PEDIATRICS Vol. 106 No. 2 August 2000, pp. 276-281

Perineal Group A Streptococcal Disease in a Pediatric Practice

Nancy P. Mogielnicki, PA, MPH^*, Joseph D. Schwartzman, MD, and John A. Elliott, PhD^§

From the Departments of ^* Pediatrics and Community and Family Medicine and  Pathology, Dartmouth Medical School, Lebanon, New Hampshire; and ^§ Respiratory Diseases Branch, Centers for Disease Control and Prevention, Atlanta, Georgia.

	ABSTRACT

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Objective.   This study was designed to document the frequency and define the clinical, epidemiologic, and microbiologic characteristics of perineal disease caused by group A -hemolytic streptococci (GAS) in a pediatric practice in which increased numbers of cases had been observed.

Methods.  Clinical, epidemiologic, and microbiologic data were collected on all culture-confirmed cases of perineal GAS disease during the calendar year 1997. GAS isolates from clinical cases and a comparison group of children with GAS pharyngitis were analyzed by T typing, emm gene analysis, and pulsed-field gel electrophoresis (PFGE).

Results.  Twenty-three cases of GAS perineal disease were diagnosed during 4530 office visits in 1997. Thirteen cases had perianal disease, 8 had vulvovaginal infection, and 2 were infected at both sites. No cases of penile disease were identified. Infections peaked in late winter and early spring and affected children with an average age of 5 years with a range of perineal, gastrointestinal, and genitourinary symptoms. Analysis of T and emm types showed the majority (82%) of perineal isolates to be T 28 emm 28, showing 2 closely related PFGE patterns. In contrast, the pharyngeal isolates were distributed among 6 different T and emm types.

Conclusion.  Perineal infection caused by GAS may be a relatively common diagnosis in a pediatric or family practice setting. There may be specific GAS types that have a tropism for perineal tissues but the mechanism of infection is yet to be established.  Key words:  streptococcal infections, vulvovaginitis, perineum, skin diseases, infectious.

Perineal disease caused by group A -hemolytic streptococci (GAS) has been reported in the pediatric literature for >30 years. Most common are case reports of perianal^1-14 or vulvovaginal disease,^15-21 with occasional reports of streptococcal balanitis,^22-25 but informal inquiry suggests that these diagnoses continue to be relatively rare among clinicians who care for children.

This research was prompted by the observation of an apparent increase in diagnosed cases of both perianal disease and vulvovaginitis caused by GAS beginning in 1995 in a small pediatric practice. Most cases occurred in epidemiologically linked clusters but others seemed to be isolated infections. Increased case finding appeared to mirror increased streptococcal pharyngitis diagnosis in the community. Perianal and vulvovaginal disease seemed to have many epidemiologic and clinical characteristics in common.

This study was designed to document the validity of these observations and to define the clinical, epidemiologic, and microbiologic characteristics of perineal GAS disease by examining clinical data on children with these infections, by analyzing their perineal and pharyngeal streptococcal isolates, and by comparing these findings with the existing literature on the subject.

	METHODS

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Clinical cases were defined as all children who presented to this Lebanon, New Hampshire, pediatric practice during the 1997 calendar year with perineal symptoms and physical findings consistent with published reports of GAS infection and whose cultures of symptomatic tissues were positive for GAS. Cases that were diagnosed presumptively and treated without culture were excluded, as were recurrences of infection shortly after treatment, considered to be relapse. Culture material was collected by rolling or stroking a dry swab over the affected perianal or intralabial tissues.

Epidemiologic data, including date of diagnosis, age, gender, town of residence, day care and/or school, and parents' occupations were collected on each case. Clinical data included symptoms, findings on physical examination, presence or absence of clinical pharyngitis, and recent GAS exposure. Laboratory evidence of GAS pharyngitis was collected primarily in cases with throat symptoms or evidence of clinical pharyngitis on physical examination.

Analysis of available isolates from clinical cases and from a comparison group of children with GAS pharyngitis was performed by the Streptococcus Laboratory of the Centers for Disease Control and Prevention and included T typing and 5' emm sequence analysis of individual GAS isolates and pulsed-field gel electrophoresis (PFGE) pattern analysis of an isolate subgroup.

A literature search was conducted to compare characteristics of this case series with previous studies, to identify common characteristics of perianal, vulvovaginal, and penile GAS disease, and to review hypotheses relating to transmission of GAS to a perineal site.

	RESULTS

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In 1997, 23 culture-confirmed cases of perianal and/or vulvovaginal GAS infection were diagnosed during approximately 4530 routine office visits. No cases of penile infection were identified. Table 1 presents data related to these cases, which are numbered according to chronologic order of diagnosis and clustered according to epidemiologic associations. Data include month of diagnosis, age, gender, site of infection, town of residence, school and/or day care attended, and GAS isolate characteristics.

