1959. These data comprise an extension. of those already reported and, in addition, In the school years 1955 through

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1 Since 1955, an epidemiologic investigation of streptococcal infection has been conducted in three Philadelphia schools. On the basis of their findings, the investigators question the utility of school detection programs based on current means of discovering streptococcal infection. EPIDEMIOLOGIC STUDIES OF STREPTOCOCCAL INFECTION IN SCHOOL CHILDREN David Cornield, M.D.; John P. Hubbard, M.D., F.A.P.H.A.; T. N. Harris, M.D.; and Ruth Weaver, M.D. epidemiologic study of streptococcal infections has been conducted in three elementary schools in Philadelphia since November, The children have been studied to determine the carrier rate, the rate of clinically manifest infection, and, in the first three years of the program, the effect of various schedules of treatment with penicillin on both the carrier rate and the rate of infection. Previously reported data from the years 1955 to 19571,2 indicated that: (1) in each of the school years approximately one-half of the children had one or more positive cultures for beta-hemolytic streptococci regardless of attempts at carrier control by penicillin treatment; (2) the rate of clinically manifest streptococcal infection remained relatively low in all schools independently of the existing carrier rate or treatment programs instituted; (3) relatively few of the children with respiratory symptoms had positive cultures for beta-hemolytic streptococci and, even in the group with positive cultures, most of the children presented symptoms of undifferentiated upper respiratory illness. This paper presents additional information acquired in years 1957 through These data comprise an extension of those already reported and, in addition, results from serologic studies made during Methods In the school years 1955 through 1958, children of three schools were followed, and throat cultures were taken routinely each month. Cultures were also obtained, either in the school or at home, from children developing any of the following symptoms or signs: hyperemic pharynx with or without exudate, cervical adenopathy, or earache. The presence of fever was also noted. For children whose only complaint was that of sore throat, the throat was examined for evidence of pharyngeal inflammation before the throat culture was taken. A follow-up throat culture was taken after a threeweek interval on all children who had cultures positive for beta-hemolytic streptococci in association with respiratory illness. A trained technician who was employed through the four years of the study was responsible for obtaining specimens. The over-all effectiveness of penicillin 242 VOL. 51, NO. 2. A.J.P.H.

2 STREPTOCOCCAL INFECTIONS IN SCHOOL CHILDREN therapy for children with throat cultures positive for streptococci was studied by use of the following treatment schedule: (1) In School G, penicillin was given to all children with positive cultures, whether carriers or with symptoms of respiratory illness, and also to contacts having positive cultures; (2) in School B, penicillin was dispensed only to those children with respiratory symptoms in whom a positive throat culture was obtained; (3) in School W, no penicillin was recommended or provided. However, positive cultures were reported to the parents and note made of any treatment given to the child by the family physician. In the years 1955 through 1958, in two of the schools, throat cultures were also obtained on family contacts of children who were found to have positive cultures either on routine culture or at the time of a respiratory illness. In , the study was limited to children attending School B. They were surveyed as in the foregoing with the exception that positive throat cultures from ill children were reported to the family but no penicillin was provided for treatment (the same procedure as with School W iri the previous years). Blood serums were also obtained at regular intervals from all children and coded as follows: (1) specimens obtained at the beginning of the school year from all participants-r1; (2) serums obtained on all streptococcal carriers within four days after the carrier state was discovered-r2; (3) serums obtained at the end of the school vear on all children who had had consistently negative throat cultures throughout the term (both on routine survey and in association with respiratory illness) -R3; (4) acute phase serums were taken immediately following any respiratory illness; if a positive throat culture were obtained from such a child -B1; if the culture were negative- N1; (5) convalescent serums obtained three weeks after acute serums, in children who had had an acute respiratory illness B2 or N2- Laboratory Methods Laboratory methods were described in detail in previous publications.2-4 A poured plate method was used for isolation of streptococci. The cultures were graded from one to five plus on the basis of frequency of streptococcal isolations as follows: One Plus-One colony of beta-hemolytic streptococci for each 100 or more colonies of other microorganisms Two Plus-One colony of beta-hemolytic streptococci per 50 to 100 colonies of other microorganisms Three Plus-One colony of beta-hemolytic streptococei per 20 to 50 of other microorganisms Four Plus-One colony of beta-hemolytic streptococci per five to 20 colonies of other microorganisms Five Plus-A pure or almost pure culture of beta-hemolytic streptococci was obtained. Antistreptolysin (ASO) titrations were done using a modification of the original Todd technic.3 Antihyaluronidase (AH) titrations were done using the mucin clot prevention method.4 The data are recorded in Table 5 and Figure 1 as geometric mean titers. Results In the last two years of the studv ( ), positive cultures were again obtained in approximately onehalf of the study population (Table 1). As noted previously, the routine cultures from healthy children accounted for the large majority of these positive reports. The average monthly carrier rate for each of the schools was as follows: School School School Year G B W FEBRUARY,

