Abstract

Aims

Highly active antiretroviral therapy (HAART) dramatically reduces human immunodeficiency virus (HIV)-associated morbidity and mortality, but adverse effects of HAART are becoming an increasing challenge, especially in the setting of acute coronary syndromes (ACS). We thus performed a comprehensive review of studies focusing on ACS in HIV patients.

Methods and results

MEDLINE/PubMed was systematically screened for studies reporting on ACS in HIV patients. Baseline, treatment, and outcome data were appraised and pooled with random-effect methods computing summary estimates [95% confidence intervals (CIs)]. A total of 11 studies including 2442 patients were identified, with a notably low prevalence of diabetes [10.86 (4.11, 17.60); 95% CI]. Rates of in-hospital death were 8.00% (2.8, 12.5; 95% CI), ascribable to cardiovascular events for 7.90% (2.43, 13.37; 95% CI), with 2.31% (0.60, 4.01; 95% CI) developing cardiogenic shock. At a median follow-up of 25.50 months (11.25, 42; 95% CI), no deaths were recorded, with an incidence of 9.42% of acute myocardial infarction (2.68, 16.17; 95% CI) and of 20.18% (9.84, 30.51; 95% CI) of percutaneous coronary revascularization. Moreover, pooled analysis of the studies reporting incidence of acute myocardial infarction in patients exposed to protease inhibitors showed an overall significant risk of 2.68 (odds ratio 1.89, 3.89; 95% CI).

Conclusion

Human immunodeficiency virus patients admitted for ACS face a substantial short-term risk of death and a significant long-term risk of coronary revascularization and myocardial infarction, especially if receiving protease inhibitors.

See page 813 for the editorial comment on this article (doi:10.1093/eurheartj/ehr413)

Introduction

Antiretroviral therapies dramatically reduced human immunodeficiency virus (HIV)-associated morbidity and mortality.1 Consequently, detrimental effects of both disease progression and antiretroviral therapy are becoming an increasing challenge for physicians managing this high-risk subset of patients.2

In the USA, cardiovascular disease represents the third cause of death or hospitalization for these patients.3 Coronary artery disease is an emerging complication, related both to traditional risk factors and to specific features of these patients. Actually smoking and hypertriglyceridaemia are more common than among non-HIV patients, while both the heightened proinflammatory state and antiretroviral drugs4–8 offer a substrate for the development of premature atherosclerosis and atherothrombosis.9–11

Many studies have provided features and outcomes with acute coronary artery disease in HIV patients, and the influence of antiretroviral therapy in them, providing notable results, often limited by the small number of patients. Especially, some reports demonstrated a higher incidence of acute coronary syndromes (ACS) in patients under treatment with antiretroviral drugs, in particular protease inhibitors.12,13

Thus, a meta-analysis was performed to critically appraise risk factors and outcomes of these patients, and their relationship with antiretroviral drugs.

Methods

The present research was elaborated according to the current guidelines, including the recent Preferred Reporting Items for Systematic reviews and Meta-Analyses (PRISMA) amendment to the Quality of Reporting of Meta-analyses (QUOROM) statement, and recommendations from The Cochrane Collaboration and Meta-analysis Of Observational Studies in Epidemiology (MOOSE).14–17 No language restriction was applied.

Search strategy and study selection

Pertinent articles were searched in Medline, Cochrane Library, Biomed Central, and Google Scholar in keeping with established methods15 with Mesh strategy and with terms related to HIV patients admitted with a diagnosis of ACS: (coronary AND (stent* OR ptca OR angioplasty OR cabg OR (bypass AND (graft* OR surgery)) AND (hiv OR aids OR (human AND immunodeficiency AND virus)). Studies appraising only HIV patients or HIV and non-HIV patients were included.

Two independent reviewers (G.B.-Z. and F.D.) first screened retrieved citations at the title and/or abstract level, with divergences resolved after consensus. If potentially pertinent, they were then appraised as complete reports according to the following explicit selection criteria. Studies were included if investigating HIV patients presenting with ACS, while exclusion criteria were (i) non-human setting, (ii) duplicate reporting (in which case the manuscript reporting the largest sample of patients with HIV was selected), or (iii) HIV patients undergoing cardiac surgical procedure other than for ACS.