Thirteen cases had perianal infection only, 8 had vulvovaginal infection only, and 2 cases were infected at both sites, yielding a rate of approximately 1 case of perineal GAS disease per 200 patients seen, 1 case of perianal disease per 300, and 1 case of vulvovaginal disease per 450 patient visits.

Figure 1 shows the age and gender distribution of these cases. The age distribution reveals a mean age and median age of 5 years and a range from 1 to 11 years. Fifty-seven percent of the entire sample was female. Ten (77%) of the 13 patients with perianal disease were male.

View larger version (19K): [in this window] [in a new window]   Fig. 1.   Age and gender distribution of 23 cases of perineal streptococcal disease.

Figure 2 presents the seasonal distribution of these cases and of all cases of GAS pharyngitis diagnosed during 1997 at the medical center of which the pediatric practice is a component. Over half (57%) of cases of GAS disease occurred in the months of March, April, and May. Review of laboratory records does not show an increase in the background rate of streptococcal pharyngitis diagnosis during 1997. 

View larger version (22K): [in this window] [in a new window]   Fig. 2.   Seasonal distribution of 23 cases of perineal GAS disease in a pediatric practice and cases of pharyngeal GAS at Dartmouth Hitchcock Medical Center, 1997.

In the families of all cases at least 1 parent was employed. Occupations included medicine, education and school athletics, law, and business, reflecting the generally high socioeconomic status of families in this pediatric practice.

Patients presented with a variety of clinical syndromes, but all had symptoms referable to perineal tissues. Perianal and/or vulvar pruritis was the most common symptom in the group as well as the most common chief complaint. Among those with perianal disease, symptoms ranged from perianal pruritis or tenderness to abdominal pain and rectal bleeding. Girls with vulvovaginitis complained of a variety of symptoms including dysuria, pruritis, tenderness, and discharge.

Perianal and/or vulvovaginal erythema was universally present on examination but mentioned by parents in fewer than half the cases. This inflammation was sometimes mild and pink, but more often described as "beefy" red, and occasionally associated with edema. A papular rash was at times noted on buttocks or labia, but lesions did not resemble impetigo. Only 3 patients in the group had pus or discharge visible on examination and 1 girl with vulvovaginitis had a scarlatiniform rash over the lower abdomen. One patient developed guttate psoriasis, thought to be related to his perianal GAS disease.

On review of systems only 5 patients complained of current or recent sore throat. On examination, however, 11 cases had a clinical pharyngitis, defined by erythema and occasional exudate. None had petechiae. Nine of these were tested for pharyngeal GAS infection, and 8 were positive. Three of the 12 cases without clinical pharyngitis or sore throat were tested for pharyngeal GAS, and all were positive. None of the cases was febrile at the office visit, but 3 had a history of recent fever of 102°F or higher.

Eighteen cases reported contact with a recently diagnosed case of GAS disease, and 10 of these had specific exposure to someone with perineal infection. Examination of town, day care, and/or school associations in Table 1 reveals several types of epidemiologic links among cases. The patients lived in 8 different small towns in New Hampshire and Vermont, attended 8 different elementary schools, and 12 different day cares and nursery schools. Although 7 cases had no evident connection to others in the group, the remainder were linked to at least one other case by familial relationship, friendship, school, or day care association.

Table 1 also shows microbiologic analysis of GAS isolates that were available for typing. Fourteen of the 17 perineal isolates were T 28 emm 28 and all of these showed 1 of 2 PFGE patterns, designated A and C. T 9/13/14/27/28 emm 77 isolates showed a PFGE pattern designated B. Microbiologic GAS analysis supported most known epidemiologic associations. The data in the cluster which includes cases 2, 4, 11, 12 and 13 suggest that siblings 2 and 4 were initially infected with a genetically similar organism. When case 2 returned 6 months later, her isolate at that time was the same type as her friend, case 11. Cases 15 and 17 attended the same school but were in different classrooms and were not known to be friends.

Table 2 compares these results with analysis of a group of 14 pharyngeal GAS isolates obtained from children who presented with sore throat. This pharyngeal group was slightly older with a mean and median age of 6 and range of 3 to 11 years. Seven (50%) were female, and the chronologic distribution was similar to cases of perineal disease. Patients were not cultured to rule out perineal disease. The 17 perineal isolates consisted of 3 different T/emm types with 94% of the perineal specimens belonging to only 2 T/emm types. In contrast, the 14 pharyngeal isolates were more evenly distributed among 6 different T/emm types. (The fact that the T 12 isolate and the T nontypeable isolate had identical emm types and PFGE patterns suggests that they should be considered in the same group.)