3 Table 1-Per cent of Children with One or More Positive Cultures Approximately 50 Per cent of Children Had One or More Positive Cultures Each Year School G School B School W Year Number Per cent Number Per cent Number Per cent Over 40 per cent of the children in School G were treated with penicillin during the course of the school year. In each of the study years, the carrier rates in this school (School G) were found to be considerably lower than in the other two schools where no penicillin was given to the carriers. The incidence of respiratory infection associated with throat cultures positive for beta-hemolytic streptococci is noted in Table 2. There was no significant difference in the "infection" rate in the three schools regardless of the penicillin treatment program used. Further, the over-all "infection" rate was at a low level through each year of the study with no increase in streptococcal infections occurring at the time when high streptococcal carrier rates were noted. Table 3 contains follow-up data on both carriers and children with respiratory illness and positive cultures. Persistently positive carrier cultures were found most frequently where antibiotic therapy was not recommended and the number of positive follow-up cultures also varied directly with the extent of antibiotic control attempted. The frequency of occurrence of signs and symptoms suggestive of streptococcal illness is listed in Table 4. A comparison between those children with such symptoms who had positive cultures and those who had negative cultures at the time of the original clinical diagnosis shows no significant difference in the frequency of individual signs and symptoms in the two groups. Thus the clinical differentiation between streptococcal and nonstreptococcal illness was unreliable. Further, it seemed likely that many of the children considered to be in the streptococcal infection category actually represented carriers who had contracted intercurrent nonstreptococcal respiratory illness. An attempt was made to distinguish between the two groups by the use of several laboratory technics: 1. Grouping and typing of streptococei obtained from carriers and symptomatic children in 1958 revealed that 72 per cent of the former and 76 per cent of the latter were of group A, with a greater frequency of typable strains in the symptomatic group (23 per cent compared with 39 per cent). However, because of the great percentage of untypable strains encountered, this criterion was not helpful in diagnosing the individual case. 2. Bacterial counts were done on positive cultures obtained from children with respiratory illness and from carriers. Fortytwo per cent of the children with respiratory illness and positive cultures for beta-hemolytic streptococci had "four plus" or "five plus" cultures. However, in comparing the bacterial counts with symptomatology, even for those children with red throats and tonsillar exudate, 45 per cent had only "one plus" or "two plus" bacterial counts. Further, 18 per cent of the carrier group with no manifest symptoms had "four plus" or "five plus" cultures. These figures indicate that cultures from symptomatic children contained larger numbers of streptococci more frequently than did cultures from carriers, but even VOL. 51. NO. 2, A.J.P.H.

4 STREPTOCOCCAL INFECTIONS IN SCHOOL CHILDREN Table 2-"Infection" Rate: Number Group A Beta-Hemolytic Streptococcal "Infections" per 100 Children per School Year The "Infection" Rate is Similar in the Three Schools Regardless of Penicillin Treatment Program School School School Year G* B* W Schools included in penicillin treatment program. in the latter group there was a large number of children who yielded a heavy growth of streptococci. Bacterial counts per se, in the individual case, therefore, did not conclusively help to distinguish the child with definite streptococcal disease from the carrier. 3. In immunologic studies done on ill children, there was no significant difference in geometric mean ASO titers or AH titers of the acute or convalescent blood serums obtained from children with either positive or negative throat cultures (Table 5). Six of the 58 children with negative cultures had significant increases in the ASO or AH titers (a fourfold increase in titer) and two had significant decreases. In the group of children with positive cultures only six of 35 had significant increases in the ASO or AH titer and none had significant decreases. Thus, the serologic studies did not serve to distinguish between the two groups of children. Six of the children with negative cultures had significant antibody rises, probably representing infections missed by the use of routine bacteriologic methods for streptococcal isolation. In 29 of 35 cases with positive cultures in a group of children with manifest clinical infection, there was no significant immunologic response, suggesting that these cases represented nonstreptococcal respiratory illnesses with coincident streptococci in the throat. In reviewing the entire group of ill children, it was found that an ASO titer of 256 or greater (a range suggestive of recent streptococcal infection) was found among children with negative streptococcal cultures, in 33 per cent of the serums obtained in the acute stage of the infection and in 31 per cent of serums at the convalescent stage. Similar data were obtained from the children with positive cultures, among whom 32 per cent had an acute phase serum with a titer 256 or greater and 38 per cent had a convalescent serum with a titer in this range. In addition to specimens obtained in association with respiratory illness, serums were drawn at regular intervals through the school year. The results are shown in Table 5. Comparison of the children who became carriers (R1- R2) with those who remained free of streptococci throughout the school year (1R1-R3), revealed no significant difference in the mean ASO and AH titers in the two groups. However, of a total of 115 children in the carrier group, 32 showed significant ASO or AH increases and none showed significant de- Table 3-Follow-Up Data: Effect of Penicillin Treatment on: (1) Persistence of Streptococci in Throat Cultures of Carriers; (2) Rates of Streptococcal "Infections" The Per cent of Positive Follow-Up Cultures Varies with the Extent of Antibiotic Treatment (1) Per cent of Carriers Positive Three Months or More School School School Year G* B W (2) Per cent of "Infections" with Positive Cultures at Three Week Follow-Up School School School Year G* B* W Schools included in penicillin treatment program. FEBRUARY,

