Original Article
The Prognostic Value of Cellular and Serologic Markers in Infection with Human Immunodeficiency Virus Type 1
N Engl J Med 1990; 322:166-172January 18, 1990DOI: 10.1056/NEJM199001183220305
- Abstract
- Abstract
We evaluated three cellular and five serologic markers that are affected by infection with the human immunodeficiency virus type 1 (HIV-1 ) for their ability to predict the progression to clinical acquired immunodeficiency syndrome (AIDS). The cellular markers were the number of CD4+ T cells, the number of CD8+ T cells, and the ratio of CD4+ T cells to CD8+ T cells. The serologic markers were the serum levels of neopterin (a product of stimulated macrophages), beta2-microglobulin, soluble interleukin-2 receptors, IgA, and HIV p24 antigen. We evaluated the usefulness of these measures as markers of the progression to AIDS prospectively, over four years, in a cohort of 395 HIV-seropositive homosexual men who were initially free of AIDS.
CD4+ T cells (expressed as an absolute number, a percentage of lymphocytes, or a ratio of CD4+ to CD8+ T cells) were the best single predictor of the progression to AIDS, but the serum neopterin and beta2-microglobulin levels each had nearly as much predictive power. The neopterin level appeared to be a slightly better predictor than the beta2-microglobulin level. The levels of IgA, interleukin-2 receptors, and p24 antigen had less predictive value. A stepwise multivariate analysis indicated that the best predictors, in descending order, were CD4+ T cells (the percentage of lymphocytes or the CD4+: CD8+ ratio), the serum level of neopterin or beta2-microglobulin, the level of IgA, that of interleukin-2 receptors, and that of p24 antigen. The last three markers had little additional predictive power beyond that of the first two.
We conclude that of the eight markers studied, progression to AIDS was predicted most accurately by the level of CD4+ T cells in combination with the serum level of either neopterin or beta2-microglobulin. At least one of these two serum markers, which reflect immune activation, should be used along with measurement of CD4+ T cells in disease-classification schemes and in the evaluation of responses to therapy. (N Engl J Med 1990; 322:166–72.)
Article Activity
- Article
THE identification of factors that correlate with, and possibly contribute to, the outcome of infection with the human immunodeficiency virus (HIV) is important for our understanding of the pathogenesis and natural history of HIV infection and in designing therapeutic trials. Weighing the relative contribution of such factors is also important.
It was recognized early that CD4+ T cells are the main targets of HIV infection and that a substantial reduction in the number of CD4+ T cells is required for the development of AIDS.1 , 2 Several epidemiologic studies have confirmed the importance of reductions in the number of CD4+ T cells and have contributed quantitative data on the relation of the level of CD4+ T cells to AIDS.3 4 5 6 7 8 Impairments in T-cell function —for instance, impaired T-cell proliferation, production of interleukin-2, and expression of interleukin-2 receptors9 10 11 12 — also occur.
Activation of immune cells is also evident in HIV infection, notably in the population of CD8+ T cells,13 14 15 and evidence of activation has been found in B cells as well.16 , 17 Studies of CD8+ T cells and B cells have emphasized the broad scope of immune activation by HIV infection. The association of these changes with clinical outcome has not been evaluated, however.
We chose to study four soluble products of immunecell activation that are readily measured in serum — neopterin, soluble interleukin-2 receptors, IgA, and beta2-microglobulin — and HIV p24 antigen, a measure of viral activity. Neopterin, a metabolite of guanosine triphosphate, is produced by macrophages when they are stimulated by interferon gamma from activated T cells.18 The level of soluble interleukin-2 receptors reflects the activation of T cells, and the number of CD8+ T cells reflects the stimulation of that population. The level of IgA reflects B-cell activation, and that of beta2-microglobulin reflects lymphoid activation more generally. Serum and urinary neopterin levels have been shown in several studies to be elevated in patients with HIV infection and to correlate well with prognosis.19 20 21 Elevation of neopterin levels is at least partly independent of changes in CD4+ T cells. Furthermore, the combination of CD4+ T-cell and neopterin measurements is a better indicator of prognosis than either used alone.21 Beta2-microglobulin levels are also elevated in HIV infection, and in seropositive homosexual men the serum beta2-microglobulin level is strongly correlated with the risk of progression to AIDS.22 23 24 The level of soluble interleukin-2 receptors is elevated in patients with HIV infection, as well, and preliminary data suggest a good correlation with the disease stage as indicated by the CD4+ T-cell level.25 Serum levels of IgA may also be elevated in HIV infection and have been found to be related to prognosis.8 Serum levels of p24 antigen were included in this study as a separate marker of HIV activity. The presence of detectable p24 in serum has been shown to be associated with a poor prognosis.26 , 27 The presence of detectable HIV antigen in serum is presumed to indicate increased viral production.
