CD4 Viral Load Discrepancy
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1 (C)2001 The Japanese Society for AIDS Research The Journal of AIDS Research Case Report CD4 Viral Load Discrepancy Yasuhiro KATO1,3), Teruhisa FUJII2), Noboru TAKATA2), Kazuhiro UEDA3) and Mitchell D. FELDMAN4) 1) Department of Pediatrics, National Hiroshima Hospital 2) Division of Blood Transfusion Services, Hiroshima University Medical Hospital 3) Department of Pediatrics, Hiroshima University School of Medicine 4) Division of General Internal Medicine and Center for AIDS Prevention Studies, Department of Medicine, University of California, San Francisco Case : A 22-year-old Japanese male with hemophilia B and AIDS was described. His clinical course had been complicated by recurrent herpes zoster and oral candidiasis. Poor adherence to former antiretroviral therapy might have been associated with the multi-drug resistance in genotypic analysis. After starting a regimen consisting of stavudine, lamivudine, saquinavir, and nelfinavir, substantial improvements both in CD4+cell counts and clinical status were seen despite his plasma viral load consistently showing titers above 4.0 log10 copies/ml. Discussion : A number of patients who initiate highly active antiretroviral therapy eventually experience virologic failure. Medication for such patients has been switched based on the viral load, a surrogate marker for clinical progression of HIV infection. However, these patients have few therapeutic options. What constitutes failure of antiretroviral therapy is still controversial. It may be premature for clinicians to change antiretroviral therapy solely on the finding of detectable viral loads. Key words : CD4, discrepancy, HAART, HIV, viral load The Journal of AIDS Research 3 : 82-86, 2001 Introduction The goal of antiretroviral therapy for human immunodeficiency virus (HIV) infection is to lengthen and improve the quality of the patient's life. Many patients experience both immunologic and virologic responses to highly active antiretroviral therapy (HAART, which includes at least one protease inhibitor with two reverse-transcriptase inhibitors) in terms of increased CD4 + cell counts in peripheral blood and reduced levels of plasma HIV RNA)) Unfortunately, about one tenth of patients who initiate HAART eventually experience virologic failure.2-6) For such patients, medication is often switched or modified based on the viral load, a surrogate marker for clinical Correspondence : Yasuhiro KATO, MD, PhD, Department of Pediatrics, National Hiroshima Hospital, 513 Jike, Saijo-cho, Higashi-Hiroshima, Hiroshima, , Japan Fax : , Yasuhiro.Kato@mb7.seikyou.ne.jp Received May 20, 2000 ; Accepted February 9, 2001 progression of HIV infection.7,8) Therapeutic options may be limited for these patients and medication crossresistance and drug-drug interaction are matters of concern.9,10) We describe a patient with AIDS on HAART who had substantial increase in CD4+cell counts and improvement in clinical status although this patient was not able to achieve or sustain undetectable viral loads. What constitutes failure of antiretroviral therapy is still controversial. It may be premature for clinicians to change antiretroviral therapy solely on the finding of detectable viral loads, especially in patients for whom there are a limited number of drugs available. Case Report The patient was a 22-year-old Japanese male with hemophilia B and AIDS. He was treated with nonheated plasma derived factor IX concentrates. At 8 years old, he tested positive for HIV-1 antibody. His history of antiretroviral therapy, plasma HIV-1 RNA levels, and CD4+cell counts are illustrated in Figure 1. Plasma HIV-1 RNA quantification was performed 82(18)
2 The Journal of AIDS Research Vol.3 No Figure 1. History of antiretroviral therapy, plasma HIV-1 RNA levels, and CD4+cell counts. by use of a reverse transcriptase polymerase chain reaction assay (Amplicor HIV-1 Monitor Test version 1.0, Roche Diagnostic Systems, Branchburg, NJ, USA) according to the manufacturer's instructions. Virologic failure was defined as a decrease in plasma viral load more than 1.0 log10 copies/ml compared with baseline or achievement of undetectable plasma HIV RNA levels throughout the period of follow-up. CD4 + cell counts were monitored by flow cytometry. Immunological response was defined as an increase in the number of CD4 + cells more than 50/0 above baseline throughout the period of follow-up. The patient was initially treated with zidovudine (ZDV) and didanosine (ddi) from 1992, but adherence to this regimen, (as indicated by pharmacy records and patient reporting) was poor and it was eventually discontinued in June 1996 due to side effects. The clinical course was complicated by recurrent herpes zoster and oral candidiasis. Zalcitabine (ddc) and stavudine (d4 T) were then added and the viral load decreased initially, but this regimen (ddc