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Prospective evaluation of the effects of antiretroviral therapy on body composition in HIV-1-infected men starting therapy

Mallon, Patrick WGa,b; Miller, Johnb; Cooper, David Aa; Carr, Andrewb

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From the aNational Centre in HIV Epidemiology and Clinical Research, University of New South Wales, Sydney and the bHIV, Immunology and Infectious Diseases Clinical Services Unit, St Vincent's Hospital Sydney Ltd., Sydney, Australia.

Correspondence to Dr Patrick W.G. Mallon, NCHECR, 376 Victoria Street, Darlinghurst, Sydney NSW 2010, Australia. Tel: +61 2 9332 4648; fax: +61 2 9332 1837; e-mail:

Received: 23 May 2002; revised: 22 November 2002; accepted: 5 December 2002.

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Objective: Little prospective data are published on the natural history of HIV-associated lipodystrophy (HIVLD) in individuals beginning their first antiretroviral regimen. To investigate this a study was designed to explore changes in body composition occurring with antiretroviral therapy.

Study design: A non-randomized, prospective, exploratory study of 40, HIV-infected men, naive to treatment, beginning antiretroviral therapy. Regular assessments of body composition, and metabolic and immunological parameters were performed.

Results: Mean follow-up was 96 (SD 45) weeks of therapy. There were increases in limb fat, central abdominal fat and lean mass over the initial 24 weeks of therapy followed by a selective, progressive loss of limb fat from week 24. There was a median 13.6% [interquartile range (IQR), 0.9–26.3] loss of limb fat per year from week 24 onwards. Treatment with stavudine, higher baseline HIV RNA, higher baseline ‘T’ score and lower week 24 lean mass were associated with higher rate of limb fat loss from week 24. In multivariate analysis, treatment with stavudine was the strongest independent factor associated with rate of limb fat loss (P = 0.05). Hypercholesterolaemia developed early in treatment, whereas hypertriglyceridaemia, hyperinsulinaemia and decreased bone mineral density developed later. The largest changes in CD4 cell counts and HIV viral load, seen early into treatment, were associated with gain rather than loss of fat.

Conclusions: This is the first prospective study demonstrating that treatment with antiretrovirals results in progressive, selective loss of limb fat. Loss of limb fat occurred after the period of most intense immune restoration, making an immune aetiology unlikely.

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Individuals receiving antiretroviral therapy for the treatment of HIV-1 infection have experienced peripheral lipoatrophy [1], gain in visceral fat [2], hyperlipidaemia and insulin resistance, all of which have been grouped under the common heading of HIV-associated lipodystrophy (HIVLD).

The pathogenesis of HIVLD is likely to involve numerous mechanisms, such as the inhibition of DNA polymerase gamma in mitochondria by nucleoside reverse transcriptase inhibitors (NRTIs) leading to mitochondrial dysfunction in fat [3,4], abnormalities of fat differentiation resulting from the effects of protease inhibitors on transcription factors such as sterol regulatory element-binding protein-1 (SREBP-1) [5,6] and increased apoptosis of fat cells secondary to these many insults [7]. Changes in immune status resulting from therapy, and the effects of secondary cytokine activation on fat tissue, could explain some changes seen in HIVLD [8] although evidence to support this view is lacking.

Cross-sectional cohorts have shown an association between HIVLD and older age, lower baseline CD4 cell counts, the use of and duration of use of protease inhibitors (PI) and of NRTIs [9–14] particularly when PIs and NRTIs are used in combination [9]. Although the syndrome is well described, a lack of objective, prospective data prevents identification of possible primary and secondary defects. In one prospective study, any form of patient- or physician-reported lipodystrophy was seen in 17% of individuals at 18 months [10], but the study only included individuals taking PI-containing regimens.

We hypothesised that lipoatrophy occurs as a result of treatment with, and duration of, antiretroviral therapy, rather than being purely an immune phenomenon. To explore this hypothesis, we studied a cohort of antiretroviral-naive, HIV-infected men starting a variety of antiretroviral regimens, to determine changes in body composition resulting from therapy, and factors associated with these changes.

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Study population

HIV-infected men, referred by their treating physicians, were sequentially recruited from the HIV Clinics of St Vincent's Hospital, Sydney, Australia. All patients had documented HIV-1 infection, were at least 18 years old, had no active AIDS-defining illness, no previous antiretroviral exposure and were at a stage of their illness where their treating physicians considered antiretroviral therapy appropriate. As this was a non-randomized study, the treating physician made decisions regarding the components of baseline antiretroviral regimens, and any subsequent treatment changes. All patients provided written, informed consent after approval of the study by the Human Research Ethics Committee.

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Baseline demographics were collected. The following assessments were performed at baseline, weeks 12, 24 and then every 24 weeks thereafter; CD4+ lymphocyte counts, plasma HIV RNA, fasting total cholesterol, estimated low-density lipoprotein (LDL) cholesterol, high-density lipoprotein (HDL) cholesterol, triglyceride, glucose and insulin [1,15].

Total and regional body composition was quantified at screening, and at weeks 12, 24, 48 and every 48 weeks thereafter by dual-energy X-ray absorptiometry (DEXA) (Lunar DPXL; Madison, Wisconsin, USA) at a single reading site. Estimates of central abdominal fat (CAF) and spinal bone mineral density (represented by ‘T’ score) were determined from a central window measurement [1,15].

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All analyses were by intention-to-treat and included follow-up data on all subjects who started their treatment regardless of subsequent treatment changes. The primary endpoint was change in limb fat measured by DEXA with secondary endpoints of changes in CAF, total cholesterol and estimated LDL cholesterol, triglycerides, glucose, insulin and ‘T’ score. Data were collected on a specifically designed database (Logicielle, Sydney, Australia) and non-parametric analyses were applied. Paired comparisons were analysed using the Wilcoxon signed rank test, unpaired comparisons using the Mann–Whitney test and correlations between sets of variables using Spearman rank correlation coefficient tests. The Kruskal–Wallis test was used to compare three group samples. Simple and multiple regression analyses were performed to examine the relationship between variables. P values of less than 0.05 were considered significant.

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Forty patients were recruited between July 1997 and May 2000 with analysis performed in December 2001. At the time of analysis, all patients were alive, 90% of the cohort had completed 96 weeks of therapy and 50% had completed 144 weeks of therapy.