In addition to these five markers, we examined three serologic measures of T-cell changes: the level (number and percentage) of CD4+ T cells, the number of CD8+ T cells, and the ratio of CD4+ to CD8+ T cells. In a previous study of the usefulness of the number and percentage of CD4+ T cells and the CD4+:CD8+ ratio in predicting the development of AIDS in HIV-seropositive homosexual men,28 all three measures were found to be useful as markers of the progression to AIDS at one, two, and three years of follow-up. The percentage of CD4+ T cells, however, had slightly greater prognostic value and was less variable on repeated measurements. The percentage of CD4+ T cells is obtained directly from flow-cytometric measurements and does not have the complications of variability that result from the need to use total white-cell and differential white-cell counts in calculating the number of CD4+ T cells.
We evaluated the relation of these eight measures to prognosis, both separately and in combination, in a prospective study of 395 HIV-seropositive homosexual men whom we examined and followed up for three or more years to identify the development of AIDS.
Methods
Subjects
A random sample of 400 men was selected from the 813 HIV-seropositive homosexual men enrolled at the Los Angeles center in the Multicenter AIDS Cohort Study. Five of the participants had missing values for one or more of the serum markers under consideration. All analyses reported here are based on the 395 men for whom complete data were available. These men (median age, 33 years) were followed up at six-month intervals for four years or until they received the diagnosis of AIDS. At three years, 82 percent were still being followed up; the median duration of follow-up was 45 months (5th percentile, 8 months; 95th percentile, 44 months). During the follow-up period, 84 of the men were known to have been given a diagnosis of AIDS. Blood samples were obtained at entry in 1984 and at all follow-up visits, and serum was separated and stored. Measurements of T-cell subsets were made in the fresh blood samples. Details of recruitment for the Multicenter AIDS Cohort Study, the characteristics of the cohort at base line, and the changes in levels of CD4+ T cells have been published elsewhere.29 , 30 Seropositive status was determined by enzyme-linked immunosorbent assay (Genetic Systems, Seattle) and confirmed by Western blot analysis.31 A sample of 46 homosexual men who were seronegative throughout the period of observation was used as a reference group.32
Measurement of Lymphocyte Subsets
Whole-blood samples drawn in tubes containing EDTA were stained with monoclonal antibodies and the percentages of CD3+, CD4+, and CD8+ T cells in peripheral-blood lymphocytes were determined by flow-cytometric procedures. The numbers of CD4+ and CD8+ T cells were determined by obtaining total and differential white-cell counts and multiplying by the appropriate factor obtained on flow cytometry.
Betaj-Microglobulin Assay
Beta2-microglobulin was measured by radioimmunoassay (Pharmacia, Uppsala, Sweden) with use of standards provided by the manufacturer.23
Neopterin Assay
Neopterin, which is a pyrazinopyrimidine derivative, was measured by radioimmunoassay (Neopterin–RIAcid, Henning, Berlin, Germany) purchased from DRG International (Mountainside, N.J.).
Assay for Soluble Interleukin-2 Receptors
Soluble interleukin-2 receptors were measured by enzyme-linked immunosorbent assay according to methods similar to those used by Prince et al.,25 with an anti–interleukin-2 receptor capture antibody (L54-P98, Becton Dickinson, Mountain View, Calif.) and dilutions of a standard for soluble interleukin-2 receptors (4000 U per milliliter, Becton Dickinson) and peroxidase-coupled secondary anti–soluble interleukin-2–receptor antibody (2AB, Becton Dickinson). Data are expressed in units.25
IgA Assay
FIAX StiQ (M.A. Bioproducts, Walkersville, Md.) coated with immunosorbents was used to bind IgA and then immersed in fluorescein isothiocyanate–labeled goat antihuman immunoglobulin specific for IgA, and the fluorescence of the bound antibodies was measured. IgA levels were interpolated from a standard curve.
Detection of HIV p24 Antigen
We measured p24 antigen with a commercial solid-phase enzyme immunoassay (Dupont, NEN Research Products, Wilmington, Del.).33 The concentrations of p24 antigen present in serum samples were interpolated from a standard curve.
