Vol. 29, No. 10
JOURNAL OF CLINICAL MICROBIOLOGY, Oct. 1991, p. 2139-2143
0095-1137/91/102139-05$02.00/0 Copyright C) 1991, American Society for Microbiology
Characterization of Risk Factors for Helicobacter pylori Infection among Men Attending a Sexually Transmitted Disease Clinic: Lack of Evidence for Sexual Transmission LOUIS B. POLISH,"2t JOHN M. DOUGLAS, JR. ,12,3* ARTHUR J. DAVIDSON,2'3 GUILLERMO I. PEREZ-PEREZ,4 AND MARTIN J. BLASER4 Division of Infectious Diseases, Department of Medicine,' and Department of Preventive Medicine,3 University of
Colorado School of Medicine, Denver, Colorado 80262; Denver Disease Control Service, Denver Department of Health and Hospitals, Denver, Colorado 8020445072; and Division of Infectious Diseases, Department of Medicine, and Division of Infectious Diseases, Vanderbilt University School of Medicine, and Veterans Affairs Medical Center, Nashville, Tennessee 372324 Received 4 January 1991/Accepted 27 June 1991
The mechanism of transmission of Helicobacter pylori is unknown. To investigate the role of sexual behavior and demographic factors in the acquisition of H. pyloni infection, we evaluated the seroprevalence of antibody to H. pylori in 370 men attending an urban sexually transmitted diseases clinic. Sera from the following three groups were analyzed by enzyme-linked immunosorbent assay for H. pyloni-specific immunoglobulin G: 78 human immunodeficiency virus (HIV)-seropositive homosexual men, 102 HIV-seronegative homosexual men, and 190 HIV-seronegative heterosexual men. Overall, the seroprevalence of H. pyloni was 100 of 370 men (27%), with rates of 18% in HIV-seropositive homosexual men and 20% in HIV-seronegative homosexual men versus 35% in heterosexual men (P < 0.005, x2 test). By ethnic group, 21 (12%) of 181 Caucasian men, 40 (41%) of 97 black men, and 37 (43%) of 87 Hispanic men were seropositive (P < 0.001, X2 test). Multivariate analysis revealed that race was associated with H. pyloni seropositivity independent of HIV status, sexual preference, or age. There was no relationship between H. pylori seropositivity and the number of lifetime sexual partners or previous sexually transmitted diseases. Three HIV-seropositive men with H. pylori immunoglobulin G had essentially identical antibody titers over 8 to 16 months of follow-up. In conclusion, black and Hispanic men have significantly higher H. pylori seroprevalence rates than do Caucasian men, but neither sexual behavior nor HIV infection influences the presence or persistence of H. pylori antibody. Further evaluation of the factors associated with these ethnic differences may lead to a better understanding of H. pyloni acquisition and transmission.
Epidemiologic investigation of Helicobacter pylori (formerly Campylobacter pylori) (12) infection has largely been based on detection of the bacteria from specimens obtained at the time of endoscopy. Infection is chronic, lasting for years or decades and possibly for life (22). Infected individuals mount an antibody response to H. pylori (17, 29), and recent refinements permit sufficiently high specificity and sensitivity of immunoglobulin G (IgG) and IgA assays for use as diagnostic tests (7, 8, 25). Given this degree of accuracy, serologic diagnosis has become an important tool to further define the epidemiology of H. pylori infection (24). The mechanism of H. pylori transmission remains unknown. Marshall and colleagues (17) found that H. pylori antibody in women attending a sexually transmitted disease (STD) clinic is more common in those women with reactive serologic tests for syphilis than in those without reactive serologic tests for syphilis. In addition, Aceti et al. (1) found that antibody levels were higher in homosexual men than in age-matched heterosexual men. Both studies suggest that sexual behavior could be important in the transmission of this organism. These observations are consistent with the known potential for oral-anal sexual transmission in homosexual men of a variety of enteric pathogens including * Corresponding author. t Present address: Hepatitis Branch, Division of Viral Diseases, Centers for Disease Control, Atlanta, GA 30333.
Shigella sp., Salmonella sp., Campylobacter sp., Giardia lamblia, Entamoeba histolytica, and hepatitis A virus (4, 27, 28). To investigate the role of sexual behavior and demographic characteristics in the acquisition of H. pylori, we evaluated the seroprevalence of infection in 370 men attending an urban STD clinic. MATERIALS AND METHODS
Population. Sera from 2,168 men collected from May 1987 through July 1988 in the course of studies of human immunodeficiency virus (HIV) seroprevalence in the Denver Metro Health Clinic for STD were available for evaluation. Of these, a total of 370 serum samples were selected from among the following three clinical groups: HIV-seropositive homosexual men (n = 78), HIV-seronegative homosexual men (n = 102), and HIV-seronegative heterosexual men (n = 190). In order to achieve a broad demographic distribution within each group, specimens were selected chronologically from available samples on the basis of age group (40
HIV- nomosexual HIV- Heterosexual
N=38
0
CI
30
0 C'
20
40 in Years Age FIG. 1. Seroprevalence of H. pylori infection by age, sexual preference, and HIV status among 370 men attending the Denver Metro Health Clinic.
