Radionuclide imaging of inflammation in atherosclerotic vascular disease among people living with HIV infection: current practice and future perspective

European Journal of Hybrid Imaging - Tập 3 - Trang 1-16 - 2019
Ismaheel O. Lawal1, Alfred O. Ankrah1,2, Anton C. Stoltz3, Mike M. Sathekge1
1Department of Nuclear Medicine, University of Pretoria & Steve Biko Academic Hospital, Pretoria, South Africa
2Department of Nuclear Medicine and Molecular Imaging, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands
3Infectious Disease Unit, Department of Internal Medicine, University of Pretoria & Steve Biko Academic Hospital, Pretoria, South Africa

Tóm tắt

People living with human immunodeficiency virus (HIV) infection have twice the risk of atherosclerotic vascular disease compared with non-infected individuals. Inflammation plays a critical role in the development and progression of atherosclerotic vascular disease. Therapies targeting inflammation irrespective of serum lipid levels have been shown to be effective in preventing the occurrence of CVD. Radionuclide imaging is a viable method for evaluating arterial inflammation. This evaluation is useful in quantifying CVD risk and for assessing the effectiveness of anti-inflammatory treatment. The most tested radionuclide method for quantifying arterial inflammation among people living with HIV infection has been with F-18 FDG PET/CT. The level of arterial uptake of F-18 FDG correlates with vascular inflammation and with the risk of development and progression of atherosclerotic disease. Several limitations exist to the use of F-18 FDG for PET quantification of arterial inflammation. Many targets expressed on macrophage, a significant player in arterial inflammation, have the potential for use in evaluating arterial inflammation among people living with HIV infection. The review describes the clinical utility of F-18 FDG PET/CT in assessing arterial inflammation as a risk for atherosclerotic disease among people living with HIV infection. It also outlines potential newer probes that may quantify arterial inflammation in the HIV-infected population by targeting different proteins expressed on macrophages.

Tài liệu tham khảo

Abdelbaky A, Corsini E, Figueroa AL, Fontanez S, Subramanian S, Ferencik M et al (2013) Focal arterial inflammation precedes subsequent calcification in the same location: a longitudinal FDG-PET/CT study. Circ Cardiovasc Imaging 6:747–754 Aukrust P, Bjornsen S, Lunden B (2000) Persistently elevated levels of von Willebrand factor antigen in HIV infection. Downregulation during highly active antiretroviral therapy. J Thromb Haemost 84:183–187 Bernasconi E, Uhr M, Magenta L, Ranno A, Telenti A (2001) Homocysteinemia in HIV-infected patients treated with highly active antiretroviral therapy. AIDS. 15:1081–1082 Bleul CC, Wu L, Hoxie JA, Springer TA, Mackay CR (1997) The HIV coreceptors CXCR4 and CCR5 are differentially expressed and regulated on T lymphocytes. Proc Natl Acad Sci U S A 94:1925–1930 Bucerius J, Dijkgraaf I, Mottaghy FM, Schurgers LJ (2018) Target identification for the diagnosis and intervention of vulnerable atherosclerotic plaques beyond 18F-fluorodeoxyglucose positron emission tomography imaging: promising tracers on the horizon. Eur J Nucl Med Mol Imaging. Epub ahead of print on 09 October Bucerius J, Hyafil F, Verberne HJ, Slart RHJA, Linder O, Sciagra R et al (2016) Position paper of the Cardiovascular Committee of the European Association of nuclear medicine (EANM) on PET imaging of atherosclerosis. Eur J Nucl Med Mol Imaging 43:780–792 Bucerius J, Mani V, Moncrieff C, Machac J, Fuster V, Farkouh ME et al (2014) Optimizing 18F-FDG PET/CT imaging of vessel wall inflammation: the impact of 