Adolescent Medicine

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Chlamydia trachomatis Infections in Adolescents

Thomas A. Bell, MD, MPH*

Chlamydia trachomatis is the sexually transmitted disease that has the greatest impact on the reproductive health of adolescents. Being a sexually experienced adolescent is a major risk factor for acquiring this organism through coitus"5 The reasons for this depend on the organism, the host, and the nature of medical care and public health programs. Reviews of the chlamydiae have appeared in other recent Clinics issues. 2 . 28. 42. 48 I shall try to complement them by emphasizing the clinical problems faced by the clinician who treats adolescent patients. MICROBIOLOGY

Chlamydia trachomatis has two biologic variants: those that cause lymphogranuloma venereum, which are rare in adolescents in the United States, and those that cause trachoma and genital infections. The oculogenital variants of C. trachomatis inhabit columnar or cuboidal epithelium, which is usually in the urethra, cervix, endometrium, fallopian tube, or, in infants, in the respiratory tract. Repeated infection may cause scarring. This is especially prominent in trachoma, but it may also be relevant to genitourinary infections. 38 Symptoms usually appear at least 1 week after acquisition of the infection. The duration of untreated chlamydial infection is diffiicult to ascertain because it is difficult to find infected persons with credible stories of protracted sexual abstinence. Subclinical infection for nearly 2 years is possible (C. Lipinski, personal communication). EPIDEMIOLOGY An estimated 3 to 5 million cases of C. trachomatis infection occur in the United States annually!l at an estimated cost of $2.2 billion. 58 Chlamydia trachomatis is so common that its detection is one of the most important parts of the care of sexually experienced adolescents. 56 Certainly the nature of adolescents' sexual 'Assistant Professor of Pediatrics and Epidemiology, University of Washington, Seattle, Washington

Medical Clinics of North America-Vol. 74, No. 5, September 1990

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behavior and their lack of routine medical care contribute to their burden of disease. Physiologic characteristics such as ectropion of the endocervical epithelium') may also contribute. Chlamydia trachomatis is less confined to the urban poor than is Neisseria gonorrhoeae or Treponema pallidum. High rates have been found in rural New Mexico"·!6 and Alaska,55 and in suburban Long Island, ]'I;ew York.!! Estimates of the prevalence of chlamydial infection in sexually experienced adolescent women are generally in the range of 8%!2 to 35%,49 and in comparable asymptomatic adolescent men, 8%46 to 22%.! Ideally, health departments should have the responsibility of detecting cases in the general population and of ensuring that sexual consorts of infected persons are treated. In practice, health departments have done little to try to control or eradicate chlamydial infections. The plans of the Centers for Disease Control to start a national control program analogous to those for gonorrhea and syphilis were thwarted by the epidemic of human immunodeficiency virus (HIV). Local health departments also have lacked the resources to deal with chlamydial infections. Screening programs are left to other agencies and to private practitioners. Fortunately, some methods for screening adolescents are affordable, and can be applied to populations of asymptomatically infected persons. These methods deserve wider use than they have received to date, especially as governmental programs to control the spread of chlamydial infections are inadequate. CLINICAL MANIFESTATIONS AND DIAGNOSIS The clinician treating the adolescent patient has two responsibilities for detecting chlamydial infections. The better defined is that of making an accurate microbiologic diagnosis in the patient with an illness possibly caused by C. trachomatis. The most frequently encountered manifestations are urethritis and epididymitis in men, and cervicitis, urethritis/urethral syndrome, endometritis, salpingitis, and perihepatitis in women. 2. 28 A specific microbiologic diagnosis suggests specific measures to follow, such as treatment, notification of sexual consorts, and, in certain jurisdictions, reporting of a communicable disease. The means available for making a specific diagnosis have proliferated as a result of advances in molecular biology. However, many such methods have technical limitations or costs that are prohibitive for adolescent patients or publicly funded health care. The Centers for Disease Control have published policy guidelines for management of chlamydial infections that assume that specific diagnostic tests will not be used in many clinical situations. 9, 10 Their proposed alternative approach is to manage many clinical syndromes with which C. trachomatis has been associated as though it were their primary etiology. This philosophy is problematic because many manifestations of chlamydial infection defy precise definition, and because evidence for their chlamydial etiology is inconclusive. Also, chlamydial infections have clinical manifestations that are not specific for given microbial or other etiologies. 6 In men, the most common manifestation of chlamydial infection is urethritis. For more than a decade, its detection has been based on either observation of purulent exudate, of which patients are not always aware, or on microscopic examination of secretions obtained by swabbing the urethra. However, this approach may be unnecessarily invasive. An adequate microbiologic diagnosis may be made by examining an apparent urethral discharge for N. gonorrhoeae and testing it for C. trachomatis. If the patient is symptomatic but has no expressible discharge, the first-voided aliquot of urine may be cultured for N. gonorrhoeae and tested for pyuria by using a dipstick that detects leukocyte esterase. 33 , 47 Detection of pyuria