plus d4t) subsequently was changed to d4t, lamivudine (3TC), and indinavir (IDV) due to the increase in his viral load. Frequent vomiting subsided after IDV was switched to saquinavir (SQV) in October 1997 ; however the viral load increased again on this regimen. Sequential plasma samples were collected from this patient, and the pol genes of the virion RNA populations were directly sequenced. The first genotypic analysis performed in February 1998 showed multiple codons in both the reverse transcriptase (RT) and protease genes that differed from those of the wild-type virus, and that have been associated with multi-drug resistance (Table 1). Ritonavir (RTV), started on April 1998, was interrupted after one week because of severe nausea and vertigo and he was started on nelfinavir (NFV) monotherapy. This monotherapy, though outside of treatment guidelines, was adopted because no other drugs were considered to be effective and were acceptable to the patient. Plasma viral load gradually increased and a second genotypic analysis was performed after 5 months of NFV monotherapy in September. The nucleoside-resistance mutations found in the first analysis disappeared except reverse transcriptase M41L and T215Y/F ZDV resistance mutations and he was started on a four drug regimen consisting of d4t, 3TC, SQV, and NFV from October Compliance with this regimen was excellent. His viral load decreased only 0.8 log10 copies/ml on this regimen accompanied by an increase to more than 300 cells/Đl in CD4 + cell count. The third and fourth genotypic analyses were performed in February 1999 and January 2000, respectively. Mutations conferring resistance to 3TC, ddc, ddi, and d4t were demonstrated while this patient was on the four drug regimen. Protease mutations were present through four consecutive assays. At the most recent assessment, despite his viral RNA consistently showing titers of more than 30,000 copies/ml, drastic improvements in CD4+cell counts (i.e. 560 cells/Đl) were seen on his
3 Y Kato et al.: CD4 Rise Despite Detectable Viral Load Table 1 Results of genotypic HIV drug resistance assays He has had no further opportu- four drug therapy. nistic infections. Discussion A major aim of antiretroviral therapy for HIV infection is to keep the viral load undetectable or at least suppressed as fully as possible.11) As previously reported, there is a direct relationship between increases in CD4 + cell counts and reduction of viral loads as a result of HAART.12,13) Our case report suggests that lack of virological response to therapy is not a clear predictor of clinical outcome in a patient exhibiting immunological but not virological response to treatment. Although it is widely accepted that monitoring of the plasma viral load is important in HIV clinical practice, the viral load is not always directly associated with disease progression. There has been increased interest recently in the observed discrepancy between CD4 + cell count and viral load. Kaufmann et al. first stated that although a significant proportion of patients taking HAART will not be able to achieve or sustain undetectable viral loads, these patients may nonetheless experience significant immunological benefits.) Piketty et al. suggested one tenth of patients with advanced HIV disease treated on HAART exhibited increased CD4 + cell counts in the absence of significant decrease in plasma viral load. These patients experienced a low incidence of AIDSdefining events, similar to that of immunological and virological responder patients.3) There is no obvious
4 The Journal of AIDS Research Vol.3 No explanation for this phenomenon. One possibility is that even when virologic failure occurs on treatment, the viral load is usually significantly below the pretreatment baseline. In our case, there was also a plasma viral load reduction compared with the period before the four drug regimen. In addition, protease inhibitors are thought to function primarily by rendering newly produced virus noninfectious.1,2,14) Other recent studies show HAART reserves some of the immunoactivation that is associated with HIV infection and that this may be independent of its antiviral activity.15-18) Regardless of which of these hypotheses is more accurate, our observation raises more questions about whether these patients should switch early to a different regimen. Therapeutic options are limited for such patients.4,19) Moreover, medication cross-resistance and drug-drug interaction are matters of concern.9,10) Medication for such patients has been switched based on the viral load, a surrogate marker for clinical progression of HIV infection. What constitutes failure of antiretroviral therapy is still controversial. Genotypeguided therapy results in a sustained reduction in plasma viral load in the heavily pre-treated patient population.20,21) More research is needed to guide clinicians and patients on whether to switch early