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Original Article

Transient High Levels of Viremia in Patients with Primary Human Immunodeficiency Virus Type 1 Infection

Eric S. Daar, M.D., Tarsem Moudgil, M.S., Richard D. Meyer, M.D., and David D. Ho, M.D.

N Engl J Med 1991; 324:961-964April 4, 1991

Abstract
Abstract

Background.

The rapidly evolving clinical picture of primary infection with the human immunodeficiency virus type 1 (HIV-1) suggests that a better understanding of the kinetics of viral replication in vivo during the short period before seroconversion may provide insight into the pathogenesis of the acquired immunodeficiency syndrome (AIDS).

Full Text of Background. ...

Methods and Results.

Titers of infectious HIV-1 were determined by end-point-dilution culture in sequential samples of plasma and peripheral-blood mononuclear cells from four patients with primary infection, with peak titers of 1000 to 10,000 tissue-culture—infective doses per milliliter of plasma and 100 to 10,000 infective doses per 106 peripheral-blood mononuclear cells. The high viral burden in mononuclear cells was confirmed by quantitative studies using a polymerase-chain-reaction method. In as little as 10 days, the high HIV-1 load in both plasma and cells decreased spontaneously and precipitously, at least 100-fold, in all four patients.

Full Text of Methods and Results. ...

Conclusions.

Although p24 core antigenemia and viral isolation have previously been described during primary HIV-1 infection, this report documents the large viral burden during the acute phase of infection. The rapid and spontaneous decline in the viral load suggests an effective immune response in the host that, if understood, may be used to combat AIDS. (N Engl J Med 1991; 324:961–4.)

Full Text of Conclusions. ...

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Article

PRIMARY infection with the human immunodeficiency virus type 1 (HIV-1) associated with seroconversion is most commonly manifested as an acute illness characterized by fever, myalgia, rash, gastrointestinal symptoms, and at times neurologic complications.1 2 3 The period from the onset of illness to seroconversion has ranged from eight days to three months,3 , 4 with virus detectable in the cerebrospinal fluid, peripheral-blood mononuclear cells (PBMC), and plasma before the development of an antibody response.3 , 5 6 7 8 The acute nature of this clinical syndrome and its prompt resolution in one to two weeks suggest that the kinetics of HIV-1 replication in vivo change rapidly. To date, however, no quantitative analysis of the viral burden in primary HIV-1 infection has been performed, although transiently high serum levels of HIV-1 core protein (p24) have been noted.7 , 8 We therefore undertook extensive virologic studies of sequential blood samples obtained from four recent patients with primary HIV-1 infection, using a method of end-point-dilution culture9 and a quantitative technique involving the polymerase chain reaction (PCR).10

Case Reports

Patient 1

Patient 1 was a 34-year-old homosexual man who had been in good health until approximately two weeks before hospitalization, when fever, pharyngitis, fatigue, and cervical lymphadenopathy developed, along with a red macular rash over his face and upper body. He was seen by his private physician, and a throat culture and Monospot test were negative. Treatment with ampicillin resulted in little improvement in his symptoms, and persistent fever, sore throat, and rash led to an infectious-disease consultation one week after the onset of the symptoms. At that time, the patient reported that six weeks before the onset of his illness, he had had his only sexual contact since testing negative for HIV-1 antibodies seven months previously. His peak temperature was 38.9°C (102°F), but his pharynx was not inflamed. The neck was supple, with bilateral lymphadenopathy, and his neurologic examination was completely normal. Blood was obtained for HIV-1 studies because of the possibility of acute infection. On day 9 of the illness, the patient noted the onset of lower-extremity paresthesia and weakness, which rapidly progressed to complete lower-extremity paralysis over the ensuing five days, requiring hospitalization on day 14. A lumbar puncture was performed, and an examination of the cerebrospinal fluid showed 7×106 lymphocytes per liter and an elevated protein level of 2.17 g per liter. Other laboratory studies at that time revealed a leukocyte count of 6.9×109 per liter, with 0.49 granulocyte and 0.47 lymphocyte; a hematocrit of 0.49; an absolute CD4 lymphocyte count of 0.4×109 per liter; and a helper/suppressor lymphocyte ratio of 0.3. A presumptive diagnosis was made of Guillain—Barré syndrome associated with primary HIV-1 infection. Within 36 hours of admission, the patient required mechanical ventilation. Eight courses of plasmapheresis were performed, with a gradual increase in the patient's motor strength. Mechanical ventilation was discontinued on day 31, and the patient was discharged to a rehabilitation facility on day 42. He subsequently regained approximately 80 percent of his motor strength and was otherwise asymptomatic.

