Original Article
Seroprevalence of HTLV-I and HTLV-II among Intravenous Drug Users and Persons in Clinics for Sexually Transmitted Diseases
N Engl J Med 1992; 326:375-380February 6, 1992
- Abstract
- Abstract
Background.
The human T-cell lymphotropic virus Type I (HTLV-I) is associated with adult T-cell leukemia and myelopathy, whereas HTLV-II infection has uncertain clinical consequences. We assessed the seroprevalence of these retroviruses among intravenous drug users and among patients seen at clinics for sexually transmitted diseases (STD clinics).
Methods.
We used serum samples that were collected in eight cities in 1988 and 1989 during surveys of human immunodeficiency virus infection among intravenous drug users entering treatment and persons seen in STD clinics. The serum samples were tested for antibodies to HTLV, and positive specimens were tested further by a synthetic peptide-based enzyme-linked immunosorbent assay to differentiate between HTLV-I and HTLV-II.
Results.
Among 3217 intravenous drug users in 29 drug-treatment centers, the median seroprevalence rates of HTLV varied widely according to city (range, 0.4 percent in Atlanta to 17.6 percent in Los Angeles). Seroprevalence increased sharply with age, to 32 percent in persons over 44 years of age. HTLV infection was more common among blacks (15.5 percent) and Hispanics (10.7 percent) than among whites (4.1 percent), and it was strongly associated with a history of heroin injection (P≤0.001). Among 5264 patients in 24 STD clinics, the median rates of HTLV infection were much lower (range, 0.1 percent in Atlanta and Newark to 2.0 percent in Los Angeles). Again, this infection was more common among intravenous drug users (7.6 percent) than among non—drug users (0.7 percent). Eighty-four percent of the seropositive samples from drug-treatment centers and 69 percent of those from STD clinics were due to HTLV-II infection (P = 0.03).
Conclusions.
HTLV infection is common among intravenous drug users and is primarily caused by HTLV-II. Among patients seen at STD clinics, HTLV is strongly associated with intravenous drug use, but the retrovirus is also prevalent among non—drug users. (N Engl J Med 1992;326:375–80.)
Media in This Article
Figure 1
Seroprevalence Rates of HTLV (Solid Bars) and HIV (Stippled Bars) in Patients Studied at Drug-Treatment Centers in Eight Cities, 1988 and 1989.Figure 2
Seroprevalence Rates of HTLV (Solid Bars) and HIV (Stippled Bars) in Patients Studied at STD Clinics in Eight Cities, 1988 and 1989.Article Activity
- Article
HUMAN T-cell lymphotropic viruses Type I (HTLV-I) and Type II (HTLV-II) are closely related retroviruses.1 HTLV-I is associated with adult T-cell leukemia and with myelopathy or tropical spastic paraparesis.2 HTLV-II, first isolated from a patient with a variant of hairy-cell leukemia, has not been consistently associated with any specific disease. Seroreactivity to HTLV has been well documented among intravenous drug users in several major U.S. metropolitan areas.3 , 4 Reported seroprevalence rates in intravenous drug users have ranged from 2 percent to 49 percent. These rates are difficult to compare, however, because of differences in study design, in sampling schemes, in the HTLV serologic tests, and in the definition of seropositivity. In some studies in which lymphocytes were available from HTLV-seropositive intravenous drug users, assays using the polymerase chain reaction have showed the seroreactivity to be due mostly to HTLV-II.5 , 6
In addition to parenteral transmission by blood transfusion7 and transmission from mother to child,8 HTLV can be transmitted sexually.9 Data on the prevalence of HTLV infection in sexually active persons in the United States are limited.10
In 1988, the Centers for Disease Control (CDC), in collaboration with local and state health departments, began national surveillance to obtain a standardized assessment of the rates of infection with the human immunodeficiency virus (HIV) in serum samples from various population groups.11 These serologic surveys provided a unique opportunity for systematic assessment of the seroprevalence and epidemiologic characteristics of HTLV in two relevant populations: intravenous drug users in drug-treatment centers and patients in clinics for sexually transmitted diseases (STD clinics). Anonymous serum samples from patients in eight cities were tested for HTLV antibodies with uniform serologic tests and standardized criteria for seropositivity. In addition, HTLV-seropositive specimens were tested by type-specific peptide assays to differentiate HTLV-I from HTLV-II.
