ADOLESCENT GYNECOLOGY, PART 11: THE SEXUALLY ACTIVE ADOLESCENT 0031-3955/99 $8.00 + .OO

ADOLESCENTS AND SEXUALLY TRANSMITTED DISEASES

Mitchell A. Gevelber, MD, and Frank M. Biro, MD

As much as the care of adolescents with sexually transmitted diseases (STDs) is an issue of proper diagnosis and treatment, it is also an issue of patient education and disease prevention. Diagnoses of STDs in adolescents are as much psychosocial diagnoses as medical diagnoses. This article discusses the developmental aspects of adolescent sexuality that place adolescents at risk for acquiring STDs, the diagnosis and management of cervicitis and genital ulcers, and prevention strategies in which pediatricians can play a significant role.

SCOPE OF THE PROBLEM

Approximately 3 million teenagers in the United States acquire STDs each year?* STDs have substantial personal and public costs. A landmark report on STDs in the United States and their burden on individual health and economic consequences was issued by the Institute of Medicine. Estimates of total costs for STDs, excluding HIV, were $10 billion in 1994.37

The increasing prevalence of HIV among adolescents heightens the need for early detection and treatment of other STDs, as highlighted by a 1997 publication by the Centers for Disease Control and Prevention (CDC) Advisory Committee for HIV and STD Pre~enti0n.l~ Epidemiologic studies reveal a synergistic effect between HIV and other STDs; the risk for HIV infection was increased twofold to fivefold in persons infected with other STDs, including both ulcerative (e.g., syphilis, chancroid, or herpes) and nonulcerative (Neisseria gonorrhoeae and Chla- mydia trachomatis) pathogens. In HIV-infected hosts, ulcers, which bleed easily and can come into contact with mucosal surfaces during sexual contact, provide an exudative source of HIV. Inflammatory STDs serve as cofactors that facilitate transmission of HIV by increasing HIV viral shedding and the HIV RNA copy

From the Division of Adolescent Medicine, Children’s Hospital Medical Center, Cincin- nati, Ohio

PEDIATRIC CLINICS OF NORTH AMERICA

VOLUME 46 NUMBER 4 * AUGUST 1999 ~

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number (“viral load”) in genital secretions. The report recommends that early detection and treatment of curable STDs that facilitate HIV transmission should be a central and explicit component of all strategies to prevent the transmission of HIV.

RISK FOR SEXUALLY TRANSMITTED DISEASE IN THE CONTEXT OF ADOLESCENT DEVELOPMENT

Adolescent sexual development is a normal aspect of human development, expressed variably from birth to adulthood.33 To the extent that the risk for STDs is related to sexual behaviors, an understanding of adolescent sexual development and sexual activity is important to understanding the risk for STD acquisition in teens. Numerous developmental variables contribute to increased STD risk among adolescents, including psychosexual maturation, cognitive de- velopment, biologic maturation, knowledge and perceptions, management skills, and sociocultural context?

It is incumbent on pediatricians to view adolescent sexuality not simply as risk-taking behaviors (with potential pitfalls of STDs and pregnancy) but rather as a developmental process of developing healthy attitudes and behaviors in which pediatricians may play an important role.29 This lifestyle perspective enables pediatricians to gain insight into the decision making of teens and possible avenues for intervention.

Psychosexual Maturation

Psychosexual maturation includes developing comprehension of relation- ships by adolescents. Through the teenage years, adolescents develop the ability to maintain emotionally intimate friendships and relationships. For some, this includes becoming comfortable with their sexuality and exploring sexual behav- iors. As teens begin to initiate sexual behaviors, their communication skills and abilities to negotiate behaviors with their partners, or their comfort with their own sexuality, may be inadequate. For example, adolescents may be sufficiently comfortable to engage in intercourse but not to discuss sexual behaviors with their partners (“erotophobia”).30

Cognitive Development

During adolescence, usually at about the age of 14 years, the ability to think abstractly (formal operations) develops, permitting adolescents to use abstract concepts, consider the future, and think hypothetically. Younger adolescents may not have acquired the ability to think about the consequences of their actions. Older teens, despite developing formal operations, may not display safe sexual behaviors, possibly reflecting their sexual inexperience, difficulty with condom negotiation, or impact of emotions on decision Some adolescent behav- iors have been understood as an aspect of egocentrism, the personal fable, ”It won‘t happen to me.” Adolescents who have never had an STD, compared with those who have, perceive STDs as being less prevalent among friends and adolescents in general.% In addition, adolescents perceive a greater prevalence of STDs among adolescents in general than among their friends, suggesting a lower perceived personal risk.

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Knowledge of Sexually Transmitted Diseases and Sociocultural Context

Teens often lack accurate knowledge about the signs and symptoms of STDs, as well as awareness of the asymptomatic nature of some STDS.~ Perceived parental and family support, communication among family members, and paren- tal supervision and monitoring may play an important protective role? Adoles- cents whose parents are available and provide supervision tend to engage in less sexual risk-taking behavior; in part, this may be mediated through limiting the time that young couples spend alone. Peer groups may also contribute to adolescent behaviors and knowledge. Adolescents who perceive their friends as using condoms are more likely to plan to use condoms them~e1ves.l~ A relation- ship exists between substance use and sexual activity (and risk for STD acquisi- tion); this relationship is, however, unlikely causal and more likely reflects a lifestyle containing several elements of health risk.32

Biologic Development

Biologic factors contribute to the increased susceptibility of female adoles- cents to STDs through anatomic and biobehavioral aspects. Female adolescents with an earlier onset of puberty relative to peers are more likely to engage in sexual activity earlier. Those who initiate intercourse at younger ages tend to accumulate more sexual partners and use less discretion when selecting partners and are less likely to use condoms at first intercourse? In the first few years after menarche, the columnar epithelium extends to the outer surface of the cervix (ectocervix). Columnar epithelium is more susceptible than squamous epithelium to gonorrhea or chlamydia infection.% Furthermore, it is in this transition zone from squamous to columnar epithelium that human papillomavi- rus infection and dysplasia occur.12

Sexual Activity

The Youth Risk Behavior Surveyls is a large, nationally representative survey of US private and public high school students in grades 9 to 12 and provides a measurement of adolescent sexual involvement. These statistics represent the behaviors of students in school and not the behaviors of adolescents who were absent or out of school. Statistics from the 1995 survey (compared with the same surveys in 1990, 1991, and 1993) suggested that rates of sexual activity among US high school students had stabilized and that the rate of condom use at last intercourse had increased over that time.ffi More recent results from the 1997 survey show a continuation of the trend for increased condom use and a decrease in the rates of sexual intercourse (48.4% ever sexually active).ls Rates were higher for black adolescents (72.6%) than white (43.6%) or Hispanic adoles- cents (52.2%). In 1995, the median age reported for first intercourse was similar for male and female adolescents, 16.4 years for male and 16.5 years for female adolescents; median age for first intercourse was younger for black male adoles- cents (13.6 y). Although surveys from 1990 to 1993 reported a significantly younger age of first intercourse for black female adolescents than white or Hispanic female adolescents, no significant difference was reported in the 1995 survey. Between 1990 and 1997, no change occurred in the percentage of all students reporting engaging in intercourse in the previous 3 months (3438%).

