Original Article
Clinical Manifestations and Predictors of Disease Progression in Drug Users with Human Immunodeficiency Virus Infection
N Engl J Med 1992; 327:1697-1703December 10, 1992
- Abstract
- Abstract
Background and Methods.
To examine the clinical course of human immunodeficiency virus (HIV) infection in injection-drug users, we conducted a prospective study of a cohort of patients in a methadone-treatment program in New York City from July 1985 through December 1990. The patients underwent standardized evaluations at base line and semiannually thereafter and received on-site primary medical care. Rates of progression to the acquired immunodeficiency syndrome (AIDS) and major outcomes before the development of AIDS were examined by univariate analyses; the risk of AIDS was also assessed by product-limit survival analysis and proportional-hazards regression.
Results.
Of 318 HIV-seropositive patients who did not yet have AIDS (171 men and 147 women), 90 were black, 179 were Hispanic, and 49 were white; the median age was 33 years. Over a median of 3.0 years of follow-up, 55 (17 percent) received a diagnosis of AIDS (incidence per 100 person-years, 5.8). Major outcomes before the development of AIDS included oral candidiasis (incidence per 100 person-years, 11.2), pyogenic bacterial infections including pneumonia and sepsis (8.0), pulmonary tuberculosis (1.2), multiple constitutional symptoms (13.6), and herpes zoster (1.3). There were 41 deaths from AIDS, and 13 seropositive patients without AIDS (4.1 percent) died of bacterial infections, as compared with only 1 of 411 seronegative patients studied (P<0.001). The incidence of AIDS was 62 percent lower among those who took zidovudine than among those who did not (P = 0.02). In the multivariate analysis, progression to AIDS was best predicted by low numbers and percentages of CD4+ lymphocytes, nonuse of zidovudine, and the presence of oral candidiasis, bacterial infections, or tuberculosis. There was no consistent relation between progression to disease and the continued use of injection drugs.
Conclusions.
HIV-infected injection-drug users have progression to AIDS at rates comparable to those of other HIV-infected groups, but they have substantial pre-AIDS morbidity and mortality, particularly from bacterial infections, which also appear to predict disease progression. (N Engl J Med 1992;327:1697–703.)
Media in This Article
Figure 1
Cumulative Proportion of Patients Remaining AIDS-free during Follow-up after Their First CD4+ Cell Count of ≤500 Cells per Cubic Millimeter, According to Zidovudine Use during Follow-up.Table 1
Demographic Characteristics and Progression to AIDS in 318 HIV-Seropositive Injection-Drug Users.Article Activity
- Article
INJECTION-DRUG users account for an increasing proportion of the cases of human immunodeficiency virus (HIV) infection and the acquired immunodeficiency syndrome (AIDS) in North America, Europe, and certain regions of the developing world.1 2 3 4 Given the key role of injection-drug users in the AIDS epidemic, an understanding of the natural history and clinical course of HIV infection in such persons is of great importance. Most reported prospective studies of the natural history of HIV infection, however, have been conducted among homosexual men, patients with hemophilia, and transfusion recipients.5 6 7 8 9 10 11
The few published prospective studies of HIV infection among drug users have not focused on the specific clinical manifestations of disease, which may differ from those seen in other populations.12 13 14 15 16 17 18 19 20 Prognostic markers for the progression of HIV disease, which are increasingly important in therapeutic decision making, have also been derived largely from other populations and must be examined further among drug users.5 6 7 8 9 , 14 15 16 , 21 22 23 24 25 26 In addition, the demographic, clinical, and behavioral variables that may influence the rate of progression of HIV disease have not been fully assessed in studies of injection-drug users.12 , 13 , 15 , 27 28 29 30 31 More information is also needed about the effects of HIV-related therapy in this population.
To address these questions, we have been conducting an ongoing prospective study of HIV infection among participants in a methadone-maintenance program in New York City.32 33 34 35 36 This report analyzes the clinical manifestations of HIV infection, the rates and predictors of disease progression, and the effect of preventive medical interventions in this cohort over the first six years of observation.
