of streptococcal carriers in general pediatric practice is a controversial issue. Estimates of their number vary with the study population and with the methods used. Since diagnosis of GABHS throat infection is based in large part on the finding of the organisms with an appropriate culture in the sick patient, differentiation between the carrier and the individual with bona fide illness is of importance. In this study we sought to determine the incidence of GABHS carriers in well children, and in children seen with both presumed and documented viral illnesses with sore throat. We also examined the incidence of GABHS carriage following an appropriate treatment course for GABHS tonsillopharyngitis with 10 days of oral penicillin V potassium, oral cephalosporins, and oral macrolides.

This was a prospective study (October 1996 through June 1997) conducted at the Elmwood Pediatric Group, which is a private practice group of board-certified pediatricians, located in the suburbs of Rochester, NY. Our patients are drawn from all socioeconomic groups, although predominantly middle- and upper-middle class families. Four study groups were defined for the purposes of this study. Group 1 included well children. For 31 consecutive weeks, on the same day of the week, approximately 10 randomly selected patients visiting Elmwood Pediatric Group for routine well-child care, allergy injections, or other nonacute illnesses had a throat swab of their oropharynx obtained for isolation of GABHS. Children with any illness referable to the upper respiratory tract were specifically excluded. Group 2 were children with sore throat and apparent viral upper respiratory tract infection (URI). Again, on the same day of the week for 31 consecutive weeks, the Elmwood Pediatric Group care providers collected nose and throat viral cultures from approximately 10 children as a sentinel practice for the National Institutes of Health epidemiological surveillance program under a Vaccine and Treatment Evaluation Unit contract with the University of Rochester. Group 3 included children from group 2 whose viral culture was positive, representing a subset of group 2. Group 4 were children presenting with sore throat, positive rapid antigen detection test results or positive culture confirmed as due to GABHS infection, and who were treated for 10 days with oral penicillin V potassium, oral cephalosporins, or oral macrolides.

LABORATORY METHODS

Throat swabs for bacterial isolation were processed by routine in-office culture methods in our office laboratory (Clinical Laboratory Improvement Amendments, level 3 approved, 1992). For patients in group 4, if a rapid GABHS antigen detection test result was positive, then a throat culture was not taken and the rapid test result was considered definitive evidence of the presence of GABHS infection. Throat swabs were plated on sheep blood agar, a bacitracin disk was placed on the inoculum, and the agar was stabbed in several areas. Plates were incubated aerobically at 35°C and examined for 2 successive days for the presence of β-hemolytic streptococci. Isolates with typical streptococcal colony morphologic features that were sensitive to bacitracin were classified as group A. Appropriate positive and negative quality-control cultures were plated daily. The GABHS colony counts were categorized as 4+ if more than 100 colony-forming units were present, and 3+ if 51 to 100, 2+ if 11 to 50, and 1+ if 1 to 10 colony-forming units were present.

VIRAL CULTURE METHODS

Nose and throat swabs were placed in viral transport media and stored at 4°C overnight. The next-day cultures were taken to the University of Rochester and processed according to standard techniques in the laboratory of Caroline Breese Hall, MD.

SYMPTOMS AND SIGNS OF PRESUMED VIRAL URI

Symptoms and signs of acute infection compatible with the diagnosis of presumed viral URI included sore throat, fever, headache, coryza, cough, malaise, myalgia, tonsillopharyngeal redness, swollen and/or tender anterior cervical lymph nodes, and chest rhonchi.

SYMPTOMS AND SIGNS OF ACUTE GABHS INFECTION

Symptoms and signs of acute infection compatible with the diagnosis of GABHS tonsillopharyngitis included sore throat, fever, headache, malodorous breath, facial flush, nausea, vomiting, tonsillopharyngeal redness and/or exudate, palatal petechiae, and swollen and/or tender anterior cervical lymph nodes. Treated patients were seen at follow-up visits 14 to 21 days after initiation of antibiotic therapy. During the follow-up visit, symptoms of GABHS throat infection were again solicited, a limited examination pertaining to the possibility of recurrent throat infection was undertaken, and a throat swab was obtained for routine culture of GABHS.