Statistical Analysis
Kaplan–Meier plots34 were used to illustrate the distributions of AIDS-free time for different groups of patients, stratified according to the values of covariates at enrollment. The maximized log-likelihoods from the proportional-hazards model35 were used to assess the predictive value of the covariates, singly and in combination, when the covariates were treated as continuous variables. A stepwise proportional-hazards model was used to determine the relative importance of the covariates in predicting the progression to AIDS. The logarithms of all the covariates except p24 antigen and IgA were used in the analysis. The coefficients of the best-fitting equations (see Results) were rescaled so that the coefficient of the number of CD4+ T cells would be 1. Pairwise interactions between covariates were considered by including in the model the product of two covariates as an additional explanatory variable. The relative hazards from the model were used to quantify the effects of the covariates when the subjects were divided into four groups on the basis of the covariates.
The comparison among the indexes used as markers is illustrated by dividing the 395 participants into four groups with sample sizes of 220, 100, 50, and 25 for all the markers. The actual group in which each patient was placed depended on the marker under consideration. The group of 25 patients comprised those with the most abnormal values for a given marker, the group of 220 patients had the least abnormal values, and the groups of 50 and 100 patients had intermediate values. (The definitions of the groups for each marker are shown in Table 2Table 2
Relative-Hazard Characteristics According to Patient Groups for Each Marker.*.) The exact choice of group sizes was arbitrary, but the aim was to emphasize the extremes of the levels of each marker with the smaller samples. In addition, it was necessary to use the same sized groups for different markers. A more complete description of the rationale for this approach is presented by Taylor et al.28 When the covariates were considered in combination, a score for each participant could be calculated from the best-fitting linear combination of covariates obtained from the proportional-hazards model. Then each patient was classified in one of four groups according to this score.The correlation between variables was assessed with use of Spearman's rank-correlation coefficient.
Results
Table 1Table 1
Levels of Cellular and serologic Markers in Asymptomatic HIV-Seropositive and HIV-Seronegative Homosexual Men.* shows the results of measurements of three cellular and five serologic indicators that are altered by HIV infection in 395 HIV-seropositive men who were initially free of AIDS and 46 HIV-seronegative homosexual men. The cellular measures are the absolute number and the percentage of CD4+ T cells, the number of CD8+ T cells, and the ratio of CD4+ to CD8+ T cells. The serum measures are the levels of neopterin, beta-2-microglobulin, soluble interleukin-2 receptors, IgA, and HIV p24 antigen. The percentages of HIV-seropositive men with values outside the 10th-to-90th-percentile range for heterosexual men are also indicated (Table 1). The measures with values outside the normal range, in order of frequency, were the CD4+:CD8+ ratio, the percentage of CD4+ cells, the number of CD8+ cells, and the serum neopterin level.Predictive Value of Individual Immune Indexes
The relation of AIDS to various levels of each of the indexes at study enrollment is illustrated in Kaplan–Meier plots of the frequency of the development of AIDS (Fig. 1Figure 1
Kaplan–Meier Plots of the Proportion without AIDS of 395 Homosexual Men in Whom the Number of CD4+ T Cells (A), the Percentage of CD4+ T Cells in Total Lymphocytes (B), the Number of CD8+ T Cells (C), and the Ratio of CD4+ to CD8+ T Cells (D) Were Measured. and 2Figure 2
Kaplan–Meier Plots for Serum Neopterin Level (A), Serum Beta2-Microglobulin Level (B), Serum p24 Antigen Level (C), and Serum IgA Level (D).). Additional data, including the range of values for each measure, the relative hazard for each of the four patient groups, and the maximized log-likelihood obtained from the proportional-hazards model, are presented in Table 2.On the basis of the results of each measurement, the patients were divided into four groups, from those with the most abnormal values to those with the most normal (Fig. 1 and 2). In this context, the group with the levels nearest those of the reference population (the group of 220 patients), which included 56 percent of the men, was defined as having a relative hazard of having AIDS of 1.0 (there was a low incidence of AIDS in this group, as is evident in all parts of Fig. 1 through 3Figure 3
Kaplan–Meier Plots for the Best Linear Combination of Covariates, Combining the Number of CD4+ T Cells and the Serum Neopterin Level (A) and the Number of CD4+ T Cells and the Serum Levels of Neopterin, Soluble Interleukin-2 Receptors (SIL-2R), and p24 Antigen.). Thus, these calculations emphasize the importance of using different levels for each marker and the relative hazard of progression to AIDS within the indicated levels.All measurements of CD4+ T cells had a strong association with subsequent progression to AIDS (Table 2). The ratio of CD4+ to CD8+ T cells may be slightly more useful as a predictor than the percentage or number of CD4+ cells. Levels of CD8+ T cells have little predictive value.