Data extraction

Two unblinded independent reviewers (G.B.-Z. and F.D.) abstracted the following data on pre-specified forms: authors, journal, and year of publication, location of the study group, baseline features, death, myocardial infarction, and revascularization. Endpoints of interest were incidence of adverse outcomes and their relationship to antiretroviral therapies. Rates of death, of cardiovascular death, and of cardiogenic shock were appraised. Moreover, at follow-up, rates of myocardial infarction, evaluated according to European Guidelines,16 and of percutaneous coronary revascularization (both repeat revascularization on the target vessel/lesion and on de novo stenosis) were evaluated.

Internal validity and quality appraisal

Unblinded independent reviewers (G.B.-Z. and F.D.) evaluated the quality of included studies on pre-specified forms. Modifying the MOOSE items to take into account the specific features of included studies,17 we separately abstracted and appraised study design, setting, data source, as well as risk of analytical, selection, adjudication, detection, and attrition bias (expressed as low, moderate, or high risk of bias, as well as incomplete reporting leading to inability to ascertain the underlying risk of bias). Moreover, we awarded overall credibility of studies included to summarized previous features. Zero points were assigned for retrospective design and one-centre study, and one for prospective arrangement and for a multicentre setting. Moreover, two points were ascribed for low risk of bias, one for moderate risk, and zero for high risk or unclear. If the sum of these scores was 10, a very high credibility was granted, if it was between 7 and 9 high, between 4 and 6 moderate, between 1 and 3 low, and 0 very low.

Data analysis and synthesis

Continuous variables are reported as mean (standard deviation) or median (range). Categorical variables are expressed as n/N (%). Statistical pooling was performed according to a random-effect model with generic inverse-variance weighting, computing risk estimates with 95% confidence intervals (CIs), using RevMan 5 (The Cochrane Collaboration, The Nordic Cochrane Centre, and Copenhagen, Denmark). A small study bias was appraised by graphical inspection of funnel plots. Standard hypothesis testing was set at the two-tailed 0.05 level.

Results

A total of 236 citations were first screened and appraised at the abstract level; 19 articles were selected, among which 4 were excluded because of investigating also non-coronary cardiac surgery,18–21 three because of including HIV patients undergoing percutaneous coronary intervention also in stable clinical settings, 1,22,23 and 2 because of investigating baseline features of HIV patients.4,24 Finally, 11 studies were included in our review2,12,13,19,25–31 (Figure 1).

Figure 1

Review profile.

Figure 1

Review profile.

The methodological assessment is reported in Table 1, showing an overall good quality of the selected studies, most of them being prospective, half of them multicentre, without a high risk of analysed bias. Moreover, for each study, definitions of adverse events and single follow-up were evaluated (see Supplementary material online, Appendix Table SA).

Table 1

Methodological evaluation and quality appraisal of selected studies

 11 studies (%) 
Region of origin 1 Africa (10%) 
4 Europe (36%) 
5 North America (45%) 
1 worldwide (10%) 
Location of the study 
 One centre 5 (45%) 
 Multicentre 6 (55%) 
Organization of the study 
 Retrospective 4 (30%) 
 Prospective 7 (70%) 
Source of data 
 Clinical database 10 (91%) 
 Organizational database 1 (9%) 
Risk of analytical bias 
 Low 3 (28%) 
 Medium 8 (72%) 
Risk of selection bias 
 Low 7 (72%) 
 Medium 4 (28%) 
Risk of attrition bias 
 Low 6 (54%) 
 Medium 3 (27%) 
 Unclear 2 (28%) 
Risk of adjudication bias 
 Low 1 (10%) 
 Medium 6 (54%) 
 Unclear 4 (36%) 
Overall credibility 
 Low 1 (10%) 
 Medium 5 (45%) 
 High 4 (32%) 
 Very high 1 (10%) 
 11 studies (%) 
Region of origin 1 Africa (10%) 
4 Europe (36%) 
5 North America (45%) 
1 worldwide (10%) 
Location of the study 
 One centre 5 (45%) 
 Multicentre 6 (55%) 
Organization of the study 
 Retrospective 4 (30%) 
 Prospective 7 (70%) 
Source of data 
 Clinical database 10 (91%) 
 Organizational database 1 (9%) 
Risk of analytical bias 
 Low 3 (28%) 
 Medium 8 (72%) 
Risk of selection bias 
 Low 7 (72%) 
 Medium 4 (28%) 
Risk of attrition bias 
 Low 6 (54%) 
 Medium 3 (27%) 
 Unclear 2 (28%) 
Risk of adjudication bias 
 Low 1 (10%) 
 Medium 6 (54%) 
 Unclear 4 (36%) 
Overall credibility 
 Low 1 (10%) 
 Medium 5 (45%) 
 High 4 (32%) 
 Very high 1 (10%) 

A total of 2442 patients were included, showing at pooled analysis an overall average incidence of traditional cardiovascular risk factors, except for diabetes [10.86 (4.11, 17.60); 95% CI] (Table 2).