18F-FDG circulation time, injected dose, uptake parameters, and fasting blood glucose levels. Eur J Nucl Med Mol Imaging 41:369–383 Bucerius J, Schmaljohann J, Böhm I, Palmedo H, Guhlke S, Tiemann K et al (2008) Feasibility of 18F-fluoromethylcholine PET/CT for imaging of vessel wall alterations in humans-first results. Eur J Nucl Med Mol Imaging 35:815–820 Carr A, Samaras K, Burton S, Law M, Freund J, Chisholm DJ et al (1998a) A syndrome of peripheral lipodystrophy, hyperlipidaemia and insulin resistance in patients receiving HIV protease inhibitors. AIDS. 12:F51–F58 Carr A, Samaras K, Chisholm DJ, Cooper DA (1998b) Pathogenesis of HIV-1-protease inhibitor-associated peripheral lipodystrophy, hyperlipidaemia, and insulin resistance. Lancet. 351:1881–1883 Chow FC, Regan S, Zanni MV, Looby SE, Bushnell CD, Meigs JB et al (2018) Elevated ischemic stroke risk among women living with HIV infection. AIDS. 32:59–67 Cybulsky MI, Gimbrone MA Jr (1991) Endothelial expression of a mononuclear leukocyte adhesion molecule during atherogenesis. Science. 251:788–791 Cybulsky MI, Iiyama K, Li H, Zhu S, Chen M, Iiyama M et al (2001) A major role for VCAM-1, but not ICAM-1, in early atherosclerosis. J Clin Invest 107:1255–1262 D:A:D Study Group (2003) Combination Antiretroviral Therapy and the Risk of Myocardial Infarction. N Engl J Med 349:1993–2003 D:A:D Study Group (2008) Use of nucleoside reverse transcriptase inhibitors and risk of myocardial infarction in HIV-infected patients enrolled in the D:A:D study: a multi-cohort collaboration. Lancet 371:1417–1426 Derlin T, Habermann CR, Lengyel Z, Busch JD, Wisotzki C, Mester J et al (2011) Feasibility of 11C-acetate PET/CT for imaging of fatty acid synthesis in the atherosclerotic vessel wall. J Nucl Med 52:1848–1854 Duprez DA, Neuhaus J, Kuller LH, Tracy R, Belloso W, De Wit S et al (2012) Inflammation, coagulation and cardiovascular disease in HIV-infected individuals. PLoS One 7:e44454. https://doi.org/10.1371/journal.pone.0044454 Durand M, Sheehy O, Bril JG, Lelorier J, Tremblay C (2011) Association between HIV infection, antiretroviral therapy, and risk of acute myocardial infarction: a cohort and nested case-control study using Quebec’s public health insurance database. JAIDS. 57:245–253 Ecker J, Liebisch G, Englmaier M, Grandl M, Robenek H, Schmitz G (2010) Induction of fatty acid synthesis is a key requirement for phagocytic differentiation of human monocyte. Proc Natl Acad Sci U S A 107:7812–7822 Fan J, Watanabe T (2013) Inflammatory reactions in the pathogenesis of atherosclerosis. J Atheroscler Thromb 10:63–71 Feng Y, Broder CC, Kennedy PE, Berger EA (1996) HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor. Science. 272:872–877 Figueroa AL, Abdelbaky A, Truong QA, Corsini E, MacNabb MH, Lavender ZR et al (2013) Measurement of arterial activity on routine FDG PET/CT images improves prediction of risk of future CV event. JACC Cardiovasc Imaging 6:1250–1259 Flinn WR, McDananiel MD, Yao JS (1984) Antithrombin III deficiency as a reflection of dynamic protein metabolism in patients undergoing vascular reconstruction. J Vasc Surg 1:888–895 Freiberg MS, Chang CH, Kuller LH, Skanderson M, Lowy E, Kraemer KL et al (2013) HIV infection and the risk of acute myocardial infarction. JAMA Intern Med 173:614–622 Gao X, Qian P, Cen D, Hong W, Peng Q, Xue M (2018) Synthesis of phosphatidylcholine in rats with oleic acid-induced pulmonary edema and effects of exogeneous pulmonary surfactant on its de novo synthesis. PLoS One 13:e0193719 Glass TR, Ungsedhapand C, Wolbers M, Weber R, Vernazza PL, Rickenbach M et al (2006) Prevalence of risk factors for cardiovascular disease in HIV-infected patients over time: the Swiss HIV cohort study. HIV Med. 7:404–410 