ANTIBIOTIC TREATMENT

Oral penicillin V potassium was administered for 10 days at a daily dose of 20 to 40 mg/kg, 2 or 3 times daily. Various oral cephalosporins were used, including first-, second-, and third-generation drugs, and dosing was according to manufacturers' recommendations and continued for 10 days. Macrolide therapy consisted of a 10-day course of erythromycin estolate or erythromycin ethylsuccinate, or a 5-day course of azithromycin administered according to manufacturers' recommendations. Compliance was not actively monitored.

STATISTICS

We used χ2 analysis to assess differences in GABHS carriage rates among the study groups.

The incidence of GABHS carriers among 227 well children seen in our practice was 2.5%. Among the 296 children seen with sore throat of presumed viral etiology the incidence was 4.4%, and among the 87 children seen with sore throat and documented viral illness it was 6.9% (P =.16; Table 1). Two thirds of positive GABHS throat cultures in carriers were 3+ or 4+ and one third were 2+ or less for colony counts. No child older than 10 years was a GABHS carrier and the mean age of GABHS carriers was 6.7±1.4 years. The 6 children with concurrent documented viral illness and GABHS isolation had viral cultures positive for adenovirus (n=1), enteroviruses (n=2), influenza B virus (n=1), herpes simplex virus (n=1), and respiratory syncytial virus (n=1).

Table Graphic Jump LocationTable 1. Characteristics of Selected Pediatric Patients

Four to 11 days after treatment with oral penicillin V, 81 (11.3%) of 718 children harbored GABHS, but were asymptomatic as were 22 (4.3%) of 508 children treated with an oral cephalosporin and 10 (7.1%) of 140 children treated with an oral macrolide (Table 2). There was a definite difference in posttreatment carrier incidence among the 3 treatment groups (P<.001), between penicillin- and cephalosporin-treated children (P <.001), and a trend between penicillin- and macrolide-treated children (P=.19). Ninety-two (81.4%) of the 113 GABHS carriers following antibiotic treatment were 4+ or 3+ in colony counts, with the remainder of cultures being 2+ or less.

Table Graphic Jump LocationTable 2. Characteristics of Patients After Treatment for GABHS* Throat Infections

Contrary to the results of our study, others117 have found that the carrier rate for GABHS in apparently healthy children is sufficiently common to cast doubt on the value of cultures or rapid antigen detection tests as a diagnostic tool. In 1972, Wannamaker18 wrote

Various studies of normal populations of children, e.g., school surveys, have indicated carrier rates during the school year varying from 10% to 40%. An overall average might be at least 15% to 20%. One must assume that at least 15% to 20% of all children with pharyngitis will have a positive culture for GABHS on this basis alone. Superimposing this figure on that for acute pharyngitis one must conclude that about half of all patients from whom GABHS can be isolated are exhibiting this organism as chronic carriers rather than as acute infections.

However, review of those studies, published in the 1940s to 1960s, which Wannamaker relied on, clarifies why this statement is not applicable to the patient encountered in private practice.

In longitudinal surveys of streptococcal illness among children in residential homes, orphanages, closed schools, or American Indian reservations, the study setting and the frequency and number of cultures taken from individuals is critical to the interpretation of results. Carriage of GABHS occurs more commonly in such closed or semiclosed populations.8,1214 The findings do not reflect the incidence of carriage in a community-based private pediatric practice. In practice we are primarily interested in knowing the incidence of carriers when a single culture is taken from a single patient at a single time since this permits a basis for comparison with a diagnostic culture taken from an ill patient with tonsillopharyngitis. Studies that involve taking repeated cultures from an individual to estimate the pattern and total exposure to GABHS are looking to answer a different question.