Table 2

Cardiovascular evaluation

 Pooled analysis (95% CI)a 
Age (years) 61 (58, 64) 
Male gender 80.45 (77.22, 83.69) 
Hypertensive patients 22.29 (14.23, 30.34) 
Dyslipidaemic patients 42.50 (33.35, 51.64) 
Patients with hypertriglyceridaemia 45.03 (23.68, 66.38) 
Diabetic mellitus type 2 patients 10.86 (4.11, 17.60) 
Patients actual or previous smoker 60.30 (56.62, 63.99) 
 Pooled analysis (95% CI)a 
Age (years) 61 (58, 64) 
Male gender 80.45 (77.22, 83.69) 
Hypertensive patients 22.29 (14.23, 30.34) 
Dyslipidaemic patients 42.50 (33.35, 51.64) 
Patients with hypertriglyceridaemia 45.03 (23.68, 66.38) 
Diabetic mellitus type 2 patients 10.86 (4.11, 17.60) 
Patients actual or previous smoker 60.30 (56.62, 63.99) 

aAll data reported as mean or percentages.

Pooled analysis of HIV disease characteristics are reported in Table 3, showing a time from HIV diagnosis to ACS of 7.45 years (2.38, 12.51; 95% CI), with most of the patients exposed to nucleoside reverse-transcriptase inhibitors [84.23% (74.15, 94.3; 95% CI)] and protease inhibitors [66.21% (59.77, 72.65; 95% CI)].

Table 3

Human immunodeficiency virus disease characteristics

 Pooled analysis (95% CI)a 
Time from diagnosis of HIV infection (years) 7.45 (2.38, 12.51) 
Median CD4+ cell count per mm3 382.71 (309.34, 456.09) 
Patients exposed to protease inhibitors (previous and current) 66.21 (59.77, 72.65) 
Duration of therapy (years) 4.01 (0.95, 7.07) 
Patients exposed to non-nucleoside reverse-transcriptase inhibitors (previous and current) 29.81 (8.36, 51.26) 
Patients exposed to nucleoside reverse-transcriptase inhibitors 84.23 (74.15, 94.31) 
 Pooled analysis (95% CI)a 
Time from diagnosis of HIV infection (years) 7.45 (2.38, 12.51) 
Median CD4+ cell count per mm3 382.71 (309.34, 456.09) 
Patients exposed to protease inhibitors (previous and current) 66.21 (59.77, 72.65) 
Duration of therapy (years) 4.01 (0.95, 7.07) 
Patients exposed to non-nucleoside reverse-transcriptase inhibitors (previous and current) 29.81 (8.36, 51.26) 
Patients exposed to nucleoside reverse-transcriptase inhibitors 84.23 (74.15, 94.31) 

aAll data reported as mean or percentages.

At admission, most patients presented with ST-segment elevation myocardial infarction (STEMI) [57.19% (47.64, 66.75; 95% CI)], with one-vessel disease as the most angiographic presentation [52.83% (34.83, 70.83; 95% CI)], and percutaneous transluminal coronary angioplasty as the most exploited revascularization strategy [54.23% (38.97, 69.49; 95% CI)] (Table 4).

Table 4

Acute coronary syndrome presentation, angiographic findings, and revascularization strategies

 Pooled analysis (95% CI)a 
Patients admitted with unstable angina/non-segment elevation myocardial infarction 46.08 (38.13, 54.02) 
Patients admitted with segment elevation myocardial infarction 57.19 (47.64, 66.75) 
Angiographic findings 
 One-vessel disease 52.83 (34.83, 70.83) 
 Multivessel disease 46.27 (36.30, 56.24) 
Percutaneous transluminal coronary angioplasty 54.23 (38.97, 69.49) 
Coronary artery bypass graft 11.80 (4.32, 19.28) 
 Pooled analysis (95% CI)a 
Patients admitted with unstable angina/non-segment elevation myocardial infarction 46.08 (38.13, 54.02) 
Patients admitted with segment elevation myocardial infarction 57.19 (47.64, 66.75) 
Angiographic findings 
 One-vessel disease 52.83 (34.83, 70.83) 
 Multivessel disease 46.27 (36.30, 56.24) 
Percutaneous transluminal coronary angioplasty 54.23 (38.97, 69.49) 
Coronary artery bypass graft 11.80 (4.32, 19.28) 

aAll data reported as mean or percentages.