5 Table 4 Analysis of Signs and Symptoms in Respiratory Infections ( ) No Clinical Difference Was Noted Between Children with Positive Cultures and Those with Negative Cultures Positive Culture Negative Culture Signs and Symptoms Number Per cent Number Per cent Red throat Red throat with exudate Swollen glands Earache Fever over 101'F creases, suggesting that about 25 per cent of these children had subclinical infections which could not have been diagnosed without the routine throat culture and immunologic studies. In the group of 79 children who had no positive cultures during the course of the school year, ten showed significant increases in either ASO or AH titer, indicating the probable occurrence of streptococcal infection not revealed by routine throat cultures. The fact that 36 per cent of the carriers and only 15 per cent of the noncarriers had ASO titers of 256 or greater adds further evidence to this opinion. In Figure 1 the geometric mean ASO titers of children in acute and convalescent stages of respiratory illness are compared with the mean titers of streptococcal carriers. The groups with positive cultures are further analyzed by graphing throat culture colony counts against ASO titers. There is no immunologic distinction between the group of ill children and the carriers, and none can be noted on comparing the children who had "four or five plus" cultures with those who had cultures with fewer streptococci. Among observations of a more general nature, comparisons of streptococcal carrier rates and infection rates in the various age groups revealed no significant differences between the six- to nine-year-old classes and the nine-to twelve-year-old group. Likewise, family size and economic status as determined by the criterion of number of people per bedroom did not seem to influence the frequency with which a child became a carrier, or to affect the infection rate. Only 10 per cent of the families of children who had positive cultures had members with streptococci in their throat and only about one-half of the group of family contacts had streptococci of the same type as the school child. Discussion The program described in the foregoing was originally initiated to determine practical and effective methods for community control of beta-hemolytic streptococcal infections, with a view to the primary prevention of rheumatic fever. This epidemiological study seemed particularly urgent in view of the spreading popularity of the streptococcal detection programs already in operation (47 programs by 1959) throughout the United States.5 Because of the results demonstrated in this study, we question the efficacy and advisability of programs in which penicillin treatment is recommended for any child with a respiratory illness in whose throat streptococci are found. 246 VOL. 51. NO. 2, A.J.P.H.

6 STREPTOCOCCAL INFECTIONS IN SCHOOL CHILDREN Throughout the four years of our study, more than 50 per cent of the children under observation had one or more positive cultures for beta-hemolytic streptococci at some time during the school year. Thus, when attempts were made to eradicate streptococci from the throats of the carriers as well as from the children with clinical infection, it was necessary to treat one-half of a school population with penicillin. Further, despite carrier rates ranging up to 29.8 per cent, comparable to those cited elsewhere,1 the incidence of streptococcal illness remained relatively low with the monthly incidence of "streptococcal infection" varying from 1.4 to 2.4 per 100 children studied. This rate is comparable to that reported recently from England by Williams,6 who recorded 1.9 infections per 100 children per month in a similar school population. Brumfitt7 emphasized the difficulty in clinical differentiation between the streptococcal and nonstreptococcal illnesses and suggested the term benign streptococcal sore throat for the poorly defined illness due to streptococci occurring in an endemic pattern. To help determine which child, among those who had streptococci in the throat, had a streptococcal infection and thus deserved treatment, an attempt was made to differentiate between the child who was carrying streptococci when he developed intercurrent respiratory illness and the child whose illness was due solely to the presence of pathogenic streptococci. The following methods were used: (1) Analysis of the symptomatology-in children with respiratory illness, there was no significant difference in the signs or symptoms between the group who had positive cultures and the group who had negative cultures; (2) bacterial counts-although a greater percentage of the children with pure or almost pure growth of streptococci was found in the group of patients with respiratory illness than among well children who had cultures taken routinely, a large number of asymptomatic children also had a heavy growth of streptococci in their throats, and, even in the group of children with exudative pharyngitis and fever, approximately 50 per cent had low bacterial counts; (3) immunologic methods --serums obtained at the acute and Table 5-Antistreptolysin-O and Antihyaluronidase Data: Titer Changes in Carriers, Noncarriers, and Children with Respiratory Illness Titer Increases Were Noted in a Large Number of Carriers and in Only a Small Per cent of Children with "Infections" Number with Significant Mean ASO Titer Mean AH Titer Number Titer Changes Acute Conv. Acute Conv. Category of Cases (2 Tube) Stage Stage Stage Stage N1-N2 58 6T B1-B2 35 6T R1-R T R1-R T Serums Code: Ni-N2 =Respiratory illness, negative culture Bi-B2 =Respiratory illness, positive culture Ri = Routine at start of school year R2 =Routine-following onset of carrier state R3 =Routine -nd of year (no positive cultures in year) FEBRUARY,

