American Journal of Epidemiology Copyright © 1992 by The Johns Hopkins University School of Hygiene and Public Health All rights reserved
Vol 136, No. 6 Printed in U. S.A.
Comparative Behavioral Epidemiology of Gonococcal and Chlamydial Infections among Patients Attending a Baltimore, Maryland, Sexually Transmitted Disease Clinic
Edward W. Hook III, 12 Cindy A. Reichart,1 Dawn M. Upchurch,3 Phyllis Ray,2 David Celentano,3 and Thomas C. Quinn14
Between April 1988 and May 1989,400 males and 400 females attending a Baltimore, Maryland, sexually transmitted disease clinic were enrolled in a study evaluating and comparing behaviors associated with culture-proven gonococcal or chlamydial infection. The subjects were enrolled consecutively, and were all seen by the same clinician. Among participants of each sex, gonorrhea but not chlamydia was associated with increasing numbers of recent (the past 30 days) sexual partners. Compared with males with neither infection, factors independently associated with increased risk of gonorrhea included age less than 20 years (odds ratio (OR) = 1.93), the presence of genitourinary symptoms (OR = 8.07), and recent exposure to a new sexual partner (OR = 2.78); risk for chlamydial infection in males was associated with genitourinary symptoms (OR = 2.83) and was significantly reduced in those reporting multiple recent (OR = 0.19) or new (OR = 0.07) sexual partners. Among females, age less than 20 years was independently associated with gonococcal (OR = 1.86) and chlamydial (OR = 7.79) infections in comparison with females with neither infection. No other behavioral factors were associated with chlamydial infection for females in this study; however, having a regular sexual partner was associated with significantly elevated risk of gonorrhea (OR = 3.85), while the presence of genital tract symptoms was associated with diminished risk (OR = 0.29) for gonorrhea. These data suggest that there are differences in the behaviors associated with gonorrheal and chlamydial infections and that different strategies may be useful in efforts to control these infections. Am J Epidemiol 1992;136:662-72. chlamydia; gonorrhea; sex behavior; sexually transmitted diseases, bacterial
Infections due to Neisseria gonorrhoeae and Chlamydia trachomatis are the two most common bacterial sexually transmitted diseases in the United States. Over four million new infections occur each year, and complications of these infections lead to ma-
jor long-term morbidity, including infertility and ectopic pregnancy (1, 2). In general, consideration of these two pathogens has emphasized their parallel clinical spectrums, frequent coexistence, and similar routes of transmission (3, 4). Nonetheless, there are
Received for publication November 29, 1991, and in final form April 30, 1992 Abbreviations. Cl, confidence interval; OR, odds ratio. 1 School of Medicine, The Johns Hopkins University, Baltimore, MD. 2 Baltimore City Health Department, Baltimore, MD. 3 School of Hygiene and Public Health, The Johns Hopkins University, Baltimore, MD. 4 National Institute of Allergy and Infectious Diseases, Bethesda, MD. Reprint requests to Dr. Edward W. Hook III, Division of Infectious Diseases, Department of Medicine, School of Medicine, The University of Alabama at Birmingham, 229
Tmsley Harrison Tower, 1900 University Boulevard, UAB Station, Birmingham, AL 35294-0006 These data were presented in part at the Seventh International Symposium on Human Chlamydial Infections, Harrison Hot Springs, British Columbia, Canada, June 2429, 1990. This work was supported by grant Al-16959 from the National Institute of Allergy and Infectious Diseases. The authors thank Mary Shepherd for her helpful comments and statistical assistance, Koren Waters for manuscript preparation, and Theresa Neuman, Laura Welsh, and Graciella Jaschek for microbiologic technical support
662
Behavioral Epidemiology of Gonorrhea and Chlamydia
also important differences between these pathogens and the diseases they cause. Gonorrhea is more often clinically apparent, and its signs and symptoms tend to be more overt (4-6). The incubation period for symptomatic gonorrhea is briefer than that for chlamydia. Gonococcal infections are disproportionately concentrated in lower socioeconomic status populations and minorities, while chlamydial infections are more common in the young, in women using oral contraceptives, and in persons of higher socioeconomic status (6). In addition, in many localities, gonorrhea, but not chlamydia, is the target of publicly funded control efforts which often include free screening for infection and notification of exposed partners ("contacts") by health department specialists. The purpose of this study was to examine differences in the epidemiology of these two infections, focusing on clinical presentations and behavioral factors associated with culture-proven N. gonorrhoeae and C. trachomatis infections among patients at a Baltimore, Maryland, sexually transmitted disease clinic. Elucidation of such differences might prove helpful in designing control strategies for these infections.