The bacteriologic method used for isolation of GABHS also is relevant. Many earlier longitudinal surveys relied on highly sensitive methods that are not commonly used in practice. These included selective media, pour plates, and anaerobic or carbon dioxide incubation of plates. Such procedures increase the proportion of positive cultures that are often missed with simpler, standard office methods. The question arises whether less sensitive bacteriologic methods result in missed significant clinical disease. We suggest that an appropriate standard would be the methods of Denny et al19 and Wannamaker et al,20 which established the value of penicillin therapy in eradication of GABHS from the tonsillopharynx as a primary prevention technique for acute rheumatic fever. In those studies, the culture methods were more similar to those routinely used in our office practice.

The GABHS carriers in our study population had higher colony counts than often reported; however, the relation between colony count and carrier status has been previously challenged.21 Although the children in group 2 (children with sore throat and apparent viral URI) appeared to have viral URIs, and typical symptoms and signs of GABHS infection were absent, we cannot exclude the possibility that some of these children had concurrent bona fide GABHS infection as well as viral infections.

There continues to be recognized disagreement with regard to the significance of the carrier state.22 Some investigators have regarded the presence of GABHS in the nasopharynx as a source of danger and suggest eradication is a desirable goal,3,8 while others have argued that given the vast number of school children who are regular carriers, it seems inappropriate to proceed on a course of attempting to eradicate GABHS since there is a marginal relationship to clinically significant illness and sequelae on a community-wide basis.2,5,12,15 The widely held notion that GABHS carriers are harmless to themselves and to others is not accurate. Kuttner and Krumwiede23 described a number of GABHS outbreaks caused by carriers at the Irvington House on the Hudson River, NY, prior to the advent of antibiotics. They showed in their institutional study setting that the carrier could be an important vector in these infections and that the frequency of spread and resulting disease was often characteristic of a specific strain of GABHS. Thus, between epidemics, although 10% of children were found to be carriers, often none showed a great tendency to contagiousness. However, during certain other periods of observation, major and minor outbreaks occurred usually by strains of GABHS that were new to the institution; several of these outbreaks were introduced by carriers. In a family setting, James et al24 showed that children with clinical illness infect other members of the family approximately 25% of the time, whereas children who are carriers infect other members of the family about 9% of the time. Asymptomatic spread of GABHS from a streptococcal carrier within a family has been described to occur.25 The same GABHS strains that are responsible for invasive, toxic shock and necrotizing fasciitis infections may be prevalent among carriers and patients with symptomatic pharyngitis in a community2632; transmission of these strains from the carrier reservoir to the latter groups of patients likely occurs.33

Since we did not M and T type our strains in this study, we are unable to comment on strain variation presented in our carrier population. In the acute GABHS–infected patients who received antibiotic treatment, acquisition of a new strain vs persistence of the original infecting strain may occur. When serotyping of strains is done, our group34 and others20,35 have previously shown that after antibiotic treatment, about two thirds of the isolates will be the same serotype and one third will be new acquisitions.

We elected not to measure antistreptolysin O and anti-DNase B titers in our study population. In different study populations, Kaplan et al36 found that streptococcal antibody rises were observed in only 5% of asymptomatic individuals with positive cultures for GABHS, and Moffett et al14 found that about 5% of individuals who are asymptomatic and who have no GABHS isolated on throat swabs show significant antistreptolysin O and/or anti-DNase B rises. Extrapolation from those studies to ours should be done cautiously since the study settings were different, but their results are suggestive that we might have found measurable antibody rises in about 5% of our asymptomatic population of carriers and in our culture-negative cohort. Antistreptolysin O and anti-DNase B antibody rises occur in approximately 60% of individuals following apparent acute GABHS infection,16 but that does not mean the rest are carriers.22 Antibiotic treatment of GABHS throat infections suppresses the antibody response significantly,37 making the validity of the 60% estimate questionable. Some of the patients in the antibiotic-treated population of our study could have been carriers. However, based on the carrier rates in asymptomatic patients and patients with viral sore throats, it is unlikely that the number exceeded 5%.