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with dipsticks is more sensitive than is examination of a urethral specimen and is as sensitive as microscopic examination of urine for leukocytes. 39 The microbiologic diagnosis of a chlamydial infection in this situation may be negotiated between the patient and the physician. A more definitive alternative is that of swabbing the urethra and testing the sample by any of various means, such as isolation· or a method that detects chlamydial antigens or DNA. The less traumatic alternative is that of using an enzyme immunoassay to test the sediment from the first-catch aliquot of urine for chlamydial antigen. Almost all such cases of pyuria in adolescent men are caused by urethritis. If the symptoms cannot be explained because there is no pyuria, prostatitis should be considered. The other problem for the clinician treating the male adolescent is that of detecting asymptomatic infections in persons who are being evaluated for unrelated conditions. The prevalence of chlamydial infection in almost all populations of male adolescents is high enough to warrant screening their urine with dipsticks. Those whose first-catch aliquot contains leukocyte esterase require further evaluation. As with overt urethritis, chlamydial or gonococcal infection is present in approximately half of such cases. 33, 47 Another method of detecting pyuria is examination of noncentrifuged urine with a hemocytometer counting chamber or a comparable disposable device. A concentration of 10,000 leukocytes/mll( = 10/mm3 ) indicates pyuria. 13 Leukocytes in urine lyse spontaneously. Consequently, the concentration detected by microscopy will decrease with time, but the amount ofleukocyte esterase will increase. 25 Detection of chlamydial infection in female adolescents presents differcnt problems. Symptoms of genital infection in females are usually not specific for the infected organ, and chlamydial infections arc less often symptomatic than in males. The clinical diagnoses that most clearly warrant specific microbiologic diagnosis and appropriate treatment are pelvic inflammatory disease 27 and perihepatitis. 57 The clinical criteria used to diagnose these conditions are imprecise, and they are sufficiently serious that a specific microbiologic diagnosis is almost always warranted. 19 However, chlamydial infections are sufficiently common in adolescents that their presence does not preclude the presence of some other condition such as appendicitis. The more common problems facing the clinician are the evaluation of complaints of vaginal discharge or dysuria and the assessment of the health of the patient's genital tract during evaluation for some unrelated purpose such as contraception, routine screening for cervical cancer, or evaluation of pregnancy. The patient presenting with the complaint of vaginal discharge may have some other condition such as a bacterial vaginosis or Candida infection, for which the pelvic examination allows specific testing. For the adolescent patient, cost-benefit considerations suggest that specific testing for C. trachomatis is clearly justified if a test of reasonable cost is available. 31.32,41 Similarly, sexually transmitted infections are often the cause of dysuria in women, and this complaint in an adolescent should not be casually considered to be caused by postcoital bacterial cystitis. The acute urethral syndrome is usually defined as the presence of symptoms in the lower urinary tract in the absence of a specific pathogen. It is one of the conditions for which the Centers for Disease Control recommend specific antichlamydial therapy.9. 10 However, the basis for this is debatable. In a manner analogous to infection in men, C. trachomatis infects the female urethra. Among female adolescents, it may be isolated from both the urethra in one third,4, 6 and from the urethra alone in less than 5%.6 In the first study to define the role of C. trachomatis in acute urethral syndrome, its isolation was associated with more than 8000 leukocytes/ml of uncentrifuged midstream urine that contained fewer than 34,000 colonies of bacteria/m I in the absence of herpes genitalis or vaginitis. 52 Of the 16