Methods
Subjects
The HTLV serologic survey was conducted from April 1988 through January 1990 in eight sentinel cities participating in national HIV surveillance11: Los Angeles, Denver, Atlanta, New Orleans, Newark, New York, Cleveland, and Seattle. The surveys followed standardized protocols, were anonymous and unlinked (i.e., blinded), and used blood specimens collected from consecutive eligible patients for routine diagnostic purposes during clinic visits. Demographic information was retained, as well as limited data on risk factors and HIV-test results.
At the participating drug-treatment centers, persons entering treatment who reported having injected illicit drugs during the past year were eligible; persons who reported only alcohol use and those who requested only HIV testing were excluded. To avoid sampling the same subjects repeatedly, only new entrants and persons who were having blood drawn for the first time during the survey period were enrolled. At the STD clinics, clients who were making an initial visit because of a new STD or who had not visited the clinic during the previous three months were eligible, but clients attending the clinic for follow-up visits or coming specifically for HIV testing were excluded from the study. Although it is theoretically possible that patients returning to the clinic because of a new STD after three months had another specimen collected, this is unlikely. STD clinics usually reach the number of samples required for the survey in less than three months, and blood is generally not drawn again during that interval. In both surveys, serum samples that remained after HIV testing were frozen at —20°C until testing.
At the drug-treatment centers, 177 to 530 serum samples were chosen per city. In Los Angeles, Denver, Atlanta, Seattle, Newark, Cleveland, and New Orleans, these were all consecutive HIV-tested specimens, and in New York, for logistic reasons related to storage, they were a random sample of all such specimens. At the STD clinics, 446 to 1150 serum samples were chosen per city. In Los Angeles, Denver, Atlanta, Seattle, Newark, and Cleveland, these were consecutive HIV-tested specimens, and in New Orleans and New York, also for logistic reasons, they were a random sample of all such specimens. In each sample, ≥0.2 ml of serum remained after HIV testing. The lower number of patients tested at the drug-treatment centers was due, in most instances, to the lack of additional samples.
Laboratory Tests
The serum samples were screened for HTLV with a commercial HTLV-I enzyme-linked immunosorbent assay (ELISA) (Dupont, Wilmington, Del.), and repeatedly reactive samples were tested further by Western blotting and radioimmunoprecipitation.12 Seropositivity was defined as the presence of antibody to gag p24 and env gp46 or gp61/68, according to the criteria of the Public Health Service.13 Serum samples with antibody to these HTLV antigens that did not fulfill the above criteria were considered indeterminate. All other serum samples, including those repeatedly reactive on ELISA but without bands on Western blotting, were considered negative.
To differentiate between HTLV-I infection and HTLV-II infection, HTLV-seropositive serum samples were tested further by commercially available, synthetic peptide-based ELISA tests shown to be 100 percent specific in differentiating the two retroviruses.14 Seropositive samples were tested first with a peptide-based ELISA (SynthEIA HTLV-I EIA RV900250 and SynthEIA HTLV-II EIA RV900750, United Biomedical, Lake Success, N.Y.), performed and interpreted according to the instructions of the manufacturer. Specimens in which HTLV-I and HTLV-II could not be differentiated by this method were tested further with another peptide-based ELISA (Select-HTLV B-005, IAF Biochem. International, Montreal) performed according to the instructions of the manufacturer.
HlV testing was performed at the laboratories of state and local health departments with whole-virus-lysate ELISA and Western blot assays licensed by the Food and Drug Administration. HIV-1 Western blot assays were interpreted according to the criteria of the Association of State and Territorial Public Health Laboratory Directors and the CDC.15
Statistical Analysis
The participants with indeterminate results of HTLV serologic testing were included in the denominator for the calculation of seroprevalence rates but were excluded from the other analyses. Prevalence rates were calculated for each clinic, and median rates were computed for all the clinics in each city. For comparison, HIV prevalence rates were calculated similarly for the samples tested. All the analyses were stratified according to city, and the significance of the associations between the characteristics of the participants and HTLV or HIV seropositivity was determined with the Cochran—MantelHaenszel statistic. A log-linear model was used to examine the variation in HTLV and HIV rates according to city. Data were pooled for presentation in tabular form.