Methods
Study Setting and Design
Starting in mid-1985, as described elsewhere,32 33 34 current and former injection-drug users were recruited for the study at a hospital-affiliated methadone-maintenance program in the Bronx, New York. After providing informed consent, the patients underwent a standardized interview about their drug use, medical history, and any current clinical symptoms. Physical examinations were performed, and blood specimens were obtained. Reevaluations were scheduled every six months. Laboratory tests performed according to the study protocol included serum HIV-antibody testing by enzyme immunoassay with confirmation by the Western blot assay (Abbott, Chicago, from 1985 through 1987; Dupont, Wilmington, Del., from 1988 through 1990); complete blood counts and studies of lymphocyte subgroups (Centers for Disease Control and Prevention [CDCP], Atlanta, from 1986 through 1988; New York Blood Center, New York, in 1989 and 1990); and determinations of serum β2-microglobulin (Pharmacia, Uppsala, Sweden) and p24 antigen (Coulter, Hialeah, Fla.).
Outcome Surveillance and Definitions
Disease outcomes were identified by active surveillance that integrated clinical data with information obtained during formal research visits.35 All the patients received primary medical care at the methadone program37; hospitalizations were routinely monitored and hospital records reviewed. Surveillance was facilitated by the requirement that hospitals must contact the methadone program for authorization to provide methadone for program clients. Clinical diagnoses made in the course of visits for research or medical care were abstracted, as were data on zidovudine use and antipneumocystis prophylaxis. When patients left the methadone program, members of the research staff maintained contact in order to enhance their retention in the study and follow-up.38 The tracking of patients was expedited by confidential verification of their status in the vital records and AIDS registries of the New York City Department of Health and by periodic queries through the National Death Index.
This report principally concerns the follow-up of the HIV-seropositive patients in the cohort, except for the analysis of mortality, which compares the seropositive and the seronegative groups. For the HIV-seropositive patients, we calculated incidence rates for AIDS and other specified HIV-related disease outcomes preceding a diagnosis of AIDS.33 , 34 , 39 40 41 42 These outcomes included oral candidiasis, a single episode of bacterial pneumonia or sepsis, pulmonary tuberculosis, herpes zoster, and the presence of two or more of the following constitutional symptoms: unintended weight loss of more than 5 lb (2.3 kg), unexplained fever of more than two weeks' duration, and diarrhea of more than two weeks' duration.
In making a diagnosis of AIDS, we used the definition formulated by the CDCP, as revised in 1987.40 All AIDS diagnoses and deaths were confirmed by a review of the hospital, clinic, or autopsy records or a review of the death certificates. Diagnoses of disease outcomes other than AIDS were confirmed with standardized diagnostic criteria and case definitions33 , 34 and were included in the analysis only when they predated any AIDS diagnosis. Similarly, deaths were attributed to causes other than AIDS only if they preceded any AIDS-defining diagnosis.
Follow-up
The follow-up period began with enrollment in the study or the first positive HIV-antibody test of serum, whichever came later. Patients who were enrolled in the study from July 1, 1985, through December 31, 1989, were eligible for inclusion; the follow-up period for this analysis ended on December 31, 1990. Preliminary analyses showed that the intensity of surveillance for certain disease outcomes decreased among patients leaving the methadone program during the study period. Therefore, for such patients, the follow-up period used in the study of mortality ended on December 31, 1990; in the study of AIDS, it ended one year after departure from the methadone program; and in the study of other HIV-related outcomes, it ended one week after departure.
Because indicators of compliance with zidovudine therapy and antipneumocystis prophylaxis were not systematically available, an intention-to-treat analysis was used, based on the clinic records. The group that did not receive either therapy included both patients who declined treatment and those followed during the first several years of the study, before these treatments became available. In this analysis, medication use was considered to begin with the start of the first period in which the medication was prescribed for more than 30 days, and time was accrued continuously.
Statistical Analysis
In the comparisons of disease risk, relative risk was estimated with ratios of incidence rates per 100 person-years, with the chi-square statistic based on the normal approximation to the binomial.43 Intervals before the progression to AIDS were compared by constructing product-limit estimates of the percentage of patients remaining AIDS-free; differences were tested by the MantelHaenszel log-rank test.