	DISCUSSION

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The data of this case series, in conjunction with the previous literature on the subject, provide a consistent picture of a pediatric infectious disease. It is not clear whether identification of this cluster of perineal infections was a local phenomenon or evidence of more widespread change. The frequency of visits for perianal infection in this series (approximately 1 case per 300 patients seen) was higher than the 1/2000 visit frequency noted by Amren et al in 1966¹ and closer to the frequency of 1/218 visits for perianal disease noted in active case finding by Kokx and colleagues in 1987.⁴ Comparable frequencies for vulvovaginal and penile infection are not available.

A high index of suspicion may have contributed to the case numbers in this series, although evidence suggesting that perineal infections do not resolve spontaneously argues against this explanation. Several case reports note symptom persistence, often for many months, until appropriate diagnosis and effective treatment are instituted.^3,6,7,19,20

Although perineal streptococcal infection may occur in adults,^6,17,37 it is primarily a disease of early childhood. All pediatric cases in the literature and in this series are prepubertal, with ages ranging from infancy to preteen years, but clustering in the preschool and early school age group.^1-25 This age distribution mirrors that of streptococcal impetigo but is markedly different from streptococcal pharyngitis, which is seen more often in children 5 to 15 years old.³⁶

Other clinical and epidemiologic characteristics of our 1997 series are consistent with previous case descriptions. Vulvovaginitis and balanitis are gender-specific infections, and the majority of perianal disease occurs in males.^1-14 In perianal disease, pruritis and/or pain are the most common symptoms, and erythema is a universal finding in symptomatic children.^1-14 The presenting symptoms of vulvovaginitis may be more variable, but erythematous tissues are present in most cases.^18-20 Disease is usually mild if diagnosed early, but perianal disease in particular can result in significant problems with stool retention, constipation, and fecal incontinence^3,8 and can lead to avoidable invasive procedures^8,19 or accusations of sexual abuse.²³ Acute guttate psoriasis may be triggered by perineal GAS disease and can be treated effectively with antibiotics.^6,7,11

Many hypotheses are offered in the literature to explain transmission of GAS to perineal tissues, but none has been conclusively proven. The seasonal distribution of cases in this and other series is consistent with the typical patterns of GAS pharyngitis in temperate climates³⁶ suggesting an association with respiratory infection.^17,21 This case series offers indirect support for the theory of autoinoculation or gastrointestinal spread from an infected nasopharynx because 92% of the pharyngeal GAS tests were positive, whether or not symptoms and/or signs of pharyngitis were present. This rate of concurrence between pharyngeal and perineal culture result is higher than the 28% to 75% range cited in previous pediatric reports,^{1,2,4,6,11-14,18,20,23,25} which have a combined rate of approximately 55%. Recovery of GAS from the nose or throat was rare in the literature on asymptomatic anal and vaginal GAS carriage in health care workers.^{27-29,31,32,34} The fact that all of the cases in this series were diagnosed within a month of symptom onset suggests that GAS may be eliminated from the nasopharynx with time, leading to negative results of pharyngeal tests in cases in which symptoms or asymptomatic carriage have been present for a longer period.

The issue of asymptomatic perineal carriage among children has been addressed by Asnes and Vail,³⁸ who found a 6% rate of perianal GAS among 100 children with GAS pharyngitis. Schoenknecht and colleagues³⁹ cultured 133 adults and 22 children, all healthy, and recovered perianal GAS from only 1 young man. Heller and colleagues¹⁶ studied 50 children with symptoms of vulvovaginitis and recovered GAS in 10%, but vaginal cultures of 21 asymptomatic control children did not reveal any GAS carriage.

Evidence against nasopharyngeal to perineal spread has been presented by Ferrieri and colleagues⁴⁰ who documented the transmission of GAS first to normal skin, then to pyoderma lesions and finally to the nasopharynx. Barzilai and colleagues¹⁴ suggest that perianal pruritis from GAS infection may lead to scratching and consequent digital-oral inoculation. Several cases in this study had perineal symptoms preceding clinical pharyngitis including 1 boy who was treated with topical steroids for "proctitis" and returned 1 week later with fever and GAS pharyngitis.

Gastrointestinal carriage from swallowed organisms is an alternative transmission hypothesis. Although Hare and Maxted⁴² documented GAS in the stool of patients with scarlet fever many years ago, there is little recent evidence to support or refute this hypothesis conclusively. There are cases of streptococcal proctocolitis in the literature,^4,19,43 and one study of an asymptomatic carrier of perianal organisms noted GAS in the colon.³⁹ Abdominal pain, stooling problems, and rectal bleeding are often cited as symptoms associated with some perianal GAS disease, but it is not clear whether this is related to intestinal infectious processes or to stool-withholding, constipation, and perianal bleeding secondary to external pain and inflammation.