MATERIALS AND METHODS Study population
From April 1988 to May 1989, patients attending the Eastern Health District sexually transmitted disease clinic of the Baltimore City Health Department and being seen by a single clinician were invited to participate in the study. Consecutive series of 400 men and 400 women attending the clinic for reasons other than follow-up or testing for cure evaluations were eligible for enrollment; only three persons approached regarding study participation declined to do so. All subjects gave written informed consent for study enrollment using a consent form approved by the Joint Committee on Clinical Investigation of the Johns Hopkins University School of Medicine.
663
Clinical evaluation and specimen collection
Patients were interviewed using a standardized data collection form which included specific questions regarding sexual practices, prior sexually transmitted diseases, the nature of relationships with recent sexual partners, and selected demographic characteristics. As part of the questionnaire, a detailed sexual history was obtained, emphasizing sexual experiences which occurred in the 30 days prior to the clinic visit. In addition to numbers of sex partners, we elicited information describing the types of recent sexual relationships in which patients were involved. Participants were asked to classify their sex partners over the preceding 30 days into one of three mutually exclusive groups previously found to be useful for describing interpersonal contexts associated with the likelihood of gonococcal infection and condom use in this population (7, 8). In this classification, a partner with whom the patient had had sex for the first time during the 30 days preceding study enrollment was defined as a "new" partner. For sexual relationships of greater than 1 month's duration, relationships were defined by the interviewer as follows. A "regular" partner was defined as a person with whom the patient had been sexually active "often," similar to a "boyfriend" or "girlfriend." In contrast, a "casual" partner was one with whom the patient reported having sex on a more occasional basis for more than 1 month. These relationships appeared somewhat less serious, and partners were often described by patients as being "friends." Following completion of the questionnaire, a directed physical examination was performed. In men, two urethral specimens were collected using wire-shaft, Dacrontipped swabs. The first swab was used for preparation of a Gram stain specimen and for inoculation of culture medium for N. gonorrhoeae; the second swab was passed at least 1 cm beyond the first and was placed into transport medium for inoculation of cultures for C. trachomatis. In women, specimens were collected during a speculum ex-
664
Hook et al.
amination as follows. Following removal of adherent cervico-vaginal secretions with large cotton-tipped swabs, an endocervical sample was collected for preparation of a Gram stain and inoculation of modified Thayer-Martin medium for gonorrhea culture. A second endocervical swab was collected and was used to inoculate transport medium for C. tmchomatis culture. Microbiologic culture methods
N. gonorrhoeae. Specimens for gonorrhea culture were inoculated directly onto modified Thayer-Martin medium and were incubated for 24-48 hours in a 5 percent carbon dioxide atmosphere. Presumptive N. gonorrhoeae was identified on the basis of colonial morphology, Gram stain, and oxidase test; the identity of presumptive N. gonorrhoeae was confirmed using fluorescein-conjugated monoclonal antibodies (9) (Syva Corporation, Palo Alto, California). C. trachomatis. Chlamydia cultures were obtained using sterile Dacron-tipped swabs, placed in transport medium, and stored at 4°C until they could be frozen at -70°C (424 hours). Within 4 days of acquisition, specimens were thawed and 400/il of transport medium was inoculated into four microtiter plate wells for culture on McCoy cell monolayers as described previously (10). Following 48-72 hours of incubation, duplicate wells were evaluated using fluoresceinconjugated antichlamydial monoclonal antibodies to C. trachomatis (Syva Corporation) to detect positive cultures. Cultures which were negative at 48-72 hours were passed for blind subculture and reevaluated again 48-72 hours later. Cultures that were still negative following blind subculture were classified as negative. Statistical analysis. The data were analyzed using SAS software (11). Patients with positive cultures for both N. gonorrhoeae and C. trachomatis were excluded from the analysis. We used the chi-squared test to test for bivariate associations. In the multivariate analyses, a logistic transformation was used.
First, patients with gonorrhea were compared with patients with neither gonorrhea nor chlamydia infection. Second, cases with chlamydia infection were compared with the same group. In this way, adjusted odds ratios were computed, comparing the relative odds of disease for those with the characteristic of interest (e.g., gonorrhea or chlamydia) to those without that characteristic. Finally, in a third multivariate logistic regression analysis, characteristics distinguishing the two infections were compared. RESULTS Patient characteristics and prevalence of infection
Eight hundred consecutive patients (400 males and 400 females) attending the sexually transmitted disease clinic for reasons other than follow-up evaluation were enrolled in the study. Specimens from eight patients (six males and two females) were toxic to the cell cultures used for chlamydia detection. Because no chlamydia culture data were available, these participants were excluded from the analyses. The remaining 394 males and 398 females comprise the subjects of this report (table 1). The area served by the clinic is comprised of primarily lower income, nonwhite census tracts of the city. Those characteristics are reflected in the demographic distribution of the participants, who were predominately young, single, black residents of inner-city Baltimore. Seventy-five percent of the participants gave a history of a prior sexually transmitted disease; 45 percent of males and 31 percent of females reported previous episodes of gonorrhea. Since patients tended to be unfamiliar with C. trachomatis as a sexually transmitted disease pathogen, a history of prior chlamydial infection was not sought. The prevalences of gonorrheal and chlamydial infection at the time of study enrollment were 29 percent and 10 percent, respectively, for males and 23 percent and 14 percent, respectively, for females. Eleven (2.8 percent) males and 22 (5.5 percent)
Behavioral Epidemiology of Gonorrhea and Chlamydia
665
females had coexistent gonococcal and chlamydial infections. Patients with coexistent gonorrhea and chlamydia were too few to permit separate analysis and could not be included with patients who had gonorrhea only, chlamydia only, or neither infection; therefore, they were excluded from further analyses.