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women who satisfied these criteria, C. trachomatis was isolated from the urethra of only 25%. In a study in contraception clinics, C. trachomatis was isolated from 33% of women with "sterile pyuria."" In a British venereology clinic, C. trachomatis was isolated from the urethra of 12 of 25 women with pyuria and no other pathogen, versus 2 of 19 without pyuria but with a pathogen. However, N. gonorrhoeae was the most common cause of pyuria among women without conventional bacterial causes of cystitis,'}7 Studies of patients in an adolescent clinic,6 a family medicine clinic,5 an emergency room,14 and a urology clinics found little or no evidence for C. trachomatis as a cause of the acute urethral syndrome. A general problem in the studies of acute urethral syndrome is the use of midstream urine, which is appropriate for studying bacteriuria, cystitis, and pyelonephritis, but is likely to miss the pus associated with urethritis, which will be washed out in the first part of the urine stream. Diagnosis of the acute urethral syndrome might be enhanced by use of leukocyte esterase dipsticks to test both first-catch and midstream aliquots of urine. The most common manifestation of chlamydial infection is mucopurulent cervicitis. The first reported objective criteria for the diagnosis of mucopurulent cervicitis were the presence of yellow or green secretions on a swab from the endocervix or the presence of an average of 10 polymorphonuclear leukocytesl X 1000 field in the five most concentrated fields where the cells were in monolayers on a 2 cm 2 smear with fewer than 100 vaginal epithelial cells. Either of these findings was present in half of the women with C. trachomatis infection, and they were not associated with other infections. 7 These rigorous criteria for interpretation of Gram-stained smears make them cumbersome for use in busy clinical settings. Other studies have not necessarily found them useful in predicting the presence of C. trachomatis (Table 1).1.5 17.22,24. 26,30. 34, 36, 40, 54, 59 The prevalence of C. trachomatis in populations in which mucopurulent cervicitis has been studied has ranged from 7%7 to 22%.6.7 The range of prevalence rates of mucopurulent cervicitis, as diagnosed by the presence of purulent cervical secretions, friability of the cervical epithelium, or erythema of same, was 3% in university students 34 to 50% in a venereology clinic. 7 The most sensitive indicator of chlamydial infection in any of the studies was mucopus (64% in a venereology clinic). 7 In studies in which physical signs of mucopurulent cervicitis Table 1. Sensitivity and Positive Predictive Value of Gross Physical Signs of Mucopurulent Cervicitis for Isolation of Chlamydia trachomatis

from Unselected Patients

SENSITIVITY AND POSITIVE PREDICTIVE VALUE* REFERENCE

POPULATION

6 30 54 17 15 40 7 24 26

Adolescent Adolescent Adolescent University Contraception Gynecology Venereology Venereology Venereology

Mucopus

Erythema

Friability

-,40 -,43 -.51 32, 32t 52, 31 t NS 29,29 42, 13 54,25 39,23 27, 19 { significantly associated } 64,26 NS NS 36,24 NS NS { 25,23

Abbreviation: NS = not significantly associated. *Values not reported for signs without significant association with isolation of C. trachomatis. tNot significant in multivariate analysis.

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were associated with the presence of C. trachomatis, thc positive predictive values of these signs were from 13% for erythema l7 to 51% for mucopus." The best performance of Gram-stained smear of endocervical secretions was in a venereology clinic, where it was 91 % sensitive but only 29% predictive of chlamydial infection. 7 In an adolescent clinic, the smear was associated with chlamydial infection only among blacks, but among them, it was 96% sensitive and 53% predictive. 30 Three studies have found an independent association of mucopurulent cervicitis with N. gonorrhoeae,26. 40 • .59 whereas three others have noV·14 ..16 This is one of the more puzzling aspects of mucopurulent cervicitis, because N. gonorrhoeae is obviously pyogenic. Other organisms associated with mucopurulent cervicitis have been Ureaplasma urealyticum34 and herpes simplex virus. 26.59 Trichomonas vaginalis is associated with hemorrhagic ectocervicitis (colpitis macularis) but not with endocervical mucopus. 26 Oral contraception was associated with mucopurulent cervicitis in one study. 59 In summary, the evidence for C. trachomatis' causing mucopurulent cervicitis is strong, and that for the etiologic role of N. gonorrhoeae is weaker but plausible. Mucopurulent cervicitis as diagnosed by physical examination and the Gram-stained smear has low predictive value for the presence of either organism and low sensitivity for both organisms in most studies. The poor performance of mucopurulent cervicitis as an indicator of gonococcal and chlamydial infection in clinical studies may reflect the methodologic difficulties of its diagnosis. The original criteria for interpretation of the Gram-stained smear' are probably too complex for widespread use. Associations with Ureaplasma urealyticum colonization and bacterial vaginosis are probably spurious or confounded because most women with either condition do not have inflammation. The association of oral contraception may reflect a physiologic change in the endocervical epithelium. Thus, the urethral syndrome and mucopurulent cervicitis are such nonspecific indicators of infection that vast numbers of women would be treated unnecessarily if all such cases were treated. Accurate diagnosis of chlamydial infection in women requires the use of specific tests.