All median baseline metabolic parameters were within normal limits (Table 1), as were body mass index (BMI) and bone mineral density. Almost half the cohort received a regimen containing a PI, with indinavir being the most common PI used. Five subjects received a regimen containing both PIs and non-nucleoside reverse transcriptase inhibitors (NNRTI). Roughly equal numbers were prescribed one of the three most common dual NRTI backbone regimens at that time: didanosine and stavudine, stavudine and lamivudine, and zidovudine and lamivudine.

Table 1
Table 1
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Over the course of the study, 16 (40%) subjects changed therapy. Four (10%) subjects changed class from a PI to a NNRTI-containing regimen an average of 23 (range 12–36) months into the study. One subject changed from a PI to a NNRTI-containing regimen due to virological failure 2 years into the study. All remaining changes were secondary to side effects. The most common drugs involved were stavudine with 11 changes after a mean of 7 [3–12] months of treatment (six secondary to neuropathy, one secondary to symptomatic lactic acidaemia, one secondary to adherence problems and three for side effects not otherwise specified), didanosine (ddI) with five changes after a mean of 10 (3–24) months (three secondary to neuropathy, one secondary to nausea and one for other side effects), and indinavir with four changes after a mean of 8 (3–12) months (two secondary to renal calculi, one secondary to paronychia and one secondary to other side effects). No subject changed therapy as a result of changes in body composition.

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Immunological and virological responses to therapy

Seventy percent of the cohort achieved viral load < 400 copies/ml by week 12, with no significant change seen between weeks 12 and 144 (Fig. 1b). At the time of analysis, 82% of the cohort achieved an undetectable viral load (HIV RNA < 400 copies/ml). Median baseline CD4 cell count was 246 × 106 cells/l (range 0 to 836 × 106 cells/l). The largest rise in median CD4 lymphocyte count occurred by week 24 (median increase of 126 × 106 cells/l, P < 0.0001), with a further significant rise between weeks 24 and 144 (increase of 56 × 106 cells/l, P < 0.05).

Fig. 1
Fig. 1
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Body composition

There was a significant rise in BMI (22.5 to 24, P < 0.05) and lean mass (3% rise from baseline, P < 0.01) by week 12, which was sustained to week 48. At week 96 BMI had decreased to a level not significantly different from baseline. Total body fat increased by median 20% to week 24 (P < 0.001) with no significant changes from week 24 onwards.

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Limb fat

There was an increase in limb fat (median 5.6 versus 6.9 kg), CAF (1.0 versus 1.3 kg) and lean mass (52.5 versus 54.7 kg) to week 24 coinciding with the largest changes in CD4 and HIV RNA (Figs 1a and 2a). From week 24 onwards there was a selective, progressive loss of limb fat with median limb fat mass at weeks 96 and 144 being significantly less than baseline (median loss of 1.6 and 3.0 kg, respectively). During the initial period, 57% patients experienced greater than 10% gain in limb fat mass. Subsequently, however, 46% patients lost more than 10% limb fat mass and 48% patients lost at least 1 kg between baseline and week 96. From week 24, there was a median 13.6% [interquartile range (IQR), 0.9–26.3] loss of limb fat per year of treatment. This loss occurred after the period of greatest change in CD4 and HIV RNA (Fig. 1).

Fig. 2
Fig. 2
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Older age correlated with a lower baseline limb fat. Higher baseline CAF and truncal fat correlated with higher baseline limb fat. The biggest gains in limb fat from baseline to week 24 were seen in those with higher baseline CAF and truncal fat, higher baseline HIV RNA and higher baseline ‘T’ scores. When baseline and week 24 patient, treatment, immune, morphological and metabolic factors were analysed, subjects treated with stavudine, those with higher baseline HIV RNA, higher baseline ‘T’ score and higher week 24 lean mass had a significantly greater rate of loss of limb fat from week 24 (percentage loss per year) (Tables 2–4). Multivariate analysis revealed use of stavudine to be associated with a significantly increased rate of loss of limb fat (P = 0.05).

Table 2
Table 2
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Table 3
Table 3
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Table 4
Table 4
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Central abdominal fat

In contrast to limb fat, after an initial increase to week 24, CAF was maintained after week 24, remaining significantly greater than baseline out to week 144 (Fig. 2b). Baseline factors predicting larger mass of CAF at week 24 included higher baseline total fat, limb fat, truncal fat and CAF, higher insulin concentrations and higher BMI (Table 2). Factors associated with a greater percentage change in CAF between baseline and week 24 included lower baseline cholesterol and CD4 cell count and higher baseline HIV RNA. Subjects with more CAF at week 24 also had significantly higher week 24 truncal, limb and total fat, higher cholesterol, triglycerides, insulin, and lower HDL cholesterol and a higher BMI (Table 3). A greater change in CD4 cell count from baseline correlated with changes in limb fat, truncal fat, CAF and total fat. Those taking a PI-containing regimen had significantly higher and those taking a NNRTI regimen had significantly lower CAF at week 24.

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Bone mineral density

The ‘T’ score rose slightly to week 24 and then fell significantly to week 48 remaining significantly lower than baseline out to week 144. The percentage of the cohort with ‘T’ scores less than −1 (consistent with osteopenia) rose from 13% at baseline to 22% at week 144. There was little change in the number of the subjects with ‘T’ scores less than −2.5 consistent with osteoporosis (1 at baseline, 2 at week 144).

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Metabolic parameters

Changes in metabolic parameters are illustrated in Figure 3. Fasting total cholesterol and estimated LDL cholesterol rose significantly early into treatment with the largest rise occurring by week 12 (Fig. 3a). Both remained significantly higher than baseline out to week 144. In contrast triglyceride concentrations did not rise significantly until week 96 and remained elevated out to week 144 (Fig. 3b). Similarly, insulin concentrations rose late with significantly higher insulin concentrations occurring at week 144 (Fig. 3b). Changes in fasting insulin were not significantly different between those prescribed PI-containing regimens [median, 1.2 mmol/l per year (IQR, −0.87 to 3.27)] and those prescribed PI-sparing regimens [0.65 mmol/l per year (IQR −0.7 to 2)].