Patient 2

Patient 2 was a 30-year-old homosexual man who had been in good health until five days before admission, when a sore throat, fever (temperature to 38.9°C [102°F]), and anorexia developed. On the second day of his illness, myalgia and a facial erythematous papular rash developed. On day 3 the rash extended to his back, upper body, and extremities, prompting his hospitalization for further evaluation. The patient stated that he had never been tested for antibodies to HIV-1 and that his most recent sexual contact had occurred approximately three months previously. His temperature at the time of admission was 38.2°C (100.8°F), and he had a mildly inflamed pharynx and a supple neck without lymphadenopathy. Initial serologic studies were negative for Epstein–Barr virus, cytomegalovirus, syphilis, and hepatitis A and B viruses, as well as HIV-1. His leukocyte count was 4.4×109 per liter. The hemoglobin level was 146 g per liter, and the absolute CD4 lymphocyte count was 0.76×109 per liter, with a helper/suppressor lymphocyte ratio of 2.0. The patient's symptoms gradually resolved without therapy. Over the ensuing six months he remained asymptomatic, although his absolute CD4 lymphocyte count decreased to 0.25×109 per liter.

Patient 3

Patient 3 was a 29-year-old homosexual man who had been in good health until approximately two weeks before admission, when transient fever, myalgia, nausea, vomiting, and diarrhea developed. He tested negative for HIV-1 antibodies at that time, although he reported having had many sexual partners over the previous several years. The recurrence of symptoms, along with a diffuse, confluent, and erythematous rash, prompted his hospitalization. The patient reported no sore throat, headache, or neck stiffness. His temperature was 39.9°C (103.9°F), and a physical examination was unremarkable except for the rash. Serologic tests for hepatitis A and B viruses, Epstein–Barr virus, cytomegalovirus, syphilis, and HIV-1 were all negative at the time of admission. Other laboratory tests showed a leukocyte count of 1.5×109 per liter, with 0.63 lymphocyte and 0.24 granulocyte, and a hemoglobin level of 137 g per liter. The absolute CD4 lymphocyte count was 0.38×109 per liter, with a helper/suppressor lymphocyte ratio of 1.4. Over the ensuing two weeks, the patient's rash and fever resolved, and the leukocyte count returned to normal.

Patient 4

Patient 4 was a 27-year-old homosexual man who had been in good health until the development of cervical lymphadenopathy, pharyngitis, and fever (temperature to 38.3°C [101°F]) approximately 10 days before his first presentation. Several days later, he also noted an erythematous maculopapular rash over his back, chest, and extremities, including the palms and soles, but not his face. In addition, he reported myalgia, neck stiffness, and headache. The patient had reportedly tested negative for HIV-1 antibodies three weeks before his illness, although he had had a number of sexual contacts in the preceding year, the most recent of which occurred eight weeks before the onset of his illness. At his first presentation, he had an absolute CD4 lymphocyte count of 0.97×109 per liter, with a helper/suppressor lymphocyte ratio of 2.0. His illness resolved completely over the ensuing two weeks, and he remained asymptomatic.