It has been suggested that the superiority of treatment with cephalosporins (and perhaps macrolides) in comparison with penicillin in bacteriologic outcome following acute GABHS tonsillopharyngitis is due to enrollment of carriers in comparative studies and due to more effective eradication of the carrier state with the broader spectrum agents.38 Our results challenge this notion. The carrier rate in our practice is 2.5% to 6.9% and studies in similar populations have found carrier rates of 8.3%39 to 10.9%.40 In contrast, there is generally a 20% to 25% higher eradication rate after cephalosporin41 and azithromycin42 treatment as compared with penicillin. Thus, our results show that the GABHS carrier state follows penicillin treatment more often than following cephalosporin or macrolide treatment, but other, much larger factor(s)41 must contribute to differences in eradication rates among these therapies.

Accepted for publication November 4, 1998.

Anne B. Francis, MD, Carmen Noriega, MD, Kathy White Ryan, PNP, of the Elmwood Pediatric Group participated in this work.

Corresponding author: Michael E. Pichichero, MD, University of Rochester Medical Center, Elmwood Pediatric Group, Department of Microbiology/Immunology, 601 Elmwood Ave, Box 672, Rochester, NY 14642 (e-mail: mepo@uhura.cc.rochester.edu).

Editor's Note: Well, here you have it folks. Data from the "real world" (Rochester qualifies) that differs from classical information. Which world do you practice in?—Catherine D. DeAngelis, MD