Fig. 3
Fig. 3
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The change in total and LDL cholesterol per year of treatment was 0.44 and 0.24 mmol/l, respectively. In a multivariate analysis of baseline variables, treatment with PIs (P = 0.006), lower baseline cholesterol (P = 0.02), and lower baseline lean mass (P = 0.04) were independently associated with greater increases in total cholesterol. Similarly, use of PIs (P = 0.002) and lower baseline LDL (P = 0.04) were associated with the largest rises in LDL cholesterol.

The change in triglycerides concentrations was 0.14 mmol/l per year of treatment. No baseline factor determined change in triglyceride, although those with greater change in cholesterol per year also had significantly larger rises in triglycerides per year (P = 0.01).

HDL cholesterol rose by 0.1 mmol/l at week 24 (P < 0.01) but the rise was not sustained past week 96. Fasting glucose concentrations did not change (4.7 mmol/l at baseline versus 4.85 mmol/l at week 144).

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The complexity of the mechanisms underlying HIVLD is reflected in the results of this exploratory study. Most of the components of HIVLD, such as central fat accumulation, peripheral lipoatrophy and hyperlipidaemia were observed. Contributions by drug classes and specific drugs, in addition to immunological and virological responses to therapy, were all shown to have some correlation with changes in body composition. From these results, a sequence of events begins to emerge, providing an insight into possible primary and secondary events in the development of HIVLD. Of importance, these results reveal trends that run counter to some currently held theories about the possible mechanisms underlying HIVLD.

The gains in both central abdominal fat and limb fat seen during the first 24 weeks of treatment could be explained by general improvements in health and nutrition associated with treatment of HIV viraemia and reversal of the associated catabolic state. The simultaneous increase in lean mass also seen during this period support this viewpoint, suggesting that these changes result from general improvements in nutrition rather than a fat-specific process.

The gain in CAF during the initial 24 weeks of therapy may reflect the visceral fat accumulation reported in HIVLD [2]. From week 24 onwards, there was an obvious selective, progressive loss of limb fat whereas both CAF and lean mass were maintained (Figs 1 and 2). This likely represents the lipoatrophy that is characteristic of HIVLD. Maintained levels of CAF in the presence of limb fat loss (Fig. 1) could result in the central fat becoming more pronounced clinically to patients or physicians as limb fat declined.

Of interest is the correlation noted between CAF and limb fat. Although by 3 years both gain in central fat and loss of limb fat are present, the two processes do not appear to be occurring simultaneously and may be part of separate aetiologies – the increase in CAF probably in response to nutritional improvement (and therefore a secondary effect of drug treatment), whereas the loss of limb fat was probably a result of long-term antiretroviral drug use. However, excess fat accumulation resulting from changes in nutritional requirements alone would be expected to decrease over time as the body gains muscle mass. The fact that this fails to occur in this cohort may indicate that the persistent accumulation of abdominal fat seen after week 24 is a reflection of a pathological process. Whether this is related to immune restoration, continued drug exposure or other process is unclear from this study.

Loss of limb fat, however, developed in the absence of significant changes in HIVVL, and after the largest change in CD4 cell count had already occurred (Fig. 1a and 1b). This runs contrary to the hypothesis that HIVLD is part of a cytokine-driven ‘immune reconstitution’ phenomenon [8,16]. Indeed, during the period of most intense immune recovery, there was actually a gain, rather than a loss, of both limb fat and CAF.

Complex relationships between morphological and metabolic changes are apparent from this study. Those with higher baseline cholesterol values gained less limb fat and CAF to week 24 (Table 2). A first impression may be that these subjects already have high baseline body fat deposits, thus explaining the higher cholesterol values and lower relative fat gains. However this was not the case, as no significant correlations existed between baseline cholesterol levels and mass of total or compartmental body fat (data not shown).

The importance of the cholesterol values is reflected in their strong association with subsequent loss of limb fat (Table 3). Such an association has previously been reported [17]. There are marked inter-individual variations in the function of adipose tissue, with evidence supporting a genetic basis for this variation [18]. If higher cholesterol levels reflect poorly functioning adipose tissue, these individuals may be at higher risk of further adipose tissue dysfunction, resulting from the additional and continuing insults from antiretrovirals on adipose tissue (e.g. SREBP-1c) [5,6] or mitochondrial function [4]. This could explain the changes seen in this cohort.

Higher insulin concentrations associated with high CAF mass, seen in this study, is an association that has been well described in HIV-infected [19] and uninfected populations [20]. Other PI- induced mechanisms of insulin resistance, such as those involving dysfunction of the GLUT-4 glucose transporter [21,22], result in an acute insulin resistance. Although in vitro evidence exists to support such a mechanism, such an acute process should result in high insulin concentrations early in the course of treatment. This was not seen in this study, with hyperinsulinaemia occurring later into treatment.

Although the most detailed prospective study to date, the results from this study should be viewed in the context of study limitations. It could be argued that the fact that this was a non-randomized study, with no untreated controls, using various antiretroviral regimens, in a cohort of male only patients is a limitation. In addition, the use of total body DEXA to estimate CAF and bone mineral density is imperfect. Although significant associations were detected, these should be viewed in the context of the number of subjects involved in the study. It could be argued that the large number of comparisons studied and the multiple data points used leaves the results prone to false positives, although non-parametric analyses were employed in an attempt to limit this.

The number of treatment changes may or may not be viewed as a limitation. Treatment changes happen frequently in routine practice and as such, this study may provide a more accurate description of the development of HIVLD in clinical practice. In addition, development of HIVLD was not used as a reason for changing treatment. The impact of treatment changes on the overall analysis was minimal. For example, there were no significant differences in the rate of limb fat loss in those who stopped stavudine, nor in the accumulation of CAF in those who stopped indinavir (data not shown).

Objective changes in body composition correlating with HIV associated lipodystrophy [1,2] only became readily apparent after 2 years of antiretroviral treatment in this cohort. This has consequences with respect to published studies alluding to the metabolically friendly profile of certain drugs or drug combinations [23], which have a relatively short follow-up period. Importantly, this study shows how the development of lipoatrophy is relatively independent of changes in immune function, being more a product of continued exposure to antiretroviral drugs.