to a nadir of 15 percent in the 25- to 29-year age group, and increased again to 24 percent among males aged 30 years or more (table 2). The prevalence of C. trachomatis in males did not vary with age, although a greater percentage of adolescents and males aged 20-24 years were infected than males aged 25 years or more. In females, the prevalence of both infections was greatest in adolescents and declined steadily with age. The reasons for attending the clinic differed between males and females. Two thirds (255 of 383) of males attended the clinic for symptom evaluation, 15 percent attended following notification of exposure to an infected person, and 19 percent attended for other reasons, such as screening. In contrast, 45 percent of females attended the clinic for symptom evaluation, 23 percent attended as contacts of infected persons, and 31 percent visited the clinic for other services, including screening, pregnancy testing, and contraceptive evaluation. Disease prevalence also varied when participants were stratified by sex and reason for visit (table 2). Among males, gonorrhea was present in 37 percent of symptomatic patients, 11 percent of sexual contacts, and 3 percent of males attending for other reasons. Less variation in chlamydia prevalence was observed among males when they were stratified by reason for visit: 9 percent of males seen for symptom evaluation had positive chlamydia cultures, as did 11 percent of sexual contacts. In females, as in males, gonorrhea prevalence but not chlamydia prevalence varied with reason for clinic attendance (table 2). Gonorrhea and chlamydia rates were 9 percent and 8 percent, respectively, in females attending for symptom evaluation, 40 percent and 11 percent in females who were recent contacts of an infected person, and 15 percent and 9 percent in females attending for other reasons.
Relation of age and reason for visit to gonococcal and chlamydial infection
Relation of numbers and types of sexual partners to gonorrhea and chlamydia prevalence
In males, gonorrhea prevalence was greatest (38 percent) among adolescents, declined
Males attending the clinic tended to report more sexual partners during their lifetime
TABLE 1. Demographic characteristics and disease prevalence in 792 persons attending an inner-city sexually transmitted disease clinic in Baltimore, Maryland, 1988-1989 Characteristic
Men (n = 394)
Women (n = 398)
No.
%
No.
%
Age (years) 30
74 129 83 108
19 33 21 27
153 104 70 71
38 26 18 18
Race Black Other
387 7
98 2
378 20
95 5
Marital status Single or divorced Married
369 25
94 6
379 19
95 5
Education (years) 12
142 195 57
36 50 15
191 160 47
48 40 12
Currently in school
72
18
144
36
Currently employed
270
69
182
46
History of prior sexually transmitted disease
300
76
294
74
History of gonorrhea
179
45
125
31
Culture results Culture positive for N. gonorrhoeae Culture positive for C. trachomatis
133
29
90
23
40
10
56
14
666
Hook et al.
TABLE 2. Prevalence of gonorrhea and chlamydia among persons attending an inner-city sexually transmitted disease clinic, by selected demographic and clinical characteristics*: Baltimore, Maryland, 1988-1989 Females (n = 376)
Males (n = 383)
%
Characteristic
%
No.
No. Gonorrhea
Chlamydia
Neither
Gonorrhea
Chlamydia
Neither
142 98 67 69
22
19 5 3
59 76 82 88
Age (years) 30
71 124 80 108
38 30 15 24
8 12
5
54 58 81 71
Education (years) 12
136 192 55
33 27 11
4 10 9
63 64 80
177 152 47
19 16 19
13 5 6
68 78 74
255
37
9
54
169
9
8
82
57 71
11
11
79 97
88 117
40 15
11 9
49 77
History of gonorrhea
176
31
7
62
118
17
6
77
Age (years) at first sexual intercourse 18
72 145 131 34
28 30 24 18
6 8 8 9
67 63 67 74
16 136 174 48
25 15 21 15
19 12 6 6
56 74 72 79
Reason for visit Symptoms Contact with someone with a sexually transmitted disease Other
4
3
19 15 12
* Excludes 33 participants (11 males and 22 females) who were infected with both pathogens.