Rates of in-hospital death (Figure 2) were 8.00% (2.8, 12.5; 95% CI), ascribable to cardiovascular events for 7.90% (2.43, 13.37; 95% CI), with 2.31% (0.60, 4.01; 95% CI) developing cardiogenic shock.

Figure 2

In-hospital and long-term outcomes. *Up to 30 days. **Follow-up of 25.50 (11.25, 42 months, 95% CI).

Figure 2

In-hospital and long-term outcomes. *Up to 30 days. **Follow-up of 25.50 (11.25, 42 months, 95% CI).

At a median follow-up of 25.50 months (11.25, 42; 95% CI), no deaths were recorded, with an incidence of 9.42% of acute myocardial infarction (2.68, 16.17; 95% CI) and of 20.18% (9.84, 30.51; 95% CI) of percutaneous coronary revascularization.

Moreover, pooled analysis of two25,28 studies reporting the incidence of acute myocardial infarction in patients exposed to protease inhibitors showed an overall significant risk of 2.68 (odds ratio 1.89, 3.89; 95% CI).

Discussion

Nowadays, HIV-infected patients live longer owing to more effective antiretroviral therapy. At the same time, while this population becomes older, the cardiovascular risk of morbidity and death increases, and also the prevalence of chronic conditions related to this disease. With our systematic review and meta-analysis, we intended to summarize available data about risk factors, angiographic and clinical presentation at admission, and safety of antiretroviral therapy, reporting the current knowledge about the physiopathology of HIV infection.

The risk of coronary heart disease in HIV patients is influenced both from traditional risk factors and from specific features of this disease. Our meta-analysis shows an overall average incidence of traditional cardiovascular risk factors, except for diabetes, as can be expected in a young population. In contrast, in some studies, cigarette smoking was more prevalent in HIV patients.32 Moreover, lack of data makes it not possible to analyse the burden of illicit drug users, which was reported more frequently among HIV-infected patients and which i's known to confer a higher thrombotic risk.33 Nonetheless, as confirmed in the present work, in various large cohorts, HIV-infected patients showed high percentages of hypertriglyceridaemia, also related to their young age.34,35 Many authors36–38 suggest virus involvement in the atherosclerosis process through direct effects on cholesterol processing and transport, attraction and activation of monocytes at the intimal wall, inducing inflammatory response and endothelial proliferation.

In our meta-analysis, high rates of in-hospital death were recorded, probably because of STEMI being the most common presentation and of frequent occurrence of multivessel. ST-segment elevation myocardial infarction rates were higher than in contemporary ACS registries of non-HIV patients,39,40 and similar differences were found for multivessel involvement. These two factors combined together could easily explain high rates of in-hospital events in HIV patients.41 The peculiar type of coronary disease in HIV patients derived both from cardiovascular risk factors and enhanced from viral pathological process and side effects of antiretroviral drugs could explain such findings.

Furthermore, our report confirms an important risk of non-fatal reinfarction after ACS. This finding could be in part explained considering the young age of the population. Also the prothrombotic state may be involved in the higher incidence of thrombo-embolic events and in-stent thrombosis as reported in some studies.19 The whole mechanisms underlying the disease are probably not completely clear, but again the HIV infection by itself and the antiretroviral therapy associated with chronic inflammation could play a role in the risk of plaque rupture and atherothrombosis.42,43 As reported previously,44,45 HIV infection has a direct toxic effect upon the endothelium and increases interleukin-6 production that is implicated in the pathogenesis of ACS. Moreover, the prothrombotic tendency increases proportionally to the viral load and the CD4 cell count.

No deaths were recorded in the follow-up. This could be due to many reasons. First, HIV patients may benefit from the use of more recent therapies and/or aggressive risk factor modification. Moreover, the present meta-analysis included studies obtained from centres with great experience and expertise in managing patients with HIV and coronary artery disease.

Finally, we observe that most of the patients presenting with coronary artery disease are exposed to protease inhibitors or nucleoside reverse-transcriptase inhibitors. In the pooled analysis, we are able to include only the protease inhibitors therapy, whereas incomplete data about other therapies are available in the selected articles. The metabolic syndrome consisting of lipid abnormalities and insulin resistance induced by the protease inhibitors certainly plays a role as a cofactor promoting the progression of underlying coronary lesions eliciting plaque inflammation and rupture. Anyway, as reported from many authors,46,47 a clear dose–effect relationship has not been found. The better way to manage these patients is addressing the modifiable risk factor, keeping close attention to drug interactions in the presence of a high cardiovascular risk profile.