Multivariate analysis was conducted with proportional-hazards (Cox) regression, with Egret software (Statistics and Epidemiology Research, Seattle). All the regression models were constructed to take into account a number of observations per person, and thus they were able to accommodate covariates that varied with time. Modeling was carried out by adding categorized covariates to the model one at a time and examining the likelihood-ratio statistic (i.e., twice the change in the model log likelihood), the overall model likelihood, and the effect of the addition of covariates on the coefficients and Wald's statistics for variables already included in the model. The criteria for inclusion were a likelihood-ratio statistic ≥3.5 or a 5 percent change in one or more of the other variables. Zidovudine use was included as a control variable in all models that contained clinical criteria or conditions.
Results
Characteristics of the Population
A total of 731 patients were enrolled in the study. Of these, 532 (73 percent) were enrolled in 1985 or 1986, and 199 (27 percent) were enrolled from 1987 through 1989. The median follow-up in the methadone program for the overall group was 3.0 years (range, 2 weeks to 5.5 years). The study participants did not differ from the nonparticipants enrolled in the methadone program with respect to demographic variables or length of time receiving methadone treatment.32 33 34
Of the 731 patients, 306 (42 percent) were HIV-seropositive at entry; 14 of the 425 remaining patients (3 percent) subsequently seroconverted. Two patients who had AIDS at the time of enrollment were excluded from the study, leaving 318 seropositive patients. At the initial evaluation, 27 of these (8 percent) had documented oral candidiasis. By the end of the study period, 200 of the 318 patients (63 percent) either had remained in the methadone program continuously or had left the program and were known to have later received a diagnosis of AIDS or to have died; 118 patients (37 percent) had left the methadone program without subsequent AIDS diagnoses or deaths identified through the study surveillance. Table 1Table 1
Demographic Characteristics and Progression to AIDS in 318 HIV-Seropositive Injection-Drug Users. shows selected demographic characteristics of the sample.Incidence of AIDS
Fifty-five of the 318 HIV-seropositive patients (17 percent) went on to have AIDS during the study (5.8 cases per 100 person-years). The incidence rates of AIDS rose with increasing age at entry into the study; these rates did not differ according to either sex or racial or ethnic group (Table 1). Patients who reported engaging in daily drug injection during at least one six-month period of follow-up did not have incidence rates of AIDS that were significantly different from those of patients who used drugs less frequently or not at all. The most common AIDS-defining illness was Pneumocystis carinii pneumonia, seen in 23 of the 55 patients (42 percent); the other AIDS-defining illnesses are shown in Table 1.
Mortality Rates
The crude mortality rate in the HIV-seropositive patients was 6.0 deaths per 100 person-years, as compared with 1.6 deaths per 100 person-years in the HIV-seronegative patients (P<0.001, by the exact test for person-time) (Tables 2Table 2
Overall Mortality among HIV-Seropositive and HIV-Seronegative Injection-Drug Users. and 3Table 3
Cause-Specific Mortality among HIV-Seropositive and HIV-Seronegative Injection-Drug Users.). Of 72 deaths among the seropositive patients, 41 (57 percent) were due to AIDS, and 13 (18 percent) were due to bacterial pneumonia or sepsis in the patients without AIDS. The death rate from bacterial pneumonia and sepsis was significantly higher in the seropositive patients than in the seronegative patients (P<0.001). The death rates for cirrhosis or liver failure, drug overdose, trauma, and other causes did not differ significantly according to HIV serologic status.AIDS and Major Outcomes before AIDS
Table 4Table 4