Results
For the 3217 intravenous drug users entering 29 drug-treatment centers, the median clinic rates of HTLV seroprevalence in the eight cities ranged from a low of 0.4 percent for two clinics in Atlanta to a high of 17.6 percent for six clinics in Los Angeles, followed by 14.4 percent for two clinics in New Orleans and 9.4 percent for four clinics in Seattle. The geographic distribution of HTLV was significantly different from that of HIV, which was most prevalent in Newark (28.6 percent) and New York (18.5 percent) and least prevalent in Seattle (0.7 percent) and Los Angeles (1.8 percent) (P<0.001) (Fig. 1Figure 1
Seroprevalence Rates of HTLV (Solid Bars) and HIV (Stippled Bars) in Patients Studied at Drug-Treatment Centers in Eight Cities, 1988 and 1989.).HTLV seroprevalence rates for intravenous drug users entering drug treatment were similar in men and in women, but they increased significantly with age in all sites and were significantly higher among nonwhites than among whites (Table 1Table 1
Characteristics of Persons Studied at Drug-Treatment Centers with Respect to Seropositivity for HTLV or HIV.). The rates were significantly higher when heroin was the primary drug injected, and they were also higher in heterosexual patients than in those who were homosexual or bisexual. In contrast, HIV seroprevalence rates were significantly higher in men than in women, although this difference was mostly due to the association of HIV with homosexual or bisexual activity in men (Table 1). As with HTLV, HIV seroprevalence rates among intravenous drug users were significantly higher in nonwhites than in whites, and they increased with age, though less dramatically (Table 1). HIV was associated with a homosexual or bisexual orientation, but the association varied significantly from city to city.HTLV seroprevalence rates were much lower among the 5264 patients seen at the STD clinics than in the intravenous drug users; they ranged from 0.1 percent in two Newark clinics and three Atlanta clinics to 2.0 percent in two Los Angeles clinics. Seroprevalence rates for HTLV at the STD clinics were lower than the rates for HIV (Fig. 2Figure 2
Seroprevalence Rates of HTLV (Solid Bars) and HIV (Stippled Bars) in Patients Studied at STD Clinics in Eight Cities, 1988 and 1989.).Among the patients at the STD clinics, HTLV seroprevalence rates were also similar among men and women and were highest in blacks. No significant difference in these rates was found between whites and nonwhites, however (Table 2Table 2
Characteristics of Persons Studied at STD Clinics with Respect to Seropositivity for HTLV or HIV.). HTLV seroprevalence rates for the patients at the STD clinics were associated with age and were significantly higher in persons with a history of intravenous drug use since 1978 than in those without such a history (P<0.001); they were also higher in persons who had exchanged drugs or money for sex (P<0.01) (Table 2). HIV seroprevalence rates for these same persons were higher in men than in women, but the difference varied significantly from city to city (Table 2). The exclusion of men with a homosexual or bisexual orientation resulted in similar HIV rates in men (2.5 percent) and in women (1.8 percent). Like HTLV, HIV was associated with age and a history of intravenous drug use; unlike HTLV, however, it was also significantly associated with a homosexual or bisexual orientation in men.When the HTLV analyses were restricted to the 4980 patients at the STD clinics who had no history of intravenous drug use, the association between HTLV and the exchange of drugs or money for sex was not significant (P = 0.29), and no further association with blood transfusion or sexual orientation was found.
Among intravenous drug users, the association between HTLV and HIV was significant when the data for all the cities were combined (adjusted odds ratio, 2.2), with the strongest association observed in New York (Table 3Table 3
Association between HTLV and HIV in Intravenous Drug Users Entering Drug Treatment.*). Among the patients at the STD clinics, there was also an association between HTLV and HIV (adjusted odds ratio, 2.7; 95 percent confidence interval, 1.0 to 6.9; P = 0.04), although there were only 52 HTLV-positive samples.Of the 294 HTLV-seropositive serum samples from the drug-treatment clinics and the 52 such samples from the STD clinics, 234 (80 percent) and 32 (62 percent), respectively, contained sufficient serum to permit further testing by the peptide-based ELISA. Of those samples, 197 from the drug-treatment centers (84 percent) and 22 from the STD clinics (69 percent) could be classified as having HTLV-II infection, whereas 19 (8 percent) and 6 (19 percent), respectively, had HTLV-I infection. In 18 of 234 samples from the drug-treatment centers (7.7 percent) and 4 of 32 samples from the STD clinics (13 percent), the two infections could not be differentiated. HTLV-II infection was more common in the patients studied in the drug-treatment centers than in those from the STD clinics (odds ratio, 2.4; 95 percent confidence interval, 0.98 to 5.9; P = 0.03). It was at least 2.5 times more prevalent than HTLV-I in both settings in all the cities except Atlanta, where there was insufficient remaining serum for peptide testing. Of the 6 patients with HTLV-I at the STD clinics, 1 (17 percent) had a history of intravenous drug use, as compared with 6 of the 22 patients with HTLV-II infection (27 percent) (P = 0.5 by Fisher's exact test).