Limitations

Our work shares several important limitations. First, data about the odds ratio for myocardial infarction after proton-pump inhibitors use derived neither from randomized clinical trial nor from multivariate adjustment, thus being generating hypothesis only, without the aim of inference. Moreover, we appraised infrequent events, with all the limits about reporting uncommon outcomes.47 Secondly, no data were pooled about the influence of nucleoside and non-reverse-transcriptase inhibitors on outcomes, because of the absence in the included original researches, Thirdly, data about illicit drugs used, especially cocaine, were present in only one study,2 and thus, it was not possible to address their influence on outcomes. Furthermore, in the selected articles, data about chemokines receptor CCR5 inhibitors48 (entry inhibitors) therapy were not reported probably because of its recent approval by the Food and Drug Administration.45 These classes of drugs could provide new insights because of the critical role of chemokines and their receptors in the pathology of atherosclerosis. Moreover, no data on cardiac rupture and reperfusion success were obtained, thus limiting the exploration of mechanisms of in-hospital death.

Supplementary material

Supplementary material is available at European Heart Journal online.

Conflict of interest: none declared.

References

1
Boccara
F
Teiger
E
Cohen
A
Ederhy
S
Janower
S
Odi
G
Di Angelantonio
E
Barbarini
G
Barbaro
G
Percutaneous coronary intervention in HIV infected patients: immediate results and long term prognosis
Heart
 , 
2006
, vol. 
92
 (pg. 
543
-
544
)
2
Boccara
F
Mary-Krause
M
Teiger
E
Lang
S
Lim
P
Wahbi
K
Beygui
F
Milleron
O
Gabriel Steg
P
Funck-Brentano
C
Slama
M
Girard
PM
Costagliola
D
Cohen
A
Prognosis of Acute Coronary Syndrome in HIV-infected patients (PACS) Investigators
Acute coronary syndrome in human immunodeficiency virus-infected patients: characteristics and 1 year prognosis
Eur Heart J
 , 
2011
, vol. 
32
 (pg. 
41
-
50
)
3
Palella
FJ
Jr
Baker
RK
Moorman
AC
Chmiel
JS
Wood
KC
Brooks
JT
Holmberg
SD
Mortality in the highly active antiretroviral therapy era: changing causes of death and disease in the HIV outpatient study
J Acquir Immune Defic Syndr
 , 
2006
, vol. 
43
 (pg. 
27
-
34
)
4
Lafeuillade
A
Alessi
MC
Poizot-Martin
I
Boyer-Neumann
C
Zandotti
C
Quilichini
R
Aubert
L
Tamalet
C
Juhan-Vague
I
Gastaut
JA
Endothelial cell dysfunction in HIV infection
J Acquir Immune Defic Syndr
 , 
1992
, vol. 
5
 (pg. 
127
-
131
)
5
Sipsas
N
Sfikakis
PP
Sfikakis
P
Choremi
H
Kordossis
T
Serum concentrations of soluble intercellular adhesionmolecule-1 and progress towards disease in patients infected with HIV
J Infect
 , 
1994
, vol. 
29
 (pg. 
271
-
282
)
6
Feingold
KR
Krauss
RM
Pang
M
Doerrler
W
Jensen
P
Grunfeld
C
The hypertriglyceridemia of acquired immunodeficiency syndrome is associated with an increased prevalence of low density lipoprotein subclass pattern B
J Clin Endocrinol Metab
 , 
1993
, vol. 
76
 (pg. 
1423
-
1427
)
7
Bukrinsky
M
Sviridov
D
Human immunodeficiency virus infection and macrophage cholesterol metabolism
J Leukoc Biol
 , 
2006
, vol. 
80
 (pg. 
1044
-
1051
)
8
Triant
VA
Lee
H
Hadigan
C
Grinspoon
SK
Increased acute myocardial infarction rates and cardiovascular risk factors among patients with human immunodeficiency virus disease
J Clin Endocrinol Metab
 , 
2007
, vol. 
92
 (pg. 
2506
-
2512
)
9
Obel
N
Thomsen
HF
Kronborg
G
Larsen
CS
Hildebrandt
PR
Sorensen
HT
Gerstoft
J
Ischemic heart disease in HIV-infected and HIV-uninfected individuals: a population-based cohort study
Clin Infect Dis
 , 
2007
, vol. 
44
 (pg. 
1625
-
1631
)
10
Saves
M
Chene
G
Ducimetiere
P
Leport
C
Le Moal
G
Amouyel
P
Arveiler
D
Ruidavets
JB
Reynes
J
Bingham
A
Raffi
F
Risk factors for coronary heart disease in patients treated for human immunodeficiency virus infection compared with the general population
Clin Infect Dis
 , 
2003
, vol. 
37
 pg. 
29
 