Methods

Sequential plasma samples from all four patients were tested for p24 antigen with a commercial enzyme immunoassay (Abbott Laboratories, North Chicago). HIV-1—specific antibodies in the plasma from each patient were measured with a commercial enzyme immunoassay and Western blot assay (Genetic Systems, Seattle). An aliquot (0.2 ml) of cell-free cerebrospinal fluid from Patient 1 was found to be positive for HIV-1 on culture by a method described elsewhere.11 The quantitation of infectious HIV-1 in freshly obtained plasma and PBMC was performed by the methods of end-point-dilution culture, as described previously.9 Titers of infectious virus in plasma were expressed as tissue-culture—infective doses (TCID) per milliliter, and titers in PBMC were expressed as TCID per 106 cells.

The determination of HIV-1 DNA copy numbers in PBMC was performed by the quantitative PCR method of Pang et al.10 Briefly, 1.0 μg of DNA from each sample was subjected to 25 cycles of PCR, with 32Pend-labeled oligonucleotide primers (M661-CCTGCGTCGAGAGACTCCTCTGG and M667-GGCTAACTAGGGAACCCACTG) from the LTR/gag region. The amplified product was then subjected to electrophoresis on an 8 percent acrylamide gel and analyzed by autoradiography.

Results

Seroconversion to HIV-1 was documented by enzyme immunoassay in all four patients on the basis of the development and subsequent increase in specific antibodies in plasma (Fig. 1Figure 1Sequential Changes in HIV-1 Antibody Titers (Solid Circles) and p24 Antigen Concentrations (Open Circles) in the Plasma of the Four Patients Studied, and in Their Titers of Infectious HIV-1 in Plasma (Open Triangles) and PBMC (Solid Triangles).). The specificity of the humoral response also broadened with time, as shown on Western blotting, with antibodies recognizing progressively more HIV-1 proteins during the course of seroconversion (data not shown). The kinetics of the development of the HIV-1—specific antibody response were temporally similar in all four patients, including Patient 1, who underwent repeated plasmapheresis.

When the four patients were first seen, p24 antigen was readily detectable in the plasma of each, with very high peak levels ranging from 1200 to 4200 pg per milliliter (Fig. 1). In Patients 1, 2, and 4, however, the p24 antigen concentrations decreased precipitously to undetectable levels within 7 to 12 days. In Patient 3 (Fig. 1) the rate of decline in the plasma level of p24 antigen could not be assessed accurately because no blood samples were obtained between days 15 and 48.

Peak titers of infectious HIV-1 in the plasma of these four patients who seroconverted, as determined by end-point-dilution culture, ranged from 1000 to 10,000 TCID per milliliter (Fig. 1) — levels of infectious HIV-1 previously found only in patients with the acquired immunodeficiency syndrome (AIDS) or the AIDS-related complex.9 Subsequently, the plasma HIV-1 titers dropped to 1 to 2 TCID per milliliter in all the patients (Fig. 1). This rapid decline in cell-free virus in plasma occurred over an interval of 9 to 39 days.

Peak titers of infectious HIV-1 in PBMC ranged from 100 to 10,000 TCID per 106 cells and also decreased rapidly to titers of 1 to 10 TCID per 106 cells over an interval of 10 to 36 days (Fig. 1). The decline in the viral burden in all four patients occurred spontaneously, without any antiretroviral treatment.

The transient high levels of HIV-1 in these patients with primary infection were confirmed by quantitative PCR methods. Figure 2Figure 2Quantitation of HIV-1 DNA in PBMC by PCR. shows that the number of HIV-1 DNA copies in PBMC was highest during the symptomatic phase of the acute illnesses. When the PCR signals in Figure 2 were quantified by scintillation counting and compared with those from control standards, the peak DNA copy numbers in PBMC were calculated as 6930 to 12,900 per 106 cells. These numbers decreased precipitously to 220 to 1660 per 106 cells over an interval of 6 to 34 days (Fig. 3Figure 3Sequential Determinations of HIV-1 DNA Copy Numbers in PBMC from Patients 1 (○), 2 (□), 3(), and 4 ().).