DISCUSSION This study was based on the use of a serologic assay to detect serum IgG to H. pylori as a means of determining the prevalence of infection. The assay has been validated previously in comparison with examination of H. pylori in gastric biopsy specimens and has sensitivity and specificity each exceeding 90% (7, 8, 11, 23, 32, 33). Therefore, serology is a reliable tool for diagnosing H. pylori infections in seroepidemiologic studies (6, 13, 18, 19, 22, 24, 26). The source of H. pylori as well as the mechanism of its transmission to humans remain unknown. Since H. pylori is present in low concentrations in gastric juice and has not been isolated from saliva, feces, or urethral or vaginal swabs, plausible modes of person-to-person transmission have not been proposed (5). Attempts to better define mechanisms of transmission through serologic studies have yielded conflicting results. Mentally retarded institutionalized residents were found to have higher seropositivity rates TABLE 2. Multivariate analysis of factors associated with H. pylori seropositivity
White
3 Black *} Hispanic
60~
._D
HIV-seropositive homosexual men found to have H. pylori antibody (Table 3). Antibody titers remained elevated and essentially constant over 8 to 16 months in all three men. Data regarding T4 cell count and stage of HIV infection were not available.
No. (%) H. pylori:
Factor
oQ 5Q.
Seropositive (n
=
100)
(n = 270)
Adjusted odds ratio
95% confidence intervals
Seronegative
0
a)
40cn ._= 0
Non-Caucasian ethnicity
72 (72)
110 (41)
5.7
3.1-10.3
Homosexual
34 (34)
146 (54)
0.7
0.4-1.3
1.0
0.9-1.0
1.1
0.5-2.5
a 30-
preference
c 20
N=41
N=17
0
L 10 a.
N-S
0O
Age in Years FIG. 2. Seroprevalence of H. pylori infection by age and ethnicamong 368 men attending the Denver Metro Health Clinic.
ity
Age (yr)
JOURNAL OF CLINICAL MICROBIOLOGY, Oct. 1991, p. 2139-2143
0095-1137/91/102139-05$02.00/0 Copyright C) 1991, American Society for Microbiology
Characterization of Risk Factors for Helicobacter pylori Infection among Men Attending a Sexually Transmitted Disease Clinic: Lack of Evidence for Sexual Transmission LOUIS B. POLISH,"2t JOHN M. DOUGLAS, JR. ,12,3* ARTHUR J. DAVIDSON,2'3 GUILLERMO I. PEREZ-PEREZ,4 AND MARTIN J. BLASER4 Division of Infectious Diseases, Department of Medicine,' and Department of Preventive Medicine,3 University of
Colorado School of Medicine, Denver, Colorado 80262; Denver Disease Control Service, Denver Department of Health and Hospitals, Denver, Colorado 8020445072; and Division of Infectious Diseases, Department of Medicine, and Division of Infectious Diseases, Vanderbilt University School of Medicine, and Veterans Affairs Medical Center, Nashville, Tennessee 372324 Received 4 January 1991/Accepted 27 June 1991
The mechanism of transmission of Helicobacter pylori is unknown. To investigate the role of sexual behavior and demographic factors in the acquisition of H. pyloni infection, we evaluated the seroprevalence of antibody to H. pylori in 370 men attending an urban sexually transmitted diseases clinic. Sera from the following three groups were analyzed by enzyme-linked immunosorbent assay for H. pyloni-specific immunoglobulin G: 78 human immunodeficiency virus (HIV)-seropositive homosexual men, 102 HIV-seronegative homosexual men, and 190 HIV-seronegative heterosexual men. Overall, the seroprevalence of H. pyloni was 100 of 370 men (27%), with rates of 18% in HIV-seropositive homosexual men and 20% in HIV-seronegative homosexual men versus 35% in heterosexual men (P < 0.005, x2 test). By ethnic group, 21 (12%) of 181 Caucasian men, 40 (41%) of 97 black men, and 37 (43%) of 87 Hispanic men were seropositive (P < 0.001, X2 test). Multivariate analysis revealed that race was associated with H. pyloni seropositivity independent of HIV status, sexual preference, or age. There was no relationship between H. pylori seropositivity and the number of lifetime sexual partners or previous sexually transmitted diseases. Three HIV-seropositive men with H. pylori immunoglobulin G had essentially identical antibody titers over 8 to 16 months of follow-up. In conclusion, black and Hispanic men have significantly higher H. pylori seroprevalence rates than do Caucasian men, but neither sexual behavior nor HIV infection influences the presence or persistence of H. pylori antibody. Further evaluation of the factors associated with these ethnic differences may lead to a better understanding of H. pyloni acquisition and transmission.