LABORATORY TESTS FOR CHLAMYDIA TRACHOMATlS Detailed comparisons of diagnostic methods have recently been published. 2 23.28 Presumptive laboratory diagnosis of C. trachomatis infections has become more widely available in recent years with the advent of several methods to detect chlamydial antigens or DNA in lieu of isolating the organism in cell culture. The claims of manufacturers of these tests are difficult to evaluate because the versions of the tests that are used for published studies may not be those currently marketed. Many of the manufacturers' data on the performance of these tests are not published. Tests for C. trachomatis are not without their problems of application and interpretation. Isolation of the organism by a competent laboratory may be considered to be almost perfectly specific but is less than perfectly sensitive. The method for collection of specimens may be of great importance, as evidenced by the 18 to 31 % improvement in the rate of isolation from the cervix when nylon brushes instead of swabs were used to collect specimens from the endocervix. 29 However, such brushes are more likely than swabs to cause the cervix to bleed. Nonculture methods are usually less specific, and the clinician must interpret them in the context of the clinical presentation. False-positive results may have serious physical and emotional consequences for patients. In forensic cases, isolation is the only satisfactory method of detection.

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TREATMENT If a chlamydial infection has been definitively diagnosed either by isolation or an appropriate test for chlamydial antigens or DNA, the choice of treatment is relatively simple. Chlamydia trachomatis is susceptible to several inexpensive antimicrobials, especially tetracyclines, erythromycin, and sulfonamides. Quinolones and rifampin are also active against it, but they are less useful clinically."" The most recent recommendations from the Centers for Disease Control are that adults be treated preferentially with a 7 day course of doxycycline, 100 mg twice a day, or tetracycline, 500 mg four times a day. Alternatives include erythromycin base, 500 mg four times a day, erythromycin ethylsuccinate, 800 mg, or sulfisoxazole, 500 mg four times a day for 10 days. 10 These regimens are not the only ones that are potentially useful. Erythromycin is available in a sustained-release form that needs to be taken only three times per day. One of the more intriguing alternatives, yet one that has received little attention, is a 3-day course of co-trimoxazole (trimethoprim/sulfamethoxazole).50 Amoxicillin may have some activity, but sufficient doubt exists about its efficacy in vivo to preclude its use as the drug of choice. A characteristic of most studies of the treatment of chlamydial infections is a cure rate of less than unity."3 However, the Centers for Disease Control recommendations do not include one for a test of cure "when treatment has been completed" because "antimicrobial resistance ... to recommended regimens has not been observed. "10 This is in contrast to studies of treatment of gonorrhea with modern drugs, and suggests that re-infection is not a sufficient explanation. Lack of compliance with protracted regimens may explain some failures, but such compliance is a fact of life. Some refractory infections almost certainly result from the organism's hardiness, which, fortunately, has yet to include genetic resistance to commonly used antimicrobials. The treatment of clinical syndromes that may be caused by C. trachomatis is more controversial. Recommendations from the Centers for Disease Control tend to favor treating these syndromes as if C. trachomatis were the only important pathogen involved. 9, 10 In contrast, the Canadian Ministry of Health has recently recommended that these syndromes generally be treated as if the patient were infected with both C. trachomatis and N. gonorrhoeae. '8 Whether empiric treatment for both chlamydial and gonococcal infection should be given at the same time before the results of tests for specific organisms are available will depend on the likelihood that the patient will return for treatment later, and on the prevalence of tetracycline-resistant N. gonorrhoeae in the community. In most areas, such resistant strains are common enough to preclude the use of tetracyclines as the sole treatment for gonorrhea. Management of microscopic pyuria detected by dipstick analysis includes a pursuit of a specific diagnosis. In some cases, treatment may be warranted based on a presumptive diagnosis of urethritis before a specific microbiologic diagnosis is available. Cost-benefit analyses of patients seen in venereologic clinics have revealed that empiric treatment of all patients irrespective of diagnosis would be costeffective, if not necessarily judicious. 32 However, such analyses provide justification for empiric treatment of microscopic pyuria, which is, of course, a more specific indicator of chlamydial infection than is mere attendance at a clinic. The treatment of choice would be a tetracycline. Of these, doxycyline is the easiest to use and more likely to be taken compliantly. 20 Mucopurulent cervicitis and symptoms of the acute urethral syndrome respond to antichlamydial therapy, but not as well if C. trachomatis is not present. 3,5. 5l Doxycycline is the treatment of choice. Sexual consorts of adolescents with C. trachomatis deserve specific antichla-