11
Boccara
F
Ederhy
S
Janower
S
Benyounes
N
Odi
G
Cohen
A
Clinical characteristics and mid-term prognosis of acute coronary syndrome in HIV-infected patients on antiretroviral therapy
HIV Med
 , 
2005
, vol. 
6
 (pg. 
240
-
244
)
12
Mary-Krause
M
Cotte
L
Simon
A
Partisani
M
Costagliola
D
Clinical Epidemiology Group from the French Hospital Database
Increased risk of myocardial infarction with duration of protease inhibitor therapy in HIV-infected men
AIDS
 , 
2003
, vol. 
17
 (pg. 
2479
-
2486
)
13
Matetzky
S
Domingo
M
Kar
S
Noc
M
Shah
PK
Kaul
S
Daar
E
Cercek
B
Acute myocardial infarction in human immunodeficiency virus-infected patients
Arch Intern Med
 , 
2003
, vol. 
163
 (pg. 
457
-
460
)
14
Moher
D
Cook
DJ
Eastwood
S
Olkin
I
Rennie
D
Stroup
DF
Improving the quality of reports of meta-analyses of randomised controlled trials: the QUOROM statement. Quality of Reporting of Meta-analyses
Lancet
 , 
1999
, vol. 
354
 (pg. 
1896
-
1900
)
15
Stroup
DF
Berlin
JA
Morton
SC
Olkin
I
Williamson
GD
Rennie
D
Moher
D
Becker
BJ
Sipe
TA
Thacker
SB
Meta-analysis of observational studies in epidemiology: a proposal for reporting.: Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group
JAMA
 , 
2000
, vol. 
283
 (pg. 
2008
-
2012
)
16
Bertrand
ME
Simoons
ML
Fox
KA
Wallentin
LC
Hamm
CW
McFadden
E
De Feyter
PJ
Specchia
G
Ruzyllo
W
Task Force on the Management of Acute Coronary Syndromes of the European Society of Cardiology
Management of acute coronary syndromes in patients presenting without persistent ST-segment elevation
Eur Heart J
 , 
2002
, vol. 
23
 (pg. 
1809
-
1840
)
17
Higgins
JPT
Green
S
Cochrane Handbook for Systematic Reviews of Interventions Version 5.0.2 [updated September 2009]
 , 
2009
The Cochrane Collaboration
 