Epidemiologic investigation of Helicobacter pylori (formerly Campylobacter pylori) (12) infection has largely been based on detection of the bacteria from specimens obtained at the time of endoscopy. Infection is chronic, lasting for years or decades and possibly for life (22). Infected individuals mount an antibody response to H. pylori (17, 29), and recent refinements permit sufficiently high specificity and sensitivity of immunoglobulin G (IgG) and IgA assays for use as diagnostic tests (7, 8, 25). Given this degree of accuracy, serologic diagnosis has become an important tool to further define the epidemiology of H. pylori infection (24). The mechanism of H. pylori transmission remains unknown. Marshall and colleagues (17) found that H. pylori antibody in women attending a sexually transmitted disease (STD) clinic is more common in those women with reactive serologic tests for syphilis than in those without reactive serologic tests for syphilis. In addition, Aceti et al. (1) found that antibody levels were higher in homosexual men than in age-matched heterosexual men. Both studies suggest that sexual behavior could be important in the transmission of this organism. These observations are consistent with the known potential for oral-anal sexual transmission in homosexual men of a variety of enteric pathogens including * Corresponding author. t Present address: Hepatitis Branch, Division of Viral Diseases, Centers for Disease Control, Atlanta, GA 30333.
Shigella sp., Salmonella sp., Campylobacter sp., Giardia lamblia, Entamoeba histolytica, and hepatitis A virus (4, 27, 28). To investigate the role of sexual behavior and demographic characteristics in the acquisition of H. pylori, we evaluated the seroprevalence of infection in 370 men attending an urban STD clinic. MATERIALS AND METHODS
Population. Sera from 2,168 men collected from May 1987 through July 1988 in the course of studies of human immunodeficiency virus (HIV) seroprevalence in the Denver Metro Health Clinic for STD were available for evaluation. Of these, a total of 370 serum samples were selected from among the following three clinical groups: HIV-seropositive homosexual men (n = 78), HIV-seronegative homosexual men (n = 102), and HIV-seronegative heterosexual men (n = 190). In order to achieve a broad demographic distribution within each group, specimens were selected chronologically from available samples on the basis of age group (40
HIV- nomosexual HIV- Heterosexual
N=38
0
CI
30
0 C'
20
40 in Years Age FIG. 1. Seroprevalence of H. pylori infection by age, sexual preference, and HIV status among 370 men attending the Denver Metro Health Clinic.
DISCUSSION This study was based on the use of a serologic assay to detect serum IgG to H. pylori as a means of determining the prevalence of infection. The assay has been validated previously in comparison with examination of H. pylori in gastric biopsy specimens and has sensitivity and specificity each exceeding 90% (7, 8, 11, 23, 32, 33). Therefore, serology is a reliable tool for diagnosing H. pylori infections in seroepidemiologic studies (6, 13, 18, 19, 22, 24, 26). The source of H. pylori as well as the mechanism of its transmission to humans remain unknown. Since H. pylori is present in low concentrations in gastric juice and has not been isolated from saliva, feces, or urethral or vaginal swabs, plausible modes of person-to-person transmission have not been proposed (5). Attempts to better define mechanisms of transmission through serologic studies have yielded conflicting results. Mentally retarded institutionalized residents were found to have higher seropositivity rates TABLE 2. Multivariate analysis of factors associated with H. pylori seropositivity
White
3 Black *} Hispanic
60~
._D
HIV-seropositive homosexual men found to have H. pylori antibody (Table 3). Antibody titers remained elevated and essentially constant over 8 to 16 months in all three men. Data regarding T4 cell count and stage of HIV infection were not available.
No. (%) H. pylori:
Factor
oQ 5Q.
Seropositive (n
=
100)
(n = 270)
Adjusted odds ratio
95% confidence intervals
Seronegative
0
a)
40cn ._= 0
Non-Caucasian ethnicity
72 (72)
110 (41)
5.7
3.1-10.3
Homosexual
34 (34)
146 (54)
0.7
0.4-1.3
1.0
0.9-1.0
1.1
0.5-2.5
a 30-
preference
c 20
N=41
N=17
0
L 10 a.
N-S
0O
Age in Years FIG. 2. Seroprevalence of H. pylori infection by age and ethnicamong 368 men attending the Denver Metro Health Clinic.
ity
Age (yr)