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mydial therapy. Those with illnesses possibly of chlamydial etiology but whose spccific tests are ncgative arc more problematic. vVhen possible, sexual consorts should be examined and counseled together. Sometimes a consort will be found to be infected even though the index patient's tests arc negative. Empiric therapy for persons with negative tests should be offered with attention to the unique characteristics of both the index patient and the eonsort(s). SUMMARY The guidelines of the Centers for Disease Control should be applied with appreciation of their limitations. The serious sequelae of chlamydial infections in young patients warrant vigorous antichlamydial therapy and specific microbiologic diagnosis. Until public health authorities implement control programs, the efforts of individual practitioners will probably be the mainstay of the fight against C.

trachomatis.

AUTHOR'S NOTE A recently published cost-based decision analysis strongly favors screening the urine of sexually experienced male adolescents with dipsticks rather than specific tests for C. trachomatis. A screening program becomes cost-effective if the prevalence of infection is more than 21 %. (From Randolph AG, Washington AE: Screening for Chlamydia trachomatis in adolescent males: A cost-based decision analysis. Am J Public Health 80:545, 1990; also see Alexander ER: Is it cost-beneficial to screen adolescent males for Chlamydia? Am J Public Health 80:531, 1990.) REFERENCES 1. Adger H, Shafer M-A, Sweet RL, et al: Screening for Chlamydia trachomatis and Neisseria gonorrhoeae in adolescent males: Value of first-catch urine examination. Lancet 2:944, 1984 2. Batteiger B, Jones RB: Chlamydial infections. Infect Dis Clin North Am 1:55, 1987 3. Bell TA, Ebenezer MR: Chlamydia trachomatis and Neisseria gonorrhoeae in asymptomatic family planning patients in rural New Mexico. West J Med 150:543, 1989 4. Bell TA, Farrow JA, Stamm WE, et al: Sexually transmitted diseases in females in a juvenile detention center. Sex Transm Dis 12:140, 1985 5. Berg AO, Heidrich FE, Fihn SD, et al: Establishing the cause of genitourinary symptoms in women in a family practice: Comparison of clinical examination and comprehensive microbiology. JAM A 251:620, 1984 6. Blythe MJ, Katz BP, Orr DP, et al: Historical and clinical factors associated with Chlamydia trachomatis genitourinary infection in female adolescents. J Pediatr 112: 1000, 1988 7. Brunham RC, Paavonen J, Stevens CE, et al: Mucopurulent cervicitis-the ignored counterpart in women of urethritis in men. N Engl J Med 311:1, 1984 8. Bump RC, Copeland WE: Urethral isolation of the genital mycoplasmas and Chlamydia trachomatis in women with chronic urologic complaints. Am J Obstet Gynecol 152:38, 1985 9. Centers for Disease Control: Chlamydia trachomatis infections: Policy guidelines for prevention and control. Morbid Mortal Weekly Rep 34 (suppl 3S):53S, 1985 10. Centers for Disease Control: Sexually transmitted diseases treatment guidelines, 1989. In Holmes KK, Mardh P-A, Sparling PF, et al (eds): Sexually Transmitted Diseases, ed 2. New York, McGraw-Hill, 1990, p A-I 11. Fisher M, Swenson PD, Risucci D, et al: Chlamydia trachomatis in suburban adolescents. J Pediatr 11:617, 1987

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15. 16. 17. 18. 19. 20. 21. 22. 23. 24. 25. 26. 27. 28. 29. 30. 31. 32. 33. 34. 35. 36.