18
Blyth
DF
Buckels
NJ
Sewsunker
RR
Khan
S
Mathivha
TM
An experience with cardiopulmonary bypass in HIV-infected patients
Cardiovasc J S Afr
 , 
2006
, vol. 
17
 (pg. 
178
-
185
)
19
Mestres
CA
Chuquiure
JE
Claramonte
X
Muñoz
J
Benito
N
Castro
MA
Pomar
JL
Miró
JM
Long-term results after cardiac surgery in patients infected with the human immunodeficiency virus type-1 (HIV-1)
Eur J Cardiothorac Surg
 , 
2003
, vol. 
23
 (pg. 
1007
-
1016
discussion 1016
20
Jiménez-Expósito
MJ
Mestres
CA
Claramonte
X
Cartañá
R
Josa
M
Pomar
JL
Mulet
J
Miró
JM
En representación del Grupo de Estudio de Endocarditis del Hospital Clínic-IDIBAPS [Mortality and morbidity in HIV-infected patients undergoing coronary artery bypass surgery: a case control study]
Rev Esp Cardiol
 , 
2006
, vol. 
59
 (pg. 
276
-
279
)
21
Trachiotis
GD
Alexander
EP
Benator
D
Gharagozloo
F
Cardiac surgery in patients infected with the human immunodeficiency virus
Ann Thorac Surg
 , 
2003
, vol. 
76
 (pg. 
1114
-
1118
discussion 1118
22
Ren
X
Trilesskaya
M
Kwan
DM
Nguyen
K
Shaw
RE
Hui
PY
Comparison of outcomes using bare metal vs. drug-eluting stents in coronary artery disease patients with and without human immunodeficiency virus infection
Am J Cardiol
 , 
2009
, vol. 
104
 (pg. 
216
-
222
)
23
Segev
A
Cantor
WJ
Strauss
BH
Outcome of percutaneous coronary intervention in HIV-infected patients
Catheter Cardiovasc Interv
 , 
2006
, vol. 
68
 (pg. 
879
-
881
)
24
Hsue
PY
Lo
JC
Franklin
A
Bolger
AF
Martin
JN
Deeks
SG
Waters
DD
Progression of atherosclerosis as assessed by carotid intima–media thickness in patients with HIV infection
Circulation
 , 
2004
, vol. 
109
 (pg. 
1603
-
1608
)
25
Friis-Møller
N
Reiss
P
Sabin
CA
Weber
R
Monforte
A
El-Sadr
W
Thiébaut
R
De Wit
S
Kirk
O
Fontas
E
Law
MG
Phillips
A
Lundgren
JD
DAD Study Group
Class of antiretroviral drugs and the risk of myocardial infarction
N Engl J Med
 , 
2007
, vol. 
356
 (pg. 
1723
-
1735
)
26
Escaut
L
Monsuez
JJ
Chironi
G
Merad
M
Teicher
E
Smadja
D
Simon
A
Vittecoq
D
Coronary artery disease in HIV infected patients
Intensive Care Med
 , 
2003
, vol. 
29
 (pg. 
969
-
973
)
27
Becker
AC
Sliwa
K
Stewart
S
Libhaber
E
Essop
AR
Zambakides
CA
Essop
MR
Acute coronary syndromes in treatment-naïve black South Africans with human immunodeficiency virus infection
J Interv Cardiol
 , 
2010
, vol. 
23
 (pg. 
70
-
77
)
28
Holmberg
SD
Moorman
AC
Williamson
JM
Tong
TC
Ward
DJ
Wood
KC
Greenberg
AE
Janssen
RS
HIV Outpatient Study (HOPS) Investigators
Protease inhibitors and cardiovascular outcomes in patients with HIV-1
Lancet
 , 
2002
, vol. 
360
 (pg. 
1747
-
1748
)
29
Ambrose
JA
Gould
RB
Kurian
DC
DeVoe
MC
Pearlstein
NB
Coppola
JT
Siegal
FP
Frequency of and outcome of acute coronary syndromes in patients with human immunodeficiency virus infection
Am J Cardiol
 , 
2003
, vol. 
92
 (pg. 
301
-
303
)
30
Varriale
P
Saravi
G
Hernandez
E
Carbon
F
Acute myocardial infarction in patients infected with human immunodeficiency virus
Am Heart J
 , 
2004
, vol. 
147
 (pg. 
55
-
59
)
32
Hsue
PY
Giri
K
Erickson
S
MacGregor
JS
Younes
N
Shergill
A
Waters
DD
Clinical features of acute coronary syndromes in patients with human immunodeficiency virus infection
Circulation
 , 
2004
, vol. 
109
 (pg. 
316
-
319
)
33
Aboulafia
DM
Mitsuyasu
RT
Hematologic abnormalities in AIDS
Hematol Oncol Clin North Am
 , 
1991
, vol. 
5
 (pg. 
195
-
214
)
34
Savès
M
Chêne
G
Ducimetière
P
Leport
C
Le Moal
G
Amouyel
P
Arveiler
D
Ruidavets
JB
Reynes
J
Bingham
A
Raffi
F
French WHO MONICA Project and the APROCO (ANRS EP11) Study Group
French WHO MONICA Project and the APROCO (ANRS EP11) Study Group. Risk factors for coronary heart disease in patients treated for human immunodeficiency virus infection compared with the general population
Clin Infect Dis
 , 
2003
, vol. 
37
 (pg. 
292
-
298
)
35
Kaplan
RC
Kingsley
LA
Sharrett
AR
Li
X
Lazar
J
Tien
PC
Mack
WJ
Cohen
MH
Jacobson
L
Gange
SJ
Ten-year predicted coronary heart disease risk in HIV-infected men and women
Clin Infect Dis
 , 
2007
, vol. 
45
 (pg. 
1074
-
1081
)
36
Riddler
SA
Smit
E
Cole
SR
Li
R
Chmiel
JS
Dobs
A
Palella
F
Visscher
B
Evans
R
Kingsley
LA
Impact of HIV infection and HAART on serum lipids in men
JAMA
 , 
2003
, vol. 
289
 (pg. 
2978
-
2982
)
37
Shahmanesh
M
Das
S
Stolinski
M
Shojaee-Moradie
F
Jackson
NC
Jefferson
W
Cramb
R
Nightingale
P
Umpleby
AM
Antiretroviral treatment reduces very-low-density lipoprotein and intermediate-density lipoprotein apolipoprotein B fractional catabolic rate in human immunodeficiency virus-infected patients with mild dyslipidemia
J Clin Endocrinol Metab
 , 
2005
, vol. 
90
 (pg. 
755
-
760
)
38
Mujawar
Z
Rose
H
Morrow
MP
Pushkarsky
T
Dubrovsky
L
Mukhamedova
N
Fu
Y
Dart
A
Orenstein
JM
Bobryshev
YV
Bukrinsky
M
Sviridov
D
Human immunodeficiency virus impairs reverse cholesterol transport from macrophages
PLoS Biol
 , 
2006
, vol. 
4
 pg. 
e365
 