Discussion
This large, standardized serologic survey of HTLV in high-risk populations in the United States allowed a more accurate estimate of the prevalence of HTLV infection in intravenous drug users and patients at STD clinics than have previous studies based on voluntary testing.16 Our blinded survey confirms that HTLV infection is common among intravenous drug users throughout the United States and that unlike HIV infection, HTLV infection is more prevalent among intravenous drug users than in any other group at risk for HIV.17 , 18 Our data on patients attending STD clinics document that in the United States HTLV infection is not limited to intravenous drug users. The mean seroprevalence of HTLV in patients at STD clinics who had no history of intravenous drug use was 0.7 percent, 10 times higher than the rates reported in voluntary blood donors. 19 , 20
In intravenous drug users entering drug treatment, the HTLV seroprevalence rates ranged from 0.4 percent to 18 percent; these rates varied according to geographic location, with a distribution different from that of HIV. Although the highest rates of HIV among intravenous drug users in this sample as well as in the complete survey were found in the cities on the Atlantic coast,21 we found the highest HTLV rates among intravenous drug users in Los Angeles, New Orleans, and Seattle.
Our study confirms that most of the HTLV seroreactivity among intravenous drug users in the United States is due to infection with HTLV-II. The only other populations in which HTLV-II has been reported are groups of American Indians.22 , 23 Further investigation, including molecular studies of HTLV-II strains isolated from intravenous drug users and American Indians, are needed to define the relation between the viruses infecting these populations.
The demographic data and limited data on risky behavior collected in this survey allow some insight into the epidemiologic features of HTLV infection in intravenous drug users, especially as compared with those of HIV infection. Like HIV, HTLV is generally more prevalent among nonwhite intravenous drug users, and the highest seroprevalence rates for both HIV and HTLV are among blacks. HTLV infection is more prevalent among older intravenous drug users, however, probably reflecting a presence in this population that is older and more endemic than that of the more recently introduced HIV.24 , 25 The association of HTLV with the use of heroin as the primary injected drug may also be due to more established infection that began at a time when heroin was the drug of choice. This association persists, however, after adjustment for age (odds ratio, 3.4, as compared with 3.2 before age adjustment). Further in-depth studies into behavior associated with drug use are needed for this association to be fully understood and explored. Another major difference between HTLV and HIV is that HIV is more prevalent among men with a homosexual or bisexual orientation who use intravenous drugs, which probably reflects the presence of a double risk for HIV in these men.
In all eight cities, the HTLV seroprevalence rates in patients at the STD clinics (range, 0.1 percent to 2.0 percent) were lower than the rates among intravenous drug users entering treatment. The rates of HTLV seroprevalence at the STD clinics paralleled those found in the drug-treatment centers; that is, they were lowest in the cities where the rates at the drug-treatment clinics were lowest and highest in the cities where those rates were highest, whereas the HIV rates observed in the STD clinics did not correlate with those in the drug-treatment clinics. This difference is explained by the fact that in the patients attending STD clinics, HTLV was associated primarily with intravenous drug use, whereas HIV is highly prevalent in homosexual or bisexual men in addition. A similar association of HTLV and intravenous drug use has also been reported among female prostitutes in the United States, in whom HTLV seroprevalence averages 7 percent.26
To differentiate between HTLV-I infection and HTLV-II infection, we relied on newly developed synthetic peptide-based ELISAs, which have demonstrated a 100 percent specificity in the correct classification of specimens typed by the polymerase chain reaction.14 These tests, with reported sensitivities ranging from 89 to 98 percent,14 allowed us to classify 92 percent of the seropositive samples tested. The peptide-based ELISAs open new doors for the study of the epidemiology of these infections, allowing us to confirm the suspicion, based on the use of the polymerase chain reaction in earlier studies,5 , 6 , 24 that among intravenous drug users HTLV-II is far more prevalent than HTLV-I. In all the cities where peptide testing was done, and in both the drug-treatment centers and the STD clinics, the frequency of HTLV-II infection exceeded that of HTLV-I. This relative difference in prevalence does not appear to be due to a higher prevalence of HTLV-I in persons who do not use intravenous drugs. With these assays, nonblinded studies of more specific aspects of drug use and other behavior associated with HTLV-I and HTLV-II should now be possible.