Graebe M, Pedersen SF, Borgwardt L, Højgaard L, Sillesen H, Kjaer A (2009) Molecular pathology in vulnerable carotid plaques: correlation with [18]-fluorodeoxyglucose positron emission tomography (FDG-PET). Eur J Vasc Endovasc Surg 37:714–721 Gupta SK, Pillarisetti K, Lysko PG (1999) Modulation of CXCR4 expression and SDF-1alpha functional activity during differentiation of human monocytes and macrophages. J Leukoc Biol 66:135–143 Hellberg S, Liljenbäck H, Eskola O, Morisson-Iveson V, Morrison M, Trigg W et al (2018) Positron emission tomography imaging of macrophages in atherosclerosis with 18F-GE-180, a radiotracer for translocator protein (TSPO). Contrast Media Mol Imaging. https://doi.org/10.1155/2018/9186902 Hsue PY, Ribaudo HJ, Deeks SG, Bell T, Ridker PM, Fichtebaum C et al (2018) Safety and impact of low-dose methotrexate on endothelial function and inflammation in individuals with treated human immunodeficiency virus: AIDS clinical trial group study A5314. Clin Infect Dis. Epub ahead of print on 14 September Hui DY (2003) Effects of HIV protease inhibitor therapy on lipid metabolism. Prog Lipid Res 42:81–92 Hyafil F, Pelisek J, Laitinen I, Schottelius M, Mohring M, Döring Y et al (2017) Imaging the cytokine receptor CXCR4 in atherosclerotic plaques with the radiotracer 68Ga-Pentixafor for PET. J Nucl Med 58:499–506 Hyle EP, Mayosi BM, Middlekoop K, Mosepele M, Martey EB, Walensky RP et al (2017) The association between HIV and atherosclerotic cardiovascular disease in sub-Saharan Africa. A systematic review. BMC Public Health 17:954 Insull W Jr, Bartsch GE (1966) Cholesterol, triglyceride, and phospholipid content of intima, media, and atherosclerotic fatty streak in human thoracic aorta. J Clin Invest 45:513–523 Kato K, Schober O, Ikeda M, Schäfers M, Ishigaki T, Kies P et al (2009) Evaluation and comparison of 11C-choline and calcification in aortic and common carotid arterial walls with combined PET/CT. Eur J Nucl Med Mol Imaging 36:1622–1628 Knudsen A, Hag AMF, Loft A, von Benzon E, Keller SH, Møller HJ et al (2015) HIV infection and arterial inflammation assessed by 18F-fluorodeoxyglucose (FDG) positron emission tomography (PET): a prospective cross-sectional study. J Nucl Cardiol 22:372–380 Kuller LH, Tracy R, Belloso W, De Wit S, Drummond F, Lane HC et al (2008) Inflammatory and coagulation biomarkers and mortality in patients with HIV infection. PLoS Med 5:e203. https://doi.org/10.1371/journal.pmed.0050203 Lamare F, Hinz R, Gaemperli O, Pugiliese F, Mason JC, Camici PG et al (2011) Detection and quantification of large-vessel inflammation with 11C-(R)-PK11195 PET/CT. J Nucl Med 52:33–39 Lawal I, Sathekge M (2016) F-18 FDG PET/CT imaging of cardiac and vascular inflammation and infection. Br Med Bull 120:55–74 Lawal IO, Ankrah AO, Popoola GO, Lengana T, Sathekge MM (2018) Arterial inflammation in young patients with human immunodeficiency virus infection: a cross-sectional study using F-18 FDG PET/CT. J Nucl Cardiol. Epub ahead of print on 07 February. https://doi.org/10.1007/s12350-018-1207-x Lee HJ, Barback CV, Hoh CK, Qin Z, Kader K, Hall DJ et al (2017) Fluorescence-based molecular imaging of porcine urinary bladder sentinel lymph nodes. J Nucl Med 58:547–553 Lee R, Kim J, Paeng JC, Byun JW, Cheon GJ, Lee DS et al (2018) Measurement of 68Ga-DOTATOC uptake in the thoracic aorta and its correlation with cardiovascular risk. Nucl Med Mol Imaging 52:279–286 Li X, Heber D, Leike T, Beitzke D, Lu X, Zhang X et al (2017) [68Ga]Pentixafor-PET/MRI for the detection of chemokine receptor 4 expression in atherosclerotic plaques. Eur J Nucl Med Mol Imaging. Epub ahead of print on September 21. https://doi.org/10.1007/s00259-017-3831-0 Libby P (2006) Inflammation and cardiovascular disease mechanisms. Am J Clin Nutr 83(suppl):456S–460S Lijfering WM, Ten Kate MK, Sprenger HG, Van der Meer J (2006) Absolute risk of venous and arterial thrombosis in HIV-infected patients and effects of combination anti-retroviral therapy. J Thromb Haemost 4:1928–1930 Liss MA, Stroup SP, Cand ZQ, Hoh C, Hall DJ, Vera DR et al (2014) Robotic-assisted fluorescence sentinel lymph node mapping using multi-nodal image-guidance in an animal model. Urology. 