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The rates of students reporting four of more lifetime sexual partners remained relatively stable between 1990 and 1997 at 16% to 19%. The rates of students reporting four or more partners were higher among black students than white or Hispanic students. The reported use of condoms among all students at last intercourse increased from 46% in 1990 to 56% in 1997. Male adolescents consis- tently reported higher rates of condom use than did female adolescents, with black male adolescents reporting higher rates than white or Hispanic male adolescents.

Sexual activity has a much broader meaning than just penile-vaginal penetra- tion, and simply asking adolescents whether they are sexually active is not sufficient. Adolescents may have had intercourse only once, more than a year ago, and are not presently sexually active. Adolescents may not be physically active during intercourse but may be passive. Oral or anal sex may not be considered ”sexually active.” A recent survey of 2066 Los Angeles County high school students who had never had intercourse highlights the variety of sexual activities in which these adolescents engage.59 Despite describing themselves as “virgins,“ 29% had engaged in masturbation of an opposite gender partner, 31% had been masturbated by a partner of the opposite gender, 9% had engaged in heterosexual fellatio with ejaculation, 10% had engaged in heterosexual cunnilin- gus, and 1% had engaged in heterosexual anal intercourse.

DISCUSSING SEXUALITY WITH ADOLESCENTS

Adolescents and their parents perceive that one of the roles of physicians is to discuss sensitive topics, including sexuality.5z A s&dy of 845 high school students in Boston reported that 82% wanted to hear information about STDs, 73% about condoms, 70% about sex, 80% about safe sex, and 85% about HIV; however, more than half of adolescents also reported feeling uncomfortable initiating discussions of these issues with their physicians. In a study of parental opinions of topics to be discussed during an office visit, discussion of STDs was believed to be important by 91%, safe sex by 85%, and contraception by 85%.’’ Some parents believed that several topics should not be discussed, including STDs (4%), safe sex (8%), and contraception (7%). Discussion of topics dealing with sexuality demand that physicians be respectful of the needs and sensitivi- ties of patients and their parents.

A complete sexual history is an important, challenging component of the adolescent visit. The sexual history taking allows physicians the opportunity to provide preventive counseling and education, and appropriate treatment and intervention. Questions should focus on sexual orientation (i.e., heterosexual, homosexual, or bisexual), gender of sex partners, sexual practices (i.e., anal, oral, or vaginal intercourse), number of sexual partners (lifetime and past 3-6 mo), history of sexual abuse or rape, use of contraception and protection (e.g., con- doms), and history of STDs or pregnancy.

One study found that self-report is a reliable method of gathering informa- tion about adolescents’ sexual activity and contraceptive behaviors. The most reliable reflection of STD risk relates to gathering specific information about condom use with the last two or more partners (rather than general questions about condom use patterns, i.e., always, sometimes, or never).6z The validity regarding self-reported sexual history is not consistent across all studies.69 One study found agreement between information on several STDs that was from an interview in a research study and from a chart review; however, accuracy was only fair regarding information on Pap smears and urogenital human

ADOLESCENTS AND SEXUALLY TRANSMI'ITED DISEASES 751

papillomavirus infections.36 A study evaluating the accuracy of self-reported pregnancy and STD in an adolescent population at high risk for HN found that, over a 1-year period, only 46% of patients accurately reported STDs and pregnancies when verified by chart review; 40% of patients reported no STD or pregnancy despite chart documentation.26 Although this study was unable to identify the source of poor validity, it questioned the validity of self-reported sexual behavior. Interviewing adolescents privately (without their guardians present) and discussing issues of confidentiality may be helpful in developing rapport and eliciting a useful history.

SCREENING AND TREATING SEXUALLY TRANSMITTED DISEASES IN ADOLESCENTS

Much has been written regarding diagnosis and treatment of STDs, includ- ing a thorough review published in Pediatric Clinics of North This article discusses two clinical presentations, cervicitis and genital ulcers, as para- digms for diagnostic and management issues. For the convenience of readers, Table 1 shows the most recent treatment guidelines from the CDC.

Cervicitis

Cervicitis may be classified into ectocervicitis (involving the squamous epithelium, which lines the ectocervix and vagina) and endocervicitis (involving the columnar epithelium of the endocervical canal). Ectocervicitis may occur as a result of infection with trichomoniasis or candidiasis. Herpes simplex virus (HSV) may cause both ectocervicitis and endocervicitis. The major causes of endocervicitis, as defined by the CDC 1998 STD Treatment Guidelines (gonor- rhea, chlamydia, and mucopurulent cervicitis), are discussed below.

Epidemiology

Chlamydia and gonorrhea are the two most frequently reported notifiable infectious diseases in the United States.m Chlamydia is the most common bacte- rial sexually transmitted infection in the United States, with an estimated 4 million cases reported annually." CDC surveillance data show that among 15- to 19-year-old female adolescents in 1996, the rate of gonorrhea is 757 per 100,000 and the rate of chlamydia is 2068 per 100,000.60 Prevalence data on chlamydia infection among sexually active adolescents typically range from 5% to 12%17; however, rates of infection among high-risk groups at STD clinics may be as high as 40%.1° Although the overall incidence of gonorrhea has declined since 1975, female adolescents (15-19 y), when adjusted for history of sexual activity, have a twice the rate of gonorrheal infection as that of any other age group16 (Fig. 1).