and in the preceding year than females (table 3). Median numbers of sexual partners, lifetime and in the past year, were 20 and 4, respectively, for males and 5 and 2, respectively, for females. In the 30 days preceding clinic attendance, the median number of sexual partners for both sexes was one; 42 percent of males and 15 percent of females reported having had two or more sexual partners. For males, gonorrhea was not associated with number of lifetime sexual partners. However, when stratified by number of partners in the preceding year or the preceding 30 days, significant associations were noted (table 3). For chlamydia infection, no association between numbers of sexual partners and the likelihood of infection could be discerned for male participants, irrespective of the time frame used. For females, there was a tendency to be
culture-positive for N. gonorrhoeae with greater numbers of sexual partners, although for each time frame, those reporting the most sexual partners were somewhat less likely to have gonorrhea than females in other categories. The prevalence of C. trachomalis infection did not increase with increasing numbers of sexual partners over any of the time intervals studied. Rather, the highest prevalence of C. trachomatis infection occurred in females reporting fewer partners in their lifetime or in the past 30 days and in females with more than one but less than four partners in the past year. To address the possibility that the nature of patients' relationships with their recent sexual partners might be associated with risk for gonorrhea or chlamydia, we stratified participants hierarchically by sex and by their self-reported relationship to their sex-
Behavioral Epidemiology of Gonorrhea and Chlamydia
667
TABLE 3. Isolation of gonococcus and chlamydia in sexually transmitted disease clinic patients, by numbers of sex partners over a lifetime, the past year, and the preceding 30 days: Baltimore, Maryland, 1988-1989 Females (n = 376)
Males (n = 383) No. of partners
%
%
No
Lifetime* 30 Past year 0-1 2-4 5-9 210
Past 30 days 0 1 2 >3
No. Gonorrhea
Chlamydia
Gonorrhea
Chlamydia
77 92 69
25 26 22
141
31
9 3 10 9
263 70 18
14 29 33
11 3 1
24
17
4
50 179 83 71
14 26 34
16 6 6 7
142 198 26 10
12 21 27 20
12 12 10
18 205
11 21
9
38 281
5 18 33
13 10 2
29
109
34
7
49
51
39
4
8
5
• Data were missing for four males and one female with gonorrhea.
ual partners in the 30 days preceding clinic attendance (table 4). For males, gonococcal infection was most common in those reporting sex with a new partner, was less common in those reporting casual partners, and was lowest in males reporting sex only with regular partners. In contrast, for chlamydia infections, the association with type of partner was reversed. Chlamydia was most common in males reporting only regular sexual partners, intermediate in those who reported casual partners, and lowest (2 percent) in men who reported having had new sexual partners in the preceding 30 days. In females, although there was no clear relation between types of recent sexual part-
ners and gonorrhea prevalence, chlamydia was again most common in females reporting sex only with regular partners (10 percent), compared with 3 percent in females with casual partners and 4 percent in females reporting new partners (table 4). Multivariate analysis of risk factors associated with N. gonorrhoeae and C. trachomatis infection
To further evaluate the relative import of variables found to be associated with gonorrhea or chlamydia infections, we performed multivariate logistic regression analyses (table 5). To determine which factors were independently associated with likeli-
TABLE 4. Isolation of gonococcus and chlamydia in sexually transmitted disease clinic patients, by type of most recent sexual relationship*: Baltimore, Maryland, 1988-1989
Gonorrhea
Chlamydia
Total no.
No.
%
No.
%
171 82 112
24 26 50
14 32 45
22 5 2
CO CM
Regular Casual New
Females (n == 338)
Males (n = 365)
CO
Type of partner in the past 30
Gonorrhea
Chlamydia
Total no.
No.
%
No.
%
275 37 26
53 9 4
19 24 15
28 1 1
10 3 4
* Patients with no sexual partners in the preceding 30 days were excluded. Hierarchical classification: any new partner > any causal partner > regular partner(s) only.
668
Hook et al.
TABLE 5. Adjusted odds ratios for gonorrheal or chlamydial infection in persons attending an inner-city sexually transmitted disease clinic, Baltimore, Maryland, 1988-1989 Males Factor
Gonorrhea OR*
Age 1 partner in the past 30 days Regular partner Casual partner New partner Casual/new partner
95% Clt
Females Chlamydia
OR
95% Cl
1.93 1.02-3.64* 1.40 0.52-3.77 8.07 3.71-17.57*** 2.83 1.09-7.30* 0.97 1.01 1.86 2.78
0.45-2.17 0.50-2.06 0.83-4.16 1.64-6.07*
2.85 1.04 0.19 0.07
Chlamydia
Gonorrhea
OR
95% Cl
1.86 1.05-3.27* 0.29 0.16-0.54***
2.33 0.63-8.69 0.91-8.94f 0.31-3.47 3.85 1.27-11.73* 0.05-0.77* 0.01-0.39*** 0.76 0.18-1.56
OR
95% Cl
7.79 3.28-18.47*** 0.91 0.43-1.91 0.49 0.06-4.18 0.93 0.31-2.72
0.47 0.05-4.16
• p < 0.05; *• p < 0.01; *•* p < 0.001. tp
Vol 136, No. 6 Printed in U. S.A.