to a different regimen for patients experiencing virologic failure, especially when therapeutic options are limited. Acknowledgements : We are greatly indebted to Dr. Wataru Sugiura (AIDS Research Center, National Institute of Infectious Diseases, Japan) for performing genotypic analysis of the drug-resistant mutations of HIV-1. References 1) Fessel WJ, Krowka JF, Sheppard HW, Gesner M, Tongson S, Weinstein S, Ascher M, Kwok S, Christopherson C : Dissociation of immunologic and virologic responses to highly active antiretroviral therapy. J Acquir Immune Defic Syndr 23: , ) Kaufmann D, Pantaleo G, Sudre P, Telenti A : CD4-cell count in HIV-1-infected individuals remaining viraemic with highly active antiretroviral therapy (HAART). Lancet 351: , ) Piketty C, Castiel P, Belec L, Batisse D, Si Mohamed A, Gilquin J, Gonzalez-Canali G, Jayle D, Karmochkine M, Weiss L, Aboulker JP, Kazatchkine MD : Discrepant response to triple combination antiretroviral therapy in advanced HIV disease. AIDS 12: , ) Levitz SM : Improvement in CD4 + cell counts despite persistently detectable HIV load. N Engl J Med 338: , ) Renaud M, Katlama C, Mallet A, Calves V, Carcelain G, Tubiana R, Jouan M, Caumes E, Agut H, Bricaire F, Debre P, Autran B : Determinants of paradoxical reconstitution after protease inhibitor-containing antiretroviral regimen. AIDS 13: , ) Barreiro PM, Dona MC, Castilla J, Soriano V : Patterns of response (CD4 count and viral load) at 6 months in HIV-infected patients on highly active antiretroviral therapy. AIDS 13: , ) Mellors JW, Rinaldo CT, Gupta P, White RM, Todd JA, Kingsley LA : Prognosis in HIV-1 infection predicted by the quantity of virus in plasma. Science 272: , ) Marschner IC, Collier AC, Coombs RW, D'Aquila RD, DeGruttola VD : Use of changes in plasma levels of human immunodeficiency virus type 1 RNA to assess the clinical benefit of antiretroviral therapy. J Infect Dis 177:40-47, ) McDonald CK, Kuritzkes DR : Human immunodeficiency virus type 1 protease inhibitors. Arch Intern Med 157: , ) Kato Y, Fujii T, Mizoguchi N, Takata N, Ueda K, Feldman MD, Kayser SR : Potential interaction between ritonavir and carbamazepine. Pharmacotherapy 20: , ) Carpenter CC, Fischl MA, Hammer SM, Hirsch MS, Jacobsen DM, Katzenstein DA, Montaner JS, Richman DD, Saag MS, Schooley RT, Thompson MA, Vella S, Yeni PG, Volberding PA : Antiretroviral therapy for HIV infection in 1997 : updated recommendations of the International AIDS Society-USA panel. JAMA 277: , ) Perelson AS, Essunger P, Cao Y, Vesanen M, Hurley A, Saksela K, Markowitz M, Ho DD : Decay characteristics of HIV-1-infected compartments during combination therapy. Nature 387: , ) Staszewski S, Miller V, Sabin C, Schlecht C, Gute P, Stamm S, Leder T, Berger A, Weidemann E, Hill A, Phillips A : Determinants of sustainable CD4 lymphocyte count increases in response to antiretroviral therapy. AIDS 13: , ) Flexner C : HIV-protease inhibitors. N Engl J Med 338: , ) Weiss L, Ancuta P, Girard PM, Bouhlal H, Roux A, Cavaillon NH, Kazatchkine MD : Restoration of normal interleukin-2 production by CD4+T cells of human immunodeficiency virus-infected patients after 9 months of highly active antiretroviral therapy. J Infect Dis 180: , ) Kaufmann GR, Zaunders JJ, Cunningham P, Cooper DA : Phenotypic analysis of CD8+T lymphocytes in a cohort of HIV type 1-infected patients treated with saquinavir, ritonavir, and two nucleoside analogs for 1 year, and association with plasma HIV type 1 RNA.
5 Y Kato et al.: CD4 Rise Despite Detectable Viral Load AIDS Res Hum Retroviruses 15: , ) Sousa AE, Chaves AF, Doroana M, Antunes F, Victorino RM: Early reduction of the over-expression of CD40L, OX40 and Fas on T cells in HIV-1 infection during triple anti-retroviral therapy: possible implications for lymphocyte traffic and functional recovery. Clin Exp Immunol 116: , ) Bucy RP, Hockett RD, Derdeyn CA, Saag MS, Squires K, Sillers M, Mitsuyasu RT, Kilby JM: Initial increase in blood CD4 (+) lymphocytes after HIV antiretroviral therapy reflects redistribution from lymphoid tissues. J Clin Invest 103: , ) Deeks SG, Barbour JD, Martin JN, Swanson MS, Grant RM: Sustained CD4+T cell response after virologic failure of protease inhibitor-based regimens in patients with human immunodeficiency virus infection. J Infect Dis 181: , ) Verhofstede C, Wanzeele FV, Gucht BVD, Cabooter ND, Plum J: Interruption of reverse transcriptase inhibitors or a switch from reverse transcriptase to protease inhibitors resulted in a fast reappearance of virus strains with a reverse transcriptase inhibitor-sensitive genotype. AIDS 13: , ) Clevenbergh P, Durant J, Halfon P, del Giudice P: Mondain V, Montagne N, Schapiro JM, Boucher CA, Dellamonica P: Persisting long-term benefit of genotypeguided treatment for HIV-infected patients failing HAART. The Viradapt Study: week 48 follow-up. Antivir Ther 5:65-70, (22)
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