39
Gale
CP
Manda
SO
Weston
CF
Birkhead
JS
Batin
PD
Hall
AS
Evaluation of risk scores for risk stratification of acute coronary syndromes in the Myocardial Infarction National Audit Project (MINAP) database
Heart
 , 
2009
, vol. 
95
 (pg. 
221
-
227
)
40
Ang
DS
Wei
L
Kao
MP
Lang
CC
Struthers
AD
A comparison between B-type natriuretic peptide, global registry of acute coronary events (GRACE) score and their combination in ACS risk stratification
Heart
 , 
2009
, vol. 
95
 (pg. 
1836
-
1842
)
41
Jolly
SS
Shenkman
H
Brieger
D
Fox
KA
Yan
AT
Eagle
KA
Steg
PG
Lim
KD
Quill
A
Goodman
SG
GRACE Investigators
Quantitative troponin and death, cardiogenic shock, cardiac arrest and new heart failure in patients with non-ST-segment elevation acute coronary syndromes (NSTE ACS): insights from the Global Registry of Acute Coronary
Heart
 , 
2011
, vol. 
97
 (pg. 
197
-
202
)
42
El-Sadr
WM
Lundgren
JD
Neaton
JD
Gordin
F
Abrams
D
Arduino
RC
Babiker
A
Burman
W
Clumeck
N
Cohen
CJ
Cohn
D
Cooper
D
Darbyshire
J
Emery
S
Fatkenheuer
G
Gazzard
B
Grund
B
Hoy
J
Klingman
K
Losso
M
Markowitz
N
Neuhaus
J
Phillips
A
Rappoport
C
CD4+ count-guided interruption of antiretroviral treatment
N Engl J Med
 , 
2006
, vol. 
355
 (pg. 
2283
-
2296
)
43
Oliviero
U
Bonadies
G
Apuzzi
V
Foggia
M
Bosso
G
Nappa
S
Valvano
A
Leonardi
E
Borgia
G
Castello
G
Napoli
R
Sacca
L
Human immunodeficiency virus per se exerts atherogenic effects
Atherosclerosis
 , 
2009
, vol. 
204
 (pg. 
586
-
589
)
44
Karmochkine
M
Ankri
A
Calvez
V
Bonmarchant
M
Coutellier
A
Herson
S
Plasma hypercoagulability is correlated to plasma HIV load [letter]
Thromb Haemost
 , 
1998
, vol. 
80
 (pg. 
208
-
209
)
45
Birx
DL
Redfield
RR
Tencer
K
Fowler
A
Burke
DS
Tosato
G
Induction of interleukin-6 during human immunodeficiency virus infection
Blood
 , 
1990
, vol. 
76
 (pg. 
2303
-
2310
)
46
Boue
F
Wallon
C
Goujard
C
Barre-Sinoussi
F
Galanaud
P
Delfraissy
JF
HIV induces IL-6 production by human B lymphocytes: role of IL-4
J Immunol
 , 
1992
, vol. 
148
 (pg. 
3761
-
3767
)
47
Klein
D
Hurley
L
Sorel
M
Sidney
S
Do protease inhibitors increase the risk for coronary heart disease in patients with HIV1 infection
J AIDS
 , 
2002
, vol. 
30
 (pg. 
471
-
477
)
48
Jones
K
Maguire
J
Davenport
A
Chemokine receptor CCR5: from AIDS to atherosclerosis
Br J Pharmacol
 , 
2011
, vol. 
162
 (pg. 
1453
-
1469
)

Supplementary data

Comments

0 Comments