The risk for acquiring these infections is associated with specific demo- graphics, sexual behaviors, and level of sexual activity. Adolescents who are pregnant, incarcerated, users of injectable drugs, gay, prostitutes, or runaways are at increased risk. Earlier onset of sexual activity and inconsistent condom use put adolescents at increased risk. The use of oral contraceptives (possibly by extending the columnar epithelium to the ectocervix) and concurrent gonoccocal infection are risk factors for chlamydia1 infection. Of note, the presence of one

ADOLESCENTS AND SEXUALLY TRANSMI'ITED DISEASES 751

papillomavirus infections.36 A study evaluating the accuracy of self-reported pregnancy and STD in an adolescent population at high risk for HN found that, over a 1-year period, only 46% of patients accurately reported STDs and pregnancies when verified by chart review; 40% of patients reported no STD or pregnancy despite chart documentation.26 Although this study was unable to identify the source of poor validity, it questioned the validity of self-reported sexual behavior. Interviewing adolescents privately (without their guardians present) and discussing issues of confidentiality may be helpful in developing rapport and eliciting a useful history.

SCREENING AND TREATING SEXUALLY TRANSMITTED DISEASES IN ADOLESCENTS

Much has been written regarding diagnosis and treatment of STDs, includ- ing a thorough review published in Pediatric Clinics of North This article discusses two clinical presentations, cervicitis and genital ulcers, as para- digms for diagnostic and management issues. For the convenience of readers, Table 1 shows the most recent treatment guidelines from the CDC.

Cervicitis

Cervicitis may be classified into ectocervicitis (involving the squamous epithelium, which lines the ectocervix and vagina) and endocervicitis (involving the columnar epithelium of the endocervical canal). Ectocervicitis may occur as a result of infection with trichomoniasis or candidiasis. Herpes simplex virus (HSV) may cause both ectocervicitis and endocervicitis. The major causes of endocervicitis, as defined by the CDC 1998 STD Treatment Guidelines (gonor- rhea, chlamydia, and mucopurulent cervicitis), are discussed below.

Epidemiology

Chlamydia and gonorrhea are the two most frequently reported notifiable infectious diseases in the United States.m Chlamydia is the most common bacte- rial sexually transmitted infection in the United States, with an estimated 4 million cases reported annually." CDC surveillance data show that among 15- to 19-year-old female adolescents in 1996, the rate of gonorrhea is 757 per 100,000 and the rate of chlamydia is 2068 per 100,000.60 Prevalence data on chlamydia infection among sexually active adolescents typically range from 5% to 12%17; however, rates of infection among high-risk groups at STD clinics may be as high as 40%.1° Although the overall incidence of gonorrhea has declined since 1975, female adolescents (15-19 y), when adjusted for history of sexual activity, have a twice the rate of gonorrheal infection as that of any other age group16 (Fig. 1).

The risk for acquiring these infections is associated with specific demo- graphics, sexual behaviors, and level of sexual activity. Adolescents who are pregnant, incarcerated, users of injectable drugs, gay, prostitutes, or runaways are at increased risk. Earlier onset of sexual activity and inconsistent condom use put adolescents at increased risk. The use of oral contraceptives (possibly by extending the columnar epithelium to the ectocervix) and concurrent gonoccocal infection are risk factors for chlamydia1 infection. Of note, the presence of one

754 GEVELBER & BIRO

Figure 1. Gonorrhea (GC) and chlamydia rate in women by age group. Light bar = GC; medium bar = chlamydia. (Data from Division of STD Prevention: Sexually transmitted disease surveillance, 1995. Atlanta, United States Department of Health and Human Ser- vices, September 1996; and Abma J, Chandra A, Mosher W, et al: Fertility, family planning, and women's heath: New data from the 1995 National Survey of Family Growth. National Center for Health Statistics, Vital Health Stat 2339, 1997.)

STD increases the risk that others are also present and should suggest the need to further evaluate for other STDs, including HIV.

Approximately one third of adolescent women with chlamydia or with gonorrhda have no symptoms6; however, all infections may have significant sequelae despite the absence of symptoms. Adolescents with cervicitis are at increased risk for genital upper tract infections (PID) and the complications of infertility, perihepatitis, ectopic pregnancy, and chronic pelvic pain. Between 10% and 20% of untreated gonococcal infections in women lead to PID.'O One to three percent of adolescents with untreated gonorrhea develop disseminated gonococcal infection with classic findings, including arthralgias, septic arthritis, tenosynovitis, and petechial or pustular skin lesions.1o Pregnant women with

754 GEVELBER & BIRO

Figure 1. Gonorrhea (GC) and chlamydia rate in women by age group. Light bar = GC; medium bar = chlamydia. (Data from Division of STD Prevention: Sexually transmitted disease surveillance, 1995. Atlanta, United States Department of Health and Human Ser- vices, September 1996; and Abma J, Chandra A, Mosher W, et al: Fertility, family planning, and women's heath: New data from the 1995 National Survey of Family Growth. National Center for Health Statistics, Vital Health Stat 2339, 1997.)

STD increases the risk that others are also present and should suggest the need to further evaluate for other STDs, including HIV.

Approximately one third of adolescent women with chlamydia or with gonorrhda have no symptoms6; however, all infections may have significant sequelae despite the absence of symptoms. Adolescents with cervicitis are at increased risk for genital upper tract infections (PID) and the complications of infertility, perihepatitis, ectopic pregnancy, and chronic pelvic pain. Between 10% and 20% of untreated gonococcal infections in women lead to PID.'O One to three percent of adolescents with untreated gonorrhea develop disseminated gonococcal infection with classic findings, including arthralgias, septic arthritis, tenosynovitis, and petechial or pustular skin lesions.1o Pregnant women with

ADOLESCENTS AND SEXUALLY TRANSMITIED DISEASES 755

gonorrhea or chlamydial infection are at increased risk for postpartum endome- tritis; their infants are subject to conjunctivitis, and, in the case of chlamydia, pneumonitis. As discussed earlier, cervicitis places infected adolescents at in- creased risk for HIV infection.

Clinical Presentation

Presenting symptoms of cervicitis commonly include vaginal discharge, dysuria, urinary frequency (caused by associated urethritis), dyspareunia, and vaginal bleeding with intercourse. The classic finding on physical examination is mucopurulent cervicitis, defined as a purulent, yellow-green endocervical exudate visible in the endocervical canal or on an endocervical swab specimen. The cervix is often friable, bleeding when the sample is obtained, and tender to palpation. Microscopic examination of the exudate with saline or Gram stain reveals the presence of white blood cells.