Zanen  HCGanor  SVanToorn  M A continuous study of hemolytic streptococci in throats of normal children, adults, and aged men. Am J Hyg. 1959;69265- 273
Pike  RMFashena  GJ Frequency of hemolytic streptococci in the throats of well children in Dallas. Am J Public Health. 1946;36611- 622
Link to Article
Saslaw  MSStreitfeld  MM Group A β hemolytic streptococci and rheumatic fever in Miami, Florida, I: bacteriologic observations, from October 1954 through May 1955. Dis Chest. 1959;35175- 193
Link to Article
Cornfeld  DWerner  GWeaver  R  et al.  Streptococcal infection in a school population. Ann Intern Med. 1958;491305- 1319
Link to Article
Kincaid  CKNelson  ECBurnham  TW Incidence of β hemolytic streptococcus. Wisc Med J. 1961;60643- 648
Nicholas  WCSteele  CP Occurrence of groupable β-hemolytic streptococci. JAMA. 1962;181197- 205
Link to Article
Quinn  RWFederspiel  CF The occurrence of hemolytic streptococci in school children in Nashville, Tennessee, 1961-1967. Am J Epidemiol. 1973;9722- 33
Holmes  MCWilliams  REO Streptococcal infections among children in a residential home, IV: outbreaks of infection. J Hyg. 1958;56211- 237
Link to Article
Krause  RMRammelkamp  CH  JrDenny  FW  Jr  et al.  Studies of the carrier state following infection with group A streptococci, I: effect of climate. J Clin Invest. 1962;41568- 574
Link to Article
Krause  RMRammelkamp  CH  Jr Studies of the carrier state following infection with group A streptococci, II: infectivity of streptococci isolated during acute pharyngitis and during the carrier state. J Clin Invest. 1962;41575- 578
Link to Article
Coburn  AF The carrier problem in the dissemination of hemolytic streptococcus. US Naval Bull. 1944;42325- 335
Mozziconacci  PGerbeaux  CCaravano  R  et al.  A study of group A hemolytic carriers among school children. Acta Paediatr Scand. 1960;49711
Link to Article
Holmes  MCWilliams  REO Streptococcal infections among children in a residential home. J Hyg. 1958;5643
Link to Article
Moffett  HLCramblett  HGSmith  A Group A streptococcal infections in a children's home. Pediatrics. 1964;3311
Cornfeld  DHubbard  JP A four-year study of the occurrence of β-hemolytic streptococci in 64 school children. N Engl J Med. 1961;264211- 215
Link to Article
Kaplan  ELTop  FH  JrDudding  BAWannamaker  LW Diagnosis of streptococcal pharyngitis: differentiation of active infection from the carrier state in the symptomatic child. J Infect Dis. 1971;123490- 501
Link to Article
Quinn  RW Hemolytic streptococci in Nashville school children. South Med J. 1980;73288- 296
Link to Article
Wannamaker  LW Perplexity and precision in the diagnosis of streptococcal pharyngitis. AJDC. 1972;124352- 358
Denny  FWWannamaker  LWBrink  WR  et al.  Prevention of rheumatic fever: treatment of the preceding streptococcic infection. JAMA. 1950;142151- 153
Link to Article
Wannamaker  LWRammelkemp  CR  JrDenny  FW  et al.  Prophylaxis of acute rheumatic fever by treatment of the preceding streptococcal infection with various amounts of depot penicillin. Am J Med. 1951;10673- 695
Link to Article
Gerber  MARandolph  MFMayo  DR The group A streptococcal carrier state: a reexamination. AJDC. 1988;142562- 565
Dunlap  MBHarvey  HS The carrier state and type-specific immunity in streptococcal disease. AJDC. 1967;114229- 243
Kuttner  AGKrumwiede  E Observations on the effect of streptococcal upper respiratory infections on rheumatic children: a three-year study. J Clin Invest. 1941;20273- 287
Link to Article
James  WEBadger  GFDingle  JH A study of illnesses in a group of Cleveland families, XIX: the epidemiology of the acquisition of group A streptococci and of associated illness. N Engl J Med. 1960;262687- 694
Link to Article
Nguyen  LLevy  DFerroni  AGehanno  PBerche  P Molecular epidemiology of Streptococcus pyogenes in an area where acute pharyngotonsillitis is endemic. J Clin Microbiol. 1997;352111- 2114
Kiska  DLThiede  BBaracciolo  J  et al.  Invasive group A streptococcal infections in North Carolina: epidemiology, clinical features, and genetic and serotype analysis of causative organisms. J Infect Dis. 1997;176992- 1000
Link to Article
DiPersio  JRFile  TMStevens  DLGardner  WGPetropoulos  GKawaljit  D Spread of serious disease-producing M3 clones of group A streptococcus among family members and healthcare workers. Clin Infect Dis. 1996;22490- 495
Link to Article
Ichiyama  SNakashima  KShimokata  K  et al.  Transmission of Streptococcus pyogenes causing toxic shock-like syndrome among family members and confirmation by DNA macrorestriction analysis. J Infect Dis. 1997;175723- 726
Link to Article
Cockerill  FRMacDonald  KLThompson  RL  et al.  An outbreak of invasive group A streptococcal disease associated with high carriage rates of the invasive clone among school-aged children. JAMA. 1997;27738- 43
Link to Article
Musser  JMHauser  ARKim  MHSchlievert  PMNelson  KSelander  RK Streptococcus pyogenes causing toxic-shock-like syndrome and other invasive diseases: clonal diversity and pyrogenic exotoxin expression. Proc Natl Acad Sci U S A. 1991;882668- 2672
Link to Article
Musser  JMKapur  VPeters  JE  et al.  Real-time molecular epidemiologic analysis of an outbreak of Streptococcus pyogenes invasive disease in US Air Force trainees. Arch Pathol Lab Med. 1994;118128- 133
Muotiala  ASeppälä  HHuovinen  PVuopic-Varkila  J Molecular comparison of group A streptococci of TIMI serotype from invasive and noninvasive infections in Finland. J Infect Dis. 1997;175392- 395
Link to Article
Cockerill  FR  IIISchlievert  PMMusser  JM Epidemiology of invasive streptococcal infections. J Infect Dis. 1998;1771773- 1774
Link to Article
Breese  BBDisney  FATalpey  WB The prevention of type specific immunity to streptococcal infections due to the therapeutic use of penicillin. AJDC. 1960;100353- 359
Stillerman  MBernstein  SH Streptococcal pharyngitis therapy. AJDC. 1964;10773- 84
Kaplan  ELGastanaduy  ASHuwe  BB The role of the carrier in treatment failures after antibiotic therapy for group A streptococci in the upper respiratory tract. J Lab Clin Med. 1981;98326- 335
Valkenburg  HAVarerkorn  MJGoslings  WROLorrier  JCde Moor  CEMaxted  WR Streptococcal pharyngitis in the general population, II: the attack rate of rheumatic fever and acute glomerulonephritis in patients not treated with penicillin. J Infect Dis. 1971;124348- 358
Link to Article
Shulman  STGerber  MATanz  RRMarkowitz  M Streptococcal pharyngitis: the case for penicillin therapy. Pediatr Infect Dis J. 1994;131- 7
Link to Article
Ginsburg  CMMcCracken  GHCrow  SD  et al.  Seroepidemiology of the group A streptococcal carriage state in a private pediatric practice. AJDC 1985;139614- 617
Hoffman  S The throat carrier rate of group A and other β hemolytic streptococci among patients in general practice. Acta Pathol Microbiol Immunol Scand. 1985;93347- 351(section B)
Pichichero  MEMargolis  PA A comparison of cephalosporins and penicillins in the treatment of group A β hemolytic streptococcal pharyngitis: a meta-analysis supporting the concept of microbial copathogenicity. Pediatr Infect Dis J. 1991;10275- 281
Link to Article
Still  JG Management of pediatric patients with group A β-hemolytic Streptococcus pharyngitis: treatment options. Pediatr Infect Dis J. 1995;14S57- 61
Link to Article