The clinical importance of HTLV-II remains obscure. Yet there is a definite need, in view of its prevalence in intravenous drug users, to identify any associated clinical manifestations. The association of HIV and HTLV in intravenous drug users and patients at STD clinics is also especially important in view of the suggestion that HTLV can act as a cofactor to accelerate the natural history of HIV infection.27
Presented in part at the 6th International Conference on AIDS. San Francisco, June 20–24, 1990.
We are indebted to the following persons for coordinating the study in the different cities: Peter Kerndt and Wesley Ford, Los Angeles County Department of Health Services; Elfreda Stanley and Jane Carr, Office of Infectious Diseases, Georgia Department of Human Resources, Atlanta; Isaac Weisfuse, New York City Health Department, and Bruce Coles, New York State Department of Health, Albany; Lori Borden, Public Health Department, Colorado Department of Health, Denver, and John Douglas, Denver Public Health; Robert Campbell, Max Proffitt, and Colleen Starkey, Cleveland Clinic Foundation; Ron Altman, Wayne Pizzuti, and S.I. Shahied, State of New Jersey Department of Health, Newark; Mark Dal Corso and Marion Alleman, State of Louisiana Department of Health and Hospitals, New Orleans; Noreen Harris, Sharon Hopkins, and June Nakata, King County Department of Public Health, Seattle; to Wanda Moore and Catherine Spruill for assistance in various aspects of the study, including data coordination and management; to Van Munn and Meade Morgan, for programming and statistical assistance; to Gene McCray and David Allen, who developed the HIV surveys in the STD clinics and drug-treatment centers; to the staff of the Epidemiology Response Laboratory at the CDC, for assistance with handling specimens; to John Oconnor for excellent editorial assistance; and to James Curran for critical review of the manuscript.
Source Information
From the Retrovirus Diseases Branch, Division of Viral and Rickettsial Diseases (R.F.K., T.M.H., B.R., J.E.K.), and the Division of HIV/AIDS (I.M.O.), National Center for Infectious Diseases, and the Division of STD/HIV Prevention (R.O.C.), National Center for Prevention Services, Centers for Disease Control, Atlanta; and United Biomedical, Inc., Lake Success, N.Y. (B.H.). Address reprint requests to Dr. Khabbaz at the Retrovirus Diseases Branch, MS-A32, Centers for Disease Control, 1600 Clifton Rd., Atlanta, GA 30333.
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GIANGUGLIELMO ZEHENDER, LUCA MERONI, STEFANIA PICONI, CHIARA DE MADDALENA, CARLO PARRAVICINI, MARIO CLERICI, ANNA L. RIDOLFO, MAURO MORONI, MASSIMO GALLI. (1995) Frequent Detection of Antibodies against HTLV Antigens in Patients with AIDS-Related Non-Hodgkin Lymphoma. AIDS Research and Human Retroviruses 11:7, 823-827
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S. MAAYAN, E. N. SHUFMAN, D. ENGELHARD, D. SHOUVAL. (1994) Exposure to hepatitis B and C and to HTLV-1 and 2 among Israeli drug abusers in Jerusalem. Addiction 89:7, 869-874
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EDUARDO DUEÑAS-BARAJAS, JAIME E. BERNAL, DIHANNA R. VAUGHT, IGNACIO BRICEÑO, CLEMENCIA DURÁN, RICHARD YANAGIHARA, D. CARLETON GAJDUSEK. (1992) Coexistence of Human T-Lymphotropic Virus Types I and II Among the Wayuu Indians from the Guajira Region of Colombia. AIDS Research and Human Retroviruses 8:11, 1851-1855
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