Comparative Behavioral Epidemiology of Gonococcal and Chlamydial Infections among Patients Attending a Baltimore, Maryland, Sexually Transmitted Disease Clinic
Edward W. Hook III, 12 Cindy A. Reichart,1 Dawn M. Upchurch,3 Phyllis Ray,2 David Celentano,3 and Thomas C. Quinn14
Between April 1988 and May 1989,400 males and 400 females attending a Baltimore, Maryland, sexually transmitted disease clinic were enrolled in a study evaluating and comparing behaviors associated with culture-proven gonococcal or chlamydial infection. The subjects were enrolled consecutively, and were all seen by the same clinician. Among participants of each sex, gonorrhea but not chlamydia was associated with increasing numbers of recent (the past 30 days) sexual partners. Compared with males with neither infection, factors independently associated with increased risk of gonorrhea included age less than 20 years (odds ratio (OR) = 1.93), the presence of genitourinary symptoms (OR = 8.07), and recent exposure to a new sexual partner (OR = 2.78); risk for chlamydial infection in males was associated with genitourinary symptoms (OR = 2.83) and was significantly reduced in those reporting multiple recent (OR = 0.19) or new (OR = 0.07) sexual partners. Among females, age less than 20 years was independently associated with gonococcal (OR = 1.86) and chlamydial (OR = 7.79) infections in comparison with females with neither infection. No other behavioral factors were associated with chlamydial infection for females in this study; however, having a regular sexual partner was associated with significantly elevated risk of gonorrhea (OR = 3.85), while the presence of genital tract symptoms was associated with diminished risk (OR = 0.29) for gonorrhea. These data suggest that there are differences in the behaviors associated with gonorrheal and chlamydial infections and that different strategies may be useful in efforts to control these infections. Am J Epidemiol 1992;136:662-72. chlamydia; gonorrhea; sex behavior; sexually transmitted diseases, bacterial
Infections due to Neisseria gonorrhoeae and Chlamydia trachomatis are the two most common bacterial sexually transmitted diseases in the United States. Over four million new infections occur each year, and complications of these infections lead to ma-
jor long-term morbidity, including infertility and ectopic pregnancy (1, 2). In general, consideration of these two pathogens has emphasized their parallel clinical spectrums, frequent coexistence, and similar routes of transmission (3, 4). Nonetheless, there are
Received for publication November 29, 1991, and in final form April 30, 1992 Abbreviations. Cl, confidence interval; OR, odds ratio. 1 School of Medicine, The Johns Hopkins University, Baltimore, MD. 2 Baltimore City Health Department, Baltimore, MD. 3 School of Hygiene and Public Health, The Johns Hopkins University, Baltimore, MD. 4 National Institute of Allergy and Infectious Diseases, Bethesda, MD. Reprint requests to Dr. Edward W. Hook III, Division of Infectious Diseases, Department of Medicine, School of Medicine, The University of Alabama at Birmingham, 229
Tmsley Harrison Tower, 1900 University Boulevard, UAB Station, Birmingham, AL 35294-0006 These data were presented in part at the Seventh International Symposium on Human Chlamydial Infections, Harrison Hot Springs, British Columbia, Canada, June 2429, 1990. This work was supported by grant Al-16959 from the National Institute of Allergy and Infectious Diseases. The authors thank Mary Shepherd for her helpful comments and statistical assistance, Koren Waters for manuscript preparation, and Theresa Neuman, Laura Welsh, and Graciella Jaschek for microbiologic technical support
662
Behavioral Epidemiology of Gonorrhea and Chlamydia
also important differences between these pathogens and the diseases they cause. Gonorrhea is more often clinically apparent, and its signs and symptoms tend to be more overt (4-6). The incubation period for symptomatic gonorrhea is briefer than that for chlamydia. Gonococcal infections are disproportionately concentrated in lower socioeconomic status populations and minorities, while chlamydial infections are more common in the young, in women using oral contraceptives, and in persons of higher socioeconomic status (6). In addition, in many localities, gonorrhea, but not chlamydia, is the target of publicly funded control efforts which often include free screening for infection and notification of exposed partners ("contacts") by health department specialists. The purpose of this study was to examine differences in the epidemiology of these two infections, focusing on clinical presentations and behavioral factors associated with culture-proven N. gonorrhoeae and C. trachomatis infections among patients at a Baltimore, Maryland, sexually transmitted disease clinic. Elucidation of such differences might prove helpful in designing control strategies for these infections.
MATERIALS AND METHODS Study population
From April 1988 to May 1989, patients attending the Eastern Health District sexually transmitted disease clinic of the Baltimore City Health Department and being seen by a single clinician were invited to participate in the study. Consecutive series of 400 men and 400 women attending the clinic for reasons other than follow-up or testing for cure evaluations were eligible for enrollment; only three persons approached regarding study participation declined to do so. All subjects gave written informed consent for study enrollment using a consent form approved by the Joint Committee on Clinical Investigation of the Johns Hopkins University School of Medicine.