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The authors wish to thank the patients for their participation in the study. We also wish to acknowledge the help with the design of the statistical analysis provided by Dr Matthew Law from the National Centre in HIV Epidemiology and Clinical Research, Sydney, Australia.

Sponsorship: The National Centre in HIV Epidemiology and Clinical Research is funded by the Commonwealth Department of Health and Aged Care through the Australian National Council on AIDS, Hepatitis C and Related Diseases and its Research Advisory Committee.

P.W.G.M. is supported by funds from the National Heart Lung and Blood Institute of the National Institutes of Health, grant number RO1 HL65953-01.

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Lundgren, JD; Battegay, M; Behren, G; De Wit, S; Guaraldi, G; Katlama, C; Martinez, E; Nair, D; Powderly, WG; Reiss, P; Sutinen, J; Vigano, A
HIV Medicine, 9(2): 72-81.
Dermatologic Clinics
Lipodystrophy Syndromes
Herranz, P; de Lucas, R; Perez-Espana, L; Mayor, M
Dermatologic Clinics, 26(4): 569-+.
American Journal of Physiology-Endocrinology and Metabolism
Reducing plasma HIV RNA improves muscle amino acid metabolism
Yarasheski, KE; Smith, SR; Powderly, WG
American Journal of Physiology-Endocrinology and Metabolism, 288(1): E278-E284.
Drug Safety
Long-term safety and tolerability of the lamivudine/abacavir combination as components of highly active antiretroviral therapy
Castillo, SA; Hernandez, JE; Brothers, CH
Drug Safety, 29(9): 811-826.

American Journal of Clinical Nutrition
Micronutrients in HIV-positive persons receiving highly active antiretroviral therapy
Drain, PK; Kupka, R; Mugusi, F; Fawzi, WW
American Journal of Clinical Nutrition, 85(2): 333-345.

Expert Opinion on Drug Metabolism & Toxicology
Toxic metabolic syndrome associated with HAART
Haugaard, SB
Expert Opinion on Drug Metabolism & Toxicology, 2(3): 429-445.
HIV Clinical Trials
A Prospective Study of Body Fat Redistribution, Lipid, and Glucose Parameters in HIV-Infected Patients Initiating Combination Antiretroviral Therapy
Walmsley, S; Cheung, AM; Fantus, G; Gough, K; Smaill, F; Azad, A; Diong, C; Raboud, J
HIV Clinical Trials, 9(5): 314-323.
HIV Clinical Trials
A Meta-Analysis of Six Placebo-Controlled Trials of Thiazolidinedione Therapy for HIV Lipoatrophy
Raboud, JM; Diong, C; Carr, A; Grinspoon, S; Mulligan, K; Sutinen, J; Rozenbaum, W; Cavalcanti, RB; Wand, H; Costagliola, D; Walmsley, S
HIV Clinical Trials, 11(1): 39-50.
Mitochondrial dysfunction in AIDS and its treatment
Gerschenson, M; Brinkman, K
Mitochondrion, 4(): 763-777.
Jama-Journal of the American Medical Association
Metabolic and skeletal complications of HIV infection - The price of success
Morse, CG; Kovacs, JA
Jama-Journal of the American Medical Association, 296(7): 844-854.

Dermatologic Surgery
Safety and efficacy of poly-L-lactic acid injections in persons with HIV-associated lipoatrophy: The US experience
Mest, DR; Humble, G
Dermatologic Surgery, 32(): 1336-1345.
AIDS Patient Care and Stds
Antiretroviral therapies associated with lipoatrophy in HIV-infected women
Tien, PC; Barron, Y; Justman, JE; Hyman, C; Cohen, MH; Young, M; Kovacs, A; Cole, SR
AIDS Patient Care and Stds, 21(5): 297-305.
HIV Clinical Trials
Improvements in Subcutaneous Fat, Lipid Profile, and Parameters of Mitochondrial Toxicity in Patients with Peripheral Lipoatrophy When Stavudine is Switched to Tenofovir (LIPOTEST Study)
Ribera, E; Paradineiro, JC; Curran, A; Sauleda, S; Garcia-Arumi, E; Castella, E; Puiggros, C; Crespo, M; Feijoo, M; Diaz, M; del Saz, SV; Planas, M; Sureda, D; Falco, V; Ocana, I; Pahissa, A
HIV Clinical Trials, 9(6): 407-417.
Plos One
Increasing Rates of Obesity among HIV-Infected Persons during the HIV Epidemic
Crum-Cianflone, N; Roediger, MP; Eberly, L; Headd, M; Marconi, V; Ganesan, A; Weintrob, A; Barthel, RV; Fraser, S; Agan, BK
Plos One, 5(4): -.
ARTN e10106
Clinical Infectious Diseases
The challenge of understanding articles about health-related quality of life
Wilson, I
Clinical Infectious Diseases, 39(3): 434-436.

HIV Clinical Trials
Progression of lipodystrophy (LD) with continued thymidine analogue usage: Long-term follow-up from a randomized clinical trial (the PIILR study)
Martin, A; Smith, D; Carr, A; Hoy, J; Chuah, J; Mallal, S; Law, M; Clements, M; Cooper, DA
HIV Clinical Trials, 5(4): 192-200.

HIV Medicine
Pronounced lipoatrophy in HIV-infected men receiving HAART for more than 6 years compared with the background population
Hansen, AB; Lindegaard, B; Obel, N; Andersen, O; Nielsen, H; Gerstoft, J
HIV Medicine, 7(1): 38-45.

International Journal of Clinical Practice
Long-term complications of antiretroviral therapy: lipoatrophy
Waters, L; Nelson, M
International Journal of Clinical Practice, 61(6): 999-1014.
Wiener Klinische Wochenschrift
Prevalence and risk factors for osteopenia/osteoporosis in an HIV-infected male population
Tomazic, J; Ul, K; Volcansek, G; Gorensek, S; Pfeifer, M; Karner, P; Prezelj, J; Vidmar, G; Vidmar, L
Wiener Klinische Wochenschrift, 119(): 639-646.
AIDS Research and Human Retroviruses
Mitochondrial Oxidative Phosphorylation Protein Levels in Peripheral Blood Mononuclear Cells Correlate with Levels in Subcutaneous Adipose Tissue within Samples Differing by HIV and Lipoatrophy Status
Shikuma, CM; Gerschenson, M; Chow, D; Libutti, DE; Willis, JH; Murray, J; Capaldi, RA; Marusich, M
AIDS Research and Human Retroviruses, 24(): 1255-1262.
Journal of Antimicrobial Chemotherapy
Evolving perspectives on HIV-associated lipodystrophy syndrome: moving from lipodystrophy to non-infectious HIV co-morbidities
Guaraldi, G; Baraboutis, IG
Journal of Antimicrobial Chemotherapy, 63(3): 437-440.
Current HIV Research
Progenitor Cell Types in HIV-1 Infection: Bioactivity and Emerging Targets for Treatment
Cotter, EJ; Doran, PP; Powderly, WG
Current HIV Research, 7(5): 508-518.