Diagnostic Testing

Cell culture remains the gold standard for evaluation and the only evidence allowed in forensic cases for both gonorrhea and chlamydia. Both culture tech- niques have a specificity approaching 100%; the culture does not grow if the organism is not present. Unlike culture for gonorrhea, which has a sensitivity of 80% to 95%, culture for chlamydia is only 70% to 85% sensitive; the culture may be negative despite the presence of infection.

Newer diagnostic methods for gonorrhea and chlamydia that are more sensitive, more rapid, and more easily handled and processed than cultures are available. These methods include DFA (direct fluorescent antibodies directed against organisms, detected through staining with fluorescent antibody), EIA (enzyme-linked immunoassays using antibodies labeled with an enzyme), nu- cleic acid hybridization using a nucleic acid probe complementary to a section of the organism's DNA or RNA, PCR (polymerase chain reaction using DNA polymerase to amplify oligonucleotide complements to a specific DNA strand of the organism), and LCR (ligase chain reaction using DNA ligase to amplify oligonucleotide complements to specific DNA strands of the organism). Sensitiv- ies and specificities of these methods vary according to method, collection of specimen, and specimen source (e.g., urinary, endocervical, or urethral). Each method has advantages and disadvantages?, lo, 40, 65, DFA and EIA are quickly processed. DFA allows direct evaluation for sample adequacy (through the visualization of columnar cells) but is subject to interlaboratory variability. DFA and EL4 are less sensitive in low-prevalence populations because specimens from female adolescents in low-prevalence populations contain fewer organ- isms.l0 Nonamplified DNA probes are easy to use, and one sample may be used to test for both gonorrhea and chlamydia. Amplified DNA techniques (LCR and PCR) are highly sensitive, and studies suggest that they may be most useful in noninvasive sampling (i.e., urine or vaginal introitus specimensy -; however, because of the exquisite sensitivity of these methods, the tests (especially PCR) are susceptible to contamination and lower specificity.

Issues of specimen collection, storage, and transportation are important to culture and nonculture methods for gonorrheal and chlamydia1 diagnosis. Chla- mydia sp are obligate, intracellular organisms, and viable organisms for culture must be collected from urethral or endocervical cells (not vaginal secretions). Culture specimens should be obtained by rotating a swab for 10 to 20 seconds firmly against the endocervical canal (1-2 cm inside); one should avoid swabs

756 GEVELBER & BIRO

with wooden shafts, which interfere with culture. Nonculture test kits provide specific swabs to be used. Several methods require that specimens be stored and transported at specific temperatures. Of note, preliminary studies suggest that self-collected swabs from the vaginal introitus may be an alternative to direct endocervical specimens.67

Treatment

The management options for specific etiologic organisms for cervicitis are shown in Table 1. Single-dose therapy should be used as much as possible; this strategy eliminates issues of compliance. One article discussed the overall effectiveness of the treatment of chlamydia, using twice-a-day administration of doxycycline for a duration of 1 week. Although two thirds of patients took sufficient quantity to effectively cure chlamydia (96% cure), 10% of patients took six or fewer capsules; the overall effectiveness of a prescription for 1 week's therapy was 86'3'0." All patients treated for cervicitis should abstain from sexual intercourse for at least 7 days following the completion of their and their partners' therapy.

Patients treated for gonorrhea, either definitive or presumptive, should also receive treatment for chlamydia because chlamydia occurs as a coinfection in as many as 50% of cases of gonococcal cervicitis. Furthermore, treatment of patients with gonorrhea with two agents may prevent the development of resistant strains of gonorrhea. Because the rate of treatment failure with recommended protocols is very low, "tests of cure" are no longer rec0mnended.2~ Physicians should be aware that PCR and LCR may remain positive for up to 3 weeks despite effective treatment because of the detection of residual DNA targets following the clearance of infection.l0

Although either gonorrhea or chlamydia may cause mucopurulent cervicitis, often, neither is identified. If locating the patient may be difficult, or if the likelihood of infection is high based on sexual history or community prevalence, the patient may be treated empirically. Other causes of cervicitis, such as Tricho- monas infection or cervical dysplasia, should be ruled out. Although the role of ureaplasma and mycoplasma in the cause of cervicitis has not been well defined, these organisms are sensitive to standard chlamydia1 therapies. In general, if cervicitis persists despite antibiotic treatment for gonorrhea and chlamydia, the purulent exudate is most likely the result of nonspecific inflammation of the ectropion, and further antibiotic treatment is unlikely to be helpful.

Genital Ulcers

Genital ulcers are erosions of the skin or mucous membrane tissue. The most common causes for genital ulcers are genital herpes, syphilis, and chan- croid, although more than one sexually transmitted organism is seen in as many as 10% of patients with genital ulcers. To place these diseases in perspective, in 1997, approximately 200,000 initial visits were made for genital herpes, 50,000 reported cases of syphilis, and 300 reported cases of chancroid." The presenta- tion of these diseases may overlap. In an article regarding the evaluation of genital ulcers in male patients, the classic signs of the three diseases (i.e., multiple, shallow, tender ulcers in patients with herpes; painless, indurated ulcer in patients with syphilis; and deep, undermined purulent ulcer in patients with chancroid) were found to be specific but not sensitive.= Because chancroid is

ADOLESCENTS AND SEXUALLY TRANSh4llTED DISEASES 757

rare except in a few defined endemic areas, the discussion of genital ulcers focuses on genital herpes and syphilis.

Herpes Simplex Virus

Herpes simplex virus is the most common cause of genital ulcers. In a recent study of adolescents, 62% were seropositive for HSV type 1, and 12% were positive for HSV type 2.% A study examining the temporal trends in HSV 2 antibodies found that the seroprevalence of HSV 2 increased 30% over the previous two decades.3l This study also noted that fewer than 10% of patients with positive serology reported a history of genital herpes. Patients with a history of oral herpes are less likely to acquire genital disease but, if they acquire genital disease, are also more likely to have asymptomatic disease."

Genital infections may be classified as true primary disease (i.e., no antibod- ies to HSV 1 or 2 antibodies), nonprimary (i.e., heterologous HSV antibodies), or recurrent (i.e., homologous antibodies present). The most common cause of recurrent genital herpes is HSV 2 (66Y0, compared with 34% with HSV 1); HSV 1 has a proportionately greater likelihood of occurrence in first-episode genital infection than in recurrent genital infection (40% versus z%)."