663
Clinical evaluation and specimen collection
Patients were interviewed using a standardized data collection form which included specific questions regarding sexual practices, prior sexually transmitted diseases, the nature of relationships with recent sexual partners, and selected demographic characteristics. As part of the questionnaire, a detailed sexual history was obtained, emphasizing sexual experiences which occurred in the 30 days prior to the clinic visit. In addition to numbers of sex partners, we elicited information describing the types of recent sexual relationships in which patients were involved. Participants were asked to classify their sex partners over the preceding 30 days into one of three mutually exclusive groups previously found to be useful for describing interpersonal contexts associated with the likelihood of gonococcal infection and condom use in this population (7, 8). In this classification, a partner with whom the patient had had sex for the first time during the 30 days preceding study enrollment was defined as a "new" partner. For sexual relationships of greater than 1 month's duration, relationships were defined by the interviewer as follows. A "regular" partner was defined as a person with whom the patient had been sexually active "often," similar to a "boyfriend" or "girlfriend." In contrast, a "casual" partner was one with whom the patient reported having sex on a more occasional basis for more than 1 month. These relationships appeared somewhat less serious, and partners were often described by patients as being "friends." Following completion of the questionnaire, a directed physical examination was performed. In men, two urethral specimens were collected using wire-shaft, Dacrontipped swabs. The first swab was used for preparation of a Gram stain specimen and for inoculation of culture medium for N. gonorrhoeae; the second swab was passed at least 1 cm beyond the first and was placed into transport medium for inoculation of cultures for C. trachomatis. In women, specimens were collected during a speculum ex-
664
Hook et al.
amination as follows. Following removal of adherent cervico-vaginal secretions with large cotton-tipped swabs, an endocervical sample was collected for preparation of a Gram stain and inoculation of modified Thayer-Martin medium for gonorrhea culture. A second endocervical swab was collected and was used to inoculate transport medium for C. tmchomatis culture. Microbiologic culture methods
N. gonorrhoeae. Specimens for gonorrhea culture were inoculated directly onto modified Thayer-Martin medium and were incubated for 24-48 hours in a 5 percent carbon dioxide atmosphere. Presumptive N. gonorrhoeae was identified on the basis of colonial morphology, Gram stain, and oxidase test; the identity of presumptive N. gonorrhoeae was confirmed using fluorescein-conjugated monoclonal antibodies (9) (Syva Corporation, Palo Alto, California). C. trachomatis. Chlamydia cultures were obtained using sterile Dacron-tipped swabs, placed in transport medium, and stored at 4°C until they could be frozen at -70°C (424 hours). Within 4 days of acquisition, specimens were thawed and 400/il of transport medium was inoculated into four microtiter plate wells for culture on McCoy cell monolayers as described previously (10). Following 48-72 hours of incubation, duplicate wells were evaluated using fluoresceinconjugated antichlamydial monoclonal antibodies to C. trachomatis (Syva Corporation) to detect positive cultures. Cultures which were negative at 48-72 hours were passed for blind subculture and reevaluated again 48-72 hours later. Cultures that were still negative following blind subculture were classified as negative. Statistical analysis. The data were analyzed using SAS software (11). Patients with positive cultures for both N. gonorrhoeae and C. trachomatis were excluded from the analysis. We used the chi-squared test to test for bivariate associations. In the multivariate analyses, a logistic transformation was used.
First, patients with gonorrhea were compared with patients with neither gonorrhea nor chlamydia infection. Second, cases with chlamydia infection were compared with the same group. In this way, adjusted odds ratios were computed, comparing the relative odds of disease for those with the characteristic of interest (e.g., gonorrhea or chlamydia) to those without that characteristic. Finally, in a third multivariate logistic regression analysis, characteristics distinguishing the two infections were compared. RESULTS Patient characteristics and prevalence of infection
Eight hundred consecutive patients (400 males and 400 females) attending the sexually transmitted disease clinic for reasons other than follow-up evaluation were enrolled in the study. Specimens from eight patients (six males and two females) were toxic to the cell cultures used for chlamydia detection. Because no chlamydia culture data were available, these participants were excluded from the analyses. The remaining 394 males and 398 females comprise the subjects of this report (table 1). The area served by the clinic is comprised of primarily lower income, nonwhite census tracts of the city. Those characteristics are reflected in the demographic distribution of the participants, who were predominately young, single, black residents of inner-city Baltimore. Seventy-five percent of the participants gave a history of a prior sexually transmitted disease; 45 percent of males and 31 percent of females reported previous episodes of gonorrhea. Since patients tended to be unfamiliar with C. trachomatis as a sexually transmitted disease pathogen, a history of prior chlamydial infection was not sought. The prevalences of gonorrheal and chlamydial infection at the time of study enrollment were 29 percent and 10 percent, respectively, for males and 23 percent and 14 percent, respectively, for females. Eleven (2.8 percent) males and 22 (5.5 percent)
Behavioral Epidemiology of Gonorrhea and Chlamydia
665
females had coexistent gonococcal and chlamydial infections. Patients with coexistent gonorrhea and chlamydia were too few to permit separate analysis and could not be included with patients who had gonorrhea only, chlamydia only, or neither infection; therefore, they were excluded from further analyses.