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JJ, Rettig pJ, Kaplan DW: Prevalence of cervical Chlamydia trachomatis and Neisseria gonorrhoeae in female adolescents. Pediatrics 71:333, 1983 Gillenwater JY: Detection of urinary leukocytes by Chemstrip-L. J Urol 125:383, 1981 Greenberg RN, Rein MF, Sanders CV, et al: Urethral syndrome in women [letter]. JAM A 245:923, 1981 Handsfield HH, Jasman LL, Roberts PL, et al: Criteria for selective screening for Chlamydia trachornatis infection in women attending family planning clinics. JAMA 255:1730, 1986 Harrison HR, Boyce WT, Haffner WHJ, et al: The prevalence of genital Chlamydia trachornatis and mycoplasmal infections during pregnancy in an American Indian population. Sex Transm Dis 10:184, 1983 Harrison HR, Costin M, Meder JB, et al: Cervical Chlamydia trachomatis infection in university women: Relationship to history, contraception, ectopy, and cervicitis. Am J Obstet Gynecol 153:244, 1985 Health and Welfare Canada: 1988 Guidelines for the treatment of sexually transmitted diseases in neonates, children, adolescents and adults. Can Dis Weekly Rep 14S2:1, 1988 Jacobsen L, Westriim L: Objectivized diagnosis of pelvic inflammatory disease. Diagnostic and prognostic value of routine laparoscopy. Am J Obstet Gynecol 105:1088, 1969 Jordan WC: Doxycycline vs. tetracycline in the treatment of men with gonorrhea: The compliance factor. Sex Transm Dis 8:105, 1982 Judson FN: Assessing the number of genital chlamydial infections in the United States. J Reprod Med 30:269, 1985 Katz BP, Caine VA, Jones RB: Diagnosis of mucopurulent cervicitis among women at risk for Chlamydia trachornatis infection. Sex Transm Dis 16:103, 1989 Kellogg JA: Clinical and laboratory considerations of culture vs antigen assays for detection of Chlamydia trachomatis from genital specimens. Arch Pathol Lab Med 1133:453, 1989 Kent GP, Harrison RH, Berman SM, et al: Screening for Chlamydia trachomatis infection in a sexually transmitted disease clinic: Comparison of diagnostic tests with clinical and historical risk factors. Sex Transm Dis 15:51, 1988 Kierkegaard H, Feldt-Rasmussen U, Horder M, et al: Falsely negative urinary leukocyte counts due to delayed examination. Scand J Clin Lab Invest 40:259, 1980 Magder LS, Harrison HR, Ehret JM, et al: Factors related to genital Chlamydia trachornatis and its diagnosis by culture in a sexually transmitted disease clinic. Am J Epidemiol 28:298, 1988 Mardh P-A: An overview of infectious agents of salpingitis, their biology, and recent advances in methods of detection. Am J Obstet Gynecol 138:933, 1980 McGregor JA: Chlamydial infections in women: A review. Ob stet Gynecol Clin North Am 16:679, 1989 Moncada J, Schachter J, Shipp M, et al: Cytobrush in collection of cervical specimens for detection of Chlamydia trachomatis. J Clin Microbiol 27:183, 1989 Moscicki B, Shafer M-A, Millstein SG, et al: The use and limitations of endocervical Gram stains and mucopurulent cervicitis as predictors for Chlamydia trachomatis in female adolescents. Am J Obstet Gynecol 157:65, 1987 Nettleman MD, Jones RB: Cost-effectiveness of screening women at moderate risk for genital infections caused by Chlamydia trachomatis. JAMA 260:207, 1988 Nettleman MD, Jones RB, Roberts SD, et al: Cost-effectiveness of culturing for Chlamydia trachornatis. A study in a clinic for sexually transmitted diseases. Ann Intern Med 105:189, 1986 O'Brien SF, Bell TA, Farrow JA: Use of a leukocyte esterase dipstick to detect asymptomatic infection with Chlamydia trachomatis or Neisseria gonorrhoeae in asymptomatic adolescent male detainees. Am J Public Health 78:1583, 1988 Paavonen J, Critchlow CW, DeRouen T, et al: Etiology of cervical inflammation. Am J Ob stet Gynecol 154:556, 1986 Paavonen J, Roberts PL, Stevens CE, et al: Randomized treatment of mucopurulent cervicitis with doxycyline or amoxicillin. Am J Ob stet Gynecol 161:128, 1989 Paavonen J, Stevens CE, W0lner-Hanssen P, et al: Colposcopic manifestations of cervical and vaginal infections. Obstet Gynecol Surv 43:373, 1988