The incubation period for genital herpes is typically 6 days, with a range from 2 to 20 days. Genital infections include local and systemic symptoms. Local symptoms include itching, dysuria, local pain, and painful inguinal adenopathy. The lesions begin as small papules or vesicles that become pustular and then ulcerate. The lesions then crust and heal. On the average, 16 to 24 lesions are present in a primary genital infection. The virus is shed from the onset of vesicles to the appearance of crusting or re-epithelialization, typically 16 to 20 days. Systemic symptoms include fever, headache, malaise, and myalgia and occur 3 or 4 days after the appearance of lesions. Decreased severity and shorter duration of illness occur in patients with nonprimary or recurrent disease.

Diagnostic approaches include culture, PCR, DFA, and EIA. Although cell culture is considered the standard, studies show that that PCR has the greatest sensitivity.@

As noted in Table 1, treatment approaches include management of clinical outbreaks and prophylaxis. Daily prophylaxis is recommended if six or more episodes occur per year. Discontinuation of prophylactic medication at 1 year is warranted to reevaluate the need for ongoing use. Interested readers should review the CDC Treatment Guidelines for HIV-infected patients."

Syphilis

Syphilis is caused by the organism Treponema pallidum. Presentations include primary syphilis, secondary syphilis, latent disease, and tertiary syphilis. Latent syphilis acquired in the preceding year is called early latent syphilis; other cases of latent syphilis are late latent syphilis or syphilis of unknown duration. Reported cases of primary and secondary syphilis have decreased steadily since 1990, with significant differences in rates of syphilis by ethnicity. In 1997, the rates for adolescents 15 to 19 years of age were 0.2 per 100,000 white, non- Hispanic males and 0.9 per 100,000 white, non-Hispanic females; 1.7 per 100,000 Hispanic males and 2.7 per 100,000 Hispanic females; and 15.2 per 100,000 black, non-Hispanic males and 31.6 per 100,000 black, non-Hispanic females. Sigruficant regional differences were found in the United States, with the highest rates in the south (6.6 per 100,000) and lowest rates in the west (1.0 per 100,000) (Centers

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for Disease Control and Prevention, Division of Sexually Transmitted Disease Prevention, Statistics and Data Management Branch, personal communication).

Primary syphilis presents typically as a single, painless, indurated ulcer with sharp, defined margins, although nonclassic ulcers may appear in one third of cases. Chancres usually appear 2 or 3 weeks after exposure but may go unnoticed because they can be small or located on the cervix. Six to eight weeks after the healing of the chancre, secondary syphilis presents, often (in 90% of cases) as a maculopapular rash that may involve the palms and soles. In addi- tion, one third of patients have lesions on the mucous membranes, and three fourths have adenopathy. Systemic symptoms in patients with secondary syphi- lis include fever, headache, malaise, and weight loss. Secondary syphilis occurs 2 to 12 weeks after exposure.

The definitive diagnosis of syphilis is established by darkfield examination or DFA tests from exudate or tissue of an ulcerative lesion. In most cases, however, the diagnosis is made through serologic testing. Two types of serologic tests can be used: (1) nontreponemal tests (e.g., VDRL and RPR) and (2) trepone- ma1 tests (e.g., fluorescent treponemal antibody absorption and microhemagglut- ination assay to T. pallidurn). Serologic tests depend on the development of antibodies and thus may be negative in early syphilis despite the presence of a chancre. In addition, false-positive nontreponemal tests can occur in various conditions (e.g., lupus). Confirmatory treponemal testing is thus performed when nontreponemal testing is positive. Posttreatment follow-up mandates serial nontreponemal titers to ensure adequate treatment. Persistence of low-level antibodies may occur, depending on the stage at which treatment is given. HIV infection or reinfection with syphilis should always be considered when nontreponemal titers fail to decrease as expected despite appropriate treatment. A discussion of diagnosing neurosyphilis or syphilis in HIV-infected patients is beyond the scope of this article.

SCREENING

Asymptomatic infection (i.e., infection without identified symptoms) is an important contributing factor to the high prevalence of STDs among adolescents. Asymptomatic infection occurs with many sexually transmitted agents (e.g., HSV, human papillomavirus, chlamydia, gonorrhea, HIV, and hepatitis B and C), creating a large reservoir of unrecognized, infected individuals who are capable of transmitting that infection.

One study has demonstrated that screening and treating asymptomatic, high-risk women can reduce the incidence of adverse sequelae (e.g., pelvic inflammatory disease) resulting from chlamydial ~ervicitis.~~ Annual screening of sexually active female adolescents for asymptomatic chlamydial infection is recommended? 65 although some physicians suggest that, because of the high incidence and prevalence of chlamydia in adolescents, screening every 6 months may be more appr~priate.'~

In considering which diagnostic test to select for chlamydial screening, the distinction between testing and screening is important. Screening tests for asymptomatic people must have a high specificity, but given a lower prevalence and pretest probability, false-positive results are still an issue. Guidelines from the CDC recommend that positive results of nonculture methods in low-preva- lence or low-risk populations should be confirmed by another method?* Diag- nostic testing of symptomatic people, with a higher prevalence and pretest probability, is accomplished using any of the best EIA, DFA, DNA probe, or

ADOLESCENTS AND SEXUALLY TRANSMI’ITED DISEASES 759

LCR or PCR techniques. Leukocyte esterase testing in female adolescents is not a useful predictor of cervicitis. LCR and PCR techniques on urine specimens may prove useful in periodic screening of asymptomatic female adolescents who do not otherwise require pelvic examinations.4’ The availability of this technique raises important issues involving the future role of the pelvic e~amination.~~, 61

Given the rate of asymptomatic gonococcal and chlamydial infection in male adolescents and the morbidity associated with these infections, especially in female adolescents, screening sexually active male adolescents is essential. Formerly believed was that female adolescents were more likely to acquire STDs from infected partners than were male adolescents; however, transmission rates between male and female adolescents have been shown to be the same. A study comparing the use of chlamydial culture and PCR gene amplification methods in 494 couples suggests that the belief about heterosexual transmission rates was a result of the lower sensitivity of culture compared with PCR.S1 Infection was documented using the PCR technique in two thirds of male sexual partners of infected female adolescents and two thirds of female partners of infected male adolescents. In addition, overall infection rates were similar when comparing PCR results (14.2% of male and 15.8% of female adolescents) but different when using culture (8.5% of male and 12.9% of female adolescents). Although screen- ing for infection simply, painlessly, and accurately is now feasible with nucleic acid amplification diagnostic tests, these techniques are costly and may not be readily available in all communities.