The serum neopterin level is also a strong predictor of the progression to AIDS (Table 2), followed — in descending order — by the serum levels of beta2-microglobulin, IgA, and soluble interleukin-2 receptors. The presence of HIV p24 antigen in serum could be detected in only 12 percent of the patients. However, the presence of p24 antigen was associated with a poor prognosis.
Correlations between Variables
Comparisons were made to determine whether the changes in the variables correlated closely with each other (Table 3Table 3
Correlations among Markers in 395 HIV-Seropositive Men.). As expected, the several ways of measuring CD4+ T cells correlated well with each other, especially the CD4+:CD8+ ratio and the percentage of CD4+ cells in total lymphocytes (since the ratio was calculated from the percentages). Absolute numbers correlated less well because the total and differential white-cell counts necessary to determine absolute numbers of cells are widely variable. Changes in the neopterin and beta2-microglobulin levels correlated well with each other but not quite so well with changes in measurements of CD4+ T cells. This finding is consistent with the view that these markers reflect different aspects of the pathologic process in HIV infection.Combined Predictive Value
The evidence described above indicates that several of the serum markers are independent of the measures of CD4+ cells (and of each other). For this reason, combinations of one or more serum markers with the measures of CD4+ T cells (number, percentage, or ratio) were also assessed in a stepwise manner with the proportional-hazards model. The relative-hazard ratios for the four groups of patients according to various combinations of markers are given in Table 4Table 4
Multivariate Analyses of the Relation of Markers to the Progression to AIDS.*.The combination of the serum neopterin level with measurements of CD4+ T cells had a substantially greater prognostic value than either used alone. The AIDS-free survival of the patients in the four groups is shown in Kaplan–Meier graphs in Figure 3A, and the results for combinations of covariates are shown in Table 4. The equation for the best linear combination of markers for predicting AIDS — the number of CD4+ T cells and the neopterin level — is log(CD4+ number) − 1.07 log(neopterin). The analogous equation for beta2-microglobulin is log(CD4+ number) − 0.83 log(beta2-microglobulin), and that for p24 antigen is log(CD4+ number) − 0.49 p24 antigen. The three cutoff points that defined the four patient groups in the equations shown above were 2.31, 2.87, and 3.45 for CD4+ number and neopterin level; 4.78, 5.19, and 5.73 for CD4+ number and beta2-microglobulin level; and 5.31, 5.75, and 6.17 for CD4+ and p24 antigen. Interactions between the number of CD4+ cells and the level of neopterin, beta2-microglobulin, or p24 antigen were not statistically significant.
Multivariate stepwise analyses indicated that the best predictors of progression to AIDS were, in descending order, the CD4+:CD8+ ratio, the neopterin level, IgA level, level of soluble interleukin-2 receptors, and p24 antigen level; this analysis provided even greater definition of hazard (Table 4 and Fig. 3B). If the percentage of CD4+ T cells was specified first, the remaining measures emerged in the following, descending order of usefulness: the neopterin level, level of soluble interleukin-2 receptors, IgA level, and p24 antigen level. If the number of CD4+ T cells was specified first, the order was as follows: the level of soluble interleukin-2 receptors, IgA level, neopterin level, and p24 antigen level. For all these models, the P value associated with all the markers except p24 antigen was less than 0.05; for p24 antigen the P value was between 0.05 and 0.10. The beta2-microglobulin level does not appear in the models, because the beta2-microglobulin and neopterin levels are strongly correlated. The selection of neopterin (which has slightly greater prognostic value) leaves the beta2-microglobulin level without additional predictive power. The equation for the best linear combination of these five measures is log(CD4+ number) − 1.26 log(neopterin) − 0.72 log(soluble interleukin-2 receptors) − 0.0030 IgA − 0.64 p24. In practical terms, however, the increased separation between the curves and hazard ratios for five measures as compared with two is of marginal significance.
Discussion
This study was undertaken to determine whether the use of eight cellular and serologic indexes as markers of different aspects of the immune-system response to HIV infection could improve the prediction of the course of HIV infection and the development of AIDS. This was, indeed, the case. Furthermore, we found that these markers had different degrees of usefulness in predicting prognosis, and that the most important elements were decreased numbers of CD4+ T cells and increased levels of serum neopterin or beta2-microglobulin. Interestingly, two products of immune stimulation — increased serum levels of beta2-microglobulin and neopterin — reflect the prognosis for the development of AIDS almost or equally as well as the reductions in the number of CD4+ T cells.