Discussion

These four patients presented with clinical syndromes and laboratory findings consistent with primary HIV-1 infection, including Patient 1, who had an unusual life-threatening Guillain—Barré syndrome. The reason for the varied presentations of acute HIV-1 infection is unknown, but it is likely to involve a number of factors, including the immune response of the host and the quantity, virulence, or tropism of the infecting viral strains. There have been several reports demonstrating that the presence of syncytium-inducing and fast-growing isolates correlates with the rate of progression to AIDS.12 13 14 In the present study, the HIV-1 isolates were not characterized systematically with respect to their in vitro functional properties. However, all such isolates from these patients were found to replicate very efficiently in normal PBMC without the formation of syncytia (data not shown).

High levels of p24 antigen in plasma and the recovery of HIV-1 from PBMC and plasma have been demonstrated previously in the setting of acute infection.5 6 7 8 The HIV-1 burden has not been quantified, however, although some investigators have assumed high titers to be present.15 In these four cases, we document the presence of high levels of infectious HIV-1 in plasma and PBMC (1000 to 10,000 TCID per milliliter and 100 to 10,000 TCID per 106 cells, respectively) during primary infection. The levels detected in the samples from these patients are comparable to, or higher than, those already reported for patients with AIDS or AIDS-related complex.9 The transient high-level viremia described here may be a common phenomenon during acute HIV-1 infection, but it is possible that less symptomatic patients who seroconvert may have lower levels of circulating virus. Nevertheless, the findings in this study imply that there is a window period during acute HIV-1 infection when the patient is seronegative, yet highly infectious.

The high levels of infectious HIV-1 found in the PBMC of these patients during seroconversion have been confirmed by quantitative PCR studies that count copies of viral DNA. Although there is a general correlation between the copy numbers of DNA and the titers of infectious HIV-1 in PBMC, the numbers of infected cells determined with these two techniques are not equivalent (Fig. 1 and 3). The discrepancy may result from the selective distribution of viral DNA in infected cells, the ability of the PCR to detect viral DNA that is incapable of encoding infectious virions, or differences in efficiency among the PCR primers used to detect viral DNA. Nevertheless, the general correlation of infectious viral titers with the quantitative results of the PCR suggests that these techniques are reliable and applicable to clinical studies.

Sequential quantitative studies of HIV-1 in these four patients demonstrate an effective and rapid mechanism for limiting viral replication in vivo. Although it is possible that the decline in viral load is due to a self-restricting phenomenon, because of the lack of stimulated target cells in vivo,16 it is more likely that the drop in viral titer reflects the development of effective immune responses in the host. Although the components of this effective immune response are yet to be delineated, the rapid decline in viral replication observed in these four patients may be consistent with an effective response of cytotoxic T lymphocytes, as seen in other viral infections.17 18 19 It will be important to study future cases of primary infection to define the precise immune measures that are responsible for this potent anti—HIV-1 activity. In addition, it will be important to study how HIV-1 replication overcomes the specific immune responses as the disease progresses, permitting high levels of the virus to return.9 A better understanding of these processes may allow us to exploit the beneficial anti—HIV-1 immune responses to develop more effective treatment strategies for AIDS.

Supported by grants (AI 25541, AI 28747, AI 27742, and AI 24030) from the National Institutes of Health and by the Friars' Charitable Foundation and the Aaron Diamond Foundation.

We are indebted to Drs. Wendy Clough, Peter Ruane, Alvin Sellers, and Ashley Lipshultz for clinical assistance; to Drs. Shen Pang and Irvin Chen for technical advice; to Drs. John Chia and Wendell Ching for helpful suggestions; and to Wendy Chen for illustrations.

Source Information

From the Division of Infectious Diseases, Department of Medicine, Cedars—Sinai Medical Center, UCLA School of Medicine, Los Angeles (E.S.D., T.M., R.D.M.); and the Aaron Diamond AIDS Research Center, New York University School of Medicine, New York (D.D.H.). Address reprint requests to Dr. Ho at the Aaron Diamond AIDS Research Center, New York University School of Medicine, 455 First Ave., New York, NY 10016.

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