Incidence of AIDS and Other Diseases before the Development of AIDS in HIV-Seropositive Patients, According to Base-Line CD4+ Cell Count. shows the incidence rates of AIDS and six major outcomes preceding the development of AIDS among the HIV-seropositive patients, both overall and as stratified according to CD4+ T-lymphocyte count at base line. The incidence of any disease outcome before the development of AIDS was 24.1 events per 100 person-years, approximately four times the incidence rate of AIDS. The increased rate of progression to AIDS in patients with base-line CD4+ counts of 200 or fewer cells per cubic millimeter (17.6 cases per 100 person-years) was observed entirely among the patients with base-line CD4+ counts of 150 or fewer cells per cubic millimeter; the rate of progression to AIDS in patients with 151 to 200 CD4+ cells per cubic millimeter did not differ from that in patients with base-line counts ranging from 201 to 500 per cubic millimeter. Rates of oral candidiasis, bacterial infections, and pulmonary tuberculosis increased with declining base-line CD4+ counts. Forty-one of 49 cases of bacterial pneumonia (84 percent) were caused by Streptococcus pneumoniae (24 cases) or Haemophilus influenzae (17 cases).The occurrence of certain disease outcomes was analyzed further in relation to CD4+ counts measured in the six months before the diagnosis of disease. For the patients with AIDS, the median CD4+ lymphocyte count within the preceding six months was 137 per cubic millimeter (range, 18 to 911), as compared with 317 per cubic millimeter (range, 8 to 789) for those with bacterial infections, 324 per cubic millimeter (range, 45 to 949) for those with oral candidiasis, 397 per cubic millimeter (range, 91 to 1771) for those with constitutional symptoms, and 408 per cubic millimeter (range, 31 to 1840) for those remaining asymptomatic.
Effects of Zidovudine Therapy on Progression to AIDS
Progression to AIDS was analyzed with regard to zidovudine therapy and antipneumocystis prophylaxis during follow-up. This analysis was limited to patients who had reached either a count of 500 or fewer CD4+ lymphocytes per cubic millimeter with two or more constitutional symptoms or a count of 200 or fewer CD4+ lymphocytes per cubic millimeter regardless of symptoms, at some point during follow-up. Of 116 such patients, 50 (43 percent) received zidovudine; of these, 26 also received antipneumocystis prophylaxis. The rate of progression to AIDS was 62 percent lower in the treated group than in the untreated group (6.6 vs. 17.3 cases per 100 person-years; rate ratio, 0.38; 95 percent confidence interval, 0.16 to 0.90; P = 0.02). Product-limit estimation also indicated that AIDS-free time was significantly prolonged among the patients who received zidovudine (P = 0.01 by MantelHaenszel log-rank test) (Fig. 1Figure 1
Cumulative Proportion of Patients Remaining AIDS-free during Follow-up after Their First CD4+ Cell Count of ≤500 Cells per Cubic Millimeter, According to Zidovudine Use during Follow-up.). The beneficial effects of zidovudine were seen both in patients who used injection drugs during follow-up and in those who did not.Multivariate Analysis of Predictors of AIDS
On the basis of preliminary analyses, three categories of the CD4+ lymphocyte count were used in the final multivariate models: 151 to 500, 51 to 150, and ≤50 per cubic millimeter (reference category, >500 per cubic millimeter), with separate terms representing the additional effect when the percentage of CD4+ lymphocytes among total lymphocytes fell to 5.0 or less in each category of the cell count. Other laboratory markers considered for the model included serum β2-microglobulin, serum p24 antigen, and thrombocyte and leukocyte counts.
In the multivariate analysis, there was no effect on the risk of AIDS with any demographic variable. Increased age was inversely associated with CD4+ lymphocyte count; no association between age and the progression to AIDS was seen once the CD4+ cell count was held constant. There was no independent effect of the rate of decline of the CD4+ count on the risk of AIDS when we controlled for the number of CD4+ cells itself. No additional effect on the risk of AIDS was found for any other laboratory marker, once the CD4+ count was controlled for. In the multivariate analysis, the use of zidovudine was associated with a 63 percent reduction in the risk of progression to AIDS (95 percent confidence interval, 87 percent to -8 percent). Persistent injection of illicit drugs was not associated with progression to AIDS.