84:982 Lo J, Lu MT, Ihenachor EJ, Wei J, Looby SE, Fitch KV et al (2015) Effects of statin therapy on coronary artery plaque volume and high risk plaque morphology in HIV-infected patients with subclinical atherosclerosis: a randomized double-blind placebo-controlled trial. Lancet HIV 2:e52–e63 Luehmann HP, Pressly ED, Detering L, Wang C, Pierce R, Woodard PK et al (2014) PET/CT imaging of chemokine receptor CCR% in vascular injury model using targeted nanoparticles. J Nucl Med 55:629–634 Majluf-Cruz A, Silva-Estrada M, Sánchez-Barboza R, Montiel-Manzano G, Treviño-Pérez S, Santoscoy-Gómez M et al (2004) Venous thrombosis among patients with AIDS. Clin Appl Thromb Hemost 10:19–25 Malmberg C, Ripa RS, Johnbeck CB, Knigge U, Langer SW, Mortensen J et al (2015) 64Cu-DOTATATE for noninvasive assessment of atherosclerosis in large arteries and its correlation with risk factors: head-to-head comparison with 68Ga-DOTATOC in 60 patients. J Nucl Med 56:1895–1900 Mary-Krause M, Cotte L, Simon A, Partisani M (2003) Costagliola D, and the clinical epidemiology group from the French hospital database. AIDS. 17:2479–2486 Mavroudis CA, Majumder B, Loizides S, Christophides T, Johnson M, Rakhit RD (2013) Coronary artery disease and HIV; getting to the HAART of the matter. Int J Cardiol 167:1143–1153 McMurray HF, Parthasarathy S, Steinberg D (1993) Oxidatively modified low density lipoprotein is a chemoattractant for human T lymphocytes. J Clin Invest 92:1004–1008 Meester EJ, Krenning BJ, de Blois RH, Norenberg JP, de Jong M, Bernsen MR et al (2018) Imaging of atherosclerosis, targeting LFA-1 on inflammatory cells with 111In-DANBIRT. J Nucl Cardiol. Epub ahead of print on 13 March Morlat P, Roussillon C, Henard S, Salmon D, Bonnet F, Cacoub P et al (2014) Causes of death among HIV-infected patients in France in 2010 (national survey): trends since 2000. AIDS. 28:1181–1191 Mosepele M, Molefe-Baikai-Molefe OJ, Grinspoon SK, Triant VA (2018) Benefits and risks of statin therapy in HIV-infected population. Curr Infect Dis Rep 20:20 Musselwhite LW, Sheikh V, Norton TD, Rupert A, Porter BO, Penzak SR et al (2011) Markers of endothelial dysfunction, coagulation and tissue fibrosis independently predict venous thromboembolism in HIV. AIDS. 25:787–795 Obel N, Farkas DK, Kronborg G, Larsen CS, Pedersen G, Riis A et al (2010) Abacavir and risk of myocardial infarction in HIV-infected patients on highly active antiretroviral therapy: a population-based nationwide cohort study. HIV Med 11:130–136 Ridker PM, Everett BM, Thuren T, MacFadyen JG, Chang WH, Ballantyne C et al (2017) Antiinflammatory therapy with Canakinumab for atherosclerotic disease. N Engl J Med 377:1119–1131 Rominger A, Saam T, Wolpers S, Cyran CC, Schmidt M, Foerster S et al (2009) 18F-FDG PET/CT identifies patients at risk for future vascular events in an otherwise asymptomatic cohort with neoplastic disease. J Nucl Med 50:1611–1620 Rudd JHF, Myers KS, Bansilal S, Machac J, Pinto CA, Tong C et al (2008) Atherosclerosis inflammation imaging with 18F-FDG PET: carotid, iliac, and femoral uptake reproducibility, quantification methods, and recommendations. J Nucl Med 49:871–878 Rudd JHF, Warburton EA, Fryer TD, Jones HA, Clark JC, Antoun N et al (2002) Imaging atherosclerotic plaque inflammation with [18F]-Fluorodeoxyglucose positron emission tomography. Circulation. 