7 Figure A Lf) A50 Aczate, Phase. COLONY COUNT 3+I + SERUM CODE B,-Ba RI-R2 0~~E 0 ~A ASO titer change is plotted logarithmically against bacterial colony counts. On abscissa is plotted the initial ASO titer; on the ordinate the convalescent ASO titer. Points on the lower oblique line represent children whose ASO titer neither rose nor fell during convalescence. The upper oblique line represents an increase of 100 per cent in titer in convalescence. Each point represents the geometric mean ASO titer for the group of children designated by the code system in the box at the bottom of the chart. Serums Code: N1-N2 ==Respiratory illness, negative culture B1-B2 =Respiratory illness, positive culture Ri R2 10 =Routine-at start of school year =Routine-following onset of carrier state convalescent stage, at the same time as the initial and follow-up cultures on children with respiratory illness, showed no significant difference in the titers of two streptococcal antibodies between the children who had positive cultures and those who did not. In addition, a number of children without respiratory illness had streptococcal antibody titer increases, indicating occurrences of occult infection. Correlation of the ASO titer changes with the bacterial counts 248 VOL. 51. NO. 2, A.J.P.H.

8 STREPTOCOCCAL INFECTIONS IN SCHOOL CHILDREN performed on cultures of the children who had positive cultures indicated no greater titer rise in the groups with heavier streptococcal growth. Summary An epidemiologic study of streptococcal infection has been conducted in three Philadelphia schools since In each of the years, comparable data indicated a relatively high carrier rate for beta-hemolytic streptococci and a low incidence of respiratory infection accompanied by throat cultures positive for streptococci. It was not possible to distinguish the child with streptococcal infection from the child with nonstreptococcal infection on clinical grounds. Bacterial counts on positive cultures did not help to differentiate between streptococcal carriers who had intercurrent respiratory infections and the children with bonafide streptococcal disease. Serologic studies for two antistreptococcal antibodies were also not helpful in this regard. In v7iew of the data cited in this paper, we question the advisability of instituting school streptococcal detection programs which are based on current means of detecting streptococcal infection. ACKNOWLEDGMENT-The authors wish to thank Mrs. Shirley Earle for her work as technician on this program. REFERENCES 1. Cornfeld, D.; Werner, G.; Weaver, R.; Bellows, M. T.; and Hubbard, J. P. Streptococcal Infection in a School Population: Preliminary Report. Ann. Int. Med. 49:1305 (Dec.), Werner, G.; Cornfeld, D.; Hubbard, J. P.; and Rake, G. A Study of Streptococcal Infection in a School Population: Laboratory Methodology. Ibid. 49:1320 (Dec.), Harris, T. N. Complement Fixation versus Streptococcal Nucleoprotein in Sera of Patients with Rheumatic Fever and Others. J. Exper. Med. 87:57, Harris, T. N., and Harris, S. Studies in the Relation of Hemolytic Streptococcus to Rheumatic Fever, V. Streptococcal Antihyaluronidase (Mucin Clot Pre. vention) Titers in the Sera of Patients with Rheumatic Fever, Streptococcal Infection and Others. Am. J. M. Sc. 217:174, Bennett, A. M. Personal communication, New York, N. Y.: American Heart Association. 6. Williams, R. E. 0. Laboratory Diagnosis of Streptococcal Infection. WHO Bull. 19, Brumfitt, W.; O'Grady, F.; and Slake, J. D. H. Benign Streptococcal Sore Throat. Lancet 2 :419, Drs. Cornfeld, Hubbard, and Harris are associated with the Department of Preventive Medicine, University of Pennsylvania School of Medicine, Philadelphia, Pa. Dr. Weaver is with the Division of Medical Services, Board of Public Education, Philadelphia. This paper was presented before a Joint Session of the American Heart Association, the American School Health Association, and the Maternal and Child Health and Public Health Nursing Sections of the American Public Health Association at the Eighty-Seventh Annual Meeting in Atlantic City, N. J., October 22, This study was conducted by the Department of Public Health and Preventive Medicine, the University of Pennsylvania School of Medicine, and the Children's Hospital of Philadelphia, Pa. The National Heart Institute aided this investigation by Research Grants (Nos. H-3301 and H-869). FEBRUARY

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