A proportional-hazards model was used to examine the relation between CD4+ lymphocyte counts and percentages, disease outcomes other than AIDS, and the risk of progression to AIDS (Table 5Table 5
Proportional-Hazards Model of the Risk of Progression to AIDS, According to Clinical Condition and CD4+ Count.*). In this model, we evaluated the effect on the risk of AIDS of our previously defined clinical conditions other than AIDS, after adjustment for CD4+ count and zidovudine use. The risk of AIDS increased with declining CD4+ counts and was higher in subjects with CD4+ percentages ≤5.0 at any given CD4+ count. Any history of oral candidiasis or serious bacterial infections (including pulmonary tuberculosis) during follow-up independently increased the risk by 5.4 or 3.7 times, respectively. The risk of AIDS in patients with both these conditions was almost 20 times higher with CD4+ counts above 500 per cubic millimeter, and more than 1000 times higher when CD4+ counts were both ≤150 per cubic millimeter and ≤5.0 percent. No other clinical conditions were associated with the risk of AIDS after oral candidiasis and bacterial infections were included in the model.Discussion
This study demonstrates that although injection-drug users with HIV infection share some features with other HIV-infected groups, they have certain distinctive clinical characteristics. The most distinctive was the finding of serious bacterial infections — bacterial pneumonia, sepsis, and tuberculosis — that were important both as predictors of progression to AIDS and as a source of HIV-related morbidity and mortality before AIDS. Our study further shows that in drug users, as in other populations,25 , 44 , 45 , the use of zidovudine is associated with delayed progression of disease and prolonged AIDS-free survival.
Increases in morbidity, mortality, or both that are associated with HIV-related bacterial infections or tuberculosis have now been reported among drug users in the United States and several European countries.18 , 19 , 33 34 35 , 46 47 48 49 In this study, the rate of serious bacterial infections among the HIV-seropositive patients was approximately 40 percent higher than the incidence rate of AIDS, with approximately one death from bacterial infections for every three deaths from AIDS. Measures of the incidence of AIDS alone thus substantially underestimate the burden of disease in this population. The high rate of serious bacterial infections among HIV-infected users of injection drugs significantly exceeds the background rate of such infections among drug users and is higher than that observed in other HIV-infected groups.20 , 33 34 35 , 47 In a previous study in our cohort, this phenomenon was statistically independent of drug injection and the use of alcohol or tobacco.33 Since we included only bacterial infections occurring before the development of AIDS, our study provides a minimal estimate of their impact in this population. Bacterial infections that occur after the diagnoses of AIDS remain an additional important source of morbidity and mortality among drug users and may increase with declining CD4+ counts.20
In HIV-infected patients, pyogenic bacterial infections with encapsulated organisms have been attributed to the adverse effects of HIV infection on humoral immunity and B-cell function as well as to the effects on T lymphocytes.33 , 50 51 52 53 Our analysis of CD4+ counts made near the time of diagnosis indicates that such bacterial infections, though accelerated at CD4+ counts below 200 per cubic millimeter, begin to increase in frequency at a range of CD4+ cells (median, 314 per cubic millimeter) intermediate between the levels seen in patients with AIDS and those seen in asymptomatic subjects. The majority of the cases of bacterial pneumonia were caused by S. pneumoniae and H. influenzae; this suggests the potential importance of both pneumococcal polysaccharide54 and H. influenzae type b vaccines for HIV-infected drug users,55 although current guidelines endorse use of the latter vaccine less clearly.54 Further study is also needed to determine whether prophylactic antibiotic regimens — including, perhaps, trimethoprim–sulfamethoxazole, which many patients receive as prophylaxis for P. carinii pneumonia — might also reduce the risk of serious bacterial infections in HIV-infected drug users.
Another respect in which our population differed from other groups, especially homosexual men, was in the distribution of AIDS-defining illnesses. Thirty-one of the 55 persons with AIDS (56 percent) did not meet the strict diagnostic criteria for the case definition of AIDS used by the CDCP before 1987, including 8 with extrapulmonary tuberculosis. This suggests that the diagnosis of AIDS and the expression of severe immunodeficiency among HIV-infected drug users were substantially underestimated in earlier HIV-classification systems.19 , 49 , 56 , 57
Our study found no difference in rates of progression to AIDS or in the distribution of AIDS-defining illnesses according to sex or racial or ethnic group. Although older age was predictive of the progression to AIDS in the univariate analysis, as in several other reports,6 , 15 , 58 age was not an independent predictor of AIDS in the multivariate analysis. It cannot be determined from this study whether the observation of lower CD4+ cell counts in older patients reflects a true biologic effect or a longer time since primary HIV infection.