Screening for syphilis is recowended for all adolescents diagnosed with additional STD. In high-prevalence populations, screening should be performed annually in sexually active adolescents.

PREVENTION OF SEXUALLY TRANSMllTED DISEASES IN ADOLESCENTS

Because of their longitudinal relationships with patients and their families, pediatricians have a unique opportunity to provide information and to counsel adolescents about their developing sexuality. Whether pediatricians are taking advantage of this opportunity is unclear. As has been mentioned, physicians are recommended to take a sexual history, discuss risk prevention, and provide confidential care. The annual preventive visit provides an excellent opportunity to discuss these issues, but studies of physician behavior show that, although 84% of physicians ask about cigarette use, only 52% ask about condom use and 27% about sexual orientation.’ A 1992 study of Los Angeles public high school students evaluated adolescents’ recall of discussions with their physicians about sexual behaviors, condom use, HIV prevention, and sexual orientation.= Few adolescents recalled such discussions: 39% reported discussions with their physi- cians about how to avoid getting AIDS from sex; 37% about how to use a condom if having vaginal intercourse; 13% about how to use a condom; 15% about their own sex life; 13% about how to say no when they do not want to have sex; and 8% about whether they are attracted to boys, girls, or both. More than half believed that discussing matters of AIDS, STDs, avoiding pregnancy, and use of condoms would be helpful. Although 75% believed (or trusted?) their doctors to not tell their parents if they asked about sex in general, only 44% trusted their doctors not to tell their parents if they had an STD.

Prevention efforts can be categorized into three types: (1) primary, (2) secondary, and (3) tertiary. Primary prevention focuses on decreasing the number of new cases of STDs (i.e., decreasing incidence) by avoiding the exposure

760 GEVELBER & BIRO

and preventing the infection. Examples include condom use and hepatitis B vaccination. Secondary prevention aims to decrease the number of existing cases through early detection and treatment (i.e., decreasing prevalence), with the most common approach being screening of asymptomatic carriers. Tertiary prevention focuses on reducing the medical and psychological consequences of STDs. These categories of prevention are interrelated. Prompt evaluation and treatment of STDs (i.e., secondary prevention) can decrease the risk for pelvic inflammatory disease or transmission to a newborn (i.e., tertiary prevention) and the chance it will be spread to new partners (i.e., primary prevention).

Unlike the spread of other infectious agents, the risk for STD acquisition is largely behavioral. Therefore, in addition to considering factors of age, develop- mental level, race or ethnicity, education level, gender, and sexual orientation, health care providers should consider specific levels of sexual involvement when considering educational efforts to modify behavior.44 In a recent study, adolescents were assigned to one of five groups based on sexual experience to define the distinction between sexually active and not sexually active. "Delay- ers" were those who had never engaged in sexual intercourse and stated a less than 50% likelihood of doing so in the next year. "Anticipators" were those who had not yet engaged in sexual intercourse but who reported at least a 50% likelihood of doing so in the next year. "One-timers" were those who reported they had sexual intercourse only once. "Steadies" were those who had only one partner but had engaged in intercourse multiple times. "Multiples" were those who had more than one sexual partner and had engaged in intercourse multiple times. Although messages reinforcing the decision to postpone sexual involve- ment may be appropriate for delayers, anticipators may need specific informa- tion and skills to more safely negotiate a sexual relationship. One-timers, who may not anticipate further sexual intercourse, may benefit from messages rein- forcing abstinence. Steadies, involved in what they feel is a safe, monogamous relationship, may choose not to use condoms. Preventive counseling messages should be directed to the specific experience of individual adolescents.

Primary prevention stresses increasing knowledge and skills that adoles- cents need to avoid exposure. Just as adolescents who begin to smoke are aware that smoking causes cancer, awareness or knowledge of the existence of STDs is not sufficient to prevent STDS.~~ Depending on the needs of the adolescent, behavioral interventions may focus on abstaining from sex, delaying initiation of sexual intercourse, reducing the number of sex partners, participating in noncoital sexual activities, and using condoms consistently and correctly. Older teens may have misperceptions regarding peers' behaviors and attitudes. Inter- ventions may aim at correcting misperceptions and at developing the social skills necessary to negotiate sexual situations (e.g., use of condoms) with a partner.

Interventional programs have been shown to be effective. An evaluation of a school-based condom availability program that provided unrestricted access to condoms showed improved condom use among male adolescents and a strong effect on students' intentions to use condoms and male adolescents' use at first vaginal intercourse but no increase in sexual activity among students.% A randomized, controlled trial of abstinence and of safer-sex interventions showed that both methods reduced HIV risk-associated behaviors but that safer- sex interventions may be more effective with sexually experienced adolescents and may have longer effects.38

One important primary STD prevention strategy that should be mentioned is hepatitis B vaccination. All young men and women should receive this vaccine before completing adolescence.

Secondary prevention, limiting the prevalence of STDs, can be implemented

ADOLESCENTS AND SEXUALLY TRANSMITTED DISEASES 761

through improving access to medical care, using appropriate medical manage- ment (including adherence with medication), and encouraging partner notifica- tion to prevent reinfection and transmission to others. Beyond screening and treatment of STDs, clinicians can impact on STD transmission and reinfection through counseling about sexual decision making; identlfying barriers to behav- ioral change; and encouraging less-risky behaviors, such as abstinence or partner number reduction. To prevent future infections, clinicians can educate teens about asymptomatic infection, signs of infection, and need for annual screening. Physician involvement in the notification of partners of adolescents diagnosed with STDs can range from encouraging patients to tell their partners and giving reminder cards with the diagnosis, to referral of cases to a local or state health department

Although discussing the choice of abstinence and safer, nonpenetrative sexual behaviors is important, after adolescents have chosen to be sexually active, consistent and correct condom use may be the best protection from STDs. Pediatricians can play an important role in supporting and encouraging the consistent use of condoms by sexually active adolescents? In one study, adoles- cents who had discussed AIDS with their physicians were 1.7 times more likely to use condoms, and adolescents who carried condoms were 2.7 times more likely to use condoms.” Trends regarding adolescent condom use are shown in Table 2. Preventive efforts aimed at changing behavior must increase condom use self-efficacy and develop skills to communicate with partners about STD prevention issues before intercourse.63