Figures

Tables

Table Graphic Jump LocationTable 1. Characteristics of Selected Pediatric Patients
Table Graphic Jump LocationTable 2. Characteristics of Patients After Treatment for GABHS* Throat Infections

References

Zanen  HCGanor  SVanToorn  M A continuous study of hemolytic streptococci in throats of normal children, adults, and aged men. Am J Hyg. 1959;69265- 273
Pike  RMFashena  GJ Frequency of hemolytic streptococci in the throats of well children in Dallas. Am J Public Health. 1946;36611- 622
Link to Article
Saslaw  MSStreitfeld  MM Group A β hemolytic streptococci and rheumatic fever in Miami, Florida, I: bacteriologic observations, from October 1954 through May 1955. Dis Chest. 1959;35175- 193
Link to Article
Cornfeld  DWerner  GWeaver  R  et al.  Streptococcal infection in a school population. Ann Intern Med. 1958;491305- 1319
Link to Article
Kincaid  CKNelson  ECBurnham  TW Incidence of β hemolytic streptococcus. Wisc Med J. 1961;60643- 648
Nicholas  WCSteele  CP Occurrence of groupable β-hemolytic streptococci. JAMA. 1962;181197- 205
Link to Article
Quinn  RWFederspiel  CF The occurrence of hemolytic streptococci in school children in Nashville, Tennessee, 1961-1967. Am J Epidemiol. 1973;9722- 33
Holmes  MCWilliams  REO Streptococcal infections among children in a residential home, IV: outbreaks of infection. J Hyg. 1958;56211- 237
Link to Article
Krause  RMRammelkamp  CH  JrDenny  FW  Jr  et al.  Studies of the carrier state following infection with group A streptococci, I: effect of climate. J Clin Invest. 1962;41568- 574
Link to Article
Krause  RMRammelkamp  CH  Jr Studies of the carrier state following infection with group A streptococci, II: infectivity of streptococci isolated during acute pharyngitis and during the carrier state. J Clin Invest. 1962;41575- 578
Link to Article
Coburn  AF The carrier problem in the dissemination of hemolytic streptococcus. US Naval Bull. 1944;42325- 335
Mozziconacci  PGerbeaux  CCaravano  R  et al.  A study of group A hemolytic carriers among school children. Acta Paediatr Scand. 1960;49711
Link to Article
Holmes  MCWilliams  REO Streptococcal infections among children in a residential home. J Hyg. 1958;5643
Link to Article
Moffett  HLCramblett  HGSmith  A Group A streptococcal infections in a children's home. Pediatrics. 1964;3311
Cornfeld  DHubbard  JP A four-year study of the occurrence of β-hemolytic streptococci in 64 school children. N Engl J Med. 1961;264211- 215
Link to Article
Kaplan  ELTop  FH  JrDudding  BAWannamaker  LW Diagnosis of streptococcal pharyngitis: differentiation of active infection from the carrier state in the symptomatic child. J Infect Dis. 1971;123490- 501
Link to Article
Quinn  RW Hemolytic streptococci in Nashville school children. South Med J. 1980;73288- 296
Link to Article
Wannamaker  LW Perplexity and precision in the diagnosis of streptococcal pharyngitis. AJDC. 1972;124352- 358
Denny  FWWannamaker  LWBrink  WR  et al.  Prevention of rheumatic fever: treatment of the preceding streptococcic infection. JAMA. 1950;142151- 153
Link to Article
Wannamaker  LWRammelkemp  CR  JrDenny  FW  et al.  Prophylaxis of acute rheumatic fever by treatment of the preceding streptococcal infection with various amounts of depot penicillin. Am J Med. 1951;10673- 695
Link to Article
Gerber  MARandolph  MFMayo  DR The group A streptococcal carrier state: a reexamination. AJDC. 1988;142562- 565
Dunlap  MBHarvey  HS The carrier state and type-specific immunity in streptococcal disease. AJDC. 1967;114229- 243
Kuttner  AGKrumwiede  E Observations on the effect of streptococcal upper respiratory infections on rheumatic children: a three-year study. J Clin Invest. 1941;20273- 287
Link to Article