Clinical characteristics are powerful predictors of the risk of progression to AIDS in HIV-infected drug users. The strongest clinical predictor was oral candidiasis; a history of bacterial pneumonia, sepsis, or tuberculosis was also predictive, even after oral candidiasis was accounted for. The predictive importance of these conditions was seen for all CD4+ counts, indicating that these entities have prognostic implications independent of CD4+ cell levels. Oral candidiasis has long been known to predict progression to AIDS7 , 8 , 59; to our knowledge, however, no elevated risk with bacterial infections or tuberculosis has previously been found among drug users. Further study is needed to explore the possible pathophysiologic basis for this observation.
As in other populations,5 , 7 , 8 , 12 , 14 , 15 , 22 23 24 the number and percentage of CD4+ lymphocytes were the most powerful laboratory markers predicting progression to AIDS. In this cohort, a threshold level of 150 CD4+ lymphocytes per cubic millimeter was found to be especially predictive of an increased risk of AIDS. No other laboratory markers were independent predictors of AIDS, once the CD4+ count was taken into account. In contrast to findings in homosexual men,21 , 22 serum β2-microglobulin was not an independent predictor of AIDS in our population, an observation supported by a recent study of users of injection drugs in Baltimore.12
This study shows that zidovudine use was associated with a slowing of the progression to AIDS, a finding that has not previously been reported in an observational study with a large sample of drug users. These results highlight the critical importance of strategies to provide effective HIV-related care for drug users, who at present are less likely to receive such care than other populations.60 61 62 HIV-infected drug users have readily accepted primary medical care services in the setting of our methadone program.37 The development of such services is also urgently needed for drug users not enrolled in drug-treatment programs.
This analysis was not intended to examine in detail the relation between illicit-drug injection and the progression of HIV disease, although according to simple bivariate and multivariate analyses daily users of injection drugs were not at a higher risk of progression to AIDS than those who used injection drugs less frequently or not at all. Although there is continuing uncertainty about the hypothesis of drug-related acceleration of HIV disease,12 , 13 , 15 , 27 28 29 30 31 , 63 it may be more relevant to consider the potential adverse effects of drug abuse on the receipt of HIV-related medical care. Active drug users may be less likely than other people to receive primary medical care services and thus to benefit from HIV-related interventions.37 , 64 With the growing number of injection-drug users in the worldwide AIDS epidemic, it will be essential to develop comprehensive strategies to address the interconnected needs for medical care, drug treatment, adequate housing, and other social services in this high-risk population.65
Supported in part by a cooperative agreement (U64CCU200714) with the Centers for Disease Control and Prevention and by a grant (DAO4347–05) from the National Institute on Drug Abuse and a grant from the Aaron Diamond Foundation.
We are indebted to Charles Parker, Susan Tozzi, Jeffrey Gates, Amparo Bernal, Rose Rivera, Andrea Gachupin-Garcia, Sara McLaughlin, Nancy Budner, and Gail Green for their important contributions, and to the patients and staff of the Drug Abuse Treatment Program. This paper is dedicated to the memory of our valued friend and colleague, Jeffrey R. Gates, R.N.
Source Information
From the Department of Epidemiology and Social Medicine (P.A.S., P.A., D.H., D.B., E.E.S., R.S.K., K.D., G.H.F.) and the Department of Internal Medicine (E.E.S., R.S.K., K.D., G.H.F.), Division of Infectious Diseases, Montefiore Medical Center, Albert Einstein College of Medicine, Bronx, N.Y. Address reprint requests to Dr. Selwyn at the AIDS Program, Yale–New Haven Hospital, Yale University School of Medicine, 20 York St., New Haven, CT 06504.
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