HIV Medicine
Cervical lipomatosis in HIV-infected patients: a case-control study
Palacios, R; Galindo, MJ; Arranz, J; Lozano, F; Estrada, V; Rivero, A; Morales, D; Asensi, V; del Arco, A; Munoz, A; Santos, J
HIV Medicine, 8(1): 17-21.

Journal of Infection
suPAR associates to glucose metabolic aberration during glucose stimulation in HIV-infected patients on HAART
Andersen, O; Eugen-Olsen, J; Kofoed, K; Iversen, J; Haugaard, SB
Journal of Infection, 57(1): 55-63.
Clinical Infectious Diseases
The pharmacogenetics of antiretroviral therapy: A review of studies to date
Quirk, E; McLeod, H; Powderly, W
Clinical Infectious Diseases, 39(1): 98-106.

Journal of Antimicrobial Chemotherapy
Therapeutic approaches to combating lipoatrophy: do they work?
Martin, A; Mallon, PWG
Journal of Antimicrobial Chemotherapy, 55(5): 612-615.
AIDS Reviews
Pathogenesis of lipodystrophy and lipid abnormalities in patients taking antiretroviral therapy
Mallon, PWG
AIDS Reviews, 9(1): 3-15.

Genetic analysis implicates resistin in HIV lipodystrophy
Ranade, K; Geese, WJ; Noor, M; Flint, O; Tebas, P; Mulligan, K; Powderly, W; Grinspoon, SK; Dube, MP
AIDS, 22(): 1561-1568.

Clinical Nutrition
Antiretroviral therapy affects the composition of weight loss in HIV infection: Implications for clinical nutrition
Maia, BS; Engelson, ES; Wang, J; Kotler, DP
Clinical Nutrition, 24(6): 971-978.
European Journal of Clinical Investigation
Impact of antiretroviral therapy on visfatin and retinol-binding protein 4 in HIV-infected subjects
Schindler, K; Haider, D; Wolzt, M; Rieger, A; Gmeinhart, B; Luger, A; Nowotny, P; Ludvik, B
European Journal of Clinical Investigation, 36(9): 640-646.

Scandinavian Journal of Infectious Diseases
Antiretroviral treatment of HIV infection: Swedish recommendations 2007
Josephson, F; Albert, J; Flamholc, L; Gisslen, M; Karlstrom, O; Lindgren, SR; Navter, L; Sandstrom, E; Svedhem-Johansson, V; Svennerholm, B; Sonnerborg, A
Scandinavian Journal of Infectious Diseases, 39(): 486-507.
Journal of Infection
Risk of premature atherosclerosis and ischemic heart disease associated with HIV infection and antiretroviral therapy
Calza, L; Manfredi, R; Pocaterra, D; Chiodo, F
Journal of Infection, 57(1): 16-32.
AIDS Reviews
Epidemiology, Assessment, and Management of Excess Abdominal Fat in Persons with HIV Infection
Moyle, G; Moutschen, M; Martinez, E; Domingo, P; Guaraldi, G; Raffi, F; Behrens, G; Reiss, P
AIDS Reviews, 12(1): 3-14.

Jama-Journal of the American Medical Association
Growth hormone-releasing hormone in HIV-infected men with lipodystrophy - A randomized controlled trial
Koutkia, P; Canavan, B; Breu, J; Torriani, M; Kissko, J; Grinspoon, S
Jama-Journal of the American Medical Association, 292(2): 210-218.

Muscle & Nerve
Oxidative stress, chronic disease, and muscle wasting
Moylan, JS; Reid, MB
Muscle & Nerve, 35(4): 411-429.
Effect of atazanavir and ritonavir on the differentiation and adipokine secretion of human subcutaneous and omental preadipocytes
Jones, SP; Waitt, C; Sutton, R; Back, DJ; Pirmohamed, M
AIDS, 22(): 1293-1298.

Antiviral Therapy
Adipocyte differentiation, mitochondrial gene expression and fat distribution: differences between zidovudine and tenofovir after 6 months
Boothby, M; McGee, KC; Tomlinson, JW; Gathercole, LL; McTernan, PG; Shojaee-Moradie, F; Umpleby, AM; Nightingale, P; Shahmanesh, M
Antiviral Therapy, 14(8): 1089-1100.
Journal of Drugs in Dermatology
Monophasic, Cohesive-polydensified-matrix Crosslinking-technology-based Hyaluronic Acid Filler for the Treatment of Facial Lipoatrophy in HIV-infected Patients
Pavicic, T; Ruzicka, T; Korting, HC; Gauglitz, G
Journal of Drugs in Dermatology, 9(6): 690-695.

Clinical Infectious Diseases
Perirenal fat diameter measured by echography could be an early predictor of lipodystrophy in HIV type 1-infected patients receiving highly active antiretroviral therapy
Asensi, V; Martin-Roces, E; Carton, JA; Collazos, J; Maradona, JA; Alonso, A; Medina, M; Aburto, JM; Martinez, E; Rojo, C; Bustillo, E; Fernandez, C; Arribas, JM
Clinical Infectious Diseases, 39(2): 240-247.

Clinical Infectious Diseases
CD4(+) cell count, viral load, and highly active antiretroviral therapy use are independent predictors of body composition alterations in HIV-infected adults: A longitudinal study
McDermott, AY; Terrin, N; Wanke, C; Skinner, S; Tchetgen, E; Shevitz, AH
Clinical Infectious Diseases, 41(): 1662-1670.