to a nadir of 15 percent in the 25- to 29-year age group, and increased again to 24 percent among males aged 30 years or more (table 2). The prevalence of C. trachomatis in males did not vary with age, although a greater percentage of adolescents and males aged 20-24 years were infected than males aged 25 years or more. In females, the prevalence of both infections was greatest in adolescents and declined steadily with age. The reasons for attending the clinic differed between males and females. Two thirds (255 of 383) of males attended the clinic for symptom evaluation, 15 percent attended following notification of exposure to an infected person, and 19 percent attended for other reasons, such as screening. In contrast, 45 percent of females attended the clinic for symptom evaluation, 23 percent attended as contacts of infected persons, and 31 percent visited the clinic for other services, including screening, pregnancy testing, and contraceptive evaluation. Disease prevalence also varied when participants were stratified by sex and reason for visit (table 2). Among males, gonorrhea was present in 37 percent of symptomatic patients, 11 percent of sexual contacts, and 3 percent of males attending for other reasons. Less variation in chlamydia prevalence was observed among males when they were stratified by reason for visit: 9 percent of males seen for symptom evaluation had positive chlamydia cultures, as did 11 percent of sexual contacts. In females, as in males, gonorrhea prevalence but not chlamydia prevalence varied with reason for clinic attendance (table 2). Gonorrhea and chlamydia rates were 9 percent and 8 percent, respectively, in females attending for symptom evaluation, 40 percent and 11 percent in females who were recent contacts of an infected person, and 15 percent and 9 percent in females attending for other reasons.
Relation of age and reason for visit to gonococcal and chlamydial infection
Relation of numbers and types of sexual partners to gonorrhea and chlamydia prevalence
In males, gonorrhea prevalence was greatest (38 percent) among adolescents, declined
Males attending the clinic tended to report more sexual partners during their lifetime
TABLE 1. Demographic characteristics and disease prevalence in 792 persons attending an inner-city sexually transmitted disease clinic in Baltimore, Maryland, 1988-1989 Characteristic
Men (n = 394)
Women (n = 398)
No.
%
No.
%
Age (years) 30
74 129 83 108
19 33 21 27
153 104 70 71
38 26 18 18
Race Black Other
387 7
98 2
378 20
95 5
Marital status Single or divorced Married
369 25
94 6
379 19
95 5
Education (years) 12
142 195 57
36 50 15
191 160 47
48 40 12
Currently in school
72
18
144
36
Currently employed
270
69
182
46
History of prior sexually transmitted disease
300
76
294
74
History of gonorrhea
179
45
125
31
Culture results Culture positive for N. gonorrhoeae Culture positive for C. trachomatis
133
29
90
23
40
10
56
14
666
Hook et al.
TABLE 2. Prevalence of gonorrhea and chlamydia among persons attending an inner-city sexually transmitted disease clinic, by selected demographic and clinical characteristics*: Baltimore, Maryland, 1988-1989 Females (n = 376)
Males (n = 383)
%
Characteristic
%
No.
No. Gonorrhea
Chlamydia
Neither
Gonorrhea
Chlamydia
Neither
142 98 67 69
22
19 5 3
59 76 82 88
Age (years) 30
71 124 80 108
38 30 15 24
8 12
5
54 58 81 71
Education (years) 12
136 192 55
33 27 11
4 10 9
63 64 80
177 152 47
19 16 19
13 5 6
68 78 74
255
37
9
54
169
9
8
82
57 71
11
11
79 97
88 117
40 15
11 9
49 77
History of gonorrhea
176
31
7
62
118
17
6
77
Age (years) at first sexual intercourse 18
72 145 131 34
28 30 24 18
6 8 8 9
67 63 67 74
16 136 174 48
25 15 21 15
19 12 6 6
56 74 72 79
Reason for visit Symptoms Contact with someone with a sexually transmitted disease Other
4
3
19 15 12
* Excludes 33 participants (11 males and 22 females) who were infected with both pathogens.