These findings indicate the importance of both immune deficits (decreased numbers of CD4+ T cells) and immune stimulation (as reflected by increased levels of neopterin, beta2-microglobulin, soluble interleukin-2 receptors, and IgA) in predicting prognosis. Immune stimulation occurs very early in HIV infection, and evidence of it can be found in the first serum samples that demonstrate seroconversion (HIV antibody).21 , 24 Not only does a specific immune response (antibody) occur, but general immune stimulation also occurs that can be seen in increases in the numbers of CD8+ T cells1 , 2 and in serum levels of soluble interleukin-2 receptors,25 IgA,8 beta2-microglobulin,22 23 24 and neopterin.19 20 21
The mechanisms for these increases are not fully understood. Interferon gamma, however, induces the production of neopterin in vitro.18 The increased production of interferon gamma in HIV infection is likely to be the immediate cause of the increased neopterin level. Whether this or other mechanisms are responsible for the elevated levels of beta2-microglobulin and soluble interleukin-2 receptors is under investigation. Increased production of interleukin-6 has recently been demonstrated in HIV infection36; since interleukin-6 stimulates the production of immunoglobulin by B cells, this increase may account for the elevated serum IgA levels. Detectable serum levels of HIV p24 antigen may also reflect lymphokine stimulation, since mitogen-induced lymphokine production and cellular proliferation are associated with increased production of HIV.37
Although HIV antigenemia is associated with the progression of the disease,26 , 27 p24 antigen is generally not detectable in the serum of 85 percent or more of asymptomatic HIV-seropositive men. Furthermore, it is undetectable in a considerable number of patients with the AIDS-related complex or AIDS. Thus, the clinical usefulness of routine testing for this marker has been questioned.38 Not surprisingly, HIV p24 antigenemia was found to be a minor contributor to predicting prognosis in the present study.
The markers of immune stimulation, neopterin and beta2-microglobulin, are of special interest because recent studies have demonstrated that they can predict the future rate of decrease in CD4+ T cells for at least two or three years.21 , 24 Also, beta2-microglobulin and neopterin levels were shown to have predictive value at normal, intermediate, or markedly reduced levels of CD4+ T cells. This finding indicates that their usefulness is not restricted to portions of the course of HIV infection.
The serologic tests have the advantage of being relatively inexpensive, and serum can be stored for convenient testing. Tests for beta2-microglobulin and IgA are widely available, and tests for serum neopterin could be. In our experience, the variability of the serum measurements on repeated testing of the same patients is less than that for numbers of CD4+ T cells.
The serum markers reflect major immunologic consequences of HIV infection; their measurement should thus be valuable in evaluating antiviral therapy. Furthermore, the serum markers are compounds with relatively rapid turnover, so that changes in HIV activity induced by therapy may be detected more rapidly and with greater accuracy with these markers than by relying solely on changes in the levels of CD4+ T cells or patient survival. Incorporation of suitable serum markers in clinical trials could facilitate the evaluation of more antiviral drugs and schedules of administration. Also, decisions about counseling and support for patients and their families already rely on measurements of CD4+ T cell levels. Thus, the serum immune-activation markers, in conjunction with measurements of CD4+ T cells, can provide valuable data for the management of HIV infection and AIDS as well as for the understanding of their pathogenesis, prognosis, and treatment.
Supported by grants from the National Institutes of Health (AI-23606, AI15332, AI-72631, and CA-16042), the Danish Cancer Society (to Dr. Hofmann), and the Psychoneuroimmunology Program at UCLA (to Dr. Melmed).
We are indebted to many persons who participated in this study, including Imu Esmail, Mehran Bozorgmehri, Alex Rezai, Najibullah Aziz, Hripi Nishanian, Susan Stehn, Diana Liao, and the members of the Flow Cytometry Laboratory of the Center for Interdisciplinary Research in Immunology and Disease and the Multicenter AIDS Cohort Study Clinical Study Group at the University of California at Los Angeles; Drs. Anne Jackson and Noel Warner of Becton Dickinson, who generously provided reagents for the assays of soluble interleukin-2 receptors; and Karen Hogan-Lane, who provided valuable assistance in the preparation of reports and the manuscript.
Source Information
From the Center for Interdisciplinary Research in Immunology and Disease, Jonsson Comprehensive Cancer Center, UCLA School of Medicine (J.L.F., B.H., R.M., P.N., J.V.G.), and UCLA School of Public Health (J.M.G.T., R.D.). Address reprint requests to Dr. Fahey at the Department of Microbiology and Immunology, UCLA School of Medicine, 12–262 Factor Bldg., Los Angeles, CA 90024–1747.
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