James  WEBadger  GFDingle  JH A study of illnesses in a group of Cleveland families, XIX: the epidemiology of the acquisition of group A streptococci and of associated illness. N Engl J Med. 1960;262687- 694
Link to Article
Nguyen  LLevy  DFerroni  AGehanno  PBerche  P Molecular epidemiology of Streptococcus pyogenes in an area where acute pharyngotonsillitis is endemic. J Clin Microbiol. 1997;352111- 2114
Kiska  DLThiede  BBaracciolo  J  et al.  Invasive group A streptococcal infections in North Carolina: epidemiology, clinical features, and genetic and serotype analysis of causative organisms. J Infect Dis. 1997;176992- 1000
Link to Article
DiPersio  JRFile  TMStevens  DLGardner  WGPetropoulos  GKawaljit  D Spread of serious disease-producing M3 clones of group A streptococcus among family members and healthcare workers. Clin Infect Dis. 1996;22490- 495
Link to Article
Ichiyama  SNakashima  KShimokata  K  et al.  Transmission of Streptococcus pyogenes causing toxic shock-like syndrome among family members and confirmation by DNA macrorestriction analysis. J Infect Dis. 1997;175723- 726
Link to Article
Cockerill  FRMacDonald  KLThompson  RL  et al.  An outbreak of invasive group A streptococcal disease associated with high carriage rates of the invasive clone among school-aged children. JAMA. 1997;27738- 43
Link to Article
Musser  JMHauser  ARKim  MHSchlievert  PMNelson  KSelander  RK Streptococcus pyogenes causing toxic-shock-like syndrome and other invasive diseases: clonal diversity and pyrogenic exotoxin expression. Proc Natl Acad Sci U S A. 1991;882668- 2672
Link to Article
Musser  JMKapur  VPeters  JE  et al.  Real-time molecular epidemiologic analysis of an outbreak of Streptococcus pyogenes invasive disease in US Air Force trainees. Arch Pathol Lab Med. 1994;118128- 133
Muotiala  ASeppälä  HHuovinen  PVuopic-Varkila  J Molecular comparison of group A streptococci of TIMI serotype from invasive and noninvasive infections in Finland. J Infect Dis. 1997;175392- 395
Link to Article
Cockerill  FR  IIISchlievert  PMMusser  JM Epidemiology of invasive streptococcal infections. J Infect Dis. 1998;1771773- 1774
Link to Article
Breese  BBDisney  FATalpey  WB The prevention of type specific immunity to streptococcal infections due to the therapeutic use of penicillin. AJDC. 1960;100353- 359
Stillerman  MBernstein  SH Streptococcal pharyngitis therapy. AJDC. 1964;10773- 84
Kaplan  ELGastanaduy  ASHuwe  BB The role of the carrier in treatment failures after antibiotic therapy for group A streptococci in the upper respiratory tract. J Lab Clin Med. 1981;98326- 335
Valkenburg  HAVarerkorn  MJGoslings  WROLorrier  JCde Moor  CEMaxted  WR Streptococcal pharyngitis in the general population, II: the attack rate of rheumatic fever and acute glomerulonephritis in patients not treated with penicillin. J Infect Dis. 1971;124348- 358
Link to Article
Shulman  STGerber  MATanz  RRMarkowitz  M Streptococcal pharyngitis: the case for penicillin therapy. Pediatr Infect Dis J. 1994;131- 7
Link to Article
Ginsburg  CMMcCracken  GHCrow  SD  et al.  Seroepidemiology of the group A streptococcal carriage state in a private pediatric practice. AJDC 1985;139614- 617
Hoffman  S The throat carrier rate of group A and other β hemolytic streptococci among patients in general practice. Acta Pathol Microbiol Immunol Scand. 1985;93347- 351(section B)
Pichichero  MEMargolis  PA A comparison of cephalosporins and penicillins in the treatment of group A β hemolytic streptococcal pharyngitis: a meta-analysis supporting the concept of microbial copathogenicity. Pediatr Infect Dis J. 1991;10275- 281
Link to Article
Still  JG Management of pediatric patients with group A β-hemolytic Streptococcus pharyngitis: treatment options. Pediatr Infect Dis J. 1995;14S57- 61
Link to Article