Journal of Clinical Endocrinology & Metabolism
Approach to the human immunodeficiency virus-infected patient with lipodystrophy
Brown, TT
Journal of Clinical Endocrinology & Metabolism, 93(8): 2937-2945.
No effect of rosiglitazone for treatment of HIV-1 lipoatrophy: randomised, double-blind, placebo-controlled trial
Carr, A; Workman, C; Carey, D; Rogers, G; Martin, A; Baker, D; Wand, H; Law, M; Samaras, K; Emery, S; Cooper, DA
Lancet, 363(): 429-438.

New England Journal of Medicine
Medical progress - Cardiovascular risk and body-fat abnormalities in HIV-infected adults
Grinspoon, S; Carr, A
New England Journal of Medicine, 352(1): 48-62.

Journal of Clinical Densitometry
Reproducibility of DXA estimations of body fat in HIV lipodystrophy - Implications for clinical research
Cavalcanti, RB; Cheung, AM; Raboud, J; Walmsley, S
Journal of Clinical Densitometry, 8(3): 293-297.
Antiviral Therapy
Evaluation of the HIV lipodystrophy case definition in a placebo-controlled, 144-week study in antiretroviral-naive adults
Law, M; Puls, R; Cheng, AK; Cooper, DA; Carr, A
Antiviral Therapy, 11(2): 179-186.

Journal of Antimicrobial Chemotherapy
Evolving perspectives on HIV-associated lipodystrophy syndrome: moving from lipodystrophy to non-infectious HIV co-morbidities
Guaraldi, G; Baraboutis, IG
Journal of Antimicrobial Chemotherapy, 64(3): 437-440.
Immunophenotype of HIV plus patients during CD4 cell-monitored treatment interruption: role of the IL-7/IL-7 receptor system
Nemes, E; Lugli, E; Nasi, M; Ferraresi, R; Pinti, M; Bugarini, R; Borghi, V; Prati, F; Esposito, R; Cossarizza, A; Mussini, C
AIDS, 20(): 2021-2032.

AIDS Reviews
Pharmacogenetics of Adverse Effects Due To Antiretroviral Drugs
Vidal, F; Gutierrez, F; Gutierrez, M; Olona, M; Sanchez, V; Mateo, G; Peraire, J; Vilades, C; Veloso, S; Lopez-Dupla, M; Domingo, P
AIDS Reviews, 12(1): 15-30.

Role of mitochondria in HIV lipoatrophy: insight into pathogenesis and potential therapies
McComsey, GA; Walker, UA
Mitochondrion, 4(): 111-118.
Antiretroviral therapy and the prevalence of osteopenia and osteoporosis: a meta-analytic review
Brown, TT; Qaqish, RB
AIDS, 20(): 2165-2174.

AIDS Patient Care and Stds
Assessment of Ultrasound for Use in Detecting Lipoatrophy in HIV-Infected Patients Taking Combination Antiretroviral Therapy
Viskovic, K; Richman, I; Klasnic, K; Hernandez, A; Krolo, I; Rutherford, GW; Romih, V; Begovac, J
AIDS Patient Care and Stds, 23(2): 79-84.
Journal of Infectious Diseases
In vivo, nucleoside reverse-transcriptase inhibitors alter expression of both mitochondrial and lipid metabolism genes in the absence of depletion of mitochondrial DNA
Mallon, PWG; Unemori, P; Sedwell, R; Morey, A; Rafferty, M; Williams, K; Chisholm, D; Samaras, K; Emery, S; Kelleher, A; Cooper, DA; Carr, A
Journal of Infectious Diseases, 191(): 1686-1696.

Nature Clinical Practice Endocrinology & Metabolism
Therapy Insight: body-shape changes and metabolic complications associated with HIV and highly active antiretroviral therapy
Falutz, J
Nature Clinical Practice Endocrinology & Metabolism, 3(9): 651-661.
Diabetes Obesity & Metabolism
Antiretroviral therapy and the human immunodeficiency virus - improved survival but at what cost?
Bradbury, RA; Samaras, K
Diabetes Obesity & Metabolism, 10(6): 441-450.
Transactions of the Royal Society of Tropical Medicine and Hygiene
Weight evolution in HIV-1 infected women in Rwanda after stavudine substitution due to lipoatrophy: comparison of zidovudine with tenofovir/abacavir
van Griensven, J; Zachariah, R; Rasschaert, F; Atte, EF; Reid, T
Transactions of the Royal Society of Tropical Medicine and Hygiene, 103(6): 613-619.
Jornal De Pediatria
Lipodystrophy in children and adolescents with acquired immunodeficiency syndrome and its relationship with the antiretroviral therapy employed
Sarni, ROS; de Souza, FIS; Battistini, TRB; Pitta, TS; Fernandes, AP; Tardini, PC; Fonseca, FLA; dos Santos, VP; Lopez, FA
Jornal De Pediatria, 85(4): 329-334.
Journal of Antimicrobial Chemotherapy
Peripheral and visceral fat changes following a treatment switch to a non-thymidine analogue or a nucleoside-sparing regimen in HIV-infected subjects with peripheral lipoatrophy: results of ACTG A5110
Tebas, P; Zhang, J; Hafner, R; Tashima, K; Shevitz, A; Yarasheski, K; Berzins, B; Owens, S; Forand, J; Evans, S; Murphy, R
Journal of Antimicrobial Chemotherapy, 63(5): 998-1005.
Toxicologic Pathology
The Role of Protease Inhibitors in the Pathogenesis of HIV-Associated Lipodystrophy: Cellular Mechanisms and Clinical Implications
Flint, OP; Noor, MA; Hruz, PW; Hylemon, PB; Yarasheski, K; Kotler, DP; Parker, RA; Bellamine, A
Toxicologic Pathology, 37(1): 65-77.
Clinical and Experimental Immunology
Low plasma level of adiponectin is associated with stavudine treatment and lipodystrophy in HIV-infected patients
Lindegaard, B; Keller, P; Bruunsgaard, H; Gerstoft, J; Pedersen, BK
Clinical and Experimental Immunology, 135(2): 273-279.
HIV Medicine
British HIV Association (BHIVA) guidelines for the treatment of HIV-infected adults with antiretroviral therapy (2005)
Gazzard, B
HIV Medicine, 6(): 1-61.