12. Fraser 13. 14.

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37. Panja SK: Urethral syndrome in women attending a clinic for sexually transmitted diseases. Br J Vener Dis 59:179, 1983 38. Patton DL, Kuo C-C, Wang S-P, et al: Distal tubal obstruction induced by repeated Chlamydia trachomatis salpingeal infection in pig-tailed macaques. J Infect Dis 155:1292, 1987 39. Perera SAB, Jones C, Srikantha V, et al: Leukocyte esterase test as rapid screen for nongonococcal urethritis. Genitourin Med 63:380, 1987 40. Phillips RS, Hanff PA, Holmes MD, et al: Chlamydia trachomatis cervical infection in women seeking routine gynecologic care: Criteria for selective testing. Am J Med 86:515, 1989 41. Phillips RS, Aronson 0, Taylor WC, et al: Should tests for Chlamydia trachomatis cervical infection be done during routine gynecologic visits? An analysis of the costs of alternative strategies. Ann Intern Med 107:188, 1987 42. Rosenfeld WD, Clark J: Vulvovaginitis and cervicitis. Pediatr Clin North Am 36:489, 1989 43. Sanders LL, Harrison HR, Washington AE: Treatment of sexually transmitted chlamydial infections. JAM A 255:1750, 1986 44. Schachter J, Stoner E, Moncada J: Screening for chlamydial infections in women attending family planning clinics--evaluation of presumptive indicators for therapy. West J Med 138:375, 1983 45. Shafer M-A, Beck A, Blain B, et al: Chlamydia trachomatis: Important relationships to race, contraception, lower genital tract infection, and Papanicolaou smear. J Pediatr 104:141, 1984 46. Shafer M-A, Prager V, Shalwitz, et al: Prevalence of urethral Chlamydia trachomatis and Neisseria gonorrhoeae among asymptomatic, sexually active adolescent boys. J Infect Dis 156:223, 1987 47. Shafer M-A, Schachter J, Moscicki B, et al: Urinary leukocyte esterase screening test for asymptomatic chlamydial and gonococcal infections in males. JAM A 262:2562, 1989 48. Shafer M-A, Sweet RL: Pelvic inflammatory disease in adolescent females. Pediatr Clin North Am 36:513, 1989 49. Soren K, Willis E: Chlamydia and the adolescent girl. Am J Dis Child 143:51, 1989 50. Stamm WE, Guinan ME, Johnson C, et al: Effect of Neisseria gonorrhoeae treatment regimens on simultaneous infection with Chlamydia trachomatis. N Engl J Med 310:545, 1984 51. Stamm WE, Running K, McKevitt M, et al: Treatment of acute urethral syndrome. N Engl J Med 304:956, 1981 52. Stamm WE, Wagner KF, Amsel R, et al: Causes of the acute urethral syndrome in women. N Engl J Med 303:409, 1980 53. Terruhn V: Formwandel und Epithelentwicklung der Portio vaginalis uteri von der Begurt bis zur Adoleszenz. Arch Gynecol 229:123, 1980 54. Thejls H, Rahm VA, Rosen G, et al: Correlation between chlamydia infection and clinical evaluation, vaginal wet smear, and cervical swab test in female adolescents. Am J Ob stet Gynecol 157:974, 1987 55. Toomey KE, Rafferty MP, Stamm WE: Unrecognized high prevalence of Chlamydia trachomatis cervical infection in an isolated Alaska population. JAMA 258:53, 1987 56. U.S. Preventive Services Task Force: Guide to Clinical Preventive Services: An Assessment of the Effectiveness of 169 Interventions. Report of the US Preventive Services Task Force. Baltimore, Williams & Wilkins, 1989, p xlviii 57. Wang S-P, Eschenbach DA, Holmes KK, et al: Chlamydia trachomatis as cause of FitzHugh-Curtis syndrome. Am J Obstet Gynecol 138:1034, 1980 58. Washington AE, Johnson RE, Sanders LL: Chlamydia trachomatis infections in the United States: What are they costing us? JAMA 257:2070, 1987 59. Willmott FE: Mucopurulent cervicitis: a clinical entity? Genitourin Med 64:169; 1988

Address reprint requests to Thomas A. Bell, MD, MPH SC-36 Department of Epidemiology University of Washington Seattie, WA 98195

Chlamydia trachomatis infections in adolescents.

The guidelines of the Centers for Disease Control should be applied with appreciation of their limitations. The serious sequelae of chlamydial infecti...
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