Correspondence

CME
Also Meets CME requirements for:
Browse CME for all U.S. States
Accreditation Information
The American Medical Association is accredited by the Accreditation Council for Continuing Medical Education to provide continuing medical education for physicians. The AMA designates this journal-based CME activity for a maximum of 1 AMA PRA Category 1 CreditTM per course. Physicians should claim only the credit commensurate with the extent of their participation in the activity. Physicians who complete the CME course and score at least 80% correct on the quiz are eligible for AMA PRA Category 1 CreditTM.
Note: You must get at least of the answers correct to pass this quiz.
Please click the checkbox indicating that you have read the full article in order to submit your answers.
Your answers have been saved for later.
You have not filled in all the answers to complete this quiz
The following questions were not answered:
Sorry, you have unsuccessfully completed this CME quiz with a score of
The following questions were not answered correctly:
Commitment to Change (optional):
Indicate what change(s) you will implement in your practice, if any, based on this CME course.
Your quiz results:
The filled radio buttons indicate your responses. The preferred responses are highlighted
For CME Course: A Proposed Model for Initial Assessment and Management of Acute Heart Failure Syndromes
Indicate what changes(s) you will implement in your practice, if any, based on this CME course.
Submit a Comment

Multimedia

Some tools below are only available to our subscribers or users with an online account.

Web of Science® Times Cited: 37

Related Content

Customize your page view by dragging & repositioning the boxes below.

Articles Related By Topic
Related Collections
PubMed Articles
JAMAevidence.com

Users' Guides to the Medical Literature
Clinical Resolution

Users' Guides to the Medical Literature
Clinical Scenario