AIDS Patient Care and Stds
Psychometric properties of a lipodystrophy scale
Lee, D; Patel, P; Sachs, J; Basinger, S; Mathews, WC; Barber, RE
AIDS Patient Care and Stds, 20(1): 30-35.

Tropical Medicine & International Health
Determinants of unplanned antiretroviral treatment interruptions among people living with HIV in Yaounde, Cameroon (EVAL survey, ANRS 12-116)
Marcellin, F; Boyer, S; Protopopescu, C; Dia, A; Ongolo-Zogo, P; Koulla-Shiro, S; Abega, SC; Abe, C; Moatti, JP; Spire, B; Carrieri, MP
Tropical Medicine & International Health, 13(): 1470-1478.
Social Science & Medicine
"When in the body, it makes you look fat and HIV negative": The constitution of antiretroviral therapy in local discourse among youth in Kahe, Tanzania
Ezekiel, MJ; Talle, A; Juma, JM; Klepp, KI
Social Science & Medicine, 68(5): 957-964.
Arquivos Brasileiros De Endocrinologia E Metabologia
Bone mineral density in HIV-infected women taking antiretroviral therapy: a systematic review
de Carvalho, EH; Gelenske, T; Bandeira, F; de Albuquerque, MDPM
Arquivos Brasileiros De Endocrinologia E Metabologia, 54(2): 133-142.

Expert Opinion on Therapeutic Patents
Cardiovascular risk associated with antiretroviral therapy in IV-infected patients
Calza, L; Manfredi, R; Chiodo, F
Expert Opinion on Therapeutic Patents, 16(): 1497-1516.

Expert Opinion on Pharmacotherapy
Strategies in the treatment of HIV-1-associated adipose redistribution syndromes
Gutierrez, MDM; Mateo, G; Domingo, P
Expert Opinion on Pharmacotherapy, 8(): 1871-1884.
HIV Medicine
Early changes in adipokine levels and baseline limb fat may predict HIV lipoatrophy over 2 years following initiation of antiretroviral therapy
Calmy, A; Carey, D; Mallon, PWG; Wand, H; Law, M; Cooper, DA; Carr, A
HIV Medicine, 9(2): 101-110.
New Microbiologica
Bone alterations during HIV infection
De Crignis, E; Cimatti, L; Borderi, M; Gibellini, D; Re, MC
New Microbiologica, 31(2): 155-164.

Clinical Infectious Diseases
HIV-associated lipoatrophy: What are the kinder, gentler agents?
Dube, MP
Clinical Infectious Diseases, 42(2): 281-282.

HIV Clinical Trials
Changes in body fat measured by DEXA in patients taking different formulations of stavudine
Yang, Y; Wilder-Smith, A; Panchalingam, A; Tha, NO; Paton, NI
HIV Clinical Trials, 6(6): 337-343.

HIV Clinical Trials
Stavuldine but not Didanosine as part of HAART contributes to peripheral lipoatrophy: A substudy from the Antiretroviral regimen evaluation study (ARES)
Lowe, SH; Hassink, EAM; van Eck-Smit, BLF; Borleffs, JCC; Lange, JMA; Reiss, P
HIV Clinical Trials, 8(5): 337-344.
HIV Medicine
Lipodystrophy and weight changes: data from the Swiss HIV Cohort Study, 2000-2006
Nguyen, A; Calmy, A; Schiffer, V; Bernasconi, E; Battegay, M; Opravil, M; Evison, JM; Tarr, PE; Schmid, P; Perneger, T; Hirschel, B
HIV Medicine, 9(3): 142-150.
Ultrasound in Medicine and Biology
Comparability of echographic and tomographic assessments of body fat changes related to the hiv associated adipose redistribution syndrome (HARS) in antiretroviral treated patients
Gulizia, R; Vercelli, A; Gervasoni, C; Uglietti, A; Ortu, M; Ferraioli, G; Galli, M; Filice, C
Ultrasound in Medicine and Biology, 34(7): 1043-1048.
Radiologia Medica
Ultrasonographic assessment of lipodystrophy in HIV-1-infected patients
Grima, PF; Chiavaroli, R; Grima, P
Radiologia Medica, 114(1): 141-151.
HIV Medicine
Evolution of bone mineral density in AIDS patients on treatment with zidovudine/lamivudiine plus abacavir or lopinavir/ritonavir
Rivas, P; Gorgolas, M; Garcia-Delgado, R; Diaz-Curie, M; Goyenechea, A; Fernandez-Guerrero, M
HIV Medicine, 9(2): 89-95.
AIDS Patient Care and Stds
Treatment Options for HIV-Associated Central Fat Accumulation
Cofrancesco, J; Freedland, E; McComsey, G
AIDS Patient Care and Stds, 23(1): 5-18.
Collegium Antropologicum
Dyslipidemia and Adherence to the Mediterranean Diet in Croatian HIV-Infected Patients during the First Year of Highly Active Antiretroviral Therapy
Turcinov, D; Stanley, C; Canchola, JA; Rutherford, GW; Novotny, TE; Begovac, J
Collegium Antropologicum, 33(2): 423-430.