In counseling teens about risk reduction, the determinants of condom use must be understood. A study of high-risk female adolescents showed that those who had been sexually active for a longer time more often viewed intercourse with condoms as not enjoyable and perceived their partners as viewing inter- course with condoms as not enjoyable. Longer relationships before sex were associated with having condoms available and partner insistence on condom ~ s e . 5 ~ In a sample of 266 sexually active adolescents, consistent condom users (compared with inconsistent users) had greater intentions to use condoms in the future, were more likely to believe that their friends used condoms, believed that latex condoms were protective against HIV, and were less likely to have a history of drug use. Knowledge or fear of HIV was not significantly different among consistent and inconsistent users of condoms.13 A study of 403 junior high school students in an inner-city school district in California showed that perceived costs associated with condom use, the belief that condoms are pre- venting AIDS, and fewer than three sex partners were most predictive of consis- tent condom ~ s e . 2 ~ ”Costs” associated with condom use included decreased

Table 2. PERCENTAGE OF SEXUALLY ACTIVE HIGH SCHOOL STUDENTS USING CONDOMS AT LAST INTERCOURSE

Demographic 1991 1993 1995 1997

Female 38.0 46.0 48.6 50.8 Male 54.6 59.2 60.5 62.5 White 46.6 52.3 52.5 55.8 African American 48.0 56.5 66.1 64.0 Hispanic 37.6 46.1 44.4 48.3 Average 46.2 52.8 54.4 56.8

Datafrom Centers for Disease Control and Prevention: Trends in sexual risk behaviors among high school students-United States, 1991-1997. MMWR Morb Mortal Wkly Rep 47749-752,1998.

762 GEVELBER 81 BIRO

enjoyment and spontaneity, purchasing the condoms, and negotiating with one's partner. An analysis of the 1991 National Survey of Adolescent Males revealed that condom use was most likely at the beginning of a relationship but declined as the relationship c0ntinued.3~ Condom use during the first episode of inter- course with their most recent partners decreased with age (59% of 17 to 18-year- olds, 56% of 19 to 20-year-olds, and 46% of 21 to 22-year-olds).

Results of a study of the intentions to use condoms revealed that male adolescents who were not sexually active were responsive to information about condoms obtained from peers, teachers, and health care providers in the school setting. Younger adolescents (< 15 y) and those involved in less-committed relationships were more likely to intend to use condoms.% A similar study revealed that the intentions of sexually active male adolescents were most affected by having a favorable attitude toward personal contraceptive responsi- bility in sexual relations.& Teens with partners using contraceptive pills had less intention to use condoms. These male adolescents were not found to be receptive to information about condoms from any source (i.e., parents, peers, school, or the media). Among younger sexually active male adolescents, the intention to use condoms was associated with supportive parental attitudes on sexuality and contraception.

Using data from the 1988 National Survey of Adolescent Males, the intent to use condoms by sexually experienced and inexperienced male adolescents was largely influenced by the belief that male adolescents are responsible for contraception and the perception that the use of condoms has a low cost in terms of reduction in pleasure and a high benefit in gaining the partner's appreciation.% Male adolescents' attitudes toward responsibility in contraception (including asking the partner whether she is using contraception, responsibility for a child, responsibility of the male adolescent to help the female partner pay for contraceptive pills if she is using them, and responsibility to discuss contraception) were important in determining intended condom use.

Although condoms may be the best protection available, they are not per- fect. A study of men aged 17 to 22 years in the National Survey of Adolescent Males showed that 23% of those using condoms reported at least one condom break during the previous year, and, of all condoms used, 2.5% broke?' Increased experience with, and knowledge about, condom use reduced the risk for break- age. Men who had ever had (or with partners who had ever had) STDs were twice as likely as others to have reported a broken condom. This finding suggests that counseling and training on the correct use of condoms is important. Talking to teens about condoms is discussed in the box on page 763.

SUMMARY

Pediatricians with busy practices have limited time to spend with each patient. But because much of adolescent morbidity and mortality is related to behavioral issues, time and energy are crucial to providing effective counseling and care to adolescents. Many barriers to provision of services to adolescents exist, including time, space, d&or, office hours, office fees, and support person- nel."

Despite these barriers to care of adolescents and, in particular, sexually active adolescents, the need for pediatricians to provide these services is clear. Services include anticipatory guidance and counseling about developing sexual- ity and sexual behaviors, as well as management of health consequences of sexual behavior.

764 GEVELBER & BIRO

Primary care providers have an opportunity to assist adolescents to develop mature and healthy sexual relationships. This necessitates a full understanding of each patient’s unique situation, listening to adolescents’ concerns, and honest and straightforward discussion of sensitive information. Beginning the process of discussion of sexuality and relationships early in the pediatric years may help adolescents and their parents to develop healthy sexual attitudes and behaviors.

References

1. Abma J, Chandra A, Mosher W, et a1 Fertility, family planning, and women’s health: New data from the 1995 National Survey of Family Growth. Vital Health Stat

2. American Academy of Pediatrics, Committee on Adolescence: Condom availability for youth. Pediatrics 95:281-285, 1995

3. American Medical Association: Guidelines for Adolescent Preventative Services. Chi- cago, Department of Adolescent Health, American Medical Association, 1992

4. Biglan A, Metzler C, Wirt R, et al: Social and behavioral factors associated with high- risk sexual behavior among adolescents. J Behav Med 13245261,1990

5. Biro F, Reising S, Doughman J, et al: A comparison of diagnostic methods in adolescent girls with and without symptoms of chlamydial urogenital infection. Pediatrics 93476, 1994

6. Biro F, Rosenthal S, Kiniyalocts M: Gonococcal and chlamydial genitourinary infections in symptomatic and asymptomatic adolescent women. Clin Pediatr 34:419, 1995

7. Biro F, Rosenthal S, Stanberry L Knowledge of gonorrhea in adolescent females with a history of STD. Clin Pediatr 33601-605, 1994

8. Biro F, Rosenthal S Adolescents and sexually transmitted diseases: Diagnosis, develop- mental issues, and prevention. J Pediatr Health Care 9256262,1995

9. Biro F Adolescents and Sexually Transmitted Diseases. Maternal and Child Health Technical Information Bulletin. Washington, DC; National Center for Education in Maternal and Child Health in cooperation with the Maternal and Child Health Bureau, Health Resources and Services Administration, Public Health Service, US Department of Health and Human Services, 1992

10. Black C: Current methods of laboratorv diamosis of Chlumvdiu truchomutis infections.

231-114, 1997

11.