and in the preceding year than females (table 3). Median numbers of sexual partners, lifetime and in the past year, were 20 and 4, respectively, for males and 5 and 2, respectively, for females. In the 30 days preceding clinic attendance, the median number of sexual partners for both sexes was one; 42 percent of males and 15 percent of females reported having had two or more sexual partners. For males, gonorrhea was not associated with number of lifetime sexual partners. However, when stratified by number of partners in the preceding year or the preceding 30 days, significant associations were noted (table 3). For chlamydia infection, no association between numbers of sexual partners and the likelihood of infection could be discerned for male participants, irrespective of the time frame used. For females, there was a tendency to be
culture-positive for N. gonorrhoeae with greater numbers of sexual partners, although for each time frame, those reporting the most sexual partners were somewhat less likely to have gonorrhea than females in other categories. The prevalence of C. trachomalis infection did not increase with increasing numbers of sexual partners over any of the time intervals studied. Rather, the highest prevalence of C. trachomatis infection occurred in females reporting fewer partners in their lifetime or in the past 30 days and in females with more than one but less than four partners in the past year. To address the possibility that the nature of patients' relationships with their recent sexual partners might be associated with risk for gonorrhea or chlamydia, we stratified participants hierarchically by sex and by their self-reported relationship to their sex-
Behavioral Epidemiology of Gonorrhea and Chlamydia
667
TABLE 3. Isolation of gonococcus and chlamydia in sexually transmitted disease clinic patients, by numbers of sex partners over a lifetime, the past year, and the preceding 30 days: Baltimore, Maryland, 1988-1989 Females (n = 376)
Males (n = 383) No. of partners
%
%
No
Lifetime* 30 Past year 0-1 2-4 5-9 210
Past 30 days 0 1 2 >3
No. Gonorrhea
Chlamydia
Gonorrhea
Chlamydia
77 92 69
25 26 22
141
31
9 3 10 9
263 70 18
14 29 33
11 3 1
24
17
4
50 179 83 71
14 26 34
16 6 6 7
142 198 26 10
12 21 27 20
12 12 10
18 205
11 21
9
38 281
5 18 33
13 10 2
29
109
34
7
49
51
39
4
8
5
• Data were missing for four males and one female with gonorrhea.
ual partners in the 30 days preceding clinic attendance (table 4). For males, gonococcal infection was most common in those reporting sex with a new partner, was less common in those reporting casual partners, and was lowest in males reporting sex only with regular partners. In contrast, for chlamydia infections, the association with type of partner was reversed. Chlamydia was most common in males reporting only regular sexual partners, intermediate in those who reported casual partners, and lowest (2 percent) in men who reported having had new sexual partners in the preceding 30 days. In females, although there was no clear relation between types of recent sexual part-
ners and gonorrhea prevalence, chlamydia was again most common in females reporting sex only with regular partners (10 percent), compared with 3 percent in females with casual partners and 4 percent in females reporting new partners (table 4). Multivariate analysis of risk factors associated with N. gonorrhoeae and C. trachomatis infection
To further evaluate the relative import of variables found to be associated with gonorrhea or chlamydia infections, we performed multivariate logistic regression analyses (table 5). To determine which factors were independently associated with likeli-
TABLE 4. Isolation of gonococcus and chlamydia in sexually transmitted disease clinic patients, by type of most recent sexual relationship*: Baltimore, Maryland, 1988-1989
Gonorrhea
Chlamydia
Total no.
No.
%
No.
%
171 82 112
24 26 50
14 32 45
22 5 2
CO CM
Regular Casual New
Females (n == 338)
Males (n = 365)
CO
Type of partner in the past 30
Gonorrhea
Chlamydia
Total no.
No.
%
No.
%
275 37 26
53 9 4
19 24 15
28 1 1
10 3 4
* Patients with no sexual partners in the preceding 30 days were excluded. Hierarchical classification: any new partner > any causal partner > regular partner(s) only.
668
Hook et al.
TABLE 5. Adjusted odds ratios for gonorrheal or chlamydial infection in persons attending an inner-city sexually transmitted disease clinic, Baltimore, Maryland, 1988-1989 Males Factor
Gonorrhea OR*
Age 1 partner in the past 30 days Regular partner Casual partner New partner Casual/new partner
95% Clt
Females Chlamydia
OR
95% Cl
1.93 1.02-3.64* 1.40 0.52-3.77 8.07 3.71-17.57*** 2.83 1.09-7.30* 0.97 1.01 1.86 2.78
0.45-2.17 0.50-2.06 0.83-4.16 1.64-6.07*
2.85 1.04 0.19 0.07
Chlamydia
Gonorrhea
OR
95% Cl
1.86 1.05-3.27* 0.29 0.16-0.54***
2.33 0.63-8.69 0.91-8.94f 0.31-3.47 3.85 1.27-11.73* 0.05-0.77* 0.01-0.39*** 0.76 0.18-1.56
OR
95% Cl
7.79 3.28-18.47*** 0.91 0.43-1.91 0.49 0.06-4.18 0.93 0.31-2.72
0.47 0.05-4.16
• p < 0.05; *• p < 0.01; *•* p < 0.001. tp