The possibility of airborne spread has been a significant factor in postsurgical GAS wound infection since McKee and colleagues demonstrated airborne transmission of GAS from a perianal site in 1966.^27-29,32,34 The literature on GAS wound infection, recently summarized by Kolmos and colleagues, contains 3 decades of case reports that frequently implicate asymptomatic perianal or vaginal carriage as the source of infection.^26-35 Fomites such as toilet seats or towels and bathwater have also been implicated in cases of perineal GAS disease,^4,12 but their role is unclear.

The universal day care, preschool, or school attendance rate among these cases reflects the experience of most children in this pediatric practice and may be a significant environmental factor. Saxén and colleagues¹² have reported a small outbreak within a day care center, and epidemiologic patterns within this 1997 case series suggest day care and school transmission as well.

There is abundant support within these data and in the previous literature for the use of the inclusive term "perineal." Many case reports note coexistent perianal-vulvovaginal or perianal-penile disease,^{1,5,11,14,19,23,25,37} and infection at different sites in epidemiologically linked contacts is shown in this series (Table 1.) It is likely that portal of entry and mode of spread to these 3 sites are closely linked.

The field of molecular genetics has provided increasingly sensitive tools for epidemiologic analysis of GAS disease that traditionally relied on serologic typing of T and M antigens. In this study serologic T typing was supplemented by molecular determination of the variable portion of the emm gene, which can usually predict the M serotype.⁴⁴ In addition, the strains were compared by PFGE, which relies on the ability of certain restriction enzymes to digest the entire bacterial genome into large fragments that can be separated by electrophoresis into a pattern sorted by molecular mass.

The small number of strains distinguished by these techniques and causing GAS perineal disease in this area is remarkable. Although there is diversity among the small number of pharyngeal isolates analyzed, the perineal isolate analysis shows significant homogeneity despite geographic and chronologic variability. These data suggest that there may be epidemiologic links among cases that are not obvious and that the T 28 emm 28 strain may carry factors that promote tropism for perineal tissues.

Historic changes in both the epidemiology of GAS disease and in the distribution of serotypes have been described^45-47 and may be reflected in the relative distribution of T 28 and M 28, which are relatively common serotypes among isolates causing both superficial and invasive infection.^12,40,45 In 1966 Amren et al¹ found 6 different T types among 10 perianal isolates, but none of T 28. In 1987 Kokx et al⁴ analyzed 12 perianal isolates, 5 of which (42%) were T 28 and found the same type in an asymptomatic control. Saxén et al¹² found genotypically identical T 28 strains in their analysis of day care-related perianal disease in 1997. Colman and colleagues⁴⁵ studied the serotypes of GAS isolates collected in Britain during 1980 to 1990 and found M type R 28 in 16% of isolates from vaginal cultures, and in 26% of GAS puerperal infections. T 28 is the serotype reported in 33% of cases of GAS wound infections and invasive disease caused by carriers of perianal or vulvovaginal GAS.^27,29-35

	CONCLUSION

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This study has documented the relatively common diagnosis of perineal GAS disease in a general pediatrics practice. These data suggest that pediatric and family practice clinicians should be alert for this phenomenon, especially at times of increased GAS diagnosis in the community and among preschool and young school-aged children with perineal, gastrointestinal, or genitourinary symptoms or with psoriatic lesions.

These data show that perineal GAS infection in this geographic area over a period of several months was caused primarily by 2 closely related strains, suggesting that there may be factors specific to T type 28, emm 28, which may increase the likelihood of perineal infection. Although young age and day care or school attendance are likely risk factors for infection, conclusive evidence of a specific mode of transmission remains elusive. Documentation of perineal GAS disease at other practice sites and further analysis of suspect GAS types will be necessary for clarification of this phenomenon.

	ACKNOWLEDGMENTS

We wish to thank Stacy Walters, MD, Maryellen Belletsky, and Diane Kittredge, MD, for participation in case finding and specimen collection; Deborah Zuaro, MAT, MT, Christine Mulligan, MT, and Brian Jackson, MD, for microbiologic analysis and laboratory data review at Dartmouth Hitchcock Medical Center; Bernard Beall, PhD, for emm typing at the Centers for Disease Control and Prevention; and Gene H. Stollerman, MD, and James K. Todd, MD, for expert advice and support.

	FOOTNOTES

Received for publication Aug 10, 1999; accepted Dec 8, 1999.

Address correspondence to Nancy P. Mogielnicki, PA, MPH, Community Health Center, Dartmouth Hitchcock Medical Center, One Medical Center Drive, Lebanon, NH 03756. E-mail: nancy.p.mogielnicki{at}hitchcock.org

	ABBREVIATIONS

GAS, group A -hemolytic streptococci; PFGE, pulsed-field gel electrophoresis.

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