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, ” Clin Microbiol Rev 1016@-184, 1997 Braverman P, Strasburger V: Office-based adolescent health care: Issues and solutions. Adolescent Medicine: State-of-the-Art Reviews 81-14, 1997 Brookman R Sexually transmitted diseases. In Levine MD, McAnamey ER (eds): Early Adolescent Transitions. Indianapolis, IN, Lexington Books /DC Heath, 1990, pp 149-165 Brown LK, DiClemente RJ, Park T: Predictors of condom use in sexually active adolescents. J Adolesc Health 13:651-657, 1992 Burstein G, Gaydos C, Diener-West M, et al: Incident Chlamydia truchomutis infections among inner-city adolescent females. JAMA. 280521-526, 1998 Cavanaugh R, Hastings-Tolsma M, Keenan D, et al: Anticipatory guidance for the adolescent parents’ Concerns. Clin Pediatr 32542-545, 1993 Centers for Disease Control and Prevention, Division of STD/HIV Prevention: Sexually Transmitted Disease Surveillance, 1994. Atlanta, Centers for Disease Control and Pre- vention, 1995 Centers for Disease Control and Prevention: Recommendations for the prevention and management of Chlumvdiu truchomutis infections, 1993. MMWR Morb Mortal Wklv Rev , - 42:1-%, 1993 Centers for Disease Control and Prevention: Trends in sexual risk behaviors amone: high school students-United States, 1991-1997. MMWR Morb Mortal Wkly Re;

Centers for Disease Control and Prevention: HIV prevention through early detection and treatment of other sexually transmitted diseases-United States. MMWR Morb Mortal Wkly Rep 47:l-24, 1997 Centers for Disease Control and Prevention: Ten leading nationally notifiable infectious diseases-United States, 1995. MMWR Morb Mortal Wkly Rep 45883-884,1996

47749-752, 1998

764 GEVELBER & BIRO

Primary care providers have an opportunity to assist adolescents to develop mature and healthy sexual relationships. This necessitates a full understanding of each patient’s unique situation, listening to adolescents’ concerns, and honest and straightforward discussion of sensitive information. Beginning the process of discussion of sexuality and relationships early in the pediatric years may help adolescents and their parents to develop healthy sexual attitudes and behaviors.

References

1. Abma J, Chandra A, Mosher W, et a1 Fertility, family planning, and women’s health: New data from the 1995 National Survey of Family Growth. Vital Health Stat

2. American Academy of Pediatrics, Committee on Adolescence: Condom availability for youth. Pediatrics 95:281-285, 1995

3. American Medical Association: Guidelines for Adolescent Preventative Services. Chi- cago, Department of Adolescent Health, American Medical Association, 1992

4. Biglan A, Metzler C, Wirt R, et al: Social and behavioral factors associated with high- risk sexual behavior among adolescents. J Behav Med 13245261,1990

5. Biro F, Reising S, Doughman J, et al: A comparison of diagnostic methods in adolescent girls with and without symptoms of chlamydial urogenital infection. Pediatrics 93476, 1994

6. Biro F, Rosenthal S, Kiniyalocts M: Gonococcal and chlamydial genitourinary infections in symptomatic and asymptomatic adolescent women. Clin Pediatr 34:419, 1995

7. Biro F, Rosenthal S, Stanberry L Knowledge of gonorrhea in adolescent females with a history of STD. Clin Pediatr 33601-605, 1994

8. Biro F, Rosenthal S Adolescents and sexually transmitted diseases: Diagnosis, develop- mental issues, and prevention. J Pediatr Health Care 9256262,1995

9. Biro F Adolescents and Sexually Transmitted Diseases. Maternal and Child Health Technical Information Bulletin. Washington, DC; National Center for Education in Maternal and Child Health in cooperation with the Maternal and Child Health Bureau, Health Resources and Services Administration, Public Health Service, US Department of Health and Human Services, 1992

10. Black C: Current methods of laboratorv diamosis of Chlumvdiu truchomutis infections.

231-114, 1997

11.

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14.

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, ” Clin Microbiol Rev 1016@-184, 1997 Braverman P, Strasburger V: Office-based adolescent health care: Issues and solutions. Adolescent Medicine: State-of-the-Art Reviews 81-14, 1997 Brookman R Sexually transmitted diseases. In Levine MD, McAnamey ER (eds): Early Adolescent Transitions. Indianapolis, IN, Lexington Books /DC Heath, 1990, pp 149-165 Brown LK, DiClemente RJ, Park T: Predictors of condom use in sexually active adolescents. J Adolesc Health 13:651-657, 1992 Burstein G, Gaydos C, Diener-West M, et al: Incident Chlamydia truchomutis infections among inner-city adolescent females. JAMA. 280521-526, 1998 Cavanaugh R, Hastings-Tolsma M, Keenan D, et al: Anticipatory guidance for the adolescent parents’ Concerns. Clin Pediatr 32542-545, 1993 Centers for Disease Control and Prevention, Division of STD/HIV Prevention: Sexually Transmitted Disease Surveillance, 1994. Atlanta, Centers for Disease Control and Pre- vention, 1995 Centers for Disease Control and Prevention: Recommendations for the prevention and management of Chlumvdiu truchomutis infections, 1993. MMWR Morb Mortal Wklv Rev , - 42:1-%, 1993 Centers for Disease Control and Prevention: Trends in sexual risk behaviors amone: high school students-United States, 1991-1997. MMWR Morb Mortal Wkly Re;

Centers for Disease Control and Prevention: HIV prevention through early detection and treatment of other sexually transmitted diseases-United States. MMWR Morb Mortal Wkly Rep 47:l-24, 1997 Centers for Disease Control and Prevention: Ten leading nationally notifiable infectious diseases-United States, 1995. MMWR Morb Mortal Wkly Rep 45883-884,1996

47749-752, 1998

ADOLESCENTS AND SEXUALLY TRANSMITTED DISEASES 765

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26. Clark L, Brasseux C, Richmond D, et al: Are adolescents accurate in self-report of frequencies of sexually transmitted diseases and pregnancies? J Adolesc Health

27. DiClemente R, Durbin M, Siege1 D, et a1 Determinants of condom use among junior high school students in a minority, inner-city school district. Pediatrics 89:197-202,1992

28. DiCarlo RP, Martin DH. The clinical diagnosis of genital ulcer disease in men. Clin Infect Dis 25:292-298, 1997

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Address reprinf requests to Frank M. Biro, MD

Division of Adolescent Medicine Children’s Hospital Medical Center

3333 Burnet Avenue Cincinnati, OH 45229

96:52-58,1995

55177-183, 1998