Scandinavian Journal of Infectious Diseases
Body composition changes in 308 Norwegian HIV-positive patients
Bergersen, BM; Sandvik, L; Bruun, JN
Scandinavian Journal of Infectious Diseases, 36(3): 186-191.
Journal of Clinical Virology
Mitochondrial DNA depletion in adipose tissue of HIV-infected patients with peripheral lipoatrophy
Buffet, M; Schwarzinger, M; Amellal, B; Gourlain, K; Bui, P; Prevot, M; Deleuze, J; Morini, JP; Gorin, I; Calvez, V; Dupin, N
Journal of Clinical Virology, 33(1): 60-64.
Metabolic syndrome and hyperlipidemia in HIV-positive patients
Behrens, GMN
Herz, 30(6): 458-466.
HIV Medicine
Impact of switching from zidovudine/lamivudine to tenofovir/emtricitabine on lipoatrophy: the RECOMB study
Ribera, E; Larrousse, M; Curran, A; Negredo, E; Clotet, B; Estrada, V; Sanz, J; Berenguer, J; Rubio, R; Pulido, F; Ferrer, P; Alvarez, ML; Arterburn, S; Martinez, E
HIV Medicine, 14(6): 327-336.
Bmc Infectious Diseases
Early loss of bone mineral density is correlated with a gain of fat mass in patients starting a protease inhibitor containing regimen: the prospective Lipotrip study
Bonnet, E; Ruidavets, JB; Genoux, A; Mabile, L; Busato, F; Obadia, M; Prevoteau, F; Marchou, B; Massip, P; Marion-Latard, F; Delpierre, C; Bernard, J; Perret, B
Bmc Infectious Diseases, 13(): -.
ARTN 293
Journal of Nutrition
Sex, Smoking, and Socioeconomic Status Are Associated with Body Composition among Tuberculosis Patients in a Deuterium Dilution Cross-Sectional Study in Mwanza, Tanzania
PrayGod, G; Range, N; Faurholt-Jepsen, D; Jeremiah, K; Faurholt-Jepsen, M; Aabye, MG; Magnussen, P; Changalucha, J; Andersen, AB; Wells, JCK; Friis, H
Journal of Nutrition, 143(5): 735-741.
Journal of Antimicrobial Chemotherapy
Switching to lopinavir/ritonavir with or without abacavir/lamivudine in lipoatrophic patients treated with zidovudine/abacavir/lamivudine
Bernardino, JI; Pulido, F; Martinez, E; Arrizabalaga, J; Domingo, P; Portilla, J; Ocampo, A; Munoz, J; Torres, R; Arribas, JR
Journal of Antimicrobial Chemotherapy, 68(6): 1373-1381.
Zidovudine/lamivudine contributes to insulin resistance within 3 months of starting combination antiretroviral therapy
Blümer, RM; van Vonderen, MG; Sutinen, J; Hassink, E; Ackermans, M; van Agtmael, MA; Yki-Jarvinen, H; Danner, SA; Reiss, P; Sauerwein, HP
AIDS, 22(2): 227-236.
PDF (165) | CrossRef
Considerations on the increase in blood pressure among antiretroviral-naive patients starting HAART
Martínez, E; López Bernaldo de Quirós, JC; Miralles, C; Podzamczer, D
AIDS, 21(3): 384-386.
PDF (322) | CrossRef
Reduction of mitochondrial DNA content and respiratory chain activity occurs in adipocytes within 6–12 months of commencing nucleoside reverse transcriptase inhibitor therapy
Hammond, E; Nolan, D; James, I; Metcalf, C; Mallal, S
AIDS, 18(5): 815-817.

PDF (170)
Growth hormone secretion among HIV infected patients: effects of gender, race and fat distribution
Koutkia, P; Eaton, K; You, SM; Breu, J; Grinspoon, S
AIDS, 20(6): 855-862.
PDF (228) | CrossRef
Lipodystrophy is an independent predictor of hypertriglyceridemia during pregnancy in HIV-infected women
Anzidei, G; Meloni, A; Vimercati, A; Polizzi, C; Nogare, ER; Alberico, S; Ravizza, M; Floridia, M; Guaraldi, G; Tamburrini, E; Tibaldi, C; Bucceri, A
AIDS, 20(6): 944-947.
PDF (411) | CrossRef
Effect of pravastatin on body composition and markers of cardiovascular disease in HIV-infected men—a randomized, placebo-controlled study
Mallon, PW; Miller, J; Kovacic, JC; Kent-Hughes, J; Norris, R; Samaras, K; Feneley, MP; Cooper, DA; Carr, A
AIDS, 20(7): 1003-1010.
PDF (236) | CrossRef
Cardiovascular disease in HIV-positive patients
Kamin, DS; Grinspoon, SK
AIDS, 19(7): 641-652.
PDF (2393) | CrossRef
The role of adipokines in relation to HIV lipodystrophy
Sweeney, LL; Brennan, AM; Mantzoros, CS
AIDS, 21(8): 895-904.
PDF (155) | CrossRef
Baseline HIV RNA and the when to start question: time to stop asking this question?
Mussini, C
AIDS, 20(8): 1197-1198.
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Metabolic outcomes in a randomized trial of nucleoside, nonnucleoside and protease inhibitor-sparing regimens for initial HIV treatment
Haubrich, RH; Riddler, SA; DiRienzo, AG; Komarow, L; Powderly, WG; Klingman, K; Garren, KW; Butcher, DL; Rooney, JF; Haas, DW; Mellors, JW; Havlir, DV; for the AIDS Clinical Trials Group (ACTG) A5142 Study Team,
AIDS, 23(9): 1109-1118.
PDF (384) | CrossRef
Metabolic bone disease in HIV infection
Borderi, M; Gibellini, D; Vescini, F; De Crignis, E; Cimatti, L; Biagetti, C; Tampellini, L; Re, MC
AIDS, 23(11): 1297-1310.
PDF (272) | CrossRef
First line zidovudine/lamivudine/lopinavir/ritonavir leads to greater bone loss compared to nevirapine/lopinavir/ritonavir
van Vonderen, MG; Lips, P; van Agtmael, MA; Hassink, EA; Brinkman, K; Geerlings, SE; Sutinen, J; Ristola, M; Danner, SA; Reiss, P
AIDS, 23(11): 1367-1376.
PDF (212) | CrossRef
Stavudine in antiretroviral therapy: is this the end?
Brinkman, K
AIDS, 23(13): 1727-1729.
PDF (240) | CrossRef
Long-term safety and effects of tesamorelin, a growth hormone-releasing factor analogue, in HIV patients with abdominal fat accumulation
Kotler, D; Somero, M; Berger, D; Brown, S; Richmond, G; Fessel, J; Turner, R; Grinspoon, S; Falutz, J; Allas, S; Mamputu, J; Potvin, D
AIDS, 22(14): 1719-1728.
PDF (298) | CrossRef
Effects of boosted tipranavir and lopinavir on body composition, insulin sensitivity and adipocytokines in antiretroviral-naive adults
Carr, A; Ritzhaupt, A; Zhang, W; Zajdenverg, R; Workman, C; Gatell, JM; Cahn, P; Chaves, R
AIDS, 22(17): 2313-2321.
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Back to Top | Article Outline

HIV; lipodystrophy; highly active antiretroviral therapy; densitometry; X-ray; adipose tissue; metabolic syndrome X

© 2003 Lippincott Williams & Wilkins, Inc.


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