105:2708–2711 Sene D, Piette JC, Cacoub P (2008) Antiphospholipid antibodies, antiphospholipid syndrome and infections. Autoimmune Rev 7:272–277 Shah ASV, Stelzle D, Lee KK, Beck EJ, Alam S, Clifford S et al (2018) Global burden of atherosclerotic cardiovascular disease in people living with the human immunodeficiency virus: a systematic review and meta-analysis. Circulation. 138:1100–1112 Silvola JMU, Li XG, Virta J, Marjamäki P, Liljenbäck H, Hytönen JP et al (2018) Aluminium fluoride-18 labeled folate enables in vivo detection of atherosclerotic plaque inflammation by positron emission tomography. Sci Rep 8:9720 Subramanian S, Tawakol A, Burdo TH, Abbara S, Wei J, Vijayakumar J et al (2012) Arterial inflammation in patients with HIV. JAMA. 308:379–386 Tarkin JM, Joshi FR, Evans NR, Chowdhury MM, Figg NL, Shah AV et al (2017) Detection of atherosclerotic inflammation by 68Ga-DOTATATE PET compared to [18F]FDG PET imaging. J Am Coll Cardiol 69:1774–1791 Tawakol A, Ishai A, Li D, Pakx RAP, Hur S, Kaiser Y et al (2017) Association of Arterial and Lymph Node Inflammation with distinct inflammatory pathways in human immunodeficiency virus infection. JAMA Cardiol 2:163–171 Tawakol A, Migrino RQ, Bashian GG, Bedri S, Vermylen D, Cury RC et al (2006) In vivo 18F-Fluorodeoxyglucose positron emission tomography imaging provides a noninvasive measure of carotid plaque inflammation in patients. J Am Coll Cardiol 48:1818–1824 UNAIDS (2018) Global HIV & AIDS statistics. Fact sheet. Available on https://www.unaids.org>resources>fact-sheet. Accessed 27 Oct 2018 Vigne J, Thackeray J, Essers J, Makowski M, Varasteh Z, Curaj A et al (2018) Current and emerging preclinical approaches for imaging-based characterization of atherosclerosis. Mol Imaging Biol. Epub ahead of print on 24 September Walenkamp AME, Lapa C, Herrmann K, Wester HJ (2017) CXCR4 ligands: the next big hit? J Nucl Med 58:77S–82S Wei L, Pertryk J, Gaudet C, Kamkar M, Gan W, Duan Y et al (2018) Development of an inflammation imaging tracer, 111In-DOTA-DAPTA, targeting chemokine receptor CCR5 and preliminary evaluation in an ApoE−/− atherosclerosis mouse model. J Nucl Cardiol. Epub ahead of print on 07 February Weinberg D, Thackeray JT, Daum G, Sohns JM, Kropf S, Wester HJ et al (2018) Clinical molecular imaging of chemokine receptor CXCR4 expression in atherosclerotic plaque using 68Ga-Pentixafor PET: correlation with cardiovascular risk factors and calcified plaque burden. J Nucl Med 59:266–272 Xia W, Hilgenbrink AR, Matteson EL, Lockwood MB, Cheng JX, Low PS (2009) A functional folate receptor is induced during macrophage activation and can be used to target drugs to activated macrophages. Blood. 113:438–446 Yamashita T, Kawashima S, Ozaki M, Namiki M, Inoue N, Hirata K et al (2002) Propagermanium reduces atherosclerosis in apolipoprotein E knockout mice via inhibition of macrophage infiltration. Artrioscler Thromb Vasc Biol 22:969–974 Yarasheski KE, Laciny E, Overton ET, Reeds DN, Harrod M, Baldwin S et al (2012) 18FDG PET-CT imaging detects arterial inflammation and early atherosclerosis in HIV-infected adults with cardiovascular disease risk factors. J Inflamm 9:22. https://doi.org/10.1186/1476-9255-9-26 Zanni MV, Toribio M, Robbins GK, Burdo TH, Lu MT, Ishai AE et al (2016) Effects of antiretroviral therapy on immune function and arterial inflammation in treatment-naïve patients with human immunodeficiency virus infection. JAMA Cardiol 1:474–480 Zanni MV, Toribio M, Wilks MQ, Lu MT, Burdo TH, Walker J et al (2017) Application of a novel CD206+ macrophage-specific arterial imaging strategy in HIV-infected individuals. J Infect Dis 215:1264–1269